{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T03:05:16Z","timestamp":1760151916475,"version":"build-2065373602"},"reference-count":44,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2022,11,30]],"date-time":"2022-11-30T00:00:00Z","timestamp":1669766400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>With almost 638 million cases and over 6 million deaths worldwide, the SARS-CoV-2 pandemic represents an unprecedented healthcare challenge. Although the management and natural history of COVID-19 patients have changed after the introduction of active therapies and vaccination, the development of secondary infections complicates hospital stay. This is a single-center, retrospective, observational study that explores the incidence and microbiology of hospital-acquired infections (HAIs) in two subsequent populations of hospitalized patients with COVID-19. Demographic, pre-hospitalization baseline characteristics, therapeutic options and microbiology data about secondary infections were collected for a total of 1153 cases. The second population appeared to have a higher median age (73 vs. 63 years, respectively), comorbidities (median Charlson Comorbidity Index Score was 4 vs. 1, respectively) and incidence of secondary infections (23.5% vs. 8.2%) with respect to the first. A higher incidence of multi-drug resistant organisms (MDROs), including difficult-to-treat resistant (DTR) Pseudomonas, methicillin-resistant Staphylococcus aureus (MRSA) and vancomycin-resistant Enterococcus (VRE), was also observed. Both patients\u2019 characteristics and poor adherence to standard hygiene and infection control protocols may have contributed to the higher incidence of these events and may have impacted on the natural history of the disease. In-hospital mortality rates were similar, despite the introduction of active therapies against COVID-19 (24.7% vs. 23.5%, respectively). The incidence of HAIs may have contributed to the unchanged mortality and prompts for more effective antimicrobial stewardship and infection control procedures in COVID-19.<\/jats:p>","DOI":"10.3390\/microorganisms10122372","type":"journal-article","created":{"date-parts":[[2022,11,30]],"date-time":"2022-11-30T05:45:22Z","timestamp":1669787122000},"page":"2372","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Incidence and Microbiology of Hospital-Acquired Infections in COVID-19 Patients between the First and the Second Outbreak of the SARS-CoV-2 Pandemic: A Retrospective, Observational Study"],"prefix":"10.3390","volume":"10","author":[{"given":"Corti","family":"Nicol\u00f2","sequence":"first","affiliation":[{"name":"Infectious Disease Unit, San Gerardo Hospital, 20900 Monza, Italy"},{"name":"Residency School in Infectious and Tropical Diseases, University of Milano-Bicocca, 20900 Monza, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6739-6826","authenticated-orcid":false,"given":"Tordato","family":"Federica","sequence":"additional","affiliation":[{"name":"Department of Biomedical Sciences, Humanitas University, Pieve Emanuele, 20072 Milan, Italy"},{"name":"Infectious Disease Unit, IRCCS Humanitas Research Hospital, Rozzano, 20089 Milan, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Guendalina","family":"De Nadai","sequence":"additional","affiliation":[{"name":"Emergency Department, IRCCS Humanitas Research Hospital, Italy IRCCS Humanitas Research Hospital, Rozzano, 20089 Milan, Italy"},{"name":"Residency School in Emergency Medicine, Humanitas University, Pieve Emanuele, 20072 Milan, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0129-2055","authenticated-orcid":false,"given":"Mapelli","family":"Sarah","sequence":"additional","affiliation":[{"name":"IRCCS Humanitas Research Hospital, Rozzano, 20089 Milan, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1510-7703","authenticated-orcid":false,"given":"Garlanda","family":"Cecilia","sequence":"additional","affiliation":[{"name":"Department of Biomedical Sciences, Humanitas University, Pieve Emanuele, 20072 Milan, Italy"},{"name":"IRCCS Humanitas Research Hospital, Rozzano, 20089 Milan, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Pocaterra","family":"Daria","sequence":"additional","affiliation":[{"name":"Infectious Disease Unit, IRCCS Humanitas Research Hospital, Rozzano, 20089 Milan, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Casana","family":"Maddalena","sequence":"additional","affiliation":[{"name":"Infectious Disease