Advertisement

Prevalence of syphilis, human immunodeficiency virus, hepatitis B virus, and human T-lymphotropic virus infections and coinfections during prenatal screening in an urban Northeastern Brazilian population

Open AccessPublished:August 06, 2015DOI:https://doi.org/10.1016/j.ijid.2015.07.022

      Highlights

      • Syphilis was most prevalent (2.8%) among pregnant women in Maceió
      • HIV, HTLV, & HBV infections had 0.3%, 0.2%, & 0.4% prevalence, respectively
      • HIV-infected pregnant women had 5.71-fold greater risk of T. pallidum coinfection
      • Syphilis and HIV seroconversion occurred in 0.5% & 0.06% pregnant women, respectively
      • Among women carrying HTLV, 4.2% also had HBV infection

      Summary

      Objectives

      To evaluate prevalences of Treponema pallidum, human immunodeficiency virus (HIV), human T-lymphotropic virus (HTLV), and hepatitis B virus (HBV) infections and coinfections during prenatal screening in an urban Northeastern Brazilian population through a large dataset.

      Methods

      Secondary data were obtained from the Maceió (Alagoas, Brazil) municipal prenatal screening program from June 2007 to May 2012. Dried blood serum tests from 54,813 pregnant women were examined to determine prevalences of T. pallidum, HIV, HTLV, and HBV infections and coinfections, and the seroconversion rates for syphilis and HIV infection. Socio-demographic variables associated with syphilis and HIV infection were identified.

      Results

      The prevalences of syphilis, HIV, HTLV, and HBV infections were 2.8%, 0.3%, 0.2%, and 0.4%, respectively. Pregnant women infected with T. pallidum had a 4.62-fold greater risk of HIV coinfection, and pregnant women infected with HIV had a 5.71-fold greater risk of T. pallidum coinfection. Seroconversion for syphilis and HIV during pregnancy occurred in 0.5% and 0.06% of women, respectively. Among the women carrying HTLV, 4.2% also had an HBV infection.

      Conclusions

      Syphilis was twice as prevalent among pregnant women in Maceió, compared to the national average, and coinfections with syphilis/HIV and HTLV/HBV were significantly associated among these pregnant women.

      Keywords

      1. Introduction

      Early diagnosis and proper management during pregnancy and after childbirth can reduce mother-to-child transmission of syphilis, the human immunodeficiency virus (HIV), the human T-cell lymphotropic virus (HTLV), and the hepatitis B virus (HBV).
      • Mussi-Pinhata M.M.
      • Quintana S.M.
      Screening for infectious diseases during pregnancy: which test and which situation.
      • Ando Y.
      • Matsumoto Y.
      • Nakano S.
      • Saito K.
      • Kakimoto K.
      • Tanigawa T.
      • et al.
      Long-term follow up study of vertical HTLV-I infection in children breast-fed by seropositive mothers.
      Approximately 1.5 million pregnant women worldwide are infected with Treponema pallidum annually; if untreated, 50% of them will experience adverse events, including stillbirth, prematurity, and deaths.
      • Newman L.
      • Kamb M.
      • Hawkes S.
      • Gomez G.
      • Say L.
      • Seuc A.
      • et al.
      Global estimates of syphilis in pregnancy and associated adverse outcomes: analysis of multinational antenatal surveillance data.
      Furthermore, in 2006, the World Health Organization reported that 2.3% of pregnant women tested positive for HIV infections in low-and middle-income countries.

      World Health Organization. Taking stock: HIV in children - the state of affairs. Geneva: World Health Organization 2006. Available at: http://apps.who.int/iris/handle/10665/69760. Accessed on March 13, 2015.

      Thus, the elimination of mother-to-child transmission of HIV and syphilis have been incorporated into the World Health Organization's Millennium Development Goals 4, 5, and 6.

      World Health Organization. The global elimination of congenital syphilis: rationale and strategy for action. Geneva: World Health Organization 2008. Available at:. http://www.who.int/reproductivehealth/publications/rtis/9789241595858/en/. Accessed on March 13, 2015.

      To achieve these goals, prenatal screening is critical to preventing mother-to-child transmission via interventions during pregnancy, childbirth, and the post-partum period.

      World Health Organization. Taking stock: HIV in children - the state of affairs. Geneva: World Health Organization 2006. Available at: http://apps.who.int/iris/handle/10665/69760. Accessed on March 13, 2015.

      World Health Organization. The global elimination of congenital syphilis: rationale and strategy for action. Geneva: World Health Organization 2008. Available at:. http://www.who.int/reproductivehealth/publications/rtis/9789241595858/en/. Accessed on March 13, 2015.

      An estimated 240 million individuals worldwide are infected with HBV, with a male:female distribution ratio of approximately 1.5:1.

      World Health Organization. Fact sheet No. 204: Hepatitis b. Available at: http://www.who.int/mediacentre/factsheets/fs204/en/. Accessed on March 13, 2015.

