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An algorithm for quantitatively estimating non-occupational pesticide exposure intensity for spouses in the Agricultural Health Study

Abstract

Residents of agricultural areas experience pesticide exposures from sources other than direct agricultural work. We developed a quantitative, active ingredient-specific algorithm for cumulative (adult, married lifetime) non-occupational pesticide exposure intensity for spouses of farmers who applied pesticides in the Agricultural Health Study (AHS). The algorithm addressed three exposure pathways: take-home, agricultural drift, and residential pesticide use. Pathway-specific equations combined (i) weights derived from previous meta-analyses of published pesticide exposure data and (ii) information from the questionnaire on frequency and duration of pesticide use by applicators, home proximity to treated fields, residential pesticide usage (e.g., termite treatments), and spouse’s off-farm employment (proxy for time at home). The residential use equation also incorporated a published probability matrix that documented the likelihood active ingredients were used in home pest treatment products. We illustrate use of these equations by calculating exposure intensities for the insecticide chlorpyrifos and herbicide atrazine for 19,959 spouses. Non-zero estimates for ≥1 pathway were found for 78% and 77% of spouses for chlorpyrifos and atrazine, respectively. Variability in exposed spouses’ intensity estimates was observed for both pesticides, with 75th to 25th percentile ratios ranging from 7.1 to 7.3 for take-home, 6.5 to 8.5 for drift, 2.4 to 2.8 for residential use, and 3.8 to 7.0 for the summed pathways. Take-home and drift estimates were highly correlated (≥0.98), but were not correlated with residential use (0.01‒0.02). This algorithm represents an important advancement in quantifying non-occupational pesticide relative exposure differences and will facilitate improved etiologic analyses in the AHS spouses. The algorithm could be adapted to studies with similar information.

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References

  1. Deziel NC, Friesen MC, Hoppin JA, Hines CJ, Thomas K, Beane Freeman LE. A review of non-occupational pathways for pesticide exposure in women living in agricultural areas. Environ Health Perspect. 2015;123:515–24.

    Article  CAS  Google Scholar 

  2. Blair A, Zahm SH. Methodologic issues in exposure assessment for case-control studies of cancer and herbicides. Am J Ind Med. 1990;18:285–93.

    Article  CAS  Google Scholar 

  3. Hoppin JA, Adgate JL, Eberhart M, Nishioka M, Ryan PB. Environmental exposure assessment of pesticides in farmworker homes. Environ Health Perspect. 2006;114:929–35.

    Article  CAS  Google Scholar 

  4. Carreon T, Butler MA, Ruder AM, Waters MA, Davis-King KE, Calvert GM, et al. Gliomas and farm pesticide exposure in women: the upper midwest health study. Environ Health Perspect. 2005;113:546–51.

    Article  CAS  Google Scholar 

  5. Folsom AR, Zhang S, Sellers TA, Zheng W, Kushi LH, Cerhan JR. Cancer incidence among women living on farms: findings from the Iowa women’s health study. J Occ Env Med. 1996;38:1171–6.

    Article  CAS  Google Scholar 

  6. Aschengrau A, Ozonoff D, Coogan P, Vezina R, Heeren T, Zhang Y. Cancer risk and residential proximity to cranberry cultivation in massachusetts. Am J Public Health. 1996;86:1289–96.

    Article  CAS  Google Scholar 

  7. Glorennec P, Serrano T, Fravallo M, Warembourg C, Monfort C, Cordier S, et al. Determinants of children’s exposure to pyrethroid insecticides in western france. Environ Int. 2017;104:76–82.

    Article  CAS  Google Scholar 

  8. Duell EJ, Millikan RC, Savitz DA, Newman B, Smith JC, Schell MJ, et al. A population-based case-control study of farming and breast cancer in North Carolina. Epidemiology. 2000;11:523–31.

    Article  CAS  Google Scholar 

  9. Cockburn M, Mills P, Zhang X, Zadnick J, Goldberg D, Ritz B. Prostate cancer and ambient pesticide exposure in agriculturally intensive areas in california. Am J Epidemiol. 2011;173:1280–8.

