Taskeng
Taskeng
Taskeng
2007-2016
National tuberculosis prevalence surveys 2007-2016
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iii
Contents
Preface v
Acknowledgements vii
Abbreviations xv
Sudan 217
Thailand 225
Uganda 233
United Republic of Tanzania 241
Viet Nam 249
Zambia 257
Zimbabwe 265
v
Preface
At the time of publication of this book in early 2021, tuberculosis (TB) remains a major cause of ill health and one of the top
causes of death worldwide.
During the period 2000–2015, global and national efforts to reduce the burden of TB disease had the aim of achieving global
TB targets that were set as part of the United Nations (UN) Millennium Development Goals (MDGs), the World Health
Organization’s (WHO) Stop TB Strategy (2006–2015) and the Stop TB Partnership’s Global Plan to Stop TB (2006–2015).
Three targets were set: to halt and reverse TB incidence by 2015; to halve the TB mortality rate by 2015 compared with 1990;
and to halve the prevalence of TB disease by 2015 compared with 1990.
In 2006, WHO established a Global Task Force on TB Impact Measurement, convened by the TB monitoring, evaluation and
strategic information (TME) unit of WHO’s Global Tuberculosis Programme. The Task Force’s aim was to ensure a robust,
rigorous and consensus-based assessment of whether the 2015 TB targets were achieved at global, regional and national
levels. At its second meeting, held in 2007, the Task Force agreed on three strategic areas of work for the period 2007–
2015: strengthening of routine national surveillance systems (notification and vital registration) in all countries; national TB
prevalence surveys in 22 global focus countries; and periodic review of the methods used by WHO to translate surveillance
and survey data into estimates of TB disease burden. The 22 global focus countries were a prioritised subset of 53 countries
considered eligible to implement a national TB prevalence survey: 13 in Africa and 9 in Asia.
Global recognition of the importance of national TB prevalence surveys was reinforced and supported by considerable national
interest in and commitment to implementing such surveys, which had started to grow and intensify in many countries during
the early-mid 2000s.
In 2007, however, the goal of completing a large number of national TB prevalence surveys in a relatively short period of time
was a daunting task. The number of recent national surveys was small, and global and national experience and expertise in
their design, implementation and analysis was scarce. Between 1990 and 2006, only a handful of countries in Asia successfully
completed a national TB prevalence survey. No national survey had been attempted in the WHO African Region since the
1950s, with the sole exception of a survey in Eritrea in 2005 that was limited by the diagnostic methods used to detect people
with TB.
What followed was an unprecedented national, regional and global effort to implement national TB prevalence surveys.
Between 2007 and the end of 2016, 24 countries implemented a total of 25 national surveys using methods recommended by
WHO. The 24 countries comprised 18 of the 22 global focus countries and six other countries. The 25 surveys consisted of 13
in Asia and 12 in Africa.
The outcome is a wealth of new data. These data were crucial to WHO’s assessment of whether the 2015 TB targets were met
at global, regional and country levels, by providing a much better understanding of the burden of TB disease, including its
distribution by age and sex, and reliable evidence about trends in countries where a repeat survey was done. The data have also
provided new evidence about the symptoms experienced by people with undiagnosed TB in the community, the extent of gaps
between the number of people with TB in the community and the number of people officially detected with TB, and health
care-seeking behaviour in the public and private sectors, in turn shining new light on reasons for delays in diagnosing people
with TB and for the underreporting of people diagnosed with TB to national authorities. Collectively, survey findings have
informed the policies, plans and programmatic actions needed to address gaps in TB diagnosis and treatment and to reduce
the burden of TB disease. Finally, the 24 countries have a robust baseline for assessing progress towards new global targets set
in the UN Sustainable Development Goals (2016–2030) and WHO’s End TB Strategy (2016–2035).
vi Preface
At the global level, efforts to support the design, implementation, analysis and reporting of national TB prevalence surveys
between 2007 and 2016 were led and coordinated by a subgroup of the WHO Global Task Force on TB Impact Measurement.
This subgroup was led by staff in WHO’s TME unit.
In 2016, it was our collective view that the methods, results, successes achieved, challenges faced and lessons learned from the
25 national surveys implemented 2007–2016 should be comprehensively documented in a book. We viewed such a product as
a global public good, that should be available to all those with an interest in and commitment to using survey findings, now
and in the future.
As with implementation of the 25 surveys themselves, the book is the result of a major global, regional and national
collaborative and collective effort, with more than 450 contributors from all around the world. We are proud of the final
product, wholeheartedly thank all those who made it possible, and hope that it will be a valuable resource for many people for
many years to come.
March 2021
Acknowledgements
This book represents a global collaborative effort of more than 450 people.
A core team of six people at WHO headquarters conceptualized the book and led and coordinated its production: Katherine
Floyd, Philippe Glaziou, Sayori Kobayashi, Irwin Law, Ikushi Onozaki and Charalambos Sismanidis. This core team was led
by Katherine Floyd.
The core team prepared the five cross-cutting chapters that form Part I of the book. Chapter 1 was prepared by Katherine Floyd,
Philippe Glaziou, Irwin Law and Ikushi Onozaki. Chapter 2 and Chapter 3 were prepared by Irwin Law, with contributions
from Katherine Floyd, Philippe Glaziou, Sayori Kobayashi, Ikushi Onozaki and Marina Tadolini (WHO consultant). Chapter
4 was prepared by Katherine Floyd. Chapter 5 was prepared by Katherine Floyd, Irwin Law and Charalambos Sismanidis, with
contributions from Philippe Glaziou.
The country-specific chapters for the 25 national TB prevalence surveys that were completed 2007–2016, which form Part II
of the book, were prepared by the WHO core team together with key members of the national survey teams and people who
provided technical assistance to these teams. Sayori Kobayashi and Irwin Law produced and checked the final datasets and
reports that were used for each chapter in close collaboration with national survey teams, analysed the data and produced the
standard sets of figures and tables that are featured in each chapter. The text of each chapter was drafted by national survey
teams in collaboration with the WHO core team; all chapters were reviewed and finalized by Katherine Floyd and Irwin Law.
Key contributors from the national survey teams to the preparation of the country-specific chapters were as follows:
• Bangladesh: Vikarunnessa Begum, Mourad Gumusboga, Mohammad Mushtuq Husain, Mahmudur Rahman,
Mohammed Sayeedur Rahman, Ahmad Raihan Sharif.
• Cambodia: Mao Tan Eang.
• China: Zhang Hui, Yanni Sun, Lixia Wang, Xia Yin Yin.
• Democratic People’s Republic of Korea: Nam Ju O, Kamar Rezwan, O Hyang Son.
• Ethiopia: Zeleke Alebachew.
• Gambia: Ifedayo Adetifa.
• Ghana: Zeleke Alebachew, Frank Bonsu.
• Indonesia: Maria Christian, Bintari Dwihardiani, Dina Lolong.
• Kenya: Hillary Kipruto, Enos Okumu Masini, Nkirote Mwirigi, Jane Nabongo, Geoffrey Okallo.
• Lao People’s Democratic Republic: Phonenaly Chittamany, Jacque Sebert.
• Malawi: Rhoda Banda, James Mpungu.
• Mongolia: Tsolmon Boldoo, Yasunori Ichimura, Naranzul Dambaa, Narantuya Jadambaa.
• Myanmar: Thandar Lwin, Norio Yamada, Kiyohiko Izumi.
• Nigeria: Philip Patrobas Dashi.
• Pakistan: Razia Fatima, Mahboob ul haq, Nasir Mahmood, Ejaz Qadeer, Sabira Tahseen, Aashifa Yaqoob.
• Philippines: Bicbic Amarillo, Celina Garfin, Mary Ann Lansang, Leilani Naval, Olivia Sison, Rajendra Yadav.
• Rwanda: Patrick Migambi.
• Sudan: Asrar Mohammed Abdelsalam, Igbal Ahmed Elbasheer, Heba Kamal Hamed Elneel, Mai Mohammed Eltigany.
viii Acknowledgements
The WHO core team is grateful to the government of Japan and the United States Agency for International Development
(USAID) for providing the funding that was necessary to produce the book.
A full list of all contributors organized by country, followed by a list of contributors who provided international technical
assistance organized according to their institutional affiliation, is provided below.
Cambodia
National survey team: Koy Bonamy, Mao Tan Eang*, Chea Manith, Saint Saly, Peou Satha, Tieng Sivanna, Pheng Sok, Keo
Sokonth, Kouet Pichenda.
Technical assistance: Emily Bloss, Sian Floyd, Philippe Glaziou, Yutaka Hoshino, Kunihiko Ito, Hiroko Matsumoto,
Hiroyuki Nishiyama, Kosuke Okada, Ikushi Onozaki, Masaki Ota, Charalampos Sismanidis, Tetsuhito Sugamoto, Sara
Whitehead, Rajendra Yadav, Norio Yamada, Kiyomi Yamamoto, Takashi Yoshiyama.
China
National survey team: Cao Jiping, Chen Mingting, Chen Wei, Chen Yude, Cheng Shiming, Du Xin, Duanmu Hongjin, He
Guangxue, Jiang Shiwen, Jin Shuigao, Li Jun, Li Renzhong, Pan Yuxuan, Qian Yuanfu, Ruan Yunzhou, Shi Hongsheng, Tang
Danlin, Tu Dehua, Wang Lixia*, Wang Shengfen, Wang Xiexiu, Wang Zhongren, Wu Zhenglai, Xia Yinyin, Xu Caihong, Xu
Weiguo, Zhang Hui, Zhang Zongde, Zhao Fengzeng, Zhao Yanlin, Zheng Suhua, Zhou Lin, Zhou Xinhua, Zhu Guilin, Zhu
Lizhen, Zou Jiqian.
Technical assistance: Philippe Glaziou, Ikushi Onozaki, Charalampos Sismanidis.
Ethiopia
National survey team: Almaz Abebe, Mulualem Agonafer, Zeleke Alebachew, Menelik Balcha, Tibebu Biniam, Feleke Dana,
Molla Endale, Gashawtena Fantu, Tedla Fiseha, Amha Kebede*, Eshetu Lema, Shewalem Negash, Fasil Tsegaye, Sale
Workneh.
Technical assistance: Wilfred Nkhoma, Ikushi Onozaki, Peou Satha, Charalampos Sismanidis, Marina Tadolini, Hazim
Timimi.
Gambia
National survey team: Ifedayo Adetifa*, Beatrice dei Alorse, William dei Alorse, Martin Antonio, Adedapo Bashorun, Elina
Cole, Edward Demba, Simon Donkor, Umberto D’Alessandro, David Jeffries, Lindsay Kendall, Ma Ansu Kinteh, Christopher
Linda, Ramatoulie Manne, Kodjovi Mlaga, Catherine Bi Okoi, Semeeh Omoleke.
Technical assistance: Bimbo Fasan, Sian Floyd, Jan van den Hombergh, John Mayanda, Ikushi Onozaki, Charalampos
Sismanidis, Marina Tadolini, Etienne Leroy Terquiem.
Ghana
National survey team: Kwasi Addo*, Robertson Adiei, Sauda Ahmed, Jane Amponsah, Herve Awako, Prince Boni, Frank
Bonsu*, Ellis Owusu Dabo, Francisca Dzata, Raymond Yaw Gockah, John Gyapong, Kwadwo Koram, Nii Nortey Hanson
Nortey, Michael Omari, Augustina Badu Peprah.
Technical assistance: Zeleke Alebachew, Irwin Law, Wilfred Nkhoma, Ikushi Onozaki, Charalampos Sismanidis, Marina
Tadolini.
Indonesia
National survey team: Narendro Arifia, Elisabeth Bernadeth, Retno Kusuma Dewi, M. Bintari Dwihardiani, Darmawati,
Irfan Ediyanto, M.N. Farid, Aziza G. Icksan, Jubaedi, Dina Bisara Lolong*, Lamria Pangaribuan, Pandu Riono, Risnawati
Ainur Rofiq, Safrizal, Ade Yoska Tilla Serihati, Francisca Srioetami, Laura Valeria.
Technical assistance: Philippe Glaziou, Irwin Law, Ikushi Onozaki, Charalampos Sismanidis, Marina Tadolini.
Kenya
National survey team: Janet Agaya, Jeremiah Chakaya, Martin Githiomi, Joel Kangangi, Maureen Kamene Kimenye,
Richard Kiplimo, Hillary Kipruto*, Dickson Kirathe, Bernard Langat, Maurice Maina, Veronica Manduku, Enos Masini,
Brenda Mungai, Rose Mwirigi, Margaret Ndisha, Amos Ndombi, Faith Ngari, James Ng’ang’a, Janice Njoroge, Obadiah
Njuguna, Drusilla Nyaboke, Geoffrey Okallo, Jane Ong’ang’o*, Joseph Sitienei*, Anja Vant’Hoog, Josephine Wahogo.
Technical assistance: Emily Bloss, Martien W. Borgdorff, Kevin Cain, Julia Ershova, Sayori Kobayashi, Irwin Law, Wilfred
Nkhoma, Peou Satha, Marina Tadolini, Hazim Timimi.
* Principal investigator
x Acknowledgements
Malawi
National survey team: Rhoda Banda, Masy Chiocha, Isaiah Dambe, Andrew Dimba, Henry Kanyerere, Damson Kathyola,
Sidon Konyani, Charles Mandambwe, Lameck Mlauzi, James Mpunga*, Alister Munthali*, Suzgo Mzumara, Daniel
Nyangulu, Ishmael Nyasulu, George B. Samuti.
Technical assistance: Julia Ershova, Sian Floyd, Irwin Law, Patrick Moonan, Wilfred Nkhoma, Ikushi Onozaki, Peou Satha.
Mongolia
National survey team: Puntsag Banzragch, Tsolmon Boldoo, Buyankhishig Burneebaatar, Naranzul Dambaa, Narantuya
Jadambaa, Naranbat Nyamadawa, Soe Nyunt-U, Bayasgalan Purev, Tugsdelger Sovd*, Oyuntuya Tumenbayar.
Technical assistance: M. Bintari Dwihardiani, M.N. Farid, Yasunori Ichimura, Satoshi Mitarai, Ikushi Onozaki, Norio
Yamada.
Myanmar
National survey team: Si Thu Aung, Tin Mi Mi Khaing, Thandar Lwin, Tin Tin Mar, Win Maung*, Bo Myint, Hnin
Wai, Lwin Myo, Wint Wint Nyunt, Htar Htar Oo, San San Shein, Htay Lwin, Thandar Thwin, Ti Ti, Moe Zaw, Myo Zaw.
Technical assistance: Eva Nathanson, Kosuke Okada, Ikushi Onozaki, Norio Yamada.
Nigeria
National survey team: Haruna Adamu, Babalola Akin, Awe Ayodele, Osakwe Puis Chijioke, Emmanuel Idigbe, Daniel
Olusoji James, Jose Michael Madu, Chukwueme Nkemdilim, Joshua Obasanya*, Osahon Ogbweiwe, Samuel Ogiri, Moses
Onoh, Philip Patrobas, Abiola Tubi, Gideon Zaphania.
Technical assistance: Julia Ershova, Daniella Cirillo, Eugene McCray, Wilfred Nkhoma, Ikushi Onozaki, Narayan Pendse,
Charalampos Sismanidis.
Pakistan
National survey team: Riaz Ahmed, Mohammad Asif, Razia Fatima*, Zulfiqar Ul Hassan, Abdul Mannan, Aisha Mariam,
Ejaz Qadeer*, Sabir Rehman, Alamdar Hussain Rizvi, Zia Samad, Ghulam Nabi Shaikh, Arshad Shamsi, Sabira Tahseen*.
Technical assistance: Amal Bassili, Nico Kalisvaart, Masja Straetemans, Edine Tiemersma.
Philippines 2007
National survey team: Lena Ablis, Virgil Belen, Gerardo Beltran, Jennifer Chua, Albert Angelo Concepcion, Grace Egos,
Maricar Galipot, Ruffy Guilatco, Joselito Legaspi, Vivian Lofranco, Nellie Mangubat, Onofre Edwin Merilles, Leilani Naval,
Ruth Orillaza-Chi, Ma. Imelda Quelapio*, Nona Rachel Mira, Sistla Radhakrishna, Genesis Ramos, Jesus Sarol, Thelma E.
Tupasi*.
Philippines 2016
National survey team: Marissa Alejandria*, Maria Lourdes Amarillo, Concepcion Ang, Luis Anos, Joseph Adrian
Buensalido, Johanna Patricia Cañal, Jose Rene Cruz, Anjo Benedict Fabellon, Nori Jane Galagar, Anna Marie Celina Garfin*,
Noel Juban, Mary Ann Lansang*, Jacinto Blas Mantaring III, Myrna Mendoza*, Allison Noel, Rodelia Pascua, Sonia Salamat,
Olivia Sison, Aser Sisona.
Technical assistance: M. Bintari Dwihardiani, Julia Ershova, Yasunori Ichimura, Irwin Law, Hiroko Matsumoto, Ikushi
Onozaki, Tetsuhiro Sugamoto, Marina Tadolini.
* Principal investigator
Acknowledgements xi
Rwanda
National survey team: Pauline Basinga*, Michel Gasana*, Louise Kalisa, Elaine Kamanzi, Ndeziki Mashengesho, Patrick
Migambi, Julie Mugabekazi, Calvin Mugabo, Jules Kamugunga Mulinzi, Védaste Ndahindwa, Alaine Umubyeyi Nyaruhirira,
Liliane Umutesi, Claude Bernard Uwizeye*.
Technical assistance: Nico Kalisvaart, Eveline Klinkenberg*, Ikushi Onozaki, Peou Satha.
Sudan
National survey team: Abdelaeem, Sawsan Mustafa Abdalla, Nahid Abdelgader, Ahmed Elhaj Ali, Fatih Alrahaman Ali,
Abdel-rahaman, Asrar Mohammed Abdelsalam, Alfakie, Ayyed Muneam El-Dulaimi, Igbal Ahmed Elbasheer*, Hozifa
Omer Eljak, Heba Kamal Hamed Elneel, Majda Elsayed, Mai Mohammed Eltigany, Sami Abdel Hameed, Hashim Salah
Hamza, Nazar Alnoor Ibrahim, Sumia Yousif Mohammed, Mona Hassen Mustafa, Mustafa, Mohammed Osman, Hasham
Alamin Salem.
Technical assistance: Amal Bassili, Kiyohiko Izumi, Ikushi Onozaki, Sabira Tahseen, Fasil Tsegaye, Norio Yamada.
Thailand
National survey team: Sakchai Chaiamahapurk, Autagorn Chunmathong, Pavasuth Chutjuntaravong, Wilawan Dangsaart,
Ratree Dokkabowt, Ornnipa Iamsamang, Kamonwan Imduang, Sirinapha Jittimanee, Phalin Kamolwat, Wiriya Madasin,
Nuntaporn Meksawasdichai, Sriprapa Nateniyom*, Auyporn Petborisuit, Pattana Pokaew, Hataichanok Pukcharern, Walaya
Sitti, Saijai Smithtikarn, Runjuan Sukkavee, Supaporn Wattanatoan, Narong Wongba.
Technical assistance: Ikushi Onozaki, Norio Yamada.
Uganda
National survey team: Ronald Anguzu, Moses Joloba, Samuel Kasozi, Bruce Kirenga, Harriet Kisembo, Frank Mugabe*,
Kenneth Musisi, Annet Nagudi, Abel Nkolo, Okot Martin Nwang, Elizeus Rutebemberwa*, Rogers Sekibira, Racheal
Tumwebaze, William Worodria.
Technical assistance: Emily Bloss, Julia Ershova, Wilfred Nkhoma, Ikushi Onozaki, Peou Satha, Charalampos Sismanidis,
Marina Tadolini.
Viet Nam
National survey team: Bao Thuyet, Chu Manh Dung, Dinh Ngoc Sy*, Do Trong Nghia, Ha Thuc Van, Nguyen Binh Hoa,
Nguyen Cong Chi, Nguyen Van Cu, Nguyen Van Hung, Nguyen Viet Nhung*, Pham Vuong Khac, Thai Anh Sam, Tran
Ngoc Thach, Vu Ngoc Tuan.
Technical assistance: Martien W. Borgdorff, Frank G.J. Cobelens, Edine Tiemersma, Nico Kalisvaart, Agnes Gebhard,
Marleen Vree.
Zambia
National survey team: Mashina Chomba, Pascalina Chanda-Kapata*, Nathan Kapata*, Patrick Katemangwe, Mazyanga
Mazuba Liwewe, Chitani Mbewe, Mine Metitiri, Sam Msariri, Lutinala Nalomba, William Ngosa, Jane Shawa, Chris Silavwe,
Veronica Sunkuntu, Mathias Tembo.
Technical assistance: Julia Ershova, Nico Kalisvaart, Eveline Klinkenberg, Wilfred Nkhoma, Ikushi Onozaki, Charalampos
Sismanidis.
* Principal investigator
xii Acknowledgements
Zimbabwe
National survey team: Joconiah Chirenda, Patrick Hazangwe, Martin Mapfurira, Eve Marima, Ronnie Matambo, Ellen
Munemo, Junior Mutsvangwa*, Hebert Mutunzi, Dumisani Ndlovu, Mkhokeli Ngwenya, Charles Sandy*, Peter Shiri,
Nicholas Siziba.
Technical assistance: Mourad Gumusboga, Kunihiko Ito, Fasil Tsegaye Kassa, Wilfred Nkhoma, Kosuke Okada, Ikushi
Onozaki, Marina Tadolini, Hazim Timimi, Norio Yamada.
Supranational reference laboratory for TB, San Raffaele Scientific Institute, Milan, Italy
Daniella Cirillo.
* Principal investigator
Acknowledgements xiii
Supranational reference laboratory for TB, Institute of Tropical Medicine, Antwerp, Belgium
Mourad Gumusboga, Armand Van Deun.
Independent consultants
Zeleke Alebachew, Ethiopia; M.N. Farid, Indonesia; Bimbo Fasan, Nigeria; Yasunori Ichimura, Japan; Marina Tadolini, Italy;
Sabira Tahseen, Pakistan; Etienne Leroy Terquiem, France; Fasil Tsegaye, Ethiopia.
xiv
xv
Abbreviations
AFB acid-fast bacilli
BCG Bacille Calmette-Guérin
C&NCD Communicable and Noncommunicable Disease Administration
CAD computer aided detection
CDC Centers for Disease Control and Prevention
CI confidence interval
CXR chest X-ray
DDR direct digital radiography
DOTS directly observed treatment, short course
FATA Federally Administered Tribal Areas
FIND Foundation for Innovative New Diagnostics
FM fluorescence microscopy
GCP good clinical practice
GDMP good data management practices
GFC global focus countries
Global Fund Global Fund to Fight AIDS, Tuberculosis and Malaria
HBC high TB burden country
HEPA high efficiency particulate air
HIV human immunodeficiency virus
IGRA interferon gamma release assay
JATA Japan Anti-Tuberculosis Association
JICA Japanese International Cooperation Agency
k coefficient of between cluster variation
LED light-emitting diode
LJ Löwenstein–Jensen media
LPA line-probe assay
MDG Millennium Development Goal
MDR-TB multidrug-resistant tuberculosis
MGIT mycobacteria growth indicator tube
MMR mass miniature radiography
MoH ministry of health
MRCG Medical Research Council Unit, The Gambia
MTB Mycobacterium tuberculosis
NTM nontuberculous mycobacteria
NTLP National Tuberculosis and Leprosy Program
NTP national tuberculosis programme
NTRL national TB reference laboratory
ODPC Office of Disease Prevention and Control
xvi Abbreviations
P:N prevalence:notification
PIN personal identification number
PNB para-nitrobenzoic acid
PPS probability proportional to size
RIF rifampin
RIT Research Institute of Tuberculosis
SDG Sustainable Development Goal
SOP standard operating procedure
SRL supranational reference laboratory
TB tuberculosis
TBMU TB management unit
UI uncertainty interval
UN United Nations
UNAIDS Joint United Nations Programme on HIV/AIDS
US United States
WHO World Health Organization
ZIMSTAT Zimbabwe National Statistics Agency
ZN Ziehl-Neelsen
1
PART I
Examining chest X-rays in the field during the 2010–2011 national TB prevalance survey of Ethiopia.
Photo credit: Yasunori Ichimura
3
Chapter 1
Introduction
This book is about national surveys of the prevalence of of TB cases compulsory were introduced in these and
tuberculosis (TB) disease that were completed between various other industrializing (and now high-income)
2007 and 2016. During this 10-year period there was an countries. In combination, these national notification
unprecedented national, regional and global effort to and VR systems have allowed the burden of TB disease
implement such surveys. Particular attention was given to (in terms of numbers of cases and deaths each year) to
a group of 22 global focus countries (GFCs) in Asia and be reliably monitored using routine health information
Africa that, in 2007, were selected by the World Health systems for several decades, with a few time series
Organization (WHO) Global Task Force on TB Impact covering a span of more than 100 years (Fig. 1.1).
Measurement (1). The ultimate goal is that all countries can reliably track
Between 2007 and the end of 2016, 24 countries their TB epidemics using national notification and VR
implemented a total of 25 national TB prevalence systems. However, although all countries have national
surveys1 using methods recommended by WHO (2); the notification systems for TB, and report notification data
24 countries comprised 18 of the 22 GFCs, and six other to WHO on an annual basis (4), the number of notified
countries. The book documents the survey methods cases each year is generally not a good proxy for the actual
used, results and their implications, successes achieved, number of new cases. This is due to (1) underreporting,
challenges faced, and lessons learned for future surveys. especially in countries with large private sectors or in
It ends with a discussion of prevalence surveys post-2016. which people with TB seek care in public facilities that
This opening chapter explains the rationale for are not linked to the national TB programme (NTP) and
conducting national TB prevalence surveys; provides a associated reporting systems; and (2) underdiagnosis,
historical overview of where, when and how they were especially in countries where there are geographic or
implemented in the years up to 2007; and describes why financial barriers to seeking health care. In the early
prevalence surveys in 22 GFCs became one of three 2000s, national VR systems of high quality and coverage
strategic areas of work pursued by the WHO Global had not been established in many parts of the world
Task Force on TB Impact Measurement between 2007 (including most countries with a high burden of TB), and
and 2015. It ends with a summary of the 25 national TB there was limited progress between 2000 and 2012 (5).
prevalence surveys that were completed between 2007 In the absence of national notification and VR systems
and 2016, which are the subject of the rest of the book. of high quality and coverage, national population-based
surveys of the prevalence of TB disease provide an
alternative way of measuring the burden of TB disease.
1.1 Why are national TB prevalence surveys Such surveys allow direct measurement of the number of
needed? TB cases in the population at a given point in time, and the
Dr Robert Koch announced that he had discovered distribution of cases by age and sex. Repeat surveys allow
Mycobacterium tuberculosis (M. tuberculosis) as the assessment of trends, and of the impact of interventions
cause of TB on 24 March 1882, an event now marked to reduce the burden of disease in the period since the last
annually as World TB Day (3). At that time, TB was one survey. Other benefits of surveys include documentation
of the leading causes of death in European countries, with of health care seeking behaviour in the public and private
cause-of-death data from national vital registration (VR) sectors; identification of reasons why people with TB were
systems showing mortality rates of over 100 per 100 000 not diagnosed before the survey or officially reported
population per year. National laws that made reporting
1
The country that implemented two surveys was the Philippines.
4 National TB prevalence surveys 2007–2016
Fig. 1.1
Trends in TB incidence (solid line) and TB mortality (dashed line) based on data from national notification and national VR systems,
selected countries
to national authorities (or both); and development or population, respectively). They also showed that most
improvement of strategies and interventions for TB case cases (79%) had not been diagnosed before the survey
finding, diagnosis and treatment. and were in those aged 30 years or over. As a result, a
systematic programme of MMR screening, previously
restricted to those under the age of 30 years, was expanded
1.2 The first wave of national TB prevalence
to cover the whole population. Registration and case-
surveys: 1953–1960 holding systems were also introduced.
The first national TB prevalence surveys were
WHO implemented a series of surveys in 12 African
implemented in the 1950s, in East Asia and Africa (Fig.
countries between 1955 and 1960 (16). Of these, 11 were
1.2).1
national surveys: Basutoland (Lesotho), Bechuanaland
The first survey was implemented in Japan in 1953, (Botswana), Gambia, Ghana, Liberia, Nigeria, Sierra
followed by a repeat survey in 1958 (12-14). These Leone, Swaziland (Eswatini), Tanganyika (United
surveys used mass miniature radiography (MMR) as Republic of Tanzania), Uganda and Zanzibar. A survey
an initial screening tool for pulmonary TB; diagnosis was also implemented in Kenya, excluding Nairobi and
was based on smear microscopy and culture. MMR was the country’s northern province. Survey investigations
developed in 1936, and free-of-charge MMR was one of were based on a technical guide published by WHO
12 interventions for TB control recommended by the first (17), and included tuberculin skin tests, chest X-rays
World Health Assembly in July 1948 (15). Results from and sputum examination by direct microscopy. In five
the first survey in Japan alarmed national authorities by countries, X-ray examination was not possible because
revealing a high prevalence of radiologically active and the necessary equipment was not available. Culture
bacteriologically confirmed cases (3.4% and 0.75% of the examinations were generally done for all smear-positive
1
A full historical listing of all surveys implemented up to 2012 specimens and a random sample of smear-negative
in Asia is provided in Onozaki et al. (2015) (10). For surveys in specimens. The estimated prevalence of bacteriologically
Africa, a listing is provided in WHO (2007) (11).
PART I: An overview of the 25 surveys implemented 2007–2016 5
Fig. 1.2
Countries that implemented a national TB prevalence survey, 1953–1960
confirmed TB was 1.5%, with men (2%) having a higher Elsewhere in the WHO Western Pacific Region,
prevalence than women (0.7%); however, there were national surveys were implemented in China (1979),
proportionally more smear-positive cases in women Malaysia (1970), the Republic of Korea (1965, 1970 and
(0.4%) than in men (0.5%). 1975), Samoa (1975) and Singapore (1975).
Pakistan conducted a survey in 1959, but from the Outside the WHO Western Pacific Region, surveys
available information it is not clear whether this was a were conducted in Bangladesh (1964), Indonesia
national or subnational survey (18). In 1955–1959, India (1979‒1982), Iraq (1970), Libya (1976), Myanmar (1972),
carried out subnational TB prevalence surveys (19). Netherlands (1970), Sri Lanka (1970) and Thailand
(1960‒1964 and 1977). Most of these surveys used MMR
for screening, and sputum and culture examination for
1.3 National TB prevalence surveys in Asia in the
diagnosis.
1960s and 1970s
Several subnational surveys in south India were
In the 1960s and 1970s, 14 countries implemented a total
also implemented under the leadership of the National
of 19 national TB prevalence surveys (Fig. 1.3). Multiple
Tuberculosis Institute in Bangalore from 1961 to 1968
surveys were implemented in Japan (three), the Republic
(20).
of Korea (three) and Thailand (two).1
After surveys in 1953 and 1958, repeat surveys were
implemented in Japan in 1963, 1968 and 1973. These 1.4 The 1980s and 1990s: A period of few
showed a rapid reduction in the number of cases, with national TB prevalence surveys
an annual decline estimated at about 10% per year up to Few national TB prevalence surveys were implemented in
the late 1970s – one of the fastest national declines in TB the 1980s and 1990s; six countries implemented a total of
disease burden ever recorded (Fig. 1.1). 11 surveys (Fig. 1.4).1
1
A full historical listing of all surveys implemented up to 2012 In Asia, the series of surveys at 5-year intervals that
in Asia is provided in Onozaki et al. (2015) (10). For surveys in started in the Republic of Korea in 1965 was continued,
Africa, a listing is provided in WHO (2007) (11).
6 National TB prevalence surveys 2007–2016
Fig. 1.3
Countries that implemented a national TB prevalence survey in the 1960s and 1970s
with a further four surveys completed in 1980, 1985, 1990 • In some countries, increased urbanization
and 1995. The survey in 1995 was the last to be carried and improved living conditions led to reduced
out in the country. The other five countries in Asia that willingness among the general population to
implemented surveys were Bangladesh (1987), China participate in surveys. For example, in the
(1984 and 1990), Pakistan (1987), Philippines (1981 and Republic of Korea, where seven national surveys
1997) and Thailand (1991–1992). were conducted every 5 years from 1965 to 1995,
Reasons for the relatively small number of surveys urban participants progressively increased from
included: 34% (1965) to 74% (1995) of the total, and survey
participation rates declined from 96% (1965) to
• In 1974, WHO recommended that MMR
87% (1995) (22, 23). Similarly, in the five national
should not be used for TB case finding (21). This
surveys in Japan from 1953 to 1973, participation
recommendation affected investments in mobile
declined from 99% to 89% (24).
radiographic equipment, and NTPs prioritized
bacille Calmette-Guérin (BCG) vaccination and the • In a growing number of countries, the quality
diagnosis and treatment of people seeking medical and coverage of routine TB surveillance data
care over systematic screening programmes in the improved. These data provided most if not all of the
general population. information needed to monitor the TB epidemic
and inform TB policy, strategy and planning.
• There were declines in disease burden in countries
that had previously implemented surveys. In
countries such as Japan, the Republic of Korea, 1.5 The early to mid 2000s: Few national TB
Singapore and Sri Lanka, these declines meant that prevalence surveys, but growing interest in
increasingly large sample sizes would be required, them
which were prohibitive for logistical and cost
From 2000 to 2006, six surveys that used a variety of
reasons.
methods were implemented (Table 1.1).
PART I: An overview of the 25 surveys implemented 2007–2016 7
Fig. 1.4
Countries that implemented a national TB prevalence survey in the 1980s and 1990s
Only two of these surveys (China, 2000 and Cambodia, pulmonary TB cases and to successfully treat
2002) used both smear microscopy and culture for diagnostic 85% of these cases by 2000, a target date that was
testing, and achieved a sufficiently high participation rate later reset to 2005 (27). The first indicator became
for results to be nationally representative. The surveys in commonly known as the case detection rate. The
Eritrea (2004) and Indonesia (2004) used smear microscopy numerator was the annual number of new cases of
only (25); the survey in Malaysia (2003) had a very low smear-positive TB notified to national authorities
participation rate in urban areas; and the survey in Thailand in a year, and the denominator was an estimate of
collected sputum samples only from those who reported the incidence of smear-positive TB (i.e. the number
symptoms, owing to delays in reading MMRs. of new cases of smear-positive TB) in the same year.
Recognizing the value of updated guidance and greater • WHO declared TB a global health emergency in
standardization in survey methods, the WHO Regional 1993 (28).
Office for the Western Pacific took the initiative to develop • In 1994, WHO published a framework for
a handbook on national TB prevalence surveys (11); this effective TB control (29). This was subsequently
later became known as the red book. Recommendations branded as the DOTS strategy, which was WHO’s
drew heavily on the 2002 survey in Cambodia. recommended approach to TB control until the end
Although the number of national TB prevalence of 2005.1 The DOTS strategy had five components, 2
surveys implemented during this period was small, there
was growing interest in them. This occurred in the context 1
The DOTS strategy was succeeded by the Stop TB Strategy (30) in 2006
of a series of developments that started in the early to mid (which included an updated version of DOTS as its first component) and
by the End TB Strategy in 2016.
1990s:
2
The five components of the DOTS strategy were; political commitment;
• The World Health Assembly agreed the first-ever diagnosis by quality-assured sputum smear microscopy; standardized
targets for global TB control in 1991 (26). The short-course chemotherapy with direct observation of treatment (DOT);
a regular and uninterrupted supply of high-quality anti-TB drugs; and
targets were to detect 70% of new smear-positive a standardized system for recording and reporting of cases and their
treatment outcomes.
8 National TB prevalence surveys 2007–2016
Table 1.1
National TB prevalence surveys implemented in 2000–2006
Country Year Specific survey characteristics
China 2000 The last national survey to include all age groups (>3 months of age); fluoroscopy used for screening;
smear microscopy and culture used for diagnostic testing.
Cambodia 2002 Screening done using an interview about symptoms and direct CXR with onsite full-size film
development using portable equipment; smear microscopy and culture used for diagnostic testing.
Malaysia 2003 Symptom screening done at home and CXR screening at a health facility; smear microscopy and
culture used for diagnostic testing; survey results were not usable owing to a low participation rate in
urban areas.
Eritrea 2004 Sputum smear specimens taken from all participants but no CXR screening; smear microscopy used
for diagnostic testing (no culture).
Indonesia 2004 Implemented as part of a national health demographic survey. Sputum specimens taken from any
participant reporting a productive cough of any duration; no CXR screening; smear microscopy used
for diagnostic testing (no culture).
Thailand 2006 An interview about symptoms and MMR were used for screening. Survey results were not usable
because sputum samples were not collected from participants who had an abnormal MMR but did not
report symptoms, due to delays in reading MMRs and providing feedback about results.
CXR: chest X-ray; MMR: mass miniature radiography.
and its main aim was to achieve the global targets From 2000 until 2015, national, regional and global
of a 70% case detection rate and an 85% treatment efforts in TB control focused on achievement of the
success rate for smear-positive pulmonary TB targets set by the World Health Assembly, the UN and the
cases. By 2000, almost all WHO Member States Stop TB Partnership.
had adopted the DOTS strategy (31). Up to 2005, the greatest attention was given to the
• In 1999, TB was declared a crisis in the WHO World Health Assembly targets of a 70% case detection
Western Pacific Region. In response, WHO and 85% treatment success rate. There was considerable
established the Stop TB Special Project, which interest in estimates of TB incidence, because it was the
aimed to halve 2000 levels of TB prevalence and denominator of the first target.
mortality by 2010. This was the first time that a After a series of consultations, the first estimates of TB
regional target for TB prevalence had been set (32). incidence produced by WHO for the national, regional
• The United Nations (UN) Millennium and global levels were for 1997 (35). Subsequently, WHO
Development Goals (MDGs) were adopted by published updated estimates annually in its global TB
all UN Member States in 2000 (33). Targets were report. Given that notification data in many countries
defined for each of the eight MDGs. One of the were not a good proxy for TB incidence (owing to
targets under MDG 6 was that the TB incidence underreporting and underdiagnosis), and in the frequent
rate (new cases per 100 000 population per year) absence of other direct measurements of TB disease (e.g.
should be declining by 2015. The MDG framework prevalence surveys or cause-of-death data from national
also included four other TB indicators: prevalence VR systems), these estimates relied heavily on two things:
per 100 000 population, the mortality rate, the case expert opinion about the gap between notifications and
detection rate and the treatment success rate. the true level of TB incidence, and tuberculin survey data.
• In the context of the MDGs, regional targets set in the National authorities, including ministries of health
WHO Western Pacific Region and a resolution passed and their NTPs whose performance in making progress
at a summit of the Group of Eight (G8) countries in towards the World Health Assembly targets was being
Okinawa, Japan, the Stop TB Partnership set global regularly assessed and reported, became increasingly
targets to halve TB prevalence and mortality (per interested in improving the evidence available to inform
100 000 population) by 2015 compared with levels in estimates of TB incidence, in particular through the
1990 (34). This was the first time that a global target implementation of a national TB prevalence survey.
for TB prevalence was set. This interest was reinforced by growing evidence and
PART I: An overview of the 25 surveys implemented 2007–2016 9
consensus that methods used to estimate TB incidence From 2006 to 2015, efforts in TB control at national,
from tuberculin survey data were problematic (36, 37); regional and global levels were focused on achieving the
the inclusion of TB prevalence as an MDG indicator; the three “impact” targets of the Stop TB Strategy.
setting of regional and global targets for reductions in TB In June 2006, WHO established a Global Task Force on
prevalence; and the launch of the Stop TB Strategy. TB Impact Measurement (1). The main aim of the Task
Force was to ensure that assessment of whether the 2015
1.6 The decade 2007–2016: a period of targets were achieved at global, regional and national
unprecedented national, regional and global levels was robust, rigorous and consensus-based (38).
After its first meeting in 2006, which focused on a review
efforts to implement national TB prevalence
of available methods to estimate TB disease burden (39),
surveys
the second meeting in December 2007 was used to discuss
In 2006, the DOTS strategy was succeeded by the Stop and reach agreement on strategic areas of work to be
TB Strategy (30) which, in line with the MDGs, had an pursued by the Task Force between 2008 and 2015. Three
end date of 2015. The new strategy had three targets for strategic areas of work were defined: strengthening of
2015, all of which were related to reductions in TB disease routine surveillance systems (notification and VR) in all
burden. The targets were that TB incidence should be countries; implementing national TB prevalence surveys
falling (in line with the TB target under MDG 6), and that in 22 GFCs; and periodic review of the methods used to
1990 levels of TB prevalence and mortality (per 100 000 translate surveillance and survey data into estimates of
population) should be halved by 2015 (thus incorporating TB disease burden (40).
the targets that had been set by the Stop TB Partnership
The 22 GFCs for national TB prevalence surveys (13 in
for the MDG indicators of prevalence and mortality).
Africa and 9 in Asia) were selected based on four major
Table 1.2
The four groups of criteria used to identify countries in which national surveys of the prevalence of TB disease could be justified in the
period up to 2015
Group of criteria Explanation
Group 1 →
1. Estimated prevalence of smear-positive TB ≥100 • Major contribution to the global burden of TB disease. Sample size small
per 100 000 population and enough to make surveys feasible in terms of cost and logistics.
2. Accounts for ≥1% of the estimated total number • Excludes countries whose contribution to the global burden of TB disease is
of smear-positive TB cases globally and insignificant for the purposes of global and regional assessments of burden and
impact.
3. CDR for smear-positive TB ≤50% or >100% • CDR ≤50% or >100% indicates weak reporting systems and problematic TB
estimates, respectively.
Group 2 →
1. Estimated prevalence of smear-positive TB ≥70 • Less stringent criteria for the TB prevalence rate, but incorporates countries
per 100 000 population and with high HIV prevalence and therefore where there is potential for a rapid
2. Accounts for ≥1% of the estimated total number increase in TB incidence and prevalence rates.
of smear-positive TB cases globally and
3. Estimated HIV prevalence rate in the adult
population (15–49 years) ≥1%
Group 3 →
1. Estimated prevalence of smear-positive TB ≥200 • Less stringent criteria for a country’s contribution to the global burden of TB
per 100 000 population and disease, but incorporates countries with particularly high TB prevalence per
2. Accounts for ≥0.5% of the estimated total 100 000 population.
number of smear-positive TB cases globally
Group 4 →
1. Nationwide survey implemented between 2000 • Prior survey data allow monitoring of trends.
and 2007 or
2. Nationwide survey planned before 2010 • High motivation of NTP to conduct a survey.
CDR: case detection rate; HIV: human immunodeficiency virus; NTP: national TB programme.
When the criteria were applied in December 2007, the sources of data used were WHO (2007) (41), the WHO global TB database and UNAIDS/WHO (2006) (42).
10 National TB prevalence surveys 2007–2016
Table 1.3
The 22 GFCs for TB prevalence surveys selected by the WHO Global Task Force on TB Impact Measurement
Criteria met
(group number as High-burden Data from baseline survey conducted
Region and country defined in Table 1.2) country?a between around 1990 and 2008?
WHO African Region
Ethiopia 1,3 Yes No
Ghana 1,2 No No
Kenya 2,4 Yes No
Malawi 1,2,3,4 No No
Mali 1,2,3,4 No No
Mozambique 1,2,3 Yes No
Nigeria 1,2,3,4 Yes No
Rwanda 1,2,3 No No
Sierra Leone 1,2,3 No No
South Africa 2,3 Yes No
Uganda 1,2,3,4 Yes No
United Republic of Tanzania 1,2,3,4 Yes No
Zambia 2,3 No No
WHO Eastern Mediterranean Region
Pakistan 1,4 Yes Yes (1987)
WHO South-East Asia Region
Bangladesh 4 Yes Yes (2008–2009)
Indonesia 4 Yes Yes (2004)
Myanmar 4 Yes Yes (1994)
Thailand 2,4 Yes Yes (1991, 2006)
WHO Western Pacific Region
Cambodia 2,3 Yes Yes (2002)
China 4 Yes Yes (1990, 2000)
Philippines 4 Yes Yes (1981, 1997, 2007)
Viet Nam 4 Yes Yes (2007)
GFC: global focus country; WHO: World Health Organization.
a
“High burden” refers to the 22 high TB burden countries (HBCs) that were defined by WHO for the period 1998–2015. The 22 HBCs were the countries that ranked first
to 22nd in terms of their estimated number of incident cases of TB per year. In 2015, WHO reviewed and updated the definition and a list of 30 HBCs was defined for the
period 2016–2020.
groups of criteria (Table 1.2) and are shown in Table 1.3 of the estimated number of TB cases in each of the four
(2). WHO regions where routine surveillance systems were
A total of 53 countries met one of the four groups weakest (i.e. the African, Eastern Mediterranean, South-
of criteria shown in Table 1.2. There were two major East Asia and Western Pacific regions).1
reasons for selecting a subset of 22 GFCs. The first was From the beginning of 2008, substantial efforts were
that providing the necessary technical support to all of made to design and implement national TB prevalence
the 53 countries would be challenging if not impossible, surveys, and to analyse and report results. At the global
given the relatively limited expertise at that time in the level, these efforts were led and coordinated under the
design and implementation of prevalence surveys at
both global and country levels. The second was that, in 1
The other two WHO regions – the European Region and the Region
of the Americas – already had relatively strong notification and VR
combination, the GFCs accounted for a substantial share systems.
PART I: An overview of the 25 surveys implemented 2007–2016 11
umbrella of the WHO Global Task Force on TB Impact agencies, financial partners and lead investigators
Measurement, and more specifically by a Task Force involved in surveys implemented in the 1990s and
subgroup on national TB prevalence surveys that was led 2000s, with a total of 50 co-authors;
by WHO staff in the Global Tuberculosis Programme’s • expert reviews of protocols, using a checklist based
TB monitoring and evaluation unit. on guidance provided in the lime book (2);
Examples of key actions, activities and products of the • organization of multicountry workshops hosted by
Task Force subgroup on national TB prevalence surveys countries that had recently launched survey field
included: operations (Ethiopia in October 2010, Cambodia
• sending high-level letters from WHO to the in July 2011 and Ghana in May 2013), to enable a
ministers of health of each GFC, to explain why mixture of support for all countries combined with
the country had been selected as a priority for an opportunity to observe a survey at first hand;
a national TB prevalence survey and to offer • organization of study tours to countries where
guidance and support from the Task Force; surveys were being implemented for countries that
• organization of multicountry workshops for were in the preparation phase; and
protocol development; • coordination and provision of technical assistance
• development of updated guidance on standardized to all countries, with an emphasis on Asia–Asia,
methods for undertaking national TB prevalence Asia–Africa and Africa–Africa (AA) collaboration.
surveys in the form of a handbook, which became This global effort reinforced and supported the
known as the lime book (2). This was used as the considerable interest in and commitment to implementing
foundation of all national TB prevalence surveys a national TB prevalence survey that had been growing
implemented from 2010 to 2016 and was produced and intensifying in many countries during the early
as a major collaborative effort among technical 2000s (including in those outside the list of 22 GFCs).
Fig. 1.5
The 24 countries that implemented a national TB prevalence survey in 2007–2016 and that are the subject of this book
Of the 13 GFCs in Africa, nine completed a survey (blue); all nine GFCs in Asia completed at least one survey (blue). Six other countries
completed a survey but were not GFCs (red).
Fig. 1.6
National surveys of the prevalence of TB disease, 1950–2016
DPR Korea: Democratic People’s Republic of Korea; Lao PDR: Lao People’s Democratic Republic; UR Tanzania: United Republic of Tanzania.
a
The survey listed is the one in Bangladesh in 2015, which is featured in this book. There was also a survey in 2008, but this did not use the screening and diagnostic
algorithm recommended in the lime book and for this reason is not counted in the total of 25 surveys.
