Antimicrobial Resistance and Whole-Genome Characterisation of High-Level Ciprofloxacin-Resistant Salmonella Enterica Serovar Kentucky ST 198 Strains Isolated from Human in Poland

Background: Salmonella Kentucky belongs to zoonotic serotypes that demonstrate that the high antimicrobial resistance and multidrug resistance (including fluoroquinolones) is an emerging problem. To the best of our knowledge, clinical S. Kentucky strains isolated in Poland remain undescribed. Methods: Eighteen clinical S. Kentucky strains collected in the years 2018–2019 in Poland were investigated. All the strains were tested for susceptibility to 11 antimicrobials using the disc diffusion and E-test methods. Whole genome sequences were analysed for antimicrobial resistance genes, mutations, the presence and structure of SGI1-K (Salmonella Genomic Island and the genetic relationship of the isolates. Results: Sixteen of 18 isolates (88.9%) were assigned as ST198 and were found to be high-level resistant to ampicillin (>256 mg/L) and quinolones (nalidixic acid MIC ≥ 1024 mg/L, ciprofloxacin MIC range 6–16 mg/L). All the 16 strains revealed three mutations in QRDR of GyrA and ParC. The substitutions of Ser83 → Phe and Asp87 → Tyr of the GyrA subunit and Ser80→Ile of the ParC subunit were the most common. One S. Kentucky isolate had qnrS1 in addition to the QRDR mutations. Five of the ST198 strains, grouped in cluster A, had multiple resistant determinants like blaTEM1-B, aac(6′)-Iaa, sul1 or tetA, mostly in SGI1 K. Seven strains, grouped in cluster B, had shorter SGI1-K with deletions of many regions and with few resistance genes detected. Conclusion: The results of this study demonstrated that a significant part of S. Kentucky isolates from humans in Poland belonged to ST198 and were high-level resistant to ampicillin and quinolones.

[1]  The European Union Summary Report on Antimicrobial Resistance in zoonotic and indicator bacteria from humans, animals and food in 2019–2020 , 2022, EFSA journal. European Food Safety Authority.

[2]  Rongchang Chen,et al.  National Prevalence of Salmonella enterica Serotype Kentucky ST198 with High-Level Resistance to Ciprofloxacin and Extended-Spectrum Cephalosporins in China, 2013 to 2017 , 2021, mSystems.

[3]  R. Kaas,et al.  ResFinder 4.0 for predictions of phenotypes from genotypes , 2020, The Journal of antimicrobial chemotherapy.

[4]  K. Nagy,et al.  The European Union Summary Report on Antimicrobial Resistance in zoonotic and indicator bacteria from humans, animals and food in 2017/2018 , 2020, EFSA journal. European Food Safety Authority.

[5]  A. Sahebkar,et al.  Prevalence of fluoroquinolone-resistant Salmonella serotypes in Iran: a meta-analysis , 2020, Pathogens and global health.

[6]  Junyoung Kim,et al.  The Traveler-associated High-level Ciprofloxacin-resistant Salmonella enterica Serovar Kentucky in the Republic of Korea. , 2019, Journal of global antimicrobial resistance.

[7]  W. Messens,et al.  The European Union One Health 2018 Zoonoses Report , 2019, EFSA journal. European Food Safety Authority.

[8]  P. Courvalin,et al.  Population-based inference of aminoglycoside resistance mechanisms in Escherichia coli , 2019, EBioMedicine.

[9]  S. Baker,et al.  Endemic fluoroquinolone-resistant Salmonella enterica serovar Kentucky ST198 in northern India , 2019, Microbial genomics.

[10]  M. Popowska,et al.  Ciprofloxacin and nalidixic acid resistance of Salmonella spp. isolated from retail food in Poland. , 2018, International journal of food microbiology.

[11]  D. Shah,et al.  Complete Genome Sequence of a Ciprofloxacin-Resistant Salmonella enterica subsp. enterica Serovar Kentucky Sequence Type 198 Strain, PU131, Isolated from a Human Patient in Washington State , 2018, Genome Announcements.

