Men who have sex with men (MSM) are the group most at risk of acquiring HIV in the UK, and increases in HIV and other sexually transmitted infections (STIs) remain a matter of concern . Current estimates suggest that, in 2005, 28 000 MSM in the UK were living with HIV, and although the uptake of HIV testing has increased markedly , an estimated 32%i remained unaware of their HIV-positive status .
Undiagnosed infection presents a significant risk for the onward transmission of HIV. In USA it is estimated that at least half of new sexually transmitted HIV infections originate from people unaware of their HIV-positive status . US studies have shown that gay men with undiagnosed infection often delay HIV testing, are afraid of receiving a positive result, and have low-risk perceptions despite reporting HIV-related sexual risk behaviours and STIs [4–7]. It is estimated that testing at-risk MSM biannually could contribute to a two-thirds reduction in HIV exposures , but this relies in part on an assumption of lower sexual risk among those aware of their HIV-positive status [3,9].
In UK community-based surveys, HIV-positive men generally report higher levels of sexual risk behaviour than HIV-negative or never tested men [10–12], but differences between men who are, and are not, aware of their HIV status, and the role of undiagnosed HIV in the UK epidemic, have not been explored. In this paper, we explore the extent of undiagnosed HIV among gay men in five UK cities (London, Brighton, Manchester, Glasgow, and Edinburgh), and examine the similarities and differences between men with undiagnosed HIV, men aware of their HIV-positive status, and HIV-negative men.
In London, Brighton, and Manchester, samples of gay bars, clubs, and saunas (59 in London, 19 in Brighton, and 12 in Manchester) were surveyed between 2003 and 2004 (November 2003 to January 2004 in London, February 2004 in Brighton, and June to August 2003 in Manchester) [10,12]. In Glasgow and Edinburgh, all but one of the exclusively gay bars (six and five, respectively) were surveyed over a 2-week period in April and May 2005, using time and location sampling to obtain a representative sample of these venues. Bars were surveyed in the early (1900–2100 h) and late evening (2100–2300 h) and no bar was visited twice in the same evening. At the end of the 2-week period each bar had been visited at both time points on each day of the week. All men present or entering the venues were asked to participate. One sauna in each city was surveyed over two early evenings . In all five cities, trained fieldworkers distributed anonymous, self-complete questionnaires, and OraSure oral fluid collection kits (OraSure Technologies, Inc., Bethlehem, Pennsylvania, USA) to collect samples to be tested for HIV antibodies. Ethical approval was granted for the London, Brighton, and Manchester surveys by the UCL/UCLH Committees on the Ethics of Human Research, and for Glasgow and Edinburgh by the University of Glasgow, Faculty of Medicine Ethics Committee for Nonclinical Research involving Human Subjects.
The comparable questionnaires included demographics, HIV testing history, perceived HIV status, and experience of STIs in the previous year. Questions on sexual behaviour included number of partners, partner type, and knowledge of partners' HIV status (from which the level of serosorting among diagnosed HIV-positive men was derived). The oral fluid samples from London, Brighton, and Manchester were analysed at the Central Public Health Laboratory, and the samples from Glasgow and Edinburgh at the West of Scotland Specialist Virology Centre. Specimens were screened for anti-HIV using an enzyme immunoassay (England – GACELISA HIV 1 & 2; Abbott Laboratories, Maidenhead, UK; Scotland – Vironostika HIV-UniForm II plus 0; BioMerieux UK Ltd, Basingstoke, UK); all positives were rescreened, and repeat reactives were confirmed using a western blot test (England – HIV blot 2.2, Genelabs; Scotland – New LAV blot 1; Biorad Laboratories Ltd, Hemel-Hempstead, UK).
Questionnaires were obtained from 4384 men [70% response rate (RR)]. Oral fluid samples were obtained from 84% of the men who participated in the surveys – 3672 men, 61% RR (London 63%, Brighton 67%, Manchester 70%, Glasgow 48%, Edinburgh 55%). The men who did and did not provide samples were not markedly different in terms of demographics, HIV testing history or sexual risk behaviour [10,12]. Three thousand, five hundred and one samples had a confirmed positive or negative result and are included in this paper's analyses (171 were excluded because of either insufficient sample volume, unconfirmed results, specimen could not be matched to a questionnaire, respondent had already completed the questionnaire in the last 6 months, or the respondent did not report sex with another man in the previous year).
