Factors associated with HIV seroconversion in gay men in England at the start of the 21 st century

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1 1 HIV and STI Department. Health Protetion Ageny Centre for Infetions, UK; 2 Department of Infetious Disease Epidemiology, Imperial College Faulty of Mediine, London, UK; 3 Sigma Researh, University of Portsmouth, UK; 4 Centre for Sexual Health and HIV Researh, University College London, London, UK; 5 Statistis and Modelling and Bioinformatis Department, Health Protetion Ageny Centre for Infetions, UK Correspondene to: Neil Madonald, Department of Infetious Disease Epidemiology, Imperial College London, Norfolk Plae, London W2 1PG, UK; n.madonald@imperial.a.uk All the authors ontributed to the development and writing of the paper. NM, GE, CM, FH, JI, KF, VG, RP and BE ontributed to the design and management of the study. In addition, KB and HW ontributed to the analysis. All authors have ontributed to the drafting, reviewing and revision of the manusript and have approved the final version. Aepted 2 November 2007 Published Online First 14 November 2007 Fators assoiated with HIV seroonversion in gay men in England at the start of the 21 st entury N Madonald, 1,2 G Elam, 1 F Hikson, 3 J Imrie, 4 C A MGarrigle, 1 K A Fenton, 1,4 K Baster, 5 H Ward, 1,2 V L Gilbart, 1 R M Power, 4 B G Evans 1 ABSTRACT Objetives: To detet and quantify urrent risk fators for HIV seroonversion among gay men seeking repeat tests at sexual health linis. Design: Unmathed ase ontrol study onduted in London, Brighton and Manhester, UK. Methods: 75 ases (reent HIV positive test following a negative test within the past 2 years) and 157 ontrols (reent HIV negative test following a previous negative test within the past 2 years) ompleted a omputerassisted self interview foused on sexual behaviour and lifestyle between HIV tests. Results: Cases and ontrols were similar in soiodemographis, years sine ommening sex with men, lifetime number of HIV tests, reasons for seeking their previous HIV tests and the interval between last HIV tests (mean = 10.5 months). Risk fators between tests inluded unproteted reeptive anal interourse (URAI) with partners not believed to be HIV negative (adjusted odds ratio (AOR) and 95% onfidene interval 4.1, 1.8 to 9.3), where inreased risk was assoiated with onomitant use of nitrite inhalants, reeiving ejaulate and inreasing numbers of partners. Independent risk was also deteted for unproteted insertive anal interourse (UIAI) with more than one man (AOR 2.7, 1.3 to 5.5) and use of nitrite inhalants (AOR 2.4, 1.1 to 5.2). Conlusions: HIV serodisordant unproteted anal interourse remains the primary ontext for HIV transmission among gay men, with inreased risk assoiated with being the reeptive partner, reeiving ejaulate and use of nitrite inhalants. Although the HIV transmission risk of URAI is widely aknowledged, this study highlights the risk of UIAI and that nitrite inhalants may be an important failitator of transmission when HIV exposure ours. Sex between men remains the main fous of HIV transmission in the UK, aounting for over 2300 new diagnoses reported for 2005 and an estimated 84% of all infetions likely to have been aquired within the ountry. 12 Surveillane of high risk behaviour and sexually transmitted infetions (STIs) among men who have sex with men (MSM) have shown worsening trends in reent years, with the proportion of MSM reporting unproteted anal interourse in the past year rising to 42% in 2000 in London and rates of STIs reahing reord levels in England and Wales. 34 The re-emergene of syphilis at the end of the 1990s and lymphogranuloma venereum in 2004 gives further ause for onern for the sexual health of MSM in the UK. 56 HIV prevention strategies are based on theories about whih behaviours an ause HIV transmission (relative risk) and the prevalene of suh behaviours in the population of onern (attributable risk). Risk fator studies were among the earliest responses to the AIDS epidemi. Empirial knowledge of HIV transmission through sex between men has primarily been derived from studies onduted in the first deade of the epidemi The largest of these was the Multi- Center AIDS Cohort Study, 12 onduted in epientres in the USA, whih identified unproteted reeptive anal interourse (URAI) as the main risk fator for HIV seroonversion, a finding repliated in most other studies. Behaviours inreasing the likelihood of exposure, suh as high numbers of sexual partners, and fators thought to inrease the