    Article  Google Scholar 

  10. Rull RP and Ritz B. 2003. Historical pesticide exposure in California using pesticide use reports and land-use surveys: an assessment of misclassification error and bias. Send to Environ Health Perspect. 13:1582–9.

    Article  Google Scholar 

  11. Ward MH, Lubin J, Giglierano J, Colt JS, Wolter C, Bekiroglu N, et al. Proximity to crops and residential exposure to agricultural herbicides in Iowa. Environ Health Perspect. 2006;114:893–7.

    Article  CAS  Google Scholar 

  12. Maxwell SK, Airola M, Nuckols JR. Using landsat satellite data to support pesticide exposure assessment in california. Int J Health Geogr. 2010;9:1.

    Article  Google Scholar 

  13. Curwin BD, Hein MJ, Sanderson WT, Striley C, Heederik D, Kromhout H, et al. Urinary pesticide concentrations among children mothers and fathers living in farm and non-farm households in Iowa. Ann Occup Hyg. 2007;511:53–65.

    Google Scholar 

  14. Alexander BH, Burns CJ, Bartels MJ, Acquavella JF, Mandel JS, Gustin C, et al. Chlorpyrifos exposure in farm families: results from the farm family exposure study. J Expo Sci Environ Epidemiol. 2006;16:447–56.

    Article  CAS  Google Scholar 

  15. Alexander BH, Mandel JS, Baker BA, Burns CJ, Bartels MJ, Acquavella JF, et al. Biomonitoring of 2,4-dichlorophenoxyacetic acid exposure and dose in farm families. Environ Health Perspect. 2007;115:370–6.

    Article  CAS  Google Scholar 

  16. Arbuckle TE, Ritter L. Phenoxyacetic acid herbicide exposure for women on Ontario farms. J Toxicol Environ Health A. 2005;68:1359–70.

    Article  CAS  Google Scholar 

  17. Barr DB, Thomas K, Curwin B, Landsittel D, Raymer J, Lu C, et al. Biomonitoring of exposure in farmworker studies. Environ Health Perspect. 2006;114:936–42.

    Article  CAS  Google Scholar 

  18. Dopart PJ and Friesen MC. New opportunities in exposure assessment of occupational epidemiology: use of measurements to aid exposure reconstruction in population-based studies. Curr Environ Health Rep. 2017. 4:355–363. https://doi.org/10.1007/s40572-017-0153-0.

    Article  Google Scholar 

  19. Negatu B, Vermeulen R, Mekonnen Y, Kromhout H. A method for semi-quantitative assessment of exposure to pesticides of applicators and re-entry workers: an application in three farming systems in ethiopia. Ann Occup Hyg. 2016;60:669–83.

    Article  Google Scholar 

  20. Coble J, Thomas KW, Hines CJ, Hoppin JA, Dosemeci M, Curwin B, et al. An updated algorithm for estimation of pesticide exposure intensity in the agricultural health study. Int J Environ Res Public Health. 2011;8:4608–22.

    Article  Google Scholar 

  21. Dosemeci M, Alavanja MC, Rowland AS, Mage D, Zahm SH, Rothman N, et al. A quantitative approach for estimating exposure to pesticides in the agricultural health study. Ann Occ Hyg. 2002;46:245–60.

    CAS  Google Scholar 

  22. Hines CJ, Deddens JA, Jaycox LB, Andrews RN, Striley CA, Alavanja MC. Captan exposure and evaluation of a pesticide exposure algorithm among orchard pesticide applicators in the Agricultural Health Study. Ann Occup Hyg. 2008;52:153–66.

    CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  24. Thomas KW, Dosemeci M, Coble JB, Hoppin JA, Sheldon LS, Chapa G, et al. Assessment of a pesticide exposure intensity algorithm in the agricultural health study. J Expo Sci Environ Epidemiol. 2010;20:559–69.

    Article  CAS  Google Scholar 

  25. Gladen BC, Sandler DP, Zahm SH, Kamel F, Rowland AS, Alavanja MC. Exposure opportunities of families of farmer pesticide applicators. Am J Ind Med. 1998;34:581–7.

