{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,18]],"date-time":"2026-04-18T08:51:28Z","timestamp":1776502288529,"version":"3.51.2"},"reference-count":54,"publisher":"American Veterinary Medical Association (AVMA)","issue":"8","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["ajvr"],"published-print":{"date-parts":[[2015,8]]},"abstract":"<jats:title>Abstract<\/jats:title>\n<jats:p><jats:bold>OBJECTIVE<\/jats:bold> To evaluate the effects of dietary nonphytate phosphorus (NPP) content on ileal lymphocyte subpopulations and cytokine expression in the cecal tonsils and spleen of hens that were or were not inoculated with <jats:italic>Salmonella<\/jats:italic> Typhimurium.<\/jats:p>\n<jats:p><jats:bold>ANIMALS<\/jats:bold> 64 <jats:italic>Salmonella<\/jats:italic>-free hens.<\/jats:p>\n<jats:p><jats:bold>PROCEDURES<\/jats:bold> Hens were fed a diet with 0.22% (control; n = 32) or 0.42% (high-P; 32) NPP for 6 weeks and then orally inoculated with <jats:italic>S<\/jats:italic> Typhimurium (5 \u00d7 10<jats:sup>7<\/jats:sup> CFUs) or PBSS. Tissues were obtained from 8 <jats:italic>S<\/jats:italic> Typhimurium\u2013inoculated and 8 PBSS-inoculated hens from each group at 2 and 7 days postinoculation (DPI). Percentages of ileal CD4+ and CD8+ lymphocytes were determined by flow cytometry. Cytokine mRNA expression was determined by quantitative real-time PCR assays.<\/jats:p>\n<jats:p><jats:bold>RESULTS<\/jats:bold> For <jats:italic>S<\/jats:italic> Typhimurium\u2013inoculated hens, plasma parathyroid hormone concentration was significantly increased and 1,25-dihydroxyvitamin D<jats:sub>3<\/jats:sub> concentration was decreased in hens fed the high-P diet, compared with values in hens fed the control diet. <jats:italic>Salmonella<\/jats:italic> Typhimurium inoculation caused an increase in the percentage of ileal CD8+ lymphocytes and the expression of interleukin (IL)-1\u03b2, IL-6, IL-8, interferon-\u03b3, IL-12, and IL-18 in the cecal tonsils and spleen and a decrease in the expression of IL-4 and IL-10 in the cecal tonsils. Hens fed the high-P diet had significantly increased splenic expression of interferon-\u03b3 at 2 DPI and IL-1\u03b2, IL-6, IL-12, and IL-18 at 7 DPI, compared with hens fed the control diet.<\/jats:p>\n<jats:p><jats:bold>CONCLUSIONS AND CLINICAL RELEVANCE<\/jats:bold> Results suggested there was a T-helper 1 cytokine reaction in the cecal tonsils and spleen of <jats:italic>S<\/jats:italic> Typhimurium\u2013inoculated hens, and dietary NPP content altered calcium regulation hormone concentrations and affected splenic cytokine expression.<\/jats:p>","DOI":"10.2460\/ajvr.76.8.710","type":"journal-article","created":{"date-parts":[[2015,7,24]],"date-time":"2015-07-24T14:02:01Z","timestamp":1437746521000},"page":"710-718","source":"Crossref","is-referenced-by-count":9,"title":["Effect of dietary nonphytate phosphorus content on ileal lymphocyte subpopulations and cytokine expression in the cecal tonsils and spleen of laying hens that were or were not orally inoculated with Salmonella Typhimurium"],"prefix":"10.2460","volume":"76","author":[{"given":"Shi P.","family":"Bai","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yong","family":"Huang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yu H.","family":"Luo","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lei L.","family":"Wang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xue M.","family":"Ding","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jian P.","family":"Wang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Qiu F.","family":"Zeng","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ke Y.","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1272","reference":[{"key":"ref1","series-title":"Basic animal nutrition and feeding","first-page":"125","author":"Pond","year":"2005"},{"key":"ref2","series-title":"Nutrient requirements of poultry","first-page":"19","year":"1994"},{"key":"ref3","series-title":"Poult