Hypertrophic response to unilateral isokinetic resistance training DONA
J. HOUSH,
TERRY
J. HOUSH,
GLEN
concentric
0. JOHNSON,
AND
WEI-KOM
CHU
Department of Oral Biology, College of Dentistry, University of Nebraska Medical Center, Lincoln 685830740; Human Performance Laboratory, University of Nebraska-Lincoln, Lincoln 68588-0229; and Department of Radiology, University of Nebraska Medical Center, Omaha, Nebraska 68105-1045
muscle fiber CSA after concentric isokinetic training. Other investigators (4,9,18,25), however, have found no such increases. The differences in the results of these studies may be due to factors such as genetics or the effect of concentric isokinetic training on strength and cross- training status of the subjects; however, it is likely that sectional area (CSA) of selected extensor and flexor muscles of the discrepancies in findings were due, in part, to differthe forearm and leg, 2) examine the potential for preferential ences in the techniques used to determine muscle CSA. hypertrophy of individual muscles within a muscle group, 3) The most commonly utilized methods for determining identify the location (proximal, middle, or distal level) of hy(6,9,16,18,25,29), muspertrophy within an individual muscle, and 4) determine the muscle CSA are anthropometry cle biopsy (4, 6,8, 12, 16), ultrasound (16), computer-aseffect of unilateral concentric isokinetic training on strength sisted tomography (CAT) scan (26), and magnetic resoand hypertrophy of the contralateral limbs. Thirteen untrained male college students [mean age 25.1 t 6.1 (SD) yr] volunnance imaging (MRI) (3, 19, 21, 22). MRI has distinct teered to perform six sets of 10 repetitions of extension and advantages over the other procedures. For example, MRI flexion of the nondominant limbs three times per week for 8 is especially sensitive for examining soft tissues, such as wk, using a Cybex II isokinetic dynamometer. Pretraining and muscle, and unlike the CAT scan, does not expose the posttraining peak torque and muscle CSA measurements for subject to the hazards of ionizing radiation. Furtherboth the dominant and nondominant limbs were determined utilizing a Cybex II isokinetic dynamometer and magnetic reso- more, it is difficult to precisely identify anatomic landanthropometric measurements, nance imaging scanner, respectively. The results indicated sig- marks for repeated biopsy samples require invasive procedures and are usenificant (P < 0.0008) hypertrophy in all trained muscle groups as well as preferential hypertrophy of individual muscles and at ful in answering certain research questions (for example, specific levels. None of the muscles of the contralateral limbs cell hypertrophy), but may not be representative of the increased significantly in CSA. In addition, significant (P < whole muscle or all muscles within a muscle group, and it 0.0008) increases in peak torque occurred for trained forearm is often difficult to distinguish among tissues to the deextension and flexion as well as trained leg flexion. There were gree necessary for CSA assessment using ultrasound. no significant increases in peak torque, however, for trained leg The sensitivity and safety associated with MRI make it extension or for any movement in the contralateral limbs. especially useful for examining unresolved issues related These data suggest that concentric isokinetic training results to the effects of exercise training on skeletal muscle. For in significant strength and hypertrophic responses in the example, it has not been clearly established if concentric trained limbs. isokinetic training results in preferential hypertrophy of individual muscles within a muscle group or if an individcross-sectional area; strength; cross-training; contralateral; ual muscle hypertrophies to a greater degree at a particumagnetic resonance imaging lar location (proximal, middle, or distal level). In addition, the accurate measurement of muscle CSA using MRI could be used to clarify the mechanisms underlying the cross-training phenomenon that occurs in the contraWHILE CONSTANT external resistance strength training Therefore, has been shown to result in muscular hypertrophy and lateral limb (2,7,12,14,16,17,22,24,27-29). the purposes of this investigation were to use MRI and increased strength (1, 8, 29), the physiological adaptations associated with concentric isokinetic training are Cybex technology to I) determine the effect of concentric isokinetic training on strength and CSA of selected exless clear. Several studies have reported increased tensor and flexor muscles of the forearm and leg, 2) exstrength as a result of concentric isokinetic training (4,6, amine the potential for preferential hypertrophy of indi9, 16, l&22,25); however, the effectiveness of this form of exercise for producing muscular hypertrophy remains vidual muscles within a muscle group, 3) identify the location (proximal, middle, or distal level) of hypertrophy controversial. Recent studies by Coyle et al. (6), Krotwithin an individual muscle, and 4) determine the effect kiewski et al. (16), and Narici et al. (22) have reported of unilateral concentric isokinetic training on strength increased total muscle cross-sectional area (CSA) while Coyle et al. and Krotkiewski et al. also found increased and hypertrophy of the contralateral limbs. HOUSH, DONA J., TERRY J. HOUSH, GLEN 0. JOHNSON, AND WEI-KOM CHU. Hypertrophic response to unilateral concentric isokinetic resistance training. J. Appl. Physiol. 73(l): 65-70, 1992.-The purposes of this study were to 1) determine the
0161-7567/92
$2.00 Copyright 0 1992 the American Physiological
Society
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66
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Subjects. Thirteen adult men [age 25.1 t 6.1 (SD) yr, height 183.8 t 5.4 cm, weight 87.0 t 17.6 kg] volunteered to serve as subjects for this investigation, and informed consent was received before inclusion in the study. The subjects were untrained (not involv red in any regular exercise program) and none had been involved in any type of resistance exercise training in recent years. Because of their inactive lifestyles, these subjects had the most potential for change in strength and CSA. The subjects were asked to refrain from vigorous physical activity, other than the protocol specified by the investigator, for the duration of the study. Determination of strength. All strength testing was performed on a calibrated isokinetic dynamometer (Cybex II, Lumex, Ronkonkoma, NY). Previous studies by Fleck et al. (lo), Mawdsley and Knapik (20), and Nielsen et al. (23) have reported high test-retest reliability for isokinetic leg extension on a Cybex II. In addition, unpublished data from the authors’ laboratory have demonstrated a test-retest (1 wk between tests) reliability coefficient of r = 0.94 for leg extension at 2.09 rad/s using the Cybex II in young male subjects who were similar to those in the present investigation. The subjects were stabilized during practice, testing, and training via straps at the chest and hips or distal thigh for the arm or thigh exercises, respectively. The subjects and the dynamometer were positioned in accordance with the Cybex user’s manual (13), and great care was taken to align the anatomic axis of the joint with the mechanical axis of the dynamometer. After initial instruction and demonstration regarding the use of this device, the subjects were asked to perform a practice set of