Transgenerational susceptibility to leukaemia induction resulting from preconception, paternal irradiation

International Journal of Radiation Biology

Volumn 75, Issue 7, 1999, Pages 801-810

  Lord, B I ^a  

^a CHRISTIE HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADOLESCENT; ADULT; ATOMIC BOMB SURVIVOR; CHILD; CHILDHOOD LEUKEMIA; DISEASE PREDISPOSITION; ENVIRONMENTAL EXPOSURE; HUMAN; IRRADIATION; LEUKEMOGENESIS; NONHODGKIN LYMPHOMA; NUCLEAR REACTOR; PRIORITY JOURNAL; RADIATION DOSE; RADIATION EXPOSURE; RADIODIAGNOSIS; REVIEW;

ANIMALS; CHILD; CLUSTER ANALYSIS; FATHERS; FEMALE; GREAT BRITAIN; HUMANS; LEUKEMIA; LEUKEMIA, RADIATION-INDUCED; LYMPHOMA, NON-HODGKIN; MALE; MODELS, BIOLOGICAL; NEOPLASMS, RADIATION-INDUCED; NUCLEAR WARFARE; OCCUPATIONAL EXPOSURE; POPULATION DYNAMICS; POWER PLANTS; PREGNANCY; RADIOBIOLOGY; TUMOR VIRUS INFECTIONS;

EID: 0032794907     PISSN: 09553002     EISSN: None     Source Type: Journal    
DOI: 10.1080/095530099139854     Document Type: Review

References (89)

1. AEXANDER, F. E., CHAN, L. C., LAM, T. H., YUEN, P., LEUNG, N. K., HA, S. Y., YUEN, H. L., LI, C. K., LAU, Y. L. and GREAVES, M. F., 1997, Clustering of childhood leukaemia in Hong Kong: association with the childhood peak and common acute lymphoblastic leukaemia and with population mixing. British Journal of Cancer, 75, 457-463.
2. ANDERSSON, M., JUEL, K., ISHIKAWA, Y. and STORM, H. H., 1994, Effects of preconceptional irradiation on mortality and cancer incidence in the offspring of patients given injections of thorotrast. Journal of the National Cancer Institute, 86, 1866-1870.
3. BITHELL, J. F., DUTTON, S. J., DRAPER, G. J. and NEARY, N. M., 1994, Distribution of childhood leukaemias and non-Hodgkin's lymphomas near nuclear installations in England and Wales. British Medical Journal, 309, 501-505.
4. BLACK, D., 1984, Investigation of the possible increased incidence of cancer in West Cumbria. Report of the Independent Advisory Group (London: HMSO).
5. BNFL, 1998, 'No cause for concern' in new report. BNFL News, August 1998, p. 5.
6. BUCKLEY, J. D., ROBISON, L. L., SWOTINSKY, R., GARABRANT, D. H., LEBEAU, M., MANCHESTER, P., NESBIT, M. E., ODOM, L., PETERS, J. M. and WOODS, W. G., 1989, Occupational exposures of parents of children with acute nonlymphocytic leukemia: a report from the Children's Cancer Study Group. Cancer Research, 49, 4030-4037.
7. CATTANACH, B. M., PAPWORTH, D., PATRICK, G., GOODHEAD, D. T., HACKER, T., COBB, L. and WHITEHILL, E., 1998, Investigation of lung tumour induction in C3H/H mice, with and without tumour promotion with urethane, following paternal X-irradiation. Mutation Research, 403, 1-12.
8. J mice following paternal X-irradiation. International Journal of Radiation Biology, 67, 606-616.
9. CHOMET, P. S., WESSLER, R. and DELLAPORTA, S. L., 1987, Inactivation of the maize transposable element Activator (Ac) is associated with its UNA modification. EMBO Journal, 6, 295-302.
10. COMARE, 1996, Possible effects of paternal preconception irradiation in cancer. Committee on Medical Aspects of Radiation in the Environment, 4th report (London: Department of Health), pp. 82-96.
