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Association of HIV Preexposure Prophylaxis With Incidence of Sexually Transmitted Infections Among Individuals at High Risk of HIV Infection

Educational Objective
To understand the relationship of HIV preexposure prophylaxis to the incidence of bacterial sexually transmitted infections.
1 Credit CME
Key Points

Question  Is the use of HIV preexposure prophylaxis (PrEP) associated with increased risk of sexually transmitted infections (STIs) among individuals at high risk of HIV infection?

Findings  In this longitudinal study of 2981 mostly gay and bisexual men who received daily HIV preexposure prophylaxis, STI incidence was 91.9 per 100 person-years, with 736 participants (25%) accounting for 2237 (76%) of all STIs. Among 1378 participants with preenrollment STI testing data available, receipt of PrEP after study enrollment was associated with an increased incidence of STIs compared with preenrollment (adjusted incidence rate ratio, 1.12).

Meaning  Findings suggest the importance of frequent testing for STIs among gay and bisexual men using PrEP.

Abstract

Importance  Emerging evidence suggests that risk of bacterial sexually transmitted infections (STIs) increases among gay and bisexual men following initiation of HIV preexposure prophylaxis (PrEP).

Objective  To describe STI incidence and behavioral risk factors among a cohort of predominantly gay and bisexual men who use PrEP, and to explore changes in STI incidence following PrEP commencement.

Design, Setting, and Participants  The Pre-exposure Prophylaxis Expanded (PrEPX) Study, a multisite, open-label intervention study, was nested within the Australian Collaboration for Coordinated Enhanced Sentinel Surveillance (ACCESS) clinic network. A total of 4275 participants were enrolled (July 26, 2016–April 1, 2018) in Victoria, Australia. Of these, 2981 enrolled at 5 ACCESS clinics (3 primary care, 1 sexual health, and 1 community-based HIV rapid testing service), had at least 1 follow-up visit, and were monitored until April 30, 2018.

Exposures  Upon enrollment, participants received daily oral tenofovir disoproxil fumurate and emtricitabine for HIV PrEP, quarterly HIV and STI testing, and clinical monitoring.

Main Outcomes and Measures  The primary outcome was incidence of chlamydia, gonorrhea, or syphilis. Incidence rates and hazard ratios describing behavioral risk factors of STI diagnosis were calculated. Incidence rate ratios (IRRs), adjusted for change in testing frequency, described changes in STI incidence from 1-year preenrollment to study follow-up among participants with preenrollment testing data (n = 1378).

Results  Among the 2981 individuals (median age, 34 years [interquartile range, 28-42]), 98.5% identified as gay or bisexual males, 29% used PrEP prior to enrollment, 89 (3%) withdrew and were censored at date of withdrawal, leaving 2892 (97.0%) enrolled at final follow-up. During a mean follow-up of 1.1 years (3185.0 person-years), 2928 STIs were diagnosed among 1427 (48%) participants (1434 chlamydia, 1242 gonorrhea, 252 syphilis). STI incidence was 91.9 per 100 person-years, with 736 participants (25%) accounting for 2237 (76%) of all STIs. Among 2058 participants with complete data for multivariable analysis, younger age, greater partner number, and group sex were associated with greater STI risk, but condom use was not. Among 1378 participants with preenrollment testing data, STI incidence increased from 69.5 per 100 person-years prior to enrollment to 98.4 per 100 person-years during follow-up (IRR, 1.41 [95% CI, 1.29-1.56]). After adjusting for testing frequency, the increase in incidence from 1 year preenrollment to follow-up was significant for any STI (adjusted IRR, 1.12 [95% CI, 1.02-1.23]) and for chlamydia (adjusted IRR, 1.17 [95% CI, 1.04-1.33]).

Conclusions and Relevance  Among gay and bisexual men using PrEP, STIs were highly concentrated among a subset, and receipt of PrEP after study enrollment was associated with an increased incidence of STIs compared with preenrollment. These findings highlight the importance of frequent STI testing among gay and bisexual men using PrEP.

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Article Information

Corresponding Author: Michael W. Traeger, MSc, Burnet Institute, 85 Commercial Rd, Melbourne, Victoria 3004, Australia (michael.traeger@burnet.edu.au).

Accepted for Publication: March 3, 2019.

Author Contributions: Mr Traeger and Dr Wright had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Drs Wright and Stoové, as co-senior authors, contributed equally to this article. Coordination of the Australian Collaboration for Coordinated Enhanced Sentinel Surveillance (ACCESS): Drs Stoové and Hellard.

