{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,26]],"date-time":"2026-10-26T19:52:29Z","timestamp":1793044349493,"version":"4.5.0"},"reference-count":85,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2022,8,26]],"date-time":"2022-08-26T00:00:00Z","timestamp":1661472000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100012236","name":"Alberta Agriculture and Forestry","doi-asserted-by":"publisher","award":["2019F101R"],"award-info":[{"award-number":["2019F101R"]}],"id":[{"id":"10.13039\/100012236","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100012236","name":"Alberta Agriculture and Forestry","doi-asserted-by":"publisher","award":["2019H001R"],"award-info":[{"award-number":["2019H001R"]}],"id":[{"id":"10.13039\/100012236","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Canadian Poultry Research Council (Poultry Science Cluster Project 1373 Activity 14)","award":["2019F101R"],"award-info":[{"award-number":["2019F101R"]}]},{"name":"Canadian Poultry Research Council (Poultry Science Cluster Project 1373 Activity 14)","award":["2019H001R"],"award-info":[{"award-number":["2019H001R"]}]},{"name":"Alberta Innovates (CD-60)","award":["2019F101R"],"award-info":[{"award-number":["2019F101R"]}]},{"name":"Alberta Innovates (CD-60)","award":["2019H001R"],"award-info":[{"award-number":["2019H001R"]}]},{"name":"Canadian Glycomics Network","award":["2019F101R"],"award-info":[{"award-number":["2019F101R"]}]},{"name":"Canadian Glycomics Network","award":["2019H001R"],"award-info":[{"award-number":["2019H001R"]}]},{"name":"lberta Chicken Producers","award":["2019F101R"],"award-info":[{"award-number":["2019F101R"]}]},{"name":"lberta Chicken Producers","award":["2019H001R"],"award-info":[{"award-number":["2019H001R"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>A microbiota transplant (MT) originating from mature adult chicken ceca and propagated in bioreactors was administered to day-old broiler chicks to ascertain the degree to which, and how, the MT affects Clostridium perfringens (Cp)-incited necrotic enteritis (NE). Using a stress predisposition model of NE, birds administered the MT and challenged with Cp showed fewer necrotic lesions, and exhibited a substantially higher \u03b1- and \u03b2-diversity of bacteria in their jejunum and ceca. Birds challenged with Cp and not administered the MT showed decreased Lactobacillus and increased Clostridium sensu strico 1 in the jejunum. In ceca, Megamonas, a genus containing butyrate-producing bacteria, was only present in birds administered the MT, and densities of this genus were increased in birds challenged with Cp. Metabolite profiles in cecal digesta were altered in birds administered the MT and challenged with the pathogen; 59 metabolites were differentially abundant following MT treatment, and the relative levels of short chain fatty acids, butyrate, valerate, and propionate, were decreased in birds with NE. Birds administered the MT and challenged with Cp showed evidence of enhanced restoration of intestinal barrier functions, including elevated mRNA of MUC2B, MUC13, and TJP1. Likewise, birds administered the MT exhibited higher mRNA of IL2, IL17A, and IL22 at 2-days post-inoculation with Cp, indicating that these birds were better immunologically equipped to respond to pathogen challenge. Collectively, study findings demonstrated that administering a MT containing a diverse mixture of microorganisms to day-old birds ameliorated NE in broilers by increasing bacterial diversity and promoting positive immune responses.<\/jats:p>","DOI":"10.3390\/pathogens11090972","type":"journal-article","created":{"date-parts":[[2022,8,29]],"date-time":"2022-08-29T22:53:42Z","timestamp":1661813622000},"page":"972","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":21,"title":["Microbiota Transplantation in Day-Old Broiler Chickens Ameliorates Necrotic Enteritis via Modulation of the Intestinal Microbiota and Host Immune Responses"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8939-5277","authenticated-orcid":false,"given":"Sarah J. 