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Letter
Vancomycin-resistant Enterococcus
faecium Clone in Swine, Europe
Carla Novais,* Teresa M. Coque,† Patrick Boerlin,‡ Inmaculada Herrero,§
Miguel A. Moreno,§ Lucas Dominguez,§ and Luísa Peixe*
*REQUIMTE at Universidade do Porto, Porto, Portugal; †Hospital Universitario
Ramón y Cajal, Madrid, Spain; ‡University of Guelph, Ontario, Canada;
and §Universidad Complutense de Madrid, Madrid, Spain
Suggested
citation for this article
To the Editor: The use of antimicrobial agents for growth promotion
(AGP) in food-producing animals has been extensively debated because of
the risk of establishing a reservoir of antimicrobial resistance genes
or antimicrobial-resistant organisms of potential relevance for human
health. This concern has motivated the progressive ban of the use of different
AGP in the European Union, which began in 1997 with avoparcin and will
end in 2006 (1). Worldwide trade of living animals for
food production or breeding and of meat products enables multidrug-resistant
pathogens to spread across national borders.
Intercontinental dissemination of antimicrobial-resistant bacteria associated
with food animals has been described for particular clones such as Salmonella
enterica Typhimurium DT104 or Escherichia coli O157:H7 and
for transferable genetic elements such as the genomic island SG1 or the
streptococcal plasmid pRE25 (2). Vancomycin-resistant
enterococci (VRE) in European farms were initially associated with the
intensive use of avoparcin; however, the persistence of VRE in food animal
environments after years of avoparcin withdrawal indicates that coselection
by further antimicrobial or other agents, increased fitness of strains,
and mobile genetic elements cannot be ruled out (1–3).
A specific clone was recently detected among vancomycin-resistant E.
faecium (VREF) isolated from different swine farms in Denmark and
Switzerland and from a healthy Danish woman without antimicrobial drug
exposure who ate pork, chicken, and beef (4,5). Since
Portugal and Spain maintain commercial trade of food-producing swine (living
or meat products) between them and with other European countries, including
Denmark (http://www.dgv.min-agricultura.pt/dgv.nsf),
we investigated a possible relationship among VREF swine fecal isolates
from Portugal and Spain and compared these isolates with the Swiss/Danish
clone. We studied 3 VREF from a Figueira da Foz slaughterhouse in central
Portugal (1997–1998) and 3 VREF isolates from 3 Spanish slaughterhouses
in Valencia, Lugo, and Murcia in eastern, northern, and southern Spain,
respectively (1998–2000). These isolates were recovered in the course
of previous surveillance studies (C. Novais/I. Herrero, unpub data). Antimicrobial
susceptibility was tested for 13 antimicrobial agents by using the agar
dilution method (6). Clonal relationships were analyzed
by pulsed-field gel electrophoresis (PFGE) and characterization of pur-K
alleles by amplification and further sequencing (6,7;
http://efaecium.mlst.net). Species
identification, genes coding for antimicrobial resistance genes or for
putative virulence traits, and the backbone structure of Tn1546
were analyzed by polymerase chain reaction followed by sequencing when
necessary (6,8). Broth and filter mating were performed
by using E. faecium GE1 as recipient strain (6).
Following criteria published elsewhere (6), the VREF
isolates studied were considered a single clone (0–4 bands difference
by PFGE). Some vancomycin-susceptible E. faecium swine isolates
(VSEF) from Spain and Switzerland showed an SmaI-PFGE pattern closely
related to that of VREF isolates (data not shown; [4]).
Representative VREF of each country harbored the allele 9 of the housekeeping
gene purK, previously found among E. faecium isolates from
swine and healthy persons (7). All VREF isolates were
resistant to glycopeptides (vanA), erythromycin [erm(B)],
and tetracycline. Two Spanish isolates were also highly resistant to streptomycin
and kanamycin [aph(3´)-IIIa] (Table).
All VREF isolates tested carried a Tn1546 type D, previously found
in isolates from food-producing animals (8). This element
showed alterations in orf1 and a G-T point mutation in the position
8234 at vanX. Transfer of vancomycin resistance was detected for
the Swiss (4), Spanish, and Portuguese isolates and was
associated with erythromycin resistance in all cases. Tetracycline resistance
was also transferable in the Spanish strains. No virulence traits were
detected.
We describe the simultaneous occurrence of a VREF strain among swine
in 4 distant European countries for at least a 4-year period. Tn1546
type D has been largely described in European swine isolates, which indicates
stability of this particular type among the high diversity of Tn1546
described to date (8). The finding of a group of genetically
closely related strains, which include both VSEF and VREF isolates and
which harbor a particular purK allele previously associated with
E. faecium swine strains, might mirror wide dissemination of a
host-specific clone more prone than others to acquire and spread different
antimicrobial resistance, as reported for human clinical E. faecium
isolates (9). Since enterococci from swine are able to
colonize in the human gut (5,7) and isolates harboring
purK-9 can be recovered from hospitalized patients with severe
infections (10), specific swine enterococcal strains
might represent a risk for antimicrobial resistance spread in the clinical
setting. Further analyses need to be performed to understand the role
of international animal movements, animal feed, and colonized farmers
in the spread of this particular strain and to assess whether this clone
shows an increased fitness in the porcine intestine when compared to other
E. faecium strains.
C. Novais was supported
by a fellowship from Fundação para a Ciência e Tecnologia (SFRH/BD/3372/2000).
References
- Phillips I, Casewell M, Cox T, Groot B, Friis C, Jones
R, et al. Does
the use of antibiotics in food animals pose a risk to human health?
