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Published in: BMC Public Health 1/2011

Open Access 01-12-2011 | Research article

Pesticide exposure and lymphohaematopoietic cancers: a case-control study in an agricultural region (Larissa, Thessaly, Greece)

Authors: Maria Kokouva, Nikolaos Bitsolas, Georgios M Hadjigeorgiou, George Rachiotis, Nikolaos Papadoulis, Christos Hadjichristodoulou

Published in: BMC Public Health | Issue 1/2011

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Abstract

Background

The causality of lymphohaematopoietic cancers (LHC) is multifactorial and studies investigating the association between chemical exposure and LHC have produced variable results. The aim of this study was to investigate the relationships between exposure to pesticides and LHC in an agricultural region of Greece.

Methods

A structured questionnaire was employed in a hospital-based case control study to gather information on demographics, occupation, exposure to pesticides, agricultural practices, family and medical history and smoking. To control for confounders, backward conditional and multinomial logistic regression analyses were used. To assess the dose-response relationship between exposure and disease, the chi-square test for trend was used.

Results

Three hundred and fifty-four (354) histologically confirmed LHC cases diagnosed from 2004 to 2006 and 455 sex- and age-matched controls were included in the study. Pesticide exposure was associated with total LHC cases (OR 1.46, 95% CI 1.05-2.04), myelodysplastic syndrome (MDS) (OR 1.87, 95% CI 1.00-3.51) and leukaemia (OR 2.14, 95% CI 1.09-4.20). A dose-response pattern was observed for total LHC cases (P = 0.004), MDS (P = 0.024) and leukaemia (P = 0.002). Pesticide exposure was independently associated with total LHC cases (OR 1.41, 95% CI 1.00 - 2.00) and leukaemia (OR 2.05, 95% CI 1.02-4.12) after controlling for age, smoking and family history (cancers, LHC and immunological disorders). Smoking during application of pesticides was strongly associated with total LHC cases (OR 3.29, 95% CI 1.81-5.98), MDS (OR 3.67, 95% CI 1.18-12.11), leukaemia (OR 10.15, 95% CI 2.15-65.69) and lymphoma (OR 2.72, 95% CI 1.02-8.00). This association was even stronger for total LHC cases (OR 18.18, 95% CI 2.38-381.17) when eating simultaneously with pesticide application.

