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OPEN Factors influencing intention to

obtain the HPV vaccine in South
East Asian and Western Pacific
Received: 5 June 2017
Accepted: 9 February 2018 regions: A systematic review and
meta-analysis
Published: xx xx xxxx

Diviya Santhanes1, Che Pui Yong1, Yan Ye Yap1, Pui San Saw1, Nathorn Chaiyakunapruk1,2,3,4 &
Tahir Mehmood Khan   1,4,5
Since licensing in 2006, there has been poor uptake of the HPV vaccine among the targeted population
in the South East Asia Region (SEAR) and Western Pacific Region (WPR). A systematic review was
conducted to identify the studies exploring the relationship between factors and intention for HPV
vaccination among women in SEAR and WPR countries. Nineteen studies were identified as suitable for
qualitative synthesis, and three as suitable for meta-analysis. Most women had a positive intention to
have an HPV vaccine (range 57%–85%). Having a positive intention to vaccinate was significantly higher
among women not aware of HPV infection (OR: 1.34, 95% CI: 1.02–1.76) and HPV vaccine (OR: 1.57,
95% CI: 1.26–1.96). Lower knowledge level and less confidence in safety and efficacy of the vaccine,
negatively affected intention to vaccinate. Perceiving the vaccine to be expensive, low perception of
contracting HPV infection and cervical cancer, and lack of concrete recommendations from healthcare
providers also negatively affected intention to vaccinate. This review suggests the decision-making
processes of women in SEAR and WPR is influenced by the cost of vaccination, perceived efficacy and
safety of vaccine, provision of information on vaccination, and the awareness about HPV infection and
the HPV vaccine.

Human papillomavirus (HPV) has been recognised as the leading cause of cervical cancer, which in turn is the
fourth-most prevalent cancer among women worldwide1. The World Health Organization’s (WHO) South East
Asia Region (SEAR) and Western Pacific Region (WPR) have two of the highest burdens of cervical cancer1–3.
In 2012, approximately 94,000 and 43,000 deaths from cervical cancer were recorded in the SEAR and the WPR,
respectively1. HPV vaccines offer a promising breakthrough to curb the global burden of cervical cancer. Since
2006, the vaccine has been approved for use in over 100 countries. The United States was the first country to
introduce a publicly funded HPV immunisation program4. In the WPR, Australia introduced its funded HPV
immunisation schedule in 2007, followed by Malaysia in 2010 and Japan in 20114. Conversely, there are no pub-
licly funded HPV immunisation programs in the SEAR. An estimated 118 million women have been targeted
for HPV immunisation worldwide and the number of fully vaccinated females in low- to upper-middle-income
countries ranges from 1 million to 13.3 million, indicating a low uptake for HPV vaccination in these areas4. The
lower response to HPV vaccination is reported to be due to vaccine hesitancy, which underpins reduced vaccine
uptake and is defined as a delay in acceptance or refusal of vaccines despite availability of vaccine services5.

1
School of Pharmacy, Monash University Malaysia, Bandar Sunway, Selangor, Malaysia. 2Center of Pharmaceutical
Outcomes Research (CPOR), Department of Pharmacy Practice, Faculty of Pharmaceutical Sciences, Naresuan
University, Phitsanulok, Thailand. 3School of Pharmacy, University of Wisconsin, Madison, USA. 4Asian Centre for
Evidence Synthesis in Population, Implementation and Clinical Outcomes, (PICO), Health and Well-being Cluster,
Global Asia in the 21st Century (GA21) Platform, Monash University Malaysia, Bandar Sunway, Selangor, Malaysia.
5
The Institute of Pharmaceutical Sciences (IPS), University of Veterinary & Animal Sciences (UVAS), Outfall
road, Lahore, Pakistan. Correspondence and requests for materials should be addressed to T.M.K. (email: tahir.
[email protected])

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Figure 1.  Flowchart for identification and inclusion of articles in systematic review.

In this situation, it is vital to explore how the women in the SEAR and the WPR respond to the HPV vaccine;
i.e., their intention to vaccinate. This systematic review is one of the first efforts to identify the factors influencing
a woman’s intention to have the HPV vaccine. This review will also gauge the knowledge, beliefs and attitude
towards the vaccine among women from the WPR and SEAR, as these are fundamental when making decisions
about vaccination. To date, existing systematic reviews have summarised predictors of HPV vaccine intention
and decision-making among women from the US, the UK, Australia and North America generally, and among
African Americans in the US specifically2,6,7. However, none have demonstrated a clear association between influ-
ences and intention to vaccinate. Moreover, these systematic reviews have not explored the factors leading to
vaccine hesitancy among women from the SEAR and WPR. These reviews also lack any quantitative analysis
that associates the factors with intention to vaccinate for HPV2,6,7. This gap in the existing literature needs to be
addressed, especially for the SEAR and WPR, which are regions in which a large female population of various
ethnic, religious and socio-demographic backgrounds reside. The findings from this review will be valuable as the
provision of statistical and qualitative data synthesis will further strengthen the association of factors that influ-
ence women’s decision-making regarding vaccination against HPV. Hence, this information will be of assistance
in devising suitable interventions to improve access and acceptability to HPV vaccination in the SEAR and WPR.

