In the United States, the reported number of primary and secondary (P&S) syphilis cases reached a historic low of 5979 cases and an annual rate of 2.1 cases per 100,000 population in 2000.1 Since then, the number of P&S syphilis cases has been increasing, and the epidemiology has shifted from heterosexuals to gay, bisexual, and other men who have sex with men (collectively referred to as MSM).2–4 In 2014, the number of reported P&S syphilis cases in the United States was 19,999, 3.3 times that of 2000, and the annual rate was 6.3 cases per 100,000 population, 2.9 times that of 2000.5 More than 90% of reported P&S syphilis cases were in men, and MSM accounted for 83% of male cases where sex of the sex partner was known.5 In recent years, the largest increases in reported P&S syphilis were observed among Hispanic and white MSM and MSM aged 25–29 years.6
Among MSM, syphilis facilitates the transmission of HIV, as it increases the likelihood of transmitting HIV approximately 2 to 3 fold.7 Syphilis causes inflammatory genital ulcers and lesions which can increase the risk of HIV transmission and acquisition.7 Some risk behaviors such as unprotected anal sex and sex with multiple partners increase the likelihood of acquiring both syphilis and HIV infection. High rates of HIV-coinfection among MSM infected with P&S syphilis and high HIV seroconversion rates after P&S syphilis infection have been reported.7,8 Syphilis also complicates the clinical course of HIV. It has been shown that syphilis increases the viral load and decreases CD4 counts in HIV-infected patients and is associated with a higher rate of treatment failure in HIV-infected persons.5–7
Syphilis screening is the first step to effective treatment, partner notification, and education programs that help reduce risky sex behaviors and have been the cornerstone of syphilis prevention measures in the United States.2 Since 2006, the Centers for Disease Control and Prevention (CDC) has recommended that all sexually active MSM receive routine annual laboratory screening for common sexually transmitted diseases (STDs), including syphilis. More frequent STD screening (ie, at 3 to 6-month intervals) is recommended for MSM who have multiple or anonymous partners, have sex in conjunction with illicit drug use, use methamphetamine, or have sex partners who participate in these activities.9–11 Routine screening may help facilitate more rapid treatment of infections and, in turn, reduce the likelihood of ongoing transmission within sexual networks.
Given the increased burden of syphilis among MSM in the United States and CDC's annual syphilis testing recommendation for sexually active MSM, there is a need to examine the syphilis testing and diagnosis patterns among them. The objective of this analysis is to assess self-reported syphilis screening and diagnosis trends among sexually active MSM from 2008 to 2014 in the United States by selected characteristics using 3 cycles (2008, 2011, and 2014) of cross-sectional survey data from CDC's National HIV Behavioral Surveillance (NHBS). Results of this analysis provide the first national picture of syphilis screening practices among MSM. These data are critical to evaluating the effectiveness of CDC's annual syphilis testing recommendations among sexually active MSM and identifying subpopulations that would benefit from enhanced syphilis intervention strategies in the United States.
NHBS staff members working in 20 metropolitan statistical areas (MSAs) with large burden of acquired immune deficiency syndrome (AIDS) collected cross-sectional behavioral data among MSM in 2008, 2011, and 2014 using venue-based sampling (VBS). The 20 MSAs12 were Atlanta, GA; Baltimore, MD; Boston, MA; Chicago, IL; Dallas, TX; Denver, CO; Detroit, MI; Houston, TX; Los Angeles, CA; Miami, FL; Nassau, NY; Newark, NJ; New Orleans, LA; New York City, NY; Philadelphia, PA; San Diego, CA; San Francisco, CA; San Juan, PR; Seattle, WA; and Washington, DC.
NHBS VBS procedures have been previously published13,14 and are briefly summarized here. First, NHBS staff identified appropriate venues (eg, bars, social organizations, and sex venues) and days and times when men frequented those venues. In 2008, only venues in which 75% of men attending were MSM were eligible for inclusion; this threshold was lowered to 50% in 2011 because venues had become more integrated by sexual orientation. Second, venues and corresponding day/time periods were chosen randomly each month for recruitment events. Third, staff members systematically approached men to screen for eligibility at each recruitment event. Men eligible to be interviewed were aged ≥18 years, residents of the participating city, able to complete the interview in English or Spanish, and willing and able to provide informed consent. In addition, in 2011 and 2014, only men who reported having ever had oral or anal sex with another man were interviewed. Although eligibility criteria differed, the same analysis criteria were used for all years in this analysis. We included sexually active MSM who completed the interview, provided valid responses determined by the interviewer, and reported having had sex with another man during the previous 12 months for this analysis. After participants provided informed consent, trained interviewers conducted anonymous face-to-face interviews using a standardized questionnaire about demographics, HIV-associated behaviors, and use of prevention and testing services.
