Antibiotic resistance and virulence of faecal enterococci isolated from food-producing animals in Tunisia

Autor: Klibi, N.; Aouini, R.; Borgo, F.; Ben Said, L.; Ferrario, C.; Dziri, R.; Boudabous, A.; Torres Manrique, Carmen; Ben Slama, K.; 

Tipo de documento: Artículo de revista

Revista: Annals of Microbiology. ISSN: 1590-4261. Año: 2015. Número: 2. Volumen: 65. Páginas: 695-702.

Texto completo open access 

JCR (datos correspondientes al año 2014):
Science  Área: BIOTECHNOLOGY & APPLIED MICROBIOLOGY  Quartil: Q4  Lugar área: 129/162  F. impacto: 0,990 
Science  Área: MICROBIOLOGY  Quartil: Q4  Lugar área: 129/162  F. impacto: 0,990 

SCIMAGO (datos correspondientes al año 2014):
,388  SNIP: ,72 



  • Aarestrup, F.M., Agerso, Y., Gerner-Smidt, P., Madsen, M., Jensen, L., Comparison of antimicrobial resistance phenotypes and resistance genes in Enterococcus faecalis and Enterococcus faecium from humans in the community, broilers, and pigs in Denmark (2000) Diagn Microbiol Infect Dis, 37, pp. 127-137. , COI: 1:CAS:528:DC%2BD3cXktV2qsLo%3D, PID: 10863107
  • Aarestrup, F.M., Butaye, P., Witte, W., Non human reservoirs of enterococci. In The Enterococci : Pathogenesis, Molecular Biology and antibiotic Resistance, ed. Washington, ASM Press, pp (2002) 55–99
  • Arias, C.A., Robredo, B., Singh, K.V., Torres, C., Panesso, D., Murray, B.E., Rapid identification of Enterococcus hirae and Enterococcus durans by PCR and detection of a homologue of the E. hirae mur-2 gene in E. durans (2006) J Clin Microbiol, 44, pp. 1567-1570. , COI: 1:CAS:528:DC%2BD28XkvVamur4%3D, PID: 16597896
  • Arias, C.A., Murray, B.E., Emergence and management of drug-resistant enterococcal infections (2008) Expert Rev Anti Infect Ther, 6, pp. 637-655. , COI: 1:CAS:528:DC%2BD1cXht1Glu7vJ, PID: 18847403
  • Borgo, F., Ferrario, C., Ricci, G., Fortina, M.G., Genotypic intraspecies heterogeneity of Enterococcus italicus: data from dairy environments (2013) J Basic Microbiol, 53, pp. 20-28. , COI: 1:CAS:528:DC%2BC3sXht1Cntr8%3D, PID: 22581461
  • Butaye, P., Devriese, L.A., Haesebrouck, F., Differences in antibiotic resistance patterns of Enterococcus faecalis and Enterococcus faecium strains isolated from farm and pet animals (2001) Antimicrob Agents Chemother, 45, pp. 1374-1378. , COI: 1:CAS:528:DC%2BD3MXjtF2hu7w%3D, PID: 11302798
  • Byappanahalli, M.N., Nevers, M.B., Korajkic, A., Staley, Z.R., Harwood, V.J., Enterococci in the environment (2012) Microbiol Mol Biol Rev, 76, pp. 685-706. , COI: 1:CAS:528:DC%2BC3sXhsVOjt7c%3D, PID: 23204362
  • Clementi, F., Aquilanti, L., Recent investigations and updated criteria for the assessment of antibiotic resistance in food lactic acid bacteria (2011) Anaerobe, 17, pp. 394-398. , COI: 1:CAS:528:DC%2BC38XhtlSntw%3D%3D, PID: 21515393
  • Performance Standards for antimicrobial Susceptibility Testing
  • Twenty-Second Informational Supplement (2012) CLSI document, pp. 100-122. , Wayne, PA: Clinical and Laboratory Standards Institute
