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Published in: Malaria Journal 1/2013

Open Access 01-12-2013 | Research

Ascaris co-infection does not alter malaria-induced anaemia in a cohort of Nigerian preschool children

Authors: Francisca A Abanyie, Courtney McCracken, Patrick Kirwan, Síle F Molloy, Samuel O Asaolu, Celia V Holland, Julie Gutman, Tracey J Lamb

Published in: Malaria Journal | Issue 1/2013

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Abstract

Background

Co-infection with malaria and intestinal parasites such as Ascaris lumbricoides is common. Malaria parasites induce a pro-inflammatory immune response that contributes to the pathogenic sequelae, such as malarial anaemia, that occur in malaria infection. Ascaris is known to create an anti-inflammatory immune environment which could, in theory, counteract the anti-malarial inflammatory immune response, minimizing the severity of malarial anaemia. This study examined whether Ascaris co-infection can minimize the severity of malarial anaemia.

Methods

Data from a randomized controlled trial on the effect of antihelminthic treatment in Nigerian preschool-aged (6–59 months) children conducted in 2006–2007 were analysed to examine the effect of malaria and Ascaris co-infection on anaemia severity. Children were enrolled and tested for malaria, helminths and anaemia at baseline, four, and eight months. Six hundred and ninety subjects were analysed in this study. Generalized linear mixed models were used to assess the relationship between infection status and Ascaris and Plasmodium parasite intensity on severity of anaemia, defined as a haemoglobin less than 11 g/dL.

Results

Malaria prevalence ranged from 35-78% over the course of this study. Of the malaria-infected children, 55% were co-infected with Ascaris at baseline, 60% were co-infected four months later and 48% were co-infected eight months later, underlining the persistent prevalence of malaria-nematode co-infections in this population. Over the course of the study the percentage of anaemic subjects in the population ranged between 84% at baseline and 77% at the eight-month time point. The odds of being anaemic were four to five times higher in children infected with malaria compared to those without malaria. Ascaris infection alone did not increase the odds of being anaemic, indicating that malaria was the main cause of anaemia in this population. There was no significant difference in the severity of anaemia between children singly infected with malaria and co-infected with malaria and Ascaris.

Conclusion

In this cohort of Nigerian preschool children, malaria infection was the major contributor to anaemia status. Ascaris co-infection neither exacerbated nor ameliorated the severity of malarial anaemia.
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Literature
1.
go back to reference WHO: World malaria report 2011. 2011, Geneva: World Health Organization WHO: World malaria report 2011. 2011, Geneva: World Health Organization
2.
go back to reference Snow RW, Omumbo JA, Lowe B, Molyneux CS, Obiero JO, Palmer A, Weber MW, Pinder M, Nahlen B, Obonyo C, Newbold C, Gupta S, Marsh K: Relation between severe malaria morbidity in children and level of Plasmodium falciparum transmission in Africa. Lancet. 1997, 349: 1650-1654. 10.1016/S0140-6736(97)02038-2.CrossRefPubMed Snow RW, Omumbo JA, Lowe B, Molyneux CS, Obiero JO, Palmer A, Weber MW, Pinder M, Nahlen B, Obonyo C, Newbold C, Gupta S, Marsh K: Relation between severe malaria morbidity in children and level of Plasmodium falciparum transmission in Africa. Lancet. 1997, 349: 1650-1654. 10.1016/S0140-6736(97)02038-2.CrossRefPubMed
3.
go back to reference Lamb TJ, Langhorne J: The severity of malarial anaemia in Plasmodium chabaudi infections of BALB/c mice is determined independently of the number of circulating parasites. MalarJ. 2008, 7: 68-10.1186/1475-2875-7-68.CrossRef Lamb TJ, Langhorne J: The severity of malarial anaemia in Plasmodium chabaudi infections of BALB/c mice is determined independently of the number of circulating parasites. MalarJ. 2008, 7: 68-10.1186/1475-2875-7-68.CrossRef
4.
go back to reference Price RN, Simpson JA, Nosten F, Luxemburger C, Hkirjaroen L, ter Kuile F, Chongsuphajaisiddhi T, White NJ: Factors contributing to anemia after uncomplicated falciparum malaria. AmJTrop Med Hyg. 2001, 65: 614-622. Price RN, Simpson JA, Nosten F, Luxemburger C, Hkirjaroen L, ter Kuile F, Chongsuphajaisiddhi T, White NJ: Factors contributing to anemia after uncomplicated falciparum malaria. AmJTrop Med Hyg. 2001, 65: 614-622.
