Occupational Exposure to Benzene and Risk of Breast Cancer: Systematic Review and Meta-Analysis
Main Article Content
Keywords
Benzene, Meta-analysis, Occupational exposure
Abstract
Introduction: Benzene is a recognized carcinogen; however, its association with breast cancer is not well established. Hence, a meta-analysis of cohort and case-control studies was performed to determine the association between occupational benzene exposure and the risk of breast cancer. Methods: A systematic literature review identified 7573 publications from which 23 cohort and case-control studies were retained and evaluated using meta-analyses (fixed effects model). PRISMA guidelines were followed. Our protocol was registered in the PROSPERO database (Registration No. CRD42022379720). Study quality was assessed using a modified Newcastle-Ottawa scale (NOS).Results: The summary relative risk (RR) for ever-benzene exposure was 1.08 (95% CI=1.03-1.14, I2=38.6%, n=23 risk estimates); corresponding RR for cancer incidence and mortality were 1.08 (95% CI=1.02-1.14, I2=56.1%, n=16) and 1.10 (95% CI=0.87-1.37, I2<0.001%, n=10). However, heterogeneity was detected for sex (p-het=0.002), publication year (p-het<0.001), study design (p-het<0.001), study quality (p-het<0.001), and industry of employment (p-het=0.03). The RR for high level of exposure showed positive association with breast cancer 1.35 (95% CI=1.06-1.72, I2 =<0.001%, n=3) and (P-het=0.64). Publication bias was detected (p=0.03).Conclusions: The results of our meta-analysis indicate a positive association between occupational benzene exposure and an increased risk of breast cancer, particularly when exposed to higher levels of benzene. However, bias and confounding could not be excluded.
References
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31. Lagorio S, Forastiere F, Iavarone I, et al. Mortality of filling station attendants. Scand J Work Environ Health. 1994;20(5):331-8.
32. Satin KP, Wong O, Yuan LA, et al. A 50-year mortality follow-up of a large cohort of oil refinery workers in Texas. J Occup Environ Med. 1996;38(5):492-506.
33. Collingwood KW, Raabe GK, Wong O. An updated cohort mortality study of workers at a northeastern United States petroleum refinery. Int Arch Occup Environ Health. 1996;68(5):277-88.
34. Lynge E, Andersen A, Nilsson R, et al. Risk of cancer and exposure to gasoline vapors. Am J Epidemiol 1997;145(5):449-58.
35. Pukkala E. Cancer incidence among Finnish oil refinery workers, 1971-1994. J Occup Environ Med 1998;40(8):675-9.
36. Petralia SA, Vena JE, Freudenheim JL, et al. Risk of premenopausal breast cancer in association with occupa-tional exposure to polycyclic aromatic hydrocarbons and benzene. Scand J Work Environ Health. 1999;25(3):215-21.
37. Bulbulyan MA, Ilychova SA, Zahm SH, Astashevsky SV, Zaridze DG. Cancer mortality among women in the Rus-sian printing industry. Am J Ind Med. 1999;36(1):166-71.
38. Petralia SA, Chow WH, McLaughlin J, Jin F, Gao YT, Dosemeci M. Occupational risk factors for breast cancer among women in Shanghai. Am J Ind Med. 1998;34(5):477-83.
39. Kauppinen T, Pukkala E, Saalo A, Sasco AJ. Exposure to chemical carcinogens and risk of cancer among Finnish laboratory workers. Am J Ind Med. 2003;44(4):343-50.
40. Lewis R, Schnatter A, Drummond I, et al. Mortality and cancer morbidity in a cohort of Canadian petroleum workers. Occup Environ Med. 2003;60(12):918-928.
41. Sorahan T, Kinlen L, Doll R. Cancer risks in a historical UK cohort of benzene exposed workers. Occup Environ Med. 2005;62(4):231-236.
42. Costantini AS, Gorini G, Consonni D, Miligi L, Giovannetti L, Quinn M. Exposure to benzene and risk of breast cancer among shoe factory workers in Italy. Tumori. 2009;95(1):8-12.