The 2 main outcomes in this analysis are syphilis screening and syphilis diagnosis in the past 12 months. During the interview, each participant was asked questions on whether he had been tested by a doctor or other health care provider for syphilis in the past 12 months, and whether he had been told by a doctor or other health care provider that he had syphilis in the past 12 months. Participants who reported having had a syphilis test or having been told that they had syphilis by a doctor in the past 12 months were defined as having had a recent syphilis test. Participants were considered to have been diagnosed with syphilis in the past 12 months if they reported having been told by a doctor or other health care provider that they had syphilis. These outcome measures were collected in all 3 cycles of the MSM NHBS included in this analysis.
For each year, we calculated percentages of syphilis screening and diagnosis by selected characteristics, including age, race/ethnicity, highest level of education completed, below or above federal poverty level based on participants' self-reported incomes and U.S. Department of Health and Human Services poverty guidelines, current health insurance status, self-reported HIV status, number of sexual partners in the past 12 months (1–10 vs. >10, the 10 partner cutoff was the most relevant cut point for diagnosis trends), health provider visit in the past 12 months, and region of residence. To assess whether percentage with syphilis screening and diagnosis changed over time, we used separate Poisson regression models with generalized estimating equations clustered on recruitment event to calculate prevalence ratios (PRs) and 95% confidence intervals (CIs) (PROC GENMOD in SAS v9.3.2).15 Year was included in the model as an ordinal variable; individual interaction terms for each covariate by year were included in the models to examine changes over time by subgroup. Each PR measures change in the outcome for a 3-year change in interview year (ie, 2008–2011 or 2011–2014). The models were also adjusted for race/ethnicity, current insurance, and whether the participant saw a health care provider in the past 12 months. Adjusted models did not differ from unadjusted models and are not shown. Analysis of syphilis diagnosis was limited to participants who reported syphilis screening.
A total of 30,062 MSM were interviewed in the 3 NHBS cycles. Among them, 28,295 (94%; 2014: n = 9694; 2011: n = 9291; and 2008: n = 9310) MSM who were sexually active in the 12 months before the interview were included in the analysis (Table 1). In all 3 years, participants' demographic characteristics were similar. Overall, participants were about evenly distributed in each age group, with slightly more aged 30–39 years (7283, 26%) and fewer aged 50 years or older (3421, 12%); there were more non-Hispanic white (white) MSM (11,494, 41%) than non-Hispanic black (black; 7380, 26%) and Hispanic or Latino (Hispanic; 7215, 26%) MSM. Education, poverty level, self-reported HIV status, the number of sexual partners in the last 12 months, and region of residence were similar across all 3 study years. The percentage of participants with current health insurance increased from 68% in 2008, to 70% in 2011, and to 79% in 2014. The percentage of participants who reported seeing a health care provider in the past 12 months increased from 77% from 2008, to 80% in 2011, and to 83% in 2014.
Syphilis Screening in the Past 12 Months
Among 28,295 MSM included in the analysis, 11,900 (2014: n = 4699; 2011: n = 3688; and 2008: n = 3513) reported syphilis screening in the past 12 months (Table 2). Overall, 49% reported syphilis screening in 2014, a significant increase from 40% in 2011 and 38% in 2008 (PR 1.13, 95% CI: 1.11 to 1.16). From 2008 to 2014, percentage with syphilis screening increased in every subgroup examined, except for MSM aged >50 years (33% in 2008 to 34% in 2014). The largest increases in syphilis screening between 2008 and 2014 were among MSM aged 30–39 years (37%–52%, PR 1.17, 95% CI: 1.13 to 1.22), white MSM (35%–48%, PR 1.14, 95% CI: 1.11 to 1.18), MSM who completed some college or higher degree (40%–51%, PR 1.13, 95% CI: 1.10 to 1.15), MSM with income above the federal poverty level (38%–50%, PR 1.14, 95% CI: 1.12 to 1.17), MSM with insurance (40%–51%, PR 1.13, 95% CI: 1.10 to 1.15), MSM who self-reported being HIV negative (35%–45%, PR 1.13, 95% CI: 1.11 to 1.16), MSM who reported >10 sex partners (48%–65%, PR 1.16, 95% CI: 1.12 to 1.20), and MSM residing in the northeast (32%–50%, PR 1.26, 95% CI: 1.19 to 1.32).
