Mimiaga, Matthew J. ScD, MPH*†; Mayer, Kenneth H. MD*‡;; Reisner, Sari L. MA*; Gonzalez, Alex MD, MPH*; Dumas, Bill RN§; Vanderwarker, Rodney BA*; Novak, David S. MSW§; Bertrand, Thomas MPH§
From the *The Fenway Institute, Fenway Community Health, Boston, Massachusetts; † Harvard Medical School/Massachusetts General Hospital, Boston, Massachusetts; ‡ Brown Medical School/Miriam Hospital, Providence, Rhode Island; § The Massachusetts Department of Public Health, Boston, Massachusetts
The authors thank the Medical Department of Fenway Community Health for their diligent assistance with participant recruitment, and the much missed Dr. Sylvie Ratelle for her oversight and expertise with protocol development.
Correspondence: Matthew J. Mimiaga, The Fenway Institute, Research and Evaluation Department, Fenway Community Health, Prudential Tower, 4th floor, 800 Boylston Street, Boston, MA 02119. E-mail: email@example.com.
Received for publication August 30, 2007, and accepted November 26, 2007.
Background: The purpose of this project was to determine the prevalence of asymptomatic sexually transmitted diseases (STDs) among men who have sex with men (MSM) in the Boston area who had been sexually active (oral and/or anal sex) with another male within the past year.
Methods: Over a 1-month period (March 2007), asymptomatic MSM in care at a Boston community health center (n = 114) were screened for gonorrhea and chlamydia using the BD ProbeTec technique. Deidentified medical record data were analyzed and linked to prevalence monitoring results.
Results: Eleven percent of the sample tested positive for one of the 2 STDs (gonorrhea or chlamydia) from at least one mucosal site. Individuals who were infected with an STD were considerably more likely to have a prior history of one or more STD infections when compared with those without an STD history (OR = 3.69; P <0.02). There were no significant differences observed in psychosocial and other behavioral risk factors between patients with or without an STD.
Conclusions: Screening asymptomatic MSM using nucleic acid amplification tests (NAATs) revealed a substantial STD burden that might not have been diagnosed using traditional assays. These data are critical for the design of effective public health interventions for this population.
MEN WHO HAVE SEX with men (MSM) continue to be at increased risk for HIV infection and other viral and bacterial sexually transmitted diseases (STDs).1 In Massachusetts, MSM accounted for approximately 40% of all recently diagnosed HIV/AIDS infections and HIV incidence among Massachusetts MSM increased from 292 in 2004 to 315 in 2005.2 In many US cities, including Boston, increased rates of chlamydia, gonorrhea, and syphilis have been reported, especially among HIV-infected MSM.3 The chlamydia infection rate in US men increased by 43.5% (from 112.3 to 161.1 cases per 100,000 men) from 2001 through 20051; this amplified rate of infection might be attributed to increased screening among men over the past several years. Between 2001 and 2005, there was a greater than 3-fold increase in infectious syphilis cases among Massachusetts MSM and a 33-fold increase in diagnosed cases of quinolone-resistant gonorrhea (QRNG) among MSM (2 cases in 2001; 66 cases in 2005).2
Research exploring perceptions of barriers and facilitators to STD screening among MSM in the Boston area has shown that MSM are most likely to be screened for STDs if they are symptomatic or are told by a partner of a recent exposure, and least likely to be screened if they do not consider themselves to be at risk, lack access to free and anonymous testing, or are not experiencing symptoms.4 The implication that MSM tend to seek STD screening only after they have active symptoms raises concerns for public health practice.
The most recent and highly sensitive STD testing technology, nucleic acid amplification tests (NAATs), is a molecular-based assay which allows minimal quantities of a target nucleic acid to be detected and amplified from clinical specimens.5 NAATs have several unique advantages, chief among which is its increased sensitivity and detection of asymptomatic STDs, such as gonorrhea and chlamydia, when compared with culture specimens.6,7 Yet whereas culture and isolation of the organism in traditional STD testing yields 100% specificity, NAATs increased sensitivity compromises its specificity (>99.0%), which can result in false-positive test results.8 Specificity can be improved by additional testing with an alternative assay or by testing a second specimen, and is recommended.5,9
The primary purpose of this project was to determine the prevalence of asymptomatic STDs among MSM in the Boston area who had been sexually active (oral and/or anal sex) with another male within the past year. Consistent with research showing a strong association between psychosocial risk factors and STD/HIV risk among MSM,10–13 a secondary aim was to assess the psychosocial risk factors associated with STD history and diagnosis. Finally, this project sought to evaluate the effectiveness of nucleic amplification testing in a front-line community health care setting. Given that STDs facilitate HIV acquisition and transmission and serve as markers of behavioral risk,14,15 local prevalence data on asymptomatic STDs can provide critical information about the local epidemiology of HIV infection and potential innovative public health screening programs utilizing new technologies.