  • Colombo, F., Borgo, F., Fortina, M.G., Genotypic characterization of non starter lactic acid bacteria involved in the ripening of artisanal Bitto PDO cheese (2009) J Basic Microbiol, 49, pp. 521-530. , COI: 1:CAS:528:DC%2BC3cXht1Ohu7s%3D, PID: 19810037
  • CA-SFM: Comité de l’Antibiogramme de la Société Française de Microbiologie (2010). Edition de Janvier 2010. 49 pagesDe Leener, E.D., Decostere, A., De Graef, E.M., Moyaert, H., Haesebrouck, F., Presence and mechanism of antimicrobial resistance among enterococci from cats and dogs (2005) Microb Drug Resist, 11, pp. 395-403. , PID: 16359201
  • Del Campo, R., Ruiz-Garbajosa, P., Sanchez-Moreno, M.P., Baquero, F., Torres, C., Canton, R., Coque, T.M., Antimicrobial resistance in recent fecal enterococci from healthy volunteers and food handlers in Spain: genes and phenotypes (2003) Microb Drug Resist, 9, pp. 47-60. , PID: 12705683
  • De Urraza, P.J., Gomez-Zavaglia, A., Lozano, M.E., Romanowski, V., De Antoni, G.L., DNA fingerprinting of thermophilic lactic acid bacteria using repetitive sequence-based polymerase chain reaction (2000) J Dairy Res, 67, pp. 381-392. , PID: 11037234
  • Fisher, K., Phillips, C., The ecology, epidemiology and virulence of Enterococcus (2009) Microbiology, 155, pp. 1749-1757. , COI: 1:CAS:528:DC%2BD1MXotVaqsL8%3D, PID: 19383684
  • Galkiewicz, J.P., Kellogg, C.A., Cross-kingdom amplification using bacteria-specific primers: complications for studies of coral microbial ecology (2008) Appl Environ Microbiol, 74, pp. 7828-7831. , COI: 1:CAS:528:DC%2BD1MXnvVeh, PID: 18931299
  • Guardabassi, L., Schwarz, S., Lloyd, D.H., Pet animals as reservoirs of antimicrobial-resistant bacteria (2004) J Antimicrob Chemother, 54, pp. 321-332. , COI: 1:CAS:528:DC%2BD2cXnt1Wis7g%3D, PID: 15254022
  • Hammerum, A.M., Enterococci of animal origin and their significance for public health (2012) Clin Microbiol Infect, 18, pp. 619-625. , COI: 1:CAS:528:DC%2BC38XhtFOhtrzP, PID: 22487203
  • Hwang, I.Y., Suk, K.L., Hyun, O.K., Choi, K.P., Suk, C.J., Yong, H.P., Hyang, M.N., Occurrence of virulence determinants in fecal Enterococcus faecalis isolated from pigs and chickens in Korea (2011) J Microbiol Biotechnol, 21, pp. 1352-1355. , COI: 1:CAS:528:DC%2BC38XhvFOktbw%3D, PID: 22210624
  • Jackson, C.R., Fedorka-Cray, P.G., Barrett, J.B., Use of a genus- and species-specific multiplex PCR for identification of enterococci (2004) J Clin Microbiol, 42, pp. 3558-3565. , COI: 1:CAS:528:DC%2BD2cXnt1Ogt70%3D, PID: 15297497
  • Jackson, C.R., Lombard, J.E., Dargatz, D.A., Fedorka-Cray, P.J., Prevalence, species distribution and antimicrobial resistance of enterococci isolated from US dairy cattle (2010) Lett Appl Microbiol, 52, pp. 41-48. , PID: 21114506
  • Klare, I., Konstabel, C., Mueller-Bertling, S., Werner, G., Strommenger, B., Kettlitz, C., Borgmann, S., Witte, W., Spread of ampicillin/vancomycin-resistant Enterococcus faecium of the epidemic-virulent clonal complex-17 carrying the genes esp and hyl in German hospitals (2005) Eur J Clin Microbiol Infect Dis, 24, pp. 815-825. , COI: 1:STN:280:DC%2BD28%2FgsV2itQ%3D%3D, PID: 16374593
