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Evidence that Childhood Acute Lymphoblastic Leukemia is Associated with an Infectious Agent Linked to Hygiene Conditions

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Abstract

Objectives: The incidence of acute lymphoblastic leukemia (ALL) in children has shown temporal and geographic variation during the 20th century, with higher rates in developed nations appearing in the first half of the century, but with persisting low rates in developing nations. We sought to assess the relation of childhood ALL with hygiene conditions, an aspect of socioeconomic development affecting rates of exposure to infectious agents.

Methods: Infection patterns for hepatitis A virus (HAV), an agent with a fecal-oral route of transmission, were used to indicate hygiene conditions in different populations, with emphasis on instructive United States and Japanese data. A catalytic model was fit to these data, estimating the HAV force of infection and age-specific seroprevalence rates over time. These analyses were used to assess the temporal relationship of changes in HAV infection rates to changes in childhood leukemia mortality and incidence rates.

Results: We observed an inverse relationship between HAV infection prevalence and rates of childhood leukemia. Further, decreases in the HAV force of infection in the United States and Japan appear to have preceded increases in childhood leukemia rates. We describe a model based on a putative leukemia-inducing agent with a change in infection rate over time correlated with that of HAV that describes well the temporal trends in childhood leukemia rates for White children in the US and for Japanese children.

Conclusion: The data suggest that improved public hygiene conditions, as measured by decreased prevalence of HAV infection, are associated with higher childhood ALL incidence rates. The model that we present supports the plausibility of the hypothesis that decreased childhood exposure to a leukemia-inducing agent associated with hygiene conditions leads to higher rates of ALL in children by increasing the frequency of in utero transmission caused by primary infection during pregnancy (or by increasing the number of individuals infected in early infancy because of lack of protective maternal antibodies). Cancer causes and Control 1998, 9, 285-298

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References

  1. Hewitt D. Some features of leukaemia mortality. Br J Prev Social Med 1955; 9: 81–8.

    Google Scholar 

  2. Gilliam A, Walter W. Trends of mortality from leukemia in the United States, 1921–55. Public Health Rep 1958; 73: 773–84.

    Google Scholar 

  3. Linet MS, Devesa SS. Descriptive epidemiology of childhood leukaemia. Br J Cancer 1991; 63: 424–9.

    Google Scholar 

  4. Fleming AF. Leukaemias in Africa. Leukemia 1993; 7Suppl 2: S138–41.

    Google Scholar 

  5. Slocumb J, MacMahon B. Changes in mortality rates from leukemia in the first five years of life. N Engl J Med 1963; 268: 922–5.

    Google Scholar 

  6. Stewart A, Webb J, Hewitt D. A survey of childhood malignancies. Br Med J 1958; 1: 1495–508.

    Google Scholar 

  7. Court-Brown W, Doll R. Leukemia in childhood and young adult life. Trends in mortality in relation to aetiology. Br Med J 1961; 1: 981–8.

    Google Scholar 

  8. Burnet M. Leukemia as a problem in preventive medicine. N Engl J Med 1958; 259: 423–31.

    Google Scholar 

  9. Fleming AF. Epidemiology of the leukaemias in Africa. Leuk Res 1979; 3: 51–9.

    Google Scholar 

  10. Greaves M, Pegram S, Chan L. Collaborative Group Study of the Epidemiology of Acute Lymphoblastic Leukaemia Subtypes: Background and First Report. In: Greaves M, Chan L, eds. Epidemiology of Leukaemia and Lymphoma. Oxford, UK: Pergamon Press, 1985: 55–73.

    Google Scholar 

  11. Greaves MF, Colman SM, Beard ME, et al. Geographical distribution of acute lymphoblastic leukaemia subtypes: second report of the collaborative group study. Leukemia 1993; 7: 27–34.

    Google Scholar 

  12. Pinkel D, Nefzger D. Some epidemiological features of childhood leukemia in the Buffalo, N.Y., area. Cancer 1959; 12: 351–8.

    Google Scholar 

  13. Browning D, Gross S. Epidemiological studies of acute childhood leukemia. A survey of Cuyahoga county, Ohio. Am J Dis Child 1968; 116: 576–85.

    Google Scholar 

  14. Fasal E, Jackson EW, Klauber MR. Birth characteristics and leukemia in childhood. J Natl Cancer Inst 1971; 47: 501–9.

