HHS Public Access Author manuscript Author Manuscript
J Acquir Immune Defic Syndr. Author manuscript; available in PMC 2017 May 01. Published in final edited form as: J Acquir Immune Defic Syndr. 2016 May 1; 72(1): 79–86. doi:10.1097/QAI.0000000000000933.
Incidence of HIV infection and Sexually Transmitted Infections and Related Risk Factors among Very Young Men Who Have Sex with Men Robert Garofalo, MD, MPH1,2, Anna L. Hotton, PhD, MPH3, Lisa M. Kuhns, PhD, MPH1,2, Beau Gratzer, MPP1,4, and Brian Mustanski, PhD5
Author Manuscript
1Ann
& Robert H. Lurie Children’s Hospital of Chicago, Chicago, IL. USA
2Northwestern
University, Feinberg School of Medicine, Department of Pediatrics, Chicago, IL.
USA 3Division
of Infectious Diseases, John H. Stroger Hospital
4Howard
Brown Health Center, Chicago, IL
5Northwestern
University, Feinberg School of Medicine, Department of Medical Social Sciences, Chicago, IL USA
Abstract Author Manuscript
Introduction—The HIV epidemic continues to disproportionately affect men who have sex with men (MSM) in the US, with over a third of new infections in MSM occurring in younger men. Very few studies have reported on HIV and STI incidence and related risks among younger MSM, particularly among minors under 18 years of age. Methods—Data analyzed herein are from a longitudinal study of HIV-risk among 450 very young MSM in Chicago ages 16–20, recruited via respondent-driven sampling and followed for two years, with annual HIV and STI testing. We report estimated cumulative HIV and STI incidence over the 24-month follow-up using Kaplan-Meier methods and evaluated associations with incident infections using Cox Proportional Hazards regression.
Author Manuscript
Results—The final analytic sample was primarily non-White (83%); median age was 19; 25% of the sample was under age 18. 26 new HIV infections were detected over 632 person-years of follow-up. HIV incidence was 4.11/100 person years (95% CI=2.80–6.04) and STI incidence was 6.22/100 person-years (95% CI=4.54–8.51). Cumulative HIV incidence over 24 months of followup was 7.32% (95% CI= 5.05–10.57), with higher incidence among racial/ethnic minorities. In multivariate analyses, non-White race and recent sexual partner concurrency were associated with both HIV and STI infection; HIV testing history and sex with an HIV-positive partner were associated with increased risk of HIV infection.
Corresponding author: Robert Garofalo, Ann & Robert H. Lurie Children’s Hospital of Chicago, 225 E. Chicago Avenue, #161, Chicago, IL. 60611, [email protected].
Garofalo et al.
Page 2
Author Manuscript
Discussion—High rates of incident HIV infection and STIs among very young MSM and the relationship between incidence and race/ethnicity, concurrency and partner characteristics indicate potential focal points of future intervention and the need for continued vigilance. Keywords HIV/STI Infection; HIV/STI Epidemiology; Young Men Who Have Sex with Men
INTRODUCTION
Author Manuscript
In its fourth decade, the HIV epidemic continues to disproportionately affect gay, bisexual and other men who have sex with men (collectively referred to as MSM) in the United States.1 Male-to-male sexual contact accounted for 65% of the approximately 47,000 new HIV infections during 2013,1 even though MSM only represent 2% of the population.2 Over 30% of new infections among MSM occur in young MSM (YMSM) aged 13–24,3 and young Black MSM accounted for more new infections than any other age group or race of MSM.3 Despite a recent increase in attention focused on prevention among YMSM,4 they continue to be vulnerable to becoming infected with HIV.5
Author Manuscript
Assessing HIV incidence allows researchers and practitioners to better understand the current and on-going epidemic in specific populations. Stall and colleagues conducted a meta-analysis of published incidence rates among MSM and found stable annual HIV incidence (2.39%) between 1995 and 2005,6 the first decade after the introduction of highly active antiretroviral treatment (HAART). Alarmingly, the researchers reported that if such incidence was sustained, cumulative prevalence of infection by age 40 would be 40%.6 Using a CDC estimate of 4.0% annual HIV incidence among Black YMSM,7 Stall et al estimated cumulative prevalence of 59.3% by age 40.6
Author Manuscript
