Approximately 5%–10% of persons receiving care at HIV clinics are infected with Neisseria gonorrhoeae (NG) and/or Chlamydia trachomatis (CT) at any given time.1–7 Detecting and treating these generally asymptomatic infections improves health by preventing their spread and downstream complications and may also reduce HIV transmission through (1) identifying opportunities for counseling about risky sexual behavior and (2) decreasing mucosal inflammation and HIV RNA levels at the site of infection.8–10 Starting in 2003, the United States and other countries have recommended at least annual NG/CT screening among the relatively broad group of all sexually active persons living with HIV (PLWH).11
Since 2003, a number of clinical cohorts have reported increases in NG/CT testing.12–14 These increases notwithstanding, overall NG/CT testing has remained low. In 7 geographically diverse HIV clinics within the HIV Research Network (HIVRN) cohort, NG/CT testing increased each year starting in 2004, but as of 2010 the annual testing rate was still only 39% of patients engaged in care.14 Data from the nationally representative Medical Monitoring Project and from other large cohorts have shown similarly low NG/CT screening rates as recently as 2011.12,13,15,16
Since publication of screening recommendations, HIV clinics in Maryland, US, and Ontario, Canada, separately reported that several-year increases in annual NG/CT testing were countered by declines in NG/CT test positivity such that overall NG/CT case detection remained constant.12,17 The failure of increased testing to increase case detection leads to questions about the utility of the broad approach to screening all sexually active PLWH as compared to a more targeted approach.12,18 In this study, we determined trends in NG/CT test positivity and case detection in the HIVRN during 2004–2014, to assess whether case detection increased with the known rise in testing over this period. Based on known variation in testing rates and test positivity by sexual risk group,12,14,19 we stratified analyses by men who have sex with men (MSM), men who have sex exclusively with women (MSW), and women.
The HIVRN includes 12 adult HIV clinical care sites that are widely distributed across the United States.20 Sites prospectively collect demographic, laboratory, and visit data from electronic medical records and structured chart reviews. Submission of NG/CT laboratory data is optional for HIVRN sites, and we restricted this analysis to 4 sites (from 4 different states including 2 in the West, 1 in the South, and 1 in the Northeast) that submitted complete NG/CT testing and result data from January 1, 2004, through December 31, 2014. Three additional HIVRN sites previously examined for testing trends14 were excluded because they were unable to submit comprehensive result data before 2010 or testing or result data subsequent to 2010. We did not include the few years of data available from these sites because of risk of introducing bias in multiyear trends. We included all patients aged 18 years or older during calendar years of active follow-up, defined as having at least 1 outpatient visit and 1 CD4 count within the calendar year. Patients were allowed to return to observation after one or more years of active follow-up. Institutional review boards at the individual sites and the data coordinating center at Johns Hopkins University School of Medicine approved the collection and use of these data.
The primary outcomes were (1) testing, defined as having at least 1 NG and/or CT test at any body site (genitalia, rectum, or mouth) during a year of active follow-up in care; (2) test positivity, defined as having at least 1 positive NG and/or CT result during any year when testing occurred, regardless of the number of tests performed; and (3) case detection, defined as having at least 1 positive NG and/or CT result during a year of active follow-up in care (with untested persons being included in the denominator). Data distinguishing the body sites of tests were unavailable. For each HIVRN site, data were retrieved from institutional electronic health record databases. These databases contain data on assays ordered at the institution. However, in no case do the databases contain laboratory data performed outside the institution (for example at a public sexually transmitted infection clinic).
For the purpose of exploring how many distinct testing episodes occurred for an individual patient within a year, we grouped tests into episodes based on occurring within 30 days of one another. By this we hoped to eliminate instances of counting tests of cure or of patients providing simultaneously ordered samples from different body sites on different days as separate testing episodes.
