C-Gait for Detecting Freezing of Gait in the Early to Middle Stages of Parkinson's Disease: A Model Prediction Study

Zi-Yan Chen, Hong-Jiao Yan, Lin Qi, Qiao-Xia Zhen, Cui Liu, Ping Wang, Yong-Hong Liu, Rui-Dan Wang, Yan-Jun Liu, Jin-Ping Fang, Yuan Su, Xiao-Yan Yan, Ai-Xian Liu, Jianing Xi, Boyan Fang, Zi-Yan Chen, Hong-Jiao Yan, Lin Qi, Qiao-Xia Zhen, Cui Liu, Ping Wang, Yong-Hong Liu, Rui-Dan Wang, Yan-Jun Liu, Jin-Ping Fang, Yuan Su, Xiao-Yan Yan, Ai-Xian Liu, Jianing Xi, Boyan Fang

Abstract

Objective: Efficient methods for assessing walking adaptability in individuals with Parkinson's disease (PD) are urgently needed. Therefore, this study aimed to assess C-Gait for detecting freezing of gait (FOG) in patients with early- to middle-stage PD.

Method: People with PD (PWP) diagnosis (Hoehn and Yahr stages 1-3) were recruited from April 2019 to November 2019 in Beijing Rehabilitation Hospital. The participants performed six items of walking adaptability on an instrumented treadmill augmented with visual targets and obstacles (C-Mill). The patient's walking adaptability was evaluated by C-Gait assessment and traditional walking tests, and FOG-related indexes were collected as outcome measures. Two discriminant models were established by stepwise discriminant analysis; area under the receiver operating characteristic (ROC) curve (AUC) was used to validate the models.

Result: In total, 53 patients were included in this study. Most C-Gait assessment items had no or low correlations with traditional walking tests. The obstacle avoidance (r = -0.639, P = 0.003) and speed of adaptation (r = -0.486, P = 0.035) items could lead to FOG with high sensitivity. In addition, the C-Gait assessment model (AUC = 0.755) had slightly better discrimination of freezers from non-freezers compared with traditional walking test models (AUC = 0.672); specifically, obstacle avoidance and speed of adaptation have uniquely discriminant potential.

Conclusion: C-gait assessment could provide additional value to the traditional walking tests for PD. Gait adaptability assessment, as measured by C-Gait, may be able to help identify freezers in a PD population.

Keywords: C-Gait assessment; Parkinson’s disease; freezing of gait; rehabilitation; walking adaptability.

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2021 Chen, Yan, Qi, Zhen, Liu, Wang, Liu, Wang, Liu, Fang, Su, Yan, Liu, Xi and Fang.

Figures

FIGURE 1
FIGURE 1
Spearman’s correlation coefficients between C-Gait assessment scores. In this study, correlation coefficients of 0–0.25, 0.25–0.50, 0.50–0.75, and 0.75–1.00 were considered to indicate very low, low, moderate, and high correlations, respectively. Slalom walking (SW), tandem walking (TW), obstacle avoidance (OA), visually guided stepping (VGS), reaction to unexpected perturbation (RUP), and speed of adaptation (SA) were on the x-axis, while traditional walking test measures were on the y-axis, i.e., The New Freezing of Gait Questionnaire (NFOG-Q), Unified Parkinson’s Disease Rating Scale Part III, item 11, and Freezing of Gait (UPDRS 3.11 FOG). Color types and shades provide a visualization of the direction and strength of the correlations, respectively. The numbers shown in each square correspond to different colors, indicating the Spearman’s correlation coefficient (rs) from Spearman’s rank correlation analysis of each pair. * Correlation is statistically significant at the P < 0.05 level; ** Correlation is statistically significant at the P < 0.01 level.
FIGURE 2
FIGURE 2
Receiver operating characteristic (ROC) curves of two discriminant models for freezing of gait (FOG). The areas under the ROC curves (AUCs) for DM1 and DM2 were 0.672 and 0.755, respectively. DM1, discriminant model 1 (traditional walking tests); DM2, discriminant model 2 (C-Gait assessment).

