Niccolai, Linda M. PhD*; Livingston, Kara A. BA*; Richardson, Wanda BA†; Jenkins, Heidi BA†
SINCE THE FIRST OUTBREAKS in the current syphilis epidemic occurred in 1999,1,2 a number of studies have been conducted to describe the resurgence in North America and Western Europe. A review of these studies indicates that the increases are predominantly among men who have sex with men (MSM), the median age group is 35–39 years, most cases have been among whites (though recent increases among minorities have been observed3), and HIV positivity ranges from 48 to 64%.4 The current epidemic has been associated with certain behaviors, including anonymous and/or multiple sex partners and the use of illicit drugs including methamphetamine and sildenafil (e.g., Viagara). Unfortunately, this epidemic does not yet show signs of abatement, with annual increases in primary and secondary syphilis rates exceeding 10% for every year since 2000.5
Mixing patterns among infected and susceptible individuals is a key dimension of infectious disease epidemiology. Nationally, sex partner meeting venues appear to be an important element of transmission dynamics in the context of the current syphilis epidemic, and various reports have provided estimates of the prevalence of meeting sex partners in venues among MSM with syphilis. Select estimates include gay bars and clubs reported by 20% of 415 cases in San Francisco in 2002 and 49% of 88 cases in New York City in 2001; bathhouses reported by 13% of 415 cases in San Francisco in 2002, 26% among 66 cases in southern California in 2000, and 52% of 88 cases in New York City in 2001; Internet use reported by 3% of 66 cases in southern California in 2000, 14% of 103 cases in New York City in 2001, 23% of 850 cases in Los Angeles county in 2001–2003, and 55% of 53 cases in San Francisco in 2002–2003; public spaces reported by 19% of 53 cases in San Francisco in 2002–2003 and 22% of 103 cases in New York City in 2001; private parties reported by 33% of 88 cases in New York City in 2001; and bookstores reported by 6% of 415 cases in San Francisco in 2002.6–12 In these venues, it can be relatively easy to have multiple, anonymous sex partners during a relatively short period of time. Fifty percent of MSM with syphilis reported having anonymous sex in one report,6 and 88% of all sex partners were met at anonymous venues in another report.1
Travel is another element of mixing patterns that is an important determinant of the spread of infectious diseases, though this has not been studied as extensively in the context of the current syphilis epidemic. The mobility of MSM who travel for circuit parties or to visit certain venues (e.g., bathhouses), who use the Internet to meet distant sex partners, or who meet sex partners during travel for other reasons are of concern for rapid geographic dissemination.4,13 Though travel is often mentioned through an association with Internet use14 or circuit parties15 empirical data are lacking. In one report of MSM with syphilis in San Francisco, 25% of Internet partners were not local.8
Most of what we know about the current epidemiology of syphilis has been reported from major cities with large MSM communities that have experienced relatively large epidemics.1,2,7,9–11 Much less is known about the current epidemiology of syphilis in other parts of the United States. We recently reported the spatial epidemiology of early syphilis among men in Connecticut,16 a state with relatively small metropolitan areas and a primary and secondary (P&S) syphilis rate below the national average (1.3 vs. 2.7 per 100,000 population).5 Using enhanced surveillance data from 2004, we observed geographic dispersal of cases within the state and a high proportion of out-of-state sex partners, suggesting that Connecticut is not a core area of endemic transmission. The goal of the current study was to explore trends over time in sex partner meeting venues and out-of-state sex partners, 2 important elements of mixing patterns critical for understanding the spread of sexually transmitted infections, in the context of the current syphilis epidemic in Connecticut. Specifically, our analytic objectives were to: 1) describe the prevalence of meeting sex partners in venues and having out-of-state sex partners among cases of syphilis among MSM in Connecticut from 2000 to 2005; 2) examine trends in and correlates of meeting partners in sex venues and having out-of-state sex partners; and 3) estimate the association between these 2 factors. Knowing how and where MSM with syphilis meet sex partners is critical for prevention of further spread of infection.4
Materials and Methods
The present analyses are based on data routinely collected by the Connecticut health department for disease control activities. As in all states, reporting of early syphilis (P&S and early latent) by providers and laboratories is mandated by law. Standardized surveillance case report forms provide information about age, sex, race/ethnicity, town of residence, and stage of infection. Disease Intervention Specialists (DIS) then conduct in-depth, face-to-face interviews with cases to provide counseling and education, to ensure adequate treatment, and to initiate partner notification in which identifying and locating information about sex partners is obtained so that they may be notified of their potential exposure and the possible need for treatment. In addition to the standard case report form, DIS complete a locally developed 2-page record to capture more detailed information from cases. In 2002, in response to the syphilis resurgence observed nationally, a more detailed protocol for interviewing cases was developed. Two notable changes relevant for the current analysis were the inclusion of data collection on sex partner meeting venues (including Internet) and the specific location of out-of-state sex partners. Also, rather than relying on individuals' initiating the report of behaviors and partner characteristics, DIS actively asked all questions on the 2-page record of all MSM cases. After the interview, the DIS supervisor reviewed all reports for completeness and consistency across DIS. The relatively small number of cases and DIS in the state allow for systematic review of this information.
