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. 1998 Aug;106(Suppl 4):937–946. doi: 10.1289/ehp.98106s4937

Biomarkers of leukemia risk: benzene as a model.

M T Smith 1, L Zhang 1
PMCID: PMC1533331  PMID: 9703476

Abstract

Although relatively rare, leukemias place a considerable financial burden on society and cause psychologic trauma to many families. Leukemia is the most common cancer in children. The causes of leukemia in adults and children are largely unknown, but occupational and environmental factors are strongly suspected. Genetic predisposition may also play a major role. Our aim is to use molecular epidemiology and toxicology to find the cause of leukemia and develop biomarkers of leukemia risk. We have studied benzene as a model chemical leukemogen, and we have identified risk factors for susceptibility to benzene toxicity. Numerous studies have associated exposure to benzene with increased levels of chromosome aberrations in circulating lymphocytes of exposed workers. Increased levels of chromosome aberrations have, in turn, been correlated with a heightened risk of cancer, especially for hematologic malignancy, in two recent cohort studies in Europe. Conventional chromosome analysis is laborious, however, and requires highly trained personnel. Further, it lacks statistical power, as only a small number of cells can be examined. The recently developed fluorescence in situ hybridization (FISH) and polymerase chain reaction (PCR)-based technologies have allowed the detection of specific chromosome aberrations. These techniques are far less time consuming and are more sensitive than classical chromosomal analysis. Because leukemias commonly show a variety of specific chromosome aberrations, detection of these aberrations by FISH and PCR in peripheral blood may provide improved biomarkers of leukemia risk.

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Selected References

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  1. Aksoy M., Dinçol K., Akgün T., Erdem S., Dinçol G. Haematological effects of chronic benzene poisoning in 217 workers. Br J Ind Med. 1971 Jul;28(3):296–302. doi: 10.1136/oem.28.3.296. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alexander F. E., Leon D. A., Cartwright R. A. Isolation, car ownership, and small area variation in incidence of acute lymphoblastic leukaemia in children. Paediatr Perinat Epidemiol. 1996 Oct;10(4):411–417. doi: 10.1111/j.1365-3016.1996.tb00066.x. [DOI] [PubMed] [Google Scholar]
  3. Aul C., Gattermann N., Schneider W. Age-related incidence and other epidemiological aspects of myelodysplastic syndromes. Br J Haematol. 1992 Oct;82(2):358–367. doi: 10.1111/j.1365-2141.1992.tb06430.x. [DOI] [PubMed] [Google Scholar]
  4. Biernaux C., Loos M., Sels A., Huez G., Stryckmans P. Detection of major bcr-abl gene expression at a very low level in blood cells of some healthy individuals. Blood. 1995 Oct 15;86(8):3118–3122. [PubMed] [Google Scholar]
  5. Bithell J. F., Draper G. J. Apparent association between benzene and childhood leukaemia: methodological doubts concerning a report by Knox. J Epidemiol Community Health. 1995 Aug;49(4):437–439. doi: 10.1136/jech.49.4.437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bonassi S., Abbondandolo A., Camurri L., Dal Prá L., De Ferrari M., Degrassi F., Forni A., Lamberti L., Lando C., Padovani P. Are chromosome aberrations in circulating lymphocytes predictive of future cancer onset in humans? Preliminary results of an Italian cohort study. Cancer Genet Cytogenet. 1995 Feb;79(2):133–135. doi: 10.1016/0165-4608(94)00131-t. [DOI] [PubMed] [Google Scholar]
