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Original Studies

Self-Reported Chlamydia and Gonorrhea Testing and Diagnosis Among Men Who Have Sex With Men—20 US Cities, 2011 and 2014

Hoots, Brooke E. PhD*; Torrone, Elizabeth A. PhD; Bernstein, Kyle T. PhD; Paz-Bailey, Gabriela MD, PhD*; for the NHBS Study Group

Author Information
Sexually Transmitted Diseases: July 2018 - Volume 45 - Issue 7 - p 469-475
doi: 10.1097/OLQ.0000000000000786
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Chlamydial and gonococcal infections are the 2 most frequently reported infectious diseases in the United States.1 Untreated chlamydia (CT) or gonorrhea (GC) may increase a person’s chances of acquiring or transmitting human immunodeficiency virus (HIV),2 particularly among gay, bisexual, and other men who have sex with men (hereafter referred to as MSM), who are disproportionately affected by HIV.3

Asymptomatic infection with CT or GC is common and health care providers frequently rely on screening tests to detect infection.4 The CDC provides screening guidelines for CT and GC, and since 2006 has recommended that MSM be screened at least annually for both infections, and more frequently (every 3–6 months) for MSM at increased risk.4 The CDC recommends that MSM are screened at exposed anatomic sites, irrespective of condom use, including the urethra and rectum for CT and the urethra, rectum, and pharynx for GC.

Among men, national rates of reported CT have steadily increased since 2000, and rates of reported GC have increased since 2009; however, CT and GC case report data are limited in that they do not include complete information on sex of sex partners, so trends among MSM cannot be calculated. Additionally, because CT and GC infections are often asymptomatic, case report data are heavily influenced by changes in screening practices, and observed case rates cannot provide information on whether increases are due to increases in screening, indicate increases in incidence, or both. Population-based surveillance, such as CDC’s National HIV Behavioral Surveillance (NHBS), are critical to help monitor trends in CT and GC among MSM.

To monitor compliance with screening recommendations and address gaps in case report data, we used NHBS data collected in 2011 and 2014 to assess changes in self-reported CT and GC testing and diagnosis among MSM.

METHODS

The NHBS monitors HIV-associated behaviors and HIV prevalence in cities with high acquired immune deficiency syndrome burden among 3 populations at high risk for infection: MSM, persons who inject drugs, and heterosexuals at increased risk for HIV infection. Data are collected in annual rotating cycles such that each population is sampled every 3 years. Cross-sectional behavioral data reported in this analysis are from MSM recruited for interviews and HIV testing through venue-based time-space sampling (VBS) in NHBS surveys in 20 cities in 2011 and 2014. The NHBS VBS procedures have been previously published.5,6 Men were systematically approached at recruitment events to screen for eligibility (aged ≥ 18 years, lived in a participating city, ever had sex with another man, and able to complete the interview in English or Spanish), and interviews were conducted using a standardized questionnaire covering demographics, HIV-associated behaviors, and use of HIV prevention and testing services. The NHBS activities were approved by local institutional review boards in each participating city. The NHBS activities were determined to be research in which the Centers for Disease Control and Prevention (CDC) was not directly engaged and therefore did not require review by the CDC institutional review board.

Men who have sex with men who were currently sexually active, defined as having 1 or more male partners in the past 12 months, were included in the analyses. The main outcomes in this analysis were self-reported CT and GC testing and diagnosis in the past 12 months. Testing was ascertained from the question, “In the past 12 months, were you tested by a doctor or other health care provider for a sexually transmitted disease like gonorrhea, chlamydia, or syphilis? Do not include tests for HIV or hepatitis.” If the participant answered yes, he was then asked separately if he was tested for CT and if he was tested for GC. Analyses of CT and GC diagnosis data were limited to participants who reported CT and GC testing, respectively. Diagnosis was ascertained from the question, “In the past 12 months, has a doctor or health care provider told you that you had…” and was asked for CT and GC separately. Data on anatomical site of testing and diagnosis were not obtained.