      Based on these statistics, we can assume that there are approximately 90 million female carriers of HBV, many of whom are of childbearing age. Their babies can also become chronic carriers of the HBV s-antigen (HBsAg) if they do not receive preventative treatment.
      • Lee C.
      • Gong Y.
      • Brok J.
      • Boxall E.H.
      • Gluud C.
      Effect of hepatitis B immunisation in newborn infants of mothers positive for hepatitis B surface antigen: systematic review and meta-analysis.
      In addition, these individuals have a greater risk of developing hepatocellular carcinoma.
      • Peeters M.
      • D⿿Arc M.
      • Delaporte E.
      The origin and diversity of human retroviruses.
      Therefore, the identification of pregnant women who are carriers of HBsAg is an important strategy for preventing mother-to-child transmission.
      • Lee C.
      • Gong Y.
      • Brok J.
      • Boxall E.H.
      • Gluud C.
      Effect of hepatitis B immunisation in newborn infants of mothers positive for hepatitis B surface antigen: systematic review and meta-analysis.
      An estimated 15⿿20 million people worldwide are infected with HTLV-1 or HTLV-2,
      • Peeters M.
      • D⿿Arc M.
      • Delaporte E.
      The origin and diversity of human retroviruses.
      and mother-to-child transmission typically occurs during breastfeeding.
      • Peeters M.
      • D⿿Arc M.
      • Delaporte E.
      The origin and diversity of human retroviruses.
      There are no national data regarding the number of pregnant women who are carriers of HTLV in Brazil, and the Ministry of Health does not currently recommend prenatal screening for HTLV.
      • Monteiro D.L.M.
      • Taquette S.R.
      • Barmpas D.B.S.
      • Rodrigues N.C.
      • Teixeira S.A.
      • Villela L.H.
      • et al.
      Prevalence of HTLV-1/2 in pregnant women living in the metropolitan area of Rio de Janeiro.
      However, because they have common transmission routes, increases in the prevalences of syphilis and infection with HIV, HTLV, and HBV can overlap. In addition, their magnitude and vulnerability to preventive methods during pregnancy makes them global public health concerns (albeit to differing degrees).
      • Griffiths E.C.
      • Pedersen A.B.
      • Fenton A.
      • Petchey O.L.
      The nature and consequences of coinfection in humans.
      Therefore, we conducted this large study to determine the prevalences of syphilis and HIV, HTLV, and HBV infections and coinfections during prenatal screening among pregnant women in an urban Northeastern Brazilian population. In addition, we evaluated the seroconversion rates of syphilis and HIV infection, and evaluated the association between various socio-demographic variables and syphilis or HIV infection.

      2. Materials and methods

      This study used a descriptive, observational, cross-sectional design to evaluate data from the Maceió antenatal infectious diseases screening registry. The Maceió Municipal Health Office authorized the use of these data (July 2012) and the ethics committee of the Instituto de Medicina Integral Prof. Fernando Figueira approved the study design (CAAE: 06733812.2.0000.5201; Plataforma Brasil).

      2.1 Population, prenatal testing, data collection, and processing

      Maceió, the capital of the State of Alagoas, is located in northeastern Brazil and had 76,862 births between June 2007 and May 2012.

      Brasil. Ministério da Saúde. DATASUS. Informações de Saúde. Available at: http://tabnet.datasus.gov.br/cgi/tabcgi.exe?sinasc/cnv/nval.def. Accessed on July 25, 2014.

      Based on an average miscarriage rate of 16% in northeastern Brazil,

      Brasil. Ministério da Saúde. Departamento de Ações Programáticas Estratégicas. Manual dos Comitês de Mortalidade Materna. Available at: http://bvsms.saude.gov.br/bvs/publicacoes/comites_mortalidade_materna_3ed.pdf. Accessed on July 25, 2014.

      it was estimated that 89,159 pregnancies occurred in Maceió during this period. Approximately 74.7% of the population are public healthcare users,

      Agência Nacional de Saúde Suplementar. Dados e Indicadores do Setor. Available at: http://www.ans.gov.br/perfil-do-setor/dados-e-indicadores-do-setor. Accessed on April 24, 2015.

      which indicates that more than 66,600 of the pregnant mothers received public healthcare.
      Between June 2007 and May 2012, 54,813 pregnant women who sought treatment at the Maceió Universal Healthcare System (Sistema ÿnico de Saúde, SUS) were screened for T. pallidum, HIV, HTLV, and HBV infections during their first prenatal care visit. The Municipal Health Office antenatal disease screening program screened 61.4% of all pregnancies in the municipality, and 82.3% of pregnancies that received prenatal care via the public healthcare system during this period. The evaluation form for the included women recorded their date of birth, self-reported ethnicity, number of abortions, gestational age at the first prenatal visit, and district of residence, based on the 7 health districts in Maceió. Those health districts are defined using common geographic characteristics, and have significant urban social inequalities.

      Brasil. Prefeitura Municipal de Maceió. Secretaria Municipal de Assistência Social. Plano Municipal de Assistência Social de Maceió 2014-2017. Available at: http://www.maceio.al.gov.br/wp-content/uploads/admin/documento/2014/08/pmas_Maceió_2014_2017-finalizado-para-upar.pdf. Accessed on February 14, 2015.

      The screening program consisted of collecting capillary blood samples via S&S #903 filter paper (Schleicher & Schuell, Keene, NH) for serological testing at the laboratory of the Instituto de Pesquisa e Diagnóstico Laboratorial of the Association of Parents and Friends of Handicapped Children of Maceió (Associação de Pais e Amigos dos Excepcionais: APAE Maceió). In this laboratory, the blood samples were re-suspended for enzyme-linked immunosorbent assay (ELISA) testing for anti-T. pallidum antibodies, anti-HTLV antibodies, HBsAg, anti-HBc antibodies, and anti-HIV antibodies, according to the manufacturer's specifications. The specific kits were the Q-Preven Total Syphilis-DBS, Q-Preven HIV 1+2-DBS, Q-Preven HTLV-1+2-DBS, and Q-Preven HBsAg-DBS, which are manufactured by Symbiosis Diagnóstica Ltd (São Paulo, Brazil). When a woman tested positive for any of these tests, a second peripheral blood sample was collected and analyzed via conventional testing at the same laboratory to confirm the preliminary findings. Pregnant women were considered to be infected with T. pallidum based on the Venereal Disease Research Laboratory (VDRL) test (any titer), with HIV based on ELISA and western blot (WB) anti-HIV testing, with HTLV-1 and -2 based on ELISA and WB anti-HTLV-1 and -2 testing, and with HBV based on anti-HBc and HBsAg ELISA testing. Only pregnant women who underwent the entire diagnostic procedure for each disease were included in our analyses. During the third trimester, capillary blood was collected again to screen for syphilis and HIV infection, using the same criteria (Figure 1).
      Figure thumbnail gr1
      Figure 1Flowchart for the Municipal Health of Maceió prenatal screening program during the study period.

