Research Review By Christopher Howard©

Date Posted:

March 2010

Study Title:

Time course of changes in muscle and tendon properties during strength training and detraining

Authors:

Kubo K, Ikebukuro T, Yata H, Tsunoda N & Kanehisa H

Author's Affiliations:

Department of Life Science, University of Tokyo, Tokyo, Japan; Department of Physical Education, Kokushikan University, Tokyo, Japan; and Sports Science Laboratory, Wako University, Tokyo, Japan

Publication Information:

Journal of Strength & Conditioning Research 2010; 24(2): 322-331.

Background Information:

It is widely accepted that initial increases in muscle strength from resistance training are due to neural factors and that subsequent gains in strength are due to muscle hypertrophy. For example, Moritani and deVries (1) have reported that muscle strength increased after 2 weeks of resistance training with no increase in muscle size.

Several studies (2,3 for example) have shown that muscle hypertrophy then results after 8-12 weeks of resistance training. Recently, researchers have begun to examine the effects of resistance training on the properties of human tendons. According to this research, the stiffness of human tendons and muscle strength and mass increased significantly after 12-16 weeks of training. However, studies of shorter duration (6-8 weeks) resulted in minimal increase in those parameters (3). Therefore, it is presumed that adaptations of the human tendon occur much slower than those of muscle tissue in response to resistance training.

While resistance training increases muscle strength, muscle size and neural drive to muscle, it has been shown that detraining results in reduced muscle strength, muscle size, and neural drive (4). There have been no reports on the effects of detraining on human tendons.

However, Kubo et al. (5) and Reeves et al. (6) have demonstrated that the stiffness of human tendons is decreased after bed rest. Information on the time course of changes in muscle and tendon properties during training and detraining is essential for improving performance and limiting injury.

The purpose of this study was to investigate the time course of changes in mechanical and morphological properties of human muscle and tendon during isometric training and detraining.

Pertinent Results:

  • In the training group, maximal voluntary isometric strength increased by 29.6% after 2 months and by 40.5% after 3 months.
  • Muscle activation level increased by 7.3% and mEMG (m=mean, or average) increased 27.4% after 2 months and by 8.9% and 35% after 3 months, respectively.
  • Neither maximal voluntary isometric strength, muscle activation level, nor mEMG changed during 3 months of detraining.
  • The cross-sectional area of the quadriceps as a whole increased by 5.5% after 3 months of training. After 1 month of detraining, quadriceps cross-sectional area had decreased to pre-training levels.
  • No changes in the above variables were noted among the control group.
  • The stiffness of the tendon increased 54% after 3 months of training and returned to pre-training levels after 2 months of detraining.
  • No significant change in the cross-sectional area of the patella tendon was found during training or detraining.
  • No changes were noted in tendon variables in the control group during the length of the experimental period.

Clinical Application & Conclusions:

There are a few important findings of this study. First, it appears that adaptations in the tendon due to resistance training are slower than those of muscle and nervous tissue. Secondly, the adaptations of the tendon during detraining occur faster than those of muscle and nervous tissue. In addition, it was found that increases in MVC, neural activation level and mEMG remained even during 3 months of detraining, while the cross-sectional area decreased after just one month of detraining.

It is important to take note of the results of this study when training athletes for increased performance, preventing injuries, and rehabilitation after an injury. Adaptations in muscle and tendon occur at different rates in response to training and detraining, it is important to design resistance training programs accordingly.

The muscular and nervous systems will respond to resistance training quicker than tendons will, therefore it is important to not overload the tendons in the initial phases of training. In addition, detraining results in changes in the tendon well in advance of changes in the muscular and nervous system, thus making them more susceptible to injury. Consequent re-training should be conservative at first to account for these differences.

Study Methods:

