Received: 5 May 2021 | Revised: 12 July 2021 | Accepted: 10 August 2021

DOI: 10.1002/ijgo.13879

FIGO CANCER REPORT 2021

Worldwide initiatives to eliminate cervical cancer

Sarikapan Wilailak1 | Malika Kengsakul2 | Sean Kehoe3,4

1
Department of Obstetrics and
Gynecology, Faculty of Medicine Abstract
Ramathibodi Hospital, Mahidol University,
In 2020, more than 600 000 women were diagnosed with cervical cancer and 342 000
Bangkok, Thailand
2
Department of Obstetrics and
women died worldwide. Without comprehensive control, rates of cervical cancer inci-
Gynecology, Panyananthaphikkhu dence and mortality are expected to worsen. In 2020, the World Health Organization
Chonprathan Medical Center,
Srinakharinwirot University, Nonthaburi,
adopted the global strategy to eliminate cervical cancer to the threshold of four cases
Thailand per 100 000 women within the 21st century, using a triple pillar intervention strat-
3
Oxford Gynecological Cancer Center, egy comprising 90% of girls fully vaccinated by the age of 15 years, 70% of women
Churchill Hospital, Oxford, UK
4 screened by the age of 35 years and again by 45 years, and 90% of women with pre-
St Peter's College, Oxford, UK
cancer treated and 90% of women with invasive cancer managed. In countries with
Correspondence
high cervical cancer incidence, a tremendous effort will be needed to overcome the
Sarikapan Wilailak, Division of
Gynecologic Oncology, Department of challenges. This article discusses the efforts in place to accelerate achievement of this
Obstetrics and Gynecology, Ramathibodi
ambitious goal.
Hospital, Mahidol University, 270 Rama
VI Road Ratchathewi, Bangkok 10400,
Thailand. KEYWORDS
Email: sarikapanw@gmail.com cervical cancer, elimination initiatives, FIGO Cancer Report, prevention, screening, treatment

the leading cause of death in Sub-­Saharan Africa, Melanesia, South

1 | E PI D E M I O LO G Y O F C E RV I C A L America, and Southeast Asia. 2 In addition, an increasing incidence
C A N C E R WO R LDW I D E rate was reported in many areas across Africa (Eastern, Southern,
and Middle Africa), with the highest incidence in Eswatini. 2 In a pop-
Cervical cancer is the fourth most diagnosed cancer and the fourth ulous country such as India, approximately 100 000 new cases are
leading cause of cancer death in women worldwide. In 2020, diagnosed and 60 000 women die from cervical cancer annually, ac-
GLOBOCAN estimated that 604 000 women were diagnosed with counting for nearly one-­third of all cervical cancer deaths globally.3
1
cervical cancer and 342 000 women died from the disease. Over the
past decades, incidence and mortality rates of cervical cancer have
declined in most regions of the world. However, large geographic 2 | C E RV I C A L C A N C E R R I S K FAC TO R S
variation in morbidity and mortality rates are observed. Globally,
the estimated age-­standardized incidence rate of cervical cancer The two major histologic types of cervical cancer are squamous cell
was 13.1 per 100 000 women and varied among countries (from less carcinoma and adenocarcinoma. Several studies have demonstrated
than 2 to 75 per 100 000 women). 2 Despite the primary prevention that these histologies share common risk factors.4–­6 The funda-
of novel vaccination and secondary prevention of cancer screen- mental risk factor for developing cervical cancer is persistent on-
ing, cervical cancer remains the most common female cancer and cogenic HPV infection, with approximately 99.7% of cervical cancer

FIGO CANCER REPORT 2021

This is an open access article under the terms of the Creative Commons Attribution-­NonCommercial-­NoDerivs License, which permits use and distribution in
any medium, provided the original work is properly cited, the use is non-­commercial and no modifications or adaptations are made.
© 2021 The Authors. International Journal of Gynecology & Obstetrics published by John Wiley & Sons Ltd on behalf of International Federation of Gynecology
and Obstetrics

