Different protocols for analyzing behavior and adaptability in obstacle crossing in Parkinson’s disease

Figures & data

Figure 1 The model describing the elements that affect dynamic postural control during locomotion.

Note: Copyright © 2013. John Wiley and Sons. Reproduced from Earhart GM. Dynamic control of posture across locomotor tasks. Mov Disord. 2013;28(11): 1501–1508.³

Figure 2 Cognitive impairment predicted dementia, although gait abnormalities increased the risk for falling (shaded arrows).

Notes: A complete understanding suggests that cognitive impairment and gait abnormalities, coupled with dementia and falls, are related to each other (white arrows). In the light of recent evidence, gait abnormalities predict dementia and cognitive impairment raises fall risk (gray arrows); based on the close relationship between cognition and gait on the one hand, integrated tools for risk estimation are needed (bracket). Furthermore, the possible lines of intervention (black arrows) could rely on increasing cognition for fall prevention and on walking training for lessening dementia risk. Copyright © 2013. John Wiley and Sons. Reproduced from Amboni M, Barone P, Hausdorff JM. Cognitive contributions to gait and falls: evidence and implications. Mov Disord. 2013;28(11):1520–1533.³¹

Figure 3 This figure depicts the laboratory setup for testing continuous and intermittent walks.

Notes: The authors highlight that continuous walking protocols may be more reliable. Reprinted from Gait Posture, 37(4), Galna B, Lord S, Rochester L, Is gait variability reliable in older adults and Parkinson’s disease? Towards an optimal testing protocol, 580–585, Copyright (2013), with permission from Elsevier.³⁸

Figure 4 (A) Examples of apparatus and gait parameters used to calculate the approach, crossing, and recovery steps during obstacle crossing. (B) An example of horizontal and vertical obstacle clearance parameters.

Note: Reprinted from Arch Phys Med Rehabil, 93(4), Stegemöller EL, Buckley TA, Pitsikoulis C, Barthelemy E, Roemmich R, Hass CJ, Postural instability and gait impairment during obstacle crossing in Parkinson’s disease, 703–709, Copyright (2012), with permission from Elsevier.⁹
Abbreviations: LF, leading foot; TF, trailing foot.

Figure 5 Schematic illustration of the experimental set-up analyzing anticipatory postural adjustments upon gait initiation crossing an obstacle.

Note: Reproduced from Yiou E, Artico R, Teyssedre CA, Labaune O, Fourcade P. Anticipatory postural control of stability during gait initiation over obstacles of different height and distance made under reaction-time and self-initiated instructions. Front Hum Neurosci. 2016;10:449.⁴⁷

Figure 6 Top view of the laboratory setting of the effect of Tai Chi Chuan training in obstacle crossing behavior, analyzed by kinematics (Vicon motion analysis system) and kinetic ground reaction forces (Kistler force plates).

Note: The effect of Tai Chi Chuan on obstacle crossing strategy in older adults. Chang YT, Huang CF, Chang JH. Research in Sports Medicine. 26 Jun 2015. Reprinted by permission of the publisher (Taylor & Francis Ltd, http://www.tandfonline.com).⁵²

Table 1 Relation between gait and cognition throughout obstacle crossing in young and old healthy subjects and in Parkinson’s Disease

