{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,18]],"date-time":"2026-09-18T21:51:10Z","timestamp":1789768270829,"version":"4.0.1"},"reference-count":82,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2023,11,7]],"date-time":"2023-11-07T00:00:00Z","timestamp":1699315200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Qatar University"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Antibiotics"],"abstract":"<jats:p>This study investigated how the Coronavirus Disease 2019 (COVID-19) pandemic has affected the rate of healthcare-associated infections (HAIs). PubMed, Scopus and Google Scholar were searched to identify potentially eligible studies published from December 2019 to September 2022. A random effect model was used to determine the changes in the rate of HAIs during the pandemic. Thirty-seven studies, mostly from the United States (n = 13), were included. Fifteen studies described how the pandemic affected the rate of CLABSIs and CAUTIs, and eight of them showed a significant increase in CLABSIs. The risk of CLABSIs and CDIs was 27% (pooled odds ratio [OR]: 0.73; confidence interval [CI]: 0.61\u20130.89; p &lt; 0.001) and 20% (pooled OR: 1.20; CI: 1.10\u20131.31; p &lt; 0.001) higher during the pandemic compared to before the COVID-19 pandemic period, respectively. However, the overall risk of HAIs was unaffected by the pandemic (pooled OR: 1.00; 95 CI: 0.80\u20131.24; p = 0.990). Furthermore, there were no significant changes in the risk of CAUTIs (pooled OR: 1.01; 95 CI: 0.88\u20131.16; p = 0.890), and SSIs (pooled OR: 1.27; CI: 0.91\u20131.76; p = 0.16) between the two periods. The COVID-19 pandemic had no effect on the overall risk of HAIs among hospitalized patients, but an increased risk of CLABSIs and CDI were observed during the pandemic. Therefore, more stringent infection control and prevention measures and prudent interventions to promote the rational use of antibiotics are warranted across all healthcare facilities to reduce the burden of HAIs.<\/jats:p>","DOI":"10.3390\/antibiotics12111600","type":"journal-article","created":{"date-parts":[[2023,11,7]],"date-time":"2023-11-07T11:23:39Z","timestamp":1699356219000},"page":"1600","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":23,"title":["Impact of COVID-19 Pandemic on Healthcare-Associated Infections: A Systematic Review and Meta-Analysis"],"prefix":"10.3390","volume":"12","author":[{"given":"Usman","family":"Abubakar","sequence":"first","affiliation":[{"name":"Department of Clinical Pharmacy and Practice, College of Pharmacy, QU Health, Qatar University, Doha P.O. Box 2713, Qatar"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9029-8925","authenticated-orcid":false,"given":"Ahmed","family":"Awaisu","sequence":"additional","affiliation":[{"name":"Department of Clinical Pharmacy and Practice, College of Pharmacy, QU Health, Qatar University, Doha P.O. Box 2713, Qatar"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4802-6181","authenticated-orcid":false,"given":"Amer Hayat","family":"Khan","sequence":"additional","affiliation":[{"name":"Discipline of Clinical Pharmacy, School of Pharmaceutical Sciences, Universiti Sains Malaysia, George Town 11800, Malaysia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Khurshid","family":"Alam","sequence":"additional","affiliation":[{"name":"Discipline of Clinical Pharmacy, School of Pharmaceutical Sciences, Universiti Sains Malaysia, George Town 11800, Malaysia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,11,7]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1186\/s13756-016-0149-9","article-title":"Core components for effective infection prevention and control programmes: New WHO evidence-based recommendations","volume":"6","author":"Storr","year":"2017","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1198","DOI":"10.1056\/NEJMoa1306801","article-title":"Multistate point-prevalence survey of health care\u2013associated infections","volume":"370","author":"Magill","year":"2014","journal-title":"N. Engl. J. Med."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1800516","DOI":"10.2807\/1560-7917.ES.2018.23.46.1800516","article-title":"Prevalence of healthcare-associated infections, estimated incidence and composite antimicrobial resistance index in acute care hospitals and long-term care facilities: Results from two European point prevalence surveys, 2016 to 2017","volume":"23","author":"Suetens","year":"2018","journal-title":"Eurosurveillance"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1690","DOI":"10.1093\/cid\/civ095","article-title":"The burden of healthcare-associated infections in Southeast Asia: A systematic literature review and meta-analysis","volume":"60","author":"Ling","year":"2015","journal-title":"Clin. Infect. Dis."