    Google Scholar 

  15. Alexander FE, Ricketts TJ, McKinney PA, Cartwright RA. Community lifestyle characteristics and risk of acute lymphoblastic leukaemia in children [see comments]. Lancet 1990; 336: 1461–5.

    Google Scholar 

  16. Alexander FE, Cartwright RA, McKinney PA, Ricketts TJ. Leukaemia incidence, social class and estuaries: an ecological analysis. J Public Health Med 1990; 12: 109–17.

    Google Scholar 

  17. Bithell JF, Dutton SJ, Neary NM, Vincent TJ. Controlling for socioeconomic confounding using regression methods. J Epidemiol Community Health 1995; 49: S15–9.

    Google Scholar 

  18. McKinney PA, Alexander FE, Cartwright RA, Scott CS, Staines A. Acute lymphoblastic leukaemia incidence in the UK by immunophenotype. Leukemia 1993; 7: 1630–4.

    Google Scholar 

  19. McWhirter W. The relationship of incidence of incidence of childhood lymphoblastic leukaemia to social class. Br J Cancer 1982; 46: 640–5.

    Google Scholar 

  20. Draper G, Vincent T, O'Conor C, Stiller C. Socioeconomic factors and variation in incidence rates between county districts. In: Draper G, ed. The Geographical Epidemiology of Childhood Leukaemia and non-Hodgkin's Lymphoma in Great Britain. London, UK: OPCS, 1991: 37–46.

    Google Scholar 

  21. Kaye SA, Robison LL, Smithson WA, Gunderson P, King FL, Neglia JP. Maternal reproductive history and birth characteristics in childhood acute lymphoblastic leukemia. Cancer 1991; 68: 1351–5.

    Google Scholar 

  22. Stark CR, Mantel N. Maternal-age and birth-order effects in childhood leukemia: age of child and type of leukemia. J Natl Cancer Inst 1969; 42: 857–66.

    Google Scholar 

  23. Birch JM, Swindell R, Marsden HB, Morris Jones PH. Childhood leukaemia in North West England 1954–1977: epidemiology, incidence and survival. Br J Cancer 1981; 43: 324–9.

    Google Scholar 

  24. Swensen A, Ross J, Severson R, Pollock B, Robison L. The age peak in childhood acute lymphoblastic leukemia: Exploring the potential relationship with socioeconomic status. Cancer 1997; 79: 2045–51.

    Google Scholar 

  25. Muirhead CR. Childhood leukemia in metropolitan regions in the United States: a possible relation to population density? Cancer Causes Control 1995; 6: 383–8.

    Google Scholar 

  26. Liberatos P, Link BG, Kelsey JL. The measurement of social class in epidemiology. Epidemiol Rev 1988; 10: 87–121.

    Google Scholar 

  27. Greaves M. A natural history for pediatric acute leukemia. Blood 1993; 82: 1043–51.

    Google Scholar 

  28. Greaves MF, Alexander FE. An infectious etiology for common acute lymphoblastic leukemia in childhood? Leukemia 1993; 7: 349–60.

    Google Scholar 

  29. Kinlen L. Evidence for an infective cause of childhood leukaemia: comparison of a Scottish new town with nuclear reprocessing sites in Britain [see comments]. Lancet 1988; 2: 1323–7.

    Google Scholar 

  30. Alexander FE. Viruses, clusters and clustering of childhood leukaemia: a new perspective? Eur J Cancer 1993; 29A: 1424–43.

    Google Scholar 

  31. Kinlen LJ. Epidemiological evidence for an infective basis in childhood leukaemia [Editorial]. Br J Cancer 1995; 71: 1–5.

    Google Scholar 

  32. Greaves M. Aetiology of acute leukemia. Lancet 1997; 349: 344–9.

    Google Scholar 

  33. Petridou E, Kassimos D, Kalmanti M, et al. Age of exposure to infections and risk of childhood leukaemia. Br Med J 1993; 307: 774.

    Google Scholar 

  34. Smith M. Considerations on a possible viral etiology for B-precursor acute lymphoblastic leukemia of childhood. J Immunother 1997; 20: 89–100.

    Google Scholar 

  35. Arthur RR, Shah KV. Occurrence and significance of papovaviruses BK and JC in the urine. Prog Med Virol 1989; 36: 42–61.

    Google Scholar 

  36. Rowe W, Huebner R, Hartley J. Ecology of a mouse tumor virus. In: Pollard M, ed. Perspectives in Virology. New Brunswick, NJ (USA): Rutgers University Press, 1961: 177–94.

