Wild Animal Pathogens and Antimicrobial Resistance

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Veterinary Microbiology".

Deadline for manuscript submissions: closed (28 June 2023) | Viewed by 12698

Special Issue Editors


E-Mail Website
Guest Editor
Department of Biological Sciences, Macquarie University, North Ryde, NSW, Australia
Interests: wildlife disease ecology; parasitology

E-Mail Website
Guest Editor
Department of Biological Sciences, Macquarie University, North Ryde, NSW, Australia
Interests: wildlife disease ecology; microbiology

Special Issue Information

Dear Colleagues,

Tackling antimicrobial resistance requires a One Health approach that addresses the connectivity between humans and animals, and the microorganisms within each of these niches. For the animal compartment, studies of farm animals and pets have been more prolific than wild animal studies. Pets, farm animals and humans have had a greater intimacy within their shared environment far longer than they have done with wild animals; however, this is changing. Barriers between humans and wildlife are rapidly being eroded via multiple factors, including urbanization, climate change and ecotourism, resulting in increased connectivity and pathogen exchange between humans and wild animals. Many wildlife species are now well adapted to cities around the world and share urban environments and resources with humans.

An upsurge of studies of antimicrobial resistance in wildlife over recent years has demonstrated the extent to which antimicrobial-resistant pathogens, especially antibiotic-resistant bacteria, have spread to wild animal species. Diverse pathogens with resistance to clinically relevant antibiotics, and often multi-drug resistance, have been detected in taxonomically diverse wildlife that inhabit both land and sea. Many of these wild animal pathogens are strains that are typically associated with humans, indicating that the transmission pathway is from humans to wild animals, and that this microbial spread is driving new wild animal reservoirs and zoonotic pathogen emergence. It is also unclear how antimicrobial-resistant bacteria that have integrated into wildlife microbiomes impact wildlife health.

In this Special Issue, we are interested in showing the extent of the spread of pathogenic microorganisms to wildlife hosts and capturing the diversity of wildlife hosts, pathogenic classes and antimicrobial resistance determinants present in these wild animal pathogens. Overall, we aim to demonstrate the far-reaching spread of antimicrobial-resistant microorganisms from humans to wild animals and highlight the risks that this poses for both human health and wildlife health. This Special Issue will illustrate how integral wildlife is as a component of a One Health approach to addressing antimicrobial resistance and contribute to closing the epidemiological knowledge gap of antimicrobial resistance in wild animal pathogens.

Dr. Michelle Power
Dr. Fiona McDougall
Guest Editors

Manuscript Submission Information

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Keywords

  • antimicrobial resistance
  • wildlife
  • pathogens
  • zoonoses
  • reverse zoonoses
  • antibiotic
  • antibiotic resistance determinants
  • One Health
  • wildlife microbiome

Published Papers (5 papers)