Unit, IRCCS Humanitas Research Hospital, Rozzano, 20089 Milan, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7289-8823","authenticated-orcid":false,"given":"Bonfanti","family":"Paolo","sequence":"additional","affiliation":[{"name":"Infectious Disease Unit, San Gerardo Hospital, 20900 Monza, Italy"},{"name":"Department of Medicine and Surgery, University of Milano-Bicocca, 20090 Monza, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9555-5284","authenticated-orcid":false,"given":"Morelli","family":"Paola","sequence":"additional","affiliation":[{"name":"Department of Biomedical Sciences, Humanitas University, Pieve Emanuele, 20072 Milan, Italy"},{"name":"Infectious Disease Unit, IRCCS Humanitas Research Hospital, Rozzano, 20089 Milan, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,11,30]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1038\/s41579-020-00468-6","article-title":"Coronavirus biology and replication: Implications for SARS-CoV-2","volume":"19","author":"Kratzel","year":"2021","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"782","DOI":"10.1001\/jama.2020.12839","article-title":"Pathophysiology, Transmission, Diagnosis, and Treatment of Coronavirus Disease 2019 (COVID-19): A Review","volume":"324","author":"Wiersinga","year":"2020","journal-title":"JAMA-J. Am. Med. Assoc."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1159","DOI":"10.1080\/1744666X.2021.1847640","article-title":"Natural history of COVID-19 and therapeutic options","volume":"16","author":"Gautret","year":"2020","journal-title":"Expert Rev. Clin. Immunol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"e438","DOI":"10.1016\/S2352-3026(20)30145-9","article-title":"Coagulation abnormalities and thrombosis in patients with COVID-19","volume":"7","author":"Levi","year":"2020","journal-title":"Lancet Haematol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1016\/j.thromres.2020.04.013","article-title":"Incidence of thrombotic complications in critically ill ICU patients with COVID-19","volume":"191","author":"Klok","year":"2020","journal-title":"Thromb. Res."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1345","DOI":"10.1001\/jamainternmed.2020.3539","article-title":"Risk Factors Associated With Mortality Among Patients With COVID-19 in Intensive Care Units in Lombardy, Italy","volume":"180","author":"Grasselli","year":"2020","journal-title":"JAMA Intern. Med."},{"key":"ref_7","first-page":"1","article-title":"Predictors of COVID-19 severity: A literature review","volume":"31","author":"Aghagoli","year":"2021","journal-title":"Rev. Med. Virol."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Ngandu, N.K., Mmotsa, T.M., Dassaye, R., Thabetha, A., Odendaal, W., Langdown, N., and Ndwandwe, D. (2022). Hospital acquired COVID-19 infections amongst patients before the rollout of COVID-19 vaccinations, a scoping review. BMC Infect. Dis., 22.","DOI":"10.1186\/s12879-022-07128-5"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1078","DOI":"10.1093\/jac\/dkaa530","article-title":"Predictors of hospital-acquired bacterial and fungal superinfections in COVID-19: A prospective observational study","volume":"76","author":"Falcone","year":"2020","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_10","first-page":"83","article-title":"Incidence of co-infections and superinfections in hospitalized patients with COVID-19: A retrospective cohort study","volume":"27","author":"Sanjuan","year":"2021","journal-title":"Clin. Microbiol. Infect. Off. Publ. Eur. Soc. Clin. Microbiol. Infect. Dis."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"394","DOI":"10.1111\/irv.12398","article-title":"The frequency of influenza and bacterial coinfection: A systematic review and meta-analysis","volume":"10","author":"Klein","year":"2016","journal-title":"Influenza Other Respir. Viruses"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1017\/ice.2021.70","article-title":"Coronavirus disease 2019 (COVID-19) pandemic, central-line-associated bloodstream infection (CLABSI), and catheter-associated urinary tract infection (CAUTI): The urgent need to refocus on hardwiring prevention efforts","volume":"43","author":"Fakih","year":"2022","journal-title":"Infect. Control Hosp. Epidemiol."