More recent HIV incidence studies point to a troubling story for Black YMSM in the U.S. Data published from the 2008 cycle of the National HIV Behavioral Surveillance System (NHBS) estimated an annual HIV incidence rate of 2.9% for all YMSM aged 18–24; however, the annual rate for Black YMSM in the study was 5.1%.8 Koblin and colleagues reported similar findings from HIV Prevention Trials Network (HPTN) Study 061 (i.e., the BROTHERS Study) which enrolled a longitudinal cohort of Black MSM in six US cities. They found an annual HIV incidence of 3.0% for all Black MSM in the cohort, but an incidence of 5.9% for Black MSM under the age of 30.9 Sullivan and colleagues estimated 10.9 new HIV infections per 100 person years among Black MSM aged 18–24 enrolled in an Atlanta cohort study.10 Finally, in a recent study of YMSM, ages 18–19, in New York City (N=594), annual HIV incidence was 2.85 per 100 person years with a 3-year cumulative rate of 7.2% over the entire period.11 An important limitation of these studies and the HIV incidence literature more generally, is that no MSM participants were under the age of 18 at the time of enrollment. Factors associated with HIV incidence among YMSM in the studies cited above include Black or other race (vs. White),8,11 lower level of education (< high school), substance use before or during last sexual episode8 and having sex with an HIV-positive or unknown status partner.9 Koblin and colleagues found that among Black MSM in particular, younger men J Acquir Immune Defic Syndr. Author manuscript; available in PMC 2017 May 01.
Garofalo et al.
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Author Manuscript Author Manuscript
had higher levels of sexual risk (i.e., more likely to report sex with HIV-positive/unknown status partners vs. older men), were more likely to have a sexually transmitted infection (STI) at follow-up, and were less likely to have a usual place for healthcare or to have visited a health care provider recently,9 thus providing evidence for risk behavior, concomitant STIs, and health care factors as potential reasons for high incidence among younger Black MSM (vs. older). A recent analysis of data from three longitudinal studies of MSM early in the highly active antiretroviral therapy era adds to this evidence finding higher per contact risk of HIV seroconversion (i.e., per sexual act) with HIV seropositive partners in younger MSM (6.1 per 100 person years) for Black men in particular.21 Unfortunately, we were unable to find any studies that specifically estimated STI incidence among YMSM using longitudinal study designs, thus there is a need to estimate both STI and HIV incidence in concert and the predictive potential of STIs on subsequent HIV incidence. The purpose of this analysis is to fill gaps in the existing literature by calculating incidence of new HIV and urogenital gonorrhea/Chlamydia infections in very young MSM age 16–20 at baseline and to describe factors associated with new infections.
Author Manuscript
METHODS Participant Recruitment Data analyzed herein come from a longitudinal study of HIV-risk among 450 YMSM conducted between 2009 and 2015 in Chicago (known as “Crew 450”), the nation’s third largest city and the epicenter of the HIV/AIDS epidemic in the Midwest. The purpose of the study was to characterize the course, and predictors of HIV/STI risk and incident infection among YMSM. We used a modified form of respondent-driven sampling (RDS) to recruit J Acquir Immune Defic Syndr. Author manuscript; available in PMC 2017 May 01.
Garofalo et al.
Page 4
Author Manuscript
YMSM between ages 16 and 20, which yielded a greater proportion of initial recruits or “seeds” than a conventional RDS approach.22 Segmentation in patterns of recruitment by race/ethnicity and a relatively large number of Black seeds also resulted in overrepresentation of youth of color in the sample.22 Seeds were recruited through community-based convenience sampling with study promotional materials distributed via active and passive means in community locations frequented by YMSM. Eligible participants were within the target age-range at baseline, English-speaking, assigned a male sex at birth, had any prior sexual encounter with a male or identified as gay/bisexual, resided in Chicago or suburban Cook County, and were available for multiple follow-ups across 24 months. A total of four study enrollment sites in Chicago were utilized, three sites on the north side of the city and one on the near southwest side. Data Collection and Measures
Author Manuscript Author Manuscript
Following written assent/consent procedures, data were collected via computer-assisted selfinterviewing (CASI) and participants were tested for HIV/STIs; follow-up interview data were collected approximately every 6 months thereafter, with HIV/STI testing completed at 12-month intervals. In order to retain participants over time, multiple attempts to contact them using all available contact information were made, including contacting friends, relatives, or others (whom the participants had indicated would always know how to contact them). Contact information was also updated at all study visits. Commercially available locator services were used to identify new contact information for those for whom all contact information became invalid, however, because of their young age (e.g., not often traceable via utility, mortgage or other billing), these services were not effective. Participants were reimbursed $45 for their time and travel at each visit (except the baseline visit, which was divided into two visits, total compensation was $70 at baseline), and the study received approval from institutional review boards of affiliated institutions, with waiver of parental permission for the participation of minors.
