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Which HIV-infected men who have sex with men
in care are engaging in risky sex and acquiring
sexually transmitted infections: findings from a
Boston community health centre

K H Mayer, C O'Cleirigh, M Skeer, et al.
2010 86: 66-70 originally published online August 30, Sex Transm Infect2009doi: 10.1136/sti.2009.036608 Updated information and services can be found at: References
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To order reprints of this article go to: Which HIV-infected men who have sex with men incare are engaging in risky sex and acquiring sexuallytransmitted infections: findings from a Bostoncommunity health centre K H Mayer,1 C O’Cleirigh,2,3 M Skeer,2,4 C Covahey,2 E Leidolf,2 R Vanderwarker,2S A Safren2,3 among HIV-uninfected or unknown status MSM.
Objectives The primary objective was to determine the Syphilis seroreactivity rates are up to four times prevalence of sexually transmitted infections (STI) in greater among HIV-infected MSM than HIV-unin- a cohort of HIV-infected men who have sex with men fected or unknown status MSM.7 This trend of (MSM) in their primary care setting, and to identify the higher comparative rates of incident sexually demographic and behavioural characteristics of those transmitted infection (STI) among HIV-infected infected with STI and the correlates of sexual MSM is also evident in community samples both Methods At study entry, participants (n ¼ 398) were Consistent with high rates of STI among HIV- tested for STI and their medical charts were reviewed for infected MSM, some studies suggest that rates of STI results in the previous year. Data on demographics, high-risk sexual behaviours (ie, anal or vaginal substance use, sexual behaviour and HIV disease intercourse without a condom) may be up to three characteristics were collected through a computer- times higher among HIV-infected MSM compared assisted self-assessment and medical record extraction.
with HIV-uninfected MSM12 13 and higher than Logistic regression analyses assessed characteristics of HIV-infected men who have sex with women.14 those with recent STI and recent transmission risk Among community-recruited samples of HIV- infected MSM, unprotected anal intercourse has Results The sample was predominantly white (74.6%) been significantly associated with substance use and college educated (51.7%). On average, participants were 41.5 years old (SD 8.4) and had been HIV infected dysfunction medications.12 14 15 In addition, sexual for 8.6 years (SD 6.7); 9% of the sample had an STI, with transmission risk behaviour (ie, serodiscordant 6.4% testing positive for syphilis, 3.1% for gonorrhoea unprotected anal intercourse) in MSM has been and 0.25% for chlamydia. Age and years since HIV significantly related to substance use (including diagnosis were significantly associated with testing methamphetamines), non-disclosure of serostatus positive for an STI, as was engaging in transmission risk to all sexual partners and low coping self-efficacy.16 behaviour and using methamphetamine, ketamine and Among those in clinical care, transmission risk inhalants. Substance use, particularly methamphetamine behaviour has been associated with younger age, use, and being more recently diagnosed with HIV were daily alcohol use and not currently taking anti- each uniquely associated with transmission risk behaviour The presence of high rates of STI among HIV- Conclusions These results underscore the need to infected MSM and continuing high rates of sexual develop more effective secondary prevention risk behaviour with serodiscordant sexual part- interventions for HIV-infected MSM, tailored to more ners18 presents an increased risk for the sexual recently diagnosed patients, particularly those who are health of all MSM with HIV, and raises public health concerns for the increased risk of HIVtransmission. The current study supports thepublished research by providing more recent preva-lence data on STI among an urban sample of HIV- The Centers for Disease Control and Prevention has infected MSM living in the northeast. This study documented a dramatic increase in the rates of extends the existing research by relating particular sexually transmitted diseases among men who have demographic, disease and health risk behavioural sex with men (MSM) as evidenced by reports from characteristics to STI likelihood. Therefore, the major urban centres across the country over the purpose of this analysis is to: (1) report on the past 10 years.1e5 In addition, the HIV incidence prevalence of gonorrhoea, chlamydia and syphilis among MSM has been increasing consistently since among a cohort of HIV-infected MSM screened for the early 1990s, and MSM currently represent the participation in an HIV prevention intervention group with the largest number of new HIV infec- who are receiving primary care at Fenway Health; tions (53%) in the USA.6 Based upon national (2) report on the rates of sexual transmission risk surveillance at