Advertisement

Cancer Causes & Control

, Volume 30, Issue 4, pp 311–322 | Cite as

Cancer incidence in the Agricultural Health Study after 20 years of follow-up

  • Catherine C. LerroEmail author
  • Stella Koutros
  • Gabriella Andreotti
  • Dale P. Sandler
  • Charles F. Lynch
  • Lydia M. Louis
  • Aaron Blair
  • Christine G. Parks
  • Srishti Shrestha
  • Jay H. Lubin
  • Paul S. Albert
  • Jonathan N. Hofmann
  • Laura E. Beane Freeman
Original Paper
  • 264 Downloads

Abstract

Purpose

To evaluate cancer incidence in the Agricultural Health Study (AHS), a cohort of private pesticide applicators, their spouses, and commercial applicators, based on 12,420 cancers, adding 5,989 cancers, and 9 years of follow-up since last evaluation.

Methods

We calculated age, year, sex, and race-adjusted standardized incidence ratios (SIR) and 95% confidence intervals (CI) for cancer sites in the AHS relative to the general population.

Results

Overall AHS cancer incidence was lower than the general population (SIRprivate = 0.91, CI 0.89–0.93; SIRspouse = 0.89, CI 0.86–0.92; SIRcommercial = 0.83, CI 0.76–0.92), with notable deficits across applicators and spouses for oral cavity, pancreas, and lung cancers. Cancer excesses included prostate cancer, lip cancer, certain B-cell lymphomas (e.g., multiple myeloma), acute myeloid leukemia (AML), thyroid cancer, testicular cancer, and peritoneal cancer. The lung cancer deficit was strongest among applicators reporting potential exposure to endotoxin at study enrollment (tasks such as raising animals and handling stored grain).

Conclusions

Although an overall deficit in cancer was observed, there were notable exceptions, including newly observed excesses for AML, thyroid, testicular, and peritoneal cancers. Furthermore, endotoxin exposure may, in part, account for observed lung cancer incidence deficits. Cancer incidence patterns in the AHS suggest farm exposures’ relevance to cancer etiology.

Keywords

Farming Cancer Incidence Pesticides Endotoxin 

Notes

Acknowledgments

This work was supported by the Intramural Research Program of the National Institutes of Health, the National Cancer Institute at the National Institutes of Health (Z01-CP010119), and the National Institute of Environmental Health Sciences at the National Institutes of Health (Z01-ES049030). Data in this analysis are based on Agricultural Health Study releases P1REL201701 and AHSREL201706.

Supplementary material

10552_2019_1140_MOESM1_ESM.docx (41 kb)
Supplementary material 1 (DOCX 40 KB)

