Background: This cluster randomized trial was performed to test whether one-stop service could better prevent congenital syphilis than the conventional antenatal screening service in Mongolia.
Methods: Out of 14 antenatal clinics in 6 districts of Ulaanbaatar, 7 were randomly selected for the one-stop service and the remaining for the conventional service. Intervention clinics provided on-site rapid syphilis testing and immediate treatment for positive cases and their partners. In control clinics, syphilis screening services with routine off-site rapid plasma regain testing and case management were followed. Analysis was intention to treat.
Results: Of 3850 antenatal women recruited in each group, the proportion of syphilis testing at the first visit and third trimester was over 99% in the intervention group and 79.6% and 61.5% in the control group, respectively (P <0.001 for both periods). Correspondingly, syphilis cases detected in the intervention group were 73 (1.9%) and 20 (0.5%) for the first visit and third trimester, respectively, and 27 (0.9%) and 2 (0.08%) in the control group; and 98.9% (92/93) of the detected cases in the intervention group and 89.6% (26/29) in the control group were adequately treated (P = 0.02). The corresponding treatment rates for sexual partners were 94.6% and 55.2% (P <0.001). One congenital syphilis case out of 3632 deliveries in the intervention group, compared to 15 of 3552 in the control group, was diagnosed, a reduction of 93.5% (95% confidence interval, 66.0%–98.6%).
Conclusions: One-stop services increased the detection rate of syphilis, treated more positive women and their partners, and effectively reduced the rate of congenital syphilis.
One-stop services increased the detection rate of syphilis, treated more syphilis infected antenatal women and their partners, and effectively reduced rate of congenital syphilis.
From the *Department of Human Reproduction and Medical Genetics, State Research Center on Maternal and Child Health, Ulaanbaatar, Mongolia; and †Epidemiology Unit, Prince of Songkla University, Songkhla, Thailand
The authors thank the staff of the intervention and control clinics, the district health supervisors of the 6 participating district general hospitals (Drs. Panzila, Ariumaa, Tsetsegmaa, Davaasuren, Sainbuyan, and Erdenechimeg) and all the participating women. The authors also like to thank Katherine Ba-Thike (WHO HQ), Massimo Ghidinelli (WHO Regional Office for the Western Pacific), and Narantuya (WHO Country Office in Mongolia), for their valuable comments.
Supported by the Special Programme of Research, Development and Research Training in Human Reproduction, World Health Organization, through a re-entry grant awarded to the first author.
Correspondence: Bayalag Munkhuu, MD, MSc, Department of Medical Genetics and Human Reproduction, State Research Center on Maternal and Child Health, Amarsanaa St, PO box 24/677, Bayangol District, Ulaanbaatar, Mongolia. E-mail: firstname.lastname@example.org.
Received for publication February 3, 2009, and accepted April 15, 2009.
Congenital syphilis is a serious but preventable disease. Antenatal syphilis screening (ASYS) is one of the most effective ways for prevention and most countries do have policies providing for universal screening for syphilis in pregnant women. However, for various reasons, in many developing countries the policies are not systematically implemented, resulting in failure of the syphilis seropositive couples to receive treatment during the course of the pregnancy.1–3
The rapid increase in number of cases of active syphilis, as well as other sexually transmitted infections (STIs), among adults during the past decades can be attributed to the rapid social, economical and behavioral changes in the country.4,5 As a result, the incidence of congenital syphilis has been increasing and consequently is raising a public health concern in Mongolia. Congenital syphilis was recorded in 2 new case reports in 1995 and has increased to 51 new cases in 2006.4 The actual number was likely to be much higher since the diagnosis was based on clinical criteria only. Adverse pregnancy outcomes, such as miscarriages and stillbirths due to maternal syphilis, are usually not diagnosed and thus underreported.
The current resurgence of congenital syphilis is an indication of the difficulties experienced by basic services of antenatal care (ANC) and ASYS in Mongolia. There are approximately 55,000 births reported annually and about 98% of pregnant women attend antenatal services.4 Although syphilis screening for pregnant women is usually provided free of charge in ANC services, only a fraction is actually screened. In 2006, the ASYS coverage was reported in 77% in Ulaanbaatar, the capital city of Mongolia,6 and 60.9% nationally; however, this rate was less than 50% among those who live in rural remote regions or among nomadic women.4
Routine ASYS regulations in the country stipulate that only a few specialized laboratories for STIs are allowed to perform syphilis tests and only venereologists are authorized to treat syphilis infected pregnant women and undertake contact tracing. This organization of the services has led to antenatal women needing to travel to the laboratories, situated at the District General Hospitals or at the National Center of Infectious Diseases (NCID). The tests are done in batches, resulting in delay of diagnosis and treatment and inconvenience to the clients discouraging them from actively participating in the prevention of congenital syphilis policy.
