Missed opportunities for congenital syphilis and HIV perinatal transmission prevention
Oportunidades perdidas na prevenção da sífilis congênita e da transmissão vertical do HIV
Oportunidades perdidas en la prevención de la sífilis congénita y de la transmisión vertical del HIV
Celeste Souza RodriguesI; Mark Drew Crosland GuimarãesII; Cibele Comini CésarIII
IGerência de Vigilância em Saúde e Informação. Secretaria Municipal de Saúde de Belo Horizonte. Belo Horizonte, MG, Brasil
IIDepartamento de Medicina Preventiva e Social. Faculdade de Medicina. Universidade Federal de Minas Gerais (UFMG). Belo Horizonte, MG, Brasil
IIIDepartamento de Estatística. Instituto de Ciências Exatas. UFMG. Belo Horizonte, MG, Brasil
OBJECTIVE: To estimate the prevalence of missed opportunities for congenital syphilis and HIV prevention in pregnant women who had access to prenatal care and to assess factors associated to non-testing of these infections.
METHODS: Cross-sectional study comprising a randomly selected sample of 2,145 puerperal women who were admitted in maternity hospitals for delivery or curettage and had attended at least one prenatal care visit, in Brazil between 1999 and 2000. No syphilis and/or anti-HIV testing during pregnancy was a marker for missed prevention opportunity. Women who were not tested for either or both were compared to those who had at least one syphilis and one anti-HIV testing performed during pregnancy (reference category). The prevalence of missed prevention opportunity was estimated for each category with 95% confidence intervals. Factors independently associated with missed prevention opportunity were assessed through multinomial logistic regression.
RESULTS: The prevalence of missed prevention opportunity for syphilis or anti-HIV was 41.2% and 56.0%, respectively. The multivariate analysis showed that race/skin color (non-white), schooling (<8 years), marital status (single), income (<3 monthly minimum wages), having sex during pregnancy, history of syphilis prior to the current pregnancy, number of prenatal care visits (<6), and last prenatal visit before the third trimester of gestation were associated with an increased risk of missed prevention opportunity. A negative association with missed prevention opportunity was found between marital status (single), prenatal care site (hospital) and first prenatal visit in the third trimester of gestation.
CONCLUSIONS: High rates of non-tested women indicate failures in preventive and control actions for HIV infection and congenital syphilis. Pregnant women have been discontinuing prenatal care at an early stage and are failing to undergo prenatal screening for HIV and syphilis.
Descriptors: Syphilis, Congenital, prevention & control. HIV Infections, prevention & control. Disease Transmission, Vertical, prevention & control. Prenatal Care. Cross-Sectional Studies. Missed Prevention Opportunity.
OBJETIVO: Estimar a prevalência de oportunidade perdida de prevenção a sífilis e HIV entre gestantes que tiveram acesso ao pré-natal e fatores associados a não-testagem para esses agravos.
MÉTODOS: Estudo transversal com amostra aleatória de 2.145 puérperas do Brasil, 1999 e 2000 admitidas em maternidades para parto ou curetagem e que haviam realizado pelo menos uma consulta de pré-natal. A não-realização de exame de teste para sífilis e/ou anti-HIV durante a gravidez foi usada como marcador para oportunidade perdida de prevenção. Mulheres que realizaram apenas exame de sífilis ou apenas o anti-HIV, ou não realizaram nenhum, foram comparadas àquelas que realizaram os dois (categoria de referência). A prevalência de oportunidade perdida de prevenção foi estimada para cada categoria, com intervalo de confiança de 95%. Os fatores associados com oportunidade perdida de prevenção foram analisados por meio de regressão logística multinomial.
RESULTADOS: A prevalência de oportunidade perdida de prevenção para a realização do teste de sífilis ou anti-HIV foi de 41,2% e 56,0%, respectivamente. A análise multivariada indicou que raça/cor (não branca), escolaridade (< 8 anos de estudo), estado civil (solteira), renda <3 salários mínimos, relação sexual durante a gravidez, relato de não ter tido sífilis anterior à gravidez atual, realização de seis ou mais consultas de pré-natal e a realização da última visita antes do terceiro trimestre de gravidez estavam associados a maior risco de ter oportunidade perdida de prevenção. Observou-se uma associação negativa entre estado civil (solteira), local de realização do pré-natal (hospital) e a realização da primeira consulta de pré-natal no terceiro trimestre com oportunidade perdida de prevenção.
