{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,28]],"date-time":"2026-09-28T05:35:36Z","timestamp":1790573736897,"version":"4.1.0"},"reference-count":79,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2022,10,29]],"date-time":"2022-10-29T00:00:00Z","timestamp":1667001600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"the Canadian Poultry Research Council (Poultry Science Cluster Project 1373 Activity 14)","award":["2019F101R"],"award-info":[{"award-number":["2019F101R"]}]},{"name":"Results Driven Agriculture Research","award":["2019F101R"],"award-info":[{"award-number":["2019F101R"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Salmonella enterica serovar Typhimurium incites salmonellosis in many different species including chickens and human beings. Acute salmonellosis was studied in neonatal broiler chicks by orally inoculating 2-day-old chicks with S. Typhimurium DT104. The temporal impact of disease (1, 2, and 4 days post-inoculation) on the structure and function of the enteric microbiota, on the bird\u2019s immune response in the ileum, cecum, and colon, and on the metabolome of digesta, breast muscle, liver, serum, and hippocampus were examined. Substantive histopathologic changes were observed in the small and large intestine, including the colon of chicks inoculated with S. Typhimurium, and increased in magnitude over the experimental time period. A variety of inflammatory genes (IFN\u03b3, IL8, IL10, INOS, MIP1\u03b2, TGF\u03b22, TLR4, and TLR15) were temporally regulated. In addition, the metabolome of ileal digesta, breast muscle, liver, serum, and hippocampus was temporally altered in infected chicks. Although the structure of bacterial communities in digesta was not affected by S. Typhimurium infection, metabolomic analysis indicated that the function of the microbiota was changed. Collectively, the study findings demonstrate that infection of neonatal chicks by S. Typhimurium imparts a temporal and systemic impact on the host, affecting the immune system, the metabolome, and the function of the enteric microbiota.<\/jats:p>","DOI":"10.3390\/pathogens11111257","type":"journal-article","created":{"date-parts":[[2022,10,30]],"date-time":"2022-10-30T09:01:42Z","timestamp":1667120502000},"page":"1257","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":14,"title":["Infection by Salmonella enterica Serovar Typhimurium DT104 Modulates Immune Responses, the Metabolome, and the Function of the Enteric Microbiota in Neonatal Broiler Chickens"],"prefix":"10.3390","volume":"11","author":[{"given":"Danisa M.","family":"Bescucci","sequence":"first","affiliation":[{"name":"Lethbridge Research and Development Centre, Agriculture and Agri-Food Canada, Lethbridge, AB T1J 4B1, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9934-9856","authenticated-orcid":false,"given":"Tony","family":"Montina","sequence":"additional","affiliation":[{"name":"Department of Chemistry and Biochemistry, University of Lethbridge, Lethbridge, AB T1K 3M4, Canada"},{"name":"Southern Alberta Genome Sciences Centre, University of Lethbridge, Lethbridge, AB T1K 3M4, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Valerie F.","family":"Boras","sequence":"additional","affiliation":[{"name":"Chinook Regional Hospital, Alberta Health Services, Lethbridge, AB T1J 1W5, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"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":[[2022,10,29]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","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":"ref_2","doi-asserted-by":"crossref","first-page":"259","DOI":"10.14745\/ccdr.v47i56a03","article-title":"Salmonella enterica serovars associated with bacteremia in Canada, 2006\u20132019","volume":"47","author":"Tamber","year":"2021","journal-title":"Can. Commun. Dis. Rep."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1046\/j.1462-2920.2001.00213.x","article-title":"The chicken, the egg and Salmonella enteritidis","volume":"3","year":"2001","journal-title":"Environ. Microbiol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"5993","DOI":"10.1128\/IAI.00695-07","article-title":"Chicken cecum immune response to Salmonella enterica serovars of different levels of invasiveness","volume":"75","author":"Berndt","year":"2007","journal-title":"Infect. Immun."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"9327","DOI":"10.1007\/s00253-020-10887-3","article-title":"Transcriptome profiling analysis of caeca in chicks challenged with Salmonella Typhimurium reveals differential expression of genes involved in host mucosal immune response","volume":"104","author":"Khan","year":"2020","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"194","DOI":"10.1016\/S0034-5288(18)30685-4","article-title":"Observations on the pathogenesis of experimental Salmonella Typhimurium infection in chickens","volume":"42","author":"Barrow","year":"1987","journal-title":"Res. Vet. Sci."