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Sexually Transmitted Diseases:
doi: 10.1097/OLQ.0000000000000097
Original Study

Reduction in Mother-to-Child Transmission of Syphilis For 10 Years in Shenzhen, China

Hong, Fu-Chang MD*; Yang, Ying-Zhou MD*; Liu, Xiao-Li MD*; Feng, Tie-Jian MD*; Liu, Jiang-Bo MD, PhD; Zhang, Chun-Lai MS*; Lan, Li-Na MS*; Yao, Mian-Zhi MS; Zhou, Hua MD, PhD§

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From the *Department of Dermatology and STD, Shenzhen Centre for Chronic Disease Control and Prevention, Shenzhen, China; †Department of Dermatology and ‡Central Laboratory, Shenzhen Bao’an Maternal and Child Health Hospital, Shenzhen, Guangdong, China; and §Xi Xiang People’s Hospital, Bao’an District, Shenzhen, Guangdong, China

Conflicts of interest and source of funding: The Programme of Prevention of Mother-to-Child Transmission of Syphilis in Shenzhen was supported by Shenzhen government. This work is currently funded by grants (No.201102029, 201202104) from Shenzhen Science and Technology Innovation Commission and a grant (No. 20110610) from Baoan Science and Technology Innovation Commission.

Correspondence: Jiang-Bo Liu, MD, PhD, is to be contacted at the Department of Dermatology, Shenzhen Bao’an Maternal and Child Health Hospital, Shenzhen, Guangdong, China. E-mail: Hua Zhou, MD, PhD, Xi Xiang Peoples Hospital, Bao’an District, Shenzhen, Guangdong, China. E-mail: Fu-Chang Hong, MD, Department of Dermatology and STD, Shenzhen Centre for Chronic Disease Control and Prevention, Shenzhen, China. E-mail:

Received for publication June 19, 2013, and accepted December 20, 2013.

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Background: Untreated maternal syphilis can result in the fetuses being infected. Severe adverse pregnancy outcomes include stillbirth, perinatal death, low birth weight, and congenital syphilis (CS). The World Health Organization has already classified global elimination of CS as a priority. However, this preventable disease is still threatening people’s health in the world.

Methods: A Programme of Prevention of Mother-to-Child Transmission of Syphilis in Shenzhen was launched in 2002. All pregnant women in Shenzhen were screened for syphilis by serological methods at their first prenatal care visit. The infected individuals were treated with 3 weekly injections of 2.4 million units of benzathine penicillin. The babies were followed up until 18 months old to diagnose CS.

Results: Up to 2011, the Programme of Prevention of Mother-to-Child Transmission of Syphilis in Shenzhen screened 2,077,362 pregnant women and intervened in 7668 mothers infected with syphilis. The screened rate among pregnant women increased from 89.8% in 2002 to 97.4% in 2011. The proportion of those having adverse pregnant outcomes (including spontaneous abortion, premature delivery, and stillbirth) decreased from 27.3% in 2003 to 8.2% in 2011. The incidence of CS decreased from 115/100,000 in 2002 to 10/100,000 (live births) in 2011.

Conclusions: In 2002, in the face of rising CS numbers, Shenzhen adapted a syphilis control program that involved cost-free testing for pregnant women, commitment and collaboration at multiple levels of the health system, and strong supervision and government guidance. Local program and surveillance data suggest that the program has been very successful in reducing CS incidence.

Untreated maternal syphilis can result in the fetuses being infected with syphilis and lead to severe adverse pregnancy outcomes including stillbirth, miscarriage, premature delivery, perinatal death, and congenital syphilis (CS).1 Screening and treatment of syphilis during prenatal care visits has been recommended by World Bank and the World Health Organization for the minimum cost (1–3 injections of benzathine penicillin, which is simple and inexpensive) and maximum benefits to prevent these adverse pregnant outcomes.2–4 Although the World Health Organization had classified global elimination of CS as its priority since 2007,5 obstacles to eliminate CS have still been there.4,5 Interrupted programs of prenatal screening for syphilis, lack of a strong political commitment, poor collaboration between departments and medical workers, and staff without sufficient training were among these obstacles seen in program implementation.2,4,5 Patients’ hesitation to pay for the testing and treatment, stigma for visiting doctors and reluctant partner notification, and late or lack of prenatal care were obstacles seen at the patient level.6