Study	Participants		Protocol	Gait assessment	Temporal and/or distance constraints	Results
	Age	Number
Young and old healthy subjects
Pan et al^Citation12	≥55	Older adults at low (n=10) vs high risk of falling (n=10)	Performed barefoot obstacle crossing along a 6-m walkway at a self-selected speed	The subjects were classified as being at high or low risk of falling by the Tinetti Balance and Gait test (a score of >36 or <36, respectively). Gait kinematics was evaluated in different obstacle heights subsets, at 10%, 20%, and 30% of leg length	Yes	Individuals at a high risk of falling demonstrated less symmetry between the leading and trailing legs and a narrower step width
Caetano et al^Citation8	74±7/26±4	Older adults (n=50); young adults (n=21)	Randomly presented gait adaptability trials (3 trials of each) of: obstacle avoidance, short stepping target, long stepping target and no target/obstacle	Gait adaptability was accessed by using a symmetry ratio equation, which provides a comparison of the clearance profile for both legs	Yes	Older adults exhibited a more conservative adaptation strategy characterized by slow, short and multiple steps with longer time in double support, and demonstrated poorer stepping accuracy and made more stepping errors (failed to hit the stepping targets/avoid the obstacle)
Dadashi et al^Citation53	>65	Older adults (n=1,400)	Analysis of anthropometric characteristics with foot clearance kinematic measurements while walking in a 20-m unobstructed/obstructed corridor	Gait variability (range of the temporal, spatial and clearance parameters) under continuous protocols vs obstacle negotiation strategies	Yes	Provided normative dataset of gait parameters and characterized gait patterns associated with increased risk of falling
Yiou et al^Citation47	23.2±4	Young adults (n=14)	Subjects initiated gait in three conditions of obstacle height, three conditions of obstacle distance, and one obstacle-free (control) condition	Stabilizing features of gait initiation included APAs and lateral swing foot placement	Yes	Medial-lateral APAs are scaled with swing duration in order to maintain an equivalent stability across experimental conditions. The anticipatory peak of MLCOP shift, the initial ML COMvelocity and the duration of the swing phase, of gait initiation, increased with obstacle height, but not with obstacle distance
Chang et al^Citation52	>65	Tai Chi group (TCG) (n=15) vs healthy older adults (n=15)	Practice of Yang style and Tai Chi Chuan, of 108 postures. The routine was 3 days a week for 5 or more years with 8-m walkway and a height-adjustable obstacle (different heights of the obstacle [10%, 20%, and 30% of the leg length])	Defined 3 step positions as a crossing stride including stride length, stride time and stride velocity in order to determine foot-obstacle clearances and the flexion angle of the hip, knee, and ankle	No	The TCG group performed significantly faster stride velocities, longer stride lengths, and shorter stride times. TCG could also produce significantly larger forward ground reaction forces to propel the body and were able to make a significantly greater flexion angle of the hip of the leading leg compared with the general group
Hollman et al^Citation39	>65	Older adults (n=24)	Subjects walked during the normal and dual task (backward spelling) walking conditions at self-selected speeds and then repeated the tests. Determined the test-retest reliability of 3 gait parameters (pace, rhythm, and variability) during normal and dual task walking	Velocity, cadence, and variability in stride velocity were measured	No	Fewer than 10 to 20 strides may reliably measure velocity and cadence in either normal or dual task walking. Variability in stride velocity requires hundreds of strides, particularly in dual task walking
Nakano et al^Citation55	25.6±4.6	Healthy young adults (n=12)	Avoidance of a virtual white planar obstacle by lengthening or shortening their steps under free or constrained conditions (normal-walking/walk-through conditions)	The comparison of X-COM shift and placement of lateral foot during the different obstacle conditions	Dual	Temporal constraints affect postural stability in the AP and ML directions during step adjustments. AP and ML stability at swing foot contact is maintained through adjustments of step length and lateral foot placement, respectively
Ida et al^Citation56	27.3±4.7	Healthy adults (n=10)	Participants stood upright and lifted one leg to avoid colliding with a real obstacle sliding on the floor toward a participant and with its virtual image (delivered by a head-mounted display or a 3D projector)	The acceleration of the foot, the center of pressure, and electrical activity of the leg and trunk muscles were measured during the time intervals typical for early postural adjustments, anticipatory postural adjustments, and compensatory postural adjustments.	Yes	Reduced activity of the leg and trunk muscles when dealing with virtual obstacles as compared with that seen when dealing with real obstacles
