de Silva NR, Brooker S, Hotez PJ, Montresor A, Engels D, Savioli L, 2003. Soil-transmitted helminth infections: updating the global picture. Trends Parasitol 19: 547–551.
Petney TN, Andrews RH, 1998. Multiparasites communities in animals and humans: frequency, structure and pathogenic significance. Int J Parasitol 28: 377–393.
Fleming AF, 1989. Tropical obstetrics and gynaecology. 1. Anaemia in pregnancy in tropical Africa. Joint Meeting of the Royal College of Obstetricians and Gynaecologists and the Royal Society of Tropical Medicine and Hygiene, Manson House, London. Trans R Soc Trop Med Hyg 83: 441–448.
Fleming AF, 1989. The etiology of severe malaria in pregnancy in Ndola, Zambia. Ann Trop Med Parasitol 83: 37–49.
Brabin BJ, 1983. An analysis of malaria in pregnancy in Africa. Bull World Health Organ 61: 1005–1016.
McGregor IA, 1984. Epidemiology, malaria and pregnancy. Am J Trop Med Hyg 33: 517–525.
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.
Steketee RW, Wirima JJ, Hightower AW, Heymann DL, Breman JG, 1996. The effect of malaria and malaria prevention in pregnancy on offspring birthweight, prematurity, and intrauterine growth retardation in rural Malawi. Am J Trop Med Hyg 55: 33–41.
Sullivan AD, Nyirenda T, Cullinan T, Taylor T, Harlow SD, James SA, Meshnick SR, 1999. Malaria infection during pregnancy: intrauterine growth retardation and preterm delivery in Malawi. J Infect Dis 179: 1580–1583.
Fried M, Duffy PE, 1996. Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science 272: 1502–1504.
Beeson JG, Rogerson SJ, Cooke BM, Reeder JC, Chai W, 2000. Adhesion of Plasmodium falciparum-infected erythrocytes to hyaluronic acid in placental malaria. Nat Med 6: 86–90.
Beck S, Mockenhaupt FP, Bienzle U, Eggelte TA, Thompson WN, Stark K, 2001. Multiplicity of Plasmodium falciparum infection in pregnancy. Am Soc Trop Med Hyg 65: 631–636.
Ndomugyenyi R, Kabatereine N, Olsen A, Magnusses P, 2002. Malaria and hookworm infections in relation to heamoglobin and serum ferritin levels in pregnancy in Masindi district, western Uganda. Trans R Soc Trop Med Hyg 102: 130–136.
Drake L, Korchev Y, Bashford L, Djamgoz M, Wakelin D, Ashall F, Bundy D, 1994. The major secreted product of the whipworm, Trichuris, is a pore-forming protein. Philos Trans R Soc Lond B Biol Sci 257: 255–261.
Hotez PJ, Brooker S, Bethony JM, Bottazzi ME, Loukas A, Xiao S, 2004. Hookworm infection. N Engl J Med 351: 799–807.
Cline BL, Little MD, Bartholomew RK, Halsey NA, 1984. Larvicidal activity of albendazole against Necator americanus larvae in human volunteers. Larvae in human volunteers. Am J Trop Hyg 33: 387–394.
Muhangi L, Woodburn P, Omara M, Omoding N, Kizito D, Mpairwe H, Nabulime J, Ameke C, Morison L, Elliot 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.
Parul C, Subarna KK, Keith PW, 2004. Antenatal anthelmintic treatment, birthweight, and infant survival in rural Nepal. Lancet 364: 981–983.
Egwunyenga AO, Ajayi JA, Nmorsi OPG, Duhlinska-Popova DD, 2001. Plasmodium/intestinal helminth coinfections among pregnant Nigerian women. Mem Inst Oswaldo Cruz, Rio de Janeiro 96:1055–1059.
Torre D, Speranza F, Martegani R, 2002. Role of proinflammatory and anti-inflammatory cytokines in the immune response to Plasmodium falciparum malaria. Lancet Infect Dis 2: 719–720.
Basavaraju SV, Schant P, 2006. Soil-transmitted helminths and Plasmodium falciparum malaria: epidemiology, clinical manifestations, and the role of nitric oxide in malaria and geohelminth coinfection. Do worms have a protective role in P. falciparum infection? Mt Sinai J Med 73: 1098–1105.
