The prevalence and epidemiology of anal intercourse (AI) and rectal sexually transmitted infections (STIs) are well characterized among men who have sex with men (MSM); however, less is known among women. A number of studies have examined AI among women and suggest that it is a commonly practiced behavior. In a recent national survey in the United States, up to 46% of women reported ever having AI,1 with estimates of recent experience with AI among women ranging from 10% to 22% of clients attending sexually transmitted disease (STD) clinics and 5% to 42% of substance using women.2–6 In one study, up to 18% of women responding to a population-based survey reported having AI a few times per year to monthly, with 4% reporting AI a few times per month.7 In studies of women at high risk for STIs where condom use was assessed, most of the women reported never using condoms for AI, suggesting increased likelihood of exposure to STIs, including human immunodeficiency virus (HIV).4,5 In fact, it has been estimated that approximately 7-times more women than men engage in unprotected receptive AI.8
Although there is increasing evidence of the significant prevalence of unprotected AI among women, very few data are available on the epidemiology of rectal STIs among women. This is largely because women are rarely tested for anorectal STIs. In recent studies of MSM, the prevalence of rectal chlamydia ranged from 4% to 9% and rectal gonorrhea from 7% to 9%.9–12 Interestingly, one of these studies noted that more than 53% of chlamydia infections and 64% of gonococcal infections would be missed if only urogenital sites were tested.9 In one of the few studies conducted in women, the prevalence of rectal chlamydia and gonorrhea was 17.5% and 13.4%, respectively.13 Although the authors noted that 6% to 34% of infections would be missed in the absence of rectal testing, the small number of women included in this study (n = 97) limited the extent of their analyses. In the two other studies that have been published to date, the prevalence of rectal gonorrhea was 7%, and the prevalence of rectal chlamydia ranged from 6% to 13%.14,15 Although these studies seem to indicate that rectal testing may be relevant in women, particularly among those who report AI, very little is known about the risk of rectal chlamydia and gonorrhea in women. Therefore, we sought to investigate the prevalence and correlates of rectal STIs among women attending public STD clinics in Los Angeles County. These data will not only help conceptualize the development of appropriate and effective prevention interventions aimed at reducing the acquisition of rectal STIs/HIV among women but may also inform future rectal screening guidelines for women.
MATERIALS AND METHODS
We conducted a retrospective, cross-sectional study among women attending public STD clinics in Los Angeles County, California. In these clinics, rectal screening guidelines for women were established in January 2008 such that all women reporting AI in the past 90 days (or longer if rectal symptoms were present) should be screened for rectal chlamydia/gonorrhea. Consequently, only women reporting AI were screened, and no testing was conducted among women who did not report AI. All women who were tested for these infections and who attended one of the twelve public STD clinics between January 2008 and December 2010 were eligible for inclusion in this study. The study was approved by the institutional review boards of the University of California Los Angeles and the Los Angeles County Department of Public Health.
Data Collection and Measurements
Existing clinic medical record and data collection systems were used to abstract study data. The STD clinic intake form, which is used as part of intake and risk assessment, was used to collect information on demographics, sexual practices, and other risk behaviors. The assessments were conducted by a nurse or other trained public health staff at the time of the clinic visit using face-to-face interviews. Specifically, clients were routinely questioned about the type of sexual contact in the past 90 days including vaginal, anal, and oral sex. In addition, clients reported whether in the past 12 months they (1) exchanged drugs or money for sex; (2) were incarcerated or had a sex partner who was recently incarcerated; (3) had sex with an injection drug user or a known HIV-positive person; and (4) reported substance use including cocaine, crack, heroin, marijuana, and methamphetamine.
Laboratory results for chlamydia and gonorrhea, including the source of the specimen (urine, cervical, vaginal, or rectal swab) were also collected. All women seen for new visits were routinely screened for urogenital chlamydia and gonorrhea (defined as having a positive, vaginal, or cervical specimen) using nucleic acid amplification testing technology (Aptima Combo 2; GenProbe, San Diego, CA). Chlamydia and gonorrhea rectal tests were also conducted using the GenProbe Aptima Combo 2 test after validation performed by the Los Angeles County Public Health Laboratory. The rectal gonorrhea test was validated first and became available in the clinics starting in January 2008 followed by validations studies for rectal chlamydia, which became available for use in the clinics in late 2008.
