Factors associated with hepatitis B vaccination among men who have sex with men: a systematic review of published research

Abstract

This systematic review identified and synthesised evidence from published research regarding personal and environmental factors associated with hepatitis B virus (HBV) vaccination uptake among gay men and other men who have sex with men (MSM) in low prevalence, high-income countries. A systematic literature search identified 18 eligible papers that addressed factors potentially associated with HBV vaccination uptake among MSM, of which 16 reported research conducted in the US. Studies assessed possible associations between HBV vaccination among MSM and socio-demographic characteristics, behavioural and social-cognitive factors and indicators of health service access. Converging evidence was found for associations between HBV vaccination and younger age, gay self-identification, and not using alcohol and drugs; evidence suggests a lack of association between HBV vaccination and ethnicity. There was converging evidence for associations between HBV vaccination and social-cognitive factors, in particular knowledge, perceived vulnerability and perceived severity regarding HBV infection, and perceived barriers to HBV vaccination. Evidence further supported associations between HBV vaccination and indicators of health service access. While research regarding factors associated with HBV vaccination among MSM remains limited, the identified correlates of HBV vaccination among MSM provide important guidance for the development of health promotion interventions to effectively increase coverage of HBV vaccination among MSM.

Keywords

Gay men men who have sex with men hepatitis B virus vaccination barriers and facilitators social-cognitive factors health system factors

Introduction

With more than two billion people infected globally, hepatitis B virus (HBV) infection is one of the most serious and common infectious diseases.¹ About 350 million individuals worldwide live with a chronic HBV infection, and more than four million acute HBV infections are noted every year.¹ Prevalence of chronic HBV infection is labelled low (<2%) in the general population in high-income countries in North America, Western and Northern Europe and Oceania, in comparison to countries in East and South-East Asia and Sub-Saharan Africa, where prevalence is labelled high (>8%); prevalence of chronic HBV is intermediate (2–8%) in some Eastern European countries.¹ Although HBV endemicity is generally low in high-income countries, HBV prevalence is elevated among particular population groups, including gay men and other men who have sex with men (MSM), who make up 15–25% of people affected by HBV in the US alone.²

While there are few treatment options for HBV, a safe and effective vaccine has been available for more than 30 years to prevent HBV infection among susceptible people.³ Ten years after the HBV vaccine first became available, the World Health Organization recommended universal infant HBV vaccination.¹ Universal immunisation programmes can be effective in decreasing HBV incidence, and in the US incidence of HBV among infants decreased by 89% after implementation of the universal vaccination programme.⁴ Despite this success of universal immunisation programmes, some countries with low prevalence have not implemented universal vaccination programmes to prevent HBV in the population (e.g. the UK) or have initiated this only recently (e.g. The Netherlands). Instead or concurrently these countries maintain targeted programmes that provide HBV vaccination to selective population groups at increased risk, including MSM.⁵

A targeted programme providing free HBV vaccination was implemented in The Netherlands in 2002. A comprehensive evaluation of this programme is the first to show that targeted vaccination programmes can be effective.⁶ Notably, the incidence of reported acute HBV infections was found to have fallen from 1.8 per 100,000 inhabitants in 2004 to 1.2 in 2012, mostly due to a reduction in the number of cases among MSM.⁶ The Netherlands implemented a universal infant HBV vaccination programme only in 2011, based on a renewed assessment of cost-effectiveness and long-term population health benefits.⁷ In the absence of catch-up programmes, targeted vaccination of key affected population groups will have to be continued in parallel until these groups are protected through universal vaccination, which may take several decades.⁸ Coverage of targeted HBV vaccination remains however limited and less than 40% of MSM in Amsterdam who are susceptible to HBV infection are estimated to be fully protected.⁸ Several scenarios have been modelled to strengthen the impact of targeted HBV vaccination.⁹

To successfully promote targeted HBV vaccination among MSM it is critical to identify modifiable factors that shape vaccination behaviour in order to develop health promotion interventions that can effectively address these factors. According to the socio-ecologic perspective, a conceptual approach commonly used in health promotion to inform understanding of health behaviour and guide intervention development, the dynamic interrelations between individual and environmental factors play a critical role in health behaviour change.¹⁰ Individual level factors include demographic characteristics (e.g. age), behavioural factors (e.g. sexual risk taking), as well as social-cognitive factors (e.g. attitudes). The environmental level reflects all factors outside the individual, encompassing social factors (e.g. social support), cultural factors (e.g. values and norms), as well as system and political factors (e.g. health care access). We used this socio-ecological perspective to guide the synthesis of the available evidence regarding the multitude of individual and environmental factors examined in previous studies for possible associations with HBV vaccination uptake among MSM.

