Objectives: To measure the coverage of antenatal syphilis screening and identify factors related to women not being screened.
Goal: To assess the syphilis control program in Mongolia.
Study design: Antenatal care records of women in 16 antenatal care clinics of 6 districts were reviewed. Additionally, postpartum women were interviewed to identify potential factors for not being screened.
Results: Among 3519 antenatal records, the coverage of syphilis screening was 77.7%. Of 2735 screened women, 54 (2.0%) had reactive serological results and subsequently received treatment. Four late antenatal care comers delivered infants with congenital syphilis. Being unscreened was significantly associated with late antenatal care (odds ratio OR = 2.6), lack of knowledge (OR = 5.5), history of previous sexually transmitted infection (OR = 3.7), and living far from screening services (OR = 4.9).
Conclusions: The coverage of antenatal syphilis screening is still low, with poor contact tracing. More efforts are needed to promote early antenatal care visit and improve syphilis screening systems.
Antenatal syphilis screening in Ulaanbaatar, Mongolia, has low coverage with poor contact tracing. Lack of knowledge and living far from syphilis screening services strongly increased the risk of not being screened.
From the *Department of Human Reproduction and Medical Genetics, State Research Center on Maternal and Child Health, Ulaanbaatar, Mongolia; and the †Epidemiology Unit, Faculty of Medicine, Prince of Songkla University, Songkhla, Thailand
This study was conducted while the first author was in receipt of a WHO Research Training Grant from Special Programme of Research, Development and Research Training in Human Reproduction. The Epidemiology Unit is partially supported by the Thailand Research Fund and Thai Health Promotion Foundation through the Senior Research Scholar Grant to Prof. Virasakdi Chongsuvivatwong.
Correspondence: Tippawan Liabsuetrakul, MD, PhD, Epidemiology Unit, Faculty of Medicine, Prince of Songkla University, Hat Yai, Songkhla, 90110, Thailand. E-mail: firstname.lastname@example.org.
SYPHILIS IN PREGNANCY AS a sexually transmitted infection (STI) is an important public health problem because it can lead to serious complications such as spontaneous abortion, stillbirth, and congenital infection. In Mongolia, over the past decade syphilis, as well as other STIs, has increased in the aftermath of the sudden breakup of the socialist regime and rapid political and economic changes.1 Also the incidence of syphilis in pregnant women during delivery has increased from no reported cases in 1988 to 21 cases in 1999 and 26 cases in 2000 in the State Research Center on Maternal and Child Health (MCH), whereas the number of deliveries has decreased.2 Congenital syphilis was recorded in 2 new case reports in 1995 in Ulaanbaatar and has continuously increased to 43 new cases in 2000.3
Early detection and treatment of syphilis in pregnant women is a standard measure for preventing congenital syphilis.4,5 With this noble purpose, antenatal syphilis screening (ASYS) on the first day of registration of a pregnant woman is a mandatory procedure.5 Now there are new evidence and recommendations that routine testing should be repeated in the third trimester, even in low-prevalence areas.6
Current regulations regarding ASYS in Ulaanbaatar, Mongolia, stipulate that only a few specialized laboratories for sexually transmitted diseases (STD) at the STD clinics and district general hospitals are allowed to perform the ASYS test. Also, only venereologists at the STD clinic and STD cabinets of district general hospitals are authorized to treat syphilis-infected pregnant women and undertake contact tracing. Although every antenatal care (ANC) clinic has a laboratory for urine, blood, and biochemical tests, they do not perform the serological syphilis test. Therefore, they have to send each woman to an STD laboratory for syphilis testing.
The reported positive syphilis in pregnant women and congenital syphilis have increased despite ASYS being announced and practiced routinely in Mongolia. Although the country has good systems of registration for reflecting the burden of illness and coverage of health services, there is no system for collating such important data. There is a need to review these situations and to identify risk factors for not conducting ASYS. This study aims to measure the coverage of ASYS and case management in Ulaanbaatar, Mongolia, and to identify factors related to women not being screened.
Materials and Methods
Ulaanbaatar, Mongolia, comprises 6 districts having a reported 11,000 live births per year, and 99% of all deliveries occur in 3 maternity homes and the MCH center. Antenatal care (ANC) for pregnant women is provided by a total of 16 ANC clinics, comprising 2 to 4 ANC clinics under each district general hospital. The reported ANC coverage was 97% in Ulaanbaatar in 2000.2 According to the national guidelines, serological rapid plasma reagin (RPR) test for syphilis is performed at the first ANC visit and at the third trimester free of charge. Confirmatory Treponema pallidum hemagglutination (TPHA) test is done in case of positive screening test. Sexual partners of women with reactive tests should be notified and tested. The case and her husband/sexual partner are to be treated with 3 weekly doses of 2.4 million IU of benzathine penicillin G.
