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Vaccine 37 (2019) 1601–1607

Contents lists available at ScienceDirect

Vaccine
journal homepage: www.elsevier.com/locate/vaccine

Seasonal influenza vaccination policies in the Eastern Mediterranean


Region: Current status and the way forward
Abdinasir Abubakar a, Nada Melhem b,c, Mamunur Malik a, Ghassan Dbaibo c,e, Wasiq Mehmood Khan a,
Hassan Zaraket c,d,⇑
a
Infectious Hazard Management, Department of WHO Health Emergencies Programme, WHO Regional Office for the Eastern Mediterranean, Cairo, Egypt
b
American University of Beirut, Faculty of Health Sciences, Medical Laboratory Sciences Program, 11-0236 Riad El Solh, 1107-2020 Beirut, Lebanon
c
American University of Beirut, Faculty of Medicine, Center for Infectious Diseases Research, 11-0236 Riad El Solh, 1107-2020 Beirut, Lebanon
d
American University of Beirut, Faculty of Medicine, Department of Experimental Pathology, Immunology & Microbiology, 11-0236 Riad El Solh, 1107-2020 Beirut, Lebanon
e
American University of Beirut, Faculty of Medicine, Department of Pediatrics and Adolescent Medicine, Division of Pediatric Infectious Diseases, 11-0236 Riad El Solh,
1107-2020 Beirut, Lebanon

a r t i c l e i n f o a b s t r a c t

Article history: Background: The World Health Organization recommends annual influenza vaccination, especially in
Received 30 July 2018 high-risk groups. Little is known about the adoption and implementation of influenza vaccination policies
Received in revised form 21 January 2019 in the Eastern Mediterranean Region.
Accepted 1 February 2019
Methods: A survey was distributed to country representatives at the ministries of health of the 22 coun-
Available online 19 February 2019
tries of the Region between December 2016 and February 2017 to capture data on influenza immuniza-
tion policies, recommendations, and practices in place.
Keywords:
Results: Of the 20 countries that responded to the survey, 14 reported having influenza immunization
Influenza (human)
Vaccination
policies during the 2015/2016 influenza season. All countries with an influenza immunization policy rec-
Surveys and questionnaires ommended vaccination for people with chronic medical conditions, healthcare workers and pilgrims.
Policy Two of the 20 countries did not target pregnant women. Eight countries used the northern hemisphere
Eastern Mediterranean Region formulation, one used the southern hemisphere formulation and nine used both. Vaccination coverage
was not monitored by all countries and for all target groups. Where reported, coverage of a number of
target groups (healthcare workers, children) was generally low. Data on the burden of influenza and vac-
cine protection are scarce in the Region.
Conclusions: Despite widespread policy recommendations on influenza vaccination, attaining high cover-
age rates remains a challenge in the Eastern Mediterranean Region. Tackling disparities in influenza vac-
cine accessibility and strengthening surveillance systems may increase influenza vaccine introduction
and use.
Ó 2019 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction Annual vaccination is the cornerstone for preventing infection,


severe disease, and mortality from influenza [5]. Vaccination
Seasonal influenza is an acute viral infection that affects people against influenza is particularly important for individuals at high
of all age groups worldwide. According to World Health Organiza- risk of disease complications and for those caring for them. WHO
tion (WHO) estimates, influenza viruses infect between 5% and 15% recommends annual influenza vaccination for pregnant women
of the global population, causing an estimated 3–5 million severe at any stage of pregnancy, children aged between 6 months and
cases and up to 650,000 respiratory deaths a year [1,2]. Annual sea- 5 years, elderly individuals (>65 years), individuals with chronic
sonal epidemics have also been associated with substantial health- medical conditions and healthcare workers [1,6]. In countries
care costs and productivity losses [3,4]. where influenza vaccination programmes are still in their early
stages or not well developed, WHO recommends prioritizing vacci-
nation for pregnant women, whereas other risk groups are not
⇑ Corresponding author at: American University of Beirut, Faculty of Medicine,
ranked by priority [6]. On the other hand, the United States Centers
Center for Infectious Diseases Research, 11-0236 Riad El Solh, 1107-2020 Beirut,
for Disease Control and Prevention (CDC) has taken a more univer-
Lebanon. sal approach, recommending the use of annual influenza vaccine
E-mail address: hz34@aub.edu.lb (H. Zaraket). for all persons aged 6 months [7]. However, during a vaccine

