Previous Article | Next Article 
Journal of Clinical Microbiology, June 2001, p. 2354-2355, Vol. 39, No. 6
Department of Microbiology and Virology,
Limoges University Teaching Hospital,1 and
Environmental and Veterinary Health Research
Laboratory,2 Limoges, France
Received 25 September 2000/Returned for modification 21 January
2001/Accepted 8 April 2001
Meat products were collected from public retail outlets and tested
for the presence of vancomycin-resistant enterococci (VRE) in an area
with a high prevalence of VRE reported in human fecal samples. VRE were
detected in 66% of the samples, and a predominance of VanC strains was
found, which is also true for human fecal samples.
In a previous study we reported the
high prevalence of vancomycin-resistant enterococci (VRE) in fecal
samples from hospitalized (37%) and healthy nonhospitalized (11.8%)
subjects living in the same local community (6). We found
a predominance of Enterococcus gallinarum VanC strains
(70.7%), together with 10.8% E. casseliflavus VanC strains
and 18.5% E. faecium VanA strains, without any detectable VanB strains. A partial explanation for such high VRE prevalence was
the use of a sensitive test with an enrichment broth step. Nevertheless, it was also suspected that the high levels might be
related to the fact that subjects and patients were recruited from a
predominantly agricultural area where avoparcin had been used as a
growth promoter in animal husbandry. Assuming therefore that the food
chain might be a likely source of VRE contamination in humans
(1-3, 8, 9, 12), we investigated the occurrence of VRE in
meat collected from local retail outlets.
During a 2-month period, between May and June 1999, 59 meat samples (50 pork and 9 poultry samples) were collected from butchers' shops,
supermarkets, and other retail and wholesale outlets by environmental
and veterinary health research laboratory staff. Approximately 25 g of each piece of meat was placed in 250 ml of buffered peptone water
(bioMérieux, La Balme les Grottes, France) and homogenized
with a "stomacher" (Waring blender; Poly Labo, Strasbourg, France).
After incubation at 37°C for 24 h, 0.1 ml of the diluted sample
was inoculated onto bile-esculin agar plates with and without 6 mg of
vancomycin per liter and into bile-esculin broth supplemented with 4 mg
of vancomycin per liter. Plates and broths were incubated at 37°C for
24 h. All esculin-positive broth cultures were subcultured onto
bile-esculin agar plates with and without 6 mg of vancomycin per liter.
Species identification of enterococci, susceptibility testing, and
determination of glycopeptide resistance genotypes were performed as
previously described (6). E. faecium strains
with a vanA genotype were typed by pulsed-field gel
electrophoresis (PFGE) as previously described (6) and
compared with E. faecium vanA strains of human origin
isolated in our previous study (6).
We found high VRE contamination of the locally produced meat products,
with 39 of the 59 samples (66%) being contaminated with VRE (9 poultry
samples [9 of 9] and 30 pork samples [30 of 50; 60%]). This
parallels the high prevalence of human VRE fecal colonization recorded
in our previous study (6). Other European studies have
observed VRE contamination in meat, from 8.3% of meat samples in
Germany (10) to 79% of poultry samples in The Netherlands
(14). Comparison of different data is hindered because the
samples studied and detection methods vary considerably. However, all
studies show the existence of a considerable pool of VRE in foods of
animal origin (4, 10, 11, 14, 15). To our knowledge, only
two studies are similar to our own, having effected a survey of human
VRE fecal colonization and of VRE contamination in meat available at
the retail level in one discrete geographical area (11,
14). One of these studies (carried out in The Netherlands) unexpectedly found a higher prevalence of VRE in poultry products (79%) (14) than in the fecal carriage of both
hospitalized patients and patients living in the community (only 2%)
(5). The other study (carried out in France) found a high
VRE colonization rate both in humans (17%) (7) and in
meat samples (41%) (11), though the levels recorded were
lower than those found in our study.
Forty-nine VRE strains were isolated, 5 E. faecium strains
(10.2%) with a vanA genotype, 1 E. durans strain
with a vanA genotype, 29 E. gallinarum strains
(59.2%) with a vanC1 genotype, and 14 E. casseliflavus strains (28.6%) with a vanC2 genotype.
