Gait impairment in neurological disorders: a new technological approach

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1 Gait impairment in neurological disorders: a new technological approach Roberta Semprini, MD a 1 Patrizio Sale, MD a 1 Calogero Foti, MD b Massimo Fini, MD a Marco Franceschini MD a a IRCCS San Raffaele Pisana, Rome, Italy b Physical and Rehabilitation Medicine, Public Health Department, Tor Vergata University, Rome, Italy Corresponding author: Marco Franceschini IRCCS San Raffaele Pisana Via della Pisana, 235 Rome, Italy marco.franceschini@sanraffaele.it Summary Gait recovery is considered one of the main objectives of rehabilitation interventions in neurological disabilities, as restricted movement can significantly reduce an individualʼs ability to take part in normal activities of daily living. Locomotor training has been shown to improve gait rehabilitation. Studies have recently been published on the use of robots and other devices in patients with gait disabilities, particularly in the rehabilitation of the lower limbs. However, analysis of the recent literature reveals a relative paucity of strong methodological studies. The evidence that is available, while strong, is not yet sufficient to allow definite conclusions to be drawn regarding the efficacy of these devices. From these considerations, it is clear that validated and standardized methods need to be adopted for each of the different systems available. This would help to clarify the indications for and correct use of robotic devices in the different neurological disorders. KEY WORDS: Exoskeleton, gait, rehabilitation, robot, treadmill. Introduction Gait recovery is considered one of the main objectives of rehabilitation interventions in neurological disabilities such as stroke, traumatic injuries, multiple sclerosis, Parkinsonʼs disease (PD), and peripheral nerve palsy (1). Depending on the site and extent of the lesion, the degree of disability after an acute event can range from 1 RS and PS contributed equally to this work. moderate locomotion disorders (balance problems, slow walking speed, poor endurance and physiological alterations of locomotor patterns) to more serious conditions, such as hemiparesis, hemiplegia or even paraplegia (2). Movement restrictions, in particular gait disturbances, can significantly reduce an individualʼs possibility of taking part in normal daily activities (1). Many neurophysiological studies on the role played by central and peripheral generators of movement (3-6) have shown that: i) supraspinal structures are not necessary to generate the basic motor patterns; ii) neural networks, or central pattern generators (CPGs), located entirely in the spinal cord, produce the basic rhythm of walking and are also capable of producing the rhythmic movements seen in swimming, walking and skipping, even without the control of the encephalon and sensory afferents; iii) the circuits of locomotion can be activated by signals descending from different cranial levels of the central nervous system (CNS). iv) supraspinal inputs play an important role not only in initiating locomotion but also in adapting the locomotor pattern to environmental and motivational conditions; v) the sensory afferents involved in cutaneous reflexes (esteroception) and muscle reflexes (proprioception), while not required for the activation of spinal neural networks, have important regulatory functions in preserving balance and ensuring stability in all phases of the gait cycle. Because these features are slightly modified with variations in the ground variables on which the subject is walking, robotic devices were introduced into clinical practice in order to obtain maximal benefits from gait rehabilitation programmes. Following their introduction, there appeared numerous studies (7-9) that assessed the efficacy and validity of body weight supported treadmill training (BWSTT), which uses an adjustable-speed mobile platform system, associated with classical rehabilitation treatments in patients with gait disturbances. This type of exercise, which features among the activities of functional re-education (task-oriented therapy), also has aspects which go beyond the mere recovery of movement, and these include the benefits which result from early standing. Indeed, early restoration of the standing position promotes normalization of the bodyʼs position in space and correct perception of spatial coordinates, thereby helping to prevent the onset of neurophysiological disorders. Furthermore, both the upright position and movement can help to reduce the risk of early heart disease and respiratory diseases. The aim of this review is to discuss clinical experiences in the use of these devices for rehabilitation, the advantages they offer patients and therapists, the clinical indications for their use, and their future perspectives. Functional Neurology 2009; 24(4):

