Abstract
OBJECTIVE:
Subjective visual vertical (SVV) deviation can indicate impairments of motion perception and spatial orientation in individuals with vestibular disorders. This study investigated the influence of SVV on tandem gait ability by assessing differences between temporal, spatial, and kinematic characteristics in young adults.
METHODS:
We recruited sixteen young adults with increased SVV and 17 age-matched control subjects. All subjects recruited for this study were with no history of neurological or musculoskeletal diseases. Knee and hip-joint kinematic data, spatio-temporal parameters, and gait variability were measured during tandem gait.
RESULTS:
Stride time variability and stride velocity variability were significantly greater in the experimental group than the control group (p < 0.05). In addition, a significant correlation was observed between stride time variability and SVV results (r = 0.345, p < 0.05). However, hip and knee joint angles were non-significantly different in the experimental and control groups (p > 0.05) and spatio-temporal parameters were similar between the two groups (p > 0.05).
CONCLUSION:
Stride time variability and stride velocity variability during tandem gait were significantly different in the experimental and control groups. We presume that increased SVV deviation is related to greater gait variability during tandem gait.
Introduction
The human vestibular system is a sensory system that plays a key role in maintaining postural balance based on motion perception, spatial orientation, and optical input [1, 48]. This system provides the brain with sensory signals for three-dimensional head rotations and translations by semicircular canals and otoliths, respectively [31, 45]. These complex functions require integration of vestibular inputs and signals from other sensory systems such as the optical and somatosensory systems [31, 45]. Vestibulocochlear nerves send information to vestibular nuclei about changes in head orientation and vestibular nuclei transmit motor commands to maintain upright body and head postures and balance through the vestibulospinal tract [1, 48]. Therefore, the understanding vestibular functions in the context of balance strategy of human postural control is an important topic in neurologic rehabilitation research and practice.
Several authors have suggested the use of various neurophysiological assessment techniques, such as electrocochleography, vestibular evoked myogenic potential, posturography, and subjective visual vertical (SVV) to evaluate the functions of the central and peripheral vestibular systems [10–12, 46, 56]. Among these methods, SVV testing provides a simple, inexpensive and convenient means of evaluating vestibular dysfunctions [11, 56]. SVV testing can estimate actions of the vestibular system in the human brain based on an individual’s perception of verticality [11, 56], and several studies have reported patients with a unilateral vestibular lesion exhibit significant SVV deviation at lesion sites [7, 51]. In other words, SVV deviation might indicate impairments of motion perception and spatial orientation in individuals with a central or peripheral vestibular disorder [7, 51]. However, it has been reported that SVV results of experiments on peripheral or central vestibular disorders are no different.
Several balance tests, such as walking with head turns, Romberg’s test, tandem gait tests, and the Berg Balance Test, can be used to diagnose patients with balance impairment due to vestibular disorders or neurological lesions at an early stage [3, 57]. In 2003, Wikkelsö et al. [57] reported increased backward sway in patients with hydrocephalus and abnormal SVV results. Tandem gait evaluations have also been used in various forms for many years and are known to be clinically useful and highly reliable for assessing balance and coordination abilities in older adults or patients with a vestibular disorder [16, 54]. Some studies have also combined conventional balance testing with three-dimensional gait analysis to quantitatively and objectively examine balance ability [21, 50]. However, little is known about the relationship between characteristics of tandem gait and vertical deviation as determined by SVV testing. Thus, the objective of this study was to determine the influence of SVV deviation on tandem gait characteristics in young adults by assessing differences in temporal, spatial, and kinematic characteristics.
Methods
Subjects
Sixteen young adults with increased SVV and 17 age-matched control subjects with no history of neurological or musculoskeletal disease were recruited for this study (Table 1).
Demographic data of the experimental and control groups
Demographic data of the experimental and control groups
Results are presented as means±SDs; SVV: subjective visual vertical, DHI: dizziness handicap inventory. Independent t-test and Chi-square test were used to compare demographic data. *p < 0.05.
The study inclusion criteria were as follows: (1) no history of a musculoskeletal, neurologic, or cognitive problem, (2) the ability to independently perform activities of daily living (ADL) and to walk, (3) no direct vestibular system problem (nystagmus, vertigo, ataxia, or dysarthria), and (4) a significantly elevated SVV result, that is, more than two standard deviations (SD) greater than the age-matched value determined during a prior study that used a software-based test (mean 1.51; S.D. 0.69) [5]. Symptoms of musculoskeletal, neurological, and vestibular damage were confirmed by interview and direct assessment using the Dizziness Handicap Inventory (DHI), the saccade test, and the ocular tilt reaction test [9, 35].