Conclusions

Lymphohaematopoietic cancers were associated with pesticide exposure after controlling for confounders. Smoking and eating during pesticide application were identified as modifying factors increasing the risk for LHC. The poor pesticide work practices identified during this study underline the need for educational campaigns for farmers.
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Literature
1.
go back to reference Grulich AE, Vajdic CM: The epidemiology of non-Hodgkin lymphoma. Pathology. 2005, 37 (Suppl 6): 409-19. 10.1080/00313020500370192.CrossRefPubMed Grulich AE, Vajdic CM: The epidemiology of non-Hodgkin lymphoma. Pathology. 2005, 37 (Suppl 6): 409-19. 10.1080/00313020500370192.CrossRefPubMed
2.
go back to reference Storm SS, Gu Y, Gruschkus SK, Pierce SA, Estey EH: Risk factors of myelodysplastic syndromes: a case-control study. Leukemia. 2005, 19 (Suppl 11): 1912-8. 10.1038/sj.leu.2403945.CrossRef Storm SS, Gu Y, Gruschkus SK, Pierce SA, Estey EH: Risk factors of myelodysplastic syndromes: a case-control study. Leukemia. 2005, 19 (Suppl 11): 1912-8. 10.1038/sj.leu.2403945.CrossRef
3.
go back to reference Descatha A, Jenabian A, Conso F, Ameille J: Occupational exposures and haematological malignancies: overview on human recent data. Cancer Causes Control. 2005, 16 (Suppl 8): 939-53. 10.1007/s10552-005-2301-3.CrossRefPubMed Descatha A, Jenabian A, Conso F, Ameille J: Occupational exposures and haematological malignancies: overview on human recent data. Cancer Causes Control. 2005, 16 (Suppl 8): 939-53. 10.1007/s10552-005-2301-3.CrossRefPubMed
4.
go back to reference Mester B, Nieters A, Deeg E, Elsner G, Becker N, Seidler A: Occupation and malignant lymphoma: a population based case control study in Germany. Occup Environ Med. 2006, 63: 17-26. 10.1136/oem.2005.020453.CrossRefPubMedPubMedCentral Mester B, Nieters A, Deeg E, Elsner G, Becker N, Seidler A: Occupation and malignant lymphoma: a population based case control study in Germany. Occup Environ Med. 2006, 63: 17-26. 10.1136/oem.2005.020453.CrossRefPubMedPubMedCentral
5.
go back to reference Merhi M, Raynal H, Cahuzac E, Vinson F, Cravedi JP, Gamet-Payrastre L: Occupational exposure to pesticides and risk of hematopoietic cancers: meta-analysis of case-control studies. Cancer Causes Control. 2007, 18 (Suppl 10): 1209-26. 10.1007/s10552-007-9061-1.CrossRefPubMed Merhi M, Raynal H, Cahuzac E, Vinson F, Cravedi JP, Gamet-Payrastre L: Occupational exposure to pesticides and risk of hematopoietic cancers: meta-analysis of case-control studies. Cancer Causes Control. 2007, 18 (Suppl 10): 1209-26. 10.1007/s10552-007-9061-1.CrossRefPubMed
6.
go back to reference Van Maele-Fabry G, Duhayon S, Lison D: A systematic review of myeloid leukemias and occupational pesticide exposure. Cancer Causes Control. 2007, 18 (Suppl 5): 457-78. 10.1007/s10552-007-0122-2.CrossRefPubMed Van Maele-Fabry G, Duhayon S, Lison D: A systematic review of myeloid leukemias and occupational pesticide exposure. Cancer Causes Control. 2007, 18 (Suppl 5): 457-78. 10.1007/s10552-007-0122-2.CrossRefPubMed
7.
go back to reference Lope V, Perez-Gomez B, Aragones N, Lopez-Abente G, Gustavsson P, Plato N, Zock JP, Pollan M: Occupation, exposure to chemicals, sensitizing agents, and risk of multiple myeloma in Sweden. Cancer Epidemiol Biomarkers Prev. 2008, 17 (Suppl 11): 3123-7. 10.1158/1055-9965.EPI-08-0343.CrossRefPubMed Lope V, Perez-Gomez B, Aragones N, Lopez-Abente G, Gustavsson P, Plato N, Zock JP, Pollan M: Occupation, exposure to chemicals, sensitizing agents, and risk of multiple myeloma in Sweden. Cancer Epidemiol Biomarkers Prev. 2008, 17 (Suppl 11): 3123-7. 10.1158/1055-9965.EPI-08-0343.CrossRefPubMed
