Infectious syphilis in women: what s old is new again?

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1 Original research article Infectious syphilis in women: what s old is new again? International Journal of STD & AIDS 2017, Vol. 28(1) 77 87! The Author(s) 2016 Reprints and permissions: sagepub.co.uk/journalspermissions.nav DOI: / journals.sagepub.com/home/std Souradet Y Shaw 1,2, Craig Ross 1, Deborah L Nowicki 1,3, Shelley Marshall 1, Sandy Stephen 1, Christina Davies 1, Jennifer Riddell 1, Kim Bailey 1, Lawrence J Elliott 1,2,3, Joss N Reimer 1,2,4 and Pierre J Plourde 1,2,3 Abstract The aim of this study was to examine trends in infectious syphilis epidemiology among women in Winnipeg, Canada. A descriptive study of syphilis among Winnipeg residents between 2003 and 30 June 2015 was undertaken. Adjusted rate ratios (ARR) and 95% confidence intervals (95%CI) from Poisson regression analyses are reported. Characteristics of men and women were compared using logistic regression, with adjusted odds ratios (AOR) reported. Between 2014 and 2015, the rate of syphilis was 1.7/100,000, representing a five-fold increase since All cases have been heterosexual, 90% years of age, and 59% living in Winnipeg s inner core. Approximately 24% were pregnant at diagnosis; no cases of congenital syphilis have been reported. Compared to men, women were more likely to report alcohol use (AOR: 3.8, 95% CI: ) and co-infection with chlamydia (AOR: 5.0, 95% CI: ). In conclusion, the rates of infectious syphilis are increasing among women. Prenatal screening and education for inner-core women and the health care providers serving them should be prioritized. Keywords Syphilis, women, epidemiology Date received: 20 October 2015; accepted: 22 December 2015 Introduction Increases in infectious syphilis rates have been detected in almost all Canadian provinces and territories since 1997, 1,2 reflecting trends observed in other high-income countries 3. In 2012, the rate for infectious syphilis in Canada was 5.8/100,000, with 95% of cases among men, resulting in a rate 20 times higher than for women. 2 As in other jurisdictions, 3 it is thought that the burden of syphilis in Canada is borne disproportionately by men who have sex with men (MSM). Prevention and intervention efforts both in Canada and globally have therefore focused on understanding the determinants of syphilis among MSM. 3 Notably, Internet-based media have been implicated as a means for individuals to more easily find sex partners, 4 and have posed considerable challenges for public health. 5,6 Despite early optimism that MSM-specific public health approaches might stave off the epidemic, 7,8 rates of syphilis among MSM have so far continued unabated. This failure points to complex determinants which remain insufficiently addressed, 9 and unfortunately may have allowed time for syphilis, like other epidemics, 10 to evolve. While emerging within particular core-groups (in this case, MSM), epidemics may spread into, and be sustained within relatively lower-risk groups, via bridge populations that straddle different subpopulations concurrently. 10 Public health 1 Population and Public Health Program, Winnipeg Regional Health Authority, Winnipeg, Canada 2 Department of Community Health Sciences, University of Manitoba, Winnipeg, Canada 3 Department of Medical Microbiology, University of Manitoba, Winnipeg, Canada 4 Department of Family Medicine, University of Manitoba, Winnipeg, Canada Corresponding author: Souradet Y Shaw, Department of Community Health Sciences, University of Manitoba, R070 Med Rehab Building, 771 McDermot Avenue, Winnipeg R3E0T6, Manitoba, Canada. umshaw@myumanitoba.ca

2 78 International Journal of STD & AIDS 28(1) responses must therefore continue to be responsive to changes, real or anticipated, in the epidemiology of syphilis. 8 Any signals that syphilis might be spreading into heterosexual populations, and in women in particular, may signify an important shift in syphilis epidemiology. Moreover, spread of syphilis to women requires a change in public health approaches, 11,12 emphasizing the prevention of congenital syphilis. In North America, signs of increasing congenital syphilis incidence in the state of California, published in July 2015, may signal such a change. 13 Using the latest available population-based data from a major Canadian city, the objective of this analysis was to examine trends in the epidemiology of syphilis, focusing on recent trends among women. Methods Setting The Winnipeg Health Region (WHR) is the largest health region in Manitoba. In 2010, the population of the WHR was 700,000 (70% of the Manitoba population). 