Effects of Therapeutic Gait Training Using a Prosthesis and a Treadmill for Ambulatory Patients With Hemiparesis
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1 ORIGINAL ARTICLE Effects of Therapeutic Gait Training Using a Prosthesis and a Treadmill for Ambulatory Patients With Hemiparesis Kimitaka Hase, MD, PhD, Etsuko Suzuki, PT, Maiko Matsumoto, MD, Toshiyuki Fujiwara, MD, PhD, Meigen Liu, MD, PhD 1961 ABSTRACT. Hase K, Suzuki E, Matsumoto M, Fujiwara T, Liu M. Effects of therapeutic gait training using a prosthesis and a treadmill for ambulatory patients with hemiparesis. Arch Phys Med Rehabil 2011;92: Objective: To examine the short-term effects of a newly developed hemiparetic gait training in which patients walk with a prosthesis applied to the nonparetic leg in the flexed knee position. Design: Pre-post nonrandomized controlled trial. Setting: Rehabilitation center and gait laboratory of a university hospital. Participants: Community-dwelling ambulatory volunteers (N 22) with chronic hemiparesis caused by a unilateral stroke. Intervention: Study subjects participated in a gait training program using either a below-knee prosthesis or a treadmill. Treadmill gait training was performed at a speed approximating the maximum gait velocity for each patient. The 3-week program consisted of a 5-minute gait training session 2 to 3 times a day. Main Outcome Measures: The ground reaction forces, stance time, step length and cadence during walking at a comfortable speed, and maximum gait speed, as well as the Berg Balance Score, were estimated before and after each training program. Results: In comparison with changes after the treadmill gait training, analyses of covariance demonstrated a significant increase of the fore-aft ground reaction forces during the paretic propulsion phase and a significant increase in the relative durations of the paretic and nonparetic single stance involved in a gait cycle after the prosthetic gait training (P.05). Conclusions: Prosthetic gait training would have different effects on a hemiparetic gait than treadmill gait training. The gait-related task inducing the dominant use of the paretic leg to support the body may be useful as a rehabilitative treatment to improve the kinetic abilities in the paretic stance period. Key Words: Gait; Paresis; Rehabilitation by the American Congress of Rehabilitation Medicine From the Department of Rehabilitation Medicine, Keio University School of Medicine, Tokyo (Hase, Matsumoto, Fujiwara, Liu); and Physical Therapy, Keio University Hospital, Tokyo (Suzuki), Japan. Supported by a Grant-in-Aid for Scientific Research (B) (grant no ). No commercial party having a direct financial interest in the results of research supporting this article has or will confer a benefit on the authors or on any organization with which the authors are associated. Reprint requests to Kimitaka Hase, MD, PhD, Associate Professor, Dept of Rehabilitation Medicine, Keio University School of Medicine, 35 Shinanomachi, Shinjuku-ku, Tokyo , Japan, khase@sc.itc.keio.ac.jp /11/ $36.00/0 doi: /j.apmr REHABILITATION TREATMENT for individuals with hemiparesis after a stroke aims to enhance their abilities, relieving them from a restricted community life. One of the more common concerns of ambulatory patients with hemiparesis who are living at home is that they cannot yet walk safely and efficiently. 1 Fundamentally, the patients develop adaptive and compensatory motor strategies represented by an asymmetric performance. 2-4 The mechanical demands of maintaining body balance in a dynamic situation compel the gait performance to be settled with the dominant use of the nonparetic leg and decreased walking speed. Thus, the hemiparetic gait is characterized by a reduced paretic propulsive force with a prolonged nonparetic stance time. 5-7 While getting along without the ability to generate the normal force levels of the paretic muscles, patients with hemiparesis may have diminished functional improvement of the paretic limb. The rehabilitative task of creating an opportunity for control of the body mass on the paretic leg is the very treatment required to relieve patients with hemiparesis from a restricted community life. To help patients with hemiparesis experience a dynamic and desirable gait pattern, task-specific, intensive, and progressive gait training programs using a treadmill, body-weight support system, and robotics have been developed. These devices allow the reproduction of a rhythmic gait pattern in which temporary and spatial parameters, such as gait velocity and step length, can be regulated to optimal values However, even in these