Abstract
Purpose
The purpose of the present paper is to review cohort studies that examined the occurrence of prostate cancer in pesticide manufacturing workers in order to undertake a qualitative and quantitative evaluation of the risk as well as to assess the level of epidemiological evidence for each class of chemical compounds.
Methods
Following a systematic literature search, relative risk (RR) estimates for prostate cancer were extracted from 18 studies published between 1984 and 2004. All studies were summarised and evaluated for homogeneity and publication bias. As no significant heterogeneity was detected, combined RR estimators were calculated using a fixed effect model. Meta-analyses were performed both on the whole set of data and for each chemical class separately.
Results
The meta-rate ratio estimate for all studies was 1.28 [95% confidence interval (CI) 1.05–1.58]. After stratification by specific chemical class, consistent increases in the risk of prostate cancer were found in all groups but statistical significance was found only for accidental or non-accidental exposure to phenoxy herbicides contaminated with dioxins and furans. There was no obvious indication of publication bias.
Conclusion
The overall meta-analysis provides additional quantitative evidence consistent with prior reviews focusing on other groups exposed to pesticides (farmers, pesticide applicators). The results again point to occupational exposure to pesticides as a possible risk factor for prostate cancer but the question of causality remains unanswered. Epidemiological evidence did not allow identifying a specific pesticide or chemical class that would be responsible for the increased risk but the strongest evidence comes from workers exposed to phenoxy herbicides possibly in relation with dioxin and/or furan contamination.
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References
Blair A, Zahm SH, Pearce NE, Heineman EF, Fraumeni JF (1992) Clues to cancer etiology from studies of farmers. Scand J Work Environ Health 18:209–215
van der Gulden JW, Vogelzang PF (1996) Farmers at risk for prostate cancer. Br J Urol 77:6–14
Keller BJ, Khuder SA, Schaub EA (1997) Meta-analyses of prostate cancer and farming. Am J Ind Med 31:580–586
Acquavella J, Olsen G, Cole P et al. (1998) Cancer among farmers: a meta-analysis. Ann Epidemiol 8:64–74
Van Maele-Fabry G, Willems JL (2003) Occupation related pesticide exposure and cancer of the prostate: a meta-analysis. Occup Environ Med 60:634–642
Van Maele-Fabry G, Willems JL (2004) Prostate cancer among pesticide applicators: a meta-analysis. Int Arch Occup Environ Health 77:559–570
Krstev S, Baris D, Stewart PA, Hayes RB, Blair A, Dosemeci M (1998) Risk for prostate cancer by occupation and industry: a 24-state death certificate study. Am J Ind Med 34:413–420
Andersen A, Barlow L, Engeland A, Kjaerheim K, Lynge E, Pukkala E (1999) Work-related cancer in the Nordic countries. Scand J Work Environ Health 25(Suppl 2):1–116
Zeegers MPA, Friesema IHM, Goldbohm RA, van den Brandt PA (2004) A prospective study of occupation and prostate cancer risk. J Occup Environ Med 46:271–279
Gann PH (2002) Risk factors for prostate cancer. Rev Urol 4(Suppl 5):S3–S10
Parent ME, Siemiatycki J (2001) Occupation and prostate cancer. Epidemiol Rev 23:138–143
Maroni M, Fait A (1993) Health effects in man from long-term exposure to pesticides. A review of the 1975–1991 literature. Toxicology 78:1–180
Bruce HA, Bloemen L, Allen RH (2005) Sessions on the epidemiology of agricultural exposure and cancer. Scand J Work Environ Health 31(Suppl 1):5–7
