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Antimicrobial Agents and Chemotherapy, February 2000, p. 433-436, Vol. 44, No. 2
Antibiotic Resistance Monitoring and
Reference Laboratory, Central Public Health Laboratory, London NW9
5HT,1 The Guys, King's and St. Thomas'
School of Dentistry, London SE5 9RW,2 and
Public Health Laboratory and Medical Microbiology Department,
The Guys, King's and St. Thomas' School of Medicine, London SE5
9PJ,3 United Kingdom
Received 21 June 1999/Returned for modification 17 August
1999/Accepted 16 November 1999
Twenty-eight quinupristin-dalfopristin-resistant isolates of
Enterococcus faecium from hospital patients and nonhuman
sources in European countries were studied. High-level resistance
(MICs, Quinupristin-dalfopristin is a
semisynthetic, injectable mixture of streptogramin A and B compounds
which has recently been licensed for clinical use in the United States
and in Europe for the treatment of infections caused by multiresistant
gram-positive pathogens, including glycopeptide-resistant
Enterococcus faecium (9, 17, 18). Virginiamycin,
another streptogramin A and B combination, has been used as a growth
promoter in animal feed for many years. It selects for
virginiamycin-resistant strains of E. faecium, which are
cross-resistant to quinupristin-dalfopristin (11, 12, 19)
and which may pose a risk to public health. As a consequence, the use
of virginiamycin has been banned in the European Union.
Resistance to mixtures of streptogramin A and B compounds was first
reported among staphylococci (10) and requires only resistance to the A component (15), although resistance to
both the A and B components may give a higher level of resistance (B. Bozdogan and R. Leclercq, Abstr. 39th Intersci. Conf. Antimicrob. Agents Chemother., abstr. 841, 1999). Several genes conferring resistance to type A streptogramins have been identified in
staphylococci (1-5, 7, 8). In this paper we adopt the
nomenclature proposed recently by Roberts and colleagues
(16). The staphylococcal genes vat(A),
vat(B), and vat(C) encode acetyltransferases
(2, 4, 7); vga(A) and vga(B) encode
ATP-binding proteins involved in active efflux (3, 5). Among
enterococci, Enterococcus faecalis is naturally resistant to
streptogramin A-B combinations (15), whereas most isolates
of E. faecium are susceptible. Two acetyltransferase genes,
satA (15) and satG (20),
have been characterized for strains of E. faecium resistant
to streptogramin A-B combinations. These have been renamed
vat(D) and vat(E), respectively (16).
However, vat(D) occurs in only a minority of the resistant E. faecium organisms investigated in several countries in
the European Union (11, 12), and the prevalence of
vat(E) is unknown. In this study we investigated the basis
of resistance to quinupristin-dalfopristin in a small, diverse group of
E. faecium isolates.
(This work was presented at the 39th Interscience Conference on
Antimicrobial Agents and Chemotherapy, San Francisco, Calif., September
1999.)
Twenty-eight quinupristin-dalfopristin-resistant (MICs, The MICs of quinupristin-dalfopristin (Rhone Poulenc Rorer, West
Malling, UK) and virginiamycin (Pfizer, Rixensart, Belgium) were
determined by agar incorporation in DST agar (Oxoid, Basingstoke, UK)
containing 5% lysed horse blood, with an inoculum of 104
CFU per spot. Etest strips (Cambridge Diagnostic Services, Cambridge, UK) were used for some quinupristin-dalfopristin MIC determinations. Isolates were screened by PCR for vat(A), vat(B),
vat(C), vat(D), vat(E),
vga(A), vga(B), vgb(A),
vgb(B), and erm(B). The primer sequences and
cycling conditions are listed in Table 1.
Degenerate primers M and N (Table 1), derived from motifs conserved
within streptogramin A acetyltransferases (14), were used to
detect putative genes encoding acetyltransferases in
quinupristin-dalfopristin-resistant isolates. Plasmid DNA was isolated
from E. faecium isolates by alkaline lysis (22),
separated by electrophoresis through 0.8% agarose gels, and
transferred to nylon membranes by vacuum blotting. Hybridization was
performed at high stringency using digoxigenin-labeled vat(D)- and vat(E)-specific probes, which were
prepared by incorporation of digoxigenin-11-dUTP (Roche, Lewes, UK)
into PCR products. Escherichia coli strain 39R861 (NCTC
50192), an isolate containing plasmids of known size, was used as a
source of molecular size markers.
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Mechanisms of Resistance to
Quinupristin-Dalfopristin among Isolates of Enterococcus
faecium from Animals, Raw Meat, and Hospital Patients in
Western Europe
ABSTRACT
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32 µg/ml) was associated with the presence of
vat(E) (satG) (14 isolates [50%]) or
vat(D) (satA) (6 isolates [21%]). These
genes were not detected in eight (29%) isolates with lower levels of quinupristin-dalfopristin resistance (MICs, 4 to 16 µg/ml).
This suggests the presence of further mechanisms of resistance to
quinupristin-dalfopristin in E. faecium.
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4 µg/ml)
isolates of E. faecium were collected in the United Kingdom (UK) and other European countries prior to both the licensing of
quinupristin-dalfopristin and the ban on virginiamycin use: 18 from
animals (15 from pigs and 3 from chickens), 4 from raw meat, 2 from
sewage, and 4 from UK hospital patients. Isolates from hospital
patients, raw meat, and sewage were from a collection of enterococci
kept at the Antibiotic Resistance Monitoring and Reference Laboratory.
Animal isolates were kindly provided by Pfizer Ltd., Reigate, UK).
