Elsevier

The Lancet HIV

Volume 6, Issue 6, June 2019, Pages e396-e405
The Lancet HIV

Review
Epidemiology and prevention of sexually transmitted infections in men who have sex with men at risk of HIV

https://doi.org/10.1016/S2352-3018(19)30043-8Get rights and content

Summary

Since 2012, the increasingly widespread promotion and uptake of HIV treatment as prevention and pre-exposure prophylaxis in men who have sex with men has been associated with increased sexually transmitted infections (STIs). However, numbers of STI cases have been rising for more than 20 years and the introduction of biomedical HIV interventions cannot explain the majority of the rises in STIs. The increases appear to have occurred mostly because of gradual changes in behaviour over many years, coupled in some settings with more condomless anal intercourse, and as a result of the increased screening for previously undetected asymptomatic infections. If control of STIs is to be improved, then a far greater emphasis on increased use of existing effective STI control strategies will be required, in addition to the investigation of new interventions. Central to effective STI control is accessible clinical care and screening services, which are currently inadequate in most settings. Insufficient action carries a risk of increased STI epidemics, including of newly resistant organisms.

Introduction

Two biomedical interventions have been introduced in the past decade to prevent HIV, treatment as prevention (TasP) and pre-exposure prophylaxis (PrEP), which have proven to be remarkably effective.1, 2 To our knowledge, no cases have been reported of HIV transmission from an individual on HIV treatment with an undetectable viral load, and HIV-uninfected homosexual and bisexual men who have sex with men (MSM) who are adherent to PrEP are nearly 100% protected from acquiring HIV.1 In the mid-2010s, these biomedical interventions have translated into dramatic reductions in new HIV infections among MSM at the population level in places such as San Francisco, CA, USA, London, UK, and Melbourne and Sydney, Australia.3, 4, 5, 6

In contrast to the reductions in HIV incidence, trends in bacterial sexually transmitted infections (STIs) show a different temporal pattern. The notification rates for STIs fell with the arrival of HIV in the 1980s, and then in about 2000 began to gradually rise, with an acceleration in frequency around 2010 (figure 1; appendix pp 2–5).7, 8, 9 The reasons for these rises are complex. The changes in the perception of the severity of HIV and AIDS over the past 30–40 years might have contributed to behaviour changes (ie, increases in partner numbers and decreases in condom use) and might explain some of the STI rises among MSM.7 For example, an Australian study showed a large increase in condomless anal sex with casual partners between 1998 and 2006.10 However, many other factors might also be important, including changes in mixing patterns within risk groups, use of smartphone dating applications, group sex, recreational drug use, and access to health care.7

The rises in STIs are of concern for many reasons. STIs are associated with a large financial burden worldwide. For example, in the USA, STIs cost the health-care system approximately US$16 billion a year, and cause individuals severe symptoms and complications.11 The rapid rise in syphilis infection has led to the re-emergence of congenital syphilis in some areas.12 Gonorrhoea is at risk of becoming resistant to the last first-line antibiotic treatment (dual treatment with ceftriaxone and azithromycin), prompting its elevation to an urgent resistance threat by the US Centers for Disease Control and Prevention and a global threat by WHO.13, 14 Both organisations have indicated that decreasing gonorrhoea prevalence is a key strategy to minimise rises in resistance.

In this this Review, we describe the changes in incident STIs among MSM that have occurred in the past 20 years, and in factors that might be contributing to these changes, before providing some steps that could be taken to reduce STIs in the present context of improved control of HIV.

