Assessment of listing and categorisation of animal diseases within the framework of the Animal Health Law (Regulation (EU) No 2016/429): antimicrobial‐resistant Staphylococcus aureus in cattle and horses
2022; Wiley; Volume: 20; Issue: 5 Linguagem: Inglês
10.2903/j.efsa.2022.7312
ISSN1831-4732
AutoresSøren Saxmose Nielsen, Dominique Bicout, Paolo Calistri, Elisabetta Canali, Julian Ashley Drewe, Bruno Garin‐Bastuji, José Luis Gonzales Rojas, Christian Gortázar, Mette Herskin, Virginie Michel, Miguel Ángel Miranda Chueca, Barbara Padalino, Paolo Pasquali, Helen Clare Roberts, Hans Spoolder, Karl Ståhl, Antonio Velarde, Arvo Viltrop, Christoph Winckler, Francesca Baldinelli, Alessandro Broglia, Lisa Kohnle, Julio Álvarez,
Tópico(s)Animal Disease Management and Epidemiology
ResumoEFSA JournalVolume 20, Issue 5 e07312 Scientific OpinionOpen Access Assessment of listing and categorisation of animal diseases within the framework of the Animal Health Law (Regulation (EU) No 2016/429): antimicrobial-resistant Staphylococcus aureus in cattle and horses EFSA Panel on Animal Health and Welfare (AHAW), Corresponding Author EFSA Panel on Animal Health and Welfare (AHAW) [email protected] Correspondence:[email protected]Search for more papers by this authorSøren Saxmose Nielsen, Søren Saxmose NielsenSearch for more papers by this authorDominique Joseph Bicout, Dominique Joseph BicoutSearch for more papers by this authorPaolo Calistri, Paolo CalistriSearch for more papers by this authorElisabetta Canali, Elisabetta CanaliSearch for more papers by this authorJulian Ashley Drewe, Julian Ashley DreweSearch for more papers by this authorBruno Garin-Bastuji, Bruno Garin-BastujiSearch for more papers by this authorJosé Luis Gonzales Rojas, José Luis Gonzales RojasSearch for more papers by this authorChristian Gortázar, Christian GortázarSearch for more papers by this authorMette Herskin, Mette HerskinSearch for more papers by this authorVirginie Michel, Virginie MichelSearch for more papers by this authorMiguel Ángel Miranda Chueca, Miguel Ángel Miranda ChuecaSearch for more papers by this authorBarbara Padalino, Barbara PadalinoSearch for more papers by this authorPaolo Pasquali, Paolo PasqualiSearch for more papers by this authorHelen Clare Roberts, Helen Clare RobertsSearch for more papers by this authorHans Spoolder, Hans SpoolderSearch for more papers by this authorKarl Ståhl, Karl StåhlSearch for more papers by this authorAntonio Velarde, Antonio VelardeSearch for more papers by this authorArvo Viltrop, Arvo ViltropSearch for more papers by this authorChristoph Winckler, Christoph WincklerSearch for more papers by this authorFrancesca Baldinelli, Francesca BaldinelliSearch for more papers by this authorAlessandro Broglia, Alessandro BrogliaSearch for more papers by this authorLisa Kohnle, Lisa KohnleSearch for more papers by this authorJulio Alvarez, Julio AlvarezSearch for more papers by this author EFSA Panel on Animal Health and Welfare (AHAW), Corresponding Author EFSA Panel on Animal Health and Welfare (AHAW) [email protected] Correspondence:[email protected]Search for more papers by this authorSøren Saxmose Nielsen, Søren Saxmose NielsenSearch for more papers by this authorDominique Joseph Bicout, Dominique Joseph BicoutSearch for more papers by this authorPaolo Calistri, Paolo CalistriSearch for more papers by this authorElisabetta Canali, Elisabetta CanaliSearch for more papers by this authorJulian Ashley Drewe, Julian Ashley DreweSearch for more papers by this authorBruno Garin-Bastuji, Bruno Garin-BastujiSearch for more papers by this authorJosé Luis Gonzales Rojas, José Luis Gonzales RojasSearch for more papers by this authorChristian Gortázar, Christian GortázarSearch for more papers by this authorMette Herskin, Mette HerskinSearch for more papers by this authorVirginie Michel, Virginie MichelSearch for more papers by this authorMiguel Ángel Miranda Chueca, Miguel Ángel Miranda ChuecaSearch for more papers by this authorBarbara Padalino, Barbara PadalinoSearch for more papers by this authorPaolo Pasquali, Paolo PasqualiSearch for more papers by this authorHelen Clare Roberts, Helen Clare RobertsSearch for more papers by this authorHans Spoolder, Hans SpoolderSearch for more papers by this authorKarl