{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,7]],"date-time":"2026-09-07T18:50:27Z","timestamp":1788807027911,"version":"build-2803163510"},"reference-count":59,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,5,10]],"date-time":"2022-05-10T00:00:00Z","timestamp":1652140800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Nutr."],"abstract":"<jats:p><jats:italic>Salmonella enterica<\/jats:italic> serovar Enteritidis (SE) is one of the most common pathogens associated with poultry health and foodborne Salmonellosis worldwide. The gut plays a pivotal role in inhibiting SE transintestinal transmission and contaminating poultry products. The nutritional status of vitamin D (VD) is involved in gut health apart from bone health. However, the impact of VD<jats:sub>3<\/jats:sub> nutritional status on the gut health of <jats:italic>Salmonella<\/jats:italic>-challenged hens is rarely investigated. This study investigated the impact and possible mechanisms of VD<jats:sub>3<\/jats:sub> nutritional status on the gut health of hens challenged with SE. Hens were fed basal diets with either 0 (deficient) or 3000 IU (sufficient) VD<jats:sub>3<\/jats:sub>\/kg of diet, respectively. After 10 weeks of feeding, half of the hens were orally inoculated with either SE (1 \u00d7 10<jats:sup>9<\/jats:sup> CFU \/bird). Results indicated that VD<jats:sub>3<\/jats:sub> sufficiency reversed the disruptive effects on the laying performance of hens caused by <jats:italic>Salmonella<\/jats:italic> challenge or VD<jats:sub>3<\/jats:sub> insufficiency by promoting VD<jats:sub>3<\/jats:sub> metabolism. In addition, VD<jats:sub>3<\/jats:sub> sufficiency ameliorated gut injury induced by either <jats:italic>Salmonella<\/jats:italic> or VD<jats:sub>3<\/jats:sub> deficiency, shown by reducing <jats:italic>Salmonella<\/jats:italic> load and histopathological scores, suppressing TLR4-mediated inflammatory responses, and increasing expression of TJs along with decreasing pro-apoptotic protein expression and the number of TUNEL-positive cells in the jejunum. Besides, VD<jats:sub>3<\/jats:sub> enriched the abundance of probiotics, such as <jats:italic>Lactobacillus<\/jats:italic> and <jats:italic>Bacilli<\/jats:italic>, and restored the balance of gut microflora. Collectively, dietary VD<jats:sub>3<\/jats:sub> sufficient supplementation could alleviate <jats:italic>Salmonella<\/jats:italic> or VD<jats:sub>3<\/jats:sub> deficiency-induced intestinal damage of hens <jats:italic>via<\/jats:italic> modulating intestinal immune, barrier function, apoptosis along with gut microbiota composition, revealing that VD<jats:sub>3<\/jats:sub> could act as a novel nutritional strategy defending <jats:italic>Salmonella<\/jats:italic> invasion in hens.<\/jats:p>","DOI":"10.3389\/fnut.2022.888580","type":"journal-article","created":{"date-parts":[[2022,5,10]],"date-time":"2022-05-10T09:45:42Z","timestamp":1652175942000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":13,"title":["Vitamin D3 Nutritional Status Affects Gut Health of Salmonella-Challenged Laying Hens"],"prefix":"10.3389","volume":"9","author":[{"given":"Fangshen","family":"Guo","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yanqiang","family":"Geng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Waseem","family":"Abbas","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenrui","family":"Zhen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuiqing","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuechuan","family":"Huang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuming","family":"Guo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qiugang","family":"Ma","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhong","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,5,10]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"504","DOI":"10.14202\/vetworld.2019.504-521","article-title":"A review of Salmonella enterica with particular focus on the pathogenicity and virulence factors, host specificity and antimicrobial resistance including multidrug resistance","volume":"12","author":"Jajere","year":"2019","journal-title":"Vet World."},{"key":"B2","doi-asserted-by":"publisher","first-page":"573","DOI":"10.1016\/j.ijbiomac.2016.01.031","article-title":"Yeast \u03b2-d-glucans induced antimicrobial peptide expressions against Salmonella infection in broiler chickens","volume":"85","author":"Shao","year":"2016","journal-title":"Int J Biol Macromol."