African Environmental Pressures and Carcinogenesis: The Impact on The Lymphomas, the Leukemias, and Breast cancer

Main Article Content

Christopher K. Williams, MD FRCPC

Abstract

The African environment has for millennia been dominated by rampant agents of infections, of which malaria is among the best known, virtually uncontrolled, and associated with lifelong human struggles, ameliorarated by measures as socioeconomicaly affordable. This has led to the emergence of a variety of genetic aberrations, some of which are deleterious, resulting in major disease dysparities, including benign ones like sickle cell disease, and malignancies like the leukaemias, lymphomas, and breast cancer. They include the reduced incidence and the absence of its peak in acute lymphoblastic leukaemia in the first quinquennium of Nigerian children, which is otherwise typically seen in the children of high-income countries. Conversely is the observation in acute myelogenous leukaemia, with its chloroma-associated variant and its incidence peaking in the second quinquennium. This epidemiology is akin to the recent observation of acute myelogenous leukemia among sickle cell disease patients among the people of African descent in California, USA. Chloroma-associated acute myelogenous leukemia, and Burkitt lymphoma are linked with low socioeconomic status, an epidemiological feature that is shared with triple negative breast cancer patients in West Africa and the women of African descent in the United States. While a role for the malaria-associated genetic aberration underlying the Duffy null genotype is confirmed in the diversity of the triple negative breast cancer in the women of West Africa and those of African descent in the United States, it is conceivable, but not yet established in acute myelogenous leukemia. The zoonosis-linked human T-cell lymphotropic virus type 1 infection is associated with at least 17% of non-BL-non-Hodgkin lymphoma in form of its sentinel disease, the adult T-lymphoma/leukemia, but unexpicably much lower than the 50-60% of other major endemic zones of Japan and the African descendants of the Caribeean. This report describes the clinical, laboratory, and epidemiological features of leukemia and lymphoma cases diagnosed between 1982 and 1984 in the city of Ibadan, Nigeria, some of the features of which are reminiscent of the observations of Ludwig Gross’s experiments on environmental influences, such as malnutrition and infections, on animal leukemogenesis. These events are the consequences of the primordial pressures that have shaped human genetics and pathophysiology. Evidence provided in this study, indicating association of increasing socioeconomic status with increasing frequency of the c-ALL subtype, is indicative of the prospects for leukemogenesis of acute lymphoblastic leukemia and its epidemiology in Nigerians. Some findings reported here indicate the influence of the African genetic ancestry in the etiology of acute myelogenous leukemia, while socioecomic status is linked to the etiology of childhood acute lymphoblastic leukemia, as well as a variant of chronic lymphocytic leukemia, and the chloroma-associated acute myelogenous leukemia. These observations are suggestive of the existence of pathways to etiological discoveries in the leukemias. Observations reviewed in this paper reflect examples of changes that have occurred over the past 200 years in the societal perception of health challenges among the new-found communities of colonial Africa and the Americas - from the reductionistic connotations such as in the “virgin-soil theory” - towards that of social determinants of health.

Article Details

How to Cite
WILLIAMS, Christopher K.. African Environmental Pressures and Carcinogenesis: The Impact on The Lymphomas, the Leukemias, and Breast cancer. Medical Research Archives, [S.l.], v. 12, n. 2, mar. 2024. ISSN 2375-1924. Available at: <https://esmed.org/MRA/mra/article/view/5175>. Date accessed: 18 nov. 2024. doi: https://doi.org/10.18103/mra.v12i2.5175.
Section
Research Articles

References

1. Burkitt D. A sarcoma involving the jaws in African children. Br J Surgery. 1958;197:218-223.

2. Magrath I. Epidemiology: clues to pathogenesis of Burkitt lymphoma. British Journal of Haematology. 2012;156(6):744-756.

3. Epstein MA. Historical Background: Burkitt’s lymphoma and Epstein virus. In: Lenoir GM, O’Conor, G.T., Olweny, C.L.M., ed. A Human Cancer Model: Burkitt’s Lymphom. International Agency For Research On Cancer; 1985:chap 17-27.

4. Epstein MA, Barr Y. Cultivation in vitro of human lymphoblasts from Burkitt's malignant lymphoma. Lancet. 1964:252-3.

5. Zerbini M, Ernberg I. Can Epstein–Barr Virus Infect and Transform Acute lymphoblatic leukemia the B-Lymphocytes of Human Cord Blood? Journal of General Virology. 1983;64(3):539-547.

6. Lenoir GM, Preud'Homme JL, Bernheim A, Berger R. Correlation between immunoglobulin light chain expression and variant translocation in Burkitt's lymphoma. Nature. 1982;298(5873):474-476.

7. Della-Favera R, Bregni M, Erikson J, Patterson D, Gacute lymphoblatic leukemiao R, Croce C. Human c-myc oncogene is located on the region of chromosome 8 that is translocated in Burkitt's lymphoma cells. Proc Natl Acad Sci USA. 1982:7824-7827.