5.
go back to reference Chang KH, Stevenson MM: Malarial anaemia: mechanisms and implications of insufficient erythropoiesis during blood-stage malaria. Int J Parasitol. 2004, 34: 1501-1516. 10.1016/j.ijpara.2004.10.008.CrossRefPubMed Chang KH, Stevenson MM: Malarial anaemia: mechanisms and implications of insufficient erythropoiesis during blood-stage malaria. Int J Parasitol. 2004, 34: 1501-1516. 10.1016/j.ijpara.2004.10.008.CrossRefPubMed
6.
go back to reference Jakeman GN, Saul A, Hogarth WL, Collins WE: Anaemia of acute malaria infections in non-immune patients primarily results from destruction of uninfected erythrocytes. Parasitology. 1999, 119 (Pt 2): 127-133.CrossRefPubMed Jakeman GN, Saul A, Hogarth WL, Collins WE: Anaemia of acute malaria infections in non-immune patients primarily results from destruction of uninfected erythrocytes. Parasitology. 1999, 119 (Pt 2): 127-133.CrossRefPubMed
7.
go back to reference Lamikanra AA, Brown D, Potocnik A, Casals-Pascual C, Langhorne J, Roberts DJ: Malarial anemia: of mice and men. Blood. 2007, 110: 18-28. 10.1182/blood-2006-09-018069.CrossRefPubMed Lamikanra AA, Brown D, Potocnik A, Casals-Pascual C, Langhorne J, Roberts DJ: Malarial anemia: of mice and men. Blood. 2007, 110: 18-28. 10.1182/blood-2006-09-018069.CrossRefPubMed
8.
go back to reference Dold C, Holland CV: Ascaris and ascariasis. Microbes Infect. 2011, 13: 632-637. 10.1016/j.micinf.2010.09.012.CrossRefPubMed Dold C, Holland CV: Ascaris and ascariasis. Microbes Infect. 2011, 13: 632-637. 10.1016/j.micinf.2010.09.012.CrossRefPubMed
9.
go back to reference Cooper PJ, Chico ME, Sandoval C, Espinel I, Guevara A, Kennedy MW, Urban JF, Griffin GE, Nutman TB: Human infection with Ascaris lumbricoides is associated with a polarized cytokine response. J Infect Dis. 2000, 182: 1207-1213. 10.1086/315830.CrossRefPubMed Cooper PJ, Chico ME, Sandoval C, Espinel I, Guevara A, Kennedy MW, Urban JF, Griffin GE, Nutman TB: Human infection with Ascaris lumbricoides is associated with a polarized cytokine response. J Infect Dis. 2000, 182: 1207-1213. 10.1086/315830.CrossRefPubMed
10.
go back to reference Turner JD, Faulkner H, Kamgno J, Cormont F, Van Snick J, Else KJ, Grencis RK, Behnke JM, Boussinesq M, Bradley JE: Th2 cytokines are associated with reduced worm burdens in a human intestinal helminth infection. J Infect Dis. 2003, 188: 1768-1775. 10.1086/379370.CrossRefPubMed Turner JD, Faulkner H, Kamgno J, Cormont F, Van Snick J, Else KJ, Grencis RK, Behnke JM, Boussinesq M, Bradley JE: Th2 cytokines are associated with reduced worm burdens in a human intestinal helminth infection. J Infect Dis. 2003, 188: 1768-1775. 10.1086/379370.CrossRefPubMed
11.
go back to reference Geiger SM, Massara CL, Bethony J, Soboslay PT, Carvalho OS, Correa-Oliveira R: Cellular responses and cytokine profiles in Ascaris lumbricoides and Trichuris trichiura infected patients. Parasite Immunol. 2002, 24: 499-509. 10.1046/j.1365-3024.2002.00600.x.CrossRefPubMed Geiger SM, Massara CL, Bethony J, Soboslay PT, Carvalho OS, Correa-Oliveira R: Cellular responses and cytokine profiles in Ascaris lumbricoides and Trichuris trichiura infected patients. Parasite Immunol. 2002, 24: 499-509. 10.1046/j.1365-3024.2002.00600.x.CrossRefPubMed
12.
go back to reference Figueiredo CA, Barreto ML, Rodrigues LC, Cooper PJ, Silva NB, Amorim LD, Alcantara-Neves NM: Chronic intestinal helminth infections are associated with immune hyporesponsiveness and induction of a regulatory network. Infect Immun. 2010, 78: 3160-3167. 10.1128/IAI.01228-09.PubMedCentralCrossRefPubMed Figueiredo CA, Barreto ML, Rodrigues LC, Cooper PJ, Silva NB, Amorim LD, Alcantara-Neves NM: Chronic intestinal helminth infections are associated with immune hyporesponsiveness and induction of a regulatory network. Infect Immun. 2010, 78: 3160-3167. 10.1128/IAI.01228-09.PubMedCentralCrossRefPubMed
13.