      2.2 Data analysis

      Statistical analyses were performed using Stata software (version 12.1, StataCorp LP, College Station, TX, USA), and differences with a p-value of <0.05 were considered statistically significant. The analyzed variables included the prevalences of syphilis, HIV, HTLV, and HBV infections, and the seroconversion rates for syphilis and HIV infections. The prevalences of syphilis and HIV infection were tested for associations with age group (⿤19 years old or >19 years old), self-reported ethnicity (mixed race, white, black, or Asian), number of miscarriages (<2 or ⿥2), beginning of prenatal care (<12 weeks of gestation or ⿥12 or more weeks of gestation), and the district of residence (Maceió health district 1⿿7). Differences between proportional data were compared using the chi-square test, and variables with a p-value of ⿤0.20 in the univariate analyses were included in the multivariate model.

      3. Results

      Among 54,813 pregnant women who provided capillary blood samples during their first trimester, 54,744 (99.9%) were tested for syphilis, 54,811 (99.9%) were tested for HIV infection, 54,798 (99.9%) were tested for HTLV infection, and 54,798 (99.9%) were tested for HBV infection. The birth date was reported by 99.6% of the participants, ethnicity by 92.6%, beginning of prenatal care by 85.1%, number of abortions by 75.3%, and district of residence by 85.1%. The average age was 23.3 ± 6.1 years (95% confidence interval [CI]: 15⿿35 years), and 31.5% of the participants were adolescents (⿤19 years old). Pregnant women self-reported their ethnicity as mixed race (68.3%), white (21.8%), black (8.8%), or Asian (1%). Gestational age at the beginning of prenatal care was 16.4 ± 7 weeks (95% CI: 8⿿30 weeks), and 34% of the participants began their prenatal care at ⿤12 weeks of gestation.
      Table 1 lists the prevalences of syphilis, HIV, HTLV, and HBV infections according to the participants⿿ socio-demographic and antenatal characteristics. Table 2 lists the general prevalences of syphilis, HIV, HTLV, and HBV infections. Among the pregnant women who were seronegative for syphilis or for HIV during their first trimester, 42% and 43% were tested again during their third trimester, respectively. Seroconversion for syphilis was observed in 123 (0.5%) of these participants and seroconversion for HIV occurred in 14 (0.06%) of these participants.
      Table 1Prevalence of syphilis, HIV infection, HTLV infection and HBV infection according to socio-demographic and antenatal characteristics of urban pregnant Northeastern Brazilian women (2007⿿2012).
      Syphilis

      % (screened)
      HIV infection

      % (screened)
      HTLV infection

      %

      (screened)
      HBV infection

      % (screened)
      Age (years)
       ⿤191.4 (17,220)0.3 (17,231)0.2 (17,229)0.3 (17,225)
       >193.5 (37,329)0.4 (37,385)0.2 (37,374)0.4 (37,378)
      p-value*<0.00010.10.2990.062
      Ethnicity
       White2.3 (11,090)0.2 (11,108)0.2 (11,105)0.4 (11,107)
       Non-white3.0 (39,604)0.4 (39,651)0.2 (39,642)0.4 (39,641)
       p-value*<0.00010.0140.5660.384
      Beginning of Prenatal care (weeks)
       ⿤122.3 (15,807)0.3 (15,827)0.2 (15,822)0.4 (15,823)
       >123.0 (30,763)0.4 (30,805)0.2 (30,796)0.4 (30,798)
      p-value*<0.00010.0520.240.179
      Miscarriage
       <22.5 (38,649)0.3 (38,692)0.2 (38,682)0.4 (38,684)
      >27.0 (2,546)0.5 (2,559)0.4 (2,557)0.6 (2,557)
       p-value*<0.00010.130.0390.262
      District of residence
       1st district2.2 (4,533)0.4 (4,539)0.2 (4,539)0.4 (4,540)
       2nd district4.0 (7,580)0.4 (7,598)0.4 (7,957)0.5 (7,596)
       3rd district2.6 (3,882)0.3 (3,885)0.1 (3,884)0.4 (3,885)
       4th district2.3 (5,418)0.2 (5,425)0.3 (5,423)0.3 (5,422)
       5th district3.0 (10,028)0.3 (10,035)0.2 (10,033)0.3 (10,033)
       6th district2.7 (8,152)0.5 (8,163)0.3 (8,162)0.5 (8,158)
       7th district2.6 (13,093)0.3 (13,107)0.2 (13,131)0.4 (13,105)
       p-value*<0.0010.0650.0120.528
      HIV: human immunodeficiency virus, HTLV: human T-lymphotropic virus, HBV: hepatitis B virus.
      Table 2Prevalence of syphilis, and HIV, HTLV, and HBV infections and seroconversion rates for syphilis and HIV infection among urban pregnant Northeastern Brazilian women (2007⿿2012).
      ScreenedPrevalence