No E. faecalis strains and no strains with a vanB
or vanD genotype were detected. All but two E. faecium strains were only isolated after broth enrichment. All
vanA genotype strains were isolated from pork samples (Table
1). Poultry samples were all positive for VRE but only contained vanC1 and vanC2 genotype
strains.
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.6.2354-2355.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Occurrence of Vancomycin-Resistant Enterococci in
Pork and Poultry Products from a Cattle-Rearing Area of
France
ABSTRACT
Top
Abstract
Text
References
TEXT
Top
Abstract
Text
References
TABLE 1.
VRE strain and genotype distribution in different meat
products
As in the human study (6), there was a predominance of VanC isolates and no E. faecalis strains were detected. This species distribution differs from that reported in other studies in which E. faecium and E. faecalis strains normally outnumber other species (4, 10-14). The proportion of E. gallinarum strains that we isolated is higher than that reported even by other studies using enrichment methods (10, 12, 14). In both the French (7) and Dutch (14) studies, E. faecium occurred as the principal species in human as well as meat samples.
The PFGE patterns of E. faecium vanA isolates from animal
foodstuffs are presented in Fig. 1.
Nonhuman isolates generated heterogenous PFGE patterns that were
different from those obtained with human isolates in our previous study
(6). It was not possible in our study to demonstrate a
link between vanA E. faecium strains of human and animal
origins.
|
The high VRE contamination level described in this study confirms our predictions since avoparcin had been employed by meat producers in the local area. As suggested in a previous study (6), the high VRE contamination observed in meat samples might explain the high prevalence of VRE colonization in humans, particularly since enterococcus species distribution is comparable in both studies. However, no link was observed for E. faecium vanA strains. Further analysis of E. gallinarum and E. casseliflavus strains by PFGE and analysis of transposons encoding high-level glycopeptide resistance of vanA strains might be able to shed light on possible links between human and animal VRE strains.
| |
FOOTNOTES |
|---|
* Corresponding author. Mailing address: Laboratoire de Bactériologie-Virologie-Hygiène, 2 av Martin Luther King, 87000 Limoges, France. Phone: (33) 555-05-61-66. Fax: (33) 555-05-67-22. E-mail: fdenis{at}unilim.fr.
| |
REFERENCES |
|---|
|
Top
Abstract
Text
References
|
|---|
| 1. | Aarestrup, F. M. 1995. Occurrence of glycopeptide resistance among Enterococcus faecium isolates from conventional and ecological poultry farms. Microb. Drug Resist. 1:255-257[Medline]. |
| 2. | Bager, F., M. Madsen, J. Christensen, and F. M. Aarestrup. 1997. Avoparcin used as a growth promoter is associated with the occurrence of vancomycin-resistant Enterococcus faecium on Danish poultry and pig farms. Prev. Vet. Med. 31:95-112[CrossRef][Medline]. |
| 3. |
Bates, J.,
J. Z. Jordens, and D. T. Griffiths.
1994.
Farm animals as a putative reservoir for vancomycin-resistant enterococcal infection in man.
J. Antimicrob. Chemother.
34:507-516 |
| 4. |
Chadwick, P. R.,
N. Woodford,
E. B. Kaczmarski,
S. Gray,
R. A. Barrell, and B. A. Oppenheim.
1996.
Glycopeptide-resistant enterococci isolated from uncooked meat.
J. Antimicrob. Chemother.
38:908-909 |
| 5. | Endtz, H. P., N. van den Braak, A. Van Belkum, J. A. J. W. Kluytmans, J. G. M. Koeleman, L. Spanjaard, A. Voss, A. J. L. Weersink, C. M. J. E. Vandenbroucke-Grauls, A. G. M. Buiting, A. Van Duin, and H. A. Verbrugh. 1997. Fecal carriage of vancomycin-resistant enterococci in hospitalized patients and those living in the community in The Netherlands. J. Clin. Microbiol. 35:3026-3031[Abstract]. |
| 6. |
Gambarotto, K.,
M. C. Ploy,
P. Turlure,
C. Grélaud,
C. Martin,
D. Bordessoule, and F. Denis.
2000.
Prevalence of vancomycin-resistant enterococci in fecal samples from hospitalized patients and nonhospitalized controls in a cattle-rearing area of France.
