Abstract
HIV diagnoses among men who have sex with men (MSM) have been increasing in several high-income countries. A better understanding of the sexual behavior trends among MSM can be useful for informing HIV prevention. We conducted a systematic review of studies that examined behavioral trends (1990–2013) in any condomless anal sex, condomless anal sex with an HIV-discordant partner, and number of partners. Studies included come from the United States, Europe, and Australia. We found increasing trends in condomless anal sex and condomless anal sex with an HIV-discordant partner, and a decreasing trend in number of partners. The increase in condomless anal sex may help to explain the increase in HIV infections. More explanatory research is needed to provide insight into factors that contribute to these behavior trends. Continuous monitoring of HIV, risk behaviors, and use of prevention and treatment is needed to evaluate prevention efforts and monitor HIV transmission risk.
Keywords: HIV, risk behaviors, men who have sex with men, condom use
Introduction
Gay, bisexual, and other men who have sex with men (collectively referred to as MSM) remain a core population affected by HIV in many parts of the world (1). In several high-income countries, including France, the Netherlands, the United Kingdom, and the United States, overall trends in HIV diagnoses are in decline except among MSM, where they have been increasing since early 2000 (2, 3). Although HIV diagnoses do not necessarily reflect recent HIV infection, the increase in HIV diagnoses in several high-income countries occurred during the same time period as a rise in primary and secondary syphilis among MSM, and the increase was apparently not correlated with changes in HIV testing (2), suggesting a true increase in HIV infections among MSM.
Several factors contribute to the high transmission rates among MSM, including high background prevalence of HIV, type and frequency of sex acts, number of sex partners, HIV status of partners, treatment and viral load status (if partners are HIV-positive), and whether pre-exposure prophylaxis (PrEP) is being used. HIV transmission among MSM is higher than among other populations in part because of the higher transmission probabilities during anal sex. The estimated per-act probability of acquiring HIV is 138 per 10,000 exposures for condomless receptive anal sex compared to 8 per 10,000 exposures for condomless receptive vaginal sex (4). Evidence also shows that the number of sex partners affects the risk of HIV transmission (5, 6). The more partners a person has, the more likely to have a partner with HIV whose viral load is not suppressed or to have a sex partner with a sexually transmitted infection (STI) - both factors can increase the risk of HIV transmission. However, antiretroviral therapy (ART) lowers the viral load of HIV-positive partners who adhere to the medication which, in turn, reduces HIV transmission to HIV-negative partners (7). In studies from both Europe (8) and Australia (9) there have been no HIV transmissions among MSM couples where the HIV-positive partner was on ART. Taking antiretroviral drugs as PrEP has also shown protective effects of HIV infection among HIV-negative MSM (10); while showing no evidence of risk compensation (11–13). Daily PrEP is recommended as one effective option for MSM at substantial risk of HIV acquisition (14).
While the scale-up of early detection and treatment may make the end of the HIV epidemic possible (15), there is evidence that reductions in condom use may jeopardize the population-level benefits of ART (16–18). Mathematical modeling suggests that the increases in HIV incidence in the United Kingdom, over a period in which ART coverage and viral suppression were also increasing, was likely due to the counter-effect of concomitant increases in condomless sex among MSM who were not virally suppressed (16). Increases in STIs, which facilitate HIV transmission, could also play a role in the increasing HIV incidence. However, increases in STIs are also likely to be the result of increases in condomless sex. Modeling work from the Netherlands reached similar conclusions and suggested that the reductions in HIV incidence due to ART and earlier HIV diagnosis had been offset by increases in risk behaviors among MSM in the Netherlands (17). These findings show that modest increases in condomless sex are enough to overcome the beneficial effects of ART at a population level (16, 17).
A better understanding of the sexual behavior trends among MSM would be useful for informing changes in the risk of HIV acquisition or transmission, for identifying sub-groups that would benefit the most from HIV prevention interventions, and resource allocation within the United States and other high-income countries. In this report, we evaluate changes in sexual risk behaviors among MSM in high-income countries. We conducted a systematic review of studies that examined sexual behaviors among MSM over time (1990–2013) to determine the trends for three behaviors that are predictors of HIV transmission: condomless anal sex (with any, casual or main partners), condomless anal sex with a partner of unknown or discordant HIV status, and number of sex partners.
Methods
Systematic Search
A systematic literature search was conducted to locate citations that assessed changes over time in sexual risk behaviors and prevalence of STIs among MSM. A Centers for Disease Control and Prevention (CDC) librarian conducted a search of multiple electronic databases (Medline, Embase, Global Health, PsychInfo, CAB Abstracts, CINHAL, Sociological Abstracts, Web of Science, Cochrane Library, and LILACS). Indexing and keyword terms were cross-referenced using Boolean logic in three areas: [1] sexual risk behavior/STI descriptors (sexual behavior, safe sex, protected sex, unsafe sex, unprotected sex, anal intercourse, condom use, high-risk sex, barebacking, sex partner, sex risk, sexually transmitted disease, STD, sexually transmitted infection, STI, syphilis, gonorrhea, Chlamydia, Lymphogranuloma venereum, LGV), [2] MSM descriptors (homosexuality, men who have sex with men, MSM, men having sex with men, gay men, bisexual men, homosexual), and [3] descriptors related to change over time (trend, pattern, change, increase, decrease, unchanged, over time, epidemiology, survey, surveillance). No language restriction was applied to the automated search. The systematic searches were conducted in May 2014 and updated in May 2015. The full searches are available from the corresponding author.
Inclusion/Exclusion Criteria
This paper focuses on sexual risk behaviors among MSM (a separate paper focuses on syphilis trends (19)). Studies were included in this systematic review if they [1] were conducted in a high-income country (based on the World Bank definition (20)), [2] were published between January 2004 and May 2015, [3] reported data on MSM for at least two time points, and [4] reported on relevant sexual behaviors. Relevant sexual risk behaviors included: condomless anal sex (with any, casual or main partners), condomless anal sex with a partner of unknown/discordant HIV status, and number of sex partners. It usually took many years for the studies that examined behavioral trends to collect and analyze data before the findings were published. We chose a publication cut-off of 2004 because it covered ten years from the original search date and allowed the focus to be on more recent behavior trends. Several studies that we reviewed reported data points back to 1990. These data points were included in this systematic review if the studies met the inclusion criteria. Studies were excluded at the abstract level if they were (a) modeling, review or intervention papers, (b) published in languages other than English (most were conducted in low or middle income countries or the abstracts did not provide sufficient information), or (c) conference abstracts, posters, or dissertations. Studies were excluded at the full-report level if they (d) covered only specific sub-populations (e.g., sex workers), and (e) had duplicated data sources (see data abstraction and analysis for more information).
Data abstraction and analysis
A trained coder screened the titles and abstracts of 7,113 citations for eligibility (Figure 1). After review of the abstracts, 6,830 were determined to not meet the inclusion criteria, and the remaining 283 were retained for retrieval of the full-length article. Upon reviewing the full-length article, 51 were determined to meet the inclusion criteria and were coded for the following: study date, location, sampling method, sample size, HIV status of participants, sexual behavior outcomes, assessment time frame, and study results. The full-report data abstraction was reviewed by an additional person to verify accuracy. Discrepancies were reconciled between the coders. To avoid potential bias in the trend analyses, we excluded an additional 14 papers for the following reasons at the full-report level: specific sub-populations (i.e., sex workers; n=2) and duplicated data source (n=12).
We applied the following rules for guiding data abstraction for analyses. For studies that reported multiple sexual behavior outcomes, separate analyses were conducted for condomless anal sex, condomless anal sex with casual partners, condomless anal sex with main partners, condomless anal sex with a partner of unknown/discordant HIV status, and number of partners. This approach allowed us to examine the trends with all available data in the literature. For the studies that reported condomless anal sex, we selected the data for all study participants regardless of their HIV status, unless the study only reported data on HIV-positive or HIV-negative participants without reporting data on all study participants, then we treated HIV-positive and HIV-negative participants as separate samples in the analyses. For studies that reported on condomless sex with a partner of unknown/discordant HIV status, the results stratified by HIV status were used as separate samples in the analyses. If stratified results were not reported, the overall results were used. The analysis for number of partners was stratified into two groups of studies – studies that measured multiple partners with a high cut point (10+ to 21+ partners) and those with a lower cut point (2+ to 6+ partners).
For each study sample, we abstracted the percentage of persons who engaged in a specific sexual behavior at each assessment time (i.e., year of data collection). Multi-level models were used to examine the overall trends, with the study treated as the random-effect and year as the fixed effect. The beta, which represents the slope of the line on the log scale, was reported. A positive beta represents an upward trend, a negative number represents a downward trend. The larger the beta, the steeper the slope. Additionally, we conducted “knot” analyses to determine whether the direction of the trend changed at a particular year. While all the included studies were published between 2004 and 2015, the data collected were between 1990 and 2013. A knot was set at year 2002 because it is about the mid-point of the data collected across studies and ART had improved and become more widely available around this time. For the knot analyses, the slope of the line was allowed to change at 2002 generating two estimates for the slope: one for 1992 to 2002 and one for 2003 to the latest data collection date (usually 2012 or 2013). The results from multi-level models without and with a knot were both reported. If a change in significance or direction of the slope occurred with the addition of the knot, the summary line presented in the figure was based on the knot analysis result. If no significant change in slope occurred based on the knot analyses, the summary line presented in the figure was based on the overall result. Sensitivity analyses were also conducted by stratifying the studies by HIV status and study design.
