Archives of Physical Medicine and Rehabilitation
Volume 84, Issue 6 , Pages 843-848, June 2003

Agonist contractions against electrically stimulated antagonists1

  • Tojiro Yanagi, MD

      Affiliations

    • Rehabilitation Center Kurume University, Kurume City, Japan
  • ,
  • Naoto Shiba, MD

      Affiliations

    • Rehabilitation Center Kurume University, Kurume City, Japan
    • Corresponding Author InformationReprint requests to Naoto Shiba, MD, Rehabilitation Center, Kurume University, 155-1 Kokubu-machi, Kurume City, Fukuoka 8390863, Japan
  • ,
  • Takashi Maeda, PT

      Affiliations

    • Rehabilitation Center Kurume University, Kurume City, Japan
  • ,
  • Kiyohiko Iwasa, PT

      Affiliations

    • Rehabilitation Center Kurume University, Kurume City, Japan
  • ,
  • Yuichi Umezu, MD

      Affiliations

    • Rehabilitation Center Kurume University, Kurume City, Japan
  • ,
  • Yoshihiko Tagawa, PhD

      Affiliations

    • Department of Mechanical Engineering, Kurume Institute of Technology, Kurume City, Japan
  • ,
  • Shigeaki Matsuo, PhD

      Affiliations

    • Department of Mechanical Engineering, Kurume Institute of Technology, Kurume City, Japan
  • ,
  • Kensei Nagata, MD

      Affiliations

    • Toyama Prefectural Koshi Rehabilitation Hospital, Toyama City, Japan
  • ,
  • Toshiyasu Yamamoto, PhD

      Affiliations

    • Department of Orthopaedics, Kurume University, Kurume City, Japan
  • ,
  • Jeffrey R Basford, MD, PhD

      Affiliations

    • Department of Physical Medicine & Rehabilitation, Mayo Clinic and Foundation, Rochester MN, USA

Article Outline

Abstract 

Yanagi T, Shiba N, Maeda T, Iwasa K, Umezu Y, Tagawa Y, Matsuo S, Nagata K, Yamamoto T, Basford JR. Agonist contractions against electrically stimulated antagonists.

Objective:

To assess an exercise program that uses electrically stimulated antagonists to resist agonist muscle contractions.

Design:

In 1 limb, electrically stimulated antagonists resisted elbow flexion and extension. In the other, stimulation occurred without volitional muscle contraction.

Setting:

A biomechanics laboratory in Japan.

Participants:

Twelve men between the ages of 19 and 24 years. Subjects served as their own controls.

Intervention:

Subjects trained 3 times a week for 12 weeks. Each session consisted of 10 sets of 10 elbow flexor and extensor contractions.

Main Outcome Measures:

Isokinetic elbow extension and flexion torques. Biceps and triceps brachii cross-sectional areas.

Results:

Elbow extension torques increased (32.85% at 30°/s, 27.20% at 60°/s, 26.16% at 90°/s; all P≤.02) over the training period in limbs that trained against electrically stimulated antagonists. Control limb extension torque increases were smaller (8.52% –14.91%) and did not reach statistical significance. Elbow flexion torques improved in both groups, but the changes did not reach statistical significance. Cross-sectional areas increased in all muscles but were most marked in the antagonist stimulated limbs: triceps 16.20% versus 4.25% (P=.01) and biceps 16.65% versus 7.00% (P=.005).

Conclusions:

Exercises that use electrically stimulated antagonist muscles may be effective in increasing muscle strength and mass.

Keywords:  Electric stimulation, Exercise, Muscles, Rehabilitation, Torque

 

NEUROMUSCULAR ELECTRIC stimulation (NMES) is widely used to lessen immobilization-associated muscle weakness, to strengthen muscles, and to improve function in people with neuromuscular disabilities.1, 2 Although NMES has been in use for more than 40 years, its clinical value and optimal application remain controversial. However, several facts have been established. For example, research has found that NMES is effective in strengthening limb muscles after surgery.3, 4 In addition, several researchers5, 6 have found that the muscle strength of healthy subjects can be increased by 10% to 20% with 3 to 6 weeks of high-intensity stimulation.

NMES research typically focuses on the direct stimulation of the muscles to be exercised. Although this approach does produce strength gains,1, 2, 3, 4, 5, 6 the gains are realized more slowly than patients would like. Also, the approach may be little more effective than traditional weight-based resistance training programs.5, 6 An NMES program that could produce faster or larger gains in strength and muscle bulk than is possible with current approaches would be attractive.

