Population dynamics and antimicrobial resistance of Salmonella Derby ST40 from Shenzhen, China

Salmonella enterica subsp. enterica serovar Derby (S. Derby) is one of the most common serotypes responsible for salmonellosis in humans and animals. The two main sequence types (ST) observed in China are ST40 and ST71, with ST40 presently being the most common in Shenzhen. Recent years have seen an increasing number of cases of salmonella caused by ST40 S. Derby, but the epidemiology is not clear. We gathered 314 ST40 S. Derby isolates from food and patient samples for 11 years in Shenzhen; 76 globally prevalent representative strains were also collected. Whole-genome sequencing (WGS) combined with drug resistance phenotyping was used to examine population structural changes, inter-host associations, drug resistance characteristics, and the food-transmission risks of ST40 S. Derby in Shenzhen over this period. The S. enterica evolutionary tree is divided into five clades, and the strains isolated in Shenzhen were primarily concentrated in Clades 2, 4, and 5, and thus more closely related to strains from Asian (Thailand and Vietnam) than European countries. Our 11-year surveillance of S. Derby in Shenzhen showed that Clades 2, 4, and 5 are now the dominant epidemic branches, and branches 2 and 5 are heavily multi-drug resistant. The main resistance pattern is ampicillin-tetracycline-ciprofloxacin-chloramphenicol-nalidixic acid-streptomycin-sulfamethoxazole/trimethoprim. This may lead to a trend of increasing resistance to ST40 S. Derby in Shenzhen. Using a segmentation of ≤3 SNP among clone clusters, we discovered that Clades 2 and 4 contained multiple clonal clusters of both human- and food-derived strains. The food-derived strains were mainly isolated from pig liver, suggesting this food has a high risk of causing disease outbreaks in Shenzhen.

[1]  Ruifu Yang,et al.  Outbreak dynamics of foodborne pathogen Vibrio parahaemolyticus over a seventeen year period implies hidden reservoirs , 2022, Nature Microbiology.

[2]  P. Bork,et al.  Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation , 2021, Nucleic Acids Res..

[3]  Simon D.W. Frost,et al.  The Bacteria Genome Pipeline (BAGEP): an automated, scalable workflow for bacteria genomes with Snakemake , 2020, PeerJ.

[4]  M. Allard,et al.  Antimicrobial resistance and related gene analysis of Salmonella from egg and chicken sources by whole-genome sequencing , 2020, Poultry science.

[5]  Ruth E. Timme,et al.  Optimizing open data to support one health: best practices to ensure interoperability of genomic data from bacterial pathogens , 2020, One Health Outlook.

[6]  Yujun Cui,et al.  Whole-Genome Analysis of Salmonella enterica Serovar Enteritidis Isolates in Outbreak Linked to Online Food Delivery, Shenzhen, China, 2018 , 2020, Emerging infectious diseases.

[7]  R. Uemura,et al.  IncI1 Plasmid Associated with blaCTX-M-2 Transmission in ESBL-Producing Escherichia coli Isolated from Healthy Thoroughbred Racehorse, Japan , 2020, Antibiotics.

[8]  H. Hasman,et al.  PlasmidFinder and In Silico pMLST: Identification and Typing of Plasmid Replicons in Whole-Genome Sequencing (WGS). , 2020, Methods in molecular biology.

[9]  M. Achtman,et al.  The EnteroBase user's guide, with case studies on Salmonella transmissions, Yersinia pestis phylogeny, and Escherichia core genomic diversity , 2019, Genome research.

[10]  M. Denis,et al.  Experimental infection of pigs by Salmonella Derby, S. Typhimurium and monophasic variant of S. Typhimurium: Comparison of colonization and serology. , 2019, Veterinary microbiology.

[11]  Jerome H. Kim,et al.  The global burden and epidemiology of invasive non-typhoidal Salmonella infections , 2018, Human vaccines & immunotherapeutics.

[12]  S. le Hello,et al.  Complete Genome Sequence of Salmonella enterica subsp. enterica Serotype Derby, Associated with the Pork Sector in France , 2018, Microbiology Resource Announcements.

[13]  W. Rabsch,et al.  Evaluation of WGS based approaches for investigating a food-borne outbreak caused by Salmonella enterica serovar Derby in Germany. , 2017, Food microbiology.

[14]  K. Nagy,et al.  The European Union summary report on trends and sources of zoonoses, zoonotic agents and food‐borne outbreaks in 2016 , 2017, EFSA journal. European Food Safety Authority.

[15]  Z. Pan,et al.  Subtyping Salmonella enterica serovar Derby with multilocus sequence typing (MLST) and clustered regularly interspaced short palindromic repeats (CRISPRs) , 2017 .

[16]  R. Kaas,et al.  Is the Evolution of Salmonella enterica subsp. enterica Linked to Restriction-Modification Systems? , 2016, mSystems.