Results
Figure 1 summarizes the study selection process. Among the 37 included studies that provided behavioral trend data between 1990 to 2013, 13 were conducted in the United States (21–33), nine in continental Europe (34–42), seven in Australia (43–49), five in the United Kingdom (50–54), two in New Zealand (55, 56), and one in Canada (57). Twenty-nine studies examined condomless anal sex (Table I), 16 examined condomless anal sex with a discordant or unknown HIV-status partner (Table II), and 16 examined number of partners (Table III). The majority were repeated cross-sectional studies (n=26) while six were longitudinal cohorts (27, 34, 35, 42, 44, 57) and five were retrospective medical record analyses from STD clinics or emergency rooms (23, 36, 38, 47, 49). Most sampled MSM specifically, but two analyses were based on general population surveys (21, 50). Recall periods differed across studies and variables, but most common were past year, past six months, past three months, and last sex. There was not substantial change in age composition across study samples over time.
Table I.
Author (year) | Location | Years of Data Collection |
Sampling Method | Sample | Outcome time frame |
Results reported by authors |
---|---|---|---|---|---|---|
Leichliter et al. (2013) | USA | 2002, 2006–2010 | National Survey of Family Growth - multistage national probability sample of 15–44 year olds living in US households | 2002: N=197; age distribution: 15–24 N=57, 25–34 N=64, 35–44 N=76 2006–2010: N=272; age distribution: 15–24 N=77, 25–34 N=97, 35–44 N=98 (HIV prevalence not reported) | At last sex | Any type of partner: No change |
CDC (2013) | USA | 2005, 2008, 2011 | Venue-based sampling of MSM in 20 cities | 2005: N=11,457 (13% HIV+); age distribution: 18–24 N=2,235, 25–29 N=1,911, 30–39 N=3,879, ≥40 N=3,432 2008: N=9,253 (12% HIV+); age distribution: 18–24 N=2,071, 25–29 N=1,711, 30–39 N=2,562, ≥40 N=2,909 2011: N=9,253 (13% HIV+); age distribution: 18–24 N=2,352, 25–29 N=1,750, 30–39 N=2,190, ≥40 N=2,961 | 1 year | Any type of partner: Increase |
Golden et al. (2008) | Seattle, Washington | 2002–2007 | All MSM attending STD clinics | 2002: HIV− N=1,282; HIV+ N=166 2003: HIV− N=1,214; HIV+ N=160 2004: HIV− N=1,236; HIV+ N=261 2005: HIV− N=1,373; HIV+ N=182 2006: HIV− N=2,134; HIV+ N=260 2007: HIV− N=1,718; HIV+ N=232 Age distribution overall (not presented by year): <24 N=2,170, 25–29 N=2,303, 30–34 N=2,071, 35–39 N=2,117, ≥40 N=3,788 | 1 year | Any type of partner: HIV+: No change HIV−: No change |
Kalichman et al. (2007) | Atlanta, Georgia | 1997, 2005, 2006 | Venue intercept procedures at Gay Pride events | 1997: N=511 (14% HIV+); age distribution: mean 33.6, SD 8.4 2005: N=473 (14% HIV+); age distribution: mean 34.3, SD 10.4 2006: N=449 (17% HIV+); age distribution: mean 34.8, SD 10.1 | 6 months | Any type of partner: Increase |
Osmond et al. (2007) | San Francisco, California | 1997, 2002 | Random-digit-dial telephone survey of MSM households | 1997: N=915 (20% HIV+); age distribution: 18–29 15.9%, 30–39 38.0%, 40–49 28.4%, ≥50 17.7% 2002: N=879 (27% HIV+); age distribution: 18–29 8.5%, 30–39 31.8%, 40–49 30.6%, ≥50 29.1% | 1 year | Any type of partner: Increase |
Scheer et al. (2008) | San Francisco, California | 1998–2007 | Street-based intercept interview at gay-oriented events, outside gay clubs/bars, and in gay neighborhoods | N > 1,200 per year (HIV prevalence and age distribution not reported) | Not reported | Any type of partner: Increase |
McFarland et al. (2012) | San Francisco, California | 2008–2009 | Venue-based sampling of MSM | N=732 (21% HIV+); Age distribution (baseline): 18–24 14%, 25–34 34%, 35–44 27%, 45–54 15%, ≥55 10% (1-year cohort) | 6 months | Any type of partner: HIV+: No change HIV−: No change |
Pantalone et al. (2015) | New York City | 2003–2008 | Intercept sampling at 2 large lesbian, gay, bisexual community events | 2003: N=610; age distribution: 18–40 N=416, >40 N=194 2004: N=418; age distribution: 18–40 N=282, >40 N=136 2005: N=421; age distribution: 18–40 N=268, >40 N=153 2006: N=384; age distribution: 18–40 N=261, >40 N=123 2007: N=254; age distribution: 18–40 N=170, >40 N=84 2008: N=423; age distribution: 18–40 N=267, >40 N=156 (100% HIV−) | 3 months | Casual partner: HIV−: decrease |
George et al. (2006) | Montreal, Canada | 1997–2003 | Convenience sampling: Recruitment by posters, internet, gay print media, & information cards at gay pride week | N=1,587 (100% HIV−); age distribution: <30 N=753, ≥30 N=843 (cohort) | 6 months | Any type of partner: HIV−: Increase |
Mercer et al. (2004) | Britain | 1990, 2000 | Stratified probability samples of the general population | 1990: N=100; age distribution not reported 2000: N=175; age distribution: mean 31.5 (HIV prevalence not reported) | 4 weeks | Any type of partner: No change |
Hickson et al. (2013) | England | 2001, 2008 | Convenience sampling: Recruitment via internet banner ads on gay dating sites, news sites, and community health promotion organization sites | 2001: N=3,517 (3% HIV+); age distribution: <20 N=409, 20–29 N=1,407, 30–39 N=1,036, 40–49 N=480, ≥50 N=185 2008: N=1,382 (9% HIV+); age distribution: <20 N=56, 20–29 N=396, 30–39 N=387, 40–49 N=348, ≥50 N=195 | 1 year | Any type of partner: No change |
Lattimore et al. (2011) | London, England | 1998–2005, 2008 | Venue-based recruitment of gay men at gyms | 1998: N=834 (14% HIV+); age distribution: median 34 range 17–74 1999: N=630 (16% HIV+); age distribution: median 34 range 20–67 2000: N=739 (16% HIV+); age distribution: median 35 range 20–77 2001: N=735 (16% HIV+); age distribution: median 35 range 17–72 2002: N=828 (15% HIV+); age distribution: median 35 range 17–74 2003: N=498 (16% HIV+); age distribution: median 36 range 18–65 2004: N=670 (18% HIV+); age distribution: median 37 range 20–69 2005: N=482 (16% HIV+); age distribution: median 36 range 21–67 2008: N=648 (23% HIV+); age distribution: median 39 range 20–87 | 3 months | Any type of partner: 1998–2001 increase, 2001–2005 & 2005–2008 no change |
Williamson et al. (2006) | London, England | 1996, 1999, 2002 | Venue-based recruitment at commercial gay venues | 1996: N=1,895 (HIV prevalence not reported); age distribution: median 30 1999: N=1,368 (13% HIV+); age distribution: median 32 2002: N=1,325 (11% HIV+); age distribution: median 33 | 1 year | Any type of partner: Increase |
Hart et al. (2005) | Glasgow and Edinburgh, Scotland | 1996, 1999, 2002 | Venue-based recruitment at gay bars | 1996: N=2,276; age distribution: 15–25 N=620, >25 N=1,630 1999: N=2,498; age distribution: 15–25 N=614, >25 N=1,788 2002: N=1,734; age distribution: 15–25 N=528, >25 N=1,114 (HIV prevalence not reported) | 1 year | Any type of partner: Increase |
