Skip to main content
SpringerLink
Log in

A weight-of-evidence review of colorectal cancer in pesticide applicators: the agricultural health study and other epidemiologic studies

  • Review
  • Published:
International Archives of Occupational and Environmental Health Aims and scope Submit manuscript

Abstract

Objective

To systematically evaluate epidemiologic studies on pesticides and colon cancer and rectal cancer in agricultural pesticide applicator populations using a transparent “weight-of-evidence” (WOE) methodological approach.

Methods

Twenty-nine (29) publications from the Agricultural Health Study (AHS) and 13 additional epidemiologic studies were identified that reported data for pesticide applicators and/or specific pesticide compounds and colorectal, colon, or rectal cancer. The AHS evaluated pesticide applicators as well as dose–response associations for specific pesticide compounds, whereas the large majority of non-AHS evaluated applicators but did not analyze specific compounds or dose–response trends. This WOE assessment of 153 different pesticide–outcome pairs emphasized several key evidentiary features: existence of statistically significant relative risks, magnitude of observed associations, results from the most reliable exposure assessments, and evidence of convincing dose–response relationships (i.e., those monotonically increasing, with statistically significant trend tests).

Results

Occupation as a pesticide applicator or pesticide application as a farming-related function was not associated with increasing the risk of colon or rectal cancer. Deficits of colon or rectal cancer were observed across most studies of pesticide applicators. After applying the WOE methodology to the epidemiologic studies of specific pesticide compounds and colon or rectal cancer, a number of pesticide–outcome pairs were identified and evaluated further based on positive statistical associations. Of these, only two—aldicarb and colon cancer and imazethapyr and proximal colon cancer—appears to warrant further discussion regarding a possible causal relationship, although the epidemiologic data are limited. For the remainder, a lack of a clear dose–response trend, inconsistencies in associations between exposure metrics and comparison groups, imprecise associations, variable participation rates for analyses of specific compounds, and the reliance upon data from one study (the AHS) limit interpretation regarding risk.

Conclusion

The available epidemiologic evidence does not support a causal relationship between occupation as a pesticide applicator or specific pesticide exposures and colon or rectal cancer.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

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(1):64–74

    Article  CAS  Google Scholar 

  • 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(8):680–685

    Article  CAS  Google Scholar 

  • Acquavella JF, Alexander BH, Mandel JS, Burns CJ, Gustin C (2006) Exposure misclassification in studies of agricultural pesticides: insights from biomonitoring. Epidemiology 17:69–74

    Article  Google Scholar 

  • Alavanja MC, Sandler DP, McMaster SB, Zahm SH, McDonnell CJ, Lynch CF, Pennybacker M, Rothman N, Dosemeci M, Bond AE, Blair A (1996) The Agricultural Health Study. Environ Health Perspect 104(4):362–369

    Article  CAS  Google Scholar 

  • Alavanja MC, Sandler DP, Lynch CF, Knott C, Lubin JH, Tarone R, Thomas K, Dosemeci M, Barker J, Hoppin JA, Blair A (2005) Cancer incidence in the agricultural health study. Scand J Work Environ Health 31(Suppl 1):39–45

    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(1):18–24

    CAS  Google Scholar 

  • Alexander DD, Cushing CA, Lowe KA, Sceurman B, Roberts MA (2009) Meta-analysis of animal fat or animal protein intake and colorectal cancer. Am J Clin Nutr 89(5):1402–1409

    Article  CAS  Google Scholar 

  • Aschengrau A, Seage GR (2003) Essentials of epidemiology in public health. Jones and Bartlett, Sudbury

    Google Scholar 

  • 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

    Google Scholar 

  • Beaglehole R, Bonita R, Kjellström T (1993) Basic epidemiology. World Health Organization, Geneva

    Google Scholar 

  • Beane Freeman LE, Bonner MR, Blair A, Hoppin JA, Sandler DP, Lubin JH, Dosemeci M, Lynch CF, Knott C, Alavanja MC (2005) Cancer incidence among male pesticide applicators in the Agricultural Health Study cohort exposed to diazinon. Am J Epidemiol 162(11):1070–1079

    Article  Google Scholar 

  • 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(5):724–730

    Article  CAS  Google Scholar 

  • Bhopal RS (2005) Concepts of epidemiology: an integrated introduction to the ideas. Oxford University Press, Oxford