Bivariate analyses were conducted to explore differences by demographic and sexual behavior characteristics for the four outcomes (self-reported testing for CT and GC, and self-reported diagnosis of CT and GC). The primary exposure assessed in this analysis was year of NHBS survey (2011 vs 2014). Prevalence ratios and 95% confidence intervals (CIs) were calculated from log-linked Poisson regression models with generalized estimating equations clustered on VBS recruitment event. Separate models were built for each covariate and outcome combination. Models included year, the covariate of interest, and the interaction term between year and the covariate. Prevalence ratios correspond to the change in the outcome with respect to interview year (2011–2014). Other variables associated with the covariates and outcomes in bivariate analyses with P values less than 0.10 were considered as potential confounders in the multivariable models and a change-in-estimate approach was used to reduce models; variables that changed the prevalence ratio by 10% or more were retained in the model as confounders. If no covariates were retained as confounders, the unadjusted models are presented. To examine which demographic groups were more likely to be tested for CT and GC in 2014, we also developed models as described above with the demographic variable in question as the exposure and CT or GC testing as the outcome restricting the data to the 2014 survey sample. All analyses were conducted using SAS 9.3 (SAS Institute Inc., Cary, NC).

RESULTS

In 2011, 9881 men were eligible for and completed the NHBS survey. After excluding those with incomplete (n = 53) or invalid interviews (n = 9) and those who were not currently sexually active (n = 729), 9256 were left for analysis. In 2014, 10,457 men were eligible for and completed the NHBS survey. After excluding those with incomplete (n = 72) or invalid interviews (n = 16) and those who were not currently sexually active (n = 563), 9640 were left for analysis.

Approximately 40% of the sample was white in each year (Table 1). Although there was no difference in the 2011 and 2014 samples by race, the 2011 sample was slightly younger than the 2014 sample (44% 18–29 years in 2011 versus 42% in 2014, P = 0.001). Health insurance coverage increased between the 2 sample years, with 70% reporting current health insurance in 2011 and 79% in 2014 (P < 0.001), as did self-reported HIV prevalence (13% in 2011 and 16% in 2014, P < 0.001). Men who have sex with men in 2014 were more likely to report 6 or more partners in the past 12 months and to have disclosed their same-sex behavior to a provider (P < 0.001 for both).

TABLE 1
TABLE 1:
Characteristics of Sexually Active MSM in 20 US Cities—National HIV Behavioral Surveillance, 2011 and 2014

CT Testing

For the CT testing analysis, 68 men in 2011 and 79 in 2014 were missing testing data, leaving 9188 and 9561 men, respectively, for analysis (Table 2). Prevalence of self-reported CT testing in the past 12 months in 2011 was 37.2%, and increased to 46.7% in 2014, for an overall prevalence ratio of 1.25 (95% CI, 1.20–1.30). Testing significantly increased and with a similar magnitude to the overall increase among all subgroups except those with unknown HIV status.

TABLE 2
TABLE 2:
Prevalence of Self-Reported CT and GC Testing in the Past 12 Months Among MSM in 20 US Cities—National HIV Behavioral Surveillance, 2011 and 2014

In 2014, those of other race were more likely to report testing for CT compared with whites (prevalence ratio [PR], 1.10; 95% CI, 1.02–1.19) (Fig. 1A). The MSM with HIV were also more likely to report testing in the previous 12 months compared with those who reported being HIV-negative (PR, 1.37; 95% CI, 1.31–1.44). Testing was less common with increasing age (PR, 0.67; 95% CI, 0.63–0.71 among those 40 years or older compared with those 18–29 years), and among those with current insurance compared with those without (PR, 0.79; 95% CI, 0.75–0.84). Testing was also less common among those who reported fewer sex partners in the past 12 months (PR, 0.58; 95% CI, 0.54–0.62 among those with 1 partner compared to those with 6+; PR, 0.75; 95% CI, 0.72–0.79 among those with 2–5 partners compared to those with 6+) and among those who had not disclosed same sex behavior to their health care provider (PR, 0.54; 95% CI, 0.50–0.59).