The exposure of primary interest was time in calendar years. We defined MSM as persons who self-identified as men and reported ever having male sexual contact at the time of enrollment into the cohort. Additional time-fixed exposures included HIVRN clinical site, race/ethnicity, and injection drug use (IDU) as an HIV risk factor. Time-variable exposures included age in years, the annual number of HIV provider visits, CD4 count, and HIV RNA, with the latter 2 variables defined as the first recorded value of each calendar year.
We created binary outcome variables for testing, test positivity, and case detection within each patient year (PY) and conducted analyses at the PY level. We performed logistic regression to assess separate time trends in testing, test positivity, and case detection using generalized estimating equations to adjust variance for within-person correlation. Based on previous testing results for 2004–2010 and on initial, graphical inspection of the data, we parameterized time linearly. Our overall population model included sexual risk group (MSM, MSW, or women) as an exposure. We then created separate models within each group. All multivariate models included HIVRN clinical site as a covariate, results of which are suppressed. We used Stata 14.0 (StataCorp LP, College Station, TX) to conduct all analyses.
A total of 15,614 patients contributed 69,694 PY during the 2004–2014 study period. The median number of years in care was 3 (interquartile range, 1–6). The sample was 50% MSM, 26% MSW, and 24% women (Table 1). Overall, the median age in the first year of observation was 44 years old; for MSM it was 42, for MSW 47, and for women 42. The full cohort was 44% non-Hispanic Black, including 26% of MSM, 58% of MSW, and 65% of women. During the first year of observation, the median number of HIV provider visits for the full sample and for each subgroup was 3 (interquartile range, 2–5). Eleven percent of all 69,694 PY involved only a single HIV provider visit within the calendar year. During the first year of observation, 42% of the overall cohort had an HIV RNA level >400 copies/mL on the first measurement of the year, with little variation among MSM, MSW, and women. Among patients observed during 2014, this percentage decreased to 19%, again with little variation by sexual risk group.
Annual NG/CT Testing
Overall, 11,184 patients (72%) underwent NG/CT testing during at least 1 of the years of study observation. During 2004, 22% of the overall cohort had NG/CT testing performed at least once, including 23% of MSM, 15% of MSW, and 29% of women (Fig. 1A). In general, the proportion of patients tested for NG/CT increased year over year among the full cohort and among each subgroup. In 2014, 60% of the overall cohort was tested for NG/CT, unadjusted odds ratio (OR) per year over the study interval 1.16 (95% confidence interval: 1.15 to 1.16). In 2014, 67% of MSM were tested [unadjusted OR per year 1.18 (1.17–1.19)], 49% of MSW were tested [1.16 (1.15–1.17)], and 57% of women were tested [1.12 (1.11–1.13)].
Seventy-four percent of 31,419 PY with any NG/CT testing included just 1 testing episode, 19% 2 episodes, and 7% 3 or more episodes. Eighty-two percent of testing episodes included just 1 sample (99% of which were tested for both NG and CT), 10% of episodes included 2 samples (drawn at different times and/or body sites), 5% included 3 samples, and 3% more than 3 samples.
In multivariate analysis (Table 2), annual testing increased over time among the full group, adjusted OR (AOR) per year 1.22 (1.21–1.22). MSM [AOR 0.99 (0.93– 1.05)] were equally likely and MSW [0.72 (0.68–0.76)] were less likely to be tested than women. Age, race/ethnicity, number of visits, CD4 count >200 cells/μL, and HIV RNA >400 copies/mL were also associated with testing. In addition to calendar time, factors with the largest effect size in the full group model included younger age (AOR for <30 years old, 2.60 [2.40–2.82] and for 30-39 years old, 1.96 [1.85–2.08], both compared with ≥50 years old), and number of visits (2.03 [1.93–2.13] for ≥7 visits compared with ≤3 visits). Calendar time was strongly associated with testing in each subgroup, MSM AOR 1.25 (1.24–1.26), MSW 1.20 (1.19–1.22), and women 1.17 (1.16–1.19). The pattern of factors associated with testing among each of the subgroups generally resembled the pattern in the full group.