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Research

23 pages, 3885 KiB  
Article
High Prevalence of Beta-Lactam-Resistant Escherichia coli in South Australian Grey-Headed Flying Fox Pups (Pteropus poliocephalus)
by Fiona McDougall, Wayne Boardman and Michelle Power
Microorganisms 2022, 10(8), 1589; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10081589 - 07 Aug 2022
Cited by 5 | Viewed by 2001
Abstract
The emergence of antimicrobial-resistant Escherichia coli in wildlife is concerning—especially resistance to clinically important beta-lactam antibiotics. Wildlife in closer proximity to humans, including in captivity and in rescue/rehabilitation centres, typically have a higher prevalence of antimicrobial-resistant E. coli compared to their free-living counterparts. [...] Read more.
The emergence of antimicrobial-resistant Escherichia coli in wildlife is concerning—especially resistance to clinically important beta-lactam antibiotics. Wildlife in closer proximity to humans, including in captivity and in rescue/rehabilitation centres, typically have a higher prevalence of antimicrobial-resistant E. coli compared to their free-living counterparts. Each year, several thousand Australian fruit bat pups, including the grey-headed flying fox (GHFF; Pteropus poliocephalus), require rescuing and are taken into care by wildlife rescue and rehabilitation groups. To determine the prevalence of beta-lactam-resistant E. coli in rescued GHFF pups from South Australia, faecal samples were collected from 53 pups in care. A combination of selective culture, PCR, antimicrobial susceptibility testing, whole-genome sequencing, and phylogenetic analysis was used to identify and genetically characterise beta-lactam-resistant E. coli isolates. The prevalence of amoxicillin-, amoxicillin-plus-clavulanic-acid-, and cephalosporin-resistant E. coli in the 53 pups was 77.4% (n = 41), 24.5% (n = 13), and 11.3% (n = 6), respectively. GHFF beta-lactam-resistant E. coli also carried resistance genes to aminoglycosides, trimethoprim plus sulphonamide, and tetracyclines in 37.7% (n = 20), 35.8% (n = 19), and 26.4% (n = 14) of the 53 GHFF pups, respectively, and 50.9% (n = 27) of pups carried multidrug-resistant E. coli. Twelve E. coli strain types were identified from the 53 pups, with six strains having extraintestinal pathogenic traits, indicating that they have the potential to cause blood, lung, or wound infections in GHFFs. Two lineages—E. coli ST963 and ST58 O8:H25—were associated with human extraintestinal infections. Phylogenetic analyses determined that all 12 strains were lineages associated with humans and/or domestic animals. This study demonstrates high transmission of anthropogenic-associated beta-lactam-resistant E. coli to GHFF pups entering care. Importantly, we identified potential health risks to GHFF pups and zoonotic risks for their carers, highlighting the need for improved antibiotic stewardship and biosafety measures for GHFF pups entering care. Full article
(This article belongs to the Special Issue Wild Animal Pathogens and Antimicrobial Resistance)
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17 pages, 1946 KiB  
Article
Occurrence and Characteristics of ESBL- and Carbapenemase- Producing Escherichia coli from Wild and Feral Birds in Greece
by Zoi Athanasakopoulou, Celia Diezel, Sascha D. Braun, Marina Sofia, Alexios Giannakopoulos, Stefan Monecke, Dominik Gary, Domenique Krähmer, Dimitris C. Chatzopoulos, Antonia Touloudi, Periklis Birtsas, Matina Palli, Giorgos Georgakopoulos, Vassiliki Spyrou, Efthymia Petinaki, Ralf Ehricht and Charalambos Billinis
Microorganisms 2022, 10(6), 1217; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10061217 - 14 Jun 2022
Cited by 4 | Viewed by 2068
Abstract
Wild and feral birds are known to be involved in the maintenance and dissemination of clinically-important antimicrobial-resistant pathogens, such as extended-spectrum β-lactamase (ESBL) and carbapenemase-producing Enterobacteriaceae. The aim of our study was to evaluate the presence of ESBL- and carbapenemase-producing Escherichia coli among [...] Read more.
Wild and feral birds are known to be involved in the maintenance and dissemination of clinically-important antimicrobial-resistant pathogens, such as extended-spectrum β-lactamase (ESBL) and carbapenemase-producing Enterobacteriaceae. The aim of our study was to evaluate the presence of ESBL- and carbapenemase-producing Escherichia coli among wild and feral birds from Greece and to describe their antimicrobial resistance characteristics. In this context, fecal samples of 362 birds were collected and cultured. Subsequently, the antimicrobial resistance pheno- and geno-type of all the obtained E. coli isolates were determined. A total of 12 multidrug-resistant (MDR), ESBL-producing E. coli were recovered from eight different wild bird species. Eleven of these isolates carried a blaCTX-M-1 group gene alone or in combination with blaTEM and one carried only blaTEM. AmpC, fluoroquinolone, trimethoprim/sulfamethoxazole, aminoglycoside and macrolide resistance genes were also detected. Additionally, one carbapenemase-producing E. coli was identified, harboring blaNDM along with a combination of additional resistance genes. This report describes the occurrence of ESBL- and carbapenemase-producing E. coli among wild avian species in Greece, emphasizing the importance of incorporating wild birds in the assessment of AMR circulation in non-clinical settings. Full article
(This article belongs to the Special Issue Wild Animal Pathogens and Antimicrobial Resistance)
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10 pages, 868 KiB  
Article
Oral Bacteria and Their Antibiotic Susceptibilities in Taiwanese Venomous Snakes
by Po-Chun Chuang, Wen-Hao Lin, Yi-Chun Chen, Chun-Chih Chien, I-Min Chiu and Tein-Shun Tsai
Microorganisms 2022, 10(5), 951; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10050951 - 30 Apr 2022
Cited by 8 | Viewed by 2463
Abstract
Wound infections after venomous snakebites are clinically important. Information regarding the nature and antibiotic susceptibilities of snake oral bacterial flora could support empiric antibiotic therapy. Wild venomous snakes were collected from southern Taiwan: a total of 30 each of Bungarus multicinctus, Naja [...] Read more.
