Gait Analysis in Patients With Parkinson's Disease Off Dopaminergic Therapy

Article Outline

• Abstract
• Methods
  • Subjects
    • Patients
    • Controls
  • Gait Analysis
  • Statistical Analysis
• Results
  • Time-Distance Parameters
  • Lower-Extremity Joint Angles
  • Kinetics
• Discussion
  • Time-Distance Parameters
  • Lower-Extremity Joint Angles
  • Kinetics
• Conclusions
• References
• Copyright

Abstract 

Švehlík M, Zwick EB, Steinwender G, Linhart WE, Schwingenschuh P, Katschnig P, Ott E, Enzinger C. Gait analysis in patients with Parkinson's disease off dopaminergic therapy.

Objective

To compare time-distance, kinematic, and kinetic gait parameters in patients with idiopathic Parkinson's disease (PD) off dopaminergic therapy with a group of healthy control subjects.

Design

A group-comparison study.

Setting

Gait analysis laboratory.

Participants

Patients with PD (n=20) and healthy age-matched controls (n=20).

Interventions

Not applicable.

Main Outcome Measures

Time-distance, kinematic, and kinetic gait variables.

Results

PD patients walked slower with shorter stride-length, comparable cadence, and longer double support times. Kinematics showed a reduction of the range of motion in the hip, knee, and ankle joints. Maximum hip extension and the ankle plantar flexion were significantly reduced. Kinetic gait parameters showed reduced push-off ankle power and lift-off hip power generation. Strong correlations between these important body advancement mechanisms and the walking velocity were observed.

Conclusions

In addition to previously described dysfunctional kinematics, abnormal kinetic parameters play an important role in the characterization of gait in PD patients off therapy. Hence, these parameters could be used to document treatment effects of parkinsonian gait disorders.

Key Words: Biomechanics, Levodopa, Neurologic gait disorders, Parkinson Disease, Rehabilitation

List of Abbreviations: PD, Parkinson's disease, L-dopa, levodopa, ROM, range of motion

IDIOPATHIC PARKINSON'S DISEASE is a chronic, progressive neurologic disorder affecting approximately 1 in every 100 people over 65 years of age. Gait disorders are a hallmark of the condition and are associated with a loss of independence¹ and an increased incidence of falls.² Clinically, patients with PD tend to show a shuffling gait pattern with shortened stride length, reduced overall velocity, and increased stance phase durations.³ Moreover, reduced or absent arm swing; reduced trunk rotation; and decreased amplitude of motion at the hips, knees, and ankles are characteristic of the PD gait.⁴ Gait deficiencies in PD arise from a disturbance in the motor set function of the basal ganglia specifically involved in the regulation of movement amplitude.⁵ Basal ganglia also appear to inhibit movements via direct and indirect pathways⁶ and contribute to the regulation of postural alignment and axial motor control.⁷, ⁸ Visual cues are known to improve the gait of PD patients, possibly by bypassing the faulty basal ganglia. They may develop through the patient's ability to utilize visual feedback to regulate the movement amplitude, thus reducing reliance on kinesthetic feedback.⁵

Early studies investigating parkinsonian gait disorders used footswitches and stride analyzers to describe abnormalities in spatial-temporal parameters of gait (velocity, stride length, or cadence).⁹, ¹⁰ More recently, computer-assisted gait analysis has been adopted as an objective measurement tool to describe kinematic parameters.¹¹, ¹² Morris et al¹³ and Lewis et al⁵ described both the kinematic and kinetic features of parkinsonian gait and found reduced plantar flexion at toe-off and insufficient ankle power generation. However, only 1 study by Sofuwa et al¹⁴ has compared quantitative spatiotemporal, kinematic, and kinetic gait analysis parameters of PD patients on dopaminergic therapy to a group of healthy elderly controls. To our knowledge, no equivalent study investigating PD patients off therapy has been published. However, such an approach may provide greater insight into the nature of the motor deficits caused by the disorder itself, as the medication might have confounding effects on force generation patterns.⁵ Therefore, we set out to compare time distance, kinematic, and kinetic gait parameters of PD patients off therapy with a group of healthy control subjects to circumvent these limitations.

