Occupational exposure to organophosphate pesticides and hematologic neoplasms: a systematic review

Moura, Luiza Taciana Rodrigues de; Bedor, Cheila Nataly Galindo; Lopez, Rossana Veronica Mendoza; Santana, Vilma Sousa; Rocha, Talita Máira Bueno da Silveira da; Wünsch Filho, Victor; Curado, Maria Paula

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Revista Brasileira de Epidemiologia

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ORIGINAL ARTICLE • Rev. bras. epidemiol. 23 • 2020 • https://doi.org/10.1590/1980-549720200022 copy

Occupational exposure to organophosphate pesticides and hematologic neoplasms: a systematic review

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT:

Objective:

To update findings of observational analytical studies on the association between occupational exposure to organophosphates and hematologic malignancies.

Methodology:

Systematic literature review, including cohort and case-control studies, without limitation of publication time, in Portuguese and English. The articles were traced from June 2017 to July 2019 in PubMed, MEDLINE, LILACS, Web of Science, and Scopus databases. The qualitative bias risk assessment was performed using the Newcastle-Ottawa Scale and the Downs and Black Checklist. Results were presented according to the Preferred Reporting Items for Systematic reviews and Meta-Analyses (PRISMA).

Results:

Seventeen studies evaluated as good/high methodological quality were eligible. Exposure to diazinon (1 cohort), phonophos (1 cohort), dichlorvos, crotoxiphos and famphur (1 case control) was associated with leukemia, while exposure to organophosphate was associated to lymphomas (6 case control); the risk of non-Hodgkin’s lymphoma was higher in those exposed to diazinon (1 control case) and malathion (3 control case) than non-exposed ones. Multiple myeloma occurred more commonly in organophosphate exposed than in non-exposed individuals (1 case-control).

Conclusion:

Occupational exposure to organophosphates increases the risk of hematologic malignancies, especially among individuals with longer exposure periods. Worker monitoring and exposure control measures are recommended.

Keywords:
Hematologic neoplasms; Agrochemicals; Risk factors; Epidemiology; Review; Occupational health

Authors/year/country	Study population /sample	Exposure Measurement / outcome	Adjusted RR/OR (95%CI)
Beanne Freeman et al. 2005 USA²⁰20. Beane Freeman LE, Bonner MR, Blair A, Hoppin JA, Sandler DP, Lubin JH, et al. Cancer incidence among male pesticide applicators in the Agricultural Health Study cohort exposed to diazinon. Am J Epidemiol 2005; 162(11): 1070-9. http://doi.org/10.1093/aje/kwi321 https://doi.org/http://doi.org/10.1093/a...	23,106 pesticide applicators	Questionnaire HN, leukemia, and NHL	Diazinon: Leukemia RR = 3.36 (1.08 - 10.49). High intensity HN: RR = 2.01 (1.02 - 3.94); NHL RR = 1.7 (0.56 - 5.18); Leukemia RR = 2.88 (0.92 - 9.93)
Mahajan et al. 2006 USA²¹21. Mahajan R, Blair A, Lynch CF, Schroeder P, Hoppin JA, Sandler DP, et al. Fonofos exposure and cancer incidence in the agricultural health study. Environ Health Perspect 2006; 114(12): 1838-42. http://doi.org/10.1289/ehp.9301 https://doi.org/http://doi.org/10.1289/e...	45,372 pesticide applicators	Questionnaire HN and leukemia	Phonophos: High intensity exposure/days HN RR = 1.14 (0.64 - 2.02); Leukemia RR = 2.67 (1.06 - 6.70)
Mahajan et al. 2006 USA²²22. Mahajan R, Bonner MR, Hoppin JA, Alavanja MCR. Phorate exposure and incidence of cancer in the Agricultural Health Study. Environ Health Perspect 2006; 114(8): 1205-9. http://doi.org/10.1289/ehp.8911 https://doi.org/http://doi.org/10.1289/e...	21,016 pesticide applicators	Questionnaire HN	Phorate: High exposure in number of days during life HN RR = 0.64 (0.52 - 2.17)
Bonner et al. 2007 USA²³23. Bonner MR, Coble J, Blair A, Beane Freeman LE, Hoppin JA, Sandler DP, et al. Malathion Exposure and the Incidence of Cancer in the Agricultural Health Study. Am J Epidemiol 2007; 166(9): 1023-34. https://doi.org/10.1093/aje/kwm182 https://doi.org/https://doi.org/10.1093/...	19,717 pesticide applicators	Questionnaire HN, leukemia, and NHL	Malathion. High exposure in number of days during life HN RR = 1.27 (0.75 - 2.16); Leukemia RR = 1.65 (0.71 - 3.86); NHL RR = 0.81 (0.33 - 2.01)
Koutros et al. 2008 USA²⁴24. Koutros S, Mahajan R, Zheng T, Hoppin JA, Ma X, Lynch CF, et al. Dichlorvos exposure and human cancer risk: results from the Agricultural Health Study. Cancer Causes Control 2008; 19(1): 59-65. http://doi.org/10.1007/s10552-007-9070-0 https://doi.org/http://doi.org/10.1007/s...	49,762 pesticide applicators	Questionnaire HN	Dichlorvos. High intensity exposure /days HN RR = 1.00 (0.51 - 1.96)
Bonner et al. 2010 USA²⁵25. Bonner MR, Williams BA, Rusiecki JA, Blair A, Beane Freeman LE, Hoppin JA, et al. Occupational exposure to terbufos and the incidence of cancer in the Agricultural Health Study. Cancer Causes Control 2010; 21(6): 871-7. https://doi.org/10.1007/s10552-010-9514-9 https://doi.org/https://doi.org/10.1007/...	44,624 pesticide applicators	Questionnaire HN, leukemia, and NHL	Terbufos. High intensity exposure HN OR = 1.25 (0.83 - 1.87); Leukemia OR = 1.37 (0.69 - 2.75); NHL OR= 1.22 (0.67 - 2.22)

