Human Movement Science 29 (2010) 843–852

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Human Movement Science

journal homepage: www.elsevier .com/locate/humov

Obstacle crossing in people with Parkinson’s disease: Footclearance and spatiotemporal deficits

Brook Galna a,b,*, Anna T. Murphy b,c, Meg E. Morris a

a School of Physiotherapy, The University of Melbourne, Victoria 3010, Australiab Clinical Research Centre for Movement Disorders and Gait, Southern Health Centre, Victoria 3192, Australiac Monash Ageing Research Centre, Monash University, Victoria 3800, Australia

a r t i c l e i n f o

Article history:Available online 3 December 2009

PsycINFO classification:23303297

Keywords:Parkinson’s diseaseGaitObstacle crossingAccidental falls

0167-9457/$ - see front matter � 2009 Elsevier B.doi:10.1016/j.humov.2009.09.006

* Corresponding author. Address: School of Phys8344 0486; fax: +613 8344 4188.

E-mail address: b.galna@pgrad.unimelb.edu.au

a b s t r a c t

This study investigates the effects of Parkinson’s disease (PD) on foottrajectories and spatiotemporal gait adaptations when approachingand stepping over a ground-based obstacle. Twenty people withmild-moderate PD and 20 age and sex matched controls walked 10steps at their preferred speed along a walkway and stepped overan obstacle (height 10% of leg length � 600 mm � 10 mm). Controlparticipants also performed trials at the same speed and step lengthas their matched PD participant. People with PD approached andstepped over the obstacle slower and with smaller steps, but had asimilar foot clearance. Those with PD were also more likely to stepon the obstacle because they did not place their foot close enoughto the front of the obstacle before crossing it to accommodate fortheir reduced step length. During the lead limb crossing step, peoplewith PD increased their step width, whereas controls maintained anarrow step width. These findings indicate that people with PD havedifficulty lengthening their step over the obstacle rather thanincreasing foot height. Increasing step width is a possible compensa-tion strategy used to overcome postural instability during obstaclecrossing in those with PD.

� 2009 Elsevier B.V. All rights reserved.

1. Introduction

The ability to make gait adjustments to safely clear obstacles at home and in the community, suchas rugs, shower recesses, and roadside curbs, is thought to be compromised in many people with

V. All rights reserved.

iotherapy, The University of Melbourne, Victoria 3010, Australia. Tel.: +613

(B. Galna).

844 B. Galna et al. / Human Movement Science 29 (2010) 843–852

Parkinson’s disease (PD). This study examines foot clearance and spatiotemporal characteristics ofobstacle crossing in people with PD compared with age and sex matched controls. A prospective fallsstudy found that 62% of people with PD fell within a 100 day period (Stolze et al., 2004). Tripping overobstacles was the cause of nearly a third of these falls. It is plausible that obstacle crossing deficits pre-dispose people with PD to a greater risk of trips and falls. By describing obstacle crossing deficits inpeople with PD, this study will identify key variables to guide clinical assessment of obstacle crossingin people with PD. Identifying key deficits will also provide a foundation to explore the biomechanicaland neural mechanisms for obstacle crossing deficits.

Hypokinesia is a hallmark of PD (Morris, Huxham, McGinley, Dodd, & Iansek, 2001; Morris, Iansek,McGinley, Matyas, & Huxham, 2005), although it is unclear how PD affects obstacle crossing. Reducedamplitude of foot trajectories over the obstacle may increase the risk of tripping. Placing the trail foottoo close to the obstacle prior to stepping over it may result in lower trail limb clearance (Chou &Draganich, 1998), while placing the trail foot too far from the obstacle may lead to stepping on theobstacle with the lead heel.

Three experiments have previously reported foot clearance difficulties during obstacle crossing inpeople with PD. Two treadmill studies compared obstacle crossing in people with PD and unimpairedparticipants (Dietz & Michel, 2008; van Hedel, Waldvogel, & Dietz, 2006). Participants were asked toguide their foot as close to the top of the obstacle as possible without touching it. Those with PD hadhigher lead foot clearances, however performance might differ when participants have no specificinstructions on how to guide their foot over the obstacle. A pilot study of obstacle crossing in five peo-ple with mild to moderate PD reported an increased lead foot clearance when participants were onlevo-dopa medication compared to off levo-dopa medication (Pieruccini-Faria et al., 2006). Lead footplacement after the obstacle was not affected by medication status. As there was no control group, theeffects of PD could not be interpreted from the results. The current study is the first to compare obsta-cle crossing in people with PD and a control group when the obstacle crossing task is not constrainedby a treadmill or by specific instructions to modify foot clearance.

