Background
Scaling and timing internal control required for automatic and rhythmical movements are impaired and archetypally linked to the basal ganglia dysfunction in Parkinson’s disease (PD). As a result of such impairment, a reduced gait speed, shorter stride length, reduced arm swing and a random walking pattern (i.e. increased gait variability) are typical features of PD gait [
1‐
5]. From the specific temporal point of view, the inability to produce a steady gait rhythm, which result in more random stride-to-stride variability, is one of the primary temporal gait disorders and can indicate a sensitive marker of a higher fall risk in PD [
5,
6].
Interestingly, the randomness of PD gait was recently emphasized by subtle deterioration of the temporal organization of gait variability, using the long-range autocorrelations (LRA) assessment [
6]. In addition, close correlations with disease severity and balance status were demonstrated in PD [
6]. In a more theoretical framework, LRA have indeed been suggested as an indicator of adaptive abilities characterizing healthy systems [
5,
7‐
9]. As a corollary, deviations from an optimal level of variability in either the direction of randomness or the over-regularity are thought to reflect the loss of the adaptive capabilities of the system [
8].
Consequently, interventions that improve LRA might be beneficial in PD gait, which is characterized by less efficient adaptive resources. Among numerous rehabilitative approaches, Nordic Walking (NW) holds a special place in PD as an emerging and promising strategy to stimulate an active lifestyle [
10]. Using specially designed poles, NW involves an intentional coordination between upper and lower limbs and could constitute an interesting option to enhance the stride length and the gait speed [
11‐
13]. Furthermore, the use of Nordic poles may act as an external cue, triggering intact circuits and bypassing the defective basal ganglia—SMA loop. This permits compensating for the impaired scaling and timing control in PD [
12].
However, it remains unknown whether Nordic Walking, without any long-term training, can influence real-time spatial and temporal gait variables in Parkinson’s disease, and especially long-range autocorrelations. Therefore, this study is aimed primarily at assessing LRA, as well as spatiotemporal gait variables, by means of comparison between NW and Usual Walking (UW) in PD. Considering NW may act as an external cue to restore control movement [
12], our primary hypothesis is that gait variability would become less random and spatiotemporal gait variables would improve with such a rehabilitative approach. Secondarily, the study is aimed at comparing long-range autocorrelations and gait variables in the PD population to healthy adults while usual and Nordic walking.
Discussion
In this study, we aimed to gain more insight into the immediate effect of Nordic walking on the temporal organization of gait variability (i.e. LRA) as well as on spatiotemporal gait variables in PD participants. Actively involving rhythmic movements of the upper body, Nordic walking (NW) leads to significant improvement of LRA compared to the more random gait pattern highlighted during the usual walking session (UW). Additionally, NW enhances step length without any change in gait speed. Interestingly, LRA and step length collected from the NW session are similar to that of the healthy population. Those findings strongly support resorting to the use of Nordic poles in the struggle against the randomness of PD gait and the typical gait hypokinesia.
The randomness of PD gait pattern on UW contrasts with the structured gait pattern of age-matched healthy adults. Indeed, stride duration variability on UW appears less structured in PD (i.e. lower LRA exponent values). LRA, highlighted in gait and other rhythmic physiological signals, are thought of as the signature of subtle and complex interactions between subcomponents constituting dynamical systems [
9,
32]. Locomotor systems ranks among those systems that need to continuously adapt their pattern to constraints imposed by daily living activities [
8]. The randomness of PD gait pattern could thus result from the defective activity among interacting subcomponents (e.g. basal ganglia). Furthermore, the breakdown of LRA highlighted in the specific context of basal ganglia disorders (e.g. Parkinson’s and Huntington’s diseases) was strongly associated with balance and functional status, and was suggested as a quantitative clinical measure of dynamic instability [
6,
33].
Compensating or restoring interactions among multiple components involved in healthy gait pattern is a key factor in restoring adaptability and flexibility of locomotion. Interestingly, NW can modulate some temporal organization in PD gait pattern (Fig.
