Quantitative assessment of cochlear and vestibular ganglion neurons in temporal bones with chronic otitis media

Abstract

Purpose

In this study, we aimed to determine whether or not COM leads to loss of spiral and Scarpa ganglion neurons.

Methods

From the human temporal bone (HTB) collection at the University of Minnesota we selected human temporal bones with COM, defined as the presence of clinically intractable tissue abnormalities in the middle ear (cholesteatoma, perforation of the eardrum, granulation tissue, fibrosis, tympanosclerosis, and cholesterol granuloma). We also selected HTBs from donors with no ear diseases as controls. We quantitatively analyzed the number of spiral and Scarpa ganglion cells and compared the results obtained in the control and study groups.

Results

In both COM and control groups we observed a significant negative correlation between age and number of both spiral (R = -0.632; P < 0.001; 95% CI − 0.766 to − 0.434) and Scarpa ganglion (R = − 0.404; P = 0.008; 95% CI − 0.636 to − 0.051) cells. We did not find any significant differences in the number of spiral ganglion cells (in total or per segment) or in the density of Scarpa ganglion cells (in each vestibular nerve or both) in the COM group as compared with controls (P > 0.05).

Conclusions and relevance

Our results did not demonstrate significant loss of cochlear or vestibular peripheral ganglion neuron loss in HTBs with COM as compared with controls.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. 1.

    Monasta L, Ronfani L, Marchetti F et al (2012) Burden of disease caused by otitis media: systematic review and global estimates. PLoS ONE 7:e36226. https://doi.org/10.1371/journal.pone.0036226

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  2. 2.

    de Penido NO, Chandrasekhar SS, Borin A et al (2016) Complications of otitis media: a potentially lethal problem still present. Braz J Otorhinolaryngol 82:253–262. https://doi.org/10.1016/j.bjorl.2015.04.007

    Article  Google Scholar 

  3. 3.

    Cordeiro FP, da Costa Monsanto R, Kasemodel ALP et al (2018) Extended high-frequency hearing loss following the first episode of otitis media. Laryngoscope 128:2879–2884. https://doi.org/10.1002/lary.27309

    Article  PubMed  Google Scholar 

  4. 4.

    Tucci DL, Wilson BS, O’Donoghue GM (2017) The growing—and now alarming—burden of hearing loss worldwide. Otol Neurotol 38:1387. https://doi.org/10.1097/MAO.0000000000001593

    Article  PubMed  Google Scholar 

  5. 5.

    Aarhus L, Tambs K, Hoffman HJ, Engdahl B (2016) Childhood otitis media is associated with dizziness in adulthood: the HUNT cohort study. Eur Arch Otorhinolaryngol 273:2047–2054. https://doi.org/10.1007/s00405-015-3764-9

    Article  PubMed  Google Scholar 

  6. 6.

    Aarhus L, Homøe P, Engdahl B (2020) Otitis media in childhood and disease in adulthood: a 40-year follow-up study. Ear Hear 41:67–71. https://doi.org/10.1097/AUD.0000000000000729

    Article  PubMed  Google Scholar 

  7. 7.

    Paparella MM, Oda M, Hiraide F, Brady D (1972) Pathology of sensorineural hearing loss in otitis media. Ann Otol Rhinol Laryngol 81:632–647. https://doi.org/10.1177/000348947208100503

    CAS  Article  PubMed  Google Scholar 

  8. 8.

    da Costa SS, Paparella MM, Cruz OLM, Rollin GAFS (1995) Chronic otitis media: a clinical-histopathological correlation. Otolaryngol Neck Surg 113:P110–P110. https://doi.org/10.1016/S0194-5998(05)80735-1

    Article  Google Scholar 

  9. 9.

    Livingston G, Sommerlad A, Orgeta V et al (2017) Dementia prevention, intervention, and care. Lancet 390:2673–2734. https://doi.org/10.1016/S0140-6736(17)31363-6

    Article  PubMed  Google Scholar 

  10. 10.

    Lin FR, Metter EJ, O’Brien RJ et al (2011) Hearing loss and incident dementia. Arch Neurol 68:214–220. https://doi.org/10.1001/archneurol.2010.362

    Article  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Paparella MM (1991) Interactive inner-ear/middle-ear disease, including perilymphatic fistula. Acta Otolaryngol Suppl 485:36–45

    CAS  Article  Google Scholar 

  12. 12.

    Cureoglu S, Schachern PA, Paparella MM, Lindgren BR (2004) Cochlear changes in chronic otitis media. Laryngoscope 114:622–626. https://doi.org/10.1097/00005537-200404000-00006

    Article  PubMed  Google Scholar 

  13. 13.

    Goycoolea MV (2001) Clinical aspects of round window membrane permeability under normal and pathological conditions. Acta Otolaryngol (Stockh) 121:437–447

    CAS  Article  Google Scholar 

  14. 14.

    Goycoolea MV, Paparella MM, Goldberg B et al (1980) Permeability of the middle ear to staphylococcal pyrogenic exotoxin in otitis media. Int J Pediatr Otorhinolaryngol 1:301–308

    CAS  Article  Google Scholar 

  15. 15.