Among 11,184 patients tested at least once over the full study period, 1176 (10.5%) had at least 1 positive result for NG/CT or both. Within the full cohort, test positivity increased from 3.6% in 2004 to 6.5% in 2014, unadjusted OR per year 1.05 (1.03–1.07) (Fig. 1B). This increasing trend was driven by the increase among MSM from 5.6% in 2004 to 10.1% in 2014, unadjusted OR per year 1.07 (1.05–1.09). Crude test positivity was stable among both MSW and women, unadjusted ORs per year 0.95 (0.88–1.02) and 1.01 (0.94–1.09), respectively. The mean over time was 1.9% among MSW and 1.6% among women.
In multivariate analysis (Table 3), test positivity increased within the full cohort [AOR per year 1.10 (1.07–1.12)]. MSM [AOR 4.09 (3.31–5.05)] and MSW [1.57 (1.18–2.08)] were more likely than women to test positive. In stratified analyses, test positivity increased among MSM [1.12 (1.09–1.15)], was stable among MSW 0.96 (0.89–1.04), and increased among women 1.09 (1.02–1.16). Younger age was strongly associated with test positivity within the full group [AOR for <30 years old, 5.33 (4.32–6.59), and for 30–39 years old, 3.16 (2.59–3.85)] and in each subgroup. Race/ethnicity was not associated with test positivity in the full group nor in any subgroup. Among MSM, having >3 visits, CD4 >200 cells/μL, and RNA >400 copies/μL were associated with having a positive test result.
Among the full cohort, case detection increased from 0.8% of patients engaged in care in 2004 (whether tested or not) being found to have NG/CT or both at least once to 3.9% in 2014 [unadjusted OR per year 1.15 (1.13–1.17) (Fig. 1C)]. Case detection increased among each subgroup: among MSM from 1.3% to 6.8% (unadjusted OR per year 1.16 [1.14–1.18]), among MSW from 0.3% to 1.0% [1.06 (1.00–1.13)], and among women from 0.5% to 0.9% [1.05 (1.00–1.11)]. In multivariate analyses (Table 4), case detection increased over time in the full group and in each subgroup. MSM had nearly 4 times the odds [AOR 3.94 (3.16–4.91)] and MSW approximately the same odds [1.31 (0.99–1.74)] as women for being diagnosed with NG/CT. Younger age was associated with case detection in all subgroups. Non-IDU status, higher CD4 count, and HIV RNA >400 copies/mL were associated with case detection among both MSM and MSW. Race/ethnicity was not associated with case detection.
As a sensitivity analysis, we examined test positivity and case detection trends separately for NG and CT (testing trends were identical as 99% of testing episodes included assays for both bacteria). Inferences in the sensitivity analysis were unchanged. Among the full group, univariate test positivity time trends were 1.07 (1.04–1.10) per year for NG and 1.06 per year (1.03–1.08) for CT (multivariate test positivity models did not converge). Multivariate case detection time trends were 1.21 (1.18–1.25) per year for NG and 1.20 (1.17–1.22) per year for CT.
Finally, we examined combined NG/CT outcomes within each HIVRN site to assess whether trends seen in the full study population were evident in the individual sites. Within each site, NG/CT testing increased over time within the full clinic population [OR's per year ranged from 1.11 (1.09–1.13) to 1.17 (1.15–1.18)] and AOR's per year from 1.14 (1.06–1.23) to 1.23 (1.22–1.25). Test positivity was stable or increasing in univariate analysis in 3 HIVRN sites; the statistical model for the fourth site did not converge. Test positivity increased in multivariate analysis in 2 sites, and models in the other 2 sites did not converge. Case detection increased in every HIVRN site in univariate analysis [OR's per year ranged from 1.07 (1.02–1.13) to 1.15 (1.13–1.18)] and in multivariate analysis in 2 sites for which models converged.
Over 11 years in our 4-site sample, NG/CT testing expanded steadily overall and within each subgroup, reaching 60% within the full population (67% of MSM, 49% of MSW, and 57% of women) in 2014. Contrary to previous studies, test positivity also increased overall and was either increasing or stable within each subgroup. This resulted in steady increases in case detection. In other words, as a greater percentage of patients was tested each year, a greater percentage of patients infected with NG/CT was identified, overall and within each subgroup.