},{"key":"B3","doi-asserted-by":"publisher","first-page":"2654","DOI":"10.3382\/ps\/pey119","article-title":"Effect of dietary Bacillus coagulans supplementation on growth performance and immune responses of broiler chickens challenged by Salmonella enteritidis","volume":"97","author":"Zhen","year":"2018","journal-title":"Poult Sci."},{"key":"B4","doi-asserted-by":"publisher","first-page":"306","DOI":"10.1186\/1756-0500-4-306","article-title":"MLVA polymorphism of Salmonella enterica subspecies isolated from humans, animals, and food in Cambodia","volume":"4","author":"van Cuyck","year":"2011","journal-title":"BMC Res Notes."},{"key":"B5","doi-asserted-by":"publisher","first-page":"1615","DOI":"10.3855\/jidc.5393","article-title":"Similarities between Salmonella Enteritidis isolated from humans and captive wild animals in South Africa","volume":"8","author":"Smith","year":"2014","journal-title":"J Infect Dev Ctries"},{"key":"B6","doi-asserted-by":"publisher","first-page":"e87933","DOI":"10.1371\/journal.pone.0087933","article-title":"Risk factors for human salmonellosis originating from pigs, cattle, broiler chickens and egg laying hens: a combined case-control and source attribution analysis","volume":"9","author":"Mughini-Gras","year":"2014","journal-title":"PloS one"},{"key":"B7","doi-asserted-by":"publisher","DOI":"10.2903\/j.efsa.2017.5077","volume":"15","year":"2017","journal-title":"Efsa J"},{"key":"B8","doi-asserted-by":"publisher","first-page":"e05596","DOI":"10.2903\/j.efsa.2019.5596","article-title":"Salmonella control in poultry flocks and its public health impact","volume":"17","author":"Koutsoumanis","year":"2019","journal-title":"Efsa J."},{"key":"B9","doi-asserted-by":"publisher","first-page":"774","DOI":"10.4315\/0362-028x-73.4.774","article-title":"Salmonella in chicken: current and developing strategies to reduce contamination at farm level","volume":"73","author":"Vandeplas","year":"2010","journal-title":"J Food Prot."},{"key":"B10","doi-asserted-by":"publisher","first-page":"217","DOI":"10.3389\/fmicb.2014.00217","article-title":"Antibiotic alternatives: the substitution of antibiotics in animal husbandry?","volume":"5","author":"Cheng","year":"2014","journal-title":"Front Microbiol"},{"key":"B11","doi-asserted-by":"publisher","first-page":"4465","DOI":"10.3382\/ps\/pez282","article-title":"Effect of dietary probiotics and prebiotics on the performance of broiler chickens","volume":"98","author":"Al-Khalaifa","year":"2019","journal-title":"Poult Sci."},{"key":"B12","doi-asserted-by":"publisher","first-page":"196","DOI":"10.1016\/j.psj.2020.09.065","article-title":"Effect of benzoic acid on production performance, egg quality, intestinal morphology, and cecal microbial community of laying hens","volume":"100","author":"Gong","year":"2021","journal-title":"Poult Sci."},{"key":"B13","doi-asserted-by":"publisher","first-page":"62","DOI":"10.16\/j.jnutbio.2015.11.018","article-title":"Fermented milk with probiotic Lactobacillus rhamnosus S1K3 (MTCC5957) protects mice from salmonella by enhancing immune and non-immune protection mechanisms at intestinal mucosal level","volume":"30","author":"Kemgang T","year":"2016","journal-title":"J Nutr Biochem"},{"key":"B14","doi-asserted-by":"publisher","first-page":"100930","DOI":"10.1016\/j.psj.2020.12.027","article-title":"Centennial review: effects of vitamins A, D, E, and C on the chicken immune system","volume":"100","author":"Shojadoost","year":"2021","journal-title":"Poult Sci."},{"key":"B15","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1159\/000486536","volume":"72","author":"Gil","year":"2018","journal-title":"Vitamin D: Classic and Novel Actions Ann Nutr Metab."},{"key":"B16","doi-asserted-by":"publisher","first-page":"62","DOI":"10.5414\/alx1430e","article-title":"Immunomodulation by vitamin D","volume":"2","author":"Worm","year":"2018","journal-title":"Allergol Select."},{"key":"B17","doi-asserted-by":"publisher","first-page":"108942","DOI":"10.1016\/j.jnutbio.2022.108942","article-title":"Vitamin D3 and zinc synergistically induce regulatory T cells and suppress interferon-\u03b3 production in mixed lymphocyte culture","volume":"102","author":"Schmitt","year":"2022","journal-title":"J Nutr Biochem."