Knowledge of key factors possibly associated with HBV vaccination uptake is likely to provide insight into factors that are amenable to change,¹¹ and may guide future research, policy and the development of effective health promotion interventions to stimulate the uptake of HBV vaccination among MSM. To date, however, little attention has been given to synthesising the research evidence regarding factors that may affect HBV vaccination among MSM. An earlier systematic review identified several factors that were associated with HBV vaccination uptake among MSM,¹² including younger age, greater openness about one’s sexual identity, higher perceived risk of HBV infection and better access to health care. However, this review included only a small number of pertinent studies (k = 8).¹² To strengthen understanding of factors of HBV vaccination among MSM we conducted an updated and extended literature review and evidence synthesis, drawing on more and recent studies of factors possibly associated with HBV vaccination uptake among MSM. Taking a socio-ecologic perspective, the aim of the present literature review is to identify and synthesise evidence regarding the diversity of factors that may promote HBV vaccination among MSM in low prevalence, resource-rich countries.

Methods

Identification of relevant studies

The electronic databases PubMed, PsychINFO, Embase and Web of Science were searched for peer-reviewed publications reporting empirical studies of factors possibly associated with HBV vaccination uptake among MSM. All four databases were searched using combinations of the following keywords: HBV (and variants including viral hepatitis and hepatitis B infection); AND vaccination (and variants including vaccine and immunisation); AND MSM (and variants including homosexual men, gay men and bisexual men). The reference sections of all retrieved papers were examined to identify any additional studies. The literature search covered publications from inception of the database until February 2014. Empirical studies published in English that reported quantitative statistical analyses to assess factors possibly associated with HBV vaccination uptake among MSM in high-income countries were eligible for inclusion.

The literature search initially yielded 792 papers across databases (406 in PubMed; 170 in PsychINFO; 114 in Embase; 102 in Web of Science). After removal of 223 duplicates, the titles and abstracts of the remaining 569 papers were inspected to establish preliminary eligibility. Papers concerned with hepatitis A vaccination (k = 4) were excluded, as were papers reporting studies that addressed other infectious diseases (e.g. HIV; k = 70), that reported clinical research (k = 207), epidemiological studies (k = 42), intervention evaluation studies (k = 54), or on HBV vaccination policy (k = 86). Furthermore, we excluded papers (k = 75) that focused on population groups other than MSM (e.g. people who inject drugs), papers reporting qualitative research, and papers (k = 6) written in another language than English (e.g. German; k = 4). Papers with HBV vaccination intention (k = 2) or HBV vaccination completion as the sole outcome measure (k = 1) were also excluded. This screening procedure resulted in a final sample of 18 eligible papers, each reporting one study, that were included in the evidence synthesis (see Figure 1).^13–30

Assessment of methodological quality of included studies

Methodological quality of the included studies was assessed using a standardised tool developed by the National Institute for Health and Clinical Excellence.³¹ This tool is an established quality appraisal checklist consisting of 19 items to determine external and internal validity of the included papers.³¹ Three items specified criteria regarding external validity (e.g. description of the population; representation of the population), and 16 items specified various criteria regarding internal validity (e.g. theory-based selection of variables; assessment of outcome measures; appropriateness of the analytical methods). Each paper was awarded an overall methodological quality rating for internal validity and external validity, based on the average scoring of the pertinent checklist items: high (++), medium (+) or low internal/external validity (−).