https://doi.org/10.1016/j.vaccine.2019.02.001
0264-410X/Ó 2019 The Authors. Published by Elsevier Ltd.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
1602 A. Abubakar et al. / Vaccine 37 (2019) 1601–1607

shortage, the CDC recommends that vaccination efforts be focused While mortality surveillance data for influenza were reportedly
on high-risk groups only with no order by priority [7]. collected by 16 countries (Afghanistan, Egypt, Iran, Iraq, Jordan,
The WHO Eastern Mediterranean Region, which consists of 22 Kuwait, Libya, Morocco, Oman, Palestine, Saudi Arabia, Sudan, Syr-
countries (Afghanistan, Bahrain, Djibouti, Egypt, Iran, Iraq, Jordan, ia, Tunisia, UAE, and Yemen), only 10 provided mortality data
Kuwait, Lebanon, Libya, Morocco, Oman, Pakistan, Palestine, Qatar, (Egypt, Iran, Iraq, Jordan, Kuwait, Morocco, Oman, Syria, Tunisia,
Saudi Arabia, Somalia, Sudan, Syria, Tunisia, United Arab Emirates and Yemen). Mortality among reported influenza cases ranged
(UAE) and Yemen) is home to nearly 10% of the world’s population. from 0% in Jordan to 15% in Morocco during the 2015/2016 season.
However, as of 2014, the Region’s share of influenza vaccines is Fifteen countries also reported collecting data on influenza-
roughly 2.2% of the globally distributed doses [8]. The Region lies associated hospitalizations (Afghanistan, Egypt, Iran, Iraq, Jordan,
on a number of migratory bird flyways and is thus at risk of the Kuwait, Morocco, Oman, Pakistan, Palestine, Saudi Arabia, Syria,
emergence of new influenza viruses [9]. We undertook a survey Tunisia, UAE, and Yemen), yet only nine provided data on hospital-
to assess the adoption and implementation of influenza vaccina- ization rates (Egypt, Iran, Iraq, Jordan, Morocco, Oman, Syria, Tuni-
tion policies in the Region to provide the data needed for evaluat- sia, and Yemen). The frequency of hospitalization among reported
ing and developing guidelines for influenza prevention with the influenza cases ranged from 0.004% in Iran to 21.7% in Iraq.
goal of increasing vaccination coverage.

