EEG-controlled functional electrical stimulation rehabilitation for chronic stroke: system design and clinical application
Long Chen1,2, Bin Gu1, Zhongpeng Wang1, Lei Zhang2, Minpeng Xu1, Shuang Liu2, Feng He1,2, Dong Ming1,2()
1. Neural Engineering & Rehabilitation Laboratory, Department of Biomedical Engineering, College of Precision Instruments and Optoelectronics Engineering, Tianjin University, Tianjin 300072, China 2. Academy of Medical Engineering and Translational Medicine, Tianjin University, Tianjin 300072, China
Stroke is one of the most serious diseases that threaten human life and health. It is a major cause of death and disability in the clinic. New strategies for motor rehabilitation after stroke are undergoing exploration. We aimed to develop a novel artificial neural rehabilitation system, which integrates brain--computer interface (BCI) and functional electrical stimulation (FES) technologies, for limb motor function recovery after stroke. We conducted clinical trials (including controlled trials) in 32 patients with chronic stroke. Patients were randomly divided into the BCI-FES group and the neuromuscular electrical stimulation (NMES) group. The changes in outcome measures during intervention were compared between groups, and the trends of ERD values based on EEG were analyzed for BCI-FES group. Results showed that the increase in Fugl Meyer Assessment of the Upper Extremity (FMA-UE) and Kendall Manual Muscle Testing (Kendall MMT) scores of the BCI-FES group was significantly higher than that in the sham group, which indicated the practicality and superiority of the BCI-FES system in clinical practice. The change in the laterality coefficient (LC) values based on μ-ERD (ΔLCm-ERD) had high significant positive correlation with the change in FMA-UE(r= 0.6093, P=0.012), which provides theoretical basis for exploring novel objective evaluation methods.
EJ Benjamin, P Muntner, A Alonso, MS Bittencourt, CW Callaway, AP Carson, AM Chamberlain, AR Chang, S Cheng, SR Das, FN Delling, L Djousse, MSV Elkind, JF Ferguson, M Fornage, LC Jordan, SS Khan, BM Kissela, KL Knutson, TW Kwan, DT Lackland, TT Lewis, JH Lichtman, CT Longenecker, MS Loop, PL Lutsey, SS Martin, K Matsushita, AE Moran, ME Mussolino, M O’Flaherty, A Pandey, AM Perak, WD Rosamond, GA Roth, UKA Sampson, GM Satou, EB Schroeder, SH Shah, NL Spartano, A Stokes, DL Tirschwell, CW Tsao, MP Turakhia, LB VanWagner, JT Wilkins, SS Wong, SS Virani. Heart disease and stroke statistics—2019 update: a report from the American Heart Association. Circulation 2019; 139(10): e56–e528 https://doi.org/10.1161/CIR.0000000000000659
pmid: 30700139
2
Q Yang, X Tong, L Schieb, A Vaughan, C Gillespie, JL Wiltz, SC King, E Odom, R Merritt, Y Hong, MG George. Vital signs: recent trends in stroke death rates—United States, 2000–2015. MMWR Morb Mortal Wkly Rep 2017; 66(35): 933–939 https://doi.org/10.15585/mmwr.mm6635e1
pmid: 28880858
3
EJ Benjamin, MJ Blaha, SE Chiuve, M Cushman, SR Das, R Deo, SD de Ferranti, J Floyd, M Fornage, C Gillespie, CR Isasi, MC Jiménez, LC Jordan, SE Judd, D Lackland, JH Lichtman, L Lisabeth, S Liu, CT Longenecker, RH Mackey, K Matsushita, D Mozaffarian, ME Mussolino, K Nasir, RW Neumar, L Palaniappan, DK Pandey, RR Thiagarajan, MJ Reeves, M Ritchey, CJ Rodriguez, GA Roth, WD Rosamond, C Sasson, A Towfighi, CW Tsao, MB Turner, SS Virani, JH Voeks, JZ Willey, JT Wilkins, JH Wu, HM Alger, SS Wong, P Muntner. Heart disease and stroke statistics—2017 update: a report from the American Heart Association. Circulation 2017; 135(10): e146–e603 https://doi.org/10.1161/CIR.0000000000000485
pmid: 28122885
4