[17]  Z. Pan,et al.  Phenotypic characteristics and genotypic correlation between Salmonella isolates from a slaughterhouse and retail markets in Yangzhou, China. , 2016, International journal of food microbiology.

[18]  Ruth Timme,et al.  Practical Value of Food Pathogen Traceability through Building a Whole-Genome Sequencing Network and Database , 2016, Journal of Clinical Microbiology.

[19]  Z. Pan,et al.  Salmonella isolated from the slaughterhouses and correlation with pork contamination in free market , 2016 .

[20]  Michael J. Palumbo,et al.  Characterization of Foodborne Outbreaks of Salmonella enterica Serovar Enteritidis with Whole-Genome Sequencing Single Nucleotide Polymorphism-Based Analysis for Surveillance and Outbreak Detection , 2015, Journal of Clinical Microbiology.

[21]  Jacqueline A. Keane,et al.  Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins , 2014, Nucleic acids research.

[22]  A. von Haeseler,et al.  IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies , 2014, Molecular biology and evolution.

[23]  Björn Usadel,et al.  Trimmomatic: a flexible trimmer for Illumina sequence data , 2014, Bioinform..

[24]  J. Bray,et al.  MLST revisited: the gene-by-gene approach to bacterial genomics , 2013, Nature Reviews Microbiology.

[25]  Alexey A. Gurevich,et al.  QUAST: quality assessment tool for genome assemblies , 2013, Bioinform..

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

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

[28]  Xingfen Yang,et al.  Laboratory-based surveillance of non-typhoidal Salmonella infections in Guangdong Province, China. , 2012, Foodborne pathogens and disease.

[29]  W. Rabsch,et al.  Diversity of Salmonella enterica serovar Derby isolated from pig, pork and humans in Germany. , 2011, International journal of food microbiology.

[30]  Zijian Feng,et al.  Laboratory-based surveillance of nontyphoidal Salmonella infections in China. , 2011, Foodborne pathogens and disease.

[31]  E. Nielsen,et al.  Association between phylogeny, virulence potential and serovars of Salmonella enterica. , 2010, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[32]  Aamir Fazil,et al.  The global burden of nontyphoidal Salmonella gastroenteritis. , 2010, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[33]  Xianghui Liang,et al.  Novel CTX-M {beta}-lactamase genotype distribution and spread into multiple species of Enterobacteriaceae in Changsha, Southern China. , 2009, The Journal of antimicrobial chemotherapy.

[34]  Adam P. Arkin,et al.  FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix , 2009, Molecular biology and evolution.

[35]  S. Simjee,et al.  A pan-European survey of antimicrobial susceptibility towards human-use antimicrobial drugs among zoonotic and commensal enteric bacteria isolated from healthy food-producing animals. , 2009, The Journal of antimicrobial chemotherapy.

[36]  Ziyong Sun,et al.  Characterization of Salmonella enterica isolates from infants and toddlers in Wuhan, China. , 2008, The Journal of antimicrobial chemotherapy.

[37]  J. Castañon,et al.  History of the use of antibiotic as growth promoters in European poultry feeds. , 2007, Poultry science.

[38]  F. Weill,et al.  WHO Collaborating Centre for Reference and Research on Salmonella ANTIGENIC FORMULAE OF THE SALMONELLA SEROVARS , 2007 .

[39]  Richard J Zeckhauser,et al.  Antibiotic resistance as a global threat: Evidence from China, Kuwait and the United States , 2006, Globalization and health.

[40]  I. Lasa,et al.  BapA, a large secreted protein required for biofilm formation and host colonization of Salmonella enterica serovar Enteritidis , 2005, Molecular microbiology.

[41]  Mi-jin Lee,et al.  Identification of Salmonella gallinarum virulence genes in a chicken infection model using PCR-based signature-tagged mutagenesis. , 2005, Microbiology.

[42]  S. Herrera-León,et al.  Salmonella Derby Clonal Spread from Pork , 2005, Emerging infectious diseases.

[43]  C. Chiu,et al.  Antimicrobial resistance in nontyphoid Salmonella serotypes: a global challenge. , 2004, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[44]  J. Rodríguez,et al.  Available options in the management of non-typhi Salmonella , 2004, Expert opinion on pharmacotherapy.

[45]  M. Barza Potential mechanisms of increased disease in humans from antimicrobial resistance in food animals. , 2002, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[46]  C. Solano,et al.  Bap, a Staphylococcus aureus Surface Protein Involved in Biofilm Formation , 2001, Journal of bacteriology.

[47]  E. Friedman,et al.  AN OUTBREAK OF HOSPITAL-ASSOCIATED INFECTIONS DUE TO SALMONELLA DERBY. , 1963, JAMA.

[48]  R. Mushin An outbreak of gastro-enteritis due to Salmonella derby , 1948, Journal of Hygiene.