Leet T, Acquavella J, Lynch C et al. (1996) Cancer incidence among alachlor manufacturing workers. Am J Ind Med 30:300–306
Sathiakumar N, Delzell E (1997) A review of epidemiological studies of triazine herbicides and cancer. Crit Rev Toxicol 27:599–613
MacLennan PA, Delzell E, Sathiakumar N, Myers SL (2003) Mortality among triazine herbicide manufacturing workers. J Toxicol Environ Health-Part A 66:501–517
Breslow NE, Day NE (1987) Statistical methods in cancer research: The design and analysis of cohort studies. IARC scientific publications, vol. II, no. 82. International Agency for Research on Cancer, Lyon
Wong O, Brocker W, Davis HV, Nagle GS (1984) Mortality of workers potentially exposed to organic and inorganic brominated chemicals, DBCP, TRIS, PBB, and DDT. Br J Ind Med 41:15–24
Collins JJ, Strauss ME, Levinskas GJ, Conner PR (1993) The mortality experience of workers exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin in a trichlorophenol process accident. Epidemiology 4:7–13
Ramlow JM, Spadacene NW, Hoag SR, Stafford BA, Cartmill JB, Lerner PJ (1996) Mortality in a cohort of pentachlorophenol manufacturing workers, 1940–1989. Am J Ind Med 30:180–194
Bodner KM, Collins JJ, Bloemen LJ, Carson ML (2003) Cancer risk for chemical workers exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Occup Environ Med 60:672–675
Fingerhut MA, Halperin WE, Marlow DA et al. (1991) Cancer mortality in workers exposed to 2,3,7,8-tetrachlorodibenzo-para-dioxin. N Engl J Med 324:212–218
Steenland K, Piacitelli L, Deddens J, Fingerhut M, Chang LI (1999) Cancer, heart disease, and diabetes in workers exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. J Natl Cancer Inst 91:779–786
Cook RR, Townsend JC, Ott MG, Silverstein LG (1980) Mortality experience of employees exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). J Occup Med 22:530–532
Hooiveld M, Heederik DJ, Kogevinas M et al. (1998) Second follow-up of a Dutch cohort occupationally exposed to phenoxy herbicides, chlorophenols, and contaminants. Am J Epidemiol 147:891–901
Becher H, Flesch JD, Kauppinen T et al. (1996) Cancer mortality in German male workers exposed to phenoxy herbicides and dioxins. Cancer Causes Control 7:312–321
Flesch-Janys D, Steindorf K, Gurn P, Becher H (1998) Estimation of the cumulated exposure to polychlorinated dibenzo- p-dioxins/furans and standardized mortality ratio analysis of cancer mortality by dose in an occupationally exposed cohort. Environ Health Perspect 106:655–662
Bueno de Mesquita HB, Doornbos G, Van der Kuip DA, Kogevinas M, Winkelmann R (1993) Occupational exposure to phenoxy herbicides and chlorophenols and cancer mortality in The Netherlands. Am J Ind Med 23:289–300
Hooiveld M, Heederik D, Bueno de Mesquita HB (1996) Preliminary results of the second follow-up of a Dutch cohort of workers occupationally exposed to phenoxy herbicides, chlorophenols and contaminants. Organohalogen Compounds 30:185–189
Clarke M, Oxman AD (eds) (2000) Cochrane Reviewers’ Handbook 4.1 (updated June 2000). In: Review Manager (RevMan) (computer program). Version 4.1. The Cochrane Collaboration 2000, Oxford, England
Lipsett M, Campleman S (1999) Occupational exposure to diesel exhaust and lung cancer: a meta-analysis. Am J Public Health 89:1009–1017
Woolf B (1955) On estimating the relation between blood group and disease. Ann Hum Genet 19:251–253
Stewart RE, Dennis LK, Dawson DV, Resnick MI (1999) A meta-analysis of risk estimates for prostate cancer related to tire and rubber manufacturing operations. J Occup Environ Med 41:1079–1084