go back to reference Turner JD, Jackson JA, Faulkner H, Behnke J, Else KJ, Kamgno J, Boussinesq M, Bradley JE: Intensity of intestinal infection with multiple worm species is related to regulatory cytokine output and immune hyporesponsiveness. J Infect Dis. 2008, 197: 1204-1212. 10.1086/586717.CrossRefPubMed Turner JD, Jackson JA, Faulkner H, Behnke J, Else KJ, Kamgno J, Boussinesq M, Bradley JE: Intensity of intestinal infection with multiple worm species is related to regulatory cytokine output and immune hyporesponsiveness. J Infect Dis. 2008, 197: 1204-1212. 10.1086/586717.CrossRefPubMed
14.
go back to reference Wammes LJ, Hamid F, Wiria AE, de Gier B, Sartono E, Maizels RM, Luty AJ, Fillie Y, Brice GT, Supali T, Smits HH, Yazdanbakhsh M: Regulatory T cells in human geohelminth infection suppress immune responses to BCG and Plasmodium falciparum. Eur J Immunol. 2010, 40: 437-442. 10.1002/eji.200939699.CrossRefPubMed Wammes LJ, Hamid F, Wiria AE, de Gier B, Sartono E, Maizels RM, Luty AJ, Fillie Y, Brice GT, Supali T, Smits HH, Yazdanbakhsh M: Regulatory T cells in human geohelminth infection suppress immune responses to BCG and Plasmodium falciparum. Eur J Immunol. 2010, 40: 437-442. 10.1002/eji.200939699.CrossRefPubMed
15.
go back to reference Hagel I, Cabrera M, Puccio F, Santaella C, Buvat E, Infante B, Zabala M, Cordero R, Di Prisco MC: Co-infection with Ascaris lumbricoides modulates protective immune responses against Giardia duodenalis in school Venezuelan rural children. Acta Trop. 2011, 117: 189-195. 10.1016/j.actatropica.2010.12.001.CrossRefPubMed Hagel I, Cabrera M, Puccio F, Santaella C, Buvat E, Infante B, Zabala M, Cordero R, Di Prisco MC: Co-infection with Ascaris lumbricoides modulates protective immune responses against Giardia duodenalis in school Venezuelan rural children. Acta Trop. 2011, 117: 189-195. 10.1016/j.actatropica.2010.12.001.CrossRefPubMed
16.
go back to reference Brutus L, Watier L, Hanitrasoamampionona V, Razanatsoarilala H, Cot M: Confirmation of the protective effect of Ascaris lumbricoides on Plasmodium falciparum infection: results of a randomized trial in Madagascar. AmJTrop Med Hyg. 2007, 77: 1091-1095. Brutus L, Watier L, Hanitrasoamampionona V, Razanatsoarilala H, Cot M: Confirmation of the protective effect of Ascaris lumbricoides on Plasmodium falciparum infection: results of a randomized trial in Madagascar. AmJTrop Med Hyg. 2007, 77: 1091-1095.
17.
go back to reference Nacher M, Singhasivanon P, Traore B, Vannaphan S, Gay F, Chindanond D, Franetich JF, Mazier D, Looareesuwan S: Helminth infections are associated with protection from cerebral malaria and increased nitrogen derivatives concentrations in Thailand. AmJTrop Med Hyg. 2002, 66: 304-309. Nacher M, Singhasivanon P, Traore B, Vannaphan S, Gay F, Chindanond D, Franetich JF, Mazier D, Looareesuwan S: Helminth infections are associated with protection from cerebral malaria and increased nitrogen derivatives concentrations in Thailand. AmJTrop Med Hyg. 2002, 66: 304-309.
18.
go back to reference Nacher M, Singhasivanon P, Silachamroon U, Treeprasertsuk S, Vannaphan S, Traore B, Gay F, Looareesuwan S: Helminth infections are associated with protection from malaria-related acute renal failure and jaundice in Thailand. AmJTrop Med Hyg. 2001, 65: 834-836. Nacher M, Singhasivanon P, Silachamroon U, Treeprasertsuk S, Vannaphan S, Traore B, Gay F, Looareesuwan S: Helminth infections are associated with protection from malaria-related acute renal failure and jaundice in Thailand. AmJTrop Med Hyg. 2001, 65: 834-836.