  7. Buckley J. D., Robison L. L., Swotinsky R., Garabrant D. H., LeBeau M., Manchester P., Nesbit M. E., Odom L., Peters J. M., Woods W. G. Occupational exposures of parents of children with acute nonlymphocytic leukemia: a report from the Childrens Cancer Study Group. Cancer Res. 1989 Jul 15;49(14):4030–4037. [PubMed] [Google Scholar]
  8. Chan C. C., Spengler J. D., Ozkaynak H., Lefkopoulou M. Commuter exposures to VOCs in Boston, Massachusetts. J Air Waste Manage Assoc. 1991 Dec;41(12):1594–1600. doi: 10.1080/10473289.1991.10466955. [DOI] [PubMed] [Google Scholar]
  9. Chen H., Sandler D. P., Taylor J. A., Shore D. L., Liu E., Bloomfield C. D., Bell D. A. Increased risk for myelodysplastic syndromes in individuals with glutathione transferase theta 1 (GSTT1) gene defect. Lancet. 1996 Feb 3;347(8997):295–297. doi: 10.1016/s0140-6736(96)90468-7. [DOI] [PubMed] [Google Scholar]
  10. Compton P. J., Hooper K., Smith M. T. Human somatic mutation assays as biomarkers of carcinogenesis. Environ Health Perspect. 1991 Aug;94:135–141. doi: 10.1289/ehp.94-1567966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Crane M. M., Strom S. S., Halabi S., Berman E. L., Fueger J. J., Spitz M. R., Keating M. J. Correlation between selected environmental exposures and karyotype in acute myelocytic leukemia. Cancer Epidemiol Biomarkers Prev. 1996 Aug;5(8):639–644. [PubMed] [Google Scholar]
  12. Cremer T., Lichter P., Borden J., Ward D. C., Manuelidis L. Detection of chromosome aberrations in metaphase and interphase tumor cells by in situ hybridization using chromosome-specific library probes. Hum Genet. 1988 Nov;80(3):235–246. doi: 10.1007/BF01790091. [DOI] [PubMed] [Google Scholar]
  13. Ding X. J., Li Y., Ding Y., Yang H. Z. Chromosome changes in patients with chronic benzene poisoning. Chin Med J (Engl) 1983 Sep;96(9):681–685. [PubMed] [Google Scholar]
  14. Downing J. R., Head D. R., Curcio-Brint A. M., Hulshof M. G., Motroni T. A., Raimondi S. C., Carroll A. J., Drabkin H. A., Willman C., Theil K. S. An AML1/ETO fusion transcript is consistently detected by RNA-based polymerase chain reaction in acute myelogenous leukemia containing the (8;21)(q22;q22) translocation. Blood. 1993 Jun 1;81(11):2860–2865. [PubMed] [Google Scholar]
  15. Eastmond D. A., Pinkel D. Detection of aneuploidy and aneuploidy-inducing agents in human lymphocytes using fluorescence in situ hybridization with chromosome-specific DNA probes. Mutat Res. 1990 Oct;234(5):303–318. doi: 10.1016/0165-1161(90)90041-l. [DOI] [PubMed] [Google Scholar]
  16. Eastmond D. A., Rupa D. S., Hasegawa L. S. Detection of hyperdiploidy and chromosome breakage in interphase human lymphocytes following exposure to the benzene metabolite hydroquinone using multicolor fluorescence in situ hybridization with DNA probes. Mutat Res. 1994 Jul;322(1):9–20. doi: 10.1016/0165-1218(94)90028-0. [DOI] [PubMed] [Google Scholar]
  17. Eastmond D. A., Schuler M., Rupa D. S. Advantages and limitations of using fluorescence in situ hybridization for the detection of aneuploidy in interphase human cells. Mutat Res. 1995 Dec;348(4):153–162. doi: 10.1016/0165-7992(95)90003-9. [DOI] [PubMed] [Google Scholar]
  18. Eastmond D. A., Smith M. T., Ruzo L. O., Ross D. Metabolic activation of phenol by human myeloperoxidase and horseradish peroxidase. Mol Pharmacol. 1986 Dec;30(6):674–679. [PubMed] [Google Scholar]
  19. Erdoğan G., Aksoy M. Cytogenetic studies in thirteen patients with pancytopenia and leukaemia associated with long-term exposure to benzene. New Istanbul Contrib Clin Sci. 1973 Oct;10(4):230–247. [PubMed] [Google Scholar]
  20. Fleming A. F. Benzene in petrol: a continuing hazard. Lancet. 1990 Oct 27;336(8722):1076–1077. doi: 10.1016/0140-6736(90)92556-w. [DOI] [PubMed] [Google Scholar]
