An intensive task-oriented circuit training positively impacts gait biomechanics in MS patients

1 Introduction

Multiple sclerosis (MS) is a demyelinating disease characterized by progressive clinical impairment, resulting in muscle weakness, sensory disturbances, spasticity, gait ataxia, visual deficits and cognitive impairment (Karussis et al. 2014). Disease progression has a variable course, finally leading to severe functional disabilities with an important impact on health, independence and quality of life (Compston et al. 2008). MS structural damage can impair a huge variety of subsystems involved in the collection and integration of sensory information towards the selection of appropriate motor responses (Heesen et al. 2008): slow ambulation, difficulty in response to postural adjustments and postural instability represent the subsequent dysfunctions (Cattaneo et al. 2014). Gait disturbances frequently appear along disease progression, and almost 85% of patients report ambulatory dysfunctions as their main complaint (Comber et al. 2017): reduced walking speed, step length, cadence, increased step width and stride variability and reduced dynamic excursion at all lower-extremity joints represent the most common features (Comber et al. 2017). Abnormal gait pattern, along with static and dynamic balance impairment (Peebles et al. 2018), contributes to reduce mobility and functional abilities and increases risk of falls (Giannì et al. 2014). Indeed, fall rates in this population is considerably high, with recent literature indicating that a percentage between 52% and 63% of patients will experience a fall in a 2–6 months period (Mazumder et al. 2015). Everyday life activity is the most frequent involved situation (Gunn et al. 2014), with almost 80% of falls occurring during postural transfers and 60% during gait tasks (Sosnoff et al. 2011). Then, the critical loop between postural instability, gait abnormalities, falls and risk of falls suggests that these are key factors to be addressed while prescribing training interventions.

As currently known, updated reviews and international guidelines recommend physical activity in MS people (Sà et al. 2014), stating its positive effects on cardiovascular fitness, fatigue, walking capacities and quality of life (Dettmers et al. 2009, Rampello et al. 2007). In fact, stating that ambulatory function is necessary for daily activity, promoting customized strategies addressing patients’ walking abilities may have significant clinical impact. The rehabilitation of gait disorders primarily involves aerobic exercise, resistance training and gait training to enhance gait efficiency and safety and to correct abnormal gait patterns. Gait training, such as conventional treadmill training, body weight-supported treadmill training or robotic-assisted treadmill training, has been used in MS with positive results on walking performance (Bethoux 2013). Recently, a two weeks high-intensity task-oriented rehabilitation training (TOCT) has revealed feasible and safe in MS people with moderate mobility impairments, with benefits on motor function, walking abilities and quality of life (Chisari et al. 2014).

On this panorama, despite the growing literature about rehabilitation in MS, only few studies focused on quantitatively assessing gait biomechanics changes induced by training interventions (Rodgers et al. 1999, Pau et al. 2017, Gutierrez et al. 2005). Recently, the most benefical effects of rehabilitation strategies were revealed on spatio-temporal parameters assessed with gait analysis (Pau et al. 2017, Guner et al. 2015), while kinematic evaluations evidenced improvement restricted to dynamic range of movement (ROM). Interestingly, Gutierrez et al. (2005) pointed out the normalization of stride parameters and symmetrisation of toe clearance between two lower limbs induced by a lower-limb resistance training. Anyway, to our knowledge, no one of the aforementioned studies focused on specific association between clinical assessment of neurological impairment and the effects of training interventions on ambulatory function in MS.

On this background, the aim of this study is to test the efficacy of a previously validated Task-Oriented Circuit Training (TOCT) on gait kinematics in MS patient with mild-moderate disability (Chisari et al. 2014). Since our previous investigations pointed out functional improvements during walking tests and increased quality of life, our hypothesis is that individuals with MS who underwent the TOCT program would exhibit positive modifications in gait biomechanics. Moreover, we evaluate if patients with a specific neurological impairment, assessed with clinical scores, could reveal specific gait improvements after our training intervention. In particular, we hypothesized that the characterization of gait modifications on the basis of patients’ clinical features may help physicians to plan rehabilitation needs and target treatment options.

