Long-Term Monitoring of Gait in Parkinson's Disease

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Long-term monitoring of gait in Parkinson's


Disease
Article in Gait & Posture August 2007
DOI: 10.1016/j.gaitpost.2006.09.011 Source: PubMed

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Gait & Posture 26 (2007) 200207


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Long-term monitoring of gait in Parkinsons disease


Steven T. Moore a,*, Hamish G. MacDougall a, Jean-Michel Gracies a,
Helen S. Cohen b, William G. Ondo c
b

a
Department of Neurology, Mount Sinai School of Medicine, New York, NY 10029, USA
Bobby R. Alford Department of OtolaryngologyHead and Neck Surgery, Baylor College of Medicine, Houston, TX, USA
c
Department of Neurology, Baylor College of Medicine, Houston, TX, USA

Received 4 May 2006; received in revised form 21 July 2006; accepted 8 September 2006

Abstract
A new system for long-term monitoring of gait in Parkinsons disease (PD) has been developed and validated. The characteristics of every
stride taken over 10-h epochs were acquired using a lightweight ankle-mounted sensor array that transmitted data wirelessly to a small pocket
PC at a rate of 100 Hz. Stride was calculated from the vertical linear acceleration and pitch angular velocity of the leg with an accuracy of
5 cm. Results from PD patients (5) demonstrate the effectiveness of long-term monitoring of gait in a natural environment. The small, variable
stride length characteristic of Parkinsonian gait, and fluctuations of efficacy associated with levodopa therapy, such as delayed onset, wearing
off, and the off/on effect, could reliably be detected from long-term changes in stride length.
# 2006 Elsevier B.V. All rights reserved.
Keywords: Stride length; Levodopa; Parkinsonian; Locomotion; Accelerometer

1. Introduction
Parkinsons disease (PD) is a common neurodegenerative
disorder reflecting a progressive loss of dopaminergic and
other sub-cortical neurons [1]. Levodopa, the metabolic
precursor to dopamine, has commonly been used to manage
the motor symptoms of PD for over 40 years by regenerating
depleted dopamine at the striatum. Although initially
effective, as the disease advances the duration of each dose
shortens (the wearing off effect), necessitating more frequent
levodopa administration. In addition, the development of
dyskinesias (involuntary movements) and the off/on
phenomenon (abrupt and unpredictable locomotor responses
to individual doses of levodopa) can limit mobility and
complicate dosing [2].
Typically, clinical evaluation involves brief observation
during simple motor tasks, such as getting up out of a chair
and walking a short distance. Assessment of long-term
* Corresponding author at: Mount Sinai School of Medicine, Department
of Neurology, Box 1135, 1 E 100th Street, New York, NY 10029, USA.
Tel.: +1 212 241 9306; fax: +1 212 831 1610.
E-mail address: [email protected] (S.T. Moore).
0966-6362/$ see front matter # 2006 Elsevier B.V. All rights reserved.
doi:10.1016/j.gaitpost.2006.09.011

medication response usually takes the form of a patient


diary, where the Parkinsonian state is noted as on (i.e.,
effectively medicated), off or on with dyskinesias
[3,4]. However, self-reporting can be unreliable [5]. The
Unified Parkinsons Disease Rating Scale (UPDRS) [6],
although widely utilized in research studies [7], has
significant limitations. Analysis of gait is limited to
assigning a single value between 0 (normal) and 4 (unable
to walk, even with assistance) from brief clinical
observation. Given the complexity of determining the
optimal levodopa dosing schedule, a more objective means
of assessing gait over longer periods during normal daily
life may significantly improve management of locomotor
dysfunction in PD.
Wrist or belt mounted accelerometers (activity monitors)
have been used for long-term monitoring of motor
fluctuations in PD [811], although on and off phases
cannot be reliably determined in individual subjects. A more
brute-force approach to accelerometry (six tri-axial
accelerometers; mounted on both upper arms, both upper
legs, the sternum and one wrist) could distinguish on and
off phases [12], as well as dyskinesias from voluntary
movements [13]. However, the complexity and intrusive

