Pesticide use and inflammatory bowel disease in licensed pesticide applicators and spouses in the Agricultural Health Study

Pesticide exposure has been linked to some autoimmune diseases and colorectal cancer, possibly via alteration of gut microbiota or other mechanisms. While pesticides have been linked to gut dysbiosis and inflammation in animal models, few epidemiologic studies have examined pesticides in relation to...

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Veröffentlicht in:Environmental research 2024-05, Vol.249, p.118464-118464, Article 118464
Hauptverfasser: Chen, Dazhe, Parks, Christine G., Hofmann, Jonathan N., Beane Freeman, Laura E., Sandler, Dale P.
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creator Chen, Dazhe
Parks, Christine G.
Hofmann, Jonathan N.
Beane Freeman, Laura E.
Sandler, Dale P.
description Pesticide exposure has been linked to some autoimmune diseases and colorectal cancer, possibly via alteration of gut microbiota or other mechanisms. While pesticides have been linked to gut dysbiosis and inflammation in animal models, few epidemiologic studies have examined pesticides in relation to inflammatory bowel disease (IBD). We evaluated use of pesticides and incident IBD in 68,480 eligible pesticide applicators and spouses enrolled in the Agricultural Health Study. Self-reported IBD cases were identified from follow-up questionnaires between enrollment (1993–1997) and 2022. We evaluated IBD incidence in relation to self-reported ever use of 50 pesticides among applicators and spouses. We also explored associations with intensity-weighted lifetime days (IWLD) of pesticide use among male applicators. Covariate-adjusted hazard ratios (HR) and 95% confidence intervals (CI) were calculated using Cox regression. We identified 454 IBD cases, including 227 among male applicators. In analyses with applicators and spouses combined, associations were positive (HR > 1.2) for ever vs. never use of five organochlorine insecticides, three organophosphate insecticides, one fungicide, and five herbicides. HRs were highest for dieldrin (HR = 1.59, 95%CI: 1.03, 2.44), toxaphene (HR = 1.61, 95%CI: 1.17, 2.21), parathion (HR = 1.42, 95%CI: 1.03, 1.95), and terbufos (HR = 1.53, 95%CI: 1.19, 1.96). We had limited power in many IWLD of pesticide use analyses and did not find clear evidence of exposure-response trends; however, we observed elevated HRs in all tertiles of IWLD use of terbufos compared to never use (T1 vs. never use HR = 1.52, 95%CI: 1.03, 2.24; T2 vs. never use HR = 1.53, 95%CI: 1.04, 2.26; T3 vs. never use HR = 1.51, 95%CI: 1.03, 2.23). Exposure to specific pesticides was associated with elevated hazards of IBD. These findings may have public health importance given the widespread use of pesticides and the limited number of known modifiable environmental risk factors for IBD. •Pesticide use may contribute to inflammatory bowel disease (IBD) via gut dysbiosis.•We studied ever and lifetime use of 50 pesticides and IBD in a farming population.•Positive associations were found for ever vs. never use of 14 pesticides.•HRs were highest for ever use of dieldrin, toxaphene, parathion, and terbufos.•IBD incidence was increased at all levels of lifetime days of terbufos use.
