Evidence for bilaterally delayed and decreased obstacle avoidance responses while walking with a lower limb prosthesis

doi:10.1016/j.clinph.2009.03.003

Clinical Neurophysiology

Volume 120, Issue 5, May 2009, Pages 1009-1015

https://doi.org/10.1016/j.clinph.2009.03.003 Get rights and content

Abstract

Objective

To examine whether the increased failure rates in obstacle avoidance of patients with lower limb amputation can be understood on the basis of increased delay and/or decreased amplitudes of obstacle avoidance responses.

Methods

Subjects performed obstacle avoidance on a treadmill while EMG recordings were made of several major muscles of the leg.

Results

It was found that subjects with a lower limb amputation have delayed responses (e.g. delays of 20 ms for the Biceps Femoris) and have decreased response amplitudes (36–41% smaller). Furthermore, such changes were observed not only on the prosthetic side, but also on the sound side. The decreased amplitudes were associated with increased failure rates in the obstacle avoidance task.

Conclusions

It is concluded that the bilaterally delayed and reduced responses in persons with a lower limb prosthesis reflect a basic reorganization within the central nervous system aimed at providing synchronized activity in both lower limbs, even though the peripheral deficit involves only one limb.

Significance

The present results on obstacle avoidance responses can be used to evaluate future prosthetic training involving obstacle crossings for amputee rehabilitation.

Introduction

Patients with a lower limb amputation are less successful than healthy controls when avoiding a suddenly appearing obstacle (Hofstad et al., 2006). In the present study, the question is asked why this deficit in OA (obstacle avoidance) occurs. A likely outcome is that the responses of the subjects are less effective (longer delay, smaller amplitude). There is evidence that the fastest responses in OA are due to a subcortical path (Weerdesteyn et al., 2004, Reynolds and Day, 2005a, Reynolds and Day, 2007) while later responses may rely more on pathways involving the motor cortex and voluntary control. It is possible for example that these patients have learned not to rely on fast responses but rather to rely on the late cortical responses. Another possibility is that these patients are less active in daily life than normal and therefore have less chances to exercise OA (“disuse” hypothesis (Renstrom et al., 1983b, Isakov et al., 1996, Lilja et al., 1998, Moirenfeld et al., 2000).

A second important issue is whether the changes in responses are bilateral. With a one-sided peripheral deficit (such as after amputation), a unilateral reorganisation of the motor cortex would be expected and then a delay in onset latencies on the prosthetic side would be plausible (without concomitant delay on the intact side). However, both stumbling reactions and OA responses require almost simultaneous activations on the contralateral (Pijnappels et al., 2004) and ipsilateral (Schillings et al., 2000) side. Furthermore, the higher failure rates are seen either when the prosthetic or the non-prosthetic leg is used in the OA task, suggesting that both legs react slower than normal (Hofstad et al., 2006). Would it make sense to have bilateral slowing of responses even when only one side is affected? A difference in delay on the two sides would make it difficult to achieve a well-coordinated synchronous response. This can explain some of the data on unilateral hemisphere lesions. For example, in hemiparetic cerebral palsy (CP) a delay (compared to control subjects) of fast adjustments of ongoing movements of the upper extremity was seen both on the affected and non-affected side (van Thiel et al., 2002). This implies a reorganization which is especially advantageous in movements requiring bilateral coordination.

In the present study, it was examined whether the increased failure rates in obstacle avoidance of patients with lower limb amputation could be explained by changes in latencies and/or amplitudes of obstacle avoidance responses. It was hypothesized, on the basis of the arguments presented above, that there would be a bilateral increase in latency and also a reduction of amplitudes of the OA reactions in these muscles.