sexually transmitted disease clinics, behaviour among this group; and (3) identify the median positivity rates for gonorrhoea and chla- significant correlates of STI and sexual transmission mydia are higher among HIV-infected MSM than Sex Transm Infect 2010;86:66e70. doi:10.1136/sti.2009.036608 indicators (binge drinking (ie, consuming five or more alcoholic beverages in a single day at least once), any crystal metham- phetamine use, any use of other specific drugs (ie, marijuana, Participants were 398 HIV-infected MSM screened for partici- crack, cocaine, heroin, ketamine, opiates, tranquilizers or barbi- pation in an HIV prevention intervention trial through Fenway turates, hallucinogens, or inhalants) and a composite of other Health, the largest ambulatory facility caring for MSM in New England, and tested for STI at study entry, or a chart review Mental health indicators were assessed through various indicated that they had received STI testing in the year before psychosocial batteries in the audio computer-assisted self-inter- study assessment. Men who met the inclusion criteria for the view. Depression was defined as screening positive for either prevention intervention trial were: (1) infected with HIV; (2) major depressive syndrome or other depressive syndrome within received primary HIV care at Fenway Health; (3) were 18 years the past 2 weeks, as measured by the nine-item depression of age or older; and (4) self-identified as MSM. This study severity scale of the patient health questionnaire (PHQ).19 In utilised cross-sectional, baseline measures from the prevention addition, patients were considered to have an anxiety disorder if they met screen-in criteria for any of the following disorders:panic disorder, as measured by the panic disorder severity scale of the PHQ,19 other anxious syndrome, as assessed by the PHQ,19 Participant recruitment for the 12-month study began in July social phobia, as captured by the MINI-SPAN,20 and post- 2004 and participant follow-up continued to August 2008. To traumatic stress disorder, as measured by the four-item SPAN.21 assess diagnoses of STI, participants were tested for syphilis,gonorrhoea and chlamydia. Syphilis screening of blood samples utilised the rapid plasma reagin method and reactive serologies Analyses were conducted using SPSS and SAS statistical soft- had confirmatory fluorescent treponemal antibody absorption ware packages. Descriptive statistics were assessed for all vari- performed. Specimen collection to detect gonococcal and chla- ables. Bivariate logistic regression analyses were conducted to mydia urethritis was performed using urine samples via nucleic assess the relationship between the outcome (STI) and each acid amplification testing. The prevalence of rectal and independent variable. Because most of the variation in STI can pharyngeal gonorrhoea and chlamydia was extracted from the be accounted for by transmission risk behaviour (as the participants’ medical records. Testing methodology before predominant method for contracting syphilis, gonorrhoea and August 2006 utilised PCR technology. Subsequent to August chlamydia among MSM is through unprotected anal inter- 2006, the amplification method used was changed to strand course), we conducted a second set of bivariate logistic regres- displacement amplification, as a result of changes in available sion models examining the effect of the independent variables assays at the testing laboratory (Quest).
(excluding sexual risk behaviour) on the dichotomous trans- CD4 cell count and plasma HIV-RNA were routinely mission risk behaviour outcome. Due to the overlap in variation measured at least quarterly as part of ongoing primary care.
with the independent variables and the outcomes, and the With permission from the participants, the results of these redundancy of running multivariable models with both biological measures were captured from the lab server (Quest) or outcomes (STI and transmission risk behaviour), we a priori via hard copy report, and translated or entered into an electronic chose only to present the multivariable model of the intervening medical record system (Logician/Centricity EMR), followed by outcome (transmission risk behaviour). As such, variables that extraction into a Microsoft Access database.
were statistically significant (p<0.05) in the second set ofbivariate analyses were retained in a multivariable logistic regression analysis, which controlled for race/ethnicity and Behavioural data were collected via surveys administered education, regardless of significance level. Furthermore, in the through the audio computer-assisted self-interview system that case in which two significant variables were highly correlated, we were given during the screen-in process for participation in the chose to include only one in the final model to eliminate the prevention intervention study. The survey lasted for approxi- threat of multicollinearity posed by putting highly correlated mately one hour and included the measures below.
