Occupational exposure to organochlorine insecticides and cancer incidence in the Agricultural Health Study
Corresponding Author
Mark P. Purdue
Division of Cancer Epidemiology and Genetics, Occupational and Environmental Epidemiology Branch, National Cancer Institute, National Institutes of Health, Rockville, Maryland, USA
Fax: 301-402-1819.
6120 Executive Blvd., EPS 8109, Occupational and Environmental Epidemiology Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD 20852, USASearch for more papers by this authorJane A. Hoppin
Epidemiology Branch, National Institute of Environmental Health Sciences, National Institutes of Health, Research Triangle Park, North Carolina, USA
Search for more papers by this authorAaron Blair
Division of Cancer Epidemiology and Genetics, Occupational and Environmental Epidemiology Branch, National Cancer Institute, National Institutes of Health, Rockville, Maryland, USA
Search for more papers by this authorMustafa Dosemeci
Division of Cancer Epidemiology and Genetics, Occupational and Environmental Epidemiology Branch, National Cancer Institute, National Institutes of Health, Rockville, Maryland, USA
Search for more papers by this authorMichael C.R. Alavanja
Division of Cancer Epidemiology and Genetics, Occupational and Environmental Epidemiology Branch, National Cancer Institute, National Institutes of Health, Rockville, Maryland, USA
Search for more papers by this authorCorresponding Author
Mark P. Purdue
Division of Cancer Epidemiology and Genetics, Occupational and Environmental Epidemiology Branch, National Cancer Institute, National Institutes of Health, Rockville, Maryland, USA
Fax: 301-402-1819.
6120 Executive Blvd., EPS 8109, Occupational and Environmental Epidemiology Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD 20852, USASearch for more papers by this authorJane A. Hoppin
Epidemiology Branch, National Institute of Environmental Health Sciences, National Institutes of Health, Research Triangle Park, North Carolina, USA
Search for more papers by this authorAaron Blair
Division of Cancer Epidemiology and Genetics, Occupational and Environmental Epidemiology Branch, National Cancer Institute, National Institutes of Health, Rockville, Maryland, USA
Search for more papers by this authorMustafa Dosemeci
Division of Cancer Epidemiology and Genetics, Occupational and Environmental Epidemiology Branch, National Cancer Institute, National Institutes of Health, Rockville, Maryland, USA
Search for more papers by this authorMichael C.R. Alavanja
Division of Cancer Epidemiology and Genetics, Occupational and Environmental Epidemiology Branch, National Cancer Institute, National Institutes of Health, Rockville, Maryland, USA
Search for more papers by this authorAbstract
Organochlorine (OC) insecticides have been regulated as possible human carcinogens primarily on the basis of animal studies. However, the epidemiologic evidence is inconsistent. We investigated the relationship between cancer incidence and OC insecticide use among pesticide applicators enrolled in the Agricultural Health Study, a prospective cohort study of 57,311 licensed applicators in Iowa and North Carolina enrolled between 1993 and 1997. Information on ever use of 7 OC insecticides (aldrin, chlordane, DDT, dieldrin, heptachlor, lindane, toxaphene) was collected from a self-administered questionnaire at enrollment. Lifetime exposure-days to OC insecticides were calculated using additional data from a take-home questionnaire completed by 25,291 participants (44% of total). We found no clear evidence of an association between use of OC insecticides and incident cancers (N = 1,150) ascertained through December, 2002. When we focused on individual insecticides and structurally similar groups (aldrin and dieldrin; chlordane and heptachlor), significantly increased relative risks of some cancers were observed for use of some chemicals (rectal cancer and chlordane, lung cancer and dieldrin, non-Hodgkin lymphoma (NHL) and lindane, melanoma and toxaphene, leukemia and chlordane/heptachlor). Some significant decreased relative risks were also observed (colon cancer and aldrin; overall cancer and heptachlor). In conclusion, we did not observe any clear relationship between cancer risk and the use of OC insecticides. Our chemical-specific findings are based on small numbers and multiple comparisons, and should be interpreted with caution; however, some observed associations (lindane and NHL, chlordane/heptachlor and leukemia) are supported by previous evidence. © 2006 Wiley-Liss, Inc.
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References
- 1 International Agency for Research on Cancer. Occupational cancer in developing countries. Lyon: IARC, 1994. IARC Scientific Publication No. 129.
