{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,31]],"date-time":"2026-07-31T19:22:13Z","timestamp":1785525733364,"version":"3.56.0"},"reference-count":39,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2025,2,18]],"date-time":"2025-02-18T00:00:00Z","timestamp":1739836800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100007129","name":"Shandong Provincial Natural Science Foundation","doi-asserted-by":"publisher","award":["ZR2022QH216"],"award-info":[{"award-number":["ZR2022QH216"]}],"id":[{"id":"10.13039\/501100007129","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Microbiol."],"abstract":"<jats:sec><jats:title>Background<\/jats:title><jats:p>The prevalence of carbapenem-resistant <jats:italic>Enterobacteriaceae<\/jats:italic> (CRE) has emerged as a serious public health problem worldwide, and the data on the fecal carriage of CRE strains in hospitalized children remain limited. This study aimed to investigate the molecular characteristics of intestinal colonization of CRE in hospitalized children in Shandong, China.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>A retrospective study was conducted from August to November 2023. Antimicrobial susceptibility testing was performed by the broth microdilution method. Carbapenemase genes, drug resistance genes, and plasmid replicon types were detected using multiplex real-time PCR and whole-genome sequencing. Multilocus sequence typing (MLST) was used to determine the genetic relationships between strains.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>A total of 20 CRE isolates were identified from 432 fecal samples, with a fecal carriage rate of 4.6%. The CRE isolates predominantly consisted of <jats:italic>Escherichia coli<\/jats:italic> (<jats:italic>E. coli<\/jats:italic>, <jats:italic>n<\/jats:italic>\u202f=\u202f13) and <jats:italic>Klebsiella strains<\/jats:italic> (<jats:italic>n<\/jats:italic>\u202f=\u202f6). CRE isolates showed a high resistance rate of 90\u2013100% to seven <jats:italic>\u03b2<\/jats:italic>-lactam antibiotics. Resistance rates for other antibiotics such as trimethoprim-sulfamethoxazole, tetracycline, azithromycin, ciprofloxacin, chloramphenicol, nalidixic acid, and streptomycin were 90, 85, 85, 80, 75, 75, and 75%, respectively. CRE isolates showed low resistance to amikacin (20%), and none of the isolates were resistant to tigecycline. Additionally, the multidrug resistance rate of CRE isolates was 95%. All CRE strains carried sulfonamide antibiotic and <jats:italic>\u03b2<\/jats:italic>-lactamase resistance genes, of which the most common \u03b2-lactamase resistance genes were <jats:italic>bla<\/jats:italic><jats:sub>NDM-1<\/jats:sub> (<jats:italic>n<\/jats:italic>\u202f=\u202f9), <jats:italic>bla<\/jats:italic><jats:sub>NDM-5<\/jats:sub> (<jats:italic>n<\/jats:italic>\u202f=\u202f7) and <jats:italic>bla<\/jats:italic><jats:sub>OXA-1<\/jats:sub> (<jats:italic>n<\/jats:italic>\u202f=\u202f7). Resistance genes to tetracycline and macrolide antibiotics were also widespread among the strains. The study found that IncFIB and IncFII series plasmids were present in 84 and 42% of the CRE strains, respectively. Additionally, Col, IncFIA, IncC, IncHI2, and IncX series plasmids were also detected. MLST analysis revealed diverse sequence types (STs) among CRE isolates, with ST167 being a common ST among <jats:italic>E. coli<\/jats:italic> isolates.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusion<\/jats:title><jats:p>This study revealed <jats:italic>bla<\/jats:italic><jats:sub>NDM<\/jats:sub><jats:italic>E. coli<\/jats:italic> were the dominant isolates in fecal samples of hospitalized children in Shandong Province, with a broad multidrug resistance to antibiotics, emphasizing that infection control measures need to be taken to limit the spread of these strains.