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Nitrite inhalant use among young gay and bisexual men in Vancouver during a period of increasing HIV… Lampinen, Thomas M; Mattheis, Kelly; Chan, Keith; Hogg, Robert S Mar 15, 2007

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ralssBioMed CentBMC Public HealthOpen AcceResearch articleNitrite inhalant use among young gay and bisexual men in Vancouver during a period of increasing HIV incidenceThomas M Lampinen*1,2, Kelly Mattheis3, Keith Chan2 and Robert S Hogg2,4Address: 1Department of Health Care and Epidemiology, University of British Columbia, Vancouver, Canada, 2BC Centre for Excellence in HIV/AIDS, Vancouver, Canada, 3Department of Family Practice, Faculty of Medicine, University of British Columbia, Vancouver, Canada and 4Faculty of Health Sciences, Simon Fraser University, Burnaby, CanadaEmail: Thomas M Lampinen* - tlamp@telus.net; Kelly Mattheis - kgmatt@telus.net; Keith Chan - kchan@cfenet.ubc.ca; Robert S Hogg - bobhogg@cfenet.ubc.ca* Corresponding author    AbstractBackground: Nitrite inhalants ("poppers") are peripheral vasodilators which, since the beginningof the epidemic, have been known to increase risk for acquiring HIV infection among men who havesex with men (MSM). However, few studies in recent years have characterized use. From 1999 to2004, new HIV diagnoses among MSM in British Columbia increased 78%, prompting us to examinethe prevalence and correlates of this modifiable HIV risk factor.Methods: Self-administered questionnaires were completed between October 2002 and May2004 as part of an open cohort study of HIV-seronegative young MSM. We measured nitriteinhalant use during the previous year and use during sexual encounters with casual partnersspecifically. Correlates of use were identified using odds ratios.Results: Among 354 MSM surveyed, 31.6% reported any use during the previous year. Nitriteinhalant use during sexual encounters was reported by 22.9% of men and was strongly associatedwith having casual partners, with greater numbers of casual partners (including those with positiveor unknown serostatus) and with anal intercourse with casual partners. Nitrite inhalant use wasnot associated with non-use of condoms with casual sexual partners per se.Conclusion: Contemporary use of nitrite inhalants amongst young MSM is common and a strongindicator of anal intercourse with casual sexual partners. Since use appears to increase theprobability of infection following exposure to HIV, efforts to reduce the use of nitrite inhalantsamong MSM should be a very high priority among HIV prevention strategies.BackgroundNitrite inhalants ("poppers") are peripheral vasodilatorsused by men who have sex with men (MSM) to facilitateand enhance sexual intercourse [1]. Throughout the AIDSepidemic, studies have associated use of nitrite inhalantsmore recently and directly, with increased risk of HIVseroconversion [1-10]. Recent seroincidence studies esti-mate that up to 28% of contemporary HIV infectionsamong MSM can be attributed to nitrite inhalant use [8].Published: 15 March 2007BMC Public Health 2007, 7:35 doi:10.1186/1471-2458-7-35Received: 21 July 2006Accepted: 15 March 2007This article is available from: http://www.biomedcentral.com/1471-2458/7/35© 2007 Lampinen et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.Page 1 of 6(page number not for citation purposes)among MSM with prevalent HIV infection, with sexualbehaviours that entail risk of acquiring HIV infection and,Among MSM studied in San Francisco between 1985 and1991, the prevalence of poppers use varied annually fromBMC Public Health 2007, 7:35 http://www.biomedcentral.com/1471-2458/7/3529.9% to 35.9% [7]. Consistent users of poppers were 2.5times (95% CI 1.2 – 4.9) more likely to seroconvert thannon-users. Among 3257 MSM surveyed in 6 US citiesbetween 1995 and 1997, use of poppers during the previ-ous 6 months was reported at 26.9% of study visits and inmultivariate analyses, was associated with a 2.2-fold (95%CI 1.4–3.7) increased risk of HIV seroconversion [8].More recently, we reported a similar 2.2-fold unadjustedrelative hazard for HIV seroconversion associated with useof poppers in an open cohort of young MSM [9].Detailed studies of nitrite use among MSM during the past5 years are scarce. One random