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Dynamic postural control during simple and complex locomotor tasks in persons with early stage Parkinson’s disease

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Dynamic postural control during simple and complex locomotor tasks in persons with early stage Parkinson’s disease

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DYNAMIC POSTURAL CONTROL DURING SIMPLE AND COMPLEX
LOCOMOTOR TASKS IN PERSONS WITH EARLY STAGE PARKINSON’S
DISEASE

by

Jooeun Song

------------------------------------------------------------------------------------------------------------

A Dissertation Presented to the
FACULTY OF THE USC GRADUATE SCHOOL
UNIVERSITY OF SOUTHERN CALIFORNIA
In Partial Fulfillment of the
Requirements for the Degree
DOCTOR OF PHILOSOPHY
(BIOKINESIOLOGY)

May 2010

Copyright 2010 Jooeun Song
ii
DEDICATION

I dedicate this dissertation to my father, ChiHong Song, and my mother, EunAh
Yoo who have been tremendously supportive and provided me all the love,
strength, encouragement over all these years.

To my sister, Jooyoung Song, who continues to give love, strength, and support
throughout my life.

To my brother, SeungHo Song, who always encourages me to think positively.

With my heart-felt gratitude, to my fiancé, Eddy Jung, who has been inspiring me
with courage and giving me constant love, concern, and support.

iii
ACKNOWLEDGMENTS

Without the remarkable guidance and support of many people, it would not
have been possible for me to complete this dissertation. It is my pleasure to
acknowledge and thank them for their contributions. I would like to acknowledge
the financial support of the Division of Biokinesiology and Physical Therapy, the
Magistro Family Foundation Research Grant, the Grant-In-Aid Award at
American Society of Biomechanics, and the James Zumberge Research and
Innovation fund.
My deepest gratitude is to my graduate advisor and my committee
chairman, Dr. George Salem. His continues guidance, mentorship, and patience
helped me in developing my research skills. I would also like to thank Dr. Susan
Sigward for her continued support and encouragement; she has always been
willing to listen; Dr. Fisher who has brought me into this wonderful Parkinson’s
disease research area and has given me many insightful comments; Dr.
Petzinger for sharing with me much knowledge and experience in the area of
Parkinson’s disease; Dr. Azen whose valuable suggestions and knowledge in
statistics has contributed greatly to the analysis of my data.
I would like to give my appreciation to all of my colleagues in the
Musculoskeletal Biomechanics Research Laboratory. They have supported me in
many different ways and were always willing to share their time and provide help
over the past six plus years.

iv
This dissertation would not have been completed without the study
participants. I am grateful to each of them who were willing to donate their time
and energy with me.
Many friends have supported me through these many years in this foreign
country. I greatly value their friendship and I deeply appreciate their support and
encouragement.
v
TABLE OF CONTENTS

DEDICATION ii

ACKNOWLEDGMENTS iii

LIST OF TABLES vii

LIST OF FIGURES viii

ABBREVIATIONS AND OPERATIONAL DEFINITIONS x

ABSTRACT xii

CHAPTER I: OVERVIEW & SPECIFIC AIMS 1

CHAPTER II: LITERATURE REVIEW 5
Statement of the problem: 5
Definition of Parkinson’s disease (PD) 5
Basic neuro-anatomy of the basal ganglia and dopaminergic system 5
Neurophysiology of the dopaminergic system 6
The role of the dopaminergic system in regulating: 7
Movement velocity 7
Force control 8
Sequential movements 9
Pre-planned vs. on-line processed motor control 10
Postural control 11
Gait characteristics in persons with advanced PD 11
Gait characteristics in persons with early stage PD 12
Motor behaviors during more complex locomotor tasks 13
Measuring postural control: static condition 15
Measuring postural control: dynamic condition 16
Summary 17

vi

CHAPTER III: EFFECTS OF EARLY STAGE PARKINSON’S DISEASE
ON DYNAMIC POSTURAL CONTROL DURING GAIT
TERMINATION 18
Introduction 18
Methods 19
Participants 19
Protocol 21
Data analysis 22
Statistical Analysis 23
Results 24
Discussion 27

CHAPTER IV: ALTERED DYNAMIC POSTURAL CONTROL
DURING STEP TURNING IN PERSONS WITH
EARLY STAGE PARKINSON’S DISEASE 30
Introduction 30
Methods 31
Participants 31
Protocol 32
Data analysis 33
Statistical Analysis 35
Results 35
Discussion 39

CHAPTER V: THE INFLUENCE OF DIFFERENT TYPES OF TURNING
STRATEGIES ON DYNAMIC POSTURAL CONTROL IN
PERSONS WITH EARLY STAGE PARKINSON’S DISEASE 42
Introduction 42
Methods 44
Participants 44
Protocol 45
Data analysis 46
Statistical Analysis 47
Results 47
Discussion 50

CHAPTER VI: SUMMARY AND CONCLUSIONS 54

REFERENCES 58
vii
LIST OF TABLES

Table 1: Subject characteristics, Mean (standard deviation). 25

Table 2: Approach gait velocity during the step and the spin turn,
Mean (standard deviation). 47

Table 3: Each participant’s step versus spin turn ratio. 48
viii
LIST OF FIGURES

Figure 1: Schematic representation of task complexity
in locomotor tasks. 2

Figure 2: BG Circuit – Direct and indirect pathways. 6

Figure 3: Gait parameters during self-selected walking
in persons with EPD and HC participants
(Gold bar – EPD and Cardinal bar- HC). 13

Figure 4: Foot schematic representation for unplanned condition. 21

Figure 5: Calculation of dynamic postural control
in the AP and the ML direction. 24

Figure 6: The Peak COP-eCOM distances in the AP (A) and
the ML (B) direction between groups and conditions.
†denotes statistically significant difference (P<0.01). 26

Figure 7: Schematic representation of the COP and
the eCOM trajectories during the step turn.
Solid line: eCOM trajectory
Purple dotted line: COP trajectory
Phase 1: from approach step to pivot step;
Phase 2: from pivot step to acceleration step 34

Figure 8-1: The resultant COP -eCOM distance between groups
during the step turn cycle.
Gold line: Persons with early stage Parkinson’s disease
Cardinal line: Healthy controls
Gray shadow: Double limb support time
White shadow: Single limb support time
†denotes statistically significant difference
between groups (P<0.01).
*denotes statistically significant difference
between phases (P<0.05). 36

Figure 8-2: The COP-COG distance between groups
during the step turn cycle
Gold line: Persons with early stage Parkinson’s disease
Cardinal line: Healthy controls
Gray shadow: Double limb support time
White shadow: Single limb support time
†denotes statistically significant difference (P<0.01). 37
ix
Figure 8-3: The resultant COM velocity between groups
during the step turn cycle
Gold line: Persons with early stage Parkinson’s disease
Cardinal line: Healthy controls
Gray shadow: Double limb support time
White shadow: Single limb support time
†denotes statistically significant difference (P<0.01). 38

Figure 9: The resultant COP -eCOM distance between groups
during the step and the spin turn
Gold: Persons with early stage Parkinson’s disease
Cardinal: Healthy controls
Solid line: Step turn
Dotted line: Spin turn
Gray shadow: Double limb support time
White shadow: Single limb support time
†denotes statistically significant difference (P<0.01). 49

x
ABBREVIATIONS AND OPERATIONAL DEFINITIONS

Basal Ganglia (BG):
A group of subcortical nuclei (i.e. striatum, globus pallidus, substantia nigra, and
subthalamic nucleus) in the brain interconnected with the cerebral cortex,
thalamus, and brainstem, which help to regulate movements

Parkinson’s Disease (PD):
A progressive neurodegenerative disorder resulting from the loss of dopamine-
secreting cells in the BG, particularly in the region of the substantia nigra

Preplanning:
Formulating a motor program of action prior to execution of a movement

On-line processing:
Modification of the planned action, in response to environment stimuli, during a
movement

Posture:
The relative position of the various parts of the body with respect to one another
and to the environment

Postural Control:
The ability to alter the magnitudes and patterns of segmental kinematics (e.g.
trunk & limb movements) in order to direct body position in response to external
mechanical demands

Dynamic postural control:
The ability to alter the magnitudes and patterns of segmental kinematics in order
to direct body position in response to external mechanical demands during
movement

Postural instability:
Loss of equilibrium of body position

Center of Mass (COM)
The location of the equilibrium point of the total body mass

Center of Gravity (COG)
The location of the projected COM to the ground

Base of Support (BOS)
The greatest area within the lines connecting the outer perimeter of each of the
points where the body contacts the ground

xi
Center of Pressure (COP)
The equilibrium point of the distribution of the resultant ground reaction force
applied to BOS

Extrapolated Center of Mass (eCOM)
The modified COM position which is influenced by the COM velocity and leg
length

Persons with Early-Stage Parkinson’s Disease (EPD)
Diagnosed with Parkinson’s disease within the past 3 years and Hoehn & Yahr
stage 1 or 2

Healthy Control (HC) Subjects
Age and gender matched participants without any disease or disability

