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NeuroRehabilitation 35 (2014) 279289 279

DOI:10.3233/NRE-141122
IOS Press

The Four Square Step Test in individuals


with Parkinsons disease: Association with
executive function and comparison with
older adults
Kathleen E. McKeea,b and Madeleine E. Hackneyc,d,
a Emory University School of Medicine, Atlanta, GA, USA
b Department of Neurology, Massachusetts General Hospital, Boston, MA, USA
c Atlanta Veterans Affairs Rehabilitation R&D Center of Excellence for Visual and Neurocognitive Rehabilitation,

Atlanta, GA, USA


d Department of Medicine, Division of General Medicine and Geriatrics, Emory University School of Medicine,

Atlanta, GA, USA

Abstract.
BACKGROUND: In Parkinsons disease (PD), motor and cognitive impairments interact to affect functional performance
adversely. A valid mobility test, the Four Square Step Test (FSST) involves multidirectional stepping over obstacles. FSST
performance may also be associated with cognitive performance.
OBJECTIVES: This study determined the feasibility and reliability of an obstacle-based FSST in older individuals with versus
without PD, and evaluated the association of PD performance of FSST with tests of cognition.
METHODS: Thirty-one individuals with mild-moderate PD, evaluated while ON medications, completed the obstacle-based
FSST, other mobility and cognitive measures. FSST performance was compared between a PD participant sub-set (n = 24) and 24
age-matched older adults. Data were analyzed with independent t-tests, correlations, and linear regression.
RESULTS: Obstacle-based FSST was feasible and reliable within sessions in those with PD. Median best FSST time among
individuals with PD was 11.72 s (9.99, 13.98) and FSST had concurrent validity with tests of mobility, and cognitive dual-tasking.
Among cognitive tests, Trails Making Test B, which evaluates executive function, emerged as a sole contributor (49%) of variance.
FSST performance did not differ between those with PD and older adults.
CONCLUSION: The obstacle-based FSST is feasible and reliable in those with PD. The relationship between cognitive status
and performance on the FSST did not appear to be strongly disease-stage dependent. Using FSST in the clinic may help assess
the health status of a motor-cognitive interaction in individuals with PD.

Keywords: Parkinsons disease, mobility limitation, cognition, accidental falls

1. Introduction
Address for correspondence: Madeleine E. Hackney, Ph.D.,
Individuals with Parkinsons disease (PD) have
Division of General Medicine and Geriatrics, Research Health motor and cognitive impairments that interact, impair-
Scientist, Rehab R&D Center (151R), Atlanta VA Medical Cen-
ter, 1670 Clairmont Rd. (12C145), Decatur, GA 30033, USA. Tel.:
ing the ability to complete activities of daily living
+1 404 321 6111 x 5006; Mobile: +1 314 412 4852; E-mails: (ADLs), increasing fall risk and decreasing qual-
mehackn@emory.edu, madeleine.hackney@gmail.com. ity of life (QOL). Motor symptoms include postural

1053-8135/14/$27.50 2014 IOS Press and the authors. All rights reserved
280 K.E. McKee and M.E. Hackney / Four Square Step Test in PD

instability, gait impairment, and bradykinesia. Cog- important to investigate the effect of an obstacle-based
nitive difficulties include impaired spatial cognition FSST in those with PD. Here, the FSST was studied in
(Possin, Filoteo, Song, & Salmon, 2008), set-switching older adults with idiopathic PD to 1) establish feasibil-
(Cools, Barker, Sahakian, & Robbins, 2001), execu- ity and reliability in those with PD, using 2.5 cm rods, as
tive function, and attention (Hausdorff et al., 2006). An per the original Dite & Temple protocol (Dite & Temple,
added cognitive task in a dual-task paradigm can exac- 2002), 2) examine concurrent validity with motor, cog-
erbate PD motor symptoms (Leroi, Collins, & Marsh, nitive, and cognitive dual-tasking tests, and 3) compare
2006). Axial impairment and postural instability in PD PD performance on FSST to that of age-matched older
indicate increased risk of dementia (Taylor et al., 2008). adults. Because a) an association between mobility
Likely, these problems stem from the impairment of and executive function exists and b) negotiating raised
overlapping neural systems serving both cognitive and obstacles while performing the FSST likely requires
motor function (Domellof, Elgh, & Forsgren, 2011). divided attention, cognitive dual-tasking and executive
For example, people with PD have trouble with both function tests were expected to predict performance on
planning and initiating movement. Because of signif- the FSST. Given the known impairments in movement
icant and overlapping effects of motor and cognitive initiation and planning experienced by individuals with
symptoms on ADLs, QOL, and fall risk, clinical tests PD, it was hypothesized that individuals with PD would
that provide a window into the health status of neuro- need more time to complete the FSST and would be
motor processes involving motor-cognitive interaction more variable in performance than age-matched older
are imperative to enhance clinical care in PD. individuals without PD.
Given the strong relationship between dynamic bal-
ance tasks and cognitive function (Paul, Sherrington,
Fung, & Canning, 2013), performance on the Four 2. Materials and methods
Square Step Test (FSST), a valid test of mobility involv-
ing movement initiation, planning, and coordination, 2.1. Participants
may provide information about the relative health of the
motor-cognitive interaction in people with PD. Feasi- The Institutional Review Board at Emory University
ble and reliable in older adults (Dite & Temple, 2002), School of Medicine approved this work. All participants
stroke survivors (Blennerhassett & Jayalath, 2008), provided written informed consent before participat-
those with vestibular disorders (Whitney, Marchetti, ing. Participants with PD were recruited through flyers,
Morris, & Sparto, 2007), and multiple sclerosis (Wag- referral, PD newsletters, support groups, and web-
ner, Norris, Van Dillen, Thomas, & Naismith, 2013), the sites. Telephone interviews were used to screen for
FSST requires participants to initiate multidirectional PD diagnosis. On the day of testing for the present
movement in a challenging sequence, while stepping study, all participants with PD were rated on the Uni-
over 2.5 cm diameter rods arranged in a cross (Dite fied Parkinsons Disease Rating Scale motor subscale
& Temple, 2002). Because many individuals with PD III (UPDRS-III) (Fahn & Elton, 1987) by two trained
exhibit deficiencies in planning and executing com- evaluators and scores were subsequently averaged.
plex, goal-directed behavior (Plotnik, Giladi, Dagan, PD participants included individuals with a diagnosis
& Hausdorff, 2011), completing the FSST may reveal of idiopathic definite PD (Hoehn and Yahr (H&Y)
deficits related to neuromotor processes that are neces- stages I-III) (Racette, Rundle, Parsian, & Perlmut-
sary for dividing attention between mental processing ter, 1999), demonstrated benefit from anti-parkinsonian
and postural control. However, the extent to which cog- medication, no other history of neurological insult and
nitive resources are involved in FSST performance is were at least 50 years old. All older adults were recruited
equivocal. from several senior independent living communities in a
Duncan & Earhart previously demonstrated FSST large urban metro area. Because Dite and Temple (Dite
reliability for individuals with PD using flat measuring & Temple, 2002) established FSST as a valid measure
sticks to form four squares on the floor over which the in older adults over age 65, a sub-analysis of individu-
patient should step (Duncan & Earhart, 2013). How- als over age 65 with PD (mean age 73 y, range 6582 y)
ever, age and neurological impairment progressively and older adults without PD (mean age 75.75 y, range
affect the ability to avoid raised obstacles during gait 6582 y) was conducted here. Older adult participants
(Weerdesteyn, Nienhuis, & Duysens, 2005). To eval- independently resided in senior living communities,
uate the real world impact of PD impairments, it is were screened briefly on the telephone for cognitive
K.E. McKee and M.E. Hackney / Four Square Step Test in PD 281