8.
go back to reference Svec MA, Ward MH, Dosemeci M, Checkoway H, De Roos AJ: Risk of lymphatic or haematopoietic cancer mortality with occupational exposure to animals or the public. Occup Environ Med. 2005, 62: 726-35. 10.1136/oem.2005.021550.CrossRefPubMedPubMedCentral Svec MA, Ward MH, Dosemeci M, Checkoway H, De Roos AJ: Risk of lymphatic or haematopoietic cancer mortality with occupational exposure to animals or the public. Occup Environ Med. 2005, 62: 726-35. 10.1136/oem.2005.021550.CrossRefPubMedPubMedCentral
9.
go back to reference Baris D, Silverman DT, Brown LM, Swanson GM, Hayes RB, Schwartz AG, Liff JM, Schoenberg JB, Pottern LM, Greenberg RS, Stewart PA: Occupation, pesticide exposure and risk of multiple myeloma. Scand J Work Environ Health. 2004, 30 (Suppl 3): 215-22.CrossRefPubMed Baris D, Silverman DT, Brown LM, Swanson GM, Hayes RB, Schwartz AG, Liff JM, Schoenberg JB, Pottern LM, Greenberg RS, Stewart PA: Occupation, pesticide exposure and risk of multiple myeloma. Scand J Work Environ Health. 2004, 30 (Suppl 3): 215-22.CrossRefPubMed
10.
go back to reference Fritschi L, Johnson KC, Kliewer EV, Fry R, Canadian Cancer Registries Epidemiology Research Group: Animal-related occupations and the risk of leukemia, myeloma, and non-Hodgkin's lymphoma in Canada. Cancer Causes Control. 2002, 13 (Suppl 6): 563-71. 10.1023/A:1016331128897.CrossRefPubMed Fritschi L, Johnson KC, Kliewer EV, Fry R, Canadian Cancer Registries Epidemiology Research Group: Animal-related occupations and the risk of leukemia, myeloma, and non-Hodgkin's lymphoma in Canada. Cancer Causes Control. 2002, 13 (Suppl 6): 563-71. 10.1023/A:1016331128897.CrossRefPubMed
11.
go back to reference Seidler A, Mohner M, Berger J, Mester B, Deeg E, Elsner G, Nieters A, Becker N: Solvent exposure and malignant lymphoma: a population-based case-control study in Germany. J Occup Med Toxicol. 2007, 2: 2-10.1186/1745-6673-2-2.CrossRefPubMedPubMedCentral Seidler A, Mohner M, Berger J, Mester B, Deeg E, Elsner G, Nieters A, Becker N: Solvent exposure and malignant lymphoma: a population-based case-control study in Germany. J Occup Med Toxicol. 2007, 2: 2-10.1186/1745-6673-2-2.CrossRefPubMedPubMedCentral
12.
go back to reference Chiu BC, Dave BJ, Blair A, Gapstur SM, Zahm SH, Weisenburger DD: Agricultural pesticide use and risk of t(14;18)-defined subtypes of non-Hodgkin lymphoma. Blood. 2006, 108 (Suppl 4): 1363-9. 10.1182/blood-2005-12-008755.CrossRefPubMedPubMedCentral Chiu BC, Dave BJ, Blair A, Gapstur SM, Zahm SH, Weisenburger DD: Agricultural pesticide use and risk of t(14;18)-defined subtypes of non-Hodgkin lymphoma. Blood. 2006, 108 (Suppl 4): 1363-9. 10.1182/blood-2005-12-008755.CrossRefPubMedPubMedCentral
13.
go back to reference 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: 2264-69. 10.1158/0008-5472.CAN-03-3604.CrossRefPubMed 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: 2264-69. 10.1158/0008-5472.CAN-03-3604.CrossRefPubMed
14.
go back to reference Agopian J, Navarro JM, Gac AC, Lecluse Y, Briand M, Grenot P, Gauduchon P, Ruminy P, Lebailly P, Nadel B, Roulland S: Agricultural pesticide exposure and the molecular connection to lymphomagenesis. J Exp Med. 2009, 206 (Suppl 7): 1473-83. 10.1084/jem.20082842.CrossRefPubMedPubMedCentral Agopian J, Navarro JM, Gac AC, Lecluse Y, Briand M, Grenot P, Gauduchon P, Ruminy P, Lebailly P, Nadel B, Roulland S: Agricultural pesticide exposure and the molecular connection to lymphomagenesis. J Exp Med. 2009, 206 (Suppl 7): 1473-83. 10.1084/jem.20082842.CrossRefPubMedPubMedCentral
15.