CONCLUSÕES: Altas percentagens de gestantes não testadas apontam falhas na prevenção e controle da infecção pelo HIV e da sífilis congênita pelos serviços de saúde. As gestantes continuam interrompendo o cuidado pré-natal precocemente e não conseguindo realizar os procedimentos de triagem para HIV e sífilis.
Descritores: Sífilis Congênita, prevenção e controle. Infecções por HIV, prevenção e controle. Transmissão Vertical de Doença, prevenção e controle. Cuidado Pré-Natal. Estudos Transversais. Oportunidade Perdida de Prevenção.
OBJETIVO: Estimar la prevalencia de oportunidad de pérdida de prevención de la sífilis y el HIV entre gestantes que tuvieron acceso al pre-natal y factores asociados con la no evaluación de estos agravios.
MÉTODOS: Se realizó estudio transversal con muestra aleatoria de 2.145 puérperas de Brasil, 1999 y 2000 admitidas en maternidades para parto o curetaje y que habían realizado al menos una consulta de pre-natal. La no realización del examen de prueba para sífilis y/o anti-HIV durante el embarazo fue usada como marcador para oportunidad de pérdida de prevención. Las mujeres que realizaron sólo examen de sífilis o sólo examen de anti-HIV, o que no realizaron ninguno, fueron comparadas con las que realizaron los dos (categoría de referencia). La prevalencia de oportunidad de pérdida de prevención fue estimada para cada categoría, con intervalo de confianza de 95%. Los factores asociados con la oportunidad de pérdida de prevención fueron analizados por medio de regresión logística multinomial.
RESULTADOS: La prevalencia de oportunidad de pérdida de prevención para la realización de la prueba de sífilis o anti-HIV fue de 41,2% e 56,0%, respectivamente. El análisis multivariado indicó que raza/color (no blanca), escolaridad (< 8 años de estudio), estado civil (soltera), renta < 3 salarios mínimos, relación sexual durante el embarazo, no haber tenido sífilis anterior al embarazo actual, realización de seis o mas consultas de pre-natal y la realización de la última visita antes del tercer trimestre de embarazo, estaban asociados con mayor riesgo de tener oportunidad de pérdida de prevención. Se observó una asociación negativa entre estado civil (soltera), lugar de realización de pre-natal (hospital) y la realización de la primera consulta pre-natal en el tercer trimestre con oportunidad de pérdida de prevención.
CONCLUSIONES: Altos porcentajes de gestantes no evaluadas señalan fallas en la prevención y control de la infección por HIV y de la sífilis congénita en los servicios de salud. Las gestantes continúan interrumpiendo el cuidado pre-natal precozmente y no logran realizar los procedimientos de selección para HIV y sífilis.
Descriptores: Sífilis Congénita, prevención y control. Infecciones por HIV, prevención y control. Transmisión Vertical de Enfermedad, prevención y control. Atención Prenatal. Estudios Transversales. Oportunidad Pérdida de Prevención.
Infectious diseases transmitted from mother to child during pregnancy and during labor are still an important and preventable cause of morbimortality among newborns. Maternal syphilis may result in fetal and neonatal death, fetal hydropsy, intrauterine growth retardation, as well as preterm infants.5,9 It is estimated that 40% of pregnancies in women with non-treated primary or secondary syphilis evolve into fetal loss or neonatal death.4 In recent years, an increase in syphilis prevalence in developing and industrialized countries has been seen, especially primary and secondary syphilis in childbearing women, with a consequent increase in the rate of neonatal syphilis.2,16
In 1993, the Brazilian Ministry of Health developed a plan for the elimination of congenital syphilis in accordance with proposals formulated by the World Health Organization and the Pan American Health Organization. The goal was to achieve an incidence rate equal to or lower than 1 case/1,000 newborns.a Despite easy and inexpensive diagnosis and treatment, syphilis prevalence was still between 3.5 and 4.0% in 1999 according to the Brazilian Ministry of Health.a In addition, a national multicenter study carried out in 2000 among puerperal women admitted for labor or curettage in public maternities showed a syphilis seroprevalence of 1.7% and a strong association with not being tested for HIV and syphilis.10
HIV vertical transmission is still of public health concern, although it has decreased in several countries. Current recommendations for the prevention of vertical transmission include HIV testing during pregnancy and labor, and for those HIV-positive, the use of combined antiretroviral drugs during pregnancy and the use of zidovudine during labor and by the newborn.1,b Despite universal availability of HIV testing, including rapid tests, and prophylactic medication in Brazil, children are still getting infected. Data from the Brazilian National STD/AIDS Program show that HIV vertical transmission accounted for 83.6% of AIDS cases among children under 13 years of age between 1983 and 2004. In 2004, the number of reported new cases was still of concern (n=450).c In addition, a surveillance study based on sentinel maternities with parturient women conducted in the five regions of Brazil showed an HIV infection prevalence of 0.6%.d
It is well known that an elevated proportion of congenital syphilis cases and HIV perinatal transmission is found among women who had low prenatal care attendance, which suggests that full opportunities for maternal infection diagnosis and treatment may be potentially lost.11 A study by Warner et al18 (2001) shows that each syphilis case in pregnant women should be considered as a potential case of HIV infection and, at the same time, as a potential opportunity for prevention through counseling. Peters et al7 (2003) concluded that prenatal care and anti-HIV testing prior to delivery are the greatest opportunities for prevention of HIV vertical transmission. The actions developed for the prevention of both, HIV vertical transmission and congenital syphilis, are thus strongly similar and related to adequate prenatal and delivery assistance.