Section snippets

Subjects

Eight subjects with a unilateral trans-tibial amputation participated in this study. The reason for amputation was traumatic in all subjects. All could walk independently on a treadmill without a walking aid. The subjects had no stump problems and did not suffer from problems of the nervous or musculoskeletal system. They all had good visual abilities and a high activity level (K3-level (HCFA, 2001)). The 5 males and 3 females were between the age of 23 and 49 years and had been using their

Results

Each participant could perform all trials safely, without getting exhausted. To ensure proper comparison, the treadmill speed was equal for the subjects with a lower limb amputation and the controls. Walking of the two groups was comparable, in confirmation of the previous study (Hofstad et al., 2006). The mean stride length was 93.7 and 85.1 cm for the control and amputation group, respectively, and the mean stance time duration was 70% and 72% of the step cycle in the two groups. Fig. 1 shows

Discussion

In the present study, OA was investigated in a group of patients with a trans-tibial amputation while walking on a treadmill. The results confirmed previously reported findings that patients with a trans-tibial amputation show increased failure rates compared to healthy controls during the OA task (>20% vs. 2%, respectively), particularly under high time pressure (Hofstad et al., 2006). The aim of the present study was to investigate the EMG onset latencies and response amplitudes of the lower

Acknowledgements

The authors gratefully acknowledge the contributions of POM Nijmegen (Prosthetics and Orthotics Centre) for assistance on subject recruitment of the amputation group and for giving support to the equipment of the gait laboratory. Furthermore, the authors would like to thank Nanny Steinmeijer, MD, Petra van Rees, Sasja Verhoeff and Hester Wijsen for their assistance in collecting the data.

