Syphilis test availability and uptake at medical facilities in southern China
Li-Gang Yang a, Joseph D Tucker a, Cheng Wang a, Song-Ying Shen a, Xiang-Sheng Chen b, Bin Yang a & Rosanna Peeling c
a. Guangdong Provincial Center for STI Control & Prevention, Division of STD Control, No.10 Xian Lie Dong Heng Rd, Guangzhou 510500, China.
b. National Center for STD Control, Nanjing, China.
c. Diagnostics Department, London School of Hygiene & Tropical Medicine, London, England.
Correspondence to Li-Gang Yang (e-mail: firstname.lastname@example.org).
(Submitted: 30 April 2011 – Revised version received: 16 July 2011 – Accepted: 19 July 2011 – Published online: 27 September 2011.)
Bulletin of the World Health Organization 2011;89:798-805. doi: 10.2471/BLT.11.089813
The last decade has seen a pronounced resurgence of syphilis in China,1–3 especially in south-eastern coastal provinces, which carry the greatest disease burden.4,5 One such province is Guangdong. In 2009 it reported 39 112 syphilis cases and prevalence reached 41 cases per 100 000 total population, or nearly twice the rate in all of China (25 per 100 000).6 Syphilis is now the second most commonly reported communicable disease in Guangdong province,6 where a high prevalence has been observed among female sex workers7 and men who have sex with men.8,9
Mother-to-child syphilis transmission is an important public concern in epidemic areas because syphilis can cause spontaneous abortion, stillbirth and irreversible congenital defects.10 These adverse outcomes are fortunately preventable through effective prenatal screening programmes. However, organizing such programmes is challenging, especially in places where the health system faces problems. For example, in 2001 the state of Florida in the United States of America (USA) passed a law requiring that at least two syphilis tests be administered during pregnancy, but operational research from Miami showed that only 83% of pregnant women were screened at least once.11 In a study from Mongolia, only 77% of 3519 pregnant women were screened and the presence of congenital syphilis showed an association with late-term antenatal care and with living farther from care services.12 The influence of health systems issues on timely prenatal syphilis screening has been observed in several other countries, including Bolivia, Kenya and South Africa.13
In a project in Shenzhen (Guangdong province) in which 477 656 pregnant women were screened for syphilis, 0.5% had a positive treponemal test and mother-to-child transmission was prevented in 99.1% of these cases as a result of screening.14 Although Shenzhen is the most developed city in Guangdong province and the one with the best medical infrastructure, most municipalities have far fewer resources, less equipped laboratories and limited syphilis testing capacity. The non-treponemal test, which is the one most commonly used to screen for syphilis, requires trained laboratory personnel, a refrigerator, a centrifuge and a rotator.15 Although China’s new 10-year National Syphilis Control Plan explicitly mandates widespread prenatal screening for syphilis, the existence of local capacity to undertake such screening, especially in resource constrained regions, is unclear. This study examined the status of syphilis testing capacity, prenatal syphilis screening coverage and types of syphilis tests in different types of medical facilities offering prenatal care in Guangdong province.
Guangdong province is in south-eastern China and borders the South China Sea. Several administrative levels exist in the province, from municipality down to county/district, to township and to village. In 2010 there were 21 municipalities divided into 121 counties/districts. Of these 21 municipalities, seven (Guangzhou, Zhongshan, Zhuhai, Dongguan, Shenzhen, Jiangmen and Fushan) are in the central, more developed region known as the Pearl River Delta. Of the 14 less developed, more resource-constrained municipalities, seven (Chaozhou, Shantou, Jieyang, Shanwei, Huizhou, Heyuan and Meizhou) are in the east of the province, five (Zhaoqing, Yunfu, Yangjiang, Maoming and Zhanjing) are in the west and two (Qingyuan and Shaoguan) are in the north.16 The Pearl River Delta had 11.4 primary syphilis cases per 100 000 population in 2008, a rate much higher than the province’s overall rate of 7.6 primary syphilis cases per 100 000.4 The case definition of syphilis in China includes both clinical criteria as well as laboratory confirmation with treponemal and non-treponemal tests.