- 2 Gorman S, Tynan E. Persistent organic pollutants—a legacy of environmental harm and threats to health. Environ Strategy Notes 2003; 6: 1–4.
- 3 Santillo D, Johnston P, Stringer R. A catalogue of gross contamination. Organochlorine production and exposure in India. Pesticides News 1997; 36: 4–6.
- 4 Soto AM, Sonnenschein C, Chung KL, Fernandez MF, Olea N, Serrano FO. The E-SCREEN assay as a tool to identify estrogens: an update on estrogenic environmental pollutants. Environ Health Perspect 1995; 103 ( Suppl 7): 113–22.
- 5 Kelce WR, Stone CR, Laws SC, Gray LE, Kemppainen JA, Wilson EM. Persistent DDT metabolite p,p′-DDE is a potent androgen receptor antagonist. Nature 1995; 375: 581–85.
- 6 Dich J, Zahm SH, Hanberg A, Adami HO. Pesticides and cancer. Cancer Causes Control 1997; 8: 420–43.
- 7 Calle EE, Frumkin H, Henley SJ, Savitz DA, Thun MJ. Organochlorines and breast cancer risk. CA Cancer J Clin 2002; 52: 301–9.
- 8 Alavanja MC, Samanic C, Dosemeci M, Lubin J, Tarone R, Lynch CF, Knott C, Thomas K, Hoppin JA, Barker J, Coble J, Sandler DP et al. Use of agricultural pesticides and prostate cancer risk in the Agricultural Health Study cohort. Am J Epidemiol 2003; 157: 800–14.
- 9 Alavanja MC, Dosemeci M, Samanic C, Lubin J, Lynch CF, Knott C, Barker J, Hoppin JA, Sandler DP, Coble J, Thomas K, Blair A. Pesticides and lung cancer risk in the agricultural health study cohort. Am J Epidemiol 2004; 160: 876–85.
- 10 Garabrant DH, Held J, Langholz B, Peters JM, Mack TM. DDT and related compounds and risk of pancreatic cancer. J Natl Cancer Inst 1992; 84: 764–71.
- 11 Hoppin JA, Tolbert PE, Holly EA, Brock JW, Korrick SA, Altshul LM, Zhang RH, Bracci PM, Burse VW, Needham LL. Pancreatic cancer and serum organochlorine levels. Cancer Epidemiol Biomarkers Prev 2000; 9: 199–205.
- 12 Cocco P, Fadda D, Billai B, D'Atri M, Melis M, Blair A. Cancer mortality among men occupationally exposed to dichlorodiphenyltrichloroethane. Cancer Res 2005; 65: 9588–94.
- 13 International Agency for Research on Cancer. Overall evaluations of carcinogenicity: an updating of IARC monographs volumes 1 to 42. Lyon: IARC, 1987. Monographs on the Evaluation of Carcinogenic Risk to Humans, Supplement 7.
- 14 International Agency for Research on Cancer. Occupational exposures in insecticide application, and some pesticides. Lyon: IARC, 1991. IARC Monographs on the Evaluation of Carcinogenic Risk to Humans, vol. 53.
- 15 International Agency for Research on Cancer. Some thyrotropic agents. Lyon: IARC, 2001. IARC Monographs on the Evaluation of Carcinogenic Risk to Humans, vol. 79.
- 16 Alavanja MC, Sandler DP, McMaster SB, Zahm SH, McDonnell CJ, Lynch CF, Pennybacker M, Rothman N, Dosemeci M, Bond AE, Blair A. The Agricultural Health Study. Environ Health Perspect 1996; 104: 362–69.
- 17 Agency for Toxic Substances and Disease Registry (ATSDR). Toxicological profile for aldrin and dieldrin. Atlanta, GA: U.S. Department of Health and Human Services, 2002.
- 18 Agency for Toxic Substances and Disease Registry (ATSDR). Toxicological profile for chlordane. Atlanta, GA: U.S. Department of Health and Human Services, 1994.
- 19 Agency for Toxic Substances and Disease Registry (ATSDR). Toxicological profile for DDT, DDE, DDD. Atlanta, GA: U.S. Department of Health and Human Services, 2002.
- 20 Agency for Toxic Substances and Disease Registry (ATSDR). Toxicological profile for heptachlor and heptachlor epoxide. Atlanta, GA: U.S. Department of Health and Human Services, 2005.
