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Obstacle crossing in Parkinson's disease: Mediolateral sway of the centre of mass during level-ground walking and obstacle crossing
Gait & Posture 38 (2013) 790–794
Contents lists available at SciVerse ScienceDirect
Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost
Obstacle crossing in Parkinson’s disease: Mediolateral sway of the centre of mass during level-ground walking and obstacle crossing Brook Galna a,*, Anna T. Murphy b,c, Meg E. Morris d a
Institute for Ageing and Health, Clinical Ageing Research Unit, Newcastle University, Newcastle Upon Tyne NE4 5PL, United Kingdom Clinical Research Centre for Movement Disorders and Gait, Southern Health Centre, Victoria 3192, Australia c Monash Ageing Research Centre, Monash University, Victoria 3800, Australia d School of Allied Health, Musculoskeletal Research Centre, La Trobe University, Victoria 3084, Australia b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 8 September 2012 Received in revised form 13 February 2013 Accepted 26 March 2013
Background: Falls are common in idiopathic Parkinson’s disease (PD) and frequently occur when walking and crossing obstacles. Objective: To determine whether people with mild to moderately severe PD have abnormal centre of mass (CoM) motion in response to the perturbations of level-ground walking and obstacle crossing. Method: Mediolateral excursion and velocity of the CoM were measured using three-dimensional motion analysis and force platforms in 20 people with mild to moderately severe PD at the peak dose of their PD medication, and 20 age and sex matched healthy control participants. Results: People with PD had greater sideways sway than healthy older adults when walking, particularly when walking over obstacles. People with PD also maintained their CoM more medial to their stance foot throughout the swing phase of gait compared to controls. The severity of motor symptoms in people with PD, measured using the UPDRS-III, was associated with faster sideways CoM motion but not increased CoM excursions. Conclusions: Environmental hazards, such as ground-based obstacles, may accentuate postural instability in people with PD. Increased mediolateral sway might be due to impaired postural responses or kinematic compensations to increase foot clearance. Fall prevention programs could benefit from inclusion of components educating people with PD about the risks associated with obstacle crossing when walking. ß 2013 Elsevier B.V. All rights reserved.
Keywords: Parkinson’s disease Gait Obstacle crossing Centre of mass
1. Introduction Postural instability during level-ground walking and obstacle crossing is common and disabling in people with PD. As well as predisposing people with PD to tripping, it can also be associated with a fear of falling and loss of confidence in walking [1,2]. Falls occur in up to 60% of people with PD [3] and sideways falls are a leading cause of lateral hip fractures in older adults [4]. Sideways falls are also associated with high mortality rates [5]. Investigating mediolateral balance in people with PD is important because evidence from posturography studies indicates that people with moderate-severe PD do not control their balance as well as healthy older adults [6–9]. Several gait studies have shown that people with PD have postural instability during walking and in particular during obstacle crossing [6,10–12]. Parkinson’s disease is associated with
* Corresponding author. Tel.: +44 0191 248 1250; fax: +44 0191 248 1251. E-mail address: [email protected] (B. Galna). 0966-6362/$ – see front matter ß 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.gaitpost.2013.03.024
reduced harmonic ratios of head acceleration during gait, suggesting that people with PD have a less rhythmic gait and less stable gait than unimpaired people of the same age [11]. Adkin et al. [6] also showed that people with moderately severe PD had abnormal trunk sway during a range of clinical and gait tasks. These tasks included self-paced walking, standing up from a chair and responding to a push or pull. Our previous work has shown that people with PD walk slowly with short steps during level-ground walking [13] and obstacle crossing [10]. In one sample people with PD were found to widen their steps and spend more time in double limb support when they were required to walk over an obstacle. These gait changes were argued to be a compensatory mechanism to allow the person to gain greater stability in order to prevent falls [10]. It is unclear how PD affects mediolateral stability of centre of mass (CoM) motion in challenging tasks such as walking over obstacles. It also remains to be seen whether postural abnormalities when walking over obstacles are related to the severity of motor symptoms in people with PD. In line with the findings that PD usually results in a poverty of movement [13,14], this study
B. Galna et al. / Gait & Posture 38 (2013) 790–794
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Fig. 1. Panel A shows the CoM–CoP inclination angle (u) is calculated as the angle defined by the centre of pressure, centre of mass and the projection of the centre of mass on the ground. Panels B and C illustrate example trajectories of CoM velocity and CoM–CoP. Closed circles represent maximums, open circles represent minimums and the open square represents the CoM motion at the time the swing limb foot was above the obstacle. The CoM stays medial to the CoP throughout the entire swing phase (B), with the minimum medial CoM–CoP angle (*) occurring in the first 50% of swing and the peak medial CoM–CoP (*) occurring near then end of the swing phase. Panel B shows that the CoM moves laterally in the first 50% of step duration, towards the stance limb, before moving medially. Peak lateral CoM velocity occurs in the first 25% of the step (*) and peak medial velocity occurs near foot contact (*). Additional discrete outcome measures presented in this study include CoM excursions as well as the position and velocity of the CoM at the time the lead forefoot was above the obstacle (&).
