High prevalence of extended-spectrum and plasmidic AmpC beta-lactamase-producing Escherichia coli from poultry in Tunisia

Autor: Maamar, E.; Hammami, S.; Alonso, C.A.; Dakhli, N.; Abbassi, M.S.; Ferjani, S.; Hamzaoui, Z.; Saidani, M.; Torres Manrique, Carmen; Boutiba-Ben, Boubaker, I.; 

Tipo de documento: Artículo de revista

Revista: International Journal of Food Microbiology. ISSN: 0168-1605. Año: 2016. Volumen: 231. Páginas: 69-75.

JCR (datos correspondientes al año 2014):
Science  Área: FOOD SCIENCE & TECHNOLOGY  Quartil: Q1  Lugar área: 12/123  F. impacto: 3,082 
Science  Área: MICROBIOLOGY  Quartil: Q2  Lugar área: 12/123  F. impacto: 3,082 

SCIMAGO (datos correspondientes al año 2014):
1,334  SNIP: 1,606 



  • Ben Said, L., Jouini, A., Klibi, N., Dziri, R., Alonso, C.A., Boudabous, A., Ben Slama, K., Torres, C., Detection of extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae in vegetables, soil and water of the farm environment in Tunisia (2015) Int. J. Food Microbiol., 203, pp. 86-92
  • Ben Sallem, R., Ben Slama, K., Rojo-Bezares, B., Porres-Osante, N., Jouini, A., Klibi, N., Boudabous, A., Torres, C., IncI1 plasmids carrying bla(CTX-M-1) or bla(CMY-2) genes in Escherichia coli from healthy humans and animals in Tunisia (2014) Microb. Drug Resist., 20 (5), pp. 495-500
  • Ben Sallem, R., Ben Slama, K., Sáenz, Y., Rojo-Bezares, B., Estepa, V., Jouini, A., Gharsa, H., Torres, C., Prevalence and characterization of extended-spectrum beta-lactamase (ESBL)- and CMY-2-producing Escherichia coli isolates from healthy food-producing animals in Tunisia (2012) Foodborne Pathog. Dis., 9 (12), pp. 1137-1142
  • Ben Slama, K., Ben Sallem, R., Jouini, A., Rachid, S., Moussa, L., Sáenz, Y., Estepa, V., Torres, C., Diversity of genetic lineages among CTX-M-15- and CTX-M-14-producing Escherichia coli strains in a Tunisian hospital (2011) Curr. Microbiol., 62 (6), pp. 1794-1801
  • Ben Slama, K., Jouini, A., Ben Sallem, R., Somalo, S., Sáenz, Y., Estepa, V., Boudabous, A., Torres, C., Prevalence of broad-spectrum cephalosporin-resistant Escherichia coli isolates in food samples in Tunisia, and characterization of integrons and antimicrobial resistance mechanisms implicated (2010) Int. J. Food Microbiol., 137 (2-3), pp. 281-286
  • Brinas, L., Moreno, M.A., Zarazaga, M., Porrero, C., Sáenz, Y., Garcia, M., Dominguez, L., Torres, C., Detection of CMY-2, CTX-M-14, and SHV-12 beta-lactamases in Escherichia coli fecal-sample isolates from healthy chickens (2003) Antimicrob. Agents Chemother., 47 (6), pp. 2056-2058
  • Carattoli, A., Animal reservoirs for extended spectrum beta-lactamase producers (2008) Clin. Microbiol. Infect., 14, pp. 117-123
  • Carattoli, A., Resistance plasmid families in Enterobacteriaceae (2009) Antimicrob. Agents Chemother., 53 (6), pp. 2227-2238
  • Carattoli, A., Bertini, A., Villa, L., Falbo, V., Hopkins, K.L., Threlfall, E.J., Identification of plasmids by PCR-based replicon typing (2005) J. Microbiol. Methods, 63 (3), pp. 219-228
  • Carattoli, A., Lovari, S., Franco, A., Cordaro, G., Di Matteo, P., Battisti, A., Extended-spectrum beta-lactamases in Escherichia coli isolated from dogs and cats in Rome, Italy, from 2001 to 2003 (2005) Antimicrob. Agents Chemother., 49 (2), pp. 833-835
  • Cergole-Novella, M.C., Guth, B.E., Castanheira, M., Carmo, M.S., Pignatari, A.C., First description of bla(CTX-M-14)- and bla(CTX-M-15)-producing Escherichia coli isolates in Brazil (2010) Microb. Drug Resist., 16 (3), pp. 177-184
  • Clermont, O., Bonacorsi, S., Bingen, E., Rapid and simple determination of the Escherichia coli phylogenetic group (2000) Appl. Environ. Microbiol., 66 (10), pp. 4555-4558
  • Performance standards for antimicrobial susceptibility testing twenty-third informational supplement (2013) Vol. CLSI document M100-S23