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While pesticides have been linked to gut dysbiosis and inflammation in animal models, few epidemiologic studies have examined pesticides in relation to inflammatory bowel disease (IBD). We evaluated use of pesticides and incident IBD in 68,480 eligible pesticide applicators and spouses enrolled in the Agricultural Health Study. Self-reported IBD cases were identified from follow-up questionnaires between enrollment (1993–1997) and 2022. We evaluated IBD incidence in relation to self-reported ever use of 50 pesticides among applicators and spouses. We also explored associations with intensity-weighted lifetime days (IWLD) of pesticide use among male applicators. Covariate-adjusted hazard ratios (HR) and 95% confidence intervals (CI) were calculated using Cox regression. We identified 454 IBD cases, including 227 among male applicators. In analyses with applicators and spouses combined, associations were positive (HR &gt; 1.2) for ever vs. never use of five organochlorine insecticides, three organophosphate insecticides, one fungicide, and five herbicides. HRs were highest for dieldrin (HR = 1.59, 95%CI: 1.03, 2.44), toxaphene (HR = 1.61, 95%CI: 1.17, 2.21), parathion (HR = 1.42, 95%CI: 1.03, 1.95), and terbufos (HR = 1.53, 95%CI: 1.19, 1.96). We had limited power in many IWLD of pesticide use analyses and did not find clear evidence of exposure-response trends; however, we observed elevated HRs in all tertiles of IWLD use of terbufos compared to never use (T1 vs. never use HR = 1.52, 95%CI: 1.03, 2.24; T2 vs. never use HR = 1.53, 95%CI: 1.04, 2.26; T3 vs. never use HR = 1.51, 95%CI: 1.03, 2.23). Exposure to specific pesticides was associated with elevated hazards of IBD. These findings may have public health importance given the widespread use of pesticides and the limited number of known modifiable environmental risk factors for IBD. •Pesticide use may contribute to inflammatory bowel disease (IBD) via gut dysbiosis.•We studied ever and lifetime use of 50 pesticides and IBD in a farming population.•Positive associations were found for ever vs. never use of 14 pesticides.•HRs were highest for ever use of dieldrin, toxaphene, parathion, and terbufos.•IBD incidence was increased at all levels of lifetime days of terbufos use.</description><identifier>ISSN: 0013-9351</identifier><identifier>EISSN: 1096-0953</identifier><identifier>DOI: 10.1016/j.envres.2024.118464</identifier><identifier>PMID: 38354883</identifier><language>eng</language><publisher>Netherlands: Elsevier Inc</publisher><subject>Adult ; Aged ; Agriculture ; animals ; Autoimmune disease ; chlorinated hydrocarbons ; colorectal neoplasms ; dieldrin ; dysbiosis ; Farmers - statistics &amp; numerical data ; Female ; fungicides ; Humans ; Incidence ; inflammation ; Inflammatory bowel disease ; Inflammatory Bowel Diseases - chemically induced ; Inflammatory Bowel Diseases - epidemiology ; intestinal microorganisms ; Iowa - epidemiology ; Male ; males ; Middle Aged ; Occupational Exposure - adverse effects ; Occupational exposures ; Organochlorines ; parathion ; Pesticides ; Pesticides - toxicity ; public health ; regression analysis ; risk ; Spouses - statistics &amp; numerical data ; terbufos ; toxaphene</subject><ispartof>Environmental research, 2024-05, Vol.249, p.118464-118464, Article 118464</ispartof><rights>2024</rights><rights>Published by Elsevier Inc.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c441t-22a347eae136613cf6840d197fe6cd9b059d81cdc74a1f6d1d33dd7f138279d33</citedby><cites>FETCH-LOGICAL-c441t-22a347eae136613cf6840d197fe6cd9b059d81cdc74a1f6d1d33dd7f138279d33</cites><orcidid>0000-0001-9951-5458 ; 0000-0002-1043-5812 ; 0000-0002-6776-0018</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0013935124003682$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,3536,27903,27904,65309</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38354883$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Chen, Dazhe</creatorcontrib><creatorcontrib>Parks, Christine G.</creatorcontrib><creatorcontrib>Hofmann, Jonathan N.</creatorcontrib><creatorcontrib>Beane Freeman, Laura E.</creatorcontrib><creatorcontrib>Sandler, Dale P.