From *The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina; and †The London School of Hygiene and Tropical Medicine, London, U.K.
Correspondence: Myron S. Cohen, MD, The Center for Infectious Diseases, 2nd Floor Bioinformatics Building, 130 Mason Farm Road, UNC–Chapel Hill, Chapel Hill, NC 27599. E-mail: email@example.com.
Received for publication August 24, 2006, and accepted September 5, 2006.
Syphilis was first recognized in China in the 1500s and was most likely brought to China by Portuguese traders.1 By the time of the “liberation” of China in 1949, syphilis was one of the most common causes for medical care, and prevalence surveys revealed a massive epidemic in sex workers and national minority populations.2
The Chinese Communist government made treatment and prevention of syphilis a priority3 and inspired a prolonged and successful but draconian “campaign” to accomplish this goal. By 1964, syphilis was very rare,4 and the infection was probably virtually eliminated until China opened its international borders to Western tourists and commerce in the early 1980s. The first resurgent cases of syphilis were recognized in China in 1979,5 and a national surveillance system has demonstrated a steady and disturbing spread of the disease throughout the country.6
In this issue of STD, 2 articles address this situation. First, Lin et al7 review the Chinese and English literature since 2000 in an attempt to better estimate the magnitude of the syphilis epidemic. The results suggest that syphilis infections are currently being detected at relatively low prevalence (0.2–0.7%) in the general population and antenatal screening clinics, but at much greater prevalence in high-risk populations. Syphilis was detected in 3% to 11% of sex workers (a sad reminder of the pre-Mao past) and 10% to 18% of men reporting sex with men (MSM). A substantial rise in yearly prevalence was noted in all groups studied, reaching a 4.4% yearly increase in MSM. The rapid spread of syphilis in MSM in China is also being observed in gay communities in other parts of the world.8
Also in this issue, Ruan et al9 report on their systematic examination of sexually transmitted diseases and HIV in female sex workers in Xichang City in Sichuan Province. Three hundred forty-three of an estimated 2,800 sex workers were included in the study, representing 94 separate establishments. Twenty-one percent of sex workers had also been employed as waitresses, demonstrating the potential for a large “gray market” of sex work among women in service trades. More than 15% of the women studied had syphilis, whereas other sexually transmitted infections were less common. Acquisition of syphilis was significantly associated with length of time as a sex worker, low-end sex trade, sexual relations with a nonmonogamous steady partner, and injecting drug use.
These articles demonstrate a widespread and rapidly increasing syphilis epidemic in China and lead to 3 key questions: Why has syphilis returned? What are the immediate and long-term consequences of this epidemic? What can be done about it?
Rapid change in societal values, sexual behaviors, and social forces favor the spread of sexually transmitted diseases. Parish et al demonstrated an exceptional prevalence of genital tract chlamydia infections in a nationwide survey of sexually transmitted diseases that also emphasized the emergence of sex work and increased rates of sexual partner change.10 Lack of sufficient control of commercial sex, a booming economy, and a more open society are all ingredients for the current epidemic. Massive migration of men trying to find work in urban areas and considerable gender imbalance in many parts of China can only increase the demands for commercial sex workers.11
In addition, powerful biologic forces may be at play. Syphilis infections evoke an immune response that might affect the probability of reinfection and/or modify the natural history of the disease. In a controversial modeling study, Grassley et al argued that waxing and waning syphilis epidemics are less reflective of societal interventions than population-level exposure and immunity.12 Given the virtual absence of syphilis in China until recent years, it is hard to imagine a population more vulnerable than the Chinese.
The untoward consequences of syphilis hardly need emphasis. Given China’s one child family planning policy, successful pregnancies could not be of greater importance to women anxious to start a family. Yet syphilis infection in pregnancy leads to substantial fetal wastage, low-birth-weight infants (leading to increased vulnerability and risk of other morbidities), and the risk of congenital syphilis.13 Incident syphilis infection has been correlated with both vertical14 and sexual transmission of HIV.15
The syphilis epidemic in China has attracted little national or international attention and few new resources. However, there is no doubt that interventions to control syphilis are urgently needed, and there are only a limited number of structural and biologic options possible. The great success of China’s sexually transmitted disease campaign in the 1950s can be ascribed to a patriotic mass screening campaign, virtual eradication of prostitution using severe and often punitive approaches, a completely closed society, and the availability of free single-dose therapy.2 Clearly, a “repeat performance” of this approach in today’s China is impossible. However, health and population services in China offer other possibilities: the employment of new rapid and sensitive rapid screening tests,13 the potential use of oral antibiotic therapy for some patients in some settings,16 depending on the prevalence of resistance,17 and the clearcut Chinese commitment to family planning.