3.4. Influenza vaccine recommendations


2. Materials and methods
Children. Of the countries with an influenza vaccination policy
The survey consisted of a 38-item questionnaire that was devel-
during the 2015/2016 season, two countries (2/14), Libya and
oped based on available relevant literature on influenza vaccina-
Qatar, included seasonal influenza vaccine in the childhood immu-
tion. The self-administered survey was distributed by email to
nization schedule. Qatar targeted children <5 years of age. No
influenza focal points at the ministries of health (MOHs) of all
specific age group was given by Libya.
countries of the Region between December 2016 and February
Adults. Four countries (4/14) had influenza vaccination recom-
2017. The survey included questions on mechanisms in place to
mendations for adults during the 2015/2016 season: Oman, Qatar,
monitor influenza vaccination coverage; vaccination coverage;
Syria, and UAE. Oman and Qatar provided information on the age
the existence of an official influenza vaccination policy (adopted
groups targeted, indicating that influenza vaccination was recom-
by MOH), the national recommendations for influenza vaccination;
mended for persons >60 years of age.
and planned policies with regard to the national influenza immu-
People with chronic illnesses. All countries with recommenda-
nization programme. Groups which were defined as risk or target
tions for influenza vaccination recommended the influenza vaccine
groups were defined in the survey. However, the age groups for
for people with chronic illnesses (e.g. diabetes, asthma, renal dis-
whom vaccine is recommended were not defined in the survey
ease) (Table 1). All but two countries, Jordan and Lebanon, recom-
but rather asked in an open-ended question as these might vary
mended influenza vaccination for persons with immunological
from country to another.
disorders and/or HIV/AIDS. Ten countries recommended vaccina-
tion for individuals with morbid obesity, and nine recommended
3. Results vaccination for those with spinal cord injuries and disorders that
can result in pulmonary impairment and complications from respi-
3.1. Response rate ratory illness. However, only five countries recommended vaccina-
tion for individuals on long-term aspirin use.
In total, 20 countries from the Region completed the question- Pregnant women. Annual vaccination of pregnant women was
naire, a response rate of 90.9%. Responses were not received from recommended by all countries that had an influenza vaccination
Bahrain and Djibouti. policy, except Egypt and Lebanon, which had no specific recom-
mendations for this group (Table 2). Only Iraq, Kuwait, and Libya
recommended maternal influenza vaccination during the early
3.2. Seasonal influenza vaccination policies
postpartum period.
Healthcare workers. All countries with an influenza vaccina-
Of the 20 countries for which the data were available, 14
tion policy had recommendations for vaccination of hospital health
reported having seasonal influenza vaccination policies at the time
care workers against influenza during the 2015/2016 season
surveyed (Egypt, Iran, Iraq, Jordan, Kuwait, Lebanon, Libya, Oman,
(Table 3). All but two (Lebanon and Syria) also recommended influ-
Palestine, Qatar, Saudi Arabia, Syria, Tunisia, and UAE). Of these
enza vaccination for laboratory health care workers. Furthermore,
14, five (Iran, Libya, Qatar, Syria, and Tunisia) reported including
11/14 countries recommended seasonal influenza vaccination for
the influenza vaccine in their national immunization programme
health care workers at long-term care facilities and 10/14 recom-
(NIP). However, no details were provided as to whether NIP funds
mended vaccination for those working at outpatient care clinics.
the vaccine or it simply oversees its implementation. Morocco and
Occupational groups (non-healthcare settings). A smaller
Somalia, on the other hand, reported having plans on the develop-
number of countries reported having influenza vaccine recommen-
ment and implementation of official influenza vaccination policies
dations for one or more occupational groups (Table 4). Eleven
in the next 5 years.
(11/14) countries recommended influenza vaccination for investi-
gators of human influenza outbreaks, but only seven recom-
3.3. Seasonal influenza surveillance for the 2015/2016 season mended vaccination for investigators of animal influenza
outbreaks. Furthermore, seven (7/14) countries recommended sea-
Of the 20 countries, 17 reported having active influenza surveil- sonal influenza vaccination for airline crew members. For essential
lance systems (Afghanistan, Egypt, Iran, Iraq, Jordan, Kuwait, Leba- and emergency services (e.g. police, fire, and rescue staff), vaccina-
non, Morocco, Oman, Pakistan, Palestine, Qatar, Saudi Arabia, tion was recommended by six (6/14) countries. Likewise, vaccina-
Sudan, Syria, Tunisia, and Yemen). All but one country (Pakistan) tion of military personnel was also recommended by six (6/14)
reported using data from existing surveillance systems to help countries. Egypt, Iran, Iraq, Libya, and Tunisia had recommenda-
guide policy-makers and ensure well-informed policy decisions. tions in place for persons working in the animal sector. Iraq was
A. Abubakar et al. / Vaccine 37 (2019) 1601–1607 1603

Table 1
Seasonal influenza vaccine recommendations for clinical risk groups in countries of the Eastern Mediterranean Region.