Mwangi TW, Bethony J, Brooker S, 2006. Malaria and helminth interactions in humans: an epidemiological viewpoint. Ann Trop Med Parasitol 100: 551–570.
Yazdanbakhsh M, Van der Biggelaar A, Maizels RM, 2001. Th2 responses without atopy: immunoregulation in chronic helminth infections and reduced allergic disease. Trends Immunol 22: 372–377.
Yatich NJ, Yi J, Agbenyega T, Turpin A, Rayner JC, Stiles JK, Ellis WO, Funkhouser E, Ehiri JE, Williams JH, Jolly PE, 2009. Malaria and intestinal helminth co-infection among pregnant women in Ghana: prevalence and risk factors. Am J Trop Med Hyg 80: 896–901.
25. World Health Organization, 1991. A guide for programme managers. Parasitology 103: 291–298.
Ayisi JG, van Eijk AM, ter Kuile FO, Kolczak MS, Otieno JA, Misore AO, Kager PA, Steketee RW, Nahlen BL, 2003. The effect of dual infection with HIV and malaria on pregnancy outcome in western Kenya. AIDS 17: 585–594.
World Health Organization, 1981. Development of Indicators for Monitoring Progress Towards Health for All by the Year 2000. (Health for All Series, Vol. 4). Geneva: World Health Organization.
Williams RL, Creasy RK, Cunningham GC, Hawes WE, Norris FD, Tashiro M, 1982. Fetal growth and perinatal viability in California. Obstet Gynecol 59: 624–632.
Hosmer D, Lemeshow S, 2000. Applied Logistic Regression. Second Edition. New York: Wiley and Sons Inc.
Bouyou-Akotet MK, Ionete-Collard DE, Mabika-Manfoumbi M, Matsiegu PB, Mavoungou E, Kombila M, 2003. Prevalence of Plasmodium falciparum infection in pregnant women in Gabon. Malar J 2: 18.
Ronald LA, Kenny SL, Klinkenberg E, Akoto AO, Boakye I, Barnish G, Donnelly M, 2006. Malaria and anemia among children in two communities of Kumasi, Ghana: a cross-sectional survey. Malar J 5: 105.
Marchesini P, Crawley J, 2004. Reducing the Burden of Malaria in Pregnancy. Geneva: Roll Back Malaria Department, World Health Organization.
Tako EA, Zhou A, Lohoue J, Leke R, Taylor DW, Leke R, 2005. Risk factors for placental malaria and its effect on pregnancy outcome in Yaounde, Cameroon. Am J Trop Med Hyg 72: 236–242.
Brabin BJ, 1991. The risks and severity of malaria in pregnant women. Applied Field Research in Malaria Reports 1: 21–25.
Shulman CE, Graham WJ, Jilo H, Lowe S, Obiero J, Snow RW, Marsh K, 1996. Malaria is an important cause of anemia in primigravid: evidence from a district hospital in coastal Kenya. Trans R Soc Trop Med Hyg 90: 535–539.
Desai M, ter Kuile FO, Nosten F, McGready R, Asamoa K, Brabin B, Newman R, 2007. Epidemiology and burden of malaria in pregnancy. Lancet Infect Dis 7: 93–104.
Nacher M, Singhasivanon P, Treeprasertsuk S, Vannaphan S, Traore B, Looareesuwan S, Gay F, 2002. Intestinal helminths and malnutrition are independently associated with protection from cerebral malaria in Thailand. Ann Trop Med Parasitol 96: 5–13.
Yazdani M, Tadbiri M, Shakeri S, 2004. Maternal hemoglobin level, prematurity, and low birth weight. Int J Gynaecol Obstet 85: 163–164.
Shah BK, Baig LA, 2005. Association of anemia with parasitic infestation in pregnant Nepalese women: results from a hospital-based study done in eastern Nepal. J Ayub Med Coll Abbottabad 1: 5–9.
de Silva NR, Sirisena JL, Gunasekera DP, Ismail MM, de Silva HJ, 1999. Effect of mebendazole therapy during pregnancy on birth outcome. Lancet 3: 1145–1149.
Migasena S, Gilles M, 1987. Hookworm infection. Beiliere's Clinical Trop Med and Com Dis 2: 617–627.