tested the hypothesis that people with PD have reduced and slower mediolateral CoM motion than controls during both level-ground walking and obstacle crossing. It was also hypothesised that increased severity of PD motor symptoms would be associated with reduced speed and size of mediolateral CoM motion during both level-ground walking and obstacle crossing. 2. Methodology 2.1. Participants The participants and testing protocol relevant to this study have been described previously [10]. Twenty people with mild to moderate idiopathic PD and 20 age and sex matched control participants were recruited from a movement disorders clinic in Melbourne, Australia. All participants were screened prior to testing to ensure they did not have any orthopaedic, cardiothoracic or neurological conditions, apart from PD, that would impede their walking or ability to participate in the study safely. A neurologist confirmed their primary diagnosis of idiopathic PD. Because we were primarily interested in the effects of bradykinesia on CoM motion in people with PD, participants who had frequent freezing of gait or dyskinesias were excluded from the study. People with PD were tested at the peak dose of their levodopa medication cycle, as assessed by a physiotherapist with extensive experience with PD. This project was approved by the Southern Health Human Research Ethics Comittee (#60088B) and, consistent with the declaration of Helsinki, all participants signed an informed consent form before testing. 2.2. Procedure Prior to walking, people with PD completed the Mini Mental State Examination [15]. The motor component (part III) of the Unified Parkinson’s Disease Rating Scale was assessed throughout the testing session for participants with PD [16]. Participants were instructed to walk along a 10 m walkway at their preferred pace. For obstacle crossing trials, the starting position was calculated to be 10 steps away from the obstacle, using the average step length from two initial level-ground walking trials. The height of the foam obstacle (600 mm wide 10 mm deep) was adjusted to 10% of leg length (100 mm). Both people with PD and controls were instructed to walk at their preferred pace during testing. Control participants were asked to also complete the walking tasks at the same pace and step length as their matched PD participant. To achieve this, controls practiced walking with horizontal
white cues placed for their initial five steps placed at the criterion step length. They were timed using a stop watch and asked to walk faster or slower to achieve the desired speed. As many practice trials as needed were allowed to familiarise the controls to the matched pace condition. Centre of mass was calculated with a VICON three-dimensional motion analysis system (version 5.1, Oxford), using the built in full body Plug-in-Gait gait model. The CoM was defined as the centroid of the lower limb, pelvis, trunk, head and arm segment masses. Segment proportions and inertial properties were estimated using the cadaver studies [17, p. 60]. Using the centre of pressure (CoP) data from force plates embedded in the walkway, CoM–CoP inclination angles were calculated. The CoM–CoP inclination angle was defined as the angle between the CoP, CoM and projection of the CoM on the floor (Fig. 1, panel A). Excursion of the CoM–CoP inclination angle has previously been used to look at dynamic stability during gait in older adults [18]. The CoM–CoP inclination angle is also potentially a more sensitive measure of postural instability because it accounts for the position of the CoP as well as the height of the CoM [18]. 2.3. Discrete variables of CoM motion For this report, we concentrated on CoM motion during the swing phase of gait, which is defined as the time the foot leaves the ground to the time it contacts the ground again. For obstacle crossing trials, we examined the first step over the obstacle (also known as the lead crossing step). The outcome variables measured in this study include the mediolateral excursions of the CoM, the CoM–CoP inclination angle, and peak medial and lateral velocity of the CoM (Fig. 1, panels B and C). For obstacle crossing trials, the CoM–CoP inclination angle and CoM velocity were also measured in the mid-swing phase, when the meta-tarsal phalangeal joint of the lead foot was directly above the obstacle [10]. 2.4. Data management Four trials were analysed for level-ground walking and eight trials for obstacle crossing (four trials stepping over the obstacle first with the left foot and four trials with the right foot). Outcome variables from left and right strides were averaged. 2.5. Statistical procedures Repeated measures ANOVAs were used to test for Group (Control and PD) and Condition (level-ground walking and obstacle crossing) main effects and interactions. Pearson correlations were used to examine the strength of the linear
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Table 1 Group means (standard deviation) for centre of mass motion, and the correlation between outcome measures and the UPDRS III expressed as Pearson’s r (p value). PD
Variable
Control Preferred
Level ground walking CoM excursion (mm) Inclination angle excursion (8) Peak medial velocity (mm s 1) Peak lateral velocity (mm s 1) Obstacle crossing CoM excursion (mm) Inclination angle excursion (8) Inclination at obstacle crossing (8) Peak medial velocity (mm s 1) Peak lateral velocity (mm s 1) Velocity at obstacle crossing (mm s
1
)
Correlation with UPDRS III Matched
37.0 (10.3) .89 (.41) 90.2 (23.3) 65.3 (23.3)
30.3 (6.3) .96 (.29) 78.6 (20.0) 58.4 (21.6)
33.8 (12.0) 1.03 (.37) 84.9 (33.5) 64.0 (25.8)
.295 .034 .622 .606
(.206) (.888) (.003) (.005)
43.4 (11.3) 1.30 (.55) 3.35 (.58) 93.1 (24.7) 82.6 (28.8) 6.6 (16.0)
36.4 (7.0) 1.10 (.28) 2.96 (.60) 83.3 (18.6) 55.2 (33.0) 14.2 (17.1)
38.0 (11.8) 1.08 (.39) 3.05 (.56) 89.6 (28.6) 64.6 (32.5) 11.1 (12.7)
.290 .403 .077 .519 .316 .047
(.214) (.078) (.748) (.019) (.175) (.843)
relationships between PD motor disability and CoM motion for both level-ground walking and obstacle crossing. For interpretation purposes, alpha was set at .05.
3. Results 3.1. Participants Twenty people with mild to moderate idiopathic PD ((Mean SD) Age: 65.6 7.7 years; Sex: 4 females; Height: 1.69 .08 m; Mass: 76.6 13.0; MMSE: 28.1 1.5) and 20 age and sex matched control participants (Age: 65.3 8.0 years; Sex: 4 females; Height: 1.70 .08 m; Mass: 75.8 11.0) were recruited. Participants had mild to moderately severe PD (Hoehn and Yahr stage: I–III; UPDRS III: 12.6 5.1 (scored on most affected side); Ldopa dose equivalence: 662.5 360 mg).
