Implications of Foraging and Interspecies Interactions of Birds for Carriage of Escherichia coli Strains Resistant to Critically Important Antimicrobials
Globally, gulls have been associated with carriage of high levels of strains resistant to critically important antimicrobials (CIAs), a major concern, as these antimicrobials are the sole alternative or one among only a few alternatives available to treat severe life-threatening infections in humans...
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Published in: | Applied and environmental microbiology Vol. 86; no. 20 |
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Abstract | Globally, gulls have been associated with carriage of high levels of
strains resistant to critically important antimicrobials (CIAs), a major concern, as these antimicrobials are the sole alternative or one among only a few alternatives available to treat severe life-threatening infections in humans. Previous studies of Australian silver gulls demonstrated high levels of resistance to CIAs, particularly fluoroquinolone and extended-spectrum cephalosporins, among
strains (carriage at 24% and 22%, respectively). This study aimed to identify and characterize strains from four distinct bird species inhabiting a common coastal environment, determine the frequency of carriage of CIA-resistant
strains, and examine if these resistant clones and their resistance-encoding mobile genetic elements (MGEs) could be transmitted between species. CIA-resistant
was detected in silver gulls (53%), little penguins (11%), and feral pigeons (10%), but not in bridled terns. In total, 37 different sequence types (STs) were identified, including clinically significant human-associated lineages, such as ST131, ST95, ST648, ST69, ST540, ST93, ST450, and ST10. Five main mobile genetic elements associated with
-positive
strains isolated from three bird species were detected. Examination of clonal lineages and MGEs provided indirect evidence of transfer of resistance between bird species. The carriage of CIA-resistant
by gulls and pigeons with proximity to humans, and in some instances food-producing animals, increases the likelihood of further bidirectional dissemination.
It has been shown that 20% of Australian silver gulls carry drug-resistant
strains of anthropogenic origin associated with severe diseases, such as sepsis and urinary tract infections, in humans. To further characterize the dynamics of drug-resistant
in wildlife populations, we investigated the carriage of critically important antimicrobial (CIA) drug-resistant
in four bird species in a common environment. Our results indicated that gulls, pigeons, and penguins carried drug-resistant
strains, and analysis of mobile genetic elements associated with resistance genes indicated interspecies resistance transfer. Terns, representing a bird species that forages on natural food sources at sea and distant from humans, did not test positive for drug-resistant
This study demonstrates carriage of CIA-resistant bacteria in multiple bird species living in areas commonly inhabited by humans and provides further evidence for a leapfrog effect of resistance in wildlife, facilitated by feeding habits. |
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AbstractList | It has been shown that 20% of Australian silver gulls carry drug-resistant
Escherichia coli
strains of anthropogenic origin associated with severe diseases, such as sepsis and urinary tract infections, in humans. To further characterize the dynamics of drug-resistant
E. coli
in wildlife populations, we investigated the carriage of critically important antimicrobial (CIA) drug-resistant
E. coli
in four bird species in a common environment. Our results indicated that gulls, pigeons, and penguins carried drug-resistant
E. coli
strains, and analysis of mobile genetic elements associated with resistance genes indicated interspecies resistance transfer. Terns, representing a bird species that forages on natural food sources at sea and distant from humans, did not test positive for drug-resistant
E. coli
. This study demonstrates carriage of CIA-resistant bacteria in multiple bird species living in areas commonly inhabited by humans and provides further evidence for a leapfrog effect of resistance in wildlife, facilitated by feeding habits.
Globally, gulls have been associated with carriage of high levels of
Escherichia coli
strains resistant to critically important antimicrobials (CIAs), a major concern, as these antimicrobials are the sole alternative or one among only a few alternatives available to treat severe life-threatening infections in humans. Previous studies of Australian silver gulls demonstrated high levels of resistance to CIAs, particularly fluoroquinolone and extended-spectrum cephalosporins, among
E. coli
strains (carriage at 24% and 22%, respectively). This study aimed to identify and characterize strains from four distinct bird species inhabiting a common coastal environment, determine the frequency of carriage of CIA-resistant
E. coli
strains, and examine if these resistant clones and their resistance-encoding mobile genetic elements (MGEs) could be transmitted between species. CIA-resistant
E. coli
was detected in silver gulls (53%), little penguins (11%), and feral pigeons (10%), but not in bridled terns. In total, 37 different sequence types (STs) were identified, including clinically significant human-associated lineages, such as ST131, ST95, ST648, ST69, ST540, ST93, ST450, and ST10. Five main mobile genetic elements associated with
bla
CTX-M
-positive
E. coli
strains isolated from three bird species were detected. Examination of clonal lineages and MGEs provided indirect evidence of transfer of resistance between bird species. The carriage of CIA-resistant
E. coli
by gulls and pigeons with proximity to humans, and in some instances food-producing animals, increases the likelihood of further bidirectional dissemination.