Components of the Study
The study was approved by the ethics committee of the State Research Center on MCH, Ulaanbaatar, Mongolia, and consisted of 2 parts: a retrospective review of ANC records and a cross-sectional interview study with postpartum women. For the first part, raw data were obtained from ANC records of all 16 ANC clinics during January 2002 to January 2003 to measure the ASYS coverage. To calculate the sample size for this part, we assumed a prevalence of screening of about 60% of ANC attendees, to be estimated with a precision (95% confidence interval) of ±10% points. Thus, we needed at least 96 records from each service unit. Socioeconomic variables available in this dataset included age, residence, educational level, employment, and marital status.
For the second part, the postpartum women admitted at 3 maternity homes and MCH centers during June 2003 to September 2003 were approached for verbal informed consent and interviewed to identify the potential predictors for not being screened. Among the screened women, we assumed 10% exposure to a risk factor (e.g., staying far from the service unit). This percentage was assumed to be 20% among the unscreened. Given α = 0.05, β = 0.2, and estimated ratio of screened:unscreened of 3:2, the sample size required for this part was 267 screened and 178 unscreened women, and all consecutive cases during the study period were recruited. In analysis of the risk factors, the outcome variable was ASYS status as screened (0) and unscreened (1). The predictor variables to be tested were age, marital status, education, residence, risky sexual behavior, gestational age at first ANC, history of previous STI, knowledge about infection and ASYS, and travel time from a woman’s home to ANC clinic and to ASYS service in minutes.
Questions on risky sexual behavior covered extramarital sex, new sexual partner in the past 12 months, casual sex, exchange of sex for money, and not using a condom with extramarital partners. Knowledge about the infection and ASYS was measured by the following 4 questions: “Is syphilis harmful for a pregnant woman’s health?” “Is syphilis dangerous for an unborn baby?” “Is the blood test for syphilis necessary among pregnant women?” and “Is the blood test for syphilis useful for preventing your unborn baby from infection?” Each question was scored “0” for an undecided answer, “−1” for an incorrect answer, “+1” for a correct answer. The scores were then summed and the total score cut into 2 levels: “positive” if the total score was >0 and “negative” if the total score was ≤0.
Data were computerized using Epi-Info 6.04 (Centers for Disease Control and Prevention, Atlanta, GA) and analyzed using Stata 7.0 (Stata Corporation, 2000) software. The coverage of ASYS was described as percentage adjusted for available demographic variables. Univariate comparison of screened and unscreened women was performed using χ2 test, and the variables with a significance level of 0.2 or less were initially included in a logistic regression model. Those with highest likelihood ratio P value were removed one by one based on backward elimination strategy until the model contained only significant variables with P ≤0.05.
Part 1: Coverage of ASYS and Case Management
Out of 3519 ANC reviewed records, 2735 women were tested for syphilis during pregnancy (77.7%, 95% CI 76.3%–79.1%). Stratification by district general hospital showed that the coverage of syphilis screening during pregnancy in the district general hospitals 5 and 6 was lower than that in the other hospitals, even after adjusting for woman’s age, residence, education level, employment, and marital status (Table 1).
Figure 1 shows the flow chart of the coverage of ASYS and case management in this study. Among all 3519 pregnant women reviewed, 697 (19.8%) women attended the ANC clinics for the first time when the gestational age was over 28 weeks of gestation. The proportion of unscreened in this group was high (54.8%) when compared with the proportion among those who came before the 28 weeks (14.2%). All 54 serological positive cases received an adequate dose of benzathine penicillin G (3 weekly doses of 2.4 million IU), except 2 cases who were allergic to penicillin and were treated with oral erythromycin. Thirty-one sexual partners of cases with reactive serology (57.4%) were notified for a blood test, and the results were all reactive, but only 12 of them were documented as having been treated. After a month of treatment, a repeat RPR test was performed in only 50 out of the 54 cases, and the titer decreased in 42. The remaining 8 were retreated, resulting in subsequent fall of titer a month later. Eventually, 4 positive mothers, who had first ANC visit after 28 weeks of gestation, delivered liveborn infants with early congenital syphilis. One of them had not been screened and was not treated antenatally.
Part 2: Factors Related to Women Not Being Screened
Totally, 445 women were interviewed (267 screened and 178 unscreened). The mean age of the interviewed postpartum women was 26.9 years (range, 17–43 years) and there was no significant difference in mean age between the screened (26.6 years) and unscreened (27.4 years). Univariate comparisons of demographic, behavioral, and ANC characteristics of screened and unscreened women are displayed in Table 2. The unscreened group was significantly more likely to be unmarried, have lower level education, to reside outside Ulaanbaatar, to report risky sexual behavior and previous STI, to come for ANC later than 28 weeks of gestation, to have less knowledge on the infection/ASYS, and to live far from ANC and ASYS services.