These results generally support the broad screening approach (that all sexually active PLWH be considered for testing at least annually) that has been recommended in the United States since 2003.11 A more targeted approach, for example limiting screening to MSM <30 years old, might be more appropriate if broad screening did not yield increased case detection.18 The increase in case detection contrasts the findings of 2 previous studies (one of which occurred at 1 HIVRN site with that site's 2004–2007 data included in the present study).12,17 However, increased case detection with increased screening has been reported in a cohort in Washington State and in a US military cohort in the past decade.21,22 The present study occurred over a longer period since guideline publication and in a larger sample than the previous studies.
Although supportive, the present study does not provide conclusive evidence for a broad approach to NG/CT screening. Data from other centers and disease modeling studies comparing various targets would provide more evidence. Also, the current screening guidelines include the proviso that patients at particularly high risk (for example, those recently positive for NG/CT) should be screened multiple times per year. Our study focused only on breadth—who should be screened annually—not the frequency of screening among those screened. Future studies might determine the extent to which more frequent testing within a year tends to yield more frequent case detection.
The increase in testing we observed demonstrates the feasibility of implementing NG/CT screening above rates of 20%–40% that were reported by many centers in the past decade.13,15,16,21,23,24 These relatively low rates stood in contrast to syphilis testing rates that have consistently been much higher in other cohorts13,15,21 and averaged 66% in the HIVRN during 2004–2010.14 At least 1 other multisite HIV cohort has reported achieving 50%–60% NG/CT testing rates as of 2009.25 Unique barriers to NG/CT screening include time to obtain urine and mucosal swab samples, difficulty engaging in sexual history discussions, and the lack of Food and Drug Administration approval for rectal and oral site nucleic acid test kits.18,26 Each of the 4 clinics in our sample undertook one or more systematic efforts to increase NG/CT screening during 2004–2014. Interventions included provider education, electronic health record reminders, clinic-wide performance reports, individual provider report cards, and coupling rectal NG/CT screening with rectal cancer screening. Assessing the individual effectiveness of each intervention is an area for future work.
Despite the increase, there is still room to improve testing according to the current guidelines. Although the ceiling level of “sexually active” persons is not known, it is probably at least as high as the 77% of patients who were screened for syphilis in 2010 in the HIVRN.14 Self-collection of rectal and vaginal samples is accurate, may be preferable to provider collection, and may be one way to further increase screening.27–29
Increasing rates of NG and CT within the HIVRN sites' metropolitan areas may have contributed to the increasing test positivity among MSM and to the stable test positivity among MSW and women. Nationally, the combined reported rates of NG and CT in the general population increased approximately 30% from 2004 to 2014 with parallel increases among men and women.19 Similar increases were seen in the 4 metropolitan areas hosting the HIVRN sites.19,30 Although there are no comprehensive surveillance data regarding NG and CT specifically among MSM, there are indications through the Gonococcal Isolate Surveillance Project that increases among MSM may have exceeded increases among MSW and women.19 However, even if expanding community-level NG and CT epidemics contributed to the test positivity trends we observed, this does not change the inference that a broad screening strategy may currently be appropriate.
Another possible contributor to the increase in NG/CT test positivity among MSM is expanded screening at the rectal and oral sites. Historically, screening at these sites has been much lower (<10% annually) than urine screening.3,12,13,17 However, the rectal and oral sites are much more likely to harbor asymptomatic disease with 50%–85% of infections existing at the extragenital compartment and not having concurrent genital tract infection. Increasing screening at extragenital sites is frequently described as a priority.2,3,12,13,31,32 One HIVRN clinic undertook an intervention to specifically increase rectal NG/CT screening (coupling rectal NG/CT screening with rectal cancer screening). Unfortunately, we do not have data on body site of testing and cannot assess the extent to which extragenital testing might be contributing to the increased test positivity. This again does not affect support for a broad screening strategy. As a greater percentage of patients were tested (regardless of body site), a greater percentage were identified as having NG/CT.