six repetitions of extension and flexion of the nondominant forearm and leg at 2.09 rad/s to familiarize them with the Cybex II. During this practice session the first two repetitions of each set involved submaximal effort, while the last four repetitions involved maximal effort. The determination of the dominant limb was based on throwing and kicking preference. On a separate day, 24-48 h after the practice session, the subjects were asked to perform one set of three maximal effort repetitions of extension and flexion of the forearm and leg (dominant and nondominant) at 2.09 rad/s. The highest value for each movement was selected as the representative peak torque. The peak torque values were not corrected for gravity, and damping was set at two. The subjects underwent posttraining strength testing in the same manner 1 day after the completion of the 8-wk training period. Determination of muscle CSA. The subjects underwent MRI (General Electric Signa 1.5-T system) for the determination of the CSA of the extensors and fle xors of the dominant and nondominant l forearm a.nd leg. Repetition time and echo time were set at 600 and 20 ms, respectively. Coronal scans were used to determine the distance between the insertion of the deltoid and the inferior border of the medial epicondyle of the humerus, and subsequently three axial scans were taken at an average of -55 (proximal level), 70 (middle level), and 85% (distal level) of this distance to achieve cross sections of the
MUSCULAR
HYPERTROPHY
major forearm extensors and flexors. Similarly, coronal scans of the thighs were utilized to determine the length of the femur from the superior border of the head to the inferior border of the medial condyle. Three axial scans were then taken at ~33 (proximal level), 50 (middle level), and 67% (distal level) of this distance to obtain cross sections of all major leg extensors and flexors (Fig. 1). Because of the difficulty in delineating the individual muscles of the arm, the CSA of the entire forearm extensor and flexor groups were measured. The extensor group was composed of the three heads of the triceps brachii, whereas the flexor group consisted of the biceps brachii and brachialis muscles, in addition to the brachioradialis at the distal level. Muscles of the leg extensor and flexor groups were measured individually and included the muscles of the quadriceps femoris (vastus lateralis, vastus intermedius, vastus medialis, and rectus femoris) and the hamstrings (long head of biceps femoris, semitendinosus, and semimembranosus), respectively. For each axial scan, CSA computation was accomplished by projecting the image onto a data viewing screen and tracing the outline of each muscle or muscle group with the magnifying cursor of the traverse arm of a digitizer. (model 1224, Numonics Digitizer, Montgomery, PA). The “area” function of the digitizer was utilized to calculate the CSA of each muscle group or individual muscle. During a pilot study, the test-retest reliability for repeated CSA measurements on 10 subjects was found to be r = 0.996. The subjects underwent posttraining determination of muscle CSA in the same manner 1 day after the posttest for muscular strength. Warm-up. A 6-min warm-up preceded all practice, testing, and training sessions. This consisted of 3 min of submaximal arm cranking (at 0.25 kp) and 3 min of submaximal cycle ergometery (at 0.50 kp). Training. Training was performed three times per week for 8 wk. Each session consisted of six sets of 10 repetitions of extension and flexion of the nondominant forearm and leg at 2.09 rad/s. Two-minute rest periods were allowed between sets. This training velocity was the same as that of Narici et al. (22). Statistical anaZysis. It was the intent of this investigation to examine the effect of the isokinetic exercise on each muscle or muscle group (forearm extensors, forearm flexors, vastus lateralis, vastus intermedius, vastus medialis, rectus femoris, biceps femoris, semitendinosus, and semimembranosus) at each level (proximal, middle and distal) for both the trained and untrained limbs (arms and thighs). This resulted in 52 comparisons for hypertrophy plus eight strength measures (peak torque for extension and flexion of the trained and untrained, forearms and legs). Thus there were 60 planned comparisons that were decided on before the initiation of this investigation. With respect to planned comparisons, are usually deKeppel (15) has stated, “Experiments signed with specific hypotheses in mind, and most researchers conduct analyses relevant to these hypotheses directly without reference to the outcome of the omnibus F test.” Furthermore, Keppel has stated, “Most research begins with the formulation of one or more research hypotheses-statements about how behavior will be in-
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67
FIG. 1. Axial magnetic resonance imaging scans of extensor and flexor muscles of forearm (left) and leg (right), showing proximal (A), middle (B), and distal (C) anatomic cross sections.
fluenced if such and such treatment differences are manipulated. Experiments are designed specifically to test these particular research hypotheses. Most typically it is possible to design an experiment that will provide information relevant to several research hypotheses. Tests designed to shed light on these particular questions are planned before the start of an experiment and clearly represent the primary focus of analysis. A researcher is not interested in the omnibus F test-this test is more appropriate in the absence of specific hypotheses. Thus, most researchers form, or at least imply, an analysis plan when they specify their research hypotheses and design experiments to test them. This plan consists of a set of analytical comparisons chosen to extract information that is critical to the status of the research questions responsible for the initiation of the experiment in the first place. As you will see, analytical comparisons can be
conducted directly on a set of data without reference to the significance or nonsignificances of the omnibus F test.” Because the present investigation was designed with specific planned comparisons in mind, differences in peak torque and CSA across training were determined using paired t tests. To control for the possibility of alpha inflation, the Bonferroni adjustment (15) was used and resulted in a per comparison alpha of P < 0.0008(0.05/ 60). This decision was consistent with the recommendation of Keppel: “If the number of planned comparisons exceeds the number of degrees of freedom associated with the overall treatment mean square, I suggest the use of the modified Bonferroni test to maintain the family wise error for planned comparisons. . . . ” It should be recognized, however, that the Bonferroni adjustment (15) is a conservative correction for the potential alpha inflation. Therefore, although the risk of committing a
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TABLE 1. Changes in isokinetic strength Pretraining,
Trained FE FF Contralateral FE FF Trained LE LF Contralateral LE LF
N. m
Posttraining,
N m l
%Change
50.0t10.4 49.6-t-9.9
68.0tll.O 59.8t8.8
36.0* 20.6*
52.8-kl3.0 55.9t11.9
60.5t13.5 61.9k11.8
14.6 10.6
180.8t29.2 115.2t25.9
2Ol.Ok38.9 140.2k29.8
11.2 21.7*
185.2t29.6 114.2t21.8
197.6k30.6 131.1t23.0
6.7 14.8
Values are means t SD for 13 subjects. FE, forearm extensors; FF, forearm flexors; LE, leg extensors; LF, leg flexors. * P < 0.0008.