probability of transmission, suh as the presene of other STIs, have also been reported with varying degrees of onsisteny. Sine there are far more sexual HIV exposures than transmissions, behaviours that failitate HIV transmission when exposure ours are important targets for prevention programmes. Currently, England s HIV prevention strategy for MSM, 13 first implemented in 1998 and updated in 2003, identifies HIV sero-disordant unproteted anal interourse, ondom failure, the introdution of HIV infeted semen into the mouth or anus of uninfeted men, onurrent STIs (speifially gonorrhoea, syphilis and herpes) and the absene of post-exposure prophylaxis in men exposed to HIV, as behaviours with suffiient evidene of both relative and attributable risk among MSM in England to warrant being population level targets. The UK s INSIGHT (Investigation of New Seroonversions In Gay men who HIV Test) Projet was established in 2001 to determine whether these fators driving HIV seroonversion in MSM at the beginning of the 21st entury remain urrent, are aompanied by new fators and, if indiated, to inform hanges in these population goals/objetives for HIV prevention. MATERIALS AND METHODS A ase-ontrol study was onduted at seven sexual health linis in London (5), Manhester (1) and Brighton (1), whih together aount for more than half the diagnoses of HIV aquired through sex between men in England. Phased reruitment of partiipants ran from September 2002 to Otober 2004, with most linis reruiting ontinuously over a 12 month period. Subsets of purposively seleted respondents partiipated in follow up in-depth interviews exploring the ontext of HIV seroonversion. The results of the qualitative study are reported separately. 8 Sex Transm Infet 2008;84:8 13. doi: /sti

2 STUDY POPULATION Cases (HIV seroonverters) were defined as gay men over 16 years old, who had a reent HIV positive test result at one of the partiipating linis, having had an HIV negative test result within the previous two years. Controls were drawn from the same population but had had a HIV negative test result on both oasions. Men whose interval period between tests was less than three months, potentially in the window period for antibody detetion, were exluded. Cases were given time to adjust to their diagnosis before being reruited but were approahed within a month of testing HIV positive. Controls were reruited immediately after reeiving their HIV negative test result and any post-test ounselling. Clini staff identified and reruited partiipants and provided a private spae for them to omplete the study questionnaire. STUDY PROCEDURES A omputer-assisted self interview (CASI) was used to ollet data from the partiipants. The ontent was guided by urrent and speulative theories about determinants of HIV transmission, with questions developed from a range of existing studies, and using ognitive interview testing with the initial reruits. The CASI asked about key sexual behaviours (insertive anal interourse, reeptive anal interourse and reeptive oral sex) between their last two HIV tests, in two different ways. First, they were asked to report the aggregate numbers of men, by pereived HIV status (known HIV positive, presumed HIV negative and unknown) at the time the sex ourred. Seond, they were asked to report partner speifi behaviours with up to three regular partners and aggregate behaviours with asuals. Partiipants were also asked about use of soial and sexual venues and forms of media used to meet sex partners, inident diagnoses of STIs, overall health, linial depression, and use of alohol and rereational drugs between their HIV tests. Cases ompleted the same CASI as ontrols and submitted their responses via the internet. No questionnaire data were held at the lini after submission. All partiipants provided written informed onsent. The study was approved by the South West Multi-entre Researh Ethis Committee and loal Ethis Committees overing the partiipating sites. STATISTICAL ANALYSIS Variables were examined to determine their assoiation with HIV seroonversion using Stata (version 9.0; Stata Corp, College Station, TX, USA). Continuous variables were explored using t tests. For ategorial variables odds ratios (OR) 95% onfidene intervals (CI) and p values were obtained using logisti regression. Variables that were assoiated with being a seroonverter (p(0.2) were used as preditor variables in multivariable logisti regression models. This provides a onvenient approah to ontrol the assoiations of interest for any potential