{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,4]],"date-time":"2026-10-04T21:19:26Z","timestamp":1791148766381,"version":"4.1.0"},"reference-count":50,"publisher":"Public Library of Science (PLoS)","issue":"10","license":[{"start":{"date-parts":[[2014,10,22]],"date-time":"2014-10-22T00:00:00Z","timestamp":1413936000000},"content-version":"unspecified","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/publicdomain\/zero\/1.0\/"}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0109332","type":"journal-article","created":{"date-parts":[[2014,10,22]],"date-time":"2014-10-22T17:50:30Z","timestamp":1414000230000},"page":"e109332","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":145,"title":["Non-Hodgkin Lymphoma Risk and Insecticide, Fungicide and Fumigant Use in the Agricultural Health Study"],"prefix":"10.1371","volume":"9","author":[{"given":"Michael C. R.","family":"Alavanja","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jonathan N.","family":"Hofmann","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Charles F.","family":"Lynch","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cynthia J.","family":"Hines","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kathryn H.","family":"Barry","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joseph","family":"Barker","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dennis W.","family":"Buckman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kent","family":"Thomas","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dale P.","family":"Sandler","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jane A.","family":"Hoppin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stella","family":"Koutros","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gabriella","family":"Andreotti","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jay H.","family":"Lubin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aaron","family":"Blair","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Laura E.","family":"Beane Freeman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2014,10,22]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1093\/oxfordjournals.aje.a121324","article-title":"Leukemia and multiple myeloma in farmers","volume":"94","author":"S Milham","year":"1971","journal-title":"Am J Epidemiol"},{"key":"ref2","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1002\/ijc.2910290303","article-title":"Farming and mortality from non-Hodgkin\u2019s lymphoma: a case-control study","volume":"29","author":"KP Cantor","year":"1982","journal-title":"Int J Cancer"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"397","DOI":"10.5271\/sjweh.2208","article-title":"Cancer among farmers: A review","volume":"11","author":"A Blair","year":"1985","journal-title":"Scand J Work Environ Health"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1093\/oxfordjournals.aje.a113993","article-title":"Malignant lymphoma and multiple myeloma linked with agricultural occupation in a New Zealand cancer registration-base-study","volume":"121","author":"NE Pearce","year":"1985","journal-title":"Am J Epidemiol"},{"key":"ref5","doi-asserted-by":"crossref","first-page":"215","DOI":"10.5271\/sjweh.782","article-title":"Occupation, pesticide exposure and risk of multiple myeloma","volume":"30(3)","author":"D Baris","year":"2004","journal-title":"Scand J Work Environ Health"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"663","DOI":"10.1007\/s10552-012-9921-1","article-title":"Poultry and livestock exposure and cancer risk among farmers in the agricultural health study","volume":"23","author":"LE Beane Freeman","year":"2012","journal-title":"Cancer Causes Control"},{"key":"ref7","unstructured":"Cordes DH, Rea DF (1991) Farming: A Hazardous Occupation. In: Health Hazards of Farming. Occupational Medicine: State of the Art Reviews. Vol6(3). Hanley &amp; Belfus, Inc., Philadelphia, PA."