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Published in: Malaria Journal 1/2012

Open Access 01-12-2012 | Research

Haemoglobin variants and Plasmodium falciparum malaria in children under five years of age living in a high and seasonal malaria transmission area of Burkina Faso

Authors: Edith C Bougouma, Alfred B Tiono, Alphonse Ouédraogo, Issiaka Soulama, Amidou Diarra, Jean-Baptiste Yaro, Espérance Ouédraogo, Souleymane Sanon, Amadou T Konaté, Issa Nébié, Nora L Watson, Megan Sanza, Tina JT Dube, Sodiomon B Sirima

Published in: Malaria Journal | Issue 1/2012

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Abstract

Background

Genetic factors play a key role in determining resistance/susceptibility to infectious disease. Susceptibility of the human host to malaria infection has been reported to be influenced by genetic factors, which could be confounders if not taken into account in the assessment of the efficacy of interventions against malaria. This study aimed to assess the relationship between haemoglobin genotypes and malaria in children under five years in a site being characterized for future malaria vaccine trials.

Methods

The study population consisted of 452 children living in four rural villages. Hb genotype was determined at enrolment. Clinical malaria incidence was evaluated over a one-year period using combined active and passive surveillance. Prevalence of infection was evaluated via bi-annual cross-sectional surveys. At each follow-up visit, children received a brief clinical examination and thick and thin blood films were prepared for malaria diagnosis. A clinical malaria was defined as Plasmodium falciparum parasitaemia >2,500 parasites/μl and axillary temperature ≥37.5°C or reported fever over the previous 24 hours.

Results

Frequencies of Hb genotypes were 73.2% AA; 15.0% AC; 8.2% AS; 2.2% CC; 1.1% CS and 0.2% SS. Prevalence of infection at enrolment ranged from 61.9%-54.1% among AA, AC and AS children. After one year follow-up, clinical malaria incidence (95% CI) (episodes per person-year) was 1.9 (1.7-2.0) in AA, 1.6 (1.4-2.1) in AC, and 1.7 (1.4-2.0) in AS children. AC genotype was associated with lower incidence of clinical malaria relative to AA genotype among children aged 1–2 years [rate ratio (95% CI) 0.66 (0.42-1.05)] and 2–3 years [rate ratio (95% CI) 0.37 (0.18-0.75)]; an association of opposite direction was however apparent among children aged 3–4 years. AS genotype was associated with lower incidence of clinical malaria relative to AA genotype among children aged 2–3 years [rate ratio (95% CI) 0.63 (0.40-1.01)].

