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Sexually Transmitted Diseases:
doi: 10.1097/01.olq.0000222703.12018.58
Article

China’s Syphilis Epidemic: A Systematic Review of Seroprevalence Studies

Lin, Charles C. BA*†; Gao, Xing MD†; Chen, Xiang-Sheng MD, PhD†; Chen, Qiang MD†; Cohen, Myron S. MD‡

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From the *University of California, San Francisco School of Medicine, San Francisco, California; the †National Center for STD Control, Chinese Academy of Medical Sciences (CAMS) & Peking Union Medical College (PUMC) Institute of Dermatology, Nanjing, China; and the ‡Division of Infectious Diseases, University of North Carolina, Chapel Hill, North Carolina

Support for this study was provided by the Fogarty-Ellison Fellowship for Global Health and the WHO Western Pacific Region.

Correspondence: Charles C. Lin, BA, and Xiang-Sheng Chen, MD, PhD, National Center for STD Control, 12 Jiangwangmiao Street, Nanjing, Jiangsu Province 210042, China. E-mail: charles.lin@ucsf.edu.

Received for publication January 16, 2006, and accepted March 17, 2006.

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Abstract

Objective: The objective of this study was to investigate syphilis prevalence among low- and high-risk groups in China.

Goal: The goal of this study was to explore the magnitude of China’s syphilis epidemic.

Study Design: A systematic literature review of syphilis seroprevalence studies in China was performed searching PubMed and the Chinese Periodicals Database (CPD).

Results: Five and 169 studies were retrieved from PubMed and the CPD, respectively. From 2000 to 2005, select low-risk groups had the following median syphilis prevalence: antenatal women (0.45%), premarital individuals (0.66%), and food and service employees (0.3%). Select high-risk groups had the following median prevalence: incarcerated female sex workers (12.49%), drug users (6.81%), and men who have sex with men (14.56%). In the last decade, prevalence has increased in all groups with the steepest rises seen among high-risk groups.

Conclusions: Syphilis infection is increasing among low- and high-risk groups in China, suggesting unsafe sexual behavior that may accelerate HIV transmission and challenge current syphilis prevention and control efforts.

AT THE TIME OF THE FORMATION of the People’s Republic of China (1949), sexually transmitted diseases (STDs) were among the most common causes for medical care.1 Syphilis was detected in as many as 17% of the general population in some urban areas (i.e., Nanjing) and in more than 50% of prostitutes.1,2 Mao Zedong established a national STD control program in 1954, which used a combination of community mobilization, mass screening, and treatment.1 This STD prevention program proved among the most successful in the history of mankind. Data collected in 1964 demonstrated virtual eradication of STDs.2

However, with the end of China’s closed door policy, STDs reemerged with a vengeance. The first sporadic cases of syphilis were detected in 1979. To detect the magnitude of the problem, the National STD Center in Nanjing developed an STD enhanced recording and reporting surveillance system in 19873 that now includes 26 sentinel sites. This system has tracked a nearly 20-fold increase in syphilis incidence from 0.17 cases per 100,000 individuals in 1989 to 4.31 cases per 100,000 individuals in 1998.3 This increase can be attributed to a variety of reasons, including profound stigma against STDs, which contributes to poor public knowledge about these diseases, inadequate health care-seeking behavior, and promulgation of unsafe sexual practices, which have grave implications for the sexual transmission of HIV. In addition, in a country where couples are limited to having one child, prevention of congenital syphilis is of crucial importance.

However, questions remain about the accuracy of these data. The recent organizational change shifting STD prevention and control efforts under the supervision of the Chinese Center for Disease Control may have disrupted case reporting. In addition, local Chinese STD experts have estimated that the nation’s case reporting surveillance system may only catch 10% of total syphilis infections. Because a case reporting system is inherently subject to underreporting, other countries such as the United States use routine prevalence studies to supplement and evaluate case report data. Although not as accurate as population-based incident case reports in tracking new cases over a specific time period, sentinel prevalence studies, which are nominally a component of China’s nationwide surveillance system, would provide valuable information such as syphilis prevalence for different risk groups. Unfortunately, they are limited to date.

