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Syphilis caused by Treponema pallidum can be transmitted transplacentally from a pregnant woman to her fetus. Without treatment, maternal syphilis is estimated to result in adverse birth outcomes (ABOs) in 50%–80% of affected pregnancies (1). Congenital syphilis (CS) as one of the ABOs can be prevented by early detection of maternal syphilis through testing and prompt treatment to cure maternal and fetal infections (2). The World Health Organization (WHO) launched the global initiative to eliminate mother-to-child transmission (EMTCT) of syphilis in 2007 and integrated interventions of maternal syphilis into the existing elimination of HIV in 2015 (3). Syphilis screening for cases and treatment for infected pregnant women and their infants as a vital component of the national program on preventing mother-to-child transmission (PMTCT) of HIV, syphilis, and HBV has been available freely in China since 2010 and achieved universal coverage since 2015 (4). A better understanding of the implementation and outcomes of the program on PMTCT of syphilis is needed for future strategies to achieve the WHO goal of EMTCT of syphilis. The data from the surveillance systems revealed that there was a marked increase in the coverage of syphilis screening of pregnant women and treatment for syphilis-seropositive pregnant women and their infants in China between 2011 and 2018. Meanwhile, the incidence of CS significantly dropped from 91.6 cases per 100,000 live births to 18.4 cases per 100,000 live births. However, treatment rates and adequate treatment rates of syphilis-seropositive pregnant women were below the criteria of validation of EMTCT of syphilis and regional disparities were found. Hence, the current PMTCT intervention strategies need to be strengthened continuously with further commitments. More effort is needed to remove roadblocks to achieving high coverage of adequate treatment.
The report described the coverage of maternal syphilis screening and treatment for syphilis-seropositive pregnant women and their infants in China using the 2011–2018 national information system of PMTCT of HIV, syphilis, and HBV management data. The national information system of PMTCT of HIV was established in 2007 by the National Center for Women and Children’s Health of China CDC. Since 2011, the system started to collect data on PMTCT of syphilis and HBV. Data on syphilis screening of pregnant women and treatment of syphilis-seropositive pregnant women and their infants was collected through mandatory case-reporting and monthly work statements by health facilities, including general hospitals, maternal and children’s hospitals, and other health providers across China. Data on CS cases from the national sexually transmitted disease (STD) surveillance system during 2011–2018 were analyzed (5). Birth data, used for determining the number of live births, were derived from the annual report of maternal and child health.
Syphilis-seropositive diagnosis required positive results from both types of serologic tests for syphilis: non-treponemal and treponemal. The diagnosis of CS cases was based on the national PMTCT action plan (6). Prophylaxis treatment referred to treatment of eligible newborn infants with one dose of intramuscular benzathine benzylpenicillin after birth. Eligible infants included: 1) born to seropositive mothers without standard treatment, or 2) born to seropositive mothers with standard treatment and with a reactive non-treponemal serology titer less than fourfold more than that of the mother before delivery (5). Treatment for seropositive pregnant women referred to treating seropositive women with penicillin, ceftriaxone, or erythromycin where appropriate during pregnancy. Adequate treatment defined by the WHO referred to treating seropositive women with at least one dose of intramuscular benzathine benzylpenicillin at least 30 days before delivery (3). The SPSS software (version 23.0, IBM Corp, Armonk, NY, USA) was used for all analyses. The rates of screening and treatment were presented as frequencies and proportions. Pearson’s Chi-square test and trends Chi-square test were applied to compare rates in different years. A p-value of <0.05 was considered statistically significant and calculated for 95% confidence intervals (95% CI).
