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Review

European Wild Carnivores and Antibiotic Resistant Bacteria: A Review

by
Andreia Garcês
1,2,* and
Isabel Pires
3
1
Exotic and Wildlife Service from the Veterinary Hospital University of Trás-os-Montes and Alto Douro, Quinta dos Prados, 4500-801 Vila Real, Portugal
2
Centre for Research and Technology of Agro-Environmental and Biological Sciences, CITAB, Inov4Agro, University of Trás-os-Montes and Alto Douro, UTAD, Quinta de Prados, 5000-801 Vila Real, Portugal
3
Center of Animal and Veterinary Science CECAV University of Trás-os-Montes and Alto Douro, Quinta dos Prados, 4500-801 Vila Real, Portugal
*
Author to whom correspondence should be addressed.
Antibiotics 2023, 12(12), 1725; https://0-doi-org.brum.beds.ac.uk/10.3390/antibiotics12121725
Submission received: 12 November 2023 / Revised: 5 December 2023 / Accepted: 13 December 2023 / Published: 13 December 2023
(This article belongs to the Special Issue Antibiotics Resistance in Animals and the Environment)
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Abstract

:
Antibiotic resistance is a global concern that affects not only human health but also the health of wildlife and the environment. Wildlife can serve as reservoirs for antibiotic-resistant bacteria, and antibiotics in veterinary medicine and agriculture can contribute to the development of resistance in these populations. Several European carnivore species, such as wolves, foxes, otters, and bears, can be exposed to antibiotics by consuming contaminated food, water, or other resources in their habitats. These animals can also be indirectly exposed to antibiotics through interactions with domestic animals and human activities in their environment. Antibiotic resistance in wildlife can harm ecosystem health and also impact human health indirectly through various pathways, including zoonotic disease transmission. Moreover, the spread of resistant bacteria in wildlife can complicate conservation efforts, as it can threaten already endangered species. This review aims to describe the presence of antibiotic-resistant bacteria in wild carnivores in Europe.

1. Introduction

Antimicrobial resistance (AMR) is considered one of the leading public health problems of the 21st century [1]. Although AMR has always existed, the overuse and misuse of antibiotics have increased antibiotic-resistant strains [2]. In recent decades, selective pressure has been generated by the use of antibiotics in medicine, veterinary, and agricultural practices, which has been responsible for a significant increase in antibiotic resistance [3].
“One Health” is a concept wherein human, animal, and environmental health are interconnected [4]. One of the greatest problems with “One Health” is antimicrobial resistance. This problem affects these three groups simultaneously. Humans and domestic and wild animals can be hosts and spreaders of AMR bacteria. Moreover, bacteria are continuously exchanged between the different environmental niches [5,6].
Although most wildlife prefer to live far from humans, some species have adapted and can live in contact with domestic animals or humans in urban environments. Therefore, they can be recognized as potential indicators of AMR dissemination [7]. Wild animals usually do not receive antibiotics or veterinary care, except in cases of interventions in endangered animals, admissions to wildlife rehabilitation centers, or treatments during disease outbreaks [8]. Studies have shown that AMR in most wildlife is associated with environmental exposure to anthropogenic AMR contamination [8]. Air, water, land, and food are some of the sources of AMR [9]. Bodies of water, such as rivers, lakes, or seas, can be contaminated with industrial discharges, agricultural discharges (fecal sludge from farms), domestic sewage, discharges from hospitals (human and veterinary), and wastewater treatment plants, among others [8,10,11]. Fertilizers used in agriculture can be a source of AMR [8]. In addition to environmental pressures, there are intrinsic mechanisms in bacteria that may contribute to the development of antimicrobial resistance, such as bacterial permeability, efflux pumps, target receptor modification, or horizontal gene transfer between bacteria via mobile genetic elements (e.g., plasmids, transposons, integrons) [3,12]. The presence of AMR in wildlife is also associated with other factors, such as habitat use, foraging behavior, and species’ habitats [3,8]. Habitat destruction, the loss of biodiversity, climate change, the accumulation of toxic pollutants, and the invasion of exotic species and pathogens have also contributed to the spread of AMR [13].
Contact between anthropogenic source areas and wild animals has increased due to human expansion. Some animals—for example, foxes and hedgehogs—have adapted and now live and thrive in urban areas [1,14]. Animals in these areas can feed on human domestic waste [15]. These contacts can potentially contribute to the emergence of new pathogens and AMR in wildlife, which can promote higher mortality rates. When animals survive, they can become bacterial reservoirs and spread throughout the environment again [13,16]. A study performed in Botswana showed that the prevalence of AMR Escherichia coli was highest in carnivores (62.5%) and animals using urban habitats (25.6%) when compared to herbivores (9.1%) and animals using protected/rural habitats (9.0%) [8].
Despite the abundance of literature on AMR in the medical and veterinary fields, available studies focus mainly on some bacterial species, such as Escherichia coli or Salmonella spp., and some species of wild animals, mainly birds and mammals [6,7,8]. Carnivores are a very diverse group of species in Europe, with some populations living in remote areas and others in urban areas in close contact with humans [10,15].
This review aims to describe the presence of antibiotic-resistant bacteria in wild carnivores in Europe.

2. European Wild Carnivorous

Carnivora is an order of mammals that eats meat, by predation or necrophagy. They have specialized teeth for their meat-based diet, with fang-like canines, which they use to kill their prey and cut the meat into pieces [17,18]. Some animals in this order can also consume vegetation, insects (omnivores), and meat [17]. Carnivores can be found in diverse habitats, including cold polar regions, desert regions, forests, open seas, and urban areas [19]. The order Carnivora includes 16 families and 9 terrestrial families: Canidae, Felidae, Ursidae, Procyonidae, Mustelidae, Herpestidae, Viverridae, and Hyaenidae.
In Europe, there are approximately 63 species of carnivorous mammals, both terrestrial and marine. Some of these species are threatened according to the IUCN Red List of Threatened Species, such as the Iberian lynx (endangered) or the Balkan lynx (critically endangered) [17]. These include larger predators, such as wolves, bears, and lynxes, and smaller carnivores like foxes, weasels, and mustelids. Historically, throughout the continent, these species have all experienced a dramatic decline in their populations and distributions due to anthropogenic factors (hunting, habitat destruction, pollution) [18,20,21].
In Table 1, we present some information regarding the distribution, conservation status, and diet of some of the carnivorous species included in this review, to understand better the source of the acquisition of AMR strains of bacteria.

3. Antibiotic Resistance in Wild Carnivores

For this review, the inclusion criteria were as follows: studies only performed in free-range animals, species of European terrestrial carnivores, studies conducted in Europe, and studies that included bacteria, phenotypic resistance, and/or resistance genes.
The initial search identified 2578 articles on the databases (ResearchGate, MEDLINE, PubMed, Web of Science, and Google Scholar) using the terms “bacteria”, “antibiotic resistance”, “carnivorous”, “AMR”, “Europe”, “resistance genes”, “European mammals”, “One Health”, and “bioindicator”. On the 2578 articles collected, a first screening was performed based on the information in the abstracts. A total of 2178 were excluded since they did not have the necessary information for the review. From the remaining 400, 65 were duplicates and therefore excluded. Another 235 were excluded due to geography (studies performed outside Europe). Eleven were removed due to language, since only English, Spanish, and Portuguese manuscripts were included in this review. With a secondary exclusion filter screening the full articles, 78 were excluded since they were not performed in wild animals or did not include all the information required, and 9 were not open-access full articles. Therefore, a total of 36 articles had all the information required and were included in this review (Figure 1). Table 2, Table 3, Table 4 and Table 5 is presented the information from the papers selected.

3.1. Species and Spatial Distribution

The main families of carnivores where studies were carried out, in descending order, were as follows: 11.1% (n = 4) Ursidae, 16.6% (n = 6) Felidae, 19.4% (n = 7) Canidae, and 52.7% (n = 19) Mustilidae. The species with the most AMR studies was Vulpes vulpes with 12 studies, followed by Lutra lutra with 11 studies.
The countries where the studies were carried out, in ascending order, were as follows: 41.6% (n = 15) Portugal, 25% (n = 9) Italy, 8.3% (n = 3) Norway, 8.3% (n = 3) Germany, 8.3% (n = 3) Slovakia, 5.5% (n = 2) Ireland, 5.5% (n = 2) Slovenia, 5.5% (n = 2) Poland, 2.7% (n = 1) Austria, 2.7% (n = 1) Sweden, 2.7% (n = 1) United Kingdom. Figure 2 represents the number of studies by carnivorous species in each country included in this review.