Indeed, emergent focus on antenatal clients and coordination with the National Population and Family Planning Commission Bureau to reduce the risk for syphilis in pregnancy seem entirely warranted. The World Health Organization has recently developed a global action plan to eliminate congenital syphilis.18 To inform development of the action plan, a global review of national level syphilis control policies was carried out. This highlighted the following areas as central for national programs: 1) ensure advocacy and sustained political commitment for a successful health initiative; 2) increase access to, and quality of, health services; and 3) establish surveillance, monitoring, and evaluation systems.
Finally, China’s success in the control of syphilis 50 years ago was clearly just as political as it was biomedical.3 Interventions at the level of the health services will only be successful when syphilis is recognized as an important issue by Chinese decision-makers setting the health policy agenda. Political support for policy implementation is crucial for all types of sexual and reproductive health interventions,19 including the control of syphilis.20
1.Wang J. Origin of syphilis in China. Chung Hua I Hsueh Tsa Chih 1923; 9:17–20.
2.Liu M, Chen YS, Liu HY, et al. Report on screening of venereal diseases in Hezuo City of Gannan Tibet Autonomous Prefecture. Chin J Dermatol 1958; 6:76–77.
3.Cohen MS, Henderson GE, Hamilton H, et al. Eradication of syphilis in China—Lessons for the 20th century? J Infect Dis 1996; 174:S223–230.
4.Hu CK YG, Wang GC, Yun GL. Ten years of accomplishments in dermatology and venereology. Chin J Dermatol 1959; 7:290–294.
5.Gong XD, Zhang GC, Ye SZ, et al. Epidemiological analysis of syphilis in China from 1985 to 2000. Chin J Sex Transm Inf 2001; 1:1–6.
6.Chen XS, Gong XD, Liang GJ, et al. Epidemiologic trends of sexually transmitted diseases in China. Sex Transm Dis 2000; 27:138–42.
7.Lin CC, Gao X, Chen X-S, et al. China’s syphilis epidemic: A systematic review of seroprevalence studies. Sex Transm Dis. 2006; 33:726–736.
8.Centers for Disease Control and Prevention. Primary and secondary syphilis—United States, 2003–2004. MMWR Morb Mortal Wkly Rep 2006; 55:269–273.
9.Ruan Y, Cao X, Qian H-Z, et al. Syphilis among female sex workers in southwestern China: Potential for HIV transmission. Sex Transm Dis. 2006; 33:719–723.
10.Parish WL, Laumann EO, Cohen MS, et al. Population-based study of chlamydial infection in China: A hidden epidemic. JAMA 2003; 289:1265–1273.
11.Tucker JD, Henderson GE, Wang TF, et al. Surplus men, sex work, and the spread of HIV in China. AIDS 2005; 19:539–547.
12.Grassly NC, Fraser C, Garnett GP. Host immunity and synchronized epidemics of syphilis across the United States. Nature 2005; 433:417–421.
13.Peeling RW, Mabey D, Fitzgerald DW, Watson-Jones D. Avoiding HIV and dying of syphilis. Lancet 2004; 364:1561–1563.
14.Mawapasa V, Rogerson S, Kwiek J, et al. Maternal syphilis is associated with an increase risk of maternal to child transmission of HIV-1 in Malawi. AIDS. 2006; 20(14):1869–1877.
15.Reynolds SJ, Risbud AR, Shepherd ME, et al. High rates of syphilis among STI patients are contributing to the spread of HIV-1 in India. Sex Transm Infect 2006; 82:121–126.
16.Riedner G, Rusizoka M, Todd J, et al. Single-dose azithromycin versus penicillin G benzathine for the treatment of early syphilis. N Engl J Med 2005; 353:1236–1244.
17.Mitchell SJ, Engelman J, Kent CK, et al. Azithromycin-resistant syphilis infection: San Francisco, California 2000–2004. Clin Infect Dis 2006; 42:337–345.
18.Hossain M, Broutet N, Hawkes S. The elimination of congenital syphilis: A comparison of national policies to the WHO proposed action plan for the elimination of congenital syphilis. Sex Transm Dis. In press.
19.Buse K, MartinHilber A, Widyantoro N, Hawkes S. Managing the politics of evidence-based sexual and reproductive health care. Lancet. In press.
20.Gloyd S, Chai S, Mercer MA. Antenatal syphilis in sub-Saharan Africa: Missed opportunities for mortality reduction. Health Policy and Planning 2001; 16:29–34.