Dennis LK (2000) Meta-analysis for combining relative risks of alcohol consumption and prostate cancer. Prostate 42:56–66
Swaen GG, de Jong G, Slangen JJ, van Amelsvoort LG (2002) Cancer mortality in workers exposed to dieldrin and aldrin: an update. Toxicol Ind Health 18:63–70
Ott MG, Zober A (1996) Cause specific mortality and cancer incidence among employees exposed to 2,3,7,8-TCDD after a 1953 reactor accident. Occup Environ Med 53:606–612
Acquavella JF, Delzell E, Cheng H, Lynch CF, Johnson G (2004) Mortality and cancer incidence among alachlor manufacturing workers 1968–99. Occup Environ Med 61:680–685
MacLennan PA, Delzell E, Sathiakumar N et al. (2002) Cancer incidence among triazine herbicide manufacturing workers. J Occup Environ Med 44:1048–1058
Lynge E (1998) Cancer incidence in Danish phenoxy herbicide workers, 1947–1993. Environ Health Perspect 106(Suppl 2):683–688
Egger M, Davey SG, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634
Shindell S, Ulrich S (1986) Mortality of workers employed in the manufacture of chlordane: an update. J Occup Med 28:497–501
Amoateng-Adjepong Y, Sathiakumar N, Delzell E, Cole P (1995) Mortality among workers at a pesticide manufacturing plant. J Occup Environ Med 37:471–478
Wang HH, MacMahon B (1979) Mortality of workers employed in the manufacture of chlordane and heptachlor. J Occup Med 21:745–748
Ditraglia D, Brown DP, Namekata T, Iverson N (1981) Mortality study of workers employed at organochlorine pesticide manufacturing plants. Scand J Work Environ Health 7:140–146
Brown DP (1992) Mortality of workers employed at organochlorine pesticide manufacturing plants—an update. Scand J Work Environ Health 18:155–161
Jager KW (1970) Aldrin, dieldrin, endrin and telodrin—an epidemiological and toxicological study of long term occupational exposure. Elsevier Publishing Company, Amsterdam
Versteeg JPJ, Jager KW (1973) Long-term occupational exposure to the insecticides aldrin, dieldrin, endrin and telodrin. Br J Ind Med 30:201–202
Van Raalte HGS (1977) Human experience with dieldrin in perspective. Ecotoxicol Environ Saf 1:203–210
Ribbens PH (1985) Mortality study of industrial workers exposed to aldrin, dieldrin and endrin. Int Arch Occup Environ Health 56:75–79
de Jong G (1991) Long-term health effects of aldrin and dieldrin. Toxicol Lett (Suppl):1–206
de Jong G, Swaen GM, Slangen JJ (1997) Mortality of workers exposed to dieldrin and aldrin: a retrospective cohort study. Occup Environ Med 54:702–707
Acquavella JF, Riordan SG, Anne M, Lynch CF, Collins JJ, Ireland BK, Heydens WF (1996) Evaluation of mortality and cancer incidence among alachlor manufacturing workers. Environ Health Perspect 104:728–733
Sathiakumar N, Delzell E, Austin H, Cole P (1992) A follow- up-study of agricultural chemical production workers. Am J Ind Med 21:321–330
Sathiakumar N, Delzell E, Cole P (1996) Mortality among workers at two triazine herbicide manufacturing plants. Am J Ind Med 29:143–151
Hearn S, Ott MG, Kolesar RC, Cook RR (1984) Mortality experience of employees with occupational exposure to DBCP. Arch Environ Health 39:49–55
Olsen GW, Bodner KM, Stafford BA, Cartmill JB, Gondek MR (1995) Update of the mortality experience of employees with occupational exposure to 1,2-dibromo-3-chloropropane (DBCP). Am J Ind Med 28:399–410
Saracci R, Kogevinas M, Bertazzi PA et al. (1991) Cancer mortality in workers exposed to chlorophenoxy herbicides and chlorophenols. Lancet 338:1027–1032
Kauppinen TP, Kogevinas M, Johnson E et al. (1993) Chemical exposure in manufacture of phenoxy herbicides and chlorophenols and in spraying of phenoxy herbicides. Am J Ind Med 23:903–920
