{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,23]],"date-time":"2026-10-23T20:55:02Z","timestamp":1792788902745,"version":"4.5.0"},"reference-count":49,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2023,2,2]],"date-time":"2023-02-02T00:00:00Z","timestamp":1675296000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"project PDI-PFE-CDI 2021","award":["40PFE\/30.12.2021"],"award-info":[{"award-number":["40PFE\/30.12.2021"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Antibiotics"],"abstract":"<jats:p>Although the COVID-19 pandemic has held the spotlight over the past years, the antimicrobial resistance (AMR) phenomenon continues to develop in an alarming manner. The lack of strict antibiotic regulation added to the overuse of antimicrobials fueled the AMR pandemic. This paper aims to analyze and identify the impact of the COVID-19 pandemic on antibiotic resistance patterns of Enterococcus spp. The study was designed as a retrospective observational study. Enterococcus spp. infections data were collected from one academic hospital in Cluj-Napoca, Romania over 18 months. A statistical analysis was performed to compare antibiotic resistance phenotypes identified. We recorded an increase in the isolation rates of Enterococcus spp. strains, from 26 isolates (26.53%) during Period A (November 2020\u2013April 2021) to 42 strains (42.85%) during Period C (November 2021\u2013April 2022). The number of strains with resistance to vancomycin increased from 8 during Period A to 17 during Period C. Of the total 36 strains with resistance to vancomycin, 25 were identified as E. faecium. SARS-CoV-2 patients (n = 29) proved to be at risk to develop an E. faecium co-infection (n = 18). We observed that strains with resistance to ampicillin (n = 20) and vancomycin (n = 15) are more often isolated from these patients. All changes identified in our study are to be considered in the light of COVID-19 pandemic, highlighting the threatening AMR phenomenon in Romania. Further studies should be performed to quantify the worldwide effects of these pandemics.<\/jats:p>","DOI":"10.3390\/antibiotics12020312","type":"journal-article","created":{"date-parts":[[2023,2,3]],"date-time":"2023-02-03T02:35:10Z","timestamp":1675391710000},"page":"312","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":9,"title":["A Tale of Two Pandemics: Antimicrobial Resistance Patterns of Enterococcus spp. in COVID-19 Era"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3930-5920","authenticated-orcid":false,"given":"Dan Alexandru","family":"Toc","sequence":"first","affiliation":[{"name":"Department of Microbiology, Iuliu Hatieganu University of Medicine and Pharmacy, 8 Victor Babe\u0219 Street, 400000 Cluj-Napoca, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8881-7688","authenticated-orcid":false,"given":"Alexandru","family":"Botan","sequence":"additional","affiliation":[{"name":"Faculty of Medicine, Iuliu Hatieganu University of Medicine and Pharmacy, 8 Victor Babe\u0219 Street, 400000 Cluj-Napoca, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ana Maria Cristia","family":"Botescu","sequence":"additional","affiliation":[{"name":"Faculty of Medicine, Iuliu Hatieganu University of Medicine and Pharmacy, 8 Victor Babe\u0219 Street, 400000 Cluj-Napoca, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vlad Dumitru","family":"Brata","sequence":"additional","affiliation":[{"name":"Faculty of Medicine, Iuliu Hatieganu University of Medicine and Pharmacy, 8 Victor Babe\u0219 Street, 400000 Cluj-Napoca, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ioana Alina","family":"Colosi","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Iuliu Hatieganu University of Medicine and Pharmacy, 8 Victor Babe\u0219 Street, 400000 Cluj-Napoca, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carmen","family":"Costache","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Iuliu Hatieganu University of Medicine and Pharmacy, 8 Victor Babe\u0219 Street, 400000 Cluj-Napoca, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lia Monica","family":"Junie","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Iuliu Hatieganu University of Medicine and Pharmacy, 8 Victor Babe\u0219 Street, 400000 Cluj-Napoca, Romania"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,2,2]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1016\/S1473-3099(11)70316-4","article-title":"The crisis of no new antibiotics--what is the way forward?","volume":"12","author":"Piddock","year":"2012","journal-title":"Lancet Infect. Dis."},{"key":"ref_2","first-page":"277","article-title":"The antibiotic resistance crisis: Part 1: Causes and threats","volume":"40","author":"Ventola","year":"2015","journal-title":"P T A Peer-Rev. J. Formul. Manag."