Alberto Ranavolo

Gait pattern in inherited cerebellar ataxias

Our aim was to perform a comprehensive analysis of the global and segmental features of gait in patients with genetically confirmed inherited ataxias. Sixteen patients with autosomal dominant (spinocerebellar ataxia, SCA1 or 2) or recessive (Friedreich’s ataxia, FRDA) ataxia were studied. We used a motion analysis system to record gait kinematic and kinetic data. We measured the mean values of global (time–distance parameters, COM displacement, support moment) and segmental gait parameters (joint displacement and inter-joint coordination), as both discrete and continuous variables, and their variability and correlations with International Cooperative Ataxia Rating Scale (ICARS) scores. We found a marked difference in all global gait parameters between the ataxic patients and the controls and close correlations between longer stride and stance duration and lower gait, posture and total ICARS scores. The only difference between the two patient groups was a shorter step length in the FRDA patients. As regards the segmental features, we found a significantly different waveform shape for all continuous kinematic and kinetic measures between the ataxic patients and the healthy controls, but only minor differences for the discrete measures. Intersegmental coordination evaluated using the continuous relative phase method revealed an irregular alternating joint behaviour without clear evidence of the synchronous pattern of alternating proximal/distal joint seen in healthy subjects. For almost all gait parameters we observed a markedly higher intra-subject variability in the ataxic patients versus the controls, which was strongly related to the clinical ICARS scores. Patients with chronic, progressive inherited ataxias lose the ability to “stabilize” a walking pattern that can be repeated over time. The most peculiar aspect of the gait of inherited ataxia patients, regardless the different genetic forms, seems to be the presence of increased variability of all global and segmental parameters rather than an invariant abnormal gait pattern.

Locomotor patterns in cerebellar ataxia

Several studies have demonstrated how cerebellar ataxia (CA) affects gait, resulting in deficits in multijoint coordination and stability. Nevertheless, how lesions of cerebellum influence the locomotor muscle pattern generation is still unclear. To better understand the effects of CA on locomotor output, here we investigated the idiosyncratic features of the spatiotemporal structure of leg muscle activity and impairments in the biomechanics of CA gait. To this end, we recorded the electromyographic (EMG) activity of 12 unilateral lower limb muscles and analyzed kinematic and kinetic parameters of 19 ataxic patients and 20 age-matched healthy subjects during overground walking. Neuromuscular control of gait in CA was characterized by a considerable widening of EMG bursts and significant temporal shifts in the center of activity due to overall enhanced muscle activation between late swing and mid-stance. Patients also demonstrated significant changes in the intersegmental coordination, an abnormal transient in the vertical ground reaction force and instability of limb loading at heel strike. The observed abnormalities in EMG patterns and foot loading correlated with the severity of pathology [International Cooperative Ataxia Rating Scale (ICARS), a clinical ataxia scale] and the changes in the biomechanical output. The findings provide new insights into the physiological role of cerebellum in optimizing the duration of muscle activity bursts and the control of appropriate foot loading during locomotion.

Neuromuscular adjustments of gait associated with unstable conditions.

A compact description of coordinated muscle activity is provided by the factorization of electromyographic (EMG) signals. With the use of this approach, it has consistently been shown that multimuscle activity during human locomotion can be accounted for by four to five modules, each one comprised of a basic pattern timed at a different phase of gait cycle and the weighting coefficients of synergistic muscle activations. These modules are flexible, in so far as the timing of patterns and the amplitude of weightings can change as a function of gait speed and mode. Here we consider the adjustments of the locomotor modules related to unstable walking conditions. We compared three different conditions, i.e., locomotion of healthy subjects on slippery ground (SL) and on narrow beam (NB) and of cerebellar ataxic (CA) patients on normal ground. Motor modules were computed from the EMG signals of 12 muscles of the right lower limb using non-negative matrix factorization. The unstable gait of SL, NB, and CA showed significant changes compared with controls in the stride length, stride width, range of angular motion, and trunk oscillations. In most subjects of all three unstable conditions, >70% of the overall variation of EMG waveforms was accounted for by four modules that were characterized by a widening of muscle activity patterns. This suggests that the nervous system adopts the strategy of prolonging the duration of basic muscle activity patterns to cope with unstable conditions resulting from either slippery ground, reduced support surface, or pathology.