go back to reference Kato I, Watanabe-Meserve H, Koerg 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 (Suppl 13): 1275-81. 10.1289/ehp.7070.CrossRefPubMedPubMedCentral Kato I, Watanabe-Meserve H, Koerg 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 (Suppl 13): 1275-81. 10.1289/ehp.7070.CrossRefPubMedPubMedCentral
16.
go back to reference 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 exposure in men: cross-Canada study of pesticide and health. Cancer Epidemiol Biomarkers Prev. 2001, 10: 1155-63.PubMed 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 exposure in men: cross-Canada study of pesticide and health. Cancer Epidemiol Biomarkers Prev. 2001, 10: 1155-63.PubMed
17.
go back to reference Mills PK, Yang R, Riordan D: Lymphohematopoietic cancers in the United Farm Workers of America (UFW), 1988-2001. Cancer Causes Control. 2005, 16 (Suppl 7): 823-30. 10.1007/s10552-005-2703-2.CrossRefPubMed Mills PK, Yang R, Riordan D: Lymphohematopoietic cancers in the United Farm Workers of America (UFW), 1988-2001. Cancer Causes Control. 2005, 16 (Suppl 7): 823-30. 10.1007/s10552-005-2703-2.CrossRefPubMed
18.
go back to reference Van Balen E, Font R, Cavalle' N, Font L, Garcia-Villanueva M, Benavente Y, Brennar P, De Sanjose S: Exposure to non-arsenic pesticides is associated with lymphoma among farmers in Spain. Occup Environ Med. 2006, 63: 663-8. 10.1136/oem.2005.024026.CrossRefPubMedPubMedCentral Van Balen E, Font R, Cavalle' N, Font L, Garcia-Villanueva M, Benavente Y, Brennar P, De Sanjose S: Exposure to non-arsenic pesticides is associated with lymphoma among farmers in Spain. Occup Environ Med. 2006, 63: 663-8. 10.1136/oem.2005.024026.CrossRefPubMedPubMedCentral
19.
go back to reference Orsi L, Delabre L, Monnereau A, Delval P, Berthou C, Fenaux P, Marit G, Soubeyran P, Huguet F, Milpied N, Leporrier M, Hemon D, Troussard X, Clevel J: Occupational exposure to pesticides and lymphoid neoplasms among men: results of a French case-control study. Occup Environ Med. 2009, 66 (Suppl 5): 291-298. 10.1136/oem.2008.040972.CrossRefPubMed Orsi L, Delabre L, Monnereau A, Delval P, Berthou C, Fenaux P, Marit G, Soubeyran P, Huguet F, Milpied N, Leporrier M, Hemon D, Troussard X, Clevel J: Occupational exposure to pesticides and lymphoid neoplasms among men: results of a French case-control study. Occup Environ Med. 2009, 66 (Suppl 5): 291-298. 10.1136/oem.2008.040972.CrossRefPubMed
21.
go back to reference Centers for Disease Control and Prevention-CDC: CDC-NCHS-National Center for Health Statistics "Data definitions" Current smoker, Alcohol consumption. Atlanta USA. [updated 2002 June; accessed 2003 May]. Not available anymore in the form used, [http://www.cdc.gov] Centers for Disease Control and Prevention-CDC: CDC-NCHS-National Center for Health Statistics "Data definitions" Current smoker, Alcohol consumption. Atlanta USA. [updated 2002 June; accessed 2003 May]. Not available anymore in the form used, [http://​www.​cdc.​gov]
23.
go back to reference Norusis M: Multinomial logistic regression analysis. SPSS 16.0 Advanced Statistical Procedures. Edited by: Norusis M. 2007, Companion Upper Saddle-River, N.J: Prentice Hall, Inc, 43-68. Norusis M: Multinomial logistic regression analysis. SPSS 16.0 Advanced Statistical Procedures. Edited by: Norusis M. 2007, Companion Upper Saddle-River, N.J: Prentice Hall, Inc, 43-68.
24.
go back to reference Blair A, Freeman LB: Epidemiologic studies of cancer in agricultural populations: observations and future directions. J Agromedicine. 2009, 14 (Suppl 2): 125-131. 10.1080/10599240902779436.CrossRefPubMedPubMedCentral Blair A, Freeman LB: Epidemiologic studies of cancer in agricultural populations: observations and future directions. J Agromedicine. 2009, 14 (Suppl 2): 125-131. 10.1080/10599240902779436.CrossRefPubMedPubMedCentral
25.