rehabilitative situations, patients with hemiparesis can employ compensatory motor strategies using the nonparetic leg for performing a bipedal gait. Recent clinical and neurophysiologic studies concerning motor recovery of a paretic hand have suggested that the repeated use of the paretic limb, as well as the reduced sensory input from the nonparetic limb, should be involved in a rehabilitative task to provide functional improvements of the paretic limb. 12 To realize the relatively dominant use of the paretic leg together with the reduced input from the nonparetic leg, we developed a new method for hemiparetic gait training in which the patients must walk with a prosthesis applied to the nonparetic leg. 13 The resulting physiotherapeutic task may enable reorganization of the gait performance characterized by a reduced propulsive force. The aim of this study was to quantitatively assess the methodological issues and short-term effects of the prosthetic gait training (PGT) and compare them with those of treadmill gait training (TGT). METHODS Participants To safely and smoothly begin the PGT, patients who could independently ambulate with a prosthesis, even if they had undergone amputation of the nonparetic leg, 14 were enrolled. Inclusion criteria for the study were as follows: (1) 6 months ANCOVA GRF PGT TGT List of Abbreviations analysis of covariance ground reaction force prosthetic gait training treadmill gait training
2 1962 PROSTHETIC GAIT TRAINING FOR HEMIPARESIS, Hase after the onset of a first-ever stroke; (2) proprioceptive acuity for detecting the direction of about 5 of passive movements of the paretic ankle joint; and (3) independent 10-m walking without a cane. Exclusion criteria were as follows: (1) any known heart disease; (2) an orthopedic disease influencing gait training; (3) cognitive and communication problems that could hinder cooperation; and (4) previous TGT. One of main purposes of this study was to identify the training effects on propulsion insufficiency of the paretic leg. Through a reliability study on ground reaction force (GRF) data derived from stroke patients, Campanini and Merlo 15 indicated that a change of 1% of body weight for the mean value of the propulsive part could be considered significant in a follow-up evaluation. Assuming a common within-group SD of 1.0, a power analysis indicated that a sample size of 11 subjects in each group was sufficient to detect differences of 1% of body weight in mean propulsive force with a power of.85 and 2-tailed of.05. A total of 22 subjects, 42 to 80 years of age, gave their informed consent to participate in this study. TGT was prescribed to patients with hemiparesis who wanted to do it before PGT or who had participated in the therapeutic program for a paretic hand. The characteristics and the pretraining clinical scores of 11 patients in the PGT group and the other 11 in the TGT group are shown in table 1. There was no significant difference in the lower limb motor impairments evaluated by the Fugl-Meyer Assessment, the Modified Ashworth Scale assessment of the ankle joint, maximum gait speed, and the Berg Balance Score between the PGT and TGT groups. Apparatus A prosthesis designed to simulate an amputee s gait was used for gait training. It is a kind of orthosis for providing a new gait task (fig 1). A socket holding the nonparetic leg in the 90 -flexed knee position that was developed according to previous hemiparetic PGT experiences 13 was made for individual patients. To reproduce an actual gait pattern using the nonparetic leg, a less flexed knee position is desirable, but the increased shear force over the socket often results in skin injuries during gait training. A foot support required to prevent the leg sliding down from the less-flexed socket provides sensory feedback of the nonparetic ankle and foot load, which contradicts the PGT concepts. On the other hand, the 90 flexed socket would give an additional training effect through a reduction of compensatory nonparetic propulsive forces by shortening the hamstrings. The knee and ankle joints were fixed at 0 to control the paretic leg stance safely. A custom foot device was made, consisting of a flat and wide sole, with a short forefoot and a rocker bottom to allow easier toe clearance. As a result, patients with hemiparesis using the prosthesis are able to perform gait training without excessive controls for the nonparetic stance by dominantly using the paretic leg. Interventions Gait training sessions with a prosthesis or treadmill a were conducted 3 to 5 times per week. All patients implemented the training schedule for 3 weeks. In the gait training