2 R. Semprini et al. Devices Electromechanical and robot-assisted gait training devices are used in rehabilitation and can help to improve walking in patients with disabilities following stroke or other brain injuries. Several studies have been published on the use of robots and other devices in the rehabilitation of the lower limbs. Finch and Barbeau in 1991 (10) first advanced the idea of home physical support systems for patients with neurological disabilities, such as systems of straps to support the weight of the body and assist the legs during treadmill walking (11,12). This kind of system consists of a treadmill and a mounting frame with a harness in which the patient is mechanically supported while walking on the treadmill (11). Because the body weight support (BWS) system unloads the patientʼs body weight symmetrically from the lower limbs as the patient moves forwards, balance control is improved and falls are avoided. Furthermore, using a combined BWS-treadmill system makes it possible to achieve stabilization of the trunk, reducing the postural requirement, and also gives the patient the opportunity to repeat several complete step cycles. The speed of the treadmill, which is adjustable, is set according to the patientʼs supposed level of motivation, while the percentage of body weight unloading employed during gait training with BWS is +/- 30% (12-14). Under the supervision of a physiotherapist, BWSTT stabilizes the trunk, allows correct transfer of load even from the hemiplegic limb, and selective activity of the anti-gravity muscles; it can therefore promote the early achievement of correct and complete rehabilitation. The support can be reduced progressively over sessions until the point is reached at which (if the clinical situation allows it) it can be eliminated altogether. On the other hand, the relief of both lower limbs symmetrically by the load suspension can result in an asymmetrical gait pattern, which is more effective than that produced in the gait re-education programme with assistance of the traditional type. Studies have been performed in different types of patients, but acute and chronic stroke patients have been the focus of particular attention. Several studies using conventional gait training have been conducted on patients with sub-acute stroke unable to walk. These patients received conventional treatment consisting of overground or treadmill gait training (5-7,10,11). The differences between walking on a treadmill and walking over ground have been examined in healthy adults (5,15,16) and in individuals with stroke (9,11). Hesse et al. (17) developed a BWSTT device that needs the presence of only one therapist. This mechanical system (Gait Trainer GT1) automatically advances each leg alternately. The patientʼs feet are positioned on mobile media operated by an external system that simulates the movement of the feet during stance and swing. This walking can be programmed for the individual patient. The movement produced reflects natural human gait, although it is not identical. The vertical and horizontal movements of the centre of mass are controlled by cables attached to a harness. The patientʼs knees are free and not blocked by orthoses, thereby allowing the therapist direct contact with the patient. This makes it possible to personalize any corrective interventions. New automated electromechanical and robot-assisted gait training devices (exoskeletons) have also been developed to improve walking after stroke and several other pathologies. These devices, also known as robotic gait orthoses, facilitate the emergence of a bilaterally symmetrical gait pattern, assisting the individual as he/she actively attempts to advance each limb while walking on the treadmill. Motors on each robotic leg facilitate the movement of the hip and knee joints in accordance with trajectories programmed by the manufacturer on the basis of a healthy individualʼs gait pattern. The pre-programmed walking pattern corresponds to normal gait kinematics as reflected, for example, in: gait cycle timing, inter-limb and inter-joint coordination, appropriate limb loading, and afferent signalling. Experimental research into CPGs (11) stimulated the creation of Lokomat, a robot developed to facilitate the delivery and management of BWSTT therapies, designed to be used by a trained operator (18). The Lokomat robotic system is composed of four parts: a robotic exoskeleton allowing customized adjustment of orthoses, a load-lightening system, a step ergometer (treadmill), and two PCs with integrated software control. The exoskeleton, which is first adapted to the patientʼs anthropometric measurements, provides partial BWS and moves the lower limbs of the patient who is standing on a treadmill (simulating gait). The temporal and spatial parameters of the step can be adjusted and adapted to the individual patient. All the kinetic data acquired during the walking are fed back to the patient and operator. The exoskeleton robot is equipped with motorized systems to allow automatic advance of the lower limb according to the speed set on the treadmill. The support system is electronic and monitors the force sensors; this ensures smooth running of the treadmill, low inertia, and the maintenance of biomechanically correct movement. The robotic system is able to generate gait patterns that reflect typical physiological activities like walking, with