Cover of Increasing uptake of hepatitis A, hepatitis B and human papillomavirus (HPV) vaccinations in gay, bisexual and other men who have sex with men

Increasing uptake of hepatitis A, hepatitis B and human papillomavirus (HPV) vaccinations in gay, bisexual and other men who have sex with men

Reducing sexually transmitted infections (STIs)

Evidence review F

NICE Guideline, No. 221

London: National Institute for Health and Care Excellence (NICE); .
ISBN-13: 978-1-4731-4612-9
Copyright © NICE 2022.

1. Effective and cost-effective interventions to increase uptake of vaccinations in men who have sex with men

1.1. Review question

What interventions are effective and cost effective at increasing uptake of hepatitis A, hepatitis B or human papillomavirus (HPV) vaccination in gay, bisexual and other men who have sex with men (MSM)?a

1.1.1. Introduction

Sexually transmitted infections (STIs) include a range of clinical syndromes that can be acquired and transmitted through sexual activity and may be caused by various types of pathogens, including bacteria, fungi, viruses, and parasites. It can affect personal wellbeing, mental health and relationships and can also lead to serious health problems including pelvic inflammatory disease, ectopic pregnancy or infertility. Preventive interventions can reduce the spread of infection and avoid complications and consequences.

From 1st April 2018 there has been a national HPV vaccination programme for men who have sex with men. This offers the vaccine to those aged up to and including 45-years-old through Specialist Sexual Health Services (SSHS) and/or HIV clinics. A pilot conducted in 2016/17 and using data from the GUMCAD and HARS reporting systems found first dose uptake was 45.5% (3.4% were offered and declined the vaccine, and 50.9% had no vaccination code), though this was expected to be an underestimate of true uptake due to variations in data recording. Uptake rates following the full introduction of the programme are not yet available for England, but a similar programme in Scotland had an uptake of 63.7% among eligible MSM attending sexual health clinics in 2017/18.

Since June 2017, it has been recommended that all men who have sex with men attending HIV, GUM or sexual health clinics should be opportunistically offered vaccination against hepatitis A. There are currently no published national data on uptake rates for this vaccination.

1.1.2. Summary of the protocol

Table 1. PICO inclusion criteria.

Table 1

PICO inclusion criteria.

1.1.3. Methods and process

This evidence review was developed using the methods and process described in Developing NICE guidelines: the manual. Methods specific to this review question are described in the review protocol in Appendix A and the methods document.

Declarations of interest were recorded according to NICE’s conflicts of interest policy.

1.1.4. Identification of public health evidence

The effectiveness and qualitative reviews were carried out using a single literature search (Appendix B). 858 references were identified for title and abstract screening and 81 quantitative papers were ordered for full-text review. Of these, 3 RCTs met the inclusion criteria for the effectiveness review, as outlined in the review protocol. 78 studies were excluded. See Appendix C for a PRISMA flow diagram of the study selection process.

1.1.4.1. Included studies

Of the 3 RCTs included for the effectiveness review, 1 study was conducted in the Netherlands and two in the USA. 1 study reported on hepatitis B vaccination uptake and the other two studies reported on HPV vaccination uptake. See Table 2 for included study details for the effectiveness review.

1.1.4.2. Excluded studies

The full list of excluded studies and reasons for exclusion are in Appendix J.

Table 2. Summary of studies included in the effectiveness evidence review.

Table 2

Summary of studies included in the effectiveness evidence review.

See Appendix D for full evidence tables.

1.1.5. Summary of the effectiveness evidence

Table 3. Summary of findings table.

Table 3

Summary of findings table.

See appendix F for full GRADE Tables.

1.1.6. Economic evidence

A search for relevant economic studies was undertaken, using the strategy in appendix B and applying a cost-effectiveness filter. 146 references were identified from this literature search; all of which were excluded during title and abstract screening. As such, no economic studies were included to inform this review question.

1.1.7. Economic model

No economic modelling was undertaken for this review question.

2. Barriers and facilitators for increasing uptake of vaccines in men who have sex with men

2.1. Review question

What are the barriers to, and facilitators for, increasing uptake of hepatitis A, hepatitis B or human papillomavirus (HPV) vaccinations in men who have sex with men?