Like other parts of China, Guangdong has a vertically organized public hospital system that goes from the municipal level down to the township level. A municipality generally has one municipal general hospital (known as a people’s hospital or central hospital), one municipal hospital for women and children and one municipal hospital of traditional Chinese medicine. Administratively nested within municipalities, counties and districts have corollary general hospitals, women’s and children’s hospitals and traditional Chinese medicine hospitals. Each township has one hygiene station, which is a public health-care post offering basic services. General hospitals and women’s and children’s hospitals are where most pregnant women in urban areas seek prenatal care and deliver their babies. In contrast, most women in rural China deliver their babies either at home or at a township-level hygiene station. High-risk or complicated pregnancies are referred to county- or municipal-level facilities that provide a higher level of care.
This study was conducted in the 14 less developed municipalities selected for inclusion in the health services research project. All departments for the control of sexually transmitted infections (STIs) at the municipality level were contacted by phone to invite them to participate in a research project jointly organized by the Guangdong Provincial STI Control Department and the Guangdong Provincial Health Bureau. Eleven municipalities representing all the major regions outside the Pearl River Delta agreed to participate. The local STI control centre in each of these municipalities filled out a written survey developed by the Guangdong Provincial STI Control Department in collaboration with the Guangdong Provincial Health Bureau. Since the Provincial Health Bureau has jurisdiction over all hospitals in the province, it has the authority to conduct projects that cut across different health systems. The main goal of the survey was to record data about syphilis testing in all clinical facilities where women in the administrative region give birth. Data regarding whether or not a woman was tested for syphilis were obtained from internal administrative clinic records. Women whose syphilis test results were positive were treated with antibiotics in accordance with standard Chinese guidelines.
The survey was conducted in all hospitals that delivered babies within the municipality and included the following items: name of hospital; type of hospital (general, women’s and children’s, traditional Chinese medicine, hygiene station); administrative level (municipal, county/district, township); total number of women who delivered babies in 2006–2008; number of pregnant women screened for syphilis at least once before delivery in 2006–2008; treponemal and non-treponemal syphilis screening tests available as of 2008.
Local STI control centres, with technical assistance from the Guangdong Provincial Centre for STI Control and the Provincial Health Bureau, collected all the surveys from local hospitals and reported back to the Guangdong Provincial Centre for STI Control. One hospital that had inconsistent data was contacted and asked to clarify the requested information. In line with previous research, a health systems variable analysing the number of annual pregnancies was dichotomized into > 1000 pregnancies and ≤ 1000 pregnancies.17 Data were entered into Excel 2010 (Microsoft, Redmond, USA) and analysed using SPSS 11.5 (SPSS Inc., Chicago, USA). χ2 tests and Wilcoxon ranks sum tests were used to analyse the data, with statistical significance set at P < 0.05.
This research study was exempted from ethical review by the Guangdong Provincial STD Control Centre Institutional Review Board in Guangzhou, China.
Of the 109 medical facilities studied, most (76/109) were hygiene stations and belonged to the township administrative level. Of the 109 medical facilities, 51 were in the western part of the province. The 109 medical settings recorded a total of 494 680 births from 2004–2008; 125 645 of these births occurred in 2008, and that year 57% (71 449/125 645) of the pregnant women who attended the 109 medical facilities received at least one syphilis test. Of the pregnant women in the sample who were not screened for syphilis, 61% (32 863/54 196) had attended prenatal clinics without syphilis screening capacity and 39% (21 333/54 196) had attended a clinic with screening capacity but had not been screened.
Syphilis testing capacity
Local syphilis testing capacity at medical facilities following pregnant women was limited in this sample. Of the 109 medical facilities studied, only 40 (36.7%) provided some form of syphilis testing (Table 1). The most limited syphilis testing capacity was observed at hygiene stations; of the 76 facilities of this type, only 9 (11%) performed syphilis tests. Four of the 76 hygiene stations were near municipal or county capitals; of these four hygiene stations, three offered syphilis testing. Women’s and children’s hospitals, traditional Chinese medicine hospitals and general hospitals all had significantly higher syphilis testing capacity than hygiene stations. The most limited syphilis testing capacity was seen at the township administrative level, with only 9 of the 75 (12%) medical care facilities having such capacity. Medical settings with fewer deliveries per year had more limited syphilis testing capacity. There was no difference in syphilis test capacity between different regions in Guangdong province.