IMPORTANCE
It has been shown that 20% of Australian silver gulls carry drug-resistant
Escherichia coli
strains of anthropogenic origin associated with severe diseases, such as sepsis and urinary tract infections, in humans. To further characterize the dynamics of drug-resistant
E. coli
in wildlife populations, we investigated the carriage of critically important antimicrobial (CIA) drug-resistant
E. coli
in four bird species in a common environment. Our results indicated that gulls, pigeons, and penguins carried drug-resistant
E. coli
strains, and analysis of mobile genetic elements associated with resistance genes indicated interspecies resistance transfer. Terns, representing a bird species that forages on natural food sources at sea and distant from humans, did not test positive for drug-resistant
E. coli
. This study demonstrates carriage of CIA-resistant bacteria in multiple bird species living in areas commonly inhabited by humans and provides further evidence for a leapfrog effect of resistance in wildlife, facilitated by feeding habits. Globally, gulls have been associated with carriage of high levels of strains resistant to critically important antimicrobials (CIAs), a major concern, as these antimicrobials are the sole alternative or one among only a few alternatives available to treat severe life-threatening infections in humans. Previous studies of Australian silver gulls demonstrated high levels of resistance to CIAs, particularly fluoroquinolone and extended-spectrum cephalosporins, among strains (carriage at 24% and 22%, respectively). This study aimed to identify and characterize strains from four distinct bird species inhabiting a common coastal environment, determine the frequency of carriage of CIA-resistant strains, and examine if these resistant clones and their resistance-encoding mobile genetic elements (MGEs) could be transmitted between species. CIA-resistant was detected in silver gulls (53%), little penguins (11%), and feral pigeons (10%), but not in bridled terns. In total, 37 different sequence types (STs) were identified, including clinically significant human-associated lineages, such as ST131, ST95, ST648, ST69, ST540, ST93, ST450, and ST10. Five main mobile genetic elements associated with -positive strains isolated from three bird species were detected. Examination of clonal lineages and MGEs provided indirect evidence of transfer of resistance between bird species. The carriage of CIA-resistant by gulls and pigeons with proximity to humans, and in some instances food-producing animals, increases the likelihood of further bidirectional dissemination. It has been shown that 20% of Australian silver gulls carry drug-resistant strains of anthropogenic origin associated with severe diseases, such as sepsis and urinary tract infections, in humans. To further characterize the dynamics of drug-resistant in wildlife populations, we investigated the carriage of critically important antimicrobial (CIA) drug-resistant in four bird species in a common environment. Our results indicated that gulls, pigeons, and penguins carried drug-resistant strains, and analysis of mobile genetic elements associated with resistance genes indicated interspecies resistance transfer. Terns, representing a bird species that forages on natural food sources at sea and distant from humans, did not test positive for drug-resistant This study demonstrates carriage of CIA-resistant bacteria in multiple bird species living in areas commonly inhabited by humans and provides further evidence for a leapfrog effect of resistance in wildlife, facilitated by feeding habits. Globally, gulls have been associated with carriage of high levels of Escherichia coli strains resistant to critically important antimicrobials (CIAs), a major concern, as these antimicrobials are the sole alternative or one among only a few alternatives available to treat severe life-threatening infections in humans. Previous studies of Australian silver gulls demonstrated high levels of resistance to CIAs, particularly fluoroquinolone and extended-spectrum cephalosporins, among E. coli strains (carriage at 24% and 22%, respectively). This study