Country Clinical risk groups


Chronic medical condition Immunological HIV/ Long-term Any Extreme Residents of nursing homes and
disorders AIDS aspirin use condition obesity other chronic care facilities
Afghanistan No seasonal influenza vaccination policy
Egypt R R R NR – R NR
Iran R R R – R R R
Iraq R R R R R R R
Jordan R NR NR NR – NR NR
Kuwait R R R R R R R
Lebanon R NR NR NR NR NR NR
Libya R R R R R R R
Morocco No seasonal influenza vaccination policy
Oman R R R NR NR NR NR
Pakistan No seasonal influenza vaccination policy
Palestine R R R NR R R R
Qatar R R R R R – R
Saudi Arabia R R R R R R R
Somalia No seasonal influenza vaccination policy
Sudan No seasonal influenza vaccination policy
Syria R R R – R R NR
Tunisia R R – NR R R –
UAE R R R – – R R
Yemen No seasonal influenza vaccination policy

R: recommended, NR: not recommended, UAE: United Arab Emirates.


–: no data.

an official vaccination policy at the time of the survey, three coun-


Table 2
Seasonal influenza vaccine recommendations for women during pregnancy and the tries (Morocco, Pakistan, and Sudan) indicated that influenza vac-
early postpartum period in countries of the Eastern Mediterranean Region. cination is recommended for pilgrims. On the other hand, only
five countries recommended influenza vaccination for refugees,
Country Risk factor
and none recommended vaccination for expatriates.
Pregnant women Women up to two weeks post-delivery
Afghanistan No seasonal influenza vaccination policy
3.5. Vaccination monitoring and coverage
Egypt NR NR
Iran R –
Iraq R R Six (6/14) countries reported data on influenza vaccination cov-
Jordan R – erage among high-risk groups during the 2015/2016 season: Egypt,
Kuwait R R Jordan, Kuwait, Morocco, Oman, and Saudi Arabia. Kuwait was the
Lebanon NR NR
Libya R R
only country of the Region that provided coverage data for children
Morocco No seasonal influenza vaccination policy >5 years, reporting a vaccination rate of only 2%. Data on vaccina-
Oman R – tion coverage for pregnant women was also reported by one coun-
Pakistan no seasonal influenza vaccination policy try (Oman), where the vaccination rate was 90%. Three countries,
Palestine R –
on the other hand, provided information on coverage for persons
Qatar R –
Saudi Arabia R – with specific illnesses. Vaccination coverage in this target group
Somalia No seasonal influenza vaccination policy ranged from 2% for people with non-communicable diseases (car-
Sudan No seasonal influenza vaccination policy diovascular, diabetes, long-term aspirin use, immunological disor-
Syria R NR ders, and obesity) in Kuwait to >70% for all high-risk groups in
Tunisia R NR
UAE R –
Saudi Arabia. Furthermore, information on coverage of healthcare
Yemen No seasonal influenza vaccination policy workers was provided by six countries and ranged from 39% in
Kuwait to 100% in Egypt. Finally, three of the 14 countries recom-
R: recommended, NR: not recommended, UAE: United Arab Emirates.
–: no data.
mending influenza vaccination for pilgrims in 2015/2016 reported
data on coverage; vaccination coverage was 100% in all three
the only country that had recommendations for families raising countries.
pigs, poultry, and/or waterfowl.
Other risk groups. Eight countries recommended seasonal 3.6. Formulation and type of vaccine
influenza vaccination for people living in long-term care facilities
(e.g. nursing homes and other chronic-care facilities) (Table 5). Fur- Eighteen (18/20) countries which responded to the survey pro-
thermore, four countries recommended influenza vaccination for vided information on vaccine formulation used. Of these, eight
all household members and caregivers of children under 5 years used the Northern Hemisphere formulation (Iran, Jordan, Lebanon,
and people aged 50 years and older. In addition, six countries Morocco, Pakistan, Palestine, Syria, and Tunisia), one used the
had recommendations for all household contacts of persons at high Southern Hemisphere formulation (Sudan), and nine used both for-
risk of influenza complications (e.g. individuals with chronic med- mulations (Egypt, Iraq, Kuwait, Libya, Oman, Qatar, Saudi Arabia,
ical conditions or suppressed immune systems, older people, chil- UAE, and Yemen).
dren <6 months; i.e. a cocooning strategy). Seventeen (17/20) countries provided information on the type
Pilgrims, expatriates, and refugees. Annual influenza vaccina- (s) of influenza vaccine licensed for use. Thirteen countries
tion of pilgrims was recommended by all 14 countries with an reported using inactivated trivalent influenza vaccines (Egypt, Iran,
influenza vaccination policy (Table 6). Among the countries lacking Iraq, Jordan, Kuwait, Lebanon, Morocco, Oman, Pakistan, Qatar,
1604 A. Abubakar et al. / Vaccine 37 (2019) 1601–1607

Table 3
Seasonal influenza vaccine recommendations for healthcare workers in countries of the Eastern Mediterranean Region by healthcare setting.