type I error across all comparisons is maintained at P < 0.05, there is an increased risk of committing a type II error. Thus, in the present investigation, the use of the Bonferroni adjustment (15) allows for a high degree of confidence in the statistically significant findings but also increases the possibility that significant changes went undetected. RESULTS Strength. The results indicated significant increases in peak torque across training for all movements on the trained side of the body except leg extension. There were no significant changes in peak torque in the contralateral limbs (Table 1). Muscle CSA. Significant differences in CSA were found across training for the trained forearm extensors (proximal and middle levels) as well as for the trained forearm flexors (all three levels). The training did not result in significant changes in the CSA of the contralatera1 forearm extensors or flexors. For the trained leg extensors, only the rectus femoris (all three levels), vastus lateralis (middle level), and vastus intermedius (middle level) increased in CSA. The contralateral leg extensors showed no significant changes in CSA for any muscle. The trained leg flexors showed significant increases in CSA for the semitendinosus (all three levels) and biceps femoris (middle level). There were no significant changes in the CSA of any of the contralateral leg flexors (Table 2). DISCUSSION
The results of this study demonstrated hypertrophy (8.0-34.4%) of the individual muscles of all muscle groups of the trained limbs. These findings were consistent with those of Krotkiewski et al. (16), Coyle et al. (6), and Narici et al. (22), who also reported hypertrophy in trained limbs after concentric isokinetic training. The muscular hypertrophy exhibited in the present investigation is especially noteworthy because it resulted from isokinetic training without eccentric contractions. This is in contrast to Cote et al. (5), who postulated that the absence of a hypertrophic response in their investigation may have been due to the lack of an eccentric component in the training protocol. Therefore, the concept that an
HYPERTROPHY
eccentric phase of contraction is necessary for muscular hypertrophy does not appear to be valid for isokinetic training in untrained men. Previous investigations by Lesmes et al. (18), Costill et al. (4), Pearson and Costill (25), and Duncan et al. (9) found no hypertrophy after concentric isokinetic training. Many of the techniques used in these studies, however, such as anthropometry (6,9,16,18,25,29), muscle biopsy (4, 6, 8, 12, 16), ultrasound (16), and CAT scan (26) may not have been sensitive to changes in muscle CSA. The MRI technique utilized in the present investigation and that of Narici et al. (22) provided precise images that were easily measured for highly accurate quantification of muscle CSA. In addition, the results of this study indicated preferential hypertrophy of individual muscles within a muscle group as well as at specific levels within an individual muscle. Narici et al. (22) reported preferential hypertrophy of the vastus intermedius at the proximal onethird of the femur and the rectus femoris at the midfemur level only. In the present investigation, the rectus femoris increased in CSA at all three levels, whereas the vastus lateralis and vastus intermedius increased at the middle (midfemur) level only. The reasons for the differences in the findings of these studies are unclear because the training protocols were similar. Narici et al., however, trained the dominant thigh while the nondominant thigh was trained in the present investigation. It is likely that the muscles of the nondominant thigh were less trained at the beginning of this study and therefore were more responsive to the training stimulus than those of the dominant thigh trained in the study of Narici et al. Future investigations should address this hypothesis by training both the dominant and nondominant limbs and examining differences in the patterns of hypertrophy. Preferential hypertrophy of individual quadriceps muscles may also be a function of their level of activation during isokinetic contraction (22). Narici et al. (22) described unpublished observations in which integrated electromyography was used to simultaneously examine the activation patterns of the vastus medialis, rectus femoris and vastus lateralis during isokinetic leg extension at 2.09 rad/s. Their information indicated that the vastus medialis exhibited the highest level of activation, followed by 30% less for the rectus femoris and 60% less for the vastus lateralis. No information was presented for the vastus intermedius. With respect to hypertrophy, Narici et al. stated, “This study has shown a preferential hypertrophy of the VM (vastus medialis) and VI (vastus intermedius) as compared to that of R (rectus femoris) and VL (vastus lateralis) muscles.” These authors (22) suggested that the degree of hypertrophy was related to the level of activation. In the present study, however, the rectus femoris of the trained leg hypertrophied to a greater extent than the other quadriceps muscles (Table 2). Thus the existence of a causative relationship between the level of activation during contractions and the degree of hypertrophy exhibited as a result of training remains speculative. There have been no studies before the present investigation that have used MRI technology to examine the effect of concentric isokinetic training on hypertrophy in
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ISOKINETIC TABLE
TRAINING
AND MUSCULAR
69
HYPERTROPHY
2. Changes in muscle cross-sectional area Proximal Pretraining
Trained FE FF Contralateral FE FF Trained LE VL VI VM RF Contralateral LE VL VI VM RF Trained LF BF ST SM Contralateral LF BF ST SM
Level, cm2
Posttraining
Middle %Change
Pretraining
Level, cm2
Posttraining
Distal %Change
Pretraining
Level, cm2
Posttraining
%Change
22.8 14.8
25.7 17.0
12.4* 14.4*
17.2 19.9
20.3 22.1
17.7* 11.0*
9.3 20.9
10.7 23.5
14.6 12.2”
24.9 15.3
24.1 16.2
-3.0 6.2
17.3 20.2
17.3 20.6
-0.3 2.0
10.8 22.9
10.3 23.2
-4.6 1.1
19.6 16.4 4.1 9.6
19.8 17.5 4.4 10.9
1.1 6.7 7.8 13.1*
23.7 22.8 9.0 6.1
25.6 24.6 10.6 7.5
i3.0* 8.0* 17.0 22.0*
14.7 16.3 16.3 1.5
16.7 17.5 17.9 2.1
13.4 7.6 9.9 34.4*
18.8 17.5 5.8 10.1
18.7 17.5 5.5 10.8
-0.8 0.1 -4.8 6.6
23.2 24.3 11.4 7.3
23.8 24.9 11.6 7.8
2.6 2.5 1.5 6.7
14.6 16.1 18.9 1.8
16.0 16.3 19.4 2.0
9.6 1.1 2.6 14.0
1.3 4.9
1.6 6.0
23.3 21.7*
8.0 7.2 3.2
9.2 9.0 3.8
15.0* 25.9* 19.9
9.5 4.9 9.4
10.6 6.1 10.0
11.9 24.2* 6.8
1.1 5.1
1.1 5.6
1.8 10.5
8.2 7.4 3.2
8.7 8.1 3.5
7.0 9.1 7.5
9.4 5.1 9.9
9.2 5.3 10.2
-2.2 3.1 2.6
Values are means for 13 subjects. VL, vastus lateralis; VI, vastus semitendinosus; SM, semimembranosus. * P < 0.0008.
