Chlamydia trachomatis and Neisseria gonorrhoeae infections are two of the most common bacterial sexually transmitted infections in the United States. In 2016, among women, there were more than 1 million cases of C trachomatis (657/100,000) and nearly 200,000 cases of N gonorrhoeae (121/100,000) reported.1 Currently, the U.S. Preventive Services Task Force and the Centers for Disease Control and Prevention recommend routine screening for both C trachomatis and N gonorrhoeae in all sexually active women aged 24 years and younger and in women 25 years or older who are at increased risk.2 Although screening recommendations for women focus on urogenital disease, C trachomatis and N gonorrhoeae infections may occur at extragenital sites, including the rectum, concurrently with or independent of genital infection.
Numerous studies have highlighted the importance of screening for C trachomatis and N gonorrhoeae infection in extragenital sites in addition to genital specimens in men who have sex with men.3–6 In a cohort of men who have sex with men tested in a network of U.S. sexually transmitted disease (STD) clinics, testing for only genital infections missed 70% of all prevalent C trachomatis and N gonorrhoeae infections in this population.5 Centers for Disease Control and Prevention recommendations include that clinicians use the patient-reported history of sexual exposure to guide site-specific screening (eg, C trachomatis and N gonorrhoeae rectal testing in men who report receptive anal intercourse during the preceding year).2 There are currently no recommendations for extragenital screening among women.
We aimed to examine the prevalence and treatment of rectal C trachomatis and N gonorrhoeae among women reporting receptive anal intercourse in a network of STD or sexual health clinics and estimate the proportion of missed infections if women were tested at the genital site only.
MATERIALS AND METHODS
This was a cross-sectional analysis using data from the STD Surveillance Network, a sentinel surveillance system comprised of 10 state and local health jurisdictions conducting facility-based surveillance in publicly funded, urban STD or sexual health clinics. Five of the 10 jurisdictions collect and transmit data on self-reported sexual practices among women and contributed data to this analysis: Baltimore, Los Angeles, Multnomah County, New York City, and Philadelphia. Each jurisdiction has between one and 12 STD clinics, which are operated directly by the jurisdiction and have their own protocol for rectal C trachomatis and N gonorrhoeae testing in women.
The data collected in the STD Surveillance Network include age, race, ethnicity, coinfection with human immunodeficiency virus (HIV; defined as documentation of a positive HIV antibody test or a self-reported history of HIV infection) as well as information on sexual risk behavior. Specifically, clients are asked about anatomic site(s) of sexual exposure and number and sex of sexual partner(s) in the previous 3 months. Results of nucleic acid amplification tests for C trachomatis and N gonorrhoeae and treatment are also recorded. Treatment data were analyzed by reviewing antibiotic drug and dose regimens prescribed within 3 weeks of specimen collection on or after the visit where they reported receptive anal intercourse.
We identified all visits from January 2015 to December 2016 in which a female patient reported receptive anal intercourse in the preceding 3 months. To minimize overrepresentation of women who presented for care multiple times, we included only the first visit at which rectal intercourse was reported in the analysis. For each visit, we determined whether there was a documented C trachomatis or N gonorrhoeae test on the visit in which receptive anal intercourse was reported and estimated anatomic site-specific testing coverage (eg, number of women for whom a rectal C trachomatis or N gonorrhoeae test was recorded/total number of women in whom receptive anal intercourse was reported). We estimated anatomic site-specific C trachomatis and N gonorrhoeae positivity (eg, number of positive rectal C trachomatis or N gonorrhoeae tests divided by the total number of positive or negative rectal C trachomatis or N gonorrhoeae tests); genital positivity was based on a positive result from a test conducted on an endocervical, vaginal, or urine specimen. We determined the proportion of rectal infections that would be missed if only genital screening was performed by calculating the number of women with a positive rectal-only test/total number tested at both the rectal and genital anatomic sites.
All laboratories serving the participating STD clinics completed verification studies per Clinical Laboratory Improvement Amendments specifications to demonstrate adequate nucleic acid amplification performance on rectal specimens. Only positive and negative nucleic acid amplification results were included in the overall analysis. Data analysis was performed using SAS 9.3. The STD Surveillance Network project was reviewed by the Centers for Disease Control and Prevention and was determined not to be research, so institutional review board review was not required.
