McGregor IA, 1984. Epidemiology, malaria and pregnancy. Am J Trop Med Hyg 33: 517–525.
Watson-Jones D, Weiss HA, Changalucha JM, Todd J, Gumodoka B, Bulmer J, Balira R, Ross D, Mugeye K, Hayes R, Mabey D, 2007. Adverse birth outcomes in United Republic of Tanzania–impact and prevention of maternal risk factors. Bull World Health Organ 85: 9–18.
McGregor IA, Wilson ME, Billewicz WZ, 1983. Malaria infection of the placenta in The Gambia, west Africa; its incidence and relationship to stillbirth, birthweight and placental weight. Trans R Soc Trop Med Hyg 77: 232–244.
Lawn JE, Blencowe H, Waiswa P, Amouzou A, Mathers C, Hogan D, Flenady V, Froen JF, Qureshi ZU, Calderwood C, Shiekh S, Jassir FB, You D, McClure EM, Mathai M, Cousens S, 2016. Stillbirths: rates, risk factors, and acceleration towards 2030. Lancet 387: 587–603.
Brabin BJ, 1983. An analysis of malaria in pregnancy in Africa. Bull World Health Organ 61: 1005–1016.
Johnson HL, Ghanem KG, Zenilman JM, Erbelding EJ, 2011. Sexually transmitted infections and adverse pregnancy outcomes among women attending inner city public sexually transmitted diseases clinics. Sex Transm Dis 38: 167–171.
Investigators of the Johns Hopkins Study of Cervicitis and Adverse Pregnancy Outcome, 1989. Association of Chlamydia trachomatis and Mycoplasma hominis with intrauterine growth retardation and preterm delivery. Am J Epidemiol 129: 1247–1257.
Blas MM, Canchihuaman FA, Alva IE, Hawes SE, 2007. Pregnancy outcomes in women infected with Chlamydia trachomatis: a population-based cohort study in Washington state. Sex Transm Infect 83: 314–318.
Liu B, Roberts CL, Clarke M, Jorm L, Hunt J, Ward J, 2013. Chlamydia and gonorrhoea infections and the risk of adverse obstetric outcomes: a retrospective cohort study. Sex Transm Infect 89: 672–678.
Rours GI, Duijts L, Moll HA, Arends LR, de Groot R, Jaddoe VW, Hofman A, Steegers EA, Mackenbach JP, Ott A, Willemse HF, van der Zwaan EA, Verkooijen RP, Verbrugh HA, 2011. Chlamydia trachomatis infection during pregnancy associated with preterm delivery: a population-based prospective cohort study. Eur J Epidemiol 26: 493–502.
Elliott B, Brunham RC, Laga M, Piot P, Ndinya-Achola JO, Maitha G, Cheang M, Plummer FA, 1990. Maternal gonococcal infection as a preventable risk factor for low birth weight. J Infect Dis 161: 531–536.
Cotch MF, Pastorek JG 2nd, Nugent RP, Hillier SL, Gibbs RS, Martin DH, Eschenbach DA, Edelman R, Carey JC, Regan JA, Krohn MA, Klebanoff MA, Rao AV, Rhoads GG, 1997. Trichomonas vaginalis associated with low birth weight and preterm delivery. The Vaginal Infections and Prematurity Study Group. Sex Transm Dis 24: 353–360.
Sutton MY, Sternberg M, Nsuami M, Behets F, Nelson AM, St Louis ME, 1999. Trichomoniasis in pregnant human immunodeficiency virus-infected and human immunodeficiency virus-uninfected congolese women: prevalence, risk factors, and association with low birth weight. Am J Obstet Gynecol 181: 656–662.
Hillier SL, Nugent RP, Eschenbach DA, Krohn MA, Gibbs RS, Martin DH, Cotch MF, Edelman R, Pastorek JG 2nd, Rao AV, McNellis D, Regan JA, Carey JC, Klebanoff MA; for the Vaginal Infections and Prematurity Study Group, 1995. Association between bacterial vaginosis and preterm delivery of a low-birth-weight infant. N Engl J Med 333: 1737–1742.
Riduan JM, Hillier SL, Utomo B, Wiknjosastro G, Linnan M, Kandun N, 1993. Bacterial vaginosis and prematurity in Indonesia: association in early and late pregnancy. Am J Obstet Gynecol 169: 175–178.