The primary aim is to examine whether lead and trail foot clearance are underscaled in people withPD when walking over a ground-based obstacle. Foot placement is investigated before and after obsta-cle crossing. We tested the hypothesis that people with PD have a reduced foot clearance over theobstacle compared to controls.

A further aim was to examine how people with PD adapt their spatiotemporal characteristics ofgait when approaching and stepping over an obstacle. This is important because the strategies peoplewith PD use to walk over obstacles may affect safety. It has been previously shown that shorteningstep length in front of the obstacle prior to crossing can lead to falls in older adults (Chen, Ashtonm-iller, Alexander, & Schultz, 1994). Our hypothesis was that people with PD would walk with smallerand slower steps compared with controls walking at their preferred speed, and use similar step strat-egies regardless of walking speed. To test this, we compared people with PD to controls walking attheir preferred pace as well as controls walking at a matched speed and step length.

In addition to step length adaptations, we investigated whether people with PD had postural insta-bility during obstacle crossing. Postural instability was indirectly quantified by measuring step widthand double limb support duration. People with PD have been shown to have postural instability in up-right stance (Morris, Iansek, Smithson, & Huxham, 2000; van Wegen, van Emmerik, Wagenaar, & Ellis,2001) and level-ground walking (Lowry, Smiley-Oyen, Carrel, & Kerr, 2009; Rochester et al., 2008). Itwas hypothesized that postural deficits would become more apparent during obstacle crossing andresult in people with PD compensating by either widening their step or increasing the time they spentin double limb support.

2. Methods

2.1. Participants

Level-ground walking and obstacle crossing was observed in 20 people with PD and 20 age and sexmatched control participants (Table 1). Control participants were recruited through community

Table 1Participant details. Standard deviations are reported in the brackets. Results of paired t-tests between groups are presented as p-values.

Subject Age (year) Sex Height (m) Mass (kg) MMSE/30 H&Y/5 UPDRS(III) /56

L-dopa doseequivalence (mg)

PD mean 65.6 (7.7) 4f16m

1.69 (0.08) 76.6 (13) 28.1 (1.5) Range 1–3 12.6 (5.1) 662.5

Control mean 65.3 (8.0) 4f16m

1.70 (0.08) 75.8 (11) 28.6 (1.6)

p-Value .178 .717 .824 .148

f = Female, m = Male.

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groups such as Rotary International. Community dwelling people with PD were recruited through lo-cal neurologists. They were screened to confirm a primary diagnosis of idiopathic PD and to ensurethat they did not suffer from freezing episodes or gait dyskinesia. Participants were included if theywere aged 45–80 years and were able to walk 10 m independently. They were excluded if they hada musculoskeletal, orthopaedic, or neurological disorder other than PD that affected their walkingor if they scored less than 24 on the Mini-Mental State Examination (MMSE). People with PD weretested during the peak dose of their medication. PD severity was determined using the motor compo-nent of the Unified Parkinson’s Disease Rating Scale (UPDRS) (Fahn, Elton, & UPDRS Program Members,1987) and the Hoehn and Yahr Scale (H&Y) (Hoehn & Yahr, 1967). The motor component of the UPDRSis scored out of 56, with a higher score indicating more severe motor symptoms. The H&Y scale isscored from zero to five, with a higher score also indicating more severe symptoms. Control partici-pants were matched to each PD participant by sex and age (±3 years). Written consent was obtainedfrom all participants prior to testing in accordance with the Helsinki declaration and the ethics ap-proval obtained from our local ethics research committee.

2.2. Equipment

Spatiotemporal variables were measured using an eight-camera VICON 612 3-D motion analysissystem, in conjunction with workstation software (Vicon Peak, Oxford, UK). The VICON system is a va-lid tool for measuring spatial and temporal variables of gait and has been shown to have good concur-rent validity with instrumented walkways (Webster, Wittwer, & Feller, 2005). The mean cameraresolution over the period of data capture was 1.6 mm. Retroreflective markers (14 mm diameter)were placed on bilateral calcaneus, the anterior superior aspect of the phalanx and the base of the firstand fifth metatarsal phalangeal joints. Two markers were also placed on the obstacle to determine itsposition during obstacle crossing trials. The obstacle (600 mm wide � 10 mm deep) and adjustablebrackets were both made of foam, colored bright yellow. Obstacle height was adjusted to 10% of leglength.