Sci","doi-asserted-by":"publisher","first-page":"748","DOI":"10.1093\/ps\/79.5.748","article-title":"Nonphytate phosphorus requirement of laying hens with and without phytase on a phase feeding program","volume":"79","author":"Keshavarz","year":"2000"},{"key":"ref4","series-title":"Poult Sci","doi-asserted-by":"publisher","first-page":"224","DOI":"10.1093\/ps\/79.2.224","article-title":"The effects of dietary available phosphorus levels and phytase on performance of young and older laying hens","volume":"79","author":"Boling","year":"2000"},{"key":"ref5","series-title":"Poult Sci","doi-asserted-by":"publisher","first-page":"757","DOI":"10.1093\/ps\/84.5.757","article-title":"Hy-Line W-36 and Hy-Line W-98 laying hens respond similarly to dietary phosphorus levels","volume":"84","author":"Snow","year":"2005"},{"key":"ref6","series-title":"Fish Shellfish Immunol","doi-asserted-by":"publisher","first-page":"159","DOI":"10.1016\/S1050-4648(02)00155-9","article-title":"The effect of dietary phosphorus deficiency on the immune responses of European whitefish (Coregonus lavaretus L.)","volume":"15","author":"Jokinen","year":"2003"},{"key":"ref7","series-title":"J Anim Sci","doi-asserted-by":"publisher","first-page":"413","DOI":"10.2527\/2001.792413x","article-title":"Dietary phosphorus and an inflammatory challenge affect performance and immune function of weanling pigs","volume":"79","author":"Kegley","year":"2001"},{"key":"ref8","series-title":"Salmonella enterica serovar Enteritidis in humans and animals: epidemiology, pathogenesis and control","first-page":"183","article-title":"Contamination of eggs and poultry meat with Salmonella enterica serovar Enteritidis","author":"Humphrey","year":"1999"},{"key":"ref9","series-title":"J Nutr","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1093\/jn\/84.2.191","article-title":"Influence of dietary factors upon Salmonella typhimurium infection in the guinea pig","volume":"84","author":"Nabb","year":"1964"},{"key":"ref10","series-title":"Proc Soc Exp Biol Med","doi-asserted-by":"publisher","first-page":"953","DOI":"10.3181\/00379727-141-36909","article-title":"Effect of dietary phosphorus on blood phosphorus and leukocyte levels in experimental salmonellosis","volume":"141","author":"Doak","year":"1972"},{"key":"ref11","series-title":"Life Sci","doi-asserted-by":"publisher","first-page":"959","DOI":"10.1016\/0024-3205(73)90086-6","article-title":"Effect of dietary phosphorus on reticuloendothelial clearance of Salmonella organisms in endotoxin treated guinea pigs","volume":"13","author":"Doak","year":"1973"},{"key":"ref12","series-title":"Avian Pathol","doi-asserted-by":"publisher","first-page":"102","DOI":"10.1080\/03079450600597535","article-title":"Heterophil cytokine mRNA profiles from genetically distinct lines of chickens with differential heterophil-mediated innate immune responses","volume":"35","author":"Swaggerty","year":"2006"},{"key":"ref13","series-title":"Microbiology","doi-asserted-by":"publisher","first-page":"3217","DOI":"10.1099\/00221287-146-12-3217","article-title":"Differential cytokine expression in avian cells in response to invasion by Salmonella typhimurium, Salmonella enteritidis and Salmonella gallinarum","volume":"146","author":"Kaiser","year":"2000"},{"key":"ref14","series-title":"Poult Sci","doi-asserted-by":"publisher","first-page":"1907","DOI":"10.1093\/ps\/85.11.1907","article-title":"Cytokine expression in chicken peripheral blood mononuclear cells after in vitro exposure to Salmonella enterica serovar Enteritidis","volume":"85","author":"Kaiser","year":"2006"},{"key":"ref15","series-title":"Avian Dis","doi-asserted-by":"publisher","first-page":"396","DOI":"10.1637\/8642-020309-Reg.1","article-title":"Induction of CXC chemokine messenger-RNA expression in chicken oviduct epithelial cells by Salmonella enterica serovar Enteritidis via the type three secretion system-1","volume":"53","author":"Li","year":"2009"},{"key":"ref16","series-title":"Infect Immun","doi-asserted-by":"publisher","first-page":"2152","DOI":"10.1128\/IAI.72.4.2152-2159.2004","article-title":"Rapid