    Google Scholar 

  37. Battegay M, Feinstone S. Hepatitis A virus. In: Willson R, ed. Viral Hepatitis: Diagnosis, Treatment, Prevention. New York, NY (USA): Marcel Dekker, Inc., 1997: 35–84.

    Google Scholar 

  38. McDowell A, Engel A, Massey JT, Maurer K. Plan and operation of the Second National Health and Nutrition Examination Survey, 1976–1980. Vital Health Stat [1] 1981; Series 1: 1–144.

  39. Forthofer RN. Investigation of nonresponse bias in NHANES II. Am J Epidemiol 1983; 117: 507–15.

    Google Scholar 

  40. Schenzle D, Dietz K, Frosner GG. Antibody against hepatitis A in seven European countries. II. Statistical analysis of cross-sectional surveys. Am J Epidemiol 1979; 110: 70–6.

    Google Scholar 

  41. Ikematsu H, Kashiwagi S, Hayashi J, et al. A seroepidemiologic study of hepatitis A virus infections: statistical analysis of two independent cross-sectional surveys in Okinawa, Japan. Am J Epidemiol 1987; 126: 50–4.

    Google Scholar 

  42. Sacks M, Seeman I. A statistical study of mortality from leukemia. Blood 1947; 2: 1–14.

    Google Scholar 

  43. Cooke J. The occurrence of leukemia. Blood 1954; 9: 340–7.

    Google Scholar 

  44. Ries L, Kosary C, Hankey B, Miller B, Harras A, Edwards B, eds. SEER Cancer Statistics Review, 1973–1994. Bethesda, MD (USA): National Cancer Institute, 1997.

    Google Scholar 

  45. Grove R, Hetzel A. Vital Statistics Rates in the United States 1940–1960 (Public Health Service Publication No. 1677). Washington, DC: US Government Printing Office, 1968.

    Google Scholar 

  46. Parkin DM, Whelan S, Ferlay J, Raymond L, Young J, eds. Cancer Incidence in Five Continents, Volume VII. Lyon, France: International Agency for Research on Cancer, 1997.

    Google Scholar 

  47. Fraumeni JF Jr, Miller R. Epidemiology of human leukemia: Recent observations. J Natl Cancer Inst 1967; 38: 593–605.

    Google Scholar 

  48. Parkin DM, Stiller C, Draper G, Bieber C. The international incidence of childhood cancer. Int J Cancer 1988; 42: 511–20.

    Google Scholar 

  49. Ajiki W, Hanai A, Tsukuma H, Hiyama T, Fujimoto I. Incidence of childhood cancer in Osaka, Japan, 1971–1988: reclassification of registered cases by Birch's scheme using information on clinical diagnosis, histology and primary site. Jpn J Cancer Res 1994; 85: 139–46.

    Google Scholar 

  50. Koff RS. Seroepidemiology of hepatitis A in the United States. J Infect Dis 1995; 171Suppl 1: S19–23.

    Google Scholar 

  51. Shapiro CN, Coleman PJ, McQuillan GM, Alter MJ, Margolis HS. Epidemiology of hepatitis A: seroepidemiology and risk groups in the USA. Vaccine 1992; 10Suppl 1: S59–62.

    Google Scholar 

  52. US Bureau of the Census. Historical Statistics of the United States, 1789–1945. Washington, DC: US Government Printing Office, 1949.

    Google Scholar 

  53. Hirst K, Butler N, Dawkings M. Infant and Perinatal Mortality in England and Wales. Washington, DC: US Government Printing Office 1968; Public Health Service Pub. No. 1000: Series 3, No. 12.

    Google Scholar 

  54. Szmuness W, Dienstag JL, Purcell RH, Harley EJ, Stevens CE, Wong DC. Distribution of antibody to hepatitis A antigen in urban adult populations. N Engl J Med 1976; 295: 755–9.

    Google Scholar 

  55. Soda T, Kimurra M, Hirayama T, Tsunoda R, Suganuma T, Ueda K. Recent Retardation of Mortality Rates in Japan. Washington, DC: US Government Printing Office, 1968; Public Health Service Pub. No. 1000: Series 3, No. 10.

    Google Scholar 

  56. Akbar SM, Onji M, Kanaoka M, et al. The seroepidemiology of hepatitis A and B in a Japanese town. Asia Pac J Public Health 1992; 6: 26–9.