impairment, and had no history of progressive neuro- failed to complete the sequence accurately, lost balance,
logic disorder. Both groups could walk 3 or more meters touched a rod, or turned his/her hips from facing for-
with or without an assistive device. ward. Three successful trials were recorded as trials 1,
2, and 3. The fastest time was selected for concurrent
2.2. Procedure validity and group analyses. Participants were asked to
stop in place at the end of the test, and were offered bal-
Trained raters administered all tests. Individuals with ance assistance while research assistants removed the
PD and older adults were questioned about their medi- rods.
cal history, and fall history. Participants were classified
as fallers if they reported they had experienced an 2.3.1. Measure of disease severity
unintentional loss of balance that resulted in landing on Unied Parkinsons Disease Rating Scale Motor
a lower surface or the ground one or more times in the Subscale III (UPDRS-III) (Fahn & Elton, 1987) and
previous year. They also answered a single item ques- Hoehn & Yahr (H&Y) Stage of Disease Severity were
tionnaire about their fear of falls (on a 7 point scale). administered and scored by two qualified and trained
Testing for those with PD occurred while they were raters. UPDRS-Motor Subscale scores range from 0
ON medications at a participant-determined opti- (asymptomatic) to 108. H&Y stages range from 0
mal time. PD participants were tested with all the (asymptomatic) to 5 (wheelchair bound/bedridden).
measures described below in a single testing session. Scores from the two raters, which were highly corre-
Older adults without PD participated in only the FSST, lated, were averaged to provide a final score assessing
Berg Balance Scale (BBS), gait speed assessments, and disease severity in individuals with PD.
completed the Activities-specific Balance Confidence
Scale (ABC), and Beck Depression Inventory (BDI)-II 2.3.2. Measures of motor function
questionnaires. Timed Up and Go Test (TUG) (Morris, Morris, &
Iansek, 2001), valid in those with PD, measures func-
2.3. Measures tional mobility and was administered as published.
Six Minute Walk Test (6MWT) (Guyatt et al., 1985)
The Four Square Step Test (FSST) (Dite & Tem- assesses exercise tolerance. Participants were instructed
ple, 2002) required participants to step clockwise then to walk as far as they could in six minutes.
counterclockwise into four squares created by rods Thirty Second Chair Stand (Rikli & Jones, 2001)
measuring approximately 100 cm in length and 2.5 cm assesses lower body strength. Participants were asked
in diameter, arranged on the ground in a cross. One to rise from a chair to full standing as many times as
trained rater demonstrated, administered, and timed possible in 30 seconds.
the test with a stopwatch while a second rater spot- Berg Balance Scale (BBS) (Berg, Wood-Dauphinee,
ted the participant and provided verbal cues. The test & Williams, 1995) is a 14 item performance-oriented
was demonstrated at least two times. As in Blennerhas- measure of balance in older adults. The BBS has excel-
set et al. (Blennerhassett & Jayalath, 2008), directions lent inter- and intra-rater reliability (0.980.99). The
were modified slightly from the Dite and Temple proto- items, Time to Turn and Steps to Turn, which measure
col (Dite & Temple, 2002) for safety. Participants were the time and number of steps needed for a participant to
instructed to perform the test as quickly and as safely complete a 360 degree turn were individually analyzed.
as you can. Cues were provided regarding direction Turns in both directions were timed and steps counted;
of travel and safety (Pick up your feet.). Participants the greatest time and largest number of steps needed
were instructed to complete the step sequence without were used for analyses.
touching the rods and ensuring both feet contacted the Gait Speed (Bohannon, 1997) assesses multi-
floor in each square. The participant started with both directional preferred and fast walking speeds. Partici-
feet in square 1, with their back to square 4 and stepped pants performed three trials each of walking forward at
over the rods and into the squares in this order: 2, 3, 4, preferred pace, backward at preferred pace, and forward
1, 4, 3, 2, 1. Timing began when the participant initi- as fast as possible, all over 20 feet. For the latter, partic-
ated movement and stopped when both feet were back ipants were instructed to walk as quickly but as safely
in square 1 after completing the entire sequence. Tri- as they could. Qualified raters timed participants with a
als were repeated if the participant performed such that stopwatch as the first heel passed the starting line, and
it was clear he/she did not understand the instructions, stopped when the second heel passed the second line.
282 K.E. McKee and M.E. Hackney / Four Square Step Test in PD

