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Clinical Neurophysiology xxx (2015) xxx–xxx

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Clinical Neurophysiology
journal homepage: www.elsevier.com/locate/clinph

The effects of additional arm weights on arm-swing magnitude and gait


patterns in Parkinson’s disease
Jiyeon Yoon a, Jinse Park b,⇑,1, Kunbo Park c, Geunyeol Jo d, Haeyu Kim e, Wooyoung Jang f,1, Ji Sun Kim g,1,
Jinyoung Youn h,1, Eung Seok Oh i,1, Hee-Tae Kim j, Chang Hong Youm k
a
Department of Physical Therapy, Haeundae Paik Hospital, Inje University, Busan, Republic of Korea
b
Department of Neurology, Haeundae Paik Hospital, Inje University, Busan, Republic of Korea
c
Department of Orthopaedic Surgery, Haeundae Paik Hospital, Inje University, Busan, Republic of Korea
d
Department of Physical Medicine and Rehabilitation, Haeundae Paik Hospital, Inje University, Busan, Republic of Korea
e
Department of Neurological Surgery, Haeundae Paik Hospital, Inje University, Busan, Republic of Korea
f
Department of Neurology, Gangneung Asan Hospital, University of Ulsan College of Medicine, Gangneung, Republic of Korea
g
Department of Neurology, Soonchunhyang University College of Medicine, Seoul, Republic of Korea
h
Department of Neurology, Samsung Medical Center, College of Medicine, Sungkyunkwan University, Seoul, Republic of Korea
i
Department of Neurology, Chungnam National University Hospital, College of Medicine, Daejun, Republic of Korea
j
Department of Neurology, College of Medicine, Hanyang University, Seoul, Republic of Korea
k
Department of Coaching, College of Medicine, Dong-A University, Busan, Republic of Korea

a r t i c l e i n f o h i g h l i g h t s

Article history:
 Decreased arm swing is a typical gait characteristic in Parkinson’s disease.
Accepted 6 June 2015
 Adding weight to the arm facilitates limb movements in Parkinson’s disease.
Available online xxxx
 Additional arm weight improves gait disturbance in Parkinson’s disease.

Keywords:
Arm swing
Motion analysis a b s t r a c t
Rehabilitation
Objective: Recently, arm facilitation has been interested in gait rehabilitation. However, there have been
Parkinson’s disease
few studies concerning arm facilitation in patients with Parkinson’s disease (PD). The aim of our study
was to investigate the effect of increasing arm weights on gait pattern in patients with PD.
Methods: Twenty-seven patients with PD were enrolled, and they underwent gait analysis using a
three-dimensional motion capture system. Sandbags were applied to the distal forearms in all partici-
pants. We compared gait parameters including arm swing, pelvic motion, spatiotemporal data, and rel-
ative rotational angle between the weighted and unweighted gaits.
Results: The total arm-swing amplitude and pelvic rotation were significantly higher when walking with
additional arm weights than without arm weights. Cadence, walking speed, stride length, and swing
phase were significantly higher, whereas stride time, double-support time, and stance phase were signif-
icantly lower, when walking with additional arm weights than without arm weights.
Conclusions: We conclude that adding weights to the arm during walking may facilitate arm and pelvic
movements, which results in changes to gait patterns. The therapeutic use of additional arm weights
could be considered for gait rehabilitation in PD to improve gait impairment.
Significance: Arm-swing facilitation using weight load improved gait in Parkinson’s disease.
Ó 2015 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights
reserved.

1. Introduction

⇑ Corresponding author at: Department of Neurology, Haeundae Paik Hospital, Gait disturbance and postural instability have been thoroughly
Inje University, 875 Haeun-daero, Haeundaegu, Busan 612-030, Republic of Korea.
described in Parkinson’s disease (PD). Slow velocity with shuffling,
Tel.: +82 51 797 2082; fax: +82 51 797 0640.
E-mail address: jinsepark@gmail.com (J. Park).
dragging steps, small stride/step length, forward-stooped gait, and
1
KOJYP study group. decreased arm swing are typical gait characteristics in PD.

http://dx.doi.org/10.1016/j.clinph.2015.06.005
1388-2457/Ó 2015 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.

