In many countries, the prevalence of bacterial sexually transmissible infections (STIs) such as gonorrhea, chlamydia, and syphilis is high among men who have sex with men (MSM).1 – 4 STIs in MSM are of particular public health importance because of their potential to increase human immunodeficiency virus (HIV) transmission. Recent studies have demonstrated associations between chlamydia, gonorrhea, and syphilis infection and HIV seroconversion.5,6
More frequent screening for bacterial STIs has the potential to improve detection of these largely asymptomatic infections, interrupting transmission and improving control. For HIV-infected men, the detection and treatment of other STIs could potentially reduce onward transmission of HIV. Guidelines in a number of countries call for regular screening of MSM. For example, US and Australian guidelines recommend that all MSM be screened for urethral and rectal chlamydia, pharyngeal and rectal gonorrhea, syphilis, and HIV at least once a year, with 3 to 6 monthly screening of higher-risk MSM.7,8 However, available data suggest that the rate of screening for these infections among MSM is low in many countries.9 – 12 Barriers to clinicians performing and men undertaking screening for STIs have been identified and include clinicians' lack of awareness and skills to undertake STI screening, as well as perceptions among some MSM that STIs are less serious than HIV.13,14
To help inform strategies that clinical services can use to help increase STI screening of MSM, we undertook a systematic review to identify clinic-based interventions efficacious at increasing screening and detection of gonorrhea, chlamydia, and syphilis among MSM.
We conducted a systematic review by searching MEDLINE for studies between 1990 and June 2011 using the following key words and variations: “men who have sex with men” or “MSM” or “gay” or “homosexual” or “bisexual”; and “syphilis” or “chlamydia” or “gonorrhea” or “gonorrhoea” or “sexually transmitted disease” or “STD” or “sexually transmitted infection” or “STI”. Only English language publications were included. Reference lists of selected studies were also checked for other potentially relevant studies.
A publication was considered for inclusion if it reported on the evaluation of a clinic-based intervention aimed at increasing bacterial STI screening rates (proportion of men screened); rescreening rates (proportion of men screened again); or detection rates (proportion of men tested diagnosed with an infection) in MSM, and if it included a control group or control period.
Studies were excluded if they did not include a control group or control period; reported screening rates in the absence of a specific intervention; involved STI screening outside of clinics such as outreach services and online testing services; focused on partner notification for STIs; or were studies designed to increase the sensitivity of laboratory testing methods in MSM populations, for example, studies comparing the use of nucleic acid amplification testing with culture.
For each study that met the inclusion criteria, information was extracted on the study setting, target population, study design, nature of the intervention, comparison periods, outcomes, sample size, and statistical methods used. We also calculated crude odds ratios (ORs) based on data from the studies where these were available in the published paper.
We conducted a frequency analysis of information related to the clinic (location, type), intervention type, and evaluation methods (sample size, design, period of the evaluation, and reported outcomes).
The primary outcome for each study was the screening rate, rescreening rate, and/or detection rate for individual STIs where data on individual STIs were provided. Otherwise, we cite summary figures with more than 1 STI included.
For each study, we abstracted the OR indicating the proportion tested in the intervention group compared with controls. For studies that did not provide an OR, we calculated the OR using STATA 11 (StataCorp, College Station, TX), including 95% confidence intervals, if the necessary figures were provided in the paper.
Overview of Studies and Interventions
The results of the search are summarized in Figure 1. We identified 1809 papers, with 8 satisfying the inclusion criteria.13,15 – 21 The studies with the effects of their various interventions are summarized in Table 1. The studies were conducted in Australia (n = 6), the United States (n = 1), and the United Kingdom (n = 1). Six studies reported screening rates as a primary outcome,13,15,17,19 – 21 with an additional study focused on rescreening.17 A further study examined serological follow-up for syphilis after syphilis treatment.16 This study was included because of the potential for repeat serology to identify reinfections with syphilis. Three studies reported screening data on all 3 STIs (gonorrhea, chlamydia, and syphilis),13,18,19 1 reported on gonorrhea and chlamydia only,15 and 4 reported on syphilis only.16,17,20,21 In 2 studies, infections were described by anatomical site.13,15
All studies reported using a retrospective, observational design with a control period. One study also used a concurrent comparison group,18 and the remaining 7 a historical comparison group. Three studies included HIV-positive men only,17,19,20 1 included HIV-negative men only,18 and 4 included both HIV-positive and HIV-negative men.