S.T. Moore et al. / Gait & Posture 26 (2007) 200207

nature of multiple body-segment accelerometry limits its use


outside of the research environment.
Although gross body acceleration data can provide an
objective alternative to periodic self reporting of motor state,
it does not indicate the functional locomotor capacity of the
individual; i.e., how well the patient is walking. One of the
cardinal features of PD is locomotor dysfunction; shortened
stride length, increased variability of stride [1416],
shuffling gait, and freezing [17]. To characterize pathological gait in the PD patient it is necessary to accurately
monitor stride length over extended periods. A number of
ambulatory systems have employed gyroscopes to measure
the angular velocity of the thigh and/or shank, and integrated
these waveforms to obtain the angular extent of leg swing,
which when scaled by subject height yields an estimate of
stride length [18,19]. Stride length estimates were relatively
inaccurate, with an error of 15% [18]. A more recent
realization utilizing gyroscopes on the shank of both legs
and a third gyroscope on the right thigh improved stride
length accuracy to 7 cm, and was capable of logging for up
to 2.5 h [20,21]. However, cables used to relay data from legmounted gyroscopes to a central logging unit create an
unacceptable trip hazard and interfere with patients normal
daily activity, limiting their use in the community.
In this paper, we describe a novel ambulatory system for
accurate measurement of every stride taken over extended
periods (up to 10 h). Clinical features of PD, such as small,
variable stride length and fluctuations in motor performance
with levodopa administration, were well correlated with data
obtained from the stride monitor. Long-term stride
monitoring may significantly improve pharmacological
management of PD symptoms, particularly in the advanced
stages of the disease where abrupt and unpredictable
responses to levodopa complicate dosing.

201

years [38 (S.D. 7.7)], and height from 153 to 183 cm [167
(S.D. 12.2)]. Seven participants diagnosed with idiopathic
Parkinsons disease (three males and four females) were
enrolled to verify measurement accuracy (2) and obtain pilot
data (5) on the efficacy of long-term stride monitoring. Age
ranged from 65 to 85 years [72.0 (S.D. 7.4)], age at onset of PD
from 40 to 79 years [57.7 (S.D. 13.3)], and height from 160 to
193 cm [172.1 (S.D. 11.8)]. The study was approved by the
Institutional Review Boards at the Mount Sinai School of
Medicine and Baylor College of Medicine and Affiliated
Hospitals, and was performed in accordance with the ethical
standards of the 1964 Declaration of Helsinki. Participants
gave informed consent prior to their inclusion in the study.
2.2. Hardware

2. Methods

The stride monitor consisted of two subsystems. A small


Inertial Measurement Unit (IMU: 28 mm  38 mm  54
mm; MT9, Xsens, Enschede, The Netherlands), with a 9 V
battery and Bluetooth serial transmitter (BL-819, RS232
Bluetooth Converter, Brainboxes Ltd., Liverpool, United
Kingdom), was mounted around the shank (just above the
ankle) using an elasticized strap and Velcro. The IMU
transduced 3D linear acceleration and angular velocity of the
lower limb at a sample rate of 100 Hz. In addition, a Pocket PC
(iPAQ 2200, Hewlett Packard, Palo Alto, CA), worn in a small
pouch around the waist, acquired the leg movement data
wirelessly (via Bluetooth) from the IMU within an effective
range of 100 m, and stored data files on a secure digital (SD)
flash memory card. The shank-mounted components (IMU,
battery and Bluetooth transmitter) weighed less than 130 g, or
less than 2% of the mass of the shank and foot [22], which
should not significantly affect movement of the lower limb.
The PC weighed 146 g, and was slightly larger than a cell
phone (119 mm  77 mm  16 mm). The stride monitor was
unobtrusive and did not interfere with the participants normal
activities.

2.1. Research participants

2.3. Data processing

Ten healthy participants (five males and five females), with


no history of gait abnormalities, provided calibration and
validation of the stride monitor. Age ranged from 30 to 55

Vertical linear acceleration and pitch angular velocity


(sagittal plane) of the shank were used to assess gait (Fig. 1).
During upright stance there was a DC offset of 9.8 m/s2 in

Fig. 1. Vertical linear acceleration (dashed trace) and pitch angular velocity (solid trace) from the stride monitor during locomotion. The negative portion of the
angular velocity trace corresponds to forward rotation of the leg during the swing phase.

