Muscle-Damaging Exercise Affects Isokinetic Torque More at Short Muscle Length

Abstract

Skurvydas, A, Brazaitis, M, and Kamandulis, S. Muscle-damaging exercise affects isokinetic torque more at short muscle length. J Strength Cond Res 25(5): 1400-1406, 2011-The aim of this study was to investigate the differences in the length-dependent changes in quadriceps muscle torque during voluntary isometric and isokinetic contractions performed after severe muscle-damaging exercise. Thirteen physically active men (age = 23.8 ± 3.2 years, body weight = 77.2 ± 4.5 kg) performed stretch-shortening cycle (SSC) exercise comprising 100 drop jumps with 30-second intervals between each jump. Changes in the voluntary and electrically evoked torque in concentric and isometric conditions at different muscle lengths, muscle soreness, and plasma creatine kinase (CK) activity were assessed within 72 hours after SSC exercise. Isokinetic knee extension torque decreased significantly (p < 0.05) at all joint angles after SSC exercise. At 2 minutes and at 72 hours after SSC exercise, the changes in knee torque were significantly smaller at 80° (where 180° = full knee extension) than at 110-130°. At 2 minutes after SSC exercise, the optimal angle for isokinetic knee extension torque shifted by 9.5 ± 8.9° to a longer muscle length (p < 0.05). Electrically induced torque at low-frequency (20-Hz) stimulation decreased significantly more at a knee joint angle of 130° than at 90°. The subjects felt acute muscle pain and CK activity in the blood increased to 1,593.9 ± 536.2 IU·L⁻¹ within 72 hours after SSC exercise (p < 0.05). This study demonstrates that the effect of muscle-damaging exercise on isokinetic torque is greatest for contractions at short muscle lengths. These findings have practical importance because the movements in most physical activities are dynamic in nature, and the decrease in torque at various points in the range of motion during exercise might affect overall performance.

Introduction

It is generally agreed that disrupted force-bearing structures and damage to the excitation-contraction coupling system are present in the muscle immediately after it has been subjected to a series of eccentric or stretch-shortening cycle (SSC, otherwise called plyometric) exercise (^26,27,35). Symptoms of exercise-induced muscle damage include prolonged impairment of muscle function as measured in voluntary and electrically induced contractions (^{8,12,17,31,33,34}). There is also strong evidence for low-frequency fatigue (LFF) (^28,31,33), protein leakage from injured muscle fibers, and delayed-onset muscle soreness, stiffness, and swelling (^9,31).

Muscle-damaging exercise causes a rightward shift in the optimum joint angle for voluntary isometric strength (^10,21,24). This shift in the optimal angle is thought to reflect an increase in series compliance caused by myofibril disruption involving sarcomere disorganization (²²). Jones et al. (¹⁸) found a transient shift of ∼4° in the optimal joint angle to a longer muscle length during a twitch in resting human triceps surae muscle immediately after eccentric exercise. Chen et al. (¹⁰) found a similar optimal angle shift of ∼4° in isometric contractions after 30 eccentric actions. It was concluded that frequency-dependent length-force characteristics in stimulated muscle reflects a complex interaction of the length-dependent calcium sensitivity, potentiation of the contractile system, distribution of sarcomere length, and interactions between the force exerted and aponeurosis length (²⁹).

The effects of muscle-damaging exercise on the muscle length-torque relationship might be specific to the type of movement. Most athletic events involve dynamic rather than isometric torque. Assuming that performance is related more to dynamic strength than to isometric strength, it is important to understand the effect of muscle damage on the muscle length-torque relationship in dynamic actions. There is some evidence to suggest that the optimal joint angle changes during isokinetic contraction (³⁷). Yeung and Yeung (³⁷) found a significant shift (∼4°) in the peak torque angle to longer muscle lengths (at 60°·s⁻¹) after a submaximal 10-minute stepping eccentric exercise. However, the results obtained after submaximal eccentric exercise may not be representative of events after a demanding high-force, low-intensity SSC protocol (e.g., 100 maximal drop jumps at 30-second intervals).