Wound infections after venomous snakebites are clinically important. Information regarding the nature and antibiotic susceptibilities of snake oral bacterial flora could support empiric antibiotic therapy. Wild venomous snakes were collected from southern Taiwan: a total of 30 each of Bungarus multicinctus, Naja atra, Protobothrops mucrosquamatus, and Trimeresurus stejnegeri; 3 Deinagkistrodon acutus; and 4 Daboia siamensis. The species and antibiotic susceptibilities of their oral bacteria were determined. Aerobic gram-negative bacteria, especially Pseudomonas aeruginosa and Proteus vulgaris, were the most abundant. Proteus vulgaris were more abundant in B. multicinctus, N. atra, and P. mucrosquamatus than in T. stejnegeri (40%, 43.3%, and 40% vs. 13.3%, respectively). The gram-negative species were less susceptible to first- and second-generation cephalosporins and ampicillin-sulbactam than to third-generation cephalosporins, fluoroquinolones, carbapenems, or piperacillin-tazobactam. The most abundant aerobic gram-positive species cultured was Enterococcus faecalis, which was more abundant in N. atra than in other snakes (p < 0.001) and was highly susceptible to ampicillin, high-level gentamicin, penicillin, teicoplanin, and vancomycin. Bacteroides fragilis and Clostridium species were the most common anaerobic bacteria. The anaerobic organisms were highly susceptible to metronidazole and piperacillin. As a reference for empiric antimicrobial therapy, third-generation cephalosporins, fluoroquinolones, carbapenems, or piperacillin-tazobactam can be initiated in venomous snakebites wound infections. Full article
(This article belongs to the Special Issue Wild Animal Pathogens and Antimicrobial Resistance)
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18 pages, 1283 KiB  
Article
Imported Pet Reptiles and Their “Blind Passengers”—In-Depth Characterization of 80 Acinetobacter Species Isolates
by Franziska Unger, Tobias Eisenberg, Ellen Prenger-Berninghoff, Ursula Leidner, Torsten Semmler and Christa Ewers
Microorganisms 2022, 10(5), 893; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms10050893 - 24 Apr 2022
Cited by 4 | Viewed by 2666
Abstract
Reptiles are popular pet animals and important food sources, but the trade of this vertebrate class is—besides welfare and conservation—under debate due to zoonotic microbiota. Ninety-two shipments of live reptiles were sampled during border inspections at Europe’s most relevant transshipment point for the [...] Read more.
Reptiles are popular pet animals and important food sources, but the trade of this vertebrate class is—besides welfare and conservation—under debate due to zoonotic microbiota. Ninety-two shipments of live reptiles were sampled during border inspections at Europe’s most relevant transshipment point for the live animal trade. Acinetobacter spp. represented one significant fraction of potentially MDR bacteria that were further analyzed following non-selective isolation or selective enrichment from feces, urinate, or skin samples. Taxonomic positions of respective isolates were confirmed by MALDI-TOF MS and whole-genome sequencing analysis (GBDP, dDDH, ANIb, and rMLST). The majority of the 80 isolates represented established species; however, a proportion of potentially novel taxa was found. Antimicrobial properties and genome-resistance gene screening revealed novel and existing resistance mechanisms. Acinetobacter spp. strains were most often resistant to 6–10 substance groups (n = 63) in vitro. Resistance to fluorchinolones (n = 4) and colistin (n = 7), but not to carbapenems, was noted, and novel oxacillinase variants (n = 39) were detected among other genes. Phylogenetic analysis (MLST) assigned few isolates to the known STs (25, 46, 49, 220, and 249) and to a number of novel STs. No correlation was found to indicate that MDR Acinetobacter spp. in reptiles were associated with harvesting mode, e.g., captive-bred, wild-caught, or farmed in natural ecosystems. The community of Acinetobacter spp. in healthy reptiles turned out to be highly variable, with many isolates displaying a MDR phenotype or genotype. Full article
(This article belongs to the Special Issue Wild Animal Pathogens and Antimicrobial Resistance)
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11 pages, 1122 KiB  
Article
First Report of CC5-MRSA-IV-SCCfus “Maltese Clone” in Bat Guano
by Assia Mairi, Abdelaziz Touati, Alix Pantel, Alex Yahiaoui Martinez, Mourad Ahmim, Albert Sotto, Catherine Dunyach-Remy and Jean-Philippe Lavigne
Microorganisms 2021, 9(11), 2264; https://0-doi-org.brum.beds.ac.uk/10.3390/microorganisms9112264 - 31 Oct 2021
Cited by 5 | Viewed by 1964
Abstract
Methicillin-resistant Staphylococcus aureus (MRSA) is a widespread pathogen that could cause different illnesses in both human and animals. Presence of MRSA in animals raises concerns of their capacity to act as reservoirs, particularly in wild animals. This study aimed to characterize the resistance [...] Read more.
Methicillin-resistant Staphylococcus aureus (MRSA) is a widespread pathogen that could cause different illnesses in both human and animals. Presence of MRSA in animals raises concerns of their capacity to act as reservoirs, particularly in wild animals. This study aimed to characterize the resistance and virulence patterns of S. aureus strains isolated from bat guano in Algeria. From March to May 2016, 98 bat guano samples from Aokas’s cave (Bejaia, Algeria) were collected. Swabs were taken for microbiological studies. Isolates were identified by Vitek® MS system, and antibiotic susceptibility was determined by disk diffusion method. The clonal origin, virulence and antibiotic resistance profiles of S. aureus isolates were characterized by whole genome sequencing. Eleven S. aureus strains were obtained from the 98 guano samples. Seven isolates were sensitive to all antibiotics tested and four (36.3%) were resistant to penicillin G, cefoxitin and fusidic acid. The four MRSA isolates were assigned to the sequence type ST149 and related to spa type t010. These isolates harbored a SCCmecIV element and the fusidic acid resistance element Q6GD50 (fusC). They carried different virulence genes including several enterotoxins (sea, egc enterotoxin locus, sec, sel), and the toxic shock syndrome toxin (tst). Our results highlight that bat guano may constitute an important reservoir of MRSA strains. Full article
(This article belongs to the Special Issue Wild Animal Pathogens and Antimicrobial Resistance)
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