Ethnic differences in susceptibility to malaria: What have we learned from immuno-epidemiological studies in West Africa?

Acta Tropica

Volumn 146, Issue , 2015, Pages 152-156

  Arama, Charles ^a   Maiga, Bakary ^a   Dolo, Amagana ^a   Kouriba, Bourèma ^a   Traoré, Boubacar ^a   Crompton, Peter D ^b   Pierce, Susan K ^b   Troye Blomberg, Marita ^c   Miller, Louis H ^b   Doumbo, Ogobara K ^a  

^a Sociétés   (Mali)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

Ethnic; Fulani; Immunity; Malaria; Susceptibility; Sympatric

Indexed keywords

C REACTIVE PROTEIN; CYTOKINE; FC RECEPTOR;

DISEASE INCIDENCE; EPIDEMIOLOGY; ETHNICITY; HEALTH GEOGRAPHY; HOST-PARASITE INTERACTION; IMMUNITY; MALARIA;

ANTIGEN PRESENTING CELL; CELLULAR IMMUNITY; CLINICAL FEATURE; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; DISEASE TRANSMISSION; ETHNIC DIFFERENCE; HOST RESISTANCE; HUMAN; INFECTION RATE; INFECTION RESISTANCE; INFECTION RISK; INFECTION SENSITIVITY; MALARIA; REVIEW; SINGLE NUCLEOTIDE POLYMORPHISM; WEST AFRICAN; AFRICA; DISEASE PREDISPOSITION; EPIDEMIOLOGY; ETHNIC GROUP; ETHNOLOGY; GENETIC VARIABILITY; GENETICS; HOST PARASITE INTERACTION; MALARIA FALCIPARUM; PATHOGENICITY; PLASMODIUM FALCIPARUM;

WEST AFRICA;

PLASMODIUM FALCIPARUM;

AFRICA, WESTERN; DISEASE SUSCEPTIBILITY; EPIDEMIOLOGIC STUDIES; ETHNIC GROUPS; GENETIC VARIATION; HOST-PARASITE INTERACTIONS; HUMANS; MALARIA, FALCIPARUM; PLASMODIUM FALCIPARUM;

EID: 84926369052     PISSN: 0001706X     EISSN: 18736254     Source Type: Journal    
DOI: 10.1016/j.actatropica.2015.03.023     Document Type: Review

References (54)