E. faecium strain BM4145 [vat(D)] (kindly supplied by P. Courvalin, Institut Pasteur, Paris, France) and three
strains of staphylococci, BM3093 [vat(A) vga(A)
vgb(A)], BM12235 [vat(B) vga(B)],
and BM12392 [vgb(B) vat(C)] (kindly supplied by
N. El-Solh, Institut Pasteur, Paris, France), were used as positive PCR
controls. A vat(E)-positive control strain was not available
for this study. The identity of all isolates was confirmed by
amplification of the E. faecium-specific gene encoding
D-alanyl-D-alanine ligase (21).
TABLE 1.
Primer sequences and PCR conditions used for
streptogramin resistance genes
The 28 quinupristin-dalfopristin-resistant isolates of E. faecium studied were divided into three categories: 6 (21%)
isolates (from live pigs in Belgium, Germany, Spain, and The
Netherlands) contained vat(D), 14 (50%) isolates (from UK
hospital patients, from live pigs and poultry, and from raw poultry
meat in Spain, Germany, and the UK) contained vat(E), and 8 (29%) isolates (from live pigs, raw poultry meat, and sewage in
Belgium, Spain, and the UK) contained neither of these genes (Table
2). The MICs of both
quinupristin-dalfopristin and virginiamycin were 32 µg/ml for all
vat(D)- or vat(E)-positive isolates. In contrast,
the eight vat(D)-negative, vat(E)-negative
isolates had lower levels of resistance to quinupristin-dalfopristin
(MICs, 4 to 16 µg/ml) and virginiamycin (MICs, 2 to 4 µg/ml). None
of the isolates carried the vat(A), vat(B),
vat(C), vga(A), and vga(B)
streptogramin A resistance genes or the vgb(A) and
vgb(B) streptogramin B resistance genes (4, 6)
previously detected in staphylococci. The erm(B) gene,
conferring macrolide-lincosamide-streptogramin B resistance (13), was detected in 82% of the isolates tested and in
75% of isolates in each quinupristin-dalfopristin resistance
category (Table 2). The absence of erm(B) from some
vat(D)- or vat(E)-positive isolates does not rule
out the presence of other genes conferring resistance to streptogramin
B compounds; it has been reported recently that resistance to both the
A and B components is necessary to confer high-level resistance to
streptogramin combinations on E. faecium (Bozdogan and
Leclercq, 39th ICAAC).
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When degenerate primers M and N were used to detect genes likely to encode streptogramin A acetyltransferases, amplicons of ca. 150 bp were obtained from the 20 vat(D)- or vat(E)-positive isolates but from none of the 8 negative isolates. When the DNA was blotted onto nylon membranes, the M and N amplicons from vat(D)-positive strains hybridized only with a vat(D)-specific probe, and those from vat(E)-positive isolates hybridized only with a vat(E)-specific probe. Plasmid DNA prepared from the eight vat(D)-negative, vat(E)-negative isolates failed to hybridize with either vat(D)- or vat(E)-specific probes. The vat(E)-specific probe hybridized with plasmids in the range of 35 to 100 MDa in all vat(E)-positive isolates (not shown).
The proportion of quinupristin-dalfopristin-resistant isolates shown to contain vat(D) (21%) is similar to that reported by other workers (11, 12). The majority of vat(D)-negative isolates (63% [14 of 22]) carried the recently described vat(E) gene (20). Our data indicate wide dissemination of vat(E), which we confirmed to be plasmid mediated, among enterococci from diverse sources and countries. One of the resistance plasmids now known to carry vat(E) could be transferred in vitro to a sensitive laboratory strain of E. faecium (23). Eight diverse isolates expressed lower levels of streptogramin resistance but contained no detectable acetyltransferase genes. The degenerate primers used yielded products with the five genes, vat(A) to vat(E), known to encode streptogramin A acetyltransferases, but we cannot rule out the possibility that these isolates contain unrelated acetyltransferases. However, their streptogramin resistance may have resulted from a mechanism unrelated to acetyltransferase production. Active efflux associated with ATP-binding cassette transporters (3, 5) is the only other mechanism reported to confer resistance to streptogramin A compounds, and it is possible that these isolates have such a mechanism, although the demonstration of this requires further study.
In conclusion, we have shown that distinct categories of quinupristin-dalfopristin resistance exist in isolates of E. faecium. The Vat(D) and Vat(E) acetyltransferases occurred in enterococci from different European countries and conferred resistance to both quinupristin-dalfopristin and virginiamycin. An undefined mechanism conferred higher levels of resistance to quinupristin-dalfopristin than to virginiamycin. A wide distribution of vat(D) in strains from human and nonhuman sources has been reported previously (11, 12, 19). Similarly, in this study we detected vat(E) on plasmids in E. faecium isolated from farm animals, meat, and UK hospital patients; comparable findings have been reported in Germany (20). None of the UK patients had received quinupristin-dalfopristin. It therefore seems likely that exchange of resistant strains or resistance genes may occur between E. faecium isolates from nonhuman and human sources. Until such time as these fears are proven to be unfounded, the occurrence of virginiamycin-resistant E. faecium in animals must be considered to remain a potential risk to public health, the extent of which has yet to be quantified.
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ACKNOWLEDGMENTS |
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We are grateful to Pim Kon (Rhone Poulenc Rorer Ltd.) for providing quinupristin-dalfopristin, to Pfizer for providing virginiamycin and resistant isolates of E. faecium from animals, and to Anette Hammerum and Lars Jensen (Danish Veterinary Laboratory) for sharing data concerning PCR primers and cycling conditions prior to publication. M.S. was supported by a Ph.D. studentship award from the PHLS Central Research and Development Fund.
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FOOTNOTES |
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* Corresponding author. Mailing address: ARMRL, CPHL, 61 Colindale Ave., London NW9 5HT, United Kingdom. Phone: 44-208-200-4400. Fax: 44-208-200-7449. E-mail: nwoodford{at}phls.nhs.uk.
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