Objectives: To compare the seroprevalence of hepatitis A in homosexual and heterosexual men to determine their susceptibility to infection and provide guidance for a policy on vaccination.
Methods: A case-control study design was utilised to compare the risk factors associated with hepatitis A in homosexual and heterosexual men attending a city centre genitourinary medicine clinic. Demographic and sexual behavioural characteristics were included in univariate and multivariate models.
Results: The overall seropositivity rate was 29% with no significant difference between homosexual and heterosexual men. Ethnicity and age were strongly associated with hepatitis A seropositivity in both homosexuals and heterosexuals. A history of sex in a sauna in homosexual men, and being born outside the United Kingdom for heterosexual men, was associated with hepatitis A seropositivity.
Conclusions: Targeted hepatitis A screening and vaccination of homosexual men attending UK genitourinary medicine clinics is not supported by the results of this study.
- hepatitis A
- sex behaviour
- sexually transmitted diseases
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Hepatitis A virus (HAV) is a robust RNA virus transmitted by the faecal-oral route and is responsible for most cases of infectious or “epidemic” hepatitis. Around 7000 cases of hepatitis A are notified each year in the United Kingdom, mostly among schoolchildren and young adults.1 In children infection is usually asymptomatic, but infection later in life can be more severe, causing prolonged illness and even fulminant hepatic failure. As societies become more affluent so the incidence of childhood disease due to overcrowding and poor sanitation falls and adult susceptibility rises. Traditional methods of transmission are then replaced in importance by other mechanisms, such as food poisoning epidemics2 and faecal-oral contamination in sexual contact.3
In the late 1970s several enteric diseases such as shigellosis, amoebiasis, and Giardia were recognised as being sexually transmissible among homosexual men.4 The advent of specific antibody testing for hepatitis A IgM and the subsequent detection of a number of outbreaks among homosexual men3,5–12 convinced many that sexual transmission was important. A recent community based study in San Francisco found that 3.3% of a sample of 411 self identified homosexual men had acute hepatitis A (as shown by anti-HAV IgM).13 Some cross sectional seroprevalence studies have also shown higher rates of hepatitis A exposure in homosexual men than in heterosexuals attending clinics for sexually transmitted diseases (STDs).3,14,15 In these studies, oral-anal or digital-anal contact,3,15 duration of homosexual activity,3,15 number of lifetime sexual partners,16 sex in saunas,11 and group sex10 have all been associated with hepatitis A exposure.
Other similar seroprevalence studies set in both the community17,18 and STD clinics16,18–25 have failed to find evidence that homosexual men have higher rates of hepatitis A than heterosexual men, although in general STD clinic attenders have higher rates than local blood donors.16,18,26
In order to determine the susceptibility of homosexual men to HAV in a non-London UK setting we conducted a seroprevalence survey of homosexual male attenders, comparing them to age matched heterosexual male attenders. We investigated the influence of putative risk factors for HAV acquisition (such as sexual behaviour) on seroprevalence to inform the optimum strategy for pre-immunisation testing.
The study was performed at a large city centre genitourinary medicine clinic in Birmingham, United Kingdom. Consecutive new or rebooked male attenders aged 16 and over who needed venepuncture for routine syphilis serology or for HIV testing were invited to participate. Subjects giving informed consent completed a questionnaire in private, which yielded the following data:
demographic data (date of birth, country of birth, self assigned ethnic status, whether raised in United Kingdom (defined as whether all of childhood was spent in United Kingdom)
travel history (ever travelled outside United Kingdom, western Europe, North America, or Australia)
clinical history (history of jaundice (and if this was known to be due to hepatitis A), history of vaccination against hepatitis A or B or both, history of HIV infection)
sexual behaviour (including number and sex of sexual partners in previous year, history of peno-vaginal, peno-anal, receptive anal, oro-genital, oro-anal, and digital-anal sex ever and in previous year).
We excluded subjects who had received normal immune globulin in the preceding 12 months, who had been immunised against hepatitis A or who were known to be infected with HIV. We categorised the remaining subjects as “homosexual” (men who reported ever having sex with other men) or “heterosexual” (men who reported never having a same sex partner), these terms being used for ease of reference. We assigned every eligible homosexual man as a case, and matched each case with two heterosexual controls from the same 5 year age band who attended on the same day. Hepatitis A total IgG was determined by ELISA (with confirmation if equivocal by radiometric assay). Subjects were informed of their hepatitis A immune status along with their other results, and those who were non-immune given an information leaflet.
Assuming a seroprevalence of 30% in the general (heterosexual) population aged 20–241 (typical of our clinic attenders) and 2:1 recruitment of heterosexual controls to homosexual cases, a total sample size of 207 (69 cases and 138 controls) was required to detect a relative risk of 1.7 with a power of 80% and alpha of 5% (epi-info version 6). A univariate comparison of demographic and behavioural factors with seropositivity for hepatitis A was performed using the χ2 test (spss v 10). Variables with a significance level less than 0.1 on univariate analysis and not exhibiting interactions with other variables were entered into a multivariate logistic regression model using a forward conditional (likelihood ratio) method (spss v 10).
A total of 213 clinic attenders participated in the study. Three patients (1.4%) with equivocal hepatitis A serology were excluded, and the analysis is based on 74 homosexual men (cases) and 136 male heterosexual controls recruited between February and September 2000. Table 1 shows the demographics of the study population. Homosexual men were more likely to be of white ethnicity.