6. Public Health England. Historical TB notification data tables to Department of Health and Human Services, CDC; 2018 (https://
end December 2017 (Table no. 1). 2018 (https://www.gov.uk/ www.cdc.gov/nchs/nvss/mortality_historical_data.htm, accessed
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15
Chapter 2
Methods
1
Only one national survey implemented over the period 2007–2016
was not included. This was the 2008 survey in Bangladesh, which
did not use the screening strategy recommended in the lime
book. Instead, sputum samples were taken from all individuals 2
The Philippines used a 10-year-old eligibility threshold for its
considered eligible based on age and residency. 2007 survey.
16 National TB prevalence surveys 2007–2016
Table 2.1
Eligibility criteria to participate in a national TB prevalence survey, 2007‒2016
Age of
eligibility
Country Year (years) Residency criteria
Bangladesh 2015‒2016 ≥15 Lived in the cluster for ≥2 weeks before the census
Cambodia 2010‒2011 ≥15 Lived in the household for ≥2 weeks before the census
China 2010 ≥15 Lived in the household for ≥6 months before the census
DPR Korea 2015‒2016 ≥15 Registered in the living administrative unit for ≥2 weeks before the census
Ethiopia 2010‒2011 ≥15 Permanent residents who stayed in the household for ≥1 night in the 14 days before the
census, and temporary visitors who stayed in the household for ≥14 days before the census
Gambia 2011‒2013 ≥15 Residents who spent ≥1 night in the household in the 4 weeks before the census day;
visitors who arrived in the household ≥4 weeks before the census
Ghana 2013 ≥15 Permanent residents who lived in the household for ≥1 day in the past 14 days, or visitors
who lived in the household for ≥7 days in the past 14 days
Indonesia 2013‒2014 ≥15 Lived in the household for ≥1 month before the census
Kenya 2015‒2016 ≥15 Lived in the selected cluster for ≥30 days before the census
Lao PDR 2010‒2012 ≥15 Slept in the household for 14 days before the census
Malawi 2013‒2014 ≥15 Slept in the household for ≥14 days before the census
Mongolia 2014‒2015 ≥15 Slept in the household for 14 days before the census
Myanmar 2009‒2010 ≥15 Lived in the household for ≥2 weeks before the census
Nigeria 2012 ≥15 Slept in the household for ≥14 days before the census
Pakistan 2010‒2011 ≥15 Slept in the household the night before the census
Philippines 2007 ≥10 No residency criteria
Philippines 2016 ≥15 Lived in the household for ≥2 weeks before the census
Rwanda 2012 ≥15 Lived in the household for ≥1 month before the interview
Sudan 2013‒2014 ≥15 Household members resident in the selected household for the past 6 months, and visitors
who spent ≥3 weeks in the household before the census
Thailand 2012‒2013 ≥15 Permanent residents based on household registration, or temporary residents or
nonresidents who had slept in the household for ≥2 weeks before the census
Uganda 2014‒2015 ≥15 Permanent residents who stayed ≥1 night in the household in the past 2 weeks; temporary
visitors who arrived ≥2 weeks before census
UR Tanzania 2011‒2012 ≥15 Slept in the household for 2 weeks before the census
Viet Nam 2006‒2007 ≥15 Lived in the household for ≥3 months before the census
Zambia 2013‒2014 ≥15 Slept in the household 24 hours before the census
Zimbabwe 2014 ≥15 Permanent residents who had slept ≥1 night in the 14 days before the census; non-
residents who had slept in the household for ≥14 days before the census
DPR Korea, Democratic People’s Republic of Korea; Lao PDR, Lao People’s Democratic Republic; UR Tanzania, United Republic of Tanzania.
2.2 Eligibility criteria surveys), in which all those aged 10 years and above
Eligibility to participate in a national TB prevalence survey were considered eligible. In most surveys, a resident was
was based on two criteria: age and residency (Table 2.1). defined as someone who had lived in the household for
Of the 25 surveys implemented in the period 2007–2016, 1
Diagnosis of TB among children is difficult with the diagnostic tools
24 used the age criterion recommended in the lime book used in prevalence surveys. For example, it is hard for children
(i.e. individuals aged ≥15 years).1 The exception was the to produce sputum samples (especially given the paucibacillary
nature of TB in children) and chest X-rays are not suitable for use
2007 survey in the Philippines (implemented before the in healthy children with a low risk of TB disease. A further problem
publication of WHO guidance on national TB prevalence is the larger sample size needed to estimate the number of cases
among children.
PART I: An overview of the 25 surveys implemented 2007–2016 17
at least 2‒4 weeks at the time of the survey census.1 The in the list of prevalent TB cases). Participants with missing
exceptions were the surveys in Pakistan and Zambia culture or Xpert results (or both) would require use of
(which classified a resident as someone who had slept in other evidence (e.g. smear and chest X-ray results) for
the household the night before the census), and those in them to be defined as a TB case. Instances of misdiagnosis
China (6 months residency), Sudan (6 months residency) or overdiagnosis could arise through data management
and Viet Nam (3 months residency). errors, cross-contamination in the laboratory or false-
positive laboratory results. In particular, participants
with a single positive bacteriological result but no other
2.3 Definition of a prevalent survey TB case
supportive evidence of TB disease required special
In 2007, a prevalent case of TB was defined as follows: attention. For example, survey participants with a single
• a definite case of smear-positive pulmonary TB: at scanty culture-positive result (i.e. <5 or 10 M. tuberculosis
least one specimen acid-fast bacilli (AFB) positive colonies on solid media) or a positive Xpert MTB/RIF
by smear microscopy and culture-positive for M. result from a centrifuged sediment were not categorized
tuberculosis; as prevalent TB cases unless there was chest X-ray
• a probable case of smear-positive pulmonary evidence of TB disease.
TB: at least one specimen AFB positive by smear Once the final list of survey cases was available, two
microscopy and chest X-ray consistent with TB categories were defined for the purposes of analysis and
disease according to the reading by the central presentation of results: smear-positive pulmonary TB
radiology team, and culture-negative or not and bacteriologically confirmed pulmonary TB. Given
available; and the diagnostic technologies currently available and
• a case of smear-negative culture-positive pulmo- the logistics of population-based surveys, prevalence
nary TB: two smear-negative slides and culture- surveys focus on the measurement of active pulmonary
positive for M. tuberculosis. TB disease in adults. Surveys cannot be used to directly
measure the prevalence of extrapulmonary disease in
Prevalent survey cases of smear-positive TB and
adults or the prevalence of TB disease in children.
smear-negative culture-positive TB were both classified
as bacteriologically confirmed TB (1).
In December 2010, WHO endorsed the rapid molecular 2.4 Screening and diagnostic testing strategies
test Xpert®MTB/RIF for the simultaneous diagnosis of The screening and diagnostic testing strategies used
TB and rifampicin-resistant TB (4), and in 2013, WHO in surveys implemented in the period 2007‒2016 are
reviewed its recommended routine case definitions for summarized in Table 2.2.
TB and issued an update (3). In the context of prevalence
surveys documented in this book, bacteriologically
confirmed TB was defined as a positive culture and/or 2.4.1 Screening
positive Xpert MTB/RIF result for M. tuberculosis. Smear Most surveys used two screening tools: an interview about
was not used to define a definite case of TB; rather, it was TB symptoms and chest X-ray. Generally, individuals
used to disaggregate cases according to their smear status. with symptoms that met screening criteria and/or a chest
Smear-positive TB was defined as a bacteriologically X-ray showing any lung shadow or findings suggestive
confirmed case (by culture and/or Xpert MTB/RIF) with of TB were considered eligible for sputum examination.
at least one AFB-positive smear result. Participants that screened negative on both interview and
Careful review of laboratory and chest X-ray results chest X-ray were categorized as not eligible for sputum
by a diagnostic panel, before finalizing the list of survey examination, and were therefore assumed not to have TB.
TB cases, was a standard part of national TB prevalence The main symptom screening criterion was a chronic
surveys. This was done not only to ensure the quality of cough (i.e. ≥2 weeks in most surveys), since this has
survey results, but also for clinical management of those been the primary screening criterion for TB in routine
with positive laboratory results (not all of whom were health services. Nine countries used cough ≥2 weeks as
eventually considered to have TB disease or were included the only symptom screening criterion. The symptom
screening criteria in seven other countries was cough ≥2
1
The aim of residency criteria is to exclude individuals who
weeks or haemoptysis, or both. A few surveys considered
intentionally move into the household in anticipation of receiving individuals to be screen positive if they reported a history
health care from the survey team, thus potentially biasing results.
18 National TB prevalence surveys 2007–2016
Table 2.2
Screening methods used in national TB prevalence surveys, 2007‒2016
Radiography
Country Symptom screening screening Other screening criteria
Bangladesh Scoring system: eligible if the total score was Direct digital Chest X-ray exempted a
≥3 a
Cambodia Cough for ≥2 weeks or haemoptysis (or both) Conventional Chest X-ray exempted
China Cough for ≥2 weeks or haemoptysis of any Conventional Participants with known active pulmonary TB
duration (or both) with normal chest X-ray, and those who were
chest X-ray exempted
DPR Korea Cough for ≥15 days or haemoptysis (or both) Conventional None
Ethiopia Cough for ≥2 weeks Conventional Participants who were exempt from or
declined chest X-ray but met one of the
following criteria: weight loss ≥3 kg in the
past month, night sweats ≥2 weeks, fever ≥2
weeks or contact with a TB patient in the past
year
Gambia Cough for ≥2 weeks, or cough <2 weeks with Direct digital Chest X-ray exempted
≥2 other symptoms, or no cough with ≥3 other
symptoms: chest pain, night sweats, shortness
of breath, loss of appetite, weight loss, fever or
haemoptysis
Ghana Cough for ≥2 weeks Direct digital Chest X-ray exempted
Indonesia Cough for ≥2 weeks or haemoptysis (or both) Direct digital Chest X-ray exempted but had at least one of
the following symptoms: cough, haemoptysis,
fever, chest pain, night sweats, loss of
appetite or shortness of breath
Kenya Cough for ≥2 weeks Direct digital Chest X-ray exempted
Lao PDR Cough for ≥2 weeks within the past month or Conventional None
haemoptysis within the past month (or both)
Malawi Any of the following symptoms for at least 1 Conventional None
week: cough, sputum production, haemoptysis,
chest pain, weight loss, night sweats, fatigue,
fever or shortness of breath
Mongolia Cough for ≥2 weeks Direct digital Chest X-ray exempted
Myanmar Cough for ≥3 weeks or haemoptysis (or both) Conventional Chest X-ray exempted
Nigeria Cough for ≥2 weeks Computed None
radiography
Pakistan Cough for ≥2 weeks, or cough of any duration if Direct digital Participants on TB treatment at the time of
there was no available chest X-ray result the survey
Philippines (2007) N/A b
Conventional None
Philippines (2016) Cough for ≥2 weeks or haemoptysis (or both) Direct digital Chest X-ray exempted
Rwanda Cough of any duration Direct digital Chest X-ray exempted
Sudan Cough for ≥2 weeks Direct digital Chest X-ray exempted or a participant was
currently on TB treatment
Thailand Scoring system: eligible if the total score was Direct digital Chest X-ray exempted c
≥3 c
Uganda Cough for ≥2 weeks Conventional Chest X-ray exempted
UR Tanzania Any of the following symptoms: cough for ≥2 Computed None
weeks, haemoptysis, fever for ≥2 weeks, weight radiography
loss or excessive night sweats
PART I: An overview of the 25 surveys implemented 2007–2016 19
Table 2.2
Continued
Radiography
Country Symptom screening screening Other screening criteria
Viet Nam Productive cough for ≥2 weeks Digital scan Chest X-ray exempted or currently on anti-TB
onsite and treatment or history of TB in preceding 2 years
mass miniature
radiography
(70x70 mm)
Zambia Any one of the following symptoms for ≥2 Direct digital None
weeks: cough, fever or chest pain
Zimbabwe Any one of the following symptoms: cough Direct digital Chest X-ray exempted
of any duration, haemoptysis in the past 12
months or drenching night sweats
DPR Korea, Democratic People’s Republic of Korea; Lao PDR, Lao People’s Democratic Republic; UR Tanzania, United Republic of Tanzania.
a
In Bangladesh, a participant was eligible if their total score was 3 points or more: cough ≥2 weeks (3 points), cough <2 weeks (1 point), haemoptysis in the past month (3
points), weight loss in the past month (1 point), fever ≥1 week in the past month (1 point) and night sweats in the past month (1 point). If the chest X-ray was exempted,
then a clinical score of 1 or 2 classified a participant as symptom-screen positive.
b
In the Philippines, symptom screening was not used as a selection criterion for sputum submission, but an interview about TB symptoms and TB history was done for
participants aged 20 years or more.
c
In Thailand, a participant was eligible if their total score was 3 or more (or ≥1 with chest X-ray exempted): cough for ≥2 weeks (3 points), haemoptysis over the past month
(3 points), cough <2 weeks (2 points), weight loss in the past month (1 point), fever ≥1 week within the past 2 weeks (1 point) and night sweats in the past month (1 point).
of TB, even in the absence of symptoms and chest X-ray A single posterior–anterior (PA) image by radiography
abnormalities. was used for chest X-ray screening in all surveys.2 From
In nine surveys, the sensitivity of symptom screening 2007, there was a transition from conventional to digital
was increased by broadening criteria, including chest X-ray imaging systems. In nine surveys, film images
combinations of cough of any duration, loss of body were developed using an automatic film processor (a
weight, chest pain, night sweats and fever. In the standard practice in surveys before 2007), but other
2007 survey in the Philippines, eligibility for sputum surveys deployed digital X-ray systems. Advantages of
submission was based only on chest X-ray screening. In digital systems included no requirement for removal of
Bangladesh and Thailand, a points-scoring system based chemicals; immediate availability of the images for chest
on reported symptoms was used.1 X-ray reading in the field; more efficient transmission
of images to a central unit; and simpler image archiving
Since professional reading by a radiologist was not
and retrieval. Computer radiography with an imaging
possible in most field sites, reporting of any chest X-ray
plate and image reader was used in the surveys in Nigeria
abnormalities (especially lung abnormalities that were
and the United Republic of Tanzania, whereas direct
consistent with TB) was encouraged in all surveys,
digital radiography (DDR) with a flat panel detector
to increase the sensitivity of screening. In 17 surveys,
subsequently became the standard technology for other
participants who declined chest X-ray investigation or
countries.
were exempt from having a chest X-ray were automatically
eligible for sputum submission; in three countries Depending on the accessibility of cluster sites and
(Ethiopia, Indonesia and Pakistan) this only applied if the available funding, countries selected a variety of chest
participant reported symptoms. X-ray delivery options, including X-ray vans, X-ray
containers loaded on a truck or portable X-ray units, or
combinations of these options.
Computer-aided detection for reading chest X-ray
1
images was tested in the context of national TB prevalence
In Bangladesh and Thailand, a participant with a symptom score of 3
points or more was eligible for sputum submission: a cough of ≥2 weeks surveys. However, as of the end of 2016, their performance
or more (3 points), a cough of less than 2 weeks (1 point), haemoptysis was not considered satisfactory, especially for diagnosis (5).
in the past month (3 points), weight loss in the past month (1 point)
fever of ≥1 week in the past month (1 point) and night sweats in
the past month (1 point). In Thailand, if participants did not have a
chest X-ray, then a score of 1 or more made them eligible for sputum 2
Given the required dose of radiation and the lower quality of images that
submission. are produced, WHO does not recommend either MMR or fluoroscopy.
20 National TB prevalence surveys 2007–2016
Table 2.3
Continued
Smear Primary culture
Country Number of Type Number of Type Xpert MTB/RIF MTB identification test HIV testing Drug susceptibility
samples samples for positive cultures testing
Pakistan 2 (1 onsite, 1 at Direct ZN 1 Direct Ogawa Yes, for PNB, MPB64: all culture- No Yes
central) smear-positive positive specimens, and
specimens LPA or Xpert MTB/RIF
without culture used with smear-positive
confirmation specimens without culture
confirmation.
National TB prevalence surveys 2007–2016
samples were also tested for rifampicin resistance using Xpert MTB/RIF.
Both logistical and statistical issues are relevant when
determining the number and size of clusters to be
culture examination, but culture was used in the repeat sampled. At least 50 clusters are strongly recommended,
surveys in 2009 and in 2014, respectively. In Myanmar, the as a compromise between minimizing sampling design
1994 survey did not include chest X-ray screening but it effects (which requires more and smaller clusters) and
was used in the 2009−2010 survey. In Cambodia, the 2002 reducing logistical constraints (by having fewer clusters).
and 2011 surveys used similar screening and diagnostic All surveys implemented in the period 2007‒2016 had
methods. In the Philippines, the 1997 and 2007 surveys 50 or more clusters (Table 2.4). Cluster sizes of 400‒800
used only chest X-ray for screening. Although the 2016 were generally recommended, because this size makes it
Philippines survey used Xpert MTB/RIF for diagnostic possible to complete chest X-ray screening within 7‒10
confirmation, comparisons with the 2007 survey results days. Most surveys had a cluster size of 500‒900 people,
could still be made because the same culture method apart from those in China (1500 people), Pakistan (1400)
(Ogawa) was used in both surveys. and Viet Nam (1500). The introduction of high-capacity
direct digital chest X-ray units made it feasible to screen
250‒300 people per day, thus enabling completion of field
2.5 Sampling design
operations in each cluster in fewer than 5 working days.
A comprehensive description of the recommended
sampling design is outlined in Chapter 5 of the lime book
(2). 2.5.3 Stratification
Most surveys used stratified designs to increase
sampling efficiency, such as urban versus rural strata,
2.5.1 Sample size
or geographically defined strata (Table 2.4). Probability
Until the advent of rapid molecular tests (in particular, proportional to size (PPS) sampling was applied to the
Xpert MTB/RIF in 2010), smear examination was the selection of primary sampling units (regions, states,
main test used for TB diagnosis in most countries. From zones or provinces), followed by smaller secondary
the mid-1990s until the mid-2000s, routine reporting of sampling units (districts, townships, subdistricts and
notified cases of smear-positive pulmonary TB and their municipalities), and so on until reaching the level of
treatment outcomes was a core component of WHO’s geographical area that comprised the population size of a
recommended global TB strategy, global TB monitoring cluster. The last stage of cluster selection sometimes used
undertaken by WHO and national TB surveillance simple random sampling.
systems. Hence, up to 2015, sample size calculations were
based on the expected national prevalence of smear-
positive pulmonary TB among adults. The expected 2.5.4 Sampling frame
prevalence was generally based on the assumption of a The sampling frame defines the areas of the country from
prevalence to notification ratio of 2:1. For repeat surveys, which clusters are selected. Ideally, all clusters should
the sample size calculation was based on the expected be included in the sampling frame to ensure optimal
decline in the prevalence of smear-positive pulmonary national representativeness. However, certain areas were
TB since the previous survey (7). After 2015, following excluded in several surveys because of security concerns
WHO’s 2013 update to TB case definitions, sample size or geographic inaccessibility. Excluded areas generally
was calculated based on the expected prevalence of covered less than 5% of the total population (Table
bacteriologically confirmed pulmonary TB in adults. 2.4). In several surveys, some clusters that were initially
24 National TB prevalence surveys 2007–2016
Table 2.4
Sampling and survey design, 2007‒2016
Country Planned Planned Cluster Stratified Geographical areas Geographical areas
sample size number size sampling excluded initially from excluded during field
of sampling frame operations
clusters
Bangladesh 100 000 125 800 Urban, rural None One cluster was replaced for
security reasons
Cambodia 39 680 62 640 Urban, rural, None None
others
China 264 000 176 1500 Urban, rural None None
DPR Korea 69 442 100 700 Urban, rural None Five clusters in Anpyon,
Kyongsong and Pukchang
county were replaced by five
others in the same counties
due to inaccessibility
Ethiopia 46 514 85 550 Urban, rural, 37 out of 810 woredas (3% None
pastoralist of the national population)
were excluded from the
sampling frame for security
reasons and due to logistical
challenges; two clusters
(kebele) were replaced before
field operations started due
to logistical challenges
Gambia 55 281 80 700 Not stratified None Three clusters were replaced
due to a large uninhabited
area in the urban area
around the capital (one
cluster), military installations
and areas around the
president’s residence (two
clusters)
Ghana 63 905 98 650 Urban, rural None None
Indonesia 78 000 156 500 Sumatra, None None
Java-Bali and
others, with each
stratified into
urban/rural
Kenya 72 000 100 720 Urban, rural None One cluster in Mandera was
excluded for security reasons
Lao PDR 40 000 50 800 Not stratified None None
Malawi 37 200 74 500 Urban, semi- None None
urban, rural
Mongolia 49 000 98 600 City, provincial None None
(city) centre, rural
/ 500
(other)
Myanmar 49 690 70 710 Region, state 32 townships were excluded Five townships (Bokepyin,
for security reasons Kunlon, Kyarinnseikkyi,
Mindat and Nattalin) were
replaced by others within
the same township during
the pre-visit, owing to
security and transportation
problems, and an insufficient
population aged 15 years
and above
PART I: An overview of the 25 surveys implemented 2007–2016 25
Table 2.4
Continued
Country Planned Planned Cluster Stratified Geographical areas Geographical areas
sample size number size sampling excluded initially from excluded during field
of sampling frame operations
clusters
Nigeria 49 000 70 700 Six zones None Three clusters in the
states of Borno and Yobe
were excluded for security
reasons; these were replaced
in the states of Adamawa,
Bauchi and Gombe
Pakistan 133 000 95 1400 Not stratified The Federally Administered Three clusters from
Tribal Areas, district Dera Balochistan (Awaran, Lehri
Bugti in Balochistan and Quetta) were replaced
and 17 tehsils of Khyber by other clusters (Hub in
Pakhtunkhwa were excluded Balochistan, Khan Pur in
for security reasons; this Punjab, and Sharda in Azad-
accounted for 6.4% of the Jammu and Kashmir) for
national population security reasons
Philippines 30 000 50 600 Metro Manila, Four barangays in other None
(2007) other urban, rural urban strata and 14
barangays in rural strata were
excluded for security reasons
and due to inaccessibility
Philippines 54 000 108 500 National Capital Before field operations Three clusters (Maco,
(2016) Region, region 3 started, one cluster in Madaya and Sipangkot
and 4A; Rest of Basilan province was barangays) were replaced for
Luzon; Visayas; excluded for security reasons security reasons, and one
Mindanao (this accounted for <1% of cluster (Holy Spirit barangay)
the national population) was dropped because the
local authorities refused
house-to-house mobilization
and interviews
Rwanda 44 500 73 610 Not stratified None None
Sudan 91 131 114 800 Urban, rural None Four clusters (two in Darfur
State, one in Gazira and
one in South Kordofan)
were cancelled for security
reasons, and one was
removed due to a protocol
violation
Thailand a
74 700 83 900 Urban, rural None None
Uganda 40 180 70 580 Urban, rural None None
UR Tanzania 46 792 62 750 Urban, semi- None None
urban, rural,
Zanzibar
Viet Nam 105 000 70 1500 Urban, rural, None None
remote
Zambia 54 400 66 825 Urban, rural None None
Zimbabwe 44 951 75 600 Urban, rural None Two clusters (Chiredzi and
Macheke) were replaced
due to logistical issues (e.g.
weather, equipment failure)
DPR Korea, Democratic People’s Republic of Korea; Lao PDR, Lao People’s Democratic Republic; UR Tanzania, United Republic of Tanzania.
a
The Bangkok metropolitan area was excluded.
26 National TB prevalence surveys 2007–2016
selected were excluded after the sampling stage had Sputum specimens were transported via cold chain to
been completed, owing to security concerns or natural a designated laboratory, ideally within 3 days of specimen
disasters. collection to allow for rapid culturing and to avoid
contamination. A maximum processing time of 7 days
after collection in the field was recommended, provided
2.6 Field operations
that the cold chain was maintained.
The main activities conducted during field operations
include a census in each cluster, screening of participants,
and the collection and transportation of sputum 2.7 Additional testing for HIV infection and drug
specimens. The survey census and collection of sputum susceptibility
specimens are summarized below (screening methods 2.7.1 HIV testing
are described in Section 2.4.1). Information about the HIV status of TB patients is essential
both for individual patient care and for understanding
2.6.1 Survey census the epidemiology of TB. However, HIV testing was not
In each survey cluster, a population listing was typically usually done as part of survey field operations owing to
obtained by local volunteers 1‒2 weeks in advance of logistical constraints (Table 2.3). Only seven of the 25
the arrival of the survey investigators. In some surveys, surveys collected data about HIV status, and all seven of
the survey investigators (or staff from the bureau of these were in Africa. In Zambia, HIV testing was offered
statistics) undertook the census. At the beginning of field in the field to every survey participant as part of the
operations, the survey investigators would confirm the survey; in Rwanda, Uganda and the United Republic of
population listing, and assess each enumerated person’s Tanzania, HIV testing was offered as part of the survey to
eligibility to participate, based on their age and residential all participants that screened positive based on symptom
status (Table 2.1). screening or chest X-ray criteria (or both), with an opt-out
modality. When incorporated in the survey, HIV testing
During the census, data on household assets were
was implemented according to national guidelines, and
collected in several surveys to measure socioeconomic
included pre- and post-test counselling. In Malawi, given
status (in Kenya, Malawi, Mongolia, Myanmar, the
the high population coverage of HIV testing, all survey
Philippines, Rwanda, the United Republic of Tanzania,
participants were asked to report their HIV status to
Viet Nam and Zambia). In some of the surveys, it was
survey investigators. In Kenya and Zimbabwe, the HIV
possible to evaluate the relationship between household
status of survey cases was obtained from linkage with
poverty and TB disease (8).1
available records in routine disease information systems.
2.6.2 Sputum collection and transportation 2.7.2 Testing for drug susceptibility
Typically, two sputum samples (spot and the following
National TB prevalence surveys are not designed to
morning) were collected. It was often a challenge to
precisely estimate the prevalence of drug-resistant TB,
obtain quality sputum samples, compared with routine
owing to the small number of survey cases. However, drug
sputum collection for coughing patients who are seeking
susceptibility testing was usually done for all survey cases
medical care. Despite a WHO recommendation to take
to inform case management (Table 2.3). In some surveys
two spot specimens 1 hour apart on the same day (i.e.
that used Xpert MTB/RIF, rifampicin-susceptibility status
front loading) (9), in the setting of prevalence surveys, a
was recorded.
spot sample followed by a morning sample the next day
was generally advised. An additional second spot sample
(i.e. a third specimen) was collected in some surveys, 2.8 Central-level activities
especially when the quality of the first specimen was poor. Apart from the organisational and logistical aspects
of surveys, the main activities conducted at the central
level (as opposed to in the field) were the confirmatory
1
This study combined individual-level data from some of these countries, reading of chest X-rays and the review of participants
and found no relationship between household socioeconomic level with positive laboratory results.
and TB disease. However, because of the small numbers of TB cases
usually detected, prevalence surveys are not an efficient study design
for investigating TB risk factors.
PART I: An overview of the 25 surveys implemented 2007–2016 27
2.8.1 Central chest X-ray reading entered into a database at the central level. Subsequently,
A second reading of chest X-rays taken in the field was the digitalization of survey data management increased
done centrally by trained radiologists, to provide quality with the use of computers, personal digital assistants,
assurance of field chest X-ray readings, and a formal tablets, digital chest X-rays, barcoding and internet-
interpretation that could be used in determining the final connectivity in the field.
list of survey cases. In surveys undertaken before the use The survey in Ghana (in 2013) was the first to rely
of Xpert MTB/RIF, probable TB survey cases were defined predominantly on electronic data entry, and the survey
using positive smear results and chest X-ray readings, in Zambia was the first to be virtually “paper-free”. The
especially when culture was negative or not available. growing use of digital technologies increased the speed
In the later surveys done in Bangladesh, Kenya and the and efficiency with which data could be cleaned and
Philippines, central chest X-ray readings were also used analysed, and helped to improve data quality. It also
to define a case when culture positivity was weak1 and required additional investment in equipment and, in
there was no other positive evidence on Xpert MTB/RIF particular, staff with specialist information technology
or smear. skills. In areas with poor internet connectivity and
In most surveys, all chest X-rays were reread; however, unreliable power supply, complete reliance on digital
in countries with limited capacity, all abnormal chest systems was not possible. Furthermore, although such
X-rays and 10‒20% of normal chest X-rays were reread. technologies have many advantages, overreliance on
Some surveys attempted to have the central reading digital systems occasionally led to insufficient attention
undertaken at the same time as field operations, but since to data quality checks. Thus, systems using paper remain
this required major logistical organization and strong relevant, especially for data quality assurance and back-
internet connectivity, it rarely happened. up purposes.
Following data cleaning, analysis of survey results
usually required specialist technical assistance to
2.8.2 Central review of participants with positive
ensure the correct application of best-practice methods
laboratory results (10). Prevalence estimates were produced using three
Each survey conducted a review of all cases by a panel statistical approaches (cluster-based analysis, and two
that typically comprised the survey coordinator, a models based on individual-level analysis and multiple
radiologist, a medical officer, head of laboratory and the imputation for missing data). Multiple imputation of
data manager. The panel was responsible for the final missing data and inverse probability weighting was the
interpretation of radiographic and laboratory results for recommended method to report final results, unless there
all participants with any positive laboratory results (e.g. was a clear and documented justification to use one of
smear, culture or Xpert MTB/RIF). The panel had two the other two methods. With one exception, all national
objectives: to define and confirm the status of TB survey surveys implemented in the period 2007‒2016 were
cases; and to refer patients for further investigations and analysed using the recommended methods.2
treatment, as needed. Typically, the panel reviewed only
one to three cases each week. All panel decisions were
documented. 2.10 Additional studies
In surveys conducted before 2007 it was common
to implement, in parallel, a tuberculin survey; the
2.9 Data management and analysis Viet Nam survey (2007) was the last survey to do this (11).
Given the sample size of a typical TB prevalence survey The practice was discontinued following updated WHO
and the need to enter data from different sources (census, policy guidance in 2009 about the limited usefulness of
household surveys, symptom screening, field and central tuberculin surveys (12).
chest X-ray readings, and laboratory and final diagnostic Data about diseases or health conditions other than TB
panel decisions), data management is a crucial, and often – for example, smoking, chronic obstructive pulmonary
underestimated component of a survey (as discussed
in Chapter 4). In surveys implemented in the period
2007‒2014, data were mostly collected on paper and then 2
The 2007 survey in Viet Nam was analysed before the development
and publication of these methods. The 2007 survey in the Philippines
1
Weak positive culture is defined as one to nine colonies of M. was initially not analysed using the recommended methods, but was
tuberculosis. reanalysed using these methods in 2009.
28 National TB prevalence surveys 2007–2016
Table 2.5
Total budget and sources of funding for national TB prevalence surveys, 2007‒2016
Country Total budget Global Fund US government Domestic funding Other
(US$ millions)
Bangladesh 3.6 ● ● – –
Cambodia 1.0 ● ● – ●
China 5.6 – – ● –
DPR Korea 1.4 ● – ● –
Ethiopia 2.8 ● – ● ●
Gambia 1.9 ● – – ●
Ghana 2.2 ● – – ●
Indonesia 4.6 ● ● – –
Kenya 5.2 ● ● – ●
Lao PDR 1.3 ● ● – –
Malawi 2.2 ● – ● –
Mongolia 1.1 ● – ● ●
Myanmar 0.9 – ● – ●
Nigeria 3.1 ● – ● ●
Pakistan 4.4 – ● – ●
Philippines (2007) Not known ● – – ●
Philippines (2016) 2.4 ● – ● –
Rwanda 2.4 ● – – ●
Sudan 1.9 ● – ● –
Thailand 1.9 ● – ● –
Uganda 2.8 ● – – –
UR Tanzania 3.4 ● ● ● ●
Viet Nam 1.1 ● – ● ●
Zambia 5.4 ● ● – ●
Zimbabwe 3.5 ● – – –
DPR Korea, Democratic People’s Republic of Korea; Global Fund, Global Fund to Fight AIDS, Tuberculosis and Malaria; Lao PDR, Lao People’s Democratic Republic; UR
Tanzania, United Republic of Tanzania; US, United States of America.
● yes; – no
disease, obesity (body mass index was measured) and 2.11 Reporting and dissemination of results
diabetes – were collected in a few surveys to assess TB A report was produced for all 25 surveys, and results
risk factors. These data were not systematically collected from 11 surveys were published in a peer-reviewed
or analysed across all surveys. However, data on the journal (7, 16-52).1 The process took about 1.3 years (and
health care seeking behaviour of survey participants with sometimes up to 3 years) from the time of completing
symptoms suggestive of TB (e.g. cough ≥2 weeks) in the field operations to official dissemination of results or
United Republic of Tanzania, Viet Nam and Zambia were publication of findings.
published (13-15). These data highlighted the location
Some survey investigators published results that
where care was initially sought, and therefore the missed
extended beyond the primary objective of estimating
opportunities to diagnose TB, but they also highlighted
national TB prevalence. Examples include the health care
that many symptomatic participants did not seek care.
1
Ghana and Rwanda submitted a paper at the time of writing. Thailand
produced one report in Thai only.
PART I: An overview of the 25 surveys implemented 2007–2016 29
seeking behaviour of survey participants in the United and guidance on programmatic approaches. Geneva,
Switzerland 2016 (https://apps.who.int/iris/bitstre
Republic of Tanzania, Viet Nam and Zambia (13-15); am/10665/252424/1/9789241511506-eng.pdf, accessed 28
the characteristics of participants with non-tuberculosis November 2019).
mycobacteria and the use of computer-aided reading 6. World Health Organization. Fluorescent light-emitting diode
of chest X-rays in Zambia (53, 54); the diagnosis and (LED) microscopy for diagnosis of tuberculosis policy. Policy
statement. Geneva, Switzerland 2011 (https://apps.who.int/
treatment of TB in the private sector, and the association iris/bitstream/handle/10665/44602/9789241501613_eng.pdf,
between TB and household expenditure in Viet Nam accessed 28 November 2019).
(55, 56). Pooled survey data have been used to help 7. Mao TE, Okada K, Yamada N, Peou S, Ota M, Saint S et al. Cross-
understand differences in TB burden by sex, and the sectional studies of tuberculosis prevalence in Cambodia between
2002 and 2011. Bull World Health Organ. 2014;92(8):573–81
effect of household poverty on TB (8, 57). (https://www.ncbi.nlm.nih.gov/pubmed/25177072, accessed 28
November 2019).
8. Siroka A, Law I, Macinko J, Floyd K, Banda RP, Hoa NB et al.
2.12 Ethics approval The effect of household poverty on tuberculosis. Int J Tuberc
Lung Dis. 2016;20(12):1603–8 (https://www.ncbi.nlm.nih.gov/
All surveys were approved by their respective national pubmed/27931334, accessed 28 November 2019).
ethical review boards, and all protocols were reviewed 9. TB diagnostics and laboratory strengthening - WHO policy
and approved by partner agencies (e.g. those providing [website]. 2007 (https://www.who.int/tb/areas-of-work/
technical assistance) and the WHO Global Task Force on laboratory/policy_diagnosis_pulmonary_tb/en/, accessed 26
April 2019).
TB impact measurement.
10. Floyd S, Sismanidis C, Yamada N, Daniel R, Lagahid J, Mecatti F et
al. Analysis of tuberculosis prevalence surveys: new guidance on
best-practice methods. Emerg Themes Epidemiol. 2013;10(1):10
2.13 Budgeting and financing (https://www.ncbi.nlm.nih.gov/pubmed/24074436, accessed 28
As reported by the survey teams, the Global Fund was November 2019).
11. Hoa NB, Cobelens FG, Sy DN, Nhung NV, Borgdorff MW,
a crucial source of financing for all but three surveys
Tiemersma EW. First national tuberculin survey in Viet Nam:
(Table 2.5; further details in individual country characteristics and association with tuberculosis prevalence. Int
profiles). Other international funders, especially the US J Tuberc Lung Dis. 2013;17(6):738–44 (https://www.ncbi.nlm.nih.
gov/pubmed/23676155, accessed 28 November 2019).
government, also made major contributions to survey
12. TB impact measurement policy and recommendations for how
funding. Some countries were able to fully or partially to assess the epidemiological burden of TB and the impact
fund their surveys from domestic resources. Most of the of TB control. Stop TB policy paper no. 2, Geneva: World
international technical assistance for the 25 surveys was Health Organization; 2009 (https://apps.who.int/iris/bitstream/
handle/10665/44231/9789241598828_eng.pdf, accessed 22
funded by the US government and the Japan International November 2019).
Cooperation Agency. 13. Chanda-Kapata P, Kapata N, Masiye F, Maboshe M, Klinkenberg
E, Cobelens F et al. Health seeking behaviour among
individuals with presumptive tuberculosis in Zambia. PLoS
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PART I: An overview of the 25 surveys implemented 2007–2016 31
Use of a digital chest X-ray during the 2015-2016 national TB prevalence survey of Kenya.
Photo credit: Jane Rahedi Ong’ang’o / KEMRI
33
Chapter 3
3.1 Survey population, enrolment and participation of whether a future survey should be attempted will be
Table 3.1 shows the size of the planned sample needed, especially if there are further increases in the
population in national tuberculosis (TB) prevalence proportion of the population living in urban or more
surveys implemented in 2007–2016. The table also shows economically developed areas. This is discussed further
the actual size of the eligible population, the number of in Chapter 5.
people who participated, the participation rate and the
number of participants who screened positive for sputum 3.1.2 Eligibility for sputum examination
examination.
The proportion of participants who were eligible for
sputum examination averaged 16%, ranging from a low
3.1.1 Participation of 4% of screened participants in China to a high of 40%
The participation rate was high in most surveys, at ≥80% in the 2016 survey in the Philippines (Table 3.1). The
of the eligible population in 19 of 25 surveys (Fig. 3.1 proportion was more than 20% in Bangladesh, Indonesia,
and Table 3.1). The six countries with lower participation Mongolia, Myanmar, the Philippines (2007 and 2016)
rates were Gambia, Nigeria, the Philippines (in 2016), and Sudan, due to high yields from chest X-ray screening.
Thailand, the United Republic of Tanzania and Zimbabwe. In 15 of 25 surveys, chest X-ray screening identified
In general, participation rates were higher among more participants eligible for sputum examination than
females, and middle and older age groups, compared symptom screening (Table 3.1). However, the opposite
with males and younger age groups (see Part II for applied in Malawi, the United Republic of Tanzania and
details). Reasons for non-participation were not routinely Zambia; these African countries used a broader range of
documented, but included previous work-related health symptoms with the aim of increasing the sensitivity of the
assessments or ease of access to health facilities (both screening algorithm in a high HIV prevalence setting.1
of which reduced the incentive to participate for the Of the other seven surveys, screening yields were similar,
purposes of having a chest X-ray examination), as well and one survey (Philippines 2007) did not systematically
as lack of time. use symptoms for screening purposes.
Achieving high levels of participation in highly
urban settings, especially capital cities, was challenging 3.2 TB prevalence and updated estimates of TB
in almost all countries. The most extreme example was disease burden
the Bangkok metropolitan area of Thailand, in which 3.2.1 Prevalence of pulmonary TB disease
only 26% of the eligible population participated. Results
Surveys showed that the estimated prevalence of
from Bangkok were subsequently excluded from the final
pulmonary TB per 100 000 population was high in many
analysis.
countries, but there was also considerable variation
In the Republic of Korea, the repetition of prevalence
surveys every 5 years was discontinued after 1995
because of declining participation (in the context of
an increasingly urbanized and modern environment) 1
The symptom screening criteria used in Malawi were any symptom for at
and a reduction in disease burden, which would have least 1 week, including cough, sputum production, haemoptysis, chest
pain, weight loss, night sweats, fatigue, fever or shortness of breath; in
necessitated much larger sample sizes (1). In countries the United Republic of Tanzania, cough of ≥2 weeks, or haemoptysis
that were not able to achieve a high participation rate in or fever of ≥2 weeks, or weight loss or excessive night sweats; and in
Zambia, cough of ≥2 weeks, or fever of ≥2 weeks, or chest pain of ≥2
surveys implemented in 2007–2016, careful consideration weeks.
34
Table 3.1
Summary of sampling population, survey participants and screening outcomes
Country Timeframe Planned Number Survey Number of participants eligible for sputum examination
of field sample of people participants
operations population eligible to
Number Rate Sym+, % Sym+, % Sym-, % Others % Any % Any % Total %
participate
(%) CXR+ CXR-/ N/A CXR+ Sym+ CXR+ eligible
Africa
Ethiopia 2010–2011 46 514 51 667 46 697 90% 806 1.7% 2220 4.8% 3013 6.5% 41 0.09% 3026 6.5% 3819 8.2% 6080 13%
Gambia 2011–2013 55 281 55 832 43 100 77% 1026 2.4% 2436 5.7% 2384 5.5% 102 0.24% 3462 8.0% 3410 7.9% 5948 14%
Ghana 2013 63 905 67 757 61 726 91% 771 1.2% 1198 1.9% 4387 7.1% 1942 3.1% 1969 3.2% 5158 8.4% 8298 13%
National TB prevalence surveys 2007–2016
Kenya 2015–2016 72 000 76 291 63 050 83% 1241 2.0% 2896 4.6% 5184 8.2% 394 0.62% 4137 6.6% 6425 10% 9715 15%
Malawi 2013–2014 37 200 39 026 31 579 81% 381 1.2% 2334 7.4% 717 2.3% N/A N/A 2715 8.6% 1098 3.5% 3432 11%
Nigeria 2012 49 000 77 797 44 186 57% 746 1.7% 1720 3.9% 2222 5.0% N/A N/A 2466 5.6% 2968 6.7% 4688 11%
Rwanda 2012 44 500 45 058 43 128 96% 545 1.3% 2092 4.9% 2107 4.9% 3 0.01% 2637 6.1% 2652 6.1% 4747 11%
Sudan 2013–2014 91 131 96 979 83 202 86% 1823 2.2% 840 1.0% 9838 12% 5040 6.1% 2663 3.2% 11 661 14% 17 541 21%
Uganda 2014–2015 40 180 45 293 41 154 91% 552 1.3% 2162 5.3% 2298 5.6% 130 0.32% 2714 6.6% 2850 6.9% 5142 12%
UR Tanzania 2011–2012 46 792 65 664 50 447 77% 804 1.6% 3459 6.9% 2039 4.0% N/A N/A 4263 8.5% 2843 5.6% 6302 12%
Zambia 2013–2014 54 400 54 830 46 099 84% 1505 3.3% 2948 6.4% 2255 4.9% N/A N/A 4453 10% 3760 8.2% 6708 15%
Zimbabwe 2014 44 951 43 478 33 736 78% 628 1.9% 1205 3.6% 2803 8.3% 1184 3.5% 1833 5.4% 3431 10% 5820 17%
Total 83% 1.8% 4.7% 6.2% 1.7% 6.5% 8.0% 14%
Asia
Bangladesh 2015–2016 100 000 108 834 98 710 91% 3077 3.1% 4217 4.3% 13 300 13% N/A N/A 7294 7.4% 16 377 17% 20 594 21%
Cambodia 2010–2011 39 680 40 423 37 417 93% 710 1.9% 1206 3.2% 2699 7.2% 165 0.44% 1916 5.1% 3409 9.1% 4780 13%
China 2010 264 000 263 281 252 940 96% 797 0.32% 4665 1.8% 2189 0.87% 2174 0.86% 5462 2.2% 2986 1.2% 9825 3,9%
DPR Korea 2015–2016 70 000 71 877 60 683 84% 1028 1.7% 1916 3.2% 1858 3.1% N/A N/A 2944 4.9% 2886 4.8% 4802 7,9%
Indonesia 2013–2014 78 000 76 576 67 944 89% 4459 6.6% 4093 6.0% 6743 10% 151 0.22% 8552 13% 11 202 16% 15 446 23%
Lao PDR 2010–2012 40 000 46 079 39 212 85% 1312 3.3% 1927 4.9% 3107 7.9% N/A N/A 3239 8.3% 4419 11% 6346 16%
Mongolia 2014–2015 49 000 60 031 50 309 84% 817 1.6% 1729 3.4% 7064 14% 749 1.5% 2546 5.1% 7881 16% 10 359 21%
Myanmar 2009–2010 49 690 57 607 51 367 89% 1258 2.4% 433 0.84% 9364 18% 1180 2.3% 1691 3.3% 10 622 21% 12 235 24%
Pakistan 2010–2011 133 000 131 329 105 913 81% 2819 2.7% 2598 2.5% 5042 4.8% 12 0.01% 5417 5.1% 7861 7.4% 10 471 10%
Philippines 2007 30 000 22 867 20 643 90% N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A 5378 26%
Philippines 2016 54 000 61 466 46 689 76% 1444 3.1% 1371 2.9% 10 702 23% 5080 11% 2815 6.0% 12 146 26% 18 597 40%
Thailand 2012–2013 90 000 78 839 62 536 79% 526 0.84% 1757 2.8% 3767 6.0% N/A N/A 2283 3.7% 4293 6.9% 6050 10%
Viet Nam 2006–2007 105 000 103 924 94 179 91% 518 0.55% 3522 3.7% 2972 3.2% 993 1.1% 4040 4.3% 3490 3.7% 8005 8,5%
Total 87% 2.3% 3.3% 9.3% 2.2% 5.7% 12% 17%
CXR, chest X-ray; DPR Korea, Democratic People’s Republic of Korea; Lao PDR, Lao People’s Democratic Republic; N/A, not applicable; Sym, symptom; UR Tanzania, United Republic of Tanzania; +, positive; -, negative.
PART I: An overview of the 25 surveys implemented 2007–2016 35
Fig. 3.1
Participation rate in 25 surveys (24 countries) implemented in 2007−2016
DPR Korea, Democratic People’s Republic of Korea; Lao PDR, Lao People’s Democratic Republic; UR Tanzania, United Republic of Tanzania.
among countries and between Africa and Asia (Fig. 3.2 119 (95% CI: 103–135) in China to 1159 (95% CI: 1016–
and Table 3.2). 1301) in the Philippines (in 2016). As in the surveys in
In African countries, the prevalence of smear-positive African countries, the proportion of bacteriologically
pulmonary TB per 100 000 population aged 15 years or confirmed pulmonary TB cases that were smear-positive
above ranged from 74 (95% confidence interval [CI]: varied widely, from 33% in Cambodia to 68% in Pakistan
48–99) in Rwanda to 319 (95% CI 232–406) in Zambia. (Table 3.2).
Similarly, the prevalence of bacteriologically confirmed The systematic use of culture (as well as Xpert® MTB/
pulmonary TB per 100 000 population aged 15 years RIF in three of the later surveys)1 identified more smear-
or above ranged from 119 (95% CI: 79–160) in Rwanda negative than smear-positive pulmonary TB cases in all
to 638 (95% CI: 502–774) in Zambia. There was great but the following eight surveys: China, the Democratic
variation in the proportion of bacteriologically confirmed People’s Republic of Korea, Nigeria, Pakistan, Rwanda,
pulmonary TB cases that were smear-positive in Africa, Sudan, Viet Nam and Zambia (Table 3.2).
from a low of 24% in Zimbabwe to a high of 62% in
Rwanda (Table 3.2).
3.2.2 Prevalence of pulmonary TB disease
In Asian countries, the prevalence of smear-positive disaggregated by age and sex
pulmonary TB per 100 000 population aged 15 years or
The distribution of prevalent cases by age is shown in
above ranged from 66 (95% CI: 53–79) in China to 434
Fig. 3.3a for surveys in African countries and Fig. 3.3b
(95% CI: 350–518) in the Philippines (in 2016). Similarly,
for surveys in Asian countries. In the latter, there was
the prevalence of bacteriologically confirmed TB per
100 000 population aged 15 years or above ranged from
1
Bangladesh (2015), Kenya (2015) and the Philippines (2016).