43. Peplonska B, Stewart P, Szeszenia-Dąbrowska N, et al. Occupational exposure to organic solvents and breast cancer in women. Occup Environ Med. 2010;67(11):722-729.
44. Bonneterre V, Mathern G, Pelen O, et al. Cancer incidence in a chlorochemical plant in Isère, France: an occu-pational cohort study, 1979-2002. Am J Ind Med. 2012;55(9):756-67.
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48. Laouali N, Pilorget C, Cyr D, et al. Occupational exposure to organic solvents and risk of male breast cancer: a European multicenter case-control study. Scand J Work Environ Health. 2018;44(3):310-322.
49. Pedersen JE, Strandberg-Larsen K, Andersson M, Hansen J. Occupational exposure to specific organic solvents and risk of subtypes of breast cancer in a large population of Danish women, 1964-2016. Occup Environ Med. Published online October 22, 2020. Doi: 10.1136/oemed-2020-106865
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51. Westra S, Goldberg MS, Labrèche F, Baumgartner J, Ho V. The association between the incidence of postmen-opausal breast cancer and occupational exposure to selected organic solvents, Montreal, Canada, 2008-2011. Am J Ind Med. 2023;66(11):911-927.
52. Mozzoni P, Poli D, Pinelli S, et al. Benzene Exposure and MicroRNAs Expression: In Vitro, In Vivo and Human Findings. Int J Environ Res Public Health. 2023;20(3):1920.
53. Yusoff NA, Abd Hamid Z, Budin SB, Taib IS. Linking Benzene, in Utero Carcinogenicity and Fetal Hematopoi-etic Stem Cell Niches: A Mechanistic Review. Int J Mol Sci. 2023;24(7):6335.
54. Brody JG, Rudel RA. Environmental pollutants and breast cancer. Environ Health Perspect. 2003;111(8):1007-19.
55. Houle CD, Ton T-VT, Clayton N, Huff J, Hong H-HL, Sills RC. Frequent p53 and H-ras Mutations in Benzene- and Ethylene Oxide-Induced Mammary Gland Carcinomas from B6C3F1 Mice. Toxicol Pathol. 2006;34(6):752-762.
56. Huff JE, Haseman JK, DeMarini DM, et al. Multiple-site carcinogenicity of benzene in Fischer 344 rats and B6C3F1 mice. Environ Health Perspect. 1989;82:125-63.
57. Mulware SJ. The mammary gland carcinogens: the role of metal compounds and organic solvents. Int J Breast Cancer. 2013:640851.
58. Kortenkamp A, Martin O, Faust M, et al. State of the art assessment of endocrine disrupters: final report. Brus-sels: European Commission 442, 2011.
59. Ohyama KI, Nagai F, Tsuchiya Y. Certain styrene oligomers have proliferative activity on MCF-7 human breast tumor cells and binding affinity for human estrogen receptor. Environ Health Perspect. 2001;109(7):699-703.
60. Reutman SR, LeMasters GK, Knecht EA, et al. Evidence of reproductive endocrine effects in women with occu-pational fuel and solvent exposures. Environ Health Perspect. 2002;110(8):805-11.
61. Ekenga CC, Parks CG, D'Aloisio AA, DeRoo LA, Sandler DP. Breast Cancer Risk after Occupational Solvent Ex-posure: the Influence of Timing and Setting. Cancer Research. 2014;74(11):3076-3083.
62. Diamanti-Kandarakis E, Jean-Pierre B, Giudice LC, et al. Endocrine-disrupting chemicals: an Endocrine Soci-ety scientific statement. Endocr Rev. 2009;30(4):293-342.
63. Macon MB, Fenton SE. Endocrine disruptors and the breast: early life effects and later life disease. J Mammary Gland Biol Neoplasia. 2013;18(1):43-61.
64. Capleton AC, Levy LS. An overview of occupational benzene exposures and occupational exposure limits in Europe and North America. Chem Biol Interact. 2005;153-154:43-53.
65. He Y, Si Y, Li X, Hong J, Yu C, He N. The relationship between tobacco and breast cancer incidence: A sys-tematic review and meta-analysis of observational studies. Front Oncol. 2022;12:961970.