Overall, 61 (29% (95% CI 23% to 35%)) individuals were hepatitis A seropositive. Homosexual men were less likely to be hepatitis A seropositive than age matched heterosexual controls, although this difference was not significant (23% v 32%, p=0.1). There was a striking difference in hepatitis A seropositivity according to self assigned ethnic status (fig 1).
In a univariate analysis of all subjects, increasing age, being born outside the United Kingdom, spending childhood outside the United Kingdom, and non-white ethnicity were strongly associated with hepatitis A seropositivity, and a weaker association was found for those with a history of gonorrhoea (table 2). In homosexual men, the only significant association between sexual practices and hepatitis A seropositivity was in those ever having had sex in saunas, who were over twice as likely to be HAV seropositive with a prevalence of 37% (table 3). Hepatitis A seropositivity in homosexual men was not associated with other reported sexual behaviours, including oro-anal sex or digital-anal sex (table 3). In heterosexual men there were no associations between a variety of sexual practices and hepatitis A seropositivity (table 4). There was a trend towards heterosexual men acquiring infection at an earlier age (fig 2).
We then constructed three regression models to explore these associations, entering variables with a significance level less than 0.1 on univariate analysis into a forward conditional logistic regression model separately for each of three groups (all subjects, heterosexual men, and homosexual men). Sexual behaviour variables were only included in the models for heterosexual and homosexual subgroups. Ethnicity and age were strongly associated with hepatitis A seropositivity in all three analyses, with weaker associations found for a history of travel outside the United Kingdom or Western Europe (for all patients), history of sex in a sauna (for homosexual men) and being born outside the United Kingdom (for heterosexual men) (table 5).
Our study population had an overall HAV seropositivity prevalence of 29%, although the prevalence of 23% for homosexual men is slightly lower than reported from studies in other areas.3,13,15,19 The only sexual practice associated with HAV was for men having had homosexual sex in a sauna, an activity reported by 37% of homosexual subjects. Anonymous sex, such as occurs in dark rooms or saunas, is a consistent predictor of risk for hepatitis A infection in homosexual men in several outbreak studies.10,11,27 Many other potential behavioural risk factors, including those found to be significant in other studies,3,10,11,15,16 were not found to be relevant. This lack of association may be the result of genuine differences in the populations studied or reflect methodological differences.
Identifying risk factors associated with hepatitis A infection may be useful in targeting high risk groups for health promotion, providing advice to patients about high risk behaviours, and to inform policy for providing vaccination against infection. The UK PHLS Communicable Disease Surveillance Centre has suggested in the light of recent HAV outbreaks in London that “HAV vaccine may be considered for homosexual men whose lifestyle puts them at risk” but fails then to define what particular lifestyle this means.28 The 1996 UK DoH “Green Book” on immunisation suggests that homosexual men are at risk of HAV but stops short of recommending blanket coverage, preferring to leave the decision to the discretion of the doctor. Neither document gives guidance on preimmunisation testing, where immunisation is avoided in those testing positive for anti-HAV total IgG.
Our cross sectional study design has some inherent limitations. In particular, it is not possible to establish a causal relation between any sexual behaviour variable found to be associated with HAV infection because it is not known when the infection was acquired and whether the potential risk predated the exposure. It is also not possible to exclude recall bias, and other potentially relevant variables may not have been included. Two seroincidence studies constitute the most convincing evidence that HAV can be sexually transmitted. In the best designed, Corey et al followed 102 homosexual and 57 heterosexual non-HAV immune men for 6 and 8 months respectively. The annual incidence of HAV was 22% for homosexuals, but no cases were seen in heterosexuals.3 Coutinho et al found that 14% of 399 homosexual men seroconverted over a 690 day follow up, compared to none of 50 heterosexual men over 6 months.15 Although there is unequivocal evidence that hepatitis A can be transmitted sexually, our study in common with several others suggests that factors other than sexual practices are usually more important.
Our data show that in our cohort hepatitis A had been acquired in many men by the third and fourth decade whatever their sexual orientation, and by 35 years of age almost half had been exposed to HAV and were immune. Belonging to a non-white ethnic group was also a risk factor for HAV independent of country of birth and sexual orientation. This may be the result of higher rates of infection within subgroups of the population resulting in an increased risk of transmission, or non-white ethnicity may be a surrogate for alternative risk factors such as socioeconomic status. Being born outside the United Kingdom was associated with increased risk of hepatitis A for heterosexual men only, and travel outside the United Kingdom/western Europe slightly increased the chances of having had HAV for all subjects.
The results of this study do not provide any evidence to support the routine testing and vaccination of homosexual men for hepatitis A in UK genitourinary medicine clinics. Patients who report engaging in group or anonymous sex should be apprised of the increased risk of hepatitis A among other sexually transmitted infections. Hepatitis A does, however, remain a common infection with a rapid increase in seropositivity observed between men in the third and fourth decades of life, and is easily preventable with a durable vaccine. Further studies are needed to assess the pattern of infection in women and whether it is cost effective to offer vaccination based on age and/or ethnicity.
This study was funded by a grant from the MSSVD Clinical Development Fund.
We thank Debbie Goddard for her assistance with patient recruitment for the study, Richard Matthews (Birmingham PHLS) for serology testing, and Keith Radcliffe for assisting with the initial concept and study design.
Conflict of interest: none.
CONTRIBUTORS JR, concept, study design, grant application, supervision, manuscript ; MG, data collection, manuscript review; AT, data collection, manuscript review; GG, data collection, supervision; AW, study design, grant application, manuscript preparation.
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