8. Taub R, Kirsch I, Morton C, et al. Translocation of the c-myc gene into the immunoglobulin heavy chain locus in human Burkitt lymphoma and murine plasmacytoma cells. Proceedings of the National Academy of Sciences. 1982;79(24):7837-7841.
9. Epstein M. Historical background; Burkitt's lymphoma and Epstein-Barr virus. IARC scientific publications. 1985;(60):17.

10. Thieme HR, Dhirasakdanon T, Han Z, Trevino R. Species decline and extinction: synergy of infectious disease and Acute lymphoblatic leukemiaee effect? Journal of Biological Dynamics. 2009;3(2-3):305-323.

11. Luzzatto L, ed. Part 3: Sickle Cell Anaemia in Tropical Africa. W.B. Saunders Company Ltd; 1981. Luzzatto L, ed. Hematology In Tropical Areas; vol 3.

12. Deisseroth A, Nienhuis A, Lawrence J, Giles R, Turner P, Ruddle FH. Chromosomal localization of human β globin gene on human chromosome 11 in somatic cell hybrids. Proceedings of the National Academy of Sciences. 1978;75(3):1456-1460.

13. Lebo R, Carrano A. Burkhart-Schultz K. Dozy AM, Yu LC, Kan YW: Assignment of human p-, y, and &globin genes to the short arm of chromosome. 11

14. Forget BG. Nucleotide sequence of human β globin messenger RNA. Hemoglobin. 1977;1(8):879-881.

15. Ingram VM. A specific chemical difference between the globins of normal human and sickle-cell anaemia haemoglobin. Nature. 1956;178(4537):792-794.

16. Luzzatto L. Genetics of red cells and susceptibility to malaria. 1979;

17. Luzzatto L, Nwachuku-Jarrett E, Reddy S. Increased sickling of parasitised erythrocytes as mechanism of resistance against malaria in the sickle-cell trait. The Lancet. 1970;295(7642): 319-322.

18. Friedman MJ. Erythrocytic mechanism of sickle cell resistance to malaria. Proceedings of the National Academy of Sciences. 1978;75 (4):1994-1997.

19. Roth Jr EF, Friedman M, Ueda Y, Tellez I, Trager W, Nagel RL. Sickling rates of human AS red cells infected in vitro with Plasmodium falciparum malaria. Science. 1978;202(4368): 650-652.

20. Hobbs MR, Udhayakumar V, Levesque MC, et al. A new NOS2 promoter polymorphism associated with increased nitric oxide production and protection from severe malaria in Tanzanian and Kenyan children. The Lancet. 2002;360(9344):1468-1475.

21. Cramer JP, Mockenhaupt FP, Ehrhardt S, et al. iNOS promoter variants and severe malaria in Ghanaian children. Tropical Medicine & International Health. 2004;9(10):1074-1080.

22. Tournamille C, Colin Y, Cartron JP, Le Van Kim C. Disruption of a GATA motif in the Duffy gene promoter abolishes erythroid gene expression in Duffy–negative individuals. Nature genetics. 1995;10(2):224-228.

23. Wink DA, Vodovotz Y, Laval J, Laval F, Dewhirst MW, Mitchell JB. The multifaceted roles of nitric oxide in cancer. Carcinogenesis. 1998;19(5):711-721.

24. Glynn SA, Boersma BJ, Dorsey TH, et al. Increased NOS2 predicts poor survival in estrogen receptor–negative breast cancer patients. The Journal of clinical investigation. 2010;120(11):3843-3854.

25. Bandyopadhyay S, Zhan R, Chaudhuri A, et al. Interaction of KAI1 on tumor cells with DARC on vascular endothelium leads to metastasis suppression. Nature medicine. 2006;12(8):933-938.

26. Poiesz BJ, Ruscetti FW, Gazdar AF, Bunn PA, Minna JD, Gacute lymphoblatic leukemiao RC. Detection and isolation of type C retrovirus particles from fresh and cultured lymphocytes of a patient with cutaneous T-cell lymphoma. Proceedings of the National Academy of Sciences. 1980;77(12):7415-7419.

27. Williams CK, Alabi GO, Junaid TA, et al. Human T cell leukaemia virus associated lymphoproliferative disease: report of two cases in Nigeria. Case Reports. Br Med J (Clin Res Ed). May 19 1984;288(6429):1495-6.

28. Lloyd PC. The city of Ibadan. CUP Archive; 1967.

29. Makinde OO. Housing: central city slums, a case study of Ibadan. Journal of Environment and Earth Science. 2012;2(9):21-31.

30. Edington G, Maclean CM. Incidence of the Burkitt tumour in Ibadan, western Nigeria. British medical journal. 1964;1(5378):264.

31. Osunkoya B. Trends of experimental cancer research in Nigeria: Cancer in Nigeria. Solanke TF, Osunkoya BO, Williams CKO, Agboola OO. Ibadan University Press, Publishing House, Ibadan; 1982.