},{"key":"ref_3","unstructured":"Shaban, R.Z., Cruickshank, M., and Christiansen, K. (2013). National Surveillance and Reporting of Antimicrobial Resistance and Antibiotic usage for Human Health in Australia."},{"key":"ref_4","unstructured":"Nelson, N., Joshi, M., and Kirika, R. (2009). Submitted to the US Agency for International Development by the Strengthening Pharmaceutical Systems (SPS) Program, Management Sciences for Health."},{"key":"ref_5","unstructured":"World Health Organization (2015). Antibiotic Resistance: Multi-Country Public Awareness Survey, World Health Organization."},{"key":"ref_6","unstructured":"European Centre for Disease Prevention and Control (2022). Surveillance of Antimicrobial Resistance in Europe, 2021 Data, European Centre for Disease Prevention and Control."},{"key":"ref_7","unstructured":"(2018). European Centre for Disease Prevention and Control ECDC Country Visit to Romania to Discuss Antimicrobial Resistance Issues."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Toc, D.A., Butiuc-Keul, A.L., Iordache, D., Botan, A., Mihaila, R.M., Costache, C.A., Colosi, I.A., Chiorean, C., Neagoe, D.S., and Gheorghiu, L. (2022). Descriptive Analysis of Circulating Antimicrobial Resistance Genes in Vancomycin-Resistant Enterococcus (VRE) during the COVID-19 Pandemic. Biomedicines, 10.","DOI":"10.3390\/biomedicines10051122"},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Axente, C., Licker, M., Moldovan, R., Hogea, E., Muntean, D., Horhat, F., Bedreag, O., Sandesc, D., Papurica, M., and Dugaesescu, D. (2017). Antimicrobial consumption, costs and resistance patterns: A two year prospective study in a Romanian intensive care unit. BMC Infect. Dis., 17.","DOI":"10.1186\/s12879-017-2440-7"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"795","DOI":"10.1016\/S2213-2600(21)00138-7","article-title":"COVID-19-associated Aspergillus tracheobronchitis: The interplay between viral tropism, host defence, and fungal invasion","volume":"9","author":"Vos","year":"2021","journal-title":"Lancet Respir. Med."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"599","DOI":"10.1007\/s11046-020-00462-9","article-title":"Fungal Co-infections Associated with Global COVID-19 Pandemic: A Clinical and Diagnostic Perspective from China","volume":"185","author":"Song","year":"2020","journal-title":"Mycopathologia"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Toc, D.A., Costache, C., Botan, A., Mihaila, R.M., Colosi, I.A., Buksa, S.B., and Chiorescu, R.M. (2021). Mixed Etiology COVID-19 Associated Pulmonary Aspergillosis (CAPA)-A Case Report and Brief Review of the Literature. J. Fungi, 7.","DOI":"10.3390\/jof7100877"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"e149","DOI":"10.1016\/S1473-3099(20)30847-1","article-title":"Defining and managing COVID-19-associated pulmonary aspergillosis: The 2020 ECMM\/ISHAM consensus criteria for research and clinical guidance","volume":"21","author":"Koehler","year":"2021","journal-title":"Lancet Infect. Dis."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1007\/s11908-022-00788-z","article-title":"Les mis\u00e9rables: A Parallel between Antimicrobial Resistance and COVID-19 in Underdeveloped and Developing Countries","volume":"24","author":"Gontijo","year":"2022","journal-title":"Curr. Infect. Dis. Rep."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"106324","DOI":"10.1016\/j.ijantimicag.2021.106324","article-title":"Increased antimicrobial resistance during the COVID-19 pandemic","volume":"57","author":"Lai","year":"2021","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/j.jiph.2020.10.018","article-title":"The interrelationships between antimicrobial resistance, COVID-19, past, and future pandemics","volume":"14","author":"Ukuhor","year":"2021","journal-title":"J. Infect. Public Health"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1079","DOI":"10.1086\/533452","article-title":"Federal funding for the study of antimicrobial resistance in nosocomial pathogens: No ESKAPE","volume":"197","author":"Rice","year":"2008","journal-title":"J. Infect. Dis."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1097\/MCC.0000000000000755","article-title":"Antimicrobial resistance in ICUs: An update in the light of the COVID-19 pandemic","volume":"26","year":"2020","journal-title":"Curr. Opin. Crit. Care"},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Vrancianu, C.O., Gheorghe, I., Dobre, E.G., Barbu, I.C., Cristian, R.E., Popa, M., Lee, S.H., Limban, C., Vlad, I.M., and Chifiriuc, M.C. (2020). Emerging Strategies to Combat \u03b2-Lactamase Producing ESKAPE Pathogens. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21228527"},{"key":"ref_20","first-page":"220","article-title":"Enterococcus and COVID-19: The Emergence of a Perfect Storm?","volume":"2","author":"Toc","year":"2022","journal-title":"Int. J. Transl. Med."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"e1453","DOI":"10.1016\/S2214-109X(20)30444-7","article-title":"COVID-19 pneumonia and the appropriate use of antibiotics","volume":"8","author":"Ginsburg","year":"2020","journal-title":"Lancet Glob. Health"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"63","DOI":"10.37201\/req\/s01.19.2021","article-title":"COVID-19: Impact on prescribing and antimicrobial resistance","volume":"34","year":"2021","journal-title":"Rev. Esp. Quimioter. Publ. Soc. Esp. Quimioter."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"3386","DOI":"10.1093\/jac\/dkaa326","article-title":"Antibiotic use in patients with COVID-19: A \u2018snapshot\u2019 Infectious Diseases International Research Initiative (ID-IRI) survey","volume":"75","author":"Nadrah","year":"2020","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1397","DOI":"10.1016\/j.jiph.2020.07.003","article-title":"Molecular pathogenesis of secondary bacterial infection associated to viral infections including SARS-CoV-2","volume":"13","author":"Manna","year":"2020","journal-title":"J. Infect. Public Health"},{"key":"ref_25","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_26","first-page":"51","article-title":"Blood stream infections during the first wave of COVID-19. A short microbiological retrospective picture at Papa Giovanni XXIII Hospital, Bergamo, Italy","volume":"44","author":"Manisco","year":"2021","journal-title":"New Microbiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"e13319","DOI":"10.1111\/eci.13319","article-title":"Bloodstream infections in critically ill patients with COVID-19","volume":"50","author":"Giacobbe","year":"2020","journal-title":"Eur. J. Clin. Investig."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1395","DOI":"10.1016\/j.cmi.2020.06.025","article-title":"Bacterial and fungal coinfection among hospitalized patients with COVID-19: A retrospective cohort study in a UK secondary-care setting","volume":"26","author":"Hughes","year":"2020","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"315","DOI":"10.2146\/ajhp150029","article-title":"Comparison of telavancin and vancomycin lock solutions in eradication of biofilm-producing staphylococci and enterococci from central venous catheters","volume":"73","author":"Luther","year":"2016","journal-title":"Am. J. Health-Syst. Pharm."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Toc, D.A., Csapai, A., Popa, F., Popa, C., Pascalau, V., Tosa, N., Botan, A., Mihaila, R.M., Costache, C.A., and Colosi, I.A. (2022). Easy and Affordable: A New Method for the Studying of Bacterial Biofilm Formation. Cells, 11.","DOI":"10.3390\/cells11244119"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"5046","DOI":"10.1128\/AAC.49.12.5046-5050.2005","article-title":"Vancomycin-resistant Enterococcus faecium: Catheter colonization, esp gene, and decreased susceptibility to antibiotics in biofilm","volume":"49","author":"Raad","year":"2005","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"547","DOI":"10.1099\/jmm.0.05201-0","article-title":"Correlation between enterococcal biofilm formation in vitro and medical-device-related infection potential in vivo","volume":"52","author":"Witherden","year":"2003","journal-title":"J. Med. Microbiol."},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Csapai, A., Toc, D.A., Popa, F., Tosa, N., Pascalau, V., Costache, C., Botan, A., and Popa, C.O. (2022). 3D Printed Microfluidic Bioreactors Used for the Preferential Growth of Bacterial Biofilms through Dielectrophoresis. Micromachines, 13.","DOI":"10.3390\/mi13091377"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1186\/s13756-020-00820-8","article-title":"A nosocomial cluster of vancomycin resistant enterococci among COVID-19 patients in an intensive care unit","volume":"9","author":"Kampmeier","year":"2020","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1779","DOI":"10.1080\/07853890.2021.1988695","article-title":"Enterococcal bloodstream infections in critically ill patients with COVID-19: A case series","volume":"53","author":"Giacobbe","year":"2021","journal-title":"Ann. Med."