All participants provided informed consent and the study was approved by the institutional review board of Dankook University (Republic of Korea).
Subjective visual vertical (SVV) testing
A plastic cylindrical bucket was used to measure the subjective visual vertical (SVV). The bucket was made of inexpensive, easily obtainable materials. A vertical straight line was drawn inner base and a protractor was attached to its outer and its zero line was aligned with the straight line on the inner base of the bucket [25, 60]. A plumb bob was then hung outside the bucket such that its line aligned with the protractor zero line [25, 60]. With the test subject looking into the bucket, it was randomly rotated and then the subject was asked to turn the bucket until the line was vertical. Angular deviation from the vertical was determined using the protractor and the plumb bob line. Deviations were recorded as positive values regardless of the natures of deviations (i.e., clockwise or counterclockwise). The SVV testing was performed in a dark place to avoid reflection from the protractor. SVV testing was performed in triplicate and values were averaged.
Tandem gait
The subjects were asked to perform tandem gait barefoot by placing the toes of the back foot in contact with the heel of the forward foot without looking at their feet. A straight line of red cellophane tape was attached to the floor to allow participants to walk straight. While performing tandem gait along this red line subjects were instructed to lift their knees by 6 cm [19]. Subjects were also instructed to perform tandem gait at a self-selected comfortable speed. Testing was also performed in triplicate.
Gait analysis
Kinematic and spatio-temporal parameters were collected using a LEGSys + wearable device (BioSensics, LLC, Cambridge, MA, USA). Five wearable sensors (5.0 cm×4.2 cm×1.2 cm), that is, tri-axial gyroscopes, accelerometers, and magnetometers were connected to a computer by Bluetooth [29, 59]. Sensors were attached by Velcro straps to the anterior surfaces of both shins 3 cm above ankles, the anterior surfaces of both thighs 3 cm above the knee, and to the one side of low rear center of the posterior superior iliac spine (PSIS). The sampling frequency of the sensors was 100 Hz. Subjects were instructed to walk a 7 m walkway [38], which required five or more strides. All stride characteristics were measured during tandem gait. The kinematic and spatio-temporal parameters were obtained from the middle three strides, that is, the first and last strides were excluded [53]. Range of motion (ROM) of knee and hip joints during tandem gait, stride length, stride velocity, step length, and cadence were measured, and coefficients of variation (CV% = 100*(Std/Mean)) of stride times, stride lengths, and stride velocities were calculated [58].
The dizziness handicap inventory (DHI)
The DHI is a 25 item questionnaire that evaluates how dizziness perceived by participants affects activities of daily living (ADL) [35]. The maximum DHI score is 100 points and the minimum 0 (yes 4 points, sometimes 2 points, no 0 points).
The experimental procedure
The subjects were asked to begin in a standing position at the starting line and then to walk when given the signal “start” and to stop after arriving at the 7 m finish line, and then to remain in a standing position. Participants performed tandem gait over the entire 7 m. The procedure was repeated three times with a break between repetitions.
Statistical analysis
The analysis was conducted using SPSS software (ver. 20.0; SPSS, Inc., Chicago, IL, USA) and tested for normality using the Kolmogorov-Smirnov test. Independent t-test and the Chi-Square Test were used to determine the significances of demographic differences between the experimental and control groups, and the independent t-test was to compare group kinematic parameters, spatio-temporal parameters, and gait variabilities. A Pearson correlation analysis was used to determine the association between SVV results and gait variability. Statistical significance was accepted for p values of <0.05.
Results
Demographic data
A summary of the demographic data is provided in Table 1. SVV results were significantly higher in the experimental group than in the control group (p < 0.05), but group DHI scores were not significantly different (p > 0.05).
Kinematic parameters
The results of kinematic analyses of knee and hip joints during tandem gait are summarized in Table 2. All kinematic parameters were slightly lower in the experimental group. However, hip and knee joint angles in the two groups were not significantly different (p > 0.05).
Kinematic parameters of the experimental and control groups
Kinematic parameters of the experimental and control groups
Results are presented as means±SDs. Independent t-test was used to compare kinematic group parameters. *p < 0.05.