    Article  CAS  Google Scholar 

  26. Louis LM, Lerro CC, Friesen MC, Andreotti G, Koutros S, Sandler DP. et al. A prospective study of cancer risk among Agricultural Health Study farm spouses associated with personal use of organochlorine insecticides. Environ Health. 2017;16:95

    Article  Google Scholar 

  27. Alavanja MC, Akland G, Baird D, Blair A, Bond A, Dosemeci M, et al. Cancer and noncancer risk to women in agriculture and pest control: the Agricultural Health Study. J Occ Med. 1994;6:1247–50.

    Article  Google Scholar 

  28. Kirrane EF, Hoppin JA, Umbach DM, Samanic C, Sandler DP. Patterns of pesticide use and their determinants among wives of farmer pesticide applicators in the agricultural health study. J Occ Env Med. 2004;46:856–65.

    Article  CAS  Google Scholar 

  29. Freeman LE, Rusiecki JA, Hoppin JA, Lubin JH, Koutros S, Andreotti G, et al. Atrazine and cancer incidence among pesticide applicators in the Agricultural Health Study (1994-2007). Environ Health Perspect. 2011;119:1253–9.

    Article  CAS  Google Scholar 

  30. Deziel NC, Beane Freeman LE, Graubard BI, Jones RR, Hoppin JA, Thomas K, et al. Relative contributions of agricultural drift, para-occupational, and residential use exposure pathways to house dust pesticide concentrations: meta-regression models of published data. Environ Health Perspect. 2017;125:296–305.

    Article  CAS  Google Scholar 

  31. Deziel NC, Ward MH, Bell EM, Whitehead TP, Gunier RB, Friesen MC, et al. Temporal variability of pesticide concentrations in homes and implications for attenuation bias in epidemiologic studies. Environ Health Perspect. 2013;121:565–71.

    Article  Google Scholar 

  32. Lewis RG, Fortmann RC, Camann DE. Evaluation of methods for monitoring the potential exposure of small children to pesticides in the residential environment. Arch Environ Contam Toxicol. 1994;26:37–46.

    Article  CAS  Google Scholar 

  33. Bureau of Labor Statistics. American time use survey. 2003. http://www.bls.gov/tus/data.htm. Accessed October 2014.

  34. Gunier RB, Ward MH, Airola M, Bell EM, Colt J, Nishioka M, et al. Determinants of agricultural pesticide concentrations in carpet dust. Environ Health Perspect. 2011;119:970–6.

    Article  CAS  Google Scholar 

  35. Harnly ME, Bradman A, Nishioka M, McKone TE, Smith D, McLaughlin R, et al. Pesticides in dust from homes in an agricultural area. Environ Sci Technol. 2009;43:8767–74.

    Article  CAS  Google Scholar 

  36. Deziel NC, Colt JS, Kent EE, Gunier RB, Reynolds P, Booth B, et al. Associations between self-reported pest treatments and pesticide concentrations in carpet dust. Environ Health. 2015;14:27.

    Article  Google Scholar 

  37. Trunnelle KJ, Bennett DH, Tancredi DJ, Gee SJ, Stoecklin-Marois MT, Hennessy-Burt TE, et al. Pyrethroids in house dust from the homes of farm worker families in the micasa study. Environ Int. 2013;61:57–63.

    Article  CAS  Google Scholar 

  38. Colt JS, Cyr MJ, Zahm SH, Tobias GS, Hartge P. Inferring past pesticide exposures: a matrix of individual active ingredients in home and garden pesticides used in past decades. Environ Health Perspect. 2007;115:248–54.

    Article  CAS  Google Scholar 

  39. USEPA (U.S. Environmental Protection Agency). Interim Reregistration Eligibility Decision for Atrazine. Case No. 0062 Decision Documents for Atrazine. 2003. https://archive.epa.gov/pesticides/reregistration/web/pdf/atrazine_combined_docs.pdf.

  40. Lerro CC, Koutros S, Andreotti G, Friesen MC, Alavanja MC, Blair A et al. Organophosphate insecticide use and cancer incidence among spouses of pesticide applicators in the Agricultural Health Study. Occup Environ Med. 2005;72:736–744.

    Article  Google Scholar 

  41. Engel LS, Hill DA, Hoppin JA, Lubin JH, Lynch CF, Pierce J, et al. Pesticide use and breast cancer risk among farmers’ wives in the agricultural health study. Am J Epidemiol 15. 2005;161:121–35.

