A biofeedback cycling training to improve locomotion: a case series study based on gait pattern classification of 153 chronic stroke patients

Stroke is the leading cause of acquired adult disability [1, 2]. The most common and widely recognized deficit caused by stroke is motor impairment, which typically affects one side of the body, controlateral to the brain hemisphere where the lesion occurs. The ensuing hemiparesis foresees some degrees of motor recovery depending on the severity of the lesion and on the rehabilitative training [3]. Several studies have revealed that motor experience plays a major role in the subsequent physiological reorganization occurring in the intact tissues adjacent to the lesion [4, 5]. Clinical studies on central motor neuroplasticity support the role of goal-oriented, active, repetitive movements in the training of the paretic limb to enhance motor relearning and recovery [6–8].

The recovery of walking ability is considered the most important objective of the lower limb rehabilitation of individuals after stroke [9]. However, effective interventions for gait training are limited because extensive assistance is required for individuals with unstable balance, muscle weakness, and a persistent deficit in movement coordination.

In the last decade different studies suggested that significant improvements in the lower extremity function might result from using cycling as a rehabilitative method and that repetitive bilateral training provided by pedaling may have a positive effect on walking ability [10–13]. Cycling and walking share a similar kinematic pattern: both tasks are cyclical, require reciprocal flexion and extension movements of hip, knee, and ankle, and have an alternating activation of agonist/antagonist muscles in a well-timed and coordinated manner [14, 15]. Furthermore, cycling avoids problems of balance and can be safely performed even from a wheelchair, without requiring expensive robotic devices or the constant supervision of a therapist which are, on the contrary, necessary to support body weight and to prevent falls during gait training. For all these reasons, leg cycling training is a safer and more economic intervention to supplement functional ambulation training after stroke and it is also becoming an interesting option for home rehabilitation of hemiparetic patients.

Providing an online feedback about patients' performance to the training improves patients' motivation, allows the therapists to assess the exercise and may lead to an enhancement in the motor relearning process [16]. This rehabilitative method is well known with the term of biofeedback (BF) and consists of the use of instrumentation to make covert physiological processes more overt. BF refers to an artificial feedback on biological quantities, transferred to a biological system (human) [17]. The use of BF re-endows patients with sensorimotor impairments with the ability to assess physiological responses and possibly to relearn self-control of those responses [18]. Besides, continued training could establish new sensory engrams and help the patients to perform tasks without feedback [19]. To maximize the effect of BF it may be important to apply it within task-oriented activity and with a feedback mode that facilitates motor relearning [18]. During pedaling, visual BF methods were developed based on EMG activity [20] and power output produced during a treatment of cycling induced by electrical stimulation [21].

Because of the laterality of the motor impairment, the postural imbalance or asymmetrical movements between the two lower limbs are commonly observed in hemiparetic patients, making the recovery of a symmetrical involvement of the two legs strictly correlated with the improvement of overground locomotion [22, 23]. To minimize gait asymmetry could be clinically crucial since it may be associated with a number of negative consequences such as inefficiency, challenges to balance control, risks of musculoskeletal injury to the non-paretic lower limb and loss of bone density in the paretic lower limb [24]. During cycling, since the two legs are simultaneously acting on a single crank, not optimal solutions could be adopted by stroke patients: for example, the non- paretic leg can completely compensate for the paretic one [11], making the pedaling strategy effective in terms of speed and total power output, but strongly unbalanced. This solution could limit the possible benefits and even worsen the gait performance in terms of symmetry. To solve this problem, it could be useful to display a feedback that provides information about the forces produced at the pedals, asking patients to increase the task symmetry.

Commercial available cycle-ergometers are usually equipped with a torque sensor measuring the total torque provided by both legs at the crank, but this signal does not allow to distinguish the contribution provided by each leg during pedaling. To overcome this limitation, in our laboratory a cycle-ergometer was instrumented by mounting strain gauges on each crank arm to measure independently the torque produced by each leg during pedaling [25]. Starting from this setup, an information fusion algorithm was implemented in order to visually display to the patient an intuitive index strictly correlated with the symmetrical involvement of the two legs in terms of torques provided at the crank arms during pedaling. The aim of the present study was to develop a BF controller and to evaluate its feasibility and clinical efficacy as a rehabilitation treatment for chronic stroke patients. The hypothesis was that a 2-week BF cycling treatment might induce some improvements not only in the pedaling performance but also in the walking ability both in terms of gait speed and symmetry indices. A case series study was designed and participants were recruited based on a gait pattern classification of a population of 153 chronic stroke patients. In particular, subjects representative of each category were included in the study in order to identify those patients who can benefits the most from the proposed treatment.

The present work investigated the feasibility and utility of a biofeedback cycling treatment and its effects on cycling unbalance and walking parameters in three case studies of chronic stroke patients. After having performed a gait pattern categorization of a population of 153 chronic stroke patients, three participants, each of them representative of one of the clusters in which the population resulted to be divided, were enrolled in the study: S1 presented a slow and almost symmetric gait; S2, the most impaired one, was characterized by a very asymmetrical and slow gait; S3 showed the strongest and fastest gait, but still exhibited gait asymmetry due to an overuse of the healthy limb. In our experimental approach we tried to keep to the key ingredients for motor functional recovery providing an intensive and repetitive task training able to maintain a high active involvement of the patients during the intervention [18]. Furthermore, to maximize patients' involvement we increased the task difficulty as participants' skill improved.

