1887

Abstract

Wild animals are one of the putative reservoirs of antimicrobial-resistant bacteria, but the significance of raccoon dogs remains to be investigated.

Raccoon dogs can be a reservoir of antimicrobial-resistant bacteria.

This study aimed to explore the prevalence of antimicrobial resistance, mainly extended-spectrum cephalosporins resistance, in isolates from faeces of 80 Japanese raccoon dogs in Kanagawa Prefecture, Japan.

All of the 80 faecal samples were streaked onto deoxycholate-hydrogen sulfate-lactose (DHL) and cefotaxime (CTX)-supplemented DHL (DHL-CTX) agars. Susceptibilities to ten antimicrobials were determined using the agar dilution method. Additionally, extended-spectrum β-lactamases (ESBLs) and AmpC-type β-lactamases (ABLs) were identified in addition to sequence types (STs), in ESC-resistant isolates by a polymerase chain reaction and sequencing.

Out of all the samples, 75 (93.8 %) and 20 (25.0 %) isolates were isolated by DHL and DHL-CTX agars, respectively. Significantly higher resistance rates to most of the drugs were found in DHL-CTX-derived isolates than DHL-derived isolates (<0.01). Genetic analysis identified CTX-M-14 (=6), CTX-M-2 (=2), CTX-M-1 (=1) and CTX-M-55 (=1) as ESBLs, and CMY-2 (=8) and DHA-1 (=1) as ABLs in 20 DHL-CTX-derived isolates. Most of the detected STs were related to Japanese humans (i.e. ST10, ST58, ST69, ST131, ST357, ST648 and ST4038). Notably, this is the first report on ST69, ST131, ST155 and ST648, which are well-known international high-risk clones in Japanese raccoon dogs.

Our findings underscore the need to understand the significance of raccoon dogs as an antimicrobial-resistant bacteria reservoir using one health approach.

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2022-12-16
2024-05-04
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References