2.1.1. Introduction

Current practice recommends that men who have sex with men attending HIV, GUM or sexual health clinics should be opportunistically offered vaccination against hepatitis A and there is a national HPV vaccination programme for men who have sex with men aged up-to and including 45 years attending Specialist Sexual Health Services (SSHS) and/or HIV clinics. Data on vaccine uptake rates are not available but strategies for improving uptake are important as vaccinations against hepatitis A, hepatitis B and HPV are important STI prevention strategies. The purpose of this review is to establish the barriers to, and facilitators for, vaccine uptake in MSM.

2.1.2. Summary of the protocol

Table 4. PICO inclusion criteria.

Table 4

PICO inclusion criteria.

For the full review protocol see appendix A.

2.1.3. Methods and process

This evidence review was developed using the methods and process described in Developing NICE guidelines: the manual. Methods specific to this review question are described in the review protocol in appendix A and the methods document.

Declarations of interest were recorded according to NICE’s conflicts of interest policy.

2.1.4. Identification of qualitative evidence

The effectiveness and qualitative reviews were carried out using a single literature search (Appendix B). 858 references were identified for title and abstract screening and 18 qualitative papers were ordered for full-text review. Of these, 9 qualitative studies reported in 10 papers met the inclusion criteria for the qualitative review, as outlined in the review protocol. 8 studies were excluded.

2.1.4.1. Included studies

Of the 9 qualitative studies included in the qualitative review, 1 study was conducted in Canada, 2 in the United Kingdom, and 6 in the USA. All studies reported on the barriers to, facilitators for, or acceptability of HPV vaccine. Studies reported individual, provider and system level barriers, facilitators or acceptability. See Table 5 for included study details.

2.1.4.2. Excluded studies

The full list of excluded studies and reasons for exclusion are in Appendix J.

Table 5. Summary of studies included in the qualitative evidence review.

Table 5

Summary of studies included in the qualitative evidence review.

See Appendix D for full evidence tables

2.1.5. Summary of the qualitative evidence

2.1.5.1. Summary of themes and sub-themes

Iterative aggregation of codes generated two main themes and 10 sub-themes. These are outlined in Table 6.

Table 6. Summary of themes and sub-themes.

Table 6

Summary of themes and sub-themes.

2.1.5.2. Summary of qualitative findings

The qualitative findings for the barriers to and facilitators for HPV vaccination in MSM are presented in Table 7. Full CERQual tables are presented in Appendix G.

Table 7. Summary of qualitative findings.

Table 7

Summary of qualitative findings.

3. Integration and discussion of the evidence

3.1. Mixed methods integration

Are the results/findings from individual syntheses supportive or contradictory?

The effectiveness evidence showed that text-messaging based interventions designed to increase vaccine uptake were effective at increasing HPV vaccine initiation MSM. Similarly, an intervention focusing on implementation intention formation (prompting participants to consider ways to implement their intentions to get vaccinated by thinking about when, where and how they would obtain hepatitis B vaccine) was effective at increasing hepatitis B vaccine initiation in MSM. The text-messaging based interventions were not effective in supporting HPV vaccine completion and there were no studies that examined hepatitis B vaccine completion.

The qualitative evidence generated themes that showed a lack of information about HPV, HPV-related disease, and the HPV vaccine was a barrier to vaccination in MSM. This supports findings from the effectiveness review because the interventions that were effective at increasing vaccination initiation included information-based components that educated people about HPV and HPV-related disease.

Does the qualitative evidence explain why the intervention is/is not effective?

The qualitative evidence highlighted lack of knowledge about HPV as a barrier to vaccination, particularly relating to the widespread perception that HPV is something that only affects cisgender women. It also showed vaccine hesitancy, uncertainty about vaccine effectiveness and concerns about side effects were barriers to vaccination. Interventions that provided information about HPV, the vaccine, how it works, and potential side effects were effective in improving vaccine initiation, which suggests that the interventions were effective because they filled knowledge gaps or allayed fears about the vaccine that were acting as barriers to initial vaccine uptake.