3). LRA exponents were indeed significantly higher with Nordic poles than with usual walking in PD participants and similar to that of the healthy population, characterized by functional and adaptive locomotion (Tables
2 and
3 and Figs.
2 and
3). The use of Nordic poles allows a more temporally organized behaviour than with UW, which suggest a more effective and powerful coordination of sub-components constituting the locomotor system [
8,
9,
32].
Note that the α exponent seemed to decrease between the two walking conditions in healthy adults (Table
2). However, the exponent value remained at a “healthy” level (Mean α exponent ± SD: 0.56 ± 0.17) [
34]. In addition, such eventual decrease of LRA should be considered within the integrated approach applied in our study. While the effect size is small (Cohen’s d = 0.21) and non-statistically significant (
p = 0.453) for the α exponent in healthy population, no effect size was demonstrated for the Hurst exponent (Cohen’s d = 0.12;
p = 0.562). On the other hand, the increase of α exponent is large and highly significant (Cohen’s d = 1.07;
p < 0.001) in PD participants and evolves in the same way that H exponent (Cohen’s d = 1.05;
p < 0.001). Therefore, the use of Nordic poles is beneficial for the PD walking pattern whereas it does not affect the walking pattern of healthy population.
Modulation of spatio-temporal gait parameters also seems different for people with PD walking with and without the Nordic poles (Tables
2 and
3 and Fig.
5). Although the gait speed in UW and in NW remained slower than in healthy adults, the overall modulation of spatio-temporal gait parameters with the Nordic poles was similar to healthy adults. While the reduced gait speed during UW was largely attributed to hypokinesia (significant reduction of step length), the gait speed in NW is modulated by both a significant improvement in step length and a reduction in gait cadence, which is particularly interesting in PD gait disorders management. Although the reduction of gait cadence could be perceived as dramatic, it should be noted that such decrease is usually observed with attentional strategies that specifically focus on step length criterion [
28,
35].
Decreased gait speed in PD is indeed largely attributed to difficulties in generating appropriate stride length while cadence control, used as a compensatory mechanism, remains intact [
1‐
4]. However, Morris et al. demonstrated that the ability to generate a normal stepping pattern is not lost in PD [
2]. Normal movement amplitude could be indeed elicited in PD given the appropriate conditions such as the use of attentional resources or external cues [
2,
28]. Both strategies appear to share the same mechanism of focusing attention on the stride length criterion [
2].
Attention involvement in gait control on NW could be highlighted by a higher magnitude of gait variability (i.e. CV of stride duration variability; Fig.
4), as recently suggested by Ayoubi et al. in their meta-analysis [
25]. Attentional strategies are indeed often used to compensate for the impaired automaticity and could be involved in NW [
2,
36]. People with PD need to continuously think about their movement, sequencing the whole movement into sub-movement and the use of the frontal cortex facilitates movement size and timing regulation [
36]. During NW, both PD and healthy participants were implicitly focused on walking and their attention was directed to the desired movement patterns [
12]. The higher magnitude of the stride duration variability observed in all participants could be the signature of the attention involved in the task being performed, which could be observed with novice participants [
37]. In addition, walking with Nordic poles involves the intentional action to move upper limbs in a coordinated fashion with legs, improving the movement of the most affected side in PD.
Therefore, NW appears to be an interesting rehabilitative option as arm swing is reduced in PD [
38]. Recent studies agree wholeheartedly with the usefulness of arm swing on the stability of gait, especially in the elderly [
38,
39]. Moreover, gait seems to be more stable when the arm swing is amplified and could normalize the gait speed and the step length in this population [
38]. As already highlighted by Punt et al., this finding is important as the fall risk is already high for the elderly, and even more so in PD [
39,
40]. From this point of view, including arm swing in rehabilitation programmes, it seems to be an interesting strategy to normalize the PD gait pattern [
38,
41]. In particular, it has been suggested that normalizing coordination between limbs could improve gait in people with PD [
38].