The idea of using electric stimulation to provide the training resistance to a contracting muscle (much as a dumbbell provides resistance to the elbow flexors during an elbow curl) is particularly alluring. We, therefore, decided to turn the traditional NMES paradigm around and investigate a situation in which the antagonist of the muscle being exercised was stimulated. Specifically, we developed a hybrid strengthening technique that uses the force generated by an electrically stimulated antagonist to provide resistance to a volitionally contracting agonist. In other words, the agonist performs a volitional concentric contraction against an electrically stimulated antagonist (fig 1).

  • View full-size image.
  • Fig 1. 

    Schematic model of the exercise method. Note that both the volitionally activated agonist and the electrically stimulated antagonist contract during joint motion. The result is that both muscles are exercised and that a longitudinal compressive load is placed on the bone

The purpose of this study was to compare the muscle strengthening and bulk increasing benefits of this hybrid approach with the benefits of a conventional NMES program.

Back to Article Outline

Methods 

The study protocol was approved by the institutional review board of Kurume University. Informed consent to participate was obtained from 12 healthy right-hand dominant sedentary men. Subjects were required to have normal musculoskeletal examinations (ie, normal strength, sensation [light touch, sharp, proprioception], coordination, range of motion [ROM]). Hand dominance was determined in accordance with the Edinburgh Inventory.7 Subjects were block randomized into 2 groups of 6. In 1 group, the hybrid exercise program was performed with the right upper extremities and a conventional NMES program was performed with the left. In the other group, the hybrid program was performed with the left upper extremities and the control program was performed with the right. Participants were not paid.

Exercise 

Hybrid exercise 

Subjects trained 3 times a week (Mondays, Wednesdays, Fridays) for 12 weeks. Each exercise session consisted of 10 sets of 10 reciprocal 2-second elbow flexion and extension contractions. Sets were separated by 1-minute rest intervals, and an exercise session was completed in 15 minutes and 40 seconds. Exercises were performed in a standardized manner, with the biceps brachii stimulated as the subject volitionally extended his elbow and the triceps brachii stimulated as he volitionally flexed his elbow (see Electric Stimulation Protocol below). Joint ROM was measured with a goniometer and restricted to an arc that extended from 15° to 105° of elbow flexion. Subjects changed the direction of their joint movement when the stimulator emitted a tone (fig 2).

  • View full-size image.
  • Fig 2. 

    The subject exercises the left arm for the hybrid method and the right arm for the control method. Specially made gel-coated metal fiber electrodes are placed over the motor points of the biceps and triceps brachii. One pair of electrodes is placed over the each muscle of each upper limb. To avoid the influence of gravity, the subjects set their upper limbs onto the cushions, which have a 30° angular surface. The hybrid exercise is performed from 15° to 105° of flexion during elbow flexion and extension motion

Control exercise 

A similar program was followed with the control limb, except that the elbow was immobilized in a brace at 60° of flexion and the subject was instructed not to attempt a volitional muscle contraction.

Electric stimulation protocol 

Electric stimulation device 

The electric stimulation device was developed by this group and has been described previously.8 Briefly, it consists of a waveform generator and a microcomputer that delivers stimulating signals to as many as 8 individually controlled electrodes. Frequency, intensity, and waveform characteristics can be individually selected for each pair of electrodes. In this experiment, a pair of 2×6cm custom-made gel-coateda silver fiber electrodes were placed over the motor points of the biceps and triceps brachii that had been isolated by moving a probe over the skin surface to find the lowest threshold for electric stimulation.

Stimulation waveform 

A 5000Hz carrier frequency was modulated at 20Hz (2.4ms on, 47.6ms off) to deliver a rectangular waveform for 2-second intervals.

Stimulation intensity 

The maximum comfortable intensity was determined at each session by increasing the stimulation voltage until the subjects reported discomfort. Mean voltage for NMES was 60.35±19.55V. Output powers were less than 10W, and the stimulation parameters included current intensities of less than 10mA/cm2 and voltage less than 80V (fig 2).

Torque measurements 

Maximal isokinetic elbow flexion and extension torques were measured with a KIN-COMb dynamometer at a baseline immediately before the exercise trial began, as well as at the 6-week midpoint and 12-week conclusion of the exercise program. Subjects were tested at angular velocities of 30°, 60°, and 90°/s with their forearm in a neutral position while they sat in a chair with their shoulder and body fixed to a frame. The averages of 3 maximal elbow extension and flexion torque were used in calculations.