The purpose of this study was to investigate the differences in length-dependent changes in muscle torque in the quadriceps muscle during voluntary isometric and isokinetic contraction performed after severe muscle-damaging exercise. The second aim was to identify any differences in the length-dependent changes in quadriceps muscle torque during voluntary and electrically induced exercise performed after muscle-damaging exercise. The quadriceps muscle was stimulated electrically to provide an objective measure of the changes in contractile function that are independent of neural factors, such as the individual's motivation and the level of motor unit recruitment (¹⁴).

Methods

Experimental Approach to the Problem

To investigate the length-dependent differences in muscle function after muscle-damaging exercise, the subjects performed the SSC exercise comprising 100 intermittent drop jumps from a height of 0.5 m with a countermovement to a 90° angle in the knee and immediate maximal rebound. The jumps were performed with a 30-second interval between each. The moderate height of the platform was selected to induce muscle damage but allow the subjects to feel comfortable jumping from (³²). The long interval between jumps was chosen to minimize changes in energy metabolites that can affect muscle function. We chose the exercise volume of 100 jumps on the assumption that this is an adequate number of muscle stretches to induce the changes indicative of severe muscle damage. Indicators of muscle damage included decreased voluntary and electrically evoked muscle torque, increased blood creatine kinase (CK) concentration, muscle soreness, and LFF within 3 days after the SSC exercise. These changes served as the dependent variables, and the SSC exercise was the independent variable. The equipment and technique for measuring muscle torque were the same as those reported in a previous study (³¹). Clark et al. (¹¹) observed moderate to high levels of reliability (intraclass correlation coefficients >0.70) of voluntary and evoked force tests similar to those used in our study.

Subjects

Healthy men took part in this study (mean ± SD: age = 23.8 ± 3.2 years, body weight = 77.2 ± 4.5 kg, height = 179.9 ± 3.6 cm, n = 13). The subjects were physically active but did not take part in any formal physical exercise or sport program. They had not been involved in any specific fitness training programs during recent years. Each subject was informed of the experimental risk and signed a written informed consent form before investigation. Approval from the Ethics Committee of Kaunas University of Medicine for use of human subjects was received before data collection.

Procedures

Experimental Protocol

Three to five days before the experiment, the subjects were introduced to the electrical stimulation procedure and the different voluntary tasks. On the experimental day, a blood sample was taken to measure CK activity, and rectal and muscle temperatures were measured. The subject was then seated in the Biodex chair and allowed to rest for 5 minutes, after which the muscle contractile properties were recorded at short and long muscle lengths in the following sequence: 20 Hz (P20), 100 Hz (P100), isometric maximal voluntary contraction (MVC) and isokinetic torque at 30°·s⁻¹. The time interval between each measurement was 1 minute in all cases. Isometric torque at different angles was recorded randomly. This was followed by the SSC exercise protocol comprising 100 drop jumps at an interval of 30 seconds between each from a height of 0.5 m with a countermovement to a 90° angle in the knee and an immediate maximal rebound. During the jumps, the subjects kept their hands on the waist. Jumps were performed using the contact mat (Powertimer Testing System, Newtest, Finland). The height of the jumps was calculated by applying the following formula: H = 1.226 × (Tf)² (m), where Tf = flight time (seconds) (⁵). The subjects received verbal feedback about their performance after each jump and were encouraged to execute the jumps as high as possible. The muscle contractile properties were measured again at 2 minutes and 72 hours after the SSC exercise. Muscle soreness and plasma CK activity were also determined within 72 hours after exercise.

Torque Measurements and Electrical Stimulation

The torque of the knee extensor muscles was measured using an isokinetic dynamometer (System 3; Biodex Medical Systems, Shirley, NY, USA). The sensitivity of the Biodex System 3 in torque measurements is ± 1.36 N·m. The subjects sat upright in the dynamometer chair, and isometric torque was measured during contractions at a knee joint positioned at 130° and again at 90° angle (full knee extension = 180°). Maximal voluntary contraction was reached and maintained for ∼3 seconds before relaxation and was measured twice at each angle; the larger value was used in the analysis. The subjects were carefully instructed to contract the muscle as fast and strongly as possible (¹). The output from the force transducer was also displayed on a voltmeter in front of the subject.