    Google Scholar 

  57. Abdool Karim SS, Coutsoudis A. Sero-epidemiology of hepatitis A in black South African children. S Afr Med J 1993; 83: 748–50.

    Google Scholar 

  58. Botha JF, Blackburn NK, Schoub BD, Kew MC. The prevalence of antibodies to the hepatitis A virus in Owambo children. Trop Gastroenterol 1994; 15: 15–7.

    Google Scholar 

  59. Mohamud KB, Aceti A, Mohamed OM, et al. [The circulation of the hepatitis A and B viruses in the Somali population]. Ann Ital Med Int 1992; 7: 78–83.

    Google Scholar 

  60. Ayoola EA. Antibody to hepatitis A virus in healthy Nigerians. J Natl Med Assoc 1982; 74: 465–8.

    Google Scholar 

  61. Werner GT, Frosner GG, Fresenius K. Prevalence of serological hepatitis A and B markers in a rural area of northern Zaire. Am J Trop Med Hyg 1985; 34: 620–4.

    Google Scholar 

  62. Darwish M, Faris R, Clemens J, Rao M, Edelman R. High seroprevalence of hepatitis A, B, C, and E viruses in residents in an Egyptian village in The Nile Delta: a pilot study. Am J Trop Med Hyg 1996; 54: 554–8.

    Google Scholar 

  63. Thuring E, Joller-Jemelka HI, Sareth H, Sokhan U, Reth C, Grob P. Prevalence of markers of hepatitis viruses A, B, C and of HIV in healthy individuals and patients of a Cambodian province. Southeast Asian J Trop Med Public Health 1993; 24: 239–49.

    Google Scholar 

  64. Queiroz DA, Cardoso DD, Martelli CM, et al. Risk factors and prevalence of antibodies against hepatitis A virus (HAV) in children from day-care centers, in Goiania, Brazil. Rev Inst Med Trop Sao Paulo 1995; 37: 427–33.

    Google Scholar 

  65. Arankalle V, Tsarev S, Chadha M, et al. Age-specific prevalence of antibodies to hepatitis A and E viruses in Pune, India, 1982 and 1992. J Infect Dis 1995; 171: 447–50.

    Google Scholar 

  66. Fleming AF. Possible aetiological factors in leukaemias in Africa. Leuk Res 1988; 12: 33–43.

    Google Scholar 

  67. Kamel AM, Assem MM, Jaffe ES, Magrath I, Aboul Enein MI, Hindawy DS. Immunological phenotypic pattern of acute lymphoblastic leukaemia in Egypt. Leuk Res 1989; 13: 519–25.

    Google Scholar 

  68. Parkin DM, Stiller C, Draper G, Bieber C, Terracini B, Young J. International Incidence of Childhood Cancer. Lyon, France: International Agency for Research on Cancer, 1988.

    Google Scholar 

  69. Booth K, Amato D. Leukaemia in Papua New Guinea. Trop Geogr Med 1978; 30: 343–9.

    Google Scholar 

  70. Tu J, Li FP. Incidence of childhood tumors in Shanghai, 1973–77. J Natl Cancer Inst 1983; 70: 589–92.

    Google Scholar 

  71. Alert J, Jimenez J. Malignant tumors in Cuban children. Fourth triennial 1973–1975 of the national cancer registry. Neoplasma 1980; 27: 739–44.

    Google Scholar 

  72. Nandakumar A, Anantha N, Appaji L, et al. Descriptive epidemiology of childhood cancers in Bangalore, India. Cancer Causes Control 1996; 7: 405–10.

    Google Scholar 

  73. Mejia-Arangure JM, Fajardo-Gutierrez A, Bernaldez-Rios R, Farfan-Canto JM, Ortiz-Fernandez A, Martinez-Garcia MD. Incidence trends of acute leukemia among the children of Mexico City: 1982–1991. Arch Med Res 1996; 27: 223–7.

    Google Scholar 

  74. Barr RD, McCulloch PB, Mehta S, Kendall AG. Acute leukaemia in Kenya. Scott Med J 1972; 17: 330–3.

    Google Scholar 

  75. Kasili EG, Taylor JR. Leukaemia in Kenya. East Afr Med J 1970; 47: 461–8.

    Google Scholar 

  76. Nishi M, Miyake H, Takeda T, Shimada M. Epidemiology of childhood leukemia in Hokkaido, Japan. Int J Cancer 1996; 67: 323–6.