Results
Study selection.  Details of the study selection process are described in Fig. 1. A total of 5,546 research
articles were identified through the initial search, of which 5,483 did not meet the inclusion criteria and were
therefore excluded. Only 63 studies were considered eligible and examined in further detail. After further consid-
eration, 44 articles were excluded: 6 were qualitative or mixed-methods synthesis studies, and 38 did not evaluate

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Results obtained
Sample size Secondary NOS
Study Country Objective Respondents Recruitment site (response rate %) Primary outcome outcome Score
Evaluation of knowledge
Positive intention
about the Pap smear,
Poor knowledge of for 77% and
Charakorn C. HPV, and the HPV Both mothers and
Thailand Hospital 536 (70%) HPV infection and 84% of mothers 5
et al.23 vaccine, and the their daughters
HPV vaccine and daughters,
acceptability of the
respectively
vaccine to Thai women
27.5% and 37.6%
Total of 1022
To provide a more of mothers
Schoolgirls aged (39.3%) and 1005
representative and Schoolgirls from 5 intended to
between 11 and (50.2%) mothers
updated assessment constituency areas vaccinate Willingness to pay
Choi HCW 18 years old, and in 2008 and 2012
Hong Kong on the acceptability of and mothers through daughters’ in for full course of 6
et al.11 mothers with respectively.
female adolescent HPV random-digit dialling 2008 and 2012, vaccination
daughter(s) ≤ 18 2167 (96.2%)
vaccination in Hong telephone interviewing respectively. 27.1%
years old for schoolgirls’
Kong of schoolgirls in
survey
2008.
To investigate why Mothers’
Japanese adolescent knowledge about
girls decline, continue HPV vaccine
or discontinue their and attitude
Mothers with 16% intended
Egawa-Takata T HPV vaccination, how 2828 mothers towards cervical
Japan daughters aged Internet to get daughters 5
et al.13 their mothers influence (28.3%) cancer screening
10–18 vaccinated
their decisions, and the influenced their
mothers’ feelings about decision to get
future HPV vaccination their daughters
for their daughters vaccinated
To investigate the
prevalence of use of
HPV vaccination in the
daughters of obstetricians
and gynecologists, and Doctors’ daughters: The number
their attitudes related HPV vaccinations of vaccinated 64% intended
Egawa-Takata T
Japan to the HPV vaccine and before (2012) and Hospital 264 (46%) daughters was to get daughters 1
et al., 201612
cervical cancer screening, after (2014) the lower in 2014 than vaccinated
to gain insights into their adverse news releases in 2012
reasoning for or against
recommending HPV
vaccination for their
daughters
To examine young
women’s perceptions
Undergraduate Low awareness and
and acceptability of 44% of women
female students year knowledge of HPV
Gu C et al.8 China human papillomavirus Medical college 119 (94.3%) intended to get 7
1 to 4, aged 18 or vaccine and cervical
vaccination and factors vaccinated
above cancer
influencing acceptability
in mainland China
To examine health beliefs Full-time female
and intention to obtain undergraduate Poor awareness of 63% of students
Five universities in
Hsu YY et al. 16
Taiwan HPV vaccination among students attending 845 HPV infection and intended to obtain 7
Taiwan
undergraduate women in 5 universities in HPV vaccine HPV vaccine
Taiwan Taiwan
Assessing knowledge
Poor awareness
and awareness of HPV, Khokana, a suburban 77.5% of women
and knowledge
Johnson DC cervical cancer and HPV Women attending community, and intended to obtain
Nepal 749 of HPV, cervical 6
et al.22 vaccines among rural health camps Sanphebagar, a rural HPV vaccine if
cancer and HPV
and suburban women community offered for free
vaccine
in Nepal
To examine knowledge
and beliefs regarding
Thai women Knowledge about
HPV and cervical
Juntasopeepun aged 18–24 years 56.5% intended to HPV and cervical
Thailand cancer and to predict University 391 7
P et al.24 in Chiang Mai, receive the vaccine cancer were
vaccination intention
Thailand moderate
among young women in
Thailand
To examine the Intention to get
relationships between vaccinated was
attitudes toward and not high, and
Sixteen colleges located Intention gets lower
intention to receive the Female Korean women were not
Kang HS et al.14 Korea in 16 regions across the 1600 (87%) when attitude is 5
HPV vaccination and college students confident of the
nation negative
intention to use condoms vaccine’s safety and
among Korean female changes in sexual
college students behaviour
Wanting more
To examine knowledge
education about the
about HPV and
Female Awareness and vaccine, perceived
attitudes towards HPV
Kang HY et al.15 Korea undergraduate University 339 (94.7%) knowledge of HPV severity and 6
and HPV vaccination
students was poor knowledge of HPV
among Korean female
associated with
undergraduate students
intention

