THE NATIONAL PLAN TO ELIMINATE syphilis from the United States was launched in October 1999.1 Disease eradication (defined as the “permanent reduction to zero of the worldwide incidence of infection”) was not considered feasible because of high rates of syphilis in many parts of the world. However, disease elimination (defined as “controlling the manifestations of a disease so that it is no longer considered a public health problem” or as “reduction to zero of a specified disease in a defined geographic area as a result of deliberate efforts”) was considered plausible for the United States both because of historically low rates of infection and restriction to a limited number of geographic areas, as well as the availability of cheap and effective diagnostic tests and therapy. The plan defined syphilis elimination at the national level as the absence of sustained transmission in the United States, with an operational goal of ≤1000 cases of primary and secondary syphilis reported per year. Modeling projections estimated that with implementation of a fully funded elimination program, reported cases could be reduced by almost 80% by 2003, while, without the program, cases would likely increase by over 40% (Table 1).
In many respects, there has been great progress in syphilis elimination in the United States since 1998, with the declines that had been occurring in the 1990s before the launch of the national plan continuing in most populations. Racial disparities, a major focus of syphilis elimination, have been markedly reduced. The black:white rate ratio of primary and secondary syphilis fell from 34 in 1998 to 5 in 2003.2,3 Although this change is in part attributable to increased rates per 100,000 among whites from 1998 to 2003 (0.5–1.5), it a reflects a substantially larger absolute decrease in rates among blacks (16.9–7.8).2,3 Among women, cases have decreased from 3100 cases to 1218 (Table 1), a 61% reduction not far from the 80% decrease that had been projected. In addition, over the same time period, reported cases of congenital syphilis, one of the most devastating consequences of syphilis, decreased by more than 50%, from 841 to 413.2,3 Finally, syphilis has continued to remain geographically concentrated despite its reemergence in some areas where it was previously quite rare.4,5 From 1998 to 2003, the proportion of counties reporting no cases of primary and secondary syphilis increased slightly, from 78% to 81%, while the number of counties responsible for 50% of reported cases decreased from 28 to 19.2,3
However, as described by Peterman et al.,6 the downward trend in overall cases of syphilis began to reverse in 2001, with increases occurring each year since then. This increase has occurred only in men, among whom numbers of reported cases increased 52% from 1998 to 2003, and it appears likely that the change is largely attributable to cases among men who have sex with men (MSM). Although sex partner gender is not presently included in national surveillance data, this premise is supported by reports of outbreaks of syphilis in MSM from a number of large US cities4,5,7 and by the steady increase in the male:female case ratio of cases of primary and secondary syphilis since 1998 (Table 1). Estimates from models based on changes in the male:female case ratio over time indicate that by 2003, MSM comprised over 60% of US cases of primary/secondary syphilis (Heffelfinger J et al. Trends in primary and secondary syphilis in the United States: the reemergence of syphilis among men who have sex with men; submitted for publication). The rise of cases in MSM in the United States is consistent with observations from many other developed countries.8 The reasons for the resurgence remain unclear; however, increases in high-risk sexual behavior (contributed to by both improvements in human immunodeficiency virus [HIV] treatment and increases in recreational drug use), demographic changes in MSM populations (including the growth of the prevalent diagnosed HIV infected MSM population), and expansions in social and sexual networks facilitating rapid partner change all appear to be contributory.9
Syphilis control in the United States was initiated by Surgeon General Thomas Parran in 1937 based on 5 key elements: (1) case finding through serologic screening; (2) prompt, effective therapy for infected persons; (3) identification of people exposed to infectious syphilis; (4) mandatory serologic evaluation of people who might transmit infections to others (including premarital and obstetric screening); and (5) public education about the disease manifestations and consequences.10,11 Although this approach was successful in dramatically reducing syphilis rates in the United States over the next 60 years, US rates remained substantially higher than in most developed countries, with marked racial disparities. Thus, the 1999 plan was based on a new set of approaches that expanded upon, but did not replace, Parran’s traditional elements. These approaches included 2 cross-cutting strategies (enhanced surveillance and strengthened community partnerships) that were tools for evaluating and facilitating implementation of 3 specific intervention strategies (rapid outbreak response, expanded clinical and laboratory services, and enhanced health promotion).1 A geographic focus was established to concentrate efforts primarily on areas with current high rates of syphilis (high morbidity areas) and secondarily on areas with high potential for syphilis reemergence (potentially reemergent areas), based on past high rates or large populations of persons from groups traditionally at high risk for syphilis. Although this approach has been successful in the originally targeted communities of minority heterosexuals, the resurgence of syphilis among MSM raises important concerns and indicates that each of the 5 strategies of the elimination plan needs to be critically examined and refocused.