Minkoff H, Grunebaum AN, Schwarz RH, Feldman J, Cummings M, Crombleholme W, Clark L, Pringle G, McCormack WM, 1984. Risk factors for prematurity and premature rupture of membranes: a prospective study of the vaginal flora in pregnancy. Am J Obstet Gynecol 150: 965–972.
World Health Organization, 2012. Intermittent Preventive Treatment of Malaria in Pregnancy Using Sulfadoxine-Pyrimethamine (IPTp-SP). Updated WHO Policy Recommendation (October 2012). Available at: http://www.who.int/malaria/iptp_sp_updated_policy_recommendation_en_102012.pdf?ua=1.
World Health Organization, 2004. A Strategic Framework for Malaria Prevention and Control During Pregnancy in the Africa Region. Brazzaville, Congo: World Health Organization Regional Office for Africa.
van Eijk AM, Hill J, Larsen DA, Webster J, Steketee RW, Eisele TP, ter Kuile FO, 2013. Coverage of intermittent preventive treatment and insecticide-treated nets for the control of malaria during pregnancy in sub-Saharan Africa: a synthesis and meta-analysis of national survey data, 2009–11. Lancet Infect Dis 13: 1029–1042.
Desai M, Gutman J, Taylor SM, Wiegand RE, Khairallah C, Kayentao K, Ouma P, Coulibaly SO, Kalilani L, Mace KE, Arinaitwe E, Mathanga DP, Doumbo O, Otieno K, Edgar D, Chaluluka E, Kamuliwo M, Ades V, Skarbinski J, Shi YP, Magnussen P, Meshnick S, Ter Kuile FO, 2015. Impact of sulfadoxine-pyrimethamine resistance on effectiveness of intermittent preventive therapy for malaria in pregnancy at clearing infections and preventing low birth weight. Clin Infect Dis 62: 323–333.
Kayentao K, Garner P, van Eijk AM, Naidoo I, Roper C, Mulokozi A, MacArthur JR, Luntamo M, Ashorn P, Doumbo OK, ter Kuile FO, 2013. Intermittent preventive therapy for malaria during pregnancy using 2 vs 3 or more doses of sulfadoxine-pyrimethamine and risk of low birth weight in Africa: systematic review and meta-analysis. JAMA 309: 594–604.
Kuznik A, Habib AG, Manabe YC, Lamorde M, 2015. Estimating the public health burden associated with adverse pregnancy outcomes resulting from syphilis infection across 43 countries in sub-Saharan Africa. Sex Transm Dis 42: 369–375.
World Health Organization, 1991. Management of patients with sexually transmitted diseases. Report of a WHO Study Group. World Health Organ Tech Rep Ser 810: 1–103.
Pettifor A, Walsh J, Wilkins V, Raghunathan P, 2000. How effective is syndromic management of STDs? A review of current studies. Sex Transm Dis 27: 371–385.
Chico RM, Mayaud P, Ariti C, Mabey D, Ronsmans C, Chandramohan D, 2012. Prevalence of malaria and sexually transmitted and reproductive tract infections in pregnancy in sub-Saharan Africa. JAMA 307: 2079–2086.
Chico RM, Moss WJ, 2015. Prevention of malaria in pregnancy: a fork in the road? Lancet 386: 2454–2456.
Chaponda EB, Chandramohan D, Michelo C, Mharakurwa S, Chipeta J, Chico RM, 2015. High burden of malaria infection in pregnant women in a rural district of Zambia: a cross-sectional study. Malar J 14: 380.
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Chaudhry U, Saluja D, 2002. Detection of Neisseria gonorrhoeae by PCR using orf1 gene as target. Sex Transm Infect 78: 72.
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Malarial infection and curable sexually transmitted and reproductive tract infections (STIs/RTIs) are important causes of adverse birth outcomes. Reducing the burden of these infections in pregnancy requires interventions that can be easily integrated into the antenatal care (ANC) package. However, efforts to integrate the control of malarial infection and curable STIs/RTIs in pregnancy have been hampered by a lack of evidence related to their coinfection. Thus, we investigated the prevalence of coinfection among pregnant women of rural Zambia. A prospective cohort study was conducted in Nchelenge District, Zambia, involving 1,086 first ANC attendees. We screened participants for peripheral malarial infection and curable STIs/RTIs (syphilis, Chlamydia, gonorrhea, trichomoniasis, and bacterial vaginosis), and collected relevant sociodemographic data at booking. Factors associated with malarial and STI/RTI coinfection were explored using univariate and multivariate regression models. Among participants with complete results (N = 1,071), 38.7% (95% confidence interval [CI] = 35.7–41.6) were coinfected with malaria parasites and at least one STI/RTI; 18.9% (95% CI = 16.5–21.2) were infected with malaria parasites only; 26.0% (95% CI = 23.5–28.8) were infected with at least one STI/RTI but no malaria parasites, and 16.4% (95% CI = 14.1–18.6) had no infection. Human immunodeficiency virus (HIV)-infected women had a higher risk of being coinfected than HIV-uninfected women (odds ratio [OR] = 3.59 [95% CI = 1.73–7.48], P < 0.001). The prevalence of malarial and STI/RTI coinfection was high in this population. An integrated approach to control malarial infection and STIs/RTIs is needed to reduce this dual burden in pregnancy.
