Duration of carriage of multidrug-resistant bacteria in dogs and cats in veterinary care and co-carriage with their owners

Abstract

Background: The emergence and spread of multidrug-resistant organisms (MDROs) represent a threat to human and animal health.

Objectives: To assess duration of carriage of MDROs in dogs and cats presented to veterinary clinics/hospitals in Switzerland. To estimate prevalence, duration of and risk factors for MDRO carriage in their owners and the occurrence of co-carriage in owner-pet pairs.

Methods: Prospective, longitudinal, observational study. Nasal swabs and fecal samples were collected from 50 owners of dogs and cats presented to 3 large veterinary hospitals, 1 medium-sized clinic and 1 practice. If pet or owner tested positive for a MDRO, follow-up samples were collected for up to 8 months. Methicillin-resistant (MR) Staphylococcus aureus, MR S. pseudintermedius, MR coagulase-negative staphylococci (MRCoNS), MR Macrococcus spp., cephalosporinase- and carbapenemase-producing (CP) Enterobacterales were isolated and further characterized by MALDI-TOF MS, microdilution, β-lactam resistance gene detection, REP/ERIC-PCR, multilocus sequence typing or whole-genome sequencing. Risk factors for MDRO carriage in owners were explored based on questionnaire-derived data.

Results: Five out of 50 owners carried 3rd generation cephalosporin-resistant Enterobacterales (3GC-R-Ent.), and 5/50 MRCoNS. In 3 dogs and 4 cats carriage of 3GC-R-Ent. persisted for up to 136 days after discharge (median 99 days, IQR 83 days, range 36-136 days), in two cats isolates were carbapenem-resistant. Owner-pet co-carriage was not observed. No specific risk factors for MDRO carriage in owners were identified.

Conclusions: After discharge from veterinary care, dogs and cats may carry 3GC-R-Ent. for prolonged time periods. Carriage of MDROs was common in owners, but pet-owner co-carriage of the same MDRO was not observed.

Keywords: 3GC-R, Third Generation Cephalosporin-resistant; 3GC-R-Ent., Third Generation Cephalosporin-resistant Enterobacterales; AMR, Antimicrobial resistance; CI, Confidence interval; CLSI, Clinical and Laboratory Standards Institute; COL-R, Colistin-resistant; CP, Carbapenemase-producing; CR, Carbapenem-resistant; CRE, Carbapenem-resistant Enterobacterales; Carbapenemase-producing Enterobacterales; Co-carriage; Companion animal; ERIC-PCR, Enterobacterial repetitive intergenic consensus polymerase chain reaction; ESBL, Extended spectrum β-lactamase; ESBL-E. coli, ESBL-producing Escherichia coli; ESBL-KP, ESBL-producing Klebsiella pneumoniae; EUCAST, European Committee on Antimicrobial Susceptibility Testing; Extended-spectrum β-lactamase; IQR, Interquartile range; KP, Klebsiella pneumoniae; MALDI-TOF MS, Matrix-assisted laser desorption/ionization time of flight mass spectrometry; MDR, Multidrug-resistant; MDROs, Multidrug-resistant organisms; MICs, Minimal inhibitory concentrations; MLST, Multilocus sequence typing; MR, Methicillin-resistant; MRCoNS, Methicillin-resistant coagulase-negative staphylococci; MRSA, Methicillin-resistant Staphylococcus aureus; MRSP, Methicillin-resistant Staphylococcus pseudintermedius; REP-PCR, Repetitive element palindromic polymerase chain reaction; ST, Sequence type; TMP-S, Trimethoprim/sulfamethoxazole; Transmission; WGS, Whole-genome sequencing; pAmpC, Plasmid-encoded AmpC.

Fig. 1

Study design. Out of a population of 271 animals enrolled in a large prevalence study, 25 dogs and 9 cats, which had tested positive for MDRO carriage and 2 dogs belonging to a MDRO positive owner were followed up by nasal and rectal swabbing for up to 8 months. 50 owners of animals participating in this study submitted nasal swabs and/or fecal samples, 38 submitted questionnaires. Five owner-cat pairs and 16 owner-dog pairs were followed to monitor for co-colonization. The part of this study in the grey box has been previously reported [11]. Abbreviations: MDROs, multidrug-resistant organisms.

Fig. 2

Duration of carriage of multidrug-resistant organisms in dogs, cats and their respective owners. Only dogs and cats which were colonized with genetically related isolates beyond 30 days are shown. For a graphical overview of all cases included in the follow-up study see Supplemental Figs. 1–3. P: Presentation; D: Discharge. Red symbols: MDRO isolated. Green symbols: no MDRO isolated. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) Presentation □ Discharge ○ Follow-up Antimicrobial treatments Potentiated aminopenicillins Fluoroquinolones Abbreviations: CP: carbapenemase-producing; ESBL: extended spectrum β-lactamase-producing; E. coli: Escherichia coli; KP: Klebsiella pneumoniae; E. cloacae: Enterobacter cloacae; MR: Methicillin-resistant; S.: Staphylococcus

Fig. 3

Representative cases from the co-colonization study. While several owner-pet pairs showed colonization with multidrug-resistant organisms, co-colonization with genetically related organisms was not detected in any of the 21 owner-pet paires in the study. For a graphical overview of all cases included in the co-colonization study see supplemental Figs. 1 and 2. P: Presentation; D: Discharge. Red symbols: MDRO isolated. Green symbols: no MDRO isolated. Open symbol: no sample analyzed. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) Presentation □ Discharge ○ Follow-up Antimicrobial treatments First generation cephalosporin Potentiated aminopenicillin Fluoroquinolone Clindamycin + trimethoprim+sulphamethoxazole Perioperative cefazolin