This study was conducted in a group of high-risk young adults recruited into a cohort study in preparation for HIV-1 vaccine trials and therefore selected on the basis of their high-risk behaviors, including commercial sex work. In this population, the burden of untreated STIs identified at enrolment was relatively high, even with the use of limited screening methods. Not surprisingly, basic microscopic examination of vaginal, cervical, urethral and rectal secretions identified a large number of STIs in persons not complaining of discharge, who would not normally have been treated using a syndromic approach. Limitations of the syndromic approach are widely recognized [7
], especially for the detection of cervicitis, which is often asymptomatic in women [15
]. We found that both vaginal trichomoniasis and urethritis would also have been frequently missed if symptoms alone were used to identify STIs in our cohort. Microscopy also allowed us to avoid treating all women with vaginal discharge and a positive STI risk assessment for cervicitis, as recommended by WHO syndromic treatment guidelines in the absence of microscopy [7
]. This practice leads to increased cost and the potential for adverse effects and drug resistance [12
]. Therefore, we conclude that the addition of basic microscopy can be a valuable intervention in adults who are identified for cohort recruitment based on their presumed higher risk for HIV-1 infection.
Clearly, additional cases of STI would have been identified by expanded screening, including culture for T. vaginalis
and N. gonorrheae
or nucleic acid amplification testing (NAAT) for N. gonorrheae
and C. trachomatis
. For example, the prevalence of gonococcal cervicitis was 5% at enrolment into a Mombasa-based female sex worker cohort in which culture has been routinely available [16
]. Using only microscopy in our cohort, we found no cases of gonococcal cervicitis by Gram stain alone. In a recent circumcision trial of mostly heterosexual Kenyan men, NAAT testing identified gonococcal urethritis in 2% of participants, and C. trachomatis
in 5%; T. vaginalis
was detected by culture in 2% [6
]. We found a 1% prevalence of gonococcal urethritis by Gram stain alone, and were unable to identify C. trachomatis
or T. vaginalis
infections. Because herpes simplex infection is an important cause of GUD and increases the risk of HIV-1 transmission [17
], specific testing for HSV-2 infections would also be valuable for counseling and patient management purposes. While our data demonstrate that even low-cost microscopy can have considerable value in high-risk populations, expanded screening would be needed to estimate the prevalence of specific infectious etiologies and further reduce the STI burden in our study population.
Several reports have shown that anal intercourse in both men and women may be more common than was previously thought in sub-Saharan Africa [18
]. Despite strong local convictions that MSM behaviour, in particular, is incompatible with traditional African culture, recent studies in Senegal and Kenya have proven otherwise [8
]. Ferguson and Morris have stressed the importance of specific, carefully worded questions to assess the occurrence of anal intercourse in women [23
]. Both recall and social desirability bias may influence responses; in a South African coital diary study, FSWs reported a total of 5 anal sex acts per week compared to only 1 anal act per week when responding to a recall questionnaire [24
]. Despite increasing evidence that anal intercourse is an important and not uncommon risk factor for HIV/AIDS, questions on RAI initially included in the recently conducted national AIDS indicator survey in Kenya were rejected as being too offensive to ask (Larry Marum, personal communication). Unfortunately data on the general population practice of anal sex in Kenya remains elusive. In our high-risk cohort, we found that men and women frequently reported RAI in the previous three months. Frequency of condom use was lower for anal intercourse than for vaginal intercourse, as reported in previous African studies [22
]. The majority of women reporting RAI were sex workers, but other women did report this practice. Sex workers report receiving higher payment for RAI versus vaginal intercourse (unpublished observation); in addition, some women may use RAI as a form of birth control or to avoid vaginal sex during menstruation. Given that anal sex is not uncommon among high-risk adults, we recommend that STI screening include questions on RAI and the diagnosis of proctitis when symptoms are present; this is particularly important in research settings and programs aiming to reduce the risk of HIV-1 acquisition.
Unprotected RAI is reported to be the most efficient mode of sexual transmission of HIV among both MSM and heterosexual couples [26
], and increasing attention has recently been drawn to the role anal intercourse plays in HIV-1 transmission in sub-Saharan Africa [8
]. We have, like others, presented evidence that African MSM are at higher risk of HIV-1 infection [8
]. In our cohort men who practiced RAI had a higher HIV-1 prevalence risk than those practicing only insertive anal intercourse [8
]. Among women in our cohort, RAI was not associated with prevalent HIV-1 infection, but women practicing RAI were more likely to have syphilis. It is not clear why this difference was found, although possibilities include differences in syphilis or HIV-1 prevalence among insertive partners, differences in condom use or sexual practices not captured by our questionnaires, or different biologic susceptibilities between men and women. Questions about RAI have not been routinely included in studies of syphilis risk factors in African women [32
], and our research suggests that such questions are an important component of a sexual risk assessment in general.
Our STI screening program was conducted in the context of a large, multicenter HIV-1 cohort study aiming to recruit high-risk adults in preparation for HIV-1 vaccine trials. Study findings challenge general approaches to recruiting at-risk adults. First, to identify volunteers at the highest risk for HIV-1 infection, it may be preferable to inquire about specific sexual behaviour rather than rely on transactional sex, numbers of partners, and condom use as the sole indicators. Second, volunteers reporting recent anal sex may harbor anal infections that should be managed appropriately for public health reasons. Recent guidelines on the management of proctitis recommend proctoscopy and collection of Gram stain for all people reporting anal receptive intercourse [34
]. Third, HIV-1 prevention studies will target vulnerable and socially isolated people who lack access to appropriate health care. Since STI treatment can reduce both the risk of HIV-1 acquisition and transmission [36
], the incorporation of STI screening into prevention studies not only provides benefit to research participants, but also to the communities at large. Lastly, populations at higher risk of HIV-1 infection are increasingly more difficult to identify and retain, especially in areas in Africa where general population HIV-1 prevalence and incidence are declining [1
]. STI screening and treatment may aid in the retention of volunteers — the crux of any intervention study. We have not presented data on incident STI in this paper, nor have we been able to assess the optimal period for repeat STI screening in this population. Further research into optimal STI screening procedures, in particular for screening of persons practicing RAI, is clearly needed.
In conclusion, adults with high-risk sexual behavior are at increased risk of both HIV-1 and other STIs, and may have a substantial burden of untreated STI upon entry into research studies. Basic microscopy is a valuable, low-cost component of STI screening that can identify asymptomatic infections and avoid overtreatment of STIs based on non-specific symptoms. Soliciting a history of RAI in high-risk persons is important to identify persons in need of intensified risk reduction counseling. Further research into appropriate methods for proctitis screening in developing countries would add to the value of such screening. We believe that improving STI screening should be integrated into HIV-1 prevention research targeting high-risk populations, as an important service to participants and their communities.