Please cite this article in press as: Yoon J et al. The effects of additional arm weights on arm-swing magnitude and gait patterns in Parkinson’s disease. Clin
Neurophysiol (2015), http://dx.doi.org/10.1016/j.clinph.2015.06.005
2 J. Yoon et al. / Clinical Neurophysiology xxx (2015) xxx–xxx

Rhythmic arm swings are connected to movements of the head, Table 1


trunk, and pelvis, and they play an important role for postural sta- Participants’ characteristics.

bility and energy efficiency during walking (Dietz et al., 2001; Mean ± SD Range
Gutnik et al., 2005). The reduction of arm swing is one of major Age (years) 74.0 ± 5.7 64–90
characteristics in patients with PD, and arm swing would be lost Gender 15 males/12 females
in the early stage of PD (Roggendorf et al., 2012). Height (cm) 157.5 ± 8.2 142.2–175.4
A variety of gait trainings in rehabilitation program for patients Weight (kg) 57.9 ± 9.4 42.3–74.7
BMI (kg/m2) 23.3 ± 2.7 17.5–28.5
with PD have been performed to improve gait function and mobil- Duration (month) 22.2 ± 20.7 0.5–71
ity by using a treadmill, assistive devices, and cueing strategies H&Y stage 2.5 ± 0.5 2–3
such as verbal, visual, or auditory cueing (Kegelmeyer et al., UPDRS III (points) 22.8 ± 7.7 10–43
2013; Spaulding et al., 2013). Recently, there is a growing interest
BMI: Body mass index; H&Y stage: Hoehn and Yahr stage; UPDRS III: Unified
on arm movements in patients with PD, such as arm-swing asym- Parkinson’s disease scale part 3.
metry or amplitude (Lewek et al., 2010; Roggendorf et al., 2012).
Therefore, increasing arm swing also is one of the important pur-
poses of gait rehabilitation for PD patients. Meyns et al. reported plates (AMTI, Watertown, MA, USA) synchronized with the Nexus
that arm facilitation in rehabilitation program for patients with program (version 1.7) for data collection at 1000 Hz, and the events
PD is very important, but, to date, there is little information regard- of gait cycle were recorded simultaneously. In total, 16 retroreflec-
ing this (Meyns et al., 2013). tive markers were used to indicate the segments. Twelve markers
A vast amount of evidence has suggested that an added load to were attached on the anterior and posterior superior iliac spines,
the body has an effect on altered gait parameters, and it improved femoral epicondyle, and malleolus, second metatarsal head, and
postural balance (Donker et al., 2005; Duysens et al., 2000). The posterior calcaneus bilaterally for the kinematics of lower extrem-
added weight to the arms would be effective in changing arm ities. For the amplitude of arm swing, four markers were bilaterally
movements, and it could lead to influence on the interaction placed on acromion processes and on the middle point of ulna and
between limb movements during walking (Donker et al., 2005). radius. The marker placement was performed by one experienced
This change of arm movement could result in the improvement researcher to minimize the error.
of gait parameters and pelvic motion. To our knowledge, previous
reports have only investigated healthy subjects, and little is known 2.3. Procedures
regarding the facilitation of arm movement in patients with PD.
The aim of this study was to investigate whether additional arm Prior to performing the dynamic trials, all participants under-
weight could alter the gait patterns as well as arm-swing ampli- took a static trial to determine the movement of the pelvis, upper,
tude during walking in PD. We hypothesized that additional arm and lower limbs. Each PD patient who took part in this study
weight would increase arm-swing amplitude, and it would walked barefoot along a 20-foot walkway at an individually pre-
improve the spatiotemporal parameters and pelvic motion in ferred pace, and the patient performed five trials with and without
patients with PD. arm weights (in random order). Two sandbags weighing 0.45 kg
(Sammons Preston, Bolingbrook, IL, USA) were used as arm
weights. The patients with PD wore sandbags with Velcro straps
2. Methods
on the distal one-third portion of the forearm bilaterally.
Unfortunately, there was no report about the appropriate weight
2.1. Study participants
on the patient with PD. Several previous studies for healthy sub-
jects related to the arm weight used a 1.2- or 1.8-kg weight on each
Twenty-seven patients with PD (15 males and 12 females)
arm. Considering that our subjects are old and weak, we selected
meeting the United Kingdom Parkinson’s Disease Society Brain
0.45 kg.
Bank diagnostic criteria were enrolled for this study (Hughes
No specific instructions regarding gait posture as well as arm
et al., 1993). Basic demographic and clinical information were
swing were provided to participants. Each participant took a break
obtained including disease duration, body mass index (BMI), and
for 1 min between tasks to minimize the fatigue.
disease severity. Clinical severity was assessed by the United
Parkinson’s Disease Rating Scale part III (UPDRS III) and Hoehn
2.4. Data analysis
and Yahr (H&Y) stage. The demographic data of participants are
presented in Table 1. Inclusion criteria for participants were as fol-
Motion data capture and post-processing of marker trajectories
lows: (1) in H&Y stages 2–3; (2) complaining of gait disturbance
were performed using the Nexus 1.7 software (Vicon, Fareham,
but able to walk without assistance; and (3) having proper cogni-
UK). The tri-planar motions of pelvis were calculated relative to
tion to understand the study information. Exclusion criteria were
the global coordinate system, and arm swing was calculated by
recommended for (1) any primary orthopedic, neurological dis-
the angle between the arm and virtual vertical axis. The kinematics
eases, and visual disturbances other than PD, and (2) having com-
of pelvic motions was presented for sagittal, coronal, and trans-
plaints that affect independent walking. All patients with PD were
verse planes defined as anterior–posterior tilt, obliquity, and rota-
on medication. The study was approved by the institutional review
tion, respectively. Each pelvic motion was calculated as the
board at the Haeundae Paik Hospital (Busan, Korea). All patients
amplitude (maximum–minimum values).
understood the study procedure and purpose, and they gave writ-
The arm swing was divided into anteversion and retroversion of
ten informed consent before participation.
the shoulder joint. The anteversion was defined for maximum pos-
itive values, and the retroversion was done for minimum negative
2.2. Gait analysis values (Fig. 1(a)). In addition, all arm-swing amplitudes including
total, anteversion, and retroversion were calculated as the average
An eight-camera three-dimensional motion analysis system of the left and right side. The relative angle of the shoulder relative
(Vicon, Fareham, UK) was used at a sample rate of 100 Hz for the to the pelvis was obtained by subtracting the virtual shoulder line
quantification of arm swing, pelvic motions, and spatiotemporal through the markers on the acromion from the pelvis within each
parameters. Heel strike and toe-off were obtained from two force single step (Fig. 1(b)). The right step indicates from left heel strike