Moreover, CS had been neglected and even forgotten for a period.7,8 Currently, most CS cases are reported in developing countries and regions, such as Sub-Saharan Africa.9 However, over the past decade, the incidence of CS had increased in developed countries.10,11 In mainland China, although this preventable disease was considered eradicated in the 1960s,12,13 it was reported that CS might be reaching epidemic status in recent years. The incidence of CS was higher than 100 cases per 100,000 live births in 8 provinces in 2011.14 Nationwide, the incidence of CS was estimated at nearly 80 cases per 100,000 live births.14 Shenzhen, one of the developed cities in mainland China, witnessed a rapidly increasing incidence of syphilis from 1980s to the end of the last century.15 The first case of CS in Shenzhen was reported in 1996.16 Within 6 years, the incidence of CS in Shenzhen rose to 115.3 cases per 100,000 live births.17 This was approximately 20 times higher than the mean incidence of CS in China in the year of 2002. To control and prevent CS, the Programme of Prevention of Mother-to-Child Transmission of Syphilis in Shenzhen (PPSS) was launched in 2002. In 2003, the incidence of CS began to decline. By 2011, the incidence of CS in Shenzhen dropped to 10.4 cases per 100,000 live births.17–20 Herein, we summarize our 10-year progress in implementing the PPSS.

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Program Organizations and Duties

The PPSS was established by the Health Bureau of Shenzhen, which planed, organized, monitored, and provided financial support to the program. It is composed of the following units: The Shenzhen Center for Chronic Disease Control (CCDC) and Shenzhen Maternal and Children’s Health Hospital. The CCDC was in charge of making guidelines, training personnel, and supervising the whole system. Experts in Shenzhen Maternal and Children’s Health Hospital offered help to assess the risk of pregnancy for mothers infected with syphilis.

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Managing Pregnant Women Infected With Syphilis and Their Infants

Hospitals that provide prenatal health care offered free syphilis serological screening to pregnant women at their first obstetric examinations. Pregnant women with positive results for syphilis were further evaluated for confirmation. The diagnostic criteria and treatment of maternal syphilis were based on the CDC guideline.21 Monthly serological tests for syphilis were performed before delivery, and the infected mothers would be retreated when a reduction in 2 dilution series in the serum titer was not observed within 3 months or the titer increased. Figure 1 shows a flowchart of the intervention for pregnant women with syphilis (including screening, identification, treatment, and follow-up for both mother and child).

Figure 1
Figure 1
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Infants were examined by a fluorescent treponemal antibody absorption test with a fluorochrome-labeled antihuman IgM on fractionated sera. A positive IgM test result showed the presence of CS. Offsprings with a negative IgM test were followed up by serological tests until the 18th month after birth if they were considered as having possible CS according to CDC guidelines.21 A positive result of Treponema pallidum particle agglutination at the 18th month after birth was used as a retrospective validation of the diagnosis of CS.21 With positive syphilis serological test results, when the serum titer gradually increased, or clinical signs of CS were detected during follow-up, the neonate was diagnosed as having CS and treated accordingly.19,22 Follow-up and syphilis serological testing were performed every 3 months until negative findings were obtained.

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Monitoring and Assessing the PPSS Execution

To keep the PPSS running, staff in sections of prenatal care, gynecology, obstetrics, neonatology, dermatology and sexually transmitted diseases (STDs), and clinical laboratory and those concerned must undergo training to execute their responsibility correctly in PPSS. The duties of CCDC included establishing reference laboratory for quality control; making workbook for the doctors; educating and training staff including doctors, nurses, and managers; and budgeting, supervising, and assessing the implement of the PPSS in all participated hospitals. Periodic and nonperiodic monitoring and assessment were performed by using a standard score sheet (Table 1) at the program execution organizations to ensure the effectiveness of the PPSS.

Table 1
Table 1
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Analysis of the Pregnancy Outcomes of Mothers Intervened by the PPSS

After the intervention, the pregnancy outcomes of mothers, which included stillbirth, perinatal death, low birth weight, and CS, were recorded and presented by proportion. The categorical variables were described by numbers and percentages. The variable trend of numbers was tested by trend χ2. A level of 5% (P < 0.05) was considered statistically significant. All statistical analyses were performed using SPSS (version 13.0; SPSS Inc, Chicago, IL).

