Muscle Electrical Impedance Properties and Activation Alteration After Functional Electrical Stimulation-Assisted Cycling Training for Chronic Stroke Survivors: A Longitudinal Pilot Study

Abstract

Electrical impedance myography (EIM) is a sensitive assessment for neuromuscular diseases to detect muscle inherent properties, whereas surface electromyography (sEMG) is a common technique for monitoring muscle activation. However, the application of EIM in detecting training effects on stroke survivors is relatively few. This study aimed to evaluate the muscle inherent properties and muscle activation alteration after functional electrical stimulation (FES)-assisted cycling training to chronic stroke survivors. Fifteen people with chronic stroke were recruited for 20 sessions of FES-assisted cycling training (40 min/session, 3-5 sessions/week). The periodically stimulated and assessed muscle groups were quadriceps (QC), tibialis anterior (TA), hamstrings (HS), and medial head of gastrocnemius (MG) on the paretic lower extremity. EIM parameters [resistance (R), reactance (X), phase angle (θ), and anisotropy ratio (AR)], clinical scales (Fugl-Meyer Lower Extremity (FMA-LE), Berg Balance Scale (BBS), and 6-min walking test (6MWT)] and sEMG parameters [including root-mean square (RMS) and co-contraction index (CI) value] were collected and computed before and after the training. Linear correlation analysis was conducted between EIM and clinical scales as well as between sEMG and clinical scales. The results showed that motor function of the lower extremity, balance, and walking performance of subjects improved after the training. After training, θ value of TA (P = 0.014) and MG (P = 0.017) significantly increased, and AR of X (P = 0.004) value and AR of θ value (P = 0.041) significantly increased on TA. The RMS value of TA decreased (P = 0.022) and a significant reduction of CI was revealed on TA/MG muscle pair (P < 0.001). Significant correlation was found between EIM and clinical assessments (AR of X value of TA and FMA-LE: r = 0.54, P = 0.046; X value of TA and BBS score: 0.628, P = 0.016), and between sEMG and clinical scores (RMS of TA and BBS score: r = -0.582, P = 0.029). This study demonstrated that FES-assisted cycling training improved lower limb function by developing coordinated muscle activation and facilitating an orderly myofiber arrangement. The current study also indicated that EIM can jointly evaluate lower extremity function alteration with sEMG after rehabilitation training. Clinical Trail Registration: The study was registered on the Clinical Trial Registry (trial registration number: NCT03208439, https://clinicaltrials.gov/ct2/show/NCT03208439).

Keywords: cycling; electrical impedance; electromyography (EMG); functional electrical stimulation (FES); stroke.

Figure 1

(A) The setup of FES-assisted cycling training system. The pedaling angle was monitored by a goniometer. (B) Using quadriceps as an example for sEMG electrodes placement. (C) Using quadriceps as an example for EIM electrodes placement. The outer two electrodes (the red and black one) were current electrodes, inner two electrodes (the yellow and blue one) were voltage electrodes. Each test lasted for few seconds and three tests were conducted repeatedly at each direction of the arrangement.

Figure 2

FES stimulation ranges generated from healthy subjects. (A) Mean sEMG envelop of three normal subjects: HS, dark blue; QC, dark green; GL, black; TA, yellow. The red dotted lines are the muscle activation thresholds. The y-axis is the contraction level in the range of 0 to 100% normalized by MVC. (B) FES stimulation pattern within one revolution: four averaged signals mapping periods of stimulation during cycling. HS, hamstrings; QC, quadriceps; MG, medial head of gastrocnemius; TA, tibialis anterior.

Figure 3

EIM parameters alteration after training. For comparison between paretic and non-paretic muscles, there is a significant reduction of θ and X value in paretic TA and MG. After training, the paretic TA and MG both presented significant increase of θ value. TA, tibialis anterior; MG, medial head of gastrocnemius; X, reactance; θ, phase angle. ^*P < 0.05.

Figure 4

Anisotropy Ratio parameter comparison. For comparison between paretic and non-paretic muscles, significantly lower AR of θ value was shown in TA, significantly lower AR of X value was shown in TA and MG. After training, only TA presented significant increase on the AR of θ and AR of X values. AR, anisotropy ratio; X, reactance; θ, phase angle; TA, tibialis anterior; MG, Medial head of gastrocnemius. ^*P < 0.05.

Figure 5

Comparison of the paretic muscles using sEMG parameters. After training, RMS of TA significantly decreased, CI of TA/MG muscle pair significantly decreased. sEMG, surface electromyography; TA, tibialis anterior; MG, medial head of gastrocnemius; CI, co-contraction index; X, reactance; θ, phase angle. ^*P < 0.05.

Figure 6

Muscle activation alteration of TA and MG before and after training in one subject (Subject No 12). The sEMG-enveloped signal during the middle three revolutions of cycling is demonstrated. X-axis represents the cycling angles of the pedals. The zero degree of the pedal was set so that the two pedals were in the same line which was vertical to the ground. Yellow curve: sEMG envelope of MG, Blue curve: sEMG envelope of TA. After training, the activation of both two muscle pairs decreased, and MG muscle presented a more independent and rhythmic activation pattern (CI value of TA and MR muscle pair: pretraining: 0.168, posttraining: 0.139). TA, tibialis anterior; sEMG, surface electromyography; MG, medial head of Gastrocnemius.

Figure 7

(A) Clinical score comparisons. (B) Correlation between FMAac and AR of X value for TA. (C) Correlation between FMAac and X value of TA. (D) Correlation between BBS and RMS value of TA. AR, anisotropy ratio; RMS, root mean square; TA, tibialis anterior; FMA-LE, Fugl-Meyer assessment of lower extremity; FMAac, Fugl-Meyer assessment of ankle joint and coordination segments; FMAkc, Fugl-Meyer assessment of knee joint and coordination segments; BBS, Berg Balance Scale; 6MWT, 6-minute Walking Test. ^*P < 0.05.