36 National TB prevalence surveys 2007–2016
Fig. 3.2
Estimates of the prevalence of bacteriologically confirmed pulmonary TB in those aged ≥15 years in 25 surveys (24 countries)
implemented in 2007−2016
DPR Korea, Democratic People’s Republic of Korea; Lao PDR, Lao People’s Democratic Republic; UR Tanzania, United Republic of Tanzania.
a clear pattern in which prevalence increased with age In other countries, surveys suggested considerable
(an exception was the Democratic People’s Republic community transmission.
of Korea). In African countries, this pattern was only A striking finding across all surveys was the much
observed in Ghana and Rwanda, although in Malawi and higher burden of TB disease in men compared with
the United Republic of Tanzania there was an increase women (Fig. 3.4). The male to female ratio of the
between the age groups of 45–54 years and of 65 years or prevalence of bacteriologically confirmed TB was 2.3
more, after an earlier peak in the age group 35–44 years. (95% CI: 2.0–2.6) overall, but ranged from 1.2 in Ethiopia
In most African countries, there was a peak in prevalence to more than 4 in Uganda and Viet Nam. It was higher
per 100 000 population in the age groups 35–44 or 45– in Asia (2.6) than in Africa (2.0). These results mean
54 years,1 which could be explained at least in part by the that men account for about 66–70% of the burden of TB
impact of the HIV epidemic. disease among adults in Asia and Africa.
As transmission declines, more incident cases arise
from past rather than recent infection. Therefore, a pattern
3.2.3 Estimates of the prevalence of TB, all ages and
in which prevalence increases with age suggests that
transmission is falling. It is encouraging that prevalence
all forms
surveys indicated that transmission is potentially Following surveys, estimates of the prevalence of TB for
declining in many Asian countries as well as in Ghana, all ages (i.e. including those aged <15 years) and all forms
Malawi, Rwanda and the United Republic of Tanzania. (i.e. including extrapulmonary as well as pulmonary TB)
were updated by WHO in consultation with national
authorities. Fig 3.5 compares the updated estimates with
1
The estimated absolute number of TB cases in each age group is shown the most recent estimates published before survey results
in Fig. 3 of the country profiles in Part II. became available.
Table 3.2
Estimated prevalence of smear-positive and bacteriologically confirmed pulmonary TB
Country Smear-positive pulmonary TB Bacteriologically confirmed pulmonary TB Proportion of
Number Prevalence per 95% k b
Number Prevalence per 95% kb bacteriologically
of cases 100 000 population aged confidence of cases 100 000 population aged confidence confirmed cases that were
≥15 years a interval ≥15 years a interval smear-positive
Africa
Ethiopia 47 108 73–143 0.7 110 277 208–347 0.4 39
Gambia 34 90 53–127 1.3 77 212 152–272 0.7 42
Ghana 64 111 76–145 0.9 202 356 288–425 0.7 31
Kenya 123 230 174–286 0.7 305 558 455–662 0.7 41
Malawi 62 220 142–297 1.1 132 452 312–593 1.1 49
Nigeria 107 318 225–412 0.9 144 524 378–670 0.7 61
Rwanda 27 74 48–99 N/Ac 40 119 79–160 0.7 62
Sudan 57 87 52–121 1.3 112 183 128–238 1.3 48
Uganda 66 174 111–238 0.9 160 401 292–509 0.8 43
c
UR Tanzania 134 275 232–326 0.6 N/A N/A N/A N/A N/A
Zambia 135 319 232–406 0.8 265 638 502–774 0.7 50
d
Zimbabwe 23 82 47–118 N/A 107 344 268–420 0.3 24
Asia
Bangladesh 108 113 87–139 0.7 278 287 244–330 0.5 39
Cambodia 103 271 212–348 0.6 314 831 707–977 0.5 33
China 188 66 53–79 0.9 347 119 103–135 0.5 55
DPR Korea 187 330 283–377 2.0 340 587 520–655 0.6 56
Indonesia 165 257 210–303 0.7 426 759 590–961 0.5 34
Lao PDR 107 278 199–356 0.7 237 595 457–733 0.7 47
Mongolia 88 204 143–265 1.5 248 560 455–665 0.9 36
Myanmar 123 242 186–315 0.8 311 613 502–748 0.7 39
Pakistan 233 270 217–323 0.6 341 398 333–463 0.6 68
Philippines (2007) 55 280 190–370 1.0 136 660 530–800 0.6 42
Philippines (2016) 173 434 350–518 0.6 446 1159 1016–1301 0.6 37
Thailand 58 104 55–195 1.0 142 242 176–332 0.5 43
Viet Nam 174 197 150–244 0.8 269 307 249–366 0.6 64
DPR Korea, Democratic People’s Republic of Korea; Lao PDR, Lao People’s Democratic Republic; N/A, not applicable; TB, tuberculosis; UR Tanzania, United Republic of Tanzania.
a
Estimates are based on the use of robust standard errors with missing value imputation and inverse probability weighting for all countries except the United Republic of Tanzania, for which a cluster-level model of analysis was used.
b
k is the coefficient of variation of the cluster-specific TB prevalences.
c
The number of bacteriologically confirmed pulmonary TB cases could not be verified for the United Republic of Tanzania.
d
For Rwanda and Zimbabwe, k could not be calculated because the design effect was less than one.
PART I: An overview of the 25 surveys implemented 2007–2016
37
38 National TB prevalence surveys 2007–2016
Fig. 3.3a
Estimated age-specific prevalence of bacteriologically confirmed pulmonary TB for surveys implemented in Africa in 2010−2016
The red line denotes the best estimate and the blue shaded areas are the 95% confidence intervals.
In all countries, estimates of TB prevalence based on and lower in 10 countries (most noticeably in Ethiopia,
national surveys were much more precise than presurvey Gambia and Zimbabwe).
estimates (i.e. uncertainty intervals were much narrower).
In most countries, best estimates based on surveys
3.3 Trends in TB prevalence measured in repeat
were also within the uncertainty interval of presurvey
estimates. Best estimates of TB prevalence based on
surveys
survey results were higher than presurvey estimates in Among countries that conducted prevalence surveys
15 countries (most noticeably in Ghana, Indonesia, Lao between 2007 and 2016, three countries had undertaken
People’s Democratic Republic, Malawi, Mongolia, the at least one survey in the preceding 20 years: Cambodia
Philippines (2016) and the United Republic of Tanzania) (2002), China (1990, 2000 and 2010) and the Philippines
PART I: An overview of the 25 surveys implemented 2007–2016 39
Fig. 3.3b
Estimated age-specific prevalence of bacteriologically confirmed pulmonary TB for surveys implemented in Asia in 2007−2016
The red line denotes the best estimate and the blue shaded areas are the 95% confidence intervals.
DPR Korea, Democratic People’s Republic of Korea; Lao PDR, Lao People’s Democratic Republic; TB, tuberculosis.
(1997 and 2007). Trends in TB prevalence based on (see also Chapter 1). The reduction in TB prevalence in
surveys conducted since 2007 are shown in Fig. 3.6. China between 2000 and 2010 occurred during a period
The repeat surveys in Cambodia and China of nationwide expansion of DOTS (from half to all of
demonstrated that substantial reductions in TB the country). The reduction in Cambodia occurred
prevalence can be achieved within 10 years. Observed during a period when DOTS services were expanded to
reductions in the prevalence of smear-positive pulmonary health centres as well as hospitals, making TB diagnostic
TB in particular were consistent with the prioritization and treatment services much more accessible (2-4).
given to detection and cure of the most infectious cases However, the Philippines fourth national survey, in 2016,
within the framework of the DOTS strategy, which was showed concerning results. Following a reduction in TB
recommended by WHO between the mid-1990s and 2006 prevalence between 1997 and 2007, no decline occurred
40 National TB prevalence surveys 2007–2016
Fig. 3.4
The sex ratio (male to female) of bacteriologically confirmed pulmonary TB cases detected in prevalence surveys implemented in
2007−2016
DPR Korea, Democratic People’s Republic of Korea; Lao PDR, Lao People’s Democratic Republic; TB, tuberculosis; UR Tanzania, United Republic of Tanzania.
a
The sex ratio of smear−positive TB cases is shown for the United Republic of Tanzania.
Fig. 3.5
Estimates of TB prevalence (all ages, all forms of TB) for 25 surveys (24 countries), before (in blue) and after (in red) results became
available from national TB prevalence surveys implemented in 2007−2016
Countries are listed in decreasing order according to the before−after difference.
DPR Korea, Democratic People’s Republic of Korea; Lao PDR, Lao People’s Democratic Republic; UR Tanzania, United Republic of Tanzania.
PART I: An overview of the 25 surveys implemented 2007–2016 41
Fig. 3.6
Trends in bacteriologically confirmed pulmonary TB measured in repeat surveys in Cambodia, China and the Philippines
Shaded areas represent uncertainty intervals.
a
The trend is for culture-confirmed cases.
between 2007 and 2016. This may be linked to broader (median 48%, range 21–70%) would have been identified
determinants of the TB epidemic, notably levels of if relying on symptom screening alone (Table 3.3). Other
poverty and undernutrition (5). cases were identified due to chest X-ray screening.
Although not featured in this book, repeat surveys in Among countries that used chronic cough alone as a
Myanmar in 2018 and Viet Nam in 2017 showed large symptom screening criterion, the proportion of people
reductions in disease burden from 2009 to 2018 and from with bacteriologically confirmed pulmonary TB that did
2007 to 2017, respectively (6). not report this symptom ranged from 36% in Nigeria to
79% in Mongolia. When chronic cough or haemoptysis
(or both) were used, the proportion ranged from 43% in
3.4 Proportion of survey cases reporting
the Democratic People’s Republic of Korea and Indonesia
symptoms that met screening criteria to 79% in Myanmar. When cough and other TB-related
A consistent finding in all surveys was that a high symptoms were used, the proportion ranged from 30% in
proportion of people with bacteriologically confirmed Malawi to 66% in Thailand (Fig. 3.7, Table 3.3).
pulmonary TB did not report symptoms that met
These findings can be explained by the fact that a
screening criteria. Although symptom screening criteria
prevalence survey identifies many people in the earlier
varied between countries (Table 3.2), only about half
stages of TB disease, before symptoms become more
of the bacteriologically confirmed pulmonary TB cases
serious. These people will remain a source of transmission
42
Table 3.3
Screening outcomes of bacteriologically confirmed pulmonary TB cases
Country Number of Symptom screening definition a Symptom Symptom Symptom Other Proportion Proportion
bacteriologically positive, positive, chest negative, chest screening identified identified by
confirmed TB chest X-ray X-ray X-ray positive category a by symptom chest X-ray
cases positive negative/ N/A screening (%) screening (%)
Ethiopia 110 Cough ≥2 weeks 45 12 53 0 52% 89%
Ghana 202 Cough ≥2 weeks 67 15 85 35 41% 75%
Kenya 305 Cough ≥2 weeks 115 32 154 4 48% 88%
Mongolia 248 Cough ≥2 weeks 44 7 194 3 21% 96%
National TB prevalence surveys 2007–2016
Fig. 3.7
Proportion of prevalent TB cases that were symptom−screen negative in surveys implemented in 2007−2016
DPR Korea, Democratic People’s Republic of Korea; Lao PDR, Lao People’s Democratic Republic; UR Tanzania, United Republic of Tanzania.
a
The Philippines (2007) survey did not use symptom screening; however, symptom−related data were collected from all detected TB cases.
until they experience symptoms that prompt them to Among those who do seek care, widening the use of
seek health care. Even if they had sought care at an earlier chest X-ray screening in primary health care facilities
stage, it is unlikely (with existing screening criteria) that and raising awareness among health care staff about
they would have been referred for further laboratory the magnitude and characteristics of TB cases in the
testing on the basis of reported symptoms. community could contribute to earlier diagnosis.
As access to TB diagnostic and treatment services
improve, the proportion of prevalent cases in the 3.5 Detection and reporting gaps
community that do report the ‘classic’ symptoms of
When measurements of prevalence are compared with
pulmonary TB should fall. A prevalence survey in which
official case notification data, prevalence surveys can
a high proportion of cases do not report symptoms may
identify gaps in detection and reporting. Overall ratios
indicate relatively good access to TB diagnosis and care,
of prevalent (P) to notified (N) cases are shown in Fig.
whereas a low proportion tends to suggest that access
3.8a, and ratios disaggregated by sex are shown in Fig.
needs to be improved. An example of this was Nigeria,
3.8b–d.1 Ratios ranged from 0.62 in Gambia to 5.8 in
where many cases found in the survey already had
Nigeria. For all countries except the Philippines in 2007
symptoms that should have prompted care seeking and
and Zimbabwe, the ratio was higher in men than women.
prompt diagnostic testing at health facilities. An increased
proportion of cases not reporting symptoms in a repeat Cross-country and male/female differences in the P:N
survey is consistent with improved health care services. ratio show that in several countries it should be possible
This was a pattern found in the 2010–2011 survey in 1
The P:N ratio is an approximate indicator (expressed in years) of case
Cambodia, in which the prevalence of people with smear- detection by the NTP (7). The higher the ratio, the longer the time taken
for a prevalent case to be notified to the NTP. Some cases may exit the
positive pulmonary TB that reported symptoms fell by
pool of prevalent cases without being notified, for example because they
56% compared with 2002. self-cure or die, or because they are detected and treated by providers
not linked to official reporting systems.
44 National TB prevalence surveys 2007–2016
Fig. 3.8a
TB prevalence to TB notification (P:N) ratio in surveys implemented in 2007−2016 a
DPR Korea, Democratic People’s Republic of Korea; Lao PDR, Lao People’s Democratic Republic; UR Tanzania, United Republic of Tanzania.
a
The comparison is for smear−positive pulmonary TB for all countries except for Bangladesh, DPR Korea, Kenya, Uganda and Zimbabwe, for which the comparison is for
bacteriologically confirmed pulmonary TB.
Fig. 3.8b
TB prevalence to TB notification (P:N) ratio (male) in surveys implemented in 2007−2016 a
DPR Korea, Democratic People’s Republic of Korea; Lao PDR, Lao People’s Democratic Republic; UR Tanzania, United Republic of Tanzania.
a
The comparison is for smear−positive pulmonary TB for all countries except for Bangladesh, DPR Korea, Kenya, Uganda and Zimbabwe, for which the comparison is for
bacteriologically confirmed pulmonary TB.
PART I: An overview of the 25 surveys implemented 2007–2016 45
Fig. 3.8c
TB prevalence to TB notification (P:N) ratio (female) in surveys implemented in 2007−2016 a
DPR Korea, Democratic People’s Republic of Korea; Lao PDR, Lao People’s Democratic Republic; UR Tanzania, United Republic of Tanzania.
a
The comparison is for smear−positive pulmonary TB for all countries except for Bangladesh, DPR Korea, Kenya, Uganda and Zimbabwe, for which the comparison is for
bacteriologically confirmed pulmonary TB.
Fig. 3.8d
Comparison of the TB prevalence to TB notification (P:N) ratio between men (green) and women (orange) in surveys implemented in
2007−2016 a
DPR Korea, Democratic People’s Republic of Korea; Lao PDR, Lao People’s Democratic Republic; UR Tanzania, United Republic of Tanzania.
a
The comparison is for smear-positive pulmonary TB for all countries except for Bangladesh, DPR Korea, Kenya, Uganda and Zimbabwe, for which the comparison is for
bacteriologically confirmed pulmonary TB.
46 National TB prevalence surveys 2007–2016
to achieve better (i.e. lower) ratios with strategies and testing policies, the logistics of taking blood samples in
technologies for TB diagnosis and treatment that are the field, and the concern that survey participation might
already available, and to close reporting and detection be negatively affected by refusing an HIV test. None of
gaps for men. Although the burden of TB disease was the surveys in Asia included HIV testing. HIV testing
consistently higher in men, P:N ratios were systematically results or the HIV status of participants (or both) were
lower among women, suggesting that women were obtained as part of the surveys in seven African countries:
accessing available diagnostic and treatment services Kenya, Malawi, Rwanda, Uganda, the United Republic of
more effectively (8). Development of strategies to improve Tanzania, Zambia and Zimbabwe (Table 3.4).
care seeking and diagnosis among men are warranted in HIV testing during field operations was done in only
many countries. four countries: Rwanda, Uganda, the United Republic
In some countries, P:N ratios also indicated that older of Tanzania and Zambia. In Rwanda, Uganda and the
people with TB were detected less effectively (Fig. 3.9). United Republic of Tanzania, only those eligible for
This may reflect financial and geographical accessibility sputum examination were offered an HIV test. In Zambia,
barriers. Older people may also have greater tolerance HIV testing was offered to all survey participants. In
of symptoms or associate symptoms with other chronic Zambia, 2063 (6.7%) of those tested were HIV-positive.
health conditions, leading to delayed care seeking and In Rwanda, Uganda and the United Republic of Tanzania,
associated investigations. the proportions of those tested who were HIV-positive
In Indonesia (9) and Viet Nam (10), the records were 4.9%, 9.6% and 5.0%, respectively.
of survey participants on treatment at the time of the In Malawi, all participants were asked if they had
survey were linked to the records of newly detected cases ever been tested for HIV, and were invited to disclose
from routine TB surveillance, enabling the magnitude their status; verbal acknowledgement of HIV status was
of underreporting of detected cases to be measured. In provided for 19 703 (62%) participants, of which 1840
Indonesia, of the participants who reported that they were (9.3%) reported that they were HIV-positive. In Kenya and
on TB treatment, only 19% (24/125) were identified in Zimbabwe, records of survey cases were linked to records
the national TB register, which helps to explain the high from routine HIV treatment and care programmes. The
P:N ratio. In Viet Nam, 10% (37/353) of the participants proportion of survey cases who were HIV-positive was
that screened positive and were recently treated for TB 13% in Kenya and 51% in Zimbabwe.
had not been reported to the NTP. HIV prevalence among prevalent TB cases was
Whenever possible, future surveys should include systematically lower than HIV prevalence among newly
comparison of the records of cases on treatment at the notified cases (Fig. 3.10), probably reflecting the faster
time of the survey with a national case-based electronic progression of TB disease in people living with HIV,
TB database, to assess the level of underreporting. which prompts earlier care seeking. It is also plausible
Alternatively, or in addition,1 national inventory studies that the expansion of HIV care programmes since the
(11) can be used to measure levels of underreporting. early 2000s contributed to earlier detection and treatment
A good example was the national inventory study in of TB among people living with HIV.
Indonesia, which was prompted by findings from the
national TB prevalence survey.2
3.7 Health care seeking behaviour
Patterns of health care seeking behaviour can help to
3.6 HIV testing and the prevalence of HIV identify actions that could be taken to shorten the time to
Although HIV testing is a routine part of TB case TB diagnosis and treatment. They may also indicate care
management, collection of data about HIV status was providers that need to be better engaged with the NTP,
not standardized in prevalence surveys implemented in including to ensure reporting of detected cases.
2007–2016. Reasons included variation in national HIV Although there was limited standardization in the
data on health care seeking behaviour that were collected
during surveys implemented in 2007–2016, it was clear
1
Cases detected before survey investigations are typically not as well that a large proportion of symptomatic participants
documented as survey cases detected during investigations, particularly
had not sought care before the survey (Table 3.5). The
in countries where culture or Xpert MTB/RIF are not routinely used.
2
Results and lessons learned from this study were documented in the
median proportion of those reporting symptoms that
2018 WHO global TB report (12).
PART I: An overview of the 25 surveys implemented 2007–2016 47
Fig. 3.9
TB prevalence to TB notification (P:N) ratio by age group in surveys implemented in 2007−2016 a
DPR Korea, Democratic People’s Republic of Korea; Lao PDR, Lao People’s Democratic Republic; UR Tanzania, United Republic of Tanzania.
a
The comparison is for smear-positive pulmonary TB for all countries except for Bangladesh, DPR Korea, Kenya, Uganda and Zimbabwe, for which the comparison is for
bacteriologically confirmed pulmonary TB.
48
Table 3.4
HIV status of participants and bacteriologically confirmed pulmonary TB cases
Participants Participants who screened positive Bacteriologically confirmed pulmonary TB cases
a
Country Number of % HIV- % HIV- % Total Number of % HIV- % HIV- % Total Number % HIV- % HIV- %
participants positive negative screened participants positive negative TB who were positive negative
who were tested positive who were cases tested for
for HIV, or had tested for HIV or with
documented HIV HIV, or with reported
status documented HIV status
HIV status
b
Kenya N/A N/A N/A N/A N/A N/A 9715 N/A N/A N/A N/A N/A N/A 305 245 80% 41 17% 204 67%
c a
Malawi 19 703 62% 1840 9.3% 17 863 91% 3432 2066 60% 339 16% 1708 83% 132 78 59% 22 28% 52 67%
National TB prevalence surveys 2007–2016
d
Rwanda N/A N/A N/A N/A N/A N/A 4747 4445 94% 218 4.9% 4227 95% 40 36 90% 1 2.8% 35 97%
d
Uganda N/A N/A N/A N/A N/A N/A 5142 4386 85% 422 9.6% 3964 90% 160 145 91% 39 27% 106 73%
d,e
UR Tanzania N/A N/A N/A N/A N/A N/A 6302 6302 100 318 5.0% 5984 95% N/A N/A N/A N/A N/A N/A N/A
f
Zambia 30 584 66% 2062 6.7% 28 522 93% 6708 N/A N/A N/A N/A N/A N/A 265 134 51% 36 27% 98 73%
g
Zimbabwe N/A N/A N/A N/A N/A N/A 5820 N/A N/A N/A N/A N/A N/A 107 83 78% 42 51% 41 49%
HIV, human immunodeficiency virus; N/A, not applicable; UR Tanzania, United Republic of Tanzania.
a
For Malawi and Zambia, the denominator is the total number of survey participants as shown in Table 3.1.
b
In Kenya, HIV testing was not done as part of the survey. HIV data were obtained from the national HIV reporting system of linked TB cases.
c
In Malawi, there was verbal reporting of HIV status only. Of 2066 participants who screened positive, 19 had unknown status. For 48 out of 78 bacteriologically confirmed TB cases, their HIV status was unknown.
d
In Rwanda, Uganda and the United Republic of Tanzania, only those who screened positive were tested for HIV during field operations.
e
In the United Republic of Tanzania, bacteriologically confirmed TB cases could not be verified.
f
In Zambia, all survey participants were invited to be tested for HIV during field operations.
g
In Zimbabwe, all bacteriologically confirmed TB cases detected by the survey were offered HIV counselling and testing as part of routine treatment management and were not directly tested as part of the survey.
PART I: An overview of the 25 surveys implemented 2007–2016 49
Fig. 3.10
HIV prevalence in TB survey cases compared with HIV prevalence in notified TB cases expressed as a ratio, in surveys implemented in
2007−2016
met screening criteria who had not yet sought care was high positive predictive values can be demonstrated in
42% (range, 10–67%), suggesting that there are barriers the population group targeted by active case finding.
to accessing health services. Commonly used diagnostics – particularly direct
Among those that had sought health care, most did so microscopic examination of sputum smear samples –
within the public sector (Table 3.6). In a few countries need to be upgraded with better technology, including
(mostly in Asia), 30% or more of the symptomatic WHO-approved rapid diagnostics that are more sensitive
participants sought care in the private sector; examples and more specific than sputum microscopy.
included Bangladesh, Indonesia, Malawi, Myanmar
and the Philippines (in 2016). Pharmacies were also an
3.9 Conclusions
important point of care in a few countries, especially in
Asia. The observed proportion of cases treated in the The 25 national TB prevalence surveys implemented in
private health sector is a useful measure of the need for Africa and Asia between 2007 and 2016 provided a better
engagement of NTPs with the private sector. understanding of the national, regional and global burden
of TB disease, and of gaps in TB detection and treatment.
The surveys showed a much higher burden in men than
3.8 Diagnostic performance of smear women, an ageing epidemic in most of Asia and a peak
microscopy in prevalence in the younger age groups in most African
High proportions of false-positive results from direct countries. They also showed that actions are needed
microscopic examination of smears were observed in to improve access to health care and to ensure prompt
several surveys (Table 3.7). In these surveys, TB was diagnosis when care is sought, especially among men.
ruled out based on results from culture and Xpert MTB/ Repeat surveys in Asian countries have demonstrated that
RIF (or LPA), with false-positive results probably due to substantial reductions in the burden of TB disease can be
nontuberculous mycobacteria. achieved within 10 years, and all 25 surveys provide a
These findings provide evidence that sputum smear valuable baseline for future assessment of trends.
microscopy is also likely to be an unreliable diagnostic
test for TB in the context of active case finding, unless
50
Table 3.5
Health care seeking behaviour among participants who were symptom-screen positive
Country Participants No % Location of care sought
who were action
symptom- taken Consulted % Type of facility Phar- % Tradi- % Other % Unspec- % Self- % Un- %
screen medical macy tional ified treated known
Public % Private % Other %
positive facility
facility facility facility
Africa
Ethiopia 3026 1932 64% 848 28% 628 74% 199 23% 21 2.5% 40 1.3% 3 0.10% N/A N/A 55 1.8% N/A N/A 148 4.8%
Gambia 3462 1424 41% 1706 49% 1398 82% 220 13% 88 5.2% 17 0.49% 14 0.40% 24 0.69% N/A N/A N/A N/A 277 8.0%
Ghana 1969 264 13% 793 40% 695 88% 61 7.7% 37 4.7% 324 17% 20 1.0% N/A N/A N/A N/A 567 29% 1 0.10%
National TB prevalence surveys 2007–2016
a
Kenya 4137 2763 67% 1257 30% 1047 N/A 198 N/A 3 N/A 56 N/A 9 N/A N/A N/A N/A N/A N/A N/A 117 2.8%
Malawi 2715 1096 40% 1280 47% 901 70% 379 30% N/A N/A 32 1.2% 41 1.5% 4 0.15% N/A N/A 236 8.7% 26 0.96%
Nigeria 2466 604 24% 800 32% 628 79% 172 21% N/A N/A 319 13% 11 0.45% 9 0.36% 3 0.12% 680 28% 40 1.6%
Rwandaa 2855 1934 68% 921 32% 941 N/A 48 N/A 38 N/A 101 N/A 54 N/A N/A N/A N/A N/A 0 0 N/A N/A
Sudan 2663 575 22% 1308 49% 1077 82% 90 6.9% 141 11% 52 2.0% 49 1.8% N/A N/A 69 2.6% N/A N/A 610 23%
Uganda 2714 1059 39% 1201 44% 1038 86% 146 12% 17 1.4% 421 16% 11 0.41% N/A N/A N/A N/A 22 0.81% 0 0%
UR Tanzania 3388 1688 50% 481 14% 445 93% 36 7.5% N/A N/A 147 4.3% 11 0.32% 257 7.6% 155 4.6% N/A N/A 649 19%
Zambia 4453 2534 57% 1829 41% 1680 92% 75 4.1% 74 4.0% 16 0.36% 1 0.02% N/A N/A N/A N/A N/A N/A 73 1.6%
Zimbabwea 1833 1130 62% 486 26% 438 N/A 45 N/A N/A N/A 17 N/A 13 N/A N/A N/A N/A N/A N/A N/A 217 12%
Asia
Bangladeshb 26 882 12 48% 6545 24% 1816 28% 2182 33% 2547 39% 6533 24% 23 0.10% 191 0.71% N/A N/A 643 2.4% N/A N/A
947
Cambodia 1916 197 10% 1261 66% 947 75% 305 24% 9 0.71% 401 21% 21 1.10% 6 0.31% N/A N/A 28 1.5% 2 0.10%
China 5462 N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A
DPR Korea 2944 1192 41% 1743 N/A 1743 100% N/A N/A N/A N/A N/A N/A 3 0.10% N/A N/A N/A N/A 0 0% 6 0.20%
Indonesia 8552 3685 43% 2231 26% 1178 53% 672 30% 381 17% 2636 31% N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A
Lao PDR 3239 1210 37% 1148 35% 990 86% 106 9.2% 52 4.5% 690 21% 26 0.80% N/A N/A N/A N/A N/A N/A 165 5.1%
Mongolia 2546 1179 46% 950 37% 920 97% 30 3.1% N/A N/A 222 8.7% 2 0.08% 59 2.3% N/A N/A N/A N/A 30 1.2%
Myanmar 1691 440 26% 363 22% 197 54% 166 46% N/A N/A 271 16% 243 14% 39 2.3% N/A N/A 307 18% 28 1.7%
Pakistan 5417 N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A
Philippines N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A
(2007)c
Philippines 2815 1142 41% 530 N/A 359 67% 162 31% 9 1.7% 4 N/A 10 N/A N/A N/A N/A N/A 1130 N/A 18 0.64%
(2016)a
Thailandd 2283 N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A N/A
Viet Nam 4172 2248 54% 1228 29% 1029 84% 199 16% N/A N/A 671 16% 25 0.60% N/A N/A N/A N/A N/A N/A N/A N/A
DPR Korea, Democratic People’s Republic of Korea; Lao PDR, Lao People’s Democratic Republic; N/A, not applicable; UR Tanzania, United Republic of Tanzania.
a
a In Kenya, the Philippines (2016), Rwanda and Zimbabwe participants could select more than one category.
b
In Bangladesh, data on health care seeking behaviour were available for participants who reported at least one TB symptom (i.e. cough, haemoptysis, weight loss, fever, night sweats).
c
In Philippines (2007), there was no symptom screening and therefore no health seeking behaviour data obtained.
d
In Thailand, limited data were available and were not reported.
PART I: An overview of the 25 surveys implemented 2007–2016 51
Table 3.6
Location of treatment for participants who were on treatment at the time of the survey
Country Number of Public % Private % Other % Unknown Location of treatment
participants who were sector sector sector sector for participants who
on treatment at the were on treatment at
time of the survey the time of the survey
Africa
Ethiopia 75 54 72% 7 9.3% 3 4.0% 11 15%
Gambia 38 38 100% 0 0% 0 0% 0 0%
Ghana 48 42 88% 1 2.1% 5 10% 0 0%
Kenyaa 62 23 37% 0 0% 1 1.6% 38 61%
Malawia 12 10 83% 2 17% 0 0% 0 0%
Nigeria 82 56 68% 14 17% 5 6.1% 7 8.5%
Rwanda 21 – – – – – – – –
Sudan 104 69 66% 1 1.0% 4 3.8% 30 29%
Uganda 61 57 93% 4 6.6% 0 0% 0 0%
UR Tanzania 88 – – – – – – – –
Zambia 114 61 54% 1 0.9% 0 0% 52 46%
Zimbabwe 84 – – – – – – – –
Asia
Bangladesh 57 16 28% 10 18% 18 32% 13 23%
Cambodia 80 72 90% 6 7.5% 0 0% 2 2.5%
China 73 72 99% 0 0% 1 1.4% 0 0%
DPR Korea 106 101 95% 0 0% 0 0% 5 4.7%
Indonesia 125 68 54% 52 42% 5 4.0% 0 0%
Lao PDR 42 21 50% 0 0% 0 0% 21 50%
Mongolia 129 126 98% 0 0% 3 2.3% 0 0%
Myanmar 79 63 80% 14 18% 0 0% 2 2.5%
Pakistan 146 – – – – – – – –
Philippines – – – – – – – – –
(2007)
Philippines 170 134 79% 15 8.8% 24 14% 1 0.59%
(2016)b
Thailand 66 53 80% 3 4.5% 3 4.5% 7 11%
Viet Nam 64 46 72% 2 3.1% 0 0% 16 25%
DPR Korea, Democratic People’s Republic of Korea; Lao PDR, Lao People’s Democratic Republic; UR Tanzania, United Republic of Tanzania.
– no data were available.
a
In Kenya and Malawi, data were available only for participants who were eligible for sputum submission.
b
In the Philippines (2016), some participants identified more than one location.
52 National TB prevalence surveys 2007–2016
Table 3.7
Percentage of smear-positive results that were not confirmed TB.
Results shown for surveys in which specimens were tested using smear microscopy, rapid molecular tests and culture a
Country Number of participants with at least one Participants with smear-positive specimens
smear-positive specimen excluded as a TB case
Number %
Bangladesh 125 17 14%
Ghana 198 138 70%
Indonesia 291 126 43%
Kenya 141 18 13%
Malawi 163 101 62%
Mongolia 92 5 5.4%
Pakistan 236 29 12%
Philippines (2016) 183 10 5.5%
Sudan 61 4 6.6%
Uganda 91 25 27%
Zambia 356 221 62%
Zimbabwe 206 183 89%
a
Results are shown for surveys in which specimens were tested using smear microscopy and the systematic use of rapid molecular tests. All surveys used Xpert MTB/RIF except
Sudan which used line probe assay (LPA). Bangladesh and Kenya used both culture and Xpert MTB/RIF whereas other surveys used Xpert (or LPA) to confirm smear-positive
specimens only.
References 8. Horton KC, MacPherson P, Houben RM, White RG, Corbett EL.
Sex Differences in tuberculosis burden and notifications in low-
1. Hong YP, Kim SJ, Lew WJ, Lee EK, Han YC. The seventh
and middle-income countries: a systematic review and meta-
nationwide tuberculosis prevalence survey in Korea, 1995. Int J
analysis. PLoS Med 2016: 13: e1002119.
Tuberc Lung Dis. 1998;2(1):27–36 (https://www.ncbi.nlm.nih.
gov/pubmed/9562108, accessed 22 November 2019). 9. Ministry of Health – Republic of Indonesia, National Institute
of Health Research and Development. Indonesia tuberculosis
2. Mao TE, Okada K, Yamada N, Peou S, Ota M, Saint S et al. Cross-
prevalence survey 2013–2014. Jakarta, Indonesia: 2015.
sectional studies of tuberculosis prevalence in Cambodia between
2002 and 2011. Bull World Health Organ. 2014;92(8):573–81 10. Hoa NB, Cobelens FG, Sy DN, Nhung NV, Borgdorff MW, EW
(https://www.ncbi.nlm.nih.gov/pubmed/25177072, accessed 28 T. Diagnosis and treatment of tuberculosis in the private sector,
November 2019). Vietnam. Emerging infectious diseases. 2011;17(3):562–4
(https://www.ncbi.nlm.nih.gov/pubmed/21392464, accessed 28
3. Tupasi TE, Radhakrishna S, Chua JA, Mangubat NV, Guilatco
November 2019).
R, Galipot M et al. Significant decline in the tuberculosis burden
in the Philippines ten years after initiating DOTS. Int J Tuberc 11. World Health Organization. Assessing tuberculosis under-
Lung Dis. 2009;13(10):1224–30 (https://www.ncbi.nlm.nih.gov/ reporting through inventory studies. Geneva, Switzerland 2012
pubmed/19793426, accessed 28 November 2019). (https://www.who.int/tb/publications/inventory_studies/en/,
accessed 20 November 2019).
4. Wang L, Zhang H, Ruan Y, Chin DP, Xia Y, Cheng S et al.
Tuberculosis prevalence in China, 1990–2010; a longitudinal 12. Global tuberculosis report 2018. Geneva: World Health
analysis of national survey data. Lancet. 2014;383(9934):2057–64 Organization; 2018 (https://apps.who.int/iris/bitstream/han
(https://www.ncbi.nlm.nih.gov/pubmed/24650955, accessed 28 dle/10665/274453/9789241565646-eng.pdf?ua=1, accessed 1
November 2019). February 2020).
5. Global tuberculosis report 2017. Geneva: World Health
Organization; 2017 (http://apps.who.int/iris/bitstre
am/10665/259366/1/9789241565516-eng.pdf?ua=1, accessed 1
February 2020).
6. Global tuberculosis report 2019. Geneva: World Health
Organization; 2019 (https://apps.who.int/iris/bitstream/hand
le/10665/329368/9789241565714-eng.pdf, accessed 1 February
2020).
7. Borgdorff MW. New measurable indicator for tuberculosis case
detection. Emerg Infect Dis 2004: 10: 1523–1528.
53
Chapter 4
Chapter 3 provided an overview of the main results operations. Three countries completed repeat surveys
from the 25 national TB prevalence surveys completed that enabled assessment of trends in TB disease burden:
between 2007 and the end of 2016, including what they Cambodia, China and the Philippines.
showed about the distribution of TB disease by age and Most countries (19 of 25) also succeeded in achieving
sex. The overview also showed trends over time (for any a high participation rate (more than 80%). Nine countries
countries that completed repeat surveys) and discussed (Bangladesh, Cambodia, China, Ethiopia, Ghana, the
the implications of all results for policy, planning and Philippines in 2007, Rwanda, Uganda and Viet Nam)
programmatic action. managed to achieve participation rates of 90% or more,
In addition to the major success of producing valuable with an exceptionally high participation rate (96%) in
new data, this chapter highlights other aspects of survey China and Rwanda.
success. It also identifies the main challenges that were Other survey successes identified by multiple
faced during the process from deciding to implement countries included good data management (n=6), a
a survey through to finalizing and disseminating the strong laboratory (n=5), and timely finalization and
results. Lessons learned from both survey successes and dissemination of results (n=8). Surveys that described
challenges, which should be useful for informing future laboratory work as a “survey success” included those
surveys, are then summarized. in which the laboratory used was either part of a long-
For all three topics, this chapter synthesizes the more established research unit (e.g. Gambia) or a national
detailed assessments of successes, challenges and lessons reference laboratory. In the survey in Uganda, the
learned that are reported by those who led or contributed national reference laboratory was also a supranational
to each survey in the country-specific chapters (Part II) reference laboratory.
of this book. Survey successes mentioned by a single country were:
• the ability to generate subnational (provincial) as
4.1 Successes well as national estimates of prevalence (China,
Survey successes are summarized in Table 4.1. reflecting the survey’s very large sample size);
All surveys provided an up-to-date direct • full domestic funding for the survey (China);
measurement of the burden of TB disease, and other • capacity development for health care workers
valuable information about the status of the TB epidemic during the survey (Cambodia);
and access to care. This information was used to inform • smooth field operations (Cambodia);
national policy, national strategic plans, advocacy and • the enhancement of laboratory and operational
resource mobilization. Of the 25 surveys, 21 were in research capacity (Ghana); and
countries that completed either their first-ever national
TB prevalence survey (n=18) or the first survey to
• the opportunity to see challenges in case
management and surveillance in the most remote
include culture testing (n=3) according to the screening
areas of the country, often for the first time (Lao
and diagnostic algorithm recommended in the lime book
People’s Democratic Republic).
(1). In 2011, Ethiopia became the first African country
in decades to implement a national survey using this
algorithm; also impressive was the short time (about 4.2 Challenges
1 year) between the decision by Ethiopia’s Ministry The major challenges faced in surveys are summarized in
of Health to conduct a survey and the start of field Table 4.2, with the top five challenges shown in Fig. 4.1.
54
Table 4.1
Survey successes as reported by countries (see Part II for details)
Country First national Repeat Up-to-date direct measurement of TB Direct High Good data Strong Timely
survey completed national disease burden and other valuable measurement participation management b laboratory c finalization and
(ever or for many survey information about the status of the TB of trends in TB rate (>80%) dissemination
years)a completed epidemic and access to care provided disease burden of results d
Bangladesh ● ● ● ●
Cambodia ● ● ● ● ●
China ● ● ● ● ●
DPR Korea ● ● ●
National TB prevalence surveys 2007–2016
Ethiopia ● ● ●
Gambia ● ● ●
Ghana ● ● ● ●
Indonesia ● ● ●
Kenya ● ● ●
Lao PDR ● ● ●
Malawi ● ● ● ● ●
Mongolia ● ● ● ●
Myanmar ● ● ● ● ●
Nigeria ● ●
Pakistan ● ● ●
Philippines ● ● ● ●
(2007)
Philippines ● ● ● ●
(2016)
Rwanda ● ● ●
Sudan ● ● ●
Thailand ● ●
Uganda ● ● ● ● ● ●
UR Tanzania ● ●
Viet Nam ● ● ● ●
Zambia ● ● ● ● ●
Zimbabwe ● ● ● ●
a
The survey in Bangladesh was the first national survey that used the methods recommended in the lime book (1); the survey in Ethiopia was the first in the country as well as the first in decades in Africa that used culture; the
survey in Indonesia was the first for decades using both X-ray and culture; and the survey in Myanmar was the first in the country to use culture.
b
Countries that had a data management plan, had no major data issues in the field, and took <1 year to clean data after field operations were completed.
c
Countries that did not have have laboratory protocol violations and had high culture confirmation of smear-positive cases (≥85%).
d
Countries that did not have long delays before results were accepted by public health authorities, and provided an official report and/or paper within a few years of completing field operations.
Table 4.2
Major challenges faced in surveys as reported by countries (see Part II for details)
Country Time to secure Lengthy Security Gaps Internal Participation Overheating Data Laboratory Delays in Delays
funding or process issues between migration (≤80%)a or breakdown management work central reading in
funding to procure population affecting of X-ray (primarily of X-rays or writing
interruptions X-ray in national residential machines issues related difficulties the
during survey equipment and survey eligibility during field to culture in retaining survey
census criteria operations testing) radiologists report
Bangladesh ● ● ●
Cambodia ● ● ●
China ● ● ●
DPR Korea ● ● ●
Ethiopia ● ● ● ●
Gambia ● ● ●
Ghana ● ● ● ● ●
Indonesia ● ● ●
Kenya ● ● ●
Lao PDR ● ● ●
Malawi ● ● ● ● ●
Mongolia ●
Myanmar ● ● ● ● ●
Nigeria ● ● ● ● ●
Pakistan ● ● ●
Philippines ● ●
(2007)
Philippines ● ● ●
(2016)
Rwanda ● ● ●
Sudan ● ● ● ●
Thailand ● ● ●
Uganda ● ●
UR Tanzania ● ● ● ●
Viet Nam ●
Zambia
Zimbabwe ● ● ●
a
In addition, many countries reported challenges with participation in at least one of the following subcategories: the first survey clusters, younger age groups, men and urban (especially wealthier) areas.
● yes
PART I: An overview of the 25 surveys implemented 2007–2016
55
56 National TB prevalence surveys 2007–2016
Fig. 4.1
Top five challenges in 25 surveys as reported by countries
The top challenge, identified by 16 countries, was • use of sputum cups that were suboptimal for
laboratory-related work (primarily issues related to culture testing (Myanmar);
culture testing). Examples of such challenges included: • security issues in the part of the country where
• potential cross-contamination of samples during the national reference laboratory was located,
transportation from the field to the laboratory (e.g. which limited monitoring and technical assistance
Bangladesh and Malawi); (Nigeria); and
• a need to rely on only two laboratories owing to • difficulties maintaining a cold chain, especially in
difficulties in standardizing laboratory work hot or heatwave conditions (e.g. Pakistan and the
(Cambodia); Philippines).
• the difficulty of standardizing techniques when Despite these issues, in 15 of 16 countries, the number
multiple laboratories were used (e.g. China and the of culture-confirmed survey cases was considerably
Philippines); higher than the number of survey cases that were smear
• a lower yield than expected from culture specimens positive, as expected. The exception was the United
(e.g. China, Pakistan, Rwanda and the United Republic of Tanzania, for which it was concluded that
Republic of Tanzania); culture results could not be used (and hence the results in
this book are restricted to smear-positive cases).
• backlogs and delays in culture inoculation, linked
to the high volume of specimens (e.g. Sudan and The second most frequent challenge, identified by
the United Republic of Tanzania); 11 countries, was data management. Examples of such
challenges included:
• testing of only one specimen (instead of the
recommended number of two) using culture in • slow data entry (e.g. Cambodia, the Democratic
some (e.g. Indonesia) or all (e.g. Ethiopia) clusters People’s Republic of Korea and Nigeria);
owing to limited laboratory capacity; • use of software designed for a national census that
• the time required to establish the laboratory was not suited to a prevalence survey (e.g. Ethiopia);
capacity needed for culture testing (e.g. this took 2 • overreliance on internet connectivity in the field
years in Lao People’s Democratic Republic); for electronic data entry (Kenya and Sudan), which
was later resolved through use of a local area
PART I: An overview of the 25 surveys implemented 2007–2016 57
Table 4.3
Lessons learned for future surveys as reported by countries (see Part II for details)
1
Further discussion of the role of molecular tests in addressing challenges
with culture testing in prevalence surveys is included in Chapter 5.
60
Transporting chest X-ray equipment during the 2016 national TB prevalence survey of the Philippines.
Photo credit: Raldy Benavente / FACE Inc (Philippines)
61
Chapter 5
Future direction
The introductory chapter of this book highlighted that As illustrated in Chapter 3 and in the country-specific
national notification and vital registration systems can chapters that form Part II of this book, a substantial new
be used to reliably monitor the burden of TB disease (in body of knowledge was generated by the 25 surveys
terms of numbers of cases and deaths each year) in many completed in 24 countries1 (including 18 of the 22
high-income countries, with a few countries having time GFCs) between 2007 and 2016. Data were used to update
series of data that cover a span of more than 100 years. estimates of TB disease burden, including time trends in
It also highlighted that while the ultimate goal is that the three countries that conducted repeat surveys, and to
all countries can reliably track their TB epidemics using inform national policy, national strategic plans, advocacy
such systems, in the early 2000s this goal had not been and resource mobilization. Chapter 4 then synthesized
achieved in many countries with a high burden of TB. survey successes (including and beyond the generation
Although all countries (including high TB burden and use of survey data), challenges and lessons learned
countries) had national notification systems for TB and during the time between the initial decision to implement
were reporting notification data to WHO on an annual a survey and dissemination of results, based on the more
basis, in most countries the number of notified cases was detailed descriptions provided in Part II.
not a good proxy for the actual number of new cases. This Looking forward, and building on Chapter 3 and
was due to a mixture of underreporting of detected cases, Chapter 4, this final chapter of Part I addresses three
duplicated case reporting, some level of overdiagnosis of important questions:
bacteriologically unconfirmed cases and underdiagnosis.
• Are national TB prevalence surveys still relevant?
National VR systems of high quality and coverage had yet
to be established in many parts of the world. • Where do national TB prevalence surveys remain
relevant?
This situation was the reason for the establishment of
the WHO Global Task Force on TB Impact Measurement • Should national TB prevalence surveys be done
in 2006. The task force had the aim of ensuring a robust, differently in future?
rigorous and consensus-based assessment of whether TB
targets set for 2015 in the UN MDGs and the WHO Stop 5.1 Are national TB prevalence surveys still
TB Strategy were achieved. It included national surveys of relevant?
the prevalence of TB disease in 22 global focus countries
In 2013, WHO published a TB surveillance checklist of
(GFCs) as one of its three strategic areas of work during
standards and benchmarks that can be used to assess
the period 2007–2015 (1). Such surveys were recognized
the quality and coverage of national notification and VR
as providing an alternative way of directly and reliably
systems (2). Although much progress in strengthening
measuring the burden of TB disease, with repeat surveys
national TB notification systems was made between 2007
allowing assessment of trends. Other recognized benefits
and 2016, at the end of this period, most countries with a
of surveys were that they could be used to document the
high burden of TB still lacked systems that met the levels
distribution of disease by age and sex; to better understand
of quality and coverage necessary for notification data to
health care seeking behaviour in the public and private
provide a direct measure of TB incidence (3). In WHO’s
sectors; to identify reasons why people with TB were not
Global tuberculosis report 2019, the data used to estimate
diagnosed before the survey or officially reported to national
TB incidence in high TB burden countries were sourced
authorities (or both); and to inform the development or
mainly from national TB prevalence surveys (4). In the
improvement of strategies and interventions for TB case
finding, diagnosis and treatment. 1
Two surveys were implemented in the Philippines (2007 and 2016).
62 National TB prevalence surveys 2007–2016
Table 5.1
Suggested epidemiological criteria for assessing whether a country should consider implementing a prevalence survey post-2016 for
two major groups of countries, as discussed by the WHO Global Task Force on TB Impact Measurement in April 2016
Criteria Explanation
Group 1 → Countries that conducted a national prevalence survey in 2007–2016a (Fig. 5.1)
1. Estimated prevalence of bacteriologically • Sample size small enough (<70 000 individuals) to make surveys feasible in
confirmed TB ≥250 per 100 000 population terms of cost and logistics.
aged ≥15 years during the previous survey.
and
2. More than 7 years since the last survey.a • Time between surveys sufficient to allow a statistically meaningful comparison
of prevalence.