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Limited research has focused on older prosthesis users despite the expected compounded effects of age and amputation on sensorimotor function, balance, and falls. This study compared sensorimotor factors and standing balance between older individuals with and without transtibial amputation, hypothesizing that prosthesis users would demonstrate worse sensorimotor function. Secondarily we assessed the relationship between standing balance and somatosensation in prosthesis users.
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In able-bodied adults, lead-limb toe clearance during obstacle crossing is typically reported to be around 12 cm but is about half that for amputees (Buckley et al., 2013), regardless of whether leading with the intact or the prosthetic limb (Hill et al., 1997). Irrespective of which limb they lead with, unilateral trans-tibial amputees (UTAs) make ten times as many errors than able-bodied individuals when trying to avoid obstacles during treadmill locomotion (Hofstad et al., 2006; Hofstad et al., 2009); due to bilaterally delayed response times, indicative of central nervous system (CNS) reorganisation (Hofstad et al., 2009). This reduced toe clearance and CNS reorganisation suggest that UTAs will have a higher trip risk when crossing obstacles compared to able-bodied individuals, and this higher trip risk may explain their increased incidence of falling (Miller et al., 2001).
Unilateral trans-tibial amputees have bilaterally reduced toe clearance, and an increased risk of foot contact, while crossing obstacles compared to the able-bodied. While the able-bodied tend to lead with a ‘preferred’ limb it is equivocal whether amputees prefer to lead with the intact or prosthetic limb. This study determined the effects of laterality, compared to side of amputation, on amputees' obstacle crossing performance. To help understand why laterality could affect performance we also assessed knee proprioception for both limbs.
Foot placement and toe clearance parameters were recorded while nine amputees crossed obstacles of varying heights leading with both their intact and prosthetic limbs. Joint-position sense was also assessed. Participants self-reported which limb was their preferred (dominant) limb.
There were no significant differences in foot placements or toe clearance variability across lead-limb conditions. There were no significant differences in toe clearance between intact and prosthetic lead-limbs (p = 0.28) but toe clearance was significantly higher when amputees led with their preferred compared to non-preferred limb (p = 0.025). There was no difference in joint-position sense between the intact and residual knees (p = 0.34) but joint-position sense tended to be more accurate for the preferred, compared to non-preferred limb (p = 0.08).
Findings suggest that, despite the mechanical constraints imposed by use of a prosthesis, laterality may be as important in lower-limb amputees as it is in the able bodied. This suggests that amputees should be encouraged to cross obstacles leading with their preferred limb.
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Ambulating with a transfemoral prosthesis is not only associated with high metabolic costs (Hoffman, Sheldahl, Buley, & Sandford, 1997), it also requires a considerable larger amount of cognitive resources compared to walking in individuals with intact limbs (Geurts & Mulder, 1994; Geurts, Mulder, Nienhuis, & Rijken, 1991; Heller, Datta, & Howitt, 2000; Hofstad et al., 2009; Williams et al., 2006).
Walking with a lower limb prosthesis comes at a high cognitive workload for amputees, possibly affecting their mobility, safety and independency. A biocooperative prosthesis which is able to reduce the cognitive workload of walking could offer a solution. Therefore, we wanted to investigate whether different levels of cognitive workload can be assessed during symmetrical, asymmetrical and dual-task walking and to identify which parameters are the most sensitive. Twenty-four healthy subjects participated in this study. Cognitive workload was assessed through psychophysiological responses, physical and cognitive performance and subjective ratings. The results showed that breathing frequency and heart rate significantly increased, and heart rate variability significantly decreased with increasing cognitive workload during walking (p < .05). Performance measures (e.g., cadence) only changed under high cognitive workload. As a result, psychophysiological measures are the most sensitive to identify changes in cognitive workload during walking. These parameters reflect the cognitive effort necessary to maintain performance during complex walking and can easily be assessed regardless of the task. This makes them excellent candidates to feed to the control loop of a biocooperative prosthesis in order to detect the cognitive workload. This information can then be used to adapt the robotic assistance to the patient’s cognitive abilities.
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Hill et al. [11] concluded that modulations of the stance limb served to position the pelvis further back from the obstacle as the height of the obstacle increased. Transfemoral (TF) amputee subjects make use of adjustment strategies to compensate for the loss of muscles and sensory input in their prosthetic limb during obstacle avoidance, and they learn to cope with bilaterally delayed and decreased obstacle avoidance responses in both limbs [13]. Vrieling et al. [14,15] found that the prosthetic knee flexion during obstacle avoidance of transfemoral amputee subjects was reduced in comparison with unimpeded walking and compared to TT amputees and able-bodied subjects.
In this study, conditions that enable a prosthetic knee flexion strategy in transfemoral amputee subjects during obstacle avoidance were investigated. This study explored the hip torque principle and the static ground principle as object avoidance strategies. A prosthetic limb simulator device was used to study the influence of applied hip torques and static ground friction on the prosthetic foot trajectory. Inverse dynamics were used to calculate the energy produced by the hip joint. A two-dimensional forward dynamics model was used to investigate the relation between obstacle–foot distance and the necessary hip torques utilized during obstacle avoidance. The study showed that a prosthetic knee flexion strategy was facilitated by the use of ground friction and by larger active hip torques. This strategy required more energy produced by the hip compared to a knee extension strategy. We conclude that when an amputee maintains enough distance between the distal tip of the foot and the obstacle during stance, he or she produces sufficiently high, yet feasible, hip torques and uses static ground friction, the amputee satisfies the conditions for enable stepping over an obstacle using a knee flexion strategy.
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Considering the above-mentioned limitations, we studied dual-task interference during OA (1) using a primary and secondary task that require continuous attention, (2) with the explicit instruction to perform as well as possible on both tasks, (3) using BF response times and composite scores. Previous research showed that even subtle changes in response times of the BF muscle are detectable [14]. Composite scores were previously used to deal with speed-accuracy trade-offs on a verbal reaction time task [15].
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Failures in obstacle crossing were noted and checked after the measurement using video recordings. Muscle activation of the biceps femoris of the crossing leg and the rectus femoris of the contralateral (supporting) leg were recorded, because the first responses to the obstacle are observed in these muscles [19,20]. Electromyography (EMG) electrodes were placed on the bellies of the muscles according to SENIAM guidelines (sample frequency 1000 Hz) [21].
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Evidence for bilaterally delayed and decreased obstacle avoidance responses while walking with a lower limb prosthesis

Abstract

Objective

Methods

Results

Conclusions

Significance

Introduction

Section snippets

Subjects

Results

Discussion

Acknowledgements

Neuroscience

Brain Res Rev

Electroencephalogr Clin Neurophysiol

Gait Posture

J Biomech

Arch Phys Med Rehabil

Clin Biomech

Arch Phys Med Rehabil

Arch Phys Med Rehabil

J Biomech

Curr Biol

J Neurosci Methods

Neuropsychologia

Gait Posture

Brain Res Brain Res Rev

Hum Mov Sci

Hum Mov Sci

J Biomech

Arch Phys Med Rehabil

Gating of sensation and evoked potentials following foot stimulation during human gait

Exp Brain Res

Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation

Nature

Energy expenditure of trans-tibial amputees during ambulation at self-selected pace

Prosthet Orthot Int