Descriptive statistics including mean, range, and frequency distributions were performed for all demographic and risk behavior characteristics. Given the differences in the epidemiology of chlamydia and gonorrhea by age, we stratified our analyses by age with separate analyses for women 25 years or younger and those 26 years or older. The specific cutoff of age 25 years was based on screening guidelines that recommend annual chlamydia testing of all sexually active women 25 years or younger.16 Differences between groups were evaluated using t tests and Mantel-Haenszel χ2 methods as appropriate. Because clients could have repeated visits during the 3-year study period, we used hierarchical regression models with generalized estimating equations to account for the within-subject correlations.17,18 Variables tested for inclusion in the multivariable models were based on univariate analyses or specified a priori as risk factors based on the existing literature. In addition, separate models were analyzed for each age group to determine whether the association between risk behaviors and rectal chlamydia and gonorrhea were modified across levels of age.
Characteristics of Study Population
Between January 2008 and December 2010, 34,585 visits were made by women. Anal intercourse status was assessed in 84% of these visits, with 12.2% (n = 3541) reporting AI in the past 90 days. Among this group, 59% (n = 2084) were tested for rectal chlamydia or gonorrhea and were included in this analysis. Furthermore, these visits were based on 1644 unique women, with the majority (86%) having had one visit during the 3-year study period. An additional 9% (n = 148) had only two visits, and 5% (n = 88) had three or more visits during the 3-year study period. The descriptive statistics described later and presented in Tables 1 and 2 refer to all visits made by these women. Given that not all women who reported AI were tested for rectal chlamydia or gonorrhea, we compared those who had a rectal swab with those who did not in terms of demographics and sexual risk behaviors such as transactional sex, history of incarceration, and substance use. With the exception of age, there was no difference between women who had a rectal swab and those who did not. Specifically, women in the younger age groups reporting AI were more likely to be tested for rectal chlamydia or gonorrhea compared with women in the older age groups (e.g., 64% of women 14–19 years vs. 54% of women ≥35 years; P < 0.01).
Among the 2084 visits by women included in this analysis, nearly 62% were 30 years or younger, with 48% identifying as African American, 33% as Hispanic, and 12% as white (Table 1). In the 12 months before their visit, 5% reported exchanging drugs or money for sex, 7% reported being incarcerated, and 2% reported a partner who was an injection drug user. In more than 40% of visits, women reported substance use in the past 12 months, which included marijuana, crack/cocaine, methamphetamine, and ecstasy.
Rectal Chlamydia and Gonorrhea Positivity
Urogenital and rectal chlamydia testing was conducted in 1203 visits by women during the study period. The overall percentage of tests positive for chlamydia was 16.0% (n = 193), with urogenital chlamydia being 12.0% and rectal chlamydia being 14.6% (Fig. 1). Among those positive, the majority were positive for chlamydia at both rectal and urogenital sites (63.2%, 122/193), and 25.4% (49/193) with chlamydia infections had a rectal but not urogenital infection. Rectal testing increased the number of chlamydia cases detected by 34% from 144 to 193 chlamydia cases. More rectal gonorrhea tests were conducted compared with rectal chlamydia, given that rectal gonorrhea testing was validated and available sooner than rectal chlamydia testing. The overall percentage of tests positive for gonorrhea in the 2026 visits in which women were tested at both urogenital and rectal sites was 4.0% (n = 81), with positivity for urogenital gonorrhea being 3.3% and rectal gonorrhea being 3.0% (Fig. 2). Among those positive for gonorrhea, more than half were positive for gonorrhea rectally and urogenitally (55.6%, 45/81), whereas 18.5% (15/81) of gonorrhea infections were rectal infections with no urogenital infection. Testing women for rectal gonorrhea increased the gonorrhea case finding by 22.7% from 66 to 81 gonorrhea cases.
We also found that rectal chlamydia or gonorrhea positivity varied by age, with the levels highest among those in the youngest age groups (Table 2). Furthermore, rectal STI positivity varied by behavioral risk factors. In STD clinic visits by young women (≤25 years), rectal chlamydia or gonorrhea was more prevalent based on reported sex partner characteristics. Specifically, visits in which women reported a recently incarcerated sex partner (21.1% vs. 15.3%, P = 0.05), a sex partner with injection drug use (46.5% vs. 15.5%, P < 0.01), or an HIV-positive sex partner (66.7% vs. 15.8%, P = 0.02) had a higher percent positivity for rectal chlamydia or gonorrhea. Likewise, the proportion of women visits with a positive rectal test result was higher among those with a concurrent urogenital infection as compared with those without a urogenital infection (54.2% vs. 6.6%, P < 0.01). In visits by women older than 25 years, no differences were noted in rectal chlamydia or gonorrhea percent positivity by sexual risk behaviors, except for substance use (Table 2). Specifically, 10.6% of women visits with reported substance use had a positive rectal chlamydia or gonorrhea test result as compared with 5.8% of visits in which substance use was not reported (P < 0.01). Similar to younger women, the proportion of positive rectal chlamydia or gonorrhea was higher in visits where a concurrent urogenital infection was identified (55.3% vs. 4.0%; P < 0.01).
