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Title: Benzene Exposure Near the U.S. Permissible Limit Is Associated with Sperm Aneuploidy

Journal Article · · Environmental Health Perspectives
 [1];  [2];  [3];  [4];  [4];  [4];  [2];  [4];  [4];  [5];  [2];  [4]
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Life Sciences Division; Chinese Center for Disease Control and Prevention, Beijing (China). National Inst. of Occupational Health and Poison Control; DOE/OSTI
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Life Sciences Division
  3. Chinese Center for Disease Control and Prevention, Beijing (China). National Inst. of Occupational Health and Poison Control
  4. Univ. of California, Berkeley, CA (United States). School of Public Health
  5. Univ. of North Carolina, Chapel Hill, NC (United States)

Background: Benzene is a common industrial chemical known to induce leukemia and other blood disorders, as well as aneuploidy, in both human blood cells and sperm at exposures > 10 ppm. Recent reports have identified health effects at exposure levels < 1 ppm, the permissible exposure limit (PEL; 8 hr) set by the U.S. Occupational Safety and Health Administration. Objective: We investigated whether occupational exposures to benzene near 1 ppm induce aneuploidy in sperm. Methods: We used multicolor fluorescence in situ hybridization to measure the incidence of sperm with numerical abnormalities of chromosomes X, Y, and 21 among 33 benzene-exposed men and 33 unexposed men from Chinese factories. Individual exposures were assessed using personal air monitoring and urinary concentrations of benzene and trans,trans-muconic acid (E,E-MA). Air benzene concentrations were not detectable in unexposed men; in exposed men, concentrations ranged from below the detection limit to 24 ppm (median, 2.9 ppm), with 27% of exposed men (n = 9) having concentrations of ≤ 1 ppm. Exposed men were categorized into low and high groups based on urinary E,E-MA (median concentrations of 1.9 and 14.4 mg/L, respectively; median air benzene of 1 and 7.7 ppm, respectively), and aneuploidy frequencies were compared with those of unexposed men. Results: Sperm aneuploidy increased across low- and high-exposed groups for disomy X [incidence rate ratio (IRR) = 2.0; 95% confidence interval (CI), 1.1–3.4; and IRR = 2.8; 95% CI, 1.5–4.9, respectively], and for overall hyperhaploidy for the three chromosomes investigated (IRR = 1.6; 95% CI, 1.0–2.4; and IRR = 2.3; 95% CI, 1.5–3.6, respectively). We also found elevated disomy X and hyperhaploidy in the nine men exposed to ≤ 1 ppm benzene compared with unexposed men (IRR = 1.8; 95% CI, 1.1–3.0; and IRR = 2.0; 95% CI, 1.1–3.9, respectively). Conclusions: Benzene appeared to increase the frequencies of aneuploid sperm for chromosomes associated with chromosomal abnormality syndromes in human offspring, even in men whose air benzene exposure was at or below the U.S. permissible exposure limit.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1627102
Journal Information:
Environmental Health Perspectives, Journal Name: Environmental Health Perspectives Journal Issue: 6 Vol. 118; ISSN 0091-6765
Publisher:
National Institute of Environmental Health SciencesCopyright Statement
Country of Publication:
United States
Language:
English

References (61)