AP:
Anterior-Posterior

ML:
Medial-Lateral

xii
ABSTRACT
While persons with early stage Parkinson’s disease (EPD) typically
demonstrate minor levels of physical impairment and disability,
10,21
they often
have difficulty with transitional movements.
66
To date, most of the studies
evaluating such transitional movements in persons with PD have focused on
those individuals in advanced stages of the disease; little is known in regards to
persons with EPD. The primary objective of this dissertation was to characterize
dynamic postural control utilized in response to increased task demands during
transitional locomotor tasks in persons with EPD. To achieve this goal, three
separate studies were undertaken.
The purpose of study #1 was to compare dynamic postural control,
between persons with EPD and HC participants, during preplanned and
unplanned gait termination. Center of pressure (COP) and full body kinematics
(i.e., extrapolated center of mass [eCOM]) were used to quantify dynamic
postural control in 15 persons with EPD and 10 HC participants during
preplanned and unplanned stopping tasks. Compared to HC subjects, persons
with EPD exhibited significantly shorter distances in the AP direction, between
the COP and the eCOM during both stopping tasks. Group differences, however,
were not influenced by task type. These findings suggest that persons with EPD
adopt a more cautious postural control strategy, reducing the COM momentum
during both stopping tasks. Moreover, the results suggest that dynamic postural
control during gait termination is altered even in the early stages of PD.
xiii
The purpose of study #2 was to compare dynamic postural control
between persons with EPD and HC participants, during preplanned step turning.
Participant criteria, instrumentation, and data analysis for this experiment were
described in study #1. Participants were instructed to walk at self-selected pace
to a designated location and turn to the side of their dominant limb at a 90
°
angle.
The turning cycle was divided into two phases, based upon the three steps
(approach, pivot, and acceleration) required to complete the turn. The peak
distance between the COP and the eCOM was calculated during each phase.
Individuals with EPD demonstrated significantly shorter COP-eCOM distances
compared to HC subjects during both phases. These group differences were
influenced by both a shorter distance between the COP and the COM, and a
slower COM velocity. These findings further support that persons with EPD adopt
a more cautious movement strategy when transitioning from one walking
direction to another.
The purpose of study #3 was to: 1) compare turning preferences between
persons with EPD and HC participants, 2) examine the influence of EPD on
postural control during the spin turn, and 3) determine whether postural control
differences between subjects with EPD and HC participants are influenced by
turn type. Participant criteria for this experiment and details of instrumentation
and data analysis are described in study #1. The frequency of the step- and spin-
turn strategies was recorded for each participant. In addition, the peak COP-
eCOM distances produced during preplanned step and spin turns were examined.
Persons with EPD used the step turn strategy 1.4 times more frequently than the
xiv
spin turn when compared to age matched control subjects. Compared to the
control group, persons with EPD utilized shorter COP-eCOM distances during
both the step turn and the spin turn. Peak COP-eCOM distances were similar
between the two types of turn strategies within each group.
Taken together, findings from this dissertation provides evidence that
persons with EPD select a postural control strategy that decreases disequilibrium
and mobility, and increases stability, during more complex locomotor tasks.
Additionally, it demonstrates that functional impairments can be detected during
more complex locomotor activities, even in the early stages of PD, when clinical
signs of gait disturbance are often absent. This information may be used to
quantify disease severity, develop task specific interventions for persons with
EPD, and examine the effects of such interventions.
1
CHAPTER I
OVERVIEW
In order to appropriately prescribe safe and effective interventions to
increase or preserve functional independence in persons with Parkinson’s
disease (PD), the functional limitations and adopted compensatory strategies
associated with locomotion must be better understood. To date, however,
research involving locomotion in persons with PD has focused on the initiation of
movement,
28,45
or simple walking tasks that do not include changes in direction or
speed.
52,64,69
Functional walking, however, requires speed modulation and
directional changes events which occur frequently during activities of daily living
(ADLs). Although several studies have demonstrated the importance of the basal
ganglia and dopaminergic system in regulating: 1) acceleration & deceleration,
72

2) axial coordination,
74,75
and 3) postural control,
1,24
these studies are difficult to
extrapolate to overall ADLs or even locomotion, because they focused on
relatively simplistic, non-functional movement tasks such as upper-extremity
target tracing.
72,74,75
Additionally, it appears that both the occurrence and degree
of impairment associated with movement tasks in persons with PD are influenced
by prior knowledge (or lack of knowledge) of the task goals
4,39
and visual cueing
during movement performance.
18,40,42,59
The degree to which these factors
influence postural control during functional walking tasks, however, is poorly
understood. Lastly, these factors have not been examined in persons with early-
stage PD (EPD); yet, interventions that improve and/or preserve postural control
may be most effective in the early stages of the disease.
2
The objective of this dissertation was to characterize dynamic postural
control, quantified using the peak COP-eCOM distance, in persons with EPD
across a set of functional tasks with increasing complexity (Figure 1). This
information may be used to: 1) better identify the severity and progression of
locomotor impairment in EPD, and 2) appropriately prescribe safe and effective
interventions that increase or preserve functional independence. To accomplish
this goal, 3 studies with the following aims were proposed:

Figure 1. Schematic representation of task complexity in locomotor tasks.
3
SPECIFIC AIMS AND HYPOTHESES
Specific Aim 1: To compare dynamic postural control, (as quantified using the
peakCOP-eCOM distance), between persons with EPD and HC participants,
during preplanned and unplanned gait termination
Hypothesis 1.1: Persons with EPD would demonstrate smaller peak COP-
eCOM distances, compared to HC participants, during both preplanned and
unplanned gait termination.
Hypothesis 1.2: Persons with EPD and HC participants would demonstrate
greater peak COP-eCOM distances during unplanned, compared to
preplanned, gait termination.
Hypothesis 1.3: The magnitude of the difference in peak COP-eCOM
distance between groups would be greater in the unplanned condition
compared to the preplanned condition.

Specific Aim 2: To compare dynamic postural control, (as quantified using the
peak COP-eCOM distance), between persons with EPD and HC participants,
during preplanned step turning.
Hypothesis 2.1: Persons with EPD would demonstrate smaller peak COP-
eCOM distances compared to HC participants, during preplanned step turning.
Hypothesis 2.2: Smaller peak COP-eCOM distances observed in persons
with EPD would be influenced by smaller peak COP-COG distance but not by
COM velocity.

4
Specific Aim 3: To compare turning preference (step vs. spin) in persons with
EPD and HC participants, and to determine if postural control differences are
influenced by turn type.
Hypothesis 3.1: Persons with EPD would demonstrate a higher frequency of
step turns compared to HC participants.
Hypothesis 3.2: Persons with EPD would demonstrate smaller peak COP-
eCOM distances compared to HC participants during preplanned spin turn.
Hypothesis 3.3: The magnitude of the difference in peak COP-eCOM
distance between persons with EPD and HC participants would be greater
during the spin turn compared to the step turn.

5
CHAPTER II

LITERATURE REVIEW

STATEMENT OF THE PROBLEM
Definition and Incidence of Parkinson’s disease
PD is a progressive neurodegenerative disorder associated with several
motor impairments including bradykinesia, resting tremor, rigidity, and impaired
postural abnormalities.
58
The disease is characterized by reduced dopaminergic
function, with the first clinical signs appearing after approximately 80% of the
dopamine cells of the substantia nigra have degenerated.
20
PD is common
among older adults, affecting more than 10% of Americans.
50
Moreover, it is
predicted that 40 million people in the world will have this progressive
neurological condition within the next 10 years.
36
The incidence of early-onset PD
in the USA appears to be increasing and is currently 3 people per 100,000 per
year in those aged 30-49 years.
63

Basic Neuro-anatomy of the Basal Ganglia and Dopaminergic System
The dopaminergic system is regulated by the basal ganglia (BG) - a group
of subcortical nuclei comprised of the striatum, the external globus pallidus (GPe),
the internal globus pallidus (GPi), the substantia nigra, and the subthalamic
nucleus (STN).
34
Specifically, the striatum can be divided to the caudate nucleus
and the putamen. The substantia nigra includes the dopaminergic neurons in the
pars compacta (SNc) and the GABAergic (gamma-amino butyric acid) neurons in
the pars reticulate (SNr). The BG is involved in a complex loop connecting it to
6
various areas of the cortex. Information from the frontal, prefrontal, and parietal
areas of the cortex passes through the BG, and then returns to the
supplementary motor area via the thalamus. The BG is thus believed to facilitate
movement by channeling information from various regions of the cortex to the
supplementary motor area.

Neurophysiology: Direct and Indirect Pathways of the Dopaminergic
System

Figure 2. BG Circuit – direct and indirect pathways
Disruption of normal dopaminergic output from the substantia nigra interferes
with the complex BG circuit. The striatum receives excitatory input from the
cortex and other regions of the brain and projects to the nuclei via direct and
indirect pathways within the BG (Figure 2).
32,34
Activation of the direct pathway
7
results in net excitation of the thalamocortical circuits. On the other hand,
activation of the indirect pathway increases excitatory drive to the STN and the
BG output nuclei, resulting in inhibition of the thalamocortical circuit. As a result,
activation of the direct pathway facilitates movement, whereas activation of the
indirect pathway inhibits movement. Dopamine appears to enhance transmission
through the direct pathway and suppress transmission through the indirect
pathway. The net effect of dopamine, then, is to enhance movement.
Consequently, deficiency of dopamine inhibits the direct pathway and facilitates
the indirect pathway, resulting in bradykinesia, hypokinesia, or akinesis.