Continued

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Results obtained
Sample size Secondary NOS
Study Country Objective Respondents Recruitment site (response rate %) Primary outcome outcome Score
To evaluate the
willingness of Thai
mothers to get their
76.9% of parents
daughters vaccinated
intended to get
against HPV if it is free
Female parents of Knowledge vaccinated if offered
Kruiroongroj S of charge (acceptance) or
Thailand adolescent girls aged Secondary schools 1200 (71.7%) regarding the HPV for free and 68.9% 3
et al.25 if it is not free of charge
12–15 vaccine was low were willing to pay
(willingness to pay), and
if vaccine was not
to examine their current
offered for free
knowledge regarding
HPV vaccine and cervical
cancer
Knowledge 84.6% of women
Women aged
To assess women’s and awareness intended to get
14–59 living in 6 community clusters
knowledge about HPV were low among vaccinated if the
Li J et al.9 China metropolitan and from 3 major cities and 6024 (95.8) 7
and their acceptance of women in both HPV vaccine was
rural regions of rural areas in 3 provinces
the vaccines metropolitan and made available to
China
rural areas them
To assess the knowledge,
acceptability, attitudes Family practice
Knowledge and
and feasibility concerning and obstetrics and
awareness related 46% intended to
Montgomery HPV and cervical cancer All women between gynaecology clinics and
India 225 (90%) to HPV and receive the HPV 5
MP et al.21 among adult women the ages of 18 and 44 postnatal wards within
cervical cancer vaccine
in Dakshina Kannada the hospital Karnataka,
was low
district of the southern India
state of Karnataka, India
65.7% and 55.8%
To determine the
Mothers with at least of mothers
acceptability rates of Knowledge of
one child under 18 intended to get
Sam IC et al.19 Malaysia HPV vaccination by University hospital 362 HPV and the HPV 5
years old attending daughters and
Malaysian mothers for vaccine was low
outpatient clinics sons vaccinated,
daughters
respectively
To assess the knowledge Knowledge
Two thirds of
and attitudes towards Women aged Rural villages in the of HPV, HPV
respondents
HPV, HPV vaccination between 18 and 25 states of Perak and vaccination and
Wong LP 20
Malaysia 589 (84.7%) professed an 4
and cervical cancer years and living in Pahang in Peninsular cervical cancer
intention to receive
among young women in the household Malaysia were extremely
the HPV vaccine
rural settings poor
To explore awareness As a part of a larger study
Adult women aged
and acceptability of on reported history of Only 3.2% intended
18–69 who were
HPV vaccination and Pap smear tests, health to obtain the
officially registered
to identify factors experiences, perceptions Awareness of HPV vaccine. Intention
Yen CF et al.17 Taiwan as having physical 438 4
influencing HPV of cervical cancer and vaccine was poor increased up to 60%
disabilities in Taipei
acceptability among HPV vaccination among if the vaccine was
City as of March
women with physical women with physical offered for free
2009
disabilities in Taiwan disabilities in Taiwan.
Mothers and
54% intended
partners were
to receive HPV
To examine attitudes influential in
vaccine at low
toward and acceptability vaccination
Three communities in price, whereas
Young AM of HPV vaccination Women aged from decisions together
Philippines the Central Visayan 435 only 30% and 31% 4
et al.26 among a community- 18 to 52 years old with access to
region intended to receive
based sample of women transportation,
at moderate
in the Philippines social support
and high prices,
and benefits of
respectively
vaccination
To investigate awareness
and knowledge of HPV/
the HPV vaccine and Awareness and Only 26.49% of
potential acceptance of Mothers of daughters knowledge of mothers intended to
Yu Y et al.10 China Weihai, China 1578 (85.3%) 5
the HPV vaccine among aged 9–17 years old HPV/HPV vaccine get their daughters
mothers with a teenage was poor vaccinated
daughter in Weihai,
Shandong, China
Among the
unvaccinated
participants
To describe the (n = 230), 41.7%
Female students
knowledge, attitudes had no intention to Knowledge of HPV
Zhuang QY attending a tertiary
Singapore and practices of young University 255 receive the vaccine and cervical cancer 6
et al.18 institution in
women regarding HPV and 27.0% cited was found to be low
Singapore
vaccination lack of information
as a major
barrier to HPV
vaccination

Table 1.  General characteristics of 19 included cross-sectional studies.