aimed to identify and characterize strains from four distinct bird species inhabiting a common coastal environment, determine the frequency of carriage of CIA-resistant E. coli strains, and examine if these resistant clones and their resistance-encoding mobile genetic elements (MGEs) could be transmitted between species. CIA-resistant E. coli was detected in silver gulls (53%), little penguins (11%), and feral pigeons (10%), but not in bridled terns. In total, 37 different sequence types (STs) were identified, including clinically significant human-associated lineages, such as ST131, ST95, ST648, ST69, ST540, ST93, ST450, and ST10. Five main mobile genetic elements associated with blaCTX-M-positive E. coli strains isolated from three bird species were detected. Examination of clonal lineages and MGEs provided indirect evidence of transfer of resistance between bird species. The carriage of CIA-resistant E. coli by gulls and pigeons with proximity to humans, and in some instances food-producing animals, increases the likelihood of further bidirectional dissemination. |
Author | Abraham, Rebecca Jane Gunasekera, Samantha Dunlop, James Nicholas Laird, Tanya Barton, Mary Mukerji, Shewli Stegger, Marc O'Dea, Mark Jordan, David Abraham, Sam |
Author_xml | – sequence: 1 givenname: Shewli surname: Mukerji fullname: Mukerji, Shewli organization: Antimicrobial Resistance and Infectious Diseases Laboratory, College of Science, Health, Engineering and Education, Murdoch University, Murdoch, Western Australia, Australia – sequence: 2 givenname: Samantha surname: Gunasekera fullname: Gunasekera, Samantha organization: Antimicrobial Resistance and Infectious Diseases Laboratory, College of Science, Health, Engineering and Education, Murdoch University, Murdoch, Western Australia, Australia – sequence: 3 givenname: James Nicholas surname: Dunlop fullname: Dunlop, James Nicholas organization: Conservation Council WA and Citizen Science Program, Perth, Western Australia, Australia – sequence: 4 givenname: Marc orcidid: 0000-0003-0321-1180 surname: Stegger fullname: Stegger, Marc organization: Department of Bacteria, Parasites and Fungi, Statens Serum Institut, Copenhagen, Denmark – sequence: 5 givenname: David surname: Jordan fullname: Jordan, David organization: NSW Department of Primary Industries, Wollongbar, New South Wales, Australia – sequence: 6 givenname: Tanya surname: Laird fullname: Laird, Tanya organization: Antimicrobial Resistance and Infectious Diseases Laboratory, College of Science, Health, Engineering and Education, Murdoch University, Murdoch, Western Australia, Australia – sequence: 7 givenname: Rebecca Jane surname: Abraham fullname: Abraham, Rebecca Jane organization: Antimicrobial Resistance and Infectious Diseases Laboratory, College of Science, Health, Engineering and Education, Murdoch University, Murdoch, Western Australia, Australia – sequence: 8 givenname: Mary surname: Barton fullname: Barton, Mary organization: Clinical and Health Sciences, University of South Australia, Adelaide, South Australia, Australia – sequence: 9 givenname: Mark surname: O'Dea fullname: O'Dea, Mark email: dea@murdoch.edu.au, s.abraham@murdoch.edu.au organization: Antimicrobial Resistance and Infectious Diseases Laboratory, College of Science, Health, Engineering and Education, Murdoch University, Murdoch, Western Australia, Australia m.o'dea@murdoch.edu.au s.abraham@murdoch.edu.au – sequence: 10 givenname: Sam orcidid: 0000-0003-0950-2317 surname: Abraham fullname: Abraham, Sam email: dea@murdoch.edu.au, s.abraham@murdoch.edu.au organization: Antimicrobial Resistance and Infectious Diseases Laboratory, College of Science, Health, Engineering and Education, Murdoch University, Murdoch, Western Australia, Australia m.o'dea@murdoch.edu.au s.abraham@murdoch.edu.au |
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Keywords | CTX-M Escherichia coli ST131 bird gulls penguins mobile genetic elements Antimicrobial resistance pigeons |
Language | English |