},{"key":"B18","doi-asserted-by":"publisher","first-page":"627","DOI":"10.3389\/fimmu.2016.00627","article-title":"Role of vitamin D in the hygiene hypothesis: the interplay between vitamin D, Vitamin D receptors, gut microbiota, and immune response","volume":"7","author":"Clark","year":"2016","journal-title":"Front Immunol."},{"key":"B19","doi-asserted-by":"publisher","first-page":"e2032","DOI":"10.1002\/rmv.2032","article-title":"The interplay between vitamin D and viral infections","volume":"29","author":"Teymoori-Rad","year":"2019","journal-title":"Rev Med Virol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"2300","DOI":"10.3390\/molecules25102300","article-title":"Effects of vitamin D supplementation on inflammation, colonic cell kinetics, and microbiota in colitis: a review","volume":"25","author":"Garcia","year":"2020","journal-title":"Molecules"},{"key":"B21","doi-asserted-by":"publisher","first-page":"105663","DOI":"10.1016\/j.jsbmb.2020.105663","article-title":"Vitamin D and intestinal homeostasis: barrier, microbiota, and immune modulation","volume":"200","author":"Fakhoury","year":"2020","journal-title":"J Steroid Biochem Mol Biol."},{"key":"B22","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fimmu.2019.00001","article-title":"Vitamin D Is Required for ILC3 Derived IL-22 and Protection from citrobacter rodentium infection","volume":"10","author":"Lin","year":"2019","journal-title":"Front Immunol."},{"key":"B23","doi-asserted-by":"publisher","first-page":"364","DOI":"10.3382\/ps\/pez502","article-title":"Effects of additional dosage of vitamin D(3), vitamin D(2), and 25-hydroxyvitamin D(3) on calcium and phosphorus utilization, egg quality and bone mineralization in laying hens","volume":"99","author":"Adhikari","year":"2020","journal-title":"Poult Sci."},{"key":"B24","doi-asserted-by":"publisher","DOI":"10.1155\/2012\/189096","article-title":"CD8+ T-Cell deficiency, epstein-barr virus infection, vitamin D deficiency, and steps to autoimmunity: a unifying hypothesis","author":"Pender","year":"2012","journal-title":"Autoimmune Dis"},{"key":"B25","doi-asserted-by":"publisher","first-page":"101382","DOI":"10.1016\/j.psj.2021.101382","article-title":"Effects of the in ovo injection of vitamin D(3) and 25-hydroxyvitamin D(3) in Ross 708 broilers subsequently challenged with coccidiosis I performance, meat yield and intestinal lesion incidence(1,2,3)","volume":"100","author":"Fatemi","year":"2021","journal-title":"Poult Sci."},{"key":"B26","doi-asserted-by":"publisher","first-page":"48","DOI":"10.1016\/j.jsbmb.2014.11.020","article-title":"Vitamin D deficiency in pregnant women impairs regulatory T cell function","volume":"147","author":"Vijayendra Chary","year":"2015","journal-title":"J Steroid Biochem Mol Biol."},{"key":"B27","doi-asserted-by":"publisher","first-page":"10256","DOI":"10.1038\/s41598-019-46578-x","article-title":"Pretreatment with probiotic Enterococcus faecium NCIMB 11181 ameliorates necrotic enteritis-induced intestinal barrier injury in broiler chickens","volume":"9","author":"Wu","year":"2019","journal-title":"Sci Rep"},{"key":"B28","doi-asserted-by":"publisher","first-page":"2460","DOI":"10.1093\/bioinformatics\/btq461","article-title":"Search and clustering orders of magnitude faster than BLAST","volume":"26","author":"Edgar","year":"2010","journal-title":"Bioinformatics."},{"key":"B29","doi-asserted-by":"publisher","first-page":"R60","DOI":"10.1186\/gb-2011-12-6-r60","article-title":"Metagenomic biomarker discovery and explanation","volume":"12","author":"Segata","year":"2011","journal-title":"Genome Biol."},{"key":"B30","doi-asserted-by":"publisher","first-page":"814","DOI":"10.1038\/nbt.2676","article-title":"Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences","volume":"9","author":"Morgan","year":"2013","journal-title":"Nature biotechnol"},{"key":"B31","doi-asserted-by":"publisher","first-page":"1911","DOI":"10.1210\/jc.2011-0385","article-title":"Evaluation, treatment, and prevention of vitamin D deficiency: an Endocrine Society clinical practice guideline","volume":"96","author":"Holick","year":"2011","journal-title":"J Clin Endocrinol Metab."},{"key":"B32","doi-asserted-by":"publisher","first-page":"58","DOI":"10.1186\/s12986-018-0293-8","article-title":"Dietary vitamin D(3) supplementation protects laying hens against lipopolysaccharide-induced immunological stress","volume":"15","author":"Geng","year":"2018","journal-title":"Nutr Metab (Lond)."