A Data-Driven Investigation on Surface Electromyography Based Clinical Assessment in Chronic Stroke

Fuqiang Ye, Bibo Yang, Chingyi Nam, Yunong Xie, Fei Chen, Xiaoling Hu, Fuqiang Ye, Bibo Yang, Chingyi Nam, Yunong Xie, Fei Chen, Xiaoling Hu

Abstract

Background: Surface electromyography (sEMG) based robot-assisted rehabilitation systems have been adopted for chronic stroke survivors to regain upper limb motor function. However, the evaluation of rehabilitation effects during robot-assisted intervention relies on traditional manual assessments. This study aimed to develop a novel sEMG data-driven model for automated assessment. Method: A data-driven model based on a three-layer backpropagation neural network (BPNN) was constructed to map sEMG data to two widely used clinical scales, i.e., the Fugl-Meyer Assessment (FMA) and the Modified Ashworth Scale (MAS). Twenty-nine stroke participants were recruited in a 20-session sEMG-driven robot-assisted upper limb rehabilitation, which consisted of hand reaching and withdrawing tasks. The sEMG signals from four muscles in the paretic upper limbs, i.e., biceps brachii (BIC), triceps brachii (TRI), flexor digitorum (FD), and extensor digitorum (ED), were recorded before and after the intervention. Meanwhile, the corresponding clinical scales of FMA and MAS were measured manually by a blinded assessor. The sEMG features including Mean Absolute Value (MAV), Zero Crossing (ZC), Slope Sign Change (SSC), Root Mean Square (RMS), and Wavelength (WL) were adopted as the inputs to the data-driven model. The mapped clinical scores from the data-driven model were compared with the manual scores by Pearson correlation. Results: The BPNN, with 15 nodes in the hidden layer and sEMG features, i.e., MAV, ZC, SSC, and RMS, as the inputs to the model, was established to achieve the best mapping performance with significant correlations (r > 0.9, P < 0.001), according to the FMA. Significant correlations were also obtained between the mapped and manual FMA subscores, i.e., FMA-wrist/hand and FMA-shoulder/elbow, before and after the intervention (r > 0.9, P < 0.001). Significant correlations (P < 0.001) between the mapped and manual scores of MASs were achieved, with the correlation coefficients r = 0.91 at the fingers, 0.88 at the wrist, and 0.91 at the elbow after the intervention. Conclusion: An sEMG data-driven BPNN model was successfully developed. It could evaluate upper limb motor functions in chronic stroke and have potential application in automated assessment in post-stroke rehabilitation, once validated with large sample sizes. Clinical Trial Registration: www.ClinicalTrials.gov, identifier: NCT02117089.

Keywords: chronic stroke; clinical assessment; data-driven model; surface electromyography; upper limb.

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 Ye, Yang, Nam, Xie, Chen and Hu.

Figures

Figure 1
Figure 1
The experimental setup and representative sEMG signals. (A) The sEMG-driven robotic hand system. (B) The setup for data acquisition during the vertical bare hand evaluation task. (C) The representative raw sEMG trials for the four muscles of TRI, BIC, ED, and FD in a vertical bare hand evaluation task. Each movement during the evaluation task was manually marked by the experiment operator.
Figure 2
Figure 2
(A) The procedure of sEMG signal processing. (B) The structure of the three-layer backpropagation neural network (BPNN) data-driven model.
Figure 3
Figure 3
Significant correlations yielded by the four-channel sEMG signals, i.e., ED, FD, BIC, and TRI, before the 20-session intervention. Correlations between the mapped scores and manual (A) Fugl–Meyer Assessment shoulder/elbow (FMA-SE) scores and (B) Fugl–Meyer Assessment wrist/hand (FMA-WH) scores.
Figure 4
Figure 4
Significant correlations yielded by the four-channel sEMG, i.e., ED, FD, BIC, and TRI, after the 20-session intervention. Correlations between the mapped scores and manual (A) Fugl–Meyer Assessment shoulder/elbow (FMA-SE) scores and (B) Fugl–Meyer Assessment wrist/hand (FMA-WH) scores.