The qualitative evidence suggested that some of the barriers to vaccination completion were related to the need for multiple doses, the long time intervals between doses, and the potential inconvenience of having to schedule appointments around other commitments. The effectiveness evidence showed that vaccine completion rates were generally very low in both the intervention and control arms (range 1.3% to 11%) and the text messaging based interventions were not effective in improving HPV vaccine course completion. The interventions may not have been effective because they focused more on information, motivation and behaviour needs rather than addressing issues relating to scheduling and appointment flexibility. Nevertheless, the interventions did include regular text or email reminders which still did not appear to be effective at facilitating vaccine course completion.

Does the qualitative evidence explain differences in the direction and size of effect across the included quantitative studies?

Quantitative findings for interventions to increase both HPV vaccine initiation and completion had relatively wide confidence intervals, indicating some uncertainty in the estimate of effect. This uncertainty may be partly explained by the qualitative findings because they identified a range of different barriers to, and facilitators for, vaccination. Different people may require different support from interventions to overcome personal barriers and encourage them to obtain vaccination, so digital interventions that focused primarily on information, motivation and behavioural needs may be effective for some, but not all people, contributing to the wide confidence intervals seen in the quantitative evidence.

Which aspects of the quantitative evidence were/were not explored in the qualitative studies?

The quantitative evidence included interventions that focused on intention formation implementation and how to move people from considering vaccination to making a specific plan to obtain it. The qualitative evidence looked more broadly at person- and system-level factors that may act as barriers or facilitators to vaccination, rather than individual approaches to supporting people in making behavioural changes that encouraged vaccination. The quantitative evidence also assessed the effectiveness of text- and email-based interventions while the qualitative evidence only considered app-based approaches for booking appointments and creating a reminder system and did not explore the potential barriers and facilitators for text messaging-based interventions.

Which aspects of the qualitative evidence were/were not tested in the quantitative studies?

The qualitative evidence highlighted themes relating to health care professionals and their role in supporting people to obtain vaccination. Specific themes included the importance of HCPs being open, accepting, and non-judgemental; that HCPs were considered to be the most trusted source of information about vaccination; and that recommendations from HCPs were seen as something that would substantially influence people’s decision to obtain the vaccine. Findings from the qualitative evidence also showed that people wanted vaccinations to be offered during other routine interactions with HCPs such as general sexual health checks or STI testing. The quantitative evidence did not examine the role of health care practitioners and did not evaluate the efficacy of offering vaccinations during other clinical interactions.

3.2. The committee's discussion and interpretation of the evidence

The qualitative and quantitative reviews are presented as a combined discussion.

3.2.1. The outcomes that matter most

The committee discussed the evidence and agreed that vaccine uptake is the most important outcome, but also emphasised the importance of vaccine course completion. They agreed that both vaccine initiation and vaccine course completion should be considered together.

The committee discussed and agreed on the importance of considering the barriers to or facilitators for vaccine uptake and completion, described by those who are likely to benefit from having vaccines, that may have substantial impact on the effectiveness of any intervention that aims to increase vaccine uptake.

The committee considered it important that gay, bisexual and other men who have sex with men are aware of, and able to easily access, HPV, Hepatitis A and Hepatitis B vaccinations. Particularly in relation to HPV they noted that many people in this group will not have been included in the school’s vaccination programme that has now been expanded to include boys. In future this group will have been offered vaccination at school, but currently this group have not been included as the vaccination programme did not initially include boys.

3.2.2. The quality of the evidence

Quantitative evidence

The committee discussed the lack of evidence on vaccine uptake in gay, bisexual and other men who have sex with men, with only 3 studies identified: two for HPV and one for Hepatitis B vaccination. They noted that there were some methodological concerns about these included papers because of the lack of detail provided about the randomisation methods used and on allocation concealment methods. They further noted that the studies had not specified the number of vaccine doses offered.