    Google Scholar 

  • Blair A, Zahm SH (1991) Cancer among farmers. Occup Med 6(3):335–354

    CAS  Google Scholar 

  • Blair A, Malker H, Cantor KP, Burmeister L, Wiklund K (1985) Cancer among farmers. A review. Scand J Work Environ Health 11(6):397–407

    Article  CAS  Google Scholar 

  • Blair A, Tarone R, Sandler D, Lynch C, Rowland A, Wintersteen W, Steen W, Dosemeci M, Alavanja M (2000) Reliability of reporting on lifestyle and agricultural factors by a sample of participants in the agricultural health study from iowa. Ann Epidemiol 10(7):478

    Article  Google Scholar 

  • Blair A, Tarone R, Sandler D, Lynch CF, Rowland A, Wintersteen W, Steen WC, Samanic C, Dosemeci M, Alavanja MC (2002) Reliability of reporting on life-style and agricultural factors by a sample of participants in the Agricultural Health Study from Iowa. Epidemiology 13(1):94–99

    Article  Google Scholar 

  • Blair A, Sandler DP, Tarone R, Lubin J, Thomas K, Hoppin JA, Samanic C, Coble J, Kamel F, Knott C, Dosemeci M, Zahm SH, Lynch CF, Rothman N, Alavanja MC (2005) Mortality among participants in the agricultural health study. Ann Epidemiol 15(4):279–285

    Article  Google Scholar 

  • Boffetta P, Couto E, Wichmann J, Ferrari P, Trichopoulos D, Bueno-de-Mesquita HB, van Duijnhoven FJ, Buchner FL, Key T, Boeing H, Nothlings U, Linseisen J, Gonzalez CA, Overvad K, Nielsen MR, Tjonneland A, Olsen A, Clavel-Chapelon F, Boutron-Ruault MC, Morois S, Lagiou P, Naska A, Benetou V, Kaaks R, Rohrmann S, Panico S, Sieri S, Vineis P, Palli D, van Gils CH, Peeters PH, Lund E, Brustad M, Engeset D, Huerta JM, Rodriguez L, Sanchez MJ, Dorronsoro M, Barricarte A, Hallmans G, Johansson I, Manjer J, Sonestedt E, Allen NE, Bingham S, Khaw KT, Slimani N, Jenab M, Mouw T, Norat T, Riboli E, and Trichopoulou A. 2010. Fruit and vegetable intake and overall cancer risk in the European prospective investigation Into Cancer and Nutrition (EPIC). J Natl Cancer Inst

  • Bonner MR, Lee WJ, Sandler DP, Hoppin JA, Dosemeci M, Alavanja MC (2005) Occupational exposure to carbofuran and the incidence of cancer in the Agricultural Health Study. Environ Health Perspect 113(3):285–289

    Article  CAS  Google Scholar 

  • Bonner MR, Coble J, Blair A, Beane Freeman LE, Hoppin JA, Sandler DP, Alavanja MC (2007) Malathion exposure and the incidence of cancer in the agricultural health study. Am J Epidemiol 166(9):1023–1034

    Article  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(2):239–247

    Article  CAS  Google Scholar 

  • Christensen CH, Platz EA, Andreotti G, Blair A, Hoppin JA, Koutros S, Lynch CF, Sandler DP, Alavanja MC (2010) Coumaphos exposure and incident cancer among male participants in the Agricultural Health Study (AHS). Environ Health Perspect 118(1):92–96

    CAS  Google Scholar 

  • Coble J, Arbuckle T, Lee W, Alavanja M, Dosemeci M (2005) The validation of a pesticide exposure algorithm using biological monitoring results. J Occup Environ Hyg 2:194–201

    Article  CAS  Google Scholar 

  • Cogliano VJ, Baan RA, Straif K, Grosse Y, Secretan MB, El GF, Kleihues P (2004) The science and practice of carcinogen identification and evaluation. Environ Health Perspect 112(13):1269–1274

    Article  CAS  Google Scholar 

  • Colditz GA, Cannuscio CC, Frazier AL (1997) Physical activity and reduced risk of colon cancer: implications for prevention. Cancer Causes Control 8(4):649–667

    Article  CAS  Google Scholar 

  • De Roos AJ, Blair A, Rusiecki JA, Hoppin JA, Svec M, Dosemeci M, Sandler DP, Alavanja MC (2005) Cancer incidence among glyphosate-exposed pesticide applicators in the Agricultural Health Study. Environ Health Perspect 113(1):49–54