THE INFLUENCE OF THE DOPAMINERGIC SYSTEM DURING MOTOR
ACTIVITIES

Movement velocity
Previous studies have demonstrated that persons with reduced
dopaminergic function have difficulty increasing movement velocity.
71,72
For
example, Turner and colleagues used positron emission tomography to
investigate the functional neuroanatomy of the BG during medial and lateral
rotations of the shoulder under different movement velocities in healthy
participants.
72
Significant changes in regional cerebral blood flow, correlating
positivity with the velocity were found in left primary sensorimotor, left GP, and
right anterior cerebellum. The activation of GP discharges with increasing
movement velocity suggested that the BG motor circuit was involved
8
preferentially in scaling movement velocity. These findings were corroborated by
Turner and colleagues (2003) in a follow-up experiment.
71
In this study, cortical
and subcortical regions were less active with movements in persons with PD
than in healthy control (HC) participants. Regions of hypoactivation included the
left frontoparietal cortical regions, right globus pallidus, left insula, occipital lobe,
and ipsilateral and midline cerebellum. This impaired recruitment of cortical and
subcortical systems was pronounced with increasing movement velocity. Taken
together, the velocity-related activation of subcortical regions (i.e. globus
pallidus) supports the hypothesized role of the BG motor circuit in the
control of movement velocity.

Force Control
A number of studies have demonstrated the role of the BG in regulating
force control. Mak and colleagues reported that people with PD had reduced rate
of torque development while standing up from a sitting position compared to HC
participants.
43,61
Isometric force tracking and force aiming has also been
investigated in persons with PD.
37
Perhaps the most interesting finding was an
inability to precisely release force. Another recent investigation used functional
magnetic resonance imaging, to quantify the activation of cortical and subcortical
regions while healthy young adults pinched a grip device with their middle finger
and thumb to produce force.
73
All participants were required to produce force in
response to four different conditions: 1) fast pulse, 2) fast hold, 3) medium hold,
and 4) slow hold. Findings demonstrated an inverse relationship between the
9
rate of force production and activation of the subthalamic nucleus and internal
globus pallidus. Based upon these studies, it appears that the BG and
dopaminergic systems play an important role in modulating force
production and relaxation.

Sequential movements
Persons with PD have difficulty in planning and performing sequential or
simultaneous motor acts. A convincing set of data demonstrate that persons with
PD have difficulty in assembling movement components, such as transport and
grasp during a reaching task.
2,11
Similarly, Vaugoyeau and colleagues reported a
delayed onset of pelvic rotation with respect to the shoulder during stepping
tasks in persons with PD.
74,75
The findings were consistent with those reported by
Poizner and colleagues (2000) who also proposed that the temporal
coordination of different body segments were disrupted in persons with PD.
60
To
test this hypothesis, they had participants track a target while pointing with their
dominate arm and sitting in a chair. To reach the target, participants moved with
a combination of arm and trunk movements. While the control participants
performed synchronized or well-coordinated arm and trunk motions, persons with
PD demonstrated large time intervals between arm and trunk motions at the
beginning and termination of movement. Taken together, these studies
demonstrate the importance of the dopaminergic system in regulating the
temporal coordination of different body-segment motions.

10
Pre-planned vs. On-line Processed Motor Control
Recent evidence suggests that motor impairments associated with PD are
exaggerated when the task requires on-line processing. During on-line
processed tasks, the participants are instructed to perform one of several
movement alterations (e.g. stop or turn right) in response to an external cue (e.g.
lighted arrow). During preplanned activities, participants are instructed to
perform a given task in advance of movement initiation.
Bishop and colleagues demonstrated that the inability to generate
breaking force during gait termination was magnified when the task required on-
line processing.
4
Similarly, Leis and colleagues (2005)

demonstrated that when
directions were given during a movement, as opposed to before movement
initiation, both reaction time and execution time were longer in persons with PD
compared to HC participants.
39
Additionally, longer reaction time and movement
time with the on-line processing were exacerbated with more complex tasks:
from discrete to sequential movements of the upper extremity. Taken together,
these findings suggest that the degree of motor impairment associated
with advanced PD is influenced by complex interactions between the
degree of difficulty of the movement and amount of prior knowledge of the
task.

11
Postural Control
Posture is defined as “the relative position of the various parts of the body
with respect to one another and to the environment”.
15
When body position
cannot be maintained in response to these demands, there is postural
instability and an increased risk of falling. Researchers have hypothesized that
persons with PD have postural instability because of: 1) increased muscular
coactivation;
19
2) impaired hip, trunk, and arm muscle responses;
9
and 3)
increased center of mass (COM) displacements.
31
Additionally, postural control
is correlated with self-reported psychological reactions including fear of falling in
persons with PD.
1,24
For example, Franchignoni and colleagues demonstrated
that postural instability during the Berg Balance Test resulted from complex
interactions among motor impairments, reduced physical capabilities, and fear of
falling.
24
Moreover, Adkin and colleagues (2003) reported that persons with PD
had significantly reduced balance confidence, as measured by the Activities-
specific Balance Confidence (ABC) scale compared with HC participants.
1

ADVANCED PD GAIT CHARACTERISTICS
Spatio-temporally, PD gait is characterized by a reduced walking speed,
stride length and an increased double limb support time / decreased single limb
support time.
52,64,69
Biomechanically, gait in persons with advanced PD is
associated with decreased peak joint angles, moments, and powers.
64,69
Although a number of studies have quantified altered gait parameters in persons
with PD, these previous analyses were limited to investigations using persons
12
with advanced stage PD. Although several studies have characterized
postural instability in persons with PD during standing and simple pre-
planned walking tasks, postural control strategies during more complex
locomotor tasks in persons with EPD have not been well characterized.

EPD GAIT CHARACTERISTICS
In our preliminary study , thirty persons with EPD, defined as being diagnosed
within the past 3 yrs and Hoehn & Yahr stage 1-2, performed three 6-meter
walking trials at two movement speeds: 1) self selected (SS), and 2) “as fast as
possible” (AFAP). Ground reaction forces (GRFs) were measured at 1560Hz and
an 8-camera motion analysis system (60 Hz) was used to quantify segment
kinematics and joint range of motion. The net joint moments were calculated
using standard inverse dynamics procedures. Paired t-tests were used to assess
the differences between walking conditions (P < 0.05). Data for gait
characteristics in HC participants were obtained from published report.
35
There
were no group differences in gait velocity or stride length during SS and AFAP
walking (P > 0.05; Figure 3). In addition, individuals with EPD increased their
walking speed by preferentially increasing hip ROM, and both hip and knee
NJMs, without altering ankle mechanics in agreement with previous reports
regarding HC participants.
35
These findings suggest that simple straight
walking at a self-selected pace or as fast as possible, does not adequately
discriminate motor impairment between persons with EPD and HC
participants.
13

Figure 3. Gait parameters during self-selected walking in persons with EPD and
HC participants
Gold bar: Persons with early stage Parkinson’s disease
Cardinal bar: Healthy control participants

MOTOR BEHAVIORS DURING MORE COMPLEX LOCOMOTOR TASKS
In the “real world”, humans must ambulate within their environmental
constraints, responding not only to expected obstacles (e.g. furniture), but also to
sudden events (e.g. changing light signals). Moreover, persons with EPD report
having trouble negotiating obstacles and doorways and difficulty in turning.
66

Persons with advanced PD are five times more likely to experience a fall-related
injury during turning than the generally healthy older population.
6,67,68
Moreover,
falls and freezing behavior occur more frequently when the activity requires on-
line processing.
3
These reports along with our earlier pilot studies suggest that
14
we are more likely to observe differences in movement dynamics between
persons with EPD and HC participants when examining more complex functional
motor behaviors. Turning while walking is one such behavior that requires: 1)
deceleration of the body, 2) controlled rotation of the axial segments, and 3)
acceleration of the body.
8,27,56,79
In addition, Taylor and colleagues reported that
every ten steps, two turns are used to carry out everyday activities.
70
A recent
study by Crenna and colleagues (2007) demonstrated that persons with EPD
completed turning with reduced maximum of head-trunk relative rotation, as well
as reduced head rotation. Moreover, persons with EPD started rotating their
head and the trunk almost simultaneously, whereas HC participants started
turning their head toward the intended direction of travel followed by rotation of
their trunk.
17
However, they focused their investigation on the spatial and
temporal relations among axial segment rotations during turning.
17
They did not
examine measures of dynamic postural control during turning, or the influence of
on-line processing. Therefore, it may be necessary to examine postural
control associated with more complex activities, such as gait termination
and turning tasks, in order to differentiate between these cohorts.