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Rychlik, I. (2020). Composition and function of chicken gut microbiota. Animals, 10.","DOI":"10.3390\/ani10010103"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1113\/jphysiol.1980.sp013366","article-title":"Effects of dietary intake of sodium chloride on sugar and amino acid transport across isolated hen colon","volume":"305","author":"Lind","year":"1980","journal-title":"J. Physiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1111\/j.1469-7793.2001.00197.x","article-title":"Aldosterone mediates the changes in hexose transport induced by low sodium intake in chicken distal intestine","volume":"535","author":"Garriga","year":"2001","journal-title":"J. Physiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"284","DOI":"10.1080\/08830185.2019.1659258","article-title":"Chicken toll-like receptors and their significance in immune response and disease resistance","volume":"38","author":"Nawab","year":"2019","journal-title":"Int. Rev. Immunol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"736739","DOI":"10.3389\/fvets.2021.736739","article-title":"Biological function of short-chain fatty acids and its regulation on intestinal health of poultry","volume":"8","author":"Liu","year":"2021","journal-title":"Front. Vet. Sci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"790","DOI":"10.1038\/nri3535","article-title":"Microbiota-mediated colonization resistance against intestinal pathogens","volume":"13","author":"Buffie","year":"2013","journal-title":"Nat. Rev. Immunol."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Zaytsoff, S.J.M., Montina, T., Boras, V.F., Brassard, J., Moote, P.E., Uwiera, R.R.E., and Inglis, G.D. (2022). Microbiota transplantation in day-old broiler chickens ameliorates necrotic enteritis via modulation of the intestinal microbiota and host immune responses. Pathogens, 11.","DOI":"10.3390\/pathogens11090972"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Stanley, D., Geier, M.S., Hughes, R.J., Denman, S.E., and Moore, R.J. (2013). Highly variable microbiota development in the chicken gastrointestinal tract. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0084290"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"235","DOI":"10.3389\/fmicb.2018.00235","article-title":"Host and environmental factors affecting the intestinal microbiota in chickens","volume":"9","author":"Kers","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"61","DOI":"10.3389\/fvets.2015.00061","article-title":"Salmonella enterica serovars Enteritidis infection alters the indigenous microbiota diversity in young layer chicks","volume":"2","author":"Mon","year":"2015","journal-title":"Front. Vet. Sci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.aninu.2015.02.004","article-title":"Towards the control of necrotic enteritis in broiler chickens with in-feed antibiotics phasing-out worldwide","volume":"1","author":"Wu","year":"2015","journal-title":"Anim. Nutr."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1007\/s11306-016-1105-7","article-title":"NMR-based metabolic characterization of chicken tissues and biofluids: A model for avian research","volume":"12","author":"Mappley","year":"2016","journal-title":"Metabolomics"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"4809","DOI":"10.1038\/s41598-020-60892-9","article-title":"Integrative analysis of gut microbiome and metabolites revealed novel mechanisms of intestinal Salmonella carriage in chicken","volume":"10","author":"Mon","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"345","DOI":"10.3382\/ps\/pev349","article-title":"AMPK and mTOR: Sensors and regulators of immunometabolic changes during Salmonella infection in the chicken","volume":"95","author":"Kogut","year":"2016","journal-title":"Poult. Sci."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1186\/1297-9716-44-35","article-title":"Salmonella enterica Typhimurium infection causes metabolic changes in chicken muscle involving AMPK, fatty acid and insulin\/mTOR signaling","volume":"44","author":"Arsenault","year":"2013","journal-title":"Vet. Res."