- 21 Agency for Toxic Substances and Disease Registry (ATSDR). Toxicological profile for hexachlorocyclohexanes (HCH). Atlanta, GA: U.S. Department of Health and Human Services, 2005.
- 22 Agency for Toxic Substances and Disease Registry (ATSDR). Toxicological profile for toxaphene. Atlanta, GA: U.S. Department of Health and Human Services, 1996.
- 23 Dosemeci M, Alavanja MC, Rowland AS, Mage D, Zahm SH, Rothman N, Lubin JH, Hoppin JA, Sandler DP, Blair A. A quantitative approach for estimating exposure to pesticides in the Agricultural Health Study. Ann Occup Hyg 2002; 46: 245–60.
- 24
Blair A,
Cantor KP,
Zahm SH.
Non-Hodgkin's lymphoma and agricultural use of the insecticide lindane.
Am J Ind Med
1998;
33:
82–7.
10.1002/(SICI)1097-0274(199801)33:1<82::AID-AJIM9>3.0.CO;2-Y CAS PubMed Web of Science® Google Scholar
- 25 McDuffie HH, Pahwa P, McLaughlin JR, Spinelli JJ, Fincham S, Dosman JA, Robson D, Skinnider LF, Choi NW. Non-Hodgkin's lymphoma and specific pesticide exposures in men: cross-Canada study of pesticides and health. Cancer Epidemiol Biomarkers Prev 2001; 10: 1155–63.
- 26 Rupa DS, Reddy PP, Reddi OS. Genotoxic effect of benzene hexachloride in cultured human lymphocytes. Hum Genet 1989; 83: 271–73.
- 27 Infante PF, Epstein SS, Newton WA,Jr. Blood dyscrasias and childhood tumors and exposure to chlordane and heptachlor. Scand J Work Environ Health 1978; 4: 137–50.
- 28 Epstein SS, Ozonoff D. Leukemias and blood dyscrasias following exposure to chlordane and heptachlor. Teratog Carcinog Mutagen 1987; 7: 527–40.
- 29 Chuang LF, Chuang RY. The effect of the insecticide heptachlor on ras proto-oncogene expression in human myeloblastic leukemia (ML-1) cells. Toxicology 1991; 70: 283–92.
- 30 Chuang LF, Chuang RY. Heptachlor and the mitogen-activated protein kinase module in human lymphocytes. Toxicology 1998; 128: 17–23.
- 31 Brown LM, Blair A, Gibson R, Everett GD, Cantor KP, Schuman LM, Burmeister LF, Van Lier SF, Dick F. Pesticide exposures and other agricultural risk factors for leukemia among men in Iowa and Minnesota. Cancer Res 1990; 50: 6585–91.
- 32 Cantor KP, Blair A, Everett G, Gibson R, Burmeister LF, Brown LM, Schuman L, Dick FR. Pesticides and other agricultural risk factors for non-Hodgkin's lymphoma among men in Iowa and Minnesota. Cancer Res 1992; 52: 2447–55.
- 33 Hardell L, Liljegren G, Lindstrom G, Van Bavel G, Broman K, Fredriksson M, Hagberg H, Nordstrom M, Johansson B. Increased concentrations of chlordane in adipose tissue from non-Hodgkin's lymphoma patients compared with controls without a malignant disease. Int J Oncol 1996; 9: 1139–42.
- 34 Cantor KP, Strickland PT, Brock JW, Bush D, Helzlsouer K, Needham LL, Zahm SH, Comstock GW, Rothman N. Risk of non-Hodgkin's lymphoma and prediagnostic serum organochlorines: β-hexachlorocyclohexane, chlordane/heptachlor-related compounds, dieldrin, and hexachlorobenzene. Environ Health Perspect 2003; 111: 179–83.
- 35 Majumdar SK, Kopelman HA, Schnitman MJ. Dieldrin-induced chromosome damage in mouse bone-marrow and WI-38 human lung cells. J Hered 1976; 67: 303–7.
- 36 Ribbens PH. Mortality study of industrial workers exposed to aldrin, dieldrin and endrin. Int Arch Occup Environ Health 1985; 56: 75–9.
- 37 de Jong G, Swaen GM, Slangen JJ. Mortality of workers exposed to dieldrin and aldrin: a retrospective cohort study. Occup Environ Med 1997; 54: 702–7.
- 38 Swaen GM, de Jong G, Slangen JJ, van Amelsvoort LG. Cancer mortality in workers exposed to dieldrin and aldrin: an update. Toxicol Ind Health 2002; 18: 63–70.