Lower Limb Antagonist Muscle Co-Activation and its Relationship with Gait Parameters in Cerebellar Ataxia

Increased antagonist muscle co-activation, seen in motor-impaired individuals, is an attempt by the neuromuscular system to provide mechanical stability by stiffening joints. The aim of this study was to investigate the co-activation pattern of the antagonist muscles of the ankle and knee joints during walking in patients with cerebellar ataxia, a neurological disease that strongly affects stability. Kinematic and electromyographic parameters of gait were recorded in 17 patients and 17 controls. Ankle and knee antagonist muscle co-activation indexes were measured throughout the gait cycle and during the sub-phases of gait. The indexes of ataxic patients were compared with those of controls and correlated with clinical and gait variables. Patients showed increased co-activity indexes of both ankle and knee muscles during the gait cycle as well as during the gait sub-phases. Both knee and ankle muscle co-activation indexes were positively correlated with disease severity, while ankle muscle co-activation was also positively correlated with stance and swing duration variability. Significant negative correlations were observed between the number of self-reported falls per year and knee muscle co-activation. The increased co-activation observed in these cerebellar ataxia patients may represent a compensatory strategy serving to reduce gait instability. Indeed, this mechanism allows patients to reduce the occurrence of falls. The need for this strategy, which results in excessive muscle co-contraction, increased metabolic costs and cartilage degeneration processes, could conceivably be overcome through the use of supportive braces specially designed to provide greater joint stability.

Four‐week trunk‐specific rehabilitation treatment improves lateral trunk flexion in Parkinson's disease

People with Parkinsons disease (PD) often have a posture characterized by lateral trunk flexion poorly responsive to antiparkinsonian drugs. To examine the effects of a rehabilitation programme (daily individual 90‐minute‐sessions, 5‐days‐a‐week for 4‐consecutive weeks) on lateral trunk flexion and mobility, 22 PD patients with mild to severe lateral trunk flexion, and 22 PD patients without trunk flexion were studied. Patients were evaluated using the Unified Parkinsons Disease Rating Scale motor subscale (UPDRS‐III) score, and the kinematic behavior of the trunk was recorded by means of an optoelectronic system to determine: a) trunk flexion, inclination and rotation values in the erect standing posture; b) ranges of trunk flexion and inclination during trunk movements. After the treatment, significant decreases in trunk flexion [24°(4) vs. 14°(3), P < 0.001] and inclination in the static condition [23°(5) vs. 12°(4), P < 0.001)] were observed, both of which were maintained at the 6‐month follow up. During the trunk flexion task, a significantly increased range of trunk flexion [64°(15) vs. 83°(15), P < 0.001] was observed; similarly, during the lateral bending task, the range of trunk inclination was found to be significantly increased, both toward the side of the trunk deviation [29°(8) vs. 42°(13), P < 0.01] and toward the contralateral side [14°(6) vs 29°(11), P < 0.01]. No further significant changes were observed at the 6‐month follow‐up. Trunk flexion and inclination values in the upright standing posture correlated slightly with the UPDRS‐III score. Our findings show that significant improvements in axial posture and trunk mobility can be obtained through the 4‐week rehabilitation programme described, with a parallel improvement in clinical status.

Kinematic and Electromyographic Study of the Nociceptive Withdrawal Reflex in the Upper Limbs during Rest and Movement

This study set out to evaluate nociceptive withdrawal reflex (NWR) excitability and the corresponding mechanical response in the upper limbs during rest and movement. We used a three-dimensional motion analysis system and a surface EMG system to record, in 10 healthy subjects, the NWR in eight upper limb muscles and the corresponding mechanical response in two experimental conditions: rest and movement (reaching for, picking up, and moving a cylinder). The NWR was elicited through stimulation of the index finger with trains of pulses delivered at multiples of the pain threshold (PT). We correlated movement types (reach-to-grasp, grasp-and-lift), movement phases (acceleration, deceleration), and muscle activity types (shortening, lengthening, isometric) with the presence/absence of the NWR (reflex-muscle pattern), with NWR size values, and with the mechanical responses. At rest, when the stimulus was delivered at 4× PT, the NWR was present, in all muscles, in >90% of trials, and the mechanical response consisted of wrist adduction, elbow flexion, and shoulder anteflexion. At this stimulus intensity, during movement, the reflex-muscle pattern, reflex size, and mechanical responses were closely modulated by movement type and phase and by muscle activity type. We did not find, during movement, significant correlations with the level of EMG background activity. Our findings suggest that a complex functional adaptation of the spinal cord plays a role in modulating the NWR in the transition from rest to movement and during voluntary arm movement freely performed in three-dimensional space. Study of the upper limb NWR may provide a window onto the spinal neural control mechanisms operating during movement.

