Gait initiation in Parkinson&apos;s disease: comparison of timing and displacement during anticipatory postural adjustments as a function of motor severity and apathy in a large cohort

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Abstract

Introduction

Gait initiation is preceded by three anticipatory postural adjustment (APA) phases. In Parkinson's disease (PD) generated force, displacement and timing during APA differ from healthy controls. APA might be influenced by disease status, weight or emotion. It is unknown how motor severity, disease duration or presence of apathy influences APA timing and displacement.

Methods

We included 99 people with PD and 50 healthy controls (HC) to perform five gait initiation trials following an auditory cue. Force plates measured timing and center of pressure (CoP) displacement during APA phases.

Results

Time to gait initiation (tGI) was higher in the PD group (p < 0.001, t = 2.74, 95%CI (0.008, 0.066)). The first two APA phases (APA1 and APA2a) lasted longer in PD (respectively p < 0.001, t = 3.87, 95%CI (0.091, 0.28) and p < 0.001, t = 4.1, 95%CI (0.031, 0.091)). Mean CoP displacement, variability in timing and displacement did not differ. A multiple regression model was used to determine if clinical variables were related to gait initiation parameters. tGI was predicted by age (p < 0.001) and weight (p = 0.005). The duration of APA1 was predicted by weight (p = 0.006) and APA2a by age (p < 0.001). Variability in duration of the locomotor phase (LOC) was predicted by age (p < 0.001).

Conclusion

tGI and initial APA phases are longer in PD than in HC. There are no significant differences in variability of timing or displacement between the two groups. Gait initiation parameters are independent of disease duration, motor severity, medication usage or apathy in PD. Our findings suggest that cueing does not speed up gait initiation but reduces variability.

Highlights

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Gait initiation requires shifting of weight during different anticipatory postural adjustment (APA) phases.
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It's unclear what impacts APA phases' duration and displacement in Parkinson's disease.
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Age and weight determine timing and displacement of certain APA phases in Parkinson's disease.
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Medication use, disease duration and motor severity have no impact on APA phases in Parkinson's disease.
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Cueing in gait initiation reduces variability in APA phases in Parkinson's disease.

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Most cited references 36

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MDS clinical diagnostic criteria for Parkinson's disease.

Ronald Postuma, Daniela Berg, Matthew Stern … (2015)

This document presents the Movement Disorder Society Clinical Diagnostic Criteria for Parkinson's disease (PD). The Movement Disorder Society PD Criteria are intended for use in clinical research but also may be used to guide clinical diagnosis. The benchmark for these criteria is expert clinical diagnosis; the criteria aim to systematize the diagnostic process, to make it reproducible across centers and applicable by clinicians with less expertise in PD diagnosis. Although motor abnormalities remain central, increasing recognition has been given to nonmotor manifestations; these are incorporated into both the current criteria and particularly into separate criteria for prodromal PD. Similar to previous criteria, the Movement Disorder Society PD Criteria retain motor parkinsonism as the core feature of the disease, defined as bradykinesia plus rest tremor or rigidity. Explicit instructions for defining these cardinal features are included. After documentation of parkinsonism, determination of PD as the cause of parkinsonism relies on three categories of diagnostic features: absolute exclusion criteria (which rule out PD), red flags (which must be counterbalanced by additional supportive criteria to allow diagnosis of PD), and supportive criteria (positive features that increase confidence of the PD diagnosis). Two levels of certainty are delineated: clinically established PD (maximizing specificity at the expense of reduced sensitivity) and probable PD (which balances sensitivity and specificity). The Movement Disorder Society criteria retain elements proven valuable in previous criteria and omit aspects that are no longer justified, thereby encapsulating diagnosis according to current knowledge. As understanding of PD expands, the Movement Disorder Society criteria will need continuous revision to accommodate these advances.

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The Lille apathy rating scale (LARS), a new instrument for detecting and quantifying apathy: validation in Parkinson's disease.