As expected from previous studies,12,14,19 MSM were the most likely group to be tested and to test positive. Younger age is also a well-established risk factor for NG/CT.12,19,22 African American race is associated with increased NG/CT prevalence in the general US population.19 However, this association has not consistently been seen among HIV cohorts.3,12,22,33 Among MSM, the association of test positivity (and case detection) with more annual visits may be at least partly due to reverse causation, with positive test results prompting provider visits for treatment and/or further testing.
HIV transmission risk is greatly reduced when HIV RNA is suppressed through antiretroviral therapy.34 Although nonsuppressed HIV RNA at the first visit of the year was associated with a slightly increased likelihood of NG/CT test positivity and case detection, the majority of our cohort (81% in 2014) had suppressed HIV RNA at the first visit (although not necessarily consistent suppression year long), and most NG/CT case detection occurred among these persons. This finding is relevant to future studies that would attempt to determine the utility of NG/CT screening for reducing HIV transmission. It is not clear why having unsuppressed HIV RNA was independently associated with NG/CT case detection. It is possible that psychosocial characteristics such as depression and/or active drug use could be underlying factors leading to both nonadherence to antiretroviral therapy and to risky sexual behavior.
This study has several limitations. First, as stated above, we cannot distinguish body sites of tests. Second, we cannot distinguish screening tests from diagnostic tests. Some of the increases in testing we observed may have resulted from an increase in symptomatic cases, reported exposures, or reported risky behaviors. However, because community NG/CT epidemics expanded by only 30% over the study interval, we would not expect increased diagnostic testing to have contributed the majority of the nearly 300% increase in testing during the study interval. Third, because our laboratory data collection does not capture assays ordered outside the institution, our results likely underestimate the breadth of testing and case detection. However, although there may have been some exceptions (patients verbally reporting outside testing or providers receiving outside test results), we expect the data we capture closely resemble the data that would have been available to clinicians. Finally, although our sample is a relatively large HIV cohort from geographically distributed sites, it includes only 4 distinct sites, and these sites cannot be assumed to be representative of either their local communities or the nation.
In summary, NG/CT testing increased steadily for 11 years following the publication of screening guidelines. NG/CT test positivity did not fall over this interval, and case detection therefore increased steadily along with testing. These findings support the current broad approach to screening. Despite progress, our sites can continue to expand the percent of patients screened annually. That expansion may be expected to yield further NG/CT case detection and thus to help reduce overall NG/CT and HIV transmission and complications.
Participating Sites: Alameda County Medical Center, Oakland, California (Howard Edelstein, M.D.); Children's Hospital of Philadelphia, Philadelphia, Pennsylvania (Richard Rutstein, M.D.); Drexel University, Philadelphia, Pennsylvania (Amy Baranoski, M.D., Sara Allen, C.R.N.P.); Fenway Health, Boston, Massachusetts (Stephen Boswell, M.D.); Johns Hopkins University, Baltimore, Maryland (K.A.G., Richard Moore, M.D., Allison Agwu M.D.); Montefiore Medical Group, Bronx, New York (Robert Beil, M.D.); Montefiore Medical Center, Bronx, New York (Uriel Felsen, M.D.); Oregon Health and Science University, Portland, Oregon (P.T.K.); Parkland Health and Hospital System, Dallas, Texas (Ank Nijhawan, M.D., Muhammad Akbar, M.D.); St. Jude's Children's Research Hospital and University of Tennessee, Memphis, Tennessee (Aditya Gaur, M.D.); Mount Sinai St. Luke's and Mount Sinai West, New York, New York (Judith Aberg, M.D., Antonio Urbina, M.D.); Tampa General Health Care, Tampa, Florida (Charurut Somboonwit, M.D.); Trillium Health, Rochester, New York (William Valenti, M.D.); University of California, San Diego, California (W.C.M.); Sponsoring Agencies Agency for Healthcare Research and Quality, Rockville, Maryland (Fred Hellinger, Ph.D., John Fleishman, Ph.D., Irene Fraser, Ph.D.); Health Resources and Services Administration, Rockville, Maryland (Robert Mills, Ph.D., Faye Malitz, M.S.); and Data Coordinating Center Johns Hopkins University (Richard Moore, M.D., Jeanne Keruly, C.R.N.P., K.A.G., Cindy Voss, M.A., Charles Collins, M.P.H., Rebeca Diaz-Reyes) Works Cited.