Given its importance for STD prevention efforts and as a facilitating cofactor in HIV transmission, a lucid understanding of syphilis in China is needed. The objective of this study is to shed light on this epidemic by using a systematic, descriptive, quantitative literature review to estimate current syphilis prevalence and trends among high-risk groups and the general population. This data will be used to develop STD prevention and control strategy. To our knowledge, this is the first literature review of syphilis prevalence in China.

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Materials and Methods

A computerized search for published literature was performed on September 24, 2005, using PubMed and its Chinese equivalent, the Chinese Periodicals Database (CPD), one of the most comprehensive Chinese scientific literature databases that includes over 7400 journals and 15 million articles catalogued from 1979 to the present. Journal type was not used as a screening criterion for the CPD search because reliable syphilis prevalence studies are published in a wide range of Chinese periodicals, including national, provincial, and university-affiliated journals. Thus, recognized journals such as the Chinese Journal of Public Health and the Chinese Journal of AIDS/STD were included, as were lesser known, area-specific journals such as the Shanghai Journal of Preventive Medicine and the Southern China Journal of Dermatology and Venereology. An initial search through PubMed using the key words “syphilis” and “China,” and CPD, using the keyword “syphilis,” was limited to articles published after 2000 and resulted in 31 and 3736 hits, respectively. Given this large number of studies and the fact that most studies reporting syphilis prevalence would be retrieved in a search using the key word, “syphilis,” additional key words such as “STDs” were not used.

To focus the search, articles were chosen if they described serologic prevalence studies in mainland China that used both a screening nontreponemal test (rapid plasma reagin, Veneral Disease Research Laboratory, unheated serum reagin, or toluidine red unheated serum test) and a treponemal-based confirmatory test (fluorescent treponemal antibody absorption, Treponema pallidum particle agglutination assay, T. pallidum hemagglutination, or T. pallidum enzyme-linked immunosorbent assay) to corroborate clinical findings in identifying syphilis cases. To minimize outliers while retaining a sufficient number of studies, research sample population size had to be >500 people, except in the case of possible female sex workers (FSWs), incarcerated FSWs, men who have sex with men (MSM), and drug users, in which a dearth of studies required relaxing these criteria to >80 subjects. Studies were selected if they specifically researched one or more of the following population groups: antenatal women; premarital individuals; blood donors (both commercial and voluntary); internal migrant workers; employees at hotels, restaurants, and railroad stations (hereafter called “food and service employees”); employees at entertainment centers, beauty salons, and bathhouses where commercial sex is not the primary service offered and thus only engaged in by a subset of the employee population (hereafter called “possible FSWs”); FSWs who have been incarcerated or placed in reeducation centers (hereafter called “incarcerated FSWs”); MSM; and drug users. Although one study of nonincarcerated FSWs was located in PubMed, none were found in the CPD, presumably because the illegal nature of and stigma toward prostitution in China makes it particularly difficult to research identified FSWs outside of detention centers.

Studies were excluded if they specifically involved foreigners or if the sample population was not clearly defined. Based on the latter criteria, many studies were excluded because they researched a heterogeneous mix of employees at hotels, restaurants, saunas, bars, and massage parlors without providing distinct syphilis prevalence data for each group. Studies were also excluded if the year of data collection was not explicit or if average prevalence data spanning more than 3 years was presented without individual yearly statistics. The reference sections of these papers were examined and relevant papers were subsequently obtained and added to the list from the original search.

Syphilis prevalence data and study sample characteristics were extracted from these articles and entered into an Excel spreadsheet. Data accuracy was double-checked manually. Statistical analysis including linear regression was performed using functions within Excel. To minimize bias introduced by outliers, a median value for syphilis prevalence with a corresponding interquartile range was calculated for each population group. Substantial heterogeneity in study design of the selected studies prevented a more rigorous meta-analysis from being performed.