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E.","family":"Uwiera","sequence":"additional","affiliation":[{"name":"Department of Agricultural, Food and Nutritional Science, University of Alberta, Edmonton, AB T6G 2R3, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1769-7863","authenticated-orcid":false,"given":"G. Douglas","family":"Inglis","sequence":"additional","affiliation":[{"name":"Lethbridge Research and Development Centre, Agriculture and Agri-Food Canada, Lethbridge, AB T1J 4B1, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,8,26]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Bojanova, D.P., and Bordenstein, S.R. (2016). Fecal transplants: What is being transferred?. PLoS Biol., 14.","DOI":"10.1371\/journal.pbio.1002503"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1111\/cei.13397","article-title":"Immunological mechanisms underpinning faecal microbiota transplantation for the treatment of inflammatory bowel disease","volume":"199","author":"Quraishi","year":"2020","journal-title":"Clin. Exp. Immunol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1016\/j.vetimm.2018.11.002","article-title":"Fecal microbiota transplantation as a tool to treat and reduce susceptibility to disease in animals","volume":"206","author":"Niederwerder","year":"2018","journal-title":"Vet. Immunol. Immunopathol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1080\/03079457.2016.1150587","article-title":"Necrotic enteritis predisposing factors in broiler chickens","volume":"45","author":"Moore","year":"2016","journal-title":"Avian Pathol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1016\/j.anifeedsci.2005.12.003","article-title":"Potential strategies for controlling necrotic enteritis in broiler chickens in post-antibiotic era","volume":"129","author":"Dahiya","year":"2006","journal-title":"Anim. Feed Sci. Technol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s13568-020-00989-6","article-title":"Probiotics mitigating subclinical necrotic enteritis (SNE) as potential alternatives to antibiotics in poultry","volume":"10","author":"Khalique","year":"2020","journal-title":"AMB Express"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1592","DOI":"10.3389\/fimmu.2017.01592","article-title":"Probiotic enhanced intestinal immunity in broilers against subclinical necrotic enteritis","volume":"8","author":"Wang","year":"2017","journal-title":"Front. Immunol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1111\/j.1472-765X.2004.01474.x","article-title":"In Vivo characterization of Lactobacillus johnsonii FI9785 for use as a defined competitive exclusion agent against bacterial pathogens in poultry","volume":"38","author":"Narbad","year":"2004","journal-title":"Lett. Appl. Microbiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"4185","DOI":"10.1128\/AEM.71.8.4185-4190.2005","article-title":"Inhibition of Clostridium perfringens by a novel strain of Bacillus subtilis isolated from the gastrointestinal tracts of healthy chickens","volume":"71","author":"Teo","year":"2005","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1186\/s13568-017-0439-5","article-title":"Preventing subclinical necrotic enteritis through Lactobacillus johnsonii BS15 by ameliorating lipid metabolism and intestinal microflora in broiler chickens","volume":"7","author":"Qing","year":"2017","journal-title":"AMB Express"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1038\/241210a0","article-title":"New aspects of Salmonella infection in broiler production","volume":"241","author":"Nurmi","year":"1973","journal-title":"Nature"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"627","DOI":"10.1080\/00071667308416073","article-title":"Prevention of the growth of Salmonella infantis in chicks by the flora of the alimentary tract of chickens","volume":"14","author":"Rantala","year":"1973","journal-title":"Br. Poult. Sci."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"e3587","DOI":"10.7717\/peerj.3587","article-title":"The time-course of broiler intestinal microbiota development after administration of cecal contents to incubating eggs","volume":"5","author":"Donaldson","year":"2017","journal-title":"PeerJ"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"e02330-17","DOI":"10.1128\/AEM.02330-17","article-title":"Fecal microbiota transplant from highly feed-efficient donors shows little effect on age-related changes in feed-efficiency-associated fecal microbiota from chickens","volume":"84","author":"Siegerstetter","year":"2018","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2750","DOI":"10.1038\/s41598-020-59125-w","article-title":"Early-life microbiota transplantation affects behavioural responses, serotonin and immune characteristics in chicken lines divergently selected on feather pecking","volume":"10","author":"Rodenburg","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_16","unstructured":"Price, K. (2022). Guts of Growth: To Clean or Not to Clean?, Canadian Poultry. Available online: https:\/\/www.canadianpoultrymag.com\/guts-of-growth-to-clean-or-not-to-clean\/."