Table 3 summarizes the independent risk factors for being unscreened using multivariate logistic regression analysis. The odds of unscreened status were increased significantly in women having late ANC (OR = 2.6, 95% CI 1.6–4.2), having lack of knowledge about the infection and ASYS (OR = 5.5, 95% CI 2.7–11.3), reporting previous STI (OR = 3.7, 95% CI 1.5–9.2), and living far from ASYS service unit (OR = 4.9, 95% CI 3.0–7.8). Interaction terms did not contribute significantly to the fit of the model.
Despite free ASYS, almost a quarter of pregnant women attending ANC in the study did not get it. Of those who were screened, about a fifth had it late (greater than 28 weeks of gestation), and as many as 1 in 50 had reactive test results. Among the positive cases, the cure was confirmed in 90%, but the contact tracing and treatment were completed in only 57% and 22%, respectively. Finally, about 6% of detected and treated mothers gave birth to liveborn infants with congenital syphilis.
The percentage of the ASYS coverage in the current study was higher than the percentages reported in studies from some other developing countries.7–9 However, it was still low because universal ASYS is recommended4 and provided free of charge in Ulaanbaatar, Mongolia. It is of critical concern that women coming for ANC in the first or second trimesters remain unscreened. This shows an inadequacy of the syphilis screening in pregnancy. Low ASYS in 2 districts (5 and 6) may be explained by the fact that these districts are the most remote where the women have difficulty getting to the ANC clinics, leading to their showing up late for ANC. This is supported by the more advanced mean gestational ages at first ANC of pregnant women in these districts compared with that in the other districts.
Moreover, the effect of distance from the patients’ accommodation (mainly Mongolian traditional tents/gers) to the health services center and late attendance for the first ANC were confirmed in the second part of this study where these issues were explored through direct interview. Laboratories in ANC clinics have not performed the syphilis test; thus, pregnant women have to go to STD clinics or district general hospitals for testing. Performing this test in different places from the ANC clinics leads to pregnant women’s having to undertake extra long travel, with the consequent delay or failure to be screened. Combining with ANC providers’ ignorance, pregnant women missed the chance of ASYS, although these women came for ANC in time. For policy implications, there is a great need to produce a special educational program for pregnant women to promote their general awareness on early ANC and STI prevention and for ANC providers regarding the need for universal ASYS and counseling skills because providers play an essential role in women’s health-seeking behavior. A 1-stop service including ANC and the ASYS test in the same place is the critical issue that needs to be implemented.
Screening pregnant women for syphilis, treating those who are seroreactive, and preventing reinfection will be effective if screening is performed early in pregnancy10 because the fetus can be infected before the 12th week of gestation.11 Although the national ANC coverage reported was high (97%) in Mongolia, one-fifth of the pregnant women in our study initiated ANC late in pregnancy. Our results revealed that late first ANC is strongly associated with decreased ASYS and congenital syphilis cases occurred in women who had late ANC.
Identified potential factors for not being screened in our study are similar to the risk factors of infants with congenital syphilis such as unmarried status, lower education level, remote residence, having risky sexual behavior, lack of ANC, as well as starting ANC late, which were reported previously in both developed and developing countries.12–16 Thus, these patients are a very important target population for correcting the problem. An additional significant factor associated with failure of ASYS was lack of awareness about the infection/screening. Women with previous history of STI were also less likely to be tested for syphilis. A history of previous STI was reported as being a risk factor for early congenital syphilis in a study from Malaysia.17 This may indicate that despite being at high risk for STI, these women may have other barriers to access to health care.
The sudden rise of syphilis/STI was noted not only in Mongolia1–3 but also in both neighboring countries, i.e., Russia18 and China,19 and among the postcommunist East European and Central Asian states.20 This confirms that the countries that have rapid changes in social and sexual behavioral lives urgently need to assess the magnitude of syphilis in pregnancy and congenital syphilis, the system of ASYS services, and the national disease control program. Pregnant women, ANC providers, and the system of ANC and ASYS are the important factors for the coverage of ASYS, as well as the reasons for not being screened, which were revealed in this study. To achieve the goal of eliminating congenital syphilis globally, these factors need to be explored vigorously in the countries with high prevalence of syphilis in pregnancy, congenital syphilis, and low coverage of antenatal screening.
