Skip to main content

Auditory and vestibular dysfunction in patients with Parkinson’s disease

Abstract

Background

Motor dysfunction in patients with Parkinson disease (PD) is just the tip of the iceberg. Auditory and vestibular dysfunction in patients with PD gained much attention owing to them being one of the nonmotor symptoms.

Aim

To explore abnormalities of pure tone audiometry (PTA), brainstem auditory evoked potentials (BAEPs), vestibular evoked myogenic potential (VEMP), and videonystagmography (VNG) in patients with PD and their correlation with motor and cognitive dysfunction.

Patients and methods

The study was conducted on 20 patients with PD and 15 controls. Selected patients were subjected to evaluation of motor symptoms using Unified Parkinson’s Disease Rating Scale (UPDRS) and cognitive function using Parkinson disease-Cognitive Rating Scale (PD-CRS). PTA, BAEPs, cervical VEMPs, and VNG were carried out for all patients and controls.

Results

Patients with PD show higher mean hearing thresholds at all PTA frequencies in both ears than controls. Analysis of BAEP demonstrated that patients with PD have significantly prolonged absolute latencies of wave III and wave V and interpeak latencies of I–III and I–V in both ears than controls. VEMP findings revealed that patients have significantly delayed P13 and N23 latencies and smaller P13–N23 amplitude in both ears than controls. VNG findings showed canal paresis in 60% of patients with PD and nystagmus in 60% of patients with PD. Correlative results revealed statistically significant correlations between VEMP parameters and UPDRS as well as PD-CRS, but there were no statistically significant correlations between PTA frequencies or BAEP latencies and UPDRS or PD-CRS.

Conclusion

Auditory and vestibular dysfunction is common in PD but cannot be totally correlated with the motor and cognitive symptoms.

References

  1. 1

    Hirsch E, Jenner P, Przedborski S. Pathogenesis of Parkinson’s disease. Mov Disord 2013; 28:24–30.

    PubMed  CAS  Google Scholar 

  2. 2

    Pringsheim T, Jette N, Frolkis A, Steeves TD. The prevalence of Parkinson’s disease: a systematic review and meta-analysis. Mov Disord 2014; 29:1583–1590.

    PubMed  Google Scholar 

  3. 3

    Tolosa E, Gaig C, Santamaría J, Compta Y. Diagnosis and the premotor phase of Parkinson disease. Neurology 2009; 72 (Suppl):S12–S20.

    PubMed  Google Scholar 

  4. 4

    Hughes A, Daniel S, Kilford L, Lees A. Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 1992; 55:181–184.

    PubMed  PubMed Central  CAS  Google Scholar 

  5. 5

    Chaudhuri K, Odin P, Antonini A, Martinez-Martin P. Parkinson’s disease: the non-motor issues. Parkinsonism Relat Disord 2011; 17:717–723.

    PubMed  Google Scholar 

  6. 6

    Grinberg L, Rueb U, Alho A, Heinsen H. Brainstem pathology and nonmotor symptoms in PD. J Neurol Sci 2010; 289:81–88.

    PubMed  Google Scholar 

  7. 7

    Seidel K, Mahlke J, Siswanto S, Kruger R, Heinsen H, Auburger G, et al. The brainstem pathologies of Parkinson’s disease and dementia with Lewy bodies. Brain Pathol 2015; 25:121–135.

    PubMed  Google Scholar 

  8. 8

    Dickson D, Braak H, Duda J, Duyckaerts C, Gasser T, Halliday G, et al. Neuropathological assessment of Parkinson’s disease: refining the diagnostic criteria. Lancet Neurol 2009; 8:1150–1157.

    PubMed  CAS  Google Scholar 

  9. 9

    Jellinger K. A critical evaluation of current staging of alpha-synuclein pathology in Lewy body disorders. Biochim Biophys Acta 2009; 1792:730–740.

    PubMed  CAS  Google Scholar 

  10. 10

    Jellinger KA. Neuropathobiology of non-motor symptoms in Parkinson disease. J Neural Transm 2015; 122:1429–1440.