14 Consistent with both Canadian and global trends, the rates of infectious syphilis have been increasing in the WHR since ,15. The WHR is divided into 12 Community Areas (CAs), which are administrative areas used for planning and policy purposes. Two CAs (Point Douglas and Downtown) compose the WHR s inner-core 16 ; historically, these two CAs are characterized by relatively lower socio-economic status, and a higher burden of poorer health outcomes, including higher sexually transmitted and blood-borne infection (STBBI) rates. 14 Infectious syphilis surveillance database In Manitoba, all positive syphilis results are reportable to the provincial ministry of health. Results are then referred to Regional Health Authorities based on the client s region of residence and assigned to a public health nurse (PHN) for case management. PHNs within the Winnipeg Regional Health Authority s (WRHA) public health team complete a case surveillance form. Key variables include sociodemographic (e.g. date of birth, gender), clinical (e.g. symptoms, staging) and behavioural and social risk factor information. Data from these forms are maintained in an electronic database. Definitions Infectious syphilis was defined as all cases of primary, secondary, early latent and incubating syphilis, as per the protocol of Manitoba Health, Healthy Living and Seniors (MHHLS). 17 Staging of infectious syphilis was based on information from the testing physician, and reviewed by two WRHA Medical Officers of Health. Inclusion criteria included having a specimen collection date between 1 January 2003 and 30 June 2015, and being a resident of the WHR, defined according to postal code at the time of testing. Population data were derived from the provincial insurance registry and provided by MHHLS. Statistical methods Rate calculations. The crude annual incidence rate of infection was calculated using the corresponding midpoint population as the denominator. Rates were directly age-standardized to the 2006 Canadian population (provided by Statistics Canada) and 95% confidence intervals (95%CI) were calculated using the Tiwari et al. 18 formula. Descriptive analysis. Information was grouped into five categories: infection characteristics, demographics, coinfections, meeting places and risk factors. Although PHNs are highly trained to query cases/contacts, certain information (e.g. ethnicity, meeting places, behavioural risk factors) may not always be captured. Thus, information is incomplete for some questions. Cases are described by time period of infection, with years being grouped based on empirical evidence of changes in syphilis incidence. For the purpose of this analysis, years are grouped into , , and Briefly, the interval between 2003 and 2005 saw an outbreak of syphilis among heterosexual couples in Winnipeg. The interval between 2006 and 2013 saw two outbreaks among MSM (with the 2013 outbreak still ongoing). The last interval ( ) was chosen due to our interest in examining the most recent available data, as well as a marked increase in the number of women reporting infectious syphilis, starting in Given the small number of cases in women (N ¼ 52), only results from bivariate analyses are presented, using Pearson s Chi square test of association to detect differences by period. Multivariable modeling. Poisson regression models were used to test the association between independent variables and rates of syphilis among women over the three time periods, with the logarithm of the population used to calculate rates. The availability of population data for a select number of variables limited the number of variables that could be used. Thus, for the purposes of regression modeling, age group (<20, 20 29, and 40þ years), year of infection ( , , and ), and geographic residence (inner-core