expression of chemokines and proinflammatory cytokines in newly hatched chickens infected with Salmonella enterica serovar Typhimurium","volume":"72","author":"Withanage","year":"2004"},{"key":"ref17","series-title":"Infect Immun","doi-asserted-by":"publisher","first-page":"5173","DOI":"10.1128\/IAI.73.8.5173-5182.2005","article-title":"Cytokine and chemokine responses associated with clearance of a primary Salmonella enterica serovar Typhimurium infection in the chicken and in protective immunity to rechallenge","volume":"73","author":"Withanage","year":"2005"},{"key":"ref18","series-title":"Infect Immun","doi-asserted-by":"publisher","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"},{"key":"ref19","series-title":"Microbes Infect","doi-asserted-by":"publisher","first-page":"1191","DOI":"10.1016\/S1286-4579(01)01479-4","article-title":"Cytokines in host defense against Salmonella","volume":"3","author":"Eckmann","year":"2001"},{"key":"ref20","series-title":"Zentralbl Veterinarmed B","first-page":"459","article-title":"Experimental oral infection of specific pathogen-free laying hens and cocks with Salmonella Enteritidis strains","volume":"42","author":"Methner","year":"1995"},{"key":"ref21","series-title":"Res Vet Sci","doi-asserted-by":"publisher","first-page":"716","DOI":"10.1016\/j.rvsc.2011.12.018","article-title":"Analysis of immune-related gene expression in chicken peripheral blood mononuclear cells following Salmonella enterica serovar Enteritidis infection in vitro","volume":"93","author":"Pan","year":"2012"},{"key":"ref22","series-title":"Vet Immunol Immunopathol","doi-asserted-by":"publisher","first-page":"259","DOI":"10.1016\/j.vetimm.2006.08.006","article-title":"Changes in immune-related gene expression and intestinal lymphocyte subpopulations following Eimeria maxima infection of chickens","volume":"114","author":"Hong","year":"2006"},{"key":"ref23","series-title":"Nucleic Acids Res","doi-asserted-by":"publisher","first-page":"e45","DOI":"10.1093\/nar\/29.9.e45","article-title":"A new mathematical model for relative quantification in real-time RT-PCR","volume":"29","author":"Pfaffl","year":"2001"},{"key":"ref24"},{"key":"ref25","series-title":"J Clin Invest","doi-asserted-by":"publisher","first-page":"1603","DOI":"10.1172\/JCI115755","article-title":"Role of monokines in the metabolic effects of endotoxin","volume":"89","author":"Adi","year":"1992"},{"key":"ref26","series-title":"J Anim Sci","doi-asserted-by":"publisher","first-page":"1514","DOI":"10.2527\/1997.7561514x","article-title":"Time course of increased plasma cytokines, cortisol, and urea nitrogen in pigs following intraperitoneal injection of lipopolysaccharide","volume":"75","author":"Webel","year":"1997"},{"key":"ref27","series-title":"J Vet Med A Physiol Pathol Clin Med","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1111\/j.1439-0442.2006.00804.x","article-title":"The influence of intramammary lipopolysaccharide infusion on serum Ca, P, vitamin D, cytokines and cortisol concentrations in lactating sows","volume":"53","author":"Wang","year":"2006"},{"key":"ref28","series-title":"Nord Vet Med","first-page":"406","article-title":"Effect of E. coli ectotoxin on calcium and phosphate concentration in serum of dairy cows","volume":"36","author":"Sandstedt","year":"1984"},{"key":"ref29","series-title":"Vet Immunol Immunopathol","doi-asserted-by":"publisher","first-page":"359","DOI":"10.1016\/S0165-2427(97)00082-2","article-title":"Analysis of splenic and thymic lymphocyte subpopulations in chickens infected with Salmonella enteritidis","volume":"59","author":"Sasai","year":"1997"},{"key":"ref30","series-title":"Vet Immunol Immunopathol","doi-asserted-by":"publisher","first-page":"143","DOI":"10.1016\/S0165-2427(00)00264-6","article-title":"Gamma\/delta T cell response of chickens after oral administration of attenuated and non-attenuated Salmonella typhimurium