Gulls as Sources of Environmental Contamination by Colistin-resistant Bacteria

Franklin, Alan B.; Ramey, Andrew M.; Bentler, Kevin T.; Barrett, Nicole L.; McCurdy, Loredana M.; Ahlstrom, Christina A.; Bonnedahl, Jonas; Shriner, Susan A.; Chandler, Jeffrey C.

doi:10.1038/s41598-020-61318-2

Cited by 39 publications

(29 citation statements)

References 30 publications

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“…Therefore, gulls have been considered valid sentinel species, especially to explore the influence of urbanization on microbial communities [ 4 ]. Indeed, gulls act as potential reservoirs of pathogenic and antibiotic-resistant bacteria, and might spread these strains across the different environments they inhabit [ 4 , 5 ]. The dramatic growth of the urban gull populations raises important health concerns, especially considering that the routes of acquisition and dissemination have not been elucidated, thus impeding the development of appropriate control measures [ 6 ].…”

Section: Introductionmentioning

confidence: 99%

Prevalence and Antimicrobial Resistance of Enteropathogenic Bacteria in Yellow-Legged Gulls (Larus michahellis) in Southern Italy

Russo

Pace

Varriale

et al. 2021

Animals

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Wild birds may host and spread pathogens, integrating the epidemiology of infectious diseases. Particularly, Larus spp. have been described as responsible for the spread of many enteric diseases, primarily because of their large populations at landfill sites. The aim of this study was to examine the role of yellow-legged gulls as a source of enteropathogenic bacteria such as Campylobacter spp., Salmonella spp., Shiga toxin-producing Escherichia coli and Yersinia spp., with particular attention to antibiotic-resistant strains. Enteropathogenic bacteria were isolated from 93/225 yellow-legged gulls examined from April to July, during a four-year period (2016–2019). Specifically, Campylobacter spp. was isolated from 60/225 samples (26.7%), and identified as C. coli (36/60) and as C. jejuni (24/60). Salmonella spp. was isolated from 3/225 samples (1.3%), and identified as Salmonella arizonae. Shiga toxin-producing E. coli were isolated from 30/225 samples (13.3%) samples, and serotyped as E. coli O128 (12/30) O26 (9/30), O157 (6/30) and O11 (3/30); Yersinia spp. was never detected. Isolated strains exhibited multidrug resistance, including vitally important antibiotics for human medicine (i.e., fluoroquinolones, tetracyclines). Our study emphasizes the importance of yellow-legged gulls as potential reservoirs of pathogenic and resistant strains and their involvement in the dissemination of these bacteria across different environments, with resulting public health concerns.

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Section: Introductionmentioning

confidence: 99%

Prevalence and Antimicrobial Resistance of Enteropathogenic Bacteria in Yellow-Legged Gulls (Larus michahellis) in Southern Italy

Russo

Pace

Varriale

et al. 2021

Animals

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“…In these small-scale experiments, mcr-1 was reliably detected when the initial inoculum was ≥10 2 CFU/g feces (data not shown). However, our previous data suggests that fecal shedding of these mcr-1 E. coli occurs at levels of ≤10 2 CFU/g feces, supporting the need to validate upstream enrichment strategies (Franklin et al, 2020).…”

Section: Validation Of the Methods For Detection Of Mcr-1 E Coli In Fmentioning

confidence: 81%

Validation of a screening method for the detection of colistin-resistant E. coli containing mcr-1 in feral swine feces

Chandler¹,

Franklin²,

Bevins³

et al. 2020

Journal of Microbiological Methods

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A method was developed and validated for the detection of colistin-resistant Escherichia coli containing mcr-1 in the feces of feral swine. Following optimization of an enrichment method using EC broth supplemented with colistin (1 μg/mL) and vancomycin (8 μg/mL), aliquots derived from 100 feral swine fecal samples were spiked with of one of five different mcr-1 positive E. coli strains (between 10 0 and 10 4 CFU/g), for a total of 1110 samples tested. Enrichments were then screened using a simple boil-prep and a previously developed real-time PCR assay for mcr-1 detection. The sensitivity of the method was determined in swine feces, with mcr-1 E. coli inocula of 0.1-9.99 CFU/g (n = 340), 10-49.99 CFU/g (n = 170), 50-99 CFU/g (n = 255), 100-149 CFU/g (n = 60), and 200-2200 CFU/g (n = 175), which were detected with 32%, 72%, 88%, 95%, and 98% accuracy, respectively. Uninoculated controls (n = 100) were negative for mcr-1 following enrichment.