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Results

A total of 5 and 169 papers from PubMed and CPD, respectively, met the search criteria. By specific sample population, the 169 CPD papers included 19 premarital,4–22 19 antenatal,23–41 40 blood donor (33 volunteer,42–74 one commercial,75 6 combined,76–81), 19 food and service employee,82–100 11 possible FSW,101–111 21 incarcerated FSW or incarcerated FSW clients,112–132 4 MSM,133–136 28 drug users,137–164 and 8 multigroup studies,165–172 (Fig. 1). Data from all studies were collected in public or governmental health facilities and virtually all were performed in urban areas. None of the studies provided incidence data nor did they specify if data were collected anonymously. The 5 studies gathered from the PubMed search included one each of premarital individuals, nonincarcerated FSWs, and drug users and 2 of migrant workers.

Fig. 1
Fig. 1
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Chinese Periodicals Database Studies

During the last 5 years, from 2000 to 2005, food and service employees had the lowest median syphilis prevalence, 0.30%, with an interquartile range (IQR) of 0.2% to 0.5%. As plotted in Figure 2, the prevalence increased approximately 0.04% per year. The majority of the studies enrolled participants undergoing routine employment physical examinations at local health centers.

Fig. 2
Fig. 2
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Syphilis prevalence data reported in studies of premarital youth and antenatal women are plotted in Figure 3. Fitted trend lines show prevalence increasing at approximately 0.09% annually for both groups. From 2000 to 2005, median syphilis prevalence (IQR) was 0.66% (0.31–1.43%) for premarital individuals and 0.45% (0.29–0.6%) for antenatal women. There was one extreme outlier among premarital studies reported by Fujian’s Xiapu County (6.3%).

Fig. 3
Fig. 3
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From 2000 to 2005, volunteer and commercial blood donors had a median syphilis prevalence (IQR) of 0.37% (0.20–0.65%) and 2.86% (1.71–9.90%), respectively. As shown in Figure 4, syphilis prevalence increased more rapidly for commercial (0.64% per year) versus volunteer donors (0.09% per year). In the 4 studies that directly compared both groups over the same time period, syphilis prevalence for commercial donors was higher than that of volunteers in the tourist destinations of Zhangjiajie (Hunan province) and Meishan (Sichuan province), but comparable to that in the other sites.

Fig. 4
Fig. 4
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Among those involved with sex work, a scatterplot shows that syphilis burden is heaviest among incarcerated FSWs, followed by incarcerated FSW clients, and then possible FSWs (Fig. 5). During 2000 to 2005, median syphilis prevalence (IQR) for incarcerated FSWs, incarcerated FSW clients, and possible FSWs was 12.49% (4.95–17.8%), 3.04% (2.99–5.79%), and 0.83% (0.62–1.3%), respectively. Syphilis prevalence increased at a higher rate for incarcerated FSWs (1.41% per year) than for incarcerated FSW clients (0.75% per year) and possible FSWs (0.13% per year). All studies of FSWs were comprised of completely female samples.

Fig. 5
Fig. 5
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The highest syphilis prevalence was observed among MSM and drug users (Fig. 6). All 4 MSM studies were conducted after 2000 and the median syphilis prevalence (IQR) was 14.56% (10.61–18.7%). Three of the studies were conducted in the south (Guangdong province) and the other in the northeast (Liaoning province). Self-identified MSM comprised the study sample in three of the studies. Despite a limited number of data points, a regression line plotted a 4.5% annual rise in syphilis (Fig. 6). Compared with other high-risk groups such as incarcerated FSWs, incarcerated FSW clients, and drug users, MSM have the highest median prevalence and experience the highest rate of syphilis rise. Among studies of drug users, most were conducted in compulsory drug abuse treatment centers, where intravenous drug users make up a large majority of the incarcerated. Median syphilis prevalence (IQR) was 6.81% (5.01–11.17%) from 2000 to 2005, increasing over time at an average of 0.96% per year. Female drug users had 2- to 10-fold higher syphilis prevalence than males. Very high prevalence (>10%) was reported in sites in Fujian, Gansu, Guangdong, Sichuan, and Xinjiang (Uygur population) provinces.