sessions, the physiotherapist facilitated extension of the paretic limb hip joint during the late stance phase. Blood pressure and pulse rate were evaluated manually before and immediately after every training session. If a systolic pressure of 150mmHg, a diastolic pressure of 100mmHg, or a pulse rate of 90 beats/min were exceeded before training, these parameters were monitored during gait training. Moreover, if increases in systolic ( 40mmHg) or in diastolic blood pressure ( 20mmHg) from resting blood pressure or an increase in pulse rate to greater than 150 beats/min occurred, training was discontinued. The skin condition of the nonparetic leg over the socket of a prosthesis was checked after the training session and if there was any redness, soft pads or a towel was used for reducing the pressure and shearing force of the prosthesis. Prosthetic gait training. Before the first training session, patients were given an opportunity to walk within parallel bars to practice swinging the nonparetic leg with a prosthesis. Then, the PGT sessions over the ground were assisted by a physiotherapist who faced the patient and supported the patient s arms or trunk. The early sessions were so strenuous for patients with hemiparesis that they were asked only to keep the trunk upright. After getting used to walking with a prosthesis, the patients were encouraged to perform rhythmical walking. Each training session was intended to last for 5 minutes, but a session was stopped if a patient became physically exhausted or hyperextension of the paretic knee joint occurred during the stance phase. If the subject could not complete 5 minutes of PGT in the first and second sessions, the third session was canceled. Thus, 2 to 3 PGT sessions a day were performed with an interval between sessions of several minutes for resting. Table 1: Subject Characteristics and Experimental Schedules Characteristics and Schedules PGT Group (n 11) TGT Group (n 11) P Subject Characteristics Age (y) Sex (male/female) 9/2 9/ Time since stroke (mo) Diagnosis (infarction/hemorrhage) 7/4 7/ Affected side (right/left) 6/5 5/6.670 Fugl-Meyer score (0 34) MAS (0 5) Maximum gait speed (m/s) Berg Balance Score (0 56) Training and Evaluation Schedules Days for training Training sessions Day of posttraining evaluation NOTE. Values are mean SD or as otherwise indicated. Raw data are provided. Statistics calculated using Mann-Whitney U and 2 tests. Abbreviation: MAS, Modified Ashworth Scale of ankle plantar flexors.
3 PROSTHETIC GAIT TRAINING FOR HEMIPARESIS, Hase 1963 cool-down walking, and this training was repeated 2 to 3 times a day with an interval between sessions of several minutes for resting. All patients completed the gait training program. The 3-week training and posttraining evaluation schedules between groups are shown in table 1. In the beginning of PGT, 5 subjects could not perform 3 sessions a day. However, there was no significant difference in the numbers of days and sessions for training, as well as the posttraining evaluation day. The clinical study to evaluate the effects of hemiparetic gait training was approved by the Keio University School of Medicine Ethics Committee. Measurements Gait analyses were performed at the study onset and in 2 to 5 days after 9 to 12 days of the gait training sessions. With the use of force platforms, c 3-dimensional GRFs were recorded over 10 gait cycles during walking without shoes at a comfortable speed (sampling rate, 1000Hz). If the patient used an ankle-foot orthosis for usual walking, a flexible ready-made orthosis was used to keep the patient safe during gait analyses. Then the maximum gait speeds while walking in the usual gait style across a 10-m walkway and the Berg Balance Score were measured. Data Analyses The GRF data were analyzed on an off-line computer. The kinetic 3-component GRF data were normalized by body weight for each subject (%GRF). Because the vertical GRF pattern in a hemiparetic gait often presented as a single peak rather than double peaks, the peak values were used to evaluate the weight-bearing on each leg. The lateral %GRF values were calculated as the lateral GRF component area divided by its time duration and averaged. Figure 2 shows the raw data on the fore-aft GRF under the paretic and nonparetic foot in pretraining (see fig 2A) and posttraining (see fig 2C), together with the one in intra-pgt (see fig 2B). The fore-aft GRF traces were divided into braking and propulsion phases according to the baseline. As the most appropriate parameters for assessing the progress of propulsion ability in patients with hemiparesis, 15 the mean amplitudes of an area