3.2. Bacteria, Antibiotic Resistance Pattern, and Resistance Genes

Most of the studies were performed in fecal samples or rectal swabs; therefore, the bacteria isolated mostly were microbiota from the gut microflora (Figure 3).
Regarding phenotype resistance, Figure 4 considers the number of articles that describe, in particular, each type of antibiotic resistance reported in the various Carnivora families: Canidae, Ursidae, Felidae, and Mustelidae. The studies are also summarized in Table 2 and Table 3. Many papers report multi-resistant bacteria. The methodology used in these articles was very similar, using the disk diffusion method (DDM) as antibiotic sensitivity testing. All the terminology was also standardized to be included in this graphic.
Based on the information collected in the different articles regarding the antibiotic resistance phenotype, it was possible to observe that three of the carnivore families—Canidae, Felidae, and Mustilidae—presented high levels of resistance to ampicillin and tetracyclines (Figure 4). In the case of the Ursidae family, it is impossible to extract any valid information due to the limited number of studies, and the resistance pattern is quite similar.

4. Carnivores and Antibiotic Resistance

Antibiotic-resistant bacteria can be acquired by carnivorous species in several ways, mainly through direct and indirect exposure to these resistant strains from anthropogenic sources and domestic animals [10,62]. Normally, these animals are not treated with antibiotic therapy, except in some particular cases in which some individuals are admitted to wild animal rehabilitation centers due to illness or trauma. However, even in these cases, exposure to these agents is brief [64,65]. Major predators can generally travel great distances across the territory for food. They can disperse AMR over large areas, a key element of AMR dynamics in the ecosystem [66].
Some species of animals are natural carriers of AMR bacteria. For example, European hedgehogs (Erinaceus europaeus) are natural carriers of MRSA that have been selected as a response to the presence of b-lactam-producing microorganisms (Trichophyton erinacei) in the microbiome of this animal [67].
The greatest problem is the contamination of the environment with antibiotic resistance determinants and resistance drivers (e.g., antibiotic residues, pesticides, heavy metals) from agriculture, waste disposal, or the disposal of wastewater of human and veterinary origin [8]. The dispersion of these agents in the environment is a public health problem, as it can lead to the emergence and proliferation of pathogens that are difficult or impossible to treat [8,63]. The dispersion of these agents has negative economic and health consequences for humans and animals [68].
Several studies have already been carried out on the presence and impact of antibiotic-resistant bacteria in wildlife across various vertebrates, from birds to reptiles [69,70]. Based on already available data, the prevalence of antibiotic-resistant bacteria depends on multiple factors, such as habitat use, the foraging strategy of the species, behavior, and territory [8].
Unfortunately, not all European carnivore species are represented in this review, as no data are available for some of them [62]. This article’s main limitation is that it does not allow a realistic comparison between different species. This demonstrates that it is necessary to collect more data on other species and in different regions, in the long term, to compare the impact that the use and abuse of antibiotics have on these animals.
Most of the studies included in this review were conducted in Southern and Eastern European countries (Figure 3). This fact may be partly associated with the greater diversity of animals in these regions. However, it is also possible that it is related to the fact that several Southern and Eastern European countries have reported higher levels of antibiotic resistance in livestock, often linked to differences in agricultural practices, regulations, and intensive livestock production. In addition, many of these regions are highly industrialized [71,72].
Concerning the available data, it is possible to observe that most studies were conducted on small mammals (Figure 3), mainly from the Mustilidae family. This may be associated with the fact that large carnivore populations (wolf, bear, wolverine, lynx) have declined in Europe and their numbers are very small [62,73]. Most of these populations are threatened and protected by law [34,52]; therefore, it is necessary to access samples from these individuals to carry out studies [37,74]. In addition to being threatened, some species, such as polar bears, live in very remote areas, difficult to access and with harsh climates [25,50].
One of the most represented species is the red fox (Vulpes vulpes). This may be associated with its omnivorous diet and adaptability to urban centers. Currently, these animals can be easily found in several European cities, feeding on human waste and in close contact with domestic animals [26,42]. Due to this behavior, they can be excellent bioindicators of the presence of AMR in the environment [47,75]. Animals such as foxes, which live close to humans and often depend on their waste for food, are more susceptible to these agents. Similar studies in birds in Southern France detected carbapenem-resistant E. coli isolates in yellow-legged gulls (Larus michahellis) feeding in landfills. However, no isolates were obtained from slender-billed gulls (Chroicocephalus genie) provided from deep-sea fish [76]. Another source of contamination may be the prey of small species, such as rodents or insects, which may represent a link between humans/domestic animals and predators [76]. In the case of flies, these are usually found in contaminated waste and can travel quite a long distance as vectors of AMR bacteria, infecting wild/domestic animals and humans [66]. Moreover, scavenging contaminated carcasses or consuming peridomestic prey may promote exposure to AMR [8].
The most observed species of bacteria were E. coli and Enterococcus spp. (Figure 3) in general in the four families of carnivores. E. coli prevailed in all families except Felidae, where Enterococcus spp. was the most prominent bacterial species. The results were expected since most samples originated from feces or rectal swabs [52,72].
Although the use of antibiotics in livestock farming has been reduced to minimal use under EU regulations [1], sulfamethoxazole, ampicillin, and tetracycline were the primary resistance types reported in livestock animals [77,78]. Tetracycline and ampicillin are also some of the most commonly used antibiotics in human medicine, and resistance to these isolates is frequently reported [79]. In the data collection, almost all carnivore families have resistance to ampicillin, tetracyclines, and sulfonamides. This may be an indication that livestock and humans may be the potential sources of these forms of AMR in wild carnivores.
Some resistant bacteria are more dangerous than others, as in the case of extended-spectrum beta-lactamase (ESBL)-producing bacteria, vancomycin-resistant Enterococci (VRE), and methicillin-resistant Staphylococcus aureus (MRSA) [44,62]. Infections with these bacteria are challenging to treat and can lead to severe complications [62,63]. The presence of ESBL has been reported in Iberian wolves [32,34], red foxes, badgers [58], and European otters [54,56]; VRE in Iberian wolves [36]; and MRSA in European otters and the European lynx [45,57]
The mecA gene is the main genetic determinant responsible for methicillin resistance in Staphylococcus aureus. In the studies presented where MRSA was observed, it was isolated from mecC, which is homologous for mecA [45,57]. Vancomycin resistance in Enterococcus is commonly associated with two genes, vanA and vanB. These genes were isolated in the Iberian wolf [37]. Several genes are associated with ESBL production, such as TEM, SHV, and CTX-M. These genes have been identified in Iberian wolves [32,34], red foxes, badgers [58], and European otters [54,56]. Other important genes are blaCTX-M, blaCMY, tetM, and ermB, also isolated in several species, indicating that bacteria or resistance originated in human or domestic animals [78,79].
The correlation between AMR and the United Nations Sustainable Development Goals (SDGs) is a global health concern and has specific implications for wildlife populations, including carnivores in Europe [80]. As these animals play vital roles in ecosystems, their health is interconnected with the broader environmental and human health goals outlined in the SDGs. In the context of carnivores, AMR can have cascading effects on ecosystems. For example, the use of antibiotics in domestic animals, which is linked to AMR, can indirectly impact carnivores through food chain dynamics [81]. Additionally, the spread of antibiotic-resistant bacteria in the environment, including water bodies, can affect carnivores that rely on these resources. This aligns with SDG 15 (Life on Land) and SDG 14 (Life Below Water), emphasizing the importance of safeguarding terrestrial and aquatic ecosystems. Moreover, the potential transmission of antibiotic-resistant bacteria between wildlife, livestock, and humans underscores the interconnectedness of SDG 3 (Good Health and Well-Being). Efforts to mitigate AMR in carnivores involve understanding and addressing the factors contributing to the spread of resistance, emphasizing the need for interdisciplinary approaches that span the environmental, veterinary, and human health domains. In the broader context of SDG 17 (Partnerships for the Goals), collaboration between environmental scientists, veterinarians, public health experts, and policymakers becomes crucial [80]. Shared knowledge and coordinated efforts are necessary to develop strategies that protect carnivores, ecosystems, and public health from the threats posed by AMR [81]. Addressing AMR in carnivores aligns with the holistic and interconnected approach of the SDGs, recognizing that the health of wildlife is intrinsically linked to broader sustainability and well-being goals for the planet and its inhabitants [82].