Author Manuscript
In terms of demographic indicators, participant age, race/ethnicity, and highest level of education were captured at the baseline interview as was self-reported HIV testing history (ever tested). Predictor variables were selected from a review of HIV among YMSM.5 Recall of prior six-month substance use and sexual risk were collected at baseline as well as all follow-up points and included: alcohol use, marijuana use, other drug use (i.e., cocaine, heroin, methamphetamines, opiates; non-prescription depressants, stimulants; psychedelics, Ecstasy, gamma hydroxybutyrate –GHB, Ketamine, and any inhalants), alcohol use during sex, drug use during sex, total male partners, unprotected anal sex with a male partner, sex with an HIV positive partner, sex with an unknown status partner, having exchanged sex for money or shelter, having concurrent sexual partners (i.e., either the participant or their most recent sexual partners), victimization by a sex partner (i.e., any affirmative response for any sex partner to the question: “Has [partner] ever hit, slapped, punched or hurt you?”), and having a male partner ≥ 5 years older. We included these last two variables in particular because of the young age of participants and prior work suggesting that developmental vulnerabilities, such as the assumed authority of older partners may put them at risk.23 HIV infection was determined by oral OraQuick/Orasure™ testing for those with unknown status and by self-report for those with known status (self-reported HIV-positive status was
J Acquir Immune Defic Syndr. Author manuscript; available in PMC 2017 May 01.
Garofalo et al.
Page 5
Author Manuscript
confirmed for 71% of self-reported cases via Orasure™, medical records or HIV-related medication prescription verification). Urogenital gonorrhea and Chlamydia infections were determined via urine polymerase chain reaction (PCR; Roche Diagnostics). Statistical Analysis
Author Manuscript
Urogenital gonorrhea and Chlamydia infection were combined and analyzed as a single composite outcome (herein referred to as STI) to improve power and because risk factors for the acquisition of urogenital gonorrhea and Chlamydia are similar. Results and conclusions did not change when the two infections were examined individually (data not shown). Analyses were conducted separately for HIV and STI to identify similarities or dissimilarities between exposures and associated risk of each infection. For STI, person-time was calculated as the time in months from the baseline visit (or the last visit at which the patient tested negative) to the first positive test. Participants with multiple infections were censored at the time of first infection. Loss to follow-up was defined as a case missing at a given time point not due to withdrawal, with no data provided at subsequent study visits. If participants missed a study visit and provided data at subsequent time points, all available data was included in the analysis. Participants who were lost to follow-up were censored at the last time point at which they provided data.
Author Manuscript
For HIV, person-time was calculated as the time from baseline to the last visit at which the patient tested negative or the midpoint of the interval between the first positive test and the preceding negative test for those who tested positive.24 We also calculated person-time using the date of the first positive test rather than the midpoint as the time of HIV infection and results were not substantially changed; presented findings use the midpoint as the time of infection. Cumulative HIV incidence was estimated using the Kaplan-Meier method. Incidence rates of HIV and STI were compared across exposure categories using the logrank test.
Author Manuscript
To assess the effect of fixed and time-varying exposures on HIV and STI, we fit extended Cox regression models with fixed and time-varying covariates to estimate univariable and multivariable hazard ratios for associations of exposures with incident infections. Age at baseline, race/ethnicity, education, ever having been tested for HIV, and infection with gonorrhea or Chlamydia at baseline were treated as time-fixed covariates for analysis. All other variables, including sexual behaviors and substance use, were assessed as timevarying. The timeframe for all exposures was the previous 6 months. The reported exposure at the time of infection was the exposure status associated with infection. For time-varying exposures, participants could contribute to exposed and unexposed risk sets at different time points. Variables with p
J Acquir Immune Defic Syndr. Author manuscript; available in PMC 2017 May 01. Published in final edited form as: J Acquir Immune Defic Syndr. 2016 May 1; 72(1): 79–86. doi:10.1097/QAI.0000000000000933.