Figure 5
Figure 5
Significant correlations yielded by the two-channel sEMG signals after the 20-session intervention. Correlation between the mapped scores and manual (A) Fugl–Meyer Assessment shoulder/elbow (FMA-SE) scores, from muscles pair of BIC and TRI, (B) Fugl–Meyer Assessment wrist/hand (FMA-WH) scores, from muscle pair of ED and FD.
Figure 6
Figure 6
Correlations yielded by the mismatched testing condition with the four-channel sEMG signals, i.e., ED, FD, BIC, and TRI. Correlation between the mapped scores and manual (A) Fugl–Meyer Assessment shoulder/elbow (FMA-SE) scores and (B) Fugl–Meyer Assessment wrist/hand (FMA-WH) scores.
Figure 7
Figure 7
Significant correlations between the mapped scores and MASs scales yielded by the bandpass filtered (10–200 Hz) four-channel sEMG signals, i.e., ED, FD, BIC, and TRI. The correlations between the mapped scores and MASs (A) at elbow for the pre-intervention dataset, (B) at elbow for the post-intervention dataset, (C) at wrist for the pre-intervention dataset, (D) at wrist for the post-intervention dataset, (E) at fingers for the pre-intervention dataset, and (F) at fingers for the post-intervention dataset.
Figure 8
Figure 8
The differences of sEMG parameters between the pre- and post-intervention sessions. The x-axis indicates the target muscles (BIC and FD) and muscle pairs (FD-BIC, FD-TRI, and BIC-TRI). The y-axis indicates the corresponding CI of the muscle pairs and the normalized sEMG activation level at the target muscles. The significant differences are indicated as * for P ≤ 0.05, ** for P ≤ 0.01, and ***for P ≤ 0.001, using the paired t-test.
Figure 9
Figure 9
The differences of clinical scales between the pre- and post-intervention sessions. (A) Sub-FMA scores, (B) MASs. The significant differences are indicated as * for P ≤ 0.05, ** for P ≤ 0.01, and ***for P ≤ 0.001, using the paired t-test for the FMA and the Wilcoxon test for the MAS.

References

    1. Aisen M., Sevilla D., Gibson G., Kutt H., Blau A., Edelstein L., et al. . (1995). 3, 4-diaminopyridine as a treatment for amyotrophic lateral sclerosis. J. Neurol. Sci. 129, 21–24. 10.1016/0022-510X(94)00225-D
    1. Ashworth B. (1964). preliminary trial of carisoprodol in multiple sclerosis. Practitioner 192, 540–542.
    1. Atzori M., Müller H. (2019). Fast signal feature extraction using parallel time windows. Front. Neurorobotics 13:74. 10.3389/fnbot.2019.00074
    1. Aung Y. M., Al-Jumaily A. (2013). Estimation of upper limb joint angle using surface EMG signal. Int. J. Adv. Robot. Syst. 10:369. 10.5772/56717
    1. Bakhti K. K. A., Laffont I., Muthalib M., Froger J., Mottet D. (2018). Kinect-based assessment of proximal arm non-use after a stroke. J. Neuroengineering Rehabil. 15:104. 10.1186/s12984-018-0451-2
    1. Basteris A., Nijenhuis S. M., Stienen A. H., Buurke J. H., Prange G. B., Amirabdollahian F. (2014). Training modalities in robot-mediated upper limb rehabilitation in stroke: a framework for classification based on a systematic review. J. Neuroengineering Rehabil. 11:111. 10.1186/1743-0003-11-111
    1. Boger Z., Guterman H. (1997). Knowledge extraction from artificial neural network models, in IEEE International Conference on Systems, Man, and Cybernetics. Computational Cybernetics and Simulation: IEEE; (Orlando, FL: ), 3030–3035. 10.1109/ICSMC.1997.633051
    1. Brewer M. B., Crano W. D. (2000). Research design and issues of validity, Handbook of Research Methods in Social and Personality Psychology, eds Reis H. T., Judd C. M. (Cambridge: Cambridge University Press; ). 3–16.