Kauppinen TP, Pannett B, Marlow DA, Kogevinas M (1994) Retrospective assessment of exposure through modeling in a study on cancer risks among workers exposed to phenoxy herbicides, chlorophenols and dioxins. Scand J Work Environ Health 20:262–271
Kogevinas M, Becher H, Benn T et al. (1997) Cancer mortality in workers exposed to phenoxy herbicides, chlorophenols, and dioxins. An expanded and updated international cohort study. Am J Epidemiol 145:1061–1075
Lynge E (1985) A follow-up study of cancer incidence among workers in manufacture of phenoxy herbicides in Denmark. Br J Cancer 52:259–270
Lynge E (1987) Background and design of a Danish cohort study of workers in phenoxy herbicide manufacture. Am J Ind Med 11:427–437
Lynge E (1993) Cancer in phenoxy herbicide manufacturing workers in Denmark, 1947–87—an update. Cancer Causes Control 4:261–272
Coggon D, Pannett B, Winter PD, Acheson ED, Bonsall J (1986) Mortality of workers exposed to 2 methyl-4 chlorophenoxyacetic acid. Scand J Work Environ Health 12: 448–454
Bishop CM, Jones AH (1981) Non-Hodgkins lymphoma of the scalp in workers exposed to dioxins. Lancet 318:369
Coggon D, Pannett B, Winter P (1991) Mortality and incidence of cancer at four factories making phenoxy herbicides. Br J Ind Med 48:173–178
Becher H, Wahrendorf J, Angerer R (1992) A cohort study on persons exposed to phenoxy acid herbicides and their contaminants in Germany—design and 1st results. Chemosphere 25:1007–1014
Manz A, Berger J, Dwyer JH, Flesch-Janys D, Nagel S, Waltsgott H (1991) Cancer mortality among workers in chemical-plant contaminated with dioxin. Lancet 338:959–964
Flesch-Janys D, Berger J, Gurn P et al. (1995) Exposure to polychlorinated dioxins and furans (PCDD/F) and mortality in a cohort of workers from a herbicide-producing plant in Hamburg, Federal Republic of Germany. Am J Epidemiol 142:1165–1175
Becher H, Steindorf K, Flesch-Janys D (1998) Quantitative cancer risk assessment for dioxins using an occupational cohort. Environ Health Perspect 106:663–670
Thiess AM, Frentzel-Beyme R (1977) Mortality study of persons exposed to dioxin following an accident which occurred in the BASF on November 1953. Proceedings of the Vth International Conference Medichem, San Francisco, pp. 228–236
Thiess AM, Frentzel-Beyme R, Link R (1982) Mortality study of persons exposed to dioxin in a trichlorophenol-process accident that occurred in the BASF AG on November 17, 1953. Am J Ind Med 3:179–189
Zober A, Messerer P, Huber P (1990) 34-year mortality follow-up of BASF employees exposed to 2,3,7,8-Tcdd after the 1953 accident. Int Arch Occup Environ Health 62:139–157
Zober A, Ott MG, Messerer P (1994) Morbidity follow-up-study of BASF employees exposed to 2,3,7,8-tetrachlorodibenzo- p-dioxin (Tcdd) after a 1953 chemical reactor incident. Occup Environ Med 51:479–486
Zober A, Messerer P, Ott MG (1997) BASF studies: epidemiological and clinical investigations on dioxin-exposed chemical workers. Teratog Carcinog Mutagen 17:249–256
Zack JA, Suskind RR (1980) The mortality experience of workers exposed to tetrachlorodibenzodioxin in a trichlorophenol process accident. J Occup Med 22:11–14
Zack JA, Gaffey WR (1983) A mortality study of workers employed at the Monsanto Company plant in Nitro, West Virginia. Environ Sci Res 26:575–591
Bond GG, Wetterstroem NH, Roush GJ, McLaren EA, Lipps TE, Cook RR (1988) Cause specific mortality among employees engaged in the manufacture, formulation, or packaging of 2,4-dichlorophenoxyacetic acid and related salts. Br J Ind Med 45:98–105