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"228","DOI":"10.1016\/S0140-6736(10)61458-4","article-title":"Burden of endemic health-care-associated infection in developing countries: Systematic review and meta-analysis","volume":"377","author":"Allegranzi","year":"2011","journal-title":"Lancet"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1186\/s40545-022-00500-5","article-title":"Healthcare-associated infections in Africa: A systematic review and meta-analysis of point prevalence studies","volume":"15","author":"Abubakar","year":"2022","journal-title":"J. Pharm. Policy Pract."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s13756-020-00722-9","article-title":"Point-prevalence survey of hospital acquired infections in three acute care hospitals in Northern Nigeria","volume":"9","author":"Abubakar","year":"2020","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1016\/j.ijid.2019.06.002","article-title":"Hand hygiene in low-and middle-income countries","volume":"86","author":"Loftus","year":"2019","journal-title":"Int. J. 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":"565","DOI":"10.1016\/j.ajic.2018.09.014","article-title":"Barriers to hand hygiene practices among health care workers in sub-Saharan African countries: A narrative review","volume":"47","author":"Ataiyero","year":"2019","journal-title":"Am. J. Infect. Control"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1016\/j.ajic.2021.11.030","article-title":"Compared hand hygiene compliance among healthcare providers before and after the COVID-19 pandemic: A rapid review and meta-analysis","volume":"50","author":"Wang","year":"2022","journal-title":"Am. J. Infect. Control"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"946","DOI":"10.1017\/ice.2020.141","article-title":"Impact of COVID-19 on traditional healthcare-associated infection prevention efforts","volume":"41","author":"Stevens","year":"2020","journal-title":"Infect. Control Hosp. Epidemiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1016\/j.jgar.2021.02.013","article-title":"Antimicrobial resistance research in a post-pandemic world: Insights on antimicrobial resistance research in the COVID-19 pandemic","volume":"25","author":"Rossolini","year":"2021","journal-title":"J. Glob. Antimicrob. Resist."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1007\/s13337-021-00695-2","article-title":"The potential impact of the COVID-19 pandemic on antimicrobial resistance and antibiotic stewardship","volume":"32","author":"Subramanya","year":"2021","journal-title":"Virus Dis."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"436","DOI":"10.1016\/j.pedn.2021.09.004","article-title":"The impact of visiting restrictions during the COVID-19 pandemic on pediatric patients","volume":"61","author":"McBride","year":"2021","journal-title":"J. Pediatr. Nurs."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1398","DOI":"10.3855\/jidc.14066","article-title":"Practices and perception of healthcare workers towards infection control measures during the COVID-19 pandemic: A cross-sectional online survey from Nigeria","volume":"16","author":"Abubakar","year":"2022","journal-title":"J. Infect. Dev. Ctries."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"n160","DOI":"10.1136\/bmj.n160","article-title":"PRISMA 2020 explanation and elaboration: Updated guidance and exemplars for reporting systematic reviews","volume":"372","author":"Page","year":"2021","journal-title":"BMJ"},{"key":"ref_18","unstructured":"Wells, G.A., Shea, B., O\u2019Connell, D., Peterson, J., Welch, V., Losos, M., and Tugwell, P. (2023, September 03). The Newcastle-Ottawa Scale (NOS) for Assessing the Quality of Nonrandomised Studies in Meta-Analyses. Available online: https:\/\/www.ohri.ca\/programs\/clinical_epidemiology\/oxford.asp."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1016\/0196-6553(88)90053-3","article-title":"CDC definitions for nosocomial infections, 1988","volume":"16","author":"Garner","year":"1988","journal-title":"Am. J. Infect. Control"},{"key":"ref_20","unstructured":"European Center for Disease Prevention and Control (2016). Point Prevalence Survey of Healthcare Associated Infections and Antimicrobial Use in European Acute Care Hospitals\u2014Protocol Version 5.3."