5. Conclusions

Studies have shown that AMR can be found in various wildlife populations, including wild mammal carnivores, most likely of anthropogenic origin. This poses a risk to these animals, humans, and other animals that come into contact with them. While predicting the exact future of AMR in wild carnivores is challenging, the issue will likely continue to be a concern if proper measures are not taken to address it. Several studies have identified AMR bacteria and antibiotic resistance genes in wild carnivores, including foxes, raccoons, and wild felids, as it was possible to conclude with this review. Antibiotic resistance in these animals is often linked to anthropogenic activities, environmental contamination, and interactions with human-influenced areas.
The future of AMR in wild carnivores depends on understanding the extent and impact of antibiotic resistance in these populations, which is essential for the development of effective strategies to mitigate its spread. Monitoring the prevalence of antibiotic-resistant bacteria in these populations, studying the mechanisms of resistance, and identifying the sources of antibiotic exposure are crucial measures in addressing this issue. Wild carnivores can be useful bioindicators of AMR in the environment. Moreover, promoting the responsible use of antibiotics in veterinary medicine and agriculture, and implementing measures to reduce environmental contamination with antibiotics, can help to minimize the emergence and spread of antibiotic resistance in wild mammal carnivores and other wildlife populations. Collaboration between wildlife conservationists, veterinarians, and public health experts is essential to develop comprehensive strategies to preserve both animals, especially threatened species, and human health in the face of antibiotic resistance under the “One Health” concept.

Author Contributions

Conceptualization, A.G.; methodology, A.G. and I.P.; software, A.G. and I.P.; validation A.G. and I.P.; formal analysis, A.G. and I.P.; investigation, A.G. and I.P.; resources, A.G. and I.P.; data curation, A.G. and I.P.; writing—original draft preparation, A.G. and I.P.; writing—review and editing, A.G. and I.P.; visualization, A.G. and I.P.; supervision, A.G. and I.P.; project administration, A.G.; funding acquisition, I.P. All authors have read and agreed to the published version of the manuscript.