References

    1. Alcock L., Galna B., Hausdorff J. M., Lord S., Rochester L. (2018). Gait & posture special issue: gait adaptations in response to obstacle type in fallers with Parkinson’s disease. Gait Posture 61 368–374. 10.1016/j.gaitpost.2018.01.030
    1. Alves G., Forsaa E. B., Pedersen K. F., Gjerstad M. D., Larsen J. P. (2008). Epidemiology of Parkinson’s disease. J. Neurol. 255 18–32. 10.1007/s00415-008-5004-3
    1. Balasubramanian C. K., Clark D. J., Fox E. J. (2014). Walking adaptability after a stroke and its assessment in clinical settings. Stroke Res. Treat. 2014 142–162. 10.1155/2014/591013
    1. Bloem B. R., Marinus J., Almeida Q., Dibble L., Nieuwboer A., Post B., et al. (2016). Measurement instruments to assess posture, gait, and balance in Parkinson’s disease: critique and recommendations. Mov. Disord. 31 1342–1355. 10.1002/mds.26572
    1. Caetano M. J. D., Lord S. R., Allen N. E., Brodie M. A., Song J., Paul S. S., et al. (2017). Stepping reaction time and gait adaptability are significantly impaired in people with Parkinson’s disease: implications for fall risk. Parkinsonism Relat. Disord. 47 32–38. 10.1016/j.parkreldis.2017.11.340
    1. Choi S. M., Jung H. J., Yoon G. J., Kim B. C. (2019). Factors associated with freezing of gait in patients with Parkinson’s disease. Neurol. Sci. 40 293–298. 10.1007/s10072-018-3625-6
    1. Coolen B., Beek P. J., Geerse D. J., Roerdink M. (2020). Avoiding 3D obstacles in mixed reality: does it differ from negotiating real obstacles? Sensors 20:1095. 10.3390/s20041095
    1. Cools R., Barker R. A., Sahakian B. J., Robbins T. W. L. (2003). Dopa medication remediates cognitive inflexibility, but increases impulsivity in patients with Parkinson’s disease. Neuropsychologia 41 1431–1441. 10.1016/s0028-3932(03)00117-9
    1. Cooper J. A., Sagar H. J., Tidswell P., Jordan N. (1994). Slowed central processing in simple and go/no-go reaction time tasks in Parkinson’s disease. Brain 117 517–529. 10.1093/brain/117.3.517
    1. Duncan R. P., Leddy A. L., Earhart G. M. (2011). Five times sit-to-stand test performance in Parkinson’s Disease. Arch. Phys. Med. Rehabil. 92 1431–1436. 10.1016/j.apmr.2011.04.008
    1. Folstein M. F., Folstein S. E., McHugh P. R. (1975). “Mini-mental state”: a practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 12 189–198. 10.1016/0022-3956(75)90026-6
    1. Galna B., Murphy A. T., Morris M. E. (2013). Obstacle crossing in Parkinson’s disease: mediolateral sway of the centre of mass during level-ground walking and obstacle crossing. Gait Posture 38 790–794. 10.1016/j.gaitpost.2013.03.024
    1. Geerse D. J., Roerdink M., Marinus J., Hilten J. J. (2018). Assessing Walking Adaptability in Parkinson’s disease: “the interactive walkway”. Front. Neurol. 9:1096. 10.3389/fneur.2018.01096
    1. Grillner S., Wallen P. (1985). Central pattern generators for locomotion, with special reference to vertebrates. Annu. Rev. Neurosci. 8 233–261. 10.1146/annurev.ne.08.030185.001313
    1. Hoehn M. M., Yahr M. D. (1967). Parkinsonism: onset, progression and mortality. Neurology 17 427–442. 10.1212/wnl.17.5.427
    1. Hunt D., Stuart S., Nell J., Hausdorff J. M., Galna B., Rochester L., et al. (2018). Do people with Parkinson’s disease look at task relevant stimuli when walking? an exploration of eye movements. Behav. Brain Res. 348 82–89. 10.1016/j.bbr.2018.03.003
    1. Kader M., Ullén S., Iwarsson S., Odin P., Nillsson M. H. (2017). Factors contributing to perceived walking difficulties in people with Parkinson’s disease. J. Parkinsons Dis. 7 397–407. 10.3233/JPD-161034