    Article  Google Scholar 

  • Delancey JO, Alavanja MC, Coble J, Blair A, Hoppin JA, Austin HD, Beane Freeman LE (2009) Occupational exposure to metribuzin and the incidence of cancer in the Agricultural Health Study. Ann Epidemiol 19(6):388–395

    Article  Google Scholar 

  • 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(Suppl 4):140–146

    CAS  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(2):245–260

    Article  CAS  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(4):579–583

    Article  CAS  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(4):279–288

    Article  CAS  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(1):14–21

    Article  CAS  Google Scholar 

  • Goodman SN, Samet JM (2006) Cause and cancer epidemiology. In: Schottenfeld D, Fraumeni J (eds) Cancer epidemiology and prevention, 3rd edn. Oxford University Press, New York

    Google Scholar 

  • Gordis L (2000) Epidemiology. W.B. Saunders, Philadelphia

    Google Scholar 

  • Gray GM, Graham JD (1998) The Agricultural Health Study: Strengths and Limitations. Risk in Perspective: Harvard Center for Risk Analysis 6:1–4

    CAS  Google Scholar 

  • Gray GM, Goldstein BD, Bailar J, Davis DL, Delzell D et al (2000) The Federal Government’s Agricultural Health Study: A Critical Review with Suggested Improvements. Human Ecol Risk Assess 6(1):47–71

    Article  CAS  Google Scholar 

  • Greenburg DL, Rusiecki J, Koutros S, Dosemeci M, Patel R, Hines CJ, Hoppin JA, Alavanja MC (2008) Cancer incidence among pesticide applicators exposed to captan in the Agricultural Health Study. Cancer Causes Control 19(10):1401–1407

    Article  Google Scholar 

  • Hardell L, Eriksson M, Lenner P, Lundgren E (1981) Malignant lymphoma and exposure to chemicals, especially organic solvents, chlorophenols and phenoxy acids: a case-control study. Br J Cancer 43(2):169–176

    Google Scholar 

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

    CAS  Google Scholar 

  • Hoar SK, Blair A, Holmes FF, Boysen C, Robel RJ (1985) Herbicides and colon cancer. Lancet 1(8440):1277–1278

    Article  CAS  Google Scholar 

  • Hou L, Lee WJ, Rusiecki J, Hoppin JA, Blair A, Bonner MR, Lubin JH, Samanic C, Sandler DP, Dosemeci M, Alavanja MC (2006) Pendimethalin exposure and cancer incidence among pesticide applicators. Epidemiology 17(3):302–307

    Article  Google Scholar 

  • Huxley RR, Ansary-Moghaddam A, Clifton P, Czernichow S, Parr CL, Woodward M (2009) The impact of dietary and lifestyle risk factors on risk of colorectal cancer: a quantitative overview of the epidemiological evidence. Int J Cancer 125(1):171–180

    Article  CAS  Google Scholar 

  • Jacobs ET, Thompson PA, Martinez ME (2007) Diet, gender, and colorectal neoplasia. J Clin Gastroenterol 41(8):731–746

    Article  Google Scholar 

  • Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ (2009) Cancer statistics, 2009. CA Cancer J Clin 59(4):225–249

    Article  Google Scholar 

  • Jenab M, Bueno-de-Mesquita HB, Ferrari P, van Duijnhoven FJ, Norat T, Pischon T, Jansen EH, Slimani N, Byrnes G, Rinaldi S, Tjonneland A, Olsen A, Overvad K, Boutron-Ruault MC, Clavel-Chapelon F, Morois S, Kaaks R, Linseisen J, Boeing H, Bergmann MM, Trichopoulou A, Misirli G, Trichopoulos D, Berrino F, Vineis P, Panico S, Palli D, Tumino R, Ros MM, van Gils CH, Peeters PH, Brustad M, Lund E, Tormo MJ, Ardanaz E, Rodriguez L, Sanchez MJ, Dorronsoro M, Gonzalez CA, Hallmans G, Palmqvist R, Roddam A, Key TJ, Khaw KT, Autier P, Hainaut P, Riboli E (2010) Association between pre-diagnostic circulating vitamin D concentration and risk of colorectal cancer in European populations:a nested case-control study. BMJ 340:b5500