Funding

The participation of Pires I was supported by the projects UIDB/CVT/00772/2020 and LA/P/0059/2020, funded by the Portuguese Foundation for Science and Technology (FCT) (project UIDB/CVT/0772/2020). The participation of Garcês A. was supported by National Funds from the Portuguese Foundation for Science and Technology (FCT), under project UIDB/04033/2020.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Mo, S.S.; Urdahl, A.M.; Madslien, K.; Sunde, M.; Nesse, L.L.; Slettemeås, J.S.; Norström, M. What Does the Fox Say? Monitoring Antimicrobial Resistance in the Environment Using Wild Red Foxes as an Indicator. PLoS ONE 2018, 13, e0198019. [Google Scholar] [CrossRef] [PubMed]
  2. Costa, D.; Poeta, P.; Sáenz, Y.; Vinué, L.; Coelho, A.C.; Matos, M.; Rojo-Bezares, B.; Rodrigues, J.; Torres, C. Mechanisms of Antibiotic Resistance in Escherichia coli Isolates Recovered from Wild Animals. Microb. Drug Resist. 2008, 14, 71–77. [Google Scholar] [CrossRef] [PubMed]
  3. Sousa, M.; Gonçalves, A.; Silva, N.; Serra, R.; Alcaide, E.; Zorrilla, I.; Torres, C.; Caniça, M.; Igrejas, G.; Poeta, P. Acquired Antibiotic Resistance among Wild Animals: The Case of Iberian Lynx (Lynx pardinus). Vet. Q. 2014, 34, 105–112. [Google Scholar] [CrossRef] [PubMed]
  4. Suárez-Pérez, A.; Corbera, J.A.; González-Martín, M.; Tejedor-Junco, M.T. Multidrug-Resistant Phenotypes of Escherichia coli Isolates in Wild Canarian Egyptian Vultures (Neophron percnopterus majorensis). Animals 2021, 11, 1692. [Google Scholar] [CrossRef]
  5. Baros Jorquera, C.; Moreno-Switt, A.I.; Sallaberry-Pincheira, N.; Munita, J.M.; Flores Navarro, C.; Tardone, R.; González-Rocha, G.; Singer, R.S.; Bueno, I. Antimicrobial Resistance in Wildlife and in the Built Environment in a Wildlife Rehabilitation Center. One Health 2021, 13, 100298. [Google Scholar] [CrossRef] [PubMed]
  6. CDC. One Health. Available online: https://www.who.int/news-room/questions-and-answers/item/one-health (accessed on 11 April 2023).
  7. Smoglica, C.; Di Francesco, C.E.; Angelucci, S.; Antonucci, A.; Innocenti, M.; Marsilio, F. Occurrence of the Tetracycline Resistance Gene tetA(P) in Apennine Wolves (Canis lupus italicus) from Different Human–Wildlife Interfaces. J. Glob. Antimicrob. Resist. 2020, 23, 184–185. [Google Scholar] [CrossRef]
  8. Ramey, A.M.; Ahlstrom, C.A. Antibiotic resistant bacteria in wildlife: Perspectives on trends, acquisition and dissemination, data gaps, and future directions. J. Wildl. Dis. 2019, 56, 1–15. [Google Scholar] [CrossRef]
  9. Sens-Junior, H.; Trindade, W.A.; Oliveira, A.F.; Zaniolo, M.M.; Serenini, G.F.; Araujo-Ceranto, J.B.; Gonçalves, D.D.; Germano, R.M. Bacterial Resistance in Bats from the Phyllostomidae Family and Its Relationship with Unique Health. Pesq. Vet. Bras. 2018, 38, 1207–1216. [Google Scholar] [CrossRef]
  10. Sherley, M.; Gordon, D.M.; Collignon, P.J. Variations in Antibiotic Resistance Profile in Enterobacteriaceae Isolated from Wild Australian Mammals. Env. Microbiol 2000, 2, 620–631. [Google Scholar] [CrossRef] [PubMed]
  11. Gharout-Sait, A.; Touati, A.; Ahmim, M.; Brasme, L.; Guillard, T.; Agsous, A.; de Champs, C. Occurrence of Carbapenemase-Producing Klebsiella pneumoniae in Bat Guano. Microb. Drug Resist. 2019, 25, 1057–1062. [Google Scholar] [CrossRef] [PubMed]
  12. Blanco, G.; Lemus, J.A.; Grande, J.; Gangoso, L.; Grande, J.M.; Donázar, J.A.; Arroyo, B.; Frías, O.; Hiraldo, F. Retracted Geographical Variation in Cloacal Microflora and Bacterial Antibiotic Resistance in a Threatened Avian Scavenger in Relation to Diet and Livestock Farming Practices. Environ. Microbiol. 2007, 9, 1738–1749. [Google Scholar] [CrossRef] [PubMed]
  13. Oliveira, M.; Pedroso, N.; Sales-Luís, T.; Santos-Reis, M.; Tavares, L.; Vilela, C. Evidence of Antimicrobial Resistance in Eurasian Otter (Lutra lutra Linnaeus, 1758) Fecal Bacteria in Portugal. In Wildlife: Destruction, Conservation and Biodiversity; Nova Science Publishers: New York, NY, USA, 2009; pp. 201–221. ISBN 978-1-60692-974-2. [Google Scholar]
  14. Dwi Ash-Santri, A.; Cantya Prakasita, V.; Kristian Adi, Y.; Budipitojo, T.; Endang Tri Hastuti Wahyuni, A. Isolation, Identification, and Antimicrobial Susceptibility Test of Bacteria from Vulva Swab of African Pygmy Hedgehog (Atelerix albiventris) and Sunda Porcupine (Hystrix javanica). BIO Web Conf. 2021, 33, 06009. [Google Scholar] [CrossRef]
  15. Baker, P.J.; Harris, S. Urban Mammals: What Does the Future Hold? An Analysis of the Factors Affecting Patterns of Use of Residential Gardens in Great Britain. Mammal Rev. 2007, 37, 297–315. [Google Scholar] [CrossRef]
  16. Oliveira, M.; Pedroso, N.; Sales-Luís, T.; Santos-Reis, M.; Tavares, L.; Vilela, C. Antimicrobial-Resistant Salmonella Isolated from Eurasian Otters (Lutra Lutra Linnaeus, 1758) in Portugal. J. Wildl. Dis. 2010, 46, 1257–1261. [Google Scholar] [CrossRef]
  17. Bellani, G.G. Chapter 1—Order of Carnivores (Carnivora). In Felines of the World; Bellani, G.G., Ed.; Academic Press: Cambridge, MA, USA, 2020; pp. 1–12. ISBN 978-0-12-816503-4. [Google Scholar]
  18. Clark, T.W.; Curlee, A.P.; Reading, R.P. Crafting Effective Solutions to the Large Carnivore Conservation Problem. Conserv. Biol. 1996, 10, 940–948. [Google Scholar] [CrossRef]
  19. Carnivore-Mammal Classification|Britannica. Available online: https://www.britannica.com/animal/carnivore-mammal (accessed on 31 October 2023).
  20. Farris, Z.J.; Golden, C.D.; Karpanty, S.; Murphy, A.; Stauffer, D.; Ratelolahy, F.; Andrianjakarivelo, V.; Holmes, C.M.; Kelly, M.J. Hunting, Exotic Carnivores, and Habitat Loss: Anthropogenic Effects on a Native Carnivore Community, Madagascar. PLoS ONE 2015, 10, e0136456. [Google Scholar] [CrossRef]
  21. Trouwborst, A. Managing the Carnivore Comeback: International and EU Species Protection Law and the Return of Lynx, Wolf and Bear to Western Europe. J. Environ. Law 2010, 22, 347–372. [Google Scholar] [CrossRef]
  22. Martes foina. Britannica. Available online: https://naturdata.com/especie/ (accessed on 1 November 2023).
  23. Mustela putorius. Britannica. Available online: https://naturdata.com/especie/ (accessed on 1 November 2023).
  24. Dewey, T.; Ballenger, L. Ursus arctos (Brown Bear). Available online: https://animaldiversity.org/accounts/Ursus_arctos/ (accessed on 1 November 2023).
  25. Jirik, K. Polar Bear (Ursus maritimus). Available online: https://ielc.libguides.com/sdzg/factsheets/polarbear/summary (accessed on 1 November 2023).
  26. Letková, V.; Lazar, P.; Čurlík, J.; Goldová, M.; Košuthová, L.; Mojžišová, J. The Red Fox (Vulpes vulpes L.) as a Source of Zoonoses. Vet. Arh. 2006, 76, 73–81. [Google Scholar]
  27. Rafferty, R. Badger. Available online: https://www.britannica.com/animal/badger (accessed on 29 November 2023).
  28. Fusillo, R.; Romanucci, M.; Marcelli, M.; Massimini, M.; Della Salda, L. Health and Mortality Monitoring in Threatened Mammals: A First Post Mortem Study of Otters (Lutra lutra L.) in Italy. Animals 2022, 12, 609. [Google Scholar] [CrossRef]
  29. Canis lupus subsp. italicus Altobello. 1921. Available online: https://www.gbif.org/species/165635864 (accessed on 2 November 2023).
  30. Canis lupus signatus. Britannica. Available online: https://naturdata.com/especie/ (accessed on 2 November 2023).
  31. Lynx pardinus. Britannica. Available online: https://naturdata.com/especie/ (accessed on 2 November 2023).
  32. Ivory, A. Canis aureus (Golden Jackal). Available online: https://animaldiversity.org/accounts/Canis_aureus/ (accessed on 2 November 2023).
