Journal Mobile Options
Table of Contents
Vol. 116, No. 3, 2006
Issue release date: October 2006
Acta Haematol 2006;116:153–164

Non-Hodgkin Lymphoma and Pesticide Exposure: 25 Years of Research

Dreiher J. · Kordysh E.
Department of Epidemiology and Health Services Evaluation, Faculty of Health Sciences, Ben-Gurion University of the Negev, Beer-Sheva, Israel

Individual Users: Register with Karger Login Information

Please create your User ID & Password

Contact Information

I have read the Karger Terms and Conditions and agree.

To view the fulltext, please log in

To view the pdf, please log in


Over the past 40 years, a substantial rise in the incidence of non-Hodgkin lymphoma (NHL) has been observed. Epidemiologic studies aimed at understanding this rise have revealed some association with occupational exposure. NHL is common among farmers, where pesticides have been described as the culprit. The association between pesticides and NHL has been demonstrated mainly in case-control studies, while retrospective cohorts have been less convincing. Pesticides including chlorphenol and phenoxyacetic acid herbicides, organochlorines, and organophosphate insecticides, carbamates, and fungicides have been associated with NHL. Although the causality has not been clearly proven, both genotoxic and nongenotoxic mechanisms for lymphomagenesis have been proposed. The leveling-off of NHL incidence in certain countries may be the result of a favorable change in pesticide usage patterns. Future studies, such as the Agricultural Health Study, may clarify the uncertainties regarding this issue.

Copyright / Drug Dosage

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher or, in the case of photocopying, direct payment of a specified fee to the Copyright Clearance Center.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in goverment regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.


  1. Bhatia S, Robison LL: Epidemiology of non-Hodgkin’s lymphoma. Curr Opin Hematol 1999;6:201–204.
  2. Ries LAG, Eisner MP, Kosary CL, Hankey BF, Miller BA, Clegg L, Mariotto A, Feuer EJ, Edwards BK (eds): SEER Cancer Statistics Review, 1975–2001. Bethesda, National Cancer Institute, 2004. Available at
  3. Hennessy BT, Hanrahan EO, Daly PA: Non-Hodgkin lymphoma: an update. Lancet Oncol 2004;5:341–353.
  4. Devesa SS, Fears T: Non-Hodgkin’s lymphoma time trends: United States and international data. Cancer Res 1992;52(suppl):5432s–5440s.
  5. Clarke CA, Glaser SL: Changing incidence of non-Hodgkin lymphomas in the United States. Cancer 2002;94:2015–2023.
  6. Vose JM, Chiu BCH, Cheson B, Dancey J, Wright J: Update on epidemiology and therapeutics for non-Hodgkin’s lymphoma. Presented at the American Society of Hematology, Philadelphia, December 6–10, 2002.
  7. Blair A, Zahm SH: Cancer among farmers. Occup Med 1991;6:335–354.
  8. Fleming LE, Bean JA, Rudolph M, Hamilton K: Mortality in a cohort of licensed pesticide applicators in Florida. Occup Environ Med 1999;56:14–21.
  9. Zahm SH: Mortality study of pesticide applicators and other employees of a lawn care service company. J Occup Environ Med 1997;39:1055–1067.
  10. Pearce N, Bethwaite P: Increasing incidence of non-Hodgkin’s lymphoma: occupational and environmental factors. Cancer Res 1992;52(suppl):5496s–5500s.
  11. Zahm SH, Blair A: Pesticides and non-Hodgkin’s lymphoma. Cancer Res 1992;52(suppl): 5485s–5488s.
  12. Hoar SK, Blair A, Holmes FF, Boysen CD, Robel RJ, Hoover R, Fraumeni JF Jr: Agricultural herbicides use and risk of lymphoma and soft-tissue sarcoma. JAMA 1986;256:1141–1147.
  13. Fritschi L, Siemiatycki J: Lymphoma, myeloma and occupation: results of a case-control study. Int J Cancer 1996;67:498–503.
  14. Fleming LE, Bean JA, Rudolph M, Hamilton K: Cancer incidence in a cohort of licensed pesticide applicators in Florida. J Occup Environ Med 1999;41:279–288.
  15. McDuffie HH, Pahwa P, Spinelli JJ, McLaughlin JR, Fincham S, Robson D, Dosman JA, Hu J: Canadian male farm residents, pesticide safety handling practices, exposure to animals and non-Hodgkin’s lymphoma (NHL). Am J Ind Med 2002;(suppl 2):54–61.

