{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T05:00:20Z","timestamp":1790830820407,"version":"4.1.0"},"reference-count":37,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T00:00:00Z","timestamp":1790812800000},"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. Cell. Infect. Microbiol."],"abstract":"\n Objective<\/jats:title>\n To characterize the distribution and antimicrobial resistance evolution of ESKAPEEc pathogens causing pediatric bloodstream infections in Sichuan Province across the COVID-19 era, and to systematically evaluate the epidemiology of carbapenem resistance (CR), difficult-to-treat resistance (DTR), and MIC drift in vancomycin and linezolid, thereby addressing a long-standing gap in longitudinal pediatric multidrug-resistant surveillance in Southwest China.<\/jats:p>\n <\/jats:sec>\n \n Methods<\/jats:title>\n A multicenter retrospective study was conducted using pediatric blood culture data from 134 healthcare institutions in Sichuan Province between 2017 and 2025.\u00a0A total of 20,018 isolates were included and stratified into pre-pandemic, pandemic, and post-pandemic periods. Antimicrobial susceptibility testing and DTR classification were interpreted according to CLSI M100 (35th edition) criteria. Statistical analyses were performed using WHONET 5.6 and SPSS 26.0.<\/jats:p>\n <\/jats:sec>\n \n Results<\/jats:title>\n \n A total of 5,236 ESKAPEEc isolates were identified, accounting for 26.2% of all bloodstream isolates. Detection rates increased during the pandemic period and declined thereafter. Carbapenem resistance rates in\n Escherichia coli<\/jats:italic>\n and\n Klebsiella pneumoniae<\/jats:italic>\n were significantly higher in the post-pandemic period compared with the pre-pandemic baseline. The overall DTR prevalence was 8.6%, with\n Acinetobacter baumannii<\/jats:italic>\n exhibiting the highest DTR burden (87.3%) despite a declining temporal trend, whereas DTR in\n K. pneumoniae<\/jats:italic>\n increased progressively over time. Reliance on CR criteria alone failed to identify a substantial proportion of DTR-positive\n E. coli<\/jats:italic>\n isolates. All\n Staphylococcus aureus<\/jats:italic>\n isolates remained susceptible to vancomycin and linezolid\n in vitro<\/jats:italic>\n , with stable vancomycin MIC distributions; however, a high-MIC subpopulation among linezolid-treated MRSA isolates increased significantly over time (r=0.767,\n P<\/jats:italic>\n \u00a0=\u00a00.016). Distinct age-stratified differences were observed in both pathogen distribution and resistance profiles.\n <\/jats:p>\n <\/jats:sec>\n \n Conclusions<\/jats:title>\n The COVID-19 pandemic exerted a bidirectional and sustained impact on the pediatric ESKAPEEc landscape and resistance ecology in Sichuan Province. Post-pandemic escalation of carbapenem resistance persists. The persistently high DTR burden in A. baumannii and early MIC drift toward linezolid in MRSA represent two critical regional threats in pediatric infectious disease management. Regional surveillance systems should incorporate DTR metrics alongside CR monitoring and implement age-stratified, precision-based antimicrobial stewardship strategies.<\/jats:p>\n <\/jats:sec>","DOI":"10.3389\/fcimb.2026.1914448","type":"journal-article","created":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T04:45:28Z","timestamp":1790829928000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":0,"title":["Distribution, carbapenem resistance and DTR dynamics of ESKAPEEc pathogens from pediatric bloodstream infections in Sichuan Province, 2017-2025: epidemiological characteristics under COVID-19 pandemic and emerging linezolid MIC creep"],"prefix":"10.3389","volume":"16","author":[{"given":"Shanshan","family":"Long","sequence":"first","affiliation":[{"name":"Department of Laboratory Medicine, Sichuan Provincial People\u2019s Hospital, University of Electronic Science and Technology of China","place":["Chengdu, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Min","family":"Zhong","sequence":"additional","affiliation":[{"name":"Department of Laboratory Medicine, Sichuan Provincial People\u2019s Hospital, University of Electronic Science and Technology of China","place":["Chengdu, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xin","family":"Liu","sequence":"additional","affiliation":[{"name":"Department of Laboratory Medicine, Sichuan Provincial People\u2019s Hospital, University of Electronic Science