Authors/year/country	Study population/sample	Exposure Measurement /outcome	Adjusted OR (95%CI)
Kachuri et al. 2013 Canada⁸8. Kachuri L, Demers PA, Blair A, Spinelli JJ, Pahwa M, McLaughlin JR, et al. Multiple pesticide exposures and the risk of multiple myeloma in Canadian men. Int J Cancer 2013; 133(8): 1846-58. http://doi.org/10.1002/ijc.28191 https://doi.org/http://doi.org/10.1002/i...	342 Cases/1,357 Controls	Questionnaire and interview MM	Use of 1 type of OP OR = 1.16 (0.75 - 1.1) Malation OR = 1,12 (0,71 - 1,74)
Mills et al. 2005 USA²⁶26. Mills PK, Yang R, Riordan D. Lymphohematopoietic Cancers in the United Farm Workers of America (UFW), 1988-2001. Cancer Causes Control 2005; 16(7): 823-30. http://doi.org/10.1007/s10552-005-2703-2 https://doi.org/http://doi.org/10.1007/s...	131 Cases/ Controls (5:1)	UFW membership form data Leukemia, NHL and MM	Leukemia diazinon: OR = 1.32 (0.65 - 2.65)/ malathion OR = 1.3 (0.91 - 3.67). NHL: diazinon OR = 1,39 (0,76 - 2,53)/malation OR = 1,77 (0,99 - 3,17).MM sem associação
Waddell et al. 2001 USA²⁷27. Waddell BL, Zahm SH, Baris D, Weisenburger DD, Holmes F, Burmeister LF, et al. Agricultural use of organophosphate pesticides and the risk of non-Hodgkin’s lymphoma among male farmers (United States). Cancer Causes Control 2001; 12(6): 509-17. http://doi.org/10.1023/A:1011293208949 https://doi.org/http://doi.org/10.1023/A...	748 Cases /2,236 Controls	Interview NHL	Malathion > 20 years of use OR = 1.7 (1.1 - 2.9)
Hohenadel et al. 2011 Canada²⁸28. Hohenadel K, Harris SA, McLaughlin JR, Spinelli JJ, Pahwa P, Dosman JA, et al. Exposure to Multiple Pesticides and Risk of Non-Hodgkin Lymphoma in Men from Six Canadian Provinces. Int J Environ Res Public Health 2011; 8(6): 2320-30. http://doi.org/10.3390/ijerph8062320 https://doi.org/http://doi.org/10.3390/i...	513 Cases /1,506 Controls	Questionnaire and interview NHL	Use of 1 type of OP: OR = 2.10 (1.5 - 2.94). Use of 2 or + types of OP OR = 1.69 (1.04 - 2.74)
Costas et al. 2015 6 European countries²⁹29. Costas L, Infante-Rivard C, Zock JP, Van Tongeren M, Boffetta P, Cusson A, et al. Occupational exposure to endocrine disruptors and lymphoma risk in a multi-centric European study. Brit J Cancer 2015; 112(7): 1251-6. http://doi.org/10.1038/bjc.2015.83 https://doi.org/http://doi.org/10.1038/b...	2,178 Cases /2,457 Controls	Interview Lymphomas and MM	OP: Mature B-cell lymphoma OR = 1.10 (1.01 - 1.2) MM OR = 1.22 (1.06 - 1.41)
