{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,19]],"date-time":"2026-10-19T21:56:18Z","timestamp":1792446978429,"version":"4.5.0"},"reference-count":35,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2023,6,22]],"date-time":"2023-06-22T00:00:00Z","timestamp":1687392000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Antibiotics"],"abstract":"<jats:p>The COVID-19 pandemic led to unprecedented stress on healthcare systems worldwide, forming settings of concern for increasing antimicrobial resistance. We investigated the impact of SARS-CoV-2 preventive measures against healthcare-associated infections (HAIs) from antibiotic-resistant bacteria in two tertiary-care hospitals. We compared infection rates between March 2019 and February 2020 (pre-intervention period) and March 2020 and February 2021 (COVID-19 intervention period) from drug-resistant ESKAPEE bacteria (methicillin-resistant Staphylococcus aureus; vancomycin-resistant Enterococci; carbapenem-resistant Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, Enterobacter species and Escherichia coli). Over 24 months, 586 drug-resistant ESKAPEE HAIs occurred in 439 patients (0.3% of 179,629 inpatients) with a mean age of 63 years, with 43% being treated in intensive care units (ICUs), and having a 45% inpatient mortality rate. Interrupted time series analysis revealed increasing infection rates before the intervention that were sharply interrupted by abrupt drops for most pathogens and henceforth remained stable in the ICUs but progressively increased in ordinary wards. In the ICUs, the pooled infection rate was 44% lower over the intervention period compared to the pre-intervention period (incidence rate ratio (IRR) 0.56, 95%CI 0.41\u20130.75, p &lt; 0.001). Pooled infection rates in the wards were slightly higher over the COVID-19 period (IRR 1.12, 95%CI 0.87\u20131.45, p = 0.368). The findings confirmed the ancillary beneficial impact of the enhanced bundle of transmission-based precautions adopted against SARS-CoV-2 in rapidly constraining antimicrobial-resistant HAIs in two Greek hospitals.<\/jats:p>","DOI":"10.3390\/antibiotics12071088","type":"journal-article","created":{"date-parts":[[2023,6,23]],"date-time":"2023-06-23T01:54:56Z","timestamp":1687485296000},"page":"1088","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Impact of SARS-CoV-2 Preventive Measures against Healthcare-Associated Infections from Antibiotic-Resistant ESKAPEE Pathogens: A Two-Center, Natural Quasi-Experimental Study in Greece"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-7135-3258","authenticated-orcid":false,"given":"Emmanouil","family":"Bolikas","sequence":"first","affiliation":[{"name":"Laboratory of Biostatistics, School of Medicine, University of Crete, 71003 Heraklion, Greece"},{"name":"Infection Control Committee, Venizeleio-Pananeio General Hospital, 71409 Heraklion, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eirini","family":"Astrinaki","sequence":"additional","affiliation":[{"name":"Infection Control Committee, University Hospital of Heraklion, 71110 Heraklion, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Evangelia","family":"Panagiotaki","sequence":"additional","affiliation":[{"name":"Infection Control Committee, Venizeleio-Pananeio General Hospital, 71409 Heraklion, Greece"},{"name":"Department of Clinical Microbiology, Venizeleio-Pananeio General Hospital, 71409 Heraklion, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Efsevia","family":"Vitsaxaki","sequence":"additional","affiliation":[{"name":"Infection Control Committee, University Hospital of Heraklion, 71110 Heraklion, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stamatina","family":"Saplamidou","sequence":"additional","affiliation":[{"name":"Infection Control Committee, University Hospital of Heraklion, 71110 Heraklion, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ioannis","family":"Drositis","sequence":"additional","affiliation":[{"name":"Infection Control Committee, Venizeleio-Pananeio General Hospital, 71409 Heraklion, Greece"},{"name":"Department of Medical Oncology, Venizeleio-Pananeio General Hospital, 71409 Heraklion, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dimitra","family":"Stafylaki","sequence":"additional","affiliation":[{"name":"Department