32. Savage L. Former African cancer research powerhouse makes plans for a return to greatness. Journal of the National Cancer Institute. 2007;99(15):1144-1151.

33. Rettig RA. The story of the national cancer act of 1971. 1977.

34. Rettig RA. Cancer crusade: the story of the National Cancer Act of 1971. iUniverse; 2005.

35. DeVita VT, Chu E. A history of cancer chemotherapy. Cancer research. 2008;68(21): 8643-8653. doi:DOI: 10.1158/0008-5472.CAN-07-6611

36. Williams CKO. Barrier to successful management of breast cancer. In: Breast Cancer In Women Of African Descent. Breast Cancer In Women of African Descent. Springer; 2006.

37. Ultmann JE, Baxter MD, Lierman T. The Government and Cancer Medicine. In: Bast RC, Kufe DW, Pollock RE, Weichselbaum RR, Holland JF, Frei III E, eds. Cancer Medicine. 5 ed. B.C. Decker Inc.; 2000:1024-1034.

38. Oyo State: A Survey of Resources for Development. (1981).

39. Anonymous. World Bank Report: Nigeria: Country Economic Memorandum. 1981.

40. Williams CK, Bamgboye EA. Estimation of incidence of human leukaemia subtypes in an urban African population. Oncology. 1983; 40(6):381-6.

41. Beard C. Histopathological definition of Burkitt's tumor. Bull World Health Organ. 1969;40:601-607.

42. Greaves MF, Pegram SM, Chan L. Collaborative group study of the epidemiology of acute lymphoblastic leukaemia subtypes: background and first report. Leukemia Research. 1985;9(6):715.

43. Greaves MF, Colman SM, Beard ME, et al. Geographical distribution of acute lymphoblastic leukaemia subtypes: second report of the collaborative group study. Leukemia. Jan 1993;7(1):27-34.

44. Ritz J, Pesando JM, Notis-McConarty J, Lazarus H, Schlossman SF. A monoclonal antibody to human acute lymphoblastic leukaemia antigen. Nature. Feb 7 1980;283 (5747):583-5.

45. Lebacq-Verheyden AM, Ravoet AM, Bazin H, Sutherland DR, Tidman N, Greaves MF. Rat AL2, AL3, AL4 and AL5 monoclonal antibodies bind to the common acute lymphoblastic leukaemia antigen (CACUTE LYMPHOBLATIC LEUKEMIAA gp 100). International Journal of Cancer. Sep 15 1983; 32(3):273-9.

46. Brodsky FM, Parham P, Barnstable CJ, Crumpton MJ, Bodmer WF. Monoclonal antibodies for analysis of the HLA system. Immunological Reviews. 1979;47:3-61.

47. Tax W, Willems H, Kibbelaar M, et al. Monoclonal antibody against human thymocytes and T lymphocytes. In: Peeters H, ed. Protides of the biological fluids. Pergamon Press; 1982:701-704.

48. Greaves MF. Analysis of the clinical and biological significance of lymphoid phenotypes in acute leukemia. Cancer Research. Nov 1981;41(11 Pt 2):4752-66.

49. Greaves MF. Subtypes of acute lymphoblastic leukaemia: implications for the pathogenesis and epidemiology of leukaemia. Pathogenesis of Leukemia and Lymphoma: Environmental Influences. Raven Press; 1984:129.

50. Bollum F. Terminal deoxynucleotidyl transferase as a hematopoietic cell marker. Blood. 1979;54(6):1203-1215.

51. Kung P, Goldstein G, Reinherz EL, Schlossman SF. Monoclonal antibodies defining distinctive human T cell surface antigens. Science. Oct 19 1979;206(4416):347-9.

52. Reinherz EL, Kung PC, Goldstein G, Levey RH, Schlossman SF. Discrete stages of human intrathymic differentiation: analysis of normal thymocytes and leukemic lymphoblasts of T-cell lineage. Proceedings of the National Academy of Sciences of the United States of America. Mar 1980;77(3):1588-92.

53. Jondacute lymphoblatic leukemia M, Holm G, Wigzell H. Surface markers of human T and B lymphocytes forming non-immune rosettes with sheep red blood cells. J exp Med. 1972;136:207.

54. Stathopoulos G, Elliott E. Formation of mouse or sheep redblood-cell rosettes by lymphocytes from normal and leukaemic individuals. The Lancet. 1974;303(7858):600-601.

55. Borowitz MJ, Shuster JJ, Civin CI, et al. Prognostic significance of CD34 expression in childhood B-precursor acute lymphocytic leukemia: a Pediatric Oncology Group study. Journal of Clinical Oncology. 1990;8(8):1389-1398.

56. Foroni L, Foldi J, Matutes E, et al. α, β and γ T‐cell receptor genes: rearrangements correlate with haematological phenotype in T cell leukaemias. British Journal of Haematology. 1987;67(3):307-318.