11. COOK-MOZAFFARI, P. J., DARBY, S. C., DOLL, R., FORMAN, D., HERMON, C., PIKE, M. C. and VINCENT, T., 1989, Geographical variation in mortality from leukaemia and other cancers in England and Wales in relation to proximity to nuclear installations, 1968-1978. British Journal of Cancer, 59, 476-485.
12. COSGROVE, G. E., SELBY, P. B., UPTON, A. C., MITCHELL, T. J., STEELE, M. H. and RUSSELL, W. L., 1993, Lifespan and autopsy findings in the first generation offspring of X-irradiated male mice. Mutational Research in Genetics, Toxicology and Test-Biomonitors of Environmental Occupational Exposure, 319, 71-79.
13. Cox, R., 1992, Transgeneration carcinogenesis: are there genes that break ihr rules? Radiological Protection Bulletin, 129, 15-23.
14. DEXTER, T. M., SCHOFIELD, R., LAJTHA, L. G. and MOORE, M., 1974, Studies on the mechanisms of chemical leukaemogenesis. British Journal of Cancer, 30, 325-331.
15. DOLL, R., EVANS, H. J. and DARBY, S. C., 1994, Paternal exposure not to blame. Nature, 367, 678-680.
16. DRAPER, G. J., LITTLE, M. P., SORAHAN, T., KINLEN, L. J., BUNCH, K. J., CONQUEST, A. J., KENDALL, G. M., KNEALE, G. W., LANCASHIRE, R. J., MUIRHEAD, C. R., O'CONNOR, C. M. and VINCENT, T. J., 1997, Cancer in the offspring of radiation workers: a record linkage study. British Medical Journal, 315, 1181-1188.
17. ERFLE, V., SCHMIDT, J., STRAUSS, G. P., HEHLMANN, R. and LUZ, A., 1986, Activation and biological properties of endogenous viruses in radiation osteosarcomagenesis. Leukaemia Research, 10, 905-913.
18. GARDNER, M. J., SNEE, M. P., HALL, A. J., POWEL, C. A., DOWNES, S. and TERRELL, J. D., 1990, Results of a case controlled study of leukaemia and lymphoma among young people near Sellafield Nuclear Plant in West Cumbria. British Medical Journal, 300, 423-429.
19. GRAHAM, S., LEVIN, M. L., LILIENFIELD, A. M., SCHUMAN, L. M., GIBSON, R., DOWD, J. E. and HEMPLEMANN, L., 1966, Preconception, intrauterine and postnatal irradiation as related to leukaemia. National Cancer Institute Monographs, 19, 347-371.
20. GREAVES, M. F. and ALEXANDER, F. E., 1993, An infectious etiology for common acute lymphoblastic leukaemia in childhood? Leukaemia, 7, 349-360.
21. GREEN, D., HOWELLS, G. R., HUMPHREYS, E. R. and VENNART, J., 1975, Localisation of plutonium in mouse testes. Nature, 255, 77-79.
22. HAWKINS, M. M., DRAPER, G.J. and SMITH, R. A., 1989, Cancer among 1,348 offspring of survivors of childhood cancer. International Journal of Cancer, 43, 975-978.
23. HEALTH AND SAFETY EXECUTIVE, 1993, HSE investigation of leukuemia and other cancers in the children of male workers at Sellafield (London: HSE).
24. HEALTH AND SAFETY EXECUTIVE, 1994, HSE investigation of leukaemia and other cancers in the children of male workers at Sellafield: review of the results published in October 1993 (London: HSE).
25. HOLLIDAY, R., 1987, The inheritance of epigenetic defects. Science, 238, 163-170.
26. HOYES, K. P., JOHNSON, C., JOHNSTON, R. E., LENDON, R. G., HENDRY, J. H., SHARMA, H. L. and MORRIS, I. D., 1995, Testicular toxicity of the transferrin binding radionuclide Indium-114m in adult and neonatal rats. Reproductive Toxicology, 9, 297-305.