First, enhanced surveillance remains a cornerstone of syphilis control and elimination efforts. Syphilis surveillance is more than just tracking disease trends. Good disease-control activity assures that persons with syphilis are treated appropriately, while outstanding disease control provides treatment early enough to reduce transmission. Reaching cases early enough to accomplish this objective requires continued emphasis on rapid reporting after diagnosis. Thus, effective surveillance provides the basis for public health activities targeted at high-risk individuals and vulnerable communities, as well as for evaluating the effectiveness of prevention interventions. One obvious deficiency in existing national surveillance data, the lack of reporting on gender of partners, is now being addressed. Such information will help identify changes in disease incidence among MSM at the national level. Other relevant information, such as HIV status, geographic and social networks for syphilis transmission, and commercial sex venues involved in transmission, may be more readily available from local research and enhanced surveillance efforts, as described in the reports in this issue from San Francisco and Florida.12,13 Such activities may complement more routinely collected surveillance data, thereby enhancing our ability to better target prevention efforts. In addition, because health care facilities outside of STD clinics are the source of a large and growing proportion of reported cases of syphilis in men in general2,3 and of MSM in particular,12,14 there is a need to build collaborative relationships with, and encourage rapid reporting from, those providers. In this regard, community partnerships are as important for surveillance activities as they are for the other strategies of the syphilis elimination plan. Finally, as the resurgence of syphilis among MSM may presage increases among heterosexual populations, surveillance systems should be attentive to evidence of bridging of syphilis into new populations, especially women of childbearing age.
Second, strengthened community partnerships are likely to be as important for elimination of syphilis among MSM12,13 as they appear to have been in the recent past for HIV prevention in this community.15,16 In both populations, issues such as restoring and building trust and ensuring the development of culturally competent interventions are crucial. Thus, attention must be paid to identifying and engaging key opinion leaders within the MSM community who influence men’s health, health-seeking or sexual risk behaviors. In so doing, consideration should also be given to the diversity within the MSM community, especially about variations in cultural and ethnic backgrounds, HIV status, and identification and affinity to the gay community. Of importance, as was the case for communities with high rates of syphilis in heterosexual minorities, syphilis alone is unlikely to arouse much concern among MSM who are dealing with other health and social issues, in this case, HIV infection, methamphetamine abuse, and discrimination issues. This situation suggests that interventions may be more successful if they take a broader “wellness approach” that links syphilis prevention with other health concerns, such as the efforts described by Blank et al.17 Establishing working partnerships with and mobilizing key healthcare professionals (e.g., HIV providers and private practitioners) who work with MSM can form a foundation from which other activities can develop. These partnerships include collaborations with the owners of establishments where MSM are likely to socialize or meet new sexual partners (including internet websites and chat rooms) as summarized in the paper by Taylor et al.18
Third, rapid outbreak response in areas with predominantly MSM syphilis presents new challenges. Many MSM with syphilis have recently traveled to other cities to meet sex partners,7,19 effectively establishing links between transmission networks and facilitating rapid spread to other areas and thus making local containment more difficult. In addition, the large proportion of partners of MSM with syphilis who are anonymous reduces the likelihood of their being rapidly located and treated. Thus, for rapid response efforts to be effective, they will depend on innovative strategies for reaching partners,20 such as venue-based approaches (including internet chat rooms) and e-mail, as well as increased reliance on approaches to rapidly informing communities and providers of the presence of an outbreak. Responding to an outbreak can be more rapidly effective if outbreak response planning includes strategies to work with communities and care providers.21 Such preparation can be enhanced by early coordination with programs working in the areas of HIV prevention and care.
Fourth, expanded clinical and laboratory services previously focused primarily on services run by health departments. However, as noted above, many MSM acquiring syphilis have good access to health care and may be seeing providers regularly, especially those with HIV infection. Thus, for syphilis among MSM, expanding services means working with existing HIV care providers to alter their routine to include screening for syphilis and be attentive to possible symptoms and signs of disease. Innovative efforts to educate and mobilize health care providers on the appropriate clinical and public health management of syphilis, such as those described in this issue,14 will likely be required, especially in cities experiencing MSM outbreaks. Other methods of expanding testing services, such as the use of outreach venues, may be more costly if they require new infrastructures. For example, as described by Ciesielski et al. in this issue, even in cities experiencing relatively large MSM outbreaks, outreach testing at clubs, bathhouses, and other venues frequented by MSM can be low yield and thus relatively expensive for the number of infections detected.22 In the future, the commercialization of rapid syphilis diagnostic tests in the United States, now available in many other countries, could enhance the benefit of screening in both clinical and outreach settings.23 Other innovations in service expansion, such as expanding laboratory access by using internet-based forms, may be helpful in some locales, and their evaluation is a priority.12 Unfortunately, options to simplify treatment have been made more difficult by the recent detection of high levels of resistance to azithromycin,24 an otherwise promising approach to single-dose oral therapy.