To measure isokinetic concentric torque, 3 continuous repetitions of knee extension were performed at maximal intensity at an angle velocity of 30°·s⁻¹ at a joint angle between 70 and 150°. The knee was set passively at the starting position, and knee flexion was not performed. Isokinetic torque at 80, 90, 100, 110, 120, and 130° and at the optimal knee angles were analyzed, and the changes in the optimal angle were recorded.

The equipment and procedure for electrical stimulation were essentially the same as described previously (³¹). The torque was measured at electrical stimulation at 20 and 100 Hz using 1-second trains of stimuli at the knee angles of 130 and 90° with a 10-second rest interval between the impulses. The change in the P20/P100 ratio after exercise was used to evaluate LFF (^30,32). Direct muscle stimulation was applied using 2 carbonized rubber electrodes covered with a thin layer of electrode gel (Medigel, Modi'in, Israel). One of the electrodes (6 × 11 cm) was placed transversely across the width of the proximal portion of the quadriceps femoris. Another electrode (6 × 20 cm) covered the distal portion of the muscle above the patella. A standard electrical stimulator (MG 440; Medicor, Budapest, Hungary) was used. The electrical stimulation was delivered in square-wave pulses of 0.5-millisecond duration. The tolerance of volunteers to electrical stimulation was assessed on a separate occasion, and only participants who showed good compliance with the procedure were recruited for the study. The intensity of electrical stimulation was selected individually by applying single stimuli to the muscles tested. During this procedure, the voltage was increased until no increment in single-twitch torque could be detected by an additional 10% increase in current strength.

The rate of torque development during isometric MVC (RTDv) and contraction evoked by stimulation at 100-Hz frequency (RTDs) was measured. Contractile RTD was determined as the peak slope of torque per 10 milliseconds (Δ torque/Δ 10 milliseconds). The relative RTD was determined as the RTD normalized relative to maximal torque (% torque per second [1]). The same methods were used to determine rate of torque relaxation during muscle contractions evoked by stimulation at 100-Hz frequency (RTR).

Plasma Creatine Kinase Activity

Approximately 5 ml of blood was drawn from the vena cubiti media of the arm before exercise and 72 hours after exercise. Plasma samples were pipetted into microcentrifuge tubes and stored in a −20° C freezer until analysis. Plasma CK activity (IU·L⁻¹) was determined using an automatic biochemical analyzer (Monarch; Instrumentation Laboratory SpA, USA, and Italy). The normal reference range for men for CK using this method is between 24 and 195 IU·L⁻¹ according to the manual provided with the analyzer.

Muscle Soreness

Muscle soreness was reported subjectively using a visual analog scale from 0 to 10 points. Each number on the scale has descriptive words for soreness: 0 (none), 1 (very slight), 2 (slight), 3 (mild), 4 (less than moderate), 5 (moderate), 6 (more than moderate), 7 (intense), 8 (very intense), 9 (barely tolerable) and 10 (intolerably intense). The participants were required to indicate the severity of soreness in their quadriceps during 2-3 squats at 24, 48, and 72 hours after SSC exercise (³¹).

Rectal and Muscle Temperatures Measurement

Rectal and muscle temperatures were measured before and immediately after SSC. Rectal temperature was measured using a thermocouple (Rectal Probe, Ellab, Hvidovre, Denmark) inserted 12 cm past the anal sphincter. Muscle temperature was measured using a needle microprobe (MKA, Ellab, Hvidovre, Denmark) inserted 3 cm into the vastus lateralis muscle of the left leg.

Statistical Analyses

The descriptive data are presented as mean ± SD. If significant effects were found, post hoc testing involved applying paired t-tests with a Bonferroni correction for multiple comparisons. The level of significance was set at 0.05. Based on an alpha level of 0.05, the sample size (n = 13), SD, and the average level before and after eccentric exercise, the statistical power was calculated for all mechanical indicators. Statistical power in all cases was more than 80%. Cohen's effect size was calculated using the following formula: (d = average of variables before − average of variables after)/SD of variables after.