Financial support: This study was financially supported by the International Centers of Excellence for Malaria Research (ICEMR) in southern Africa, and the U.S. National Institutes of Health from NIH/NIAID grant U19AI089680 (Malaria Transmission and the Impact of Control Efforts in southern Africa) with John Hopkins University Bloomberg School of Public Health and the University of Zambia School Of Medicine (UNZA-SoM), and the Research Support Center at the UNZA-SoM through the southern African Consortium for Research Excellence (SACORE), which is part of the African Institutions Initiative grant of the Wellcome Trust (Company No. 2711000), a charity (No. 210183) registered in England, as well as the Commonwealth Scholarship Commission in the United Kingdom.
Authors' addresses: Enesia Banda Chaponda, Department of Biological Sciences, University of Zambia School of Natural Sciences, Lusaka, Zambia, E-mail: enesia.chaponda@gmail.com. R. Matthew Chico, Department of Disease Control, Faculty of Public Health and Policy, London School of Hygiene and Tropical Medicine, E-mail: matthew.chico@lshtm.ac.uk. Jane Bruce, Department of Disease Control and Vector Biology, London School of Hygiene and Tropical Medicine, London, United Kingdom, E-mail: jane.bruce@lshtm.ac.uk. Charles Michelo, Department of Public Health, University of Zambia School of Medicine, Lusaka, Zambia, E-mail: ccmichelo@yahoo.com. Bellington Vwalika, Department of Obstetrics and Gynaecology, University of Zambia School of Medicine, Lusaka, Zambia, E-mail: bvwalika@rzhrg-mail.org. Sungano Mharakurwa, Faculty of Health Sciences, Africa University, Mutare, Zimbabwe, and Department of Medical Microbiology and Immunology, Johns Hopkins University Bloomberg School of Public Health, Baltimore, MD, E-mail: mharakurwas@africau.edu. Mike Chaponda, Department of Clinical Sciences, Tropical Diseases Research Centre, Ndola, Zambia, E-mail: mikechaponda@yahoo.com. James Chipeta, Department of Paediatrics and Child Health, University of Zambia School of Medicine, Lusaka, Zambia, E-mail: assistdeanresearch@smuth-mru.org.zm. Daniel Chandramohan, Department of Disease Control, London School of Hygiene and Tropical Medicine, London, United Kingdom, E-mail: daniel.chandramohan@lshtm.ac.uk.
McGregor IA, 1984. Epidemiology, malaria and pregnancy. Am J Trop Med Hyg 33: 517–525.
Watson-Jones D, Weiss HA, Changalucha JM, Todd J, Gumodoka B, Bulmer J, Balira R, Ross D, Mugeye K, Hayes R, Mabey D, 2007. Adverse birth outcomes in United Republic of Tanzania–impact and prevention of maternal risk factors. Bull World Health Organ 85: 9–18.
McGregor IA, Wilson ME, Billewicz WZ, 1983. Malaria infection of the placenta in The Gambia, west Africa; its incidence and relationship to stillbirth, birthweight and placental weight. Trans R Soc Trop Med Hyg 77: 232–244.
Lawn JE, Blencowe H, Waiswa P, Amouzou A, Mathers C, Hogan D, Flenady V, Froen JF, Qureshi ZU, Calderwood C, Shiekh S, Jassir FB, You D, McClure EM, Mathai M, Cousens S, 2016. Stillbirths: rates, risk factors, and acceleration towards 2030. Lancet 387: 587–603.
Brabin BJ, 1983. An analysis of malaria in pregnancy in Africa. Bull World Health Organ 61: 1005–1016.
Johnson HL, Ghanem KG, Zenilman JM, Erbelding EJ, 2011. Sexually transmitted infections and adverse pregnancy outcomes among women attending inner city public sexually transmitted diseases clinics. Sex Transm Dis 38: 167–171.