References

  1. 1.
    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 18:209–215CrossRefGoogle Scholar
  2. 2.
    Acquavella J, Olsen G, Cole P et al (1998) Cancer among farmers: a meta-analysis. Ann Epidemiol 8:64–74CrossRefGoogle Scholar
  3. 3.
    Kirkeleit J, Riise T, Bjorge T, Christiani DC (2013) The healthy worker effect in cancer incidence studies. Am J Epidemiol 177:1218–1224CrossRefGoogle Scholar
  4. 4.
    Alavanja MC, Sandler DP, Lynch CF et al (2005) Cancer incidence in the agricultural health study. Scand J Work Environ Health. 31 Suppl 1: 39–45; discussion 5–7Google Scholar
  5. 5.
    Eriksson M, Hardell L, Carlberg M, Akerman M (2008) Pesticide exposure as risk factor for non-Hodgkin lymphoma including histopathological subgroup analysis. Int J Cancer 123:1657–1663CrossRefGoogle Scholar
  6. 6.
    Fortes C, Mastroeni S, Melchi F et al (2007) The association between residential pesticide use and cutaneous melanoma. Eur J Cancer 43:1066–1075CrossRefGoogle Scholar
  7. 7.
    Koutros S, Alavanja MC, Lubin JH et al (2010) An update of cancer incidence in the Agricultural Health Study. J Occup Environ Med 52:1098–1105CrossRefGoogle Scholar
  8. 8.
    Merhi M, Raynal H, Cahuzac E, Vinson F, Cravedi JP, Gamet-Payrastre L (2007) Occupational exposure to pesticides and risk of hematopoietic cancers: meta-analysis of case-control studies. Cancer Causes Control 18:1209–1226CrossRefGoogle Scholar
  9. 9.
    Samanic CM, De Roos AJ, Stewart PA, Rajaraman P, Waters MA, Inskip PD (2008) Occupational exposure to pesticides and risk of adult brain tumors. Am J Epidemiol 167:976–985CrossRefGoogle Scholar
  10. 10.
    Van Maele-Fabry G, Libotte V, Willems J, Lison D (2006) Review and meta-analysis of risk estimates for prostate cancer in pesticide manufacturing workers. Cancer Causes Control 17:353–373CrossRefGoogle Scholar
  11. 11.
    Nordby KC, Andersen A, Kristensen P (2004) Incidence of lip cancer in the male Norwegian agricultural population. Cancer Causes Control 15:619–626CrossRefGoogle Scholar
  12. 12.
    Lemarchand C, Tual S, Leveque-Morlais N et al (2017) Cancer incidence in the AGRICAN cohort study (2005–2011). Cancer epidemiology. 49: 175–185Google Scholar
  13. 13.
    Blair A, Zahm SH (1995) Agricultural exposures and cancer. Environ Health Perspect 103(Suppl 8):205–208CrossRefGoogle Scholar
  14. 14.
    Ramirez CC, Federman DG, Kirsner RS (2005) Skin cancer as an occupational disease: the effect of ultraviolet and other forms of radiation. Int J Dermatol 44:95–100CrossRefGoogle Scholar
  15. 15.
    Merchant J (1987) Agricultural exposures to organic dusts. Occupational medicine (Philadelphia, Pa.). 2: 409–425Google Scholar
  16. 16.
    Tual S, Silverman DT, Koutros S et al (2016) Use of dieselized farm equipment and incident lung cancer: findings from the agricultural health study cohort. Environ Health Perspect 124:611–618CrossRefGoogle Scholar
  17. 17.
    Koutros S, Beane Freeman LE, Lubin JH et al (2013) Risk of total and aggressive prostate cancer and pesticide use in the agricultural health study. Am J Epidemiol 177:59–74CrossRefGoogle Scholar
  18. 18.
    Alavanja MC, Hofmann JN, Lynch CF et al (2014) Non-hodgkin lymphoma risk and insecticide, fungicide and fumigant use in the agricultural health study. PloS ONE 9:e109332CrossRefGoogle Scholar
  19. 19.
    Freeman LEB, DeRoos AJ, Koutros S et al (2012) Poultry and livestock exposure and cancer risk among farmers in the agricultural health study. Cancer Cause Control 23:663–670CrossRefGoogle Scholar
  20. 20.
    Basinas I, Sigsgaard T, Kromhout H, Heederik D, Wouters IM, Schlunssen V (2015) A comprehensive review of levels and determinants of personal exposure to dust and endotoxin in livestock farming. J Exposure Sci Environ Epidemiol 25:123–137CrossRefGoogle Scholar
  21. 21.
    Alavanja MC, Sandler DP, McMaster SB et al (1996) The Agricultural Health Study. Environ Health Perspect 104:362–369CrossRefGoogle Scholar
  22. 22.
    Fritz AG (2000) International Classification of Diseases for Oncology: ICD-O: World Health OrganizationGoogle Scholar
  23. 23.