15
MEASURING POSTURAL CONTROL: STATIC CONDITION
Postural control is the ability to alter the magnitude and patterns of
segmental kinematics (e.g. trunk & limb movements) in order to direct body
position in response to external mechanical demands imposed during static and
dynamic tasks such as turning.
15,31
The most common method for quantifying
postural control is based upon the movements of center of mass (COM).
5
The
COM represents the location of the balance point of an object, where the mass of
the system is evenly distributed and the torques acting on the system, in all
directions, are equal.
46

A person is said to be “posturally stable” whenever the line of action of the
person's COM referred to as COG passes through (within) their BOS.
46
The BOS
is defined as the greatest area within the lines connecting the outer perimeter of
each of the points where the body contacts the ground. If the COG falls outside
of the BOS, the system is not in equilibrium. Additionally, when the COG is
within the BOS, the closer the COG is to the border of the BOS, the less stable
the system becomes. On the other hand, if the COG falls outside of the BOS, the
farther the COG is away from the border of the BOS, the less stable the system
becomes. By far, the majority of studies examining postural control in HC
participants and persons with advanced PD have utilized static assessments
performed during standing.
12,19,25,31,77,78
These studies have demonstrated that
body sway increases (measured as the COM displacement or the COP
displacement) as a function of normal aging
25,77
and disease, such as PD.
19,31

16
MEASURING POSTURAL CONTROL: DYNAMIC CONDITION
Dynamic postural control is the ability to alter the magnitude and patterns
of segmental kinematics in order to direct body position in response to external
mechanical demands imposed during movements.
41
Dynamic postural control is
more difficult than static postural control because during dynamic activities, the
BOS is continually changing both its location and area. Moreover, the loss of
dynamic postural control contributes to falls during ADLs.
29,48,62
Unlike a static
assessment, the calculation of postural control in a dynamic situation must take
into account not only the position of the COG but also the effects of the
magnitude and direction of the COM velocity.
30
Forward progression of the COM
during dynamic tasks (i.e. gait) requires a forward rotation of the COM around the
supporting limb during each consecutive step. Hof illustrated this concept by
invisioning the body as an inverted pendulum, where the axis of rotation of the
pendulum is the ankle joint of the supporting limb, and the COM moves in an arc
motion.
30
The linear COM velocity moving along this arc is related to the length of
the “pendulum” or limb. Hof and colleagues termed this relationship the natural
frequency of the pendulum which is equivalent to leg length.
30
The natural
freqency is calculated as √ (g/l) where g is the acceleration of gravity and l is the
length of the leg measured from the ankle joint center to the COM. Consequently,
when the COM velocity is normalized by this frequency and added to the COM
position, it creates a new COM position which is influenced by the COM velocity
and the natural frequency. Hof termed this variable the “extrapolated centre of
mass” (eCOM) (equation1).
17

eCOM = COG + (COM vel/ √ (g/l)) (equation 1)
Consequently, the distance between the COP and the eCOM is used to quantify
dynamic postural control during locomotor tasks (equation 2).
30

Dynamic Postural Control = COP- (COG + COM vel/ √ (g/l) (equation 2).

SUMMARY
The BG and dopaminergic system are important modulators of
acceleration & deceleration, axial coordination, postural control, and on-line
motor processing; however, PD studies to date have focused on relatively
simplistic movement tasks, such as preplanned upper-extremity target tracing,
walking, and gait initiation. Moreover, these factors have not been examined in
persons with EPD; yet, interventions that improve and/or preserve postural
control may be most effective in the early stages of the disease.

18
CHAPTER III
EFFECTS OF EARLY STAGE PARKINSON’S DISEASE ON DYNAMIC
POSTURAL CONTROL DURING GAIT TERMINATION
INTRODUCTION
Persons with early-stage Parkinson’s disease (EPD) typically demonstrate
few clinical symptoms and minimal levels of functional impairment during simple
locomotor tasks. For example, during self-selected and fast walking, gait velocity
and stride length are similar when compared to healthy age-matched
individuals.
10,21
Nonetheless, self-reports and biomechanical studies suggest that
persons with EPD have difficulty with transitional movements including turning.
66

Gait termination is another transitional activity that has received attention
in persons with advanced PD, but not in those with EPD.
4,55
Gait termination can
be challenging, because the central nervous system must act to control braking
forces, both in magnitude and direction, so that the center of mass (COM) is
positioned within the base of support (BOS).
26,47
These challenges can be
magnified during common activities of daily living, when gait termination is
triggered by obstacles suddenly coming to attention. The effects of preplanned
versus unplanned gait termination in persons with advanced PD were recently
examined by Bishop and colleagues.
4
They reported that persons with advanced
PD adopted different muscle activation patterns during preplanned and
unplanned stopping, compared to healthy control participants Although not
reported in the study, these differences are likely to influence control of the
body’s COM and ultimately the postural control strategies adopted during this
19
task. Oates and colleagues (2008) recently reported that persons with advanced
PD demonstrated slower walking velocity, shorter steps, and altered postural
control by measuring the distance between the BOS and the extrapolated COM
(eCOM) during both preplanned and unplanned gait termination compared to
healthy control(HC) participants.
55
Although both of these studies demonstrated
that gait termination is altered in the advanced stages of PD, neither study
quantified the influence of EPD on this important activity of daily living.
Therefore, the purpose of this investigation was to evaluate the influence
of EPD on gait termination by quantifying the postural control strategies adopted
during preplanned and unplanned gait termination tasks. We hypothesized that
persons with EPD would demonstrate decreased peak COP-eCOM distances
during both preplanned and unplanned gait termination, and that these
differences would be magnified in the unplanned condition. Information from this
investigation may provide the basis for 1) designing objective functional
performance evaluations for persons with EPD and 2) prescribing safe and
effective interventions to increase and/or preserve functional independence in
this cohort.

METHODS
Participants
Fifteen persons with EPD and ten HC subjects participated. A diagnosis of
idiopathic EPD was confirmed by a fellowship trained movement disorder
specialist.
20
Participants with EPD were tested in the “on” medication state (i.e., fully
responding to their PD medications). At the time of testing, none of the
participants exhibited dyskinesia, dystonia, or other signs of involuntary
movement.
Inclusion criteria for the study were the following: (1) age 18 years old,
(2) able to ambulate at least 14 meters (time not measured) without a walker or
other devices, (3) persons diagnosed with PD within 3 years,
65
(4) Hoehn & Yahr
stage 1-2 (5) stable in PD medications, and (6) age and gender-matched healthy
control participants. The following criteria were used to exclude participants from
the study: (1) surgical intervention for persons with PD, (2) Mini Mental State
Exam (MMSE) score < 24,
23
(3) co-morbidities affecting gait (diabetes,
musculoskeletal injury, arthritis), (4) severe vision problems, and (5) pregnancy.
All testing took place in the Musculoskeletal Biomechanics Research
Laboratory at University of Southern California. Procedures were explained to
each participant and each participant signed an informed consent form approved
by the Institutional Review Board of the University of Southern California.

21
Protocol

Figure 4. Foot schematic representation for unplanned condition.
For the preplanned condition, participants were instructed to walk 4
meters at a self-selected pace and then terminate walking by stepping with the
leading limb immediately after two targeted stanchions, and placing the trailing
limb next to the leading limb. For the unplanned condition, participants were
again instructed to walk at a self-selected pace and “stop as soon as possible” in
response to a light signal during randomly selected trials. The light signal was
triggered at heel strike one step prior to the force plate (Figure 4).
4
Trials in which
participants took additional steps were not analyzed. The sequence of the
conditions was randomized. Kinematic data was sampled at 60Hz using a motion
analysis system (Vicon 612, Oxford Metrics LTD. Oxford, England). Reflective
markers (14 mm spheres) were placed bilaterally on the skin over specific
anatomical landmarks including the anterior, posterior, and lateral head,
22
acromion processes, anterior and posterior shoulders, greater tubercles of
humerus, medial and lateral humeral epicondyles, medial and lateral wrists, third
metacarpo phalangeal joints, 7
th
cervical vertebrae, sternoclavicular notch, iliac
crests, anterior superior iliac spines, posterior superior iliac spines, L5-S1 joint,
medial and lateral femoral epicondyles, medial and lateral malleoli, first and fifth
metatarsal heads, and first proximal/distal phalanx. Additionally, cluster markers
were placed with a band over the upper arms, lower arms, thighs, shanks, and
shoe heels. Reflective markers were identified manually within the VICON
Workstation software and then imported into Visual 3D software (C-Motion,
Rockville, MD). 3D marker coordinates were low-pass filtered at a cut-off
frequency of 6Hz.
Data Analysis
The position of the total body COM was defined using the weighted sum of
the COM of all 15 segments. The COG was calculated based on the medial-
lateral and the anterior-posterior locations of the COM. Instantaneous velocity of
the total body COM (COM
vel
) was computed from the linear total body COM
positions (COM
pos
) using the following equation 1:
COM
vel n
= [COM
pos

n+1
– COM
pos

n-1
] / 2 ∆t where, n = event frame
(equation 1)
COP was determined from force plate measurements (AMTI force plate 1.2m x
1.2m, 1560Hz).

23
To quantify postural control during gait termination, the distance between
the COP and the eCOM (COG + COM vel/ √ (g/l)) was calculated and averaged
across three successful trials, using the methodology previously described by
Hof (equation 2).
30

Postural Control = COP- (COG + COM vel/ √ (g/l) (equation 2)
The peak COP-eCOM distances in the anterior-posterior (AP) and in the
medial-lateral (ML) direction were calculated during the period from the heel
strike of the leading limb to the heel strike of the trailing limb during the period
when COM deceleration is greatest (Figure 5). The heel strike of each limb was
determined by the force plate. The average approach velocity across three
successful trials was also recorded.
Statistical Analysis
Two-way repeated measure 2 X 2 (group x condition) ANOVAs were used
to determine if postural control in the AP and ML directions differed between
persons with EPD and HC participants and the two stopping conditions. All
statistical analyses were performed using SPSS 15.0 (Chicago, IL) with an alpha
level set of 0.05.

