{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,19]],"date-time":"2026-09-19T00:06:41Z","timestamp":1789776401214,"version":"4.0.1"},"reference-count":49,"publisher":"Elsevier BV","issue":"5","license":[{"start":{"date-parts":[[2025,5,1]],"date-time":"2025-05-01T00:00:00Z","timestamp":1746057600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2025,5,1]],"date-time":"2025-05-01T00:00:00Z","timestamp":1746057600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"},{"start":{"date-parts":[[2025,3,10]],"date-time":"2025-03-10T00:00:00Z","timestamp":1741564800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"DOI":"10.13039\/100020507","name":"KOSGEB","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100020507","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Poultry Science"],"published-print":{"date-parts":[[2025,5]]},"DOI":"10.1016\/j.psj.2025.105024","type":"journal-article","created":{"date-parts":[[2025,3,12]],"date-time":"2025-03-12T20:36:27Z","timestamp":1741811787000},"page":"105024","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":2,"title":["A novel trivalent inactivated Salmonella vaccine formulated with CpG ODNs to enhance the cellular immunity in chickens"],"prefix":"10.1016","volume":"104","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5527-7336","authenticated-orcid":false,"given":"Tamer","family":"Kahraman","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6568-2899","authenticated-orcid":false,"given":"Fuat Cem","family":"Yagci","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5878-8775","authenticated-orcid":false,"given":"Ahmet","family":"Ceylan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4550-9321","authenticated-orcid":false,"given":"Ali","family":"Calik","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0009-2358-0160","authenticated-orcid":false,"given":"Ibrahim Oguzhan","family":"Tarman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4536-2959","authenticated-orcid":false,"given":"Fadime","family":"Kiran","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.psj.2025.105024_bib0001","series-title":"Cellular and Molecular Immunology E-Book","author":"Abbas","year":"2014"},{"key":"10.1016\/j.psj.2025.105024_bib0002","doi-asserted-by":"crossref","first-page":"1041","DOI":"10.3390\/vaccines9091041","article-title":"A novel approach against Salmonella: a review of polymeric nanoparticle vaccines for broilers and layers","volume":"9","author":"Acevedo-Villanueva","year":"2021","journal-title":"Vaccines."},{"key":"10.1016\/j.psj.2025.105024_bib0003","doi-asserted-by":"crossref","DOI":"10.3389\/fimmu.2024.1383476","article-title":"A TLR4 ligand-based adjuvant for promoting the immunogenicity of typhoid subunit vaccines","volume":"15","author":"Alugupalli","year":"2024","journal-title":"Front. Immunol."},{"key":"10.1016\/j.psj.2025.105024_bib0005","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0105713","article-title":"TLR ligands induce antiviral responses in chicken macrophages","volume":"9","author":"Barjesteh","year":"2014","journal-title":"PLoS One"},{"key":"10.1016\/j.psj.2025.105024_bib0006","doi-asserted-by":"crossref","first-page":"727","DOI":"10.1016\/j.vaccine.2023.12.054","article-title":"The commercial vaccine provides cross-protection by reducing colonization of Salmonella enterica serovars Infantis and Hadar in turkeys","volume":"42","author":"Bearson","year":"2024","journal-title":"Vaccine"},{"key":"10.1016\/j.psj.2025.105024_bib0007","doi-asserted-by":"crossref","DOI":"10.3389\/fmicb.2023.1327739","article-title":"Early vaccination of laying hens with the live bivalent Salmonella vaccine AviPro\u2122 Salmonella DUO results in successful vaccine uptake and increased gut colonization","volume":"14","author":"Cawthraw","year":"2024","journal-title":"Front. Microbiol."