The three trials from each condition were averaged and began with two moves, and progressed to a maximum
speed (m/s) was derived. of 9 moves, with 2 trials per level. Participants were
given one practice trial of 2 moves. Participants contin-
2.3.3. Measures of cognitive function ued to the next level if at least one trial was correctly
The Montreal Cognitive Assessment (MoCA) is a 30 performed. Span (number of moves remembered) was
point test, administered in approximately 10 minutes, considered for analyses.
which provides a measure of global status of cogni- Body Position Spatial Task (BPST) (Hackney, Hall,
tive impairment through the assessment of a range Echt, & Wolf, 2013) is modeled after Corsi blocks.
of executive functions including orientation, memory In BPST, the rater demonstrated (verbally and visu-
recall, visuospatial function, attention/concentration, ally) a pattern of side, forward and quarter turning (in
and language. The MoCA achieves high sensitivity place) steps after which the participant repeated the pat-
and specificity for detecting mild cognitive impairment tern. The rater began with two moves, and progressed
(Nasreddine et al., 2005) and is valid and reliable in to a maximum of 9 moves, with 2 trials per level.
people with PD (Chou et al., 2010). In order to per- Participants were given one practice trial of 2 moves.
form subanalyses on the PD group dichotomized by Participants continued to the next level if at least one
cognitive status (i.e., some cognitive impairment vs. no trial was correctly performed. Span (number of moves
cognitive impairment), a cutoff of 26 and greater was remembered) was considered for analyses.
used for those with no cognitive impairment (Hoops
et al., 2009). 2.3.4. Measures of dual-tasking
Trails Making Tests A and B (Reitan & Wolfson, Dual Timed Up and Go Test (Morris et al., 2001) is
2004) is a neuropsychological task of visual attention, a measure of functional mobility that is valid in those
processing speed, and executive function. In Trails A, with PD. Participants were timed while they performed
a test of visual motor speed and numeric sequencing, both single TUG (as described above) and a concur-
the participant connects numbers scattered on the page rent cognitive component (Cognitive-TUG; counting
in ascending order. In Trails B, a test of global frontal backwards by 3 s (serial 3 s) from a random number
lobe dysfunction and executive function, the participant between 20 and 100) or manual component (Manual-
connects numbers and letters on a page in alternat- TUG, carrying full glass of water). Before completing
ing ascending order (i.e., 1-A-2-B-3-C, etc.). Research Cognitive-TUG, the participant was given three,
assistants instructed participants to connect the let- 15-second trials of serial 3 s while seated.
ters or numbers as quickly as possible, without lifting
the pen/pencil from the paper, and allowed a practice 2.3.5. Questionnaires
attempt for both Trails A and B. Errors made while com- The participants completed the following question-
pleting the task were pointed out immediately so the naires within one week prior to their testing session.
participant could correct them. Time to complete each Parkinsons Disease Questionnaire-39 (PDQ-39)
trial (up to a maximum of 300 seconds) was recorded, (Peto, Jenkinson, Fitzpatrick, & Greenhall, 1995) is a
including time required to correct errors. Four individu- health-related quality of life measure for persons with
als with PD exceeded the maximum of 300 s on Trails B. PD that is validated. The summary index score was used
Brooks Spatial Task (Brooks, 1967) employs mental in analyses.
imagery to visualize and remember spatial locations. Freezing of Gait Questionnaire (FOGQ) (Giladi
It requires participants to remember the placement of et al., 2000) is a subjective evaluation of perception
numbers on a 4x4 matrix visualized in their mind and of freezing of gait phenomenon. Participants were clas-
then repeat the location of the numbers back to the sified as freezers by having a score greater than 1 on
rater. Participants began with a practice span of three item 3 of the FOGQ.
numbers and progressed up to 8 numbers. All levels Activities-specic Balance Condence Scale (ABC)
were completed regardless of performance on preced- (Powell & Myers, 1995) asks 16 questions related to
ing levels. The percentages correct (out of 50 items) confidence the participant would feel about not losing
were considered for analyses. his/her balance in life situations.
Reverse Corsi Blocks Visuospatial Task (Kessels, van Beck Depression Inventory-II (BDI-II) (Silberman
den Berg, Ruis, & Brands, 2008) requires participants to et al., 2006) is a well-validated test of depression
watch the examiner point to a series of blocks on a tray, recommended by the American Academy of Neurology
and then repeat the pattern backwards. The examiner for screening individuals with PD.
K.E. McKee and M.E. Hackney / Four Square Step Test in PD 283

2.4. Data analysis ships, post hoc regressions investigated the independent
contributions of disease stage, executive function and
Data were entered and cross-verified by research cognitive status to performance on the FSST. F-tests
assistants. Descriptive analyses were performed on determined equality of variance between outcome mea-
intrinsic participant characteristics and outcome mea- sures performance of older adults and those with PD,
sures. Trial to trial variability of each individuals three and independent t tests were used to determine dif-
trials was determined by calculating the coefficient of ferences between them. Independent t-tests or Mann
variation (CV): the standard deviation divided by the Whitney U tests (in the case of nonparametric samples)
mean and multiplied by 100. The stability of mea- were also performed on the fastest of three mean FSST
sures was examined within sessions by conducting times (i.e., the best time) for PD groups, stratified by
intraclass correlation coefficient analyses (ICC) (model fall, freezing and cognitive status. Alpha was 0.05.
3,1 single measures, consistency one way random).
FSST data were not normally distributed; therefore,
the association between FSST and concurrent motor 3. Results
and cognitive measures and self-reported data (demo-
graphics, fall incidence, psychosocial measures) were Thirty-four individuals with mild-moderate PD
determined with Spearmans correlation coefficient. (stage 1.5: n = 6, stage 2: n = 13, stage 2.5: n = 9, stage
After exploring associations through correlational anal- 3: n = 6) and 26 older adults, agreed to participate. One
yses, mobility and cognitive variables were entered into PD participant (stage 2.5) was excluded for suspected
separate simultaneous linear regressions to determine malingering. Two PD (stage 2.5 & 3) and two older
predictive validity for FSST performance. By examin- adult participants were excluded because they could not
ing the strength of association (standardized weights) attempt the FSST on the day of assessment. Thirty-one
of independent variables to the dependent variable, the PD and a subset of 24 PD and 24 age matched older
models were refined. To further explore key relation- adult participants are characterized in Table 1.