Table 1. Associations between syphilis testing capacity and health system variables in Chinese medical facilities where deliveries were attended in 2008, Guangdong province, China
Prenatal syphilis testing coverage
In 2008, the 40 medical facilities with syphilis testing capacity recorded a total of 92 782 births. Only 77% (71 449/92 782) of the mothers who delivered received some form of syphilis testing. Syphilis screening coverage rates were higher at women’s and children’s hospitals, general hospitals, higher administrative levels and medical facilities with a larger number of deliveries (Table 2).
Table 2. Pregnant women screened for syphilis in different types of medical facilities, Guangdong province, China, 2008
Very few medical facilities in this study were able to meet the national benchmark of ≥ 80% for syphilis screening coverage. Of the 40 medical facilities that had syphilis testing capacity, only 26 (65%) reached the coverage benchmark, and 11 of them were children’s and women’s hospitals (Table 3).
Table 3. Predictors of > 80% pregnant women screened for syphilis at medical facilities where deliveries were attended in 2008 in Guangdong province, China
Types of syphilis tests
Of the hospitals that offered syphilis testing, very few had the capacity to perform both treponemal tests (e.g. the Treponema pallidum particle agglutination assay, or TPPA) and non-treponemal tests (e.g. the toluidine red unheated serum test, or TRUST) that are necessary to diagnose syphilis according to the Chinese case definition. The majority (85%) of medical facilities only performed non-treponemal tests. Only one women’s and children’s hospital performed both non-treponemal and treponemal tests. One tenth of all the hospitals had enzyme immunoassays for syphilis diagnosis (Table 4).
Table 4. Syphilis testing methods available at various medical facilities where deliveries were attended in 2008, Guangdong province, China
To our knowledge, this is the first description of the uptake and availability of syphilis testing in medical facilities in China. Our data show that syphilis tests are not universally available in these settings, especially in hygiene stations, where many pregnant women receive prenatal care.18
Studies in other contexts have also found low syphilis screening coverage among pregnant women. Only 57% of the pregnant women who attended the 109 hospitals included in this study received syphilis testing. This rate is higher than the average of 38% and 43% observed in sub-Saharan Africa19 and the United Republic of Tanzania,20 respectively, but lower than the 77% syphilis screening coverage rate reported in Mongolia.12 The National Syphilis Control Plan in China established a 2015 benchmark to routinely screen 80% of pregnant women in cities and 60% of pregnant women in rural areas for syphilis. Reaching the benchmark in urban areas may be easier because women’s and children’s hospitals and general hospitals, which showed high screening coverage rates in our study, are where most urban women seek prenatal care. Conversely, achieving the benchmark in rural areas may be more challenging for several reasons. First, hygiene stations are the main and sometimes only facilities that provide prenatal care in those catchment areas, and in our sample such facilities had a screening coverage of only 10.3%. Second, in less developed regions some women still give birth at home and have fewer opportunities to be tested for syphilis. The rate of delivery in health facilities has increased in recent years21 but has not reached 100% yet.
Our finding that testing capacity at hygiene stations is limited is consistent with the findings of other studies in China.22 The geographic barriers and lack of financial support described in studies outside China may be limiting syphilis testing capacity at hygiene stations in China as well.12,23 China’s new health-care reform plan emphasizes infrastructural and human resource development within the three-tier facility network (county, town and village level),24 with hygiene stations playing a key role at the township level. Health care reform may help to increase syphilis testing capacity at the local, hygiene station level, but it remains to be determined whether reform will directly affect the availability of syphilis testing and key infrastructure.
