Characterization and whole genome sequencing of closely related multidrug-resistant Salmonella enterica serovar Heidelberg isolates from imported poultry meat in the Netherlands

• Published in: PloS one Vol. 14; no. 7; p. e0219795
• Main Authors: van den Berg, Redmar R, Dissel, Serge, Rapallini, Michel L B A, van der Weijden, Coen C, Wit, Ben, Heymans, Raymond
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 22.07.2019; Public Library of Science (PLoS)
• Subjects: Animals; Anti-Bacterial Agents - pharmacology; Antibiotics; Antiinfectives and antibacterials; Antimicrobial agents; Biology and Life Sciences; Cefotaxime; Ceftazidime; Cephalosporins; Chickens; Ciprofloxacin; Cladistic analysis; Cluster Analysis; Drug resistance; Drug Resistance, Multiple, Bacterial - drug effects; Drug Resistance, Multiple, Bacterial - genetics; Epidemiology; Food; Gene sequencing; Genes, Bacterial; Genetic aspects; Genomes; Geographical distribution; Geographical locations; Health risks; Identification; Incompatibility; Laboratories; Meat; Meat - microbiology; Medicine and Health Sciences; Multidrug resistance; Multidrug resistant organisms; Multilocus Sequence Typing; Netherlands; Nucleotides; People and places; Phenotypes; Phylogeny; Plasmids; Polymorphism, Single Nucleotide - genetics; Poultry; Poultry (Animals); Poultry - microbiology; Product safety; Public health; Risk factors; Salmonella; Salmonella enterica; Salmonella enterica - drug effects; Salmonella enterica - genetics; Salmonella enterica - isolation & purification; Salmonellosis; Serogroup; Single-nucleotide polymorphism; Surveillance; Whole Genome Sequencing; β Lactamase; Netherlands; South America; Brazil; Argentina; United States > US; North America
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0219795

Multidrug-resistant Salmonella enterica serovar Heidelberg isolates are frequently recovered in the Netherlands from poultry meat imported from South America. Our aim was to retrospectively assess the characteristics of the antimicrobial determinants, gene content and the clonal relatedness of 122 unique S. Heidelberg isolates from chicken meat from Brazil (n = 119) and Argentina (n = 3) that were imported between 2010 and 2015. These isolates were subjected to antimicrobial susceptibility testing, PCR and Illumina HiSeq2500 whole genome sequencing. Draft genomes were assembled to assess the gene content, and the phylogenetic relationships between isolates were determined using single nucleotide polymorphisms. Ciprofloxacin-resistance was identified in 98.4% of the isolates and 83.7% isolates showed resistance to the extended-spectrum cephalosporins cefotaxime and ceftazidime (83.6% and 82.8% respectively). Of the latter, 97.1% exhibited an AmpC phenotype and contained blaCMY-2, whereas the remaining three isolates contained an extended spectrum beta-lactamase. Of the 99 extended-spectrum cephalosporins-resistant isolates harboring CMY-2 plasmids, 56.6% contained the incompatibility group I1 replicon. Phylogenetic cluster analysis showed that all isolates from Brazil clustered together, with 49% occurring in clusters larger than 5 isolates that revealed intra-cluster similarities based on geographical location and/or resistance profiles. The remaining isolates were classified in smaller clusters or as singletons, highlighting the large diversity of S. Heidelberg in the poultry chain in Brazil that was revealed by this study. Considering the potential public health risk associated with multidrug-resistant S. Heidelberg in imported poultry, collaborative whole genome sequencing-based surveillance is needed to monitor the spread, pathogenic properties and epidemiological distribution of these isolates.