of Clinical Microbiology and Microbial Pathogenesis, University Hospital of Heraklion, 71110 Heraklion, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Georgios","family":"Chamilos","sequence":"additional","affiliation":[{"name":"Infection Control Committee, University Hospital of Heraklion, 71110 Heraklion, Greece"},{"name":"Department of Clinical Microbiology and Microbial Pathogenesis, University Hospital of Heraklion, 71110 Heraklion, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Achilleas","family":"Gikas","sequence":"additional","affiliation":[{"name":"Infection Control Committee, University Hospital of Heraklion, 71110 Heraklion, Greece"},{"name":"Department of Internal Medicine, School of Medicine, University of Crete, 71003 Heraklion, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0255-5926","authenticated-orcid":false,"given":"Diamantis P.","family":"Kofteridis","sequence":"additional","affiliation":[{"name":"Infection Control Committee, University Hospital of Heraklion, 71110 Heraklion, Greece"},{"name":"Department of Internal Medicine, School of Medicine, University of Crete, 71003 Heraklion, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9526-3852","authenticated-orcid":false,"given":"Evangelos I.","family":"Kritsotakis","sequence":"additional","affiliation":[{"name":"Laboratory of Biostatistics, School of Medicine, University of Crete, 71003 Heraklion, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,6,22]]},"reference":[{"key":"ref_1","unstructured":"Antimicrobial Resistance Collaborators (2022). Global Burden of Bacterial Antimicrobial Resistance in 2019: A Systematic Analysis. Lancet, 399, 629\u2013655."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"e00181-19","DOI":"10.1128\/CMR.00181-19","article-title":"Antimicrobial Resistance in ESKAPE Pathogens","volume":"33","author":"Forde","year":"2020","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Kalpana, S., Lin, W.-Y., Wang, Y.-C., Fu, Y., Lakshmi, A., and Wang, H.-Y. (2023). Antibiotic Resistance Diagnosis in ESKAPE Pathogens-A Review on Proteomic Perspective. Diagnostics, 13.","DOI":"10.3390\/diagnostics13061014"},{"key":"ref_4","doi-asserted-by":"crossref","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":"ref_5","doi-asserted-by":"crossref","first-page":"3045","DOI":"10.1093\/jac\/dkab300","article-title":"Impact of the COVID-19 Pandemic on the Surveillance, Prevention and Control of Antimicrobial Resistance: A Global Survey","volume":"76","author":"Tomczyk","year":"2021","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1657","DOI":"10.1093\/cid\/ciaa773","article-title":"Coronavirus Disease 2019 and Antimicrobial Resistance: Parallel and Interacting Health Emergencies","volume":"72","author":"Nieuwlaat","year":"2021","journal-title":"Clin. Infect. Dis."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"(2023, April 15). US Centers for Disease Control and Prevention, National Center for Emerging and Zoonotic Infectious Diseases, Division of Healthcare Quality Promotion. COVID-19: U.S. Impact on Antimicrobial Resistance, Special Report 2022. Available online: https:\/\/doi.org\/10.15620\/cdc:117915.","DOI":"10.15620\/cdc:117915"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1748","DOI":"10.1093\/cid\/ciab688","article-title":"The Impact of Coronavirus Disease 2019 (COVID-19) on Healthcare-Associated Infections","volume":"74","author":"Baker","year":"2022","journal-title":"Clin. Infect. Dis."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"320","DOI":"10.1016\/j.jiph.2022.12.022","article-title":"Impact of COVID-19 Pandemic on Multidrug Resistant Gram Positive and Gram Negative Pathogens: A Systematic Review","volume":"16","author":"Abubakar","year":"2023","journal-title":"J. Infect. Public Health"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"302","DOI":"10.1016\/j.cmi.2022.12.006","article-title":"Antibiotic Resistance Associated with the COVID-19 Pandemic: A Systematic Review and Meta-Analysis","volume":"29","author":"Langford","year":"2023","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Yang, X., Liu, X., Li, W., Shi, L., Zeng, Y., Xia, H., Huang, Q., Li, J., Li, X., and