The DOI matches its Crossref record; 102 of the 104 references it cites were found in a registry or an index.
Vancomycin-resistant enterococci: why are they here, and where do they come from?
Abstract
Vancomcyin-resistant enterococci (VRE) have emerged as nosocomial pathogens in the past 10 years, causing epidemiological controversy. In the USA, colonisation with VRE is endemic in many hospitals and increasingly causes infection, but colonisation is absent in healthy people. In Europe, outbreaks still happen sporadically, usually with few serious infections, but colonisation seems to be endemic in healthy people and farm animals. Vancomycin use has been much higher in the USA, where emergence of ampicillin-resistant enterococci preceded emergence of VRE, making them very susceptible to the selective effects of antibiotics. In Europe, avoparcin, a vancomycin-like glycopeptide, has been widely used in the agricultural industry, explaining the community reservoir in European animals. Avoparcin has not been used in the USA, which is consistent with the absence of colonisation in healthy people. From the European animal reservoir, VRE and resistance genes have spread to healthy human beings and hospitalised patients. However, certain genogroups of enterococci in both continents seem to be more capable of causing hospital outbreaks, perhaps because of the presence of a specific virulence factor, the variant esp gene. By contrast with the evidence of a direct link between European animal and human reservoirs, the origin of American resistance genes remains to be established. Considering the spread of antibiotic-resistant bacteria and resistance genes, the emergence of VRE has emphasised the non-existence of boundaries between hospitals, between people and animals, between countries, and probably between continents.
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“This disturbance can lead to the growth and expansion of pathogens within the intestine (including antibiotic-resistant pathogens), where these pathogens can exploit the absence of competitors and the nutrient-enriched gut environment.”
From Role of the gut microbiota in nutrient competition and protection against intestinal pathogen colonization (2023) · cites this paper as [30]
In the citing paper
“This promotes intestinal colonization (and even domination) by pathogens such as Clostridioides difficile , carbapenem-resistant Enterobacteriaceae (CRE) and vancomycin-resistant Enterococcus (VRE) [30–32].”
From Role of the gut microbiota in nutrient competition and protection against intestinal pathogen colonization (2023) · cites this paper as [30]
In the citing paper
“Antibiotic treatment – especially treatment with broad-spectrum antibiotics – kills members of the gut microbiota and disrupts colonization resistance (Fig. 1).”
From Role of the gut microbiota in nutrient competition and protection against intestinal pathogen colonization (2023) · cites this paper as [30]
Citations
Cites
Plasmid-Mediated Resistance to Vancomycin and Teicoplanin in Enterococcus Faecium
Leclercq, R., Derlot, E., Duval, J., & Courvalin, P. M. (1988) · New England Journal of Medicine · doi:10.1056/nejm198807213190307 · Cited by 1,411
Epidemiology of Drug Resistance: Implications for a Post—Antimicrobial Era
Cohen, M. L. (1992) · Science · doi:10.1126/science.257.5073.1050 · Cited by 1,310
VANCOMYCIN-RESISTANT ENTEROCOCCI
Uttley, A. C., Collins, C. H., Naidoo, J., & George, R. C. (1988) · The Lancet · doi:10.1016/s0140-6736(88)91037-9 · Cited by 1,237
Noble, W. C., Virani, Z., & Cree, R. G. A. (1992) · FEMS Microbiology Letters · doi:10.1016/0378-1097(92)90528-v · Cited by 935
Recommendations for Preventing the Spread of Vancomycin Resistance
(1995) · Infection Control and Hospital Epidemiology · doi:10.1086/647066 · Cited by 902
