Middle ear biofilm and sudden deafness - a light and transmission electron microscopy study

Hao Li; Karin Staxäng; Hanif M Ladak; Sumit Agrawal; Helge Rask-Andersen

doi:10.3389/fneur.2024.1495893

Middle ear biofilm and sudden deafness - a light and transmission electron microscopy study

Front Neurol. 2024 Dec 13:15:1495893. doi: 10.3389/fneur.2024.1495893. eCollection 2024.

Authors

Hao Li¹, Karin Staxäng², Hanif M Ladak^{3

4

5}, Sumit Agrawal^{3

4

5}, Helge Rask-Andersen¹

Affiliations

¹ Department of Surgical Sciences, Otorhinolaryngology and Head and Neck Surgery, Uppsala University, Uppsala, Sweden.
² The Rudbeck TEM Laboratory, BioVis Platform, Uppsala University, Uppsala, Sweden.
³ Department of Otolaryngology-Head and Neck Surgery, Western University, London, ON, Canada.
⁴ Department of Medical Biophysics, Western University, London, ON, Canada.
⁵ Department of Electrical and Computer Engineering, Western University, London, ON, Canada.

Abstract

Background: There still exists controversy about whether the healthy human middle ear mucosa is sterile or if it may harbor a diverse microbiome. Considering the delicacy of the human round window membrane (RWM), different mechanisms may exist for avoiding inner ear pathogen invasion causing sensorineural deafness. We re-analyzed archival human RWMs using light and transmission electron microscopy after decalcification to determine if bacteria are present in clinically normal human middle ears. We also searched for the presence of inborn immune defensive mechanisms within the round window niche (RWN), as previously reported in non-human primate ears.

Materials and methods: Five round window niches, removed and directly fixed at transcochlear petroclival meningioma surgery, were re-investigated after ethical permission using light and transmission electron microscopy. The morphology of the RWM, including its bony attachment and pseudomembrane outline, was analyzed. Moreover, 64 human temporal bones were investigated using synchrotron phase-contrast imaging (SR-PCI) aiming to identify potentially "hidden" spaces, including the RWN potentially harboring infectious material.

Results: Histologic evidence of free-living bacteria and biofilm was found in 40% of RWNs in seemingly "healthy" middle ears. The RWM in these ears was pathologically changed with repealed epithelial and intercellular junctional integrity. Putative membranous defense machinery consisted of a lymphatic drainage system together with free phagocytic cells seemingly serving to protect the inner ear from alleged pathogens. Synchrotron analyses showed that a pseudomembrane was present in the human round window niche (RWN) in 80% of the specimens, of which 20% were complete. In 3%, the RWN contained dense tissue or serous fluid plugs partly obstructing the RWN. Infralabyrinthic clefts and tympanomeningeal fissures (Hyrtl's fissure) were occasionally enclosed by delicate membranes near the round window. These may represent predilection sites for "hidden" infections potentially endangering inner ear function, particularly in connection with round window surgery.

Conclusion: Considering the fragility of the normal human RWM, we speculate that occult colonies of biofilm may be a factor in surgeries involving the RWM, sensorineural hearing loss, and hearing preservation/fibrosis following cochlear implantation, and more controversially in hidden perilymph leaks causing sudden deafness and labyrinthine pathology.

Keywords: biofilm; human; occult infection; round window; sudden deafness; synchrotron phase-contrast imaging.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This study was supported by the Swedish Research Council (2022-03339), the Tysta Skolan Foundation, and the Swedish Deafness Foundation (hrf). We also acknowledge the kind donations of private funds made by Arne Sundström, Sweden. The project was supported by MED-EL Elektromedizinische Geräte GmbH, Innsbruck, Austria under the agreement and contract with Uppsala University. Part of the research described in this paper was performed at the Canadian Light Source, a national research facility of the University of Saskatchewan, which is supported by the Canada Foundation for Innovation (CFI), the Natural Sciences and Engineering Research Council (NSERC), the National Research Council (NRC), the Canadian Institutes of Health Research (CIHR), the Government of Saskatchewan, and the University of Saskatchewan.