Although the ANC coverage is high and ASYS is provided free of charge, around a quarter of pregnant women were not tested and thus missed being treated. This indicates a need to improve the services of which the complexity of ASYS was mainly hypothesized. A one-stop service for ASYS with on-site rapid syphilis test, prompt treatment of syphilis cases and their sexual partners, and counseling at the same place or antenatal clinics was therefore planned. The aim of this trial was to test whether the one-stop service could better prevent congenital syphilis than the conventional ASYS service in Ulaanbaatar, Mongolia.
MATERIALS AND METHODS
Since the intervention was based on practices, rather than individuals, it was considered impossible to randomize the individual patients into 2 screening options in the same clinics. A cluster randomized trial was thus applied.
The study protocol was reviewed and approved by the Institutional Ethics Committee of Mongolia, the corresponding health authorities where the trial was implemented, the Scientific and Ethical Review Group of the Special Programme of Research, Development, and Research Training in Human Reproduction, World Health Organization (WHO), and the WHO Ethics Review Committee.
Study Areas and Participants
There are approximately 11,000 live births per year in Ulaanbaatar, and 99% of these occur in 3 maternity hospitals and the State Research Centre on Maternal and Child Health (MCH Center). ANC services are provided by 16 antenatal clinics linked to 6 district general hospitals and MCH Center. The MCH Center was excluded from sampling because the centre is responsible for the whole country, while 2 of the 16 antenatal clinics were also excluded due to a small attendance. Of the remaining 14 antenatal clinics, 7 were randomly assigned into the intervention group. The rest were assigned to the conventional service group. Figure 1 shows locations of the 14 antenatal clinics and NCID in Ulaanbaatar. The identification of the intervention or control group was not shown and kept anonymously due to ethical issues.
All new ANC attendees with a single pregnancy were eligible for the study. Predefined exclusion criteria were: women known to be unable to return for the scheduled antenatal visit during the study period, living outside Ulaanbaatar, unwilling to give informed consent, and absence of a willing guardian for under aged women.
ANC providers in both intervention and control clinics received training but the contents provided were different. Two separate workshops for the intervention and control groups were organized.
In the intervention clinics, the first 2-day workshop was held for obstetrician-gynecologists (OB-GYNs) and nurses. The main agendas included highlighting the importance of decentralizing the ASYS service, logistics, the organization of the one-stop service, and case reporting. The second 2-day workshop was also held for OB-GYNs and covered the specific knowledge on maternal and congenital syphilis, case detection and management, counseling, and contact tracing. A manual of the test reading was distributed to all relevant providers in order to assure a correct and reliable interpretation of the rapid syphilis test results. The intervention clinics were supplied with the necessary materials, such as lancet, rapid syphilis tests, and benzathine penicillin injectable sets.
In the control clinics, ANC providers (nurses and OB-GYNs) in the control clinics participated in a 2-day training workshop on the project overview, logistics of the project, and case reporting. The OB-GYNs received refresher training on the same topics as the intervention group to reduce the bias of training effect on our main outcomes. As with the intervention group, treatment of syphilis cases and their partners was given free of charge. Benzathine penicillin was supplied for treatment but not facilities for serological tests.
In both intervention and control clinics, all pregnant women presenting to the antenatal clinics were checked by the nurses on their eligibility for entering the study. All eligible subjects were then approached, given information about the study, and asked to join. Subjects who agreed were then asked to give informed consent to participate in the study. The syphilis tests were done twice during pregnancy at the first antenatal visit and at the third trimester of gestation. The third syphilis testing was provided immediately after delivery among the women who had been seronegative during ANC. Regardless of the group randomized to, all syphilis cases received 3 doses of benzathine penicillin on a weekly basis. Neonates of seropositive women were then examined and positive cases were given an injection of benzathine penicillin following the WHO guidelines.7
ASYS in the Intervention Clinics.
The one-stop service included the following elements (i) on-site screening for syphilis using rapid treponemal syphilis tests at the first antenatal visit and at the third trimester of gestation; (ii) immediate on-site treatment for seropositive women and their sexual partners with benzathine penicillin; and (iii) pre- and posttest counseling.
