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Article

Extended-Spectrum β-Lactam Resistant Klebsiella pneumoniae and Escherichia coli in Wild European Hedgehogs (Erinaceus europeus) Living in Populated Areas

1
Departament de Sanitat i Anatomia Animal, Universitat Autònoma de Barcelona (UAB), 08193 Cerdanyola del Vallès, Spain
2
IRTA, Centre de Recerca en Sanitat Animal (CReSA, IRTA-UAB), Campus de la Universitat Autònoma de Barcelona, 08193 Cerdanyola del Vallès, Spain
3
Catalan Wildlife Service, Centre de Fauna Salvatge de Torreferrussa, 08130 Santa Perpètua de Mogoda, Spain
*
Author to whom correspondence should be addressed.
Animals 2021, 11(10), 2837; https://doi.org/10.3390/ani11102837
Submission received: 8 September 2021 / Revised: 22 September 2021 / Accepted: 23 September 2021 / Published: 28 September 2021
(This article belongs to the Special Issue Antimicrobial Resistance: Surveillance and New Strategies)

Simple Summary

The alarming emergence of antimicrobial resistance (AMR) in human and veterinary medicine has activated awareness for monitoring the levels of AMR pollution in the environment and wildlife. European hedgehogs (Erinaceus europaeus) are common wild species habiting urban areas in Europe. In this study, the occurrence and distribution of extended-spectrum β-lactam (ESBL) resistant enterobacteria and AMR genes were assessed in wild European hedgehogs in Catalonia, NE Spain. The results showed that 36.8% of the animals were detected as carriers of β-lactamase/carbapenemase resistance genes, with a special occurrence of human nosocomial bacteria such as Klebsiella pneumoniae, Escherichia coli, and Citrobacter freundii. In addition, more than half of the enterobacteria presented a multidrug resistance (MDR) phenotype and 31% of the isolates had an extended XDR profile. No differences in the spatial distribution of animals with AMR genes were observed within the study region. The results of this study suggest that the close contact with human areas predispose the transmission of AMR genes to wild hedgehogs because they either inhabit and/or feed in an anthropogenic environment. In conclusion, hedgehogs could be good sentinels or bioindicators of AMR environmental pollution, especially in highly populated areas with high human activity.

Abstract

Wildlife has been suggested to be a good sentinel of environmental health because of its close interaction with human populations, domestic animals, and natural ecosystems. The alarming emergence of antimicrobial resistance (AMR) in human and veterinary medicine has activated/triggered the awareness of monitoring the levels of AMR pollution in wildlife. European hedgehogs (Erinaceus europaeus) are common wild species habiting urban areas in Europe. However, there are few studies conducted in hedgehogs as reservoirs of AMR bacteria or genes. The aim of this study was to assess the occurrence and distribution of ESBL, AmpC, and carbapenem-resistant enterobacteria and AMR genes in wild European hedgehogs in Catalonia, a densely populated region of NE Spain. A total of 115 hedgehogs admitted at the Wildlife Rehabilitation Center of Torreferrussa were studied. To our knowledge, this is the first description of β-lactam resistant enterobacteria in wild hedgehogs. Interestingly, 36.8% (42/114) of the animals were detected as carriers of β-lactamase/carbapenemase resistance genes. Klebsiella spp. (59.6%), and specifically K. pneumoniae (84.6%), were the bacteria with the highest proportion of resistance genes, followed by E. coli (34.6%) and C. freundii (5.8%). The most frequently detected genetic variants were blaCTX-M-15 (19.3%), blaSHV-28 (10.5%), blaCMY-1 (9.7%), blaCMY-2 (8.8%), and blaOXA-48 (1.7%). In addition, 52% (27/52) of the isolates presented a multidrug resistance (MDR) phenotype and 31% had an extended drug resistance (XDR) profile. No clustering of animals with AMR genes within the study region was shown in the spatial analysis, nor differences in the proportion of positive animals among regions, were detected. The results of this study suggest that wild European hedgehogs could be good sentinels of AMR environmental pollution, especially in areas with a high human population density, because they either inhabit and/or feed in an anthropogenic environment. In conclusion, it is crucial to raise awareness of the strong interconnection between habitats and compartments, and therefore this implies that AMR issues must be tackled under the One Health approach.
Keywords: wild European hedgehogs; antimicrobial resistance; ESBL; K. pneumoniae; E. coli wild European hedgehogs; antimicrobial resistance; ESBL; K. pneumoniae; E. coli

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MDPI and ACS Style

Garcias, B.; Aguirre, L.; Seminati, C.; Reyes, N.; Allepuz, A.; Obón, E.; Molina-Lopez, R.A.; Darwich, L. Extended-Spectrum β-Lactam Resistant Klebsiella pneumoniae and Escherichia coli in Wild European Hedgehogs (Erinaceus europeus) Living in Populated Areas. Animals 2021, 11, 2837. https://doi.org/10.3390/ani11102837

AMA Style

Garcias B, Aguirre L, Seminati C, Reyes N, Allepuz A, Obón E, Molina-Lopez RA, Darwich L. Extended-Spectrum β-Lactam Resistant Klebsiella pneumoniae and Escherichia coli in Wild European Hedgehogs (Erinaceus europeus) Living in Populated Areas. Animals. 2021; 11(10):2837. https://doi.org/10.3390/ani11102837

Chicago/Turabian Style

Garcias, Biel, Laia Aguirre, Chiara Seminati, Nerea Reyes, Alberto Allepuz, Elena Obón, Rafael A. Molina-Lopez, and Laila Darwich. 2021. "Extended-Spectrum β-Lactam Resistant Klebsiella pneumoniae and Escherichia coli in Wild European Hedgehogs (Erinaceus europeus) Living in Populated Areas" Animals 11, no. 10: 2837. https://doi.org/10.3390/ani11102837

APA Style

Garcias, B., Aguirre, L., Seminati, C., Reyes, N., Allepuz, A., Obón, E., Molina-Lopez, R. A., & Darwich, L. (2021). Extended-Spectrum β-Lactam Resistant Klebsiella pneumoniae and Escherichia coli in Wild European Hedgehogs (Erinaceus europeus) Living in Populated Areas. Animals, 11(10), 2837. https://doi.org/10.3390/ani11102837

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