2 Materials and methods

3 Results

3.2 Kinematic data

As regard knee biomechanics, we observed a statistically significant increase in angular excursion (45,63±8,9 at T0 vs 49,26±8,68 at T1) after rehabilitation treatment in the whole study sample (Fig. 1a, b). No significant difference was revealed in hip and ankle angular excursions after TOCT in the whole study sample (Fig. 1a, b).

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Fig. 1

Hip, Knee and Ankle ROM (a) and kinematics (b) before (T0) and after (T1) training in the all study sample. *Significant at p < 0.05.

When considering the two subgroups of subjects, we observed, after training, a statistically significant increase in knee dynamic excursion in Group 1 (43,27±10,34 at T0 vs 48,03±10,40 at T1) but not in Group 2 (48,87±5,43 at T0 vs 50,96±5,77) (Table 3). While, ROMs at all lower extremity joints did not significantly modify between Group 1 and Group 2 after (T1) training intervention (Table 4).

As regard sagittal plane kinematics, we found that at T1 Group 1 patients presented a peak ankle plantarflexion angle (PAPA_ES) in the early stance (PAPA_ES = –5,28±5,03 at T0 vs PAPA_ES = –1,66±5,3 at T1; p = 0.026) and a peak ankle dorsiflexion angle (PADA_TS) in terminal stance significantly higher (PADA_TS = 9,60±3,64 at T0 vs PADA_TS = 12,37±5,19 at T1, p = 0.008), (Table 5). As regard knee dynamics, we found a significant increase in peak knee flexion angle (PKFA) after TOCT training (PKFA = 53±12,40 at T0 vs PKFA = 58,81±10,45 at T1; p = 0.021). While, when considering Group 2 patients, sagittal plane kinematics revealed no significant changes in ankle, knee and hip biomechanics (Table 5, Fig. 2).

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Table 5

Ankle, knee and hip biomechanics in Group 1 and Group 2 before (T0) and after (T1) training intervention

Parameters	Group 1 TO	Group 1 T1	p	Group 2 TO	Group 2 T1	p
Ankle
PAPA_ES	–5,28±5,03	–1,66±5,3	0,026*	–1,18±2,98	0,65±5,49	0,77
PADA_TS	9,60±3,64	12,37±5,19	0,008*	14,17±3,14	13,68±5,21	0,77
PAPA_TO	–3,63±9,20	–2,50±8.38	0,11	7,67±9,21	2,60±6,49	0,12
PADA_S	1,93±3,99	2,80±6,08	0,65	7,73±4,33	5,54±6,12	0,57
Knee
PKEA	7,40±11,37	10,25±10,84	0,18	6,23±10,74	5,84±9,15	0,77
PKFA	53±12,40	58,81±10,45	0,021*	55,45±13,29	55,66±13,90	0,88
Hip
PHEA	2,07±8,78	2,90±7,61	0,72	0,82±11,38	–6,31±10,73	0,09
PHFA	38,56±8,78	39,84±8,74	0,72	38,27±12,44	32,78±9,61	0,09

Note. Values are mean±standard deviation (SD). Group 1, pyramidal positive patients; Group 2, cerebellar positive patients. Abbreviations: PAPA_ES, peak ankle plantarflexion angle in early stance; PADA_TS, peak ankle dorsiflexion angle in terminal stance; PAPA_TO, peak ankle plantarflexion angle at toe-off; PADA_S, peak ankle dorsiflexion angle in swing; PKEA, peak knee extension angle; PKFA, peak knee flexion angle; PHEA, peak hip extension angle; PHFA, peak hip flexion angle; ^*Significant at p < 0.05.

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Fig. 2

Hip, knee and ankle kinematics in Group 1 and Group 2 before (T0) and after (T1) training intervention. *Significant at p < 0.05.

