Comprehensive assessment of walking function after human spinal cord injury

Lea Awai1; Armin Curt    Spinal Cord Injury Center, Balgrist University Hospital, Zürich, Switzerland
1 Corresponding author: Tel.:+41-44-386-37-34; Fax: +41-44-386-37-31 email address: lawai@paralab.balgrist.ch

Abstract

Regaining any locomotor function after spinal cord injury is not only of immediate importance for affected patients but also for clinical research as it allows to investigate mechanisms underlying motor impairment and locomotor recovery. Clinical scores inform on functional outcomes that are clinically meaningful to value effects of therapy while they all lack the ability to explain underlying mechanisms of recovery. For this purpose, more elaborate recordings of walking kinematics combined with assessments of spinal cord conductivity and muscle activation patterns are required. A comprehensive assessment framework comprising of multiple complementary modalities is necessary. This will not only allow for capturing even subtle changes induced by interventions that are likely missed by standard clinical outcome measures. It will be fundamental to attribute observed changes to naturally occurring spontaneous recovery in contrast to specific changes induced by novel therapeutic interventions beyond the improvements achieved by conventional therapy.

Keywords

spinal cord injury

motor

walking

function

recovery

outcome measures

human

1 Introduction

In incomplete spinal cord injury (iSCI), walking is characterized by manifold complex alterations like a slower than normal speed (Awai and Curt, 2014; Pepin et al., 2003), limited hip and knee flexion during swing (Perry and Burnfield, 2010), insufficient hip extension during stance, and excessive plantar flexion during swing (van der Salm et al., 2005). These observed impairments of joint and limb movements could be based on different underlying mechanisms such as limitations in hip flexion during swing phase that were attributed to muscle weakness, while the reduced knee flexion during swing was related to aberrant coactivation of antagonistic extensor muscles (Ditunno and Scivoletto, 2009). Thus, a multimodal and comprehensive approach to study normal and altered gait and its recovery is required for elucidating underlying mechanisms of gait control.

The majority of clinical studies that monitor recovery processes or training effects during different interventions after spinal cord injury (SCI) chose measures of walking performance (i.e., walking speed/distance) and functional independence (e.g., type of required assistive device, performance during activities of daily living) to reflect motor function (Fig. 1). However, "motor function" and "walking function" are ill-defined terms as they rather nonspecifically refer to different aspects of gait (i.e., speed and time-distance parameters, type of walking assistance), while such outcomes may not be well compared across studies and remain nonconclusive at explaining mechanisms of recovery. Even the examination of highly selected measures (e.g., changes in single joint angles), although presenting very concise information, is likely limited at elucidating underlying complex interactions. In order to acquire more comprehensive evaluations to address questions of physiological gait control as well as observed alterations and recovery profiles in iSCI, combined multimodal assessments are required. Especially in high risk and potentially high-return clinical trials (phase I/II studies), investigators should consider any possible efforts to search for complementary information (including surrogate markers) beyond standard clinical outcome measures. These readouts may reveal more detailed insights into different mechanisms of action that eventually may be important to identify effects evoked by specific interventions (i.e., obvious as well as clinically masked changes).

2 Clinical Assessments of Recovery

2.1 Neurological Assessments

The completeness of lesion (i.e., the preservation of sensory function below the level of lesion) is crucial for the clinical description and prediction of ambulatory outcome (Maynard et al., 1979; Waters et al., 1994). Patients who are ASIA A early after injury have little chance of regaining functional ambulation, while ASIA B patients may reach a functional level (Crozier et al., 1992; Maynard et al., 1979; Waters et al., 1994). However, it is commonly accepted that the ASIA classification is too crude to reveal functional changes (i.e., improved walking ability) that may occur within one ASIA grade (i.e., ASIA D patients may increase walking speed and muscle strength without a conversion in ASIA grade).

For a general evaluation of motor function, the assessment of ASIA motor scores as well as the spinal cord independence measure III (SCIM III) was strongly recommended (Labruyere et al., 2010). Even though the lower extremity motor scores (LEMS) are assessed in a lying position while the respective muscles are activated in a nontask specific manner (i.e., not during locomotion), LEMS were shown to be a good predictor for ambulatory outcome after rehabilitation (van Middendorp et al., 2011; Zorner et al., 2010). Furthermore, the LEMS of both legs were found to correlate best with walking speed, distance, and ambulatory capacity in chronic iSCI subjects compared to unilateral LEMS of the individual lower limb muscles (Kim et al., 2004). Thus, muscle strength seems to be an important determinant for walking performance (speed and distance) but may not have an influence on movement quality. It was shown that iSCI patients have preserved movement accuracy in the lower limbs despite diminished muscle strength, which distinguished them from stroke patients. The latter showed both diminished muscle strength in the affected leg as well as bilaterally impaired movement accuracy (van Hedel et al., 2010), suggesting that movement accuracy may not be corrupted by muscle weakness in iSCI.

2.2 Functional Assessments

The SCIM was developed as a scale to score disability in patients with SCI (Catz et al., 1997). In acute patients, the SCIM III was evaluated to have the most appropriate performance with respect to specific psychometric properties (i.e., reliability, validity, reproducibility, responsiveness) when compared to other measures such as Functional Independence Measure, Walking Index for Spinal Cord Injury (WISCI), Modified Barthel Index, Timed Up & Go, 6-minute walk test (6MinWT), or 10-meter walk test (10MWT) (Furlan et al., 2011). Compared to measures of walking capacity (i.e., speed, WISCI), the SCIM also assesses improvements in ASIA A and B patients who are wheelchair bound (van Hedel and Dietz, 2009). Depending on the aim of a study, the appropriate outcome measures should be chosen. If walking function and its recovery are to be investigated and the question of whether or not patients improve locomotor function and by what means they might improve their walking capacity, the SCIM score might not be a sensitive tool while it does inform on to what extent a patient can perform activities of daily living independent of aids or support from third parties.

Recovery of walking function is routinely assessed by functional outcome measures such as the widely used 10MWT and 6MinWT (Alcobendas-Maestro et al., 2012; Buehner et al., 2012; Hayes et al., 2014; Jayaraman et al., 2013; Kim et al., 2004; Kumru et al., 2013; Petersen et al., 2012a; van Hedel et al., 2006), where walking speed and distance (endurance) are evaluated (Fig. 1). Walking capacity (speed and distance) are important prerequisites for successful community ambulation (Lapointe et al., 2001).

Despite improvements in walking speed during rehabilitation, iSCI patients typically show a reduced velocity compared to a healthy control cohort, especially when asked to walk at their maximally possible walking speed (Awai and Curt, 2014; Lapointe et al., 2001; Pepin et al., 2003; van Hedel et al., 2007). Several studies discussed the question as to whether the 10MWT and 6MinWT actually bear complementary information (Forrest et al., 2014; van Hedel et al., 2007). van Hedel et al. (2007) found a certain redundancy in walking speed assessed by these two measures when performed at a comfortable walking speed, while the results at maximal speed revealed additional...