In 2014, syphilis screening was most commonly reported by MSM who were aged 25–29 years (56%), HIV-positive MSM (68%), MSM with >10 sexual partners in the past 12 months (65%), and MSM who saw a health care provider in the last 12 months (54%) (Table 2). Syphilis screening was least commonly reported by MSM who were aged 50 years and older (34%), MSM who completed less than high school education (41%), MSM without health insurance (42%), MSM who had ≤10 sexual partners in the past 12 months (45%), and MSM who did not see a health care provider in the past 12 months (25%).
Syphilis Diagnosis in the Past 12 Months
Among 11,900 MSM who reported syphilis screening, 1114 (2014: n = 509; 2011: n = 280; and 2008: n = 299) reported syphilis diagnosis in the past 12 months (Table 3). Overall, 11% reported a diagnosis of syphilis in 2014, a significant increase from 8% in 2011 and 9% in 2008 (PR 1.16, 95% CI: 1.07 to 1.25). From 2008 to 2014, syphilis diagnosis increased among MSM aged 25–29 years (6%–10%, PR 1.39, 95% CI: 1.16 to 1.65) and 30–39 years (9%–12%, PR 1.21, 95% CI: 1.06 to 1.38), black MSM (9%–14%, PR 1.30, 95% CI: 1.13 to 1.48), MSM who completed high school (10%–13%, PR 1.18, 95% CI: 1.02 to 1.36) and college or higher education (7%–10%, PR 1.19, 95% CI: 1.08 to 1.31), MSM with health insurance (8%–10%, PR 1.19, 95% CI: 1.08 to 1.30), HIV-positive MSM (15%–21%, PR 1.20, 95% CI: 1.07 to 1.34), MSM reported >10 sexual partners (11%–17%, PR 1.30, 95% CI: 1.14 to 1.49), MSM who saw a health provider in the last 12 months (8%–11%, PR 1.19, 95% CI: 1.09 to 1.28), and MSM residing in the midwest (3%–10%, PR 1.75, 95% CI: 1.35 to 2.26).
In 2014, syphilis diagnosis was most commonly reported by black MSM (14%), MSM who completed less than high school education (21%), MSM with income below federal poverty level (17%), HIV-positive MSM (21%), MSM who had >10 sexual partners in the past 12 months (17%), and MSM residing in the south (13%) (Table 3). Syphilis diagnosis was least commonly reported by MSM who were aged 50 years and older (9%), white MSM (8%), MSM who had completed some college or higher education (10%), MSM with income above federal poverty level (9%), HIV-negative MSM (8%), MSM who had ≤10 sexual partners in the past 12 months (9%), and MSM residing in the west (9%).
We examined self-reported syphilis testing and diagnosis trends among MSM from 2008 to 2014 to advance our understanding of syphilis testing and diagnosis patterns over time among MSM in the United States. We found that self-reported syphilis screening and diagnosis within 12 months of the NHBS interview among sexually active MSM increased from 2008 to 2014. The largest increases in syphilis screening between 2008 and 2014 were among MSM aged 30–39 years and MSM who reported >10 sex partners. The largest increases in syphilis diagnosis among those screened were observed among MSM who were aged 25–29 years, black, HIV positive, and reported >10 sexual partners.
Despite significant increases in syphilis screening in the past 12 months from 2008 to 2014, less than half of sexually active MSM reported recent syphilis screening in 2014, and among high-risk MSM subgroups (ie, HIV-positive MSM and MSM reported >10 sexual partners), the percentage reporting syphilis screening in the past 12 months was less than 70%. The results suggest that syphilis testing among sexually active MSM is suboptimal, especially among higher risk MSM (ie, MSM with >10 sexual partners). Timely syphilis testing facilitates prompt identification of syphilis infection, which consequently helps interrupt the continued transmission of syphilis among sexually active MSM through effective syphilis treatment, and timely notification, testing, and treatment of all sexual partners of the index case. Timely testing is of particular importance for mitigating ongoing syphilis transmission among high-risk MSM. These results highlight the importance of expanding coverage of syphilis testing and eliminating delays in obtaining syphilis tests among sexually active and high-risk MSM.
