Initiating walking from quiet standing is a seemingly simple, yet complex, task that requires generation of momentum while simultaneously maintaining postural stability. This delicate balance is achieved in part by anticipatory postural adjustments (APA). During quiet stance, the location of the whole body’s center of mass (COM) and the ground reaction force’s (GRF) center of pressure (COP) are coupled; oscillating about each other in the transverse plane to maintain postural stability (35). During gait initiation (GI), however, the APA purposefully uncouple the movement of the COM and COP. Before any appreciable movement of the COM, the COP is shifted posterior and lateral toward the initial stepping limb (swing limb). Whereas the backward movements of the COP result from the bilateral deactivation of the triceps surae musculature coupled with activation of the tibialis anterior, the lateral COP movement is achieved by hip abductor activation and stance limb knee flexion (23). This COP shift increases the components of the GRF anteriorly and toward the support limb (stance limb) leading to the generation of momentum in those directions (5). Thus, the APAs generate the initial momentum needed to begin walking, whereas the COM remains within the base of support (28).
Alterations in APA are considered a major pathophysiological mechanism underlying dysfunctional GI performance in persons with Parkinson’s disease (PD) (22,30,31). Previous studies suggested that the APAs are abnormally prolonged and reduced in amplitude compared with age-matched control subjects (16,17). This pattern of behavior is associated with increased movement preparation time (24,25,30), reduced swing limb loading (14), and less effective uncoupling of the COP and COM (16,22). Further, there are multiple abnormalities associated with the first step in individuals with PD including reduced propulsive forces (10,14), reduced step length and velocity, and less forward movement of the COM during single-limb support of the stance limb (6,16,21).
Although both the postural and stepping components are improved by antiparkinsonian medication (7,30), even when optimally medicated, GI performance remains impaired relative to age-matched controls (6,17,22,30). Thus, alternative interventions, such as rehabilitative therapy, play an important role in treating postural instability and gait dysfunction in this population. Unfortunately, external cueing and exercise have been shown to enhance only certain aspects of GI performance (7,11,15). Recently, robotic assistance given at the onset of the GI APA was shown to reduce APA duration and produce an earlier step onset and a faster first step (25). Further, a single session of robotic-assisted training provided some therapeutic improvement in APA duration and step onset time (24). Although promising, these interventions require external input. One intrinsic strategy that may influence GI behavior is altering the initial stance condition. Rocchi et al. (30) have shown that GI performed from a wide stance width was associated with larger COP displacements in groups of participants with and without PD. However, despite the ability to amplify the APA with stance width, individuals with PD had more difficulty initiating from the wide stance. To our knowledge, little is known regarding the influence of manipulating the anteroposterior aspects of the initial stance position.
In this current study, we evaluated the influence of foot positioning on GI by manipulating the position of the swing limb (Fig. 1). We hypothesized that a posterior translated swing foot would improve APA and stepping characteristics because the backward translated foot creates lower extremity alignments that more closely match ongoing gait, namely, an elongated base of support requiring greater force production to accelerate the COM.
Twelve persons with idiopathic PD, 12 age-matched healthy older adults (HOA), and 12 healthy young adults (HYA) participated (Table 1). Inclusion criteria for the individuals with PD included diagnosis of idiopathic PD by a movement disorders neurologist, a modified Hoehn and Yahr stage of II or III, and a score of ≥1 on Unified Parkinson’s Disease Rating Scale questions 14 and 29. Scores of ≥1 indicate that the participant experiences freezing of gait or start hesitation and slowed walking with increased cadence and short steps. HOA inclusion criteria included lack of a history of PD and within a 2-yr age match of one of the PD participants of the same gender. HYA were neurologically healthy between the ages of 18 and 30 yr. Exclusion criteria included use of an assistive walking device or any cardiovascular, musculoskeletal, or vestibular disorders that prohibited the subject from standing and initiating a step independently. Participants provided written informed consent before participating as approved by the university’s institutional review board.