Jansen et al. (2011) | Amsterdam, Netherlands | 1995–2009 | Amsterdam Cohort Studies - Convenience sampling from STI clinics and MSM meeting places and chain referral | N=1,642 (100% HIV−); age distribution (baseline): median 28.8 IQR 24.8–35.9 (cohort) | 6 months | Any type of partner: HIV−: increase |
Stolte et al. (2004) | Amsterdam, Netherlands | 2000–2003 | HIV+ men from the Amsterdam Cohort Studies - Convenience sampling from STI clinics and MSM meeting places and chain referral | N=57 (100% HIV+); age distribution (baseline): median 43 IQR 37.8–53.6 (cohort) | 6 months | Casual partner: HIV+: Increase |
Op de Coul et al. (2013) | Netherlands | 2009–2011 | All STD clinic attendees | 2009: N=16,304 2010: N=19,535 2011: N=21,719 (overall 15% HIV+); Age distribution overall (not presented by year): 15–24 N=11,837, 25–34 N=22,448, 35–44 N=23,979, 45–55 N=16,385, >55 N=7,689 | 6 months | Casual partner: increase |
Cowan et al. (2012) | Denmark | 2000, 2001, 2002, 2006, 2009 | Convenience sampling: Recruitment through gay and HIV-related websites and venues attended by MSM | 2000: N=1,745 (11% HIV+) 2001: N=1,574 (9% HIV+) 2002: N=1,538 (11% HIV+) 2006: N=3,141 (8% HIV+) 2009: N=1,310 (9% HIV+); Age distribution not reported | 1 year | Any type of partner: Increase |
Casalino et al. (2014) | Paris, France | 2006–2012 | All MSM who visited an emergency department after a sexual exposure to HIV | 2006: N=71 2007: N=101 2008: N=95 2009: N=78 2010: N=142 2011: N=147 2012: N=154 (100% HIV−); age distribution not reported | At last sex | Any type of partner: HIV−: Increase |
Moreau-Gruet et al. (2006) | Switzerland | 1992, 1994, 1997, 2000 | Convenience sampling: Surveys were inserted into gay magazines and distributed in homosexual associations, bars, and saunas | 1992: N=934 (11% HIV+); age distribution: <20 <1%, 20–29 31%, 30–39 32%, 40–49 24%, ≥50 13% 1994: N=1,195 (10% HIV+); age distribution: <20 1%, 20–29 33%, 30–39 38%, 40–49 17%, ≥50 11% 1997: N=1,097 (11% HIV+); age distribution: <20 1%, 20–29 24%, 30–39 42%, 40–49 18%, ≥50 14% 2000: N=918 (11% HIV+); age distribution: <20 1%, 20–29 16%, 30–39 43%, 40–49 21%, ≥50 18% | 1 year | Casual partner: Increase Main partner: No change |
Bozicevic et al. (2012) | Zagreb, Croatia | 2006, 2011 | Recruitment by respondent driven sampling of MSM | 2006: n=350 (4.5%HIV+); age distribution: median 27 2011: n=387 (2.8% HIV+); age distribution: median 28 | At last sex | Casual partner: No change Main partner: No change |
Klavs et al. (2009) | Ljubljana, Slovenia | 2001–2008 | Venue-based convenience sample of MSM | Range N=68–124 (average N=89) per year (HIV prevalence and age distribution not reported) | 1 year | Any type of partner: No change |
Saxton et al. (2014) | Auckland, New Zealand | 2002, 2004, 2006, 2008, 2011 | Convenience sampling in community locations (fair day, gay bars, sex-on-site venues) | 2002: n=812 (5% HIV+); age distribution: <30 31.1%, 30–44 48.5%, ≥45 20.4% 2004: n=1,220 (4.8% HIV+); age distribution: <30 33.4%, 30–44 42.2%, ≥45 24.4% 2006: n=1,228 (3.5% HIV+); age distribution: <30 33.4%, 30–44 44.0%, ≥45 22.7% 2008: n=1,527 (4.3% HIV+); age distribution: <30 31.8%, 30–44 38.9%, ≥45 29.3% 2011: n=1,304 (5.9% HIV+); age distribution: <30 35.8%, 30–44 35.5%, ≥45 28.7% | 6 months | Casual partner: increase 2002–2011, 2006–2011 no change 2002–2006 Main partner: no change 2002–2011, 2002–2006, 2006–2011 |
Saxton et al. (2015) | Auckland, New Zealand | 2006, 2008, 2011 | Convenience sample: Web-based | 2006: N=647 (1.4% HIV+); age distribution: mean 34.1 2008: N=443 (2.1% HIV+); age distribution: mean 33.3 2011: N=523 (3.3% HIV+); age distribution: mean 35.1 | 6 months | Casual partner: no change Main partner: no change |
Zablotska et al. (2011) | Australia | 1998–2009 | Gay Community Periodic Surveys (GCPS) - Venue-based recruitment | Average annual sample size (range) New South Wales: N=2,642 (2,222–3,732); age distribution: mean 35.6 SD 9.5 Victoria: N=1,907 (1,578–2,064); age distribution: mean 34.8 SD 10.1 Queensland: N=1,428 (1,225–1,787); age distribution: mean 33.0 SD 11.0 South Australia: N=595 (463–864); age distribution not reported Western Australia: N=894 (750–1,035); age distribution not reported Australian Capital Territory: N=296 (255–350); age distribution not reported (HIV prevalence not reported) | 6 months | New South Wales: Casual partners: Decrease Main partners: Increase Victoria: Casual partners: Increase Main partners: Increase Queensland: Casual partners: Increase Main partners: Increase South Australia: Casual partners: Increase Main partners: Increase Western Australia: Casual partners: Increase Main partners: Increase Australian Capital Territory: Casual partners: Increase Main partners: Increase |
Prestage et al. (2005) | Sydney, Australia | 1993–1995, 2001–2003 | Convenience sampling at gay community events, venues, and other sources: 1993–1995 Sydney Men and Sexual Health; 2001–2002 Positive Health (HIV+); 2001–2003 Health in Men (HIV−) | 1993–1995 HIV+: N=191; age distribution: <25 9.7%, ≥50 4.6% 2001–2002 HIV+: N=154; age distribution: <25 0.0%, ≥50 19.4% 1993–1995 HV−: N=737; age distribution: <25 29.3%, ≥50 6.4% 2001–2003 HIV−: N=920; age distribution: <25 10.5%, ≥50 9.6% | 6 months | Casual partner: HIV+: increase HIV−: increase |
Van de Ven et al. (2004) | Sydney, Australia | 1999, 2002 | Venue community-based recruitment at gay bars, sex on-premises venues, and social events/meetings | 1999: N=319 (3.2% HIV+); age distribution: median 29 range 19–65 2002: N=457 (3.6% HIV+); age distribution: median 30 range 19–65 | 6 months | Casual partner: No change Main partner: No change |
Zablotska et al. (2009) | Sydney, Australia | 2003–2006 | Convenience sampling at gay community events, venues, and other sources: 2 cohorts – Positive Health (pH) and Health in Men (HIM) | pH: N=760 (HIV+); age distribution (in 2006): median 46 range 26–72 HIM: N=1,427 (HIV−); age distribution (in 2006): median 36 range 18–73 (cohorts) | 6 months | Casual partner: HIV+: Increase HIV−: Decrease |
Chow et al. (2015) | Melbourne, Australia | 2008–2013 | All MSM attending a sexual health clinic | 2008: casual N=724; main N=396 2009: casual N=1,780; main N=887 2010: casual N=1,320; main N=668 2011: casual N=2,470; main N=1,227 2012: casual N=3,030; main N=1,493 2013: casual N=3,637; main N=1,698 (HIV prevalence not reported); Age distribution overall (not presented by year): median 30 range 14–85 | 1 year | Casual partner: increase Main partner: no change |
Table II.