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intention of receiving the HPV vaccine among their respondents. Studies investigating acceptability towards
HPV vaccination or willingness to receive HPV vaccination were also included, as the assessment of HPV vaccine
initiation was similar to studies investigating intention. A final number of 19 descriptive, cross-sectional studies
met the inclusion criteria and were included for systematic review. Of these, 16 had marked diversity in measures
of outcome reporting, and so were described in a qualitative synthesis manner. Three articles were identified as
having similar comparator and outcome groups and underwent meta-analysis.

Characteristics of included studies.  The characteristics of all included studies are shown in Table 1. All
19 studies selected for review were descriptive and cross-sectional surveys in study design and used self-reported
questionnaires to assess study outcomes. All studies were published in English and conducted post-licensure of
the HPV vaccine (after 2006). The geographical distribution of these studies was widespread, with research car-
ried out in China8–10, Hong Kong11, Japan12,13, Korea14,15, Taiwan16,17, Singapore18, Malaysia19,20, India21, Nepal22,
Thailand23–25 and the Philippines26. Respondents were recruited from healthcare settings (including obstetrics and
gynaecology clinics21,23, hospitals12,19,21 and health camps22, educational environments (including schools10,11,25,
colleges14,24 and tertiary institutions8,15,16,18,24), random digit dialling11, community clusters9,17,20,26 and the inter-
net13. The included studies all involved female respondents, with a total sample size of 22,533. Respondents con-
sisted of mothers/parents with daughters eligible for HPV vaccination10,12,13,19,22,25, adult women8,9,14–18,20,21,24,26
and a combination11,13 (mothers and daughters). In most of the included studies, the primary outcomes assessed
were factors such as awareness, knowledge and attitudes or health beliefs of respondents on practices and preven-
tive measures of HPV infection9,10,13,15–17,20–23,25. Intention, acceptability or willingness to have the HPV vaccine
were often secondary outcomes. Two studies investigated vaccine intention for the women themselves and their
daughters9,23, seven studies for their daughters only10–13,19,22,25 and ten studies for getting vaccinating themsel
ves8,14–18,20,21,24,26. Mothers were the decision-makers for daughters who were of adolescent age9,12,13,19,23. Studies
among adult women in the SEAR and WPR demonstrated that they themselves made the decision about being
vaccinated8,14,17,18,24,26. The influence of others (such as parents, partners/husbands) on a woman’s decision to have
the HPV vaccine was not explored in most included studies in this review. Eleven studies reported that more
than half of their respondents (Range: 56.5% – 84.6%) had a positive intention of undergoing the vaccination for
themselves or their daughters9,12,14–16,18–20,23–25. In comparison, in seven studies fewer than half of the respondents
(Range: 3.2% – 46%) had a positive intention to be vaccinated8,10,11,13,17,21,26. More women expressed an intention
to have a vaccine (Range: 60% – 97.8%) if it was offered for free, as reported in four studies17,19,22,25.

Quality assessment of included studies.  The quality assessment of all included studies in the review is described
in Supplementary Table S3. Eight included studies were of good quality8,9,11,15,16,18,22,24, with scores ranging from
6 to 7; six studies had average quality10,13,14,19,21,23 with a score of 5; and the remaining five studies were of poor
quality, with scores ranging from 3 to 412,20,25,26.

Factors influencing intention to obtain HPV vaccine.  Knowledge on preventive measures of HPV infec-
tion and its complications.  Having awareness of HPV, the HPV vaccine, cervical cancer or genital warts does
not necessarily mean good knowledge of these. In addition, the type and number of questionnaire items used to
assess the knowledge level of women differed markedly between studies, so it was challenging to combine the
results. Overall, five studies reported that women having better knowledge on preventive measures of HPV infec-
tion and its complications are more likely to express intention to receive the vaccine8,10,15,20,23. Only one study, by
Juntasopeepun, et al.24, reported that there was no significant association between knowledge level of HPV and
cervical cancer and intention to get vaccinated, among young Thai women24.

Perceived susceptibility to HPV and cervical cancer.  Eight studies associated women’s perception of contracting
HPV and cervical cancer in the future to intention to vaccinate8,9,13,15,16,21,24,26. Women who perceive themselves
to be at risk of contracting HPV infection and cervical cancer were more likely to have the vaccine than women
who do not. In addition, not many women felt that they are at risk of getting HPV or cervical cancer. Three stud-
ies reported, respectively, that only 4% (n = 8) of Indian women, 9.5% (n = 37) of Philippine women and 20% of
Malaysian women felt that they were at risk of getting HPV20,21,26.

Perceived seriousness of disease.  Three studies measured the perceptions of respondents to disease severity of
HPV infection and cervical cancer15,16,24. Two studies stated that female university students who perceived cervi-
cal cancer as very serious had higher chances of getting vaccinated against HPV compared to those who thought
otherwise15,16. The study by Juntasopeepun, et al.24, among college-aged Thai women did not find a significant
association between women’s perception of severity of cervical cancer and intention to vaccinate.