57. Saxinger C, Gacute lymphoblatic leukemiao R. Application of the indirect enzyme-linked immunosorbent assay microtest to the detection and surveillance of human T cell leukemia-lymphoma virus. Laboratory Investigation. 1983;49(3):371-7.

58. Lillehoj E, Tal C, Nguyen A, Alexander S. Characterization of env and tax encoded polypeptides of human T-cell leukemia virus type I. Clin Biotechnol. 1989;1:27-41.

59. Anderson DC, Epstein J, Pierik L, et al. Licensure of screening tests for antibody to human T-lymphotropic virus type I. MMWR. 1988;37(48):736-40,745-7.

60. Ayeni O. Demographic characteristics of Nigeria: an analysis of population data from 1931-1965. University of London; 1975.

61. Williams CKO, Essien EM. Spectrum of haemopoietic and lymphoreticular neoplasia in Ibadan. vol Chapter 10. Cancer In Nigeria. University of Ibadan Press; 1983:83-93.

62. Odebiyi A. Socio-economic status, illness, behaviour and attitudes towards disease etiology in Ibadan. Niger Behav Sci J. 1980;3: 172-186.

63. Yin JL, Williams BG, Arthur CK, Ma DD. Interferon response in chronic myeloid leukaemia correlates with ABL/BCR expression: a preliminary study. Research Support, Non-U.S. Gov't. Br J Haematol. Mar 1995;89(3): 539-45.

64. Williams CKO, Liu L. Burkitt's lymphoma: a human tumor model for studies of dose intensity and other chemotherapy principles. presented at: Annual Meeting of the American Association for Cancer Research, Abstract #1178; 1996;

65. Williams CKO, Foroni L, Luzzatto L, Saliu I, Greaves M. Reduced incidence of common acute lymphoblastic leukaemia and its absence in the first quinquenium in an African population is consistent with a role for delayed infection in its aetiology. In: Proceedings of the 38th Annual Meeting of the American Society of Clinical Oncology. 2002:

66. Williams CKO, Dada AJ, Levine A, et al. Geographical variation in human T-lymphotropic virus types I and II infection in Nigeria. presented at: 6th International Conference on AIDS; 20-24 June 1990 1990; Volume 2, abstract No. FA.11.; San Francisco, CA.

67. Williams CKO, Dada A, Blattner WA. Some epidemiological features of the human T-cell lymphotropic virus type I (HTLV-I) and ATL in Nigerians. Leukemia. 1994;8:S77-S82.

68. Williams CKO, Alexander SS, Bodner A, al. e. Frequency of adult T-cell leukemia/ lymphoma and HTLV-I in Ibadan, Nigeria. British journal of cancer. 1993;67:783-786.

69. Williams CKO, Alabi GO, Junaid GA, al. e. Human T-cell leukemia virus associated lymphoproliferative disease: Report of 2 cases in Nigeria. British Journal of Medicine. 1984;288:1495-96.

70. Williams CKO, Akingbehin NA, Seriki O, Folami AO. Efficacy of a high-dose cytosine arabinoside (ARA-C) containing regimen in the control of advanced Burkitt's lymphoma (ADV-BL) - A preliminary assessment. 1985:

71. Williams CKO. Some biological and epidemiological characteristics of human leukaemias in Africans. vol 63. Virus-associated cancers in Africa. International Agency for Cancer Research.; 1985.

72. Williams CKO. Clustering of Burkitt's lymphoma and other high-grade malignant lymphoproliferative diseases, but not acute lymphoblastic leukemia among socio-economicacute lymphoblatic leukemiay deprived Nigerians. East African medical journal. 1988;65(No.4):253-263.

73. Williams CKO. Epidemiology of childhood leukemia/lymphoma in resource-poor countries: Nature's manifestation of Ludwig Gross's experiments on environmental influence on animal leukemogenesis? presented at: 104th Annual Meeting of the American Association for Cancer Research; April 2013 2013;

74. Williams CKO. Childhood leukemia and lymphoma: African experience supports a role for environmental factors. In: Proceedings of the 103rd Annual Meeting of the American Association for Cancer Research. 2012:

75. Williams CKO. Survival disparity in childhood acute lymphoblastic leukemia (CHD-ACUTE LYMPHOBLATIC LEUKEMIA): Lessions from chacute lymphoblatic leukemiaenges in Nigeria (NGR). presented at: Proceedings of the 48th Annual Meeting of the American Society of Clinical Oncology; June 1-5, 2012; Abstract #e17013. 2012;

76. Williams CKO. Clinical manifestation of lymphoid leukaemias in Ibadan. Nig Med J. 1986;16(5-6):51-56.

77. Williams CK, Oyejide CO. Chemotherapeutic responsiveness of acute lymphoblastic leukaemia in young Nigerians. West African Journal of Medicine. 1986;5(4): 257-265.

78. Williams CK, Ogan O. Chronic myeloid leukemia associated with impairment of hearing. Br Med J (Clin Res Ed). Jun 8 1985;290(6483):1705.