3.2. Excursions of the CoM and inclination angle Mediolateral motion of the CoM during level-ground walking and obstacle crossing are presented in Table 1 and are illustrated in Fig. 2. For mediolateral excursions, a main effect for group showed that people with PD swayed sideways 21% more than controls walking at their preferred pace (F(1,19) = 8.7, p = .008) but only 12% greater than controls walking at a matched pace (F(1,13) = 2.7, p = .123). A condition main effect indicated people had greater mediolateral sway during obstacle crossing than level-ground walking (F(1,19) = 11.8, p = .003). People with PD did not increase the amount they swayed during obstacle crossing any more than control participants (group condition interaction: F(1,19) = .016, p = .901).
Fig. 2. Group means for centre of mass motion for people with PD (^) and controls walking at their preferred pace (&) and matched pace (~).
B. Galna et al. / Gait & Posture 38 (2013) 790–794
There were no group main effects for mediolateral inclination angles when people with PD were compared to controls walking at their preferred pace (F(1,19) = .852, p = .368) or matched pace (F(1,13) = .128, p = .728). Greater inclination angle excursions were seen during obstacle crossing compared to level-ground walking (F(1,19) = 23.2, p < .001). Interestingly, a group condition interaction showed a greater increase in inclination angle excursions from level-ground walking to obstacle crossing in people with PD compared to controls walking at their preferred (F(1,19) = 12.0, p = .003) and matched pace (F(1,13) = .126, p = .004). When the lead foot was directly above the obstacle, inclination angles were 13% greater in people with PD than controls walking at their preferred pace, indicating people with PD maintained their CoM more medial to their CoP compared to controls, but not at their matched pace (Preferred pace: F (1,19) = 4.9, p = .039; Matched pace: F (1,13) = 1.6, p = .232). 3.3. Centre of mass velocity People with PD swayed laterally faster than controls walking at their preferred pace (F(1,19) = 4.5, p = .046) but not controls walking at a matched pace (F(1,13) = .846, p = .374). A condition main effect also indicated that participants reached faster peak lateral velocities during obstacle crossing compared to levelground walking (F (1,19) = 4.5, p = .048). A group condition interaction showed people with PD swayed faster laterally during obstacle crossing compared to controls walking at their preferred pace yet not for level-ground walking (F (1,19) = 6.201, p = .022). A similar interaction was seen when controls walked at a matched pace but was not statistically significant (F (1,13) = 2.6, p = .132). Peak medial velocity did not differ between people with PD and controls (Preferred pace: F(1,19) = 2.6, p = .122; Matched pace F(1,13) = .177, p = .681), or between level-ground walking and obstacle crossing conditions (F (1,19) = 3.29, p = .085). There was also no group condition interaction for peak medial velocity (Preferred pace: F (1,19) = .137, p = .715; Matched pace F(1,13) = 2.6, p = .132). Mediolateral CoM velocity when the lead foot was above the obstacle was similar between groups regardless of pace (Preferred pace: F(1,19) = 1.8, p = .194; Matched pace: F(1,13) = .129, p = .725). 3.4. Relationship between CoM motion and PD motor disability The strength of relationships between CoM variables and the motor component of the UPDRS is reported in Table 1. There was a moderate and statistically significant positive linear relationship between motor disability and mediolateral sway, whereby those with more severe motor symptoms swayed faster. Faster medial sway was also related to more severe motor disability when the lead forefoot was directly above the obstacle. Neither excursions of the CoM nor inclination angle during level-ground walking or obstacle crossing were related to severity of motor disability. Although more severe motor disability was related to greater inclination angle excursions during obstacle crossing, this finding was not statistically significant (r = .408, p = .078). 4. Discussion Although poverty of movement is a hallmark symptom of PD, this study showed that some people with PD walk with greater and faster mediolateral sway than control participants, especially when walking over obstacles. Although contrary to our original hypothesis, this finding is consistent with previous studies that have shown disturbed balance in people with PD in standing [6,19]
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and during gait [6,11,12]. Increased speed and sway of CoM motion during obstacle crossing may reflect a compensation made by some people with PD to improve their foot clearance during obstacle crossing. Our previous work has shown that some people with PD use a pelvis hiking strategy to increase foot clearance during obstacle crossing to compensate for a more flexed ankle and knee during of the stance limb [20]. It is possible that adopting a pelvis hiking strategy leads to increased trunk sway and therefore increases the amplitude of their mediolateral CoM motion. Mediolateral motion of the CoM did not differ between people with PD and control participants when walking at the same speed and step length. A recent study of healthy adults has shown that mediolateral excursion of the centre of mass is larger when walking more slowly [21]. The same phenomenon was seen in this study, with controls slightly increasing their mediolateral CoM sway when walking as slow as those with PD. Despite matching speed and step length, PD participants still tended to have a larger and faster mediolateral CoM motion than controls. This may reflect that the basic pattern of CoM sway is not affected by people with PD, rather it is a problem of scaling and walking speed consistent with what has been observed during the lower limb kinematics of level-ground walking in people with PD [14]. People with PD maintained their CoM more medial to their CoP compared to controls when their lead limb was crossing over the obstacle. This may be a compensation to reduce the risk of having a lateral fall. This strategy, however, also places those with PD at greater risk of falling medially, especially if their foot was to contact the obstacle, rendering them unable to place that foot to the side they are falling. People with PD with more severe motor disability demonstrated greater postural instability, as shown by faster peak lateral velocities during level-ground walking and obstacle crossing, as well as faster peak medial velocity during level-ground walking. This is in agreement with Blaszczyk et al. [19] who reported a moderate linear relationship between greater mediolateral sway during quiet stance and more severe PD symptoms. It has previously been shown that the postural responses of people with PD are slower and under scaled when perturbed from a standing position [22], and that these responses worsen with the progression of the disease [23]. Similarly, faster CoM sway in people with PD who have more severe motor symptoms might be the result of reduced postural responses to perturbations acting during levelground walking and obstacle crossing. Whereas levodopa medication is frequently prescribed to improve motor function in people with PD, there is emerging evidence that postural stability does not improve with medication alone [24]. Several physiotherapy interventions are available to improve gait impairments [25]. It is plausible that these interventions might also improve postural stability during obstacle crossing. They include strengthening, teaching people with PD to use cueing strategies and aerobic exercises [26,27]. Treadmill based virtual reality training can also improve obstacle crossing in people with PD [28]. However, auditory cueing strategies that involve listening to music whilst walking have been seen to impair obstacle crossing in some people with PD in single session studies, however the longer terms effects are still unclear [29]. The ability to generalise the findings of this study to the broader population with PD is somewhat limited due to the modest sample size and the exclusion of people with frequent freezing of gait and severe dyskinesia. Recent studies have examined the phenomena of freezing of gait in relation to treadmill walking [30], yet the effects of dyskinesia in people with PD on obstacle crossing have not been investigated. Future research is also needed to examine underlying mechanisms of increased amplitude and speed of mediolateral CoM sway in people with PD.