},{"key":"ref_13","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_14","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1016\/j.cmi.2020.10.021","article-title":"Secondary infections in patients hospitalized with COVID-19: Incidence and predictive factors","volume":"27","author":"Ripa","year":"2021","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_15","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_16","doi-asserted-by":"crossref","unstructured":"Ceparano, M., Baccolini, V., Migliara, G., Isonne, C., Renzi, E., Tufi, D., De Vito, C., De Giusti, M., Trancassini, M., and Alessandri, F. (2022). Acinetobacter baumannii Isolates from COVID-19 Patients in a Hospital Intensive Care Unit: Molecular Typing and Risk Factors. Microorganisms, 10.","DOI":"10.3390\/microorganisms10040722"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"M\u00f6llers, M., von Wahlde, M.K., Schuler, F., Mellmann, A., B\u00f6ing, C., Schwierzeck, V., Schneider, J.S., and Kampmeier, S. (2022). Outbreak of MRSA in a Gynecology\/Obstetrics Department during the COVID-19 Pandemic: A Cautionary Tale. Microorganisms, 10.","DOI":"10.3390\/microorganisms10040689"},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Bazaid, A.S., Barnawi, H., Qanash, H., Alsaif, G., Aldarhami, A., Gattan, H., Alharbi, B., Alrashidi, A., Al-Soud, W.A., and Moussa, S. (2022). Bacterial Coinfection and Antibiotic Resistance Profiles among Hospitalised COVID-19 Patients. Microorganisms, 10.","DOI":"10.3390\/microorganisms10030495"},{"key":"ref_19","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_20","doi-asserted-by":"crossref","first-page":"1827","DOI":"10.15585\/mmwr.mm6948e1","article-title":"Increase in Hospital-Acquired Carbapenem-Resistant Acinetobacter baumannii Infection and Colonization in an Acute Care Hospital During a Surge in COVID-19 Admissions\u2014New Jersey, February\u2013July 2020","volume":"69","author":"Perez","year":"2020","journal-title":"MMWR Morb. Mortal. Wkly. Rep."},{"key":"ref_21","first-page":"1622","article-title":"Bacterial co-infection and secondary infection in patients with COVID-19: A living rapid review and meta-analysis","volume":"26","author":"Langford","year":"2020","journal-title":"Clin. Microbiol. Infect. Off. Publ. Eur. Soc. Clin. Microbiol. Infect. Dis."},{"key":"ref_22","unstructured":"ECDC, and WHO (2022). Antimicrobial Resistance Surveillance in Europe (2016\u20132020), WHO."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1186\/s13756-018-0370-9","article-title":"Risk factors for hospitalized patients with resistant or multidrug-resistant Pseudomonas aeruginosa infections: A systematic review and meta-analysis","volume":"7","author":"Raman","year":"2018","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1256","DOI":"10.1016\/j.ajic.2021.06.005","article-title":"Risk factors for isolation of multi-drug resistant organisms in coronavirus disease 2019 pneumonia: A multicenter study","volume":"49","author":"Son","year":"2021","journal-title":"Am. J. Infect. Control"},{"key":"ref_25","first-page":"228","article-title":"Risk factors for carbapenem-resistant Gram-negative bacterial infections: A systematic review","volume":"27","author":"Giannella","year":"2021","journal-title":"Clin. Microbiol. Infect. Off. Publ. Eur. Soc. Clin. Microbiol. Infect. Dis."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"693","DOI":"10.1056\/NEJMoa2021436","article-title":"RECOVERY Collaborative Group. Dexamethasone in Hospitalized Patients with Covid-19","volume":"384","author":"Horby","year":"2021","journal-title":"N. Engl. J. Med."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1813","DOI":"10.1056\/NEJMoa2007764","article-title":"Remdesivir for the Treatment of Covid-19\u2014Final Report","volume":"383","author":"Beigel","year":"2020","journal-title":"N. Engl. J. Med."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1111\/j.1469-0691.2011.03570.x","article-title":"Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance","volume":"18","author":"Magiorakos","year":"2012","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"801","DOI":"10.1001\/jama.2016.0287","article-title":"The Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3)","volume":"315","author":"Singer","year":"2016","journal-title":"JAMA"},{"key":"ref_30","unstructured":"WHO (2020). Clinical Management of Severe Acute Respiratory Infection (SARI) When COVID-19 Disease Is Suspected, WHO."},{"key":"ref_31","unstructured":"SIMIT (2020). Vademecum per La Cura Delle Persone Con Malattia Da COVID-19, SMIT. Ver. 2.0 13.03.2020."