Figure 1
Figure 1:
A, PRs and 95% CIs comparing prevalence of CT testing within selected demographic groups, 2014. B, PRs and 95% CIs comparing prevalence of GC testing within selected demographic groups, 2014. HCP, health care provider.

CT Diagnosis

Of those who reported CT testing in the past 12 months, 5 men in 2011 and 2 men in 2014 were missing diagnosis data, leaving 3417 and 4459 for analysis, respectively (Table 3). Prevalence of self-reported CT diagnosis in the past 12 months was 7.7% in 2011 and 10.6% in 2014, for an overall PR of 1.37 (95% CI, 1.18–1.59). The CT diagnoses increased among most subgroups, although the magnitude of the increases differed. Blacks and Hispanics had a higher prevalence of reported CT diagnoses than whites and persons of other race/ethnicity in 2011, but whites and MSM of other race/ethnicity experienced greater relative increases in diagnoses between 2011 and 2014. Men who have sex with men aged 18 to 29 years had the highest prevalence of CT diagnoses in 2011, but MSM aged 30 to 39 years had a greater increase (adjusted PR [aPR], 1.93; 95% CI, 1.42–2.63 for ages 30–39 years vs aPR, 1.20; 95% CI, 0.98–1.48 for ages 18–29 years), resulting in similar prevalences for the 2 age groups in 2014. Prevalence also increased more and resulted in higher prevalences among those without current insurance (PR, 1.56; 95% CI, 1.17–2.08) and those who were self-reported HIV-positive (PR, 1.55; 95% CI, 1.14–2.10).

TABLE 3
TABLE 3:
Prevalence of Self-Reported CT and GC Diagnosis in the Past 12 Months Among MSM in 20 U.S. Cities—National HIV Behavioral Surveillance, 2011 and 2014

GC Testing

For the GC testing analysis, 58 men in 2011 and 77 in 2014 were missing testing data, leaving 9198 and 9563 men for analysis (Table 2). Self-reported prevalence of GC testing in the past 12 months was 38.0% in 2011 and increased to 47.3% in 2014, for a prevalence ratio of 1.24 (95% CI, 1.19–1.29). As with CT testing, GC testing increased among all subgroups except those of unknown HIV status, and the increases seen were of a similar magnitude to that seen overall. The percentage of agreement between reporting CT testing and GC testing (Cohen’s κ statistic) was 0.95, meaning it was unlikely for a man to report being tested for one infection and not the other.

GC Diagnosis

Of those who reported GC testing in the past 12 months, 3 in 2011 and 7 in 2014 were missing data on GC diagnosis, leaving 3490 and 4514 for analysis, respectively (Table 3). Prevalence of self-reported GC diagnosis increased from 10.1% in 2011 to 14.2% in 2014 (PR, 1.40; 95% CI, 1.23–1.60). Although prevalence of GC diagnoses was higher than CT diagnoses, the magnitude of the increase in diagnoses between 2011 and 2014 was similar. Whites and MSM of “other” race/ethnicity experienced greater increases in GC diagnoses between the 2 study years (PR, 1.68; 95% CI, 1.35–2.09 for whites; PR, 2.27; 95% CI, 1.44–3.58 for “other”), resulting in these groups having a higher prevalence of GC diagnoses in 2014 compared with blacks and Hispanics. Those older than 30 years also had greater increases in GC prevalence (PR, 1.70; 95% CI, 1.33–2.18), which led to 30- to 39-year-olds matching the prevalence of 18- to 29-year-olds in 2014. Although those without current insurance did not experience a statistically significant increase in GC diagnoses (PR, 1.15; 95% CI, 0.92–1.45), those with insurance did (PR, 1.58; 95% CI, 1.35–1.85).

In 2014, prevalence of GC testing within selected demographic groups was similar to that of CT testing (Fig. 1B).

