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Serosorting and recreational drug use are risk factors for diagnosis of genital infection with chlamydia and gonorrhoea among HIV-positive men who have sex with men: results from a clinical cohort in Ontario, Canada
  1. Ramandip Grewal1,
  2. Vanessa G Allen2,
  3. Sandra Gardner3,4,
  4. Veronika Moravan5,
  5. Darrell H S Tan6,7,8,
  6. Janet Raboud3,7,
  7. Ahmed M Bayoumi1,6,7,8,
  8. Rupert Kaul6,
  9. Tony Mazzulli2,11,
  10. Frank McGee12,
  11. Sean B Rourke1,5,13,
  12. Ann N Burchell1,3,14
  13. in collaboration with the OHTN Cohort Study Research Team
    1. 1Centre for Research on Inner City Health, Li Ka Shing Knowledge Institute, St. Michael's Hospital, Toronto, Ontario, Canada
    2. 2Public Health Laboratories, Public Health Ontario, Toronto, Ontario, Canada
    3. 3Dalla Lana School of Public Health, University of Toronto, Toronto, Ontario, Canada
    4. 4Baycrest Health Science, Toronto, Ontario, Canada
    5. 5Ontario HIV Treatment Network, Toronto, Ontario, Canada
    6. 6Department of Medicine, University of Toronto, Toronto, Ontario, Canada
    7. 7Toronto General Research Institute, University Health Network, Toronto, Ontario, Canada
    8. 8Division of Infectious Diseases, St. Michael's Hospital, Toronto, Ontario, Canada
    9. 9Institute of Health Policy, Management and Evaluation, University of Toronto, Toronto, Ontario, Canada
    10. 10Division of General Internal Medicine, St. Michael's Hospital, Toronto, Ontario, Canada
    11. 11Department of Microbiology, Mount Sinai Hospital/University Health Network, Toronto, Ontario, Canada
    12. 12AIDS Bureau, Ontario Ministry of Health and Long-Term Care, Toronto, Ontario, Canada
    13. 13Department of Psychiatry, University of Toronto, Toronto, Ontario, Canada
    14. 14Department of Family and Community Medicine, St. Michael's Hospital, Toronto, Ontario, Canada
    1. Correspondence to Dr Ann N Burchell, Department of Family and Community Medicine and Li Ka Shing Knowledge Institute, St. Michael's Hospital, 30 Bond Street, Toronto, Ontario, Canada M5B 1W8; burchella{at}smh.ca

    Abstract

    Objectives Rates of chlamydia and gonorrhoea have been rising in urban centres in Canada, particularly among HIV-positive men who have sex with men (MSM). Our objective was to identify behavioural risk factors for diagnosis with chlamydia and gonorrhoea in this population, with a focus on the HIV status of sexual partners.

    Methods The OHTN Cohort Study follows people in HIV care across Ontario. We restricted the analysis to 1997 MSM who completed questionnaires in 2010–2013 at one of seven clinics that submit all chlamydia and gonorrhoea tests to the provincial public health laboratory; we obtained test results via record linkage. We estimated cumulative incidences using Kaplan–Meier methods and identified risk factors for diagnosis of a composite outcome (chlamydia or gonorrhoea infection) using Cox regression.

    Results At follow-up, there were 74 new chlamydia/gonorrhoea diagnoses with a 12-month cumulative incidence of 1.7% (95% CI 1.1% to 2.2%). Risk factors for chlamydia/gonorrhoea diagnosis were: 5+ HIV-positive partners (HR=3.3, 95% CI 1.4 to 7.8; reference=none) and recreational drug use (HR=2.2, 95% CI 1.2 to 3.9).

    Conclusions Heightened risks with recreational drug use and multiple HIV-positive partners suggest that chlamydia/gonorrhoea may have achieved high prevalence in certain sexual networks among HIV-positive MSM. Interventions to promote safer sex and timely testing among MSM are needed.