All cases of early syphilis among MSM from 2000 to 2005 were included in the present analyses. Because of the small number of cases in 2000 (n = 4), the years 2000 and 2001 were combined for all subsequent analyses. Sex partner meeting venues consisted of all places reported by cases when asked by DIS during interviews and included gay bars and clubs, bathhouses, the Internet, public spaces, private parties, bookstores, newspaper advertisements, and massage parlors. Location of sex partners during the time in which cases likely acquired their infection was classified as in-state and out-of-state. Correlates of meeting sex partners in venues and having out-of-state sex partners were determined by likelihood ratio χ2 tests and logistic regression modeling. Potential correlates included age (≤30 vs. >30 years), race (white vs. nonwhite), diagnosis (P&S vs. early latent), residence of case (metropolitan vs. nonmetropolitan), clinic of diagnosis (public vs. private), and self-reported HIV status (positive vs. negative/unknown). Metropolitan residence included living in the cities of Bridgeport, Hartford, New Haven, or Stamford; all other towns were considered nonmetropolitan. Trend tests were conducted to determine the association of year of diagnosis with meeting sex partners in venues and having out-of-state sex partners. In the multivariable models, year of diagnosis was modeled as both continuous and categorical (“dummy coded”) variables; these models were compared using goodness-of-fit tests to assess the appropriateness of modeling a linear trend. The relationships between meeting sex partners in specific venues and having out-of-state sex partners were described by 2-way associations and corresponding likelihood ratio χ2 or Fisher's exact P-values as appropriate.
All data used in this study existed before the start of research and no further contact with patients was necessary, and study staff did not obtain any identifiable information about any case or sex partner (e.g., name, description, or specific locating information). This study was exempt from review by the Yale University institutional review board.
A total of 185 cases of syphilis were reported among MSM in Connecticut from 2000 to 2005 (Table 1). An additional 52 cases among men not reporting sex with men and 42 cases among women were not included in the present analyses. The median age of these cases was 36.1 ± 9.5 years, and 56% were white. The number of cases per year increased dramatically during this time period, from 4 in 2000 to 60 in 2005, representing 10–52% increases per year for each year included in the analysis. Forty percent of the cases lived in metropolitan areas, and 37% of the cases self-reported HIV-positive serostatus.
Sex partner meeting venue information was systematically collected beginning in 2002, and was therefore available for 166 out of 185 cases (90%). Fifty-two percent (n = 86) of cases reported meeting sex partners at one or more venues that facilitate multiple and/or anonymous sexual encounters. These venues are reported in Table 1. The most common venues were gay clubs or bars (22%), Internet (18%), and adult bookstores (12%). Eighteen individuals (11%) reported using more than one type of venue. Likelihood ratio χ2 tests revealed bivariate associations between meeting sex partners in venues and older age (P = 0.07), later year of diagnosis (P = 0.04 by trend test), and nonmetropolitan residence (P = 0.05) (Table 2). The significant temporal trend is shown in Figure 1. Multivariable logistic regression modeling revealed that independent correlates of meeting sex partners in venues were later year of diagnosis and nonmetropolitan residence of the case (Table 2).