onfounding fators. Models were onstruted using a hierarhial approah based on a proximate-determinants framework similar to Boerma and Weir. 16 Bakward elimination models were used to explore distal fators, retaining those where p(0.2. For the key sexual behaviour variables, multivariable analysis was restrited to adjusting for any report of URAI with men not believed to be HIV negative. RESULTS Charateristis of HIV seroonverters and ontrols A total of 75 ases and 157 ontrols were reruited to the study, with an overall response rate of 72%, with no substantial differene in response rates between ases and ontrols. The two groups were similar in terms of demographis, with a mean age at last HIV test of 35 years, over 90% white ethniity, around half eduated to degree level and three-quarters were employed (table 1). Seventy-seven per ent of partiipants desribed themselves as gay and most were open or ompletely open to others about their sexuality. Sexual and HIV testing histories were also omparable with ases reporting a mean of 16 years sine first anal sex, 7 years sine first HIV test, six HIV tests in total and a mean interval of 10.6 months between the last two HIV tests (10.5 for ontrols). Cases reported a median of 15 sexual partners in the interval ompared to 12 for ontrols (p = 0.113). Forty seven per ent of ases reported sex with at least one man they knew to be HIV positive ompared to 36% of ontrols, although this differene was not statistially signifiant. Similarly, there were no signifiant differenes in numbers of sexual partners who were believed HIV negative or of unknown HIV status, the latter omprising the majority of sexual ontats. Anal interourse was reported by all ases and 97% of ontrols. Fators assoiated with HIV seroonversion Between HIV tests, 83% of ases and 55% of ontrols reported URAI, rude odds ratio (OR) 3.9 (2.0 to 7.7) with inreasing risk evident with inreasing numbers of men (table 2). URAI with at least one known HIV positive man was reported by 28% of ases and 11% of ontrols (OR 3.2, 1.6 to 6.4). This risk inreased sharply where nitrite inhalants were used (OR 9.3, 3.3 to 26.2) and where ejaulation ourred, partiularly involving Table 1 Soiodemographi harateristis, sexual and HIV testing histories of the INSIGHT ase-ontrol study partiipants Cases n=75 Controls n = 157 Categorial variables % % Ethniity White Non-white 4 9 Country of birth UK Outside UK Eduation: years sine aged 16 Left shool with no qualifiations Up to 2 years More than 3 years Eduated to degree level Employment Employed (full or part time) Unemployed 9 8 Student 5 8 Sexuality Desribes themselves as gay Completely or open to most about sexuality Continuous variables mean range mean range Age at seond last HIV test Months between last 2 HIV tests Age at last HIV test Sexual and HIV testing history Years sine first anal sex Years sine first visit to STI lini Years sine first ever HIV test Lifetime number of HIV tests STI, sexually transmitted infetions. HIV Sex Transm Infet 2008;84:8 13. doi: /sti

3 URAI with more than one HIV positive man (OR 5.5, 1.0 to 28.9). A similar pattern was observed with URAI with men of unknown HIV status (OR 4.3, 2.4 to 7.8), although there was no further inrease in risk observed with use of nitrite inhalants in this ontext, inreasing numbers of men, ejaulation and ejaulation with more than one man all showed inreased risk. In ontrast, no statistial assoiation was found between HIV seroonversion and URAI pratises with men believed to be HIV negative (table 2). Signifiant risks were found for URAI with regular partners (OR 2.4, 1.4 to 4.3) and with asuals (OR 3.7, 2.0 to 6.8). Unproteted insertive anal interourse (UIAI) was reported by 76% of ases and 61% of ontrols (OR 2.1, 1.1 to 3.8), with inreased risk for UIAI with more than one man (OR 4.5, 2.5 to 8.0) and to a lesser extent with five or more men (OR 2.5, 1.2 to 4.9). Although men who reported UIAI with known HIV positive and unknown status men were at inreased risk of seroonversion, there was no strong evidene for inreasing risk with UIAI with inreasing numbers of men. Having adjusted for URAI with men not believed to be HIV negative, seroonversion was found to be signifiantly assoiated with UIAI with more than one man (adjusted odds ratio (AOR) 2.7, 1.4 to 5.2), more than one man not believed to be HIV negative (AOR 2.0, 1.1 to 3.7) and more than five suh men (AOR 2.3, 1.1 to 5.1) (table 2). Table 2 Any report of: Sexual behaviours of the INSIGHT ase-ontrol study partiipants