Effect of electromyographic biofeedback training on motor function of quadriceps femoris in patients with incomplete spinal cord injury: A randomized controlled trial

Abstract

BACKGROUND:

Electromyographic biofeedback (EMG BF) training is an effective method of promoting motor learning and control in neurorehabilitation, but its effect on quadriceps femoris muscle in individuals with spinal cord injury (SCI) is unknown.

OBJECTIVE:

The aim of the study was to investigate the therapeutic effect of EMG BF training on motor function of quadriceps femoris in patients with incomplete SCI.

METHODS:

Thirty-three incomplete paraplegic patients with quadriceps femoris strength ranging grade 1 to grade 3 less than 6 months post-injury were enrolled. Control group (n = 16) received conventional physical therapy to enhance quadriceps femoris strength, while intervention group (n = 17) was treated with conventional physical therapy and EMG BF training. All received treatment once a day for 30 days. Surface electromyograph (sEMG), muscle strength and thigh circumference size were assessed to evaluate motor function of quadriceps femoris. Activities of daily living (ADL) was evaluated by Modified Barthel Index (MBI). All the measures evaluated three times in total.

RESULTS:

Compared to the control group, intervention group significantly improved on sEMG values and strength of quadriceps femoris (P_sEMG < 0.001, P_strength < 0.05). sEMG values of quadriceps femoris increased earlier than strength of quadriceps femoris in intervention group (P_rest = 0.07, P_active = 0.031). There were no statistical differences in thigh circumference size and ADL scores between groups (P_thigh > 0.05, P_ADL = 0.423).

CONCLUSIONS:

EMG BF training appeared to be a useful tool to enhance motor function of quadriceps femoris in patients with incomplete SCI. sEMG could quantify the changes of single muscle myodynamia precisely before visible or touchable changes occur.

Keywords

Spinal cord injury quadriceps femoris electromyographic biofeedback rehabilitation

1 Introduction

Spinal cord injury (SCI) is a neurological condition with motor, sensory, and autonomic dysfunction at and below the level of injury (Dietz & Curt 2006). SCI would have a profound physical, psychological, and socioeconomic impact on the affected person’s life (Wyndaele & Wyndaele 2006). Despite the progress in medical and surgical management, SCI still is a devastating condition and a big challenge to cure. Though spontaneous recovery from SCI is hindered by the limited ability of the mammalian central nervous system (Dietz & Curt 2006), exercise training could be an effective therapy to promote functional recovery for SCI patients (Fu et al., 2016). Motor recovery plays an increasingly important role in modern SCI rehabilitation to reduce activity limitations and participation restrictions. Restoration of motor function is one of the highest priorities in SCI patients (Alam et al., 2016). Compared to the complete SCI conditions, SCI patients with incomplete injury have more potential for recovery (Raineteau & Schwab 2001). Early recovery of muscle strength post incomplete SCI has been identified as a useful predictor of ambulatory capacity (Kim et al., 2004).

Quadriceps femoris, the largest muscle group in the body and the greatest extensor muscle of the knee, would be weaken significantly in individuals with SCI. Functional evaluation and therapy are necessary in the process of SCI rehabilitation. But in most cases, patients usually receive evaluation by manual muscle testing (MMT) that is not helpful for precise assessment. And most of them receive therapy in a passive way rather than participating in the rehabilitation actively, which is not useful for promoting to control body movement with consciousness.

Biofeedback training is an effective method of promoting motor learning and control and is allied to rehabilitation for the recovery from paralysis or for strengthening muscle (Suzuki et al., 2017). The principle of biofeedback is to provide audio or visual feedback of body parameters that a person is usually not aware of (Baumueller et al., 2017). EMG biofeedback is a common modality of biofeedback and has applied to a wide range of diseases such as osteoarthritis (Anwer et al., 2011), post-anterior cruciate ligament reconstruction (Christanell et al., 2012) and juvenile rheumatoid arthritis (Eid et al., 2016), which suggested that EMG biofeedback is more positive in enhancing knee extension and facilitating the recovery of quadriceps when combined with conventional therapeutic modalities.