Pretest counseling and interviews were carried out in a private counseling room. After the interview, about 10 μL of whole blood from all consenting new attendees was collected by finger prick. The on-site rapid test was assayed with SD Bioline Syphilis 3.0 (Standard Diagnostics Inc., Kyunggi-do, Korea) according to the manufacturer’s specifications. The results were available in 10 to 15 minutes. Women testing negative on the rapid assays were provided with posttest counseling by ANC providers and invited for second testing during the third trimester of pregnancy. Women testing positive by the rapid test had their venous blood further collected and sent to the reference laboratory. Women without a history of drug allergy were initially treated free of charge with initial dose of benzathine penicillin G 2.4 million units intramuscular. The confirmation test at the reference laboratory was carried out using Rapid Plasma Regain (RPR) titre (Omega Immutrep-RPR, Omega Diagnostics, Alva, United Kingdom) and the positive samples were further tested Treponema pallidum hemagglutination (TPHA) (Immutrep TPHA, Omega Diagnostics, Alva, United Kingdom). Women who tested positive on both RPR and TPHA tests were subsequently given 2 doses of benzathine penicillin at weekly intervals. The contact tracing was based on a voluntary agreement between the woman and the OB-GYN. The husbands/sexual partners were invited to come at their earliest convenience to the clinics for free treatment.
All women attending for ANC who had been seronegative at the first visit were retested by the rapid treponemal test at the third trimester of gestation. Those women who were seropositive at the first visit, were retested by only RPR to detect possible reinfection. For quality control reasons, 10% of the sera negative samples and all positive sera were sent to the reference laboratory where the test was done again without awareness of the initial test results.
ASYS in the Control Clinics.
After being admitted to the antenatal clinic, a pregnant woman could visit any District General Hospital or the NCID for free initial testing with RPR and, where necessary, TPHA confirmation test. The test result is normally collected by the woman and brought to the ANC service. Women testing positive for syphilis are sent to a venereologist for appropriate case management and follow-up control, including contact tracing and counseling. Routine treatment is 3 weekly doses (2.4 million international unit) of benzathine penicillin and this is given free of charge.
Outcome Assessments and Case Reporting
The primary outcome of the study was (1) utilization of ASYS at the first antenatal visit and at the third trimester of gestation; (2) detected syphilis cases; and (3) number of congenital syphilis cases. Congenital syphilis was defined if any the following existed:8 (i) neonate manifesting classic signs of congenital syphilis, such as hepatosplenomegaly, rash, condyloma lata, and snuffles; (ii) neonate whose mothers have a syphilitic lesion at delivery; (iii) neonate born to mother with positive RPR and TPHA who are untreated or inadequately treated at delivery (if mothers received nonpenicillin therapy, or penicillin administered <30 days before the delivery), regardless of signs in the infant; (intravenously) neonate born to mother with positive RPR and TPHA whose serological response to penicillin was not documented or was equivocal (the definition of appropriate response for primary or secondary syphilis is a 4-fold decline in nontreponemal titres by 3 months and for early latent syphilis is a 4-fold decline in nontreponemal titers by 6 months); (v) neonate with RPR titers 4-fold or greater than the mother’s titer; and (vi) Treponemas seen in autopsy material by silver stain or dark field in stillborns born to mother with positive RPR and TPHA.
The secondary outcome set included1 adequate treatment (percentage of seropositive cases completing 3 doses of benzathine penicillin before delivery) and2 percentage of completely treated husbands/sexual partners of seropositive women.
In the study, syphilis cases are defined as the women attending for ANC who had positive rapid treponemal tests confirmed by RPR and TPHA in the intervention group or who had positive RPR confirmed by TPHA in the control group. At the second syphilis testing (at third trimester) and third syphilis testing (after delivery), only new syphilis cases were reported.
Most recently, 51 cases of congenital syphilis were diagnosed in 2006 in Ulaanbaatar.4 Without an intervention, the incidence of congenital syphilis was estimated at 6/1000 and the aim of the intervention was to reduce this number to below 1/1000. Using a significance level of 5%, a power of 80%, and assuming that the intraclass correlation is 0.001, as shown in a previous study,5 the required sample was calculated to be 3183 per group (2-sided test) or 455 subjects per clinic. After adjusting for an expected loss to follow-up rate of 20%, 550 subjects per clinic, a total of 3850 subjects were required and recruited in each group.