During 2011–2018, the number of pregnant women screened for syphilis raised from 7,303,093 to 15,060,037, which indicated a twofold increase. The rates of maternal syphilis screening during pregnancy (predelivery and at labor) and predelivery increased from 85.0% (7,303,093/8,590,863) and 47.5% (4,084,096/8,590,863) to 99.5% (15,060,037/ 15,132,674) and 93.9% (14,203,528/15,132,674), respectively. A total of 263,154 syphilis-seropositive pregnant women had been detected, with a maternal syphilis positive rate of 2.40‰ (95% CI: 2.39‰–2.41‰) between 2011 and 2018. The rate increased from 2.03‰ (95% CI: 2.00‰–2.06‰) to 3.05‰ (95% CI: 3.03‰–3.08‰) (trend χ2 = 3575.84, p<0.001) during the study period. (Table 1)
Year No. of pregnant women Syphilis test during pregnancy Syphilis test predelivery Syphilis-seropositive pregnant women n % n % n ‰ (95% CI)* 2011 8,590,863 7,303,093 85.0 4,084,096 47.5 14,822 2.03 (2.00−2.06) 2012 12,061,754 11,470,728 95.1 7,446,927 61.7 23,101 2.01 (1.99−2.04) 2013 13,074,271 12,597,061 96.4 8,749,303 66.9 27,435 2.18 (2.15−2.20) 2014 13,796,336 13,724,595 99.5 10,481,076 76.0 31,757 2.31 (2.29−2.34) 2015 13,983,083 13,823,676 98.9 11,495,493 82.2 33,279 2.41 (2.38−2.43) 2016 18,325,702 18,223,078 99.4 16,051,482 87.6 40,213 2.21 (2.19−2.23) 2017 17,566,853 17,517,666 99.7 15,971,783 90.9 46,562 2.66 (2.63−2.68) 2018 15,132,674 15,060,037 99.5 14,203,528 93.9 45,985 3.05 (3.03−3.08) Total 112,531,536 109,719,934 97.5 88,483,688 78.6 263,154 2.40 (2.39−2.41) * ‰=the proportion of syphilis-seropositive pregnant women among pregnant women who received syphilis test during pregnancy. Table 1. Testing rates and positive rates of maternal syphilis among pregnant women, China, 2011−2018.
The treatment rates of syphilis-seropositive pregnant women and the prophylaxis treatment rates of their newborn infants consistently raised during the study period. In 2018, the treatment rate and the prophylaxis rate were 84.3% (29,982/35,578) and 69.5% (24,799/35,671), respectively. Along with increasing uptake of treatment for infected mothers and their infants, the incidence of CS reduced from 91.6 cases per 100,000 live births to 18.4 cases per 100,000 live births between 2011 and 2018. (Figure 1)
Figure 1.Treatment rates of syphilis-seropositive pregnant women and their newborn infants, and the incidence of congenital syphilis (CS), China, 2011–2018.
Among 31 provincial-level administrative divisions (PLADs) of the mainland of China, the treatment rates of 7 (22.6%) PLADs were higher than 90% and that of 4 (12.9%) PLADs were higher than 95%. None of the provinces achieved an adequate treatment rate of 95% in 2018. Compared with 2017, the treatment rates and the adequate treatment rates of 19 (61.3%) provinces significantly increased (p<0.05), but of 2 provinces (Hainan and Qinghai) decreased (p<0.05) in 2018. No statistically significant differences were found in 2 rates of Beijing, Liaoning, Shanghai, and Jilin between 2017 and 2018. (Table 2)
PLADs 2017 2018 No. of sero-positive pregnant women Treatment Adequate treatment No. of sero-positive pregnant women Treatment Adequate treatment No. % No. % No. % No. % Yunnan 1,963 1,901 96.8 1,692 86.2 1,959 1,916 97.8 1,787 91.2* Hunan 2,420 2,269 93.8 1,838 76.0 2,615 2,527 96.6* 2,185 83.6* Zhejiang 2,559 2,384 93.2 2,123 83.0 2,176 2,088 96.0* 1,898 87.2* Beijing 274 255 93.1 232 84.7 218 209 95.9 196 89.9 Sichuan 2,821 2,593 91.9 1,886 66.9 2,931 2,745 93.7* 2,117 72.2* Guizhou 2,312 2,082 90.1 1,308 56.6 2,556 2,371 92.8* 1,759 68.8* Tianjin 313 205 65.5 173 55.3 339 307 90.6* 240 70.8* Guangdong 3,130 2,742 87.6 2,008 64.2 3,213 2,864 89.1 2,286 71.1* Liaoning 1,145 999 87.2 912 79.7 1,220 1,069 87.6 989 81.1 Guangxi 2,190 1,835 83.8 1,609 73.5 2,071 1,799 86.9* 1,594 77.0* Ningxia 189 139 73.5 105 55.6 209 180 86.1* 123 58.9 Anhui 1,803 1,386 76.9 1,164 64.6 1,684 1,442 85.6* 1,247 74.0* Shanxi 655 457 69.8 306 46.7 677 568 83.9* 421 62.2* Xinjiang 1,151 886 77.0 723 62.8 1,182 973 82.3* 843 71.3* Jiangsu 1,817 1,400 77.1 1,170 64.4 1,885 1,537 81.5* 1,336 70.9* Hainan 321 295 91.9 186 57.9 162 129 79.6* 75 46.3* Chongqing 841 607 72.2 479 57.0 773 602 77.9* 512 66.2* Jiangxi 717 531 74.1 341 47.6 716 554 77.4 406 56.7* Shanghai 436 313 71.8 243 55.7 365 282 77.3 219 60.0 Fujian 1,447 1,006 69.5 851 58.8 1,479 1,135 76.7* 1,006 68.0* Qinghai 273 235 86.1 152 55.7 424 324 76.4* 195 46.0* Henan 889 595 66.9 308 34.6 986 744 75.5* 475 48.2* Hebei 639 280 43.8 236 36.9 794 562 70.8* 461 58.1* Shaanxi 587 334 56.9 238 40.5 616 410 66.6* 322 52.3* Heilongjiang 890 529 59.4 398 44.7 761 499 65.6* 400 52.6* Inner Mengolia 552 257 46.6 172 31.2 614 387 63.0* 292 47.6* Hubei 589 313 53.1 243 41.3 624 382 61.2* 313 50.2* Shandong 1,161 618 53.2 420 36.2 1,400 854 61.0* 673 48.1* Jilin 654 379 58.0 297 45.4 653 389 59.6 313 47.9 Gansu 129 63 48.8 35 27.1 153 80 52.3 60 39.2* Tibet† NA NA NA NA NA 123 54 43.9 33 26.8 Total 34,867 27,888 80.0 21,848 62.7 35,578 29,982 84.3* 24,776 69.6* Note: Adequate treatment: at least one injection of 2.4 million units of intramuscular benzathine benzylpenicillin at least 30 days prior to delivery.