digit dial survey con-ducted in 2003 reported that poppers were used duringthe previous six months by 18.6% of HIV-seronegativeMSM residing in Seattle, Washington [4]. Use was signifi-cantly more common among men reporting recent unpro-tected anal intercourse with a sexual partner whose HIVstatus was positive or unknown than among men notreporting such unprotected sex (28.9% of 45 vs. 6.2% of195), though in multivariate analyses, this associationapproached but was not statistically significant (OR = 2.7,95% CI 0.9–8.0).The substantial contribution of nitrite inhalants to con-temporary HIV infections among MSM is well established.Remarkably, in recent years mention of nitrite inhalantsin HIV prevention messages has become exceedingly rare.Risk reduction counselling guidelines do not include clearand specific messages about the increased risk for acquir-ing HIV infection associated with nitrite use [11,12].Indeed, it is no longer clear whether HIV-seronegativemen even receive specific counselling or appreciate theserisks associated with nitrite inhalants.In the province of British Columbia, annual reports ofnew HIV diagnoses among MSM from 1999 and 2004increased 78% (from 95 to 169) [13,14].This tremendous increase in HIV infections among MSMin BC, the importance of poppers as a modifiable risk fac-tor for HIV seroconversion, and the scarcity of recentrelated research prompted us to study the prevalence andcorrelates of contemporary nitrite inhalant use amongyoung MSM in Vancouver.MethodsThe Vanguard Project was a prospective, open cohortstudy of HIV incidence and risk behaviours among youngMSM [15,16]. Briefly, HIV-seronegative self-identified gayand bisexual men between 18 and 30 years of age wholived in Vancouver were recruited at community events, incommunity clinics and through advertisements in localpost-test counselling and completed a confidential self-administered questionnaire. Written informed consentwas obtained from participants according to a protocolapproved by the University of British Columbia ResearchEthics Board.Results from our previous study showed the association ofsubstance use and unprotected anal intercourse (UAI)depends on the type of drug-use measure (any use vs. usespecifically during sexual encounters), type of sexual part-ner (casual vs. regular) and sexual position (insertive vs.receptive) [5]; therefore, we examined the associationbetween high-risk sexual behaviours and nitrite inhalantuse with these distinctions in mind. The present analysiswas restricted to the eighth and final wave of data collec-tion, October 2002 through May 2004. Participants wereasked whether they had engaged in any protected and/orunprotected anal intercourse (receptive, insertive, orboth) during the previous year with regular and casualpartners, respectively. Regular partners were defined asthose with whom the participant had sex with at leastonce a month; casual partners were those with whom theparticipant had sex with less than once a month. Menwere asked to report numbers of regular and casual part-ners, by partners' HIV serostatus (positive, negative,unknown). Men reported any use of licit and illicit drugsduring the previous year. In addition, they specified thosedrugs used shortly before or during sex with regular andcasual partners, respectively, stratified by partners' HIVserostatus.We compared men who did and did not report use ofnitrite inhalants using Pearson's chi-square, Fisher's exact,and Wilcoxon rank-sum tests. Correlates of use were iden-tified using odds ratios (OR) with exact 95% confidenceintervals (CI) computed using PEPI for Windows softwareVersion 4.18 [17].ResultsAmong 354 MSM study participants, 66.4% were white,13.6% were Canadian-Aboriginal, 51.3% had completedcollege, 51.1% were employed full-time, and 7.0% wereHIV-seropositive. Use of poppers during the previous yearwas reported by 112 men (31.6%). Compared to non-users, men who used poppers were younger [median age30, (interquartile range, IQR 26.5, 340) vs. 32, (IQR 29,35), p = 0.003], more likely to have stable housing (92.0%vs. 83.2% p = 0.032), and more likely to report an annualincome greater than CDN$10,000 (89.2% vs. 78.8%, p =0.028). Previous-year use of poppers was not significantlyassociated with race-ethnicity, having completed highschool