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Vestibular-evoked myogenic potential abnormalities in Parkinson’s disease with freezing of gait

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Abstract

Background

Vestibular dysfunction is closely associated with the pathophysiology of Parkinson’s disease (PD) accompanied by freezing of gait (FOG); however, evidence supporting this clinical association is lacking. Vestibular-evoked myogenic potentials (VEMPs) have been widely acknowledged as a crucial electrophysiological parameter in the clinical evaluation of vestibular function.

Objective

The present study investigated the possible correlation of FOG occurrence with VEMP observations in patients diagnosed with PD.

Methods

Altogether, 95 idiopathic PD patients were recruited into the present cross-sectional study. All patients underwent motor and non-motor assessments using serial scales. In addition, the electrophysiological vestibular evaluation was conducted, which included cervical (cVEMP) and ocular VEMP (oVEMP) assessments. Furthermore, the correlations of bilateral c/oVEMP absence with clinical phenotypes, especially FOG, among the PD patients were analyzed.

Results

Among the 95 patients with PD, 44 (46.3%) had bilateral oVEMP absence and 23 (24.2%) had bilateral cVEMP absence, respectively. The proportions of patients with bilateral oVEMP absence (77.8% vs 30.9%, p = 0.004) and bilateral cVEMP absence (44.4% vs 19.5%, p = 0.035) were higher in the patient group exhibiting FOG than in the group without FOG. Following the adjustment of confounding variables, bilateral oVEMP absence (OR = 8.544, p = 0.007), rather than bilateral cVEMP absence, was shown to independently predict FOG occurrence in patients with PD.

Conclusion

The close correlation between bilateral oVEMP absence and FOG in PD patients sheds new light on the possible role of central vestibular/upper brainstem dysfunction in FOG development in patients with PD.

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Data availability

The datasets used and analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Bohnen NI, Roytman S, Griggs A et al (2022) Decreased vestibular efficacy contributes to abnormal balance in Parkinson’s disease. J Neurol Sci 440:120357. https://doi.org/10.1016/j.jns.2022.120357

    Article  PubMed  PubMed Central  Google Scholar 

  2. Huh YE, Hwang S, Kim K et al (2016) Postural sensory correlates of freezing of gait in Parkinson’s disease. Parkinsonism Relat Disord 25:72–77. https://doi.org/10.1016/j.parkreldis.2016.02.004

    Article  PubMed  Google Scholar 

  3. Bohnen NI, Kanel P, van Emde BM et al (2022) Vestibular sensory conflict during postural control, freezing of gait, and falls in Parkinson’s disease. Mov Disord 37:2257–2262. https://doi.org/10.1002/mds.29189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Park JH, Kim MS, Kang SY (2022) Initial vestibular function may be associated with future postural instability in Parkinson’s disease. J Clin Med 11:5608. https://doi.org/10.3390/jcm11195608

    Article  PubMed  PubMed Central  Google Scholar 

  5. Di Lazzaro G, Schirinzi T, Giambrone MP et al (2018) Pisa syndrome in Parkinson’s disease: evidence for bilateral vestibulospinal dysfunction. Parkinsons Dis 2018:8673486. https://doi.org/10.1155/2018/8673486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. de Natale ER, Ginatempo F, Paulus KS et al (2015) Abnormalities of vestibular-evoked myogenic potentials in idiopathic Parkinson’s disease are associated with clinical evidence of brainstem involvement. Neurol Sci 36:995–1001. https://doi.org/10.1007/s10072-014-2054-4

    Article  PubMed  Google Scholar 

  7. Cui W, Duan Z, Feng J (2022) Assessment of vestibular-evoked myogenic potentials in Parkinson’s disease: a systematic review and meta-analysis. Brain Sci 12:956. https://doi.org/10.3390/brainsci12070956

    Article  PubMed  PubMed Central  Google Scholar 

  8. Park J-H, Kang SY (2021) Dizziness in Parkinson’s disease patients is associated with vestibular function. Sci Rep 11:18976. https://doi.org/10.1038/s41598-021-98540-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Shalash AS, Hassan DM, Elrassas HH et al (2017) Auditory- and vestibular-evoked potentials correlate with motor and non-motor features of Parkinson’s disease. Front Neurol 8:55. https://doi.org/10.3389/fneur.2017.00055

    Article  PubMed  PubMed Central  Google Scholar 

  10. Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression and mortality. Neurology 17:427–442. https://doi.org/10.1212/wnl.17.5.427

    Article  CAS  PubMed  Google Scholar 

  11. Postuma RB, Berg D, Stern M et al (2015) MDS clinical diagnostic criteria for Parkinson’s disease. Mov Disord 30:1591–1601. https://doi.org/10.1002/mds.26424

    Article  PubMed  Google Scholar 

  12. Giladi N, Shabtai H, Simon ES et al (2000) Construction of freezing of gait questionnaire for patients with Parkinsonism. Parkinsonism Relat Disord 6:165–170. https://doi.org/10.1016/s1353-8020(99)00062-0