Ståhl, Karl StåhlSearch for more papers by this authorAntonio Velarde, Antonio VelardeSearch for more papers by this authorArvo Viltrop, Arvo ViltropSearch for more papers by this authorChristoph Winckler, Christoph WincklerSearch for more papers by this authorFrancesca Baldinelli, Francesca BaldinelliSearch for more papers by this authorAlessandro Broglia, Alessandro BrogliaSearch for more papers by this authorLisa Kohnle, Lisa KohnleSearch for more papers by this authorJulio Alvarez, Julio AlvarezSearch for more papers by this author First published: 10 May 2022 https://doi.org/10.2903/j.efsa.2022.7312 Requestor: European Commission Question number: EFSA-Q-2022-00094 Panel members: Søren Saxmose Nielsen, Julio Alvarez, Dominique Joseph Bicout, Paolo Calistri, Elisabetta Canali, Julian Ashley Drewe, Bruno Garin-Bastuji, José Luis Gonzales Rojas, Christian Gortázar, Mette Herskin, Virginie Michel, Miguel Ángel Miranda Chueca, Barbara Padalino, Paolo Pasquali, Helen Clare Roberts, Hans Spoolder, Karl Ståhl, Antonio Velarde, Arvo Viltrop and Christoph Winckler. Declarations of interest: The declarations of interest of all scientific experts active in EFSA's work are available at https://ess.efsa.europa.eu/doi/doiweb/doisearch. Acknowledgments: The AHAW Panel wishes to thank Wannes Vanderhaeghen from AMCRA for conducting the extensive literature review under the contract PO/EFSA/ALPHA/2021/04. The AHAW Panel also wishes to thank Verena Oswaldi from EFSA for the support provided for this scientific output. Adopted: 30 March 2022 AboutSectionsPDF ToolsExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Abstract Staphylococcus aureus (S. aureus) was identified among the most relevant antimicrobial-resistant (AMR) bacteria in the EU for cattle and horses in previous scientific opinions. Thus, it has been assessed according to the criteria of the Animal Health Law (AHL), in particular criteria of Article 7 on disease profile and impacts, Article 5 on its eligibility to be listed, Annex IV for its categorisation according to disease prevention and control rules as in Article 9, and Article 8 for listing animal species related to the bacterium. The assessment has been performed following a methodology previously published. The outcome is the median of the probability ranges provided by the experts, which indicates whether each criterion is fulfilled (lower bound ≥ 66%) or not (upper bound ≤ 33%), or whether there is uncertainty about fulfilment. Reasoning points are reported for criteria with uncertain outcome. According to the assessment here performed, it is uncertain whether AMR S. aureus can be considered eligible to be listed for Union intervention according to Article 5 of the AHL (60–90% probability). According to the criteria in Annex IV, for the purpose of categorisation related to the level of prevention and control as in Article 9 of the AHL, the AHAW Panel concluded that the bacterium does not meet the criteria in Sections 1, 2 and 4 (Categories A, B and D; 1–5%, 5–10% and 10–33% probability of meeting the criteria, respectively) and the AHAW Panel was uncertain whether it meets the criteria in Sections 3 and 5 (Categories C and E, 33–90% and 60–90% probability of meeting the criteria, respectively). The animal species to be listed for AMR S. aureus according to Article 8 criteria include mainly mammals, birds, reptiles and fish. 1 Introduction The European Food Safety Authority (EFSA) received a mandate from the European Commission to investigate the global state of play as regards antimicrobial-resistant (AMR) animal pathogens that cause transmissible animal diseases (Term of Reference (ToR) 1), to identify the most relevant AMR bacteria in the European Union (EU) (first part of ToR 2), to summarise the existing or potential animal health impact of those identified bacteria in the EU (second part of ToR 2) and to perform the assessment of those bacteria to be listed and categorised according to the criteria in Article 5, Annex IV according to Article 9 and Article 8 within the Regulation (EU) No 2016/4291 on transmissible animal diseases ('Animal Health Law') (ToR 3). The global state of play for AMR animal pathogens that cause transmissible animal diseases (ToR 1) and the results of the