The committee discussed the evidence and noted that the interventions had a positive impact on HPV vaccine initiation but not on HPV vaccine completion. It was also noted that the finding for HPV vaccine completion had a very wide confidence interval, suggesting a high degree of imprecision for this outcome. The committee agreed that the evidence was useful in drafting recommendations on vaccine initiation and agreed that while there was a lack of evidence for interventions to encourage vaccine completion, it was important to also make recommendations about this because people need to have both doses of the vaccine to be fully protected. This absence of evidence prompted the committee to make a qualitative research recommendation on the barriers to HPV vaccine course completion and how people think they might be encouraged to complete it.

The committee highlighted that while the 7- and 9-month follow ups described in the two trials fit with the recommended HPV vaccine course of doses at 0, 1 and 4 months, in practice doses are often more widely spaced and, in some clinics, at least a year is allowed to complete the full course. The committee therefore considered that 7- and 9-month follow-up periods were a relatively short timeframe for people to complete the vaccine doses and this may have contributed to the lack of effect for this outcome.

The committee discussed the evidence showing an effect of motivational information and implementation intention formation activities on improving Hepatitis B vaccine uptake, though it was not clear from the study what the vaccination schedule was or whether participants completed their course. As noted previously, the committee considered vaccine completion to be important so this was acknowledged as a limitation of the applicability of this evidence. The committee also noted that drop out was 25% higher in the intervention group than the control group, although attrition analyses found no significant differences between participants in the experimental and control groups, or between completers and those lost to follow-up, indicating that attrition was not selective. The committee discussed the limited evidence for specific interventions that aim to improve vaccine uptake. They considered that there was not sufficient evidence to specifically recommend any of the included interventions, but they recognised the importance of including vaccination information within healthcare and specifically sexual health services that gay, bisexual and other men who have sex with men use. They noted that even though the evidence alone was insufficient, with the broader experience and expertise of the committee members, they were able to make recommendations about the importance of opportunistically providing information on and discussing vaccination with gay, bisexual and other men who have sex with men during routine or other healthcare appointments.

The committee noted the NICE guidance on behaviour change: individual approaches and noted that the recommendations about behaviour change techniques that could be effective may be useful when thinking about approaches to improving vaccine uptake.

Qualitative evidence

Evidence addressing barriers to and facilitators for increasing uptake of vaccination in gay, bisexual and other men who have sex with men was only identified for HPV vaccination. Nonetheless, the committee discussed and agreed that many of the identified themes for both barriers and facilitators identified for HPV vaccination for gay, bisexual and other men who have sex with men are also applicable to the other vaccines. These include barriers such as those around the approachability of healthcare staff for gay, bisexual and other men who have sex with men, the need for clear information about vaccines and the possible provision of vaccines as part of other healthcare visits. The committee discussed the identified barriers including a general lack of knowledge about HPV and HPV related diseases and vaccines; and concerns about vaccine effectiveness and potential side effects. Additional barriers included possible stigma or concerns about having discussions with healthcare professionals and the impact of previous negative experiences of this; and some potential difficulties with the scheduling of vaccines. The committee also discussed the identified facilitators including increasing knowledge and awareness of the benefits of getting vaccines, the influence of the views of healthcare providers on vaccination decisions, the possibility of vaccinations being offered during routine sexual health or other healthcare visits.. The Committee agreed that the themes identified were similar to those that they had expected and reflected their expertise and clinical experience.

The committee discussed the qualitative evidence in combination with the findings from the quantitative review and noted that the qualitative evidence supported the importance of discussing vaccination opportunistically. They also discussed the evidence that noted that there can be a misconception that HPV only has relevance for cisgender females and that the link with male cancers may not be widely known. The committee considered that this misconception also supports the recommendation for opportunistic discussion as it may be that gay, bisexual and other men who have sex with men do not know that the vaccination is relevant for them.

The evidence identified that there are ongoing concerns for gay, bisexual and other men who have sex with men around the perceived approachability of healthcare staff and this affects whether or not they are comfortable discussing their sexual history. The committee further discussed and agreed that gay, bisexual and other men who have sex with men need to feel confident discussing their healthcare needs, concerns, and sexual history with healthcare professionals without any apprehension about a negative reaction or stigma. The committee agreed that healthcare settings need to adopt approaches that will signal to gay, bisexual and other men who have sex with men that healthcare providers will support and facilitate these important discussions. They discussed programmes such as the ‘You’re Welcome’ quality criteria, which lays out key principles that help health services to be young people friendly, and considered how similar approaches could be used for gay, bisexual and other men who have sex with men to provide assurance to those using the services that it is designed with their needs in mind.

