- Email: [email protected]
The effects of additional arm weights on arm-swing magnitude and gait patterns in Parkinson’s disease
Clinical Neurophysiology xxx (2015) xxx–xxx
Contents lists available at ScienceDirect
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 Department of Neurology, Haeundae Paik Hospital, Inje University, Busan, Republic of Korea 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 b c
a r t i c l e
i n f o
Article history: Accepted 6 June 2015 Available online xxxx Keywords: Arm swing Motion analysis Rehabilitation Parkinson’s disease
h i g h l i g h t s Decreased arm swing is a typical gait characteristic in Parkinson’s disease. Adding weight to the arm facilitates limb movements in Parkinson’s disease. Additional arm weight improves gait disturbance in Parkinson’s disease.
a b s t r a c t Objective: Recently, arm facilitation has been interested in gait rehabilitation. However, there have been 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 participants. We compared gait parameters including arm swing, pelvic motion, spatiotemporal data, and relative 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 significantly 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, Inje University, 875 Haeun-daero, Haeundaegu, Busan 612-030, Republic of Korea. Tel.: +82 51 797 2082; fax: +82 51 797 0640. E-mail address: [email protected] (J. Park). 1 KOJYP study group.
Gait disturbance and postural instability have been thoroughly described in Parkinson’s disease (PD). Slow velocity with shuffling, dragging steps, small stride/step length, forward-stooped gait, and 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, trunk, and pelvis, and they play an important role for postural stability and energy efficiency during walking (Dietz et al., 2001; Gutnik et al., 2005). The reduction of arm swing is one of major characteristics in patients with PD, and arm swing would be lost in the early stage of PD (Roggendorf et al., 2012). A variety of gait trainings in rehabilitation program for patients with PD have been performed to improve gait function and mobility by using a treadmill, assistive devices, and cueing strategies such as verbal, visual, or auditory cueing (Kegelmeyer et al., 2013; Spaulding et al., 2013). Recently, there is a growing interest on arm movements in patients with PD, such as arm-swing asymmetry or amplitude (Lewek et al., 2010; Roggendorf et al., 2012). Therefore, increasing arm swing also is one of the important purposes of gait rehabilitation for PD patients. Meyns et al. reported that arm facilitation in rehabilitation program for patients with PD is very important, but, to date, there is little information regarding this (Meyns et al., 2013). A vast amount of evidence has suggested that an added load to the body has an effect on altered gait parameters, and it improved postural balance (Donker et al., 2005; Duysens et al., 2000). The added weight to the arms would be effective in changing arm movements, and it could lead to influence on the interaction between limb movements during walking (Donker et al., 2005). This change of arm movement could result in the improvement of gait parameters and pelvic motion. To our knowledge, previous reports have only investigated healthy subjects, and little is known regarding the facilitation of arm movement in patients with PD. The aim of this study was to investigate whether additional arm weight could alter the gait patterns as well as arm-swing amplitude during walking in PD. We hypothesized that additional arm weight would increase arm-swing amplitude, and it would improve the spatiotemporal parameters and pelvic motion in patients with PD. 2. Methods 2.1. Study participants Twenty-seven patients with PD (15 males and 12 females) meeting the United Kingdom Parkinson’s Disease Society Brain Bank diagnostic criteria were enrolled for this study (Hughes et al., 1993). Basic demographic and clinical information were obtained including disease duration, body mass index (BMI), and disease severity. Clinical severity was assessed by the United Parkinson’s Disease Rating Scale part III (UPDRS III) and Hoehn and Yahr (H&Y) stage. The demographic data of participants are presented in Table 1. Inclusion criteria for participants were as follows: (1) in H&Y stages 2–3; (2) complaining of gait disturbance but able to walk without assistance; and (3) having proper cognition to understand the study information. Exclusion criteria were recommended for (1) any primary orthopedic, neurological diseases, and visual disturbances other than PD, and (2) having complaints that affect independent walking. All patients with PD were on medication. The study was approved by the institutional review board at the Haeundae Paik Hospital (Busan, Korea). All patients understood the study procedure and purpose, and they gave written informed consent before participation. 2.2. Gait analysis An eight-camera three-dimensional motion analysis system (Vicon, Fareham, UK) was used at a sample rate of 100 Hz for the quantification of arm swing, pelvic motions, and spatiotemporal parameters. Heel strike and toe-off were obtained from two force
Table 1 Participants’ characteristics.
Age (years) Gender Height (cm) Weight (kg) BMI (kg/m2) Duration (month) H&Y stage UPDRS III (points)
Mean ± SD
Range
74.0 ± 5.7 15 males/12 females 157.5 ± 8.2 57.9 ± 9.4 23.3 ± 2.7 22.2 ± 20.7 2.5 ± 0.5 22.8 ± 7.7
64–90 142.2–175.4 42.3–74.7 17.5–28.5 0.5–71 2–3 10–43
BMI: Body mass index; H&Y stage: Hoehn and Yahr stage; UPDRS III: Unified Parkinson’s disease scale part 3.