Our findings suggest that large gaps exist between routine syphilis testing capacity in resource-constrained regions of China and screening coverage targets under the National Syphilis Control Plan. However, this study was conducted in 2008 and several provincial and national programmes to improve syphilis testing capacity have been implemented since. Our findings triggered the launching of a Guangdong pilot programme for rapid syphilis testing at prenatal care facilities in the 14 study municipalities.25 The rapid treponemal test provides an inexpensive, simple and quick diagnostic method with good test characteristics.26 Our health service study describes a major opportunity to substantially expand the scope of routine syphilis testing through the use of the rapid syphilis test. Effectively providing syphilis testing and ensuring 100% prenatal screening coverage are important preconditions for successfully achieving the goals established by China’s National Syphilis Control Plan. Rapid point-of-care syphilis testing27–30 is an excellent option, especially in rural areas with limited laboratory facilities. However, laboratory quality control must be considered when implementing syphilis screening in prenatal care facilities since inaccurate syphilis testing has been described in other areas31 and in Guangdong province.32
This study has several limitations. First, the exact barriers to syphilis screening, such as lack of electricity and trained personnel, were not recorded. The National Syphilis Control Plan explicitly calls for expanding the training of medical personnel in syphilis programme management.33 Second, this study only sampled public medical facilities providing prenatal care in southern China and the findings may not be applicable to other regions and types of facilities. We believe, however, that the hygiene stations in this study are probably very similar to facilities in other middle- and low-income settings where prenatal clinics have limited infrastructure and medical personnel.34 Third, deliveries at home or in private prenatal care facilities were not sampled, and both settings are characterized by lower syphilis testing capacity.35 Finally, the timing of prenatal care, a crucial aspect of congenital syphilis prevention, was not determined.36 Timely prenatal care, preferably in the first trimester, is essential for effective syphilis prevention programmes.37
The elimination of congenital syphilis is a global health priority, but organizing effective prenatal screening, especially in the resource-constrained settings most heavily affected by congenital syphilis, remains a substantial challenge. Our research has identified the type of prenatal care facilities in these settings that would benefit the most from rapid syphilis testing. Further research is necessary to guide comprehensive implementation of the National Syphilis Control Plan in China and to meet established targets for the elimination of congenital syphilis.
This study was funded by the Guangdong Provincial Medical Science and Technology Research Funding Award(C2009020), the WHO Rapid Syphilis Test Project (UNICEF/UNDP/World Bank/WHO A70577), the National STD Control Centre and an NIH Fogarty K01 Award (US NIH 1K01TW008200-01A1).
- Chen ZQ, Zhang GC, Gong XD, Lin C, Gao X, Liang GJ, et al., et al. Syphilis in China: results of a national surveillance programme. Lancet 2007; 369: 132-8 doi: 10.1016/S0140-6736(07)60074-9 pmid: 17223476.
- Chen XS, Yin YP, Tucker JD, Gao X, Cheng F, Wang TF, et al., et al. Detection of acute and established HIV infections in sexually transmitted disease clinics in Guangxi, China: implications for screening and prevention of HIV infection. J Infect Dis 2007; 196: 1654-61 doi: 10.1086/522008 pmid: 18008249.
- Tucker JD, Chen XS, Peeling RW. Syphilis and social upheaval in China. N Engl J Med 2010; 362: 1658-61 doi: 10.1056/NEJMp0911149 pmid: 20445179.
- Yang LG, Tucker JD, Yang B, Shen SY, Sun XF, Chen YF, et al., et al. Primary syphilis cases in Guangdong province 1995–2008: opportunities for linking syphilis control and regional development. BMC Public Health 2010; 10: 793- doi: 10.1186/1471-2458-10-793 pmid: 21192782.
- The national syphilis and gonorrhea epidemiology analysis report 2009. Nanjing: National Centre for STD Control; 2009.
- Yang L. Annual STD surveillance for Guangdong province, China. Presented at the Guangdong Annual STI Control Conference, Huidong, China, 15–16 April 2010.
- Li Y, Detels R, Lin P, Fu X, Deng Z, Liu Y, et al., et al. Prevalence of HIV and STIs and associated risk factors among female sex workers in Guangdong province, China. J Acquir Immune Defic Syndr 2010; 53: S48-53 doi: 10.1097/QAI.0b013e3181c7d72f pmid: 20104110.