RJ Nudo, BM Wise, F SiFuentes, GW Milliken. Neural substrates for the effects of rehabilitative training on motor recovery after ischemic infarct. Science 1996; 272(5269): 1791–1794 https://doi.org/10.1126/science.272.5269.1791
pmid: 8650578
5
E Taub, G Uswatte, T Elbert. New treatments in neurorehabili-tation founded on basic research. Nat Rev Neurosci 2002; 3(3): 228–236 https://doi.org/10.1038/nrn754
pmid: 11994754
ME Nelson, WJ Rejeski, SN Blair, PW Duncan, JO Judge, AC King, CA Macera, C Castaneda-Sceppa. Physical activity and public health in older adults: recommendation from the American College of Sports Medicine and the American Heart Association. Med Sci Sports Exerc 2007; 39(8): 1435–1445 https://doi.org/10.1249/mss.0b013e3180616aa2
pmid: 17762378
8
N Takeshima, NL Rogers, ME Rogers, MM Islam, D Koizumi, S Lee. Functional fitness gain varies in older adults depending on exercise mode. Med Sci Sports Exerc 2007; 39(11): 2036–2043 https://doi.org/10.1249/mss.0b013e31814844b7
pmid: 17986913
9
W Yu, C An, H Kang. Effects of resistance exercise using Thera-band on balance of elderly adults: a randomized controlled trial. J Phys Ther Sci 2013; 25(11): 1471–1473 https://doi.org/10.1589/jpts.25.1471
pmid: 24396213
10
T Takahashi, D Koizumi, MM Islam, M Watanabe, M Narita, N Takeshima. Effects of passive exercise machine-based training on day care service user frail elderly. Rigakuryoho Kagaku 2011; 26: 209–213 https://doi.org/10.1589/rika.26.209
11
T Takahashi, MM Islam, D Koizumi, M Narita, N Takeshima. The effects of low intensity exercises performed by community-dwelling chronic stroke patients on passive movement-type machines. Rigakuryoho Kagaku 2012; 27(5): 545–551 https://doi.org/10.1589/rika.27.545
MH Granat, AC Ferguson, BJ Andrews, M Delargy. The role of functional electrical stimulation in the rehabilitation of patients with incomplete spinal cord injury—observed benefits during gait studies. Paraplegia 1993; 31(4): 207–215 https://doi.org/10.1038/sc.1993.39
pmid: 8493035
14
EM Wassermann. Changes in motor representation with recovery of motor function after stroke: combined electrophysiological and imaging studies. EEG Clin Neurophysiol 1995; 97(4): S26 https://doi.org/10.1016/0924-980X(95)92506-H
15
LR Hochberg, MD Serruya, GM Friehs, JA Mukand, M Saleh, AH Caplan, A Branner, D Chen, RD Penn, JP Donoghue. Neuronal ensemble control of prosthetic devices by a human with tetraplegia. Nature 2006; 442(7099): 164–171 https://doi.org/10.1038/nature04970
pmid: 16838014
16
S Silvoni, A Ramos-Murguialday, M Cavinato, C Volpato, G Cisotto, A Turolla, F Piccione, N Birbaumer. Brain-computer interface in stroke: a review of progress. Clin EEG Neurosci 2011; 42(4): 245–252 https://doi.org/10.1177/155005941104200410
pmid: 22208122
17
MA Cervera, SR Soekadar, J Ushiba, JDR Millán, M Liu, N Birbaumer, G Garipelli. Brain-computer interfaces for post-stroke motor rehabilitation: a meta-analysis. Ann Clin Transl Neurol 2018; 5(5): 651–663 https://doi.org/10.1002/acn3.544
pmid: 29761128
18
S Qiu, W Yi, J Xu, H Qi, J Du, C Wang, F He, D Ming. Event-related β EEG changes during active, passive movement and functional electrical stimulation of the lower limb. IEEE Trans Neural Syst Rehabil Eng 2016; 24(2): 283–290 https://doi.org/10.1109/TNSRE.2015.2476481
pmid: 26441422
19
BM Young, J Williams, V Prabhakaran. BCI-FES: could a new rehabilitation device hold fresh promise for stroke patients? Expert Rev Med Devices 2014; 11(6): 537–539 https://doi.org/10.1586/17434440.2014.941811
pmid: 25060658
R Looned, J Webb, ZG Xiao, C Menon. Assisting drinking with an affordable BCI-controlled wearable robot and electrical stimulation: a preliminary investigation. J Neuroeng Rehabil 2014; 11(1): 51 https://doi.org/10.1186/1743-0003-11-51