  • Eckert, C., Gautier, V., Arlet, G., DNA sequence analysis of the genetic environment of various blaCTX-M genes (2006) J. Antimicrob. Chemother., 57 (1), pp. 14-23
  • Ewers, C., Li, G., Wilking, H., Kiessling, S., Alt, K., Antao, E.M., Laturnus, C., Wieler, L.H., Avian pathogenic, uropathogenic, and newborn meningitis-causing Escherichia coli: how closely related are they? (2007) Int. J. Med. Microbiol., 297 (3), pp. 163-176
  • Girlich, D., Poirel, L., Carattoli, A., Kempf, I., Lartigue, M.F., Bertini, A., Nordmann, P., Extended-spectrum beta-lactamase CTX-M-1 in Escherichia coli isolates from healthy poultry in France (2007) Appl. Environ. Microbiol., 73 (14), pp. 4681-4685
  • Grami, R., Mansour, W., Dahmen, S., Mehri, W., Haenni, M., Aouni, M., Madec, J.Y., The blaCTX-M-1 IncI1/ST3 plasmid is dominant in chickens and pets in Tunisia (2013) J. Antimicrob. Chemother., 68 (12), pp. 2950-2952
  • Horton, R.A., Randall, L.P., Snary, E.L., Cockrem, H., Lotz, S., Wearing, H., Duncan, D., Coldham, N.G., Fecal carriage and shedding density of CTX-M extended-spectrum [beta]-lactamase-producing Escherichia coli in cattle, chickens, and pigs: implications for environmental contamination and food production (2011) Appl. Environ. Microbiol., 77 (11), pp. 3715-3719
  • Huber, H., Zweifel, C., Wittenbrink, M.M., Stephan, R., ESBL-producing uropathogenic Escherichia coli isolated from dogs and cats in Switzerland (2013) Vet. Microbiol., 162 (2-4), pp. 992-996
  • Johnson, J.R., Stell, A.L., Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise (2000) J. Infect. Dis., 181 (1), pp. 261-272
  • Johnson, J.R., Kuskowski, M.A., Owens, K., Gajewski, A., Winokur, P.L., Phylogenetic origin and virulence genotype in relation to resistance to fluoroquinolones and/or extended-spectrum cephalosporins and cephamycins among Escherichia coli isolates from animals and humans (2003) J. Infect. Dis., 188 (5), pp. 759-768
  • Johnson, Logue, C.M., Johnson, J.R., Kuskowski, M.A., Sherwood, J.S., Barnes, H.J., DebRoy, C., Nolan, L.K., Associations between multidrug resistance, plasmid content, and virulence potential among extraintestinal pathogenic and commensal Escherichia coli from humans and poultry (2012) Foodborne Pathog. Dis., 9 (1), pp. 37-46
  • Johnson, J.R., O'Bryan, T.T., Kuskowski, M., Maslow, J.N., Ongoing horizontal and vertical transmission of virulence genes and papA alleles among Escherichia coli blood isolates from patients with diverse-source bacteremia (2001) Infect. Immun., 69 (9), pp. 5363-5374
  • Jouini, A., Vinue, L., Slama, K.B., Sáenz, Y., Klibi, N., Hammami, S., Boudabous, A., Torres, C., Characterization of CTX-M and SHV extended-spectrum beta-lactamases and associated resistance genes in Escherichia coli strains of food samples in Tunisia (2007) J. Antimicrob. Chemother., 60 (5), pp. 1137-1141
  • Kilani, H., Abbassi, M.S., Ferjani, S., Mansouri, R., Sghaier, S., Ben Salem, R., Jaouani, I., Boubaker, I.B., Occurrence of bla CTX-M-1, qnrB1 and virulence genes in avian ESBL-producing Escherichia coli isolates from Tunisia (2015) Frontiers in cellular and infection microbiology, 5, p. 38
  • Kohler, C.D., Dobrindt, U., What defines extraintestinal pathogenic Escherichia coli? (2011) Int. J. Med. Microbiol., 301 (8), pp. 642-647
  • Saunders, L., Establishing the new red algal subclass Corallinophycidae (2007) Mol. Phylogenet. Evol., 43 (3), pp. 1118-1130
  • Liébana, E., Carattoli, A., Coque, T.M., Hasman, H., Magiorakos, A.P., Mevius, D., Peixe, L., Threlfall, J., Public health risks of enterobacterial isolates producing extended-spectrum beta-lactamases or AmpC beta-lactamases in food and food-producing animals: an EU perspective of epidemiology, analytical methods, risk factors, and control options (2013) Clin. Infect. Dis., 56 (7), pp. 1030-1037
  • Machado, E., Canton, R., Baquero, F., Galan, J.C., Rollan, A., Peixe, L., Coque, T.M., Integron content of extended-spectrum-beta-lactamase-producing Escherichia coli strains over 12 years in a single hospital in Madrid, Spain (2005) Antimicrob. Agents Chemother., 49 (5), pp. 1823-1829