Fig. 6
Fig. 6
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Median syphilis prevalence and interquartile ranges from 2000 to 2005 are summarized in Table 1. In general, higher syphilis burden is clustered in the economically developed northeastern, eastern, and southern coastal provinces.

Table 1
Table 1
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PubMed Studies

Comparable syphilis prevalence was observed among studies retrieved in PubMed. Among premarital couples in rural and urban areas in 3 representative provinces, 0.33% to 0.71% of premarital individuals were infected.173 In van den Hoek et al, 13.87% of 966 FSWs in Guangdong were infected with syphilis.174 Also, in a study of injecting drug users in Sichuan, 15.3% were seropositive for syphilis.175

Two other studies retrieved from PubMed focused on the floating, or migrant, population in China. In one study of male rural migrants working as construction workers, market vendors, and factory workers in Shanghai, 1% of participants had syphilis.176 In a separate study of market vendors in eastern China, 1.8% of self-reported sexually active individuals were infected with syphilis.177

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Discussion

This study reveals an escalating syphilis epidemic at its most severe state since the infection was effectively eliminated on the mainland 4 decades ago. Among all risk groups, syphilis infection is increasing. The increase is most pronounced among high-risk individuals such as incarcerated FSWs and drug users, in whom syphilis prevalence has risen by roughly 1.4% and 4.5% per year, respectively. Although syphilis burden certainly differs by location, the fact that the majority of the collected data were reported by longitudinal studies makes it likely that results reflect temporal trends rather than geographic variability. Lending credence to these trends, which were derived from syphilis prevalence data reported in the Chinese literature, are similar findings from the 5 studies published in peer-reviewed English-language journals.

Syphilis prevalence was similar across low-risk groups approximating the general population: food and service employees, voluntary blood donors, antenatal women, and premarital youth. Unexpectedly, the median prevalence for possible FSWs, 0.83%, was only slightly higher. Because these studies provided limited information on the sexual behavioral risk characteristics of the individuals studied, it is difficult to conclude why the prevalence was so low. The most likely explanation is that the study samples included many employees at karaoke establishments, dance halls, massage parlors, saunas, and bars that did not engage, if at all, in commercial sex work. Another possibility is that possible FSWs and incarcerated FSWs represent 2 groups with distinct demographic and STD risk characteristics. Poorer, less-educated FSWs, typically at higher risk for STDs, may be disproportionately represented in the incarcerated FSW studies because they have fewer means to deflect increased police attention. In contrast, possible FSWs may be able to avoid incarceration because of social connections, financial recourses, or as a result of working in a protected establishment, which could influence safer sex practices and thus lead to lower syphilis prevalence. Both of these reasons probably contribute to the difference in syphilis prevalence between possible and incarcerated FSWs, a finding that underscores that FSWs and their associated STD risk profiles lie on a spectrum.178

With China’s total population estimated at 1.3 billion people, the sheer number of high-risk individuals suggests a worrisome epidemic. China is estimated to have 5 to 10 million FSWs,179,180 5 to 10 million MSM,181 6 to 8 million drug users,182 and 120 million migrant workers.183 Considering the overlap between these groups and unclear infection rates in rural areas, it is difficult to extrapolate to estimate total national disease burden. However, rough calculations suggest that millions are infected with syphilis among these groups alone.

The spread of syphilis is of important public health significance for several reasons. First, the dire consequences of congenital syphilis are magnified in a country where couples are limited to having one child. With universal antenatal screening, congenital syphilis could be curtailed. Second, STDs, particularly those that cause genital ulcers such as syphilis, contribute to the spread of HIV by increasing infectiousness and/or susceptibility.184 Increased HIV shedding has been reported in the semen of men with genital ulcers,185 and individuals with genital ulcer disease have adjusted risk ratios for HIV acquisition ranging from 2.2 to 11.3.186 Although the majority of studies gathered here did not specify syphilis and HIV coinfection rates, the 4 MSM studies reported HIV seroprevalence ranging from 1.0% to 3.4%, suggesting syphilis infection may be contributing to HIV transmission in this group.

