Sickle cell allele HBB-rs334(T) is associated with decreased risk of childhood Burkitt lymphoma in East Africa.
Journal
American journal of hematology
ISSN: 1096-8652
Titre abrégé: Am J Hematol
Pays: United States
ID NLM: 7610369
Informations de publication
Date de publication:
27 Nov 2023
27 Nov 2023
Historique:
revised:
30
09
2023
received:
07
08
2023
accepted:
23
10
2023
medline:
27
11
2023
pubmed:
27
11
2023
entrez:
27
11
2023
Statut:
aheadofprint
Résumé
Burkitt lymphoma (BL) is an aggressive B-cell lymphoma that significantly contributes to childhood cancer burden in sub-Saharan Africa. Plasmodium falciparum, which causes malaria, is geographically associated with BL, but the evidence remains insufficient for causal inference. Inference could be strengthened by demonstrating that mendelian genes known to protect against malaria-such as the sickle cell trait variant, HBB-rs334(T)-also protect against BL. We investigated this hypothesis among 800 BL cases and 3845 controls in four East African countries using genome-scan data to detect polymorphisms in 22 genes known to affect malaria risk. We fit generalized linear mixed models to estimate odds ratios (OR) and 95% confidence intervals (95% CI), controlling for age, sex, country, and ancestry. The ORs of the loci with BL and P. falciparum infection among controls were correlated (Spearman's ρ = 0.37, p = .039). HBB-rs334(T) was associated with lower P. falciparum infection risk among controls (OR = 0.752, 95% CI 0.628-0.9; p = .00189) and BL risk (OR = 0.687, 95% CI 0.533-0.885; p = .0037). ABO-rs8176703(T) was associated with decreased risk of BL (OR = 0.591, 95% CI 0.379-0.992; p = .00271), but not of P. falciparum infection. Our results increase support for the etiological correlation between P. falciparum and BL risk.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NCI NIH HHS
ID : HHSN261201100007I
Pays : United States
Organisme : NCI NIH HHS
ID : HHSN261201100063C
Pays : United States
Organisme : NHGRI NIH HHS
ID : Z01HG200362
Pays : United States
Organisme : HHS
Pays : United States
Informations de copyright
© 2023 Wiley Periodicals LLC. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.
Références
Mbulaiteye SM, Devesa SS. Burkitt lymphoma incidence in five continents. Hemato. 2022;3:434-453.
López C, Burkhardt B, Chan JKC, et al. Burkitt lymphoma. Nat Rev Dis Primers. 2022;8:78.
Carpenter LM, Newton R, Casabonne D, et al. Antibodies against malaria and Epstein-Barr virus in childhood Burkitt lymphoma: a case-control study in Uganda. Int J Cancer. 2008;122:1319-1323.
Mutalima N, Molyneux E, Jaffe H, et al. Associations between Burkitt lymphoma among children in Malawi and infection with HIV, EBV and malaria: results from a case-control study. PloS One. 2008;3:e2505.
Aka P, Vila MC, Jariwala A, et al. Endemic Burkitt lymphoma is associated with strength and diversity of Plasmodium falciparum malaria stage-specific antigen antibody response. Blood. 2013;122:629-635.
Derkach A, Otim I, Pfeiffer RM, et al. Associations between IgG reactivity to Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) antigens and Burkitt lymphoma in Ghana and Uganda case-control studies. EBioMedicine. 2019;39:358-368.
Johnston WT, Mutalima N, Sun D, et al. Relationship between Plasmodium falciparum malaria prevalence, genetic diversity and endemic Burkitt lymphoma in Malawi. Sci Rep. 2014;4:3741.
Arisue N, Chagaluka G, Palacpac NMQ, et al. Assessment of mixed Plasmodium falciparum sera5 infection in endemic Burkitt lymphoma: a case-control study in Malawi. Cancers (Basel). 2021;13:13.
Proceedings of the IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Epstein-Barr virus and Kaposi's sarcoma herpesvirus/human herpesvirus 8. IARC Monogr Eval Carcinog Risks Hum. 1997;70:1-492.
Thomas N, Dreval K, Gerhard DS, et al. Genetic subgroups inform on pathobiology in adult and pediatric Burkitt lymphoma. Blood. 2023;141:904-916.