    PubMed  CAS  Google Scholar 

  11. 11

    Del Tredici K, Rub U, De Vos R, Bohl J, Braak H. Where does Parkinson disease pathology begin in the brain? J Neuropathol Exp Neurol 2002; 61:413–426.

    PubMed  Google Scholar 

  12. 12

    Pollak L, Kushnir M, Stryjer R. Diagnostic value of vestibular evoked myogenic potentials in cerebellar and lower-brainstem strokes. Neurophysiol Clin 2006; 36:227–233.

    PubMed  CAS  Google Scholar 

  13. 13

    Pötter-Nerger M, Govender S, Deuschl G, Volkmann J, Colebatch J. Selective changes of ocular vestibular myogenic potentials in Parkinson’s disease. Mov Disord 2015; 30:584–589.

    PubMed  Google Scholar 

  14. 14

    Vitale C, Marcelli V, Allocca R, Santangelo G, Riccardi P, Erro R, et al. Hearing impairment in Parkinson’s disease: expanding the nonmotor phenotype. Mov Disord 2012; 27:1530–1535.

    PubMed  Google Scholar 

  15. 15

    Lai S, Liao K, Lin C, Lin C, Sung F. Hearing loss may be a nonmotor feature of Parkinson’s disease in older people in Taiwan. Eur J Neurol 2014; 21:752–757.

    PubMed  Google Scholar 

  16. 16

    Carpenter M. Core text of neuroanatomy. Baltimore, MD: Williams & Wilkins 1985. pp. 137–149.

    Google Scholar 

  17. 17

    Shammah-Lagnado S, Alheid F, Heimer L. Efferent connections of the caudal part of the globus pallidus in the rat. J Comp Neurol 1996; 376:489–507.

    PubMed  CAS  Google Scholar 

  18. 18

    Chan F, Armstrong I, Pari G, Riopelle R, Munoz D. Deficits in saccadic eye-movement control in Parkinson’s disease. Neuropsychologia 2005; 43:784–796.

    PubMed  Google Scholar 

  19. 19

    Vidailhet M, Rivaud S, Gouider-Khouja N, Pillon B, Gaymard B, Agid Y, et al. Saccades and antisaccades in parkinsonian syndromes. Adv Neurol 1999; 80:377–382.

    PubMed  CAS  Google Scholar 

  20. 20

    Nakamura T, Kanayama R, Sano R, Ohki M, Kimura Y, Aoyagi M, et al. Quantitative analysis of ocular movements in Parkinson’s disease. Acta Otolaryngol Suppl 1991; 481:559–562.

    PubMed  CAS  Google Scholar 

  21. 21

    Lekwuwa G, Barnes G, Collins C, Limousin P. Progressive bradykinesia and hypokinesia of ocular pursuit in Parkinson’s disease. J Neurol Neurosurg Psychiatry 1999; 66:746–753.

    PubMed  PubMed Central  CAS  Google Scholar 

  22. 22

    Garbutt S, Riley D, Kumar A, Han Y, Harwood M, Leigh R. Abnormalities of optokinetic nystagmus in progressive supranuclear palsy. J Neurol Neurosurg Psychiatry 2004; 75:1386–1394.

    PubMed  PubMed Central  CAS  Google Scholar 

  23. 23

    Hughes A, Ben-Shlomo Y, Daniel S, Lees A. What features improve the accuracy of clinical diagnosis in Parkinson’s disease: a clinicopathologic study. Neurology 1992; 42:1142–1146.

    PubMed  CAS  Google Scholar 

  24. 24

    Fahn S, Elton R, and Members of The UPDRS Development Committee. Unified Parkinson’s Disease Rating Scale. In: Fahn S, Marsden C, Calne D, Goldstein M, editors. Recent developments in Parkinson’s disease (153–63). Florham Park, NJ: Macmillan Health Care Information; 1987.

    Google Scholar 

  25. 25

    Pagonabarraga J, Kulisevsky J, Llebaria G, García-Sánchez C, Pascual-Sedano B, Gironell A. Parkinson’s disease-cognitive rating scale: a new cognitive scale specific for Parkinson’s disease. MovDisord 2008; 23:998–1005.

