Arm-plane representation of shoulder compensation during pointing movements in patients with stroke

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Abstract

Improvements in functional motor activities are often accompanied by motor compensations to overcome persistent motor impairment in the upper limb. Kinematic analysis is used to objectively quantify movement patterns including common motor compensations such as excessive trunk displacement during reaching. However, a common motor compensation to assist reaching, shoulder abduction, is not adequately characterized by current motion analysis approaches. We apply the arm-plane representation that accounts for the co-variation between movements of the whole arm, and investigate its ability to identify and quantify compensatory arm movements in stroke subjects when making forward arm reaches. This method has not been previously applied to the analysis of motion deficits. Sixteen adults with right post-stroke hemiparesis and eight healthy age-matched controls reached in three target directions (14 trials/target; sampling rate: 100 Hz). Arm-plane movement was validated against endpoint, joint, and trunk kinematics and compared between groups. In stroke subjects, arm-plane measures were correlated with arm impairment (Fugl-Meyer Assessment) and ability (Box and Blocks) scores and were more sensitive than clinical measures to detect mild motor impairment. Arm-plane motion analysis provides new information about motor compensations involving the co-variation of shoulder and elbow movements that may help to understand the underlying motor deficits in patients with stroke.

Introduction

Upper limb movements in patients with stroke are often accompanied by motor compensations such as excessive trunk and/or scapular movement (Cirstea and Levin, 2000, Niessen et al., 2008). Reaches of the paretic arm are also characterized by abnormal muscle co-activation of the shoulder abductors with the elbow extensors (Dewald et al., 1995, Kisiel-Sajewicz et al., 2011), a stereotypical pattern that has been described as an abnormal flexor synergy (Twitchell, 1951, Brunnstrom, 1970) and thought to be due to substitution of corticospinal pathways by corticobulbar motor pathways (Dewald and Beer, 2001, Ellis et al., 2009). The use of motor compensations and stereotypical movement synergies may contribute to functional improvements without the occurrence of genuine motor recovery, defined here as the reappearance of movement patterns typically seen in healthy subjects (Levin et al., 2009, Levin and Panturin, 2009). Thus, in order to identify motor improvement due to spontaneous processes or intervention, it is necessary to differentiate between gains in motor ability due to confounders such as compensation and use of synergies from those due to true motor recovery.

Recently, several studies have focused on characterizing recovery of upper limb movement in stroke by identifying the covariance between individual degrees of freedom of the arm (Alt Murphy et al., 2011, Van Kordelaar et al., 2012). However, normal goal-directed movement does not result from a series of independent joint rotations but rather from the coordination of several joints together, often referred to as a synergy (Latash, 2010). The notion of movement synergy differs from that of the abnormal movement synergies described in stroke patients in the early part of the last century (Twitchell, 1951, Brunnstrom, 1970). The abnormal upper limb flexor synergy is described by scapular, shoulder and elbow movements that are constrained to move together. This synergy is characterized by the loss of independent joint motion and the presence of stereotypical movements consisting of elbow flexion, forearm supination, shoulder abduction and external rotation and scapular retraction and/or elevation (Brunnstrom, 1970, Bourbonnais et al., 1989, Dewald and Beer, 2001). Previous studies have characterized this multi-joint flexor synergy during isometric efforts (Dewald et al., 1995, Beer et al., 2000, Dewald and Beer, 2001) and during planar arm reaching movement with and without proximal limb support (e.g., Sukal et al., 2007). However, the contribution of the abnormal synergy to natural 3D functional reaching movement, characterizing the motor impairment during real-world arm use, has not been described.

Mathematical representations of kinematic covariance can be useful for the description of upper limb motor synergies. One such geometrical formulation is the arm-triangle, described by Hestenes (1994). The arm-triangle is formed by the proximal and distal arm segments, and the vector connecting the shoulder and wrist. The combined motion of the three degrees of freedom (DoF) of the shoulder is reflected by rotation and translation of the rigid body formed by the arm-triangle. Elbow flexion–extension movement is described by the change in the arm-triangle shape. The plane in which the triangle is embedded is termed the arm-plane. Arm-plane motion has been used to analyze kinematic redundancy and inter-joint coordination for pointing (Berman et al., 2008), grasping (Wang, 1999) and object manipulation tasks in healthy subjects (Klein Breteler and Meulenbroek, 2006). This method has not been previously applied to the analysis of motion deficits. It has the potential to provide a more detailed description of angular co-variation and motor compensation during reaching tasks in subjects with stroke. Since it takes into account the co-variation between adjacent arm joints, we hypothesized that the arm-triangle measure would provide more detailed information about the contribution of arm synergy patterns to deficits in functional reaching than descriptions of individual joint rotations or clinical measures in this patient group. This description of abnormal synergy patterns during functional arm tasks may provide clinicians with a better focus for motor retraining aimed at improving upper limb function in patients with stroke. While a description of rotations based on the arm-triangle requires some specific computations, because it is done with a reduced marker set, in practice it simplifies the data collection process. Calculations are based on three markers (only those delimiting the arm triangle) as opposed to having a full rigid-body representation with a minimum of three markers per segment to define six degrees of freedom (three translations, three rotations).

