Advances in understanding benzene health effects and susceptibility

Annual Review of Public Health

Volumn 31, Issue , 2010, Pages 133-148

  Smith, Martyn T ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Genetic polymorphism; Hematology; Leukemia; Molecular epidemiology; Risk assessment

Indexed keywords

ALKYLATING AGENT; AROMATIC HYDROCARBON RECEPTOR; BENZENE; ETOPOSIDE; GYRASE INHIBITOR; MERBARONE;

ACUTE GRANULOCYTIC LEUKEMIA; ACUTE LEUKEMIA; ACUTE LYMPHOBLASTIC LEUKEMIA; BLOOD TOXICITY; CANCER RISK; CHEMICAL CARCINOGENESIS; CHILDHOOD LEUKEMIA; CHRONIC MYELOID LEUKEMIA; DNA POLYMORPHISM; ENVIRONMENTAL EXPOSURE; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; GENOME ANALYSIS; HEMATOLOGIC MALIGNANCY; HUMAN; LEUKEMOGENESIS; MEDICAL RESEARCH; METABOLISM; MYELODYSPLASTIC SYNDROME; NONHODGKIN LYMPHOMA; OCCUPATIONAL EXPOSURE; POPULATION RISK; PRIORITY JOURNAL; REVIEW; RISK ASSESSMENT;

BENZENE; CARCINOGENS, ENVIRONMENTAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENVIRONMENTAL EXPOSURE; EPIDEMIOLOGIC STUDIES; HEMATOLOGIC NEOPLASMS; HUMANS; LEUKEMIA, MYELOID, ACUTE; RECEPTORS, ARYL HYDROCARBON;

EID: 77952720805     PISSN: 01637525     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.publhealth.012809.103646     Document Type: Review

References (129)

1. Aksoy M. 1988. Benzene hematotoxicity. In Benzene Carcinogenicity, ed. M Aksoy, pp. 59-112. Boca Raton, FL: CRC Press
2. Aksoy M. 1989. Hematotoxicity and carcinogenicity of benzene. Environ. Health Perspect. 82:193-197
3. Aksoy M, Dincol K, Akgun T, Erdem S, Dincol G. 1971. Haematological effects of chronic benzene poisoning in 217 workers. Br. J. Ind. Med. 28:296-302
4. Aksoy M, Dincol K, Erdem S, Akgun T, Dincol G. 1972. Details of blood changes in 32 patients with pancytopenia associated with long-term exposure to benzene. Br. J. Ind. Med. 29:56-64
5. Albertini R, Clewell H, Himmelstein MW, Morinello E, Olin S, et al. 2003. The use of non-tumor data in cancer risk assessment: reflections on butadiene, vinyl chloride, and benzene. Regul. Toxicol. Pharmacol. 37:105-132
6. Badham HJ, Winn LM. 2009. In utero exposure to benzene disrupts fetal hematopoietic progenitor cell growth via reactive oxygen species. Toxicol. Sci. In press
7. Baker RK, Kurz EU, Pyatt DW, Irons RD, Kroll DJ. 2001. Benzene metabolites antagonize etoposide-stabilized cleavable complexes of DNA topoisomerase IIalpha. Blood 98:830-833
8. Bechtold WE, Willis JK, Sun JD, Griffith WC, Reddy TV. 1992. Biological markers of exposure to benzene: S-phenylcysteine in albumin. Carcinogenesis 13:1217-1220
9. Beelte S, Haas R, Germing U, Jansing P-J. 2008. Practice of recognizing benzene-caused occupational diseases in 2006. Med. Klin. 103:553-560 (In German)
10. Beelte S, Haas R, Germing U, Jansing P-J. 2009. Paradigm change in the assessment of myeloid and lymphoid neoplasms associated with occupational benzene exposure. Med. Klin. 104:197-203 (In German)
11. Bollati V, Baccarelli A, Hou L, Bonzini M, Fustinoni S, et al. 2007. Changes in DNA methylation patterns in subjects exposed to low-dose benzene. Cancer Res. 67:876-880
12. Brosselin P, Rudant J, Orsi L, Leverger G, Baruchel A, et al. 2009. Acute childhood leukaemia and residence next to petrol stations and automotive repair garages: the ESCALE study (SFCE). Occup. Environ. Med. 66:598-606
