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Biofilm formation on tympanostomy tubes depends on methicillin-resistant Staphylococcus aureus genetic lineage

European Archives of Oto-Rhino-Laryngology volume 273, pages 615–620 (2016)Cite this article

Abstract

Bacterial biofilm formation has been implicated in the high incidence of persistent otorrhoea after tympanostomy tube insertion. The aim of the study was to investigate whether biofilm formation on tympanostomy tubes depends on the genetic profile of methicillin-resistant Staphylococcus aureus (MRSA) strains. Capacity of biofilm formation on fluoroplastic tympanostomy tubes (TTs) was tested on 30 MRSA strains. Identification and methicillin resistance were confirmed by PCR for nuc and mecA genes. Strains were genotypically characterised (SCCmec, agr and spa typing). Biofilm formation was tested in microtiter plate and on TTs. Tested MRSA strains were classified into SCCmec type I (36.7 %), III (23.3 %), IV (26.7 %) and V (13.3 %), agr type I (50 %), II (36.7 %) and III (13.3 %), and 5 clonal complexes (CCs). All tested MRSA strains showed ability to form biofilm on microtiter plate. Capacity of biofilm formation on TTs was as following: 13.3 % of strains belonged to the category of no biofilm producers, 50 % to the category of weak biofilm producers and 36.7 % to moderate biofilm producers. There was a statistically significant difference between CC, SCCmec and agr types and the category of biofilm production on TTs tubes (p < 0.001): CC5, SCCmecI type and agrII type with a moderate amount of biofilm, and CC8 and agrI type with a low amount of biofilm. Biofilm formation by MRSA on TTs is highly dependent on genetic characteristics of the strains. Therefore, MRSA genotyping may aid the determination of the possibility of biofilm-related post-tympanostomy tube otorrhea.

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References

  1. Oberman JP, Derkay CS (2004) Posttympanostomy tube otorrhea. Am J Otolaryngol 25:110–117

    Article  PubMed  Google Scholar 

  2. Park H, Jang CH, Cho YB, Choi CH (2007) Antibacterial effect of tea-tree oil on methicillin-resistant Staphylococcus aureus biofilm formation of the tympanostomy tube: an in vitro study. In vivo 21:1027–1030

    PubMed  Google Scholar 

  3. Wang JC, Hamood AN, Saadeh C, Cunningham MJ, Yim MT, Cordero J (2014) Strategies to prevent biofilm-based tympanostomy tube infections. Int J Pediatr Otorhinolaryngol 78:1433–1438

    Article  PubMed  Google Scholar 

  4. Lee EJ, Kwon JH, Park AY, Lee WS, Son EJ (2012) Nasal colonization of methicillin-resistant Staphylococcus aureus in patients with chronic suppurative otitis media. Korean J Audiol 16:75–79

    PubMed Central  Article  PubMed  Google Scholar 

  5. Moellering RC (2012) MRSA: the first half century. J Antimicrob Chemother 67:4–11

    Article  CAS  PubMed  Google Scholar 

  6. Gotz F (2002) Staphylococcus and biofilms. Mol Microbiol 43:1367–1378

    Article  CAS  PubMed  Google Scholar 

  7. Hartnick CJ, Shott S, Willging JP, Myer CM III (2000) Methicillin-resistant Staphylococcus aureus otorrhea after tympanostomy tube placement: an emerging concern. Arch Otolaryngol Head Neck Surg 126:1440–1443

    Article  CAS  PubMed  Google Scholar 

  8. Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167–193

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  9. Biedlingmaier JF, Samaranayake R, Whelan P (1998) Resistance to biofilm formation on otologic implant materials. Otolaryngol Head Neck Surg 118:444–445

    CAS  PubMed  Google Scholar 

  10. Barakate M, Beckenham E, Curotta J, Da Cruz M (2007) Bacterial biofilm adherence to middle-ear ventilation tubes: scanning electron micrograph images and literature review. J Laryngol Otol 121:993–997

    Article  CAS  PubMed  Google Scholar 

  11. Boye K, Bartels MD, Andersen IS, Møller JA, Westh H (2007) A new multiplex PCR for easy screening of methicillin-resistant Staphylococcus aureus SCCmec types I-V. Clin Microbiol Infect 13:725–727

    Article  CAS  PubMed  Google Scholar 

  12. Lina G, Boutite F, Tristan A, Bes M, Etienne J, Vandenesch F (2003) Bacterial competition for human nasal cavity colonization: role of Staphylococcal agr alleles. Appl Environ Microbio l69:18–23

  13. Harmsen D, Claus H, Witte W et al (2003) Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol 4:5442–5448

    Article  Google Scholar 

  14. Stepanović S, Vuković D, Hola V et al (2007) Quantification of biofilm microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS 115:891–899

    Article  PubMed  Google Scholar 

  15. Berry JA, Biedlingmaier JF, Whelan PJ (2000) In vitro resistance to bacterial biofilm formation on coated fluoroplastic tympanostomy tubes. Otolaryngol Head Neck Surg 123:246–251

    Article  CAS  PubMed  Google Scholar 

  16. Karlan MS, Mufson RA, Grizzard MB, Buscemi PA, Hench L, Goldberg EP (1981) Potentiation of infections by biomaterials: a comparison of three materials. Otolaryngol Head Neck Surg 89:528–534