24

Figure 5. Calculation of dynamic postural control in AP and ML directions.
Black foot print: the leading limb
Gray foot print: the trailing limb
Purple dotted line: trajectory of the COP
Black solid line: trajectory of the eCOM
Purple circle: an example of the location of the COP
at the heel strike of the leading limb
Black circle: an example of the location of the eCOM
at the heel strike of the leading limb
COP: center of pressure, eCOM : extrapolated center of mass
AP: anterior-posterior, ML: medial-lateral

RESULTS
Participant characteristics are provided in Table 1. There were no
significant group differences for age, height, or weight. (P > 0.05). There were
also no significant differences for approach gait velocity in either the preplanned
(1.41± 0.12 vs. 1.51 ± 0.12 m/s; P > 0.05) or unplanned condition (1.42 ± 0.11 vs.
1.48 ± 0.14 m/s; P > 0.05).
25
Table1. Mean and standard deviation of participant’s characteristics
Group
EPD HC Significance
Age (yr) 62 (9.1) 60 (8.5) p =0.57
Height (m) 1.68 (0.07) 1.72 (0.09) p =0.33
Weight (kg) 68.9 (12.1) 74.8 (17.2) p =0.20
Mean (SD)
EPD: Persons with early stage Parkinson’s disease
HC: Healthy Controls

Significant main effects of group and condition were found for the peak
COP-eCOM distance (P < 0.05). When compared to HC participants, persons
with EPD demonstrated significantly shorter COP - eCOM distances in the AP
direction during both preplanned (71.5% difference; 0.07± 0.04 vs. 0.12 ± 0.03 m;
P = 0.004) and unplanned (25% difference; 0.20 ± 0.04 vs. 0.25 ± 0.05 m; P
=0.004) conditions (Figure 6). The effect sizes for the mean differences in the
COP-eCOM distances between the two groups were 1.41 for preplanned
condition and 1.10 for unplanned condition, indicating large group difference
effects. In contrast with the AP direction, there were no group differences in the
COP-eCOM distances in the ML direction during either condition (F=0.92, 1.453;
P > 0.05).
For both groups, the distances between the COP and the eCOM in the
unplanned condition were greater than those in the preplanned condition (p <
0.001). There were no interaction effects.

26

Figure 6. The Peak COP-eCOM distance in the AP (A) and the ML (B) direction
between groups and conditions
Gold: persons with early stage Parkinson’s disease
Cardinal: Healthy control participants
AP: anterior-posterior, ML: medial-lateral
† denotes P <0.01

27
DISCUSSION
This study identified significant postural control differences in persons with
EPD compared to HC participants during gait termination. Persons with EPD
demonstrated shorter distances between the COP and the eCOM in the AP
direction during both the preplanned and unplanned gait termination tasks. There
was, however, no group difference in the ML direction. Compared to preplanned
condition, both groups demonstrated greater peak COP-eCOM distances in the
AP direction in unplanned condition.
Our findings of altered postural control during gait termination support the
notion that persons with PD often have difficulty with set-shifting tasks.
11,60

Specifically, a convincing set of data demonstrate that persons with advanced
PD manifest problems in assembling and switching from one phase to another
during sequential movements, such as transport and grasp during a reaching
task.
11,60
In addition, previous reports demonstrated that the temporal
coordination of body segments is disrupted in persons with advanced PD during
sit-to-stand tasks and stepping activities.
42,74,75
Using a smaller COP-eCOM
distance during gait termination reduces the torque demands of the
neuromuscular system. Perhaps more important, it also reduces the risk of the
COP falling outside of the base of support, and therefore fall risk. Decreased
muscular strength,
53
rate of force development,
43,61
muscle coordination,
4
and
balance control,
5,24
which are all well established consequences of advanced PD,
may influence gait termination strategies in persons with EPD. Further studies
correlating COP-eCOM distance with other attributes of physical performance will
28
be needed to tease out these potential underlying mechanisms. Additionally,
psychological considerations, including fear of falling
1
and reduced balance
confidence
24
may also influence the COP-eCOM distances.
The results of the current study are consistent with a previous study by
Oates and colleagues.
55
They reported that persons with advanced PD also
demonstrated shorter BOS-eCOM distance in the AP direction during both
preplanned and unplanned gait termination compared to HC participants. Our
findings, expand upon this report and suggest that dynamic postural control is
altered even in the early stages of PD. Similar to our results, Oates and
colleagues found that no group difference of the ML BOS-eCOM distance in
either the preplanned or unplanned condition.
55
Our results of altered postural control in the AP direction but not in the ML
direction are consistent with other reports of direction-specific postural instability
in persons with PD.
31
Horak and colleagues reported that persons with advanced
PD had greater difficulty modifying their postural responses in the direction of the
perturbation, and these effects were magnified in the AP direction.
31

Both groups demonstrated greater COP-eCOM distances during
unplanned gait termination compared to the preplanned condition. These findings
parallel those of a previous investigation by Hase and colleagues.
26
They
reported that healthy individuals increased the magnitude of muscle activation in
the unplanned condition when compared to the preplanned condition.
26
Because
greater peak COP-eCOM distances are likely to be associated with greater
muscle activity and kinetics, we extrapolated upon this idea and hypothesized
29
that the difference in COP-eCOM distances between persons with EPD and HC
participants would be magnified in the unplanned condition. The results of the
current study, however, did not support our hypothesis. The findings suggest
that both groups increase their COP-eCOM distance to a similar extent in the
unplanned compared to the planned condition.
The findings of the current study provide evidence that functional
impairments can be detected even in the early stages of PD, when clinical signs
of gait disturbance are often absent.
13
This information may be used to quantify
disease severity, develop task specific interventions for persons with EPD, and
quantify the effects of such interventions.

30
CHAPTER IV
ALTERED DYNAMIC POSTURAL CONTROL DURING STEP TURNING
IN PERSONS WITH EARLY STAGE PARKINSON’S DISEASE
INTRODUCTION
Postural control is the ability to alter the magnitude and patterns of
segmental kinematics (e.g. trunk & limb movements) in order to direct body
position in response to external mechanical demands imposed during static and
dynamic tasks such as turning.
15,31
Functional independence, and consequently
quality of life is compromised in individuals with postural control deficits. Persons
with early stage PD (EPD) typically demonstrate few clinical symptoms and
minimal levels of functional impairment, such as reduced gait velocity and stride
length, during simple movement tasks including straight walking.
10,21
However,
they often demonstrate altered postural control during standing tasks
13
and report
difficulty with turning.
66
In persons with advanced PD, difficulty with turning is a
sensitive indicator of a higher prevalence of freezing and falling.
8,76

Turning presents unique challenges to individuals with impaired postural
control because

it requires them to initiate a state of disequilibrium in order to
change directions during an ongoing movement.
79
This disequilibrium requires
separation of the center of gravity (COG) and the center of pressure (COP) of the
individual where the COG represents the vertical projection of the center of
mass (COM) on the ground and the COP is the equilibrium point of the
distribution of the resultant ground reaction force applied to the base of
support.
12,16,33
Despite reports of difficulty turning in persons with EPD, studies to
31
date have not characterized the postural control strategies used during turning in
this cohort. Early identification of these strategies may be used to develop
effective intervention protocols that: 1) improve turning capabilities, 2) increase
balance confidence and 3) reduce fall risk and fear of falling in persons with EPD.
Therefore, the purpose of this study was to characterize the differences in
postural control during a step turning activity, between persons with EPD and
healthy age-matched control (HC) participants. We hypothesized that persons
with EPD would use a dynamic postural control strategy, which reduces the
demands of the neuromuscular system, compared to HC participants.

METHODS
Participants
Fifteen persons with EPD and 10 HC subjects participated. A diagnosis of
idiopathic PD was confirmed by a fellowship trained movement disorder
specialist. Participants with EPD were tested in the “on” medication state (i.e.,
fully responding to their PD medications). At the time of testing, none of the
participants exhibited dyskinesia, dystonia, or other signs of involuntary
movement.
The inclusion criteria for the study were the following: (1) age 18 years
old, (2) able to ambulate at least 14 meters (time not measured) without a walker
or other devices, (3) persons diagnosed with PD within 3 years,
65
(4) Hoehn &
Yahr stage 1-2, (5) stable in PD medications, and (6) age and gender-matched
HC participants.
32
The following criteria were used to exclude participants from the study: (1)
surgical intervention for persons with PD, (2) Mini Mental State Exam (MMSE)
score < 24,
23
(3) co-morbidities affecting gait (diabetes, musculoskeletal injury,
arthritis), (4) severe vision problems, and (5) pregnancy.
All testing took place in the Musculoskeletal Biomechanics Research
Laboratory at University of Southern California. Procedures were explained to
each participant and each participant signed an informed consent form approved
by the Institutional Review Board of the University of Southern California.
Protocol
Participants walked 4 meters at a self selected pace and turned to their
dominant direction (the direction of the limb with which side they would kick a ball)
at a 90
°
angle, at a location designated by stanchions. The starting point was
adjusted so that the subjects performed a step turn for each trial. A step turn is
defined as a change in direction opposite to the pivot foot.
17,27,70

Kinematic data was sampled at 60 Hz using a motion analysis system
(Vicon 612, Oxford Metrics LTD. Oxford, England). Reflective markers (14 mm
spheres) were placed bilaterally on the skin over specific anatomical landmarks
including the anterior, posterior, and lateral head, acromion processes, anterior
and posterior shoulders, greater tubercles of humerus, medial and lateral
humeral epicondyles, medial and lateral wrists, third metacarpo phalangeal joints,
7
th
cervical vertebrae, sternoclavicular notch, iliac crests, anterior superior iliac
spines, posterior superior iliac spines, L5-S1 joint, medial and lateral femoral
epicondyles, medial and lateral malleoli, first and fifth metatarsal heads, and first
33
proximal/distal phalanx. Additionally, cluster markers were placed with a band
over the upper arms, lower arms, thighs, shanks, and shoe heels. Reflective
markers were identified manually within the VICON Workstation software and
then imported into Visual 3D software (C-Motion, Rockville, MD). 3D marker
coordinates were low-pass filtered at a cut-off frequency of 6Hz.
Data Analysis
The position of the total body COM was defined using the weighted sum of
the COM of all 15 segments. The COG was calculated based on the medial-
lateral and the anterior-posterior locations of the COM. Instantaneous velocity of
the total body COM (COM
vel
) was computed from the linear total body COM
positions (COM
pos
) using the following equation 1:
COM
vel n
= [COM
pos

n+1
– COM
pos

n-1
] / 2 ∆t where, n = event frame
(equation 1)
The gait cycle phases were determined using a force plate and the vertical
velocity of the virtual center of each foot.
54
COP was determined from force plate
measurements during single and double limb stance (AMTI force plate 1.2m x
1.2m, 1560Hz).
To quantify postural control during turning, the distance between the COP
and the extrapolated COM (eCOM) (COG + COM vel/ √ (g/l)) was calculated
during three successful trials, using the method previously described by Hof
(equation 2).
30