variables in the same multivariable model. In that regard,although multiple drugs were examined individually in the bivariate models, in the multivariable model, we only included The primary dependent variable was a dichotomous indicator of a dichotomous composite measure of any drug use (excluding having been diagnosed with a bacterial STI (syphilis, gonorrhoea methamphetamine) and crystal methamphetamine use.
or chlamydia) within the past year. The primary independentvariable was transmission risk behaviour, operationalised as whether or not participants had unprotected insertive or receptive anal sex with possible serodiscordant (HIV-negative or The sample characteristics are presented in table 1.
unknown status) partners within the past 6 months. Further- Less than 10% of the sample had been diagnosed with an STI more, we examined the unprotected insertive and receptive anal within the past year, and among those who had (n ¼ 36), 69.4% sex components of transmission risk behaviour as separate had been diagnosed with syphilis, 33.3% with gonorrhoea and independent variables. Additional independent variables of 2.8% with chlamydia. Of the gonorrhoea and chlamydia diag- interest included demographics (age, race/ethnicity, education noses (n ¼ 13), 61.5% were from a urethral source, 30.8% were and annual income), HIV disease status and treatment (number rectal and 7.7% were pharyngeal. Of the nine participants whose of years since being diagnosed with HIV, CD4 cell count, STI was diagnosed as part of their primary care, five were tested undetectable viral load (less than 75 copes/ml) and currently in response to clinical symptom presentation and four of those being on antiretroviral medications), mental health indicators tested were asymptomatic but reported possible exposure.
(posttraumatic stress disorder symptoms, depression and The mean age of the participants was 41.5 years (SD 8.4), anxiety) and past 3-month dichotomous substance use 43.3% of the participants had an annual income greater than US Sex Transm Infect 2010;86:66e70. doi:10.1136/sti.2009.036608 Type of STI (among those with an STIdiagnosis) GED, General Educational Development; STI, sexually transmitted infection.
$40 000, and the sample was largely white (74.6%) and college 1.78 to 8.28); age (standardised) (OR 0.63, 95% CI 0.44 to 0.91); educated (51.7%). On average, participants had been diagnosed number of years since HIV diagnosis (standardised) (OR 0.66, with HIV for 8.6 years (SD 6.7), had a CD4 cell count of 523.1 95% CI 0.45 to 0.97); and crystal methamphetamine (OR 3.37, cells/mm3 (SD 299.3) and had a mean plasma HIV-RNA of 14 95% CI 1.67 to 6.81), ketamine (OR 4.48, 95% CI 1.83 to 11.00) 777 copies/ml (SD 46 332). Approximately half (54.5%) of the and inhalant use (OR 2.60, 95% CI 1.28 to 5.30).
sample had an undetectable viral load and 66.1% were taking Similarly, in the additional bivariate analyses, age (OR 0.76, anti-HIV medication at the time of the survey. Within the 3 95% CI 0.62 to 0.94), number of years since HIV diagnosis (OR months before the survey, 19.3% of the sample reported binge 0.57, 95% CI 0.46 to 0.70), crystal methamphetamine use (OR drinking, 22.9% reported using crystal methamphetamine and 4.25, 95% CI 2.45 to 7.38), ketamine use (OR 7.66, 95% CI 2.62 to 56.8% reported using other drugs. Approximately half (50.5%) of 22.34) and inhalant use (OR 4.22, 95% CI 2.62 to 6.78) were all the sample reported engaging in transmission risk behaviour significantly associated with transmission risk behaviour at baseline (table 2). Additional significant independent variablesincluded: use of marijuana (OR 1.86, 95% CI 1.21 to 2.84), tranquilizers or barbiturates (OR 2.00, 95% CI 1.03 to 3.89), The bivariate logistic regression analyses that examined the hallucinogens (OR 4.07, 95% CI 1.81 to 9.16), viagra (OR 3.64, effect of the independent variables on STI demonstrated that of 95% CI 2.09 to 6.36); a composite measure of other drug use (OR all of the demographic, sexual risk, HIV, mental health and 3.18, 95% CI 2.08 to 4.85) and having a detectable viral load (OR substance use indicators, the following variables were statisti- cally significantly associated with having been diagnosed with Due to the high correlation between age and years since HIV an STI within the past year: transmission risk behaviour (odds diagnosis (r ¼ 0.44; p<0.001), only the number of years since HIV ratio (OR) 4.41, 95% CI 1.88 to 10.36); unprotected sero- diagnosis was included in the multivariable model, as the focus of discordant insertive anal sex (OR 2.11, 95% CI 1.04 to 4.30); this study was the HIV-related correlates of transmission risk unprotected serodiscordant receptive anal sex (OR 3.86, 95% CI behaviour. In the final multivariable model, years since HIV Sex Transm Infect 2010;86:66e70. doi:10.1136/sti.2009.036608 Results from the bivariate and multivariable logistic regression analyses with the outcome of transmission *The multivariable model adjusted for race/ethnicity and education. OR, odds ratio.