  21. Ford A. M., Pombo-de-Oliveira M. S., McCarthy K. P., MacLean J. M., Carrico K. C., Vincent R. F., Greaves M. Monoclonal origin of concordant T-cell malignancy in identical twins. Blood. 1997 Jan 1;89(1):281–285. [PubMed] [Google Scholar]
  22. Ford A. M., Ridge S. A., Cabrera M. E., Mahmoud H., Steel C. M., Chan L. C., Greaves M. In utero rearrangements in the trithorax-related oncogene in infant leukaemias. Nature. 1993 May 27;363(6427):358–360. doi: 10.1038/363358a0. [DOI] [PubMed] [Google Scholar]
  23. Forni A. M., Cappellini A., Pacifico E., Vigliani E. C. Chromosome changes and their evolution in subjects with past exposure to benzene. Arch Environ Health. 1971 Nov;23(5):385–391. doi: 10.1080/00039896.1971.10666024. [DOI] [PubMed] [Google Scholar]
  24. Forni A. Chromosome changes and benzene exposure. A review. Rev Environ Health. 1979;3(1):5–17. [PubMed] [Google Scholar]
  25. Forni A. Chromosome studies in workers exposed to benzene or toluene or both. Arch Environ Health. 1971 Mar;22(3):373–378. [PubMed] [Google Scholar]
  26. Forni A., Moreo L. Chromosome studies in a case of benzene-induced erythroleukaemia. Eur J Cancer. 1969 Nov;5(5):459–463. doi: 10.1016/0014-2964(69)90099-1. [DOI] [PubMed] [Google Scholar]
  27. Forni A., Moreo L. Cytogenetic studies in a case of benzene leukaemia. Eur J Cancer. 1967 Nov;3(4):251–255. doi: 10.1016/0014-2964(67)90005-9. [DOI] [PubMed] [Google Scholar]
  28. Franchini G. Molecular mechanisms of human T-cell leukemia/lymphotropic virus type I infection. Blood. 1995 Nov 15;86(10):3619–3639. [PubMed] [Google Scholar]
  29. Gale K. B., Ford A. M., Repp R., Borkhardt A., Keller C., Eden O. B., Greaves M. F. Backtracking leukemia to birth: identification of clonotypic gene fusion sequences in neonatal blood spots. Proc Natl Acad Sci U S A. 1997 Dec 9;94(25):13950–13954. doi: 10.1073/pnas.94.25.13950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Goldstein B. D. Benzene toxicity. Occup Med. 1988 Jul-Sep;3(3):541–554. [PubMed] [Google Scholar]
  31. Gray J. W., Pinkel D., Brown J. M. Fluorescence in situ hybridization in cancer and radiation biology. Radiat Res. 1994 Mar;137(3):275–289. [PubMed] [Google Scholar]
  32. Greaves M. F. Aetiology of acute leukaemia. Lancet. 1997 Feb 1;349(9048):344–349. doi: 10.1016/s0140-6736(96)09412-3. [DOI] [PubMed] [Google Scholar]
  33. Hagmar L., Brøgger A., Hansteen I. L., Heim S., Högstedt B., Knudsen L., Lambert B., Linnainmaa K., Mitelman F., Nordenson I. Cancer risk in humans predicted by increased levels of chromosomal aberrations in lymphocytes: Nordic study group on the health risk of chromosome damage. Cancer Res. 1994 Jun 1;54(11):2919–2922. [PubMed] [Google Scholar]
  34. Hansen N. E., Karle H., Jensen O. M. Trends in the incidence of leukemia in Denmark, 1943-77: an epidemiologic study of 14,000 patients. J Natl Cancer Inst. 1983 Oct;71(4):697–701. [PubMed] [Google Scholar]
  35. Hartle R. Exposure to methyl tert-butyl ether and benzene among service station attendants and operators. Environ Health Perspect. 1993 Dec;101 (Suppl 6):23–26. doi: 10.1289/ehp.93101s623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Hasle H., Kerndrup G., Jacobsen B. B. Childhood myelodysplastic syndrome in Denmark: incidence and predisposing conditions. Leukemia. 1995 Sep;9(9):1569–1572. [PubMed] [Google Scholar]
  37. Hayes R. B., Yin S. N., Dosemeci M., Li G. L., Wacholder S., Chow W. H., Rothman N., Wang Y. Z., Dai T. R., Chao X. J. Mortality among benzene-exposed workers in China. Environ Health Perspect. 1996 Dec;104 (Suppl 6):1349–1352. doi: 10.1289/ehp.961041349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Infante P. F., Schwartz E., Cahill R. Benzene in petrol: a continuing hazard. Lancet. 1990 Sep 29;336(8718):814–815. doi: 10.1016/0140-6736(90)93282-t. [DOI] [PubMed] [Google Scholar]