Data analysis was performed using SPSS 12.0 (SPSS Inc., Chicago, Illinois, USA). The Pearson χ2 test was used for bivariate comparisons and binary logistic regression was used to produce odds ratios and to assess their significance. A P value of less than 0.05 was considered to be statistically significant. Multivariate logistic regression models of sexual risk behaviour were conducted to compare outcomes for HIV-negative, undiagnosed HIV-positive, and diagnosed HIV-positive men. City of recruitment, age, education, employment status, and HIV testing history were controlled for in these models as potential confounders given their association with HIV status, and significant city differences in each of these factors (data not shown). All factors were entered as categorical variables. Interactions between HIV status and the significant confounding factors in the multivariate models were examined. Men with missing data on any of the sexual risk behaviours were excluded from these analyses (N = 455).
Of the 3501 men in the sample, 318 men tested HIV positive (9.1%). Of these, 187 (58.8%) were diagnosed (i.e., they reported previously receiving a positive HIV test result and were aware of their HIV-positive status) and 131 (41.2%) were undiagnosed (i.e., they reported previously testing HIV negative or had never tested and were not aware of their HIV-positive status). The proportion of HIV-positive men who were undiagnosed was 44.1% in London, 33.3% in Brighton, 36.7% in Manchester, 48.1% in Glasgow, and 36.4% in Edinburgh (P = 0.56).
Table 1 shows the characteristics of HIV-negative, undiagnosed, and diagnosed HIV-positive men. HIV-negative men were generally younger than undiagnosed and diagnosed HIV-positive men. The majority of the men surveyed had some education beyond secondary school, but this was significantly lower among the men diagnosed with HIV. There was a similar pattern for employment, with fewer men with diagnosed HIV being currently employed. Undiagnosed men were more likely to report their most recent HIV test was in the 12 months prior to the survey than HIV-negative men, but were less likely to report never having tested. In total, 103 (81.1%) undiagnosed men reported having had a previous HIV test (92.2% tested negative; the remainder reported not knowing the result).
Of the 131 men with undiagnosed HIV, only five (3.8%) thought they might be HIV positive, 81 (62.3%) thought they were HIV negative, and 44 (33.8%) reported that they did not know their HIV status. In comparison, 1.2% of the 3183 HIV-negative men thought they might be HIV positive, 83.8% thought they were negative, and 14.9% reported that they did not know their HIV status (P < 0.001).
Table 2 shows the reported sexual risk behaviours (in the previous year) of HIV-negative, undiagnosed, and diagnosed men (N = 3046). In general, undiagnosed and diagnosed men reported significantly more sexual partners, sexual risk behaviour, and STIs in the previous year than HIV-negative men. Men who were aware of their HIV-positive status reported the highest levels of sexual risk.
Multivariate logistic regression, adjusting for city of recruitment, age, education, employment status, and HIV testing history was used to assess these associations. When compared with HIV-negative men, the adjusted odds of having 10 or more sexual partners, having 10 or more anal intercourse partners, having two or more unprotected anal intercourse (UAI) partners, and of having an STI in the previous year were significantly higher for both undiagnosed and diagnosed men (Table 3). The odds of having UAI with casual partners, and UAI with partners of unknown or discordant HIV status were only significantly higher for diagnosed positive men (Table 3).
In the multivariate regression model for UAI with two or more partners, there was a significant interaction between HIV status and HIV testing history (Table 3). Although the general pattern was for increased odds among men who reported testing in the previous year, men who had tested in the previous year and were diagnosed HIV positive had lower odds of UAI with two or more partners. In the multivariate regression model for having an STI in the previous year, there was also a significant interaction between HIV status and HIV testing history (Table 3). The general pattern was again for increased odds among men who reported HIV testing in the previous year, but the trend differed by HIV status. Although the odds of having an STI in the previous year were greater among HIV-negative men who had had an HIV test in the previous year, the odds of having an STI in the previous year were lower among both undiagnosed and diagnosed men who had had an HIV test in the previous year. There were no other significant interactions.
Table 2 shows that 75 undiagnosed men reported not having UAI with partners of unknown/discordant HIV status, and Table 3 shows that undiagnosed men were not more likely to report this behaviour than HIV-negative men. However, 11 of these 75 men did report having what they must have thought was concordant UAI. Having been unaware of their own HIV-positive status, this UAI could actually have been discordant. Adding these 11 men to the 31 reporting UAI with partners of unknown/discordant HIV status increases the proportion of undiagnosed men who potentially had unknown/discordant partners to 39.6%, after which, the adjusted odds of this behaviour were significantly higher for undiagnosed men compared to HIV-negative men (odds ratio (OR) 2.30, 95% confidence interval (CI) 1.53–3.45).