1. Alkadarou T., Musa A., Alkadarou A., Mahfouz M.S., Troye-Blomberg M., Elhassan A.M., Elhassan I.M. Immunological characteristics of hyperreactive malarial splenomegaly syndrome in Sudanese patients. J. Trop. Med. 2013, 2013:961051.
2. Anderson B., Vullo C. Did malaria select for primary adult lactase deficiency?. Gut 1994, 35:1487-1489.
3. Arama C., Giusti P., Bostrom S., Dara V., Traore B., Dolo A., Doumbo O., Varani S., Troye-Blomberg M. Interethnic differences in antigen-presenting cell activation and TLR responses in Malian children during Plasmodium falciparum malaria. PLoS ONE 2011, 6:e18319.
4. Bereczky S., Dolo A., Maiga B., Hayano M., Granath F., Montgomery S.M., Daou M., Arama C., Troye-Blomberg M., Doumbo O.K., Farnert A. Spleen enlargement and genetic diversity of Plasmodium falciparum infection in two ethnic groups with different malaria susceptibility in Mali, West Africa. Trans. R. Soc. Trop. Med. Hyg. 2006, 100:248-257.
5. Bersaglieri T., Sabeti P.C., Patterson N., Vanderploeg T., Schaffner S.F., Drake J.A., Rhodes M., Reich D.E., Hirschhorn J.N. Genetic signatures of strong recent positive selection at the lactase gene. Am. J. Hum. Genet. 2004, 74:1111-1120.
6. Bolad A., Farouk S.E., Israelsson E., Dolo A., Doumbo O.K., Nebie I., Maiga B., Kouriba B., Luoni G., Sirima B.S., Modiano D., Berzins K., Troye-Blomberg M. Distinct interethnic differences in immunoglobulin G class/subclass and immunoglobulin M antibody responses to malaria antigens but not in immunoglobulin G responses to nonmalarial antigens in sympatric tribes living in West Africa. Scand. J. Immunol. 2005, 61:380-386.
7. Bostrom S., Giusti P., Arama C., Persson J.O., Dara V., Traore B., Dolo A., Doumbo O., Troye-Blomberg M. Changes in the levels of cytokines, chemokines and malaria-specific antibodies in response to Plasmodium falciparum infection in children living in sympatry in Mali. Malar. J. 2012, 11:109. 10.1186/1475-2875-11-109.
8. Bryceson A.D., Fleming A.F., Edington G.M. Splenomegaly in Northern Nigeria. Acta Trop. 1976, 33:185-214.
9. Cherif M.K., Sanou G.S., Maiga B., Israelsson E., Ouedraogo A.L., Bougouma E.C., Diarra A., Ouedraogo A., Ouattara A.S., Troye-Blomberg M., Dolo A., Cavanagh D.R., Theisen M., Modiano D., Sirima S.B., Nebie I. FcgammaRIIa polymorphism and anti-malaria-specific IgG and IgG subclass responses in populations differing in susceptibility to malaria in Burkina Faso. Scand. J. Immunol. 2012, 75:606-613.
10. Creasey A., Giha H., Hamad A.A., El Hassan I.M., Theander T.G., Arnot D.E. Eleven years of malaria surveillance in a Sudanese village highlights unexpected variation in individual disease susceptibility and outbreak severity. Parasitology 2004, 129:263-271.
11. Dolo A., Modiano D., Maiga B., Daou M., Dolo G., Guindo H., Ba M., Maiga H., Coulibaly D., Perlman H., Blomberg M.T., Toure Y.T., Coluzzi M., Doumbo O. Difference in susceptibility to malaria between two sympatric ethnic groups in Mali. Am. J. Trop. Med. Hyg. 2005, 72:243-248.
12. Dolo A., Coulibaly M., Maiga B., Daou M., Arama C., Troye-Blomberg M., Doumbo O. Humoral immune anti-Plasmodium falciparum AMA1 and MSP1 response in two ethnic groups living in sympatry in Mali. Bull. Soc. Pathol. Exot. 2012, 105:364-369.
13. Dolo A., Maiga B., Dara V., Tapily A., Tolo Y., Arama C., Daou M., Doumbo O. Place of malaria among febrile illnesses in two ethnic tribes living in sympatry in Mali from 1998 to 2008. Bull. Soc. Pathol. Exot. 2012, 105:377-383.
14. Dolo A., Maiga B., Tolo Y., Tapily A., Arama C., Daou M., Baby M., Traore B., Doumbo O. Relationship between malaria and anemia in two ethnic groups living in sympatry in Mali. Bull. Soc. Pathol. Exot. 2012, 105:370-376.