Retrospective review of ANC records in ANC clinics may result in a limitation to finding information on some pregnant women who might have obtained a RPR test in private laboratories with no documentation in the ANC records, leading to an underestimation of ASYS coverage. However, such cases are very few because the serological test for syphilis is expensive in those laboratories. Our study reviewed all 16 ANC clinics of 6 district general hospitals and should represent the actual coverage of ASYS in Ulaanbaatar, Mongolia. Although the interview of postpartum women to identify factors influencing screening status could result in recall or information bias, such bias was reduced by using well-trained interviewers who were local caregivers, whom the postpartum women trusted and who were masked to the results of ASYS.
In conclusion, the coverage of ASYS is still low in Ulaanbaatar, with poor contact tracing. The failure of universal ASYS as WHO recommended was detected. Pregnant women’s knowledge on the importance of early ANC, awareness of infection and ASYS, and convenience of the ASYS system are essential to raise the coverage of ASYS and probably decline the factors for not being screened. Consultation and promotion of knowledge about infection and the need for ASYS should be introduced to every ANC clinic in order to reduce the proportion of unscreened and untreated pregnant women and the incidence of congenital syphilis in Ulaanbaatar.
1. Purevdawa E, Moon TD, Baigalmaa C, et al. Rise in sexually transmitted diseases during democratization and economic crisis in Mongolia. Int J STD AIDS 1997; 8:398–401.
2. State Research Center on Maternal and Child Health. Annual Statistics of State Research Center on Maternal and Child Health 2000, Ulaanbaatar: State Research Center on Maternal and Child Health, 2000.
3. Ministry of Health, National Center for Health Development. Health Indicators of Mongolia 2000. Ulaanbaatar: Ministry of Health, 2000.
4. World Health Organization. Maternal and Perinatal Infection: Report of a WHO Consultation. Geneva: World Health Organization, 1991.
5. Centers for Disease Control and Prevention. Sexually transmitted diseases treatment guidelines 2002. MMWR Recomm Rep 2002; 51:1–78.
6. Lumbiganon P, Piaggio G, Villar J, et al. The epidemiology of syphilis in pregnancy. Int J STD AIDS 2002; 13:486–494.
7. Southwick KL, Blanco S, Santander A, et al. Maternal and congenital syphilis in Bolivia, 1996: prevalence and risk factors. Bull World Health Organ 2001; 79:33–42.
8. Tikhonova L, Salakhov E, Southwick K, et al. Congenital syphilis in the Russian Federation: magnitude, determinants, and consequences. Sex Transm Infect 2003; 79:106–110.
9. Temmerman M, Gichangi P, Fonck K, et al. Effect of a syphilis control programme on pregnancy outcome in Nairobi, Kenya. Sex Transm Infect 2000; 76:117–121.
10. Watson-Jones D, Gumodoka B, Weiss H, et al. Syphilis in pregnancy in Tanzania, II: the effectiveness of antenatal syphilis screening and single dose benzathine penicillin treatment for the prevention of adverse pregnancy outcomes. J Infect Dis 2002; 186:948–957.
11. Berman SM. Maternal syphilis: pathophysiology and treatment. Bull World Health Organ 2004; 82:433–438.
12. Walker DG, Walker GJ. Forgotten but not gone: the continuing scourge of congenital syphilis. Lancet Infect Dis 2002; 2:432–436.
13. Warner L, Rochat RW, Fichtner RR, et al. Missed opportunities for congenital syphilis prevention in an urban southeastern hospital. Sex Transm Dis 2001; 28:92–98.
14. Rawstron SA, Jenkins S, Blanchard S, et al. Maternal and congenital syphilis in Brooklyn, NY: epidemiology, transmission, and diagnosis. Am J Dis Child 1993; 147:727–731.
15. Mobley JA, McKeown RE, Jackson KL, et al. Risk factors for congenital syphilis in infants of women with syphilis in South Carolina, USA. Am J Public Health 1998; 88:597–602.
16. Desenclos JC, Scaggs M, Wroten JE. Characteristics of mothers of live infants with congenital syphilis in Florida, 1987–1989. Am J Epidemiol 1992; 136:657–661.
17. Lim CT, Koh MT, Sivanesaratnam V. Early congenital syphilis: a continuing problem in Malaysia. Med J Malaysia 1995; 50:131–135.
18. Borisenko KK, Tichonova LI, Renton AM. Syphilis and other sexually transmitted infections in the Russian Federation. Int J STD AIDS 1999; 10:665–668.
19. Chen XS, Gong XD, Liang GJ, Zhang GC. Epidemiological trends of sexually transmitted diseases in China. Sex Transm Dis 2000; 27:138–142.
20. Renton AM, Borisenko KK, Meheus A, Gromyko A. Epidemics of syphilis in the newly independent states of the former Soviet Union. Sex Transm Infect 1998; 74:165–166.