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

International Archives of Occupational and Environmental Health

Volumn 85, Issue 7, 2012, Pages 715-745

  Alexander, Dominik D ^a   Weed, Douglas L ^b   Mink, Pamela J ^c   Mitchell, Meghan E ^d  

^a EXPONENT INC   (United States)

^b DLW Consulting Services LLC   (United States)

^c EMORY UNIVERSITY   (United States)

^d NONE

Author keywords

Colorectal cancer; Epidemiology; Pesticides; Systematic review; Weight of evidence

Indexed keywords

PESTICIDE;

AGRICULTURE; CHEMICALLY INDUCED DISORDER; COHORT ANALYSIS; COLORECTAL TUMOR; DATA MINING; EPIDEMIOLOGY; FEMALE; HUMAN; MALE; OCCUPATIONAL DISEASE; OCCUPATIONAL EXPOSURE; REVIEW; RISK ASSESSMENT; RISK FACTOR;

AGRICULTURAL WORKERS' DISEASES; AGRICULTURE; COHORT STUDIES; COLORECTAL NEOPLASMS; DATA MINING; EPIDEMIOLOGIC STUDIES; FEMALE; HUMANS; MALE; OCCUPATIONAL EXPOSURE; PESTICIDES; RISK ASSESSMENT; RISK FACTORS;

EID: 84866735356     PISSN: 03400131     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00420-011-0723-7     Document Type: Review

References (96)

1. 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
2. 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
3. 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
4. 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
5. 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
6. 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
7. 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
8. Aschengrau A, Seage GR (2003) Essentials of epidemiology in public health. Jones and Bartlett, Sudbury
9. 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
10. Beaglehole R, Bonita R, Kjellström T (1993) Basic epidemiology. World Health Organization, Geneva
11. 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
12. 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
13. Bhopal RS (2005) Concepts of epidemiology: an integrated introduction to the ideas. Oxford University Press, Oxford
14. Blair A, Zahm SH (1991) Cancer among farmers. Occup Med 6(3):335-354
15. 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
16. 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
17. 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
18. 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
19. Boffetta P, Couto E, Wichmann J, Ferrari P, Trichopoulos D, Buenode-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
20. 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
21. 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
22. 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
23. 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
24. 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
25. 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
26. 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
27. 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
28. 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
29. 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
30. 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
31. 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
32. 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
33. 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
34. 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
35. Gordis L (2000) Epidemiology. W. B. Saunders, Philadelphia
36. Gray GM, Graham JD (1998) The Agricultural Health Study: Strengths and Limitations. Risk in Perspective: Harvard Center for Risk Analysis 6:1-4
37. 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
38. 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
39. 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
40. Hill AB (1965) The environment and disease: association or causation? Proc R Soc Med 58:295-300
41. Hoar SK, Blair A, Holmes FF, Boysen C, Robel RJ (1985) Herbicides and colon cancer. Lancet 1(8440):1277-1278
42. 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
43. 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
44. Jacobs ET, Thompson PA, Martinez ME (2007) Diet, gender, and colorectal neoplasia. J Clin Gastroenterol 41(8):731-746
45. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ (2009) Cancer statistics, 2009. CA Cancer J Clin 59(4):225-249
46. 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 prediagnostic circulating vitamin D concentration and risk of colorectal cancer in European populations: a nested case-control study. BMJ 340:b5500
47. Johns LE, Houlston RS (2001) A systematic review and meta-Analysis of familial colorectal cancer risk. Am J Gastroenterol 96(10):2992-3003
48. Journal of the American Medical Association (JAMA) (2009) Available from http://jama.ama-Assn.org/misc/ifora.dtl#SystematicReviewIncludingMetaanalysis
49. 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
50. 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
51. 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
52. 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
53. 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
54. 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
55. 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
56. 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
57. 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
58. 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
59. MacMahon B, Pugh TF (1970) Epidemiology: principles and methods. Little, Brown and Company, Boston
60. 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
61. 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
62. 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
63. 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
64. Mulrow CD (1987) The medical review article: state of the science. Ann Intern Med 106(3):485-488
65. Mulrow CD (1994) Rationale for systematic reviews. BMJ 309(6954):597-599
66. National Cancer Institute DoCEaG (2004) Agricultural Health Study Aims to Clarify Cancer-Pesticide Association. Available from http://www.dceg.cancer.gov
67. National Library of Medicine (2008) Available from http://www.nlm.nih. gov/nichsr/hta101/ta101014.html
68. Norat T, Riboli E (2002) Fruit and vegetable consumption and risk of cancer of the digestive tract: meta-Analysis of published casecontrol and cohort studies. IARC Sci Publ 156:123-125
69. Oxman AD (1994) Checklists for review articles. BMJ 309(6955):648-651
70. 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
71. 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
72. 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
73. Ries L A G, 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
74. Rothman KJ, Greenland S (1998) Modern epidemiology. Lippincott-Raven, Philadelphia
75. Rothman KJ, Greenland S (2005) Causation and causal inference in epidemiology. Am J Public Health 95(Suppl 1):S144-S150
76. Rothman KJ, Greenland S, Lash TL (2008) Modern epidemiology. Wolters Kluwer Health/Lippincott Williams & Wilkins, Philadelphia
77. 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
78. 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
79. 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
80. 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
81. 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
82. 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
83. '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
84. 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]
85. 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
86. United States Preventive Services Task Force (USPSTF) (2008) Procedure manual. Section 4: Evidence Report Development
87. US Environmental Protection Agency (2009) EPA creating framework for human health data in pesticide assessments. Available from http://www.InsideEPA. com
88. 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
89. 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
90. Weed DL (1997) On the use of causal criteria. Int J Epidemiol 26(6):1137-1141
91. Weed DL (2000) Interpreting epidemiological evidence: how metaanalysis and causal inference methods are related. Int J Epidemiol 29(3):387-390
92. Weed DL (2005) Weight of evidence: a review of concept and methods. Risk Anal 25(6):1545-1557
93. Weed DL, Gorelic LS (1996) The practice of causal inference in cancer epidemiology. Cancer Epidemiol Biomarkers Prev 5(4):303-311
94. 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]
95. 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
96. Willett CG (2001) Cancer of the lower gastrointestinal tract. B. C. Decker, Hamilton