27. HOYES, K. P., SHARMA, H. L., JACKSON, H., HENDRY, J. H. and MORRIS, I. D., 1994, Spermatogenic and mutagenic damage after paternal exposure to systemic Indium-114m. Radiation Research, 139, 185-193.
28. 224Ra of myeloid leukaemia and osteosarcoma in male CBA mice. International Journal of Radiation Biology, 47, 239-217.
29. 23yPu of myeloid leukaemia and osteosarcoma in female CBA mice. International Journal of Radiation Biology, 51, 331-339.
30. JÄHNER, D., STUHLMANN, H., STEWARD, C. L., HARBERS, K., LOHLER, J., SIMON, I. and JAENISCH, R., 1982, De novo methylation and expression of retroviral genomes during mouse embryogenesis. Nature, 298, 623-628.
31. KADHIM, M. A., LORIMORE, S. A., TOWNSEND, K. M. S., GOODHEAD, D. T., BUCKLE, V. J. and WRIGHT, E. G., 1995, Radiation-induced genomic instability: delayed cytogenic aberrations and apoptosis in primary human bone marrow cell. International Journal of Radiation Biology, 67, 287-293.
32. KINLEN, L. J., 1992, Malignancy in autoimmune disease. Journal of Autoimmunity, 5 (Suppl. A), 363-371.
33. KINLEN, L. J., 1993a, Childhood leukaemia and non-Hodgkin's lymphoma in young people living close to nuclear reprocessing sites. Biomedical Pharmacotherapy, 47, 429-434.
34. KINLEN, L. J., 1993b, Can paternal preconceptional radiation account for the increase of leukaemia and non-Hodgkin's lymphoma in Seascale? British Medical Journal, 307, 444-445.
35. KINLEN, L. J., 1997, High contact paternal occupations, infection and childhood leukaemia: five studies of unusual population-mixing of adults. British Journal of Cancer, 76, 1539-1545.
36. KINLEN, L. J., CLARK, K. and BALKWILL, A., 1993a, Paternal preconceptional radiation exposure in the nuclear industry and leukaemia and non-Hodgkin's lymphoma in young people in Scotland. British Medical Journal, 306, 1153-1158.
37. KINLEN, L. J., CLARKE, K. and HUDSON, C., 1990, Evidence from population mixing in British new towns 1946-1985 of an infective basis for childhood leukaemia. Lancet, 336, 944-945.
38. KINLEN, L. J., DICKSON, M. and STILLER, C. A., 1995, Childhood leukaemia and nou-Hodgkin's lymphoma near large rural construction sites, with a comparison with Sellafield nuclear site. British Medical Journal, 310, 763-768.
39. KINLEN, L. J. and HUDSON, C., 1991, Childhood leukaemia and poliomyelitis in relation to military encampments in England and Wales in the period of national military service, 1950 1963. British Medical Journal, 303, 1357-1362.
40. KINLEN, L. J. and JOHN, S. M., 1994, Wartime evacuation and mortality from childhood leukaemia in England and Wales in 1945 1949. British Medical Journal, 309, 1197-1202.
41. KINLEN, L. J., O'BRIEN, F., CLARKE, K., BALKWILL, A. and MATTHEWS, F., 1993b, Rural population mixing and childhood leukaemia: effects of the North Sea oil industry in Scotland, British Medical Journal, 306, 743-748.
42. KINLEN, L. J. and PETRIDOU, E., 1995, Childhood leukemia and rural population movements: Greece, Italy and other countries. Cancer Causes and Control, 6, 445-450.
43. KNEALE, G. W. and STEWART, A. M., 1980, Pre-conception X-rays and childhood cancers. British Journal of Cancer, 41, 222-226.
44. LI, F. P., FINE, W., JAFFE, N., HOLMES, G. E. and HOLMES, F. F., 1979, Offspring of patients treated for cancer in childhood. Journal of the National Cancer Institute, 62, 1193-1197.
