Diagnosing and treating sexually transmitted diseases (STDs) are important both for the health of human immunodeficiency virus (HIV)-infected persons, their sexual partner(s), and for HIV prevention efforts, as STD coinfection can increase the risk of HIV transmission.1–3 HIV-infected persons might also be at increased risk of acquiring STDs because of continuation of high risk sexual behaviors,4–6 and may be at increased risk of developing complications of some STDs.7 Therefore, screening and treating STDs in HIV-infected persons are important individual level HIV prevention interventions with both individual and public health benefits.7–10
In the United States, guidelines have been published that include recommendations for the management of HIV-infected persons (HIV Medical Association of America in 2004 and 2009),8,11 the prevention of HIV transmission by HIV-infected persons (Centers for Disease Control and Prevention [CDC], Health Resources and Services Administration, National Institutes of Health, and HIV Medical Association of America in 2003),9 and STD screening of men who have sex with men (MSM) (CDC in 2002 and 2006).10,12 Together, these 3 sets of guidelines recommend at least annual screening of all sexually active HIV-infected MSM for syphilis; urethral chlamydia and gonorrhea in men who have had insertive sex during the preceding year; rectal chlamydia and gonorrhea in men who have had receptive anal sex during the preceding year; and pharyngeal gonorrhea in men who have had receptive oral sex during the preceding year. More frequent screening at 3 to 6 month intervals may be indicated for MSM at higher risk of acquiring STDs.
The high prevalence of STDs among MSM underscores the importance of screening, as many of these infections are asymptomatic.13–17 For example, one study found the following positivity among tests of asymptomatic MSM: 7.6% for rectal chlamydia, 6.1% for rectal gonorrhea, and 7.8% for pharyngeal gonorrhea; positivity was higher among HIV-infected than uninfected men.14 Among MSM with syphilis, high rates of HIV coinfection have been reported, ranging from 45% to 90%,18,19 although these rates might overestimate syphilis and HIV coinfection among MSM in HIV clinics. We did not find any large scale studies that reported syphilis, chlamydia, and gonorrhea screening rates and positivity in at-risk HIV-infected MSM.
Our objective was to determine whether providers who care for HIV-infected MSM in large HIV clinics followed the published guidelines and screened asymptomatic men for syphilis, chlamydia, and gonorrhea at exposed anatomical sites. Among screened asymptomatic HIV-infected MSM, we calculated the positivity of syphilis, urethral and rectal chlamydia, and urethral, rectal, and pharyngeal gonorrhea.
We evaluated STD screening at 8 large HIV clinics in 6 US cities with historically high rates of syphilis: Atlanta, Chicago, Los Angeles, Miami, New York, and San Francisco. To be included in the study, HIV clinics were required to provide health services for at least 200 HIV-infected MSM per year. Clinics were also selected to include Ryan White grantees, a mix of public and private clinics, and a racially and ethnically diverse study sample. Among the selected 8 clinics, annual numbers of HIV-infected MSM who received care ranged from 701 to 2010. We selected a random sample of patients for review and abstraction of their medical records, with a goal of 200 records from each clinical site. Patients were eligible for inclusion if they were male, age 18 years or older, HIV-infected, and had a history of sex with men. Clinic staff conducted medical record reviews and abstractions, and entered data on worksheets that were developed to extract information on patients' demographic characteristics, insurance status, social and medical history, clinical complaints, physical examinations, and laboratory testing. Information from the patient's first visit to the clinic through the abstraction date was included. Seven of 8 clinics had partial year data for 2006, and 1 clinic had none. Deidentified patient data were entered into an Access database. The Institutional Review Board at CDC, Battelle, and each clinic reviewed the study protocol, and the study was determined to be nonresearch.
For patients who had visits from 2004 to 2006, we estimated demographic characteristics, primary health insurance, the number of visits by year, and the percentage of visits where the patient was asymptomatic for an STD. For patients who had an initial visit to the clinic before 2004, abstracted data from visits that occurred from 1998 to 2003 were used to determine patient characteristics such as race, ethnicity, and insurance coverage because these data were typically only collected at the initial visit. We also estimated the percentage of patients in different categories of mean HIV viral load and mean CD4 count in 2004, 2005, and 2006. We determined the percentage of patients who were on antiretroviral therapy (ART) in each year.