Data were computerized using EpiData (The EpiData Association Odense, Denmark) and analyzed using R software (The R foundation for Statistical Computing, Vienna, Austria). The analysis was undertaken as intention to treat. Differences in the proportions of syphilis testing at the first antenatal visit and at the third trimester of gestation, number of detected syphilis cases during the pregnancy, adequate treatment, treated partners, and congenital syphilis were compared. Since the main outcomes were nested within clinics, Rao and Scott’s χ2 test9 in “survey” package was used in the univariate analysis. For multivariate analysis, a multilevel analysis was carried out having individual women at the first (lower level) and the clinic at the second level (higher) using the “lme4” package. Women’s characteristics were independent, explanatory variables.
Recruitment started in August 2007 and all follow-up data were completed in August 2008. Figure 2 shows the flow of study clusters and eligible women throughout the trial. We collected follow-up data on 94.3% of enrollees at delivery in the intervention and 92.6% in the control. The proportion of overall missing did not vary between the groups (P = 0.1). The study groups were well balanced for distribution of baseline characteristics, such as mean age, education, and marital status; although significant differences were observed for gestational age at first ANC and multiple sexual partners (Table 1).
As shown in Figure 3, of 3850 pregnant recruited in each group, the proportion of syphilis testing at the first visit was over 99% in the intervention and 79.6% in the control group (P <0.001). In the third trimester, 94 (2.4%) and 27 (0.7%) women in the respective groups were lost to follow-up, all of whom had had a negative test at the first visit. Of the remaining 3683 and 3796 (not included previous seropositives at the first visit) who revisited at the third trimester, 99.7% and 62.1% had the second test (P <0.001) in the intervention and control groups, respectively. In the corresponding 2 periods, 73 (1.9%) and 20 (0.5%) cases of syphilis were detected in the intervention group and 27(0.9%) and 2 (0.08%) were in the control group (P <0.001 for first test and P = 0.01 for second test).
Eventually, 98.9% (92/93) of the overall detected cases in the intervention and 89.6% (26/29) in the control group were adequately treated (P = 0.02). The corresponding overall treatment rates of the sexual partners were 94.6% versus 55.2% (P <0.001). Only 1 congenital syphilis case out of 3632 deliveries in the intervention group versus 15 out of 3552 in the control (P = 0.002) were ascertained at the end, a reduction of 93.5% (95% CI, 66.0%–98.6%). The only case of congenital syphilis in the intervention group was born to a late ANC (38 weeks of gestation) comer, a woman who had been seropositive in the first visit, and had received only single injection of benzathine penicillin and did not return until delivery. A total of 13 women who tested positive by the rapid test assays during pregnancy, yet were negative at confirmation had unnecessarily received the first dose of penicillin at the antenatal clinics. Of total, 10 revealed that they had previously been treated for syphilis but the information was not obtained before RPR results were available.
Multilevel analysis was separately computed for main outcomes with the same set of independent variables that were significant with the univariate analysis. After adjustment, the primary and secondary outcomes were all significantly associated with the intervention except adequate treatment of positive cases (Table 2).
Our study provides evidence that one-stop service on ASYS implemented in antenatal clinics was more effective for the prevention of congenital syphilis. Almost all antenatal clients in the intervention clinics tested for syphilis at both time points of testing, resulting in more seropositive cases detected. A higher proportion of the syphilis infected women and their sexual partners were completely treated. Finally, the intervention resulted in a markedly lower number of congenital syphilis cases than the control group.