Author (year) | Location | Years of Data Collection |
Sampling Method | Sample | Outcome time frame |
Results reported by authors |
---|---|---|---|---|---|---|
CDC (2013) | USA | 2008, 2011 | Venue-based sampling of MSM in 20 cities | 2008: N=9,253 (12% HIV+); age distribution: 18–24 N=2,071, 25–29 N=1,711, 30–39 N=2,562, ≥40 N=2,909 2011: N=9,253 (13% HIV+); age distribution: 18–24 N=2,352, 25–29 N=1,750, 30–39 N=2,190, ≥40 N=2,961 | At last sex | Overall: No change HIV+: No change HIV−: No change |
Golden et al. (2008) | Seattle, Washington | 2002–2007 | All MSM attending STD clinics | 2002: HIV− N=1,282; HIV+ N=166 2003: HIV− N=1,214; HIV+ N=160 2004: HIV− N=1,236; HIV+ N=261 2005: HIV− N=1,373; HIV+ N=182 2006: HIV− N=2,134; HIV+ N=260 2007: HIV− N=1,718; HIV+ N=232 Age distribution overall (not presented by year): <24 N=2,170, 25–29 N=2,303, 30–34 N=2,071, 35–39 N=2,117, ≥40 N=3,788 | 1 year | HIV+: Decrease HIV−: No change |
Menza et al. (2011) | Seattle, Washington | 2003, 2006 | Random-digit dial household telephone survey | 2003: N=400 (13% HIV+); age distribution: median 38 range 19–90 2006: N=400 (13% HIV+); age distribution: median 44 range 20–83 | 1 year | Overall: No change HIV+: No change HIV−: No change |
McFarland et al. (2012) | San Francisco, California | 2008–2009 | venue-based sampling of MSM (1-year cohort) | N=732 (21% HIV+) Age distribution (baseline): 18–24 14%, 25–34 34%, 35–44 27%, 45–54 15%, ≥55 10% (1-year cohort) | 6 months | HIV+: No change HIV−: No change |
Scheer et al. (2008) | San Francisco, California | 2005–2007 | Street-based intercept interview at gay-oriented events, outside gay clubs/bars, and in gay neighborhoods | N > 1200 per year (HIV prevalence and age distribution not reported) | Not reported | HIV+: No change HIV−: Increase |
Osmond et al. (2007) | San Francisco, California, USA | 1997, 2002 | Random-digit-dial telephone survey of MSM households | 1997: N=915 (20% HIV+); age distribution: 18–29 15.9%, 30–39 38.0%, 40–49 28.4%, ≥50 17.7% 2002: N=879 (27% HIV+); age distribution: 18–29 8.5%, 30–39 31.8%, 40–49 30.6%, ≥50 29.1% | 1 year | Overall: Increase |
Pantalone et al. (2015) | New York City | 2003–2008 | Intercept sampling at 2 large lesbian, gay, bisexual community events | 2003: N=104; age distribution: 18–40 N=59, >40 N=45 2004: N=84; age distribution: 18–40 N=45, >40 N=39 2005: N=69; age distribution: 18–40 N=36, >40 N=33 2006: N=87; age distribution: 18–40 N=37, >40 N=50 2007: N=36; age distribution: 18–40 N=19, >40 N=17 2008: N=86; age distribution: 18–40 N=41, >40 N=45 (100% HIV+) | 3 months | Casual partner: HIV+: no change |
George et al. (2006) | Montreal, Canada | 1997–2003 | Convenience sampling: recruitment by posters, internet, gay print media, & information cards at gay pride week | N=1,587 (100% HIV−); age distribution (baseline): <30 N=753, ≥30 N=843 (cohort) | 6 months | HIV−: Increase |
Hickson et al. (2013) | England | 2001, 2008 | Convenience sampling: Recruitment via internet banner ads on gay dating sites, news sites, and community health promotion organization sites | 2001: N=3,517 (3% HIV+); age distribution: <20 N=409, 20–29 N=1,407, 30–39 N=1,036, 40–49 N=480, ≥50 N=185 2008: N=1,382 (9% HIV+); age distribution: <20 N=56, 20–29 N=396, 30–39 N=387, 40–49 N=348, ≥50 N=195 | 1 year | Known discordant: HIV+: No change HIV−: No change |
Lattimore et al. (2011) | London, England | 1998–2005, 2008 | Venue-based recruitment of gay men at gyms | 1998: N=834 (14% HIV+); age distribution: median 34 range 17–74 1999: N=630 (16% HIV+); age distribution: median 34 range 20–67 2000: N=739 (16% HIV+); age distribution: median 35 range 20–77 2001: N=735 (16% HIV+); age distribution: median 35 range 17–72 2002: N=828 (15% HIV+); age distribution: median 35 range 17–74 2003: N=498 (16% HIV+); age distribution: median 36 range 18–65 2004: N=670 (18% HIV+); age distribution: median 37 range 20–69 2005: N=482 (16% HIV+); age distribution: median 36 range 21–67 2008: N=648 (23% HIV+); age distribution: median 39 range 20–87 | 3 months | Overall: 1998–2001 increase, 2001–2005 decrease, 2005–2008 no change HIV+: 1998–2001 increase, 2001–2005 decrease, 2005–2008 no change HIV−: 1998–2001 increase, 2001–2005 & 2005–2008 No change |
Williamson et al. (2006) | London, England & Glasgow, Scotland | 1996, 1999, 2002 | Venue-based recruitment at commercial gay venues | London: 1996: N=1,895 (HIV prevalence not reported); age distribution: median 30 1999: N=1,368 (13% HIV+); age distribution: median 32 2002: N=1,325 (11% HIV+); age distribution: median 33 Glasgow: 1996: N=1,245 (HIV prevalence not reported); age distribution: median 30 1999: N=1,442 (HIV prevalence not reported); age distribution: median 31 2002: N=972 (7% HIV+); age distribution: median 30 | 1 year | London: Increase Glasgow: Increase |
Moreau-Gruet et al. (2006) | Switzerland | 1994, 1997, 2000 | Convenience sampling: surveys were inserted into gay magazines and distributed in homosexual associations, bars, and saunas. | 1994: N=1195 (10% HIV+); age distribution: <20 1%, 20–29 33%, 30–39 38%, 40–49 17%, ≥50 11% 1997: N=1097 (11% HIV+); age distribution: <20 1%, 20–29 24%, 30–39 42%, 40–49 18%, ≥50 14% 2000: N=918 (11% HIV+); age distribution: <20 1%, 20–29 16%, 30–39 43%, 40–49 21%, ≥50 18% | 1 year | Main partner: Overall Decrease |
Seng et al. (2011) | France | 2000–2009 | Patients with primary HIV-1 infection attending any of 85 hospitals | N=670 (100% HIV+); age distribution (baseline): median 34 IQR 29–40 (cohort) | 6 months | Casual partner: HIV+: Increase |
Cowan et al. (2012) | Denmark | 2000, 2001, 2002, 2006, 2009 | Convenience sampling: recruitment through gay and HIV-related websites and venues attended by MSM | 2000: N=1,745 (11% HIV+) 2001: N=1,574 (9% HIV+) 2002: N=1,538 (11% HIV+) 2006: N=3,141 (8% HIV+) 2009: N=1,310 (9% HIV+); Age distribution not reported | 1 year | Overall: Increase |
Stolte et al. (2004) | Amsterdam, Netherlands | 2000–2003 | HIV+ men included in the Amsterdam Cohort Studies - Convenience sampling from STI clinics and MSM meeting places and chain referral | N=57 (100% HIV+); age distribution (baseline): median 43 IQR 37.8–53.6 (cohort) | 6 months | Main partner: HIV+: No change |
Zablotska et al. (2009) | Sydney, Australia | 2003–2006 | Convenience sampling at gay community events, venues, and other sources: 2 cohorts – Positive Health (PH) and Health in Men (HIM) | PH: N=760 (HIV+); age distribution (in 2006): median 46 range 26–72 HIM: N=1,427 (HIV−); age distribution (in 2006): median 36 range 18–73 (cohorts) | 12 months | Known discordant casual partners: HIV+: No change HIV−: Increase |
Table III.
Author (year) | Location | Years of Data Collection |
Sampling Method | Sample | Outcome time frame – cut point |
Results reported by authors |
---|---|---|---|---|---|---|
Kellogg et al. (2013) | San Francisco, California | 2004, 2008 | Street intercept sampling of MSM | 2004: N=1,079 (13% HIV+); age distribution: median 34 IQR 28–42 2008: N=545 (17% HIV+); age distribution: median 36 IQR 28–45 | 6 months – 6+ partners | Overall: No change |
Sudhinaraset et al. (2013) | San Francisco, California | 2005, 2008, 2011 | Venue-based time-location recruitment in gay venues/areas | 2005: N=332 (25% HIV+); age distribution: <30 N=99, ≥30 N=233 2008: N=444 (23% HIV+); age distribution: <30 N=126, ≥30 N=318 2011: N=431 (23% HIV+); age distribution: <30 N=123, ≥30 N=308 | 6 months – 6+ partners | Overall: No change |
Reilly et al. (2014) | New York City | 2005, 2008, 2011 | Venue-based time-location recruitment in gay venues/areas | 2005: N=457 (19% HIV+); age distribution: 18–30 N=247, >30 N=210 2008: N=550 (29% HIV+); age distribution: 18–30 N=244, >30 N=306 2011: N=510 (19% HIV+); age distribution: 18–30 N=278, >30 N=232 | 1 year – 4+ partners | Overall: Decrease |
Fendrich et al. (2010) | Chicago, Illinois | 1997, 2002 | Random-digit-dial telephone survey of MSM households (1997); household sampling from two zip codes with high MSM residential density (2002) | 1997 n=288 (100% HIV−); age distribution: 18–29 26%, 30–39 44%, 40–49 20%, ≥50 10% 2002 n=151 (100% HIV−); age distribution: 18–29 20%, 30–39 40%, 40–49 28%, ≥50 12% | 1997: 1 year; 2002: 6 months – 2+ partners | HIV−: No change |
Hickson et al. (2013) | England | 2001, 2008 | Convenience sampling: Recruitment via internet banner ads on gay dating sites, news sites, and community health promotion organization sites | 2001: N=3,517 (3% HIV+); age distribution: <20 N=409, 20–29 N=1,407, 30–39 N=1,036, 40–49 N=480, ≥50 N=185 2008: N=1,382 (9% HIV+); age distribution: <20 N=56, 20–29 N=396, 30–39 N=387, 40–49 N=348, ≥50 N=195 | 1 year – 5+ partners | Overall: No change HIV+: No change HIV−: Decrease |