diagnosis, drug use and crystal methamphetamine use all iour in other metropolitan centres throughout the USA (ie, remained significant (table 2). These results indicated that each Chicago, Los Angeles, New York, San Francisco).12 14e16 26 additional year since HIV diagnosis was associated with The increased incidence of syphilis in this cohort may be a reduced odds (OR 0.60, 95% CI 0.48 to 0.76) of transmission reflective of serosorting, when men may selectively disclose their risk behaviour, and that men who reported using crystal meth- HIV status and/or have unprotected sex with more HIV-infected amphetamine within the past 3 months (OR 2.57, 95% CI 1.37 partners in order to be able to have unprotected anal sex without to 4.82) or men who reported using any recreational drugs within the concern of transmitting to others, which could concentrate the past 3 months (OR 2.17, 95% CI 1.32 to 3.58) had a greater the syphilis epidemic among HIV-infected MSM. The increased odds of transmission risk behaviour. Having a detectable viral incidence of syphilis in the current sample may also represent load was no longer statistically significant in the multivariable the fact that HIV-infected MSM may be more susceptible to model, which was due, at least partly, to the significant correla- contracting syphilis compared with their uninfected counter- tions (p<0.01) between this variable and other variables in the parts.27 Furthermore, a recent review of secular trends of STI at model, including crystal methamphetamine use and the number Fenway Health over the past decade documents that syphilis has been increasing, revealing that approximately half of the newcases of syphilis at the health centre are among HIV-infected MSM, even though these men represent less than 20% of the full The results of this study indicate that 9.0% of HIV-infected MSM population getting primary care at Fenway Health.28 MSM in care in a Boston community health centre had been These results are most appropriately interpreted with diagnosed with at least one STI during a one-year period, with a consideration of the limitations of this study. These analyses reactive syphilis tests accounting the majority of cases. The are presented within a cross-sectional design and as such neither presence of STI can compromise the health of people living with causal relationships nor the directionality of the relationship can HIV through several mechanisms, including increasing suscep- be inferred. Several of the measures were based upon patient tibility to reinfection and superinfection by disrupting mucosal self-report and are vulnerable to the biases of that methodology.
barriers to infection or by increasing the presence of HIV- In addition, information concerning the prevalence of STI susceptible inflammatory cells in the genital tract.22 In addition, reported here was obtained from both study-related procedures several recent reports have documented significant acute at study entry and through STI assays conducted through decreases in CD4 cell counts and acute increases in HIV viral clinical care, which may contribute to bias in estimating stable RNA in response to syphilis infection,23e25 which could STI rates in this sample. Finally, the sample only included men compromise effective antiretroviral therapy. Moreover, the pres- who received primary care, specifically at Fenway Health, and ence of STI among HIV-infected MSM already in care provides was mostly white (75%), which limits the generalisability of the convincing evidence of ongoing risky sexual behaviour in this findings. However, because Massachusetts provides universal group, creating risks for HIV transmission to uninfected sexual access to health care and there is state support to supplement partners, because STI may increase HIV infectiousness by facili- Ryan White (federal aid) programmes, there is no reason to tating HIV shedding in the genital tract or the rectal mucosa.22 expect that HIV-infected MSM clients receiving care at Fenway The results of the current study also identified that HIV- Health would differ radically from other HIV-infected MSM in infected MSM who were younger or more recently diagnosed care in other HIV specialty clinics in the Boston area. However, as with HIV, or who reported methamphetamine, ketamine, or Fenway Health is known for providing comprehensive services to inhalant use in the past 3 months or unprotected anal inter- the region’s gay and lesbian communities, it is possible that some course in the past 6 months, were significantly more likely to potential clients who want less public awareness of their sexual have had a new bacterial STI result in the past year. Slightly orientation and/or HIV status could seek care elsewhere, so that more than half the sample reported one or more episode of the cohort in this study might be riskier than men receiving care unprotected anal intercourse with a serodiscordant partner in at other centres, but rigorous comparative data are not available.