15. Doumbo S., Tran T.M., Sangala J., Li S., Doumtabe D., Kone Y., Traore A., Bathily A., Sogoba N., Coulibaly M.E., Huang C.Y., Ongoiba A., Kayentao K., Diallo M., Dramane Z., Nutman T.B., et al. Co-infection of long-term carriers of Plasmodium falciparum with Schistosoma haematobium enhances protection from febrile malaria: a prospective cohort study in Mali. PLoS Negl. Trop. Dis. 2014, 8:e3154.
16. Farouk S.E., Dolo A., Bereczky S., Kouriba B., Maiga B., Farnert A., Perlmann H., Hayano M., Montgomery S.M., Doumbo O.K., Troye-Blomberg M. Different antibody- and cytokine-mediated responses to Plasmodium falciparum parasite in two sympatric ethnic tribes living in Mali. Microbes Infect. 2005, 7:110-117.
17. Greenwood B.M., Groenendaal F., Bradley A.K., Greenwood A.M., Shenton F., Tulloch S., Hayes R. Ethnic differences in the prevalence of splenomegaly and malaria in The Gambia. Ann. Trop. Med. Parasitol. 1987, 81:345-354.
18. Greenwood B., Marsh K., Snow R. Why do some African children develop severe malaria?. Parasitol. Today 1991, 7:277-281.
19. Hartgers F.C., Yazdanbakhsh M. Co-infection of helminths and malaria: modulation of the immune responses to malaria. Parasite Immunol. 2006, 28:497-506.
20. Israelsson E., Vafa M., Maiga B., Lysen A., Iriemenam N.C., Dolo A., Doumbo O.K., Troye-Blomberg M., Berzins K. Differences in Fcgamma receptor IIa genotypes and IgG subclass pattern of anti-malarial antibodies between sympatric ethnic groups in Mali. Malar. J. 2008, 7:175. 10.1186/1475-2875-7-175.
21. Israelsson E., Ekstrom M., Nasr A., Dolo A., Kearsley S., Arambepola G., Homann M.V., Maiga B., Doumbo O.K., Elghazali G., Giha H.A., Troye-Blomberg M., Berzins K., Tornvall P. Marked differences in CRP genotype frequencies between the Fulani and sympatric ethnic groups in Africa. Malar. J. 2009, 8:136. 10.1186/1475-2875-8-136.
22. Israelsson E., Maiga B., Kearsley S., Dolo A., Homann M.V., Doumbo O.K., Troye-Blomberg M., Tornvall P., Berzins K. Cytokine gene haplotypes with a potential effect on susceptibility to malaria in sympatric ethnic groups in Mali. Infect. Genet. Evol. 2011, 11:1608-1615.
23. Krishnegowda G., Hajjar A.M., Zhu J., Douglass E.J., Uematsu S., Akira S., Woods A.S., Gowda D.C. Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: cell signaling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity. J. Biol. Chem. 2005, 280:8606-8616.
24. Kwiatkowski D.P. How malaria has affected the human genome and what human genetics can teach us about malaria. Am. J. Hum. Genet. 2005, 77:171-192.
25. Lokki A.I., Jarvela I., Israelsson E., Maiga B., Troye-Blomberg M., Dolo A., Doumbo O.K., Meri S., Holmberg V. Lactase persistence genotypes and malaria susceptibility in Fulani of Mali. Malar. J. 2011, 10:9. 10.1186/1475-2875-10-9.
26. Luoni G., Verra F., Arca B., Sirima B.S., Troye-Blomberg M., Coluzzi M., Kwiatkowski D., Modiano D. Antimalarial antibody levels and IL4 polymorphism in the Fulani of West Africa. Genes Immun. 2001, 2:411-414.
27. Maiga B., Dolo A., Toure O., Dara V., Tapily A., Campino S., Sepulveda N., Risley P., Silva N., Corran P., Rockett K.A., Kwiatkowski D., MalariaGEN Consortium, Clark T.G., Troye-Blomberg M., Doumbo O.K. Human candidate polymorphisms in sympatric ethnic groups differing in malaria susceptibility in Mali. PLOS ONE 2013, 8:e75675.
28. Maiga B., Dolo A., Campino S., Sepulveda N., Corran P., Rockett K.A., Troye-Blomberg M., Doumbo O.K., Clark T.G. Glucose-6-phosphate dehydrogenase polymorphisms and susceptibility to mild malaria in Dogon and Fulani, Mali. Malar. J. 2014, 13:270. 10.1186/1475-2875-13-270.