Concerns about side effects of HPV vaccine.  A total of seven studies associated concerns about side effects of the
HPV vaccine with non-receipt of HPV vaccination. Six of these studies found that a female parent or a young
women’s concern about the adverse effects of the vaccine negatively affected vaccination intentions8,10,12,20,25. Only
one study by Hsu, et al.16, reported that the HPV vaccine’s adverse effects had no significant association with
intention to vaccinate.

Confidence in the efficacy of the vaccine.  Four studies predicted that women’s confidence in the efficacy of the
HPV vaccine would affect the intention to vaccinate. Women’s intention to receive the HPV vaccine increases if
they are confident in the efficacy of the vaccine in combating cervical cancer, as demonstrated by two studies8,13.
Mothers who doubted the efficacy of the vaccine were not likely to accept the vaccination for their daughters10,19.

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Figure 2.  Forest plot of the two studies estimating the effect of awareness of HPV infection on positive
intention to have the HPV vaccine.

Figure 3.  Forest plot of the three studies estimating the effect of awareness of HPV vaccine on positive
intention to have the HPV vaccine.

Cost of HPV vaccine.  Five studies associated cost concerns with intention to vaccinate. Of these, three studies
reported that the cost of the vaccine was a barrier to vaccination16,19,24. One study in India stated that only 12%
(n = 202) of women would agree to pay for all three doses of HPV vaccine, at a cost of $360 US dollars21. On the
contrary, the cost of the vaccine was not a profound barrier among mothers in Shandong, China: only 3.79%
(n = 1,160) of them thought the vaccine was too expensive10.

Concerns about risky sexual behaviour.  Concerns about risky sexual behaviour were only shown among a minor-
ity of female Thai and Korean college students when asked for their reasons for non-vaccination against HPV14,25.

Recommendation from others.  Women who received a recommendation from others to opt for vaccination were
more likely to accept the vaccine compared to those who did not receive any recommendation. The healthcare
provider was cited as the most trusted source of recommendation16,20,24,26. Women who received recommenda-
tions from a healthcare provider were more likely to undergo HPV vaccination16,26.

Educational need.  Needing more information on HPV-related aspects was shown to have a profound effect
in two studies15,18. Lack of information was the main reason why Singaporean and Korean university students
refused vaccination. Only two studies reported concerns about the source of the vaccine9,10. Doubts about the
sources of the vaccine were the major reason for unwillingness to get vaccinated among Chinese women in both
rural and metropolitan areas and a minority of mothers in Shandong, China10.

Awareness of HPV infection and HPV vaccine.  Of the 19 included studies, only two examined the relationship
between awareness of HPV infection and positive intention to vaccinate8,16. Women who are unaware of HPV have a
higher chance 1.34 times greater [1.34 (CI 95% 1.02—1.76)] than those aware of HPV of getting vaccinated (Fig. 2),
with no heterogeneity identified within and between the included studies [Tau2 = 0.00, Chi = 0.11, df = 1; I2 = 0%].
Three studies examined the relationship between awareness of HPV vaccine and intention to vaccinate8,16,24.
The likelihood of positive intention to undergo HPV vaccination is 1.57 times [1.57 (CI 95% 1.26—1.96)] higher
among women unaware of the HPV vaccine compared to women aware of HPV vaccine (Fig. 3). Again, no heter-
ogeneity was found between these three studies [Tau2 = 0.00, Chi = 0.01, df = 2; I2 = 0%].

Discussion
This is the first systematic review that scrutinizes the literature on factors influencing the intention of women in
countries in the SEAR and WPR to get HPV vaccines. Investigating their intention to receive HPV vaccines and
how it is affected by influential factors is a useful insight to devise strategies that can remove the barriers involved
and facilitate a more positive intention of vaccinating against HPV.
In regions of high cervical cancer mortality such as SEAR and WPR, this review revealed that young women
and female parents generally have positive intentions (57% to 65% of respondents) to get themselves or their
children vaccinated against HPV. Despite this, concerns and barriers were identified when a women hesitates to
obtain HPV vaccine.
Based on the results from our meta-analysis, women unaware of HPV infection and the availability of HPV
vaccine are respectively 1.34 and 1.57 times more likely to receive vaccination. It is possible that women in the ‘una-
ware’ group possessed limited information, for example from media sources or friends and may consider the HPV