GI trials were performed along a 10-m walkway surrounded by an 11-camera motion capture system (Vicon, Oxford, UK) collecting at 120 Hz. GRF and moments were collected at 1200 Hz from a force plate (model 4060-10; Bertec, Columbus, OH) embedded within the walkway surface. Participants were barefoot and wore tight-fitting clothing. Retroflective markers were placed over bony landmarks according to the Plug-in-Gait marker system. Subjects performed 30 GI trials, 10 trials in each of the three stance conditions (Fig. 1). During the forward and back conditions, the initial starting position of the swing limb was translated 0.5-ft-length forward or backward, respectively, from normal quiet stance. Within each condition, five trials were conducted with each limb on the force plate. Trials were performed in random block method, balanced across participants, for each of the three stance conditions and limb placements (swing limb or stance limb on the force plate). For example, participants performed five trials of a condition and force plate combination (i.e., back swing limb on force plate) followed by sequential blocks of five trials at a different condition–force plate combination (normal swing limb on force plate, etc.). Initial foot positioning for the normal condition and stance width was self-selected and was subsequently constrained via tracings on the floor for consistency across conditions. The stepping leg during GI was the participant’s preferred stepping leg during the normal condition, and this stepping leg was maintained throughout the experiment. Force plate data and kinematics were sampled for the 5 s immediately preceding the auditory signal, defined as quiet standing. The participants were instructed “after hearing the auditory signal, pause and then when you are comfortable, walk to the end of the walkway at your natural pace.”
The mean individual values from the experimental trials for each dependent variable during each stance condition were analyzed and compared across group and condition. We evaluated the average magnitude of swing limb loading during quiet standing (vertical GRF beneath the swing limb as percent of body mass), peak swing limb loading (difference between max and quiet standing average swing limb vertical GRF), peak stance limb propulsive force generation (difference between max and quiet standing average stance limb anteroposterior GRF), APA duration (defined here as the onset of an asymmetric change of the vertical GRF under the swing limb (>5%) until maximum swing limb loading ), and the kinematic COM velocity at the instance of swing limb toe-off, swing limb heel strike, and stance limb heel strike (Fig. 2). The SD of the position of the COM in the frontal plane was used as a surrogate measure of postural stability during quiet standing. In addition, participants ranked the three positions in regard to the most stable and easiest from which to start walking.
GRF- and COM-related variables were evaluated using two separate 2 × 3 (group × stance condition) MANOVA with repeated measures to test for differences while controlling for type 1 error. Statistical significance was set at P ≤ 0.05. When the MANOVA detected significance, follow-up mixed-model univariate ANOVAs were performed as suggested previously (32). When significant group and stance condition main effects were observed, univariate contrasts were conducted using Bonferroni adjustments.
All participants completed the experimental trials without incident such as festination, freezing, or loss of balance. The MANOVA evaluating the GRF data revealed main effects for group (F8,62 = 4.25, P < 0.001) and position (F8,26 = 24.25, P < 0.001). Similarly, for the COM variables, the global MANOVA identified group (F8,62 = 4.67, P < 0.001) and position main effects (F8,62 = 34.17, P < 0.001). A significant interaction was not observed for either the GRF (F16,54 = 0.945, P > 0.05) or COM data (F16,54 = 1.22, P > 0.05). Thus, the remainder of the results are focused on the evaluation of position and group main effects.
Follow-up univariate ANOVAs detected position effects for both variables related to swing limb loading as well as stance limb propulsive force generation (Fig. 3). During the APA period, the participants were able to increase loading onto the swing limb significantly more during the back compared with the two other conditions (both P < 0.001). During the forward condition, swing limb loading was significantly less than that observed in the normal condition (P < 0.01). Propulsive force generated by the stance limb was also greater in the back relative to the normal and forward conditions (P < 0.001). No significant differences in the duration of the APA period among conditions were detected (back = 488 ± 118 ms, normal = 485 ± 130 ms, forward = 530 ± 124 ms).
Initiating gait with the swing limb initially back led to significantly greater velocity of the COM (relative to both normal and forward conditions) when the swing limb left the ground (P < 0.001) as well at the end of both the first (P < 0.01) and second steps (P < 0.01) (Fig. 4). Conversely, the forward-positioned swing limb retarded development of COM velocity (compared with both the normal and back conditions) until the end of the second step where it became similar to that observed in the normal condition (P = 0.12).