Four studies aimed at increasing screening for gonorrhea and chlamydia, with or without syphilis (Table 1).13,15,18,19 A further 4 studies focused on syphilis screening, detection, or serological follow-up (Table 2).16,17,20,21 Four studies evaluated the use of interventions that used newer technologies.15,16,18,21 Hotton et al16 evaluated the use of an electronic medical record system in a US primary care clinic to enhance serological follow-up after treatment for syphilis. In this intervention, all clinical, laboratory, and diagnostic data were stored electronically in the electronic record. The record allowed disease intervention specialists to generate reminders for themselves to contact patients for follow-up syphilis screening. Specialists created a flag at the time of diagnosis or treatment, which triggered a reminder message in the record for the specialist to contact patients so they would return to the clinic for retesting. Lister et al15 examined the use of a computer alert on an electronic medical record to remind clinicians in an STI clinic to screen for gonorrhea and chlamydia during clinical consultations. The clinic routinely collected clinical information on a computerized system during consultations, which included history of sex partners in the prior 12 months. If a male client had 1 or more male sex partners in the previous 12 months, this clinical information triggered the computer reminder during a clinical consultation. In the same STI clinic, Bissessor et al21 assessed the effect of a computer alert on an electronic medical record to remind clinicians to undertake 3-monthly syphilis testing of MSM with ≥10 male partners in the prior 12 months. Here, entry of ≥10 male partners triggered an alert to screen higher-risk MSM for syphilis 3-monthly during the consultation. In a study by Bourne et al,18 SMS (short text messaging) reminders for repeat STI screening were sent to men after an initial consultation at an STI clinic. In this intervention, an SMS reminder template was added to the patient electronic database and clinicians were encouraged to offer SMS reminders for 3- to 6-monthly HIV/STI retesting to MSM tailored to their level of risk.
In 4 other studies, STI screening was linked to other clinical activities with the aim of boosting STI testing. Cohen et al17 examined the effect of regular serological screening for syphilis during routine HIV care with the aim of detecting asymptomatic syphilis infections. Bissessor et al20 determined the impact of including syphilis serology with blood tests performed as part of routine HIV monitoring. By default, a request for syphilis serology was automatically included on all pathology request forms used in the HIV clinic for the monitoring of HIV-positive patients. Ryder et al13 assessed the impact of the introduction of clinic guidelines recommending at least annual STI screening of MSM in an STI clinic. Botes et al19 examined the effect of including STI screening with anal cytologic screening. In this intervention, STI testing was offered to MSM taking part in an anal cytologic screening program.
Impact of Interventions
Increases in screening, rescreening, or detection of selected bacterial STIs were seen in all 8 studies (Tables 1 and 2). In the evaluation by Hotton et al, use of an electronic medical record reminder to specialists improved syphilis retesting rates at 6 months from 64% to 81% (P = 0.047).16 Lister et al found that a computer alert on an electronic medical record that reminded doctors to screen MSM for gonorrhea and chlamydia during consultations significantly increased screening for these 2 infections from 78% to 83% (P = 0.023).15 In the study by Bissessor et al, use of a computer alert on an electronic medical record that reminded clinicians during consultations to undertake 3-monthly syphilis testing of higher-risk MSM increased the proportion of high-risk MSM screened for syphilis from 77% to 89% (P < 0.001) and the proportion of early syphilis detected that was asymptomatic from 16% to 53% (P < 0.001).21 Bourne et al found that an SMS reminder for repeat STI screening after an STI consultation increased rescreening from 31% (P < 0.001) in the pre-intervention group and 30% (P < 0.001) in the concurrent comparison group to 64% in the intervention group.18
In their study, Cohen et al demonstrated that regular serological screening for syphilis during routine HIV care increased the proportion of HIV-positive individuals screened for syphilis from 3% to 85% (P value not available).17 In the study by Bissessor et al, where syphilis serology was included with blood tests performed as part of routine HIV monitoring, there was an increase in the median number of syphilis tests performed in the prior 12 months from 1 to 2 and an increase in the proportion of early syphilis detected that was asymptomatic (21%–85%, P < 0.001). There was also a significant decrease in the median time between the midpoint since last syphilis serology and detection: from 107 to 45 days (P = 0.018).20 Ryder et al found that the introduction of clinic guidelines recommending at least annual STI screening of MSM increased screening for gonorrhea, chlamydia, and syphilis from 43% to 61% (P < 0.001).13 In the study by Botes et al, screening for gonorrhea, chlamydia, and syphilis increased from 20% to 35% (P < 0.001) when STI screening was undertaken with anal cytologic screening.19