3 Shaw et al. 79 vs. non-core) were inputted as independent variables. Rate ratios and 95% CIs from bivariate and multivariable analyses were produced. For multivariable analyses, all three independent variables were entered into a single multivariable model. Comparison between men and women. Men and women diagnosed between 1 January 2014 and 30 June 2015 were compared on infection characteristics, demographics, co-infections, meeting places and risk factors using Pearson s Chi square tests of association in bivariate analyses. Variables significant at the p <.20 level, and where cell sizes were greater than 1, were retained as dependent variables for the purposes of multivariable modeling. The main objective was to test the association between female sex (the primary independent variable) and each of the variables significant at the p <.20 level in bivariate analyses. A priori, each model was adjusted for age group, ethnicity and residency in the inner core. Adjusted odds ratios (AOR) and 95% CIs from multivariable logistic regression analyses were produced. All analyses were performed using Stata 13 (StataCorp, College Station, TX). All two-way interactions were tested using the user-written mfpigen program in Stata. Sexual network visualization. Contact-tracing data were collected and entered into a database for cases diagnosed since 1 January For the purposes of these analyses, the network diagrams focus only on the eight women diagnosed in Network diagrams were produced using Ucinet. Results The age-standardized rate of syphilis among women was 1.2/100,000 (95% CI: ) between 2003 and 2015 (n ¼ 52; Table 1). Also, the rates among men (8.8/100,000; 95% CI: ) were over seven times higher. For women, the age-standardized rate was 3.2/100,000 (95% CI: ) between 2003 and 2005, 0.3/100,000 (95% CI: ) between 2006 and 2013, and then rebounded to 1.7/100,000 (95% CI: ) between 2014 and No cases of congenital syphilis were diagnosed during this time period. Descriptive analysis Results from bivariate analyses are shown in Table 2. Almost all cases were heterosexual. In the most recent time period (i.e ), approximately 41% of women were staged as primary syphilis, 35% as early latent, and 18% as secondary syphilis (p ¼.143). Fiftynine percent were from the inner core of the WHR (p ¼.224) and 59% self-identified as Aboriginal (p ¼.563, 77% of those who reported an ethnicity). Approximately 24% were pregnant at the time of diagnosis (p ¼.311); all pregnant women were followed by public health and provided appropriate prenatal care. Chlamydia co-infection was high, at 24% (p ¼.804), while there was an absence of HIV or gonorrhea coinfections. Bars (18%, p ¼.087) and the web/ Internet (including social media sites and networking apps ), at 18% (p ¼.038), were the most commonly reported ways of meeting sex partners, although most women reported none of the options. Finally, selfreported engagement in sex work (6%) was lower in the most recent time period than in earlier time periods (e.g. 26% in , p ¼.214), while reported noninjection drug use (29%) was higher than other time periods (p ¼.052). Network visualization (Figure 1) revealed that two women who were reported to public health in 2015 were connected to the largest component (a component is a network structure where a path exists from any one node to any other node), comprised of 205 individuals (34% of cases and contacts from 2013 onward). This component had a mix of MSM, bisexual and heterosexual sexual cases and contacts, and contained Table 1. Frequency and age-standardized rates (per 100,000), infectious syphilis, by sex, winnipeg health region ( ). a Females Males Total Year Number Agestandardized rate 95% CI Number Agestandardized rate 95% CI Number Agestandardized rate 95% CI Total a Up to 30 June 2015.

4 80 International Journal of STD & AIDS 28(1) Table 2. Selected characteristics, female infectious syphilis cases, WHR ( , n ¼ 52). a Total No. % No. % No. % No. % p b Infection Characteristics Transmission Heterosexual Bisexual Staging Primary Secondary Early latent Incubating Number of contacts þ Demographics Age group < þ Inner-core Non-core Inner-core Ethnicity Caucasian Aboriginal Other No information Pregnant No Yes Co-infections HIV status <0.001 HIV Negative HIV Positive Chlamydia positive No Yes Gonorrhea positive No Yes HBV positive No Yes HCV positive No (continued)

5 Shaw et al. 81 Table 2. Continued Total No. % No. % No. % No. % p b Yes Meeting places Met in bathhouse No Yes Met on chatline No Yes Met on web/internet No Yes Met at bar No Yes Met at hotel No Yes Risk Factors Sex worker No Yes Injection drug use No Yes Non-injection drug use No Yes Alcohol use No Yes a Up to 30 June 2015 and includes incubating, primary, secondary, early latent & incubating who were Winnipeg Health Region residents. b Based on Pearson s Chi square test. individuals who were part of the original 2013 outbreak among MSM, illustrating the evolution of the syphilis outbreak. Both women were under the age of 24, selfidentified as Aboriginal, and were residents of the inner core (not shown). Multivariable models Results from Poisson regression models examining the association between age, year and geographic residence on rates of