Conclusions

In this cohort of children, AC or AS genotype was associated with lower risk of clinical malaria relative to AA genotype only among children aged one to three years. It would be advisable for clinical studies of malaria in endemic regions to consider haemoglobin gene differences as a potentially important confounder, particularly among younger children.
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Literature
1.
go back to reference Snow RW, Guerra CA, Noor AM, Myint HY, Hay SI: The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature. 2005, 434: 214-217. 10.1038/nature03342.PubMedCentralCrossRefPubMed Snow RW, Guerra CA, Noor AM, Myint HY, Hay SI: The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature. 2005, 434: 214-217. 10.1038/nature03342.PubMedCentralCrossRefPubMed
2.
go back to reference Le Hesran JY, Personne I, Personne P, Fievet N, Dubois B, Beyeme M, Boudin C, Cot M, Deloron P: Longitudinal study of Plasmodium falciparum infection and immune responses in infants with or without the sickle cell trait. Int J Epidemiol. 1999, 28: 793-798. 10.1093/ije/28.4.793.CrossRefPubMed Le Hesran JY, Personne I, Personne P, Fievet N, Dubois B, Beyeme M, Boudin C, Cot M, Deloron P: Longitudinal study of Plasmodium falciparum infection and immune responses in infants with or without the sickle cell trait. Int J Epidemiol. 1999, 28: 793-798. 10.1093/ije/28.4.793.CrossRefPubMed
3.
go back to reference Migot-Nabias F, Mombo LE, Luty AJ, Dubois B, Nabias R, Bisseye C, Millet P, Lu CY, Deloron P: Human genetic factors related to susceptibility to mild malaria in Gabon. Genes Immun. 2000, 1: 435-441. 10.1038/sj.gene.6363703.CrossRefPubMed Migot-Nabias F, Mombo LE, Luty AJ, Dubois B, Nabias R, Bisseye C, Millet P, Lu CY, Deloron P: Human genetic factors related to susceptibility to mild malaria in Gabon. Genes Immun. 2000, 1: 435-441. 10.1038/sj.gene.6363703.CrossRefPubMed
4.
go back to reference Lusingu JP, Vestergaard LS, Mmbando BP, Drakeley CJ, Jones C, Akida J, Savaeli ZX, Kitua AY, Lemnge MM, Theander TG: Malaria morbidity and immunity among residents of villages with different Plasmodium falciparum transmission intensity in North-Eastern Tanzania. Malar J. 2004, 3: 26-10.1186/1475-2875-3-26.PubMedCentralCrossRefPubMed Lusingu JP, Vestergaard LS, Mmbando BP, Drakeley CJ, Jones C, Akida J, Savaeli ZX, Kitua AY, Lemnge MM, Theander TG: Malaria morbidity and immunity among residents of villages with different Plasmodium falciparum transmission intensity in North-Eastern Tanzania. Malar J. 2004, 3: 26-10.1186/1475-2875-3-26.PubMedCentralCrossRefPubMed
5.
go back to reference Hill AV, Allsopp CE, Kwiatkowski D, Anstey NM, Twumasi P, Rowe PA, Bennett S, Brewster D, McMichael AJ, Greenwood BM: Common west African HLA antigens are associated with protection from severe malaria. Nature. 1991, 352: 595-600. 10.1038/352595a0.CrossRefPubMed Hill AV, Allsopp CE, Kwiatkowski D, Anstey NM, Twumasi P, Rowe PA, Bennett S, Brewster D, McMichael AJ, Greenwood BM: Common west African HLA antigens are associated with protection from severe malaria. Nature. 1991, 352: 595-600. 10.1038/352595a0.CrossRefPubMed
6.
go back to reference Haldane JBS: The rate of mutation of human genes. Cong Genet. 1949, 35: 267-273. Haldane JBS: The rate of mutation of human genes. Cong Genet. 1949, 35: 267-273.
7.