  39. Jakobsson R., Ahlbom A., Bellander T., Lundberg I. Acute myeloid leukemia among petrol station attendants. Arch Environ Health. 1993 Jul-Aug;48(4):255–259. doi: 10.1080/00039896.1993.9940369. [DOI] [PubMed] [Google Scholar]
  40. Jensen R. H., Bigbee W. L. Direct immunofluorescence labeling provides an improved method for the glycophorin A somatic cell mutation assay. Cytometry. 1996 Apr 1;23(4):337–343. doi: 10.1002/(SICI)1097-0320(19960401)23:4<337::AID-CYTO10>3.0.CO;2-U. [DOI] [PubMed] [Google Scholar]
  41. Ji B. T., Shu X. O., Linet M. S., Zheng W., Wacholder S., Gao Y. T., Ying D. M., Jin F. Paternal cigarette smoking and the risk of childhood cancer among offspring of nonsmoking mothers. J Natl Cancer Inst. 1997 Feb 5;89(3):238–244. doi: 10.1093/jnci/89.3.238. [DOI] [PubMed] [Google Scholar]
  42. Kagan J. Molecular biology of chromosomal aberrations in leukemia/lymphoma. Hematol Pathol. 1993;7(3):159–201. [PubMed] [Google Scholar]
  43. Karacić V., Skender L., Bosner-Cucancić B., Bogadi-Sare A. Possible genotoxicity in low level benzene exposure. Am J Ind Med. 1995 Mar;27(3):379–388. doi: 10.1002/ajim.4700270307. [DOI] [PubMed] [Google Scholar]
  44. Karacić V., Skender L., Prpić-Majić D. Occupational exposure to benzene in the shoe industry. Am J Ind Med. 1987;12(5):531–536. doi: 10.1002/ajim.4700120507. [DOI] [PubMed] [Google Scholar]
  45. Kawai T., Yamaoka K., Uchida Y., Ikeda M. Benzene exposure in a Japanese petroleum refinery. Toxicol Lett. 1990 Jul;52(2):135–139. doi: 10.1016/0378-4274(90)90147-e. [DOI] [PubMed] [Google Scholar]
  46. Kazak A. E., Barakat L. P., Meeske K., Christakis D., Meadows A. T., Casey R., Penati B., Stuber M. L. Posttraumatic stress, family functioning, and social support in survivors of childhood leukemia and their mothers and fathers. J Consult Clin Psychol. 1997 Feb;65(1):120–129. doi: 10.1037//0022-006x.65.1.120. [DOI] [PubMed] [Google Scholar]
  47. Kessler I. I., Lilienfeld A. M. Perspectives in the epidemiology of leukemia. Adv Cancer Res. 1969;12:225–302. doi: 10.1016/s0065-230x(08)60332-2. [DOI] [PubMed] [Google Scholar]
  48. Kishi R., Katakura Y., Yuasa J., Miyake H. [Association of parents' occupational exposure to cancer in children. A case-control study of acute lymphoblastic leukemia]. Sangyo Igaku. 1993 Nov;35(6):515–529. doi: 10.1539/joh1959.35.515. [DOI] [PubMed] [Google Scholar]
  49. Knox E. G., Gilman E. A. Hazard proximities of childhood cancers in Great Britain from 1953-80. J Epidemiol Community Health. 1997 Apr;51(2):151–159. doi: 10.1136/jech.51.2.151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Knox E. G. Leukaemia clusters in childhood: geographical analysis in Britain. J Epidemiol Community Health. 1994 Aug;48(4):369–376. doi: 10.1136/jech.48.4.369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Koop D. R., Laethem C. L., Schnier G. G. Identification of ethanol-inducible P450 isozyme 3a (P450IIE1) as a benzene and phenol hydroxylase. Toxicol Appl Pharmacol. 1989 Apr;98(2):278–288. doi: 10.1016/0041-008x(89)90233-0. [DOI] [PubMed] [Google Scholar]
  52. Linet M. S., Hatch E. E., Kleinerman R. A., Robison L. L., Kaune W. T., Friedman D. R., Severson R. K., Haines C. M., Hartsock C. T., Niwa S. Residential exposure to magnetic fields and acute lymphoblastic leukemia in children. N Engl J Med. 1997 Jul 3;337(1):1–7. doi: 10.1056/NEJM199707033370101. [DOI] [PubMed] [Google Scholar]
  53. Liu Y., Hernandez A. M., Shibata D., Cortopassi G. A. BCL2 translocation frequency rises with age in humans. Proc Natl Acad Sci U S A. 1994 Sep 13;91(19):8910–8914. doi: 10.1073/pnas.91.19.8910. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. London S. J., Lehman T. A., Taylor J. A. Myeloperoxidase genetic polymorphism and lung cancer risk. Cancer Res. 1997 Nov 15;57(22):5001–5003. [PubMed] [Google Scholar]