</creatorcontrib><title>Pesticide use and inflammatory bowel disease in licensed pesticide applicators and spouses in the Agricultural Health Study</title><title>Environmental research</title><addtitle>Environ Res</addtitle><description>Pesticide exposure has been linked to some autoimmune diseases and colorectal cancer, possibly via alteration of gut microbiota or other mechanisms. While pesticides have been linked to gut dysbiosis and inflammation in animal models, few epidemiologic studies have examined pesticides in relation to inflammatory bowel disease (IBD). We evaluated use of pesticides and incident IBD in 68,480 eligible pesticide applicators and spouses enrolled in the Agricultural Health Study. Self-reported IBD cases were identified from follow-up questionnaires between enrollment (1993–1997) and 2022. We evaluated IBD incidence in relation to self-reported ever use of 50 pesticides among applicators and spouses. We also explored associations with intensity-weighted lifetime days (IWLD) of pesticide use among male applicators. Covariate-adjusted hazard ratios (HR) and 95% confidence intervals (CI) were calculated using Cox regression. We identified 454 IBD cases, including 227 among male applicators. In analyses with applicators and spouses combined, associations were positive (HR &gt; 1.2) for ever vs. never use of five organochlorine insecticides, three organophosphate insecticides, one fungicide, and five herbicides. HRs were highest for dieldrin (HR = 1.59, 95%CI: 1.03, 2.44), toxaphene (HR = 1.61, 95%CI: 1.17, 2.21), parathion (HR = 1.42, 95%CI: 1.03, 1.95), and terbufos (HR = 1.53, 95%CI: 1.19, 1.96). We had limited power in many IWLD of pesticide use analyses and did not find clear evidence of exposure-response trends; however, we observed elevated HRs in all tertiles of IWLD use of terbufos compared to never use (T1 vs. never use HR = 1.52, 95%CI: 1.03, 2.24; T2 vs. never use HR = 1.53, 95%CI: 1.04, 2.26; T3 vs. never use HR = 1.51, 95%CI: 1.03, 2.23). Exposure to specific pesticides was associated with elevated hazards of IBD. These findings may have public health importance given the widespread use of pesticides and the limited number of known modifiable environmental risk factors for IBD. •Pesticide use may contribute to inflammatory bowel disease (IBD) via gut dysbiosis.•We studied ever and lifetime use of 50 pesticides and IBD in a farming population.•Positive associations were found for ever vs. never use of 14 pesticides.•HRs were highest for ever use of dieldrin, toxaphene, parathion, and terbufos.•IBD incidence was increased at all levels of lifetime days of terbufos use.</description><subject>Adult</subject><subject>Aged</subject><subject>Agriculture</subject><subject>animals</subject><subject>Autoimmune disease</subject><subject>chlorinated hydrocarbons</subject><subject>colorectal neoplasms</subject><subject>dieldrin</subject><subject>dysbiosis</subject><subject>Farmers - statistics &amp; numerical data</subject><subject>Female</subject><subject>fungicides</subject><subject>Humans</subject><subject>Incidence</subject><subject>inflammation</subject><subject>Inflammatory bowel disease</subject><subject>Inflammatory Bowel Diseases - chemically induced</subject><subject>Inflammatory Bowel Diseases - epidemiology</subject><subject>intestinal microorganisms</subject><subject>Iowa - epidemiology</subject><subject>Male</subject><subject>males</subject><subject>Middle Aged</subject><subject>Occupational Exposure - adverse effects</subject><subject>Occupational exposures</subject><subject>Organochlorines</subject><subject>parathion</subject><subject>Pesticides</subject><subject>Pesticides - toxicity</subject><subject>public health</subject><subject>regression analysis</subject><subject>risk</subject><subject>Spouses - statistics &amp; 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numerical data</topic><topic>terbufos</topic><topic>toxaphene</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Chen, Dazhe</creatorcontrib><creatorcontrib>Parks, Christine G.</creatorcontrib><creatorcontrib>Hofmann, Jonathan N.</creatorcontrib><creatorcontrib>Beane Freeman, Laura E.</creatorcontrib><creatorcontrib>Sandler, Dale P.