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Methods 

Subjects 

Twenty patients with idiopathic PD (13 men, 7 women) were recruited from the local movement disorders clinic at the Department of Neurology at Medical University of Graz, Austria. Inclusion criteria were PD according to UK Parkinson's Disease Society Brain Bank clinical diagnostic criteria¹⁵; age 50 to 80 years; dopaminergic medication; no concurrent neurologic, orthopedic, or other medical conditions affecting gait; absence of dementia based on prior cognitive assessment; Hoehn and Yahr stages 1 to 4 off therapy; and the ability to walk along a 12-m walkway at least 5 times without assistance. Participants were asked to stop short-acting dopaminergic medications (standard preparations of L-dopa and short-acting dopamine agonists) at least 12 hours before the study and long-acting preparations (cabergoline, control release preparations of L-dopa) at least 24 hours beforehand, which induced a relative and clearly defined “off” state.¹⁶ Two subjects had a history of rare freezing when walking and 3 had a history of festination, but we did not observe any freezing of gait during testing.

Twenty healthy subjects (10 men, 10 women) aged 50 to 80 years with no current neurologic, orthopedic, or other medical conditions affecting gait made up the control group. The control group was age matched to the PD group. Although the groups were not sex matched, there was no statistically significant difference in the leg lengths that could have influenced our results. The Mini-Mental State Examination scores did not differ between the groups.

All participants gave written informed consent according to the 1991 Declaration of Helsinki, and the study was approved by the local research ethics committee. Before gait analysis, all patients were examined according to the Unified Parkinson's Disease Rating Scale motor rating scale¹⁷ and classified with the Hoehn and Yahr disability scale.¹⁸ Details concerning demographics, clinical data, and medication for the patients are given in table 1.

Table 1. Demographic, Clinical, and Drug Details of PD Patients

Patient	Age	Sex	MMSE	Years Since Diagnosis	Side Most Affected	UPDRS III Off Therapy	Hoehn and Yahr Stage	Levodopa (DD, mg)	Dopamine Agonists (DD, mg)	Other PD Medication (DD, mg)
1	67	M	23	4	R	42	2,5	—	pra,4.5mg	sel,10mg
2	67	M	23	10	L	15	2	—	per,3mg	—
3	65	M	21	4	L	49	2	450mg	—	—
4	66	F	26	11	R	38	2	300mg	rop,21mg	sel,10mg
5	76	M	20	1	L	35	2	300mg	—	—
6	59	F	28	8	L	52	3	700mg	pra,4.5mg	sel,10mg
7	73	M	27	10	L	39	2,5	800mg	pra,6.0mg	—
8	76	M	28	3.5	L	37	2	500mg	pra,3mg	—
9	67	M	24	5	L	49	2	—	pra,3mg	—
10	70	M	26	10	L	42	2,5	300mg	pra,3mg	sel,10mg
11	71	F	27	5	R	35	2	150mg	pra,3mg	—
12	63	M	24	10	R	30	2	300mg	pra,3mg	sel,10mg
13	75	F	27	1	R	32	2,5	150mg	pra,1.5mg	—
14	52	M	30	3	R	31	2	—	rop,15mg	—
15	60	M	29	5	L	57	3	400mg	rop,12mg	—
16	74	M	22	5	R	51	2	150mg	cab,3mg	—
17	56	M	28	7	R	45	2,5	300mg	cab,4mg	sel,10mg
18	57	F	27	7.5	R	31	2	150mg	cab,4.5mg	sel,10mg
19	66	F	24	9	L	32	2	600mg	pra,4.5mg	—
20	76	F	28	6	R	15	1,5	100mg	pra,2mg	—

Abbreviations: F, female; M, male; MMSE, Mini-Mental State Examination; UPDRS III, Unified Parkinson's Disease Scale–motor part; DD, daily dose; pra, pramipexole; per, pergolide; rop, ropinirole; cab, cabergoline; sel, selegiline; R, right; L, left.