},{"key":"ref8","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1080\/10937404.2012.632358","article-title":"Occupational pesticide exposure and cancer risk. A Review","volume":"1594","author":"M Alavanja","year":"2012","journal-title":"J. Toxicol Environ Health B Critic Review"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"120","DOI":"10.3322\/caac.21170","article-title":"Increased cancer burden among pesticide applicators and others due to pesticide exposure","volume":"63(2)","author":"MCR Alavanja","year":"2013","journal-title":"CA, Cancer J Clin"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"509","DOI":"10.1023\/A:1011293208949","article-title":"Agricultural use of organophosphate pesticides and the risk of non-Hodgkin\u2019s lymphoma among male farmers (United States)","volume":"12","author":"BL Waddell","year":"2001","journal-title":"Cancer Causes and Control"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"1209","DOI":"10.1007\/s10552-007-9061-1","article-title":"Occupational exposure to pesticides and risk of hematopoietic cancers: meta-analysis of case-control studies","volume":"18","author":"M Merhi","year":"2007","journal-title":"Cancer Causes Control"},{"key":"ref12","unstructured":"IARC (1991) International Agency for Research on Cancer (IARC). Occupational Exposures in Insecticide applications and some pesticides. Lyon, France: IARC, 1991. Monographs on the Evaluation of Carcinogenic Risk to Humans, volume 53."},{"key":"ref13","doi-asserted-by":"crossref","first-page":"130","DOI":"10.1093\/jncimonographs\/lgu013","article-title":"Etiologic Heterogeneity Among NHL Subtypes: The InterLymph NHL Subtypes Project","volume":"48","author":"LM Morton","year":"2014","journal-title":"J Natl Cancer Institute"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"362","DOI":"10.1289\/ehp.96104362","article-title":"The Agricultural Health Study","volume":"104","author":"MCR Alavanja","year":"1996","journal-title":"Environ Health Perspect"},{"key":"ref15","doi-asserted-by":"crossref","first-page":"800","DOI":"10.1093\/aje\/kwg040","article-title":"Use of agricultural pesticides and prostate cancer risk in the Agricultural Health Study Cohort","volume":"157(9)","author":"MC Alavanja","year":"2003","journal-title":"Am J Epidemiol"},{"key":"ref16","unstructured":"SEER Program, National Cancer Institute. Available: <ext-link xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" ext-link-type=\"uri\" xlink:href=\"http:\/\/seer.cancer.gov\/lymphomarecode\" xlink:type=\"simple\">http:\/\/seer.cancer.gov\/lymphomarecode<\/ext-link> Accessed September 15, 2013."},{"key":"ref17","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1182\/blood-2006-11-051672","article-title":"Proposed classifciation of lymphoid neoplasms for epidemiologic research from the Pathology Working Group of the International Lymphoma Epidemiology Consortium (InterLymph)","volume":"110(2)","author":"LM Morton","year":"2007","journal-title":"Blood"},{"key":"ref18","unstructured":"Percy C, Fritz A, Ries L (2001) Conversion of neoplasms by topography and morphology from the International Classification of Disease for Oncology, second edition, to International Classification of Diseases for Oncology, 3<sup>rd<\/sup> ed. Cancer Statistics Branch, DCCPS, SEER Program, National Cancer Institute; 2001."},{"key":"ref19","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1038\/jes.2012.31","article-title":"Using multiple imputation to assign pesticide use for non-respondents in the follow-up questionnaire in the Agricultural Health Study J","volume":"22(4)","author":"SL Heltshe","year":"2012","journal-title":"Exp Sci Environ Epidemiol"},{"key":"ref20","doi-asserted-by":"crossref","first-page":"4608","DOI":"10.3390\/ijerph8124608","article-title":"An updated algorithm for estimation of pesticide exposure intensity in the Agricultural Health Study","volume":"8(12)","author":"J Coble","year":"2011","journal-title":"Int J Environ Res Public Health"},{"key":"ref21","unstructured":"ATSDR (2005) Agency for Toxic Substances and Disease Registry. Toxicological profile for Alpha-, Beta-, Gamma- and Delta- Hexachlorcyclohexane, August, 2005. Available: <ext-link xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" ext-link-type=\"uri\" xlink:href=\"http:\/\/www.atsdr.cdc.gov\/Toxprofiles\/tp43.pdf\" xlink:type=\"simple\">http:\/\/www.atsdr.cdc.gov\/Toxprofiles\/tp43.pdf<\/ext-link>. Accessed 2013 Sep 15."},{"key":"ref22","unstructured":"EPA (2006a) US Environmental Protection Agency (2006). Lindane; Cancellation Order December 13, 2006. Federal Register\/Vol 71, number 239, page 74905."},{"key":"ref23","unstructured":"Stockholm Convention Report (2009) Report of the conference of the Parties of the Stockholm Convention on Persistent Organic Pollutants on the work of its fourth meeting. Convention on Persistent Organic Pollutants. Fourth Meeting, Geneva, 4\u20138 May 2009. Available: http;\/\/chm.pops.int\/Portals\/0\/Repository\/COP4\/UNEP-POPS-COP.4\u201338.English.pdf."