Please cite this article in press as: Yoon J et al. The effects of additional arm weights on arm-swing magnitude and gait patterns in Parkinson’s disease. Clin
Neurophysiol (2015), http://dx.doi.org/10.1016/j.clinph.2015.06.005
J. Yoon et al. / Clinical Neurophysiology xxx (2015) xxx–xxx 3

Fig. 1. Arm swing is divided into anteversion (+) and retroversion () by the angle calculated between the arm perpendicular axis and virtual vertical axis by generated pelvis
(a) lateral view). The relative angle between the shoulder and pelvis is calculated between the virtual shoulder line and pelvic line (b) view from above).

to right heel strike, and the left step does the reverse. The angle is Table 2
closer to 0°, which indicates that the pelvis and shoulder rotation is Comparison of the arm and pelvic kinematics with and without arm weights in PD
patients.
in phase (Huang et al., 2011). The total arm-swing amplitude and
total amplitude of the relative angle between the shoulder and pel- Without arm With arm P
vis were calculated as maximum minus minimum values during weight weight

one-stride cycle. Arm swing (°)


We also evaluate the effect to arm-swing asymmetry. The sym- Anteversion 10.15 ± 9.63 17.98 ± 9.16 0.000*
Retroversion 6.47 ± 9.08 10.06 ± 8.15 0.000*
metry angle (SA), as proposed by Zifchock et al. (2006), is used to
Amplitude 16.61 ± 10.19 28.45 ± 12.80 0.000*
evaluate the arm-swing asymmetry in patients with PD during
Pelvic kinematics (°)
gait. The SA was calculated by the following equation:
Pelvic tilt 2.93 ± 1.13 2.84 ± 1.36 0.553*
  Pelvic obliquity 3.98 ± 1.43 4.12 ± 5.09 0.559*
 X
45  arctan L Pelvic rotation 5.78 ± 2.16 6.70 ± 2.63 0.013*
X R

SA ¼
90  100ð%Þ Relative rotational angle (°)
Shoulder pelvis 7.36 ± 4.05 8.50 ± 4.61 0.126