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S.T. Moore et al. / Gait & Posture 26 (2007) 200207

the vertical acceleration, and changes in this value were used


to distinguish periods where the participant was supine (see
Fig. 5A). A moving RMS trace of the vertical acceleration
waveform was calculated using a sliding window of 2 s
width [23]. Locomotor activity was defined as periods where
the RMS acceleration was greater than 0.4 m/s2 above
baseline [23]. According to the right-hand rule, negative
pitch angular velocity corresponded to the forward rotation
of the leg during the swing phase of locomotion (Fig. 1). An
initial stride length estimate (SLi) was calculated as follows:
SLi 2l sin

 
a
2

(1)

where l is the length of the leg from the trochanter (hip joint)
to the ground, and a is the angular extent of the swing phase
(determined from integration of the angular velocity trace).
Determining stride length from leg swing alone is reasonably accurate for small stride lengths (<1 m). However, this
technique underestimates larger strides due to the considerable forward motion of the body over the stance foot in
addition to the component generated by leg swing. It was
therefore necessary to provide a calibration algorithm based
on the initial stride estimate to correct for longer strides.
Changes in stride length following levodopa administration in participants with Parkinsons disease were
assessed by fitting an exponential function to binned mean
stride data (each bin comprising 60 sequential strides) using
the LevenbergMarquardt algorithm [24,25]. The time
constant of the exponential rise or decay of stride length was
estimated from the best fit (see Figs. 4B and 5B).
2.4. Calibration
The stride monitor was primarily calibrated using a direct
measure of stride length obtained from 10 healthy
participants walking along a 30-m hallway. Healthy controls
were utilized as it was necessary to acquire angular velocity
data over a wide range of stride lengths (0.21.5 m) to
determine the calibration algorithm; varying stride length on
demand is beyond the capabilities of most PD patients,
particularly in the off state. An aluminum tube was taped to
the heel of the left shoe and a whiteboard marker inserted
such that the tip left a single dot on the floor during each foot
placement. Simultaneous estimates of stride length were
obtained from the stride monitor, also attached to the left leg.
Actual stride length was determined from measurement of
the distance between successive dots on the floor.
Participants were instructed to walk at a natural pace but
to vary gait according to verbal commands to produce a
range of stride lengths, including small shuffling steps
typical of Parkinsons disease. The pen technique was
chosen as it allowed calibration of the stride monitor over a
wide range, was relatively accurate (5 mm error), and
facilitated calibration outside of the laboratory. Accuracy of
the device to monitor pathological (Parkinsonian) gait was

evaluated by two different techniques; (1) the pen technique


described above, and (2) comparing stride monitor measures
with those obtained from a video motion analysis system
tracking horizontal foot movement with an accuracy of
5 mm (Optitrack, NaturalPoint, Corvallis, OR).
2.5. Stride monitoring of PD patients
Long-term stride monitoring (left leg) was performed on
five PD patients at the Baylor College of Medicine
Movement Disorders Clinic, Houston, TX. Stride length
data was collected in two participants over a period of
75 min in the clinic. For the other three participants, the
stride monitor was activated at the clinic prior to patients
departure and collected from their home after 6 h of data
acquisition during normal daily activity. They were also
asked to keep a simple diary of activities and PD-related
medication administration at approximately 30-min intervals.

3. Results
3.1. Calibration
Ten healthy controls travelled 27.9 m (S.D. 1.8) over 27
strides (S.D. 3.6) while traversing the 30-m corridor. Plotting
height-normalized true-versus-estimated stride lengths from
the 10 controls revealed a non-linear but consistent
relationship, such that it was possible to generalize a
calibration algorithm applicable to all participants (Fig. 2).
To correct for underestimation of large (>1 m) strides due to
forward motion of the body over the stance foot, a leastsquares fit (Labview Advanced Analysis Package, National
Instruments, Austin, TX) was applied to the heightnormalized initial stride length estimates (SLni) (Fig. 2,
solid black circles) of the form:
SLnc a0 a1 sin SL2ni a2 3 cos SLni
a4 SL4ni

a3
SLni 1
(2)

where SLnc is the height-normalized corrected stride length


(Fig. 2, solid grey circles), and the coefficients ai were
(43.3, 21.9, 14.9, 1.4, 2.3). The resultant corrected stride
length measures exhibited a highly linear relationship to
true stride length (r = 0.98) (Fig. 2, dashed black line). The
mean error was 2.8% (CI 1.1) of participant height (maximum error 9%), or 5 cm for the average participant height
of 167 cm. The error per stride was also estimated by
comparing the total distance traveled down the hallway
(cumulative stride length of the true and corrected values)
and dividing by the number of strides taken for each
participant. Mean error was similar to that calculated from
the height-normalized data at 4.8 cm (CI 1.1), with a maximum error of 8 cm.