Robbiani DF, Deroubaix S, Feldhahn N, et al. Plasmodium infection promotes genomic instability and AID-dependent B cell lymphoma. Cell. 2015;162:727-737.
Torgbor C, Awuah P, Deitsch K, Kalantari P, Duca KA, Thorley-Lawson DA. A multifactorial role for P. falciparum malaria in endemic Burkitt's lymphoma pathogenesis. PLoS Pathog. 2014;10:e1004170.
Mbulaiteye SM, Talisuna AO, Ogwang MD, McKenzie FE, Ziegler JL, Parkin DM. African Burkitt's lymphoma: could collaboration with HIV-1 and malaria programmes reduce the high mortality rate? Lancet. 2010;375:1661-1663.
Bouvard V, Baan RA, Grosse Y, et al. Carcinogenicity of malaria and of some polyomaviruses. Lancet Oncol. 2012;13:339-340.
Billo MA, Johnson ES, Doumbia SO, et al. Sickle cell trait protects against Plasmodium falciparum infection. Am J Epidemiol. 2012;176(suppl 7):S175-S185.
Williams AO. Haemoglobin genotypes, ABO blood groups, and Burkitt's tumour. J Med Genet. 1966;3:177-179.
Hesseling PB, Jam DT, Palmer DD, et al. Burkitt's lymphoma patients in Northwest Cameroon have a lower incidence of sickle cell trait (Hb AS) than healthy controls. S Afr Med J. 2016;106:10693.
Ahamed SG, Ibrahim UA, Kagu MB. Synergistic protective effect of sickle cell trait and blood group-O on the risk of endemic Burkitt's lymphoma. Gulf J Oncolog. 2018;1:11-16.
Pike MC, Morrow RH, Kisuule A, Mafigiri J. Burkitt's lymphoma and sickle cell trait. Br J Prev Soc Med. 1970;24:39-41.
Nkrumah FK, Perkins IV. Sickle cell trait, hemoglobin C trait, and Burkitt's lymphoma. Am J Trop Med Hyg. 1976;25:633-636.
Mulama DH, Bailey JA, Foley J, et al. Sickle cell trait is not associated with endemic Burkitt lymphoma: an ethnicity and malaria endemicity-matched case-control study suggests factors controlling EBV may serve as a predictive biomarker for this pediatric cancer. Int J Cancer. 2014;134:645-653.
Gouveia MH, Bergen AW, Borda V, et al. Genetic signatures of gene flow and malaria-driven natural selection in sub-Saharan populations of the “endemic Burkitt lymphoma belt”. PLoS Genet. 2019;15:e1008027.
Mackinnon MJ, Mwangi TW, Snow RW, Marsh K, Williams TN. Heritability of malaria in Africa. PLoS Med. 2005;2:e340.
Legason ID, Pfeiffer RM, Udquim KI, et al. Evaluating the causal link between malaria infection and endemic Burkitt lymphoma in northern Uganda: a mendelian randomization study. EBioMedicine. 2017;25:58-65.
Williams TN, Mwangi TW, Wambua S, et al. Negative epistasis between the malaria-protective effects of alpha+-thalassemia and the sickle cell trait. Nat Genet. 2005;37:1253-1257.
Gupta AK, Kirchner KA, Nicholson R, et al. Effects of alpha-thalassemia and sickle polymerization tendency on the urine-concentrating defect of individuals with sickle cell trait. J Clin Invest. 1991;88:1963-1968.
Peprah S, Ogwang MD, Kerchan P, et al. Risk factors for Burkitt lymphoma in east African children and minors: a case-control study in malaria-endemic regions in Uganda, Tanzania and Kenya. Int J Cancer. 2020;146:953-969.
Peprah S, Ogwang MD, Kerchan P, et al. Inverse association of falciparum positivity with endemic Burkitt lymphoma is robust in analyses adjusting for pre-enrollment malaria in the EMBLEM case-control study. Infect Agent Cancer. 2021;16:40.
Smith T, Felger I, Tanner M, Beck HP. Premunition in Plasmodium falciparum infection: insights from the epidemiology of multiple infections. Trans R Soc Trop Med Hyg. 1999;93(suppl 1):59-64.