45. LITTLE, M. P., WAKEFORD, R. and CHARLES, M. W., 1994a, An analysis of leukaemia, lymphoma and other malignancies together with certain categories of non-cancer mortality in the first generation offspring (f-1) of the Japanese bomb survivors. Journal of Radiological Protection, 14, 203-218.
46. LITTLE, M. P., WAKEFORD, R. and CHARLES, M. W., 1994b, A comparison of the risks of leukaemia in the offspring of the Sellafield workforce born in Seascale and those born elsewhere in West Cumbria with the risks in the offspring of the Ontario and Scottish workforces and the Japanese bomb survivors. Journal of Radiological Protection, 14, 187-201.
47. LITTLE, M. P., WAKEFORD, R., CHARLES, M. W. and ANDERSSON, M., 1996, A comparison of the risks of leukaemia and NHL in the first generation offspring (Fl) of the Danish Thorotrast patients with those observed in other studies of parental preconception irradiation. Journal of Radiological Protection, 16, 1-9.
48. LORD, B. L., WOOLFORD, L. B., WANG, L., STONES, V. A., MCDONALD, D., LORIMORE, S. A-, PAPWORTH, D., WRIGHT, E, G. and SCOTT, D., 198a, Tumour induction by methyl-nitroso-ura following preconceptional paternal contamination with plutonium-239. British Journal of Cancer, 78, 301-311.
49. LORD, B. L., WOOLFORD, L. B., WANG, L., STONES, V. A., MCDoNALD, D., LORIMORE, S. A., WRIGHT, E. G. and SCOTT, D., 1998b, Induction of lympho-haemopoietic. malignancy: impact of preconception paternal irradiation. International Journal of Radiation Biology, 74, 721-728.
50. LUKE, G. A., RICHES, A. C. and BUYANT, P. E., 1997, Genomic instability in haemopoielic cells of F1 generation mice of irradiated male parents. Mutagenesis, 12, 147-152.
51. LUNNING, K. G., FROLLEN, H. and NILSSON, A., 1976, Genetic effects of P-239 salt injections in male mice. Mutation Research, 34, 539-542.
52. MAJOR, T. R., 1979, Induction of myeloid leukaemia by whole body single exposure of GBA male mice to X-rays. British Journal of Cancer, 40, 903-913.
53. MCLAUGHLIN, J. R., KING, W. D., ANDERSON, T. W., CLARKE, E. A. and ASHMORE, J. P., 1993a, Paternal radiation exposure and leukaemia in offspring: the Ontario ease control study. British Medical Journal, 307, 959-66.
54. MCLAUGLIN, J. R., KING, W. D., ANDERSSON, T. W.M., CLARKE, E. A. and ASHMORE, J. P., 1993b, Paternal radiation exposure and leukaemia in offspring: the Ontario case control study (editorial correction to McLaughlin et al. 1993a). British Medical Journal, 307, 1257.
55. MITRETTER, K., SCHMIDT, J., LUZ, A., ATKINSON, M. J., HOFLER, H., ERFLE, and STRACSS, G. P., 1994, Disruption of the murine p53 gene by insertion of an endogenous retrovirus-like element (Etm) in a cell line from radiation induced osteosarcoma. Virology, 200, 837-841.
56. MULVIHILL, J. J., MYERS, M. H., CONNELLY, R. R., BYRNE, J., AUSTIN, D. F., BRAGG, K., COOK, J. W., HASSINGER, D. D., HOLMES, F. F., HOLMES, G. F., KRAUSE, M. R., LATOURETTF, H. B., MEIGS, J. W., NAUGHTON, M. D., STEINHORN, S. C., STRONG, L. C., TETA, M. J. and WEVER, P. J., 1987, Cancer in offspring of long-term survivors of childhood and adolescent cancer. Lancet, i, 813-817.
57. NEWS, 1998, 'Uncertainty over leukaemia link to nuclear reactor'. Nature, 396, 402.
58. NOMURA, T., 1982, Parental exposure to X-rays and chemicals induces heritable tumours and anomalies in mice. Nature, 296, 575-577.