    Google Scholar 

  26. 26

    Soliman S, Fathalla A, Shehat M. Development of Arabic staggered spondee words. XXXX 1985; 2:1220–1246.

    Google Scholar 

  27. 27

    Soliman S. Speech discrimination audiometry using Arabic phonetically-balanced words. Ain Shams Med J 1976; 27:27–30.

    Google Scholar 

  28. 28

    Murofushi T, Shimizu K, Takegoshi H, Cheng P. Diagnostic value of prolonged latencies in the vestibular evoked myogenic potential. Arch Otolorngol Head Neck Surg 2001; 127:1069–1072.

    CAS  Google Scholar 

  29. 29

    Rigual N. Otolaryngologic manifestations of rheumatoid arthritis. Ear Nose Throat J 1987; 6:18–22.

    Google Scholar 

  30. 30

    Yýlmaz S, Karalý E, Tokmak A, Güçlü E, Koçer A, Oztürk O. Auditory evaluation in Parkinsonian patients. Eur Arch Otorhinolaryngol 2009; 266:669–671.

    PubMed  Google Scholar 

  31. 31

    Fradis M, Samet A, Ben-David J, Podoshin L, Sharf B, Wajsbort J, et al. Brainstem auditory evoked potentials to different stimulus rates in parkinsonian patients. Eur Neurol 1988; 28:181–186.

    PubMed  CAS  Google Scholar 

  32. 32

    Tachibana H, Takeda M, Sugita M. Short-latency somatosensory and brainstem auditory evoked potentials in patients with Parkinson’s disease. Int J Neurosci 1989; 44:321–326.

    PubMed  CAS  Google Scholar 

  33. 33

    Gawel M, Das P, Vincent S, Rose F. Visual and auditory evoked responses in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 1981; 44:227–232.

    PubMed  PubMed Central  CAS  Google Scholar 

  34. 34

    Tsuji S, Muraoka S, Kuroiwa Y, Chen K, Gadusek C. Auditory brainstem evoked response (ABSR) of Parkinson dementia complex and amyotrophic lateral sclerosis in Guam and Japan. Rinsho Shinkeigaku 1981; 21:37–41.

    PubMed  CAS  Google Scholar 

  35. 35

    Chiappa K. Short-latency somatosensory evoked patentials: methodology. In: Chiappa KII, editor. Evoked potential in clinical medicine. New York, NY: Raven Press 1983. pp. 204–313.

    Google Scholar 

  36. 36

    Prasher D, Bannister R. Brainstem auditory evoked potentials in patients with multiple system atrophy with progressive autonomic failure (Shy Drager syndrome). J Neurol Neurosurg Psychiatry 1986; 49:278–289.

    PubMed  PubMed Central  CAS  Google Scholar 

  37. 37

    Alexa D, Alexa L, Popa L, Paduraru D, Ignat B, Constantinescu A, et al. Brainstem auditory evoked potentials in Parkinson’s disease. Rom J Neurol Psychiatry 2013; XII4:XX.

  38. 38

    Pollak L, Prohorov T, Kushnir M, Rabey M. Vestibulocervical reflexes in idiopathic Parkinson disease. Neurophysiol Clin 2009; 39:235–240.

    PubMed  CAS  Google Scholar 

  39. 39

    Halberstadt A, Balaban C. Selective anterograde tracing of the individual serotonergic and nonserotonergic components of the dorsal raphe nucleus projection to the vestibular nuclei. Neuroscience 2007; 147:207–223.

    PubMed  PubMed Central  CAS  Google Scholar 

  40. 40

    De Natale E, Ginatempo F, Paulus K, Manca A, Mercante B, Pes G, et al. Paired neurophysiological and clinical study of the brainstem at different stages of Parkinson’s disease. Clin Neurophysiol 2015a;126:1871–1878.

    Google Scholar 

  41. 41

    De Natale E, Ginatempo F, Paulus K, Pes G, Manca A, Tolu E, et al. Abnormalities of vestibularevoked myogenic potentials in idiopathic Parkinson’s disease are associated with clinical evidence of brainstem involvement. Neurol Sci 2015b;36:995–1001.