To our knowledge, this is the first systematic review of clinic-based interventions aimed at increasing the screening and detection of bacterial STIs among MSM. Although there are many published studies of STI prevalence among MSM, there are few data measuring STI screening rates in MSM, and even fewer studies that have specifically assessed the efficacy of clinic-based strategies aimed at improving STI screening in this population. Of the small number of studies that were identified, which used a range of intervention, all demonstrated an increase in screening rates for selected bacterial STIs including gonorrhea and chlamydia, with 2 studies showing increased detection of asymptomatic, early syphilis.17,20,21
There are limitations to this review and to the studies included. First, and perhaps the most important, all studies discussed in this review compared data before and after an intervention: none were randomized controlled trials. Therefore, it is difficult to know whether the increases in screening and/or detection rates seen were entirely a result of the interventions or to some extent a result of other unmeasured factors. Second, we did not search the gray literature such as conference abstracts; thus, it is possible that some evaluations were not identified, particularly those with negative outcomes. Third, the extent to which the specific interventions would be effective in different populations of MSM and different clinical services is unknown. Owing to the heterogeneity of the interventions and the various outcomes, we were unable to pool the outcomes to determine a summary effect. Nevertheless, most of the studies were conducted in specialist sexually transmitted disease or HIV clinics where awareness of and screening rates for STIs were presumably already high; yet, further improvements in screening were seen. In clinical settings where awareness among health care providers and STI screening rates among MSM is low, the potential for greater impact with the various measures used would presumably be even greater.
Although the strategies aimed at improving STI screening among MSM varied substantially, several included the application of newer technologies such as the use of electronic medical record systems that incorporated alerts for clinicians during consultations or reminders for clinicians to undertake subsequent retesting. In 1 study, the alert resulted in a more comprehensive range of tests being undertaken, with chlamydia and gonorrhea screening of all recommended anatomical sites (rectal, pharyngeal, and urine) increasing from 41% to 83%.15 Computer alerts have also been shown to improve HIV screening in Veteran Affairs clinics in the United States,22 chlamydia screening rates among young women attending Australian general practice clinics, and practice in other disciplines such as measurement of blood pressure,23 vaccination,24 – 26 and prescription of medications.27 In addition to the use of alerts and reminders, electronic medical record systems that include electronic ordering of laboratory tests allow predefined sets of tests to be ordered together by default. This would potentially increase completeness of testing, for example, to ensure pharyngeal, urine, anal, and serological specimens are taken concurrently, and linkage of STI testing with other clinical activities, such as HIV monitoring of HIV-positive MSM. Once established, such electronic alerts, reminders, and links require minimal staffing or ongoing costs.
In one of the studies included in this review, SMS messages increased rescreening for STIs. SMS reminders are relatively cheap, and the acceptability of SMS reminders has been demonstrated in the sexual health context.28,29 SMS or e-mail reminders for STI screening can be offered and automatically sent to patients attending STI clinics through routine clinical use of computer-assisted self-interview. Furthermore, in settings where laboratory results are incorporated into the electronic record, SMS reminders to patients for repeat STI testing could be sent automatically after receipt of an initially positive laboratory result.
Overall, the results of the studies included in this review suggest that screening for and detection of bacterial STIs in MSM can be improved in clinical settings using a range of approaches. Some of the interventions identified in this review would have modest operating costs and require limited staffing to maintain once established.18 Wider adoption of these interventions and the development of innovative interventions appear to be warranted. Future randomized studies should examine the use of multifaceted approaches that combine several different interventions including the application of new technologies.
1. Public Health Laboratory System. Increased transmission of syphilis in Brighton and Greater Manchester among men who have sex with men. Commun Dis Rep CDR Wkly 2000; 10:383–386.
3. Vodstrcil LA, Fairley CK, Fehler G, et al.. Trends in chlamydia and gonorrhea positivity among heterosexual men and men who have sex with men attending a large urban sexual health service in Australia, 2002–2009. BMC Infect Dis 2011; 11:158.
4. Workowski KA, Berman S. Sexually transmitted diseases treatment guidelines, 2010. MMWR Recomm Rep 2010; 59:1–110.
5. Bernstein KT, Marcus JL, Nieri G, et al.. Rectal gonorrhea and chlamydia reinfection is associated with increased risk of HIV seroconversion. J Acquir Immune Defic Syndr 2009; 53:537–543.
6. Jin F, Prestage GP, Zablotska I, et al.. High rates of sexually transmitted infections in HIV positive homosexual men: Data from two community based cohorts. Sex Transm Infect 2007; 83:397–399.