  55. Look A. T. Oncogenic transcription factors in the human acute leukemias. Science. 1997 Nov 7;278(5340):1059–1064. doi: 10.1126/science.278.5340.1059. [DOI] [PubMed] [Google Scholar]
  56. Major J., Jakab M., Kiss G., Tompa A. Chromosome aberration, sister-chromatid exchange, proliferative rate index, and serum thiocyanate concentration in smokers exposed to low-dose benzene. Environ Mol Mutagen. 1994;23(2):137–142. doi: 10.1002/em.2850230211. [DOI] [PubMed] [Google Scholar]
  57. Matutes E., Morilla R., Farahat N., Carbonell F., Swansbury J., Dyer M., Catovsky D. Definition of acute biphenotypic leukemia. Haematologica. 1997 Jan-Feb;82(1):64–66. [PubMed] [Google Scholar]
  58. McKinney P. A., Alexander F. E., Cartwright R. A., Parker L. Parental occupations of children with leukaemia in west Cumbria, north Humberside, and Gateshead. BMJ. 1991 Mar 23;302(6778):681–687. doi: 10.1136/bmj.302.6778.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Midzenski M. A., McDiarmid M. A., Rothman N., Kolodner K. Acute high dose exposure to benzene in shipyard workers. Am J Ind Med. 1992;22(4):553–565. doi: 10.1002/ajim.4700220410. [DOI] [PubMed] [Google Scholar]
  60. Mitelman F., Nilsson P. G., Brandt L., Alimena G., Gastaldi R., Dallapiccola B. Chromosome pattern, occupation, and clinical features in patients with acute nonlymphocytic leukemia. Cancer Genet Cytogenet. 1981 Nov;4(3):197–214. doi: 10.1016/0165-4608(81)90014-5. [DOI] [PubMed] [Google Scholar]
  61. Mott M. G., Boyse J., Hewitt M., Radford M. Do mutations at the glycophorin A locus in patients treated for childhood Hodgkin's disease predict secondary leukaemia? Lancet. 1994 Apr 2;343(8901):828–829. doi: 10.1016/s0140-6736(94)92027-3. [DOI] [PubMed] [Google Scholar]
  62. Natarajan A. T., Boei J. J., Darroudi F., Van Diemen P. C., Dulout F., Hande M. P., Ramalho A. T. Current cytogenetic methods for detecting exposure and effects of mutagens and carcinogens. Environ Health Perspect. 1996 May;104 (Suppl 3):445–448. doi: 10.1289/ehp.96104s3445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Pedersen-Bjergaard J., Pedersen M., Roulston D., Philip P. Different genetic pathways in leukemogenesis for patients presenting with therapy-related myelodysplasia and therapy-related acute myeloid leukemia. Blood. 1995 Nov 1;86(9):3542–3552. [PubMed] [Google Scholar]
  64. Pedersen-Bjergaard J., Philip P. Two different classes of therapy-related and de-novo acute myeloid leukemia? Cancer Genet Cytogenet. 1991 Aug;55(1):119–124. doi: 10.1016/0165-4608(91)90246-q. [DOI] [PubMed] [Google Scholar]
  65. Picciano D. Cytogenetic study of workers exposed to benzene. Environ Res. 1979 Jun;19(1):33–38. doi: 10.1016/0013-9351(79)90031-8. [DOI] [PubMed] [Google Scholar]
  66. Piedrafita F. J., Molander R. B., Vansant G., Orlova E. A., Pfahl M., Reynolds W. F. An Alu element in the myeloperoxidase promoter contains a composite SP1-thyroid hormone-retinoic acid response element. J Biol Chem. 1996 Jun 14;271(24):14412–14420. doi: 10.1074/jbc.271.24.14412. [DOI] [PubMed] [Google Scholar]
  67. Pui C. H. Childhood leukemias. N Engl J Med. 1995 Jun 15;332(24):1618–1630. doi: 10.1056/NEJM199506153322407. [DOI] [PubMed] [Google Scholar]
  68. Ross D. Metabolic basis of benzene toxicity. Eur J Haematol Suppl. 1996;60:111–118. doi: 10.1111/j.1600-0609.1996.tb01656.x. [DOI] [PubMed] [Google Scholar]