plates (AMTI, Watertown, MA, USA) synchronized with the Nexus program (version 1.7) for data collection at 1000 Hz, and the events of gait cycle were recorded simultaneously. In total, 16 retroreflective markers were used to indicate the segments. Twelve markers were attached on the anterior and posterior superior iliac spines, femoral epicondyle, and malleolus, second metatarsal head, and posterior calcaneus bilaterally for the kinematics of lower extremities. For the amplitude of arm swing, four markers were bilaterally placed on acromion processes and on the middle point of ulna and radius. The marker placement was performed by one experienced researcher to minimize the error. 2.3. Procedures Prior to performing the dynamic trials, all participants undertook a static trial to determine the movement of the pelvis, upper, and lower limbs. Each PD patient who took part in this study walked barefoot along a 20-foot walkway at an individually preferred pace, and the patient performed five trials with and without 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 on the distal one-third portion of the forearm bilaterally. Unfortunately, there was no report about the appropriate weight on the patient with PD. Several previous studies for healthy subjects related to the arm weight used a 1.2- or 1.8-kg weight on each arm. Considering that our subjects are old and weak, we selected 0.45 kg. No specific instructions regarding gait posture as well as arm swing were provided to participants. Each participant took a break for 1 min between tasks to minimize the fatigue. 2.4. Data analysis Motion data capture and post-processing of marker trajectories were performed using the Nexus 1.7 software (Vicon, Fareham, UK). The tri-planar motions of pelvis were calculated relative to the global coordinate system, and arm swing was calculated by the angle between the arm and virtual vertical axis. The kinematics of pelvic motions was presented for sagittal, coronal, and transverse planes defined as anterior–posterior tilt, obliquity, and rotation, respectively. Each pelvic motion was calculated as the amplitude (maximum–minimum values). The arm swing was divided into anteversion and retroversion of the shoulder joint. The anteversion was defined for maximum positive values, and the retroversion was done for minimum negative values (Fig. 1(a)). In addition, all arm-swing amplitudes including total, anteversion, and retroversion were calculated as the average of the left and right side. The relative angle of the shoulder relative to the pelvis was obtained by subtracting the virtual shoulder line through the markers on the acromion from the pelvis within each 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
3
J. Yoon et al. / Clinical Neurophysiology xxx (2015) xxx–xxx
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 closer to 0°, which indicates that the pelvis and shoulder rotation is in phase (Huang et al., 2011). The total arm-swing amplitude and total amplitude of the relative angle between the shoulder and pelvis were calculated as maximum minus minimum values during one-stride cycle. We also evaluate the effect to arm-swing asymmetry. The symmetry angle (SA), as proposed by Zifchock et al. (2006), is used to evaluate the arm-swing asymmetry in patients with PD during gait. The SA was calculated by the following equation:
X 45 arctan L X R SA ¼ 100ð%Þ 90 XL and XR are the angles of the left and right arm swing, respectively. A higher SA value indicates higher asymmetry. 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 time, stride length, double support, swing phase, and stance phase. The arm-swing amplitude and asymmetry, the relative angle between the shoulder and pelvis, and kinematic pelvic motion have been mentioned earlier. 2.5. Statistical analysis SAS software package (version 9.1, Cary, NC, USA) was used to perform the statistical analysis. For considering the difference of walking speed in each trial, we compared the gait parameters including arm and pelvic kinematics, and spatiotemporal parameters between with and without arm weights using paired t-test. The level of significance was set at p < 0.05. 3. Results 3.1. Arm swing and pelvic kinematics Table 2 summarizes the result of paired t-test for arm and pelvic kinematic parameters. Anteversion and retroversion of arm swing were significantly longer when walking with arm weights. Consequently, arm-swing amplitude also showed a significant increase when patients with PD walked with arm weights
Table 2 Comparison of the arm and pelvic kinematics with and without arm weights in PD patients.
Arm swing (°) Anteversion Retroversion Amplitude Pelvic kinematics (°) Pelvic tilt Pelvic obliquity Pelvic rotation
Without arm weight
With arm weight
P
10.15 ± 9.63 6.47 ± 9.08 16.61 ± 10.19
17.98 ± 9.16 10.06 ± 8.15 28.45 ± 12.80
0.000* 0.000* 0.000*
2.93 ± 1.13 3.98 ± 1.43 5.78 ± 2.16
2.84 ± 1.36 4.12 ± 5.09 6.70 ± 2.63
0.553* 0.559* 0.013*
Relative rotational angle (°) Shoulder pelvis 7.36 ± 4.05 amplitude
8.50 ± 4.61
0.126
Paired t-test was used for the comparison of change on each scale score between two groups. These values represented with the standard deviations. * p < 0.05.
(p < 0.05). Most patients except three patients showed increasing arm-swing amplitude, and this effect developed immediately from the first trial to the last trial. In pelvic kinematics, pelvic rotation showed a significant increase with the use of arm weights (p < 0.05). There was no difference in pelvic tilt and obliquity between gaits with and without arm weights. There was an increasing tendency to the relative angles between the shoulder and pelvis during the right and left step when patients with PD walked with arm weights; however, there was no statistical significance. Arm-swing asymmetry did not significantly differ between two conditions (p > 0.05). In total, the SA increased in 14 of 27 patients, and it decreased in 13. 3.2. Spatiotemporal parameters Table 3 shows the spatiotemporal parameters. All spatiotemporal variables were significantly different between gaits with and without arm weights. Cadence, walking speed, stride length, and swing phase of gait cycle were greater for gaits with weights than without weights (p < 0.05). Stride time, double-support time, and stance phase of gait cycle were less for gaits with arm weights than without arm weights (p < 0.05). We evaluated the correlation between arm-swing amplitude 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 Comparison of the spatiotemporal parameters with and without arm weights in PD patients.
