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Prostate cancer among pesticide applicators: a meta-analysis

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Abstract

Objectives: To analyse data from peer-reviewed, case-referent and cohort studies, studying the occurrence of prostate cancer in pesticide applicators and in some other, related, occupational categories, in order to determine a possible relationship of cancer of the prostate with pesticide exposure; to calculate a meta-rate ratio and to compare it with the meta-rate ratios obtained in a previous meta-analysis performed over a shorter time (1995–2001) in a broader exposure category, including many pesticide-related agricultural and non-agricultural occupations. Methods: Medline was searched for the years between 1966 and 2003, and relevant studies were identified from 1986 on. We conducted a meta-analysis of 22 studies complying with the inclusion criteria in order to pool their relative risk (RR) estimates. Studies were summarised and assessed for homogeneity and publication bias. Results: The meta-rate ratio, based on 22 estimates of RR, is 1.24 [95% confidence interval (95% CI) 1.06–1.45]. This pooled risk estimate for the occupational categories selected is higher than the one previously calculated for farmers in general over a shorter period of publication. Substantial heterogeneity of rate ratios exists between the different studies. The major source of heterogeneity identified is geographic location. Increased meta-rate ratios are observed for studies derived from North America as well as from Europe, the meta-rate ratios from Europe being lower than those from North America. There is no obvious indication of publication bias. Conclusion: The increased meta-rate ratio for prostate cancer in agricultural pesticide applications provides additional evidence for a possible relationship between pesticide exposure and prostate cancer. The homogeneity observed between the individual rate ratios, after we had regrouped the data according to geographic location, tends to increase the consistency of the association. However, the data available from the individual studies do not provide sufficient exposure information for firm conclusions to be drawn about pesticide exposure as the cause of prostate cancer, independently from other factors.

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References

  • Acquavella J, Olsen G, Cole P, Ireland B, Kaneene J, Schuman S, Holden L (1998) Cancer among farmers: a meta-analysis. Ann Epidemiol 8:64–74

    Article  CAS  PubMed  Google Scholar 

  • Acquavella J, Doe J, Tomenson J, Chester G, Cowell J, Bloemen L (2003) Epidemiologic studies of occupational pesticide exposure and cancer: regulatory risk assessments and biologic plausibility. Ann Epidemiol 13:1–7

    Article  PubMed  Google Scholar 

  • Alavanja MC, Sandler DP, McDonnell CJ, Lynch CF, Pennybacker M, Zahm SH, Mage DT, Steen WC, Wintersteen W, Blair A (1999) Characteristics of pesticide use in a pesticide applicator cohort: the Agricultural Health Study. Environ Res 80:172–179

    Article  CAS  PubMed  Google Scholar 

  • Alavanja MC, Samanic C, Dosemeci M, Lubin J, Tarone R, Lynch CF, Knott C, Thomas K, Hoppin JA, Barker J, Coble J, Sandler DP, Blair A (2003) Use of agricultural pesticides and prostate cancer risk in the agricultural health study cohort. Am J Epidemiol 157:800–814

    Article  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Aronson KJ, Siemiatycki J, Dewar R, Gerin M (1996) Occupational risk factors for prostate cancer: results from a case–control study in Montreal, Quebec, Canada. Am J Epidemiol 143:363–373

    CAS  PubMed  Google Scholar 

  • Band PR, Le ND, Fang R, Threlfall WJ, Gallagher RP (1999) Identification of occupational cancer risks in British Columbia. Part II: a population-based case–control study of 1516 prostatic cancer cases. J Occup Environ Med 41:233–247

    Google Scholar 

  • Blair A, Zahm SH (1991) Cancer among farmers. Occup Med 6:335–354

    CAS  PubMed  Google Scholar 

  • Blair A, Malker H, Cantor KP, Burmeister L, Wiklund K (1985) Cancer among farmers. Scand J Work Environ Health 11:397–407

    CAS  PubMed  Google Scholar 

  • Blair A, Zahm SH, Pearce NE, Heineman EF, Fraumeni JF Jr (1992) Clues to cancer etiology from studies of farmers. Scand J Work Environ Health 18:209–215

    CAS  PubMed  Google Scholar 

  • Burmeister LF (1981) Cancer mortality in Iowa farmers, 1971–78. J Natl Cancer Inst 66:461–464

    CAS  PubMed  Google Scholar 

  • Burmeister LF, Everett GD, Van Lier SF, Isacson P (1983) Selected cancer mortality and farm practices in Iowa. Am J Epidemiol 118:72–77

    CAS  PubMed  Google Scholar 

  • Buxton JA, Gallagher RP, Le ND, Band PR, Bert JL (1999) Occupational risk factors for prostate cancer mortality in British Columbia, Canada. Am J Ind Med 35:82–86

