Soon after the onset of the AIDS epidemic in the early 1980s, sexually transmitted disease (STD) prevalence among men who have sex with men (MSM) declined; however, in the past decade, increases in syphilis and rectal gonorrhea have been reported among MSM in the United States,1–8 including Massachusetts MSM.9 Most published information on STDs among MSM is from patients evaluated at public STD clinics. Limited data are available on MSM who receive their healthcare from primary care or general medical clinics.
Founded in 1971, Fenway Community Health (FCH) in Boston, MA provides comprehensive care for one of the largest groups of gay and bisexual persons in the Northeast United States and is 1 of the 7 lesbian, gay, bisexual, and transgender-focused community health centers in the United States.10 In 2000, FCH reported 50,850 visits by 8361 individuals, including more than 1000 individuals receiving HIV-associated care which increased in 2007 to 71,348 visits by 10,387 individuals including more than 1200 individuals receiving HIV-associated care. FCH provides a diverse array of clinical services including, but not limited to, comprehensive primary medical care and specialty services, mental health and addiction services, preventive care and health promotion, community education and outreach programs, family and parenting services, and HIV/STD counseling and testing. FCH is currently the largest provider of care for MSM in New England. From January 2003 through December 2004, there were 21,927 MSM visits reported at FCH.
The objectives of this analysis were: (1) to evaluate patterns of gonorrhea (urethral, rectal, and pharyngeal), chlamydia, and syphilis screening and prevalence in all MSM at FCH; (2) to evaluate STD screening and prevalence in asymptomatic MSM at FCH; and (3) to compare gonorrhea and chlamydia prevalence and syphilis seroreactivity between HIV-infected and HIV-uninfected MSM seen in a large primary care clinic setting.
MATERIALS AND METHODS
Participants and Procedures
Most national notifiable STD surveillance data reported to Centers for Disease Control and Prevention (CDC) do not include information regarding sexual behaviors,9 so national trends about STDs among MSM in the United States were not available. In order to address the lack of information about STDs among MSM, the CDC MSM Prevalence Monitoring Project was established in 1999 to: (1) assess the prevalence of, and trends in, STDs, HIV, and sexual risk behaviors among MSM and (2) support the use of this information to enhance STD and HIV prevention and control efforts in MSM. Established by the CDC in collaboration with state and local health departments and community clinics, the MSM Prevalence Monitoring Project obtained data during routine clinical care according to clinician discretion and local clinic protocols.
As part of the MSM Prevalence Monitoring Project, FCH collected and analyzed all chlamydia, gonorrhea, syphilis, and HIV test results performed between January 1, 2003 through December 31, 2004 among MSM aged 15 to 65 years. Using medical chart abstraction, male patients were identified as MSM for this analysis if any of the following conditions were met: (1) the patient self-reported as gay or bisexual during registration, (2) the patient was tested for a rectal STD, or (3) the clinician documented that the patient was gay/bisexual or that the patient had a male sex partner(s).
Depending upon test availability, test types used for each STD were the following: (1) urethral gonorrhea: urethral swab for culture or nucleic acid amplification tests, or nucleic acid probe of urine specimen; (2) rectal and pharyngeal gonorrhea: swab for culture; chlamydia: nucleic acid amplification tests or nucleic acid probes on urine (no routine rectal or pharyngeal testing for chlamydia was performed); (3) syphilis: rapid plasma reagin test, with positive tests confirmed by the microhemagglutination assay.
Data Analysis
STD positivity was calculated as the number of positive (or reactive) test results divided by the total number of positive and negative test results among MSM. Indeterminate, inadequate, and contaminated test results were excluded. Gonorrhea and chlamydia positivity and syphilis seroreactivity were calculated by age, race/ethnicity, and HIV status among MSM.