2.3. Procedure

Initially, participants walked barefoot along a 10-m linoleum walkway without an obstacle for twotrials to determine their preferred step length. In total, four level-ground walking trials and 16 obsta-cle crossing trials, comprising equal numbers of left and right crossing steps were analyzed. Partici-pants were instructed to ‘‘walk [over the obstacle and] to the end of the walkway at your preferredpace”. Condition order was counter-balanced after the initial two level-ground walking trials. Partic-ipants started 10 steps from the obstacle, as calculated from their pre-determined preferred level-ground walking step length. The crossing limb was manipulated by instructing the participants tostart walking with a particular foot.

It was possible that any differences in key outcome measures could be due to people with PD walk-ing slower and with shorter steps. To test this, we had 14 control participants walk at a similar speedand step length as their PD counterpart. White cardboard strips were placed horizontally to the

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walkway as a guide to the matched step length. Walking speed information obtained from a stopwatch was given to make sure they walked at a comparable speed. Practice trials were encourageduntil participants were able to walk consistently at the required speed and step length. These trialswere conducted in addition to the preferred walking condition. Six control participants found thematched walking condition difficult and were not able to walk at both the correct speed and steplength in the matched condition. Data from these participants were excluded from the analysis forthe matched comparisons.

2.4. Data processing

Marker trajectories were filtered using a quintic spline (Woltering) filter with a predicted meansquared error of 20 mm2. Two steps approaching the obstacle, two crossing steps (lead and trail),and a recovery step after the obstacle were examined. Spatiotemporal measures included step length,step duration, single limb support duration, double limb support duration, and step width. Verticalforefoot-obstacle clearance and placement of the heel from the obstacle after crossing were measuredfor the lead limb crossing step. Vertical toe-obstacle clearance and trail foot placement in front of theobstacle prior to crossing were measured for the trail limb crossing step. To account for anatomicaldifferences between matched pairs, step length was normalized to leg length and step width was nor-malized to pelvic width. Pelvis width was measured as the distance between the two anterior superioriliac spines.

2.5. Statistical analysis

A series of two-way repeated-measures analysis of variance (ANOVA) were used to test for groupmain effects and group-by-step interactions for spatiotemporal variables. Foot clearance variableswere tested using two-way paired t-tests. In the event of an interaction or group main effect, post-hoc analysis involved two-sided paired t-tests for each step to compare differences between peoplewith and without PD at preferred and matched conditions. We did not document the nature of stepmain effects as we were solely interested in the effects of PD on obstacle crossing. Post-hoc pairedt-tests were also used to compare group differences of step-to-step change scores for each of the spa-tiotemporal variables. Given the exploratory nature of this experiment, p-values of post-hoc tests werenot adjusted as this would increase the probability of making a type II error.

3. Results

3.1. Data analysis

Thirty-nine of the 42 data sets analyzed in this study were normally distributed and so parametrictests were justified to test the difference between groups. The assumption of sphericity was breachedin a majority of occasions and so Greenhouse-Geisser corrections were made to the degrees of free-dom for the two-way repeated-measures ANOVA.

3.2. Foot clearance

People with PD had a similar lead, p = .470, and trail, p = .168, forefoot clearance compared to thecontrol participants (Fig. 1 and Table 2). Those with PD placed their lead foot closer to the obstacleafter crossing, p = .002. Two people with PD stepped on the obstacle with their leading foot three timeseach during the testing session. No obstacle contacts occurred in the control group during capturedtrials, however one control participant contacted the top of the obstacle with the toe of their trail limbduring a practice trial for the matched condition. Both groups had similar trail limb foot placement infront of the obstacle, p = .300.

When matched for speed and step length, control participants placed their trail foot closer to thefront of the obstacle, p = .027, and their lead foot landed further from the obstacle after crossing,

Fig. 1. Group mean foot trajectories during obstacle crossing. Error bars represent 95% confidence intervals. Pictures of feetindicate walking direction and the markers on the feet show what part of the foot trajectory is displayed.

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p = .009. There was no statistical difference in toe clearance between the PD and control participantsfor the matched condition for lead, p = .155, or trail limbs, p = .071.

3.3. Spatial and temporal adaptations

Group main effects for speed, p < .001, step length, p < .001 and double limb support, p = .002, indi-cated that people with PD approached and stepped over the obstacle slower and with smaller stepsthan control participants, while also spending more time in double limb support. Post-hoc tests fora step by group interaction in step duration, p < .001, indicated that people with PD increased theirstep duration, p = .014, during the last approach step and lead limb crossing step, p < .001, more thancontrols. A step by group interaction also occurred for single limb support, p < .001, whereby peoplewith PD also increased time spent in single limb support during the lead limb step more than controls,

Table 2(a) Spatiotemporal variables, obstacle clearance and foot placement for people with PD and controls walking at preferred steplength and speed (n = 20 pairs). (b) Spatiotemporal variables, obstacle clearance and foot placement for people with PD andcontrols walking at a similar step length and speed (n = 14 pairs).