    Google Scholar 

  77. Knudson A. Ethnic differences in childhood leukemia as revealed by a study of antecedent variables. Cancer 1965; 18: 815–8.

    Google Scholar 

  78. Bhargava M, Kumar R, Karak A, Kochupillai V, Arya LS, Mohanakumar T. Immunological subtypes of acute lymphoblastic leukemia in north India. Leuk Res 1988; 12: 673–8.

    Google Scholar 

  79. Rajalekshmy KR, Abitha AR, Pramila R, Gnanasagar T, Maitreyan V, Shanta V. Immunophenotyping of acute lymphoblastic leukaemia in Madras, India. Leuk Res 1994; 18: 183–90.

    Google Scholar 

  80. Wilkinson R. The frequency of hepatitis A and B viruses as the offending viral type in suspected hepatitis. S Afr Med J 1983; 63: 82–5.

    Google Scholar 

  81. Rego EM, Garcia AB, Viana SR, Falcao RP. Characterization of acute lymphoblastic leukemia subtypes in Brazilian patients. Leuk Res 1996; 20: 349–55.

    Google Scholar 

  82. Kellett C. Acute leukaemia in one of identical twins. Arch Dis Child 1937; 12: 239.

    Google Scholar 

  83. Fraumeni JF Jr. Infectious mononucleosis and acute leukemia. JAMA 1971; 215: 1159.

    Google Scholar 

  84. Austin DF, Karp S, Dworsky R, Henderson BE. Excess leukemia in cohorts of children born following influenza epidemics. Am J Epidemiol 1975; 101: 77–83.

    Google Scholar 

  85. Fedrick J, Alberman ED. Reported influenza in pregnancy and subsequent cancer in the child. Br Med J 1972; 2: 485–8.

    Google Scholar 

  86. Hakulinen T, Hovi L, Karkinen J, Penttinen K, Saxen L. Association between influenza during pregnancy and childhood leukaemia. Br Med J 1973; 4: 265–7.

    Google Scholar 

  87. Shore RE, Pasternack BS, Curnen MG. Relating influenza epidemics to childhood leukemia in tumor registries without a defined population base: a critique with suggestions for improved methods. Am J Epidemiol 1976; 103: 527–35.

    Google Scholar 

  88. Vianna NJ, Polan AK. Childhood lymphatic leukemia: prenatal seasonality and possible association with congenital varicella. Am J Epidemiol 1976; 103: 321–32.

    Google Scholar 

  89. Adelstein AM, Donovan JW. Malignant disease in children whose mothers had chickenpox, mumps, or rubella in pregnancy. Br Med J 1972; 4: 629–31.

    Google Scholar 

  90. van Steensel-Moll HA, Valkenburg HA, van Zanen GE. Childhood leukemia and infectious diseases in the first year of life: a register-based case-control study. Am J Epidemiol 1986; 124: 590–4.

    Google Scholar 

  91. Schlehofer B, Blettner M, Geletneky K, et al. Seroepidemiological analysis of the risk of virus infections for childhood leukaemia. Int J Cancer 1996; 65: 584–90.

    Google Scholar 

  92. Knox EG, Stewart AM, Kneale GW. Foetal infection, childhood leukaemia and cancer. Br J Cancer 1983; 48: 849–52.

    Google Scholar 

  93. Fleming A. Childhood leukaemia [Letter; Comment]. Lancet 1991; 337: 361.

    Google Scholar 

  94. Gold E, Nankervis G. Cytomegalovirus. In: Evans A, ed. Viral Infections of Humans: Epidemiology and Control, 3rd Ed. New York, NY (USA): Plenum Medical Book Company, 1989: 169–89.

    Google Scholar 

  95. Tookey PA, Ades AE, Peckham CS. Cytomegalovirus prevalence in pregnant women: the influence of parity. Arch Dis Child 1992; 67: 779–83.

    Google Scholar 

  96. Evans A, Cox F, Nankervis G, et al. A health and seroepidemiological survey of a community in Barbados. Int J Epidemiol 1974; 3: 167–75.

    Google Scholar 

  97. Evans AS, Cook JA, Kapikian AZ, Nankervis G, Smith AL, West B. A serological survey of St Lucia. Int J Epidemiol 1979; 8: 327–32.