Gait Analysis 

Gait analysis was performed with the use of a 12-camera motion capturing system^a and 4 force plates^b mounted under the walkway. Marker arrangement, calculation methods, and model assumptions applied have been described in detail by Kadaba et al.¹⁹ Calculations of kinematic parameters for the pelvis and the hip, knee, and ankle joints as well as kinetic parameters for the hip, knee, and ankle joint were performed by using the Vicon Clinical Manager.^a Moment and power parameters were normalized to the weight of the patients. Power generation and absorption patterns in the sagittal plane were calculated and labeled according to the method described by Winter.²⁰ All patients walked at self-selected speeds along a 12-m walkway, and only steady-state walking was measured. For each patient, a minimum of 5 trials per limb providing a clear foot force plate contact were captured. From each trial, only 1 gait cycle was used to calculate the patient's mean trial. Pelvic kinematics and sagittal plane kinematic and kinetic parameters of the hip, knee, and ankle joints, as well as time-distance parameters (gait velocity, cadence, stride length, single and double support time) were used as outcome measures in this study.

Statistical Analysis 

Time-distance parameters, kinematics, and kinetic data were compared with the values obtained from the control group by using unpaired Student t tests after testing for normal distribution. Bonferroni correction for multiple testing was applied, and P values of less than .001 were considered as statistically significant. A Pearson correlation coefficient was used to express the relationship between the velocity and the main propulsion generation variables. All analyses were calculated by using the Statistica 6.0^c software.

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Results 

Time-Distance Parameters 

The PD group showed decreased walking velocity and stride length, whereas cadence did not differ from the control group (table 2). The double-limb support and the stance phase of gait were prolonged in the PD group.

Table 2. Time-Distance Parameters for the PD Group and the Control Group

Abbreviations: CI, confidence interval; GC, gait cycle.

Lower-Extremity Joint Angles 

The ROMs were reduced at all lower-extremity joints in the PD group (table 3). PD subjects walked with a markedly increased pelvic tilt. Pelvic obliquity and transversal rotation did not differ between the groups. The extent of maximum hip flexion was comparable between the groups. In the control group, the maximum hip extension showed higher values and the maximum hip extension occurred earlier during the gait cycle than in the PD group (fig 1). The PD group walked with an increased knee flexion during the single-support phase. Although there was no significant difference in maximum knee flexion, its timing occurred later during the swing phase in the PD group. Differences were most pronounced at the ankle joint. The mean plantar flexion during the first rocker was reduced in the PD group. PD patients walked with slightly increased dorsal flexion during the whole stance phase. Although the maximal dorsal flexion did not differ between the groups, a reduction of the plantar flexion at toe-off was observed. This resulted in decreased ankle ROM during push-off. Whereas the timing of maximum dorsal flexion occurred later in the PD group, the timing of maximum plantar flexion was comparable between the groups.