13. Chen H, Eastmond DA. 1995. Topoisomerase inhibition by phenolic metabolites: a potential mechanism for benzene's clastogenic effects. Carcinogenesis 16:2301-2307
14. Cho JY. 2008. Suppressive effect of hydroquinone, a benzene metabolite, on in vitro inflammatory responses mediated by macrophages, monocytes, and lymphocytes. Mediat. Inflamm. 2008:298010
15. Cronkite EP. 1961. Evidence for radiation and chemicals as leukemogenic agents. Arch. Environ. Health 3:297-303
16. Delore P, Borgomano C. 1928. Leucemie aigue au cours de l'intoxication benzenique: sur l'origine toxique de certaines leucemies aigues et leur relations avec les anemies graves. J. Med. Lyon. 9:227-233
17. Deweese JE, Osheroff N. 2009. The DNA cleavage reaction of topoisomerase II: wolf in sheep's clothing. Nucleic Acids Res. 37:738-748
18. Dougherty D, Garte S, Barchowsky A, Zmuda J, Taioli E. 2008. NQO1, MPO, CYP2E1, GSTT1 and GSTM1 polymorphisms and biological effects of benzene exposure\a literature review. Toxicol. Lett. 182:7-17
19. Eastmond DA, Mondrala ST, Hasegawa L. 2005. Topoisomerase II inhibition by myeloperoxidase-activated hydroquinone: a potential mechanism underlying the genotoxic and carcinogenic effects of benzene. Chem. Biol. Interact. 153-54:207-216
20. Environ. Prot. Agency. 2007. Control of hazardous air pollutants from mobile sources. http://www. epa. gov/fedrgstr/EPA-AIR/2007/February/Day-26
21. Falini B, Nicoletti I, Martelli MF, Mecucci C. 2007. Acute myeloid leukemia carrying cytoplasmic/mutated nucleophosmin (NPMc+ AML): biologic and clinical features. Blood 109:874-885
22. Fazi F, Rosa A, Fatica A, Gelmetti V, De Marchis ML, et al. 2005. A minicircuitry comprised of microRNA-223 and transcription factors NFI-A and C/EBPalpha regulates human granulopoiesis. Cell 123:819-831
23. Forni AM, Cappellini A, Pacifico E, Vigliani EC. 1971. Chromosome changes and their evolution in subjects with past exposure to benzene. Arch. Environ. Health 23:385-391
24. Frohling S, Dohner H. 2004. Disruption of C/EBPalpha function in acute myeloid leukemia. N. Engl. J. Med. 351:2370-2372
25. Glass DC, Gray CN, Adams GG, Manuell RW, Bisby JA. 2001. Validation of exposure estimation for benzene in the Australian petroleum industry. Toxicol. Ind. Health 17:113-127
26. Glass DC, Gray CN, Jolley DJ, Gibbons C, Sim MR, et al. 2003. Leukemia risk associated with low-level benzene exposure. Epidemiology 14:569-577
27. Glass DC, Gray CN, Jolley DJ, Gibbons C, Sim MR. 2005. Health Watch exposure estimates: Do they underestimate benzene exposure? Chem. Biol. Interact. 153-54:23-32
28. Glass DC, Gray CN, Jolley DJ, Sim MR, Fritschi L. 2004. Benzene exposure and leukemia. Epidemiology 15:510-511
29. Goldstein B. 2004. Benzene exposure and leukemia. Epidemiology 15:509-510
30. Goldstein BD. 1988. Benzene toxicity. Occup. Med. 3:541-554
31. Gowans ID, Lorimore SA, McIlrath JM, Wright EG. 2005. Genotype-dependent induction of transmissible chromosomal instability by gamma-radiation and the benzene metabolite hydroquinone. Cancer Res. 65:3527-3530
32. Greaves MF, Wiemels J. 2003. Origins of chromosome translocations in childhood leukaemia. Nat. Rev. Cancer 3:639-649
33. Guo W, Lasky JL, Chang CJ, Mosessian S, Lewis X, et al. 2008. Multi-genetic events collaboratively contribute to Pten-null leukaemia stem-cell formation. Nature 453:529-533