    External Resources

  16. Wang Y, Lewis-Michl EL, Hwang SA, Fitzgerald EF, Stark AD: Cancer incidence among a cohort of female farm residents in New York State. Arch Environ Health 2002;57:561–567.
  17. Kato I, Watanabe-Meserve H, Koenig KL, Baptiste MS, Lillquist PP, Frizzera G, Burke JS, Moseson M, Shore RE: Pesticide product use and risk of non-Hodgkin lymphoma in women. Environ Health Perspect 2004;112:1275–1281.
  18. Cantor KP, Blair A, Everett G, Gibson R, Burmeister LF, Brown LM, Schuman L, Dick FR: Pesticides and other agricultural risk factors for non-Hodgkin’s lymphoma among men in Iowa and Minnesota. Cancer Res 1992;52:2447–2455.
  19. Fabbro-Peray P, Daures JP, Rossi JF: Environmental risk factors for non-Hodgkin’s lymphoma: a population-based case-control study in Languedoc-Roussillon, France. Cancer Causes Control 2001;12:201–212.
  20. World Health Organization: Public Health Impact of Pesticides Used in Agriculture. Geneva, WHO, 1990.
  21. Dich J, Zahm SH, Hanberg A, Adami HO: Pesticides and cancer. Cancer Causes Control 1997;8:420–443.
  22. Hillman J: Pesticides; in Harbinson RD (ed): Hamilton and Hardy’s Industrial Toxicology, ed 5. St. Louis, Mosby-Year Book, 1998, pp 411–470.
  23. Hardell L: Malignant lymphoma of histiocytic type and exposure to phenoxyacetic acids or chlorophenols. Lancet 1979;i:55–56.