79. Williams CK, Johnson AO, Blattner WA. Human T-cell leukaemia virus in Africa: possible roles in health and disease. IARC Sci Publ. 1984;(63):713-26.

80. Williams CK, Foroni L, Luzzatto L, Saliu I, Levine A, Greaves MF. Childhood leukaemia and lymphoma: African experience supports a role for environmental factors in leukaemogenesis. ecancermedicalscience. 2014;8

81. Williams C, Folami A, Laditan A, Ukaejiofo E. Childhood acute leukaemia in a tropical population. British journal of cancer. 1982;46(1):89.

82. Williams CK, Essien EM, Bamgboye EA. Trends in leukemia incidence in Ibadan, Nigeria. Pathogenesis of Leukemia and Lymphoma: Environmental Influences. Raven Press; 1984:17-27.

83. Williams CK, Dada A, Blattner WA. Some epidemiological features of the human T-cell lymphotropic virus type I (HTLV-I) and ATL in Nigerians. Leukemia. 1994;8(Suppl 1):S77-82.

84. Williams CK, Alexander SS, Bodner A, et al. Frequency of adult T-cell leukaemia/lymphoma and HTLV-I in Ibadan, Nigeria. Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, P.H.S. British journal of cancer. Apr 1993;67(4):783-6.

85. Williams CK. Some biological and epidemiological characteristics of human leukemias in Africa. vol 63. Virus-associated Cancers in Africa. International Agency for Research on Cancer; 1984:713-726.

86. Williams CK. Clustering of Burkitt's lymphoma and other high-grade malignant lymphoproliferative diseases, but not acute lymphoblastic leukaemia among socio-economicacute lymphoblatic leukemiay deprived Nigerians. Research Support, Non-U.S. Gov't. East African medical journal. Apr 1988;65(4):253-63.

87. Williams CK. Influence of life-style on the pattern of leukaemia and lymphoma subtypes among Nigerians. Research Support, Non-U.S. Gov't. Leuk Res. 1985;9(6):741-5.

88. Williams CK. Some biological and epidemiological characteristics of human leukaemia in Africans. IARC Sci Publ. 1984; (63):687-712.

89. Williams CK. Management of malignant lymphoproliferative disorders of the nervous system. Afr J Med Med Sci. 1984;13(3-4):93-101.

90. Williams C, Saxinger C, Alabi G, et al. Clinical correlates of retroviral serology in Nigerians. In: Giraldo G, Beth-Giraldo E, Clumeck N, Garbi M-R, Kyalwazi SK, de The G, eds. AIDS and Associated Cancers in Africa. Kaeger; 1988:71-84.

91. Williams C, Folami A, Seriki O. Patterns of treatment failure in Burkitt's lymphoma. European Journal of Cancer and Clinical Oncology. 1983;19(6):741-746.

92. Williams C. Some biological and epidemiological characteristics of human leukaemia in Africans. IARC scientific publications. 1984;(63):687.

93. Williams C. Neoplastic diseases of the haemopoietic system in Ibadan: preliminary report of a prospective study. Afr J Med Sci. 1985;14:89-94.

94. Williams C. Some biological and epidemiological characteristics of human leukaemias in Africa. vol 9. Virus-associated cancers in Africa,. International Agency for Research on Cancer.; 1984.

95. Reis LG, Kosary KL, Hankey BF, Miller BA, Edwards BK. SEERS Cancer Statistics Review, 1973-1996. 1998.

96. Yamamoto JF, Goodman MT. Patterns of leukemia incidence in the United States by subtype and demographic characteristics, 1997–2002. Cancer Causes & Control. 2008; 19:379-390.

97. Bowman E, Presbury G, Melvin S, George SL, Simone J. A comparative analysis of acute lymphocytic leukemia in White and Black children: presenting clinical features and immunologic markers. Pathogenesis of leukemias and lymphomas: Environmental influences. Raven Press; 1984.

98. Birch JM, Marsden HB, Swindell R. Incidence of malignant disease in childhood: a 24-year review of the Manchester Children's Tumour Registry data. British journal of cancer. 1980; 42(2):215.

99. Young Jr J, Miller RW. Incidence of malignant tumors in US children. The Journal of pediatrics. 1975;86(2):254.

100. Greaves MF, Janossy G, Peto J, Kay H. Immunologicacute lymphoblatic leukemiay defined subclasses of acute lymphoblastic leukaemia in children: their relationship to presentation features and prognosis. British Journal of Haematology. Jun 1981;48(2):179-97.

101. Royston I, Minowada J, LeBien T, et al. Phenotypes of adult acute lymphoblastic leukemia defined by monoclonal antibodies. Human leucocyte markers detected by monoclonal antibodies. 1983.

102. Foroni L, Catovsky D, Rabbitts T, Luzzatto L. DNA rearrangements of immunoglobulin genes correlate with phenotypic markers in B-cell malignancies. Molecular biology & medicine. 1984;2(1):63.