(1999) · American Journal of Infection Control · doi:10.1016/s0196-6553(99)70031-3 · Cited by 899
Vancomycin-Resistant Enterococcal Infections
Murray, B. E. (2000) · New England Journal of Medicine · doi:10.1056/nejm200003093421007 · Cited by 894
Donskey, C. J., Chowdhry, T. K., Hecker, M. T., Hoyen, C. K., Hanrahan, J., Hujer, A. M., Hutton‐Thomas, R., Whalen, C. C., Bonomo, R. A., & Rice, L. B. (2000) · New England Journal of Medicine · doi:10.1056/nejm200012283432604 · Cited by 691
Aarestrup, F. M., Seyfarth, A. M., Emborg, H., Pedersen, K., Hendriksen, R. S., & Bager, F. (2001) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.45.7.2054-2059.2001 · Cited by 653
Arthur, M., Molinas, C., Depardieu, F., & Courvalin, P. M. (1993) · Journal of Bacteriology · doi:10.1128/jb.175.1.117-127.1993 · Cited by 600
Research works printed but not linked: 5
- Hayden MK, Blom DW, Lyle EA, et al. The risk of hand and glove contamination by health care workers after contact with a VRE-positive patient or the patients' environment. Proceedings of the 41st Interscience Conference on Antimicrobial Agents and Chemotherapy; Chicago; Dec 2001: abstract K/1334
- Vandenbroucke-Grauls, 2000, Succesvolle bestrijding van een epidemie met vancomycineresistente Enterococcus faecium op een hematologische afdeling, Ned Tijdschr Med Microbiol, 8, S28
- van der Steen, 2000, Uitbraak van vancomycine-resistente Enterococcus faecium op een afdeling nefrologie, Ned Tijdschr Geneesk, 144, 2568
- Mascini, 2000, Epidemische verheffing van verscheidene genotypen van vancomycine-resistente Enterococcus faecium in een Academisch Ziekenhuis, Ned Tijdschr Geneesk, 144, 2572
- Routsi, 2001, Clinical and molecular surveillance of glycopeptide-resistant Enterococcus faecium in a Greek ICU, Intens Care Med, 27, S151
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Graziani, L., Giani, T., Farese, A., Lauria, N. D., Mantengoli, E., Riccobono, E., Rossolini, G. M., Bartoloni, A., Spinicci, M., The Icare Study Group, et al. (2026) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkag069 · Cited by 4
Căliman-Sturdza, O. A. (2024) · Infectious diseases · doi:10.5772/intechopen.114918 · Cited by 4
Antibacterial drug resistance patterns in poultry isolated enterococci
Asadpour, L. (2012) · African Journal of Microbiology Research · doi:10.5897/ajmr12.187 · Cited by 4
INVESTIGATION OF MILK AND SOME DAIRY PRODUCTS FOR FECAL POLLUTION INDICATORS
El-Prince, E., Sayed, M., Farghaly, M., & ABDEL-RAHMAN, A. M. (2010) · Assiut Veterinary Medical Journal/Maǧallaẗ Asyūṭ al-ṭibiyyaẗ al-baytariyyaẗ · doi:10.21608/avmj.2010.174224 · Cited by 4
Sin, J. H., Ipe, D. S., Hamlet, S. M., Walsh, L. J., Love, R. M., & George, R. (2021) · Photodiagnosis and Photodynamic Therapy · doi:10.1016/j.pdpdt.2021.102344 · Cited by 4
Gyssens, I. C. (2010) · CRC Press eBooks · doi:10.1201/b13787-52 · Cited by 4
Fecal strains Enterococcus mundtii from wild ruminants, their safety and postbiotic potential
Lauková, A., Focková, V., Maďar, M., Bełżecki, G., Miltko, R., & Simonová, M. P. (2025) · Veterinary Research Communications · doi:10.1007/s11259-025-10701-3 · Cited by 3
Delamare, C., Lameloise, V., Lozniewski, A., Perrin, M., Baudin, C., Sellies, J., Mf, D., & Bemer, M. (2008) · Pathologie Biologie · doi:10.1016/j.patbio.2008.07.034 · Cited by 3
Enterococcal Infections and Antimicrobial Resistance in a Tertiary Care Hospital, Eastern India
Sahu, L. S., Dash, M., Paty, B. P., Purohit, G. K., & Chayan, N. (2015) · Afro-Egyptian Journal of Infectious and Endemic Diseases · doi:10.21608/aeji.2015.17846 · Cited by 3
Palmieri, C., Ratsch, I.-M., Princivalli, M. S., Candelaresi, C., Magi, G., Spinaci, C., Coppa, G. V., & Facinelli, B. (2007) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkm387 · Cited by 3
[Antibiotic resistance: measures urgently needed].