Results

The average height of last 5 drop jumps decreased by 5.8% ± 7.1% compared with first 5 jumps (p < 0.05) during the SSC exercise (Figure 1). Rectal temperature increased from 37.1 ± 0.4°C before to 39.1 ± 0.4°C (p < 0.05) after the SSC exercise, and muscle temperature increased from 36.7 ± 0.4 to 39.9 ± 0.4°C (p < 0.05). The subjects felt acute muscle pain (8-9 points) 24-48 hours after the SSC exercise; pain decreased significantly at 72 hours (6.5 ± 1.3 points) after SSC. The CK activity in the blood increased from 161.6 ± 122.5 IU·L⁻¹ before the SSC exercise to 1,593.9 ± 536.2 IU·L⁻¹ at 72 hours after the SSC exercise (p < 0.05).

Figure 1: Mean (±SD) height of the drop jumps during 100 repetitions performed with 30-second rest intervals from the 0.5 m-high platform with a countermovement to a knee angle of 90° and immediate maximal rebound.

Before the SSC exercise, MVC, P20, and P100 were significantly greater at a knee angle of 130° than at 90° (Table 1). The voluntary and electrically induced muscle torque decreased significantly and did not recover within 72 hours after the SSC exercise (Figure 2). Low-frequency fatigue was apparent after the SSC exercise because the P20/P100 ratio decreased significantly at both 130 and 90° joint angles after SSC and did not recover within 72 hours. P20 decreased more at the shorter muscle length (130° knee joint angle) than at the longer muscle length (90° knee joint angle) (Figure 3). The relative RTR changed only at 2 minutes after the SSC exercise: RTR increased from 1,560.0 ± 200.6% to 2,110.1 ± 600.0% torque per second at the longer muscle length and from 1,710.0 ± 410.1 to 2,140.4 ± 240.4% torque per second at the shorter muscle length. RTDv and RTDs did not change after the SSC exercise.

Table 1: Pre-exercise values of indices of electrostimulation-induced and voluntary induced contractions of quadriceps muscle (n = 13).^*†

Figure 2: Mean (±SD) torque, in percent, compared with the pre-exercise values of isometric maximal voluntary contraction (MVC), electrically evoked contraction by 100-Hz (P100) and 20-Hz (P20) stimulation, and isokinetic concentric contraction at the optimal angle (ITopt) 2 minutes and 72 hours after 100 drop jumps. Isometric torque was measured with the leg fixed at a knee joint angle of 130 or 90° (where 180° is full knee extension). Significant difference (p < 0.05) between the pre-exercise value (*) or between 130 and 90° (†).

Figure 3: Mean (±SD) ratio of torque at 90 and 130° knee angles during isometric maximal voluntary contraction (MVC), isokinetic concentric contraction (IT), and electrically evoked contraction at 100-Hz (P100) and 20-Hz (P20) stimulation (180° = full knee extension). The variables were measured 2 minutes and 72 hours after the 100 drop jumps. *Significantly different (p < 0.05) from the pre-exercise value.

Isokinetic knee extension torque decreased significantly (p < 0.05) at all angles after the SSC exercise (Figure 4). However, the changes in knee torque were significantly smaller at 80° than at 110-130°. Before the SSC exercise, the optimal angle for knee extension torque was 110.5 ± 4.8°. The optimal angle shifted to a significantly longer muscle length, to a joint angle of 101 ± 8.9° at 2 minutes after the SSC exercise. However, the optimal angle of 106.0 ± 10.2° did not differ from the pre-exercise angle at 72 hours after the SSC exercise.

Figure 4: Mean (±SD) isokinetic knee extension torque at different joint angles, in percent, compared with the pre-exercise level. Torque was measured 2 minutes and 72 hours after the 100-drop jumps. Significant difference (p < 0.05) between the pre-exercise value (*) or the value at a knee angle of 80°.