assessment of the most relevant AMR bacteria in the EU (first part of ToR 2) for cattle and horses were published in separate EFSA scientific opinions (EFSA AHAW Panel, 2021a,b). According to the results of the assessment already conducted, Staphylococcus aureus (S. aureus) was identified among the most relevant AMR bacteria in the EU for cattle and horses due to their frequent involvement in a variety of infections in both species (and especially mastitis in the case of cattle) and the high levels of phenotypic resistance to commonly used antimicrobials (particularly β-lactams) found in strains of animal origin. This scientific opinion presents the results of the assessment on AMR S. aureus in cattle and horses on its eligibility to be listed and categorised within the AHL framework. Special focus is placed on the animal health impact of AMR S. aureus in cattle and horses in the EU, which is also summarised here as part of the assessment conducted according to the profile of the infection and its impact on animal welfare (Article 7). Background and Terms of Reference as provided by the requestor The background and ToRs as provided by the European Commission for the present document are reported in Sections 1.1 and 1.2 of the scientific opinion on the ad hoc method to be followed for the assessment of animal diseases caused by bacteria resistant to antimicrobials within the AHL framework (EFSA AHAW Panel, 2021c). Interpretation of the Terms of Reference The interpretation of the ToRs is as in Sections 1.2.3 and 1.3.3 of the scientific opinion on the ad hoc method to be followed for the assessment of animal diseases caused by bacteria resistant to antimicrobials within the AHL framework (EFSA AHAW Panel, 2021c). The present document reports the results of the assessment on AMR S. aureus in cattle and horses according to the criteria of the AHL articles as follows: Article 7: AMR S. aureus infection profile and impacts; Article 5: eligibility of AMR S. aureus infection to be listed; Article 9: categorisation of AMR S. aureus infection according to disease prevention and control rules as in Annex IV; Article 8: list of animal species (also apart from cattle and horses) related to AMR S. aureus infection. 2 Data and methodologies The methodology applied in this opinion is described in detail in a dedicated document about the ad hoc method developed for assessing any animal disease for listing and categorisation of animal diseases within the AHL framework (EFSA AHAW Panel, 2017). In order to take into account the specifics related to animal diseases caused by bacteria resistant to antimicrobials, the term 'disease' as in the AHL was interpreted in a broader sense, referring also to colonisation by commensal and potentially opportunistic bacteria, and the general presence of the identified AMR bacteria in the EU, depending on each criterion. The following assessment was performed by the EFSA Panel on Animal Health and Welfare (AHAW) based on the information collected and compiled in form of a fact sheet as in Section 3.1 of the present document. The outcome is the median of the probability ranges provided by the experts, which are accompanied by verbal interpretations only when they fall within the ranges as spelled out in Table 1. Table 1. Approximate probability scale recommended for harmonised use in EFSA (EFSA Scientific Committee, 2018) Probability term Subjective probability range Almost certain 99–100% Extremely likely 95–99% Very likely 90–95% Likely 66–90% About as likely as not 33–66% Unlikely 10–33% Very unlikely 5–10% Extremely unlikely 1–5% Almost impossible 0–1% 3 Assessment Assessment of AMR Staphylococcus aureus according to Article 7 criteria of the AHL 3.1.1 Article 7(a) Disease profile This fact sheet summarises current knowledge on the presence, importance, control and prevention of AMR S. aureus in cattle and horses. For cattle, the focus of the fact sheet is on resistance against antimicrobials used for dry cow therapy and treatment of mastitis (cefoperazone, oxacillin, neomycin, penicillin, penicillin–novobiocin, pirlimycin) and other infections such as of the respiratory and digestive system, metritis and skin/soft tissue infections (ceftiofur, enro-/ciprofloxacin, erythromycin, sulfa-TMP) (EFSA