We determined the number of times a patient had been screened for syphilis, chlamydia by anatomical site (urethral and rectal), and gonorrhea by anatomical site (urethral, rectal, and pharyngeal) in 2004, 2005, and 2006. From this, we also estimated the annual screening rate for syphilis, chlamydia, and gonorrhea at each of the 8 clinics, by calculating which selected patients had been screened at least once during a given calendar year. Documentation of sexual activity was not evident for 73.4% of reviewed clinic visits. A study of risk behavior among HIV-infected MSM at an HIV clinic found that most had at least one sex partner in the past 12 months,20 thus we made the assumption that patients in our study were sexually active and should have been screened for STDs. We determined whether patients were eligible for chlamydia or gonorrhea screening based on the organism and potential site of infection, and whether symptoms were noted in the medical record. For example, if a patient had no signs or symptoms of urethral, rectal, or pharyngeal infections, then we considered the patient to be eligible for screening at these anatomical sites. Also, if a patient had urethral symptoms, but no rectal signs or symptoms, he was eligible for rectal screening. A patient was considered to be asymptomatic at the urethral site if there were no dysuria, discharge, lesions, or ulcers; at the rectal site if there were no pain, pruritus, discharge, lesions, or ulcers; or at the pharyngeal site if there were no sore throat, oral lesions, or ulcers. We estimated the percentage of men who were tested for syphilis regardless of symptoms, similar to the method used by the Health Resources and Services Administration to calculate Ryan White clinical performance measures of syphilis screening.21 Because the percentage of men with signs or symptoms of syphilis is quite low, the rate of syphilis testing is approximately the rate of syphilis screening and will be referred to as “screening” in our study.
Syphilis screening tests included nontreponemal serologic tests for syphilis: rapid plasma reagin (RPR) tests or venereal disease research laboratory tests. An incident syphilis infection was defined as a patient who had a reactive RPR test and evidence of a confirmed or presumptive infection in the medical record. Chlamydia or gonorrhea screening tests included nucleic acid amplification tests (NAATs), DNA hybridization tests, or culture. NAATs used for urethral screening included both those that test urethral swab specimens and urine samples. Two of the 8 clinics used NAATs for testing rectal and pharyngeal specimens (Table 1). We estimated the positivity of chlamydia (urethral and rectal) and gonorrhea (urethral, rectal, and pharyngeal) screening tests from 2004 to 2006. The percentages of patients screened were compared using the chi-square test, and a 2-sided P < 0.05 was considered statistically significant. Time trends in the rate of screening were considered to be statistically significant if the Mantel-Haenszel chi-square test P was <0.05.
We reviewed medical records of 1334 patients who had 14,831 visits from 1998 to 2007, and 14,659 (98.8%) of these visits occurred during the study period of 2004–2006. Among the 1334 patients, 995 had visits during 2004, 1321 during 2005, and 652 during 2006. The mean age in 2005 was 40.6 years and ranged from 19 to 73 years (Table 1). Patients in the study were racially and ethnically diverse, and had varied primary insurance coverage. Seven of 8 clinics were Ryan White grantees. In our study, 23.0% of the patients were enrolled in the AIDS Drug Assistance Program. Among 14,659 clinic visits made by the 1334 patients from 2004 to 2006, the majority of patient visits (85.4%) had no genital, rectal, or pharyngeal symptoms documented in the medical record. Approximately half of the patients had a low HIV viral load, and most were receiving ART (Table 2). For example, in 2005, 48.0% of the patients had a mean viral load less than or equal to 400 copies/mL, including those with an undetectable viral load; 36.8% had a mean CD4 cell count >500 cells/mm3; and 76.4% were receiving ART.