with a positive peak as well as one with a negative peak for braking force were calculated. The stance time and step length were measured and averaged from the vertical components of GRF and center of pressure position data. The changes in temporal gait pattern were quantified by calculating the percentage of paretic and nonparetic single stance periods in a gait cycle (%single-stance). Fig 1. A prosthesis applied to nonparetic leg in flexed knee position. Treadmill gait training. After a few minutes of warm-up walking on the treadmill, the gait speed was increased, in communication with the patient, to the highest speed at which the patient could walk safely and without stumbling or toe dragging. The patients grasped a side bar with the nonparetic hand to control the body and maintain safe treadmill walking. An overhead harness without body weight support b was applied to some beginners. A physiotherapist who stood behind the patient stabilized the pelvis to induce weight-bearing on the paretic leg, in particular, during mid to late stance. If the patient was unable to maintain the speed with an optimal gait pattern, the speed was adequately reduced. The duration of a gait training session was 5 minutes in addition to the warm-up and Statistics Baseline characteristics were compared between the PGT and TGT groups using the Mann-Whitney U test and chisquare test as appropriate. To evaluate the effectiveness of the training, analysis of covariance (ANCOVA) was conducted after confirmation of a linear relationship between the baseline and outcome measurements, as well as no interaction between the groups and baseline measurements. The level of significance was set at P.05. The statistical analyses were performed using the JMP software. d RESULTS Changes in GRF Parameters in the Stance Phase During gait with a prosthesis, the patient shown in figure 2 required long-term contribution of the paretic leg for propul-
4 1964 PROSTHETIC GAIT TRAINING FOR HEMIPARESIS, Hase Fig 2. Raw data on fore-aft GRF (GRFf-a) under the paretic and nonparetic foot in the pretraining (A), intratraining on the 8th day for PGT (B), and posttraining (C) in a representative subject with right hemiparesis. Note that the intratraining GRFs were measured while a physiotherapist supported both arms of the patient. Abbreviation: BW, body weight. sion under the condition of a remarkably decreased nonparetic propulsive force. As a result, a larger propulsive force with the peak shifted toward the end of the paretic stance was developed after the PGT. Also in the posttraining gait, an increased paretic braking duration and nonparetic propulsive force were found in this patient. The 3-component %GRF values in the stance phase during comfortable walking and the results of ANCOVA are provided in table 2. The changes in propulsive force of the paretic leg differed significantly between groups in ANCOVA (P.05), being significantly larger in the PGT group than in the TGT group. There was a trend of different intervention effect in the lateral %GRF under the nonparetic foot (P.086), but no differences were detected between groups for changes of the GRF-related parameters except for the paretic propulsive force. Table 2: Comparison of %GRF Values During Comfortable Walking PGT Group (n 11) TGT Group (n 11) Variables Pre Post Pre Post Vertical GRF 1st peak (%) Paretic side Nonparetic Lateral GRF (%) Paretic side Nonparetic Fore-aft GRF (%) Propulsive force Paretic side Nonparetic side Braking force Paretic side Nonparetic side NOTE. Values are mean SD or as otherwise indicated. Statistics calculated using ANCOVA. P
5 PROSTHETIC GAIT TRAINING FOR HEMIPARESIS, Hase 1965 Table 3: Comparison of Temporospatial Gait Parameters and Balance Score PGT Group (n 11) TGT Group (n 11) Variables Pre Post Pre Post Comfortable gait speed (m/s) Stance time (s) Paretic side Nonparetic side Single stance time (%) Paretic side Nonparetic side Step length (cm) Paretic side Nonparetic side Cadence (steps/min) Maximum gait speed (m/s) Berg Balance Score (0 56) NOTE. Values are mean SD or as otherwise indicated. Statistics calculated using ANCOVA. P Changes in Temporal and Spatial Gait Patterns and Balance Ability The temporal and spatial gait parameters during comfortable walking, the maximum gait speed, and the Berg Balance Scores before and after gait training sessions are presented in table 3. The changes of the %single-stance values in the paretic and nonparetic leg differed significantly between groups in ANCOVA (P.05), with increases after the PGT. However, there were no significant differences in the changes of the other temporospatial gait