Factors Associated With Rectal Chlamydia or Gonorrhea
On the basis of multivariable analyses, factors associated with rectal chlamydia or gonorrhea varied by age group (Table 3). Among women in the younger age group, after controlling for the presence of a concurrent urogenital chlamydia or gonorrhea infection, those who reported a sex partner with injection drug use were nearly five times as likely to test positive for rectal chlamydia or gonorrhea (adjusted odds ratio [AOR], 4.78; 95% confidence interval [CI], 1.02–22.45). Likewise, having an HIV-positive sex partner was also associated with rectal chlamydia or gonorrhea (AOR, 4.85; 95% CI, 1.02–22.93). Among women 26 years or older, after adjusting for a concurrent urogenital infection, those who reported substance use were more likely to have rectal chlamydia or gonorrhea as compared with those who did not report substance use (AOR, 1.77; 95% CI, 1.04–3.02).
Findings from this study indicate that rectal chlamydia and gonorrhea positivity among women who report AI is similar to that of urogenital infections. We also found that up to one third of cases—more so for chlamydia than gonorrhea—would be missed in the absence of rectal testing. Furthermore, the relatively large study population and high occurrence of rectal chlamydia and gonorrhea allowed us to further explore factors associated with these infections. To our knowledge, this is one of the first studies to report an independent association between sexual risk behaviors and rectal chlamydia and gonorrhea among women even after controlling for multiple other known risk factors for STIs. In addition, we were able to demonstrate that factors predictive of rectal STIs among women varied by age.
Consistent with the few studies that have been published thus far, we found that rectal chlamydia and gonorrhea positivity among women was comparable with that of urogenital infections.13–15 Previous studies have demonstrated the importance of extragenital testing among MSM, with evidence indicating that a third and as much as 64% of gonorrhea infections and 53% of chlamydia infections would be missed in the absence of rectal testing.9,19 In these studies, the prevalence of rectal-only infections was high, and the proportion of infections that were dual infections at both urethral and rectal sites were low. These findings are different from our study, which show a higher level of concordance between rectal and urogenital infections. This difference may partly be explained by sexual and risk behavior differences when comparing MSM with women but also anatomical differences, which limit the potential for spread of contaminated secretions and fluids from the urogenital site to the rectum. Although rectal testing data on women have been limited, in a study among women attending an STD clinic in San Francisco, rectal swabs were collected from women receiving a pelvic examination, regardless of whether they reported AI. In this study, the overall prevalence of rectal and urogenital chlamydia/gonorrhea was 6.0% and 6.7%, respectively, and rectal testing increased chlamydia and gonorrhea case finding by 14.8%, which is substantially lower than the 23% to 34% noted in our study.14 This difference is likely because the San Francisco study included women who did not report AI and were therefore at lower risk of rectal infection. Our findings support the author’s suggestion that the utility of rectal screening is likely to be higher in a population with a higher overall prevalence of chlamydia and gonorrhea.
In fact, the personal and public health benefits of rectal testing in women are unclear. First, although rectal infections among women may result from unprotected AI, it is possible that infected vaginal secretions may result in a false-positive rectal test result.20,21 Second, screening and treating women for urogenital tract infections with chlamydia and gonorrhea has been proven to reduce the incidence of pelvic inflammatory disease and other reproductive health sequelae such as ectopic pregnancy, infertility, and chronic pelvic pain.22–24 In contrast, the health benefit of rectal screening for women has yet to be determined. However, given that all the women in this study reported anal intercourse and many reported additional high-risk behaviors, testing and treating these women not only has implications in reducing HIV risk25,26 but in the absence of testing/treatment, the opportunity for chlamydia or gonorrhea transmission to partners and re-infection of these women seem great.
