{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T16:24:18Z","timestamp":1790871858976,"version":"4.1.0"},"reference-count":47,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2024,7,17]],"date-time":"2024-07-17T00:00:00Z","timestamp":1721174400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["72374228, 72074234, 72204275"],"award-info":[{"award-number":["72374228, 72074234, 72204275"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100001547","name":"China Medical Board","doi-asserted-by":"publisher","award":["CMB-OC-19-337"],"award-info":[{"award-number":["CMB-OC-19-337"]}],"id":[{"id":"10.13039\/100001547","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Public Health"],"abstract":"<jats:sec><jats:title>Objectives<\/jats:title><jats:p>The emergency response to the COVID-19 pandemic may disrupt hospital management activities of antimicrobial resistance (AMR). This study aimed to determine the changing AMR trend over the period in China when stringent COVID-19 response measures were implemented.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>This retrospective study was conducted in a designated hospital for COVID-19 patients in Guangzhou, China from April 2018 to September 2021. The prevalence of 13 antimicrobial-resistant bacteria was compared before and after the COVID-19 responses through Chi-square tests. Interrupted time series (ITS) models on the weekly prevalence of AMR were established to determine the changing trend. Controlled ITS models were performed to compare the differences between subgroups.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>A total of 10,134 isolates over 1,265\u2009days were collected. And antimicrobial-resistant strains presented in 38.6% of the testing isolates. The weekly AMR prevalence decreased by 0.29 percentage point (95% CI [0.05\u20130.80]) after antimicrobial stewardship (AMS) policy, despite an increase in the prevalence of penicillin-resistant <jats:italic>Streptococcus pneumoniae<\/jats:italic> (from 0\/43 to 15\/43, <jats:italic>p<\/jats:italic>\u2009&amp;lt;\u20090.001), carbapenem-resistant <jats:italic>Escherichia coli<\/jats:italic> (from 20\/1254 to 41\/1184, <jats:italic>p<\/jats:italic>\u2009=\u20090.005), and carbapenem-resistant <jats:italic>Klebsiella pneumoniae<\/jats:italic> (from 93\/889 to 114\/828, <jats:italic>p<\/jats:italic>\u2009=\u20090.042). And the changing trend did not vary by gender (male vs. female), age (&amp;lt;65 vs. \u226565\u2009years), service setting (outpatient vs. inpatient), care unit (ICU vs. non-ICU), the primary site of infection (Lung vs. others), and Gram type of bacteria (positive vs. negative).<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusion<\/jats:title><jats:p>The response to COVID-19 did not lead to an increase in overall AMR; however, it appears that management strategy on the prudent use of antimicrobials likely contributed to a sizable long-term drop. The frequency of several multidrug-resistant bacteria continues to increase after the COVID-19 epidemic. It is crucial to continue to monitor AMR when COVID-19 cases have surged in China after the relaxation of restriction measures.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fpubh.2024.1419344","type":"journal-article","created":{"date-parts":[[2024,7,17]],"date-time":"2024-07-17T04:33:11Z","timestamp":1721190791000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":9,"title":["Multiple impacts of the COVID-19 pandemic and antimicrobial stewardship on antimicrobial resistance in nosocomial infections: an interrupted time series analysis"],"prefix":"10.3389","volume":"12","author":[{"given":"Weibin","family":"Li","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xinyi","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chaojie","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xu","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lin","family":"Shi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yingchao","family":"Zeng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Haohai","family":"Xia","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jia","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Manzhi","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shifang","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaojie","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bo","family":"Hu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lianping","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2024,7,17]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"e398","DOI":"10.1016\/S2542-5196(18)30186-4","article-title":"Anthropological