Group 2 → Countries that did not implement a national prevalence survey in 2007–2016 (Fig. 5.2)
1. Estimated TB incidenceb ≥150 per 100 000 • Sample sizeb small enough (<70 000 individuals) to make surveys feasible in
population per year (all forms, all ages). terms of cost and logistics, taking into account added uncertainty due to the
and use of rapid molecular tests with performance that may be inferior to culture.
2. No nationwide VR system with standard coding • No reliable direct measurement of TB disease burden.
of causes of deaths.
and
3. Infant mortality rate >10/1000 live births. • Indirect indicator of low access to quality health services, as defined in the
WHO checklist of standards and benchmarks for TB surveillance and VR.
VR: vital registration; WHO: World Health Organization.
a
Surveys conducted before 2000 may lack comparability with surveys implemented according to the screening and diagnostic algorithm recommended in the lime book (8).
An interval of about 7–10 years between two surveys is recommended.
b
Country-specific prevalence estimates have not been published by WHO post-2016 because prevalence is not a high-level indicator of the End TB Strategy. For sample size
calculations, prevalence in the age group 15 years or more may be predicted from incidence.
same report, estimates of TB mortality were based on which was defined as “Priority studies to periodically
national VR data for 123 countries (including nine of the measure TB disease burden”. The task force meeting was
30 included in WHO’s list of high TB burden countries). also used to discuss the countries in which national TB
Given this situation, the rationale for using national prevalence surveys remained relevant. The suggested
TB prevalence surveys as an alternative way to directly epidemiological criteria for assessing whether a country
measure the burden of TB disease and trends remained should consider implementing a survey are shown in
as valid at the end of 2016 as it was in 2007. Table 5.1, and the countries in each of the two groups
defined in Table 5.1 (based on data available at the end of
2019) are shown in Fig. 5.1 and Fig. 5.2.
5.2 Where do national TB prevalence surveys
remain relevant? Among the 24 countries in Group 1 (i.e. those that
implemented a survey in 2007–2016 and that met the
In April 2016, the WHO Global Task Force on TB Impact
criteria shown in Table 5.1), it is worth highlighting that
Measurement held a meeting to discuss progress achieved
five did not meet the criteria for a further survey because
during the period 2007–2015, and its work in the post-
of their relatively low measured level of TB disease
2015 era of the UN Sustainable Development Goals
burden; these countries were China, Gambia, Rwanda,
(SDGs, which succeeded the MDGs) and WHO’s End
Sudan and Thailand. In these countries, the focus should
TB Strategy (which succeeded the Stop TB Strategy) (5).
be on maintaining or strengthening national notification
The SDGs, set for 2030, were adopted by all UN Member
and VR systems.
States in September 2015 (6). The End TB Strategy was
adopted by all WHO Member States at the World Health Of the 29 countries in Group 2, four stood out in
Assembly in 2014; it covers the period 2016–2035, with terms of their share of estimated TB disease burden
milestones for 2020 and 2025 and targets for 2030 and from a global perspective: Democratic Republic of the
2035 (7). Congo, India, Mozambique and South Africa. Of these,
South Africa completed a survey in 2019, Mozambique
During its April 2016 meeting, the task force agreed
completed one in 2020 and India started a survey in 2019.
on an updated mission and five strategic areas of work,
In addition, surveys were completed in Namibia (2018),
initially for the period 2016–2020 (likely to apply and be
Nepal (2019) and Lesotho (2019), and planning for a
extended to 2021–2025). National TB prevalence surveys
survey in Botswana was initiated in 2018.
were retained under the new third strategic area of work,
PART I: An overview of the 25 surveys implemented 2007–2016 63
Fig. 5.1
Countries that conducted a national TB prevalence survey in 2007–2016 and that met the Group 1 criteria based on data available at the
end of 2019 (N=19, red) a
Fig. 5.2
Countries that met the Group 2 criteria for implementing a national TB prevalence survey based on data available at the end of 2019 a
Countries that had already completed or started implementation of a survey by the end of 2019 are shown in blue and remaining countries
are shown in red.
Fig. 5.3
Percentage of people who were eligible for sputum testing (i.e. they reported symptoms suggestive of TB or had an abnormal chest
X-ray) that had culture confirmed pulmonary TB, for surveys implemented in 2007–2016
Recognizing the limitations of both culture and Xpert accurate. To facilitate their use, roles and responsibilities
testing in the context of a national TB prevalence survey, are defined as follows:
WHO organized meetings between 2018 and 2020 to • The sponsor or sponsors provide the financing for
discuss the best way forward, based on accumulating a survey. Examples include external agencies (e.g.
evidence from surveys in which Xpert and culture were the Global Fund to Fight AIDS, Tuberculosis and
used alongside each other. As of early 2020, one option Malaria, development agencies or the national
under consideration for countries without the capacity government) and may include a mixture of
to conduct high-quality culture testing in the context of agencies. Sponsors can request regular reports
a national prevalence survey was as follows: the use of from survey implementing agencies, and reports
two Xpert Ultra tests on two separate sputum samples may be linked to periodic release of funds.
for all participants who screen positive (to maximize
• The principal investigator represents all survey
sensitivity), followed by culture testing for any participant
investigators. That person is responsible for
with an Xpert Ultra positive test result (thus addressing
leading the development of the protocol and
the suboptimal specificity of Xpert Ultra by using the
standard operating procedures (SOPs) and for
reference standard as a confirmatory test to eliminate
ensuring review. The principal investigator is
false-positive Xpert Ultra results). Prevalence estimates
also responsible for the recruitment of competent
would then need to be adjusted to account for the lower
staff, and leads the writing of the final report and
sensitivity of the Xpert Ultra test (i.e. adjustment for
scientific papers.
false-negative Xpert Ultra results).
• Investigators contribute to survey design (including
A final set of recommendations related to the diagnostic
the development of a protocol and SOPs, and
algorithm to be used in future surveys, designed to make
ethics review and approval), implementation of
optimal use of both culture and Xpert, is planned for
field operations including quality control, analysis
publication in a new edition of the WHO handbook on
of results and preparation of a survey report.
prevalence surveys that will succeed the lime book.1
During field operations, this includes ensuring the
accuracy, completeness, legibility and timeliness
5.3.2 Adapting and using the principles of good of the data reported in data collection tools. Data
clinical practice that have been established for that are derived from source documents should
clinical trials in the context of national TB be consistent with the source documents; if this
prevalence surveys is not the case, discrepancies should be explained.
To achieve maximum data quality, a standard
Good clinical practice (GCP) is a set of internationally
set of quality assurance procedures2 should be
recognized ethical and scientific quality requirements that
in place. These include checking that batches of
must be followed when designing, conducting, recording
newly entered records are consistent with defined
and reporting clinical trials that involve people (14). They
standards.
have been used in the context of drug development in
particular. • Survey monitors assess the implementation of
survey operations, including checking protocol
Adapting GCP principles to the context of a national
modifications and checking for protocol violations.
TB prevalence survey could help to prevent or mitigate
They may conduct batch checks of data. They
challenges related to data management. They could also
advise investigators about their findings and
contribute to enhancing survey quality more broadly,
provide recommendations for corrective actions if
by strengthening oversight, monitoring processes and
needed. They also report to an independent data
ensuring that any recommendations are implemented
monitoring committee (or board) and may assist
in a timely way. An independent evaluation of national
the principal investigator to prepare the final
TB prevalence surveys conducted in 2015 included a
recommendation to explore the relevance of GCP to
future national TB prevalence surveys (5). 1
At the time of writing, this was planned for publication in 2021.
GCP requirements are designed to ensure two things: 2
Quality assurance is a process of systematic activities designed to
the protection of the rights, safety and well-being of ensure, assess and confirm the quality of the data collected during
a survey. Quality-assured data are those that are suitable for their
all participants; and that data are comprehensive and intended purpose in terms of their accuracy, timeliness, accessibility
and comparability between database and source documents.
68 National TB prevalence surveys 2007–2016
report. In the context of GCP, study monitors • use of multiple paper-based forms for the same
represent the sponsor. individual should be avoided.
• An independent data monitoring committee (or
board) may be established by the sponsor to assess 5.3.3 Invest more resources in the work required
the progress of the survey at regular intervals once results are finalized, especially to ensure
(based on reports from survey monitors) and to
the timely production of survey reports
provide recommendations to the sponsor about
and effective communication of findings and
whether to continue, modify or stop the survey.
their implications
The first three of these elements were present in
In 10 of the 25 surveys implemented in 2007–2016,
all national TB prevalence surveys implemented in
producing the final survey report took a considerable
2007–2016. Survey monitoring by external experts (the
amount of time (more than 1 year in 8 countries). The
fourth element) was also commonly in place, provided
presence of a permanent full-time survey monitor (in
by staff of international agencies or by people who had
line with GCP) could help to address this challenge, since
held senior roles in previous surveys in other countries
one of that person’s responsibilities would be to provide
(via the Asia–Asia, Asia–Africa and Africa–Africa
regular reports with material that could subsequently
collaboration highlighted in Chapter 4). However, a
be used in the final survey report. More generally, more
formal and independent data monitoring committee was
resources for report writing (people with the right skills
not established for any of the surveys (although many had
and time, and funding for production costs including
oversight from a survey committee, expert advisory group
editing and printing) need to be committed when a
or equivalent). It was also the case that there was not
survey budget is first developed and approved.
necessarily any obligation for investigators to implement
all of the recommendations made by external experts. Experience in several countries also highlighted
the importance of good communication of results to
WHO initiated the development of guidance on the
key decision-makers (e.g. planners, policy-makers and
adaptation and use of GCP and good data management
those with responsibility for communicable diseases in
practices (GDMP) within the context of national
the ministry of health). During discussions, emphasis
population-based surveys of TB disease (including
should be given to survey validity; quality assurance
national TB prevalence surveys) and health facility based
procedures; monitoring (including external monitoring);
surveys in 2019, in collaboration with WHO/TDR – the
and how survey findings provide valuable information
WHO Special Programme for Research and Training in
for decision-making on policies, prioritization and future
Tropical Diseases, which has conducted extensive training
budgeting for TB control. When to engage with national
in the application of GCP in clinical trials. The final
and local media also needs careful thought.
document will provide guidance on how to implement
the key GCP/GDMP principles to maximize data The last chapter of the lime book (8), on “Analysis
credibility (i.e. comprehensive and accurate data collected and reporting”, focused on best-practice methods for
in an ethical manner) within the scope of population- the analysis of survey data and how to present results.1
based surveys and health facility based surveys. The book did not include a subsequent chapter on the
production of a survey report and communication of
Other challenges related to data management can
results. Such additional guidance will be part of the next
be addressed using the lessons learned from previous
WHO edition of this handbook.
surveys (documented in Chapter 4). Examples of lessons
learned are that:
• a competent and responsive data management team References
is essential, and this team should be involved from 1. Global tuberculosis report 2015. Geneva: World Health
Organization; 2015 (https://apps.who.int/iris/bitstream/
the initial stages of survey preparations through to handle/10665/191102/9789241565059_eng.pdf, accessed 8
completion of data analysis and report writing; January 2020).
• electronic data capture systems in the field and 2. WHO. Standards and Benchmarks for tuberculosis surveillance
and vital registration systems. WHO, 2014 http://apps.who.int/
laboratories can significantly facilitate and increase iris/bitstream/10665/112673/1/9789241506724_eng.pdf?ua=1.
the efficiency of data collection, validation and
analysis; and
1
This guidance was subsequently updated and published in a journal
article by Floyd et al. (2013) (15).
PART I: An overview of the 25 surveys implemented 2007–2016 69
PART II
BANGLADESH
2015–2016
Summary statistics
Participation rate 91%
Symptom screening
Cough ≥2 weeks 6 467 (6.6%)
Cough <2 weeks 12 909 (13%)
Haemoptysis in the past month 472 (0.5%)
Weight loss in the past month 3 615 (3.7%)
Fever ≥1 week in the past month 7 546 (7.6%)
Night sweats in the past month 3 819 (3.9%)
Score ≥3 pointsa 7 260 (7.4%)
Score 1 or 2 with chest X-ray exempteda 34 (0.03%)
Total symptom-screen positivea 7 294 (7.4%)
Eligible for sputum examination 20 594 (21%) Symptom positive, chest X-ray positive 3 077 (15%)
Symptom positive, chest X-ray negative or N/A 4 217 (20%)
Symptom negative, chest X-ray positive 13 300 (65%)
Other N/A
Submitted specimens
At least one specimen 20 463 (99%)
Both specimens 20 010 (97%)
Laboratory result
At least one culture result availableb 20 378 (99%)
At least one Xpert result available 20 425 (99%)
Total bacteriologically confirmed cases 278 Symptom positive, chest X-ray positive 79 (28%)
Symptom positive, chest X-ray negative or N/A 27 (9.7%)
Symptom negative, chest X-ray positive 172 (62%)
Other N/A
a
Eligible for sputum collection.
b
Cultures that were either contaminated and/or missing without a definitive result (i.e. MTB, NTM, negative) were excluded.
c
Definite: MTB confirmed by culture and/or Xpert. Probable: no definition.
76 National TB prevalence surveys 2007–2016
Fig. 1: Participation rate by age and sex Fig. 4: Cluster variation of the number of bacteriologically
confirmed TB casesb
100
30
Participation rate (%)
25
Number of clusters
20
90
15
10
80 0
15–24 25–34 35–44 45–54 55–64 ≥65 0 1 2 3 4 5 6 7 8 9
Age group (years) Number of bacteriologically confirmed TB cases
Male Female
Fig. 2: TB prevalence per 100 000 population by age Fig. 5: Ratio of bacteriologically confirmed TB prevalence to
notifications by age and by sexc
1200 5.0
Prevalence per 100 000 population
800 3.5
3.0
600 2.5
2.0
400
1.5
200 1.0
0.5
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 15–24 25–34 35–44 45–54 55–64 ≥65 Male Female Total
Age group (years) Age group (years) and sex (≥15)
Bacteriologically confirmed TB Smear-positive TB
Fig. 3: Estimated number of bacteriologically confirmed TB cases Fig. 6: Estimates of TB prevalence (all ages, all forms of TB) before
and prevalence per 100 000 population, by agea (in blue) and after (in red) the national TB prevalence surveyd
90 000 1200
Estimated number of bacteriologically
80 000
1000
70 000
confirmed TB cases
60 000 800
50 000
600
40 000
30 000 400
20 000
200
10 000
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 200 300 400 500 600
Age group (years) Prevalence per 100 000 population
a
The estimated number of bacteriologically confirmed TB cases is the product of age-specific prevalence per 100 000 population and population estimates from the UN Population Division
(2015 revision).
b
The data suggest that the distribution of cases by cluster (blue bars) is significantly different from the theoretical distribution (red line) (mean 2.22, variance 3.63, p<0.05). The
theoretical distribution assumes cases are distributed at random i.e. no clustering effect.
c
Notification rates were estimated using notifications of bacteriologically confirmed pulmonary TB (2015) obtained from the NTP, and population estimates from the UN Population Division
(2015 revision).
d
The blue bar denotes the best estimate of prevalence and its range that was indirectly derived from the estimate of incidence previously published by WHO, adjusted to the year of the
prevalence survey based on previously published trends in incidence.
BANGLADESH 77
Background The notification rate increased from 45 per 100 000 popu-
lation in 1990 to 102 per 100 000 population in 2010 (7).
Bangladesh’s population was 161 million in 2015. It was WHO estimated incidence to be 227 (95% CI: 200–256)
one of the 22 high tuberculosis (TB) burden countries per 100 000 population and prevalence to be 404 (95%
(HBCs) defined by WHO as a top priority for global efforts CI: 211–659) per 100 000 population in 2014. The case
in TB control in 1998 and throughout the Millennium detection rate was 53% (95% CI: 47–60) in 2014 (8).
Development Goal (MDG) era (2000–2015), and one of
the top 30 HBCs defined by WHO for the period 2016– Bangladesh carried out national TB prevalence surveys
2020. In 2015, Bangladesh was a lower-middle-income in 1964–1966, in 1987–1988 and in 2007–2009 (9–11). In
country with an average gross national income (GNI) contrast to the methodology recommended by the WHO
per person of US$ 1190 per year (1). The prevalence of Global Task Force on TB Impact Measurement, the 2007–
HIV in the general population aged 15–49 years was 2009 survey was based on “smear from everybody”; that
<0.1% (95% confidence interval [CI]: <0.1–<0.1%) (2), is, without screening, sputum samples were collected
and it was estimated that 0.1% (95% CI: 0.08–0.2%) of TB from every eligible participant for smear examinations
patients were coinfected with HIV (3). (and a subsequent chest X-ray was taken if a smear was
positive). Adjusted smear-positive TB prevalence in those
In Bangladesh in the 1960s and 1970s, TB services were aged 15 years or more in the 2007–2009 survey was 79
based in TB clinics or hospitals, and then expanded to (95% CI: 47–134) per 100 000 population.
124 upazila health complexes (UHCs) between 1980 and
1986 (the period of the second health and population In December 2007, Bangladesh was one of the 22 global
plan). During the third health and population plan (1986– focus countries for a national TB prevalence survey
1991), TB services were integrated with leprosy under the selected by the WHO Global Task Force on TB Impact
Mycobacterial Disease Control unit of the Directorate Measurement. Recognizing that a new prevalence survey
General of Health Services (DGHS). The National – carried out in accordance with recommended methods
TB Control Programme (NTP) adopted the WHO- – was needed to understand the current TB burden (12)
recommended DOTS strategy during the fourth health and to measure the impact of the NTP, the Ministry of
and population plan (1992–1998); it was implemented in Health decided in 2012 to implement a fourth national
four upazilas in November 1993 and expanded to cover TB prevalence survey. Field operations were conducted
all upazilas by mid-1998 (4-6). from March 2015 to April 2016.
Key methods and results the smear-positive cases, 48% were symptom-
screen positive;
There were 125 survey clusters in two strata (urban and • for smear-positive pulmonary TB, the ratio of
rural), with a target cluster size of 800 individuals. A prevalence to notifications (P:N ratio) was 2.8
total of 148 126 individuals from 9594 households were overall, but varied from 1.9 in those aged 55–64
enumerated in the survey census, of whom 108 834 (73%) years to 4.3 in those aged 65 years or more, and
was higher for men than women (3.6 versus 1.9);
were eligible and invited to participate. Of these, 98 710
• among the bacteriologically confirmed TB
(91%) did so. All participants were screened according
cases, 90% had no previous history of anti-
to the 2011 algorithm recommended by WHO; that is, TB treatment and only 3.2% were on anti-TB
using a chest X-ray and an interview about symptoms treatment at the time of the survey; and
(12). A total of 20 594 participants (21%) were eligible for • of the 101 bacteriologically confirmed and 48
sputum examination; of these, 20 463 (99%) submitted at smear-positive TB survey cases that screened
least one sputum specimen and 20 010 (97%) submitted positive for symptoms and were not on anti-TB
two sputum specimens. treatment at the time of the survey, 32 (32%) and
15 (31%), respectively, had previously sought
Sputum from 20 425 participants was tested with Xpert® care in a public or private health facility for their
MTB/RIF. Of these participants, 269 (1.3%) were positive symptoms.
for Mycobacterium tuberculosis (MTB); of these, 12
(4.4%) were also rifampicin (RIF) resistant, 231 (86%)
were RIF sensitive and 26 (9.6%) were indeterminate.
Due to potential cross-contamination, 13 Xpert-positive
results were annulled.
CAMBODIA
2010–2011
Summary statistics
Participation rate 93%
Key people
Name Role Organization
Mao Tan Eang Chairman National Centre for TB and Leprosy Control (CENAT)
Peou Satha Survey coordinator/chief of radiology CENAT
Pheng Sok Heng Chief of laboratory CENAT
Koy Bonamy Chief of census CENAT
Tieng Sivanna Chief of statistics CENAT
Kouet Pichenda Field team leader CENAT
Keo Sokonth Field team leader CENAT
Saint Saly Field team leader CENAT
Chea Manith Field team leader CENAT
Kosuke Okada Supervisor (project leader) Research Institute of Tuberculosis/Japan Anti-Tuberculosis Association (RIT/JATA)
Norio Yamada Supervisor (epidemiology/statistics) RIT/JATA
Masaki Ota Supervisor (epidemiology/data management) RIT/JATA
Takashi Yoshiyama Supervisor (chest X-ray examination (diagnosis)) RIT/JATA
Kunihiko Ito Supervisor (chest X-ray examination (diagnosis)) RIT/JATA
Hiroyuki Nishiyama Supervisor (chest X-ray examination (diagnosis)) RIT/JATA
Yutaka Hoshino Supervisor (chest X-ray examination (film shooting)) RIT/JATA
Hiroko Matsumoto Supervisor (bacteriological examination (quality assurance)) RIT/JATA
Tetsuhito Sugamoto Supervisor (bacteriological examination (culture, identification RIT/JATA
and DST))
Kiyomi Yamamoto Coordinator/data management RIT/JATA
Ikushi Onozaki Technical assistance (survey advisor) WHO headquarters
Rajendra Yadav Technical assistance (survey advisor) WHO Cambodia
Emily Bloss Technical assistance (survey advisor) US Centers for Disease Control and Prevention (CDC)
Sara Whitehead Technical assistance (survey advisor) US Centers for Disease Control and Prevention (CDC)
Philippe Glaziou Technical assistance (statistics) WHO headquarters
Charalampos Sismanidis Technical assistance (analysis) WHO headquarters
Sian Floyd Technical assistance (analysis) London School of Hygiene & Tropical Medicine
Symptom screening
Cough ≥2 weeksa 1 804 (4.8%)
Haemoptysisa 319 (0.9%)
Sputum production 15 698 (42%)
Chest pain 11 405 (31%)
Fever 17 811 (48%)
Total symptom-screen positivea 1 916 (5.1%)
Eligible for sputum examination 4 780 (13%) Symptom positive, chest X-ray positive 710 (15%)
Symptom positive, chest X-ray negative or N/A 1 206 (25%)
Symptom negative, chest X-ray positive 2 699 (57%)
Otherb 165 (3.5%)
Submitted specimens
At least one specimen 4 612 (97%)
Both specimens 4 598 (96%)
Laboratory result
At least one culture result availablec 4 602 (98%)
Total bacteriologically confirmed cases 314 Symptom positive, chest X-ray positive 88 (28%)
Symptom positive, chest X-ray negative or N/A 5 (1.6%)
Symptom negative, chest X-ray positive 218 (69%)
Otherb 3 (1.0%)
a
Eligible for sputum collection.
b
Chest X-ray exempted and symptom-screen negative, and other.
c
Cultures that were either contaminated and/or missing without a definitive result (i.e. MTB, NTM, negative) were excluded.
d
Definite: MTB confirmed by culture. Probable: MTB not confirmed by culture but two smear-positive slides, or one smear-positive slide with chest X-ray suggestive of TB.
e
Definite: MTB confirmed by culture. Probable: culture-positive (but MTB not confirmed) and chest X-ray suggestive of TB.
84 National TB prevalence surveys 2007–2016
Fig. 1: Participation rate by age and sex Fig. 4: Cluster variation of the number of bacteriologically
confirmed TB casesb
100 12
10
Participation rate (%)
Number of clusters
8
90 6
80 0
15–24 25–34 35–44 45–54 55–64 ≥65 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14
Age group (years) Number of bacteriologically confirmed TB cases
Male Female
Fig. 2: TB prevalence per 100 000 population by age Fig. 5: Ratio of smear-positive TB prevalence to notifications by
age and by sexc
4000 2.5
Prevalence per 100 000 population
2500 1.5
2000
1500 1.0
1000
0.5
500
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 15–24 25–34 35–44 45–54 55–64 ≥65 Male Female Total
Age group (years) Age group (years) and sex (≥15)
Bacteriologically confirmed TB Smear-positive TB
Fig. 3: Estimated number of bacteriologically confirmed TB cases Fig. 6: Estimates of TB prevalence (all ages, all forms of TB) before
and prevalence per 100 000 population, by agea (in blue) and after (in red) the national TB prevalence surveyd
18 000 3500
Estimated number of bacteriologically
16 000
3000
14 000
2500
confirmed TB cases
12 000
10 000 2000
8 000 1500
6 000
1000
4 000
2 000 500
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 500 700 900 1100
Age group (years) Prevalence per 100 000 population
a
The estimated number of bacteriologically confirmed TB cases is the product of age-specific prevalence and population estimates from the UN Population Division (2015 revision).
b
The data suggest that the distribution of cases by cluster (blue bars) was significantly different from the theoretical distribution (red line) (mean 5.06, variance 11.0, p<0.05). The
theoretical distribution assumes cases are distributed at random i.e. no clustering effect.
c
Notification rates were estimate of using notifications obtained from the WHO global TB database, and population estimates from the UN Population Division (2015 revision).
d
The blue bar denotes the best estimated prevalence and its range that was indirectly derived from the estimate of incidence previously published by WHO, adjusted to the year of the
prevalence survey based on previously published trends in incidence.
CAMBODIA 85
Background was 1208 (95% CI: 997–1463) per 100 000 population.
The notification rate of new smear-positive TB cases
Cambodia’s population was 15 million in 2011, and peaked in 2005, and subsequently stagnated for 3 years.
the average gross national income (GNI) per person
was US$ 810 per year, making it a low-income country In December 2007, Cambodia was selected by the WHO
(1). It was one of the 22 high tuberculosis (TB) burden Global Task Force on TB Impact Measurement as one
countries (HBCs) defined by WHO as a top priority of 22 global focus countries to undertake a national TB
for global efforts in TB control in 1998 and throughout prevalence survey. The aim was to better understand the
the Millennium Development Goal (MDG) era (2000– burden of TB disease at national and global levels, and to
2015), and one of the top 30 HBCs defined by WHO for assess trends in countries with a baseline survey. A second
the period 2016–2020. In 2011, the prevalence of HIV national TB prevalence survey was needed to obtain an
in the general population aged 15–49 years was 0.8% up-to-date measurement of the burden of TB disease and
(95% confidence interval [CI]: 0.7–0.9%) (2), and it was to assess trends since the 2002 survey. Planning for this
estimated that 5.1% (95% CI: 4.6–5.6%) of TB patients second survey started in September 2009, and the survey
were coinfected with HIV (3). was implemented in 2010–2011 (8).
1
The original report is in the Khmer language; excerpts have been translated 2
In the 2002 survey, four provinces (Mondulkiri, Rattanakiri, Preah Vihear and
by the Documentation Center of Cambodia for the Cambodian Genocide Steung Treng) were excluded because of serious difficulties in accessing these
Program. provinces and their relatively small population (<3% at that time). In the 2010
survey, for the purposes of comparisons between the two surveys, these four
provinces were grouped into a stratum separate from the areas covered in the
2002 survey.
86 National TB prevalence surveys 2007–2016
asymptomatic TB cases (38%). By 2011, symptomatic Major successes, challenges and lessons
smear-positive TB cases accounted for 44% of all cases. learned
Only 23% of people with smear-negative, culture-positive
TB met the 2011 NTP definition of an individual with Major successes included smooth survey operations
presumptive TB. conducted in a highly transparent manner, a high
participation rate, capacity development of health workers
This evolution in the TB epidemic had two major at the central and local level, and rapid dissemination of
programmatic implications. The first was a need to key results at a large dissemination event (in February
strengthen diagnostic capacity for outpatients with 2012, within 5 months of the completion of field
respiratory symptoms, by reviewing and updating the operations). Funding was mobilized from several sources
diagnostic algorithm which had previously relied heavily (JICA, the Global Fund and USAID) and was efficiently
on smear microscopy. Suggested updates included more managed. After the survey, staff and equipment (e.g.
extensive use of chest X-ray for people with any respiratory chest X-ray machines) deployed for the survey were used
symptom, including a referral system for people with to undertake active case finding in specific geographical
smear-negative presumptive TB to a health facility hotspots identified by the survey and in specific
equipped to carry out chest X-rays, and the replacement subpopulations (e.g. the elderly).
of smear microscopy with more sensitive diagnostic tools,
such as Xpert® MTB/RIF. The second implication was that Challenges were limited, but included a need to rely
active case detection activities should be expanded to on two laboratories, given issues with standardizing
specific groups with a high prevalence of TB, such as the laboratory work in other parts of country; slow data
elderly, household contacts of people with smear-positive entry; some gaps between the population identified in
TB and people coinfected with HIV. the survey census and the national census data due to
seasonal migration; and rescheduling of one cluster
Other implications included: operation due to border security issues.
• a need to improve the capacity of health-care Important lessons learned for future surveys were that:
workers to clinically recognize TB disease, given
that 55% of those with smear-positive TB and • institutional memory from a previous survey
cough of any duration had already sought care substantially facilitates a subsequent survey; the
(and 45% of these cases had consulted a public core staff of the 2002 survey led the 2011 survey,
health facility); more than half (55%) of those and the same international experts (from WHO
with smear-negative, culture-positive TB and and JICA) provided technical assistance; and
a cough of any duration had also previously • the availability of trained staff and survey
sought care; and equipment previously mobilized for active case
• a need to consider the wider use of TB preventive detection in high-risk populations (in the case
therapy, especially among older people with of Cambodia, since 2006) can help to ensure
a chest X-ray suggestive of inactive TB and smooth survey operations.
negative bacteriological test results.
References
1. The World Bank (https://data.worldbank.org/country, accessed
April 2017).
2. UNAIDS (http://aidsinfo.unaids.org/, accessed April 2017).
3. World Health Organization. Global Tuberculosis Database. 2017.
(http://www.who.int/tb/country/en/, accessed April 2017).
4. Report of the Research Committee on Pol Pot’s Genocidal Regime
Phnom Penh, Cambodia: 1983 (http://www.dccam.org/, accessed
May 2017). The original report is in the Khmer language; excerpts
have been translated by the Documentation Center of Cambodia
for the Cambodian Genocide Program.
5. WHO Tuberculosis Programme. (1994). WHO Tuberculosis
Programme: framework for effective tuberculosis
control. World Health Organization. (http://www.who.int/iris/
handle/10665/58717, accessed January 2018).
6. World Health Organization. Global tuberculosis programme.
Global tuberculosis control report 1997. Geneva: WHO; (https://
apps.who.int/iris/bitstream/handle/10665/63354/WHO_
TB_97.225_(part1).pdf?sequence=1, accessed January 2018).
7. Report of the national TB prevalence survey, 2002. Phnom Penh:
Cambodia Ministry of Health; 2005.
8. Report of the second national TB prevalence survey, 2011.
Phnom Penh: Cambodian Ministry of Health; 2012 (http://open_
jicareport.jica.go.jp/pdf/12120325.pdf, accessed January 2018).
9. World Health Organization. Tuberculosis prevalence surveys:
a handbook (WHO/HTM/TB/2010.17). Geneva: WHO; 2011
(https://apps.who.int/iris/bitstream/handle/10665/44481/
9789241548168_eng.pdf, accessed August 2017).
10. Mao TE, Okada K, Yamada N, Peou S, Ota M, Saint S et al. Cross-
sectional studies of tuberculosis prevalence in Cambodia between
2002 and 2011. Bull World Health Organ. 2014;92(8):573–581
(https://www.ncbi.nlm.nih.gov/pubmed/25177072, accessed May
2017).
89
CHINA
2010
Summary statistics
Participation rate 96%
Symptom screening
Cough ≥2 weeksa 5 364 (2.1%)
Haemoptysisa 293 (0.1%)
Sputum production N/A
Chest pain N/A
Fever N/A
Total symptom-screen positivea 5 462 (2.2%)
Eligible for sputum examination 9 825 (3.9%) Symptom positive, chest X-ray positive 797 (8.1%)
Symptom positive, chest X-ray negative or N/A 4 665 (48%)
Symptom negative, chest X-ray positive 2 189 (22%)
Otherb 2 174 (22%)
Submitted specimens
At least one specimen N/A
Both specimens N/A
Laboratory result
At least one culture result availablec 9 684 (99%)
Total bacteriologically confirmed cases 347 Symptom positive, chest X-ray positive 143 (41%)
Symptom positive, chest X-ray negative or N/A 17 (5.0%)
Symptom negative, chest X-ray positive 182 (52%)
Otherf 5 (1.4%)
a
Eligible for sputum collection.
b
Chest X-ray exempted and symptom-screen negative (2 167), other (not specified) (7).
c
Cultures that were either contaminated and/or missing without a definitive result (i.e. MTB, NTM, negative) were excluded.
d
Definite: MTB confirmed by culture. Probable: MTB not confirmed by culture, and non NTM (all 42 participants had culture-negative results).
e
Definite: MTB confirmed by culture. Probable: no definition.
f
Chest X-ray exempted and symptom-screen negative (4), other (not specified) (1).
92 National TB prevalence surveys 2007–2016
Fig. 1: Participation rate by age and sex Fig. 4: Cluster variation of the number of bacteriologically
confirmed TB casesb
100 50
45
40
Participation rate (%)
Number of clusters
35
30
90 25
20
15
10
5
80 0
15–24 25–34 35–44 45–54 55–64 ≥65 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18
Age group (years) Number of bacteriologically confirmed TB cases
Male Female
Fig. 2: TB prevalence per 100 000 population by age Fig. 5: Ratio of smear-positive TB prevalence to notifications by
age and by sexc
500 3.0
Prevalence per 100 000 population
350
2.0
300
250 1.5
200
150 1.0
100
0.5
50
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 15–24 25–34 35–44 45–54 55–64 ≥65 Male Female Total
Age group (years) Age group (years) and sex (≥15)
Bacteriologically confirmed TB Smear-positive TB
Fig. 3: Estimated number of bacteriologically confirmed TB cases Fig. 6: Estimates of TB prevalence (all ages, all forms of TB) before
and prevalence per 100 000 population, by agea (in blue) and after (in red) the national TB prevalence surveyd
300 000
250
250 000
200
200 000
150
150 000
100 000 100
50 000 50
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 60 90 120 150
Age group (years) Prevalence per 100 000 population
a
The estimated number of bacteriologically confirmed TB cases is the product of age-specific prevalence and population estimates from the UN Population Division (2015 revision).
b
The data suggest that the distribution of cases by cluster (blue bars) was significantly different from the theoretical distribution (red line) (mean 1.97, variance 5.55, p<0.05). The
theoretical distribution assumes cases are distributed at random i.e. no clustering effect.
c
Notification rates were estimated using notifications obtained from the WHO global TB database, and population estimates from the UN Population Division (2015 revision).
d
The blue bar denotes the best estimate of prevalence and its range that was indirectly derived from the estimate of incidence previously published by WHO, adjusted to the year of the
prevalence survey based on previously published trends in incidence.
CHINA 93
defined based on geography and economic status, with for whom there were results about health-care
wealth generally declining from east to west. seeking behaviour) had previously sought care
in a public or private health facility.
Other key results were: The survey showed that TB prevalence declined
• the male to female ratio was 3.1 for smear- substantially between 1990 and 2010. Based on analysis of
positive TB and 3.0 for bacteriologically results according to the diagnostic protocol used in 1990
confirmed TB; to allow for a fair comparison, the prevalence of smear-
• prevalence per 100 000 population increased positive TB fell from 170 (95% CI: 166–174) per 100 000
with age, as did the absolute number of population in 1990 to 59 (95% CI: 49–72) per 100 000
bacteriologically confirmed TB cases; over 60% population in 2010. In the 1990s, the prevalence of
(219/347) of prevalent TB cases were aged 55 or
smear-positive TB fell only in the provinces where DOTS
more;
was implemented. After 2000, declines were observed
• among the bacteriologically confirmed TB
cases, 46% were symptom-screen positive, and in all provinces. Of the total reduction in the prevalence
of the smear-positive cases, 49% were symptom- of smear-positive TB from 1990–2010, 70% occurred
screen positive; after 2000.
• for smear-positive pulmonary TB, the ratio of
prevalence to notifications (P:N ratio) was 1.7
overall, but varied from 0.7 in those aged 15–24
years to 2.5 in the age groups 55–64 years and 65 Implications of results
years or more; also, it was higher for men than
for women (1.8 versus 1.4); The halving of TB prevalence in 20 years was assisted
• among the bacteriologically confirmed TB by a nationwide DOTS programme being implemented
cases, 85% had no previous history of anti-TB throughout the country’s network of local centres for
treatment and 2.6% were on anti-TB treatment disease control, improved reporting and referral hospital
at the time of the survey; and systems, and a policy of free treatment for all patients with
• of the 153 bacteriologically confirmed survey active pulmonary TB, alongside rapid socioeconomic
cases that screened positive for symptoms and development. Specifically, there were tremendous
were not on anti-TB treatment at the time of the increases in GNI per capita (from US$ 330 in 1990 to
survey, 48% (73 of the 151 for whom there were
results about health-care seeking behaviour) US$ 4340 in 2010) and in living conditions overall (the
had previously sought care in a public or human development index improved from 0.501 in 1990
private health facility for their symptoms; and to 0.699 in 2010) (1,8). The overall fall in the prevalence of
of the 87 smear-positive TB cases who reported TB, in combination with the reduction in the proportion
symptoms but were not on anti-TB treatment of prevalent cases with a previous history of TB, also had
at the time of the survey, 57% (49 of the 86
Photo credit: Yin Yin Xia Photo credit: Yin Yin Xia
CHINA 95
a major impact on reducing the burden of multidrug- survey census”. In practice, the definition of “six months
resistant TB (MDR-TB). residency in the household” was used since this was the
official government definition. Using this more restrictive
Clear differences in TB prevalence between men and criterion, 10% of otherwise-eligible invitees were defined
women, and across age groups and geographic regions as non-permanent residents, and just over 20% of people
also showed the need for considerable further efforts, identified by the survey census were not included in the
such as policy or programmatic measures targeted to survey because they had moved in the past six months.
particular population groups and regions. TB control and In addition, the survey team could not find 30% of the
policy should prioritize western and central China, rural registered population in the survey clusters; this probably
areas, the elderly, ethnic minorities and those who are also reflected internal migration, especially of young men
poor. It was also recognized that central and provincial to urban areas.
governments should strengthen funding support and
input for infrastructure, facilities and human resources The second challenge involved culture testing. Although
for these areas and population groups. the central team and the National TB Reference
Laboratory made extensive efforts to standardize survey
The survey also showed that there was a need to improve operations in all provinces, the yield from cultured
TB notification and treatment of patients with TB within sputum specimens was low or non-existent in some
the hospital sector. provinces. In other TB prevalence surveys in Asia, the
number of smear-negative culture-positive TB cases was
1.2–2.0 times higher than the number of smear-positive
Major successes, challenges and lessons TB cases.2 Among 31 provinces in the prevalence survey
learned in China, only six (19%) had a ratio of smear-negative
culture-positive to smear-positive TB cases of 1.5 and
The 2010 survey followed methods recommended in the above. Five other provinces had no yield from cultured
first (2007) edition of WHO’s handbook on prevalence sputum specimens.
surveys (9). This included three modifications compared
with the fourth (2000) survey:
• inclusion of adults (aged ≥15 years) only;1 References
• no tuberculin skin testing; and
1. The World Bank (https://data.worldbank.org/country, accessed
• use of direct chest X-ray (posteroanterior) film April 2017).
images instead of fluoroscopy screening. 2. World Health Organization. Global Tuberculosis Database. 2017.
(http://www.who.int/tb/country/en/, accessed April 2017).
Major successes included implementation of the survey
3. WHO Tuberculosis Programme. (1994). WHO Tuberculosis
within two years of initiating planning; full mobilization Programme: framework for effective tuberculosis
of funding required for field operations at provincial level, control. World Health Organization. (http://www.who.int/iris/
which enabled field operations to be completed within handle/10665/58717, accessed January 2018).
four months; a high participation rate; a sample large 4. World Health Organization. Global tuberculosis programme.
Global tuberculosis control report 1997. Geneva: WHO; (https://
enough to produce precise provincial as well as national apps.who.int/iris/bitstream/handle/10665/63354/WHO_
estimates of TB prevalence; and prompt finalization of TB_97.225_(part1).pdf?sequence=1, accessed January 2018).
results and production of a survey report. 5. Wang L, Zhang H, Ruan Y, Chin DP, Xia Y, Cheng S et al.
Tuberculosis prevalence in China, 1990–2010; a longitudinal
There were two major challenges. The first was the level of analysis of national survey data. Lancet. 2014;383(9934):2057–
2064 (https://www.ncbi.nlm.nih.gov/pubmed/24650955, accessed
internal migration in China. The technical expert group May 2017).
established to provide advice on the survey suggested 6. Disease Control Bureau of the Ministry of Health – Chinese
that the residential criteria for determining whether Center for Disease Control and Prevention. Report on the 5th
people were eligible to participate in the survey should national tuberculosis epidemiological survey in China – 2010.
Beijing, China: Military Medical Science Press; 2011.
be defined as “resident for one month at the time of the
1
The 2000 survey included children as well as adults; for every case found 2
Cambodia: 2.0 (smear-positive TB cases: smear-negative culture-positive TB
among children, 8000 children were screened. cases = 103:211), Indonesia: 1.6 (165:261), Lao PDR: 1.2 (107:130), Mongolia:
1.8 (88:160), Myanmar: 1.5 (123:188) and Thailand: 1.5 (58:84).
96 National TB prevalence surveys 2007–2016
DEMOCRATIC PEOPLE’S
REPUBLIC OF KOREA
2015–2016
Summary statistics
Participation rate 84%
Key people
Name Role Organization
Kim Hyong Hun Chair of steering committee Ministry of Public Health (MoPH)
Ri Chan Hyok Member of steering committee, principal investigator MoPH
Choe Tong Chol Member of steering committee MoPH
Jo Won Ryong Leader of central survey data management team MoPH
Rim Gye Tong Leader of central survey management team MoPH
Choe Tal Bom Leader of central survey interview team Pyongyang Medical college under Kim Il Sung university
Ri Jong Chan Leader of central survey chest X-ray team Central TB Preventive Institute (CTPI)
Yun Jong Chol Leader of central survey laboratory team CTPI
Ko Jin Hyok Survey coordinator TB Programme Management Unit (PMU), MoPH
Partha Pratim Mandal TB medical officer WHO South-East Asia Regional Office (SEARO)
Mubeen Aslam Global Fund programme coordinator UNICEF, Democratic People's Republic of Korea
M. Bintari Dwihardiani Technical assistance (survey advisor) WHO Indonesia
Philippe Glaziou Technical assistance (analysis) WHO headquarters
Charalambos Sismanidis Technical assistance (analysis) WHO headquarters
a
The boundaries and names shown and the designations used on this map do not
imply the expression of any opinion whatsoever on the part of the World Health
Organization concerning the legal status of any country, territory, city or area or of
its authorities, or concerning the delimitation of its frontiers or boundaries.
98 National TB prevalence surveys 2007–2016
Symptom screening
Cough ≥2 weeksa 2 805 (4.6%)
Haemoptysisa 267 (0.4%)
Weight loss 1 032 (1.7%)
Fever 1 335 (2.2%)
Night sweats 1 214 (2.0%)
Total symptom-screen positivea 2 944 (4.9%)
Eligible for sputum examination 4 802 (7.9%) Symptom positive, chest X-ray positive 1 028 (21%)
Symptom positive, chest X-ray negative or N/A 1 916 (40%)
Symptom negative, chest X-ray positive 1 858 (39%)
Other N/A
Submitted specimens
At least one specimen 4 586 (96%)
Both specimens 4 462 (93%)
Laboratory result
At least one culture result availableb 4 583 (95%)
Total bacteriologically confirmed cases 340 Symptom positive, chest X-ray positive 187 (55%)
Symptom positive, chest X-ray negative or N/A 7 (2.1%)
Symptom negative, chest X-ray positive 146 (43%)
Other N/A
a
Eligible for sputum collection.
b
Cultures that were either contaminated and/or missing without a definitive result (i.e. MTB, NTM, negative) were excluded.
c
Definite: MTB confirmed by culture. Probable: MTB not confirmed by culture but chest X-ray abnormal findings at central reading.
d
Definite: MTB confirmed by culture, with having either chest X-ray abnormal findings at central reading or follow-up evidence. Probable: no definition.
100 National TB prevalence surveys 2007–2016
Fig. 1: Participation rate by age and sex Fig. 4: Cluster variation of the number of bacteriologically
confirmed TB casesb
100
22
20
90 18
Participation rate (%)
Number of clusters
16
14
80 12
10
8
70 6
4
2
60 0
15–24 25–34 35–44 45–54 55–64 ≥65 0 1 2 3 4 5 6 7 8 9 10 11
Age group (years) Number of bacteriologically confirmed TB cases
Male Female
Fig. 2: TB prevalence per 100 000 population by age Fig. 5: Ratio of bacteriologically confirmed TB prevalence to
notifications by age and by sexc
1200 2.5
Prevalence per 100 000 population
1000
Prevalence : notification ratio
2.0
800
1.5
600
1.0
400
200 0.5
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 15–24 25–34 35–44 45–54 55–64 ≥65 Male Female Total
Age group (years) Age group (years) and sex (≥15)
Bacteriologically confirmed TB Smear-positive TB
Fig. 3: Estimated number of bacteriologically confirmed TB cases Fig. 6: Estimates of TB prevalence (all ages, all forms of TB) before
and prevalence per 100 000 population, by agea (in blue) and after (in red) the national TB prevalence surveyd
35 000 1000
Estimated number of bacteriologically
900
30 000
800
25 000 700
confirmed TB cases
600
20 000
500
15 000
400
10 000 300
200
5 000
100
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 400 800 1200
Age group (years) Prevalence per 100 000 population
a
The estimated number of bacteriologically confirmed TB cases is the product of age-specific prevalence and population estimates from the UN Population Division (2019 revision).
b
The data did not suggest that the distribution of cases by cluster (blue bars) was significantly different from the theoretical distribution (red line) (mean 3.4, variance 4.22, p=0.12). The
theoretical distribution assumes cases are distributed at random i.e. no clustering effect.
C
Notification rates were estimated using notifications obtained from the WHO global TB database, and population estimates from the UN Population Division (2019 revision).
d
The blue bar denotes the best estimate of prevalence and its range that was indirectly derived from the estimate of incidence previously published by WHO, adjusted to the year of the
prevalence survey based on previously published trends in incidence.
DEMOCRATIC PEOPLE’S REPUBLIC OF KOREA 101
Other implications included the need to: Major successes, challenges and lessons
• strengthen community screening for TB
learned
to ensure earlier detection, treatment and
Despite financial and technological constraints, the
notification of cases;
first national TB prevalence survey of the Democratic
• review the surveillance system, given that a large
proportion of TB cases (26%) on treatment were People’s Republic of Korea managed to achieve its
not notified to the NTP; primary objective and field operations were successfully
• review the use of and access to chest X-ray completed within a year.
screening in the early detection of cases,
given that 43% (146/340) of bacteriologically Almost all national TB prevalence surveys since 2015 used
confirmed survey cases were only identified by Xpert MTB/RIF or Xpert Ultra, in addition to culture, as
chest X-ray; part of the diagnostic algorithm for all participants who
• expand the range of laboratory tests to diagnose screened positive. However, given important limitations,
TB beyond smear and culture, recognizing that the Democratic People’s Republic of Korea’s survey was
high-level negotiations would be required to only able to use smear and culture, as was originally
ensure the sustainable use and expansion of
recommended in the lime book (5). Other constraints
Xpert MTB/RIF;
included reliance on paper instead of electronic data
• strengthen health services, especially at the
peripheral level (Ri/Dong clinic and city/ collection systems, and conventional instead of digital
county hospital) – for example, by raising mobile chest X-ray machines. The survey was among
health worker awareness of TB symptoms and those that cost the least to implement, at US$ 1.4 million.
making diagnostics more widely available; many The Global Fund contributed about US$ 900 000, with
bacteriologically confirmed cases had sought the remainder being supplied by the Ministry of Public
care before diagnosis, including nearly half of all
Health.
symptomatic smear-positive TB cases, but not
been diagnosed; and
The survey’s high level of participation (84%) was probably
• strengthen community awareness of TB, since due to strong leadership and extensive community
more than 40% (1193/2944) of participants
with chronic cough or haemoptysis (or both) at engagement by the large survey teams (six teams of 25
the time of the survey had not sought care for people) and central survey team (>100 people).
their symptoms – men accounted for the vast
majority of symptomatic participants.