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"2645","DOI":"10.1016\/j.psj.2019.12.037","article-title":"Research Note: Effect of organic acid mixture on growth performance and Salmonella Typhimurium colonization in broiler chickens","volume":"99","author":"Adhikari","year":"2020","journal-title":"Poult. Sci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"e01569-20","DOI":"10.1128\/AEM.01569-20","article-title":"Salmonella enterica serovar Typhimurium temporally modulates the enteric microbiota and host responses to overcome colonization resistance in swine","volume":"86","author":"Bescucci","year":"2020","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_24","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_25","doi-asserted-by":"crossref","first-page":"1116","DOI":"10.1128\/IAI.71.3.1116-1124.2003","article-title":"Allelic variation in TLR4 is linked to susceptibility to Salmonella enterica serovar Typhimurium infection in chickens","volume":"71","author":"Leveque","year":"2003","journal-title":"Infect. Immun."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1016\/S0165-2427(02)00153-8","article-title":"Involvement of lipopolysaccharide related receptors and nuclear factor kappa B in differential expression of inducible nitric oxide synthase in chicken macrophages from different genetic backgrounds","volume":"88","author":"Dil","year":"2002","journal-title":"Vet. Immunol. Immunopathol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1006\/mpat.1994.1015","article-title":"Heterophils are decisive components in the early responses of chickens to Salmonella enteritidis infections","volume":"16","author":"Kogut","year":"1994","journal-title":"Microb. Pathog."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1046\/j.1462-5822.2000.00051.x","article-title":"Salmonella Typhimurium mutants that downregulate phagocyte nitric oxide production","volume":"2","author":"Eriksson","year":"2000","journal-title":"Cell. Microbiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1051\/vetres:2008043","article-title":"Early immune response following Salmonella enterica subspecies enterica serovar Typhimurium infection in porcine jejunal gut loops","volume":"40","author":"Meurens","year":"2009","journal-title":"Vet. Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1016\/j.vetimm.2008.05.015","article-title":"Reduced nitric oxide production and iNOS mRNA expression in IFN-gamma-stimulated chicken macrophages transfected with iNOS siRNAs","volume":"125","author":"Cheeseman","year":"2008","journal-title":"Vet. Immunol. Immunopathol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"4922","DOI":"10.1128\/IAI.00417-06","article-title":"Caspase-1-mediated activation of interleukin-1beta (IL-1beta) and IL-18 contributes to innate immune defenses against Salmonella enterica serovar Typhimurium infection","volume":"74","author":"Raupach","year":"2006","journal-title":"Infect. Immun."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1692","DOI":"10.1128\/IAI.74.3.1692-1698.2006","article-title":"Induction of a novel chicken toll-like receptor following Salmonella enterica serovar Typhimurium infection","volume":"74","author":"Higgs","year":"2006","journal-title":"Infect. Immun."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1016\/j.exppara.2013.01.002","article-title":"Upregulation of chicken TLR4, TLR15 and MyD88 in heterophils and monocyte-derived macrophages stimulated with Eimeria tenella in vitro","volume":"133","author":"Zhou","year":"2013","journal-title":"Exp. Parasitol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1186\/1297-9716-44-99","article-title":"Diacylated lipopeptide from Mycoplasma synoviae mediates TLR15 induced innate immune responses","volume":"44","author":"Oven","year":"2013","journal-title":"Vet. Res."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"2839","DOI":"10.1128\/IAI.71.5.2839-2858.2003","article-title":"Pretreatment of mice with streptomycin provides a Salmonella enterica Serovar Typhimurium colitis model that allows analysis of both pathogen and host","volume":"71","author":"Barthel","year":"2003","journal-title":"Infect. Immun."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"484","DOI":"10.1111\/j.1439-0442.2004.00588.x","article-title":"Expression of inflammatory cytokines (TNF-alpha, IL-1, IL-6 and IL-8) in colon of pigs naturally infected with Salmonella typhimurium and S. choleraesuis","volume":"50","author":"Cho","year":"2003","journal-title":"J. Vet. Med. A Physiol. Pathol. Clin. Med."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"343","DOI":"10.4162\/nrp.2015.9.4.343","article-title":"Butyrate modulates bacterial adherence on LS174T human colorectal cells by stimulating mucin secretion and MAPK signaling pathway","volume":"9","author":"Jung","year":"2015","journal-title":"Nutr. Res. Pract."