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wileyonlinelibrary.com/journal/ijgo Int J Gynecol Obstet. 2021;155(Suppl. 1):102–106.
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WILAILAK et al. 103

tumors associated with oncogenic HPV infection. HPV 16 and HPV Knaul et al.17 described similar characteristics between cervical
18 account for two-­thirds of cervical carcinoma in all continents.5 cancer and neglected tropical diseases in that: (1) they commonly
Additional oncogenic HPV genotypes are 31, 33, 35, 45, 52, 58, and affect poor people; (2) the population at risk is overlooked by policy
59, which lead to cancer at several sites, such as the cervix, vulvar, makers; (3) they are associated with stigma and discrimination; (4)
vagina, and anus.5 they impact female morbidity and mortality; (5) they are neglected in
HPV transmits primarily through sexual contact and most peo- clinical research; and (6) they can be controlled and prevented. The
ple are infected shortly after the onset of sexual activity.7 HPV authors state that “cervical cancer is not a disease of the past, it is a
infection can be transmitted not only by penetrative sexual inter- disease of the poor”.17
7
course but also skin-­to-­skin genital contact. In general, early HPV If left uncontrolled, cervical cancer rates are expected to worsen.
infection can cause clinically detectable low-­grade cervical cell ab- The estimated annual number of cervical cancer cases is expected to
normalities. However, these usually spontaneously resolve within increase from 570 000 to 700 000 between 2018 and 2030, while
12–­24 months.5 When infection with oncogenic HPV genotypes is the annual number of deaths is projected to rise from 311 000 to
persistent, the risk of developing high-­grade cervical cell abnormal- 400 000 and the vast majority of women in LMICs will suffer with-
ities increases and can proceed to cancer within 10–­15 years if left out the ability to seek a healthcare provider.12 This inequality is no
5,8
untreated. Additional cofactors for cervical cancer are early onset longer acceptable in our globalized era, and it must be promptly
of sexual activity, multiple sexual partners, high-­risk sexual partner, regulated.
history of sexually transmitted infections, history of vulval or vagi- In May 2018, World Health Organization (WHO) Director-­
nal precancerous and cancerous lesions, smoking, oral contraceptive General, Dr Tedros Adhanom Ghebreyesus, brought cervical can-
pills, and immunocompromise.9,10 cer back to global attention when he called for the elimination of
Scientists and researchers have developed novel tools for both cervical cancer to the threshold of four cases per 100 000 women.
prevention and treatment of cervical cancer. Furthermore, high-­ In 2020, WHO adopted a global strategy for eliminating cervical
grade precancerous and early-­stage cervical cancer can be treated cancer through a triple pillar intervention strategy: 90% of girls fully
effectively.8 Consequently, cervical cancer should be considered the vaccinated by the age of 15 years, 70% of women screened by the
most preventable cancer in our lifetime. age of 35 years and again by 45 years, and 90% of women with pre-
cancer treated and 90% of women with invasive cancer managed.18
Comprehensive cooperation between organizations and health pol-
3 | O B S TAC LE S TO C E RV I C A L C A N C E R icy makers is crucial, especially in countries with a high incidence of
SCREENING cervical cancer.

