{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T22:08:46Z","timestamp":1790114926673,"version":"4.0.1"},"reference-count":28,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2023,2,1]],"date-time":"2023-02-01T00:00:00Z","timestamp":1675209600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004564","name":"Ministry of Education, Science and Technological Development of the Republic of Serbia","doi-asserted-by":"publisher","award":["200110"],"award-info":[{"award-number":["200110"]}],"id":[{"id":"10.13039\/501100004564","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Antibiotics"],"abstract":"<jats:p>Our aim was to investigate gut colonization with carbapenem-resistant Enterobacterales (CRE) in the population of preterm neonates at discharge from a tertiary care center in Serbia. The study included 350 randomly selected neonates\/infants discharged in the period April 2018\u2013May 2019. CRE colonization was present in 88\/350 (25.1%) of patients. Klebsiella pneumoniae producing KPC and OXA-48 carbapenemase were detected in 45 and 42 subjects, respectively, while NDM producing Escherichia coli was identified in one patient only. All OXA-48 strains harbored blaCTX-M-15, while both blaTEM and blaSHV were present in all but one KPC-producing strain. CRE isolates exhibited a multidrug resistance pattern with uniform fluoroquinolone resistance, universal susceptibility to colistin, and variable susceptibility to aminoglycosides. Administration of carbapenems was common (~50%) and it was strongly associated with colonization, as well as the combinational therapeutic regimens that included meropenem, contrary to ampicillin\u2013sulbactam\/colistin therapy and prolonged course of the initial therapy (ampicillin\/amikacin \u2265 7 days). Other risk factors for CRE carriage were level of immaturity, admission to neonatal intensive care unit, prolonged hospitalization and invasive procedures. Although the rate of clinically and\/or laboratory proven systemic infections was significantly higher among colonized patients, CRE infection was confirmed in one patient only (1.1%) that was colonized with NDM E. coli. Clonal relatedness of CRE isolates was high, with seven and eight clusters detected among KPC (N = 30) and OXA-48 (N = 37) producing strains, respectively. The follow up of the 31 KPC-colonized patients after discharge from hospital revealed common decolonization within one month (~68%). In conclusion, our results demonstrated a high rate of CRE colonization that is most likely related to carbapenem consumption and lack of screening as important infection prevention practice.<\/jats:p>","DOI":"10.3390\/antibiotics12020284","type":"journal-article","created":{"date-parts":[[2023,2,1]],"date-time":"2023-02-01T02:52:02Z","timestamp":1675219922000},"page":"284","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":16,"title":["Intestinal Colonization of Preterm Neonates with Carbapenem Resistant Enterobacteria at Hospital Discharge"],"prefix":"10.3390","volume":"12","author":[{"given":"Vera","family":"Mijac","sequence":"first","affiliation":[{"name":"University of Belgrade, Faculty of Medicine, Institute of Microbiology and Immunology, Department of Microbiology, 11000 Belgrade, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Snezana","family":"Brkic","sequence":"additional","affiliation":[{"name":"Institute for Laboratory Diagnostics Konzilijum, 11000 Belgrade, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marija","family":"Milic","sequence":"additional","affiliation":[{"name":"Institute of Neonatology, 11000 Belgrade, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marina","family":"Siljic","sequence":"additional","affiliation":[{"name":"University of Belgrade, Faculty of Medicine, Institute of Microbiology and Immunology, Department of Microbiology, 11000 Belgrade, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0453-5945","authenticated-orcid":false,"given":"Valentina","family":"Cirkovic","sequence":"additional","affiliation":[{"name":"University of Belgrade, Faculty of Medicine, Institute of Microbiology and Immunology, Department of Microbiology, 11000 Belgrade, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vladimir","family":"Perovic","sequence":"additional","affiliation":[{"name":"University of Belgrade, Faculty of Medicine, Institute of Microbiology and Immunology, Department of Immunology, 11000 Belgrade, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9932-6403","authenticated-orcid":false,"given":"Milos","family":"Markovic","sequence":"additional","affiliation":[{"name":"University of Belgrade, Faculty of Medicine, Institute of Microbiology and Immunology, Department of Immunology, 11000 Belgrade, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ivana","family":"Cirkovic","sequence":"additional","affiliation":[{"name":"University