Materials and Methods
Design, Recruitment, and Procedures
Over a 1-month period (March 2007), Fenway Community Health (FHC),16 the largest freestanding community healthcare and research facility specializing in HIV/AIDS care and serving the needs of the lesbian, gay, bisexual, and transgender community in the greater Boston area, conducted a surveillance project in partnership with the Massachusetts Department of Public Health, STD Division, to monitor the prevalence of asymptomatic STDs among MSM health center patients (n = 114). All male patients who came to FHC for a medical visit and had been sexually active (oral and/or anal sex) with another man in the past year were offered STD screening using BD ProbeTec ET Chlamydia trachomatis and Neisseria gonorrhoeae Amplified DNA Assays (BD ProbeTec). To assess performance characteristics of NAATs in this setting, additional testing was conducted for gonorrhea using conventional culture techniques.9 In addition, validation was conducted on NAATs testing at the laboratory to assess the performance of Probetec tests for nonurethral sites.
The surveillance project protocol entailed obtaining a rectal swab, which was tested by the BD ProbeTec for gonorrhea and chlamydia; and another rectal swab was collected using BBL CultureSwab Plus and inoculated on Thayer Martin media. A pharyngeal swab was also tested for gonorrhea (collected with BBL CultureSwab Plus and inoculated on a Thayer Martin plate); urine was tested using BD ProbeTec for gonorrhea and chlamydia. Patients had to agree to have all tests to participate. The Massachusetts Department of Public Health, Division of STD Prevention provided the NAAT kits, donated by Becton Dickinson.
Samples were stored at room temperature and batch transported to the Massachusetts State Laboratory Institute (MSLI) daily. Results were provided in real time (cultures in 2–3 days and NAATs 3–10 days). Positive results were communicated by phone to an identified contact at FCH and triage for treatment was coordinated between the research and clinical staff. A retrospective review of the surveillance project data were approved by the FCH Institutional Review Board. Relevant data were extracted from patient medical records, including HIV status and prior history of STDs (through key word searches of the patients’ electronic medical records as well as laboratory reports). Psychosocial risk factors were examined using DSM-IV-TR Axis I diagnoses for depression, anxiety, PTSD, adjustment disorders, and substance use disorders.17
Deidentified electronic medical record data were analyzed and linked to prevalence monitoring results. Data extracted from patient electronic medical records were entered into an MS Excel database and analyzed with SPSS statistical software. For all analyses, α was set at the P <0.05 level. The univariate distributions for each of the variables relevant to the analysis were examined, including HIV serostatus, age, insurance status, race/ethnicity, sexual and substance use history where available. Data were analyzed examining proportional differences using chi-square tests and, where cell sizes were small, Fisher’s exact tests. Odds ratios (ORs) were calculated to assess the risk of particular outcomes. Correlations were used to assess the extent to which scores on two variables occupy the same relative position.
Demographics of the convenience sample (n = 114) are described in Table 1. The mean age of participants was 40.68 (range = 19–68; SD = 10.33). The majority of MSM were white (68%); 11% were racial/ethnic minority; 22% were of unknown race/ethnicity. Most participants were privately insured (78%); 13% were publicly insured, 4% were uninsured, and 5% were self-pay. Overall, 22% of the sample was HIV-infected. There were no statistically significant differences in demographics between those infected with an STD and those who were uninfected.
Of the 114 MSM who were screened for gonorrhea and chlamydia over the 1-month project period, 11% tested positive for an STD (Table 2). NAAT-detected urethral chlamydia positivity was 2.6% and urethral gonorrhea was 1.0%. NAAT-detected rectal chlamydia positivity was 6.1% and NAAT-detected rectal gonorrhea was 1.7%. There were no cases of rectal gonorrhea (culture) detected or pharyngeal gonorrhea (culture) detected. There was one indeterminate NAAT rectal gonorrhea result, which was not confirmed by culture.