Likewise, EMG biofeedback is helpful for SCI patients to increase muscle strength and alleviate pain (Holtermann et al., 2010; Jensen et al., 2010). Petrofsky (Holtermann et al., 2010; Jensen et al., 2010) reported that EMG biofeedback increased strength and reduced Trendelenburg gait much more than just therapy alone in incomplete SCI. However, there are only a few intervention based studies on quadriceps femoris muscle in individuals with SCI. Therefore, the purpose of this study was to investigate the effect of EMG biofeedback training on improving motor function of quadriceps femoris in patients with incomplete SCI.

2 Methods

2.1 Patients

Patients were recruited who were aged from 18 to 60 years old, with a confirmed diagnosis of traumatic incomplete SCI (American Spinal Injury Association (ASIA): injury level Thoracic10 - Lumar1, grade B-D), time since injury was less than 6 months, quadriceps femoris strength was from grade 1 to grade 3 and no spasticity in the lower limbs measured by MMT and Modified Ashworth Scale respectively. Patients were excluded if they had other neurological disorders other than SCI, lower limb amputation and fracture, hearing and vision impairment, severe cardiopulmonary disorder, were unable to cooperate. 40 patients were recruited and allocated to either intervention group or control group using a random sequence. Intervention group received EMG BF along with conventional physical therapy, while control group only received conventional physical therapy (see Fig. 1).

Fig. 1

Flow diagram of the study.

The study protocol was approved by the Ethics Committee of China Rehabilitation Research Center (reference number: 2017-014-1), and written informed consent was obtained from each patient prior to the study. The clinical trial was registered in the Chinese Clinical Trial Registry (no. ChiCTR1800018891, http://www.chictr.org.cn).

2.2 Evaluations

sEMG is a bioelectric time series signal obtained from neuromuscular system by electrode stick on the surface of the tested muscle. Studies showed that sEMG is a kind of objective detection technology to evaluate neuromuscular function state accurately, which can be used for quantitative and qualitative analysis of neuromuscular function. Malone et al. and Watanabe et al. approved reliability and validity of sEMG on testing neuromuscular function (Malone et al., 2011; Watanabe & Akima 2011). Mathur et al. believed that the median frequency and amplitude of sEMG on quadriceps had repeatability (Mathur et al., 2005). Fauth et al. (Fauth et al., 2010) found that sEMG is a reliable method to evaluate repeatability on quadriceps femoris and hamstring isometric contraction by their research about the reliability of sEMG evaluation on quadriceps and hamstring activities. So sEMG can be used to evaluate the function of neuromuscular system after SCI.

sEMG analysis mainly includes time-domain analysis and frequency-domain analysis. We used root mean square (RMS), one of time-domain analysis, in the evaluation progress by EMG BF machine. RMS reflects variation in a period of time, it associated with synchronization between motor unit recruitment and exciting rhythms, it can reflect muscle activity state in time dimension (Croce & Miller 2003). RMS is the most reliable parameter in the time-domain analysis, which is often used in quantitative analysis in the field of sEMG with rare illusion and interference (Criswell 2010). Kim believed that RMS amplitude can be acted as a parameter to evaluate muscle strength and muscle tension, the greater value, the greater muscle strength and tension (Kim et al., 2011).

In a quiet room with constant temperature about 25 centigrade, the patient lied on the intervention bed, a pair of surface-adhesive electrodes was positioned on the medial belly of quadriceps femoris (rectus femoris, respectively 10cm and 30cm far from suprapatellaris), a reference electrode was located between the above two surface electrodes.

The patients were asked to (1) rest with both legs relaxing on the bed for 10 seconds to compute the resting level of sEMG values of quadriceps femoris: mean root mean square (RMS); (2) perform classical isometric contraction of quadriceps involves “pressing the back of the knee downward through the bed, and holding the leg in the same position for 10 seconds”. The maximum RMS of quadriceps femoris was counted after the voluntary isometric contraction. Stable values of mean RMS and maximum RMS were calculated after three times of continuous evaluations.

Other evaluations included quadriceps femoris strength evaluation using ASIA Impairment Scale (AIS) (motor function examination); measurement of thigh circumference where testing location was 15 cm far from the upper edge of patella; activities of daily living (ADL) scores to assess the patient’s self-care ability by Modified Barthel Index (MBI) scale. All patients were evaluated three times in total, respectively before the intervention, 15 days and 30 days after starting the intervention.

