{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,30]],"date-time":"2026-10-30T10:41:47Z","timestamp":1793356907397,"version":"4.5.0"},"reference-count":38,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2022,8,9]],"date-time":"2022-08-09T00:00:00Z","timestamp":1660003200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Germany Ministry of Public Health"},{"name":"European Centre for Disease Prevention and Control (ECDC)"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Hospital outbreaks with vancomycin-resistant enterococci (VRE) pose a serious health threat and a challenge to infection prevention and control (IPC). We herein report on a VRE outbreak of unprecedented extent in Southern Germany (October 2015\u2013November 2019). We used descriptive epidemiology and whole-genome sequencing (WGS) for a detailed outbreak investigation. Of the 2905 cases, 2776 (95.3%) were colonized, whereas from 127 (3.7%), VRE could be isolated from otherwise sterile body fluids or sites unlikely for enterococci colonization. Cases had a median age of 78 years (IQR 68\u201384) and 1339\/2905 (46%) were female. The majority of isolates sequenced belonged to the clonal lineage ST80\/CT1013 (212\/397, 53%). Nosocomial transmission was observed as well as the constant import of VRE into the hospital. Extensive IPC measures were implemented and terminated the outbreak in late 2019, eventually. Our study shows that the combination of epidemiological and genomic analyses is indispensable for comprehensive outbreak investigations. The adaptation of IPC measures to these findings, their timely implementation, and strict execution also allow containment of large VRE outbreaks in hospital settings.<\/jats:p>","DOI":"10.3390\/microorganisms10081603","type":"journal-article","created":{"date-parts":[[2022,8,10]],"date-time":"2022-08-10T04:20:32Z","timestamp":1660105232000},"page":"1603","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":27,"title":["Controlling an Unprecedented Outbreak with Vancomycin-Resistant Enterococcus faecium in Germany, October 2015 to November 2019"],"prefix":"10.3390","volume":"10","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5167-3836","authenticated-orcid":false,"given":"Jennifer K.","family":"Bender","sequence":"first","affiliation":[{"name":"Nosocomial Pathogens and Antibiotic Resistances Unit, Department of Infectious Diseases, Robert Koch Institute, 38855 Wernigerode, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Julia","family":"Hermes","sequence":"additional","affiliation":[{"name":"Healthcare-Associated Infections, Surveillance of Antibiotic Resistance and Consumption Unit, Department of Infectious Disease Epidemiology, Robert Koch Institute, 13353 Berlin, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7231-3741","authenticated-orcid":false,"given":"Lutz T.","family":"Zabel","sequence":"additional","affiliation":[{"name":"Alb Fils Kliniken GmbH, 73035 G\u00f6ppingen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8242-711X","authenticated-orcid":false,"given":"Sebastian","family":"Haller","sequence":"additional","affiliation":[{"name":"Healthcare-Associated Infections, Surveillance of Antibiotic Resistance and Consumption Unit, Department of Infectious Disease Epidemiology, Robert Koch Institute, 13353 Berlin, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nadja","family":"M\u00fcrter","sequence":"additional","affiliation":[{"name":"Local Health Authority G\u00f6ppingen, 73033 G\u00f6ppingen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hans-Peter","family":"Blank","sequence":"additional","affiliation":[{"name":"Charit\u00e9 Comprehensive Cancer Center, 10117 Berlin, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guido","family":"Werner","sequence":"additional","affiliation":[{"name":"Nosocomial Pathogens and Antibiotic Resistances Unit, Department of Infectious Diseases, Robert Koch Institute, 38855 Wernigerode, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ingo","family":"H\u00fcttner","sequence":"additional","affiliation":[{"name":"Alb Fils Kliniken GmbH, 73035 G\u00f6ppingen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tim","family":"Eckmanns","sequence":"additional","affiliation":[{"name":"Healthcare-Associated Infections, Surveillance of Antibiotic Resistance and Consumption Unit, Department of Infectious Disease Epidemiology, Robert Koch Institute, 13353 Berlin, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,8,9]]},"reference":[{"key":"ref_1","unstructured":"Gilmore, M.S., Clewell, D.B., Ike, Y., and Shankar, N. (2014). Enterococcal disease, epidemiology, and implications for treatment. Enterococci: From Commensals to Leading Causes of Drug Resistant Infection, Massachusetts Eye and Ear Infirmary."},{"key":"ref_2","first-page":"1","article-title":"Antimicrobial-resistant pathogens associated with adult healthcare-associated infections: Summary of data reported to the National Healthcare Safety Network, 2015\u20132017","volume":"41","author":"Abner","year":"2020","journal-title":"Infect. Control. Hosp. Epidemiol."},{"key":"ref_3","unstructured":"World Health Organization (2017). WHO List of Bacteria for Which New Antibiotics Are Urgently Needed, WHO."