There were few regular international missions to provide An important lesson learned for future surveys was
technical assistance, due to administrative challenges the importance of good planning and collaboration for
and access restrictions. A technical consultant from smooth implementation. Specifically, the procurement
the national TB prevalence survey team of Indonesia of laboratory and chest X-ray equipment should be
provided some in-country advice (June 2016), and two completed before starting field operations, and sufficient
laboratory experts from the supranational reference lead times allowed for this purpose.
laboratory in Hong Kong Special Administrative Region
reviewed laboratory progress and results (July 2016).
There was good engagement with the WHO country
References
office and WHO headquarters to support data review,
final analysis and report writing. Collaboration with 1. The World Bank (https://data.worldbank.org, accessed July 2017).
multiple international stakeholders, from procurement 2. UNAIDS (https://aidsinfo.unaids.org/, accessed July 2017).
3. World Health Organization. Global Tuberculosis Database. 2017
to dissemination, also helped to ensure that the survey
(https://www.who.int/tb/data/en/, accessed July 2017).
was a success.
4. Report of DPRK National TB Prevalence Survey (2015–2016),
Department of TB and Hepatitis, Ministry of Public Health,
Major challenges included interruptions of funding in Democratic People’s Republic of Korea; 2017.
2014 that led to a 1-year delay before field operations 5. World Health Organization. Tuberculosis prevalence surveys:
could be started. In addition, there were long delays in a handbook. Geneva: WHO; 2011 (https://apps.who.int/iris/
bitstream/handle/10665/44481/9789241548168_eng.pdf,
the procurement of mobile conventional chest X-ray accessed August 2017).
machines. This meant that the survey could only start 6. World Health Organization. Global tuberculosis report 2017.
with two instead of four field teams during phase one of Geneva: WHO; 2017 (https://www.who.int/tb/data/en/, accessed
the survey (October to November 2015). Extended delays July 2017).
from the end of field operations to the final dissemination 7. World Health Organization. Global tuberculosis report 2015.
Geneva: WHO; 2015 (https://www.who.int/tb/data/en/, accessed
of results were due to insufficient human resources for July 2017).
data entry, analysis and report writing. Other challenges
included the replacement of five clusters due to poor road
conditions.
ETHIOPIA
2010–2011
Summary statistics
Participation rate 90%
Key people
Name Role Organization
Amha Kebede Director general, principal investigator Ethiopian Public Health Institute
Zeleke Alebachew Survey coordinator Ethiopian Public Health Institute
Fasil Tsegaye Deputy survey coordinator Ethiopian Public Health Institute
Almaz Abebe Directorate director, Infectious and Non Infectious Disease Research Ethiopian Public Health Institute
Eshetu Lema Senior laboratory advisor Ethiopian Public Health Institute
Mulualem Agonafer Laboratory manager Ethiopian Public Health Institute
Gashawtena Fantu Central X-ray radiologist Saint Paul’s Hospital
Molla Endale Central X-ray radiologist Saint Paul’s Hospital
Shewalem Negash Central X-ray radiologist Saint Paul’s Hospital
Feleke Dana Data manager Ethiopian Public Health Institute
Menelik Balcha Field team leader Ethiopian Public Health Institute
Sale Workneh Field team leader Ethiopian Public Health Institute
Tedla Fiseha Field team leader Ethiopian Public Health Institute
Tibebu Biniam Field team leader Ethiopian Public Health Institute
Wilfred Nkhoma Technical assistance (survey advisor) WHO Regional Office for Africa (AFRO)
Ikushi Onozaki Technical assistance (survey advisor) WHO headquarters
Marina Tadolini Technical assistance (survey advisor) Consultant, Italy
Peou Satha Technical assistance (survey advisor) Consultant, Cambodia
Hazim Timimi Technical assistance (data management) WHO headquarters
Charalampos Sismanidis Technical assistance (design and analysis) WHO headquarters
a
The boundaries and names shown and the designations used on this map do not
imply the expression of any opinion whatsoever on the part of the World Health
Organization concerning the legal status of any country, territory, city or area or of
its authorities, or concerning the delimitation of its frontiers or boundaries.
106 National TB prevalence surveys 2007–2016
Symptom screening
Cough ≥2 weeksa 3 026 (6.5%)
Cough (any duration) 5 930 (13%)
Night sweats ≥2 weeks 8 177 (18%)
Fever ≥2 weeks 5 920 (13%)
Weight loss ≥3 kg in past month 10 014 (21%)
Total symptom-screen positivea 3 026 (6.5%)
Eligible for sputum examination 6 080 (13%) Symptom positive, chest X-ray positive 806 (13%)
Symptom positive, chest X-ray negative or N/A 2 220 (36%)
Symptom negative, chest X-ray positive 3 013 (50%)
Otherb 41 (1.0%)
Submitted specimens
At least one specimen 5 868 (97%)
Both specimens 5 606 (92%)
Laboratory result
At least one culture result availablec 5 503 (91%)
Total bacteriologically confirmed cases 110 Symptom positive, chest X-ray positive 45 (41%)
Symptom positive, chest X-ray negative or N/A 12 (11%)
Symptom negative, chest X-ray positive 53 (48%)
Other 0 (0%)
a
Eligible for sputum collection.
b
One of the following: weight loss ≥3 kg in the past month, night sweats ≥2 weeks, fever ≥2 weeks or contact with a TB patient in the past year while chest X-ray exempted.
c
Cultures that were either contaminated and/or missing without a definitive result (i.e. MTB, NTM, negative) were excluded.
d
Definite: MTB confirmed by culture. Probable: MTB not confirmed by culture but chest X-ray consistent with TB.
e
Definite: MTB confirmed by culture with chest X-ray consistent with TB. Probable: MTB confirmed by culture but without chest X-ray consistent with TB.
108 National TB prevalence surveys 2007–2016
Fig. 1: Participation rate by age and sex Fig. 4: Cluster variation of the number of bacteriologically
confirmed TB casesb
100 30
25
Participation rate (%)
Number of clusters
20
90 15
10
80 0
15–24 25–34 35–44 45–54 55–64 ≥65 0 1 2 3 4 5
Age group (years) Number of bacteriologically confirmed TB cases
Male Female
Fig. 2: TB prevalence per 100 000 population by age Fig. 5: Ratio of smear-positive TB prevalence to notifications by
age and by sexc
600 3.5
Prevalence per 100 000 population
3.0
Prevalence : notification ratio
500
2.5
400
2.0
300
1.5
200
1.0
100 0.5
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 15–24 25–34 35–44 45–54 55–64 ≥65 Male Female Total
Age group (years) Age group (years) and sex (≥15)
Bacteriologically confirmed TB Smear-positive TB
Fig. 3: Estimated number of bacteriologically confirmed TB cases Fig. 6: Estimates of TB prevalence (all ages, all forms of TB) before
and prevalence per 100 000 population, by agea (in blue) and after (in red) the national TB prevalence surveyd
60 000 400
Estimated number of bacteriologically
350
50 000
300
confirmed TB cases
40 000
250
30 000 200
150
20 000
100
10 000
50
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 200 300 400 500
Age group (years) Prevalence per 100 000 population
a
The estimated number of bacteriologically confirmed TB cases is the product of age-specific prevalence and population estimates from the UN Population Division (2015 revision).
b
The data did not suggest that the distribution of cases by cluster (blue bars) was significantly different from the theoretical distribution (red line) (mean 1.29, variance 1.59, p=0.12).
The theoretical distribution assumes cases are distributed at random i.e. no clustering effect.
c
Notification rates were estimated using notifications obtained from the WHO global TB database, and population estimates from the UN Population Division (2015 revision).
d
The blue bar denotes the best estimate of prevalence and its range that was indirectly derived from the estimate of incidence previously published by WHO, adjusted to the year of the
prevalence survey based on previously published trends in incidence.
ETHIOPIA 109
Major successes, challenges and lessons Only one specimen per participant was taken for culture;
learned therefore, the prevalence of culture-positive TB may
have been underestimated. Nonetheless, the relatively
This was the first-ever national TB prevalence survey in high culture contamination rate may have contributed to
Ethiopia, and the first national survey in Africa in more higher culture yields than those found in other African
than 50 years to be successfully implemented according surveys that used culture with Löwenstein-Jensen media.
to screening and diagnostic methods recommended
in the 2011 edition of WHO’s handbook on national An important lesson for future surveys was that the high
TB prevalence surveys (6). It only took just over 1 year level of commitment from different stakeholders was
between the decision to undertake a survey and the key to prompt survey preparation and implementation
start of field operations. The population coverage (97%), (the shortest preparation period of any survey in Africa
participation rate (90%) and sputum collection rate (97%) in the period 2009–2015). This commitment had many
were all very high. benefits. For example, it ensured the early appointment of
a full-time survey coordinator, close collaboration with
Major challenges in the early stages of the survey included the WHO Country Office and WHO headquarters, and
mismanagement of sputum specimens, backlogs in excellent collaboration with the NTP. Other important
culture inoculation and a high culture contamination rate benefits included Asia-Africa collaboration, combined
(up to 15% for cultures in the first week of the survey). with technical assistance from WHO and an independent
With strong leadership from the principal investigator consultant. Members of the survey team from Cambodia
and the survey’s technical working group, major efforts provided technical assistance to the Ethiopian survey
were made to address these challenges. Problems with team; the staff person leading WHO’s global work on
management of sputum specimens were resolved, and national TB prevalence surveys made more than 10 visits
the overall contamination rate for the survey was 6% during the course of the survey; and an independent
(360/5868). Other challenges included delays in the consultant (funded by the Italian Cooperation) provided
procurement of chest X-ray equipment; difficulties in regular assistance throughout the survey, from protocol
retaining radiologists during field operations; and the development to reporting of results.
use of data management software that was not suited to
the flow of data collection in a prevalence survey, which
caused delays in data capture. Due to security and logistical
challenges, 3% of the total population was excluded from
the sampling frame (e.g. parts of Somaliland and areas
bordering Eritrea).
References
1. The World Bank (https://data.worldbank.org/country, accessed
April 2017).
2. UNAIDS (http://aidsinfo.unaids.org/, accessed April 2017).
3. World Health Organization. Global Tuberculosis Database. 2017.
(http://www.who.int/tb/country/en/, accessed April 2017).
4. Kebede AH, Alebachew Z, Tsegaye F, Lemma E, Abebe A,
Agonafir M et al. The first population-based national tuberculosis
prevalence survey in Ethiopia, 2010–2011. Int J Tuberc Lung
Dis. 2014;18(6):635–639 (https://www.ncbi.nlm.nih.gov/
pubmed/24903931, accessed April 2017).
5. First Ethiopian national population based tuberculosis prevalence
survey. Addis Ababa: Ministry of Health, Federal Democratic
Republic of Ethiopia; Ethiopian Health and Nutrition Research
Institute; 2011 (http://www.ephi.gov.et/images/downloads/
Tuberculosis%20Prevalence%20Survey.pdf, accessed May 2017).
6. World Health Organization. Tuberculosis prevalence surveys:
a handbook (WHO/HTM/TB/2010.17). Geneva: WHO; 2011
(https://apps.who.int/iris/bitstream/handle/10665/44481/
9789241548168_eng.pdf, accessed August 2017).
113
GAMBIA
2011–2013
Summary statistics
Participation rate 77%
Summary statistics
Bacteriologically confirmed TB (≥15 years)
• Prevalence per 100 000 population 212
• Male:female ratio 3.1
Key people
Name Role Organization
Ifedayo Adetifa Principal investigator Medical Research Council (MRC) Unit-The Gambia
Ma Ansu Kinteh Survey coordinator MRC Unit-The Gambia
Martin Antonio Unit microbiologist and head of MRC TB Reference Laboratory MRC Unit-The Gambia
Ramatoulie Manne Radiology coordinator MRC Unit-The Gambia
Beatrice dei Alorse Radiology coordinator MRC Unit-The Gambia
Simon Donkor Data manager MRC Unit-The Gambia
Adedapo Bashorun Field team leader MRC Unit-The Gambia
Christopher Linda Field team leader MRC Unit-The Gambia
Semeeh Omoleke Field team leader MRC Unit-The Gambia
Lindsay Kendall Biostatistician MRC Unit-The Gambia
David Jeffries Biostatistician MRC Unit-The Gambia
Edward Demba Scientific officer-mycobacteriology MRC Unit-The Gambia
Catherine Bi Okoi Scientific officer-mycobacteriology MRC Unit-The Gambia
Kodjovi Mlaga Scientific officer-mycobacteriology MRC Unit-The Gambia
William dei Alorse Scientific officer-mycobacteriology MRC Unit-The Gambia
Umberto D’Alessandro Epidemiologist/head of Disease Control and Elimination Theme MRC Unit-The Gambia
Elina Cole Senior project administrator MRC Unit-The Gambia
Ikushi Onozaki Technical assistance (survey advisor) WHO headquarters
Marina Tadolini Technical assistance (survey advisor) Consultant, Italy
Charalampos Sismanidis Technical assistance (design and analysis) WHO headquarters
Sian Floyd Technical assistance (analysis) London School of Hygiene & Tropical Medicine, UK
Etienne Leroy Terquiem Technical assistance (radiology advisor) Consultant, France
Jan van den Hombergh Technical assistance (radiology advisor) PharmAccess, Tanzania
John Mayanda Technical assistance (radiology advisor) PharmAccess, Tanzania
Bimbo Fasan Technical assistance (radiology advisor) Lagos state university teaching hospital, Nigeria
Symptom screening
Cough ≥2 weeksa 962 (2.2%)
Haemoptysis 210 (0.5%)
Fever 6 637 (15%)
Chest pain 6 551 (15%)
Night sweats 1 595 (3.7%)
Cough <2 weeks with ≥2 other TB symptomsa 1 372 (3.2%)
No cough with ≥3 other TB symptomsa 1 128 (2.6%)
Total symptom-screen positivea 3 462 (8.0%)
Eligible for sputum examination 5 948 (14%) Symptom positive, chest X-ray positive 1 026 (17%)
Symptom positive, chest X-ray negative or N/A 2 436 (41%)
Symptom negative, chest X-ray positive 2 384 (40%)
Otherb 102 (1.7%)
Submitted specimens
At least one specimen 5 436 (91%)
Both specimens 5 309 (89%)
Laboratory result
At least one culture result availablec 5 209 (88%)
Total bacteriologically confirmed cases 77 Symptom positive, chest X-ray positive 32 (41%)
Symptom positive, chest X-ray negative or N/A 12 (16%)
Symptom negative, chest X-ray positive 33 (43%)
Other 0 (0%)
a
Eligible for sputum collection.
b
Chest X-ray exempted and symptom-screen negative.
c
Cultures that were either contaminated and/or missing without a definitive result (i.e. MTB, NTM, negative) were excluded.
d
Definite: MTB confirmed by culture. Probable: MTB not confirmed by culture but two AFB positive or one AFB positive with chest X-ray suggestive of TB.
e
Definite: MTB confirmed by culture. Probable: no definition.
116 National TB prevalence surveys 2007–2016
Fig. 1: Participation rate by age and sex Fig. 4: Cluster variation of the number of bacteriologically
confirmed TB casesb
100 35
90 30
Participation rate (%)
Number of clusters
25
80
20
70 15
10
60
5
50 0
15–24 25–34 35–44 45–54 55–64 ≥65 0 1 2 3 4 5 6
Age group (years) Number of bacteriologically confirmed TB cases
Male Female
Fig. 2: TB prevalence per 100 000 population by age Fig. 5: Ratio of smear-positive TB prevalence to notifications by
age and by sexc
600 1.0
Prevalence per 100 000 population
Fig. 3: Estimated number of bacteriologically confirmed TB cases Fig. 6: Estimates of TB prevalence (all ages, all forms of TB) before
and prevalence per 100 000 population, by agea (in blue) and after (in red) the national TB prevalence surveyd
1 000 400
Estimated number of bacteriologically
900
Prevalence per 100 000 population
350
800
300
confirmed TB cases
700
600 250
500 200
400 150
300
100
200
100 50
0 0
15–34 35–54 ≥55 200 400 600 800
Age group (years) Prevalence per 100 000 population
a
The estimated number of bacteriologically confirmed TB cases is the product of age-specific prevalence and population estimates from the UN Population Division (2015 revision).
b
The data did not suggest that the distribution of cases by cluster (blue bars) was significantly different from the theoretical distribution (red line) (mean 0.96, variance 1.53, p=0.06).
The theoretical distribution assumes cases are distributed at random i.e. no clustering effect.
c
Notification rates were estimated using notifications obtained from the WHO global TB database, and population estimates from the UN Population Division (2015 revision).
d
The blue bar denotes the best estimate of prevalence and its range that was indirectly derived from the estimate of incidence previously published by WHO, adjusted to the year of the
prevalence survey based on previously published trends in incidence.
GAMBIA 117
This survey was the only one where the P:N ratio was
less than one for all categories (all age groups, male
and female). Possible explanations for this included an
NTP that was able to efficiently detect and treat cases
in the community as in high-resource settings, or over-
diagnosis of smear-positive TB cases in routine health
care services.
• a need to consider targeted interventions given that the implementing agency for the survey
among older people, including paying (Medical Research Council Unit, The Gambia (MRCG))
particular attention to this group during contact was an affiliate of the Medical Research Council UK.
investigations and active case finding (given the
However, following the survey, the radiology equipment
cultural acceptance of chronic cough among the
elderly); and was handed over to the government to help improve TB
• a need for increased funding for implementation diagnosis.
of targeted interventions, wider use and better
interpretation of X-rays, and improvements to The MRCG laboratory had excellent capacity, made
diagnostics. considerable efforts to ensure high-quality sputum
samples and used best practices in the decontamination
process. They pioneered the use of MGIT for primary
Major successes, challenges and lessons diagnosis and identification of MTB. Nevertheless,
learned culture contamination rates were relatively high (11%),
in part because of the use of liquid culture. The relatively
This was the first survey in Africa to have been outsourced high contamination rate might have contributed to
by the NTP and conducted by a reputable research higher yields by culture (i.e. there were more smear-
institute. In addition, it was the first survey for which negative, culture-positive specimens than smear-positive,
results led to a statistically significant downward estimate culture-positive ones). The contamination rate within the
of TB burden, thus confirming the value of undertaking laboratory for routine samples was within the prescribed
a survey and validating the notion that WHO estimates ranges for both solid and liquid media cultures.
were previously too high.
The survey was fully implemented by MRCG staff.
One major challenge was ensuring participation, Although the NLTP was represented by a designated
particularly in urban areas. Overall, the target of an 85% liaison person (deputy programme manager) for
participation rate was not achieved. The survey was also implementation and on the survey steering committee
prolonged to 13 months, and the start of the survey was (NLTP manager), their involvement was relatively limited.
delayed due to logistical problems. A particular difficulty More active engagement would have helped to build
was the procurement of mobile X-rays, due to a greater ownership of survey results and strengthened use
combination of the high unit cost and the need to adhere of the results in national strategic planning.
to European Union procurement rules and procedures
References
1. The World Bank (https://data.worldbank.org/country, accessed
April 2017).
2. UNAIDS (http://aidsinfo.unaids.org/, accessed April 2017).
3. World Health Organization. Global Tuberculosis Database. 2017.
(http://www.who.int/tb/country/en/, accessed April 2017).
4. WHO Tuberculosis Programme. (1994). WHO Tuberculosis
Programme: framework for effective tuberculosis
control. World Health Organization. (http://www.who.int/iris/
handle/10665/58717, accessed January 2018).
5. World Health Organization. Global tuberculosis programme.
Global tuberculosis control report 1997. Geneva: WHO; (https://
apps.who.int/iris/bitstream/handle/10665/63354/WHO_
TB_97.225_(part1).pdf?sequence=1, accessed January 2018).
6. The Gambian survey of tuberculosis prevalence (GAMSTEP).
Banjul, The Gambia: Medical Research Council Unit, The Gambia;
2014.
7. Adetifa IM, Kendall L, Bashorun A, Linda C, Omoleke S, Jeffries
D et al. A tuberculosis nationwide prevalence survey in Gambia,
2012. Bull World Health Organ. 2016;94(6):433–441 (https://
www.ncbi.nlm.nih.gov/pubmed/27274595, accessed August
2017).
8. World Health Organization. Tuberculosis prevalence surveys:
a handbook (WHO/HTM/TB/2010.17). Geneva: WHO; 2011
(https://apps.who.int/iris/bitstream/handle/10665/44481/
9789241548168_eng.pdf, accessed August 2017).
121
GHANA
2013
Summary statistics
Participation rate 91%
Key people
Name Role Organization
Frank Bonsu Principal investigator Ghana Health Service, National TB Control Programme (NTP)
Kennedy Kwasi Addo Co-principal investigator Noguchi Memorial Institute, University of Ghana
John Gyapong Co-investigator University of Ghana
Ellis Owusu Dabo Co-investigator Kwame Nkrumah University of Science and Technology
Kwadwo Koram Co-investigator Noguchi Memorial Institute, University of Ghana
Augustina Badu Peprah Co-investigator Komfo anokye teaching hospital, Kumasi
Raymond Yaw Gockah Survey coordinator Ghana Health Service, NTP
Francisca Dzata NTP laboratory focal point Ghana Health Service, NTP
Michael Omari Head of chest clinic laboratory Korle bu teaching hospital, Laboratory
Robertson Adiei Cartographer Ghana Statistical Service, NTP
Nii Nortey Hanson Nortey Deputy NTP manager Ghana Health Service, NTP
Jane Amponsah Data manager Ghana Health Service, NTP
Sauda Ahmed Assistant data manager Ghana Health Service, NTP
Herve Awako ICT manager TABS Consult (data/IT management)
Prince Boni Data planning TABS Consult (data/IT management)
Zeleke Alebachew Technical assistance (report writing) Consultant, Ethiopia
Irwin Law Technical assistance (survey advisor) WHO headquarters
Wilfred Nkhoma Technical assistance (survey advisor) WHO Regional Office for Africa (AFRO)
Ikushi Onozaki Technical assistance (survey advisor) WHO headquarters
Marina Tadolini Technical assistance (survey advisor) Consultant, Italy
Charalampos Sismanidis Technical assistance (analysis) WHO headquarters
a
The boundaries and names shown and the designations used on this map do not
imply the expression of any opinion whatsoever on the part of the World Health
Organization concerning the legal status of any country, territory, city or area or of
its authorities, or concerning the delimitation of its frontiers or boundaries.
122 National TB prevalence surveys 2007–2016
Symptom screening
Cough ≥2 weeksa 1 969 (3.2%)
Haemoptysis 273 (0.4%)
Sputum production 2 274 (3.7%)
Fever 1 405 (50%)b
Chest pain 1 898 (67%)b
Weight loss 1 242 (44%)b
Night sweats 1 172 (42%)b
Total symptom-screen positivea 1 969 (3.2%)
Eligible for sputum examination 8 298 (13%) Symptom positive, chest X-ray positive 771 (9.3%)
Symptom positive, chest X-ray negative or N/A 1 198 (14%)
Symptom negative, chest X-ray positive 4 387 (53%)
Otherc 1 942 (23%)
Submitted specimens
At least one specimen 8 126 (98%)
Both specimens 7 706 (93%)
Laboratory result
At least one culture result availabled 7 531 (91%)
Fig. 1: Participation rate by age and sex Fig. 4: Cluster variation of the number of bacteriologically
confirmed TB casesb
100
25
20
Participation rate (%)
Number of clusters
90
15
10
80
70 0
15–24 25–34 35–44 45–54 55–64 ≥65 0 1 2 3 4 5 6 7 8 9 10
Age group (years) Number of bacteriologically confirmed TB cases
Male Female
Fig. 2: TB prevalence per 100 000 population by age Fig. 5: Ratio of smear-positive TB prevalence to notifications by
age and by sexc
1200 4.5
Prevalence per 100 000 population
Fig. 3: Estimated number of bacteriologically confirmed TB cases Fig. 6: Estimates of TB prevalence (all ages, all forms of TB) before
and prevalence per 100 000 population, by agea (in blue) and after (in red) the national TB prevalence surveyd
12 000 1000
Estimated number of bacteriologically
900
Prevalence per 100 000 population
10 000 800
700
confirmed TB cases
8 000
600
6 000 500
400
4 000 300
200
2 000
100
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 100 200 300 400
Age group (years) Prevalence per 100 000 population
a
The estimated number of bacteriologically confirmed TB cases is the product of age-specific prevalence and population estimates from the UN Population Division (2015 revision).
b
The data suggested that the distribution of cases by cluster (blue bars) was significantly different from the theoretical distribution (red line) (mean 2.06, variance 4.08, p<0.05). The
theoretical distribution assumes cases are distributed at random i.e. no clustering effect.
c
Notification rates were estimate of using smear-positive pulmonary TB notifications (2013) obtained from the NTP, and population estimates from the UN Population Division (2015
revision).
d
The blue bar denotes the best estimate of prevalence and its range that was indirectly derived from the estimate of incidence previously published by WHO, adjusted to the year of the
prevalence survey based on previously published trends in incidence.
GHANA 125
• for smear-positive pulmonary TB, the ratio of This was further compounded by the large proportion of
prevalence to notifications (P:N ratio) was 2.5 people who self-treated, with a high usage of pharmacies
overall, but varied from 0.9 in those aged 25–34 as a first point of health care.
years to 3.8 in those aged 55–64 years, and it was
higher for men than for women (3.1 versus 1.8); Based on survey findings, the national TB control
• among bacteriologically confirmed TB cases, implementation strategy (TB strategic plan 2015–2020)
95% had no previous history of anti-TB was updated to include:
treatment and only 4.5% were on anti-treatment
at the time of the survey; and • a revised screening and diagnostic algorithm that
• of the 73 bacteriologically confirmed and 37 included chest X-ray and culture and/or Xpert®
smear-positive TB survey cases that screened MTB/RIF in addition to smear microscopy and
positive for symptoms and were not on anti-TB symptoms;
treatment at the time of the survey, 33 (45%) and • introduction of a policy to use chest X-ray as
17 (46%), respectively, had previously sought part of active TB case finding in vulnerable
care in a public or private health facility for their populations and in health-care settings;
symptoms.
• wider use of Xpert MTB/RIF throughout the
programme to detect bacteriologically confir-
med cases and to exclude nontuberculous
Implications of results mycobacteria (NTM); and
• targeting of TB screening activities to specific
The estimated TB prevalence (all forms, all ages) based on subpopulations, such as men and the elderly.
the survey (290 per 100 000 population; 95% CI: 196–384)
In addition, the evidence of TB-related stigma and poor
was approximately three times higher than the pre-survey
knowledge about TB in the general population prompted
estimate (92 per 100 000 population; 95% CI: 44–158).
the development of a national communications strategy
Furthermore, the survey clearly revealed undiagnosed TB
with stakeholders. The survey also highlighted gaps in
cases in the community, with many missed opportunities
the surveillance system that needed to be addressed; in
for diagnosis, including a high proportion of patients
particular, underreporting of smear-negative culture-
with chronic cough who visited both public and private
positive TB cases to the NTP.
health facilities but were not offered sputum examination.
Culture and Xpert MTB/RIF testing showed that a smear- survey one of the most technologically advanced
positive test result did not always indicate TB disease, (among those conducted in 2009–2016) in
especially in a community setting as opposed to a clinical terms of data management; beyond the survey,
this subsequently improved data management
setting. In active TB case finding, TB cannot be diagnosed capacity within the NTP; and
based on smear examination alone.
• the active community screening, specimen
collection and transportation required in the
survey improved working relationships between
Major successes, challenges and lessons the NTP and research institutes.
learned The survey faced several challenges. It took four years
from the start of survey preparations in 2008 to reach
The major overarching success was that the first national the point at which field operations could be launched.
TB prevalence survey in Ghana in more than 50 years The major reason for this delay was the substantial time
was successfully implemented, with a high participation taken to acquire digital X-ray units. When the survey was
rate. A key part of the success story was that the survey designed, the timely delivery of such units was expected
was led and coordinated by the NTP, with stakeholders from a large Netherlands-Ghana project to equip the
from research institutes, the national statistical service, district hospital network with digital equipment, based
universities and the Ministry of Health. The survey team on a concessional loan and national counterpart funding.
also benefited from substantial technical assistance, In practice, the project was not approved by the Dutch
coordinated by the WHO Global Task Force on TB national parliament for several years and the NTP had to
Impact Measurement. mobilize other funds to procure the X-ray units needed
for the survey.
Other successes included:
• the survey enhanced national capacity to conduct During field operations there were logistical challenges.
culture examinations, drug susceptibility testing Transportation across harsh terrain caused some
and action-oriented operational research; breakdowns in container X-ray units, which needed to be
• collaboration with the private sector in data replaced with portable units that had shockproof boxes. In
planning, management and storage made the one of the two laboratories used in the survey, there was a
References
1. The World Bank (https://data.worldbank.org/country, accessed
April 2017).
2. UNAIDS (http://aidsinfo.unaids.org/, accessed April 2017).
3. World Health Organization. Global Tuberculosis Database. 2017.
(http://www.who.int/tb/country/en/, accessed April 2017).
4. WHO Tuberculosis Programme. (1994). WHO Tuberculosis
Programme: framework for effective tuberculosis
control. World Health Organization. (http://www.who.int/iris/
handle/10665/58717, accessed January 2018).
5. World Health Organization. Global tuberculosis programme.
Global tuberculosis control report 1997. Geneva: WHO; (https://
apps.who.int/iris/bitstream/handle/10665/63354/WHO_
TB_97.225_(part1).pdf?sequence=1, accessed January 2018).
6. World Health Organization. Tuberculosis prevalence surveys:
a handbook (WHO/HTM/TB/2010.17). Geneva: WHO; 2011
(https://apps.who.int/iris/bitstream/handle/10665/44481/
9789241548168_eng.pdf, accessed August 2017).
129
INDONESIA
2013–2014
Summary statistics
Participation rate 89%
Key people
Name Role Organization
Dina Bisara Lolong Principal investigator National Institute of Health Research and Development (NIHRD)
Francisca Srioetami Regional coordinator NIHRD
Lamria Pangaribuan Regional coordinator NIHRD
Ainur Rofiq Regional coordinator NIHRD
Retno Kusuma Dewi Laboratory coordinator National TB Programme (NTP)
Irfan Ediyanto Vice laboratory coordinator NTP
Aziza G. Icksan Radiology coordinator Persahabatan hospital
Narendro Arifia Data manager NIHRD
Safrizal Field team leader The National TB Prevalence Survey team (NPS team) of NIHRD
Darmawati Field team leader NPS team of NIHRD
Risnawati Field team leader NPS team of NIHRD
Ade Yoska Tilla Serihati Field team leader NPS team of NIHRD
Elisabeth Bernadeth Field team leader NPS team of NIHRD
Laura Valeria Field team leader NPS team of NIHRD
M.N. Farid Technical assistance (statistics, data management) TB Operational Research Group (TORG)
Pandu Riono Technical assistance (statistics) TORG
Jubaedi Technical assistance (data management) WHO Indonesia
M. Bintari Dwihardiani Technical assistance (survey advisor) WHO Indonesia
Ikushi Onozaki Technical assistance (survey advisor) WHO headquarters
Irwin Law Technical assistance (survey advisor) WHO headquarters
Marina Tadolini Technical assistance (survey advisor) Consultant, Italy
Charalampos Sismanidis Technical assistance (analysis) WHO headquarters
Philippe Glaziou Technical assistance (analysis) WHO headquarters
Symptom screening
Cough ≥2 weeksa 8 377 (12%)
Haemoptysisa 897 (1.3%)
Sputum production 17 001 (25%)
Chest pain 13 614 (20%)
Fever 12 510 (18%)
Total symptom-screen positivea 8 552 (13%)
Eligible for sputum examination 15 446 (23%) Symptom positive, chest X-ray positive 4 459 (29%)
Symptom positive, chest X-ray negative or N/A 4 093 (26%)
Symptom negative, chest X-ray positive 6 743 (44%)
Otherb 151 (1.0%)
Submitted specimens
At least one specimen 15 141 (98%)
Both specimens 14 604 (95%)
Laboratory result
At least one culture result availablec 14 773 (96%)
Total bacteriologically confirmed cases 426 Symptom positive, chest X-ray positive 217 (51%)
Symptom positive, chest X-ray negative or N/A 25 (5.8%)
Symptom negative, chest X-ray positive 184 (43%)
Other 0 (0%)
a
Eligible for sputum collection.
b
151 pregnant women reported at least one of following TB symptoms: cough, haemoptysis, fever, chest pain, night sweats, loss of appetite, shortness of breath.
c
Cultures that were either contaminated and/or missing without a definitive result (i.e. MTB, NTM, negative) were excluded.
d
Definite: MTB confirmed by culture and/or Xpert. Probable: MTB not confirmed by culture and/or Xpert but chest X-ray suggestive of TB.
e
Definite: MTB confirmed by culture and/or Xpert. Probable: For six out of seven, cultures were identified by niacin but not MPT64, with chest X-ray suggestive of TB. One case was a
pregnant participant who was Xpert-positive, but whose culture specimen was contaminated.
132 National TB prevalence surveys 2007–2016
Fig. 1: Participation rate by age and sex Fig. 4: Cluster variation of the number of bacteriologically
confirmed TB casesb
100
35
30
Participation rate (%)
Number of clusters
90 25
20
15
80
10
70 0
15–24 25–34 35–44 45–54 55–64 ≥65 0 1 2 3 4 5 6 7 8 9 10 11
Age group (years) Number of bacteriologically confirmed TB cases
Male Female
Fig. 2: TB prevalence per 100 000 population by age Fig. 5: Ratio of smear-positive TB prevalence to notifications by
age and by sexc
2500 6.0
Prevalence per 100 000 population
4.0
1500
3.0
1000
2.0
500
1.0
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 15–24 25–34 35–44 45–54 55–64 ≥65 Male Female Total
Age group (years) Age group (years) and sex (≥15)
Bacteriologically confirmed TB Smear-positive TB
Fig. 3: Estimated number of bacteriologically confirmed TB cases Fig. 6: Estimates of TB prevalence (all ages, all forms of TB) before
and prevalence per 100 000 population, by agea (in blue) and after (in red) the national TB prevalence surveyd
1600
Prevalence per 100 000 population
300 000
1400
250 000
confirmed TB cases
1200
200 000 1000
a
The estimated number of bacteriologically confirmed TB cases is the product of age-specific prevalence and population estimates from the UN Population Division (2015 revision).
b
The data suggested that the distribution of cases by cluster (blue bars) was significantly different from the theoretical distribution (red line) (mean 2.73, variance 5.09, p<0.05). The
theoretical distribution assumes cases are distributed at random i.e. no clustering effect.
c
Notification rates were estimated using smear-positive pulmonary TB notifications (2013) obtained from the NTP, and population estimates from the UN Population Division (2015
revision).
d
The blue bar denotes the best estimate of prevalence and its range that was indirectly derived from the estimate of incidence previously published by WHO, adjusted to the year of the
prevalence survey based on previously published trends in incidence.
INDONESIA 133
supervision mechanisms, and monitoring and clinic) given the low positive predictive value of
evaluation tools should be prepared for this smear microscopy without confirmatory testing,
purpose; compared with culture; and
• a need for intensified case finding for TB, which • a need for increased funding to implement all
has since become one of the major strategies of of the policy and programmatic measures listed
the NTP; above, especially given the major finding of the
• a need for improved access to health facilities, survey that the burden of TB disease was double
including via provision of universal health the level previously estimated.
insurance, so that symptomatic individuals
would be more likely to seek immediate
treatment; Major successes, challenges and lessons
• a need for the general population to be made learned
more aware that anti-TB treatment in standard
health facilities is free of charge, to encourage The overarching major success was that the survey was
people to seek care promptly; successfully implemented with high quality and a high
• a need to use chest X-rays more widely, to participation rate, and that it was the first in the country
improve case detection; for example, as part of for decades to include chest X-ray screening combined
community outreach or among key populations,
with diagnosis using culture as well as smear microscopy.
such as prisoners, people living with HIV, people
with comorbidities and the elderly; Several major challenges included those listed below.
• a need to increase the number of qualified
laboratories to improve access to, and the speed • The procurement process for chest X-ray
of, diagnosis, especially in rural areas where equipment was slow. It took 18 months and
geographical barriers hinder the rapid delivery delayed the start of the survey. Subsequently,
of specimens to referral laboratories; setting up and using the chest X-ray equipment
• a need for the NTP to implement innovative in the field generated some problems with
strategies to supervise TB service quality in all data collection. These were partly alleviated by
health facilities, including those in the private the availability of in-country servicing of the
sector; equipment, which facilitated timely repairs and
troubleshooting.
• a need to understand that a positive smear result
should not be the basis for providing anti-TB • Collecting and processing sputum specimens
treatment (especially in the context of active was demanding, and some contamination of
case finding in the community rather than in a specimens occurred. Morning specimens had
higher rates of contamination (431 [3%] of
14 569 specimens) than spot specimens (47
[1%] of 4433).
• Culture failed to grow in some settings, perhaps
because of geographical challenges (e.g. poor
road conditions and the difficulty of maintaining
a cold chain in the context of high temperatures
and humidity), poor sample handling and the
limited number of laboratories.
• The quality of laboratories may have varied,
even though laboratory experts evaluated
and validated the performance quality of the
laboratories used in the survey.
• Limited culture capacity meant that it was only
possible to culture two specimens for every
participant who submitted sputum samples in
one third of survey clusters; in the remaining
survey clusters, only one specimen was
cultured. To mitigate this problem, Xpert MTB/
RIF was used when culture failed (e.g. from
contamination in all tubes).
KENYA
2015–2016
Summary statistics
Participation rate 83%
Symptom screening
Cough ≥2 weeksb 4 137 (6.6%)
Sputum production 3 256 (5.2%)
Haemoptysis 393 (0.6%)
Chest pain 12 290 (19%)
Fever 4 937 (7.8%)
Total symptom-screen positivea 4 137 (6.6%)
Eligible for sputum examination 9 715 (15%) Symptom positive, chest X-ray positive 1 241 (13%)
Symptom positive, chest X-ray negative or N/A 2 896 (30%)
Symptom negative, chest X-ray positive 5 184 (53%)
Otherc 394 (4.1%)
Submitted specimens
At least one specimen 9 120 (94%)
Both specimens 7 763 (80%)
Laboratory result
At least one culture result availabled 8 761 (90%)
At least one Xpert MTB/RIF result available 8 936 (92%)
Total bacteriologically confirmed cases 305 Symptom positive, chest X-ray positive 115 (38%)
Symptom positive, chest X-ray negative or N/A 32 (10%)
Symptom negative, chest X-ray positive 154 (50%)
Otherc 4 (1.3%)
a
429 participants declined a chest X-ray, and 137 participants did not have a chest X-ray due to malfunctioning X-ray machines.
b
Eligible for sputum collection.
c
Chest X-ray exempted and symptom-screen negative.
d
Cultures that were either contaminated and/or missing without a definitive result (i.e. MTB, NTM, negative) were excluded.
e
Definite: MTB confirmed by culture and/or Xpert. Probable: no definition.
140 National TB prevalence surveys 2007–2016
Fig. 1: Participation rate by age and sex Fig. 4: Cluster variation of the number of bacteriologically
confirmed TB casesb
100
20
90
Participation rate (%)
Number of clusters
15
80
10
70
5
60 0
15–24 25–34 35–44 45–54 55–64 ≥65 0 1 2 3 4 5 6 7 8 9 10 11 12 13
Age group (years) Number of bacteriologically confirmed TB cases
Male Female
Fig. 2: TB prevalence per 100 000 population by age Fig. 5: Ratio of bacteriologically confirmed TB prevalence to
notifications by age and by sexc
1000 7.0
Prevalence per 100 000 population
900
6.0
Prevalence : notification ratio
800
700 5.0
600
4.0
500
400 3.0
300 2.0
200
1.0
100
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 15–24 25–34 35–44 45–54 55–64 ≥65 Male Female Total
Age group (years) Age group (years) and sex (≥15)
Bacteriologically confirmed TB Smear-positive TB
Fig. 3: Estimated number of bacteriologically confirmed TB cases Fig. 6: Estimates of TB prevalence (all ages, all forms of TB) before
and prevalence per 100 000 population, by agea (in blue) and after (in red) the national TB prevalence surveyd
60 000 800
Estimated number of bacteriologically
700
50 000
600
confirmed TB cases
40 000
500
30 000 400
300
20 000
200
10 000
100
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 200 300 400 500
Age group (years) Prevalence per 100 000 population
a
The estimated number of bacteriologically confirmed TB cases is the product of age-specific prevalence and population estimates from the UN Population Division (2015 revision).
b
The data suggested that the distribution of cases by cluster (blue bars) was significantly different from the theoretical distribution (red line) (mean 3.08, variance 7.63, p<0.05). The
theoretical distribution assumes cases are distributed at random i.e. no clustering effect.
c
Notification rates were estimated using bacteriologically confirmed pulmonary TB notifications (2015) obtained from the NTP, and population estimates from the UN Population Division
(2015 revision).
d
The blue bar denotes the best estimate of prevalence and its range that was indirectly derived from the estimate of incidence previously published by WHO, adjusted to the year of the
prevalence survey based on previously published trends in incidence.
KENYA 141
suggested that the screening criteria used in Major successes, challenges and lessons
routine clinical settings should be reviewed and learned
that expanded use of chest X-ray as a screening
tool should be considered; The national TB prevalence survey in Kenya 2015–
• since more than half of the bacteriologically 2016 was successfully implemented. This was the first
confirmed cases were smear-negative and were African survey to use Xpert MTB/RIF and culture for
diagnosed by culture or Xpert MTB/RIF (or
both), use of diagnostic tools besides smear all participants who screened positive, and despite the
microscopy should be expanded; resulting increase in workload for the national reference
• about 70% of participants who reported a chronic laboratory, the survey demonstrated that using both
cough did not seek care, even though the Kenya tests was feasible. Good communication throughout the
Demographic Health Survey of 2014 found survey contributed to these achievements. This included
that about 80% of those aged 15–49 years knew high levels of community engagement (especially during
that TB is spread through the air by coughing visits prior to survey field operations) that fostered
(11); nonetheless, the general population may
be unaware of the actual symptoms of TB, and survey participation, and regular meetings and close
consequently delay seeking care; this suggested collaboration between the NTLD-P, various implementing
that improving community awareness about TB partners and technical agencies that facilitated effective
symptoms as well as the availability of free TB project management and ownership of the final survey
services at public health facilities could help to results.
improve health care seeking behaviour;
• the relatively high proportion of symptomatic Challenges faced during the survey, and associated
cases who had sought some care before the lessons learned, included those listed below.
survey but were not diagnosed with TB
suggested a need to improve access to diagnostics • The procurement process for digital chest X-ray
and treatment, as well as a need to review the machines by the WHO Regional Office for
screening algorithm and develop strategies Africa was lengthy, which delayed the start of
to improve patient awareness and health-care the survey by more than a year.
provider knowledge of TB symptoms; and
• the prevalence of HIV infection among
bacteriologically confirmed TB cases with
known HIV status (17%; 41/2451) was lower
than that reported among notified TB cases
(33%) (12); this suggested that while there has
been a strong focus on the TB/HIV programme,
a large TB burden exists among those who are
HIV-negative, for which more programmatic
action is required.
1
41 were HIV-positive and 204 were HIV-negative.
Photo credit: Marina Tadolini
144 National TB prevalence surveys 2007–2016
LAO PEOPLE’S
DEMOCRATIC REPUBLIC
2010–2012
Summary statistics
Participation rate 85%
Symptom screening
Cough ≥2 weeksa 3 211 (8.2%)
Haemoptysisa 991 (2.5%)
Sputum production N/A
Chest pain N/A
Fever N/A
Total symptom-screen positivea 3 239 (8.3%)
Eligible for sputum examination 6 346 (16%) Symptom positive, chest X-ray positive 1 312 (21%)
Symptom positive, chest X-ray negative or N/A 1 927 (30%)
Symptom negative or N/A, chest X-ray positiveb 3 107 (49%)
Other N/A
Submitted specimens
At least one specimen 6 290 (99%)
Both specimens 6 253 (98%)
Laboratory result
At least one culture result availablec 6 251 (99%)
Total bacteriologically confirmed cases 237 Symptom positive, chest X-ray positive 111 (47%)
Symptom positive, chest X-ray negative or N/A 7 (3.0%)
Symptom negative, chest X-ray positive 119 (50%)
Other N/A
a
Eligible for sputum collection.
b
Symptom-screening results were not available for eight people.
c
Cultures that were either contaminated and/or missing without a definitive result (i.e. MTB, NTM, negative) were excluded.
d
Definite: MTB confirmed by culture. Probable: MTB not confirmed by culture but chest X-ray suggestive of TB.
e
Definite: MTB confirmed by two culture specimens, or by one culture with chest X-ray suggestive of TB. Probable: MTB confirmed by one culture with five or more colonies without chest
X-ray suggestive of TB, or by one culture with less than five colonies and chest X-ray suggestive of TB.
148 National TB prevalence surveys 2007–2016
Fig. 1: Participation rate by age and sex Fig. 4: Cluster variation of the number of bacteriologically
confirmed TB casesb
100
8
Participation rate (%)
Number of clusters
90 6
4
80
2
70 0
15–24 25–34 35–44 45–54 55–64 ≥65 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16
Age group (years) Number of bacteriologically confirmed TB cases
Male Female
Fig. 2: TB prevalence per 100 000 population by age Fig. 5: Ratio of smear-positive TB prevalence to notifications by
age and by sexc
3500 4.5
Prevalence per 100 000 population
Fig. 3: Estimated number of bacteriologically confirmed TB cases Fig. 6: Estimates of TB prevalence (all ages, all forms of TB) before
and prevalence per 100 000 population, by agea (in blue) and after (in red) the national TB prevalence surveyd
6 000 3000
Estimated number of bacteriologically
5 000 2500
confirmed TB cases
4 000 2000
3 000 1500
2 000 1000
1 000 500
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 0 200 400 600 800
Age group (years) Prevalence per 100 000 population
a
The estimated number of bacteriologically confirmed TB cases is the product of age-specific prevalence and population estimates from the UN Population Division (2015 revision).
b
The data suggested that the distribution of cases by cluster (blue bars) was significantly different from the theoretical distribution (red line) (mean 4.74, variance 15.5, p<0.05). The
theoretical distribution assumes cases are distributed at random i.e. no clustering effect.
c
Notification rates were estimated using notifications obtained from the WHO global TB database, and population estimates from the UN Population Division (2015 revision).
d
The blue bar denotes the best estimate of prevalence and its range that was indirectly derived from the estimate of incidence previously published by WHO, adjusted to the year of the
prevalence survey based on previously published trends in incidence.
LAO PEOPLE’S DEMOCRATIC REPUBLIC 149
A total of 237 bacteriologically confirmed pulmonary • of the 113 bacteriologically confirmed and 67
TB cases was identified, including 107 cases of smear- smear-positive TB survey cases that screened
positive TB. The prevalence of smear-positive TB was 278 positive for symptoms and were not on anti-TB
treatment at the time of the survey, 42 (37%) and
(95% CI: 199–356) per 100 000 population (among those 27 (43%), respectively, had previously sought
aged ≥15 years) and for bacteriologically confirmed TB care in a public or private health facility for their
it was 595 (95% CI: 457–733) per 100 000 population. symptoms.
Prevalence in rural clusters was higher than in urban
clusters.