Discussion

We investigated the length-dependent changes in isokinetic contraction torque after SSC exercise. A larger strength deficit in the quadriceps muscle occurred at the shorter muscle length, and the optimal knee extension torque angle shifted to a significantly longer muscle length during isokinetic contractions immediately after the SSC exercise. The effect of muscle damage on isokinetic contraction torque was similar to the length-dependent effect on isometric torque found in previous studies (^10,21,24). This is relevant for athletes because most movements are dynamic in athletic events and the isokinetic voluntary contraction is more specific to sports than is the isometric contraction.

The exercise protocol has been chosen because it induces only slight changes in energy metabolism in the muscle. Drop jumps with an active phase (when the subject is in contact with the mat) of 0.3-0.4 seconds at 30-second intervals are unlikely to induce significant changes in the content of energy metabolites. Thus, any minor changes in energy metabolism would not be the main cause of the decrease in voluntary and electrically induced muscle performance after the SSC exercise, and we could assume that these were related to exercise-induced muscle damage (^8,12,30,33) and changes in the excitation-contraction coupling system (^26,31,35). The SSC exercise caused indirect signs of muscle damage such as muscle soreness, increased plasma CK activity, decreased height of the drop jump, P20, P100, MVC, isokinetic torque (Figures 1, 2, and 4). These changes were accompanied by shifts in the optimal isokinetic torque angle to a longer muscle length and increased LFF. We estimated the magnitude of damage as severe on the basis of the nearly 40% decrease in MVC, increase in CK activity to 1,600 IU·L⁻¹, and pain ranked close to “intolerably intense” at 72 hours after the SSC exercise. It is of great interest that the decrease in the drop jump was less than the decreases in MVC and isokinetic torque. This finding is consistent with the data of Harrison and Gaffney (¹⁶) who showed that muscle damage significantly affects SSC cycle performance by causing greater decrease in the height of squat compared to the height of drop jumps. Reduction in neuromuscular system performance induced by SSC exercise cannot be attributed to muscle damage alone and might also reflect differences in the modulation of reflexes, stiffness interaction, and compensation by central motor command (²⁰).

The greater decrease in isokinetic torque at the shorter muscle length can be explained partly by a rightward shift in the muscle length-tension relationship. We found a significant shift (9.5 ± 7.3°) of the optimal knee angle in the torque test to a longer muscle length immediately after the SSC exercise. However, the shift in the optimal knee angle was significantly smaller 72 hours after the SSC exercise, whereas the decline in isokinetic torque remained the largest at the shorter muscle length. The rightward shift in the muscle length-tension relationship has been attributed to an increase in the series compliance of the muscle because of disrupted sarcomeres (^15,22,24), and this shift is considered a reliable indicator of both muscle damage (^10,24) and muscle fatigue (⁷). A recent study showed that the shift in peak torque in rabbit hind limb dorsiflexor muscles is caused by a combination of damage and postexercise fatigue (⁶). Other studies show that calcium sensitivity is muscle length dependent (⁴) and that calcium release decreases after eccentric contractions (³). This may increase the magnitude of shift in optimal muscle length. Such calcium-related effects after eccentric contractions may directly reflect the proposed sarcomere disruption. However, the extent to which a shift in optimal angle contributes to a reduction in voluntary torque after exercise will depend on the size of the shift, the test angle chosen, and the shape of the torque-angle relationship for that muscle group.

Yeung and Yeung (³⁷) tested the optimal angle shift during isokinetic contraction (at 60°·s⁻¹). After a 10-minute stepping eccentric exercise, the peak torque angle shifted significantly by ∼4° to a longer muscle length. Chen et al. (¹⁰) found a similar shift in the optimal angle in isometric contraction after 30 eccentric actions. By contrast, we found a greater shift in the optimal angle, by ∼10°, to a longer muscle length. This discrepancy might reflect that our exercise was more intense and may have induced greater muscle damage. Unexpectedly, we found no length-dependent changes in isometric MVC after the SSC exercise, which might be explained by our testing MVC at only 2 joint angles-130 and 90°. These angles place the muscle at close to its optimal length of 110-120° (²⁵) and may not have tested the muscle length-tension relationship fully.