In 2000 the Brazilian Ministry of Health launched a large national program which aimed at guaranteeing improved quality of care to women and children during pregnancy, delivery and puerperium. It included allocating financial resources to towns and maternity wards and specific recommendations for HIV and syphilis prevention such as HIV and syphilis testing and treatment.13
Despite Brazilian government investment in this area and the availability of prevention and treatment actions, there is limited knowledge to what extent women who have access to prenatal care are indeed receiving adequate attention, including counseling, the recommended number of visits, and specifically the opportunity for HIV and syphilis testing.
In this perspective, the present study aimed at determining the prevalence of pregnant women who missed prevention opportunities during prenatal care and to assess factors associated to non-testing to these infections.
This cross-sectional study is part of a larger national multicenter study, which was developed in 1999 and 2000e with the support of the National STD/AIDS Program and the Brazilian Ministry of Health Maternal and Child Health Program. A random probability sample of pregnant women was selected proportionally to the number of deliveries estimated per state and by the number of maternities in each one of 24 states. The detailed methodology has been previously published.10
Briefly, 3,233 pregnant women admitted for labor or curettage were randomly selected upon admission to the maternity ward according to a pre-defined schedule. An interview and blood collection for syphilis diagnosis were carried out after delivery or curettage. Sociodemographic, behavioral and obstetric data were obtained by structured interview. Data from current hospitalization and prenatal care were also obtained from medical charts to complete the database. For the analysis, only those women who had had at least one prenatal care visit were included, yielding a final sample size of 2,145 pregnant women. Venereal Disease Research Laboratories (VDRL) test and anti-HIV testing during the current pregnancy was used as a marker for the assessment of missed prevention opportunities. Women tested for HIV only, syphilis only (VDRL) or neither of them was compared to those tested for both (reference category).
The prevalence of missed prevention opportunities for VDRL and anti-HIV testing was defined as:
- VDRL: the number of pregnant women who had not been VDRL tested during pregnancy divided by the total of pregnant women in the sample;
- anti-HIV: the number of pregnant women who had not been anti-HIV tested during prenatal care divided by the total of pregnant women in the sample.
A descriptive analysis was performed and differences in proportions were assessed by chi-square test. Significance level was set at 0.05. The magnitude and the independent effect between selected variables and missed prevention opportunities were estimated through odds ratios (OR) with 95% confidence interval obtained from multinomial logistic regression. This method allows for OR estimation considering a dependent variable with more than two categories. Each category was compared to the reference category in a single process3 as follows: 1. pregnant women who reported anti-HIV testing only; 2. those who reported VDRL testing only; and 3. those who reported not being tested by either test. Each category was compared to those women who reported being tested by both tests during prenatal care. The criterion for initiating multivariate modeling was the presence of association between variables and the dependent variable at p-value <0.20 in the univariate analysis. Only those variables showing statistical significance of less than 0.05 remained in the final model.
Informed consent was obtained from all women participating in the study and the research project was approved by Research Ethics Committee of Universidade Federal de Minas Gerais.
Both tests were performed in 32.1% (n=688) of 2,145 women, 26.9% (n=576) were tested for VDRL only and 12.0% (n=258) for anti-HIV only; 29.0% (n=623) had not been tested during the current prenatal care. The overall prevalence of missed prevention opportunities for each test was 41.2% (95% CI: 31.4%;50.6%) for VDRL and 56.0% (95% CI: 46.3%;65.7%) for anti-HIV.