Those who were infected with an STD were considerably more likely to have a prior lifetime history of 1 or more STD infections when compared with individuals who were uninfected (OR = 3.69; P <0.02) (Table 1). Almost half of the men screened had a previous history of one or more STDs. HIV-infected participants were more likely to have history of STDs than HIV-uninfected participants (OR = 4.36; P <0.001).
Psychosocial Risk Factors
There were no significant differences observed in psychosocial risk factors between STD-infected and STD-uninfected participants. However, depression (38%), anxiety (15%), and other mental health diagnoses (e.g., PTSD and adjustment disorder) (11%) were common in this patient population. Moreover, 19% of MSM had been diagnosed with a substance use disorder (SUD) and SUD was associated with having depression (P <0.01). Tobacco use was common (18% of sample) and participants with a prior history of STDs were more likely to currently use tobacco or to have a history of tobacco use as compared to MSM without a history of STDs (OR = 2.74; P <0.04). Relative to HIV-uninfected participants, HIV-infected individuals were more likely to have an SUD (OR = 3.29; P <0.01) and were more likely to currently use tobacco or to have a history of tobacco use (OR = 2.27; P <0.000). Approximately 4% of the sample had been sexually abused as children. Childhood sexual abuse was also associated with having depression (P <0.01) and SUD (P <0.01).
The current study utilized NAAT technology for STD testing to determine the prevalence of asymptomatic STDs among MSM who had been sexually active (oral and/or anal sex) with another male within the past year. Asymptomatic MSM health center patients were screened for gonorrhea and chlamydia, using the highly sensitive BD ProbeTec. Overall, 11% of MSM tested positive. There was a higher positivity rate for asymptomatic rectal gonorrhea by NAAT testing (1.7%) when compared with testing by culture. Rectal chlamydia was detected among 6.1% of asymptomatic men. Overall, we would have missed 7.8% of infection (either CG or CT) had we only screened for urine. These findings suggest that screening asymptomatic MSM using NAAT allows for the detection of STDs that may not be diagnosable using other traditional assays and is consistent with other MSM studies.18,19 Moreover, the prior focus on symptomatic clinic populations may miss the broader at risk population who may harbor untreated, largely asymptomatic infections.6
Individuals who were infected with an STD were considerably more likely to have a prior history of one or more STDs relative to those who were uninfected. However, there were no statistically significant differences in psychosocial risk factors between participants infected with STDs and those without, because many potentiators of risky sexual practices, e.g., depression, substance use, and other mental health comorbidities were common among MSM with and without an STD. Although these findings suggest that a history of previous STDs may be the best predictor of asymptomatic STD infection as opposed to psychosocial risk factors such as depression, anxiety, or substance abuse, additional research is warranted to explore the relationship between sexual and behavioral risks and psychosocial risk factors.
Although there were no significant differences observed between STD infected and STD uninfected MSM by serostatus, there were many significant differences observed between HIV-infected and HIV-uninfected participants overall. HIV-infected participants were more likely to have multiple risk factors, including a history of STDs, substance use disorder, and tobacco use when compared with HIV-uninfected participants.
A limitation to the current study is associated with the specificity of NAAT technology. BD ProbeTec has a higher rate of false-positive test results relative to traditional culture assays.8 There has also been concern that sequence variation may occur among some gonococcal populations and use of NAATs may result in false negatives because of inhibitory substances that may suppress detection in the strand displacement assay utilized by BD ProbecTec.20
The determination of asymptomatic STD prevalence among MSM in the Boston area is an important step in documenting epidemiologic trends in this population, to intervene to curb rising rates of STDs among MSM and to monitor behaviors that may lead to further increases in the local HIV epidemic. Moreover, local STD prevalence data can help inform health care provider STD screening guidelines for MSM, ensuring culturally competent and high-quality care. Despite the noted limitations, routine NAAT screening for gonorrhea and chlamydia seems highly warranted in this setting.
1. CDC. Sexually Transmitted Disease Surveillance, 2005. Atlanta: U.S. Department of Health and Human Services, Centers for Disease Control and Prevention; 2006.