    Google Scholar 

  98. Schopfer K, Lauber E, Krech U. Congenital cytomegalovirus infection in newborn infants of mothers infected before pregnancy. Arch Dis Child 1978; 53: 536–9.

    Google Scholar 

  99. Liu Z, Wang E, Taylor W, et al. Prevalence survey of cytomegalovirus infection in children in Chengdu. Am J Epidemiol 1990; 131: 143–50.

    Google Scholar 

  100. Kunitake T, Kitamura T, Guo J, Taguchi F, Kawabe K, Yogo Y. Parent-to-child transmission is relatively common in the spread of the human polyomavirus JC virus. J Clin Microbiol 1995; 33: 1448–51.

    Google Scholar 

  101. Gardner S, Knowles W. Human polyomaviruses. In: Zuckerman A, Bantvala J, Pattison J, eds. Principles and Practice of Clinical Virology. Chichester, UK: John Wiley & Sons, 1995: 635–51.

    Google Scholar 

  102. Bernal W, Smith HM, Williams R. A community prevalence study of antibodies to hepatitis A and E in inner-city London. J Med Virol 1996; 49: 230–4.

    Google Scholar 

  103. Tettmar RE, Masterton RG, Strike PW. Hepatitis A immunity in British adults-an assessment of the need for pre-immunisation screening. J Infect 1987; 15: 39–43.

    Google Scholar 

  104. Nandwani R, Caswell S, Boag F, Lawrence AG, Coleman JC. Hepatitis A seroprevalence in homosexual and heterosexual men. Genitourin Med 1994; 70: 325–8.

    Google Scholar 

  105. Stiller CA, Draper GJ. Trends in childhood leukaemia in Britain 1968–1978. Br J Cancer 1982; 45: 543–51.

    Google Scholar 

  106. Backer J, Aagenaes O. Infant Mortality Problems in Norway. Washington, DC: US Government Printing Office 1967; Public Health Service Pub. No 1000: Series 3, No. 8.

    Google Scholar 

  107. Bjelke E. Leukemia in children and young adults in Norway: Type distribution, incidence, and survival. Cancer 1964; 17: 248–55.

    Google Scholar 

  108. Ericsson JL, Karnstrom L, Mattsson B. Childhood cancer in Sweden, 1958–1974. I. Incidence and mortality. Acta Paediatr Scand 1978; 67: 425–32.

    Google Scholar 

  109. Lehmann NI, Gust ID. The prevalence of antibody to hepatitis A virus in two populations in Victoria. Med J Aust 1977; 2: 731–2.

    Google Scholar 

  110. Gust ID, Lehmann NI, Lucas CR, Ferris AA, Locarnini SA. Studies on the epidemiology of hepatitis A in Melbourne. In: GN V, Cohen S, Schmid R, eds. Viral hepatitis: A Contemporary Assessment of Etiology, Epidemiology, Pathogenesis, and Prevention. Philadelphia, PA (USA): Franklin Institute Press, 1978: 105–12.

    Google Scholar 

  111. Gust I, Lehmann N, Lucas C. Relationship between prevalence of antibody to hepatitis A antigen and age: A cohort effect? J Infect Dis 1978; 138: 425–6.

    Google Scholar 

  112. Petridou E, Revinthi K, Alexander FE, et al. Space-time clustering of childhood leukaemia in Greece: evidence supporting a viral aetiology. Br J Cancer 1996; 73: 1278–83.

    Google Scholar 

  113. Kobayashi A. Changing patterns of parasitic infections in Japan. In: Croll N, Cross J, eds. Human Ecology and Infectious Diseases. New York, NY (USA): Academic Press, 1983: 137–68.

    Google Scholar 

  114. Kuni C. Parasite control activities in Japan: Government-expert-private sector partnership. In: Croll N, Cross J, eds. Human Ecology and Infectious Diseases. New York, NY (USA): Academic Press, 1983: 169–85.

    Google Scholar 

  115. Tominaga S, Aoki K, Fujimoto I, Kurihara M. Cancer Mortality and Morbidity Statistics. Tokyo, Japan: Japan Scientific Societies Press, 1994; Gann Monogr Cancer Res, Vol. 41.

    Google Scholar 

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Smith, M.A., Simon, R., Strickler, H.D. et al. Evidence that Childhood Acute Lymphoblastic Leukemia is Associated with an Infectious Agent Linked to Hygiene Conditions. Cancer Causes Control 9, 285–298 (1998). https://doi.org/10.1023/A:1008873103921

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