AHAW Panel, 2021a). For these antimicrobials, geographically varying levels of resistance have been described, predominantly in S. aureus isolates from the udder or milk and with highest levels in Asia and Africa (EFSA AHAW Panel, 2021a). The mecA gene, responsible for methicillin resistance in S. aureus (MRSA), is specifically mentioned. The presence of the mecA gene is considered as conferring resistance to all β-lactam antibiotics, even though heterogeneous and borderline resistance phenotypes exist (Chambers, 1997). Attention is also granted to MRSA carrying the mecC gene, a more recently described variant of the mecA gene (García-Álvarez et al., 2011). Beta-lactam resistance caused by non-mec genes (e.g. due to penicillinases) are mentioned where relevant. For horses, the focus is on S. aureus associated with skin and soft tissue infections (SSTIs) and exhibiting resistance to fusidic acid, methicillin, sulfa-TMP, gentamicin, tetracyclines and enro-/ciprofloxacin (EFSA AHAW Panel, 2021b). S. aureus are Gram-positive, non-motile, facultative anaerobic, typically coagulase-positive cocci that live as commensals on the skin, in the nose and on diverse mucous membranes of humans and animals (Kluytmans et al., 1997; Haag et al., 2019). They behave as opportunistic pathogens causing SSTIs and a range of other infections in virtually all hosts, animals and humans, with in the latter frequent lethal outcomes, especially due to MRSA in, e.g. bacteraemia, endocarditis and pneumonia (Lee et al., 2018). In animals, it is best known as a cause of mastitis in dairy cattle, being one of the major mastitis pathogens (Reyher et al., 2012; Rainard et al., 2018), of SSTI in various animal species, including horses (Devriese et al., 1985; Sieber et al., 2011), and of skin and skeletal disorders in poultry (Heidemann Olsen et al., 2018; Szafraniec et al., 2022). Mastitis is an inflammation of the mammary gland, and in general, the vast majority of mastitis cases are due to an intramammary infection (IMI) caused by a microorganism. The latter starts with the penetration into the mammary gland and proliferation in milk, followed by the dissemination in the cisterns and throughout the duct system, triggering an inflammatory reaction with an influx of leucocytes, leading to elevated somatic cell counts (SCC). The host response may be varied but in S. aureus mastitis typically involves an initial clinical stage with visual clinical signs (swelling, firmness, warmth, tenderness of the udder, clotted milk, elevated body temperature, etc.) that may disappear in a few days with the condition evolving into a subclinical stage, with sometimes more or less intense flare-up episodes (Rainard et al., 2018). In this context, a distinction will be made between infection with (AMR) S. aureus, leading to disease (inflammation) of the infected tissue, hence comprising both clinical and subclinical mastitis in dairy cows and clinical horse SSTI, and (healthy) presence of (AMR) S. aureus, with isolates originating from typical carriage sites such as the nose. Literature on AMR S. aureus in animals, including cattle and horses, in the last two decades is dominated by MRSA. This is due to the emergence of livestock-associated (LA-)MRSA capable of causing human infections (Voss et al., 2005), hence considered a third type of MRSA relevant for human healthcare – along with hospital-associated (HA-)MRSA and community-associated (CA-)MRSA (van Alen et al., 2017; Lee et al., 2018). The general construction of the sections below is that facts about 'LA-MRSA (of clonal complex 398)' in cattle and horses are described first, including other resistances of interest (RoI) for this fact sheet when available. Secondly, facts about (some) 'other MRSA' strains in cattle and horses (including other RoIs when available) are presented. Thirdly, 'non-MRSA' in cattle and horses exhibiting other RoIs are discussed. When S. aureus is mentioned in general, results are described not linked to particular resistant strains. 