Sensitivity Analyses

There were 53 men in 2011 and 38 men in 2014 who reported a CT diagnosis without reporting testing for CT in the prior 12 months. Similarly, there were 79 men in 2011 and 49 men in 2014 who reported a GC diagnosis without reporting testing for GC in the prior 12 months. These men were not included in the diagnoses analyses because those analyses were restricted to those who reported testing in the past 12 months. There are several potential reasons for why these men may not have reported testing, but reported a sexually transmitted disease (STD) diagnosis. First, they may have not recalled being tested, but recalled being told about their STD diagnosis. Second, they may have received expedited partner therapy7 for CT or GC from a sexual partner and assumed this was a diagnosis. Finally, they may have been presumptively treated for CT or GC by a physician based on symptoms or based on the diagnosis of a sexual partner. To examine the effect of inclusion of these self-reported diagnoses, we built additional models for CT and GC diagnoses not restricting the denominator to those who reported testing in the past 12 months.

For CT, self-reported diagnoses increased from 3.4% (318/9247) in 2011 to 5.3% (512/9633) in 2014 (PR, 1.54; 95% CI, 1.33–1.78). For GC, self-reported diagnoses increased from 4.7% (432/9249) in 2011 to 7.2% (689/9629) in 2014 (PR, 1.53; 95% CI, 1.34–1.74). Our prevalence ratios restricted to tested persons were similar to these estimates, but were more conservative.

DISCUSSION

Among MSM participating in NHBS during the 2011 and 2014 cycles, we found an increase in the proportion of MSM who reported being tested for CT or GC and increases in the self-reported diagnoses of these 2 bacterial STDs. Prevalence of self-reported testing and diagnosis in the past 12 months increased among most subgroups between 2011 and 2014. Testing prevalence was similar for CT and GC, which is expected since testing for both infections is often performed through dual-screening tests.4 Although self-reported testing for CT or GC increased from 2011 to 2014, it is important to note that less than half of MSM (47%) in 2014 reported receiving a test for CT or GC in the prior 12 months. Between 2011 and 2014, self-reported testing for CT or GC increased by 25% and 24%, respectively. Yet, the self-reported prevalence of these 2 bacterial infections increased by 37% and 40% among those tested.

Changes in the availability of extragenital (rectal and oropharyngeal) CT/GC tests could partially account for the increases in reported screening. Currently, no commercially available CT or GC nucleic acid amplification tests (NAATs), which increase case finding, have been approved by the Food and Drug Administration for use with rectal or oropharyngeal swab specimens.4 Culture is the only approved method for diagnosis at these sites. However, an increasing number of public health and commercial laboratories are using Clinical Laboratory Improvement Amendments guidelines and conducting verification studies for off-label use of NAATs, allowing these test results to then be used for clinical management4; as such, more clinical sites are offering extragenital testing, likely resulting in increased screening among MSM. The NHBS does not ask about anatomical site of test, so we are unable to determine from our data if more extragenital tests were done in 2014 compared with 2011.

An increase in extragenital screening could also be contributing to the higher-magnitude increase in diagnoses. Urogenital testing alone misses a significant percentage of chlamydial and gonococcal infections among MSM because it misses other sites of sexual contact, particularly among men who only report receptive anal sex or oral sex.8,9 In a recent review of 7 studies reporting the prevalence of extragenital infections in MSM, Chan et al10 reported that if MSM had been screened for urogenital infections alone and not at rectal and oropharyngeal sites, 14% to 85% of GC and CT infections would have been missed. Because extragenital testing increases not only the number of tests done (and therefore the number of diagnoses) but also the likelihood that some MSM test positive, the increase we see in CT and GC diagnoses may be attributable to an increase in extragenital testing. The increase in testing may also reach a subgroup of MSM that potentially has higher prevalences of CT and GC. For example, screening increased the most among MSM in the 30- to 39-year-old age group, and this group also experienced the greatest increase in diagnoses.