34. Hackanson B, Bennett KL, Brena RM, Jiang J, Claus R, et al. 2008. Epigenetic modification of CCAAT/enhancer binding protein alpha expression in acute myeloid leukemia. Cancer Res. 68:3142-3151
35. Hamilton A. 1931. Benzene (benzol) poisoning. General review. Arch. Pathol. Lab. Med. 11:434
36. Hayes RB, Songnian Y, Dosemeci M, Linet M. 2001. Benzene and lymphohematopoietic malignancies in humans. Am. J. Ind. Med. 40:117-126
37. Hayes RB, Yin SN, DosemeciM, Li GL, Wacholder S, et al. 1997. Benzene and the dose-related incidence of hematologic neoplasms in China. Chinese Academyof Preventive Medicine-National Cancer Institute Benzene Study Group. J. Natl. Cancer Inst. 89:1065-1071
38. Hayes RB, Yin SN, Rothman N, Dosemeci M, Li G, et al. 2000. Benzene and lymphohematopoietic malignancies in China. J. Toxicol. Environ. Health A 61:419-432
39. Henderson AP, Bleasdale C, Delaney K, Lindstrom AB, Rappaport SM, et al. 2005. Evidence for the formation of Michael adducts from reactions of (E, E)-muconaldehyde with glutathione and other thiols. Bioorg. Chem. 33:363-373
40. Hirabayashi Y, Inoue T. 2009. Aryl hydrocarbon receptor biology and xenobiotic responses in hematopoietic progenitor cells. Biochem. Pharmacol. 77:521-535
41. Hirabayashi Y, Yoon BI, Li GX, Fujii-Kuriyama Y, Kaneko T, et al. 2008. Benzene-induced hematopoi-etic toxicity transmitted by AhR in wild-type mouse and nullified by repopulation with AhR-deficient bone marrow cells: time after benzene treatment and recovery. Chemosphere 73:S290-94
42. Hutt AM, Kalf GF. 1996. Inhibition of human DNA topoisomerase II by hydroquinone and p-benzoquinone, reactive metabolites of benzene. Environ. Health Perspect. 104(Suppl. 6):1265-1269
43. Infante PF, Rinsky RA, Wagoner JK, Young RJ. 1977. Leukaemia in benzene workers. Lancet 2:76-78
44. Irons RD, Stillman WS. 1996. The process of leukemogenesis. Environ. Health Perspect. 104(Suppl. 6):1239-1246
45. Irons RD, Stillman WS, Colagiovanni DB, Henry VA. 1992. Synergistic action of the benzene metabolite hydroquinoneonmyelopoietic stimulating activityof granulocyte/macrophage colony-stimulating factor in vitro. Proc. Natl. Acad. Sci. USA 89:3691-3695
46. Iskander K, Jaiswal AK. 2005. Quinone oxidoreductases in protection against myelogenous hyperplasia and benzene toxicity. Chem. Biol. Interact. 153-54:147-157
47. Kim S, Vermeulen R, Waidyanatha S, Johnson BA, Lan Q, et al. 2006. Modeling human metabolism of benzene following occupational and environmental exposures. Cancer Epidemiol. Biomark. Prev. 15:2246-2252
48. Kirkeleit J, Riise T, Gjertsen BT, Moen BE, Bra?tveit M, Øystein B. 2008. Effects of benzene on human hematopoiesis. Open Hematol. J. 2:87-102
49. Krishnan B, Morgan GJ. 2007. Non-Hodgkin lymphoma secondary to cancer chemotherapy. Cancer Epidemiol. Biomark. Prev. 16:377-380
50. Lan Q, Vermeulen R, Zhang L, Li G, Rosenberg PS, et al. 2006. Benzene exposure and hematotoxicity: response. Science 312:998-999
51. Lan Q, Zhang L, Li G, Vermeulen R, Weinberg RS, et al. 2004. Hematotoxicity in workers exposed to low levels of benzene. Science 306:1774-1776
52. Lan Q, Zhang L, Shen M, Jo WJ, Vermeulen R, et al. 2009. Large-scale evaluation of candidate genes identifies associations between DNA repair and genomic maintenance and development of benzene hematotoxicity. Carcinogenesis 30:50-58
53. Lan Q, Zhang L, Shen M, Smith MT, Li G, et al. 2005. Polymorphisms in cytokine and cellular adhesion molecule genes and susceptibility to hematotoxicity among workers exposed to benzene. Cancer Res. 65:9574-9581