},{"key":"10.1016\/j.psj.2025.105024_bib0008","unstructured":"CDC. 2022. Salmonella. Available at: https:\/\/www.cdc.gov\/Salmonella\/index.html (Accessed July 20, 2022)."},{"key":"10.1016\/j.psj.2025.105024_bib0009","doi-asserted-by":"crossref","first-page":"863","DOI":"10.3390\/ijerph15050863","article-title":"Campylobacteriosis, salmonellosis, yersiniosis, and listeriosis as zoonotic foodborne diseases: a review","volume":"15","author":"Chlebicz","year":"2018","journal-title":"Int. J. Environ. Res. Public Health."},{"key":"10.1016\/j.psj.2025.105024_bib0010","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1586\/erv.10.162","article-title":"Hepatitis B surface antigen-1018 ISS adjuvant-containing vaccine: a review of HEPLISAV\u2122 safety and efficacy","volume":"10","author":"Cooper","year":"2011","journal-title":"Expert Rev. Vaccines."},{"key":"10.1016\/j.psj.2025.105024_bib0011","doi-asserted-by":"crossref","first-page":"390","DOI":"10.1590\/S1517-83822008000200034","article-title":"Control of Salmonella enterica serovar Enteritidis in laying hens by inactivated Salmonella Enteritidis vaccines","volume":"39","author":"de Freitas Neto","year":"2008","journal-title":"Braz J Microbiol"},{"key":"10.1016\/j.psj.2025.105024_bib0012","unstructured":"EFSA. 2021. Salmonella. Available at: https:\/\/www.efsa.europa.eu\/en\/topics\/topic\/Salmonella (Accessed July 20, 2022)."},{"key":"10.1016\/j.psj.2025.105024_bib0013","doi-asserted-by":"crossref","first-page":"e46094","DOI":"10.1371\/journal.pone.0046094","article-title":"Phase 1 study in malaria na\u00efve adults of BSAM2\/Alhydrogel\u00ae+CPG 7909, a blood stage vaccine against P. falciparum malaria","author":"Ellis","year":"2012","journal-title":"PLoS One"},{"key":"10.1016\/j.psj.2025.105024_bib0014","doi-asserted-by":"crossref","first-page":"813","DOI":"10.1637\/7194-041204R","article-title":"Protection of neonatal chicks against a lethal challenge of Escherichia coli using DNA containing cytosine-phosphodiester-guanine motifs","volume":"48","author":"Gomis","year":"2004","journal-title":"Avian Dis"},{"key":"10.1016\/j.psj.2025.105024_bib0015","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1637\/11684-060617-Reg.1","article-title":"Intrapulmonary delivery of CpG-ODN microdroplets provides protection against Escherichia coli septicemia in neonatal broiler chickens","volume":"61","author":"Goonewardene","year":"2017","journal-title":"Avian Dis"},{"key":"10.1016\/j.psj.2025.105024_bib0016","doi-asserted-by":"crossref","first-page":"9028","DOI":"10.1038\/s41598-021-88386-2","article-title":"CpG-ODN induced antimicrobial immunity in neonatal chicks involves a substantial shift in serum metabolic profiles","volume":"11","author":"Goonewardene","year":"2021","journal-title":"Sci. Rep."},{"key":"10.1016\/j.psj.2025.105024_bib0017","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1637\/10832-032814-Reg","article-title":"Protection of neonatal broiler chickens following in ovo delivery of oligodeoxynucleotides containing CpG motifs (CpG-ODN) formulated with carbon nanotubes or liposomes","volume":"59","author":"Gunawardana","year":"2015","journal-title":"Avian Dis"},{"key":"10.1016\/j.psj.2025.105024_bib0018","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1038\/s41598-018-36588-6","article-title":"Synthetic CpG-ODN rapidly enriches immune compartments in neonatal chicks to induce protective immunity against bacterial infections","volume":"9","author":"Gunawardana","year":"2019","journal-title":"Sci. Rep."},{"key":"10.1016\/j.psj.2025.105024_bib0019","article-title":"CpG-ODN induces a dose-dependent enrichment of immunological niches in the spleen and lungs of neonatal chicks that correlates with the protective immunity against Escherichia coli","volume":"13","author":"Gunawardana","year":"2020","journal-title":"J. Immunol. Res."