Cadence (steps/min) Walking speed (m/s) Stride time (s) Stride length (m) Double support (s) Stance phase (% gait cycle) Swing phase (% gait cycle)
Without arm weight
With arm weight
p
101.78 ± 13.44 0.62 ± 0.19 1.21 ± 0.21 0.73 ± 0.21 0.35 ± 0.11 64.14 ± 4.02 35.57 ± 4.29
109.24 ± 12.94 0.73 ± 0.22 1.12 ± 0.15 0.81 ± 0.22 0.29 ± 0.10 62.79 ± 3.71 37.12 ± 3.67
0.000* 0.000* 0.000* 0.007* 0.000* 0.004* 0.001*
Paired t-test was used for the comparison of change on each scale score between two groups. These values represented with the standard deviations. * p < 0.05.
analysis of the relationship between arm swing and gait parameters. Walking speed and stride length showed significant correlation with the total arm-swing amplitude (r = 0.58, r = 0.57, p < 0.05). The other gait parameters including cadence, double support, stride time, swing, and stance phase were not significantly related to arm swing. 4. Discussion Our study described the effects of additional arm weights on the arm swing, pelvic kinematics, and spatiotemporal parameters in ambulating patients with PD. Several reports demonstrated that patients with PD showed reduced walking velocity and stride length and hip joint kinematics compared with healthy controls in a quantitative gait analysis (Sofuwa et al., 2005). Gait parameters, including kinematic and spatiotemporal data assessed in our study, are usually impaired in PD. In this study, arm-swing amplitude was increased with the use of weights. This finding is in line with those of previous studies, which investigated the effects of adding weights during walking in healthy controls (Duysens et al., 2000). Arm swing plays an important role for counterbalancing the movements of contralateral pelvis and lower limb, although arm swing is not regarded as an essential prerequisite for walking (Zehr and Duysens, 2004). Additional arm weights could change the inertia moments and the natural pendular frequency of upper extremities. Increased angular acceleration of arm swing was associated with increases in the angular displacement of shoulder joints, and greater anterior acceleration of shoulder joints resulted in greater arm retraction (Pontzer et al., 2009). Adding mass to the upper or lower limbs changed arm movements as a compensatory mechanism for maintaining stable gait (Bonnard and Pailhous, 1991). We postulated that increased retraction may contribute to increased total arm swing in our study. This is in line with the results found by Behrman et al. who reported that deliberately increased arm swing was the effective strategy to improve walking pattern such as increased velocity (Behrman et al., 1998). The additional sandbags to the wrist could act as a sensory input, and the perception of altered arm swing through repetitive walking could activate the motor cortex for locomotion. However, some previous studies contrast with our results. Arm-swing amplitude decreases to compensate forearm mass and to minimize the energy cost, although adding arm mass has been known to increase the muscular recruitment of the upper limbs (Donker et al., 2002). However, upper limb movements could be changed under various walking speeds on the treadmill in healthy people (Donker et al., 2005, 2002; Pontzer et al., 2009). In that study, the weight of arm loading was four times more, and gait speed also was much faster than our study (>1.5 km/h).
We postulated that light adding mass on self-preferred gait would be effective to arm facilitation in PD. Arm swing is often regarded as a way of counteracting free vertical moments caused by the swing legs (Li et al., 2001). In particular, arm retroversion provides gait stabilization by minimizing body rotation at the initial swing phase. In patients with PD, prominent impairment in arm retroversion was found to be an early sign of gait disturbance (Roggendorf et al., 2012). The arm retroversion happens throughout the swing phase from the pre-swing of ipsilateral foot-off (Murray et al., 1967). For this reason, we speculated that an increased retroversion by additional arm weights might result in an increased swing phase and a decreased stance phase. In addition, this change of gait cycle might 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 with that without weights. The pelvis plays a role as a mobile link between the two lower limbs, and an increased pelvic rotation during swing phase adds to step length (Lovejoy, 2005). The increase of the relative angle between the shoulder and pelvis indicates that the shoulder line moves more at an antiphase with the pelvic line. This mild increase could have an effect on the increased pelvic rotation by improved coordination between the shoulder and pelvis. We postulated that the greater pelvic rotation in our result may be a cause for the increased stride length. However, adding arm weights did not significantly change the trunk coordination in PD patients. PD patients walked using a similar strategy as patients with low back pain who keep the stiff trunk and swing the arm more (Huang et al., 2011). Cadence is defined as the number of steps per minute. An increase in cadence may be considered as an increased stride frequency and walking speed. In addition, walking speed is determined by the combination of stride length and frequency (Huang et al., 2010). In our study, cadence, walking speed, and stride length were increased, and the stride time was decreased when walking with arm weights. This indicates that adding arm weights results in the improvement of gait by increasing the stride length as well as frequency. Although cadence is considered to be increased in PD, evidence is controversial. Some reports showed normal or decreased cadence in PD (Morris et al., 1996). Unfortunately, we did not compare the cadence between normal controls and PD group. As per our result, we assumed that cadence might not be increased in participants compared with normal controls. Further studies are warranted comparing cadence with normal controls. Dietz and Michel verified that patients with PD preserve basic quadrupedal limb coordination (Dietz and Michel, 2008). The authors suggest that the arm and leg are coupling via the activity of spinal interneuron. Neural connections between the upper and lower limbs exist, which increases muscle activation in another limb during rhythmic tasks (Huang and Ferris, 2009; Kawashima et al., 2008). In addition, Bruijn et al. found that arm and leg movements contribute to control the body angular momentum compared with the pelvis or thorax movement (Bruijn et al., 2008). Our results showed that arm-swing amplitude was correlated with stride length, which is in accordance with previous reports. With such findings, the alteration of spatiotemporal parameters when walking with arm weights might be explained in respect of synchronizing the upper and lower limb movements. Based on previous reports, we speculated that an increased arm movement may facilitate lower limb movement especially stride length via spino-bulbar-spinal reflex pathway. There were several limitations in this study. We did not compare the results with a control group, so we could not exclude a 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
