JAYARAMAN, GAYATRI C. PhD, MPH*; READ, RONALD R. MD, PhD†‡; SINGH, AMEETA BMBS§∥
SYPHILIS IS a sexually transmitted disease (STD) caused by the bacterium Treponema pallidum. Infectious syphilis can be divided into three stages (primary, secondary, and early latent) and is usually of less than 1 year's duration. Untreated syphilis can result in serious sequelae to almost every organ system, including the central nervous system. Infection during pregnancy can result in transmission to child, miscarriage, stillbirth, or premature death of the child. Because syphilis facilitates the transmission of HIV, 1 eliminating syphilis is important not only to prevent the sequelae of infection but also to control the spread of HIV.
In 1996 Canadian experts set a national goal for reducing the rate of infectious syphilis to less than or equal to 0.5 case/100,000 population. 2 This target seemed achievable during 1997, when the rates of infectious syphilis in Canada declined to 0.4/100,000 population. 3 However, a series of local outbreaks in Vancouver, British Columbia, among commercial sex workers, 4 in the Yukon among heterosexuals, 4 and in Ottawa, Ontario, 5 and Montreal, Quebec, 6 among men who have sex with men (MSM) suggests that current prevention and control efforts have been ineffective in eliminating this disease.
We report an outbreak of infectious syphilis in Calgary, Alberta, between September 2000 and April 2002. The outbreak began among MSM and shifted to include heterosexual persons. Given the proximity of these infections in time and place, we had an opportunity to assess risk exposure-specific determinants of the outbreak.
Infection with syphilis became a notifiable condition under the public health legislation in the province of Alberta in 1929. This means that primary caregivers and laboratories are required to nominally report all individuals with newly diagnosed syphilis infection to provincial public health authorities. Public health nurses contact the attending physician for further information on the reported case and follow up with the infected individuals by counseling them about their infectiousness to others, by referring them to clinics for treatment and by identifying partners who may be unaware of their exposure.
In this analysis, we included persons with infectious syphilis diagnosed between January 1, 2000, and April 30, 2002, at the STD clinic in Calgary, Alberta. This is the only publicly funded clinic for Southern Alberta, providing services to a population base of 867,519 individuals (City of Calgary, Civic Census Summary, 2001). The clinic provides diagnosis and treatment of STDs on a walk-in basis, hepatitis B vaccination, confidential HIV testing, phone-in advice, counseling and education, contact-tracing, partner notification, and referrals. It is the only clinic in Southern Alberta to offer all these services. Public health staff members at the clinic conduct contact-tracing for suspected cases and collect demographic, epidemiologic, and clinical data on all confirmed cases.
For this study, STD clinic charts of persons with infectious syphilis diagnosed between January 1, 2000, and April 30, 2002, were reviewed to obtain demographic, epidemiologic, and clinical data. Demographic data included gender, age at diagnosis of syphilis, ethnicity, and city of residence. Epidemiologic data included sexual contact history, partner information, age at which sexual activity was initiated, sexual risk behaviors, history of drug use, and history of testing for HIV and other STDs. Clinical data included date of positive syphilis test, stage of syphilis infection, mode of presentation, and coinfection with HIV or other STDs.
Diagnosis of syphilis was made on the basis of a combination of history, clinical findings, dark-field microscopy, and serology for syphilis. Serological testing for syphilis was conducted at the Provincial Laboratory for Public Health (PLPH) with the rapid plasma reagin (RPR) test. Confirmatory testing was performed with the Treponema pallidum hemagglutination assay and/or the fluorescent treponemal antibody absorption test.
Figure 1 details the syphilis outbreak in Calgary between September 2000 and April 2002, including potential sexual networks (refer to the legend for further details). The outbreak began in September 2000 when two cases of infectious syphilis were diagnosed at the STD clinic. Between October and December 2000, six more cases of infectious syphilis were diagnosed, corresponding to a rate of 0.9/100,000 population for the year 2000. All eight cases involved MSM, and this wave of the outbreak continued through June 2001, when five more cases were diagnosed. One additional case of infectious syphilis, diagnosed in December 2001, could be attributed to male-to-male sex.
During May 2001 the first case of heterosexually acquired infectious syphilis in more than 2 years in Calgary was diagnosed at the STD clinic. Between September and December 2001, nine additional cases of infectious syphilis acquired through heterosexual contact were diagnosed at the STD clinic, for a rate of 1.8/100,000 population during 2001. During the first 4 months of 2002, eight cases of infectious syphilis were diagnosed, including the first identified case of locally acquired congenital syphilis diagnosed in more than 10 years in Calgary. All eight cases have been due to heterosexual contact (Fig. 1).
Of the 14 cases diagnosed among MSM, four were linked to sexual contacts residing in the city of Vancouver, located in the neighboring western province of British Columbia, and one individual was linked to a sexual contact in the city of Montreal, located in the eastern province of Quebec. In contrast, the outbreak among heterosexuals was solely attributable to locally acquired infections. Two individuals infected through heterosexual contact may have acquired their infection in British Columbia and then transmitted it to clients in Calgary, but this scenario is unlikely, given the stage of their infection and the dates on which they were out of the province.
