Characterization of extended spectrum β-lactamase producing Escherichia coli strains isolated from urogenital system of dogs in Van province of Turkey

Document Type : Full paper (Original article)

Authors

1 MSc in Microbiology, Department of Veterinary Microbiology, Institute of Health Sciences, Van Yuzuncu Yil University, Van, Turkey

2 Department of Microbiology, Faculty of Veterinary Medicine, Siirt University, Siirt, Turkey

Abstract

Background: Escherichia coli is a bacterial agent that causes urogenital system infection in dogs. Beta-lactam (β-lactam) group antibiotics are frequently used in the treatment of E. coli infections. Aims: This study aimed to investigate the presence of extended-spectrum β-lactamase (ESBL) and plasmidic AmpC in E. coli strains isolated from the urogenital tracts of 125 dogs. Methods: Fifty E. coli strains were identified by conventional bacteriological and PCR methods. Disk diffusion method was used for the determination of antimicrobial susceptibility of the isolates as well as productions of plasmidic AmpC and ESBL. The presence of blaTEM, blaSHV, and blaCTX-M group genes was determined in the isolates by PCR. ERIC-PCR was also used for genotyping of the isolates. Results: Although 22 (44%) of 50 E. coli isolates were found to be ESBL positive, no isolate shows plasmidic AmpC β-lactamase production. Among 22 ESBL positive isolates, blaTEM, blaSHV, and blaCTX-M group 1 genes were found in 11 (50%), 1 (4.54%), and 6 (27.27%) isolates, respectively. The highest resistance was observed against tetracycline (28%), followed by streptomycin (24%), trimethoprim-sulfamethoxazole (24%), and chloramphenicol (22%), respectively. In the isolates, 11 different main profiles were also determined by ERIC-PCR. It was shown that ESBL positive isolates were related to G10 profiles. Conclusion: The use of extended spectrum β-lactam group antibiotics for the treatment of E. coli infections in dogs is critical; nevertheless, they may not be effective due to the high rate of resistance to this antibiotic group in E. coli.