Subjects:
  • The study consisted of 14 healthy men, which were randomly assigned to either the training group or the control group.
  • The subjects were physically active, but had not participated in any organized program of exercise for at least 1 year prior to the study.
Procedures:
  • Experimental Design: The training group was tested every month during training (3 months) and detraining (3 months). The control group was tested at the end of the training period (3 months) and at the end of the detraining period (3 months).
  • Training and Detraining: Training consisted of unilateral knee extension in the seated position 4 times per week for 3 months. The training protocol involved isometric knee extensions at 70% of maximal voluntary isometric strength. Subjects performed 10 contractions of 15 seconds duration, with 30 seconds rest between repetitions. Maximal voluntary isometric strength was measured every month and training loads were adjusted based on test results. After the 3 month training period, subjects underwent a 3 month detraining period.
  • Muscle Strength and Neural Activation Level: Maximal voluntary isometric strength of the knee extensor muscles was determined on a dynamometer. The subject sat in an adjustable chair with back support and hip joint flexed at an angle of 80° to standardize the measurements. The ankle was firmly attached to the lever arm of the dynamometer with a strap and fixed with knee joint at an angle of 90°. The center of rotation of the dynamometer was visually aligned with the center of rotation of the knee joint. When the voluntary torque peaked, evoked twitch contractions were imposed by supramaximal electrical stimulations. The stimulating electrodes were placed on the skin over the femoral nerve at the inguinal region (cathode) and the mid belly of the quadriceps muscle (anode). Rectangular pulses (triple stimuli with a 500-ms duration for one stimulus and an inter-stimulus interval of 10 milliseconds) were delivered using a high-voltage stimulator. The difference between peak twitch torque and MVC (twitch torque) was measured. The same stimulation was given to the muscle at rest (control twitch torque). The neural activation level (%) of the knee extensor muscles was calculated as: (1 - [twitch torque during MVC/control twitch torque]) x 100.
  • Mechanical Properties of Tendon: Subjects exerted isometric knee extension torque from zero (relaxed) to MVC within 5 seconds. Ultrasound was used to obtain a longitudinal image of the vastus lateralis muscle (VL) at the level of 50% of the thigh length a distance between the greater trochanter and the lateral epicondyle of the femur. The knee joint torque (TQ) measured by the dynamometer was converted to muscle force (Fm) by the following equation: Fm = k x TQ x MA; where k is the relative contribution of VL to force production during knee extension, expressed as the percentage of its physiological cross-sectional area (CSA) to that of the quadriceps femoris muscle, 22% (30), and MA is the moment arm length of the quadriceps femoris muscle at the knee joint flexed at an angle of 90°, which was estimated from the thigh length of each subject. In the present study, the Fm and L values above 50% MVC were fitted to a linear regression equation, the slope of which was adopted as an index of the stiffness.
  • Electromyographic Activity: EMG activity was recorded during the measurement of the maximal voluntary isometric strength and tendon properties. Bipolar surface electrodes (5 mm in diameter) were placed over the bellies of VL, RF, vastus medialis (VM), and biceps femoris (BF) muscles with a constant interelectrode distance of 25 mm. Reference electrodes were placed on the lateral tibial condyle. The electrodes were connected to a preamplifier and differential amplifier with a bandwidth of 5–500 Hz (model 1253A; NEC Medical Systems, Tokyo, Japan). The EMG signals were transmitted to a computer at a sampling rate of 1 kHz. The EMG was full-wave rectified and integrated for a 1.0-second period of steady force output for the measurement of MVC to give integrated EMG. In addition, the mean of integrated electromyography in the knee extensors (VL, RF, VM) was defined as mEMG. To investigate the antagonist muscle activity of the BF (coactivation level), the integrated EMG of the BF was measured during knee extension contraction. To determine the maximal activation of the BF, a maximal knee flexion isometric contraction was performed at the same angle (90° of knee joint). The integrated EMG was normalized with respect to the integrated EMG value of BF at the same angle when acting as agonist at maximal effort.
  • Cross-Sectional Area of Muscle and Tendon: Measurements of muscle and tendon CSA were carried out by magnetic resonance imaging. The muscles investigated were: rectus femoris, vastus lateralis, vastus intermedius, and vastus medialis. From the axial image, outlines of each muscle were traced and the traced images were transferred to a computer for CSA calculation using a public domain National Institutes of Health image software package. The average of the muscle CSA at 3 positions (30, 50, and 70% of the femur length) was calculated. In addition, the measurement of patella tendon CSA was taken at the 3 positions: 10, 20, and 30 mm below the patella for the patella tendon. The average of CSA at 3 positions was calculated as the representative of tendon CSA. For the control group (n = 6), the muscle thickness for knee extensors was measured with an ultrasonic apparatus at the anterior surface 50% of the femur length. The muscles involved in the measurement of muscle thickness were rectus femoris and vastus intermedius. In addition, the thickness of patella tendon was measured at 50% of tendon length. It is important to note that MRI was not used to measure muscle and tendon CSAs for control group.
Statistical Analyses:
One-way analysis of variance (ANOVA) with repeated measures was used to detect significant differences in the measured variables. Tukey’s post hoc test of critical difference was used to identify significant differences among means.

Study Strengths / Weaknesses:

One weakness of this study is that MRI was not used to evaluate the control group, but was used on the exercise group. Although the researchers cite evidence that MRI and ultrasound values correlate well to one another, it would have strengthened the study if both groups were evaluated in the same manner.

Another weakness of this study is that it used isometric knee extension as the training method. This is not how athletes in the real world train although it does allow for the much more controlled environment necessary in research. In the future, it will be important to evaluate the use of compound exercises in eliciting adaptations in the muscle and tendon.

Additional References:

  1. Moritani, T and deVries, H. Potential for gross muscle hypertrophy in older men. J Gerontol 1980; 35: 672–682.
  2. Blazevich, AJ, Cannavan, D, Coleman, DR, and Horne, S. Influence of concentric and eccentric resistance training on architectural adaptation in human quadriceps muscles. J Appl Physiol 2007; 103: 1565–1575.
  3. Kubo, K, Kanehisa, H, and Fukunaga, T. Effects of resistance and stretching training programs on the viscoelastic properties of tendon structures in vivo. J Physiol 2002; 538: 219–226.
  4. Narici, MV, Roi, GS, Landoni, L, Minetti, AE, and Cerretelli, P. Changes in force, cross-sectional area and neural activation during strength training and detraining of the human quadriceps. Eur J Appl Physiol 1989; 59: 310–319.
  5. Kubo, K, Akima, H, Ushiyama, J, Tabata, I, Fukuoka, H, Kanehisa, H, and Fukunaga T. Effects of resistance training during bed rest on the viscoelastic properties of tendon structures in lower limb. Scand J Med Sci Sports 2004; 14: 296–302.
  6. Reeves, ND, Maganaris, CN, Ferretti, G, and Narici, MV. Influence of 90-day simulated microgravity on human tendon mechanical properties and effect of resistive countermeasures. J Appl Physiol 2005; 98: 2278–2286.