go back to reference Allison AC: The distribution of the sickle-cell trait in East Africa and elsewhere, and its apparent relationship to the incidence of subtertian malaria. Trans R Soc Trop Med Hyg. 1954, 48: 312-318. 10.1016/0035-9203(54)90101-7.CrossRefPubMed Allison AC: The distribution of the sickle-cell trait in East Africa and elsewhere, and its apparent relationship to the incidence of subtertian malaria. Trans R Soc Trop Med Hyg. 1954, 48: 312-318. 10.1016/0035-9203(54)90101-7.CrossRefPubMed
9.
go back to reference Rihet P, Flori L, Tall F, Traore AS, Fumoux F: Hemoglobin C is associated with reduced Plasmodium falciparum parasitemia and low risk of mild malaria attack. Hum Mol Genet. 2004, 13: 1-6. 10.1093/hmg/ddh084.CrossRefPubMed Rihet P, Flori L, Tall F, Traore AS, Fumoux F: Hemoglobin C is associated with reduced Plasmodium falciparum parasitemia and low risk of mild malaria attack. Hum Mol Genet. 2004, 13: 1-6. 10.1093/hmg/ddh084.CrossRefPubMed
10.
go back to reference Kreuels B, Kreuzberg C, Kobbe R, Ayim-Akonor M, Apiah-Thompson P, Thompson B, Ehmen C, Adjei S, Langefeld I, Adjei O, May J: Differing effects of HbS and HbC traits on uncomplicated falciparum malaria, anemia, and child growth. Blood. 2010, 115: 4551-4558. 10.1182/blood-2009-09-241844.CrossRefPubMed Kreuels B, Kreuzberg C, Kobbe R, Ayim-Akonor M, Apiah-Thompson P, Thompson B, Ehmen C, Adjei S, Langefeld I, Adjei O, May J: Differing effects of HbS and HbC traits on uncomplicated falciparum malaria, anemia, and child growth. Blood. 2010, 115: 4551-4558. 10.1182/blood-2009-09-241844.CrossRefPubMed
11.
go back to reference Williams TN, Mwangi TW, Wambua S, Alexander ND, Kortok M, Snow RW, Marsh K: Sickle cell trait and the risk of Plasmodium falciparum malaria and other childhood diseases. J Infect Dis. 2005, 192: 178-186. 10.1086/430744.PubMedCentralCrossRefPubMed Williams TN, Mwangi TW, Wambua S, Alexander ND, Kortok M, Snow RW, Marsh K: Sickle cell trait and the risk of Plasmodium falciparum malaria and other childhood diseases. J Infect Dis. 2005, 192: 178-186. 10.1086/430744.PubMedCentralCrossRefPubMed
12.
go back to reference Verra F, Bancone G, Avellino P, Blot I, Simpore J, Modiano D: Haemoglobin C and S in natural selection against Plasmodium falciparum malaria: a plethora or a single shared adaptive mechanism?. Parassitologia. 2007, 49: 209-213.PubMed Verra F, Bancone G, Avellino P, Blot I, Simpore J, Modiano D: Haemoglobin C and S in natural selection against Plasmodium falciparum malaria: a plethora or a single shared adaptive mechanism?. Parassitologia. 2007, 49: 209-213.PubMed
13.
go back to reference Gilles HM, Fletcher KA, Hendrickse RG, Lindner R, Reddy S, Allan N: Glucose-6-phosphate-dehydrogenase deficiency, sickling, and malaria in African children in South Western Nigeria. Lancet. 1967, 1: 138-140.CrossRefPubMed Gilles HM, Fletcher KA, Hendrickse RG, Lindner R, Reddy S, Allan N: Glucose-6-phosphate-dehydrogenase deficiency, sickling, and malaria in African children in South Western Nigeria. Lancet. 1967, 1: 138-140.CrossRefPubMed
14.
go back to reference Guinet F, Diallo DA, Minta D, Dicko A, Sissoko MS, Keita MM, Wellems TE, Doumbo O: A comparison of the incidence of severe malaria in Malian children with normal and C-trait hemoglobin profiles. Acta Trop. 1997, 68: 175-182. 10.1016/S0001-706X(97)00089-2.CrossRefPubMed Guinet F, Diallo DA, Minta D, Dicko A, Sissoko MS, Keita MM, Wellems TE, Doumbo O: A comparison of the incidence of severe malaria in Malian children with normal and C-trait hemoglobin profiles. Acta Trop. 1997, 68: 175-182. 10.1016/S0001-706X(97)00089-2.CrossRefPubMed