66. Jones ME, Schoemaker MJ, Wright LB, Ashworth A, Swerdlow AJ. Smoking and risk of breast cancer in the Gen-erations Study cohort. Breast Cancer Res. 2017;19(1):118.
67. Kim AS, Ko HJ, Kwon JH, Lee JM. Exposure to Secondhand Smoke and Risk of Cancer in Never Smokers: A Me-ta-Analysis of Epidemiologic Studies. Int J Environ Res Public Health 2018;15(9):1981.
68. Mehrgou A, Akouchekian M. The importance of BRCA1 and BRCA2 genes mutations in breast cancer devel-opment. Med J Islam Repub Iran. 2016;30:369.
69. Rumgay H, Shield K, Charvat H, et al. Global burden of cancer in 2020 attributable to alcohol consumption: a population-based study. Lancet Onclol. 2021;22(8):1071-1080.
70. Alessandro G, Andrea D, Giorgio M, et al. Occupational benzene exposure and risk of head and neck cancer: a systematic review and meta-analysis. Environ Res. 2024;120033. ISSN 0013-9351, Doi: https://doi.org/10.1016/j.envres.2024.120033.
2. Rodgers KM, Udesky JO, Rudel RA, Brody JG. Environmental chemicals and breast cancer: An updated review of epidemiological literature informed by biological mechanisms. Environ Res. 2018;160:152-182.
3. Sun YS, Zhao Z, Yang ZN, et al. Risk Factors and Preventions of Breast Cancer. Int J Biol Sci. 2017;13(11):1387-1397.
4. Xiao W, Huang J, Wang J, Chen Y, Hu N, Cao S. Occupational exposure to organic solvents and breast cancer risk: a systematic review and meta-analysis. Environ Sci Pollut Res Int. 2022;29(2):1605-1618.
5. Rudel RA, Ackerman JM, Attfield KR, Brody JG. New exposure biomarkers as tools for breast cancer epidemiol-ogy, biomonitoring, and prevention: a systematic approach based on animal evidence. Environ Health Per-spect. 2014;122(9):881-95
6. IARC (1987) IARC Working Group on the Evaluation of Carcinogenic Risks to Humans.
7. IARC (2012) Chemical Agents and Related Occupations.
8. Nordlinder R, Ramnäs O. Exposure to Benzene at Different Work Places in Sweden. Ann Occup Hyg. 1987;31(3):345-355.
9. Costantini AS, Benvenuti A, Vineis P, et al. Risk of leukemia and multiple myeloma associated with exposure to benzene and other organic solvents: evidence from the Italian Multicenter Case-control study. Am J Ind Med 2008;51(11):803-11.
10. Paustenbach DJ, Bass RD, Price P. Benzene toxicity and risk assessment, 1972-1992: implications for future regulation. Environ Health Perspect. 1993;101 Suppl 6(Suppl 6):177-200.
11. IARC (1982) Some Industrial Chemicals and Dyestuffs, IARC Monographs on the Evaluation of the Carcino-genic Risk of Chemicals to Humans Volume 29.
12. Schnatter AR, Rosamilia K, Wojcik NC. Review of the literature on benzene exposure and leukemia subtypes. Chem Biol Interact. 2005;153-154:9-21.
13. Snyder R. Leukemia and benzene. Int J Environ Res Public Health. 2012;9(8):2875-93.
14. Tomatis L. IARC Benzene Report. Science. 1982;218(4569):214-214.
15. McHale CM, Zhang L, Smith MT. Current understanding of the mechanism of benzene-induced leukemia in humans: implications for risk assessment. Carcinogenesis. 2012.33(2):240-52.
16. Ross D.The role of metabolism and specific metabolites in benzene-induced toxicity: evidence and issues. J Toxicol Environ Health. 2000;A 61(5-6):357-72.
17. Whysner J, Reddy MV, Ross PM, Mohan M, Lax EA. Genotoxicity of benzene and its metabolites. Mutat Res. 2004;566(2):99-130.
