{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,23]],"date-time":"2026-06-23T10:36:09Z","timestamp":1782210969283,"version":"3.54.5"},"reference-count":46,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2021,3,16]],"date-time":"2021-03-16T00:00:00Z","timestamp":1615852800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Vet. Sci."],"abstract":"<jats:p>The present study was designed to explore the <jats:italic>Salmonella<\/jats:italic> prevalence and antimicrobial resistance characteristics in the context of chick mortality at hatching in China. Between December 2015 and August 2017, 1,288 dead-in-shell chicken embryos were collected from four breeder chicken hatcheries in Tai'an, Rizhao, Jining, and Heze, China. <jats:italic>Salmonella<\/jats:italic> isolates were successfully recovered from 6.7% of these embryos (86\/1,288) and were evaluated for serotype, antimicrobial susceptibility, Class 1 integron prevalence, antimicrobial resistance gene expression, and multilocus sequence typing (MLST). <jats:italic>Salmonella<\/jats:italic> Thompson (37.2%), and <jats:italic>Salmonella<\/jats:italic> Infantis (32.6%) were the two most prevalent isolates in these chicken embryos, and 66.3% of isolates exhibited robust ampicillin resistance, while 55.8% of isolates exhibited multi-drug resistance (MDR). The majority of isolates harbored the <jats:italic>bla<\/jats:italic><jats:sub>TEM<\/jats:sub> gene (74.4%), with the <jats:italic>qnrS<\/jats:italic> gene also being highly prevalent (50.0%). In contrast, just 27.9% of these isolates carried Class 1 integrons. These 86 isolates were separated into four sequence types (STs), whereby ST26 (32.2%) was the most prevalent. Overall, these results suggested that <jats:italic>Salmonella<\/jats:italic> infections may be an important cause of chicken embryo mortality in China, and that efforts to support the appropriate use of antibiotics in managing poultry populations are essential.<\/jats:p>","DOI":"10.3389\/fvets.2021.581946","type":"journal-article","created":{"date-parts":[[2021,3,16]],"date-time":"2021-03-16T04:31:31Z","timestamp":1615869091000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":26,"title":["Prevalence and Antimicrobial Resistance of Salmonella Isolated From Dead-in-Shell Chicken Embryos in Shandong, China"],"prefix":"10.3389","volume":"8","author":[{"given":"Xiaonan","family":"Zhao","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zijing","family":"Ju","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guisheng","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jie","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fangkun","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hui","family":"Tang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaomin","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuhong","family":"Sun","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2021,3,16]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1017\/S1462399407000373","article-title":"Salmonella-induced enteritis: molecular pathogenesis and therapeutic implications","volume":"9","author":"Layton","year":"2007","journal-title":"Expert Rev Mol Med."},{"key":"B2","doi-asserted-by":"publisher","first-page":"226","DOI":"10.1016\/j.meegid.2013.01.020","article-title":"Analysis of pulsed field gel electrophoresis profiles using multiple enzymes for predicting potential source reservoirs for strains of Salmonella enteritidis and Salmonella typhimurium isolated from humans","volume":"16","author":"Son","year":"2013","journal-title":"Infect Genet Evol."},{"key":"B3","doi-asserted-by":"publisher","first-page":"516","DOI":"10.1001\/jama.1993.03510040036011","article-title":"Salmonella serotype Tennessee in powdered milk products and infant formula Canada and the United States","volume":"42","year":"2014","journal-title":"Morb Mortal Wkly Rep."},{"key":"B4","doi-asserted-by":"publisher","first-page":"128","DOI":"10.1093\/infdis\/170.1.128","article-title":"Increase in antimicrobial-resistant Salmonella infections in the United States, 1989-1990","volume":"170","author":"Lee","year":"1994","journal-title":"J Infect Dis."},{"key":"B5","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1186\/s12879-015-0784-4","article-title":"Serotypes, seasonal trends, and antibiotic resistance of non-typhoidal Salmonella from human patients in Guangdong Province, China, 2009-2012","volume":"15","author":"Liang","year":"2015","journal-title":"BMC Infect Dis."