54. Landgren O, Albitar M, Ma W, Abbasi F, Hayes RB, et al. 2009. B-cell clones as early markers for chronic lymphocytic leukemia. N. Engl. J. Med. 360:659-667
55. Landgren O, Kyle RA, Hoppin JA, Beane Freeman LE, Cerhan JR, et al. 2009. Pesticide exposure and risk of monoclonal gammopathy of undetermined significance in the Agricultural Health Study. Blood 113:6386-6391
56. Larson RA, Le Beau MM. 2005. Therapy-related myeloid leukaemia: a model for leukemogenesis in humans. Chem. Biol. Interact. 153-54:187-195
57. Lau A, Belanger CL, Winn LM. 2009. In utero and acute exposure to benzene: investigation of DNA double-strand breaks and DNA recombination in mice. Mutat. Res. 676:74-82
58. Ley TJ, Mardis ER, Ding L, Fulton B, McLellan MD, et al. 2008. DNA sequencing of a cytogenetically normal acute myeloid leukaemia genome. Nature 456:66-72
59. Li B, Li YQ, Yang LJ, Chen SH, Yu W, et al. 2009. Decreased T-cell receptor excision DNA circles in peripheral blood mononuclear cells among benzene-exposed workers. Int. J. Immunogenet. 36:107-111
60. Lindsey RH Jr, Bender RP, Osheroff N. 2005. Effectsofbenzene metabolites on DNA cleavage mediated by human topoisomerase II alpha: 1, 4-hydroquinone is a topoisomerase II poison. Chem. Res. Toxicol. 18:761-770
61. Lobato MN, Metzler M, Drynan L, Forster A, Pannell R, Rabbitts TH. 2008. Modeling chromosomal translocations using conditional alleles to recapitulate initiating events in human leukemias. J. Natl. Cancer Inst. Monogr. 39:58-63
62. Long DJ 2nd, Gaikwad A, Multani A, Pathak S, Montgomery CA, et al. 2002. Disruption of the NAD(P)H:quinone oxidoreductase 1 (NQO1) gene in mice causes myelogenous hyperplasia. Cancer Res. 62:3030-3036
63. Lv L, Kerzic P, Lin G, Schnatter AR, Bao L, et al. 2007. The TNF-α 238A polymorphism is associated with susceptibility to persistent bone marrow dysplasia following chronic exposure to benzene. Leuk. Res. 31:1479-1485
64. Mardis ER, Ding L, Dooling DJ, Larson DE, McLellan MD, et al. 2009. Recurring mutations found by sequencing an acute myeloid leukemia genome. N. Engl. J. Med. 361:1058-1066
65. McDonald TA, Waidyanatha S, Rappaport SM. 1993. Production of benzoquinone adducts with hemoglobin and bone-marrow proteins following administration of [13C6]benzene to rats. Carcinogenesis 14:1921-1925
66. McHale CM, Wiemels JL, Zhang L, Ma X, Buffler PA, et al. 2003. Prenatal origin of childhood acute myeloid leukemias harboring chromosomal rearrangements t(15;17) and inv(16). Blood 101:4640-4641
67. McKinney PA, Alexander FE, Cartwright RA, Parker L. 1991. Parental occupations of children with leukaemia in west Cumbria, north Humberside, and Gateshead. Br. Med. J. 302:681-687
68. Michaels D. 2008. Doubt Is Their Product: How Industry's Assault on Science Threatens Your Health. New York: Oxford Univ. Press
69. Mistry AR, Felix CA, Whitmarsh RJ, Mason A, Reiter A, et al. 2005. DNA topoisomerase II in therapy-related acute promyelocytic leukemia. N. Engl. J. Med. 352:1529-1538
70. Morgan GJ, Alvares CL. 2005. Benzene and the hemopoietic stem cell. Chem. Biol. Interact. 153-54:217-222
71. Mrozek K, Bloomfield CD. 2008. Clinical significance of the most common chromosome translocations in adult acute myeloid leukemia. J. Natl. Cancer Inst. Monogr. 39:52-57