Section snippets

Changes in STI epidemics

WHO has estimated that in 2012, 357 million new infections of four curable STIs (chlamydia, gonorrhoea, syphilis, and trichomoniasis) occurred worldwide.15 In this Review, we focus on STIs among MSM, as this population is at greatest risk of acquiring HIV and comprise the majority of people prescribed PrEP in developed countries. No global estimates have been made for the annual number of STIs among MSM because the data are difficult to obtain from surveillance systems. In this Review, we

Behavioural and structural changes contributing to the rise of STIs in MSM

The rises in STIs have been associated with gradual changes in sexual behaviours since 2000, and further changes that have occurred resulting from the introduction of PrEP since the mid-2010s. A 2018 meta-analysis concluded that MSM using PrEP were 24% more likely to acquire a bacterial STI than MSM not using PrEP, partially because of the increase in condomless anal sex.37 Within communities, the introduction of PrEP has been temporally associated with substantial increases in condomless sex

Possible interventions to prevent and control STIs

Interventions to reduce STIs at the population level require the capacity to reduce one or more of the following: the transmissibility of the STI, the rate of partner change, or the duration of infectiousness for an STI (table).

Successful control measures for STIs in this era of biomedical interventions for HIV will require the optimisation of each separate intervention for STI control. Without optimising each one of these interventions, the incidence of STIs will probably continue to rise in

Conclusions

STIs dramatically reduced during the AIDS epidemic in the 1980s, but diagnosed cases of STIs have increased since the late 1990s as HIV became more treatable and risk behaviours increased. STI risk behaviours, and STI incidence, have continued to increase since then. The reasons for the rises in STIs over the past 20 years are complex and involve changes in many different aspects of sexual behaviour and clinical testing, and widespread use of recently developed biomedical interventions for HIV

Search strategy and selection criteria

In August, 2018, we searched terms in PubMed and Google Scholar to identify key reports and references related to the topic of this Review. We included all publications and published reports up to July 31, 2018. The search terms were “sexually transmitted infections”, “sexually transmitted diseases”, “men who have sex with men”, “prevalence”, “sexual practices”, “surveillance”, and “sexual behaviours”. We restricted our search to English language articles only. We also identified surveillance

References (103)

  • G Prestage et al.

    How has the sexual behaviour of gay men changed since the onset of AIDS: 1986–2003

    Aust N Z J Public Health

    (2005)
  • LA Eaton et al.

    Serosorting sexual partners and risk for HIV among men who have sex with men

    Am J Prev Med

    (2007)
  • CK Fairley et al.

    Doxycycline post-exposure prophylaxis: let the debate begin

    Lancet Infect Dis

    (2018)
  • EPF Chow et al.

    Human papillomavirus in young women with Chlamydia trachomatis infection 7 years after the Australian human papillomavirus vaccination programme: a cross-sectional study

    Lancet Infect Dis

    (2015)
  • L Zhang et al.

    Targeted human papillomavirus vaccination for young men who have sex with men in Australia yields significant population benefits and is cost-effective

    Vaccine

    (2017)
  • SL Gottlieb et al.

    The global roadmap for advancing development of vaccines against sexually transmitted infections: update and next steps

    Vaccine

    (2016)
  • H Petousis-Harris et al.

    Effectiveness of a group B outer membrane vesicle meningococcal vaccine against gonorrhoea in New Zealand: a retrospective case-control study

    Lancet

    (2017)
  • J-M Molina et al.

    Post-exposure prophylaxis with doxycycline to prevent sexually transmitted infections in men who have sex with men: an open-label randomised substudy of the ANRS IPERGAY trial

    Lancet Infect Dis

    (2018)
  • RM Grant et al.

    Preexposure chemoprophylaxis for HIV prevention in men who have sex with men

    N Engl J Med

    (2010)
  • AE Brown et al.

    Fall in new HIV diagnoses among men who have sex with men (MSM) at selected London sexual health clinics since early 2015: testing or treatment or pre-exposure prophylaxis (PrEP)?

    Euro Surveill

    (2017)
  • E Jasek et al.

    Sexually transmitted infections in Melbourne, Australia from 1918 to 2016: nearly a century of data

    Commun Dis Intell Q Rep

    (2017)
  • H Mohammed et al.

    100 years of STIs in the UK: a review of national surveillance data

    Sex Transm Infect

    (2018)
  • IB Zablotska et al.

    Differing trends in sexual risk behaviours in three Australian states: New South Wales, Victoria and Queensland, 1998–2006

    Sex Health

    (2008)
  • Incidence, prevalence and cost of sexually transmitted infections in the United States, 2013

  • Syphilis in women and babies: 2017 snapshot for California

  • Antibiotic resistance threats in the United States, 2013

  • Global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics

    (2017)
  • L Newman et al.