    CAS  PubMed  Google Scholar 

  17. Karlan MS, Skobel B, Grizzard M et al (1980) Myringotomy tube materials: bacterial adhesion and infection. Otolaryngol Head Neck Surg 88:783–795

    CAS  PubMed  Google Scholar 

  18. Biedlingmaier JF, Samaranayake R, Whelan P (1997) Resistance to biofilm formation on otologic implant materials. Otolaryngol Head Neck Surg 118:444–451

    Google Scholar 

  19. Fishman I, Sykes KJ, Horvat R, Selvarangan R, Newland J, Wei JL (2011) Demographics and microbiology of otorrhea through patent tubes failing ototopical and/or oral antibiotic therapy. Otolaryngol Head Neck Surg 145:1025–1029

    Article  PubMed  Google Scholar 

  20. Cheng J, Javia L (2012) Methicillin-resistant Staphylococcus aureus (MRSA) pediatric tympanostomy tube otorrhea. Int J Pediatr Otorhinolaryngol 76:1795–1798

    Article  PubMed  Google Scholar 

  21. Wertheim HF, Melles DC, Vos MC et al (2005) The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis 5:751–762

    Article  PubMed  Google Scholar 

  22. Ćirković I, Đukić S, Carević B, Mazić N, Mioljević V, Stepanović S (2014) Methicillin-resistant Staphylococcus aureus nasal carriage among hospitalized patients and healthcare workers in the Clinical Center of Serbia. Arch Biol Sci 66:87–92

    Article  Google Scholar 

  23. Chang J, Lee SH, Choi J, Im GJ, Jung HH (2011) Nasopharynx as a microbiologic reservoir in chronic suppurative otitis media: preliminary study. Clin Exp Otorhinolaryngol 4(3):122–125

    PubMed Central  Article  PubMed  Google Scholar 

  24. Richer SL, Wenig BL (2009) The efficacy of preoperative screening and the treatment of methicillin-resistant Staphylococcus aureus in an otolaryngology surgical practice. Otolaryngol Head Neck Surg 140:29–32

    Article  PubMed  Google Scholar 

  25. Lin CD, Tsai MH, Lin CW et al (2012) Association of adenoid hyperplasia and bacterial biofilm formation in children with adenoiditis in Taiwan. Eur Arch Otorhinolaryngol 269:503–511

    Article  PubMed  Google Scholar 

  26. Smith K, Perez A, Ramage G, Lappin D, Gemmell CG, Lang S (2008) Biofilm formation by Scottish clinical isolates of Staphylococcus aureus. J Med Microbiol 57:1018–1023

    Article  PubMed  Google Scholar 

  27. Archer NK, Mazaitis MJ, Costerton W, Leid JG, Powers ME, Shirtliff ME (2011) Staphylococcus aureus biofilms: properties, regulation and roles in human disease. Virulence 2:445–459

    PubMed Central  Article  PubMed  Google Scholar 

  28. Monecke S, Coombs G, Shore AC et al (2011) A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus. PLoS One 6:e17936

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  29. Vandenesch F, Naimi T, Enright MC et al (2003) Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence. Emerg Infect Dis 9:978–984

    PubMed Central  Article  PubMed  Google Scholar 

  30. Cirkovic I, Sørum M, Radenkovic D, Vlahovic MS, Larsen AR (2013) National surveillance reveals findings of Panton-Valentine leukocidin positive meticillin-resistant Staphylococcus aureus in Serbia. J Med Microbiol 62:342–344

    Article  PubMed  Google Scholar 

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Acknowledgments

Research reported in this publication was supported by the Ministry of Education, Science and Technological Development, Republic of Serbia (Project No. ON175039).

Conflict of interest

None declared.

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Affiliations

  1. Clinic for Otorhinolaryngology and Maxillofacial Surgery, Clinical Centre of Serbia, 11000, Belgrade, Serbia

    Ana Jotić, Jovica Milovanović, Bojan Pavlović & Snežana Ješić

  2. Faculty of Medicine, University of Belgrade, 11000, Belgrade, Serbia

    Ana Jotić, Jovica Milovanović, Bojan Pavlović, Snežana Ješić & Mijomir Pelemiš

  3. Department of Microbiology and Immunology, Faculty of Pharmacy, University of Belgrade, 11221, Belgrade, Serbia

    Dragana D. Božić

  4. Clinic for Infectious and Tropical Diseases, Clinical Centre of Serbia, 11000, Belgrade, Serbia

    Mijomir Pelemiš

  5. Institute of Microbiology and Immunology, Faculty of Medicine, University of Belgrade, Dr Subotića 1, 11000, Belgrade, Serbia

    Marko Novaković & Ivana Ćirković

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  1. Ana Jotić
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  2. Dragana D. Božić
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Correspondence to Ivana Ćirković.

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Jotić, A., Božić, D.D., Milovanović, J. et al. Biofilm formation on tympanostomy tubes depends on methicillin-resistant Staphylococcus aureus genetic lineage. Eur Arch Otorhinolaryngol 273, 615–620 (2016). https://doi.org/10.1007/s00405-015-3607-8

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  • DOI: https://doi.org/10.1007/s00405-015-3607-8

Keywords

  • MRSA
  • Biofilm formation
  • Tympanostomy tubes
  • Genetic lineages