Results

Details of the 18 included studies are depicted in Table 1. The majority of studies were conducted in the US (k = 16), and study sample sizes ranged from 35 to 1943 participants.^13,14 Nearly all studies (k = 17) had a cross-sectional design, and most (k = 12) used self-reported HBV vaccination status as outcome variable. One study had a prospective design and assessed vaccination uptake through data linkage with a HBV vaccination registry.¹⁵ Two studies assessed uptake of a vaccination offer,^16,17 and three studies used serological markers to assess HBV vaccination.^14,18,19 Two papers reported only bivariate analyses,^13,20 while most papers (k = 16) reported both bivariate and multivariate analyses. To ensure comparability of reported findings across studies, only the results of bivariate analysis are presented in this evidence synthesis. Studies were comparable with respect to methodological quality; most studies were rated as high or medium on the methodological quality appraisal.

Table 1.

Characteristics and methodological quality of the included studies (n = 18).

Study characteristics						Quality appraisal
Authors	Country	N eligible for HBV vaccination	Study design	Outcome variable	Data analysis	Sample and recruitment	Method of selection of exposure group	Validity of outcome measures	Appropriateness of the analytical methods
Neighbors et al.¹³	US	35	C	SR	B	++	+	+	−
Weinbaum et al.¹⁴	US	1943	C	SM	B/M	++	+	++	++
De Wit et al.¹⁵	NL	290	L	VR	B/M	+	++	++	++
Rudy et al.¹⁶	US	425	C	AV	B/M	++	++	+	++
Storholm et al.¹⁷	US	815	C	AV	B/M	++	+	++	++
Pitasi et al.¹⁸	US	157	C	SM	B/M	++	+	++	++
Diamond et al.¹⁹	US	368	C	SM	B/M	++	+	++	++
Ostrow et al.²⁰	US	194	C	SR	B	++	+	+	+
Rhodes et al.²¹	US	102	C	SR	B/M	+	−	−	+
Rhodes et al.²²	US	64	C	SR	B/M	++	+	+	+
Rhodes et al.²³	US	194	C	SR	B/M	++	+	+	+
Siconolfi et al.²⁴	US	98	C	SR	B/M	++	+	++	++
Gilbert et al.²⁵	US	519	C	SR	B/M	++	++	+	+
Matthews et al.²⁶	US	373	C	SR	B/M	++	+	+	++
Dufour et al.²⁷	CA	327	C	SR	B/M	++	+	++	+
Rhodes and Hergenrather²⁸	US	227	C	SR	B/M	++	++	+	++
Rhodes et al.²⁹	US	216	C	SR	B/M	++	++	+	++
Rhodes and Diclemente³⁰	US	83	C	SR	B/M	++	++	+	++

CA: Canada, NL: The Netherlands, US: United States of America, L: longitudinal, C: cross-sectional, SR: self-report, SM: serological markers, VR: vaccination registry; AV: acceptance of vaccination offer, B: bivariate analysis, M: multivariate analysis.

High (for that particular aspect of study design, the study has been designed/conducted to minimise the risk of bias.

Medium (either the information is not clear from the way the study is reported, or that study may not have addressed all potential sources of bias).

−

Low (in aspects of the study design significant sources of bias may persist).

Factors associated with HBV vaccination

We classified the various factors that were examined for possible association with HBV vaccination uptake among MSM in the included papers into three individual-level categories (i.e. socio-demographic characteristics, behavioural factors and social-cognitive factors), and one environmental-level category (i.e. health care access).¹⁰

Socio-demographic characteristics

As shown in Table 2, 10 of 14 studies found a significant association between HBV vaccination and younger age,^{15,16,18,19,21–26} one study found an opposite association,¹⁴ and three studies found no association.^13,20,27 Five of 10 studies found no significant association between HBV vaccination and socio-economic status,^{13,18,24,25,27} four studies found a significant positive association with higher socio-economic status,^14,20,21,26 and one study reported a negative association.¹⁶ Five of seven studies found no significant association between HBV vaccination and race/ethnicity,^{13,17,18,22,24} the other two papers reported that HBV vaccination was significantly associated with white race/ethnicity.^14,20 The one study that assessed an association between being in a regular relationship and vaccination uptake found a significant association.¹⁵

Table 2.

Evidence regarding factors potentially associated with HBV vaccination uptake among MSM.