    Article  Google Scholar 

  • Johns LE, Houlston RS (2001) A systematic review and meta-analysis of familial colorectal cancer risk. Am J Gastroenterol 96(10):2992–3003

    Article  CAS  Google Scholar 

  • Journal of the American Medical Association (JAMA) (2009) Available from http://jama.ama-assn.org/misc/ifora.dtl#SystematicReviewIncludingMetaanalysis

  • Kang D, Park SK, Beane-Freeman L, Lynch CF, Knott CE, Sandler DP, Hoppin JA, Dosemeci M, Coble J, Lubin J, Blair A, Alavanja M (2008) Cancer incidence among pesticide applicators exposed to trifluralin in the Agricultural Health Study. Environ Res 107(2):271–276

    Article  CAS  Google Scholar 

  • Koutros S, Mahajan R, Zheng T, Hoppin JA, Ma X, Lynch CF, Blair A, Alavanja MC (2008) Dichlorvos exposure and human cancer risk: results from the Agricultural Health Study. Cancer Causes Control 19(1):59–65

    Article  Google Scholar 

  • Koutros S, Lynch CF, Ma X, Lee WJ, Hoppin JA, Christensen CH, Andreotti G, Freeman LB, Rusiecki JA, Hou L, Sandler DP, Alavanja MC (2009) Heterocyclic aromatic amine pesticide use and human cancer risk: results from the US Agricultural Health Study. Int J Cancer 124(5):1206–1212

    Article  CAS  Google Scholar 

  • La VC, Negri E, Decarli A, D’Avanzo B, Gallotti L, Gentile A, Franceschi S (1988) A case-control study of diet and colo-rectal cancer in northern Italy. Int J Cancer 41(4):492–498

    Article  Google Scholar 

  • Lee WJ, Blair A, Hoppin JA, Lubin JH, Rusiecki JA, Sandler DP, Dosemeci M, Alavanja MC (2004a) Cancer incidence among pesticide applicators exposed to chlorpyrifos in the Agricultural Health Study. J Natl Cancer Inst 96(23):1781–1789

    Article  CAS  Google Scholar 

  • Lee WJ, Hoppin JA, Blair A, Lubin JH, Dosemeci M, Sandler DP, Alavanja MC (2004b) Cancer incidence among pesticide applicators exposed to alachlor in the Agricultural Health Study. Am J Epidemiol 159(4):373–380

    Article  Google Scholar 

  • Lee WJ, Sandler DP, Blair A, Samanic C, Cross AJ, Alavanja MC (2007) Pesticide use and colorectal cancer risk in the Agricultural Health Study. Int J Cancer 121(2):339–346

    Article  CAS  Google Scholar 

  • Leet T, Acquavella J, Lynch C, Anne M, Weiss NS, Vaughan T, Checkoway H (1996) Cancer incidence among alachlor manufacturing workers. Am J Ind Med 30(3):300–306

    Article  CAS  Google Scholar 

  • Lynch SM, Rusiecki JA, Blair A, Dosemeci M, Lubin J, Sandler D, Hoppin JA, Lynch CF, Alavanja MC (2006) Cancer incidence among pesticide applicators exposed to cyanazine in the agricultural health study. Environ Health Perspect 114(8):1248–1252

    Article  CAS  Google Scholar 

  • Lynch SM, Mahajan R, Beane Freeman LE, Hoppin JA, Alavanja MC (2009) Cancer incidence among pesticide applicators exposed to butylate in the Agricultural Health Study (AHS). Environ Res 109(7):860–868

    Article  CAS  Google Scholar 

  • MacMahon B, Pugh TF (1970) Epidemiology: principles and methods. Little, Brown and Company, Boston

    Google Scholar 

  • Mahajan R, Blair A, Lynch CF, Schroeder P, Hoppin JA, Sandler DP, Alavanja MC (2006a) Fonofos exposure and cancer incidence in the agricultural health study. Environ Health Perspect 114(12):1838–1842

    CAS  Google Scholar 

  • Mahajan R, Bonner MR, Hoppin JA, Alavanja MC (2006b) Phorate exposure and incidence of cancer in the agricultural health study. Environ. Health Perspect 114(8):1205–1209

    Article  CAS  Google Scholar 

  • Mahajan R, Blair A, Coble J, Lynch CF, Hoppin JA, Sandler DP, Alavanja MC (2007) Carbaryl exposure and incident cancer in the Agricultural Health Study. Int J Cancer 121:1799–1805