7. Centers for Disease Control and Prevention. Outbreak of syphilis among men who have sex with men—Southern California. MMWR 2001; 50:117–120.
9. Lister NA, Smith A, Read T, et al.. Testing men who have sex with men for Neisseria gonorrhoeae
and Chlamydia trachomatis
prior to the introduction of guidelines at an STD clinic in Melbourne. Sex Health 2004; 1:47–50.
10. Donovan B, Bodsworth NJ, Rohrsheim R, et al.. Characteristics of homosexually active men with gonorrhoea during an epidemic in Sydney, Australia. Int J STD AIDS 2001; 12:437–443.
11. Gunn RA, O'Brien CJ, Lee MA, et al.. Gonorrhea screening among men who have sex with men: Value of multiple anatomic site testing, San Diego, California, 1997–2003. Sex Transm Dis 2008; 35:845–848.
12. McMillan A, Kell P, Ward H. Diagnosing chlamydia and managing proctitis in men who have sex with men: Current UK practice. Sex Transm Infect 2008; 84:97–100.
13. Ryder N, Bourne C, Rohrsheim R. Clinical audit: Adherence to sexually transmitted infection screening guidelines for men who have sex with men. Int J STD AIDS 2005; 16:446–449.
14. Holt M, Bernard D, Race K. Gay men's perceptions of sexually transmissible infections and their experiences of diagnosis: “Part of the way of life” to feeling “dirty and ashamed.” Sex Health 2010; 7:411–416.
15. Lister NA, Smith A, Fairley CK. Introduction of screening guidelines for men who have sex with men at an STD clinic, the Melbourne Sexual Health Centre, Australia. Sex Health 2005; 2:241–244.
16. Hotton AL, Gratzer B, Pohl D, et al.. Factors associated with repeat syphilis testing at a large urban LGBT health clinic: Chicago, IL 2002–2008. Sex Transm Dis 2010; 38:205–209.
17. Cohen CE, Winston A, Asboe D, et al.. Increasing detection of asymptomatic syphilis in HIV patients. Sex Transm Infect 2005; 81:217–219.
18. Bourne C, Knight V, Guy R, et al.. Short message service reminder intervention doubles sexually transmitted infection/HIV re-testing rates among men who have sex with men. Sex Transm Infect 2011; 87:229–231.
19. Botes LP, McAllister J, Ribbons E, et al.. Significant increase in testing rates for sexually transmissible infections following the introduction of an anal cytological screening program, targeting HIV-positive men who have sex with men. Sex Health 2011; 8:76–78.
20. Bissessor M, Fairley CK, Leslie D, et al.. Frequent screening for syphilis as part of HIV monitoring increases the detection of early asymptomatic syphilis among HIV-positive homosexual men. J Acquir Immune Defic Syndr 2010; 55:211–216.
21. Bissessor M, Fairley CK, Leslie D, et al.. Use of a computer alert increases detection of early, asymptomatic syphilis among higher-risk men who have sex with men. Clin Infect Dis 2011; 53:57–58.
22. Goetz MB, Hoang T, Bowman C, et al.. A system-wide intervention to improve HIV testing in the Veterans Health Administration. J Gen Intern Med 23 2008; 1200–1207.
23. McDowell I, Newell C, Rosser W. A randomized trial of computerized reminders for blood pressure screening in primary care. Med Care 1989; 27:297–305.
24. Dexter PR, Perkins S, Overhage JM, et al.. A computerized reminder system to increase the use of preventive care for hospitalized patients. N Engl J Med 2001; 345:965–970.
25. Rosser WW, Hutchison BG, McDowell I, et al.. Use of reminders to increase compliance with tetanus booster vaccination. CMAJ 1992; 146:911–917.
26. McDowell I, Newell C, Rosser W. Comparison of three methods of recalling patients for influenza vaccination. CMAJ 1986; 135:991–997.
27. Koide D, Ohe K, Ross-Degnan D, et al.. Computerized reminders to monitor liver function to improve the use of Etretinate. Int J Med Inform 2000; 57:11–19.
28. Lim MS, Hocking JS, Hellard ME, et al.. SMS STI: A review of the uses of mobile phone text messaging in sexual health. Int J STD AIDS 2008; 19:287–290.
© Copyright 2012 American Sexually Transmitted Diseases Association
29. Lim MS, Sacks-Davis R, Aitken CK, et al.. Randomised controlled trial of paper, online and SMS diaries for collecting sexual behaviour information from young people. J Epidemiol Community Health 2010; 64:885–889.