Kluijtmans, J. A. J. W., Vandenbroucke‐Grauls, C. M. J. E., & van der Meer, J. W. (2010) · PubMed · Cited by 3
Chahad, O. B., Barros‐Velázquez, J., Calo‐Mata, P., & Bour, M. E. (2015) · African Journal of Microbiology Research · doi:10.5897/ajmr2014.6685 · Cited by 3
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Terkuran, M., Turhan, E. Ü., & Erginkaya, Z. (2019) · Springer eBooks · doi:10.1007/978-3-030-24903-8_18 · Cited by 3
Arbabi, L., Boustanshenas, M., Rahbar, M., Majidpour, A., Shayanfar, N., Afshar, M., Adabi, M., Owlia, P., & Taher, M. T. (2016) · Journal of Molecular Biology Research · doi:10.5539/jmbr.v6n1p35 · Cited by 3
Use of molecular epidemiology in infectious disease surveillance
Besser, J. M. (2013) · Wiley eBooks · doi:10.1002/9781118543504.ch39 · Cited by 3
Ortiz, A., Banks, H. T., Castillo‐Chávez, C., Chowell, G., & Wang, X. (2010) · Journal of Inverse and Ill-Posed Problems · doi:10.1515/jiip.2011.004 · Cited by 2
Terminal room disinfection: how much BETR can it get?
Crotty, M. P., & Jackson, P. J. (2017) · The Lancet · doi:10.1016/s0140-6736(16)32412-6 · Cited by 2
Koffi, A. A. A., Şanlı, N. Ö., Çiftçioğlu, G., & Arda, N. (2024) · Biology Bulletin · doi:10.1134/s1062359024607092 · Cited by 2
Politique de dépistage des BMR : quand et qui faut-il dépister ?
Birgand, G., & Lucet, J. (2013) · Revue Francophone des Laboratoires · doi:10.1016/s1773-035x(13)72079-3 · Cited by 3
Siddig, L. A., Bayoumi, M., & Elhadi, N. (2023) · PeerJ · doi:10.7717/peerj.16169 · Cited by 2
Tigecycline: a new antimicrobial agent against multiresistant bacteria
Cercenado, E. (2007) · Therapy · doi:10.2217/14750708.4.3.255 · Cited by 2
Çepoğlu, H., Adıgüzel, M. C., BAĞCIGİL, A. F., & Ak, S. (2016) · Journal of Anatolian Environmental and Animal Sciences · doi:10.35229/jaes.280740 · Cited by 2
Microbial pathogenesis and biofilm mediated by Enterococcus
Mousavi, M. R. N., & Rostami, F. (2018) · Reviews in Medical Microbiology · doi:10.1097/mrm.0000000000000132 · Cited by 2
Modeling the transmission of vancomycin-resistant enterococcus (VRE) in hospitals: A case study
Ortiz, A. R., Banks, H. T., Castillo‐Chávez, C., Chowell, G., Torres‐Viera, C., & Wang, X. (2010) · NCSU Libraries Repository (North Carolina State University Libraries) · Cited by 2
Liguori, G., Villari, P., Boccia, S., Gallé, F., Onofrio, V. D., Marzuillo, C., Amore, R., & Rossano, F. (2024) · Italian Journal of Public Health · doi:10.2427/5880 · Cited by 2
Selective decontamination of the digestive tract: all questions answered?
Bonten, M. J. M., Joore, H. C. A., de Jongh, B. M., Kluytmans, J. A. J. W., Kuijper, E. J., van Leeuwen, H. J., de Smet, A. M. G. A., & Vandenbroucke‐Grauls, C. M. J. E. (2003) · Critical Care · doi:10.1186/cc1881 · Cited by 2
Self-citationBrkic, S. V., Bugaric, P., Topalov, D., & Cirkovic, I. B. (2017) · Srpski arhiv za celokupno lekarstvo · doi:10.2298/sarh160411035b · Cited by 1
Controlling the Spread of Resistant Pathogens in the Intensive Care Unit
Palmore, T. N., & Henderson, D. K. (2017) · Springer eBooks · doi:10.1007/978-3-319-47266-9_41 · Cited by 1
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Henderson, D. K. (2009) · Humana Press eBooks · doi:10.1007/978-1-60327-595-8_43 · Cited by 1
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Livorsi, D. J., Stenehjem, E. A., & Gaynes, R. P. (2012) · Springer eBooks · doi:10.1007/978-1-4614-4496-1_2 · Cited by 1
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Sharma, S. K. (2023) · Springer eBooks · doi:10.1007/978-981-19-5802-1_41 · Cited by 1
Akıneden, A., Çiçek, C., Türkel, S., Khan, I. U. H., & Abdulmawjood, A. A. (2024) · Polish Journal of Microbiology · doi:10.33073/pjm-2024-030 · Cited by 1