72. Nedelcheva V, Gut I, Soucek P, Tichavská B, Týnkova L, et al. 1999. Metabolism of benzene in human liver microsomes: individual variations in relation to CYP2E1 expression. Arch. Toxicol. 73:33-40
73. Paustenbach DJ, Price PS, Ollison W, Blank C, Jernigan JD, et al. 1992. Reevaluation of benzene exposure for the Pliofilm (rubberworker) cohort (1936-1976). J. Toxicol. Environ. Health 36:177-231
74. Paxton MB. 1996. Leukemia risk associated with benzene exposurein the Pliofilm cohort. Environ. Health Perspect. 104(Suppl. 6):1431-1436
75. Pedersen-Bjergaard J, Andersen MK, Andersen MT, Christiansen DH. 2008. Geneticsof therapy-related myelodysplasia and acute myeloid leukemia. Leukemia 22:240-248
76. Pedersen-Bjergaard J, Christiansen DH, Desta F, Andersen MK. 2006. Alternative genetic pathways and cooperating genetic abnormalities in the pathogenesis of therapy-related myelodysplasia and acute myeloid leukemia. Leukemia 20:1943-1949
77. Powley MW, Carlson GP. 2000. Cytochromes P450 involved with benzene metabolism in hepatic and pulmonary microsomes. J. Biochem. Mol. Toxicol. 14:303-309
78. Qu Q, Shore R, Li G, Jin X, Chen LC, et al. 2002. Hematological changes among Chinese workers with a broad range of benzene exposures. Am. J. Ind. Med. 42:275-285
79. Rappaport SM, Kim S, Lan Q, Vermeulen R, Waidyanatha S, et al. 2009. Evidence that humans metabolize benzene via two pathways. Environ. Health Perspect. 117:946-952
80. Rappaport SM, Waidyanatha S, Qu Q, Shore R, Jin X, et al. 2002. Albumin adducts of benzene oxide and 1, 4-benzoquinone as measures of human benzene metabolism. Cancer Res. 62:1330-1337
81. Rappaport SM, Waidyanatha S, Yeowell-O'Connell K, Rothman N, Smith MT, et al. 2005. Protein adducts as biomarkers of human benzene metabolism. Chem. Biol. Interact. 153-54:103-109 (Pubitemid 40797800)
82. Ren X, Lim S, Smith MT, Zhang L. 2009. Werner syndrome protein, WRN, protects cells from DNA damage induced by the benzene metabolite hydroquinone. Toxicol. Sci. 107:367-375
83. Rinsky RA, Hornung RW, Silver SR, Tseng CY. 2002. Benzene exposure and hematopoietic mortality: a long-term epidemiologic risk assessment. Am. J. Ind. Med. 42:474-480
84. Rinsky RA, Smith AB, Hornung R, Filloon TG, Young RJ, et al. 1987. Benzene and leukemia. An epidemiologic risk assessment. N. Engl. J. Med. 316:1044-1050
85. Rivedal E, Witz G. 2005. Metabolites of benzene are potent inhibitors of gap-junction intercellular communication. Arch. Toxicol. 79:303-311
86. Ross D. 2000. The role of metabolism and specific metabolites in benzene-induced toxicity: evidence and issues. J. Toxicol. Environ. Health A 61:357-372
87. Rothman N, Smith MT, Hayes RB, Traver RD, Hoener B, et al. 1997. Benzene poisoning, a risk factor for hematological malignancy, is associated with the NQO1 609C-T mutation and rapid fractional excretion of chlorzoxazone. Cancer Res. 57:2839-2842
88. Santesson GG. 1897. Uber chronische Vergiftungen mit steinkohlen Benzin. Vier todes falle. Arch. Hyg. 31:336-376
89. Scélo G, Metayer C, Zhang L, Wiemels JL, Aldrich MC, et al. 2009. Household exposure to paint and petroleum solvents, chromosomal translocations, and the risk of childhood leukemia. Environ. Health Perspect. 117:133-139
90. Selling L. 1916. Benzol as a leucotoxin. Studies on the degeneration and regeneration of the blood and haematopoietic organs. Johns Hopkins Hosp. Rep. 17:83-148
