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Correct species identification (reclassification in CNCTC) of strains of Staphylococcus intermedius-group can improve an insight into their evolutionary history

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Abstract

A group of 59 putative strains of Staphylococcus intermedius/Staphylococcus pseudintermedius deposited in the Czech National Collection of Type Cultures (CNCTC, National Institute for Public Health, Prague, Czech Republic) and the National Reference Laboratory for Staphylococci (NRL for Staphylococci, National Institute for Public Health, Prague, Czech Republic) was reclassified using polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP). There the biggest human collection of S. pseudintermedius in Europe was analysed; 44 samples (75%) were of human origin. Twenty-two percent (n = 13) of the strains were isolated from animals, and two staphylococci were of unknown origin. This study revealed the prevalence of Staphylococcus pseudintermedius (94%, n = 53) vs. Staphylococcus intermedius (6%, n = 6) in the collection of human and veterinary staphylococci after reclassification. Results of PCR-RFLP analysis were verified by comparison with a repetitive element sequence-based polymerase chain reaction (Rep-PCR) analysis on 26 (44%) randomly selected strains. Due to a low-resolution ability of PCR-RFLP to separate Staphylococcus intermedius from Staphylococcus delphini, four isolates of Staphylococcus intermedius were biochemically verified further to exclude the presence of Staphylococcus delphini in the collection. Our results indicate that S. intermedius and S. pseudintermedius have occurred independently over an age-long period of their co-evolution.

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References

  • Bannoehr J, Ben Zakour NL, Waller AS, Guardabassi L, Thoday KL, van den Broek AHM, Fitzgerald JR (2007) Population genetic structure of the Staphylococcus intermedius group: insights into agr diversification and the emergence of methicillin-resistant strains. J Bacteriol 189:8685–8692. https://doi.org/10.1128/JB.01150-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bannoehr J, Franco A, Iurescia M, Battisti A, Fitzgerald JR (2009) Molecular diagnostic identification of Staphylococcus pseudintermedius. J Clin Microbiol 47:469–471. https://doi.org/10.1128/JCM.01915-08

    Article  CAS  PubMed  Google Scholar 

  • Ben Zakour NL, Beatson SA, van den Broek AHM, Thoday KL, Fitzgerald JR (2012) Comparative genomics of the Staphylococcus intermedius Group of Animal Pathogens. Front Cell Infect Microbiol 2:44. https://doi.org/10.3389/fcimb.2012.00044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bond R, Loeffler A (2012) What’s happened to Staphylococcus intermedius? Taxonomic revision and emergence of multi-drug resistance. J Small Anim Pract 53:147–154

    Article  CAS  PubMed  Google Scholar 

  • Chrobak D, Kizerwetter-Świda M, Rzewuska M, Moodley A, Guardabassi L, Binek M (2011) Molecular characterization of Staphylococcus pseudintermedius strains isolated from clinical samples of animal origin. Folia Microbiol (Praha) 56:415–422

    Article  CAS  Google Scholar 

  • Devriese LA, Vancanneyt M, Baele M et al (2005) Staphylococcus pseudintermedius sp. nov., a coagulase-positive species from animals. Int J Syst Evol Microbiol 55:1569–1573. https://doi.org/10.1099/ijs.0.63413-0

    Article  CAS  PubMed  Google Scholar 

  • Devriese LA, Hermans K, Baele M, Haesebrouck F (2009) Staphylococcus pseudintermedius versus Staphylococcus intermedius. Vet Microbiol 133:206–207. https://doi.org/10.1016/J.VETMIC.2008.06.002

    Article  PubMed  Google Scholar 

  • Fitzgerald JR (2009) The Staphylococcus intermedius group of bacterial pathogens: species re-classification, pathogenesis and the emergence of methicillin resistance. Vet Dermatol 20:490–495. https://doi.org/10.1111/j.1365-3164.2009.00828.x

    Article  PubMed  Google Scholar 

  • Hájek V (1976) Staphylococcus intermedius, a new species isolated from animals. Int J Syst Bacteriol 26(4):401–408

    Article  Google Scholar 

  • Jorgensen JH, Pfaller MA, Carrroll k LML, Funke G, Richter S, Warnock DW (2015) Manual of clinical microbiology. ASM Press, Washington

    Google Scholar 

  • Kmieciak W, Szewczyk EM (2018) Are zoonotic Staphylococcus pseudintermedius strains a growing threat for humans? Folia Microbiol (Praha)

  • Murugaiyan J, Walther B, Stamm I, Abou-Elnaga Y, Brueggemann-Schwarze S, Vincze S, Wieler LH, Lübke-Becker A, Semmler T, Roesler U (2014) Species differentiation within the Staphylococcus intermedius group using a refined MALDI-TOF MS database. Clin Microbiol Infect 20:1007–1014

    Article  CAS  PubMed  Google Scholar 

  • Olive DM, Bean P (1999) Principles and applications of methods for DNA-based typing of microbial organisms. J Clin Microbiol 37:1661–1669

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pompilio A, DeNicola S, Crocetta V et al (2015) New insights in S. pseudintermedius pathogenicity: antibiotic-resistant biofilm formation by a human wound-associated strain. BMC Microbiol 15:109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruzauskas M, Couto N, Pavilonis A, Klimiene I, Siugzdiniene R, Virgailis M, Vaskeviciute L, Anskiene L, Pomba C (2016) Characterization of Staphylococcus pseudintermedius isolated from diseased dogs in Lithuania. Pol J Vet Sci 19:7–14