Cervical cancer screening based on Pap smear or conventional cytol-

ogy was introduced in the 1940s by Dr George Papanicolaou. Fifty 4 | S TR ATEG Y TO S C A LE U P COV E R AG E
years later, this screening test had been widely implemented in na- O F H P V VACC I N ATI O N
tional cervical cancer screening programs and was developed into
liquid-­based cytology in the early 2000s.11 Although it has similar Primary prevention via HPV vaccination is one of the major chal-
sensitivity to conventional cytology, liquid-­based cytology reduces lenges for low HDI countries. In fact, less than 30% of LMICs have
the rate of inadequate samples, increases screening capacity by par- implemented national HPV vaccination programs, while this has
tially automated analysis, and offers HPV testing.11 been accomplished in over 80% of high-­income countries.12
A significant reduction in the incidence of cervical cancer has Three HPV vaccines are currently prequalified by WHO: a biva-
been reported in many countries, mainly in high-­income nations, lent vaccine targeting HPV 16 and HPV 18; a quadrivalent vaccine
for example the UK, USA, and European countries.11 Differences targeting HPV types 6, 11, 16, and 18; and a nonavalent vaccine tar-
in incidence and mortality rates reflect disparities in access to geting HPV types 31, 33, 45, 52, and 58, in addition to HPV 6, 11, 16,
12,13
screening and treatment across and within countries ; for ex- and 18. In 2009, WHO recommended implementation of HPV vacci-
ample, the Human Development Index (HDI) and poverty rates nation into national immunization programs. WHO also recommends
accounted for over 50% of the global difference in mortality.13 two vaccine doses for girls aged 9–­14 years, as this is the most cost-­
The failure of cervical cancer screening in low HDI countries is effective public health strategy against cervical cancer.19 However,
mainly the result of unorganized public health policy and lack of obstacles to achieving this are evident: (1) lack of an existing service
resources, infrastructure, and community awareness14; in contrast, platform to deliver the vaccine in this age group in some countries;
in high HDI countries, failure results from nonparticipation, under-­ (2) strong social communication and movement are required to en-
screening, and loss to follow-­up of abnormal results.15,16 Recent sure acceptance and compliance with a two-­dose schedule (a survey
data demonstrated that only 44% of women in low-­and middle-­ in India by Hull et al. 20 reported that only 40% of parents accepted
income countries (LMICs) have ever been screened for cervical HPV vaccination prior to health counselling, with safety of the vac-
cancer and the lowest screening rate (16.9%) was reported among cine followed by the perception that it could be seen as permission
women in Sub-­S aharan Africa.16 to engage in sexual activity given as the most common concerns);
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104 WILAILAK et al.