proximal arms and forearm as one mechanical segment for arm swing; hence, the elbow motion and the arm length were ignored. The sandbag with the same weight was applied to all participants who had various body metrics, so we did not control the arm-swing symmetry and could not investigate the best appropriate weight to improve gait parameters. We only compared changes in short-term responses, thus making it difficult to confirm whether the effects will continue for a long time. Further studies should investigate the effects of various weights to improve the arm-swing symmetry during walking and the long-term effect of adding arm weights for the gait training in patients with PD. In conclusion, adding arm weights during walking is useful in facilitating the arm swing, and it improves the gait patterns in patients with PD. Therefore, the effort of the upper limb may influence lower limb rehabilitation in patients with PD. Acknowledgement This research is supported by Soonchunhyang University hospital. Conflicts of interest: The authors have no potential conflicts of interest to report concerning this article, and they have nothing to disclose. References Behrman AL, Teitelbaum P, Cauraugh JH. Verbal instructional sets to normalise the temporal and spatial gait variables in Parkinson’s disease. J Neurol Neurosurg Psychiatry 1998;65:580–2. Bonnard M, Pailhous J. Intentional compensation for selective loading affecting human gait phases. J Mot Behav 1991;23:4–12. Bruijn SM, Meijer OG, van Dieen JH, Kingma I, Lamoth CJ. Coordination of leg swing, thorax rotations, and pelvis rotations during gait: the organisation of total body angular momentum. Gait Posture 2008;27:455–62. Dietz V, Fouad K, Bastiaanse CM. Neuronal coordination of arm and leg movements during human locomotion. Eur J Neurosci 2001;14:1906–14. Dietz V, Michel J. Locomotion in Parkinson’s disease: neuronal coupling of upper and lower limbs. Brain 2008;131:3421–31. Donker SF, Daffertshofer A, Beek PJ. Effects of velocity and limb loading on the coordination between limb movements during walking. J Mot Behav 2005;37:217–30. Donker SF, Mulder T, Nienhuis B, Duysens J. Adaptations in arm movements for added mass to wrist or ankle during walking. Exp Brain Res 2002;146:26–31.
5
Duysens J, Clarac F, Cruse H. Load-regulating mechanisms in gait and posture: comparative aspects. Physiol Rev 2000;80:83–133. Gutnik B, Mackie H, Hudson G, Standen C. How close to a pendulum is human upper limb movement during walking? Homo 2005;56:35–49. Huang HJ, Ferris DP. Upper and lower limb muscle activation is bidirectionally and ipsilaterally coupled. Med Sci Sports Exerc 2009;41:1778–89. Huang Y, Meijer OG, Lin J, Bruijn SM, Wu W, Lin X, et al. The effects of stride length and stride frequency on trunk coordination in human walking. Gait Posture 2010;31:444–9. Huang YP, Bruijn SM, Lin JH, Meijer OG, Wu WH, Abbasi-Bafghi H, et al. Gait adaptations in low back pain patients with lumbar disc herniation: trunk coordination and arm swing. Eur Spine J 2011;20:491–9. Hughes AJ, Daniel SE, Blankson S, Lees AJ. A clinicopathologic study of 100 cases of Parkinson’s disease. Arch Neurol 1993;50:140–8. Kawashima N, Nozaki D, Abe MO, Nakazawa K. Shaping appropriate locomotive motor output through interlimb neural pathway within spinal cord in humans. J Neurophysiol 2008;99:2946–55. Kegelmeyer DA, Parthasarathy S, Kostyk SK, White SE, Kloos AD. Assistive devices alter gait patterns in Parkinson disease: advantages of the four-wheeled walker. Gait Posture 2013;38:20–4. Lewek MD, Poole R, Johnson J, Halawa O, Huang X. Arm swing magnitude and asymmetry during gait in the early stages of Parkinson’s disease. Gait Posture 2010;31:256–60. Li Y, Wang W, Crompton RH, Gunther MM. Free vertical moments and transverse forces in human walking and their role in relation to arm-swing. J Exp Biol 2001;204:47–58. Lovejoy CO. The natural history of human gait and posture. Part 1. Spine and pelvis. Gait Posture 2005;21:95–112. Meyns P, Bruijn SM, Duysens J. The how and why of arm swing during human walking. Gait Posture 2013;38:555–62. Morris ME, Iansek R, Matyas TA, Summers JJ. Stride length regulation in Parkinson’s disease. Normalization strategies and underlying mechanisms. Brain 1996;119:551–68. Murray MP, Sepic SB, Barnard EJ. Patterns of sagittal rotation of the upper limbs in walking. Phys Ther 1967;47:272–84. Pontzer H, Holloway JH, Raichlen DA, Lieberman DE. Control and function of arm swing in human walking and running. J Exp Biol 2009;212:523–34. Roggendorf J, Chen S, Baudrexel S, van de Loo S, Seifried C, Hilker R. Arm swing asymmetry in Parkinson’s disease measured with ultrasound based motion analysis during treadmill gait. Gait Posture 2012;35:116–20. Sofuwa O, Nieuwboer A, Desloovere K, Willems AM, Chavret F, Jonkers I. Quantitative gait analysis in Parkinson’s disease: comparison with a healthy control group. Arch Phys Med Rehabil 2005;86:1007–13. Spaulding SJ, Barber B, Colby M, Cormack B, Mick T, Jenkins ME. Cueing and gait improvement among people with Parkinson’s disease: a meta-analysis. Arch Phys Med Rehabil 2013;94:562–70. Zehr EP, Duysens J. Regulation of arm and leg movement during human locomotion. Neuroscientist 2004;10:347–61. Zifchock RA, Davis I, Hamill J. Kinetic asymmetry in female runners with and without retrospective tibial stress fractures. J Biomech 2006;39:2792–7.