or college, full time employment, or HIV serosta-tus.Page 2 of 6(page number not for citation purposes)gay newspapers. At baseline and annually thereafter, par-ticipants underwent HIV serologic testing with pre- andBMC Public Health 2007, 7:35 http://www.biomedcentral.com/1471-2458/7/35Compared to men who did not report nitrite inhalant use,users were more likely to also report previous-year use ofother substances, including alcohol (96.4% vs. 82.4%),marijuana (73.2% vs. 53.7%), ecstasy (48.2% vs. 21.5%),crystal methamphetamine (39.5% vs. 21.1%), gammahydroxybutrate (GHB) (28.0% vs. 7.5%) and ketamine(22.2% vs. 8.8%) (all p < 0.001), as well as cocaine(39.5% vs. 23.0%, p = 0.002). Men who did and did notreport use of poppers were not significantly different withregard to previous-year use of cigarettes, crack cocaine,amphetamines (other than crystal methamphetamine),lysergic acid (LSD), or heroin. Compared to non-users,men who used nitrite inhalants were more likely to havemet sexual partners in bars (53.6% vs. 34.0%), on theInternet (45.5% vs. 27.1%), and in bathhouses (37.5% vs.17.6%) (all p < 0.001).Among 349 men (99%) who answered the question, pre-vious-year use of poppers during sexual encounters wasreported by 80 (22.9%). In the sample overall, men whoused poppers during sexual encounters were significantlymore likely to report unprotected receptive anal inter-course with a casual partner [25 (31%) of 80 vs. 26 (10%)of 269, OR = 4.0, 95% CI 2.2–8.3)]. However, this associ-ation could indicate that men who use poppers duringsexual encounters are more likely to have a casual partner,or are more likely to have anal intercourse with a casualpartner, or are more likely to have receptive than insertiveintercourse with a casual partner, or are less likely to use acondom during anal receptive encounters with casualpartners. To explore each of these possibilities, we pro-gressively restricted the sample to examine each associa-tion in turn.Compared to non-users, men reporting nitrite inhalantuse during sexual encounters had a 17-fold increased like-lihood of having casual partners (Table 1) and greaternumbers of them (median 8 vs. 4, p < 0.001). Among the234 men with casual partners, users of poppers hadgreater numbers of them during the previous year, includ-ing partners whose HIV status was unknown (median 7vs. 4, p = 0.0001), seronegative (median 5 vs. 2, p = 0.004)and seropositive (median 2 vs. 1, p = 0.072).Furthermore, among men with casual partners, those whoused poppers were almost seven times more likely thannon-users to report engaging in anal intercourse withthese partners (Table 1), the odds being similarlyincreased for insertive (OR = 2.9) as for receptive (OR =3.4) anal intercourse (Table 1). In contrast, once analyseswere restricted to those 148 and 133 men reporting inser-tive and receptive intercourse with casual partners, respec-tively, use of poppers was much less strongly and non-significantly associated with unprotected encounters ofeither sort (Table 1).In summary, use of poppers during sexual encounters wasstrongly associated both with having greater numbers ofcasual partners (of every HIV serostatus) and with engag-ing in anal intercourse with casual partners. However,among men who reported anal intercourse with casualpartners, use of poppers during these encounters was notTable 1: Characteristics of study participants, by self-reported previous-year use of poppers during sexual intercourse with casual partners (n = 349)Poppers use with casual partnersYes (n = 80)No. (%)No (n = 269)No. (%)Odds Ratio (95% CI)Has casual partner(s) 75 (96.2) 159 (59.1) 17.3 (5.4–87.5)No casual partner(s) 3 (3.9) 110 (40.9)Any anal intercourse with casual partner 70 (93.3) 103 (67.3) 6.8 (2.5–22.8)No anal intercourse with casual partner 5 (6.7) 50 (32.7)Receptive anal intercourse (RAI) with casual partner 58 (77.3%) 75 (50.0%) 3.4 (1.8–6.8)No RAI with casual partner 17 (22.7%) 75 (50.0%)Unprotected RAI with casual partner 25 (43.1) 26 (34.7) 1.4 (0.7–3.1)No unprotected RAI with casual partner 33 (56.9) 49 (65.3)Insertive anal intercourse (IAI) with casual partner 60 (80.0) 88 (57.9) 2.9 (1.5–6.0)No IAI with casual partner 15 (20.0) 64 (42.1)Unprotected IAI with casual partner 29 (48.3) 29 (33.0) 1.9 (0.9–3.9)Page 3 of 6(page number not