Country Healthcare setting


Hospitals Outpatients care clinics Laboratories Long-term facilities
Afghanistan No seasonal influenza vaccination policy
Egypt R R R R
Iran R – R R
Iraq R R R R
Jordan R R R R
Kuwait R R R R
Lebanon R NR NR NR
Libya R R R R
Morocco No seasonal influenza vaccination policy
Oman R R R
Pakistan No seasonal influenza vaccination policy
Palestine R R R R
Qatar R R R R
Saudi Arabia R R R R
Somalia No seasonal influenza vaccination policy
Sudan No seasonal influenza vaccination policy
Syria R NR NR NR
Tunisia R NR R NR
UAE R R R R
Yemen No seasonal influenza vaccination policy

R: recommended, NR: not recommended, –: no data.


UAE: United Arab Emirates.

Table 4
Seasonal influenza vaccine recommendations for occupational groups in countries of the Eastern Mediterranean Region.

Country Work setting


Essential services Military Veterinary Poultry Families that raise pigs, Airline Investigators of human Investigators of animal
(police, firemen, etc.) services services industry poultry or waterfowl workers influenza outbreaks influenza outbreaks
Afghanistan No seasonal influenza vaccination policy
Egypt – – R – – R R R
Iran R R R R – R R R
Iraq R R R R R R R R
Jordan NR NR NR NR NR NR R –
Kuwait R R NR NR NR R R NR
Lebanon NR NR NR NR NR NR NR NR
Libya R R R R – – R R
Morocco No seasonal influenza vaccination policy
Oman NR R NR NR NR NR NR NR
Pakistan No seasonal influenza vaccination policy
Palestine NR NR NR NR NR NR R NR
Qatar – – – – – R R R
Saudi Arabia NR NR NR NR NR NR R R
Somalia No seasonal influenza vaccination policy
Sudan No seasonal influenza vaccination policy
Syria NR NR NR NR NR – R NR
Tunisia R R R R NR R R R
UAE R – – – – R – –
Yemen No seasonal influenza vaccination policy

R: recommended, NR: not recommended, –: no data.


UAE: United Arab Emirates.

Saudi Arabia, Syria, and Tunisia), three reported using inactivated The main outlets for seasonal influenza vaccination reported by
quadrivalent influenza vaccines (Palestine, Qatar, and Tunisia), 14 countries were primary health care centres, hospitals, and out-
and one reported using the high-dose, inactivated, trivalent influ- patient clinics (Egypt, Iran Iraq, Jordan, Kuwait, Lebanon, Libya,
enza vaccine (Libya). Sudan was the only country of the Region that Oman, Palestine, Qatar, Saudi Arabia, Syria, Tunisia, and UAE). Fur-
used the live-attenuated trivalent influenza vaccine. thermore, seven countries reported providing influenza vaccines
through community pharmacies, albeit to a lesser extent than hos-
3.7. Vaccine providers and outlets for vaccination pitals and clinics (Egypt, Lebanon, Morocco, Oman, Pakistan, Pales-
tine, and Syria). Occupational health services and schools, on the
Seventeen (17/20) countries reported data on seasonal influ- other hand, were reported to be the least common outlets for the
enza vaccine providers and principal outlets for administration. administration of seasonal influenza vaccines.
Influenza vaccine was available solely through the public sector
in four countries (Iran, Iraq, Sudan and Tunisia). In the remaining 3.8. Promotion of seasonal influenza vaccination
13 countries, the vaccine was available through both the public
and the private sectors (Egypt, Jordan, Kuwait, Lebanon, Libya, Most countries (14/20) reported the use of a wide range of
Morocco, Oman, Pakistan, Palestine, Qatar, Saudi Arabia, Syria, media activities to promote vaccination programmes (Egypt, Iran,
and UAE). Iraq, Jordan, Kuwait, Libya, Morocco, Oman, Pakistan, Palestine,
A. Abubakar et al. / Vaccine 37 (2019) 1601–1607 1605