  • Klibi, N., Ben Slama, K., Sáenz, Y., Masmoudi, A., Zanetti, S., Sechi, L.A., Boudabous, A., Torres, C., Detection of virulence factors in high-level gentamicin-resistant Enterococcus faecalis and Enterococcus faecium isolates from a Tunisian hospital (2007) Can J Microbiol, 53, pp. 372-379. , COI: 1:CAS:528:DC%2BD2sXntV2msrw%3D, PID: 17538646
  • Klibi, N., Ben Slimen, N., Fhoula, I., López, M., Ben Slama, K., Daffonchio, D., Boudabous, A., Ouzari, H., Genotypic diversity, antibiotic resistance and bacteriocin production of enterococci isolated from rhizospheres (2012) Microbes Environ, 27, pp. 533-537. , PID: 23124764
  • Klibi, N., Said, L.B., Jouini, A., Slama, K.B., López, M., Sallem, R.B., Boudabous, A., Torres, C., Species distribution, antibiotic resistance and virulence traits in enterococci from meat in Tunisia (2013) Meat Sci, 93, pp. 675-680. , COI: 1:CAS:528:DC%2BC3sXhvVSrtw%3D%3D, PID: 23273480
  • Kojima, A., Morioka, A., Kijima, M., Ishihara, K., Fujisawa, T., Tamura, Y., Takahashi, T., Classification and antimicrobial susceptibilities of Enterococcus species isolated from apparently healthy food-producing animals in Japan (2010) Zoonoses Public Health, 57, pp. 137-141. , COI: 1:CAS:528:DC%2BC3cXjvFyrsLY%3D, PID: 19243566
  • Kuhn, I., Iverson, A., Burman, L.G., Ollsson-Liljequist, B., Franklin, A., Finn, M., Aarestrup, F., Möllby, R., Comparison of enterococcal populations in animals, humans, and the environment European study (2003) Int J Food Microbiol, 88, pp. 133-145. , PID: 14596986
  • Lebreton, F., Van Schaik, W., McGuire, A.M., Godfrey, P., Griggs, A., Mazumdar, V., Corander, J., Gilmore, M.S., Emergence of epidemic multidrug-resistant Enterococcus faecium from animal and commensal strains (2013) MBio, 4, 10p
  • Muller, T., Ulrich, A., Ott, E.M., Muller, M., Identification of plant-associated enterococci (2001) J Appl Microbiol, 91, pp. 268-278. , COI: 1:CAS:528:DC%2BD3MXmtlWltbc%3D, PID: 11473591
  • Murray, B.E., The life and times of the Enterococcus (1990) Clin Microbiol Rev, 3, pp. 46-65. , COI: 1:STN:280:DyaK3c7isVWktQ%3D%3D, PID: 2404568
  • Murray, B.E., Diversity among multidrug-resistant enterococci (1998) Emerg Infect Dis, 4, pp. 37-47. , COI: 1:CAS:528:DyaK1cXhsVGkurg%3D, PID: 9452397
  • Nakayama, J., Kariyama, R., Kumon, H., Description of a 23.9-kilobase chromosomal deletion containing a region encoding fsr genes which mainly determines the gelatinase-negative phenotype of clinical isolates of Enterococcus faecalis in urine (2002) Appl Environ Microbiol, 68, pp. 3152-3155. , COI: 1:CAS:528:DC%2BD38XksVWqtbo%3D, PID: 12039782
  • Nilsson, O., Vancomycin resistant enterococci in farm animals—occurrence and importance (2012) Infect Ecol Epidemiol, 2, 8p
  • Olsen, R.H., Schonheyder, H.C., Christensen, H., Bigaard, M., Enterococcus faecalis of human and poultry origin share virulence genes supporting the zoonotic potential of E. faecalis (2012) Zoonoses Public Health, 59, pp. 256-263. , COI: 1:STN:280:DC%2BC38zotFSnug%3D%3D, PID: 22122842