29. Maiga B., Dolo A., Toure O., Dara V., Tapily A., Campino S., Sepulveda N., Corran P., Rockett K., Clark T., Blomberg M.T., Doumbo O. Fcgamma Receptor IIa-H131R polymorphism and malaria susceptibility in sympatric ethnic groups, Fulani and Dogon of Mali. Scand. J. Immunol. 2014, 79:43-50.
30. Mangano V.D., Luoni G., Rockett K.A., Sirima B.S., Konate A., Forton J., Clark T.G., Bancone G., Sadighi Akha E., Kwiatkowski D.P., Modiano D. Interferon regulatory factor-1 polymorphisms are associated with the control of Plasmodium falciparum infection. Genes Immun. 2008, 9:122-129.
31. McCall M.B., Hopman J., Daou M., Maiga B., Dara V., Ploemen I., Nganou-Makamdop K., Niangaly A., Tolo Y., Arama C., Bousema J.T., van der Meer J.W., van der Ven A.J., Troye-Blomberg M., Dolo A., Doumbo O.K., et al. Early interferon-gamma response against Plasmodium falciparum correlates with interethnic differences in susceptibility to parasitemia between sympatric Fulani and Dogon in Mali. J. Infect. Dis. 2010, 201:142-152.
32. Mendez D., Hernaez M.L., Kamali A.N., Diez A., Puyet A., Bautista J.M. Differential carbonylation of cytoskeletal proteins in blood group O erythrocytes: potential role in protection against severe malaria. Infect. Genet. Evol. 2012, 12:1780-1787.
33. Merkenschlager M. Focus on epigenetic control of host defence: editorial. Immunology 2013, 139:275-276.
34. Modiano D., Petrarca V., Sirima B.S., Bosman A., Nebie I., Diallo D., Lamizana L., Esposito F., Coluzzi M. Plasmodium falciparum malaria in sympatric ethnic groups of Burkina Faso, west Africa. Parassitologia 1995, 37:255-259.
35. Modiano D., Petrarca V., Sirima B.S., Nebie I., Diallo D., Esposito F., Coluzzi M. Different response to Plasmodium falciparum malaria in west African sympatric ethnic groups. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:13206-13211.
36. Modiano D., Chiucchiuini A., Petrarca V., Sirima B.S., Luoni G., Perlmann H., Esposito F., Coluzzi M. Humoral response to Plasmodium falciparum Pf155/ring-infected erythrocyte surface antigen and Pf332 in three sympatric ethnic groups of Burkina Faso. Am. J. Trop. Med. Hyg. 1998, 58:220-224.
37. Modiano D., Chiucchiuini A., Petrarca V., Sirima B.S., Luoni G., Roggero M.A., Corradin G., Coluzzi M., Esposito F. Interethnic differences in the humoral response to non-repetitive regions of the Plasmodium falciparum circumsporozoite protein. Am. J. Trop. Med. Hyg. 1999, 61:663-667.
38. Modiano D., Luoni G., Petrarca V., Sodiomon Sirima B., De Luca M., Simpore J., Coluzzi M., Bodmer J.G., Modiano G. HLA class I in three West African ethnic groups: genetic distances from sub-Saharan and Caucasoid populations. Tissue Antigens 2001, 57:128-137.
39. Nasr A., Elghazali G., Giha H., Troye-Blomberg M., Berzins K. Interethnic differences in carriage of haemoglobin AS and Fcgamma receptor IIa (CD32) genotypes in children living in eastern Sudan. Acta Trop. 2008, 105:191-195.
40. Nasr A., Iriemenam N.C., Giha H.A., Balogun H.A., Anders R.F., Troye-Blomberg M., ElGhazali G., Berzins K. FcgammaRIIa (CD32) polymorphism and anti-malarial IgG subclass pattern among Fulani and sympatric ethnic groups living in eastern Sudan. Malar. J. 2009, 8:43. 10.1186/1475-2875-8-43.
41. Paganotti G.M., Babiker H.A., Modiano D., Sirima B.S., Verra F., Konate A., Ouedraogo A.L., Diarra A., Mackinnon M.J., Coluzzi M., Walliker D. Genetic complexity of Plasmodium falciparum in two ethnic groups of Burkina Faso with marked differences in susceptibility to malaria. Am. J. Trop. Med. Hyg. 2004, 71:173-178.