2.3 Randomization and allocation concealment procedure

A block randomization with random block sizes of 2 or 4 was performed by a specialist who was involved neither in the intervention nor in the assessments. 40 sealed envelopes were labeled with 1–40 according to the consecutively assigned patient numbers. According to random numbers each envelope included the information on group assignment.

2.4 Interventions

2.4.1 EMG BF training

In a quiet room with constant temperature about 25 centigrade, the patients in intervention group lied on the intervention bed, a pair of surface-adhesive electrodes were attached to the belly of the quadriceps femoris muscle (respectively 10 cm and 30 cm far from suprapatellaris). A hard pillow would be put under the knee for those patients who had quadriceps femoris strength equals or greater than grade 3. The patients were asked to extend the knees actively with rhythm according to the computer order “work-rest” (contraction-relax). Meanwhile they must paid attention to the sEMG signals on the display screen and do their best to increase the sEMG signal amplitude at the “work” time. Patients would be relaxed at the “rest” time. About 60 repetitions of “work-rest” circles in the whole training time. The machine would stopped automatically when the training finished. The training time was about 30 minutes. Training once a day for 30 days.

2.4.2 Conventional physical therapy

All patients in the two groups received conventional physical therapies session of 1 hour once a day for 30 days, including regular quadriceps femoris strength training, position transfer, sitting pedaling, balance training, standing training.

2.5 Statistical analysis

The statistical analysis was performed using the Statistical Package for Social Sciences (SPSS) version 20. If the measurement data accorded with normal distribution, differences between intra-group were statistically analyzed using paired t-test, and differences between two groups were calculated using independent sample t-test. Data were reported as means±standard deviation (SD) within the text and table. If the measurement data did not accord with normal distribution, intra-group differences between before and after intervention using non-parametric Wilcoxon signed-rank test, and differences between two groups were examined using independent sample rank test (Mann-Whitney U test). Data were reported as median (25th, 75th Percentiles) within the text and table. A significance level of P < 0.05 was used to identify statistical significance.

3 Results

33 incomplete SCI patients (24 men and 9 women) and 60 pieces of quadriceps femoris muscles in this trail finally. 17 patients (12 men and 5 women) with the age of 36.18±9.08 years and 30 pieces of quadriceps femoris muscles in intervention group and 16 patients (12 men and 4 women) with the age of 36.63±9.34 years and 30 pieces of quadriceps femoris muscles in control group. The two groups were matched for all variables. No statistically significant differences were found in the sample characteristics (see Table 1) or in baseline measures between the two groups (see Table 2).

Table 1
Characteristics of the patients

Intervention (n = 17) Control (n = 16)

Age (mean±SD) 36.18±9.08 36.63±9.34

Male/Female 12/5 12/4

Days post injury (mean±SD) 47.53±33.17 48.38±29.17

ASIA (B/C/D) 10/5/2 9/6/1

Injury level (T/L) 10/7 8/8

	Intervention (n = 17)	Control (n = 16)
Age (mean±SD)	36.18±9.08	36.63±9.34
Male/Female	12/5	12/4
Days post injury (mean±SD)	47.53±33.17	48.38±29.17
ASIA (B/C/D)	10/5/2	9/6/1
Injury level (T/L)	10/7	8/8

ASIA: American Spinal Injury Association; T: Thoracic; L: Lumbar.

Table 2

Outcome measures before and after intervention

	Baseline		Midpoint		Final
	Intervention	Control	Intervention	Control	Intervention	Control
Quadriceps sEMG
μV, median (25th, 75th percentiles) Mean RMS (resting state)	0.78 (0.45, 2.15)	0.50 (0.42, 1.26)	1.89 (0.79, 3.02)^*#	0.76 (0.58, 1.30)^*	2.12 (0.98, 4.56)^*#	0.97 (0.68, 2.11)^*
Maximum RMS (active contraction)	37.49 (12.15, 173.55)	54.38 (10.48, 116.35)	149.45 (51.71, 253.81)^*# #	83.31 (14.99, 132.98)^*	202.46 (78.18, 363.23)^*# #	101.79 (28.22, 199.08)^*
Quadriceps strength
Grade, median (25th, 75th percentiles)	2.00 (1.00, 3.00)	2.00 (1.00, 3.00)	2.00 (2.00, 3.00)^*	2.00 (1.00, 3.00)	2.50 (2.00, 4.00)^*# #	2.00 (1.00, 3.00)^**
Thigh circumference
15cm above the superior border of patella, mean±SD
Left	38.03±3.94	36.97±3.24	38.13±3.98^***# # #	36.97±3.24^***	38.17±4.01^***# # #	36.97±3.24^***
Right	36.77±3.35	37.03±3.23	36.77±3.35^***# # #	37.07±3.28^***	36.77±3.35^***# # #	37.03±3.23^***
ADL scores
Mean±SD	57.06±13.00	57.19±12.78	61.17±14.31^*	59.38±12.63^**	65.59±13.56^*	61.56±11.36^*