15.
go back to reference Jeremiah ZA, Jeremiah TA, Emelike FO: Frequencies of some human genetic markers and their association with Plasmodium falciparum malaria in the Niger Delta, Nigeria. J Vector Borne Dis. 2010, 47: 11-16.PubMed Jeremiah ZA, Jeremiah TA, Emelike FO: Frequencies of some human genetic markers and their association with Plasmodium falciparum malaria in the Niger Delta, Nigeria. J Vector Borne Dis. 2010, 47: 11-16.PubMed
16.
go back to reference Aggarwal R, Mishra A, Crochet P, Sirimanna P, Darzi A: Effect of caffeine and taurine on simulated laparoscopy performed following sleep deprivation. Br J Surg. 2011, 98: 1666-1672. 10.1002/bjs.7600.CrossRefPubMed Aggarwal R, Mishra A, Crochet P, Sirimanna P, Darzi A: Effect of caffeine and taurine on simulated laparoscopy performed following sleep deprivation. Br J Surg. 2011, 98: 1666-1672. 10.1002/bjs.7600.CrossRefPubMed
17.
go back to reference Modiano D, Luoni G, Sirima BS, Simpore J, Verra F, Konate A, Rastrelli E, Olivieri A, Calissano C, Paganotti GM, D'Urbano L, Sanou I, Sawadogo A, Modiano G, Coluzzi M: Haemoglobin C protects against clinical Plasmodium falciparum malaria. Nature. 2001, 414: 305-308. 10.1038/35104556.CrossRefPubMed Modiano D, Luoni G, Sirima BS, Simpore J, Verra F, Konate A, Rastrelli E, Olivieri A, Calissano C, Paganotti GM, D'Urbano L, Sanou I, Sawadogo A, Modiano G, Coluzzi M: Haemoglobin C protects against clinical Plasmodium falciparum malaria. Nature. 2001, 414: 305-308. 10.1038/35104556.CrossRefPubMed
18.
go back to reference Williams TN: How do hemoglobins S and C result in malaria protection?. J Infect Dis. 2011, 204: 1651-1653. 10.1093/infdis/jir640.CrossRefPubMed Williams TN: How do hemoglobins S and C result in malaria protection?. J Infect Dis. 2011, 204: 1651-1653. 10.1093/infdis/jir640.CrossRefPubMed
19.
go back to reference Williams TN, Mwangi TW, Roberts DJ, Alexander ND, Weatherall DJ, Wambua S, Kortok M, Snow RW, Marsh K: An immune basis for malaria protection by the sickle cell trait. PLoS Med. 2005, 2: e128-10.1371/journal.pmed.0020128.PubMedCentralCrossRefPubMed Williams TN, Mwangi TW, Roberts DJ, Alexander ND, Weatherall DJ, Wambua S, Kortok M, Snow RW, Marsh K: An immune basis for malaria protection by the sickle cell trait. PLoS Med. 2005, 2: e128-10.1371/journal.pmed.0020128.PubMedCentralCrossRefPubMed
20.
go back to reference Williams TN, Obaro SK: Sickle cell disease and malaria morbidity: a tale with two tails. Trends Parasitol. 2011, 27: 315-320. 10.1016/j.pt.2011.02.004.CrossRefPubMed Williams TN, Obaro SK: Sickle cell disease and malaria morbidity: a tale with two tails. Trends Parasitol. 2011, 27: 315-320. 10.1016/j.pt.2011.02.004.CrossRefPubMed
21.
go back to reference Ayi K, Turrini F, Piga A, Arese P: Enhanced phagocytosis of ring-parasitized mutant erythrocytes: a common mechanism that may explain protection against falciparum malaria in sickle trait and beta-thalassemia trait. Blood. 2004, 104: 3364-3371. 10.1182/blood-2003-11-3820.CrossRefPubMed Ayi K, Turrini F, Piga A, Arese P: Enhanced phagocytosis of ring-parasitized mutant erythrocytes: a common mechanism that may explain protection against falciparum malaria in sickle trait and beta-thalassemia trait. Blood. 2004, 104: 3364-3371. 10.1182/blood-2003-11-3820.CrossRefPubMed