[12]  A. Aseffa,et al.  Molecular epidemiology of fluoroquinolone resistant Salmonella in Africa: A systematic review and meta-analysis , 2018, PloS one.

[13]  P. Fey,et al.  Nontyphoidal Salmonella enterica Nonsusceptible to Both Levofloxacin and Ceftriaxone in Nebraska, United States 2014-2015. , 2018, Foodborne pathogens and disease.

[14]  M. Ouellette,et al.  Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis. , 2017, The Lancet. Infectious diseases.

[15]  Khalil Abudahab,et al.  Microreact: visualizing and sharing data for genomic epidemiology and phylogeography , 2016, Microbial genomics.

[16]  C. H. Camargo,et al.  Presence of plasmid-mediated quinolone resistance determinants and mutations in gyrase and topoisomerase in Salmonella enterica isolates with resistance and reduced susceptibility to ciprofloxacin. , 2016, Diagnostic microbiology and infectious disease.

[17]  N. Speybroeck,et al.  World Health Organization Global Estimates and Regional Comparisons of the Burden of Foodborne Disease in 2010 , 2015, PLoS medicine.

[18]  S. Kariuki,et al.  Antimicrobial resistance and management of invasive Salmonella disease. , 2015, Vaccine.

[19]  Yanlong Yin,et al.  Salmonella Serotype Determination Utilizing High-Throughput Genome Sequencing Data , 2015, Journal of Clinical Microbiology.

[20]  R. Kaas,et al.  Solving the Problem of Comparing Whole Bacterial Genomes across Different Sequencing Platforms , 2014, PloS one.

[21]  A. Hoszowski,et al.  Prevalence and characterisation of quinolone resistance mechanisms in Salmonella spp. , 2014, Veterinary microbiology.

[22]  W. Rabsch,et al.  The global establishment of a highly-fluoroquinolone resistant Salmonella enterica serotype Kentucky ST198 strain , 2013, Front. Microbiol..

[23]  M. Magnani,et al.  Plasmid-mediated quinolone resistance (PMQR) and mutations in the topoisomerase genes of Salmonella enterica strains from Brazil , 2013, Brazilian journal of microbiology : [publication of the Brazilian Society for Microbiology].

[24]  S. le Hello,et al.  Genetic lineages of Salmonella enterica serovar Kentucky spreading in pet reptiles. , 2013, Veterinary microbiology.

[25]  G. Horsman,et al.  Ciprofloxacin-Resistant Salmonella enterica Serovar Kentucky in Canada , 2013, Emerging infectious diseases.

[26]  F. Weill,et al.  Early Strains of Multidrug-Resistant Salmonella enterica Serovar Kentucky Sequence Type 198 from Southeast Asia Harbor Salmonella Genomic Island 1-J Variants with a Novel Insertion Sequence , 2012, Antimicrobial Agents and Chemotherapy.

[27]  A. Hoszowski,et al.  First isolation of ESBL-producing Salmonella and emergence of multiresistant Salmonella Kentucky in turkey in Poland , 2012 .

[28]  Ole Lund,et al.  Multilocus Sequence Typing of Total-Genome-Sequenced Bacteria , 2012, Journal of Clinical Microbiology.

[29]  Mina Kim,et al.  Prevalence of plasmid-mediated quinolone resistance and mutations in the gyrase and topoisomerase IV genes in Salmonella isolated from 12 tertiary-care hospitals in Korea. , 2011, Microbial drug resistance.

[30]  J. Wain,et al.  International spread of an epidemic population of Salmonella enterica serotype Kentucky ST198 resistant to ciprofloxacin. , 2011, The Journal of infectious diseases.

[31]  S. Djordjevic,et al.  SGI1-K, a Variant of the SGI1 Genomic Island Carrying a Mercury Resistance Region, in Salmonella enterica Serovar Kentucky , 2006, Antimicrobial Agents and Chemotherapy.

[32]  F. Weill,et al.  Ciprofloxacin-resistant Salmonella Kentucky in Travelers , 2006, Emerging infectious diseases.

[33]  K. Holt,et al.  The complete sequence of Salmonella genomic island SGI1-K. , 2015, The Journal of antimicrobial chemotherapy.