Table 1
Participant characteristics and selected mobility measuresa
PD (n = 31) PD Subset (n = 24) Older Adults (n = 24) p values
UPDRS-III Motor Subscale 27.30 (6.6) 28.60 (6.0)
Hoehn & Yahr Stage 2.00 (2.0, 2.5) 2.00 (2.0, 2.5)
Bradykinesia Item 0.81 (0.8) 0.88 (0.8)
Duration of PD (years) 7.23 (5.3) 6.25 (4.6)
Freezer (%) 29% 33%
Freezing of Gait Questionnaire 5.03 (4.9) 5.13 (4.5)
PDQ39 Summary Index 18.97 (8.8) 18.59 (7.5)
Sex 12F; 19M 8F; 16M 17F; 7M 0.019
Age (years) 69.65 (7.7) 73.00 (5.0) 75.75 (5.0) 0.063
Height (meters) 1.70 (0.1) 1.70 (0.1) 1.66 (0.1) 0.155
Weight (kg) 65.66 (27.1) 74.96 (13.1) 68.66 (13.2) 0.104
Number Comorbidities 3.10 (1.5) 3.38 (1.6) 3.50 (1.9) 0.805
Number Prescription Medications 6.20 (5.0) 6.39 (5.3) 3.68 (2.8) 0.038
Use of Assistive Device (%) 23% 29% 38% 0.760
Hx of 1 falls in Past Year (%) 55% 54% 42% 0.564
Fear of Falling 2.97 (1.5) 3.17 (1.5) 2.58 (1.7) 0.214
Activities Specific Bal. Conf. Scale 80.47 (15.0) 78.40 (15.6) 78.01 (19.9) 0.945
Quality of Life 5.21 (0.9) 5.21 (1.0) 5.33 (1.1) 0.675
Beck Depression Inventory-II (/63) 11.50 (6.0) 10.68 (6.2) 6.46 (3.8) 0.009
Berg Balance Scale (/56) 51.94 (3.0) 51.88 (2.9) 50.98 (3.8) 0.364
Forward Preferred Gait Speed (m/s) 1.00 (0.2) 0.98 (0.2) 1.03 (0.2) 0.451
Backward Preferred Gait Speed (m/s) 0.67 (0.3) 0.63 (0.2) 0.66 (0.3) 0.709
Fast (Forward) Gait Speed (m/s) 1.36 (0.3) 1.35 (0.3) 1.25 (0.2) 0.211
Abbreviations: PD, Parkinsons Disease; UPDRS, Unified Parkinsons Disease Rating Scale; Hx, History. a Values are means (standard deviation)
except Hoehn & Yahr is reported median (first, third interquartile) and dichotomous variables are reported as percentages. P values are calculated
between PD Subset and OA groups. Rating worry about falling/Rating quality of life from 1 (low) to 7 (high). Fishers Exact Test Equal
Variances Not Assumed.
284 K.E. McKee and M.E. Hackney / Four Square Step Test in PD

3.1. Feasibility of FSST for clinical use for Table 3


participants with PD, with obstacles and Spearmans correlation coefficients between FSST and concurrent
measures of physical and cognitive function and self-reported data
external cueing for individuals with PD (n = 31)

No adverse events (falls or injuries) occurred during Motor and dual tasking
testing. The safety precautions described in Methods Timed Up and Go (s) 0.734
Timed Up and Go-Cognitive (s) 0.634
were observed. Many participants demonstrated poor Timed Up and Go-Manual (s) 0.556
obstacle-awareness during the FSST and several had to Berg Balance Scale (/56) 0.659
initiate more than three times to obtain three valid trials. 360 degree Turn Time (s) 0.492
No participants refused to complete the test. Forward Preferred Gait Speed (m/s) 0.463
Backward Preferred Gait Speed (m/s) 0.575
Fast (Forward) Gait Speed (m/s) 0.564
3.2. Reliability within sessions for individuals with 6 Minute Walk Test (m) 0.476
PD 30 Second Chair Stand (s) 0.475
Steps to Turn 360 degrees 0.339
Trials 1 and 2 were strongly correlated (ICC = 0.735 Cognition
(0.5120.865), F value 6.539, p < 0.001), as were tri- Trails A (s) 0.715
Trails B (s) 0.513
als 2 and 3 (ICC = 0.876 (0.7590.939), F: 15.194, Corsi Blocks Spatial Task (span) 0.460
p < 0.001). There was moderate correlation between Brooks (% correct) 0.405
trials 1 and 3 (ICC = 0.543 (0.2240.758) F: 3.376, Montreal Cognitive Assessment (/30) 0.453
Body Position Spatial Task (span) 0.355
p = 0.001).
Psychosocial
Activities Specific Bal. Conf. Scale (%) 0.468
3.3. Concurrent validity for individuals with PD Fear of Falls 0.419
PDQ39 Summary Index 0.023
PD participant performance on outcome measures Freezing of Gait Questionnaire 0.216
Beck Depression Inventory-II 0.255
is described in Table 2. The median FSST-best time
Disease Severity/Demographics
for individuals with PD was 11.72 seconds (Confi- UPDRS 0.499
dence Interval (CI): 9.99, 13.98) and the trial-to-trial H&Y Staging 0.470
variability was CV: M = 14.1, SD = 11.5. Table 3 lists Bradykinesia 0.163
Time with PD 0.036
Spearmans correlation coefficients between FSST and Number of Comorbidities 0.270
concurrent measures of motor, dual-tasking, cognitive Number of Rx Medications 0.249
and psychosocial function, disease severity and demo- Age 0.077
graphics. Sex 0.118
Education (y) 0.177
Correlation is significant at the 0.01 level (2-tailed).
Table 2
PD Participant Performance on Measures of Motor and Cognitive
Function (n = 31)
3.4. Motor and dual-tasking
Mean (SD) Range
Four Square Trial 1 (s) 15.9 (5.8) 8.329.8
Four Square Trial 2 (s) 14.5 (6.7) 8.332.6 The FSST was strongly correlated with the TUG,
Four Square Trial 3 (s) 13.0 (4.6) 8.325.4 BBS, time to turn, forward, fast, and backward gait
Four Square Best (s) 12.9 (4.5) 8.327.9 speed, 6MWT, and chair stand. FSST was weakly
360 degree Turn Time (s) 4.6 (3.0) 2.719.0
correlated with steps to turn. FSST was strongly corre-
Steps to Turn 360 degrees 9.3 (3.4) 6.020.0
6 Minute Walk Test (m) 409.8 (95.3) 171.0631.2 lated with Cognitive-TUG and Manual-TUG (Table 3).
30 Second Chair Stand (s) 11.8 (2.7) 7.019.0 To determine which of the motor and dual-tasking
Timed Up and Go (s) 9.9 (2.8) 6.719.3 variables had the most predictive validity for FSST
Just Counting Accuracy (# correct/s) 0.5 (0.3) 0.11.0
Timed Up and Go-Cognitive (s) 14.3 (7.1) 6.942.6
performance, the variables forward, fast, and back-
TUG-c Accuracy (# correct/s) 0.4 (0.2) 0.00.9 ward gait, 6MWT, 30 s chair stand, time to turn, BBS,
Timed Up and Go-Manual (s) 12.7 (3.6) 7.525.5 TUG, Manual-TUG, and Cognitive-TUG were simul-
Trails A (s) 48.5 (41.8) 22.5252.3 taneously entered as predictors in a linear regression.
Trails B (s) 122.4 (90.0) 44.4300.0
Brooks (% correct) 62.6 (18.8) 4.090.0
Through a series of refinements of the model, 84.8
Body Position Spatial Task (span/9) 3.7 (1.0) 2.05.0 percent (F: 50.226) of the variance was explained
Corsi Blocks Spatial Task (span/9) 4.4 (1.3) 2.08.0 by Cognitive-TUG (standardized = 0.471, p = 0.002),
Montreal Cognitive Assessment (/30) 25.5 (3.0) 20.030.0 TUG (standardized = 0.350, p = 0.018), and time to
K.E. McKee and M.E. Hackney / Four Square Step Test in PD 285

turn (standardized = 0.236, p = 0.009). To determine


the relationship FSST may have had with dual-tasking
motor and cognitive skills, a forward stepwise linear
regression was performed on TUG, Manual-TUG and
Cognitive-TUG. Cognitive-TUG emerged as the sole
contributor accounting for 75.9% of the variance (F:
91.185) of FSST performance (standardized = 0.871,
p < 0.001).