Intra-group comparison to baseline, ^*P < 0.01, ^**P < 0.05,^***P > 0.05. Comparison with control group at the same period, ^#P < 0.01, ^# #P < 0.05, ^# # #P > 0.05. RMS: root mean square. *Statistically significant difference between intra-group, ^#Statistically significant difference between inter-group.

Both groups showed significant differences on sEMG values of quadriceps femoris at 15 days, 30 days after intervention respectively (P < 0.01), and the intervention group improved better than the control group at the same evaluation period (P < 0.05) (see Table 2).

Quadriceps femoris strength improved significantly at 15 days and 30 days after intervention in intervention group (P < 0.01), while quadriceps femoris strength in control group improved significantly just at 30 days after intervention (P < 0.05), and the two groups had significant difference at 30 days after intervention (P < 0.05) (see Table 2).

Both groups all had no statistical differences on thigh circumference size before and after intervention (P > 0.05) (see Table 2).

The ADL scores improved significantly in both groups at 15 days and 30 days after intervention (P < 0.05), but with no statistical significance between groups (P > 0.05) (see Table 2).

4 Discussion

The result showed that the sEMG amplitude of quadriceps femoris after training improved significantly than pre-intervention in two groups. This suggested that both training methods are helpful to increase electric activity of quadriceps femoris, which had same result compared to other previous research (De Biase et al., 2011; Govil & Noohu 2013; Kesemenli et al., 2014; Petrofsky 2001).

The CNS can increase the strength of muscle contraction by increasing the number of motor units recruitment. In SCI condition, quadriceps femoris lost part of control from CNS, the numbers of motor units is grossly reduced and are not uniform (Govil & Noohu 2013), the capacity of muscle excitability and contraction decreased, EMG signal amplitude is affected finally. EMG BF could reflect the functional status of neuromuscular system by acquired quadriceps femoris sEMG (RMS) with non-invasive in incomplete SCI patients.

The increased sEMG amplitude is related to the recovery of neural pathways. On one hand, the body has the ability to repair itself which called CNS plasticity. On the other hand, rehabilitation training could promote neural pathways repair by increasing sensory input and information feedback. Animal experiment and clinical research showed that rehabilitation training could improve the excitability of motor nerve in cerebral cortex (Nardone et al., 2013), and promote the reshaping of the spinal cord neurons synaptic (Armadadasilva et al., 2013) and neural functional recovery (Armadadasilva et al., 2013).

Our study showed that there were significant differences in changes of sEMG amplitude on quadriceps femoris after the intervention between groups. It means EMG BF training is a better way to activate and restore electrical signals of quadriceps function than conventional physical therapy.

First of all, EMG BF training is a kind of method with effect of neuromuscular electrical stimulation, which can give muscle tissue a certain passive sensory stimulation, and stimulate sensory conduction and movement activities on the muscle. Previous research showed that neuromuscular electrical stimulation can maintain or restore volume and strength of quadriceps (Durigan et al., 2014). When the quadriceps femoris has a weak contraction that does not reach the target EMG amplitude, EMG BF instrument would promote muscle contraction by acting on external electrical stimulation on the muscle.

Secondly, EMG BF has visual and auditory function, it can provide patients with appropriate feedback and guide patients to take participate in rehabilitation training actively. SCI patients often have hypesthesia or no feeling below the injury level, their ability to perceive stimulation decreased, but EMG BF instrument may be a good solution to this problem. Patients can contract muscle to exceed the baseline or target EMG value based on the amplitude of myoelectric value displayed on the screen directly. In terms of auditory feedback, EMG BF instrument can remind patients to conduct muscle contraction and relaxation rhythmically, avoiding muscle fatigue.