alternate flexion/extension of the joint components typically involved in the step cycle. Using these mechanical and robotic systems a patient can cover between 500 and 1500 metres, recording a high number of steps in a single 40-minute treatment session. Clinical experiences The aims of rehabilitation in patients with motor impairment (due to stroke, multiple sclerosis, brain traumas, PD) are to get the patient walking independently, to maximize gait speed and endurance, and also to reduce costs. Traditional rehabilitation programmes have shown that task specificity and intensity of training, in terms of hours of therapy, are the main determinants of functional improvement in patients suffering from motor disability (19). In fact, intensive task-oriented (as opposed to nontask-oriented) practice can induce greater improvements in walking competence (20,21). Task-oriented training can also be developed with a more functional approach, e.g. organized as a circuit with series of workstations designed to increase opportunities to improve the efficacy of the rehabilitation practice (22). In particular, the presence of workstations allows the therapist to customize the training programme to the individual participant, modifying variables such as intensity, frequency and duration of exercise, number of repetitions and com plexity of exercises (23). 180 Functional Neurology 2009; 24(4):

3 Gait impairment in neurological disorders: a new technological approach Conventional gait training depends on the manual support and guidance provided by physical therapists, particularly in patients with severely impaired motor and postural control (24); in view of this limitation, the idea of introducing mechanical support systems in order to increase the efficacy of treadmill gait training (also reducing costs and the time therapists need to devote to individual patients) gained prominence (25). Systems for supporting a percentage of body weight, in order to allow safe weight shifting and stepping, were developed and BWSTT became a reality. Since the introduction of this support into rehabilitation programmes, several studies have set out to evaluate its reliability (26,27). On the one hand, these studies, analyzing the spatial-temporal and kinetic parameters of gait, have given encouraging results, suggesting that the use of this support might improve walking outcomes, partly by allowing patients, through progressive repetitive practice, to re-learn the motor patterns of walking: limb loading, velocity, and stride length (28). However, on the other hand, they have also highlighted disadvantages. The use of treadmill training may make natural execution of the locomotor pattern difficult. Other possible drawbacks are the patientʼs limited control of the joints of the lower limbs, and the repetition of only kinematically normal, standard steps throughout the entire training session (29). Another consideration was the awkward position of the therapist during the entire training session. Hence, new automated locomotion systems were developed to facilitate step training and to reduce or eliminate the need for manual assistance from the physical therapist (29). Robotic assistive treadmill devices, or gait machines, like the Lokomat or the Gait Trainer GTI, have been commercially available for years and shown varying patterns of therapeutic efficacy (30-33). Early studies in patients suffering from acute and chronic disabilities, in particular patients with partial or complete spinal cord lesions, demonstrated that BWSTT gave better results only in patients with partial lesions of the spinal cord, while those with complete lesions showed no improvement at all (34). More recently BWSTT was used for the rehabilitation of stroke patients (35). Most studies evaluating the efficacy of BWSTT in this population compared it with traditional rehabilitation training. Among people with stroke, BWSTT was found to produce significant improvements only in patients who could already walk independently at the start of the treatment. Although the results of these studies (34,35) showed statistically significant improvements, Cochrane systematic review analyses (26,27) failed to demonstrate for treadmill training, with or without BWS, any added efficacy in patients with stroke compared with traditional rehabilitation training. However, in view of the paucity of well-designed large-scale studies, the need for validation of automated support systems in terms of activities of daily living and quality of life domains in systematic studies, and also the great number of variables not considered in individual studies (i.e. walking speed and endurance in independent walkers, lack of independent walking in severe cases, continued lack of independent walking), it was concluded that more studies are needed. Thus, in general, data on BWSTT cannot yet be considered conclusive. Body weight supported treadmill training has also been used in patients with multiple sclerosis, in whom gait disturbances may develop from the early phases of the disease (36). The results suggested that BWSTT could potentially be a useful intervention for reducing gait