    Morton LM, Turner JJ, Cerhan JR et al (2007) Proposed classification of lymphoid neoplasms for epidemiologic research from the Pathology Working Group of the International Lymphoma Epidemiology Consortium (InterLymph). Blood 110:695–708CrossRefGoogle Scholar
  24. 24.
    NAACCR (2016) SEER*Stat Database: NAACCR Incidence Data - CiNA Analytic File, 1995–2014, Public Use (which includes data from CDC’s National Program of Cancer Registries (NPCR), CCCR’s Provincial and Territorial Registries, and the NCI’s Surveillance, Epidemiology and End Results (SEER) Registries), certified by the North American Association of Central Cancer Registries (NAACCR) as meeting high-quality incidence data standards for the specified time periods, submitted December 2016.: NAACCRGoogle Scholar
  25. 25.
    Breslow NE, Lubin JH, Marek P, Langholz B (1983) Multiplicative models and cohort analysis. J Am Stat Assoc 78:1–12CrossRefGoogle Scholar
  26. 26.
    Breslow NE, Day N (1987) Statistical methods in cancer research Vol II-The design and analysis of cohort studiesGoogle Scholar
  27. 27.
    Pierce DA, Preston DL (1993) Joint analysis of site-specific cancer risks for the atomic-bomb survivors. Radiat Res 134:134–142CrossRefGoogle Scholar
  28. 28.
    CDC (1995) Behavioral risk factor surveillance system survey data. Centers for Disease Control and Prevention (CDC), AtlantaGoogle Scholar
  29. 29.
    Lenters V, Basinas I, Beane-Freeman L et al (2010) Endotoxin exposure and lung cancer risk: a systematic review and meta-analysis of the published literature on agriculture and cotton textile workers. Cancer Causes Control 21:523–555CrossRefGoogle Scholar
  30. 30.
    Brucker-Davis F (1998) Effects of environmental synthetic chemicals on thyroid function. Thyroid 8:827–856CrossRefGoogle Scholar
  31. 31.
    Kitahara CM, Linet MS, Beane Freeman LE et al (2012) Cigarette smoking, alcohol intake, and thyroid cancer risk: a pooled analysis of five prospective studies in the United States. Cancer Causes Control 23:1615–1624CrossRefGoogle Scholar
  32. 32.
    Freeman LEB, Rusiecki JA, Hoppin JA et al (2011) Atrazine and cancer incidence among pesticide applicators in the agricultural health study (1994–2007). Environ Health Perspect 119:1253–1259CrossRefGoogle Scholar
  33. 33.
    Lerro CC, Koutros S, Andreotti G et al (2015) Organophosphate insecticide use and cancer incidence among spouses of pesticide applicators in the Agricultural Health Study. Occupational and environmental medicine. 72: 736–744Google Scholar
  34. 34.
    Goldner WS, Sandler DP, Yu F et al (2013) Hypothyroidism and pesticide use among male private pesticide applicators in the agricultural health study. J Occup Environ Med 55:1171–1178CrossRefGoogle Scholar
  35. 35.
    Goldner WS, Sandler DP, Yu F, Hoppin JA, Kamel F, Levan TD (2010) Pesticide use and thyroid disease among women in the Agricultural Health Study. Am J Epidemiol 171:455–464CrossRefGoogle Scholar
  36. 36.
    Shrestha S, Parks CG, Goldner WS et al (2018) Incident thyroid disease in female spouses of private pesticide applicators. Environ Int 118:282–292CrossRefGoogle Scholar
  37. 37.
    Lerro CC, Beane Freeman LE, Della Valle CT et al (2018) Occupational pesticide exposure and subclinical hypothyroidism among male pesticide applicators. Occup Environ Med. 75: 79–89CrossRefGoogle Scholar
  38. 38.
    Fleming LE, Bean JA, Rudolph M, Hamilton K (1999) Cancer incidence in a cohort of licensed pesticide applicators in Florida. J Occup Environ Med 41:279–288CrossRefGoogle Scholar
  39. 39.
    Frost G, Brown T, Harding AH (2011) Mortality and cancer incidence among British agricultural pesticide users. Occupational medicine (Oxford, England). 61: 303–310Google Scholar
  40. 40.
    McGlynn KA, Trabert B (2012) Adolescent and adult risk factors for testicular cancer. Nat Rev Urol 9:339–349CrossRefGoogle Scholar
  41. 41.
    Danzo BJ (1997) Environmental xenobiotics may disrupt normal endocrine function by interfering with the binding of physiological ligands to steroid receptors and binding proteins. Environ Health Perspect 105:294–301CrossRefGoogle Scholar
  42. 42.
    Liu Q, Lin JX, Shi QL, Wu B, Ma HH, Sun GQ (2011) Primary peritoneal serous papillary carcinoma: a clinical and pathological study. Pathol Oncol Res 17:713–719CrossRefGoogle Scholar