of Belgrade, Faculty of Medicine, Institute of Microbiology and Immunology, Department of Microbiology, 11000 Belgrade, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4643-4272","authenticated-orcid":false,"given":"Maja","family":"Stanojevic","sequence":"additional","affiliation":[{"name":"University of Belgrade, Faculty of Medicine, Institute of Microbiology and Immunology, Department of Microbiology, 11000 Belgrade, Serbia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,2,1]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"S28","DOI":"10.1093\/infdis\/jiw282","article-title":"The Epidemiology of Carbapenem-Resistant Enterobacteriaceae: The Impact and Evolution of a Global Menace","volume":"215","author":"Logan","year":"2017","journal-title":"J. Infect. Dis."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"2053","DOI":"10.1007\/s10096-021-04296-1","article-title":"Treatment for carbapenem-resistant Enterobacterales infections: Recent advances and future directions","volume":"40","author":"Tompkins","year":"2021","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis. Off. Publ. Eur. Soc. Clin. Microbiol."},{"key":"ref_3","first-page":"251","article-title":"The relationship between Gram-negative colonization and bloodstream infections in neonates: A systematic review and meta-analysis","volume":"24","author":"Folgori","year":"2018","journal-title":"Clin. Microbiol. Infect. Off. Publ. Eur. Soc. Clin. Microbiol. Infect. Dis."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1016\/j.ajic.2015.12.005","article-title":"Risk of infection following colonization with carbapenem-resistant Enterobactericeae: A systematic review","volume":"44","author":"Tischendorf","year":"2016","journal-title":"Am. J. Infect. Control"},{"key":"ref_5","first-page":"1","article-title":"ESCMID guidelines for the management of the infection control measures to reduce transmission of multidrug-resistant Gram-negative bacteria in hospitalized patients","volume":"20","author":"Tacconelli","year":"2014","journal-title":"Clin. Microbiol. Infect. Off. Publ. Eur. Soc. Clin. Microbiol. Infect. Dis."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Wang, J., Lv, Y., Yang, W., Zhao, P., and Yin, C. (2022). Epidemiology and clinical characteristics of infection\/colonization due to carbapenemase-producing Enterobacterales in neonatal patients. BMC Microbiol., 22.","DOI":"10.1186\/s12866-022-02585-z"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1093\/jpids\/piw014","article-title":"Colonization With Antimicrobial-Resistant Gram-Negative Bacilli at Neonatal Intensive Care Unit Discharge","volume":"6","author":"Clock","year":"2017","journal-title":"J. Pediatr. Infect. Dis. Soc."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1097\/QCO.0000000000000371","article-title":"Antimicrobial-resistant Gram-negative infections in neonates: Burden of disease and challenges in treatment","volume":"30","author":"Folgori","year":"2017","journal-title":"Curr. Opin. Infect. Dis."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"e01440-17","DOI":"10.1128\/AAC.01440-17","article-title":"Multicenter Study of the Risk Factors for Colonization or Infection with Carbapenem-Resistant Enterobacteriaceae in Children","volume":"61","author":"Chiotos","year":"2017","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Arhoune, B., El Fakir, S., Himri, S., Moutaouakkil, K., El Hassouni, S., Benboubker, M., Hmami, F., and Oumokhtar, B. (2021). Intense intestinal carriage and subsequent acquisition of multidrug-resistant enterobacteria in neonatal intensive care unit in Morocco. PLoS ONE, 16.","DOI":"10.1371\/journal.pone.0251810"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/j.jinf.2019.05.013","article-title":"High prevalence of colonisation with carbapenem-resistant Enterobacteriaceae among patients admitted to Vietnamese hospitals: Risk factors and burden of disease","volume":"79","author":"Tran","year":"2019","journal-title":"J. Infect."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"e4607","DOI":"10.1093\/cid\/ciaa1295","article-title":"Household Transmission of Carbapenemase-Producing Enterobacterales (CPE) in Ontario, Canada","volume":"73","author":"Jamal","year":"2020","journal-title":"Clin. Infect. Dis. Off. Publ. Infect. Dis. Soc. Am."