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as a bigger health concern in comparison to those who are more aware of the subject. The mixed views on HPV
vaccination makes it difficult for parents and young women to make informed decisions27. Our findings of a lower
intention to vaccinate associated with improved awareness are consistent with those of Trim, et al.28, obtained from
a systematic review of mostly American and European studies (81.1% of included studies). Although the percentage
of parents who have heard about HPV rose over time from 60% (2005) to 93% (2009), the intention to vaccinate
declined from 80% (2008) to 41% (2011)28. The reason for this decline was that parents were concerned about the
safety of the vaccine and wanted more information28. This further affirms that the decision-making process for the
HPV vaccination is multifactorial, and an assessment of what hinders women from taking the HPV vaccine needs
to consider all the influential factors29. Thus, it is essential to understand that being aware of HPV vaccination and
the decision to be vaccinated against the HPV are two different issues, and ‘being well aware’ does not necessarily
indicate that an individual will opt for vaccination for their children. Yang, et al.30 reported that personal beliefs and
understanding about vaccination are the main factors that dictate the decision not to vaccinate or to seek exemp-
tion from mandatory vaccination among well-educated respondents in California. Perlman, et al.29 identified high
levels of acceptability of the HPV vaccine despite low levels of knowledge and mixed levels of awareness of cervical
cancer, HPV and the HPV vaccine29. It is hard to judge why lower awareness led to higher acceptability of the HPV
vaccine, however, a possibility is that due to lack of knowledge individuals may consider the HPV as a bigger health
concern in comparison to those who are well educated or more aware of the HPV and its vaccine. Although the fall
in HPV vaccine uptake with awareness may be considered counterintuitive, it affirms the multifactorial nature of the
decision-making process and underlines the need for assessment of all influential factors. It may be wise to focus on
‘belief modification’ of the public to improve vaccine uptake by targeting information on the importance and safety
of vaccines to specific sections of the community30.
From our study, it was evident that wanting more information on HPV vaccination was a reason for refusal
among women in the SEAR and WPR. Reviews by Holman, et al.6, and Kessels, et al.7, in high-income countries
(the US, the UK, Canada and Australia) associated parental satisfaction with the amount and quality of informa-
tion with vaccine uptake, whereas vaccine refusal was linked to dissatisfaction with information6,7.
Safety concerns about the vaccine were also found to be profound. Most included studies revealed that women
concerned about the side effects of the vaccine had a more negative intention to undergo vaccination8,10,12,20,25.
This resonates with findings from Hopkins, et al.31, and Kessels, et al.7, here parental concerns about vaccine safety
and side effects negatively affected vaccine initiation.
Our review revealed that women in the SEAR and WPR had doubts about the efficacy of the HPV vaccine. A
lack of confidence in the vaccine’s ability to prevent cervical cancer was associated with a more negative inten-
tion to get vaccinated8,10,13,19. This negative belief was also reflected in other countries; for example, the US and
in Africa, where increased confidence in the vaccine led to a positive intention to have the HPV vaccine 32–35.
Effectiveness of other vaccines such as polio and measles influenced respondents’ receipt of the HPV vaccine,
as reported by both Katahoire, et al.36 and Ports, et al.37. In addition, parents from developed countries who had
previously had their child vaccinated against meningitis or had a positive belief in the efficacy of the vaccine were
more likely to get their child vaccinated against HPV28. Confidence in the efficacy of the HPV vaccine was cited
in only four studies in this review. In these studies, women who perceived the vaccine to be effective in combating
cervical cancer and HPV infection were more likely to receive the vaccination. This was only discussed in African
studies, but the results were very varied making it difficult to come to a conclusion38.
The cost of the vaccine was a significant barrier for women in the SEAR and WPR, as the HPV vaccine is
not funded in most countries in these regions39,40. To date, the only countries that have introduced the HPV
vaccine in their national immunisation schedule since its licensure are Australia, Bhutan, Brunei Darussalam,
Japan, Malaysia, Singapore, Micronesia and Palau, which together comprise 21% (8/38) of countries in the two
regions41–43. As both the SEAR and WPR mostly consist of low- and middle-income countries (LMIC), setting up
a publicly funded HPV immunisation program can be costly, and access to cervical cancer screening programs
and healthcare facilities can be a significant issue31,44. In a study by Ferrer, et al.39, financial concerns came up in
high-income countries (HIC) such as the US, Hong Kong and Sweden39. Women in the US were reluctant to go
for an HPV vaccination due to the lack of reimbursement by insurance companies, and women in Hong Kong
(one of the countries that does not offer free HPV vaccination) thought the vaccine was too expensive33,39. The
HPV vaccine is available to girls aged 13 to 17 in Sweden on a paying basis, which is a barrier for poor families39.
A study by Cunningham, et al.38, in Africa on the intention to get the HPV vaccine also revealed cost concerns
as an important barrier. Some participants thought the vaccine should be offered for free, while others indicated
willingness to pay, but substantially less than the actual cost38. However, cost was not an evident barrier where the
vaccine was offered for free, such as in Australia, where the vaccine was provided free for a limited time, prompt-
ing young women to get vaccinated39,40.
In both the SEAR and WPR, women who perceived they are at low risk of contracting HPV cervical cancer
were less likely to get vaccinated compared to women who thought otherwise. Many women in both these regions
also did not feel they are at risk of acquiring HPV infection and cervical cancer, although the reason for this was
not explored in all relevant studies. The minority of women who felt they were at risk was reported in the inter-
national literature as well. Low perception of the risk of HPV acquisition and misperceptions of need based on
sexual activity was also reported in the review by Holman, et al.6, on HIC. In addition, women who perceived
themselves at risk of getting HPV infection or cervical cancer were more likely to have the vaccine. In compari-
son, studies in Africa reported otherwise: most parents and adults perceived the risk of HPV infection of cervical
cancer for their daughters as high, ranging from 41% to 78%, but its relationship with intention to vaccinate
was mixed38. Women in the SEAR and WPR who saw cervical cancer as a serious disease had higher chances
of getting vaccinated. This finding resonated with Trim, et al.28, and Cunningham, et al.35, which were literature
reviews of HIC and Africa respectively, and which showed that those who recognized cervical cancer as a disease
of higher severity were also more likely to accept the vaccine.