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"557","DOI":"10.1136\/bmj.327.7414.557","article-title":"Measuring inconsistency in meta-analyses","volume":"327","author":"Higgins","year":"2003","journal-title":"BMJ"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1186\/s13756-021-00959-y","article-title":"The impact of the COVID-19 pandemic on healthcare-associated infections in intensive care unit patients: A retrospective cohort study","volume":"10","author":"Baccolini","year":"2021","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Jabarpour, M., Dehghan, M., Afsharipour, G., Hajipour Abaee, E., Mangolian Shahrbabaki, P., Ahmadinejad, M., and Maazallahi, M. (2021). The impact of COVID-19 outbreak on nosocomial infection rate: A case of Iran. Can. J. Infect. Dis. Med. Microbiol., 2021.","DOI":"10.1155\/2021\/6650920"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"00469580211067930","DOI":"10.1177\/00469580211067930","article-title":"Trends of Healthcare-associated Infections in a Tuinisian University Hospital and Impact of COVID-19 Pandemic","volume":"58","author":"Ghali","year":"2021","journal-title":"INQUIRY J. Health Care Organ. Provis. Financ."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Chen, C., Zhu, P., Zhang, Y., and Liu, B. (2021). Effect of the \u201cNormalized Epidemic Prevention and Control Requirements\u201d on hospital-acquired and community-acquired infections in China. BMC Infect. Dis., 21.","DOI":"10.1186\/s12879-021-06886-y"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"117111","DOI":"10.1016\/j.jns.2020.117111","article-title":"The potential impact of enhanced hygienic measures during the COVID-19 outbreak on hospital-acquired infections: A pragmatic study in neurological units","volume":"418","author":"Irelli","year":"2020","journal-title":"J. Neurol. Sci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1249","DOI":"10.1007\/s00268-022-06539-4","article-title":"Hospital Acquired Infections in Surgical Patients: Impact of COVID-19-Related Infection Prevention Measures","volume":"46","author":"Tham","year":"2022","journal-title":"World J. Surg."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1016\/j.ajic.2021.11.015","article-title":"Impact of COVID-19 on an infection prevention and control program, Iowa 2020\u20132021","volume":"50","author":"Alsuhaibani","year":"2022","journal-title":"Am. J. Infect. Control"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1016\/j.jhin.2021.09.020","article-title":"Increase in the frequency of catheter-related bloodstream infections during the COVID-19 pandemic: A plea for Control","volume":"119","author":"Carrillo","year":"2022","journal-title":"J. Hosp. Infect."},{"key":"ref_30","doi-asserted-by":"crossref","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":"ref_31","doi-asserted-by":"crossref","first-page":"831","DOI":"10.1016\/j.ajic.2022.02.030","article-title":"Impact of COVID-19 on hospital acquired infections","volume":"50","author":"Halverson","year":"2022","journal-title":"Am. J. Infect. Control"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"e34","DOI":"10.1093\/cid\/ciac684","article-title":"The Disproportionate Impact of COVID-19 Pandemic on Healthcare-Associated Infections in Community Hospitals: Need for Expanding the Infectious Disease Workforce","volume":"76","author":"Advani","year":"2022","journal-title":"Clin. Infect. Dis."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1017\/ice.2021.70","article-title":"Coronavirus disease 2019 (COVID-19) pandemic, central-line\u2013associated 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_34","doi-asserted-by":"crossref","first-page":"e11","DOI":"10.1017\/ash.2021.237","article-title":"Evaluation of healthcare-associated infection rates in patients with hematologic malignancies and stem cell transplantation during the coronavirus disease 2019 (COVID-19) pandemic","volume":"2","author":"Bobbitt","year":"2022","journal-title":"Antimicrob. Steward. Healthc. Epidemiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1186\/s13756-022-01108-9","article-title":"No increase of device associated infections in German intensive care units during the start of the COVID-19 pandemic in 2020","volume":"11","author":"Geffers","year":"2022","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"11","DOI":"10.36518\/2689-0216.1296","article-title":"Hand Hygiene and Hospital-Acquired Infections During COVID-19 Increased Vigilance: One Hospital\u2019s Experience","volume":"2","author":"Kong","year":"2021","journal-title":"HCA Healthc. J. Med."