J. Clin. Microbiol.
38:620-624 |
| 7. | Guerin, F., J. D. Perrier-Gros-Claude, V. Foissaud, T. Masseron, and J. Thierry. 1998. Entérocoques résistants à la vancomycine en France. Presse Med. 27:1427-1429. |
| 8. | Klare, I., H. Heier, H. Claus, G. Böhme, S. Marin, G. Seltmann, R. Hakenbeck, V. Antanassova, and W. Witte. 1995. Enterococcus faecium strains with vanA-mediated high-level glycopeptide resistance isolated from animal foodstuffs and fecal samples of humans in the community. Microb. Drug Resist. 1:265-272[Medline]. |
| 9. | Klare, I., H. Heier, H. Claus, R. Reissbrodt, and W. Witte. 1995. vanA-mediated high-level glycopeptide resistance in Enterococcus faecium from animal husbandry. FEMS Microbiol. Lett. 125:165-172[CrossRef][Medline]. |
| 10. |
Klein, G.,
A. Pack, and G. Reuter.
1998.
Antibiotic resistance patterns of enterococci and occurrence of vancomycin-resistant enterococci in raw minced beef and pork in Germany.
Appl. Environ. Microbiol.
64:1825-1830 |
| 11. | Perrier-Gros-Claude, J. D., P. L. Courrier, J. M. Bréard, J. L. Vignot, T. Masseront, D. Garin, J. Thierry, and E. Garrabé. 1998. Entérocoques résistants aux glycopeptides dans les viandes. BEH no. 12/98. |
| 12. | Quednau, M., S. Ahrné, A. C. Petersson, and G. Molin. 1998. Antibiotic-resistant strains of Enterococcus isolated from Swedish and Danish retailed chicken and pork. J. Appl. Microbiol. 84:1163-1170[CrossRef][Medline]. |
| 13. | Turtura, G. C., and P. Lorenzelli. 1994. Gram-positive cocci isolated from slaughtered poultry. Microbiol. Res. 149:203-213[Medline]. |
| 14. |
Van Den Braak, N.,
A. Van Belkum,
M. Van Keulen,
J. Vliegenthart,
H. A. Verbrugh, and H. P. Endtz.
1998.
Molecular characterization of vancomycin-resistant enterococci from hospitalized patients and poultry products in The Netherlands.
J. Clin. Microbiol.
36:1927-1932 |
| 15. | Wegener, H. C., M. Madsen, N. Nielsen, and F. M. Aarestrup. 1997. Isolation of vancomycin resistant Enterococcus faecium from food. Int. J. Food Microbiol. 35:57-66[CrossRef][Medline]. |
Journal of Clinical Microbiology, June 2001, p. 2354-2355, Vol. 39, No. 6
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.6.2354-2355.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Dufour, M., Manson, J. M., Bremer, P. J., Dufour, J.-P., Cook, G. M., Simmonds, R. S.
(2007). Characterization of Monolaurin Resistance in Enterococcus faecalis. Appl. Environ. Microbiol.
73: 5507-5515
[Abstract] [Full Text] -
Garnier, F., Gambarotto, K., Denis, F., Ploy, M.-C.
(2004). Molecular study of vancomycin-resistant enterococci isolated from humans and from food in a cattle-rearing area of France. J Antimicrob Chemother
54: 236-239
[Abstract] [Full Text] -
Moubareck, C., Bourgeois, N., Courvalin, P., Doucet-Populaire, F.
(2003). Multiple Antibiotic Resistance Gene Transfer from Animal to Human Enterococci in the Digestive Tract of Gnotobiotic Mice. Antimicrob. Agents Chemother.
47: 2993-2996
[Abstract] [Full Text] -
Manson, J. M., Keis, S., Smith, J. M. B., Cook, G. M.
(2003). Characterization of a Vancomycin-Resistant Enterococcus faecalis (VREF) Isolate from a Dog with Mastitis: Further Evidence of a Clonal Lineage of VREF in New Zealand. J. Clin. Microbiol.
41: 3331-3333
[Abstract] [Full Text] -
Manson, J. M., Keis, S., Smith, J. M. B., Cook, G. M.
(2003). A Clonal Lineage of VanA-Type Enterococcus faecalis Predominates in Vancomycin-Resistant Enterococci Isolated in New Zealand. Antimicrob. Agents Chemother.
47: 204-210
[Abstract] [Full Text]
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Copyright © 2009 by the American Society for Microbiology. For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»