},{"key":"10.1016\/j.psj.2025.105024_bib0020","doi-asserted-by":"crossref","first-page":"1060","DOI":"10.1002\/etc.4702","article-title":"Modulatory effects of Pb2+ on virally challenged chicken macrophage (HD-11) and B-lymphocyte (DT40) cell lines in vitro","volume":"39","author":"Han","year":"2020","journal-title":"Environ. Toxicol. Chem."},{"key":"10.1016\/j.psj.2025.105024_bib0021","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1016\/j.femsim.2004.07.009","article-title":"In vitro activation of chicken leukocytes and in vivo protection against Salmonella enteritidis organ invasion and peritoneal S. enteritidis infection-induced mortality in neonatal chickens by immunostimulatory CpG oligodeoxynucleotide","volume":"43","author":"He","year":"2005","journal-title":"FEMS Immunol. Med. Microbiol."},{"key":"10.1016\/j.psj.2025.105024_bib0022","doi-asserted-by":"crossref","DOI":"10.2141\/jpsa.2023002","article-title":"Screening of optimal CpG-oligodeoxynucleotide for anti-inflammatory responses in the avian macrophage cell line HD11","volume":"60","author":"Ichikawa","year":"2023","journal-title":"J. Poult. Sci."},{"key":"10.1016\/j.psj.2025.105024_bib0023","doi-asserted-by":"crossref","first-page":"6774","DOI":"10.1038\/s41467-021-27029-6","article-title":"A phase I\/II randomized trial of H56:IC31 vaccination and adjunctive cyclooxygenase-2-inhibitor treatment in tuberculosis patients","volume":"12","author":"Jenum","year":"2021","journal-title":"Nat Commun"},{"key":"10.1016\/j.psj.2025.105024_bib0024","doi-asserted-by":"crossref","first-page":"460","DOI":"10.4049\/jimmunol.0901921","article-title":"Chicken TLR21 is an innate CpG DNA receptor distinct from mammalian TLR9","volume":"185","author":"Keestra","year":"2010","journal-title":"J. Immunol."},{"key":"10.1016\/j.psj.2025.105024_bib0025","doi-asserted-by":"crossref","first-page":"3086","DOI":"10.1073\/pnas.1319268111","article-title":"Nonagonistic dectin-1 ligand transforms CpG into a multitask nanoparticulate TLR9 agonist","volume":"111","author":"Kobiyama","year":"2014","journal-title":"Proc. Natl. Acad. Sci."},{"key":"10.1016\/j.psj.2025.105024_bib0026","doi-asserted-by":"crossref","first-page":"709","DOI":"10.1146\/annurev.immunol.20.100301.064842","article-title":"CpG motifs in bacterial DNA and their immune effects","volume":"20","author":"Krieg","year":"2022","journal-title":"Annu. Rev. Immunol."},{"key":"10.1016\/j.psj.2025.105024_bib0027","doi-asserted-by":"crossref","DOI":"10.3389\/fvets.2021.730700","article-title":"CAvant\u00ae WO-60 as an effective immunological adjuvant for avian influenza and newcastle disease vaccine","volume":"8","author":"Lee","year":"2021","journal-title":"Front. Vet. Sci."},{"key":"10.1016\/j.psj.2025.105024_bib0028","doi-asserted-by":"crossref","first-page":"1235","DOI":"10.1021\/pr7005928","article-title":"Downregulation of Tsx and OmpW and upregulation of OmpX are required for iron homeostasis in Escherichia coli","volume":"7","author":"Lin","year":"2008","journal-title":"J. Proteome Res."},{"key":"10.1016\/j.psj.2025.105024_bib0029","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1056\/NEJMoa1714021","article-title":"Prevention of M. tuberculosis infection with H4:IC31 vaccine or BCG revaccination","volume":"379","author":"Nemes","year":"2018","journal-title":"N Engl J Med"},{"key":"10.1016\/j.psj.2025.105024_bib0030","doi-asserted-by":"crossref","first-page":"140","DOI":"10.3389\/fnut.2019.00140","article-title":"Cooperation of oligodeoxynucleotides and synthetic molecules as enhanced immune modulators","volume":"6","author":"Nigar","year":"2019","journal-title":"Front Nutr"},{"key":"10.1016\/j.psj.2025.105024_bib0031","doi-asserted-by":"crossref","first-page":"407","DOI":"10.3201\/eid1903.111866","article-title":"Attribution of foodborne illnesses, hospitalizations, and deaths to food commodities by using outbreak data, United States, 1998\u20132008","volume":"19","author":"Painter","year":"2013","journal-title":"Emerg. Infect. Dis."