Concept and design: Traeger, Fairley, Chang, Lal, Mak, Batrouney, Lockwood, Stoové, Wright.

Acquisition, analysis, or interpretation of data: Traeger, Cornelisse, Asselin, Price, Roth, Willcox, Tee, Fairley, Chang, Armishaw, Vujovic, Penn, Cundill, Forgan-Smith, Gall, Pickett, Lal, Mak, Spelman, Nguyen, Murphy, Ryan, El-Hayek, West, Ruth, Lockwood, Hoy, Hellard, Stoové, Wright.

Drafting of the manuscript: Traeger, Fairley, Forgan-Smith, West, Stoové, Wright.

Critical revision of the manuscript for important intellectual content: Cornelisse, Asselin, Price, Roth, Willcox, Tee, Fairley, Chang, Armishaw, Vujovic, Penn, Cundill, Gall, Pickett, Lal, Mak, Spelman, Nguyen, Murphy, Ryan, El-Hayek, Ruth, Batrouney, Lockwood, Hoy, Hellard, Stoové, Wright.

Statistical analysis: Traeger, Tee, Spelman, Stoové.

Obtained funding: Price, Tee, West, Hellard, Wright.

Administrative, technical, or material support: Cornelisse, Asselin, Price, Tee, Fairley, Chang, Forgan-Smith, Gall, Pickett, Lal, Nguyen, Ryan, El-Hayek, West, Ruth, Batrouney, Lockwood, Hellard, Stoové, Wright.

Supervision: Chang, Lal, Mak, Stoové, Wright.

Other - Recruitment, data acquisition: Tee.

Other - Mentoring and management of key authors: Hellard.

Other - Principal investigator of the PrEPX Study: Wright.

Conflict of Interest Disclosures: Dr Cornelisse reports receipt of speaker’s fees and conference assistance from Gilead Sciences, speaker’s fees and conference assistance from Merck Sharp & Dohme, and advisory board fees from ViiV Healthcare outside the submitted work. Dr Stoové reports receipt of grants from the Commonwealth Department of Health and the National Health and Medical Research Council during the conduct of the study. Mr Asselin reports receipt of grants from the Australian Department of Health and the Victorian Department of Health and Human Services during the conduct of the study. Mr Price reports receipt of grants from the Department of Health Victorian government, Thorne Harbour Health, and Alfred Health during the conduct of the study. Dr Fairley reports receipt of grants from the Department of Health and Human Services during the conduct of the study. Dr Chang reports receipt of grants from the Australian National Health and Medical Research Council during the conduct of the study. Dr Vujovic reports receipt of nonfinancial support from Alfred Health and Thorne Harbour Health; and grants from the Department of Health Victorian government during the conduct of the study. Dr Ryan reports receipt of grants from Alfred Health, the Victorian government, and Thorne Harbour Health during the conduct of the study. Ms El-Hayek reports receipt of grants from the Australian Department of Health during the conduct of the study. Mr West reports receipt of grants from Victorian Department of Health and Human Services during the conduct of the study. Mr Lockwood reports receipt of grants from the Victorian government and Thorne Harbour Health during the conduct of the study. Dr Hoy reports receipt of grants from the Victorian government during the conduct of the study. Dr Hellard reports receipt of grants from Gilead, AbbVie, and Bristol-Myers Squibb during the conduct of the study. Dr Wright reports receipt of grants from the Victorian government, the Tasmanian government, Thorne Harbour Health, and the South Australian government during the conduct of the study; other from Gilead Sciences (free study drug, compensation to her institution for chairing a nursing education session and for attending an advisory board meeting, and uncompensated attendance for attending 2 Gilead meetings regarding listing of Truvada on the Australian pharmaceutical benefits scheme); grants from Gilead Science and Merck Sharp & Dohme outside the submitted work; and financial support from Gilead Sciences, Abbott Laboratories, Janssen-Cilag, Boehringer Ingelheim, ViiV Healthcare, and Merck Sharp & Dohme. No other disclosures were reported.

Funding/Support: The Pre-exposure Prophylaxis Expanded (PrEPX) Study was supported by funding from the Victorian Department of Health and Human Services, Thorne Harbour Health, and Alfred Health. Dr Cornelisse receives a stipend from the research training program of the Australian government’s Department of Education and Training. Dr Stoové is supported by a National Health and Medical Research Council (NHMRC) senior research fellowship. Dr Chang is supported by an NHMRC early career fellowship (APP1092160). The Burnet Institute gratefully acknowledges support received from the Victorian Operational Infrastructure Support Program. Gilead Sciences donated study drug to the VicPrEP study (precursor to this study).