The committee discussed accessibility of vaccination appointments and the possibility of combining this with other healthcare visits. The qualitative evidence suggested that ensuring flexibility about when vaccines are given and reducing the number of visits by combining vaccines or combining vaccination with other healthcare visits may improve uptake. The committee agreed to recommend that services consider ways they can do this. The committee noted that one study identified the possible use of mobile apps for booking appointments and reminding people about them. They agreed that this is already current practice and approaches like this are already in use.

3.2.3. Benefits and harms

The committee agreed that improving vaccine uptake and completion in gay, bisexual and other men who have sex with men is beneficial. They noted that there is a widespread misconception that the HPV vaccine is only important for cisgender women and that the link with male cancers is not known, so correcting this misconception is important. The committee also recognised that there are people who consider vaccines harmful, and that many gay, bisexual and other men who have sex with men do not consider vaccination important, so providing clear information about the benefits and harms of HPV, Hepatitis A and Hepatitis B vaccines is important. The quantitative and qualitative evidence did not identify any harms of HPV and hepatitis B vaccinations.

3.2.4. Cost effectiveness and resource use

No economic evidence was identified for this review question. Nevertheless, the committee discussed the potential cost-effectiveness and resource impact of the recommendations made. They agreed that the recommendations on providing information and opportunistically assessing eligibility for vaccination should reflect current practice, and therefore did not consider that there would be a substantial resource impact associated with implementing them.

Combining vaccinations alongside other routine healthcare (either care around sexual health or more general healthcare) would be expected to increase rates of vaccination and be a more efficient and therefore less costly method of providing vaccination, as the person does not need an additional separate appointment solely for the purpose of delivering the vaccination. The committee noted such an approach would not be suitable for all vaccine eligible men but would be a cost-effective approach for those it can be delivered to.

It was also noted that because these vaccines had already been assessed as being cost-effective by the Joint Committee on Vaccination and Immunisation, an increase in the number of people being vaccinated should also be cost-effective.

3.3. Recommendations supported by this evidence review

This evidence review supports recommendations 1.4.1 to 1.4.4 and the research recommendation on barriers to vaccination course completion.

3.4. References – included studies

    3.4.1. Effectiveness

    • Bass Michael, Gerend Mary A., Madkins Krystal et al (2021) Evaluation of a Text Messaging-Based Human Papillomavirus Vaccination Intervention for Young Sexual Minority Men: Results from a Pilot Randomized Controlled Trial. Annals of behavioral medicine: a publication of the Society of Behavioral Medicine 55(4): 321–332 [PMC free article: PMC8025080] [PubMed: 32914838]

    • Reiter Paul L, Katz Mira L, Bauermeister Jose A et al (2018) Increasing Human Papillomavirus Vaccination Among Young Gay and Bisexual Men: A Randomized Pilot Trial of the Outsmart HPV Intervention. LGBT health 5(5): 325–329 [PMC free article: PMC6034390] [PubMed: 29979642]

    • Vet Raymond; de Wit John B F; Das Enny (2014) The role of implementation intention formation in promoting hepatitis B vaccination uptake among men who have sex with men. International journal of STD & AIDS 25(2): 122–9 [PubMed: 24216031]

    3.4.2. Qualitative

    • Apaydin Kaan Z, Fontenot Holly B, Shtasel Derri et al (2018) Facilitators of and barriers to HPV vaccination among sexual and gender minority patients at a Boston community health center. Vaccine 36(26): 3868–3875 [PMC free article: PMC5990434] [PubMed: 29778516]

    • Fontenot Holly B, Fantasia Heidi C, Vetters Ralph et al (2016) Increasing HPV vaccination and eliminating barriers: Recommendations from young men who have sex with men. Vaccine 34(50): 6209–6216 [PubMed: 27838067]