Third, the spread of syphilis reflects unsafe sexual practices, which have an obvious potential to fuel the heterosexual transmission of other STDs, including HIV. In their large study of premarital couples, Hesketh et al173 found similar syphilis prevalence in rural and urban areas in 3 provinces: Yunnan (home of the largest number of injecting drug users in China), Zhejiang (the province with the highest STD incidence), and Shaanxi (a poor central province with low STD and HIV prevalence). Although this suggests widespread unsafe sexual practices, HIV does not yet appear to have spread significantly beyond localized epidemics through heterosexual transmission. Hesketh et al173 found no cases of HIV in Zhejiang or Shaanxi. In Yunnan, they did report HIV cases among known high-risk injecting drug users, but unexpectedly, also among low-risk, nondrug users.173 These results hint that in some places, HIV prevalence may have reached a threshold from which rapid heterosexual spread into the general population can occur. As Yang et al187 conclude in their systematic review of behavioral studies in China, risk factors that contributed to the explosive heterosexual HIV epidemics in Thailand and Cambodia, including high rates of sex worker patronage, low rates of condom use during commercial sex, and concurrent sex with both FSWs and casual sex partners, all exist in China currently.

Particularly concerning is the increasing prevalence of syphilis among high-risk potential bridge populations. Among drug users, females were infected at 2 to 10 times the rate as their male counterparts. This is probably because a significant percentage of female drug users (52–98%) exchange sex for drugs.187 The extent to which these individuals engage in commercial sex work to supplement their income determines their importance as a bridge population in spreading STDs and HIV to the general population. Another crucial group are Chinese MSM, up to 70% to 90% of whom marry wives to adhere to social mores and thus have heterosexual and homosexual partners.188 Although syphilis prevalence is high among MSM, there is growing evidence that HIV is spreading among these individuals as well. In 2004, the Chinese CDC reported >1% HIV infection among MSM and declared them to be the next highest risk group after injection drug users. As increasing social acceptance and more widespread internet use allow men to pursue sexual partners, an underlying practice of unsafe sex may facilitate STD and HIV transmission among MSM and their wives.

Although the results of this study have shed light on China’s syphilis epidemic, it has a few limitations. First, the collected data predominantly reflects urban populations; little research on sexual transmission of HIV has been done in rural areas. A large and growing floating population serving as a bridge between urbanites and farmers may facilitate transmission of STDs and HIV among rural inhabitants. Worse, poor healthcare access and delivery in rural areas render their inhabitants more vulnerable. Second, there may be selection bias in that all of the CPD data were collected from studies conducted in public or government facilities. With the strong stigma associated with STDs, many Chinese patients seek care at pharmacies or private clinics. Although there is no strong evidence that more patients with STDs are seeking treatment at public and government clinics, this phenomenon could contribute to the observed increase in syphilis prevalence. Information about this subset of patients is important both to monitor syphilis spread and to direct control efforts. Third, information about crucial population groups such as migrant workers and FSW clients is limited with only certain subsets of these groups studied. Further research should focus on addressing these unknowns. Fourth, although rising syphilis prevalence was observed for all analyzed population groups, this does not necessarily represent an increase in new cases, because some of these studies may have been conducted anonymously and thus unable to determine duplicate syphilis diagnoses. Nevertheless, these results do strongly suggest a proliferation of new syphilis cases because they lend credence to the rising incidence reported by the nationwide surveillance system.

Although a more robust surveillance system accurately tracking the spread of syphilis and other STDs is central to developing an effective response, results from this study indicate that prompt prevention and control measures are equally as important to avert further spread of syphilis and other STDs. Public health officials invested in STD work can take heart in knowing that syphilis has already been effectively eliminated once in China. However, the draconian measures used so successfully in the 1950s depended on a society closely monitored and controlled by the government.189 In China’s more open society today, effective control of the syphilis epidemic will rest on adaptations of more familiar public health tools, including population-based screening, education, and harm reduction techniques. In addition, existing standardized treatment guidelines must be widely disseminated and followed to treat syphilis cases. Together, these efforts should be directed at decreasing STD/HIV morbidity and reducing risky behavior among high-risk areas and populations.

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