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5. Conclusion Some people with mild to moderate PD sway sideways abnormally far and fast when walking, which is exaggerated when crossing obstacles. Increasing motor disability is also related to faster sideways sway during gait. Abnormal mediolateral CoM sway when walking might reflect a poverty of postural responses or possibly a compensatory kinematic strategy used by people with PD to maintain a safe foot clearance. Understanding the kinematic and neural underpinnings of abnormal postural control in PD will help therapists better target interventions to reduce slips, trips and falls. Acknowledgements We wish to acknowledge the National Health and Medical Research Council of Australia #466630, the Melbourne Physiotherapy School and the Lions Club of Australia for their financial support; Southern Health for access to their testing facilities; and Dr. Ernie Butler for his assistance in recruitment. Conflict of interest None of the authors have conflicts of interest to declare. References [1] Lamont RM, Morris ME, Woollacott MH, Brauer SG. Community walking in people with Parkinson’s disease. Parkinson’s Disease 2012;2012:856237. [2] Stolze H, Klebe S, Zechlin C, Baecker C, Friege L, Deuschl G. Falls in frequent neurological diseases—prevalence, risk factors and aetiology. Journal of Neurology 2004;251(1):79–84. [3] Pickering RM, Grimbergen YAM, Rigney U, Ashburn A, Mazibrada G, Wood B, et al. A meta-analysis of six prospective studies of falling in Parkinson’s disease. Movement Disorders 2007;22(13):1892–900. [4] Greenspan SL, Myers ER, Kiel DP, Parker RA, Hayes WC, Resnick NM. Fall direction, bone mineral density, and function: risk factors for hip fracture in frail nursing home elderly. American Journal of Medicine 1998;104(6):539–45. [5] Resnick NM, Greenspan SL. Senile osteoporosis reconsidered. JAMA – Journal of the American Medical Association 1989;261(7):1025–9. [6] Adkin AL, Bloem BR, Allum JHJ. Trunk sway measurements during stance and gait tasks in Parkinson’s disease. Gait & Posture 2005;22(3):240–9. [7] Horak FB, Nutt JG, Nashner LM. Postural Inflexibility in Parkinsonian subjects. Journal of the Neurological Sciences 1992;111(1):46–58. [8] Mitchell S, Collins JJ, Deluca CJ, Burrows A, Lipsitz LA. Open-loop and closed-loop postural control mechanisms in parkinsons-disease—increased mediolateral activity during quiet standing. Neuroscience Letters 1995;197(2):133–6. [9] Nardone A, Schieppati M. Balance in Parkinson’s disease under static and dynamic conditions. Movement Disorders 2006;21(9):1515–20. [10] Galna B, Murphy AT, Morris ME. Obstacle crossing in people with Parkinson’s disease: foot clearance and spatiotemporal deficits. Human Movement Science 2010;29(5):843–52.
[11] Latt MD, Menz HB, Fung VS, Lord SR. Acceleration patterns of the head and pelvis during gait in older people with Parkinson’s disease: a comparison of fallers and nonfallers. Journals of Gerontology Series A Biological Sciences and Medical Sciences 2009;64(6):700–6. [12] Stegemoller EL, Buckley TA, Pitsikoulis C, Barthelemy E, Roemmich R, Hass CJ. Postural instability and gait impairment during obstacle crossing in Parkinson’s disease. Archives of Physical Medicine and Rehabilitation 2012;93(4): 703–9. [13] Morris ME, Iansek R, Matyas TA, Summers JJ. The pathogenesis of gait hypokinesia in Parkinson’s disease. Brain 1994;117(Pt 5):1169–81. [14] Morris M, Iansek R, McGinley J, Matyas T, Huxham F. Three-dimensional gait biomechanics in Parkinson’s disease: evidence for a centrally mediated amplitude regulation disorder. Movement Disorders 2005;20(1):40–50. [15] Folstein m, Folstein S, McHugh P. Mini-mental state. A practical method for grading the congitive state of patients for the clinician. Journal of Psychiatric Research 1975;12:189–98. [16] Fahn S, Elton R, M.o.t.U.d. committee. Unified Parkinson’s disease rating scale. In: Fahn MC, Calne S, Goldstein DBM, editors. Recent developments in Parkinson’s disease. Florham Park, NJ: MacMillan Healthcare Information; 1987. p. 153–63. [17] Winter DA. Biomechanics and the motor control of human movement. 3 ed. Hoboken, New Jersey: Wiley & Sons; 2005. [18] Huang SC, Lu TW, Chen HL, Wang TM, Chou LS. Age and height effects on the center of mass and center of pressure inclination angles during obstaclecrossing. Medical Engineering & Physics 2008;30(8):968–75. [19] Blaszczyk JW, Orawiec R, Duda-Kiodowska D, Opala G. Assessment of postural instability in patients with Parkinson’s disease. Experimental Brain Research 2007;183(1):107–14. [20] Galna B, Murphy A, Morris M. Lower limb kinematics during obstacle crossing in people with Parkinson’s disease. In: 19th international conference of the international society of posture and gait research; 2009. [21] Tesio L, Rota V, Chessa C, Perucca L. The 3D path of the centre of mass during adult human walking on a force treadmill. Journal of Biomechanics 2010; 5:938–44. [22] Horak FB, Dimitrova D, Nutt JG. Direction-specific postural instability in subjects with Parkinson’s disease. Experimental Neurology 2005;193(2): 504–21. [23] Mancini M, Carlson-Kuhta P, Zampieri C, Nutt JG, Chiari L, Horak FB. Postural sway as a marker of progression in Parkinson’s disease: a pilot longitudinal study. Gait & Posture 2012;36(3):471–6. [24] Benatru I, Vaugoyeau M, Azulay JP. Postural disorders in Parkinson’s disease. Neurophysiologie Clinique-Clinical Neurophysiology 2008;38(6):459–65. [25] Proud EL, Morris ME. Skilled hand dexterity in Parkinson’s disease: effects of adding a concurrent task. Archives of Physical Medicine and Rehabilitation 2010;91(5):794–9. [26] Morris ME. Preventing falls in older people. British Medical Journal 2012;345. [27] Morris ME, Martin CL, Schenkman ML. Striding out with Parkinson disease: evidence-based physical therapy for gait disorders. Physical Therapy 2010; 90(2):280–8. [28] Mirelman A, Maidan I, Herman T, Deutsch JE, Giladi N, Hausdorff JM. Virtual reality for gait training: can it induce motor learning to enhance complex walking and reduce fall risk in patients with Parkinson’s disease? Journals of Gerontology Series A Biological Sciences and Medical Sciences 2011;66(2): 234–40. [29] Brown LA, de Bruin N, Doan J, Suchowersky O, Hu B. Obstacle crossing among people with Parkinson disease is influenced by concurrent music. Journal of Rehabilitation Research and Development 2010;47(3):225–31. [30] Nanhoe-Mahabier W, Delval A, Snijders AH, Weerdesteyn V, Overeem S, Bloem BR. The possible price of auditory cueing: influence on obstacle avoidance in Parkinson’s disease. Movement Disorders 2012;27(4):574–8.