    Article  CAS  PubMed  Google Scholar 

  • Cantor KP, Booze CFJ (1991) Mortality among aerial pesticide applicators and flight instructors: a reprint. Arch Environ Health 46:110–116

    CAS  PubMed  Google Scholar 

  • Cantor KP, Silberman W (1999) Mortality among aerial pesticide applicators and flight instructors: follow-up from 1965–1988. Am J Ind Med 36:239–247

    Article  CAS  PubMed  Google Scholar 

  • Cerhan JR, Cantor KP, Williamson K, Lynch CF, Torner JC, Burmeister LF (1998) Cancer mortality among Iowa farmers: recent results, time trends, and lifestyle factors (United States). Cancer Causes Control 9:311–319

    Article  CAS  PubMed  Google Scholar 

  • Checkoway H, DiFerdinando G, Hulka B, Mickey D (1987) Medical, life-style, and occupational risk factors for prostate cancer. The Prostate 10:79–88

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • De Roos AJ, Zahm SH, Cantor KP, Weisenburger DD, Holmes FF, Burmeister LF, Blair A (2003) Integrative assessment of multiple pesticides as risk factors for non-Hodgkin’s lymphoma among men. Occup Environ Med 60: electronic paper: e11 (http://www.occenvmed.com/cgi/content/full/60/9/e11)

  • DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7:177–188

    Article  CAS  PubMed  Google Scholar 

  • Dich J, Wiklund K (1998) Prostate cancer in pesticide applicators in Swedish agriculture. Prostate 34:100–112

    Article  CAS  PubMed  Google Scholar 

  • Dich J, Zahm SH, Hanberg A, Adami HO (1997) Pesticides and cancer. Cancer Causes Control 8:420–443

    Article  CAS  PubMed  Google Scholar 

  • Dosemeci M, Alavanja MC, Rowland AS, Mage D, Zahm SH, Rothman N, Lubin, JH, Hoppin JA, Sandler DP, Blair A (2002) A quantitative approach for estimating exposure to pesticides in the agricultural health study. Ann Occup Hyg 46:245–260

    Article  CAS  PubMed  Google Scholar 

  • Egger M, Davey SG, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629–634

    CAS  PubMed  Google Scholar 

  • Ernster VL, Selvin S, Brown SM, Sacks ST, Winkelstein W Jr, Austin DF (1979) Occupation and prostatic cancer. A review and retrospective analysis based on death certificates in two California counties. J Occup Med 21:175–183

    CAS  PubMed  Google Scholar 

  • Ewings P, Bowie C (1996) A case–control study of cancer of the prostate in Somerset and east Devon. Br J Cancer 74:661–666

    CAS  PubMed  Google Scholar 

  • Figa-Talamanca I, Mearelli I, Valente P, Bascherini S (1993) Cancer mortality in a cohort of rural licensed pesticide users in the province of Rome. Int J Epidemiol 22:579–583

    CAS  PubMed  Google Scholar 

  • Fincham SM, Hanson J, Berkel J (1992) Patterns and risks of cancer in farmers in Alberta. Cancer 69:1276–1285

    CAS  PubMed  Google Scholar 

  • Fleming LE, Bean JA, Rudolph M, Hamilton K (1999a) Cancer incidence in a cohort of licensed pesticide applicators in Florida. J Occup Environ Med 41:279–288

    Google Scholar 

  • Fleming LE, Bean JA, Rudolph M, Hamilton K (1999b) Mortality in a cohort of licensed pesticide applicators in Florida. Occup Environ Med 56:14–21

    CAS  PubMed  Google Scholar 

  • Fleming LE, Gomez-Marin O, Zheng D, Ma F, Lee D (2003) National Health Interview Survey: mortality among US farmers and pesticide applicators. Am J Ind Med 43:227–233

    Article  PubMed  Google Scholar 

  • Forastiere F, Quercia A, Miceli M, Settimi L, Terenzoni B, Rapiti E, Faustini A, Borgia P, Cavariani F, Perucci CA (1993) Cancer among farmers in central Italy. Scand J Work Environ Health 19:382–389

    PubMed  Google Scholar 

  • Gambini GF, Mantovani C, Pira E, Piolatto PG, Negri E (1997) Cancer mortality among rice growers in Novara Province, northern Italy. Am J Ind Med 31:435–441

    Article  CAS  PubMed  Google Scholar 

  • Garry VF, Kelly JT, Sprafka JM, Edwards S, Griffith J (1994) Survey of health and use characterization of pesticide appliers in Minnesota. Arch Environ Health 49:337–343