    1. Burden F., Winkler D. (2008). Bayesian Regularization of Neural Networks. Artificial Neural Networks. 23–42. 10.1007/978-1-60327-101-1_3
    1. Campanini I., Disselhorst-Klug C., Rymer W. Z., Merletti R. (2020). Surface EMG in clinical assessment and neurorehabilitation: barriers limiting its use. Front. Neurol. 11:934. 10.3389/fneur.2020.00934
    1. Coote S., Murphy B., Harwin W., Stokes E. (2008). The effect of the GENTLE/s robot-mediated therapy system on arm function after stroke. Clin. Rehabil. 22, 395–405. 10.1177/0269215507085060
    1. De Villiers J., Barnard E. (1993). Backpropagation neural nets with one and two hidden layers. IEEE Trans. Neural Netw. 4, 136–141. 10.1109/72.182704
    1. Dobbin K. K., Simon R. M. (2011). Optimally splitting cases for training and testing high dimensional classifiers. BMC Med. Genomics 4:31. 10.1186/1755-8794-4-31
    1. Dobkin B. H. (2005). Rehabilitation after stroke. N. Engl. J. Med. 352, 1677–1684. 10.1056/NEJMcp043511
    1. Dromerick A. W. (2002). Clinical features of spasticity and principles of treatment, in Clinical Evaluation and Management of Spasticity, eds Gelber D. A., Jeffery D. R. (Berlin: Springer; ). 13–26. 10.1007/978-1-59259-092-6_2
    1. Evans J. D. (1996). Straightforward Statistics for the Behavioral Sciences. Pacific Grove, Thomson Brooks/Cole Publishing Co.
    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. Freedman D. A. (2009). Statistical Models: Theory and Practice. Cambridge: Cambridge University Press. 10.1017/CBO9780511815867
    1. Fugl-Meyer A. R., Jääskö L., Leyman I., Olsson S., Steglind S. (1975). The post-stroke hemiplegic patient. 1. a method for evaluation of physical performance. Scand. J. Rehabil. Med. 7:13.
    1. Harris J. E., Eng J. J. (2010). Strength training improves upper-limb function in individuals with stroke: a meta-analysis. Stroke 41, 136–140. 10.1161/STROKEAHA.109.567438
    1. Hecht-Nielsen R. (1992). Theory of the backpropagation neural network, in Neural Networks for Perception, ed Wechsler H. (Washington, DC: Elsevier; ), 65–93. 10.1016/B978-0-12-741252-8.50010-8
    1. Hermens H. J., Freriks B., Merletti R., Stegeman D., Blok J., Rau G., et al. . (1999). European recommendations for surface electromyography. Roessingh Res. Dev. 8, 13–54.
    1. Hof A. L., Van Den Berg J. (1981). EMG to force processing I: an electrical analogue of the hill muscle model. J. Biomech. 14, 747–758. 10.1016/0021-9290(81)90031-2
    1. Hu X., Tong K., Li R., Xue J., Ho S., Chen P. (2012). The effects of electromechanical wrist robot assistive system with neuromuscular electrical stimulation for stroke rehabilitation. J. Electromyogr. Kinesiol. 22, 431–439. 10.1016/j.jelekin.2011.12.010
    1. Hu X., Tong K., Song R., Zheng X., Leung W. (2009b). A comparison between electromyography-driven robot and passive motion device on wrist rehabilitation for chronic stroke. Neurorehabil. Neural Repair 23, 837–846. 10.1177/1545968309338191
    1. Hu X., Tong K., Song R., Zheng X., Lui K., Leung W., et al. . (2009a). Quantitative evaluation of motor functional recovery process in chronic stroke patients during robot-assisted wrist training. J. Electromyogr. Kinesiol. 19, 639–650. 10.1016/j.jelekin.2008.04.002
    1. Hu X., Tong K., Wei X., Rong W., Susanto E., Ho S. (2013). The effects of post-stroke upper-limb training with an electromyography (EMG)-driven hand robot. J. Electromyogr. Kinesiol. 23, 1065–1074. 10.1016/j.jelekin.2013.07.007
    1. Huang Y., Nam C., Li W., Rong W., Xie Y., Liu Y., et al. . (2020). A comparison of the rehabilitation effectiveness of neuromuscular electrical stimulation robotic hand training and pure robotic hand training after stroke: a randomized controlled trial. Biomed. Signal Process. Control 56:101723. 10.1016/j.bspc.2019.101723
    1. Hudgins B., Parker P., Scott R. N. (1993). A new strategy for multifunction myoelectric control. IEEE Trans. Biomed. Eng. 40, 82–94. 10.1109/10.204774
    1. Karsoliya S. (2012). Approximating number of hidden layer neurons in multiple hidden layer BPNN architecture. Int. J. Eng. Trends Technol. 3, 714–717. Available online at:
    1. Kim M.-S., Joo M. C., Sohn M. K., Lee J., Kim D. Y., Lee S.-G., et al. . (2020). Development and validation of a prediction model for home discharge in patients with moderate stroke: the Korean stroke cohort for functioning and rehabilitation study. Top. Stroke Rehabil. 27, 453–461. 10.1080/10749357.2019.1711338
    1. Krebs H. A., Volpe B. (2013). Rehabilitation robotics, in Handbook of Clinical Neurology, eds Barnes M. P., Good D. C. (Amsterdam: Elsevier; ), 283–294.