Contents lists available at SciVerse ScienceDirect
Gait & Posture journal homepage: www.elsevier.com/locate/gaitpost
Obstacle crossing in Parkinson’s disease: Mediolateral sway of the centre of mass during level-ground walking and obstacle crossing Brook Galna a,*, Anna T. Murphy b,c, Meg E. Morris d a
Institute for Ageing and Health, Clinical Ageing Research Unit, Newcastle University, Newcastle Upon Tyne NE4 5PL, United Kingdom Clinical Research Centre for Movement Disorders and Gait, Southern Health Centre, Victoria 3192, Australia c Monash Ageing Research Centre, Monash University, Victoria 3800, Australia d School of Allied Health, Musculoskeletal Research Centre, La Trobe University, Victoria 3084, Australia b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 8 September 2012 Received in revised form 13 February 2013 Accepted 26 March 2013
Background: Falls are common in idiopathic Parkinson’s disease (PD) and frequently occur when walking and crossing obstacles. Objective: To determine whether people with mild to moderately severe PD have abnormal centre of mass (CoM) motion in response to the perturbations of level-ground walking and obstacle crossing. Method: Mediolateral excursion and velocity of the CoM were measured using three-dimensional motion analysis and force platforms in 20 people with mild to moderately severe PD at the peak dose of their PD medication, and 20 age and sex matched healthy control participants. Results: People with PD had greater sideways sway than healthy older adults when walking, particularly when walking over obstacles. People with PD also maintained their CoM more medial to their stance foot throughout the swing phase of gait compared to controls. The severity of motor symptoms in people with PD, measured using the UPDRS-III, was associated with faster sideways CoM motion but not increased CoM excursions. Conclusions: Environmental hazards, such as ground-based obstacles, may accentuate postural instability in people with PD. Increased mediolateral sway might be due to impaired postural responses or kinematic compensations to increase foot clearance. Fall prevention programs could benefit from inclusion of components educating people with PD about the risks associated with obstacle crossing when walking. ß 2013 Elsevier B.V. All rights reserved.
Keywords: Parkinson’s disease Gait Obstacle crossing Centre of mass
1. Introduction Postural instability during level-ground walking and obstacle crossing is common and disabling in people with PD. As well as predisposing people with PD to tripping, it can also be associated with a fear of falling and loss of confidence in walking [1,2]. Falls occur in up to 60% of people with PD [3] and sideways falls are a leading cause of lateral hip fractures in older adults [4]. Sideways falls are also associated with high mortality rates [5]. Investigating mediolateral balance in people with PD is important because evidence from posturography studies indicates that people with moderate-severe PD do not control their balance as well as healthy older adults [6–9]. Several gait studies have shown that people with PD have postural instability during walking and in particular during obstacle crossing [6,10–12]. Parkinson’s disease is associated with
* Corresponding author. Tel.: +44 0191 248 1250; fax: +44 0191 248 1251. E-mail address: [email protected] (B. Galna). 0966-6362/$ – see front matter ß 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.gaitpost.2013.03.024
reduced harmonic ratios of head acceleration during gait, suggesting that people with PD have a less rhythmic gait and less stable gait than unimpaired people of the same age [11]. Adkin et al. [6] also showed that people with moderately severe PD had abnormal trunk sway during a range of clinical and gait tasks. These tasks included self-paced walking, standing up from a chair and responding to a push or pull. Our previous work has shown that people with PD walk slowly with short steps during level-ground walking [13] and obstacle crossing [10]. In one sample people with PD were found to widen their steps and spend more time in double limb support when they were required to walk over an obstacle. These gait changes were argued to be a compensatory mechanism to allow the person to gain greater stability in order to prevent falls [10]. It is unclear how PD affects mediolateral stability of centre of mass (CoM) motion in challenging tasks such as walking over obstacles. It also remains to be seen whether postural abnormalities when walking over obstacles are related to the severity of motor symptoms in people with PD. In line with the findings that PD usually results in a poverty of movement [13,14], this study
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Fig. 1. Panel A shows the CoM–CoP inclination angle (u) is calculated as the angle defined by the centre of pressure, centre of mass and the projection of the centre of mass on the ground. Panels B and C illustrate example trajectories of CoM velocity and CoM–CoP. Closed circles represent maximums, open circles represent minimums and the open square represents the CoM motion at the time the swing limb foot was above the obstacle. The CoM stays medial to the CoP throughout the entire swing phase (B), with the minimum medial CoM–CoP angle (*) occurring in the first 50% of swing and the peak medial CoM–CoP (*) occurring near then end of the swing phase. Panel B shows that the CoM moves laterally in the first 50% of step duration, towards the stance limb, before moving medially. Peak lateral CoM velocity occurs in the first 25% of the step (*) and peak medial velocity occurs near foot contact (*). Additional discrete outcome measures presented in this study include CoM excursions as well as the position and velocity of the CoM at the time the lead forefoot was above the obstacle (&).
