King CH, Dickman K, Tisch DJ, 2005. Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 365: 1561–1569.
Ashford RW, Craig PS, Oppenheimer SJ, 1992. Polyparasitism on the Kenya coast. 1. Prevalence, and association between parasitic infections. Ann Trop Med Parasitol 86: 671–679.
Ezeamama AE, McGarvey ST, Acosta LP, Zierler S, Manalo DL, Wu HW, Kurtis JD, Mor V, Olveda RM, Friedman JF, 2008. The synergistic effect of concomitant schistosomiasis, hookworm, and Trichuris infections on children's anemia burden. PLoS Negl Trop Dis 2: e245.
Brooker S, Akhwale W, Pullan R, Estambale B, Clarke SE, Snow RW, Hotez PJ, 2007. Epidemiology of Plasmodium-helminth co-infection in Africa: populations at risk, potential impact on anemia, and prospects for combining control. Am J Trop Med Hyg 77: 88–98.
Adegnika AA, Ramharter M, Agnandji ST, Ateba Ngoa U, Issifou S, Yazdanbahksh M, Kremsner PG, 2010. Epidemiology of parasitic co-infections during pregnancy in Lambarene, Gabon. Trop Med Int Health 15: 1204–1209.
Ndibazza J, Muhangi L, Akishule D, Kiggundu M, Ameke C, Oweka J, Kizindo R, Duong T, Kleinschmidt I, Muwanga M, Elliott AM, 2010. Effects of deworming during pregnancy on maternal and perinatal outcomes in Entebbe, Uganda: a randomized controlled trial. Clin Infect Dis 50: 531–540.
Navitsky RC, Dreyfuss ML, Shrestha J, Khatry SK, Stoltzfus RJ, Albonico M, 1998. Ancylostoma duodenale is responsible for hookworm infections among pregnant women in the rural plains of Nepal. J Parasitol 84: 647–651.
Friedman JF, Mital P, Kanzaria HK, Olds GR, Kurtis JD, 2007. Schistosomiasis and pregnancy. Trends Parasitol 23: 159–164.
Ndyomugyenyi R, Kabatereine N, Olsen A, Magnussen P, 2008. Efficacy of ivermectin and albendazole alone and in combination for treatment of soil-transmitted helminths in pregnancy and adverse events: a randomized open label controlled intervention trial in Masindi District, western Uganda. Am J Trop Med Hyg 79: 856–863.
Allen HE, Crompton DW, de Silva N, LoVerde PT, Olds GR, 2002. New policies for using anthelmintics in high risk groups. Trends Parasitol 18: 381–382.
Desai M, ter Kuile FO, Nosten F, McGready R, Asamoa K, Brabin B, Newman RD, 2007. Epidemiology and burden of malaria in pregnancy. Lancet Infect Dis 7: 93–104.
Steketee RW, Nahlen BL, Parise ME, Menendez C, 2001. The burden of malaria in pregnancy in malaria-endemic areas. Am J Trop Med Hyg 64: 28–35.
Yatich NJ, Jolly PE, Funkhouser E, Agbenyega T, Rayner JC, Ehiri JE, Turpin A, Stiles JK, Ellis WO, Jiang Y, Williams JH, 2010. The effect of malaria and intestinal helminth coinfection on birth outcomes in Kumasi, Ghana. Am J Trop Med Hyg 82: 28–34.
Egwunyenga AO, Ajayi JA, Nmorsi OP, Duhlinska-Popova DD, 2001. Plasmodium/intestinal helminth co-infections among pregnant Nigerian women. Mem Inst Oswaldo Cruz 96: 1055–1059.
Christian P, Khatry SK, West KP Jr, 2004. Antenatal anthelmintic treatment, birthweight, and infant survival in rural Nepal. Lancet 364: 981–983.
Larocque R, Casapia M, Gotuzzo E, MacLean JD, Soto JC, Rahme E, Gyorkos TW, 2006. A double-blind randomized controlled trial of antenatal mebendazole to reduce low birthweight in a hookworm-endemic area of Peru. Trop Med Int Health 11: 1485–1495.
Haider BA, Humayun Q, Bhutta ZA, 2009. Effect of administration of antihelminthics for soil transmitted helminths during pregnancy. Cochrane Database Syst Rev CD005547.