    1. Lambercy O., Dovat L., Yun H., Wee S. K., Kuah C. W., Chua K. S., et al. . (2011). Effects of a robot-assisted training of grasp and pronation/supination in chronic stroke: a pilot study. J. Neuroengineering Rehabil. 8:63. 10.1186/1743-0003-8-63
    1. Langhorne P., Bernhardt J., Kwakkel G. (2011). Stroke rehabilitation. Lancet 377, 1693–1702. 10.1016/S0140-6736(11)60325-5
    1. Lecun Y., Touresky D., Hinton G., Sejnowski T. (1998). A theoretical framework for back-propagation, in Proceedings of the 1988 Connectionist Models Summer School (Pittsburg, PA: ), 21–28.
    1. Levin M. F., Kleim J. A., Wolf S. L. (2009). What do motor “recovery” and “compensation” mean in patients following stroke? Neurorehabil. Neural Repair 23, 313–319. 10.1177/1545968308328727
    1. Li Q., Huang Y. (2010). An auditory-based feature extraction algorithm for robust speaker identification under mismatched conditions. IEEE Trans. Audio Speech Lang. Process. 19, 1791–1801. 10.1109/TASL.2010.2101594
    1. Li S., Kamper D. G., Rymer W. Z. (2006). Effects of changing wrist positions on finger flexor hypertonia in stroke survivors. Muscle Nerve 33, 183–190. 10.1002/mus.20453
    1. Li X., Liu J., Li S., Wang Y.-C., Zhou P. (2014). Examination of hand muscle activation and motor unit indices derived from surface EMG in chronic stroke. IEEE Trans. Biomed. Eng. 61, 2891–2898. 10.1109/TBME.2014.2333034
    1. Lyle R. C. (1981). A performance test for assessment of upper limb function in physical rehabilitation treatment and research. Int. J. Rehabil. Res. 4, 483–492. 10.1097/00004356-198112000-00001
    1. Merletti R., Campanini I., Rymer W. Z., Disselhorst-Klug C. (2021). Surface Electromyography: barriers limiting widespread use of sEMG in clinical assessment and neurorehabilitation. Front. Neurol. 12:642257. 10.3389/fneur.2021.642257