The need for a more effective alternative approach to ASYS is obvious since in many developing countries antenatal women remain unscreened for syphilis, thus remain untreated.3 To address the challenge to detect and treat syphilis infected antenatal women at their first ANC visit, an intervention on decentralized ASYS was developed and assessed in studies from some developing countries.10–15 The findings of the studies showed that the decentralized service of ASYS could detect and treat more maternal syphilis in pregnancy or could reduce congenital syphilis.10–13 One African study in 2003 documented a 75% decrease in rates of congenital syphilis after allowing for decentralized screening of maternal syphilis.12 Another South African study using decision-analytic cost-effectiveness modeling demonstrated that on-site rapid testing prevented over 80% of predicted cases of congenital syphilis.13
Our randomized study demonstrates that one-stop service with on-site rapid treponemal syphilis test with treatment and counseling is able to increase the coverage of screening and improve the rate of case detection in women and their partners as well as facilitate completion of treatment and dramatically reduce the incidence of congenital syphilis. There were 2 previous randomized controlled trials to evaluate the one-stop service on ASYS; however, the findings of these studies could not be compared directly to our findings because the on-site syphilis tests were different. In a study of Bique et al, on-site RPR was compared to centralized RPR and showed a significant improvement of perinatal mortality in the on-site RPR arm.14 In contrast, the comparison of on-site and centralized RPR did not show an improvement in either the proportion receiving adequate follow-up or the perinatal loss rate in a study of Myer et al.15
There are several reasons to explain how the one-stop service has played an important role in the reducing rates of congenital syphilis in the study. First, on-site testing is convenient to women, resulting in universal ASYS coverage at both time points of testing. Conventional centralized services for ASYS in Mongolia require women to have at least one extra visit in order to be fully tested for syphilis and to make return visits to get their test results. This inconvenience leads to delay or loss of contacts and subsequently leaves a number of syphilis cases undetected and untreated.6 A study in Mozambique reported that the similar intervention could increase the antenatal syphilis testing by over 90%.16
Second, once substantially increased syphilis screening coverage the intervention could detect a significant number of syphilis cases among antenatal clients. Besides demonstrating the success of detection rate in the intervention the study confirmed the previously reported comparatively high rates of syphilis among pregnant women in the country and the necessity of universal ASYS.4,6 The 20 incident cases identified would have been undetected and untreated if screening test at the third trimester had not been performed in the intervention clinics. Conversely, in control clinics coverage of syphilis testing at the third trimester was only 68.9% and could detect only 2 cases of active syphilis. These data support the necessity of performing syphilis testing also at the third trimester of gestation.17 Moreover, our data support the recommendation that syphilis testing should be performed on all women at the time of delivery if they were not tested for syphilis during pregnancy.17 Had it not been done, 15 seropositive women in the control group would have been missed during the delivery.
Third, the one-stop services for ASYS allowed prompt treatment of seropositive cases which resulted in a higher proportion of adequately treated women before delivery in the intervention than the control group. A similar success rate was reported by a Bolivian study in 2007. Using the on-site rapid syphilis testing the study detected more active syphilis cases among pregnant women and over 80% of those who tested positive received all 3 recommended doses of penicillin before delivery.10 The treatment success can be explained by the immediate access to the test results, for example, women receive their test results while they are still in the antenatal clinics. In fact, high rates of patients do not return for collecting test results in many countries, and this results in delay of early treatment or no treatment at all.18 One study found that only 24.5% of women with syphilis were treated when they were sent to the referral clinics for syphilis therapy.19
Fourth, notification and treatment of sexual partners at the one-stop service can be implemented. Similarly, the Bolivian project also reported that over three-quarters (498/577) of the male partners were identified at the time of testing and most of them (383/498) presented for treatment.10 The increase in percentage of partner notification and treatment could be explained by active counseling provided by ANC doctors. A recent Bolivian study findings suggested that screening for domestic violence and counseling about partner notification should be integrated into screening programs, since women who do not fear their partner’s reactions were more likely to notify them of their infection status.20 Notification to male partners is not only important to their own health, but is critical in preventing reinfection of women. Emphasis on notification of partners of pregnant women with syphilis has been associated with a 3-fold improvement in pregnancy outcome.21
Finally, one-stop service is effective in prevention of congenital syphilis. A 93.5% case reduction would mean significant relief of this health burden since several complications are well known to occur in congenital syphilis, such as miscarriages, stillbirths, and early neonatal deaths.2
Our study did not look at the reasons of low syphilis screening coverage in the control group. However, our previous study in 2006 showed that late ANC visit, lack of knowledge on the importance of ASYS and awareness of the infection, long travel to ASYS service, overcrowding at STI laboratories, and living far from service spot were related to unscreened in routine syphilis screening in Ulaanbaatar.6
With these good results, the current one-stop service is still not perfect. One seropositive woman received inadequate treatment due to late ANC resulting in congenital syphilis. Although the male partner treatment percentage was significantly higher in the intervention than control group, 5 sex partners remained untreated, thus the women could be reinfected. There were some limitations of this study. First, incomplete follow-up was still detected in our study but the figure was small (5.7%). Although they were initially seronegative, the final status of the women and their newborns were unknown. Second, since the all women testing positive by the rapid test received immediate treatment, some women had unnecessarily received first dose of penicillin because the rapid treponemal tests can not differentiate between women with current infection and those who have previously treated for the infection. However, this condition could be avoided mostly if they were interviewed on their previous history of diagnosis and treatment. Last, the syphilis tests were supplied to the intervention arm but not in the control arm. Since, it is known that logistical supply issues are at the core of why some programs fail and this may result in an advantage of intervention arm. However, there were no any shortages of routine RPR at the control arm during the study period.