We also found that rectal chlamydia and gonorrhea positivity was higher among those who were younger, with positivity as high as 21.3% among those in the youngest age group. Furthermore, among those 25 years or younger, rectal positivity was significantly higher among women who had a sex partner who reported injection drug use or was HIV positive. The association remained even after controlling for the potential overlap in risk factors associated with having a urogenital infection. This finding is not surprising given that the prevalence of sexual risk behaviors and STIs are much higher among both injection drug users and those who are HIV positive.27–30 This suggests that women with rectal chlamydia or gonorrhea likely belong to sexual risk networks with very high STI and HIV transmission probabilities. Although none of the women in this study were HIV positive, these findings highlight the importance of rectal testing and stress the importance of specific counseling messages for women related to the risks associated with unprotected AI.
Our findings should be interpreted in light of some of the limitations of this study. Owing to the sensitivity of nucleic acid amplification testing, it is possible that some positive test results were not true rectal infections but rather were caused by cross contamination in women with urogenital chlamydia or gonorrhea. This would have resulted in a higher estimate of overall rectal disease prevalence but should not significantly impact the rectal-only disease prevalence nor its contribution to increased case finding. Assessment of AI and other sexual risk behaviors was based on self-report and assessed by clinic staff using face-to-face interview methods. Although this information was collected in the context of health care, interview-based data on socially stigmatized or illicit activities may suffer from reliability and validity issues. During an interview, patients may be reluctant to disclose information regarding sensitive, socially stigmatized, or illegal activities, resulting in response bias and a potential underestimation of these behaviors.31–33 Given that rectal swabs are only collected from women who report AI, the potential underreporting of AI may have biased our estimates of rectal chlamydia and gonorrhea. Furthermore, not all women reporting AI had a rectal swab collected. Although there were no differences in sexual risk behaviors, the difference in rectal testing by age may have also biased our estimates of rectal chlamydia and gonorrhea. Finally, this study was based on participants who attended public STD clinics and therefore may not be generalizable to other populations.
Our results indicate that levels of rectal chlamydia and gonorrhea among women at STD clinics who report recent AI are similar to that of urogenital infections. Furthermore, our findings highlight the fact that a relatively large number of infections in this population would be missed in the absence of rectal testing. We also found that women with rectal chlamydia or gonorrhea were more likely to report individual and sexual network characteristics that place them at high risk for continued transmission and acquisition of STIs including HIV. These results have implications for those who provide medical care to clients at STD clinics and highlight the need for rectal screening recommendations for women, specific patient counseling messages related to condom use for AI, the risks associated with unprotected AI and substance use, and the increased risk for the transmission or acquisition of HIV and other STIs.
1. Herbenick D, Reece M, Schick V, et al.. Sexual behavior in the United States: Results from a national probability sample of men and women ages 14–94. J Sex Med 2010; 7 (suppl 5): 255–265.
2. Gorbach PM, Manhart LE, Hess KL, et al.. Anal intercourse among young heterosexuals in three sexually transmitted disease clinics in the United States. Sex Transm Dis 2009; 36: 193–198.
3. Satterwhite CL, Kamb ML, Metcalf C, et al.. Changes in sexual behavior and STD prevalence among heterosexual STD clinic attendees: 1993–1995 versus 1999–2000. Sex Transm Dis 2007; 34: 815–819.
4. Koblin BA, Hoover DR, Xu G, et al.. Correlates of anal intercourse vary by partner type among substance-using women: Baseline data from the UNITY Study. AIDS Behav 2008; 14: 132–140.
5. Tian LH, Peterman TA, Tao G, et al.. Heterosexual anal sex activity in the year after an STD clinic visit. Sex Transm Dis 2008; 35: 905–909.
6. Javanbakht M, Guerry S, Gorbach PM, et al.. Prevalence and correlates of heterosexual anal intercourse among clients attending public sexually transmitted disease clinics in Los Angeles County. Sex Transm Dis 2010; 37: 369–376.
7. Herbenick D, Reece M, Schick V, et al.. Sexual behaviors, relationships, and perceived health status among adult women in the United States: Results from a national probability sample. J Sex Med 2010; 7 (suppl 5): 277–290.
8. Halperin DT. Heterosexual anal intercourse: Prevalence, cultural factors, and HIV infection and other health risks, Part I. AIDS Patient Care STDS 1999; 13: 717–730.
9. 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.
10. Ivens D, Macdonald K, Bansi L, et al.. Screening for rectal chlamydia infection in a genitourinary medicine clinic. Int J STD AIDS 2007; 18: 404–406.