3.5. Cognition

FSST was strongly correlated with Trails A, Trails B,


and Corsi Blocks, and correlated with Brooks, MoCA,
and BPST (Table 3). The variables Corsi span, BPST Fig. 1. The relationship of cognitive status and stage of disease
span, percent correct on the Brooks spatial test, and time with performance on the FSST. The PD group was subdivided into
to complete Trails A and B were entered in a simulta- H&Y stage 1.5 (diamonds), 2 (squares), 2.5 (triangles) and 3 (cir-
cles), and the correlation of FSST performance to performance on
neous regression. Through a series of refinements of Montreal Cognitive Assessment (MoCA) is depicted. Cognitive sta-
the model, Trails B (standardized : 0.696, p < 0.001) tus is more strongly related to FSST performance than is disease
emerged as the sole significant contributor accounting stage.
for 48.5% of the total variance (F: 27.211).

3.6. Psychosocial function To further explore these relationships, a regression


was performed that looked at the independent contri-
FSST was strongly correlated with balance confi- butions of disease stage, executive function (Trails B),
dence as measured by the ABC Scale, and correlated and cognitive status (MoCA) to performance on the
with fear of falls. FSST was only weakly correlated with FSST. The overall model explained 55.2 percent of the
PDQ39-SI, FOG, or BDI-II (r < 0.300) (Table 3). variance (F: 11.079, p < 0.001). Trails B was the only
variable that significantly contributed to the variance
3.7. Disease severity and demographics (standardized = 0.517, p = 0.003).

FSST was correlated with disease severity, as mea- 3.9. Group comparisons
sured by both the UPDRS and H&Y staging. FSST
correlations between the bradykinesia score on the Fallers vs. non-Fallers among individuals with PD:
UPDRS, time with PD, sex, number of comorbidities, Time needed to complete FSST did not differ signifi-
number of prescription medications, age, or years of cantly between fallers (M = 13.99, SD = 5.4 range: [9.1,
education were not of clinical relevance or practical 27.9]) and non-fallers (M = 11.64, SD = 2.8 range: [8.3,
significance (r < 0.300) (Table 3). 17.5]) (equal variances not assumed, p = 0.133).
Freezers vs. non-Freezers among individuals with
3.8. Post-hoc analyses exploring relationship PD: Time needed to complete the FSST did not dif-
between stage of disease, executive function, fer significantly between freezers (M = 13.76, SD = 5.0
cognitive status, and performance on FSST range: [9.2, 25.4]) and non-freezers (M = 12.60,
SD = 4.4 range: [8.3, 27.9]) (p = 0.524).
To further explore the relationship between stage of No cognitive impairment vs. some cognitive impair-
disease, cognitive status (MoCA), and performance on ment among individuals with PD (as measured by the
FSST, the PD group was subdivided into H&Y stages MoCA with cut off score 26): These two PD subgroups
1.5, 2, 2.5 and 3. There was an inverse correlation were not significantly different on stage of disease
between performance on FSST and performance on (Some cognitive impairment (n = 16): Median = 2.25,
MoCA (lower FSST score with higher MoCA score); 1st interquartile = 2, 3rd interquartile = 3; No cognitive
whilst the correlation between stage of disease and impairment (n = 15): Median = 2.00 1st interquar-
performance on FSST appeared weaker. These relation- tile = 1.5, 3rd interquartile = 2.5; p = 0.145), nor sex
ships are graphically depicted in Fig. 1. distribution (p = 0.957), nor freezer status (p = 0.401).
286 K.E. McKee and M.E. Hackney / Four Square Step Test in PD

However, performance on the FSST by those with some studies of FSST among older adults (Dite & Tem-
cognitive impairment (M = 14.67 SD = 5.6 seconds) was ple, 2002), stroke survivors (Blennerhassett & Jayalath,
significantly slower (p = 0.026) than those with no cog- 2008), and individuals with vestibular disorders (Whit-
nitive impairment (M = 11.08 SD = 2.0 seconds). ney et al., 2007), potentially because motor learning
Individuals with PD versus Older Adults: Table 1 is slower and uses more brain activity in individuals
includes comparison of a subset of 24 individuals with PD than those without (Nieuwboer, Rochester,
with PD and 24 age-matched older adults. The two Muncks, & Swinnen, 2009). These participants with
groups were not significantly different in age, height, PD also needed 2 seconds more to perform the FSST
weight, number of co-morbidities, use of assistive than previously reported values (Duncan & Earhart,
device, falls history, fear of falling, balance confi- 2013), likely because this studys participants nego-
dence, quality of life, performance on the BBS, nor gait tiated 2.5 cm rods rather than flat sticks. Similar to
function (Table 1). The PD group had more prescrip- previous work (Duncan & Earhart, 2013) motor out-
tion medications, more depression, and more males, come measures and disease severity were significantly
but notably there was no correlation between sex and correlated to FSST performance, in initial correla-
FSST performance (Table 3). Time needed to com- tional analyses. However, post-hoc regression analyses
plete FSST did not differ significantly between the exploring relationship between stage of disease, execu-
PD subset (M = 13.27, SD = 4.99, range: [8.25, 27.93]) tive function, cognitive status, and performance on the
and older adults (M = 13.66, SD = 5.12, range: [6.59, FSST revealed an inverse correlation between FSST
25.71]) (p = 0.790). Trial-to-trial variability was also performance and performance on MoCA (faster FSST
not significantly different (PD subset: CV: M = 13.8, time with higher MoCA score), and lack of a strong
SD = 11.3; older adults: CV: M = 14.3, SD = 9.3; correlation between stage of disease and performance
p = 0.885). on FSST. FSST may thus provide a unique assess-
ment of motor-cognitive interactions not fully evaluated
by isolated measures of disease severity or cognitive
4. Discussion function.