18. Wiwanitkit V. Benzene, cytochrome, carcinogenesis: A topic in preventive toxicology. Indian J Occup Environ Med. 2014;18(2):97-9.
19. Gray JM, Rasanayagam S, Engel C, Rizzo J. State of the evidence 2017: an update on the connection between breast cancer and the environment. Environmental Health. 2017;16(1):94.
20. Falzone L, Marconi A, Loreto C, Franco S, Spandidos DA, Libra M. Occupational exposure to carcinogens: Ben-zene, pesticides and fibers (Review). Mol Med Rep. 2016;14(5):4467-4474.
21. Fenga C. Occupational exposure and risk of breast cancer. Biomed Rep. 2016;4(3):282-292.
22. Leso V, Ercolano ML, Cioffi DL, Iavicoli I. Occupational Chemical Exposure and Breast Cancer Risk According to Hormone Receptor Status: A Systematic Review. Cancers. 2019;11(12):1882.
23. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and me-ta-analyses: The PRISMA statement. Int Surg J. 2010;8,336–341.
24. Sassano M, Seyyedsalehi MS, Boffetta P. Occupational benzene exposure and colorectal cancer: A systematic review and meta-analysis. Environ Res. 2024257:119213.
25. Seyyedsalehi MS, Bonetti M, Shah D, DeStefano V, Boffetta P. Occupational benzene exposure and risk of kid-ney and bladder cancers: a systematic review and meta-analysis. Eur J Cancer Prev.2024;10.1097. 10.1097/CEJ.0000000000000911
26. Wells GA, Shea B, O'Connell D, et al. The Newcastle-Ottawa Scale (NOS) for Assessing the Quality of Nonran-domised Studies in Meta-analyses. Ottawa: Ottawa Hospital Research Institute. Available at http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp [Last Accessed on 23 Sep 2024].
27. DerSimonian R, Laird N. Meta-analysis in clinical trials. CCT. 1986;7(3):177-188.
28. Egger M, Smith GD, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. Bmj. 1997;315(7109):629-63.
29. Paci E, Buiatti E, Seniori Costantini AS, et al. Aplastic anemia, leukemia and other cancer mortality in a cohort of shoe workers exposed to benzene. Scand J Work Environ Health. 1989;15(5):313-8.
30. Szeszenia-Dabrowska N, Wilczyńska U, Kaczmarek T, Szymczak W. Cancer mortality among male workers in the Polish rubber industry. Pol J Occup Med Environ Health. 1991;4(2):149-57.
31. Lagorio S, Forastiere F, Iavarone I, et al. Mortality of filling station attendants. Scand J Work Environ Health. 1994;20(5):331-8.
32. Satin KP, Wong O, Yuan LA, et al. A 50-year mortality follow-up of a large cohort of oil refinery workers in Texas. J Occup Environ Med. 1996;38(5):492-506.
33. Collingwood KW, Raabe GK, Wong O. An updated cohort mortality study of workers at a northeastern United States petroleum refinery. Int Arch Occup Environ Health. 1996;68(5):277-88.
34. Lynge E, Andersen A, Nilsson R, et al. Risk of cancer and exposure to gasoline vapors. Am J Epidemiol 1997;145(5):449-58.
35. Pukkala E. Cancer incidence among Finnish oil refinery workers, 1971-1994. J Occup Environ Med 1998;40(8):675-9.
36. Petralia SA, Vena JE, Freudenheim JL, et al. Risk of premenopausal breast cancer in association with occupa-tional exposure to polycyclic aromatic hydrocarbons and benzene. Scand J Work Environ Health. 1999;25(3):215-21.
37. Bulbulyan MA, Ilychova SA, Zahm SH, Astashevsky SV, Zaridze DG. Cancer mortality among women in the Rus-sian printing industry. Am J Ind Med. 1999;36(1):166-71.
38. Petralia SA, Chow WH, McLaughlin J, Jin F, Gao YT, Dosemeci M. Occupational risk factors for breast cancer among women in Shanghai. Am J Ind Med. 1998;34(5):477-83.
