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Original research
Hepatitis A vaccine uptake among men who have sex with men from a time-limited vaccination programme in Melbourne in 2018
  1. Sam Burrell1,2,
  2. Lenka A Vodstrcil1,2,
  3. Christopher K Fairley1,2,
  4. Alex Kilner1,3,
  5. Catriona S Bradshaw1,2,
  6. Marcus Y Chen1,2,
  7. Eric P F Chow1,2
  1. 1 Melbourne Sexual Health Centre, Alfred Health, Carlton, Victoria, Australia
  2. 2 Central Clinical School, Monash University, Melbourne, Victoria, Australia
  3. 3 Melbourne Medical School, The University of Melbourne, Melbourne, Victoria, Australia
  1. Correspondence to Associate Professor Eric P F Chow, Melbourne Sexual Health Centre, Alfred Health, Carlton, Victoria 3053, Australia; eric.chow{at}monash.edu

Abstract

Objectives In 2017, an outbreak of hepatitis A among gay, bisexual and other men who have sex with men (MSM) was reported in Victoria, Australia. In 2018, the Victorian government implemented a free hepatitis A vaccination programme targeting all Victorian MSM. This study aimed to determine hepatitis A vaccine uptake among MSM in a sexual health clinic in Melbourne.

Methods All MSM attending the Melbourne Sexual Health Centre (MSHC) in 2018 were included. Chart review was performed to determine the proportion of men vaccinated for at least one dose of hepatitis A and to examine why men did not receive the vaccine. Multivariable logistic regression was performed to examine the factors associated with vaccine uptake. Vaccine uptake was defined as receipt of at least one dose of hepatitis A vaccine.

Results Of the 9582 MSM who attended MSHC in 2018, 61.3% (95% CI 60.3% to 62.2%) self-reported already being immune to hepatitis A. Of the 3713 remaining eligible men, 62.7% (95% CI 61.1% to 64.2%) received at least one dose of the hepatitis A vaccine on the day of attendance. Compared with MSM not living with HIV and not taking pre-exposure prophylaxis (PrEP), MSM taking PrEP (adjusted OR 1.28; 95% CI 1.01 to 1.62) were more likely to receive the vaccine. 1386 men (37.3%) did not receive the vaccine and 55.4% were not offered the vaccine by their treating clinician. 300 men (21.6%) were identified as non-immune after serological testing but did not return for vaccination. By the end of 2018, 85.5% of MSHC attendees (8196/9582) were immune to hepatitis A.

Conclusion The critical vaccination threshold for hepatitis A has been estimated at >70%. Continuation of the targeted hepatitis A vaccination programme will improve immunity among the MSM population to prevent ongoing transmission and the likelihood of future outbreaks.

  • vaccine
  • prevention
  • behaviours
  • public health
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Introduction

Hepatitis A virus (HAV) is one of the most common causes of acute hepatitis globally. According to the World Health Organization, it resulted in 13.7 million illnesses and 28 000 deaths worldwide in 2010.1 HAV is transmitted though the faecal–oral route, either through ingestion of contaminated food or water, or among gay, bisexual and other men who have sex with men (MSM) through sexual contact.

In many low-income and middle-income regions, acquisition of HAV during childhood is common with acquired immunity to the virus during adulthood. However, in countries with a low prevalence of HAV (eg, Australia), there is a low incidence of childhood infection and passive immunisation and thus there are a large proportion of susceptible adults.2 This allows for the occurrence of outbreaks, which particularly affect populations that are at higher risk such as MSM, intravenous drug users and international travellers.3

Outbreaks of HAV among MSM have been reported in Australia as well as many high-income countries such as the UK, the USA, France and the Netherlands since 2016.4–6 In Victoria, Australia, an outbreak of HAV (including one confirmed death) was identified in 2017, and most cases were local MSM who had not travelled overseas.7 In previous outbreaks in other countries, some governments have initiated a targeted HAV vaccination programme for MSM, which proved efficacious at increasing immunity and reducing infection rates.8 9

In January 2018, the Victorian Department of Health and Human Services (DHHS) funded a free HAV vaccination programme targeting all MSM living in Victoria, Australia. All MSM in Victoria were eligible for the two-dose course of hepatitis A vaccine (Havrix 1440; GlaxoSmithKline), with the second dose given 6–12 months after the first dose.7 At the same time, the Victorian DHHS began to offer free meningococcal ACWY (Menactra; Sanofi) and human papillomavirus (HPV) (Gardasil; Merck & Co.) vaccines for eligible MSM, while an existing hepatitis B vaccination programme continued.7 10 The ‘Little Pricks’ campaign was launched in 2018 to increase the uptake of all four vaccines in MSM in Victoria, which was run by the Victorian DHHS in partnership with a community-based organisation Thorne Harbour Health (formerly Victorian AIDS Council).