Williamson et al. (2006) | London, England & Glasgow, Scotland | 1996, 1999, 2002 | Venue-based recruitment at commercial gay venues | London: 1996: N=1,895 (HIV prevalence not reported); age distribution: median 30 1999: N=1,368 (13% HIV+); age distribution: median 32 2002: N=1,325 (11% HIV+); age distribution: median 33 Glasgow: 1996: N=1,245 (HIV prevalence not reported) ; age distribution: median 30 1999: N=1,442 (HIV prevalence not reported); age distribution: median 31 2002: N=972 (7% HIV+); age distribution: median 30 | 1 year – 6+ partners | London: Increase Glasgow: No change |
Op de Coul et al. (2013) | Netherlands | 2007–2011 | All STD clinic attendees | 2007: N=11,026 2008: N=13,754 2009: N=16,304 2010: N=19,535 2011: N=21,719 (overall 15% HIV+) Age distribution overall (not presented by year): 15–24 N=11,837, 25–34 N=22,448, 35–44 N=23,979, 45–55 N=16,385, >55 N=7,689 | 6 months – 3+ partners | Overall: Increase |
Moreau-Gruet et al. (2006) | Switzerland | 1992, 1994, 1997, 2000 | Convenience sampling: Surveys were inserted into gay magazines. Surveys were also distributed in homosexual associations, bars, and saunas | 1992: N=934 (11% HIV+); age distribution: <20 <1%, 20–29 31%, 30–39 32%, 40–49 24%, ≥50 13% 1994: N=1,195 (10% HIV+); age distribution: <20 1%, 20–29 33%, 30–39 38%, 40–49 17%, ≥50 11% 1997: N=1,097 (11% HIV+); age distribution: <20 1%, 20–29 24%, 30–39 42%, 40–49 18%, ≥50 14% 2000: N=918 (11% HIV+); age distribution: <20 1%, 20–29 16%, 30–39 43%, 40–49 21%, ≥50 18% | 1 year – 11+ partners | Overall: No change |
Klavs et al. (2009) | Ljubljana, Slovenia | 2001–2008 | Venue-based convenience sample of MSM | Range N=68–124 (average N=89) per year (HIV prevalence and age distribution not reported) | 12 months – 11+ partners | Overall: Decrease |
Saxton et al. (2014) | Auckland, New Zealand | 2002, 2004, 2006, 2008, 2011 | Convenience sampling in community locations (fair day, gay bars, sex-on-site venues) | 2002: N=812 (5.0% HIV+); age distribution: <30 31.1%, 30–44 48.5%, ≥45 20.4% 2004: N=1,220 (4.8% HIV+); age distribution: <30 33.4%, 30–44 42.2%, ≥45 24.4% 2006: N=1,228 (3.5% HIV+); age distribution: <30 33.4%, 30–44 44.0%, ≥45 22.7% 2008: N=1,527 (4.3% HIV+); age distribution: <30 31.8%, 30–44 38.9%, ≥45 29.3% 2011: N=1,304 (5.9% HIV+); age distribution: <30 35.8%, 30–44 35.5%, ≥45 28.7% | 6 months – 21+ partners | Overall: Decrease |
Saxton et al. (2015) | Auckland, New Zealand | 2006, 2008, 2011 | Convenience sampling: Web-based | 2006: N=647 (1.4% HIV+); age distribution: mean 34.1 2008: N=443 (2.1% HIV+); age distribution: mean 33.3 2011: N=523 (3.3% HIV+); age distribution: mean 35.1 | 6 months – 21+ partners | Overall: Decrease |
Holt et al. (2013) | Australia | 2000/2001, 2008/2009 | Venue-based recruitment - Gay Community Periodic Surveys (GCPS) | 2000–2001: N=10,537 (11% HIV+); age distribution: HIV+ mean 39.2, HIV− mean 34.9 2008–2009: N=11,083 (10% HIV+); age distribution: HIV+ mean 42.1, HIV− mean 35.7 | 6 months – 11+ partners | HIV+: Decrease HIV−: Decrease |
Prestage et al. (2005) | Sydney, Australia | 1993–1995, 2001–2003 | Convenience sampling at gay community events, venues, and other sources: 1993–1995 Sydney Men and Sexual Health; 2001–2002 Positive Health; 2001–2003 Health in Men | 1993–1995 HIV+: N=191; age distribution: <25 9.7%, ≥50 4.6% 2001–2002 HIV+: N=154; age distribution: <25 0.0%, ≥50 19.4% 1993–1995 HV−: N=737; age distribution: <25 29.3%, ≥50 6.4% 2001–2003 HIV−: N=920; age distribution: <25 10.5%, ≥50 9.6% | 6 months – 10+ partners | HIV+: No change HIV−: No change |
Van de Ven et al. (2004) | Sydney, Australia | 1999, 2002 | Venue community-based recruitment at gay bars, sex on-premises venues, and social events/meetings | 1999: N=319 (3.2% HIV+); age distribution: median 29 range 19–65 2002: N=457 (3.6% HIV+); age distribution: median 30 range 19–65 | 6 months – 11+ partners | Overall: No change |
Vodstrcil et al. (2011) | Melbourne, Australia | 2002–2009 | all MSM attending a sexual health clinic with a positive STD result | N=7133 – total; age distribution: median 31 range 15–84 (HIV prevalence not reported) | 3 months – 2+ partners | Overall: Decrease |
Chow et al. (2015) | Melbourne, Australia | 2007–2013 | All MSM attending a sexual health clinic | 2007: N=2,607 2008: N=3,191 2009: N=3,566 2010: N=4,082 2011: N=4,614 2012: N=5,422 2013: N=6,188 (HIV prevalence not reported) Age distribution overall (not presented by year): median 30 range 14–85 | 12 months –11+ partners | Overall: Decrease |
Condomless anal sex with any, casual or main sex partners
Among the 29 studies that examined condomless anal sex from 1990 to 2013 (21–28, 34–41, 43–47, 50–57), 19 findings were included in the analysis of condomless anal sex (Figure 2), 19 findings were included in the analysis of condomless anal sex with casual partners (Figure 3A), and 12 findings were included in the analysis of condomless anal sex with main partners (Figure 3B). Figure 2 showed an upward trend in condomless anal sex with any partners from 1990 to 2012 among most of the study samples. The results of the multi-level models indicated a significant positive slope for the summary line (overall analysis without knot for the time period 1990–2012: beta = 0.05, p < 0.001; with a knot: 1990–2002, beta = 0.07, p < 0.001; 2003–2012, beta = 0.04, p < 0.001). Sensitivity analyses showed similar results when only cross-sectional studies were included. There were not enough cohort studies to run a separate sensitivity analysis. Sensitivity analysis among HIV-positive samples and HIV-negative samples also did not differ substantially. Figure 3 also showed upward trends in condomless anal sex by partner type. As seen in Figure 3A, the summary line indicated a significant increase in the percentage of MSM who engaged in condomless anal sex with casual partners over time (overall analysis without knot for the time period 1992–2013: beta = 0.05, p<0.001; with a knot: 1992–2002, beta = 0.10, p < 0.001; 2003–2013, beta = 0.03, p < 0.001). Similarly, Figure 3B showed a significant increase in the percentage of MSM who engaged in condomless anal sex with main partners over time (overall analysis without knot for the time period 1992–2013: beta = 0.03, p < 0.001; with a knot: 1992–2002, beta = 0.07, p < 0.001; 2003–2013, beta = 0.01, p = 0.004). Sensitivity analyses showed for CAS with a casual partner, results were similar when only cross-sectional studies were included. There were not enough cohort studies or studies with stratified results by HIV status to run separate sensitivity analyses. None of the CAS with a main partner studies were cohort designs and none presented data stratified by HIV status.
Condomless anal sex with a partner of unknown/discordant HIV status
From the 16 studies that examined condomless anal sex with a partner of unknown/discordant HIV status from 1994 to 2011 (22, 23, 25–29, 35, 37, 39, 42, 44, 51–53, 57), 25 findings were included in the analysis (Figure 4). The results of the multi-level models indicated a significant increase in the behavior over time (overall analysis without knot for the time period 1994–2011: beta = 0.03, p < 0.001; with a knot: 1994–2002, beta = 0.05, p < 0.001; 2003–2011, beta = 0.02, p < 0.001). Results were not substantially different for sensitivity analyses that stratified by study design or HIV status. However, although the slopes were similar to the overall analysis, sensitivity analyses for HIV-positive samples and HIV-negative samples did not result in significant betas for the 2003–2011 time period.
Number of sex partners
Sixteen studies examined trends in numbers of partners between 1992 and 2013 (30–33, 36, 39, 41, 45–49, 51, 53, 55, 56). Since the included studies had a wide range of cut-points from 2 or more partners to greater than 20 partners, we divided the studies into two groups: 2+ to 6+ partners (9 findings, Figure 5A) and 10+ to 21+ partners (10 findings, Figure 5B). The multi-level models without a knot did not produce stable results for either group. However, the models with a knot at 2002 generated an estimate for the summary line parameters. The knot analysis of the studies with a cut-point at 2 to 6 partners showed that the percentages of MSM who reported 2+ to 6+ partners did not change between 1992 and 2002 (beta = 0.004, p = 0.75, Figure 5A). There was an increase from 2003 to 2013 (beta = 0.08, p < 0.001, Figure 5A) primarily due to one large study that had a significant increasing trend. When this study was removed from the analysis, the slope from 2003 to 2013 was negative (beta = −0.02, p = 0.05). The knot analysis of the studies with a cut-point at 10 to 21 partners showed that the percentages of MSM who reported having 10+ to 21+ partners did not change between 1992 and 2002, and there was a significant downward trend from 2003 to 2011 (1992–2002, beta = 0.005, p = 0.55; 2003–2011, beta = −0.04, p < 0.001). None of the studies for the number of sex partners outcome were cohorts, and too few reported results stratified by HIV status to conduct a stratified analysis.