Measurement of muscle bulk 

Biceps and triceps brachii cross-sectional areas (CSAs) were measured on the same days that the torque determinations were made (ie, at the baseline, middle, end of the exercise trial). A standardized procedure was followed. The position of the midpoint between the acromial process and medial epicondyle was marked with an indelible marker at the first session and renewed as necessary throughout the experiment. An adhesive 5×5×5mm daub of gel was placed on the mark at the time that CSA determinations were made, and scout views were used to ensure that the scanning position did not change between sessions. CSAs were measured on the display of a magnetic resonance imaging (MRI) device (Hitachi Airis IIc) by a blinded observer. Changes in CSA with time were defined as the ratio of the change in CSA over the period studied divided by the baseline value, that is, CSA change=([CSA at the midpoint or end of the exercise trial/CSA at baseline]−1).

Statistics 

Standard methods were used to calculate mean values and standard deviations. Torques at baseline were compared with torques found at the 6-week midpoint and at the 12-week conclusion of the exercise trial. CSA changes were compared at the same intervals. The F distribution and 2-tailed Student t tests were used. P values of ≤.05 were considered to be significant. Statistical analyses were performed with SPSS, version 8.0,d for Windows.

Back to Article Outline

Results 

The mean age of the participants was 21.5 years (range, 19–24y). All subjects attended all 36 sessions of the training program. There were no injuries, but a few individuals complained of postexercise delayed-onset muscle soreness early in the program.

Muscle force measurement: elbow extension torque 

Hybrid exercise 

The maximal extension torques of the hybrid exercise group at baseline were 29.92±5.70Nm at 30°/s, 29.42±5.42Nm at 60°/s, and 28.67±5.31Nm at 90°/s. At the 6-week midpoint, these values had increased to 33.75±6.90Nm, 31.83±6.85Nm, and 30.33±7.14Nm, respectively. At completion of the 12-week training, these torques had further increased to 39.75±9.76Nm, 37.42±9.88Nm, and 36.17±9.83Nm. Although the increases in extension torque at 6 weeks did not reach statistical significance, the increases at 12 weeks were marked and statistically significant (32.85% at 30°/s, P=.007; 27.20% at 60°/s, P=.03; 26.16% at 90°/s, P=.02, respectively; fig 3A).

  • View full-size image.
  • Fig 3. 

    Muscle force measurements of isometric (A) elbow extension and (B) flexion torque (Nm) at before, 6 weeks, and 12 weeks after exercise were presented, respectively. Muscle force had increased significantly after 12 weeks

Control limbs 

Maximum extension torques in the control limbs at baseline were 31.33±6.85Nm at 30°/s, 31.33±7.75Nm at 60°/s, and 30.08±7.35Nm at 90°/s. At the midpoint of the program, these values had increased to 35.5±6.23Nm, 33.58±5.07Nm, and 32.42±4.66Nm, respectively. Although these torques had further increased after 12 weeks (36.00±8.45Nm, 34.00±7.85Nm, 33.00±7.68Nm, respectively), neither the 6- nor 12-week changes were statistically significant (fig 3A)

Muscle force measurement: elbow flexion torque 

Hybrid exercise 

Maximum flexion torques at baseline were 28.33±9.86Nm at 30°/s, 26±7.93Nm at 60°/s, and 24.33±6.98Nm at 90°/s in the hybrid-trained limbs. At the 6-week midpoint they had increased, albeit in a statistically insignificant manner relative to baseline, to 32.08±7.42Nm, 28.75±6.43Nm, and 28.08±7.30Nm, respectively. Progress plateaued, and, at the end of the program, flexion torques (32.92±9.54Nm at 30°/s, 30.75±9.55Nm at 60°/s, 29.58±9.29Nm at 90°/s) differed insignificantly from their baseline values.

Control limbs 

Flexion torques in the control limbs were 26.75±5.88Nm at 30°/s, 24.33±5.61Nm at 60°/s, and 22.42±5.35Nm at 90°/s at baseline. At the midpoint of training, they had increased to 30.25±7.23Nm at 30°/s, 28.5±6.26Nm at 60°/s, and 26.75±5.55Nm at 90°/s, respectively, but did not differ significantly from their baseline measurements. At the end of training, the torques had further increased to 32.17±9.40Nm at 30°/s, 29.25±8.52Nm at 60°/s, and 27.58±8.10Nm at 90°/s, but the changes remained insignificant (fig 3B).