In our study, P20 decreased more than P100 did after the SSC exercise at both the shorter and longer muscle lengths (Figure 2), indicating that the muscles were subjected to LFF, especially at the shorter muscle length. Low-frequency fatigue is characterized by a relative loss of force at low stimulation frequencies, whereas force is impaired only slightly or not at all at high frequencies (^19,28,31). The decreased torque production in muscle cells after SSC exercise might, in principle, be caused by (a) reduced Ca²⁺ release from the sarcoplasmic reticulum leading to decreased free myoplasmic [Ca²⁺] ([Ca²⁺]i), (b) decreased myofibrillar Ca²⁺ sensitivity, and (c) reduced ability of the contractile machinery to produce force (^2,36). In a simplified model, factors (a) and (b) would cause a greater decrease in force at low than at high stimulation frequencies because of the sigmoidal shape of the force-[Ca²⁺]_i relationship, whereas factor (c) would give a similar decrease in force at all stimulation frequencies. We observed markedly greater force reduction after the SSC exercise in muscles stimulated at 20 Hz than at 100 Hz (Figure 2), which supports the important roles of factor (a) and (b) in the SSC-induced force depression. We note, however, that sarcomere instability induced by eccentric contractions can shift the optimal length for active force production to longer lengths, which may exaggerate the force depression at low stimulation frequencies (²³). Our finding that, immediately after the SSC exercise, LFF was greater at the shorter muscle length is interesting and may reflect the observation that muscle damage induces a shift in the optimal muscle torque in the direction of longer muscle lengths (²⁷). However, we did not observe this shift in torque induced by electrostimulation at high frequencies.

It is also interesting that RTR improved after SSC exercise, whereas P20 and P100 decreased significantly (Figure 2). Two main factors might have affected these phenomena: increased muscle temperature or reduced Ca²⁺ release from the sarcoplasmic reticulum leading to decreased ([Ca²⁺]_i. Muscle contraction and relaxation rate both increase with increasing muscle temperature (¹³), and the changes in RTR after SSC might have been diminished by the 3.2° increase in muscle temperature.

The functional significance of length-dependent changes in isokinetic strength after muscle-damaging exercise should not be ignored. The weakest part in the kinetic chain of command leading to muscle contraction can limit overall performance, and an athlete's performance can be affected by the decline in strength at the optimal or weakest part in the range of movement. Thus, the greater damaging effect on muscle function at short quadriceps length might influence the athlete's performance, for example during power squats. One question is whether the changes in length-dependent isokinetic strength at slow velocity observed in our study also apply at higher velocities. Further studies should examine the length-dependent strength changes at high velocities, including changes in cross-bridge attachment and problems with vibration and other artifacts.

In summary, our study showed that drop jumping affects isokinetic torque more at a shorter muscle length and that the changes in knee torque during electrostimulation at low frequency were length dependent. However, the length-dependent effects after severe muscle-damaging exercise were not observed in maximal voluntary isometric contraction torque or torque induced by electrostimulation at high frequency. We tested isometric torque at only 2 joint angles, and these angles may not represent the muscle length-tension relationship fully. The rate of torque relaxation induced by electrostimulation improved after muscle-damaging exercise and did not depend on the length of the muscle tested.

Practical Applications

Coaches and trainers and athletes need to be aware of the impact of exercise-induced muscle damage on the changes in length-related isokinetic torque in dynamic movements. The force decrease in any part of the range of motion during the exercises might affect overall performance. This study demonstrates that the effect of severe muscle-damaging exercises on isokinetic torque is the greatest at short muscle lengths and that the optimal isokinetic torque-angle shifts to a significantly longer muscle length immediately after SSC cycle exercises. Therefore, these findings should be considered when applying this type of exercises and evaluating muscle function at a particular point in time.

Acknowledgments

This study was supported by Lithuanian State Science and Studies Foundation. The authors wish to thank the subjects who volunteered and participated in this study. We state that there is no conflict of interest. We disclose professional relationships with companies or manufacturers who will benefit from the results of the present study and state that the results of the present study do not constitute endorsement of the product by the authors or the National Strength and Conditioning Association. We did not receive any funding from National Institutes of Health, Welcome Trust, Howard Hughes Medical Institute, and others.