      (95% CI)
      Second test (n)Seroconversion rate (95% CI)
      Syphilis54,7442.8 (2.69⿿2.97)23,0030.5 (0.45⿿0.64)
      HIV infection54,8110.3 (0.29⿿0.39)23,5490.06 (0.03⿿0.10)
      HTLV infection54,7980.2 (0.18⿿0.26)--
      HBV infection54,7980.4 (0.36⿿0.47)--
      HIV: human immunodeficiency virus, HTLV: human T-lymphotropic virus, HBV: hepatitis B virus, CI: confidence interval.
      Syphilis was more prevalent among women who were >19 years old, compared to among adolescents (adjusted odds ratio [aOR]: 1.87; p < 0.001), although age was not significantly associated with HIV prevalence. Syphilis and HIV infections were more prevalent among self-reported non-white women, compared to white women (aORs: 1.63 and 1.26, respectively; p < 0.05). Syphilis was more prevalent among women who began prenatal care after 12 weeks of gestation and among women who had ⿥2 miscarriages (aORs: 1.21 and 1.87, respectively; both p < 0.01), although there was no significant association with the prevalence of HIV infection. Syphilis was more prevalent among pregnant women from Maceió health districts 2 and 5 (aORs: 1.92 and 1.40 respectively; both p < 0.05), although there were no district-specific differences in the prevalences of HIV infection (Table 3, Table 4).
      Table 3Univariate and multivariate analysis of socio-demographic factors that were associated with syphilis among urban pregnant Northeastern Brazilian women (2007⿿2012).
      Univariate analysisMultivariate analysis
      The final model was adjusted for age group, ethnicity, miscarriages, beginning of prenatal care, district of residence and HIV infection. HIV: human immunodeficiency virus, OR: odds ratio, CI: confidence interval.
      OR95% CIpOR95% CIp
      Age >19 years2.552.22⿿2.920.0011.871.53⿿2.280.001
      Non-white1.331.17⿿1.530.0011.261.06⿿1.500.009
      ⿥2 miscarriages2.922.48⿿3.450.0011.871.54⿿2.270.001
      Beginning of prenatal care

      (>12 weeks of gestational age)
      1.291.14⿿1.460.0011.211.05⿿1.410.009
      District of residence0.0010.001
       1st district1.00
       2nd district1.831.42⿿2.300.0011.921.44⿿2.640.001
       3rd district1.200.95⿿1.580.2091.390.95⿿1.970.069
       4th district1.020.78⿿1.330.8781.020.71⿿1.490.899
       5th district1.361.09⿿1.720.0071.401.03⿿1.890.031
       6th district1.240.99⿿1.580.0701.340.97⿿1.830.073
       7th district1.170.93⿿1.470.1701.220.90⿿1.640.199
      HIV infection6.174.12⿿9.250.0014.622.72⿿7.840.001
      a The final model was adjusted for age group, ethnicity, miscarriages, beginning of prenatal care, district of residence and HIV infection. HIV: human immunodeficiency virus, OR: odds ratio, CI: confidence interval.
      Table 4Univariate and multivariate analysis of socio-demographic factors that were associated with HIV infection among urban pregnant Northeastern Brazilian women (2007⿿2012)
      Univariate analysisMultivariate analysis
      The final model was adjusted for ethnicity and Treponema pallidum infection. HIV: human immunodeficiency virus, OR: odds ratio, CI: confidence interval.
      OR95% CIpOR95% CIp
      Age >19 years1.310.95⿿1.830.101
      Non-white1.691.11⿿2.590.0151.631.05⿿2.540.030
      ⿥2 miscarriages1.550.87⿿2.750.133
      Beginning of prenatal care

      (>12 weeks of gestational age)
      1.410.99⿿2.000.050
      District of residence0.073
       1st district1.220.68⿿2.180.511
       2nd district1.450.91⿿2.330.119
       3rd district1.070.56⿿2.040.848
       4th district0.700.36⿿1.370.296
       5th district1.000.61⿿1.620.990
       6th district1.701.08⿿2.640.020
       7th district1.00
      Syphilis6.174.12⿿9.250.0015.713.75⿿8.690.001
      a The final model was adjusted for ethnicity and Treponema pallidum infection. HIV: human immunodeficiency virus, OR: odds ratio, CI: confidence interval.
      The overall prevalence of coinfection was 0.08%, and the proportions of coinfections are listed in Table 5, Table 6. Pregnant women who were infected with T. pallidum had a 4.62-fold greater risk of being coinfected with HIV (p < 0.001), and pregnant women who were infected with HIV had a 5.71-fold greater risk of being coinfected with T. pallidum (p < 0.001) (Table 3, Table 4). Among pregnant women with syphilis, 3 (0.5%) seroconverted to HIV during pregnancy (p < 0.001), and the rate ratio for HIV seroconversion among these women was 11.02-fold greater than that among women who did not have syphilis (p < 0.001). One woman who was infected with HIV seroconverted to syphilis during pregnancy, and another seroconverted to both HIV and syphilis during pregnancy. However, HIV and HTLV coinfection was not observed in the study population.
      Table 5Prevalences of coinfections among urban pregnant Northeastern Brazilian women (2007⿿2012).
      CoinfectionScreened%
      SyphilisHIV54,7420.050
      HTLV54,7290.007
      HBV54,7290.009
      HIVHBV54,7960.002
      HTLV54,7290
      HTLVHBV54,7830.009
      HIV: human immunodeficiency virus, HTLV: human T-lymphotropic virus, HBV: hepatitis B virus.
      Table 6Proportion of coinfections with syphilis, HIV, HTLV, and hepatitis B among urban pregnant Northeastern Brazilian women (2007⿿2012).
      Coinfections (%)
      nSyphilisHIVHTLVHepatitis B
      Syphilis1,550-1.80.30.3
      p-value<0.0010.6880.581
      HIV infection18615.1-00.5
      p-value<0.0010.786
      HTLV infection1183.4a0-4.2
      p-value0.688<0.001
      Hepatitis B2262.20.4b2.2-
      p-value0.5810.786<0.001
      a Baseline = 116; b baseline = 225. HIV: human immunodeficiency virus, HTLV: human T-lymphotropic virus, HBV: hepatitis B virus.