Moreover, when comparing ankle kinematics in the two subgroups of participants, we found that peak ankle dorsiflexion angle in terminal stance (PADA_TS = 9,60±3,64 in Group 1 vs PADA_TS = 14,17±3,14 in Group 2; p = 0.01) and peak ankle dorsiflexion angle in the swing time (PADA_S = 1,93±3,99 in Group 1 vs PADA_S = 7,73±4,33 in Group 2; p = 0.01) were significantly lower in Group 1 before TOCT training (Fig. 3). While, after TOCT training, peak ankle dorsiflexion angle in terminal stance (PADA_TS = 12,37±5,19 in Group 1 vs PADA_TS = 13,68±5,21 in Group 2; p = 0.45) and peak ankle dorsiflexion angle in the swing time (PADA_S = 2,80±6,08 in Group 1 vs PADA_S = 5,54±6,12 in Group 2; p = 0.41) were not significantly different between the two subgroups of subjects (Fig. 3).

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Fig. 3

Sagittal plane ankle kinematics at two time intervals (T0 and T1) in the two subgroups of patients (Group 1 and Group 2). *Significant at p < 0.05.

The importance of addressing ambulatory function in people with MS is gaining interest, and different rehabilitative training programs have been proposed to improve motor performance and quality of life. Since our previous findings evidenced the efficacy of a gait specific training on functional abilities and health related quality of life in MS, we investigated gait characteristics changes induced by this rehabilitation treatment. In particular, we tested two main hypothesis: 1) motor improvement induced by the intervention may be associated to positive modifications in gait biomechanics; 2) patients with a specific neurological involvement, assessed with clinical scores, may reveal specific gait improvements after TOCT training intervention.

In the whole sample of patients, our findings confirmed the results reported in previous studies, i.e. decreased gait velocity, shorter steps, increased double limb support and step width and reduced dynamic excursion at all lower-extremity joints (Kabada et al. 1990, Severini et al. 2017).

As regard spatio-temporal parameters, we did not evidence any improvement in the whole study sample after rehabilitation intervention. Anyway, we found an increased walking velocity, reduced double limb support time and stance time duration in Group 2 compared to Group 1, after the two-week training period. As known, these parameters represent measures of walking stability: MS people usually increase double limb support time and stance duration time to compensate for fear of falling or postural instability (Sosnoff et al. 2012). Therefore, despite the fact that no relative improvement was evidenced in Group 2, we revealed that patients with prevalent cerebellar impairment displayed a less conservative gait strategy compared to patients with prevalent pyramidal impairment after training period.

The main findings of the present study are related to knee kinematics. In fact, we found that knee range of movement was significantly improved after the specific training approach in the whole study sample, moving its value towards normality parameters (Kabada et al. 1990). The novelty of our data is the fact that a two-week intensive program positively modified knee angular excursions in mild impaired MS subjects. It might be hypothesized that a combination of factors, such as treadmill training associated with repetitive task-specific goals in the TOCT program, contributed to changes in knee biomechanics. In fact, recently, it was discussed that treadmill training is capable of affecting the functional ROM of the lower limbs during walking in MS people and the gains in kinematics and kinetics of gait reflect improved functional abilities during motor performance (Peruzzi et al. 2017). In our study, task-specific repetitive exercises required the participants to a more coordinated and forceful moving, reaching higher degrees of joint excursions. From a rehabilitative point of view, previous studies pointed out the main effect of rehabilitation interventions occurring on spatio-temporal parameters recorded with Gait Analysis (Guner et al. 2015, Gutierrez et al. 2005). To our knowledge, only a short-term yoga program, comprehending an aerobic training on bicycle, induced a trend in improvement in dynamic range of movement of lower limb joints (Pau et al. 2017). In summary, our advice is that including a relevant amount of treadmill training, along with task-specific exercises in a rehabilitation intervention, may have clearly identifiable benefits on gait biomechanics in mild-moderate impaired MS people.

The second part of our study focused on identifying differences in ambulatory pattern induced by the specific training in two subgroups of patients, divided on the basis of clinical functional examination.