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"6816","DOI":"10.1128\/AEM.69.11.6816-6824.2003","article-title":"Diversity and succession of the intestinal bacterial community of the maturing broiler chicken","volume":"69","author":"Lu","year":"2003","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1111\/1574-6968.12608","article-title":"The chicken gastrointestinal microbiome","volume":"360","author":"Oakley","year":"2014","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"5880","DOI":"10.1128\/AEM.01616-15","article-title":"Effects of xylo-oligosaccharides on broiler chicken performance and microbiota","volume":"81","author":"Eeckhaut","year":"2015","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"101726","DOI":"10.1016\/j.psj.2022.101726","article-title":"A stress-induced model of acute necrotic enteritis in broiler chickens using dietary corticosterone administration","volume":"101","author":"Zaytsoff","year":"2022","journal-title":"Poult. Sci."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/j.vetmic.2012.03.032","article-title":"Changes in the caecal microflora of chickens following Clostridium perfringens challenge to induce necrotic enteritis","volume":"159","author":"Stanley","year":"2012","journal-title":"Vet. Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Stanley, D., Wu, S.-B., Rodgers, N., Swick, R., and Moore, R.J. (2014). Differential responses of cecal microbiota to fishmeal, Eimeria and Clostridium perfringens in a necrotic enteritis challenge model in chickens. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0104739"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"308","DOI":"10.1080\/03079457.2016.1152625","article-title":"Microbial shifts associated with necrotic enteritis","volume":"45","author":"Antonissen","year":"2016","journal-title":"Avian Pathol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"188","DOI":"10.1016\/j.vetmic.2014.01.007","article-title":"Two necrotic enteritis predisposing factors, dietary fishmeal and Eimeria infection, induce large changes in the caecal microbiota of broiler chickens","volume":"169","author":"Wu","year":"2014","journal-title":"Vet. Microbiol."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Zaytsoff, S.J.M., Uwiera, R.R.E., and Inglis, G.D. (2020). Physiological stress mediated by corticosterone administration alters intestinal bacterial communities and increases the relative abundance of Clostridium perfringens in the small intestine of chickens. Microorganisms, 8.","DOI":"10.3390\/microorganisms8101518"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Kubasova, T., Kollarcikova, M., Crhanova, M., Karasova, D., Cejkova, D., Sebkova, A., Matiasovicova, J., Faldynova, M., Pokorna, A., and Cizek, A. (2019). Contact with adult hen affects development of caecal microbiota in newly hatched chicks. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0212446"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Low, K.E., Xing, X., Moote, P.E., Inglis, G.D., Venketachalam, S., Hahn, M.G., King, M.L., Jones, C.Y., Jones, D.R., and Willats, W.G.T. (2020). Combinatorial glycomic analyses to direct cazyme discovery for the tailored degradation of canola meal non-starch dietary polysaccharides. Microorganisms, 8.","DOI":"10.3390\/microorganisms8121888"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"100069","DOI":"10.1016\/j.infpip.2020.100069","article-title":"Regulation, risk and safety of faecal microbiota transplant","volume":"2","author":"Merrick","year":"2020","journal-title":"Infect. Prev. Pract."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"114045","DOI":"10.1016\/j.jviromet.2020.114045","article-title":"Treatments of porcine fecal samples affect high-throughput virome sequencing results","volume":"289","author":"Gauthier","year":"2021","journal-title":"J. Virol. Methods"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"784","DOI":"10.3389\/fendo.2019.00784","article-title":"Gut Bacteriophage: Current understanding and challenges","volume":"10","author":"Sutton","year":"2019","journal-title":"Front. Endocrinol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/j.foodcont.2014.03.034","article-title":"Susceptibility of Clostridium perfringens to antimicrobials produced by lactic acid bacteria: Reuterin and nisin","volume":"44","author":"Garde","year":"2014","journal-title":"Food Control"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1155\/2013\/237921","article-title":"The role of cell surface architecture of lactobacilli in host-microbe interactions in the gastrointestinal tract","volume":"2013","author":"Sengupta","year":"2013","journal-title":"Mediat. Inflamm."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1007\/BF02046035","article-title":"Bacteroides hypermegas nov. spec","volume":"29","author":"Harrison","year":"1963","journal-title":"Antonie Van Leeuwenhoek"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Inglis, G.D., Wright, B.D., Sheppard, S.A., Abbott, D.W., Oryschak, M.A., and Montina, T. (2021). Expeller-pressed canola (Brassica napus) meal modulates the structure and function of the cecal microbiota, and alters the metabolome of the pancreas, liver, and breast muscle of broiler chickens. Animals, 11.","DOI":"10.3390\/ani11020577"},{"key":"ref_35","first-page":"979","article-title":"Bifidobacteria and butyrate-producing colon bacteria: Importance and strategies for their stimulation in the human gut","volume":"7","author":"Selak","year":"2016","journal-title":"Front. Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"729","DOI":"10.1038\/nrgastro.2013.180","article-title":"The gut as a sensory organ","volume":"10","author":"Furness","year":"2013","journal-title":"Nat. Rev. Gastroenterol. Hepatol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1080\/19490976.2015.1134082","article-title":"Formation of short chain fatty acids by the gut microbiota and their impact on human metabolism","volume":"7","author":"Morrison","year":"2016","journal-title":"Gut Microbes"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Sergeant, M., Constantinidou, C., Cogan, T.A., Bedford, M.R., Penn, C.W., and Pallen, M.J. (2014). Extensive microbial and functional diversity within the chicken cecal microbiome. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0091941"},{"key":"ref_39","first-page":"93","article-title":"The avian cecum: A review","volume":"107","author":"Clench","year":"1995","journal-title":"Wilson Bull."},{"key":"ref_40","first-page":"449","article-title":"Effects of dietary essential amino acid deficiencies on immunological variables in broiler chickens","volume":"83","author":"Konashi","year":"2000","journal-title":"Br. J. Nutr."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"2091","DOI":"10.1007\/s00726-017-2494-2","article-title":"The role of methionine on metabolism, oxidative stress, and diseases","volume":"49","author":"Li","year":"2017","journal-title":"Amino Acids"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1186\/s40104-021-00568-0","article-title":"Progress of amino acid nutrition for diet protein reduction in poultry","volume":"12","author":"Kidd","year":"2021","journal-title":"J. Anim. Sci. Biotechnol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"5074","DOI":"10.3382\/ps\/pez297","article-title":"Structural analysis of broiler chicken small intestinal mucin O-glycan modification by Clostridium perfringens","volume":"98","author":"MacMillan","year":"2019","journal-title":"Poult. Sci."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1038\/nrmicro2538","article-title":"Mucin dynamics and enteric pathogens","volume":"9","author":"McGuckin","year":"2011","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1007\/s00418-002-0432-0","article-title":"Microbial\u2013host interactions specifically control the glycosylation pattern in intestinal mouse mucosa","volume":"118","author":"Freitas","year":"2002","journal-title":"Histochem. Cell Biol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1007\/s005350050216","article-title":"Colonization of microflora in mice: Mucosal defense against luminal bacteria","volume":"34","author":"Fukushima","year":"1999","journal-title":"J. Gastroenterol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"L484","DOI":"10.1152\/ajplung.1996.271.3.L484","article-title":"Dexamethasone suppresses mucus production and MUC-2 and MUC-5AC gene expression by NCI-H292 cells","volume":"271","author":"Kai","year":"1996","journal-title":"Am. J. Physiol. Lung Cell. Mol. Physiol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1186\/s13099-020-00362-9","article-title":"Host responses to Clostridium perfringens challenge in a chicken model of chronic stress","volume":"12","author":"Zaytsoff","year":"2020","journal-title":"Gut Pathog."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Lind\u00e9n, S.K., Florin, T.H.J., and McGuckin, M.A. (2008). Mucin dynamics in intestinal bacterial infection. PLoS ONE, 3.","DOI":"10.1371\/journal.pone.0003952"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1335","DOI":"10.3382\/ps.2011-02062","article-title":"Quantitative analyses of genes associated with mucin synthesis of broiler chickens with induced necrotic enteritis","volume":"91","author":"Forder","year":"2012","journal-title":"Poult. Sci."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"557","DOI":"10.1038\/mi.2012.98","article-title":"MUC1 and MUC13 differentially regulate epithelial inflammation in response to inflammatory and infectious stimuli","volume":"6","author":"Sheng","year":"2013","journal-title":"Mucosal Immunol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1016\/j.molimm.2014.01.004","article-title":"Immune regulatory activities of fowlicidin-1, a cathelicidin host defense peptide","volume":"59","author":"Bommineni","year":"2014","journal-title":"Mol. Immunol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1684\/ejd.2011.1273","article-title":"Psychological stress regulates antimicrobial peptide expression by both glucocorticoid and beta-adrenergic mechanisms","volume":"21","author":"Man","year":"2011","journal-title":"Eur. J. Dermatol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1081","DOI":"10.3382\/ps.2011-01948","article-title":"Differential gene expression profiles of \u03b2-defensins in the crop, intestine, and spleen using a necrotic enteritis model in 2 commercial broiler chicken lines","volume":"91","author":"Hong","year":"2012","journal-title":"Poult. Sci."