22.
go back to reference Kennedy JR: Malaria: a vaccine concept based on sickle haemoglobin's augmentation of an innate autoimmune process to band 3. Int J Parasitol. 2001, 31: 1275-1277. 10.1016/S0020-7519(01)00236-3.CrossRefPubMed Kennedy JR: Malaria: a vaccine concept based on sickle haemoglobin's augmentation of an innate autoimmune process to band 3. Int J Parasitol. 2001, 31: 1275-1277. 10.1016/S0020-7519(01)00236-3.CrossRefPubMed
23.
go back to reference Roberts DJ, Williams TN: Haemoglobinopathies and resistance to malaria. Redox Rep. 2003, 8: 304-310. 10.1179/135100003225002998.CrossRefPubMed Roberts DJ, Williams TN: Haemoglobinopathies and resistance to malaria. Redox Rep. 2003, 8: 304-310. 10.1179/135100003225002998.CrossRefPubMed
24.
go back to reference Ferreira A, Marguti I, Bechmann I, Jeney V, Chora A, Palha NR, Rebelo S, Henri A, Beuzard Y, Soares MP: Sickle hemoglobin confers tolerance to Plasmodium infection. Cell. 2011, 145: 398-409. 10.1016/j.cell.2011.03.049.CrossRefPubMed Ferreira A, Marguti I, Bechmann I, Jeney V, Chora A, Palha NR, Rebelo S, Henri A, Beuzard Y, Soares MP: Sickle hemoglobin confers tolerance to Plasmodium infection. Cell. 2011, 145: 398-409. 10.1016/j.cell.2011.03.049.CrossRefPubMed
25.
go back to reference Ilboudo-Sanogo E, Tiono BA, Sagnon N, Cuzin Ouattara N, Nebie I, Sirima SB: Temporal dynamics of malaria transmission in two rural areas of Burkina Faso with two ecological differences. J Med Entomol. 2010, 47: 618-624. 10.1603/ME09102.CrossRefPubMed Ilboudo-Sanogo E, Tiono BA, Sagnon N, Cuzin Ouattara N, Nebie I, Sirima SB: Temporal dynamics of malaria transmission in two rural areas of Burkina Faso with two ecological differences. J Med Entomol. 2010, 47: 618-624. 10.1603/ME09102.CrossRefPubMed
26.
go back to reference Hackett CJ: On the origin of the human treponematoses (Pinta, Yaws, Endemic Syphilis and Venereal Syphilis). Bull World Health Organ. 1963, 29: 7-41.PubMedCentralPubMed Hackett CJ: On the origin of the human treponematoses (Pinta, Yaws, Endemic Syphilis and Venereal Syphilis). Bull World Health Organ. 1963, 29: 7-41.PubMedCentralPubMed
27.
go back to reference Diallo DA, Doumbo OK, Dicko A, Guindo A, Coulibaly D, Kayentao K, Djimde AA, Thera MA, Fairhurst RM, Plowe CV, Wellems TE: A comparison of anemia in hemoglobin C and normal hemoglobin A children with Plasmodium falciparum malaria. Acta Trop. 2004, 90: 295-299. 10.1016/j.actatropica.2004.02.005.CrossRefPubMed Diallo DA, Doumbo OK, Dicko A, Guindo A, Coulibaly D, Kayentao K, Djimde AA, Thera MA, Fairhurst RM, Plowe CV, Wellems TE: A comparison of anemia in hemoglobin C and normal hemoglobin A children with Plasmodium falciparum malaria. Acta Trop. 2004, 90: 295-299. 10.1016/j.actatropica.2004.02.005.CrossRefPubMed
28.
go back to reference Nebie I, Cuzin-Ouattara N, Diallo DA, Cousens SN, Theisen M, Corradin G, Traore AS, Esposito F: Humoral responses to defined malaria antigens in children living since birth under insecticide treated curtains in Burkina Faso. Acta Trop. 2003, 88: 17-25. 10.1016/S0001-706X(03)00189-X.CrossRefPubMed Nebie I, Cuzin-Ouattara N, Diallo DA, Cousens SN, Theisen M, Corradin G, Traore AS, Esposito F: Humoral responses to defined malaria antigens in children living since birth under insecticide treated curtains in Burkina Faso. Acta Trop. 2003, 88: 17-25. 10.1016/S0001-706X(03)00189-X.CrossRefPubMed