    Global estimates of the prevalence and incidence of four curable sexually transmitted infections in 2012 based on systematic review and global reporting

    PLoS One

    (2015)
  • VJ Cornelisse et al.

    Increased detection of pharyngeal and rectal gonorrhea in men who have sex with men after transition from culture to nucleic acid amplification testing

    Sex Transm Dis

    (2017)
  • JL Marcus et al.

    Infections missed by urethral-only screening for chlamydia or gonorrhea detection among men who have sex with men

    Sex Transm Dis

    (2011)
  • Sexually transmitted infections and screening for chlamydia in England, 2017

    (2018)
  • Chlamydia infection—annual epidemiological report for 2016

    (2016)
  • HIV, viral hepatitis and sexually transmissible infections in Australia: annual surveillance report 2017

    (2017)
  • SL Goddard et al.

    Increasing yield of pharyngeal Chlamydia trachomatis among male gay and bisexual clinic attendees in Sydney: an observational study

    Sex Health

    (2017)
  • LA Barbee et al.

    Effect of nucleic acid amplification testing on detection of extragenital gonorrhea and chlamydial infections in men who have sex with men sexually transmitted disease clinic patients

    Sex Transm Dis

    (2014)
  • RC Passaro et al.

    Body parts matter: social, behavioral, and biological considerations for urethral, pharyngeal, and rectal gonorrhea and chlamydia screening among MSM in Lima, Peru

    Sex Transm Dis

    (2018)
  • M DeSilva et al.

    A case-control study evaluating the role of internet meet-up sites and mobile telephone applications in influencing a syphilis outbreak: Multnomah County, Oregon, USA, 2014

    Sex Transm Infect

    (2016)
  • O Peuchant et al.

    Changing pattern of Chlamydia trachomatis strains in Lymphogranuloma venereum outbreak, France, 2010–2015

    Emerg Infect Dis

    (2016)
  • Lymphogranuloma venereum—Annual Epidemiological Report for 2016

    (2018)
  • CA Boutin et al.

    Lymphogranuloma venereum in Quebec: re-emergence among men who have sex with men

    Canada Commun Dis Rep

    (2018)
  • C Charre et al.

    Hepatitis A outbreak in HIV-infected MSM and in PrEP-using MSM despite a high level of immunity, Lyon, France, January to June 2017

    Euro Surveill

    (2017)
  • F Jin et al.

    Sexual transmission of hepatitis C virus among gay and bisexual men: a systematic review

    Sex Health

    (2017)
  • NA Medland et al.

    Predictors and incidence of sexually transmitted Hepatitis C virus infection in HIV positive men who have sex with men

    BMC Infect Dis

    (2017)
  • E Hoornenborg et al.

    MSM starting preexposure prophylaxis are at risk of hepatitis C virus infection

    AIDS

    (2017)
  • K Mohan et al.

    What is the overlap between HIV and shigellosis epidemics in England: further evidence of MSM transmission?

    Sex Transm Infect

    (2018)
  • RV Tauxe et al.

    The persistence of Shigella flexneri in the United States: increasing role of adult males

    Am J Public Health

    (1988)
  • I Simms et al.

    Intensified shigellosis epidemic associated with sexual transmission in men who have sex with men—Shigella flexneri and S. sonnei in England, 2004 to end of February 2015

    Euro Surveill

    (2015)
  • MW Traeger et al.

    Effects of pre-exposure prophylaxis for the prevention of human immunodeficiency virus infection on sexual risk behavior in men who have sex with men: a systematic review and meta-analysis

    Clin Infect Dis

    (2018)
  • KL Hess et al.

    Trends in sexual behavior among men who have sex with men (MSM) in high-income countries, 1990–2013: a systematic review

    AIDS Behav

    (2017)
  • G Paz-Bailey et al.

    Trends in condom use among MSM in the United States: the role of antiretroviral therapy and seroadaptive strategies

    AIDS

    (2016)
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