    • CHLAMYDIA INFECTION
    • GAY MEN
    • GONORRHOEA
    • HIV
    • SEXUAL BEHAVIOUR

    This is an Open Access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/

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    Introduction

    Rates of chlamydia and gonorrhoea have risen in urban centres in Canada including an increase in case reports among men who have sex with men (MSM).1 Coinfection with HIV is particularly concerning because sexually transmitted infections (STIs) can increase likelihood of HIV transmission.1 In Ontario, Canada, we previously reported demographic and clinical risk factors for new chlamydia and gonorrhoea diagnoses among an HIV clinical cohort followed from 2008 to 2011.2 Risk was highest among MSM, particularly among younger MSM and (for gonorrhoea) among MSM with unsuppressed viral load, with little variation between ethnic groups.2 However, full characterisation of risk requires examination of behavioural risk factors since sexual behaviour and prevalence in sexual networks drive STI risk. ‘Serosorting’, selecting sexual partners of the same HIV serostatus, could raise STI risk since condoms may be used less frequently, which could concentrate infection in sexual networks of HIV-positive persons.3 Recreational drug use has also been linked to sexual risk taking.1 ,4 ,5 Our objective was to extend our previous analysis by longitudinally exploring behavioural risk factors for diagnoses of genital chlamydia and gonorrhoea infection among HIV-positive MSM attending HIV care in Ontario, specifically focusing on the risks associated with serosorting and recreational drug use.

    Methods

    We analysed data from the Ontario HIV Treatment Network Cohort Study (OCS) which follows persons attending 10 HIV clinics across Ontario. The province has publicly funded, universal access to medically necessary healthcare. The OCS has been described in detail elsewhere6 and received ethical approval from the University of Toronto HIV Research Ethics Board (protocol reference 23954) and participating sites. Participation is voluntary. Data were collected through chart review, annual interviews and record linkage with the Public Health Ontario Laboratories (PHOL). At PHOL, simultaneous cotesting of chlamydia and gonorrhoea urine specimens was done by nucleic acid amplification testing using the Gen-Probe Aptima assay (Gen-Prose, San Diego, California, USA). Canadian guidelines recommend chlamydia and gonorrhoea testing annually for MSM at ongoing risk, regardless of HIV status.1

    Our focus was on sexual behaviour and recreational drug use risk factors, adjusting for age, region and time-updated viral load as potential confounders. Men reported recreational drug use in face-to-face interviews. Next, they self-completed a computerised sexual behaviour questionnaire without interviewers present.

    As of 12/2013, there were 6408 enrolees. Our analysis included 1997 male participants reporting non-heterosexual orientation or sex with men as an HIV risk factor; self-completed at least one sexual behaviour questionnaire between 2010 and 2013 and attended one of seven clinics that submitted all chlamydia and gonorrhoea tests to PHOL, the primary provider for chlamydia and gonorrhoea tests for sexual health clinics (HIV specialty and primary care clinics may also send specimens to private laboratories).

    We conducted all statistical analyses using SAS V.9.3 (SAS Institute, Cary, North Carolina, USA). p Values were two-sided and statistical significance was determined using the p value of <0.05. We used Kaplan–Meier methods to estimate the cumulative incidence proportions tested for or diagnosed with chlamydia or gonorrhoea following completion of the first sexual behaviour questionnaire. As previously done, diagnosis rates were calculated among tested and untested participants2 thus underestimating true incidence since asymptomatic infections among those untested are excluded from the numerator.

    For risk factor analysis, we grouped chlamydia and gonorrhoea into a composite outcome to improve statistical power and because their modes of transmission and clinical/public health implications are similar; HR estimates for separate chlamydia and gonorrhoea outcomes were not meaningfully different. For men diagnosed more than once, we selected the earliest event, which occurred rarely. We excluded participants with missing data (1.3% of observations) and two cases with zero event times. Men with no events were censored using the earliest of the dates of loss to follow-up, death or 31 December 2013.

    Results

    At completion of their first sexual behaviour questionnaire, men were aged 48 years, on average (table 1). The median number of years since HIV diagnosis was 18 (IQR 10–24). The majority (64.4%) were sexually active in the preceding 3 months, whereas a minority (20.9%) reported recreational drug use (table 1).

    Table 1

    Characteristics of HIV-positive men who have sex with men (MSM) at completion of their first sexual behaviour questionnaire, OHTN Cohort Study, 2010–2013

    Men were followed a median of 2.9 years (IQR 1.8–3.3) for a sum of 5833 person-years. The Kaplan–Meier cumulative probabilities of testing for chlamydia/gonorrhoea were 24.6% at 12 months and 33.1% at 24 months. In all, 35.1% (700/1997) were tested over the entire course of follow-up. The majority of tests were ordered by participating HIV clinics (87.6%) with only 3.0% ordered by sexual health/STI/community health clinics and 9.3% by other health providers. Stratum-specific 12-month testing probabilities ranged from 15.8% among sexually inactive men to 42.5% among men reporting 5+ partners (table 2).