Fifth, enhanced health promotion is especially important at the beginning of an epidemic when persons at risk are not aware of the symptoms and signs of infection. Social marketing campaigns to increase awareness, such as those described by Vega and Roland,25 may facilitate early recognition of lesions or rashes that would lead to treatment and interruption of transmission. The recent release of a Syphilis Elimination Toolkit by the CDC offers a resource that should enhance the ability of local communities to develop such campaigns (http://www.cdc.gov/std/SEE/default.htm). In addition, the high rates of coinfection with syphilis and HIV in outbreak sites underscore the importance of risk reduction interventions for HIV-positive men, as noted by Buchacz et al.26 These approaches will need to identify new triggers for encouraging safer sex, routine STD screening, and HIV disclosure. They will also need to clarify currently mixed messages about safer sex as it applies to STD and HIV transmission, in particular the relatively greater role of oral sex in transmitting syphilis than HIV.27 Partner notification is also considered a key component of health promotion and has been a mainstay of syphilis control since the time of Parran. As described by Hogben et al.28 in this issue, the success of partner services activities among MSM with syphilis has been lower than in past efforts due to factors such as providers unaccustomed to working with public health staff, partner anonymity, and mistrust of partner services by MSM. Given these issues, strengthened ties with community groups and providers serving MSM may be particularly helpful in improving the efficiency and yield of partner services. Likewise, innovative approaches such as those noted above will be important in reaching anonymous partners.
Many cities are experiencing syphilis outbreaks and thus have enacted their outbreak response plans. Most programs have needed to adapt those plans because of the changes in the populations at risk. The papers in this special issue summarize the experience from 8 large US cities with a variety of prevention interventions that are components of more comprehensive syphilis elimination plans, and, for many, there is some indication of their relative value, permitting some preliminary conclusions (Table 2). Of greatest importance may be focused efforts to increase awareness, both among providers serving MSM—improving diagnosis of clinical disease and also screening of those at risk—as well as the community in order to enhance early treatment and strengthen community partnerships. Partner services will continue to be an important aspect of syphilis outbreak control, especially with improved provider and community support, but relatively less cost-effective, given difficulty in reaching anonymous partners. Finally, screening in outreach locations appears to be a lower priority because of higher marginal costs of outreach staff and relatively low yields, although it may have collateral benefits if combined with other prevention activities such as HIV testing and hepatitis B immunization or as a contributor to community awareness of the outbreak. Clearly, more information is needed to optimize syphilis elimination approaches, including both innovative operational research to better understand the programmatic impact of various strategies, as well as more systematic monitoring and evaluation of prevention activities.
In summary, while reversals of the decade-long downward trend in syphilis in the United States are concerning and point to the need for a critical reassessment of strategies, they are not a cause for alarm. From the initiation of the national syphilis elimination effort, it was assumed that the “plan [would need to] evolve over time as new lessons [were] learned and applied.”1 Such midcourse corrections in response to new developments are the hallmark of disease elimination and eradication programs, since at their implementation, “[while] it is not possible to predict what unexpected events will occur, one can predict that they will occur.”29 After 15 years of declining risky behavior and STD rates among MSM, the resurgence of syphilis among at least some groups, while explainable, constitutes such an unexpected event. The lessons described in this special issue represent an encouraging summary of how syphilis elimination efforts can respond to this emerging challenge.
1. CDC. The National Plan to Eliminate Syphilis from the United States. Atlanta, GA: US Department of Health and Human Services, CDC, National Center for HIV, STD, and TB Prevention, 1999:1–84. Available at: http://www.cdc.gov/stopsyphilis/plan.pdf
2. Centers for Disease Control and Prevention. Sexually Transmitted Disease Surveillance, 1998. Atlanta, GA: US Department of Health and Human Services, 1999.
3. Centers for Disease Control and Prevention. Sexually Transmitted Disease Surveillance, 2003. Atlanta, GA: US Department of Health and Human Services, 2004.
4. Centers for Disease Control and Prevention. Resurgent bacterial sexually transmitted diseases among men who have sex with men: King County, Washington, 1997–1999. MMWR Morb Mortal Wkly Rep 1999; 48:773–777.
5. Centers for Disease Control and Prevention. Trends in primary and secondary syphilis and HIV infections in men who have sex with men: San Francisco and Los Angeles, California, 1998–2002. MMWR Morb Mortal Wkly Rep 2004; 53:575–578.
6. Peterman TA, Heffelfinger JD, Swint EB, et al. The changing epidemiology of syphilis. Sex Transm Dis 2005; 32(10)supplement:S4–S10.