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"G218","DOI":"10.1152\/ajpgi.00095.2013","article-title":"Glucocorticoids regulate barrier function and claudin expression in intestinal epithelial cells via MKP-1","volume":"306","author":"Fischer","year":"2014","journal-title":"Am. J. Physiol. Gastrointest Liver Physiol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"L40","DOI":"10.1152\/ajplung.00299.2010","article-title":"Differential effects of claudin-3 and claudin-4 on alveolar epithelial barrier function","volume":"301","author":"Mitchell","year":"2011","journal-title":"Am. J. Physiol. Lung Cell. Mol. Physiol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1128\/CMR.00046-08","article-title":"Pathogen recognition and inflammatory signaling in innate immune defenses","volume":"22","author":"Mogensen","year":"2009","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"612","DOI":"10.1038\/ni.3742","article-title":"Interleukin 17 is a chief orchestrator of immunity","volume":"18","author":"Veldhoen","year":"2017","journal-title":"Nat. Immunol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"628","DOI":"10.1016\/j.immuni.2008.07.018","article-title":"Interleukin-17 promotes autoimmunity by triggering a positive-feedback loop via interleukin-6 induction","volume":"29","author":"Ogura","year":"2008","journal-title":"Immunity"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1080\/03079457.2010.508777","article-title":"Advances in avian immunology\u2014prospects for disease control: A review","volume":"39","author":"Kaiser","year":"2010","journal-title":"Avian Pathol."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1016\/S0145-305X(02)00076-9","article-title":"Establishment of immune competence in the avian GALT during the immediate post-hatch period","volume":"27","author":"Sklan","year":"2003","journal-title":"Dev. Comp. Immunol."},{"key":"ref_62","unstructured":"Roberts, A.P., and Mullany, P. (2016). Minibioreactor arrays (mbras) as a tool for studying C. difficile physiology in the presence of a complex community. Clostridium Difficile: Methods and Protocols, Methods in Molecular Biology, Springer Science + Business Media."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"2815","DOI":"10.1128\/IAI.01524-14","article-title":"Epidemic Clostridium difficile strains demonstrate increased competitive fitness compared to nonepidemic isolates","volume":"82","author":"Robinson","year":"2014","journal-title":"Infect. Immun."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1186\/s13099-016-0152-y","article-title":"Influence of pCP1NetB ancillary genes on the virulence of Clostridium perfringens poultry necrotic enteritis strain CP1","volume":"9","author":"Zhou","year":"2017","journal-title":"Gut Pathog."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1016\/j.anaerobe.2018.04.011","article-title":"Expansion of the Clostridium perfringens toxin-based typing scheme","volume":"53","author":"Rood","year":"2018","journal-title":"Anaerobe"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1186\/1297-9716-43-74","article-title":"The successful experimental induction of necrotic enteritis in chickens by Clostridium perfringens: A critical review","volume":"43","author":"Shojadoost","year":"2012","journal-title":"Vet. Res."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1016\/j.rvsc.2008.02.007","article-title":"Sub-clinical necrotic enteritis in broiler chickens: Novel etiological consideration based on ultra-structural and molecular changes in the intestinal tissue","volume":"85","author":"Olkowski","year":"2008","journal-title":"Res. Vet. Sci."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1080\/03079450701589118","article-title":"Quantification of gut lesions in a subclinical necrotic enteritis model","volume":"36","author":"Gholamiandehkordi","year":"2007","journal-title":"Avian Pathol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1292\/jvms.16-0500","article-title":"Experimental induction of necrotic enteritis in chickens by a netB-positive Japanese isolate of Clostridium perfringens","volume":"79","author":"To","year":"2017","journal-title":"J. Vet. Med. Sci."