The characteristics of the affected individuals are shown in Table 1. Several interesting differences were noted between the two risk groups. In general, the MSM were older than the heterosexuals, with median ages of 37 years (26–57) and 24 years (19–36), respectively. Whereas 35.7% of the MSM were coinfected with HIV, none of the heterosexuals were positive for HIV infection. For nearly one-half of the MSM (42.9%), sexual contact was initiated in bars and/or bathhouses. It is interesting that 28.6% of MSM used a single Internet chat room to arrange sexual contact with anonymous partners. Among heterosexuals, 64.7% were either commercial sex workers or their clients. Whereas 71% of MSM reported excessive alcohol use, 41.2% of the heterosexuals reported injecting crack cocaine. A small proportion of MSM (14.3%) and heterosexuals (5.9%) used other illicit noninjection drugs, such as marijuana.
Compared with cases involving MSM, the heterosexuals’ infectious syphilis tended to be diagnosed at a later stage. Whereas 92.9% of the MSM had primary or secondary syphilis diagnosed, 64.7% of heterosexuals had infectious syphilis diagnosed during these two stages. Among MSM, 90% presented at the STD clinic with lesions or ulcers characteristic of syphilis infection. In contract, 29.4% of the heterosexuals had infectious syphilis diagnosed either through routine STD screening or through contact-tracing. On average, more contacts were reported among heterosexuals than among the MSM (3 ± 2 and 2 ± 1 reported contacts per case, respectively).
Contact-tracing was initiated and completed for all individuals for whom sufficient identifying information was provided by the case. Among MSM, of 36 contacts who were identified by the cases, sufficient information was provided on 7 individuals (19.4%) for contact-tracing purposes (Fig. 1 and Table 1). Of these seven contacts, five tested positive and two negative for infectious syphilis. Of note, one of the five positive cases presented at the STD clinic before contact-tracing was initiated. Among the heterosexuals, of 62 contacts identified by the cases, sufficient information was provided on 14 individuals (22.6%) for contact-tracing purposes (Fig. 1 and Table 1). Of these 14 named contacts, 8 tested positive and 6 negative for infectious syphilis. Of note, six of the eight positive cases presented at the STD clinic before contact-tracing was initiated.
We also identified several similarities between the two risk groups. The majority of the individuals in this outbreak were white (78.5% of MSM and 88.2% of heterosexuals). All individuals for whom information was available were sexually active by 24 years of age, with the majority of individuals initiating sexual activity when they were between 15 and 20 years old. The majority of individuals (85.8% of MSM and 64.7% of heterosexuals) sought repeated testing for HIV infection. Among the heterosexuals, 29.4% were coinfected with other STDs (gonorrhea, chlamydia, and herpes) at the time of syphilis diagnosis and 35.3% had a history of infection with STD pathogens other than HIV. Among the MSM, 7.1% were coinfected with STD pathogens other than HIV at the time of diagnosis with infectious syphilis; however, 64.3% had a history of such infections.
The public health staff at the STD clinic launched a series of multifaceted interventions in response to the outbreak. In November 2000, MSM attending the STD clinic were asked to inform their peers about a potential syphilis outbreak and to refer them to the STD clinic for counseling and testing. A more formal approach in December 2000 involved the dissemination of information through a popular gay magazine. In February 2001, a second article was printed in the gay magazine to serve as a community alert. This approach was met with some success, as measured by a noticeable increase in the number of MSM seeking counseling and testing services at the STD clinic between February and June 2001. Also, three cases of secondary syphilis were identified directly as a result of individuals’ seeking testing at the STD clinic after reading the second article on syphilis in a gay community magazine.
Two approaches were used to access MSM who may be using cyberspace to meet their sex partners: (1) the Internet provider was asked to advertise in an Alberta-based chat room the services offered at the STD clinic, and (2) two physicians joined a popular gay chat room and answered questions about STDs. As a part of an effort to curb the outbreak, in March 2001, syphilis alerts were sent from the STD clinic to physicians, clinics, and hospitals in the Calgary health region. These alerts reminded health care providers of the signs and symptoms of syphilis and urged them to refer suspected cases to the STD clinic for follow-up. Because it was recognized that many of the sex trade workers were also injection drug users, in October 2001 a local needle-exchange program was asked to disseminate information about the outbreak in Calgary, to initiate syphilis testing from their outreach van and at fixed sites, and to refer their clients to the STD clinic.
Between November 2001 and May 2002, 26 syphilis tests were offered through the outreach van, and 47 tests were offered at fixed sites. No individual tested positive for infectious syphilis through these services. Since March 2002, all sex trade workers attending the clinic were given STD clinic cards to share with their customers. This latter approach was marginally successful in reaching a population of individuals who may not otherwise seek testing for STDs.
This study examined the characteristics of an outbreak of infectious syphilis propagated by male-to-male sex and heterosexual contact. The results highlight key differences in the risk factor-specific characteristics of the outbreak, despite the proximity of time and place of these infections. It also suggests some similarities between these two groups. This information should be considered in the design of prevention and control strategies.