},{"key":"B33","doi-asserted-by":"publisher","first-page":"2608","DOI":"10.1016\/j.psj.2019.12.054","article-title":"Effect of dietary 25-hydroxycholecalciferol supplementation and high stocking density on performance, egg quality, and tibia quality in laying hens","volume":"99","author":"Wang","year":"2020","journal-title":"Poult Sci."},{"key":"B34","doi-asserted-by":"publisher","first-page":"1087S","DOI":"10.1093\/ajcn\/87.4.1087S","article-title":"Blood biomarkers of Vitamin D status","volume":"87","author":"Zerwekh","year":"2008","journal-title":"Am J Clin Nutr"},{"key":"B35","doi-asserted-by":"publisher","first-page":"7226","DOI":"10.3389\/fimmu.2021.627226","article-title":"Association between vitamin D exposure and head and neck cancer: a systematic review with meta-analysis","volume":"12","author":"Pu","year":"2021","journal-title":"Front Immunol"},{"key":"B36","unstructured":"Vitamin D protects against oxidative stress, inflammation and hepatorenal damage induced by acute paracetamol toxicity in rat31021\n            El-BoshyM\n            BaSalamah MA\n            AhmadJ\n            IdrisS\n            MahbubA\n            Abdelghany AH\n          31255668Free Radical Biology and Medicine.1412019"},{"key":"B37","doi-asserted-by":"publisher","first-page":"2427","DOI":"10.1007\/s10620-015-3620-1","article-title":"Vitamin D status is associated with intestinal inflammation as measured by fecal calprotectin in crohn's disease in clinical remission","volume":"60","author":"Raftery","year":"2015","journal-title":"Dig Dis Sci."},{"key":"B38","doi-asserted-by":"publisher","first-page":"481","DOI":"10.1002\/iid3.408","article-title":"Active vitamin D3 attenuates the severity of Salmonella colitis in mice by orchestrating innate immunity","volume":"9","author":"Huang","year":"2021","journal-title":"Immun Inflamm Dis."},{"key":"B39","doi-asserted-by":"publisher","first-page":"445","DOI":"10.1053\/j.gastro.2020.08.060","article-title":"AGA clinical practice update on management of inflammatory bowel disease in elderly patients: expert review","volume":"160","author":"Ananthakrishnan","year":"2021","journal-title":"Gastroenterology."},{"key":"B40","doi-asserted-by":"publisher","first-page":"799","DOI":"10.1038\/nri2653","article-title":"Intestinal mucosal barrier function in health and disease","volume":"9","author":"Turner","year":"2009","journal-title":"Nat Rev Immunol."},{"key":"B41","doi-asserted-by":"publisher","first-page":"487","DOI":"10.1111\/j.1365-2184.2012.00845.x","article-title":"Programmed cell death pathways in cancer: a review of apoptosis, autophagy and programmed necrosis","volume":"90","author":"Ouyang","year":"2012","journal-title":"Cell Prolif."},{"key":"B42","doi-asserted-by":"publisher","first-page":"1235","DOI":"10.3382\/ps\/pey443","article-title":"Effect of probiotics on fecal excretion, colonization in internal organs and immune gene expression in the ileum of laying hens challenged with Salmonella Enteritidis","volume":"98","author":"Adhikari","year":"2019","journal-title":"Poult Sci."},{"key":"B43","doi-asserted-by":"publisher","first-page":"3230","DOI":"10.4049\/jimmunol.1100058","article-title":"Activation of TLR2 enhances tight junction barrier in epidermal keratinocytes","volume":"187","author":"Yuki","year":"2011","journal-title":"J Immunol."},{"key":"B44","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1016\/j.aninu.2020.10.003","article-title":"Insights into host-microbe interaction: What can we do for the swine industry?","volume":"7","author":"Fan","year":"2021","journal-title":"Animal Nutrition."},{"key":"B45","doi-asserted-by":"publisher","first-page":"181","DOI":"10.7762\/cnr.2021.10.3.181","article-title":"Vitamin D and the gut microbiota: a narrative literature review","volume":"10","author":"Tangestani","year":"2021","journal-title":"Clin Nutr Res."},{"key":"B46","doi-asserted-by":"publisher","first-page":"3378","DOI":"10.3390\/nu13103378","article-title":"The association between vitamin D and gut microbiota: a systematic review of human studies","volume":"13","author":"Bellerba","year":"2021","journal-title":"Nutrients."