    External Resources

  24. Acquavella J, Doe J, Tomenson J, Chester G, Cowell J, Bloemen L: Epidemiologic studies of occupational pesticide exposure and cancer: regulatory risk assessments and biologic plausibility. Ann Epidemiol 2003;13:1–7.
  25. Zahm SH, Weisenburger DD, Babbitt PA, Saal RC, Vaught JB, Cantor KP, Blair A: A case-control study of non-Hodgkin’s lymphoma and the herbicide 2,4-dichlorophenoxyacetic acid (2,4-D) in eastern Nebraska. Epidemiology 1990;1:349–356.
  26. Blair A, Cantor KP, Zahm SH: Non-Hodgkin’s lymphoma and agricultural use of the insecticide lindane. Am J Ind Med 1998;33:82–87.
  27. Baris D, Zahm SH, Cantor KP, Blair A: Agricultural use of DDT and risk of non-Hodgkin’s lymphoma: pooled analysis of three case-control studies in the United States. Occup Environ Med 1998;55:522–527.
  28. Waddell BL, Zahm SH, Baris D, Weisenburger DD, Holmes F, Burmeister LF, Cantor KP, Blair A: Agricultural use of organophosphate pesticides and the risk of non-Hodgkin’s lymphoma among male farmers (United States). Cancer Causes Control 2001;12:509–517.
  29. Zheng T, Zahm SH, Cantor KP, Weisenburger DD, Zhang Y, Blair A: Agricultural exposure to carbamate pesticides and risk of non-Hodgkin lymphoma. J Occup Environ Med 2001;43:641–649.
  30. Chiu BCH, Weisenburger DD, Zahm SH, Cantor KP, Gapstur SM, Holmes F, Burmeister LF, Blair A: Agricultural pesticide use, familial cancer and risk of non-Hodgkin lymphoma. Cancer Epidemiol Biomarkers Prev 2004;13:525–531.
  31. Hooiveld M, Heederik DJ, Kogevinas M, Boffetta P, Needham LL, Patterson DG Jr, Bueno-de-Mesquita HB: Second follow-up of a Dutch cohort occupationally exposed to phenoxy herbicides, chlorophenols, and contaminants. Am J Epidemiol 1998;1:891–901.
  32. Hardell L, Eriksson M: A case-control study of non-Hodgkin’s lymphoma and exposure to pesticides. Cancer 1999;85:1353–1360.
  33. Miligi L, Costantini AS, Bolejack V, Veraldi A, Benvenuti A, Nanni O, Ramazzotti V, Tumino R, Stagnaro E, Rodella S, Fontana A, Vindigni C, Vineis P: Non-Hodgkin’s lymphoma, leukemia, and exposures in agriculture: results from the Italian multicenter case-control study. Am J Ind Med 2003;44:627–636.
  34. Waterhouse D, Carman WJ, Schottenfeld D, Gridley G, McLean S: Cancer incidence in the rural community of Tecumseh, Michigan: a pattern of increased lymphopoietic neoplasms. Cancer 1996;77:763–770.
  35. Briggs NC, Levine RS, Hall HI, Cosby O, Brann EA, Hennekens CH: Occupational risk factors for selected cancers among African American and White men in the United States. Am J Public Health 2003;93:1748–1752.
  36. Alavanja MCR, Blair A, Masters MN: Cancer mortality in the US flour industry. J Natl Cancer Inst 1990;82:840–848.
  37. Sperati A, Rapiti E, Settimi L, Quercia A, Terenzoni B, Forastiere F: Mortality among male licensed pesticide users and their wives. Am J Ind Med 1999;36:142–146.
  38. Hardell L, Eriksson M, Lenner P, Lundgren E: Malignant lymphoma and exposure to chemicals, especially organic solvents, chlorophenols and phenoxy acids: a case-control study. Br J Cancer 1981;43:169–176.
  39. Thorn A, Gustavsson P, Sadigh J, Westerlund-Hannestrand B, Hogstedt C: Mortality and cancer incidence among Swedish lumberjacks exposed to phenoxy herbicides.Occup Environ Med 2000;57:718–720.
  40. Woods JS, Polissar L, Severson RK, Heuser LS, Kulander BG: Soft tissue sarcoma and non-Hodgkin’s lymphoma in relation to phenoxyherbicide and chlorinated phenol exposure in western Washington. J Natl Cancer Inst 1987;78:899–910.
  41. 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: Cancer mortality in workers exposed to phenoxy herbicides, chlorophenols, and dioxins. An expanded and updated international cohort study. Am J Epidemiol 1997;145:1061–1075.
  42. McDuffie HH, Pahwa P, McLaughlin JR, Spinelli JJ, Fincham S, Dosman JA, Robson D, Skinnider LF, Choi NW: Non-Hodgkin’s lymphoma and specific pesticide exposures in men: cross-Canada study of pesticides and health. Cancer Epidemiol Biomarkers Prev 2001;10:1155–1163.
  43. Burns CJ, Beard KK, Cartmill JB: Mortality in chemical workers potentially exposed to 2,4-dichlorophenoxyacetic acid (2,4-D) 1945–94: an update.Occup Environ Med 2001;58:24–30.
  44. Frumkin H: Agent Orange and cancer: an overview for clinicians. CA Cancer J Clin 2003;53:245–255.
  45. Hardell L, Eriksson M: Is the decline of the increasing incidence of non-Hodgkin’s lymphoma in Sweden and other countries a result of cancer preventive measures? Environ Health Perspect 2003;111:1704–1706.
  46. Lampi P, Hakulinen T, Luostarinen T, Pukkala E, Teppo L: Cancer incidence following chlorophenol exposure in a community in southern Finland. Arch Environ Health 1992;47:167–175.
  47. Hertzman C, Teschke K, Ostry A, Hershler R, Dimich-Ward H, Kelly S, Spinelli JJ, Gallagher RP, McBride M, Marion SA: Mortality and cancer incidence among sawmill workers exposed to chlorophenate wood preservatives. Am J Public Health 1997;87:71–79.
  48. Rusiecki JA, De Roos A, Lee WJ, Dosemeci M, Lubin JH, Hoppin JA, Blair A, Alavanja MCR: Cancer incidence among pesticide applicator exposed to atrazine in the Agricultural Health Study. J Natl Cancer Inst 2004;96:1375–1382.
  49. De Roos AJ, Zahm SH, Cantor KP, Weisenburger DD, Holmes FF, Burmeister LF, Blair A: Integrative assessment of multiple pesticides as risk factors for non-Hodgkin’s lymphoma among men. Occup Environ Med 2003;60:E11.