Having UAI only with casual partners of the same HIV status (serosorting) was reported by 29 men with diagnosed HIV (representing 42.0% of the men who reported UAI with casual partners and 18.5% of the total with diagnosed HIV). Among men who received their HIV-positive diagnosis over a year ago (N = 100), 18.0% reported only having UAI with casual partners of the same HIV status, 32.0% reported UAI with partners of unknown/discordant HIV status, and 48.0% reported having a STI, in the 12 months leading up to the survey.
The present study examines for the first time differences between gay men with diagnosed and undiagnosed HIV infection in the UK. In our community-based surveys, 9% of MSM were HIV positive and 41% of the men who tested positive were unaware of their status, slightly higher than the current UK Health Protection Agency estimate of 32% .
First, there are some limitations to consider when interpreting our results. Only men who visit the venues surveyed had the opportunity to participate. HIV prevalence and undiagnosed infection in the wider UK population of gay men could be different and cannot be surmised from these results. It is also possible that men who only have safer sex could have been more willing to participate in the surveys than men who do not, therefore underestimating actual levels of sexual risk behaviour. There is no way to determine this but the anonymous, self-complete nature of the surveys hopefully limited this bias.
The response rates for providing oral fluid samples were relatively low, and may not be representative of the venue populations. Declining response rates is a trend evident in the cities where regular surveys are conducted [13,14]. However, the overall survey response rate was higher (70%), and there were few differences between the men who provided oral fluid samples and the men who did not [10,12]. This suggests that the men who provided oral fluid specimens were representative of the larger venue-based sample.
Finally, the analyses are limited to available variables, excluding potential risk factors, such as sexual orientation, marital status, and ethnicity. In the London, Brighton, and Manchester surveys, the small number of nonwhites or nongay identified respondents limits the usefulness of these data for statistical analysis (89% of these samples were white, 92% reported they were gay) . These questions were not included in Glasgow and Edinburgh, but Web-based surveys suggest numbers are similarly small among Scottish gay men . Our venue-based surveys are necessarily reliant on short questionnaires and instead focus on sexual risk behaviours. Although it is important that these limitations are considered, the significant differences we found between HIV-negative, undiagnosed, and diagnosed HIV-positive men have important implications for HIV prevention.
Only one in five men with undiagnosed infection had never had an HIV test and two-thirds still perceived their status to be negative, similar to studies elsewhere [5,6,8]. Just under half reported testing negative in the 12 months leading up to the surveys, suggesting many were recent seroconverters (assuming there was limited recall bias in their reporting). Although these men could be frequent testers and receive a positive diagnosis in the future, at the time of the surveys they were making incorrect assumptions about their status, were not accessing clinical HIV services, and could unknowingly be putting others at risk of acquiring HIV; particularly given that they were significantly more likely than HIV-negative men to report multiple partners, which is a known risk factor for HIV . With high viral loads at seroconversion, they could have been highly infectious [17,18], but were basing their sexual risk decisions on an assumption of negativity. This highlights the limits of HIV status disclosure risk reduction strategies for HIV-negative men [19–21].
It is encouraging to note there was not a substantial pool of undiagnosed infection among those who have never tested. Late diagnosis of HIV infection is more common among the heterosexual population in the UK, but in 2005, 22% of MSM diagnosed with HIV had a CD4 cell count less than 200 cells/μl and 7% had a clinical AIDS diagnosis . Therefore, late diagnosis remains of concern for never, or not recently, tested men. Further efforts should be made to promote regular testing among MSM at risk, either through clinics or alternative community-based initiatives [22,23].
However, our findings suggest that relying on a past HIV-negative test result, even within the previous year, may be an ineffective prevention strategy without the additional interventions of condom use and reduced partner numbers. Widespread, routine HIV testing in a range of clinical settings has recently been strongly recommended in the US , and current UK guidelines recommend routine, opt-out HIV testing in genitourinary medicine (GUM) settings [17,25,26]. Although the US Center for Disease Control and Prevention (CDC) recommends that sexually active MSM should be tested at least annually , one study estimated that testing at-risk MSM biannually could contribute to a two-thirds reduction in HIV exposures . Sexual health services are ideally placed to recall men who have tested negative for HIV but who report high-risk behaviours for regular retesting. Services throughout the UK should assiduously offer HIV testing to MSM presenting with STIs.