syphilis among women are reported in Table 3. Compared to those years of age, rates were significantly lower among those <20 years [adjusted RR (ARR): 0.1, 95% CI: ] and 40 years or older (ARR: 0.2, 95% CI: ). Rates among women residing in the inner core were eight-fold higher (ARR: 7.6, 95% CI: ) compared to non-core residents, adjusted for age group and year of infection. Compared to , the rates were significantly higher in (ARR: 5.4, 95% CI: ). A statistically significant interaction (p ¼.021) between age group and geographic area was detected. Addition of the interaction term did not substantially change the strength or statistical significance of the increase in rates observed between 2014 and 2015 (Supplemental Table S1). However, using 20- to 29-year-old women who did not reside in the inner core as reference, 20- to 29-year-old (adjusted RR: 5.0, 95% CI: ) and 30- to 39-year-old

6 82 International Journal of STD & AIDS 28(1) Figure 1. Sexual network, infectious syphilis cases and contacts, Winnipeg Health Region (1 January June 2015). Note: Women connected to men who have sex with men/bisexual cases circled. Table 3. Crude rates (per 100,000), and rate ratios and 95% confidence intervals from Poisson regression models, female infectious syphilis cases, Winnipeg Health Region ( ). a Crude rate Model I b Crude rate ratio (95% CI) Model II b Adjusted rate ratio (95% CI) Age group (years) < ( )* 0.1 ( )* Ref Ref ( ) 1.2 ( ) 40þ ( )* 0.2 ( )* Year ( )* 8.2 ( )* Ref Ref ( )* 5.4 ( )* Geographic area Non-core 0.47 Ref Ref Inner-core ( )* 7.6 ( )* a Up to 30 June b Model I: bivariate analyses; Model II: multivariable analysis, includes all variables in Table 3. *p <.001 (adjusted RR: 7.3, 95%CI: ) inner-core women had significantly higher rates of infectious syphilis over this time period. All other two-way interactions were not statistically significant at the p <.05 level. Results from bivariate analyses comparing men and women diagnosed from 2014 onwards are displayed in Table 4. All 17 women reported being heterosexual. Women were more likely to report Aboriginal ethnicity (59% vs. 18%, p <.001), be co-infected with chlamydia at the time of their syphilis diagnosis (24% vs. 5%, p ¼.003), and more likely to report alcohol use (53% vs. 18%, p ¼.001). Women were less likely to be HIVinfected (0% vs. 27%, p ¼.013), and to report meeting their partner on the web/internet (18% vs. 48%, p ¼.019). Variables meeting the criteria for multivariable analyses included chlamydia positivity, meeting on the web/internet and alcohol use. Adjusted for age group, ethnicity and inner-core residency, and compared to men, female infectious syphilis cases were 5.0 times the odds of being co-infected with chlamydia (95% CI: ) and 3.8 times the odds of reporting alcohol use (95% CI: ). Discussion Despite the hope that syphilis might be eliminated early in the twenty-first century, 8 and the belief, as recently as

7 Shaw et al. 83 Table 4. Selected characteristics, male and female infectious syphilis cases, WHR ( ). a Female Male Total No. % No. % No. % p-value b Ratio (95% CI) c Adjusted Odds Transmission <0.001 Heterosexual Bisexual MSM only Unknown Staging Primary Secondary Early Latent Incubating Number of contacts þ Unknown Age group < þ Inner core Non-core Inner core Ethnicity <0.001 Caucasian Aboriginal Other No information HIV status HIV-negative HIV-positive Chlamydia-positive No ( )* Yes Gonorrhea-positive No Yes HBV-positive No Yes HCV-positive No Yes Met in bathhouse No (continued)

8 84 International Journal of STD & AIDS 28(1) Table 4. Continued. Female Male Total No. % No. % No. % p-value b Ratio (95% CI) c Adjusted Odds Yes Met on chatline No Yes Met on web/internet ( ) No Yes Met at bar No Yes Met at hotel No Yes Pregnant <0.001 No Yes Sex trade worker No Yes Injection drug use No Yes Non-injection drug use No Yes Alcohol use ( )* No Yes a Includes incubating, primary, secondary, early latent & incubating who were Winnipeg residents. b Based on Pearson s Chi square test. c Variables significant at the p <.20 level were used as dependent variables in multivariable logistic regression models, with female sex entered as the main independent variable, adjusted for age group, inner-core residency and ethnicity. *p < , that locally acquired syphilis was curtailed in Manitoba, 15 our results suggest a more sobering reality. In addition to the re-emergence of syphilis among MSM, syphilis among women is also now increasing in the WHR. For comparison, our age-standardized rate of 1.7/100,000 between 2014 and 2015 among women was higher than the latest available data from the USA (0.9/100,000 in 2013), as well as the highest rate observed in the USA between 2005 and 2013 (1.5/100,000 in 2008). 