In individuals over age 50 with idiopathic PD, the 4.2. Association of cognitive function with FSST
FSST involving the negotiation of raised obstacles, is performance
feasible, reliable, and a valid measure of motor function.
Additionally, because FSST performance was associ- Here, regression offered Trails Ba test of exec-
ated with executive function and cognitive dual-task utive function, as a significant cognitive contributor to
performance, FSST may have potential to evaluate the variance in FSST performance. Further, that Cognitive-
health status of the motor-cognitive interaction, i.e., TUG emerged as a stronger contributor than TUG, the
neuromotor processes involving overlapping or shared latter being a demonstrated predictor of FSST perfor-
motor and cognitive systems. Curiously, those with PD mance (Dite & Temple, 2002; Duncan & Earhart, 2013;
performed similarly to age-matched individuals with- Whitney et al., 2007), indicates that FSST may use
out PD in both time to complete and variability in cognitive resources akin to those used in mental calcu-
performance. Further, PD performance on the FSST lation and divided attention. These findings corroborate
did not appear to be strongly stratified by disease work suggesting relationships between executive func-
severity. tion and gait performance under dual-task conditions
(Plotnik et al., 2011) and tasks that demand anticipatory
4.1. Feasibility, reliability, and concurrent validity postural adjustment with a change in base of support
with motor & disease severity measures (Paul et al., 2013). Additionally, correlations revealed
moderate-strong relationships between FSST perfor-
Obstacle-based FSST was feasible and reliable in mance and performance on tests of attentional/mental
these participants. That FSST was only weakly cor- status, visuospatial cognition, and mental imagery. A
related with demographics (e.g., age, education, sex) relationship between complex motor tasks like FSST,
suggests broad validity of the test for individuals and pure tests of cognitive function suggests that a
with PD regardless of demographic variables. Test- common dopaminergic system, with additional cholin-
retest reliability noted here and elsewhere (Duncan & ergic and cortical involvement, underlies performance
Earhart, 2013) are lower than correlations noted in of both functions.
K.E. McKee and M.E. Hackney / Four Square Step Test in PD 287

4.3. Subgroup comparisons tests may have decreased predictive validity for PD fall
status.
It was surprising that age-matched older adults and
PD participants did not differ significantly on FSST 4.4. Limitations
performance. It is possible that neurodegenerative pro-
cesses specific to PD may not affect the relationship A key limitation of this study is that cognitive per-
between executive and physical functioning above formance data from the healthy older adult sample are
and beyond that of normal aging processes. How- unavailable. It is thus challenging to determine from
ever, the healthy older sample was not evaluated for this studys results whether individuals who have more
cognitive performance and therefore, whether over- cognitive symptoms (regardless of the presence of a
all cognitive/executive status is most responsible for movement disorder) perform more poorly on the FSST.
FSST performance remains equivocal for the present Other limitations include a small sample size, which
study. A possible explanation for the non-differential limited power, and the differing sex distribution of the
results between those with and without PD could be the two cohorts (PD and healthy older adult). Although
attentional cues, which were provided during FSST to sex distributions were appropriate for the given pop-
maximize safety of participants. Such cues may have ulation, the fact that there were more women in the
allowed those with PD to compensate sufficiently for older adult group than in the PD group may have
bradykinesia, movement initiation, planning and other impacted performance on the FSST. Notably, there were
motor impairments, thus allowing them to perform no strong correlations between FSST performance and
more like older adults without PD. Abundant evidence sex. Several additional limitations should be addressed
has demonstrated that external, attentional cues have in future studies. Confirming test-retest reliability of
improved mobility (Lohnes & Earhart, 2011) and move- the obstacle-based FSST for people with PD over longer
ment initiation (Jiang & Norman, 2006) in individuals intervals, i.e., weeks and months, is necessary. Employ-
with PD. During externally cued movements, people ing additional cognitive dual-tasks and demonstrating
with PD might bypass the malfunctioning basal ganglia correlation would strengthen the findings observed here
(Freedland et al., 2002), and activate the Cerebellar- with serial 3 s dual-tasking. Future testing should also
Thalamo-Cortical (CTC) neural network, in a manner include assessment of FSST without cueing, and while
similar to that noted in age-matched controls (Lewis PD participants are OFF medications. Testing with-
et al., 2007). The well-known facilitating effects of out cueing may demonstrate a difference in FSST
cues for freezing of gait (Jiang & Norman, 2006) may performance between individuals with PD and older
also explain lack of differential findings between freez- adults. Testing those with PD while OFF medications
ers and non-freezers, which is consistent with previous is important to determine if the relationships between
work (Duncan & Earhart, 2013). bradykinesia, executive performance, and FSST perfor-
Post-hoc analysis was unable to generate a reliable mance are stronger. Increased bradykinesiaa reliable
cut-off point to identify fallers vs. non-fallers among clinical measure of the nigrostriatal lesion in PDis
individuals with PD. For the studys older adults, the associated with the presence of MCI and impaired
Dite and Temple (Dite & Temple, 2002) cut-off of 15 executive performance (Poletti et al., 2012). However,
seconds (PPV 86%, NPV 94%) remained a reasonable bradykinesia was not shown to be a significant contrib-
cut-off to identify multiple fallers (2 or more falls in utor here, potentially because participants were tested
the last 6 months). However, in the PD sub-set a cut- ON medications.
off of 15 seconds had sensitivity of 20%, specificity of
86%, a PPV of 50%, and an NPV of 60%, which indi-
cates that individuals with PD who are multiple fallers 5. Conclusions
can perform reasonably quickly on the FSST, reducing
the ability of the test to identify fallers. Other divided The FSST, a test of multi-directional mobility
attention, mentally involving paradigms (i.e., the dual- and obstacle avoidance, is feasible, reliable, and a
task), with which FSST appears to be related, have also valid measure of motor function and possibly motor-
been found to have minimal predictive value for falls in cognitive interaction. Although falls are a functional
individuals with PD (Smulders et al., 2012). Because outcome of high relevance to independence, morbidity
individuals with PD with severe balance impairment and mortality in both older adult populations and those
may retain capacity to move relatively quickly, timed with PD, no clear relationship was established between
288 K.E. McKee and M.E. Hackney / Four Square Step Test in PD

