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Suppression head impulse test paradigm (SHIMP) characteristics in people with Parkinson’s disease compared to healthy controls

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Abstract

The suppression head impulse test paradigm (SHIMP) is a newly described indicator of vestibular function which yields two measures: vestibulo-ocular reflex (VOR) gain and a saccadic response. It is an alternative and complementary test to the head impulse test paradigm (HIMP). Parkinson’s disease (PD) has known saccadic and central vestibular pathway dysfunction. This paper is the first description of SHIMP VOR gain and saccade characteristic in this population. This prospective observational study measured the SHIMP VOR gain and saccade characteristics in 39 participants with idiopathic PD and compared this to 40 healthy controls (HC). The effect of group, demographic variables and SHIMP characteristics were evaluated. SHIMP VOR gains were not significantly different between groups (p = 0.10). Compared to HC, the PD group mean SHIMP peak saccade velocity was significantly reduced by an average of 77.07°/sec (p < 0.001), and SHIMP saccade response latency was longer, with an average delay of 23.5 ms (p = 0.003). SHIMP saccade peak velocity was also associated with both head impulse velocity (p = 0.002) and SHIMP VOR gain (p = 0.004) variables, but there was no significant influence of these variables when SHIMP saccade peak velocity was considered as a predictor of PD (p = 0.52–0.91). VOR gains were unaffected by PD. PD-specific saccadic dysfunction, namely reduced peak saccade velocities and prolonged response latencies, were observed in the SHIMP-induced saccade responses. VOR gain using slow phase eye velocity is preferred as the indicator of vestibular function in the SHIMPs paradigm as non-vestibular factors affected saccade peak velocity.

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adapted from Rey-Martinez J, Yanes J, Esteban J, Sanz R and Martin-Sanz E (2017) The Role of Predictability in Saccadic Eye Responses in the Suppression Head Impulse Test of Horizontal Semicircular Canal Function. Front. Neurol. 8:536. https://doi.org/10.3389/fneur.2017.00536 with authors' permission and also in accordance with copyright terms: "© 2017 Rey-Martinez, Yanes, Esteban, Sanz and Martin-Sanz. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms."

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Data availability

Raw data supplied in the supplementary material.

Abbreviations

GLMM:

Generalised linear mixed-effect statistical model

HIMP:

Head impulse test paradigm

HC:

Healthy controls

IND:

Indeterminate PD subtype

LEDD:

Levodopa daily equivalent dose

LME:

Linear mixed-effect statistical model

MMSE:

Mini-Mental State Examination

PD:

Parkinson’s disease

PIGD:

Postural instability/gait dysfunction PD subtype

SHIMP:

Suppression head impulse test paradigm

TD:

Tremor dominant PD subtype

VOR:

Vestibulo-ocular reflex

vHIT:

Video head impulse test

VGS:

Visually guided saccades

References

  • Aw ST, Chen L, Todd MJ, Barnett MH, Halmagyi GM (2017) Vestibulo-ocular reflex deficits with medial longitudinal fasciculus lesions. J Neurol 264:2119–2129

    Article  PubMed  Google Scholar 

  • Bassetto JM, Zeigelboim BS, Jurkiewicz AL, Klagenberg KF (2008) Neurotological findings in patients with Parkinson’s disease. Rev Bras Otorrinolaringol (Engl Ed) 74:350–355

    Article  Google Scholar 

  • Breiman L (2001) Random forests. Mach Learn 45:5–32

    Article  Google Scholar 

  • Chen L, Halmagyi GM (2018) Central lesions with selective semicircular canal involvement mimicking bilateral vestibulopathy. Front Neurol. https://doi.org/10.3389/fneur.2018.00264

    Article  PubMed  PubMed Central  Google Scholar 

  • Cipparrone L, Ginanneschi A, Degl’Innocenti F, Porzio P, Pagnini P, Marini P (1988) Electro-oculographic routine examination in Parkinson’s disease. Acta Neurol Scand 77:6–11

    Article  CAS  PubMed  Google Scholar 

  • Crane BT, Demer JL (1999) Latency of voluntary cancellation of the human vestibulo-ocular reflex during transient yaw rotation. Exp Brain Res 127:67–74

    Article  CAS  PubMed  Google Scholar 

  • de Natale E et al (2015a) Paired neurophysiological and clinical study of the brainstem at different stages of Parkinson’s disease. Clin Neurophysiol 126:1871–1878

    Article  PubMed  Google Scholar 

  • de Natale ER et al (2015b) Abnormalities of vestibular-evoked myogenic potentials in idiopathic Parkinson’s disease are associated with clinical evidence of brainstem involvement. Neurol Sci 36:995–1001

    Article  PubMed  Google Scholar 

  • de Waele C, Shen QW, Magnani C, Curthoys IS (2017) A novel saccadic strategy revealed by suppression head impulse testing of patients with bilateral vestibular loss. Front Neurol 8:10. https://doi.org/10.3389/fneur.2017.00419

    Article  Google Scholar 

  • Dewan N, MacDermid JC (2014) Fall Efficacy Scale-International (FES-I). J Physiother 60:60