103. Mauch PM, Kalish LA, Kadin M, Coleman CN, Osteen R, Hellman S. Patterns of presentation of Hodgkin disease. Implications for etiology and pathogenesis. Cancer. 1993;71(6):2062-2071.

104. Glaser SL, Jarrett RF. 1 The epidemiology of Hodgkin's disease. Baillière's clinical haematology. 1996;9(3):401-416.

105. Wacute lymphoblatic leukemiaace TA, Martin DN, Ambs S. Interactions among genes, tumor biology and the environment in cancer health disparities: examining the evidence on a national and global scale. Carcinogenesis. 2011;32(8):1107-1121.

106. Newman LA, Jenkins B, Chen Y, et al. Hereditary susceptibility for triple negative breast cancer associated with western sub-saharan african ancestry: Results from an international surgical breast cancer collaborative. Annals of surgery. 2019;270(3): 484-492.

107. Davis MB, Newman LA. Oncologic anthropology: an interdisciplinary approach to understanding the association between geneticacute lymphoblatic leukemiay defined African ancestry and susceptibility for triple negative breast cancer. Current Breast Cancer Reports. 2021:1-12.

108. Ayoola E. Antibody to hepatitis A virus in healthy Nigerians. Journal of the National Medical Association. 1982;74(5):465.

109. Smith MA, Simon R, Strickler HD, McQuillan G, Ries LAG, Linet MS. Evidence that childhood acute lymphoblastic leukemia is associated with an infectious agent linked to hygiene conditions. Cancer Causes & Control. 1998;9(3):285-298.

110. Bernal W, Smith H, Williams R. A community prevalence study of antibodies to hepatitis A and E in inner‐city London. Journal of medical virology. 1996;49(3):230-234.

111. O'conor GT, Davies J. Malignant Tumors in African Children, with special reference to Malignant Lymphoma. Journal of Pediatrics. 1960;56(4):526-35.

112. Acute lymphoblatic leukemiaan NC, Watson- Williams, E.G. A study of leukaemias among Nigerians in Ibadan. Karger; 1963: 906-915.

113. Davies J, Owor R. Chloromatous tumours in African children in Uganda. British medical journal. 1965;2(5458):405.

114. Sonnet J, Michaux J, Hekster C. Incidence and forms of leukaemia among the Congolese Bantus. Tropical and Geographical Medicine. 1966;18(4):272-286.

115. Gelfand M. Leukaemia in the African with special reference to splenomegaly in the lymphatic form. Tropical Medicine and Hygiene News. 1967;70(4):85-7.

116. Haddock D. The pattern of leukaemia in Accra, Ghana. Journal of Tropical Medicine and Hygiene. 1967;70(3):60-62.

117. Lothe F. Leukaemia in Uganda. Tropical and Geographical Medicine. 1967;19(3):163-171.

118. Kasili E, Taylor JR. Leukaemia in Kenya. East African medical journal. 1970;47(9):461-8.

119. Edington G, Hendrickse M. The geographical pathology of cancer in Africa with special reference to the western state of Nigeria and tumours of lymphoreticular tissue. Dokita. 1972;4:1-9.

120. Essien E. Leukaemia in Nigerians: the chronic leukaemias. East African medical journal. 1976;53(2):96-103.

121. Essien E. Leukaemia in Nigerians. I. The acute leukaemias. The African journal of medical sciences. 1972;3(2):117-130.

122. Jeffrey C, Gelfand M. Leukaemia in the Rhodesian African. Journal of Tropical Medicine and Hygiene. 1972;75(9):176-9.

123. Amsel S, Nabembezi J. Two-year survey of hematologic malignancies in Uganda. Journal of the National Cancer Institute. 1974;52(5):1397-1401.

124. Lowe R. The incidence of leukaemia in the Rhodesian African-A five year hospital survey. Central African Journal of Medicine. 1974;20(4):80-84.

125. Williams AO. Tumors of childhood in Ibadan, Nigeria. Cancer. Aug 1975;36(2):370-8.

126. IZZIA K. LES LEUCEMIES LYMPHOIDES CHRONIQUES AU ZAIRE. A PROPOS DE 39 CAS. 1977;

127. Fleming AF. Epidemiology of the leukaemias in Africa. Leukemia Research. 1979;3(2):51-9.

128. Macdougacute lymphoblatic leukemia LG, Jankowitz P, Cohn R, Bernstein R. Acute Childhood Leukemia in Johannesburg: Ethnic Differences in Incidence, Cell Type, and Survival. J Pediatr Hematol Oncol. 1986;8 (1):43.

129. Hayhoe F. CLINICAL AND CYTOLOGICAL RECOGNITION AND DIFFERENTIATION. Lectures on Haematology. 1960:113.

130. Çavdar AO, Gözdaşoǧglu S, Arcasoy A, Demiraǧ B. Chlorama-like ocular manifestations in Turkish children with acute myelomonocytic leukaemia. The Lancet. 1971;297(7701):680-682.