1. Kalichman SC, Pellowski J, Turner C. Prevalence of sexually transmitted co-infections in people living with HIV/AIDS: systematic review with implications for using HIV treatments for prevention. Sex Transm Infect. 2011;87:183–190.
2. Soni S, White JA. Self-screening for Neisseria gonorrhoeae and Chlamydia
trachomatis in the human immunodeficiency virus clinic—high yields and high acceptability. Sex Transm Dis. 2011;38:1107–1109.
3. Rieg G, Lewis RJ, Miller LG, et al. Asymptomatic sexually transmitted infections in HIV-infected men who have sex with men: prevalence, incidence, predictors, and screening strategies. AIDS Patient Care STDS. 2008;22:947–954.
4. Phipps W, Stanley H, Kohn R, et al. Syphilis, chlamydia
, and gonorrhea
screening in HIV-infected patients in primary care, San Francisco, California, 2003. AIDS Patient Care STDS. 2005;19:495–498.
5. Heiligenberg M, van der Loeff MFS, de Vries HJ, et al. Low prevalence of asymptomatic sexually transmitted infections in HIV-infected heterosexuals visiting an HIV clinic in The Netherlands. AIDS. 2012;26:646–649.
6. Heiligenberg M, Wermeling PR, van Rooijen MS, et al. Recreational drug use during sex and sexually transmitted infections among clients of a city sexually transmitted infections clinic in Amsterdam, the Netherlands. Sex Transm Dis. 2012;39:518–527.
7. Carpenter RJ, Refugio ON, Adams N, et al. Prevalence and factors associated with asymptomatic gonococcal and chlamydial infection among US Navy and Marine Corps men infected with the HIV: a cohort study. BMJ Open. 2013;3:e002775.
8. Johnson LF, Lewis DA. The effect of genital tract infections on HIV-1 shedding in the genital tract: a systematic review and meta-analysis. Sex Transm Dis. 2008;35:946–959.
9. Fisher JD, Fisher WA, Cornman DH, et al. Clinician-delivered intervention during routine clinical care reduces unprotected sexual behavior among HIV-infected patients. JAIDS J Acquir Immune Defic Syndr. 2006;41:44–52.
10. Cohen MS, Hoffman IF, Royce RA, et al. 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.
11. Health Resources and Services Administration, Administration Services, HIV Medicine Association of the Infectious Diseases Society of America, others. 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.
12. Burchell AN, Grewal R, Allen VG, et al. Modest rise in chlamydia
and gonorrhoea testing did not increase case detection in a clinical HIV cohort in Ontario, Canada. Sex Transm Infect. 2014;90:608–614.
13. Hoover KW, Butler M, Workowski K, et al. STD screening of HIV-infected MSM
in HIV clinics. Sex Transm Dis. 2010;37:771–776.
14. Berry SA, Ghanem KG, Mathews WC, et al. Brief report: gonorrhea
testing increasing but still lagging in HIV clinics in the United States. JAIDS J Acquir Immune Defic Syndr. 2015;70:275–279.
15. Blair JM, Fagan JL, Frazier EL, et al. Behavioral and clinical characteristics of persons receiving medical care for HIV infection—medical Monitoring Project, United States, 2009. MMWR Surveill Summ. 2014;63(suppl 5):1–22.
16. Grewal R, Allen VG, Gardner S, et al. Serosorting and recreational drug use are risk factors for diagnosis of genital infection with chlamydia
and gonorrhoea among HIV-positive men who have sex with men: results from a clinical cohort in Ontario, Canada. Sex Transm Infect. 2017;93:71–75.