    Goycoolea MV, Muchow D, Schachern P (1988) Experimental studies on round window structure: function and permeability. Laryngoscope 98:1–20. https://doi.org/10.1288/00005537-198806001-00002

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Monsanto RC, Schachern P, Paparella MM et al (2017) Progression of changes in the sensorial elements of the cochlear and peripheral vestibular systems: the otitis media continuum. Hear Res 351:2–10. https://doi.org/10.1016/j.heares.2017.05.003

    Article  PubMed  PubMed Central  Google Scholar 

  17. 17.

    da Costa Monsanto R, Erdil M, Pauna HF et al (2016) Pathologic changes of the peripheral vestibular system secondary to chronic otitis media. Otolaryngol Head Neck Surg 155:494–500. https://doi.org/10.1177/0194599816646359

    Article  Google Scholar 

  18. 18.

    Kodama A, Ishii T, Oka Y, Uebo K (1988) Histopathology of the inner ear in chronic otitis media. Equilibr Res 47:94–100

    Article  Google Scholar 

  19. 19.

    Kaya S, Tsuprun V, Hizli Ö et al (2016) Quantitative assessment of cochlear histopathologic findings in patients with suppurative labyrinthitis. JAMA Otolaryngol Head Neck Surg 142:364–369. https://doi.org/10.1001/jamaoto.2015.3803

    Article  PubMed  Google Scholar 

  20. 20.

    Schachern PA, Paparella MM, Hybertson R et al (1992) Bacterial tympanogenic labyrinthitis, meningitis, and sensorineural damage. Arch Otolaryngol Head Neck Surg 118:53–57

    CAS  Article  Google Scholar 

  21. 21.

    Paparella MM, Schachern PA, Yoon TH et al (1990) Otopathologic correlates of the continuum of otitis media. Ann Otol Rhinol Laryngol Suppl 148:17–22

    CAS  Article  Google Scholar 

  22. 22.

    Otte J, Schunknecht HF, Kerr AG (1978) Ganglion cell populations in normal and pathological human cochleae. Implications for cochlear implantation. Laryngoscope 88:1231–1246. https://doi.org/10.1288/00005537-197808000-00004

    CAS  Article  PubMed  Google Scholar 

  23. 23.

    Richter E (1980) Quantitative study of human Scarpa’s ganglion and vestibular sensory epithelia. Acta Otolaryngol (Stockh) 90:199–208

    CAS  Article  Google Scholar 

  24. 24.

    Abercrombie M (1946) Estimation of nuclear population from microtome sections. Anat Rec 94:239–247

    CAS  Article  Google Scholar 

  25. 25.

    Casselbrant ML, Furman JM, Rubenstein E, Mandel EM (1995) Effect of otitis media on the vestibular system in children. Ann Otol Rhinol Laryngol 104:620–624. https://doi.org/10.1177/000348949510400806

    CAS  Article  PubMed  Google Scholar 

  26. 26.

    Cureoglu S, Schachern PA, Rinaldo A et al (2005) Round window membrane and labyrinthine pathological changes: an overview. Acta Otolaryngol (Stockh) 125:9–15. https://doi.org/10.1080/00016480410022534

    Article  Google Scholar 

  27. 27.

    Goycoolea MV, Lundman L (1997) Round window membrane. Structure function and permeability: a review. Microsc Res Tech 36:201–211. https://doi.org/10.1002/(SICI)1097-0029(19970201)36:3%3c201:AID-JEMT8%3e3.0.CO;2-R

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  28. 28.

    MacArthur CJ, Pillers D-AM, Pang J et al (2011) Altered expression of middle and inner ear cytokines in mouse otitis media. Laryngoscope 121:365–371. https://doi.org/10.1002/lary.21349

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. 29.

    MacArthur CJ, Hausman F, Kempton JB et al (2013) Otitis Media Impacts Hundreds of Mouse Middle and Inner Ear Genes. PLoS ONE 8:e75213. https://doi.org/10.1371/journal.pone.0075213

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. 30.

    Paparella MM, Goycoolea MV, Meyerhoff WL, Shea D (1979) Endolymphatic hydrops and otitis media. Laryngoscope 89:43–58

    CAS  PubMed  Google Scholar 

  31. 31.

    Makary CA, Shin J, Kujawa SG et al (2011) Age-related primary cochlear neuronal degeneration in human temporal bones. J Assoc Res Otolaryngol 12:711–717. https://doi.org/10.1007/s10162-011-0283-2

    Article  PubMed  PubMed Central  Google Scholar 

  32. 32.

    Linthicum FH, Fayad J (2009) Spiral ganglion cell loss is unrelated to segmental cochlear sensory system degeneration in humans. Otol Neurotol 30:418–422

    Article  Google Scholar 

  33. 33.

    Kaya S, Tsuprun V, Hızlı Ö et al (2016) Cochlear changes in serous labyrinthitis associated with silent otitis media: a human temporal bone study. Am J Otolaryngol 37:83–88. https://doi.org/10.1016/j.amjoto.2015.10.002

    Article  PubMed  Google Scholar 

  34. 34.