},{"key":"B6","doi-asserted-by":"publisher","first-page":"153","DOI":"10.1016\/j.vetmic.2005.10.034","article-title":"Distribution of Salmonella enterica serovars from humans, livestock and meat in Vietnam and the dominance of Salmonella Typhimurium phage type 90","volume":"113","author":"Vo","year":"2006","journal-title":"Vet Microb."},{"key":"B7","doi-asserted-by":"publisher","first-page":"8159567","DOI":"10.1155\/2019\/8159567","article-title":"Occurrence and characterization of Salmonella isolated from large-scale breeder farms in Shandong Province, China","volume":"5","author":"Yang","year":"2019","journal-title":"Biomed Res Int"},{"key":"B8","doi-asserted-by":"publisher","first-page":"00597","DOI":"10.3389\/fcimb.2020.00497","article-title":"Epidemiological investigation and antimicrobial resistance profiles of Salmonella isolated from breeder hicken hatcheries in Henan, China","volume":"15","author":"Xu","year":"2020","journal-title":"Front Cell Infect Microbiol"},{"key":"B9","doi-asserted-by":"publisher","first-page":"131","DOI":"10.1016\/j.vetmic.2009.07.009","article-title":"Prevalence of Salmonella associated with chick mortality at hatching and their susceptibility to antimicrobial agents","volume":"140","author":"Maryam","year":"2010","journal-title":"Vet Microbiol"},{"key":"B10","doi-asserted-by":"publisher","first-page":"290","DOI":"10.1080\/03079457.2013.788129","article-title":"Antimicrobial resistance, presence of integrons and biofilm formation of Salmonella Pullorum isolates from eastern China (1962-2010)","volume":"42","author":"Gong","year":"2013","journal-title":"Avian Pathol."},{"key":"B11","doi-asserted-by":"publisher","first-page":"30","DOI":"10.1016\/j.ijfoodmicro.2014.03.030","article-title":"Serotype distribution and antibiotic resistance of Salmonella in food-producing animals in Shandong province of China, 2009 and 2012","volume":"180","author":"Lai","year":"2014","journal-title":"Int J Food Microbiol."},{"key":"B12","doi-asserted-by":"publisher","first-page":"1117","DOI":"10.1016\/j.psj.2019.10.044","article-title":"Prevalence and characteristics of multidrug-resistant mcr-1-positive Escherichia coli isolates from broiler chickens in Tai'an, China","volume":"99","author":"Song","year":"2020","journal-title":"Poultry Sci"},{"key":"B13","doi-asserted-by":"publisher","first-page":"4374","DOI":"10.3382\/ps\/pey305","article-title":"Analyses of prevalence and molecular typing reveal the spread of antimicrobial-resistant Salmonella infection across two breeder chicken farms","volume":"97","author":"Fei","year":"2018","journal-title":"Poultry Sci."},{"key":"B14","doi-asserted-by":"publisher","first-page":"608","DOI":"10.1038\/nrmicro1462","article-title":"Integrons: agents of bacterial evolution","volume":"4","author":"Mazel","year":"2006","journal-title":"Nat Rev Microbiol"},{"key":"B15","doi-asserted-by":"publisher","first-page":"589","DOI":"10.1016\/j.mib.2010.08.005","article-title":"Antibiotic resistance in the environment: a link to the clinic?","volume":"13","author":"Wright","year":"2010","journal-title":"Curr Opin Microbiol"},{"key":"B16","doi-asserted-by":"publisher","first-page":"583","DOI":"10.2307\/1592082","article-title":"Transmission of Salmonella typhimurium during hatching of broiler chicks","volume":"38","author":"Cason","year":"1994","journal-title":"Avian Dis"},{"key":"B17","doi-asserted-by":"publisher","first-page":"1571","DOI":"10.1093\/ps\/79.11.1571","article-title":"Salmonella penetration of egg shells and proliferation in broiler hatching eggs: a review","volume":"79","author":"Cox","year":"2000","journal-title":"Poultry Sci"},{"key":"B18","doi-asserted-by":"publisher","first-page":"479","DOI":"10.3389\/fvets.2020.00479","article-title":"Occurrence and characterization of Salmonella isolated from chicken breeder flocks in nine Chinese provinces","volume":"7","author":"Song","year":"2020","journal-title":"Front Vet Sci"},{"key":"B19","doi-asserted-by":"publisher","first-page":"230","DOI":"10.1016\/j.ijfoodmicro.2010.07.034","article-title":"Prevalence and antimicrobial resistance of Salmonella in retail foods in northern China","volume":"143","author":"Yan","year":"2010","journal-title":"Int J Food Microbiol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1016\/S0168-1605(03)00154-5","article-title":"Interlaboratory diagnostic accuracy of a Salmonella specific PCR-based method","volume":"89","author":"Malorny","year":"2003","journal-title":"Int J Food Microb."