  69. Ross D., Traver R. D., Siegel D., Kuehl B. L., Misra V., Rauth A. M. A polymorphism in NAD(P)H:quinone oxidoreductase (NQO1): relationship of a homozygous mutation at position 609 of the NQO1 cDNA to NQO1 activity. Br J Cancer. 1996 Sep;74(6):995–996. doi: 10.1038/bjc.1996.477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Rosvold E. A., McGlynn K. A., Lustbader E. D., Buetow K. H. Identification of an NAD(P)H:quinone oxidoreductase polymorphism and its association with lung cancer and smoking. Pharmacogenetics. 1995 Aug;5(4):199–206. doi: 10.1097/00008571-199508000-00003. [DOI] [PubMed] [Google Scholar]
  71. Rothman N., Haas R., Hayes R. B., Li G. L., Wiemels J., Campleman S., Quintana P. J., Xi L. J., Dosemeci M., Titenko-Holland N. Benzene induces gene-duplicating but not gene-inactivating mutations at the glycophorin A locus in exposed humans. Proc Natl Acad Sci U S A. 1995 Apr 25;92(9):4069–4073. doi: 10.1073/pnas.92.9.4069. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Rothman N., Li G. L., Dosemeci M., Bechtold W. E., Marti G. E., Wang Y. Z., Linet M., Xi L. Q., Lu W., Smith M. T. Hematotoxicity among Chinese workers heavily exposed to benzene. Am J Ind Med. 1996 Mar;29(3):236–246. doi: 10.1002/(SICI)1097-0274(199603)29:3<236::AID-AJIM3>3.0.CO;2-O. [DOI] [PubMed] [Google Scholar]
  73. Rothman N., Smith M. T., Hayes R. B., Li G. L., Irons R. D., Dosemeci M., Haas R., Stillman W. S., Linet M., Xi L. Q. An epidemiologic study of early biologic effects of benzene in Chinese workers. Environ Health Perspect. 1996 Dec;104 (Suppl 6):1365–1370. doi: 10.1289/ehp.961041365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Rothman N., Smith M. T., Hayes R. B., Traver R. D., Hoener B., Campleman S., Li G. L., Dosemeci M., Linet M., Zhang L. Benzene poisoning, a risk factor for hematological malignancy, is associated with the NQO1 609C-->T mutation and rapid fractional excretion of chlorzoxazone. Cancer Res. 1997 Jul 15;57(14):2839–2842. [PubMed] [Google Scholar]
  75. Rushton L. Benzene exposure in the petroleum distribution industry associated with leukemia in the United Kingdom: overview of the methodology of a case-control study. Environ Health Perspect. 1996 Dec;104 (Suppl 6):1371–1374. doi: 10.1289/ehp.961041371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Sandler D. P., Collman G. W. Cytogenetic and environmental factors in the etiology of the acute leukemias in adults. Am J Epidemiol. 1987 Dec;126(6):1017–1032. doi: 10.1093/oxfordjournals.aje.a114741. [DOI] [PubMed] [Google Scholar]
  77. Sandler D. P., Ross J. A. Epidemiology of acute leukemia in children and adults. Semin Oncol. 1997 Feb;24(1):3–16. [PubMed] [Google Scholar]
  78. Sasiadek M., Jagielski J., Smolik R. Localization of breakpoints in the karyotype of workers professionally exposed to benzene. Mutat Res. 1989 Oct;224(2):235–240. doi: 10.1016/0165-1218(89)90161-4. [DOI] [PubMed] [Google Scholar]
  79. Sasiadek M. Nonrandom distribution of breakpoints in the karyotypes of workers occupationally exposed to benzene. Environ Health Perspect. 1992 Jul;97:255–257. doi: 10.1289/ehp.9297255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Savitz D. A., Whelan E. A., Kleckner R. C. Effect of parents' occupational exposures on risk of stillbirth, preterm delivery, and small-for-gestational-age infants. Am J Epidemiol. 1989 Jun;129(6):1201–1218. doi: 10.1093/oxfordjournals.aje.a115241. [DOI] [PubMed] [Google Scholar]
  81. Sawyers C. L., Denny C. T., Witte O. N. Leukemia and the disruption of normal hematopoiesis. Cell. 1991 Jan 25;64(2):337–350. doi: 10.1016/0092-8674(91)90643-d. [DOI] [PubMed] [Google Scholar]
  82. Sawyers C. L. Molecular genetics of acute leukaemia. Lancet. 1997 Jan 18;349(9046):196–200. doi: 10.1016/S0140-6736(96)07535-6. [DOI] [PubMed] [Google Scholar]
  83. Sellyei M., Keleman E. Chromosome study in a case of granulocytic leukaemia with 'Pelgerisation' 7 years after benzene pancytopenia. Eur J Cancer. 1971 Feb;7(1):83–85. doi: 10.1016/0014-2964(71)90099-5. [DOI] [PubMed] [Google Scholar]