3.1.1.1 Article 7(a)(i) Animal species concerned by the disease It is accepted that S. aureus shows host specificity; this was originally based on phenotypic traits and has since been confirmed with molecular data (Fitzgerald, 2012; Haag et al., 2019). Host adaptation might occur frequently and quickly, in various lineages and to several host species, including cattle and horses (Lowder et al., 2009; Spoor et al., 2013; Akkou et al., 2018; Grunert et al., 2018; Magro et al., 2018; Wang et al., 2018). Cattle is considered a major exchange host with humans (Haag et al., 2019). Yet, contamination and spill-over events from other hosts also occur commonly (Boss et al., 2016). From the multitude of recent studies offering typing results, the enormous diversity of S. aureus strains and complexity of S. aureus lineages become more and more apparent (Boss et al., 2016), but actual host adaptation is not always investigated. Moreover, many studies do not conclude on the type of non-infection related presence (contamination, intermittent carriage or true colonisation) the isolation of (AMR) S. aureus in animals implies (Magro et al., 2018). Hence, isolation of S. aureus from an animal provides, as such, little evidence about the degree to which the animal species is affected by it (e.g. whether it can be considered a reservoir or a natural host species). Furthermore, it is difficult to say whether all animals apparently 'susceptible' for non-AMR S. aureus (= where S. aureus has been isolated from) are also 'susceptible' to AMR S. aureus or vice versa, and if the isolation of AMR S. aureus pertains to a real reservoir or a temporary presence due to a spill-over event or a selection pressure (e.g. use of antimicrobials). To deal with this complexity, the tables, lists or texts below, pertaining to the subsequent parameters, have been drafted as follows: 'Naturally susceptible' species (wildlife/domestic) include those species where natural (= not experimentally caused) presence of S. aureus – resistant or not – has been demonstrated. This can include isolates from infections or healthy presence. 'Experimentally susceptible' species (wildlife/domestic) include those species where the presence of S. aureus – resistant or not – has been experimentally induced. This can include isolates from infections or healthy presence. The sections on 'reservoir species' (wildlife/domestic) focus on (AMR) S. aureus lineages that have been suggested or shown to be adapted to a certain host species or might be suspected to have a reservoir in a certain species due to frequent detection in that species. A 'wildlife species' has been considered free-living or living in captivity but without being bred for the purpose of living alongside humans (held in zoos or parks, or as exotic pets); 'domestic species' as living in captivity and having been bred for the purpose of living alongside humans. Susceptible animal species Parameter 1 – Naturally susceptible wildlife species (or family/order) S. aureus has been isolated from a huge variety of animal species, ranging from mammals (terrestrial and aquatic) to birds, reptiles, fish and insects. Table 2 lists those species from which S. aureus with one or more RoIs for this fact sheet have been isolated. If available in the referenced study, the Latin name is provided in the table; if not, the common name is given. The mentioned resistances can pertain to different studies or different isolates in one study; no distinction is made between pheno- and genotypic resistance; MRSA might have been determined genotypically (mecA) or phenotypically (oxacillin and/or cefoxitin resistance); mecC is specifically mentioned. The review of Heaton et al. (2020) provides the most extensive summary to date of the presence of (AMR) S. aureus in wildlife, including the species, molecular types and antibiotic resistances identified – if available. When a species (group) was included in any of the referenced studies, it was not systematically investigated whether there could be additional references for the same species or additional species from that group. Table 2. List of wildlife species (groups) where S. aureus with RoIs for this fact sheet has been isolated Species (group) Antimicrobial resistance Reference Mammals Small mammals Hammer-headed bat (Hypsignathus monstrosus) MRSA, TET Loncaric et al. (2019) Indian flying fox (Pteropus giganteus) mecC Heaton et al. (2020) Straw-coloured fruit bat (Eidolon helvum) CIP, CLI, ERY, FUS, PEN, TET