fall status and FSST in this study. However, a num- lational Sciences of the National Institutes of Health
ber of other significant relationships were demonstrated under Award Number UL1TR000454. The content is
between FSST and other functional abilities. FSST per- solely the responsibility of the authors and does not
formance had a demonstrated strong relationship with necessarily represent the official views of the National
motor skills such as turning in place, mobility, and cog- Institutes of Health. The Emory School of Medicine
nitive dual-taskingall of which are necessary to be Discovery Program supported KE McKee, and Depart-
able to function independently, and fully participate in ment of VA R&D Service Career Development Awards
life situations. Additionally there was lack of a strong (E7108M and N0870 W) supported ME Hackney.
correlation between stage of disease and performance
on FSST. The FSST may thus shed light upon motor-
cognitive interactions independent of disease severity References
that affect functional abilities in those with PD. Given
limited knowledge about relationships between cogni-
Berg, K., Wood-Dauphinee, S., & Williams, J. I. (1995). The Balance
tive state, motor skill, and PD, the FSST test should Scale: Reliability assessment with elderly residents and patients
be considered to be included in a battery of tests uti- with an acute stroke. Scandinavian Journal of Rehabilitation
lized for impairments that might not be observed with Medicine, 27(1), 27-36.
pure motor, cognitive, or disease severity assessments Blennerhassett, J. M., & Jayalath, V. M. (2008). The Four Square
in individuals with PD. Given that specific impairments Step Test is a feasible and valid clinical test of dynamic stand-
ing balance for use in ambulant people poststroke. Archives of
may be elicited with specific balance and mobility tests Physical Medicine and Rehabilitation, 89(11), 2156-2161. doi:
(Paul et al., 2013), understanding the effects of real 10.1016/j.apmr.2008.05.012
world tasks like FSST upon motor-cognitive interac- Bohannon, R. W. (1997). Comfortable and maximum walking speed
tions may help elucidate the neuropathology of clinical of adults aged 2079 years: Reference values and determinants.
signs in PD. Age and Ageing, 26(1), 15-19.
Brooks, L.R. (1967). The suppression of visualization by reading. Q
Exp J Psychol, 19(4), 289-299.
Chou, K. L., Amick, M. M., Brandt, J., Camicioli, R., Frei, K.,
Acknowledgments Gitelman, D., et al. (2010). A recommended scale for cogni-
tive screening in clinical trials of Parkinsons disease. Movement
We would like to thank those who assisted in data Disorders, 25(15), 2501-2507. doi: 10.1002/mds.23362
Cools, R., Barker, R. A., Sahakian, B. J., & Robbins, T. W. (2001).
acquisition and entry: Allison Bascas, Marco Coelho, Mechanisms of cognitive set flexibility in Parkinsons disease.
Dabin Choi, Carly DiLeo, Kevin Huang, Virginia Pow- Brain, 124(Pt 12), 2503-2512.
ers, Adrienne Wimberly, Kedra Woodard and Nathalie Dite, W., & Temple, V. A. (2002). A clinical test of stepping and
Angel. We acknowledge the Emory Center for Health change of direction to identify multiple falling older adults.
in Aging. We also acknowledge Clairmont Oaks, Clair- Archives of Physical Medicine and Rehabilitation, 83(11), 1566-
1571.
mont Place, Kingsbridge and Wesley Woods Towers Domellof, M. E., Elgh, E., & Forsgren, L. (2011). The relation
retirement communities for providing space for the between cognition and motor dysfunction in drug-naive newly
assessments and we thank the administrative staff for diagnosed patients with Parkinsons disease. Movement Disor-
each institution. We acknowledge Dr. William De ders, 26(12), 2183-2189. doi: 10.1002/mds.23814
LAune for statistical assistance. Duncan, R. P., & Earhart, G. M. (2013). Four Square Step Test Perfor-
mance in People With Parkinson Disease. Journal of Neurologic
Physical Therapy. doi: 10.1097/NPT.0b013e31827f0d7a
Fahn, S., & Elton, R.L. (1987). Unified Parkinsons Disease Rat-
Declaration of interest ing Scale. In S. Fahn, C. D. Marsden, M. Goldstein & D. B.
Calne (Eds.), Recent Developments in Parkinsons Disease (Vol.
There are no conflicts of interest. The study spon- 2). Florham Park, NJ: Macmillan Healthcare Information.
Freedland, R. L., Festa, C., Sealy, M., McBean, A., Elghazaly, P.,
sors played no role in the study design, collection, Capan, A., et al. (2002). The effects of pulsed auditory stimula-
analysis and interpretation of data, the writing of the tion on various gait measurements in persons with Parkinsons
manuscript, the final conclusions drawn, or in the deci- Disease. NeuroRehabilitation, 17(1), 81-87.
sion to submit the manuscript for publication. The Giladi, N., Shabtai, H., Simon, E. S., Biran, S., Tal, J., & Korczyn,
Dan and Merrie Boone Foundation, the Emory Center A. D. (2000). Construction of freezing of gait questionnaire for
patients with Parkinsonism. Parkinsonism & Related Disorders,
for Injury Control, and the Emory Center for Health 6(3), 165-170.
in Aging supported the study. This study was also Guyatt, G. H., Sullivan, M. J., Thompson, P. J., Fallen, E. L., Pugsley,
supported by the National Center for Advancing Trans- S. O., Taylor, D. W., & Berman, L. B. (1985). The 6-minute walk:
K.E. McKee and M.E. Hackney / Four Square Step Test in PD 289