Discussion
This systematic review of studies conducted in high-income countries indicated increasing sexual risk behaviors over time among MSM. The upward trends were seen not only in condomless anal sex, condomless anal sex with casual partners and main partners, but also in condomless anal sex with partners of unknown or discordant HIV status, the highest-risk behavior for HIV transmission and acquisition. For these behaviors there was a steady increase from the 1990s through 2013, but the knot analysis suggested the rate of increase may have been slightly lower in 2003 and later compared to the earlier years. This could possibly be explained by a more rapid change in condom norms after the introduction of ART with a slowing of change overtime. Although there may be a decreasing trend in the number of sex partners since 2002, the increasing condomless anal sex, especially with partners of unknown or discordant HIV status, may partially explain the increase in HIV infections among MSM in high-income countries despite increasing treatment coverage during the same time frame, as seen in other studies (58).
There are several plausible explanations for why condomless anal sex is increasing. Condom fatigue, complacency about HIV, availability of other prevention options, optimism about HIV treatments, and the adoption of seroadaptive strategies may have eroded consistent condom use (18, 59). For example, MSM could be engaging in more serosorting or they, or their partners, could be on ART and virally suppressed or on PrEP to lower risk of HIV transmission. A recent study in the United States using the National HIV Behavioral Surveillance data found that the increases in condomless sex among MSM from 2005 to 2014 were not associated with serosorting or ART (60). Although the study found evidence of serosorting among HIV-positive MSM there was no indication that HIV-negative MSM were serosorting beyond what would be expected by chance (61). Based on our review, there appears to be a downward trend in the number of partners since 2002. The reason for this trend is unclear. However, researchers in Australia have noted a shift away from open relationships among MSM, which could help explain the reduction in number of partners (48). The extent to which the downward trend is actually occurring and why it might be occurring requires further examination. Other potential correlates of condomless sex that have been examined in the literature include methamphetamine use, alcohol use (62, 63), depression (64), and increased access to internet and mobile-app for seeking sexual partners (65, 66). The evidence on what contributes to these trends among MSM is still limited. Our study echoes the call for comprehensive HIV prevention for MSM (2, 3, 67) as well as more explanatory research to help understand the contributors of these trends.
The HIV prevention paradigm has expanded in recent years to include a focus on biomedical interventions such as ART and PrEP and helping people identify the best prevention option or options for them and their partners (68). PrEP was not widely available during the time period of the studies included in this review. This new prevention tool could help to offset the increased risk due to increases in condomless anal sex (16). As PrEP becomes more widely used, studies can evaluate its impact on HIV transmission rates and sexual behaviors. To better understand the influence and impact of ART and PrEP use, behavioral surveillance systems need to include more nuanced measures of biomedical prevention (69, 70). However, awareness of HIV status is not universal and increasing efforts are needed to reach optimal uptake of biomedical interventions. In addition, condom use continues to be a critical component of a comprehensive approach to HIV prevention among MSM (71) and condoms protect against many STIs which have been increasing among MSM worldwide. The United States CDC as well UNAIDS recommend condom distribution programs as part of an effective combination prevention program (72, 73). Furthermore, condom promotion interventions have success in increasing condom use among MSM, as evidenced by an intervention in New Zealand (74).
The results of this systematic review should be considered in light of the following limitations. The sexual risk behavior data were self-reported and these sensitive behaviors may have been under-reported. This may have been a bigger issue in some studies than others due to variations in data collection method (face-to-face interview versus self-interview). The outcome definitions also varied from study to study, in particular the recall period time frame. The samples in the included studies may not be representative of all MSM as many were convenience samples or venue-based recruitment samples. In some countries, the trends may differ across communities of MSM and thus the overall trend on the country level masks these differences. Only studies written in English were included in the review. Therefore, some studies from non-English speaking countries could have been excluded. The exclusion of studies published before 2004 could have resulted in missing some trend studies that covered the earlier time period. Because the samples presented the age composition results in different manners (median, mean, categorical), it was impossible to control for age in the analyses to better understand the impact of different generations of MSM on HIV risk. Study limitations also pointed to further research needs. Collecting and reporting sex behavior data stratified by HIV-status of participants and partners, standardizing the collection of key indicators for comparison purposes, and collecting additional measures on the use of biomedical prevention strategies (e.g., participants and partner use of ART and PrEP) will facilitate data synthesis and increase our understanding of why these behavioral trends are occurring.
The landscape of HIV prevention has changed substantially in the past decade, both because of biomedical advances such as ART and PrEP and because of the evolution of the risk environment for MSM. The increases in condomless anal sex among MSM, especially with partners of unknown or discordant HIV status, found in our review may help explain the increase in HIV infections among MSM documented in some high-income countries. Continuous monitoring of HIV, risk behaviors, and use of prevention and treatment is needed to evaluate prevention efforts and monitor HIV transmission risk.
Acknowledgments
Funding: There was no external funding source for this work.
We would like to thank Amy Lansky for her feedback on the research questions, data interpretation, and manuscript.
Footnotes
Compliance with Ethical Standards:
Ethical approval: This article does not contain any studies with human participants performed by any of the authors.
Conflict of Interest: The authors declare that they have no conflict of interest.
Disclaimer: The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention.
References
- 1.Beyrer C, Baral SD, Collins C, et al. The global response to HIV in men who have sex with men. Lancet. 2016;388(10040):198–206. doi: 10.1016/S0140-6736(16)30781-4. [DOI] [PubMed] [Google Scholar]
- 2.Sullivan PS, Hamouda O, Delpech V, et al. Reemergence of the HIV epidemic among men who have sex with men in North America, Western Europe, and Australia 1996–2005. Ann Epidemiol. 2009;19(6):423–31. doi: 10.1016/j.annepidem.2009.03.004. [DOI] [PubMed] [Google Scholar]
- 3.Beyrer C, Sullivan P, Sanchez J, et al. The increase in global HIV epidemics in MSM. AIDS. 2013;27(17):2665–78. doi: 10.1097/01.aids.0000432449.30239.fe. [DOI] [PubMed] [Google Scholar]
- 4.Patel P, Borkowf CB, Brooks JT, Lasry A, Lansky A, Mermin J. Estimating per-act HIV transmission risk: a systematic review. AIDS. 2014;28(10):1509–19. doi: 10.1097/QAD.0000000000000298. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Smith DK, Pals SL, Herbst JH, Shinde S, Carey JW. Development of a clinical screening index predictive of incident HIV infection among men who have sex with men in the United States. J Acquir Immune Defic Syndr. 2012;60(4):421–7. doi: 10.1097/QAI.0b013e318256b2f6. [DOI] [PubMed] [Google Scholar]
- 6.Menza TW, Hughes JP, Celum CL, Golden MR. Prediction of HIV acquisition among men who have sex with men. Sex Transm Dis. 2009;36(9):547–55. doi: 10.1097/OLQ.0b013e3181a9cc41. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Cohen MS, Chen YQ, McCauley M, et al. Prevention of HIV-1 infection with early antiretroviral therapy. N Engl J Med. 2011;365(6):493–505. doi: 10.1056/NEJMoa1105243. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Rodger AJ, Cambiano V, Bruun T, et al. Sexual activity without condoms and risk of HIV transmission in serodifferent couples when the HIV-positive partner is using suppressive antiretroviral therapy. JAMA. 2016;316(2):171–81. doi: 10.1001/jama.2016.5148. [DOI] [PubMed] [Google Scholar]
- 9.Grulich AE, Bavinton BR, Jin F, et al. HIV transmission in male serodiscordant couples in Australia, Thailand and Brazil. Conference on Retroviruses and Opportunistic Infections; Poster No 1019LB; February 23–26, 2015; Seattle, Washington. [Google Scholar]
- 10.Grant RM, Lama JR, Anderson PL, et al. Preexposure chemoprophylaxis for HIV prevention in men who have sex with men. N Engl J Med. 2010;363(27):2587–99. doi: 10.1056/NEJMoa1011205. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Okwundu CI, Uthman OA, Okoromah CA. Antiretroviral pre-exposure prophylaxis (PrEP) for preventing HIV in high-risk individuals. Cochrane Database Syst Rev. 2012;7:CD007189. doi: 10.1002/14651858.CD007189.pub3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Liu AY, Vittinghoff E, Chillag K, et al. Sexual risk behavior among HIV-uninfected men who have sex with men participating in a tenofovir preexposure prophylaxis randomized trial in the United States. J Acquir Immune Defic Syndr. 2013;64(1):87–94. doi: 10.1097/QAI.0b013e31828f097a. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Marcus JL, Glidden DV, Mayer KH, et al. No evidence of sexual risk compensation in the iPrEx trial of daily oral HIV preexposure prophylaxis. PLoS One. 2013;8(12):e81997. doi: 10.1371/journal.pone.0081997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.CDC. Preexposure Prophylaxis for the prevention of HIV infection in the United States – 2014: A clinical practice guideline. 2016 Jun 13; Available from: http://www.cdc.gov/hiv/pdf/prepguidelines2014.pdf.