    External Resources

  50. De Roos AJ, Blair A, Rusiecki JA, Hoppin JA, Svec M, Dosemeci M, Sandler DP, Alavanja MC: Cancer incidence among glyphosate-exposed pesticide applicators in the Agricultural Health Study. Environ Health Perspect 2005;113:49–54.
  51. Quintana PJE, Delfino RJ, Korrick S, Ziogas A, Kutz FW, Jones EL, Laden F, Garshick E: Adipose tissue levels of organochlorine pesticides and polychlorinated biphenyls and risk of non-Hodgkin’s lymphoma. Environ Health Perspect 2004;112:854–861.
  52. Gladen BC, Sandler DP, Zahm SH, Kamel F, Rowland AS, Alavanja MCR: Exposure opportunities of families of farmer pesticide applicators. Am J Ind Med 1998;34:581–587.
  53. Gianessi J: Agricultural Health Study aims to clarify cancer-pesticide association. DCEG Linkage 2004;20:1–3. Available at
  54. Flower KB, Hoppin JA, Lynch CF, Blair A, Knott C, Shore DL, Sandler DP: Cancer risk and parental pesticide application in children of Agricultural Health Study participants. Environ Health Perspect 2004;112:631–635.
  55. Hardell L, Lindstrom G, Van Bavel B, Hardell K, Linde A, Carlberg M, Liljegren G: Adipose tissue concentrations of dioxins and dibenzofurans, titers of antibodies to Epstein-Barr virus early antigen and the risk for non-Hodgkin lymphoma. Environ Res 2001;87:99–107.
  56. De Roos A, Hartge P, Lubin JH, Colt JS, Davis S, Cerhan JR, Severson RK, Cozen W, Patterson DG Jr, Needham LL, Rothman N: Persistent organochlorine chemicals in plasma and risk of non-Hodgkin’s lymphoma. Cancer Res 2005;65:11214–11226.
  57. Bolognesi C: Genotoxicity of pesticides: a review of human biomonitoring studies. Mutat Res 2003;543:251–272.
  58. Garry VF, Tarone RE, Long L, Griffith J, Kelly JT, Burroughs B: Pesticideappliers with mixed pesticide exposure: G-banded analysis and possible relationship to non-Hodgkin’s lymphoma. Cancer Epidemiol Biomarkers Prev 1996;5:11–16.
  59. Roulland S, Lebailly P, Lecluse Y, Briand M, Pottier D, Gauduchon P: Characterization of the t(14;18) BCL2-IGH translocation in farmers occupationally exposed to pesticides. Cancer Res 2004;64:2264–2269.
  60. Shaham J, Kaufman Z, Gurvich R, Levi Z: Frequency of sister-chromatid exchange among greenhouse farmers exposed to pesticides. Mutat Res 2001;491:71–80.
  61. Rakitsky VN, Koblyakov VA, Turusov V: Nongenotoxic (epigenetic) carcinogens: pesticides as an example. A critical review. Teratog Carcinog Mutagen 2000;20:229–240.
  62. Repetto R, Baliga S: Pesticides and immunosuppression: the risks to public health. Health Policy Plan 1997;12:97–106.
  63. Vine MF, Stein L, Weigle K, Schroeder J, Degnan D, Tse CKJ, Hanchette C, Backer L: Effects on the immune system associated with living near a pesticide dump site. Environ Health Perspect 2000;108:1113–1124.
  64. Hardell L, Eriksson M, Lindstrom G, Van Bavel B, Linde A, Carlberg M, Liljegren G: Case-control study on concentrations of organohalogen compounds and titers of antibodies to Epstein-Barr virus antigens in the etiology of non-Hodgkin lymphoma. Leuk Lymphoma 2001;42:619–629.

Pay-per-View Options
Direct payment This item at the regular price: USD 38.00
Payment from account With a Karger Pay-per-View account (down payment USD 150) you profit from a special rate for this and other single items.
This item at the discounted price: USD 26.50