- Feng TJ, Liu XL, Cai YM, Pan P, Hong FC, Jiang WN, et al., et al. Prevalence of syphilis and human immunodeficiency virus infections among men who have sex with men in Shenzhen, China: 2005 to 2007. Sex Transm Dis 2008; 35: 1022-4 pmid: 18830135.
- He Q, Wang Y, Lin P, Raymond HF, Li Y, Yang F, et al., et al. High prevalence of risk behaviour concurrent with links to other high-risk populations: a potentially explosive HIV epidemic among men who have sex with men in Guangzhou, China. Sex Transm Infect 2009; 85: 383-90 doi: 10.1136/sti.2009.035808 pmid: 19357129.
- Sparling PF, Swartz MN, Musher DM, Healy BP. Clinical manifestations of syphilis. Chapter 37. In: Holmes KK, Sparling PF, Stamm WE, et al., editors. Sexually transmitted diseases. 4th ed. New York: McGraw-Hill; 2008. pp. 661-84.
- Trepka MJ, Bloom SA, Zhang G, Kim S, Nobles RE. Inadequate syphilis screening among women with prenatal care in a community with a high syphilis incidence. Sex Transm Dis 2006; 33: 670-4 doi: 10.1097/01.olq.0000216032.52731.ea pmid: 16641827.
- Munkhuu B, Liabsuetrakul T, Chongsuvivatwong V, Geater A, Janchiv R. Coverage of antenatal syphilis screening and predictors for not being screened in Ulaanbaatar, Mongolia. Sex Transm Dis 2006; 33: 284-8 doi: 10.1097/01.olq.0000194577.71693.c7 pmid: 16641821.
- Deperthes BD, Meheus A, O’Reilly K, Broutet N. Maternal and congenital syphilis programmes: case studies in Bolivia, Kenya and South Africa. Bull World Health Organ 2004; 82: 410-6 pmid: 15356932.
- Cheng JQ, Zhou H, Hong FC, Zhang D, Zhang YJ, Pan P, et al., et al. Syphilis screening and intervention in 500,000 pregnant women in Shenzhen, the People’s Republic of China. Sex Transm Infect 2007; 83: 347-50 doi: 10.1136/sti.2006.023655 pmid: 17693449.
- Larsen SA, Steiner BM, Rudolph AH. Laboratory diagnosis and interpretation of tests for syphilis. Clin Microbiol Rev 1995; 8: 1-21 pmid: 7704889.
- Lin C. Red capitalism in South China: growth and development of the Pearl River Delta. Vancouver: UBC Press; 1997.
- Yeast JD, Poskin M, Stockbauer JW, Shaffer S. Changing patterns in regionalization of perinatal care and the impact on neonatal mortality. Am J Obstet Gynecol 1998; 178: 131-5 doi: 10.1016/S0002-9378(98)70639-8 pmid: 9465816.
- Mu L. Quality indicators of obstetrical facilities in Guangdong province 2005. 2006;21:1604-5.
- Gloyd S, Chai S, Mercer MA. Antenatal syphilis in sub-Saharan Africa: missed opportunities for mortality reduction. Health Policy Plan 2001; 16: 29-34 doi: 10.1093/heapol/16.1.29 pmid: 11238427.
- Watson-Jones D, Oliff M, Terris-Prestholt F, Changalucha J, Gumodoka B, Mayaud P, et al., et al. Antenatal syphilis screening in sub-Saharan Africa: lessons learned from Tanzania. Trop Med Int Health 2005; 10: 934-43 doi: 10.1111/j.1365-3156.2005.01473.x pmid: 16135202.
- Liu Y, Rao K, Wu J, Gakidou E. China’s health system performance. Lancet 2008; 372: 1914-23 doi: 10.1016/S0140-6736(08)61362-8 pmid: 18930536.
- Ye X, Wang Y, Luo Y, Gao C, Xia B. Investigation report of hygiene stations in Anhui province. J Anhui Hygiene Technol College 2001; 1: 7-.
- Gloyd S, Montoya P, Floriano F, Chadreque MC, Pfeiffer J, Gimbel-Sherr K. Scaling up antenatal syphilis screening in Mozambique: transforming policy to action. Sex Transm Dis 2007; 34: S31-6 doi: 10.1097/01.olq.0000264586.49616.72 pmid: 17592388.
