Patterns of antimicrobial agent prescription in a sentinel population of canine and feline veterinary practices in the United Kingdom

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Highlights

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Antimicrobial agent prescription was monitored in a large UK population of cats and dogs over a 2 year period (2014–2016).
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Systemic antimicrobial agents were prescribed more frequently to cats; topical prescription was more frequent in dogs.
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A temporal reduction (2014–2016) in antimicrobial agent prescription was observed in both cats and dogs in this population.
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Premises which prescribed antimicrobial agents commonly to cats generally also prescribed commonly to dogs.
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The most frequently prescribed antibiotics were cefovecin in cats and clavulanic acid potentiated amoxicillin in dogs.

Abstract

Antimicrobial resistance is an increasingly important global health threat and the use of antimicrobial agents is a key risk factor in its development. This study describes antimicrobial agent prescription (AAP) patterns over a 2 year period using electronic health records (EHRs) from booked consultations in a network of 457 sentinel veterinary premises in the United Kingdom. A semi-automated classification methodology was used to map practitioner defined product codes in 918,333 EHRs from 413,870 dogs and 352,730 EHRs from 200,541 cats, including 289,789 AAPs. AAP as a proportion of total booked consultations was more frequent in dogs (18.8%, 95% confidence interval, CI, 18.2–19.4) than cats (17.5%, 95% CI 16.9–18.1). Prescription of topical antimicrobial agents was more frequent in dogs (7.4%, 95% CI 7.2–7.7) than cats (3.2%, 95% CI 3.1–3.3), whilst prescription of systemic antimicrobial agents was more frequent in cats (14.8%, 95% CI 14.2–15.4) than dogs (12.2%, 95% CI 11.7–12.7). A decreasing temporal pattern was identified for prescription of systemic antimicrobial agents in dogs and cats. Premises which prescribed antimicrobial agents frequently for dogs also prescribed frequently for cats. AAP was most frequent during pruritus consultations in dogs and trauma consultations in cats. Clavulanic acid potentiated amoxicillin was the most frequently prescribed antimicrobial agent in dogs (28.6% of prescriptions, 95% CI 27.4–29.8), whereas cefovecin, a third generation cephalosporin, was the most frequently prescribed antimicrobial agent in cats (36.2%, 95% CI 33.9–38.5). This study demonstrated patterns in AAP over time and for different conditions in a population of companion animals in the United Kingdom.

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Possible Transmission of mcr-1–Harboring Escherichia coli between Companion Animals and Human

Xue-Fei Zhang, Yohei Doi, Xi Huang … (2016)