Variable Parkinson disease Control – preferred p-Value

(a)Level-ground walkingStep duration (s) 0.51 (0.09) 0.51 (0.03) .496Single limb support (s) 0.39 (0.03) 0.40 (0.02) .249Double limb support (s) 0.12 (0.03) 0.10 (0.01) .014*

Double limb support (% step) 23.1 (3.4) 20.4 (1.9) .003*

Step length (LL) 0.67 (0.10) 0.78 (0.08) .000*

Step velocity (LL/s) 1.33 (0.25) 1.56 (0.22) .001*

Step width (ASIS) 0.37 (0.15) 0.34 (0.13) .513

Obstacle crossingLead toe clearance (mm) 98.1 (32.4) 97.4 (21.8) .470Trail toe clearance (mm) 104.1 (26.8) 113.1 (32.1) .168Trail toe to obstacle (LL) 0.23 (0.06) 0.24 (0.07) .300Lead heel from obstacle (LL) 0.21 (0.07) 0.28 (0.08) .002*

Variable Parkinson disease Control – matched p-Value

(b)Level-ground walkingStep duration (s) 0.52 (0.06) 0.53 (0.06) .431Single limb support (s) 0.40 (0.03) 0.40 (0.03) .555Double limb support (s) 0.12 (0.03) 0.13 (0.04) .687Double limb support (% step) 23.3 (3.9) 23.3 (4.5) .971Step length (LL) 0.67 (0.09) 0.71 (0.11) .003*

Step velocity (LL/s) 1.33 (0.29) 1.38 (0.31) .058Step width (ASIS) 0.38 (0.12) 0.36 (0.14) .680

Obstacle crossingLead toe clearance (mm) 106.7 (32.7) 91.8 (24.8) .155Trail toe clearance (mm) 111.8 (25.5) 96.2 (23.3) .071Trail toe to obstacle (LL) 0.25 (0.06) 0.21 (0.06) .027*

Lead heel from obstacle (LL) 0.20 (0.06) 0.27 (0.1) .009*

LL – leg length, ASIS – width between the two anterior superior iliac spines. p-Values for paired t-test are presented forcomparisons between people with PD and control participants for preferred and matched conditions.* Flags p-values 6 .05.

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p < .001. In addition, there was a step by group interaction for step width, p = .003, which showed peo-ple with PD widened their step more than controls during the lead limb crossing step, p = .006.

Speed p = .385 and step length p = .142 were well controlled during the obstacle crossing steps forthe matched conditions, with no difference between the groups. Despite matching, there were step bygroup interactions for step duration, p < .001, single limb support, p = .006, and step width, p = .006.Post-hoc tests revealed people with PD still increased their step duration, p = .003, and single limbsupport, p = .005, more than controls during the leading step. Control participants still did not widentheir step as much as those with PD during the lead limb crossing step, p = .007. Interestingly, a groupmain effect for double limb support indicated controls spent more time in double limb support thanpeople with PD, p = .050 (see Fig. 2).

4. Discussion

This study examined the effects of PD on foot clearance during obstacle crossing. Lead and traillimb foot clearance was not shown to be different in people with PD and controls. Foot clearance re-mained similar when participants were matched for step length and velocity. This is consistent withprevious research showing that foot clearance remains similar over different walking speeds (Draga-

Fig. 2. Group mean spatiotemporal variables of gait during the two approach steps (A-2, A-1), two crossing steps (Ld, Tr), andrecovery step (R). Error bars represent within-group standard deviations. LL – leg length, ASIS – width between the anteriorsuperior iliac spines; *group difference of p 6 .05; � group difference of p 6 .05 for step-to-step change scores; � group maineffect of p 6 .05.

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nich & Kuo, 2004). This sample of people with PD was able to effectively increase their foot heightwhen stepping over an obstacle.

The foot clearance results did not support our original hypothesis that people with PD would have alower foot clearance. Parkinson disease is often associated with reduced amplitude of internally cuedmovement. Several examples of this phenomenon include a reduced step length during walking (Mor-ris et al., 2001), underscaled handwriting (Teulings & Stelmach, 1991), and quiet speech (Ho, Brad-shaw, Iansek, & Alfredson, 1999). The finding that foot clearance in those with PD was similar tocontrol participants gives rise to the hypothesis that some with PD might have used the obstacle asan external cue to regulate their foot clearance. This explanation is consistent with the large bodyof literature indicating that those with PD can normalize the size of their movement if externally cued(for a review see Rubinstein, Giladi, and Hausdorff (2002)). Further obstacle crossing studies using dy-namic obstacles, visual contrast, and secondary tasks in PD could clarify when obstacles act as a cueand when they act as a hazard.

