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Original Studies

Chlamydia, Gonorrhea, and Human Immunodeficiency Virus Infection Among Transgender Women and Transgender Men Attending Clinics that Provide Sexually Transmitted Disease Services in Six US Cities: Results From the Sexually Transmitted Disease Surveillance Network

Pitasi, Marc A. MPH*; Kerani, Roxanne P. PhD; Kohn, Robert MPH; Murphy, Ryan D. PhD, MPH§; Pathela, Preeti DrPH, MPH; Schumacher, Christina M. PhD; Tabidze, Irina MD, MPH**; Llata, Eloisa MD, MPH*

Author Information
doi: 10.1097/OLQ.0000000000000917

Transgender populations are disproportionately affected by human immunodeficiency virus (HIV) infection and may be similarly vulnerable to other sexually transmitted disease (STDs), but HIV and STD risk among transgender persons remain understudied. Transgender women (people assigned male sex at birth who identify as women, transgender women, or another transfeminine identity) are particularly vulnerable to HIV,1 with prevalence estimates as high as 39.5%.2 A meta-analysis of 9 studies that assessed HIV infection burden found that transgender women in the United States had over 34 times the odds of HIV infection compared with all adults of reproductive age.3 Many transgender women experience socioeconomic and structural barriers that lead to increased HIV risk and poorer disease outcomes among those who are infected.4 These barriers include stigma and discrimination,5 poverty and unemployment,2,6 and lack of access to culturally competent health care.7,8 Despite these known inequities, transgender women remain an underserved population with a paucity of evidence-based interventions tailored to their unique needs.

Less is known about HIV and STD risk among transgender men (people assigned female sex at birth who identify as men, transgender men, or another transmasculine identity).9 Most studies of transgender men have been limited to small convenience samples with HIV prevalence of 0% to 3%10,11; this has led to the widespread assumption that transgender men are not at high risk for HIV infection.9,12,13 However, emerging evidence suggests that transgender men who have sex with cisgender men (ie, those whose gender identity is the same as their sex assigned at birth) represent an important subgroup with higher HIV risk.13,14 Transgender men experience the same forms of marginalization experienced by transgender women, such as stigma and discrimination.15 Sexual risk behaviors are poorly understood among transgender men,9 but some studies report high frequencies of certain risk behaviors (eg, recent unprotected sex,16 multiple past-year sex partners17), similar to transgender women.

Compared with HIV, bacterial STDs such as Chlamydia trachomatis (CT) and Neisseria gonorrhoeae (GC) remain particularly understudied in the transgender population. Extragenital (ie, rectal and pharyngeal) infections among transgender populations are poorly understood despite the evidence of rectal infections as a potential marker of HIV risk18 and studies demonstrating large proportions of both transgender women and transgender men in certain settings reported receptive anal sex.17,19,20 Because extragenital infections are frequently asymptomatic,21 and extragenital screening rates among transgender persons are largely unknown, more information is needed about the epidemiology of extragenital infections in this population.

Few national population-based surveys have been able to collect data from a representative sample of the US transgender population. Public health surveillance systems based on reported cases of disease have been unable to reliably ascertain gender identity. Clinic-based data derived from medical charts, electronic health records, or other clinical sources thus remain one of the few sources of information about laboratory-confirmed HIV and other STDs in the transgender population. Previous studies have demonstrated the utility of clinic-based data in describing health outcomes among transgender people seeking care.22 The objective of this analysis was to characterize the demographics of transgender women and transgender men and describe the proportion with HIV, CT, and GC infections by anatomic site in a network of geographically diverse STD clinics and other clinics that provide STD services in the United States.

METHODS

We analyzed data from the STD Surveillance Network (SSuN), a sentinel surveillance system that conducted surveillance in 42 urban, publicly funded clinics providing STD services in 12 state and local health jurisdictions in collaboration with the Centers for Disease Control and Prevention (CDC).23 Deidentified demographic, clinical, and laboratory data from the medical records of all patients attending participating clinics were transmitted to CDC as part of routine surveillance. This analysis was limited to 6 SSuN jurisdictions that reported more than 25 transgender persons attending the participating clinic(s) between January 1, 2010, and June 30, 2013: Baltimore (2 clinics), Chicago (2 clinics), Los Angeles County (12 clinics), New York City (9 clinics), San Francisco (1 clinic), and Seattle (1 clinic). Participating clinics in Baltimore provided HIV primary care services and conducted local outreach and linkage to care efforts aimed toward men who have sex with men (MSM) and transgender communities; therefore, we excluded visits to Baltimore clinics for which the primary reason was obtaining HIV primary care services (9.2% of total visits to Baltimore clinics) to avoid biasing HIV prevalence estimates. Because few (<5) transgender men attended participating clinics in Los Angeles County, patients from Los Angeles County were not included in the analyses of transgender men. Since these activities are considered public health surveillance, institutional review board approval was not required.

