Skip to main content

Advertisement

Log in

Otitis media with effusion is not a sterile inflammatory process: scanning electron microscope evidence

  • Otology
  • Published:
European Archives of Oto-Rhino-Laryngology Aims and scope Submit manuscript

Abstract

Purpose

We aimed to demonstrate whether chronic otitis media with effusion (OME) is a sterile condition or biofilms-related disease through direct visualization of middle ear mucosa by Scanning electron microscopy (SEM) and culture of the effusion.

Methods

This case–control study included 60 children in two groups; the case group included 50 patients undergoing ventilation tube insertion (VTI) for Chronic OME (COME), and the control group included ten patients undergoing cochlear implantation (CI) surgery presenting normal middle ear mucosa. Biopsies from both groups' middle ear mucosa were evaluated for biofilm formation using scanning electron microscopy (SEM). Middle ear effusion (MEE) samples from COME patients were cultured on blood agar to detect and identify any bacterial growth. The adenoid size was evaluated and correlated to the biofilm formation in COME patients.

Results

There was a significant difference between case and control groups regarding biofilm formation (p-value < 0.001*). Biofilm was evident in 84% of the COME patients (cases group) and absent in the control group. Only 12 COME patients (24%) had positive MEE culture, however, 76.2% of patients with biofilm had a negative culture. Streptococcus pneumonia was the most common otopathogen found either alone or combined with other otopathogens. There was a significant negative correlation between adenoid size and biofilm grade among the studied patients.

Conclusion

The visual identification of middle ear biofilms indicated their role in chronic OME. Middle ear biofilms need to be expected in children with OME, especially those who do not need adenoid surgery.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Availability of data and materials

The data sets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Rosenfeld RM, Shin JJ, Schwartz SR, Coggins R, Gagnon L, Hackell JM, Hoelting D, Hunter LL, Kummer AW, Payne SC (2016) Clinical practice guideline: otitis media with effusion executive summary (update). Otolaryngol Neck Surg 154:201–214. https://doi.org/10.1177/0194599815623467

    Article  Google Scholar 

  2. Abdel Tawab HM, Tabook SMS (2019) Correlation between adenoid hypertrophy, tympanometry findings, and viscosity of middle ear fluid in chronic otitis media with effusion, Southern Oman. Ear Nose Throat J. https://doi.org/10.1177/0145561319875438

    Article  PubMed  Google Scholar 

  3. Park CW, Han JH, Jeong J-H, Cho SH, Kang MJ, Tae K, Lee SH (2004) Detection rates of bacteria in chronic otitis media with effusion in children. J Korean Med Sci 19:735–738. https://doi.org/10.3346/jkms.2004.19.5.735

    Article  PubMed  PubMed Central  Google Scholar 

  4. Schousboe LP, Ovesen T, Eckhardt L, Rasmussen LM, Pedersen CB (2001) How does endotoxin trigger inflammation in otitis media with effusion? Laryngoscope 111:297–300. https://doi.org/10.1097/00005537-200102000-00020

    Article  CAS  PubMed  Google Scholar 

  5. Post JC, Preston RA, Aul JJ, Larkins-Pettigrew M, Rydquist-White J, Anderson KW, Wadowsky RM, Reagan DR, Walker ES, Kingsley LA (1995) Molecular analysis of bacterial pathogens in otitis media with effusion. JAMA 273:1598–1604

    Article  CAS  Google Scholar 

  6. Fergie N, Bayston R, Pearson JP, Birchall JP (2004) Is otitis media with effusion a biofilm infection? Clin Otolaryngol Allied Sci 29:38–46. https://doi.org/10.1111/j.1365-2273.2004.00767.x

    Article  CAS  PubMed  Google Scholar 

  7. Bakaletz LO (2012) Bacterial biofilms in the upper airway-evidence for role in pathology and implications for treatment of otitis media. Paediatr Respir Rev 13:154–159. https://doi.org/10.1016/j.prrv.2012.03.001

    Article  PubMed  PubMed Central  Google Scholar 

  8. Slinger R, Chan F, Ferris W, Yeung SW, Denis MS, Gaboury I, Aaron SD (2006) Multiple combination antibiotic susceptibility testing of nontypeable Haemophilus influenzae biofilms. Diagn Microbiol Infect Dis 56:247–253. https://doi.org/10.1016/j.diagmicrobio.2006.04.012

    Article  CAS  PubMed  Google Scholar 

  9. Ehrlich GD, Veeh R, Wang X, Costerton JW, Hayes JD, Hu FZ, Daigle BJ, Ehrlich MD, Post JC (2002) Mucosal biofilm formation on middle-ear mucosa in the chinchilla model of otitis media. JAMA 287:1710–1715. https://doi.org/10.1001/jama.287.13.1710

    Article  PubMed  Google Scholar 

  10. Hoa M, Syamal M, Schaeffer MA, Sachdeva L, Berk R, Coticchia J (2010) Biofilms and chronic otitis media: an initial exploration into the role of biofilms in the pathogenesis of chronic otitis media. Am J Otolaryngol 31:241–245. https://doi.org/10.1016/j.amjoto.2009.02.015

    Article  PubMed  Google Scholar 

  11. Cassano P, Gelardi M, Cassano M, Fiorella ML, Fiorella R (2003) Adenoid tissue rhinopharyngeal obstruction grading based on fiberendoscopic findings: a novel approach to therapeutic management. Int J Pediatr Otorhinolaryngol 67:1303–1309. https://doi.org/10.1016/j.ijporl.2003.07.018