In conclusion, one-stop services increased the detection rate of syphilis, treated more syphilis infected women and their partners, and effectively reduced congenital syphilis. Implementation of one-stop service can be considered to improve overall access to interventions to eliminate congenital syphilis as a public health problem.
1. Hawkes S, Miller S, Reichenbach L, et al. Antenatal syphilis control: People, programmes, policies and politics. Bull World Health Organ 2004; 82:417–423.
2. Schmid GP, Stoner BP, Hawkes S, et al. The need and plan for global elimination of congenital syphilis. Sex Transm Dis 2007; 34:S5–S9.
3. Hossain M, Broutet N, Hawkes S. The elimination of congenital syphilis: A comparison of national policies to the World Health Organization proposed action plan for the elimination of congenital syphilis. Sex Transm Dis 2007; 34:S22–S30.
4. Ministry of Health, National Center for Health Development. Health Indicators of Mongolia 2007. Ulaanbaatar, Mongolia: Ministry of Health, 2008.
5. 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.
6. Munkhuu B, Liabsuetrakul T, Chongsuvivatwong V, et al. Coverage of antenatal syphilis screening and predictors for not being screened in Ulaanbaatar, Mongolia. Sex Transm Dis 2006; 33:284–288.
7. World Health Organization. Managing Newborn Problems. Geneva, Switzerland: World Health Organization, 2003.
8. World Health Organization. Guidelines for Sexually Transmitted Infections Surveillance. Geneva, Switzerland: World Health Organization, 1999. WHO/CHS/HSI/99.2; WHO/CDS/CSR/EDC/99.3; UNAIDS/99.3E.
9. Rao JN, Scott AJ. A simple method for the analysis of clustered binary data. Biometrics 1992; 48:577–585.
10. Garcia SG, Tinajeros F, Revollo R, et al. Demonstrating public health at work: A demonstration project of congenital syphilis prevention efforts in Bolivia. Sex Transm Dis 2007; 34:S37–S41.
11. Bronzan R, Mwesigwa-Kayongo D, Narkunas D, et al. Onsite rapid antenatal syphilis screening with an Immunochromatographic strip improves case detection and treatment in rural South African clinics. Sex Transm Dis 2007; 34:S55–S60.
12. Fitzgerald DW, Behets F, Preval J, et al. Decreased congenital syphilis incidence in Haiti’s rural Artibonite region following decentralized prenatal screening. Am J Public Health 2003; 93:444–446.
13. Blandford JM, Gift TL, Vasaikar S, et al. Cost-effectiveness of on-site antenatal screening to prevent congenital syphilis in rural eastern Cape Province, Republic of South Africa. Sex Transm Dis 2007; 34:S61–S66.
14. Bique Osman N, Challis K, Folgosa E, et al. An intervention study to reduce adverse pregnancy outcomes as a result of syphilis in Mozambique. Sex Transm Infect 2000; 76:203–207.
15. Myer L, Wilkinson D, Lombard C, et al. Impact of on-site testing for maternal syphilis on treatment delays, treatment rates, and perinatal mortality in rural South Africa: A randomized controlled trial. Sex Transm Infect 2003; 79:208–213.
16. Gloyd S, Montoya P, Floriano F, et al. Scaling up antenatal syphilis screening in Mozambique. Sex Transm Dis 2007; 34:S31–S36.
17. World Health Organization. Standards for Maternal and Neonatal Care. Geneva, Switzerland: World Health Organization, 2006.
18. Rotchford K, Lombard C, Zuma K, et al. Impact on perinatal mortality of missed opportunities to treat maternal syphilis in rural South Africa: Baseline results from a clinic randomized controlled trial. Trop Med Int Health 2000; 5:800–804.
19. Swingler GH, Van Coeverden de Groot HA. The antenatal prevention of congenital syphilis in a peri-urban settlement. S Afr Med J 1993; 83:34–35.
20. Diaz-Olavarrieta C, Garcia SG, Feldman BS, et al. Maternal syphilis and domestic violence in Bolivia: A gender-based analysis of implications for partner notification and universal screening. Sex Transm Dis 2007; 34:S42–S46.
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21. Gichangi P, Fonck K, Sekande-Kigondu C, et al. Partner notification of pregnant women infected with syphilis in Nairobi, Kenya. Int J STD AIDS 2000; 11:257–261.