},{"key":"10.1016\/j.psj.2025.105024_bib0032","doi-asserted-by":"crossref","DOI":"10.1016\/j.vetimm.2024.110855","article-title":"Progress in the application of Salmonella vaccines in poultry: a mini review","volume":"278","author":"Pan","year":"2024","journal-title":"Vet. Immunol. Immunopathol."},{"key":"10.1016\/j.psj.2025.105024_bib0034","doi-asserted-by":"crossref","first-page":"320","DOI":"10.3390\/vaccines3020320","article-title":"Vaccine adjuvants: from 1920 to 2015 and beyond","volume":"3","author":"Pasquale","year":"2015","journal-title":"Vaccines"},{"key":"10.1016\/j.psj.2025.105024_bib0035","doi-asserted-by":"crossref","first-page":"682","DOI":"10.1016\/S0140-6736(21)00241-5","article-title":"Safety and immunogenicity of S-Trimer (SCB-2019), a protein subunit vaccine candidate for COVID-19 in healthy adults: a phase 1, randomised, double-blind, placebo-controlled trial","volume":"397","author":"Richmond","year":"2021","journal-title":"Lancet"},{"key":"10.1016\/j.psj.2025.105024_bib0036","doi-asserted-by":"crossref","first-page":"226","DOI":"10.3390\/vaccines10020226","article-title":"Efficacy of multivalent, cochleate-based vaccine against Salmonella Infantis, S. Enteritidis and S. Typhimurium in laying hens","volume":"10","author":"Saenz","year":"2022","journal-title":"Vaccines"},{"key":"10.1016\/j.psj.2025.105024_bib0037","doi-asserted-by":"crossref","first-page":"148","DOI":"10.3390\/vaccines3010148","article-title":"Choice and design of adjuvants for parenteral and mucosal vaccines","volume":"3","author":"Savelkoul","year":"2015","journal-title":"Vaccines"},{"key":"10.1016\/j.psj.2025.105024_bib0038","doi-asserted-by":"crossref","first-page":"845","DOI":"10.3390\/vaccines9080845","article-title":"T-cell cytokine response in Salmonella Typhimurium-vaccinated versus infected pigs","volume":"9","author":"Schmidt","year":"2021","journal-title":"Vaccines"},{"key":"10.1016\/j.psj.2025.105024_bib0040","doi-asserted-by":"crossref","DOI":"10.2141\/jpsa.2024025","article-title":"Effects of synthetic CpG oligodeoxynucleotide K3 on immune response, behavior, and physiology in male layer chicks (Gallus gallus)","volume":"61","author":"Tachibana","year":"2024","journal-title":"J. Poult. Sci."},{"key":"10.1016\/j.psj.2025.105024_bib0041","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1016\/j.vetmic.2017.11.010","article-title":"Gene expression profiling of chicken cecal tonsils and ileum following oral exposure to soluble and PLGA-encapsulated CpG ODN, and lysate of Campylobacter jejuni","volume":"212","author":"Taha-Abdelaziz","year":"2017","journal-title":"Vet. Microbiol."},{"key":"10.1016\/j.psj.2025.105024_bib0042","doi-asserted-by":"crossref","first-page":"398","DOI":"10.1637\/8196-121907-Reg","article-title":"Protection of neonatal broiler chicks against Salmonella Typhimurium septicemia by DNA containing CpG motifs","volume":"52","author":"Taghavi","year":"2008","journal-title":"Avian Dis"},{"key":"10.1016\/j.psj.2025.105024_bib0043","doi-asserted-by":"crossref","first-page":"5573","DOI":"10.1128\/IAI.67.11.5573-5578.1999","article-title":"Differentiation of monocytes to macrophages primes cells for lipopolysaccharide stimulation via accumulation of cytoplasmic nuclear factor k B","volume":"67","author":"Takashiba","year":"1999","journal-title":"Infect. Immun."