impairment, but more studies are needed to support this suggestion. The use of treadmill training in PD, with or without BWS, is challenging. While PD patients have less difficulty standing, they need, in particular, to improve their motor control: these patients frequently have gait disturbance, associated with an increased risk of falls and loss of independence. A growing body of evidence suggests that treadmill training may be used as a complementary or alternative option for treating gait disturbances and enhancing quality of life in PD (37,38). A recent review analysis on treadmill training in PD concluded that patients receiving treadmill training showed improvements in their gait hypokinesia. In particular they recorded improvements in gait speed, stride length and walking distance, without adverse effects during treatment. However it is still unclear when and how this treatment should be used, and whether it should be part of routine rehabilitation programmes in this population (39). Electromechanical and robot-assisted arm training devices have been used in patients with stroke. These devices were introduced to render gait more efficient, through improvement of arm function after stroke (29). Even though individual studies have reported significant improvements in stroke patients using the Lokomat (32,33), review articles have shown that electromechanical and robot-assisted arm training after stroke improved only arm motor function and strength of the paretic arm, while activities daily living remained unchanged (40). When used in sub-acute stroke patients with moderate to severe gait impairment, robot-assisted training was not found to be as efficacious as traditional training (30,41). However, most of the cited studies involved small groups of patients, suggesting the need for caution in the clinical interpretation of their outcome results. The Lokomat has also been found to show limitations in later stages of rehabilitation. The movements required for functional walking depend on the interaction between perception and motor ability, as well as between the patient, the task assigned and the environment (42) and, unfortunately, the Lokomat, being unable to reproduce the variability of environments and movement patterns that characterizes daily living, cannot promote the necessary adaptation skills. Instead, the Lokomat, if used in early phases of a rehabilitation programme, can certainly rehearse mechanical patterns as a prerequisite for independent walking. However, although the introduction of the Lokomat in the training programme has led to improved walking outcomes compared with conventional training phases, review analysis data show that it cannot replace conventional physical therapy (33). Thus, on the basis of the current evidence, it seems that the Lokomat may serve as an adjunct in early phases of stroke in patients with limited walking. From these considerations there emerges the need for further larger studies, in order better to define the role of robot-assisted devices in stroke (29,43). Finally, recent research on the use of virtual reality systems in BWSTT in post-stroke patients deserves a mention (44,45). The results of these studies showed that gait and balance was improved more in these patients Functional Neurology 2009; 24(4):

4 R. Semprini et al. using these systems than in those undergoing the rehabilitation programme alone. The authors hypothesize that the virtual reality transforms walking or other movement into a goal-oriented task rather than a simple repetitive exercise, drawing the patients into the activity by engaging their minds. This makes the treatment a more rewarding activity improving motivation. Discussion Basic and clinical research has always provided medical practice and rehabilitation with the stimulus to achieve better results in the treatment of gait disturbances in neurological disorders (46). Attention has focused mainly on the intensity, frequency and repetitive nature of therapeutic exercise, even though more recently there has emerged the concept of rewarding rehabilitation, based on the exploitation of a virtual reality system and mental engagement. The construction of new devices (robots, exoskeletons, and other electrical systems) has facilitated gait recovery and also prompted further clinical trials and several scientific papers. Although critical analysis of the literature data on these devices has highlighted some limits, the available clinical data demonstrate, on the whole, that research is moving in the right direction. While studies in this field still show heterogeneity in score scale use, number of patients enrolled, type of pathology investigated, and degree of disability, there are nevertheless emerging new strategies and technologies designed to improve the efficacy and efficiency of rehabilitation, giving patients better results and reducing discomfort for therapists. From this perspective, assisted training emerges as a major challenge (46). Acknowledgements The authors are grateful to Prof. Roberto Gradini and Melanie Davis for technical support. References 11. 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