      4. Discussion

      The present study's findings revealed a syphilis prevalence of 2.8% among pregnant women who underwent prenatal care at public healthcare facilities in a Northeastern Brazilian capital city, which is 2.3-fold greater than the prevalence from a national study (1.20%).
      • Domingues R.M.
      • Szwarcwald C.L.
      • Souza P.R.B.
      • Leal Mdo C.
      Prevalence of syphilis in pregnancy and prenatal syphilis testing in Brazil: Birth in Brazil study.
      However, methodological differences in the diagnostic testing may have contributed to this discrepancy. Disparate prevalences have been reported in various regions of Brazil, which indicates a heterogeneous distribution of syphilis.
      • Domingues R.M.
      • Saracen V.
      • Hartz Z.M.
      • Leal Mdo C.
      Congenital syphilis: a sentinel event in antenatal care quality.
      • Lima L.H.
      • Viana M.C.
      Prevalence and risk factors for HIV, syphilis, hepatitis B, hepatitis C, and HTLV-I/II infection in low-income postpartum and pregnant women in Greater Metropolitan Vito̿ria, Espi̿rito Santo State, Brazil.
      We also observed a 0.5% seroconversion rate for syphilis during the third trimester in Maceió, which is similar to the reported national rates.
      • Domingues R.M.
      • Szwarcwald C.L.
      • Souza P.R.B.
      • Leal Mdo C.
      Prevalence of syphilis in pregnancy and prenatal syphilis testing in Brazil: Birth in Brazil study.
      Therefore, it is important to perform continued surveillance and counseling of pregnant women during all prenatal care visits, and to provide treatment for the women and their partners.
      In Brazil, the prevalence of HIV infection among pregnant women is 0.4%,
      • Domingues R.M.
      • Szwarcwald C.L.
      • Souza P.R.B.
      • Leal Mdo C.
      Prenatal testing and prevalence of HIV infection during pregnancy: data from the ⿿Birth in Brazil⿿ study, a national hospital-based study.
      although several studies have reported regional variations from 0.16% to 0.6%.
      • Botelho C.A.O.
      • Tomaz C.A.B.
      • Cunha R.V.
      • Botelho M.A.O.
      • Botelho L.O.
      • Assis D.M.
      • et al.
      Prevalence of diseases screened by a pregnancy protection program of the State of Mato Grosso do Sul, Brazil, 2004⿿2007.
      • Machado Filho A.C.
      • Sardinha J.F.J.
      • Ponte R.L.
      • Costa E.P.
      • da Silva S.S.
      • Martinez-Espinosa F.E.
      Prevalence of infection for HIV, HTLV, HBV and of syphilis and chlamydia in pregnant women in a tertiary health unit in the western Brazilian Amazon region.
      • Olbrich J.
      • Meira D.A.
      Seroprevalence of HTLV-I/II, HIV, syphilis and toxoplasmosis among pregnant women seen at Botucatu - São Paulo - Brazil. Risk factors for HTLV-I/II infection.
      In this study, we found a 0.3% seroprevalence of HIV infection among pregnant women, and a 0.06% seroconversion rate during pregnancy. This seroconversion rate occurred in a population with approximately 50% coverage during the second test, compared to 15% coverage during the second test in the national study.
      • Domingues R.M.
      • Szwarcwald C.L.
      • Souza P.R.B.
      • Leal Mdo C.
      Prenatal testing and prevalence of HIV infection during pregnancy: data from the ⿿Birth in Brazil⿿ study, a national hospital-based study.
      These findings reaffirm the consensus that pregnant women should be screened for HIV infection, and support the recommendation of a HIV second test during the third semester or delivery, in order to provide effective interventions that can prevent mother-to-child transmission.
      • Mussi-Pinhata M.M.
      • Quintana S.M.
      Screening for infectious diseases during pregnancy: which test and which situation.
      • Patterson K.B.
      • Leone P.A.
      • Fiscus S.A.
      • Kuruc J.
      • McCoy S.I.
      • Wolf L.
      • et al.
      Frequent detection of acute HIV infection in pregnant women.
      Only ethnicity was associated with HIV infection in our multivariate analysis. This higher HIV infection prevalence among non-white women is likely due to a lower socioeconomic status, which is more common among non-white women in Brazil.
      • Lopes F.
      • Buchalla C.M.
      • Ayres J.R.M.
      Black and non-Black women and vulnerability to HIV/AIDS in São Paulo, Brazil.
      Syphilis and HIV coinfection occurred in 0.05% of the pregnant women in Maceió, and our multivariate analysis revealed a strong risk of HIV-infected pregnant women becoming coinfected with T. pallidum (aOR: 5.71; p < 0.001). Among pregnant women who had HIV infection, 15.1% were coinfected with syphilis, which is approximately 5.5-fold higher than the national study rate (2.85%; aOR: 4.75).
      • Domingues R.M.
      • Szwarcwald C.L.
      • Souza P.R.B.
      • Leal Mdo C.
      Prenatal testing and prevalence of HIV infection during pregnancy: data from the ⿿Birth in Brazil⿿ study, a national hospital-based study.
      Syphilis facilitates HIV infection in several ways, and coinfection can promote the aggravation and progression of both diseases.
      • Karp G.
      • Schlaeffer F.
      • Jotkowitz A.
      • Riesenberg K.
      Syphilis and HIV co-infection.