    Table 2

    Behavioural risk factors for a diagnosis of genital chlamydia/gonorrhoea infection at follow-up among HIV-positive MSM, OHTN Cohort Study, 2010–2013

    At follow-up, 41, 46 and 74 men were diagnosed with chlamydia, gonorrhoea and either pathogen, respectively. The Kaplan–Meier 12-month cumulative incidence proportions were 1.0% (95% CI 0.6% to 1.4%) for chlamydia, 1.2% (95% CI 0.7% to 1.7%) for gonorrhoea and 1.7% (95% CI 1.1% to 2.2%) for the composite outcome. Among cases, 53% (39 of 74) had a history of syphilis compared with 9.5% among non-cases.

    Multiple sex partners and recreational drug use were significant risk factors for diagnosis (table 2). Risk was elevated among men who reported 5+ HIV-positive partners but not for multiple HIV-negative/unknown partners in the adjusted model. Recreational drug use doubled risk. Point estimates indicated elevated risk with anal sex (regardless of condom use); however, there was inadequate precision to indicate statistical significance.

    Discussion

    Among gay and other MSM in an Ontario HIV-positive clinical cohort from 2010 to 2013, the 12-month cumulative incidence of a genital chlamydia/gonorrhoea diagnosis was substantial at 1.7% (95% CI 1.1% to 2.2%). Risk factors were having multiple HIV-positive partners and recreational drug use. Strengths of our analysis include a large sample, tests from a single laboratory and 98% completion rate of the sexual behaviour questionnaire. To our knowledge, our study is the first to compare longitudinal chlamydia/gonorrhoea diagnosis rates from multiple clinics among HIV-positive MSM by partners' HIV status.

    There are limitations. Canadian and US guidelines recommend extragenital testing if engaging in oral or rectal intercourse2 yet such tests were rarely done in our setting, meaning we could not identify rectal or pharyngeal infection risk factors. A 3-month time frame for sexual behaviours mitigated recall error but resulted in unmeasured behaviour between annual questionnaires, potentially explaining the non-zero diagnosis rate among men reporting no partners. Measurement of recreational drug use via face-to-face interviews may have introduced social desirability bias. Voluntary participation may have introduced selection bias. The OCS under-represents recent diagnoses; however, participants are generalisable to HIV-positive persons in Ontario according to sex, region, age at diagnosis and HIV exposure category.7

    Recreational drug use was also a risk factor for chlamydia/gonorrhoea diagnosis in cross-sectional prevalence studies executed in clinics in Madrid and the Netherlands,4 ,5 which was demonstrated for genital, rectal and pharyngeal infections. The Netherlands study reported multiple partners as a risk factor for chlamydia, gonorrhoea and syphilis combined; however, the association became null when syphilis and chlamydia/gonorrhoea were analysed separately. The Madrid study reported risk associated with serosorting, defined as having a stable HIV-positive partner, whereas in our setting having multiple HIV-positive partners was most important.

    Only 5% of men reported 5+ HIV-positive partners, but risk was highest in this group, with 12-month diagnosis rates of 8.3% (95% CI 3.1% to 13.5%). After adjustment for HIV-positive partners, no additional risk was associated with having multiple HIV-negative/unknown partners. We propose three hypotheses. First, men may use condoms less frequently for ‘poz’ sex; however, we observed similar risks between condom users and non-users. Second, HIV-positive men may choose receptive anal sex with HIV-negative partners reducing their risk of genital infection;3 however, information on seropositioning was unavailable. Third, chlamydia/gonorrhoea may have achieved high prevalence in sexual networks among HIV-positive MSM seeking other positive men, and these networks may have low connectedness with HIV-negative MSM. That half of cases had a history of syphilis suggests presence of a core group where bacterial STIs are concentrated. In a study of German MSM, HIV-positive serosorters had threefold higher odds of bacterial STIs versus those with serodiscordant partners.8 Together with our finding of heightened risk for recreational drug use, we recommend further investigation of how ‘scene’ participation (eg, poz parties, bathhouses) influences STI risk.1 Further, as more HIV-negative men use pre-exposure prophylaxis for HIV prevention, sexual networks between HIV-negative and HIV-positive men may become more connected if serosorting becomes less common,9 resulting in more population-level transmission of bacterial STI.