Interestingly, these data point out that patients with prevalent pyramidal impairment could gain more profit by the intensive task-specific training, presenting a better knee dynamic excursion, supported by an improved knee and ankle kinematics during normal walking. In particular, during early stance, we found a reduced plantarflexion at the beginning of single limb stance. Thus, this subgroup of patients exhibited a gait pattern with the foot landing on the ground in a less plantar-flexed position. Overall, this joint position could reduce the requirement of the ankle dorsiflexors to control the plantar flexion movement during early stance (Huisinga et al. 2013). While peak plantar flexion at toe-off did not change after the two-week training period, peak dorsiflexion angle during late stance increased after training period, so we might suppose that the angular distance traveled by the ankle was higher and the amount of torque generated could be increased. Consequently, knee biomechanics revealed an improved peak flexion during the swing time of gait cycle, which turned in increased knee dynamic excursion during normal walking. Of note, when comparing ankle biomechanics between two subgroups of subjects, we found greater peak ankle dorsiflexion angle during late stance and in the swing time of gait cycle in pyramidal positive subjects, thus supposing an improved toe-clearance.

These results may have important implications in the treatment approach of such patients. In the light to assist the decision making process on training intervention in MS, these findings suggest TOCT training as a treatment opportunity to improve gait kinematics and ambulatory pattern in MS patients with a prevalent pyramidal impairment. Indeed, the significant modifications in terms of knee and ankle kinematics represent clinically meaningful changes, stating current literature on minimum detectable differences of gait kinematics in MS population and healthy subjects (Andreopoulou et al. 2019, Bates et al. 2016). Therefore, these results point out the transferability of the training program to the ambulation function with potential benefits on clinical outcomes. As known, gait pattern in MS patients is affected by abnormal strategies for mechanical work generation to compensate neuromuscular impairments (Davies et al. 2016). In particular, the reduction of knee flexion pattern and ankle dorsiflexion in the swing phase of gait cycle represent two frequently altered dynamics in MS (Nogueira et al. 2013), exposing patients to increased risk of falling due to tripping or crossing obstacles (Cofrè et al. 2016). Indeed, abnormal foot kinematics, especially the lack of push-off power at the ankle, results in an inefficient knee flexion velocity and induce an increased energy cost leading to an inefficient gait pattern (Campanini et al. 2013). In this regard, gait analysis evaluation allow the identification of specific gait abnormalities in individual patients, and may help to plan goal-oriented physical therapy. Therefore, this kind of approach may help physicians to plan rehabilitation needs and target treatment options.

Some limitations of this study have to be acknowledged: first of all, the sample size may have played a role in limiting the significance of some of the statistical comparisons carried out. Of note, we carefully evaluated the possible presence of outliers, which are likely to affect statistical analyses when the number of patients is limited, and no evidence of outliers was found in our sample for quantitative data. Another limitation to consider is that recordings were made in a setting of short-medium dimensions. Probably, the inclusion of a fully comparable control group attending a conventional rehabilitative treatment could be useful in order to confirm that the obtained results are due to the specificity of our rehabilitative approach. Finally, future perspective will be to assess gait kinematics in a large cohort of patients with a longer follow-up in order to verify whether quantitative changes persist along time and to confirm the generalizability of such an approach.

5 Conclusions

In conclusion, results provide evidence that the intensive task-specific protocol can be an effective approach to positively modify lower limb kinematics in mild-moderate impaired MS patients. Moreover, kinematic data suggest TOCT training as a treatment opportunity to improve gait kinematics and ambulatory pattern in MS patients with a prevalent pyramidal impairment.

Authors’ contribution

CT performed patients’ recruitment, clinical evaluations and gait analysis procedure, contributed to data analysis, interpreted the results and drafted the manuscript; SDM contributed to clinical evaluations and gait analysis procedure; CC designed the study, was responsible for patients’ enrolment and clinical functional evaluations, contributed to analysis and interpretation of data and to manuscript supervision. The authors read and approved the final manuscript.

Conflict of interest

I declare that each author participated sufficiently in the work to take public responsibility for the content. I affirm that I had access to all data from the study, both what is reported and what is unreported, and also that I had complete freedom to direct its analysis and its reporting, without influence from sponsors. I also affirm that there was no editorial direction or censorship from the sponsors. No part of this work has been published. No conflict of interest exists.