Multiple sclerosis affects the frequency content in the vertical ground reaction forces during walking

Abstract

Background

Multiple sclerosis is a progressive neurological disease that results in a high incident of gait disturbance. Exploring the frequency content of the ground reaction forces generated during walking may provide additional insights to gait in patients with multiple sclerosis that could lead to specific tools for differential diagnosis. The purpose of this study was to investigate differences in the frequency content of these forces in an effort to contribute to improved clinical management of this disease.

Methods

Eighteen patients and eighteen healthy controls walked across a 10 meter long walkway. The anterior–posterior and vertical ground reaction forces generated during the stance phase of gait were evaluated in the frequency domain using fast Fourier transformation. T-tests were utilized for comparison of median frequency, the 99.5% frequency, and the frequency bandwidth between patients and healthy controls and also for comparisons between patients with mild and moderate severity.

Findings

Patients with multiple sclerosis had significantly lower 99.5% frequency (P = 0.006) and median frequency (P < 0.001) in the vertical ground reaction force. No differences were found in the anterior–posterior reaction force frequency content. There were no differences between patients with mild and moderate severity.

Interpretation

The lower frequency content suggests lesser vertical oscillation of the center of gravity. Lack of differences between severities may suggest presence of differences prior to currently established diagnosis timelines. Analysis of the frequency content may potentially serve to provide earlier diagnostic assessment of this debilitating disease.

Introduction

Multiple Sclerosis (MS) is a progressive neurological disease that results in demyelination of the axons followed by the formation of dendritic scars which preclude the repair of the damaged axons (Noseworthy et al., 2000). The result of axon demyelination is slowed or blocked nerve conduction rates (Jones, 2008). MS is characterized by an array of possible symptoms such as optic neuritis, limb weakness, neurogenic bowel and bladder problems, depression, vertigo, spasticity, and other symptoms of central nervous system dysfunction (Noseworthy et al., 2000, Snook and Motl, 2009). Additionally, MS has a large impact on mobility as approximately 50% of those diagnosed with MS will advance to a stage that will require the use of a walking aid within 15 years of initial diagnosis (Confavreux and Vukusic, 2006, Tremlett et al., 2006).

Because of the strong presence of ambulatory deficits, mobility is used extensively to characterize disease severity and progression of MS (Kurtzke, 1983, Snook and Motl, 2009). Kurtzke's detailed expanded disability status scale (EDSS) is one of the most common classifications for MS (Kurtzke, 1983). The scale ranges from 0 to 10 with 0.5 point increments and is based on impairments of 8 different functional systems, but relies heavily on ambulatory ability. Scores of 6.5 and higher are marked by constant use of bilateral walking aids while scores of 6.0 and below are consistent with independent walking or intermittent use of walking aid to cover specified distances (Kurtzke, 1983). This scale is limited, however, in that it does not discriminate in the method by which the person is able to traverse the specified distance and therefore does not tell how the person moves. For example, an individual that is able to walk 100 m slowly and in an unsteady fashion with numerous gait compensations is classified the same as someone that is able to walk 100 m in a steady smooth manner but then must rest due to fatigue.

Gait analysis has also been used to classify mobility of patients with MS but has been largely limited to functional assessments and use of spatial and temporal measures. Slower walking speed, shorter stride length, and longer double stance times compared to healthy controls have been reported, while differences in joint motion at the ankle and muscle firing timing in the lower extremities have also been found (Benedetti et al., 1999, Martin et al., 2006). Gait analysis for patients with MS has not been performed to the extent that allows a comprehensive overview of the mechanical differences present. Evaluation of the mechanical differences may be able to provide a more detailed register of disease progression than temporal and spatial measures or the EDSS.

One tool to evaluate mechanical changes in walking is frequency domain analysis which provides the ability to examine the entire gait cycle and not just specific discrete points such as a maximum or a minimum value of a joint angle during the gait cycle. Frequency domain analysis provides details about the collection of frequencies that compose a particular signal (Giakas, 2004). In gait analysis, a resultant signal is the sum of multiple oscillations of movement that ultimately lead to the desired motion. Possible signals that could be analyzed from a walking pattern include the joint angular movement patterns of the ankle, knee, and hip or the ground reaction forces produced during the stance phase. Frequency domain analysis of the ground reaction forces (GRF) that are produced as forces applied against the ground during the stance phase of walking has previously been used to assess healthy and pathological gait and has been proven to be effective in outlining differences between such populations (Giakas et al., 1996, Stergiou et al., 2002, Tsepis et al., 2004). Stergiou et al. (2002) investigated the frequency domain in an elderly population and found significantly decreased frequency content in the anterior–posterior direction compared to the healthy young controls. This was attributed to decreased forward speed which is common among elderly ambulators. Giakas et al. (1996) examined the frequency domain of GRF in scoliosis patients. Their study was important as they also examined common time-dependent measures. They found significantly higher frequency domain content in all three planes with the largest effect in the medial–lateral direction. They found no significant differences in the time-dependent measures. This is valuable considering scoliosis is a tri-planar spinal deformity that seems to affect balance and walking in all three planes and yet common time-dependent measures could not detect any differences (Giakas et al., 1996).

Thus, it is possible that frequency analysis of GRF may be of benefit in patients with MS since it may detect important differences in gait mechanics of these patients that have not previously been discussed in the related literature. In order to assess the effect that MS has on gait, GRF frequency analysis can provide quantitative information about the resultant forces produced during walking. GRFs are the resultant reaction forces broken down into the three different planar components: vertical, anterior–posterior, and medial–lateral (Winter, 1991). Any differences in these specific resultant reaction force vectors may be considered differences in the forward motion (anterior–posterior component), stabilization of side-to-side motion (medial–lateral component), or the proper maintenance of an upright position (vertical component). All of these components are regulated by precise muscle activation patterns and any differences in the frequency content would point to an alteration in the underlying neuromuscular control when comparing patients with MS and healthy controls.

The aim of this study was to investigate the frequency content of the GRF of patients with MS during over-ground walking. We compared the frequency content of the GRF signals in patients with MS to healthy age-matched controls to determine if any differences in the frequency content were present. These differences in patients with MS that are otherwise healthy would likely be due to changes in the neurological system that results from the MS disease process. It was hypothesized that the frequency content of the GRF for patients with MS would be different from healthy controls. Furthermore, as MS is a progressive disease, we expected differences between patients with mild and moderate severity levels according to EDSS classification.