    Google Scholar 

  • Mozzachio AM, Rusiecki JA, Hoppin JA, Mahajan R, Patel R, Beane-Freeman L, Alavanja MC (2008) Chlorothalonil exposure and cancer incidence among pesticide applicator participants in the agricultural health study. Environ Res 108(3):400–403

    Article  CAS  Google Scholar 

  • Mulrow CD (1987) The medical review article: state of the science. Ann Intern Med 106(3):485–488

    CAS  Google Scholar 

  • Mulrow CD (1994) Rationale for systematic reviews. BMJ 309(6954):597–599

    Article  CAS  Google Scholar 

  • National Cancer Institute DoCEaG (2004) Agricultural Health Study Aims to Clarify Cancer-Pesticide Association. Available from http://www.dceg.cancer.gov

  • National Library of Medicine (2008) Available from http://www.nlm.nih.gov/nichsr/hta101/ta101014.html

  • Norat T, Riboli E (2002) Fruit and vegetable consumption and risk of cancer of the digestive tract: meta-analysis of published case-control and cohort studies. IARC Sci Publ 156:123–125

    CAS  Google Scholar 

  • Oxman AD (1994) Checklists for review articles. BMJ 309(6955):648–651

    Article  CAS  Google Scholar 

  • Park SK, Kang D, Beane-Freeman L, Blair A, Hoppin JA, Sandler DP, Lynch CF, Knott C, Gwak J, Alavanja M (2009) Cancer incidence among paraquat exposed applicators in the agricultural health study: prospective cohort study. Int J Occup Environ Health 15(3):274–281

    Article  Google Scholar 

  • Poole C, Cullen M, Irons R, Acquavella J (2005) Re: “Cancer incidence among pesticide applicators exposed to alachlor in the agricultural health study”. Am J Epidemiol 161(1):101–102

    Article  Google Scholar 

  • Purdue MP, Hoppin JA, Blair A, Dosemeci M, Alavanja MC (2007) Occupational exposure to organochlorine insecticides and cancer incidence in the Agricultural Health Study. Int J Cancer 120(3):642–649

    Article  CAS  Google Scholar 

  • Ries LAG, Melbert D, Kraphcho M et al (2008) SEER Cancer Statistics Review, 1975–2004; based on November 2006 SEER data submission, posted to the SEER web site, 2007. National Cancer Institute, Bethesda

    Google Scholar 

  • Rothman KJ, Greenland S (1998) Modern epidemiology. Lippincott-Raven, Philadelphia

    Google Scholar 

  • Rothman KJ, Greenland S (2005) Causation and causal inference in epidemiology. Am J Public Health 95(Suppl 1):S144–S150

    Article  Google Scholar 

  • Rothman KJ, Greenland S, Lash TL (2008) Modern epidemiology. Wolters Kluwer Health/Lippincott Williams & Wilkins, Philadelphia

    Google Scholar 

  • Rusiecki JA, De Roos A, Lee WJ, Dosemeci M, Lubin JH, Hoppin JA, Blair A, Alavanja MC (2004) Cancer incidence among pesticide applicators exposed to atrazine in the Agricultural Health Study. J Natl Cancer Inst 96(18):1375–1382

    Article  CAS  Google Scholar 

  • Rusiecki JA, Hou L, Lee WJ, Blair A, Dosemeci M, Lubin JH, Bonner M, Samanic C, Hoppin JA, Sandler DP, Alavanja MC (2006) Cancer incidence among pesticide applicators exposed to metolachlor in the Agricultural Health Study. Int J Cancer 118(12):3118–3123

    Article  CAS  Google Scholar 

  • Rusiecki JA, Patel R, Koutros S, Beane-Freeman L, Landgren O, Bonner MR, Coble J, Lubin J, Blair A, Hoppin JA, Alavanja MC (2009) Cancer incidence among pesticide applicators exposed to permethrin in the Agricultural Health Study. Environ Health Perspect 117(4):581–586

    CAS  Google Scholar 

  • Samanic C, Rusiecki J, Dosemeci M, Hou L, Hoppin JA, Sandler DP, Lubin J, Blair A, Alavanja MC (2006) Cancer incidence among pesticide applicators exposed to dicamba in the agricultural health study. Environ Health Perspect 114(10):1521–1526

