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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

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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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