Postural Control = COP- (COG + COM vel/ √ (g/l) (equation 2).
34
The natural freqency was calculated as √ (g/l) where g is the acceleration of
gravity and l is the length of the leg measured from the ankle joint center to the
COM.
Three consecutive steps during the turn: the approach step, the pivot step,
and the acceleration step where used to define two phases of turning.
17
Phase 1
was defined from the heel strike of the approach step to the heel strike of the
pivot step. Phase 2 was defined from the heel strike of the pivot step to the heel
strike of the acceleration step. The peak distance between the COP and the
eCOM was quantified during each phase (Figure 7). The average approach
velocity across three successful trials was also recorded.

Figure 7. Schematic representation of the COP and the eCOM trajectories
during the step turn.
Dotted purple line: COP trajectory
Solid line: eCOM trajectory
Phase 1: from approach step to pivot step; Phase 2: from pivot step to
acceleration step

35
Statistical Analysis
To determine if differences in postural control existed between persons
with EPD and HC participants across turning phases, a 2 x 2 (group x phase)
ANOVA was performed. In the case in which differences in postural control were
found between groups, independent t-tests were performed to determine if group
differences existed in the position of the COG relative to the COP and in the
COM velocity. All statistical analyses were performed using SPSS 15.0 (Chicago,
IL) with an alpha level set of 0.05.

RESULTS
There were no significant group differences for approach gait velocity
during the step turn (1.35±0.14 vs. 1.46±0.14 m; EPD vs. HC; P > 0.05).
There was a main effect of group and phase for postural control. Persons
with EPD demonstrated statistically significant shorter peak COP-eCOM
distances compared to HC participants during both Phase 1 (20.6% difference;
0.34±0.05 vs. 0.41±0.06 m; P < 0.01) and Phase2 (21.1% difference; 0.38±0.06
vs. 0.46±0.07 m; P = 0.01) of the step turn (Figure 8-1). The effect sizes for the
mean differences in the COP-eCOM distances between the two groups were
1.27 for Phase1 and 1.23 for Phase2, indicating large difference effects.
Additionally, the distances between the COP and the eCOM in Phase 2 were
greater than those in Phase 1 (P < 0.05).

36

Figure 8-1. The resultant COP -eCOM distance between groups during the step
turn cycle
Gold line: Persons with early stage Parkinson’s disease
Cardinal line: Healthy controls
Gray shadow: Double limb support time
White shadow: Single limb support time
†denotes statistically significant difference between groups (P<0.01)
*denotes statistically significant difference between phases (P<0.05)

37
Compared to control participants, persons with EPD demonstrated
statically significant shorter peak COP-COG distances during both Phase 1 (30.8%
difference; 0.13±0.03 vs. 0.17±0.03 m; P = 0.001) and Phase2 (28.6% difference;
0.21±0.05 vs. 0.27±0.04 m; P < 0.05; Figure 8-2).

Figure 8-2. The COP-COG distance between groups during the step turn cycle
Gold line: Persons with early stage Parkinson’s disease
Cardinal line: Healthy controls
Gray shadow: Double limb support time
White shadow: Single limb support time
† denotes P <0.05

38
Although there was no significant difference in the approach gait velocity
between groups, persons with EPD exhibited significantly slower COM velocity
when compared with control participants during both turning phases (0.64±0.10
vs. 0.74±0.10 m/s and 0.41±0.11 vs. 0.63±0.08 m/s; P < 0.05; Figure 8-3). The
effect sizes for the mean differences in the COM velocity between the two groups
were 1.00 for Phase1 and 2.29 for Phase 2.

Figure 8-3. The resultant COM velocity between groups during the step turn
cycle
Gold line: Persons with early stage Parkinson’s disease
Cardinal line: Healthy controls
Gray shadow: Double limb support time
White shadow: Single limb support time
† denotes P <0.05

39
DISCUSSION
This study identified significantly different postural control strategies in
persons with EPD during step turning activities compared to HC participants.
Persons with EPD utilized shorter distances between the COP and the eCOM
during the single limb stance period of both Phase 1 (from the approach to the
pivot step), and Phase 2 (from the pivot to the acceleration step), compared to
HC participants. The shorter distances between the COP and the eCOM in
persons with EPD were influenced by two factors: the shorter peak distance
between the COP and the COG and slower COM velocity during the turn.
Our results are consistent with self-reports that persons with EPD,
diagnosed for 4 years and mildly to moderately disabled, have “difficulty in
turning”.
66

Turning is a challenging task which requires deceleration of the COM,
rotation of the axial segments, and acceleration of the body in the new
direction.
27,79
Persons with PD have difficulty assembling and switching from one
movement component to another during sequential tasks
2,11,14,49
and the temporal
coordination of body segments is disrupted during functional activities.
17,74,75

During the turning sequence, individuals must control a state of disequilibrium
between the COP and the eCOM. Although separation of the COP and the
eCOM creates greater momentum during the turn, it also requires increased
neuromuscular control (e.g., neural drive, muscle forces, and joint powers) to
redirect and control this momentum. Our findings suggest that persons with EPD
select a motor control strategy that limits separation of the COP and the eCOM,
40
thereby reducing the mechanical and postural challenges of controlling the COM.
These findings are also consistent with those of Hass and colleagues during gait
initiation.
28
The separation between the COP and the COM was less during the
end of the single support phase of gait initiation in persons with advanced PD,
suggesting an inability to produce sufficient momentum or preserving stability to
compensate impaired postural control. Similarly, Buckley and colleagues
demonstrated limited COM movements, resulting in shorter distances between
the COP and the COM during sit- to-walk transitions in persons with advanced
PD.
7

There are several possible explanations for this movement strategy. First,
a shorter distance may be in response to reduced lower extremity muscle
strength in persons with PD.
53
Hahn and Chou noted that a smaller COP-COG
distance reduces the magnitude of the muscular force required to control the
COM because it decreases the moment arms created for the body weight vector
acting around centers of joint rotation in the supporting limb.
28,33
Psychological
considerations, including increased fear of falling
24
and reduced balance
confidence
1
may also influence the COP-eCOM distances used during more
complex motor activities.
The COP-eCOM differences were influenced by both the COP-COG
distance and COM velocity. Our findings agree with previous studies that
reported persons with advanced PD demonstrated slower turning velocity.
44,68

These results suggest that deficits in modulating velocity appear not only in later
41
stages but also in the early stages of the disease during more complex locomotor
tasks—such as the step turn.
The results of the current study provide further evidence that functional
impairments can be detected even in the early stages of the disease, when
clinical signs of gait disturbance are often absent.
13,80
Taken together, these
reports suggest that identifying the movement limitations associated with EPD
requires examination of more complex tasks that increase the challenge to the
vestibular and neuromuscular systems, such as turning and gait termination. The
findings also suggest that the peak COP-eCOM distance generated during
turning activities can be a useful index for quantifying disease severity and
intervention effectiveness. In order to determine whether the postural control
strategies during step turn are sensitive to disease severity, additional studies
that examine a broader range of PD disability will be necessary. Additionally,
studies will be needed to delineate the influence of exercise interventions on
postural control in persons with EPD.

42
CHAPTER V
THE INFLUENCE OF DIFFERENT TYPES OF TURNING STRATEGIES
ON DYNAMIC POSTURAL CONTROL IN PERSONS WITH EARLY STAGE
PARKINSON’S DISEASE
INTRODUCTION
Persons with early stage PD (EPD) typically demonstrate minimal levels of
clinical symptoms and functional impairments. While deficits in gait velocity and
stride length during simple movement tasks are not seen;
10,21
persons with EPD
often report difficulty with turning tasks.
66
Turning is a challenging and fall-
provoking task that is required for functional independence. It has been reported
that for every ten steps, two turns are used to carry out everyday activities.
70

Turning requires deceleration without stopping, rotation of the axial segments,
and acceleration of the body to a new direction.
70,79
When compared to simple
gait tasks, turning is more complex and is associated with greater postural
control demands, therefore, it may be more sensitive than simple gait tasks in
identifying postural control deficits in individuals with EPD.
Difficulty turning has been attributed to impaired postural control in
persons with advanced PD.
44,68,76
Specifically, Mak and colleagues (2008)
reported that persons with advanced PD demonstrated delayed onset time for
foot and center of mass (COM) medial-lateral displacement during turning,
compared to HC participants.
44
Additionally, persons with advanced PD
demonstrated longer turn duration with multiple steps and less peak trunk
angular velocity in the frontal and transverse planes compared to HC
43
subjects.
68,76
Although these studies have broadened our understanding of
turning dynamics in persons with PD, they are limited because they: 1) focused
on persons with advanced PD and not EPD; 2) they did not examine turning
preference; 3) they did not compare turn types; and 4) their outcome measures
did not account for the interactions among the center of pressure (COP), the
COM, and the COM velocity, which are needed to obtain a better understanding
of postural control during turning.
79