Malhotra I, Dent A, Mungai P, Wamachi A, Ouma JH, Narum DL, Muchiri E, Tisch DJ, King CL, 2009. Can prenatal malaria exposure produce an immune tolerant phenotype? A prospective birth cohort study in Kenya. PLoS Med 6: e1000116.
World Health Organization, UNICEF, 2004. Low Birthweight: Country, Regional and Global Estimates. Geneva: World Health Organization.
ACOG Committee on Practice Guidelines, 2008. ACOG Practice Bulletin No. 95: anemia in pregnancy. Obstet Gynecol 112: 201–207.
Hotez PJ, Brooker S, Bethony JM, Bottazzi ME, Loukas A, Xiao S, 2004. Hookworm infection. N Engl J Med 351: 799–807.
Friedman JF, Kanzaria HK, McGarvey ST, 2005. Human schistosomiasis and anemia: the relationship and potential mechanisms. Trends Parasitol 21: 386–392.
Ajanga A, Lwambo NJ, Blair L, Nyandindi U, Fenwick A, Brooker S, 2006. Schistosoma mansoni in pregnancy and associations with anaemia in northwest Tanzania. Trans R Soc Trop Med Hyg 100: 59–63.
Ndyomugyenyi R, Kabatereine N, Olsen A, Magnussen P, 2008. Malaria and hookworm infections in relation to haemoglobin and serum ferritin levels in pregnancy in Masindi district, western Uganda. Trans R Soc Trop Med Hyg 102: 130–136.
Muhangi L, Woodburn P, Omara M, Omoding N, Kizito D, Mpairwe H, Nabulime J, Ameke C, Morison LA, Elliott AM, 2007. Associations between mild-to-moderate anaemia in pregnancy and helminth, malaria and HIV infection in Entebbe, Uganda. Trans R Soc Trop Med Hyg 101: 899–907.
Gyorkos TW, Gilbert NL, Larocque R, Casapia M, 2011. Trichuris and hookworm infections associated with anaemia during pregnancy. Trop Med Int Health 16: 531–537.
Labeaud AD, Malhotra I, King MJ, King CL, King CH, 2009. Do antenatal parasite infections devalue childhood vaccination? PLoS Negl Trop Dis 3: e442.
Elliott AM, Mawa PA, Webb EL, Nampijja M, Lyadda N, Bukusuba J, Kizza M, Namujju PB, Nabulime J, Ndibazza J, Muwanga M, Whitworth JA, 2010. Effects of maternal and infant co-infections, and of maternal immunisation, on the infant response to BCG and tetanus immunisation. Vaccine 29: 247–255.
Kurtis JD, Higashi A, Wu HW, Gundogan F, McDonald EA, Sharma S, PondTor S, Jarilla B, Sagliba MJ, Gonzal A, Olveda R, Acosta L, Friedman JF, 2011. Maternal schistosomiasis japonica is associated with maternal, placental, and fetal inflammation. Infect Immun 79: 1254–1261.
Malhotra I, Ouma JH, Wamachi A, Kioko J, Mungai P, Njzovu M, Kazura JW, King CL, 2003. Influence of maternal filariasis on childhood infection and immunity to Wuchereria bancrofti in Kenya. Infect Immun 71: 5231–5237.
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Results of studies on the associations of maternal helminth infection and malaria-helminth co-infection on birth outcomes have been mixed. A group of 696 pregnant women from the Kwale district in Kenya were recruited and tested for malaria and helminth infection at delivery. Birthweight was documented for 664 infants. A total of 42.7% of the mothers were infected with Plasmodium falciparum, 30.6% with Schistosoma haematobium, 36.2% with filariasis, 31.5% with hookworm, and 5.9% with Trichuris trichiura; co-infection was present in 46.7%. Low birthweight (LBW) (weight < 2,500 grams) was present in 15.4% of the offspring, and 8.3% had a weight z-score ≤ 2 SD below the World Health Organization mean. Only gravida, age, and locale had a significant association with LBW. The high prevalence of maternal infection coupled with a higher than expected percentage of LBW highlight a need for further investigation of the association of maternal co-infection with LBW.
Financial support: This study was supported by the National Institute of Child Health and Human Development and National Institute of Health (grant no. A1064687).