  1. Gil-Gil T, Laborda P, Sanz-García F, Hernando-Amado S, Blanco P et al. Antimicrobial resistance: a multifaceted problem with multipronged solutions. Microbiologyopen 2019; 8:e945 [View Article]
    [Google Scholar]
  2. Bush K, Bradford PA. Epidemiology of β-lactamase-producing pathogens. Clin Microbiol Rev 2020; 33:e00047-19 [View Article]
    [Google Scholar]
  3. Peirano G, Pitout JDD. Extended spectrum β-lactamase producing Enterobacteriaceae: update on molecular epidemiology and treatment options. Drugs 2019; 79:1529–1541 [View Article]
    [Google Scholar]
  4. Ramos S, Silva V, Dapkevicius M de L, Caniça M, Tejedor-Junco MT et al. Escherichia coli as commensal and pathogenic bacteria among food-producing animals: health implications of Extended Spectrum β-Lactamase (ESBL) production. Animals (Basel) 2020; 10:E2239 [View Article]
    [Google Scholar]
  5. Salgado-Caxito M, Benavides JA, Adell AD, Paes AC, Moreno-Switt AI. Global prevalence and molecular characterization of extended-spectrum β-lactamase producing-Escherichia coli in dogs and cats - A scoping review and meta-analysis. One Health 2021; 12:100236 [View Article] [PubMed]
    [Google Scholar]
  6. Palmeira JD, Cunha MV, Carvalho J, Ferreira H, Fonseca C et al. Emergence and spread of cephalosporinases in wildlife: a review. Animals 2021; 11:1765 [View Article]
    [Google Scholar]
  7. Laborda P, Sanz-García F, Ochoa-Sánchez LE, Gil-Gil T, Hernando-Amado S et al. Wildlife and antibiotic resistance. Front Cell Infect Microbiol 2022; 12:873989 [View Article]
    [Google Scholar]
  8. Daszak P, Cunningham AA, Hyatt AD. Emerging infectious diseases of wildlife--threats to biodiversity and human health. Science 2000; 287:443–449 [View Article] [PubMed]
    [Google Scholar]
  9. Worsley-Tonks KEL, Gehrt SD, Miller EA, Singer RS, Bender JB et al. Comparison of antimicrobial-resistant Escherichia coli isolates from urban raccoons and domestic dogs. Appl Environ Microbiol 2021; 87:e00484–21 [View Article]
    [Google Scholar]
  10. Kim SI, Oshida T, Lee H, Min MS, Kimura J. Evolutionary and biogeographical implications of variation in skull morphology of raccoon dogs (Nyctereutes procyonoides, Mammalia: Carnivora). Biol J Linn Soc 2015; 116:856–872 [View Article]
    [Google Scholar]
  11. Yamamoto Y, Kinoshita A, Higashimoto H. Distribution and habitant selection of the raccoon dogs. Bull Kawasaki Munic Sci Mus Youth 1995; 6:83–88
    [Google Scholar]
  12. Jardine CM, Janecko N, Allan M, Boerlin P, Chalmers G et al. Antimicrobial resistance in Escherichia coli isolates from raccoons (Procyon lotor) in Southern Ontario, Canada. Appl Environ Microbiol 2012; 78:3873–3879 [View Article] [PubMed]
    [Google Scholar]
  13. Clinical Laboratory and Standard Institute Performance Standards for Antimicrobial Susceptibility Testing, 32nd. edn USA: CLSI supplement M100; 2022
    [Google Scholar]
  14. Shimizu T, Harada K, Tsuyuki Y, Kimura Y, Miyamoto T et al. In vitro efficacy of 16 antimicrobial drugs against a large collection of β-lactamase-producing isolates of extraintestinal pathogenic Escherichia coli from dogs and cats. J Med Microbiol 2017; 66:1085–1091 [View Article] [PubMed]
    [Google Scholar]
  15. Wirth T, Falush D, Lan R, Colles F, Mensa P et al. Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 2006; 60:1136–1151 [View Article] [PubMed]
    [Google Scholar]
  16. Tamamura-Andoh Y, Tanaka N, Sato K, Mizuno Y, Arai N et al. A survey of antimicrobial resistance in Escherichia coli isolated from wild sika deer (Cervus nippon) in Japan. J Vet Med Sci 2021; 83:754–758 [View Article] [PubMed]
    [Google Scholar]
  17. Wasyl D, Zając M, Lalak A, Skarżyńska M, Samcik I et al. Antimicrobial resistance in Escherichia coli isolated from wild animals in Poland. Microb Drug Resist 2018; 24:807–815 [View Article]
    [Google Scholar]
  18. Alonso CA, González-Barrio D, Tenorio C, Ruiz-Fons F, Torres C. Antimicrobial resistance in faecal Escherichia coli isolates from farmed red deer and wild small mammals. Detection of a multiresistant E. coli producing extended-spectrum beta-lactamase. Comp Immunol Microbiol Infect Dis 2016; 45:34–39 [View Article] [PubMed]
    [Google Scholar]
  19. Bachiri T, Bakour S, Ladjouzi R, Thongpan L, Rolain JM et al. High rates of CTX-M-15-producing Escherichia coli and Klebsiella pneumoniae in wild boars and Barbary macaques in Algeria. J Glob Antimicrob Resist 2017; 8:35–40 [View Article] [PubMed]
    [Google Scholar]