Table 5 Kuwait, for instance, has planned to implement regular influenza


Seasonal influenza vaccine recommendations for residents of long-term facilities and immunization campaigns for high-risk groups. Furthermore, Egypt
household contacts in countries of the Eastern Mediterranean Region.
intends to expand the recommended groups for annual influenza
Country Risk group immunization to include university students and vulnerable
Residents of long- Household Household groups. Saudi Arabia has also prepared a plan to incorporate influ-
term care facilities contacts and contacts of enza vaccination in the national immunization schedule. Other
(nursing homes caregivers of persons for plans include covering all risk groups in 2018 and progressing
and other chronic- children <5 years whom
towards universal coverage by 2020 (Libya), adopting a recom-
care facilities) and adults vaccination is
50 years recommended mendation to vaccinate people aged >60 years and <2 years
(Oman), implementing seasonal influenza vaccination policies tar-
Afghanistan No seasonal influenza vaccination policy
Egypt NR NR – geting persons at high risk identified by WHO (Morocco), and
Iran R – R strengthening existing surveillance systems (Palestine). Somalia
Iraq R NR NR expressed interest in implementing a vaccination policy for influ-
Jordan R NR NR
enza but highlighted the need for guidance on development of
Kuwait R R R
Lebanon NR NR NR
the policy, surveillance systems for influenza, capacity building,
Libya R R R purchase of vaccines, and vaccination activities in the country.
Morocco No seasonal influenza vaccination policy
Oman NR NR NR
Pakistan No seasonal influenza vaccination policy
4. Discussion
Palestine R NR NR
Qatar R – –
Saudi Arabia NR NR NR The 2015/2016 survey permitted a regional summary of the
Somalia No seasonal influenza vaccination policy national influenza immunization policies. In general, our survey
Sudan No seasonal influenza vaccination policy shows an increase in the number of countries adopting an influ-
Syria NR NR R
Tunisia R R R
enza immunization policy. Previously, a joint WHO/UNICEF report
UAE – R R identified 12 countries in the Region with seasonal influenza
Yemen No seasonal influenza vaccination policy immunization policies in 2014 [10], whereas we identified 14
R: recommended, NR: not recommended, –: no data.
countries with influenza immunization policies in 2015/2016. In
UAE: United Arab Emirates. addition, Morocco recently adopted a formal vaccination policy
after this survey was completed, bringing the total number of
countries with a policy to 15. Although a small increase, this
Table 6 reflects an improved awareness of influenza and the importance
Seasonal influenza vaccine recommendations for pilgrims, expatriates, and/or of vaccination in mitigating its burden.
refugees in countries of the Eastern Mediterranean Region.
Surveillance of influenza is essential for the selection of appro-
Country Risk group priate vaccine strains and rapid detection of new subtypes in
Pilgrims Expatriates Refugees humans [11]. Local surveillance data provide country-specific
Afghanistan No seasonal influenza vaccination policy
information on the time and type of circulating influenza strains,
Egypt R NR – which enables an informed decision to be made on the choice of
Iran R NR NR the vaccine formulation (Northern vs. Southern Hemisphere or
Iraq R NR R both) to use. Local morbidity and mortality data are also required
Jordan R NR NR
to provide a more complete picture of the burden of disease, which,
Kuwait R NR R
Lebanon R NR NR in turn, is critical to understanding the threat of influenza to public
Libya R – R health. Surveillance also provides the evidence-based data needed
Morocco No seasonal influenza vaccination policy for advocacy and assists in the development and update of preven-
Oman R NR NR
tion, control and mitigation policies for influenza [11]. Seventeen
Pakistan No seasonal influenza vaccination policy
Palestine R NR NR
of the 22 countries in the Region reported conducting surveillance
Qatar R – – for influenza. In fact, 16 national laboratories in 15 countries are
Saudi Arabia R NR NR currently designated as national influenza centres, 13 of which
Somalia No seasonal influenza vaccination policy detect and isolate influenza virus [12]. Consequently, the number
Sudan No seasonal influenza vaccination policy
of reported influenza cases in the Region doubled between 2011
Syria R – R
Tunisia R NR R and 2015 [12]. Currently, either one or both of the Northern and
UAE R – – Southern Hemisphere vaccine formulations are used in countries
Yemen No seasonal influenza vaccination policy of the Region. The increase in the availability of the local influenza
R: recommended, NR: not recommended, –: no data. data will help optimize the recommendations for vaccine formula-
UAE: United Arab Emirates. tions in the Region.
Seasonal influenza is a substantial cause of severe illness and
hospitalization in infants under 6 months of age [13]. Studies have
Qatar, Saudi Arabia, Tunisia, and UAE). The main media activities found that, in many cases, the rate of hospitalization of children
included television and radio advertising, leaflets, posters, and <6 months is three times that of children >6 months [13]. However,
emails. prevention of influenza in this age group is problematic because of
the absence of an approved vaccine, which, in turn, highlights the
3.9. Future plans crucial need for other preventive strategies [13]. Research suggests
that vaccinating pregnant women is the best preventive approach
Nine (9/20) countries identified a number of planned strategies to protect newborns through passive immunization and by reduc-
and operational policy changes needed to tackle the existing ing the risk of infection in moms and its subsequent transmission
impediments to influenza vaccination (Egypt, Kuwait, Libya, Mor- to their babies [14,15]. Vaccination was also associated with
occo, Oman, Pakistan, Palestine, Qatar, Saudi Arabia, and UAE). reduced influenza-associated complications during pregnancy,
1606 A. Abubakar et al. / Vaccine 37 (2019) 1601–1607

