Comparative study of vanA gene transfer from Enterococcus faecium to Enterococcus faecalis and to Enterococcus faecium in the intestine of mice
Nadège Bourgeois-Nicolaos
Laboratoire de Microbiologie, UFR des Sciences Pharmaceutiques et Biologiques, Université René Descartes, Paris, France
Search for more papers by this authorCarole Moubareck
Laboratoire de Microbiologie, UFR des Sciences Pharmaceutiques et Biologiques, Université René Descartes, Paris, France
Search for more papers by this authorNicole Mangeney
Laboratoire de Microbiologie, UFR des Sciences Pharmaceutiques et Biologiques, Université René Descartes, Paris, France
Search for more papers by this authorMarie-José Butel
Laboratoire de Microbiologie, UFR des Sciences Pharmaceutiques et Biologiques, Université René Descartes, Paris, France
Search for more papers by this authorFlorence Doucet-Populaire
Laboratoire de Microbiologie, UFR des Sciences Pharmaceutiques et Biologiques, Université René Descartes, Paris, France
Centre Hospitalier de Versailles, le Chesnay, France
Search for more papers by this authorNadège Bourgeois-Nicolaos
Laboratoire de Microbiologie, UFR des Sciences Pharmaceutiques et Biologiques, Université René Descartes, Paris, France
Search for more papers by this authorCarole Moubareck
Laboratoire de Microbiologie, UFR des Sciences Pharmaceutiques et Biologiques, Université René Descartes, Paris, France
Search for more papers by this authorNicole Mangeney
Laboratoire de Microbiologie, UFR des Sciences Pharmaceutiques et Biologiques, Université René Descartes, Paris, France
Search for more papers by this authorMarie-José Butel
Laboratoire de Microbiologie, UFR des Sciences Pharmaceutiques et Biologiques, Université René Descartes, Paris, France
Search for more papers by this authorFlorence Doucet-Populaire
Laboratoire de Microbiologie, UFR des Sciences Pharmaceutiques et Biologiques, Université René Descartes, Paris, France
Centre Hospitalier de Versailles, le Chesnay, France
Search for more papers by this authorEditor: Stefan Schwarz
Abstract
Vancomycin-resistant enterococci represent a large reservoir in animals because of the use of avoparcin as a growth promoter in Europe. These strains of animal origin enter the food chain and can either colonize the human gut or transfer their resistance genes to the human microbiota. In this study, we compared the transfer of vancomycin resistance from resistant animal Enterococcus faecium to sensitive human Enterococcus faecalis and E. faecium. We analysed these transfers in dibiotic mice and human faecal flora-associated mice. VanA transfer from animal E. faecium to human E. faecalis occurred in dibiotic mice. The transconjugants appeared rapidly and persisted at levels between 3.0 and 4.0 log10 colony-forming units g−1 of faeces. In human faecal flora-associated mice, vanA gene transfer was not detected towards E. faecalis but was possible between E. faecium strains. Our experiments revealed the possibility of vanA transfer from animal E. faecium to human E. faecalis in vitro and in vivo in the intestine of dibiotic mice. However, intraspecies transfer of vanA gene seems more common than interspecies transfer among enterococci.
References
- Aarestrup FM, Seyfarth AM, Emborg HD, Pedersen K, Hendriksen RS & Bager F (2001) Effect of abolishment of the use of antimicrobial agents for growth promotion on occurrence of antimicrobial resistance in fecal enterococci from food animals in Denmark. Antimicrob Agents Chemother 45: 2054 – 2059.
- Aarestrup FM, Hasman H, Jensen LB, Moreno M, Herrero IA, Dominguez L, Finn M & Franklin A (2002) Antimicrobial resistance among enterococci from pigs in three European countries. Appl Environ Microbiol 68: 4127 – 4129.
- Bager F, Madsen M, Christensen J & Aarestrup FM (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.
- van den Bogaard AE, Jensen LB & Stobberingh EE (1997) Vancomycin-resistant enterococci in turkeys and farmers. N Engl J Med 37: 1558 – 1559.
- van den Bogaard AE, Willems R, London N, Top J & Stobberingh EE (2002) Antibiotic resistance of faecal enterococci in poultry, poultry farmers and poultry slaughterers. J Antimicrob Chemother 49: 497 – 505.