Authors' addresses: Jessica K. Fairley, Division of Infectious Diseases, Emory University School of Medicine, Medical Office Tower, Atlanta, GA, E-mail: jessica.fairley@emory.edu. Donal Bisanzio and Uriel Kitron, Department of Environmental Studies, Emory University, Math and Science Center, Atlanta, GA, E-mails: dbisanz@emory.edu and ukitron@emory.edu. Charles H. King, Peter Mungai, Christopher L. King, and Indu Malhotra, Center for Global Health and Diseases, Case Western Reserve University, Biomedical Research Building, Cleveland, OH, E-mails: chk@case.edu, plmungai@yahoo.com, christopher.king@emory.edu, and ijm@case.edu. Eric Muchiri, Division of Vector Borne Diseases, Nairobi, Kenya, E-mail: ericmmuchiri@gmail.com.
King CH, Dickman K, Tisch DJ, 2005. Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 365: 1561–1569.
Ashford RW, Craig PS, Oppenheimer SJ, 1992. Polyparasitism on the Kenya coast. 1. Prevalence, and association between parasitic infections. Ann Trop Med Parasitol 86: 671–679.
Ezeamama AE, McGarvey ST, Acosta LP, Zierler S, Manalo DL, Wu HW, Kurtis JD, Mor V, Olveda RM, Friedman JF, 2008. The synergistic effect of concomitant schistosomiasis, hookworm, and Trichuris infections on children's anemia burden. PLoS Negl Trop Dis 2: e245.
Brooker S, Akhwale W, Pullan R, Estambale B, Clarke SE, Snow RW, Hotez PJ, 2007. Epidemiology of Plasmodium-helminth co-infection in Africa: populations at risk, potential impact on anemia, and prospects for combining control. Am J Trop Med Hyg 77: 88–98.
Adegnika AA, Ramharter M, Agnandji ST, Ateba Ngoa U, Issifou S, Yazdanbahksh M, Kremsner PG, 2010. Epidemiology of parasitic co-infections during pregnancy in Lambarene, Gabon. Trop Med Int Health 15: 1204–1209.
Ndibazza J, Muhangi L, Akishule D, Kiggundu M, Ameke C, Oweka J, Kizindo R, Duong T, Kleinschmidt I, Muwanga M, Elliott AM, 2010. Effects of deworming during pregnancy on maternal and perinatal outcomes in Entebbe, Uganda: a randomized controlled trial. Clin Infect Dis 50: 531–540.
Navitsky RC, Dreyfuss ML, Shrestha J, Khatry SK, Stoltzfus RJ, Albonico M, 1998. Ancylostoma duodenale is responsible for hookworm infections among pregnant women in the rural plains of Nepal. J Parasitol 84: 647–651.
Friedman JF, Mital P, Kanzaria HK, Olds GR, Kurtis JD, 2007. Schistosomiasis and pregnancy. Trends Parasitol 23: 159–164.
Ndyomugyenyi R, Kabatereine N, Olsen A, Magnussen P, 2008. Efficacy of ivermectin and albendazole alone and in combination for treatment of soil-transmitted helminths in pregnancy and adverse events: a randomized open label controlled intervention trial in Masindi District, western Uganda. Am J Trop Med Hyg 79: 856–863.
Allen HE, Crompton DW, de Silva N, LoVerde PT, Olds GR, 2002. New policies for using anthelmintics in high risk groups. Trends Parasitol 18: 381–382.
Desai M, ter Kuile FO, Nosten F, McGready R, Asamoa K, Brabin B, Newman RD, 2007. Epidemiology and burden of malaria in pregnancy. Lancet Infect Dis 7: 93–104.
Steketee RW, Nahlen BL, Parise ME, Menendez C, 2001. The burden of malaria in pregnancy in malaria-endemic areas. Am J Trop Med Hyg 64: 28–35.
Yatich NJ, Jolly PE, Funkhouser E, Agbenyega T, Rayner JC, Ehiri JE, Turpin A, Stiles JK, Ellis WO, Jiang Y, Williams JH, 2010. The effect of malaria and intestinal helminth coinfection on birth outcomes in Kumasi, Ghana. Am J Trop Med Hyg 82: 28–34.