Gebremariam A, 2005. Factors predisposing to low birth weight in Jimma Hospital south western Ethiopia. East Afr Med J 82: 554–558.
World Health Organization, 2004. A Strategic Framework for Malaria Prevention and Control during Pregnancy in the African Region. Brazzaville: WHO Regional Office for Africa, AFR/MAL/04/01.
Mavalankar DV, Gray RH, Trivedi CR, Parikh VC, 1994. Risk factors for small for gestational age births in Ahmedabad, India. J Trop Pediatr 40: 285–290.
Berglund A, Lindmark G, 1998. The impact of obstetric risk factors and socioeconomic characteristics on utilization of antenatal care. J Public Health Med 20: 455–462.
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Abstract Views | 1271 | 1080 | 761 |
Full Text Views | 401 | 12 | 4 |
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This study was conducted to investigate the effect of Plasmodium falciparum and intestinal helminth coinfection on maternal anemia and birth outcomes. A cross-sectional study of 746 women who delivered in two hospitals in Kumasi was conducted. Data were collected using an investigator-administered questionnaire and from patients' medical records. Blood was collected for determination of P. falciparum and hemoglobin levels. Adverse pregnancy outcomes were high (44.6%). Coinfection (versus no infection) was associated with 3-fold increase in low birth weight. For women with anemia, coinfection was 2.6 times and 3.5 times as likely to result in preterm deliveries and small for gestational age infants. The odds of having anemia was increased almost 3-fold by coinfection. Coinfection (versus helminth only) resulted in increased risks of anemia, low birth weight, and small for gestational age infants. This study demonstrates that women with malaria and intestinal helminth coinfection are at particular risk of adverse birth outcomes.
Financial support: This research was supported by United States Agency for International Development grant LAG-G-00-96-90013-00 for the Peanut Collaborative Support Research Program and the University of Alabama at Birmingham Framework Program for Global Health, grant R25TW007501, Fogarty International Center, National Institutes of Health.
Authors' addresses: Nelly J. Yatich, Pauline E. Jolly, and Yi Jiang, Department of Epidemiology, School of Public Health, University of Alabama at Birmingham, Birmingham, AL, E-mails: yatich@uab.edu, jollyp@uab.edu, and yjiang@ms.soph.uab.edu. Ellen Funkhouser, Division of Preventive Medicine, School of Medicine, University of Alabama at Birmingham, Birmingham, AL, E-mail: emfunk@uab.edu. Tsiri Agbenyega, School of Medical Sciences, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana Kumasi, Ghana, E-mail: tsiri@ghana.com. Julian C. Rayner, Division of Infectious Diseases, School of Medicine, University of Alabama at Birmingham, Birmingham, AL, E-mail: jrayner@uab.edu. John E. Ehiri, Department of Maternal and Child Health, School of Public Health, University of Alabama at Birmingham, Birmingham, AL, E-mail: jehiri@email.arizona.edu. Archer Turpin, Komfo Anokye Teaching Hospital, Kumasi, Ghana, E-mail: Tsiri@ghana.com. Jonathan K. Stiles, Department of Microbiology, Biochemistry, and Immunology, Morehouse School of Medicine, Atlanta, GA, E-mail: jstiles@msm.edu. William O. Ellis, Department of Biochemistry, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana Kumasi, Ghana, E-mail:elliswo@yahoo.com. Jonathan H. Williams, College of Agricultural and Environmental Sciences, University of Georgia, Griffin, GA, E-mail: twillia@griffin.uga.edu.
de Silva NR, Brooker S, Hotez PJ, Montresor A, Engels D, Savioli L, 2003. Soil-transmitted helminth infections: updating the global picture. Trends Parasitol 19: 547–551.
Petney TN, Andrews RH, 1998. Multiparasites communities in animals and humans: frequency, structure and pathogenic significance. Int J Parasitol 28: 377–393.
Fleming AF, 1989. Tropical obstetrics and gynaecology. 1. Anaemia in pregnancy in tropical Africa. Joint Meeting of the Royal College of Obstetricians and Gynaecologists and the Royal Society of Tropical Medicine and Hygiene, Manson House, London. Trans R Soc Trop Med Hyg 83: 441–448.
Fleming AF, 1989. The etiology of severe malaria in pregnancy in Ndola, Zambia. Ann Trop Med Parasitol 83: 37–49.