},{"key":"B21","first-page":"13","volume-title":"Antigenic Formulae of the Salmonella Serovars","author":"Grimont","year":""},{"key":"B22","volume-title":"Performance Standards for Antimicrobial Susceptibility Testing. 29th Informational Supplement, M100-S29","year":"2019"},{"key":"B23","doi-asserted-by":"publisher","first-page":"242","DOI":"10.1016\/j.ijantimicag.2013.12.005","article-title":"Multiple transmissible genes encoding fluoroquinolone and third-generation cephalosporin resistance co-located in non-typhoidal Salmonella isolated from food-producing animals in China","volume":"43","author":"Jiang","year":"2014","journal-title":"Int J Antimicrob Agents."},{"key":"B24","doi-asserted-by":"publisher","first-page":"1319","DOI":"10.1128\/AAC.49.4.1319-1322.2005","article-title":"bla(CTX-M) genes in clinical Salmonella isolates recovered from humans in England and Wales from 1992 to 2003","volume":"49","author":"Batchelor","year":"2005","journal-title":"Antimicrob Agents Chemother."},{"key":"B25","doi-asserted-by":"publisher","first-page":"14","DOI":"10.1016\/j.ijfoodmicro.2013.01.020","article-title":"Prevalence and characterization of Salmonella species isolated from pigs, ducks and chickens in Sichuan Province, China","volume":"163","author":"Li","year":"2013","journal-title":"Int J Food Microbiol."},{"key":"B26","doi-asserted-by":"publisher","first-page":"513","DOI":"10.1093\/jac\/dkf164","article-title":"Susceptibility of Danish Escherichia coli strains isolated from urinary tract infections and bacteraemia, and distribution of sul genes conferring sulphonamide resistance","volume":"50","author":"Kerrn","year":"2002","journal-title":"J Antimicrob Chemother"},{"key":"B27","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1016\/j.idairyj.2018.06.008","article-title":"Molecular characterisation of Staphylococcus aureus from some artisanal Brazilian dairies","volume":"85","author":"Alves","year":"2018","journal-title":"Int Dairy J"},{"key":"B28","doi-asserted-by":"publisher","first-page":"1482","DOI":"10.3389\/fmicb.2020.01482","article-title":"Prevalence, serotype, antibiotic susceptibility, and genotype of Salmonella in eggs from poultry farms and marketplaces in Yangling, Shaanxi province, China","volume":"11","author":"Li","year":"2020","journal-title":"Front Microbiol."},{"key":"B29","doi-asserted-by":"publisher","first-page":"270","DOI":"10.1016\/j.foodcont.2015.10.036","article-title":"Prevalence and antimicrobial resistance of Salmonella isolated from an integrated broiler chicken supply chain in Qingdao","volume":"62","author":"Cui","year":"2016","journal-title":"China Food Control."},{"key":"B30","doi-asserted-by":"publisher","first-page":"226","DOI":"10.1186\/s12866-019-1598-0","article-title":"Characterization of Salmonella Dublin isolated from bovine and human hosts","volume":"19","author":"Paudyal","year":"2019","journal-title":"BMC microbiol"},{"key":"B31","doi-asserted-by":"publisher","first-page":"186","DOI":"10.14745\/ccdr.v43i09a05","article-title":"Salmonella Thompson outbreak associated with consumption of chicken shawarma and the usefulness of genome sequencing in the investigation","volume":"43","author":"Gaulin","year":"2017","journal-title":"Can Commun Dis Rep"},{"key":"B32","doi-asserted-by":"publisher","first-page":"687","DOI":"10.3382\/ps\/pew342","article-title":"Population dynamics and antimicrobial resistance of the most prevalent poultry-associated Salmonella serotypes","volume":"96","author":"Shah","year":"2017","journal-title":"Poult Sci"},{"key":"B33","doi-asserted-by":"publisher","first-page":"562","DOI":"10.4315\/0362-028X-73.3.562","article-title":"Serotype, genotype, and antimicrobial susceptibility profiles of Salmonella from chicken farms in Shanghai","volume":"73","author":"Liu","year":"2010","journal-title":"J Food Protect."},{"key":"B34","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1089\/fpd.2010.0605","article-title":"Prevalence of antimicrobial resistance among Salmonella isolates from chicken in China","volume":"8","author":"Lu","year":"2011","journal-title":"Foodborne Pathog Dis."