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Aging and disease
Orginal Article |
Gait Characteristics and Brain Activity in Parkinson’s Disease with Concomitant Postural Abnormalities
Meng-sha Yao1,#, Li-che Zhou1,#, Yu-yan Tan1, Hong Jiang2, Zhi-chun Chen1, Lin Zhu1, Ning-di Luo1, Quan-zhou Wu3, Wen-yan Kang1,4,*, Jun Liu1,*
1Department of Neurology & Collaborative Innovation Center for Brain Science, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
2Department of Neurosurgery, Ruijin Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
3State Key Laboratory of ISN, School of Computer Science and Technology, Xidian University, Xi'an, Shanxi Province, China.
4Department of Neurology, Ruijin Hospital North, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
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Abstract  

To explore the underlying pathogenic mechanism of Parkinson’s disease (PD) with concomitant postural abnormalities (PDPA) through the relationship between its gait and brain function characteristics. PD patients from the neurology outpatient clinic at Ruijin Hospital were recruited and grouped according to whether postural abnormalities (including camptocormia and Pisa syndrome) were present. PD-related scale assessments, three-dimensional gait tests and brain resting-state functional magnetic imaging were performed and analyzed. The gait characteristics independently associated with PDPA were decreased pelvic obliquity angle and progressive downward movement of the center of mass during walking. PDPA features included decreased functional connectivity between the left insula and bilateral supplementary motor area, which was significantly correlated with reduced Berg Balance Scale scores. Functional connectivity between the right insula and bilateral middle frontal gyrus was decreased and significantly correlated with a decreased pelvic obliquity angle and poor performance on the Timed Up and Go test. Moreover, through diffusion tensor imaging analysis, the average fractional anisotropy value of the fibers connecting the left insula and left supplementary motor area was shown to be decreased in PDPA. There is decreased functional connectivity among the insula, supplementary motor area and middle frontal gyrus with structural abnormalities between the left insula and the left supplementary motor area; these changes in brain connectivity are probably among the causes of gait dysfunction in PDPA and provide some clues regarding the pathogenic mechanisms of PDPA.

Keywords Parkinson’s disease      postural abnormality      camptocormia      Pisa syndrome      gait     
Corresponding Authors: Wen-yan Kang,Jun Liu   
About author: These authors contributed equally to this work.
Just Accepted Date: 02 October 2019  
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Meng-sha Yao
Li-che Zhou
Yu-yan Tan
Hong Jiang
Zhi-chun Chen
Lin Zhu
Ning-di Luo
Quan-zhou Wu
Wen-yan Kang
Jun Liu
Cite this article:   
Meng-sha Yao,Li-che Zhou,Yu-yan Tan, et al. Gait Characteristics and Brain Activity in Parkinson’s Disease with Concomitant Postural Abnormalities[J]. Aging and disease, 10.14336/AD.2019.0929
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http://www.aginganddisease.org/EN/10.14336/AD.2019.0929     OR     http://www.aginganddisease.org/EN/Y0/V/I/0
PD - CCPS (n=21)PD + CCPS (n=16)p value
Age (y)64.7±4.569.0±8.40.079a
Sex (female/male, n)11/108/80.886b
BMI (kg/m2)23.3±3.723.9±3.10.616a
Education (y)10.2±3.210.6±4.20.762a
Disease duration (y)5.4±4.47.3±4.50.226a
Hoehn-Yahr stage2.0(1.0, 2.0)2.5(1.6, 3.0)0.006c
LEDD (mg)405.64±353.76d724.10±276.660.006a
MDS-UPDRS III29.0±12.239.4±12.30.023a
MMSE28.0(24.5, 28.5)27.0(26.0, 28.0)0.844c
MoCA22.7±3.922.2±5.40.757a
Table 1  Baseline information of PD patients enrolled in gait analyses.
PD - CCPS (n=13)PD + CCPS (n=7)p value
Age (y)65.0±5.469.7±8.20.138a
Sex (female/male, n)6/74/31.000b
BMI (kg/m2)23.12±4.4823.79±3.440.735a
Education (y)12.0(9.0, 13.0)10.0(8.0, 14.0)0.699c
Disease duration (y)5.4±4.98.4±5.00.215a
Hoehn-Yahr stage1.7±0.72.2±0.70.116a
MDS-UPDRS III31.6±13.835.1±12.50.581a
LEDD (mg)346.32±372.29d606.07±213.810.111a
MMSE28.0(26.0, 29.0)27.0(25.0, 27.0)0.056c
MoCA23.9±3.020.6±6.60.140a
Table 2  Baseline information of PD patients enrolled in MRI analyses.