tested the hypothesis that people with PD have reduced and slower mediolateral CoM motion than controls during both level-ground walking and obstacle crossing. It was also hypothesised that increased severity of PD motor symptoms would be associated with reduced speed and size of mediolateral CoM motion during both level-ground walking and obstacle crossing. 2. Methodology 2.1. Participants The participants and testing protocol relevant to this study have been described previously [10]. Twenty people with mild to moderate idiopathic PD and 20 age and sex matched control participants were recruited from a movement disorders clinic in Melbourne, Australia. All participants were screened prior to testing to ensure they did not have any orthopaedic, cardiothoracic or neurological conditions, apart from PD, that would impede their walking or ability to participate in the study safely. A neurologist confirmed their primary diagnosis of idiopathic PD. Because we were primarily interested in the effects of bradykinesia on CoM motion in people with PD, participants who had frequent freezing of gait or dyskinesias were excluded from the study. People with PD were tested at the peak dose of their levodopa medication cycle, as assessed by a physiotherapist with extensive experience with PD. This project was approved by the Southern Health Human Research Ethics Comittee (#60088B) and, consistent with the declaration of Helsinki, all participants signed an informed consent form before testing. 2.2. Procedure Prior to walking, people with PD completed the Mini Mental State Examination [15]. The motor component (part III) of the Unified Parkinson’s Disease Rating Scale was assessed throughout the testing session for participants with PD [16]. Participants were instructed to walk along a 10 m walkway at their preferred pace. For obstacle crossing trials, the starting position was calculated to be 10 steps away from the obstacle, using the average step length from two initial level-ground walking trials. The height of the foam obstacle (600 mm wide 10 mm deep) was adjusted to 10% of leg length (100 mm). Both people with PD and controls were instructed to walk at their preferred pace during testing. Control participants were asked to also complete the walking tasks at the same pace and step length as their matched PD participant. To achieve this, controls practiced walking with horizontal
white cues placed for their initial five steps placed at the criterion step length. They were timed using a stop watch and asked to walk faster or slower to achieve the desired speed. As many practice trials as needed were allowed to familiarise the controls to the matched pace condition. Centre of mass was calculated with a VICON three-dimensional motion analysis system (version 5.1, Oxford), using the built in full body Plug-in-Gait gait model. The CoM was defined as the centroid of the lower limb, pelvis, trunk, head and arm segment masses. Segment proportions and inertial properties were estimated using the cadaver studies [17, p. 60]. Using the centre of pressure (CoP) data from force plates embedded in the walkway, CoM–CoP inclination angles were calculated. The CoM–CoP inclination angle was defined as the angle between the CoP, CoM and projection of the CoM on the floor (Fig. 1, panel A). Excursion of the CoM–CoP inclination angle has previously been used to look at dynamic stability during gait in older adults [18]. The CoM–CoP inclination angle is also potentially a more sensitive measure of postural instability because it accounts for the position of the CoP as well as the height of the CoM [18]. 2.3. Discrete variables of CoM motion For this report, we concentrated on CoM motion during the swing phase of gait, which is defined as the time the foot leaves the ground to the time it contacts the ground again. For obstacle crossing trials, we examined the first step over the obstacle (also known as the lead crossing step). The outcome variables measured in this study include the mediolateral excursions of the CoM, the CoM–CoP inclination angle, and peak medial and lateral velocity of the CoM (Fig. 1, panels B and C). For obstacle crossing trials, the CoM–CoP inclination angle and CoM velocity were also measured in the mid-swing phase, when the meta-tarsal phalangeal joint of the lead foot was directly above the obstacle [10]. 2.4. Data management Four trials were analysed for level-ground walking and eight trials for obstacle crossing (four trials stepping over the obstacle first with the left foot and four trials with the right foot). Outcome variables from left and right strides were averaged. 2.5. Statistical procedures Repeated measures ANOVAs were used to test for Group (Control and PD) and Condition (level-ground walking and obstacle crossing) main effects and interactions. Pearson correlations were used to examine the strength of the linear
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Table 1 Group means (standard deviation) for centre of mass motion, and the correlation between outcome measures and the UPDRS III expressed as Pearson’s r (p value). PD
Variable
Control Preferred
Level ground walking CoM excursion (mm) Inclination angle excursion (8) Peak medial velocity (mm s 1) Peak lateral velocity (mm s 1) Obstacle crossing CoM excursion (mm) Inclination angle excursion (8) Inclination at obstacle crossing (8) Peak medial velocity (mm s 1) Peak lateral velocity (mm s 1) Velocity at obstacle crossing (mm s
1
)
Correlation with UPDRS III Matched
37.0 (10.3) .89 (.41) 90.2 (23.3) 65.3 (23.3)
30.3 (6.3) .96 (.29) 78.6 (20.0) 58.4 (21.6)
33.8 (12.0) 1.03 (.37) 84.9 (33.5) 64.0 (25.8)
.295 .034 .622 .606
(.206) (.888) (.003) (.005)
43.4 (11.3) 1.30 (.55) 3.35 (.58) 93.1 (24.7) 82.6 (28.8) 6.6 (16.0)
36.4 (7.0) 1.10 (.28) 2.96 (.60) 83.3 (18.6) 55.2 (33.0) 14.2 (17.1)
38.0 (11.8) 1.08 (.39) 3.05 (.56) 89.6 (28.6) 64.6 (32.5) 11.1 (12.7)
.290 .403 .077 .519 .316 .047
(.214) (.078) (.748) (.019) (.175) (.843)
relationships between PD motor disability and CoM motion for both level-ground walking and obstacle crossing. For interpretation purposes, alpha was set at .05.