    Our findings have implications for chlamydia/gonorrhoea prevention, testing and treatment among HIV-positive MSM. Non-zero diagnosis rates among men reporting condom-protected anal sex suggests some acquisition through unmeasured risk practices such as oral sex;1 sexual education messages should emphasise the differences in bacterial STI transmission routes compared with HIV. Testing was below recommended guidelines; the proportion of untested men reporting high-risk behaviours was substantial. We strongly encourage rectal testing which could detect up to 80% more asymptomatic infections.5 There is a need to design and deliver interventions to promote safer sex and testing in ways that are engaging, non-stigmatising and acceptable for men at risk. Potential clinic-based interventions to optimise testing include algorithms targeting high-risk patients, clinical decision support systems, automated patient/provider alerts and laboratory technologies to improve case detection.10

    Acknowledgments

    The authors acknowledge the contribution of the late Dr Robert S Remis for guidance on earlier versions of this work. Further, we gratefully acknowledge all of the people living with HIV who volunteered to participate in the OHTN Cohort Study and the work and support of past and present members of the Governance Committee: Adrian Betts, Anita C. Benoit, Breklyn Bertozzi, Les Bowman, Lisungu Chieza, Tracey Conway, Patrick Cupido (Chair), Tony Di Pede, Brian Finch, Michael J. Hamilton, Brian Huskins, Rick Kennedy, Ken King, Nathan Lachowsky, Joanne Lindsay, Shari Margolese, Mark McCallum, John McTavish, Colleen Price, Lori Stoltz, Darien Taylor, Rosie Thein, and Drs AMB, Evan Collins, Curtis Cooper, Clemon George, Troy Grennan, Claire Kendall, and Greg Robinson. We thank all the interviewers, data collectors, research associates and coordinators, nurses and physicians who provide support for data collection and extraction. The authors wish to thank the OCS staff for data management, IT support, and study coordination (Madison Kopansky-Giles, Jason Globerman, Beth Rachlis, Robert Hudder, Gokul Kalaimani, Lucia Light, Veronika Moravan, Nahid Qureshi) and Public Health Ontario Laboratories for supporting record linkage with the HIV viral load, chlamydia and gonorrhoea test databases.

    References

    View Abstract

    Footnotes

    • Handling editor Jackie A Cassell

    • Collaborators The OHTN Cohort Study Team consists of Dr SBR (Principal Investigator), University of Toronto and OHTN; Dr Sergio Rueda, CAMH; Dr ANB, Dr AMB, Dr Kevin Gough and Dr DHST, St Michael’s Hospital; Dr Jeffrey Cohen, Windsor Regional Hospital; Dr Curtis Cooper, Ottawa General Hospital; Dr Don Kilby, University of Ottawa Health Services; Dr Mona Loutfy and Dr Fred Crouzat, Maple Leaf Medical Clinic; Dr Anita Rachlis and Dr Nicole Mittmann, Sunnybrook Health Sciences Centre; Dr JR and Dr Irving Salit, Toronto General Hospital; Dr Edward Ralph, Dr Michael Silverman, St Joseph’s Health Care; Dr Roger Sandre, Sudbury Regional Hospital; and Dr Gerald Evans and Dr Wendy Wobeser, Hotel Dieu Hospital.

    • Contributors RG conducted the analysis and wrote the manuscript. ANB was the principal investigator who conceived the project, obtained funding and contributed to the direction of the analysis and manuscript writing; she is the guarantor. ANB and SBR directed data collection at clinic sites. VGA and TM directed laboratory analysis at the PHOL and its interpretation. SG, VM and JR provided statistical expertise. AMB, RK, DHST and FM, contributed to the study protocol and guided interpretation. All authors provided critical input into the analysis, read an earlier version of the paper, provided substantive feedback and approved the final paper.

    • Funding This work was supported by Canadian Institutes of Health Research (CIHR) operating grant 111146, CIHR New Investigator awards to ANB and to DHST, an OHTN Chair and support from the Toronto and Western Hospital Foundation Skate the Dream Fund for JR and a Fondation Baxter and Alma Ricard Chair in Inner City Health at St Michael's Hospital for AMB. The OHTN Cohort Study is funded by the AIDS Bureau, Ontario Ministry of Health and Long-Term Care.

    • Disclaimer The opinions, results and conclusions are those of the authors and no endorsement by the Ontario HIV Treatment Network or Public Health Ontario is intended or should be inferred.

    • Competing interests None declared.

    • Ethics approval University of Toronto HIV Research Ethics Board (protocol reference 23954).

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

    • Data sharing statement The OHTN may authorise the collection, use and disclosure of OCS data for the purpose of scholarly research if the proposal for the research project has been reviewed and approved and the research project principal investigator and all other members of the research project team have signed a researcher's agreement with the OHTN and adhere to all relevant OCS data and research policies.

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