  84. Selvin S., Levin L. I., Merrill D. W., Winkelstein W., Jr Selected epidemiologic observations of cell-specific leukemia mortality in the United States, 1969-1977. Am J Epidemiol. 1983 Feb;117(2):140–152. doi: 10.1093/oxfordjournals.aje.a113524. [DOI] [PubMed] [Google Scholar]
  85. Shannon K. M., Turhan A. G., Rogers P. C., Kan Y. W. Evidence implicating heterozygous deletion of chromosome 7 in the pathogenesis of familial leukemia associated with monosomy 7. Genomics. 1992 Sep;14(1):121–125. doi: 10.1016/s0888-7543(05)80293-9. [DOI] [PubMed] [Google Scholar]
  86. Shu X. O., Gao Y. T., Brinton L. A., Linet M. S., Tu J. T., Zheng W., Fraumeni J. F., Jr A population-based case-control study of childhood leukemia in Shanghai. Cancer. 1988 Aug 1;62(3):635–644. doi: 10.1002/1097-0142(19880801)62:3<635::aid-cncr2820620332>3.0.co;2-3. [DOI] [PubMed] [Google Scholar]
  87. Skalko R. G. Reproductive and developmental toxicity of the components of gasoline. Environ Health Perspect. 1993 Dec;101 (Suppl 6):143–149. doi: 10.1289/ehp.93101s6143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Smith M. A., McCaffrey R. P., Karp J. E. The secondary leukemias: challenges and research directions. J Natl Cancer Inst. 1996 Apr 3;88(7):407–418. doi: 10.1093/jnci/88.7.407. [DOI] [PubMed] [Google Scholar]
  89. Smith M. T. The mechanism of benzene-induced leukemia: a hypothesis and speculations on the causes of leukemia. Environ Health Perspect. 1996 Dec;104 (Suppl 6):1219–1225. doi: 10.1289/ehp.961041219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  90. Smith M. T., Yager J. W., Steinmetz K. L., Eastmond D. A. Peroxidase-dependent metabolism of benzene's phenolic metabolites and its potential role in benzene toxicity and carcinogenicity. Environ Health Perspect. 1989 Jul;82:23–29. doi: 10.1289/ehp.898223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  91. Snyder R., Hedli C. C. An overview of benzene metabolism. Environ Health Perspect. 1996 Dec;104 (Suppl 6):1165–1171. doi: 10.1289/ehp.961041165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  92. Subrahmanyam V. V., Ross D., Eastmond D. A., Smith M. T. Potential role of free radicals in benzene-induced myelotoxicity and leukemia. Free Radic Biol Med. 1991;11(5):495–515. doi: 10.1016/0891-5849(91)90063-9. [DOI] [PubMed] [Google Scholar]
  93. TOUGH I. M., BROWN W. M. CHROMOSOME ABERRATIONS AND EXPOSURE TO AMBIENT BENZENE. Lancet. 1965 Mar 27;1(7387):684–684. doi: 10.1016/s0140-6736(65)91835-0. [DOI] [PubMed] [Google Scholar]
  94. Tompa A., Major J., Jakab M. G. Monitoring of benzene-exposed workers for genotoxic effects of benzene: improved-working-condition-related decrease in the frequencies of chromosomal aberrations in peripheral blood lymphocytes. Mutat Res. 1994 Jan 16;304(2):159–165. doi: 10.1016/0027-5107(94)90207-0. [DOI] [PubMed] [Google Scholar]
  95. Tough I. M., Smith P. G., Court Brown W. M., Harnden D. G. Chromosome studies on workers exposed to atmospheric benzene. The possible influence of age. Eur J Cancer. 1970 Feb;6(1):49–55. doi: 10.1016/0014-2964(70)90053-8. [DOI] [PubMed] [Google Scholar]
  96. Traver R. D., Siegel D., Beall H. D., Phillips R. M., Gibson N. W., Franklin W. A., Ross D. Characterization of a polymorphism in NAD(P)H: quinone oxidoreductase (DT-diaphorase). Br J Cancer. 1997;75(1):69–75. doi: 10.1038/bjc.1997.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  97. VIGLIANI E. C., SAITA G. BENZENE AND LEUKEMIA. N Engl J Med. 1964 Oct 22;271:872–876. doi: 10.1056/NEJM196410222711703. [DOI] [PubMed] [Google Scholar]