Brabin BJ, 1983. An analysis of malaria in pregnancy in Africa. Bull World Health Organ 61: 1005–1016.
McGregor IA, 1984. Epidemiology, malaria and pregnancy. Am J Trop Med Hyg 33: 517–525.
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.
Steketee RW, Wirima JJ, Hightower AW, Heymann DL, Breman JG, 1996. The effect of malaria and malaria prevention in pregnancy on offspring birthweight, prematurity, and intrauterine growth retardation in rural Malawi. Am J Trop Med Hyg 55: 33–41.
Sullivan AD, Nyirenda T, Cullinan T, Taylor T, Harlow SD, James SA, Meshnick SR, 1999. Malaria infection during pregnancy: intrauterine growth retardation and preterm delivery in Malawi. J Infect Dis 179: 1580–1583.
Fried M, Duffy PE, 1996. Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science 272: 1502–1504.
Beeson JG, Rogerson SJ, Cooke BM, Reeder JC, Chai W, 2000. Adhesion of Plasmodium falciparum-infected erythrocytes to hyaluronic acid in placental malaria. Nat Med 6: 86–90.
Beck S, Mockenhaupt FP, Bienzle U, Eggelte TA, Thompson WN, Stark K, 2001. Multiplicity of Plasmodium falciparum infection in pregnancy. Am Soc Trop Med Hyg 65: 631–636.
Ndomugyenyi R, Kabatereine N, Olsen A, Magnusses P, 2002. Malaria and hookworm infections in relation to heamoglobin and serum ferritin levels in pregnancy in Masindi district, western Uganda. Trans R Soc Trop Med Hyg 102: 130–136.
Drake L, Korchev Y, Bashford L, Djamgoz M, Wakelin D, Ashall F, Bundy D, 1994. The major secreted product of the whipworm, Trichuris, is a pore-forming protein. Philos Trans R Soc Lond B Biol Sci 257: 255–261.
Hotez PJ, Brooker S, Bethony JM, Bottazzi ME, Loukas A, Xiao S, 2004. Hookworm infection. N Engl J Med 351: 799–807.
Cline BL, Little MD, Bartholomew RK, Halsey NA, 1984. Larvicidal activity of albendazole against Necator americanus larvae in human volunteers. Larvae in human volunteers. Am J Trop Hyg 33: 387–394.
Muhangi L, Woodburn P, Omara M, Omoding N, Kizito D, Mpairwe H, Nabulime J, Ameke C, Morison L, Elliot 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.
Parul C, Subarna KK, Keith PW, 2004. Antenatal anthelmintic treatment, birthweight, and infant survival in rural Nepal. Lancet 364: 981–983.
Egwunyenga AO, Ajayi JA, Nmorsi OPG, Duhlinska-Popova DD, 2001. Plasmodium/intestinal helminth coinfections among pregnant Nigerian women. Mem Inst Oswaldo Cruz, Rio de Janeiro 96:1055–1059.
Torre D, Speranza F, Martegani R, 2002. Role of proinflammatory and anti-inflammatory cytokines in the immune response to Plasmodium falciparum malaria. Lancet Infect Dis 2: 719–720.
Basavaraju SV, Schant P, 2006. Soil-transmitted helminths and Plasmodium falciparum malaria: epidemiology, clinical manifestations, and the role of nitric oxide in malaria and geohelminth coinfection. Do worms have a protective role in P. falciparum infection? Mt Sinai J Med 73: 1098–1105.
Mwangi TW, Bethony J, Brooker S, 2006. Malaria and helminth interactions in humans: an epidemiological viewpoint. Ann Trop Med Parasitol 100: 551–570.
Yazdanbakhsh M, Van der Biggelaar A, Maizels RM, 2001. Th2 responses without atopy: immunoregulation in chronic helminth infections and reduced allergic disease. Trends Immunol 22: 372–377.
Yatich NJ, Yi J, Agbenyega T, Turpin A, Rayner JC, Stiles JK, Ellis WO, Funkhouser E, Ehiri JE, Williams JH, Jolly PE, 2009. Malaria and intestinal helminth co-infection among pregnant women in Ghana: prevalence and risk factors. Am J Trop Med Hyg 80: 896–901.
