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Journal of Clinical Microbiology, July 2000, p. 2774-2777, Vol. 38, No. 7
0095-1137/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Characterization of Glycopeptide-Resistant Enterococcus
faecium (GRE) from Broilers and Pigs in Denmark: Genetic
Evidence that Persistence of GRE in Pig Herds Is Associated with
Coselection by Resistance to Macrolides
Frank Møller
Aarestrup*
Danish Veterinary Laboratory, DK-1790
Copenhagen, Denmark
Received 24 November 1999/Returned for modification 7 February
2000/Accepted 25 March 2000
 |
ABSTRACT |
Glycopeptide-resistant enterococci (GRE) from broilers and pigs
were characterized to investigate the background for the persistence of
GRE in pig herds. All porcine isolates belonged to closely related
pulsed-field gel electrophoretic (PFGE) types, with the ermB and vanA genes located on the same
transferable genetic element. Broiler isolates belonged to different
PFGE types. The persistence of GRE in Danish pig herds after the ban of
glycopeptides may be explained by the genetic link between
ermB and vanA and coselection by use of
macrolides for treatment and growth promotion.
| |
TEXT |
Glycopeptide-resistant enterococci
(GRE) have emerged as important pathogens since the late 1980s (6,
22). Resistance to glycopeptides in Enterococcus
faecium and Enterococcus faecalis is mediated by the
vanA, vanB, vanD, or vanE
gene cluster (12, 15, 16).
In 1993, vanA-positive GRE were isolated from food animals
in England (10), and since then, GRE containing the
vanA gene have been found among food animals in several
countries worldwide (2, 14, 19, 31). It has been shown that
the occurrence of GRE among food animals is associated with the use of
the glycopeptide avoparcin for growth promotion (1, 7, 19),
and a number of studies have shown that similar E. faecium
clones and vanA gene clusters can be found among food
animals and humans (14, 17, 26, 27, 29, 30).
Because GRE can be transferred from food animals to humans and because
of the risk of severe infections in humans, the use of avoparcin was
banned in Denmark in 1995. A ban followed in Germany in 1996 and in all
European Union countries in 1997.
Whereas several studies have shown an association between the use of
antimicrobial agents and the occurrence of resistance, only a limited
number of studies have reported changes in resistance among natural
populations after the discontinuation of antimicrobial agent usage.
Since the discontinuation of avoparcin usage in animal husbandry, a
decline in the occurrence of GRE in poultry meat has been observed in
Germany (20) and Italy (24) and in fecal samples from humans in the community in Germany (20). Similarly, in Denmark, a decline from 80% to 5% in the occurrence of GRE isolated from broilers was observed from 1995 to 1998, whereas the occurrence of
GRE in pigs remained at about 20% (8). The reason for the persistence of GRE in pig herds is not known but may be a consequence of coselection through the use of other antimicrobial agents. Thus, a
previous study found almost all GRE from pigs to be simultaneously resistant to tetracycline and macrolides (8).
In this study, GRE isolated from broilers and pigs in Denmark from 1995 through 1998 were characterized by pulsed-field gel electrophoresis
(PFGE), hybridization analysis, plasmid profiling, and transferability
studies. Studies of genetic markers may provide an explanation for the
persistence of GRE in pig herds in contrast to broiler flocks.
Bacterial isolates.
Bacterial isolates were obtained from the
Danish surveillance program for antimicrobial resistance (3,
8). A total of 35 glycopeptide-resistant E. faecium
isolates obtained from pigs and 34 isolates obtained from broilers from
1995 through 1998 were included. The isolates from broilers were
distributed as follows: 8 from 1995, 10 from 1996, 13 from 1997, and 3 from 1998. The isolates from pigs were distributed as follows: 3 from
1995, 11 from 1996, 12 from 1997, and 9 from 1998. All isolates
from pigs were simultaneously resistant to glycopeptides,
erythromycin, and tetracycline, whereas 19 (56%) and 3 (9%) of the
isolates from broilers were resistant to erythromycin and tetracycline, respectively.
PCR detection of resistance genes.