intermedius;
the muscles associated with forearm extension, forearm flexion, or leg flexion. The results of the present investigation indicated that each of these muscle groups demonstrated preferential hypertrophy of particular muscles within the muscle groups and at specific levels (proximal, middle, and/or distal). Interestingly, the semitendinosus, which is closest to the midsagittal line of the thigh, demonstrated the greatest degree of hypertrophy of the leg flexors. In addition, the biceps femoris, which is lateral at the distal end of the femur and becomes closer to the midline of the thigh as it reaches the midfemur level, exhibited hypertrophy at the middle level only. These findings, in addition to the increases in the CSA of the rectus femoris at all three levels, suggest that muscles nearest the midsagittal line of the segment may be positioned such that they receive more training stimulus than muscles which are located more medially or laterally. Only two previous studies (16, 22) have investigated the effect of unilateral concentric isokinetic training on the muscle CSA of the contralateral limb (cross-training effect) and both examined only the leg extensors. Krotkiewski et al. (16) utilized ultrasound, thigh circumferences and muscle biopsies while Narici et al. (22) used MRI technology to determine muscle CSA and neither found a cross-training effect with regard to hypertrophy. The results of the present investigation were consistent with these findings for all muscles of the contralateral side, It is interesting to note, however, that although no muscles on the contralateral side of the body demonstrated statistically significant (P > 0.0008) hypertrophy, most (forearm flexors, vastus lateralis, vastus intermedius, vastus medialis, rectus femoris, biceps femoris, semitendinosus, and semimembranosus) increased in CSA
VM,
vastus
medialis;
RF,
r&us
femoris;
BF,
bicepsfemoris; ST,
(0.1 to 14.0%) as a result of the training. In addition, although none of the changes was statistically significant (P > 0.0008), peak torque for all movements on the contralateral side of the body also increased (6.7 to 14.8%). Given the consistency of the increases in peak torque and CSA in the contralateral limbs as well as the accuracy of the Cybex II and MRI techniques, it is unlikely that these findings were due to chance or instrumentation. Furthermore, many of the increases in peak torque and CSA in the contralateral limbs were greater than those that have been reported for inactive adult male control groups (6,9, 26). Although it is not likely that adult males would hypertrophy or increase in strength as a result of 8 wk of inactivity, future studies should consider utilizing a control group in addition to the experimental group to further examine this issue. The refore 9 th .e trend (al though sign& ant) towa .rd increased muscle not statistically CSA and strength on the contralateral side of the body suggested some cross-training effect as a result of unilateral concentric isokinetic training. Hellebrandt (11) proposed two possible mechanisms to explain the crosstraining effect: 1) diffusion of motor impulses to the contralateral side of the body and 2) contraction of the musculature on the contralateral side of the body to maintain balance and assume the proper position for the unilateral exercise. It is possible that a longer period of training may have resulted in statistically significant increases in strength and CSA on the contralateral side. In summary, the results of the present investigation indicated that concentric isokinetic training resulted in 1) muscular hypertrophy o f the exten sor and flexor muscles of the trained forearm and leg; 2) preferential hypertrophy of individual extensor and flexor muscles of the trained leg; 3) preferential hypertrophy at specific levels
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of the forearm extensors, vastus lateralis, vastus intermedius, and biceps femoris of the trained limbs; and 4) no significant cross-training effect with regard to strength or CSA. The authors thank the University of Nebraska Medical Center for the support given to this project, Drs. Phoebe Kaplan and Warren Stinson for invaluable expertise, and Dr. Sharon Evans for the use of digitizing equipment and assistance with the cross-sectional area measurement process. In addition, the authors thank Sheila Thomas and Michelle Satterlee for technical assistance in the acquisition of magnetic resonance images and Lori Harrison and Edna Manning for help in the preparation of the manuscript. The authors especially thank all the men who volunteered for this study. Address for reprint requests: D. J. Housh, 5lA Dent, UNMC College of Dentistry, Lincoln, NE 68583-0740.
HYPERTROPHY
bolic capacity during strength training and detraining: a one leg model. Eur. J. Appl. Physiol. Occup. Physiol. 51: 25-35, 1983.
13* Isolated II and
Joint U.B.X.
Testing and Exercise: A Handbook for Using the Cybex T. Ronkonkoma, NY: Cybex, Div. of Lumex, 1981, p.
51-52,69-70. D. A., AND 0. M. RUTHERFORD. Human muscle strength training: the effects of three different regimes and the nature of the resultant changes. J. Physiol. Lond. 391: l-11, 1987. KEPPEL, G. Design and Analysis: A Researcher’s Handbook (2nd ed). Englewood Cliffs, NJ: Prentice-Hall, 1982, p. 106, 146-149, 165. KROTKIEWSKI, M., A. ANIANSSON, G. GRIMBY, P. BJORNTORP, AND L. SJOSTROM. The effect of unilateral isokinetic strength traiing on local adipose and muscle tissue morphology, thickness, and enzymes. Eur. J. Appl. Physiol. Occup. Physiol. 42: 271-281, 1979. KRUSE, R. D., AND D. K. MATHEWS. Bilateral effects of unilateral exercise: experimental study based on 120 subjects. Arch. Phys.
14. JONES,
15 l
16 ’ 17 .
Received 22 July 1991; accepted in final form 24 January 1992.
Med. RehabiZ. 18. LESMES, G.
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V., G. S. ROI, L. LANDONI, A. E. MINETTI, AND P. Changes in force, cross-sectional area and neural activation during strength training and detraining of the human quadriceps. Eur. J. Appl. Physiol. Occup. Physiol. 59: 310-319, 1989. NIELSEN, D. H., E. V. HELLWIG, K. L. SWANSON, B. A. MILLER, K. LEO, AND R. F. WOOLSON. Measurement reliability of isokinetic strength (Abstract). Phys. Ther. 66: 804, 1986. PARKER, R. H. The effects of mild one-legged isometric or dynamic training. Eur. J. Appl. Physiol. Occup. Physiol. 54: 262-268, 1985. PEARSON, D. R., AND D. L. COSTILL. The effects of constant external resistance exercise and isokinetic exercise training on work-induced hypertrophy. J. Appl. Sport Sci. Res. 2: 39-41, 1988. PETERSON, S. R., K. M. BAGNAL, H. A. WENGER, D. C. REID, W. R. CASTOR, AND H. A. QUINNEY. The influence of velocity-specific resistance training on the in vivo torque velocity relationship and the cross-sectional area of quadriceps femoris. J. Orthop. Sports
Phys. Ther. 10: 456-462, 1989. 27. ROSE, D. L., S. F. RADZYMINSKI,
AND R. R. BEATTY. Effect of brief maximal exercise on the strength of the quadriceps femoris. Arch.