The percentage of asymptomatic patients who were screened at least once per year for syphilis was 72.8% in 2004, 75.8% in 2005, and 66.0% in 2006, but the time trend was not significant (P = 0.28) (Table 3). Overall, chlamydia and gonorrhea screening rates at any anatomical site were markedly lower. Substantially more asymptomatic patients were tested at the urethral than the rectal and pharyngeal sites for chlamydia and gonorrhea. For example, in 2005, 17.1% were screened for urethral chlamydia and 4.3% for rectal chlamydia; 17.8% were screened for urethral gonorrhea, but only 8.5% for rectal gonorrhea and 7.7% for pharyngeal gonorrhea. Screening rates varied significantly from clinic to clinic during each year of the study: for example, in 2005, syphilis screening ranged from 46.0% to 99.0% (P < 0.001), urethral chlamydia screening from 1.1% to 41.8% (P < 0.001), rectal chlamydia screening from 0% to 17.8% (P < 0.001), urethral gonorrhea screening from 3.2% to 43.6% (P < 0.001), rectal gonorrhea screening from 0% to 17.2% (P < 0.001), and pharyngeal gonorrhea screening from 0% to 15.1% (P < 0.001). Clinics that had nongenital NAAT testing available during the study period (clinics G and H) had rates of nonurethral chlamydia and gonorrhea screening that ranged from 0% to 21.3% during 2004–2006.
Among tests of asymptomatic men screened for chlamydia, 2.3% were positive at the urethra and 9.8% at the rectum. Among tests of those asymptomatically screened for gonorrhea, 5.0% were positive at the urethra, 3.0% at the rectum, and 3.5% at the pharynx (Table 4). Positivity for NAAT and non-NAAT (DNA hybridization test and culture) at each anatomical site for chlamydia and gonorrhea is also presented in Table 4. The most marked difference between NAATs and alternative testing was found for pharyngeal gonorrhea (11.5% vs. 0.7%, respectively). Among rectal gonorrhea screening tests, 21.2% (49) had missing results and 91.8% (45) of these missing results were cultures; among the pharyngeal gonorrhea screening tests, 23.3% (47) had missing results and 93.6% (44) of these were cultures. Although 17.8% of tests among men screened for syphilis with an RPR or venereal disease research laboratory test were reactive, only 1.7% of tests lead to a documented confirmed syphilis diagnosis, and 1.1% to a presumptive syphilis diagnosis (Table 4).
This retrospective chart review in large US HIV clinics yielded important information regarding provider adherence to national guidelines for STD screening in this patient population. Among providers caring for HIV-infected MSM, we found that adherence to the recommendation for syphilis screening was much greater than for chlamydia or gonorrhea screening. Compared to our finding of syphilis screening rates of 66.0% to 75.8% and gonorrhea screening rates of 3.0% to 18.3%, a study of self-reported STD testing among HIV-negative MSM during 2003–2005 found lower rates for syphilis (39%) but higher rates for gonorrhea (36%).22
Several factors can account for our finding of higher screening rates for syphilis than for chlamydia or gonorrhea. Providers were probably aware that untreated syphilis can result in adverse health outcomes, with infection resulting in neurologic or ophthalmic manifestations, and that syphilis infection increases HIV viral load and decreases CD4 cell count in HIV-infected persons, thereby increasing the risk of transmitting HIV.23–25 Also, screening opportunities for syphilis are convenient because an order for an RPR can be easily added to other laboratory orders that accompany specimens drawn for monitoring HIV disease and treatment. Unlike chlamydia and gonorrhea screening, syphilis screening does not require taking a detailed sexual history to assess the risk of infection by anatomical site and sexual behavior, nor does it require an additional invasive specimen collection. Syphilis screening is a requirement of Ryan White grantees as a measure of quality assurance, and 7 of the 8 clinics in our study received Ryan White funding. Finally, as syphilis rates increased among MSM at the start of the current decade,26 increased public and provider awareness of the problem likely contributed to greater patient demand for screening and provider adherence to syphilis screening guidelines.
To increase syphilis screening of HIV-infected MSM who are in clinical care to optimal levels, additional interventions will be necessary, including better awareness and dissemination of the guidelines. Structural interventions also might be effective to increase screening, such as screening protocols, reminder systems, and chart prompts in electronic medical records.