Sociodemographic variables showed high proportions of non-white (64%), with < 8 years of schooling (72%), single (59%), homemaker (60%), with monthly income <3 monthly minimum wages (45%) and age < 23 years old (54%). Sexual initiation was at an early age (mean=17.1 years old), while 41% had their first pregnancy at age <18 years and 69% were > 18 years old at first delivery, 91% had at least one sexual intercourse during pregnancy and only 2% reported previous syphilis infection. Most women (58%) attended prenatal care at a health care center. Yet 20% had less than four prenatal visits and 37% had a late prenatal care start, i.e., after the first trimester of gestation. Among women who had started prenatal care after the first trimester, 38% had one to three prenatal visits. For 9% of the women, the last prenatal visit occurred before the third trimester of pregnancy, 73% of which had one to three visits.
Table 1 shows the distribution of subjects according to the tests performed and sociodemographic, behavioral and prenatal care variables, which showed association at p<0.20. Missing one or both tests during the current pregnancy was statistically associated (p<0.05) with race (non-white), lower schooling (<8 years), marital status (single), occupation (homemaker), lower monthly family income (<3 monthly minimum wages) and younger age. Similarly, younger women at first delivery and those with less than seven prenatal visits missed one or both tests. It is of concern that women tested for VDRL (15%) or anti-HIV only (23%) and women who had not been tested for either test (33%) had less than four prenatal visits. In addition, both late prenatal care start and early discontinuation (last prenatal visit before third trimester) of prenatal care were higher among women who had not been tested by either test (42% and 16%, respectively).
The multivariate analysis (Table 2) showed that not being tested for VDRL and anti-HIV was positively and significantly associated with race (non-white), lower schooling (<8 years) and monthly family income, no previous syphilis infection, fewer number of prenatal visits and early discontinuation of care. A dose-response trend was seen for family income, number of prenatal visits and time of the last visit. Not being tested for VDRL and anti-HIV was also negatively associated with receiving prenatal care at the hospital where delivery occurred. Independent positive and significant associations with not being anti-HIV tested were found for lower schooling (<8 years), being single, having sex during pregnancy and having the last prenatal visit in the second trimester. Testing for VDRL was positively and significantly associated with race (non-white), monthly family income and number of prenatal visits, and was negatively associated with marital status (single) and time of the first prenatal visit (third trimester). The p-values of Pearson's chi-square test for all three individual logistic regressions were not significant, indicating good overall fit of the model3
The proportion of pregnant women tested for VDRL and anti-HIV during their prenatal care visits was low, with a consequent high prevalence of missed prevention opportunities (41.2% and 56.0%, respectively). This finding corroborates another study conducted by the Brazilian Ministry of Health which also showed a low rate (52.0%) of parturients being tested for HIV and learning of their results during the same prenatal care.15 Schrag et al12 (2003) have found a high proportion of women being tested for syphilis but a rather smaller proportion of HIV testing during prenatal care in the United States from 1998 to 1999. Warner et al18 (2001) have also found 60.0% of missed prevention opportunities for diagnosis and treatment of syphilis during pregnancy in Atlanta (US) from 1990 to 1993. The high prevalence of missed prevention opportunities found in the present study indicates a gap in the adoption of prevention measures and proper intervention by the health services. The failure to diagnose and treat syphilis early in the pregnancy may lead to fetal loss, premature delivery and congenital syphilis, many times asymptomatic and non-diagnosed.5,9 Similarly, early HIV infection diagnosis with the use of antiretroviral drugs during pregnancy and labor and the use of zidovudine by the newborn may reduce the rates of vertical transmission to less than 2%.1
Sociodemographic variables associated to not being tested or being tested for VDRL or anti-HIV only indicate greater social vulnerability of the population studied: single women with low schooling and income. These factors may be markers of poor access to health services and testing. Such findings are consonant with other studies carried out in Brazil and in the United States, which also show low schooling as a predictor of congenital syphilis and HIV perinatal infection.15,17