    Article  PubMed  Google Scholar 

  12. Van Hoecke H, De Paepe AS, Lambert E, Van Belleghem JD, Cools P, Van Simaey L, Deschaght P, Vaneechoutte M, Dhooge I (2016) Haemophilus influenzae biofilm formation in chronic otitis media with effusion. Eur Arch Oto-Rhino-Laryngol 273(11):3553–3560. https://doi.org/10.1007/s00405-016-3958-9

    Article  Google Scholar 

  13. Daniel M, Imtiaz-Umer S, Fergie N, Birchall JP, Bayston R (2012) Bacterial involvement in otitis media with effusion. Int J Pediatr Otorhinolaryngol 76(10):1416–1422. https://doi.org/10.1016/j.ijporl.2012.06.013

    Article  CAS  PubMed  Google Scholar 

  14. Tawfik SA, Ibrahim AA, Talaat IM, El-Alkamy SS, Youssef A (2016) Role of bacterial biofilm in development of middle ear effusion. Eur Arch Oto-Rhino-Laryngol 273:4003–4009. https://doi.org/10.1007/s00405-016-4094-2

    Article  Google Scholar 

  15. Gu X, Keyoumu Y, Long L, Zhang H (2014) Detection of bacterial biofilms in different types of chronic otitis media. Eur Arch Oto-Rhino-Laryngol 271:2877–2883. https://doi.org/10.1007/s00405-013-2766-8

    Article  Google Scholar 

  16. Saafan ME, Ibrahim WS, Tomoum MO (2013) Role of adenoid biofilm in chronic otitis media with effusion in children. Eur Arch Oto-Rhino-Laryngol 270:2417–2425. https://doi.org/10.1007/s00405-012-2259-1

    Article  Google Scholar 

  17. Szalmás A, Papp Z, Csomor P, Kónya J, Sziklai I, Szekanecz Z, Karosi T (2013) Microbiological profile of adenoid hypertrophy correlates to clinical diagnosis in children. Biomed Res Int 2013:629607. https://doi.org/10.1155/2013/629607

    Article  PubMed  PubMed Central  Google Scholar 

  18. Hall-Stoodley L, Hu FZ, Gieseke A, Nistico L, Nguyen D, Hayes J, Forbes M, Greenberg DP, Dice B, Burrows A (2006) Direct detection of bacterial biofilms on the middle-ear mucosa of children with chronic otitis media. JAMA 296:202–211. https://doi.org/10.1001/jama.296.2.202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Thornton RB, Rigby PJ, Wiertsema SP, Filion P, Langlands J, Coates HL, Vijayasekaran S, Keil AD, Richmond PC (2011) Multi-species bacterial biofilm and intracellular infection in otitis media. BMC Pediatr 11:94. https://doi.org/10.1186/1471-2431-11-94

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Homøe P, Bjarnsholt T, Wessman M, Sørensen HCF, Johansen HK (2009) Morphological evidence of biofilm formation in Greenlanders with chronic suppurative otitis media. Eur Arch Oto-Rhino-Laryngol 266:1533–1538. https://doi.org/10.1007/s00405-009-0940-9

    Article  Google Scholar 

  21. Tatar EC, Ünal FÖ, Tatar I, Celik HH, Gursel B (2006) Investigation of surface changes in different types of ventilation tubes using scanning electron microscopy and correlation of findings with clinical follow-up. Int J Pediatr Otorhinolaryngol 70:411–417. https://doi.org/10.1016/j.ijporl.2005.07.005

    Article  PubMed  Google Scholar 

  22. Zuliani G, Carron M, Gurrola J, Coleman C, Haupert M, Berk R, Coticchia J (2006) Identification of adenoid biofilms in chronic rhinosinusitis. Int J Pediatr Otorhinolaryngol 70:1613–1617. https://doi.org/10.1016/j.ijporl.2006.05.002

    Article  PubMed  Google Scholar 

  23. Psaltis AJ, Ha KR, Beule AG, Tan LW, Wormald P (2007) Confocal scanning laser microscopy evidence of biofilms in patients with chronic rhinosinusitis. Laryngoscope 117:1302–1306. https://doi.org/10.1097/MLG.0b013e31806009b0

    Article  PubMed  Google Scholar 

  24. Giebink GS (1989) The microbiology of otitis media. Pediatr Infect Dis J 8:S21

    Article  Google Scholar 

  25. Hall-Stoodley L, Stoodley P (2009) Evolving concepts in biofilm infections. Cell Microbiol 11:1034–1043. https://doi.org/10.1111/j.1462-5822.2009.01323.x

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

The authors have no funding or financial relationships to disclose.

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study conception and design. Idea formulation, Methodology, Data collection and Supervision were performed by SE. Material preparation, Writing review and editing were performed by NAEN. Data analysis, Statics and final revision were performed by AAG. The first draft of the manuscript and reference collection were performed by IAA. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Ibrahim A. Abdulghaffar.

Ethics declarations

Conflicts of interest

There is no conflict of interest.

Ethics approval

All procedures performed in this study involving human participants were in accordance with the ethical standards of the institutional research editorial boards and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Consent to participate

Formal consent was signed by the parents or guardians of the participants to share in this study.

Consent for publication

Additional informed consent was obtained from all participants' parents or guardians to share and publish their data in this article.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The work was done in Otolaryngology, Clinical pathology and Microbiology Departments, Faculty of Medicine and Nanotechnology department, faculty of science, Kafrelsheikh University, Egypt.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Elzayat, S., Nosair, N., Ghazy, A.A. et al. Otitis media with effusion is not a sterile inflammatory process: scanning electron microscope evidence. Eur Arch Otorhinolaryngol 278, 2713–2721 (2021). https://doi.org/10.1007/s00405-020-06338-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00405-020-06338-4

Keywords

Navigation