Hu, B. (2023). Epidemiological Characteristics and Antimicrobial Resistance Changes of Carbapenem-Resistant Klebsiella Pneumoniae and Acinetobacter Baumannii under the COVID-19 Outbreak: An Interrupted Time Series Analysis in a Large Teaching Hospital. Antibiotics, 12.","DOI":"10.3390\/antibiotics12030431"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Segala, F.V., Pafundi, P.C., Masciocchi, C., Fiori, B., Taddei, E., Antenucci, L., De Angelis, G., Guerriero, S., Pastorino, R., and Damiani, A. (2023). Incidence of Bloodstream Infections Due to Multidrug-Resistant Pathogens in Ordinary Wards and Intensive Care Units before and during the COVID-19 Pandemic: A Real-Life, Retrospective Observational Study. Infection, 1\u20139.","DOI":"10.1007\/s15010-023-02000-3"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"e13687","DOI":"10.1111\/eci.13687","article-title":"Protective Effect of SARS-CoV-2 Preventive Measures against ESKAPE and Escherichia Coli Infections","volume":"51","author":"Gaspari","year":"2021","journal-title":"Eur. J. Clin. Investig."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"317","DOI":"10.2147\/IDR.S147459","article-title":"Prevalence, Incidence Burden, and Clinical Impact of Healthcare-Associated Infections and Antimicrobial Resistance: A National Prevalent Cohort Study in Acute Care Hospitals in Greece","volume":"10","author":"Kritsotakis","year":"2017","journal-title":"Infect. Drug Resist."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Polemis, M., Mandilara, G., Pappa, O., Argyropoulou, A., Perivolioti, E., Koudoumnakis, N., Pournaras, S., Vasilakopoulou, A., Vourli, S., and Katsifa, H. (2021). COVID-19 and Antimicrobial Resistance: Data from the Greek Electronic System for the Surveillance of Antimicrobial Resistance-WHONET-Greece (January 2018\u2013March 2021). Life, 11.","DOI":"10.3390\/life11100996"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"979","DOI":"10.1038\/nrmicro1047","article-title":"Epidemiological Interpretation of Antibiotic Resistance Studies\u2014What Are We Missing?","volume":"2","author":"Schwaber","year":"2004","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"190","DOI":"10.1016\/j.jgar.2018.04.015","article-title":"Temporal Trends and Patterns in Antimicrobial-Resistant Gram-Negative Bacteria Implicated in Intensive Care Unit-Acquired Infections: A Cohort-Based Surveillance Study in Istanbul, Turkey","volume":"14","author":"Durdu","year":"2018","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"901","DOI":"10.1086\/521255","article-title":"Statistical Analysis and Application of Quasi Experiments to Antimicrobial Resistance Intervention Studies","volume":"45","author":"Shardell","year":"2007","journal-title":"Clin. Infect. Dis."},{"key":"ref_19","first-page":"348","article-title":"Interrupted Time Series Regression for the Evaluation of Public Health Interventions: A Tutorial","volume":"46","author":"Bernal","year":"2017","journal-title":"Int. J. Epidemiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"757","DOI":"10.2147\/RMHP.S275831","article-title":"Three Statistical Approaches for Assessment of Intervention Effects: A Primer for Practitioners","volume":"14","author":"Li","year":"2021","journal-title":"Risk Manag. Healthc. Policy"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"364","DOI":"10.12788\/jhm.3543","article-title":"Methodological Progress Note: Interrupted Time Series","volume":"16","author":"Mahant","year":"2021","journal-title":"J. Hosp. Med."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Ioannou, P., Astrinaki, E., Vitsaxaki, E., Bolikas, E., Christofaki, D., Salvaraki, A., Lagoudaki, E., Ioannidou, E., Karakonstantis, S., and Saplamidou, S. (2022). A Point Prevalence Survey of Healthcare-Associated Infections and Antimicrobial Use in Public Acute Care Hospitals in Crete, Greece. Antibiotics, 11.","DOI":"10.3390\/antibiotics11091258"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1016\/j.ajic.2020.09.013","article-title":"The Impact of the COVID-19 Pandemic on Healthcare Acquired Infections with Multidrug Resistant Organisms","volume":"49","author":"Cole","year":"2021","journal-title":"Am. J. Infect. Control"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/j.ijid.2020.12.072","article-title":"The Impact of Universal Face Masking and Enhanced Hand Hygiene for COVID-19 Disease Prevention on the Incidence of Hospital-Acquired Infections in a Taiwanese Hospital","volume":"104","author":"Lo","year":"2021","journal-title":"Int. J. Infect. Dis."