  33. Foti, M.; Fisichella, V. Study of the Spread of the Antibiotic Resistance Phenomenon in a Wolf Population (Canis lupus, Linneaus 1758) in the Aspromonte National Park; Iris: San Francisco, CA, USA, 2017. [Google Scholar]
  34. Smoglica, C.; Angelucci, S.; Di Tana, F.; Antonucci, A.; Marsilio, F.; Di Francesco, C. Antibiotic Resistance in the Apennine Wolf (Canis lupus italicus): Implications for Wildlife and Human Health. Antibiotics 2023, 12, 950. [Google Scholar] [CrossRef] [PubMed]
  35. Simões, R.; Ferreira, C.; Gonçalves, J.; Álvares, F.; Rio-Maior, H.; Roque, S.; Brandão, R.; Martins da Costa, P. Occurrence of Virulence Genes in Multidrug-Resistant Escherichia coli Isolates from Iberian Wolves (Canis lupus signatus) in Portugal. Eur. J. Wildl. Res. 2012, 58, 677–684. [Google Scholar] [CrossRef]
  36. Gonçalves, A.; Igrejas, G.; Radhouani, H.; Santos, T.; Monteiro, R.; Pacheco, R.; Alcaide, E.; Zorrilla, I.; Serra, R.; Torres, C.; et al. Detection of Antibiotic Resistant Enterococci and Escherichia coli in Free Range Iberian Lynx (Lynx pardinus). Sci. Total Environ. 2013, 456–457, 115–119. [Google Scholar] [CrossRef] [PubMed]
  37. Gonçalves, A.; Igrejas, G.; Radhouani, H.; López, M.; Guerra, A.; Petrucci-Fonseca, F.; Alcaide, E.; Zorrilla, I.; Serra, R.; Torres, C.; et al. Detection of Vancomycin-Resistant Enterococci from Faecal Samples of Iberian Wolf and Iberian Lynx, Including Enterococcus faecium Strains of CC17 and the New Singleton ST573. Sci. Total Environ. 2011, 410–411, 266–268. [Google Scholar] [CrossRef] [PubMed]
  38. Di Francesco, A.; Salvatore, D.; Gobbi, M.; Morandi, B. Antimicrobial Resistance Genes in a Golden Jackal (Canis aureus L. 1758) from Central Italy. Vet. Res. Commun. 2023, 1–5. [Google Scholar] [CrossRef]
  39. Radhouani, H.; Igrejas, G.; Gonçalves, A.; Pacheco, R.; Monteiro, R.; Sargo, R.; Brito, F.; Torres, C.; Poeta, P. Antimicrobial Resistance and Virulence Genes in Escherichia coli and Enterococci from Red Foxes (Vulpes vulpes). Anaerobe 2013, 23, 82–86. [Google Scholar] [CrossRef] [PubMed]
  40. Radhouani, H.; Igrejas, G.; Carvalho, C.; Pinto, L.; Gonçalves, A.; Lopez, M.; Sargo, R.; Cardoso, L.; Martinho, A.; Rego, V.; et al. Clonal Lineages, Antibiotic Resistance and Virulence Factors in Vancomycin-Resistant Enterococci Isolated from Fecal Samples of Red Foxes (Vulpes vulpes). J. Wildl. Dis. 2011, 47, 769–773. [Google Scholar] [CrossRef] [PubMed]
  41. O’Hagan, M.J.H.; Pascual-Linaza, A.V.; Couzens, C.; Holmes, C.; Bell, C.; Spence, N.; Huey, R.J.; Murphy, J.A.; Devaney, R.; Lahuerta-Marin, A. Estimation of the Prevalence of Antimicrobial Resistance in Badgers (Meles meles) and Foxes (Vulpes vulpes) in Northern Ireland. Front. Microbiol. 2021, 12, 596891. [Google Scholar] [CrossRef]
  42. Dias, D.; Hipólito, D.; Figueiredo, A.; Fonseca, C.; Caetano, T.; Mendo, S. Unravelling the Diversity and Abundance of the Red Fox (Vulpes vulpes) Faecal Resistome and the Phenotypic Antibiotic Susceptibility of Indicator Bacteria. Animals 2022, 12, 2572. [Google Scholar] [CrossRef] [PubMed]
  43. Bertelloni, F.; Cagnoli, G.; Biagini, F.; Poli, A.; Bibbiani, C.; Ebani, V.V. Virulence Genes of Pathogenic Escherichia coli in Wild Red Foxes (Vulpes vulpes). Animals 2022, 12, 1959. [Google Scholar] [CrossRef]
  44. Botti, V.; Navillod, F.V.; Domenis, L.; Orusa, R.; Pepe, E.; Robetto, S.; Guidetti, C. Salmonella spp. and Antibiotic-Resistant Strains in Wild Mammals and Birds in North-Western Italy from 2002 to 2010. Vet. Ital. 2013, 94, 195–202. [Google Scholar]
  45. Monecke, S.; Gavier-Widen, D.; Mattsson, R.; Rangstrup-Christensen, L.; Lazaris, A.; Coleman, D.C.; Shore, A.C.; Ehricht, R. Detection of mecC-Positive Staphylococcus aureus (CC130-MRSA-XI) in Diseased European Hedgehogs (Erinaceus europaeus) in Sweden. PLoS ONE 2013, 8, e66166. [Google Scholar] [CrossRef]
  46. Hamarova, L.; Kopcakova, A.; Kocianova-Adamcova, M.; Piknova, M.; Javorsky, P.; Pristas, P. Antimicrobial Resistance of Enterococci from Wild Animals in Slovakia. Pol. J. Environ. Stud. 2021, 30, 2085–2091. [Google Scholar] [CrossRef] [PubMed]
  47. Carson, M.; Meredith, A.L.; Shaw, D.J.; Giotis, E.S.; Lloyd, D.H.; Loeffler, A. Foxes As a Potential Wildlife Reservoir for mecA-Positive Staphylococci. Vector-Borne Zoonotic Dis. 2012, 12, 583–587. [Google Scholar] [CrossRef] [PubMed]
  48. Gambino, D.; Vicari, D.; Vitale, M.; Schirò, G.; Mira, F.; Giglia, M.L.; Riccardi, A.; Gentile, A.; Giardina, S.; Carrozzo, A.; et al. Study on Bacteria Isolates and Antimicrobial Resistance in Wildlife in Sicily, Southern Italy. Microorganisms 2021, 9, 203. [Google Scholar] [CrossRef] [PubMed]
  49. Rajabi, M. An Investigation Study on Antimicrobial Resistance in Arctic Environments. Bull. Pure Appl. Sci.-Bot. 2014, 33b, 37. [Google Scholar] [CrossRef]
  50. Glad, T.; Bernhardsen, P.; Nielsen, K.M.; Brusetti, L.; Andersen, M.; Aars, J.; Sundset, M.A. Bacterial Diversity in Faeces from Polar Bear (Ursus maritimus) in Arctic Svalbard. BMC Microbiol. 2010, 10, 10. [Google Scholar] [CrossRef]
  51. Vadnov, M.; Barbič, D.; Žgur-Bertok, D.; Erjavec, M.S. Escherichia coli Isolated from Feces of Brown Bears (Ursus arctos) Have a Lower Prevalence of Human Extraintestinal Pathogenic E. coli Virulence-Associated Genes. Can. J. Vet. Res. 2017, 81, 59–63. [Google Scholar]
  52. Gonçalves, A.; Igrejas, G.; Radhouani, H.; Santos, T.; Monteiro, R.; Marinho, C.; Perez, M.J.; Canales, R.; Mendonza, J.L.; Serra, R.; et al. Iberian Lynx (Lynx pardinus) from the Captive Breeding Program as Reservoir of Antimicrobial Resistant Enterococci and Escherichia coli Isolates. J. Integr. OMICS 2013, 3, 138–144. [Google Scholar] [CrossRef]
  53. Semedo-Lemsaddek, T.; Nóbrega, C.S.; Ribeiro, T.; Pedroso, N.M.; Sales-Luís, T.; Lemsaddek, A.; Tenreiro, R.; Tavares, L.; Vilela, C.L.; Oliveira, M. Virulence Traits and Antibiotic Resistance among Enterococci Isolated from Eurasian Otter (Lutra lutra). Vet. Microbiol. 2013, 163, 378–382. [Google Scholar] [CrossRef]
  54. Semedo-Lemsaddek, T.; Pedroso, N.M.; Freire, D.; Nunes, T.; Tavares, L.; Verdade, L.M.; Oliveira, M. Otter Fecal Enterococci as General Indicators of Antimicrobial Resistance Dissemination in Aquatic Environments. Ecol. Indic. 2018, 85, 1113–1120. [Google Scholar] [CrossRef]
  55. Oliveira, M.; Sales-Luís, T.; Semedo-Lemsaddek, T.; Ribeiro, T.; Pedroso, N.; Tavares, L.; Vilela, C. Chapter 6—Antimicrobial Resistant Aeromonas Isolated from Eurasian Otters (Lutra lutra Linnaeus, 1758) in Portugal. In Animal Diversity, Natural History and Conservation; Daya Publishing House: New Delhi, India, 2011; Volume 1, pp. 123–143. [Google Scholar]
  56. Mengistu, T.S.; Garcias, B.; Castellanos, G.; Seminati, C.; Molina-López, R.A.; Darwich, L. Occurrence of Multidrug Resistant Gram-Negative Bacteria and Resistance Genes in Semi-Aquatic Wildlife-Trachemys scripta, Neovison vison and Lutra lutra-as Sentinels of Environmental Health. Sci. Total Environ. 2022, 830, 154814. [Google Scholar] [CrossRef]
  57. Loncaric, I.; Kübber-Heiss, A.; Posautz, A.; Stalder, G.; Hoffmann, D.; Rosengarten, D.; Walzer, C. Characterization of Methicillin-Resistant Staphylococcus spp. Carrying the mecC Gene, Isolated from Wildlife. J. Antimicrob. Chemother. 2013, 68, 2222–2225. [Google Scholar] [CrossRef]