go back to reference Alavanja MC, Ward MH, Reynolds P: Carcinogenicity of agricultural pesticides in adults and children. J Agromedicine. 2007, 12 (Suppl 1): 39-56. 10.1300/J096v12n01_05.CrossRefPubMed Alavanja MC, Ward MH, Reynolds P: Carcinogenicity of agricultural pesticides in adults and children. J Agromedicine. 2007, 12 (Suppl 1): 39-56. 10.1300/J096v12n01_05.CrossRefPubMed
26.
go back to reference Blair A, Sandler D, Thomas K, Hoppin JA, Kamel F, Coble J, Lee WJ, Rusiecki J, Knott C, Dosemeci M, Lynch CF, Lubin J, Alanvaja M: Disease and injury among participants in the agricultural health study. J Agric Saf Health. 2005, 11 (Suppl 2): 141-50.CrossRefPubMedPubMedCentral Blair A, Sandler D, Thomas K, Hoppin JA, Kamel F, Coble J, Lee WJ, Rusiecki J, Knott C, Dosemeci M, Lynch CF, Lubin J, Alanvaja M: Disease and injury among participants in the agricultural health study. J Agric Saf Health. 2005, 11 (Suppl 2): 141-50.CrossRefPubMedPubMedCentral
27.
go back to reference Bassil KL, Vakil C, Sanborn M, Cole DC, Kaur JS, Kerr KJ: Cancer health effects of pesticides. Systematic review. Can Fam Physician. 2007, 53: 1704-1711.PubMedPubMedCentral Bassil KL, Vakil C, Sanborn M, Cole DC, Kaur JS, Kerr KJ: Cancer health effects of pesticides. Systematic review. Can Fam Physician. 2007, 53: 1704-1711.PubMedPubMedCentral
28.
go back to reference 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: e11-10.1136/oem.60.9.e11.CrossRefPubMedPubMedCentral 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: e11-10.1136/oem.60.9.e11.CrossRefPubMedPubMedCentral
29.
go back to reference Zeeb H, Blettner M: Adult leukemia: what is the role of currently known risk factors?. Radiat Envioron Biophys. 1998, 36 (Suppl 4): 217-28. 10.1007/s004110050075.CrossRef Zeeb H, Blettner M: Adult leukemia: what is the role of currently known risk factors?. Radiat Envioron Biophys. 1998, 36 (Suppl 4): 217-28. 10.1007/s004110050075.CrossRef
30.
go back to reference Clavel J, Mandereau L, Cordier S, Le Goaster C, Hemon D, Conso F, Flandrin G: Hairy cell leukaemia, occupation, and smoking. Br J Haematol. 1995, 91 (Suppl 1): 154-61. 10.1111/j.1365-2141.1995.tb05261.x.CrossRefPubMed Clavel J, Mandereau L, Cordier S, Le Goaster C, Hemon D, Conso F, Flandrin G: Hairy cell leukaemia, occupation, and smoking. Br J Haematol. 1995, 91 (Suppl 1): 154-61. 10.1111/j.1365-2141.1995.tb05261.x.CrossRefPubMed
31.
go back to reference Eriksson M, Karlson M: Occupational and other environmental factors and multiple myeloma: a population-based case-control study. Br J Ind Med. 1992, 49: 95-103.PubMedPubMedCentral Eriksson M, Karlson M: Occupational and other environmental factors and multiple myeloma: a population-based case-control study. Br J Ind Med. 1992, 49: 95-103.PubMedPubMedCentral
32.
go back to reference Beard J, Sladden T, Morgan G, Berry G, Brooks L, McMichael A: Health impact of pesticide exposure in a cohort of outdoor workers. Environ Health Perspect. 2003, 111 (Suppl 5): 724-730.PubMedPubMedCentral Beard J, Sladden T, Morgan G, Berry G, Brooks L, McMichael A: Health impact of pesticide exposure in a cohort of outdoor workers. Environ Health Perspect. 2003, 111 (Suppl 5): 724-730.PubMedPubMedCentral
Metadata
Title
Pesticide exposure and lymphohaematopoietic cancers: a case-control study in an agricultural region (Larissa, Thessaly, Greece)
Authors
Maria Kokouva
Nikolaos Bitsolas
Georgios M Hadjigeorgiou
George Rachiotis
Nikolaos Papadoulis
Christos Hadjichristodoulou
Publication date
01-12-2011
Publisher
BioMed Central
Published in
BMC Public Health / Issue 1/2011
Electronic ISSN: 1471-2458
DOI
https://doi.org/10.1186/1471-2458-11-5

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