19.
go back to reference Kirwan P, Asaolu SO, Molloy SF, Abiona TC, Jackson AL, Holland CV: Patterns of soil-transmitted helminth infection and impact of four-monthly albendazole treatments in preschool children from semi-urban communities in Nigeria: a double-blind placebo-controlled randomised trial. BMC Infect Dis. 2009, 9: 20-10.1186/1471-2334-9-20.PubMedCentralCrossRefPubMed Kirwan P, Asaolu SO, Molloy SF, Abiona TC, Jackson AL, Holland CV: Patterns of soil-transmitted helminth infection and impact of four-monthly albendazole treatments in preschool children from semi-urban communities in Nigeria: a double-blind placebo-controlled randomised trial. BMC Infect Dis. 2009, 9: 20-10.1186/1471-2334-9-20.PubMedCentralCrossRefPubMed
20.
go back to reference Kirwan P, Jackson AL, Asaolu SO, Molloy SF, Abiona TC, Bruce MC, Ranford-Cartwright L, SM ON, Holland CV: Impact of repeated four-monthly anthelmintic treatment on Plasmodium infection in preschool children: a double-blind placebo-controlled randomized trial. BMC Infect Dis. 2010, 10: 277-10.1186/1471-2334-10-277.PubMedCentralCrossRefPubMed Kirwan P, Jackson AL, Asaolu SO, Molloy SF, Abiona TC, Bruce MC, Ranford-Cartwright L, SM ON, Holland CV: Impact of repeated four-monthly anthelmintic treatment on Plasmodium infection in preschool children: a double-blind placebo-controlled randomized trial. BMC Infect Dis. 2010, 10: 277-10.1186/1471-2334-10-277.PubMedCentralCrossRefPubMed
21.
go back to reference WHO:Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity. Vitamin and Mineral Nutrition Information System. 2011, Geneva: World Health Organization, WHO:Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity. Vitamin and Mineral Nutrition Information System. 2011, Geneva: World Health Organization,
22.
go back to reference Smith JL, Brooker S: Impact of hookworm infection and deworming on anaemia in non-pregnant populations: a systematic review. Trop Med Int Health. 2010, 15: 776-795. 10.1111/j.1365-3156.2010.02542.x.PubMedCentralCrossRefPubMed Smith JL, Brooker S: Impact of hookworm infection and deworming on anaemia in non-pregnant populations: a systematic review. Trop Med Int Health. 2010, 15: 776-795. 10.1111/j.1365-3156.2010.02542.x.PubMedCentralCrossRefPubMed
23.
go back to reference Carneiro I, Roca-Feltrer A, Griffin JT, Smith L, Tanner M, Schellenberg JA, Greenwood B, Schellenberg D: Age-patterns of malaria vary with severity, transmission intensity and seasonality in sub-Saharan Africa: a systematic review and pooled analysis. PLoS One. 2010, 5: e8988-10.1371/journal.pone.0008988.PubMedCentralCrossRefPubMed Carneiro I, Roca-Feltrer A, Griffin JT, Smith L, Tanner M, Schellenberg JA, Greenwood B, Schellenberg D: Age-patterns of malaria vary with severity, transmission intensity and seasonality in sub-Saharan Africa: a systematic review and pooled analysis. PLoS One. 2010, 5: e8988-10.1371/journal.pone.0008988.PubMedCentralCrossRefPubMed
24.
go back to reference Tshikuka JG, Scott ME, Gray-Donald K, Kalumba ON: Multiple infection with Plasmodium and helminths in communities of low and relatively high socio-economic status. Ann Trop Med Parasitol. 1996, 90: 277-293.PubMed Tshikuka JG, Scott ME, Gray-Donald K, Kalumba ON: Multiple infection with Plasmodium and helminths in communities of low and relatively high socio-economic status. Ann Trop Med Parasitol. 1996, 90: 277-293.PubMed
25.
go back to reference Worrall E, Basu S, Hanson K: Is malaria a disease of poverty? A review of the literature. Trop Med Int Health. 2005, 10: 1047-1059. 10.1111/j.1365-3156.2005.01476.x.CrossRefPubMed Worrall E, Basu S, Hanson K: Is malaria a disease of poverty? A review of the literature. Trop Med Int Health. 2005, 10: 1047-1059. 10.1111/j.1365-3156.2005.01476.x.CrossRefPubMed
26.
go back to reference Green HK, Sousa-Figueiredo JC, Basanez MG, Betson M, Kabatereine NB, Fenwick A, Stothard JR: Anaemia in Ugandan preschool-aged children: the relative contribution of intestinal parasites and malaria. Parasitology. 2011, 138: 1534-1545. 10.1017/S0031182011001016.CrossRefPubMed Green HK, Sousa-Figueiredo JC, Basanez MG, Betson M, Kabatereine NB, Fenwick A, Stothard JR: Anaemia in Ugandan preschool-aged children: the relative contribution of intestinal parasites and malaria. Parasitology. 2011, 138: 1534-1545. 10.1017/S0031182011001016.CrossRefPubMed
27.