  43. 43.
    Liao CI, Chow S, Chen LM, Kapp DS, Mann A, Chan JK (2018) Trends in the incidence of serous fallopian tube, ovarian, and peritoneal cancer in the US. Gynecol Oncol. 149: 318–323Google Scholar
  44. 44.
    Loomis D, Guyton KZ, Grosse Y et al (2017) Carcinogenicity of benzene. Lancet Oncol 18:1574–1575CrossRefGoogle Scholar
  45. 45.
    Greaves MF (1997) Aetiology of acute leukaemia. Lancet 349:344–349CrossRefGoogle Scholar
  46. 46.
    Beane Freeman LE, Blair A, Lubin JH et al (2009) Mortality from lymphohematopoietic malignancies among workers in formaldehyde industries: the National Cancer Institute Cohort. J Natl Cancer Inst 101:751–761CrossRefGoogle Scholar
  47. 47.
    Hauptmann M, Stewart PA, Lubin JH et al (2009) Mortality from lymphohematopoietic malignancies and brain cancer among embalmers exposed to formaldehyde. J Natl Cancer Inst 101:1696–1708CrossRefGoogle Scholar
  48. 48.
    Van Maele-Fabry G, Duhayon S, Lison D (2007) A systematic review of myeloid leukemias and occupational pesticide exposure. Cancer Cause Control 18:457–478CrossRefGoogle Scholar
  49. 49.
    Andreotti G, Koutros S, Hofmann JN et al (2017) Glyphosate use and cancer incidence in the agricultural health study. J Natl Cancer Inst 110:509–516Google Scholar
  50. 50.
    Lerro CC, Andreotti G, Koutros S et al (2018) Alachlor use and cancer incidence in the agricultural health study: an updated analysis. J Natl Cancer InstGoogle Scholar
  51. 51.
    Andreotti G, Freedman ND, Silverman DT et al (2017) Tobacco use and cancer risk in the agricultural health study. Cancer epidemiology, biomarkers & prevention: a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology. 26: 769–778Google Scholar
  52. 52.
    Blomberg M, Nielsen A, Munk C, Kjaer SK (2011) Trends in head and neck cancer incidence in Denmark, 1978–2007: focus on human papillomavirus associated sites. Int J Cancer 129:733–741CrossRefGoogle Scholar
  53. 53.
    Dunne EF, Unger ER, Sternberg M et al (2007) Prevalence of HPV infection among females in the United States. Jama-J Am Med Assoc 297:813–819CrossRefGoogle Scholar
  54. 54.
    Han JJ, Beltran TH, Song JW, Klaric J, Choi YS (2017) Prevalence of genital human papillomavirus infection and human papillomavirus vaccination rates among us adult men: National Health and Nutrition Examination Survey (NHANES) 2013–2014. JAMA Oncol 3:810–816CrossRefGoogle Scholar
  55. 55.
    Tual S, Lemarchand C, Boulanger M et al (2017) Exposure to farm animals and risk of lung cancer in the AGRICAN cohort. Am J Epidemiol 186:463–472CrossRefGoogle Scholar
  56. 56.
    Baron JA, Rohan TE (1996) Tobacco. In: Schottenfeld D, Fraumeni JF Jr (eds) Cancer epidemiology and prevention, 2nd edn. Oxford University Press, New York, pp 269–289Google Scholar
  57. 57.
    Wakelee HA, Chang ET, Gomez SL et al (2007) Lung cancer incidence in never smokers. J Clin Oncol 25:472–478CrossRefGoogle Scholar
  58. 58.
    CDC (2009) Cigarette smoking among adults and trends in smoking cessation - United States, 2008. MMWR. Morbidity and mortality weekly report. 2009/11/17 ed: Centers for Disease Control and Prevention (CDC). pp. 1227–1232Google Scholar

Copyright information

© This is a U.S. government work and its text is not subject to copyright protection in the United States; however, its text may be subject to foreign copyright protection 2019

Authors and Affiliations

  • Catherine C. Lerro
    • 1
    Email author
  • Stella Koutros
    • 1
  • Gabriella Andreotti
    • 1
  • Dale P. Sandler
    • 2
  • Charles F. Lynch
    • 3
  • Lydia M. Louis
    • 1
  • Aaron Blair
    • 1
  • Christine G. Parks
    • 2
  • Srishti Shrestha
    • 2
  • Jay H. Lubin
    • 4
  • Paul S. Albert
    • 4
  • Jonathan N. Hofmann
    • 1
  • Laura E. Beane Freeman
    • 1
  1. 1.Occupational and Environmental Epidemiology Branch, Division of Cancer Epidemiology and GeneticsNational Cancer InstituteRockvilleUSA
  2. 2.National Institute of Environmental Health SciencesResearch Triangle ParkUSA
  3. 3.Department of EpidemiologyUniversity of IowaIowa CityUSA
  4. 4.Biostatistics Branch, Division of Cancer Epidemiology and GeneticsNational Cancer InstituteRockvilleUSA

Personalised recommendations