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"943","DOI":"10.3382\/ps.2008-00484","article-title":"Butyric acid-based feed additives help protect broiler chickens from Salmonella enteritidis infection","volume":"88","author":"Ordonez","year":"2009","journal-title":"Poult. Sci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1080\/03079451003610586","article-title":"Control of Clostridium perfringens-induced necrotic enteritis in broilers by target-released butyric acid, fatty acids and essential oils","volume":"39","author":"Timbermont","year":"2010","journal-title":"Avian Pathol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1111\/j.1365-2036.2007.03562.x","article-title":"Review article: The role of butyrate on colonic function","volume":"27","author":"Hamer","year":"2008","journal-title":"Aliment. Pharmacol. Ther."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1136\/gut.46.4.493","article-title":"Butyrate and glucose metabolism by colonocytes in experimental colitis in mice","volume":"46","author":"Ahmad","year":"2000","journal-title":"Gut"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"154","DOI":"10.3389\/fcimb.2016.00154","article-title":"Age-related differences in the luminal and mucosa-associated gut microbiome of broiler chickens and shifts associated with Campylobacter jejuni infection","volume":"6","author":"Awad","year":"2016","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1080\/0007166041668879","article-title":"Defaecation and weight of the gastrointestinal tract contents after feed and water withdrawal in broilers","volume":"45","author":"Warriss","year":"2004","journal-title":"Br. Poult. Sci."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1002\/jez.1402520507","article-title":"Relationship of cecal and colonic motility to diet, habitat, and cecal anatomy in several avian species","volume":"3","author":"Duke","year":"1989","journal-title":"J. Exp. Zool. Suppl."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"985","DOI":"10.3389\/fmicb.2015.00985","article-title":"Salmonella Typhimurium exploits inflammation to its own advantage in piglets","volume":"6","author":"Chirullo","year":"2015","journal-title":"Front. Microbiol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"426","DOI":"10.1038\/nature09415","article-title":"Gut inflammation provides a respiratory electron acceptor for Salmonella","volume":"467","author":"Winter","year":"2010","journal-title":"Nature"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.mib.2017.07.003","article-title":"Dysbiotic Proteobacteria expansion: A microbial signature of epithelial dysfunction","volume":"39","author":"Litvak","year":"2017","journal-title":"Curr. Opin. Microbiol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"410","DOI":"10.1038\/s41579-018-0029-9","article-title":"Best practices for analysing microbiomes","volume":"16","author":"Knight","year":"2018","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Deatherage Kaiser, B.L., Li, J., Sanford, J.A., Kim, Y.M., Kronewitter, S.R., Jones, M.B., Peterson, C.T., Peterson, S.N., Frank, B.C., and Purvine, S.O. (2013). A multi-omic view of host-pathogen-commensal interplay in Salmonella-mediated intestinal infection. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0067155"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"6431","DOI":"10.1007\/s00253-015-6543-z","article-title":"Increased intracellular calcium level and impaired nutrient absorption are important pathogenicity traits in the chicken intestinal epithelium during Campylobacter jejuni colonization","volume":"99","author":"Awad","year":"2015","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_51","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_52","doi-asserted-by":"crossref","first-page":"3547","DOI":"10.1038\/s41467-020-17402-2","article-title":"Lactate released by inflammatory bone marrow neutrophils induces their mobilization via endothelial GPR81 signaling","volume":"11","author":"Bhattacharya","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"a040535","DOI":"10.1101\/cshperspect.a040535","article-title":"Glycolysis","volume":"13","author":"Chandel","year":"2021","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"2515S","DOI":"10.1093\/jn\/131.9.2515S","article-title":"Why is L-glutamine metabolism important to cells of the immune system in health, postinjury, surgery or infection?","volume":"131","author":"Newsholme","year":"2001","journal-title":"J. Nutr."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1080\/00071660902806947","article-title":"Dietary glutamine supplementation improves growth performance, meat quality and colour stability of broilers under heat stress","volume":"50","author":"Dai","year":"2009","journal-title":"Br. Poult. Sci."