Heaton et al. (2020) Black-flanked rock wallaby (Petrogale lateralis) PEN Heaton et al. (2020) Common vole (Microtus arvalis) PEN Heaton et al. (2020) European brown hare (Lepus europaeus) BLA, mecC, MRSA Heaton et al. (2020) European hedgehog (Erinaceus europaeus) CLI, ERY, FUS, GEN, mecC, MRSA, PEN, TET Heaton et al. (2020) European otter (Lutra lutra) BLA, mecC, MRSA Heaton et al. (2020) European pine marten (Martes martes) CLI, ERY, MRSA, TET Heaton et al. (2020) Mara (Dolichotis patagonum) mecC Heaton et al. (2020) Naked mole rat (Heterocephalus glaber) PEN, TET Heaton et al. (2020) Norway/Brown rat (Rattus norvegicus) MRSA, PEN, TET Heaton et al. (2020) Eastern cottontail rabbit (Sylvilagus floridanus) ERY, MRSA, TET Heaton et al. (2020) European rabbit (Oryctolagus cuniculus) mecC, PEN Heaton et al. (2020) Red fox (Vulpes vulpes) MRSA Heaton et al. (2020) Red squirrel (Sciurus vulgaris) PEN, FQ Heaton et al. (2020) Rodents and shrews (various) MRSA Heaton et al. (2020) Wood mouse (Apodemus sylvaticus) mecC, MRSA, PEN Heaton et al. (2020) Large mammals African elephant (Loxodonta africana) MRSA Heaton et al. (2020) Alpine chamois (Rupicapra rupicapra) CIP, FQ, MRSA, PEN Heaton et al. (2020) Fallow deer (Dama dama) mecC, MRSA, PEN Heaton et al. (2020) Red deer (Cervus elaphus) mecC, MRSA, PEN, TET, T/S Heaton et al. (2020) Eurasian lynx (Lynx lynx) BLA, FQ Heaton et al. (2020) Iberian ibex (Capra pyrenaica) MRSA, PEN, TET, T/S Heaton et al. (2020) Wild boar (Sus scrofa) CLI, CIP, ERY, GEN, LIN, mecC, MRSA, PEN, TET, T/S Heaton et al. (2020) Non-human primates/monkeys Chimpanzee (Pan troglodytes) CLI, ERY, MRSA, PEN, TET, T/S Heaton et al. (2020) Gorilla (Gorilla gorilla gorilla) PEN Heaton et al. (2020) Rhesus macaque (Macaca mulatta) CIP, CLI, ERY, GEN, MRSA, PEN, TET, T/S Heaton et al. (2020) Singaporean long-tailed macaque (Macaca fascicularis) CIP, ERY, GEN, KAN, MRSA, PEN, TET Heaton et al. (2020) Southern pig-tailed macaque (Macaca nemestrina) CIP, ERY, GEN, MRSA, PEN, TET Heaton et al. (2020) Red-fronted lemur (Eulemur rufifrons) PEN Heaton et al. (2020) Verraux's sifaka (Propithecus verreauxi) PEN Heaton et al. (2020) Marine mammals Common seal (Phoca vitulina) mecC Paterson et al. (2012) Risso's dolphin (Grampus griseus) MRSA, PEN Mazzariol et al. (2018) Bottlenose dolphin (Tursiops truncatus) MRSA, PEN Mazzariol et al. (2018) Short-finned pilot whale (Globicephala macrorhynchus) MRSA Hower et al. (2013) Walrus (Odobenus rosmarus) MRSA Heaton et al. (2020) Birds Common buzzard (Buteo buteo) PEN, TET Heaton et al. (2020) Common chaffinch (Fringilla coelebs) mecC Paterson et al. (2012) Canada goose (Branta canadensis) CLI, ERY, MRSA, PEN Heaton et al. (2020) Lesser yellowlegs (Tringa flavipes) CLI, ERY, MRSA Heaton et al. (2020) Magpie (Pica pica) MRSA, PEN Heaton et al. (2020) Northern bald ibis (Geronticus eremita) CIP, MRSA, PEN, TET Loncaric et al. (2019) African grey parrot (Psittacus erithacus) FQ, MRSA Rankin et al. (2005) Peregrine (Falco peregrinus) CIP Vidal et al. (2017) Rook (Corvus frugilegus) MRSA Heaton et al. (2020) Rock pigeon (Columba livia) TET Heaton et al. (2020) Screech owl (Megascops spp.) TET Heaton et al. (2020) Cinereous vulture (Aegypius monachus) CLI, ERY, MRSA, PEN, TET Heaton et al. (2020) Eurasian griffon vulture (Gyps fulvus) MRSA, TET Heaton et al. (2020) White-face whistling duck (Dendrocygna viduata) TET Heaton et al. (2020) White stork (Ciconia ciconia) ERY, FUS, mecC, MRSA, PEN, TET Heaton et al. (2020) Reptiles Turtle MRSA Walther et al. (2008) Fish Tilapia (Oreochromis niloticus) MRSA Heaton et al. (2020) Insects House flies (Musca domestica) and stable flies (Stomoxys calcitrans) MRSA Stelder et al. (2021) BLA: β-lactams; CIP: ciprofloxacin; CLI: clindamycin; ERY: erythromycin; FQ: fluoroquinolones; FUS: fusidic acid; GEN: gentamicin; KAN: kanamycin; LIN: lincomycin; MRSA: methicillin-resistant S. aureus with the mecA gene or phenotypic resistance (oxacillin and/or cefoxitin); PEN: penicillin; TET: tetracycline; T/S: trim-sulfa antimicrobials. In addition, the lists below include animal species (groups) from which S. aureus has also been isolated but where either resistances not of interest were found, either no resistances at all were found