Recently, we reported that persons with EPD utilized an altered postural
control strategy while performing preplanned step turning activities. Our findings
suggested that persons with EPD adopted a potentially safer turning strategy, by
limiting the distance between their COP and eCOM during the step turn. The
step turn is characterized by a change in direction opposite to the pivot foot. A
second turning strategy is the spin turn, which is defined as a change in direction
to the same side as the pivot foot. In healthy adults the spin turn is associated
with greater transverse plane movements and kinetics.
70
In addition, the center
of gravity (COG) is typically maintained within the base of support (BOS) during a
step turn and outside the BOS during a spin turn.
70
If the COG falls outside of the
BOS, the system becomes less stable. Thus, the spin turn is considered more
“challenging” than the step turn.
The current study expands upon our knowledge of turning in persons with
EPD by: 1) comparing turning preferences between persons with EPD and HC
participants, 2) determining the influence of EPD on postural control during the
spin turn, and 3) determining whether postural control differences between
44
subjects with EPD and HC participants are influenced by turn type. We
hypothesized that persons with EPD would prefer the step turn to the spin turn.
Secondly, we hypothesized that persons with EPD would demonstrate alterations
in postural control (decreased peak COP-eCOM distances) during the spin turn
and that this difference would be greater when compared to the step turn.

METHODS
Participants
Fifteen persons with EPD and 10 HC subjects participated. A diagnosis of
idiopathic PD was confirmed by a fellowship trained movement disorder
specialist. Participants with PD were tested in the “on” medication state (i.e., fully
responding to their PD medications). At the time of testing, none of the
participants exhibited dyskinesia, dystonia, or other signs of involuntary
movement.
The inclusion criteria for the study were the following: (1) age 18 years
old, (2) able to ambulate at least 14 meters (time not measured) without a walker
or other devices, (3) persons diagnosed with PD within 3 years,
65
(4) Hoehn &
Yahr stage 1-2, (5) stable in PD medications, and (6) age and gender-matched
HC participants. The following criteria were used to exclude participants from the
study: (1) surgical intervention for persons with PD, (2) Mini Mental State Exam
(MMSE) score < 24,
23
(3) co-morbidities affecting gait (diabetes, musculoskeletal
injury, arthritis), (4) severe vision problems, and (5) pregnancy.
45
All testing took place in the Musculoskeletal Biomechanics Research
Laboratory at University of Southern California. Procedures were explained to
each participant and each participant signed an informed consent form approved
by the Institutional Review Board of the University of Southern California.
Protocol
Participants walked 4 meters at a self selected pace and turned to their
dominant direction (the direction of the limb with which side they would kick a ball)
at a 90
°
angle, at a location designated by stanchions. Ten trials were collected.
An equal number of trials were completed starting with the right and left foot to
control for the influence of the start foot. The frequency of the spin- and step-turn
strategies was recorded for each participant.
Kinematic data was collected using a motion analysis system (Vicon 612,
Oxford Metrics LTD. Oxford, England) at a sampling frequency of 60 Hz.
Reflective markers (14 mm spheres) were placed bilaterally on the skin over
specific anatomical landmarks including the anterior, posterior, and lateral head,
acromion processes, anterior and posterior shoulders, greater tubercles of
humerus, medial and lateral humeral epicondyles, medial and lateral wrists, third
metacarpophalangeal joints, 7
th
cervical vertebrae, sternoclavicular notch, iliac
crests, anterior superior iliac spines, posterior superior iliac spines, L5-S1 joint,
medial and lateral femoral epicondyles, medial and lateral malleoli, first and fifth
metatarsal heads, and first proximal/distal phalanx. Additionally, cluster markers
were placed with a band over the upper arms, lower arms, thighs, shanks, and
shoe heels. Reflective markers were identified manually within the VICON
46
Workstation software and then imported into Visual 3D software (C-Motion,
Rockville, MD). 3D marker coordinates were low-pass filtered at a cut-off
frequency of 6Hz.
Data Analysis
The position of the total body COM was defined using the weighted sum of
the COM of all 15 segments. The COG was calculated based on the medial-
lateral and the anterior-posterior locations of the COM. Instantaneous velocity of
the total body COM (COM
vel
) was computed from the linear total body COM
positions (COM
pos
) using the following equation 1:
COM
vel n
= [COM
pos

n+1
– COM
pos

n-1
] / 2 ∆t where, n = event frame
(equation 1)
The gait cycle phases were determined using a force plate and the vertical
velocity of the virtual center of each foot.
54
COP was determined from force plate
measurements during single and double limb stance (AMTI force plate 1.2m x
1.2m, 1560Hz).
To quantify postural control during turning, the distance between the COP
and the extrapolated COM (eCOM) (COG + COM vel/ √ (g/l)) was calculated
during three successful trials, using the method previously described by Hof
(equation 2).
30

Postural Control = COP- (COG + COM vel/ √ (g/l) (equation 2).
The natural freqency was calculated as √ (g/l) where g is the acceleration of
gravity and l is the length of the leg measured from the ankle joint center to the
COM.
47
Three consecutive steps during the turn: the approach step, the pivot step,
and the acceleration step where used to define two phases of turning (Figure
1).
17
Phase 1 was defined from the heel strike of the approach step to the heel
strike of the pivot step. Phase 2 was defined from the heel strike of the pivot step
to the heel strike of the acceleration step. The peak distance between the COP
and the eCOM was quantified during each phase and averaged across trials. The
average approach velocity across three successful trials was also recorded.
Statistical Analysis
A Mann-Whitney U test was used to determine the difference in the ratio
of the number of step versus spin turns between groups. In order to determine if
differences in postural control existed between persons with EPD and HC
participants across turning strategies, a 2 x 2 (group x strategy) ANOVA was
performed for each phase. All statistical analyses were performed using SPSS
11.5 (Chicago, IL) with an alpha level as 0.05.

RESULTS
Table2. Mean and standard deviation of approach gait velocity
Group
EPD HC Significance
Step turn -
approach gait
velocity (m/s)
1.35 (0.14) 1.46 (0.14) p =0.08
Spin turn -
approach gait
velocity (m/s)
1.35 (0.13) 1.48 (0.20) p =0.09
Mean (SD)
EPD: Persons with early stage Parkinson’s disease
HC: Healthy Controls

48
There were no statistically significant differences between groups for
approach gait velocity, during both step and spin turns (P > 0.05) (Table 2). The
step/spin ratio was significantly greater in persons with EPD (P < 0.05) and they
utilized the step turn strategy 1.4 times more often than the spin turn (Table 3).
Table 3. Each participant’s step versus spin turn ratio
EPD Step/Spin HC Step/Spin
1 1 1 1
2 1.5 2 1
3 1 3 0.67
4 4 4 1
5 1 5 1
6 4 6 1
7 1 7 1
8 1 8 1.5
9 1.5 9 1
10 1 10 1
11 1.5
12 1.5
13 1.5
14 2.3
15 1
mean (SD) 1.66 ± 1.02 mean (SD) 1.02 ± 0.20
EPD: Persons with early stage Parkinson’s disease
HC: Healthy Controls

There was a main effect of group for postural control. Persons with EPD
demonstrated statistically significant shorter peak COP-eCOM distances
compared to HC participants during both step and spin turns in Phase 1 (20.6%
difference; 0.34±0.05 vs. 0.41±0.06m, 19.4% difference; 0.36±0.07 vs.
0.43±0.08m, respectively; P < 0.01) and in Phase 2 (21.2% difference; 0.38±0.06
vs. 0.46±0.07m, 35.3% difference; 0.34±0.11 vs. 0.46±0.10m, respectively; P <
0.01; Figure 9). The effect sizes for the mean differences in the peak COP-eCOM
49
distances between the two groups were 1.27 for step turn and 0.93 for spin turn
during Phase 1 and 1.23 for step turn and 0.86 for spin turn during Phase 2.
There was no main effect of types of turning strategies, indicating that the
peak COP-eCOM distances were similar across turning types for both persons
with EPD and HC subjects (Figure 9). No interaction was identified.