strains","volume":"78","author":"Berndt","year":"2001"},{"key":"ref31","series-title":"Poult Sci","doi-asserted-by":"publisher","first-page":"927","DOI":"10.3382\/ps.2007-00476","article-title":"Detection of T lymphocytes in intestine of broiler chicks treated with Lactobacillus spp. and challenged with Salmonella enterica serovar Enteritidis","volume":"87","author":"Noujaim","year":"2008"},{"key":"ref32","series-title":"Microb Pathog","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1016\/0882-4010(86)90029-X","article-title":"Independence of macrophage activation and expression of the alleles of the Ity (immunity to Typhimurium) locus","volume":"1","author":"Briles","year":"1986"},{"key":"ref33","series-title":"Microb Pathog","doi-asserted-by":"publisher","first-page":"473","DOI":"10.1006\/mpat.1993.1046","article-title":"Effect of late administration of anti-TNF alpha antibodies on a Salmonella infection in the mouse model","volume":"14","author":"Mastroeni","year":"1993"},{"key":"ref34","series-title":"Poult Sci","doi-asserted-by":"publisher","first-page":"1105","DOI":"10.3382\/ps.2007-00517","article-title":"Effects of phytate and phytase on the performance and immune function of broilers fed nutritionally marginal diets","volume":"87","author":"Liu","year":"2008"},{"key":"ref35","series-title":"Nephron","doi-asserted-by":"publisher","first-page":"212","DOI":"10.1159\/000185160","article-title":"In vitro effect of PTH on normal T cell functions","volume":"50","author":"Shasha","year":"1988"},{"key":"ref36","series-title":"Kidney Int","doi-asserted-by":"publisher","first-page":"1543","DOI":"10.1038\/ki.1990.147","article-title":"Effect of parathyroid hormone on human T cell activation","volume":"37","author":"Klinger","year":"1990"},{"key":"ref37","series-title":"Kidney Int","doi-asserted-by":"publisher","first-page":"379","DOI":"10.1038\/ki.1993.255","article-title":"Parathyroid hormone dependent T cell proliferation in uremic rats","volume":"44","author":"Lewin","year":"1993"},{"key":"ref38","series-title":"J Clin Invest","doi-asserted-by":"publisher","first-page":"657","DOI":"10.1172\/JCI111465","article-title":"1\u03b1, 25-dihydroxyvitamin D3 suppresses proliferation and immunoglobulin production by normal human peripheral blood mononuclear cells","volume":"74","author":"Lemire","year":"1984"},{"key":"ref39","series-title":"Science","doi-asserted-by":"publisher","first-page":"1438","DOI":"10.1126\/science.6427926","article-title":"1,25-dihydroxyvitamin D3: a novel immunoregulatory hormone","volume":"224","author":"Tsoukas","year":"1984"},{"key":"ref40","series-title":"Best Pract Res Clin Haematol","doi-asserted-by":"publisher","first-page":"509","DOI":"10.1016\/j.beha.2005.01.003","article-title":"Cytokines and signal transduction","volume":"18","author":"Hideshima","year":"2005"},{"key":"ref41","series-title":"J Interferon Cytokine Res","doi-asserted-by":"publisher","first-page":"73","DOI":"10.1089\/jir.2005.25.73","article-title":"IFN-gamma priming of chicken heterophils upregulates the expression of proinflammatory and Th1 cytokine mRNA following receptor-mediated phagocytosis of Salmonella enterica serovar Enteritidis","volume":"25","author":"Kogut","year":"2005"},{"key":"ref42","series-title":"Microbiol Immunol","doi-asserted-by":"publisher","first-page":"224","DOI":"10.1111\/j.1348-0421.2009.00109.x","article-title":"Cytokines profiles in chickens infected with virulent and avirulent Marek's disease viruses: interferon-gamma is a key factor in the protection of Marek's disease by vaccination","volume":"53","author":"Kano","year":"2009"},{"key":"ref43","series-title":"J Leukoc Biol","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1189\/jlb.0603252","article-title":"Interferon-gamma: an overview of signals, mechanisms and functions","volume":"75","author":"Schroder","year":"2004"},{"key":"ref44","series-title":"Leuk Lymphoma","doi-asserted-by":"publisher","first-page":"427","DOI":"10.3109\/10428199809050903","article-title":"The regulation and biological activity of