Please wait a minute...
 Home  About the Journal Editorial Board Aims & Scope Peer Review Policy Subscription Contact us
Early Edition  //  Current Issue  //  Open Special Issues  //  Archives  //  Most Read  //  Most Downloaded  //  Most Cited
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.
Download: PDF(769 KB)   HTML
Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks    

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  
E-mail this article
E-mail Alert
Articles by authors
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
URL:     OR
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
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
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
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.
[1] Doherty KM, van de Warrenburg BP, Peralta MC, Silveira-Moriyama L, Azulay JP, Gershanik OS, et al. (2011). Postural deformities in Parkinson's disease. Lancet Neurol, 10:538-549.
[2] Ponfick M, Gdynia HJ, Ludolph AC, Kassubek J (2011). Camptocormia in Parkinson's disease: a review of the literature. Neurodegener Dis, 8:283-288.
[3] Barone P, Santangelo G, Amboni M, Pellecchia MT, Vitale C (2016). Pisa syndrome in Parkinson's disease and parkinsonism: clinical features, pathophysiology, and treatment. Lancet Neurology, 15:1063-1074.
[4] Nakane S, Yoshioka M, Oda N, Tani T, Chida K, Suzuki M, et al. (2015). The characteristics of camptocormia in patients with Parkinson's disease: A large cross-sectional multicenter study in Japan. J Neurol Sci, 358:299-303.
[5] Srivanitchapoom P, Hallett M (2016). Camptocormia in Parkinson's disease: definition, epidemiology, pathogenesis and treatment modalities. J Neurol Neurosurg Psychiatry, 87:75-85.
[6] Vorovenci RJ, Biundo R, Antonini A (2016). Therapy-resistant symptoms in Parkinson's disease. J Neural Transm (Vienna), 123:19-30.
[7] Bonneville F, Bloch F, Kurys E, du Montcel ST, Welter ML, Bonnet AM, et al. (2008). Camptocormia and Parkinson's disease: MR imaging. Eur Radiol, 18:1710-1719.
[8] Frazzitta G, Balbi P, Gotti F, Maestri R, Sabetta A, Caremani L, et al. (2015). Pisa Syndrome in Parkinson's Disease: Electromyographic Aspects and Implications for Rehabilitation. Parkinsons Disease.
[9] Tinazzi M, Juergenson I, Squintani G, Vattemi G, Montemezzi S, Censi D, et al. (2013). Pisa syndrome in Parkinson's disease: an electrophysiological and imaging study. Journal of Neurology, 260:2138-2148.
[10] Margraf NG, Rohr A, Granert O, Hampel J, Drews A, Deuschl G (2015). MRI of lumbar trunk muscles in patients with Parkinson's disease and camptocormia. J Neurol, 262:1655-1664.
[11] Indovina I, Riccelli R, Chiarella G, Petrolo C, Augimeri A, Giofre L, et al. (2015). Role of the Insula and Vestibular System in Patients with Chronic Subjective Dizziness: An fMRI Study Using Sound-Evoked Vestibular Stimulation. Front Behav Neurosci, 9:334.
[12] Gallea C, Ewenczyk C, Degos B, Welter ML, Grabli D, Leu-Semenescu S, et al. (2017). Pedunculopontine network dysfunction in Parkinson's disease with postural control and sleep disorders. Mov Disord, 32:693-704.
[13] Lesourd M, Osiurak F, Baumard J, Bartolo A, Vanbellingen T, Reynaud E (2018). Cerebral correlates of imitation of intransitive gestures: An integrative review of neuroimaging data and brain lesion studies. Neurosci Biobehav Rev, 95:44-60.
[14] Tramonti C, Di Martino S, Unti E, Frosini D, Bonuccelli U, Rossi B, et al. (2017). Gait dynamics in Pisa syndrome and Camptocormia: The role of stride length and hip kinematics. Gait Posture, 57:130-135.
[15] Barkhof F, Haller S, Rombouts SA (2014). Resting-state functional MR imaging: a new window to the brain. Radiology, 272:29-49.
[16] Fjell AM, Westlye LT, Greve DN, Fischl B, Benner T, van der Kouwe AJ, et al. (2008). The relationship between diffusion tensor imaging and volumetry as measures of white matter properties. Neuroimage, 42:1654-1668.
[17] Postuma RB, Berg D, Stern M, Poewe W, Olanow CW, Oertel W, et al. (2015). MDS clinical diagnostic criteria for Parkinson's disease. Mov Disord, 30:1591-1601.
[18] Ou R, Liu H, Hou Y, Song W, Cao B, Wei Q, et al. (2018). Predictors of camptocormia in patients with Parkinson's disease: A prospective study from southwest China. Parkinsonism Relat Disord, 52:69-75.
[19] Huh YE, Kim K, Chung WH, Youn J, Kim S, Cho JW (2018). Pisa Syndrome in Parkinson's Disease: Pathogenic Roles of Verticality Perception Deficits. Scientific Reports, 8.