3. Results 3.1. Participants Twenty people with mild to moderate idiopathic PD ((Mean SD) Age: 65.6 7.7 years; Sex: 4 females; Height: 1.69 .08 m; Mass: 76.6 13.0; MMSE: 28.1 1.5) and 20 age and sex matched control participants (Age: 65.3 8.0 years; Sex: 4 females; Height: 1.70 .08 m; Mass: 75.8 11.0) were recruited. Participants had mild to moderately severe PD (Hoehn and Yahr stage: I–III; UPDRS III: 12.6 5.1 (scored on most affected side); Ldopa dose equivalence: 662.5 360 mg).
3.2. Excursions of the CoM and inclination angle Mediolateral motion of the CoM during level-ground walking and obstacle crossing are presented in Table 1 and are illustrated in Fig. 2. For mediolateral excursions, a main effect for group showed that people with PD swayed sideways 21% more than controls walking at their preferred pace (F(1,19) = 8.7, p = .008) but only 12% greater than controls walking at a matched pace (F(1,13) = 2.7, p = .123). A condition main effect indicated people had greater mediolateral sway during obstacle crossing than level-ground walking (F(1,19) = 11.8, p = .003). People with PD did not increase the amount they swayed during obstacle crossing any more than control participants (group condition interaction: F(1,19) = .016, p = .901).
Fig. 2. Group means for centre of mass motion for people with PD (^) and controls walking at their preferred pace (&) and matched pace (~).
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There were no group main effects for mediolateral inclination angles when people with PD were compared to controls walking at their preferred pace (F(1,19) = .852, p = .368) or matched pace (F(1,13) = .128, p = .728). Greater inclination angle excursions were seen during obstacle crossing compared to level-ground walking (F(1,19) = 23.2, p < .001). Interestingly, a group condition interaction showed a greater increase in inclination angle excursions from level-ground walking to obstacle crossing in people with PD compared to controls walking at their preferred (F(1,19) = 12.0, p = .003) and matched pace (F(1,13) = .126, p = .004). When the lead foot was directly above the obstacle, inclination angles were 13% greater in people with PD than controls walking at their preferred pace, indicating people with PD maintained their CoM more medial to their CoP compared to controls, but not at their matched pace (Preferred pace: F (1,19) = 4.9, p = .039; Matched pace: F (1,13) = 1.6, p = .232). 3.3. Centre of mass velocity People with PD swayed laterally faster than controls walking at their preferred pace (F(1,19) = 4.5, p = .046) but not controls walking at a matched pace (F(1,13) = .846, p = .374). A condition main effect also indicated that participants reached faster peak lateral velocities during obstacle crossing compared to levelground walking (F (1,19) = 4.5, p = .048). A group condition interaction showed people with PD swayed faster laterally during obstacle crossing compared to controls walking at their preferred pace yet not for level-ground walking (F (1,19) = 6.201, p = .022). A similar interaction was seen when controls walked at a matched pace but was not statistically significant (F (1,13) = 2.6, p = .132). Peak medial velocity did not differ between people with PD and controls (Preferred pace: F(1,19) = 2.6, p = .122; Matched pace F(1,13) = .177, p = .681), or between level-ground walking and obstacle crossing conditions (F (1,19) = 3.29, p = .085). There was also no group condition interaction for peak medial velocity (Preferred pace: F (1,19) = .137, p = .715; Matched pace F(1,13) = 2.6, p = .132). Mediolateral CoM velocity when the lead foot was above the obstacle was similar between groups regardless of pace (Preferred pace: F(1,19) = 1.8, p = .194; Matched pace: F(1,13) = .129, p = .725). 3.4. Relationship between CoM motion and PD motor disability The strength of relationships between CoM variables and the motor component of the UPDRS is reported in Table 1. There was a moderate and statistically significant positive linear relationship between motor disability and mediolateral sway, whereby those with more severe motor symptoms swayed faster. Faster medial sway was also related to more severe motor disability when the lead forefoot was directly above the obstacle. Neither excursions of the CoM nor inclination angle during level-ground walking or obstacle crossing were related to severity of motor disability. Although more severe motor disability was related to greater inclination angle excursions during obstacle crossing, this finding was not statistically significant (r = .408, p = .078). 4. Discussion Although poverty of movement is a hallmark symptom of PD, this study showed that some people with PD walk with greater and faster mediolateral sway than control participants, especially when walking over obstacles. Although contrary to our original hypothesis, this finding is consistent with previous studies that have shown disturbed balance in people with PD in standing [6,19]
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and during gait [6,11,12]. Increased speed and sway of CoM motion during obstacle crossing may reflect a compensation made by some people with PD to improve their foot clearance during obstacle crossing. Our previous work has shown that some people with PD use a pelvis hiking strategy to increase foot clearance during obstacle crossing to compensate for a more flexed ankle and knee during of the stance limb [20]. It is possible that adopting a pelvis hiking strategy leads to increased trunk sway and therefore increases the amplitude of their mediolateral CoM motion. Mediolateral motion of the CoM did not differ between people with PD and control participants when walking at the same speed and step length. A recent study of healthy adults has shown that mediolateral excursion of the centre of mass is larger when walking more slowly [21]. The same phenomenon was seen in this study, with controls slightly