Gender Identity

SSuN data transmitted to CDC contained a single element denoting the patient's gender as either male, female, transgender male-to-female, transgender female-to-male, or transgender unspecified. The source of this information varied by clinic and jurisdiction and included patient self-report at the time of registration or clinician encounter or staff documentation of the patient's gender identity. Patients who were identified as transgender during at least 1 visit during the observation period were defined as transgender in this analysis. Transgender patients who were not identified as male-to-female or female-to-male (ie, transgender unspecified) were excluded from further analyses because the small number (n = 16) precluded analysis of them as a separate group.

CT and GC Diagnoses and HIV Status

The CT and GC diagnoses were based on positive test results from urine specimens or patient- or clinician-collected urethral, vaginal, rectal, or pharyngeal swabs. Screening and diagnostic testing practices varied by clinic and jurisdiction and included both routine screening and testing in accordance with reported exposure sites. Test type used to diagnose CT and GC varied over time and by jurisdiction, but all jurisdictions used either nucleic acid amplification tests (NAAT) exclusively or both NAAT and culture. Two jurisdictions did not test for pharyngeal CT infections. HIV-infected patients were identified through positive laboratory test results documented in the medical record or patient self-report if there was no documented HIV test.

Analysis

We calculated the proportion of transgender women and transgender men who were tested and the proportion who tested positive for CT and GC overall and by anatomic site. We defined the proportion tested as the number of unique patients tested for CT/GC at 1 or more visits during the observation period divided by the total number of patients in the analytic sample. We defined the proportion positive as the number of patients who tested positive at any visit during the observation period divided by the total number of patients tested at any study visit. We calculated the proportion of HIV-infected transgender women and transgender men, which we defined as the number of patients with either self-reported or laboratory-confirmed HIV infection divided by the total number of patients in the sample. To contextualize these results, we repeated these calculations for cisgender patients attending the same clinics during the same observation period, including cisgender MSM (defined in this analysis as cisgender men who self-identified as gay or bisexual or reported ever having sex with a male partner), cisgender men who have sex with women only (MSW, defined as cisgender men who did not self-identify as gay or bisexual and did not report ever having a male sex partner), and cisgender women irrespective of sexual orientation.

Among the subset of transgender women and transgender men who had 1 or more extragenital CT or GC infections during the observation period, we calculated the proportion with 1 or more extragenital infections accompanied by a concurrent (ie, at same visit) negative urogenital test to assess how many patients had extragenital infections that would have been missed through urogenital screening alone. Those who were tested or who tested positive more than once were counted only once in all proportion calculations. All analyses were person-based and were conducted using SAS version 9.3 (SAS Institute, Cary, NC).

RESULTS

Demographics

Characteristics of the overall patient population varied by jurisdiction (Table 1). We observed differences by jurisdiction in the number of transgender patients who attended participating clinics (range, 42–167); the proportion of all patients who were transgender women (range, 0.08–0.30%), transgender men (range, <0.01–0.15%), and cisgender MSM (range: 5.3–33.5%); and the racial/ethnic composition of the patient population. A total of 506 transgender women (1045 total visits) and 120 transgender men (209 total visits) attended participating clinics in 6 SSuN jurisdictions between January 1, 2010, and June 30, 2013, and were included in the analytic sample. Table 2 displays the demographic characteristics of the transgender women and men who were seen at participating clinics. Most transgender women in the analytic sample were seen at clinics in New York City (29.6%) or Los Angeles (22.1%), were Hispanic (45.7%) or non-Hispanic black (28.3%), 30 years of age or older (51.0%), and reported having only male sex partners (90.3% of those who reported this information). Most transgender men were seen at clinics in San Francisco (36.7%) or Seattle (20.8%), were non-Hispanic white (59.2%), and were 20–29 years of age (64.2%). Among the transgender men who reported their partners' gender (n = 77), 32 (41.6%) had both male and female sex partners.