Abbreviation: PLADs=provincial-level administrative divisions; NA= not available.
* chi-square test statistically significant p<0.05.
† Tibet Autonomous Region starts to report the data in 2018, the data in 2017 was not available.Table 2. Treatment rates and adequate treatment rates of syphilis-seropositive pregnant women at the provincial level in China, 2017–2018.
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This analysis was a comprehensive overview of the national program on PMTCT of syphilis in China since 2011. The findings showed that the overall uptake of PMTCT program continued to increase and reached a high level, and perinatal transmission of syphilis decreased since the initiation of the PMTCT program. But the results showed that the positive rate and the disease burden of maternal syphilis increased yearly, and in 2018 nearly 46,000 syphilis-seropositive pregnant women were detected. The study confirmed that the interventions of PMTCT of syphilis were effective and need to be carried on consistently.
The findings showed that the coverage of syphilis screening among pregnant women increased consistently and was over 99% in 2018. Meanwhile, the rate of hospital delivery was 99.8% in China in 2018. Thus, the program has covered almost every pregnant woman in China. The PMTCT services were integrated with antenatal care (ANC), perinatal care, and child health care in China. The work of the maternal and child health (MCH) network guarantees the implementation of PMTCT services to a high level. As a result, the expansion of the screening coverage was in line with the increasing coverages of ANC and hospital delivery nationwide.
Our results showed that gaps still existed in achieving the national targets of treatment rate of syphilis-seropositive pregnant women and prophylaxis rate of their newborn infants over 90% by 2020. The study also found that the average level of adequate treatment (69.6% in 2018) was below the WHO treatment goal of 95%. Previous studies in China reported that third-trimester syphilis diagnosis, no treatment, or initiation of treatment after 37 weeks of gestation were significantly associated with increased risk of CS, and treatment before the third trimester and adequate treatment were protective factors (7-9). Late diagnosis and initiation of treatment might contribute to low adequate treatment rates and affect the effectiveness of the program. More effort is needed to improve uptake of screening during the first trimester, early diagnosis, and early initiation of treatment for maternal syphilis in the future.
The CS cases are mainly distributed in Xinjiang, Qinghai, Sichuan, Chongqing, and Guizhou in China (10). The result indicated that the rate of treatment in some PLADs with a high number of CS cases were relatively low or had no significant progress between 2017 and 2018. The differences in the program performed at the provincial level might be due to comprehensive factors embedded in the local context. Further studies are needed in PLADS to provide evidence to develop specific strategies to improve the uptake of treatment for maternal syphilis.
The study is subject to at least a few limitations. CS cases reported from the national information system of PMTCT of HIV, syphilis and HBV might be lower than the real figure due to lost follow-ups of infants born to infected mothers or lack of essential laboratory capacities. Hence, we used CS case data from the national STD surveillance system instead. Another limitation is that we could not analyze the screening rates during different trimesters of pregnancy because of a lack of data on gestational weeks of screening.
In conclusion, China has achieved universal coverage of PMTCT of syphilis for all pregnant women. However, comprehensive interventions need to be further strengthened to improve early screening, early diagnosis, and early initiation of treatment. Barriers to achieving high coverage of adequate treatment should be investigated and addressed at the provincial level to ensure prompt treatment for infected pregnant women.
Acknowledgments: We thank all of the researchers and health staff who have contributed to and supported the implementation of the national program of PMTCT of syphilis.
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