Incidence of HIV infection and Sexually Transmitted Infections and Related Risk Factors among Very Young Men Who Have Sex with Men Robert Garofalo, MD, MPH1,2, Anna L. Hotton, PhD, MPH3, Lisa M. Kuhns, PhD, MPH1,2, Beau Gratzer, MPP1,4, and Brian Mustanski, PhD5
Author Manuscript
1Ann
& Robert H. Lurie Children’s Hospital of Chicago, Chicago, IL. USA
2Northwestern
University, Feinberg School of Medicine, Department of Pediatrics, Chicago, IL.
USA 3Division
of Infectious Diseases, John H. Stroger Hospital
4Howard
Brown Health Center, Chicago, IL
5Northwestern
University, Feinberg School of Medicine, Department of Medical Social Sciences, Chicago, IL USA
Abstract Author Manuscript
Introduction—The HIV epidemic continues to disproportionately affect men who have sex with men (MSM) in the US, with over a third of new infections in MSM occurring in younger men. Very few studies have reported on HIV and STI incidence and related risks among younger MSM, particularly among minors under 18 years of age. Methods—Data analyzed herein are from a longitudinal study of HIV-risk among 450 very young MSM in Chicago ages 16–20, recruited via respondent-driven sampling and followed for two years, with annual HIV and STI testing. We report estimated cumulative HIV and STI incidence over the 24-month follow-up using Kaplan-Meier methods and evaluated associations with incident infections using Cox Proportional Hazards regression.
Author Manuscript
Results—The final analytic sample was primarily non-White (83%); median age was 19; 25% of the sample was under age 18. 26 new HIV infections were detected over 632 person-years of follow-up. HIV incidence was 4.11/100 person years (95% CI=2.80–6.04) and STI incidence was 6.22/100 person-years (95% CI=4.54–8.51). Cumulative HIV incidence over 24 months of followup was 7.32% (95% CI= 5.05–10.57), with higher incidence among racial/ethnic minorities. In multivariate analyses, non-White race and recent sexual partner concurrency were associated with both HIV and STI infection; HIV testing history and sex with an HIV-positive partner were associated with increased risk of HIV infection.
Corresponding author: Robert Garofalo, Ann & Robert H. Lurie Children’s Hospital of Chicago, 225 E. Chicago Avenue, #161, Chicago, IL. 60611, [email protected].
Garofalo et al.
Page 2
Author Manuscript
Discussion—High rates of incident HIV infection and STIs among very young MSM and the relationship between incidence and race/ethnicity, concurrency and partner characteristics indicate potential focal points of future intervention and the need for continued vigilance. Keywords HIV/STI Infection; HIV/STI Epidemiology; Young Men Who Have Sex with Men
INTRODUCTION
Author Manuscript
In its fourth decade, the HIV epidemic continues to disproportionately affect gay, bisexual and other men who have sex with men (collectively referred to as MSM) in the United States.1 Male-to-male sexual contact accounted for 65% of the approximately 47,000 new HIV infections during 2013,1 even though MSM only represent 2% of the population.2 Over 30% of new infections among MSM occur in young MSM (YMSM) aged 13–24,3 and young Black MSM accounted for more new infections than any other age group or race of MSM.3 Despite a recent increase in attention focused on prevention among YMSM,4 they continue to be vulnerable to becoming infected with HIV.5
Author Manuscript
Assessing HIV incidence allows researchers and practitioners to better understand the current and on-going epidemic in specific populations. Stall and colleagues conducted a meta-analysis of published incidence rates among MSM and found stable annual HIV incidence (2.39%) between 1995 and 2005,6 the first decade after the introduction of highly active antiretroviral treatment (HAART). Alarmingly, the researchers reported that if such incidence was sustained, cumulative prevalence of infection by age 40 would be 40%.6 Using a CDC estimate of 4.0% annual HIV incidence among Black YMSM,7 Stall et al estimated cumulative prevalence of 59.3% by age 40.6
Author Manuscript
More recent HIV incidence studies point to a troubling story for Black YMSM in the U.S. Data published from the 2008 cycle of the National HIV Behavioral Surveillance System (NHBS) estimated an annual HIV incidence rate of 2.9% for all YMSM aged 18–24; however, the annual rate for Black YMSM in the study was 5.1%.8 Koblin and colleagues reported similar findings from HIV Prevention Trials Network (HPTN) Study 061 (i.e., the BROTHERS Study) which enrolled a longitudinal cohort of Black MSM in six US cities. They found an annual HIV incidence of 3.0% for all Black MSM in the cohort, but an incidence of 5.9% for Black MSM under the age of 30.9 Sullivan and colleagues estimated 10.9 new HIV infections per 100 person years among Black MSM aged 18–24 enrolled in an Atlanta cohort study.10 Finally, in a recent study of YMSM, ages 18–19, in New York City (N=594), annual HIV incidence was 2.85 per 100 person years with a 3-year cumulative rate of 7.2% over the entire period.11 An important limitation of these studies and the HIV incidence literature more generally, is that no MSM participants were under the age of 18 at the time of enrollment. Factors associated with HIV incidence among YMSM in the studies cited above include Black or other race (vs. White),8,11 lower level of education (< high school), substance use before or during last sexual episode8 and having sex with an HIV-positive or unknown status partner.9 Koblin and colleagues found that among Black MSM in particular, younger men J Acquir Immune Defic Syndr. Author manuscript; available in PMC 2017 May 01.