Parkinson’s disease
Pieruccini-Faria et al^Citation46	69.7 (±9.3)/69.3 (±8.9)	PD patients (n=20); healthy age-matched control participants (n=19)	Walking and gaze behavior on approaching an obstacle (baseline/dual-task)	Synchronized gaze and gait data split into an early and late phase prior to the obstacle	No	In the off state, the behavior of gaze had no interactions with phase or condition suggesting that the deceleration and increased variability when approaching an obstacle is the result of a greater demand for online sensory feedback that cannot be compensated for with visual strategies. Dopamine influences planning by limiting sensorimotor processing capacity
Liao et al^Citation14	67.3±7.1; 65.1±6.7; 64.6±8.6	PD patients VRWii (n=12); PD patients TE (n=12); healthy participants (n=12)	Participants received VRWii group or TE group for 45 minutes, followed by 15 minutes of treadmill training in each session for a total of 12 sessions over 6 weeks. Obstacle crossing required the participants to walk on a 10 m walkway with an obstacle positioned in the middle of the walkway (height of the obstacle was 20% of the subject’s leg length)	Three obstacle-crossing variables (stride length and velocity; Vertical toe-obstacle clearance)	Yes	The VRWii group showed a greater improvement in obstacle crossing velocity and crossing stride length
Caetano et al^Citation13	66±6	IPD patients (n=46)	Randomized controlled trial comparing home-based step training with control (no-intervention). Intervention group participants played a step game 3 times a week for 15 minutes each session for 12 weeks	Gait adaptability performance was assessed at baseline and 12-week follow-up, and accessed with randomly presented gait adaptability trials: obstacle avoidance, short stepping target, long stepping target and no target/obstacle (three trials of each)	No	Home-based interactive videogame step training improves an ability to adapt gait in response to unpredictable stepping targets in people with PD
Pestana et al^Citation18	NA	PD patients (n=13); healthy subjects (n=13)	Performed 5 trials of unobstructed gait and 10 trials of obstacle crossing (5 crossing trials with each leg) (obstacle height of 15 cm) with and without auditory cues. Auditory cue (controlled by a metronome) was personalized for each individual according to the cadence determined by the 3 trials performed previously to start the experiment	Symmetric index of gait parameters was analyzed in the least and in the most affected limb in the different paradigms	n.i	Auditory cues in unobstructed walking decreased step velocity asymmetry in PD patients but lacked effect during obstacle crossing
Stegemöller et al^Citation9	62.2±9.1/62.0±9.3	IPD patients (n=10); healthy subjects (n=10)	9 m continuous barefoot walking with 5 trials like 1 step recovery, 1 step approach throughout obstacle crossing and normal walking	Gait parameters, obstacle clearance parameters, and COM motion	Yes	PD is more conservative and more time-consuming in dynamical stability strategy during obstacle crossing; obstacle crossing increased the mediolateral range of motion, margin of stability, duration of single limb support and reduction of the distance between COM and COP
Galna et al^Citation10		IPD patients (n=20); healthy subjects (n=20) (n=10)	10 steps at their preferred speed along a walkway and stepped over an obstacle (height 10% of leg length ×600×10 mm)	Spatiotemporal variables were measured using an eight-camera Vicon motion analysis System	Yes	PD approached and stepped over the obstacle slower and with smaller steps, but had a similar foot clearance. Those with PD were also more likely to step on the obstacle because they did not place their foot close enough to the front of the obstacle before crossing it to accommodate for their reduced step length. During the lead limb crossing step, people with PD increased their step width, whereas controls maintained a narrow step width
Smulders et al^Citation45	64.6±8.1; 66.3±7.5	Non-recurrent PD fallers (n=171); recurrent PD fallers (n=91).	Patients walked 2 times along a 10-m trajectory, both under single-task and DT conditions (combined with an auditory Stroop task)	Dual-task costs were calculated for gait speed, stride length, stride time, stride time variability, step and stride regularity, step symmetry and Stroop composite scores (accuracy/reaction time)	Yes	Stride time, stride time variability, step and stride regularity, and step symmetry did not change under DT conditions. Recurrent fallers did not show different dual-task costs compared to non-recurrent fallers