    1. Lloret S. P., Pages L. N., Damier P., Delval A., Derkinderen P. (2014). Prevalence, determinants, and effect on quality of life of freezing of gait in Parkinson disease. JAMA Neurol. 71 884–890. 10.1001/jamaneurol.2014.753
    1. Lu C., Twedell E., Elbasher R., McCabe M. (2019). Avoiding virtual obstacles during treadmill gait in Parkinson’s disease. Front. Aging Neurosci. 11:76. 10.3389/fnagi.2019.00076
    1. Matar E., Shine J. M., Naismith S. L., Lewis S. J. G. (2013). Using virtual reality to explore the role of conflict resolution and environmental salience in freezing of gait in Parkinson’s disease. Parkinsonism Relat. Disord. 19 937–942. 10.1016/j.parkreldis.2013.06.002
    1. Mazzoni P., Hristova A., Krakauer J. W. (2007). Why don’t we move faster? Parkinson’s disease, movement vigor, and implicit motivation. J. Neurosci. 27 7105–7116. 10.1523/JNEUROSCI.0264-07.2007
    1. Mohammadi F., Bruijn S. M., Vervoort G., Wegen E. E., Kwakkel G., Verschueren S., et al. (2015). Motor switching and motor adaptation deficits contribute to freezing of gait in Parkinson’s disease. Neurorehabil. Neural Repair 29 132–142. 10.1177/1545968314545175
    1. Nieuwboer A., Rochester L., Herman T., Vandenberghe W., Emil G. E., Thomaes T., et al. (2009). Reliability of the new freezing of gait questionnaire: agreement between patients with Parkinson’s disease and their carers. Gait Posture 30 459–463. 10.1016/j.gaitpost.2009.07.108
    1. Nonnekes J., Geurts A. C. H., Oude Nijhuis L. B., Geel K., Snijders A. H., Bloem B. R., et al. (2014). Reduced start react effect and freezing of gait in Parkinson’s disease: two of a kind. J. Neurol. 261 943–950. 10.1007/s00415-014-7304-0
    1. Opara J., Małecki A., Małecka E., Socha T. (2017). Motor assessment in Parkinson‘s disease. Ann. Agric. Environ. Med. 24 411–415. 10.5604/12321966.1232774
    1. Postuma R. B., Berg D., Stern M., Poewe W., Olanow C. W., Oertwl W., et al. (2015). MDS clinical diagnostic criteria for Parkinson’s disease. Mov. Disord. 30 1591–1599. 10.1002/mds.26424
    1. Shine J. M., Moore S. T., Bolitho S. J., Morris T. R., Dilda V., Naismith S. L., et al. (2012). Assessing the utility of freezing of gait questionnaires in Parkinson’s disease. Parkinsonism Relat. Disord. 18 25–29. 10.1016/j.parkreldis.2011.08.002
    1. Snijders A. H., Weerdesteyn V., Hagen Y. J., Duysens J., Giladi N., Bloem B. R. (2010). Obstacle avoidance to elicit freezing of gait during treadmill walking. Mov. Disord. 25 57–63. 10.1002/mds.22894
    1. Spildooren J., Vercruysse S., Heremans E., Galna B., Vandenbossche J., Desloovere K., et al. (2013). Head-pelvis coupling is increased during turning in patients with Parkinson’s disease and freezing of gait. Mov. Disord. 28 619–625. 10.1002/mds.25285
    1. Timmermans C., Roerdink M., Janssen T. W. J., Beek P. J., Meskers C. G. M. (2019). Automatized, standardized, and patient-tailored progressive walking-adaptability training: a proof-of- concept study. Phys. Ther. 99 882–892. 10.1093/ptj/pzz013
    1. Vervoort G., Nackaerts E., Mohammadi F., Heremans E., Verschueren S., Nieuwboer A., et al. (2013). Which aspects of postural control differentiate between patients with Parkinson’s disease with and without freezing of gait? Parkinsons Dis. 2013 1–8. 10.1155/2013/971480
    1. Wrisley D. M., Marchetti G. F., Kuharsky D. K., Whitney S. L. (2004). Reliability, internal consistency, and validity of data obtained with the functional gait assessment. Phys. Ther. 84 906–918. 10.1093/ptj/84.10.906

Source: PubMed

3
S'abonner