Keywords


Aslantaş, Ö and Yılmaz, EŞ (2017). Prevalence and molecular characterization of extended spectrum β-lactamase (ESBL) and plasmidic AmpC β-lactamase (pAmpC) producing Escherichia coli in dogs. J. Vet. Med. Sci., 79: 1024-1030.
Bortolami, A; Zendri, F; Maciuca, EI; Watrett, A; Ellis, C; Vanessa, S; Pinchbeck, G and Timofte, D (2019). Diversity, virulence and clinical significance of extended spectrum β-Lactamase and pAmpC producing Escherichia coli from companion animals. Front. Microbiol., 10: 1260-1274.
Bourne, JA; Chong, WL and Gordon, DM (2019). Genetic structure, antimicrobial resistance and frequency of human associated Escherichia coli sequence types among faecal isolates from healthy dogs and cats living in Canberra, Australia. PLoS One. 14: e0212867.
Bradford, PA (2001). Extended spectrum beta-lactamases in the 21st century. Characterization, epidemiology and detection of this important resistance threat. Clin. Micr. Rev., 14: 933-951.
Bush, K; Jacoby, GA and Medeiros, AA (1995). A functional classification scheme for β-lactamases and its correlation with molecular structure. Antimicrob. Agents. Chemother., 39: 1211-1233.
Carattoli, A; Lovari, S; Franco, A; Cordaro, G; Di, MP and Battisti, A (2005). Extended spectrum β-lactamases in Escherichia coli isolated from dogs and cats in Rome, Italy, from 2001 to 2003. Antimicrob. Agents. Chemother., 49: 833-835.
Clinical and Laboratory Standards Institute (CLSI) (2018). Performance standards for antimicrobial disk and dilution susceptibility test for bacteria isolated from animals. 4th Edn., CLSI Supplement VET08. Clinical and Laboratory Standards Institute, Wayne, PA.
Essack, SY (2001). The development of beta lactam antibiotics in response to the evolution of beta lactamases. Pharm. Res., 18: 1391-1399.
European Committee on Antimicrobial Susceptibility Testing (EUCAST) (2019). European Committee on Antimicrobial Susceptibility Testing breakpoint tables for interpretation of MICs and zone diameters. Version 9.0, valid from 2019-01-01. http://www.eucast.org.
Fransson, B; Lagerstedt, AS; Hellmen, E and Jonsson P (1997). Bacteriological findings, blood chemistry profile and plasma endotoxin levels in bitches with pyometra or other uterine diseases. Zentralbl. Veterinarmed., 44: 417-426.
Galleni, M; Amicosante, G and Frere, JM (1988). A survey of the kinetic parameters of class C beta-lactamases, cephalosporins and other beta-lactam compounds. Biochem. J., 255: 123-129.
Garcia, BS; Galan, F; Rodriguez-Iglesias, MA and Perez-Gracia, MT (2019). Detection and characterization of extended-spectrum beta-lactamases-producing Escherichia coli in animals. Vector Borne Zoonotic Dis., 19: 115-120.
Gumus, B; Celık, B; Kahraman, BB; Sıgırcı, BD and Ak, S (2017). Determination of extended spectrum beta-lactamase (ESBL) and AmpC beta lactamase producing Escherichia coli prevalence in faecal samples of healthy dogs and cats. Revue Med. Vet., 168: 46-52.
Gür, D (1997). Antibiotic resistance mechanisms in Gram-negative bacteria that gain importance in hospital infections. Hastane İnfeksiyonları Dergisi., 1: 38-45. (in Turkish).
Hagman, R and Greko, C (2005). Antimicrobial resistance in Escherichia coli isolated from bitches with pyometra and from urine samples from other dogs. Vet. Rec., 157: 193-197.
Huber, H; Zweifel, C; Wittenbrink, MM and Stephan, R (2013). ESBL-producing uropathogenic Escherichia coli isolated from dogs and cats in Switzerland. Vet. Microbiol., 162: 992-996.
Jacoby, GA (2009). AmpC beta lactamases. Clin. Microbiol. Rev., 22: 161-182.
Kaper, JB; Nataro, JP and Mobley, HL (2004). Pathogenic Escherichia coli. Nat. Rev. Microbiol., 2: 123-140.
Kapoda, DS; Ajayi, A; Somda, M; Traore, O; Guessennd, N; Ouattara, AS; Sangare, L; Alfred, S; Traore, AS and Dosso, M (2018). Distribution of resistance genes encoding ESBLs in Enterobacteriaceae isolated from biological samples in health centers in Ouagadougou, Burkina Faso. BMC Res. Notes. 11: 471-475.
Livermore, DM; Canton, R; Gniadkowski, M; Nordmann, P; Rossolini, GM; Arlet, G; Ayala, J; Coque, TM; Kern-Zdanowicz, I; Luzzaro, F; Poirel, L and Woodford, N (2007). CTX-M: changing the face of ESBLs in Europe. J. Antimicrob. Chemother., 59: 165-174.
Magiorakos, AP; Srinivasan, A; Carey, RB; Carmeli, Y; Falagas, ME; Giske, CG; Harbarth, S; Hindler, JF; Kahlmeter, G; Olsson-Liljequist, B; Paterson, DL; Rice, LB; Stelling, J; Maluta, RP; Stella, AE; Riccardi, K; Rigobelo, EC; Marin, JM; Carvalho, MB and de Ávila, FA (2012). Phenotypical characterization and adhesin identification in Escherichia coli strains isolated from dogs with urinary tract infections. Braz. J. Microbiol., 43: 375-381.
Meacham, KJ; Zhang, L; Foxman, B; Bauer, RJ and Marrs, CF (2003). Evaluation of genotyping large numbers of Escherichia coli isolates by enterobacterial repetitive intergenic consensus-PCR. J. Clin. Microbiol., 41: 5224-5226.
Moreno, A; Bello, H; Guggiana, D; Dominguez, M and Gonzalez, G (2008). Extended-spectrum β-lactamases belonging to CTX-M group produced by Escherichia coli strains isolated from companion animals treated with enrofloxacin. Vet. Microbiol., 129: 203-208.
Moyaert, H; Morrissey, I; Jong, A; El Garch, F; Klein, U; Ludwig, C; Thiry, J and Youala, M (2017). Antimicrobial susceptibility monitoring of bacterial pathogens isolated from urinary tract infections in dogs and cats across Europe: ComPath results. Microb. Drug. Resist., 23: 391-403.
