Muscle Fatigue During Intermittent

Electrical Stimulation

Toshiki Matsunaga, Yoichi Shimada, Kozo Sato, Yoshihiro Tsutsumi, Takeshi Kashiwagura, Akiko Misawa, Shigeru Ando, Satoaki Chida, Kiyomi Iizuka

Abstract- The purpose of this study is to evaluate muscle fatigue during intermittent stimulation. Twenty adult male Wistar rats were used in this experiment. The sciatic nerve and the gastrocnemius muscle were exposed surgically under general anesthesia. The gastrocnemius muscle was connected to a strain gauge and stimulated through a nerve cuff electrode attached to the sciatic nerve. Stimulation frequencies were 20Hz, 50Hz, 70Hz, and 100Hz. The pulse amplitude was set at supramaximal voltage and the pulse width was 0.2 ms. The stimulation pattern was 4 seconds of stimulation at the beginning of every 30 second period. Intermittent stimulation lasted for 15 minutes, and the contraction forces of the stimulated muscle were measured isometrically during the stimulation phase. The Strength Decrement Index (SDI) was used to assess muscle fatigue. SDI were 53.4 ± 14.5 % (Mean ± SD) at 20Hz, 33.5 ± 7.5 % at 50Hz, 33.5 ± 20.6 % at 70Hz, and 21.2 ± 6.0 % at 100Hz. Muscle fatigue was significantly greater at 20Hz than at 50Hz, 70Hz and 100Hz (p < .01). During 4 seconds of stimulation, peak contraction force was sustained at 50Hz and 70Hz rather than at 100Hz. The result of this study suggests that intermittent high-frequency stimulation (especially 50-70Hz) is clinically useful for closed-loop control.

Index Terms- Muscle fatigue, Closed-loop control, High frequency stimulation

I. INTRODUCTION

When a paralyzed muscle is activated by using FES, its force output decays with time due to fatigue. In recent years, advances in medical engineering have made it possible for paraplegic patients to remain standing assisted by FES [2], [9]. Presently used clinical FES standing systems require continued activation of the lower limb muscles, so that muscle fatigue and uncontrollable knee buckling occur in the early period [1], [2], [7], [9]. For persons with paraplegia to use FES most effectively, therefore, it is important to reduce muscle fatigue.

Closed-loop control is one of the strategies to reduce muscle fatigue [1], [8]. The system involves sensors to detect knee buckling, a computer-controlled stimulator, and electrodes for stimulation. Andrews et al [1], [2] proposed a hybrid FES system utilizing closed-loop control for the restoration of the standing position. Paraplegic patients who wear the ankle foot orthosis can remain standing without muscle activity of their lower limbs while maintaining the "C"-posture. When knee buckling occurs, the knee sensor detects the buckling motion and causes the FES system to stimulate the quadriceps muscles for a few seconds to correct the postural imbalance. The amount of stimulation required using closed-loop control is less than that of continuous stimulation, therefore, closed-loop control is expected to help reduce muscle fatigue.

The choice of stimulation frequency is another important factor in reducing muscle fatigue. Low frequency stimulation (about 20 Hz) has been used clinically for continuous stimulation [9]. It has never been studied about the optimal stimulation frequencies applied to intermittent stimulation in closed-loop control.

The purpose of this study is to assess muscle fatigue

during intermittent electrical stimulation under different

stimulation frequencies.

II. MATERIALS AND METHODS

Twenty adult male Wistar rats (432 ± 35.2 g) were anaesthetized with intraperitoneal pentabarbitol (30 mg / kg) and the medial head of gastrocnemius, with the Achilles tendon was dissected free while attached proximally to the femur. The tendon of gastrocnemius was firmly tied to a light steel link which was attached to a strain gauge. The sciatic nerve was exposed and branches to other muscles were severed. A nerve cuff electrode was attached to the sciatic nerve. The gastrocnemius muscle was then stimulated intermittently through a nerve cuff electrode, and isometric contraction force was measured during the stimulation phase. Stimulation frequencies applied in this study were 20Hz, 50Hz, 70Hz, and 100Hz. At each frequency, the electrical pulse was monophasic square waveform, and the pulse width was 0.2 ms. The pulse amplitude was set at supramaximal voltage. The intermittent stimulation pattern was 4 seconds of stimulation at the beginning of every 30 second period. This stimulation protocol lasted for 15 minutes, and the contraction forces of the stimulated muscle were measured isometrically during the stimulation phase. Pentabarbitol was administered as necessary during the experiment to maintain a deep anesthesia. The protocols for animal experimentation described in this paper were previously approved by the Animal Research Committee, Akita University School of Medicine; All subsequent animal experiments adhered to the Guidelines for Animal Experimentation of the University.

A Strength Decrement Index (SDI) was used to assess muscle fatigue [5]. SDI was calculated by the formula:

SDI (%) = (Fi - Ff) × 100 / Fi

where Fi = maximal force in the periods of initial 4 seconds of stimulation and Ff = maximal force in the period of 4

seconds of stimulation at the end of fatigue test. SDI gives the attenuation of contraction force from the beginning of stimulation. Accordingly, the lower its value the higher the resistance to fatigue. The data were reported as mean values ± standard deviation (SD). All data were analyzed statistically using a Fisher's Protected Least Significant Difference (Fisher's PLSD). Criterion for significance was a p value < .01.