    Suzuka Y, Schuknecht HF (1988) Retrograde cochlear neuronal degeneration in human subjects. Acta Otolaryngol Suppl 450:1–20

    CAS  Article  Google Scholar 

  35. 35.

    Zilberstein Y, Liberman MC, Corfas G (2012) Inner hair cells are not required for survival of spiral ganglion neurons in the adult cochlea. J Neurosci 32:405–410. https://doi.org/10.1523/JNEUROSCI.4678-11.2012

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Liberman MC, Liberman LD, Maison SF (2015) Chronic conductive hearing loss leads to cochlear degeneration. PLoS ONE 10:e0142341. https://doi.org/10.1371/journal.pone.0142341

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  37. 37.

    Okada M, Welling DB, Liberman MC, Maison SF (2019) Chronic conductive hearing loss is associated with speech intelligibility deficits in patients with normal bone conduction thresholds. Ear Hear. https://doi.org/10.1097/AUD.0000000000000787

    Article  Google Scholar 

  38. 38.

    Paparella MM, Shea D, Meyerhoff WL, Goycoolea MV (1980) Silent otitis media. Laryngoscope 90:1089–1098. https://doi.org/10.1288/00005537-198007000-00003

    CAS  Article  PubMed  Google Scholar 

  39. 39.

    da Monsanto RC, Kasemodel ALP, Tomaz A et al (2018) Current evidence of peripheral vestibular symptoms secondary to otitis media. Ann Med 50:391–401. https://doi.org/10.1080/07853890.2018.1470665

    Article  PubMed  Google Scholar 

  40. 40.

    Haapala S, Niemitalo-Haapola E, Raappana A et al (2014) Effects of recurrent acute otitis media on cortical speech-sound processing in 2-year old children. Ear Hear 35:e75–e83. https://doi.org/10.1097/AUD.0000000000000002

    Article  PubMed  Google Scholar 

  41. 41.

    Macandie C, O’Reilly BF (1999) Sensorineural hearing loss in chronic otitis media. Clin Otolaryngol 24:220–222. https://doi.org/10.1046/j.1365-2273.1999.00237.x

    CAS  Article  PubMed  Google Scholar 

  42. 42.

    Liberman MC, Kujawa SG (2017) Cochlear synaptopathy in acquired sensorineural hearing loss: manifestations and mechanisms. Hear Res 349:138–147. https://doi.org/10.1016/j.heares.2017.01.003

    Article  PubMed  PubMed Central  Google Scholar 

  43. 43.

    Kujawa SG, Liberman MC (2015) Synaptopathy in the noise-exposed and aging cochlea: primary neural degeneration in acquired sensorineural hearing loss. Hear Res 330:191–199. https://doi.org/10.1016/j.heares.2015.02.009

    Article  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Guitton MJ (2012) Tinnitus: pathology of synaptic plasticity at the cellular and system levels. Front Syst Neurosci. https://doi.org/10.3389/fnsys.2012.00012

    Article  PubMed  PubMed Central  Google Scholar 

  45. 45.

    Durán Alonso MB, Feijoo-Redondo A, Conde de Felipe M et al (2012) Generation of inner ear sensory cells from bone marrow-derived human mesenchymal stem cells. Regen Med 7:769–783. https://doi.org/10.2217/rme.12.65

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank our supporters: the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES—Brazil) (Finance code: 001), the National Institute of Neurological Disorders and Stroke of the NIH (Grant No. UG3NS107688), the International Hearing Foundation, the 5 M Lions International, and the Starkey Foundation.

Funding

RCM received a scholarship from the “Coordenação de aperfeiçoamento pessoal de nível superior” (CAPES) (Finance code: 001). The research reported in this manuscript was supported by the National Institute of Neurological Disorders and Stroke of the NIH (UG3NS107688), the International Hearing Foundation, the 5 M Lions International, and the Starkey Foundation.

Author information

Affiliations

Authors

Contributions

All authors performed similar contributions and were involved in all steps of the manuscript production. RCM, NOP and MU performed the literature review, analyzed the human temporal bones and wrote the final version of the manuscript. PS, MMP, and SC were the intellectual authors of the work, supervised the collection of data, analyzed the results and critically reviewed the final version of the manuscript.

Corresponding author

Correspondence to Rafael da Costa Monsanto.

Ethics declarations

Conflicts of interest

All authors declare that they have no conflict of interest.

Ethical approval

The Institutional Review Board of the University of Minnesota (0206M26181) and Universidade Federal de São Paulo/Escola Paulista de Medicina (UNIFESP/EPM) (1.751.916) approved this study.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Monsanto, R.C., Penido, N.O., Uchiyama, M. et al. Quantitative assessment of cochlear and vestibular ganglion neurons in temporal bones with chronic otitis media. Eur Arch Otorhinolaryngol 278, 331–338 (2021). https://doi.org/10.1007/s00405-020-06094-5

Download citation

Keywords

  • Otitis media
  • Chronic otitis media
  • Spiral ganglion cells
  • Scarpa ganglion cells
  • Hearing loss
  • Tinnitus
  • Vestibular diseases