Table 3. Kinematic Parameters for the PD Group and the Control Group

	PD Group			Control Group
Parameters	Mean	CI (5% to 95%)	SD	Mean	CI (5% to 95%)	SD	P
Ankle angle (°)
Initial contact	−1.46	−2.56to−0.36	3.43	−0.79	−2.32to.73	4.77	.477
Toe-off	−5.34	−7,17to−3,5	5.74	−10.77	−13.07to−8.48	7.17	<.001⁎
Max dorsiflexion	14.29	13–15.58	4.03	12.92	11.26–14.59	5.21	.192
Timing of max dorsiflexion	50.05	48.51–51.59	4.81	47.10	45.37–48.83	5.42	.012
Max plantarflexion	−7.55	−9.19to−5.91	5.13	−12.66	−14.8to−10.52	6.69	<.001⁎
Timing of max plantarflexion	49.25	40.42–58.08	27.61	58.00	52.3–63.7	17.81	.096
Mean dorsiflexion in stance	6.51	5.57–7.45	2.93	4.37	2.89–5.84	4.62	.015
Push-off ROM	19.63	18.01–21.26	5.09	23.70	21.88–25.52	5.69	.001⁎
ROM over gait cycle	21.84	20.2–23.48	5.13	25.58	23.91–27.25	5.22	.002
Knee angle (°)
Initial contact	6.52	5.32–7.72	3.76	5.21	3.84–6.59	4.30	.153
Mean flexion in single support	7.68	6.21–9.15	4.59	3.42	2.02–4.82	4.37	<.001⁎
Toe-off	37.09	35.69–38.48	4.37	34.07	32.2–35.95	5.86	.011
Max flexion	51.62	50.16–53.08	4.56	53.60	52.12–55.07	4.60	.057
Timing of max flexion	73.30	72.73–73.87	1.79	71.95	71.52–72.38	1.36	<.001⁎
Max extension	2.55	1.03–4.06	4.73	−2.04	−3.6to−.47	4.88	<.001⁎
ROM over gait cycle	49.07	47.09–51.05	6.20	55.63	54.03–57.23	5.00	<.001⁎
Hip angle (°)
Initial contact	32.61	30.91–34.31	5.32	32.38	30.18–34.59	6.89	.869
Max flexion	33.59	31.96–35.23	5.12	32.89	30.66–35.11	6.96	.606
Max extension	−3.71	−6.05to−1.38	7.30	−12.70	−15.3to−10.06	8.25	<.001⁎
Timing of max extension	53.35	52.69–54.01	2.07	51.85	51.33–52.37	1.63	<.001⁎
ROM over gait cycle	37.31	35.2–39.41	6.58	45.58	42.82–48.35	8.64	<.001⁎
Pelvic angle (°)
Max obliquity	1.99	1.1–2.88	2.78	2.91	2.03–3.79	2.74	.141
Min obliquity	−1.91	−2.8to−1.03	2.77	−2.96	−3.82to−2.09	2.70	.090
Mean tilt	12.87	11.57–14.17	4.07	8.69	6.69–10.68	6.24	<.001⁎
Max tilt	14.09	12.75–15.43	4.19	9.87	7.86–11.89	6.29	<.001⁎
Min tilt	11.55	10.26–12.83	4.02	7.43	5.42–9.44	6.28	<.001⁎
Max rotation	3.28	2.21–4.34	3.34	4.25	2.31–6.18	6.05	.377
Min rotation	−3.12	−4.2to−2.05	3.35	−4.31	−5.93to−2.7	5.05	.218

Abbreviations: CI, confidence interval; Max, maximum; Min, minimum.

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• Fig 1. 

  Ankle, knee, and hip kinematics and kinetics. The gray lines and areas represent the control group mean ± 1 SD. The solid and dashed black lines represent the PD group mean ± 1 SD. GC, gait cycle; gray arrow, toe-off of the control group; black arrow, toe-off of the PD group.

Kinetics 

Abnormal patterns of motion in the PD group were even more pronounced in the kinetic gait parameters. The maximum hip flexor moment was reduced in the PD group (table 4). The maximum hip extensor moment was not different between the groups (see fig 1). Power generation was reduced in the PD group for the first double support and for the preswing phase. Also, maximum hip power absorption in the stance phase was reduced in the PD group (see fig 1). At the knee, the maximum extensor moment during stance was higher in the control group as was the flexor moment during the single support phase. The PD group generated less power during single stance, and the maximum power absorbed in the late stance phase was reduced. At the ankle, the moment at loading response and the maximal extensor moment during stance were reduced in the PD group. The power generation in the PD group deteriorated in the late stance and the absorption during the loading phase was reduced when compared with the control group. There was a positive correlation between the ankle push-off power and walking velocity for both groups (table 5). We also found a positive correlation between the lift-off power generated at the hip in the preswing phase and the walking velocity. This correlation was stronger in the PD group. However, the pull-off propulsive mechanism was independent of the walking velocity in both groups.