TABLE 1
TABLE 1:
Characteristics of Clinics and Patients in 6 SSuN Jurisdictions, January 1, 2010 to June 30, 2013
TABLE 2
TABLE 2:
Demographic and Clinical Characteristics of Transgender Women and Transgender Men Attending Clinics in 6 SSuN Jurisdictions*, January 1, 2010 to June 30, 2013

HIV Status

HIV status was known for the majority of transgender women (73.7%) and men (63.3%) (Table 2). The overall proportions of HIV-infected transgender women and men were 14.2% and 8.3%. Eight of the 10 HIV-infected transgender men attended clinics in Baltimore.

CT and GC Testing and Infections

Most transgender women and transgender men were tested for CT (80.0% and 86.7%, respectively) and GC (80.2% and 87.5%, respectively) at 1 or more anatomic sites during the observation period (Table 3). Most transgender women and transgender men were tested at urogenital sites for CT (75.7% and 80.8%) and GC (77.9% and 82.5%). Fewer transgender women and transgender men were tested at extragenital sites for CT (58.9% and 40.8%) and GC (62.1% and 48.3%).

TABLE 3
TABLE 3:
C. trachomatis and N. gonorrorheae Testing and Infection Among Transgender Women and Transgender Men Attending Clinics in 6 SSuN Jurisdictions*, January 1, 2010 — June 30, 2013

Of those tested at any anatomic site, 13.1% and 12.6% of transgender women had at least 1 positive CT or GC test, respectively, during the observation period compared with 7.7% and 10.5% of transgender men. The proportions of transgender women tested who had at least 1 positive rectal CT or GC test (15.4% and 11.8%) or pharyngeal CT or GC test (5.4% and 9.8%) were higher than the proportions with positive urogenital CT or GC tests (0.8% and 2.8%). Similarly, the proportions of transgender men tested who had at least 1 positive rectal CT or GC test (15.6% and 14.7%) or pharyngeal CT or GC test (11.8% and 5.9%) were higher than the proportions of transgender men with 1or more positive urogenital CT or GC tests (4.1% and 7.1%). The proportions of transgender women and transgender men who had rectal or pharyngeal CT or GC infections were similar to those of cisgender MSM and higher than those of cisgender MSW and women (Supplemental Table 1, http://links.lww.com/OLQ/A306).

Of the transgender women with at least 1 extragenital CT infection during the observation period (n = 50), 43 (86.0%) had a concurrent negative urogenital CT test (Table 4). Similarly, among the 47 transgender women with at least 1 extragenital GC infection during the observation period, 38 (80.9%) had a concurrent negative urogenital GC test. The proportions of transgender men with a positive extragenital test who also had a concurrent negative urogenital test were lower (CT, 2/7, 28.6%; GC, 2/7, 28.6%). When rectal and pharyngeal infections were considered separately, the proportions with a concurrent negative urogenital test remained similar.

TABLE 4
TABLE 4:
Percentages of Transgender Women and Transgender Men With Extragenital Chlamydial and Gonococcal Infections and Concurrent Negative Urogenital Tests, 6 SSuN Jurisdictions*, January 1, 2010 — June 30, 2013

DISCUSSION

Our results indicate a higher proportion of extragenital CT and GC infections than urogenital infections among both transgender women and transgender men, which is consistent with visit-level positivity data from San Francisco16 and a more recent comparative study of MSM and transgender women in Peru.24 In fact, the number of extragenital infections in our analysis could have been underestimated given that 2 of 6 jurisdictions did not test for pharyngeal CT infections, and several jurisdictions used culture, a less sensitive diagnostic method than NAAT, to diagnose rectal and pharyngeal infections during portions of the observation period.25 The proportions of transgender patients with rectal or pharyngeal CT or GC infections were comparable to or higher than those of cisgender MSM attending the same clinics, widely recognized as a population disproportionately affected by HIV and STDs.