Group spatio-temporal parameters and gait variability comparisons are displayed in Table 3. Stride time variability and stride velocity variability were significantly higher in the experimental group (p < 0.05). However, stride length variability and other spatio-temporal parameters during tandem gait were not significantly different (p > 0.05). The correlation between SVV and gait variability during tandem gait is shown in Fig. 1. A statistically significant association was observed between stride time variability and SVV results (r = 0.345, p < 0.05) (Fig. 1). In contrast, stride length variability and stride velocity variability during tandem gait were not significantly correlated with SVV results (p > 0.05).
Group spatio-temporal parameters and gait variabilities
Group spatio-temporal parameters and gait variabilities
Results are presented as means±SDs. Independent t-test was used to compare group kinematic parameters. *p < 0.05.
Correlation between subjective visual vertical (SVV) results and gait variabilities. A significant correlation was observed between stride time variability and SVV results.
The purpose of this study was to investigate relations between SVV test results and characteristics of gait as determined by the tandem gait test in young adults. The main findings of the study were as follows: 1) the stride time variability and stride velocity variability were significantly greater in the experimental group than in the control group; 2) stride length variabilities were similar in the two groups; 3) kinematic and spatio-temporal parameters as revealed by tandem gait testing were non-significantly different in the two groups.
Kinematic parameters are commonly used as indices to examine problems associated with lower extremity joint angles and rotational movement during gait [4], whereas spatio-temporal parameters have been used to identify gait deviations and degrees of recovery to optimize interventions [6]. Many authors have suggested patients with a vestibular dysfunction due to a central or peripheral vestibular system injury have higher step and stride times but lower gait velocities and cadence than healthy adults [40, 47]. In 2003, Allum and Adkin described a patient with an acute unilateral peripheral vestibular deficit that exhibited an exaggerated trunk sway pattern during simple gait during the acute stage but normal results at 3 months. On the other hand, complex gait tasks, including tandem gait, measured after 3 months show no improvement in amplitude of trunk sway [2].
In the present study, kinematic and spatio-temporal parameters during tandem gait did not differ in the experimental and control groups, which may have been due to the characteristics of subjects recruited in the experimental group. In particular, they had no direct impairment of central or peripheral vestibular systems and did not complain of dizziness in their daily lives. It has been previously reported that stable walking is possible due to visual and somatosensory system balance compensation during tandem gait [49].
Gait variability plays an important role in understanding abnormal movements and provides basic data about fall risk in older adults or brain injury patients [20, 58]. It is well known that increased gait variability correlates an elevated fall risk in individuals with balance problems [23, 55]. Schniepp et al. (2011) [55] reported that individuals with a high fall risk such as mature adults and patients with vestibular system injury exhibited increased stride time variability. Marchetti et al. (2008) [47] also reported that stride time variability was elevated in patients with a vestibular disorder, such as unilateral vestibular hypofunction, Ménière disease, or a central vestibular dysfunction. In addition, previous investigations on older people with high fall risks and those with a vestibular system problem have reported increased gait variability [42, 44]. These findings are consistent with the results of the current study, in which a significant positive correlation was observed between SVV results and stride time variability which was elevated in subjects with marked SVV deviation. However, subjects in the experimental group had normal results for all vestibular function tests except for SVV deviation, which might indicate slight dysfunction of the peripheral or central vestibular system. This suggests SVV deviation may be positively related to gait variability and fall risk during tandem gait. Furthermore, our results suggest individual with high SVV deviations may not experience difficulties performed ordinary balancing tasks, such as climbing stairs, walking on slopes, and running. In other words, abnormal SVV values in normal individuals do not indicate severe impairment of vestibular function, but might affect high-level balance tasks.
In conclusion, our results indicate stride time variability and stride velocity variability during tandem gait were significantly different in or experimental and control groups, but that kinematic and spatio-temporal parameters were not. Our findings regarding gait variability during tandem gait might aid the development of intervention strategies aimed at treating patients with a high fall risk due to injury of the vestibular system. However, this study also has its limitations. First, its subjects were young normal adults, and thus, caution should be exercised when applying our results to other age groups. Second, motor learning was not excluded because we assumed motor learning could be easily induced due to the fact that the study sample comprised of normal adults and repetition of tandem gait measurement. Third, we did not pre-calculate sample size and we suggest future studies be conducted in accordingly with G*Power sample size calculations. Forth, we did not use normative values of SVV deviation through software-based assessment [4]. Future research is needed to examine various age groups using methods that exclude motor learning during tandem gait.
Conflict of interest statement
The authors state that there are no conflicts of interest which might have influenced the preparation of this manuscript.
Footnotes
Acknowledgments
This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF), funded by the Ministry of Education, Science and Technology (NRF-2018R1D1A1B07049510).