and socioeconomic factors contributing to global antimicrobial resistance: a univariate and multivariable analysis","volume":"2","author":"Collignon","year":"2018","journal-title":"Lancet Planet Health"},{"key":"ref2","doi-asserted-by":"publisher","first-page":"2439","DOI":"10.1016\/S0140-6736(24)00862-6","article-title":"Burden of bacterial antimicrobial resistance in low-income and middle-income countries avertible by existing interventions: an evidence review and modelling analysis","volume":"403","author":"Lewnard","year":"2024","journal-title":"Lancet (London, England)"},{"key":"ref3","doi-asserted-by":"publisher","first-page":"629","DOI":"10.1016\/S0140-6736(21)02724-0","article-title":"Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis","volume":"399","year":"2022","journal-title":"Lancet (London, England)"},{"key":"ref4","doi-asserted-by":"publisher","first-page":"295","DOI":"10.1016\/j.jhin.2020.01.003","article-title":"Direct medical burden of 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aeruginosa)","volume":"72","author":"Tamma","year":"2021","journal-title":"Clin Infect Dis"},{"key":"ref39","doi-asserted-by":"publisher","first-page":"256","DOI":"10.1016\/j.jinf.2023.01.008","article-title":"Changes of Klebsiella pneumoniae infection and carbapenem resistance in ICU elderly infected patients before and after the COVID-19 pandemic in Zhengzhou, China","volume":"86","author":"Ding","year":"2023","journal-title":"J Infect"},{"key":"ref40","doi-asserted-by":"publisher","first-page":"256","DOI":"10.1016\/j.jinf.2023.01.003","article-title":"Klebsiella pneumoniae infection in the paediatric population before and after the COVID-19 pandemic in Shenzhen, China","volume":"86","author":"Patil","year":"2023","journal-title":"J Infect"},{"key":"ref41","doi-asserted-by":"publisher","first-page":"1533","DOI":"10.1016\/j.ajic.2020.09.015","article-title":"Carbapenemase-producing Enterobacterales outbreak: another dark side of COVID-19","volume":"48","author":"Farfour","year":"2020","journal-title":"Am J Infect Control"},{"key":"ref42","doi-asserted-by":"publisher","first-page":"106179","DOI":"10.1016\/j.ijantimicag.2020.106179","article-title":"Emerging co-pathogens: New Delhi Metallo-beta-lactamase producing Enterobacterales infections in new York City COVID-19 patients","volume":"56","author":"Nori","year":"2020","journal-title":"Int J Antimicrob Agents"},{"key":"ref43","doi-asserted-by":"publisher","first-page":"2744","DOI":"10.3390\/jcm9092744","article-title":"Antimicrobial stewardship program, COVID-19, and infection control: spread of Carbapenem-resistant Klebsiella Pneumoniae colonization in ICU COVID-19 patients what did not work?","volume":"9","author":"Tiri","year":"2020","journal-title":"J Clin Med"},{"key":"ref44","doi-asserted-by":"publisher","first-page":"1127","DOI":"10.3390\/antibiotics10091127","article-title":"A study in a regional Hospital of a mid-Sized Spanish City Indicates a major increase in infection\/colonization by Carbapenem-resistant Bacteria, coinciding with the COVID-19 pandemic","volume":"10","author":"Cano-Mart\u00edn","year":"2021","journal-title":"Antibiotics (Basel, Switzerland)"},{"key":"ref45","doi-asserted-by":"publisher","first-page":"147","DOI":"10.1016\/j.jhin.2021.09.011","article-title":"Impact of the COVID-19 pandemic on the surveillance of antimicrobial resistance","volume":"117","author":"Hirabayashi","year":"2021","journal-title":"J Hosp Infect"},{"key":"ref46","doi-asserted-by":"publisher","first-page":"383","DOI":"10.1038\/d41586-022-04382-0","article-title":"China is relaxing its zero-COVID policy - here's what scientists think","volume":"612","author":"Mallapaty","year":"2022","journal-title":"Nature"},{"key":"ref47","doi-asserted-by":"crossref","DOI":"10.1093\/trstmh\/trab048","article-title":"Key considerations on the potential impacts of the COVID-19 pandemic on antimicrobial resistance research and 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