59. NOMURA, T., 1983, X-ray induced germ line mutation leading to tumours and its manifestation in mice given urethane post-natally. Mutation Research, 121, 59-66.
60. NOMURA, T., 1990, Of mice and men? Nature, 345, 671.
61. NOMURA, T., 1991, Paternal exposure to radiation and offspring cancer in mice: reanalysis and new evidences. Journal of Radiation Research, 2, 64-72.
62. 239Pu in mice. http://www.nrpb.org.uk/mice-is.htm
63. PARKER, L., CRAFT, A. W., SMITH, J., DICKENSON, H., WAKEFORD, R., BINKS, K., MCELVENNY, D, SCOTT, L. and SLOVAK, A., 1993, Geographical distributions of preconceptional radiation closes to fathers employed at the Sellafield nuclear installation, West Cumbria. British Medical Journal, 307, 966-971.
64. ROMAN, E., BERAL, V., CARPENTER, L., WATSON, A., BARTON, C., RYDER, H. and ASTON, D. L., 1987, Childhood leukaemia in the West Berkshire and Basingstoke and North Hampshire District Health Authorities in relation to nuclear establishments in the vicinity. British Medical Journal, 294, 597-602.
65. ROMAN, E., WATSON, A., BERAL, V., BUCKLE, S., BULL, D., BAKER, K., RYDER, H. and BARTON, C., 1993, Case-control study of leukaemia and non-Hodgkin's lymphoma among children aged 0-4 years living in West Berkshire and North Hampshire health districts. British Medical Journal 306, 615-621.
66. ROSE, K. S. B., 1990, Pre-1989 epidemiological surveys of low-level dose pre-conception irradiation. Journal of Radiological Protection, 10, 177-184.
67. SCHWARTZ, D. and DENNIS, E., 1986, Transposase activity of the AC controlling element in maize is regulated by its degree of methylation. Molecular and General Genetics, 205, 476-482.
68. SEARLE, A. G., BEECHEY, C. V., GREEN, D. and HUMPHREYS, E. R., 1976, Cytogenetic effects of protracted exposure to alpha-particles from plutonium-239 and to y-rats from cobalt-60 compared in male mice. Mutation Research, 41, 297-310.
69. SELBY, P. B., 1990, Experimental induction of dominant mutations in mammals by ionizing radiations and chemicals. Issues and Reviews in Teratology, 5, 181-253.
70. SHIONO, P. H., OHUNG, C. S. and MYRIANTHOPOULOS, N. C., 1980, Preconception radiation, intrauterine diagnostic radiation, and childhood neoplasia. Journal of the National Cancer Institute, 65, 681-686.
71. SHU, X. O., GAO, Y. T., BRINTON, L. A., LINET, M. S., TU, J. T., ZHENG, W. and FRAUMENI, J. F., 1988, A population-based case -control study of childhood leukaemia in Shanghai. Cancer, 62, 635-644.
72. SHU, X. O., JIN, F., LINT, M. S., ZHENG, W., CLEMENS, J., MILLS, J. and GAO, Y. T., 1994a, Diagnostic X-ray and ultrasound exposure and risk of childhood cancer. British Journal of Cancer, 70, 531-536.
73. SHU, X. O., REAMAN, G. H., LAMPKIN, B., SATHER, H. N., PENDERGRASS, T. W., ROBISON, L. L., and for the investigators of the Children's Cancer Group, 1994b, Association of paternal diagnostic X-ray exposure with risk of infant leukaemia. Cancer Epidemiological Biomakers Preview, 3, 645-653.
74. STEVENS, W., BREUNGER, F. W. and STOVER, B. J., 1968, In vivo studies on the interactions of Pu-IV with blood constituents. Radiation Research 33, 490-500.