Mulvey, MR; Bryce, E; Boyd, D; Marianna, OA; Christianson, S; Simor, AE and Paton, S (2004). Ambler class A extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella spp. in Canadian hospitals. Antimicrob. Agents. Chemother., 48: 1204-1214.
Oliver, A; Perez-Diaz, JC; Coque, TM; Baquero, F and Canton, R (2001). Nucleotide sequence and characterization of a novel cefotaxime-hydrolyzing beta-lactamase (CTX-M-10) isolated in Spain. Antimicrob. Agents. Chemother. 45: 616-620.
Panos, GZ; Betsi, GI and Falagas, ME (2006). Systematic review: Are antibiotics detrimental or beneficial for the treatment of patients with Escherichia coli O157:H7 infection. Aliment. Pharmacol. Ther., 24: 731-742.
Papini, R; Ebani, VV; Cerri, D and Guidi, G (2006). Survey on bacterial isolates from dogs with urinary tract infections and their in vitro sensitivity. Rev. Med. Vet., 157: 35-45.
Paredes, DO; Haro, M; Leoro-Garzon, P; Barba, P; Loaiza, K; Mora, F; Fors, M; Vinueza-Burgos, C and Fernández-Moreira, E (2019). Multidrug resistant Escherichia coli isolated from canine faeces in a public park in Quito, Ecuador. J. Glob. Antimicrob. Re., 18: 263-268.
Pool, K (2004). Resistance to beta-lactam antibiotics. Cell Mol. Life Sci., 61: 2200-2223.
Qekwana, DN; Phophi, L; Naidoo, V and Oguttu, JW (2018). Antimicrobial resistance among Escherichia coli isolates from dogs presented with urinary tract infections at a veterinary teaching hospital in South Africa. BMC Vet. Res., 14: 228-233.
Quinn, PJ; Markey, BK; Leonard, FC; Hartigan, P; Fanning, S; Fitzpatrick, E and Hartigan, PJ (2011). Enterobacteriaceae. In: Veterinary microbiology and microbial disease. (2nd Edn.), Oxford, UK, Wiley-Blackwell. PP: 263-286.
Rzewuska, M; Stefanska, I; Kizerwetter-Swida, M; Chrobak-Cmiel, D; Szczygielska, P; Lesniak, M and Binek, M (2015). Characterization of extended-spectrum β-lactamases produced by Escherichia coli strains isolated from dogs in Poland. Pol. J. Microbiol., 64: 285-288.
Sader, HS; Hsiung, A; Fritsche, TR and Jones, RN (2007). Comparative activities of cefepime and piperacillin/ tazobactam tested against a global collection of Escherichia coli and Klebsiella spp. with an ESBL phenotype. Diagn. Microbiol. Infect. Dis., 57: 341-344.
Sfaciotte, RAP; Parussolo, L; Melo, FD; Wildemann, P; Bordignon, G; Israel, ND; Leitzke, M; Wosiacki, SR; Salbego, FZ; da Costa, UM and Ferraz, SM (2021). Identification and characterization of multidrug-resistant extended-spectrum beta-lactamase-producing bacteria from healthy and diseased dogs and cats admitted to a veterinary hospital in Brazil. Microbial. Drug Resist., 27: 855-864.
Shimizu, T; Harada, K; Tsuyuki, Y; Kimura, Y; Miyamoto, T; Hatoya, S and Hikasa, Y (2017). In vitro efficacy of 16 antimicrobial drugs against a large collection of β-lactamase producing isolates of extraintestinal pathogenic Escherichia coli from dogs and cats. J. Med. Microbiol., 66: 1085-1091.
Shin, SR; Noh, SM; Jung, WK; Shin, S; Park, YK; Moon, DC; Lim, SK; Park, YH and Park, KT (2021). Characterization of extended-spectrum β-lactamase producing and AmpC β-lactamase producing Enterobacterales isolated from companion animals in Korea. Antibiotics. 10: 249-259.
Tan, TY; Ng, LSY; He, J; Koh, TH and Hsu, LY (2009). Evaluation of screening methods to detect plasmid-mediated AmpC in Escherichia coli, Klebsiella pneumoniae, and Proteus mirabilis. Antimicrob. Agents Chemother., 53: 146-149.
Tramuta, C; Nucera, D; Robino, P; Salvarani, S and Nebbia, P (2011). Virulence factors and genetic variability of uropathogenic Escherichia coli isolated from dogs and cats in Italy. J. Vet. Sci., 12: 49-55.
Versalovic, J; Koeuth, T and Lupski, R (1991). Distribution of repetitive DNA sequences in eubacteria and application to finerpriting of bacterial genomes. Nucleic Acids Res.,
19: 6823-6831.
Vila, J; Saez-Lopez, E; Johnson, JR; Romling, U; Dobrindt, U; Canton, R; Giske, CG; Naas, T; Carattoli, A; Martínez-Medina, M; Bosch, J; Retamar, P; Rodríguez-Baño, J; Baquero, F and Soto, SM (2016). Escherichia coli: an old friend with new tidings. FEMS Microbiol. Rev., 40: 437-463.
Wang, G; Clark, CG and Rodgers, FG (2002). Detection in Escherichia coli of the genes encoding the major virulence factors, the genes defining the O157:H7 serotype, and components of the type 2 shiga toxin family by multiplex PCR. J. Clin. Microbiol., 40: 3613-3619.
Windahl, U; Holst, BS; Nyman, A; Grönlund, U and Bengtsson, B (2014). Characterisation of bacterial growth and antimicrobial susceptibility patterns in canine urinary tract infections. BMC Vet. Res., 10: 1-10.
Woodford, N; Fagan, EJ and Ellington, MJ (2006). Multiplex PCR for rapid detection of genes encoding CTX-M extended-spectrum β-lactamases. J. Antimicrob. Chemother., 57: 154-155.
Yu, Z; Wang, Y; Chen, Y; Huang, M; Wang, Y; Shen, Z; Xia, Z and Li, G (2020). Antimicrobial resistance of bacterial pathogens isolated from canine urinary tract infections. Vet. Microbiol., 241: 108540.
Zogg, AL; Zurfluh, K; Schmitt, S; Nüesch-Inderbinen, M and Stephan, R (2018). Antimicrobial resistance, multilocus sequence types and virulence profiles of ESBL producing and non-ESBL producing uropathogenic Escherichia coli isolated from cats and dogs in Switzerland. Vet. Microbiol., 216: 79-84.