parameters and the Berg Balance Scores. DISCUSSION The results reveal that PGT has different short-term effects on the gait performance of ambulatory patients with chronic hemiparesis than TGT has. As expected, a task-specific intervention that minimized the compensatory strategies of the nonparetic knee and ankle joints during walking resulted in the increased paretic propulsive force and %single-stance periods. This implies that the participants acquire a skill to keep their body mass on the paretic leg in a gait cycle. It is likely that the observed improvement is strongly associated with the kinetic requirement to step the nonparetic leg with a prosthesis forward. Precise kinetic measurements in a hemiparetic gait with a prosthesis are difficult walking because walking without any help, is difficult for the patients. However, we found a remarkable decrease in propulsive force from a prosthesis with a foot device having a short forefoot and a rocker bottom (see fig 2). To swing the nonparetic leg with the functionally increased length because of impossible knee flexion, the body mass would be properly shifted to the paretic leg and stabilizing the nonparetic early stance without an ankle mechanism settling the floor impact would be stabilized by the trailing paretic leg. As a result, patients with hemiparesis who had depended on nonparetic propulsive force 6 would inevitably acquire the skill to increasingly support the body in the paretic stance period. During PGT, it was certain that the patients walked with a slower speed (see fig 2) and less step length than usual. Nevertheless, the changes of step length, cadence, and gait speed were equivalent to those by TGT at the highest walking speed. Through optimizing the relationship between postural stability and temporospatial parameters during walking, 16,17 the additional power generated by the paretic leg would be transferred to their gait performance after removal of a prosthesis. On the other hand, a trend of reduced nonparetic lateral GRF after TGT may indicate superior effectiveness of repeated highspeed walking for managing lateral dynamics on the nonparetic leg. Thus, by comparison with TGT, the task specificity of PGT exists in kinetic management by the paretic leg but not on temporospatial regulation for locomotion. Possible mechanisms underlying the changes of gait pattern in overground walking after PGT include a load feedback repeated only onto the paretic leg. The repetitive feedback from load receptors during the gait cycle is used as extensor reinforcing feedback. 18 Animal studies suggest that the loadsensitive group Ib afferents of the ankle plantar flexors and the cutaneous afferents located on the plantar surface of the foot excite the limb extensor muscles while inhibiting flexor muscles, effectively prolonging stance and delaying swing initiation. A recent human study 19 on the role of ankle-foot load afferents revealed that the stance phase load produced a significant increase in peak hip extension moment in subjects with spinal cord injury as well as in nondisabled subjects. The human Ib facilitation from the gastrocnemius to the soleus muscle requires not only loading but also locomotion movements. 20 These findings will lead us to develop a rehabilitative method in which the patients must walk with an increased paretic load. In addition, the task specificity of PGT contains continuous unloading of the nonparetic ankle and foot in a gait cycle. Although the plastic change in the central nervous system caused by unloading is unclear, the absence of load feedback may contribute to interlimb coordination such as the prolonged stance time of the sound leg in amputees. 21 Study Limitations A clear limitation of the present study is the small sample size, increasing the possibility of a type II statistical error limiting the ability to detect true changes. Moreover, there is a need for clinical trials to verify the long-term effects of PGT on patients with various degrees of symptom severity. A bipedal gait in which the nonparetic leg always participates to control dynamic postural stability during overground walking may adaptively change over time. Such adaptive changes subsequent to gait training sessions will directly influence the outcome of rehabilitative treatments. The potential application of prosthetics to assistance-based training using a body weightsupported system may extend the clinical indications and cause additional effects. We need a better understanding of which participants will achieve desirable gait patterning. A future