11. Geisler WM, Whittington WL, Suchland RJ, et al.. Epidemiology of anorectal chlamydial and gonococcal infections among men having sex with men in Seattle: Utilizing serovar and auxotype strain typing. Sex Transm Dis 2002; 29: 189–195.
12. Cook RL, St George K, Silvestre AJ, et al.. Prevalence of chlamydia and gonorrhoea among a population of men who have sex with men. Sex Transm Infect 2002; 78: 190–193.
13. Hunte T, Alcaide M, Castro J. Rectal infections with chlamydia and gonorrhoea in women attending a multiethnic sexually transmitted diseases urban clinic. Int J STD AIDS 2010; 21: 819–822.
14. Barry PM, Kent CK, Philip SS, et al.. Results of a program to test women for rectal chlamydia and gonorrhea. Obstet Gynecol 2010; 115: 753–759.
15. Sethupathi M, Blackwell A, Davies H. Rectal chlamydia trachomatis infection in women. Is it overlooked? Int J STD AIDS 2010; 21: 93–95.
16. Workowski KA, Berman S. Centers for Disease Control and Prevention (CDC). Sexually transmitted diseases treatment guidelines, 2010. MMWR Recomm Rep 2010; 59: 1–110.
17. Liang KY, Zeger SL. Longitudinal data-analysis using generalized linear-models. Biometrika 1986; 73: 13–22.
18. Zeger SL, Liang KY, Albert PS. Models for longitudinal data— A generalized estimating equation approach. Biometrics 1988; 44: 1049–1060.
19. 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.
20. Kinghorn GR, Rashid S. Prevalence of rectal and pharyngeal infection in women with gonorrhoea in Sheffield. Br J Vener Dis 1979; 55: 408–410.
21. Quinn TC, Goodell SE, Mkrtichian E, et al.. Chlamydia trachomatis
proctitis. N Engl J Med 1981; 305: 195–200.
22. Cates W Jr, Wasserheit JN, Marchbanks PA. Pelvic inflammatory disease and tubal infertility: The preventable conditions. Ann N Y Acad Sci 1994; 709: 179–195.
23. Melly MA, Gregg CR, McGee ZA. Studies of toxicity of Neisseria gonorrhoeae
for human fallopian tube mucosa. J Infect Dis 1981; 143: 423–431.
24. Westrom L, Joesoef R, Reynolds G, et al.. Pelvic inflammatory disease and fertility. A cohort study of 1,844 women with laparoscopically verified disease and 657 control women with normal laparoscopic results. Sex Transm Dis 1992; 19: 185–192.
25. 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.
26. Royce RA, Sena A, Cates W Jr, et al.. Sexual transmission of HIV. N Engl J Med 1997; 336: 1072–1078.
27. Jenness SM, Neaigus A, Hagan H, et al.. Heterosexual HIV and sexual partnerships between injection drug users and noninjection drug users. AIDS Patient Care STDS 2010; 24: 175–181.
28. Cheng WS, Garfein RS, Semple SJ, et al.. Increased drug use and STI risk with injection drug use among HIV-seronegative heterosexual methamphetamine users. J Psychoactive Drugs 2010; 42: 11–18.
29. Scott KC, Philip S, Ahrens K, et al.. High prevalence of gonococcal and chlamydial infection in men who have sex with men with newly diagnosed HIV infection: An opportunity for same-day presumptive treatment. J Acquir Immune Defic Syndr 2008; 48: 109–112.
30. Torian LV, Makki HA, Menzies IB, et al.. HIV infection in men who have sex with men, New York City Department of Health sexually transmitted disease clinics, 1990–1999: A decade of serosurveillance finds that racial disparities and associations between HIV and gonorrhea persist. Sex Transm Dis 2002; 29: 73–78.
31. Catania JA, Gibson DR, Chitwood DD, et al.. Methodological problems in AIDS behavioral research: Influences on measurement error and participation bias in studies of sexual behavior. Psychol Bull 1990; 108: 339–362.
32. Fendrich M, Johnson TP, Sudman S, et al.. Validity of drug use reporting in a high-risk community sample: A comparison of cocaine and heroin survey reports with hair tests. Am J Epidemiol 1999; 149: 955–962.
33. Newman JC, Des JDC, Turner CF, et al.. The differential effects of face-to-face and computer interview modes. Am J Public Health 2002; 92: 294–297.