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      Poor infection prevention and control standards are associated with environmental contamination with carbapenemase-producing Enterobacterales and other multidrug-resistant bacteria in Swiss companion animal clinics

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          Abstract

          Background

          Intensive medical care in companion animal clinics could pose a risk for the selection and dissemination of multidrug-resistant organisms (MDROs). Infection prevention and control (IPC) concepts are key measures to reduce the spread of MDROs, but data on IPC standards in companion animal clinics is sparse. The study assessed IPC standards in seven companion animal clinics and practices in Switzerland by structured IPC audits and combined results with environmental MDRO contamination and MDRO carriage of the personnel.

          Methods

          IPC audits were held between August 2018 and January 2019. The observations in 34 IPC areas were scored based on predefined criteria (not fulfilled/partially fulfilled/fulfilled = score 0/1/2). Environmental swabs and nasal and stool samples from veterinary personnel were tested for methicillin-resistant (MR) staphylococci and macrococci and for colistin-resistant, extended-spectrum β-lactamase- and carbapenemase-producing (CP) Enterobacterales (CPE). Species was identified by MALDI-TOF MS, antimicrobial resistance determined by microdilution and β-lactam resistance gene detection, and genetic relatedness assessed by REP−/ERIC-PCR and multilocus sequence typing.

          Results

          Of a maximum total IPC score of 68, the institutions reached a median (range) score of 33 (19–55). MDROs were detected in median (range) 8.2% (0–33.3%) of the sampling sites. Clinics with low IPC standards showed extensive environmental contamination, i.e. of intensive care units, consultation rooms and utensils. CPE were detected in two clinics; one of them showed extensive contamination with CP Klebsiella pneumoniae (ST11, bla OXA-48) and MR Staphylococcus pseudintermedius (ST551, mecA). Despite low IPC scores, environmental contamination with MDROs was low in primary opinion practices. Three employees were colonized with Escherichia coli ST131 ( bla CTX-M-15, bla CTX-M-27, bla CTX-M-14). Two employees carried CP E. coli closely related to environmental (ST410, bla OXA-181) and patient-derived isolates (ST167, bla NDM-5). MR Staphylococcus aureus (ST225, mecA) and MR S. pseudintermedius (ST551, mecA) of the same sequence types and with similar resistance profiles were found in employees and the environment in two clinics.

          Conclusions

          The study indicates that IPC standards in companion animal clinics are variable and that insufficient IPC standards could contribute to the evolution of MDROs which can be transferred between the environment and working personnel. The implementation of IPC concepts in companion animal clinics should urgently be promoted.

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          Most cited references47

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          Core components for effective infection prevention and control programmes: new WHO evidence-based recommendations

          Health care-associated infections (HAI) are a major public health problem with a significant impact on morbidity, mortality and quality of life. They represent also an important economic burden to health systems worldwide. However, a large proportion of HAI are preventable through effective infection prevention and control (IPC) measures. Improvements in IPC at the national and facility level are critical for the successful containment of antimicrobial resistance and the prevention of HAI, including outbreaks of highly transmissible diseases through high quality care within the context of universal health coverage. Given the limited availability of IPC evidence-based guidance and standards, the World Health Organization (WHO) decided to prioritize the development of global recommendations on the core components of effective IPC programmes both at the national and acute health care facility level, based on systematic literature reviews and expert consensus. The aim of the guideline development process was to identify the evidence and evaluate its quality, consider patient values and preferences, resource implications, and the feasibility and acceptability of the recommendations. As a result, 11 recommendations and three good practice statements are presented here, including a summary of the supporting evidence, and form the substance of a new WHO IPC guideline. Electronic supplementary material The online version of this article (doi:10.1186/s13756-016-0149-9) contains supplementary material, which is available to authorized users.
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            Pet animals as reservoirs of antimicrobial-resistant bacteria.

            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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              Public health risk of antimicrobial resistance transfer from companion animals.