go back to reference Magalhaes RJS, Clements ACA: Mapping the Risk of anaemia in preschool-age children: the contribution of malnutrition, malaria, and helminth infections in West Africa. PLoS Med. 2011, 8: e1000438-10.1371/journal.pmed.1000438.CrossRefPubMed Magalhaes RJS, Clements ACA: Mapping the Risk of anaemia in preschool-age children: the contribution of malnutrition, malaria, and helminth infections in West Africa. PLoS Med. 2011, 8: e1000438-10.1371/journal.pmed.1000438.CrossRefPubMed
28.
go back to reference Anah MU, Ikpeme OE, Etuk IS, Yong KE, Ibanga I, Asuquo BE: Worm infestation and anaemia among pre-school children of peasant farmers in Calabar, Nigeria. Niger J Clin Pract. 2008, 11: 220-224.PubMed Anah MU, Ikpeme OE, Etuk IS, Yong KE, Ibanga I, Asuquo BE: Worm infestation and anaemia among pre-school children of peasant farmers in Calabar, Nigeria. Niger J Clin Pract. 2008, 11: 220-224.PubMed
29.
go back to reference Melo GC, Reyes-Lecca RC, Vitor-Silva S, Monteiro WM, Martins M, Benzecry SG, Alecrim MG, Lacerda MV: Concurrent helminthic infection protects schoolchildren with Plasmodium vivax from anemia. PLoS One. 2010, 5: e11206-10.1371/journal.pone.0011206.PubMedCentralCrossRefPubMed Melo GC, Reyes-Lecca RC, Vitor-Silva S, Monteiro WM, Martins M, Benzecry SG, Alecrim MG, Lacerda MV: Concurrent helminthic infection protects schoolchildren with Plasmodium vivax from anemia. PLoS One. 2010, 5: e11206-10.1371/journal.pone.0011206.PubMedCentralCrossRefPubMed
30.
go back to reference Nkuo-Akenji TK, Chi PC, Cho JF, Ndamukong KK, Sumbele I: Malaria and helminth co-infection in children living in a malaria endemic setting of mount Cameroon and predictors of anemia. J Parasitol. 2006, 92: 1191-1195. 10.1645/GE-895R.1.CrossRefPubMed Nkuo-Akenji TK, Chi PC, Cho JF, Ndamukong KK, Sumbele I: Malaria and helminth co-infection in children living in a malaria endemic setting of mount Cameroon and predictors of anemia. J Parasitol. 2006, 92: 1191-1195. 10.1645/GE-895R.1.CrossRefPubMed
31.
go back to reference Stoltzfus RJ, Chwaya HM, Montresor A, Albonico M, Savioli L, Tielsch JM: Malaria, hookworms and recent fever are related to anemia and iron status indicators in 0- to 5-y old Zanzibari children and these relationships change with age. J Nutr. 2000, 130: 1724-1733.PubMed Stoltzfus RJ, Chwaya HM, Montresor A, Albonico M, Savioli L, Tielsch JM: Malaria, hookworms and recent fever are related to anemia and iron status indicators in 0- to 5-y old Zanzibari children and these relationships change with age. J Nutr. 2000, 130: 1724-1733.PubMed
32.
go back to reference Dufour C, Corcione A, Svahn J, Haupt R, Poggi V, Beka’ssy AN, Scime R, Pistorio A, Pistoia V: TNF-α and IFN-γ are overexpressed in the bone marrow of Fanconi anemia patients and TNF-α suppresses erythropoiesis in vitro. Blood. 2003, 102: 2053-2059. 10.1182/blood-2003-01-0114.CrossRefPubMed Dufour C, Corcione A, Svahn J, Haupt R, Poggi V, Beka’ssy AN, Scime R, Pistorio A, Pistoia V: TNF-α and IFN-γ are overexpressed in the bone marrow of Fanconi anemia patients and TNF-α suppresses erythropoiesis in vitro. Blood. 2003, 102: 2053-2059. 10.1182/blood-2003-01-0114.CrossRefPubMed
33.