Cases n=75 Unproteted reeptive oral interourse (UROI) was almost universally reported. Cases were more likely than ontrols to report UROI with HIV positive men and UROI to ejaulation in their mouth by men of unknown HIV status. However, these behaviours were not found to be statistially signifiant after adjusting for URAI with men not believed to be HIV negative. Examination of anillary sexual behaviours (reported as never, sometimes and often) showed that men who seroonverted were more likely to report any instane of giving oral anal ontat (rimming), group sex, reeptive use of sex toys and being fisted (table 3). However there was no evidene of inreased risk in men who reported often engaging in these ativities (data not shown). A multivariate model of these behaviours suggested that rimming (AOR 3.3, 1.3 to 8.5) and being fisted (AOR 3.1, 1.4 to 7.0) underlay the observed assoiations (table 3). Forty-five per ent of ases and 39% of ontrols reported a diagnosis of a STI during the interval period (inluding at the time of their most reent HIV test). Diagnoses of gonorrhoea (OR 3.6, 1.7 to 7.8) and syphilis (6.0, 1.1 to 31.8) were both assoiated with seroonversion; however, only gonorrhoea remained statistially signifiant in a multivariate model (table 3). Controls n = 157 Univariable Bivariable* % % OR 95% CI AOR 95% CI Unproteted reeptive anal interourse , , 2.59 with more than 1 man , , 4.15 with 5 or more men , , with HIV positive , , 3.37 using nitrite inhalants , , with more than 1 man , , 5.58 with ejaulation , , 8.50 with more than 1 man , , with believed HIV negative , , 1.46 using nitrite inhalants , , 2.94 with more than 1 man , , 2.53 with ejaulation , , 1.90 with more than 1 man , , 2.53 with not believed HIV negative{ , using nitrite inhalants , , 6.72 with more than 1 man , , 4.19 with 5 or more men , , 8.47 with ejaulation , , 5.24 with more than 1 man , , 8.75 with 5 or more men , , with regular partners , , 2.27 with asuals , , 3.55 Unproteted insertive anal interourse , , 2.59 with more than 1 man , , 5.20 with 5 or more men , , 3.57 with HIV positive , , 3.53 with more than 1 man , , 8.07 with believed HIV negative , , 1.31 with more than 1 man , , 2.17 with not believed HIV negative{ , , 2.87 with more than 1 man , , 3.68 with 5 or more men , , 5.12 *Controlled for unproteted reeptive anal interourse with men not believed to be HIV negative. {Combining men of known HIV positive and unknown HIV status. 10 Sex Transm Infet 2008;84:8 13. doi: /sti

4 Rereational drug use was reported by 93% of ases and 85% of ontrols; however, only 8% of ases and 3% of ontrols reported injeting any drug (mostly steroids). Any use of nitrite inhalants, methylenedioxymethamphetamine (MDMA, Estasy), ketamine, d-lysergi aid diethylamide (LSD) and Viagra were all signifiantly assoiated with seroonversion (table 3). However, examination of the frequeny of drug use (one, more than one and regularly) found no disernable trends in inreased drug use with seroonversion (data not shown). A multivariable model of drug use (any) found only nitrite inhalants assoiated with seroonversion (AOR 3.7, 1.8 to 7.8). Any use of annabis showed redued risk (AOR 0.4, 0.2 to 0.9), although this protetive effet was not apparent if regular annabis use was inluded in the model. Only 11% of ases and 12% of ontrols reported abstaining from alohol (table 3). Ninety-six per ent of ases and 94% of ontrols reported meeting new sex ontats during the interval period. However, none of the venues or media reported to meet these men was statistially assoiated with HIV seroonversion, although a multivariate model indiated that men who used the internet were more likely to seroonvert (AOR 1.9, 1.0 to 3.4) and onversely men who met men in toilets were less likely (AOR 0.3, 0.1 to 0.8) (table 3). A final logisti regression model was used to test the relationship of variables found to be assoiated with HIV seroonversion thus far: URAI with partners not known to be HIV negative; UIAI with more than one man; a diagnosis of gonorrhoea; rimming another; being fisted; use of the internet to meet men; any use of nitrite inhalants. In the final model, independent assoiations for HIV seroonversion were found for URAI with partners not known to be HIV negative (AOR 4.1, Table 3 Assoiation of other fators with HIV seroonversion among the INSIGHT ase-ontrol study partiipants Any report of: Cases n=75 Controls n = 157 Univariable Multivariable* % % OR (95% CI) AOR (95% CI) Anillary sexual behaviours Insertive oral