      We found an HTLV seroprevalence of 0.2% among the screened pregnant women. Other Brazilian studies have reported seroprevalences among pregnant women that range from 0.1% to 1.05%.
      • Olbrich J.
      • Meira D.A.
      Seroprevalence of HTLV-I/II, HIV, syphilis and toxoplasmosis among pregnant women seen at Botucatu - São Paulo - Brazil. Risk factors for HTLV-I/II infection.
      • Mello M.A.
      • Conceição A.F.
      • Sousa S.M.
      • Alcântara L.C.
      • Marin L.J.
      • Regina da Silva Raiol M.
      • et al.
      HTLV-1 in pregnant women from the Southern Bahia, Brazil: a neglected condition despite the high prevalence.
      Prenatal screening for HTLV-1 and -2 infections is not recommended in populations with a low seroprevalence, despite there being no available treatment, and the transmission rate is estimated at 2.7% for non-breastfed infants.
      • Ando Y.
      • Matsumoto Y.
      • Nakano S.
      • Saito K.
      • Kakimoto K.
      • Tanigawa T.
      • et al.
      Long-term follow up study of vertical HTLV-I infection in children breast-fed by seropositive mothers.
      Therefore, local seroprevalence studies should be performed to identify at-risk groups during prenatal care, and this information should be used to guide policy decisions regarding screening pregnant women for HTLV.
      The prevalence of HBV infection among pregnant women was 0.4% in Maceió. Previous studies have reported similar prevalences of 0.3⿿0.8% among pregnant Brazilian women.
      • Botelho C.A.O.
      • Tomaz C.A.B.
      • Cunha R.V.
      • Botelho M.A.O.
      • Botelho L.O.
      • Assis D.M.
      • et al.
      Prevalence of diseases screened by a pregnancy protection program of the State of Mato Grosso do Sul, Brazil, 2004⿿2007.
      • Liell A.P.
      • Weber D.
      • Toscan C.
      • Fornari F.
      • Madalosso L.F.
      Prevalence of HBsAg in pregnant women of Passo Fundo, RS, Brazil: comparative study between public and private health systems.
      The administration of the HBV vaccine and HBV-specific immunoglobulin within 12 h of birth increases the efficacy of the prophylactic program from 72% (through routine vaccination alone) to 97%.
      • Lee C.
      • Gong Y.
      • Brok J.
      • Boxall E.H.
      • Gluud C.
      Effect of hepatitis B immunisation in newborn infants of mothers positive for hepatitis B surface antigen: systematic review and meta-analysis.
      • Tornatore M.
      • Gonçalves C.V.
      • Bianchi M.S.
      • Germano F.N.
      • Garcés A.X.
      • Soares M.A.
      • et al.
      Co-infections associated with human immunodeficiency virus type 1 in pregnant women from southern Brazil: high rate of intraepithelial cervical lesions.
      Therefore, routine screening of pregnant women remains important in countries where the vaccine is administered, as the diagnosis of HBV infection can help guide the healthcare team in administering immunoglobulin to the newborn.
      In our data, we infrequently observed cases of coinfection with syphilis and HBV, syphilis and HTLV, or HBV and HIV; no cases of HIV and HTLV were reported. HBV and HTLV coinfection occurred in 0.009% of the participants, and although rare, this association was statistically significant. Among pregnant women who were infected with HTLV, 4.2% were also carriers of HBV (p < 0.001). We have found no other studies that have evaluated this association among pregnant women.
      Our multivariate analysis revealed that syphilis was associated with age (>19 years old), and this increased prevalence among older women may be related to successive reinfection. Non-white pregnant women had a higher prevalence of syphilis, which is similar to the national report's findings.
      • Domingues R.M.
      • Szwarcwald C.L.
      • Souza P.R.B.
      • Leal Mdo C.
      Prevalence of syphilis in pregnancy and prenatal syphilis testing in Brazil: Birth in Brazil study.
      We also found an association between syphilis and late initiation of prenatal care, which is considered an independent risk factor for high-risk pregnancies, and may indicate reduced access to health services, low education level, or lack of interest or knowledge regarding the importance of early pregnancy monitoring.
      • Pereira P.H.G.
      • Antón A.G.S.
      • Vieira Junior W.S.
      • Domingues R.A.D.
      • Melo A.L.
      • Farias C.S.
      • et al.
      Associated factors to later access to prenatal care of Health Center #1 of Paranoá, Brazil, 2005.
      In this study, syphilis was associated with the number of abortions (⿥2). Unfortunately, miscarriages and perinatal or neonatal deaths occur in 40% of children who are infected via untreated mothers,
      • Lindstrand A.
      • Bergstron S.
      • Bugalho A.
      • Zanconato G.
      • Helgesson A.M.
      • Hederstedt B.
      Prevalence of syphilis infection in Mozambican women with second trimester miscarriage and women attending antenatal care in second trimester.
      which may also indicate that these pregnant women are long-time carriers of the disease. Maceió health districts 2 and 5 also had significantly higher syphilis prevalences. Lower income and lower education, compared to other health districts, may explain those findings.