},{"key":"ref24","unstructured":"IARC (1987) International Agency for Research on Cancer (IARC). Overall evaluation of carcinogenicity: an updating of IARC monographs volume 1 to 42. Lyon, France: IARC, 1987. Monographs on the Evaluation of Carcinogenic Risk to Humans, Supplement 7."},{"key":"ref25","doi-asserted-by":"crossref","first-page":"1160","DOI":"10.1080\/15287390903091780","article-title":"Lindane-induced generation of reactive oxygen species and depletion of glutathione do not result in necrosis in renal distal tube cells","volume":"72","author":"AL Piskac-Collier","year":"2009","journal-title":"J Toxicol and Environ Health, Part A"},{"key":"ref26","doi-asserted-by":"crossref","first-page":"271","DOI":"10.1007\/BF00285170","article-title":"Genotoxic effect of benzene hexachloride in cultured human lymphocytes","volume":"83","author":"DS Rupa","year":"1989","journal-title":"Hum Genet"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1002\/(SICI)1097-0274(199801)33:1<82::AID-AJIM9>3.0.CO;2-Y","article-title":"Non-Hodgkin\u2019s lymphoma and agricultural use of the insecticide lindane","volume":"33","author":"A Blair","year":"1998","journal-title":"Am J Ind Med"},{"key":"ref28","first-page":"1155","article-title":"Non-Hodgkin\u2019s lymphoma and specific pesticide exposures in Men: Cross-Canada Study of Pesticides and Health","volume":"10","author":"HH McDuffie","year":"2001","journal-title":"Cancer, Epidemiology, Biomarkers & Prevention"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"642","DOI":"10.1002\/ijc.22258","article-title":"Occupational exposure to organochlorine insecticides and cancer incidence in the Agricultural Health Study","volume":"120(3)","author":"MP Purdue","year":"2007","journal-title":"Int J Cancer"},{"key":"ref30","unstructured":"EPA (2012) US Environmental Protection Agency 2012. DDT-A Brief History and Status. Available: <ext-link xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" ext-link-type=\"uri\" xlink:href=\"http:\/\/www.epa.gov\/pesticides\/factsheets\/chemicals\/ddt-brief-history-status.htm\" xlink:type=\"simple\">http:\/\/www.epa.gov\/pesticides\/factsheets\/chemicals\/ddt-brief-history-status.htm<\/ext-link>. Accessed 2013 Sep 15."},{"key":"ref31","unstructured":"NTP (2011) National Toxicology Program, Report on Carcinogen- Twelfth Edition. Available: <ext-link xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" ext-link-type=\"uri\" xlink:href=\"http:\/\/ntp.niehs.nih.gov\/go\/roc12\" xlink:type=\"simple\">http:\/\/ntp.niehs.nih.gov\/go\/roc12<\/ext-link>. Accessed 2013 Sep 15."},{"key":"ref32","first-page":"522","article-title":"Agricultural use of DDT and the risk of non-Hodgkin\u2019s lymphoma: pooled analysis of three case-control studies in the United States, Occup Environ Med","volume":"55","author":"D Baris","year":"1998"},{"key":"ref33","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1136\/oemed-2012-100845","article-title":"Lymphoma risk and occupational exposure to pesticides: results of the Epilymph study","volume":"70(2)","author":"P Cocco","year":"2013","journal-title":"Occupational Environ Med"},{"key":"ref34","first-page":"652","article-title":"Chronic lymphocytic leukaemia and non-Hodgkin\u2019s lymphomas by histological type in farming-animal breeding workers: a population case-control study based on a priori exposure matrics Occup Environ Med","volume":"53(10)","author":"O Nanni","year":"1996"},{"key":"ref35","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1016\/S0140-6736(97)02088-6","article-title":"A nested case-control study of non-Hodgkin lymphoma and serum organochlorine residues","volume":"350","author":"N Rothman","year":"1997","journal-title":"The Lancet"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"854","DOI":"10.1289\/ehp.6726","article-title":"Adipose tissue levels of organochlorine pesticides and chlorinated biphenyls and the risk of non-Hodgkin\u2019s lymphoma","volume":"112","author":"PJE Quintana","year":"2004","journal-title":"Environ Health Perspect"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1289\/ehp.1103573","article-title":"A prospective study of organochlorines in adipose tissue and risk of non-Hodgkin lymphoma","volume":"120(1)","author":"EV Brauner","year":"2012","journal-title":"Environ Health Perspect"},{"key":"ref38","doi-asserted-by":"crossref","first-page":"2767","DOI":"10.1002\/ijc.23005","article-title":"Organochlorines and risk of non-Hodgkin lymphoma","volume":"121(12)","author":"JJ Spinelli","year":"2007","journal-title":"Int J Cancer"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1136\/oem.2007.033548","article-title":"Plasma polychlorobiphenyl and organochlorine pesticide level and risk of major lymphoma subtypes","volume":"65","author":"P Cocco","year":"2008","journal-title":"Occup Environ Med"},{"key":"ref40","unstructured":"EPA 2006(b). U.S. Environmental Protection Agency. 