28.
Phys. Med. STEVENS,
Rehabil.
38: 157-164,
1957.
C. J., D. L. COSTILL, D. BENHAM, AND T. WHITEHEAD. Transfer of gains in muscle strength and endurance following unilateral isokinetic training (Abstract). Med. Sci. Sports Exercise 12: 121,198O.
29. WILMORE, J. H. Alterations in strength, body composition and anthropometric measurements consequent to a lo-week weight training program. Med. Sci. Sports 6: 133-138, 1974.
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J. HOUSH,
TERRY
J. HOUSH,
GLEN
concentric
0. JOHNSON,
AND
WEI-KOM
CHU
Department of Oral Biology, College of Dentistry, University of Nebraska Medical Center, Lincoln 685830740; Human Performance Laboratory, University of Nebraska-Lincoln, Lincoln 68588-0229; and Department of Radiology, University of Nebraska Medical Center, Omaha, Nebraska 68105-1045
muscle fiber CSA after concentric isokinetic training. Other investigators (4,9,18,25), however, have found no such increases. The differences in the results of these studies may be due to factors such as genetics or the effect of concentric isokinetic training on strength and cross- training status of the subjects; however, it is likely that sectional area (CSA) of selected extensor and flexor muscles of the discrepancies in findings were due, in part, to differthe forearm and leg, 2) examine the potential for preferential ences in the techniques used to determine muscle CSA. hypertrophy of individual muscles within a muscle group, 3) The most commonly utilized methods for determining identify the location (proximal, middle, or distal level) of hy(6,9,16,18,25,29), muspertrophy within an individual muscle, and 4) determine the muscle CSA are anthropometry cle biopsy (4, 6,8, 12, 16), ultrasound (16), computer-aseffect of unilateral concentric isokinetic training on strength sisted tomography (CAT) scan (26), and magnetic resoand hypertrophy of the contralateral limbs. Thirteen untrained male college students [mean age 25.1 t 6.1 (SD) yr] volunnance imaging (MRI) (3, 19, 21, 22). MRI has distinct teered to perform six sets of 10 repetitions of extension and advantages over the other procedures. For example, MRI flexion of the nondominant limbs three times per week for 8 is especially sensitive for examining soft tissues, such as wk, using a Cybex II isokinetic dynamometer. Pretraining and muscle, and unlike the CAT scan, does not expose the posttraining peak torque and muscle CSA measurements for subject to the hazards of ionizing radiation. Furtherboth the dominant and nondominant limbs were determined utilizing a Cybex II isokinetic dynamometer and magnetic reso- more, it is difficult to precisely identify anatomic landanthropometric measurements, nance imaging scanner, respectively. The results indicated sig- marks for repeated biopsy samples require invasive procedures and are usenificant (P < 0.0008) hypertrophy in all trained muscle groups as well as preferential hypertrophy of individual muscles and at ful in answering certain research questions (for example, specific levels. None of the muscles of the contralateral limbs cell hypertrophy), but may not be representative of the increased significantly in CSA. In addition, significant (P < whole muscle or all muscles within a muscle group, and it 0.0008) increases in peak torque occurred for trained forearm is often difficult to distinguish among tissues to the deextension and flexion as well as trained leg flexion. There were gree necessary for CSA assessment using ultrasound. no significant increases in peak torque, however, for trained leg The sensitivity and safety associated with MRI make it extension or for any movement in the contralateral limbs. especially useful for examining unresolved issues related These data suggest that concentric isokinetic training results to the effects of exercise training on skeletal muscle. For in significant strength and hypertrophic responses in the example, it has not been clearly established if concentric trained limbs. isokinetic training results in preferential hypertrophy of individual muscles within a muscle group or if an individcross-sectional area; strength; cross-training; contralateral; ual muscle hypertrophies to a greater degree at a particumagnetic resonance imaging lar location (proximal, middle, or distal level). In addition, the accurate measurement of muscle CSA using MRI could be used to clarify the mechanisms underlying the cross-training phenomenon that occurs in the contraWHILE CONSTANT external resistance strength training Therefore, has been shown to result in muscular hypertrophy and lateral limb (2,7,12,14,16,17,22,24,27-29). the purposes of this investigation were to use MRI and increased strength (1, 8, 29), the physiological adaptations associated with concentric isokinetic training are Cybex technology to I) determine the effect of concentric isokinetic training on strength and CSA of selected exless clear. Several studies have reported increased tensor and flexor muscles of the forearm and leg, 2) exstrength as a result of concentric isokinetic training (4,6, amine the potential for preferential hypertrophy of indi9, 16, l&22,25); however, the effectiveness of this form of exercise for producing muscular hypertrophy remains vidual muscles within a muscle group, 3) identify the location (proximal, middle, or distal level) of hypertrophy controversial. Recent studies by Coyle et al. (6), Krotwithin an individual muscle, and 4) determine the effect kiewski et al. (16), and Narici et al. (22) have reported of unilateral concentric isokinetic training on strength increased total muscle cross-sectional area (CSA) while Coyle et al. and Krotkiewski et al. also found increased and hypertrophy of the contralateral limbs. HOUSH, DONA J., TERRY J. HOUSH, GLEN 0. JOHNSON, AND WEI-KOM CHU. Hypertrophic response to unilateral concentric isokinetic resistance training. J. Appl. Physiol. 73(l): 65-70, 1992.-The purposes of this study were to 1) determine the
0161-7567/92
$2.00 Copyright 0 1992 the American Physiological
Society
65
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66
ISOKINETIC
TRAINING
AND
METHODS
Subjects. Thirteen adult men [age 25.1 t 6.1 (SD) yr, height 183.8 t 5.4 cm, weight 87.0 t 17.6 kg] volunteered to serve as subjects for this investigation, and informed consent was received before inclusion in the study. The subjects were untrained (not involv red in any regular exercise program) and none had been involved in any type of resistance exercise training in recent years. Because of their inactive lifestyles, these subjects had the most potential for change in strength and CSA. The subjects were asked to refrain from vigorous physical activity, other than the protocol specified by the investigator, for the duration of the study. Determination of strength. All strength testing was performed on a calibrated isokinetic dynamometer (Cybex II, Lumex, Ronkonkoma, NY). Previous studies by Fleck et al. (lo), Mawdsley and Knapik (20), and Nielsen et al. (23) have reported high test-retest reliability for isokinetic leg extension on a Cybex II. In addition, unpublished data from the authors’ laboratory have demonstrated a test-retest (1 wk between tests) reliability coefficient of r = 0.94 for leg extension at 2.09 rad/s using the Cybex II in young male subjects who were similar to those in the present investigation. The subjects were stabilized during practice, testing, and training via straps at the chest and hips or distal thigh for the arm or thigh exercises, respectively. The subjects and the dynamometer were positioned in accordance with the Cybex user’s manual (13), and great care was taken to align the anatomic axis of the joint with the mechanical axis