Turning strategies in patients with cerebellar ataxia

Turning while walking is a common but demanding task requiring modification of the motor program from linear walking to lateral turning and it is associated with a high risk of falls. Patients with cerebellar ataxia have unstable gait and report a high incidence of falls. In the present study, we investigated the motor strategies adopted by ataxic patients when performing turns of different degrees and directions of rotation. Ten ataxic patients and 10 controls were analyzed while performing 30°/90° turns to the right/left. We recorded the number of completed turn tasks, the number of steps needed, and the time taken to complete the task, time–distance parameters and the onset of head, trunk and pelvis reorientation. The ataxic patients were less able to complete 90° turns, displayed a greater stride width, shorter step length, and greater number of steps when turning, and were unable to flexibly adjust their stride width across the turning task. The duration of the turning task and of the segmental reorientation did not differ from control values. Our findings indicate that ataxic patients have more difficulties in performing large turns and adopt a series of compensatory strategy aimed at reducing the instability associated with turning, such as enlarge the base of support, shorten the step length, increase the number of steps, and use the “multi-step” rather than the “spin-turn” strategy. Given the high risk of falls related to this task, it would be useful to include turning training in the rehabilitation protocol of ataxic patients.

Lower-limb joint coordination pattern in obese subjects

The coordinative pattern is an important feature of locomotion that has been studied in a number of pathologies. It has been observed that adaptive changes in coordination patterns are due to both external and internal constraints. Obesity is characterized by the presence of excess mass at pelvis and lower-limb areas, causing mechanical constraints that central nervous system could manage modifying the physiological interjoint coupling relationships. Since an altered coordination pattern may induce joint diseases and falls risk, the aim of this study was to analyze whether and how coordination during walking is affected by obesity. We evaluated interjoint coordination during walking in 25 obese subjects as well as in a control group. The time-distance parameters and joint kinematics were also measured. When compared with the control group, obese people displayed a substantial similarity in joint kinematic parameters and some differences in the time-distance and in the coupling parameters. Obese subjects revealed higher values in stride-to-stride intrasubjects variability in interjoint coupling parameters, whereas the coordinative mean pattern was unaltered. The increased variability in the coupling parameters is associated with an increased risk of falls and thus should be taken into account when designing treatments aimed at restoring a normal locomotion pattern.

Strategies adopted by cerebellar ataxia patients to perform U-turns.

Cerebellar ataxia is associated with unsteady, stumbling gait, and affected patients report a high rate of falls, particularly during locomotor tasks. U-turns (180° turns while walking) require a high level of coordination in order to completely reverse the body trajectory during ongoing motion, and they are particularly challenging for patients with cerebellar ataxia. The aim of this study was to investigate the kinematic strategies adopted by ataxic patients when performing U-turns. Nine ataxic patients and ten controls were analysed as they performed 180° turns to the right while walking. We evaluated the following aspects: centre of mass velocity, body rotation, number of steps needed to complete the task, step length and step width, lower limb joint kinematics and segmental reorientation. Compared with controls, the ataxic patients showed slower deceleration and re-acceleration of the body, needed more steps to complete the U-turn, showed markedly reduced step length and were unable to modulate step width between steps. Furthermore, the patients adopted an extended joint rather than a flexed joint turning strategy, and the degree of knee flexion was found to be negatively correlated with the number of falls. Ataxic patients show an abnormal U-turn in comparison to age-matched healthy subjects. Some of the observed alterations are indicative of a primary deficit in limb-joint coordination, whereas others suggest that patients choose a compensatory strategy aimed at reducing the instability.

Planned Gait Termination in Cerebellar Ataxias

This study set out to characterise the pattern of planned gait termination in a sample of patients with cerebellar diseases. The gait termination phase was recorded, using a motion analysis system, in ten patients with primary degenerative cerebellar disease and in ten controls. The subjects were instructed to walk at different gait speeds and to stop in response to an acoustic signal. Time–distance parameters (step length, step width, double support duration, time-to-slow, stopping time, centre of mass velocity and number of steps) and stability index-related parameters (distance between the “extrapolated centre of mass” (XCoM) and centre of pressure (CoP)) were measured at both matched and self-selected gait speeds. At matched speed the patients, compared with the controls, showed a reduced step length, a greater first and second step width and used more steps to stop. At self-selected speed, almost all the parameters differed from those of the controls. Furthermore, the patients showed an increased stability index, suggesting that they need to maintain a “safety margin” between the XCoM and CoP during the gait termination. Patients develop a series of compensatory strategies in order to preserve balance during planned gait termination, e.g. increasing their step width and number of steps. Ataxic patients need to maintain a safety margin in order to avoid instability when stopping. Given the potential risk of falls when stopping, walking ataxic patients may benefit from a rehabilitation treatment focused on preserving and improving their ability to terminate gait safely.