	Direction of association^a	Study reference
Socio-demographic characteristics
Younger age	+	15,16,18,19,21–26
	−	14
	=	13,20,27
Higher socio-economic status	+	14,20,21,26
	−	16
	=	13,18,24,25,27
White ethnicity	+	14,20
	−
	=	13,17,18,22,24
Regular relationship	+	15
	−
	=
Behavioural factors
HIV+ status	+	14,21,24
	−
	=	18,20,23,27
Gay identity	+	14,15,20,21
	−
	=	24
Sexual risk-taking (e.g. high number of sexpartners, involvement in sex-trade, unprotected sex)	+	17,21,23,25,27
	−	15,16
	=	13,14,26
Use of alcohol and other drugs	+
	−	17,20,26,27
	=	14,18
Social-cognitive factors
Knowledge about HBV and HBV vaccination	+	19,22,23,25
	−
	=	16
Perceived vulnerability to HBV infection	+	15,16,19,28
	−
	=	29
Perceived severity of HBV infection	+	15,16,28–30
	−
	=
Perceived benefits of HBV vaccination	+	28
	−
	=	30
Perceived barriers to HBV vaccination	+
	−	15,16,29,30
	=	28
Attitude regarding HBV vaccination	+	15
	−
	=
Self-efficacy regarding HBV vaccination	+	28–30
	−
	=
Health care access
Having health insurance	+	21,24,25
	−
	=	18,26
Health care visits in the last 12 months	+	16,21,25,26
	−
	=
Ever tested for an STD/ diagnosed with an STD	+	16,25
	−
	=	14,18
Disclosure of sexual behaviour to health care provider	+	25–27
	−
	=
Ever exposed to health education	+	21–23
	−
	=
Ever received personal health advice	+	16,21–23,25,26,28
	−
	=	29,30

A significant positive association.

−

A significant negative association.

No significant association between factor and HBV vaccination uptake.

Behavioural factors

Four of seven studies found no significant association between HIV status and HBV vaccination,^18,20,23,27 the other three studies found a significant association with HIV-positive status.^14,21,24 Four of five studies found a significant association between identifying as gay and HBV vaccination,^14,15,20,21 the one other study found no significant association.²⁴ Five of 10 studies found a significant positive association between sexual risk-taking and HBV vaccination,^{17,21,23,25,27} two studies found a negative association,^15,16 and three studies found no significant association.^13,14,26 Four of six studies found a significant negative association between any alcohol or drug use and HBV vaccination uptake,^17,20,26,27 the two other studies found no significant association.^14,18

Social-cognitive factors

Four of five studies found a significant positive association between more knowledge of HBV and HBV vaccination and HBV vaccination uptake,^19,22,23,25 the other study found no association.¹⁶ Four of five studies found a significant positive association between higher perceived vulnerability to HBV infection and HBV vaccination,^15,16,19,28 the other study found no significant association.²⁹ All five studies found a significant positive association between HBV vaccination and perceived severity of HBV infection.^{15,16,28–30} One of two studies found a positive association between perceived benefits of HBV vaccination and HBV vaccination,²⁸ while the other study found no significant association.³⁰ Four of five studies found a significant negative association between perceived barriers to HBV vaccination and HBV vaccination uptake,^15,16,29,30 the other study found no significant association.²⁸ The one pertinent study that assessed a relation between attitude regarding HBV vaccination and HBV vaccination found a significant positive association.¹⁵ All three studies that assessed a relation between self-efficacy regarding HBV vaccination and HBV vaccination found a significant positive association.^28–30

Health service access

Three of five studies found a significant association between having health insurance and HBV vaccination,^21,24,25 the other two studies found no significant association.^18,26 Two of four studies found no significant association between having tested for an STD or being diagnosed with an STD and HBV vaccination uptake,^14,18 the other two studies found a significant association.^16,25 All studies that assessed health care visits in the last year (k = 4),^16,21,25,26 disclosure of sexual behaviour to a health care provider (k = 3),^25–27 and exposure to health education (k = 3),^21–23 found significant positive associations with HBV vaccination. Six of eight studies that reported receiving personal advice from a health service provider found a significant, positive association with HBV vaccination uptake,^{16,21–23,25,26,28} the other two studies found no significant association.^29,30