},{"key":"10.1016\/j.psj.2025.105024_bib0044","doi-asserted-by":"crossref","first-page":"6361","DOI":"10.1128\/AEM.00961-09","article-title":"Quantification of horizontal transmission of Salmonella enterica serovar Enteritidis bacteria in pair-housed groups of laying hens","volume":"75","author":"Thomas","year":"2009","journal-title":"Appl. Environ. Microbiol."},{"key":"10.1016\/j.psj.2025.105024_bib0045","unstructured":"USDA-FSIS. 2021. Serotypes profile of Salmonella isolates from meat and poultry products, January 1998 through December 2014. Available at: https:\/\/www.fsis.usda.gov\/wps\/portal\/fsis\/topics\/data-collection reports\/microbiology\/annual-serotyping-reports (Accessed August 17, 2021)."},{"key":"10.1016\/j.psj.2025.105024_bib0046","doi-asserted-by":"crossref","first-page":"2372","DOI":"10.4049\/jimmunol.166.4.2372","article-title":"Human peripheral blood cells differentially recognize and respond to two distinct CPG motifs","volume":"166","author":"Verthelyi","year":"2001","journal-title":"J. Immunol."},{"key":"10.1016\/j.psj.2025.105024_bib0047","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1016\/j.addr.2008.12.008","article-title":"Immunotherapeutic applications of CpG oligodeoxynucleotide TLR9 agonists","volume":"61","author":"Vollmer","year":"2009","journal-title":"Adv. Drug Deliv. Rev."},{"key":"10.1016\/j.psj.2025.105024_bib0049","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1038\/s41392-023-01557-7","article-title":"Vaccine adjuvants: mechanisms and platforms","volume":"8","author":"Zhao","year":"2023","journal-title":"Sig. Transduct. Target. Ther."},{"key":"10.1016\/j.psj.2025.105024_fur1","series-title":"Ross 308 Broiler Nutrition Specifications","author":"Aviagen","year":"2014"},{"key":"10.1016\/j.psj.2025.105024_fur2","first-page":"541","article-title":"Salmonella contamination: a significant challenge to the global marketing of animal food products","volume":"25","author":"Plym","year":"2006","journal-title":"Rev. Sci. Tech."},{"key":"10.1016\/j.psj.2025.105024_fur3","doi-asserted-by":"crossref","first-page":"100","DOI":"10.2174\/1875035400902010100","article-title":"S.almonella vaccines for animals and birds and their future perspective","volume":"2","author":"Singh","year":"2009","journal-title":"Open Vaccine J"},{"key":"10.1016\/j.psj.2025.105024_fur4","doi-asserted-by":"crossref","first-page":"823","DOI":"10.1016\/S0145-305X(03)00079-X","article-title":"CpG-induced immunomodulation and intracellular bacterial killing in a chicken macrophage cell line","volume":"27","author":"Xie","year":"2003","journal-title":"Dev. Comp. Immunol."}],"container-title":["Poultry Science"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0032579125002639?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0032579125002639?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2026,4,20]],"date-time":"2026-04-20T06:30:45Z","timestamp":1776666645000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0032579125002639"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,5]]},"references-count":49,"journal-issue":{"issue":"5","published-print":{"date-parts":[[2025,5]]}},"alternative-id":["S0032579125002639"],"URL":"https:\/\/doi.org\/10.1016\/j.psj.2025.105024","relation":{},"ISSN":["0032-5791"],"issn-type":[{"value":"0032-5791","type":"print"}],"subject":[],"published":{"date-parts":[[2025,5]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"A novel trivalent inactivated Salmonella vaccine formulated with CpG ODNs to enhance the cellular immunity in chickens","name":"articletitle","label":"Article Title"},{"value":"Poultry Science","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.psj.2025.105024","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2025 The Authors. Published by Elsevier Inc. on behalf of Poultry Science Association Inc.","name":"copyright","label":"Copyright"}],"article-number":"105024"}}