To the Editor: Plasmid-mediated, colistin-resistance mechanism gene mcr-1 was first identified in Escherichia coli isolates from food, food animals, and human patients in November 2015 ( 1 ). Reports on detection of mcr-1 in Enterobacteriaceae from humans and food animals soon followed from ≈12 countries ( 2 – 5 ). Here we report detection of mcr-1 in colistin-resistant E. coli isolated from companion animals and the possible transmission of mcr-1–harboring E. coli between companion animals and a person. Three mcr-1–harboring E. coli clinical isolates were identified from specimens of 3 patients admitted to a urology ward of a hospital in Guangzhou, China. E. coli isolate EC07 was identified in the urine of a 50-year-old male patient with glomerulonephritis in October 2015. Isolate EC08 was cultured from the urine of a 48-year-old male patient with prostatitis in December 2015. IsolateEC09 was identified in the blood of an 80-year-old male patient with bladder cancer 3 weeks after EC08 was identified. Review of medical records identified the patient carrying E. coli isolate EC07 as a worker at a pet shop. In light of this finding, we collected a total of 53 fecal samples from 39 dogs and 14 cats in the pet shop where the man worked. We isolated and identified colonies consistent with E. coli from fecal samples on MacConkey agar plates (Thermo Fisher, Beijing, China) and API 20E system (bioMérieux, Durham, NC, USA). We prepared crude DNA samples of isolates for PCR testing by boiling cells in water. Among them, 6 were positive for mcr-1 by PCR and sequencing (4 from dogs and 2 from cats). All 6 isolates were resistant to colistin, polymyxin B, cephalosporin, gentamicin, and ciprofloxacin by using the agar dilution method, in accordance with the European Committee on Antimicrobial Susceptibility Testing (http://www.eucast.org) for colistin and polymyxin B and Clinical and Laboratory Standards Institute guidelines (http://www.clsi.org) for the other antimicrobial drugs. We identified various resistance genes accounting for the multidrug resistance in these 9 mcr-1–positive isolates ( 6 , 7 ) (Table). We noted that E. coli isolate EC09 was also resistant to carbapenems and positive for bla IMP-4. We observed co-production of mcr-1 and IMP-type metallo-β-lactamase in E. coli. Table Characteristics of 9 mcr-1–positive Escherichia coli isolates from companion animals and human patients, Guangzhou, China Characteristic Isolate PET01 PET02 PET03 PET04 PET05 PET06 EC07 EC08 EC09 Isolation date 2016 Jan 1 2016 Jan 1 2016 Jan 2 2016 Jan 2 2016 Jan 2 2016 Jan 4 2015 Oct 10 2015 Nov 2 2015 Nov 21 Specimen source Cat Dog Dog Dog Cat Dog Human Human Human Specimen type Feces Feces Feces Feces Feces Feces Urine Urine Blood Phylogenetic group B2 D D D B2 D D B1 B1 ST† ST93 ST354 ST354 ST354 New ST354 ST354 ST156 ST156 PFGE type IV I I I V I I II III Resistance genes mcr-1, bla TEM-1, qepA mcr-1, bla TEM-1, bla CTX-M-15, fosA3, aac(6′)-Ib-cr mcr-1, bla TEM-1, bla CTX-M-15, fosA3, aac(6′)-Ib-cr mcr-1, bla TEM-1, bla CTX-M-15, fosA3, aac(6′)-Ib-cr mcr-1, bla TEM-1, bla SHV-12, bla CTX-M-15, fosA3, rmtB, qnrS, aac(6′)-Ib-cr mcr-1, bla TEM-1, bla CTX-M-15, fosA3, aac(6′)-Ib-cr mcr-1, bla TEM-1, bla CTX-M-15, fosA3, aac(6′)-Ib-cr mcr-1, bla TEM-1, bla CTX-M-55, fosA3, rmtB, qepA1 mcr-1, bla IMP-4, bla TEM-1, bla CTX-M-55, fosA3, rmtB, qepA1 MIC, μg/mL Colistin 16 8 8 16 16 8 8 8 64 Polymyxin B 16 16 16 32 16 16 8 8 64 Ampicillin >256 >256 >256 >256 >256 >256 >256 >256 >256 AMX/CLV 16 32 32 32 256 16 32 16 16 Cefotaxime 64 >256 256 >256 256 >256 256 256 >256 Ceftazidime 16 256 128 256 64 256 128 32 >256 Cefepime 8 256 128 256 16 256 64 64 >256 Gentamicin 128 >256 >256 >256 256 >256 >256 >256 >256 Amikacin 4 >256 >256 >256 >256 >256 >256 >256 >256 Ertapenem 16 Imipenem 16 Meropenem 16 Fosfomycin 32 >512 >512 >512 >512 >512 >512 >512 >512 Tigecycline <2 <2 <2 <2 <2 <2 <2 <2 4 Nitrofurantoin <16 32 32 32 128 32 64 64 32 Ciprofloxacin 256 128 128 128 64 128 128 256 256 *AMX/CLV, amoxicillin clavulanic acid; PFGE, pulsed-field gel electrophoresis; ST, sequence type. †By multilocus sequence typing. We subjected all isolates to multilocus sequence typing, in accordance with the protocol described at http://mlst.warwick.ac.uk/mlst/dbs/Ecoli, and pulsed-field gel electrophoresis as described previously ( 8 – 10 ). We identified 5 mcr-1–positive isolates from 4 dogs (PET02–04 and PET06) and isolate EC07 as sequence type (ST) 354. Isolates PET01 and PET05, identified from cats, belonged to ST93 and a new ST strain, respectively. IsolatesEC08 and EC09, from the patients who shared the same hospital room with the pet shop worker, were ST156 (Table). Results of pulsed-field gel electrophoresis were consistent with multilocus sequence typing results and showed that isolates consisted of 5 types (types I to V; Technical Appendix). Isolate EC07 was clonally related to 4 E. coli strains from dogs, according criteria described by Tenover et al. ( 10 ), suggesting possible transmission of mcr-1–harboring E. coli between dogs and the patient. Colistin resistance was successfully transferred to E. coli C600 through conjugation in all isolates, suggesting that mcr-1 was located on transferable plasmids. These findings suggest that mcr-1–producing E. coli can colonize companion animals and be transferred between companion animals and humans. The findings also suggest that, in addition to food animals and humans, companion animals can serve as a reservoir of colistin-resistant E. coli, adding another layer of complexity to the rapidly evolving epidemiology of plasmid-mediated colistin resistance in the community. Technical Appendix Pulsed-field gel electrophoresis analysis of 9 mcr-1–producing Escherichia coli isolates from companion animals and human patients, Guangzhou, China.

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Characterisation of antimicrobial usage in cats and dogs attending UK primary care companion animal veterinary practices.

E Buckland, I O'Neill, J Summers … (2016)

There is scant evidence describing antimicrobial (AM) usage in companion animal primary care veterinary practices in the UK. The use of AMs in dogs and cats was quantified using data extracted from 374 veterinary practices participating in VetCompass. The frequency and quantity of systemic antibiotic usage was described.Overall, 25 per cent of 963,463 dogs and 21 per cent of 594,812 cats seen at veterinary practices received at least one AM over a two-year period (2012-2014) and 42 per cent of these animals were given repeated AMs. The main agents used were aminopenicillin types and cephalosporins. Of the AM events, 60 per cent in dogs and 81 per cent in cats were AMs classified as critically important (CIAs) to human health by the World Health Organisation. CIAs of highest importance (fluoroquinolones, macrolides, third-generation cephalosporins) accounted for just over 6 per cent and 34 per cent of AMs in dogs and cats, respectively. The total quantity of AMs used within the study population was estimated to be 1473 kg for dogs and 58 kg for cats.This study has identified a high frequency of AM usage in companion animal practice and for certain agents classified as of critical importance in human medicine. The study highlights the usefulness of veterinary practice electronic health records for studying AM usage.

