Pesticide exposure as risk factor for non-Hodgkin lymphoma including histopathological subgroup analysis
Corresponding Author
Mikael Eriksson
Department of Oncology, University Hospital, Lund, Sweden
Department of Oncology, University Hospital, SE-221 85 Lund, SwedenSearch for more papers by this authorLennart Hardell
Department of Oncology, University Hospital, Örebro, Sweden
Search for more papers by this authorMichael Carlberg
Department of Oncology, University Hospital, Örebro, Sweden
Search for more papers by this authorMåns Åkerman
Department of Pathology, University Hospital, Lund, Sweden
Search for more papers by this authorCorresponding Author
Mikael Eriksson
Department of Oncology, University Hospital, Lund, Sweden
Department of Oncology, University Hospital, SE-221 85 Lund, SwedenSearch for more papers by this authorLennart Hardell
Department of Oncology, University Hospital, Örebro, Sweden
Search for more papers by this authorMichael Carlberg
Department of Oncology, University Hospital, Örebro, Sweden
Search for more papers by this authorMåns Åkerman
Department of Pathology, University Hospital, Lund, Sweden
Search for more papers by this authorAbstract
We report a population based case–control study of exposure to pesticides as risk factor for non-Hodgkin lymphoma (NHL). Male and female subjects aged 18–74 years living in Sweden were included during December 1, 1999, to April 30, 2002. Controls were selected from the national population registry. Exposure to different agents was assessed by questionnaire. In total 910 (91 %) cases and 1016 (92%) controls participated. Exposure to herbicides gave odds ratio (OR) 1.72, 95% confidence interval (CI) 1.18–2.51. Regarding phenoxyacetic acids highest risk was calculated for MCPA; OR 2.81, 95% CI 1.27–6.22, all these cases had a latency period >10 years. Exposure to glyphosate gave OR 2.02, 95% CI 1.10–3.71 and with >10 years latency period OR 2.26, 95% CI 1.16–4.40. Insecticides overall gave OR 1.28, 95% CI 0.96–1.72 and impregnating agents OR 1.57, 95% CI 1.07–2.30. Results are also presented for different entities of NHL. In conclusion our study confirmed an association between exposure to phenoxyacetic acids and NHL and the association with glyphosate was considerably strengthened. © 2008 Wiley-Liss, Inc.
References
- 1 Jaffe ES,Harris NL,Stein H,Vardiman JW. World Health Organization classification of tumours. Pathology and genetics. Tumours of haematopoetic and lymphoid tissues. Lyon: IARC Press, 2001.
- 2 Hardell L,Eriksson M. Is the decline of the increasing incidence of non-Hodgkin lymphoma in Sweden and other countries a result of cancer preventive measures? Environ Health Perspect 2003; 111: 1704–6.
- 3 Hardell L,Axelson O. Environmental and occupational aspects on the etiology of non-Hodgkin's lymphoma. Oncol Res 1998; 10: 1–5.
- 4 Pluda JM,Venzon DJ,Tosato G,Lietzau J,Wyvill K,Nelson DL,Jaffe ES,Karp JE,Broder S,Yarchoan R. Parameters affecting the development of non-Hodgkin's lymphoma in patients with severe human immunodeficiency virus infection receiving antiretroviral therapy. J Clin Oncol 1993; 11: 1099–107.
- 5 Patton DF,Wilkowski CW,Hanson CA,Shapiro R,Gajl-Peczalska KJ,Filipovich AH,McClain KL. Epstein-Barr virus–determined clonality in posttransplant lymphoproliferative disease. Transplantation 1990; 49: 1080–4.
- 6 Lehtinen T,Lumio J,Dillner J,Hakama M,Knekt P,Lehtinen M,Teppo L,Leinikki P. Increased risk of malignant lymphoma indicated by elevated Epstein-Barr virus antibodies—a prospective study. Cancer Causes Control 1993; 4: 187–93.
- 7 Potter M. Pathogenetic mechanisms in B-cell non-Hodgkin's lymphomas in humans. Cancer Res 1992; 52: 5522S–5528S.
- 8 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: 169–76.
- 9 Hardell L. Malignant lymphoma of histiocytic type and exposure to phenoxyacetic acids or chlorophenols. Lancet 1979; 1: 55–6.
- 10 International Agency for Research on Cancer. Polychlorinated dibenzo-para-dioxins. IARC Monogr Eval Carcinog Risks Hum 1997; 69: 333–343.
- 11 Vos JG,Moore JA,Zinkl JG. Effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin on the immune system of laboratory animals. Environ Health Perspect 1973; 5: 149–62.
- 12 Exon JH,Talcott PA,Koller LD. Effect of lead, polychlorinated biphenyls, and cyclophosphamide on rat natural killer cells, interleukin 2, and antibody synthesis. Fundam Appl Toxicol 1985; 5: 158–64.
- 13 Lu YC,Wu YC. Clinical findings and immunological abnormalities in Yu-Cheng patients. Environ Health Perspect 1985; 59: 17–29.
- 14 Kerkvliet NI,Brauner JA. Mechanisms of 1,2,3,4,6,7,8-heptachlorodibenzo-p-dioxin (HpCDD)-induced humoral immune suppression: evidence of primary defect in T-cell regulation. Toxicol Appl Pharmacol 1987; 87: 18–31.
- 15 Faustini A,Settimi L,Pacifici R,Fano V,Zuccaro P,Forastiere F. Immunological changes among farmers exposed to phenoxy herbicides: preliminary observations. Occup Environ Med 1996; 53: 583–5.