Implications of results
Other key results were:
Based on survey results, WHO estimated that the
• the male to female ratio for TB prevalence
prevalence of TB (all ages, all forms of TB) in 2011 was
was 2.8 for smear-positive TB and 2.3 for
bacteriologically confirmed TB; 540 (95% CI: 353–767) per 100 000 population; estimates
• prevalence per 100 000 population increased with for previous years were also revised. The 2011 estimate
age; the absolute number of bacteriologically was almost double the pre-survey WHO estimate that
confirmed TB cases was highest in the group was used in the initial sampling design for the survey
aged 65 years or more, and consistently high in (289 per 100 000 population in 2007). The updated
other age groups; estimate of prevalence in 2011 was 64% lower than the
• among bacteriologically confirmed TB cases, revised 1990 estimate of 1490 (95% CI: 746–2490) per
50% were symptom-screen positive, and among
100 000 population, indicating that the country had
the smear-positive cases, 66% were symptom-
screen positive; met the Millennium Development Goal target related
• for smear-positive pulmonary TB, the ratio of to TB (that incidence should be falling by 2015) and the
prevalence to notifications (P:N ratio) was 3.5 Stop TB Partnership target of halving TB prevalence
overall, but varied from 2.4 in those aged 35–44 between 1990 and 2015. Although it was not possible to
and 55–64 years to 4.2 in the age group 15–24 quantify the relative contribution of the various factors
years; the ratio was higher for men than for that led to this decline, those considered to have played
women (4.3 versus 2.6);
an important role included the countrywide expansion
• among bacteriologically confirmed TB cases, 6% of DOTS and the associated availability of free anti-TB
had no previous history of anti-TB treatment,
and only 3% were on anti-TB treatment at the medication, increases in GNI per capita (from US$ 190 in
time of the survey; and 1990 to US$ 1120 in 2011) and improvements in overall
living conditions (the Human Development Index was people suggested a reluctance to seek care,
0.397 in 1990 and 0.554 in 2011) (6,7). possibly linked to health services that were
not meeting the needs or expectations of this
In common with other countries in Asia, the survey population.
showed a markedly ageing TB epidemic, with prevalence • Diagnostic services should be improved,
in those aged 65 years or more as much as 10 times progressing from a reliance on sputum smear
the level in those under 25 years of age. This suggested microscopy to greater use of chest X-ray and
either culture or rapid tests (e.g. Xpert® MTB/
that transmission of infection was in decline and that RIF).
endogenous re-activation of TB in older age groups, as
• A smear-positive test result does not always
opposed to new infections in the younger population, indicate TB disease, especially in a community
was likely to make a growing contribution to the overall (as opposed to a clinic) setting. In active TB case
TB burden. finding, TB cannot be reliably diagnosed based
on smear examination alone.
The survey had several major programmatic, policy and • The ability of health-care workers to clinically
funding implications, which included those listed below. recognize TB disease should be improved, given
that one-third of symptomatic survey cases had
• It was clear that further efforts were needed to already sought care in a public or private health
close gaps in case detection. The gap between facility, before being detected by the survey.
prevalence and official notifications of new
cases (the P:N ratio) was among the largest Survey findings were used to prepare a funding application
found in any survey conducted between 2009 to the Global Fund to fight AIDS, TB and malaria, and to
and 2016. The particularly high P:N ratio for develop a new national strategic plan for TB.
men compared with women, and for people
aged under 35 years and 65 years or more, also
indicated a need for interventions targeted to
specific subpopulations. Major successes, challenges and lessons
• In addition to programmatic efforts, the high learned
P:N ratio indicated a broader need to strengthen
the health system, and the overall availability Major successes included completion of the survey with
and acceptability of diagnostic and treatment a small budget (US$ 1.3 million), a high participation
services. The chronicity of symptoms in older rate and the fact that many NTP staff were able to see,
first-hand and often for the first time, the challenges
of TB surveillance and case management in the more
remote areas of the country. The survey was successfully
implemented with the use of entirely conventional
or traditional survey methods (i.e. paper-based data
collection instruments, conventional chest X-ray systems
and the Kudoh culture method with Ogawa media).
References
1. The World Bank (https://data.worldbank.org/country, accessed
April 2017).
2. UNAIDS (http://aidsinfo.unaids.org/, accessed April 2017).
3. World Health Organization. Global Tuberculosis Database. 2017.
(http://www.who.int/tb/country/en/, accessed April 2017).
4. WHO Tuberculosis Programme. (1994). WHO Tuberculosis
Programme: framework for effective tuberculosis
control. World Health Organization. (http://www.who.int/iris/
handle/10665/58717, accessed January 2018).
5. World Health Organization. Global tuberculosis programme.
Global tuberculosis control report 1997. Geneva: WHO; (https://
apps.who.int/iris/bitstream/handle/10665/63354/WHO_
TB_97.225_(part1).pdf?sequence=1, accessed January 2018).
6. Law I, Sylavanh P, Bounmala S, Nzabintwali F, Paboriboune P, Iem
V et al. The first national tuberculosis prevalence survey of Lao
PDR (2010–2011). Trop Med Int Health. 2015;20(9):1146–1154
(https://www.ncbi.nlm.nih.gov/pubmed/25939366, accessed July
2017).
7. Report of the first national tuberculosis prevalence survey in Lao
PDR (2010–2011). Vientiane, Lao PDR: National Tuberculosis
Centre, Department of Communicable Diseases, Ministry of
Health - Lao PDR; 2014.
8. World Health Organization. Global tuberculosis report
2013. Geneva: WHO; 2013 (http://apps.who.int/iris/
bitstream/10665/91355/1/9789241564656_eng.pdf, accessed
January 2018).
9. World Health Organization. Tuberculosis prevalence surveys:
a handbook (WHO/HTM/TB/2010.17). Geneva: WHO; 2011
(https://apps.who.int/iris/bitstream/handle/10665/44481/
9789241548168_eng.pdf, accessed August 2017).
153
MALAWI
2013–2014
Summary statistics
Participation rate 81%
Key people
Name Role Organization
James Mpunga Principal investigator National TB Control Programme (NTP)
Rhoda Banda Survey coordinator NTP
Alister Munthali Co-principal investigator Centre for Social Research, University of Malawi
Damson Kathyola Co-investigator Ministry of Health (MOH)
Isaiah Dambe Co-investigator NTP
Ishmael Nyasulu Co-investigator WHO Malawi
Suzgo Mzumara Co-investigator (radiologist) MOH
George B. Samuti Chief of laboratory Central Reference Laboratory, MOH
Daniel Nyangulu Radiology coordinator MOH
Charles Mandambwe Data manager NTP
Masy Chiocha Data manager Centre for Social Research, University of Malawi
Andrew Dimba Field team leader NTP
Henry Kanyerere Field team leader NTP
Lameck Mlauzi Field team leader NTP
Sidon Konyani Technical assistance (epidemiologist) Centre for Social Research, University of Malawi
Julia Ershova Technical assistance (survey advisor) US Centers for Disease Control and Prevention (CDC)
Irwin Law Technical assistance (survey advisor) WHO headquarters
Patrick Moonan Technical assistance (survey advisor) US Centers for Disease Control and Prevention (CDC)
Wilfred Nkhoma Technical assistance (survey advisor) WHO Regional Office for Africa (AFRO)
Ikushi Onozaki Technical assistance (survey advisor) WHO headquarters
Peou Satha Technical assistance (radiology) CENAT, Cambodia
Sian Floyd Technical assistance (analysis) London School of Hygiene & Tropical Medicine
a
The boundaries and names shown and the designations used on this map do not
imply the expression of any opinion whatsoever on the part of the World Health
Organization concerning the legal status of any country, territory, city or area or of
its authorities, or concerning the delimitation of its frontiers or boundaries.
154 National TB prevalence surveys 2007–2016
Symptom screening
Cough ≥2 weeks 1 192 (3.8%)
Cough ≥1 week 2 047 (6.5%)
Haemoptysis ≥1 week 69 (0.2%)
Sputum production ≥1 week 1 101 (3.5%)
Chest pain ≥1 week 1 039 (3.3%)
Weight loss ≥1 week 370 (1.2%)
Night sweats ≥1 week 415 (1.3%)
Fatigue ≥1 week 496 (1.6%)
Fever ≥1 week 401 (1.3%)
Chest X-ray screening
Shortness of breath ≥1 week 431 (1.4%)
Normal 30 231 (96%)
Abnormala 1 016 (3.2%)
Any symptoms (above) ≥1 weeka 2 715 (8.6%)
Other abnormality 312 (1.0%)
Result not available 2 (<0.01%)
Total chest X-rays taken 31 561
Eligible for sputum examination 3 432 (11%) Symptom positive, chest X-ray positive 381 (11%)
Symptom positive, chest X-ray negative or N/A 2 334 (68%)
Symptom negative, chest X-ray positive 717b (21%)
Other N/A
Submitted specimens
At least one specimen 3 368 (98%)
Both specimens 3 200 (93%)
Laboratory result
At least one culture result availablec 3 327 (97%)
Total bacteriologically confirmed cases 132 Symptom positive, chest X-ray positive 25 (19%)
Symptom positive, chest X-ray negative or N/A 67 (51%)
Symptom negative, chest X-ray positive 40f (30%)
Other N/A
a
Eligible for sputum collection.
b
Out of 717, 82 participants were defined as “chest X-ray abnormal but not suggestive of TB”, but were nonetheless requested to submit sputum samples. Teams were not consistent in
their approach to sputum submission for participants with an abnormal chest X-ray (suggestive of TB or other abnormality).
c
Cultures that were either contaminated and/or missing without a definitive result (i.e. MTB, NTM, negative) were excluded.
d
Smear-positive was defined as a specimen with ≥4 AFBs. Definite: MTB confirmed by culture and/or Xpert. Probable: no definition.
e
Definite: MTB confirmed by culture and/or Xpert. Probable: no definition.
f
Four out of 40 were “abnormal but not suggestive of TB” on chest X-ray.
156 National TB prevalence surveys 2007–2016
Fig. 1: Participation rate by age and sex Fig. 4: Cluster variation of the number of bacteriologically
confirmed TB casesb
100
25
90
Participation rate (%)
20
Number of clusters
15
80
10
70
5
60 0
15–24 25–34 35–44 45–54 55–64 ≥65 0 1 2 3 4 5 6 7 8 9 10 11 12 13
Age group (years) Number of bacteriologically confirmed TB cases
Male Female
Fig. 2: TB prevalence per 100 000 population by age Fig. 5: Ratio of smear-positive TB prevalence to notifications by
age and by sexc
2500 10.0
Prevalence per 100 000 population
Fig. 3: Estimated number of bacteriologically confirmed TB cases Fig. 6: Estimates of TB prevalence (all ages, all forms of TB) before
and prevalence per 100 000 population, by agea (in blue) and after (in red) the national TB prevalence surveyd
14 000 1800
Estimated number of bacteriologically
12 000 1600
1400
10 000
confirmed TB cases
1200
8 000 1000
6 000 800
600
4 000
400
2 000
200
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 100 200 300 400
Age group (years) Prevalence per 100 000 population
a
The estimated number of bacteriologically confirmed TB cases is the product of age-specific prevalence and population estimates from the UN Population Division (2015 revision).
b
The data suggested that the distribution of cases by cluster (blue bars) was significantly different from the theoretical distribution (red line) (mean 1.78, variance 5.82, p<0.05). The
theoretical distribution assumes cases are distributed at random i.e. no clustering effect.
c
Notification rates were estimated using smear-positive pulmonary TB notifications (2013) obtained from the NTP, and population estimates from the UN Population Division (2015
revision).
d
The blue bar denotes the best estimate of prevalence and its range that was indirectly derived from the estimate of incidence previously published by WHO, adjusted to the year of the
prevalence survey based on previously published trends in incidence.
MALAWI 157
Major successes, challenges and lessons • Advice about sputum examination, which was
learned not appropriate in the context of a prevalence
survey, was provided to the central reference
The major overarching success was that the first national laboratory by an expert not directly involved
TB prevalence survey in Malawi was successfully in the survey. Although the intention was to
conduct direct smear microscopy (to allow
implemented, with a good participation rate. This was comparison with cases routinely detected
done using conventional tools (e.g. film-based portable by health services), in practice, centrifuged
chest X-ray equipment and paper-based data collection sediment was used for light-emitting diode
tools) as dictated by the relatively small budget provided (LED) fluorescent microscopy (FM). This was a
by the Global Fund and the national government. protocol violation and resulted in many scanty
smear-positive results. In 62% of the smear-
Other successes included excellent collaboration between positive specimens, Mycobacterium tuberculosis
could not be detected by either culture or
the NTP and the University of Malawi’s Centre for
Xpert® MTB/RIF. In consultation with leading
Social Research, and between the survey team, NTP and laboratory experts working with the Global
technical partners, including the United States Centers Laboratory Initiative and the Supranational
for Disease Control and Prevention (US-CDC), the Reference Laboratory for Malawi, the survey
London School of Hygiene and Tropical Medicine, and re-categorized scanty 1–3 acid-fast bacilli (AFB)
WHO, which strongly facilitated survey implementation. smears by concentrated LED FM as insignificant,
and did not classify them as smear-positive.
Given the challenges faced in some other countries, data
• There were incidents of laboratory cross-
management was effective, with on-site data entry in the
contamination. Of the specimens from 192
field, timely data cleaning and validation, and continuous participants who were positive by culture or
support from the US-CDC. The final validated data set Xpert MTB/RIF (or both), one third were found
was available within a few months of the completion of to be clustered in the laboratory logbook; that
field operations. is, consecutive specimens were positive for
M. tuberculosis. Following an extensive panel
Challenges faced during the survey included those listed review of laboratory documents, chest X-rays
below. and other information (e.g. data on family
contacts), some laboratory cross-contamination
• It took two years to secure government funding was suspected. The panel concluded that a
to support field activities and more than a year to total of 60 participants with positive laboratory
procure conventional X-ray equipment. During results should not be counted as TB cases. Of
the survey, interruptions to disbursement of these 60, 29 had a very strong suspicion of cross-
funds caused some delays in field operations. contamination and the remaining 31 had a single
• A change of the lead technical adviser during the weak positive result (i.e. culture of fewer than
final stages of survey preparations meant that five colonies) without other supportive evidence
the survey team did not benefit from technical of TB disease other than symptoms. The final
assistance during the pilot survey and the early survey results may have underestimated TB
stages of field operations. This contributed to prevalence.
some initial issues with data management, but
these were subsequently rectified.
• The suboptimal environment in which chest
X-rays were often taken. X-ray units, and the
chemical liquids used to develop and fix films,
tended to overheat in hot conditions. Field
operations were sometimes delayed while the
units were allowed to cool down. In addition,
individual identifiers were written on the films
by hand after the images had been developed.
This caused problems with later archiving and
retrieval of images for central reading, and
potentially caused some images to be mislabelled
(i.e. labelled with the wrong participant's name).
References
1. The World Bank (https://data.worldbank.org/country, accessed
April 2017).
2. UNAIDS (http://aidsinfo.unaids.org/, accessed April 2017).
3. World Health Organization. Global Tuberculosis Database. 2017.
(http://www.who.int/tb/country/en/, accessed April 2017).
4. Malawi health sector strategic plan 2011–2016: Moving
towards equity and equality. Ministry of Health, Government
of Malawi; 2011 (http://www.healthpromotion.gov.mw/index.
php/2013-08-12-12-52-31/2013-08-12-12-52-32/policies-
strategies?download=6:malawi-health-sector-strategic-
plan-2011-2016, accessed July 2017).
5. World Health Organization. Tuberculosis prevalence surveys:
a handbook (WHO/HTM/TB/2010.17). Geneva: WHO; 2011
(https://apps.who.int/iris/bitstream/handle/10665/44481/
9789241548168_eng.pdf, accessed August 2017).
6. World Health Organization. Global tuberculosis report
2013. Geneva: WHO; 2013 (http://apps.who.int/iris/
bitstream/10665/91355/1/9789241564656_eng.pdf, accessed
January 2018).
161
MONGOLIA
2014–2015
Summary statistics
Participation rate 84%
Key people
Name Role Organization
Tugsdelger Sovd Principal investigator Ministry of Health
Puntsag Banzragch Central panel team National Center for Communicable Diseases
Naranbat Nyamadawa Survey consultant Mongolian Anti-Tuberculosis Coalition
Naranzul Dambaa Survey coordinator National Center for Communicable Diseases
Tsolmon Boldoo Data manager National Center for Communicable Diseases
Bayasgalan Purev Central radiologist National Center for Communicable Diseases
Buyankhishig Burneebaatar Laboratory doctor National Tuberculosis Reference Laboratory
Oyuntuya Tumenbayar Laboratory doctor National Tuberculosis Reference Laboratory
Ikushi Onozaki Technical assistance (survey advisor) WHO headquarters
Yasunori Ichimura Technical assistance (survey advisor) Chiba University, Japan
Norio Yamada Technical assistance (survey advisor) Research Institute of Tuberculosis, Japan Anti-Tuberculosis
Association (RIT/JATA)
M. Bintari Dwihardiani Technical assistance (survey advisor) WHO Indonesia
M.N. Farid Technical assistance (survey advisor) Central Bureau of Statistics, Jakarta
Satoshi Mitarai Technical assistance (laboratory advisor) RIT/JATA
Soe Nyunt-U Technical/financial support WHO Mongolia
Narantuya Jadambaa Technical/financial support WHO Mongolia
a
The boundaries and names shown and the designations used on this map do not
imply the expression of any opinion whatsoever on the part of the World Health
Organization concerning the legal status of any country, territory, city or area or of
its authorities, or concerning the delimitation of its frontiers or boundaries.
162 National TB prevalence surveys 2007–2016
a
Direct digital radiography by chest X-ray car and mobile apparatus.
Health-care seeking behaviour among
Number %
participants who were symptom-screen positive
Laboratory methodology
Participants who were symptom-screen 2 546 –
Smear Two samples (spot, morning): direct positivea
preparation, FM (LED, auramine stain).
Location of care sought
ZN for those smears that were FM positve
• Consulted medical facility 950 37
Culture Two samples (spot, morning): direct
preparation, Ogawa media Public facility 920 97
Identification of MTB PNB, niacin test Private facility 30 3.1
TB drug susceptibility test MTBDRplus testa • Pharmacy 222 8.7
Xpert® MTB/RIF Done for smear-positive specimens (from • Traditional medicine hospital 2 0.1
the early phase of field operations)b • Others 59 2.3
HIV test Not done • Unspecified 104 4.1
a
Financial support was provided by Science and Technology Foundation Mongolia. No action taken 1 179 46
b
Xpert MTB/RIF was done for 84 out of 92 smear-positive specimens. Unknown 30 1.2
a
Cough ≥2 weeks.
Analysis and reporting
Field data collection Paper Survey participants currently on TB treatment Number %
Database Microsoft Access
® Total participants currently on TB treatment 129 –
Method of analysis MI+IPW • Treated in the public sector 126 98
Results first published in a report/paper December 2016 • Treated in the private sector 0 0
Official dissemination event March 2017 • Treated in other sector 3 2.3
Bacteriologically confirmed TB cases 11 4.4
detected by the survey who were currently
on TB treatment
MONGOLIA 163
Symptom screening
Cough ≥2 weeksa 2 546 (5.1%)
Haemoptysis 777 (1.5%)
Sputum production 6 481 (13%)
Chest pain 6 451 (13%)
Fever 1 280 (2.6%)
Total symptom-screen positivea 2 546 (5.1%)
Eligible for sputum examination 10 359 (21%) Symptom positive, chest X-ray positive 817 (7.9%)
Symptom positive, chest X-ray negative or N/A 1 729 (17%)
Symptom negative, chest X-ray positive 7 064 (68%)
Otherb 749 (7.2%)
Submitted specimens
At least one specimen 9 546 (92%)
Both specimens 9 473 (91%)
Laboratory result
At least one culture result availablec 9 527 (92%)
Total bacteriologically confirmed cases 248 Symptom positive, chest X-ray positive 44 (18%)
Symptom positive, chest X-ray negative or N/A 7 (2.8%)
Symptom negative, chest X-ray positive 194 (78%)
Otherb 3 (1.2%)
a
Eligible for sputum collection.
b
Chest X-ray exempted and symptom-screen negative.
c
Cultures that were either contaminated and/or missing without a definitive result (i.e. MTB, NTM, negative) were excluded.
d
Definite: MTB confirmed by culture and/or Xpert. Probable: MTB not confirmed by culture and/or Xpert but chest X-ray suggestive of TB.
e
Definite: MTB confirmed by culture. Probable: one scanty culture-positive without chest X-ray suggestive of TB but with chronic cough, and confirmed as TB cases by referral facilities.
164 National TB prevalence surveys 2007–2016
Fig. 1: Participation rate by age and sex Fig. 4: Cluster variation of the number of bacteriologically
confirmed TB casesb
100 25
90 20
Participation rate (%)
Number of clusters
15
80
10
70
5
60 0
15–24 25–34 35–44 45–54 55–64 ≥65 0 1 2 3 4 5 6 7 8 9 10
Age group (years) Number of bacteriologically confirmed TB cases
Male Female
Fig. 2: TB prevalence per 100 000 population by age Fig. 5: Ratio of smear-positive TB prevalence to notifications by
age and by sexc
1000 4.0
Prevalence per 100 000 population
900
3.5
Prevalence : notification ratio
800
3.0
700
600 2.5
500 2.0
400
1.5
300
1.0
200
100 0.5
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 15–24 25–34 35–44 45–54 55–64 ≥65 Male Female Total
Age group (years) Age group (years) and sex (≥15)
Bacteriologically confirmed TB Smear-positive TB
Fig. 3: Estimated number of bacteriologically confirmed TB cases Fig. 6: Estimates of TB prevalence (all ages, all forms of TB) before
and prevalence per 100 000 population, by agea (in blue) and after (in red) the national TB prevalence surveyd
4 000 700
Estimated number of bacteriologically
3 500 600
3 000
500
confirmed TB cases
2 500
400
2 000
300
1 500
200
1 000
500 100
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 250 500 750
Age group (years) Prevalence per 100 000 population
a
The estimated number of bacteriologically confirmed TB cases is the product of age-specific prevalence and population estimates from the UN Population Division (2015 revision).
b
The data suggested that the distribution of cases by cluster (blue bars) was significantly different from the theoretical distribution (red line) (mean 2.53, variance 5.49, p<0.05). The
theoretical distribution assumes cases are distributed at random i.e. no clustering effect.
c
Notification rates were estimate of using smear-positive pulmonary TB notifications (2014) obtained from the NTP, and population estimates from the UN Population Division (2015
revision).
d
The blue bar denotes the best estimated prevalence and its range that was indirectly derived from the estimate of incidence previously published by WHO, adjusted to the year of the
prevalence survey based on previously published trends in incidence.
MONGOLIA 165
new diagnostic tools beyond smear such as Xpert® MTB/ Survey successes were facilitated by excellent leadership
RIF should be introduced, and that diagnostic services from the NTP; good collaboration between the Ministry
should be decentralized across the country. of Health, the survey team and local authorities and health
centres during field operations; the appointment of a full-
Because underreporting of detected cases to national time survey coordinator and data management team
authorities probably also contributed to the gap between early in the process; and close collaboration with external
prevalence and notifications, another identified priority partners including the Global Fund to Fight AIDS,
was to strengthen the electronic reporting system with TB and Malaria, the WHO country office and WHO
appropriate supervision. headquarters. Good technical assistance throughout
While strengthening TB control efforts in general, the survey preparations and implementation helped to
importance of giving particular attention to risk groups ensure the high quality of the survey, especially given that
with a high TB prevalence and to remote areas with poorer Mongolia had no previous experience of undertaking a
access was also recognized, and reflected in Mongolia’s survey of this magnitude. Experts in prevalence surveys
5-year national TB strategic plan for 2016–2020. visited more than 10 times during the course of the
survey, and provided regular assistance throughout,
from protocol development to reporting of final results.
Good financial planning (especially with financial
Major successes, challenges and lessons contributions from the government) was also vital in
learned ensuring the smooth progress of the survey, including
Major successes included carrying out the first nationwide the ongoing maintenance of chest X-ray machines during
TB prevalence survey in Mongolia, and the first TB- field operations.
related survey in the country for more than 50 years; Major challenges included interruptions to field
achieving high population coverage (100%), with a operations during the long winter season; a lower
participation rate of 84% and a sputum collection rate of participation rate among the young, men and urban
more than 90%; reaching clusters located in remote areas clusters, especially in the wealthier parts of large cities;
with limited infrastructure; and examining all specimens and postponement of field operations following a
to a high standard in one national reference laboratory. breakdown of both X-ray machines, since no backup
Specifically, specimens from remote clusters were machines were available.
transported using a nationwide sputum transportation
system established in 2008; the overall culture (Ogawa)
contamination rate was low (1.9%; 696/37 322 tubes);
and all laboratory results were available, with an
overall recovery rate of 87% (80 culture Mycobacterium
tuberculosis [MTB]-positive among 92 smear-positive).
References
1. The World Bank (https://data.worldbank.org/country, accessed
April 2017).
2. 2010 population and housing census of Mongolia. Census
monograph, Ulaanbaatar: National Statistical Office of Mongolia;
2011.
3. UNAIDS (http://aidsinfo.unaids.org/, accessed April 2017).
4. World Health Organization. Global Tuberculosis Database. 2017.
(http://www.who.int/tb/country/en/, accessed April 2017).
5. WHO Tuberculosis Programme. (1994). WHO Tuberculosis
Programme: framework for effective tuberculosis
control. World Health Organization. (http://www.who.int/iris/
handle/10665/58717, accessed January 2018).
6. World Health Organization. Global tuberculosis programme.
Global tuberculosis control report 1997. Geneva: WHO; (https://
apps.who.int/iris/bitstream/handle/10665/63354/WHO_
TB_97.225_(part1).pdf?sequence=1, accessed January 2018).
7. Report of the first National Tuberculosis Prevalence Survey in
Mongolia (2014–2015). Ulaanbaatar city, Mongolia: Ministry of
Health; 2016.
8. Results of screening for TB in 1959–1961 in Mongolia. Mongolian
Journal of Infectious Diseases. 2012;4(47).
9. WHO Regional Office for the Western Pacific. The regional
strategic plan to stop TB in the Western Pacific. Manila,
Philippines: WHO; 2000 (https://iris.wpro.who.int/bitstream/
handle/10665.1/9849/Regional_Strategic_Plan_to_Stop_TB_
WP_eng.pdf, accessed July 2017).
10. World Health Organization. Tuberculosis prevalence surveys:
a handbook (WHO/HTM/TB/2010.17). Geneva: WHO; 2011
(https://apps.who.int/iris/bitstream/handle/10665/44481/
9789241548168_eng.pdf, accessed August 2017).
169
MYANMAR
2009–2010
Summary statistics
Participation rate 89%
Key people
Name Role Organization
Win Maung Vice-chair, lead SC, TC and CPD Director of Disease Control
Thandar Lwin Survey coordinator, lead WC National Tuberculosis Programme (NTP)
Tin Mi Mi Khaing SC and TC member Regional TB officer, Yangon
Bo Myint SC and TC member Regional TB officer, Mandalay
Tin Tin Mar TC and CPD member National TB Reference Laboratory (NTRL)
Ti Ti TC member and laboratory advisor FIND
Wint Wint Nyunt Lead laboratory unit NTRL
San San Shein TC member, lead radiology unit Regional TB Centre, Mandalay
Moe Zaw TC member, data manager NTP
Hnin Wai Lwin Myo TC member, data management, WC NTP
Si Thu Aung TC member, field team leader NTP
Htay Lwin Field team leader State TB officer, Shan East
Htar Htar Oo Field team leader NTP
Thandar Thwin TC member, field team leader Regional TB Centre, Yangon
Myo Zaw SC and TC member, monitoring & supervision WHO Myanmar
Ikushi Onozaki SC, TC, CPD and WC member WHO headquarters
Norio Yamada Technical assistance (epidemiology, analysis and WC) Research Institute of Tuberculosis, Japan Anti-Tuberculosis
Association (RIT/JATA)
Kosuke Okada SC and TC member, technical assistance (management) Japan International Cooperation Agency (JICA)
Eva Nathanson Coordination (supply and logistics), WC member WHO Myanmar
CPD: central panel for diagnosis, SC: steering committee, TC: technical committee, WC: writing committee.
Symptom screening
Cough ≥3 weeksa 1 433 (2.8%)
Haemoptysisa 285 (0.6%)
Sputum production 9 953 (19%)
Chest pain 6 827 (13%)
Fever 3 122 (6.1%)
Total symptom-screen positivea 1 691 (3.3%)
Eligible for sputum examination 12 235 (24%) Symptom positive, chest X-ray positive 1 258 (10%)
Symptom positive, chest X-ray negative or N/A 433 (3.5%)
Symptom negative, chest X-ray positive 9 364 (77%)
Otherb 1 180 (10%)
Submitted specimens
At least one specimen 12 144 (99%)
Both specimens N/A
Laboratory result
At least one culture result availablec 12 027 (99%)
Total bacteriologically confirmed cases 311 Symptom positive, chest X-ray positive 65 (21%)
Symptom positive, chest X-ray negative or N/A 1 (0.3%)
Symptom negative, chest X-ray positive 231 (74%)
Otherf 14 (4.5%)
a
Eligible for sputum collection.
b
Chest X-ray exempted and symptom-screen negative (1096), corrective action (rechecked results of the interview and chest X-ray) (70), chest X-ray uninterpretable and symptom-screen
negative (14).
c
Cultures that were either contaminated and/or missing without a definitive result (i.e. MTB, NTM, negative) were excluded.
d
Definite: MTB confirmed by culture. Probable: MTB not confirmed by culture but two smear-positive, or one smear-positive with chest X-ray consistent with TB.
e
Definite: MTB confirmed by culture with at least one of the following conditions met: culture-positive (≥1 colony) in both two specimens, culture-positive (1–4 colonies) in one specimen
and chest X-ray consistent with TB, or culture-positive (≥5 colonies) in one specimen. Probable: no definition.
f
Chest X-ray exempted and symptom-screen negative (12), symptom-screen negative and field chest X-ray negative (i.e. central chest X-ray healed TB) (1), symptom-screen negative and
chest X-ray negative (field and central) (1) (the last two cases were from the corrective action).
172 National TB prevalence surveys 2007–2016
Fig. 1: Participation rate by age and sex Fig. 4: Cluster variation of the number of bacteriologically
confirmed TB casesb
100
12
Participation rate (%)
10
Number of clusters
90
8
6
80
4
70 0
15–24 25–34 35–44 45–54 55–64 ≥65 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22
Age group (years) Number of bacteriologically confirmed TB cases
Male Female
Fig. 2: TB prevalence per 100 000 population by age Fig. 5: Ratio of smear-positive TB prevalence to notifications by
age and by sexc
2000 3.5
Prevalence per 100 000 population
1800
3.0
Prevalence : notification ratio
1600
1400 2.5
1200
2.0
1000
800 1.5
600 1.0
400
0.5
200
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 15–24 25–34 35–44 45–54 55–64 ≥65 Male Female Total
Age group (years) Age group (years) and sex (≥15)
Bacteriologically confirmed TB Smear-positive TB
Fig. 3: Estimated number of bacteriologically confirmed TB cases Fig. 6: Estimates of TB prevalence (all ages, all forms of TB) before
and prevalence per 100 000 population, by agea (in blue) and after (in red) the national TB prevalence surveyd
60 000 1600
Estimated number of bacteriologically
1400
50 000
1200
confirmed TB cases
40 000
1000
30 000 800
600
20 000
400
10 000
200
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 400 600 800 1000
Age group (years) Prevalence per 100 000 population
a
The estimated number of bacteriologically confirmed TB cases is the product of age-specific prevalence and population estimates from the UN Population Division (2015 revision).
b
The data suggested that the distribution of cases by cluster (blue bars) was significantly different from the theoretical distribution (red line) (mean 4.44, variance 13.61, p<0.05). The
theoretical distribution assumes cases are distributed at random i.e. no clustering effect.
c
Notification rates were estimated using notifications obtained from the WHO global TB database, and population estimates from the UN Population Division (2015 revision).
d
The blue bar denotes the best estimate of prevalence and its range that was indirectly derived from the estimate of incidence previously published by WHO, adjusted to the year of the
prevalence survey based on previously published trends in incidence.
MYANMAR 173
Implications of results
The 2009–2010 national TB prevalence survey revealed a
high prevalence of TB in Myanmar despite efforts since
the late 1990s to expand DOTS throughout the country.
Although the estimated prevalence of smear-positive TB
among all age groups (171 per 100 000 population; 95%
CI: 131–223) was higher than the prevalence indicated in
the 1994 survey, this did not mean that the burden of TB
increased between 1994 and 2009 because the results were
not directly comparable. The 1994 survey relied only on
symptom screening and smear microscopy whereas the
2009–2010 survey used both chest X-ray and symptoms
Photo credit: Kosuke Okada
as screening tools. Prevalence results compared using the
same screening criteria showed a 35% reduction in the
population; 95% CI: 421–649). The prevalence of prevalence of smear-positive pulmonary TB from 1994
bacteriologically confirmed TB was higher in urban areas to 2009–2010, suggesting that TB control efforts had a
(903 per 100 000 population; 95% CI: 662–1232) than major impact.
in rural areas (527 per 100 000 population; 95% CI: 410– In the 2009–2010 survey, the difference between the
677). total number of smear-positive pulmonary cases and the
Other key results were: number of those with classic TB symptoms (i.e. a chronic
cough), and between the total number of bacteriologically
• the male to female ratio was 3.3 for smear- confirmed cases and the number of smear-positive cases,
positive TB and 2.5 for bacteriologically suggested that the case detection strategies used at the
confirmed TB; time of the survey had serious limitations and that a
• prevalence per 100 000 population increased comprehensive review of approaches to case finding was
with age; however, the absolute number of warranted. For example, TB could be considered as part
bacteriologically confirmed TB cases was
relatively high in the young to middle age groups of the differential diagnosis of anyone with undiagnosed
(25–54 years); chronic symptoms, regardless of the presence of cough or
• of the bacteriologically confirmed TB survey any respiratory illness. The expansion of diagnostic tests
cases, 21% were symptom-screen positive, including chest X-ray and culture was included in the
and among smear-positive cases, 34% were national strategic plan for TB control 2011–2015.
symptom-screen positive;
• for smear-positive pulmonary TB, the ratio of The finding that the prevalence of TB was higher in the
prevalence to notifications (P:N ratio) was 2.1 states than in the regions suggested that specific efforts
overall, but varied from 0.7 in those aged 15–24 were needed to improve access to basic diagnostic
years to 3.0 in those aged 65 years or more, and services in the states, especially in the most remote areas.
was higher for men than for women (2.5 versus
1.6); Among the symptomatic TB cases, 24% (16/66) chose
• among bacteriologically confirmed TB survey to initially seek care in pharmacies or from a traditional
cases, 86% had no previous history of anti- healer. This suggested that incorporating these providers
TB treatment and only 4.2% were on anti-TB
into formal TB control and care networks could help to
treatment at the time of the survey; and
detect cases earlier.
• of the 60 bacteriologically confirmed and 37
smear-positive TB survey cases that screened The survey showed that chest X-ray was a more sensitive
positive for symptoms and were not on anti-TB
treatment at the time of the survey, 21 (35%) tool for TB detection than symptom screening. Therefore,
and 14 (38%), respectively, had previously anyone with an undiagnosed chest X-ray abnormality
sought care in a public or private health facility should be considered as a presumptive TB case and eligible
for their symptoms. for sputum examination. The diagnostic challenge was
MYANMAR 175
further illustrated by the large share of smear-negative operations. Final results, including updated estimates of
cases among all detected TB cases. Expanded use of TB disease burden (incidence, prevalence and mortality),
Xpert® MTB/RIF was one of the strategies identified to were fully disseminated to national and international
address this challenge (major expansion of culture was partners in December 2010. These estimates informed
not considered feasible, given the complexity of culture the subsequent revision of the national strategic plan for
methods and the requirement for strict infection control TB, and contributed to the mobilization of additional
measures). funding for TB care and treatment in Myanmar.
Survey results showed that specific measures were Challenges included the need to exclude 32 of 325
needed in congested urban areas where prevalence rates townships from the sampling frame due to security
were highest. Examples that were identified included issues; the fact that residency criteria for survey eligibility
intensified collaboration with the private sector, since this meant that 9.4% of those otherwise eligible were not
provided services at convenient hours for those living in included in the survey (mostly the mobile population,
urban areas. including seasonal workers); and low participation
rates in a few areas, notably a few urban clusters and
remote areas. These challenges affected the coverage and
Major successes, challenges and lessons representativeness of the survey. Delays in procuring chest
learned X-ray equipment delayed the start of survey operations,
and some equipment then failed during field operations.
The survey was successfully implemented with a high The sputum cups that were used were not optimal for the
participation rate and with a comparatively low survey- purposes of culture testing and may have caused some
specific budget (US$ 1 million, excluding the costs of NTP laboratory cross-contamination. Unfortunately, no staff
staff who worked on the survey). Even after the withdrawal were available to write a paper to summarize the key
of the financing initially committed by the Global Fund, results and lessons learned from the survey in a peer-
resources were mobilized from other sources following reviewed journal.
intensive efforts by the NTP and the WHO Country Office
in particular. Provisional results were shared with key Survey results were analysed before guidance on
officials and partners within 4 months of completing field analytical methods in the WHO handbook was finalized
(9). The results from analyses that were restricted to
survey participants (not taking into account those eligible
but not participating in the survey) were used as the
official survey results. Although the survey was carried
out rigorously and had a high participation rate with few
missing data, later analysis (that included more extended
imputation for missing data) estimated TB prevalence to
be about 10% higher than results in the official survey
report.
References
1. The World Bank (https://data.worldbank.org/country, accessed
April 2017).
2. UNAIDS (http://aidsinfo.unaids.org/, accessed April 2017).
3. World Health Organization. Global Tuberculosis Database. 2017.
(http://www.who.int/tb/country/en/, accessed April 2017).
4. WHO Tuberculosis Programme. (1994). WHO Tuberculosis
Programme: framework for effective tuberculosis
control. World Health Organization. (http://www.who.int/iris/
handle/10665/58717, accessed January 2018).
5. World Health Organization. Global tuberculosis programme.
Global tuberculosis control report 1997. Geneva: WHO; (https://
apps.who.int/iris/bitstream/handle/10665/63354/WHO_
TB_97.225_(part1).pdf?sequence=1, accessed January 2018).
6. World Health Organization. Global tuberculosis report
2009. Geneva: WHO; 2009 (http://apps.who.int/iris/
bitstream/10665/44035/1/9789241563802_eng.pdf ?ua=1,
accessed January 2018).
7. Annual report 2006. National Tuberculosis Programme,
Myanmar; 2007.
8. Report on national TB prevalence survey, 2009–2010, Myanmar.
Ministry of Health, Department of Health, Government of
Myanmar;(https://www.who.int/tb/advisory_bodies/impact_
measurement_taskforce/prevalencesurveymyanmar_2009-
10report.pdf, accessed July 2017).
9. World Health Organization. Tuberculosis prevalence surveys:
a handbook (WHO/HTM/TB/2010.17). Geneva: WHO; 2011
(https://apps.who.int/iris/bitstream/handle/10665/44481/
9789241548168_eng.pdf, accessed August 2017).
177
NIGERIA
2012
Summary statistics
Participation rate 57%
a
The boundaries and names shown and the designations used on this map do not
imply the expression of any opinion whatsoever on the part of the World Health
Organization concerning the legal status of any country, territory, city or area or of
its authorities, or concerning the delimitation of its frontiers or boundaries.
178 National TB prevalence surveys 2007–2016
Symptom screening
Cough ≥2 weeksa 2 466 (5.6%)
Haemoptysis 288 (0.7%)
Sputum production 3 551 (8.0%)
Chest pain 6 813 (15%)
Fever 8 493 (19%)
Total symptom-screen positivea 2 466 (5.6%)
Eligible for sputum examination 4 688 (11%) Symptom positive, chest X-ray positive 746 (16%)
Symptom positive, chest X-ray negative or N/A 1 720 (37%)
Symptom negative, chest X-ray positive 2 222 (47%)
Other N/A
Submitted specimens
At least one specimen 4 558 (97%)
Both specimens 4 133 (88%)
Laboratory result
At least one culture result availableb 2 662 (57%)
Total bacteriologically confirmed cases 144 Symptom positive, chest X-ray positive 76 (53%)
Symptom positive, chest X-ray negative or N/A 16 (11%)
Symptom negative, chest X-ray positive 52 (36%)
Other N/A
a
Eligible for sputum collection.
b
Cultures that were either contaminated and/or missing without a definitive result (i.e. MTB, NTM, negative) were excluded.
c
Definite: MTB confirmed by culture. Probable: MTB not confirmed by culture, but chest X-ray suggestive of TB.
d
Definite: MTB confirmed by culture. Probable: culture-positive without identification, and chest X-ray suggestive of TB.
180 National TB prevalence surveys 2007–2016
Fig. 1: Participation rate by age and sex Fig. 4: Cluster variation of the number of bacteriologically
confirmed TB casesb
100
90
15
Participation rate (%)
Number of clusters
80
70
10
60
50 5
40
30 0
15–24 25–34 35–44 45–54 55–64 ≥65 0 1 2 3 4 5 6 7 8 9 10 11 12
Age group (years) Number of bacteriologically confirmed TB cases
Male Female
Fig. 2: TB prevalence per 100 000 population by age Fig. 5: Ratio of smear-positive TB prevalence to notifications by
age and by sexc
1200 9.0
Prevalence per 100 000 population
Fig. 3: Estimated number of bacteriologically confirmed TB cases Fig. 6: Estimates of TB prevalence (all ages, all forms of TB) before
and prevalence per 100 000 population, by agea (in blue) and after (in red) the national TB prevalence surveyd
500
80 000
400
60 000
300
40 000
200
20 000 100
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 100 200 300 400
Age group (years) Prevalence per 100 000 population
a
The estimated number of bacteriologically confirmed TB cases is the product of age-specific prevalence and population estimates from the UN Population Division (2015 revision).
b
The data suggested that the distribution of cases by cluster (blue bars) was significantly different from the theoretical distribution (red line) (mean 2.06, variance 5.42, p<0.05). The
theoretical distribution assumes cases are distributed at random i.e. no clustering effect.
c
Notification rates were estimated using notifications obtained from the WHO global TB database, and population estimates from the UN Population Division (2015 revision).
d
The blue bar denotes the best estimate of prevalence and its range that was indirectly derived from the estimate of incidence previously published by WHO, adjusted to the year of the
prevalence survey based on previously published trends in incidence.
NIGERIA 181
Major successes, challenges and lessons • extremely limited access to the northern regions
learned of the country (including the National TB
Reference Laboratory used for the prevalence
The major success of this survey was that it was the first survey) for international staff;
of its kind in Nigeria and contributed to a much better • no international technical assistance to the
understanding and robust measurement of the burden of National TB Reference Laboratory in Zaria,
although local staff from the United States
TB disease in the country. It was also implemented and Centers for Disease Control and Prevention
completed in the face of several challenges beyond the continued to provide support; and
control of the NTBLCP and the survey team. • delays to the start of the survey that led to the
expiry of the contract and associated licenses for
The biggest challenge outside the control of the NTBLCP X-ray software, which had to be re-procured.
and survey teams was the security situation in the
Linked to these repercussions, other major challenges
country, which deteriorated during both preparations
included a low participation rate, especially in urban
for and implementation of the survey. In August 2011,
areas; a large number of positively-screened participants
just as survey preparations (including all procurement)
with missing culture results; and the possible under-
were almost complete and the survey was about to start,
performance of culture laboratories (related to lack of
a terrorist attack occurred in the capital of Abuja. A
technical assistance). The implications of these challenges
bomb hidden in a car exploded underneath the United
had to be investigated and adjusted for during analysis
Nations (UN) building, killing 21 people and wounding
of survey data. Even with these data limitations, analyses
60 others (including WHO staff). Following this attack,
that included imputation of missing data and sensitivity
the UN raised its rating of the security level and there was
analysis showed that the limitations did not affect the
considerable debate about whether the survey should be
main policy and programmatic implications drawn from
cancelled.
the survey. For example, even if it was assumed that
Eventually, the MoH decided to launch the survey in all those who refused to participate in the survey were
February 2012. Only three of the original list of randomly healthy (i.e. without active TB disease), the number of
selected clusters had to be replaced due to the security detected TB cases still far exceeded the number of TB
measures in place; nevertheless, the security situation had cases being detected and notified.
other serious repercussions:
Other challenges faced during the survey included:
• limited hours of operation for data collection oversampling during field operations, despite the
during cluster operations (it was done from 7am low participation rate (although field teams correctly
to 5pm); registered the population in enumeration areas, regardless
• negative attitudes, including advice (or of their willingness to participate); survey investigators
instructions) from some community leaders not
did not have access to national census data; staff from
to participate in the survey;
the Bureau of Statistics, who joined cluster operations,
changed for each cluster; a 1-month suspension of field
operations due to extreme rainfall; slow data entry from
the field and in the laboratory; and delays in finalizing
the survey report due to the departure of the survey
coordinator and the lack of a full-time officer in the
NTBLCP to oversee the survey.
References
1. The World Bank (https://data.worldbank.org/country, accessed
April 2017).
2. UNAIDS (http://aidsinfo.unaids.org/, accessed April 2017).
3. World Health Organization. Global Tuberculosis Database. 2017.
(http://www.who.int/tb/country/en/, accessed April 2017).
4. Report first national TB prevalence survey 2012 Nigeria:
Department of Public Health, Federal Republic of Nigeria; 2014
(http://www.who.int/tb/publications/NigeriaReport_WEB_NEW.
pdf, accessed May 2017).
5. World Health Organization. Tuberculosis prevalence surveys:
a handbook (WHO/HTM/TB/2010.17). Geneva: WHO; 2011
(https://apps.who.int/iris/bitstream/handle/10665/44481/
9789241548168_eng.pdf, accessed August 2017).
6. World Health Organization. Global tuberculosis report 2012.
Geneva: WHO; 2012 (http://www.who.int/tb/publications/
global_report/gtbr12_main.pdf, accessed June 2017).
185
PAKISTAN
2010–2011
Summary statistics
Participation rate 81%
Key people
Name Role Organization
Ejaz Qadeer Principal investigator National TB Control Programme (NTP)
Sabira Tahseen Co-principal investigator National TB Reference Laboratory (NTRL)
Razia Fatima Co-principal investigator NTP
Mohammad Asif Survey coordinator NTP
Alamdar Hussain Rizvi Senior microbiologist NTRL, NTP
Sabir Rehman Radiology coordinator NTP
Zia Samad Data coordinator NTP
Aisha Mariam Field team leader NTP
Abdul Mannan Soomro Field team leader NTP
Arshad Shamsi Field team leader NTP
Riaz Ahmed Field team leader NTP
Ghulam Nabi Shaikh Field team leader NTP
Zulfiqar Ul Hassan Field team leader NTP
Edine Tiemersma Technical assistance (survey advisor) KNCV Tuberculosis Foundation
Masja Straetemans Technical assistance (survey advisor) KNCV Tuberculosis Foundation
Nico Kalisvaart Technical assistance (data management) KNCV Tuberculosis Foundation
Amal Bassili Technical assistance (survey advisor) WHO Eastern Mediterranean Regional Office (EMRO)
a
The boundaries and names shown and the designations used on this map do not
imply the expression of any opinion whatsoever on the part of the World Health
Organization concerning the legal status of any country, territory, city or area or of
its authorities, or concerning the delimitation of its frontiers or boundaries.