go back to reference McDevitt MA, Xie J, Shanmugasundaram G, Griffith J, Liu A, McDonald C, Thuma P, Gordeuk VR, Metz CN, Mitchell R, Keefer J, David J, Leng L, Bucala R: A critical role for the host mediator macrophage migration inhibitory factor in the pathogenesis of malarial anemia. J Exp Med. 2006, 203: 1185-1196. 10.1084/jem.20052398.PubMedCentralCrossRefPubMed McDevitt MA, Xie J, Shanmugasundaram G, Griffith J, Liu A, McDonald C, Thuma P, Gordeuk VR, Metz CN, Mitchell R, Keefer J, David J, Leng L, Bucala R: A critical role for the host mediator macrophage migration inhibitory factor in the pathogenesis of malarial anemia. J Exp Med. 2006, 203: 1185-1196. 10.1084/jem.20052398.PubMedCentralCrossRefPubMed
34.
go back to reference Malaguarnera L, Imbesi RM, Pignatelli S, Simpore J, Malaguarnera M, Musumeci S: Increased levels of interleukin-12 in Plasmodium falciparum malaria: correlation with the severity of disease. Parasite Immunol. 2002, 24: 387-389. 10.1046/j.1365-3024.2002.00478.x.CrossRefPubMed Malaguarnera L, Imbesi RM, Pignatelli S, Simpore J, Malaguarnera M, Musumeci S: Increased levels of interleukin-12 in Plasmodium falciparum malaria: correlation with the severity of disease. Parasite Immunol. 2002, 24: 387-389. 10.1046/j.1365-3024.2002.00478.x.CrossRefPubMed
35.
go back to reference Mohan K, Stevenson MM: Interleukin-12 corrects severe anemia during blood-stage Plasmodium chabaudi AS in susceptible A/J mice. Exp Hematol. 1998, 26: 45-52.PubMed Mohan K, Stevenson MM: Interleukin-12 corrects severe anemia during blood-stage Plasmodium chabaudi AS in susceptible A/J mice. Exp Hematol. 1998, 26: 45-52.PubMed
36.
go back to reference Burgmann H, Looareesuwan S, Kapiotis S, Viravan C, Vanijanonta S, Hollenstein U, Wiesinger E, Presterl E, Winkler S, Graninger W: Serum levels of erythropoietin in acute Plasmodium falciparum malaria. AmJTrop Med Hyg. 1996, 54: 280-283. Burgmann H, Looareesuwan S, Kapiotis S, Viravan C, Vanijanonta S, Hollenstein U, Wiesinger E, Presterl E, Winkler S, Graninger W: Serum levels of erythropoietin in acute Plasmodium falciparum malaria. AmJTrop Med Hyg. 1996, 54: 280-283.
37.
go back to reference el Hassan AM, Saeed AM, Fandrey J, Jelkmann W: Decreased erythropoietin response in Plasmodium falciparum malaria-associated anaemia. Eur J Haematol. 1997, 59: 299-304.CrossRefPubMed el Hassan AM, Saeed AM, Fandrey J, Jelkmann W: Decreased erythropoietin response in Plasmodium falciparum malaria-associated anaemia. Eur J Haematol. 1997, 59: 299-304.CrossRefPubMed
38.
go back to reference Jelkmann W: Proinflammatory cytokines lowering erythropoietin production. J Interferon Cytokine Res. 1998, 18: 555-559. 10.1089/jir.1998.18.555.CrossRefPubMed Jelkmann W: Proinflammatory cytokines lowering erythropoietin production. J Interferon Cytokine Res. 1998, 18: 555-559. 10.1089/jir.1998.18.555.CrossRefPubMed
39.
go back to reference Chang KH, Tam M, Stevenson MM: Modulation of the course and outcome of blood-stage malaria by erythropoietin-induced reticulocytosis. J Infect Dis. 2004, 189: 735-743. 10.1086/381458.CrossRefPubMed Chang KH, Tam M, Stevenson MM: Modulation of the course and outcome of blood-stage malaria by erythropoietin-induced reticulocytosis. J Infect Dis. 2004, 189: 735-743. 10.1086/381458.CrossRefPubMed
40.
go back to reference Chang KH, Tam M, Stevenson MM: Inappropriately low reticulocytosis in severe malarial anemia correlates with suppression in the development of late erythroid precursors. Blood. 2004, 103: 3727-3735. 10.1182/blood-2003-08-2887.CrossRefPubMed Chang KH, Tam M, Stevenson MM: Inappropriately low reticulocytosis in severe malarial anemia correlates with suppression in the development of late erythroid precursors. Blood. 2004, 103: 3727-3735. 10.1182/blood-2003-08-2887.CrossRefPubMed
41.