All isolates were examined
for the presence of vanA, and all isolates resistant to
erythromycin and tetracycline were examined for the presence of
ermB and tet(M), respectively, using PCR as previously described (2, 5, 18).
PFGE.
DNA purification and enzyme digestion for PFGE analysis
of the isolates were performed as previously described (17).
All isolates were examined with SmaI as a restriction
enzyme. In addition, eight selected isolates (two from each year) from
pigs were examined with ApaI. Electrophoresis was performed
with a CHEF-DR III system (Bio-Rad Laboratories, Hercules, Calif.) and
1.2 or 1.4% SeaKem agarose in 0.5× Tris-borate-EDTA at 180 V. Running
conditions consisted of two phases used in sequence. Phase 1 was 2 to
8 s with a run time of 20 h. Phase 2 was 8 to 22 s with
a run time of 20 h.
Transferability of resistance.
Conjugation of vancomycin
resistance was performed with the eight isolates from pigs, which were
also examined with ApaI using the filter mating procedure as
described by Clewell et al. (13). E. faecium
BM4105RF, resistant to rifampin and fusidin, was used as a recipient.
Transconjugants were selected on Mueller-Hinton II agar plates
containing rifampin (50 µg/ml), fusidin (10 µg/ml), and vancomycin
(20 µg/ml). Conjugation of erythromycin and tetracycline resistance
was attempted with two isolates and erythromycin (20 µg/ml) and
tetracycline (10 µg/ml), respectively, instead of vancomycin.
Hybridization.
Digoxigenin-labeled DNA probes were prepared by
PCR amplification with primers for vanA, ermB,
and tet(M) and labeled with a Boehringer Mannheim
Biochemicals DNA labeling kit. Southern transfer and hybridization of
all PFGE profiles of the isolates from pigs were performed as
previously described (17) with the vanA,
ermB, and tet(M) probes. Southern transfer and
hybridization of the PFGE profiles of all transconjugants were also
performed with the ermB and vanA probes.
Plasmid profiling.
Plasmid profiling of the eight isolates
from pigs was performed with S1 nuclease as previously described
(9).
All isolates yielded positive PCR products for the vanA
gene. All 35 isolates from pigs and 17 (89%) of the 19 erythromycin-resistant isolates from broilers yielded positive PCR
products for the ermB gene. All isolates from pigs and the
three tetracycline-resistant isolates from broilers yielded positive
PCR products for the tet(M) gene.
All 34 GRE isolates from broilers belonged to different PFGE types
(more than three band differences), whereas all 35 isolates
from pigs
belonged to three closely related PFGE types, with up
to two band
differences to the most common type. Representative
types from broilers
are shown in Fig.
1, and the three
closely
related types from pigs are shown in Fig.
2. Twenty-eight isolates
from pigs
belonged to the most common type, 4 belonged to a closely
related type,
and the remaining 3 belonged to another closely
related type.
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FIG. 1.
Representative SmaI PFGE types observed among
glycopeptide-resistant E. faecium isolates from broilers in
Denmark.
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FIG. 2.
Representative SmaI PFGE types observed among
glycopeptide-resistant E. faecium isolates from pigs in
Denmark and transfer of glycopeptide resistance to E. faecium BM4105RF. Lanes 1 to 6, isolates from pigs; lane 7, E. faecium BM4105RF; lanes 8 to 13, glycopeptide-resistant
transformants of E. faecium BM4105RF corresponding to
isolates in lanes 1 to 6; lanes 1, 2, 4, and 6, the most common PFGE
type from pigs; lane 3, a closely related type, represented by four
isolates; lane 5, another closely related type, represented by three
isolates.
|
|
The
tet(M) probe hybridized to a
SmaI fragment of
approximately 135 kb in all pig isolates. The
vanA and
ermB probes hybridized
to the same
SmaI fragment
in all isolates from pigs; this fragment
was either approximately 135 or 160 kb. The
tet(M) probe hybridized
to an
ApaI
fragment of approximately 200 kb; however, the
vanA and
ermB probes did not hybridize to fragments with this
digest.