The primary aim of this study was to examine the uptake of the HAV vaccine among MSM attending a major sexual health clinic in Melbourne, Victoria after the implementation of the targeted time-limited HAV vaccination programme across Victoria. The secondary aim was to explore factors and barriers that were associated with the hepatitis A vaccine uptake among MSM.

Methods

This was a retrospective cohort study of MSM of aged 16 years and older attending the Melbourne Sexual Health Centre (MSHC) between 22 January 2018 and 31 December 2018. MSHC is the largest sexual health centre in Victoria, Australia, with approximately 50 000 consultations per year and 40% of clients attending MSHC self-identify as having had sex with another man in the past 12 months.11

MSHC uses electronic medical records containing information on medical history, demographics, immunisation status and medications. Information on demographics and sexual history is collected through a computer-assisted self-interview, which collects data on patient demographics (eg, age, country of birth), sexual practices (eg, current sex work, number of male partners in the past 12 months and condom use with male partners in the past 12 months), HIV status, current use of pre-exposure prophylaxis (PrEP) and use of intravenous drug in the past 12 months. Missing data were categorised into the ‘unknown’ category.

From 22 January 2018, MSHC began to offer a two-dose course of hepatitis A vaccine free of charge to all eligible MSM as part of the government-funded vaccination programme in Victoria. All MSM who live/reside in Victoria were eligible for the vaccine, with no age restriction.

Prior to the introduction of the programme, all clinicians at MSHC were advised and educated on the details of the programme and encouraged to offer the vaccine to all eligible MSM. Additional reminders and updates occurred throughout the year. Posters were located in some clinic rooms and the waiting room which advertised the free programme as part of the State-wide ‘Little Pricks’ campaign. Clinicians offered the hepatitis A vaccine to all eligible men who had not previously received the vaccine. For the purpose of the present study, we defined MSM who reported (either self-reported or as previously entered in the electronic medical record at a prior consult) having previously been vaccinated against hepatitis A were not ‘eligible’ to receive the free hepatitis A vaccine because these men did not require vaccination and were unlikely to be offered the vaccine by their clinician based on their medical history. This was determined by either self-reporting by clients or via the computer Clinical Practice Management System (CPMS), which records the hepatitis A vaccination status. Some clinicians offered the vaccine to clients without first testing immunity, while other clinicians would first order hepatitis A serology to determine status and, if negative, offer the vaccine on the next visit.

Frequency and proportion of MSM who received at least one dose of the hepatitis A vaccine at any consultation throughout 2018 were calculated. Vaccine uptake was defined as receipt of at least one dose of hepatitis A vaccine. A retrospective chart review was performed to collect information on the barriers and reasons among clients who did not receive or decline the vaccine. Univariable and multivariable logistic regression was performed to identify the factors associated with the hepatitis A vaccine uptake among MSM. All variables with p value <0.10 in the univariable analyses were selected and included into the final multivariable logistic regression model. The 0.05 level was used for statistical significance in the multivariable logistic regression model. All statistical analyses were conducted using SPSS V.25.

Results

There were 9582 MSM who attended MSHC at least once between 22 January 2018 and 31 December 2018, of whom 61.3% (n=5869, 95% CI 60.3% to 62.2%) were reported (self-reported or via CPMS) to already be immune to hepatitis A either from previous vaccinations or previous infections and were excluded from this analysis (figure 1). Of the 3713 remaining men who were deemed eligible for the free hepatitis A vaccine, the median age was 29 years (IQR 25–35), and 1.2% (n=43) identified as Aboriginal or Torres Strait Islander. There were 5.7% (n=212) MSM living with HIV. Of the 3501 MSM not living with HIV, 11.0% (n=385) were currently taking PrEP.

Figure 1

Flow chart of data selection. MSHC, Melbourne Sexual Health Centre; MSM, men who have sex with men.

Of the 3713 MSM who were not previously vaccinated nor immune to HAV from previous infections, 62.7% (n=2327; 95% CI 61.1% to 64.2%) had received at least one dose of the hepatitis A vaccine at MSHC in 2018. In addition to the 5869 MSM already recorded as immune to hepatitis A, a total of 85.5% of MSM (8196/9582) attending MSHC were immune to hepatitis A in 2018.