STD positivity was compared between HIV-infected patients and HIV-uninfected or patients with unknown HIV status. For comparison of STD positivity by HIV status, HIV-infected MSM were identified as those with documentation of a positive HIV antibody test at FCH or another clinic on or before the clinic visit date of interest, a self-reported history of HIV infection, or documentation of acute HIV infection (positive HIV RNA plasma viral load test with a negative antibody test) on or before the clinic visit date of interest. χ2 tests of independence were used for comparisons, and odds ratios and corresponding 95% confidence intervals were calculated. Symptom status was determined for MSM who were tested for an STD (gonorrhea, chlamydia, or syphilis). MSM were symptomatic if the provider documented that the patient was tested because of symptoms related to infection (e.g., discharge, pain on urination, sore on penis, etc.); patients were not classified as symptomatic if their symptoms did not correspond to an STD for which they tested positive. To address patterns of screening for STDs among MSM, positivity was calculated for asymptomatic MSM by the documented reason for testing, which included one of the following: (1) sexual partner diagnosed with gonorrhea, chlamydia, or syphilis (partner contact, which included patients who were told of possible exposure via third-party partner notification); (2) patient requested because of perceived “high risk” sex (i.e., sex without a condom, condom breakage, anonymous sex) in the prior 3 months; or (3) routine screening (e.g., complete physical exam, HIV follow-up appointment, entering a new relationship, or patient preference for regular screening). Reason for testing was documented by the clinician at time of testing.
RESULTS
Demographics and STD Prevalence
During 2003 to 2004, there were 21,927 visits by MSM at FCH, which accounted for over half of all visits to the health center. The majority of visits (84%) were by non-Hispanic white men, 5% were by non-Hispanic black/black males, and 5% were by Hispanic males (Table 1 ). The median age of MSM visiting FCH during this time was 39 years (range: 18–65 years).
TABLE 1: Demographics, Testing, and Gonorrhea and Chlamydia Positivity and Syphilis Seroreactivity Among MSM, Fenway Community Health, Boston, Massachusetts, 2003 to 2004
Testing for at least 1 STD was conducted during 23.4% (n = 5121) of the visits, and at 11.4% (n = 582) of these visits, there was at least 1 positive STD test result. MSM who tested for at least 1 STD had the same demographic distribution as MSM not tested for an STD. Of the 21,927 MSM visits, 6.1% included testing for urethral gonorrhea, 7.3% for pharyngeal gonorrhea, 3.4% for rectal gonorrhea, 5.8% for urethral Chlamydia, and 19.6% for syphilis (Table 1 ).
Test positivity for urethral gonorrhea was 13.4%, rectal gonorrhea 8.8%, and pharyngeal gonorrhea 1.9%. Urethral chlamydia positivity was 5.7% and syphilis seroreactivity was 6.2% (Table 1 ). Men aged 55 years and older were less likely to test positive for gonorrhea (all anatomical sites) or syphilis than men younger than 55 years; however, chlamydia positivity was comparable across age groups. There were no significant differences observed across race/ethnicity groups for all STDs.
Approximately, 40% of MSM visits were from men known to be infected with HIV (Table 1 ). Urethral gonorrhea was the most common diagnosis with 12.8% in HIV-uninfected MSM and 16.7% in HIV-infected MSM. Urethral, rectal, and pharyngeal gonorrhea, and urethral chlamydial positivity, were comparable between HIV-infected and HIV-uninfected MSM. However, HIV-infected MSM were more likely to have a seroreactive syphilis test result than HIV-uninfected men (12.6% vs. 3.5%, respectively; P < 0.0001).
Proportion of Symptomatic and Asymptomatic MSM Positive for At Least 1 STD
Among those tested for an STD, 65% of the MSM visits to FCH were from MSM, who were asymptomatic at time of testing (Table 2 ). MSM who had STD symptoms were more likely to test positive for an STD than MSM who did not have STD symptoms (OR = 3.3; 95% CI: 2.8–4.0). Among all asymptomatic MSM tested, 1.0% had urethral gonorrhea; 1.7% had pharyngeal gonorrhea; 5.6% had rectal gonorrhea; 2.3% had urethral chlamydia; and 4.6% were seroreactive for syphilis. HIV-infected MSM diagnosed with one of these STDs were more likely to be asymptomatic than HIV-uninfected MSM (OR = 2.1; 95% CI: 1.8–2.4).