The suggested reductions in new HIV infections that would result from decreases in undiagnosed infection rely on an assumption of lower sexual risk among those aware of their HIV-positive status, as well as the likely reduction in infection amongst those well controlled on antiretroviral therapy [3,8,9]. However, in our study, it was men who were aware of their HIV-positive status who reported the highest levels of sexual risk, and the higher likelihood of UAI with two or more partners among men diagnosed over a year earlier, suggests that maintenance of safer sex behaviour may be problematic for men living with HIV .
Potential risk reduction strategies for men living with HIV include serosorting and strategic positioning [29,30]. Here, evidence of serosorting was limited, which is similar to findings elsewhere . Serosorting still presents a risk of other STI transmission , and just under half of the men with diagnosed HIV reported having an STI in the previous year. This supports the recommendation for six monthly sexual health assessments among people living with HIV . In our surveys, men were not asked if they were the insertive or receptive partners, so whether they were adopting strategic positioning as a risk reduction strategy could not be determined. If men with diagnosed HIV were not the insertive partners, the actual likelihood of HIV transmission could have been reduced . Indeed, whether men were the insertive or receptive partners also, has implications for HIV transmission among HIV-negative and undiagnosed men and it is important that data on both behaviours are collected separately in future research.
Our findings suggest behaviour change, including the promotion of lower risk sexual practices, condom use, and partner number reduction, should continue to be a major component of HIV prevention efforts in the UK. There is a need for targeted prevention with different age groups, given HIV prevalence increases with age, but levels of undiagnosed infection decrease. Recent reviews have demonstrated the efficacy of behavioural interventions in reducing sexual risk among both HIV-positive and HIV-negative men [28,34,35], and though replication of successful interventions in new settings is not always straightforward [36,37], there is an urgent need to evaluate evidence-based behavioural interventions in the UK.
Sexual health services are appropriate settings for such interventions, given their access to men living with HIV and those at high risk of seroconversion. Intervention delivery by healthcare providers and in settings where people receive routine HIV care or services are two of the characteristics of successful interventions , and current US and UK guidelines recommend some may benefit from counselling on prevention, sexual risk, and behaviour change after test [17,25]. The opportunity to challenge low-risk perceptions and reinforce safer sex messages among men at high risk of seroconversion exists, and should be grasped, in clinical settings.
There is a need for a reinvigorated and tailored approach to HIV prevention among gay men in the UK. Although just under half of the men testing HIV positive were unaware of their status, the higher level of sexual risk among men living with diagnosed HIV suggests that reducing levels of undiagnosed HIV would not in itself be enough to reduce new infections. Prevention efforts should include the promotion of frequent HIV testing among men at high risk of seroconversion. However, evidence-based behavioural interventions to reduce sexual risk among these men, and among those living with diagnosed HIV, are also required, and the initiation and evaluation of these should be made a priority.
The Department of Health and Camden and Islington PCT funded the London, Brighton, and Manchester surveys. The UK Medical Research Council funded the Glasgow and Edinburgh surveys (WBS U.1300.00.005). We thank the survey staff and fieldworkers in each city, Catherine Ferrell (MRC Social and Public Health Sciences Unit), Kirsty Roy (Health Protection Scotland), Linda MacDonald (West of Scotland Specialist Virology Centre), Dr John Parry and Sharon Barnett (Health Protection Agency Centre for Infections), Lee Dodge and Rod Watson (THT South), Alistair Gault, Tim Sigsworth, and Derek Dyer (Lesbian and Gay Foundation Manchester), and John Collett (Camden Health Promotion). Our greatest thanks are to the bar, club and sauna managers, their staff, and the men who agreed to participate in the survey.
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i The 32% undiagnosed infection estimate is calculated using a multiparameter evidence synthesis through which the total number with HIV in the UK is estimated from the combination of data from the National Survey of Sexual Attitudes and Lifestyles (NATSAL), other behavioural surveys, the Unlinked Anonymous Monitoring Programme, the Survey of Prevalent HIV Infections Diagnosed, the National Study of HIV in Pregnancy and Childhood, and the 2001 Population Census. The level of undiagnosed infection for each risk group category (e.g., men who have sex with men) is calculated from information on ‘… risk group size, direct and indirect prevalence of diagnosed and undiagnosed HIV infections, proportions of infections diagnosed and the proportion of prevalent diagnoses belonging to each risk category, and total number of prevalent diagnosed cases reported.’ (The UK Collaborative Group for HIV and STI Surveillance, 2007, page 28).