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"284","DOI":"10.1017\/ice.2022.65","article-title":"Healthcare-associated infections on the intensive care unit in 21 Brazilian hospitals during the early months of the coronavirus disease 2019 (COVID-19) pandemic: An ecological study","volume":"44","author":"Porto","year":"2022","journal-title":"Infect. Control Hosp. Epidemiol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"790","DOI":"10.1017\/ice.2021.108","article-title":"Impact of COVID-19 pandemic on central-line\u2013associated bloodstream infections during the early months of 2020, National Healthcare Safety Network","volume":"43","author":"Patel","year":"2022","journal-title":"Infect. Control Hosp. Epidemiol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/j.ijid.2022.02.041","article-title":"The impact of COVID-19 on health care\u2013associated infections in intensive care units in low-and middle-income countries: International Nosocomial Infection Control Consortium (INICC) findings","volume":"118","author":"Rosenthal","year":"2022","journal-title":"Int. J. Infect. Dis."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"997","DOI":"10.1017\/ice.2022.116","article-title":"Continued Increases in HAI Incidence During the Second Year of the COVID-19 Pandemic","volume":"44","author":"Lastinger","year":"2023","journal-title":"Infect. Control Hosp. Epidemiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"e77","DOI":"10.1017\/ash.2022.223","article-title":"The initial and lingering impact of coronavirus disease 2019 (COVID-19) on catheter-associated infections in a large healthcare system in New York City","volume":"2","author":"Qiu","year":"2022","journal-title":"Antimicrob. Steward. Healthc. Epidemiol."},{"key":"ref_42","first-page":"e24254","article-title":"Impact of the COVID-19 Pandemic on Levels of Device-Associated Infections and Hand Hygiene Compliance","volume":"14","author":"AlAhdal","year":"2022","journal-title":"Cureus"},{"key":"ref_43","first-page":"210","article-title":"Surge in Ventilator-Associated Pneumonias and Bloodstream Infections in An Academic Referral Center Converted to Treat COVID-19 Patients","volume":"73","year":"2021","journal-title":"Rev. Investig. Cl\u00ednica"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1016\/j.ajic.2022.08.006","article-title":"Decreasing Catheter-Associated Urinary Tract Infection (CAUTI) at a community academic medical center using a multidisciplinary team employing a multi-pronged approach during the COVID-19 pandemic","volume":"51","author":"Whitaker","year":"2023","journal-title":"Am. J. Infect. Control"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"640","DOI":"10.1016\/j.ajic.2020.09.010","article-title":"Impact of COVID-19 prevention measures on risk of health care-associated Clostridium difficile infection","volume":"49","author":"Bentivegna","year":"2021","journal-title":"Am. J. Infect. Control"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1180","DOI":"10.1017\/ice.2022.210","article-title":"Trends in Clostridioides difficile infection rates in Canadian hospitals during the coronavirus disease 2019 (COVID-19) pandemic","volume":"44","author":"Choi","year":"2022","journal-title":"Infect. Control Hosp. Epidemiol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"966","DOI":"10.1016\/j.ajic.2020.12.008","article-title":"Substantial reduction of healthcare facility-onset Clostridioides difficile infection (HO-CDI) rates after conversion of a hospital for exclusive treatment of COVID-19 patients","volume":"49","year":"2021","journal-title":"Am. J. Infect. Control"},{"key":"ref_48","first-page":"409","article-title":"Healthcare-associated infection during the COVID-19 pandemic in a tertiary care hospital in Romania","volume":"59","author":"Manea","year":"2021","journal-title":"Rom. J. Intern. Med."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"406","DOI":"10.1017\/ice.2020.454","article-title":"Impact of the coronavirus disease 2019 (COVID-19) pandemic on nosocomial Clostridioides difficile infection","volume":"42","author":"Pintor","year":"2021","journal-title":"Infect. Control Hosp. Epidemiol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1215","DOI":"10.3892\/etm.2021.10649","article-title":"Impact of COVID-19 prevention measures on Clostridioides difficile infections in a regional acute care hospital","volume":"22","author":"Sipos","year":"2021","journal-title":"Exp. Ther. Med."