  • Matsumura, Y., Yamamoto, M., Nagao, M., Hotta, G., Matsushima, A., Ito, Y., Takakura, S., Ichiyama, S., Emergence and spread of B2-ST131-O25b, B2-ST131-O16 and D-ST405 clonal groups among extended-spectrum-beta-lactamase-producing Escherichia coli in Japan (2012) J. Antimicrob. Chemother., 67 (11), pp. 2612-2620
  • Mellata, M., Human and avian extraintestinal pathogenic Escherichia coli: infections, zoonotic risks, and antibiotic resistance trends (2013) Foodborne Pathog. Dis., 10 (11), pp. 916-932
  • Meunier, D., Jouy, E., Lazizzera, C., Kobisch, M., Madec, J.Y., CTX-M-1- and CTX-M-15-type beta-lactamases in clinical Escherichia coli isolates recovered from food-producing animals in France (2006) Int. J. Antimicrob. Agents, 28 (5), pp. 402-407
  • Millet, S., Maertens, L., The European ban on antibiotic growth promoters in animal feed: From challenges to opportunities (2011) Vet. J., 187 (2), pp. 143-144
  • Mnif, B., Ktari, S., Rhimi, F.M., Hammami, A., Extensive dissemination of CTX-M-1- and CMY-2-producing Escherichia coli in poultry farms in Tunisia (2012) Lett. Appl. Microbiol., 55 (6), pp. 407-413
  • Nandanwar, N., Janssen, T., Kuhl, M., Ahmed, N., Ewers, C., Wieler, L.H., Extraintestinal pathogenic Escherichia coli (ExPEC) of human and avian origin belonging to sequence type complex 95 (STC95) portray indistinguishable virulence features (2014) Int. J. Med. Microbiol., 304 (7), pp. 835-842
  • Paterson, D.L., Bonomo, R.A., Extended-spectrum beta-lactamases: a clinical update (2005) Clin. Microbiol. Rev., 18 (4), pp. 657-686
  • Pérez-Pérez, F.J., Hanson, N.D., Detection of plasmid-mediated AmpC beta-lactamase genes in clinical isolates by using multiplex PCR (2002) J. Clin. Microbiol., 40 (6), pp. 2153-2162
  • Reich, F., Atanassova, V., Klein, G., Extended-spectrum beta-lactamase- and AmpC-producing enterobacteria in healthy broiler chickens, Germany (2013) Emerg. Infect. Dis., 19 (8), pp. 1253-1259
  • Sáenz, Y., Brinas, L., Dominguez, E., Ruiz, J., Zarazaga, M., Vila, J., Torres, C., Mechanisms of resistance in multiple-antibiotic-resistant Escherichia coli strains of human, animal, and food origins (2004) Antimicrob. Agents Chemother., 48 (10), pp. 3996-4001
  • Saladin, M., Cao, V.T., Lambert, T., Donay, J.L., Herrmann, J.L., Ould-Hocine, Z., Verdet, C., Arlet, G., Diversity of CTX-M beta-lactamases and their promoter regions from Enterobacteriaceae isolated in three Parisian hospitals (2002) FEMS Microbiol. Lett., 209 (2), pp. 161-168
  • Sallem, R.B., Gharsa, H., Slama, K.B., Rojo-Bezares, B., Estepa, V., Porres-Osante, N., Jouini, A., Torres, C., First detection of CTX-M-1, CMY-2, and QnrB19 resistance mechanisms in fecal Escherichia coli isolates from healthy pets in Tunisia (2013) Vector Borne Zoonotic Dis., 13 (2), pp. 98-102
  • Soufi, L., Abbassi, M.S., Sáenz, Y., Vinue, L., Somalo, S., Zarazaga, M., Abbas, A., Torres, C., Prevalence and diversity of integrons and associated resistance genes in Escherichia coli isolates from poultry meat in Tunisia (2009) Foodborne Pathog. Dis., 6 (9), pp. 1067-1073
  • Soufi, L., Sáenz, Y., Vinue, L., Abbassi, M.S., Ruiz, E., Zarazaga, M., Ben Hassen, A., Torres, C., Escherichia coli of poultry food origin as reservoir of sulphonamide resistance genes and integrons (2011) Int. J. Food Microbiol., 144 (3), pp. 497-502
  • Tartof, S.Y., Solberg, O.D., Manges, A.R., Riley, L.W., Analysis of a uropathogenic Escherichia coli clonal group by multilocus sequence typing (2005) J. Clin. Microbiol., 43 (12), pp. 5860-5864
  • Tenover, F.C., Arbeit, R.D., Goering, R.V., Mickelsen, P.A., Murray, B.E., Persing, D.H., Swaminathan, B., Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing (1995) J. Clin. Microbiol., 33 (9), pp. 2233-2239