of the dynamometer. After initial instruction and demonstration regarding the use of this device, the subjects were asked to perform a practice set of six repetitions of extension and flexion of the nondominant forearm and leg at 2.09 rad/s to familiarize them with the Cybex II. During this practice session the first two repetitions of each set involved submaximal effort, while the last four repetitions involved maximal effort. The determination of the dominant limb was based on throwing and kicking preference. On a separate day, 24-48 h after the practice session, the subjects were asked to perform one set of three maximal effort repetitions of extension and flexion of the forearm and leg (dominant and nondominant) at 2.09 rad/s. The highest value for each movement was selected as the representative peak torque. The peak torque values were not corrected for gravity, and damping was set at two. The subjects underwent posttraining strength testing in the same manner 1 day after the completion of the 8-wk training period. Determination of muscle CSA. The subjects underwent MRI (General Electric Signa 1.5-T system) for the determination of the CSA of the extensors and fle xors of the dominant and nondominant l forearm a.nd leg. Repetition time and echo time were set at 600 and 20 ms, respectively. Coronal scans were used to determine the distance between the insertion of the deltoid and the inferior border of the medial epicondyle of the humerus, and subsequently three axial scans were taken at an average of -55 (proximal level), 70 (middle level), and 85% (distal level) of this distance to achieve cross sections of the
MUSCULAR
HYPERTROPHY
major forearm extensors and flexors. Similarly, coronal scans of the thighs were utilized to determine the length of the femur from the superior border of the head to the inferior border of the medial condyle. Three axial scans were then taken at ~33 (proximal level), 50 (middle level), and 67% (distal level) of this distance to obtain cross sections of all major leg extensors and flexors (Fig. 1). Because of the difficulty in delineating the individual muscles of the arm, the CSA of the entire forearm extensor and flexor groups were measured. The extensor group was composed of the three heads of the triceps brachii, whereas the flexor group consisted of the biceps brachii and brachialis muscles, in addition to the brachioradialis at the distal level. Muscles of the leg extensor and flexor groups were measured individually and included the muscles of the quadriceps femoris (vastus lateralis, vastus intermedius, vastus medialis, and rectus femoris) and the hamstrings (long head of biceps femoris, semitendinosus, and semimembranosus), respectively. For each axial scan, CSA computation was accomplished by projecting the image onto a data viewing screen and tracing the outline of each muscle or muscle group with the magnifying cursor of the traverse arm of a digitizer. (model 1224, Numonics Digitizer, Montgomery, PA). The “area” function of the digitizer was utilized to calculate the CSA of each muscle group or individual muscle. During a pilot study, the test-retest reliability for repeated CSA measurements on 10 subjects was found to be r = 0.996. The subjects underwent posttraining determination of muscle CSA in the same manner 1 day after the posttest for muscular strength. Warm-up. A 6-min warm-up preceded all practice, testing, and training sessions. This consisted of 3 min of submaximal arm cranking (at 0.25 kp) and 3 min of submaximal cycle ergometery (at 0.50 kp). Training. Training was performed three times per week for 8 wk. Each session consisted of six sets of 10 repetitions of extension and flexion of the nondominant forearm and leg at 2.09 rad/s. Two-minute rest periods were allowed between sets. This training velocity was the same as that of Narici et al. (22). Statistical anaZysis. It was the intent of this investigation to examine the effect of the isokinetic exercise on each muscle or muscle group (forearm extensors, forearm flexors, vastus lateralis, vastus intermedius, vastus medialis, rectus femoris, biceps femoris, semitendinosus, and semimembranosus) at each level (proximal, middle and distal) for both the trained and untrained limbs (arms and thighs). This resulted in 52 comparisons for hypertrophy plus eight strength measures (peak torque for extension and flexion of the trained and untrained, forearms and legs). Thus there were 60 planned comparisons that were decided on before the initiation of this investigation. With respect to planned comparisons, are usually deKeppel (15) has stated, “Experiments signed with specific hypotheses in mind, and most researchers conduct analyses relevant to these hypotheses directly without reference to the outcome of the omnibus F test.” Furthermore, Keppel has stated, “Most research begins with the formulation of one or more research hypotheses-statements about how behavior will be in-
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ISOKINETIC
TRAINING
AND MUSCULAR
HYPERTROPHY
67
FIG. 1. Axial magnetic resonance imaging scans of extensor and flexor muscles of forearm (left) and leg (right), showing proximal (A), middle (B), and distal (C) anatomic cross sections.
fluenced if such and such treatment differences are manipulated. Experiments are designed specifically to test these particular research hypotheses. Most typically it is possible to design an experiment that will provide information relevant to several research hypotheses. Tests designed to shed light on these particular questions are planned before the start of an experiment and clearly represent the primary focus of analysis. A researcher is not interested in the omnibus F test-this test is more appropriate in the absence of specific hypotheses. Thus, most researchers form, or at least imply, an analysis plan when they specify their research hypotheses and design experiments to test them. This plan consists of a set of analytical comparisons chosen to extract information that is critical to the status of the research questions responsible for the initiation of the experiment in the first place. As you will see, analytical comparisons can be
conducted directly on a set of data without reference to the significance or nonsignificances of the omnibus F test.” Because the present investigation was designed with specific planned comparisons in mind, differences in peak torque and CSA across training were determined using paired t tests. To control for the possibility of alpha inflation, the Bonferroni adjustment (15) was used and resulted in a per comparison alpha of P < 0.0008(0.05/ 60). This decision was consistent with the recommendation of Keppel: “If the number of planned comparisons exceeds the number of degrees of freedom associated with the overall treatment mean square, I suggest the use of the modified Bonferroni test to maintain the family wise error for planned comparisons. . . . ” It should be recognized, however, that the Bonferroni adjustment (15) is a conservative correction for the potential alpha inflation. Therefore, although the risk of committing a
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68
ISOKINETIC
TRAINING
AND MUSCULAR
TABLE 1. Changes in isokinetic strength Pretraining,
Trained FE FF Contralateral FE FF Trained LE LF Contralateral LE LF
N. m
Posttraining,
N m l
%Change
50.0t10.4 49.6-t-9.9
68.0tll.O 59.8t8.8
36.0* 20.6*
52.8-kl3.0 55.9t11.9
60.5t13.5 61.9k11.8
14.6 10.6
180.8t29.2 115.2t25.9
2Ol.Ok38.9 140.2k29.8
11.2 21.7*
185.2t29.6 114.2t21.8
197.6k30.6 131.1t23.0
6.7 14.8
Values are means t SD for 13 subjects. FE, forearm extensors; FF, forearm flexors; LE, leg extensors; LF, leg flexors. * P < 0.0008.
