Antimicrobial Usage and Resistance in Companion Animals: A Cross-Sectional Study in Three European Countries

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Abstract

Companion animals have been described as potential reservoirs of antimicrobial resistance (AMR), however data remain scarce. Therefore, the objectives were to describe antimicrobial usage (AMU) in dogs and cats in three European countries (Belgium, Italy, and The Netherlands) and to investigate phenotypic AMR. A questionnaire and one fecal sample per animal ( n = 303) were collected over one year and AMU was quantified using treatment incidence (TI). Phenotypic resistance profiles of 282 Escherichia coli isolates were determined. Nineteen percent of the animals received at least one antimicrobial treatment six months preceding sampling. On average, cats and dogs were treated with a standard daily dose of antimicrobials for 1.8 and 3.3 days over one year, respectively. The most frequently used antimicrobial was amoxicillin-clavulanate (27%). Broad-spectrum antimicrobials and critically important antimicrobials for human medicine represented 83% and 71% of the total number of treatments, respectively. Resistance of E. coli to at least one antimicrobial agent was found in 27% of the isolates. The most common resistance was to ampicillin (18%). Thirteen percent was identified as multidrug resistant isolates. No association between AMU and AMR was found in the investigated samples. The issue to address, regarding AMU in companion animal, lies within the quality of use, not the quantity. Especially from a One-Health perspective, companion animals might be a source of transmission of resistance genes and/or resistant bacteria to humans.

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Epidemiology of resistance to antibiotics. Links between animals and humans.

A. van den Bogaard (2000)

An inevitable side effect of the use of antibiotics is the emergence and dissemination of resistant bacteria. Most retrospective and prospective studies show that after the introduction of an antibiotic not only the level of resistance of pathogenic bacteria, but also of commensal bacteria increases. Commensal bacteria constitute a reservior of resistance genes for (potentially) pathogenic bacteria. Their level of resistance is considered to be a good indicator for selection pressure by antibiotic use and for resistance problems to be expected in pathogens. Resistant commensal bacteria of food animals might contaminate, like zoonotic bacteria, meat (products) and so reach the intestinal tract of humans. Monitoring the prevalence of resistance in indicator bacteria such as faecal Escherichia coli and enterococci in different populations, animals, patients and healthy humans, makes it feasible to compare the prevalence of resistance and to detect transfer of resistant bacteria or resistance genes from animals to humans and vice versa. Only in countries that use or used avoparcin (a glycopeptide antibiotic, like vancomycin) as antimicrobial growth promoter (AMGP), is vancomycin resistance common in intestinal enterococci, not only in exposed animals, but also in the human population outside hospitals. Resistance genes against antibiotics, that are or have only been used in animals, i.e. nourseothricin, apramycin etc. were found soon after their introduction, not only in animal bacteria but also in the commensal flora of humans, in zoonotic pathogens like salmonellae, but also in strictly human pathogens, like shigellae. This makes it clear that not only clonal spread of resistant strains occurs, but also transfer of resistance genes between human and animal bacteria. Moreover, since the EU ban of avoparcin, a significant decrease has been observed in several European countries in the prevalence of vancomycin resistant enterococci in meat (products), in faecal samples of food animals and healthy humans, which underlines the role of antimicrobial usage in food animals in the selection of bacterial resistance and the transport of these resistances via the food chain to humans. To safeguard public health, the selection and dissemination of resistant bacteria from animals should be controlled. This can only be achieved by reducing the amounts of antibiotics used in animals. Discontinuing the practice of routinely adding AMGP to animal feeds would reduce the amounts of antibiotics used for animals in the EU by a minimum of 30% and in some member states even by 50%.

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Pet animals as reservoirs of antimicrobial-resistant bacteria.

Stefan Schwarz, David H. Lloyd, Luca Guardabassi (2004)

Pet animal numbers have substantially increased in modern society and attention is increasingly devoted to pet welfare. Because of these changes, antimicrobial agents are frequently used in small animal veterinary practice, often including antimicrobial preparations used in human medicine, with heavy use of broad-spectrum agents such as aminopenicillins plus clavulanic acid, cephalosporins and fluoroquinolones. Several longitudinal studies conducted at veterinary hospitals have indicated that resistance to various antimicrobial agents has emerged amongst pet animal isolates of Staphylococcus intermedius, Escherichia coli and other bacteria, including species with a potential for zoonotic transmission and resistance phenotypes of clinical interest, such as methicillin-resistant Staphylococcus aureus, vancomycin-resistant enterococci and multidrug-resistant Salmonella Typhimurium DT104. Based on a review of the current literature, the role of pets in the dissemination of antimicrobial resistance has been given little attention when compared with that of food animals. A marked contrast is evident between the current policies on antimicrobial usage in food and companion animals. Apart from a few countries where limited data on antimicrobial usage and occurrence of resistance in bacteria from pet animals are provided, national surveillance programmes only focus on food animals. However, data on pet animals are clearly needed for guiding antimicrobial use policy in small animal veterinary practice as well as for assessing the risk of transmission of antimicrobial resistance to humans.