Leendertse, M., Willems, R. J. L., Giebelen, I. A. J., Roelofs, J. J. T. H., Top, J., Bonten, M. J. M., & van der Poll, T. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006775 · Cited by 1
Self-citationValenti, A. J. (2007) · CRC Press eBooks · doi:10.1201/b15169-20 · Cited by 1
Meat Production and Antibiotics Use
Davis, M. F., & Rutkow, L. (2017) · Springer eBooks · doi:10.1007/978-3-319-18002-1_10 · Cited by 1
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Ortiz, A. R., Banks, H. T., Castillo‐Chávez, C., Chowell, G., & Wang, X. (2010) · NCSU Libraries Repository (North Carolina State University Libraries) · Cited by 1
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Whitney, H. G. (2013) · Canadian Medical Association Journal · doi:10.1503/cmaj.113-2095 · Cited by 1
Soler‐Palacín, P., Peña-López, Y., Pujol, M., & Bastida, P. (2007) · Medicina Clínica · doi:10.1157/13107368 · Cited by 1
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Fisman, D. N. (2013) · Canadian Medical Association Journal · doi:10.1503/cmaj.113-2094 · Cited by 1
Zimmermann, K. (2013) · Universitätsbibliothek der FU Berlin Hochschulschriftenstelle u. Dokumentenserver · doi:10.17169/refubium-6080 · Cited by 1
Transfer of antimicrobial resistant bacteria in food
Gobius, K. S. (2004) · Microbiology Australia · doi:10.1071/ma04322 · Cited by 1
Veterinárias, C. A. E., da Costa, P. M., Nunes, T., Vaz‐Pires, P., & Bernardo, F. (2006) · Cited by 1
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Nascimento, F. A. F. R. (2011) · doi:10.47749/t/unicamp.2011.795453
Reservorio: redefinición del origen comunitario de las infecciones resistentes a antimicrobianos
Silbergeld, E. K., Davis, M. F., Leibler, J. H., & Peterson, A. E. (2008) · Clínicas médicas de Norteamérica
Hedberg, C. W. (2002) · University of Minnesota Digital Conservancy (University of Minnesota)
Barros, J. (2010) · Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT)
GLICOPÈPTIDS . MECANISMES D'ACCIÓ I MECANISMES DE RESISTÈNCIA
Domínguez, M. Á. (2005) · Estudis Romànics (Institut d'Estudis Catalans)
Investigation into the regulation and transfer of conjugative transposons of the Tn916-like family
Jasni, A. S. (2013) · UCL Discovery (University College London)
Molecular epidemiology of clinical Enterococcus faecium
Billström, H. (2008) · Figshare
Vancomycin resistant enterococci in Swedish broilers
Nilsson, O. (2011) · Epsilon Open Archive (Sveriges lantbruksuniversitet biblioteket (Swedish University of Agricultural Sciences))
The Role of Antibiotic Policies in Controlling VRE
Bal, A. M. (2011) · Springer eBooks · doi:10.1007/978-1-4419-1734-8_7
Enterococcus faecium infections : where bacterial virulence meets innate immunity
Leendertse, M. (2009) · UvA-DARE (University of Amsterdam)
On mobile genetic elements in enterococci : adding more facets to the complexity
Bjørkeng, E. K. (2010) · NORA - Norwegian Open Research Archives
A resistant culture - ?superbugs? in Australian hospitals
Gilbert, G. L. (2007) · Microbiology Australia · doi:10.1071/ma07182
Werner, G., Coque, T. M., Hammerum, A. M., Hope, R., Hryniewicz, W., Johnson, A., Klare, I., Kristinsson, K. G., Leclercq, R., Lester, C. H., et al. (2008)
Self-citationCurrent and emerging issues in nosocomial infections and antibiotic resistance
Tridgell, Z. (2024) · PEARL (University of Plymouth) · doi:10.24382/9tr4-1a12
da Costa, M. L. R. (2014) · Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT)
El-Ageery, S. M., & Mahran, H. N. F. (2015) · The Egyptian Journal of Medical Microbiology · doi:10.12816/0024936
Genomics and the Challenge of Infectious Disease
Primrose, S. B., & Twyman, R. M. (2003) · Genomics · doi:10.1002/9780470751282.ch3
Evans, D. H. (2005) · CRC Press eBooks · doi:10.1201/b14532-40