Annual screening for CT and GC is recommended for all sexually active MSM at all anatomic sites of sexual exposure,26 but little is known about the benefits of routine screening in transgender populations. We found that the majority of transgender women and more than a quarter of transgender men with extragenital CT or GC infections had a concurrent negative urogenital test, suggesting that these extragenital infections would have been missed by urogenital screening alone. These findings highlight the importance of obtaining comprehensive sexual histories, including anatomic site of sexual exposure, to guide screening at rectal and pharyngeal sites and suggest that more data are needed to inform screening guidelines. Additionally, many transgender women and transgender men were not tested at urogenital sites, with the proportion tested ranging widely by jurisdiction. This suggests that a variety of screening approaches were used by clinics to test for urogenital infections; in some clinics, patients might not have been tested if they did not report an exposure or have symptoms. Although this may represent an important service gap for an underserved population, it is consistent with current screening guidelines26 and similar to screening coverage observed in other populations.27 This highlights the current lack of screening and other clinical guidance specifically tailored to transgender populations. More data are needed to identify the most effective screening practices for urogenital, rectal, and pharyngeal CT and GC infections in transgender populations. Information about transgender-specific issues related to screening, such as the performance of vaginal swab tests among transgender women who have undergone vaginoplasty, is also needed to inform screening guidelines for transgender populations.

A high proportion of transgender women (14.2%) and men (8.3%) in our sample were infected with HIV. Our HIV prevalence estimate of 8.3% among transgender men is more than twice as high as previous estimates,10 although our estimate was derived from a small sample of predominantly STD clinic patients, who would be expected to have a higher HIV prevalence than other populations. The higher HIV prevalence might be explained by the manner in which HIV status was ascertained in our analysis, which included both patient self-report and laboratory test results (rather than previous estimates based almost exclusively on self-report10). Alternatively, this finding might be related to local outreach and linkage to care efforts involving Baltimore's SSuN clinics, which had the preponderance of HIV-infected transgender men (70%) even after excluding patients who presented exclusively for HIV-related care. Nevertheless, this finding, combined with the lack of existing HIV prevalence estimates and the high prevalence of risk factors among subgroups of transgender men,13,14 potentially challenges the assumption that transgender men are at low risk of HIV acquisition.9

This analysis has several limitations. First, information about patients' current anatomy, surgical history, and anatomic sites of exposure was not available. Recent data28,29 suggest that only a small minority of transgender persons have undergone procedures such as vaginoplasty, labiaplasty, phalloplasty, or metoidioplasty. Nevertheless, these information gaps limit the utility of our findings in informing the development of screening guidelines or other prevention services for the transgender population. Second, the percentages of transgender patients with a CT or GC infection were based on tests performed over a 3.5-year period during which some patients were tested repeatedly at the same anatomic site. Because patients tested repeatedly might represent a group at higher risk of STD acquisition, our results are not comparable with those from studies that report results of a single test. Third, we were unable to adequately compare results from transgender patients with those from cisgender groups because these groups had substantially different demographic characteristics, behaviors, and testing rates, and the small number of transgender patients precluded a full accounting of these potentially confounding differences. Fourth, screening practices varied by clinic during the observation period, and this might have contributed to the variability in the proportion positive for CT and GC across SSuN sites. We could not ascertain reasons for testing (ie, routine screening or targeted testing), which complicates our findings' implications for screening. Fifth, gender identity was not measured consistently across clinics, and many transgender people might not self-identify as transgender.2,13 Therefore, it is likely that we underestimated the number of transgender persons in the sample, particularly because the proportion of patients classified as transgender (0.16%) was lower than estimates of the US transgender population (0.5%).30 Finally, our data were collected more than 5 years ago; given the rapidly changing awareness of and social climate surrounding transgender identity in the United States, monitoring of extragenital and urogenital STD screening and infection should continue with more timely data.

Despite these limitations, our study provides geographically diverse, multi-clinic STD and HIV estimates for a population for which such estimates have been lacking. However, substantial gaps remain in our understanding of STD epidemiology in transgender populations. Future studies should address these gaps by collecting information about transgender participants' anatomy and surgical status and the nature of participants' recent sexual encounters, including anatomic sites of exposure, partnership types (ie, main, casual, etc.), condom use, and other relevant behaviors. It is also important that gender identity measures included in medical records are standardized to allow for comparisons across multiple platforms, sites, and studies, are flexible enough to identify gender minority patients who do not identify as transgender, and are reflective of the patient's self-identified gender.31 The diversity of observed sexual identities and partner gender, and the proportion of transgender patients with rectal and pharyngeal CT and GC infections with concurrent negative urogenital tests in our study, suggest that the potential benefit of rectal and pharyngeal CT and GC screening in transgender populations should be explored further. Publicly funded STD clinics and other clinics offering STD services are likely an important source of HIV and STD testing and treatment for transgender people residing in urban areas. Given the socioeconomic marginalization experienced by many transgender people, such clinics are well situated to function as a safety net provider for the sexual health needs of at-risk transgender communities.

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