Smith T, Beck HP, Kitua A, et al. Age dependence of the multiplicity of Plasmodium falciparum infections and of other malariological indices in an area of high endemicity. Trans R Soc Trop Med Hyg. 1999;93(suppl 1):15-20.
Broen K, Dickens J, Trangucci R, et al. Burkitt lymphoma risk shows geographic and temporal associations with Plasmodium falciparum infections in Uganda, Tanzania, and Kenya. Proc Natl Acad Sci U S A. 2023;120:e2211055120.
Maziarz M, Nabalende H, Otim I, et al. A cross-sectional study of asymptomatic Plasmodium falciparum infection burden and risk factors in general population children in 12 villages in northern Uganda. Malar J. 2018;17:240.
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.
Gouveia MH, Otim I, Ogwang MD, et al. Endemic Burkitt lymphoma in second-degree relatives in northern Uganda: in-depth genome-wide analysis suggests clues about genetic susceptibility. Leukemia. 2020;35:1209-1213.
Leal TP, Furlan VC, Gouveia MH, et al. NAToRA, a relatedness-pruning method to minimize the loss of dataset size in genetic and omics analyses. Comput Struct Biotechnol J. 2022;20:1821-1828.
Ramos E, Chen G, Shriner D, et al. Replication of genome-wide association studies (GWAS) loci for fasting plasma glucose in African-Americans. Diabetologia. 2011;54:783-788.
Horowitz HW. Fever of unknown origin or fever of too many origins? N Engl J Med. 2013;368:197-199.
Band G, Le QS, Clarke GM, et al. Insights into malaria susceptibility using genome-wide data on 17,000 individuals from Africa, Asia and Oceania. Nat Commun. 2019;10:5732.
Bousema T, Okell L, Felger I, Drakeley C. Asymptomatic malaria infections: detectability, transmissibility and public health relevance. Nat Rev Microbiol. 2014;12:833-840.
Jeffery GM, Eyles DE. The duration in the human host of infections with a Panama strain of Plasmodium falciparum. Am J Trop Med Hyg. 1954;3:219-224.
Wångdahl A, Bogale RT, Eliasson I, et al. Malaria parasite prevalence in sub-Saharan African migrants screened in Sweden: a cross-sectional study. Lancet Reg Health Eur. 2023;27:100581.
Westra HJ, Peters MJ, Esko T, et al. Systematic identification of trans eQTLs as putative drivers of known disease associations. Nat Genet. 2013;45:1238-1243.
Uyoga S, Macharia AW, Ndila CM, et al. The indirect health effects of malaria estimated from health advantages of the sickle cell trait. Nat Commun. 2019;10:856.
Rockett KA, Clarke GM, Fitzpatrick K, et al. Reappraisal of known malaria resistance loci in a large multicenter study. Nat Genet. 2014;46:1197-1204.
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.
Muriuki JM, Mentzer AJ, Mitchell R, et al. Malaria is a cause of iron deficiency in African children. Nat Med. 2021;27:653-658.
Etyang AO, Smeeth L, Cruickshank JK, Scott JA. The malaria-high blood pressure hypothesis. Circ Res. 2016;119:36-40.
Mawalla WF, Morrell L, Chirande LF, et al. Treatment delays in children and young adults with lymphoma: report from an East Africa lymphoma cohort study. Blood Adv. 2023;7(17):4962-4965.
Timmann C, Thye T, Vens M, et al. Genome-wide association study indicates two novel resistance loci for severe malaria. Nature. 2012;489:443-446.
Rowe JA, Handel IG, Thera MA, et al. 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.
Flint J, Hill AV, Bowden DK, et al. High frequencies of alpha-thalassaemia are the result of natural selection by malaria. Nature. 1986;321:744-750.
Zhong D, Koepfli C, Cui L, Yan G. Molecular approaches to determine the multiplicity of Plasmodium infections. Malar J. 2018;17:172.
Wesolowski A, Taylor AR, Chang HH, et al. Mapping malaria by combining parasite genomic and epidemiologic data. BMC Med. 2018;16:190.
de-The G, Geser A, Day NE, et al. Epidemiological evidence for causal relationship between Epstein-Barr virus and Burkitt's lymphoma from Ugandan prospective study. Nature. 1978;274:756-761.