go back to reference Othoro C, Lal AA, Nahlen B, Koech D, Orago AS, Udhayakumar V: A low interleukin-10 tumor necrosis factor-α ratio is associated with malaria anemia in children residing in a holoendemic malaria region in western Kenya. J Infect Dis. 1999, 179: 279-282. 10.1086/314548.CrossRefPubMed Othoro C, Lal AA, Nahlen B, Koech D, Orago AS, Udhayakumar V: A low interleukin-10 tumor necrosis factor-α ratio is associated with malaria anemia in children residing in a holoendemic malaria region in western Kenya. J Infect Dis. 1999, 179: 279-282. 10.1086/314548.CrossRefPubMed
42.
go back to reference Walther M, Jeffries D, Finney OC, Njie M, Ebonyi A, Deininger S, Lawrence E, Ngwa-Amambua A, Jayasooriya S, Cheeseman IH, Gomez-Escobar N, Okebe J, Conway DJ, Riley EM: Distinct roles for FOXP3 and FOXP3 CD4 T cells in regulating cellular immunity to uncomplicated and severe Plasmodium falciparum malaria. PLoS Pathog. 2009, 5: e1000364-10.1371/journal.ppat.1000364.PubMedCentralCrossRefPubMed Walther M, Jeffries D, Finney OC, Njie M, Ebonyi A, Deininger S, Lawrence E, Ngwa-Amambua A, Jayasooriya S, Cheeseman IH, Gomez-Escobar N, Okebe J, Conway DJ, Riley EM: Distinct roles for FOXP3 and FOXP3 CD4 T cells in regulating cellular immunity to uncomplicated and severe Plasmodium falciparum malaria. PLoS Pathog. 2009, 5: e1000364-10.1371/journal.ppat.1000364.PubMedCentralCrossRefPubMed
43.
go back to reference Walther M, Tongren JE, Andrews L, Korbel D, King E, Fletcher H, Andersen RF, Bejon P, Thompson F, Dunachie SJ, Edele F, de Souza JB, Sinden RE, Gilbert SC, Riley EM, Hill AV: pregulation of TGF-β, FOXP3, and CD4+CD25+ regulatory T cells correlates with more rapid parasite growth in human malaria infection. Immunity. 2005, 23: 287-296. 10.1016/j.immuni.2005.08.006.CrossRefPubMed Walther M, Tongren JE, Andrews L, Korbel D, King E, Fletcher H, Andersen RF, Bejon P, Thompson F, Dunachie SJ, Edele F, de Souza JB, Sinden RE, Gilbert SC, Riley EM, Hill AV: pregulation of TGF-β, FOXP3, and CD4+CD25+ regulatory T cells correlates with more rapid parasite growth in human malaria infection. Immunity. 2005, 23: 287-296. 10.1016/j.immuni.2005.08.006.CrossRefPubMed
44.
go back to reference Couper KN, Blount DG, Wilson MS, Hafalla JC, Belkaid Y, Kamanaka M, Flavell RA, de Souza JB, Riley EM: IL-10 from CD4CD25Foxp3CD127 adaptive regulatory T cells modulates parasite clearance and pathology during malaria infection. PLoS Pathog. 2008, 4: e1000004-10.1371/journal.ppat.1000004.PubMedCentralCrossRefPubMed Couper KN, Blount DG, Wilson MS, Hafalla JC, Belkaid Y, Kamanaka M, Flavell RA, de Souza JB, Riley EM: IL-10 from CD4CD25Foxp3CD127 adaptive regulatory T cells modulates parasite clearance and pathology during malaria infection. PLoS Pathog. 2008, 4: e1000004-10.1371/journal.ppat.1000004.PubMedCentralCrossRefPubMed
45.
go back to reference Rosario AP Fd, Lamb T, Spence P, Stephens R, Lang A, Roers A, Muller W, O’Garra A, Langhorne J: IL-27 promotes IL-10 production by effector Th1 CD4+ T cells: a critical mechanism for protection from severe immunopathology during malaria infection. J Immunol. 2012, 188: 1178-1190. 10.4049/jimmunol.1102755.CrossRef Rosario AP Fd, Lamb T, Spence P, Stephens R, Lang A, Roers A, Muller W, O’Garra A, Langhorne J: IL-27 promotes IL-10 production by effector Th1 CD4+ T cells: a critical mechanism for protection from severe immunopathology during malaria infection. J Immunol. 2012, 188: 1178-1190. 10.4049/jimmunol.1102755.CrossRef
46.