The proportion of pregnant women who had a late start of their prenatal care (37%) and the proportion who had less than four prenatal visits (20%) should be of concern. Piaggio et al8 (1998), in a multicenter study from 1994 to 1995, have found large differences of percentage across sites of women initiating prenatal care in the first trimester, from 18% in Argentina up to almost 80% in Cuba. The Demographic and Health Surveys (DHS) conducted in 1999 and supported by the United States Agency for International Development (USAID) have found that at least 50% of women reported four or more prenatal care visits in 33 of 45 countries.19
The increased risk found between not being tested and early discontinuation of prenatal care may be explained by the smaller number of visits and the lack of immediate test request in the first visit. The Brazilian Ministry of Health currently recommends that VDRL and anti-HIV testing should be carried out in the first prenatal visit, regardless of when it begins.11 These findings show the importance of better organization of health care services. In addition, the importance of expanding access, stimulating early access and the establishment of a satisfactory bond between pregnant women and prenatal care providers have been shown to positively impact on the reduction of congenital syphilis and HIV vertical transmission.12,17
The negative association found between receiving prenatal care at the hospital where delivery occurred and not being tested may indicate that prenatal screening is facilitated in settings where laboratory infrastructure is better and more easily accessible. In many primary care settings serological tests are not performed locally, but rather in distant and centralized facilities, causing patients to miss appointments or fail to return for their test results, which can, in turn, result in treatment being delayed or missed.6
The increased risk found between no previous history of syphilis and not being tested for VDRL during the current pregnancy may indicate a biased perception of less vulnerability by health professionals, and consequently, a smaller number of test requests during prenatal care. This is corroborated by a study carried out in Bolivia which indicated that prenatal care physicians usually did not request syphilis testing when they believed pregnant women did not have any risk behavior for sexually transmitted infections.14
The study results indicate serious failures in prevention actions for HIV infection and congenital syphilis control. Pregnant women are still having a late start and early discontinuation of their prenatal care, thus reducing the likelihood of taking appropriate diagnostic and treatment actions. Investments made and the efforts developed at the three governmental levels for the reduction of HIV vertical transmission and syphilis control, especially congenital syphilis, may not have been as effective. Considering that all pregnant women in the present study had access to at least one prenatal care visit, improving the organization of these services are necessary in order to increase effectiveness of syphilis and HIV control programs. Reach-out programs at the community level should be promoted, in particular among underprivileged populations. Early recruitment and the establishment of adequate bonds with prenatal care providers should also be emphasized. It is also necessary to develop strategies for health professionals in order to assure the minimum number of tests required by the Brazilian Ministry of Health. In addition, timely and adequate treatment for those tested positive for syphilis and prophylaxis for those tested positive for HIV and their exposed children should be of extreme concern and priority. Such actions, which are known to have a positive impact on the reduction of congenital syphilis and HIV infection prevalence, should be immediately sought, implemented and evaluated at all levels of care, from primary - where most women seek prenatal care - to tertiary - where women are referred to for delivery and curettage.
1. Centers for Disease Control and Prevention. Revised recommendations for HIV screening of pregnant women. MMWR Morb Mortal Wkly Rep. 2001;50(RR-19):63-86.
2. Grimberg G, Ravelli MR, Etcheves PDC, Orfus G, Pizzimenti MC. Sifilis y embarazo - control prenatal, seroprevalencia y falsos biológicos positivos. Medicina (B Aires). 2000;60(3):343-7.
3. Hosmer DW, Lemeshow S. Applied logistic regression. New York: John Wiley & Sons; 1989.
4. Lumbiganon P, Piaggio G, Villar J, Pinol A, Bakketeig L, Bergsjo P, et al. The epidemiology of syphilis in pregnancy. Int J STD AIDS. 2002;13(7):486-94. DOI: 10.1258/09564620260079653
5. Mobley JA, McKeown RE, Jackson KL, Sy F, Pahram JS, Brenner ER. Risk factors for congenital syphilis in infants of women with syphilis in South Carolina. Am J Public Health. 1998;88(4):597-602.
6. Peeling R, Ye H. Diagnostic tools for preventing and managing maternal and congenital syphilis: an overview. Bull World Health Organ. 2004;82(6):439-46.
7. Peters V, Liu KL, Dominguez K, Frederick T, Melville S, Hsu HW, et al. Missed opportunities for perinatal HIV prevention among HIV-exposed infants born 1996-2000, pediatric spectrum of HIV disease cohort. Pediatrics. 2003;111(5 Part 2):1186-91.