Although recent syphilis screening among MSM increased, syphilis diagnoses among those screened also rose, especially among MSM aged 25–29 years, black, HIV positive, and those who reported >10 sexual partners. These data suggest that the increase in syphilis diagnosis may not be due to an increase in syphilis screening: nearly every MSM subpopulation had increases in syphilis screening, but only some had an increase in syphilis diagnosis. For example, although increases in screening were significant for both HIV-positive and HIV-negative MSM, only HIV-positive MSM had significant increase in diagnosis. Furthermore, increased syphilis diagnosis is consistent with findings from previous studies that reported increased P&S syphilis cases among MSM and various MSM subpopulations, such as HIV-positive MSM, racial minority, and younger MSM in the United States.16–18 However, these previous reports were syphilis diagnoses based on case reports and were probably influenced by screening. Given that a large percentage of syphilis diagnoses occurred among HIV-positive MSM and that syphilis testing of MSM in HIV care is suboptimal, ensuring that syphilis screening is part of HIV care is critical. Among HIV-negative sexually active MSM, only one-third to less than one-half reported recent screening. As the risk of HIV infection among men was reported high after the diagnosis of syphilis,19 syphilis screening and diagnosis potentially offer opportunities for HIV screening and prevention among sexually active MSM and vice versa. In addition, as suggested by a previous study, increasing knowledge of syphilis risk and testing recommendations might be effective ways to increase syphilis screening among MSM.20
In addition to disparities by age, race/ethnicity, HIV status, and the number of sexual partners, our findings also indicate that syphilis testing and diagnosis varied by geographic areas and access to a health care provider. MSM residing in the west had the highest prevalence of syphilis screening but did not have a significant increase in syphilis diagnosis. MSM who accessed health care providers had significant increases in syphilis testing and diagnosis. For sexually active MSM, health care providers should consider assessing STD-related risks, inquiring about symptoms related to common STDs, and performing at least annual testing for syphilis and HIV.9–11 Access to health care providers not only provides an opportunity for providers' intervention but also may indicate a person's willingness to engage in testing and treatment services. Therefore, increasing syphilis awareness among sexually active MSM, encouraging MSM to access health care, and engaging providers to implement syphilis testing might be effective ways to increase syphilis screening and early diagnosis. Structural level interventions instituted at the provider level, such as convene educational meetings for providers periodically presenting syphilis epidemiology, testing guidelines, and strategies for improving detection and management, have been shown to be effective approaches to improving screening for STDs.21 Patient level interventions such as reminders for screening or rescreening through text, telephone, or postcards have been shown to be both effective and cost efficient for improving screening for STDs in clinic-based settings.21 Furthermore, between 19% and 25% MSM who did not visit health care providers in the previous year reported syphilis screening in the past 12 months, indicating that men were screened in nontraditional/nonclinical venues. This finding suggests that expanding syphilis screening in nonclinical venues might be another effective approach.
This study has the following limitations. First, MSM were recruited in 20 MSAs with high AIDS burden, and results may not be generalizable to all cities or all sexually active MSM. Cities with high AIDS burden are often the focus of increased prevention and testing campaigns, initiatives, and resources.22,23 Further research is needed to determine whether the observed increase in syphilis screening is occurring nationwide or is limited to areas with increased prevention resources. Second, our outcome measures and selected characteristics are based on self-reported data and may be subject to reporting bias. For example, self-reported visits to a health care provider in NHBS surveys may overestimate the rates of care visits where syphilis screening is offered. Numerous previous studies reported overreporting for sexually transmitted disease (sexually transmitted infection) screening and underreporting for sexually transmitted infection diagnosis.24–26 Although we are unable to assess the scope of the reporting bias, the NHBS study protocol and questionnaire were consistent over time; therefore, any bias was likely to be consistent across the years, and if so, results of the trend analysis would be valid. Third, data are not weighted to account for the complex sampling methodology required to locate, recruit, and interview MSM. Although VBS weights are not available for this analysis, variables typically correlated with VBS sampling weights, such as venue type and city were included in the analysis model to adjust for sample clustering. Given the consistency of data distribution across years, trend analysis across years should not be affected by unweighted analysis.12,14,27 Fourth, the survey population is limited to MSM who attend venues; MSM who do not attend venues may, or may not, differ from the survey population on key outcomes. For example, older MSM may be less likely to attend venues than younger MSM. Fifth, we used the PR to measure each 3-year change in the prevalence of syphilis screening and diagnosis, which assumes a monotone trend in the change. The syphilis screening demonstrated a strictly monotone increasing trend from 2008 to 2014, but not so for syphilis diagnosis. Therefore, the results for syphilis diagnosis are approximated changes per 3-year. Finally, it is not possible to completely rule out the possibility of a systematic or methodological bias in our results. However, most NHBS procedures remained unchanged from 2008 to 2014.28 Consequently, a methodological bias is unlikely.
In summary, although syphilis screening in the past 12 months significantly increased from 2008 to 2014, the percentage of recent syphilis testing was still low among sexually active MSM and high-risk MSM, including HIV-positive MSM and MSM who had multiple sexual partners. Furthermore, syphilis diagnosis among those screened increased from 2008 to 2014. These results emphasize the importance of identifying and removing barriers to ensure syphilis testing and consequently decrease syphilis transmission among sexually active MSM.
We thank the NHBS participants.
For the full list of NHBS Study Group participants, please see Supplemental Digital Content, http://links.lww.com/QAI/B33.
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