Data from CDC's STD Surveillance Network (SSuN) also support an increase in GC diagnoses over the time period. A random sample of reported GC cases was interviewed to determine MSM status in 6 SSuN jurisdictions and population denominators of MSM were estimated for the jurisdictions to calculate rates of GC among MSM.11 The estimated MSM rate increased from 1369 cases per 100,000 in 2010 to 3435 cases per 100,000 in 2015. Further, rate ratios comparing MSM with women and men who had sex with women only showed a disparity in GC among MSM compared with the other 2 groups.

Although increases in screening may account for some of the observed increases in both reported diagnoses in SSuN and self-reported history of diagnoses in NHBS, it is likely that there have been concurrent increases in incidence among MSM. In the NHBS data, the observed increase in self-reported diagnoses (37% increase for CT, 40% increase for GC) was larger than the self-reported increase in testing (25% for CT, 24% for GC) between 2011 and 2014, suggesting incidence may be contributing to observed increases in diagnoses. Although case report data are not available to estimate trends in CT and GC incidence among MSM, the number of reported cases of primary and secondary syphilis among MSM has increased during 2011 and 2014, suggesting increased transmission of STDs among MSM.1

There have been concerns in the public health community about pre exposure prophylaxis (PrEP) use resulting in lower condom use and higher STD transmission. However, in our analysis, the increases in CT and GC diagnoses in the years studied are unlikely due to use of preexposure prophylaxis, or PrEP, as self-reported use among self-reported HIV-negative MSM was less than 1% in 2011 and 4% in 2014.12 An HIV-negative MSM who is not in a monogamous relationship with a recently tested HIV-negative man and who has also been diagnosed with an STD in the past 6 months is eligible for PrEP according to the CDC clinical guidelines.13 This is an important population to offer PrEP as a prevention tool due to the higher prevalence of HIV infection among MSM and the increased risk of HIV acquisition with CT or GC coinfection.

Despite increases between the 2 periods, testing for CT and GC remains suboptimal, with less than half of MSM reporting a test in the past 12 months. Other studies have also reported relatively low levels of CT and GC testing prevalence among MSM, even at STD clinics.14,15 Barriers to testing include provider time constraints and competency.16 Providers have described needing to prioritize more urgent or complex medical assessments and not having time left for STD screening.17,18 Some providers also feel uncomfortable taking a detailed sexual history or are unfamiliar with the availability of NAAT testing, current testing guidelines, or current treatment guidelines for GC.14 Patient barriers include discomfort in discussing sexual practices and a misunderstanding about the risk for extragenital STDs.16 Among this population of MSM sampled, culturally competent health care may be associated with higher rates of screening and detection of untreated infections.

Our analysis is subject to several limitations. NHBS is conducted at venues in high HIV prevalence urban areas, so results may not be generalizable to all cities or to all MSM in participating cities. Data are self-reported and might be subject to social desirability bias or recall error. Social desirability would lead to underestimation of past diagnosis and likely overestimation of self-reported testing, whereas it is unclear how recall error would affect estimates. However, our results are based on differences between 2011 and 2014 and are less likely to be affected by bias than point estimates provided the bias remained consistent over time. The analysis is limited to 2 time points and cannot be interpreted as a trend. As mentioned above, we did not have data on anatomical site of testing to examine if the increase in testing was due to an increase in extragenital testing specifically. Finally, data are not weighted to account for complex VBS sampling methodology. Point estimates may therefore be biased by overrepresented or underrepresented subgroups of the sample. However, multivariable analysis of differences across years should not be affected by a lack of weighting.

In summary, diagnoses of both CT and GC increased among MSM beyond the magnitude of the increases in testing between 2011 and 2014. Testing in the past 12 months was low, and increased efforts are needed to meet annual STD screening recommendations among MSM at high risk for HIV. Further, MSM who are diagnosed with an STD are important candidates for interventions to reduce HIV acquisition and transmission, including PrEP among HIV-negative individuals and engagement or reengagement in care to achieve viral suppression among HIV-infected individuals.

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