},{"key":"ref_32","unstructured":"WHO (2021, January 01). Home Care for Patients with Suspected or Confirmed COVID-19 and Management of Their Contacts. World Health Organization, Available online: https:\/\/www.who.int\/publications-detail\/home-care-for-patients-with-suspected-novel-coronavirus-(ncov)-infection-presenting-with-mild-symptoms-and-management-of-contacts."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"e62","DOI":"10.1016\/S2666-5247(20)30036-7","article-title":"Low rate of bacterial co-infection in patients with COVID-19","volume":"1","author":"Adler","year":"2020","journal-title":"The Lancet Microbe."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Yu, D., Ininbergs, K., Hedman, K., Giske, C.G., Str\u00e5lin, K., and \u00d6zenci, V. (2020). Low prevalence of bloodstream infection and high blood culture contamination rates in patients with COVID-19. PLoS ONE, 15.","DOI":"10.1371\/journal.pone.0242533"},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Musuuza, J., Watson, L., Parmasad, V., Putman-Buehler, N., Christensen, L., and Safdar, N. (2020). Prevalence and outcomes of co-infection and super-infection with SARS-CoV-2 and other pathogens: A Systematic Review and Meta-analysis. medRxiv, 1\u201323.","DOI":"10.1101\/2020.10.27.20220566"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Sharifipour, E., Shams, S., Esmkhani, M., Khodadadi, J., Fatouhi-Ardakani, R., Koohpaei, A., Doosti, Z., and Golzari, S.E. (2020). Evaluation of bacterial co-infections of the respiratory tract in COVID-19 patients admitted to ICU. BMC Infect. Dis., 20.","DOI":"10.1186\/s12879-020-05374-z"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1007\/s00059-020-04923-1","article-title":"Ventilation of COVID-19 patients in intensive care units","volume":"45","author":"Thiele","year":"2020","journal-title":"Herz"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"307","DOI":"10.7883\/yoken.JJID.2020.884","article-title":"Increased Secondary Infection in COVID-19 Patients Treated with Steroids in New York City","volume":"74","author":"Reiichiro","year":"2021","journal-title":"Jpn. J. Infect. Dis."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1097\/IPC.0000000000001188","article-title":"Longer Steroid Treatment Increases Secondary Bloodstream Infection Risk Among Patients With COVID-19 Requiring Intensive Care","volume":"30","author":"Dupper","year":"2022","journal-title":"Infect. Dis. Clin. Pract."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"104806","DOI":"10.1016\/j.micinf.2021.104806","article-title":"Bacterial and fungal co-infections among COVID-19 patients in Intensive Care Unit","volume":"23","author":"Yang","year":"2021","journal-title":"Microbes Infect."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"e00163-21","DOI":"10.1128\/Spectrum.00163-21","article-title":"Coinfections with Other Respiratory Pathogens among Patients with COVID-19","volume":"9","author":"Sreenath","year":"2021","journal-title":"Microbiol. Spectr."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"12703","DOI":"10.1038\/s41598-021-92220-0","article-title":"Secondary bacterial infection in COVID-19 patients is a stronger predictor for death compared to influenza patients","volume":"11","author":"Shafran","year":"2021","journal-title":"Sci. Rep."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"715023","DOI":"10.3389\/fimmu.2021.715023","article-title":"Identifying Risk Factors for Secondary Infection Post-SARS-CoV-2 Infection in Patients With Severe and Critical COVID-19","volume":"12","author":"Guo","year":"2021","journal-title":"Front. Immunol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1958","DOI":"10.1080\/22221751.2020.1812437","article-title":"Risks and features of secondary infections in severe and critical ill COVID-19 patients","volume":"9","author":"Zhang","year":"2020","journal-title":"Emerg. Microbes Infect."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/10\/12\/2372\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:30:21Z","timestamp":1760146221000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/10\/12\/2372"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,11,30]]},"references-count":44,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2022,12]]}},"alternative-id":["microorganisms10122372"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms10122372","relation":{},"ISSN":["2076-2607"],"issn-type":[{"type":"electronic","value":"2076-2607"}],"subject":[],"published":{"date-parts":[[2022,11,30]]}}}