  98. Valentine J. L., Lee S. S., Seaton M. J., Asgharian B., Farris G., Corton J. C., Gonzalez F. J., Medinsky M. A. Reduction of benzene metabolism and toxicity in mice that lack CYP2E1 expression. Toxicol Appl Pharmacol. 1996 Nov;141(1):205–213. doi: 10.1006/taap.1996.0277. [DOI] [PubMed] [Google Scholar]
  99. Van den Berghe H., Louwagie A., Broeckaert-Van Orshoven A., David G., Verwilghen R. Chromosome analysis in two unusual malignant blood disorders presumably induced by benzene. Blood. 1979 Apr;53(4):558–566. [PubMed] [Google Scholar]
  100. Verkasalo P. K. Magnetic fields and leukemia--risk for adults living close to power lines. Scand J Work Environ Health. 1996;22 (Suppl 2):1–56. [PubMed] [Google Scholar]
  101. Vigliani E. C., Forni A. Benzene and leukemia. Environ Res. 1976 Feb;11(1):122–127. doi: 10.1016/0013-9351(76)90115-8. [DOI] [PubMed] [Google Scholar]
  102. Wiencke J. K., Spitz M. R., McMillan A., Kelsey K. T. Lung cancer in Mexican-Americans and African-Americans is associated with the wild-type genotype of the NAD(P)H: quinone oxidoreductase polymorphism. Cancer Epidemiol Biomarkers Prev. 1997 Feb;6(2):87–92. [PubMed] [Google Scholar]
  103. Wong O. Risk of acute myeloid leukaemia and multiple myeloma in workers exposed to benzene. Occup Environ Med. 1995 Jun;52(6):380–384. doi: 10.1136/oem.52.6.380. [DOI] [PMC free article] [PubMed] [Google Scholar]
  104. Xi L., Zhang L., Wang Y., Smith M. T. Induction of chromosome-specific aneuploidy and micronuclei in human lymphocytes by metabolites of 1,3-butadiene. Carcinogenesis. 1997 Sep;18(9):1687–1693. doi: 10.1093/carcin/18.9.1687. [DOI] [PubMed] [Google Scholar]
  105. Yardley-Jones A., Anderson D., Lovell D. P., Jenkinson P. C. Analysis of chromosomal aberrations in workers exposed to low level benzene. Br J Ind Med. 1990 Jan;47(1):48–51. doi: 10.1136/oem.47.1.48. [DOI] [PMC free article] [PubMed] [Google Scholar]
  106. Yin S. N., Hayes R. B., Linet M. S., Li G. L., Dosemeci M., Travis L. B., Li C. Y., Zhang Z. N., Li D. G., Chow W. H. A cohort study of cancer among benzene-exposed workers in China: overall results. Am J Ind Med. 1996 Mar;29(3):227–235. doi: 10.1002/(SICI)1097-0274(199603)29:3<227::AID-AJIM2>3.0.CO;2-N. [DOI] [PubMed] [Google Scholar]
  107. Yin S. N., Li Q., Liu Y., Tian F., Du C., Jin C. Occupational exposure to benzene in China. Br J Ind Med. 1987 Mar;44(3):192–195. doi: 10.1136/oem.44.3.192. [DOI] [PMC free article] [PubMed] [Google Scholar]
  108. Zhang L., Rothman N., Wang Y., Hayes R. B., Bechtold W., Venkatesh P., Yin S., Wang Y., Dosemeci M., Li G. Interphase cytogenetics of workers exposed to benzene. Environ Health Perspect. 1996 Dec;104 (Suppl 6):1325–1329. doi: 10.1289/ehp.961041325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  109. Zhang L., Venkatesh P., Creek M. L., Smith M. T. Detection of 1,2,4-benzenetriol induced aneuploidy and microtubule disruption by fluorescence in situ hybridization and immunocytochemistry. Mutat Res. 1994 Mar;320(4):315–327. doi: 10.1016/0165-1218(94)90084-1. [DOI] [PubMed] [Google Scholar]
  110. van Rhee F., Kasprzyk A., Jamil A., Dickinson H., Lin F., Cross N. C., Galvin M. C., Goldman J. M., Secker-Walker L. M. Detection of the BCR-ABL gene by reverse transcription/polymerase chain reaction and fluorescence in situ hybridization in a patient with Philadelphia chromosome negative acute lymphoblastic leukaemia. Br J Haematol. 1995 May;90(1):225–228. doi: 10.1111/j.1365-2141.1995.tb03408.x. [DOI] [PubMed] [Google Scholar]
  111. van Steensel-Moll H. A., Valkenburg H. A., van Zanen G. E. Childhood leukemia and parental occupation. A register-based case-control study. Am J Epidemiol. 1985 Feb;121(2):216–224. doi: 10.1093/oxfordjournals.aje.a113992. [DOI] [PubMed] [Google Scholar]

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