Finally, an effective SCI intervention strategy should be combined a strategy that will enhance spontaneous plasticity of spinal cord with a strategy that will enhance task-dependent plasticity (Hodson-Tole & Wakeling 2009). The activation of the central pattern generator (CPG) and/or extensive recruitment of spinal cord neurons can be facilitated by enabling task-dependent plasticity (Marder & Bucher 2001; Zehr et al., 2007). EMG BF training can stimulate the active training (feedback) based on the passive training (electrical stimulation). It can mobilize the patient’s internal potential well, so it could promote axons regeneration and neural circuit reorganization in spinal cord by task completion. While conventional physical therapy is poorer in the term of active participation and feedback.

Quadriceps femoris strength improved significantly earlier after intervention in intervention group than control group. This suggests that both conventional physical therapy and EMG BF training have an enhanced effect on the strength of SCI patients. However, EMG BF training is better than conventional physical therapy to enhance quadriceps femoris strength. The increase in muscle strength after the application of EMG biofeedback can be attributed to increased motor unit recruitment (Marder & Bucher 2001; Zehr et al., 2007).

Different from the sEMG amplitude changes of quadriceps femoris, quadriceps femoris strength showed significant differences between groups just at 30 days after intervention. This may be related to sensitivity of sEMG amplitude changes is higher than quadriceps femoris strength changes. sEMG can be used to quantify performance of quadriceps femoris strength in quantity. But the grade of muscle strength is fixed, quadriceps femoris strength need to complete the leap from amount to quality when quadriceps femoris strength increases per level.

The ADL scores improved significantly in both groups at 15 days and 30 days after intervention, but with no statistical significance between groups. This suggests that there is no significant influence on ADL improvement between conventional physical therapy and EMG BF training. This may be related to ADL involves a couple of functional activities, not just relying on the improvement of function of quadriceps femoris. Therefore, lots of ability training is needed to improve ADL.

Our study has several limitations. SCI rehabilitation has a certain correlation among the extent of injury and the time of intervention. Due to the limited number of cases collected in this study, the above factors were not studied in depth. Quadriceps femoris is composed of four pieces of muscles, but we just choose rectus femoris to assess sEMG values of quadriceps femoris, if vastus medialis and vastus lateralis were included, the motor function of quadriceps femoris would be demonstrated better. The course of our study is set to 30 days, if the observation time is extended, the assessment results may be more meaningful. The patients only conducted in a small sample of clinical trials, so multi-center, large sample clinical observation are needed in the future.

5 Conclusion

EMG BF training may be a good way to enhance motor function of quadriceps femoris in patients with incomplete SCI. sEMG could quantify the changes of single muscle myodynamia precisely before visible or touchable changes occur.

Footnotes

Acknowledgments

We thank all subjects who participated in this study for their time and cooperation.

Conflict of interest

The authors declare no conflict of interest.

Funding

This work was supported by the Special Fund for Basic Scientific Research of Central Public Research Institutes (no. 2014CZ-4).

References

Alam,

, Rodrigues,

, Pham,

B. N.

, & Thakor,

N. V.

(2016). Brain-machine interface facilitated neurorehabilitation via spinal stimulation after spinal cord injury: Recent progress and future perspectives. Brain Research, 1646, 25–33.

Anwer,

, Quddus,

, Miraj,

, & Equebal,

(2011). Effectiveness of electromyographic biofeedback training on quadriceps muscle strength in osteoarthritis of knee †. Archives of Physical Medicine & Rehabilitation, 29(2), 86–93.

Armadadasilva,

P. A.

, Pereira,

, Amado,

, & Veloso,

A. P.

(2013). Role of physical exercise for improving posttraumatic nerve regeneration. International Review of Neurobiology, 109(109C), 125–149.

Baumueller,

, Winkelmann,

, Irnich,

, & Weigl,

(2017). Electromyogram Biofeedback in Patients with Fibromyalgia: A Randomized Controlled Trial. Complementary Medicine Research, 24(1), 33–39.