131. Chiu H-I, Chiu H-C, Wu C-C, Cheng H-C, Wang A-G. Acute Myeloid Leukemia With Extramedullary Myeloid Sarcoma Presenting as Optic Neuropathy. Journal of Neuro-Ophthalmology. 2022:10.1097.

132. Iizuka Y, Aiso M, Oshimi K, et al. Myeloblastoma formation in acute myeloid leukemia. Leukemia research. 1992;16(6-7): 665-671.

133. Boice Jr JD. Lauriston S. Taylor lecture: radiation epidemiology—the golden age and future chacute lymphoblatic leukemiaenges. Health Physics. 2011;100(1):59-76.

134. Boice Jr JD, ed. Ionizing radiation. Oxford University Press; 2006. Shottenfeld d fj, ed. Cancer epidemiology and prevention.

135. Gilbert ES. Ionising radiation and cancer risks: what have we learned from epidemiology? International journal of radiation biology. 2009;85(6):467-482.

136. United Nations Scientific Committee on the Effects of Atomic Radiation. Report of the United Nations Scientific Committee on the effects of atomic radiation. 1988;

137. International Agency for Research on Cancer. A Review of Human Carcinogens. F. Chemical Agents and Related Occupations: IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. 2012;

138. Pui C-H, Evans WE. A 50-year journey to cure childhood acute lymphoblastic leukemia. Elsevier; 2013:185-196.

139. Court B, Doll R. Leukemia in childhood and young adult life: trends in mortality in relation to etiology. Brit Med J. 1961;1:981.

140. Magrath I, O'Conor GT, Ramot B. Pathogenesis of leukemias and lymphomas: environmental influences. (No Title). 1984;

141. MacMahon B, Koller EK. Ethnic differences in the incidence of leukemia. Blood. 1957;12(1):1-10.

142. Ramot B, Magrath I. Hypothesis: The environment is a major determinant of the immunological sub‐type of lymphoma and acute lymphoblastic leukaemia in children. British Journal of Haematology. 1982;50(2): 183-189.

143. US Bureau Of Census: Historical Statistics of the United States, 1789-1945 (US Government Printing Office, 1949) (1949).

144. McFarlane H, Olusi SO, Adesina HA, Ade-Serrano MA, Osunkoya BO. Evidence of impaired immunological response in malnourished human population. 1977:23-41.

145. McFarlane H, Hamid J. Cell-mediated immune response in malnutrition. Clinical and experimental immunology. 1973;13(1):153.

146. Smythe PM, Breton-Stiles GG, Grace HJ, et al. Thymolymphatic deficiency and depression of cell-mediated immunity in protein-calorie malnutrition. Lancet. 1971;2: 939-943.

147. Gross L. Oncogenic viruses. Oncogenic viruses. Pergamon Press; 1970.

148. Fleming AF. HTLV: try Africa. Lancet. Jan 1 1983;1(8314-5):69.

149. Brunson A, Keegan TH, Bang H, Mahajan A, Paulukonis S, Wun T. Increased risk of leukemia among sickle cell disease patients in California. Blood, The Journal of the American Society of Hematology. 2017; 130(13):1597-1599.

150. Schultz WH, Ware RE. Malignancy in patients with sickle cell disease. American journal of hematology. 2003;74(4):249-253.

151. Dores GM, Devesa SS, Curtis RE, Linet MS, Morton LM. Acute leukemia incidence and patient survival among children and adults in the United States, 2001-2007. Blood, The Journal of the American Society of Hematology. 2012;119(1):34-43.

152. Kasim K, Levacute lymphoblatic leukemiaois P, Abdous B, Auger P, Johnson KC, Group CCRER. Environmental tobacco smoke and risk of adult leukemia. Epidemiology. 2005:672-680.

153. Miller RW. Interim report: UICC international study of childhood cancer. International Journal of Cancer. 1972;10(3): 675-677.

154. Merz LE, Story CM, Osei MA, et al. Absolute neutrophil count by Duffy status among healthy Black and African American adults. Blood Advances. 2023;7(3):317-320.

155. Rappoport N, Simon AJ, Amariglio N, Rechavi G. The Duffy antigen receptor for chemokines, ACKR 1,–‘Jeanne DARC’of benign neutropenia. British journal of haematology. 2019;184(4):497-507.

156. Vona-Davis L, Rose DP. The influence of socioeconomic disparities on breast cancer tumor biology and prognosis: a review. Journal of women's health. 2009;18(6):883-893.

157. Gordon NH. Association of education and income with estrogen receptor status in primary breast cancer. American journal of epidemiology. 1995;142(8):796-803.

158. Thomson C, Hole D, Twelves C, Brewster D, Black R. Prognostic factors in women with breast cancer: distribution by socioeconomic status and effect on differences in survival. Journal of Epidemiology & Community Health. 2001;55(5):308-315.