    Article  CAS  PubMed  Google Scholar 

  13. Wu L, Wang Q, Zhao L et al (2020) Clinical and oculomotor correlates with freezing of gait in a Chinese cohort of Parkinson’s disease patients. Front Aging Neurosci 12:237. https://doi.org/10.3389/fnagi.2020.00237

    Article  PubMed  PubMed Central  Google Scholar 

  14. Kang GA, Bronstein JM, Masterman DL et al (2005) Clinical characteristics in early Parkinson’s disease in a central California population-based study. Mov Disord 20:1133–1142. https://doi.org/10.1002/mds.20513

    Article  PubMed  PubMed Central  Google Scholar 

  15. Nomura T, Inoue Y, Kagimura T et al (2011) Utility of the REM sleep behavior disorder screening questionnaire (RBDSQ) in Parkinson’s disease patients. Sleep Med 12:711–713. https://doi.org/10.1016/j.sleep.2011.01.015

    Article  PubMed  Google Scholar 

  16. Richards M, Marder K, Cote L, Mayeux R (1994) Interrater reliability of the unified Parkinson’s disease rating scale motor examination. Mov Disord 9:89–91. https://doi.org/10.1002/mds.870090114

    Article  CAS  PubMed  Google Scholar 

  17. Chen W, Chen S, Kang W-Y et al (2012) Application of odor identification test in Parkinson’s disease in China: a matched case–control study. J Neurol Sci 316:47–50. https://doi.org/10.1016/j.jns.2012.01.033

    Article  PubMed  Google Scholar 

  18. Hamilton M (1960) A rating scale for depression. J Neurol Neurosurg Psychiatry 23:56–62. https://doi.org/10.1136/jnnp.23.1.56

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Katzman R, Zhang MY, Ouang-Ya-Qu et al (1988) A Chinese version of the mini-mental state examination; impact of illiteracy in a Shanghai dementia survey. J Clin Epidemiol 41:971–978. https://doi.org/10.1016/0895-4356(88)90034-0

    Article  CAS  PubMed  Google Scholar 

  20. Xu Q, Zhou M, Jiang C et al (2021) Application of the Chinese version of the Montreal cognitive assessment-basic for assessing mild cognitive impairment in Parkinson’s disease. Brain Sci 11:1575. https://doi.org/10.3390/brainsci11121575

    Article  PubMed  PubMed Central  Google Scholar 

  21. Visser M, Marinus J, Stiggelbout AM, Van Hilten JJ (2004) Assessment of autonomic dysfunction in Parkinson’s disease: the SCOPA-AUT. Mov Disord 19:1306–1312. https://doi.org/10.1002/mds.20153

    Article  PubMed  Google Scholar 

  22. Tomlinson CL, Stowe R, Patel S et al (2010) Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord 25:2649–2653. https://doi.org/10.1002/mds.23429

    Article  PubMed  Google Scholar 

  23. Berkiten G, Tutar B, Atar S et al (2023) Assessment of the clinical use of vestibular evoked myogenic potentials and the video head impulse test in the diagnosis of early-stage Parkinson’s disease. Ann Otol Rhinol Laryngol 132:41–49. https://doi.org/10.1177/00034894211067838

    Article  PubMed  Google Scholar 

  24. Braak H, Del Tredici K, Rüb U et al (2003) Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24:197–211. https://doi.org/10.1016/s0197-4580(02)00065-9

    Article  PubMed  Google Scholar 

  25. Seidel K, Mahlke J, Siswanto S et al (2015) The brainstem pathologies of Parkinson’s disease and dementia with Lewy bodies. Brain Pathol 25:121–135. https://doi.org/10.1111/bpa.12168

    Article  PubMed  Google Scholar 

  26. Aravamuthan BR, Angelaki DE (2012) Vestibular responses in the macaque pedunculopontine nucleus and central mesencephalic reticular formation. Neuroscience 223:183–199. https://doi.org/10.1016/j.neuroscience.2012.07.054

    Article  CAS  PubMed  Google Scholar 

  27. Gallea C, Wicki B, Ewenczyk C et al (2021) Antisaccade, a predictive marker for freezing of gait in Parkinson’s disease and gait/gaze network connectivity. Brain 144:504–514. https://doi.org/10.1093/brain/awaa407

    Article  PubMed  Google Scholar 

  28. Pötter-Nerger M, Govender S, Deuschl G et al (2015) Selective changes of ocular vestibular myogenic potentials in Parkinson’s disease. Mov Disord 30:584–589. https://doi.org/10.1002/mds.26114

    Article  PubMed  Google Scholar 

  29. Rosengren SM, Young AS, Taylor RL, Welgampola MS (2022) Vestibular function testing in the 21st century: video head impulse test, vestibular evoked myogenic potential, video nystagmography; which tests will provide answers? Curr Opin Neurol 35:64–74. https://doi.org/10.1097/WCO.0000000000001023