and (3) HPV vaccines and their operational costs are relatively ex- and older who have never been exposed to HPV, are recommended
pensive. However, successful models in different countries are con- to have three vaccination doses for cervical cancer prevention. 26
tinuously being reported. Although HPV vaccination of the target population plays a lead-
Following approval by the European Medicines Agency in 2006, ing role in primary prevention, other supporting interventions are
bivalent and quadrivalent vaccines are now widely used in European also crucial to maximize efficacy. It is important to implement healthy
countries. In 2007, Switzerland implemented HPV vaccines into the sex education programs for boys and girls to raise their awareness
national vaccination program, beginning in the canton of Geneva. of sexually transmitted infections by encouraging delay in sexual
The program used school services, a public hospital, and private initiation, reducing high-­risk sexual behaviors, promoting condom
physicians as vaccination providers. Four years later, HPV vaccina- use, smoking cessation, and male circumcision in countries where
tion coverage was 72.6% and 74.8% in targeted cohorts for three it is relevant. However, these interventions should be adapted, as
and two doses, respectively. The authors suggested that the high appropriate, depending on age and culture. 27
coverage of this vaccination program in Geneva was likely related
to free vaccination and easy access to the vaccine. The combina-
tion of delivery services including schools, health services, a public 5 | PA R A D I G M S H I F T S I N C E RV I C A L
hospital, and private physicians enabled coverage of most eligible CANCER SCREENING
11–­19-­year-­old girls. 21
In 2007, Thailand recommended HPV vaccination for girls and Secondary prevention including a high coverage screening program,
women who could afford to pay for the vaccine. After 10 years of health promotion, and early precancerous treatment are essential
tremendous effort, in 2017 Thailand had successfully implemented actions to inhibit the development of cervical cancer, especially in
HPV vaccines into its national immunization program. Two free unvaccinated women and women infected with subtypes other than
doses of HPV vaccine are delivered through a school-­based service HPV 16 and HPV 18. In general, high sensitivity screening tools are the
for girls aged 11–­12 years nationwide. After 3 years of implementa- key element of effective screening.28 However, cytology-­based test-
22
tion, coverage had reached 95% of the target population. ing has been the gold standard for cervical cancer screening for over
HPV vaccination is currently the cornerstone of long-­term cer- 50 years, primarily due to its high specificity. Nevertheless, several
vical cancer control. Numerous studies have confirmed the safety, limitations have been reported, including low sensitivity, poor repro-
20,23,24
efficacy, and cost-­effectiveness of these vaccines and the ducibility, and imperfect fixation. Moreover, it requires well-­trained
number of cervical cancer cases is predicted to decrease after five personnel and expensive infrastructure that are the fundamental ob-
decades of comprehensive vaccination. 20 However, considerable fi- stacles in low-­resource settings. Despite alternative methods such as
nancial support is vital to overcome the many barriers. Fortunately, liquid-­based cytology and visual inspection using acetic acid (VIA) or
Gavi, the vaccine alliance, has been supporting pilot projects of HPV Lugol iodine, their sensitivities remain suboptimal.29,30
vaccines in many LMICs, mainly in Sub-­Saharan Africa, since 2013, Cumulative evidence supports primary HPV-­based testing as the
and by 2020 more than 30 million girls had been vaccinated in over most favorable candidate for cervical cancer screening. High-­risk
40 countries with the organization's support. 25 Although introduc- HPV-­based testing has higher sensitivity to detect high-­grade cer-
tion of HPV vaccination is challenging, it also provides many oppor- vical abnormality and cancer, and a higher negative predictive value
tunities to strengthen adolescent health through implementation of compared with cytology-­based testing. 28,29,31 Consequently, in set-
other vaccinations (such as hepatitis B, tetanus), reproductive health tings where screening intervals are long or disorganized, screening
education, HIV prevention, and nutritional support programs. with HPV-­based testing may be a reasonable alternative to cytology-­
HPV vaccination can be successfully implemented in national im- based screening.30
munization programs in different settings. Encouragingly, the num- In addition, HPV-­
based testing can be performed using self-­
ber of LMICs with national HPV vaccination programs is gradually collection, which has the potential to overcome the barriers encoun-
increasing. tered with clinician-­based screening methods.32 Several studies on
Furthermore, a strategy to scale up vaccination coverage using a HPV self-­collection testing have shown increased screening cover-
single-­dose vaccination schedule is being studied. This strategy aims age in remote areas or those with high levels of nonattendance. 28,32
to address concerns over vaccine shortages and enhance the poten- However, HPV self-­collection should be implemented with care-
tial induction of vaccination to limited-­resource settings. However, ful consideration based on local context and with continuous
evidence for the effectiveness of a single-­dose vaccination program evaluation. 28
24
remains unclear. Currently, comprehensive cooperation between In 2020, the American Cancer Society recommended cervi-
researchers, partner organizations, countries, and vaccine manufac- cal cancer screening with HPV test alone every 5 years for every
tures is essential to equally distribute two-­dose HPV vaccine sched- woman with a cervix from the age of 25–­65 years. Alternative meth-
ules to the target populations in neglected areas and to prevent ods are co-­testing using HPV and cytology testing every 5 years or
shortages of vaccines in the future. cytology testing every 3 years. In general, when an abnormal screen-
It is important to note that women who are outside the WHO ing result is found, the patient will be referred for colposcopy and
recommended vaccination group, such as women aged 16–­26 years tissue biopsy for histological confirmation, with treatment given for
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WILAILAK et al. 105