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1016\/j.ajic.2021.12.018","article-title":"Impact of COVID-19 pandemic on hospital onset bloodstream infections (HOBSI) at a large health system","volume":"50","author":"Sturm","year":"2022","journal-title":"Am. J. Infect. Control"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1016\/j.ajic.2021.09.018","article-title":"Impact of the COVID-19 pandemic on the incidence of multidrug-resistant bacterial infections in an acute care hospital in Brazil","volume":"50","author":"Polly","year":"2022","journal-title":"Am. J. Infect. Control"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1140","DOI":"10.1016\/j.ajic.2022.04.016","article-title":"Dodging the bundle\u2014Persistent healthcare-associated rhinovirus infection throughout the pandemic","volume":"50","author":"Kitt","year":"2022","journal-title":"Am. J. Infect. Control"},{"key":"ref_54","first-page":"E267","article-title":"How the COVID-19 pandemic changed postoperative infections in urology wards: A retrospective cohort study from two urology departments","volume":"16","author":"Teixeira","year":"2022","journal-title":"Can. Urol. Assoc. J."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"220","DOI":"10.1007\/s10354-022-00918-1","article-title":"Hospital-acquired infections in a tertiary hospital in Iran before and during the COVID-19 pandemic","volume":"172","author":"Mohammadi","year":"2022","journal-title":"Wien. Med. Wochenschr."},{"key":"ref_56","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":"Updates Surg."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1016\/j.jhin.2021.07.006","article-title":"Healthcare-associated infection impact with bioaerosol treatment and COVID-19 mitigation measures","volume":"116","author":"Ereth","year":"2021","journal-title":"J. Hosp. Infect."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"100080","DOI":"10.1016\/j.infpip.2020.100080","article-title":"Hospital-acquired infective endocarditis during Covid-19 pandemic","volume":"2","author":"Forteza","year":"2020","journal-title":"Infect. Prev. Pract."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1186\/s43094-022-00406-8","article-title":"Mortality and its predictors among hospitalized patients with infections due to extended spectrum beta-lactamase (ESBL) Enterobacteriaceae in Malaysia: A retrospective observational study","volume":"8","author":"Abubakar","year":"2022","journal-title":"Future J. Pharm. Sci."},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Abubakar, U., Zulkarnain, A.I., Rodr\u00edguez-Ba\u00f1o, J., Kamarudin, N., Elrggal, M.E., Elnaem, M.H., and Harun, S.N. (2022). Treatments and Predictors of Mortality for Carbapenem-Resistant Gram-Negative Bacilli Infections in Malaysia: A Retrospective Cohort Study. Trop. Med. Infect. Dis., 7.","DOI":"10.3390\/tropicalmed7120415"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"10","DOI":"10.1016\/j.idh.2021.08.001","article-title":"Unexpected benefit of COVID-19 hospital restrictions: Reduction in patients isolating with multidrug resistant organisms after restrictions were lifted","volume":"27","author":"Elliott","year":"2022","journal-title":"Infect. Dis. Health"},{"key":"ref_62","doi-asserted-by":"crossref","unstructured":"Ippolito, M., Simone, B., Filisina, C., Catalanotto, F.R., Catalisano, G., Marino, C., Misseri, G., Giarratano, A., and Cortegiani, A. (2021). Bloodstream infections in hospitalized patients with COVID-19: A systematic review and meta-analysis. Microorganisms, 9.","DOI":"10.3390\/microorganisms9102016"},{"key":"ref_63","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_64","doi-asserted-by":"crossref","first-page":"753","DOI":"10.1007\/s13312-018-1374-5","article-title":"Decreasing central line-associated bloodstream infections through quality improvement initiative","volume":"55","author":"Balla","year":"2018","journal-title":"Indian Pediatr."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"010417","DOI":"10.7189\/jogh.07.010417","article-title":"Risk factors for Clostridium difficile infections\u2013an overview of the evidence base and challenges in data synthesis","volume":"7","author":"Eze","year":"2017","journal-title":"J. Glob. Health"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/j.jinf.2016.04.008","article-title":"Risk factors for Clostridium difficile infection in hospitalized patients with community-acquired pneumonia","volume":"73","author":"Chalmers","year":"2016","journal-title":"J. Infect."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"1693","DOI":"10.1056\/NEJMoa1012413","article-title":"Host and pathogen factors for Clostridium difficile infection and colonization","volume":"365","author":"Loo","year":"2011","journal-title":"N. Engl. J. Med."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"751","DOI":"10.1017\/ice.2020.1277","article-title":"Inpatient antibiotic utilization in the Veterans\u2019 Health Administration during the coronavirus disease 2019 (COVID-19) pandemic","volume":"42","author":"Dieringer","year":"2021","journal-title":"Infect. Control Hosp. Epidemiol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"e128","DOI":"10.1017\/ash.2022.268","article-title":"Trends in hospital antibiotic utilization during the coronavirus disease 2019 (COVID-19) pandemic: A multicenter interrupted time-series analysis","volume":"2","author":"Elligsen","year":"2022","journal-title":"Antimicrob. Steward. Healthc. Epidemiol."