Measurement of muscle bulk using MRI 

The triceps and biceps brachii increased in bulk and changed in shape (ie, each became rounder; fig 4). Changes were pronounced enough to be appreciated visually (fig 5).

  • View full-size image.
  • Fig 4. 

    Example of the changes revealed by MRI in the CSA of the muscles in the right-hybrid-trained brachium. Note that the CSAs of both muscles increased and became rounded after 6 weeks. (A) Before exercise; (B) 6 weeks after hybrid exercise; and (C) 12 weeks after hybrid exercise

  • View full-size image.
  • Fig 5. 

    Increased ratio of the CSA of brachial muscles, comparing hybrid exercise with control exercise. It was remarkably greater than that of the control exercise both in biceps and triceps brachii. Abbreviation: W, week

Triceps brachii 

Triceps CSA at the 6-week midpoint of the exercise trial had increased by 16.00%±8.39% in the hybrid limbs relative to 1.80%±4.14% in the control limbs (P<.0001). At 12 weeks, this discrepancy persisted but had lessened with the triceps CSA 16.20%±11.02% in the hybrid trained limbs and 4.25%±7.87% in control limbs (P=.01).

Biceps brachii 

Similar changes occurred in the biceps. At the midpoint of training, the biceps CSA had increased 12.98%±8.32%, in the hybrid trained limbs relative to an increase of 7.04%±4.15% in the control limbs (P=.04). After 12 weeks, these changes were 16.65%±10.74% in the hybrid group relative to a 7.00%±4.54% change in control limbs (P=.005).

Back to Article Outline

Discussion 

This study shows that, at least in this sample of subjects and muscles, this hybrid exercise program produced significantly greater changes in muscle bulk and triceps brachii strength than did a conventional NMES approach. Although our sample size and the muscles studied were limited, these findings deserve further discussion.

First, this approach may offer several advantages. For example, volitional muscle contractions activate slow-twitch and fast-twitch muscle in a sequential manner.9 NMES, on the other hand, does not follow this physiologic pattern in that it activates slow-twitch muscle poorly and is most efficient in stimulating fast-twitch muscles.9, 10, 11 This nonphysiologic pattern of activation may lead to less effective strengthening and may also contribute to the reluctance of many physicians to accept electric stimulation as a common component of therapeutic muscle strengthening programs. A hybrid exercise technique may obviate some of this concern because of its more physiologic approach of using both volitional and electrically stimulated contractions.

Another potential advantage of this approach is the combination of eccentric contractions and electric stimulation. Westing et al,12 for example, reported that the muscle torque resulting from an electrically stimulated eccentric contraction was 21% to 24% greater than that produced by a voluntary eccentric contraction alone. In addition, Seger and Thorstensson13 compared the effects of electrically stimulated eccentric, isometric, and concentric contractions of the quadriceps at angular velocities similar to those of our study. They found that under similar stimulating conditions, eccentric contractions generated torques about 15% to 25% greater than those produced with isometric contractions and about 30% to 50% greater than the torques resulting from concentric contractions.

The CSA findings are also interesting. Not only were CSA increases significantly greater in the hybrid than in the control limbs at both the midpoint and the conclusion of the exercise program, but the bulk (and the strength) of the triceps brachii increased more than that of the biceps. This pattern may not be surprising, because the biceps is used actively throughout the day, whereas the triceps is used less vigorously. Thus, the triceps might have begun at a lower level of its potential maximum strength than the biceps.14 It is also possible that this discrepancy is an artifact of our study design. The biceps brachii is involved in elbow flexion, but it shares the task with the brachialis.

The hybrid program seems to be safe and well tolerated. All of our subjects attended all 36 sessions of the program. There were no injuries. A few individuals complained of postexercise, delayed-onset muscle soreness early in the program. This was not unexpected because previous reports6 on electric stimulation have noted late-onset muscle soreness, but there is virtually no evidence of damage to the muscles or tendons among people undergoing electrically stimulated muscle strengthening. In addition, our hybrid exercise used considerably lower stimulation intensities than what is typically used in many NMES studies.12, 13

Further discussion is warranted about whether this hybrid exercise can be optimized and about its appropriateness for use on other muscles, with elderly patients, or with people with osteoporosis. We plan to continue studying the short- and long-term effects of this exercise approach.