Discussion

Our systematic literature review of research assessing factors potentially associated with HBV vaccination among MSM identified 18 papers that met eligibility criteria. Drawing on a socio-ecological perspective, four categories of variables were distinguised at the personal and environmental levels: socio-demographic characteristics, behavioural factors, social-cognitive factors, and indicators of access to health care. Across studies, converging evidence was found for an association between younger age and HBV vaccination. With nine of 10 studies conducted in the US, this association may reflect US guidelines for universal infant and adolescent vaccination against HBV.² While it cannot be assumed that all MSM born after introduction of universal vaccination are vaccinated against HBV, findings suggest that, in countries with universal vaccination, efforts to promote HBV vaccination should in particular target MSM born before the introduction of such programmes. There is also converging evidence that substance using men are less likely to be vaccinated against HBV, underscoring the importance of efforts to increase awareness and offer HBV vaccination through alcohol and other drugs services, in particular health and community substance use services catering to MSM. In addition, there was converging evidence for the absence of an association among MSM between HBV vaccination and ethnicity. However, the samples of most of the reviewed studies were not ethnically diverse, and in nearly all studies participants predominantly had a Caucasian background (k = 16); only two studies were conducted with MSM of African-American background.^21,30

Converging evidence further suggests that men who self-identify as gay are more likely to be vaccinated against HBV. Gay men are possibly more aware and accepting of the risk of HBV infection, and more exposed to health education and health promotion campaigns to increase uptake and coverage of HBV vaccination than other MSM, including in community settings. Specific efforts may be required to reach out to non-gay identified MSM who would benefit from HBV vaccination. It is also prerequisite to create and ensure a safe and open health care environment that enables patients to disclose their sexual identity and/or sexual practices to a health care provider. Lack of such openness may constitute a formidable barrier to a health care provider’s awareness of patients’ specific health risks, and the absence of this important guide for health care may result in fewer recommendations to obtain HBV vaccination.³² Health care providers may need to be supported to proactively inquire about a clients sexual behaviour in a non-offensive and non-judgemental way.

All studies that assessed associations between HBV vaccination and social-cognitive factors included concepts from the Health Belief Model.^33,34 This theory posits that the extent to which an individual perceives to be susceptible to a particular disease or condition (e.g. HBV infection), and perceives this condition as severe will affect the likelihood that the individual engages in a given health behaviour (e.g. HBV vaccination). According to the health Belief Model, whether people enact a recommended health behaviour, such as HBV vaccination, is further influenced by people’s perceptions of the benefits and barriers related to the behaviour. In addition to more knowledge about HBV, there is converging evidence across studies included in this review for an association between HBV vaccination and three of four social-cognitive factors specified in the Health Belief Model: perceived risk of HBV infection, perceived severity of HBV infection, and perceived barriers to HBV vaccination (see below for a consideration of evidence regarding perceived benefits of HBV vaccination).

Perceiving a personal health threat is an important condition for protective health behaviour, but people generally tend to optimistically underestimate personal health risks.^35,36 Research from our group suggest that risk communication using a first-person testimonial may be effective in increasing risk perception for HBV among MSM.³⁷ Conceptualisations of perceived barriers of HBV vaccination varied across studies including having no time,^16,30 financial costs,^29,30 fear of getting a shot,²¹ and fear that one’s lifestyle becomes known.¹⁵ Interventions to stimulate HBV vaccination uptake among MSM can address practical barriers by informing MSM about HBV vaccination sites, operating hours of those sites and funding arrangements for HBV vaccination. Perceived barriers can also be addressed by stimulating health care professionals to provide MSM susceptible to HBV infection with information about the safety of the vaccine and to ensure the implementation of effective privacy policies at HBV vaccination sites. Furthermore, our research shows that perceived social barriers can be overcome by using role models in health communication, which proved to be an effective strategy to increase motivation to obtain HBV vaccination among MSM.³⁸

Converging evidence was also found for an association between HBV vaccination and some indicators of health care access. In particular, visits to a health care provider in the last 12 months and receiving personal advice on HBV from a health care provider were associated with being vaccinated against HBV. This underscores the importance of ensuring the accessibility of health care, making HBV vaccination available in a range of health care settings, and supporting health care providers to discuss HBV and recommend HBV vaccination to susceptible MSM. These findings also highlight the importance of active engagement with health care, and a good relationship and open communication between patients and their health care provider. As noted in the Health Belief Model, personal communication, as well as health education, about HBV and HBV vaccination can provide a cue to action for HBV vaccination.