    Article  PubMed  Google Scholar 

  • Dirnberger G, Jahanshahi M (2013) Executive dysfunction in Parkinson’s disease: a review. J Neuropsychol 7:193–224

    Article  PubMed  Google Scholar 

  • Dolowitz DA, Magid SL (1969) Comparison of electronystagmographic recordings in patients with vertigo and Parkinson’s disease. Trans Pac Coast Otoophthalmol Soc Annu Meet 50:303–314

    CAS  PubMed  Google Scholar 

  • Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198

    Article  CAS  PubMed  Google Scholar 

  • Galecki A, Burzykowski T (2013) Linear mixed-effects models using R. Springer, Berlin

    Book  Google Scholar 

  • Goetz CG et al (2008) Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord 23:2129–2170

    Article  PubMed  Google Scholar 

  • Halmagyi GM, Chen L, MacDougall HG, Weber KP, McGarvie LA, Curthoys IS (2017) The video head impulse test. Front Neurol 8:258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hawkins KE, Chiarovano E, Paul SS, Burgess AM, MacDougall HG, Curthoys IS (2021) Vestibular semicircular canal function as detected by video Head Impulse Test (vHIT) is essentially unchanged in people with Parkinson’s disease compared to healthy controls Under review

  • Leigh RJ, Zee DS (2015a) Chapter 14: disorders of ocular motility and disease affecting the basal ganglia cerebral cortex and in systemic conditions. The neurology of eye movements. Oxford University Press

    Chapter  Google Scholar 

  • Leigh RJ, Zee DS (2015b) The neurology of eye movements. Oxford University Press

    Book  Google Scholar 

  • Luke SG (2017) Evaluating significance in linear mixed-effects models in R. Behav Res Methods 49:1494–1502

    Article  PubMed  Google Scholar 

  • Lv W, Guan Q, Hu X, Chen J, Jiang H, Zhang L, Fan W (2017) Vestibulo-ocular reflex abnormality in Parkinson’s disease detected by video head impulse test. Neurosci Lett 657:211–214

    Article  CAS  PubMed  Google Scholar 

  • MacDougall HG, Weber KP, McGarvie LA, Halmagyi GM, Curthoys IS (2009) The video head impulse test: diagnostic accuracy in peripheral vestibulopathy. Neurology 73:1134–1141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • MacDougall HG et al (2016) A new saccadic indicator of peripheral vestibular function based on the video head impulse test. Neurology 87:410–418

    Article  PubMed  PubMed Central  Google Scholar 

  • Macdougall HG, McGarvie LA, Halmagyi GM, Curthoys IS, Weber KP (2013) The video Head Impulse Test (vHIT) detects vertical semicircular canal dysfunction. PLoS ONE 8:e61488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maheu M, Behtani L, Nooristani M, Delcenserie A, Champoux F (2019) Enhanced vestibulo-ocular reflex suppression in dancers during passive high-velocity head impulses. Exp Brain Res 237:411–416

    Article  PubMed  Google Scholar 

  • Manzari L, Tramontano M (2020) Suppression Head Impulse Paradigm (SHIMP) in evaluating the vestibulo-saccadic interaction in patients with vestibular neuritis. Eur Arch Otorhinolaryngol 29:29

    Google Scholar 

  • Nieuwboer A, Rochester L, Herman T, Vandenberghe W, Emil GE, Thomaes T, Giladi N (2009) Reliability of the new freezing of gait questionnaire: agreement between patients with Parkinson’s disease and their carers. Gait Posture 30:459–463

    Article  PubMed  Google Scholar 

  • Park JS, Lee JY, Nam W, Noh S, Chang SO, Kim MB (2020) Comparing the suppression head impulse paradigm and the head impulse paradigm in vestibular neuritis. Otol Neurotol 41:e76–e82

    Article  PubMed  Google Scholar 

  • Pötter-Nerger M, Reich MM, Colebatch JG, Deuschl G, Volkmann J (2012) Differential effect of dopa and subthalamic stimulation on vestibular activity in Parkinson’s disease. Mov Disord 27:1268–1275

    Article  PubMed  CAS  Google Scholar 

  • Reichert WH, Doolittle J, McDowell FH (1982) Vestibular dysfunction in Parkinson disease. Neurology 32:1133–1138

    Article  CAS  PubMed  Google Scholar 

  • Rey-Martinez J, Batuecas-Caletrio A, Matino E, Perez Fernandez N (2015) HITCal: a software tool for analysis of video head impulse test responses. Acta Otolaryngol (Stockh) 135:886–894

    Article  Google Scholar 

  • Rey-Martinez J, Yanes J, Esteban J, Sanz R, Martin-Sanz E (2017) The role of predictability in saccadic eye responses in the suppression head impulse test of horizontal semicircular canal function. Front Neurol 8:536

    Article  PubMed  PubMed Central  Google Scholar 

  • Rey-Martinez J, Thomas-Arrizabalaga I, Espinosa-Sanchez JM, Batuecas-Caletrio A, Trinidad-Ruiz G, Matino-Soler E, Perez-Fernandez N (2018) Vestibulo-ocular reflex gain values in the suppression head impulse test of healthy subjects. Laryngoscope 128:2383–2389