A new measure of exercise capacity in patients with chronic heart and well being for individuals with Parkinsons disease. Quality
failure. Canadian Medical Association Journal, 132(8), 919-923. of Life Research, 4(3), 241-248.
Hackney, M. E., Hall, C. D., Echt, K. V., & Wolf, S. L. (2013). Plotnik, M., Giladi, N., Dagan, Y., & Hausdorff, J. M. (2011). Pos-
Dancing for balance: Feasibility and efficacy in oldest-old adults tural instability and fall risk in Parkinsons disease: Impaired
with visual impairment. Nursing Research, 62(2), 138-143. doi: dual tasking, pacing, and bilateral coordination of gait during the
10.1097/NNR.0b013e318283f68e ON medication state. Experimental Brain Research, 210(3-4),
Hausdorff, J. M., Doniger, G. M., Springer, S., Yogev, G., Simon, E. 529-538. doi: 10.1007/s00221-011-2551-0
S., & Giladi, N. (2006). A common cognitive profile in elderly Poletti, M., Frosini, D., Pagni, C., Baldacci, F., Nicoletti, V., Tognoni,
fallers and in patients with Parkinsons disease: The prominence G., et al. (2012). Mild cognitive impairment and cognitive-motor
of impaired executive function and attention. Experimental Aging relationships in newly diagnosed drug-naive patients with Parkin-
Research, 32(4), 411-429. doi: 10.1080/03610730600875817 sons disease. J Neurol Neurosurg Psychiatry, 83(6), 601-606. doi:
Hoops, S., Nazem, S., Siderowf, A. D., Duda, J. E., Xie, S. X., 10.1136/jnnp-2011-301874
Stern, M. B., & Weintraub, D. (2009). Validity of the MoCA Possin, K. L., Filoteo, J. V., Song, D. D., & Salmon, D. P. (2008).
and MMSE in the detection of MCI and dementia in Parkin- Spatial and object working memory deficits in Parkinsons dis-
son disease. Neurology, 73(21), 1738-1745. doi: 10.1212/WNL. ease are due to impairment in different underlying processes.
0b013e3181c34b47 Neuropsychology, 22(5), 585-595. doi: 10.1037/a0012613
Jiang, Y., & Norman, K. E. (2006). Effects of visual and auditory Powell, L. E., & Myers, A. M. (1995). The Activities-specific Bal-
cues on gait initiation in people with Parkinsons disease. Clinical ance Confidence (ABC) Scale. Journals of Gerontology. Series
Rehabilitation, 20(1), 36-45. A: Biological Sciences and Medical Sciences, 50A(1), M28-M34.
Kessels, R. P., van den Berg, E., Ruis, C., & Brands, A. M. (2008). The Racette, B. A., Rundle, M., Parsian, A., & Perlmutter, J. S. (1999).
backward span of the Corsi Block-Tapping Task and its associa- Evaluation of a screening questionnaire for genetic studies of
tion with the WAIS-III Digit Span. Assessment, 15(4), 426-434. Parkinsons disease. American Journal of Medical Genetics,
doi: 1073191108315611 [pii] 10.1177/1073191108315611 88(5), 539-543.
Leroi, I., Collins, D., & Marsh, L. (2006). Non-dopaminergic treat- Reitan, R. M., & Wolfson, D. (2004). The Trail Making Test as an
ment of cognitive impairment and dementia in Parkinsons initial screening procedure for neuropsychological impairment
disease: A review. Journal of the Neurological Sciences, 248(1-2), in older children. Archives of Clinical Neuropsychology, 19(2),
104-114. doi: 10.1016/j.jns.2006.05.021 281-288. doi: 10.1016/s0887-6177(03)00042-8
Lewis, M. M., Slagle, C. G., Smith, A. B., Truong, Y., Bai, P., McK- Rikli, R., & Jones, C. (2001). Senior Fitness Test Manual. Champaign,
eown, M. J., et al. (2007). Task specific influences of Parkinsons IL: Human Kinetics.
disease on the striato-thalamo-cortical and cerebello-thalamo- Silberman, C. D., Laks, J., Capitao, C. F., Rodrigues, C. S., Moreira, I.,
cortical motor circuitries. Neuroscience, 147(1), 224-235. doi: & Engelhardt, E. (2006). Recognizing depression in patients with
10.1016/j.neuroscience.2007.04.006 Parkinsons disease: Accuracy and specificity of two depression
Lohnes, C. A., & Earhart, G. M. (2011). The impact of atten- rating scale. Arquivos de Neuro-Psiquiatria, 64(2B), 407-411.
tional, auditory, and combined cues on walking during single Smulders, K., Esselink, R. A., Weiss, A., Kessels, R. P., Geurts, A.
and cognitive dual tasks in Parkinson disease. Gait and C., & Bloem, B. R. (2012). Assessment of dual tasking has no
Posture, 33(3), 478-483. doi: S0966-6362(10)00459-5 [pii] clinical value for fall prediction in Parkinsons disease. Journal of
10.1016/j.gaitpost.2010.12.029 Neurology, 259(9), 1840-1847. doi: 10.1007/s00415-012-6419-4
Morris, S., Morris, M. E., & Iansek, R. (2001). Reliability of mea- Taylor, J. P., Rowan, E. N., Lett, D., OBrien, J. T., McKeith, I.
surements obtained with the Timed Up & Go test in people with G., & Burn, D. J. (2008). Poor attentional function predicts
Parkinson disease. Physical Therapy, 81(2), 810-818. cognitive decline in patients with non-demented Parkinsons dis-
Nasreddine, Z. S., Phillips, N. A., Bedirian, V., Charbonneau, S., ease independent of motor phenotype. Journal of Neurology,
Whitehead, V., Collin, I., et al. (2005). The Montreal Cognitive Neurosurgery and Psychiatry, 79(12), 1318-1323. doi: 10.1136/
Assessment, MoCA: A brief screening tool for mild cognitive jnnp.2008.147629
impairment. Journal of the American Geriatrics Society, 53(4), Wagner, J. M., Norris, R. A., Van Dillen, L. R., Thomas, F. P., &
695-699. doi: 10.1111/j.1532-5415.2005.53221.x Naismith, R. T. (2013). Four Square Step Test in ambulant persons
Nieuwboer, A., Rochester, L., Muncks, L., & Swinnen, S. P. (2009). with multiple sclerosis: Validity, reliability, and responsiveness.
Motor learning in Parkinsons disease: Limitations and potential International Journal of Rehabilitation Research, 36(3), 253-259.
for rehabilitation. Parkinsonism & Related Disorders, 15 Suppl doi: 10.1097/MRR.0b013e32835fd97f
3, S53-S58. doi: 10.1016/s1353-8020(09)70781-3 Weerdesteyn, V., Nienhuis, B., & Duysens, J. (2005). Advancing age
Paul, S. S., Sherrington, C., Fung, V. S., & Canning, C. G. progressively affects obstacle avoidance skills in the elderly. Hum
(2013). Motor and cognitive impairments in Parkinson disease: Mov Sci, 24(5-6), 865-880. doi: 10.1016/j.humov.2005.10.013
Relationships with specific balance and mobility tasks. Neu- Whitney, S. L., Marchetti, G. F., Morris, L. O., & Sparto, P. J. (2007).
rorehabilitation and Neural Repair, 27(1), 63-71. doi: 10.1177/ The reliability and validity of the Four Square Step Test for
1545968312446754 people with balance deficits secondary to a vestibular disorder.
Peto, V., Jenkinson, C., Fitzpatrick, R., & Greenhall, R. (1995). The Archives of Physical Medicine and Rehabilitation, 88(1), 99-104.
development and validation of a short measure of functioning doi: 10.1016/j.apmr.2006.10.027
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