    • Gerend M.A., Madkins K., Crosby S. et al (2019) A Qualitative Analysis of Young Sexual Minority Men's Perspectives on Human Papillomavirus Vaccination. LGBT health 6(7): 350–356 [PMC free article: PMC6797075] [PubMed: 31556791]

    • Grace Daniel, Gaspar Mark, Paquette Rachelle et al (2018) HIV-positive gay men's knowledge and perceptions of Human Papillomavirus (HPV) and HPV vaccination: A qualitative study. PloS one 13(11): e0207953 [PMC free article: PMC6264470] [PubMed: 30496221]

    • Jaiswal Jessica, LoSchiavo Caleb, Maiolatesi Anthony et al (2020) Misinformation, Gendered Perceptions, and Low Healthcare Provider Communication Around HPV and the HPV Vaccine Among Young Sexual Minority Men in New York City: The P18 Cohort Study. Journal of community health 45(4): 702–711 [PMC free article: PMC7774381] [PubMed: 32016677]

    • Kesten J.M., Flannagan C., Ruane-Mcateer E. et al (2019) Mixed-methods study in England and Northern Ireland to understand young men who have sex with men's knowledge and attitudes towards human papillomavirus vaccination. BMJ Open 9(5): e025070 [PMC free article: PMC6530382] [PubMed: 31092645]

    • Koskan Alexis M and Fernandez-Pineda Madeline (2018) Human Papillomavirus Vaccine Awareness Among HIV-Positive Gay and Bisexual Men: A Qualitative Study. LGBT health 5(2): 145–149 [PMC free article: PMC5833245] [PubMed: 29412771]

    • Koskan Alexis M and Fernandez-Pineda Madeline (2018) Anal Cancer Prevention Perspectives Among Foreign-Born Latino HIV-Infected Gay and Bisexual Men. Cancer control: journal of the Moffitt Cancer Center 25(1): 1073274818780368 [PMC free article: PMC6028166] [PubMed: 29925247]

    • Nadarzynski Tom, Smith Helen, Richardson Daniel et al (2017) Perceptions of HPV and attitudes towards HPV vaccination amongst men who have sex with men: A qualitative analysis. British journal of health psychology 22(2): 345–361 [PubMed: 28191723]

    • Wheldon C.W., Daley E.M., Buhi E.R. et al (2017) HPV vaccine decision-making among young men who have sex with men. Health Education Journal 76(1): 52–65

Appendices

Appendix A. Review protocols

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Appendix B. Literature search strategies

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Appendix C. Public health evidence study selection

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Appendix D. Effectiveness evidence

D.1. Quantitative evidence

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D.2. Qualitative evidence

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Appendix E. Forest plots

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Appendix F. GRADE tables

F.1. Human papillomavirus vaccination initiation

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F.2. Human papillomavirus vaccination completion

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F.3. Hepatitis B vaccination uptake

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Appendix G. GRADE CERQual Tables

G.1. CERQual: Barriers to increasing uptake of HPV vaccinations in gay, bisexual and other men who have sex with men (MSM)

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G.2. CERQual: Facilitators for increasing uptake of HPV vaccinations in gay, bisexual and other men who have sex with men (MSM)

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Appendix H. Economic evidence study selection

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Appendix I. Economic evidence tables

No economic evidence was identified for this review question

Appendix J. Health economic model

No economic modelling was undertaken for this review question

Appendix K. Excluded studies

Appendix L. Research recommendations – full details

L.1. Research recommendation

What are the barriers to completing the full course of hepatitis A and B or HPV vaccinations and how do people think they might be encouraged to complete it?

L.2. Why this is important

The committee discussed the lack of evidence for interventions to facilitate vaccine completion for gay, bisexual and other men who have sex with men and emphasised the importance of people having all doses of the vaccine to be fully protected. They agreed that both the quantitative and qualitative evidence focused largely on vaccine initiation so there was an evidence gap relating to vaccine completion. They considered that understanding the barriers to vaccine course completion would help to support eligible gay, bisexual and other men who have sex with men to have all vaccine doses to obtain full protection.

L.3. Rationale for research recommendation

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Footnotes

a

Throughout this review, the term men who have sex with men (MSM) is used to refer to gay, bisexual and other men who have sex with men