Prevalence of Beta-Lactam and Quinolone/Fluoroquinolone Resistance in Enterobacteriaceae From Dogs in France and Spain—Characterization of ESBL/pAmpC Isolates, Genes, and Conjugative Plasmids

Abstract

Quantitative data on fecal shedding of antimicrobial-resistant bacteria are crucial to assess the risk of transmission from dogs to humans. Our first objective was to investigate the prevalence of quinolone/fluoroquinolone-resistant and beta-lactam-resistant Enterobacteriaceae in dogs in France and Spain. Due to the particular concern about possible transmission of extended-spectrum cephalosporin (ESC)-resistant isolates from dogs to their owners, we characterized the ESBL/pAmpC producers collected from dogs. Rectal swabs from 188 dogs, without signs of diarrhea and that had not received antimicrobials for 4 weeks before the study, were quantified for total and resistant Enterobacteriaceae on selective media alone or containing relevant antibiotic concentrations. Information that might explain antibiotic resistance was collected for each dog. Extended-spectrum cephalosporin-resistant isolates were subjected to bacterial species identification (API20E), genetic lineage characterization (MLST), ESBL/pAmpC genes identification (sequencing), and plasmid characterization (pMLST). Regarding beta-lactam resistance, amoxicillin- (AMX) and cefotaxime- (CTX) resistant Enterobacteriaceae were detected in 70 and 18% of the dogs, respectively, whereas for quinolone/fluoroquinolone-resistance, Nalidixic acid- (NAL) and ciprofloxacin- (CIP) resistant Enterobacteriaceae were detected in 36 and 18% of the dogs, respectively. Medical rather than preventive consultation was a risk marker for the presence of NAL and CIP resistance. CTX resistance was mainly due to a combination of specific ESBL/pAmpC genes and particular conjugative plasmids already identified in human patients: bla CTX−M−1 /IncI1/ST3 ( n = 4), bla CMY−2 /IncI1/ST12 ( n = 2), and bla CTX−M−15 /IncI1/ST31 ( n = 1). bla SHV−12 ( n = 3) was detected in various plasmid lineages (InI1/ST3, IncI1/ST26, and IncFII). ESBL/pAmpC plasmids were located in different genetic lineages of E. coli , with the exception of two strains in France (ST6998) and two in Spain (ST602). Our study highlights dogs as a potential source of Q/FQ-resistant and ESBL/pAmpC-producing bacteria that might further disseminate to humans, and notably a serious risk of future acquisition of CTX-M-1 and CMY-2 plasmids by the owners of dogs.

High Prevalence and Diversity of Cephalosporin-Resistant Enterobacteriaceae Including Extraintestinal Pathogenic E. coli CC648 Lineage in Rural and Urban Dogs in Northwest Spain

“…The high genetic diversity and ESBL/pAmpC types found in the present study has been previously described within E. coli recovered from dogs [ 17 , 25 ], as well as the STs 93, 453, and 770, found here in isolates conforming the ExPEC status [ 17 , 25 , 26 ]. Five bla CTX-M-14 -carrying isolates recovered in this study belonged to ST770 Escherichia clade I.…”

Broad-Spectrum Cephalosporin-Resistant and/or Fluoroquinolone-Resistant Enterobacterales Associated with Canine and Feline Urogenital Infections

“…Based on the published surveys [19,[26][27][28], the use of critically important antimicrobials (amongst them 3rd and 4th generation cephalosporins and fluoroquinolones) is cited as being frequently prescribed for dogs and cats in a number of countries including Belgium, Spain, France, the United Kingdom and Germany. Carbapenems are mostly prescribed in complicated cases (MDR infections) based on results of susceptibility testing and treatment durations are longer than typically recommended in human medicine [26].…”

“…In the European Union, including Austria, especially at the University of Veterinary Medicine, Vienna, veterinarians are advised to follow strict guidelines for the use of antibiotics. Except for few countries including the Netherlands and France, veterinarians are allowed to use human-related antibiotics in companion animals, even carbapenems, but only in strictly defined and justified cases [25][26][27][28]. Despite carbapenems have no legal indication in some countries and are not used in routine practice, ISCAID and other relevant institutions have included carbapenems in their official documentation related to animals [18,29].…”

“…Despite carbapenems have no legal indication in some countries and are not used in routine practice, ISCAID and other relevant institutions have included carbapenems in their official documentation related to animals [18,29]. Close contact between humans and companion animals contributes to the propagation and exchange of resistance genes between bacteria as well as the direct transmission of all ExPEC subcategories including UPECs, so human-related clones have already been detected in companion animals [27,[30][31][32]. As a consequence, companion animals are more and more considered an important source of human infections both by ExPEC/UPEC and by multidrug-resistant bacteria (MDR) in general [20,26,[33][34][35][36].…”

Antibiotic-Resistant Escherichia Coli and Sequence Type 131 in Fecal Colonization in Dogs in Taiwan

“…Nearly half of the E. coli isolates were resistant to cefazolin, about 20% were resistant to fluoroquinolone, and about 10% were ESBL producing. Among healthy dogs in France and Spain, the rate of third generation cephalosporin resistance and fluroquinolone resistance was about 18% according to the anal swab [35]. In Pakistan, the percentage of ESBL-producing E. coli isolates in dog feces was shown to be as high as 80% [36], while data from the US showed a prevalence of less than 10% in dogs [37].…”