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"190","DOI":"10.1016\/j.ajic.2012.09.020","article-title":"Duration of carriage of carbapenem-resistant Enterobacteriaceae following hospital discharge","volume":"41","author":"Zimmerman","year":"2013","journal-title":"Am. J. Infect. Control"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Milic, M., Siljic, M., Cirkovic, V., Jovicevic, M., Perovic, V., Markovic, M., Martic, J., Stanojevic, M., and Mijac, V. (2021). Colonization with Multidrug-Resistant Bacteria in the First Week of Life among Hospitalized Preterm Neonates in Serbia: Risk Factors and Outcomes. Microorganisms, 9.","DOI":"10.3390\/microorganisms9122613"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"e31","DOI":"10.1016\/j.ajic.2018.01.007","article-title":"Predictors for gut colonization of carbapenem-resistant Enterobacteriaceae in neonates in a neonatal intensive care unit","volume":"46","author":"Singh","year":"2018","journal-title":"Am. J. Infect. Control"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"e3016","DOI":"10.1097\/MD.0000000000003016","article-title":"The Increasing Challenge of Multidrug-Resistant Gram-Negative Bacilli: Results of a 5-Year Active Surveillance Program in a Neonatal Intensive Care Unit","volume":"95","author":"Geraci","year":"2016","journal-title":"Medicine"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"407","DOI":"10.1097\/INF.0b013e3182875227","article-title":"Surveillance of multidrug-resistant Gram-negative pathogens in high-risk neonates\u2014Does it make a difference?","volume":"32","author":"Simon","year":"2013","journal-title":"Pediatr. Infect. Dis. J."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1007\/s10096-014-2232-6","article-title":"Neonatal sepsis: The gut connection","volume":"34","author":"Basu","year":"2015","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis. Off. Publ. Eur. Soc. Clin. Microbiol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"294","DOI":"10.3389\/fmicb.2020.00294","article-title":"Genomic Epidemiology of Carbapenem- and Colistin-Resistant Klebsiella pneumoniae Isolates From Serbia: Predominance of ST101 Strains Carrying a Novel OXA-48 Plasmid","volume":"11","author":"Palmieri","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1525072","DOI":"10.1155\/2018\/1525072","article-title":"Transmission Risk on a Neonatal Intensive Care Unit: Escherichia coli versus Klebsiella pneumoniae","volume":"2018","author":"Artelt","year":"2018","journal-title":"Can. J. Infect. Dis. Med. Microbiol."},{"key":"ref_21","unstructured":"(2022, December 21). World Health Organization\u2014Central Asian and European Surveillance of Antimicrobial Resistance (CAESAR). Available online: https:\/\/apps.who.int\/iris\/handle\/10665\/345873."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1016\/j.jhin.2017.10.017","article-title":"Clinical factors predicting persistent carriage of Klebsiella pneumoniae carbapenemase-producing carbapenem-resistant Enterobacteriaceae among patients with known carriage","volume":"99","author":"Kim","year":"2018","journal-title":"J. Hosp. Infect."},{"key":"ref_23","unstructured":"The European Committee on Antimicrobial Susceptibility Testing (EUCAST) (2021). Clinical Breakpoint for Bacteria, EUCAST. Version 11.0."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"490","DOI":"10.1093\/jac\/dkp498","article-title":"Development of a set of multiplex PCR assays for the detection of genes encoding important beta-lactamases in Enterobacteriaceae","volume":"65","author":"Dallenne","year":"2010","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1016\/j.diagmicrobio.2010.12.002","article-title":"Multiplex PCR for detection of acquired carbapenemase genes","volume":"70","author":"Poirel","year":"2011","journal-title":"Diagn. Microbiol. Infect. Dis."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"6823","DOI":"10.1093\/nar\/19.24.6823","article-title":"Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes","volume":"19","author":"Versalovic","year":"1991","journal-title":"Nucleic Acids Res."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Heras, J., Dom\u00ednguez, C., Mata, E., Pascual, V., Lozano, C., Torres, C., and Zarazaga, M. (2015). GelJ\u2014A tool for analyzing DNA fingerprint gel images. BMC Bioinform., 16.","DOI":"10.1186\/s12859-015-0703-0"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"3724","DOI":"10.1128\/AAC.47.12.3724-3732.2003","article-title":"Prevalence and molecular epidemiology of CTX-M extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in Russian hospitals","volume":"47","author":"Edelstein","year":"2003","journal-title":"Antimicrob. Agents Chemother."}],"container-title":["Antibiotics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-6382\/12\/2\/284\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T18:20:30Z","timestamp":1760120430000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-6382\/12\/2\/284"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,2,1]]},"references-count":28,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2023,2]]}},"alternative-id":["antibiotics12020284"],"URL":"https:\/\/doi.org\/10.3390\/antibiotics12020284","relation":{},"ISSN":["2079-6382"],"issn-type":[{"value":"2079-6382","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,2,1]]}}}