Garofalo et al.
Page 3
Author Manuscript Author Manuscript
had higher levels of sexual risk (i.e., more likely to report sex with HIV-positive/unknown status partners vs. older men), were more likely to have a sexually transmitted infection (STI) at follow-up, and were less likely to have a usual place for healthcare or to have visited a health care provider recently,9 thus providing evidence for risk behavior, concomitant STIs, and health care factors as potential reasons for high incidence among younger Black MSM (vs. older). A recent analysis of data from three longitudinal studies of MSM early in the highly active antiretroviral therapy era adds to this evidence finding higher per contact risk of HIV seroconversion (i.e., per sexual act) with HIV seropositive partners in younger MSM (6.1 per 100 person years) for Black men in particular.21 Unfortunately, we were unable to find any studies that specifically estimated STI incidence among YMSM using longitudinal study designs, thus there is a need to estimate both STI and HIV incidence in concert and the predictive potential of STIs on subsequent HIV incidence. The purpose of this analysis is to fill gaps in the existing literature by calculating incidence of new HIV and urogenital gonorrhea/Chlamydia infections in very young MSM age 16–20 at baseline and to describe factors associated with new infections.
Author Manuscript
METHODS Participant Recruitment Data analyzed herein come from a longitudinal study of HIV-risk among 450 YMSM conducted between 2009 and 2015 in Chicago (known as “Crew 450”), the nation’s third largest city and the epicenter of the HIV/AIDS epidemic in the Midwest. The purpose of the study was to characterize the course, and predictors of HIV/STI risk and incident infection among YMSM. We used a modified form of respondent-driven sampling (RDS) to recruit J Acquir Immune Defic Syndr. Author manuscript; available in PMC 2017 May 01.
Garofalo et al.
Page 4
Author Manuscript
YMSM between ages 16 and 20, which yielded a greater proportion of initial recruits or “seeds” than a conventional RDS approach.22 Segmentation in patterns of recruitment by race/ethnicity and a relatively large number of Black seeds also resulted in overrepresentation of youth of color in the sample.22 Seeds were recruited through community-based convenience sampling with study promotional materials distributed via active and passive means in community locations frequented by YMSM. Eligible participants were within the target age-range at baseline, English-speaking, assigned a male sex at birth, had any prior sexual encounter with a male or identified as gay/bisexual, resided in Chicago or suburban Cook County, and were available for multiple follow-ups across 24 months. A total of four study enrollment sites in Chicago were utilized, three sites on the north side of the city and one on the near southwest side. Data Collection and Measures
Author Manuscript Author Manuscript
Following written assent/consent procedures, data were collected via computer-assisted selfinterviewing (CASI) and participants were tested for HIV/STIs; follow-up interview data were collected approximately every 6 months thereafter, with HIV/STI testing completed at 12-month intervals. In order to retain participants over time, multiple attempts to contact them using all available contact information were made, including contacting friends, relatives, or others (whom the participants had indicated would always know how to contact them). Contact information was also updated at all study visits. Commercially available locator services were used to identify new contact information for those for whom all contact information became invalid, however, because of their young age (e.g., not often traceable via utility, mortgage or other billing), these services were not effective. Participants were reimbursed $45 for their time and travel at each visit (except the baseline visit, which was divided into two visits, total compensation was $70 at baseline), and the study received approval from institutional review boards of affiliated institutions, with waiver of parental permission for the participation of minors.