Evidence regarding a possible association between HBV vaccination among MSM and socio-economic status, HIV status, sexual risk-taking, having health insurance and tested for an STD/diagnosed with an STD was mixed, potentially reflecting that indicators of these factors varied substantially across studies. Notably, socio-economic status was assessed by income²⁷ as well as educational level,^{13,14,16,18,20,21,24–27} and indicators of sexual risk behaviours included number of sexpartners,^{13–16,21,23,25,26} involvement in sex-trade,¹⁷ and unprotected sex.²⁷ Assessment of HIV status encompassed anti-HIV serology,¹⁴ and self-reported HIV status.^{18,20,21,23,24,27} Measures of having tested for an STD/diagnosed with an STD included tested for an STD,^18,25 and diagnosed with an STD.^14,16

Limited evidence was available to gauge a potential association between HBV vaccination and relationship status; only one study, using a prospective design,¹⁵ assessed and found an association between being in regular relationship and HBV vaccination uptake among MSM. There was also limited evidence available to assess potential associations between HBV vaccination and perceived benefits, attitude and self-efficacy regarding HBV vaccination. One of only two relevant studies found perceived benefits to be associated with HBV vaccination uptake among MSM,²⁸ while the other study did not find such association.³⁰ One, prospective, study assessed and found an association between HBV vaccination and a positive attitude regarding HBV vaccination.¹⁵ Only three studies assessed, and found, a positive association between HBV vaccination and higher self-efficacy regarding HBV vaccination among MSM. Furthermore, there was limited evidence to appraise associations between HBV vaccination and disclosure of sexual behaviour to a health care provider, and exposure to health education about HBV vaccination. For each of these factors we identified three pertinent studies which reported findings supporting associations.

Limitations

Although the methodical quality of most of the reviewed studies was appraised as medium or high based on the applied checklist,³¹ there are several limitations to the identified and synthesised set of studies. The majority of studies had a cross-sectional design, which limits to possibility to draw conclusions regarding direction of causality; only one study, by our own group,¹⁵ employed a prospective design. Most studies consisted of samples of mainly white MSM which limits external validity and generalisability of findings to other ethnic groups. Generalisability of most studies was also affected by the recruitment of convenience samples. Studies were predominantly conducted in the US, and findings may not apply to high-income countries with different health systems.

A further limitation is that sample size differed widely across the included studies, resulting in differences in statistical power to asses associations. Furthermore, the majority of studies assessed self-reported HBV vaccination status as outcome variable, which may differ from objective indicators.¹⁸ Notably, individuals may not correctly recall whether they obtained vaccination or not, they may confuse hepatitis B vaccination with hepatitis A vaccination, and social desirability bias may influence the accuracy of self-reported HBV vaccination status. Only few studies used objective indicators of HBV vaccination, such as linkage with a vaccination registry,¹⁵ serological markers,^14,18,19 or acceptance of a vaccination offer.^16,17

Conclusions

The body of research assessing factors associated with HBV vaccination among MSM in low prevalence, high-income countries remains limited. Nevertheless, the results of this systematic review and evidence synthesis provide valuable guidance for the development of health promotion interventions to increase coverage of HBV vaccination. The available evidence suggests that HBV vaccination promotion among MSM should in particular target older men (including men not reached by universal infant and child HBV vaccination programmes), non-gay identified MSM, and substance-using MSM. HBV vaccination promotion interventions are likely to be most effective if they address social-cognitive factors that are amenable to change, with converging evidence underscoring the importance of addressing perceived personal risk of HBV infection, and perceived barriers to HBV vaccination. Furthermore, coverage of HBV vaccination may benefit from health promotion approaches facilitating access to HBV vaccination.

Footnotes

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was supported by a grant from the Netherlands Organization for Health Research and Development (ZonMw; grant number 23000032) to the second author. The funder had no involvement in the study design; the collection, analysis and interpretation of data; the writing of the report and the decision to submit this article for publication.

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