Brown et al. 1990 USA³⁰30. Brown LM, Blair A, Gibson R, Everett GD, Cantor KP, Schuman LM, et al. Pesticide Exposures and Other Agricultural Risk Factors for Leukemia among Men in Iowa and Minnesota. Cancer Res 1990; 50(20): 6585-91.	578 Cases /1,245 Controls	Interview Leukemia	Dichlorvos OR = 2.0 (1.2 - 3.5); crotoxiphos OR = 11.1 (2.2 - 55.0). Uso há > 20 anos: famphur OR = 11,6 (1,2 - 107,0)
Cantor et al. 1992 USA³¹31. Cantor KP, Blair A, Everett G, Gibson R, Burmeister LF, Brown LM, et al. Pesticides and other agricultural risk factors for Non-Hodgkin’s Lymphoma among men in Iowa and Minnesota. Cancer Res 1992; 52(9): 2447-55.	622 Cases /1,245 Controls	Interview NHL	Use since 1965: diazinon OR = 2.6 (1.2 - 5.9); malathion OR = 2.9 (1.1 - 7.4); Phorate OR = 1.8 (0.7 - 4.5)
Nanni et al. 1996 Italy³²32. Nanni O, Amadori D, Lugaresi C, Falcini F, Scarpi E, Saragoni A, et al. Chronic lymphocytic leukaemias and non-Hodgkin’s lymphomas by histological type in farming-animal breeding workers: a population case-control study based on a priori exposure matrices. Occup Environ Med 1996; 53(10): 652-7. https://doi.org/10.1136/oem.53.10.652 https://doi.org/https://doi.org/10.1136/...	187 Cases /977 Controls	Interview NHL and CLL	OP: NHL and CLL: OR = 1.7 (0.94 - 3.09). LNH de baixo grau e LLC OR = 2,97(1,28 - 6,91)
McDuffie et al. 2001 Canada³³33. McDuffie HH, Pahwa P, McLaughlin JR, Spinelli JJ, Fincham S, Dosman JA, et al. Non-Hodgkin’s Lymphoma and specific pesticide exposures in men. Cancer Epidemiol Biomarkers Prevent 2001; 10(11): 1155-63.	517 Cases /1,506 Controls	Questionnaire and interview NHL	OP OR = 1.73 (1.27 - 2.36). Malathion up to 2 days/year OR = 1.82 (1.25 - 2.68). Use > 2 days/year OR = 1.75 (1.02 - 3.03)
Fritschi et al. 2005 Australia³⁴34. Fritschi L, Benke G, Hughes AM, Kricker A, Turner J, Vajdic CM, et al. Occupational exposure to pesticides and risk of Non-Hodgkin’s Lymphoma. Am J Epidemiol 2005; 162(9): 849-57. https://doi.org/10.1093/aje/kwi292 https://doi.org/https://doi.org/10.1093/...	694 Cases / 694 Controls	Questionnaire and interview NHL	OP: Follicular lymphoma OR = 4.28 (1.41 - 13.0)
Cocco et al. 2013 6 European countries³⁵35. Cocco P, Satta G, Dubois S, Pili C, Pilleri M, Zucca M, et al. Lymphoma risk and occupational exposure to pesticides: results of the Epilymph study. Occup Environ Med 2013; 70: 91-8. http://doi.org/10.1136/oemed-2012-100845 https://doi.org/http://doi.org/10.1136/o...	2,348 Cases /2,462 Controls	Interview Lymphomas	OP: Lymphoma: OR = 1.6 (0.9 - 2.8). CLL: OR = 2.7 (1.2 - 6.0)

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[1] Corresponding author: Maria Paula Curado. Rua Taguá, 440, Liberdade, CEP: 01508-010, São Paulo, SP, Brasil. E-mail: mp.curado@accamargo.org.br