Overseas-born MSM had higher odds of receiving the hepatitis A vaccine than Australian-born MSM (OR 1.24; 95% CI 1.08 to 1.42) in the univariable analysis, but this association disappeared in the multivariable analysis after adjusting for other potential confounding factors such as age, sex work status, number of male partners, HIV status and PrEP use. Other factors including being a sex worker, being Indigenous, reported condomless anal sex in the past 12 months and reported intravenous drug uses in the past 12 months were not associated with the hepatitis A vaccine uptake in the univariable analyses. In adjusted analyses, MSM aged 16–25 years had higher odds of receiving the vaccine (adjusted OR (aOR) 2.49; 95% CI 2.05 to 3.01), followed by MSM aged 26–35 years (aOR 2.10; 95% CI 1.76 to 2.50), compared with MSM aged ≥36 years (table 1). Compared with MSM not living with HIV and not taking PrEP (n=3116), MSM taking PrEP (n=385) were 1.28-fold (95% CI 1.01 to 1.62) more likely to receive the hepatitis A vaccine, but it did not differ to MSM living with HIV (n=212). Men who had more than four male partners in the past 12 months were 1.28-fold (95% CI 1.08 to 1.51) more likely to receive the hepatitis A vaccine compared with men who had four or less partners in the past 12 months after adjusting for other potential confounding factors.

Table 1

Factors associated with hepatitis A vaccine uptake among 3713 men who have sex with men attending Melbourne Sexual Health Centre in 2018

There were 1386 (37.3%) MSM who were eligible for the hepatitis A vaccine but did not receive it (table 2). The majority of these men were not offered the vaccine by their clinician; for 55.4% (n=768), no reason for not receiving the vaccine was stated; these men did not receive the HAV serological test and did not re-attend the clinic in 2018; and for 3.6% (n=50), there was a logistical reason such as the vaccine not being available at the clinic or it being close to closing time. Three hundred men (21.6%) were non-immune against HAV after performing HAV serological test but did not return to the clinic for vaccination. In addition, 268 men were offered the hepatitis A vaccine, but they declined. The main reasons for declining the vaccine were requesting more time to consider getting vaccinated (n=44, 3.2%) and logistical reasons such as being unwell or lack of time (n=33, 2.4%). A small proportion of men declined the vaccine due fear of needles (n=20, 1.4%) and vaccines (n=7, 0.5%). Seventeen men (1.2%) declined the vaccine on the day and stated they would return to the clinic for the vaccine but they did not.

Table 2

Mutually exclusive reasons for declining to receive the hepatitis A vaccine among 1386 men who have sex with men

Discussion

This study shows that almost two-thirds of MSM who were unvaccinated or not immune to hepatitis A had received at least one dose of hepatitis A vaccine at MSHC by the end of 2018 from the targeted free hepatitis A vaccination programme. The government-funded hepatitis A vaccination programme in Victoria has successfully influenced and contributed to the uptake of hepatitis A vaccine among MSM in a sexual health clinic setting. MSM who were at a younger age, taking PrEP or who reported a higher number of male partners in the past 12 months had higher odds of receiving the hepatitis A vaccine. An Australian-based mathematical model published in 2016 has estimated that the proportion of MSM who are immune to HAV should reach at least 70% in order to prevent future outbreaks of HAV in MSM.12 With this vaccination programme, the proportion of men who are immune to HAV has increased from 61.3% to 85.5%. The introduction of the targeted hepatitis A vaccination programme for MSM in Victoria has been effective and successful in increasing the immunity among the MSM population, and it is likely this timely vaccination programme may prevent ongoing transmission and the likelihood of future outbreaks.

The association between the hepatitis A vaccine uptake and being of a younger age may be due to young men being more aware of their sexual health or that they were less likely to have previously been immunised either actively or passively. Higher vaccine uptake among MSM taking PrEP suggests that those already attempting to reduce their sexual health risk are more likely to continue doing so by receiving the vaccine. Higher uptake may also be due to more regular contact with service, as men on PrEP return regularly for HIV/STI check-ups. A previous study also demonstrated that MSM taking PrEP were more likely to receive HPV vaccine than MSM who did not take PrEP.10 In addition, men who had a higher number of male partners are at higher risk of acquiring HAV, and our findings indicate that this group were more likely to receive the hepatitis A vaccine which will aid in preventing future outbreaks through their sexual networks.