- 39 Settimi L, Comba P, Bosia S, Ciapini C, Desideri E, Fedi A, Perazzo PL, Axelson O. Cancer risk among male farmers: a multi-site case-control study. Int J Occup Med Environ Health 2001; 14: 339–47.
- 40 Cerhan JR, Cantor KP, Williamson K, Lynch CF, Torner JC, Burmeister LF. Cancer mortality among Iowa farmers: recent results, time trends, and lifestyle factors (United States). Cancer Causes Control 1998; 9: 311–19.
- 41 Reif J, Pearce N, Fraser J. Cancer risks in New Zealand farmers. Int J Epidemiol 1989; 18: 768–74.
- 42
Brownson RC,
Reif JS,
Chang JC,
Davis JR.
Cancer risks among Missouri farmers.
Cancer
1989;
64:
2381–6.
10.1002/1097-0142(19891201)64:11<2381::AID-CNCR2820641131>3.0.CO;2-M CAS PubMed Web of Science® Google Scholar
- 43 Wiklund K, Dich J. Cancer risks among female farmers in Sweden. Cancer Causes Control 1994; 5: 449–57.
- 44 Franceschi S, Barbone F, Bidoli E, Guarneri S, Serraino D, Talamini R, La Vecchia C. Cancer risk in farmers: results from a multi-site case-control study in north-eastern Italy. Int J Cancer 1993; 53: 740–5.
- 45 Blair A, Malker H, Cantor KP, Burmeister L, Wiklund K. Cancer among farmers. A review. Scand J Work Environ Health 1985; 11: 397–407.
- 46 Zhong Y, Rafnsson V. Cancer incidence among Icelandic pesticide users. Int J Epidemiol 1996; 25: 1117–24.
- 47 Samosh LV. Chromosome aberrations and character of satellite associations after accidental exposure of the human body to polychlorocamphene. Cytol Genet 1974; 8: 23–7.
- 48 Golden RJ, Noller KL, Titus-Ernstoff L, Kaufman RH, Mittendorf R, Stillman R, Reese EA. Environmental endocrine modulators and human health: an assessment of the biological evidence. Crit Rev Toxicol 1998; 28: 109–227.
- 49 Ritchie JM, Vial SL, Fuortes LJ, Guo H, Reedy VE, Smith EM. Organochlorines and risk of prostate cancer. J Occup Environ Med 2003; 45: 692–702.
- 50 Charles LE, Loomis D, Shy CM, Newman B, Millikan R, Nylander-French LA, Couper D. Electromagnetic fields, polychlorinated biphenyls, and prostate cancer mortality in electric utility workers. Am J Epidemiol 2003; 157: 683–91.
- 51 Pavuk M, Cerhan JR, Lynch CF, Schecter A, Petrik J, Chovancova J, Kocan A. Environmental exposure to PCBs and cancer incidence in eastern Slovakia. Chemosphere 2004; 54: 1509–20.
- 52 Ritchie JM, Vial SL, Fuortes LJ, Robertson LW, Guo H, Reedy VE, Smith EM. Comparison of proposed frameworks for grouping polychlorinated biphenyl congener data applied to a case-control pilot study of prostate cancer. Environ Res 2005; 98: 104–13.
- 53
Tarone RE,
Alavanja MC,
Zahm SH,
Lubin JH,
Sandler DP,
McMaster SB,
Rothman N,
Blair A.
The Agricultural Health Study: factors affecting completion and return of self-administered questionnaires in a large prospective cohort study of pesticide applicators.
Am J Ind Med
1997;
31:
233–42.
10.1002/(SICI)1097-0274(199702)31:2<233::AID-AJIM13>3.0.CO;2-2 CAS PubMed Web of Science® Google Scholar
- 54 Blair A, Tarone R, Sandler D, Lynch CF, Rowland A, Wintersteen W, Steen WC, Samanic C, Dosemeci M, Alavanja MC. Reliability of reporting on life-style and agricultural factors by a sample of participants in the Agricultural Health Study from Iowa. Epidemiology 2002; 13: 94–9.
- 55 Hoppin JA, Yucel F, Dosemeci M, Sandler DP. Accuracy of self-reported pesticide use duration information from licensed pesticide applicators in the Agricultural Health Study. J Expo Anal Environ Epidemiol 2002; 12: 313–8.
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