91. Sheets PL, Yost GS, Carlson GP. 2004. Benzene metabolism in human lung cell lines BEAS-2B and A549 and cells overexpressing CYP2F1. J. Biochem. Mol. Toxicol. 18:92-99
92. Shu XO, Stewart P, Wen WQ, Han D, Potter JD, et al. 1999. Parental occupational exposure to hydrocarbons and risk of acute lymphocytic leukemia in offspring. Cancer Epidemiol. Biomark. Prev. 8:783-791
93. Singh KP, Casado FL, Opanashuk LA, Gasiewicz TA. 2009. The aryl hydrocarbon receptor has a normal function in the regulation of hematopoietic and other stem/progenitor cell populations. Biochem. Pharmacol. 77:577-587
94. Smith MT. 1996. The mechanism of benzene-induced leukemia: a hypothesis and speculations on the causes of leukemia. Environ. Health Perspect. 104(Suppl. 6):1219-1225
95. Smith MT, Jones RM, Smith AH. 2007. Benzene exposure and risk of non-Hodgkin lymphoma. Cancer Epidemiol. Biomark. Prev. 16:385-391
96. Smith MT, Zhang L, Jeng M, Wang Y, Guo W, et al. 2000. Hydroquinone, a benzene metabolite, increases the level of aneusomy of chromosomes 7 and 8 in human CD34-positive blood progenitor cells. Carcinogenesis 21:1485-1490
97. Smith MT, Zhang L, Wang Y, Hayes RB, Li G, et al. 1998. Increased translocations and aneusomy in chromosomes 8 and 21 among workers exposed to benzene. Cancer Res. 58:2176-2181
98. Snyder R. 2002. Benzene and leukemia. Crit. Rev. Toxicol. 32:155-210
99. Snyder R. 2004. Xenobiotic metabolism and the mechanism(s) of benzene toxicity. Drug Metab. Rev. 36:531-547
100. Sorahan T, Kinlen LJ, Doll R. 2005. Cancer risks in a historical UK cohort of benzene exposed workers. Occup. Environ. Med. 62:231-236
101. Steinmaus C, Smith AH, Jones RM, Smith MT. 2008. Meta-analysis of benzene exposure and non-Hodgkin lymphoma: Biases could mask an important association. Occup. Environ. Med. 65:371-378
102. Stillman WS, Varella-Garcia M, Irons RD. 2000. The benzene metabolite, hydroquinone, selectively induces 5q31-and-7 in human CD34+CD19-bone marrow cells. Exp. Hematol. 28:169-176
103. Sun P, Qiu Y, Zhang Z, Wan J, Wang T, et al. 2009. Association of genetic polymorphisms, mRNA expression of p53 and p21 with chronic benzene poisoning in a Chinese occupational population. Cancer Epidemiol. Biomark. Prev. 18:1821-1828
104. Travis LB, Li CY, Zhang ZN, Li DG, Yin SN, et al. 1994. Hematopoietic malignancies and related disorders among benzene-exposed workers in China. Leuk. Lymphoma 14:91-102
105. Valentine JL, Lee SS, Seaton MJ, Asgharian B, Farris G, et al. 1996. Reduction of benzene metabolism and toxicity in mice that lack CYP2E1 expression. Toxicol. Appl. Pharmacol. 141:205-213 (Pubitemid 26414367)
106. van Steensel-Moll HA, Valkenburg HA, van Zanen GE. 1985. Childhood leukemia and parental occupation. A register-based case-control study. Am. J. Epidemiol. 121:216-224
107. Vardiman JW, Thiele J, Arber DA, Brunning RD, Borowitz MJ, et al. 2009. The 2008 revision of the World Health Organization (WHO) classification of myeloid neoplasms and acute leukemia: rationale and important changes. Blood 114:937-951
108. Vaughan AT, Betti CJ, Villalobos MJ, Premkumar K, Cline E, et al. 2005. Surviving apoptosis: a possible mechanism of benzene-induced leukemia. Chem. Biol. Interact. 153-154:179-185
109. Vigliani EC, Saita G. 1964. Benzene and leukemia. N. Engl. J. Med. 271:872-876