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Environmental research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Chen, Dazhe</au><au>Parks, Christine G.</au><au>Hofmann, Jonathan N.</au><au>Beane Freeman, Laura E.</au><au>Sandler, Dale P.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Pesticide use and inflammatory bowel disease in licensed pesticide applicators and spouses in the Agricultural Health Study</atitle><jtitle>Environmental research</jtitle><addtitle>Environ Res</addtitle><date>2024-05-15</date><risdate>2024</risdate><volume>249</volume><spage>118464</spage><epage>118464</epage><pages>118464-118464</pages><artnum>118464</artnum><issn>0013-9351</issn><eissn>1096-0953</eissn><abstract>Pesticide exposure has been linked to some autoimmune diseases and colorectal cancer, possibly via alteration of gut microbiota or other mechanisms. While pesticides have been linked to gut dysbiosis and inflammation in animal models, few epidemiologic studies have examined pesticides in relation to inflammatory bowel disease (IBD). We evaluated use of pesticides and incident IBD in 68,480 eligible pesticide applicators and spouses enrolled in the Agricultural Health Study. Self-reported IBD cases were identified from follow-up questionnaires between enrollment (1993–1997) and 2022. We evaluated IBD incidence in relation to self-reported ever use of 50 pesticides among applicators and spouses. We also explored associations with intensity-weighted lifetime days (IWLD) of pesticide use among male applicators. Covariate-adjusted hazard ratios (HR) and 95% confidence intervals (CI) were calculated using Cox regression. We identified 454 IBD cases, including 227 among male applicators. In analyses with applicators and spouses combined, associations were positive (HR &gt; 1.2) for ever vs. never use of five organochlorine insecticides, three organophosphate insecticides, one fungicide, and five herbicides. HRs were highest for dieldrin (HR = 1.59, 95%CI: 1.03, 2.44), toxaphene (HR = 1.61, 95%CI: 1.17, 2.21), parathion (HR = 1.42, 95%CI: 1.03, 1.95), and terbufos (HR = 1.53, 95%CI: 1.19, 1.96). We had limited power in many IWLD of pesticide use analyses and did not find clear evidence of exposure-response trends; however, we observed elevated HRs in all tertiles of IWLD use of terbufos compared to never use (T1 vs. never use HR = 1.52, 95%CI: 1.03, 2.24; T2 vs. never use HR = 1.53, 95%CI: 1.04, 2.26; T3 vs. never use HR = 1.51, 95%CI: 1.03, 2.23). Exposure to specific pesticides was associated with elevated hazards of IBD. These findings may have public health importance given the widespread use of pesticides and the limited number of known modifiable environmental risk factors for IBD. •Pesticide use may contribute to inflammatory bowel disease (IBD) via gut dysbiosis.•We studied ever and lifetime use of 50 pesticides and IBD in a farming population.•Positive associations were found for ever vs. never use of 14 pesticides.•HRs were highest for ever use of dieldrin, toxaphene, parathion, and terbufos.•IBD incidence was increased at all levels of lifetime days of terbufos use.</abstract><cop>Netherlands</cop><pub>Elsevier Inc</pub><pmid>38354883</pmid><doi>10.1016/j.envres.2024.118464</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0001-9951-5458</orcidid><orcidid>https://orcid.org/0000-0002-1043-5812</orcidid><orcidid>https://orcid.org/0000-0002-6776-0018</orcidid><oa>free_for_read</oa></addata></record>
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subjects Adult
Aged
Agriculture
animals
Autoimmune disease
chlorinated hydrocarbons
colorectal neoplasms
dieldrin
dysbiosis
Farmers - statistics & numerical data
Female
fungicides
Humans
Incidence
inflammation
Inflammatory bowel disease
Inflammatory Bowel Diseases - chemically induced
Inflammatory Bowel Diseases - epidemiology
intestinal microorganisms
Iowa - epidemiology
Male
males
Middle Aged
Occupational Exposure - adverse effects
Occupational exposures
Organochlorines
parathion
Pesticides
Pesticides - toxicity
public health
regression analysis
risk
Spouses - statistics & numerical data
terbufos
toxaphene
title Pesticide use and inflammatory bowel disease in licensed pesticide applicators and spouses in the Agricultural Health Study
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