      Brasil. Prefeitura Municipal de Maceió. Secretaria Municipal de Assistência Social. Plano Municipal de Assistência Social de Maceió 2014-2017. Available at: http://www.maceio.al.gov.br/wp-content/uploads/admin/documento/2014/08/pmas_Maceió_2014_2017-finalizado-para-upar.pdf. Accessed on February 14, 2015.

      Nevertheless, it is possible that non-assessed factors may also be responsible for the higher prevalences in those districts. Therefore, studies are needed to deepen our understanding of these communities⿿ characteristics and to define local public health strategies that can modify the prevalence of syphilis.
      In conclusion, our findings support continuous screening of pregnant women for syphilis, HIV, and HBV infection, especially given the severity of syphilis and HIV coinfection. While our assessment of associated factors is limited by the small number of variables that were collected during the routine screening program, this study concomitantly evaluated 4 infectious diseases and their coinfections, and determined the seroconversion rates of two diseases that have high priority in public healthcare. Furthermore, few other studies have reported the coinfection rates of infectious diseases among pregnant women. Therefore, as Maceió has urban characteristics and social, economic, and health service structures that are similar to other medium-sized Northeastern Brazilian urban centers, our findings may be relevant to promote systematic screening of pregnant women in these centers, and to support appropriate public policies and prevention strategies to improve individual and societal health.
      Conflicts of interest: None.
      Source of support: DECIT/SCTIE/MS from the National Council of Technological and Scientific Development (CNPq); Fundação de Amparo à Pesquisa de Alagoas (FAPEAL); Secretaria de Estado da Saúde de Alagoas (SESAU-AL). The funding source had no role in study design; in the collection, analysis and interpretation of data; in the writing of the report; and in the decision to submit the article for publication.
      Author contribution: AAM conceived the idea, participated in the data collection, in the literature review, and in writing and reviewing the manuscript.
      MJGM supervised the study and revised the manuscript.
      JBC supervised the study and reviewed the manuscript
      All authors have approved the final article.
      Ethics statement: The ethics committee of the Instituto de Medicina Integral Prof. Fernando Figueira approved the study design (CAAE: 06733812.2.0000.5201; Plataforma Brasil).

      References

        • Mussi-Pinhata M.M.
        • Quintana S.M.
        Screening for infectious diseases during pregnancy: which test and which situation.
        Curr Women's Health Rev. 2012; 8: 158-171
        • Ando Y.
        • Matsumoto Y.
        • Nakano S.
        • Saito K.
        • Kakimoto K.
        • Tanigawa T.
        • et al.
        Long-term follow up study of vertical HTLV-I infection in children breast-fed by seropositive mothers.
        J Infect. 2003; 46: 177-179
        • Newman L.
        • Kamb M.
        • Hawkes S.
        • Gomez G.
        • Say L.
        • Seuc A.
        • et al.
        Global estimates of syphilis in pregnancy and associated adverse outcomes: analysis of multinational antenatal surveillance data.
        PLoS Med. 2013; 10: e1001396
      1. World Health Organization. Taking stock: HIV in children - the state of affairs. Geneva: World Health Organization 2006. Available at: http://apps.who.int/iris/handle/10665/69760. Accessed on March 13, 2015.

      2. World Health Organization. The global elimination of congenital syphilis: rationale and strategy for action. Geneva: World Health Organization 2008. Available at:. http://www.who.int/reproductivehealth/publications/rtis/9789241595858/en/. Accessed on March 13, 2015.

      3. World Health Organization. Fact sheet No. 204: Hepatitis b. Available at: http://www.who.int/mediacentre/factsheets/fs204/en/. Accessed on March 13, 2015.

        • Lee C.
        • Gong Y.
        • Brok J.
        • Boxall E.H.
        • Gluud C.
        Effect of hepatitis B immunisation in newborn infants of mothers positive for hepatitis B surface antigen: systematic review and meta-analysis.
        BMJ. 2006; 332: 328-336
        • Peeters M.
        • D⿿Arc M.
        • Delaporte E.
        The origin and diversity of human retroviruses.
        AIDS Rev. 2014; 16: 23-34
        • Monteiro D.L.M.
        • Taquette S.R.
        • Barmpas D.B.S.
        • Rodrigues N.C.
        • Teixeira S.A.
        • Villela L.H.
        • et al.
        Prevalence of HTLV-1/2 in pregnant women living in the metropolitan area of Rio de Janeiro.
        PLoS Negl Trop Dis. 2014; 9: e3146
        • Griffiths E.C.
        • Pedersen A.B.
        • Fenton A.
        • Petchey O.L.
        The nature and consequences of coinfection in humans.
        J Infect. 2011; 63: 200-206
      4. Brasil. Ministério da Saúde. DATASUS. Informações de Saúde. Available at: http://tabnet.datasus.gov.br/cgi/tabcgi.exe?sinasc/cnv/nval.def. Accessed on July 25, 2014.

      5. Brasil. Ministério da Saúde. Departamento de Ações Programáticas Estratégicas. Manual dos Comitês de Mortalidade Materna. Available at: http://bvsms.saude.gov.br/bvs/publicacoes/comites_mortalidade_materna_3ed.pdf. Accessed on July 25, 2014.