interleukin 12","volume":"29","author":"Lee","year":"1998"},{"key":"ref45","series-title":"Annu Rev Immunol","doi-asserted-by":"publisher","first-page":"423","DOI":"10.1146\/annurev.immunol.19.1.423","article-title":"Interleukin-18 regulates both Th1 and Th2 responses","volume":"19","author":"Nakanishi","year":"2001"},{"key":"ref46","series-title":"APMIS","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1111\/j.1699-0463.1995.tb01092.x","article-title":"Role of interferons and other cytokines in the regulation of the immune response","volume":"103","author":"Belardelli","year":"1995"},{"key":"ref47","series-title":"Nat Rev Immunol","doi-asserted-by":"publisher","first-page":"23","DOI":"10.1038\/nri978","article-title":"Alternative activation of macrophages","volume":"3","author":"Gordon","year":"2003"},{"key":"ref48","series-title":"Nat Rev Immunol","doi-asserted-by":"publisher","first-page":"425","DOI":"10.1038\/nri2097","article-title":"(H)1 cells control themselves by producing interleukin-10","volume":"7","author":"O'Garra","year":"2007"},{"key":"ref49","series-title":"Vaccine","doi-asserted-by":"publisher","first-page":"7637","DOI":"10.1016\/j.vaccine.2012.10.020","article-title":"Humoral and cellular immune response generated by different vaccine programs before and after Salmonella Enteritidis challenge in chickens","volume":"30","author":"Penha Filho","year":"2012"},{"key":"ref50","series-title":"Vet Microbiol","doi-asserted-by":"publisher","first-page":"225","DOI":"10.1016\/j.vetmic.2007.06.026","article-title":"Cytokine gene expression in chicken cecal tonsils following treatment with probiotics and Salmonella infection","volume":"126","author":"Haghighi","year":"2008"},{"key":"ref51","series-title":"Dev Comp Immunol","doi-asserted-by":"publisher","first-page":"52","DOI":"10.1016\/j.dci.2006.04.001","article-title":"Breed effect on early cytokine mRNA expression in spleen and cecum of chickens with and without Salmonella Enteritidis infection","volume":"31","author":"Cheeseman","year":"2007"},{"key":"ref52","series-title":"J Immunol","doi-asserted-by":"publisher","first-page":"4974","DOI":"10.4049\/jimmunol.167.9.4974","article-title":"1alpha, 25-dihydroxyvitamin D3 has a direct effect on naive CD4(1) T cells to enhance the development of Th2 cells","volume":"167","author":"Boonstra","year":"2001"},{"key":"ref53","series-title":"Diabetes","doi-asserted-by":"publisher","first-page":"1301","DOI":"10.2337\/diabetes.49.8.1301","article-title":"1alpha, 25-dihydroxyvitamin D3 induces an autoantigen-specific T-helper 1\/T-helper 2 immune shift in NOD mice immunized with GAD65 (p524\u2013543)","volume":"49","author":"Overbergh","year":"2000"},{"key":"ref54","series-title":"Clin Immunol Immunopathol","doi-asserted-by":"publisher","first-page":"286","DOI":"10.1016\/0090-1229(92)90159-L","article-title":"Parathyroid hormone inhibits immunoglobulin production without affecting cell growth in human B cells","volume":"65","author":"Jiang","year":"1992"}],"container-title":["American Journal of Veterinary Research"],"original-title":[],"link":[{"URL":"https:\/\/avmajournals.avma.org\/view\/journals\/ajvr\/76\/8\/ajvr.76.8.710.xml","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/avmajournals.avma.org\/downloadpdf\/journals\/ajvr\/76\/8\/ajvr.76.8.710.xml","content-type":"text\/html","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/avmajournals.avma.org\/downloadpdf\/journals\/ajvr\/76\/8\/ajvr.76.8.710.xml","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,3,7]],"date-time":"2025-03-07T12:36:44Z","timestamp":1741351004000},"score":1,"resource":{"primary":{"URL":"https:\/\/avmajournals.avma.org\/view\/journals\/ajvr\/76\/8\/ajvr.76.8.710.xml"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2015,8]]},"references-count":54,"journal-issue":{"issue":"8"},"URL":"https:\/\/doi.org\/10.2460\/ajvr.76.8.710","relation":{},"ISSN":["0002-9645"],"issn-type":[{"value":"0002-9645","type":"print"}],"subject":[],"published":{"date-parts":[[2015,8]]}}}