amplitude

XL and XR are the angles of the left and right arm swing, respectively. Paired t-test was used for the comparison of change on each scale score between
A higher SA value indicates higher asymmetry. two groups. These values represented with the standard deviations.
*
p < 0.05.
All patients completed at least five gait cycles for each trial, and
the third trial was used for analysis. We obtained spatiotemporal
data from the software including cadence, walking speed, stride (p < 0.05). Most patients except three patients showed increasing
time, stride length, double support, swing phase, and stance phase. arm-swing amplitude, and this effect developed immediately from
The arm-swing amplitude and asymmetry, the relative angle the first trial to the last trial. In pelvic kinematics, pelvic rotation
between the shoulder and pelvis, and kinematic pelvic motion showed a significant increase with the use of arm weights
have been mentioned earlier. (p < 0.05). There was no difference in pelvic tilt and obliquity
between gaits with and without arm weights. There was an
2.5. Statistical analysis increasing tendency to the relative angles between the shoulder
and pelvis during the right and left step when patients with PD
SAS software package (version 9.1, Cary, NC, USA) was used to walked with arm weights; however, there was no statistical signif-
perform the statistical analysis. For considering the difference of icance. Arm-swing asymmetry did not significantly differ between
walking speed in each trial, we compared the gait parameters two conditions (p > 0.05). In total, the SA increased in 14 of 27
including arm and pelvic kinematics, and spatiotemporal parame- patients, and it decreased in 13.
ters between with and without arm weights using paired t-test.
The level of significance was set at p < 0.05. 3.2. Spatiotemporal parameters

3. Results Table 3 shows the spatiotemporal parameters. All spatiotempo-


ral variables were significantly different between gaits with and
3.1. Arm swing and pelvic kinematics without arm weights. Cadence, walking speed, stride length, and
swing phase of gait cycle were greater for gaits with weights than
Table 2 summarizes the result of paired t-test for arm and pelvic without weights (p < 0.05). Stride time, double-support time, and
kinematic parameters. Anteversion and retroversion of arm swing stance phase of gait cycle were less for gaits with arm weights than
were significantly longer when walking with arm weights. without arm weights (p < 0.05).
Consequently, arm-swing amplitude also showed a significant We evaluated the correlation between arm-swing amplitude
increase when patients with PD walked with arm weights and gait parameters. Pearson correlation test was used for the

Please cite this article in press as: Yoon J et al. The effects of additional arm weights on arm-swing magnitude and gait patterns in Parkinson’s disease. Clin
Neurophysiol (2015), http://dx.doi.org/10.1016/j.clinph.2015.06.005
4 J. Yoon et al. / Clinical Neurophysiology xxx (2015) xxx–xxx