Forty-three percent (79 of 185) of the cases reported having an out-of-state sex partner during the time in which they likely acquired their infection. Specific locations of out-of-state sex partners are reported in Table 1 and represent geographically diverse areas. Likelihood ratio χ2 tests revealed bivariate associations between having an out-of-state sex partner and white race (P = 0.04), and earlier year of diagnosis (P = 0.002 by trend test, Fig. 1). Multivariable logistic regression modeling revealed only earlier year of diagnosis was an independent correlate of having an out-of-state sex partner (Table 2).
Venues that were significantly associated with having an out-of-state sex partner included bathhouses and bookstores (Fig. 2). The use of bathhouses was positively associated (10% of those who had an out-of-state sex partner visited bathhouses vs. 1% of those who did not have an out-of-state sex partner, P <0.05). The use of bookstores was negatively associated (4% of those who had an out-of-state sex partner visited adult bookstores vs. 18% of those who did not have an out-of-state sex partner, P <0.05).
In this report, we examined meeting sex partners in venues that facilitate multiple and/or anonymous sexual encounters and having out-of-state sex partners during the time in which cases likely acquired their infection among MSM with early syphilis in Connecticut, a moderate prevalence state. We found use of many venues similar to reports from major urban areas, such as gay bars or clubs and the Internet, consistent with estimates in the lower range reported elsewhere (e.g., we found gay bars or clubs used by 22% of cases, vs. 20–49% reported in other populations7,8,10). We found a greater use of bookstores among syphilis cases (12% in our sample vs. 6% reported by others8), and lower use of bathhouses (5% vs. 13–52%6,7,8,10). These findings reflect what is known about local opportunities to meet sex partners.
Health department staff has long been aware of the popularity of local bookstores, and there are no bathhouses in Connecticut. We also observed that cases who met sex partners in venues were more likely to reside in nonmetropolitan areas, perhaps reflecting limited local opportunities to meet sex partners in small towns. The use of targeted venue-based prevention has been implemented in other places,16–18 and similar efforts have taken place in Connecticut. For example, the health department is collaborating with a local community-based organization to conduct syphilis testing in gay bars, a poster campaign with phone numbers to call for testing in adult bookstores, and partner notification activities over the Internet. These efforts may be especially important in places like Connecticut where many cases (60% in the current study) reside in small towns and the use of venues is increasing over time. In Connecticut, we observed an increase in the proportion of cases meeting sex partners in venues to a high of 63% in 2005; reasons for this trend are not clear, and to what degree it will continue is unknown.
Our finding that 43% of cases acquired their infection from an out-of-state sex partner supports our previous work,19 and reinforces the challenges faced in conducing partner notification in the current epidemic. It has been suggested that the role of travel is important in the current syphilis epidemic,8,14,15 and this may be particularly true for nonmetropolitan areas such as Connecticut. In the present analyses, we extended our earlier findings by examining trends over time and quantifying the relationship to meeting sex partners in venues. The decline in having out-of-state sex partners among cases over time, from >50% in 2000–2002 to 27% in 2005, suggests that transmission within the state may be increasing. Although this may increase the utility of local prevention efforts such as partner notification, it may also be a signal that transmission beyond the core group of MSM is beginning to occur. In 2004, the national rate of P&S syphilis among women did not decrease and the number of cases increased slightly for the first time in the current epidemic,5 perhaps an indication that this is beginning to occur nationally.
This analysis has several limitations that must be considered. First, these data are based on health department reports that are subject to limitations of surveillance data such as passive reporting by health care providers and laboratories and self-reported behavioral information from cases. Furthermore, in our analysis of the relationship between meeting sex partners in venues and having out-of-state sex partners, we do not know for certain that venue use occurred while traveling because venue location was not systematically collected. Finally, though not necessarily a limitation of the current study, it should be noted that the generalizability of these findings to other moderate prevalence regions of the United States is unknown.
In conclusion, trends in syphilis in Connecticut from 2000 to 2005 that show significant declines in acquiring infections from out-of-state sex partners suggest that transmission within the state may be increasing. Furthermore, knowledge about the increased use of venues to meet sex partners can be used to target local prevention efforts. The overall increase in cases in the state during this period makes prevention efforts urgent, and continued monitoring of spread within and beyond the current core group of MSM is greatly needed.
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