S.T. Moore et al. / Gait & Posture 26 (2007) 200207

Fig. 2. True (pen) versus estimated (stride monitor) stride length from 10
healthy controls, normalized by height (filled black circles). A general leastsquare error fit (grey trace) to these data was used to derive a calibration
algorithm that produced a highly linear relationship with actual stride values
(black dashed line).

Stride data obtained from two PD participants in the off


state (no dopaminergic medication in the previous 12 h)
demonstrated similar measurement accuracy. A participant
with a relatively mild form of PD (69-year-old female, age at
onset 59 years, height 173 cm) walked a distance of 4.5 m
(five strides) and simultaneous pen and stride monitor
measures of stride length (left leg) were obtained. Average
stride length was 90.1 cm (pen) and 89.2 cm (stride
monitor). Mean difference was 3.3 cm (maximum error
8 cm). A second participant (68-year-old male, age at onset
52 years, height 168 cm) with severe locomotor impairment
traversed a distance of 89 cm utilizing small shuffling steps
(seven strides). Stride length (left leg) was measured using
the stride monitor, and from a post hoc video motion analysis
of the horizontal displacement of the left foot. Average stride
length was 12.7 cm (video analysis) and 10.4 cm (stride
monitor); mean difference was 2.5 cm (maximum 4.7 cm).
Thus, at two extremes of locomotor impairment in the PD
off state, the accuracy of the stride monitor was within that
established in the 10 healthy controls.
3.2. Monitoring of gait in Parkinsons disease
Fig. 3 illustrates the differences between healthy and
Parkinsonian gait over extended periods. Over 4 h a healthy

203

participant (37-year-old male) covered a total of 3.9 km with


3071 strides, including two 1.5-km walks in an urban
environment (Manhattan) at the start and end of the epoch
(Fig. 3A, upper trace). In the intervening period the
participant walked periodically while working in a
laboratory. Stride length was stable at 1.5 m, as indicated
by the stride histogram, consistent with the typical value for
adult males [26]. This is clearly seen in the 4 min of stride
data while walking home (Fig. 3A, lower trace). In contrast,
4 h of data from a PD patient (85-year-old female, age at
onset 79 years) during normal daily activities outside of the
clinic demonstrates the cardinal features of Parkinsonian
gait; namely a small (0.5 m), highly variable stride length
(Fig. 3B, upper trace and histogram), covering a distance of
492 m with 923 strides. Note that this particular patient was
not prescribed levodopa at the time of testing. Stride data
from a well-managed PD patient (65-year-old female, age at
onset 51 years) in the on phase approximately 2 h after
levodopa administration (levodopa 150 mg, pramipexole
1.5 mg) demonstrates the effectiveness of dopaminereplacement therapy (Fig. 3C). Over a 75-min period in
the clinic stride length was relatively stable at 1 m as
observed in a 4-min interval (Fig. 3C, lower trace) as the
participant walked along a corridor (although still less than
the mean value of 1.3 m for adult females [27]).
A standard dose of levodopa typically becomes effective
2040 min after drug ingestion [28], although onset can be
considerably delayed and inconsistent in patients with
advanced PD. The effect of levodopa on stride length was
monitored in the clinic (during intermittent 30-m walks along
a corridor) in an advanced PD patient (66-year-old male, age
at onset 40 years). Over a period of 75 min post-administration (levodopa 100 mg, pramipexole 0.5 mg) stride length
increased (and variability decreased) from 24 cm (S.D. 9) to
45 cm (S.D. 6) (Fig. 4A). Freezing occurred up to 30 min postmedication, but had ceased by 50 min. The time constant of
levodopa onset (28 min) was estimated from an exponential fit
to the mean stride data (Fig. 4B).
The levodopa cycle, characterized by changes in stride
length, was also assessed from long-term monitoring in the
community. A participant with advanced PD (79-year-old
female, age at onset 69 years) wore the stride monitor for 6 h
following a morning clinic visit. Stride length was
decreasing at the clinic as the patient came off a morning
dose of levodopa (levodopa 100 mg, ropinirole 2 mg). The
patient went to bed shortly after being driven home
(Fig. 5A). Approximately 10 min prior to getting out of
bed the participant took a second dose of levodopa (levodopa
100 mg, ropinirole 2 mg) then walked to a local shopping
mall. Stride length increased steadily over 60 min following
levodopa administration, and then declined as the participant
walked home (Fig. 5A). The time constants of the onset and
decay of levodopa (Fig. 5B) were estimated at 24 and
23 min, respectively, using an exponential fit to the mean
binned stride data (each bin comprising 60 sequential
strides).