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Concerns about initiating early or risky sexual behaviour among their daughters did not prominently appear
in our review, with only two studies citing this concern. In comparison with other regions, this concern appeared
mostly among Asian mothers residing in developed countries39. Irrespective of geography and delivery setting
of the HPV vaccine, cultural sensitivity was profound among women when deciding to allow their daughters to
undergo vaccination for cervical cancer. Muslim and Asian mothers in the UK and Australia were concerned that
giving permission their daughters to be vaccinated would be seen as a sign of approval for sex before marriage45,46.
Some parents dismissed this viewpoint, such as Alaskan and Australian parents, when allowing their child to be
vaccinated against HPV39,46,47.
Support from family and friends and a physician’s recommendation are also important when women in the
SEAR and WPR decide about having the HPV vaccine. Regardless of a country’s income status and cervical
cancer mortality rate, women in the SEAR and WPR had the same concerns and barriers as women from other
countries regarding intention to have the HPV vaccine. A women receiving support from her parents, encourage-
ment from friends or recommendation from a physician is more likely to have the vaccine. Receiving a physician’s
recommendation or discussing the HPV vaccine with a physician was associated with vaccine acceptance and
initiation in numerous studies from HIC as reported by Holman, et al.6. However, it was also reported in the same
study that parents frequently cited not having a physician’s recommendation as a reason for not getting their child
vaccinated. Studies in Africa also stated similar findings: a doctor’s recommendation was positively associated
with intention to vaccinate38. There is a need for a more tailored health-promotion program for HPV vaccination.
In this, it would be useful that parents and young women understand why HPV vaccination is recommended
at a young age, the benefits of taking the HPV vaccine and how it outweighs the risks involved (such as adverse
effects), the risk factors involved in acquiring HPV infection, and the efficacy of the HPV vaccine in preventing
genital warts and cervical cancer. Abolishing the cultural and religious barriers may be impossible, but pitching
the vaccine as a cervical cancer vaccine rather than the HPV vaccine may help improve uptake. In addition, it is
recommended that parents and young women be educated on why the HPV vaccine needs to be obtained at a
young age rather than later. Although there were uncertainties about the benefits of vaccinating women aged 15
to 45 years48, Gardasil was reported to remain highly effective in preventing HPV-related diseases in females of
this age group who were HPV-naïve49 but less effective in those who may have had a previous HPV infection50.
Thus, GPs should still consider older women who may benefit from HPV vaccination by taking into account of
their previous exposure and the risk of future exposure to HPV. Reducing the cost of the vaccine also needs to be
considered; support from donations and government subsidies would be useful to help reduce the cost of getting
the HPV vaccine. Access to healthcare facilities among populations in rural settings needs to be investigated, and
suitable interventions are needed to ensure the populations there are also educated about the HPV vaccine.

Strengths and limitations of this review.  This systematic review provides a comprehensive summary
of the concerns and barriers that women in the SEAR and WPR have when making informed decisions on HPV
vaccination. It is a good reflection of factors contributing to HPV vaccine hesitancy in populations that are at high
risk of developing cervical cancer and HPV infection despite the availability of vaccine services. However, this
review is limited by studies that mostly recruited populations from cities or urban areas, so it cannot be general-
ised to other populations such as rural residents, ethnic minorities or immigrants. Further, this review may not
be applicable to all LMICs, as there may be pilot schemes or GAVI projects in which vaccine hesitancy cannot be
applied.

Conclusion
Intention to vaccinate was generally positive among women from the SEAR and WPR. The main factors that led
to a negative intention to receive the HPV vaccine were the cost of vaccination, concerns about efficacy and safety
of the vaccine, lack of information on vaccination, and lack of awareness about HPV infection and the HPV vac-
cine. Future research should involve investigations of the actual uptake and completion of HPV vaccination, and
barriers to receiving the HPV vaccine (rural areas, lower socioeconomic status, and ethnic minorities). Health
promotion programs for the HPV vaccine should clarify women’s risks of acquiring HPV infection and the ben-
efits of getting vaccinated, while being culturally sensitive.