Christanell,

, Hoser,

, Huber,

, Fink,

, & Luomajoki,

(2012). The influence of electromyographic biofeedback therapy on knee extension following anterior cruciate ligament reconstruction: a randomized controlled trial. Sports Med Arthrosc Rehabil Ther Technol, 4(1), 41.

Criswell,

(2010). Cram’s Introduction to Surface Electromyography, 2nd Edition. Physiotherapy, 84(8), 405.

Croce,

R. V.

, & Miller,

J. P.

(2003). The effect of movement velocity and movement pattern on the reciprocal co-activation of the hamstrings. Electromyogr Clin Neurophysiol, 43(8), 451–458.

De Biase,

M. E.

, Politti,

, Palomari,

E. T.

, Barrosfilho,

T. E.

, & De Camargo,

O. P.

(2011). Increased EMG response following electromyographic biofeedback treatment of rectus femoris muscle after spinal cord injury. Physiotherapy, 97(2), 175–179.

Dietz,

, & Curt,

(2006). Neurological aspects of spinal-cord repair: promises and challenges. The Lancet Neurology, 5(8), 688–694.

10.

Durigan,

J. L.

, Delfino,

G. B.

, Peviani,

S. M.

, Russo,

T. L.

, Ramirez,

, Da,

S. G. A.

,... & Salvini,

T. F.

(2014). Neuromuscular electrical stimulation alters gene expression and delays quadriceps muscle atrophy of rats after anterior cruciate ligament transection. Muscle Nerve, 49(1), 120–128.

11.

Eid,

M. A.

, Aly,

S. M.

, & El-Shamy,

S. M.

(2016). Effect of Electromyographic Biofeedback Training on Pain, Quadriceps Muscle Strength, and Functional Ability in Juvenile Rheumatoid Arthritis. Am J Phys Med Rehabil, 95(12), 921–930.

12.

Fauth,

M. L.

, Petushek,

E. J.

, Feldmann,

C. R.

, Hsu,

B. E.

, Garceau,

L. R.

, Lutsch,

B. N.

,... & Ebben,

W. P.

(2010). Reliability of surface electromyography during maximal voluntary isometric contractions, jump landings, and cutting. J Strength Cond Res, 24(4), 1131–1137.

13.

Fu,

, Wang,

, Deng,

, & Li,

(2016). Exercise Training Promotes Functional Recovery after Spinal Cord Injury. Neural Plasticity, 2016, 1–7.

14.

Govil,

, & Noohu,

M. M.

(2013). Effect of EMG biofeedback training of gluteus maximus muscle on gait parameters in incomplete spinal cord injury. Neurorehabilitation, 33(1), 147–152.

15.

Hodson-Tole,

E. F.

, & Wakeling,

J. M.

(2009). Motor unit recruitment for dynamic tasks: current understanding and future directions. J Comp Physiol B, 179(1), 57–66.

16.

Holtermann,

, Mork,

P. J.

, Andersen,

L. L.

, Olsen,

H. B.

, & Sogaard,

(2010). The use of EMG biofeedback for learning of selective activation of intra-muscular parts within the serratus anterior muscle: a novel approach for rehabilitation of scapular muscle imbalance. J Electromyogr Kinesiol, 20(2), 359–365.

17.

Jensen,

M. P.

, Barber,

, Romano,

J. M.

, Hanley,

M. A.

, Raichle,

K. A.

, Molton,

I. R.

,... & Patterson,

D. R.

(2010). Effects of Self-Hypnosis Training and EMG Biofeedback Relaxation Training on Chronic Pain in Persons with Spinal-Cord Injury. International Journal of Clinical and Experimental Hypnosis, 57(3), 239–268.

18.

Jones,

M. L.

, Evans,

, Tefertiller,

, Backus,

, Sweatman,

, Tansey,

,... & Morrison,

(2014). Activity-Based Therapy for Recovery of Walking in Chronic Spinal Cord Injury: Results from a Secondary Analysis to Determine Responsiveness to Therapy. Archives of Physical Medicine & Rehabilitation, 95(12), 2247–2252.

19.