- Chen Z. Launch of the health-care reform plan in China. Lancet 2009; 373: 1322-4 doi: 10.1016/S0140-6736(09)60753-4 pmid: 19376436.
- Yang LG. Guangdong provincial STD control projects, 2010. Presented at the Guangdong Annual STD Workshop Conference, Shaoguang, China, 14–16 April 2011.
- Tucker JD, Bu J, Brown LB, Yin YP, Chen XS, Cohen MS. Accelerating worldwide syphilis screening through rapid testing: a systematic review. Lancet Infect Dis 2010; 10: 381-6 doi: 10.1016/S1473-3099(10)70092-X pmid: 20510278.
- Bronzan RN, Mwesigwa-Kayongo DC, Narkunas D, Schmid GP, Neilsen GA, Ballard RC, et al., et al. On-site rapid antenatal syphilis screening with an immunochromatographic strip improves case detection and treatment in rural South African clinics. Sex Transm Dis 2007; 34: S55-60 doi: 10.1097/01.olq.0000245987.78067.0c pmid: 17139234.
- Munkhuu B, Liabsuetrakul T, Chongsuvivatwong V, McNeil E, Janchiv R. One-stop service for antenatal syphilis screening and prevention of congenital syphilis in Ulaanbaatar, Mongolia: a cluster randomized trial. Sex Transm Dis 2009; 36: 714-20 doi: 10.1097/OLQ.0b013e3181bc0960 pmid: 19773681.
- Munkhuu B, Liabsuetrakul T, McNeil E, Janchiv R. Feasibility of one-stop antenatal syphilis screening in Ulaanbaatar, Mongolia: women and providers perspectives. Southeast Asian J Trop Med Public Health 2009; 40: 861-70 pmid: 19842425.
- Vickerman P, Peeling RW, Terris-Prestholt F, Changalucha J, Mabey D, Watson-Jones D, et al., et al. Modelling the cost-effectiveness of introducing rapid syphilis tests into an antenatal syphilis screening programme in Mwanza, Tanzania. Sex Transm Infect 2006; 82: v38-43 doi: 10.1136/sti.2006.021824 pmid: 17215276.
- Majoko F, Munjanja S, Nystrom L, Mason E, Lindmark G. Field efficiency of syphilis screening in antenatal care: lessons from Gutu District in Zimbabwe. Cent Afr J Med 2003; 49: 90-3 pmid: 15214281.
- Xing-zhon W, He-ping Z, Jin-mei H. Quality evaluation and proficiency testing of serological test of syphilis from 2004 to 2006 in Guangdong. Chinese J Dermatol 2008; 41: 314-.
- Tucker JD, Cohen MS. China’s syphilis epidemic: epidemiology, proximate determinants of spread, and control responses. Curr Opin Infect Dis 2011; 24: 50-5 doi: 10.1097/QCO.0b013e32834204bf pmid: 21150594.
- Lehmann U, Dieleman M, Martineau T. Staffing remote rural areas in middle- and low-income countries: a literature review of attraction and retention. BMC Health Serv Res 2008; 8: 19- doi: 10.1186/1472-6963-8-19 pmid: 18215313.
- Tucker JD, Yang LG, Zhu ZJ, Yang B, Yin YP, Cohen MS, et al., et al. Integrated syphilis/HIV screening in China: a qualitative analysis. BMC Health Serv Res 2010; 10: 58- doi: 10.1186/1472-6963-10-58 pmid: 20205942.
- Zhu L, Qin M, Du L, Xie RH, Wong T, Wen SW. Maternal and congenital syphilis in Shanghai, China, 2002 to 2006. Int J Infect Dis 2010; 14: e45-8 doi: 10.1016/j.ijid.2009.09.009 pmid: 20137991.
- Kamb ML, Newman LM, Riley PL, Mark J, Hawkes SJ, et al., et al. A road map for the global elimination of congenital syphilis. Obstet Gynecol Int 2010Epub Jul 14- pmid: 20706693.