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
Contents lists available at ScienceDirect
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 Department of Neurology, Haeundae Paik Hospital, Inje University, Busan, Republic of Korea 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 b c
a r t i c l e
i n f o
Article history: Accepted 6 June 2015 Available online xxxx Keywords: Arm swing Motion analysis Rehabilitation Parkinson’s disease
h i g h l i g h t s Decreased arm swing is a typical gait characteristic in Parkinson’s disease. Adding weight to the arm facilitates limb movements in Parkinson’s disease. Additional arm weight improves gait disturbance in Parkinson’s disease.
a b s t r a c t Objective: Recently, arm facilitation has been interested in gait rehabilitation. However, there have been 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 participants. We compared gait parameters including arm swing, pelvic motion, spatiotemporal data, and relative 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 significantly 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, Inje University, 875 Haeun-daero, Haeundaegu, Busan 612-030, Republic of Korea. Tel.: +82 51 797 2082; fax: +82 51 797 0640. E-mail address: [email protected] (J. Park). 1 KOJYP study group.
Gait disturbance and postural instability have been thoroughly described in Parkinson’s disease (PD). Slow velocity with shuffling, dragging steps, small stride/step length, forward-stooped gait, and 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, trunk, and pelvis, and they play an important role for postural stability and energy efficiency during walking (Dietz et al., 2001; Gutnik et al., 2005). The reduction of arm swing is one of major characteristics in patients with PD, and arm swing would be lost in the early stage of PD (Roggendorf et al., 2012). A variety of gait trainings in rehabilitation program for patients with PD have been performed to improve gait function and mobility by using a treadmill, assistive devices, and cueing strategies such as verbal, visual, or auditory cueing (Kegelmeyer et al., 2013; Spaulding et al., 2013). Recently, there is a growing interest on arm movements in patients with PD, such as arm-swing asymmetry or amplitude (Lewek et al., 2010; Roggendorf et al., 2012). Therefore, increasing arm swing also is one of the important purposes of gait rehabilitation for PD patients. Meyns et al. reported that arm facilitation in rehabilitation program for patients with PD is very important, but, to date, there is little information regarding this (Meyns et al., 2013). A vast amount of evidence has suggested that an added load to the body has an effect on altered gait parameters, and it improved postural balance (Donker et al., 2005; Duysens et al., 2000). The added weight to the arms would be effective in changing arm movements, and it could lead to influence on the interaction between limb movements during walking (Donker et al., 2005). This change of arm movement could result in the improvement of gait parameters and pelvic motion. To our knowledge, previous reports have only investigated healthy subjects, and little is known regarding the facilitation of arm movement in patients with PD. The aim of this study was to investigate whether additional arm weight could alter the gait patterns as well as arm-swing amplitude during walking in PD. We hypothesized that additional arm weight would increase arm-swing amplitude, and it would improve the spatiotemporal parameters and pelvic motion in patients with PD. 2. Methods 2.1. Study participants Twenty-seven patients with PD (15 males and 12 females) meeting the United Kingdom Parkinson’s Disease Society Brain Bank diagnostic criteria were enrolled for this study (Hughes et al., 1993). Basic demographic and clinical information were obtained including disease duration, body mass index (BMI), and disease severity. Clinical severity was assessed by the United Parkinson’s Disease Rating Scale part III (UPDRS III) and Hoehn and Yahr (H&Y) stage. The demographic data of participants are presented in Table 1. Inclusion criteria for participants were as follows: (1) in H&Y stages 2–3; (2) complaining of gait disturbance but able to walk without assistance; and (3) having proper cognition to understand the study information. Exclusion criteria were recommended for (1) any primary orthopedic, neurological diseases, and visual disturbances other than PD, and (2) having complaints that affect independent walking. All patients with PD were on medication. The study was approved by the institutional review board at the Haeundae Paik Hospital (Busan, Korea). All patients understood the study procedure and purpose, and they gave written informed consent before participation. 2.2. Gait analysis An eight-camera three-dimensional motion analysis system (Vicon, Fareham, UK) was used at a sample rate of 100 Hz for the quantification of arm swing, pelvic motions, and spatiotemporal parameters. Heel strike and toe-off were obtained from two force
Table 1 Participants’ characteristics.
Age (years) Gender Height (cm) Weight (kg) BMI (kg/m2) Duration (month) H&Y stage UPDRS III (points)
Mean ± SD
Range
74.0 ± 5.7 15 males/12 females 157.5 ± 8.2 57.9 ± 9.4 23.3 ± 2.7 22.2 ± 20.7 2.5 ± 0.5 22.8 ± 7.7
64–90 142.2–175.4 42.3–74.7 17.5–28.5 0.5–71 2–3 10–43
BMI: Body mass index; H&Y stage: Hoehn and Yahr stage; UPDRS III: Unified Parkinson’s disease scale part 3.