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“…Because migratory birds are capable of acquiring ARGs from humans, domestic animals and the environment ( 15 , 17 , 20 , 44 , 45 , 85 – 89 ), this group has been largely suggested as reservoirs and dispersers of antimicrobial resistance ( 45 , 88 , 90 ). Despite a recent experimental study in captive ring-billed gulls ( Larus delawarensis ) in which the individuals were able to shed and contaminate the artificial environment and infect cospecifics in a controlled setting ( 91 ), further studies under natural conditions are necessary to confirm such hypothesis. Herein, migration may have not been a key factor from an epidemiological perspective of ARGs dispersal affecting humans, because despite our significant findings in Magellanic penguin [e.g., detection of ARGs in 10 out of the 11 individuals and of a gene of great public health importance ( bla TEM )], this is a highly pelagic species that spends a great part of its life cycle in the oceans ( 26 ), sustaining limited direct contact with humans.…”

Section: Discussionmentioning

confidence: 99%

Occurrence and Quantification of Antimicrobial Resistance Genes in the Gastrointestinal Microbiome of Two Wild Seabird Species With Contrasting Behaviors

Ewbank

Esperón²,

Sacristán

et al. 2021

Front. Vet. Sci.

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Antimicrobial resistance genes (ARGs) are environmental pollutants and anthropization indicators. We evaluated human interference in the marine ecosystem through the ocurrence and quantification (real-time PCRs) of 21 plasmid-mediated ARGs in enema samples of 25 wild seabirds, upon admission into rehabilitation: kelp gull (Larus dominicanus, n = 14) and Magellanic penguin (Spheniscus magellanicus, n = 11). Overall, higher resistance values were observed in kelp gulls (non-migratory coastal synanthropic) in comparison with Magellanic penguins (migratory pelagic non-synanthropic). There were significant differences between species (respectively, kelp gull and Magellanic penguin): ARGs occurrence (blaTEM [p = 0.032]; tetM [p = 0.015]; tetA [p = 0.003]; and sulII [p = 0.007]), mean number of ARGs per sample (p = 0.031), ARGs mean load percentage (aadA [p = 0.045], tetA [p = 0.031], tetM [p = 0.016], blaTEM [p = 0.032], sulII [p = 0.008]), percentage of genes conferring resistance to an antimicrobial class (betalactams [p = 0.036] and sulfonamides [p = 0.033]), mean number of genes conferring resistance to one or more antimicrobial classes (p = 0.024]), percentage of multiresistant microbiomes (p = 0.032), and clustering (p = 0.006). These differences are likely due to these species' contrasting biology and ecology - key factors in the epidemiology of ARGs in seabirds. Additionally, this is the first report of mecA in seabirds in the Americas. Further studies are necessary to clarify the occurrence and diversity of ARGs in seabirds, and their role as potential sources of infection and dispersal within the One Health chain of ARGs.

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Gulls as Sources of Environmental Contamination by Colistin-resistant Bacteria

Abstract: became colonized with M175 E. coli and was observed shedding 10 2.00 CFU/g on day 7 post inoculation (Fig. 1), indicating that this strain could be transmitted to conspecific birds.

Cited by 39 publications

References 30 publications

Prevalence and Antimicrobial Resistance of Enteropathogenic Bacteria in Yellow-Legged Gulls (Larus michahellis) in Southern Italy

Prevalence and Antimicrobial Resistance of Enteropathogenic Bacteria in Yellow-Legged Gulls (Larus michahellis) in Southern Italy

Validation of a screening method for the detection of colistin-resistant E. coli containing mcr-1 in feral swine feces

Occurrence and Quantification of Antimicrobial Resistance Genes in the Gastrointestinal Microbiome of Two Wild Seabird Species With Contrasting Behaviors

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