    Article  PubMed  Google Scholar 

  • Scarpa A et al (2020) A comparison of auditory and vestibular dysfunction in Parkinson’s disease and Multiple System Atrophy. Parkinsonism Relat Disord 71:51–57

    Article  PubMed  Google Scholar 

  • Seidel K et al (2015) The brainstem pathologies of Parkinson’s disease and dementia with lewy bodies. Brain Pathol 25:121–135

    Article  PubMed  Google Scholar 

  • Shen Q et al (2016) saccadic velocity in the new suppression head impulse test: a new indicator of horizontal vestibular canal paresis and of vestibular compensation. Front Neurol 7:160

    Article  PubMed  PubMed Central  Google Scholar 

  • Smith PF (2018) Vestibular functions and Parkinson’s disease. Front Neurol 9:1085

    Article  PubMed  PubMed Central  Google Scholar 

  • Srivastava A, Sharma R, Sood SK, Shukla G, Goyal V, Behari M (2014) Saccadic eye movements in Parkinson’s disease. Indian J Ophthalmol 62:538–544

    Article  PubMed  PubMed Central  Google Scholar 

  • Stebbins GT, Goetz CG, Burn DJ, Jankovic J, Khoo TK, Tilley BC (2013) How to identify tremor dominant and postural instability/gait difficulty groups with the movement disorder society unified Parkinson’s disease rating scale: comparison with the unified Parkinson’s disease rating scale. Mov Disord 28:668–670

    Article  PubMed  Google Scholar 

  • Terao Y, Fukuda H, Hikosaka O (2017) What do eye movements tell us about patients with neurological disorders?—An introduction to saccade recording in the clinical setting. Proc Jap Acad Ser B Phys Biol Sci Nippon Gakushiin 93:772–801

    Article  Google Scholar 

  • Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE (2010) Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord 25:2649–2653

    Article  PubMed  Google Scholar 

  • Venhovens J, Meulstee J, Bloem BR, Verhagen WIM (2016) Neurovestibular analysis and falls in Parkinson’s disease and atypical parkinsonism. Eur J Neurosci 43:1636–1646

    Article  CAS  PubMed  Google Scholar 

  • Vitale C et al (2011) Vestibular impairment and adaptive postural imbalance in parkinsonian patients with lateral trunk flexion. Mov Disord 26:1458–1463

    Article  PubMed  Google Scholar 

  • Weber KP, Aw ST, Todd MJ, McGarvie LA, Curthoys IS, Halmagyi GM (2008) Head impulse test in unilateral vestibular loss: vestibulo-ocular reflex and catch-up saccades. Neurology 70:454–463

    Article  CAS  PubMed  Google Scholar 

  • Weil RS, Schrag AE, Warren JD, Crutch SJ, Lees AJ, Morris HR (2016) Visual dysfunction in Parkinson’s disease. Brain 139:2827–2843

    Article  PubMed  PubMed Central  Google Scholar 

  • Wellings TP, Brichta AM, Lim R (2017) Altered neurofilament protein expression in the lateral vestibular nucleus in Parkinson’s disease. Exp BrainRes 235:3695–3708

    Article  CAS  Google Scholar 

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Funding

We gratefully acknowledge grant support for HGM from the Garnett Passe and Rodney Williams Memorial Foundation and the student research support for KH from the Faculty of Science, University of Sydney.

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Authors and Affiliations

Authors

Contributions

KH designed the study, performed the data collection, and wrote the manuscript. EC and SP designed the study, assisted with data collection and reviewed the manuscript. JRM designed and developed the HITCal analysis method, performed the statistical analysis and wrote part of the manuscript. AV analysed the SHIMP files using HITCal and performed the statistical analysis. HGM provided resources and revised the manuscript. IC supervised KH and revised the manuscript.

Corresponding author

Correspondence to Kim E. Hawkins.

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Conflict of interest

The authors declare they have no relevant financial or non-financial interests to disclose.

Ethics approval

The study was conducted in accordance with the ethical standards of the Helsinki Declaration of 1975, as revised in 1983. Ethical approval for this study was obtained through the University of Sydney Human Ethics review board (2017/925), and all participants gave written informed consent before enrolment in the study.

Additional information

Communicated by Francesco Lacquaniti.

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Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 Database containing all the data recorded in this study. (XLSX 48 KB)

Supplementary file2 PDF containing raw HITCal SHIMP traces for left and right impulses for both groups (PDF 3904 KB)

221_2021_6107_MOESM3_ESM.eps

Supplementary file3 ROC curve using RF model predictions to assess the developed AI model’s validity. A 0.8 area under (ROC) curve value was obtained for the developed RF model (EPS 243 KB)

Supplementary file4 (EPS 2558 KB)

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Hawkins, K.E., Rey-Martinez, J., Chiarovano, E. et al. Suppression head impulse test paradigm (SHIMP) characteristics in people with Parkinson’s disease compared to healthy controls. Exp Brain Res 239, 1853–1862 (2021). https://doi.org/10.1007/s00221-021-06107-7

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  • DOI: https://doi.org/10.1007/s00221-021-06107-7

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