Interactive effects of dietary deoxynivalenol and coccidial infection on growth performance, immune response, oxidative status, and gut health in pullets
IF 4.2 1区 农林科学Q1 AGRICULTURE, DAIRY & ANIMAL SCIENCE
Deependra Paneru , Milan K. Sharma , Doyun Goo , Hanyi Shi , Todd J. Applegate , Lilong Chai , Revathi Shanmugasundaram , Woo K. Kim
{"title":"Interactive effects of dietary deoxynivalenol and coccidial infection on growth performance, immune response, oxidative status, and gut health in pullets","authors":"Deependra Paneru , Milan K. Sharma , Doyun Goo , Hanyi Shi , Todd J. Applegate , Lilong Chai , Revathi Shanmugasundaram , Woo K. Kim","doi":"10.1016/j.psj.2025.105462","DOIUrl":null,"url":null,"abstract":"<div><div>Deoxynivalenol (DON) contamination of grains and coccidiosis are two major health and economic challenges in layer production, yet their combined effect during pullet rearing phase remains poorly understood. This study evaluated whether dietary DON exposure exacerbates the severity of <em>Eimeria</em> infection and delays recovery in growing pullets. A total of 288 Hy-Line W36 pullets (4-wk-old) were fed either a control diet containing 2.5 mg/kg DON or a naturally contaminated diet containing 14-15 mg/kg DON for 14 d. Birds were then sham‑dosed or orally inoculated with <em>E. acervulina</em> (50 000 oocysts), <em>E. maxima</em> (10 000) and <em>E. tenella</em> (10 000) in a 2 × 2 factorial design. Growth performance, gut permeability, intestinal morphology, jejunal tight‑junction and mucin gene expression, cecal tonsil cytokine profiles, T‑cell subsets, and hepatic redox indices were analyzed at 6 and 14 days post inoculation (DPI). DON alone did not depress weight gain; however, when coupled with <em>Eimeria</em> challenge it reduced feed intake by an additional 3 % (<em>P</em> = 0.038) and numerically aggravated intestinal lesions. The <em>Eimeria</em> challenge reduced body weight by 15 % at 6 DPI and 8 % at 14 DPI (<em>P</em> < 0.001), increased gut permeability and disrupted intestinal architecture (<em>P</em> < 0.001). <em>Eimeria</em> also damaged gut barrier integrity and induced Th1‑biased inflammation by downregulating <em>JAM2, OCLN, ZO1</em> and <em>MUC2</em> while upregulating <em>CLDN1, IFN‑γ</em> and <em>IL‑10 (P</em> < 0.05). DON independently downregulated jejunal <em>MUC2</em> and upregulated <em>IL‑1β</em>. The interaction delayed mucosal repair and immune dysregulation by further upregulating <em>CLDN1</em> at 14 DPI (<em>P</em> = 0.004) and splenic CD4⁺ cells at 6 DPI (<em>P</em> = 0.003). Hepatic redox indices were independently affected by <em>Eimeria</em> at 6 and 14 DPI, whereas DON at 14 DPI. In conclusion, diets containing 14-15 mg/kg DON negatively affected the immune response and jejunal <em>MUC2</em> expression with minimal adverse effects on growth in non-challenged pullets. However, when <em>Eimeria</em> infection was present, DON delayed gut repair and shifted immune balance toward inflammation. Therefore, routine mycotoxin surveillance and mitigation in pullet feeds are important, especially in cage‑free systems where <em>Eimeria spp.</em> often circulate subclinically, to prevent downstream negative effects on laying performance and profitability.</div></div>","PeriodicalId":20459,"journal":{"name":"Poultry Science","volume":"104 9","pages":"Article 105462"},"PeriodicalIF":4.2000,"publicationDate":"2025-06-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Poultry Science","FirstCategoryId":"97","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0032579125007060","RegionNum":1,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"AGRICULTURE, DAIRY & ANIMAL SCIENCE","Score":null,"Total":0}
引用次数: 0
Abstract
Deoxynivalenol (DON) contamination of grains and coccidiosis are two major health and economic challenges in layer production, yet their combined effect during pullet rearing phase remains poorly understood. This study evaluated whether dietary DON exposure exacerbates the severity of Eimeria infection and delays recovery in growing pullets. A total of 288 Hy-Line W36 pullets (4-wk-old) were fed either a control diet containing 2.5 mg/kg DON or a naturally contaminated diet containing 14-15 mg/kg DON for 14 d. Birds were then sham‑dosed or orally inoculated with E. acervulina (50 000 oocysts), E. maxima (10 000) and E. tenella (10 000) in a 2 × 2 factorial design. Growth performance, gut permeability, intestinal morphology, jejunal tight‑junction and mucin gene expression, cecal tonsil cytokine profiles, T‑cell subsets, and hepatic redox indices were analyzed at 6 and 14 days post inoculation (DPI). DON alone did not depress weight gain; however, when coupled with Eimeria challenge it reduced feed intake by an additional 3 % (P = 0.038) and numerically aggravated intestinal lesions. The Eimeria challenge reduced body weight by 15 % at 6 DPI and 8 % at 14 DPI (P < 0.001), increased gut permeability and disrupted intestinal architecture (P < 0.001). Eimeria also damaged gut barrier integrity and induced Th1‑biased inflammation by downregulating JAM2, OCLN, ZO1 and MUC2 while upregulating CLDN1, IFN‑γ and IL‑10 (P < 0.05). DON independently downregulated jejunal MUC2 and upregulated IL‑1β. The interaction delayed mucosal repair and immune dysregulation by further upregulating CLDN1 at 14 DPI (P = 0.004) and splenic CD4⁺ cells at 6 DPI (P = 0.003). Hepatic redox indices were independently affected by Eimeria at 6 and 14 DPI, whereas DON at 14 DPI. In conclusion, diets containing 14-15 mg/kg DON negatively affected the immune response and jejunal MUC2 expression with minimal adverse effects on growth in non-challenged pullets. However, when Eimeria infection was present, DON delayed gut repair and shifted immune balance toward inflammation. Therefore, routine mycotoxin surveillance and mitigation in pullet feeds are important, especially in cage‑free systems where Eimeria spp. often circulate subclinically, to prevent downstream negative effects on laying performance and profitability.
期刊介绍:
First self-published in 1921, Poultry Science is an internationally renowned monthly journal, known as the authoritative source for a broad range of poultry information and high-caliber research. The journal plays a pivotal role in the dissemination of preeminent poultry-related knowledge across all disciplines. As of January 2020, Poultry Science will become an Open Access journal with no subscription charges, meaning authors who publish here can make their research immediately, permanently, and freely accessible worldwide while retaining copyright to their work. Papers submitted for publication after October 1, 2019 will be published as Open Access papers.
An international journal, Poultry Science publishes original papers, research notes, symposium papers, and reviews of basic science as applied to poultry. This authoritative source of poultry information is consistently ranked by ISI Impact Factor as one of the top 10 agriculture, dairy and animal science journals to deliver high-caliber research. Currently it is the highest-ranked (by Impact Factor and Eigenfactor) journal dedicated to publishing poultry research. Subject areas include breeding, genetics, education, production, management, environment, health, behavior, welfare, immunology, molecular biology, metabolism, nutrition, physiology, reproduction, processing, and products.