39. Kauppinen T, Pukkala E, Saalo A, Sasco AJ. Exposure to chemical carcinogens and risk of cancer among Finnish laboratory workers. Am J Ind Med. 2003;44(4):343-50.
40. Lewis R, Schnatter A, Drummond I, et al. Mortality and cancer morbidity in a cohort of Canadian petroleum workers. Occup Environ Med. 2003;60(12):918-928.
41. Sorahan T, Kinlen L, Doll R. Cancer risks in a historical UK cohort of benzene exposed workers. Occup Environ Med. 2005;62(4):231-236.
42. Costantini AS, Gorini G, Consonni D, Miligi L, Giovannetti L, Quinn M. Exposure to benzene and risk of breast cancer among shoe factory workers in Italy. Tumori. 2009;95(1):8-12.
43. Peplonska B, Stewart P, Szeszenia-Dąbrowska N, et al. Occupational exposure to organic solvents and breast cancer in women. Occup Environ Med. 2010;67(11):722-729.
44. Bonneterre V, Mathern G, Pelen O, et al. Cancer incidence in a chlorochemical plant in Isère, France: an occu-pational cohort study, 1979-2002. Am J Ind Med. 2012;55(9):756-67.
45. Linet MS, Yin SN, Gilbert ES, et al. Chinese Center for Disease Control and Prevention-U.S. National Cancer In-stitute Benzene Study Group. A retrospective cohort study of cause-specific mortality and incidence of hema-topoietic malignancies in Chinese benzene-exposed workers. Int J Cancer. 2015;137:2184–2197.
46. Glass DC, Heyworth J, Thomson AK, Peters S, Saunders C, Fritschi L. Occupational exposure to solvents and risk of breast cancer. Am J Ind Med. 2015;58(9):915-22.
47. Gustavsson P, Andersson T, Gustavsson A, Reuterwall C. Cancer incidence in female laboratory employees: extended follow-up of a Swedish cohort study. Occup Environ Med. 2017;74(11):823-826.
48. Laouali N, Pilorget C, Cyr D, et al. Occupational exposure to organic solvents and risk of male breast cancer: a European multicenter case-control study. Scand J Work Environ Health. 2018;44(3):310-322.
49. Pedersen JE, Strandberg-Larsen K, Andersson M, Hansen J. Occupational exposure to specific organic solvents and risk of subtypes of breast cancer in a large population of Danish women, 1964-2016. Occup Environ Med. Published online October 22, 2020. Doi: 10.1136/oemed-2020-106865
50. Liu FC, Veierød MB, Kjærheim K, et al. Night shift work, chemical coexposures and risk of female breast cancer in the Norwegian Offshore Petroleum Workers (NOPW) cohort: a prospectively recruited case-cohort study. BMJ open. 2022;12(1):e056396.
51. Westra S, Goldberg MS, Labrèche F, Baumgartner J, Ho V. The association between the incidence of postmen-opausal breast cancer and occupational exposure to selected organic solvents, Montreal, Canada, 2008-2011. Am J Ind Med. 2023;66(11):911-927.
52. Mozzoni P, Poli D, Pinelli S, et al. Benzene Exposure and MicroRNAs Expression: In Vitro, In Vivo and Human Findings. Int J Environ Res Public Health. 2023;20(3):1920.
53. Yusoff NA, Abd Hamid Z, Budin SB, Taib IS. Linking Benzene, in Utero Carcinogenicity and Fetal Hematopoi-etic Stem Cell Niches: A Mechanistic Review. Int J Mol Sci. 2023;24(7):6335.
54. Brody JG, Rudel RA. Environmental pollutants and breast cancer. Environ Health Perspect. 2003;111(8):1007-19.
55. Houle CD, Ton T-VT, Clayton N, Huff J, Hong H-HL, Sills RC. Frequent p53 and H-ras Mutations in Benzene- and Ethylene Oxide-Induced Mammary Gland Carcinomas from B6C3F1 Mice. Toxicol Pathol. 2006;34(6):752-762.