Postural sway as measured by the magnitude of the SD in COM position was significantly larger in both the forward (2.3 ± 0.3) and back (2.2 ± 0.2) conditions relative to the normal stance (1.7 ± 0.2; both, P < 0.001). No significant differences were detected between the forward and back conditions (P = 0.591). Despite these results, the participants’ rankings of the conditions based on perceived stability did not show a clear bias (percentage of rankings as the most stable: forward = 32%, back = 32%, normal = 36%). The back condition was ranked the easiest position from which to start walking by 48% of the participants followed by the normal (30%) and forward (22%) conditions.
As mentioned, group main effects were identified for both GRF- and COM-related variables. Specifically when collapsed across condition, swing limb loading during the APA period was significantly lower in the PD group (Fig. 3). As expected, the HYA group produced significantly greater stance limb propulsive force (Fig. 3) and lower APA durations than the HOA and PD groups. Similarly, the HYA produced greater COM velocity at all time points (P < 0.02) than their counterparts (Fig. 4). The PD and HOA groups’ performances were not different across these variables. There was no significant difference in the SD of the COM position across groups.
Regardless of participant group, significant improvement in GI performance was observed by simply starting with the swing limb positioned 0.5-ft-length back from normal. The back condition increased the magnitude of swing limb loading without influencing APA duration, suggesting increased ability to scale task performance to postural demands. Further, the magnitude of the propulsive force and the resulting COM velocities throughout the stepping phase were significantly enhanced, meaning that a more dynamic and faster GI was achieved. These findings indicate that natural-pace GI can be acutely enhanced by manipulating the initial stance position through improved postural and stepping components.
Participants stood with significantly more loading under the initial swing limb when in the back condition. Once the initiation process began, this position facilitated further swing limb loading. This weight shift and posterior–lateral movement of the COP is a critical component of an efficient GI pattern and serves to uncouple the COP and COM. The ability to separate these two by manipulating the COP has major implications on momentum generation and balance control. Previously, Brunt et al. (4) have shown that manipulating the initial position of the limb in the sagittal plane can influence sit to stand performance, a task with a similar initial motor response to GI. Rocchi et al. (30) have also shown that widening initial stance also leads to greater loading of the swing limb. Because stance width was constant throughout our conditions, the greater weight shift was likely due to greater effectiveness of the APA. A potential stability-related factor as to why the back condition had a greater swing limb loading relative to normal is that there is a greater tolerance to asymmetrical loading. The asymmetrical loading between the two legs would cause the COM to be driven laterally and forward rather than just laterally as in the normal condition. Older adults and persons with Parkinson may not exhibit large asymmetries of limb loading to avoid destabilizing themselves in the mediolateral plane during normal stance; the diagonal stance condition would help alleviate this potential problem. Beneficial effects of the back condition were generally comparable across groups, indicating the capacity to improve the postural components of GI by simply altering the starting position. These findings should provide important information for rehabilitation specialist as they indicate that both older adults and those with neurologic impairment can use this foot placement strategy.
The duration of APA did not change across conditions; thus, participants were able to produce greater forces within the same period while in the back condition, translating into a more dynamic initiation of gait. The ability to scale force amplitude while keeping the time to reach peak force relatively constant is consistent with the notion of a pulse height neural control strategy observed by neurologically healthy subjects (12,13,26). Previous research has shown that regulation of force time parameters, particularly the rate of development, is significantly impaired in PD (1,3,9,29,33,34). Further, impairment in force development has been proposed to be one of the underlying causes of bradykinesia (27). That such a simple strategy as altering initial limb placement improved a consistently important impairment is significant.
The velocity of the COM was greatest at every time point when initiating gait from the back condition. The greatest influence of altering foot position, however, seems to occur early in the GI process, where the spatiotemporal interactions between the postural and stepping requirements occur. This finding that performance can improve in temporal relation to the switch between the two proposed motor programs governing GI is important because impaired GI performance in PD is associated with changes in the basal ganglia that result in slowing the sequential execution of the postural and stepping components (31).