29.
go back to reference Cornille-Brogger R, Fleming AF, Kagan I, Matsushima T, Molineaux L: Abnormal haemoglobins in the Sudan savanna of Nigeria. II. Immunological response to malaria in normals and subjects with sickle cell trait. Ann Trop Med Parasitol. 1979, 73: 173-183.PubMed Cornille-Brogger R, Fleming AF, Kagan I, Matsushima T, Molineaux L: Abnormal haemoglobins in the Sudan savanna of Nigeria. II. Immunological response to malaria in normals and subjects with sickle cell trait. Ann Trop Med Parasitol. 1979, 73: 173-183.PubMed
31.
go back to reference Carnevale P, Bosseno MF, Lallemant M, Feingold J, Lissouba P, Molinier M, Mouchet J: Plasmodium falciparum malaria and sickle cell gene in the popular Republic of Congo. I. Relationship between parasitemia and sicke cell trait in Djoumouna. Ann Genet. 1981, 24: 100-104.PubMed Carnevale P, Bosseno MF, Lallemant M, Feingold J, Lissouba P, Molinier M, Mouchet J: Plasmodium falciparum malaria and sickle cell gene in the popular Republic of Congo. I. Relationship between parasitemia and sicke cell trait in Djoumouna. Ann Genet. 1981, 24: 100-104.PubMed
32.
go back to reference Doumbo O, Toure A, Coulibaly B, Koita O, Traore B, Dolo A, Diallo M, Diallo AN, Quilici M: Incidence of malaria and S hemoglobinopathy in the pediatric hospital milieu in Bamako, Mali. Med Trop (Mars). 1992, 52: 169-174. Doumbo O, Toure A, Coulibaly B, Koita O, Traore B, Dolo A, Diallo M, Diallo AN, Quilici M: Incidence of malaria and S hemoglobinopathy in the pediatric hospital milieu in Bamako, Mali. Med Trop (Mars). 1992, 52: 169-174.
33.
go back to reference Gendrel D, Kombila M, Nardou M, Gendrel C, Djouba F, Richard-Lenoble D: Protection against Plasmodium falciparum infection in children with hemoglobin S. Pediatr Infect Dis J. 1991, 10: 620-621. 10.1097/00006454-199108000-00013.CrossRefPubMed Gendrel D, Kombila M, Nardou M, Gendrel C, Djouba F, Richard-Lenoble D: Protection against Plasmodium falciparum infection in children with hemoglobin S. Pediatr Infect Dis J. 1991, 10: 620-621. 10.1097/00006454-199108000-00013.CrossRefPubMed
34.
go back to reference Bruce-Chwatt LJ: Immune relations between mother and child in African endemic malaria. Arch Fr Pediatr. 1985, 42 (Suppl 2): 911-916.PubMed Bruce-Chwatt LJ: Immune relations between mother and child in African endemic malaria. Arch Fr Pediatr. 1985, 42 (Suppl 2): 911-916.PubMed
35.
go back to reference Agarwal A, Guindo A, Cissoko Y, Taylor JG, Coulibaly D, Kone A, Kayentao K, Djimde A, Plowe CV, Doumbo O, Wellems TE, Diallo D: Hemoglobin C associated with protection from severe malaria in the Dogon of Mali, a West African population with a low prevalence of hemoglobin S. Blood. 2000, 96: 2358-2363.PubMed Agarwal A, Guindo A, Cissoko Y, Taylor JG, Coulibaly D, Kone A, Kayentao K, Djimde A, Plowe CV, Doumbo O, Wellems TE, Diallo D: Hemoglobin C associated with protection from severe malaria in the Dogon of Mali, a West African population with a low prevalence of hemoglobin S. Blood. 2000, 96: 2358-2363.PubMed
36.
go back to reference Mockenhaupt FP, Ehrhardt S, Cramer JP, Otchwemah RN, Anemana SD, Goltz K, Mylius F, Dietz E, Eggelte TA, Bienzle U: Hemoglobin C and resistance to severe malaria in Ghanaian children. J Infect Dis. 2004, 190: 1006-1009. 10.1086/422847.CrossRefPubMed Mockenhaupt FP, Ehrhardt S, Cramer JP, Otchwemah RN, Anemana SD, Goltz K, Mylius F, Dietz E, Eggelte TA, Bienzle U: Hemoglobin C and resistance to severe malaria in Ghanaian children. J Infect Dis. 2004, 190: 1006-1009. 10.1086/422847.CrossRefPubMed