About one-third of eligible MSM who were not immune did not receive or decline the hepatitis A vaccine. Most MSM (55.4%) were not offered the vaccine by the clinician, with no reason documented. This could be due to the clinician having forgotten, perhaps due to clients presenting with other complex medical issues that were given priority. Furthermore, some MSM were offered serological testing of HAV prior to the vaccination because the clients were not sure about their vaccination status. As per the current clinic policy and management, only clients with a positive STI test result will be contacted, but this does not include antibody test for HAV. Instead, clients are advised to call the clinic to check their antibody test results. Past studies have shown that patient and clinician reminders are useful to increase immunisation rates.13

Following HAV outbreaks in other countries, vaccine programmes targeting MSM have also been introduced. A programme introduced in Montreal, Canada in response to an outbreak in 1995–1997 achieved a 49% coverage rate, tripling the pre-program level.8 Similarly to our study, the Canadian study by Allard and colleagues found that MSM with more partners were more likely to receive the vaccine (56% in men with four or more partners in the past 6 months compared with 44% in those with three or less). In contrast to our results, however, men aged above 25 years were more likely to receive the vaccine (52%) compared with those aged less than 25 (33%). A study of a year-long hepatitis A vaccination programme for MSM in Atlanta, USA estimated that the vaccination coverage would only be 10%–20% of the at-risk population.9 Reasons for men declining the vaccine included them believing they were not at risk, they had not heard of the vaccine or ‘not getting around to it’. Our study did not identify these specific reasons, suggesting the ‘Little Pricks’ campaign, which ran concurrently to the vaccination programme, may have increased awareness of the HAV and availability of the vaccine. Both hepatitis A vaccination programmes in Canada and the USA resulted in a decline in reported cases of hepatitis A following the introduction of the vaccination programme. It can be expected that a similar trend will occur with the programme in Victoria, and further study will be required to assess the effectiveness of the programme.

This study has several limitations. First, this study only analysed data collected from a single sexual health clinic in Melbourne, Australia. The hepatitis A vaccination programme was a State-government initiative, with all general practitioners, sexual health centres and other vaccination providers able to provide the free vaccine across Victoria. It is possible that clinicians at MSHC were more aware of the programme and more likely to offer the vaccine, as well as it being possible that men attending MSHC were more sexually active and had a high level of sexual health literacy. Clients could have received the vaccine at a different clinic, which would not be visible on our records. Second, clients self-reported their hepatitis A vaccination status to the clinician, which may have resulted in recall bias. As such, some men who were not immune may have reported as immune, possibly due to confusion with other past vaccines, particularly hepatitis B vaccine.14 Third, incomplete medical records by clinicians when documenting whether they offered the vaccine and the reasons for refusal may have affected the result of the secondary outcome in evaluating why the clients did not receive the vaccine. It is possible that some clinicians may not offer the vaccine to the clients when they have complicated consultations such as new HIV and STI diagnoses.

To conclude, this study has shown that the free time-limited government-funded hepatitis A vaccination programme for MSM in Victoria has so far been effective and successful at increasing immunity to the critical vaccine coverage among clinic attendees (ie, 70%) which may help to limit future outbreaks of HAV. In December 2018, the hepatitis A vaccination programme was extended until the end of June 2019. Continuing to offer the free hepatitis A vaccine to the MSM population would maintain high immunity levels and prevent ongoing transmission and future sporadic outbreaks among this population.

Key messages

  • An outbreak of hepatitis A among gay, bisexual and other men who have sex with men (MSM) was identified in 2017 and the Victorian government implemented a free time-limited hepatitis A vaccination programme targeting all Victorian MSM in 2018.

  • The hepatitis A vaccination uptake among MSM through a sexual health clinic was 62.7% in 2018.

  • Hepatitis A vaccination uptake was significantly associated with younger age, taking pre-exposure prophylaxis and reporting a higher number of male partners in the past 12 months.

  • Continuation of the targeted hepatitis A vaccination programme is essential to increase the hepatitis A immunity among the MSM population to prevent ongoing transmission.

Acknowledgments

We acknowledge Afrizal Afrizal for his assistance with data extraction.

References

View Abstract

Footnotes

  • Handling editor Dr Joseph D Tucker

  • Presented at Some data of this work were presented as a poster presentation at the STI & HIV 2019 World Congress in Vancouver, Canada, 14 –17 July 2019.

  • Twitter Follow Eric Chow @EricPFChow

  • Contributors EPFC and CKF designed the study. SB conducted the analysis, performed the chart review and wrote the first draft of the manuscript. LAV and EPFC assisted with data analysis and interpretation. All authors were involved in data interpretation. All authors revised the manuscript critically for important intellectual content and approved the final version.

  • Funding This study is supported by the 2018 GSK Immunisation Grants (EP000784GSK).

  • Competing interests EPFC was supported by the National Health and Medical Research Council (NHMRC) Early Career Fellowships (1091226). All other authors declare no competing interests.

  • Patient consent for publication Not required.

  • Ethics approval This study was approved by the Alfred Hospital Ethics Committee, Melbourne, Australia (no. 669/18).

  • Provenance and peer review Not commissioned; externally peer reviewed.

  • Data availability statement All data relevant to the study are included in the article or uploaded as online supplementary information.

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