19 In the UK, the rate for women was 1.0/100,000 in Finally, in 2012, the latest year where data are available for Canada, the rate was 0.5/100,000 for women. 2 In the WHR, women years of age residing in the inner-core were the most at risk for infection. In some ways, our findings reflect characteristics of syphilis-affected heterosexual populations in the Canadian province of Alberta in 2002, as reported by Jayaraman et al. 12 There, compared to MSM cases, heterosexual transmission tended to affect younger populations, and occurred in the absence of co-infection with HIV. A shift in syphilis transmission

9 Shaw et al. 85 from MSM to heterosexual populations was also documented in Manitoba in the mid-1980s. 21 In this outbreak, rates of syphilis among women increased six-fold in one year, from 0.4 to 2.5 per 100,000, while the number of infections attributable to MSM was almost unchanged. The authors hypothesized that the plateau in MSM cases may have been due to sexual behaviour change in the context of the AIDS epidemic, 21 while increases among heterosexuals was attributed to bisexual male bridge populations and sex workers. 21 Sex work was also a factor in the 2002 Alberta heterosexual outbreak. 12 Although the role of bisexual bridge populations likely remains important, we found few similarities with the mid-1980s outbreak in Manitoba. First, the increase in incidence among women in the current outbreak accompanied an increase in incidence among MSM; increased numbers among heterosexuals may therefore be a product of an overall increase in the epidemic, as opposed to a shift per se. Second, we found little reported engagement of infected women in sex work, recognizing that this information may be especially unlikely to be communicated to PHNs during case investigations due to prevailing stigma, especially for cases who are pregnant or parenting. 22 Regardless, little evidence exists clearly linking present-day sex work occupational exposures to the current rates of syphilis among women in Winnipeg. Both (self-reported) Aboriginal ethnicity and residence in Winnipeg s inner-core were important features of the ongoing outbreak in our locality. Over the entire analysis period, 67% of female cases reported Aboriginal ancestry (35/52). Stratified by residency, 83% (29/35) of inner-core cases reported Aboriginal ancestry, compared to 35% (6/17) of non-core cases (data not shown). Canadian Aboriginal populations are often highly stigmatized and are subjected to institutionalized and structural forms of oppression and racism, 23 leading to a disproportionate burden of STBBIs. In the USA, a body of literature has demonstrated how structural vulnerabilities impacting African-American communities (e.g. socio-economic exclusion, geographic ghettoization, and high incarceration rates) have amplified the risk for STBBIs. 8,24 26 In light of Manitoba having the highest incarceration rate of all Canadian provinces, with Aboriginal offenders disproportionately represented, 27,28 the current outbreak dynamics may therefore be impacted by structural determinants, such as an unbalanced male-to-female sex ratio in the urban Aboriginal community. This is supported by our finding that most women did not report a meeting venue, nor did they report using the web or Internet to seek partners, suggesting partners may be primarily drawn from local personal social and romantic networks. This differs greatly from the dynamics of the local MSM syphilis outbreak, where a more diverse geographic and demographic profile is observed, as well as a high prevalence of social media used to meet sexual partners. The high prevalence of co-infection with chlamydia and alcohol use among women, in comparison to men, is of some interest. As the primary risk group is inner-core women of Aboriginal ethnicity in this latest outbreak, the lack of mixing with non-core men may explain the high prevalence of chlamydia co-infection. Alcohol use has been shown to be highly associated with depression and risky sexual behaviour among young minority women 29 ; interventions may thus need to include mental health and substance use components. Control of syphilis requires interventions to take into account factors on a variety of levels, including individual, interpersonal, community and structural. Thus, further research into understanding the determinants of transmission among women is warranted. Alongside research and surveillance, programmatic nimbleness is needed to make an impact on syphilis rates. 