    Article  Google Scholar 

  42. Engel LS, Werder E, Satagopan J, Blair A, Hoppin JA, Koutros S, et al. Insecticide use and breast cancer risk among farmers’ wives in the Agricultural Health Study. Environ Health Perspect 6. 2017;125:097002.

    Article  Google Scholar 

  43. Bradman A, Eskenazi B, Barr DB, Bravo R, Castorina R, Chevrier J, et al. Organophosphate urinary metabolite levels during pregnancy and after delivery in women living in an agricultural community. Environ Health Perspect. 2005;113:1802–7.

    Article  CAS  Google Scholar 

  44. Butte W, Heinzow B. Pollutants in house dust as indicators of indoor contamination. Rev Env Contam Tox. 2002;175:1–46.

    CAS  Google Scholar 

  45. Simcox NJ, Fenske RA, Wolz SA, Lee IC, Kalman DA. 1995. Pesticides in household dust and soil: exposure pathways for children of agricultural families. Environ Health Perspect 10312:1126–1134.

    Article  CAS  Google Scholar 

  46. Mandel JS, Alexander BH, Baker BA, Acquavella JF, Chapman P, Honeycutt R. Biomonitoring for farm families in the farm family exposure study. Scand J Work Environ Health. 2005;31(Suppl 1):98–104.

    CAS  PubMed  Google Scholar 

  47. Arbuckle TE, Bruce D, Ritter L, Hall JC. Indirect sources of herbicide exposure for families on ontario farms. J Expo Sci Environ Epidemiol. 2006;16:98–104.

    Article  CAS  Google Scholar 

  48. Hofmann JN, Hoppin JA, Lynch CF, Poole JA, Purdue MP, Blair A, et al. Farm characteristics, allergy symptoms, and risk of non-hodgkin lymphoid neoplasms in the agricultural health study. Cancer Epidemiol Biomark Prev. 2015;24:587–94.

    Article  CAS  Google Scholar 

  49. Barouki R, Gluckman PD, Grandjean P, Hanson M, Heindel JJ. Developmental origins of non-communicable disease: implications for research and public health. Environ Health. 2012;11:42.

    Article  Google Scholar 

  50. USDA (U.S. Department of Agriculture). 2007 Census of Agriculture. Document number AC-07-A-51. 2009. http://www.agcensus.usda.gov/Publications/2007/Full_Report/usv1.pdf. Accessed March 2015.

  51. USDA (U.S. Department of Agriculture). Population & migration. 2015. http://www.ers.usda.gov/topics/rural-economy-population/population-migration.aspx. Accessed May 2015.

  52. Adgate JL, Kukowski A, Stroebel C, Shubat PJ, Morrell S, Quackenboss JJ, et al. Pesticide storage and use patterns in minnesota households with children. J Expo Sci Environ Epidemiol. 2000;10:159–67.

    Article  CAS  Google Scholar 

  53. Colt J, Lubin J, Camann D, Davis S, Cerhan J, Severson R. Comparison of pesticide levels in carpet dust and self-reported pest treatment practices in four us sites. J Expo Sci Environ Epidemiol. 2004;14:74–83.

    Article  CAS  Google Scholar 

  54. Wu XM, Bennett DH, Ritz B, Frost J, Cassady D, Lee K, et al. Residential insecticide usage in northern california homes with young children. J Expo Sci Environ Epidemiol. 2011;21:427–36.

    Article  Google Scholar 

  55. Blair A, Thomas K, Coble J, Sandler DP, Hines CH, Lynch CF, et al. Impact of pesticide exposure misclassification on estimates of relative risks in the Agricultural Health Study. J Occ Env Med. 2011;68:537–41.

    Article  CAS  Google Scholar 

  56. Fitzgerald D, Chanasyk DS, Neilson RD, Kiely D, Audette R. Farm well water quality in alberta. Water Qual Res J Can. 2001;36:565–88.

    Article  CAS  Google Scholar 

  57. Friesen MC, Lavoue J, Teschke K, van Tongeren M. Occupational exposure assessment in industry- and population-based epidemiological studies. In: Nieuwenhuijsen M, editor. Exposure Assessment in Environmental Epidemiology. 2nd Edition. New York, NY: Oxford University Press; 2015. p. 139–62.