A critical review of published data. J Antimicrob Chemother. 2004;53(Suppl
1):28–52.
- Teuber M. Veterinary
use and antibiotic resistance. Curr Opin Microbiol. 2001;4:493–9.
- Johnsen PJ, Østerhus JI, Sletvold H, Sorum M, Kruse H, Nielsen K,
et al. Persistence
of animal and human glycopeptide-resistant enterococci on two Norwegian
poultry farms formerly exposed to avoparcin is associated with a widespread
plasmid-mediated vanA element within a polyclonal Enterococcus
faecium population. Appl Environ Microbiol. 2005;71:159–68.
- Boerlin P, Wissing A, Aarestrup F, Frey J, Nicolet J. Antimicrobial
growth promoter ban and resistance to macrolides and vancomycin in enterococci
from pigs. J Clin Microbiol. 2001;39:4193–5.
- Hammerum A, Lester C, Neimann J, Porsbo L, Olsen K, Jensen L, et al.
A
vancomycin-resistant Enterococcus faecium isolate from a Danish
healthy volunteer, detected 7 years after the ban of avoparcin, is possibly
related to pig isolates. J Antimicrob Chemother. 2004;53(Suppl 3):547–9.
- Novais C, Coque TM, Sousa JC, Baquero F, Peixe L. Local
genetic patterns within a vancomycin-resistant Enterococcus faecalis
clone isolated in three hospitals in Portugal. Antimicrob Agents
Chemother. 2004;48:3613–7.
- Homan WL, Tribe D, Poznanski S, Li M, Hogg G, Spalburg E, et al. Multilocus
sequence typing scheme for Enterococcus faecium. J Clin Microbiol.
2002;40:1963–71.
- Woodford N, Adebiy AMA, Palepou MFI, Cookson B. Diversity
of VanA glycopeptide resistance elements in enterococci from humans
and animals. Antimicrob Agents Chemother. 1998;42:502–8.
- Willems RJL, Top J, van Santen M, Robinson A, Coque TM, Baquero F,
et al. Global
spread of vancomycin-resistant Enterococcus faecium from distinct
nosocomial genetic complex. Emerg Infect Dis. 2005;11:821–8.
- Coque TM, Willems RJ, Fortun J, Top J, Diz S, Canton R, et al. Population
structure of Enterococcus faecium causing bacteremia in a Spanish
university hospital: setting the scene for a future increase in vancomycin
resistance? Antimicrob Agents Chemother. 2005;49:2693–700.
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Table. Features of vancomycin-resistant
Enterococcus faecium swine isolates from European countries*
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Isolate
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PFGE
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purK
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Antimicrobial-drug susceptibility (mg/L)*†
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Resistance genes†
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Mating‡
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VC
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TC
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AMP
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TET
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ER
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CP
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CL
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GM
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KM
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SM
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LIN
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DA
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NIT
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Portugal§
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7S4
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A
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9
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>256
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256
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<2
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64
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32
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<0,5
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8
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<256
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1,000
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<256
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2
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1
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64
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vanA
erm(B)
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10–4
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8S1
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A3
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ND
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>256
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256
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<2
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32
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>32
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<0,5
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16
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<256
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<256
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<256
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2
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1
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64
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vanA
erm(B)
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10–8
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35S2
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A4
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ND
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>256
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256
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<2
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64
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>32
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<0,5
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8
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<256
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<256
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<256
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2
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0.5
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32
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vanA
erm(B)
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ND
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Spain¶
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S1
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A1
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9
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>256
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128
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<2
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>64
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>32
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<0,25
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8
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<256
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>2,000
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>2,000
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2
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1
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64
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vanA
erm(B)
aphIII
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10–5
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S2
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A2
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ND
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>256
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128
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<2
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64
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>32
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<0,25
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8
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<256
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<256
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<256
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2
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2
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64
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vanA
erm(B)
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10–4
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S8
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A1'
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ND
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>256
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128
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<2
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>64
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>32
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<0,25
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8
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<256
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>2,000
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2,000
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2
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0.5
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64
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vanA
erm(B)
aphIII
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10–5
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Switzerland#
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4D
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A
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9
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>256
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64
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<2
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64
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>32
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<0,25
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<4
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<256
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<256
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<256
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2
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4
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64
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vanA
erm(B)
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10–5
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*PFGE, pulsed-field gel electrophoresis; VC, vancomycin;
TC, teicoplanin; AMP, ampicillin; TET, tetracycline; ER, erythromycin;
CP, ciprofloxacin; CL, chloramphenicol; GM, high level of resistance
to gentamicin; KM, high-level resistance to kanamycin; SM, high-level
resistance to streptomycin; LIN, linezolid; DA, daptomycin; NIT,
nitrofurantoin; ND, not done. All isolates were TN1546 type
D.
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†Antimicrobial resistance or resistance genes detected
in transconjugants appear underlined.
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‡Conjugation frequency is expressed as transconjugants
per donors.
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§First 2 isolates were collected in 1997; third
in 1998.
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¶S1 was isolated in 1998; S2, 1999; and S8, 2000.
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#Isolate was collected in 1999.
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Suggested citation
for this article:
Novais C, Coque TM,
Boerlin P, Herrero I, Moreno MA, Dominguez L, et al. Vancomycin-resistant
Enterococcus faecium clone in swine, Europe [letter]. Emerg Infect
Dis [serial on the Internet]. 2005 Dec [date cited]. Available
from http://www.cdc.gov/ncidod/EID/vol11no12/05-0822.htm
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