P Sockeel, K Dujardin, D Devos … (2006)

Apathy is usually defined as reduced interest and participation in various activities. It is a frequent consequence of neurological and psychiatric disorders. Although various scoring methods have been proposed, there is a lack of validated, standardised instruments for detecting apathy and assessing its severity. To develop an apathy rating scale using a structured standardised interview capable of distinguishing between the condition's various features. The Lille Apathy Rating Scale (LARS) is based on a structured interview. It includes 33 items, divided into nine domains. Responses are scored on a dichotomous scale. The participants used to validate the scale consisted of 159 patients with probable Parkinson's disease and 58 healthy control subjects. The Marin Apathy Scale, the Montgomery and Asberg Depression Rating Scale, and the Mattis Dementia Rating Scale were also administered. Principal component analysis showed that the LARS probed a single construct which forms the root of an oblique factor structure reflecting four dimensions: intellectual curiosity, self awareness, emotion, and action initiation. The main psychometric properties of the LARS (internal consistency, inter-rater and test-retest reliability) were satisfactory. Concurrent validity was evaluated by reference to the Marin scale and to judgements provided by expert clinicians. Standard validity indices showed that the LARS is sensitive and capable of distinguishing between apathy and depression. As a screening tool, the scale is able to support dichotomous judgements accurately and, when greater measurement sensitivity is required, also determine the severity of apathy within a four category classification.

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Knee trembling during freezing of gait represents multiple anticipatory postural adjustments.

Jesse Jacobs, John G. Nutt, Patricia Carlson-Kuhta … (2009)

Freezing of gait (FoG) is an episodic, brief inability to step that delays gait initiation or interrupts ongoing gait. FoG is often associated with an alternating shaking of the knees, clinically referred to as knee trembling or trembling in place. The pathophysiology of FoG and of the concomitant trembling knees is unknown; impaired postural adjustment in preparation for stepping is one hypothesis. We examined anticipatory postural adjustments (APAs) prior to protective steps induced by a forward loss of balance in 10 Parkinson's disease (PD) subjects with marked FoG and in 10 control subjects. The amplitude and timing of the APAs were determined from changes in the vertical ground-reaction forces recorded by a force plate under each foot and were confirmed by electromyographic recordings of bilateral medial gastrocnemius, tibialis anterior and tensor fascia latae muscles. Protective steps were accomplished with a single APA followed by a step for control subjects, whereas PD subjects frequently exhibited multiple, alternating APAs coexistent with the knee trembling commonly observed during FoG as well as delayed, inadequate or no stepping. These multiple APAs were not delayed in onset and were of similar or larger amplitude than the single APAs exhibited by the control subjects. These observations suggest that multiple APAs produce the knee trembling commonly associated with FoG and that FoG associated with a forward loss of balance is caused by an inability to couple a normal APA to the stepping motor pattern.

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Author and article information

Contributors

Ségolène De Waele

David Crosiers

Journal

Journal ID (nlm-ta): Heliyon

Journal ID (iso-abbrev): Heliyon

Title: Heliyon

Publisher: Elsevier

ISSN (Electronic): 2405-8440

Publication date PMC-release: 20 December 2023

Publication date Collection: 15 January 2024

Publication date (Electronic): 20 December 2023

Volume: 10

Issue: 1

Electronic Location Identifier: e23740

Affiliations

[a ]Translational Neurosciences, Born-Bunge Institute, Faculty of Medicine and Health Sciences, University of Antwerp, Antwerp, Belgium

[b ]Antwerp University Hospital, Department of Neurology, Antwerp, Belgium

[c ]Research group MOVANT (Movement Antwerp), Department of Rehabilitation Sciences and Physiotherapy, Faculty of Medicine and Health Sciences, University of Antwerp, Antwerp, Belgium

[d ]ZNA Middelheim Hospital, Department of Neurology, Antwerp, Belgium

Author notes

[∗ ]Corresponding author. Drie Eikenstraat 655, 2650 Edegem, Belgium. segolene.dewaele@ 123456uantwerpen.be

[∗∗ ]Corresponding author. Drie Eikenstraat 655, 2650 Edegem, Belgium. david.crosiers@ 123456uantwerpen.be

Article

Publisher Item ID: S2405-8440(23)10948-0 Publisher ID: e23740

DOI: 10.1016/j.heliyon.2023.e23740

PMC ID: 10789592

PubMed ID: 38230232

SO-VID: b75bb824-14cd-46d9-81bb-a89df07acbe0

License:

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

History

Date received : 26 June 2023

Date revision received : 14 October 2023

Date accepted : 12 December 2023

Gait initiation in Parkinson's disease: comparison of timing and displacement during anticipatory postural adjustments as a function of motor severity and apathy in a large cohort

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Introduction

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Results

Conclusion

Highlights

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Karger: Neurology and Neuroscience

Most cited references 36

MDS clinical diagnostic criteria for Parkinson's disease.

The Lille apathy rating scale (LARS), a new instrument for detecting and quantifying apathy: validation in Parkinson's disease.

Knee trembling during freezing of gait represents multiple anticipatory postural adjustments.

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