2. MDPH. Massachusetts STD and HIV Surveillance Report: 2005. Boston: Massachusetts Department of Public Health, Bureau of Communicable Disease Control, Division of STD Prevention and HIV/AIDS Surveillance; 2006.
3. CDC. Sexually transmitted diseases treatment guidelines, 2002. MMWR Morb Mortal Wkly Rep 2002; 51:RR-6.
4. Mimiaga MJ, Goldhammer H, Belanoff C, et al. Men who have sex with men: Perceptions about sexual risk, HIV and sexually transmitted disease testing, and provider communication. Sex Transm Dis 2007; 34:113–119.
5. CDC. Screening tests to detect Chlamydia trachomatis
and Neisseria gonorrhoeae
infections–2002. MMWR Morb Mortal Wkly Rep 2002; 51:RR-15.
6. Rogers SM, Miller HG, Miller WC, et al. NAAT-identified and self-reported gonorrhea and chlamydial infections: Different at-risk population subgroups? Sex Transm Dis 2002; 29:588–596.
7. Van Der Pol B, Ferrero DV, Buck-Barrington L, et al. Multicenter evaluation of the BDProbeTec ET System for detection of Chlamydia trachomatis
and Neisseria gonorrhoeae
in urine specimens, female endocervical swabs, and male urethral swabs. J Clin Microbiol 2001; 39:1008–1016.
8. Katz AR, Effler PV, Ohye RG, et al. False-positive gonorrhea test results with a nucleic acid amplification test: The impact of low prevalence on positive predictive value. Clin Infect Dis 2004; 38:814–819.
9. Zenilman JM, Miller WC, Gaydos C, et al. LCR testing for gonorrhoea and chlamydia in population surveys and other screenings of low prevalence populations: Coping with decreased positive predictive value. Sex Transm Infect 2003; 79:94–97.
10. Taylor MM, Aynalem G, Smith LV, et al. Methamphetamine use and sexual risk behaviors among men who have sex with men diagnosed with early syphilis in Los Angeles County. Int J STD AIDS 2007; 18:93–97.
11. Stall R, Mills TC, Williamson J, et al. Association of co-occurring psychosocial health problems and increased vulnerability to HIV/AIDS among urban men who have sex with men. Am J Public Health 2003; 93:939–942.
12. Kalichman SC, Greenberg J, Abel GG. HIV-seropositive men who engage in high-risk sexual behavior: Psychological characteristics and implications for prevention. AIDS Care 1997; 9:441–450.
13. Kelly JA, Murphy DA, Bahr GR, et al. Factors associated with severity of depression and high-risk sexual behavior among persons diagnosed with human immunodeficiency virus (HIV) infection. Health Psychol 1993; 12:215–219.
14. Fleming DT, Wasserheit JN. From epidemiological synergy to public health policy and practice: The contribution of other sexually transmitted diseases to sexual transmission of HIV infection. Sex Transm Infect 1999; 75:3–17.
15. Rothenberg RB, Wasserheit JN, St Louis ME, et al. The effect of treating sexually transmitted diseases on the transmission of HIV in dually infected persons: A clinic-based estimate. Ad Hoc STD/HIV Transmission Group. Sex Transm Dis 2000; 27:411–416.
16. Mayer KH, Mimiaga MJ, VanDerwarker R. Fenway Community Health\'s model of integrated community-based LGBT care, education, and research. In: Meyer IH, Northridge ME, editors. The Health of Sexual Minorities. New York: Springer Science and Business Media, LLC; 2007:693–715.
17. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders (DSM-IV-TR), 4th ed (Text Revision). Washington, DC: Am Psychiatric Press; 2000.
18. Benn PD, Rooney G, Brown M, et al. Chlamydia trachomatis
and Neisseria gonorrhoeae
infection and the sexual behavior of men who have sex with men. Sex Transm Infect 2007; 83:106–112.
19. Kent CK, Chaw JK, Wong W, et al. Prevalence of rectal, urethral, and pharyngeal chlamydia and gonorrhea detected in 2 clinical settings among men who have sex with men: San Francisco, California, 2003. Clin Infect Dis 2005; 41:67–74.
20. Whiley DM, Tapsall JW, Sloots TP. Nucleic acid amplification testing for Neisseria gonorrhoeae
: An ongoing challenge. J Mol Diagnostics 2006; 8:3–15