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fmicb.2025.1542207","type":"journal-article","created":{"date-parts":[[2025,2,18]],"date-time":"2025-02-18T06:53:52Z","timestamp":1739861632000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":3,"title":["Fecal carriage and molecular characterization of carbapenem-resistant Enterobacteriaceae from hospitalized children in a tertiary hospital of Shandong, China"],"prefix":"10.3389","volume":"16","author":[{"given":"Xia","family":"Deng","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuyun","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peibin","family":"Hou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Na","family":"Sun","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ying","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qian","family":"Zeng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Juan","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chunping","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xin","family":"Lv","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenqiang","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ruyue","family":"Fan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2025,2,18]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"1565","DOI":"10.1021\/bi5000564","article-title":"Mechanism of quinolone action and resistance","volume":"53","author":"Aldred","year":"2014","journal-title":"Biochemistry"},{"key":"ref2","doi-asserted-by":"publisher","first-page":"23195","DOI":"10.1038\/s41598-024-74299-3","article-title":"Genomic analysis of Enterobacteriaceae from colorectal cancer patients at a tertiary hospital in Ghana: a case-control study","volume":"14","author":"Bachelle","year":"2024","journal-title":"Sci. Rep."},{"key":"ref3","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1086\/653535","article-title":"High prevalence of macrolide resistance in Mycoplasma pneumoniae isolates from adult and adolescent patients with respiratory tract infection in China","volume":"51","author":"Cao","year":"2010","journal-title":"Clin. Infect. Dis."},{"key":"ref4","doi-asserted-by":"publisher","first-page":"mfab052","DOI":"10.1093\/mtomcs\/mfab052","article-title":"A genome-wide screen reveals the involvement of enterobactin-mediated iron acquisition in Escherichia coli survival during copper stress","volume":"13","author":"Casanova-Hampton","year":"2021","journal-title":"Metallomics"},{"key":"ref5","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1016\/j.jgar.2021.11.007","article-title":"Rapid increase in occurrence of carbapenem-resistant Enterobacteriaceae in healthy rural residents in Shandong Province, China, from 2015 to 2017","volume":"28","author":"Chen","year":"2022","journal-title":"J Glob Antimicrob Resist"},{"key":"ref6","doi-asserted-by":"publisher","first-page":"1030","DOI":"10.3390\/antibiotics11081030","article-title":"Characterization of Bla(NDM-5)-and Bla(CTX-M-199)-producing ST167 Escherichia coli isolated from shared bikes","volume":"11","author":"Chen","year":"2022","journal-title":"Antibiotics (Basel)"},{"key":"ref7","doi-asserted-by":"publisher","first-page":"300","DOI":"10.1016\/j.jhin.2013.05.003","article-title":"Emergence of carbapenem-resistant Enterobacteriaceae in a UK paediatric hospital","volume":"84","author":"Drew","year":"2013","journal-title":"J. Hosp. Infect."},{"key":"ref8","doi-asserted-by":"publisher","first-page":"655","DOI":"10.2174\/1389203724666230816154117","article-title":"Current update on New Delhi Metallo-beta-lactamase (NDM) variants: new challenges in the journey of evolution","volume":"24","author":"Farooq","year":"2023","journal-title":"Curr. Protein Pept. Sci."},{"key":"ref9","doi-asserted-by":"publisher","first-page":"2628","DOI":"10.3201\/eid2710.211265","article-title":"New Delhi Metallo-beta-lactamase-producing Enterobacterales Bacteria, Switzerland, 2019-2020","volume":"27","author":"Findlay","year":"2021","journal-title":"Emerg. Infect. Dis."},{"key":"ref10","doi-asserted-by":"publisher","first-page":"e0157421","DOI":"10.1128\/spectrum.01574-21","article-title":"Clonal and horizontal transmission of Bla(NDM) among Klebsiella pneumoniae in Children's intensive care units","volume":"10","author":"Fu","year":"2022","journal-title":"Microbiol Spectr"},{"key":"ref11","doi-asserted-by":"publisher","first-page":"128","DOI":"10.1186\/s13756-021-00994-9","article-title":"Admission screening and cohort care decrease carbapenem resistant enterobacteriaceae in Vietnamese pediatric ICU's","volume":"10","author":"Garpvall","year":"2021","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"ref12","doi-asserted-by":"publisher","first-page":"907","DOI":"10.3760\/cma.j.issn.0578-1310.2018.12.005","article-title":"Antimicrobial resistance changes of carbapenem-resistant Enterobacteriaceae strains isolated from children","volume":"56","author":"Guo","year":"2018","journal-title":"Zhonghua Er Ke Za Zhi"},{"key":"ref13","doi-asserted-by":"publisher","first-page":"121869","DOI":"10.1016\/j.envpol.2023.121869","article-title":"High prevalence and genomic characteristics of carbapenem-resistant Enterobacteriaceae and colistin-resistant Enterobacteriaceae from large-scale rivers in China","volume":"331","author":"Guo","year":"2023","journal-title":"Environ. Pollut."