Role of the Funder/Sponsor: Individuals from the Victorian Department of Health and Human Services, Alfred Health, and Thorne Harbour Health were PrEPX Study coinvestigators and are coauthors on this article. They had a role in the design, review, and approval of the manuscript and in the decision to submit the manuscript for publication. None of the other funders were involved in the design, review, or approval of the manuscript.

The PrEPX Study Team: Edwina J. Wright, MBBS, PhD (Department of Infectious Diseases, Alfred Health and Monash University, Melbourne, Victoria, Australia; Disease Elimination Program, Burnet Institute, Melbourne, Victoria, Australia; and The Peter Doherty Institute of Infection and Immunity, University of Melbourne, Melbourne, Victoria, Australia), Brian Price, MBA (Department of Infectious Diseases, Alfred Health and Monash University, Melbourne, Victoria, Australia), Mark A. Stoové, Ph D (Disease Elimination Program, Burnet Institute, Melbourne, Victoria, Australia; and School of Public Health and Preventive Medicine, Monash University, Melbourne, Victoria, Australia), Simon Ruth, MSSc (Thorne Harbour Health, Melbourne, Victoria, Australia), Colin Batrouney, BA (Thorne Harbour Health, Melbourne, Victoria, Australia), John T. Lockwood, BN (Department of Infectious Diseases, Alfred Health and Monash University, Melbourne, Victoria, Australia), Michael West, BA (Sexual Health and Viral Hepatitis Service, Department of Health and Human Services, Government of Victoria, Melbourne, Victoria, Australia), Dean A. Murphy, PhD (Department of Gender and Cultural Studies, University of Sydney, Sydney, New South Wales, Australia; and The Kirby Institute, University of New South Wales, Sydney, New South Wales, Australia), John de Wit, PhD (Centre for Social Research in Health, University of New South Wales, Sydney, New South Wales, Australia), Luxi Lal, B Pharm (Disease Elimination Program, Burnet Institute, Melbourne, Victoria, Australia; and Department of Infectious Diseases, Alfred Health and Monash University, Melbourne, Victoria, Australia), Jennifer Audsley, PhD (Department of Infectious Diseases, Alfred Health and Monash University, Melbourne, Victoria, Australia; and The Peter Doherty Institute for Infection and Immunity, The University of Melbourne and Royal Melbourne Hospital, Melbourne, Victoria, Australia), Christina C. Chang, MBBS, PhD (Department of Infectious Diseases, Alfred Health and Monash University, Melbourne, Victoria, Australia; and Central Clinical School, Monash University, Melbourne, Victoria, Australia), Carol El-Hayek, MEpi (Disease Elimination Program, Burnet Institute, Melbourne, Victoria, Australia), Anne Mak, BPharm (Department of Infectious Diseases, Alfred Health and Monash University, Melbourne, Victoria, Australia), Alison Duncan, BPharm (The Alfred, Alfred Health, Melbourne, Victoria, Australia), Joe Sasadeusz, MBBS, PhD (Royal Melbourne Hospital, Melbourne, Victoria, Australia; The Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria, Australia; and The Alfred, Alfred Health, Melbourne, Victoria, Australia), Brent Allan, MSocSc (Living Positive Victoria, Melbourne, Victoria, Australia), Michael Whelan, BA (PAN-PrEP Access Now, Melbourne, Victoria, Australia), Daniel McPhail, (PrEP’d For Change, Melbourne, Victoria, Australia), David Wilson, PhD (Burnet Institute, Melbourne, Victoria, Australia), Olga Vujovic, MBBS (Department of Infectious Diseases, Alfred Health and Monash University, Melbourne, Victoria, Australia), Martin Holt, PhD (Kirby Institute, University of New South Wales, Sydney, NSW, Australia), Chris Williams, (PrEP’d For Change, Melbourne, Victoria, Australia), Steve Wesselingh, BMBS, PhD (South Australian Health and Medical Research Institute, Adelaide, South Australia, Australia), James Ward, PhD (South Australian Health and Medical Research Institute, Adelaide, South Australia, Australia), Danny Gallant, MBBS (South Australian Health and Medical Research Institute, Adelaide, South