or resistance data were not determined or unclear from the respective studies. It is hence unclear whether these species are susceptible for AMR S. aureus with RoIs, but they were considered potentially relevant. It must be noted that some of the studies referenced in Heaton et al. (2020) did not determine antimicrobial resistance in species where RoIs had been described in other studies (e.g. in one study penicillin resistance in common vole (Microtus arvalis) was identified, but in another study antimicrobial resistance was not determined in the same species). In those cases, the species is included in Table 2 but is excluded from the lists below. If available in the referenced study, the Latin name is provided; if not, the common name is given. Mammals: Banded mongoose (Mungos mungo) (Heaton et al., 2020); Bats (Nathusius pipistrelle (Pipistrellus nathusii), Egyptian fruit bat (Rousettus aegyptiacus), Peters's dwarf epauletted fruit bat (Micropteropus pusillus)) (Heaton et al., 2020); Black bear (Ursus americanus) (McBurney et al., 2000); Black rhinoceros (Diceros bicornis) (Clausen and Ashford, 1980); Capybara (Hydrochoerus hydrochaeris) (Heaton et al., 2020); Chinchilla (Chinchilla sp.) (Walther et al., 2008); Colobuses (King colobus (Colobus polykomos), Western red colobus (Piliocolobus badius)) (Heaton et al., 2020); Deer (Roe deer (Capreolus capreolus), Silka deer (Cervus nippon)) (Heaton et al., 2020); Dromedary camel (Camelus dromedaries) (Heaton et al., 2020); European badger (Meles meles) (Heaton et al., 2020); European beaver (Castor fiber) (Heaton et al., 2020); European marmot (Marmota marmota) (Heaton et al., 2020); Fox squirrel (Sciurus niger) (Heaton et al., 2020); Gabon talapoin (Miopithecus ogouensis) (Heaton et al., 2020); Grey-cheeked mangabey (Lophocebus albigena) (Heaton et al., 2020); Harbour porpoise (Phocoena phocoena) (Heaton et al., 2020); Killer whale (Orcinus orca) (Power and Murphy, 2002); Lion (Panthera leo) (Heaton et al., 2020); Macaques (Japanese macaque (Macaca fuscata), Barbary macaque (Macaca sylvanus)) (Heaton et al., 2020); Malayan tapir (Tapirus indicus) (Heaton et al., 2020); Mandrill (Mandrillus sp.) (Heaton et al., 2020); Mice (Yellow-necked mouse (Apodemus flavicollis), House mouse (Mus musculus) (Heaton et al., 2020); Mongolian sheep (Ovis ammon f. aries) (Heaton et al., 2020); Monkeys (Greater spot-nose monkey (Cercopithecus nictitans), Red-tailed monkey (Cercopithecus ascanius)) (Heaton et al., 2020); Moose (Alces alces) (Heaton et al., 2020); Mouflons (European mouflon, Mouflon (Ovis orientalis)) (Heaton et al., 2020); Moustached guenon (Cercopithecus cephus) (Heaton et al., 2020); Northern white-breasted hedgehog (Erinaceus roumanicus) (Heaton et al., 2020); Pygmy goat (Capra hircus) (Heaton et al., 2020); Raccoon (Procyon lotor) (Plommet and Wilson, 1969); Reindeer (Rangifer tarandus) (Heaton et al., 2020); Voles (Bank vole (Myodes glareolus), Field vole (Microtus agrestis)) (Heaton et al., 2020); White-eared opossum (Didelphis albiventris) (Siqueira et al., 2010); Wild cats (European wildcat (Felis silvestris), African wildcat (Felis lybica)) (Heaton et al., 2020); Yellow-footed rock wallaby (Petrogale xanthopus) (Heaton et al., 2020). Birds: Bustards (Heaton et al., 2020); Eagles (Golden eagle (Aquila chrysaetos), White-tailed eagle (Haliaeetus albicilla)) (Heaton et al., 2020); Great blue heron (Ardea herodias) (Heaton et al., 2020); Great tit (Parus major) (Heaton et al., 2020); Green woodpecker (Picus viridis) (Heaton et al., 2020); Grey partridge (Perdix perdix) (Heaton et al., 2020); Herring gull (Larus argentatus) (Monecke et al., 2016); Japanese quail (Coturnix coturnix japonica) (Monecke et al., 2016); Red kite (Milvus milvus) (Heaton et al., 2020); Swans (Black swan (Cygnus atratus), Mute swan (Cygnus olor)) (Heaton et al., 2020); Owls (Great horned owl (Bubo virginianus), Tawny owl (Strix aluco)) (Heaton et al., 2020); Teals (Baikal teal (Sibirionetta formosa), Blue-winged teal (Spatula discors)) (Heaton et al., 2020). Reptiles: Komodo dragon (Varanus komodoensis) (Montgomery et al., 2002). From these numerous susceptible animal species, an enormous diversity of molecular types of (
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