    Article  CAS  PubMed  Google Scholar 

  • Sasaki T, Kikuchi K, Tanaka Y, Takahashi N, Kamata S, Hiramatsu K (2007) Reclassification of phenotypically identified Staphylococcus intermedius strains. J Clin Microbiol 45:2770–2778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sasaki T, Tsubakishita S, Tanaka Y, Sakusabe A, Ohtsuka M, Hirotaki S, Kawakami T, Fukata T, Hiramatsu K (2010) Multiplex-PCR method for species identification of coagulase-positive staphylococci. J Clin Microbiol 48:765–769

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slettemeås JS, Mikalsen J, Sunde M (2010) Further diversity of the Staphylococcus intermedius group and heterogeneity in the MboI restriction site used for Staphylococcus pseudintermedius species identification. J Vet Diagn Investig 22:756–759

    Article  Google Scholar 

  • Somayaji R, Priyantha MA, Rubin JE (2016) Human infection due to S. pseudintermedius, as an emerging zoonosis of canine origin: report of 24 cases. Diagn Microbiol Infect Dis 85(4):471–476

    Article  CAS  PubMed  Google Scholar 

  • Starlander G, Börjesson S, Grönlund-Andersson U et al (2014) Cluster of infections caused by methicillin-resistant Staphylococcus pseudintermedius in humans in a tertiary hospital. J Clin Microbiol 52:3118–3120

    Article  PubMed  PubMed Central  Google Scholar 

  • Stegmann R, Burnens A, Maranta CA, Perreten V (2010) Human infection associated with methicillin-resistant Staphylococcus pseudintermedius ST71. J Antimicrob Chemother 65:2047–2048

    Article  CAS  PubMed  Google Scholar 

  • Švec P, Pantůček R, Petráš P, Sedláček I, Nováková D (2010) Identification of Staphylococcus spp. using (GTG)5-PCR fingerprinting. Syst Appl Microbiol 33:451–456

    Article  CAS  PubMed  Google Scholar 

  • Tabit FT (2016) Advantages and limitations of potential methods for the analysis of bacteria in milk: a review. J Food Sci Technol 53:42–49

    Article  CAS  PubMed  Google Scholar 

  • Van Hoovels L, Vankeerberghen A, Boel A et al (2006) First case of Staphylococcus pseudintermedius infection in a human. J Clin Microbiol 44:4609–4612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Varaldo PE, Kilpper-Balz R, Biavasco F et al (1988) Staphylococcus delphini sp. nov., a coagulase-positive species isolated from dolphins. Int J Syst Bacteriol 38:436–439

    Article  Google Scholar 

  • Ventrella G, Moodley A, Grandolfo E, Parisi A, Corrente M, Buonavoglia D, Guardabassi L (2017) Frequency, antimicrobial susceptibility and clonal distribution of methicillin-resistant Staphylococcus pseudintermedius in canine clinical samples submitted to a veterinary diagnostic laboratory in Italy: a 3-year retrospective investigation. Vet Microbiol 211:103–106

    Article  CAS  PubMed  Google Scholar 

  • Viau R, Hujer AM, Hujer KM et al (2015) Are Staphylococcus intermedius infections in humans cases of mistaken identity? A case series and literature review. Open Forum Infect Dis 2:ofv110

    Article  PubMed  PubMed Central  Google Scholar 

  • Zubeir IEME, Kanbar T, Alber J et al (2007) Phenotypic and genotypic characteristics of methicillin/oxacillin-resistant Staphylococcus intermedius isolated from clinical specimens during routine veterinary microbiological examinations. Vet Microbiol 121:170–176

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank Pavel Švec, Ph.D., from the Czech Collection of Microorganisms (Brno, Czech Republic) for Rep-PCR analysis of staphylococci.

Funding

This project was supported by MH CZ-DRO (“The National Institute of Public Health-NIPH, 75010330”) and SVV 260398.

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Authors and Affiliations

  1. National Reference Laboratory for Antibiotics, National Institute of Public Health, Prague, Czech Republic

    Lucia Mališová, Helena Žemličková & Vladislav Jakubů

  2. Czech National Collection of Type Cultures, National Institute of Public Health, Prague, Czech Republic

    Renáta Šafránková

  3. Faculty of Medicine in Hradec Králové, Charles University, Hradec Králové, Czech Republic

    Renáta Šafránková, Helena Žemličková & Vladislav Jakubů

  4. National Reference Laboratory for Staphylococci, National Institute of Public Health, Prague, Czech Republic

    Jana Kekláková & Petr Petráš

Authors
  1. Lucia Mališová
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  2. Renáta Šafránková
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  3. Jana Kekláková
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  4. Petr Petráš
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  5. Helena Žemličková
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  6. Vladislav Jakubů
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Correspondence to Lucia Mališová.

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Mališová, L., Šafránková, R., Kekláková, J. et al. Correct species identification (reclassification in CNCTC) of strains of Staphylococcus intermedius-group can improve an insight into their evolutionary history. Folia Microbiol 64, 231–236 (2019). https://doi.org/10.1007/s12223-018-0647-7

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  • DOI: https://doi.org/10.1007/s12223-018-0647-7

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