},{"key":"ref_4","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_5","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1186\/s13756-018-0374-5","article-title":"Outbreak report: A nosocomial outbreak of vancomycin resistant enterococci in a solid organ transplant unit","volume":"7","author":"Kreidl","year":"2018","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"11917","DOI":"10.1038\/s41598-019-48436-2","article-title":"Molecular analysis and epidemiological typing of Vancomycin-resistant Enterococcus outbreak strains","volume":"9","author":"Rangberg","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"2336","DOI":"10.1093\/cid\/ciz666","article-title":"Outbreak of Vancomycin-resistant Enterococcus faecium in Interventional Radiology: Detection Through Whole-genome Sequencing-based Surveillance","volume":"70","author":"Sundermann","year":"2020","journal-title":"Clin. Infect. Dis."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1186\/s13756-021-00906-x","article-title":"Management of a hospital-wide vancomycin-resistant Enterococcus faecium outbreak in a Dutch general hospital, 2014\u20132017: Successful control using a restrictive screening strategy","volume":"10","author":"Weterings","year":"2021","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"e00473","DOI":"10.1016\/j.heliyon.2017.e00473","article-title":"Outbreaks caused by vancomycin-resistant Enterococcus faecium in hematology and oncology departments: A systematic review","volume":"3","author":"Ulrich","year":"2017","journal-title":"Heliyon"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"e00534-13","DOI":"10.1128\/mBio.00534-13","article-title":"Emergence of epidemic multidrug-resistant Enterococcus faecium from animal and commensal strains","volume":"4","author":"Lebreton","year":"2013","journal-title":"mBio"},{"key":"ref_11","first-page":"8710","article-title":"H\u00e4ufigkeit und Verbreitung von Vancomycin-resistenten Enterokokken in Deutschland\u2014Update 2019\/2020","volume":"10","author":"Weber","year":"2021","journal-title":"Epid. Bull."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"e133","DOI":"10.1016\/S2666-5247(21)00236-6","article-title":"The interplay between community and hospital Enterococcus faecium clones within health-care settings: A genomic analysis","volume":"3","author":"Willems","year":"2022","journal-title":"Lancet Microbe"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"e216","DOI":"10.1016\/j.jhin.2018.02.016","article-title":"Recommendations for the successful control of a large outbreak of vancomycin-resistant Enterococcus faecium in a non-endemic hospital setting","volume":"100","author":"Frakking","year":"2018","journal-title":"J. Hosp. Infect."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"KRINKO (2018). Hygienema\u00dfnahmen zur Pr\u00e4vention der Infektion durch Enterokokken mit speziellen Antibiotikaresistenzen. Bundesgesundheitsblatt, 61, 51.","DOI":"10.1007\/s00103-018-2811-2"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1007\/BF02300753","article-title":"Accuracy of estimated phylogenetic trees from molecular data. II. Gene frequency data","volume":"19","author":"Nei","year":"1983","journal-title":"J. Mol. Evol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1186\/s13756-022-01081-3","article-title":"Epidemiological and genetic characteristics of vancomycin-resistant Enterococcus faecium isolates in a University Children\u2019s Hospital in Germany: 2019 to 2020","volume":"11","author":"Trautmannsberger","year":"2022","journal-title":"Antimicrob. Resist. Infect. Control."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1078\/1438-4639-00304","article-title":"Two episodes of vancomycin-resistant Enterococcus faecium outbreaks caused by two genetically different clones in a newborn intensive care unit","volume":"207","author":"Borgmann","year":"2004","journal-title":"Int. J. Hyg. Environ. Health"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1033","DOI":"10.1093\/jac\/dkn066","article-title":"Nosocomial outbreak of vancomycin-resistant Enterococcus faecium in a paediatric unit at a Turkish university hospital","volume":"61","author":"Naas","year":"2008","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"206","DOI":"10.1016\/j.ajic.2007.06.005","article-title":"Control of a hospital-wide vancomycin-resistant Enterococci outbreak","volume":"36","author":"Kurup","year":"2008","journal-title":"Am. J. Infect. Control."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1111\/j.1469-0691.2005.01331.x","article-title":"Outbreak of vancomycin-resistant Enterococcus spp. in an Italian general intensive care unit","volume":"12","author":"Peta","year":"2006","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"2474","DOI":"10.1093\/jac\/dkv142","article-title":"Multiple hospital outbreaks of vanA Enterococcus faecium in Denmark, 2012\u20132013, investigated by WGS, MLST and PFGE","volume":"70","author":"Pinholt","year":"2015","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"317","DOI":"10.3201\/eid1402.070752","article-title":"Vancomycin-resistant enterococci outbreak, Germany, and calculation of outbreak start","volume":"14","author":"Sagel","year":"2008","journal-title":"Emerg. Infect. Dis."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/S1413-8670(11)70216-1","article-title":"Outbreak of vancomycin-resistant Enterococcus in a renal transplant unit","volume":"15","author":"Tuon","year":"2011","journal-title":"Braz. J. Infect. Dis."