Before this outbreak, no locally acquired cases of infectious syphilis were reported in Calgary in more than 10 years; all infectious cases were acquired either by travelers to other countries or among recent immigrants. The rate of infectious syphilis in Calgary between 1993 and 1999 ranged from 0 to 0.3/100,000 population (STD Services, Alberta Health and Wellness, unpublished data). Between September 2000 and April 2002, 32 individuals had locally acquired infectious syphilis diagnosed in Calgary, corresponding to rates of 0.9/100,000 population during 2000 and 1.8/100,000 population during 2001. At the current level of reported infections during preparation of this article, it appeared that the rate might remain at 1.8/100,000 population for 2002. Of note, the majority of these cases (30) were diagnosed at the STD clinic.
Given some inherent limitations related to this study, our findings must be interpreted with some caution. For example, a selection bias may have occurred because most individuals attending the STD clinic are seeking confidential testing. However, we identified no significant differences between the characteristics of STD clinic clientele and those of the general population in Calgary. Indeed, a geomapping exercise revealed that persons residing in all areas of the city seek the services provided at the STD clinic (S. Samanani and R. Read, unpublished data). Both males and females seeking these services belonged to a range of socioeconomic strata, ethnicities, and age groups (S. Samanani and R. Read, unpublished data). Self-reported sexual behaviors (such as the number of sex partners in the past 6 months) and drug use behaviors may be subject to recall and social desirability biases. Contact-tracing could be completed only for individuals for whom cases provided information sufficient for such investigations. Given the relatively small sample size, we could not determine whether the observed differences in the characteristics of MSM and heterosexual groups in the outbreak were of statistical significance. Finally, a thorough evaluation of the interventions could not be conducted because of resource constraints and because information on referrals and risk groups are not collected routinely from all individuals seeking testing at the STD. Nevertheless, some interesting findings merit further discussion.
Several characteristics of the current outbreak in Calgary make it unique. This outbreak can be loosely divided into two phases. In the first phase, cases of infectious syphilis were diagnosed among MSM (September 2000 to June 2001). It is interesting that during this period, reports of the resurgence of syphilis among MSM were also issued from other Canadian cities, including Ottawa 5 and Montreal, 6 in the United States, 7–10 and in Europe. 11–15 During the second phase of the outbreak in Calgary (May 2001 to April 2002), cases of infectious syphilis were diagnosed among heterosexuals. No clear links between the MSM and heterosexual components of the outbreak were identified, but a significant number of sexual contacts in both groups were anonymous and thus untraceable. Therefore, network analysis to identify further links was not possible.
Despite the close proximity in time and place of the two phases of this outbreak, several interesting differences emerge in the characteristics of persons infected via male-to-male sex and those of persons infected through heterosexual contact. Of particular concern is that 35.7% of the MSM were coinfected with HIV. Similar rates of coinfection with HIV have been reported among MSM with diagnosed infectious syphilis in the United States. 16 This relatively high level of HIV coinfection and the identified outbreak of syphilis among MSM support the suggestion that unsafe sexual practices are increasing among MSM. 17–19 Indeed, in Canada, national trends suggest a resurgence of newly diagnosed and reported HIV positive cases among MSM. 20
Because drug use has been known to promote high-risk sexual activity, our finding that 71.4% of the MSM reported a history of excessive alcohol use is of interest. In contrast, almost one-half of the heterosexuals (41.2%) reported injecting crack cocaine. The use of a needle-exchange program to disseminate information on syphilis to the injection drug-using population may have enhanced coverage of this group. This possibility needs to be explored further. However, among the heterosexual population, the outbreak in Calgary is likely associated with the exchange of drugs or money for sex. Among MSM, sexual contact was often initiated at bars or bathhouses. Also, as reported in the United States, 21,22 some MSM used the Internet to meet sex partners.
The anonymous encounters associated with commercial sex work, the Internet, and bar or bathhouse connections continue to challenge current protocols for contact-tracing and partner notification. These challenges are compounded by the fact that the majority of persons infected with syphilis through heterosexual contact whose diagnosis was established at the STD clinic had no stable housing or employment. Contact-tracing among MSM was also difficult, largely because source cases either did not know or did not correctly remember the names of sex partners they had “met” through Internet chat rooms and in the bathhouses.
Our findings that a high proportion of both groups had a history of infection with other STD pathogens and that the majority of individuals in both groups sought repeated testing for HIV indicate that these individuals had repeated contacts with health care professionals. Although post-test counseling is vital to curb the spread of STDs, it is clear that a combination of approaches is required. The multifaceted interventions conducted by public health personnel at the STD clinic were marginally successful, as measured by some increase in the number of MSM and sex trade workers and their clients who attended the clinic. We are currently exploring cost-effective ways to better quantify these increases. Unfortunately, despite all efforts, there is no clear indication that infectious syphilis rates have subsided in Calgary. We must continue to use evidence-based prevention and control strategies while developing innovative and locally relevant approaches to bringing syphilis under control.
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