and Technology of China","place":["Chengdu, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kai","family":"Zhang","sequence":"additional","affiliation":[{"name":"Department of Laboratory Medicine, Sichuan Provincial People\u2019s Hospital, University of Electronic Science and Technology of China","place":["Chengdu, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhuorui","family":"You","sequence":"additional","affiliation":[{"name":"School of Medicine, University of Electronic Science and Technology of China","place":["Chengdu, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiangning","family":"Huang","sequence":"additional","affiliation":[{"name":"Department of Laboratory Medicine, Sichuan Provincial People\u2019s Hospital, University of Electronic Science and Technology of China","place":["Chengdu, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hua","family":"Yu","sequence":"additional","affiliation":[{"name":"Department of Laboratory Medicine, Sichuan Provincial People\u2019s Hospital, University of Electronic Science and Technology of China","place":["Chengdu, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2026,10,1]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"165","DOI":"10.1007\/s10482-025-02181-x","article-title":"Impact of COVID-19 on the prevalence of multi-drug-resistant bacteria: a literature review and meta-analysis","volume":"118","author":"Ahmed","year":"2025","journal-title":"Antonie van Leeuwenhoek"},{"key":"B2","first-page":"412","article-title":"Monitoring of vancomycin MIC trends in Staphylococcus aureus from pediatric patients in Shanghai, 2013\u20132022","volume":"61","author":"Chen","year":"2023","journal-title":"Chin. J. Pediatr."},{"key":"B3","volume-title":"Performance Standards for Antimicrobial Susceptibility Testing. 35th Ed. CLSI Supplement M100","year":"2025"},{"key":"B4","doi-asserted-by":"publisher","first-page":"564","DOI":"10.1097\/QCO.0000000000000966","article-title":"MDR\/XDR\/PDR or DTR? Which definition best fits the resistance profile of Pseudomonas aeruginosa","volume":"36","author":"Cosentino","year":"2023","journal-title":"Curr. Opin. Infect. Dis."},{"key":"B5","doi-asserted-by":"publisher","first-page":"99","DOI":"10.7196\/SAMJ.2017.v108i2.12601","article-title":"Neonatal and paediatric bloodstream infections: pathogens, antimicrobial resistance patterns and prescribing practice at Khayelitsha District Hospital, Cape Town, South Africa","volume":"108","author":"Crichton","year":"2018","journal-title":"S. Afr. Med. J."},{"key":"B6","doi-asserted-by":"publisher","first-page":"1627","DOI":"10.1007\/s10096-018-3292-9","article-title":"Incidence and antimicrobial resistance trends in bloodstream infections caused by ESKAPE and Escherichia coli at a large teaching hospital in Rome, a 9-year analysis (2007-2015)","volume":"37","author":"De Angelis","year":"2018","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"B7","doi-asserted-by":"publisher","DOI":"10.3390\/medicines12030017","article-title":"Multi-drug resistant gram-negative sepsis in neonates: the special role of ceftazidime\/avibactam and ceftolozane\/tazobactam","volume":"12","author":"Dermitzaki","year":"2025","journal-title":"Medicines (Basel)"},{"key":"B8","doi-asserted-by":"publisher","DOI":"10.3390\/antibiotics13121139","article-title":"National multicenter study on the prevalence of carbapenemase-producing Enterobacteriaceae in the post-COVID-19 era in Argentina: the RECAPT-AR study","volume":"13","author":"Echegorry","year":"2024","journal-title":"Antibiotics (Basel)"},{"key":"B9","doi-asserted-by":"publisher","first-page":"929","DOI":"10.1097\/INF.0000000000000339","article-title":"Epidemiology and clinical outcomes of multidrug-resistant, gram-negative bloodstream infections in a European tertiary pediatric hospital during a 12-month period","volume":"33","author":"Folgori","year":"2014","journal-title":"Pediatr. Infect. Dis. J."},{"key":"B10","doi-asserted-by":"publisher","DOI":"10.3390\/antibiotics15030273","article-title":"Epidemiological insights into carbapenem-resistant Enterobacterales throughout the COVID-19 pandemic in Buenos Aires, Argentina","volume":"15","author":"Gonz\u00e1lez-Espinosa","year":"2026","journal-title":"Antibiotics (Basel)"},{"key":"B11","doi-asserted-by":"publisher","first-page":"583","DOI":"10.1007\/s15010-023-02036-5","article-title":"Decrease in vancomycin MICs and prevalence of hGISA in MRSA and MSSA isolates from a German pediatric tertiary care center","volume":"51","author":"Haas","year":"2023","journal-title":"Infection"},{"key":"B12","doi-asserted-by":"publisher","first-page":"819","DOI":"10.2147\/IDR.S493139","article-title":"Diversity in adaptive evolution of methicillin-resistant Staphylococcus aureus clinical isolates under exposure to continuous linezolid stress in vitro","volume":"18","author":"Han","year":"2025","journal-title":"Infect. Drug Resist."