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Patients Management and PPSS Progress Summary

We have established a feasible and effective surveillance system for maternal syphilis in Shenzhen in the past 10 years. When a pregnant woman went to any hospital for her first prenatal care visit, she was given a cost-free test for syphilis (Fig. 1). The sera with a positive result were retested by CCDC (quality control). After the confirmation of syphilis, a specialized record for syphilis, as well as her prenatal health archive, was established. This syphilis record was then delivered from the department of gynecology and obstetrics to the clinic of STD. The later was in charge of the treatment and following up (a) for the mother till the end of pregnancy and (b) the baby till a negative reaction of the test for nontreponemal antibodies. The mother’s syphilis record could be accessed by any doctor working at STD clinics in case the mother visited different doctors. In addition, all information of the patient was gathered by CCDC, which guaranteed the continuity of the follow-up and treatment no matter what hospital the patient visited.

Once a positive result of test for syphilis was reported from the clinical laboratory, the CCDC would activate the tracing system that required the attending doctor report the case to the national monitoring system for infectious diseases within 2 days and that the infected mother must be treated at once. Within 1 month, the CCDC got the hardcopy of the syphilis record to inspect and supervise whether the infected mother was managed correctly. After delivery, the focus of PPSS turned to assess the infection of the neonate (Fig. 1).

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Screening Syphilis in Pregnant Women

From July 2002 to 2011, the PPSS screened 2,077,362 pregnant women for syphilis in Shenzhen (Fig. 2). At the beginning, the rate of all pregnant women screened by the PPSS was 89.8%. This has increased to more than 95% since 2005. In 2010 and 2011, the coverage of the PPSS increased and stabilized to the level of 97.4%. In total, the PPSS has identified 7668 cases of maternal syphilis. The highest prevalence of maternal syphilis occurred in 2005 at 0.52%, and it decreased to 0.25% in 2011 (Fig. 3).

Figure 2
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Figure 3
Figure 3
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Pregnancy Outcomes of Mothers Intervened by the PPSS

An increasing number of pregnant women with syphilis who decided to continue their gestation were observed after treatment and assessment of the risks in their fetuses. The percentage of these women was 60% in 2003, and it gradually increased to 83.8% in 2011 (trend χ2 = 62.3, P < 0.001; Fig. 4). Among these mothers, the proportion of those having adverse pregnant outcomes (including spontaneous abortion, premature delivery, and stillbirth) decreased from 27.3% in 2003 to 8.2% in 2011 (trend χ2 = 133.9, P < 0.001; Fig. 4). The percentage of induced abortion among mothers with syphilis dropped from 17.1% in 2003 to 9.1% in 2011 (trend χ2 = 17.3, P < 0.001). In addition, the rate of women lost dropped from 18.9% in 2003 to 2.3% in 2011 (trend χ2 = 81.9, P < 0.001). Although we previously reported a higher rate of ectopic pregnancy in mothers with syphilis than that in uninfected ones,18,23 we did not observe a significant trend in the rate of ectopic pregnancy during the 10-year course (trend χ2 = 2.01, P = 0.157).

Figure 4
Figure 4
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The peak incidence of CS in Shenzhen occurred in 2002, when the PPSS was launched. A reduction of incidence was observed in 2003 and 2004. After an increase in 2005, the incidence of CS steadily dropped to 10.4 cases per 100,000 live births (Fig. 5). From 2008 onward, the incidence of CS in Shenzhen has been maintained at lower than 15 cases per 100,000 live births, which is the national goal for CS control by 2020.24

Figure 5
Figure 5
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As a pilot city for Chinese reform and openness policy, Shenzhen began her rapid development in the 1980s. In 2002, 5.04 million people were registered (lived in Shenzhen for ≥1 year). By 2011, 10.46 million people were registered. In this young city, more than 90% people were immigrants. After Beijing, Shenzhen became the second city, including all 56 Chinese ethnic groups. Meanwhile, the incidence of CS was also increased rapidly. To control and prevent CS, Shenzhen government launched the PPSS, which was executed by CCDC. The PPSS is a parallel program with preventing mother-to-child transmission for HIV. Both HIV and syphilis were tested free at the same time. The results of HIV were recorded and reported to CDC instead of CCDC. Also, HIV-infected patients were followed up and managed by the CDC. In the hospitals, the 2 programs were implemented simultaneously to cut down the cost.