Investigators of the Johns Hopkins Study of Cervicitis and Adverse Pregnancy Outcome, 1989. Association of Chlamydia trachomatis and Mycoplasma hominis with intrauterine growth retardation and preterm delivery. Am J Epidemiol 129: 1247–1257.
Blas MM, Canchihuaman FA, Alva IE, Hawes SE, 2007. Pregnancy outcomes in women infected with Chlamydia trachomatis: a population-based cohort study in Washington state. Sex Transm Infect 83: 314–318.
Liu B, Roberts CL, Clarke M, Jorm L, Hunt J, Ward J, 2013. Chlamydia and gonorrhoea infections and the risk of adverse obstetric outcomes: a retrospective cohort study. Sex Transm Infect 89: 672–678.
Rours GI, Duijts L, Moll HA, Arends LR, de Groot R, Jaddoe VW, Hofman A, Steegers EA, Mackenbach JP, Ott A, Willemse HF, van der Zwaan EA, Verkooijen RP, Verbrugh HA, 2011. Chlamydia trachomatis infection during pregnancy associated with preterm delivery: a population-based prospective cohort study. Eur J Epidemiol 26: 493–502.
Elliott B, Brunham RC, Laga M, Piot P, Ndinya-Achola JO, Maitha G, Cheang M, Plummer FA, 1990. Maternal gonococcal infection as a preventable risk factor for low birth weight. J Infect Dis 161: 531–536.
Cotch MF, Pastorek JG 2nd, Nugent RP, Hillier SL, Gibbs RS, Martin DH, Eschenbach DA, Edelman R, Carey JC, Regan JA, Krohn MA, Klebanoff MA, Rao AV, Rhoads GG, 1997. Trichomonas vaginalis associated with low birth weight and preterm delivery. The Vaginal Infections and Prematurity Study Group. Sex Transm Dis 24: 353–360.
Sutton MY, Sternberg M, Nsuami M, Behets F, Nelson AM, St Louis ME, 1999. Trichomoniasis in pregnant human immunodeficiency virus-infected and human immunodeficiency virus-uninfected congolese women: prevalence, risk factors, and association with low birth weight. Am J Obstet Gynecol 181: 656–662.
Hillier SL, Nugent RP, Eschenbach DA, Krohn MA, Gibbs RS, Martin DH, Cotch MF, Edelman R, Pastorek JG 2nd, Rao AV, McNellis D, Regan JA, Carey JC, Klebanoff MA; for the Vaginal Infections and Prematurity Study Group, 1995. Association between bacterial vaginosis and preterm delivery of a low-birth-weight infant. N Engl J Med 333: 1737–1742.
Riduan JM, Hillier SL, Utomo B, Wiknjosastro G, Linnan M, Kandun N, 1993. Bacterial vaginosis and prematurity in Indonesia: association in early and late pregnancy. Am J Obstet Gynecol 169: 175–178.
Minkoff H, Grunebaum AN, Schwarz RH, Feldman J, Cummings M, Crombleholme W, Clark L, Pringle G, McCormack WM, 1984. Risk factors for prematurity and premature rupture of membranes: a prospective study of the vaginal flora in pregnancy. Am J Obstet Gynecol 150: 965–972.
World Health Organization, 2012. Intermittent Preventive Treatment of Malaria in Pregnancy Using Sulfadoxine-Pyrimethamine (IPTp-SP). Updated WHO Policy Recommendation (October 2012). Available at: http://www.who.int/malaria/iptp_sp_updated_policy_recommendation_en_102012.pdf?ua=1.
World Health Organization, 2004. A Strategic Framework for Malaria Prevention and Control During Pregnancy in the Africa Region. Brazzaville, Congo: World Health Organization Regional Office for Africa.
van Eijk AM, Hill J, Larsen DA, Webster J, Steketee RW, Eisele TP, ter Kuile FO, 2013. Coverage of intermittent preventive treatment and insecticide-treated nets for the control of malaria during pregnancy in sub-Saharan Africa: a synthesis and meta-analysis of national survey data, 2009–11. Lancet Infect Dis 13: 1029–1042.