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1263","DOI":"10.1007\/s13304-020-00884-6","article-title":"Impact of Lockdown for SARS-CoV-2 (COVID-19) on Surgical Site Infection Rates: A Monocentric Observational Cohort Study","volume":"72","author":"Losurdo","year":"2020","journal-title":"Updat. Surg."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1772","DOI":"10.1016\/j.cmi.2021.06.001","article-title":"The Interface between COVID-19 and Bacterial Healthcare-Associated Infections","volume":"27","year":"2021","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1097","DOI":"10.1016\/j.ajic.2018.04.217","article-title":"Implementation of Multimodal Infection Control and Hand Hygiene Strategies in Acute-Care Hospitals in Greece: A Cross-Sectional Benchmarking Survey","volume":"46","author":"Kritsotakis","year":"2018","journal-title":"Am. J. Infect. Control"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"e79","DOI":"10.1097\/SLA.0000000000003998","article-title":"The Consequences of Delaying Elective Surgery: Surgical Perspective","volume":"272","author":"Fu","year":"2020","journal-title":"Ann. Surg."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"103123","DOI":"10.1016\/j.iccn.2021.103123","article-title":"The Impact of Family Visitor Restrictions on Healthcare Workers in the ICU during the COVID-19 Pandemic","volume":"68","author":"Wendlandt","year":"2022","journal-title":"Intensive Crit. Care Nurs."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1000","DOI":"10.1093\/jac\/dkad035","article-title":"A Carbapenem-Focused Antimicrobial Stewardship Programme Implemented during the COVID-19 Pandemic in a Setting of High Endemicity for Multidrug-Resistant Gram-Negative Bacteria","volume":"78","author":"Spernovasilis","year":"2023","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"270","DOI":"10.1038\/s41429-023-00601-6","article-title":"Persistence of Resistance: A Panel Data Analysis of the Effect of Antibiotic Usage on the Prevalence of Resistance","volume":"76","author":"Rahman","year":"2023","journal-title":"J. Antibiot."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1016\/j.cmi.2019.08.007","article-title":"How to Start an Antimicrobial Stewardship Programme in a Hospital","volume":"26","author":"Mendelson","year":"2020","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_33","unstructured":"European Centre for Disease Prevention and Control (2023, April 15). Point Prevalence Survey of Healthcare-Associated Infections and Antimicrobial Use in European Acute Care Hospitals\u2014Protocol Version 5.3. Available online: https:\/\/www.ecdc.europa.eu\/en\/publications-data\/point-prevalence-survey-healthcare-associated-infections-and-antimicrobial-use-3."},{"key":"ref_34","first-page":"188","article-title":"Charlson Comorbidity Index: ICD-9 Update and ICD-10 Translation","volume":"12","author":"Glasheen","year":"2019","journal-title":"Am. Health Drug Benefits"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"361","DOI":"10.2105\/AJPH.94.3.361","article-title":"Improving the Reporting Quality of Nonrandomized Evaluations of Behavioral and Public Health Interventions: The TREND Statement","volume":"94","author":"Lyles","year":"2004","journal-title":"Am. J. Public Health"}],"container-title":["Antibiotics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-6382\/12\/7\/1088\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:58:35Z","timestamp":1760126315000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-6382\/12\/7\/1088"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,6,22]]},"references-count":35,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2023,7]]}},"alternative-id":["antibiotics12071088"],"URL":"https:\/\/doi.org\/10.3390\/antibiotics12071088","relation":{},"ISSN":["2079-6382"],"issn-type":[{"value":"2079-6382","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,6,22]]}}}