Galna et al^Citation38	68.1±7.3/72.2±6.3	PD patients (n=25); Healthy subjects (n=27)	Estimated the reliability of gait variability during continuous and intermittent walking then determined optimal number of steps for acceptable levels of reliability of gait variability	Gait variability was calculated for step velocity, length and width, and step, stance and swing duration	Yes	Gait variability was more reliable in continuous walking protocols with no fewer than 30 steps
Rogers et al^Citation48	72.9±9.3/73.3±9.1	PD patients (n=8); Healthy subjects (n=8)	Perturbation trials, the stance limb ground support surface was either moved vertically downward (DROP) or upward (ELEVATE) trials by 1.5 cm shortly after the onset of the APA phase	APAs for lateral weight transfer and propulsion	No	During ELEVATE trials that opposed the intended weight transfer forces, both groups rapidly adapted their stepping to preserve standing stability by decreasing step length and duration and increasing step height and foot placement laterally. PD patients demonstrated a longer APA duration, longer time to first step onset, and slower step speed than controls
Burleigh-Jacobs et al^Citation49	66.7±6.2/66.3±6.4	PD patients (n=6); Healthy subjects (n=6)	Healthy subjects and PD patients (ON/OFF levodopa conditions) were instructed to take a forward step with left foot and follow with the right in three conditions: (a) self-generated; (b) perceived a brief, 4-ms current pulse cutaneous cue delivered to the hand or the earlobe; (c) the onset of the cutaneous cue was simultaneous with the onset of a backward surface translation	Ground reaction forces and body kinematics were recorded for self-generated and cutaneous cue-triggered step initiation. The effects of assisting anticipatory postural sway with a surface translation coupled with a cutaneous cue were also examined	No	Levodopa (ON) was able to slightly counteract the decreased force production, decreased the velocity of movement, and slowed execution of the APAs for self-generated step in PD when OFF. Cutaneous cue was beneficial in all groups. The surface translation, both groups executed the APAs for step more rapidly, but the PD subjects, both ON and OFF, failed to increase the force to execute push-off more rapidly
Chong et al^Citation50	68±9; 26±9; 67±9	PD patients (n=10); 10 healthy young subjects (n=10); healthy older adults (n=10)	The subjects were analyzed in 2 experiments: (1) when the direction of a surface perturbation changed from a backward translation to a toes up rotation; and (2) when subjects were instructed to ‘give’ or ‘resist’ while responding to the translations and rotations	The ability to change set was inferred by measuring the change in the amplitude of automatic gastrocnemius or tibialis anterior muscle responses	No	PD patients did not change sensorimotor set (suppression of gastrocnemius responses to toes up rotations) immediately to the first rotation but needed several rotations to change their responses. PD patients had more difficulty in using cognitive set to modify their responses, especially when instructed to ‘resist’ the perturbations
Jacobs and Horak^Citation51	62 (49–78); 70 (66–78); 66 (52–78)	Moderate PD (n=5); severe PD patients (n=5); Healthy subjects (n=10)	Compensatory steps in response to backward surface translations in five conditions: with eyes closed, with eyes open, to a remembered visual target, to a target without seeing their legs (wearing a lightweight vest that blocked their view of their legs), and to a target while seeing their legs	Reflective markers positioned in several points of the body, with the 3-dimensional spatial coordinate information about the displacement of body segments calculated by high-resolution video cameras	No	PD patients exhibited shorter compensatory steps. Severe PD patients made larger accuracy errors when stepping toward targets, which was worsened when unable to see their legs. Patients exhibited short compensatory steps due to abnormal proprioceptive-motor integration and used visual input to take longer compensatory steps, unhelpful in more severe cases and unresponsive to levodopa

Abbreviations: AP, anterior-posterior; APA, anticipatory postural adjustments; COM, center of mass; COP, center of pressure; DT, dual-task; IPD, Idiopathic Parkinson’s Disease; ML, mediolateral; n.i, no information was available to discern about the use of temporal and/or distance constraints; PD, Parkinson Disease; TCG, Tai Chi group; TE, traditional exercise; VRWii, virtual reality–based Wii Fit exercise; X-COM, extrapolated Center of Mass.

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