patients with high-­grade cervical intraepithelial neoplasia (CIN 2 or costs are included in a country's budget and health services such as
33
higher). These multiple evaluation steps require skilled personnel universal coverage are affordable for everyone.37
and resources, which are limited in low-­resource countries. Instead, Provision of personal education on cervical cancer screening and
WHO has recommended a screen-­and-­treat method over the stan- treatment is an important factor to catalyze the public health sys-
dard process, especially in countries with geographic barriers and tem. A systematic review showed that the implementation of multi-
34
limited resources. This strategy aims to ensure that treatment is faceted roles of health providers was associated with improvement
provided soon or ideally immediately after a positive screening re- of cervical cancer control.38 Community health leaders work closely
sult. The difference between these protocols is that the treatment with the community to raise health awareness and encourage social
decision for the standard protocol is based on histology, while for movement and acceptance of cancer prevention strategies. Primary
the screen-­and-­treat method it is based on screening result. WHO care providers are trained personnel who perform the screening
expert panels also recommend an HPV test-­
and-­
treat approach test, follow-­up, counselling, and refer patients to higher facilities for
over VIA and treat.35 Nevertheless, if HPV testing is not available, diagnosis and treatment. Secondary care (district) providers are doc-
VIA and treat is suggested. However, in countries with an exist- tors and teams who perform all diagnostic and treatment services
ing appropriate screening strategy, either an HPV test or cytology and refer patients to both higher and lower levels of care. Finally,
test followed by colposcopy could be used. Regardless of screen- tertiary care providers are doctors and teams who manage patients
ing method, all women with a positive result should be evaluated with invasive and advanced disease and refer them back to primary
with VIA to assess the size of the lesion and to rule out gross malig- or secondary care facilities as appropriate.37
nancy. Cryotherapy is the most preferable treatment in the protocol. Australia is one of the world leaders in cervical cancer preven-
However, if the patient is not eligible for ablative treatment in the tion; it was the first country to implement the HPV vaccine into
case of a large lesion, large loop excision of the transformation zone national immunization programs and one of the earliest to change
(LLETZ) is recommended. Women who test negative on VIA or cy- national screening programs to HPV-­based testing. It is estimated
tology are recommended to repeat screening at 3–­5 years, whereas that Australia will eliminate cervical cancer by 2035.39 Australia
a minimum screening interval of 5 years is recommended for women and other countries with successful strategies are working closely
with a negative HPV test result. Women who undergo treatment together with partnership countries by sharing knowledge, experi-
should receive post-­treatment follow up at 1 year.35 ences, resources, and innovative low-­cost technology to accelerate
Of note, in areas of high endemic HIV infection, women should the elimination of cervical cancer globally.39
receive counselling for HIV testing. Women living with HIV are at In summary, elimination of cervical cancer is an ambitious global
higher risk of persistent HPV infection. Cervical cancer screening movement that will improve women's rights. It is time for compre-
is recommended as soon as they become sexually active, regardless hensive cooperation between countries, partnership, and external
of age. Women in endemic areas commonly develop precancerous multinational agencies to overcome the inequities. The triple pillar
lesions at a young age and progress to cancerous lesions in a short intervention strategy covers vaccination, screening, and treatment
period of time. As a result, they are advised to follow a 3-­yearly and its implementation will not only save lives and enhance quality
screening schedule.36 of life for millions of women, but also provide a great opportunity
for countries to build strong and sustainable healthcare systems.
Although it will take an enormous effort to overcome the barriers,
6 | TE RTI A RY PR E V E NTI O N : TR E ATM E NT we believe that every nation will soon reach this goal within the life-
O F I N VA S I V E C E RV I C A L C A N C E R time of today's youngest girls.

Cervical cancer is preventable and curable. However, the cure rate AU T H O R C O N T R I B U T I O N S

depends on the stage at diagnosis and efficiency of treatment. The All authors contributed to concept, research, manuscript writing,
goal of tertiary prevention is to improve the patient's quality of life review, and revision. All authors approved the final version of the
and reduce disability through effective treatment and rehabilitation. manuscript.
Multidisciplinary teams are encouraged to work together to analyze
and prepare fundamental health factors such as infrastructure, fi- C O N FL I C T S O F I N T E R E S T
nancial resources, and human resources. Recommended factors for The authors have no conflicts of interest.
effective tertiary prevention are: (1) provision of a practical referral
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