56. Huff JE, Haseman JK, DeMarini DM, et al. Multiple-site carcinogenicity of benzene in Fischer 344 rats and B6C3F1 mice. Environ Health Perspect. 1989;82:125-63.
57. Mulware SJ. The mammary gland carcinogens: the role of metal compounds and organic solvents. Int J Breast Cancer. 2013:640851.
58. Kortenkamp A, Martin O, Faust M, et al. State of the art assessment of endocrine disrupters: final report. Brus-sels: European Commission 442, 2011.
59. Ohyama KI, Nagai F, Tsuchiya Y. Certain styrene oligomers have proliferative activity on MCF-7 human breast tumor cells and binding affinity for human estrogen receptor. Environ Health Perspect. 2001;109(7):699-703.
60. Reutman SR, LeMasters GK, Knecht EA, et al. Evidence of reproductive endocrine effects in women with occu-pational fuel and solvent exposures. Environ Health Perspect. 2002;110(8):805-11.
61. Ekenga CC, Parks CG, D'Aloisio AA, DeRoo LA, Sandler DP. Breast Cancer Risk after Occupational Solvent Ex-posure: the Influence of Timing and Setting. Cancer Research. 2014;74(11):3076-3083.
62. Diamanti-Kandarakis E, Jean-Pierre B, Giudice LC, et al. Endocrine-disrupting chemicals: an Endocrine Soci-ety scientific statement. Endocr Rev. 2009;30(4):293-342.
63. Macon MB, Fenton SE. Endocrine disruptors and the breast: early life effects and later life disease. J Mammary Gland Biol Neoplasia. 2013;18(1):43-61.
64. Capleton AC, Levy LS. An overview of occupational benzene exposures and occupational exposure limits in Europe and North America. Chem Biol Interact. 2005;153-154:43-53.
65. He Y, Si Y, Li X, Hong J, Yu C, He N. The relationship between tobacco and breast cancer incidence: A sys-tematic review and meta-analysis of observational studies. Front Oncol. 2022;12:961970.
66. Jones ME, Schoemaker MJ, Wright LB, Ashworth A, Swerdlow AJ. Smoking and risk of breast cancer in the Gen-erations Study cohort. Breast Cancer Res. 2017;19(1):118.
67. Kim AS, Ko HJ, Kwon JH, Lee JM. Exposure to Secondhand Smoke and Risk of Cancer in Never Smokers: A Me-ta-Analysis of Epidemiologic Studies. Int J Environ Res Public Health 2018;15(9):1981.
68. Mehrgou A, Akouchekian M. The importance of BRCA1 and BRCA2 genes mutations in breast cancer devel-opment. Med J Islam Repub Iran. 2016;30:369.
69. Rumgay H, Shield K, Charvat H, et al. Global burden of cancer in 2020 attributable to alcohol consumption: a population-based study. Lancet Onclol. 2021;22(8):1071-1080.
70. Alessandro G, Andrea D, Giorgio M, et al. Occupational benzene exposure and risk of head and neck cancer: a systematic review and meta-analysis. Environ Res. 2024;120033. ISSN 0013-9351, Doi: https://doi.org/10.1016/j.envres.2024.120033.
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Seyyedsalehi MS, Destefano V, Shah D, Shah V, Bonetti M, Boffetta P. Occupational Exposure to Benzene and Risk of Breast Cancer: Systematic Review and Meta-Analysis. Med Lav [Internet]. 2024 Oct. 24 [cited 2024 Dec. 26];115(5):e2024034. Available from: https://mattioli1885journals.com/index.php/lamedicinadellavoro/article/view/16306
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Reviews, Commentaries, Perspectives
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How to Cite
1.
Seyyedsalehi MS, Destefano V, Shah D, Shah V, Bonetti M, Boffetta P. Occupational Exposure to Benzene and Risk of Breast Cancer: Systematic Review and Meta-Analysis. Med Lav [Internet]. 2024 Oct. 24 [cited 2024 Dec. 26];115(5):e2024034. Available from: https://mattioli1885journals.com/index.php/lamedicinadellavoro/article/view/16306