},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Castro-Lopes, A., Correia, S., Leal, C., Resende, I., Soares, P., Azevedo, A., and Paiva, J.A. (2021). Increase of antimicrobial consumption in a tertiary care hospital during the first phase of the COVID-19 pandemic. Antibiotics, 10.","DOI":"10.3390\/antibiotics10070778"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"1622","DOI":"10.1016\/j.cmi.2020.07.016","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."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"520","DOI":"10.1016\/j.cmi.2020.12.018","article-title":"Antibiotic prescribing in patients with COVID-19: Rapid review and meta-analysis","volume":"27","author":"Langford","year":"2021","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1093\/jac\/dkx413","article-title":"Impact of antimicrobial stewardship interventions on Clostridium difficile infection and clinical outcomes: Segmented regression analyses","volume":"73","author":"Patton","year":"2018","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1038\/nrgastro.2010.190","article-title":"Clostridium difficile infection: Epidemiology, risk factors and management","volume":"8","author":"Ananthakrishnan","year":"2011","journal-title":"Nat. Rev. Gastroenterol. Hepatol."},{"key":"ref_75","doi-asserted-by":"crossref","unstructured":"Abubakar, U. (2020). Antibiotic use among hospitalized patients in northern Nigeria: A multicenter point-prevalence survey. BMC Infect. Dis., 20.","DOI":"10.1186\/s12879-020-4815-4"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"1037","DOI":"10.1007\/s11096-018-0702-0","article-title":"Utilization of surgical antibiotic prophylaxis for obstetrics and gynaecology surgeries in Northern Nigeria","volume":"40","author":"Abubakar","year":"2018","journal-title":"Int. J. Clin. Pharm."},{"key":"ref_77","doi-asserted-by":"crossref","unstructured":"Abubakar, U., Syed Sulaiman, S.A., and Adesiyun, A.G. (2019). Impact of pharmacist-led antibiotic stewardship interventions on compliance with surgical antibiotic prophylaxis in obstetric and gynecologic surgeries in Nigeria. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0213395"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"1440","DOI":"10.1002\/nau.24979","article-title":"The impact of the coronavirus disease 2019 pandemic on changes in antimicrobial prophylaxis and development of genito-urinary tract infections after urodynamic study: A retrospective comparative study of a single rehabilitation hospital in Japan","volume":"41","author":"Mukai","year":"2022","journal-title":"Neurourol. Urodyn."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"e25567","DOI":"10.1097\/MD.0000000000025567","article-title":"Risk factors for surgical site infection following spinal surgery in Saudi Arabia: A retrospective case\u2013control study","volume":"100","author":"AlGamdi","year":"2021","journal-title":"Medicine"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"220","DOI":"10.1308\/rcsann.2019.0001","article-title":"Risk factors for surgical site infections in neurosurgery","volume":"101","author":"Patel","year":"2019","journal-title":"Ann. R. Coll. Surg. Engl."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1016\/j.ejso.2012.02.179","article-title":"Risk factors for surgical site infections after breast surgery: A systematic review and meta-analysis","volume":"38","author":"Xue","year":"2012","journal-title":"Eur. J. Surg. Oncol. (EJSO)"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1007\/s00590-014-1475-3","article-title":"Epidemiology and risk factors for surgical site infections in patients requiring orthopedic surgery","volume":"25","author":"Jain","year":"2015","journal-title":"Eur. J. Orthop. Surg. Traumatol."}],"container-title":["Antibiotics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-6382\/12\/11\/1600\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T21:18:53Z","timestamp":1760131133000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-6382\/12\/11\/1600"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,11,7]]},"references-count":82,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2023,11]]}},"alternative-id":["antibiotics12111600"],"URL":"https:\/\/doi.org\/10.3390\/antibiotics12111600","relation":{},"ISSN":["2079-6382"],"issn-type":[{"value":"2079-6382","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,11,7]]}}}