pmid: 24708603
22
A Biasiucci, R Leeb, I Iturrate, S Perdikis, A Al-Khodairy, T Corbet, A Schnider, T Schmidlin, H Zhang, M Bassolino, D Viceic, P Vuadens, AG Guggisberg, JDR Millán. Brain-actuated functional electrical stimulation elicits lasting arm motor recovery after stroke. Nat Commun 2018; 9(1): 2421 https://doi.org/10.1038/s41467-018-04673-z
pmid: 29925890
23
AH Do, PT Wang, CE King, A Abiri, Z Nenadic. Brain–computer interface controlled functional electrical stimulation system for ankle movement. J Neuroeng Rehabil 2011; 8(1): 49 https://doi.org/10.1186/1743-0003-8-49
pmid: 21867567
24
CM McCrimmon, CE King, PT Wang, SC Cramer, Z Nenadic, AH Do. Brain-controlled functional electrical stimulation therapy for gait rehabilitation after stroke: a safety study. J Neuroeng Rehabil 2015; 12(1): 57 https://doi.org/10.1186/s12984-015-0050-4
pmid: 26162751
25
X Zhang, AM Elnady, BK Randhawa, LA Boyd, C Menon. Combining mental training and physical training with goal-oriented protocols in stroke rehabilitation: a feasibility case study. Front Hum Neurosci 2018; 12: 125 https://doi.org/10.3389/fnhum.2018.00125
pmid: 29666575
26
T Kim, S Kim, B Lee. Effects of action observational training plus brain-computer interface-based functional electrical stimulation on paretic arm motor recovery in patient with stroke: a randomized controlled trial. Occup Ther Int 2016; 23(1): 39–47 https://doi.org/10.1002/oti.1403
pmid: 26301519
27
E Chung, SI Park, YY Jang, BH Lee. Effects of brain–computer interface-based functional electrical stimulation on balance and gait function in patients with stroke: preliminary results. J Phys Ther Sci 2015; 27(2): 513–516 https://doi.org/10.1589/jpts.27.513
pmid: 25729205
28
E Chung, JH Kim, DS Park, BH Lee. Effects of brain-computer interface-based functional electrical stimulation on brain activation in stroke patients: a pilot randomized controlled trial. J Phys Ther Sci 2015; 27(3): 559–562 https://doi.org/10.1589/jpts.27.559
pmid: 25931680
29
YY Jang, TH Kim, BH Lee. Effects of brain–computer interface-controlled functional electrical stimulation training on shoulder subluxation for patients with stroke: a randomized controlled trial. Occup Ther Int 2016; 23(2): 175–185 https://doi.org/10.1002/oti.1422
pmid: 26876690
30
NA Abduallatif, SG Elsherbini, BS Boshra, IA Yassine. Brain–computer interface controlled functional electrical stimulation system for paralyzed arm. 2016 8th Cairo International Biomedical Engineering Conference (CIBEC), Cairo, 2016. 48–51 https://doi.org/10.1109/CIBEC.2016.7836117
31
M Bockbrader, N Annetta, D Friedenberg, M Schwemmer, N Skomrock, S Colachis 4th, M Zhang, C Bouton, A Rezai, G Sharma, WJ Mysiw. Clinically significant gains in skillful grasp coordination by an individual with tetraplegia using an implanted brain–computer interface with forearm transcutaneous muscle stimulation. Arch Phys Med Rehabil 2019; 100(7): 1201–1217 https://doi.org/10.1016/j.apmr.2018.07.445
pmid: 30902630
32
J Likitlersuang, R Koh, X Gong, L Jovanovic, I Bolivar-Tellería, M Myers, J Zariffa, C Márquez-Chin. EEG-controlled functional electrical stimulation therapy with automated grasp selection: a proof-of-concept study. Top Spinal Cord Inj Rehabil 2018; 24(3): 265–274 https://doi.org/10.1310/sci2403-265
pmid: 29997429
33
BC Osuagwu, L Wallace, M Fraser, A Vuckovic. Rehabilitation of hand in subacute tetraplegic patients based on brain computer interface and functional electrical stimulation: a randomised pilot study. J Neural Eng 2016; 13(6): 065002 https://doi.org/10.1088/1741-2560/13/6/065002
pmid: 27739405
34