Vancomycin (Glycopeptide)-Resistant Enterococci in the Long-Term Care Setting
Bradley, S. (2006) · Infectious disease and therapy · doi:10.3109/9780203909447.024
Sacramento, A. G. (2011) · LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas)
García, M. L. D. G. (2013) · doi:10.18002/10612/3014
Hazarika, P. P., Konwar, T., & Hazarika, A. K. (2020) · International Journal of Advanced Research · doi:10.21474/ijar01/10672
Transplantation of a kidney from a donor with vancomycin-resistantEnterococci
Lim, J. H., Kim, C. J., Oh, J. H., Cho, A. Y., Chang, M. O., Kim, Y. S., Lee, K. Y., & Sun, I. O. (2020) · Korean Journal of Transplantation · doi:10.4285/kjt.2020.34.2.114
Anand, R. K. (2020) · Springer eBooks · doi:10.1007/978-981-15-4039-4_22
Novel computational approaches to predict and reconstruct bacterial plasmids
Alonso, S. A. (2020) · Utrecht University Repository (Utrecht University) · doi:10.33540/302
Andreu, V. P. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.01.05.574403
Stangl, F. P., Kranz, J., Wagenlehner, F. R. A., Marschall, J., Schubert, S., Medina‐Polo, J., Schneidewind, L., & Johansen, T. E. B. (2024) · Springer eBooks · doi:10.1007/978-3-319-92366-6_13
Sasidharan, S. (2025) · The Journal of Association of Chest Physicians · doi:10.4103/jacp.jacp_25_25
Çimen, C., Berends, M. S., Bathoorn, E., Lokate, M., Voss, A., Friedrich, A. W., Glasner, C., & Hamprecht, A. (2024) · Figshare · doi:10.6084/m9.figshare.26610054
Çimen, C., Berends, M. S., Bathoorn, E., Lokate, M., Voss, A., Friedrich, A. W., Glasner, C., & Hamprecht, A. (2024) · Figshare · doi:10.6084/m9.figshare.26610051
Community-acquired bleb-related endophthalmitis caused by vancomycin-resistant enterococci
Tang, C.-W., Cheng, C.-K., & Lee, T.-S. (2007) · Canadian Journal of Ophthalmology · doi:10.3129/can.j.ophthalmol.i07-057
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Stangl, F. P., & Kranz, J. (2026) · Die Urologie · doi:10.1007/s00120-026-02838-z
Janjušević, A., Minić, R., & Ćirković, I. (2026) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-026-05644-9
Metadata
- Authors
- Bonten, M. J., Willems, R., & Weinstein, R. A.
- Affiliations
- University Medical Center Utrecht (NL)
- National Institute for Public Health and the Environment (NL)
- John H. Stroger, Jr. Hospital of Cook County (US)
- Corresponding author
- Bonten, Marc JM
- Venue
- The Lancet Infectious Diseases
- Publisher
- Elsevier BV
- Published
- 2001-12
- Volume
- 1
- Issue
- 5
- Pages
- 314-325
- ISSN
- 1473-3099 (ISSN-L)
- OpenAlex
- W1998796942
- Cited by
- 400
- References
- 104
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 10 · 2023: 17 · 2022: 6 · 2021: 10 · 2020: 17 · 2019: 12 · 2018: 14 · 2017: 18 · 2016: 17 · 2015: 11 · 2014: 18 · 2013: 28 · 2012: 25
- FWCI
- 1.20
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Lancet Infectious Diseases (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Microbiology (medical) › Antibiotic Resistance in Bacteria
- Health Sciences › Medicine › Infectious Diseases › Antimicrobial Resistance in Staphylococcus
- Health Sciences › Medicine › Infectious Diseases › Antibiotic Use and Resistance
- Keywords
- vancomycin-resistant enterococci, nosocomial infections, antibiotic resistance, avoparcin, reservoir hosts, human colonization, hospital outbreak, virulence genes, esp gene, resistance gene spread, antimicrobial use
- MeSH terms
- Animals, Animal Husbandry, Anti-Bacterial Agents, Bacterial Proteins, Cross Infection, Disease Outbreaks, Europe, Humans, Membrane Proteins, North America, Vancomycin, Gram-Positive Bacterial Infections, Enterococcus, Enterococcus faecium, Infection Control, Vancomycin Resistance
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