    Article  Google Scholar 

  • Swaen GM, de Jong G, Slangen JJ, van Amelsvoort LG (2002) Cancer mortality in workers exposed to dieldrin and aldrin: an update. Toxicol Ind Health 18(2):63–70

    Article  CAS  Google Scholar 

  • Swaen GM, van Amelsvoort LG, Slangen JJ, Mohren DC (2004) Cancer mortality in a cohort of licensed herbicide applicators. Int Arch Occup Environ Health 77(4):293–295

    Article  CAS  Google Scholar 

  • ‘t Mannetje A, McLean D, Cheng S, Boffetta P, Colin D, Pearce N (2005) Mortality in New Zealand workers exposed to phenoxy herbicides and dioxins. Occup Environ Med 62(1):34–40

    Article  Google Scholar 

  • Thomas KW, Dosemeci M, Coble JB, Hoppin JA, Sheldon LS, Chapa G, Croghan CW, Jones PA, Knott CE, Lynch CF, Sandler DP, Blair AE, Alavanja MC (2009) Assessment of a pesticide exposure intensity algorithm in the agricultural health study. J Expo Sci Environ Epidemiol. [Epub ahead of print]

  • 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(3):183–191

    Article  CAS  Google Scholar 

  • United States Preventive Services Task Force (USPSTF) (2008) Procedure manual. Section 4: Evidence Report Development

  • US Environmental Protection Agency (2009) EPA creating framework for human health data in pesticide assessments. Available from http://www.InsideEPA.com

  • van Bemmel DM, Visvanathan K, Beane Freeman LE, Coble J, Hoppin JA, Alavanja MC (2008) S-ethyl-N, N-dipropylthiocarbamate exposure and cancer incidence among male pesticide applicators in the agricultural health study: a prospective cohort. Environ Health Perspect 116(11):1541–1546

    Article  Google Scholar 

  • Weed DL (1995) Causal and preventive inference. In: Greenwald P, Kramer B, Weed DL (eds) Cancer prevention and control. Marcel Dekker, New York, pp 285–302

    Google Scholar 

  • Weed DL (1997) On the use of causal criteria. Int J Epidemiol 26(6):1137–1141

    Article  CAS  Google Scholar 

  • Weed DL (2000) Interpreting epidemiological evidence: how meta-analysis and causal inference methods are related. Int J Epidemiol 29(3):387–390

    Article  CAS  Google Scholar 

  • Weed DL (2005) Weight of evidence: a review of concept and methods. Risk Anal 25(6):1545–1557

    Article  Google Scholar 

  • Weed DL, Gorelic LS (1996) The practice of causal inference in cancer epidemiology. Cancer Epidemiol Biomarkers Prev 5(4):303–311

    CAS  Google Scholar 

  • Weichenthal S, Moase C, Chan P. Weichenthal S, Moase C, Chan P (2010) A Review of Pesticide Exposure and Cancer Incidence in the Agricultural Health Study Cohort. Environ Health Perspect. 2010 May 5. [Epub ahead of print]

  • Wiklund K, Dich J, Holm LE, Eklund G (1989) Risk of cancer in pesticide applicators in Swedish agriculture. Br J Ind Med 46(11):809–814

    CAS  Google Scholar 

  • Willett CG (2001) Cancer of the lower gastrointestinal tract. B.C. Decker, Hamilton

    Google Scholar 

Download references

Conflict of interest

This work was partially supported by Crop Life America (CLA). CLA did not contribute to the design, analysis, or interpretation of the content of this review.

Author information

Authors and Affiliations

  1. Exponent Inc, Health Sciences Practice, 525 W Monroe St., Suite 1050, Chicago, IL, 60661, USA

    Dominik D. Alexander

  2. DLW Consulting Services, LLC, Salt Lake City, UT, USA

    Douglas L. Weed

  3. Emory University, Atlanta, GA, USA

    Pamela J. Mink

  4. New York, NY, USA

    Meghan E. Mitchell

Authors
  1. Dominik D. Alexander
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Douglas L. Weed
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pamela J. Mink
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Meghan E. Mitchell
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dominik D. Alexander.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Alexander, D.D., Weed, D.L., Mink, P.J. et al. A weight-of-evidence review of colorectal cancer in pesticide applicators: the agricultural health study and other epidemiologic studies. Int Arch Occup Environ Health 85, 715–745 (2012). https://doi.org/10.1007/s00420-011-0723-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00420-011-0723-7

Keywords

Search

Navigation