Table 4. Kinetic Parameters for the PD Group and the Control Group

	PD Group			Control Group
Parameters	Mean	CI (5%–95%)	SD	Mean	CI (5%–95%)	SD	P
Ankle moment (Nm/kg)
Max extensor moment in stance	1.19	1.13−1.24	.19	1.42	1.37−1.47	.14	<.001⁎
Loading response	0.07	−.08to−.05	.05	−0.09	−0.11to−0.08	.04	.021
Ankle power (W/kg)
Max generation in stance	2.13	1.94−2.32	.59	3.15	2.89−3.42	.83	<.001⁎
Absorption in loading response	−0.18	−.22to−.14	.12	−0.10	−.12to−.08	.05	<.001⁎
Knee moment (Nm/kg)
Max extensor moment	0.24	.18to0.3	.18	0.36	.29−.43	.22	.010
Max flexor moment in single support	−0.19	−.26to−.11	.23	−0.29	−.34to−.24	.16	.028
Knee power (W/kg)
Max absorption in stance	−1.14	−1.28to.99	.47	−1.50	−1.65to−1.35	.47	<.001⁎
Max generation in single support	0.26	.21−.32	.18	0.45	.36−.54	.29	<.001⁎
Hip moment (Nm/kg)
Max flexor moment	−0.83	−.93to−.73	.32	−1.13	−1.22to−1.04	.29	<.001⁎
Max extensor moment	0.66	.59−.73	.23	0.69	.62−.77	.23	.521
Hip power (W/kg)
Max generation in preswing	1.13	.99−1.28	.45	1.59	1.44−1.74	.46	<.001⁎
Max absorption in stance	−0.73	−.89to−.57	.50	−1.04	−1.19to−.89	.47	.006

Abbreviation: CI, confidence interval; Max, maximum.

Table 5. Correlation Coefficients (Pearson) and P Levels of Selected Power Generation Variables and Walking Velocity in the PD Group and the Control Group

NOTE. Values in boldface were statistically significant.

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Discussion 

This study provides detailed information regarding time-distance, kinematic, and kinetic gait parameters in PD subjects off therapy compared with a healthy control group. Because the PD patients were tested in the off phase, gait abnormalities were more pronounced than in a previous study¹⁴ that tested PD patients during the on phase of the medication cycle. Therefore, this study elucidated significant changes in additional time-distance and kinematic variables, which could have been diminished by L-dopa medication in that study.

Time-Distance Parameters 

Our findings are consistent with previous investigations on time-distance variables of parkinsonian gait.⁵, ¹⁴, ²¹ Similar to previous reports, we also did not find any difference in cadence between the PD and control group⁵ and were able to characterize the gait of PD by short steps, lower walking velocity, and relatively high cadence. To diminish the influence of sequence effect on the means of time-distance parameters, only 1 gait cycle with a clear foot force plate contact obtained during the steady-state walking was used to calculate the patient's mean trial. The finding of prolonged double support times in PD patients is in contrast with the findings of Sofuwa et al.¹⁴ This difference might be explained by the fact that Sofuwa et al tested PD patients on dopaminergic therapy, which could have influenced the double-limb support times. Such a hypothesis is supported by the finding of O'Sullivan et al²¹ who measured decreased double-limb support time after L-dopa administration. The increased time spent with both feet on the ground during the gait cycle can be a sign of instability. Postural instability can have a marked impact on the walking pattern of individuals with PD because it compromises their ability to maintain the center of mass above a narrow and constantly shifting base of support.²² Extending the duration of double-limb support times increases the time available for restabilization, thus minimizing the demands on the postural control system.¹³

Lower-Extremity Joint Angles 

In agreement with Morris et al,¹¹ we observed reduced ROM values for all major joints of the lower extremity in the PD group. Our data show a hip extension deficit, decreased knee extension during single stance support, and reduced plantar flexion of the ankle at the toe-off. Importantly, all these changes can contribute to a shortened stride length. Although these findings have been previously described,⁵ Sofuwa¹⁴ did not find any differences in the knee and hip kinematic variables comparing PD patients on therapy with a control group in their recent extensive description of PD gait.¹⁴ As Morris¹¹ described, a strong negative linear relationship was found between the severity of PD and ROM. Thus, we hypothesize that this might be an indicator of the effect of L-dopa medication in PD patients. This view is also supported by an earlier work of Morris et al¹³ in which similar changes of kinematics and ROM data after L-dopa distribution are described in a single-case study.