which range from miscarriages to preterm deliveries and death influenza vaccines [41]. Of note, the effect appeared to be greatest
[14,16,17]. Nonetheless, influenza vaccination policies in two in people aged 65 years and older [41]. This may be because elderly
countries in the Region did not include maternal influenza vaccina- people go to pharmacies more frequently than younger people, giv-
tion in their recommendations, and only one country reported ing more opportunity for pharmacists to recommend vaccination
influenza vaccination rates in this group. In addition to vaccinating to this age group. In the Region, only seven countries reported pro-
pregnant women, the American Academy of Pediatrics and the viding influenza vaccines through community pharmacies, sug-
Centers for Disease and Control Prevention recommend ‘‘cocoon- gesting that the effect of allowing pharmacists to provide
ing” as a method to protect young infants from seasonal influenza influenza vaccines on the uptake of seasonal influenza immuniza-
by ensuring all family members and close contacts receive the vac- tion is not fully appreciated. Policies to expand the role of pharma-
cine [18,19]. Despite this, only six countries of the Region recom- cists in immunization could improve the accessibility of influenza
mended vaccination for household contacts and caregivers of vaccination in the Region and increase vaccination rates.
children aged <6 months, and none reported on influenza vaccina- It is important to note that the data presented in this study was
tion rates in this group. Therefore, evidence-based data on influ- limited by its reliance on information relied to us by the survey
enza outcomes in infants in the Region are urgently needed to responders. Influenza focal points were tasked with filling out
highlight the importance of this prevention strategy. the survey and the completeness or accuracy of the responses
Avian influenza viruses are potential zoonotic disease agents may be hindered if all stakeholders in the MOH were not engaged.
that may be transmitted from infected poultry to humans [20]. Thus, data on vaccine coverage and influenza-associated deaths
As such, poultry workers and veterinarians have an occupational and hospitalizations and the methods used to obtain these esti-
risk of exposure to avian influenza viruses [20]. Five countries mates were not independently validated or verified. Finally, we
(Egypt, Iran, Iraq, Libya, and Tunisia) in the Region had recommen- did not assess the rationale or basis for making recommendations
dations in place for people working in the animal sector, all of for specific target groups in each country and whether this was
which have experienced outbreaks of avian influenza [21–25]. In based on local evidence, WHO or other organization’s
particular, human cases of H5N1 virus infection were detected in recommendations.
Egypt every year from 2006 to 2016 [26–28]. Nonetheless, the
rationale for vaccinating poultry workers with human influenza
vaccine is not clear since there is no evidence that these vaccines 5. Conclusion
protect against heterotypic avian influenza viruses [29]. One rea-
son would be that vaccination of this group against human influ- Despite widespread policy recommendations on influenza vac-
enza can reduce the potential for an infection with a human cination, attaining high coverage rates among the various popula-
virus, thus, minimizing the chance for a co-infection with an avian tions including those at risk continues to be a challenge in the