37.
go back to reference Lell B, May J, Schmidt-Ott RJ, Lehman LG, Luckner D, Greve B, Matousek P, Schmid D, Herbich K, Mockenhaupt FP, Meyer CG, Bienzle U, Kremsner PG: The role of red blood cell polymorphisms in resistance and susceptibility to malaria. Clin Infect Dis. 1999, 28: 794-799. 10.1086/515193.CrossRefPubMed Lell B, May J, Schmidt-Ott RJ, Lehman LG, Luckner D, Greve B, Matousek P, Schmid D, Herbich K, Mockenhaupt FP, Meyer CG, Bienzle U, Kremsner PG: The role of red blood cell polymorphisms in resistance and susceptibility to malaria. Clin Infect Dis. 1999, 28: 794-799. 10.1086/515193.CrossRefPubMed
38.
go back to reference Aidoo M, Terlouw DJ, Kolczak MS, McElroy PD, ter Kuile FO, Kariuki S, Nahlen BL, Lal AA, Udhayakumar V: Protective effects of the sickle cell gene against malaria morbidity and mortality. Lancet. 2002, 359: 1311-1312. 10.1016/S0140-6736(02)08273-9.CrossRefPubMed Aidoo M, Terlouw DJ, Kolczak MS, McElroy PD, ter Kuile FO, Kariuki S, Nahlen BL, Lal AA, Udhayakumar V: Protective effects of the sickle cell gene against malaria morbidity and mortality. Lancet. 2002, 359: 1311-1312. 10.1016/S0140-6736(02)08273-9.CrossRefPubMed
39.
go back to reference Crompton PD, Traore B, Kayentao K, Doumbo S, Ongoiba A, Diakite SA, Krause MA, Doumtabe D, Kone Y, Weiss G, Huang CY, Doumbia S, Guindo A, Fairhurst RM, Miller LH, Pierce SK, Doumbo OK: Sickle cell trait is associated with a delayed onset of malaria: implications for time-to-event analysis in clinical studies of malaria. J Infect Dis. 2008, 198: 1265-1275. 10.1086/592224.PubMedCentralCrossRefPubMed Crompton PD, Traore B, Kayentao K, Doumbo S, Ongoiba A, Diakite SA, Krause MA, Doumtabe D, Kone Y, Weiss G, Huang CY, Doumbia S, Guindo A, Fairhurst RM, Miller LH, Pierce SK, Doumbo OK: Sickle cell trait is associated with a delayed onset of malaria: implications for time-to-event analysis in clinical studies of malaria. J Infect Dis. 2008, 198: 1265-1275. 10.1086/592224.PubMedCentralCrossRefPubMed
40.
41.
go back to reference Marsh K, Otoo L, Hayes RJ, Carson DC, Greenwood BM: Antibodies to blood stage antigens of Plasmodium falciparum in rural Gambians and their relation to protection against infection. Trans R Soc Trop Med Hyg. 1989, 83: 293-303. 10.1016/0035-9203(89)90478-1.CrossRefPubMed Marsh K, Otoo L, Hayes RJ, Carson DC, Greenwood BM: Antibodies to blood stage antigens of Plasmodium falciparum in rural Gambians and their relation to protection against infection. Trans R Soc Trop Med Hyg. 1989, 83: 293-303. 10.1016/0035-9203(89)90478-1.CrossRefPubMed
Metadata
Title
Haemoglobin variants and Plasmodium falciparum malaria in children under five years of age living in a high and seasonal malaria transmission area of Burkina Faso
Authors
Edith C Bougouma
Alfred B Tiono
Alphonse Ouédraogo
Issiaka Soulama
Amidou Diarra
Jean-Baptiste Yaro
Espérance Ouédraogo
Souleymane Sanon
Amadou T Konaté
Issa Nébié
Nora L Watson
Megan Sanza
Tina JT Dube
Sodiomon B Sirima
Publication date
01-12-2012
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2012
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-11-154

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