Burns CJ, Beard KK, Cartmill JB (2001) Mortality in chemical workers potentially exposed to 2,4-dichlorophenoxyacetic acid (2,4-D) 1945–94: an update. Occup Environ Med 58:24–30
Ott MG, Holder BB, Olson RD (1980) A mortality analysis of employees engaged in the manufacture of 2,4,5-trichlorophenoxyacetic acid. J Occup Med 22:47–50
Cook RR, Bond GG, Olson RA, Ott MG, Gondek MR (1986) Evaluation of the mortality experience of workers exposed to the chlorinated dioxins. Chemosphere 15:1769–1776
Ott MG, Olson RA, Cook RR, Bond GG (1987) Cohort mortality study of chemical workers with potential exposure to the higher chlorinated dioxins. J Occup Med 29:422–429
Bond GG, McLaren EA, Lipps TE, Cook RR (1989) Update of mortality among chemical workers with potential exposure to the higher chlorinated dioxins. J Occup Environ Med 31:121–123
Alavanja MCR, Hoppin JA, Kamel F (2004) Health effects of chronic pesticide exposure: cancer and neurotoxicity. Annu Rev Public Health 25:155–197
Alavanja MC, Samanic C, Dosemeci M et al. (2003) Use of agricultural pesticides and prostate cancer risk in the agricultural health study cohort. Am J Epidemiol 157:800–814
Hsing AW, Devesa SS (2001) Trends and patterns of prostate cancer: what do they suggest?. Epidemiol Rev 23:3–13
Greenberg RS, Mandel J, Pastides H, Britton NL, Rudenko L, Starr TB (2001) A meta-analysis of cohort studies describing mortality and cancer incidence among chemical workers in the United States and Western Europe. Epidemiology 12:727–740
Hill A (1965) The environment and disease: association or causation. Proc R Soc Med 58:295–300
Susser M (1991) What is a cause and how do we know one—a grammar for pragmatic epidemiology. Am J Epidemiol 133:635–648
Koh D, Seow A (1999) Epidemiological basis of hazard identification. In: Sadhra S, Rampal K (eds) Occupational health. 1 Oxford: Blackwell Science Ltd, pp. 56–77
Hessel PA, Kalmes R, Smith TJ, Lau E, Mink PJ, Mandel J (2004) A nested case–control study of prostate cancer and atrazine exposure. J Occup Environ Med 46:379–385
Alberghini V, Luberto F, Gobba F, Morelli C, Gori E, Tomesani N (1991) Mortality among male farmers licensed to use pesticides. Med Lav 82:18–24
Cocco P, Blair A, Congia P, Saba G, Ecca AR, Palmas C (1997) Long-term health effects of the occupational exposure to DDT A preliminary report. Ann NY Acad Sci 837:246–256
Cocco P, Benichou J (1998) Mortality from cancer of the male reproductive tract and environmental exposure to the anti-androgen p,p′-dichlorodiphenyldichloroethylene in the United States. Oncology 55:334–339
Mills PK (1998) Correlation analysis of pesticide use data and cancer incidence rates in California counties. Arch Environ Health 53:410–413
Janssens JP, Van Hecke E, Geys H, Bruckers L, Renard D, Molenberghs G (2001) Pesticides and mortality from hormone-dependent cancers. Eur J Cancer Prev 10:459–467
Beard J, Sladden T, Morgan G, Berry G, Brooks L, McMichael A (2003) Health impacts of pesticide exposure in a cohort of outdoor workers. Environ Health Perspect 111:724–730
Mills PK, Yang R (2003) Prostate cancer risk in California farm workers. J Occup Environ Med 45:249–258
Ritchie JM, Vial SL, Fuortes LJ, Guo HJ, Reedy VE, Smith EM (2003) Organochlorines and risk of prostate cancer. J Occup Environ Med 45:692–702
Settimi L, Masina A, Andrion A, Axelson O (2003) Prostate cancer and exposure to pesticides in agricultural settings. Int J Cancer 104:458–461
Pavuk M, Cerhan JR, Lynch CF et al (2004) Environmental exposure to PCBs and cancer incidence in eastern Slovakia. Chemosphere 54:1509–1520
Lee WJ, Hoppin JA, Blair A et al (2004) Cancer incidence among pesticide applicators exposed to alachlor in the agricultural health study. Am J Epidemiol 159:373–380