  58. Vingino, A.; Roberts, M.; Wainstein, M.; West, J.; Norman, S.; Lambourn, D.; Lahti, J.; Ruiz, R.; D’angeli, M.; Weissman, S.; et al. Antibiotics Surveillance for Antibiotic-Resistant E. coli in the Salish Sea Ecosystem. Antibiotics 2021, 10, 1201. [Google Scholar] [CrossRef] [PubMed]
  59. Alonso, C.A.; Alcalá, L.; Simón, C.; Torres, C. Novel Sequence Types of Extended-Spectrum and Acquired AmpC Beta-Lactamase Producing Escherichia coli and Escherichia Clade V Isolated from Wild Mammals. FEMS Microbiol. Ecol. 2017, 93, fix097. [Google Scholar] [CrossRef]
  60. Wilson, J.S.; Hazel, S.M.; Williams, N.J.; Phiri, A.; French, N.P.; Hart, C.A. Nontyphoidal salmonellae in United Kingdom badgers: Prevalence and spatial distribution. Appl. Environ. Microbiol. 2003, 69, 4312–4315. [Google Scholar] [CrossRef] [PubMed]
  61. Darwich, L.; Vidal, A.; Seminati, C.; Albamonte, A.; Casado, A.; López, F.; Molina-López, R.A.; Migura-Garcia, L. High Prevalence and Diversity of Extended-Spectrum β-Lactamase and Emergence of OXA-48 Producing Enterobacterales in Wildlife in Catalonia. PLoS ONE 2019, 14, e0210686. [Google Scholar] [CrossRef]
  62. Osińska, M.; Nowakiewicz, A.; Zięba, P.; Gnat, S.; Łagowski, D.; Trościańczyk, A. Wildlife Carnivorous Mammals As a Specific Mirror of Environmental Contamination with Multidrug-Resistant Escherichia coli Strains in Poland. Microb. Drug Resist. 2020, 26, 1120–1131. [Google Scholar] [CrossRef]
  63. García, L.A.; Torres, C.; López, A.R.; Rodríguez, C.O.; Espinosa, J.O.; Valencia, C.S. Staphylococcus spp. from Wild Mammals in Aragón (Spain): Antibiotic Resistance Status. J. Vet. Res. 2020, 64, 373–379. [Google Scholar] [CrossRef] [PubMed]
  64. Steele, C.M.; Brown, R.N.; Botzler, R.G. Prevalences of Zoonotic Bacteria Among Seabirds in Rehabilitation Centers Along the Pacific Coast of California and Washington, USA. J. Wildl. Dis. 2005, 41, 735–744. [Google Scholar] [CrossRef] [PubMed]
  65. Garcês, A. Why Do Antibiotics Fail? A Veterinary Perspective. J. Small Anim. Adv. 2022, 1, 10–15. [Google Scholar] [CrossRef]
  66. Jacobsen, L.; Wilcks, A.; Hammer, K.; Huys, G.; Gevers, D.; Andersen, S.R. Horizontal Transfer of tet(M) and erm(B) Resistance Plasmids from Food Strains of Lactobacillus plantarum to Enterococcus faecalis JH2-2 in the Gastrointestinal Tract of Gnotobiotic Rats. FEMS Microbiol. Ecol. 2007, 59, 158–166. [Google Scholar] [CrossRef] [PubMed]
  67. Bengtsson, B.; Persson, L.; Ekström, K.; Unnerstad, H.; Uhlhorn, H.; Börjesson, S. High Occurrence of mecC-MRSA in Wild Hedgehogs (Erinaceus europaeus) in Sweden. Vet. Microbiol. 2017, 207, 103–107. [Google Scholar] [CrossRef]
  68. Aslam, B.; Khurshid, M.; Arshad, M.I.; Muzammil, S.; Rasool, M.; Yasmeen, N.; Shah, T.; Chaudhry, T.H.; Rasool, M.H.; Shahid, A.; et al. Antibiotic Resistance: One Health One World Outlook. Front. Cell. Infect. Microbiol. 2021, 11, 1153. [Google Scholar] [CrossRef] [PubMed]
  69. Bonnedahl, J.; Järhult, J.D. Antibiotic Resistance in Wild Birds. Upsala J. Med. Sci. 2014, 119, 113–116. [Google Scholar] [CrossRef]
  70. Gorski, L.; Jay-Russell, M.T.; Liang, A.S.; Walker, S.; Bengson, Y.; Govoni, J.; Mandrell, R.E. Diversity of Pulsed-Field Gel Electrophoresis Pulsotypes, Serovars, and Antibiotic Resistance Among Salmonella Isolates from Wild Amphibians and Reptiles in the California Central Coast. Foodborne Pathog. Dis. 2013, 10, 540–548. [Google Scholar] [CrossRef] [PubMed]
  71. Manyi-Loh, C.; Mamphweli, S.; Meyer, E.; Okoh, A. Antibiotic Use in Agriculture and Its Consequential Resistance in Environmental Sources: Potential Public Health Implications. Molecules 2018, 23, 795. [Google Scholar] [CrossRef] [PubMed]
  72. Joosten, P.; Ceccarelli, D.; Odent, E.; Sarrazin, S.; Graveland, H.; Van Gompel, L.; Battisti, A.; Caprioli, A.; Franco, A.; Wagenaar, J.A.; et al. Antimicrobial Usage and Resistance in Companion Animals: A Cross-Sectional Study in Three European Countries. Antibiotics 2020, 9, 87. [Google Scholar] [CrossRef] [PubMed]
  73. Kruuk, H. Carnivores. In Encyclopedia of Biodiversity; Levin, S.A., Ed.; Elsevier: New York, NY, USA, 2001; pp. 629–640. ISBN 978-0-12-226865-6. [Google Scholar]
  74. Amusa, C.; Rothman, J.; Odongo, S.; Matovu, H.; Ssebugere, P.; Baranga, D.; Sillanpää, M. The endangered African Great Ape: Pesticide residues in soil and plants consumed by Mountain Gorillas (Gorilla beringei) in Bwindi Impenetrable National Park, East Africa. Sci. Total Environ. 2021, 758, 143692. [Google Scholar] [CrossRef] [PubMed]
  75. Campbell, S.J.; Ashley, W.; Gil-Fernandez, M.; Newsome, T.M.; Di Giallonardo, F.; Ortiz-Baez, A.S.; Mahar, J.E.; Towerton, A.L.; Gillings, M.; Holmes, E.C.; et al. Red Fox Viromes in Urban and Rural Landscapes. Virus Evol. 2020, 6, veaa065. [Google Scholar] [CrossRef]
  76. Vittecoq, M.; Laurens, C.; Brazier, L.; Durand, P.; Elguero, E.; Arnal, A.; Thomas, F.; Aberkane, S.; Renaud, N.; Prugnolle, F.; et al. VIM-1 Carbapenemase-Producing Escherichia coli in Gulls from Southern France. Ecol. Evol. 2017, 7, 1224–1232. [Google Scholar] [CrossRef]
  77. Blanco, G.; Junza, A.; Segarra, D.; Barbosa, J.; Barrón, D. Wildlife Contamination with Fluoroquinolones from Livestock: Widespread Occurrence of Enrofloxacin and Marbofloxacin in Vultures. Chemosphere 2016, 144, 1536–1543. [Google Scholar] [CrossRef]
  78. Smoglica, C.; Vergara, A.; Angelucci, S.; Festino, A.R.; Antonucci, A.; Marsilio, F.; Di Francesco, C.E. Antibiotic-Resistant Bacteria Dissemination in the Wildlife, Livestock, and Water of Maiella National Park, Italy. Animals 2023, 13, 432. [Google Scholar] [CrossRef]
  79. Ulstad, C.R.; Solheim, M.; Berg, S.; Lindbæk, M.; Dahle, U.R.; Wester, A.L. Carriage of ESBL/AmpC-Producing or Ciprofloxacin Non-Susceptible Escherichia coli and Klebsiella spp. in Healthy People in Norway. Antimicrob. Resist. Infect. Control 2016, 5, 1–11. [Google Scholar] [CrossRef] [PubMed]
  80. Grijjs, J. A Guide to SDG Interactions: From Science to Implementation; International Council for Science (ICSU): Paris, France, 2017. [Google Scholar]
  81. Gajdács, M.; Urbán, E.; Stájer, A.; Baráth, Z. Antimicrobial Resistance in the Context of the Sustainable Development Goals: A Brief Review. Eur. J. Investig. Health Psychol. Educ. 2021, 11, 71–82. [Google Scholar] [CrossRef] [PubMed]
  82. WHO Study Group. Antimicrobial Resistance and the United Nations Sustainable Development Cooperation Framework: Guidance for United Nations Country Teams. Available online: https://www.who.int/publications-detail-redirect/9789240036024 (accessed on 28 November 2023).
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Figure 1. Flow diagram of data collection.
Figure 1. Flow diagram of data collection.
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Figure 2. Distribution of the studies in the different European countries by carnivorous family group.
Figure 2. Distribution of the studies in the different European countries by carnivorous family group.
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Figure 3. Bacteria species that predominate in the 36 studies in antibiotic resistance in wild carnivores.
Figure 3. Bacteria species that predominate in the 36 studies in antibiotic resistance in wild carnivores.