    CAS  PubMed  Google Scholar 

  • Golden RJ, Noller KL, Titus-Ernstoff L, Kaufman RH, Mittendorf R, Stillman R, Reese EA (1998) Environmental endocrine modulators and human health: an assessment of the biological evidence. Crit Rev Toxicol 28:109–127

    CAS  PubMed  Google Scholar 

  • Grönberg H (2003) Prostate cancer epidemiology. Lancet 361:859–864

    Article  PubMed  Google Scholar 

  • van der Gulden JW, Kolk JJ, Verbeek AL (1995) Work environment and prostate cancer risk. Prostate 27:250–257

    PubMed  Google Scholar 

  • Hill A (1965) The environment and disease: association or causation. Proc R Soc Med 58:295–300

    CAS  PubMed  Google Scholar 

  • Hsing AW, Devesa SS (2001) Trends and patterns of prostate cancer: what do they suggest? Epidemiol Rev 23:3–13

    CAS  PubMed  Google Scholar 

  • Inskip H, Coggon D, Winter P, Pannett B (1996) Mortality of farmers and farmers’ wives in England and Wales 1979–80, 1982–90. Occup Environ Med 53:730–735

    CAS  PubMed  Google Scholar 

  • Keller-Byrne JE, Khuder SA, Schaub EA (1997) Meta-analyses of prostate cancer and farming. Am J Ind Med 31:580–586

    CAS  PubMed  Google Scholar 

  • Kogevinas M, Becher H, Benn T, Bertazzi PA, Boffetta P, Bueno de Mesquita HB, Coggon D, Colin D, Flesch-Janys D, Fingerhut M, Green L, Kauppinen T, Littorin M, Lynge E, Mathews JD, Neuberger M, Pearce N, Saracci R (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

    CAS  Google Scholar 

  • Koh D, Seow A (1999) Epidemiological basis of hazard identification. In: Sadhra S, Rampal K (eds) Occupational health—risk assessment and management. Blackwell, Oxford, pp 56–77

    Google Scholar 

  • Kristensen P, Andersen A, Irgens LM, Laake P, Bye AS (1996) Incidence and risk factors of cancer among men and women in Norwegian agriculture. Scand J Work Environ Health 22:14–26

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Lipsett M, Campleman S (1999) Occupational exposure to diesel exhaust and lung cancer: a meta-analysis. Am J Public Health 89:1009–1017

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Mills PK (1998) Correlation analysis of pesticide use data and cancer incidence rates in California counties. Arch Environ Health 53:410–413

    CAS  PubMed  Google Scholar 

  • Mills PK, Yang R (2003) Prostate cancer risk in California farm workers. J Occup Environ Med 45:249–258

    PubMed  Google Scholar 

  • Morrison H, Savitz D, Semenciw R, Hulka B, Mao Y, Morison D, Wigle D (1993) Farming and prostate cancer mortality. Am J Epidemiol 137:270–280

    CAS  PubMed  Google Scholar 

  • Moses M, Johnson ES, Anger WK, Burse VW, Horstman SW, Jackson RJ, Lewis RG, Maddy KT, McConnell R, Meggs WJ, et al (1993) Environmental equity and pesticide exposure. Toxicol Ind Health 9:913–959

    CAS  PubMed  Google Scholar 

  • Notkola VJ, Husman KR, Laukkanen VJ (1987) Mortality among male farmers in Finland during 1979–1983. Scand J Work Environ Health 13:124–128

    CAS  PubMed  Google Scholar 

  • Olkin I (1994) Re: “A critical look at some popular meta-analytic methods”. Am J Epidemiol 140:297–299

    CAS  PubMed  Google Scholar 

  • Parker AS, Cerhan JR, Putnam SD, Cantor KP, Lynch CF (1999) A cohort study of farming and risk of prostate cancer in Iowa. Epidemiology 10:452–455

    Article  CAS  PubMed  Google Scholar 

  • Ritchie JM, Vial S, Fuortes LJ, Guo H, Reedy VE, Smith EM (2003) Organochlorines and risk of prostate cancer. J Occup Environ Med 45:692–702

    CAS  PubMed  Google Scholar 

  • Ritter L, Wigle DT, Semenciw RM, Wilkins K, Riedel D, Mao Y (1990) Mortality study of Canadian male farm operators: cancer mortality and agricultural practices in Saskatchewan. Med Lav 81:499–505

    CAS  PubMed  Google Scholar 

  • Rooney AA, Guillette LJ (2000) Contaminant interactions with steroid receptors: evidence for receptor binding. In: Guillette LJ, Crain DA (eds) Environmental endocrine disrupters, an evolutionary perspective. Taylor and Francis, New York, pp 82–125