Author Manuscript
In terms of demographic indicators, participant age, race/ethnicity, and highest level of education were captured at the baseline interview as was self-reported HIV testing history (ever tested). Predictor variables were selected from a review of HIV among YMSM.5 Recall of prior six-month substance use and sexual risk were collected at baseline as well as all follow-up points and included: alcohol use, marijuana use, other drug use (i.e., cocaine, heroin, methamphetamines, opiates; non-prescription depressants, stimulants; psychedelics, Ecstasy, gamma hydroxybutyrate –GHB, Ketamine, and any inhalants), alcohol use during sex, drug use during sex, total male partners, unprotected anal sex with a male partner, sex with an HIV positive partner, sex with an unknown status partner, having exchanged sex for money or shelter, having concurrent sexual partners (i.e., either the participant or their most recent sexual partners), victimization by a sex partner (i.e., any affirmative response for any sex partner to the question: “Has [partner] ever hit, slapped, punched or hurt you?”), and having a male partner ≥ 5 years older. We included these last two variables in particular because of the young age of participants and prior work suggesting that developmental vulnerabilities, such as the assumed authority of older partners may put them at risk.23 HIV infection was determined by oral OraQuick/Orasure™ testing for those with unknown status and by self-report for those with known status (self-reported HIV-positive status was
J Acquir Immune Defic Syndr. Author manuscript; available in PMC 2017 May 01.
Garofalo et al.
Page 5
Author Manuscript
confirmed for 71% of self-reported cases via Orasure™, medical records or HIV-related medication prescription verification). Urogenital gonorrhea and Chlamydia infections were determined via urine polymerase chain reaction (PCR; Roche Diagnostics). Statistical Analysis
Author Manuscript
Urogenital gonorrhea and Chlamydia infection were combined and analyzed as a single composite outcome (herein referred to as STI) to improve power and because risk factors for the acquisition of urogenital gonorrhea and Chlamydia are similar. Results and conclusions did not change when the two infections were examined individually (data not shown). Analyses were conducted separately for HIV and STI to identify similarities or dissimilarities between exposures and associated risk of each infection. For STI, person-time was calculated as the time in months from the baseline visit (or the last visit at which the patient tested negative) to the first positive test. Participants with multiple infections were censored at the time of first infection. Loss to follow-up was defined as a case missing at a given time point not due to withdrawal, with no data provided at subsequent study visits. If participants missed a study visit and provided data at subsequent time points, all available data was included in the analysis. Participants who were lost to follow-up were censored at the last time point at which they provided data.
Author Manuscript
For HIV, person-time was calculated as the time from baseline to the last visit at which the patient tested negative or the midpoint of the interval between the first positive test and the preceding negative test for those who tested positive.24 We also calculated person-time using the date of the first positive test rather than the midpoint as the time of HIV infection and results were not substantially changed; presented findings use the midpoint as the time of infection. Cumulative HIV incidence was estimated using the Kaplan-Meier method. Incidence rates of HIV and STI were compared across exposure categories using the logrank test.
Author Manuscript
To assess the effect of fixed and time-varying exposures on HIV and STI, we fit extended Cox regression models with fixed and time-varying covariates to estimate univariable and multivariable hazard ratios for associations of exposures with incident infections. Age at baseline, race/ethnicity, education, ever having been tested for HIV, and infection with gonorrhea or Chlamydia at baseline were treated as time-fixed covariates for analysis. All other variables, including sexual behaviors and substance use, were assessed as timevarying. The timeframe for all exposures was the previous 6 months. The reported exposure at the time of infection was the exposure status associated with infection. For time-varying exposures, participants could contribute to exposed and unexposed risk sets at different time points. Variables with p