- Chang S, Sievert DM, Hageman JC, et al. (2003) Infection with vancomycin-resistant Staphylococcus aureus containing the vanA resistance gene. N Engl J Med 348: 1342 – 1347.
- Descheemaeker PR, Chapelle S, Devriese LA, Butaye P, Vandamme P & Goossens H (1999) Comparison of glycopeptide-resistant Enterococcus faecium isolates and glycopeptide resistance genes of human and animal origins. Antimicrob Agents Chemother 43: 2032 – 2037.
- Doucet-Populaire F, Trieu-Cuot P, Andremont A & Courvalin P (1992) Conjugal transfer of plasmid DNA from Enterococcus faecalis to Escherichia coli in digestive tracts of gnotobiotic mice. Antimicrob Agents Chemother 36: 502 – 504.
- Dubos MO, Bourgeois-Nicolaos N, Depardieu F, Courvalin P & Doucet-Populaire F (2004) Evaluation of the GenoType Enterococcus assay for identification of enterococci at the species level and detection of van genes. Int J Antimicrob Agents 24: S192.
- Dutka-Malen S, Evers S & Courvalin P (1995) Detection of glycopeptide resistance genotypes and identification to the species level of clinical relevant enterococci by PCR. J Clin Microbiol 33: 24 – 27.
- Duval-Iflah Y, Raibaud P, Tancrède C & Rousseau M (1980) R plasmid transfer from Serratia liquifaciens to Escherichia coliin vitro and in vivo in the digestive tract of gnotobiotic mice associated with human fecal flora. Infect Immun 28: 981 – 990.
- Freter R, Brickner H, Fekete J, Vickerman MM & Carey KE (1983) Survival and implantation of Escherichia coli in the intestinal tract. Infect Immun 39: 686 – 703.
- Gambarotto K, Ploy MC, Turlure P, Grelaud C, Martin C, Bordessoule D & Denis F (2000) Prevalence of vancomycin-resistant enterococci in fecal samples from hospitalized patients and non hospitalized controls in a cattle-rearing area of France. J Clin Microbiol 38: 620 – 624.
- Gambarotto K, Ploy MC, Dupron F, Giangiobbe M & Denis F (2001) Occurrence of vancomycin-resistant enterococci in pork and poultry products from a cattle-rearing area of France. J Clin Microbiol 39: 2354 – 2355.
- Garrigues-Jeanjean N, Wittmer A, Ouriet MF & Duval-Iflah Y (1999) Transfer of the shuttle vector prri207 between Escherichia coli and Bacteroides spp. in vitro and in vivo in the digestive tract of axenic mice and in gnotoxenic mice inoculated with a human microflora. FEMS Microbiol Ecol 29: 33 – 43.
- Guardabassi L & Dalsgaard A (2004) Occurrence, structure, and mobility of Tn1546-like elements in environmental isolates of vancomycin-resistant enterococci. Appl Environ Microbiol 70: 984 – 990.
- Guardabassi L, Schwarz S & Lloyd DH (2004) Pet animals as reservoirs of antimicrobial-resistant bacteria: review. J Antimicrob Chemother 54: 321 – 332.
- Harbarth S, Cosgrove S & Carmeli Y (2002) Effects of antibiotics on nosocomial epidemiology of vancomycin resistant enterococci. Antimicrob Agents Chemother 46: 1619 – 1628.
- Huycke MM, Sahm DF & Gilmore MS (1998) Multiple-drug resistant enterococci: the nature of the problem and an agenda for the future. Emerg Infect Dis 4: 239 – 249.
- Jacob AE & Hobbs S (1974) Conjugal transfer of plasmid-borne multiple antibiotic resistance in Streptococcus faecalis var. Zymogenes. J Bacteriol 117: 360 – 372.
- Jacobsen BL, Skou M, Hammerum AM & Jensen LB (1999) Horizontal transfer of the satA gene encoding streptogramin A resistance between isogenic Enterococcus faecium strains in the gastrointestinal tract of gnotobiotic rats. Microb Ecol Health Dis 11: 241 – 247.
- Jaureguy F, Carton M, Panel P, Foucaud P, Butel MJ & Doucet-Populaire F (2004) Effects of intrapartum penicillin prophylaxis on intestinal bacterial colonization in infants. J Clin Microbiol 42: 5184 – 5188.