},{"key":"ref14","doi-asserted-by":"publisher","first-page":"1091","DOI":"10.2147\/IDR.S191387","article-title":"Raoultella ornithinolytica: emergence and resistance","volume":"13","author":"Hajjar","year":"2020","journal-title":"Infect Drug Resist"},{"key":"ref15","doi-asserted-by":"publisher","first-page":"730","DOI":"10.11817\/j.issn.1672-7347.2024.240029","article-title":"Virulence gene distribution and molecular epidemiological characteristics of carbapenem-resistant Klebsiella pneumoniae in the ICU","volume":"49","author":"Huang","year":"2024","journal-title":"Zhong Nan Da Xue Xue Bao Yi Xue Ban"},{"key":"ref16","doi-asserted-by":"publisher","first-page":"100370","DOI":"10.1016\/j.ijmmb.2023.100370","article-title":"Active surveillance for carbapenem resistant enterobacteriaceae (CRE) using stool cultures as a method to decrease CRE infections in the pediatric intensive care unit (PICU)","volume":"44","author":"Krupanandan","year":"2023","journal-title":"Indian J. Med. Microbiol."},{"key":"ref17","doi-asserted-by":"publisher","first-page":"1357","DOI":"10.1007\/s12325-023-02436-x","article-title":"Aminoglycoside-related nephrotoxicity and ototoxicity in clinical practice: A review of pathophysiological mechanism and treatment options","volume":"40","author":"Le","year":"2023","journal-title":"Adv. Ther."},{"key":"ref18","doi-asserted-by":"publisher","first-page":"101031","DOI":"10.1016\/j.drup.2023.101031","article-title":"Global distribution and genomic characteristics of carbapenemase-producing Escherichia coli among humans, 2005-2023","volume":"72","author":"Li","year":"2024","journal-title":"Drug Resist. Updat."},{"key":"ref19","doi-asserted-by":"publisher","first-page":"240","DOI":"10.1016\/j.jgar.2023.12.032","article-title":"Genomic insights into a Bla(NDM-5)-carrying Escherichia coli ST167 isolate recovered from faecal sample of a healthy individual in China","volume":"36","author":"Li","year":"2024","journal-title":"J Glob Antimicrob Resist"},{"key":"ref20","doi-asserted-by":"publisher","first-page":"2551","DOI":"10.2147\/IDR.S366480","article-title":"Three novel sequence types Carbapenem-resistant Klebsiella pneumoniae strains ST5365, ST5587, ST5647 isolated from two tertiary teaching general hospitals in Shanxi Province, in North China: molecular characteristics, resistance and virulence factors","volume":"15","author":"Liu","year":"2022","journal-title":"Infect Drug Resist"},{"key":"ref21","doi-asserted-by":"publisher","first-page":"7307","DOI":"10.2147\/IDR.S394283","article-title":"Risk factors for mortality and antimicrobial regimens in pediatric intensive care unit patients with Carbapenem-resistant Enterobacteriaceae infections: A six-year retrospective study","volume":"15","author":"Liu","year":"2022","journal-title":"Infect Drug Resist"},{"key":"ref22","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1186\/s13756-018-0346-9","article-title":"A systematic review of the epidemiology of carbapenem-resistant Enterobacteriaceae in the United States","volume":"7","author":"Livorsi","year":"2018","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"ref23","doi-asserted-by":"publisher","first-page":"2014","DOI":"10.3201\/eid2111.150548","article-title":"Carbapenem-resistant Enterobacteriaceae in children, United States, 1999-2012","volume":"21","author":"Logan","year":"2015","journal-title":"Emerg. Infect. Dis."},{"key":"ref24","doi-asserted-by":"publisher","first-page":"906","DOI":"10.1093\/jac\/dkr563","article-title":"Rapid detection of carbapenemase genes by multiplex real-time PCR","volume":"67","author":"Monteiro","year":"2012","journal-title":"J. Antimicrob. Chemother."},{"key":"ref25","doi-asserted-by":"publisher","first-page":"678","DOI":"10.1186\/s12879-019-4298-3","article-title":"Fecal carriage and molecular epidemiology of carbapenem-resistant Enterobacteriaceae from outpatient children in Shanghai","volume":"19","author":"Pan","year":"2019","journal-title":"BMC Infect. Dis."