},{"key":"B13","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2020.00908","article-title":"Dynamic changes of Staphylococcus aureus susceptibility to vancomycin, teicoplanin, and linezolid in a central teaching hospital in Shanghai, China, 2008-2018","volume":"11","author":"Jian","year":"2020","journal-title":"Front. Microbiol."},{"key":"B14","doi-asserted-by":"publisher","first-page":"1803","DOI":"10.1093\/cid\/ciy378","article-title":"Difficult-to-treat resistance in gram-negative bacteremia at 173 US hospitals: retrospective cohort analysis of prevalence, predictors, and outcome of resistance to all first-line agents","volume":"67","author":"Kadri","year":"2018","journal-title":"Clin. Infect. Dis."},{"key":"B15","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1016\/j.cmi.2019.10.031","article-title":"Burden of bacterial bloodstream infection-a brief update on epidemiology and significance of multidrug-resistant pathogens","volume":"26","author":"Kern","year":"2020","journal-title":"Clin. Microbiol. Infect."},{"key":"B16","doi-asserted-by":"publisher","DOI":"10.1017\/S0950268822001492","article-title":"Burden of multidrug and extensively drug-resistant ESKAPEE pathogens in a secondary hospital care setting in Greece","volume":"150","author":"Kritsotakis","year":"2022","journal-title":"Epidemiol. Infect."},{"key":"B17","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2025.1685606","article-title":"COVID-19 pandemic increased ESKAPEEc bloodstream infections and amplified carbapenem resistance in Chinese children: a multicenter surveillance study (2016-2023)","volume":"15","author":"Li","year":"2025","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"B18","doi-asserted-by":"publisher","DOI":"10.3389\/fpubh.2024.1419344","article-title":"Multiple impacts of the COVID-19 pandemic and antimicrobial stewardship on antimicrobial resistance in nosocomial infections: an interrupted time series analysis","volume":"12","author":"Li","year":"2024","journal-title":"Front. Public Health"},{"key":"B19","doi-asserted-by":"publisher","first-page":"1026","DOI":"10.1097\/CCM.0000000000004329","article-title":"Risk of mortality in immunocompromised children with severe sepsis and septic shock","volume":"48","author":"Lindell","year":"2020","journal-title":"Crit. Care Med."},{"key":"B20","first-page":"937","article-title":"Distribution and antimicrobial resistance of clinical isolates from pediatric blood specimens in Sichuan Province, 2016-2023","volume":"50","author":"Long","year":"2025","journal-title":"Chin. J. Antibiotics"},{"key":"B21","doi-asserted-by":"publisher","first-page":"6297","DOI":"10.2147\/IDR.S426000","article-title":"Bacterial etiology and antimicrobial resistance pattern of pediatric bloodstream infections in Beijing, 2015-2019","volume":"16","author":"Lyu","year":"2023","journal-title":"Infect. Drug Resist."},{"key":"B22","doi-asserted-by":"publisher","DOI":"10.1093\/ofid\/ofz503","article-title":"ESKAPE pathogens in bloodstream infections are associated with higher cost and mortality but can be predicted using diagnoses upon admission","volume":"6","author":"Marturano","year":"2019","journal-title":"Open Forum Infect. Dis."},{"key":"B23","doi-asserted-by":"publisher","first-page":"5815","DOI":"10.2147\/IDR.S426326","article-title":"Use of ceftazidime-avibactam for suspected or confirmed carbapenem-resistant organisms in children: a retrospective study","volume":"16","author":"Meng","year":"2023","journal-title":"Infect. Drug Resist."},{"key":"B24","doi-asserted-by":"publisher","first-page":"598","DOI":"10.1038\/s41579-024-01054-w","article-title":"ESKAPE pathogens: antimicrobial resistance, epidemiology, clinical impact and therapeutics","volume":"22","author":"Miller","year":"2024","journal-title":"Nat. Rev. Microbiol."},{"key":"B25","doi-asserted-by":"publisher","DOI":"10.1128\/spectrum.01007-26","article-title":"Difficult-to-treat resistance (DTR), treatment, and outcomes of carbapenem-resistant Enterobacterales infections in the setting of IMP-type carbapenemase predominance in Japan","volume":"14","author":"Ohyama","year":"2026","journal-title":"Microbiol. Spectr."