6 1966 PROSTHETIC GAIT TRAINING FOR HEMIPARESIS, Hase study that includes the measurement of long-term effects and minimizes the bias in the allocation of patients to treatment groups should be conducted. CONCLUSIONS The present results show that PGT has a different taskspecific effect on hemiparetic gait performance than does TGT. Rehabilitative treatments to maximize functional motor recovery of the paretic limb must consist of motor tasks in which compensatory motor strategies are eliminated as much as possible. The use of a prosthesis in hemiparetic gait training will surely provide an opportunity to use the paretic leg during walking. Such therapeutic exercises may be considered as task-oriented training for reorganizing the gait ability of patients recovering from a stroke. References 1. Lord S, McPherson K, McNaughton H, Rochester L, Weatheerall M. Community ambulation after stroke: how important and obtainable is it and what measures appear predictive? Arch Phys Med Rehabil 2004;85: Roth EJ, Merbitz C, Mroczek K, Dugan SA, Suh WW. Hemiplegic gait. Relationships between walking speed and other temporal parameters. Am J Phys Med Rehabil 1997;76: Chen CL, Chen HC, Tang SFC, Wu CY, Hong WH. Gait performance with compensatory adaptation in stroke patients with different degrees of motor recovery. Am J Phys Med Rehabil 2003; 82: Balasubramanian CK, Bowden MG, Neptune RR, Kautz SA. Relationship between step length asymmetry and walking performance in subjects with chronic hemiparesis. Arch Phys Med Rehabil 2007;88: Lamontagne A, Richards CL, Malouin F. Coactivation during gait as an adaptive behavior after stroke. J Electromyogr Kinesiol 2000;10: Bowden MG, Balasubramanian CK, Neptune RR, Kautz SA. Anterior-posterior ground reaction forces as a measure of paretic leg contribution in hemiparetic walking. Stroke 2006;37: Kim CM, Eng JJ. Symmetry in vertical ground reaction force is accompanied by symmetry in temporal but not distance variables of gait in persons with stroke. Gait Posture 2003;18: Pohl M, Mehrolz J, Ritshel C, Rückriem S. Speed-dependent treadmill training in ambulatory hemiparetic stroke patients. A randomized controlled trial. Stroke 2002;33: Werner C, von Frankenberg S, Treig T, Konrad M, Hesse S. Treadmill training with partial body weight support and an electromechanical gait trainer for restoration of gait in subacute stroke patients. A randomized crossover study. Stroke 2002;33: Patterson SL, Rodgers MM, Macko RF, Forrester LW. Effect of treadmill exercise training on spatial and temporal gait parameters in subjects with chronic stroke: a preliminary report. J Rehabil Res Dev 2008;45: Hornby TG, Campbell DD, Kahn JH, Demott T, Moore JL, Roth HR. Enhanced gait-related improvements after therapist- versus robotic-assisted locomotor training in subjects with chronic stroke: a randomized controlled study. Stroke 2008;39: Ward NS, Cohen LG. Mechanisms underlying recovery of motor function after stroke. Arch Neurol 2004;61: Hase K, Fujiwara T, Tsuji T, Liu M. Effects of prosthetic gait training for stroke patients to induce use of the paretic leg: a report of three cases. Keio J Med 2008;57: OConnell PG, Gnatz S. Hemiplegia and amputation: rehabilitation in the dual disability. Arch Phys Med Rehabil 1989;70: Campanini I, Merlo A. Reliability, smallest real difference, and concurrent validity of indices computed from GRF components in gait of stroke patients. Gait Posture 2009;30: Latt MD, Menz HB, Fung VS, Lord SR. Walking speed, cadence, and step length are selected to optimize the stability of head and pelvis accelerations. Exp Brain Res 2008;184: Teixeira-Salmela LF, Nadeau S, Milot MH, Gravel D, Requião LF. Effects of cadence on energy generation and absorption at lower extremity joints during gait. Clin Biomech 2008;23: Duysens J, Clarac F, Cruse H. Load regulating mechanisms in gait and posture: comparative aspects. Physiol Rev 2000;80: Gordon KE, Wu M, Kahn JH, Dhaher YY, Schmit BD. Ankle load modulates hip kinematics and EMG during human locomotion. J Neurophysiol 2009;101: Faist M, Hoefer C, Hodapp M, Diets V, Berger W, Duysens J. In humans Ib facilitation depends on locomotion while suppression of Ib inhibition requires loading. Brain Res 2006;1076: Isakov E, Keren O, Benjuya N. Trans-tibial amputee gait: timedistance parameters and EMG activity. Prosthet Orthot Int 2000; 24: Suppliers a. StairMaster; Quinton Cardiology Systems, Inc, 3303 Monte Villa Pkwy, Bothell, WA. b. Dynamic Unweighing System; BIODEX Medical Systems, Inc, 20 Ramsay Rd, Shirley, NY. c. Model MG-1090; Anima Corp, Shimoishihara, Chofu City, Tokyo, Japan. d. SAS Institute Inc, 100 SAS Campus Drive, Cary, NC
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