Rocchi et al. (30) reported that widening stance width leads to improved step velocity. However, individuals with PD had much more difficulty initiating a step from the wide stance, thus reducing the potential efficacy of this strategy. Mille et al. (24,25), in two separate studies of individuals with PD, have shown that a lateral assist force delivered to the hip timed with the APA can improve GI performance including velocity of the first step. Similar improvements in GI performance were realized in the current study when initiating gait from the back stance. We propose that altering foot position may be more practical than a robotically controlled lateral assist in improving performance and raises future consideration of its effects on PD freezing.
Although these results are promising, the back condition did cause significantly greater oscillations in the mediolateral position of the COM during quiet standing than the normal condition. The groups, however, did not report any differences in their sense of stability across the conditions and ranked the back condition as the easiest from which to start walking by each population of participants. While adopting a staggered stance position could be perceived as an added task demanding further postural control, previous work has shown perseverance of stopping ability with mild to moderate PD (2,8). Thus, we propose that stopping with a slightly staggered stance is potentially no more or less difficult than stopping with a parallel stance. To evaluate the real-world application of this technique, we asked 25 ambulatory persons with PD to perform planned gait termination tasks whereby they achieve a stopping position with their feet staggered. All participants (across a range of mild to moderate disease severity) were able to do so without observable loss of stability or an increase in braking time (unpublished data). Thus, we recommend that times when GI performance may be problematic for people with PD, such as at a cross walk, stopping with a staggered stance may be an appropriate strategy. In addition, participants in the present study did not report or exhibit any real difficulty in establishing this starting position likely because of the rather small asymmetry in foot placement (0.5-ft length). At times when planned stopping may be constrained yet efficient GI performance is needed (such as entrance and exit of an elevator), individuals may adjust their feet to achieve the more optimal back stance condition.
The beneficial properties exhibited by the back condition are likely due to the biomechanical advantages awarded by the spatial orientation of the body. The more extended position of the swing limb likely places greater stretch on the hip flexor and plantar flexor muscles of the limb, potentially creating a faster rate of force production and corresponding limb velocity (18,19). The back position may also facilitate the transfer of rotational momentum generated by the swing limb to help carry the COM over the stance limb (pendular dynamics), reducing the amount of energy otherwise required. Certainly, EMG analyses of the muscle activation patterns and evaluation of potential changes in corticospinal and spinal excitability are needed to better address the contributing mechanisms.
Concerning the limitations of the study, the constraint of using only a single-force platform during data collections prevented simultaneous measurement of forces beneath both swing and stance limbs. Although trials were duplicated using the same stance position to obtain both swing limb and stance limb force data as has been done previously (5), differences may have arose between these trials that are not evident in the results. GI is brought about by a motor program that governs a complex sequence of muscle activation patterns. Thus, future studies investigating differences in starting position should further evaluate changes in muscle activation to help better understand the underlying changes in behavior observed here. A potential confound exists in the use of a constrained stance width across conditions. This was done to isolate the effects of anterior–posterior modifications. Participants may have naturally altered their preferred stance widths in the forward and back conditions if allowed, which could potentially modify swing limb loading and stepping behavior (30). A larger group sample size and greater diversity of individuals with PD may increase the fidelity of our findings. Future studies should also investigate the effectiveness of this protocol in individuals with freezing of gait.
In conclusion, placing the swing limb backward 0.5-ft length from the normal stance had significant positive effects on both the postural and locomotor phases of GI in all participants. Further, initiating gait from the back condition allowed the persons with PD to initiate gait in a similar fashion as their age matched peers. These findings suggest that altering foot position may be an effective therapy to offset the typically observed deterioration in initiation performance.
This study was supported in part by the National Institutes of Health (5R03HD054594-02) and the University of Florida’s National Parkinson’s Foundation Center of Excellence.
The authors have no conflicts of interest.
The results of the present study do not constitute endorsement by the American College of Sports Medicine.
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