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1186\/s13073-021-00868-0","article-title":"The global dissemination of hospital clones of Enterococcus faecium","volume":"13","author":"Willems","year":"2021","journal-title":"Genome Med."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1388","DOI":"10.1101\/gr.204024.116","article-title":"A decade of genomic history for healthcare-associated Enterococcus faecium in the United Kingdom and Ireland","volume":"26","author":"Raven","year":"2016","journal-title":"Genome Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1186\/s13756-019-0573-8","article-title":"Near-ubiquitous presence of a vancomycin-resistant Enterococcus faecium ST117\/CT71\/vanB -clone in the Rhine-Main metropolitan area of Germany","volume":"8","author":"Falgenhauer","year":"2019","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1186\/s13756-020-00754-1","article-title":"Increase of vancomycin-resistant Enterococcus faecium strain type ST117 CT71 at Charite\u2014Universitatsmedizin Berlin, 2008 to 2018","volume":"9","author":"Weber","year":"2020","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"573","DOI":"10.1086\/598636","article-title":"A polyclonal outbreak of predominantly VanB vancomycin-resistant enterococci in northeast Ohio. Northeast Ohio Vancomycin-Resistant Enterococcus Surveillance Program","volume":"29","author":"Donskey","year":"1999","journal-title":"Clin. Infect. Dis."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1016\/j.idh.2018.12.002","article-title":"An outbreak of vanA vancomycin-resistant Enterococcus faecium in a hospital with endemic vanB VRE","volume":"24","author":"Hughes","year":"2019","journal-title":"Infect. Dis. Health"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1097\/MPH.0b013e318257a5d3","article-title":"Polyclonal outbreak of vancomycin-resistant Enterococcus faecium in a pediatric oncology department","volume":"34","author":"Iosifidis","year":"2012","journal-title":"J. Pediatr. Hematol. Oncol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1128\/AAC.01978-18","article-title":"Expansion of Vancomycin-Resistant Enterococcus faecium in an Academic Tertiary Hospital in Southwest Germany: A Large-Scale Whole-Genome-Based Outbreak Investigation","volume":"63","author":"Liese","year":"2019","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Neumann, B., Bender, J.K., Maier, B.F., Wittig, A., Fuchs, S., Brockmann, D., Semmler, T., Einsele, H., Kraus, S., and Wieler, L.H. (2020). Comprehensive integrated NGS-based surveillance and contact-network modeling unravels transmission dynamics of vancomycin-resistant enterococci in a high-risk population within a tertiary care hospital. PLoS ONE, 15.","DOI":"10.1371\/journal.pone.0235160"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"855","DOI":"10.1016\/S0140-6736(00)04206-9","article-title":"Enterococcal vanB resistance locus in anaerobic bacteria in human faeces","volume":"357","author":"Stinear","year":"2001","journal-title":"Lancet"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Bentivegna, E., Luciani, M., Arcari, L., Santino, I., Simmaco, M., and Martelletti, P. (2021). Reduction of Multidrug-Resistant (MDR) Bacterial Infections during the COVID-19 Pandemic: A Retrospective Study. Int. J. Environ. Res. Public. Health, 18.","DOI":"10.3390\/ijerph18031003"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"2001628","DOI":"10.2807\/1560-7917.ES.2021.26.45.2001628","article-title":"Hospital-acquired infections caused by enterococci: A systematic review and meta-analysis, WHO European Region, 1 January 2010 to 4 February 2020","volume":"26","author":"Brinkwirth","year":"2021","journal-title":"Euro. Surveill."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"ofw246","DOI":"10.1093\/ofid\/ofw246","article-title":"Colonization with Vancomycin-Resistant Enterococci and Risk for Bloodstream Infection Among Patients With Malignancy: A Systematic Review and Meta-Analysis","volume":"4","author":"Alevizakos","year":"2017","journal-title":"Open Forum Infect. Dis."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1016\/j.bbmt.2007.01.078","article-title":"Colonization, bloodstream infection, and mortality caused by vancomycin-resistant enterococcus early after allogeneic hematopoietic stem cell transplant","volume":"13","author":"Weinstock","year":"2007","journal-title":"Biol. Blood Marrow. Transpl."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s13756-017-0291-z","article-title":"Economic burden of nosocomial infections caused by vancomycin-resistant enterococci","volume":"7","author":"Puchter","year":"2018","journal-title":"Antimicrob. Resist. Infect. Control"}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/10\/8\/1603\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T00:06:04Z","timestamp":1760141164000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/10\/8\/1603"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,8,9]]},"references-count":38,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2022,8]]}},"alternative-id":["microorganisms10081603"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms10081603","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,8,9]]}}}