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Qualitative study of factors associated with antimicrobial usage in seven small animal veterinary practices in the UK.

Ana L P Mateus, Nick Barber, Katharina Stärk … (2014)

Responsible use of antimicrobials by veterinarians is essential to contain antimicrobial resistance in pathogens relevant to public health. Inappropriate antimicrobial use has been previously described in practice. However, there is scarce information on factors influencing antimicrobial usage in dogs and cats. We investigated intrinsic and extrinsic factors influencing decision-making of antimicrobial usage in first opinion small animal practices in the UK through the application of qualitative research methods. Semi-structured interviews were conducted with 21 veterinarians from seven veterinary first opinion practices in the UK in 2010. Topics investigated included: a) criteria used for selection of antimicrobials, b) influences by colleagues, c) influences by clients, d) pet characteristics, e) sources of knowledge, f) awareness of guidelines and g) protocols implemented in practice that may affect antimicrobial usage by veterinarians. Hypothetical scenarios selected to assess appropriateness of antimicrobial usage were: a) vomiting in a Yorkshire Terrier due to dietary indiscretion, b) deep pyoderma in a Shar-Pei, c) Feline Lower Urinary Tract disease in an 7 year-old male neutered cat and d) neutering of a 6-months dog. Interviews were recorded and transcribed by the interviewer. Thematic analysis was used to analyse content of transcribed interviews. Data management and analysis was conducted with qualitative analysis software NVivo8 (QSR International Pty Ltd). Antimicrobial usage by participants was influenced by factors other than clinical evidence and scientific knowledge. Intrinsic factors included veterinarian's preference of substances and previous experience. Extrinsic factors influencing antimicrobial selection were; perceived efficacy, ease of administration of formulations, perceived compliance, willingness and ability to treat by pet owners, and animal characteristics. Cost of therapy was only perceived as an influential factor in low, mixed socioeconomic areas. Veterinarians had limited awareness of current recommendations for responsible use in small animal practice. Social norms, particularly verbally agreed protocols influenced veterinarians. Inappropriate antimicrobial usage was identified in the therapy of non-infectious diseases and prophylaxis of routine clean surgical procedures. Discussion of clinical cases with peers and effectiveness meetings in the workplace were useful to veterinarians to share scientific knowledge. Effectiveness meetings can be a common ground for veterinarians to discuss and agree protocols for clinical conditions and surgical procedures. Protocols should be evidence-based, follow current recommendations and take into account the resources available in the workplace. Targeted training of veterinarians in the workplace with peer support should be used to promote responsible antimicrobial usage.

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Author and article information

Contributors

D.A. Singleton

Journal

Journal ID (nlm-ta): Vet J

Journal ID (iso-abbrev): Vet. J

Title: Veterinary Journal (London, England : 1997)

Publisher: Balliere Tindall

ISSN (Print): 1090-0233

ISSN (Electronic): 1532-2971

Publication date PMC-release: 1 June 2017

Publication date (Print): June 2017

Volume: 224

Pages: 18-24

Affiliations

[a ]Institute of Infection and Global Health, University of Liverpool, Leahurst Campus, Chester High Road, Neston, CH64 7TE, United Kingdom

[b ]National Institute for Health Research, Health Protection Research Unit in Emerging and Zoonotic Infections, The Farr Institute @ HeRC, University of Liverpool, Waterhouse Building, Liverpool, L69 3GL, United Kingdom

[c ]Institute of Veterinary Science, University of Liverpool, Leahurst Campus, Chester High Road, Neston, CH64 7TE, United Kingdom

Author notes

[* ]Corresponding author. D.A.Singleton@ 123456liverpool.ac.uk

[1]

Winner of the 2016 Postgraduate Student Inspiration Award presented by the UK Kennel Club.

Article

Publisher ID: S1090-0233(17)30072-2

DOI: 10.1016/j.tvjl.2017.03.010

PMC ID: 5518771

PubMed ID: 28697871

SO-VID: 9313eda1-035f-4c4f-818f-1e3a2b33cb6a

License:

This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

Patterns of antimicrobial agent prescription in a sentinel population of canine and feline veterinary practices in the United Kingdom

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Most cited references 18

Possible Transmission of mcr-1–Harboring Escherichia coli between Companion Animals and Human

Characterisation of antimicrobial usage in cats and dogs attending UK primary care companion animal veterinary practices.

Qualitative study of factors associated with antimicrobial usage in seven small animal veterinary practices in the UK.

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