42. Parroche P., Lauw F.N., Goutagny N., Latz E., Monks B.G., Visintin A., Halmen K.A., Lamphier M., Olivier M., Bartholomeu D.C., Gazzinelli R.T., Golenbock D.T. Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:1919-1924.
43. Portugal S., Doumtabe D., Traore B., Miller L.H., Troye-Blomberg M., Doumbo O.K., Dolo A., Pierce S.K., Crompton P.D. B cell analysis of ethnic groups in Mali with differential susceptibility to malaria. Malar. J. 2012, 11:162. 10.1186/1475-2875-11-162.
44. Ranciaro A., Campbell M.C., Hirbo J.B., Ko W.Y., Froment A., Anagnostou P., Kotze M.J., Ibrahim M., Nyambo T., Omar S.A., Tishkoff S.A. Genetic origins of lactase persistence and the spread of pastoralism in Africa. Am. J. Hum. Genet. 2014, 94:496-510.
45. Rowe J.A., Handel I.G., Thera M.A., Deans A.M., Lyke K.E., Kone A., Diallo D.A., Raza A., Kai O., Marsh K., Plowe C.V., Doumbo O.K., Moulds J.M. Blood group O protects against severe Plasmodium falciparum malaria through the mechanism of reduced rosetting. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:17471-17476.
46. Sanou G.S., Tiendrebeogo R.W., Ouedraogo A.L., Diarra A., Ouedraogo A., Yaro J.B., Ouedraogo E., Verra F., Behr C., Troye-Blomberg M., Modiano D., Dolo A., Torcia M.G., Traore Y., Sirima S.B., Nebie I. Haematological parameters, natural regulatory CD4+ CD25+ FOXP3+ T cells and gammadelta T cells among two sympatric ethnic groups having different susceptibility to malaria in Burkina Faso. BMC Res. Notes 2012, 5:76. 10.1186/1756-0500-5-76.
47. Sharma S., DeOliveira R.B., Kalantari P., Parroche P., Goutagny N., Jiang Z., Chan J., Bartholomeu D.C., Lauw F., Hall J.P., Barber G.N., Gazzinelli R.T., Fitzgerald K.A., Golenbock D.T. Innate immune recognition of an AT-rich stem-loop DNA motif in the Plasmodium falciparum genome. Immunity 2011, 35:194-207.
48. Shio M.T., Eisenbarth S.C., Savaria M., Vinet A.F., Bellemare M.J., Harder K.W., Sutterwala F.S., Bohle D.S., Descoteaux A., Flavell R.A., Olivier M. Malarial hemozoin activates the NLRP3 inflammasome through Lyn and Syk kinases. PLoS Pathog. 2009, 5:e1000559.
49. Torcia M.G., Santarlasci V., Cosmi L., Clemente A., Maggi L., Mangano V.D., Verra F., Bancone G., Nebie I., Sirima B.S., Liotta F., Frosali F., Angeli R., Severini C., Sannella A.R., Bonini P., et al. Functional deficit of T regulatory cells in Fulani, an ethnic group with low susceptibility to Plasmodium falciparum malaria. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:646-651.
50. Tran T.M., Samal B., Kirkness E., Crompton P.D. Systems immunology of human malaria. Trends Parasitol. 2012, 28:248-257.
51. Vafa M., Maiga B., Berzins K., Hayano M., Bereczky S., Dolo A., Daou M., Arama C., Kouriba B., Farnert A., Doumbo O.K., Troye-Blomberg M. Associations between the IL-4-590 T allele and Plasmodium falciparum infection prevalence in asymptomatic Fulani of Mali. Microbes Infect. 2007, 9:1043-1048.
52. Vafa M., Israelsson E., Maiga B., Dolo A., Doumbo O.K., Troye-Blomberg M. Relationship between immunoglobulin isotype response to Plasmodium falciparum blood stage antigens and parasitological indexes as well as splenomegaly in sympatric ethnic groups living in Mali. Acta Trop. 2009, 109:12-16.
53. Vafa M., Maiga B., Israelsson E., Dolo A., Doumbo O.K., Troye-Blomberg M. Impact of the IL-4-590 C/T transition on the levels of Plasmodium falciparum specific IgE, IgG, IgG subclasses and total IgE in two sympatric ethnic groups living in Mali. Microbes Infect. 2009, 11:779-784.
54. Youngblood B., Hale J.S., Ahmed R. T-cell memory differentiation: insights from transcriptional signatures and epigenetics. Immunology 2013, 139:277-284.