for citation purposes)No unprotected IAI with casual partner 31 (51.7) 59 (67.1)BMC Public Health 2007, 7:35 http://www.biomedcentral.com/1471-2458/7/35significantly associated with non-use of condoms duringthese encounters.With regular partners, associations between the use ofpoppers and unprotected sexual behaviours were mark-edly different. In the overall sample, use of poppers dur-ing these encounters was associated with neither insertivenor receptive unprotected anal intercourse [26 (32.5%) of80 vs. 105 (39.0%) of 269, OR = 0.8, 95% CI 0.4–1.3 and30 (37.5%) of 80 vs. 108 (40.2%) of 269, OR = 0.9, 95%CI 0.5–1.5, respectively]. Similarly, in analyses progres-sively restricted like those used to examine sexual behav-iours with casual partners, use of poppers duringencounters with regular partners was not associated withany of the behaviours measured, except for a negativeassociation with unprotected insertive anal intercourse(Table 2).DiscussionIn the present study, we investigated use of nitrite inha-lants in a large, community-recruited cohort of youngMSM during a period of rapidly increasing HIV incidencein British Columbia. We found that nearly one third ofmen reported using poppers during the previous year andthat nearly one in four reported using poppers during sex-ual encounters. Men who used poppers during sexualencounters were much more likely than non-users to havecasual partners; to have greater numbers of casual partnerswhose HIV serostatus was positive or unknown; and tohave anal intercourse with casual partners. However,among men who engaged in receptive and insertive analintercourse with their casual partners, the use of poppersduring these encounters was not significantly associatedwith the encounter being unprotected. Thus, amongyoung MSM we studied, reported use of poppers duringsexual encounters was a very strong indicator of engagingin anal intercourse with high-risk casual partners but nota significant determinant of condom use per se.The prevalence of nitrite use in our cohort is similar to the25–35% reported in the small number of related studiesof MSM published since the introduction of highly activeantiretroviral therapy [4,8,10,18-20]. It is particularlynoteworthy that the prevalence of nitrite use we observedin 2002–2004 appears unchanged from that reported bythe same cohort in 1995–1996 (34%); by comparison,the prevalence of nitrite use in an independent cohort ofMSM in Vancouver in 1985 was 43% [21].As in previous studies, we observed a strong associationbetween use of poppers and unprotected anal intercourse[4,10,18-20]. Unlike previous studies however, we pro-gressively restricted analyses to determine whether use ofnitrites is merely an indicator of having anal intercoursewith casual sexual partners or a determinant of condomuse per se; our results are more consistent with the formerthan the latter.HIV-seronegative MSM in our cohort who use popperswere more likely than non-users to engage in anal inter-course with casual partners, including those whose HIVserostatus is positive or unknown. Previous studies sug-Table 2: Characteristics of study participants, by self-reported previous-year use of poppers during sexual intercourse with regular partners (n = 349)Poppers use with regular partnersYes (n = 80) No. (%)No (n = 269) No. (%)Odds Ratio (95% CI)Has regular sex partner 54 (67.5) 184 (68.4) 1.0 (0.5–1.7)No regular sex partner 26 (32.5) 85 (31.6)Any anal intercourse with regular partner 51 (94.4) 154 (86.5) 2.6 (0.8–14.3)No anal intercourse with regular partner 3 (5.6) 24 (13.5)Receptive anal intercourse (RAI) with regular partner 46 (85.2) 140 (79.6) 1.5 (0.6–3.9)No RAI with regular partner 8 (14.8) 36 (20.5)Unprotected RAI with regular partner 30 (65.2) 108 (77.1) 0.6 (0.3–1.2)No unprotected RAI with regular partner 16 (34.8) 32 (22.9)Insertive anal intercourse (IAI) with regular partner 45 (83.3) 131 (75.3) 1.6 (0.7–4.1)No IAI with regular partner 9 (16.7) 43 (24.7)Unprotected IAI with regular partner 26 (57.8) 105 (80.2) 0.3 (0.2–0.8)Page 4 of 6(page number not for citation purposes)No unprotected IAI with regular partner 19 (42.2) 26 (19.9)BMC Public Health 2007, 7:35 http://www.biomedcentral.com/1471-2458/7/35gest that poppers confer an increased risk for HIV serocon-version via a physiological