    Google Scholar 

  42. 42

    Venhovens J, Meulstee J, Bloem B, Verhagen W. Neurovestibular analysis and falls in Parkinson’s disease and atypical parkinsonism. Eur J Neurosci 2016; 43:1636–1646.

    PubMed  CAS  Google Scholar 

  43. 43

    Van der Marck M, Klok M, Okun M, Giladi N, Munneke M, Bloem B, et al. Consensus-based clinical practice recommendations for the examination and management of falls in patients with Parkinson’s disease. Parkinsonism Relat Disord 2014; 20:360–369.

    PubMed  Google Scholar 

  44. 44

    Hassan D, Shalash A. Auditory brainstem evoked responses and vestibular evoked myogenic potentials: potential biomarkers in Parkinson’s disease. Egypt J Otolaryngol 2017; 33:508–517.

    Google Scholar 

  45. 45

    Braak H, Ghebremedhin E, Rub U, Bratzke H, Del Tredici K. Stages in the development of Parkinson’s disease-related pathology. Cell Tissue Res 2004; 318:121–134.

    PubMed  Google Scholar 

  46. 46

    Braak H, Del Tredici K, Rüb U, de vos R, Jansen Steur E, Braak E. Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 2003; 24:197–211.

    PubMed  Google Scholar 

  47. 47

    Grant M, Leigh R, Seidman S, Riley D, Hanna J. Comparison of predictable smooth ocular and combined eye-head tracking behaviour in patients with lesions affecting the brainstem and cerebellum. Brain 1992; 115:1323–1342.

    PubMed  Google Scholar 

  48. 48

    Vidailhet M, Rivaud S, Gouider-Khouja N, Pillon B, Bonnet A, Gaymard B. Eye movements in parkinsonian syndromes. Ann Neurol 1994; 35:420–426.

    PubMed  CAS  Google Scholar 

  49. 49

    Bassetto J, Zeigelboim B, Jurkiewicz A, Klagenberg K. Neurotological findings in patients with Parkinson’s disease. Braz J Otorhinolaryngol 2008; 74:350–355.

    PubMed  Google Scholar 

  50. 50

    Reichert W, Doolittle J, Mcdowell F. Vestibular dysfunction in Parkinson disease. Neurology 1982; 32:1133–1138.

    PubMed  CAS  Google Scholar 

  51. 51

    Gushikem P. Avaliação otoneurológica em idosos com tontura. 2001.84f. Tese. (Mestrado em Distúrbios da Comunicação Humana) –Universidade Federal de São Paulo- Escola Paulista de Medicina, São Paulo.

  52. 52

    Dolowitz D. Diagnosis of early Parkinson’s disease. Laryngoscope 1969; 79:1275–1280.

    PubMed  Google Scholar 

  53. 53

    Silveira S, Taguchi C, Ganança F. Comparative analysis of two lines treatment for patients with vestibular syndromes peripheral groups over the age of sixty. Acta Awho 2002; 21:14–31.

    Google Scholar 

  54. 54

    Whitney S. Treatment of the elderly with vestibular dysfunction. In: Herdman SJ, editor. Vestibular rehabilitation. 2nd ed. São Paulo: Manole; 2002. pp. 505–528.

    Google Scholar 

  55. 55

    Hain T, Ramaswamy T, Hillman M. Anatomy and Physiology of the System normal vestibular. In: Herdman SJ, editor. Vestibular rehabilitation. 2nd ed. São Paulo: Manole; 2002. pp. 3–24.

    Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Rabab Koura MD.

Additional information

This is an open access journal, and articles are distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 4.0 License, which allows others to remix, tweak, and build upon the work non-commercially, as long as appropriate credit is given and the new creations are licensed under the identical terms.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

Rights and permissions

This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Hussein, M., Koura, R. Auditory and vestibular dysfunction in patients with Parkinson’s disease. Egypt J Otolaryngol 35, 313–321 (2019). https://doi.org/10.4103/ejo.ejo_18_18

Download citation

Keywords

  • brainstem auditory evoked potentials
  • Parkinson
  • Parkinson disease-Cognitive Rating Scale
  • pure tone audiometry
  • Unified Parkinson’s Disease Rating Scale
  • vestibular evoked myogenic potentials
  • videonystagmography