Egwunyenga AO, Ajayi JA, Nmorsi OP, Duhlinska-Popova DD, 2001. Plasmodium/intestinal helminth co-infections among pregnant Nigerian women. Mem Inst Oswaldo Cruz 96: 1055–1059.
Christian P, Khatry SK, West KP Jr, 2004. Antenatal anthelmintic treatment, birthweight, and infant survival in rural Nepal. Lancet 364: 981–983.
Larocque R, Casapia M, Gotuzzo E, MacLean JD, Soto JC, Rahme E, Gyorkos TW, 2006. A double-blind randomized controlled trial of antenatal mebendazole to reduce low birthweight in a hookworm-endemic area of Peru. Trop Med Int Health 11: 1485–1495.
Haider BA, Humayun Q, Bhutta ZA, 2009. Effect of administration of antihelminthics for soil transmitted helminths during pregnancy. Cochrane Database Syst Rev CD005547.
Malhotra I, Dent A, Mungai P, Wamachi A, Ouma JH, Narum DL, Muchiri E, Tisch DJ, King CL, 2009. Can prenatal malaria exposure produce an immune tolerant phenotype? A prospective birth cohort study in Kenya. PLoS Med 6: e1000116.
World Health Organization, UNICEF, 2004. Low Birthweight: Country, Regional and Global Estimates. Geneva: World Health Organization.
ACOG Committee on Practice Guidelines, 2008. ACOG Practice Bulletin No. 95: anemia in pregnancy. Obstet Gynecol 112: 201–207.
Hotez PJ, Brooker S, Bethony JM, Bottazzi ME, Loukas A, Xiao S, 2004. Hookworm infection. N Engl J Med 351: 799–807.
Friedman JF, Kanzaria HK, McGarvey ST, 2005. Human schistosomiasis and anemia: the relationship and potential mechanisms. Trends Parasitol 21: 386–392.
Ajanga A, Lwambo NJ, Blair L, Nyandindi U, Fenwick A, Brooker S, 2006. Schistosoma mansoni in pregnancy and associations with anaemia in northwest Tanzania. Trans R Soc Trop Med Hyg 100: 59–63.
Ndyomugyenyi R, Kabatereine N, Olsen A, Magnussen P, 2008. Malaria and hookworm infections in relation to haemoglobin and serum ferritin levels in pregnancy in Masindi district, western Uganda. Trans R Soc Trop Med Hyg 102: 130–136.
Muhangi L, Woodburn P, Omara M, Omoding N, Kizito D, Mpairwe H, Nabulime J, Ameke C, Morison LA, Elliott AM, 2007. Associations between mild-to-moderate anaemia in pregnancy and helminth, malaria and HIV infection in Entebbe, Uganda. Trans R Soc Trop Med Hyg 101: 899–907.
Gyorkos TW, Gilbert NL, Larocque R, Casapia M, 2011. Trichuris and hookworm infections associated with anaemia during pregnancy. Trop Med Int Health 16: 531–537.
Labeaud AD, Malhotra I, King MJ, King CL, King CH, 2009. Do antenatal parasite infections devalue childhood vaccination? PLoS Negl Trop Dis 3: e442.
Elliott AM, Mawa PA, Webb EL, Nampijja M, Lyadda N, Bukusuba J, Kizza M, Namujju PB, Nabulime J, Ndibazza J, Muwanga M, Whitworth JA, 2010. Effects of maternal and infant co-infections, and of maternal immunisation, on the infant response to BCG and tetanus immunisation. Vaccine 29: 247–255.
Kurtis JD, Higashi A, Wu HW, Gundogan F, McDonald EA, Sharma S, PondTor S, Jarilla B, Sagliba MJ, Gonzal A, Olveda R, Acosta L, Friedman JF, 2011. Maternal schistosomiasis japonica is associated with maternal, placental, and fetal inflammation. Infect Immun 79: 1254–1261.
Malhotra I, Ouma JH, Wamachi A, Kioko J, Mungai P, Njzovu M, Kazura JW, King CL, 2003. Influence of maternal filariasis on childhood infection and immunity to Wuchereria bancrofti in Kenya. Infect Immun 71: 5231–5237.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 451 | 376 | 127 |
Full Text Views | 387 | 13 | 0 |
PDF Downloads | 99 | 6 | 0 |