The results obtained by the three patients emphasized the importance of developing biofeedback treatment approaches that are effective in maximizing underlying mechanisms responsible for neurological and adaptive recovery in individuals with hemiparesis, even in chronic state. The chosen visual feedback resulted simple to be understood by patients. Indeed, as shown in Figure 4, all patients improved their performance obtained during the biofeedback phase.

The most appealing questions for the proposed treatment are whether the effects obtained during the BF phase can be maintained also when the exercise is performed without the visual BF and most of all whether the effects obtained on cycling symmetry can be translated to the walking performance. To reply to the first question, it can be noticed that in the post-treatment assessments all patients significantly reduced their pedaling unbalance with respect to baseline (Table 3). Concerning the second question, the treatment, even short, seems to produce some modifications on the gait kinematic pattern in two of the three chronic patients.

The most significant improvement was obtained by S2, the patient who strengthened the most the paretic side (he doubled W_PL after training, see Table 3). This subject was characterized by a very slow and asymmetrical gait at baseline (mean velocity = 0.32 m/s; ST ratio = 0.57 ± 0.05; SV ratio 0.53 ± 0.14). After treatment he doubled the swing velocity of the paretic leg, meaning that the patient started to produce the inertia to generate the step also with the paretic leg and started to translate this inertia in distal propulsive force improving the kinetic both at the foot and knee (results not shown). This result is confirmed by a significant improvement of gait symmetry that was also maintained (SV ratio) or further increased (ST ratio) at follow-up. In the post-treatment assessment, S2 obtained also a significant increase of the mean gait speed that is a crucial functional indicator of an improved walking ability [30]. The self-selected speed of S2 increased of the 67% with respect to baseline changing from 0.32 m/s to 0.51 m/s; this increase can be recognized as enough to change from a category of a household walker to a full community walker, and thus it can indicate a potential improvement in the quality of life following the proposed treatment [31].

The progress on walking velocity was preserved at follow-up even if at lower levels, implying that a 2-week treatment was probably not enough to induce permanent changes in the walking ability of S2.

The biofeedback cycling treatment produced some benefits also in the gait pattern of S3. He obtained a significant change in the alternation of stance and swing phases of the healthy limb, thus reducing the compensation strategy used during walking. This behavior was exactly the same he adopted also to reduce unbalance during cycling; indeed, he significantly reduced the work produced by the healthy limb. For this patient, the improvements induced by the treatment were maintained one week after the end of the intervention. The significant benefits obtained in pedaling unbalance were not translated in a significant improvement in gait symmetry even if a slight increase of both SV and ST ratio were obtained after treatment (see S3 results in Table 4).

Finally, S1 did not change her gait pattern after only 2 weeks of treatment and maintained her slow but safe and almost symmetrical gait mostly due to a general hypotonia. Thus, our hypothesis that such a BF treatment could induce a general strengthen in S1 resulting in an increase of her gait speed was not valid. Our preliminary results seem to suggest that the proposed treatment was not useful for a patient characterized by gait symmetry parameters included in the normality ranges before treatment.

The main limitation of this study is that all the presented results need to be substantiated by testing on a larger number of patients. Furthermore, the results seem to suggest that the small number of sessions administered (n = 6) is not enough to have a clear idea about the training potentiality in producing the carry-over effect from pedaling to overground locomotion. In addition, our follow-up assessment, very close to the end of the treatment, is not representative of a long term effect of training but gives only a first indication about the maintenance of the induced motor recovery. At last, our study is limited to a population of chronic stroke patients with mild spasticity (Modified Ashworth Scale ≤ 2) and this does not cover the whole stroke population [32].

The results of this study suggest that a treatment of only 6 days is able to produce improvements in terms of pedaling unbalance and, sometimes, also in terms of walking ability, but probably a more prolonged treatment would be more effective in translating progresses from pedaling performance into locomotor capability and in maintaining the results over time. Naturally, the duration of the treatment has to be optimized depending on the specific patients' condition in strict collaboration with physicians. This study tries also to give some suggestions about how to choose patients' categories which can avail themselves of the treatment. The treatment seems to be beneficial for people with a very asymmetrical and inefficient gait such as S2 and for people that make an overuse of the healthy leg to compensate for their asymmetry, like S3.

Certainly a more robust statistical study (e.g. randomized controlled trial) is required to provide a clear evidence that a pedaling treatment with visual biofeedback significantly improves walking ability in chronic stroke patients. To validate a carry-over effect from pedaling to overground locomotion, a more prolonged treatment (e.g. a 4-week intervention) will be tested on a targeted category of individuals with stroke, i.e., patients included in the initial cluster of S2, that are characterized by a very asymmetrical and slow gait. If the effect is demonstrated on a larger and controlled scale, the proposed intervention, thanks to its safety and low price, could really have an impact also as a home-rehabilitation treatment for chronic stroke patients.