7. Paz-Bailey G, Meyers A, Blank S, et al. A case-control study of syphilis among men who have sex with men in New York City: association with HIV infection. Sex Transm Dis 2004; 31:581–587.
8. Fenton KA. A multilevel approach to understanding the resurgence and evolution of infectious syphilis in Western Europe. Euro Surveill 2004; 9:3–4.
9. Fenton KA, Imrie J. Increasing rates of sexually transmitted diseases in homosexual men in Western Europe and the United States: why? Infect Dis Clin North Am 2005; 19(2):311–331.
10. Hook EW III. Is elimination of endemic syphilis transmission a realistic goal for the USA? Lancet 1998; 351(suppl III):19–21.
11. Parran T. Shadow on the Land. Baltimore, MD: Waverly Press, 1937.
12. Klausner JD, Wolf W, Wong W, et al. The public health response to epidemic syphilis, San Francisco 1999–2003. Sex Transm Dis 2005; 32 (10) supplement:S11–S18.
13. Schmitt K, George D, Bulecza S, et al. Florida’s multifaceted response for increases in syphilis among MSM: the Miami-Ft. Lauderdale initiative. Sex Transm Dis Sex Transm Dis 2005; 32 (10) supplement:S19–S23.
14. Taylor M, Prescott L, Brown J, et al. Syphilis provider awareness campaigns, screening practices, and CDC/IDSA guidelines for STD screening among HIV-infected persons. Sex Transm Dis 2005; 32 (10) supplement:S24–S29.
15. Kegeles SM, Hays RB, Pollack LM, Coates TJ. Mobilizing young gay and bisexual men for HIV prevention: a two-community study. AIDS 1999; 13:1753–1762.
16. Hays RB, Rebchook GM, Kegeles SM. The Mpowerment Project: community-building with young gay and bisexual men to prevent HIV1. Am J Community Psychol 2003; 31:301–312.
17. Blank S, Gallagher K, Washburn K, et al. What syphilis control efforts have taught us about wellness among men who have sex with men in New York City. Sex Transm Dis 2005; 32 (10) supplement:S65–S72.
18. Taylor M, Montoya J, Cantrell R, et al. Interventions in the commercial sex industry during the rise of syphilis rates among men who have sex with men. Sex Transm Dis 2005; 32 (10) supplement:S53–S59.
19. Centers for Disease Control. Internet use and early syphilis infection among men who have sex with men: San Francisco, California, 1999–2003. MMWR Morb Mortal Wkly Rep 2003; 52:1229–1232.
20. Michaud JM, Ellen J, Johnson SM, Rompalo A. Responding to a community outbreak of syphilis by targeting sex partner meeting location: an example of a risk-space intervention. Sex Transm Dis 2003; 30:533–538.
21. Chen JL, Kodagoda D, Lawrence AM, Kerndt PR. Rapid public health interventions in response to an outbreak of syphilis in Los Angeles. Sex Transm Dis. 2002; 29:277–284.
22. Ciesielski C, Kahn RH, Taylor M, et al. Control of syphilis outbreaks in men who have sex with men: the role of screening in nonmedical settings. Sex Transm Dis 2005; 32 (10) supplement:S37–S42.
23. Siedner M, Zapitz V, Ishida M, et al. Performance of rapid syphilis tests in venous and fingerstick whole blood specimens. Sex Transm Dis 2004; 31:557–560.
24. Lukehart S, Godornes C, Molini BJ, et al. Macrolide resistance in Treponema pallidum
in the United States and Ireland. N Engl J Med 2004; 351:154–158.
25. Vega M, Roland EL. Social marketing techniques for public health communication: a review of syphilis awareness campaigns in eight US cities. Sex Transm Dis 2005; 32 (10) supplement:30–36.
26. Buchacz K, Greenberg A, Onorato I, et al. Syphilis epidemics and HIV incidence among men who have sex with men in the United States: implications for HIV prevention. Sex Transm Dis 2005; 32 (10) supplement:S73–S79.
27. Centers for Disease Control and Prevention. Transmission of primary and secondary syphilis by oral sex: Chicago, Illinois, 1998–2002. MMWR Morb Mortal Wkly Rep 2004; 53:966–968.
28. Hogben M, Paffel J, Broussard D, et al. STD partner notification with men who have sex with men: current practices and plans from eight US cities. Sex Transm Dis 2005; 32 (10) supplement:S43–S47.
29. Hinman AR, Hopkins DR. Lessons from previous eradication programs. In: Dowdle WR, Hopkins DR, eds. The Eradication of Infectious Diseases. Chichester, UK: John Wiley and Sons, 1998:19–31.