159. Bauer KR, Brown M, Cress RD, Parise CA, Caggiano V. Descriptive analysis of estrogen receptor (ER)‐negative, progesterone receptor (PR)‐negative, and HER2‐negative invasive breast cancer, the so‐cacute lymphoblatic leukemiaed triple‐negative phenotype: a population‐based study from the California cancer Registry. cancer. 2007; 109(9):1721-1728.

160. Huo D, Ikpatt F, Khramtsov A, et al. Population differences in breast cancer: survey in indigenous African women reveals over-representation of triple-negative breast cancer. Journal of Clinical Oncology. 2009;27(27):4515-4521.

161. Dunn BK, Agurs-Collins T, Browne D, Lubet R, Johnson KA. Health disparities in breast cancer: biology meets socioeconomic status. Breast cancer research and treatment. 2010;121:281-292.

162. Parise CA, Caggiano V. The influence of socioeconomic status on racial/ethnic disparities among the ER/PR/HER2 breast cancer subtypes. Journal of cancer epidemiology. 2015;2015

163. Kamangar F, Dores GM, Anderson WF. Patterns of cancer incidence, mortality, and prevalence across five continents: defining priorities to reduce cancer disparities in different geographic regions of the world. Journal of clinical oncology. 2006;24(14): 2137-2150.

164. Vainshtein J. Disparities in breast cancer incidence across racial/ethnic strata and socioeconomic status: a systematic review. Journal of the National Medical Association. 2008;100(7):833-839.

165. Catovsky D, Rose M, Goolden A, et al. Adult T-cell lymphoma-leukaemia in Blacks from the West Indies. The Lancet. 1982;319 (8273):639-643.

166. Blayney D, Jaffe E, Blattner W, et al. The human T-cell leukemia/lymphoma virus associated with American adult. Blood. 1983; 62(2):401-405.

167. Blattner W, Saxinger C, Clark J, et al. Human T-cell leukaemia/lymphoma virus-associated lymphoreticular neoplasia in Jamaica. The Lancet. 1983;322(8341):61-64.

168. Murphy E, Figueroa P, Gibbs WN, et al. Human T-lymphotropic virus type I (HTLV-I) seroprevalence in Jamaica I. Demographic determinants. American journal of epidemiology. 1991;133(11):1114-1124.

169. Cleghorn FR, Manns A, Falk R, et al. Effect of human T-lymphotropic virus type I infection on non-Hodgkin's lymphoma incidence. Journal of the National Cancer Institute. 1995;87(13):1009-1014.

170. Mozaheb Z. Epidemiology of HTLV1 Associated Lymphoma. The Ulutas Medical Journal. 2016;2(1):77-81.

171. Ericsson JE, Karnström L, MATTSSON B. CHILDHOOD CANCER IN SWEDEN, 1958–1974: I. Incidence and mortality. Acta Pædiatrica. 1978;67(4):425-432.

172. Ajuba I, Madu A, Okocha C, Ibegbulam O, Okpala I, Nna O. Frequency and clinical impact of ETV6/RUNX1, AF4‑MLL, and BCR/ABL fusion genes on features of acute lymphoblastic leukemia at presentation. Nigerian journal of clinical practice. 2016;19 (2):237-241.

173. Gessain A, Cassar O. Epidemiological aspects and world distribution of HTLV-1 infection. Frontiers in microbiology. 2012;3

174. Williams CKO, Williams CKO. Global HTLV-1/2 burden and associated diseases. Cancer and AIDS: Part II: Cancer Pathogenesis and Epidemiology. 2019:21-57.

175. Kengne M, Tsata DCW, Ndomgue T, Nwobegahay JM. Prevalence and risk factors of HTLV-1/2 and other blood borne infectious diseases among blood donors in Yaounde Central Hospital, Cameroon. Pan African Medical Journal. 2018;30(1)

176. Paruk H, Bhigjee A. Health policy implications of blood transfusion-related human T-cell lymphotropic virus type 1 infection and disease: case report. Southern African Journal of Infectious Diseases. 2015;30(4):4-5.

177. Ratner L. A role for an HTLV-1 vaccine? Frontiers in immunology. 2022;13:953650.

178. Mahieux R. A vaccine against HTLV-1 HBZ makes sense. Blood, The Journal of the American Society of Hematology. 2015;126 (9):1052-1053.

179. Santana CS, Andrade FdO, da Silva GCS, et al. Advances in preventive vaccine development against HTLV-1 infection: A systematic review of the last 35 years. Frontiers in Immunology. 2023;14:1073779.

180. Jones DS, Abdacute lymphoblatic leukemiaa M, Gone JP. Indigenous Americans—The Journal’s Historical “Indian Problem”. New England Journal of Medicine. January 4, 2024 2024;390(No. 1):1-7.

181. Jones DS. Virgin soils revisited. The William and Mary Quarterly. 2003;60(4):703-742.