186 National TB prevalence surveys 2007–2016
Symptom screening
Cough ≥2 weeksa 5 063 (4.8%)
Cough (any duration) with no chest X-ray resulta 354 (0.3%)
Haemoptysis N/A
Sputum production N/A
Chest pain N/A
Fever N/A
Total symptom-screen positivea 5 417 (5.2%)
Eligible for sputum examination 10 471 (9.9%) Symptom positive, chest X-ray positive 2 819 (27%)
Symptom positive, chest X-ray negative or N/A 2 598 (25%)
Symptom negative, chest X-ray positive 5 042 (48%)
Otherc 12 (0.1%)
Submitted specimens
At least one specimen 8 521 (81%)
Both specimens 6 810 (65%)
Laboratory result
At least one culture result availabled 7 221 (69%)
Total bacteriologically confirmed cases 341 Symptom positive, chest X-ray positive 157 (46%)
Symptom positive, chest X-ray negative or N/A 41 (12%)
Symptom negative, chest X-ray positive 142 (42%)
Otherc 1 (0.3%)
a
Eligible for sputum collection.
b
The result was not entered on the form (933) or the form was not available (81).
c
Current TB treatment with symptom-screen negative and chest X-ray normal.
d
Cultures that were either contaminated and/or missing without a definitive result (i.e. MTB, NTM, negative) were excluded.
e
Definite: MTB confirmed by culture and/or NAAT. Probable: MTB not confirmed by culture and/or NAAT, but two smear-positive or one smear-positive with chest X-ray suggestive of TB.
f
Definite: MTB confirmed by culture (more than 5 colonies, or less than 5 colonies with chest X-ray suggestive of TB). Probable: no definition.
188 National TB prevalence surveys 2007–2016
Fig. 1: Participation rate by age and sex Fig. 4: Cluster variation of the number of bacteriologically
confirmed TB casesb
100 20
90
Participation rate (%)
Number of clusters
15
80 10
70 5
60 0
15–24 25–34 35–44 45–54 55–64 ≥65 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14
Age group (years) Number of bacteriologically confirmed TB cases
Male Female
Fig. 2: TB prevalence per 100 000 population by age Fig. 5: Ratio of smear-positive TB prevalence to notifications by
age and by sexc
1800 6.0
Prevalence per 100 000 population
Fig. 3: Estimated number of bacteriologically confirmed TB cases Fig. 6: Estimates of TB prevalence (all ages, all forms of TB) before
and prevalence per 100 000 population, by agea (in blue) and after (in red) the national TB prevalence surveyd
1400
100 000
1200
confirmed TB cases
80 000
1000
60 000 800
600
40 000
400
20 000
200
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 200 300 400 500 600
Age group (years) Prevalence per 100 000 population
a
The estimated number of bacteriologically confirmed TB cases is the product of age-specific prevalence and population estimates from the UN Population Division (2015 revision).
b
The data suggested that the distribution of cases by cluster (blue bars) was significantly different from the theoretical distribution (red line) (mean 3.59, variance 8.33, p<0.05). The
theoretical distribution assumes cases are distributed at random i.e. no clustering effect.
c
Notification rates were estimated using notifications obtained from the WHO global TB database, and population estimates from the UN Population Division (2015 revision).
d
The blue bar denotes the best estimate of prevalence and its range that was indirectly derived from the estimate of incidence previously published by WHO, adjusted to the year of the
prevalence survey based on previously published trends in incidence.
PAKISTAN 189
There were 95 clusters with a target size of 1400 individuals • the male to female ratio was 1.8 for smear-
positive TB and 1.5 for bacteriologically
per cluster. No stratification was used at the time of survey
confirmed TB;
design; however, results were later analysed separately
• prevalence per 100 000 population increased
for four provinces and two regions (Punjab, Sindh, with age; however, the absolute number of
Balochistan, Khyber Pakhtunkhwa, Azad Jammu and bacteriologically confirmed TB cases was
Kashmir, Gilgit-Baltistan), and for urban and rural areas. consistently high in all age groups;
A total of 131 377 individuals from 33 324 households • among bacteriologically confirmed TB cases,
were enumerated in the survey census, of whom 131 329 58% were symptom-screen positive, and among
(99.9%) were eligible and invited to participate. Of these, the smear-positive cases, 62% were symptom-
105 913 (81%) did so. All participants were screened screen positive;
according to the 2011 algorithm recommended by WHO; • for smear-positive pulmonary TB, the ratio of
prevalence to notifications (P:N ratio) was 2.9
that is, chest X-ray and an interview about symptoms
overall, but varied from 2.1 in those aged 25–34
(9). A total of 10 471 people (10% of participants) were years to 5.3 in those aged 65 years or more, and
eligible for sputum examination; of these 8521 (81%) was higher for men than for women (3.8 versus
submitted at least one sputum specimen and 6810 (65%) 2.2);
submitted two sputum specimens. • among bacteriologically confirmed TB cases,
only 7.6% were on anti-TB treatment at the time
A total of 341 cases of bacteriologically confirmed of the survey; no data about previous history of
pulmonary TB were identified, including 233 cases of anti-TB treatment were available.
smear-positive TB. The prevalence of smear-positive No data were available on whether participants with
pulmonary TB was 270 (95% CI: 217–323) per 100 000 symptoms had sought health care.
population (among those aged ≥15 years), and for
bacteriologically confirmed TB it was 398 (95% CI:
333–463) per 100 000 population. The prevalence of
bacteriologically confirmed TB was higher in rural areas
(471 per 100 000 population; 95% CI: 377–564) than in
urban areas (310 per 100 000 population; 95% CI: 234–
386).
Implications of results Given the P:N ratio of 2.9, and results from a subsequent
TB inventory study of the level of underreporting
Based on survey results, the overall prevalence of TB of detected TB cases in 2012, it was clear that both
(all forms of TB, all ages) was estimated as 342 (95% CI: underreporting and underdiagnosis of TB needed to be
284–406) per 100 000 population. This was similar to (but addressed (10). With a large private sector, and less than
more precise than) the pre-survey estimate published by 1% of private providers reporting TB cases to national
WHO (389 per 100 000 population; 95% CI: 191–657) authorities at the time of the survey, factors identified as
(8). This result showed that TB remained a major public being of vital importance were much greater engagement
health problem in Pakistan, requiring continued high- of the private sector and mandatory notification of cases.
level political commitment and sustained funding.
The survey was the first time the specimen transport
The high number of previously undiagnosed cases system was successfully used for the transport of
detected in the community, and the fact that 68% of specimens via cold chain from field sites to the National
these were smear-positive, suggested that people may TB Reference Laboratory (NTRL). This experience was
not recognize the symptoms of TB, and that when they used to improve specimen transportation undertaken as
do seek care they may not be diagnosed. These findings part of routine programmatic activities.
indicated a need to implement strategies to increase
population awareness of TB symptoms, and to improve
the availability and quality of services for TB diagnosis
and treatment in the community. It was also recognized
Major successes, challenges and lessons
that further analysis of health-care seeking behaviour and
learned
of awareness of TB among health-care providers could Given the security and geographical challenges, the
help the programme to design specific interventions. The successful implementation of the survey was a major
higher prevalence of TB in older age groups and in rural achievement.
areas demonstrated a need for improved case finding
in these groups and areas in particular. One proposed Security concerns persisted throughout survey
option was active engagement of trained community implementation. A complete security assessment was
health workers to help identify and refer people with TB done and a handbook on security and safety was
symptoms to health services. prepared in consultation with international experts in
PHILIPPINES
2007
Summary statistics
Participation rate (chest X-ray) 90%
Total participants
Interview (TB symptom, ≥20 years) 15 242 (94%)
Chest X-ray (≥10 years) 20 643 (90%)
Symptom interview
Cough ≥2 weeks 1 927 (13%)
Haemoptysis 285 (1.9%)
Chest pain 1 668 (11%)
Fever 684 (4.5%)
Night sweats 958 (6.3%)
Eligible for sputum examination 5 378c (26%) Symptom positive, chest X-ray positive N/A
Symptom positive, chest X-ray negative or N/A N/A
Symptom negative, chest X-ray positive N/A
Other N/A
Submitted specimens
At least one specimen 5 173 (96%)
Both specimens N/A
Laboratory result
At least one culture result availabled 5 143 (96%)
Total bacteriologically confirmed cases 136 Symptom positive, chest X-ray positive N/A
Symptom positive, chest X-ray negative or N/A N/A
Symptom negative, chest X-ray positive N/A
Other N/A
a
BCG scar verification was undertaken for those aged 2 months–9 years, and a tuberculin skin test was done for two age groups (5–9 and 40–59 years) as well as those who had a chest
X-ray suggestive of TB.
b
Only chest X-ray, and not a symptom interview, was used as a screening tool to determine eligibility for sputum collection.
c
The number eligible for sputum submission was more than the number with a field chest X-ray abnormality (i.e. 4560), because some consultant radiologists were involved in field
screening and they found more chest X-ray abnormalities than field readers.
d
Cultures that were either contaminated and/or missing without a definitive result (i.e. MTB, NTM, negative) were excluded.
e
Definite: MTB confirmed by culture. Probable: MTB not confirmed by culture but chest X-ray suggestive of TB.
f
Definite: MTB confirmed by culture. Probable: no definition.
196 National TB prevalence surveys 2007–2016
Fig. 1: Participation rate by age and sex Fig. 4: Cluster variation of the number of bacteriologically
confirmed TB casesb
100 12
10
Participation rate (%)
Number of clusters
90 8
80 4
70 0
10–19 20–29 30–39 40–49 ≥50 0 1 2 3 4 5 6 7 8 9 10 11
Age group (years) Number of bacteriologically confirmed TB cases
Male Female
Fig. 2: TB prevalence per 100 000 population by age Fig. 5: Ratio of smear-positive TB prevalence to notifications by
age and by sexc
1800 3.5
Prevalence per 100 000 population
1600
3.0
Prevalence : notification ratio
1400
2.5
1200
1000 2.0
800 1.5
600
1.0
400
200 0.5
0 0
10–19 20–29 30–39 40–49 ≥50 15–24 25–34 35–44 45–54 55–64 ≥65 Male Female Total
Age group (years) Age group (years) and sex (≥15)
Bacteriologically confirmed TB Smear-positive TB
Fig. 3: Estimated number of bacteriologically confirmed TB cases Fig. 6: Estimates of TB prevalence (all ages, all forms of TB) before
and prevalence per 100 000 population, by agea (in blue) and after (in red) the national TB prevalence surveyd
100 000
800
80 000
600
60 000
400
40 000
20 000 200
0 0
10–19 20–29 30–39 40–49 ≥50 300 400 500 600
Age group (years) Prevalence per 100 000 population
a
The estimated number of bacteriologically confirmed TB cases is the product of age-specific prevalence and population estimates from the UN Population Division (2015 revision).
b
The data did not suggest that the distribution of cases by cluster (blue bars) was significantly different from the theoretical distribution (red line) (mean 2.72, variance 4.70, p=0.08).
The theoretical distribution assumes cases are distributed at random i.e. no clustering effect.
c
Notification rates were estimated using notifications obtained from the WHO global TB database, and population estimates from the UN Population Division (2015 revision). As notification
data in the WHO database was disaggregated by six age groups (as opposed to the five age groups used in the Philippines survey), crude prevalence rates for six age groups were
recalculated for this figure.
d
The blue bar denotes the best estimate of prevalence and its range that was indirectly derived from the estimate of incidence previously published by WHO, adjusted to the year of the
prevalence survey based on previously published trends in incidence.
PHILIPPINES 2007 197
The National TB Control Programme (NTP) launched A total of 136 bacteriologically confirmed pulmonary TB
the WHO-recommended DOTS strategy in 1996 (4,5) cases were identified, including 55 cases of smear-positive
and national coverage was achieved by 2005 (5,6). In TB. The prevalence of smear-positive TB was 280 (95%
2005, WHO estimated TB incidence and prevalence as CI: 190–370) per 100 000 population (among those aged
291 per 100 000 population and 450 per 100 000 popula- ≥10 years), and for bacteriologically confirmed TB it was
tion, respectively; the notification rate (new and relapse 660 (95% CI: 530–800) per 100 000 population. When
TB cases) was 165 per 100 000 population and had not extrapolated to all forms of TB and to all ages, prevalence
changed significantly since 2000. The case detection was 576 (95% CI: 515–640) per 100 000 population. There
rate (notifications of new and relapse cases divided by was no significant variation in prevalence among the
estimated incidence in the same time period) was 55% three strata.
in 2005 (8).
Among the participants who reported TB symptoms in Major successes, challenges and lessons
the 2007 survey, only one third had previously consulted learned
health facilities; nearly half of them had chosen to self-
medicate and the rest had not taken any action. Although Major successes of the 2007 survey included completing
in comparison to the 1997 survey the proportion of the survey on time, despite challenges faced during field
symptomatic participants who consulted health facilities operations, and the high coverage of the survey’s screening
increased marginally and the proportion who took no and diagnostic tests (e.g. 90% of the 22 867 participants
action dropped, the proportion who had self-medicated aged 10 years or older were examined by chest X-ray).
almost doubled. Among those in the 2007 survey who
Major challenges faced during the survey included
took no action, 45% considered their symptoms to be
the exclusion of some barangays (i.e. the smallest
harmless, 39% could not afford the cost of treatment
administrative unit) from the sampling frame because
and 4% found the distance to a health facility to be a
of security issues and inaccessibility, so the survey was
barrier. These findings highlighted a need to improve
not truly representative of the national population; it was
access to health facilities, social support and advocacy to
difficult to define the study population in some congested
communities (6).
areas because households were not clearly demarcated;
logistical challenges were experienced in some barangays
(e.g. households spread over several kilometres, or located
in geographically challenging locations such as small
islands or mountainous areas); and the quality of sputum
samples was questionable in some clusters because of the
absence of courier services, difficulties in maintaining the
cold chain in tropical conditions and delays in processing
specimens (this resulted in high specimen contamination
rates; 6.9% of 13 926 specimens on Ogawa media and
8.3% of pooled specimens on LJ slopes (6)).
References
1. The World Bank (https://data.worldbank.org/country, accessed
April 2017).
2. UNAIDS. (http://aidsinfo.unaids.org/, accessed May 2017).
3. World Health Organization. Global tuberculosis database.
Geneva: WHO; 2017 (http://www.who.int/tb/data/en/, accessed
April 2017).
4. WHO Tuberculosis Programme. (1994). WHO Tuberculosis
Programme: framework for effective tuberculosis
control. World Health Organization. (http://www.who.int/iris/
handle/10665/58717, accessed January 2018).
5. World Health Organization. Global tuberculosis programme.
Global tuberculosis control report 1997. Geneva: WHO; (https://
apps.who.int/iris/bitstream/handle/10665/63354/WHO_
TB_97.225_(part1).pdf?sequence=1, accessed January 2018).
6. Nationwide Tuberculosis Prevalence Survey 2007, final report,
Republic of the Philippines. Tropical Disease Foundation Inc.;
2008.
7. World Health Organization. Global Plan to Stop TB – Phase 1:
2001 to 2005. Geneva: WHO; (http://www.stoptb.org/global/plan/
plan0105.asp, accessed July 2017).
8. World Health Organization. Global Tuberculosis Control.
Geneva: WHO; 2007
9. Tupasi TE, Radhakrishna S, Chua JA, Mangubat NV, Guilatco R,
Galipot M et al. Significant decline in the tuberculosis burden in
the Philippines ten years after initiating DOTS. Int J Tuberc Lung
Dis. 2009;13(10):1224–1230.
10. Floyd S, Sismanidis C. The 2007 Philippines nationwide TB survey
confirmatory report of main results. London School of Hygiene &
Tropical Medicine; 2008.
201
PHILIPPINES
2016
Summary statistics
Participation rate 76%
Symptom screening
Cough ≥2 weeksa 2 458 (5.3%)
Haemoptysisa 565 (1.2%)
Fever 5 313 (11%)
Weight loss 8 188 (18%)
Night sweats 3 959 (8.5%)
Total symptom-screen positivea 2 815 (6.0%)
Eligible for sputum examination 18 597 (40%) Symptom positive, chest X-ray positive 1 444 (7.8%)
Symptom positive, chest X-ray negative or N/A 1 371 (7.4%)
Symptom negative, chest X-ray positive 10 702 (58%)
Otherb 5 080 (27%)
Submitted specimens
At least one specimen 16 242 (87%)
Both (spot and morning) specimens 15 547 (84%)
Third specimen 32 (0.2%)
Laboratory result
At least one culture result availablec 15 776 (85%)
At least one Xpert MTB/RIF result available 16 200 (87%)
Smear-positive casesd 173 (37%) Smear-negative casesd 289 (62%) Smear unknown casese 4 (0.9%)
Definite 173 Definite 289 Definite 4
Probable N/A Probable N/A Probable N/A
Total bacteriologically confirmed cases 466 Symptom positive, chest X-ray positive 132 (28%)
Symptom positive, chest X-ray negative or N/A 18 (3.9%)
Symptom negative, chest X-ray positive 298 (64%)
Otherf 18 (3.9%)
a
Eligible for sputum submission.
b
Chest X-ray exempted and symptom-screen negative (5079), poor chest X-ray image and symptom-screen negative (1).
c
Cultures that were either contaminated and/or missing without a definitive result (i.e. MTB, NTM, negative) were excluded.
d
Definite: MTB confirmed by culture and/or Xpert. Probable: no definition.
e
Definite: smear and culture not done, but MTB confirmed by Xpert. Probable: no definition.
f
Chest X-ray exempted and symptom-screen negative.
204 National TB prevalence surveys 2007–2016
Fig. 1: Participation rate by age and sex Fig. 4: Cluster variation of the number of bacteriologically
confirmed TB casesb
100 20
Participation rate (%)
90 15
Number of clusters
80 10
70 5
60 0
15–24 25–34 35–44 45–54 55–64 ≥65 0 1 2 3 4 5 6 7 8 9 10 11 12 13
Age group (years) Number of bacteriologically confirmed TB cases
Male Female
Fig. 2: TB prevalence per 100 000 population by age Fig. 5: Ratio of smear-positive TB prevalence to notifications by
age and by sexc
2500 4.5
Prevalence per 100 000 population
Fig. 3: Estimated number of bacteriologically confirmed TB cases Fig. 6: Estimates of TB prevalence (all ages, all forms of TB) before
and prevalence per 100 000 population, by agea (in blue) and after (in red) the national TB prevalence surveyd
180 000
Prevalence per 100 000 population
1600
160 000 1400
confirmed TB cases
140 000
1200
120 000
1000
100 000
800
80 000
600
60 000
40 000 400
20 000 200
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 500 700 900 1100
Age group (years) Prevalence per 100 000 population
a
The estimated number of bacteriologically confirmed TB cases is the product of age-specific prevalence and population estimates from the UN Population Division (2015 revision).
b
The data suggested that the distribution of cases by cluster (blue bars) was significantly different from the theoretical distribution (red line) (mean 4.40, variance 9.12, p<0.05). The
theoretical distribution assumes cases are distributed at random i.e. no clustering effect.
c
Notification rates were estimated using smear-positive pulmonary TB notifications (2016) obtained from the NTP, and population estimates from the UN Population Division (2015
revision).
d
The blue bar denotes the best estimate of prevalence and its range that was indirectly derived from the estimate of incidence previously published by WHO, adjusted to the year of the
prevalence survey based on previously published trends in incidence.
PHILIPPINES 2016 205
The sample size in 2016 was not designed to detect a • initiatives to reduce geographic and financial
specified effect size (e.g. 20% decline) in comparison barriers affecting access to health care;
with the 2007 survey, but rather to obtain an estimate • greater engagement of public-private mix
of prevalence in 2016 with a specified precision. The partnerships, including effective implementation
of existing legislation on mandatory notification
2016 survey was therefore not powered to detect small
of TB cases; and
differences between it and the 2007 survey. Nonetheless,
• strengthening collaboration between the NTP
this limitation did not prevent an assessment of the and other health programmes, such as those for
trend in TB disease burden since 2007. Adjustments HIV, diabetes and lung health.
were made to ensure that the two datasets and methods
In discussions towards the end of 2016, it was anticipated
were as comparable as possible, resulting in an upward
that these strategic actions would be implemented with
adjustment of the 2007 survey results, to account for
the full support of the Department of Health, and full
the more sensitive screening and diagnostic methods
mobilization of the health sector. Measures that were
used in the 2016 survey. Based on these adjustments,
agreed to be needed included the deployment of sufficient
the prevalence of culture-positive TB was 463 (95%
human resources at national and subnational levels;
CI: 333−592) per 100 000 population in 2007 and 512
increased domestic funding; a presidential executive
(95% CI: 420−603) per 100 000 population in 2016 (6).
order for drug regulation; establishment of a high-level
The probability that prevalence did not decline over the
steering group; and ensuring financial protection (and
period 2007–2016 was estimated at 75%.
sustained poverty alleviation efforts) for more than 90%
The lack of decline in TB prevalence since 2007 could of the poor through increased coverage of PhilHealth and
be explained by a combination of case-detection gaps, expanded social protection programmes.
significant delays in diagnosis, health system weaknesses,
and broader social and economic influences on the TB
epidemic. These broader influences included the level Major successes, challenges and lessons
of poverty, with 22% of people living below the national learned
poverty line in 2015; the level of undernourishment,
with a prevalence of 14% in the general population in Major successes in the survey included:
2015 and no improvement since 2008; and low coverage • high-level commitment and excellent
of health insurance and social protection (e.g. coverage coordination by the implementing agency;
of only 4% in the poorest quintile in 2013), leading to • reaching remote hamlets and villages that
financial barriers to accessing health services and high were included in the sampling frame, based
levels of TB-affected households facing catastrophic costs on efficient logistical management of field
(35% in 2016−2017) (1, 9). At a broader level, the poor teams and equipment and use of digital X-ray
and disadvantaged require adequate social protection
strategies and increased PhilHealth TB benefit packages
to reduce catastrophic costs associated with TB, especially
multidrug-resistant TB (MDR-TB).1
1
PhilHealth is the national health insurance programme.
Photo credit: Julia Ershova
208 National TB prevalence surveys 2007–2016
1
Recovery rate of MTB: number of smear-positive MTB that are culture positive
out of the number of smear-positive specimens.
209
RWANDA
2012
Summary statistics
Participation rate 96%
Key people
Name Role Organization
Michel Gasana Principal investigator Tuberculosis & Other Respiratory Communicable Diseases Division-Kigali, Rwanda
Claude Bernard Uwizeye Principal investigator US Centers for Disease Control and Prevention CDC-Kigali, Rwanda
Eveline Klinkenberg Principal investigator KNCV Tuberculosis Foundation
Pauline Basinga Principal investigator School of public health, National University of Rwanda
Patrick Migambi Co-investigator and survey coordinator Tuberculosis & Other Respiratory Communicable Diseases Division-Kigali, Rwanda
Julie Mugabekazi Co-investigator WHO Rwanda
Védaste Ndahindwa Survey statistician School of public health, National University of Rwanda
Elaine Kamanzi Survey laboratory activities coordinator National Reference Laboratory-Kigali, Rwanda
Jules Kamugunga Mulinzi Survey data manager Tuberculosis & Other Respiratory Communicable Diseases Division-Kigali, Rwanda
Alaine Umubyeyi Nyaruhirira Laboratory advisor Management Sciences for Health
Louise Kalisa Survey radiology coordinator Kigali University Teaching Hospital-Kigali, Rwanda
Calvin Mugabo Field team leader Tuberculosis & Other Respiratory Communicable Diseases Division-Kigali, Rwanda
Liliane Umutesi Field team leader Tuberculosis & Other Respiratory Communicable Diseases Division-Kigali, Rwanda
Ndeziki Mashengesho Field team leader Tuberculosis & Other Respiratory Communicable Diseases Division-Kigali, Rwanda
Nico Kalisvaart Technical assistance (data management) KNCV Tuberculosis Foundation
Ikushi Onozaki Technical assistance (survey advisor) WHO headquarters
Peou Satha Technical assistance (radiology) CENAT, Cambodia
a
The boundaries and names shown and the designations used on this map do not
imply the expression of any opinion whatsoever on the part of the World Health
Organization concerning the legal status of any country, territory, city or area or of
its authorities, or concerning the delimitation of its frontiers or boundaries.
210 National TB prevalence surveys 2007–2016
Symptom screening
Cough (any duration)a 2 637 (6.1%)
Haemoptysis 105 (0.2%)
Sputum production 2 117 (4.9%)
Fever 1 317 (3.1%)
Weight loss 4 001 (9.3%)
Total symptom-screen positivea 2 637 (6.1%)
Eligible for sputum examination 4 747 (11%) Symptom positive, chest X-ray positive 545 (12%)
Symptom positive, chest X-ray negative or N/A 2 092 (44%)
Symptom negative, chest X-ray positive 2 107 (44%)
Otherb 3 (0.1%)
Submitted specimens
At least one specimen 4 700 (99%)
Both specimens 4 412 (93%)
Laboratory result
At least one culture result availablec 4 589 (97%)
Total bacteriologically confirmed cases 40 Symptom positive, chest X-ray positive 15 (38%)
Symptom positive, chest X-ray negative or N/A 4 (10%)
Symptom negative, chest X-ray positive 21 (52%)
Other 0 (0%)
a
Eligible for sputum collection.
b
Chest X-ray exempted and symptom-screen negative.
c
Cultures that were either contaminated and/or missing without a definitive result (i.e. MTB, NTM, negative) were excluded.
d
Definite: MTB confirmed by culture. Probable: MTB not confirmed by culture but two smear-positive specimens or one smear-positive with chest X-ray suggestive of TB.
e
Definite: MTB confirmed by two cultures, or one culture with chest X-ray suggestive of TB. Probable: no definition.
212 National TB prevalence surveys 2007–2016
Fig. 1: Participation rate by age and sex Fig. 4: Cluster variation of the number of bacteriologically
confirmed TB casesb
100
40
35
Participation rate (%)
Number of clusters
30
25
90
20
15
10
5
80 0
15–24 25–34 35–44 45–54 55–64 ≥65 0 1 2 3
Age group (years) Number of bacteriologically confirmed TB cases
Male Female
Fig. 2: TB prevalence per 100 000 population by age Fig. 5: Ratio of smear-positive TB prevalence to notifications by
age and by sexc
450 3.0
Prevalence per 100 000 population
Fig. 3: Estimated number of bacteriologically confirmed TB cases Fig. 6: Estimates of TB prevalence (all ages, all forms of TB) before
and prevalence per 100 000 population, by agea (in blue) and after (in red) the national TB prevalence surveyd
4 000 300
Estimated number of bacteriologically
3 500
250
3 000
confirmed TB cases
200
2 500
2 000 150
1 500
100
1 000
50
500
0 0
15–34 35–54 ≥55 100 150
Age group (years) Prevalence per 100 000 population
a
The estimated number of bacteriologically confirmed TB cases is the product of age-specific prevalence and population estimates from the UN Population Division (2015 revision).
b
The data did not suggest that the distribution of cases by cluster (blue bars) was significantly different from the theoretical distribution (red line) (mean 0.55, variance 0.61, p=0.27).
The theoretical distribution assumes cases are distributed at random i.e. no clustering effect.
c
Notification rates were estimate of using notifications obtained from the WHO global TB database, and population estimates from the UN Population Division (2015 revision).
d
The blue bar denotes the best estimate of prevalence and its range that was indirectly derived from the estimate of incidence previously published by WHO, adjusted to the year of the
prevalence survey based on previously published trends in incidence.
RWANDA 213
The higher burden of TB among men and the elderly problem in Rwanda, by conducting genotyping of the
was consistent with routine surveillance data. However, current cases, characterizing the affected population
men were five times more likely than women to have TB, and determining the extent of the problem, as well
whereas among notified TB cases there were only twice as developing guidelines on treatment of NTM (such
as many men as women. These findings suggested under- guidelines did not exist at the time of the survey).
diagnosis among men and the elderly, and associated
differences in health-care seeking behaviour. Overall, the survey showed that current efforts in TB
prevention, diagnosis and treatment needed to be
Rwanda introduced a community health-insurance maintained while also being supplemented by new
system in 1999 to improve access to health care. In strategies, to ensure early detection and treatment of all
2012, 91% of the population was covered by this health cases, with a specific focus on key populations.
insurance and 83% of the population could access a
health-care facility within 2 hours of their home. Despite
improving access to health care, survey data showed that Major successes, challenges and lessons
people with TB or with symptoms meeting screening learned
criteria did not always seek care, especially if they were
poor, men or young adults. Overall, 70% of those with a The Rwandan survey showed that the country’s TB and
cough who had not sought care at the time of the survey TB/HIV services were well organized. However, since the
indicated that it was not important to do so; only 6% number of detected cases was so small compared with the
indicated that lack of money for transport was a barrier to estimated burden when the survey was designed, it was
accessing care (7). It appeared that people in the general hard to analyse in detail the characteristics of the detected
community were not identifying themselves as being TB cases.
at risk of developing TB disease, and that innovative
approaches would be needed to raise awareness and Most survey equipment was procured by the Rwanda
enhance care-seeking among individuals with a cough. Biomedical Center. Delays occurred in procurement
despite the process starting early. The original plan was
The survey also suggested that the existing advocacy, to import portable digital X-ray units, but this was not
communication and social mobilization strategy should possible because the national radiation authority did not
be reviewed to incorporate innovative strategies to aid approve the units. Digital units in a container system
TB control. Possibilities that were identified included were procured instead. During field operations, one
the use of role models or ambassadors, especially those digital container was accidentally dropped and required
with whom men could identify; raising awareness among a service.
health-care staff, given that only half of those who
sought care for a chronic cough were asked to submit a
sputum specimen for testing (7); improving health-care
staff awareness that men and the elderly are more likely
to have TB than other groups and are underdiagnosed;
and strategic case finding among the elderly, for example
through routine outpatient screening for TB in this age
group. After the survey, the NTP defined five high risk
groups that required greater attention: children under 15
years, people over 55 years, prisoners, people living with
HIV (PLHIV) and contacts of TB cases. In addition, the
NTP developed plans to use chest X-ray as a screening
tool among prisoners and PLHIV, and for the scale-up of
Xpert®MTB/RIF as a diagnostic tool.
human resource effort and a strong data management 7. The First National Tuberculosis Prevalence Survey 2012 in
Rwanda, Institute of HIV/AIDS, Disease Prevention & Control,
team. Tuberculosis & Other Respiratory Communicable Diseases
Division, Republic of Rwanda, Ministry of Health, 2015.
An external review confirmed that the central laboratory 8. World Health Organization. Tuberculosis prevalence surveys:
carried out culture examination in accordance with their a handbook (WHO/HTM/TB/2010.17). Geneva: WHO; 2011
standard operating procedures; that is, concentrated (https://apps.who.int/iris/bitstream/handle/10665/44481/
9789241548168_eng.pdf, accessed August 2017).
Löwenstein–Jensen media recommended by WHO.
Nonetheless, compared with surveys that used liquid
media (i.e. mycobacteria growth indicator tube), or
solid media without centrifuge (i.e. Ogawa method), the
yields by culture were limited. Of the 54 culture positive
participants, there were 38 participants with culture-
confirmed TB, and 3 of the 38 were excluded from the
final case list (in total there were 35 definite survey cases
and 5 probable cases). They had only an indication of TB
in one of the collected samples, which was not confirmed
by an indication in another sample or the central chest
X-ray reading. Therefore, it is likely that the prevalence of
bacteriologically confirmed TB was underestimated.
217
SUDAN
2013–2014
Summary statistics
Participation rate 86%
Symptom screening
Cough ≥2 weeksb 2 663 (3.3%)
Haemoptysis 221 (1.3%)c
Sputum production 2 169 (12%)c
Chest pain 4 039 (23%)c
Fever 3 657 (21%)c
Total symptom-screen positivea 2 663 (3.3%)
Eligible for sputum examination 17 541 (21%) Symptom positive, chest X-ray positive 1 823 (10%)
Symptom positive, chest X-ray negative or N/A 840 (4.8%)
Symptom negative or N/A, chest X-ray positive 9 838 (56%)
Othere 5 040 (29%)
Submitted specimens
At least one specimen 14 330 (82%)
Both specimens 11 313 (65%)
Laboratory result
At least one culture result availablef 14 017 (80%)
Smear-positive casesg 57 (51%) Smear-negative casesh 52 (46%) Smear unknown cases 3 (2.7%)
Definite 57 Definite 52 (culture MTB-positive)
Probable N/A Probable N/A
a
Of 192 individuals, 80 were exempted from chest X-ray and were not screened by interview. In addition, 112 individuals did not attend the survey site and were not screened by interview or
chest X-ray. Although a protocol violation, specimens were collected from these 112 individuals, and included in the final analysis (they were subsequently classified as off-site participants).
b
Eligible for sputum collection.
c
The denominator is 17 423 (on-site participants who screened positive).
d
Poor quality of film (13) and result missing (255). 13 (poor quality of film) out of 268 were asked to submit sputum.
e
Symptom-screen negative or missing and chest X-ray exempted (4899), symptom-screen negative and chest X-ray result N/A (13), symptom-screen negative or missing and chest X-ray negative
but currently on TB treatment (10), off-site participants (112), symptom-screen negative or missing and chest X-ray negative, not currently on TB treatment but submitted sputum in error (6).
f
Cultures that were either contaminated and/or missing without a definitive result (i.e. MTB, NTM, negative) were excluded.
g
Definite: MTB confirmed by culture and/or LPA. Probable: no definition.
h
Definite: MTB confirmed by culture. Probable: no definition.
i
Symptom-screen negative and chest X-ray exempted (9), symptom-screen negative or missing and chest X-ray negative, not currently on TB treatment but submitted sputum in error (6), off-site
participant (1).
220 National TB prevalence surveys 2007–2016
Fig. 1: Participation rate by age and sex Fig. 4: Cluster variation of the number of bacteriologically
confirmed TB casesb
100
55
50
45
Participation rate (%)
Number of clusters
90 40
35
30
25
80 20
15
10
5
70 0
15–24 25–34 35–44 45–54 55–64 ≥65 0 1 2 3 4 5 6 7 8
Age group (years) Number of bacteriologically confirmed TB cases
Male Female
Fig. 2: TB prevalence per 100 000 population by age Fig. 5: Ratio of smear-positive TB prevalence to notifications by
age and by sexc
500 7.0
Prevalence per 100 000 population
450
6.0
Prevalence : notification ratio
400
350 5.0
300
4.0
250
200 3.0
150 2.0
100
1.0
50
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 15–24 25–34 35–44 45–54 55–64 ≥65 Male Female Total
Age group (years) Age group (years) and sex (≥15)
Bacteriologically confirmed TB Smear-positive TB
Fig. 3: Estimated number of bacteriologically confirmed TB cases Fig. 6: Estimates of TB prevalence (all ages, all forms of TB) before
and prevalence per 100 000 population, by agea (in blue) and after (in red) the national TB prevalence surveyd
16 000 300
Estimated number of bacteriologically
14 000
250
12 000
confirmed TB cases
200
10 000
8 000 150
6 000
100
4 000
50
2 000
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 100 150 200 250 300
Age group (years) Prevalence per 100 000 population
a
The estimated number of bacteriologically confirmed TB cases is the product of age-specific prevalence and population estimates from the UN Population Division (2015 revision).
b
The data suggested that the distribution of cases by cluster (blue bars) was significantly different from the theoretical distribution (red line) (mean 1.03, variance 2.90, p<0.05). The
theoretical distribution assumes cases are distributed at random i.e. no clustering effect.
c
Notification rates were estimated using smear-positive pulmonary TB notifications (2013) obtained from the NTP, and population estimates from the UN Population Division (2015
revision).
d
The blue bar denotes the best estimate of prevalence and its range that was indirectly derived from the estimate of incidence previously published by WHO, adjusted to the year of the
prevalence survey based on previously published trends in incidence.
SUDAN 221
87 (95% CI: 52–121) per 100 000 population (among treatment and 7.1% were on anti-TB treatment
those aged ≥15 years), and for bacteriologically at the time of the survey; and
confirmed TB it was 183 (95% CI: 128–238) per 100 000 • of the 44 bacteriologically confirmed and 26
population. When extrapolated to all forms of TB and smear-positive TB survey cases that screened
positive for symptoms and were not on anti-TB
to all ages, prevalence was 172 (95% CI: 122–222) per
treatment at the time of the survey, 30 (68%) and
100 000 population. The prevalence of smear-positive and 16 (62%), respectively, had previously sought
bacteriologically confirmed TB was higher in urban than care in a public or private health facility for their
in rural areas. symptoms.
References
1. The World Bank (https://data.worldbank.org/country, accessed
April 2017).
2. UNAIDS (http://aidsinfo.unaids.org/, accessed April 2017).
3. World Health Organization. Global Tuberculosis Database. 2017.
(http://www.who.int/tb/country/en/, accessed April 2017).
4. World Health Organization. Global tuberculosis report
2013. Geneva: WHO; 2013 (http://apps.who.int/iris/
bitstream/10665/91355/1/9789241564656_eng.pdf, accessed
January 2018).
5. World Health Organization. Global tuberculosis report
2014. Geneva: WHO; 2014 (http://apps.who.int/iris/
bitstream/10665/137094/1/9789241564809_eng.pdf, accessed
January 2018).
6. World Health Organization. Tuberculosis prevalence surveys:
a handbook (WHO/HTM/TB/2010.17). Geneva: WHO; 2011
(https://apps.who.int/iris/bitstream/handle/10665/44481/
9789241548168_eng.pdf, accessed August 2017).
225
THAILAND
2012–2013
Summary statistics
Participation rate 79%
Key people
Name Role Organization
Sriprapa Nateniyom Principal investigator Bureau of Tuberculosis
Sirinapha Jittimanee Survey coordinator Bureau of Tuberculosis
Saijai Smithtikarn Laboratory coordinator Bureau of Tuberculosis
Wilawan Dangsaart Radiology coordinator Bureau of Tuberculosis
Wiriya Madasin Data manager Bureau of Tuberculosis
Autagorn Chunmathong Field team leader Bureau of Tuberculosis
Runjuan Sukkavee Field team leader Bangkok Metropolitan Administration
Nuntaporn Meksawasdichai Field team leader Institute for Urban Disease Control and Prevention, Bangkok
Pattana Pokaew Field team leader ODPC 1, Chiangmai
Sakchai Chaiamahapurk Field team leader ODPC 2, Pitsanulok
Pavasuth Chutjuntaravong Field team leader ODPC 3, Nakhonsawan
Supaporn Wattanatoan Field team leader ODPC 4, Saraburi
Ratree Dokkabowt Field team leader ODPC 5, Ratchaburi
Ornnipa Iamsamang Field team leader ODPC 6, Chonburi
Narong Wongba Field team leader ODPC 7, Konkaen
Phalin Kamolwat Field team leader ODPC 9, Nakhonratchasima
Walaya Sitti Field team leader ODPC 10, Ubonratchathani
Kamonwan Imduang Field team leader ODPC 11, Nakhonsrithamarat
Auyporn Petborisuit Field team leader ODPC 12, Songkhla
Norio Yamada Technical assistance (data analysis) Research Institute of Tuberculosis/Japan Anti-Tuberculosis Association (RIT/JATA)
Hataichanok Pukcharern Technical assistance (sampling methodology) National Statistics Office, Thailand
Ikushi Onozaki Technical assistance (survey methodology) WHO headquarters
Symptom screening
Cough ≥2 weeks 1 775 (2.8%)
Cough <2 weeks 4 620 (7.4%)
Haemoptysis over the past month 121 (0.2%)
Weight loss in the past month 1 679 (2.7%)
Fever ≥1 week in the past two weeks 752 (1.2%)
Night sweats in the past month 1 057 (1.7%)
Clinical score ≥3a 2 260 (3.6%)
Clinical score=1 or 2 with chest X-ray exempteda 23 (0.04%)
Total symptom-screen positivea 2 283 (3.7%)
Eligible for sputum examination 6 050 (9.7%) Symptom positive, chest X-ray positive 526 (8.7%)
Symptom positive, chest X-ray negative or N/A 1 757 (29%)
Symptom negative, chest X-ray positive 3 767 (62%)
Other N/A
Submitted specimens
At least one specimen 5 988 (99%)
Both specimens 5 720 (95%)
Laboratory result
At least one culture result availablec 5 821 (96%)
Total bacteriologically confirmed cases 142 Symptom positive, chest X-ray positive 42 (30%)
Symptom positive, chest X-ray negative or N/A 6 (4.2%)
Symptom negative, chest X-ray positive 94 (66%)
Other N/A
a
Eligible for sputum collection.
b
The result was missing or could not be read due to the poor quality of the chest X-ray.
c
Cultures that were either contaminated and/or missing without a definitive result (i.e. MTB, NTM, negative) were excluded.
d
Definite: MTB confirmed by culture. Probable: MTB not confirmed by culture, but at least one smear-positive with chest X-ray suggestive of TB, or two smear-positive, or one smear-positive
and confirmed as TB cases by referral health facilities.
e
Definite: MTB confirmed by culture (one significant culture-positive, or two scanty culture-positive, or one scanty culture-positive with chest X-ray suggestive of TB), or confirmed as TB
cases by referral health facilities. Probable: no definition.
228 National TB prevalence surveys 2007–2016
Fig. 1: Participation rate by age and sex Fig. 4: Cluster variation of the number of bacteriologically
confirmed TB casesb
100
25
90 20
Participation rate (%)
Number of clusters
15
80
10
70
5
60 0
15–24 25–34 35–44 45–54 55–64 ≥65 0 1 2 3 4 5 6 7 8
Age group (years) Number of bacteriologically confirmed TB cases
Male Female
Fig. 2: TB prevalence per 100 000 population by age Fig. 5: Ratio of smear-positive TB prevalence to notifications by
age and by sexc
800 3.0
Prevalence per 100 000 population
500 2.0
400 1.5
300
1.0
200
100 0.5
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 15–24 25–34 35–44 45–54 55–64 ≥65 Male Female Total
Age group (years) Age group (years) and sex (≥15)
Bacteriologically confirmed TB Smear-positive TB
Fig. 3: Estimated number of bacteriologically confirmed TB cases Fig. 6: Estimates of TB prevalence (all ages, all forms of TB) before
and prevalence per 100 000 population, by agea (in blue) and after (in red) the national TB prevalence surveyd
35 000 500
Estimated number of bacteriologically
450
Prevalence per 100 000 population
30 000
400
25 000
confirmed TB cases
350
20 000 300
250
15 000
200
10 000 150
100
5 000
50
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 100 150 200 250 300
Age group (years) Prevalence per 100 000 population
a
The estimated number of bacteriologically confirmed TB cases is the product of age-specific prevalence and population estimates from the UN Population Division (2015 revision).
b
The data suggested that the distribution of cases by cluster (blue bars) was significantly different from the theoretical distribution (red line) (mean 1.71, variance 3.16, p<0.05). The
theoretical distribution assumes cases are distributed at random i.e. no clustering effect.
c
Notification rates were estimated using notifications obtained from the WHO global TB database, and population estimates from the UN Population Division (2015 revision).
d
The blue bar denotes the best estimate of prevalence and its range that was indirectly derived from the estimate of incidence previously published by WHO, adjusted to the year of the
prevalence survey based on previously published trends in incidence.
THAILAND 229
Before 2012, Thailand had already carried out four Phase 1 included two strata (urban and rural), with
national TB prevalence surveys: in 1962, 1977, 1991–1992 a target cluster size of 900 individuals. No data were
and 2006. The observed prevalence of bacteriologically available on the numbers of individuals enumerated
confirmed TB declined from 500 per 100 000 population in the household census. 78 839 people were eligible
(among those aged ≥15 years) in 1962 to 310 per 100 000 and invited to participate. Of these, 62 536 (79%) did
population (among those aged ≥15 years) in 1977 and 240 so. A total of 6050 participants (9.7%) were eligible for
per 100 000 population (among those aged ≥10 years) in sputum examination based on chest X-ray and symptom
1991 (7). Although the 2006 survey used interviews and screening. Of these, 5988 (99%) submitted at least one
chest X-rays for screening, and culture for diagnostic sputum specimen and 5720 (95%) submitted two sputum
confirmation, the survey could not be used to estimate specimens.
prevalence due to a low participation rate (56%), untimely
reading of chest X-rays (this was only done after each A total of 142 bacteriologically confirmed pulmonary TB
field cluster operation), and a low sputum submission cases were identified, including 58 cases of smear-positive
rate from eligible participants (19%). The fifth national TB. The prevalence of bacteriologically confirmed TB was
survey was implemented in 2012–2013. 242 (95% CI: 176–332) per 100 000 population (among
those aged ≥15 years), and for smear-positive TB it was
104 (95% CI: 55–195) per 100 000 population. There was
no significant difference between urban strata (286 per
100 000 population; 95% CI: 158–518) and rural strata
(220 per 100 000 population; 95% CI: 170–284).
230 National TB prevalence surveys 2007–2016
late 1990s, but it may also reflect the higher sensitivity of The geographical variation in TB was also of concern.
methods used to detect smear-negative culture-positive Among 142 bacteriologically confirmed patients detected
TB in the 2012 survey. In addition, since programmatic by the survey, 81 (57%) were from the economically less-
efforts prioritized the detection and treatment of smear- developed north-eastern region. Although confidence
positive TB cases, the impact of TB control efforts was intervals were wide, results suggested that the level of TB
more likely to be seen in the prevalence of smear-positive prevalence in the north-eastern region could be more
TB. The observed prevalence of smear-positive TB in than twice that of other regions in Thailand.
1991–1992 (170 per 100 000 population, ≥10 years) was
higher than the level found in 2012 (104 per 100 000 The classical pathway to detect TB (i.e. chronic cough
population; 95% CI: 55–195, ≥15 years) (7). Nonetheless, recognition to diagnosis by smear) would only have
smear-positive TB accounted for only 41% of the total detected one-fifth of the bacteriologically confirmed TB
number of prevalent bacteriologically confirmed TB survey cases (26/142). This showed the need for wider
cases in the 2012 survey. use of chest X-rays and more sensitive tools, such as
molecular technologies, in the diagnostic pathway.
Age-specific estimates of TB prevalence in 2012 also
suggested a long-term decline in the burden of TB. Those It was also evident that the case notification system
aged 45 years or more accounted for more than two thirds needed improvement; for example, by introducing
of TB cases, suggesting that reactivation of infection from and monitoring mandatory notification of designated
the past was playing a greater role than recent infection. infectious diseases, including TB. Based on the survey, as
However, an ageing population also contributed to a many as 20% of the cases on anti-TB treatment may have
relatively slow decline in the overall burden of TB. been missed in the TB surveillance system.
References
1. The World Bank (https://data.worldbank.org/country, accessed
April 2017).
2. UNAIDS (http://aidsinfo.unaids.org/, accessed April 2017).
3. World Health Organization. Global Tuberculosis Database. 2017.
(http://www.who.int/tb/country/en/, accessed April 2017).
4. WHO Tuberculosis Programme. (1994). WHO Tuberculosis
Programme: framework for effective tuberculosis
control. World Health Organization. (http://www.who.int/iris/
handle/10665/58717, accessed January 2018).
5. World Health Organization. Global tuberculosis programme.
Global tuberculosis control report 1997. Geneva: WHO; (https://
apps.who.int/iris/bitstream/handle/10665/63354/WHO_
TB_97.225_(part1).pdf?sequence=1, accessed January 2018).
6. World Health Organization. Global tuberculosis report
2013. Geneva: WHO; 2013; (http://apps.who.int/iris/
bitstream/10665/91355/1/9789241564656_eng.pdf, accessed
January 2018).
7. Sriyabhaya N, Payanandana V, Bamrungtrakul T, Konjanart S.
Status of tuberculosis control in Thailand. Southeast Asian J Trop
Med Public Health. 1993;24(3):410–419; (http://www.tm.mahidol.
ac.th/seameo/1993-24-3/1993-24-3-410.pdf, accessed January
2018).
8. World Health Organization. Tuberculosis prevalence surveys:
a handbook (WHO/HTM/TB/2010.17). Geneva: WHO; 2011.
(https://apps.who.int/iris/bitstream/handle/10665/44481/
9789241548168_eng.pdf, accessed August 2017).
9. World Health Organization. Global tuberculosis report
2015. Geneva: WHO; 2015; (http://apps.who.int/iris/
bitstream/10665/191102/1/9789241565059_eng.pdf, accessed
January 2018).