Between January 2015 and December 2016, 94,094 visits were made by 50,785 women to STD clinics in the five jurisdictions included in this analysis. Visits when receptive anal intercourse was reported (n=4,245) were made by 3,743 unique women, or 7.4% of the total women presenting for care during the 2-year period. The majority (89.8%) of women had only one such visit during the 2-year observation period; 8.2% (n=307) of women had two visits when receptive anal intercourse was reported and 1.8% (n=74) had three to 10 visits when receptive anal intercourse was reported. The proportion of women who reported receptive anal intercourse varied across the five STD Surveillance Network jurisdictions: 572 (10.2%) in Baltimore, 690 (9.0%) in Los Angeles, 116 (8.8%) in Multnomah County, 487 (5.9%) in Philadelphia, and 1,878 (6.7%) in New York City. Nearly two thirds were older than 24 years of age, and almost half of the women were of black race (Table 1). Less than 1% (n=26) of the women were known to be living with diagnosed HIV and the majority (92%) reported only male sex partners (data not shown).
In the period of 2015–2016, 94.1% (n=3,523) of female patients were tested at the urogenital site for C trachomatis and 94.5% for N gonorrhoeae (Fig. 1). The overall proportion of women tested at the rectal site for C trachomatis and N gonorrhoeae was 76.9% (n=2,878). Testing at the rectal site for C trachomatis and N gonorrhoeae differed by jurisdiction, ranging from 49.1% to 91.4%. Among women tested only at the genital site, C trachomatis positivity was 9.1% (median 7.1%; jurisdiction range 4.4–12.1%) and N gonorrhoeae positivity was 5.4% (median 4.4%; jurisdiction range 0.0–7.1%). Less than 0.1% of the urogenital tests performed for C trachomatis or N gonorrhoeae had invalid results. Among women tested at the rectal site only, C trachomatis positivity was 26.7% (median 16.0%; jurisdiction range 0–41.7%) and N gonorrhoeae positivity was 6.1% (median 4.2%; jurisdiction range 0–17.0%). Less than 0.3% of the rectal tests performed for C trachomatis or N gonorrhoeae had invalid results.
Of the 3,743 women who reported receptive anal intercourse, the majority (n=3,585) were C trachomatis and N gonorrhoeae tested at the genital or rectal site. Although most women were tested for C trachomatis and N gonorrhoeae at the genital site, there were a few more women tested for N gonorrhoeae when compared with C trachomatis only (3,523 vs 3,536). The C trachomatis and N gonorrhoeae genital testing rate was near 90% or above across all age and race and Hispanic ethnicity groups (except for unknown race). However, there was considerable variation by STD Surveillance Network jurisdiction in the proportion of women tested at the rectal site when receptive anal intercourse was reported (Table 1).
In the subsample of women who were tested at both the genital and rectal sites for C trachomatis (n=2,818), 292 (10.4%) women with infections were identified. Of these 292 women, 61 (20.9%) were positive for genital C trachomatis-only infections, 171 (58.6%) were positive for C trachomatis at both the rectal and genital sites, and 60 (20.5%) were positive at the rectal site only (Fig. 1). Rectal testing increased the number of C trachomatis cases detected by 25.9% from 232 to 292 chlamydia cases.
In the subsample of women who were tested at both the genital and rectal sites for N gonorrhoeae (n=2,830), a total of 128 (4.5%) N gonorrhoeae infections were identified (Fig. 1). There were 31 (24.2%) women with genital N gonorrhoeae-only infections, 74 (57.8%) were positive for N gonorrhoeae at both the rectal and genital sites, and 23 (18.0%) were exclusively rectal infections. Rectal testing increased the number of N gonorrhoeae cases by 21.9% from 105 to 128 N gonorrhoeae cases.
The proportion of rectal infections in the group of women tested at both anatomic sites that would have been missed if only genital testing had been done could potentially be extrapolated to the women tested at the genital site only. From Figure 1, there were women who were C trachomatis tested (n=705) and for N gonorrhoeae (n=707) at the genital site only and, hence, there is no way to know precisely how many of these women would have tested positive for either pathogen at the rectal site. Assuming infection rates were the same among women reporting receptive anal intercourse (regardless of whether or not they had a rectal test), one can estimate how many of these women (urogenital testing only) would have been positive for a rectal-only infection had they been tested at the rectal and urogenital sites. In the case of C trachomatis, 60 of 2,818 women (95% CI 2.1%, 0.5–4.9%) were positive for C trachomatis rectal only and if applied to the women who were tested at the genital site only, presumably 4–34 more women might have had a rectal C trachomatis infection despite possibly being negative at the urogenital site. In the case of N gonorrhoeae, another 2–14 (95% CI 0.8%, 0.3–2.0%) more women might have had a rectal N gonorrhoeae infection identified.