Asito AS, Piriou E, Odada PS, et al. Elevated anti-Zta IgG levels and EBV viral load are associated with site of tumor presentation in endemic Burkitt's lymphoma patients: a case control study. Infect Agent Cancer. 2010;5:13.
Bull PC, Lowe BS, Kortok M, Molyneux CS, Newbold CI, Marsh K. Parasite antigens on the infected red cell surface are targets for naturally acquired immunity to malaria. Nat Med. 1998;4:358-360.
O'Donnell RA, de Koning-Ward TF, Burt RA, et al. Antibodies against merozoite surface protein (MSP)-1(19) are a major component of the invasion-inhibitory response in individuals immune to malaria. J Exp Med. 2001;193:1403-1412.
Goncalves BP, Huang CY, Morrison R, et al. Parasite burden and severity of malaria in Tanzanian children. N Engl J Med. 2014;370:1799-1808.
Rodriguez-Barraquer I, Arinaitwe E, Jagannathan P, et al. Quantifying heterogeneous malaria exposure and clinical protection in a cohort of Ugandan children. J Infect Dis. 2016;214:1072-1080.
Turner L, Lavstsen T, Mmbando BP, et al. IgG antibodies to endothelial protein C receptor-binding cysteine-rich interdomain region domains of Plasmodium falciparum erythrocyte membrane protein 1 are acquired early in life in individuals exposed to malaria. Infect Immun. 2015;83:3096-3103.
Eldh M, Hammar U, Arnot D, et al. Multiplicity of asymptomatic Plasmodium falciparum infections and risk of clinical malaria: a systematic review and pooled analysis of individual participant data. J Infect Dis. 2020;221:775-785.
Kidd P. Th1/Th2 balance: the hypothesis, its limitations, and implications for health and disease. Altern Med Rev. 2003;8:223-246.
Wipasa J, Suphavilai C, Okell LC, et al. Long-lived antibody and B cell memory responses to the human malaria parasites, Plasmodium falciparum and Plasmodium vivax. PLoS Pathog. 2010;6:e1000770.
Fowkes FJ, McGready R, Cross NJ, et al. New insights into acquisition, boosting, and longevity of immunity to malaria in pregnant women. J Infect Dis. 2012;206:1612-1621.
Drakeley CJ, Corran PH, Coleman PG, et al. Estimating medium- and long-term trends in malaria transmission by using serological markers of malaria exposure. Proc Natl Acad Sci U S A. 2005;102:5108-5113.
Howard M, O'Garra A. Biological properties of interleukin 10. Immunol Today. 1992;13:198-200.
Burdin N, Peronne C, Banchereau J, Rousset F. Epstein-Barr virus transformation induces B lymphocytes to produce human interleukin 10. J Exp Med. 1993;177:295-304.
Hsu DH, de Waal Malefyt R, Fiorentino DF, et al. Expression of interleukin-10 activity by Epstein-Barr virus protein BCRF1. Science. 1990;250:830-832.
Reynaldi A, Schlub TE, Chelimo K, et al. Impact of Plasmodium falciparum coinfection on longitudinal Epstein-Barr virus kinetics in Kenyan children. J Infect Dis. 2016;213:985-991.
Piriou E, Asito AS, Sumba PO, et al. Early age at time of primary Epstein-Barr virus infection results in poorly controlled viral infection in infants from Western Kenya: clues to the etiology of endemic Burkitt lymphoma. J Infect Dis. 2012;205:906-913.
Watier H, Auriault C, Capron A. Does Epstein-Barr virus infection confer selective advantage to malaria-infected children? Lancet. 1993;341:612-613.
Lam KM, Syed N, Whittle H, Crawford DH. Circulating Epstein-Barr virus-carrying B cells in acute malaria. Lancet. 1991;337:876-878.
Granai M, Lazzi S, Mancini V, et al. Burkitt lymphoma with a granulomatous reaction: an M1/Th1-polarised microenvironment is associated with controlled growth and spontaneous regression. Histopathology. 2022;80:430-442.
Band G, Leffler EM, Jallow M, et al. Malaria protection due to sickle haemoglobin depends on parasite genotype. Nature. 2022;602:106-111.