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"454","DOI":"10.1016\/j.chest.2021.04.002","article-title":"Hospital-Acquired Infections in Critically Ill Patients with COVID-19","volume":"160","author":"Grasselli","year":"2021","journal-title":"Chest"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1186\/s13054-022-04166-y","article-title":"Different epidemiology of bloodstream infections in COVID-19 compared to non-COVID-19 critically ill patients: A descriptive analysis of the Eurobact II study","volume":"26","author":"Buetti","year":"2022","journal-title":"Crit. Care"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"e31","DOI":"10.1097\/CCM.0000000000004748","article-title":"Unexpectedly High Frequency of Enterococcal Bloodstream Infections in Coronavirus Disease 2019 Patients Admitted to an Italian ICU: An Observational Study","volume":"49","author":"Bonazzetti","year":"2021","journal-title":"Crit. Care Med."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1416","DOI":"10.1017\/ice.2021.391","article-title":"Increased rates of secondary bacterial infections, including Enterococcus bacteremia, in patients hospitalized with coronavirus disease 2019 (COVID-19)","volume":"43","author":"DeVoe","year":"2022","journal-title":"Infect. Control Hosp. Epidemiol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1007\/s00134-021-06346-w","article-title":"COVID-19 increased the risk of ICU-acquired bloodstream infections: A case-cohort study from the multicentric OUTCOMEREA network","volume":"47","author":"Buetti","year":"2021","journal-title":"Intensive Care Med."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1017\/ice.2021.362","article-title":"The impact of coronavirus disease 2019 (COVID-19) on healthcare-associated infections in 2020: A summary of data reported to the National Healthcare Safety Network","volume":"43","author":"Pattabiraman","year":"2022","journal-title":"Infect. Control Hosp. Epidemiol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"e1082","DOI":"10.1093\/cid\/ciab869","article-title":"Changing Patterns of Bloodstream Infections in the Community and Acute Care Across 2 Coronavirus Disease 2019 Epidemic Waves: A Retrospective Analysis Using Data Linkage","volume":"75","author":"Zhu","year":"2022","journal-title":"Clin. Infect. Dis."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1357","DOI":"10.4315\/0362-028X.JFP-18-046","article-title":"Characteristics of High-Level Ciprofloxacin-Resistant Enterococcus faecalis and Enterococcus faecium from Retail Chicken Meat in Korea","volume":"81","author":"Kim","year":"2018","journal-title":"J. Food Prot."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Toc, D.A., Pandrea, S.L., Botan, A., Mihaila, R.M., Costache, C.A., Colosi, I.A., and Junie, L.M. (2022). Enterococcus raffinosus, Enterococcus durans and Enterococcus avium Isolated from a Tertiary Care Hospital in Romania-Retrospective Study and Brief Review. Biology, 11.","DOI":"10.3390\/biology11040598"},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Zhao, B., Ye, M.S., and Zheng, R. (2018). Enterococcus gallinarum meningitis: A case report and literature review. BMC Infect. Dis., 18.","DOI":"10.1186\/s12879-018-3151-4"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"e9875","DOI":"10.1097\/MD.0000000000009875","article-title":"The first case report of Enterococcus gallinarum meningitis in neonate: A literature review","volume":"97","author":"Li","year":"2018","journal-title":"Medicine"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"100837","DOI":"10.1016\/j.nmni.2021.100837","article-title":"Oral probiotics in coronavirus disease 2019: Connecting the gut-lung axis to viral pathogenesis, inflammation, secondary infection and clinical trials","volume":"40","author":"Baindara","year":"2021","journal-title":"New Microbes New Infect."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Fiore, E., Van Tyne, D., and Gilmore, M.S. (2019). Pathogenicity of Enterococci. Microbiol. Spectr., 74.","DOI":"10.1128\/9781683670131.ch24"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"7273","DOI":"10.1073\/pnas.1500553112","article-title":"Pheromone killing of multidrug-resistant Enterococcus faecalis V583 by native commensal strains","volume":"112","author":"Gilmore","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"}],"container-title":["Antibiotics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-6382\/12\/2\/312\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:22:53Z","timestamp":1760120573000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-6382\/12\/2\/312"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,2,2]]},"references-count":49,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2023,2]]}},"alternative-id":["antibiotics12020312"],"URL":"https:\/\/doi.org\/10.3390\/antibiotics12020312","relation":{},"ISSN":["2079-6382"],"issn-type":[{"value":"2079-6382","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,2,2]]}}}