Methods
Research protocol and registration.  A systematic review was performed using Preferred Reporting
Items for Systematic Reviews and Meta-Analyses (PRISMA). The protocol for this systematic review is registered
under Centre for Reviews and Dissemination (PROSPERO) and is available from: http://www.crd.york.ac.uk/
PROSPERO/display_record.asp?ID=CRD4201603574951.

Search strategy.  All the relevant studies from inception till 31st December 2016 were considered for inclu-
sion. Six databases, namely Pubmed, EMBASE (Ovid), PsycINFO (Ovid), Cochrane, MEDLINE (EBSCOhost)
and CINAHL Plus (EBSCOhost), were systematically searched using search terms and keywords by three inde-
pendent reviewers (DS, CP, YY). To capture all relevant influential factors involved in women’s decision-making
processes for having the HPV vaccine, the following Mesh terms were used in Pubmed, connected with Boolean
phrase AND: “papillomavirus infections”, “female”, “papillomavirus vaccines”, “health knowledge, attitudes, prac-
tice”. Details of search strategies in the remaining databases are provided in the Supplementary Table S1. No
language restrictions were imposed, but geographical restriction was applied in some databases.

Inclusion criteria.  Upon completion of the search across six databases, the following inclusion criteria were
used to identify the potential papers for qualitative and qualitative synthesis: (1) A quantitative study that exam-
ined the factors influencing women’s decision-making processes in obtaining the HPV vaccine and their intention

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to obtain the HPV vaccine; (2) The study was conducted in WHO-defined SEAR and WPR; and (3) The study
recruited participants eligible for HPV immunisation; i.e., girls aged 9–13 years old and girls aged ≥ 15 years old.
Parents who had daughter’s eligible for HPV immunisation were also included.

Study Selection.  Studies meeting the inclusion criteria were further screened for duplication by three inde-
pendent reviewers (DS, YYY and CPW). After reaching a final consensus about the article numbers, the full-text
articles of the studies were then screened for the final inclusion. Disagreements were resolved by discussion and
consensus between three reviewers (DS, YYY and CPW). If no agreement could be reached, the remaining two
reviewers (TK and PSS) made a decision. The identification and inclusion of articles is depicted in a PRISMA flow
diagram (Fig. 1).

Data Extraction Process.  The data extraction form was developed in an Excel spreadsheet. The form
was piloted from two trial reports to ensure suitability for use. A completed extraction form is attached in
Supplementary Table 2. Three reviewers (DS, YYY and CPW) extracted the relevant data from each included
study, and two review authors (TK and PSS) checked the extracted data. Disagreements were resolved by discus-
sion and consensus among all authors. No attempt was made to seek additional information from the included
primary studies.

Outcome of interest.  The primary outcome of interest for this systematic review was the intention to vac-
cinate for HPV. Any other relevant information that encompassed awareness and knowledge of HPV-related
aspects, factors accepting or rejecting vaccination, sources of information, and attitudes and beliefs, were also
considered for further comparison between the studies.

Quality assessment of included studies.  All the studies included in this systematic review were obser-
vational. The quality of the included observational studies was assessed using the Newcastle–Ottawa scale
(NOS) which reports the quality of studies on a scale of 0 to 1052. One author (DS) evaluated the quality of
included studies on both study and outcome levels (Supplementary Table S3). This was subsequently verified and
crossed-checked by TMK and PS.

Synthesis of results (quantitative).  Articles presenting data relevant to the outcomes of interest were
further subjected to Meta-analysis using Review Manager (RevMan), version 5.3. A random effects model was
applied during analysis because the true effect size varies according to differences in population from study to
study. The odds ratio (OR) was computed together with inverse variance and 95% confidence interval (CI) for
calculation. We tested for heterogeneity to measure inconsistency of effects across studies. The level of heteroge-
neity between and within studies was determined as either low (25%), moderate (50%) or high (75%)53. Studies
with binary data that was not combinable due to marked variation between studies were synthesised narratively.

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Acknowledgements
We would like to thank Monash Library staff for their support to get the full text for the papers included in this
paper. We would like to thank Global Asia 21 platform for providing financial support to hire research assistant
for this project.

Author Contributions
T.M.K., P.S.S. and N.C. conceived the idea; D.S., C.P.Y. and Y.Y.Y. performed the search and data extraction; P.S.S.
and D.S. devised the method and analysed the data; T.M.K. and N.C. verified the data and analysis. D.S., C.P.Y.
and Y.Y.Y. wrote the initial draft; T.M.K., P.S.S. and N.C. finalized the draft for submission.

Additional Information
Supplementary information accompanies this paper at https://doi.org/10.1038/s41598-018-21912-x.
Competing Interests: The authors declare no competing interests.
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