mechanism: increased risk forinfection following sexual exposure to the virus. Together,these studies suggest that the high risk for HIV seroconver-sion among MSM who use poppers reflects a synergismbetween two risks: more frequent encounters withinfected partners and a higher probability of infection fol-lowing each exposure.Nitrite inhalant use by men in our study occurred duringa rapid increase in HIV diagnoses among MSM in BC,underscoring the urgent need to reduce use of these sub-stances. It is noteworthy that others estimate that up to28% of contemporary HIV infections among MSM may beattributed to use of nitrite inhalants; this estimate reflectsboth the strength of the association with HIV seroconver-sion and the prevalence of nitrate inhalant use amongMSM [8]. Most studies report a somewhat higher risk forHIV seroconversion associated with the use of metham-phetamine than with the use of poppers. We wish toemphasize that the greater prevalence of poppers use indi-cates that in most settings, more incident HIV infectionsamong MSM can be attributed to use of nitrite inhalantsthan to use of methamphetamine.Strengths of the present study include our community-based recruitment of a large sample of young MSM; ourdistinction between any use of poppers and use duringsexual encounters specifically, between casual and regularpartners, and between insertive versus receptive anal inter-course; our assessment of perceived HIV serostatus of sex-ual partners; and the precision with which we relate use ofnitrite inhalants and use of condoms during sexualencounters with casual partners. Our study also has sev-eral limitations that should be kept in mind. High-risksexual and substance use behaviours are self-reported andsubject to under-reporting. Ours was not a random sam-ple of MSM in Vancouver and these results may not applyto other MSM, particularly those who are older or HIV-seropositive. We did not measure and so are unable torelate use of poppers with less commonly reported sexualbehaviours (for example, fisting and group sex) or withuse of condoms during specific acts of sexual intercourse.The latter limitation is common to all but a handful ofstudies that relate high-risk sexual behaviours and druguse [5].ConclusionIn summary, we report a disturbingly high prevalence ofnitrite inhalant use among young MSM during a period ofrapidly increasing HIV incidence in British Columbia. Ourresults, together with those from previous studies, suggestnitrite inhalant use by MSM is associated with a synergyanal intercourse with an infected partner and in addition,a higher probability of infection following each suchexposure. Rapid assessments are needed to determinewhether MSM are aware of HIV-related risks associatedwith use of poppers. Efforts to reduce the use of nitriteinhalants during sexual encounters should be considereda high-priority HIV prevention strategy for MSM.Competing interestsThe author(s) declare that they have no competing inter-ests.Authors' contributionsTML conceived and designed the study, supervised dataanalyses and revised drafts of the manuscript. KMreviewed literature, produced the first draft of the manu-script and, with KC, performed data analyses and manu-script revisions. RSH reviewed a draft of the manuscript.All authors read and approved the final version of themanuscript.AcknowledgementsWe thank the Vanguard Project participants and study team members Mary Lou Miller and Arn Schilder. We also thank Bonnie Devlin and Marcus Greatheart for administrative support. Drs. Lampinen and Hogg are sup-ported by the Michael Smith Foundation for Health Research.References1. 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Craib KJ, Weber AC, Cornelisse PG, Martindale SL, Miller ML,Schechter MT, Strathdee SA, Schilder A, Hogg RS: Comparison ofsexual behaviors, unprotected sex, and substance usebetween two independent cohorts of gay and bisexual men.AIDS 2000, 14(3):303-11.Pre-publication historyThe pre-publication history for this paper can be accessedhere:http://www.biomedcentral.com/1471-2458/7/35/prepubyours — you keep the copyrightSubmit your manuscript here:http://www.biomedcentral.com/info/publishing_adv.aspBioMedcentralPage 6 of 6(page number not for citation purposes)


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