},{"key":"ref26","doi-asserted-by":"publisher","first-page":"1060","DOI":"10.1002\/jcph.715","article-title":"Safety concerns surrounding quinolone use in children","volume":"56","author":"Patel","year":"2016","journal-title":"J. Clin. Pharmacol."},{"key":"ref27","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1016\/j.jgar.2021.08.001","article-title":"Environmental antimicrobial resistance and its drivers: a potential threat to public health","volume":"27","author":"Samreen","year":"2021","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref28","doi-asserted-by":"publisher","first-page":"258","DOI":"10.1016\/j.jaad.2005.10.004","article-title":"Tetracyclines: nonantibiotic properties and their clinical implications","volume":"54","author":"Sapadin","year":"2006","journal-title":"J. Am. Acad. Dermatol."},{"key":"ref29","doi-asserted-by":"publisher","first-page":"e0228079","DOI":"10.1371\/journal.pone.0228079","article-title":"Whole genome sequencing snapshot of multi-drug resistant Klebsiella pneumoniae strains from hospitals and receiving wastewater treatment plants in southern Romania","volume":"15","author":"Surleac","year":"2020","journal-title":"PLoS One"},{"key":"ref30","doi-asserted-by":"publisher","first-page":"318","DOI":"10.1016\/S1473-3099(17)30753-3","article-title":"Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis","volume":"18","author":"Tacconelli","year":"2018","journal-title":"Lancet Infect. Dis."},{"key":"ref31","doi-asserted-by":"publisher","first-page":"S196","DOI":"10.1093\/cid\/ciy660","article-title":"Phenotypic and genotypic characterization of Carbapenem-resistantEnterobacteriaceae: data from a longitudinal large-scale CRE study in China (2012\u20132016)","volume":"67","author":"Wang","year":"2018","journal-title":"Clin. Infect. Dis."},{"key":"ref32","doi-asserted-by":"publisher","first-page":"e00115-18","DOI":"10.1128\/CMR.00115-18","article-title":"NDM Metallo-beta-lactamases and their bacterial producers in health care settings","volume":"32","author":"Wu","year":"2019","journal-title":"Clin. Microbiol. Rev."},{"key":"ref33","doi-asserted-by":"publisher","first-page":"e0283923","DOI":"10.1128\/spectrum.02839-23","article-title":"Clinical and molecular epidemiology of carbapenem-resistant Enterobacteriaceae in pediatric inpatients in South China","volume":"11","author":"Xiong","year":"2023","journal-title":"Microbiol Spectr"},{"key":"ref34","doi-asserted-by":"publisher","first-page":"1237993","DOI":"10.3389\/fmicb.2023.1237993","article-title":"Pediatric intensive care unit treatment alters the diversity and composition of the gut microbiota and antimicrobial resistance gene expression in critically ill children","volume":"14","author":"Xu","year":"2023","journal-title":"Front. Microbiol."},{"key":"ref35","doi-asserted-by":"publisher","first-page":"4405","DOI":"10.2147\/IDR.S275549","article-title":"Fecal carriage and molecular epidemiology of Carbapenem-resistant Enterobacteriaceae from inpatient children in a pediatric Hospital of Shanghai","volume":"13","author":"Xu","year":"2020","journal-title":"Infect Drug Resist"},{"key":"ref36","doi-asserted-by":"publisher","first-page":"168","DOI":"10.1016\/j.pedneo.2022.05.016","article-title":"Carbapenem-resistant Enterobacteriaceae infection in children less than one year old in an Asian medical center","volume":"64","author":"Yen","year":"2023","journal-title":"Pediatr. Neonatol."},{"key":"ref37","doi-asserted-by":"publisher","first-page":"dlab032","DOI":"10.1093\/jacamr\/dlab032","article-title":"Dissemination mechanisms of NDM genes in hospitalized patients","volume":"3","author":"Zhai","year":"2021","journal-title":"JAC Antimicrob Resist"},{"key":"ref38","doi-asserted-by":"publisher","first-page":"1018682","DOI":"10.3389\/fmicb.2022.1018682","article-title":"Antimicrobial resistance and genomic characterization of Escherichia coli from pigs and chickens in Zhejiang, China","volume":"13","author":"Zhou","year":"2022","journal-title":"Front Microbiol"},{"key":"ref39","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1186\/s13756-019-0674-4","article-title":"Epidemiological characteristics of carbapenem-resistant Enterobacteriaceae collected from 17 hospitals in Nanjing district of China","volume":"9","author":"Zhou","year":"2020","journal-title":"Antimicrob. Resist. Infect. 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