},{"key":"B47","doi-asserted-by":"publisher","first-page":"2888","DOI":"10.3390\/nu11122888","article-title":"Effect of vitamin D supplementation on faecal microbiota: a randomised clinical trial","volume":"11","author":"Naderpoor","year":"2019","journal-title":"Nutrients"},{"key":"B48","doi-asserted-by":"publisher","first-page":"76","DOI":"10.1016\/j.metabol.2017.01.007","article-title":"Franco-de-Moraes AC, Folchetti LG, Ferreira SR. Gut microbiota interactions with the immunomodulatory role of vitamin D in normal individuals","volume":"69","author":"Luthold","year":"2017","journal-title":"Metabolism."},{"key":"B49","doi-asserted-by":"publisher","first-page":"111817","DOI":"10.1016\/j.biopha.2021.111817","article-title":"Immunomodulatory roles of microbiota-derived short-chain fatty acids in bacterial infections","volume":"141","author":"Ranjbar","year":"2021","journal-title":"Biomed Pharmacotherapy."},{"key":"B50","doi-asserted-by":"publisher","first-page":"710","DOI":"10.1002\/clc.23195","article-title":"Dysbiotic gut microbes may contribute to hypertension by limiting vitamin D production","volume":"42","author":"Zuo","year":"2019","journal-title":"Clin Cardiol."},{"key":"B51","doi-asserted-by":"publisher","DOI":"10.1002\/mnfr.202000188","article-title":"Microbial metabolites, postbiotics, and intestinal epithelial function","author":"Mayorgas","year":"2020","journal-title":"Mol Nutr Food Res"},{"key":"B52","doi-asserted-by":"publisher","first-page":"225","DOI":"10.1111\/1751-2980.12591","article-title":"Vitamin D administration leads to a shift of the intestinal bacterial composition in Crohn's disease patients, but not in healthy controls","volume":"19","author":"Sch\u00e4ffler","year":"2018","journal-title":"J Dig Dis."},{"key":"B53","doi-asserted-by":"publisher","DOI":"10.1016\/S0016-5085(11)60075-9","article-title":"Probiotic regulation of vitamin D receptor in intestinal inflammation","author":"Yoon","year":"2011","journal-title":"Gastroenterology"},{"key":"B54","doi-asserted-by":"publisher","first-page":"609","DOI":"10.1080\/07388551.2021.1873239","article-title":"Biotechnological applications of Bacillus licheniformis","volume":"41","author":"Muras","year":"2021","journal-title":"Crit Rev Biotechnol"},{"key":"B55","doi-asserted-by":"publisher","first-page":"18","DOI":"10.1016\/j.biochi.2015.03.007","article-title":"Multiple ways to regulate translation initiation in bacteria: mechanisms, regulatory circuits, dynamics","volume":"114","author":"Duval","year":"2015","journal-title":"Biochimie."},{"key":"B56","doi-asserted-by":"publisher","first-page":"347","DOI":"10.1111\/jam.13347","article-title":"Phylogenetic and functional characterization of the distal intestinal microbiome of rainbow trout Oncorhynchus mykiss from both farm and aquarium settings","volume":"122","author":"Lyons","year":"2017","journal-title":"J App Microbiol"},{"key":"B57","doi-asserted-by":"publisher","first-page":"e0182426","DOI":"10.1371\/journal.pone.0182426","article-title":"Disruption in the cecal microbiota of chickens challenged with Clostridium perfringens and other factors was alleviated by Bacillus licheniformis supplementation","volume":"12","author":"Lin","year":"2017","journal-title":"PLoS ONE."},{"key":"B58","doi-asserted-by":"publisher","first-page":"88","DOI":"10.1016\/j.freeradbiomed.2015.01.001","article-title":"A novel enzyme with spermine oxidase properties in bovine liver mitochondria: Identification and kinetic characterization","volume":"81","author":"Bonaiuto","year":"2015","journal-title":"Free Rad Biol Med."},{"key":"B59","doi-asserted-by":"publisher","first-page":"1024","DOI":"10.1038\/s41385-018-0019-2","article-title":"Aryl hydrocarbon receptor and intestinal immunity","volume":"11","author":"Lamas","year":"2018","journal-title":"Mucosal Immunol"}],"container-title":["Frontiers in Nutrition"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnut.2022.888580\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,5,10]],"date-time":"2022-05-10T09:45:46Z","timestamp":1652175946000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnut.2022.888580\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,5,10]]},"references-count":59,"alternative-id":["10.3389\/fnut.2022.888580"],"URL":"https:\/\/doi.org\/10.3389\/fnut.2022.888580","relation":{},"ISSN":["2296-861X"],"issn-type":[{"value":"2296-861X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,5,10]]},"article-number":"888580"}}