- Jensen LB, Ahrens P, Dons L, Jones RN, Hammerum AM & Aarestrup FM (1998) Molecular analysis of Tn1546 in Enterococcus faecium isolated from animals and humans. J Clin Microbiol 36: 437 – 442.
- Johnsen PJ, Simonsen GS, Olsvik O, Midtvedt T & Sundsfjord A (2002) Stability, persistence, and evolution of plasmid-encoded VanA glycopeptide resistance in enterococci in the absence of antibiotic selection in vitro and in gnotobiotic mice. Microb Drug Resist 8: 161 – 170.
- Johnsen PJ, Osterhus JI, Sletvold H, Sorum M, Kruse H, Nielsen K, Simonsen GS & Sundsfjord A (2005) 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 71: 159 – 168.
- Leclercq R, Deriot E, Weber M, Duval J & Courvalin P (1989) Transferable vancomycin and teicoplanin resistance in Enterococcus faecium. Antimicrob Agents Chemother 33: 10 – 15.
- Lester CH, Frimodt-Moller N & Hammerum AM (2004) Conjugal transfer of aminoglycoside and macrolide resistance between Enterococcus faecium isolates in the intestine of streptomycin-treated mice. FEMS Microbiol Lett 235: 385 – 391.
- Licht TR, Laugesen D, Jensen LB & Jacobsen BL (2002) Transfer of the pheromone-inducible plasmid pcf10 among Enterococcus faecalis microorganisms colonizing the intestine of mini-pigs. Appl Environ Microbiol 68: 187 – 193.
- Manson JM, Keis S, Smith JMB & Cook GM (2003) A clonal lineage of VanA-type Enterococcus faecalis predominates in vancomycin-resistant enterococci isolated in New Zealand. Antimicrob Agents Chemother 47: 204 – 210.
- 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.
- Murray BE, Singh KV, Heath JD, Sharma BR & Weinstock GM (1990) Comparison of genomic DNAs of different enterococcal isolates using restriction endonucleases with infrequent recognition sites. J Clin Microbiol 28: 2059 – 2063.
- Noble WC, Virani Z & Cree RG (1992) Co-transfer of vancomycin and other resistance genes from Enterococcus faecalis NCTC12201 to Staphylococcus aureus. FEMS Microbiol Lett 20: 91 – 98.
- Oprea SF, Zaidi N, Donabedian SM, Balasubramaniam M, Hershberger E & Zervos MJ (2004) Molecular and clinical epidemiology of vancomycin-resistant Enterococcus faecalis. J Antimicrob Chemother 53: 626 – 630.
- Ray AJ, Pultz NJ, Bhalla A, Aron DC & Donskey CJ (2003) Coexistence of vancomycin-resistant enterococci and Staphylococcus aureus in the intestinal tracts of hospitalized patients. Clin Infect Dis 37: 875 – 881.
- Sorensen TL, Blom M, Monnet DL, Frimodt-Moller N, Poulsen RL & Espersen F (2001) Transient intestinal carriage after ingestion of antibiotic-resistant Enterococcus faecium from chicken and pork. N Engl J Med 345: 1161 – 1166.
- Stobberingh E, van den Bogaard AE, London N, Driessen C, Top J & Willems R (1999) Enterococci with glycopeptide resistance in turkeys, turkey farmers, turkey slaughterers and (sub) urban residents in the south of the Netherlands: evidence for transmission of vancomycin resistance from animals to humans? Antimicrob Agents Chemother 43: 2215 – 2221.
- van der Waij D, Berghuis-De Vries JM & Lekkerkerk-van der Wees JEC (1971) Colonization resistance of the digestive tract in conventional and antibiotic-treated animals. J Hyg 69: 678 – 688.
- Werner G, Klare I & Witte W (1997) Arrangement of the vanA gene cluster in enterococci of different ecological origin. FEMS Microbiol Lett 155: 55 – 61.
- Willems RJ, Top J, van den Braak N, van Belkum A, Mevius DJ, Hendriks G, Santen-Verheuvel M & van Embden JD (1999) Molecular diversity and evolutionary relationships of Tn1546-like elements in enterococci from humans and animals. Antimicrob Agents Chemother 43: 483 – 491.