[20] Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P, et al. (2008). Movement Disorder Society-sponsored revision of the Unified Parkinson's Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord, 23:2129-2170.
[21] Hoehn MM, Yahr MD (1967). Parkinsonism: onset, progression and mortality. Neurology, 17:427-442.
[22] Folstein MF, Folstein SE, McHugh PR (1975). "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res, 12:189-198.
[23] Nasreddine ZS, Phillips NA, Bedirian V, Charbonneau S, Whitehead V, Collin I, et al. (2005). The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc, 53:695-699.
[24] Berg KO, Wood-Dauphinee SL, Williams JI, Maki B (1992). Measuring balance in the elderly: validation of an instrument. Can J Public Health, 83 Suppl 2:S7-11.
[25] Podsiadlo D, Richardson S (1991). The timed "Up & Go": a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc, 39:142-148.
[26] Wang J, Wang X, Xia M, Liao X, Evans A, He Y (2015). GRETNA: a graph theoretical network analysis toolbox for imaging connectomics. Front Hum Neurosci, 9:386.
[27] Lo OY, Halko MA, Zhou J, Harrison R, Lipsitz LA, Manor B (2017). Gait Speed and Gait Variability Are Associated with Different Functional Brain Networks. Front Aging Neurosci, 9:390.
[28] Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, et al. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage, 15:273-289.
[29] Yan CG, Wang XD, Zuo XN, Zang YF (2016). DPABI: Data Processing & Analysis for (Resting-State) Brain Imaging. Neuroinformatics, 14:339-351.
[30] Song XW, Dong ZY, Long XY, Li SF, Zuo XN, Zhu CZ, et al. (2011). REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS One, 6:e25031.
[31] Smith SM (2002). Fast robust automated brain extraction. Hum Brain Mapp, 17:143-155.
[32] Andersson JLR, Sotiropoulos SN (2016). An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging. Neuroimage, 125:1063-1078.
[33] Cui Z, Zhong S, Xu P, He Y, Gong G (2013). PANDA: a pipeline toolbox for analyzing brain diffusion images. Front Hum Neurosci, 7:42.
[34] Eloy M-H, Federico V, Vesna P, Carlos L, Magí A, Elena HM-L, et al.2015. Deterministic DTI tractography based on fiber assignement by continuous tracking (FACT) in ten healthy subjects in two HARDI datasets.
[35] Moraud EM, von Zitzewitz J, Miehlbradt J, Wurth S, Formento E, DiGiovanna J, et al. (2018). Closed-loop control of trunk posture improves locomotion through the regulation of leg proprioceptive feedback after spinal cord injury. Sci Rep, 8:76.
[36] Veneman JF, Menger J, van Asseldonk EH, van der Helm FC, van der Kooij H (2008). Fixating the pelvis in the horizontal plane affects gait characteristics. Gait Posture, 28:157-163.
[37] Varghese JP, Merino DM, Beyer KB, McIlroy WE (2016). Cortical control of anticipatory postural adjustments prior to stepping. Neuroscience, 313:99-109.
[38] Abe K, Uchida Y, Notani M (2010). Camptocormia in Parkinson's disease. Parkinsons Dis, 2010.
[39] Hamacher D, Herold F, Wiegel P, Hamacher D, Schega L (2015). Brain activity during walking: A systematic review. Neurosci Biobehav Rev, 57:310-327.
[40] Mihara M, Miyai I, Hattori N, Hatakenaka M, Yagura H, Kawano T, et al. (2012). Cortical control of postural balance in patients with hemiplegic stroke. Neuroreport, 23:314-319.
[1] Tan Yuan, Ke Minjing, Huang Zhijian, Chong Cheong-Meng, Cen Xiaotong, Lu Jia-Hong, Yao Xiaoli, Qin Dajiang, Su Huanxing. Hydroxyurea Facilitates Manifestation of Disease Relevant Phenotypes in Patients-Derived IPSCs-Based Modeling of Late-Onset Parkinson’s Disease[J]. Aging and disease, 2019, 10(5): 1037-1048.
[2] Qian Elizabeth, Huang Yue. Subtyping of Parkinson’s Disease - Where Are We Up To?[J]. Aging and disease, 2019, 10(5): 1130-1139.
[3] Jinghui Xu, Xiaodi Fu, Mengqiu Pan, Xiao Zhou, Zhaoyu Chen, Dongmei Wang, Xiaomei Zhang, Qiong Chen, Yanhui Li, Xiaoxian Huang, Guanghui Liu, Jianjun Lu, Yan Liu, Yafang Hu, Suyue Pan, Qing Wang, Qun Wang, Yunqi Xu. Mitochondrial Creatine Kinase is Decreased in the Serum of Idiopathic Parkinson’s Disease Patients[J]. Aging and disease, 2019, 10(3): 601-610.
[4] Shigeki Yamada,Yukihiko Aoyagi,Kazuo Yamamoto,Masatsune Ishikawa. Quantitative Evaluation of Gait Disturbance on an Instrumented Timed Up-and-go Test[J]. Aging and disease, 2019, 10(1): 23-36.