plates (AMTI, Watertown, MA, USA) synchronized with the Nexus program (version 1.7) for data collection at 1000 Hz, and the events of gait cycle were recorded simultaneously. In total, 16 retroreflective markers were used to indicate the segments. Twelve markers were attached on the anterior and posterior superior iliac spines, femoral epicondyle, and malleolus, second metatarsal head, and posterior calcaneus bilaterally for the kinematics of lower extremities. For the amplitude of arm swing, four markers were bilaterally placed on acromion processes and on the middle point of ulna and radius. The marker placement was performed by one experienced researcher to minimize the error. 2.3. Procedures Prior to performing the dynamic trials, all participants undertook a static trial to determine the movement of the pelvis, upper, and lower limbs. Each PD patient who took part in this study walked barefoot along a 20-foot walkway at an individually preferred pace, and the patient performed five trials with and without 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 on the distal one-third portion of the forearm bilaterally. Unfortunately, there was no report about the appropriate weight on the patient with PD. Several previous studies for healthy subjects related to the arm weight used a 1.2- or 1.8-kg weight on each arm. Considering that our subjects are old and weak, we selected 0.45 kg. No specific instructions regarding gait posture as well as arm swing were provided to participants. Each participant took a break for 1 min between tasks to minimize the fatigue. 2.4. Data analysis Motion data capture and post-processing of marker trajectories were performed using the Nexus 1.7 software (Vicon, Fareham, UK). The tri-planar motions of pelvis were calculated relative to the global coordinate system, and arm swing was calculated by the angle between the arm and virtual vertical axis. The kinematics of pelvic motions was presented for sagittal, coronal, and transverse planes defined as anterior–posterior tilt, obliquity, and rotation, respectively. Each pelvic motion was calculated as the amplitude (maximum–minimum values). The arm swing was divided into anteversion and retroversion of the shoulder joint. The anteversion was defined for maximum positive values, and the retroversion was done for minimum negative values (Fig. 1(a)). In addition, all arm-swing amplitudes including total, anteversion, and retroversion were calculated as the average of the left and right side. The relative angle of the shoulder relative to the pelvis was obtained by subtracting the virtual shoulder line through the markers on the acromion from the pelvis within each 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
3
J. Yoon et al. / Clinical Neurophysiology xxx (2015) xxx–xxx
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 closer to 0°, which indicates that the pelvis and shoulder rotation is in phase (Huang et al., 2011). The total arm-swing amplitude and total amplitude of the relative angle between the shoulder and pelvis were calculated as maximum minus minimum values during one-stride cycle. We also evaluate the effect to arm-swing asymmetry. The symmetry angle (SA), as proposed by Zifchock et al. (2006), is used to evaluate the arm-swing asymmetry in patients with PD during gait. The SA was calculated by the following equation:
X 45 arctan L X R SA ¼ 100ð%Þ 90 XL and XR are the angles of the left and right arm swing, respectively. A higher SA value indicates higher asymmetry. 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 time, stride length, double support, swing phase, and stance phase. The arm-swing amplitude and asymmetry, the relative angle between the shoulder and pelvis, and kinematic pelvic motion have been mentioned earlier. 2.5. Statistical analysis SAS software package (version 9.1, Cary, NC, USA) was used to perform the statistical analysis. For considering the difference of walking speed in each trial, we compared the gait parameters including arm and pelvic kinematics, and spatiotemporal parameters between with and without arm weights using paired t-test. The level of significance was set at p < 0.05. 3. Results 3.1. Arm swing and pelvic kinematics Table 2 summarizes the result of paired t-test for arm and pelvic kinematic parameters. Anteversion and retroversion of arm swing were significantly longer when walking with arm weights. Consequently, arm-swing amplitude also showed a significant increase when patients with PD walked with arm weights
Table 2 Comparison of the arm and pelvic kinematics with and without arm weights in PD patients.
Arm swing (°) Anteversion Retroversion Amplitude Pelvic kinematics (°) Pelvic tilt Pelvic obliquity Pelvic rotation
Without arm weight
With arm weight
P
10.15 ± 9.63 6.47 ± 9.08 16.61 ± 10.19
17.98 ± 9.16 10.06 ± 8.15 28.45 ± 12.80
0.000* 0.000* 0.000*
2.93 ± 1.13 3.98 ± 1.43 5.78 ± 2.16
2.84 ± 1.36 4.12 ± 5.09 6.70 ± 2.63
0.553* 0.559* 0.013*
Relative rotational angle (°) Shoulder pelvis 7.36 ± 4.05 amplitude
8.50 ± 4.61
0.126
Paired t-test was used for the comparison of change on each scale score between two groups. These values represented with the standard deviations. * p < 0.05.
(p < 0.05). Most patients except three patients showed increasing arm-swing amplitude, and this effect developed immediately from the first trial to the last trial. In pelvic kinematics, pelvic rotation showed a significant increase with the use of arm weights (p < 0.05). There was no difference in pelvic tilt and obliquity between gaits with and without arm weights. There was an increasing tendency to the relative angles between the shoulder and pelvis during the right and left step when patients with PD walked with arm weights; however, there was no statistical significance. Arm-swing asymmetry did not significantly differ between two conditions (p > 0.05). In total, the SA increased in 14 of 27 patients, and it decreased in 13. 3.2. Spatiotemporal parameters Table 3 shows the spatiotemporal parameters. All spatiotemporal variables were significantly different between gaits with and without arm weights. Cadence, walking speed, stride length, and swing phase of gait cycle were greater for gaits with weights than without weights (p < 0.05). Stride time, double-support time, and stance phase of gait cycle were less for gaits with arm weights than without arm weights (p < 0.05). We evaluated the correlation between arm-swing amplitude 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 Comparison of the spatiotemporal parameters with and without arm weights in PD patients.