the past 6 months, tended to be more recently diagnosed with Participants in this study had to have an established relationship HIV, and were more likely to have used methamphetamine or with the healthcare centre and sign an informed consent, so some other recreational drugs in the previous 3 months. These results individuals with more serious mental health concerns and/or from this Boston cohort are consistent with the characteristics unstable housing, who might also be riskier sexually, might not of HIV-infected MSM who engage in transmission risk behav- Sex Transm Infect 2010;86:66e70. doi:10.1136/sti.2009.036608 Centers for Disease Control and Prevention. Primary and secondary syphilisamong men who have sex with mendNew York City, 2001. MMWR Morb Mortal Centers for Disease Control and Prevention. Outbreak of syphilis among menwho have sex with mendSouthern California, 2000. MMWR Morb Mortal Wkly Rep < STI rates among HIV-infected MSM are high, as are rates of Centers for Disease Control and Prevention. Primary and secondary < This study demonstrates that younger age, fewer years since syphilisdUnited States, 2003e2004. MMWR Morb Mortal Wkly Rep2006;55:269e73.
HIV diagnosis and drug use are associated with developing Heffelfinger JD, Swint EB, Berman SM, et al. Trends in primary and secondary incident STI, and with engaging in transmission risk behaviour.
syphilis among men who have sex with men in the United States. Am J Public Health < Innovative secondary prevention interventions for HIV-infected Centers for Disease Control and Prevention (CDC). Fact sheet: estimates of new MSM, particularly those who are younger and substance HIV infections in the United States, August 2008. http://www.cdc.gov/hiv/topics/ users, may help to decrease risk taking in this subpopulation.
surveillance/resources/factsheets/pdf/incidence.pdf (accessed 7 July 2009).
Centers for Disease Control and Prevention (CDC). Men who have sex withmendSTD surveillance 2006. http://www.cdc.gov/STD/stats06/msm.htm (accessed The high rates of HIV and STI transmission risk behaviour reported among HIV-infected Boston MSM suggest that the Whittington WL, Collis T, Dithmer-Schreck D, et al. Sexually transmitted diseases development of effective secondary HIV prevention intervention and human immunodeficiency virus-discordant partnerships among men who havesex with men. Clin Infect Dis 2002;35:1010 programmes should be a public health priority. These results also Dodds JP. A tale of three cities: persisting high HIV prevalence, risk behaviour and suggest that these programmes could be maximally effective if undiagnosed infection in community samples of men who have sex with men. Sex they focus on younger or more recently diagnosed MSM, who Fengyi J. High rates of sexually transmitted infections in HIV positive homosexual may not have had sufficient provider contact to receive intensive men: data from two community based cohorts. Sex Transm Infect 2007;83:397e9.
prevention counselling. Given the high rate of co-infectiousness Dougan S, Evans BG, Elford J. Sexually transmitted infections in Western Europe among these HIV-infected MSM, it may be particularly impor- among HIV-positive men who have sex with men. Sex Transm Dis 2007;34:783e90.
tant for prevention efforts to be integrated into primary care as Carey JW, Mejia R, Bingham T, et al. Drug use, high risk sexual behavior, andincreased risk for recent HIV infection among men who have sex with men in Chicago a key syndemic approach to improving the sexual health of and Los Angeles. AIDS Behav. Published Online First: 23 May 2008. doi:10.1007/ young, recently diagnosed HIV-positive MSM or those with drug use issues. Furthermore, the high prevalence of co-infec- Brewer DD, Golden MR, Handsfield HH. Unsafe sexual behavior and correlates of riskin a probablility sample of men who have sex with men in the era of highly active tions in this population may have implications for biomedical antiretroviral therapy. Sex Transm Dis 2006;33:250e5.
approaches to HIV prevention, including incorporating pre- Morin SF, Myers JJ, Shade SB, et al. Predicting HIV transmission risk among HIV- exposure prophylaxis and “test and treat” strategies in prevention infected patients seen in clinical settings. AIDS Behav 2007;11(5 Suppl):6e16.
efforts. Further longitudinal research with biomedical approaches Spindler HS, Scheer S, Chen SY, et al. Viagra, methamphetamine, and HIV risk:results from a probability sample of MSM, SanFrancisco. Sex Transm Dis would be well suited to examine these relationships further.