},{"key":"B35","doi-asserted-by":"publisher","first-page":"569","DOI":"10.1111\/zph.12265","article-title":"Distribution of Salmonella serovars and antimicrobial susceptibility from poultry and swine farms in Central Vietnam","volume":"63","author":"Lettini","year":"2016","journal-title":"Zoonoses Public Health."},{"key":"B36","doi-asserted-by":"publisher","first-page":"108","DOI":"10.1186\/s12917-019-1836-6","article-title":"Prevalence of Salmonella in broiler chickens in Kagoshima, Japan in 2009 to 2012 and the relationship between serovars changing and antimicrobial resistance","volume":"15","author":"Duc","year":"2019","journal-title":"BMC Vet Res"},{"key":"B37","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1016\/j.ijfoodmicro.2013.03.021","article-title":"Isolation and molecular characterization of Salmonella enterica serovar Javiana from food, environmental and clinical samples","volume":"164","author":"Mezal","year":"2013","journal-title":"Int J Food Microbiol"},{"key":"B38","doi-asserted-by":"publisher","first-page":"3036","DOI":"10.3382\/ps.2013-03312","article-title":"Characterization of integrons and their cassettes in Escherichia coli and Salmonella isolates from poultry in Korea","volume":"92","author":"Dessie","year":"2013","journal-title":"Poultry Sci."},{"key":"B39","doi-asserted-by":"publisher","first-page":"56","DOI":"10.1016\/j.ijfoodmicro.2016.01.020","article-title":"Phenotypic characteristics and genotypic correlation between Salmonella isolates from a slaughterhouse and retail markets in Yangzhou, China","volume":"222","author":"Cai","year":"2016","journal-title":"Int J Food Microbiol."},{"key":"B40","doi-asserted-by":"publisher","first-page":"3366","DOI":"10.1016\/j.chroma.2009.01.105","article-title":"Simultaneous determination of tetracyclines in poultry muscle by capillary zone electrophoresis","volume":"1216","author":"Miranda","year":"2009","journal-title":"J Chromatogr A"},{"key":"B41","doi-asserted-by":"publisher","first-page":"602","DOI":"10.3389\/fmicb.2015.00602","article-title":"Serotypes and antimicrobial susceptibility of Salmonella spp. isolated from farm animals in China","volume":"6","author":"Kuang","year":"2015","journal-title":"Front Microbiol."},{"key":"B42","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1016\/j.bjm.2015.11.021","article-title":"Multidrug resistance and ESBL-producing Salmonella spp. isolated from broiler processing plants","volume":"47","author":"Rosangela","year":"2016","journal-title":"Braz J Microbiol"},{"key":"B43","doi-asserted-by":"publisher","first-page":"196","DOI":"10.1016\/j.bjm.2015.04.001","article-title":"Characterization of quinolone resistance in Salmonella spp. isolates from food products and human samples in Brazil","volume":"47","author":"Pribul","year":"2016","journal-title":"Braz J Microbiol."},{"key":"B44","doi-asserted-by":"publisher","first-page":"454","DOI":"10.3382\/ps\/peu133","article-title":"Characterization of quinolone resistance in Salmonella enterica sevovar Indiana from chickens in China","volume":"94","author":"Lu","year":"2015","journal-title":"Poultry Sci."},{"key":"B45","doi-asserted-by":"publisher","first-page":"1300","DOI":"10.3389\/fmicb.2017.01300","article-title":"Characterization of integrons and resistance genes in Salmonella isolates from farm animals in Shandong Province, China","volume":"8","author":"Zhao","year":"2017","journal-title":"Front Microbiol"},{"key":"B46","doi-asserted-by":"publisher","first-page":"746","DOI":"10.1093\/jac\/dkl549","article-title":"Occurrence and characteristics of class 1, 2 and 3 integrons in Escherichia coli, Salmonella and Campylobacter spp. in the Netherlands","volume":"59","author":"van","year":"2007","journal-title":"J Antimicrob Chemother"}],"container-title":["Frontiers in Veterinary Science"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fvets.2021.581946\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,3,16]],"date-time":"2021-03-16T04:31:35Z","timestamp":1615869095000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fvets.2021.581946\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,3,16]]},"references-count":46,"alternative-id":["10.3389\/fvets.2021.581946"],"URL":"https:\/\/doi.org\/10.3389\/fvets.2021.581946","relation":{},"ISSN":["2297-1769"],"issn-type":[{"value":"2297-1769","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,3,16]]},"article-number":"581946"}}