    1. Mitchell T. M. (1997). Artificial neural networks. Mach. Learn. 45, 81–127.
    1. Mostafavi S. M., Mousavi P., Dukelow S. P., Scott S. H. (2015). Robot-based assessment of motor and proprioceptive function identifies biomarkers for prediction of functional independence measures. J. Neuroengineering Rehabil. 12:105. 10.1186/s12984-015-0104-7
    1. Nam C., Rong W., Li W., Xie Y., Hu X., Zheng Y. (2017). The effects of upper-limb training assisted with an electromyography-driven neuromuscular electrical stimulation robotic hand on chronic stroke. Front. Neurol. 8:679. 10.3389/fneur.2017.00679
    1. Nazmi N., Abdul Rahman M. A., Yamamoto S.-I., Ahmad S. A., Zamzuri H., Mazlan S. A. (2016). A review of classification techniques of EMG signals during isotonic and isometric contractions. Sensors 16:1304. 10.3390/s16081304
    1. Norouzi-Gheidari N., Archambault P. S., Fung J. (2012). Effects of robot-assisted therapy on stroke rehabilitation in upper limbs: systematic review and meta-analysis of the literature. J. Rehabil. Res. Dev. 49, 479–496. 10.1682/JRRD.2010.10.0210
    1. Otten P., Kim J., Son S. H. (2015). A framework to automate assessment of upper-limb motor function impairment: a feasibility study. Sensors 15, 20097–20114. 10.3390/s150820097
    1. Page S. J., Levine P., Hade E. (2012). Psychometric properties and administration of the wrist/hand subscales of the Fugl-Meyer Assessment in minimally impaired upper extremity hemiparesis in stroke. Arch. Phys. Med. Rehabil. 93, 2373–2376. 10.1016/j.apmr.2012.06.017
    1. Phinyomark A., Phukpattaranont P., Limsakul C. (2012). Feature reduction and selection for EMG signal classification. Expert Syst. Appl. 39, 7420–7431. 10.1016/j.eswa.2012.01.102
    1. Qian Q., Hu X., Lai Q., Ng S. C., Zheng Y., Poon W. (2017). Early stroke rehabilitation of the upper limb assisted with an electromyography-driven neuromuscular electrical stimulation-robotic arm. Front. Neurol. 8:447. 10.3389/fneur.2017.00447
    1. Qian Q., Nam C., Guo Z., Huang Y., Hu X., Ng S. C., et al. . (2019). Distal versus proximal-an investigation on different supportive strategies by robots for upper limb rehabilitation after stroke: a randomized controlled trial. J. Neuroengineering Rehabil. 16, 64. 10.1186/s12984-019-0537-5
    1. Ramesh V., Baskaran P., Krishnamoorthy A., Damodaran D., Sadasivam P. (2019). Back propagation neural network based big data analytics for a stock market challenge. Commun. Stat. Theory Methods 48, 3622–3642. 10.1080/03610926.2018.1478103
    1. Sahrmann S. A., Norton B. J. (1977). The relationship of voluntary movement of spasticity in the upper motor neuron syndrome. Ann. Neurol. 2, 460–465. 10.1002/ana.410020604
    1. Scrutinio D., Ricciardi C., Donisi L., Losavio E., Battista P., Guida P., et al. . (2020). Machine learning to predict mortality after rehabilitation among patients with severe stroke. Sci. Rep. 10, 1–10. 10.1038/s41598-020-77243-3
    1. Sheela K. G., Deepa S. N. (2013). Review on methods to fix number of hidden neurons in neural networks. Math. Probl. Eng. 2013:425740. 10.1155/2013/425740
    1. Simbaña E. D. O., Baeza P. S.-H., Huete A. J., Balaguer C. (2019). Review of automated systems for upper limbs functional assessment in neurorehabilitation. IEEE Access 7, 32352–32367. 10.1109/ACCESS.2019.2901814
    1. Steyerberg E. W., Harrell Jr F. E., Borsboom G. J., Eijkemans M., Vergouwe Y., Habbema J. D. F. (2001). Internal validation of predictive models: efficiency of some procedures for logistic regression analysis. J. Clin. Epidemiol. 54, 774–781. 10.1016/S0895-4356(01)00341-9
    1. Steyerberg E. W., Harrell F. E., Jr. (2016). Prediction models need appropriate internal, internal-external, and external validation. J. Clin. Epidemiol. 69:245. 10.1016/j.jclinepi.2015.04.005
    1. Sun R., Song R., Tong K.-Y. (2013). Complexity analysis of EMG signals for patients after stroke during robot-aided rehabilitation training using fuzzy approximate entropy. IEEE Trans. Neural Syst. Rehabil. Eng. 22, 1013–1019. 10.1109/TNSRE.2013.2290017