17. Berry SA, Ghanem KG, Page KR, et al. Increased gonorrhoea and chlamydia
testing did not increase case detection in an HIV clinical cohort 1999–2007. Sex Transm Infect. 2011;87:469–475.
18. Berry SA. Gonorrhoea and chlamydia
screening in HIV clinics: time for new tools and targets. Sex Transm Infect. 2014;90:574–575.
19. Centers for Disease Control and Prevention. Sexually Transmitted Disease Surveillance 2015. Atlanta, GA: U.S. Department of Health and Human Services; 2016.
20. Yehia BR, Gebo KA, Hicks PB, et al. Structures of care in the clinics of the HIV research Network. AIDS Patient Care STDS. 2008;22:1007–1013.
21. Kahle E, Zhang Q, Golden M, et al. Trends in evaluation for sexually transmitted infections among HIV-infected people, King County, Washington. Sex Transm Dis. 2007;34:940–946.
22. Spaulding AB, Lifson AR, Iverson ER, et al. Gonorrhoea or chlamydia
in a US military HIV-positive cohort. Sex Transm Infect. 2012;88:266–271.
23. Teague R, Mijch A, Fairley CK, et al. Testing rates for sexually transmitted infections among HIV-infected men who have sex with men attending two different HIV services. Int J STD AIDS 2008;19:200–202.
24. Hutchinson J, Goold P, Wilson H, et al. Sexual health care of HIV-positive patients: an audit of a local service. Int J STD AIDS 2003;14:493–496.
25. John Snow International. HIVQUAL-US Performance Data Report: Ryan White Part C and Part D Funded Programs. 2011. Available at: http://nationalqualitycenter.org/files/hivqual-us-performance-data-report-2009-march-2-2012/
. Accessed February 26, 2017.
26. Carter JW Jr, Hart-Cooper GD, Butler MO, et al. Provider barriers prevent recommended sexually transmitted disease screening of HIV-infected men who have sex with men. Sex Transm Dis. 2014;41:137–142.
27. Dukers-Muijrers NH, Schachter J, van Liere GA, et al. What is needed to guide testing for anorectal and pharyngeal Chlamydia
trachomatis and Neisseria gonorrhoeae in women
and men? Evidence and opinion. BMC Infect Dis. 2015;15:533.
28. van der Helm JJ, Hoebe CJ, van Rooijen MS, et al. High performance and acceptability of self-collected rectal swabs for diagnosis of Chlamydia
trachomatis and Neisseria gonorrhoeae in men who have sex with men and women
. Sex Transm Dis. 2009;36:493–497.
29. Arias M, Jang D, Gilchrist J, et al. Ease, comfort, and performance of the HerSwab vaginal self-sampling device for the detection of chlamydia
trachomatis and neisseria gonorrhoeae. Sex Transm Dis. 2016;43:125–129.
30. Centers for Disease Control and Prevention. Sexually Transmitted Disease Surveillance 2008. Atlanta, GA: U.S. Department of Health and Human Services; 2009.
31. Short R, Gardner E, Blum J, et al. Prevalence of gonorrhea
infections among human immunodeficiency virus-infected men by anatomic site and presence or absence of symptoms. In: Open Forum Infectious Diseases. Vol 2. Oxford University Press; 2015:S14–S15. Available at: https://ofid-oxfordjournals-org.ezp-prod1.hul.harvard.edu/content/2/suppl_1/S14.3.full
. Accessed March 17, 2016.
32. Lutz AR. Screening for asymptomatic extragenital gonorrhea
in men who have sex with men: significance, recommendations, and options for overcoming barriers to testing. LGBT Health. 2015;2:27–34.
33. Mayer KH, O'Cleirigh C, Skeer M, et al. 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. Sex Transm Infect. 2010;86:66–70.
34. Cohen MS, Chen YQ, McCauley M, et al. Prevention of HIV-1 infection with early antiretroviral therapy. N Engl J Med. 2011;365:493–505.