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Figure 4. Occurrence of phenotypic antimicrobial resistance profile of bacteria in wild carnivores based on the articles included in this review (AMC: amoxicillin/clavulanic acid; AMP: ampicillin; STR: streptomycin; E: erythromycin; ENR: enrofloxacin; E: erythromycin; BE: benzylpenicillin; C: chloramphenicol; CD: clindamycin; CEF: ceftiofur; CEP: cephalothin; CN: gentamicin; CPN: cephalexin; CRO: ceftriaxone; CTX: cefotaxime; DXT: doxycycline; F: nitrofurantoin; IMI: imipenem; INN: cefovecin; KF: cephalothin; MAR: marbofloxacin; NEO: neomycin; PRA: pradofloxacin; PX: cefpodoxime; SXT: trimethoprim/sulfamethoxazole; TE: tetracycline; N: nalidixic acid; CIP: ciprofloxacin; KAN: kanamycin; VAN: vancomycin; Q–D: quinupristin–dalfopristin; CZA: ceftazidime; FEP: cefepime; FOX: cefoxitin: FA: fusidic acid; P: penicillin; T: tobramycin).
Figure 4. Occurrence of phenotypic antimicrobial resistance profile of bacteria in wild carnivores based on the articles included in this review (AMC: amoxicillin/clavulanic acid; AMP: ampicillin; STR: streptomycin; E: erythromycin; ENR: enrofloxacin; E: erythromycin; BE: benzylpenicillin; C: chloramphenicol; CD: clindamycin; CEF: ceftiofur; CEP: cephalothin; CN: gentamicin; CPN: cephalexin; CRO: ceftriaxone; CTX: cefotaxime; DXT: doxycycline; F: nitrofurantoin; IMI: imipenem; INN: cefovecin; KF: cephalothin; MAR: marbofloxacin; NEO: neomycin; PRA: pradofloxacin; PX: cefpodoxime; SXT: trimethoprim/sulfamethoxazole; TE: tetracycline; N: nalidixic acid; CIP: ciprofloxacin; KAN: kanamycin; VAN: vancomycin; Q–D: quinupristin–dalfopristin; CZA: ceftazidime; FEP: cefepime; FOX: cefoxitin: FA: fusidic acid; P: penicillin; T: tobramycin).
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Table 1. Species, family, distribution, diet, habitat, behavior, and conservation status (LC—Least Concern, V—Vulnerable, NT—Near Threat) of wild carnivore species from Europe.
Table 1. Species, family, distribution, diet, habitat, behavior, and conservation status (LC—Least Concern, V—Vulnerable, NT—Near Threat) of wild carnivore species from Europe.
SpeciesFamilyDistributionDietHabitatBehaviorConservation StatusRef.
Beech marten (Martes foina, Erxleben, 1777)MustelidaeEurope, except most Mediterranean islands, the Balkan peninsula, the Scandinavian peninsula, and the United KingdomPlants, fruit, rats, mice, small mammals, birdsUrban areas, forest habitats, and rural areasCrepuscular and nocturnalLC[22]
European polecat (Mustela putorius, Linnaeus, 1758)MustelidaeWestern European Russia, Western Belarus, Western Ukraine, Central and Western Europe, and North AfricaLagomorphs, small rodents, amphibians, birds, reptiles, and insectsRiparian and agricultural areas to meadows and forest areasNocturnal LC[23]
Brown bear (Ursus arctos, Linnaeus, 1758)UrsidaeEurope, Asia, Atlas Mountains, North AmericaOmnivoreMountain woodlands, forestCrepuscular LC[24]
Polar bear (Ursus maritimus, Phipps, 1774)UrsidaeGreenland, Canada, Alaska, Russia, and the Svalbard Archipelago of NorwaySeals, walruses, sea birds, eggs, small mammals, fish, reindeer/caribou, seaweed/kelp, land plantsIce fieldsDiurnal V[25]
Red fox (Vulpes vulpes, Linnaeus, 1758)CanidaeNorthern hemispherePlants, rodents, birds, leporids, porcupines, raccoons, opossums, reptiles, insects, invertebratesScrubland, forest, agricultural fields, urban areasNocturnalLC[26]
European badger (Meles meles, Linnaeus, 1758)MustelidaeEurope (except Scandinavia), Russia, and parts of AsiaOmnivores: plants, earthworms, large insects, small mammals, fruitsDeciduous, mixed, and coniferous forests, agro-silver-pastoral landscapes, Mediterranean scrub forests, and open areas with patches of riparian vegetationCrepuscular and nocturnalLC[27]
European otter (Lutra lutra, Linnaeus, 1758)MustelidaeEurasia, North Africa, the Middle East, Sri Lanka, a part of India, and IndonesiaFish, amphibians, insectsRivers, streams, marshes, lagoons, and reservoirsNocturnal NT[28]
Apennine wolf (Canis lupus italicus, Altobello, 1921)CanidaeItaly, France, Spain, SwitzerlandRoe deer, wild boar, red deer, livestock sheep, horses, Mouflon, Italian hare, birds, invertebrates, fruit, berries, grasses, herbs, and garbageTemperate coniferous forestsCrepuscular, diurnalV[29]
Iberian wolves (Canis lupus signatus, Cabrera, 1907)CanidaePortugal, SpainWild boars, rabbits, roe deer, red deer, ibexes, small carnivores, and fishTemperate forestsCrepuscular, diurnalEN[30]
Iberian Lynx (Lynx pardinus, Temminck, 1827)FelidaePortugal, SpainRabbits, small rodentsMediterranean forests of woodland and shrubland interspersed with natural and artificial pasturesCrepuscular and nocturnalEN[31]
Golden jackal (Canis aureus, Linnaeus, 1758)CanidaeSoutheastern Europe, Moldova, Asia Minor, and the CaucasusOmnivorous diet, plants, fruit, rodents, rabbitsValleys, beside rivers canals, lakes, seashoresCrepuscularLC[32]
Table 2. Antibiotic resistance in animals from the family Canidae regarding species, country, year, type of sample, bacteria isolated, antibiotic resistance, and resistance genes.
Table 2. Antibiotic resistance in animals from the family Canidae regarding species, country, year, type of sample, bacteria isolated, antibiotic resistance, and resistance genes.
SpeciesCountryYearType of SampleIsolated BacteriaAntibiotic Resistance *Resistance GenesRef.
Apennine wolf (Canis lupus italicus)Italy2015–2017Feces Citrobacter spp., Escherichia coli, Hafnia alvei, Salmonella spp., Serratia spp.AMC, AMP, STRn/a[33]
Italy2017Fecesn/aTEtetA, tetP[7]
Italy2022Endocardial swab, lung, thoracic effusionStaphylococcus pseudointermedius, Enterococcus faecalis, E. coliAMC, E, ENR, MAR, CXT, C, SXT, TE, P, DXTn/a[34]
Italy2022Peritoneal effusion, lung, endocardial swab, liver parenchyma, pleural effusionKlebsiella oxytocaAMPn/a[34]
Italy2022Forearm wound, exposed fractureStreptococcus dysgalactiae spp. equisimilis, Leclercia adecarboxilaraAMP, C, CEF, CEP, CN, CPN, DX, ENR, INN, MAR, PRA, PX, SXT, TEn/a[34]
Italy2022Carpal wound, intraarticular swabStreptococcus canis, E. coli, Pseudomonas aeruginosaAMP, C, CPN, CEP, DXT, ENR, INN, MAR, NEO, PRA, SXT, TE, AMC, CEF, CN, CPN, IMI, Fn/a[34]
Iberian wolves (Canis lupus signatus)Portugal2008–2010FecesE. coliTE, AMP, STR, CEP, N, SXT, CIPcdt, chuA, cvaC, eaeA, paa, bfpA, blaCTX-M-1, blaCTX-M-9[35]
Portugal2008–2009FecesEnterococcus faecium, E. hirae, E. faecalis, E. duransAMP, TE, STRtetM, tetL, ermB, blaTEM, tetA, tetB, aadA, strA-strB[36]
Portugal2008–2010FecesE. faecium, E. gallinarumTET, VAN, AMP, E, KANvanC1, vanA, tetM, ermB; aph(3′)-IIIa, tet(L); Tn916, hyl[37]
Golden jackal (Canis aureus)Italy2023Lung, liver, spleen, kidney, and intestinen/an/atetM, tetP, mcr-1, tetA, tetL, tetM, tetO, sul3, blaTEM−1[38]
Red Fox (Vulpes vulpes)Portugal2008–2009Feces E. coliSTR, TE, SXT, AMPadA, tetA, tetB, sul1, blaTEM[39]
Portugal2008–2009Feces E. faeciumTEtetM, tetL, ermB, aph(30)-IIIa[39]
Portugal2008–2009FecesE. faecium, E. duransTE, E ermB, tetM, tetL, Tn916[40]
Ireland 2018–2019Fecal, nasopharyngeal swabsE. coliCZA, TE, SXT, CIP, AMP, FEPn/a[41]
Norway2006FecalE. coliSXT, TE, CIP, Nn/a[1]
Portugal2017–2019FecalE. coli, Enterococcus spp.TE, C, CD, CN, AMC, AMP, BE, CEF, CEP, CZA, CPN, CROblaTEM, ermB, aadA, tetM, tetW, tetL, drfA1, drfA17[42]
Italy2016–2018FecalE. colin/aeaeA, hlyA, stx1, and stx2,[43]
Italy 2002–2010Rectal swabSalmonella enterica, S. typhimuriumAMC, TE, AMP, ENRn/a[44]
Germany, Austria, Sweden2013, 2006, 2005, 2014Nasal swabS. aureusn/agapA, katA, CoA, Spa, sbi, nuc1, sarA, saeS, vraS, agrl, hid[45]
Slovakia2020FecesEnterococcus spp.TE, AMP, VAN, En/a[46]
Spain2012–2015Nasal and rectal swabsStaphylococcus spp. CD, F, AMP, BE, FOX, FA, NEOn/a[47]
Italy 2017–2019Oral, skin, rectal, tracheal swab, fecesK. oxytocaAMP, CDn/a[48]