Figure 1.  T value graphs of two independent samples t-test for brain FC between two groups. (A) With the right middle frontal gyrus as the ROI, the FC between the ROI and right insula (peak MNI coordinates: x=38, y=11, z=1) was found to be significantly decreased in the PD + CCPS group. (B) With the left insula as the ROI, the FC between the ROI and bilateral SMA (peak MNI coordinates: left: x=-1, y=-8, z=69; right: x=7, y=-6, z=70) decreased significantly in the PD + CCPS group. (C) With the right insula as the ROI, the FC between the ROI and left middle frontal gyrus (peak MNI coordinates: x=-30, y=40, z=25) decreased significantly in the PD + CCPS group. Color bar indicates the significance levels in the clusters in t values. (p<0.05, TFCE corrected) FC: functional connectivity; ROI: region of interest; SMA: supplementary motor area; MNI: Montreal Neurological Institute.
Figure 2.  Correlation between FC and gait parameters. (A) Decreased FC between the left insula and bilateral SMA was significantly correlated with lower BBS score and (B) that between the right insula and bilateral middle frontal gyrus was correlated with decreased pelvic obliquity angle and (C) significantly longer time needed in the TUG test (p<0.05, AlphaSim corrected). The color bar indicates the correlation levels in the clusters in r values. FC: functional connectivity; SMA: supplementary motor area; BBS: Berg Balance Scale; TUG: Timed Up and Go Test.
PD - CCPS (n=21)PD + CCPS (n=16)p value
Gait-related scales
BBS54.0(50.0, 55.0)a43.5(40.3, 49.8)0.002b
TUG (s)10.3(8.5, 12.2)a16.1(10.8, 18.5)0.004b
Kinematic parameters
Cadence (steps/min)105.0±12.8104.4±14.80.905c
Double support time (s)0.24(0.21, 0.31)0.25(0.22, 0.30)0.660b
Step time (s)0.6±0.10.6±0.10.937c
Step length/height (m/m)0.32(0.30, 0.35)0.30(0.26, 0.34)0.059b
Step width/height (m/m)0.09(0.07, 0.10)0.09(0.06, 0.11)0.774b
Stride time (s)1.2±0.11.2±0.20.842c
Stride length/height (m/m)0.64±0.070.58±0.130.068c
Walking speed/height (/s)0.56±0.110.50±0.130.138c
Dynamic parameters
Pelvic tilt (°)19.0±7.122.2±9.50.256c
Pelvic obliquity (°)5.3(4.4, 6.8)3.7(3.0, 4.3)0.004b
Pelvic rotation (°)8.2(5.3, 9.5)7.7(4.2, 13.0)1.000b
Knee flexion range (°)54.5±8.554.9±11.10.903c
Ankle flexion range (°)29.7±5.329.7±5.70.989c
CoM
Lowering of CoM (yes/no, n)5/169/6d0.028e
Table 3  Gait parameters of PD patients.
Univariate analysisMultivariate analysis
p valueOR95%CIp valueOR95%CI
Pelvic obliquity (°)0.0170.546(0.332-0.899)0.0190.458(0.239-0.877)
Lowering of CoM (yes)0.0334.800(1.137-20.272)0.0238.897(1.355-58.444)
Table 4  Independently associated factors within the gait parameters of PDPA.
Figure 3.  Comparison of average FA between two groups. The PD + CCPS group exhibited decreased structural connectivity compared with the PD - CCPS group in the fiber connecting the left insula and left SMA (red nodes and red thick lines; p = 0.019). No significant differences in the other fibers were found between the two groups (p > 0.05; yellow nodes and yellow thin lines). SMA.L: left supplementary motor area; SMA.R: right supplementary motor area; INS.L: left insula; INS.R: right insula; SFGdor.L: left dorsal superior frontal gyrus; SFGdor.R: right dorsal superior frontal gyrus; MFG.L: left middle frontal gyrus; MFG.R: right middle frontal gyrus; ORBinf.L: orbital part of left inferior frontal gyrus; ORBinf.R: orbital part of right inferior frontal gyrus.
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