Reduced vestibular function is associated with longer, slower steps in healthy adults during normal speed walking

Highlights

• Lower VOR gain was associated with longer, slower steps.

• Otolith function was not associated with any gait parameter.

• VOR gain decline may lead to a greater emphasis on balance during walking.

Abstract

Background

Vestibular signals contribute to balance and walking. With aging, vestibular function declines and gait speed decreases. Vestibular loss contributes to decreasing gait speed, but this influence could be linked to spatial and/or temporal aspects of gait. We investigated the relationship between vestibular function (semicircular canal and otolith function) and spatial and temporal gait parameters in a cohort of adults.

Methods

113 community-dwelling healthy adults (mean age 72.2 (14.6) years) participating in the Baltimore Longitudinal Study of Aging were tested.

Horizontal semicircular canal (SCC) function was evaluated using quantitative vestibulo-ocular reflex gain. Otolith function was measured with cervical and ocular vestibular evoked myogenic potentials. Gait kinematics were collected during normal speed walking. Multiple linear regressions examined the association between spatial and temporal gait parameters and SCC and otolith function separately, controlling for age, gender, height, and either cadence (for spatial gait outcomes) or stride length (for temporal gait outcomes) to account for gait speed effects.

Results

Vestibular SCC function was significantly associated with both spatial and temporal gait parameters. Every 0.1 decrease in SCC function resulted in longer stride length (β = -.04 m, p = 0.004), longer stance time (β = 15.8 ms, p < 0.003), and a slower cadence (β = -2.1 steps/minute, p < 0.001). Otolith function was not associated with any gait parameter.

Conclusions

Reduced horizontal SCC function was associated with longer, slower steps in a cohort of healthy adults. These results indicate that vestibular signals contribute to specific spatial and temporal aspects of gait thought to contribute to upright balance.

Introduction

The vestibular system plays a critical role in the modulation of gait [1]. Previous research indicates that the otolith organs -- the saccule and utricle -- contribute linear acceleration cues to control gait speed [2] and to maintain upright posture during gait [3]. Semicircular canal input from vertical head rotation also contributes to walking balance and horizontal head rotation contributes to navigation [4]. The semicircular canals further provide important angular velocity input during walking which is necessary for gaze stability [5]. When there is damage to these vestibular organs and subsequent loss of sensory input during motion, normal gait patterns are compromised [6]. Recent studies have shown a link between vestibular impairment and gait abnormalities in patients with vestibular disorders such as vestibular neuritis and vestibular schwannoma, including decreased gait speed and increased variability in stance and swing time [7,8].

There is conflicting evidence however regarding relationships between measures of vestibular function and gait. The gaze stabilization test (GST) evaluates how fast the head can rotate and still read a letter clearly [9]. Both horizontal and vertical GST scores have been associated with clinical measures of walking balance [10,11], suggesting that vestibulo-ocular reflex (VOR) function is related to walking balance ability. Recently, change in horizontal semicircular canal VOR gain was associated with change in walking balance measured using the Dynamic Gait Index [12]. In contrast, horizontal semicircular canal VOR gain measured with video head impulses and rotational chair tests was not significantly associated with measures of trunk sway during walking [13]. Taken together these studies suggest a role for horizontal semicircular canal function in mediating walking balance, possibly related to foot placement [14]. Otolith function was not reported in those studies; therefore, the contributions of the saccule and utricle to dynamic balance in those studies is unknown.

Numerous basic, clinical and epidemiologic studies have demonstrated a clear loss of vestibular function associated with normal aging [15,16]. Important changes in peripheral vestibular signaling occur with advancing age including: a decrease in number of sensory hair cells [17], degeneration of the vestibular ganglion and nerve [18], and degeneration and fragmentation of otoconia [19]. Age-related vestibular physiologic deficits have been shown to result from the degeneration of these anatomical structures including abnormal angular vestibulo-ocular reflex (VOR) function [20], and diminished otolith responses as measured by reduced amplitude and increased latency of vestibular-evoked myogenic potentials (VEMPs) [21,22]. Interestingly, the overall prevalence of semicircular canal dysfunction has been determined to be higher compared to otolith dysfunction in the older population [21].

With age, gait speed decreases and the gait pattern becomes more variable [23]. Although aging has been shown to have a profound impact on both vestibular function and gait over time, few studies have investigated the changes in spatial and temporal aspects of gait associated with age-related vestibular loss. Investigation into how vestibular loss influences components of gait, such as stride length and cadence, independent of age and gait speed could be utilized to inform clinical practice to improve gait function and perhaps reduce fall risk. The purpose of this study was to identify a vestibular specific impact on spatial and temporal aspects of the gait cycle independent of age in a cohort of healthy older adults. We quantify the relationships between semicircular canal, saccular, and utricular function on spatial (stride length, step width) and temporal (cadence, swing time, stance time) gait parameters in a cohort of healthy adults.