Despite adequate forefoot clearance, people with PD had a deficit in step length regulation. Theyalso had poor planning of the trail foot placement in front of the obstacle. A short step length and slowwalking speed throughout the approach, crossing and recovery steps of obstacle crossing is consistentwith previous level-ground walking and turning studies in PD (Morris et al., 2001). Short steps did not,however, predispose people with PD to stepping on the obstacle if they placed their stance foot closerto the obstacle. A study of healthy young and older adults previously showed that when participantswalked slower, they stepped closer to the front of the obstacle (Draganich & Kuo, 2004). It might bespeculated that in this study, those with PD placed their trail foot too far from the front of the obstaclegiven their short step length, which resulted in them landing either on or close to the obstacle withtheir lead heel.

There were few differences in step or single limb support duration in the approach phase betweenthe two groups, although people with PD had a longer step duration during both lead and trail limbcrossing steps. They also lengthened their single limb support time from the last approach step tothe lead limb crossing step more than controls. Taking more time to step over the obstacle than con-trols may reflect an inability to move the foot fast enough to accommodate the higher foot trajectorydue to hypokinesia. As a result, the amount of time spent in single limb support increased more thancontrols. Single limb support is more unstable than double limb support, and so by increasing theamount of time they are spending in single limb support, people with PD may compromise their pos-tural stability.

People with PD spent more time in double limb support and widened their step more than controlswhen crossing the obstacle. Nevertheless, control participants spent more time in double limb supportwhen walking over obstacles at the same speed and step length as those with PD. Because double limbsupport time is highly correlated to walking speed (Andriacchi, Ogle, & Galante, 1977), we suggest thatpeople with PD did not spend more time in double limb support to compensate for postural instability.Instead, it might be because they walked slowly due to their hypokinesia. It is also possible that thematched condition acted as a dual task for some of the control participants and so led to increaseddouble limb support.

People with PD widened their step length when walking over the obstacle while control partici-pants maintained a narrow step width under both preferred and matched walking conditions. We sug-gest that people with PD widened their step when crossing the obstacle to compensate for posturalinstability in the frontal plane. Previous studies have shown people with PD to have poor balancein stance (Marchese, Bove, & Abbruzzese, 2003; Morris et al., 2000; Smithson, Morris, & Iansek,1998; van Wegen et al., 2001) and during level-ground walking (Lowry et al., 2009; Rochester et al.,2008). Given that sideways falls are implicated in hip fractures (Greenspan et al., 1998) and peoplewith PD have a high incidence of falls (Bloem, Hausdorff, Visser, & Giladi, 2004), further testing is war-ranted to quantify whether PD effects frontal plane motion of the body center of mass during obstaclecrossing.

Secondary analyses revealed those with moderately severe PD symptoms were more likely step onthe obstacle, walk slower, and land closer to the edge of the obstacle after crossing compared to mildlyaffected individuals. It is unclear whether the differences between mild and moderately affected indi-viduals occurred because of hypokinesia, rigidity, visual deficits, or other motor-sensory problems

B. Galna et al. / Human Movement Science 29 (2010) 843–852 851

associated with more severe PD. Larger studies, that include people with more severe PD, are neededto assess the exact relationship between disease severity and obstacle crossing performance and theresponsible underlying mechanism.

In light of the current findings, we would encourage clinicians to assess obstacle crossing in pa-tients with PD. For people with a short step length, taking a step over an obstacle from too far awaycould result in stepping on the obstacle. Importantly, having someone step closer to the obstacle mayin fact increase the likelihood of trail foot contact (Chou & Draganich, 1998). Therefore, it is advisedthat care must be taken when training obstacle crossing in PD not to put them at greater risk of a trip.Strategies that increase step length might improve foot placement in relation to the obstacle in peoplewith PD and so improve obstacle crossing safety, however this remains an untested hypothesis.

5. Conclusion

Parkinson disease did not affect lead or trail limb foot clearance during obstacle crossing. Peoplewith PD were more likely than healthy older adults to step on or close to the obstacle with their leadfoot because they had shorter steps. They did not place their trail foot any closer to the obstacle beforecrossing to accommodate for their short step length. People with PD also widened their lead limb stepover the obstacle more than controls, providing indirect evidence of postural instability in the frontalplane.

Acknowledgments

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; theGait Centre for Clinical Research Excellence for their ongoing assistance; Southern Health for accessto their testing facilities; Dr. Ernie Butler for his assistance in recruitment; and Dr. Graham Hepworthfor his statistical advice.

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