},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Brown, C.L.J., Zaytsoff, S.J.M., Montina, T., and Inglis, G.D. (2021). Corticosterone-mediated physiological stress alters liver, kidney, and breast muscle metabolomic profiles in chickens. Animals, 11.","DOI":"10.3390\/ani11113056"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1186\/s13099-020-00386-1","article-title":"The absence of murine cathelicidin-related antimicrobial peptide impacts host responses enhancing Salmonella enterica serovar Typhimurium infection","volume":"12","author":"Bescucci","year":"2020","journal-title":"Gut Pathog."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/S1043-4526(09)57003-9","article-title":"Carnosine and its possible roles in nutrition and health","volume":"57","author":"Hipkiss","year":"2009","journal-title":"Adv. Food Nutr. Res."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1016\/j.neubiorev.2019.10.004","article-title":"Glutamate receptors in domestication and modern human evolution","volume":"108","author":"Boeckx","year":"2020","journal-title":"Neurosci. Biobehav. Rev."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1196\/annals.1296.004","article-title":"Role of GABA and glutamate circuitry in hypothalamo-pituitary-adrenocortical stress integration","volume":"1018","author":"Herman","year":"2004","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1016\/j.physbeh.2015.02.027","article-title":"Metabotropic glutamate receptor-mediated signaling dampens the HPA axis response to restraint stress","volume":"150","author":"Evanson","year":"2015","journal-title":"Physiol. Behav."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"873","DOI":"10.1152\/physrev.00041.2006","article-title":"Physiology and neurobiology of stress and adaptation: Central role of the brain","volume":"87","author":"McEwen","year":"2007","journal-title":"Physiol. Rev."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1016\/j.tvjl.2005.11.007","article-title":"The role of glutamate in central nervous system health and disease\u2014A review","volume":"173","author":"Platt","year":"2007","journal-title":"Vet. J."},{"key":"ref_64","unstructured":"Canadian Council on Animal Care (2009). CCAC Guidelines on: The Care and Use of Farm Animals in Research, Teaching and Testing, Canadian Council on Animal Care."},{"key":"ref_65","first-page":"e54161","article-title":"Improved Swiss-rolling technique for intestinal tissue preparation for immunohistochemical and immunofluorescent analyses","volume":"113","author":"Bialkowska","year":"2016","journal-title":"J. Vis. Exp."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"e00243-17","DOI":"10.1128\/mSphere.00243-17","article-title":"Butyrate supplementation at high concentrations alters enteric bacterial communities and reduces intestinal inflammation in mice infected with Citrobacter rodentium","volume":"2","author":"Jiminez","year":"2017","journal-title":"mSphere"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"638","DOI":"10.1002\/jsfa.2740360803","article-title":"Determination of ethanol, volatile fatty acids, lactic and succinic acids in fermentation liquids by gas chromatography","volume":"36","author":"Playne","year":"1985","journal-title":"J. Sci. Food Agric."},{"key":"ref_68","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_69","unstructured":"RStudio (2018). RStudio: Integrated Development for R, RStudio, Inc."},{"key":"ref_70","first-page":"569","article-title":"Rapid quantification of Salmonella in seafood by real-time PCR assay","volume":"20","author":"Kumar","year":"2010","journal-title":"J. Microbiol. Biotechnol."},{"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":"581","DOI":"10.1038\/nmeth.3869","article-title":"DADA2: High-resolution sample inference from Illumina amplicon data","volume":"13","author":"Callahan","year":"2016","journal-title":"Nat. Methods"},{"key":"ref_74","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":"2010","journal-title":"Metabolomics"},{"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":"1","author":"Veselkov","year":"2009","journal-title":"Anal. Chem."},{"key":"ref_76","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_77","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_78","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_79","doi-asserted-by":"crossref","unstructured":"Pang, Z., Chong, J., Li, S., and Xia, J. (2020). MetaboAnalystR 3.0: Toward an optimized workflow for global metabolomics. 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