- 15.National HIV/AIDS strategy for the United States: Updated to 2020. 2015 Jul; Available from: https://www.aids.gov/federal-resources/national-hiv-aids-strategy/nhas-update.pdf.
- 16.Phillips AN, Cambiano V, Nakagawa F, et al. Increased HIV incidence in men who have sex with men despite high levels of ART-induced viral suppression: Analysis of an extensively documented epidemic. PLoS One. 2013;8(2):e55312. doi: 10.1371/journal.pone.0055312. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Bezemer D, de Wolf F, Boerlijst MC, et al. A resurgent HIV-1 epidemic among men who have sex with men in the era of potent antiretroviral therapy. AIDS. 2008;22(9):1071–7. doi: 10.1097/QAD.0b013e3282fd167c. [DOI] [PubMed] [Google Scholar]
- 18.Wilson DP. HIV treatment as prevention: natural experiments highlight limits of antiretroviral treatment as HIV prevention. PLoS Med. 2012;9(7):e1001231. doi: 10.1371/journal.pmed.1001231. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Abara WE, Hess KL, Neblett Fanfair R, Bernstein KT, Paz-Bailey G. Syphilis trends among men who have sex with men in the United States and western Europe: A systematic review of trend studies published between 2004 and 2015. PLoS One. 2016;11(7):e0159309. doi: 10.1371/journal.pone.0159309. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.The World Bank: Country and lending groups. 2016 Jun 17; Available from: http://data.worldbank.org/about/country-and-lending-groups#High_income.
- 21.Leichliter JS, Haderxhanaj LT, Chesson HW, Aral SO. Temporal trends in sexual behavior among men who have sex with men in the United States, 2002 to 2006–2010. J Acquir Immune Defic Syndr. 2013;63(2):254–8. doi: 10.1097/QAI.0b013e31828e0cfc. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.CDC. HIV testing and risk behaviors among gay, bisexual, and other men who have sex with men - United States. MMWR Morb Mortal Wkly Rep. 2013;62(47):958–62. [PMC free article] [PubMed] [Google Scholar]
- 23.Golden MR, Stekler J, Hughes JP, Wood RW. HIV serosorting in men who have sex with men: is it safe? J Acquir Immune Defic Syndr. 2008;49(2):212–8. doi: 10.1097/QAI.0b013e31818455e8. [DOI] [PubMed] [Google Scholar]
- 24.Kalichman SC, Eaton L, White D, et al. Beliefs about treatments for HIV/AIDS and sexual risk behaviors among men who have sex with men, 1997–2006. J Behav Med. 2007;30(6):497–503. doi: 10.1007/s10865-007-9123-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Osmond DH, Pollack LM, Paul JP, Catania JA. Changes in prevalence of HIV infection and sexual risk behavior in men who have sex with men in San Francisco: 1997 2002. Am J Public Health. 2007;97(9):1677–83. doi: 10.2105/AJPH.2005.062851. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Scheer S, Kellogg T, Klausner JD, et al. HIV is hyperendemic among men who have sex with men in San Francisco: 10-year trends in HIV incidence, HIV prevalence, sexually transmitted infections and sexual risk behaviour. Sex Transm Infect. 2008;84(6):493–8. doi: 10.1136/sti.2008.031823. [DOI] [PubMed] [Google Scholar]
- 27.McFarland W, Chen YH, Nguyen B, et al. Behavior, intention or chance? A longitudinal study of HIV seroadaptive behaviors, abstinence and condom use. AIDS Behav. 2012;16(1):121–31. doi: 10.1007/s10461-011-9936-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Pantalone DW, Tomassilli JC, Starks TJ, Golub SA, Parsons JT. Unprotected anal intercourse with casual male partners in urban gay, bisexual, and other men who have sex with men. Am J Public Health. 2015;105(1):103–10. doi: 10.2105/AJPH.2014.302093. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Menza TW, Kerani RP, Handsfield HH, Golden MR. Stable sexual risk behavior in a rapidly changing risk environment: findings from population-based surveys of men who have sex with men in Seattle, Washington, 2003–2006. AIDS Behav. 2011;15(2):319–29. doi: 10.1007/s10461-009-9626-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Kellogg TA, Hecht J, Bernstein K, et al. Comparison of HIV behavioral indicators among men who have sex with men across two survey methodologies, San Francisco, 2004 and 2008. Sex Transm Dis. 2013;40(9):689–94. doi: 10.1097/01.olq.0000431354.96087.50. [DOI] [PubMed] [Google Scholar]
- 31.Sudhinaraset M, Raymond HF, McFarland W. Convergence of HIV prevalence and inter-racial sexual mixing among men who have sex with men, San Francisco, 2004–2011. AIDS Behav. 2013;17(4):1550–6. doi: 10.1007/s10461-012-0370-3. [DOI] [PubMed] [Google Scholar]
- 32.Reilly KH, Neaigus A, Jenness SM, et al. Trends in HIV prevalence and risk behavior among men who have sex with men in New York City, 2004–2011. AIDS Educ Prev. 2014;26(2):134–43. doi: 10.1521/aeap.2014.26.2.134. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Fendrich M, Mackesy-Amiti ME, Johnson TP, Pollack LM. Sexual risk behavior and drug use in two Chicago samples of men who have sex with men: 1997 vs. 2002. J Urban Health. 2010;87(3):452–66. doi: 10.1007/s11524-009-9432-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Jansen IA, Geskus RB, Davidovich U, et al. Ongoing HIV-1 transmission among men who have sex with men in Amsterdam: A 25-year prospective cohort study. AIDS. 2011;25(4):493–501. doi: 10.1097/QAD.0b013e328342fbe9. [DOI] [PubMed] [Google Scholar]
- 35.Stolte IG, de Wit JB, van Eeden A, Coutinho RA, Dukers NH. Perceived viral load, but not actual HIV-1-RNA load, is associated with sexual risk behaviour among HIV-infected homosexual men. AIDS. 2004;18(14):1943–9. doi: 10.1097/00002030-200409240-00010. [DOI] [PubMed] [Google Scholar]
- 36.Op de Coul EL, Warning TD, Koedijk FD, Dutch STIc. Sexual behaviour and sexually transmitted infections in sexually transmitted infection clinic attendees in the Netherlands, 2007–2011. Int J STD AIDS. 2014;25(1):40–51. doi: 10.1177/0956462413491736. [DOI] [PubMed] [Google Scholar]
- 37.Cowan SA, Gerstoft J, Haff J, Christiansen AH, Nielsen J, Obel N. Stable incidence of HIV diagnoses among Danish MSM despite increased engagement in unsafe sex. J Acquir Immune Defic Syndr. 2012;61(1):106–11. doi: 10.1097/QAI.0b013e31825af890. [DOI] [PubMed] [Google Scholar]
- 38.Casalino E, Choquet C, Leleu A, et al. Trends in condom use and risk behaviours after sexual exposure to HIV: a seven-year observational study. PLoS One. 2014;9(8):e104350. doi: 10.1371/journal.pone.0104350. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39.Moreau-Gruet F, Dubois-Arber F, Jeannin A. Long-term HIV/AIDS-related prevention behaviours among men having sex with men: Switzerland 1992–2000. AIDS Care. 2006;18(1):35–43. doi: 10.1080/09540120500099886. [DOI] [PubMed] [Google Scholar]
- 40.Bozicevic I, Lepej SZ, Rode OD, et al. Prevalence of HIV and sexually transmitted infections and patterns of recent HIV testing among men who have sex with men in Zagreb, Croatia. Sex Transm Infect. 2012;88(7):539–44. doi: 10.1136/sextrans-2011-050374. [DOI] [PubMed] [Google Scholar]
- 41.Klavs I, Bergant N, Kastelic Z, Lamut A, Kustec T. Disproportionate and increasing burden of HIV infection among men who have sex with men in Slovenia: Surveillance data for 1999–2008. Euro Surveill. 2009;14(47) doi: 10.2807/ese.14.47.19419-en. [DOI] [PubMed] [Google Scholar]
- 42.Seng R, Rolland M, Beck-Wirth G, et al. Trends in unsafe sex and influence of viral load among patients followed since primary HIV infection, 2000–2009. AIDS. 2011;25(7):977–88. doi: 10.1097/QAD.0b013e328345ef12. [DOI] [PubMed] [Google Scholar]
- 43.Zablotska IB, Kippax S, Grulich A, Holt M, Prestage G. Behavioural surveillance among gay men in Australia: methods, findings and policy implications for the prevention of HIV and other sexually transmissible infections. Sex Health. 2011;8(3):272–9. doi: 10.1071/SH10125. [DOI] [PubMed] [Google Scholar]
- 44.Zablotska IB, Crawford J, Imrie J, et al. Increases in unprotected anal intercourse with serodiscordant casual partners among HIV-negative gay men in Sydney. AIDS Behav. 2009;13(4):638–44. doi: 10.1007/s10461-008-9506-x. [DOI] [PubMed] [Google Scholar]