    Google Scholar 

  • Santti R, Newbold RR, Makela S, Pylkkanen L, McLachlan JA (1994) Developmental estrogenization and prostatic neoplasia. Prostate 24:67–78

    CAS  PubMed  Google Scholar 

  • Saracci R, Kogevinas M, Bertazzi PA, Bueno-de MB, Coggon D, Green LM, Kauppinen T, L’Abbé KA, Littorin M, Lynge E, Mathews JD, Neuberger M, Osman J, Pearce N, Winkelmann R (1991) Cancer mortality in workers exposed to chlorophenoxy herbicides and chlorophenols. Lancet 338:1027–1032

    Article  CAS  PubMed  Google Scholar 

  • Settimi L, Rapiti E, Forastiere F, Fano V, Pupp N, Callopoli A, Axelson O (1998) Cancer among greenhouse owners and their relatives: results of a pilot study. Am J Ind Med 33:88–89

    Article  CAS  PubMed  Google Scholar 

  • Settimi L, Comba P, Bosia S, Ciapini C, Desideri E, Fedi A, Perazzo PL, Axelson O (2001) Cancer risk among male farmers: a multi-site case–control study. Int J Occup Med Environ Health 14:339–347

    CAS  PubMed  Google Scholar 

  • Settimi L, Masina A, Andrion A, Axelson O (2003) Prostate cancer and exposure to pesticides in agricultural settings. Int J Cancer 104:458–461

    Article  CAS  PubMed  Google Scholar 

  • Sharma-Wagner S, Chokkalingam AP, Malker HS, Stone BJ, McLaughlin JK, Hsing AW (2000) Occupation and prostate cancer risk in Sweden. J Occup Environ Med 42:517–525

    CAS  PubMed  Google Scholar 

  • Signorello LB, Adami H-O (2002) Prostate cancer. In: Adami H-O, Hunter D, Trichopoulos D (eds) Textbook of cancer epidemiology. Oxford University Press, Oxford, pp 400–428

    Google Scholar 

  • Sperati A, Rapiti E, Settimi L, Quercia A, Terenzoni B, Forastiere F (1999) Mortality among male licensed pesticide users and their wives. Am J Ind Med 36:142–146

    Article  CAS  PubMed  Google Scholar 

  • Stark AD, Chang HG, Fitzgerald EF, Riccardi K, Stone RR (1987) A retrospective cohort study of mortality among New York State Farm Bureau members. Arch Environ Health 42:204–212

    CAS  PubMed  Google Scholar 

  • Susser M (1991) What is a cause and how do we know one? A grammar for pragmatic epidemiology. Am J Epidemiol 133:635–648

    CAS  PubMed  Google Scholar 

  • Swaen GM, van VC, Slangen JJ, Sturmans F (1992) Cancer mortality among licensed herbicide applicators. Scand J Work Environ Health 18:201–204

    CAS  PubMed  Google Scholar 

  • Tessier D, Matsumura F (2001) Increased ErbB-2 tyrosine kinase activity, MAPK phosphorylation, and cell proliferation in the prostate cancer cell line LNCaP following treatment by select pesticides. Toxicol Sci 60:38–43

    Article  CAS  PubMed  Google Scholar 

  • Torchio P, Lepore AR, Corrao G, Comba P, Settimi L, Belli S, Magnani C, di Orio F (1994) Mortality study on a cohort of Italian licensed pesticide users. Sci Total Environ 149:183–191

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Wiklund K (1983) Swedish agricultural workers. A group with a decreased risk of cancer. Cancer 51:566–568

    CAS  PubMed  Google Scholar 

  • Wiklund K, Dich J, Holm LE, Eklund G (1989) Risk of cancer in pesticide applicators in Swedish agriculture. Br J Ind Med 46:809–814

    CAS  PubMed  Google Scholar 

  • Woolf B (1955) On estimating the relation between blood group and disease. Ann Hum Genet 19:251–253

    CAS  PubMed  Google Scholar 

  • Zahm SH (1997) Mortality study of pesticide applicators and other employees of a lawn care service company. J Occup Environ Med 39:1055–1067

    Article  CAS  PubMed  Google Scholar 

  • Zhong Y, Rafnsson V (1996) Cancer incidence among Icelandic pesticide users. Int J Epidemiol 25:1117–1124

    CAS  PubMed  Google Scholar 

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Acknowledgments

G.V.M.F. was supported by a grant from the Ministry of Health.

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Van Maele-Fabry, G., Willems, J.L. Prostate cancer among pesticide applicators: a meta-analysis. Int Arch Occup Environ Health 77, 559–570 (2004). https://doi.org/10.1007/s00420-004-0548-8

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