increasing their mediolateral CoM sway when walking as slow as those with PD. Despite matching speed and step length, PD participants still tended to have a larger and faster mediolateral CoM motion than controls. This may reflect that the basic pattern of CoM sway is not affected by people with PD, rather it is a problem of scaling and walking speed consistent with what has been observed during the lower limb kinematics of level-ground walking in people with PD [14]. People with PD maintained their CoM more medial to their CoP compared to controls when their lead limb was crossing over the obstacle. This may be a compensation to reduce the risk of having a lateral fall. This strategy, however, also places those with PD at greater risk of falling medially, especially if their foot was to contact the obstacle, rendering them unable to place that foot to the side they are falling. People with PD with more severe motor disability demonstrated greater postural instability, as shown by faster peak lateral velocities during level-ground walking and obstacle crossing, as well as faster peak medial velocity during level-ground walking. This is in agreement with Blaszczyk et al. [19] who reported a moderate linear relationship between greater mediolateral sway during quiet stance and more severe PD symptoms. It has previously been shown that the postural responses of people with PD are slower and under scaled when perturbed from a standing position [22], and that these responses worsen with the progression of the disease [23]. Similarly, faster CoM sway in people with PD who have more severe motor symptoms might be the result of reduced postural responses to perturbations acting during levelground walking and obstacle crossing. Whereas levodopa medication is frequently prescribed to improve motor function in people with PD, there is emerging evidence that postural stability does not improve with medication alone [24]. Several physiotherapy interventions are available to improve gait impairments [25]. It is plausible that these interventions might also improve postural stability during obstacle crossing. They include strengthening, teaching people with PD to use cueing strategies and aerobic exercises [26,27]. Treadmill based virtual reality training can also improve obstacle crossing in people with PD [28]. However, auditory cueing strategies that involve listening to music whilst walking have been seen to impair obstacle crossing in some people with PD in single session studies, however the longer terms effects are still unclear [29]. The ability to generalise the findings of this study to the broader population with PD is somewhat limited due to the modest sample size and the exclusion of people with frequent freezing of gait and severe dyskinesia. Recent studies have examined the phenomena of freezing of gait in relation to treadmill walking [30], yet the effects of dyskinesia in people with PD on obstacle crossing have not been investigated. Future research is also needed to examine underlying mechanisms of increased amplitude and speed of mediolateral CoM sway in people with PD.
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5. Conclusion Some people with mild to moderate PD sway sideways abnormally far and fast when walking, which is exaggerated when crossing obstacles. Increasing motor disability is also related to faster sideways sway during gait. Abnormal mediolateral CoM sway when walking might reflect a poverty of postural responses or possibly a compensatory kinematic strategy used by people with PD to maintain a safe foot clearance. Understanding the kinematic and neural underpinnings of abnormal postural control in PD will help therapists better target interventions to reduce slips, trips and falls. Acknowledgements We wish to acknowledge the National Health and Medical Research Council of Australia #466630, the Melbourne Physiotherapy School and the Lions Club of Australia for their financial support; Southern Health for access to their testing facilities; and Dr. Ernie Butler for his assistance in recruitment. Conflict of interest None of the authors have conflicts of interest to declare. References [1] Lamont RM, Morris ME, Woollacott MH, Brauer SG. Community walking in people with Parkinson’s disease. Parkinson’s Disease 2012;2012:856237. [2] Stolze H, Klebe S, Zechlin C, Baecker C, Friege L, Deuschl G. Falls in frequent neurological diseases—prevalence, risk factors and aetiology. Journal of Neurology 2004;251(1):79–84. [3] Pickering RM, Grimbergen YAM, Rigney U, Ashburn A, Mazibrada G, Wood B, et al. A meta-analysis of six prospective studies of falling in Parkinson’s disease. Movement Disorders 2007;22(13):1892–900. [4] Greenspan SL, Myers ER, Kiel DP, Parker RA, Hayes WC, Resnick NM. Fall direction, bone mineral density, and function: risk factors for hip fracture in frail nursing home elderly. American Journal of Medicine 1998;104(6):539–45. [5] Resnick NM, Greenspan SL. Senile osteoporosis reconsidered. JAMA – Journal of the American Medical Association 1989;261(7):1025–9. [6] Adkin AL, Bloem BR, Allum JHJ. Trunk sway measurements during stance and gait tasks in Parkinson’s disease. Gait & Posture 2005;22(3):240–9. [7] Horak FB, Nutt JG, Nashner LM. Postural Inflexibility in Parkinsonian subjects. Journal of the Neurological Sciences 1992;111(1):46–58. [8] Mitchell S, Collins JJ, Deluca CJ, Burrows A, Lipsitz LA. Open-loop and closed-loop postural control mechanisms in parkinsons-disease—increased mediolateral activity during quiet standing. Neuroscience Letters 1995;197(2):133–6. [9] Nardone A, Schieppati M. Balance in Parkinson’s disease under static and dynamic conditions. Movement Disorders 2006;21(9):1515–20. [10] Galna B, Murphy AT, Morris ME. Obstacle crossing in people with Parkinson’s disease: foot clearance and spatiotemporal deficits. Human Movement Science 2010;29(5):843–52.
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