Of the 247 women with rectal C trachomatis infections, 178 had documented treatment; 170 (68.8%) were treated with 1 g azithromycin (single dose) and eight (3.2%) were treated with oral doxycycline (100 mg twice daily for 14 days) within 21 days of a positive laboratory test. The majority (79%) were treated within 1 week of diagnosis. Treatment information was not available for the remaining 28.0% of the patients. The proportion treated with doxycycline and those treated with azithromycin did not significantly differ by anatomic site of infection (rectal only vs genital and rectal) (data not shown). Of the 100 women with rectal N gonorrhoeae infections, 74 (74.0%) were treated with 250 mg ceftriaxone and 1 g azithromycin within 21 days of a positive laboratory test; the majority (86%) were treated within 1 week of diagnosis. Treatment information was not available for the remaining 26.0% of the patients.
Using routinely collected STD clinic data, our analysis demonstrates a high proportion of rectal C trachomatis or N gonorrhoeae infections among women reporting anal sex, similar to the proportion with genital infections. Overall, 20.5% of C trachomatis rectal infections and 18.0% of N gonorrhoeae infections would have been missed and untreated by genital screening alone. Our findings are consistent with other studies that suggest that 20–40% of N gonorrhoeae infections and 10–25% of C trachomatis infections in women would be missed if rectal sites were not tested.7–14 Although STD clinics may routinely ask questions about receptive anal intercourse in clinical assessments, the practice of testing at the rectal sites in STD clinics varied considerably by jurisdiction.
One of the primary goals of routine screening for C trachomatis and N gonorrhoeae is to prevent long-term morbidity such as infertility and ectopic pregnancy in women. These sequelae usually result from genital infections ascending to the upper genital tract, explaining why testing efforts have traditionally focused on genital sites. However, rectal infections may affect upper genital tract disease by autoinoculation, a process in which the vaginal site is inoculated with an infection in the rectum.15,16 Although the contribution of this suspected transmission has yet to be quantified, more research is needed to gain insight into the relevance of rectal infections in women in terms of sequelae. Even without obvious associated morbidity, it remains important to identify missed rectal infections that can spread to male sex partners who pose additional risk to their female partners.
Missed rectal infections in women is also problematic for prevention messages, especially given that receptive anal intercourse is a relatively common practice among heterosexual populations. In a recent nationally representative survey of more than 10,000 men and women in the United States, approximately 13.2% of women aged 15–44 years reported heterosexual anal intercourse in the year before the survey, with women aged 20–29 reporting the highest prevalence at 15.9%.17 In 2008, a study conducted in three public STD clinics reported 18.7% of women had heterosexual receptive anal intercourse in a given 3-month interval.18 Receptive anal intercourse is also a highly efficient mode of HIV transmission because it is associated with higher rates of HIV transmission than vaginal intercourse.19,20 Previous studies have also reported condom use with receptive anal intercourse among heterosexuals is frequently low.18,21–23 The practice of anal sex is often discussed in the context of homosexuality but remains underreported and often associated with stigma among women who report this practice.24 Public health research on women's engagement in receptive anal intercourse remains relatively scarce, resulting in a missed opportunity to advance the field of women's sexual health and in controlling the spread and sequelae of STDs and preventing HIV.
Our study has important limitations. First, our findings may not be generalizable to all female STD clinic attendees or the general female population. Second, the design of our study deliberately selected women reporting receptive anal intercourse, potentially missing women with rectal infections who did not report receptive anal intercourse and underestimating the prevalence of rectal C trachomatis and N gonorrhoeae. Third, previous investigators have suggested the possibility that rectal C trachomatis and N gonorrhoeae in women represent false-positive results or cross-contamination or both.15,25,26 Although concordance between results of genital and rectal testing in women is strong, given our observed findings, a sizeable proportion is positive for rectal infection while simultaneously negative at the genital site. This would argue for more screening at the rectal site, even among women attending STD clinics who do not report receptive anal intercourse. Lastly, there were no data available for condom use or rectal symptoms to stratify positivity by screening compared with diagnostic testing.
Our data reveal that a sizeable burden of C trachomatis and N gonorrhoeae infections would have been missed and untreated if only genital testing was performed, supporting rectal screening among women reporting receptive anal intercourse seeking care in STD clinics. Future studies describing the clinical consequences of rectal C trachomatis and N gonorrhoeae infections and the cost–benefit of rectal screening are needed to inform future sexually transmitted infection screening guidelines. Although our data might not have included a low-risk heterosexual population, nationally representative data suggest that receptive anal intercourse is common among sexually active women, including those not seen in STD clinics. Unprotected receptive anal intercourse with an infected partner can present a risk for HIV and sexually transmitted infection acquisition, underscoring the importance of discussing receptive anal intercourse and its risks to patients in various health care settings, particularly among settings with a focus on women's health.
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