- 45.Van de Ven P, Mao L, Prestage G. Gay Asian men in Sydney resist international trend: No change in rates of unprotected anal intercourse, 1999–2002. AIDS Educ Prev. 2004;16(1):1–12. doi: 10.1521/aeap.16.1.1.27726. [DOI] [PubMed] [Google Scholar]
- 46.Prestage G, Mao L, Fogarty A, 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;29(6):530–5. doi: 10.1111/j.1467-842x.2005.tb00245.x. [DOI] [PubMed] [Google Scholar]
- 47.Chow EP, Tomnay J, Fehler G, et al. Substantial increases in chlamydia and gonorrhea positivity unexplained by changes in individual-level sexual behaviors among men who have sex with men in an Australian sexual health service from 2007 to 2013. Sex Transm Dis. 2015;42(2):81–7. doi: 10.1097/OLQ.0000000000000232. [DOI] [PubMed] [Google Scholar]
- 48.Holt M, Lee E, Prestage GP, Zablotska I, de Wit J, Mao L. The converging and diverging characteristics of HIV-positive and HIV-negative gay men in the Australian Gay Community Periodic Surveys, 2000–2009. AIDS Care. 2013;25(1):28–37. doi: 10.1080/09540121.2012.686598. [DOI] [PubMed] [Google Scholar]
- 49.Vodstrcil LA, Fairley CK, Fehler G, et al. Trends in chlamydia and gonorrhea positivity among heterosexual men and men who have sex with men attending a large urban sexual health service in Australia, 2002–2009. BMC Infect Dis. 2011;11:158. doi: 10.1186/1471-2334-11-158. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 50.Mercer CH, Fenton KA, Copas AJ, et al. Increasing prevalence of male homosexual partnerships and practices in Britain 1990–2000: Evidence from national probability surveys. AIDS. 2004;18(10):1453–8. doi: 10.1097/01.aids.0000131331.36386.de. [DOI] [PubMed] [Google Scholar]
- 51.Hickson F, Bonell C, Hargreaves J, Reid D, Weatherburn P. HIV testing and HIV serostatus-specific sexual risk behaviour among men who have sex with men living in England and recruited through the internet in 2001 and 2008. Sexuality Research and Social Policy. 2013;10(1):15–23. doi: 10.1007/s13178-012-0106-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 52.Lattimore S, Thornton A, Delpech V, Elford J. Changing patterns of sexual risk behavior among London gay men: 1998–2008. Sex Transm Dis. 2011;38(3):221–9. doi: 10.1097/OLQ.0b013e3181f2ebe1. [DOI] [PubMed] [Google Scholar]
- 53.Williamson LM, Dodds JP, Mercey DE, Johnson AM, Hart GJ. Increases in HIV-related sexual risk behavior among community samples of gay men in London and Glasgow: How do they compare? J Acquir Immune Defic Syndr. 2006;42(2):238–41. doi: 10.1097/01.qai.0000214816.03411.c9. [DOI] [PubMed] [Google Scholar]
- 54.Hart GJ, Williamson LM. Increase in HIV sexual risk behaviour in homosexual men in Scotland, 1996–2002: Prevention failure? Sex Transm Infect. 2005;81(5):367–72. doi: 10.1136/sti.2004.013995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 55.Saxton PJ, Dickson NP, Hughes AJ. Location-based HIV behavioural surveillance among MSM in Auckland, New Zealand 2002–2011: Condom use stable and more HIV testing. Sex Transm Infect. 2014;90(2):133–8. doi: 10.1136/sextrans-2013-051160. [DOI] [PubMed] [Google Scholar]
- 56.Saxton PJ, Dickson NP, Hughes AJ. Trends in web-based HIV behavioural surveillance among gay and bisexual men in New Zealand: Complementing location-based surveillance. AIDS Care. 2015;27(6):762–6. doi: 10.1080/09540121.2014.998615. [DOI] [PubMed] [Google Scholar]
- 57.George C, Alary M, Otis J, et al. Nonnegligible increasing temporal trends in unprotected anal intercourse among men who have sexual relations with other men in Montreal. J Acquir Immune Defic Syndr. 2006;41(3):365–70. doi: 10.1097/01.qai.0000209904.97502.2b. [DOI] [PubMed] [Google Scholar]
- 58.Zablotska IB, Prestage G, Middleton M, Wilson D, Grulich AE. Contemporary HIV diagnoses trends in Australia can be predicted by trends in unprotected anal intercourse among gay men. AIDS. 2010;24(12):1955–8. doi: 10.1097/QAD.0b013e32833bf74a. [DOI] [PubMed] [Google Scholar]
- 59.Kippax S, Holt M. Diversification of risk reduction strategies and reduced threat of HIV may explain increases in condomless sex. AIDS. 2016;30(18):2898–9. doi: 10.1097/QAD.0000000000001260. [DOI] [PubMed] [Google Scholar]
- 60.Paz-Bailey G, Mendoza M, Finlayson T, et al. Trends in condom use among men who have sex with men in the United States: The role of antiretroviral therapy and sero-adaptive strategies. AIDS. 2016 doi: 10.1097/QAD.0000000000001139. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 61.Paz-Bailey G, Wejnert C, Mendoza MC, Prejean J. Response to diversification of risk-reduction strategies and reduced threat of HIV may explain increases in condomless sex. AIDS. 2016;30(18):2900–1. doi: 10.1097/QAD.0000000000001261. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 62.Vosburgh HW, Mansergh G, Sullivan PS, Purcell DW. A review of the literature on event-level substance use and sexual risk behavior among men who have sex with men. AIDS Behav. 2012;16(6):1394–410. doi: 10.1007/s10461-011-0131-8. [DOI] [PubMed] [Google Scholar]
- 63.Kramer SC, Schmidt AJ, Berg RC, et al. Factors associated with unprotected anal sex with multiple non-steady partners in the past 12 months: Results from the European Men-Who-Have-Sex-With-Men Internet Survey (EMIS 2010) BMC Public Health. 2016;16:47. doi: 10.1186/s12889-016-2691-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 64.Alvy LM, McKirnan DJ, Mansergh G, et al. Depression is associated with sexual risk among men who have sex with men, but is mediated by cognitive escape and self-efficacy. AIDS Behav. 2011;15(6):1171–9. doi: 10.1007/s10461-010-9678-z. [DOI] [PubMed] [Google Scholar]
- 65.Liau A, Millett G, Marks G. Meta-analytic examination of online sex-seeking and sexual risk behavior among men who have sex with men. Sex Transm Dis. 2006;33(9):576–84. doi: 10.1097/01.olq.0000204710.35332.c5. [DOI] [PubMed] [Google Scholar]
- 66.Melendez-Torres GJ, Nye E, Bonell C. Internet sex-seeking is inconsistently linked with sexual risk in men who have sex with men: Systematic review of within-subjects comparisons. Sex Health. 2015;12(3):183–7. doi: 10.1071/SH14183. [DOI] [PubMed] [Google Scholar]
- 67.McDaid LM, Hart GJ. Sexual risk behaviour for transmission of HIV in men who have sex with men: Recent findings and potential interventions. Curr Opin HIV AIDS. 2010;5(4):311–5. doi: 10.1097/COH.0b013e32833a0b86. [DOI] [PubMed] [Google Scholar]
- 68.CDC. HIV Risk Reduction Tool. 2017 Apr 13; Available from: https://wwwn.cdc.gov/hivrisk/
- 69.Holt M, Lea T, Mao L, et al. Adapting behavioural surveillance to antiretroviral-based HIV prevention: reviewing and anticipating trends in the Australian Gay Community Periodic Surveys. Sex Health. 2016 doi: 10.1071/SH16072. [DOI] [PubMed] [Google Scholar]
- 70.Holt M. Time to accommodate antiretroviral-based HIV prevention. Lancet HIV. 2016;3(9):e400–1. doi: 10.1016/S2352-3018(16)30049-2. [DOI] [PubMed] [Google Scholar]
- 71.Lasry A, Sansom SL, Wolitski RJ, et al. HIV sexual transmission risk among serodiscordant couples: assessing the effects of combining prevention strategies. AIDS. 2014;28(10):1521–9. doi: 10.1097/QAD.0000000000000307. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 72.CDC. Condom Distribution as a Structural Level Intervention. 2017 Apr 3; Available from: https://www.cdc.gov/hiv/programresources/guidance/condoms/.
- 73.UNAIDS. UNFPA, WHO and UNAIDS: Position statement on condoms and the prevention of HIV, other sexually transmitted infections and unintended pregnancy. 2017 Apr 3; Available from: http://www.unaids.org/en/resources/presscentre/featurestories/2015/july/20150702_condoms_prevention.
- 74.Adams J, Neville S, Parker K, Huckle T. Influencing condom use by gay and bisexual men for anal sex through social marketing: A program evaluation of Get it On! Social Marketing Quarterly. 2016:1–15. [Google Scholar]