Australia, Australia), Alison Ward, MBBS (Adelaide Sexual Health Centre, Adelaide, South Australia, Australia; and Royal Adelaide Hospital, Adelaide, South Australia, Australia), Alistair Chong, BSc (The Alfred, Alfred Health, Melbourne, Victoria, Australia; and University of Melbourne, Melbourne, Victoria, Australia), Katharine McKinnon, PhD (La Trobe University, Melbourne, Victoria, Australia), Kathleen E. Ryan, PhD (Disease Elimination Program, Burnet Institute, Melbourne, Victoria, Australia; and Department of Infectious Diseases, Alfred Health and Monash University, Melbourne, Victoria, Australia), Michael W. Traeger, MSc (Disease Elimination Program, Burnet Institute, Melbourne, Victoria, Australia), Christopher K. Fairley, MBBS, PhD (Melbourne Sexual Health Centre, Alfred Health, Melbourne, Victoria, Australia; and Central Clinical School, Monash University, Melbourne, Victoria, Australia), Ivette Aguirre, BPharm (The Alfred, Alfred Health, Melbourne, Victoria, Australia), Ban Kiem Tee, MBBS (Centre Clinic, Thorne Harbour Health, Melbourne, Victoria, Australia), Norman J. Roth, MBBS (Prahran Market Clinic, Melbourne, Victoria, Australia), Vincent J. Cornelisse, (Department of Infectious Diseases, Alfred Health and Monash University, Melbourne, Victoria, Australia; Melbourne Sexual Health Centre, Alfred Health, Melbourne, Victoria, Australia; Prahran Market Clinic, Melbourne, Victoria, Australia; and Central Clinical School, Monash University, Melbourne, Victoria, Australia), Jason Asselin, BSc (Disease Elimination Program, Burnet Institute, Melbourne, Victoria, Australia), Timothy Read, MBBS, PhD (Melbourne Sexual Health Centre, Alfred Health, Melbourne, Victoria, Australia), Richard Moore, MBBS (Northside Clinic, Melbourne, Victoria, Australia), Jeff Willcox, MBBS (Northside Clinic, Melbourne, Victoria, Australia), George Forgan-Smith, MBBS (ERA Health, Melbourne, Victoria, Australia), John Gall, MBBS, PhD (ERA Health, Melbourne, Victoria, Australia), Matthew Penn, MBBS (PRONTO! Clinic, Thorne Harbour Health, Melbourne, Victoria, Australia), Pauline Cundill, BM (PRONTO! Clinic, Thorne Harbour Health, Melbourne, Victoria, Australia), Helan Lau, BN (Prahran Market Clinic, Melbourne, Victoria, Australia; and Centre Clinic, Thorne Harbour Health, Melbourne, Victoria, Australia), Danielle Collins, BN (The Alfred, Alfred Health, Melbourne, Victoria, Australia), Sian Edwards, BN (Northside Clinic, Melbourne, Victoria, Australia), Susan Boyd, BN (Northside Clinic, Melbourne, Victoria, Australia), Claire Pickett, MBBS (Ballarat Community Health Centre, Ballarat, Victoria, Australia), Emma Paige, MBBS (The Alfred, Alfred Health, Melbourne, Victoria, Australia), Amanda Wade, MBBS, PhD (Geelong Hospital, Geelong, Victoria, Australia; and Barwon Health, Geelong, Victoria, Australia), Charlotte Bell, MBBS (Adelaide Sexual Health Centre, Adelaide, South Australia, Australia; and Royal Adelaide Hospital, Adelaide, South Australia, Australia), William Donohue, MBBS, MPH (O’Brien St Practice, Adelaide, South Australia, Australia), Samuel Elliot, MBBS (Riverside Family Medical Practice, St Marys, South Australia, Australia), Helen Calabretto, PhD (SHINE SA, South Australia, Australia), Louise Owen, MBBS (Sexual Health Service Tasmania, Tasmania, Australia; Clinic 60, Hobart, Tasmania, Australia; and Clinic 34, Launceston, Tasmania, Australia), Jenny Kelsall, BA (Harm Reduction Victoria, Victoria, Australia).

Additional Information: The authors acknowledge Jenny Kelsall, BA, a PrEPX Study team member, who died during the conduct of the study.

Additional Contributions: The authors wish to acknowledge PrEPX participants, the participating study clinics and pharmacies, the HIV-affected community of Victoria, and all human and animal participants of previous preexposure prophylaxis (PrEP) studies. The authors wish to acknowledge the excellent work of other researchers that we have not been able to cite in this publication.

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