Table 3 We postulated that light adding mass on self-preferred gait would


Comparison of the spatiotemporal parameters with and without arm weights in PD be effective to arm facilitation in PD.
patients.
Arm swing is often regarded as a way of counteracting free ver-
Without arm With arm p tical moments caused by the swing legs (Li et al., 2001). In partic-
weight weight ular, arm retroversion provides gait stabilization by minimizing
Cadence (steps/min) 101.78 ± 13.44 109.24 ± 12.94 0.000* body rotation at the initial swing phase. In patients with PD,
Walking speed (m/s) 0.62 ± 0.19 0.73 ± 0.22 0.000* prominent impairment in arm retroversion was found to be an
Stride time (s) 1.21 ± 0.21 1.12 ± 0.15 0.000*
Stride length (m) 0.73 ± 0.21 0.81 ± 0.22 0.007*
early sign of gait disturbance (Roggendorf et al., 2012). The arm
Double support (s) 0.35 ± 0.11 0.29 ± 0.10 0.000* retroversion happens throughout the swing phase from the
Stance phase (% gait cycle) 64.14 ± 4.02 62.79 ± 3.71 0.004* pre-swing of ipsilateral foot-off (Murray et al., 1967). For this rea-
Swing phase (% gait cycle) 35.57 ± 4.29 37.12 ± 3.67 0.001* son, we speculated that an increased retroversion by additional
Paired t-test was used for the comparison of change on each scale score between arm weights might result in an increased swing phase and a
two groups. These values represented with the standard deviations. decreased stance phase. In addition, this change of gait cycle might
*
p < 0.05. lead to gait stabilization consequently.
Our results also showed that pelvic rotation increased, at <1°,
and the relative angle between the shoulder and pelvis for trunk
motion did not differ when walking with arm weights, compared
analysis of the relationship between arm swing and gait parame-
with that without weights. The pelvis plays a role as a mobile link
ters. Walking speed and stride length showed significant correla-
between the two lower limbs, and an increased pelvic rotation dur-
tion with the total arm-swing amplitude (r = 0.58, r = 0.57,
ing swing phase adds to step length (Lovejoy, 2005). The increase
p < 0.05). The other gait parameters including cadence, double sup-
of the relative angle between the shoulder and pelvis indicates that
port, stride time, swing, and stance phase were not significantly
the shoulder line moves more at an antiphase with the pelvic line.
related to arm swing.
This mild increase could have an effect on the increased pelvic
rotation by improved coordination between the shoulder and pel-
4. Discussion vis. We postulated that the greater pelvic rotation in our result
may be a cause for the increased stride length. However, adding
Our study described the effects of additional arm weights on the arm weights did not significantly change the trunk coordination
arm swing, pelvic kinematics, and spatiotemporal parameters in in PD patients. PD patients walked using a similar strategy as
ambulating patients with PD. Several reports demonstrated that patients with low back pain who keep the stiff trunk and swing
patients with PD showed reduced walking velocity and stride the arm more (Huang et al., 2011).
length and hip joint kinematics compared with healthy controls Cadence is defined as the number of steps per minute. An
in a quantitative gait analysis (Sofuwa et al., 2005). Gait parame- increase in cadence may be considered as an increased stride fre-
ters, including kinematic and spatiotemporal data assessed in our quency and walking speed. In addition, walking speed is deter-
study, are usually impaired in PD. mined by the combination of stride length and frequency (Huang
In this study, arm-swing amplitude was increased with the use et al., 2010). In our study, cadence, walking speed, and stride
of weights. This finding is in line with those of previous studies, length were increased, and the stride time was decreased when
which investigated the effects of adding weights during walking walking with arm weights. This indicates that adding arm weights
in healthy controls (Duysens et al., 2000). Arm swing plays an results in the improvement of gait by increasing the stride length
important role for counterbalancing the movements of contralat- as well as frequency. Although cadence is considered to be
eral pelvis and lower limb, although arm swing is not regarded increased in PD, evidence is controversial. Some reports showed
as an essential prerequisite for walking (Zehr and Duysens, normal or decreased cadence in PD (Morris et al., 1996).
2004). Additional arm weights could change the inertia moments Unfortunately, we did not compare the cadence between normal
and the natural pendular frequency of upper extremities. controls and PD group. As per our result, we assumed that cadence
Increased angular acceleration of arm swing was associated with might not be increased in participants compared with normal con-
increases in the angular displacement of shoulder joints, and trols. Further studies are warranted comparing cadence with nor-
greater anterior acceleration of shoulder joints resulted in greater mal controls.
arm retraction (Pontzer et al., 2009). Adding mass to the upper Dietz and Michel verified that patients with PD preserve basic
or lower limbs changed arm movements as a compensatory mech- quadrupedal limb coordination (Dietz and Michel, 2008). The
anism for maintaining stable gait (Bonnard and Pailhous, 1991). authors suggest that the arm and leg are coupling via the activity
We postulated that increased retraction may contribute to of spinal interneuron. Neural connections between the upper and
increased total arm swing in our study. This is in line with the lower limbs exist, which increases muscle activation in another
results found by Behrman et al. who reported that deliberately limb during rhythmic tasks (Huang and Ferris, 2009; Kawashima
increased arm swing was the effective strategy to improve walking et al., 2008). In addition, Bruijn et al. found that arm and leg move-
pattern such as increased velocity (Behrman et al., 1998). The addi- ments contribute to control the body angular momentum com-
tional sandbags to the wrist could act as a sensory input, and the pared with the pelvis or thorax movement (Bruijn et al., 2008).
perception of altered arm swing through repetitive walking could Our results showed that arm-swing amplitude was correlated
activate the motor cortex for locomotion. with stride length, which is in accordance with previous reports.
However, some previous studies contrast with our results. With such findings, the alteration of spatiotemporal parameters
Arm-swing amplitude decreases to compensate forearm mass when walking with arm weights might be explained in respect of
and to minimize the energy cost, although adding arm mass has synchronizing the upper and lower limb movements. Based on pre-
been known to increase the muscular recruitment of the upper vious reports, we speculated that an increased arm movement may
limbs (Donker et al., 2002). However, upper limb movements could facilitate lower limb movement especially stride length via
be changed under various walking speeds on the treadmill in spino-bulbar-spinal reflex pathway.
healthy people (Donker et al., 2005, 2002; Pontzer et al., 2009). There were several limitations in this study. We did not com-
In that study, the weight of arm loading was four times more, pare the results with a control group, so we could not exclude a
and gait speed also was much faster than our study (>1.5 km/h). placebo effect from the added weights. In addition, we considered

Please cite this article in press as: Yoon J et al. The effects of additional arm weights on arm-swing magnitude and gait patterns in Parkinson’s disease. Clin
Neurophysiol (2015), http://dx.doi.org/10.1016/j.clinph.2015.06.005
J. Yoon et al. / Clinical Neurophysiology xxx (2015) xxx–xxx 5

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Please cite this article in press as: Yoon J et al. The effects of additional arm weights on arm-swing magnitude and gait patterns in Parkinson’s disease. Clin
Neurophysiol (2015), http://dx.doi.org/10.1016/j.clinph.2015.06.005

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