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The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2017

(2019)

Abstract The data on antimicrobial resistance in zoonotic and indicator bacteria in 2017, submitted by 28 EU Member States (MSs), were jointly analysed by EFSA and ECDC. Resistance in zoonotic Salmonella and Campylobacter from humans, animals and food, and resistance in indicator Escherichia coli as well as meticillin‐resistant Staphylococcus aureus in animals and food were addressed, and temporal trends assessed. ‘Microbiological’ resistance was assessed using epidemiological cut‐off (ECOFF) values; for some countries, qualitative data on human isolates were interpreted in a way which corresponds closely to the ECOFF‐defined ‘microbiological’ resistance. In Salmonella from humans, as well as in Salmonella and E. coli isolates from fattening pigs and calves of less than 1 year of age, high proportions of isolates were resistant to ampicillin, sulfonamides and tetracyclines, whereas resistance to third‐generation cephalosporins was uncommon. Varying occurrence/prevalence rates of presumptive extended‐spectrum beta‐lactamase (ESBL)/AmpC producers in Salmonella and E. coli monitored in meat (pork and beef), fattening pigs and calves, and Salmonella monitored in humans, were observed between countries. Carbapenemase‐producing E. coli were detected in one single sample from fattening pigs in one MS. Resistance to colistin was observed at low levels in Salmonella and E. coli from fattening pigs and calves and meat thereof and in Salmonella from humans. In Campylobacter from humans, high to extremely high proportions of isolates were resistant to ciprofloxacin and tetracyclines, particularly in Campylobacter coli. In five countries, high to very high proportions of C. coli from humans were resistant also to erythromycin, leaving few options for treatment of severe Campylobacter infections. High resistance to ciprofloxacin and tetracyclines was observed in C. coli isolates from fattening pigs, whereas much lower levels were recorded for erythromycin. Combined resistance to critically important antimicrobials in both human and animal isolates was generally uncommon but very high to extremely high multidrug resistance levels were observed in S. Typhimurium and its monophasic variant in both humans and animals. S. Kentucky from humans exhibited high‐level resistance to ciprofloxacin, in addition to a high prevalence of ESBL.

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Journal

Journal ID (nlm-ta): Antibiotics (Basel)

Journal ID (iso-abbrev): Antibiotics (Basel)

Journal ID (publisher-id): antibiotics

Title: Antibiotics

Publisher: MDPI

ISSN (Electronic): 2079-6382

Publication date (Electronic): 16 February 2020

Publication date Collection: February 2020

Volume: 9

Issue: 2

Electronic Location Identifier: 87

Affiliations

[1 ]Veterinary Epidemiology Unit, Department of Obstetrics, Reproduction and Herd Health, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium; evelienodent@ 123456gmail.com (E.O.); s.sarrazin@ 123456lammerant.be (S.S.); jeroen.dewulf@ 123456ugent.be (J.D.)

[2 ]Department of Bacteriology and Epidemiology, Wageningen Bioveterinary Research, Houtribweg 39, 8221 RA Lelystad, The Netherlands; daniela.ceccarelli@ 123456wur.nl (D.C.); J.Wagenaar@ 123456uu.nl (J.A.W.); D.J.Mevius@ 123456uu.nl (D.M.)

[3 ]Department of Infectious Diseases and Immunology, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1, 3584 CL Utrecht, The Netherlands; haitskegraveland@ 123456hotmail.com

[4 ]Institute for Risk Assessment Sciences, Utrecht University, Yalelaan 2, 3584 CM Utrecht, The Netherlands; L.VanGompel@ 123456uu.nl

[5 ]Istituto Zooprofilattico Sperimentale del Lazio e della Toscana “M. Aleandri”, Department of General Diagnostics, National Reference Laboratory for Antimicrobial Resistance, Via Appia Nuova, 1411, 00178 Rome, Italy; antonio.battisti@ 123456izslt.it (A.B.); alessia.franco@ 123456izslt.it (A.F.)

Author notes

[* ]Correspondence: philip.joosten@ 123456ugent.be ; Tel.: +32-(0)-92647548

[†]

Current address: Research Executive Agency, European Commission, Brussels, Belgium.

Author information

Philip Joosten https://orcid.org/0000-0003-2948-8954

Antonio Battisti https://orcid.org/0000-0003-1308-199X

Jeroen Dewulf https://orcid.org/0000-0001-9843-5990

Article

Publisher ID: antibiotics-09-00087

DOI: 10.3390/antibiotics9020087

PMC ID: 7175148

PubMed ID: 32079072

SO-VID: 8e35ad31-9013-4d78-a06b-92e77f4055fd

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Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

Antimicrobial Usage and Resistance in Companion Animals: A Cross-Sectional Study in Three European Countries

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Point-Of-Care Testing for AMR

Most cited references 57

Epidemiology of resistance to antibiotics. Links between animals and humans.

Pet animals as reservoirs of antimicrobial-resistant bacteria.

The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2017

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