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      Zoonotic multidrug-resistant microorganisms among small companion animals in Germany

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          Abstract

          Antimicrobial multidrug-resistant microorganisms (MDRO) can be transmitted between companion animals and their human owners. Aim of this study was to determine the prevalence of extended spectrum beta-lactamase-producing Enterobacteriaceae (ESBL-E) and Staphylococcus aureus including methicillin-resistant S. aureus (MRSA) in different companion animal species. Dogs (n = 192), cats (n = 74), and rabbits (n = 17), treated in a veterinary practice and hospital or living in an animal shelter and private households, were sampled. All facilities were located in a region characterized by a high density of pig production. Nasal, buccal and perianal swabs were enriched and cultured on solid chromogenic selective media. A subgroup of 20 animals (13 dogs, 3 cats, 4 rabbits) was analyzed for the presence of staphylococci other than S. aureus. Amongst all animals (n = 283), twenty dogs (10.4%) and six cats (8.1%) carried S. aureus. MRSA was found in five dogs (2.6%) and two cats (2.7%). Isolates were of spa types t011, t034, t108 (all mecA-positive, ST398), and t843 ( mecC-positive, ST130), typical for livestock-associated (LA)-MRSA. Except for one dog, MRSA-positive animals did not have direct contact to husbandry. ESBL- Escherichia coli ( bla CTX-M/ bla TEM/ bla SHV genes) were present in seven dogs (3.6%), one cat (1.4%) possessed a cefotaxime-resistant Citrobacter freundii isolate (bla TEM/ bla CMY-2 genes). MDRO carriage was associated with animals from veterinary medical settings (p<0.05). One dog and one rabbit carried methicillin-resistant coagulase-negative staphylococci. The exclusive occurrence of MRSA lineages typically described for livestock stresses the impact of MDRO strain dissemination across species barriers in regional settings. Presence of ESBL-E and LA-MRSA among pets and probable dissemination in clinical settings support the necessity of a “One Health” approach to address the potential threats due to MDRO-carrying companion animals.

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          Coagulase-negative staphylococci.

          Karsten Becker, Christine Heilmann, Georg Peters (2014)
          The definition of the heterogeneous group of coagulase-negative staphylococci (CoNS) is still based on diagnostic procedures that fulfill the clinical need to differentiate between Staphylococcus aureus and those staphylococci classified historically as being less or nonpathogenic. Due to patient- and procedure-related changes, CoNS now represent one of the major nosocomial pathogens, with S. epidermidis and S. haemolyticus being the most significant species. They account substantially for foreign body-related infections and infections in preterm newborns. While S. saprophyticus has been associated with acute urethritis, S. lugdunensis has a unique status, in some aspects resembling S. aureus in causing infectious endocarditis. In addition to CoNS found as food-associated saprophytes, many other CoNS species colonize the skin and mucous membranes of humans and animals and are less frequently involved in clinically manifested infections. This blurred gradation in terms of pathogenicity is reflected by species- and strain-specific virulence factors and the development of different host-defending strategies. Clearly, CoNS possess fewer virulence properties than S. aureus, with a respectively different disease spectrum. In this regard, host susceptibility is much more important. Therapeutically, CoNS are challenging due to the large proportion of methicillin-resistant strains and increasing numbers of isolates with less susceptibility to glycopeptides.
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            CTX-M Enzymes: Origin and Diffusion

            Rafael Cantón, José-María González-Alba, Juan Carlos Galán … (2012)
            CTX-M β-lactamases are considered a paradigm in the evolution of a resistance mechanism. Incorporation of different chromosomal bla CTX-M related genes from different species of Kluyvera has derived in different CTX-M clusters. In silico analyses have shown that this event has occurred at least nine times; in CTX-M-1 cluster (3), CTX-M-2 and CTX-M-9 clusters (2 each), and CTX-M-8 and CTX-M-25 clusters (1 each). This has been mainly produced by the participation of genetic mobilization units such as insertion sequences (ISEcp1 or ISCR1) and the later incorporation in hierarchical structures associated with multifaceted genetic structures including complex class 1 integrons and transposons. The capture of these bla CTX-M genes from the environment by highly mobilizable structures could have been a random event. Moreover, after incorporation within these structures, β-lactam selective force such as that exerted by cefotaxime and ceftazidime has fueled mutational events underscoring diversification of different clusters. Nevertheless, more variants of CTX-M enzymes, including those not inhibited by β-lactamase inhibitors such as clavulanic acid (IR-CTX-M variants), only obtained under in in vitro experiments, are still waiting to emerge in the clinical setting. Penetration and the later global spread of CTX-M producing organisms have been produced with the participation of the so-called “epidemic resistance plasmids” often carried in multi-drug resistant and virulent high-risk clones. All these facts but also the incorporation and co-selection of emerging resistance determinants within CTX-M producing bacteria, such as those encoding carbapenemases, depict the currently complex pandemic scenario of multi-drug resistant isolates.
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              From “one medicine” to “one health” and systemic approaches to health and well-being☆