UK2007–2008TissuesS. sciuri group, S. equorum, S. capitisMET, CL, AMC, AMP, ENR, FD, DA, TETmecA[8]
* AMC: amoxicillin/clavulanic acid; AMP: ampicillin; STR: streptomycin; E: erythromycin; ENR: enrofloxacin; E: erythromycin; BE: benzylpenicillin; C: chloramphenicol; CD: clindamycin; CEF: ceftiofur; CEP: cephalothin; CN: gentamicin; CPN: cephalexin; CRO: ceftriaxone; CTX: cefotaxime; DXT: doxycycline; F: nitrofurantoin; IMI: imipenem; INN: cefovecin; KF: cephalothin; MAR: marbofloxacin; NEO: neomycin; PRA: pradofloxacin; PX: cefpodoxime; SXT: trimethoprim/sulfamethoxazole; TE: tetracycline; N: nalidixic acid; CIP: Ciprofloxacin; KAN: kanamycin; VAN: vancomycin; Q–D: quinupristin–dalfopristin; CZA: ceftazidime; FEP: cefepime; FOX: cefoxitin: FA: fusidic acid; DA: clindamycin; MET: methicillin.
Table 3. Antibiotic resistance in animals from the family Ursidae regarding species, country, year, type of sample, bacteria isolated, antibiotic resistance, and resistance genes.
Table 3. Antibiotic resistance in animals from the family Ursidae regarding species, country, year, type of sample, bacteria isolated, antibiotic resistance, and resistance genes.
SpeciesCountryYearType of SampleIsolated BacteriaAntibiotic Resistance *Resistance GenesRef.
Polar bear (Ursus maritimus)Svalbard2014FecalClostridialesn/ablaTEM[49]
Svalbard2004–2006FecalClostridiales, Firmicutes, E. colin/ablaTEM[50]
Brown bears (Ursus arctos)Slovenia2010–2012FecalE. colin/afimH, ompT, kpsMT, ibeA, traT[51]
Slovakia2020FecesEnterococcus spp.TE, AMP, VAN, E [46]
* AMP: ampicillin; E: erythromycin; TE: tetracycline; VAN: vancomycin.
Table 4. Antibiotic resistance in animals from the family Felidae regarding species, country, year, type of sample, bacteria isolated, antibiotic resistance, and resistance genes.
Table 4. Antibiotic resistance in animals from the family Felidae regarding species, country, year, type of sample, bacteria isolated, antibiotic resistance, and resistance genes.
SpeciesCountryYearType of SampleIsolated BacteriaAntibiotic Resistance *Resistance GenesRef.
Iberian Lynx (Lynx pardinus)Portugal2008–2010FecesE. casseliflavusTE, Q–D, E, STRvanC2, tetM, ermB, hyl, cylA, cylL,[37]
Portugal2008–2010FecesEnterococcus spp., E. coliTE, E, STR, N, SXT, cpd, cylB, and cylL, blaTEM, tetA, aadA, cmlA, dfrA1 + aadA1, dfrA12 + aadA2, fimA[36]
Portugal2008–2010FecesEnterococcus spp. TE, E, KAN, NtetM, tetL, ermB, aac (6′)-Ie-aph(2″)-Ia, ant(6)-Ia, aph(3′)-IIIa[52]
Portugal2008–2010FecesE. coliTE, STR, SXT, N, AMP, CIPblaTEM, blaSHV, tetA, tetB, aadA, strA-strB, aac(3)-II, aac (3)-IV, aadA1, dfrA1 + aadA1, estX + psp + aadA2, aer, cnf1, fimA, papC, papG-allele III[52]
Wild cat (Felis silvestris)Germany2014Nasal swabS. aureusn/agapA, katA, CoA, Spa, sbi, nuc1, sarA, saeS, vraS, agrl, hid[45]
Lynx (Lynx lynx)Sweden2006Liver tissueS. aureusn/agapA, katA, CoA, Spa, sbi, nuc1, sarA, saeS, vraS, agrl, hid, agrlV, mecC[45]
* AMP: ampicillin; STR: streptomycin; E: erythromycin; SXT: trimethoprim/sulfamethoxazole; TE: tetracycline; N: nalidixic acid; CIP: ciprofloxacin; KAN: kanamycin; Q–D: quinupristin–dalfopristin.
Table 5. Antibiotic resistance in animals from the family Mustelidae regarding species, country, year, type of sample, bacteria isolated, antibiotic resistance, and resistance genes.
Table 5. Antibiotic resistance in animals from the family Mustelidae regarding species, country, year, type of sample, bacteria isolated, antibiotic resistance, and resistance genes.
SpeciesCountryYear Type of SampleIsolated BacteriaAntibiotic Resistance *Resistance GenesRef.
Eurasian otter (Lutra lutra)Portugal 2006–2008Feces E. faecalis, E. faecium, E. duransn/aace, acm, ebpABC, gelE, cylA, tetM, pbp5, vanB, vanD, aac(60)-Ie-aph[53]
Portugal2015–2016FecesEnterococcus spp.AMC, AMP, C, CN, DA, ENR, P, TE, VANn/a[54]
Portugal2006FecesAeromonas hydrophila, A. hydrophila/caviae, A. sobriaP, CLI, E, VAN, AMP n/a[55]
Portugal2006–2008FecesS. arizona, S. pullorum, S. choleraesuis arizonaAMC, C, P, AMP, CL, ENR, GN, NA, S, TEn/a[16]
Portugal2009FecesE. coli, Enterococcus spp. CTX, ENR, Sn/a[13]
Spain2018–2021FecesE. coli, Pseudomonas fluorescens, Hafnia alvei, Serratia marcescensCIP, ENR, CN, SXT, TE, CermB, blaCTX-M-15, tetM, blaCMY-2, tetM[56]
Germany2000–2012Nasal and perineal swabsS. aureusAMC, AMP, P, mecC[57]
Portugal 2018–2019Feces E. coli,AMP, SXT, TE, CTX, KAN, CN, PX, DXT, Taac(3)-IV, aph(4)-Ia, aph(6)-Id, blaTEM-1B, lnu(F), tet(B), aac(3)-Iva, aadA1, aac(2′)-Iia, qnrB19, adA5, aph(3″)-Ib, catA1, qnrB19, qnrB82, sulII, dfrA17[58]
Slovakia2020FecesEnterococcus spp.TE, E, AMP, VANn/a[46]
Spain2012–2015Nasal and rectal swabsStaphylococcus spp. N, P, FOX, FAn/a[49]
Spain2015–2015Fecal E. coliAMP, TET, SXTdfrA1 aadA1 qacE 1, sul1, sul2, tetA[59]
Badger (Meles meles)Ireland2018–2019Fecal, nasopharyngeal swabsSalmonella spp., E. coliAMP, CZA, CEP, CTXn/a[60]
Spain2016–2017Swabs E. coliCIP, N, C, S, TblaSHV-12[61]
Poland2014–2018Rectal swabsE. coliAMP, S, KAN, C, CIP, S, N, TE aph(3¢)-Ia, strA, aph(3¢)-Ia, sul2, tetA, tetB, floR, cat, sul3[62]
Germany2011Pharyngeal swabS. aureusn/agapA, katA, CoA, Spa, sbi, nuc1, sarA, saeS, vraS, agrl, hid[45]
Spain2015–2015Fecal E. coliAMP, TEtetB[59]
Spain2012–2015Nasal and rectal swabsStaphylococcus spp. N, P, FOX, FA, CLIn/a[63]
Beech marten (Martes foina)Poland2014–2018Rectal swabsE. coliAMP, STR, KAN, C, CN, CIP, S, N, TE, CTXstrA, sul1, sul2, tetA, tetB, aph(3¢)-Ia, floR, cat, blaTEM-135[62]
Spain2012–2015Nasal and rectal swabsStaphylococcus spp. N, PEN, FOX, TEn/a[49]
Spain2015–2015Fecal E. coliAMP, NAL, CIPblaTEM-1b[59]
Spain2016–2017Swabs Citrobacter freundiiCIP, NAL, GEN, TET, SUL, TMPblack my-2, blaSHV-12[61]
European pine marten (Martes martes)Slovakia2020FecesEnterococcus spp.TE, E, AMP, VANn/a[46]
Italy 2002–2010Rectal swabSalmonella spp.AM, AMC, TEn/a[44]
Italy 2017–2019Oral, skin, rectal, tracheal swab, fecesE. coliAMP, CDn/a[48]
European polecat (Mustela putorius)Poland2014–2018Rectal swabsE. coliAMP, STR, S, TETstrA, sul2, tetA[62]
* AMC: amoxicillin/clavulanic acid; AMP: ampicillin; STR: streptomycin; E: erythromycin; ENR: enrofloxacin; E: erythromycin; BE: benzylpenicillin; C: chloramphenicol; CD: clindamycin; CEF: ceftiofur; CEP: cephalothin; CN: gentamicin; CPN: cephalexin; CRO: ceftriaxone; CTX: cefotaxime; DXT: doxycycline; F: nitrofurantoin; IMI: imipenem; INN: cefovecin; KF: cephalothin; MAR: marbofloxacin; NEO: neomycin; PRA: pradofloxacin; PX: cefpodoxime; SXT: trimethoprim/sulfamethoxazole; TE: tetracycline; N: nalidixic acid; CIP: ciprofloxacin; KAN: kanamycin; VAN: vancomycin; Q–D: quinupristin–dalfopristin; CZA: ceftazidime; FEP: cefepime; FOX: cefoxitin: FA: fusidic acid; P: penicillin; T: tobramycin.
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Garcês, A.; Pires, I. European Wild Carnivores and Antibiotic Resistant Bacteria: A Review. Antibiotics 2023, 12, 1725. https://0-doi-org.brum.beds.ac.uk/10.3390/antibiotics12121725

AMA Style

Garcês A, Pires I. European Wild Carnivores and Antibiotic Resistant Bacteria: A Review. Antibiotics. 2023; 12(12):1725. https://0-doi-org.brum.beds.ac.uk/10.3390/antibiotics12121725

Chicago/Turabian Style

Garcês, Andreia, and Isabel Pires. 2023. "European Wild Carnivores and Antibiotic Resistant Bacteria: A Review" Antibiotics 12, no. 12: 1725. https://0-doi-org.brum.beds.ac.uk/10.3390/antibiotics12121725

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