We found low rates of chlamydia and gonorrhea screening at all anatomical sites, especially at nonurethral sites. Low screening rates for gonorrhea and chlamydia suggest that substantial barriers exist for complying with these guidelines. More men were screened for rectal gonorrhea than chlamydia. It might be more difficult for a clinic to acquire chlamydial culture than gonococcal culture, and if the clinic does not have access to nongenital NAATs then rectal chlamydial testing will not be performed. Culture for either chlamydia or gonorrhea requires specialized media and specimen handling and might be considered too time consuming or costly by the clinic. Another significant barrier that prevented providers from following guidelines for nonurethral chlamydia and gonorrhea screening at most clinics was the lack of NAATs that have been cleared by the Food and Drug Administration (FDA) for testing at these anatomical sites.13 Until studies are completed that are sufficient for the FDA to clear NAATs for rectal and pharyngeal specimens, laboratories can establish performance specifications of FDA-modified NAATs for testing rectal and pharyngeal specimens. In the past, too few laboratories have established these performance specifications, although recently some large commercial (LabCorp and Quest), university, and public health laboratories have done this and currently offer NAATs for rectal and pharyngeal specimens.13,27 Although these tests are now widely available, most insurance plans will not reimburse for a non-FDA-cleared test. Even at the 2 clinics that had self-validated NAATs available for testing nonurethral specimens, screening rates were extremely low.
Because screening tests for urethral chlamydial and gonococcal infection are widely available, but urethral screening rates in our study were found to be low, other barriers must be preventing adherence to the recommendation for screening. Providers report insufficient time, competing counseling, and testing priorities during a brief office visit, and lack of skill in conducting a sexual history as reasons for not performing recommended prevention services.28 Providers must be skillful and comfortable conducting a detailed sexual history to assess STD risk by anatomical site. In our study, sexual risk assessment was not documented for 73.4% of visits, despite recommendations to conduct ongoing assessment to inform appropriate STD screening and counseling interventions.8–12 Provider-focused, structural interventions are needed to assure testing. Resources are available to facilitate both taking a detailed sexual history of anatomical site-specific sexual practices, and discussions with patients about HIV and STD transmission.9,29 Providers should be aware of these instruments and instructed in their use, and they need to be more widely disseminated. Interventions to overcome time barriers include providing reimbursement for conducting sexual risk assessment, and pay for performance and public reporting, which have been demonstrated to be effective in improving the performance of Medicare providers.30–32
We found a moderate to high percentage of positive chlamydia and gonorrhea screening tests among asymptomatic men, similar to test positivity found in other studies of MSM.13–17 The true positivity among rectal and pharyngeal specimens was likely higher because many of these patients were screened using non-NAAT methods that are less sensitive than NAATs.33,34 One study found that pharyngeal and rectal NAAT testing identified twice as many chlamydial and gonococcal infections as culture, and almost 4 times as many rectal chlamydial infections.34 In our study, a large percentage of gonorrhea culture results was missing, and this might have resulted in an under- or overestimation of gonorrhea positivity.
This evaluation has several limitations. Although patients were randomly selected at each clinic, the 8 clinics selected for the study were urban HIV clinics and might not be representative of HIV clinics in suburban or rural communities. Because well-established HIV and STD programs in urban clinics tend to have higher STD screening rates, these estimates probably cannot be generalized to less established nonurban programs. Patient sexual activity, including engaging in receptive oral sex and receptive anal sex, was poorly documented in the medical records, so the assumption that all of the patients were sexually active, and therefore should have been screened for pharyngeal and rectal chlamydia and gonorrhea may have resulted in an underestimation of screening rates. However, it was found that 76% of HIV-infected MSM reported one or more oral or anal sex partners in the past 12 months, and 65% reported anal sex partners.20 We assumed that if a patient were symptomatic for an STD, that it would be documented in the medical record. If a patient's symptoms were not documented and he was tested for an STD, then our study would have overestimated asymptomatic screening rates, and positivity for chlamydia and gonorrhea among asymptomatic patients. If patients were screened for STDs in a clinic or location other than the HIV clinic, such as an STD clinic, then our study would underestimate the rate. The rate of syphilis screening observed in 2006 was an underestimate of the actual screening rate, because most clinics stopped abstractions during 2006 and data for a full year of patient visits were not available for these clinics. Because the likelihood of a patient having been screened would be expected to increase with increasing number of visits, we would expect the screening rates to be lower for 2006, which included only partial year data for some clinics. The number of medical records abstracted at each clinic differed, possibly resulting in over- or underrepresentation of screening practices at any one clinic.