Kinetics 

Abnormal kinematic gait patterns are reflected in pathologic kinetics. The reduction of the ankle dorsal-flexion moment during loading response is consistent with findings of Sofuwa¹⁴ and was related to a reduced heel rocker. A reduction of the maximum ankle extension moment and of the ankle power generated in the preswing phase of the gait cycle (push-off power) are well described in the literature.⁵, ¹⁴, ²³ Decreased plantar-flexion ROM during push-off also leads to decreased push-off power. The importance of this push-off deficit has been shown by Judge et al,²⁴ who found that the plantar-flexor power generation was the strongest predictor of stride length in elderly subjects. Weakness of plantar-flexor muscles, which show reduced electromyographic activity in PD patients, might be one of the causes of decreased push-off power.²⁵ When weak muscles were addressed by resistance training, strength and gait performance improved in PD patients.²⁶ Another cause of the reduced plantar-flexion power at the ankle could be muscle rigidity, which is a predominant feature of PD.²⁷ Therefore, treatment strategies such as physiotherapy that are able to reduce muscle stiffness and increase plantar-flexor power may be of benefit for PD patients and possibly improve their gait.

At the knee joint, we found a lower power generation during the single stance phase of the gait cycle. This occurs with a limited knee extension during the stance phase of gait. PD patients did not generate sufficient power to extend and thereby passively stabilize the knee as did the control subjects. Decreased power absorption at the knee joint during the late stance and preswing phase could be an effect of the impaired push-off power generation at the ankle.

For the hip kinetics of PD patients, we found a reduction of the maximum extensor moment and a decreased hip power generation in the first double support. Also, the maximum flexor moment and the power generation in the second double support and preswing were reduced. Thereby, the so-called lift-off of the limb into swing phase was impaired. In the presence of an impaired ankle push-off power generation, an increased hip power generation during preswing (lift-off power) would be a feasible compensatory mechanism. In this study, PD patients could not adopt the expected compensation strategy because of their limitation in lift-off power generation at the hip. This finding is similar to a study with PD patients on L-dopa therapy¹⁴ but is in contrast to findings in healthy elderly people in whom increased hip lift-off power was described as a compensation mechanism for the reduced ankle push-off power generation.²⁴ For PD patients in this study, we documented decreased ankle push-off power generation, which strongly correlated with their walking velocity. Hence, ankle push-off power generation remains an important body propulsive mechanism even in PD patients. Although hip lift-off power generation was reduced in the PD group, it was associated with the gait velocity and seems to be an important mechanism of body advancement, especially for PD patients. Judge et al²⁴ described reduced power absorption at the knee during preswing in a group of healthy elderly people. This power absorption is a prerequisite for the transfer of the energy generated at the ankle during push-off to the more proximal body segments.²⁴ In our study, PD patients who maintained this mechanism walked at higher gait velocities.

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Conclusions 

This study describes time distance, kinematic, and kinetic gait characteristics of PD patients off therapy compared with healthy controls. It would be useful in future studies to measure the same subjects under the both on and off medication conditions. Changes observed for time-distance and kinematic parameters confirm the results of previous studies. The reduction of ankle push-off power was shown to be an important mechanism contributing to the decreased walking velocity of PD patients. Also, the expected compensatory propulsive mechanism, the lift-off power of the hip, was found to be lower in the PD patients when compared to a control group. The positive correlation of the lift-off power with the walking velocity underlines the importance of the lift-off to maintain walking velocity. To date, most rehabilitation strategies have focused on visual cues and treadmill walking programs to improve time-distance and kinematic parameters. Our data suggest that resistance training to improve the ankle plantar-flexor strength and hip extensor strength as well as techniques to ameliorate muscle stiffness might be valuable rehabilitation strategies addressing parkinsonian gait disorders.

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• a VICON–UK, 14 Minns Business Park, Wes Way, Oxford OX2 OJB, UK.
• b Advanced Mechanical Technology, Inc, Prophysics AG, Braueraistrasse 10, CH-8610 Uster, Switzerland.
• c Statistica 6.0; StatSoft Inc, 2300 East 14th St, Tulsa, OK 74104.