type I error across all comparisons is maintained at P < 0.05, there is an increased risk of committing a type II error. Thus, in the present investigation, the use of the Bonferroni adjustment (15) allows for a high degree of confidence in the statistically significant findings but also increases the possibility that significant changes went undetected. RESULTS Strength. The results indicated significant increases in peak torque across training for all movements on the trained side of the body except leg extension. There were no significant changes in peak torque in the contralateral limbs (Table 1). Muscle CSA. Significant differences in CSA were found across training for the trained forearm extensors (proximal and middle levels) as well as for the trained forearm flexors (all three levels). The training did not result in significant changes in the CSA of the contralatera1 forearm extensors or flexors. For the trained leg extensors, only the rectus femoris (all three levels), vastus lateralis (middle level), and vastus intermedius (middle level) increased in CSA. The contralateral leg extensors showed no significant changes in CSA for any muscle. The trained leg flexors showed significant increases in CSA for the semitendinosus (all three levels) and biceps femoris (middle level). There were no significant changes in the CSA of any of the contralateral leg flexors (Table 2). DISCUSSION
The results of this study demonstrated hypertrophy (8.0-34.4%) of the individual muscles of all muscle groups of the trained limbs. These findings were consistent with those of Krotkiewski et al. (16), Coyle et al. (6), and Narici et al. (22), who also reported hypertrophy in trained limbs after concentric isokinetic training. The muscular hypertrophy exhibited in the present investigation is especially noteworthy because it resulted from isokinetic training without eccentric contractions. This is in contrast to Cote et al. (5), who postulated that the absence of a hypertrophic response in their investigation may have been due to the lack of an eccentric component in the training protocol. Therefore, the concept that an
HYPERTROPHY
eccentric phase of contraction is necessary for muscular hypertrophy does not appear to be valid for isokinetic training in untrained men. Previous investigations by Lesmes et al. (18), Costill et al. (4), Pearson and Costill (25), and Duncan et al. (9) found no hypertrophy after concentric isokinetic training. Many of the techniques used in these studies, however, such as anthropometry (6,9,16,18,25,29), muscle biopsy (4, 6, 8, 12, 16), ultrasound (16), and CAT scan (26) may not have been sensitive to changes in muscle CSA. The MRI technique utilized in the present investigation and that of Narici et al. (22) provided precise images that were easily measured for highly accurate quantification of muscle CSA. In addition, the results of this study indicated preferential hypertrophy of individual muscles within a muscle group as well as at specific levels within an individual muscle. Narici et al. (22) reported preferential hypertrophy of the vastus intermedius at the proximal onethird of the femur and the rectus femoris at the midfemur level only. In the present investigation, the rectus femoris increased in CSA at all three levels, whereas the vastus lateralis and vastus intermedius increased at the middle (midfemur) level only. The reasons for the differences in the findings of these studies are unclear because the training protocols were similar. Narici et al., however, trained the dominant thigh while the nondominant thigh was trained in the present investigation. It is likely that the muscles of the nondominant thigh were less trained at the beginning of this study and therefore were more responsive to the training stimulus than those of the dominant thigh trained in the study of Narici et al. Future investigations should address this hypothesis by training both the dominant and nondominant limbs and examining differences in the patterns of hypertrophy. Preferential hypertrophy of individual quadriceps muscles may also be a function of their level of activation during isokinetic contraction (22). Narici et al. (22) described unpublished observations in which integrated electromyography was used to simultaneously examine the activation patterns of the vastus medialis, rectus femoris and vastus lateralis during isokinetic leg extension at 2.09 rad/s. Their information indicated that the vastus medialis exhibited the highest level of activation, followed by 30% less for the rectus femoris and 60% less for the vastus lateralis. No information was presented for the vastus intermedius. With respect to hypertrophy, Narici et al. stated, “This study has shown a preferential hypertrophy of the VM (vastus medialis) and VI (vastus intermedius) as compared to that of R (rectus femoris) and VL (vastus lateralis) muscles.” These authors (22) suggested that the degree of hypertrophy was related to the level of activation. In the present study, however, the rectus femoris of the trained leg hypertrophied to a greater extent than the other quadriceps muscles (Table 2). Thus the existence of a causative relationship between the level of activation during contractions and the degree of hypertrophy exhibited as a result of training remains speculative. There have been no studies before the present investigation that have used MRI technology to examine the effect of concentric isokinetic training on hypertrophy in
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ISOKINETIC TABLE
TRAINING
AND MUSCULAR
69
HYPERTROPHY
2. Changes in muscle cross-sectional area Proximal Pretraining
Trained FE FF Contralateral FE FF Trained LE VL VI VM RF Contralateral LE VL VI VM RF Trained LF BF ST SM Contralateral LF BF ST SM
Level, cm2
Posttraining
Middle %Change
Pretraining
Level, cm2
Posttraining
Distal %Change
Pretraining
Level, cm2
Posttraining
%Change
22.8 14.8
25.7 17.0
12.4* 14.4*
17.2 19.9
20.3 22.1
17.7* 11.0*
9.3 20.9
10.7 23.5
14.6 12.2”
24.9 15.3
24.1 16.2
-3.0 6.2
17.3 20.2
17.3 20.6
-0.3 2.0
10.8 22.9
10.3 23.2
-4.6 1.1
19.6 16.4 4.1 9.6
19.8 17.5 4.4 10.9
1.1 6.7 7.8 13.1*
23.7 22.8 9.0 6.1
25.6 24.6 10.6 7.5
i3.0* 8.0* 17.0 22.0*
14.7 16.3 16.3 1.5
16.7 17.5 17.9 2.1
13.4 7.6 9.9 34.4*
18.8 17.5 5.8 10.1
18.7 17.5 5.5 10.8
-0.8 0.1 -4.8 6.6
23.2 24.3 11.4 7.3
23.8 24.9 11.6 7.8
2.6 2.5 1.5 6.7
14.6 16.1 18.9 1.8
16.0 16.3 19.4 2.0
9.6 1.1 2.6 14.0
1.3 4.9
1.6 6.0
23.3 21.7*
8.0 7.2 3.2
9.2 9.0 3.8
15.0* 25.9* 19.9
9.5 4.9 9.4
10.6 6.1 10.0
11.9 24.2* 6.8
1.1 5.1
1.1 5.6
1.8 10.5
8.2 7.4 3.2
8.7 8.1 3.5
7.0 9.1 7.5
9.4 5.1 9.9
9.2 5.3 10.2
-2.2 3.1 2.6
Values are means for 13 subjects. VL, vastus lateralis; VI, vastus semitendinosus; SM, semimembranosus. * P < 0.0008.