Preventing STD infections in those with HIV infection has been a challenging public health problem for the past 3 decades. Acquisition of STDs by HIV-infected persons indicates participation in high risk behaviors that might transmit HIV to sexual partners. With the current burden of HIV infections disproportionately affecting MSM, and with increasing rates of syphilis infections among men in the United States over the past several years,35,36 it is encouraging that HIV care providers are screening most HIV-infected MSM for syphilis according to existing guidelines. Suboptimal screening rates for gonorrhea and chlamydia indicate that barriers exist for screening men for these infections. The positivity of asymptomatic chlamydial and gonococcal infections in HIV-infected MSM underscores the importance of STD screening, and interventions are needed to increase screening.
1.Cohen MS, Hoffman IF, Royce RA, et al. AIDSCAP Malawi Research Group. Reduction of concentration of HIV-1 in semen after treatment of urethritis: Implications for prevention of sexual transmission of HIV-1. Lancet 1997; 349:1868–1873.
2.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; 75:15.
3.Wasserheit JN. Epidemiological synergy. Interrelationships between human immunodeficiency virus infection and other sexually transmitted diseases. Sex Transm Dis 1992; 19:61–77.
4.Bachmann LH, Grimley DM, Waithaka Y, et al. Sexually transmitted disease/HIV transmission risk behaviors and sexually transmitted disease prevalence among HIV-positive men receiving continuing care. Sex Transm Dis 2005; 32:20–26.
5.Do AN, Hanson DL, Dworkin MS, et al. Risk factors for and trends in gonorrhea incidence among persons infected with HIV in the United States. AIDS 2001; 15:1149–1155.
6.Scheer S, Chu PL, Klausner JD, et al. Effect of highly active antiretroviral therapy on diagnoses of sexually transmitted diseases in people with AIDS. Lancet 2001; 357:432–435.
7.Kaplan JE, Benson C, Holmes KH, et al. Guidelines for prevention and treatment of opportunistic infections in HIV-infected adults and adolescents: Recommendations from CDC, the National Institutes of Health, and the HIV Medicine Association of the Infectious Diseases Society of America. MMWR Recomm Rep 2009; 58:1–207.
8.Aberg JA, Kaplan JE, Libman H, et al. Primary care guidelines for the management of persons infected with human immunodeficiency virus: 2009 update by the HIV medicine association of the infectious diseases society of America. Clin Infect Dis 2009; 49:651–681.
9.Centers for Disease Control and Prevention. Incorporating HIV prevention into the medical care of persons living with HIV. Recommendations of CDC, the Health Resources and Services Administration, the National Institutes of Health, and the HIV Medicine Association of the Infectious Diseases Society of America. MMWR Recomm Rep 2003; 52:1–24.
10.Workowski KA, Berman SM. Sexually transmitted diseases treatment guidelines, 2006. MMWR Recomm Rep 2006; 55:1–94.
11.Aberg JA, Gallant JE, Anderson J, et al. Primary care guidelines for the management of persons infected with human immunodeficiency virus: Recommendations of the HIV Medicine Association of the Infectious Diseases Society of America. Clin Infect Dis 2004; 39:609–629.
12.Centers for Disease Control and Prevention. Sexually transmitted diseases treatment guidelines 2002. MMWR Recomm Rep 2002; 51:1–78.
13.Centers for Disease Control and Prevention. Clinic-based testing for rectal and pharyngeal Neisseria gonorrhoeae
and Chlamydia trachomatis
infections by community-based organizations—five cities, United States, 2007. Morb Mortal Wkly Rep 2009; 58:716–719.