Rusiecki JA, De Roos A, Lee WJ et al (2004) Cancer incidence among pesticide applicators exposed to atrazine in the agricultural health study. J Natl Cancer Inst 96:1375–1382
Wesseling C, Ahlbom A, Antich D, Rodriguez AC, Castro R (1996) Cancer in banana plantation workers in Costa Rica. Int J Epidemiol 25:1125–1131
Riihimaki V, Asp S, Pukkala E, Hernberg S (1983) Mortality and cancer morbidity among chlorinated phenoxyacid applicators in Finland. Chemosphere 12:779–784
Riihimaki V, Asp S, Hernberg S (1982) Mortality of 2,4-dichlorophenoxyacetic acid and 2,4,5-trichlorophenoxyacetic acid herbicide applicators in Finland: first report of an ongoing prospective cohort study. Scand J Work Environ Health 8:37–42
Morrison H, Savitz D, Semenciw R et al (1993) Farming and prostate cancer mortality. Am J Epidemiol 137:270–280
Asp S, Riihimaki V, Hernberg S, Pukkala E (1994) Mortality and cancer morbidity of Finnish chlorophenoxy herbicide applicators: an 18-year prospective follow-up. Am J Ind Med 26:243–253
Torchio P, Lepore AR, Corrao G et al. (1994) Mortality study on a cohort of Italian licensed pesticide users. Sci Total Environ 149:183–191
Zahm SH (1997) Mortality study of pesticide applicators and other employees of a lawn care service company. J Occup Environ Med 39:1055–1067
Dich J, Wiklund K (1998) Prostate cancer in pesticide applicators in Swedish agriculture. Prostate 34:100–112
Schreinemachers DM, (2000) Cancer mortality in four northern wheat-producing states. Environ Health Perspect 108:873–881
Cocco P (2002) On the rumors about the silent spring. Review of the scientific evidence linking occupational and environmental pesticide exposure to endocrine disruption health effects. Cad Saude Publica 18:379–402
Stoker TE, Laws SC, Guidici DL, Cooper RL (2000) The effect of atrazine on puberty in male Wistar rats: an evaluation in the protocol for the assessment of pubertal development and thyroid function. Toxicol Sci 58:50–59
Kelce WR, Stone CR, Laws SC, Gray LE, Kemppainen JA, Wilson EM (1995) Persistent DDT metabolite p,p′-DDE is a potent androgen receptor antagonist. Nature 375:581–585
Kniewald J, Osredecki V, Gojmerac T, Zechner V, Kniewald Z (1995) Effect of S-triazine compounds on testosterone-metabolism in the rat prostate. J Appl Toxicol 15:215–218
Sanderson JT, Seinen W, Giesy JP, van den Berg M (2000) 2-Chloro-s-triazine herbicides induce aromatase (CYP19) activity in H295R human adrenocortical carcinoma cells: a novel mechanism for estrogenicity? Toxicol Sci 54:121–127
Sanderson JT, Letcher RJ, Heneweer M, Giesy JP, van den Berg M (2001) Effects of chloro-s-triazine herbicides and metabolites on aromatase activity in various human cell lines and on vitellogenin production in male carp hepatocytes. Environ Health Perspect 109:1027–1031
Hayes TB, Collins A, Lee M et al. (2002) Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses. Proc Natl Acad Sci USA 99:5476–5480
Babic-Gojmerac T, Kniewald Z, Kniewald J (1989) Testosterone metabolism in neuroendocrine organs in male rats under atrazine and deethylatrazine influence. J Steroid Biochem 33:141–146
Das PC, McElroy WK, Cooper RL (2003) Potential mechanisms responsible for chlorotriazine-induced alterations in catecholamines in pheochromocytoma (PC12) cells. Life Sci 73:3123–3138
Fujimoto N, Honda H (2003) Effects of environmental estrogenic compounds on growth of a transplanted estrogen responsive pituitary tumor cell line in rats. Food Chem Toxicol 41:1711–1717