10. World Health Organization. Global tuberculosis control: WHO
report 2011. Geneva: WHO; 2011; (http://apps.who.int/iris/
bitstream/10665/44728/1/9789241564380_eng.pdf, accessed
January 2018).
11. Department of Economic and Social Affairs. World urbanization
prospect: the 2014 revision (CD Rom edition). United Nations;
2014; (https://esa.un.org/unpd/wup/CD-ROM/, accessed January
2018)
233
UGANDA
2014–2015
Summary statistics
Participation rate 91%
Key people
Name Role Organization
Frank Mugabe Principal investigator - policy Ministry of Health
Elizeus Rutebemberwa Principal investigator - technical School of Public Health, Makerere University
Bruce Kirenga Co-principal investigator School of Public Health, Makerere University
Samuel Kasozi Study coordinator School of Public Health, Makerere University
Harriet Kisembo Study investigator, lead radiologist Mulago hospital
Okot Martin Nwang Study investigator Senior consultant pulmonologist and head of medical panel, Mulago hospital & complex
William Worodria Study investigator Department of Medicine Mulago hospital & complex
Abel Nkolo Study investigator WHO Uganda
Emily Bloss Study investigator US Centers for Disease Control and Prevention (CDC)
Moses Joloba Survey laboratory consultant and director National TB Reference Laboratory
Kenneth Musisi Laboratory manager National TB Reference Laboratory
Rogers Sekibira Data manager School of Public Health, Makerere University
Ronald Anguzu Field team leader School of Public Health, Makerere University
Annet Nagudi Field team leader School of Public Health, Makerere University
Racheal Tumwebaze Field team leader School of Public Health, Makerere University
Wilfred Nkhoma Technical assistance (survey advisor) WHO Regional Office for Africa (AFRO)
Ikushi Onozaki Technical assistance (survey advisor) WHO headquarters
Marina Tadolini Technical assistance (survey advisor) Consultant, Italy
Peou Satha Technical assistance (radiology) Consultant, Cambodia
Julia Ershova Technical assistance (data management) US Centers for Disease Control and Prevention (CDC)
Charalampos Sismanidis Technical assistance (analysis) WHO headquarters
a
The boundaries and names shown and the designations used on this map do not
imply the expression of any opinion whatsoever on the part of the World Health
Organization concerning the legal status of any country, territory, city or area or of
its authorities, or concerning the delimitation of its frontiers or boundaries.
234 National TB prevalence surveys 2007–2016
Symptom screening
Cough ≥2 weeksa 2 714 (6.6%)
Haemoptysis 263 (0.6%)
Sputum production 4 819 (12%)
Chest pain 12 142 (30%)
Fever 3 593 (8.7%)
Total symptom-screen positivea 2 714 (6.6%)
Eligible for sputum examination 5 142 (13%) Symptom positive, chest X-ray positive 552 (11%)
Symptom positive, chest X-ray negative or N/A 2 162 (42%)
Symptom negative, chest X-ray positive 2 298 (45%)
Otherb 130 (2.5%)
Submitted specimens
At least one specimen 4 844 (94%)
Both specimens 4 532 (88%)
Laboratory result
At least one culture result availablec 4 758 (93%)
Total bacteriologically confirmed cases 160 Symptom positive, chest X-ray positive 63 (39%)
Symptom positive, chest X-ray negative or N/A 16 (10%)
Symptom negative, chest X-ray positive 81 (51%)
Other 0 (0%)
a
Eligible for sputum collection.
b
Chest X-ray exempted and symptom-screen negative.
c
Cultures that were either contaminated and/or missing without a definitive result (i.e. MTB, NTM, negative) were excluded.
d
Definite: MTB confirmed by culture and/or Xpert. Probable: MTB not confirmed by culture and/or Xpert, but chest X-ray consistent with TB.
e
Definite: MTB confirmed by culture and/or Xpert with chest X-ray consistent with TB. Probable: culture weak positive (<20 colonies) in one sample and Xpert pending or N/A without
negative evidence on chest X-ray (i.e. chest X-ray not taken).
236 National TB prevalence surveys 2007–2016
Fig. 1: Participation rate by age and sex Fig. 4: Cluster variation of the number of bacteriologically
confirmed TB casesb
100
20
Participation rate (%)
Number of clusters
90 15
10
80
5
70 0
15–24 25–34 35–44 45–54 55–64 ≥65 0 1 2 3 4 5 6 7 8 9 10 11 12 13
Age group (years) Number of bacteriologically confirmed TB cases
Male Female
Fig. 2: TB prevalence per 100 000 population by age Fig. 5: Ratio of bacteriologically confirmed TB prevalence to
notifications by age and by sexc
1000 5.0
Prevalence per 100 000 population
Fig. 3: Estimated number of bacteriologically confirmed TB cases Fig. 6: Estimates of TB prevalence (all ages, all forms of TB) before
and prevalence per 100 000 population, by agea (in blue) and after (in red) the national TB prevalence surveyd
25 000 700
Estimated number of bacteriologically
600
20 000
500
confirmed TB cases
15 000
400
10 000 300
200
5 000
100
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 100 150 200 250 300
Age group (years) Prevalence per 100 000 population
a
The estimated number of bacteriologically confirmed TB cases is the product of age-specific prevalence and population estimates from the UN Population Division (2015 revision).
b
The data suggested that the distribution of cases by cluster (blue bars) was significantly different from the theoretical distribution (red line) (mean 2.29, variance 5.42, p<0.05). The
theoretical distribution assumes cases are distributed at random i.e. no clustering effect.
c
Notification rates were estimated using bacteriologically confirmed pulmonary TB notifications (2015) obtained from the NTP, and population estimates from the UN Population Division
(2015 revision).
d
The blue bar denotes the best estimate of prevalence and its range that was indirectly derived from the estimate of incidence previously published by WHO, adjusted to the year of the
prevalence survey based on previously published trends in incidence.
UGANDA 237
Urban areas had a higher prevalence per 100 000 popu- Major successes, challenges and lessons
lation than rural areas, and there were three times more learned
cases of TB among men than women. Thus, the NTLP
needed to give more attention to ensuring access to It was a major success to implement the country’s first
screening and enrolment on treatment among men and national TB prevalence survey. Survey preparations
for people living in urban areas. started in 2008, but there were long delays
primarily due to the challenge of securing funding.
The TB/HIV data showed that integration of HIV services Whereas prevalence surveys in other countries
with anti-TB treatment should be continued. introduced technologies such as digital chest X-ray
or electronic data collection in the field, the Ugandan
Of participants with smear-positive specimens, 28%
survey used only conventional chest X-ray equipment
(25/91) did not have Mycobacterium tuberculosis (MTB).
and paper-based data collection because of limitations on
Thus, a smear-positive result alone was not adequate for
funding and time. Data were entered into the database at
the detection of TB cases, especially in the context of
central level upon completion of each cluster operation.
intensified case finding or active case detection strategies.
Nonetheless, the quality of the survey was exceptionally
Before the survey, Uganda was in the list of 22 HBCs high.
as defined by WHO. The survey identified a higher
There were no major delays in survey implementation
prevalence than expected, but the results were available
resulting from major accidents or equipment failure.
only after a new list of 30 HBCs was defined by WHO for
However, the X-ray machine often had to be restarted due
the period 2016–2020. The need for good communication
to excessive humidity and heat, which affected the auto-
between all levels of WHO, the NTLP and the MoH to
film processor. Therefore, X-ray examinations were often
determine the consequences of Uganda not being in the
interrupted, and participants were kept waiting.
list of 30 TB HBCs (although it remained on the list of
high TB/HIV burden countries) was recognized. A high participation rate, both in rural and urban clusters,
was achieved due to the dedication of the central and field
teams, community involvement and careful preparation
of survey operations (especially in big cities). A high
sputum collection rate was also achieved. Uganda’s survey
was also one of the first to provide high-quality data on
Summary statistics
Participation rate 77%
Key people
Name Role Organization
Saidi M. Egwaga Principal investigator (PI) National Tuberculosis and Leprosy Programme (NTLP)
Godfrey S. Mfinanga Co-PI National Institute for Medical Research (NIMR), Muhimbili Medical Research Center
Deusdedit V. Kamara Survey coordinator NTLP
Senkoro Mbazi Assistant survey coordinator NIMR, Muhimbili Medical Research Center
Ahmed Khatib Programme manager Zanzibar Tuberculosis and Leprosy Programme
Basra Doulla Laboratory manager Central TB Reference Laboratory (CTRL), NTLP
Lulu Fundikira Radiology coordinator Muhimbili University of Health and Allied Sciences (MUHAS)
Raymond P. Shirima Data manager NTLP
Blasdus F. Njako Field team leader NTLP
Msaki John Field team leader NIMR
Rahim Ishumi Field team leader NIMR
Lugano Mtafya Field team leader NIMR
Moses Ringo Field team leader NIMR
Frank van Leth Technical assistance (survey advisor) KNCV Tuberculosis Foundation
Wilfred Nkhoma Technical assistance (survey advisor) WHO Regional Office for Africa (AFRO)
Ikushi Onozaki Technical assistance (survey advisor) WHO headquarters
Charalampos Sismanidis Technical assistance (analysis) WHO headquarters
Laboratory methodology
Health-care seeking behaviour among
Smear Three samples (spot, morning and spot; Number %
participants who were symptom-screen positive
both spot samples were examined in
Participants who were symptom-screen 3 388 –
the field, and a morning sample was
positivea
examined in the central laboratory): direct
preparation, FM (LED, auramine stain) Location of care sought
Culture One sample (morning): concentrated • Consulted medical facility 481 14
preparation, LJ media Public facility (incl. mission hospital) 445 93
Identification of MTB PNB Private facility 36 7.5
TB drug susceptibility test Done at the Antwerp SRL, not as part of • Pharmacy 147 4.3
the original protocol • Traditional centre 11 0.3
Xpert® MTB/RIF Done only for smear-positive slides to • Otherb 412 12
confirm the presence of MTB at the
Self-treated N/A N/A
Antwerp SRL, not as part of the original
protocol No action taken 1 688 50
HIV test Done for participants who screened Unknown 649 19
positive a
Data on health-care seeking behaviour were only available for participants who
reported cough ≥2 weeks and/or haemoptysis.
b
This included 257 dispensaries and 155 unspecified locations.
Analysis and reporting
Survey participants currently on TB treatment Number %
Field data collection Paper Total participants currently on TB treatment 88 –
Database EpiData • Treated in the public sector N/A N/A
Method of analysis Cluster-levela • Treated in the private sector N/A N/A
Results first published in a report/paper August 2013 • Treated in other sector N/A N/A
Official dissemination event July 2013 Smear-positive TB cases detected by the 5 3.7
a
Reported prevalence results are based on a re-analysis by WHO. survey who were currently on TB treatment
UNITED REPUBLIC OF TANZANIA 243
Symptom screening
Cough ≥2 weeksa 3 238 (6.5%)
Haemoptysisa 536 (1.1%)
Fever ≥2 weeka 932 (1.9%)
Weight lossa 531 (1.1%)
Night sweatsa 1 188 (2.4%)
Total symptom-screen positivea 4 263 (8.6%)
Eligible for sputum examination 6 302 (13%) Symptom positive, chest X-ray positive 804 (13%)
Symptom positive, chest X-ray negative or N/A 3 459 (55%)
Symptom negative, chest X-ray positive 2 039 (32%)
Other N/A
Submitted specimens
At least one specimen 5 768 (92%)
Three specimens 4 705 (75%)
Laboratory result
At least one culture result availableb 4 723 (75%)
a
Eligible for sputum collection.
b
Cultures that were either contaminated and/or missing without a definitive result (i.e. MTB, NTM, negative) were excluded.
c
Definite: MTB confirmed by culture (NTRL) and/or Xpert (Antwerp SRL). Probable: MTB not confirmed by culture or Xpert, but chest X-ray final reading “consistent with TB”. Please see
the main text for further details.
d
13 were screened negative, and these people were not part of the total number of people eligible for sputum examination. The reason for their sputum submission was unknown.
244 National TB prevalence surveys 2007–2016
Fig. 1: Participation rate by age and sex Fig. 4: Cluster variation of the number of smear-positive TB casesb
100
20
90
Participation rate (%)
Number of clusters
15
80
10
70
5
60 0
15–24 25–34 35–44 45–54 55–64 ≥65 0 1 2 3 4 5 6 7 8
Age group (years) Number of smear-positive TB cases
Male Female
Fig. 2: TB prevalence per 100 000 population by age Fig. 5: Ratio of smear-positive TB prevalence to notifications by
age and by sexc
1000 7.0
Prevalence per 100 000 population
900
6.0
Prevalence : notification ratio
800
700 5.0
600
4.0
500
400 3.0
300 2.0
200
1.0
100
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 15–24 25–34 35–44 45–54 55–64 ≥65 Male Female Total
Age group (years) Age group (years) and sex (≥15)
Smear-positive TB
Fig. 3: Estimated number of smear-positive TB cases and Fig. 6: Estimates of TB prevalence (all ages, all forms of TB) before
prevalence per 100 000 population, by agea (in blue) and after (in red) the national TB prevalence surveyd
25 000 700
Estimated number of smear-positive
600
20 000
500
15 000
400
TB cases
10 000 300
200
5000
100
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 200 400 600
Age group (years) Prevalence per 100 000 population
a
The estimated number of smear-positive TB cases is the product of age-specific prevalence and population estimates from the UN Population Division (2015 revision).
b
The data suggested that the distribution of cases by cluster (blue bars) was significantly different from the theoretical distribution (red line) (mean 2.16, variance 4.24, p<0.05). The
theoretical distribution assumes cases are distributed at random i.e. no clustering effect.
c
Notification rates were estimated using notifications obtained from the WHO global TB database, and population estimates from the UN Population Division (2015 revision).
d
The blue bar denotes the best estimate of prevalence and its range that was indirectly derived from the estimate of incidence previously published by WHO, adjusted to the year of the
prevalence survey based on previously published trends in incidence.
UNITED REPUBLIC OF TANZANIA 245
differences among three geographical strata (urban, the number of culture-positive TB cases from the survey
semi-urban and rural) in the level of smear-positive TB was underestimated. Following discussion and review of
prevalence among those aged 15 years or more. No TB laboratory results with external partners including the
cases were identified in Zanzibar. country’s Supranational Reference Laboratory (SRL) in
Antwerp, Belgium, as well as WHO, there was consensus
Other key results were: that the culture results from the prevalence survey could
• the male to female ratio for TB prevalence was not be used (8–10).
2.3 for smear-positive pulmonary TB;
In an attempt to confirm the validity of the smear-
• prevalence increased with age, with a notably
high level per 100 000 population (and estimated positive test results, and following discussions between
number of smear-positive cases) in those aged the NTLP in the United Republic of Tanzania, the head
25–44 years; of the Central TB Reference Laboratory (CTRL), the
• among smear-positive pulmonary TB cases, survey team, the KNCV Tuberculosis Foundation (the
44% were symptom-screen positive; main technical partner) and WHO, it was agreed to send
• for smear-positive pulmonary TB, the ratio of all specimen slides classified as smear-positive for testing
prevalence to notifications (P:N ratio) was 3.0 using Xpert® MTB/RIF to the SRL Antwerp. A positive
overall, but varied from 1.3 in those aged 15–
Xpert result would exclude false-positive microscopy
24 years to 6.6 in those aged 65 years or more;
the ratio was slightly higher for men than for as well as NTM (without the presence of MTB in the
women (3.3 versus 2.8); case of mixed infection). Results from the SRL (which
• among smear-positive pulmonary TB cases, 93% became available in September 2014) concluded that
had no previous history of anti-TB treatment, “...an estimate of prevalence based on microscopy-positives
and only 3.7% were receiving treatment at the could be justified” (11). The final case count, combining
time of the survey; and SRL Antwerp and survey CTRL results, was a total of
• among participants who screened-positive, 134 smear-positive TB cases, compared with 100 from
5.0% (318 of 6302) tested HIV-positive. the initial analysis based only on survey CTRL findings
No data on health-care seeking behaviour among smear- (8–10). This final count is the one used in this profile.
positive TB cases were collected.
To estimate the prevalence of bacteriologically confirmed
Unfortunately, the number of bacteriologically confirmed TB among those aged 15 years or more, data from the
TB cases could not be validated. In the survey, field teams neighbouring countries of Ethiopia, Malawi, Rwanda,
prioritized the detection of smear-positive individuals Uganda and Zambia were used. From surveys in these
in the field and the early treatment of these people. five countries, the combined estimate of the ratio of
Microscopy laboratories – using light-emitting diode bacteriologically confirmed to smear-positive TB was
fluorescence microscopy (LED FM) – were set up in 2.16:1 (standard deviation [SD]: 0.46).2 This ratio was
every cluster site by senior laboratory staff from the applied to the smear-positive prevalence estimate for the
Central TB Reference Laboratory (CTRL). However, United Republic of Tanzania, resulting in an estimate of
this had an unintended negative effect on the quality of the prevalence of bacteriologically confirmed TB of 590
samples collected, and on testing by culture. For example, (95% CI: 330–860) per 100 000 population. A further step
many samples (possibly as many as half) took more than of extrapolation to all forms of TB and all ages resulted in
a week to reach the CTRL; and a preliminary survey an estimated TB prevalence of 443 (95% CI: 258–629) per
report stated there were 100 TB cases with a smear- 100 000 population.
positive result1 and 73 with a culture-positive result (6)
- such a finding had never previously been observed in
a national TB prevalence survey that followed the 2011
WHO guidelines (7). This in turn led to concerns that
1
The NTLP’s smear-positive case definition: two smear-positive specimens 2
To extrapolate the prevalence of bacteriologically confirmed TB among those
regardless of culture result, one smear-positive specimen with chest X-ray aged ≥15 years to the prevalence of TB for all ages and all forms of TB, it was
abnormality consistent with TB, or smear-positive specimen with a culture assumed that 45% of the general population were children, that extrapulmonary
positive result. TB accounted for 23% (SD 9%) of all TB cases (based on 2008-2012 notification
data) and that the ratio of childhood to adult TB was 0.07 (SD 0.03).
UNITED REPUBLIC OF TANZANIA 247
A striking finding of the survey was that 52% of the • smear microscopy in the field is technically
feasible, but in practice it can be fraught with
identified smear-positive TB cases were aged 45 years
potential contamination issues;
or more. This indicated that prevalent TB was largely
• multiple paper forms were used for data
driven by progression from a much earlier acquisition collection (including handwritten individual
of a latent infection. In contrast, routine programmatic identifiers), and administrative errors made it
data from 2012 showed that only 28% of notified TB cases difficult or impossible to match the personal
were aged 45 years or more, indicating important gaps in identifiers on these forms with laboratory
the detection of cases in the middle to older age groups. specimens and other clinical information;
digital data entry and barcoding is vital to
The large proportion of prevalent TB cases in older age
ensure the quality of data management in future
groups points towards a historic positive effect of NTLP surveys;
control strategies; however, differences with the estimated • there was erroneous oversampling of study
number of notified TB cases suggested a need for the participants in the initial clusters, to increase
NTLP to reassess its screening and diagnostic strategies participation. Such protocol violations need to
(for example, to widen the range of symptoms considered be avoided;
when screening for TB in routine practice, and expand • some recommendations from external
the use of chest X-ray), and to create better community monitoring missions were not implemented in
awareness about the symptoms of TB. The strong a timely manner, thus potentially impacting on
survey quality;
emphasis of the NTLP on TB/HIV activities may have
• vehicles with computerized radiography
taken attention away from a large, unidentified population equipment had to be checked and serviced
of older HIV-negative people with TB. The post-survey during the survey and given the technology used,
estimate of the case detection rate (notifications of new additional manual steps and human resources
cases divided by estimated incidence) in 2015 was only were required to develop images before reading
36% (95% CI: 21–77), compared with a pre-survey
estimate of 79% (95% CI: 74–84%) (12,13).
VIET NAM
2006–2007
Summary statistics
Participation rate 91%
Symptom screening
Productive cough ≥2 weeksc 4 172 (4.5%)
Haemoptysis 134 (1.8%)d
Chest pain 2 012 (27%)d
Fever 820 (11%)d
Night sweats 470 (6.2%)d
Weight loss 885 (12%)d
Total symptom-screen positivea 4 172 (4.5%)
Eligible for sputum examination 8 005 (8.5%) Symptom positive, chest X-ray positive 518 (6.5%)
Symptom positive, chest X-ray negative or N/A 3 522 (44%)
Symptom negative, chest X-ray positive 2 972 (37%)
Otherf 993 (12%)
Submitted specimens
At least one specimen 7 648 (96%)
At least two specimens 7 554 (94%)
Three specimens 7 117 (89%)
Laboratory result
At least one culture result availableg 7 257 (91%)
a
There were 137 549 individuals in the census, and only adults (≥15 years) were counted for the prevalence survey.
b
23 160 children (6–14 years) from the same population as the prevalence survey participated in a concurrent tuberculin survey (see reference 11).
c
Eligible for sputum collection.
d
The denominator is the number of participants who had an in-depth interview (N=7580).
e
The results were not recorded.
f
Currently on TB treatment, including participants who screened positive (symptom and/or chest X-ray) (64), history of TB in the two years preceding the survey, including participants
who screened positive (symptom and/or chest X-ray) (364), chest X-ray exempted and symptom-screen negative (58), and participants who were not eligible for sputum submission but
submitted sputum based on the team leader’s decision (507).
g
Cultures that were either contaminated and/or missing without a definitive result (i.e. MTB, NTM, negative) were excluded.
h
Definite: MTB confirmed by culture. Probable: MTB not confirmed by culture but either two or more positive smears, one positive smear with chest X-ray consistent with TB.
i
Definite: MTB confirmed by culture. Probable: no definition.
j
One was chest X-ray exempted and 16 were included due to the team leader’s decision.
252 National TB prevalence surveys 2007–2016
Fig. 1: Participation rate by age and sex Fig. 4: Cluster variation of the number of bacteriologically
confirmed TB casesb
100
15
Participation rate (%)
Number of clusters
90
10
80
5
70 0
15–24 25–34 35–44 45–54 55–64 ≥65 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15
Age group (years) Number of bacteriologically confirmed TB cases
Male Female
Fig. 2: TB prevalence per 100 000 population by age Fig. 5: Ratio of smear-positive TB prevalence to notifications by
age and by sexc
1200 3.5
Prevalence per 100 000 population
3.0
Prevalence : notification ratio
1000
2.5
800
2.0
600
1.5
400
1.0
200 0.5
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 15–24 25–34 35–44 45–54 55–64 ≥65 Male Female Total
Age group (years) Age group (years) and sex (≥15)
Bacteriologically confirmed TB Smear-positive TB
Fig. 3: Estimated number of bacteriologically confirmed TB cases Fig. 6: Estimates of TB prevalence (all ages, all forms of TB) before
and prevalence per 100 000 population, by agea (in blue) and after (in red) the national TB prevalence surveyd
50 000 900
Estimated number of bacteriologically
45 000
Prevalence per 100 000 population
800
40 000 700
confirmed TB cases
35 000 600
30 000
500
25 000
400
20 000
15 000 300
200
10 000
5 000 100
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 200 300 400 500 600
Age group (years) Prevalence per 100 000 population
a
The estimated number of bacteriologically confirmed TB cases is the product of age-specific prevalence and population estimates from the UN Population Division (2015 revision).
b
The data suggested that the distribution of cases by cluster (blue bars) was significantly different from the theoretical distribution (red line) (mean 3.84, variance 9.35, p<0.05). The
theoretical distribution assumes cases are distributed at random i.e. no clustering effect.
c
Notification rates were estimated using notifications obtained from the WHO global TB database, and population estimates from the UN Population Division (2015 revision).
d
The blue bar denotes the best estimate of prevalence and its range that was indirectly derived from the estimate of incidence previously published by WHO, adjusted to the year of the
prevalence survey based on previously published trends in incidence.
VIET NAM 253
1
Tuberculin surveys were used to estimate the annual risk of infection but did
not provide a direct measure of the burden of TB disease.
Photo credit: Frank Cobelens
254 National TB prevalence surveys 2007–2016
northern zone and of 367 (95% CI: 249–486) per 100 000 much higher in men than in women, and the epidemic
population in the southern zone (10,11). was a progressively ageing one, with the highest burden
found in the oldest age groups. The survey also confirmed
Other key results were: a relatively low burden in the remote, mountainous areas
• the male to female ratio was 5.1 for smear- compared with urban and low-lying rural areas. To
positive TB and 4.5 for bacteriologically address the high TB burden in older people and men,
confirmed TB; active case finding efforts were expanded, with specific
• prevalence per 100 000 population increased attention paid to those groups.
with age, and the absolute number of
bacteriologically TB cases was also relatively Only about one half of the smear-positive TB cases found
large in older age groups (≥35 years); in the survey reported a productive cough of ≥2 weeks
• among bacteriologically confirmed TB cases, duration. Given that detection of TB cases in health
26% were symptom-screen positive, and among facilities used a screening algorithm based on the presence
the smear-positive cases, 53% were symptom-
of a persistent productive cough, a large proportion of
screen positive;
TB cases would not have met the standard screening
• for smear-positive pulmonary TB, the ratio of
prevalence to notifications (P:N ratio) was 2.3, criteria. Furthermore, over a third of the bacteriologically
but varied from 1.3 in those aged 15–34 years to confirmed cases were smear-negative, so that without
2.9 in the 35–44 year age group, and was higher culture (which was not routinely done), many cases
for men than for women (2.7 versus 1.6); could not be confirmed. These findings highlighted
• among bacteriologically confirmed TB cases, important limitations in the TB screening and diagnostic
79% had no previous history of anti-TB algorithms used for routine care (i.e. a presumptive TB
treatment and only 4% were on anti-treatment
case was identified only by symptoms – mainly a cough
at the time of the survey; and
for ≥2 weeks). They also highlighted the need to widen
• of the 196 bacteriologically confirmed and 134
smear-positive TB survey cases that screened the eligibility criteria for smear examination to other TB-
positive for symptoms,2 and were not on anti-TB related symptoms in addition to cough, and to expand
treatment at the time of the survey, 62 (32%) and the use of culture for TB diagnosis. Broader symptom
46 (34%), respectively, had previously sought screening criteria and greater use of chest X-ray were
care in a public or private health facility for their implemented in Viet Nam following the prevalence
symptoms.
survey.
2
Health-care seeking behaviour data were available for survey cases with any
TB symptoms, not just for those with chronic cough.
Photo credit: Nguyen Binh Hoa
VIET NAM 255
References
1. The World Bank (https://data.worldbank.org/country, accessed
April 2017).
2. UNAIDS (http://aidsinfo.unaids.org/, accessed April 2017).
3. World Health Organization. Global Tuberculosis Database. 2017.
(http://www.who.int/tb/country/en/, accessed April 2017).
4. WHO Tuberculosis Programme. (1994). WHO Tuberculosis
Programme: framework for effective tuberculosis
control. World Health Organization. (http://www.who.int/iris/
handle/10665/58717, accessed January 2018).
5. World Health Organization. Global tuberculosis programme.
Global tuberculosis control report 1997. Geneva: WHO; (https://
apps.who.int/iris/bitstream/handle/10665/63354/WHO_
TB_97.225_(part1).pdf?sequence=1, accessed January 2018).
6. Huong NT, Duong BD, Co NV, Quy HT, Tung LB, Bosman
M et al. Establishment and development of the National
Tuberculosis Control Programme in Vietnam. Int J Tuberc
Lung Dis. 2005;9(2):151–156 (https://www.ncbi.nlm.nih.gov/
pubmed/15732733, accessed January 2018).
7. Dye C, Maher D, Weil D, Espinal M, Raviglione M. Targets for
global tuberculosis control. Int J Tuberc Lung Dis. 2006;10(4):460–
462 (https://www.ncbi.nlm.nih.gov/pubmed/16602414, accessed
January 2018).
8. Vree M, Bui DD, Dinh NS, Nguyen VC, Borgdorff MW,
Cobelens FG. Tuberculosis trends, Vietnam. Emerg Infect Dis.
2007;13(5):796–797 (https://www.ncbi.nlm.nih.gov/pmc/articles/
PMC2738473/, accessed January 2018).
9. World Health Organization. Tuberculosis prevalence surveys:
a handbook (WHO/HTM/TB/2010.17). Geneva: WHO; 2011
(https://apps.who.int/iris/bitstream/handle/10665/44481/
9789241548168_eng.pdf, accessed August 2017).
10. Viet Nam National Tuberculosis Programme, national TB
prevalence survey in Vietnam. Ministry of Health, Viet Nam.
11. Hoa NB, Sy DN, Nhung NV, Tiemersma EW, Borgdorff MW,
Cobelens FG. National survey of tuberculosis prevalence in Viet
Nam. Bull World Health Organ. 2010;88(4):273–280 (http://www.
who.int/bulletin/volumes/88/4/09-067801/en/, accessed January
2018).
12. Hoa NB, Cobelens FG, Sy DN, Nhung NV, Borgdorff MW,
Tiemersma EW. Yield of interview screening and chest X-ray
abnormalities in a tuberculosis prevalence survey. Int J Tuberc
Lung Dis. 2012;16(6):762–767 (https://www.ncbi.nlm.nih.gov/
pubmed/22507287, accessed January 2018).
13. Hoa NB, Cobelens FG, Sy DN, Nhung NV, Borgdorff MW,
Tiemersma EW. First national tuberculin survey in Viet Nam:
characteristics and association with tuberculosis prevalence. Int J
Tuberc Lung Dis. 2013;17(6):738–744 (https://www.ncbi.nlm.nih.
gov/pubmed/23676155, accessed January 2018).
14. Hoa NB, Tiemersma EW, Sy DN, Nhung NV, Vree M, Borgdorff
MW et al. Health-seeking behaviour among adults with prolonged
cough in Vietnam. Trop Med Int Health. 2011;16(10):1260–1267
(https://www.ncbi.nlm.nih.gov/pubmed/21692960, accessed
January 2018).
15. van Leth F, Guilatco RS, Hossain S, Van’t Hoog AH, Hoa NB, van
der Werf MJ et al. Measuring socio-economic data in tuberculosis
prevalence surveys. Int J Tuberc Lung Dis. 2011;15 Suppl 2:S58–
63 (https://www.ncbi.nlm.nih.gov/pubmed/21740660, accessed
January 2018).
257
ZAMBIA
2013–2014
Summary statistics
Participation rate 84%
Key people
Name Role Organization
Nathan Kapata Principal investigator National TB and Leprosy Control Programme
Pascalina Chanda Kapata Survey coordinator and co-principal investigator Ministry of Health
William Ngosa Assistant survey coordinator Ministry of Health
Mine Metitiri Assistant survey coordinator Ministry of Health
Lutinala Nalomba Mulenga Chest diseases laboratory team lead Ministry of Health
Mathias Tembo Tropical Diseases Research Centre laboratory team lead Ministry of Health
Patrick Katemangwe University teaching hospital laboratory team lead Ministry of Health
Mazyanga Mazuba Liwewe HIV laboratory team lead Ministry of Health
Veronica Sunkuntu Radiology team lead Ministry of Health
Chris Silavwe Data manager Ministry of Health
Chitani Mbewe Field team leader Ministry of Health
Sam Msariri Field team leader Ministry of Health
Mashina Chomba Field team leader Ministry of Health
Jane Shawa Field team leader Ministry of Health
Eveline Klinkenberg Technical assistance (survey advisor) KNCV Tuberculosis Foundation
Ikushi Onozaki Technical assistance (survey advisor) WHO headquarters
Charalampos Sismanidis Technical assistance (survey advisor) WHO headquarters
Nico Kalisvaart Technical assistance (data management) KNCV Tuberculosis Foundation
Julia Ershova Technical assistance (data management) US Centers for Disease Control and Prevention (CDC)
a
The boundaries and names shown and the designations used on this map do not
imply the expression of any opinion whatsoever on the part of the World Health
Organization concerning the legal status of any country, territory, city or area or of
its authorities, or concerning the delimitation of its frontiers or boundaries.
258 National TB prevalence surveys 2007–2016
Symptom screening
Cough ≥2 weeksa 2 405 (5.2%)
Haemoptysis N/A
Sputum production N/A
Chest pain ≥2 weeksa 3 426 (7.4%)
Fever ≥2 weeksa 1 030 (2.2%)
Total symptom-screen positivea 4 453 (9.7%)
Eligible for sputum examination 6 708 (15%) Symptom positive, chest X-ray positive 1 505 (22%)
Symptom positive, chest X-ray negative or N/A 2 948 (43%)
Symptom negative, chest X-ray positive 2 255 (34%)
Other N/A
Submitted specimens
At least one specimen 6 154 (92%)
Both specimens 4 057 (61%)
Laboratory result
At least one culture result availablec 5 785 (86%)
Total bacteriologically confirmed cases 265 Symptom positive, chest X-ray positive 115 (44%)
Symptom positive, chest X-ray negative or N/A 46 (17%)
Symptom negative, chest X-ray positive 104 (39%)
Other N/A
a
Eligible for sputum collection.
b
Results were not interpretable (19), missing (136), or not available for other non-specified reasons (75). Among 230 participants, 19 who had uninterpretable chest X-ray images were
requested to submit sputum samples.
c
Cultures that were either contaminated and/or missing without a definitive result (i.e. MTB, NTM, negative) were excluded.
d
Definite: MTB confirmed by culture and/or Xpert. Probable: no definition.
260 National TB prevalence surveys 2007–2016
Fig. 1: Participation rate by age and sex Fig. 4: Cluster variation of the number of bacteriologically
confirmed TB casesb
100
12
10
Participation rate (%)
Number of clusters
90
8
6
80
4
70 0
15–24 25–34 35–44 45–54 55–64 ≥65 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19
Age group (years) Number of bacteriologically confirmed TB cases
Male Female
Fig. 2: TB prevalence per 100 000 population by age Fig. 5: Ratio of smear-positive TB prevalence to notifications by
age and by sexc
1400 3.5
Prevalence per 100 000 population
1200 3.0
Prevalence : notification ratio
1000 2.5
800 2.0
600 1.5
400 1.0
200 0.5
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 15–24 25–34 35–44 45–54 55–64 ≥65 Male Female Total
Age group (years) Age group (years) and sex (≥15)
Bacteriologically confirmed TB Smear-positive TB Data source: smear-positive pulmonary TB notified cases from NTP data (2014)
(including cases diagnosed by Xpert MTB/RIF)
Fig. 3: Estimated number of bacteriologically confirmed TB cases Fig. 6: Estimates of TB prevalence (all ages, all forms of TB) before
and prevalence per 100 000 population, by agea (in blue) and after (in red) the national TB prevalence surveyd
16 000 1000
Estimated number of bacteriologically
900
Prevalence per 100 000 population
14 000
800
12 000
700
confirmed TB cases
10 000 600
8 000 500
6 000 400
300
4 000
200
2 000
100
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 200 300 400 500
Age group (years) Prevalence per 100 000 population
a
The estimated number of bacteriologically confirmed TB cases is the product of age-specific prevalence and population estimates from the UN Population Division (2015 revision).
b
The data suggested that the distribution of cases by cluster (blue bars) was significantly different from the theoretical distribution (red line) (mean 4.02, variance 17.8, p<0.05). The
theoretical distribution assumes cases are distributed at random i.e. no clustering effect.
c
Notification rates were estimated using smear-positive pulmonary TB notifications (2014) obtained from the NTP (including TB cases diagnosed by Xpert MTB/RIF), and population
estimates from the UN Population Division (2015 revision).
d
The blue bar denotes the best estimate of prevalence and its range that was indirectly derived from the estimate of incidence previously published by WHO, adjusted to the year of the
prevalence survey based on previously published trends in incidence.
ZAMBIA 261
• the male to female ratio was 2.0 for smear- Table 1: Bacteriologically confirmed TB prevalence by wealth index
positive TB and 1.7 for bacteriologically
Bacteriologically confirmed TB
confirmed TB;
Prevalence per 100 000
95% CI
• prevalence per 100 000 population increased Wealth indexa population
with age, up to the 35–44 years age group, and Rural
was consistently high above 45 years; however, Highest 610 423–797
the absolute number of TB cases was relatively Middle 364 224–505
high in the younger age groups; Lowest 483 294–672
Urban
• of the bacteriologically confirmed TB cases,
Highest 603 386–820
61% were symptom-screen positive, and of
Middle 1251 911–1592
the smear-positive cases, 67% were symptom-
Lowest 1208 750–1666
screen positive;
a
Please refer to the official report for an explanation of how the index was derived.
• for smear-positive pulmonary TB, the ratio of
prevalence to notifications (P:N ratio) was 2.0 Table 2: Pulmonary TB prevalence by HIV status
overall, but varied from 1.6 in those aged 45–54
years to 3.2 in the 65 years and over age group, Prevalence per 100 000
95% CI
and was slightly higher for men than for women HIV status population
that a smear-positive result alone may not be adequate of field operations and dissemination of results and final
for the detection of TB cases, especially in the context of publication was relatively short (14 months).
intensified case finding or active case detection strategies.
References
Major successes, challenges and lessons 1. The World Bank (https://data.worldbank.org/country, accessed
learned April 2017).
2. UNAIDS (http://aidsinfo.unaids.org/, accessed April 2017).
Field operations were implemented within the expected
3. World Health Organization. Global Tuberculosis Database. 2017.
timeframe with minimal interruptions and with a high (http://www.who.int/tb/country/en/, accessed April 2017).
participation rate overall (84%). One of the reasons for 4. The National Tuberculosis and Leprosy Programme, TB manual
this was that the hard-to-reach rural areas were covered (3rd ed). Zambia: Ministry of Health;(http://www.who.int/hiv/
pub/guidelines/zambia_tb.pdf?ua=1, accessed July 2017).
in the early part of the survey, during the drier parts of
5. World Health Organization. Global tuberculosis report
the year. The participation rate was lower (~49%) in the 2013. Geneva: WHO; 2013 (http://apps.who.int/iris/
early stages of the survey (a common finding in surveys); bitstream/10665/91355/1/9789241564656_eng.pdf ?ua=1,
this lower rate was also linked to the long distances to be accessed January 2018).
6. Chanda-Kapata P, Kapata N, Klinkenberg E, Mulenga L, Tembo
travelled in the more remote and sparsely populated parts
M, Katemangwe P et al. Non-tuberculous mycobacteria (NTM)
of the country. The survey teams encountered some myths in Zambia: prevalence, clinical, radiological and microbiological
and misconceptions among community members about characteristics. BMC Infect Dis. 2015;15:500 (https://www.ncbi.
nlm.nih.gov/pubmed/26545357, accessed May 2017).
TB, which had some impact on the overall participation
7. Chanda-Kapata P, Kapata N, Klinkenberg E, William N, Mazyanga
rate. Measures implemented to improve participation L, Musukwa K et al. The adult prevalence of HIV in Zambia:
rates included use of in-cluster community sensitization, results from a population based mobile testing survey conducted
involvement of the local political and traditional in 2013–2014. AIDS Res Ther. 2016;13:4 (https://www.ncbi.nlm.
nih.gov/pubmed/26793264, accessed May 2017).
leadership, and ongoing community education using
8. Kapata N, Chanda-Kapata P, Ngosa W, Metitiri M, Klinkenberg
mainstream television and community radio stations to E, Kalisvaart N et al. The prevalence of tuberculosis in Zambia:
disseminate the objectives and procedures of the survey. Results from the first national TB prevalence survey, 2013–2014.
PLOS ONE. 2016;11(1):e0146392 (https://www.ncbi.nlm.nih.gov/
The 7-day period used for cluster operations was pubmed/26771588, accessed May 2017).
manageable, but sometimes required field staff to work 9. National tuberculosis prevalence survey 2013–2014 technical
report. Zambia: Ministry of Health, Government of the Republic
long hours, depending on the flow of participants. For of Zambia; 2015.
example, in rural areas, participants tended to report to 10. World Health Organization. Tuberculosis prevalence surveys:
the cluster site later in the day, meaning that the teams a handbook (WHO/HTM/TB/2010.17). Geneva: WHO; 2011
(https://apps.who.int/iris/bitstream/handle/10665/44481/
had to work late into the night to clear the queue of
9789241548168_eng.pdf, accessed August 2017).
participants, which in turn meant that transport had to 11. World Health Organization. The End TB Strategy. Geneva, WHO;
be provided to those coming from locations far from the 2014 (http://www.who.int/tb/strategy/en/, accessed July 2017).
main survey camp site. This was a valuable lesson for
future surveys, because without providing such support
the participation rate might have been lower.
ZIMBABWE
2014
Summary statistics
Participation rate 78%
Key people
Name Role Organization
Charles Sandy Principal investigator National Tuberculosis Control Programme (NTP)
Junior Mutsvangwa Co-principal investigator Biomedical Research and Training Institute
Ronnie Matambo Survey coordinator Biomedical Research and Training Institute
Dumisani Ndlovu Radiology coordinator Biomedical Research and Training Institute
Ellen Munemo Laboratory manager National Microbiology Reference Laboratory
Eve Marima Data manager The Zimbabwe National Statistics Agency (ZIMSTAT)
Hebert Mutunzi Technical working group member, laboratory NTP
Mkhokeli Ngwenya Technical working group member, survey design NTP
Joconiah Chirenda Technical working group member, survey design University of Zimbabwe, College of Health Sciences
Nicholas Siziba Technical working group member, M&E NTP
Peter Shiri Technical working group member, M&E NTP
Martin Mapfurira NTP officer NTP
Patrick Hazangwe Technical assistance WHO Zimbabwe
Wilfred Nkhoma Technical assistance (survey advisor) WHO Regional Office for Africa (AFRO)
Ikushi Onozaki Technical assistance (survey advisor) WHO headquarters
Marina Tadolini Technical assistance (survey advisor) Consultant, Italy
Fasil Tsegaye Technical assistance (survey advisor) International Union Against Tuberculosis and Lung Disease
Kunihiko Ito Technical assistance (radiology) Research Institute of Tuberculosis/Japan Anti-Tuberculosis Association (RIT/JATA)
Mourad Gumusboga Technical assistance (laboratory advisor) Supranational Reference Laboratory, Antwerp Belgium
Hazim Timimi Technical assistance (data management) WHO headquarters
Norio Yamada Technical assistance (analysis) RIT/JATA
Kosuke Okada Technical assistance (reporting) RIT/JATA
Symptom screening
Cough of any durationa 1 415 (4.2%)
Haemoptysisa 310 (0.9%)
Sputum production N/A
Chest pain N/A
Fever 283 (0.8%)
Night sweatsa 560 (1.7%)
Total symptom-screen positivea 1 833 (5.4%)
Eligible for sputum examination 5 820 (17%) Symptom positive, chest X-ray positive 628 (11%)
Symptom positive, chest X-ray negative or N/A 1 205 (21%)
Symptom negative, chest X-ray positive 2 803 (48%)
Otherc 1 184 (20%)
Submitted specimens
At least one specimen 5 705 (98%)
Both specimens 5 441 (94%)
Laboratory result
At least one culture result availabled 5 680 (98%)
Total bacteriologically confirmed cases 107 Symptom positive, chest X-ray positive 29 (27%)
Symptom positive, chest X-ray negative or N/A 10 (9.4%)
Symptom negative, chest X-ray positive 64 (60%)
Otherc 4 (3.7%)
a
Eligible for sputum collection.
b
Chest X-ray taken but results were missing.
c
Chest X-ray exempted and symptom-screen negative.
d
Cultures that were either contaminated and/or missing without a definitive result (i.e. MTB, NTM, negative) were excluded.
e
Definite: MTB confirmed by culture and/or Xpert. Probable: no definition.
268 National TB prevalence surveys 2007–2016
Fig. 1: Participation rate by age and sex Fig. 4: Cluster variation of the number of bacteriologically
confirmed TB casesb
100 25
90 20
Participation rate (%)
Number of clusters
15
80
10
70
5
60 0
15–24 25–34 35–44 45–54 55–64 ≥65 0 1 2 3 4 5 6
Age group (years) Number of bacteriologically confirmed TB cases
Male Female
Fig. 2: TB prevalence per 100 000 population by age Fig. 5: Ratio of bacteriologically confirmed TB prevalence to
notifications by age and by sexc
1000 6.0
Prevalence per 100 000 population
700
4.0
600
500 3.0
400
2.0
300
200
1.0
100
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 15–24 25–34 35–44 45–54 55–64 ≥65 Male Female Total
Age group (years) Age group (years) and sex (≥15)
Bacteriologically confirmed TB Smear-positive TB
Fig. 3: Estimated number of bacteriologically confirmed TB cases Fig. 6: Estimates of TB prevalence (all ages, all forms of TB) before
and prevalence per 100 000 population, by agea (in blue) and after (in red) the national TB prevalence surveyd
12 000 600
Estimated number of bacteriologically
10 000 500
confirmed TB cases
8 000 400
6 000 300
4 000 200
2 000 100
0 0
15–24 25–34 35–44 45–54 55–64 ≥65 200 300 400 500 600
Age group (years) Prevalence per 100 000 population
a
The estimated number of bacteriologically confirmed TB cases is the product of age-specific prevalence and population estimates from the UN Population Division (2015 revision).
b
The data did not suggest that the distribution of cases by cluster (blue bars) was significantly different from the theoretical distribution (red line) (mean 1.43, variance 1.90, p=0.06).
The theoretical distribution assumes cases are distributed at random i.e. no clustering effect.
c
Notification rates were estimated using bacteriologically confirmed pulmonary TB notifications (2014) obtained from the NTP, and population estimates from the UN Population Division
(2015 revision).
d
The blue bar denotes the best estimate of prevalence and its range that was indirectly derived from the estimate of incidence previously published by WHO, adjusted to the year of the
prevalence survey based on previously published trends in incidence.
ZIMBABWE 269
The number of smear-negative culture-positive TB cases • retrieval of X-ray images was sometimes
(84 cases) was almost four times the number of smear- problematic because the archiving and
positive culture-positive cases (23 cases). The former communication system was controlled by
the X-ray unit supplier in the Netherlands;
group cannot be definitively diagnosed under normal there was also a backlog in central reading of
programmatic conditions if routine diagnostic services X-rays due to the limited access to the internet;
rely on smear microscopy alone. Among the smear- these challenges were resolved through in-
positive participants, “smear-positive” but “culture/Xpert- country technical assistance provided by the
negative/non-TB” accounted for 89% (183/206). This Research Institute of Tuberculosis/Japan Anti-
Tuberculosis Association;
finding highlighted major concerns about the positive
predictive value of smear examination in the context of • delays in the communication of laboratory
results and follow-up of confirmed TB cases
routine health services. The survey thus demonstrated resulted in delayed case management and loss to
that the diagnostic services available at the time of the follow-up; as a result, not all confirmed TB cases
survey (which depended mostly on smear microscopy) were tested for HIV as planned; and
needed to be thoroughly reviewed. For example, there • the lack of clarity of defined roles,
was a need to assess the role of chest X-ray for individuals responsibilities and deliverables during survey
with severe or chronic respiratory symptoms (or both), preparations among the four key partners
and to expand referral services, so that presumptive TB – the survey team, the laboratory, the NTP
and the Zimbabwe National Statistics Agency
cases with negative smears could access care at facilities (ZIMSTAT); survey implementation and data
equipped with chest X-ray, culture or Xpert MTB/RIF. management were done by the Biomedical
Research Institute and ZIMSTAT, respectively;
however, the delayed sharing of datasets and
different data management processes between
Major successes, challenges and lessons the two agencies made survey management a
learned challenge; other data management issues related
to excessive delays caused by double data entry,
The survey was successfully implemented within one and the lack of a barcoding system during field
calendar year, and preliminary results were available data collection.
within six months of completing field operations.
Although the survey team in Zimbabwe did not
participate in preparatory workshops organized by
WHO for global focus countries, two visits to prevalence
surveys in Malawi and Rwanda, and technical assistance
from the Ethiopian deputy survey coordinator, greatly
assisted the team’s understanding of how to organize and
undertake a survey. This external technical support was
vital in ensuring a good-quality survey.
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