intermedius;
the muscles associated with forearm extension, forearm flexion, or leg flexion. The results of the present investigation indicated that each of these muscle groups demonstrated preferential hypertrophy of particular muscles within the muscle groups and at specific levels (proximal, middle, and/or distal). Interestingly, the semitendinosus, which is closest to the midsagittal line of the thigh, demonstrated the greatest degree of hypertrophy of the leg flexors. In addition, the biceps femoris, which is lateral at the distal end of the femur and becomes closer to the midline of the thigh as it reaches the midfemur level, exhibited hypertrophy at the middle level only. These findings, in addition to the increases in the CSA of the rectus femoris at all three levels, suggest that muscles nearest the midsagittal line of the segment may be positioned such that they receive more training stimulus than muscles which are located more medially or laterally. Only two previous studies (16, 22) have investigated the effect of unilateral concentric isokinetic training on the muscle CSA of the contralateral limb (cross-training effect) and both examined only the leg extensors. Krotkiewski et al. (16) utilized ultrasound, thigh circumferences and muscle biopsies while Narici et al. (22) used MRI technology to determine muscle CSA and neither found a cross-training effect with regard to hypertrophy. The results of the present investigation were consistent with these findings for all muscles of the contralateral side, It is interesting to note, however, that although no muscles on the contralateral side of the body demonstrated statistically significant (P > 0.0008) hypertrophy, most (forearm flexors, vastus lateralis, vastus intermedius, vastus medialis, rectus femoris, biceps femoris, semitendinosus, and semimembranosus) increased in CSA
VM,
vastus
medialis;
RF,
r&us
femoris;
BF,
bicepsfemoris; ST,
(0.1 to 14.0%) as a result of the training. In addition, although none of the changes was statistically significant (P > 0.0008), peak torque for all movements on the contralateral side of the body also increased (6.7 to 14.8%). Given the consistency of the increases in peak torque and CSA in the contralateral limbs as well as the accuracy of the Cybex II and MRI techniques, it is unlikely that these findings were due to chance or instrumentation. Furthermore, many of the increases in peak torque and CSA in the contralateral limbs were greater than those that have been reported for inactive adult male control groups (6,9, 26). Although it is not likely that adult males would hypertrophy or increase in strength as a result of 8 wk of inactivity, future studies should consider utilizing a control group in addition to the experimental group to further examine this issue. The refore 9 th .e trend (al though sign& ant) towa .rd increased muscle not statistically CSA and strength on the contralateral side of the body suggested some cross-training effect as a result of unilateral concentric isokinetic training. Hellebrandt (11) proposed two possible mechanisms to explain the crosstraining effect: 1) diffusion of motor impulses to the contralateral side of the body and 2) contraction of the musculature on the contralateral side of the body to maintain balance and assume the proper position for the unilateral exercise. It is possible that a longer period of training may have resulted in statistically significant increases in strength and CSA on the contralateral side. In summary, the results of the present investigation indicated that concentric isokinetic training resulted in 1) muscular hypertrophy o f the exten sor and flexor muscles of the trained forearm and leg; 2) preferential hypertrophy of individual extensor and flexor muscles of the trained leg; 3) preferential hypertrophy at specific levels
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70
ISOKINETIC
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AND MUSCULAR
of the forearm extensors, vastus lateralis, vastus intermedius, and biceps femoris of the trained limbs; and 4) no significant cross-training effect with regard to strength or CSA. The authors thank the University of Nebraska Medical Center for the support given to this project, Drs. Phoebe Kaplan and Warren Stinson for invaluable expertise, and Dr. Sharon Evans for the use of digitizing equipment and assistance with the cross-sectional area measurement process. In addition, the authors thank Sheila Thomas and Michelle Satterlee for technical assistance in the acquisition of magnetic resonance images and Lori Harrison and Edna Manning for help in the preparation of the manuscript. The authors especially thank all the men who volunteered for this study. Address for reprint requests: D. J. Housh, 5lA Dent, UNMC College of Dentistry, Lincoln, NE 68583-0740.
HYPERTROPHY
bolic capacity during strength training and detraining: a one leg model. Eur. J. Appl. Physiol. Occup. Physiol. 51: 25-35, 1983.
13* Isolated II and
Joint U.B.X.
Testing and Exercise: A Handbook for Using the Cybex T. Ronkonkoma, NY: Cybex, Div. of Lumex, 1981, p.
51-52,69-70. D. A., AND 0. M. RUTHERFORD. Human muscle strength training: the effects of three different regimes and the nature of the resultant changes. J. Physiol. Lond. 391: l-11, 1987. KEPPEL, G. Design and Analysis: A Researcher’s Handbook (2nd ed). Englewood Cliffs, NJ: Prentice-Hall, 1982, p. 106, 146-149, 165. KROTKIEWSKI, M., A. ANIANSSON, G. GRIMBY, P. BJORNTORP, AND L. SJOSTROM. The effect of unilateral isokinetic strength traiing on local adipose and muscle tissue morphology, thickness, and enzymes. Eur. J. Appl. Physiol. Occup. Physiol. 42: 271-281, 1979. KRUSE, R. D., AND D. K. MATHEWS. Bilateral effects of unilateral exercise: experimental study based on 120 subjects. Arch. Phys.
14. JONES,
15 l
16 ’ 17 .
Received 22 July 1991; accepted in final form 24 January 1992.
Med. RehabiZ. 18. LESMES, G.
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![[Muscle stress of rehabilitation-oriented concentric and concentric-eccentric implemented isokinetic training].](/assets/img/hold.png)