8 In this regard, the WRHA s public health team has recently consulted community partners to engage in a dialogue on which future interventions may be built. Although the increased number of syphilis cases among Winnipeg women is worrisome, incident cases remain relatively manageable, pointing to the importance of prioritizing follow-up with cases and contacts, who necessarily comprise the most susceptible pool. A continued rise in cases among women may necessitate further education of local health care providers, who may have difficulty identifying symptoms of such an uncommon infection. Syphilis screening is included in prenatal screening for all pregnant women in Manitoba, undoubtedly contributing to the absence of any congenital syphilis reported in the WHR during our study period. Considering that access to prenatal care is itself impacted by structural factors, 30 initiatives aimed at eliminating barriers to prenatal care are recommended; for example, the WRHA is currently implementing the Partners in Inner-city Integrated Prenatal Care initiative, which seeks to address inequities in prenatal care among inner-city women in Winnipeg. 31 Strengths and limitations Our analyses benefit from a number of strengths, including the use of population-based data sources, instead of using self-reported data on infections, or data from select clinical populations. There are also several limitations to our study. First and foremost, behavioural and partner-side information was limited. Second, the numbers for 2015 are only to mid Third, data likely underestimate the actual incidence of syphilis as the database is based on laboratory

10 86 International Journal of STD & AIDS 28(1) confirmation of cases. Fourth, in 2014, a change in syphilis testing algorithm was implemented in Manitoba whereby Chemiluminescent Microparticle Immunoassay (CMIA) testing was used as the initial screening test, followed up with the venereal disease research laboratory (VDRL) test as a confirmatory test. Although this change in algorithm could have impacted the number of cases detected, the changes were implemented as a means to reduce the amount of false positives; thus a decrease in the number of reported cases would have been expected, absent a real increase in incidence of syphilis among women. As well, given the bridging observed through network analysis, from MSM to bisexual and finally to heterosexual networks, we feel that observed increase in cases among women is not merely an artifact of a change in testing algorithm. Fifth, the higher proportion of women reporting alcohol and drug use (compared to men) may have been influenced by greater emphasis placed on these questions during prenatal screening. In conclusion, our analyses indicate a changing dynamic in the epidemiology of syphilis, impacting women in the city of Winnipeg, and reflecting the changing dynamics of syphilis epidemiology observed elsewhere. 13 Although the needless tragedy 13 of congenital syphilis cases has so far been avoided in Winnipeg, given the evidence that young inner-core women are most likely to be most vulnerable, and that so far, one in four cases have been pregnant at the time of testing, vigilance within this population needs to be maintained. Authors contributions SYS conceptualized the analysis, performed the analysis and wrote the first draft of the manuscript with CPR. SM, SS, CD and JR collected the data and provided critical and intellectual feedback on the interpretation of findings as well as implications. DLN contributed to the design of the analysis and provided important critical and intellectual feedback to the manuscript. CPR, KB, LJE, JNR and PJP provided extensive interpretation of the data and were involved in revising the manuscript critically and made important intellectual contributions. All authors have given final approval for the manuscript to be published, and all agree to be accountable for the work. Declaration of conflicting interests The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article. Funding The authors received no financial support for the research, authorship, and/or publication of this article. References 1. Public Health Agency of Canada. Report on sexually transmitted infections in Canada: Ottawa, ON: Centre for Communicable Diseases and Infection Control, Infectious Disease Prevention and Control Branch, Totten S, MacLean R and Payne E. 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