25. World Health Organization, 1991. A guide for programme managers. Parasitology 103: 291–298.
Ayisi JG, van Eijk AM, ter Kuile FO, Kolczak MS, Otieno JA, Misore AO, Kager PA, Steketee RW, Nahlen BL, 2003. The effect of dual infection with HIV and malaria on pregnancy outcome in western Kenya. AIDS 17: 585–594.
World Health Organization, 1981. Development of Indicators for Monitoring Progress Towards Health for All by the Year 2000. (Health for All Series, Vol. 4). Geneva: World Health Organization.
Williams RL, Creasy RK, Cunningham GC, Hawes WE, Norris FD, Tashiro M, 1982. Fetal growth and perinatal viability in California. Obstet Gynecol 59: 624–632.
Hosmer D, Lemeshow S, 2000. Applied Logistic Regression. Second Edition. New York: Wiley and Sons Inc.
Bouyou-Akotet MK, Ionete-Collard DE, Mabika-Manfoumbi M, Matsiegu PB, Mavoungou E, Kombila M, 2003. Prevalence of Plasmodium falciparum infection in pregnant women in Gabon. Malar J 2: 18.
Ronald LA, Kenny SL, Klinkenberg E, Akoto AO, Boakye I, Barnish G, Donnelly M, 2006. Malaria and anemia among children in two communities of Kumasi, Ghana: a cross-sectional survey. Malar J 5: 105.
Marchesini P, Crawley J, 2004. Reducing the Burden of Malaria in Pregnancy. Geneva: Roll Back Malaria Department, World Health Organization.
Tako EA, Zhou A, Lohoue J, Leke R, Taylor DW, Leke R, 2005. Risk factors for placental malaria and its effect on pregnancy outcome in Yaounde, Cameroon. Am J Trop Med Hyg 72: 236–242.
Brabin BJ, 1991. The risks and severity of malaria in pregnant women. Applied Field Research in Malaria Reports 1: 21–25.
Shulman CE, Graham WJ, Jilo H, Lowe S, Obiero J, Snow RW, Marsh K, 1996. Malaria is an important cause of anemia in primigravid: evidence from a district hospital in coastal Kenya. Trans R Soc Trop Med Hyg 90: 535–539.
Desai M, ter Kuile FO, Nosten F, McGready R, Asamoa K, Brabin B, Newman R, 2007. Epidemiology and burden of malaria in pregnancy. Lancet Infect Dis 7: 93–104.
Nacher M, Singhasivanon P, Treeprasertsuk S, Vannaphan S, Traore B, Looareesuwan S, Gay F, 2002. Intestinal helminths and malnutrition are independently associated with protection from cerebral malaria in Thailand. Ann Trop Med Parasitol 96: 5–13.
Yazdani M, Tadbiri M, Shakeri S, 2004. Maternal hemoglobin level, prematurity, and low birth weight. Int J Gynaecol Obstet 85: 163–164.
Shah BK, Baig LA, 2005. Association of anemia with parasitic infestation in pregnant Nepalese women: results from a hospital-based study done in eastern Nepal. J Ayub Med Coll Abbottabad 1: 5–9.
de Silva NR, Sirisena JL, Gunasekera DP, Ismail MM, de Silva HJ, 1999. Effect of mebendazole therapy during pregnancy on birth outcome. Lancet 3: 1145–1149.
Migasena S, Gilles M, 1987. Hookworm infection. Beiliere's Clinical Trop Med and Com Dis 2: 617–627.
Gebremariam A, 2005. Factors predisposing to low birth weight in Jimma Hospital south western Ethiopia. East Afr Med J 82: 554–558.
World Health Organization, 2004. A Strategic Framework for Malaria Prevention and Control during Pregnancy in the African Region. Brazzaville: WHO Regional Office for Africa, AFR/MAL/04/01.
Mavalankar DV, Gray RH, Trivedi CR, Parikh VC, 1994. Risk factors for small for gestational age births in Ahmedabad, India. J Trop Pediatr 40: 285–290.
Berglund A, Lindmark G, 1998. The impact of obstetric risk factors and socioeconomic characteristics on utilization of antenatal care. J Public Health Med 20: 455–462.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 1271 | 1080 | 761 |
Full Text Views | 401 | 12 | 4 |
PDF Downloads | 151 | 13 | 4 |