One Health Genomic Analysis of Extended-Spectrum β-Lactamase‒Producing Salmonella enterica, Canada, 2012‒2016

Extended-spectrum β-lactamases (ESBLs) confer resistance to extended-spectrum cephalosporins, a major class of clinical antimicrobial drugs. We used genomic analysis to investigate whether domestic food animals, retail meat, and pets were reservoirs of ESBL-producing Salmonella for human infection in Canada. Of 30,303 Salmonella isolates tested during 2012–2016, we detected 95 ESBL producers. ESBL serotypes and alleles were mostly different between humans (n = 54) and animals/meat (n = 41). Two exceptions were blaSHV-2 and blaCTX-M-1 IncI1 plasmids, which were found in both sources. A subclade of S. enterica serovar Heidelberg isolates carrying the same IncI1-blaSHV-2 plasmid differed by only 1–7 single nucleotide variants. The most common ESBL producer in humans was Salmonella Infantis carrying blaCTX-M-65, which has since emerged in poultry in other countries. There were few instances of similar isolates and plasmids, suggesting that domestic animals and retail meat might have been minor reservoirs of ESBL-producing Salmonella for human infection.

[1]  Jessica C. Chen,et al.  Correlation between Phenotypic and In Silico Detection of Antimicrobial Resistance in Salmonella enterica in Canada Using Staramr , 2022, Microorganisms.

[2]  Gemma C. Langridge,et al.  Characterization of a pESI-like plasmid and analysis of multidrug-resistant Salmonella enterica Infantis isolates in England and Wales , 2021, Microbial genomics.

[3]  M. J. Pons,et al.  Dissemination of a multidrug resistant CTX-M-65 producer Salmonella enterica serovar Infantis clone between marketed chicken meat and children. , 2021, International journal of food microbiology.

[4]  T. Dottorini,et al.  Epidemiological Study on Prevalence, Serovar Diversity, Multidrug Resistance, and CTX-M-Type Extended-Spectrum β-Lactamases of Salmonella spp. from Patients with Diarrhea, Food of Animal Origin, and Pets in Several Provinces of China , 2020, Antimicrobial Agents and Chemotherapy.

[5]  P. Leekitcharoenphon,et al.  Molecular epidemiology of Salmonella Infantis in Europe: insights into the success of the bacterial host and its parasitic pESI-like megaplasmid , 2020, Microbial genomics.

[6]  Samir N. Patel,et al.  Importation of Extensively Drug-Resistant Salmonella enterica Serovar Typhi Cases in Ontario, Canada , 2020, Antimicrobial Agents and Chemotherapy.

[7]  K. Kazmierczak,et al.  Longitudinal analysis of ESBL and carbapenemase carriage among Enterobacterales and Pseudomonas aeruginosa isolates collected in Europe as part of the International Network for Optimal Resistance Monitoring (INFORM) global surveillance programme, 2013-17. , 2020, The Journal of antimicrobial chemotherapy.

[8]  H. Giamarellou,et al.  Carbapenem-Sparing Strategies for ESBL Producers: When and How , 2020, Antibiotics.

[9]  Ayenew Molla Lakew,et al.  The global burden of non-typhoidal salmonella invasive disease: a systematic analysis for the Global Burden of Disease Study 2017 , 2019, The Lancet. Infectious diseases.

[10]  Jerome H. Kim,et al.  Multicountry Distribution and Characterization of Extended-spectrum β-Lactamase–associated Gram-negative Bacteria From Bloodstream Infections in Sub-Saharan Africa , 2019, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[11]  F. Baquero,et al.  Defining and combating antibiotic resistance from One Health and Global Health perspectives , 2019, Nature Microbiology.

[12]  G. Peirano,et al.  Extended-Spectrum β-Lactamase-Producing Enterobacteriaceae: Update on Molecular Epidemiology and Treatment Options , 2019, Drugs.

[13]  M. Mulvey,et al.  Dramatic rise in the proportion of ESBL-producing Escherichia coli and Klebsiella pneumoniae among clinical isolates identified in Canadian hospital laboratories from 2007 to 2016. , 2019, The Journal of antimicrobial chemotherapy.

[14]  M. Webber,et al.  The Emergence of Chromosomally Located blaCTX-M-55 in Salmonella From Foodborne Animals in China , 2019, Front. Microbiol..

[15]  D. Boxrud,et al.  Circulation of Plasmids Harboring Resistance Genes to Quinolones and/or Extended-Spectrum Cephalosporins in Multiple Salmonella enterica Serotypes from Swine in the United States , 2019, Antimicrobial Agents and Chemotherapy.