110. Waidyanatha S, Rappaport SM. 2005. Investigation of cysteinyl protein adducts of benzene diolepoxide. Chem. Biol. Interact. 153-54:261-266 (Pubitemid 40797819)
111. Walter MJ, Payton JE, Ries RE, Shannon WD, Deshmukh H, et al. 2009. Acquired copy number alterations in adult acute myeloid leukemia genomes. Proc. Natl. Acad. Sci. USA 106:12950-12955
112. Wang L, Roy SK, Eastmond DA. 2007. Differential cell cycle-specificity for chromosomal damage induced by merbarone and etoposide in V79 cells. Mutat. Res. 616:70-82
113. Ward E, Hornung R, Morris J, Rinsky R, Wild D, et al. 1996. Risk of low red or white blood cell count related to estimated benzene exposure in a rubberworker cohort (1940-1975). Am. J. Ind. Med. 29:247-257
114. Weiskotten HG, Gibbs GBF, Boggs EO, Templeton ER. 1920. The action of benzol. VI. Benzol vapor leucopenia (rabbit). J. Med. Res. 41:425-438
115. Weiskotten HG, Shwartz SC, Steinsland HS. 1916. The action of benzol on blood and blood forming tissues. J. Med. Res. 35:63-69
116. Weiss BM, Abadie J, Verma P, Howard RS, Kuehl WM. 2009. A monoclonal gammopathy precedes multiple myeloma in most patients. Blood 113:5418-5422
117. Whitworth KW, Symanski E, Coker AL. 2008. Childhood lymphohematopoietic cancer incidence and hazardous air pollutants in southeast Texas, 1995-2004. Environ. Health Perspect. 116:1576-1580
118. Wiemels JL, Cazzaniga G, Daniotti M, Eden OB, Addison GM, et al. 1999. Prenatal origin of acute lymphoblastic leukaemia in children. Lancet 354:1499-1503
119. Wiemels JL, Xiao Z, Buffler PA, Maia AT, Ma X, et al. 2002. In utero origin of t(8;21) AML1-ETO translocations in childhood acute myeloid leukemia. Blood 99:3801-3805
120. Wilbur S, Wohlers D, Paikoff S, KeithL, Faroon O. 2008. ATSDR evaluation ofhealth effects of benzene and relevance to public health. Toxicol. Ind. Health 24:263-398
121. Williams PR, Robinson K, Paustenbach DJ. 2005. Benzene exposures associated with tasks performed on marine vessels (circa 1975 to 2000). J. Occup. Environ. Hyg. 2:586-599
122. Yin SN, Hayes RB, Linet MS, Li GL, Dosemeci M, et al. 1996. An expanded cohort study of cancer among benzene-exposed workers in China. Benzene Study Group. Environ. Health Perspect. 104(Suppl. 6):1339-1341 (Pubitemid 27046166)
123. Yin SN, Li GL, Tain FD, Fu ZI, Jin C, et al. 1987. Leukaemia in benzene workers: a retrospective cohort study. Br. J. Ind. Med. 44:124-128
124. Yin SN, Li Q, Liu Y, Tian F, Du C, Jin C. 1987. Occupational exposure to benzene in China. Br. J. Ind. Med. 44:192-195
125. Yoon BI, Hirabayashi Y, Kawasaki Y, Kodama Y, Kaneko T, et al. 2002. Aryl hydrocarbon receptor mediates benzene-induced hematotoxicity. Toxicol. Sci. 70:150-156
126. Zhang B. 1996. Investigation of health status in workers exposed to low-level benzene. Chin. J. Prev. Med. 30:164-66. In Chinese
127. Zhang L, Eastmond DA, Smith MT. 2002. The nature of chromosomal aberrations detected in humans exposed to benzene. Crit. Rev. Toxicol. 32:1-42
128. Zhang L, Rothman N, Li G, Guo W, Yang W, et al. 2007. Aberrations in chromosomes associated with lymphoma and therapy-related leukemia in benzene-exposed workers. Environ. Mol. Mutagen. 48:467-474
129. Zhang L, Rothman N, Wang Y, Hayes RB, Yin S, et al. 1999. Benzene increases aneuploidy in the lymphocytes of exposed workers: a comparison of data obtained by fluorescence in situ hybridization in interphase and metaphase cells. Environ. Mol. Mutagen. 34:260-268