virus and the possibility of a subsequent reassortment event occur- Eastern Mediterranean Region. Availability of influenza vaccines
ring between these viruses [30]. is another challenge. In fact, in spite of an increase from previous
As the world’s largest mass gathering of people, the annual Hajj years, the number of influenza vaccine doses distributed in the
pilgrimage to Mecca is an optimal environment for the spread of Region in 2015 accounted for only 2.2% of the global market [8].
respiratory infections including influenza [31,32]. Nearly 40% of Effective communication of influenza vaccination policies and
pilgrims suffer from respiratory symptoms during Hajj, with influ- strong advocacy initiatives are needed to improve awareness of
enza virus being one of the most common etiologies [31,33,34]. the public and health professionals about influenza and vaccines.
The Ministry of Health of Saudi Arabia recommends that all pil- In addition, equitable distribution of and access to influenza vacci-
grims, particularly those at increased risk of severe influenza dis- nes is critical for increasing uptake. Finally, encouraging and
ease including pregnant women, receive the most recent investing in influenza surveillance and research could be particu-
influenza vaccine before leaving for the Hajj [35]. In accordance larly valuable for controlling influenza in the Region. Such research
with the Saudi Ministry of Health recommendations, 14 countries is important for making informed decisions on influenza vaccine
of the Region recommend pre-departure vaccination for all their introduction and expansion.
pilgrims, yet only three reported on influenza vaccination rates
among this group which were 100% in all three. These data suggest
Funding
satisfactory compliance with the vaccine recommendation. Yet, in
view of the limited number of countries reporting on influenza
This research was funded by the WHO Regional Office for the
vaccination rates among pilgrims, the available data are not suffi-
Eastern Mediterranean, Cairo.
ciently representative. Furthermore, the reported data contradict
those in the literature. For instance, one study found that only
19.4% of Egyptian pilgrims were vaccinated against influenza in
Competing interests
the 2015 Hajj season [36]. Another study reported that only 22%
of Hajj pilgrims from 22 countries, including some countries of
None.
the Eastern Mediterranean Region, received the influenza vaccine
in 2013 [37].
Accessibility of vaccines is one of the key barriers to improving Ethical approval
vaccination rates, including for influenza [38]. Given their ubiqui-
tous distribution, extended working hours, and walk-in policies, Not applicable.
pharmacists are in an ideal position to provide influenza vaccines
to the community and thus support increased immunization
uptake [39]. For example, a study in the United States of America Authors’ contributions
demonstrated an increase in influenza immunization rates among
people aged 65 years and older following pharmacists’ involve- Hassan Zaraket, Abdinasir Abubakar, Nada Melhem, and Wasiq
ment in the influenza vaccination programmes [40]. This is consis- Mehmood Khan designed the survey and the analysis. Hassan Zar-
tent with data from Canada that showed an increase in influenza aket supervised the data analysis and wrote the initial draft of the
immunization rates when pharmacists were allowed to administer manuscript. All the authors critically revised the manuscript.
A. Abubakar et al. / Vaccine 37 (2019) 1601–1607 1607

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