75. TAKAHASHI, T., WATENABE, H., DOHI, K. and ITO, A., 1992, 252cf relative biological effectiveness and inheritable effect of fission neutrons in mouse liver tumorigenesis. Cancer Research, 52, 1948-1953.
76. TAYLOR, G. M. and BIRCH, G. M., 1996, The hereditary basis of human leukaemia. In Leukaemia, 6th edition, edited by E. S. Henderson, T. A. Lister and M. F. Greaves (Philadelphia: Saunders Co).
77. URQUHART, J. H., BLACK, R. J., MUIRHEAD, M. J., SHARP, L., MAXWELL, M., EDEN, O. B. and JONES, D. A., 1991, Case-control study of leukaemia and non-Hodgkin's lymphoma in children in Caithness near the Dounreay nuclear installation. British Medical Journal, 302, 687-692.
78. VOROBTSOVA, I. E., 1989, Increased rancer risk as a genetic effect of ionising radiation. In Perinatal and Multigenerational Carcinogenesis, edited by N. P. Napalkov, J. M. Rice, L. Tomatis and H. Yamasaki (Lyon, France: International Agency for Research on Cancer), pp. 389-401.
79. VOROBTSOVA, I. E., 1995, Increased cancer risk and chromosomal instability in irradiated parents progeny (abstract). In Proceedings of the 25th Annual Meeting of the European Environmental Mutagenesis Society, p. 52.
80. VOROBTSOVA, I. E., ALIYAKPAROVA, C. M. and ANISIMOV, V. N., 1993, Promotion of skin cancers by 12-0-tetradecanoylphorbol-13-acetate in two generations of descendants of male mice exposed to X-irradiation. Mutation Research, 287, 207-216.
81. VOROBTSOVA, I. E. and KITAEV, E. M., 1988, Urethane-induced lung adenomas in the first generation progeny of irradiated male mice. Carcinogenesis, 9, 1931-1934.
82. VOROBTSOVA, I. E. and VOREB'EVA, M. V., 1992, The chromosomal radiosensitivity of children whose parents were exposed to antitumour radiochemotherapy (in Russian). Biulleten Eksperimentalnoi Biologii I Meditsiny, 114, 655-657.
83. VOROBTSOVA, I. E., VOREB'EVA, M. V., BOGOMAZOVA, A. N., PIUKKENEN, A. and AKKHANGEL'SKAIA, T. T., 1995, The cytogenic examination of children in the Saint Petersburg region who suffered as a result of the accident at the Chernobyl Atomic Electric Power Station. The frequency for unstable aberrations in the peripheral blood lymphocytes (in Russian). Radiation Biology and Radioecology, 35, 630-635.
84. WAKEFORD, R. and PARKER, L., 1996, Leukaemia and non-Hodgkin's lymphoma in young persons resident in small areas of West Cumbria in relation to paternal preconceptional irradiation. British Journal of Cancer, 73, 672-679.
85. WAKEFORD, R. and TAWN, E. J., 1994, Childhood leukaemia and Sellafield: the legal cases. Journal of Radiological Protection, 14, 293-316.
86. WAKEFORD, R., TAWN, E. J., MCELVENNY, D. M., BINKS, K., SCOTT, L. E. and PARKER, L., 1994, Journal of Radiological Protection, 14, 17-24.
87. YOSHIMOTO, Y., 1990, Cancer risk among children of atomic bomb survivors. A review of RERF epidemiologic studies. Radiation Effects Research Foundation. Journal of the American Medical Association, 264, 622-623.
88. YOSHIMOTO, Y., NEEL, J. V., SCHULL, W. J., KATO, H., SODA, M., ETO, R. and MABUCHI, K., 1990, Malignant tumors during the first 2 decades of life in the offspring of atomic bomb survivors. American Journal of Human Genetics. 46, 1041-1052.
89. YOSHIMOTO, Y., SCHULL, W. J., KATO, H. and NEEL, J. V., 1991, Mortality among the offspring (F1) of atomic bomb survivors, 1946 1985. Journal of Radiation Research 32, 327-351.