- 16 Hoar SK,Blair A,Holmes FF,Boysen CD,Robel RJ,Hoover R,Fraumeni JF,Jr. Agricultural herbicide use and risk of lymphoma and soft-tissue sarcoma. JAMA 1986; 256: 1141–7.
- 17 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: 349–56.
- 18
Hardell L,Eriksson M.
A case-control study of non-Hodgkin lymphoma and exposure to pesticides.
Cancer
1999;
85:
1353–60.
10.1002/(SICI)1097-0142(19990315)85:6<1353::AID-CNCR19>3.0.CO;2-1 CAS PubMed Web of Science® Google Scholar
- 19 Hardell L,Eriksson M,Degerman A. Exposure to phenoxyacetic acids, chlorophenols, or organic solvents in relation to histopathology, stage, and anatomical localization of non-Hodgkin's lymphoma. Cancer Res 1994; 54: 2386–9.
- 20
Hardell L,Eriksson M,Axelson O,Flesch-Janys D.
Epidemiological studies on cancer and exposure to dioxins and related compounds. In:
A Schecter, T Gasiewicz, eds.
Dioxins and health.
Hoboken, NJ:
John Wiley & Sons,
2003. p
729–64.
10.1002/0471722014.ch18 Google Scholar
- 21 Miligi L,Costantini AS,Veraldi A,Benvenuti A,Vineis P. Cancer and pesticides: an overview and some results of the Italian multicenter case-control study on hematolymphopoietic malignancies. Ann N Y Acad Sci 2006; 1076: 366–77.
- 22 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: 509–17.
- 23 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: 641–9.
- 24 Purdue MP,Hoppin JA,Blair A,Dosemeci M,Alavanja MC. Occupational exposure to organochlorine insecticides and cancer incidence in the agricultural health study. Int J Cancer 2007; 120: 642–9.
- 25 Colt JS,Davis S,Severson RK,Lynch CF,Cozen W,Camann D,Engels EA,Blair A,Hartge P. Residential insecticide use and risk of non-Hodgkin's lymphoma. Cancer Epidemiol Biomarkers Prev 2006; 15: 251–7.
- 26 Rusiecki JA,De Roos A,Lee WJ,Dosemeci M,Lubin JH,Hoppin JA,Blair A,Alavanja MC. Cancer incidence among pesticide applicators exposed to atrazine in the Agricultural Health Study. J Natl Cancer Inst 2004; 96: 1375–82.
- 27 Fritschi L,Benke G,Hughes AM,Kricker A,Turner J,Vajdic CM,Grulich A,Milliken S,Kaldor J,Armstrong BK. Occupational exposure to pesticides and risk of non-Hodgkin's lymphoma. Am J Epidemiol 2005; 162: 849–57.
- 28 van Balen E,Font R,Cavalle N,Font L,Garcia-Villanueva M,Benavente Y,Brennan P,de Sanjose S. Exposure to non-arsenic pesticides is associated with lymphoma among farmers in Spain. Occup Environ Med 2006; 63: 663–8.
- 29 Steinrucken HC,Amrhein N. The herbicide glyphosate is a potent inhibitor of 5-enolpyruvyl-shikimic acid-3-phosphate synthase. Biochem Biophys Res Commun 1980; 94: 1207–12.
- 30 US EPA. U.S. Environmental Protection Agency Registration Eligibility Decision (RED) Glyphosate. EPA-R-93-014. Washington DC: US Environmental Protection Agency, 1993.
- 31 World Health Organization. International programme on chemical safety. Glyphosate. Environmental health criteria 159. Geneva: WHO, 1994.
- 32 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.
- 33 Bolognesi C,Bonatti S,Degan P,Gallerani E,Peluso M,Rabboni R,Roggieri P,Abbondandolo A. Genotoxic activity of glyphosate and its technical formulation Roundup. J Agric Food Chem 1997; 45: 1957–62.
- 34 Lioi MB,Scarfi MR,Santoro A,Barbieri R,Zeni O,Di Berardino D,Ursini MV. Genotoxicity and oxidative stress induced by pesticide exposure in bovine lymphocyte cultures in vitro. Mutat Res 1998; 403: 13–20.
- 35 Lioi MB,Scarfi MR,Santoro A,Barbieri R,Zeni O,Salvemini F,Di Berardino D,Ursini MV. Cytogenetic damage and induction of pro-oxidant state in human lymphocytes exposed in vitro to gliphosate, vinclozolin, atrazine, and DPX-E9636. Environ Mol Mutagen 1998; 32: 39–46.
- 36 Hardell L,Eriksson M,Nordstrom M. Exposure to pesticides as risk factor for non-Hodgkin's lymphoma and hairy cell leukemia: pooled analysis of two Swedish case-control studies. Leuk Lymphoma 2002; 43: 1043–9.
- 37 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: 1155–63.
- 38 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.
- 39 Tatham L,Tolbert P,Kjeldsberg C. Occupational risk factors for subgroups of non-Hodgkin's lymphoma. Epidemiology 1997; 8: 551–8.
- 40 Rothman N,Cantor KP,Blair A,Bush D,Brock JW,Helzlsouer K,Zahm SH,Needham LL,Pearson GR,Hoover RN,Comstock GW,Strickland PT. A nested case-control study of non-Hodgkin lymphoma and serum organochlorine residues. Lancet 1997; 350: 240–4.
- 41 Persson B,Dahlander AM,Fredriksson M,Brage HN,Ohlson CG,Axelson O. Malignant lymphomas and occupational exposures. Br J Ind Med 1989; 46: 516–20.