The PPSS was the first program in China to prevent CS by screening syphilis among pregnant women. The incidence of CS was reduced from 115.3 to 10.4 cases per 100,000 live births after 10 years. The essential points behind the success of the PPSS were based on the following principles, which were followed since its inception: (1) hospital-based universal screening among pregnant women; (2) free screening; (3) whole course management for each case of maternal syphilis, including testing, diagnosis, treatment, health counseling, tracing the source of infection, and follow-up; (4) comprehensive intervention: a person assigned to be in charge of patient management must specify standard regimens for treatment, thorough plan for dealing with all kinds of pregnancy outcomes, as well as follow-up, test, assessment, and treatment for infected mothers, their sex partners, and their infants on schedule; (5) supervision and assessment: regular supervision and assessment were performed to identify possible difficulties or obstacles for the PPSS; and (6) government action: controlling infectious diseases and eliminating CS are the duties of the government, and thereby, the program is led by the Shenzhen government. Although the intervention procedure for patients seemed complex (Fig. 1), these 6 principles ensured that the PPSS served its purpose of controlling CS well. Although we only have observational data and cannot be certain that the reductions of CS would not have been seen without the program because it is not a randomized trial, we believe that the dramatic reduction in CS after the program began was due to its effect.

The most essential part of CS control is multilevel commitment from public health, sexually transmitted infection, maternal health, and medical agencies,25 which also applies to the PPSS. Because the management of pregnant women infected with syphilis is a multi-interdisciplinary subject intersected by prenatal health, obstetrics, neonatology, and STD clinics as well as clinical laboratories, smooth cooperation among departments is crucial for the PPSS to function well. Effective and regular supervision is the foundation of successful cooperation among departments and medical agencies. Medical agencies and/or doctors would be asked to explain the reason (i.e., accountability) if any mother with syphilis was not reported, not treated, or not followed up regularly. Under such supervision, the coverage of the PPSS reached 89.8% at the beginning and all infected mothers (100%) were treated.

It is usually difficult to diagnose whether an asymptomatic infant has CS at birth because specific criteria for the diagnosis of CS are not available.22,26 Before the PPSS was launched, medical staff and public medical workers would report cases of CS solely based on a positive toluidine red unheated serum test or T. pallidum particle agglutination result in infants, which could led to an artificial increase in the reported incidence of CS. After 2002, only cases with a specific diagnosis of CS, which sometimes need 18 months after delivery to be made, were reported.19,22 This partially explained the sharp reduction in the reported incidence of CS in 2003 and 2004. From 2005 to 2011, we also found the prevalence of maternal syphilis decreased by 50%. In our opinion, there were 2 reasons for that. First, industrial restructuring and economic crisis in recent years resulted in the emigration of workers out of Shenzhen, who were the main group with high-risk sexual behaviors and easy to be infected with syphilis.18 Second, the strict management of entertainment venues led to the reduction of commercial sex.

In 2008 and 2009, we observed a higher rate of patients who could not be followed up. The reason was that the global economic crisis resulted in the shutdown of factories in Shenzhen, which led to a large number of workers emigrating. Although the coverage of the PPSS reached as high as 97.4% of all pregnant women in Shenzhen, we still observed 20 cases of CS in 2011. The influx of immigrants was determined to be one of the sources of CS. The low rate of partner notification and partner testing represented another aspect of CS cases. Although robust systems for partner notification were widely known to be effective in controlling syphilis, including CS,7,27,28 some mothers who were afraid of social or familial disgrace and family problems were reluctant to tell their partners about the infection. A reinfection of syphilis during gestation might be the second reason,25 To continue the successful PPSS program in Shenzhen, we are now considering and assessing a secondary screening for syphilis during the third trimester of pregnancy, which has been implemented in other countries,29 to further reduce the incidence of CS. The third reason for the occurrence of CS stems is the fact that a small proportion of mothers (2.6%) did not seek prenatal care and just went to hospital for delivery.30 Therefore, comprehensive intervention from the PPSS could not work on these mothers effectively. Although failed cases among mothers who even underwent regular intervention were recorded,31,32 the proportion was less than 5%.19

We successfully overcame some difficulties and obstacles encountered in other programs.5–7 The success of the PPSS gives a reliable model for controlling CS in Chinese mainland. However, the current wave of sexual liberalism, booming commercial sex market, rural-to-urban migration, limited routine screening, incomplete partner notification, and stigma associated with STD contribute to the persistent exist of syphilis in population.25,33 In 2010, the Chinese Ministry of Health developed the program of “Planning, Prevention, and Control of Syphilis in China (2010–2020).”24 The goal of the national program is to slow down the rapid increase of syphilis and reduce the incidence of CS to less than 15 cases per 100,000 living births. How to reach this goal is a huge challenge for Chinese decision makers. The effective measures and experience discussed in this work not only can help to realize the national goals of controlling CS by 202024 but also may help to eliminate CS globally.5

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