SC Colachis 4th, MA Bockbrader, M Zhang, DA Friedenberg, NV Annetta, MA Schwemmer, ND Skomrock, WJ Mysiw, AR Rezai, HS Bresler, G Sharma. Dexterous control of seven functional hand movements using cortically-controlled transcutaneous muscle stimulation in a person with tetraplegia. Front Neurosci 2018; 12: 208 https://doi.org/10.3389/fnins.2018.00208
pmid: 29670506
35
G Pfurtscheller, GR Müller, J Pfurtscheller, HJ Gerner, R Rupp. ‘Thought’—control of functional electrical stimulation to restore hand grasp in a patient with tetraplegia. Neurosci Lett 2003; 351(1): 33–36 https://doi.org/10.1016/S0304-3940(03)00947-9
pmid: 14550907
36
H Ramoser, J Müller-Gerking, G Pfurtscheller. Optimal spatial filtering of single trial EEG during imagined hand movement. IEEE Trans Rehabil Eng 2000; 8(4): 441–446 https://doi.org/10.1109/86.895946
pmid: 11204034
37
S Makeig. Auditory event-related dynamics of the EEG spectrum and effects of exposure to tones. Electroencephalogr Clin Neurophysiol 1993; 86(4): 283–293 https://doi.org/10.1016/0013-4694(93)90110-H
pmid: 7682932
38
G Lioi, M Fleury, S Butet, A Lécuyer, C Barillot, I Bonan. Bimodal EEG-fMRI neurofeedback for stroke rehabilitation: a case report. Ann Phys Rehabil Med 2018; 61: e482–e483 https://doi.org/10.1016/j.rehab.2018.05.1127
39
T Wang, D Mantini, CR Gillebert. The potential of real-time fMRI neurofeedback for stroke rehabilitation: a systematic review. Cortex 2018; 107: 148–165 https://doi.org/10.1016/j.cortex.2017.09.006
pmid: 28992948
40
L Perronnet, A Lécuyer, M Mano, E Bannier, F Lotte, M Clerc, C Barillot. Unimodal versus bimodal EEG-fMRI neurofeedback of a motor imagery task. Front Hum Neurosci 2017; 11: 193 https://doi.org/10.3389/fnhum.2017.00193
pmid: 28473762
41
AA Savelov, MB Shtark, ME Mel’nikov, LI Kozlova, DD Bezmaternykh, EG Verevkin, ED Petrovskii, MA Pokrovskii, GM Tsirkin, PD Rudych. Dynamics of fMRI and EEG parameters in a stroke patient assessed during a neurofeedback course focused on Brodmann Area 4 (M1). Bull Exp Biol Med 2019; 166(3): 394–398 https://doi.org/10.1007/s10517-019-04358-7
pmid: 30627901
42
M Bönstrup, R Schulz, B Cheng, J Feldheim, G Thomalla, F Hummel, C Gerloff. P108. The effect of task effort on recovery-related brain activity following motor stroke assessed with fMRI and EEG. Clin Neurophysiol 2015; 126(8): e102 https://doi.org/10.1016/j.clinph.2015.04.150
A Perry, L Stein, S Bentin. Motor and attentional mechanisms involved in social interaction—evidence from mu and alpha EEG suppression. Neuroimage 2011; 58(3): 895–904 https://doi.org/10.1016/j.neuroimage.2011.06.060
pmid: 21742042
AM Ray, TDC Figueiredo, E López-Larraz, N Birbaumer, A Ramos-Murguialday. Brain oscillatory activity as a biomarker of motor recovery in chronic stroke. Hum Brain Mapp 2020; 41(5): 1296–1308 https://doi.org/10.1002/hbm.24876
pmid: 31778265
48
C Bushnell, JP Bettger, KM Cockroft, SC Cramer, MO Edelen, D Hanley, IL Katzan, S Mattke, DM Nilsen, T Piquado, ER Skidmore, K Wing, G Yenokyan. Chronic stroke outcome measures for motor function intervention trials: expert panel recommendations. Circ Cardiovasc Qual Outcomes 2015; 8(6 Suppl 3): S163–S169 https://doi.org/10.1161/CIRCOUTCOMES.115.002098
pmid: 26515205
49
S Pandian, KN Arya. Stroke-related motor outcome measures: do they quantify the neurophysiological aspects of upper extremity recovery? J Bodyw Mov Ther 2014; 18(3): 412–423 https://doi.org/10.1016/j.jbmt.2013.11.006
pmid: 25042312
50
P Boord, A Barriskill, A Craig, H Nguyen. Brain–computer interface-FES integration: towards a hands-free neuroprosthesis command system. Neuromodulation 2004; 7(4): 267–276 https://doi.org/10.1111/j.1094-7159.2004.04212.x
pmid: 22151336