Cadence (steps/min) Walking speed (m/s) Stride time (s) Stride length (m) Double support (s) Stance phase (% gait cycle) Swing phase (% gait cycle)
Without arm weight
With arm weight
p
101.78 ± 13.44 0.62 ± 0.19 1.21 ± 0.21 0.73 ± 0.21 0.35 ± 0.11 64.14 ± 4.02 35.57 ± 4.29
109.24 ± 12.94 0.73 ± 0.22 1.12 ± 0.15 0.81 ± 0.22 0.29 ± 0.10 62.79 ± 3.71 37.12 ± 3.67
0.000* 0.000* 0.000* 0.007* 0.000* 0.004* 0.001*
Paired t-test was used for the comparison of change on each scale score between two groups. These values represented with the standard deviations. * p < 0.05.
analysis of the relationship between arm swing and gait parameters. Walking speed and stride length showed significant correlation with the total arm-swing amplitude (r = 0.58, r = 0.57, p < 0.05). The other gait parameters including cadence, double support, stride time, swing, and stance phase were not significantly related to arm swing. 4. Discussion Our study described the effects of additional arm weights on the arm swing, pelvic kinematics, and spatiotemporal parameters in ambulating patients with PD. Several reports demonstrated that patients with PD showed reduced walking velocity and stride length and hip joint kinematics compared with healthy controls in a quantitative gait analysis (Sofuwa et al., 2005). Gait parameters, including kinematic and spatiotemporal data assessed in our study, are usually impaired in PD. In this study, arm-swing amplitude was increased with the use of weights. This finding is in line with those of previous studies, which investigated the effects of adding weights during walking in healthy controls (Duysens et al., 2000). Arm swing plays an important role for counterbalancing the movements of contralateral pelvis and lower limb, although arm swing is not regarded as an essential prerequisite for walking (Zehr and Duysens, 2004). Additional arm weights could change the inertia moments and the natural pendular frequency of upper extremities. Increased angular acceleration of arm swing was associated with increases in the angular displacement of shoulder joints, and greater anterior acceleration of shoulder joints resulted in greater arm retraction (Pontzer et al., 2009). Adding mass to the upper or lower limbs changed arm movements as a compensatory mechanism for maintaining stable gait (Bonnard and Pailhous, 1991). We postulated that increased retraction may contribute to increased total arm swing in our study. This is in line with the results found by Behrman et al. who reported that deliberately increased arm swing was the effective strategy to improve walking pattern such as increased velocity (Behrman et al., 1998). The additional sandbags to the wrist could act as a sensory input, and the perception of altered arm swing through repetitive walking could activate the motor cortex for locomotion. However, some previous studies contrast with our results. Arm-swing amplitude decreases to compensate forearm mass and to minimize the energy cost, although adding arm mass has been known to increase the muscular recruitment of the upper limbs (Donker et al., 2002). However, upper limb movements could be changed under various walking speeds on the treadmill in healthy people (Donker et al., 2005, 2002; Pontzer et al., 2009). In that study, the weight of arm loading was four times more, and gait speed also was much faster than our study (>1.5 km/h).
We postulated that light adding mass on self-preferred gait would be effective to arm facilitation in PD. Arm swing is often regarded as a way of counteracting free vertical moments caused by the swing legs (Li et al., 2001). In particular, arm retroversion provides gait stabilization by minimizing body rotation at the initial swing phase. In patients with PD, prominent impairment in arm retroversion was found to be an early sign of gait disturbance (Roggendorf et al., 2012). The arm retroversion happens throughout the swing phase from the pre-swing of ipsilateral foot-off (Murray et al., 1967). For this reason, we speculated that an increased retroversion by additional arm weights might result in an increased swing phase and a decreased stance phase. In addition, this change of gait cycle might 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 with that without weights. The pelvis plays a role as a mobile link between the two lower limbs, and an increased pelvic rotation during swing phase adds to step length (Lovejoy, 2005). The increase of the relative angle between the shoulder and pelvis indicates that the shoulder line moves more at an antiphase with the pelvic line. This mild increase could have an effect on the increased pelvic rotation by improved coordination between the shoulder and pelvis. We postulated that the greater pelvic rotation in our result may be a cause for the increased stride length. However, adding arm weights did not significantly change the trunk coordination in PD patients. PD patients walked using a similar strategy as patients with low back pain who keep the stiff trunk and swing the arm more (Huang et al., 2011). Cadence is defined as the number of steps per minute. An increase in cadence may be considered as an increased stride frequency and walking speed. In addition, walking speed is determined by the combination of stride length and frequency (Huang et al., 2010). In our study, cadence, walking speed, and stride length were increased, and the stride time was decreased when walking with arm weights. This indicates that adding arm weights results in the improvement of gait by increasing the stride length as well as frequency. Although cadence is considered to be increased in PD, evidence is controversial. Some reports showed normal or decreased cadence in PD (Morris et al., 1996). Unfortunately, we did not compare the cadence between normal controls and PD group. As per our result, we assumed that cadence might not be increased in participants compared with normal controls. Further studies are warranted comparing cadence with normal controls. Dietz and Michel verified that patients with PD preserve basic quadrupedal limb coordination (Dietz and Michel, 2008). The authors suggest that the arm and leg are coupling via the activity of spinal interneuron. Neural connections between the upper and lower limbs exist, which increases muscle activation in another limb during rhythmic tasks (Huang and Ferris, 2009; Kawashima et al., 2008). In addition, Bruijn et al. found that arm and leg movements contribute to control the body angular momentum compared with the pelvis or thorax movement (Bruijn et al., 2008). Our results showed that arm-swing amplitude was correlated with stride length, which is in accordance with previous reports. With such findings, the alteration of spatiotemporal parameters when walking with arm weights might be explained in respect of synchronizing the upper and lower limb movements. Based on previous reports, we speculated that an increased arm movement may facilitate lower limb movement especially stride length via spino-bulbar-spinal reflex pathway. There were several limitations in this study. We did not compare the results with a control group, so we could not exclude a 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