  • Poeta, P., Costa, D., Saenz, Y., Klibi, N., Ruiz-Larrea, F., Rodrigues, J., Torres, C., Characterization of antibiotic resistance genes and virulence factors in faecal enterococci of wild animals in Portugal (2005) J Vet Med B Infect Dis Vet Public Health, 52, pp. 396-402. , COI: 1:CAS:528:DC%2BD28Xit1GltQ%3D%3D, PID: 16283919
  • Poeta, P., Costa, D., Klibi, N., Rodrigues, J., Torres, C., Phenotypic and genotypic study of gelatinase and beta-haemolysis activities in faecal enterococci of poultry in Portugal (2006) J Vet Med B : Infect Dis Vet Public Health, 53, pp. 203-208. , COI: 1:CAS:528:DC%2BD28XmsFyqt7s%3D
  • Santos, T., Silva, N., Igrejas, G., Ridrigues, P., Micael, J., Rodrigues, T., Resendes, R., Poeta, P., Dissemination of antibiotic resistant Enterococcus spp. and Escherichia coli from wild birds of Azores Archipalago (2013) Anaerobe, 24, pp. 25-31. , COI: 1:CAS:528:DC%2BC3sXitVWjtLrE, PID: 24047647
  • Schmitz, F.J., Sadurski, R., Kray, A., Boos, M., Geisel, R., Köhrer, K., Verhoef, J., Fluit, A.C., Prevalence of macrolide-resistance genes in Staphylococcus aureus and Enterococcus faecium isolates from 24 European university hospitals (2000) J Antimicrob Chemother, 45, pp. 891-894. , COI: 1:CAS:528:DC%2BD3cXkt1arsLc%3D, PID: 10837446
  • Silva, N., Igrejas, G., Gonçalves, A., Poeta, P., Commensal gut bacteria: distribution of Enterococcus species and prevalence of E. coli phylogenetic groups in animals and humans in Portugal (2012) Ann Microbiol, 62, pp. 449-459
  • Stovcik, V., Javorsky, P., Pristas, P., Antibiotic resistance patterns and resistance genes in enterococci isolated from sheep gastrointestinal tract in Slovakia (2008) Bull Vet Inst Pulawy, 52, pp. 53-57
  • Sutcliffe, J., Grebe, T., Tait-Kamradt, A., Wondrack, L., Detection of erythromycin-resistant determinants by PCR (1996) Antimicrob Agents Chemother, 40, pp. 2562-2566. , COI: 1:CAS:528:DyaK28Xms1Smsb8%3D, PID: 8913465
  • Svec, P., Vancanneyt, M., Seman, M., Snauwaert, C., Lefebvre, K., Sedlácek, I., Swings, J., Evaluation of (GTG)<
  • inf>
  • 5<
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  • -PCR for Identification of Enterococcus spp (2005) FEMS Microbiol Lett, 247, pp. 59-63. , COI: 1:CAS:528:DC%2BD2MXltVens7w%3D, PID: 15927748
  • Top, J., Willems, R., Bonten, M., Emergence of CC17 Enterococcus faecium: from commensal to hospital-adapted pathogen (2008) FEMS Immunol Med Microbiol, 52, pp. 287-308
  • Torres, C., Tenorio, C., Portillo, A., García, M., Martínez, C., Del Campo, R., Ruiz-Larrea, F., Zarazaga, M., Intestinal colonization by vanA-or vanB2 containing enterococcal isolates of healthy animals in Spain (2003) Microb Drug Resist, 9, pp. 47-52. , COI: 1:CAS:528:DC%2BD3sXhtVSqsrzO, PID: 14633367
  • Versalovic, J., Schneider, M., De Bruijin, F.J., Lupski, J.R., Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction (1994) Methods Mol Cell Biol, 5, pp. 25-40. , COI: 1:CAS:528:DyaK2MXhtVOmsLc%3D
  • Werner, G., Hammerum, A.M., Coque, T.M., Hope, R., Hryniewics, W., Johnson, A., Klare, I., Woodford, N., Emergence and spread of vancomycin resistance among enterococci in Europe (2008) Euro Surveill, 13, 11p