Goulet BN, Hontela A (2003) Toxicity of cadmium, endosulfan, and atrazine in adrenal steroidogenic cells of two amphibian species, Xenopus laevis and Rana catesbeiana. Environ Toxicol Chem 22:2106–2113
Short P, Colborn T (1999) Pesticide use in the U.S. and policy implications: a focus on herbicides. Toxicol Ind Health 15:240–275
Straube E, Straube W, Kruger E, Bradatsch M, Jacob-Meisel M, Rose HJ (1999) Disruption of male sex hormones with regard to pesticides: pathophysiological and regulatory aspects. Toxicol Lett 107:225–231
Garry VF, Tarone RE, Kirsch IR et al. (2001) Biomarker correlations of urinary 2,4-d levels in foresters: genomic instability and endocrine disruption. Environ Health Perspect 109:495–500
Dearfield KL, McCarroll NE, Protzel A et al. (1999) A survey of EPA/OPP and open literature on selected pesticide chemicals—II. Mutagenicity and carcinogenicity of selected chloroacetanilides and related compounds. Mutat Res 443:183–221
Rosenkranz HS (1975) Genetic activity of 1,2-dibromo-3-chloropropane, a widely used fumigant. Bull Environ Contam Toxicol 14:8–12
Kato Y, Sato K, Makai S, Matano O, Goto S (1979) Metabolic fate of 1,2-dibromo-3-chloropropane (DBCP) in rats. J Pest Sci 4:195–203
Kato Y, Sato K, Matano O, Goto S (1980) Metabolic fate of DBCP in rats. 2. Alkylation of cellular macromolecules by reactive metabolic intermediates of DBCP. J Pest Sci 5:45–53
Suzuki K, Lee IP (1981) Induction of aryl hydrocarbon hydroxylase and epoxide hydrolase in rat, liver, kidney, testes, prostate gland and stomach by a potent nematocide, 1,2-dibromo-3-chloropropane. Toxicol Appl Pharmacol 58:151– 155
Ryu JC, Kim YJ, Chai YG (2002) Mutation spectrum of 1,2-dibromo-3-chloropropane, an endocrine disruptor, in the lacI transgenic Big Blue Rat2 fibroblast cell line. Mutagenesis 17:301–307
International Agency for Research on Cancer (IARC) (1987) IARC monographs on the evaluation of the carcinogenic risk of chemicals to humans, vol. 41
Ibrahim MA, Bond GG, Burke TA et al. (1991) Weight of the evidence on the human carcinogenicity of 2,4-D. Environ Health Perspect 96:213–222
Bond GG, Rossbacher R (1993) A review of potential human carcinogenicity of the chlorophenoxy herbicides MCPA, MCPP, and 2,4-DP. Br J Ind Med 50:340–348
Garabrant DH, Philbert MA (2002) Review of 2,4-dichlorophenoxyacetic acid (2,4-D) epidemiology and toxicology. Crit Rev Toxicol 32:233–257
International Agency for Research on Cancer (IARC) (1997) Polychlorinated dibenzo-para-dioxins and polychlorinated dibenzofurans. IARC Monogr Eval Carcinog Risk Chem Hum 69:1–666
Cole P, Trichopoulos D, Pastides H, Starr T, Mandel JS, (2003) Dioxin and cancer: a critical review. Regul Toxicol Pharmacol 38:378–388
Crump KS, Canady R, Kogevinas M (2003) Meta-analysis of dioxin cancer dose response for three occupational cohorts. Environ Health Perspect 111:681–687
Starr TB (2003) Significant issues raised by meta-analyses of cancer mortality and dioxin exposure. Environ Health Perspect 111:1443–1447
Steenland K, Bertazzi PA, Baccarelli A, Kogevinas M (2004) Dioxin revisited: developments since the 1997 IARC classification of dioxin as a human carcinogen. Environ Health Perspect 112:1265–1268
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V.M.F.G. was supported by a grant from the Ministry of Health.
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Van Maele-Fabry, G., Libotte, V., Willems, J. et al. Review and Meta-analysis of Risk Estimates for Prostate Cancer in Pesticide Manufacturing Workers. Cancer Causes Control 17, 353–373 (2006). https://doi.org/10.1007/s10552-005-0443-y
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DOI: https://doi.org/10.1007/s10552-005-0443-y