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Notes | Mark O’Dea and Sam Abraham contributed equally. Author order was determined both alphabetically by first name and in order of increasing seniority in the field. Citation Mukerji S, Gunasekera S, Dunlop JN, Stegger M, Jordan D, Laird T, Abraham RJ, Barton M, O’Dea M, Abraham S. 2020. Implications of foraging and interspecies interactions of birds for carriage of Escherichia coli strains resistant to critically important antimicrobials. Appl Environ Microbiol 86:e01610-20. https://doi.org/10.1128/AEM.01610-20. |
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References_xml | – ident: e_1_3_3_8_2 doi: 10.1126/science.aaw1944 – ident: e_1_3_3_29_2 – ident: e_1_3_3_22_2 doi: 10.7589/2019-04-099 – ident: e_1_3_3_19_2 doi: 10.1038/s41598-018-25474-w – ident: e_1_3_3_38_2 doi: 10.1093/bioinformatics/btu033 – ident: e_1_3_3_39_2 doi: 10.1371/journal.pcbi.1004041 – ident: e_1_3_3_18_2 doi: 10.1099/mic.0.000367 – ident: e_1_3_3_26_2 doi: 10.1128/JCM.02562-14 – ident: e_1_3_3_33_2 doi: 10.1093/jac/dkx513 – ident: e_1_3_3_2_2 doi: 10.1371/journal.pone.0224281 – ident: e_1_3_3_32_2 doi: 10.1371/journal.pone.0157718 – volume: 12 start-page: 93 year: 1988 ident: e_1_3_3_13_2 article-title: Seabird island no.188. Penguin Island, Western Australia publication-title: Corella contributor: fullname: Dunlop JN – ident: e_1_3_3_16_2 doi: 10.1128/mBio.00377-13 – volume-title: WHO critically important antimicrobials for human medicine, 6th revision year: 2018 ident: e_1_3_3_4_2 contributor: fullname: WHO – ident: e_1_3_3_11_2 doi: 10.1186/s13028-015-0166-3 – ident: e_1_3_3_17_2 doi: 10.1093/cid/ciy525 – ident: e_1_3_3_28_2 doi: 10.1016/j.ijantimicag.2014.04.011 – ident: e_1_3_3_31_2 doi: 10.1089/cmb.2012.0021 – ident: e_1_3_3_25_2 doi: 10.1038/s41396-018-0200-3 – ident: e_1_3_3_27_2 doi: 10.1111/1758-2229.12019 – ident: e_1_3_3_6_2 doi: 10.1042/EBC20160055 – ident: e_1_3_3_37_2 doi: 10.1126/science.277.5331.1453 – ident: e_1_3_3_35_2 doi: 10.1093/bioinformatics/btp352 – ident: e_1_3_3_34_2 doi: 10.1038/nmeth.1923 – ident: e_1_3_3_23_2 doi: 10.1128/AEM.03138-09 – ident: e_1_3_3_15_2 doi: 10.1093/jac/dkz242 – ident: e_1_3_3_5_2 doi: 10.1093/jac/dkl415 – ident: e_1_3_3_9_2 doi: 10.1371/journal.pone.0190380 – ident: e_1_3_3_14_2 doi: 10.1128/AEM.00861-15 – ident: e_1_3_3_40_2 doi: 10.1093/nar/gkw290 – volume: 66 start-page: 15 year: 1983 ident: e_1_3_3_21_2 article-title: Salmonella on Rottnest Island: implications for public health and wildlife management publication-title: J R Soc Western Australia contributor: fullname: Iveson JB – ident: e_1_3_3_12_2 doi: 10.1111/zph.12182 – ident: e_1_3_3_36_2 doi: 10.1099/mgen.0.000224 – ident: e_1_3_3_3_2 doi: 10.24272/j.issn.2095-8137.2017.003 – volume-title: Performance standards for antimicrobial susceptibility testing year: 2020 ident: e_1_3_3_24_2 contributor: fullname: CLSI – ident: e_1_3_3_30_2 doi: 10.1093/bioinformatics/btu170 – ident: e_1_3_3_10_2 doi: 10.1093/jac/dkw245 – ident: e_1_3_3_7_2 doi: 10.1093/jac/dkw481 – ident: e_1_3_3_20_2 doi: 10.3402/iee.v6.32334 |
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Snippet | Globally, gulls have been associated with carriage of high levels of
strains resistant to critically important antimicrobials (CIAs), a major concern, as these... It has been shown that 20% of Australian silver gulls carry drug-resistant Escherichia coli strains of anthropogenic origin associated with severe diseases,... Globally, gulls have been associated with carriage of high levels of Escherichia coli strains resistant to critically important antimicrobials (CIAs), a major... |
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SubjectTerms | Animals Antimicrobial agents Birds Cephalosporins Charadriiformes - microbiology Coastal environments Columbidae - microbiology Disease Reservoirs - microbiology Disease Reservoirs - veterinary E coli Environmental Microbiology Escherichia coli Escherichia coli - isolation & purification Escherichia coli Infections - microbiology Humans Laridae Pigeons Species Spheniscidae - microbiology Western Australia |
Title | Implications of Foraging and Interspecies Interactions of Birds for Carriage of Escherichia coli Strains Resistant to Critically Important Antimicrobials |
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