[16]  Jessica C. Chen,et al.  CTX-M-65 Extended-Spectrum β-Lactamase–Producing Salmonella enterica Serotype Infantis, United States , 2018, Emerging infectious diseases.

[17]  Mohammad Hossein Khosravi,et al.  Global, regional, and national age-sex-specific mortality for 282 causes of death in 195 countries and territories, 1980–2017: a systematic analysis for the Global Burden of Disease Study 2017 , 2018, Lancet.

[18]  A. Bharat,et al.  Characterization of a colistin-resistant Salmonella enterica 4,[5],12:i:- harbouring mcr-3.2 on a variant IncHI-2 plasmid identified in Canada. , 2018, Journal of Medical Microbiology.

[19]  K. Bush,et al.  Past and Present Perspectives on β-Lactamases , 2018, Antimicrobial Agents and Chemotherapy.

[20]  J. Crump,et al.  2017 Infectious Diseases Society of America Clinical Practice Guidelines for the Diagnosis and Management of Infectious Diarrhea. , 2017, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[21]  Z. Shao,et al.  Characterization and Distribution of the autB Gene in Neisseria meningitidis , 2017, Front. Cell. Infect. Microbiol..

[22]  P. Hawkey,et al.  Global epidemiology of CTX-M &bgr;-lactamases: temporal and geographical shifts in genotype , 2017, The Journal of antimicrobial chemotherapy.

[23]  O. Lund,et al.  PointFinder: a novel web tool for WGS-based detection of antimicrobial resistance associated with chromosomal point mutations in bacterial pathogens , 2017, The Journal of antimicrobial chemotherapy.

[24]  Jessica C. Chen,et al.  Comparative Analysis of Extended-Spectrum-β-Lactamase CTX-M-65-Producing Salmonella enterica Serovar Infantis Isolates from Humans, Food Animals, and Retail Chickens in the United States , 2017, Antimicrobial Agents and Chemotherapy.

[25]  Ryan R. Wick,et al.  Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads , 2016, bioRxiv.

[26]  Robert G. Beiko,et al.  SNVPhyl: a single nucleotide variant phylogenomics pipeline for microbial genomic epidemiology , 2016, bioRxiv.

[27]  Mónica Cartelle Gestal,et al.  Characterization of a small outbreak of Salmonella enterica serovar Infantis that harbour CTX-M-65 in Ecuador , 2016, The Brazilian journal of infectious diseases : an official publication of the Brazilian Society of Infectious Diseases.

[28]  S. Karanika,et al.  Fecal Colonization With Extended-spectrum Beta-lactamase-Producing Enterobacteriaceae and Risk Factors Among Healthy Individuals: A Systematic Review and Metaanalysis. , 2016, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[29]  Liangliang Xu,et al.  CTX-M-27 Producing Salmonella enterica Serotypes Typhimurium and Indiana Are Prevalent among Food-Producing Animals in China , 2016, Front. Microbiol..

[30]  Rene S. Hendriksen,et al.  Emergence of a Clonal Lineage of Multidrug-Resistant ESBL-Producing Salmonella Infantis Transmitted from Broilers and Broiler Meat to Humans in Italy between 2011 and 2014 , 2015, PloS one.

[31]  Rob J. L. Willems,et al.  Dissemination of Cephalosporin Resistance Genes between Escherichia coli Strains from Farm Animals and Humans by Specific Plasmid Lineages , 2014, PLoS genetics.

[32]  Shaohua Zhao,et al.  Occurrence of β-lactamase genes among non-Typhi Salmonella enterica isolated from humans, food animals, and retail meats in the United States and Canada. , 2013, Microbial drug resistance.

[33]  S. Rasmussen,et al.  Identification of acquired antimicrobial resistance genes , 2012, The Journal of antimicrobial chemotherapy.

[34]  Sergey I. Nikolenko,et al.  SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing , 2012, J. Comput. Biol..

[35]  M. Mulvey,et al.  New Delhi Metallo-β-Lactamase in Klebsiella pneumoniae and Escherichia coli, Canada , 2011, Emerging infectious diseases.

[36]  J. Folster,et al.  CTX-M–producing Non-Typhi Salmonella spp. Isolated from Humans, United States , 2011, Emerging infectious diseases.

[37]  E. Barzilay,et al.  Salmonella isolates with decreased susceptibility to extended-spectrum cephalosporins in the United States. , 2010, Foodborne pathogens and disease.

[38]  K. Mizobuchi,et al.  Complete genome sequence of the incompatibility group I1 plasmid R64. , 2010, Plasmid.

[39]  O. Gascuel,et al.  New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. , 2010, Systematic biology.