      6. Agência Nacional de Saúde Suplementar. Dados e Indicadores do Setor. Available at: http://www.ans.gov.br/perfil-do-setor/dados-e-indicadores-do-setor. Accessed on April 24, 2015.

      7. Brasil. Prefeitura Municipal de Maceió. Secretaria Municipal de Assistência Social. Plano Municipal de Assistência Social de Maceió 2014-2017. Available at: http://www.maceio.al.gov.br/wp-content/uploads/admin/documento/2014/08/pmas_Maceió_2014_2017-finalizado-para-upar.pdf. Accessed on February 14, 2015.

        • Domingues R.M.
        • Szwarcwald C.L.
        • Souza P.R.B.
        • Leal Mdo C.
        Prevalence of syphilis in pregnancy and prenatal syphilis testing in Brazil: Birth in Brazil study.
        Rev Saude Publica. 2014; 48: 766-774
        • Domingues R.M.
        • Saracen V.
        • Hartz Z.M.
        • Leal Mdo C.
        Congenital syphilis: a sentinel event in antenatal care quality.
        Rev Saude Publica. 2013; 47: 147-157
        • Lima L.H.
        • Viana M.C.
        Prevalence and risk factors for HIV, syphilis, hepatitis B, hepatitis C, and HTLV-I/II infection in low-income postpartum and pregnant women in Greater Metropolitan Vito̿ria, Espi̿rito Santo State, Brazil.
        Cad. Saude Publica. 2009; 25: 668-676
        • Domingues R.M.
        • Szwarcwald C.L.
        • Souza P.R.B.
        • Leal Mdo C.
        Prenatal testing and prevalence of HIV infection during pregnancy: data from the ⿿Birth in Brazil⿿ study, a national hospital-based study.
        BMC Infect Dis. 2015; 15: 100
        • Botelho C.A.O.
        • Tomaz C.A.B.
        • Cunha R.V.
        • Botelho M.A.O.
        • Botelho L.O.
        • Assis D.M.
        • et al.
        Prevalence of diseases screened by a pregnancy protection program of the State of Mato Grosso do Sul, Brazil, 2004⿿2007.
        Rev Patol Trop. 2008; 37 ([Portuguese]): 341-353
        • Machado Filho A.C.
        • Sardinha J.F.J.
        • Ponte R.L.
        • Costa E.P.
        • da Silva S.S.
        • Martinez-Espinosa F.E.
        Prevalence of infection for HIV, HTLV, HBV and of syphilis and chlamydia in pregnant women in a tertiary health unit in the western Brazilian Amazon region.
        Rev Bras Ginecol Obstet. 2010; 32 ([Portuguese]): 176-183
        • Olbrich J.
        • Meira D.A.
        Seroprevalence of HTLV-I/II, HIV, syphilis and toxoplasmosis among pregnant women seen at Botucatu - São Paulo - Brazil. Risk factors for HTLV-I/II infection.
        Rev Soc Bras Med Trop. 2004; 37 ([Portuguese]): 28-32
        • Patterson K.B.
        • Leone P.A.
        • Fiscus S.A.
        • Kuruc J.
        • McCoy S.I.
        • Wolf L.
        • et al.
        Frequent detection of acute HIV infection in pregnant women.
        AIDS. 2007; 21: 2303-2308
        • Lopes F.
        • Buchalla C.M.
        • Ayres J.R.M.
        Black and non-Black women and vulnerability to HIV/AIDS in São Paulo, Brazil.
        Rev Saude Publica. 2007; 41 ([Portuguese]): 39-46
        • Karp G.
        • Schlaeffer F.
        • Jotkowitz A.
        • Riesenberg K.
        Syphilis and HIV co-infection.
        Eur J Intern Med. 2009; 20: 9-13
        • Mello M.A.
        • Conceição A.F.
        • Sousa S.M.
        • Alcântara L.C.
        • Marin L.J.
        • Regina da Silva Raiol M.
        • et al.
        HTLV-1 in pregnant women from the Southern Bahia, Brazil: a neglected condition despite the high prevalence.
        Virol J. 2014; 11: 28
        • Liell A.P.
        • Weber D.
        • Toscan C.
        • Fornari F.
        • Madalosso L.F.
        Prevalence of HBsAg in pregnant women of Passo Fundo, RS, Brazil: comparative study between public and private health systems.
        Arq Gastroenterol. 2009; 46 ([Portuguese]): 75-77
        • Tornatore M.
        • Gonçalves C.V.
        • Bianchi M.S.
        • Germano F.N.
        • Garcés A.X.
        • Soares M.A.
        • et al.
        Co-infections associated with human immunodeficiency virus type 1 in pregnant women from southern Brazil: high rate of intraepithelial cervical lesions.
        Mem Inst Oswaldo Cruz, Rio de Janeiro. 2012; 107 ([Portuguese]): 205-210
        • Pereira P.H.G.
        • Antón A.G.S.
        • Vieira Junior W.S.
        • Domingues R.A.D.
        • Melo A.L.
        • Farias C.S.
        • et al.
        Associated factors to later access to prenatal care of Health Center #1 of Paranoá, Brazil, 2005.
        Comun Ciênc Saúde. 2006; 17 ([Portuguese]): 101-110
        • Lindstrand A.
        • Bergstron S.
        • Bugalho A.
        • Zanconato G.
        • Helgesson A.M.
        • Hederstedt B.
        Prevalence of syphilis infection in Mozambican women with second trimester miscarriage and women attending antenatal care in second trimester.
        Genitourin Med. 1993; 69 ([Portuguese]): 431-433