TABLE 2: Proportion of Symptomatic and Asymptomatic MSM Positive for at Least One STD, Fenway Community Health, Boston, Massachusetts, 2003 to 2004
Gonorrhea and Chlamydia Positivity and Syphilis Seroreactivity by Reason for Testing
STD positivity varied by reason for testing among asymptomatic MSM: 16.5% for patients exposed to an STD, 7.4% for patients reporting “high risk” sex, and 4.4% for patients routinely screened. Among asymptomatic MSM exposed to an STD who were tested, urethral gonorrhea positivity was 1.9%, rectal gonorrhea positivity was 19.7%, syphilis seroreactivity was 9.3%, pharyngeal gonorrhea positivity was 5.1%, and urethral chlamydia positivity was 3.9% (Table 3 ).
TABLE 3: Gonorrhea and Chlamydia Positivity and Syphilis Seroreactivity by Reason for Testing Among Asymptomatic MSM, Fenway Community Health, Boston, Massachusetts, 2003 to 2004
DISCUSSION
Urethral gonorrhea positivity was high among all MSM, and rectal gonorrhea and syphilis were frequently detected among asymptomatic MSM at FCH in Boston, MA during 2003 to 2004, raising concerns about continued growth of the STD and HIV epidemics in this population. As documented in previous studies,9,11 HIV-infected MSM in the current sample more often had an asymptomatic STD and had a greater STD burden than HIV-uninfected MSM. HIV-infected Boston area MSM were at especially high risk for urethral gonorrhea and syphilis, at 16.7% and 12.6% positivity, respectively. The positivity was comparable to 2006 CDC MSM Prevalence Monitoring Project data from 5 public STD clinics (Denver, New York, Philadelphia, San Francisco, and Seattle) and 3 community-based, gay men’s health clinics (Chicago, the District of Columbia, and Houston) where urethral gonorrhea positivity was 14% (range: 12%–31%) in HIV-infected MSM.9 In addition to increasing susceptibility to HIV reinfection, STDs are markers for high risk sexual practices through which HIV infection can be transmitted.3,12 The observed high positivity of STDs in this sample suggest the need for renewed HIV prevention efforts, among both HIV-infected and HIV-uninfected or unknown MSM.
Although fewer tests for gonorrhea were conducted than for syphilis among MSM patients at FCH, a higher gonorrhea positivity was observed than seroreactivity for syphilis among this population. This is particularly concerning given that antimicrobial resistance remains an important consideration in the treatment of gonorrhea, particularly among MSM.9,13 Given the high prevalence of asymptomatic disease14,15 and increased risk of HIV transmission associated with STDs,16,17 results show that screening for rectal gonorrhea should be prioritized among MSM. Interestingly, although positivity of gonorrhea among MSM in Boston, MA are comparable to the prevalence observed among MSM in other US cities, pharyngeal gonorrhea positivity was low (1.7%) in this sample compared to other US cities.9
Test positivity varied by reason for STD testing, with MSM who were tested due to high risk sex in the past 3 months or exposure to an STD being more frequently diagnosed with a new STD than those presenting for routine screening. Developing a set of questions to screen for the extent of sexual risk behaviors (emphasizing collection of data on various sexual behaviors, including unprotected anal and oral sex, number of times in a given period, and anonymous encounters) may assist busy clinicians in more effectively and efficiently screening MSM at highest risk (e.g., MSM with high risk sexual history in the preceding 3 months, or exposure to STDs).
There are limitations to consider when interpreting findings. First, symptom status was only determined for patients who were screened for an STD. We could not determine if some symptomatic patients were empirically treated without testing. Ideally, everyone with an STD symptom would be screened for an STD, but this could not be ascertained with the current data collection instruments. Second, although only 5% of the MSM in the FCH population did not indicate their race, this “unknown” race group had the highest screening rates for each specific infection. Third, because testing occurred over a 2-year period, it is likely that there were repeated tests for the same individual at separate occasions and we did not restrict unique patient testing in the analysis (i.e., the same person could be represented in the analysis more than one time). Finally, we did not collect data on whether syphilis seroreactivity were new diagnoses of early syphilis, how many had latent syphilis, and how many had previously treated syphilis.
Our findings suggest that a high percentage of asymptomatic MSM were screened during the reporting period, revealing a substantial STD burden that might not otherwise have been diagnosed and treated. With the frequent detection of STDs among MSM, with and without symptoms, particularly among HIV-infected MSM and those engaging in risky sexual practices, CDC guidelines for routine STD screening of MSM are clearly justified.13 These data are critical for the design of effective public health interventions for this at risk population.
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