sex (0.02, 1.50) Being rimmed (0.88, 10.83) Rimming another man (1.23, 7.23) 3.28 (1.27, 8.46) Group sex (1.04, 3.51) Sex toys: reeptive (1.08, 3.50) Fisting another man (0.85, 2.95) Being fisted (1.46, 6.60) 3.12 (1.40, 6.96) Sexually transmitted infetions Gonorrhoea (1.66, 7.77) 4.22 (1.82, 9.74) Non-speifi urethritis/chlamydia (0.21, 1.24) 0.44 (0.17, 1.13) Warts (0.41, 3.18) Syphilis (1.14, 31.80) 4.85 (0.86, 27.41) Pubi lie (0.17, 1.67) 0.39 (0.11, 1.37) Herpes (0.37, 7.92) Substane use Alohol (0.48, 2.77) Nitrite inhalants (poppers) (1.52, 5.55) 3.70 (1.75, 7.83) MDMA (Estasy) (1.44, 4.53) 1.71 (0.76, 3.85) Coaine (0.94, 2.85) Cannabis (0.62, 1.88) 0.43 (0.21, 0.86) Ketamine (1.39, 4.28) 1.99 (0.90, 4.41) Viagra (1.03, 3.14) Speed (0.78, 2.90) GHB (gamma hydroxy butyrate) (0.84, 3.18) Methamphetamine (0.60, 2.83) LSD (1.12, 7.15) 3.19 (0.99, 10.21) Mushrooms (0.56, 3.69) 0.40 (0.12, 1.34) Valium (0.43, 2.58) Steroids (0.68, 7.03) Venues used to meet men Bar/lub (0.68, 2.18) Internet (0.95, 2.91) 1.85 (1.02, 3.41) Sauna (0.79, 2.39) Cruising ground (0.80, 2.70) 1.77 (0.88, 3.56) Bakroom (0.88, 3.02) 1.58 (0.80, 3.14) Private party (0.40, 1.66) Gym (0.29, 1.47) 0.49 (0.21, 1.17) Chat line (0.54, 4.82) Toilet (0.17, 1.27) 0.26 (0.08, 0.79) College/work (0.17, 1.35) *Variables in eah tier were entered into a stepwise bakwards logistial model retaining those where p(0.2. Sex Transm Infet 2008;84:8 13. doi: /sti

5 1.8 to 9.3), UIAI with more than one man (AOR 2.7, 1.3 to 5.5) and use of nitrite inhalants (AOR 2.4, 1.1 to 5.2). DISCUSSION Although this study did not detet any new fators driving HIV seroonversion among gay men in England, the findings reemphasise the risks assoiated with unproteted reeptive anal interourse, and larify the risk assoiated with nitrite inhalants use during this ativity. The risk assoiated with UIAI has also been learly identified a pratise that many MSM may mistakenly think low risk. By reruiting men seeking repeat HIV tests at sexual health linis we speifially sampled a population at high risk of HIV aquisition. That the soiodemographis, years at risk and HIV testing histories of ases and ontrols were so similar suggests that potential biases inherent in this methodology have been suessfully ontrolled. In suh a sample, where risk profiles of ases and ontrols losely mirror eah other, the fators failitating transmission (rather than those providing opportunities for exposure) may be expeted to be deteted. Despite this design, URAI was still found to signifiantly differentiate seroonverters from non-seroonverters; this finding not only onfirms earlier work but adds to likelihood that there have been no major additions to the key behavioural drivers of HIV transmission in this population and that findings from previous studies are still valid. The study will have underestimated the relative risk of some behaviours owing to the seletion of ontrols who themselves are at inreased HIV seroonversion risk sine they were having repeated HIV tests. The response rate of over 70% is unlikely to have introdued bias and although reruitment bias is likely, the indiators presented in table 1 suggest these have been ontrolled. Using CASI is likely to maximise reporting of sensitive behaviours, but this will not have overome the reall bias inherent in suh studies. Cases were aware of their diagnosis, and ontrols similarly aware that they were uninfeted, and this may have led to differential reall of risk behaviours. The estimated odds ratios of ertain unproteted anal and oral sex fators differ markedly between the single and multivariable analysis. It is possible that this is due to some olinearity between these fators. Our ability to detet less prevalent risk fators may be limited by our sample size. Contrary to findings from the USA, 17 we found no evidene of methamphetamine s assoiation with seroonversion despite being reported by over 10% of partiipants, Rather, the drug that stands out from our study is nitrite inhalants. This independent assoiation has been reported by earlier studies 8 11 and from North Ameria more reently That onurrent use of nitrite inhalants during HIV sero-disordant unproteted Key messages Unproteted anal interourse with a partner not believed to be HIV negative remains the primary route by whih gay men aquire HIV in the UK Signifiant risk are assoiated with the insertive as well as the reeptive mode of interourse Risks from both behaviours inrease when engaged with multiple partners With the reeptive partner, risk is inreased by reeiving ejaulate and by the onurrent use of nitrite inhalants interourse failitates transmission is biologially plausible. 