The goal of the study was to describe the temporal and spatial characteristics of 3D reaching movements using arm-plane variables and to identify their relationship with upper limb motor deficits in subjects with chronic stroke. The relationship between arm-plane measures and more commonly used endpoint and joint kinematic measures was also determined.

Section snippets

Participants

Sixteen right-hemiparetic, right-handed, stroke subjects (13 males, three females; age range 65.2 ± 9.8 years) and eight healthy age-matched right-handed control subjects (three males, five females; age range 58.6 ± 7.0 years) participated in the study. No neurological, sensorimotor or orthopedic impairments were reported for the controls. Participants with stroke met the following criteria: (a) ability to understand the task, (b) >2 months following a single unilateral stroke; (c) arm recovery stage

Results

Profiles of arm-plane movements of control subjects were stereotypically sigmoid but those of stroke subjects were more variable (Fig. 3). Means and standard deviations of movement variables are presented by subject group and pointing direction in Table 2. Arm-plane variable results are detailed below.

Discussion

We describe a new way to analyze multi-joint synergies and compensatory movements of the shoulder and arm during functional reaching tasks in people with chronic stroke. Previous research has described other compensations such as trunk displacement and shoulder abduction. The new representation provides a means by which the complex change of configuration of the arm over time can be quantified. This has not been shown before from the kinematic perspective (but see Reisman and Scholz (2006) for

Conclusions

Having alternative descriptions of multi-joint motor impairment allows us to better understand how the motor system may take advantage of redundancy during the process of recovery from central nervous system lesion. The advantage of this approach in the measurement of arm movement is that it provides a way of characterizing 3D compensatory movements of the whole arm compared to individual joint planar kinematics, and that the measure can be recorded with a reduced marker set (only three markers

Acknowledgment

The authors wish to thank Dr. Valeri Goussev from McGill University and Dr. Yisrael Parmet from Ben-Gurion University for their valuable advice. We also thank Prof. Patrice (Tamar) Weiss and Dr. Harold Weingarden from the Sheba Medical Center, Israel, for their assistance in Helsinki Ethics Approval and for facilitating the data. MFL holds a Tier 1 Canada Research Chair in Motor Recovery and Rehabilitation. Supported by REPAR-FRSQ (Quebec) and the Israel–France Research Networks Program in

Tal Merdler, completed a M.Sc. degree in Industrial Engineering and Management, specializing in intelligent systems in 2011 and a B.Sc. degree in Industrial Engineering and Management, specializing in production field, in 2010 at the Ben-Gurion University of the Negev in Beer-Sheva, Israel. Her thesis was on development of objective measures for upper limb rehabilitation after stroke.

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    Tal Merdler, completed a M.Sc. degree in Industrial Engineering and Management, specializing in intelligent systems in 2011 and a B.Sc. degree in Industrial Engineering and Management, specializing in production field, in 2010 at the Ben-Gurion University of the Negev in Beer-Sheva, Israel. Her thesis was on development of objective measures for upper limb rehabilitation after stroke.

    Dario G. Liebermann, completed a Ph.D degree in applied mathematics and computer sciences in 1998 (Weizmann Institute of Sciences, Rehovot, Israel) followed by post-doc research in clinical motor neurosciences in the Faculty of Medicine of the University of Calgary, Canada. Previously, he earned a M.Sc. degree (1988) in motor control from the Faculty of Applied Sciences at the Simon Fraser University, Canada. Since 2000 he is with the Sackler Faculty of Medicine at the Tel-Aviv University and currently he is the Chairperson of the Department of Physical Therapy. Dr. Liebermann lectures and investigates neuromotor control in healthy and clinical populations.

    Mindy F. Levin, is professor in the School of Physical and Occupational Therapy at McGill. After obtaining her BSc.(PT) in 1976, she specialized in neurological clinical practice and obtained her M.Sc. in Clinical Sciences (Montreal,1985) and Ph.D. in Physiology (McGill, 1990). Following post-doctoral work in neurophysiology (Montreal 1992), Dr. Levin was researcher and professor at the School of Physiotherapy (Montreal, 1992–2004), and then Director of the Physical Therapy Program at McGill (2004–2008). Dr. Levin is/was Scientific Director, Research Centre of the Rehabilitation Institute of Montreal (1997–2001); President, International Society for Motor Control (2005–2007), founding member and Awards convenor, International Society for Virtual Rehabilitation and founding member, International Neurosciences Physical Therapy Association branch of WCPT. She holds a Tier 1 Canada Research Chair in Motor Recovery and Rehabilitation.

    Sigal Berman, is a lecturer and head of the intelligent system M.Sc. track in the department of Industrial Engineering and Management at the Ben-Gurion University of the Negev. She received a M.Sc. in Electrical and Computer Engineering, and a Ph.D. in Industrial Engineering, both from Ben-Gurion University of the Negev, Israel, and a B.Sc. in Electrical and Computer Engineering, from the Technion, Haifa, Israel. She was a research assistant at the Center for Autonomous Control Engineering at the department of Electrical and Computer Engineering, The University of New Mexico, USA and a Postdoctoral fellow at the department of Computer Science and Applied Mathematics at The Weizmann Institute of Science, Rehovot, Israel. Currently, Dr. Berman lectures and investigates robotics and human motor control.

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