Innovative programmes that facilitate education and skills Morin SF, Steward WT, Charlebois ED, et al. Predicting HIV transmission risk among building around safer sex when MSM are relatively recently HIV-infected men who have sex with men: findings from the healthy living project. JAcquir Immune Defic Syndr 2005;40:226 diagnosed and entering care may help to decrease risk taking in Drumright LN, Little SJ, Strathdee SA, et al. Unprotected anal intercourse and this subpopulation. Effective care programmes may also enhance substance use among men who have sex with men with recent HIV infection. J Acquir HIV prevention by providing substance use screening, treatment Fenton KA, Imrie J. Increasing rates of sexually transmitted diseases in homosexual and/or referral options for HIV-infected MSM in care. Similarly, men in Western Europe and the United States: why? Infect Dis Clin North Am effective prevention for positive programmes and access to treatment for concomitant STI will address the dual priorities of Spitzer RL, Korenke K, Williams JBW, for the Patient Health Questionnaire Primary reducing transmission of HIV and other STI and will improve Care Study Group. Validation and utility of a self-report version of PRIME-MD: the PHQPrimary Care Study. JAMA 1999;282:1737 the sexual health and HIV disease management among those Connor KM, Kobak KA, Churchill LE, et al. Mini-SPIN: a brief screening assessment for generalized social anxiety disorder. Depress Anxiety 2001;14:137e40.
Meltzer-Brody S, Churchill E, Davidson JR. Derivation of the SPAN, a brief diagnostic Contributors KHM is the principal investigator of the study, conceptualised the screening test for post-traumatic stress disorder. Psychiatry Res 1999;88:63e70.
manuscript and led the manuscript writing. CO and MS conducted the statistical Fleming DT, Wasserheit JN. From epidemiological synergy to public health policy and analyses and contributed to the preparation of the manuscript. CC, EL and RV consulted practice: the contribution of other sexually transmitted diseases to sexual on the project and contributed to the preparation of the manuscript. SAS is the transmission of HIV infection. Sex Transm Infect 1999;75:3e17.
co-principal investigator of the study and contributed to the development of the ´nez-On˜ate F, Aguilar M, et al. Impact of syphilis infection on HIV viral assessments used in the study and the preparation of the manuscript.
load and CD4 cell counts in HIV-infected patients. J Acquir Immune Defic Syndr2007;44:356 Funding This study was supported by NIMH grant 5R01MH068746-05 and HRSA Buchacz K, Patel P, Taylor M, et al. Syphilis increases HIV viral load and decreases grant H97HA01293 awarded to KHM and SAS.
CD4 cell counts in HIV-infected patients with new syphilis infections. AIDS Kofoed K, Gerstoft J, Mathiesen LR, et al. Syphilis and human immunodeficiency virus Ethics approval Ethics approval was obtained from Fenway Health, Boston, MA.
(HIV)-1 coinfection: influence on CD4 T-cell count, HIV-1 viral load, and treatmentresponse. Sex Transm Dis 2006;33:143 Ostrow DG, Plankey MW, Cox C, et al. Specific sex drug combinations contribute to Provenance and peer review Not commissioned; externally peer reviewed.
the majority of recent HIV seroconversions among MSM in the MACS. J AcquirImmune Defic Syndr 2009;51:349e55.
Cohen MS. When people with HIV get syphilis: triple jeopardy. Sex Transm Dis Centers for Disease Control and Prevention. Trends in primary and secondary Mimiaga MJ, Helms DJ, Reisner SL, et al. Gonococcal, chlamydia, and syphilis syphilis and HIV infections in men who have sex with men infection positivity among MSM attending a large primary care clinic, Boston, 2003 to e2002. MMWR Morb Mortal Wkly Rep 2004;53:575e8.
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