proximal arms and forearm as one mechanical segment for arm swing; hence, the elbow motion and the arm length were ignored. The sandbag with the same weight was applied to all participants who had various body metrics, so we did not control the arm-swing symmetry and could not investigate the best appropriate weight to improve gait parameters. We only compared changes in short-term responses, thus making it difficult to confirm whether the effects will continue for a long time. Further studies should investigate the effects of various weights to improve the arm-swing symmetry during walking and the long-term effect of adding arm weights for the gait training in patients with PD. In conclusion, adding arm weights during walking is useful in facilitating the arm swing, and it improves the gait patterns in patients with PD. Therefore, the effort of the upper limb may influence lower limb rehabilitation in patients with PD. Acknowledgement This research is supported by Soonchunhyang University hospital. Conflicts of interest: The authors have no potential conflicts of interest to report concerning this article, and they have nothing to disclose. References Behrman AL, Teitelbaum P, Cauraugh JH. Verbal instructional sets to normalise the temporal and spatial gait variables in Parkinson’s disease. J Neurol Neurosurg Psychiatry 1998;65:580–2. Bonnard M, Pailhous J. Intentional compensation for selective loading affecting human gait phases. J Mot Behav 1991;23:4–12. Bruijn SM, Meijer OG, van Dieen JH, Kingma I, Lamoth CJ. Coordination of leg swing, thorax rotations, and pelvis rotations during gait: the organisation of total body angular momentum. Gait Posture 2008;27:455–62. Dietz V, Fouad K, Bastiaanse CM. Neuronal coordination of arm and leg movements during human locomotion. Eur J Neurosci 2001;14:1906–14. Dietz V, Michel J. Locomotion in Parkinson’s disease: neuronal coupling of upper and lower limbs. Brain 2008;131:3421–31. Donker SF, Daffertshofer A, Beek PJ. Effects of velocity and limb loading on the coordination between limb movements during walking. J Mot Behav 2005;37:217–30. Donker SF, Mulder T, Nienhuis B, Duysens J. Adaptations in arm movements for added mass to wrist or ankle during walking. Exp Brain Res 2002;146:26–31.
5
Duysens J, Clarac F, Cruse H. Load-regulating mechanisms in gait and posture: comparative aspects. Physiol Rev 2000;80:83–133. Gutnik B, Mackie H, Hudson G, Standen C. How close to a pendulum is human upper limb movement during walking? Homo 2005;56:35–49. Huang HJ, Ferris DP. Upper and lower limb muscle activation is bidirectionally and ipsilaterally coupled. Med Sci Sports Exerc 2009;41:1778–89. Huang Y, Meijer OG, Lin J, Bruijn SM, Wu W, Lin X, et al. The effects of stride length and stride frequency on trunk coordination in human walking. Gait Posture 2010;31:444–9. Huang YP, Bruijn SM, Lin JH, Meijer OG, Wu WH, Abbasi-Bafghi H, et al. Gait adaptations in low back pain patients with lumbar disc herniation: trunk coordination and arm swing. Eur Spine J 2011;20:491–9. Hughes AJ, Daniel SE, Blankson S, Lees AJ. A clinicopathologic study of 100 cases of Parkinson’s disease. Arch Neurol 1993;50:140–8. Kawashima N, Nozaki D, Abe MO, Nakazawa K. Shaping appropriate locomotive motor output through interlimb neural pathway within spinal cord in humans. J Neurophysiol 2008;99:2946–55. Kegelmeyer DA, Parthasarathy S, Kostyk SK, White SE, Kloos AD. Assistive devices alter gait patterns in Parkinson disease: advantages of the four-wheeled walker. Gait Posture 2013;38:20–4. Lewek MD, Poole R, Johnson J, Halawa O, Huang X. Arm swing magnitude and asymmetry during gait in the early stages of Parkinson’s disease. Gait Posture 2010;31:256–60. Li Y, Wang W, Crompton RH, Gunther MM. Free vertical moments and transverse forces in human walking and their role in relation to arm-swing. J Exp Biol 2001;204:47–58. Lovejoy CO. The natural history of human gait and posture. Part 1. Spine and pelvis. Gait Posture 2005;21:95–112. Meyns P, Bruijn SM, Duysens J. The how and why of arm swing during human walking. Gait Posture 2013;38:555–62. Morris ME, Iansek R, Matyas TA, Summers JJ. Stride length regulation in Parkinson’s disease. Normalization strategies and underlying mechanisms. Brain 1996;119:551–68. Murray MP, Sepic SB, Barnard EJ. Patterns of sagittal rotation of the upper limbs in walking. Phys Ther 1967;47:272–84. Pontzer H, Holloway JH, Raichlen DA, Lieberman DE. Control and function of arm swing in human walking and running. J Exp Biol 2009;212:523–34. Roggendorf J, Chen S, Baudrexel S, van de Loo S, Seifried C, Hilker R. Arm swing asymmetry in Parkinson’s disease measured with ultrasound based motion analysis during treadmill gait. Gait Posture 2012;35:116–20. Sofuwa O, Nieuwboer A, Desloovere K, Willems AM, Chavret F, Jonkers I. Quantitative gait analysis in Parkinson’s disease: comparison with a healthy control group. Arch Phys Med Rehabil 2005;86:1007–13. Spaulding SJ, Barber B, Colby M, Cormack B, Mick T, Jenkins ME. Cueing and gait improvement among people with Parkinson’s disease: a meta-analysis. Arch Phys Med Rehabil 2013;94:562–70. Zehr EP, Duysens J. Regulation of arm and leg movement during human locomotion. Neuroscientist 2004;10:347–61. Zifchock RA, Davis I, Hamill J. Kinetic asymmetry in female runners with and without retrospective tibial stress fractures. J Biomech 2006;39:2792–7.
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