              J. Zinsstag, E. Schelling, D Waltner-Toews … (2011)
              Faced with complex patterns of global change, the inextricable interconnection of humans, pet animals, livestock and wildlife and their social and ecological environment is evident and requires integrated approaches to human and animal health and their respective social and environmental contexts. The history of integrative thinking of human and animal health is briefly reviewed from early historical times, to the foundation of universities in Europe, up to the beginning of comparative medicine at the end of the 19th century. In the 20th century, Calvin Schwabe coined the concept of “one medicine”. It recognises that there is no difference of paradigm between human and veterinary medicine and both disciplines can contribute to the development of each other. Considering a broader approach to health and well-being of societies, the original concept of “one medicine” was extended to “one health” through practical implementations and careful validations in different settings. Given the global health thinking in recent decades, ecosystem approaches to health have emerged. Based on complex ecological thinking that goes beyond humans and animals, these approaches consider inextricable linkages between ecosystems and health, known as “ecosystem health”. Despite these integrative conceptual and methodological developments, large portions of human and animal health thinking and actions still remain in separate disciplinary silos. Evidence for added value of a coherent application of “one health” compared to separated sectorial thinking is, however, now growing. Integrative thinking is increasingly being considered in academic curricula, clinical practice, ministries of health and livestock/agriculture and international organizations. Challenges remain, focusing around key questions such as how does “one health” evolve and what are the elements of a modern theory of health? The close interdependence of humans and animals in their social and ecological context relates to the concept of “human-environmental systems”, also called “social-ecological systems”. The theory and practice of understanding and managing human activities in the context of social-ecological systems has been well-developed by members of The Resilience Alliance and was used extensively in the Millennium Ecosystem Assessment, including its work on human well-being outcomes. This in turn entails systems theory applied to human and animal health. Examples of successful systems approaches to public health show unexpected results. Analogous to “systems biology” which focuses mostly on the interplay of proteins and molecules at a sub-cellular level, a systemic approach to health in social-ecological systems (HSES) is an inter- and trans-disciplinary study of complex interactions in all health-related fields. HSES moves beyond “one health” and “eco-health”, expecting to identify emerging properties and determinants of health that may arise from a systemic view ranging across scales from molecules to the ecological and socio-cultural context, as well from the comparison with different disease endemicities and health systems structures.
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                Author and article information

                Contributors
                Ursula Kaspar: Role: Data curationRole: Formal analysisRole: MethodologyRole: SupervisionRole: ValidationRole: Writing – original draft
                Alexa von Lützau: Role: Data curationRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Andreas Schlattmann: Role: InvestigationRole: MethodologyRole: Writing – original draft
                Uwe Roesler: Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing – review & editing
                Robin Köck: Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing – review & editing
                Karsten Becker:
                ORCID: http://orcid.org/0000-0002-6391-1341
                Role: ConceptualizationRole: Funding acquisitionRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Alex Friedrich: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS ONE
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, CA USA )
                ISSN (Electronic): 1932-6203
                Publication date (Electronic): 7 December 2018
                Publication date Collection: 2018
                Volume: 13
                Issue: 12
                Electronic Location Identifier: e0208364
                Affiliations
                [1 ] Institute of Medical Microbiology, University Hospital Münster, Münster, Germany
                [2 ] Institute for Animal Hygiene and Environmental Health, FU Berlin, Department of Veterinary Medicine, Berlin, Germany
                University Medical Center Groningen, NETHERLANDS
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                [¤]

                Current address: Institute of Hygiene, DRK Kliniken Berlin, Berlin, Germany

                Author information
                http://orcid.org/0000-0002-6391-1341
                Article
                Publisher ID: PONE-D-18-27339
                DOI: 10.1371/journal.pone.0208364
                PMC ID: 6285998
                PubMed ID: 30532196
                SO-VID: 5447d5b5-b0ca-47a1-bc8d-708946148f7f
                Copyright © © 2018 Kaspar et al
                License:

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                Date received : 1 October 2018
                Date accepted : 15 November 2018
                Page count
                Figures: 1, Tables: 3, Pages: 15
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100002347, Bundesministerium für Bildung und Forschung;
                Award ID: 01KI1301A
                Award Recipient :
                ORCID: http://orcid.org/0000-0002-6391-1341
                Funded by: Bundesministerium für Bildung und Forschung (DE)
                Award ID: 01KI1301A
                Award Recipient :
                Funded by: Bundesministerium für Bildung und Forschung (DE)
                Award ID: 01Kl1013C
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100002347, Bundesministerium für Bildung und Forschung;
                Award ID: 01KI1727A
                Award Recipient :
                ORCID: http://orcid.org/0000-0002-6391-1341
                Funded by: funder-id http://dx.doi.org/10.13039/501100002347, Bundesministerium für Bildung und Forschung;
                Award ID: 01KI1727A
                Award Recipient :
                Funded by: Bundesinstitut für Risikobewertung (DE)
                Award ID: 1329-557
                Award Recipient :
                ORCID: http://orcid.org/0000-0002-6391-1341
                This work was supported in part by the German Federal Ministry for Education and Research (BMBF) within the research consortia MedVet-Staph (grant no. 01KI1301A to KB and RK), RESET (grant no. 01Kl1013C to UR) and the Research Network Zoonotic Infectious Diseases (project #1Health-PREVENT, grant no. 01KI1727A to KB and RK) and in part by the Bundesinstitut für Risikobewertung (BfR) (grant no. 1329-557 to KB). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Subject: Research Article
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Eukaryota
                Subject: Animals
                Subject: Vertebrates
                Subject: Amniotes
                Subject: Mammals
                Subject: Dogs
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Eukaryota
                Subject: Animals
                Subject: Vertebrates
                Subject: Amniotes
                Subject: Mammals
                Subject: Cats
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Eukaryota
                Subject: Animals
                Subject: Animal Types
                Subject: Pets and Companion Animals
                Subject: Biology and Life Sciences
                Subject: Zoology
                Subject: Animal Types
                Subject: Pets and Companion Animals
                Subject: Biology and life sciences
                Subject: Organisms
                Subject: Bacteria
                Subject: Staphylococcus
                Subject: Staphylococcus aureus
                Subject: Methicillin-resistant Staphylococcus aureus
                Subject: Biology and life sciences
                Subject: Microbiology
                Subject: Medical microbiology
                Subject: Microbial pathogens
                Subject: Bacterial pathogens
                Subject: Staphylococcus
                Subject: Staphylococcus aureus
                Subject: Methicillin-resistant Staphylococcus aureus
                Subject: Medicine and health sciences
                Subject: Pathology and laboratory medicine
                Subject: Pathogens
                Subject: Microbial pathogens
                Subject: Bacterial pathogens
                Subject: Staphylococcus
                Subject: Staphylococcus aureus
                Subject: Methicillin-resistant Staphylococcus aureus
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Bacteria
                Subject: Staphylococcus
                Subject: Staphylococcus Aureus
                Subject: Biology and Life Sciences
                Subject: Microbiology
                Subject: Medical Microbiology
                Subject: Microbial Pathogens
                Subject: Bacterial Pathogens
                Subject: Staphylococcus
                Subject: Staphylococcus Aureus
                Subject: Medicine and Health Sciences
                Subject: Pathology and Laboratory Medicine
                Subject: Pathogens
                Subject: Microbial Pathogens
                Subject: Bacterial Pathogens
                Subject: Staphylococcus
                Subject: Staphylococcus Aureus
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Eukaryota
                Subject: Animals
                Subject: Vertebrates
                Subject: Amniotes
                Subject: Mammals
                Subject: Leporids
                Subject: Rabbits
                Subject: Research and Analysis Methods
                Subject: Animal Studies
                Subject: Experimental Organism Systems
                Subject: Animal Models
                Subject: Rabbits
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Bacteria
                Subject: Staphylococcus
                Subject: Biology and Life Sciences
                Subject: Microbiology
                Subject: Medical Microbiology
                Subject: Microbial Pathogens
                Subject: Bacterial Pathogens
                Subject: Staphylococcus
                Subject: Medicine and Health Sciences
                Subject: Pathology and Laboratory Medicine
                Subject: Pathogens
                Subject: Microbial Pathogens
                Subject: Bacterial Pathogens
                Subject: Staphylococcus
                Subject: Biology and Life Sciences
                Subject: Veterinary Science
                Subject: Veterinary Medicine
                Subject: Veterinary Surgery
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                Data Availability All relevant data are within the manuscript.

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