2006. Re-registration Eligibility Decision for Permethrin: Available: <ext-link xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" ext-link-type=\"uri\" xlink:href=\"http:\/\/www.epa.gov\/oppsrrd1\/REDs\/permethrin_red.pdf\" xlink:type=\"simple\">http:\/\/www.epa.gov\/oppsrrd1\/REDs\/permethrin_red.pdf<\/ext-link>. Accessed 2013 Sep 15."},{"key":"ref41","unstructured":"NPIC (2012). National Pesticide Information Center. Chemicals Evaluated for Carcinogenic Potential. Office of Pesticide Programs. U.S. Environmental Protection Agency. November 2012. Available: <ext-link xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" ext-link-type=\"uri\" xlink:href=\"http:\/\/npic.orst.edu\/chemicals_evaluated.pdf\" xlink:type=\"simple\">http:\/\/npic.orst.edu\/chemicals_evaluated.pdf<\/ext-link>. Accessed 2013 Sep 15."},{"key":"ref42","first-page":"E11","article-title":"Integrative assessment of multiple pesticides as risk factors for non-Hodgkin\u2019s lymphoma among men Occup Environ Med","volume":"60","author":"AJ De Roos","year":"2003"},{"key":"ref43","doi-asserted-by":"crossref","first-page":"582","DOI":"10.1289\/ehp.11318","article-title":"Cancer incidence among pesticide applicators exposed to permethrin in the Agricultural Health Study","volume":"117","author":"JA Rusiecki","year":"2009","journal-title":"Environ Health Perspect"},{"key":"ref44","unstructured":"EPA 2006(b). U.S. Environmental Protection Agency. 2006. Re-registration Eligibility Decision for Terbufos: Available: <ext-link xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" ext-link-type=\"uri\" xlink:href=\"http:\/\/www.epa.gov\/pesticides\/reregistration\/REDs\/terbufos_red.pdf\" xlink:type=\"simple\">http:\/\/www.epa.gov\/pesticides\/reregistration\/REDs\/terbufos_red.pdf<\/ext-link> Accessed 2013 Nov 18."},{"key":"ref45","unstructured":"Environmental Protection Agency, 2004. Interim registration eligibility decision: diazinon. Available: <ext-link xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" ext-link-type=\"uri\" xlink:href=\"http:\/\/www.epa.gov\/pesticides\/reregistration\/REDs\/diazinon_red.pdf\" xlink:type=\"simple\">http:\/\/www.epa.gov\/pesticides\/reregistration\/REDs\/diazinon_red.pdf<\/ext-link>. Accessed 2013 Nov 18."},{"key":"ref46","unstructured":"Donalson D, Kieley T, Grube A (2002) Pesticide industry sales and usage: 1998 and 1999 market estimates. Washington, DC.: US Environmental Protection Agency, 2002 (EPA-733-R-02\u2013001)."},{"key":"ref47","doi-asserted-by":"crossref","first-page":"1070","DOI":"10.1093\/aje\/kwi321","article-title":"Cancer incidence among male pesticide applicators in the Agricultural Health Study cohort exposed to diazinon","volume":"162","author":"LE Beane Freeman","year":"2005","journal-title":"Am J Epidemiol"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1097\/00001648-200201000-00015","article-title":"Reliability of reporting on life-style and agricultural factors by a sample of participants in the Agricultural Health Study from Iowa","volume":"13(1)","author":"R Blair A. Tarone","year":"2002","journal-title":"Epidemiology"},{"key":"ref49","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1136\/oem.2010.059469","article-title":"Impact of pesticide exposure on misclassification on estimates of relative risks in the Agricultural Health Study","volume":"68","author":"A Blair","year":"2011","journal-title":"Occup Environ Med"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1038\/jes.2009.54","article-title":"Assessment of a pesticide exposure intensity algorithm in the Agricultural Health Study","volume":"20(6)","author":"KW Thomas","year":"2010","journal-title":"J Expo Sci Environ Epidemiol"}],"container-title":["PLoS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0109332","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2019,8,16]],"date-time":"2019-08-16T13:55:07Z","timestamp":1565963707000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0109332"}},"subtitle":[],"editor":[{"given":"Suminori","family":"Akiba","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2014,10,22]]},"references-count":50,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2014,10,22]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0109332","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2014,10,22]]}}}