go back to reference Li C, Sanni LA, Omer F, Riley E, Langhorne J: Pathology of Plasmodium chabaudi chabaudi infection and mortality in interleukin-10-deficient mice are ameliorated by anti-tumor necrosis factor alpha and exacerbated by anti-transforming growth factor beta antibodies. Infect Immun. 2003, 71: 4850-4856. 10.1128/IAI.71.9.4850-4856.2003.PubMedCentralCrossRefPubMed Li C, Sanni LA, Omer F, Riley E, Langhorne J: Pathology of Plasmodium chabaudi chabaudi infection and mortality in interleukin-10-deficient mice are ameliorated by anti-tumor necrosis factor alpha and exacerbated by anti-transforming growth factor beta antibodies. Infect Immun. 2003, 71: 4850-4856. 10.1128/IAI.71.9.4850-4856.2003.PubMedCentralCrossRefPubMed
47.
go back to reference Omer FM, Riley EM: Transforming growth factor β production is inversely correlated with severity of murine malaria infection. J Exp Med. 1998, 188: 39-48. 10.1084/jem.188.1.39.PubMedCentralCrossRefPubMed Omer FM, Riley EM: Transforming growth factor β production is inversely correlated with severity of murine malaria infection. J Exp Med. 1998, 188: 39-48. 10.1084/jem.188.1.39.PubMedCentralCrossRefPubMed
48.
go back to reference Ojurongbe O, Adegbayi AM, Bolaji OS, Akindele AA, Adefioye OA, Adeyeba OA: Asymptomatic falciparum malaria and intestinal helminths co-infection among school children in Osogbo, Nigeria. J Res Med Sci. 2011, 16: 680-686.PubMedCentralPubMed Ojurongbe O, Adegbayi AM, Bolaji OS, Akindele AA, Adefioye OA, Adeyeba OA: Asymptomatic falciparum malaria and intestinal helminths co-infection among school children in Osogbo, Nigeria. J Res Med Sci. 2011, 16: 680-686.PubMedCentralPubMed
49.
go back to reference Leung AK, Chan KW: Iron deficiency anemia. Adv Pediatr. 2001, 48: 385-408.PubMed Leung AK, Chan KW: Iron deficiency anemia. Adv Pediatr. 2001, 48: 385-408.PubMed
50.
go back to reference Odunvbun ME, Okolo AA, Rahimy CM: Newborn screening for sickle cell disease in a Nigerian hospital. Public Health. 2008, 122: 1111-1116. 10.1016/j.puhe.2008.01.008.CrossRefPubMed Odunvbun ME, Okolo AA, Rahimy CM: Newborn screening for sickle cell disease in a Nigerian hospital. Public Health. 2008, 122: 1111-1116. 10.1016/j.puhe.2008.01.008.CrossRefPubMed
51.
go back to reference Akinyanju OO: A profile of sickle cell disease in Nigeria. Ann N Y Acad Sci. 1989, 565: 126-136. 10.1111/j.1749-6632.1989.tb24159.x.CrossRefPubMed Akinyanju OO: A profile of sickle cell disease in Nigeria. Ann N Y Acad Sci. 1989, 565: 126-136. 10.1111/j.1749-6632.1989.tb24159.x.CrossRefPubMed
52.
go back to reference Taylor SM, Parobek CM, Fairhurst RM: Haemoglobinopathies and the clinical epidemiology of malaria: a systematic review and meta-analysis. Lancet Infect Dis. 2012, 12: 457-468. 10.1016/S1473-3099(12)70055-5.PubMedCentralCrossRefPubMed Taylor SM, Parobek CM, Fairhurst RM: Haemoglobinopathies and the clinical epidemiology of malaria: a systematic review and meta-analysis. Lancet Infect Dis. 2012, 12: 457-468. 10.1016/S1473-3099(12)70055-5.PubMedCentralCrossRefPubMed
53.
go back to reference Onankpa B, Airede L, Paul I, Dorcas I: Pattern of pediatric HIV/AIDS: a five-year experience in a tertiary hospital. J Natl Med Assoc. 2008, 100: 821-825.PubMed Onankpa B, Airede L, Paul I, Dorcas I: Pattern of pediatric HIV/AIDS: a five-year experience in a tertiary hospital. J Natl Med Assoc. 2008, 100: 821-825.PubMed
54.
go back to reference Okechukwu AA, Okechukwu OI: Prevalence of paediatric HIV infection in Federal Capital Territory, Abuja. Niger J Med. 2011, 20: 409-413.PubMed Okechukwu AA, Okechukwu OI: Prevalence of paediatric HIV infection in Federal Capital Territory, Abuja. Niger J Med. 2011, 20: 409-413.PubMed
Metadata
Title
Ascaris co-infection does not alter malaria-induced anaemia in a cohort of Nigerian preschool children
Authors
Francisca A Abanyie
Courtney McCracken
Patrick Kirwan
Síle F Molloy
Samuel O Asaolu
Celia V Holland
Julie Gutman
Tracey J Lamb
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2013
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-12-1

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