204

S.T. Moore et al. / Gait & Posture 26 (2007) 200207

Fig. 3. (A) Four hours of stride data from a healthy participant. (B) Four hours of stride data from an unmedicated (i.e., no levodopa) PD patient during natural
daily activity outside of the clinic. (C) Stride data (75 min of intermittent walking around the clinic) from a well-managed PD patient in the on phase
approximately 2 h post levodopa administration.

S.T. Moore et al. / Gait & Posture 26 (2007) 200207

205

Fig. 4. The transition from off to on following levodopa administration was assessed in the clinic in a participant with advanced PD. (A) Stride data from
periodic walking along a corridor of length 15 m (up and back) following levodopa administration at 9:41 a.m. (B) The time constant (t) of the onset of levodopa
was estimated at 28 min using an exponential fit to the mean stride data.

206

S.T. Moore et al. / Gait & Posture 26 (2007) 200207

Fig. 5. The effect of levodopa administration during natural daily activities outside of the clinic. (A) Three hours of activity (mean and 90%CI of stride length,
plus individual values); thick black lines above the stride data indicate locomotion; thick grey lines show periods where the participant was supine. (B) An
exponential fit to binned mean stride length was used to estimate the time constant of onset (24 min) and decay (23 min) of levodopa.

4. Discussion
The results of this study demonstrate the feasibility of
accurate stride length measurement using a single shankmounted stride monitor, and the applicability of this
technique to long-term monitoring of gait in Parkinsons
disease. Improved accuracy (mean error 5 cm), relative to
previous techniques utilizing both single (15% error) [18]
and multiple (7 cm error) gyroscopes [20], was obtained
using a combined accelerometer/gyroscope sensor array and
a calibration algorithm to account for the forward motion of
the body over the stance foot. The stride monitor is small and
unobtrusive, and did not interfere with natural daily
activities during extended monitoring of gait outside of
the clinic.
Stride data obtained from PD patients demonstrated
many facets of Parkinsonian gait, such as small stride length
and larger stride-to-stride variability. Fluctuations of
efficacy associated with levodopa therapy, such as delayed
onset, wearing off, and the off/on effect, could also be
detected from long-term changes in stride length. The time
constants of onset and decay of levodopa were estimated
from stride length data acquired both at the clinic and in the
real world. In contrast, a previous laboratory study [29]
periodically assessed gait on a fixed 7-m walkway over the
levodopa cycle and found no consistent changes in stride
length, likely due to the contrived nature of the laboratory
walking task that can temporarily enhance performance in
PD patients [30]. Long-term gait assessment in a community

setting eliminates this confound and exhibits greater


sensitivity to the dynamic effects of dopamine replacement
therapy on stride length.
Locomotor impairment is one of the cardinal features of
PD but certainly not the only one. Many other PD symptoms,
such as rigidity, difficulty swallowing, stooped posture,
olfactory dysfunction, and upper-body tremor and dyskinesias, cannot be detected with the stride monitor; however,
no objective measures of these indicators are routinely used
in the clinic. Tremor can readily be measured with an
accelerometer but provides limited sensitivity to motor
complications in PD patients [11]. The complexity of
identifying off and on states and upper-body dyskinesias
(requiring six triaxial accelerometers [13]) effectively
curtails its use outside of the research environment. Despite
these recent attempts at objectivity, the essentially subjective
UPDRS remains the current standard of PD assessment.
Clinicians typically see a snapshot of the patients
motor state and management of PD often involves a trial and
error approach, relying heavily on the patients subjective
feedback to optimize the levodopa dosage regime. Objective
long-term data obtained from stride monitoring may provide
a faster and more valid end-point.

Acknowledgement
This work was supported by NASA grant NNJ04HF51G
(Steven Moore).

S.T. Moore et al. / Gait & Posture 26 (2007) 200207

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