  20. Darwich L, Seminati C, López-Olvera JR, Vidal A, Aguirre L et al. Detection of β-lactam-resistant Escherichia coli and toxigenic Clostridioides difficile strains in wild boars foraging in an anthropization gradient. Animals (Basel) 2021; 11:1585 [View Article]
    [Google Scholar]
  21. Guyomard-Rabenirina S, Reynaud Y, Pot M, Albina E, Couvin D et al. Antimicrobial resistance in wildlife in Guadeloupe (French West Indies): distribution of a Single blaCTX–M–1/IncI1/ST3 plasmid among humans and wild animals. Front Microbiol 2020; 11:1524 [View Article]
    [Google Scholar]
  22. Homeier-Bachmann T, Schütz AK, Dreyer S, Glanz J, Schaufler K et al. Genomic analysis of ESBL-producing E. coli in wildlife from North-Eastern Germany. Antibiotics (Basel) 2022; 11:123
    [Google Scholar]
  23. Mercato A, Cortimiglia C, Abualsha’ar A, Piazza A, Marchesini F et al. Wild boars as an indicator of environmental spread of ESβL-producing Escherichia coli. Front Microbiol 2022; 13:838383 [View Article]
    [Google Scholar]
  24. O’Hagan MJH, Pascual-Linaza AV, Couzens C, Holmes C, Bell C et al. 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]
  25. Osińska M, Nowakiewicz A, Zięba P, Gnat S, Łagowski D et al. A rich mosaic of resistance in extended-spectrum β-lactamase-producing Escherichia coli isolated from red foxes (Vulpes vulpes) in Poland as a potential effect of increasing synanthropization. Sci Total Environ 2022; 818:151834 [View Article]
    [Google Scholar]
  26. Selmi R, Tayh G, Srairi S, Mamlouk A, Ben Chehida F et al. Prevalence, risk factors and emergence of extended-spectrum β-lactamase producing-, carbapenem- and colistin-resistant Enterobacterales isolated from wild boar (Sus scrofa) in Tunisia. Microb Pathog 2022; 163:105385 [View Article] [PubMed]
    [Google Scholar]
  27. Patel HB, Lusk KA, Cota JM. The role of cefepime in the treatment of extended-spectrum β-lactamase infections. J Pharm Pract 2019; 32:458–463 [View Article]
    [Google Scholar]
  28. Ewers C, Bethe A, Semmler T, Guenther S, Wieler LH. Extended-spectrum β-lactamase-producing and AmpC-producing Escherichia coli from livestock and companion animals, and their putative impact on public health: a global perspective. Clin Microbiol Infect 2012; 18:646–655 [View Article] [PubMed]
    [Google Scholar]
  29. Nakano R, Nakano A, Abe M, Inoue M, Okamoto R. Regional outbreak of CTX-M-2 β-lactamase-producing Proteus mirabilis in Japan. J Med Microbiol 2012; 61:1727–1735 [View Article] [PubMed]
    [Google Scholar]
  30. Yokemura M, Hasunuma Y, Ishimatsu T, Tsunoda T, Tokuoka Y. Surveillance of CTX-M type ESBL-producing Escherichia coli isolated from intermediate and small medical facilities in Kanagawa prefecture. J Jap Soc Clin Microbiol 2019; 29:21–27
    [Google Scholar]
  31. Harada K, Shimizu T, Mukai Y, Kuwajima K, Sato T et al. Phenotypic and molecular characterization of antimicrobial resistance in Klebsiella spp. isolates from companion animals in Japan: clonal dissemination of multidrug-resistant extended-spectrum β-lactamase-producing Klebsiella pneumoniae. Front Microbiol 2016; 7:1021 [View Article]
    [Google Scholar]
  32. Harada K, Shimizu T, Mukai Y, Kuwajima K, Sato T et al. Phenotypic and molecular characterization of antimicrobial resistance in Enterobacter spp. isolates from companion animals in Japan. PLoS One 2017; 12:e0174178 [View Article] [PubMed]
    [Google Scholar]
  33. Matsumura Y, Yamamoto M, Higuchi T, Komori T, Tsuboi F et al. Prevalence of plasmid-mediated AmpC β-lactamase-producing Escherichia coli and spread of the ST131 clone among extended-spectrum β-lactamase-producing E. coli in Japan. Int J Antimicrob Agents 2012; 40:158–162 [View Article] [PubMed]
    [Google Scholar]
  34. Matsukawa M, Igarashi M, Watanabe H, Qin L, Ohnishi M et al. Epidemiology and genotypic characterisation of dissemination patterns of uropathogenic Escherichia coli in a community. Epidemiol Infect 2019; 147:e148 [View Article] [PubMed]
    [Google Scholar]
  35. Yano H, Uemura M, Endo S, Kanamori H, Inomata S et al. Molecular characteristics of extended-spectrum β-lactamases in clinical isolates from Escherichia coli at a Japanese tertiary hospital. PLoS One 2013; 8:e64359 [View Article] [PubMed]
    [Google Scholar]
  36. Mathers AJ, Peirano G, Pitout JDD. The role of epidemic resistance plasmids and international high-risk clones in the spread of multidrug-resistant Enterobacteriaceae. Clin Microbiol Rev 2015; 28:565–591 [View Article] [PubMed]
    [Google Scholar]
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