    Chapter  Google Scholar 

  58. Friesen MC, Park DU, Colt JS, Baris D, Schwenn M, Karagas MR, et al. Developing estimates of frequency and intensity of exposure to three types of metalworking fluids in a population-based case-control study of bladder cancer. Am J Ind Med. 2014;57:915–27.

    Article  Google Scholar 

  59. Goldman L, Eskenazi B, Bradman A, Jewell NP. Risk behaviors for pesticide exposure among pregnant women living in farmworker households in salinas, california. Am J Ind Med. 2004;45:491–9.

    Article  CAS  Google Scholar 

  60. Gunier RB, Nuckols JR, Whitehead TP, Colt JH, Deziel NC, Metayer C, et al. Temporal trends of insecticide concentrations in carpet dust in California from 2001-6. Environ Sci Technol. 2016;50:7761–9.

    Article  CAS  Google Scholar 

  61. Hartge P, Colt JS, Severson RK, Cerhan JR, Cozen W, Camann D, et al. Residential herbicide use and risk of non-hodgkin lymphoma. Cancer Epidemiol Biomark Prev. 2005;14:934–7.

    Article  CAS  Google Scholar 

  62. Jones RR, DellaValle CT, Flory AR, Nordan A, Hoppin JA, Hofmann JN, et al. Accuracy of residential geocoding in the agricultural health study. Int J Health Geogr. 2014;13:37.

    Article  Google Scholar 

  63. Jones RR, Yu CL, Nuckols JR, Cerhan JR, Airola M, Ross JA, et al. Farm residence and lymphohematopoietic cancers in the Iowa women’s health study. Environ Res. 2014;133:353–61.

    Article  CAS  Google Scholar 

  64. McCauley LA, Michaels S, Rothlein J, Muniz J, Lasarev M, Ebbert C. Pesticide exposure and self reported home hygiene: practices in agricultural families. AAOHNJ. 2003;51:113–9.

    Article  Google Scholar 

  65. Peters S, Carey RN, Driscoll TR, Glass DC, Benke G, Reid A, et al. The Australian Work Exposures Study: prevalence of occupational exposure to diesel engine exhaust. Ann Occup Hyg. 2015;59:600–8.

    PubMed  Google Scholar 

  66. Pronk A, Stewart PA, Coble JB, Katki HA, Wheeler DC, Colt JS, et al. Comparison of two expert-based assessments of diesel exhaust exposure in a case-control study: programmable decision rules versus expert review of individual jobs. Occ Env Med. 2012;69:752–8.

    Article  Google Scholar 

  67. Quandt SA, Arcury TA, Rao P, Snively BM, Camann DE, Doran AM, et al. Agricultural and residential pesticides in wipe samples from farmworker family residences in North Carolina and Virginia. Environ Health Perspect. 2004;112:382–7.

    Article  Google Scholar 

  68. Teitelbaum SL, Gammon MD, Britton JA, Neugut AI, Levin B, Stellman SD. Reported residential pesticide use and breast cancer risk on long island, new york. Am J Epidemiol. 2007;165:643–51.

    Article  Google Scholar 

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Acknowledgements

This work was supported by the Intramural Research Program of the National Institutes of Health, National Cancer Institute, Division of Cancer Epidemiology and Genetics (Z01CP010119) and the National Institute of Environmental Health Sciences (Z01-ES049030). NCD was supported, in part, through contract (HHSN261201400231P) and the American Cancer Society grant 127509-MRSG-15-147-01-CNE.

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Correspondence to Nicole C. Deziel.

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For transparency, NCD discloses that her spouse is an employee of the Dow Chemical Company, a producer of hundreds of chemicals and products, including pesticides. The remaining authors declare that they have no conflict of interest.

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Deziel, N.C., Beane Freeman, L.E., Hoppin, J.A. et al. An algorithm for quantitatively estimating non-occupational pesticide exposure intensity for spouses in the Agricultural Health Study. J Expo Sci Environ Epidemiol 29, 344–357 (2019). https://doi.org/10.1038/s41370-018-0088-z

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