III. RESULTS

SDI were 53.4% ± 14.5 % at 20Hz, 33.5% ± 7.5% at 50Hz, 33.5% ± 20.6% at 70Hz and 21.2% ± 6.0% at 100Hz. There were significant differences in muscle fatigue between 20Hz and 50Hz, 70Hz or 100Hz (Fisher's PLSD, p < .01). There was no significant differences among the remaining combinations (Fig. 1).

The contraction force produced by 50Hz, 70Hz and 100Hz stimulation was greater than the force produced by 20Hz stimulation. During 4 seconds of stimulation, maximal force occurred just after the beginning of stimulation at 50Hz, 70Hz and 100Hz, conversely, it occurred later in the phase at 20Hz (Fig. 2). At the end of fatigue test, the contraction forces remain relatively constant at 50Hz and 70Hz; however, the contraction forces dropped in the early periods at 100Hz stimulation (Fig. 3).

IV. DISCUSSION

Physiologically, muscle fatigue has been subgrouped into two types: (1) low frequency fatigue (LFF), induced by low frequency stimulation (e.g. 20Hz) and characterized by a subsequent long-term loss of force; and (2) high frequency fatigue (HFF), induced by high frequency stimulation (e.g. 50-100Hz) and characterized by a subsequent, rapidly recovering loss of force [3], [5], [6]. The mechanisms of LFF is thought to be impaired excitation-contraction coupling [3], [5]. On the other hand, the mechanisms of HFF is thought to be a consequence of impaired membrane excitation [7]. The characteristic of recovery patterns (slow recovery from LFF and rapid

100Hz

50Hz

20Hz

70Hz

4 sec.

50gf

Fig.2. Force output of fresh muscle during 4 seconds of stimulation at the beginning of fatigue test.

50gf

4 sec.

Fig.3. Force output of fatigued muscle during 4 seconds of stimulation at the end of fatigue test.

recovery from HFF) is caused by these differences in this physiologic mechanisms.

We compared muscle fatigue between 20Hz and 100Hz in human subjects, and reported that muscle fatigue is greater at LFF than at HFF during intermittent electrical stimulation [7]. In this study, muscle fatigue was assessed in detail (20, 50, 70 and 100Hz). Our results indicate that muscle fatigue was greater at LFF (20Hz) than at HFF (50Hz, 70Hz and 100Hz) in animals. Under continuous electrical stimulation, muscle fatigue is greater at higher frequencies. Our results suggest that muscle fatigue during intermittent electrical stimulation is not the same as fatigue under continuous stimulation. The reason is probably because of differences in the fatigue and recovery mechanisms in both low and high frequency stimulation.

In this study, muscle contraction force during high frequency stimulation remained relatively constant at 50Hz and 70Hz. It dropped in the early period at 100Hz especially at the fatigued phase. One possible explanation for these results may be that differences in the speeds of failure of muscle action potentials. For the purpose of the FES assisted standing, it is more suitable to maintain muscle contraction force at 50-70Hz stimulation.

There are some advantages to high frequency stimulation in closed-loop controls. It can produce the rapid and strong contraction of muscles. The stimulated muscles are not so easily fatigued. The fatigued muscle can recover rapidly from fatigue after the FES exercises. Our results suggest that it is possible to use high frequency stimulation for closed-loop control. We propose that the optimal high frequency intermittent stimulation is from 50Hz to 70Hz. Further study includes clinical application of high frequency stimulation to closed-loop control.

References

[1] B. J. Andrews, R. H. Baxendale, R. Barnett, G. F. Phillips, T. Yamazaki, J. P. Paul and P. A. Freeman, "Hybrid FES orthosis incorporating closed loop control and sensory feedback," J. Biomed. Eng., vol. 10, pp. 189-195, 1988.

[2] B. J. Andrews, R. W. Barnett, G. F. Phillips and C. A. Kirkwood, "Rule-based control of a hybrid FES orthosis for assisting paraplegic locomotion," Automedica, vol. 11, pp. 175-199, 1989.

[3] B. Bigland-Ritchie, D. A. Jones and J. J. Woods, "Excitation frequency and muscle fatigue: electrical responses during human voluntary and stimulated contractions," Exp. Neurol., vol. 64, pp. 414-427, 1979.

[4] H. H. Clarke, C. T. Shay and D. K. Mathews, "Strength decrement of elbow flexor muscles following exhaustive exercise," Arch. Phys. Med. Rehabil., vol. 35, pp. 560-567, 1954.

[5] R. G. Cooper, R. H. T. Edwards, H. Gibson and M. J. Stokes, "Human muscle fatigue: frequency dependence of excitation and force generation," J. Physiol., vol. 397, pp. 585-599, 1988.

[6] R. H. T. Edwards, D. K. Hill, D. A. Jones and P. A. Merton, "Fatigue of long duration in human skeletal muscle after exercise," J. Physiol., vol. 272, pp. 769-778, 1977.

[7] T. Matsunaga, Y. Shimada, K. Sato, H. Kagaya, Y. Tsutsumi, T. Kashiwagura and M. Sato, "Muscle fatigue during intermittent high and low frequency stimulation," in Proc. 2nd annual conference of the IFESS' 97 and NP' 97, Burnaby, British Columbia, Canada, 1997, pp. 15-16.

[8] J. S. Petrofsky, C. A. Phillips and D. E. Stafford, "Closed-loop control for restoration of movement in paralyzed muscle." Orthopedics, vol. 7, no. 8, pp. 1289-1302, 1984.

[9] Y. Shimada, K. Sato, E. Abe, H. Kagaya, K. Ebata, M. Oba and M. Sato, "Clinical experience of functional electrical stimulation in complete paraplegia," Spinal Cord, vol. 34, pp. 615-619, 1996.