Figure 9. The resultant COP -eCOM distance between groups during the step
and the spin turn
Gold: Persons with early stage Parkinson’s disease
Cardinal: Healthy controls
Solid line: Step turn
Dotted line: Spin turn
Gray shadow: Double limb support time
White shadow: Single limb support time
† denotes P <0.01
50
DISCUSSION
The first aim of the present investigation was to determine if there was a
difference in preferred step strategy between HC participants and those with
EPD. We observed that persons with EPD preferred the step turn strategy 60%
of the time; whereas, HC participants selected both strategies equally.
These results are consistent with reports that persons with EPD have axial
rigidity and difficulty coordinating segmental axial rotations. For example, Crenna
and colleagues (2007) reported that persons with EPD had reduced head
rotation and nearly simultaneous head and trunk movements during axial
rotations.
17
These difficulties are likely to be exacerbated during the spin turn
because this type of turn produces greater head and trunk rotations.
Motor programming delays, which have been reported in persons with
EPD may also influence the selection of the step turn over the spin turn.
38,49

Patla and colleagues (1991) demonstrated that planning time significantly
influenced the selection of turn type in healthy young adults.
57
They reported that
when the available planning and execution time was limited, the step turn was
the only turning strategy that permitted participants to successfully complete a
turn within the set boundaries of the experiment.
57

A second aim of the study was to compare postural control (peak COP-
eCOM distance) during spin turns between persons with EPD and HC
participants. Our results indicated that participants with EPD had significantly
shorter peak COP-eCOM distances compared to HC participants during both
phases of the spin turn. These findings are similar to those presented in an
51
earlier report characterizing step turns. Turning requires deceleration of the
COM, rotation of the axial segments, and acceleration of the body in the new
direction.
56,70,79
These transitional movements can be challenging to persons with
advanced PD because they have difficulty assembling and switching from one
movement component to another during sequential tasks.
42,49,59
They also have
disrupted temporal coordination of body segments during functional activities,
such as walking, step execution, and gait initiation.
17,75

During the turning sequence, individuals must control a state of
disequilibrium between the COP and the eCOM. Although separation of the
COP and the eCOM creates greater momentum, it also requires increased
neuromuscular control (e.g., neural drive, muscle forces, and joint powers) to
redirect and control this momentum. Our findings suggest that persons with EPD
select a postural control strategy that limits separation of the COP and the eCOM,
thereby reducing the mechanical and postural challenges of controlling the COM.
The decreased COP-eCOM distance observed in persons with EPD
compared to HC participants could have 2 possible explanations. First, persons
with EPD may not tolerate or generate larger COP-eCOM distances because of
reduced lower extremity muscle strength. Smaller distances require less muscle
force because they decrease the moment arms created for the body weight
vector acting around centers of joint rotation in the supporting limb.
28,33
Therefore,
shorter COP-eCOM distances may be an effort to reduce the need for muscle
force or the inability to produce adequate muscle force due to muscle
weakness.
53
Furthermore, psychological considerations may also influence the
52
COP-eCOM distance. Increased fear of falling and reduced balance confidence
have been observed in persons with advanced PD.
1,24
Previous work by Adkin
and colleagues reported that persons with advanced PD who had reduced
balance confidence demonstrated a greater degree of posture impairment
measured during standing balance tests.
1
In addition, problems of postural
control in persons with advanced PD were associated with fear of falling.
24

Because previous studies suggested that the spin turn was more
physically challenging than the step turn, we hypothesized that the magnitude of
the difference in COP-eCOM distance between EPD and HC subjects would be
greater during the spin turn. Our findings, however, indicated that the two types
of turning strategies were associated with similar peak COP-eCOM distances
and that this was consistent across groups.
Taylor and colleagues (2005) reported that the spin turn required greater
range of motion and joint torque in the frontal and the transverse plane in healthy
young adults.
70
Moreover, they demonstrated that the spin turn was less stable
because the COG was displaced outside of the BOS.
70
Others have reported
increased muscle demands of the ankle invertors and hip abductors during the
spin turn.
27
These reports, in conjunction with the current findings, suggest that
both persons with EPD and HC subjects may alter their segmental kinematics
and kinetics in order to regulate maximum COP-eCOM distances—independent
of the type of turning task.
A limitation of the current investigation is that we examined preplanned
step and spin turning in persons with EPD; however, unplanned turning events
53
often occur during activities of daily living. Further investigation is needed to
understand turning preferences and postural control during unplanned turning
events. Future studies should also examine the influence of strength, rate of
force development, fear of falling, and fall experience, on postural control during
planned and unplanned turning events. These findings may then be used to
develop task-specific interventions that improve turning capabilities in this cohort.

54
CHAPTER VI
SUMMARY AND CONCLUSIONS
Although numerous studies have quantified altered locomotor patterns in
persons with PD, most analyses were limited to investigations of persons with
advanced PD. Moreover, a majority research involving locomotion in persons
with PD has focused on simple walking tasks; however, functional walking
typically requires speed modulation and directional changes. Postural control
during functional walking tasks, however, is poorly understood and has not been
examined in persons with EPD; yet, interventions that improve and/or preserve
postural control may be most effective in the early stages of the disease.
Therefore, the overall objective of this dissertation was to better understand
postural control in persons with EPD across walking tasks of increasing
complexity (i.e., preplanned gait termination, unplanned gait termination,
preplanned step turn, and preplanned spin turn).
The purpose of study #1 was to examine the effects of EPD on postural
control during preplanned and unplanned gait termination. Compared to HC
participants, persons with EPD exhibited significantly shorter distances between
the COP and the eCOM in the AP (P < 0.05) but not the ML direction during both
preplanned and unplanned gait termination. The peak COP-eCOM distances
were greater in the unplanned condition compared to those in the preplanned
condition for both groups. These findings suggest that persons with EPD adopt a
more cautious postural control strategy during stopping but EPD does not
influence the magnitude of changes in COP-eCOM distance between preplanned
55
and unplanned gait termination. These results also demonstrate that dynamic
postural control during gait termination is altered even in the early stages of PD.
The purpose of study #2 was to examine postural control, during a
relatively less complex turn, the step turn, in persons with EPD. Complimenting
the results of study #1, individuals with EPD also demonstrated significantly
shorter peak COP-eCOM distance compared to HC participants during the step
turn (P < 0.05). This difference was influenced by: 1) shorter distances between
the COP and the COM; and 2) slower COM velocity (P < 0.05). These findings,
suggest that persons with EPD reduce overall movement amplitude (i.e., COM
displacement) in an effort to reduce disequilibrium and perhaps prevent falls.
The purpose of study #3 was: to characterize turning preference in
persons with EPD, and to determine if postural control differs between relatively
simple (step) and more complex (spin) turn types. The step/spin ratio was
significantly greater in persons with EPD (P < 0.05). Persons with EPD exhibited
shorter peak COP-eCOM distances during both the step and spin turns
compared to HC participants (P < 0.05); whereas, peak COP-eCOM distances
were similar between the two types of turn strategies within each group (P >
0.05). These results are in contrast with our original hypothesis that COP-eCOM
distances would be greater during the spin turn, and with reports in healthy
young adults that the spin turn requires greater range of motion, joint torque, and
muscle activation.
6
However, the shorter COP-eCOM distances in persons with
EPD during turning are similar to results of study #1 during gait termination and
previous findings in persons with advanced PD during gait initiation, sit-to-stand
56
tasks, and gait termination.
44,45,46
They suggests that both HC subjects and
persons with EPD alter their kinematics and kinetics in order to limit peak COP-
eCOM distances across turning types.
In conclusion, these findings demonstrate that persons with EPD adopt a
postural control strategy which may be protective in nature—by reducing the
distance between the COP and the eCOM during more complex locomotor tasks.
Moreover, these results demonstrate that differences in postural control during
more complex ADL tasks can be detected even in the early stages of PD, when
clinical signs of gait disturbance are often absent.
7,28
A smaller COP-eCOM
distance reduces disequilibrium and may help limit fall risk in this cohort.
Additional studies, however, which examine the relations among postural control
attributes and fall risk factors will be needed in order to develop safe and
effective intervention programs for persons with EPD.
Importantly, because this series of studies demonstrated significant
differences between persons with EPD and HC participants across several
complex locomotor tasks, they suggest that the peak COP-eCOM distances
generated during these activities may be useful indices for quantifying disease
severity and intervention effectiveness. Future studies, which examine a broader
range of PD disability, will be needed to determine the utility of this measure for
quantifying disease severity. Additionally, further studies will be needed to
delineate the influence of exercise interventions on postural control in persons
with EPD.
57
Taken together, our results suggest that identifying the movement
limitations associated with EPD requires examination of more complex locomotor
tasks that increase the challenge to the vestibular and neuromuscular systems,
such as stopping and turning tasks. Information obtained from this dissertation is
important in contributing to our understating of dynamic postural control in
persons with EPD and for the design of effective interventions to improve and/or
preserve postural control in persons with EPD.
58
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Abstract (if available)

Abstract While persons with early stage Parkinson’s disease (EPD) typically demonstrate minor levels of physical impairment and disability,10,21 they often have difficulty with transitional movements.66 To date, most of the studies evaluating such transitional movements in persons with PD have focused on those individuals in advanced stages of the disease

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Asset Metadata

Creator Song, Jooeun (author)

Core Title Dynamic postural control during simple and complex locomotor tasks in persons with early stage Parkinson’s disease

School School of Dentistry

Degree Doctor of Philosophy

Degree Program Biokinesiology

Publication Date 01/24/2010

Defense Date 12/23/2009

Publisher University of Southern California (original), University of Southern California. Libraries (digital)

Tag Balance,center of pressure,early-stage Parkinson’s disease,extrapolated center of mass,OAI-PMH Harvest,steering performance,stopping tasks

Language English

Contributor Electronically uploaded by the author (provenance)

Advisor Salem, George J. (committee chair), Azen, Stanley Paul (committee member), Fisher, Beth (committee member), Petzinger, Giselle (committee member), Sigward, Susan (committee member)

Creator Email jooeunso@usc.edu,junesong37@yahoo.com

Permanent Link (DOI) https://doi.org/10.25549/usctheses-m2810

Unique identifier UC1196617

Identifier etd-SONG-3437 (filename),usctheses-m40 (legacy collection record id),usctheses-c127-288442 (legacy record id),usctheses-m2810 (legacy record id)

Legacy Identifier etd-SONG-3437.pdf

Dmrecord 288442

Document Type Dissertation

Rights Song, Jooeun

Type texts

Source University of Southern California (contributing entity), University of Southern California Dissertations and Theses (collection)

Repository Name Libraries, University of Southern California

Repository Location Los Angeles, California

Repository Email cisadmin@lib.usc.edu