8. Piaggio G, Ba'aqeel H, Bergsjø P, Carroli G, Farnot U, Lumbiganon P, et al. The practice of antenatal care: comparing four study sites in different parts of the world participating in the WHO Antenatal Care Randomised Controlled Trial. Paediatr Perinat Epidemiol. 1998;12 (Suppl 2):116-41. DOI: 10.1046/j.1365-3016.12.s2.1.x
9. Ray JG. Lues-lues: maternal and fetal considerations of syphilis. Obstet Gynecol Surv. 1995;50(12):845-50. DOI: 10.1097/00006254-199512000-00003
10. Rodrigues CS, Guimarães MDC; Congenital Syphilis National Group of Study. Syphilis positivity in puerperal women: still a challenge in Brazil. Rev Panam Salud Publica. 2004:16(3):168-75. DOI: 10.1590/S1020-49892004000900003
11. Saloojee H, Velaphi S, Goga Y, Afadapa N, Steen R, Lincetto O. The prevention and management of congenital syphilis: an overview and recommendations. Bull World Health Organ. 2004;82(6):424-30.
12. Schrag SJ, Arnold KE, Mohle-Boetani JC, Lynfield R, Zell ER, Stefonek K, et al. Prenatal screening for infectious diseases and opportunities for prevention. Obstet Gynecol. 2003;102(4):753-60. DOI: 10.1016/S0029-7844(03)00671-9
13. Serruya SJ, Lago TG, Cecatti JG. Avaliação preliminar do programa de humanização no pré-natal e nascimento no Brasil. Rev Bras Ginecol Obstetr. 2004; 26(7):517-25.
14. Southwick KL, Blanco S, Santander A, Estenssoro M, Torrico F, Seoane G, et al. Maternal and congenital syphilis in Bolívia, 1996: prevalence and risk factores. Bull World Health Organ. 2001;79(1):33-42.
15. Souza Júnior PRB, Szwarcwald CL, Barbosa Júnior A, Carvalho MF, Castilho EA. Infecção pelo HIV durante a gestação: estudo-Sentinela Parturiente, Brasil, 2002. Rev Saude Publica. 2004;38(6):764-72. DOI: 10.1590/S0034-89102004000600003
16. Temmerman M, Gichangi P, Fonck K, Apers L, Claeys P, Van Renterghem L, et al. Effect of a syphilis control programme on pregnancy outcome in Nairobi, Kenya. Sex Transm Infect. 2000;76(2):117-21. DOI: 10.1136/sti.76.2.117
17. Thompson BL, Matuszak D, Dwyer DM, Nakashima A, Pearce H, Israel E. Congenital syphilis in Maryland, 1989-1991: The effect of changing the case definition and opportunities for prevention. Sex Transm Dis. 1995;22(6):364-9. DOI: 10.1097/00007435-199511000-00008
18. Warner L, Rochat RW, Fichtner RR, Stoll BJ, Nathan L, Toomey KE. Missed opportunities for congenital syphilis prevention in an Urban Southeastern Hospital. Sex Transm Dis. 2001;28(2):92-8. DOI: 10.1097/00007435-200102000-00006
19. World Health Organization. Antenatal care in developing countries: Promises, achievements and missed opportunities: an analysis of trends, levels and differentials, 1990-2001. Geneva; 2003.
Celeste de Souza Rodrigues
Av. Afonso Pena 2336, 4º andar
Gerência de Vigilância em Saúde e Informação
30130-007 Belo Horizonte, MG, Brasil
Supported by Programa Nacional de Doenças Sexualmente Transmissíveis/AIDS e Coordenação Materno-Infantil do Ministério da Saúde, Brasília, Brasil (Projeto 3659-BR CN-DST/Aids).
Article based on the doctorate thesis of CS Rodrigues, presented to Graduate Program in Public Health at Faculdade de Medicina of UFMG, in 2005.
a Ministério da Saúde Projeto de eliminação da sífilis congênita. [citado 2005 mar 15]. Disponível em: http://www.aids.gov.br/assistencia/documentos referenciais
b Ministério da Saúde. Coordenação Nacional DST/AIDS. Projeto Nascer-Maternidades. Brasília; 2002.
c Ministério da Saúde. Programa Nacional de DST/AIDS. Boletim Epidemiológico AIDST. 2004;1(1).
d Ministério da Saúde. Programa Nacional de DST/AIDS. Soroprevalência por grupo e corte. Estudo Sentinela Brasil, 1997-2000 [citado 2005 mar 15]. Disponível em: http://www.aids.gov.br/final/dados/resultados
e Guimarães MDC. Estudo de soroprevalência de sífilis em puérperas: um estudo multicêntrico nacional. Ministério da Saúde; 2000. (Relatório técnico final)