Desai M, Gutman J, Taylor SM, Wiegand RE, Khairallah C, Kayentao K, Ouma P, Coulibaly SO, Kalilani L, Mace KE, Arinaitwe E, Mathanga DP, Doumbo O, Otieno K, Edgar D, Chaluluka E, Kamuliwo M, Ades V, Skarbinski J, Shi YP, Magnussen P, Meshnick S, Ter Kuile FO, 2015. Impact of sulfadoxine-pyrimethamine resistance on effectiveness of intermittent preventive therapy for malaria in pregnancy at clearing infections and preventing low birth weight. Clin Infect Dis 62: 323–333.
Kayentao K, Garner P, van Eijk AM, Naidoo I, Roper C, Mulokozi A, MacArthur JR, Luntamo M, Ashorn P, Doumbo OK, ter Kuile FO, 2013. Intermittent preventive therapy for malaria during pregnancy using 2 vs 3 or more doses of sulfadoxine-pyrimethamine and risk of low birth weight in Africa: systematic review and meta-analysis. JAMA 309: 594–604.
Kuznik A, Habib AG, Manabe YC, Lamorde M, 2015. Estimating the public health burden associated with adverse pregnancy outcomes resulting from syphilis infection across 43 countries in sub-Saharan Africa. Sex Transm Dis 42: 369–375.
World Health Organization, 1991. Management of patients with sexually transmitted diseases. Report of a WHO Study Group. World Health Organ Tech Rep Ser 810: 1–103.
Pettifor A, Walsh J, Wilkins V, Raghunathan P, 2000. How effective is syndromic management of STDs? A review of current studies. Sex Transm Dis 27: 371–385.
Chico RM, Mayaud P, Ariti C, Mabey D, Ronsmans C, Chandramohan D, 2012. Prevalence of malaria and sexually transmitted and reproductive tract infections in pregnancy in sub-Saharan Africa. JAMA 307: 2079–2086.
Chico RM, Moss WJ, 2015. Prevention of malaria in pregnancy: a fork in the road? Lancet 386: 2454–2456.
Chaponda EB, Chandramohan D, Michelo C, Mharakurwa S, Chipeta J, Chico RM, 2015. High burden of malaria infection in pregnant women in a rural district of Zambia: a cross-sectional study. Malar J 14: 380.
Central Statistical Office (CSO), 2011. 2010 Census of Population and Housing. Lusaka, Zambia: Central Statistical Office, 12.
Ministry of Health, 2008. Health Management Information System (HMIS). Lusaka, Zambia: Ministry of Health.
Mercereau-Puijalon O, Fandeur T, Bonnefoy S, Jacquemot C, Sarthou JL, 1991. A study of the genomic diversity of Plasmodium falciparum in Senegal. 2. Typing by the use of the polymerase chain reaction. Acta Trop 49: 293–304.
Roper C, Elhassan IM, Hviid L, Giha H, Richardson W, Babiker H, Satti GM, Theander TG, Arnot DE, 1996. Detection of very low level Plasmodium falciparum infections using the nested polymerase chain reaction and a reassessment of the epidemiology of unstable malaria in Sudan. Am J Trop Med Hyg 54: 325–331.
Nugent RP, Krohn MA, Hillier SL, 1991. Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. J Clin Microbiol 29: 297–301.
Chaudhry U, Saluja D, 2002. Detection of Neisseria gonorrhoeae by PCR using orf1 gene as target. Sex Transm Infect 78: 72.
Kengne P, Veas F, Vidal N, Rey JL, Cuny G, 1994. Trichomonas vaginalis: repeated DNA target for highly sensitive and specific polymerase chain reaction diagnosis. Cell Mol Biol (Noisy-le-grand) 40: 819–831.
Schachter J, 1997. DFA, EIA, PCR, LCR and other technologies: what tests should be used for diagnosis of Chlamydia infections? Immunol Invest 26: 157–161.
World Health Organization, 2016. Maternal, Newborn, Child and Adolescent Health. Available at: http://www.who.int/maternal_child_adolescent/epidemiology/stillbirth/en/. Accessed May 18, 2016.
Watson-Jones D, Gumodoka B, Weiss H, Changalucha J, Todd J, Mugeye K, Buve A, Kanga Z, Ndeki L, Rusizoka M, Ross D, Marealle J, Balira R, Mabey D, Hayes R, 2002. Syphilis in pregnancy in Tanzania. II. The effectiveness of antenatal syphilis screening and single-dose benzathine penicillin treatment for the prevention of adverse pregnancy outcomes. J Infect Dis 186: 948–957.
Lauritsen JM, Bruus M, 2003–2005. EpiData (version 3.1). A Comprehensive Tool for Validated Entry and Documentation of Data. Odense, Denmark: The EpiData Association.
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