Validation of biomarkers in humans exposed to benzene: Urine metabolites journal May 2000
Genetic effects of petroleum fuels: II. Analysis of chromosome loss and hyperploidy in peripheral lymphocytes of gasoline station attendants journal January 1998
Aberrations in chromosomes associated with lymphoma and therapy-related leukemia in benzene-exposed workers journal January 2007
High hyperdiploid childhood acute lymphoblastic leukemia journal August 2009
Rapid determination of six urinary benzene metabolites in occupationally exposed and unexposed subjects journal April 2004
Meiosis and sex chromosome aneuploidy: how meiotic errors cause aneuploidy; how aneuploidy causes meiotic errors journal June 2006
Benzene exposure in the shoemaking industry in China, a literature survey, 1978–2004 journal November 2006
Exposure to acrylonitrile induced DNA strand breakage and sex chromosome aneuploidy in human spermatozoa journal May 2003
The origins, patterns and implications of human spontaneous mutation journal October 2000
To err (meiotically) is human: the genesis of human aneuploidy journal April 2001
The Nature of Chromosomal Aberrations Detected in Humans Exposed to Benzene journal January 2002
Frequency of XY Sperm Increases with Age in Fathers of Boys with Klinefelter Syndrome journal November 2001
Meiotic Segregation, Recombination, and Gamete Aneuploidy Assessed in a t(1;10)(p22.1;q22.3) Reciprocal Translocation Carrier by Three- and Four-Probe Multicolor FISH in Sperm journal September 1997
Increased aneusomy and long arm deletion of chromosomes 5 and 7 in the lymphocytes of Chinese workers exposed to benzene journal November 1998
Urinary benzene as a biomarker of exposure among occupationally exposed and unexposed subjects journal February 2001
Using urinary biomarkers to elucidate dose-related patterns of human benzene metabolism journal December 2005
The origin of human aneuploidy: where we have been, where we are going journal July 2007
Sperm aneuploidy in fathers of children with paternally and maternally inherited Klinefelter syndrome journal March 2002
Disomy rates for chromosomes 14 and 21 studied by fluorescent in-situ hybridization in spermatozoa from three men over 60 years of age journal July 1998
Genotoxic Effects on Spermatozoa of Carbaryl-Exposed Workers journal December 2004
Hematotoxicity in Workers Exposed to Low Levels of Benzene journal December 2004
The mechanism of benzene-induced leukemia: a hypothesis and speculations on the causes of leukemia. journal December 1996
Effects of paternal occupational exposure on spontaneous abortions. journal August 1991
Y:X Sperm Ratio in Boron-Exposed Men journal September 2007
Sperm aneuploidy among Chinese pesticide factory workers: Scoring by the FISH method journal August 1999
Validation of biomarkers in humans exposed to benzene: Urine metabolites journal May 2000
Genetic effects of petroleum fuels: II. Analysis of chromosome loss and hyperploidy in peripheral lymphocytes of gasoline station attendants journal January 1998
Numerical and structural chromosomal abnormalities detected in human sperm with a combination of multicolor FISH assays journal January 1999
Detection of sex chromosomal aneuploidies X-X, Y-Y, and X-Y in human sperm using two-chromosome fluorescence in situ hybridization journal October 1994
Cross-species sperm-FISH assays for chemical testing and assessing paternal risk for chromosomally abnormal pregnancies journal January 2005
Aberrations in chromosomes associated with lymphoma and therapy-related leukemia in benzene-exposed workers journal January 2007
High hyperdiploid childhood acute lymphoblastic leukemia journal August 2009
Cigarette smoking and aneuploidy in human sperm journal January 2001
Paternal Occupation and Childhood Cancer book January 2003
Exposure to acrylonitrile induced DNA strand breakage and sex chromosome aneuploidy in human spermatozoa journal May 2003
Rapid determination of six urinary benzene metabolites in occupationally exposed and unexposed subjects journal April 2004
An overview of published benzene exposure data by industry in China, 1960–2003 journal May 2005
Use of OctoChrome fluorescence in situ hybridization to detect specific aneuploidy among all 24 chromosomes in benzene-exposed workers journal May 2005
Meiosis and sex chromosome aneuploidy: how meiotic errors cause aneuploidy; how aneuploidy causes meiotic errors journal June 2006
Benzene exposure in the shoemaking industry in China, a literature survey, 1978–2004 journal November 2006
Pollutant Emissions from Gasoline Combustion. 1. Dependence on Fuel Structural Functionalities journal August 2008
The origins, patterns and implications of human spontaneous mutation journal October 2000
To err (meiotically) is human: the genesis of human aneuploidy journal April 2001
Exposures to Benzene and Other Volatile Compounds from Active and Passive Smoking journal October 1987
The Nature of Chromosomal Aberrations Detected in Humans Exposed to Benzene journal January 2002
Frequency of XY Sperm Increases with Age in Fathers of Boys with Klinefelter Syndrome journal November 2001
Meiotic Segregation, Recombination, and Gamete Aneuploidy Assessed in a t(1;10)(p22.1;q22.3) Reciprocal Translocation Carrier by Three- and Four-Probe Multicolor FISH in Sperm journal September 1997
Increased aneusomy and long arm deletion of chromosomes 5 and 7 in the lymphocytes of Chinese workers exposed to benzene journal November 1998
Urinary benzene as a biomarker of exposure among occupationally exposed and unexposed subjects journal February 2001
Using urinary biomarkers to elucidate dose-related patterns of human benzene metabolism journal December 2005
The origin of human aneuploidy: where we have been, where we are going journal July 2007
Increased aneuploidy in spermatozoa from testicular tumour patients after chemotherapy with cisplatin, etoposide and bleomycin journal June 2001
Sperm aneuploidy in fathers of children with paternally and maternally inherited Klinefelter syndrome journal March 2002
Relative Susceptibilities of Male Germ Cells to Genetic Defects Induced by Cancer Chemotherapies journal March 2005
Disomy rates for chromosomes 14 and 21 studied by fluorescent in-situ hybridization in spermatozoa from three men over 60 years of age journal July 1998
Genotoxic Effects on Spermatozoa of Carbaryl-Exposed Workers journal December 2004
Hematotoxicity in Workers Exposed to Low Levels of Benzene journal December 2004
Advances in Understanding Benzene Health Effects and Susceptibility journal March 2010
The mechanism of benzene-induced leukemia: a hypothesis and speculations on the causes of leukemia. journal December 1996
Effects of paternal occupational exposure on spontaneous abortions. journal August 1991
Y:X Sperm Ratio in Boron-Exposed Men journal September 2007

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Environmental Exposure to Polychlorinated Biphenyls and p,p ´-DDE and Sperm Sex-Chromosome Disomy journal April 2012
Sperm Aneuploidy in Faroese Men with Lifetime Exposure to Dichlorodiphenyldichloroethylene ( p , -DDE) and Polychlorinated Biphenyl (PCB) Pollutants journal July 2016
A Return to the Origin of the EMGS: Rejuvenating the Quest for Human Germ Cell Mutagens and Determining the Risk to Future Generations journal October 2019
Determination of t,t-muconic acid in urine samples using a molecular imprinted polymer combined with simultaneous ethyl chloroformate derivatization and pre-concentration by dispersive liquid–liquid microextraction journal October 2012
Sperm aneuploidy in infertile male patients: a systematic review of the literature journal October 2014
Environmental Exposure to Polychlorinated Biphenyls and p,p ´-DDE and Sperm Sex-Chromosome Disomy journal April 2012
Sperm Aneuploidy in Faroese Men with Lifetime Exposure to Dichlorodiphenyldichloroethylene ( p , -DDE) and Polychlorinated Biphenyl (PCB) Pollutants journal July 2016
Benzeno: reflexos sobre a saúde pública, presença ambiental e indicadores biológicos utilizados para a determinação da exposição journal December 2014