[5] Yong-Fei Zhao, Qiong Zhang, Jian-Feng Zhang, Zhi-Yin Lou, Hen-Bing Zu, Zi-Gao Wang, Wei-Cheng Zeng, Kai Yao, Bao-Guo Xiao. The Synergy of Aging and LPS Exposure in a Mouse Model of Parkinson’s Disease[J]. Aging and disease, 2018, 9(5): 785-797.
[6] Mock J. Thomas, Knight Sherilynn G, Vann Philip H, Wong Jessica M, Davis Delaney L, Forster Michael J, Sumien Nathalie. Gait Analyses in Mice: Effects of Age and Glutathione Deficiency[J]. Aging and disease, 2018, 9(4): 634-646.
[7] Zhang Li, Hao Junwei, Zheng Yan, Su Ruijun, Liao Yajin, Gong Xiaoli, Liu Limin, Wang Xiaomin. Fucoidan Protects Dopaminergic Neurons by Enhancing the Mitochondrial Function in a Rotenone-induced Rat Model of Parkinson’s Disease[J]. Aging and disease, 2018, 9(4): 590-604.
[8] De Lazzari Federica, Bubacco Luigi, Whitworth Alexander J, Bisaglia Marco. Superoxide Radical Dismutation as New Therapeutic Strategy in Parkinson’s Disease[J]. Aging and disease, 2018, 9(4): 716-728.
[9] Perez-Roca Laia, Adame-Castillo Cristina, Campdelacreu Jaume, Ispierto Lourdes, Vilas Dolores, Rene Ramon, Alvarez Ramiro, Gascon-Bayarri Jordi, Serrano-Munoz Maria A., Ariza Aurelio, Beyer Katrin. Glucocerebrosidase mRNA is Diminished in Brain of Lewy Body Diseases and Changes with Disease Progression in Blood[J]. Aging and disease, 2018, 9(2): 208-219.
[10] Zhang Meng, Deng Yong-Ning, Zhang Jing-Yi, Liu Jie, Li Yan-Bo, Su Hua, Qu Qiu-Min. SIRT3 Protects Rotenone-induced Injury in SH-SY5Y Cells by Promoting Autophagy through the LKB1-AMPK-mTOR Pathway[J]. Aging and disease, 2018, 9(2): 273-286.
[11] Sun Qian, Wang Tian, Jiang Tian-Fang, Huang Pei, Wang Ying, Xiao Qin, Liu Jun, Chen Sheng-Di. Clinical Profile of Chinese Long-Term Parkinson’s Disease Survivors With 10 Years of Disease Duration and Beyond[J]. Aging and disease, 2018, 9(1): 8-16.
[12] Su Ruijun, Sun Min, Wang Wei, Zhang Jianliang, Zhang Li, Zhen Junli, Qian Yanjing, Zheng Yan, Wang Xiaomin. A Novel Immunosuppressor, (5R)-5-Hydroxytriptolide, Alleviates Movement Disorder and Neuroinflammation in a 6-OHDA Hemiparkinsonian Rat Model[J]. Aging and disease, 2017, 8(1): 31-43.
[13] Lv Deyong, Li Jingbo, Li Hongfu, Fu Yu, Wang Wei. Imaging and Quantitative Analysis of the Interstitial Space in the Caudate Nucleus in a Rotenone-Induced Rat Model of Parkinson’s Disease Using Tracer-based MRI[J]. Aging and disease, 2017, 8(1): 1-6.
[14] Smirnova Natalya A., Kaidery Navneet Ammal, Hushpulian Dmitry M., Rakhman Ilay I., Poloznikov Andrey A., Tishkov Vladimir I., Karuppagounder Saravanan S., Gaisina Irina N., Pekcec Anton, Leyen Klaus Van, Kazakov Sergey V., Yang Lichuan, Thomas Bobby, Ratan Rajiv R., Gazaryan Irina G.. Bioactive Flavonoids and Catechols as Hif1 and Nrf2 Protein Stabilizers - Implications for Parkinson’s Disease[J]. Aging and disease, 2016, 7(6): 745-762.
[15] Sterling Nicholas W., Lichtenstein Maya, Lee Eun-Young, Lewis Mechelle M., Evans Alicia, Eslinger Paul J., Du Guangwei, Gao Xiang, Chen Honglei, Kong Lan, Huang Xuemei. Higher Plasma LDL-Cholesterol is Associated with Preserved Executive and Fine Motor Functions in Parkinson’s Disease[J]. Aging and disease, 2016, 7(3): 237-245.
Full text



Copyright © 2014 Aging and Disease, All Rights Reserved.
Address: Aging and Disease Editorial Office 3400 Camp Bowie Boulevard Fort Worth, TX76106 USA
Fax: (817) 735-0408 E-mail:
Powered by Beijing Magtech Co. Ltd