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"1117","DOI":"10.1093\/ajcn\/76.5.1117","article-title":"Selective growth of mucolytic bacteria including Clostridium perfringens in a neonatal piglet model of total parenteral nutrition","volume":"76","author":"Deplancke","year":"2002","journal-title":"Am. J. Clin. Nutr."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"5112","DOI":"10.1128\/AEM.01043-13","article-title":"Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform","volume":"79","author":"Kozich","year":"2013","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"852","DOI":"10.1038\/s41587-019-0209-9","article-title":"Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2","volume":"37","author":"Bolyen","year":"2019","journal-title":"Nat. Biotechnol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"D590","DOI":"10.1093\/nar\/gks1219","article-title":"The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools","volume":"41","author":"Quast","year":"2012","journal-title":"Nucleic Acids Res."},{"key":"ref_74","unstructured":"Anderson, M.J., Gorley, R.N., and Clarke, K.R. (2022, August 24). Permanova + for Primer. Guide to Software and Statistical Methods. ScienceOpen 2008. Available online: https:\/\/www.scienceopen.com\/document?vid=19bb860e-6a20-42d4-a081-a1f62bc8dfa1."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1021\/ac8011544","article-title":"Recursive segment-wise peak alignment of biological 1H NMR spectra for improved metabolic biomarker recovery","volume":"81","author":"Veselkov","year":"2009","journal-title":"Anal. Chem."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1007\/s11306-010-0242-7","article-title":"Dynamic adaptive binning: An improved quantification technique for NMR spectroscopic data","volume":"7","author":"Anderson","year":"2011","journal-title":"Metabolomics"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"4313","DOI":"10.1093\/bioinformatics\/bty528","article-title":"MetaboAnalystR: An R package for flexible and reproducible analysis of metabolomics data","volume":"34","author":"Chong","year":"2018","journal-title":"Bioinformatics"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"134","DOI":"10.1016\/j.ab.2010.02.005","article-title":"Statistical significance analysis of nuclear magnetic resonance-based metabonomics data","volume":"401","author":"Goodpaster","year":"2010","journal-title":"Anal. Biochem."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"1539","DOI":"10.1007\/s11306-015-0803-x","article-title":"Informative metabolites identification by variable importance analysis based on random variable combination","volume":"11","author":"Yun","year":"2015","journal-title":"Metabolomics"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"2342","DOI":"10.1093\/bioinformatics\/btq418","article-title":"MetPA: A web-based metabolomics tool for pathway analysis and visualization","volume":"26","author":"Xia","year":"2010","journal-title":"Bioinformatics"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"R19","DOI":"10.1186\/gb-2007-8-2-r19","article-title":"qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data","volume":"8","author":"Hellemans","year":"2007","journal-title":"Genome Biol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"e53781","DOI":"10.1371\/journal.pone.0053781","article-title":"Cloning, annotation and developmental expression of the chicken intestinal MUC2 gene","volume":"8","author":"Jiang","year":"2013","journal-title":"PLoS ONE"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1186\/2049-1891-3-15","article-title":"Tissue expression and developmental regulation of chicken cathelicidin antimicrobial peptides","volume":"3","author":"Achanta","year":"2012","journal-title":"J. Anim. Sci. Biotechnol."},{"key":"ref_84","unstructured":"Canadian-Council-on-Animal-Care (2022, August 24). Guidelines on: Laboratory Animal Facilities\u2014Characteristics, Design and Development. Available online: https:\/\/www.ccac.ca\/Documents\/Standards\/Guidelines\/Facilities.pdf."},{"key":"ref_85","unstructured":"Public Health Agency of Canada (2022, August 24). Canadian Biosafety Standard, (2nd edition), Available online: https:\/\/www.canada.ca\/en\/public-health\/services\/canadian-biosafety-standards-guidelines\/second-edition.html."}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/11\/9\/972\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T00:15:45Z","timestamp":1760141745000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/11\/9\/972"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,8,26]]},"references-count":85,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2022,9]]}},"alternative-id":["pathogens11090972"],"URL":"https:\/\/doi.org\/10.3390\/pathogens11090972","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,8,26]]}}}