              Antimicrobials are important tools for the therapy of infectious bacterial diseases in companion animals. Loss of efficacy of antimicrobial substances can seriously compromise animal health and welfare. A need for the development of new antimicrobials for the therapy of multiresistant infections, particularly those caused by Gram-negative bacteria, has been acknowledged in human medicine and a future corresponding need in veterinary medicine is expected. A unique aspect related to antimicrobial resistance and risk of resistance transfer in companion animals is their close contact with humans. This creates opportunities for interspecies transmission of resistant bacteria. Yet, the current knowledge of this field is limited and no risk assessment is performed when approving new veterinary antimicrobials. The objective of this review is to summarize the current knowledge on the use and indications for antimicrobials in companion animals, drug-resistant bacteria of concern among companion animals, risk factors for colonization of companion animals with resistant bacteria and transmission of antimicrobial resistance (bacteria and/or resistance determinants) between animals and humans. The major antimicrobial resistance microbiological hazards originating from companion animals that directly or indirectly may cause adverse health effects in humans are MRSA, methicillin-resistant Staphylococcus pseudintermedius, VRE, ESBL- or carbapenemase-producing Enterobacteriaceae and Gram-negative bacteria. In the face of the previously recognized microbiological hazards, a risk assessment tool could be applied in applications for marketing authorization for medicinal products for companion animals. This would allow the approval of new veterinary medicinal antimicrobials for which risk levels are estimated as acceptable for public health.
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                Author and article information

                Contributors
                bwilli@vetclinics.uzh.ch
                Journal
                Antimicrob Resist Infect Control
                Antimicrob Resist Infect Control
                Antimicrobial Resistance and Infection Control
                BioMed Central (London )
                2047-2994
                23 June 2020
                23 June 2020
                2020
                : 9
                : 93
                Affiliations
                [1 ]GRID grid.7400.3, ISNI 0000 0004 1937 0650, Clinic for Small Animal Internal Medicine, Vetsuisse Faculty, , University of Zurich, ; Zurich, Switzerland
                [2 ]GRID grid.412004.3, ISNI 0000 0004 0478 9977, Division of Infectious Diseases and Hospital Epidemiology, , University and University Hospital of Zurich, ; Zurich, Switzerland
                [3 ]GRID grid.5734.5, ISNI 0000 0001 0726 5157, Institute of Veterinary Bacteriology, , Vetsuisse Faculty, University of Bern, ; Bern, Switzerland
                [4 ]GRID grid.5734.5, ISNI 0000 0001 0726 5157, Division of Small Animal Internal Medicine, Department of Clinical Veterinary Medicine, Vetsuisse Faculty, , University of Bern, ; Bern, Switzerland
                [5 ]GRID grid.5734.5, ISNI 0000 0001 0726 5157, Graduate School of Cellular and Biomedical Sciences, University of Bern, ; Bern, Switzerland
                [6 ]GRID grid.5734.5, ISNI 0000 0001 0726 5157, Small Animal Clinic, Department of Clinical Veterinary Medicine, Vetsuisse Faculty, , University of Bern, ; Bern, Switzerland
                [7 ]GRID grid.5734.5, ISNI 0000 0001 0726 5157, Institute for Infectious Diseases, , Faculty of Medicine, University of Bern, ; Bern, Switzerland
                Author information
                http://orcid.org/0000-0002-8010-1180
                Article
                742
                10.1186/s13756-020-00742-5
                7310346
                32576281
                673926ee-ff28-4e99-b4a4-9f4ece22f1cd
                © The Author(s) 2020

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 15 January 2020
                : 29 May 2020
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100006454, Bundesamt für Lebensmittelsicherheit und Veterinärwesen;
                Award ID: 1.18.10
                Funded by: FundRef http://dx.doi.org/10.13039/501100001711, Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung;
                Award ID: 177378
                Categories
                Research
                Custom metadata
                © The Author(s) 2020

                Infectious disease & Microbiology
                infection prevention and control,small animal clinic,enterobacteriaceae,antimicrobial resistant pathogens,multidrug-resistant pathogens,colonization,zoonosis

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