Back to Article Outline

Conclusions 

It appears that the hybrid exercise technique described here is more effective in increasing muscle bulk and strength than is the conventional NMES program we used in this study. As such, it may have a role in musculoskeletal rehabilitation. However, both our sample and the muscles we studied were limited. More research is necessary to establish clear therapeutic benefits and optimal parameter choices.

Suppliers

Back to Article Outline

Acknowledgements 

We thank Akira Maeda, MD, Narita Orthopaedic Hospital, Fukuoka City, Fukuoka, Japan for providing access to the MRI device.

Back to Article Outline

References 

  1. Shimada Y, Kagaya H, Ebata K. Restoration of locomotion in paraplegics by functional electrical stimulation. In: Proceeding of the 1st International FES Symposium; 1992 July 23–25; Sendai (Japan). Sendai: Sendai FES Research Project; 1992;p. 110–114
  2. Kagaya H, Shimada Y, Ebata K. Restoration and analysis of standing-up in complete paraplegia utilizing functional electrical stimulation. Arch Phys Med Rehabil. 1995;76:876–881
  3. Delitto A, Rose SJ, McKowen JM, Lehman RC, Thomas JA, Shively RA. Electrical stimulation versus voluntary exercise in strengthening thigh musculature after anterior cruciate ligament surgery. Phys Ther. 1988;68:660–663
  4. Snyder-Mackler L, Delitto A, Bailey SL, Stralka SW. Strength of the quadriceps femoris muscle and functional recovery after reconstruction of the anterior cruciate ligament. A prospective, randomized clinical trial of electrical stimulation. J Bone Joint Surg Am. 1995;77:1166–1173
  5. Stein RB, Kimoto M, Bobet J. Biomechanics of human quadriceps muscles during electrical stimulation. J Biomech. 1999;32:347–353
  6. Balogum JA, Onilari OO, Akeju OA, Marzouk DK. High voltage electrical stimulation in the augmentation of muscle strength; effect of pulse frequency. Arch Phys Med Rehabil. 1993;74:910–916
  7. Oldfield RC. The assessment and analysis of handedness (the Edinburgh Inventory). Neuropsychologia. 1971;9:97–113
  8. Ogino M, Shiba N, Nagata K, et al.  MRI quantification of muscle activity after volitional exercise and neuromuscular electrical stimulation. Am J Phys Med Rehabil. 2002;81:446–451
  9. Montes MR, Tabernero GA, Martin-Garcia MS. Spectral electromyographic changes during muscular strengthening training based on electrical stimulation. Electromyogr Clin Neurophysiol. 1997;37:287–295
  10. Phillips CA, Petrofsky JS. Velocity of contraction of skeletal muscle as a function of activation and fiber composition (a mathematical model). J Biomech. 1980;13:549–558
  11. Clamann H, Gillies J, Skinners R, Henneman E. Quantitative measures of output of a motoneuron pool during monosynaptic reflexes. J Neurophysiol. 1979;37:1328–1337
  12. Westing SH, Seger JY, Thorstensson A. Effects of electrical stimulation on eccentric and concentric torque-velocity relationships during knee extension in man. Acta Physiol Scand. 1990;140:17–22
  13. Seger JY, Thorstensson A. Electrically evoked eccentric and concentric torque-velocity relationships in human knee extensor muscles. Acta Physiol Scand. 2000;169:63–69
  14. Joseph DZ, Frederick AM. Functional motion of the elbow. In:  Nordic M,  Frankel VH editor. Basic biomechanics of the musculoskeletal system. 2nd ed. Philadelphia: Lea & Febiger; 1989;p. 252–253
  • 1 No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the author(s) or upon any organization with which the author(s) is/are associated.
  • a Nihon Medix Co, 315-1, Mukai-machi, Minami-hanashima, Matsudo-shi, Chiba-ken, Japan.
  • b Chattanooga Group Inc, 4717 Adams Rd, Hixson, TN 37343.
  • c Hitachi Medical Corp, 1-1-14, Uchikanda, Chiyodaku, Tokyo 101-0047, Japan.
  • d SPSS Inc, 233 S Wacker Dr, 11th Fl, Chicago, IL 60606.

PII: S0003-9993(02)04948-1

doi:10.1016/S0003-9993(02)04948-1

Archives of Physical Medicine and Rehabilitation
Volume 84, Issue 6 , Pages 843-848, June 2003