Kesemenli,

C. C.

, Sarman,

, Baran,

, Memisoglu,

, Binbir,

, Savas,

,... & Koc,

(2014). A new isometric quadriceps-strengthening exercise using EMG-biofeedback. International Journal of Clinical & Experimental Medicine, 7(9), 2651–2655.

20.

Kim,

C. M.

, Eng,

J. J.

, & Whittaker,

M. W.

(2004). Level walking and ambulatory capacity in persons with incomplete spinal cord injury: relationship with muscle strength. Spinal Cord, 42(3), 156–162.

21.

Kim,

K. S.

, Seo,

J. H.

, & Song,

C. G.

(2011). Portable measurement system for the objective evaluation of the spasticity of hemiplegic patients based on the tonic stretch reflex threshold. Medical Engineering & Physics, 33(1), 62–69.

22.

Malone,

, Meldrum,

, Gleeson,

, & Bolger,

(2011). Reliability of surface electromyography timing parameters in gait in cervical spondylotic myelopathy. J Electromyogr Kinesiol, 21(6), 1004–1010.

23.

Marder,

, & Bucher,

(2001). Central pattern generators and the control of rhythmic movements. R. Curr Biol, 11(23), 986–996.

24.

Mathur,

, Eng,

J. J.

, & MacIntyre,

D. L.

(2005). Reliability of surface EMG during sustained contractions of the quadriceps. J Electromyogr Kinesiol, 15(1), 102–110.

25.

Nardone,

, Höller,

, Brigo,

, Höller,

, Christova,

, Tezzon,

,... & Trinka,

(2013). Fatigue-induced motor cortex excitability changes in subjects with spinal cord injury. Brain Research Bulletin, 99(5), 9–12.

26.

Petrofsky,

J. S.

(2001). The use of electromyogram biofeedback to reduce Trendelenburg gait. European Journal of Applied Physiology, 85(5), 491–495.

27.

Raineteau,

, & Schwab,

M. E.

(2001). Plasticity of motor system after incomplete spinal injury. Nature Reviews Neuroscience, 2(4), 263–273.

28.

Suzuki,

, Muraoka,

, & Okazaki,

(2017). Development of a low-cost EMG biofeedback device kit as an educational tool for physical therapy students. J Phys Ther Sci, 29(9), 1522–1526.

29.

Watanabe,

, & Akima,

(2011). Validity of surface electromyography for vastus intermedius muscle assessed by needle electromyography. J Neurosci Methods, 198(2), 332–335.

30.

Wyndaele,

, & Wyndaele,

J. J.

(2006). Incidence, prevalence and epidemiology of spinal cord injury: what learns a worldwide literature survey? Spinal Cord, 44(9), 523–529.

31.

Zehr,

E. P.

, Balter,

J. E.

, Ferris,

D. P.

, Hundza,

S. R.

, Loadman,

P. M.

,... & Stoloff,

R. H.

(2007). Neural regulation of rhythmic arm and leg movement is conserved across human locomotor tasks. J Physiol, 582(Pt 1), 209–227.

Effect of electromyographic biofeedback training on motor function of quadriceps femoris in patients with incomplete spinal cord injury: A randomized controlled trial

Abstract

BACKGROUND:

OBJECTIVE:

METHODS:

RESULTS:

CONCLUSIONS:

Keywords

1 Introduction

2 Methods

2.1 Patients

2.3 Randomization and allocation concealment procedure

2.4 Interventions

2.4.1 EMG BF training

2.4.2 Conventional physical therapy

2.5 Statistical analysis

3 Results

Table 1 Characteristics of the patients Intervention (n = 17) Control (n = 16) Age (mean±SD) 36.18±9.08 36.63±9.34 Male/Female 12/5 12/4 Days post injury (mean±SD) 47.53±33.17 48.38±29.17 ASIA (B/C/D) 10/5/2 9/6/1 Injury level (T/L) 10/7 8/8

5 Conclusion

Footnotes

Acknowledgments

Conflict of interest

Funding

References

Table 1
Characteristics of the patients

Intervention (n = 17) Control (n = 16)

Age (mean±SD) 36.18±9.08 36.63±9.34

Male/Female 12/5 12/4

Days post injury (mean±SD) 47.53±33.17 48.38±29.17

ASIA (B/C/D) 10/5/2 9/6/1

Injury level (T/L) 10/7 8/8