14.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.
15.Mimiaga MJ, Helms DJ, Reisner SL, et al. Gonococcal, chlamydia, and syphilis infection positivity among MSM attending a large primary care clinic, Boston, 2003 to 2004. Sex Transm Dis 2009; 36:507–511.
16.Moncada J, Schachter J, Liska S, et al. Evaluation of self-collected glans and rectal swabs from men who have sex with men for detection of Chlamydia trachomatis
and Neisseria gonorrhoeae
by use of nucleic acid amplification tests. J Clin Microbiol 2009; 47:1657–1662.
17.Whittington WL, Collis T, Dithmer-Schreck D, et al. Sexually transmitted diseases and human immunodeficiency virus-discordant partnerships among men who have sex with men. Clin Infect Dis 2002; 35:1010–1017.
18.Blocker ME, Levine WC, St Louis ME. HIV prevalence in patients with syphilis, United States Sex Transm Dis 2000; 27:53–59.
19.Buchacz K, Klausner JD, Kerndt PR, et al. HIV incidence among men diagnosed with early syphilis in Atlanta, San Francisco, and Los Angeles, 2004 to 2005. J Acquir Immune Defic Syndr 2008; 47:234–240.
20.Golden MR, Wood RW, Buskin SE, et al. Ongoing risk behavior among persons with HIV in medical care. AIDS Behav 2007; 11:726–735.
22.Tai E, Sanchez T, Lansky A, et al. Self-reported syphilis and gonorrhoea testing among men who have sex with men: National HIV behavioural surveillance system, 2003–5. Sex Transm Infect 2008; 84:478–482.
23.Buchacz K, Patel P, Taylor M, et al. Syphilis increases HIV viral load and decreases CD4 cell counts in HIV-infected patients with new syphilis infections. AIDS 2004; 18:2075–2079.
24.Kofoed K, Gerstoft J, Mathiesen LR, et al. Syphilis and human immunodeficiency virus (HIV)-1 coinfection: Influence on CD4 T-cell count, HIV-1 viral load, and treatment response. Sex Transm Dis 2006; 33:143–148.
25.Palacios R, Jimenez-Onate F, Aguilar M, et al. Impact of syphilis infection on HIV viral load and CD4 cell counts in HIV-infected patients. J Acquir Immune Defic Syndr 2007; 44:356–359.
26.Peterman TA, Heffelfinger JD, Swint EB, et al. The changing epidemiology of syphilis. Sex Transm Dis 2005; 32:S4–S10.
28.Vogel MR, Lubinski CB. Prevention with positives: Primary HIV care provider attitudes and practices. Paper presented at: National HIV Prevention Conference; June 12–15, 2005; Atlanta, GA. Abstract M2-F0901.
29.Centers for Disease Control and Prevention. Guide to Taking a Sexual History. Atlanta, GA: US Health and Human Services, 2009.
30.Fisher ES. Paying for performance—risks and recommendations. N Engl J Med 2006; 355:1845–1847.
31.Institute of Medicine. Rewarding Provider Performance: Aligning Incentives in Medicare. Washington, DC: The National Academy Press, 2007.
32.Steinbrook R. Public report cards—cardiac surgery and beyond. N Engl J Med 2006; 355:1847–1849.
33.Bachmann LH, Johnson RE, Cheng H, et al. Nucleic acid amplification tests for diagnosis of Neisseria gonorrhoeae
oropharyngeal infections. J Clin Microbiol 2009; 47:902–907.
34.Schachter J, Moncada J, Liska S, et al. Nucleic acid amplification tests in the diagnosis of chlamydial and gonococcal infections of the oropharynx and rectum in men who have sex with men. Sex Transm Dis 2008; 35:637–642.
35.Centers for Disease Control and Prevention. HIV/AIDS Surveillance Report, 2007. Atlanta, GA: US Department of Health and Human Services, 2009.
36.Centers for Disease Control and Prevention. Sexually Transmitted Disease Surveillance, 2008. Atlanta: US Department of Health and Human Services, 2009.