},{"key":"B26","doi-asserted-by":"publisher","first-page":"2459","DOI":"10.1093\/cid\/ciaa530","article-title":"Bacterial and fungal coinfection in individuals with coronavirus: a rapid review to support COVID-19 antimicrobial prescribing","volume":"71","author":"Rawson","year":"2020","journal-title":"Clin. Infect. Dis."},{"key":"B27","doi-asserted-by":"publisher","first-page":"373","DOI":"10.1186\/s12879-024-09260-w","article-title":"Bacterial etiology and antimicrobial resistance pattern of pediatric bloodstream infections: a 5-year experience in an Iranian referral hospital","volume":"24","author":"Sajedi Moghaddam","year":"2024","journal-title":"BMC Infect. Dis."},{"key":"B28","doi-asserted-by":"publisher","DOI":"10.3390\/antibiotics14090916","article-title":"The impact of COVID-19 on the epidemiology of carbapenem resistance","volume":"14","author":"Sakagianni","year":"2025","journal-title":"Antibiotics (Basel)"},{"key":"B29","doi-asserted-by":"publisher","first-page":"187","DOI":"10.1093\/cid\/ciac268","article-title":"Infectious Diseases Society of America 2022 guidance on the treatment of extended-spectrum \u03b2-lactamase producing Enterobacterales (ESBL-E), carbapenem-resistant Enterobacterales (CRE), and Pseudomonas aeruginosa with difficult-to-treat resistance (DTR-P. aeruginosa)","volume":"75","author":"Tamma","year":"2022","journal-title":"Clin. Infect. Dis."},{"key":"B30","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3201\/eid2811.220415","article-title":"Increased detection of carbapenemase-producing Enterobacterales bacteria in Latin America and the Caribbean during the COVID-19 pandemic","volume":"28","author":"Thomas","year":"2022","journal-title":"Emerg. Infect. Dis."},{"key":"B31","first-page":"1275","article-title":"The dual impact of the COVID-19 pandemic on nosocomial infections and antimicrobial resistance","volume":"32","author":"Wang","year":"2022","journal-title":"Chin. J. Nosocomiology"},{"key":"B32","doi-asserted-by":"publisher","first-page":"469","DOI":"10.1016\/j.ajic.2020.10.019","article-title":"Unintended consequences of infection prevention and control measures during COVID-19 pandemic","volume":"49","author":"Wee","year":"2021","journal-title":"Am. J. Infect. Control"},{"key":"B33","doi-asserted-by":"publisher","DOI":"10.1128\/aac.01865-24","article-title":"Emergence of carbapenem-resistant Acinetobacter baumannii clonal complex 2 in multiple hospitals in S\u00e3o Paulo state, Brazil","volume":"69","author":"Yamada","year":"2025","journal-title":"Antimicrob. Agents Chemother."},{"key":"B34","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2024.1391929","article-title":"Impacts of COVID-19 pandemic on culture-proven sepsis in neonates","volume":"14","author":"Yang","year":"2024","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1016\/j.jhin.2023.06.003","article-title":"Risk factors for bloodstream infection in paediatric haematopoietic stem cell transplantation: a systematic review and meta-analysis","volume":"139","author":"Yang","year":"2023","journal-title":"J. Hosp. Infect."},{"key":"B36","doi-asserted-by":"publisher","first-page":"61","DOI":"10.1186\/s13756-019-0499-1","article-title":"Shifting trends and age distribution of ESKAPEEc resistance in bloodstream infection, Southwest China, 2012-2017","volume":"8","author":"Yang","year":"2019","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"B37","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2023.1163312","article-title":"Bacterial distribution and drug resistance in blood samples of children in Jiangxi Region, 2017-2021","volume":"13","author":"Zhou","year":"2023","journal-title":"Front. Cell. Infect. Microbiol."}],"container-title":["Frontiers in Cellular and Infection Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2026.1914448\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T04:45:36Z","timestamp":1790829936000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2026.1914448\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,10,1]]},"references-count":37,"alternative-id":["10.3389\/fcimb.2026.1914448"],"URL":"https:\/\/doi.org\/10.3389\/fcimb.2026.1914448","relation":{},"ISSN":["2235-2988"],"issn-type":[{"value":"2235-2988","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,10,1]]},"article-number":"1914448"}}