20 However, an inrease in risk may also be beause nitrite inhalants are used to failitate anal penetration and are more likely to be used during rougher sex. Fators found to be assoiated with seroonversion in multivariate analyses that were later dropped from the final model should not be dismissed. The assoiation of gonorrhoea infetion with HIV seroonversion has been reported previously. 11 One explanation is that men have aquired gonorrhoea from the same partner as they aquired HIV, and gonorrhoea has been shown to inrease viral load in semen and in turn the likelihood of onward HIV transmission. 21 Similarly, that a quarter of ases reported being fisted suggests that engagement in this ativity, as well as taking lub drugs, may be useful markers of men at inreased risk of seroonversion. Further researh should investigate the role of drugs and alohol in the ontext of high risk sexual behaviour. This study onfirms that population level goals or objetives for HIV programmes for gay men should ontinue to fous on reduing sero-disordant unproteted anal interourse. While the potential of nitrite inhalants as a transmission failitator has been aknowledged in England s gay men HIV prevention strategy it has not been adopted as a programmati target. 16 This study suggests that this should be onsidered espeially in light of data suggesting that, after alohol, nitrite inhalants are the most widely used drug among gay men in the UK. 22 We therefore onlude that the attributable risk of nitrite inhalants to HIV seroonversion among gay men in the UK is high and that redution in their use during HIV sero-disordant unproteted interourse be adopted as a population level goal/ objetive by prevention programmes. This reommendation requires further researh on the needs assoiated with avoidane of nitrite use during HIV sero-disordant unproteted anal interourse, and the interventions that may address these needs. Aknowledgements: This researh was funded by the Medial Researh Counil (Strategi Grant number G ). 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The Committee on Publiation Ethis (COPE) has established a Grant Sheme to fund researh in the field of publiation ethis. The Sheme is designed to provide finanial support to any member of COPE for a defined researh projet that is in the broad area of the organisation s interests, and speifially in the area of ethial standards and pratie in biomedial publishing. The projet should have a speifi goal and be intended to form the kernel of a future publiation. A maximum sum of 5000 will be alloated to any one projet, but appliations for smaller sums are welomed. The terms and onditions of the Grant are as follows: At least one of the appliants must be a member of COPE. Calls for appliations will be made twie a year with losing dates of 1 Deember and 1 June. An eletroni version of the appliation form must be sent to the Administrator no later than 12 pm (noon GMT) on the losing date for onsideration by COPE Counil. The appliation must ontain a lay summary of the projet, a definition of the question to be posed, suffiient methodologial detail to allow assessment of the viability of the projet, a lear timeline and a definition of the likely deliverables. A full justifiation for the sum requested must aompany the appliation. A report on the progress of the researh should be presented within one year of the award and at the end of the projet. The grant must be used within two years from the date of award, and balane sheets must be forwarded annually. These should be sent to the Administrator. Any remaining funds after two years must be returned. It is antiipated that the work stemming from the projet will be presented at one of COPE s annual seminar meetings within 2 3 years of the award. Suh data may also be published in peer-reviewed journals. Any publiations or related presentations at meetings by the reipient emanating in part or whole from COPE s support should be duly aknowledged and opies sent to the Administrator. Appliations are reviewed by a COPE sub-ommittee. Appliants will be advised of a deision as soon as pratiable after the deadline date. An appliation form an be obtained by ontating Linda Gough, COPE administrator, at LGough@ bmj.om or For more information on COPE, see The losing date for reeipt of appliations is 1 Deember 2007 or 1 June Sex Transm Infet 2008;84:8 13. doi: /sti