Arm swing is integrated into locomotion via tight neuronal interlimb coordination using specialized neural circuits in the spinal cord (central pattern generators, CPGs) [
42]. Although such neuronal networks are able to produce coordinated motor patterns independently, the CPG output can be modulated by afferent feedback (i.e. cutaneous, joint and muscle input) and/or supraspinal input (i.e. cortical control) [
41‐
45]. Interestingly, it has been demonstrated that cutaneous stimulation of the hand evoked significant changes in lower limb kinematics in healthy adults, with an increase in dorsiflexion at the stance-swing transition [
46].
In addition, to help focus attention on walking, the use of Nordic poles could also act as an external sensory cue providing the necessary trigger in PD to bypass the defective pallidocortical circuit [
12]. Among multiple cueing modalities, auditory and visual cues are the most studied [
47,
48]. However, tactile and proprioceptive cues have also demonstrated their usefulness in the struggle against the impaired gait automaticity, despite suggestions of impaired somatosensory function in PD [
3].
From a biomechanical point of view, the use of Nordic poles implies a mechanically different movement pattern than UW [
49‐
51]. By increasing the base of support, the use of poles helps to preserve gait stability after an unpredictable perturbation [
52]. Nordic poles could serve as walking aids that are commonly prescribed to maintain balance in people with PD. However, the propulsive use of poles could reduce any alteration of the gait pattern classically observed with usual walking aids [
49,
53,
54]. Also, higher impulse values and higher knee and ankle moments in the sagittal plane compared to UW could indicate a more dynamic movement in NW [
50,
51].
Although the use of Nordic poles seems to be effective in PD, our results should be carefully extended to the whole disease severity spectrum. As recently highlighted, people with PD with only slight and mild gait impairment benefit most from NW [
55]. The coordination between limbs during gait seems to be compromised of both bradykinesia and rigidity, which increase with the pathological progression, while the adaptive abilities of arm-leg coordination is preserved in people with PD in the early stage of the disease [
56]. Also, people with PD often resort to cognitive strategies to compensate for a lack of gait automacity [
57]. However, such compensatory strategies are useful as long as the cognitive resources are preserved [
11,
57]. The attentional involvement on gait induced by the use of Nordic poles could, as a result, be thus compromised in people with PD in the latest stages of the disease.
Some limitations of this study should be addressed. Motor complications, such as freezing of gait or dyskinesia, could alter the gait dynamics. However, only two patients suffered from such complications (one from freezing of gait and one from dyskinesia of the upper limb) and none of them presented such complications during the walking trial. Also, note that participants were probably the most motivated since they already participated in a previous study. Thus, our results should be interpreted in light of this specific aspect. To better characterize the gait rhythmicity, ankle accelerometry was preferred to other locations since a significant degree of attenuation of the heel strike transient occurs during the passage to the head [
58]. Acceleration peaks are indeed higher and straighter in ankles than the trunk, or even more the head, which could improve the peak detection method by minimizing false-acceleration peak detection. Hence, the results concern the temporal organization of stride duration variability measured from accelerations of the ankles and comparisons with other studies should take into account that other studies extract gait variability from different devices (foot switches [
5,
22], inertial sensors [
59], accelerometer [
34], force platforms [
60], optoelectric system [
61]) and other body parts (trunk [
17], knee [
61], ankle [
34]) to assess LRA.
While several clinical trials were recently conducted to study the influence of NW on both motor and non-motor symptoms in PD [
10‐
12], none assessed the beneficial effects of NW program on LRA, as a gait stability index. This study can constitute a pilot study offering new perspective to better characterize the sensitivity of the temporal organization of gait variability to rehabilitation approaches. Thus, it would be interesting to investigate the effectiveness of a tailored NW program on gait stability, concurrently assessed with clinical balance measures in a randomized control clinical trial.