    1. Timmermans A. A., Lemmens R. J., Monfrance M., Geers R. P., Bakx W., Smeets R. J., et al. . (2014). Effects of task-oriented robot training on arm function, activity, and quality of life in chronic stroke patients: a randomized controlled trial. J. Neuroengineering Rehabil. 11:45. 10.1186/1743-0003-11-45
    1. Tsai A.-C., Hsieh T.-H., Luh J.-J., Lin T.-T. (2014). A comparison of upper-limb motion pattern recognition using EMG signals during dynamic and isometric muscle contractions. Biomed. Signal Process. Control. 11, 17–26. 10.1016/j.bspc.2014.02.005
    1. Tu J. V. (1996). Advantages and disadvantages of using artificial neural networks versus logistic regression for predicting medical outcomes. J. Clin. Epidemiol. 49, 1225–1231. 10.1016/S0895-4356(96)00002-9
    1. Uyanik G. K., Güler N. (2013). A study on multiple linear regression analysis. Procedia Soc. Behav. Sci. 106, 234–240. 10.1016/j.sbspro.2013.12.027
    1. Van Boxtel A. (2001). Optimal signal bandwidth for the recording of surface EMG activity of facial, jaw, oral, and neck muscles. Psychophysiology 38, 22–34. 10.1111/1469-8986.3810022
    1. Volpe B. T., Ferraro M., Lynch D., Christos P., Krol J., Trudell C., et al. . (2005). Robotics and other devices in the treatment of patients recovering from stroke. Curr. Neurol. Neurosci.Rep. 5, 465–470. 10.1007/s11910-005-0035-y
    1. Wang C., Peng L., Hou Z.-G., Li J., Zhang T., Zhao J. (2020). Quantitative assessment of upper-limb motor function for post-stroke rehabilitation based on motor synergy analysis and multi-modality fusion. IEEE Trans. Neural Syst. Rehabil. Eng. 28, 943–952. 10.1109/TNSRE.2020.2978273
    1. Wang K. L., Burns M., Xu D., Hu W., Fan S. Y., Han C. L., et al. . (2020). Electromyography biomarkers for quantifying the intraoperative efficacy of deep brain stimulation in parkinson's patients with resting tremor. Front. Neurol. 11:142. 10.3389/fneur.2020.00142
    1. Wei X. J., Tong K. Y., Hu X. L. (2011). The responsiveness and correlation between Fugl-Meyer Assessment, motor status scale, and the action research arm test in chronic stroke with upper-extremity rehabilitation robotic training. Int. J. Rehabil. Res. 34, 349–356. 10.1097/MRR.0b013e32834d330a
    1. Woo J., Chan S. Y., Sum M. W. C., Wong E., Chui Y. P. M. (2008). In patient stroke rehabilitation efficiency: influence of organization of service delivery and staff numbers. BMC Health Serv. Res. 8:86. 10.1186/1472-6963-8-86
    1. Xu L., Chen X., Cao S., Zhang X., Chen X. (2018). Feasibility study of advanced neural networks applied to sEMG-based force estimation. Sensors 18:3226. 10.3390/s18103226
    1. Xu Y., Du J., Dai L.-R., Lee C.-H. (2013). An experimental study on speech enhancement based on deep neural networks. IEEE Signal Process. Lett. 21, 65–68. 10.1109/LSP.2013.2291240
    1. Yang C., Xi X., Chen S., Miran S. M., Hua X., Luo Z. (2019). SEMG-based multifeatures and predictive model for knee-joint-angle estimation. AIP Adv. 9:095042. 10.1063/1.5120470
    1. Yang Z., Chen Y. (2016). Surface EMG-based sketching recognition using two analysis windows and gene expression programming. Front. Neurosci. 10:445. 10.3389/fnins.2016.00445
    1. Yates R. D., Goodman D. J. (1999). Probability and Stochastic Processes. Hoboken, NJ: John Willey & Sons.
    1. Yu L., Xiong D., Guo L., Wang J. (2016). A remote quantitative Fugl-Meyer Assessment framework for stroke patients based on wearable sensor networks. Comput. Methods Programs Biomed. 128, 100–110. 10.1016/j.cmpb.2016.02.012
    1. Yu S., Chen Y., Cai Q., Ma K., Zheng H., Xie L. (2020). A novel quantitative spasticity evaluation method based on surface electromyogram signals and adaptive neuro fuzzy inference system. Front. Neurosci. 14:462. 10.3389/fnins.2020.00462
    1. Zhang X., Tang X., Zhu X., Gao X., Chen X., Chen X. (2019). A regression-based framework for quantitative assessment of muscle spasticity using combined EMG and inertial data from wearable sensors. Front. Neurosci. 13:398. 10.3389/fnins.2019.00398

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