    Article  PubMed  Google Scholar 

  30. Hitier M, Besnard S, Smith PF (2014) Vestibular pathways involved in cognition. Front Integr Neurosci 8:59. https://doi.org/10.3389/fnint.2014.00059

    Article  PubMed  PubMed Central  Google Scholar 

  31. Harun A, Oh ES, Bigelow RT et al (2016) Vestibular impairment in dementia. Otol Neurotol 37:1137–1142. https://doi.org/10.1097/MAO.0000000000001157

    Article  PubMed  PubMed Central  Google Scholar 

  32. Wei EX, Oh ES, Harun A et al (2019) Increased prevalence of vestibular loss in mild cognitive impairment and Alzheimer’s disease. Curr Alzheimer Res 16:1143–1150. https://doi.org/10.2174/1567205016666190816114838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Brandt T, Schautzer F, Hamilton DA et al (2005) Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans. Brain 128:2732–2741. https://doi.org/10.1093/brain/awh617

    Article  PubMed  Google Scholar 

  34. Göttlich M, Jandl NM, Sprenger A et al (2016) Hippocampal gray matter volume in bilateral vestibular failure. Hum Brain Mapp 37:1998–2006. https://doi.org/10.1002/hbm.23152

    Article  PubMed  PubMed Central  Google Scholar 

  35. Mohammed Ali F, Westling M, Zhao LHL et al (2019) Splenius capitis: sensitive target for the cVEMP in older and neurodegenerative patients. Eur Arch Otorhinolaryngol 276:2991–3003. https://doi.org/10.1007/s00405-019-05582-7

    Article  PubMed  Google Scholar 

  36. Aitken P, Benoit A, Zheng Y et al (2016) Hippocampal and striatal M(1)-muscarinic acetylcholine receptors are down-regulated following bilateral vestibular loss in rats. Hippocampus 26:1509–1514. https://doi.org/10.1002/hipo.22651

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors would like to thank all the subjects who participated in the study.

Funding

This research was funded by Fundamental research program funding of Ninth People’s Hospital affiliated to Shanghai Jiao Tong university School of Medicine (JYZZ209), Project of Biobank from Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine (YBKB202120), Transverse Research Project of Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine (JYHX202117002), Health Management Project of Shanghai Rehabilitation Medical Association (2022KJCX008), 200 talent project from Shanghai Municipal Education Commission-Gaofeng Clinical Medicine Grant Support (20161422) and Natural Science Foundation Project from the Shanghai Municipal Science and Technology Commission (22ZR1436900).

Author information

Author notes

  1. Yuhan Jiang and Mengxi Zhou contributed equally to this work and shared the first authorship.

Authors and Affiliations

  1. Department of Neurology, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China

    Yuhan Jiang, Mengxi Zhou, Yajing Chen, Li Wu, Qing He, Lei Zhao, Jianren Liu & Wei Chen

  2. Department of Otolaryngology-Head and Neck Surgery, Shanghai Ninth People’s Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China

    Haibin Sheng & Shuai Xu

  3. Ear Institute, Shanghai Jiao Tong University School of Medicine, Shanghai, China

    Haibin Sheng & Shuai Xu

  4. Shanghai Key Laboratory of Translational Medicine on Ear and Nose Diseases, Shanghai, China

    Haibin Sheng & Shuai Xu

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  1. Yuhan Jiang
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Contributions

Wei Chen: research project—conception, organization; statistical analysis: design, review and critique; manuscript preparation—review and critique. Yuhan Jiang: research project—conception, execution; statistical analysis—design, execution, review and critique; manuscript preparation—writing of the first draft. Mengxi Zhou: research project—conception, organization; statistical analysis—design, execution, review and critique; manuscript preparation—writing of the first draft. Jianren Liu: research project—organization; statisticalanalysis—review and critique, manuscript preparation—review and critique. Yajing Chen: research project—execution; statistical analysis—review and critique. Li Wu: statistical analysis—execution, review and critique; manuscript preparation—review and critique. Qing He: statistical  analysis—design, review and critique; manuscript preparation—review and critique. Lei Zhao: statistical analysis—review and critique; manuscript preparationreview . Shuai Xu and Haibing Sheng: statistical analysis—execution.

Corresponding author

Correspondence to Wei Chen.

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Conflicts of interest

On behalf of all the authors, the corresponding author states that there is no conflict of interest.

Ethical approval

The study was conducted according to the guidelines of the Declaration of Helsinki and approved by the Medical Ethics Committee of Shanghai Ninth People’s Hospital (ethical approval number: SH9H-2021-T390-2).

Informed consent

Informed consent was obtained from all the subjects involved in the study.

Supplementary Information

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Supplementary file 1 (DOCX 17 KB)

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Jiang, Y., Zhou, M., Sheng, H. et al. Vestibular-evoked myogenic potential abnormalities in Parkinson’s disease with freezing of gait. J Neurol (2024). https://doi.org/10.1007/s00415-024-12311-6

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  • DOI: https://doi.org/10.1007/s00415-024-12311-6

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