Transfer of vancomycin resistance from all eight porcine isolates was
achieved at a frequency of 0.75 × 10
5 to 12 × 10
5 (transconjugant/donor). Transfer of vancomycin
resistance was
followed in all cases by transfer of erythromycin
resistance,
but not resistance to tetracycline, and by transfer of the
relevant
SmaI fragment (Fig.
2). The
ermB and
vanA probes hybridized to
the transferred element in all
transconjugants. Transfer of tetracycline
resistance was not achieved,
whereas transfer of erythromycin
resistance from two isolates was
achieved at approximately the
same frequency as vancomycin resistance
and was followed by transfer
of vancomycin
resistance.
S1 nuclease digestion yielded a band of the same size as the
SmaI fragment to which the
vanA and
ermB probes
hybridized.
The present study showed that the occurrence of glycopeptide resistance
in the pig population in Denmark was caused by the
presence of a single
E. faecium clone, as indicated by closely
related PFGE
profiles, that was resistant to glycopeptides, erythromycin,
and
tetracycline. Among broilers, on the contrary, several different
clones
of GRE were found. Furthermore, among the porcine isolates,
the genes
encoding resistance to glycopeptides (
vanA) and erythromycin
(
ermB) were located on the same transferable DNA element,
probably
a plasmid, as indicated by S1 nuclease digestion. Large
plasmids
containing the
vanA gene have previously been
observed among GRE
(
28).
The linkage of resistance to macrolides and glycopeptides has also been
observed in other studies (
21,
25). Furthermore,
Noble et
al. (
23) cotransferred
vanA-mediated glycopeptide
resistance
from
E. faecium to
Staphylococcus
aureus using macrolides for
selection, and Bozdogan et al.
(
11) found the
vanA and
ermAM (synonymous with
ermB) genes to be present on the same
plasmid.
It can be speculated that the linkage of resistance genes can play an
important role in the coselection or persistence of
antimicrobial agent
resistance. However, only a very few epidemiological
data support such
a hypothesis. This investigation, together with
a previous study
(
8), provides evidence that
vanA-mediated
resistance to glycopeptides has persisted among
E. faecium
in
Danish pig herds because of genetic linkage to the
ermB
gene,
conferring resistance to macrolides on the same mobile DNA
elements,
most likely large plasmids. The persistence is most probably
due
to the continued use of tylosin, which was used in very large
amounts for growth promotion in Danish pig herds. The use of tylosin
for growth promotion decreased in Denmark during the end of 1998
and
was banned in all European Union countries from July 1999.
Thus, it is
expected that the occurrence of GRE among pigs will
decrease in the
future. If this happens, it will provide further
evidence for the
hypothesis of coselection being responsible for
the persistence of GRE
in pigs. However, since all GRE from pigs
belonged to the same clone,
another explanation could be that
this clone was especially successful
in establishing in and spreading
between pig herds in Denmark. This
clone was also resistant to
tetracycline, which has been widely used
for therapy for food
animals in Denmark (
4), and this usage
also could have contributed
to the successful persistence of this
clone.
The reason for the occurrence of multiple GRE clones among the broiler
population compared to the presence of only a single
clone among GRE
from the pig population is not known. It might
be due to differences in
production or feeding or having GRE introduced
several times in the
broiler population compared to the pig
population.
In conclusion, this study showed that GRE from broilers belonged to
different clones, while the isolates from pigs belonged
to a single
clone resistant to glycopeptides, macrolides, and
tetracycline. The
ermB and
vanA genes were located on the same
transferable DNA elements, most likely large plasmids. The persistence
of GRE in Danish pig herds was most likely a consequence of coselection
by the continued use of tylosin for growth
promotion.
| |
ACKNOWLEDGMENTS |
I thank Anja Dahl and René Hendriksen for technical assistance.
This study was supported by a grant from the Danish Directorate for
Development (98-3324).
| |
FOOTNOTES |
*
Mailing address: Danish Veterinary Laboratory,
Bülowsvej 27, DK-1790 Copenhagen, Denmark. Phone: 45 35 30 01 00. Fax: 45 35 30 01 20. E-mail: faa{at}svs.dk.
| |
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Journal of Clinical Microbiology, July 2000, p. 2774-2777, Vol. 38, No. 7
0095-1137/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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