Medicine & Science in Sports & Exercise:
Clinical Sciences: Clinical Investigations
Eccentric knee flexor torque following anterior cruciate ligament surgery
OSTERNIG, LOUIS R.; JAMES, CHARLES R.; BERCADES, DAVID T.
Department of Exercise and Movement Science, University of Oregon, Eugene, OR 97403
Submitted for publication September 1995.
Accepted for publication May 1996.
Address for correspondence: Louis R. Osternig, Department of Exercise and Movement Science, University of Oregon, Eugene, Oregon 97403.
The purposes of this study were to compare eccentric knee flexor torque and muscle activation in the limbs of normal (NOR) subjects and in subjects who had undergone unilateral ACL autograft surgical reconstruction (INJ) and to assess the effect of movement speed on EMG/torque ratios and eccentric-concentric actions. Fourteen subjects (7 NOR and 7 INJ) were tested for knee eccentric flexor torque and EMG activity at four isokinetic speeds(15°, 30°, 45°, and 60°·s-1). Results revealed that post-surgical limbs (ACL) produced significantly less (P < 0.05) eccentric torque and flexor EMG activity at 60°·s-1 than uninjured (UNI) contralateral limbs. Eccentric torque rose significantly as speed increased from 45° to 60°·s-1 for surgical group uninjured limbs and NOR group left and right limbs. Eccentric flexor torque increased with speed for both groups and approximated equality with concentric extensor torque at 60°·s-1 for INJ group ACL and UNI limbs. Concentric flexor muscle EMG/torque ratios were 30-191% greater than eccentric muscle actions across groups and speeds. The results suggest that ACL dysfunction may result in reduced eccentric flexor torque at rapid movement speeds, that eccentric flexor torque increases with movement speed and may have the capacity to counter forceful extensor concentric torque, and that eccentric muscle actions produce less muscle activation per unit force than concentric actions which may reflect reduced energy cost.
The anterior cruciate ligament (ACL) is critical to normal knee function and its disruption often leads to early onset osteoarthritis(13,14,25,34). Despite these associated problems, there is considerable variability in functional outcome among the ACL-deficient population (8,35,36). Young, physically active ACL-deficient patients may be considered candidates for ACL reconstructive surgery due to the relatively low percentage of satisfactory outcomes from conservative treatment and the relatively high percentage of good surgical results in this population (3).
Prior studies suggest that knee flexor muscle activity reduces the load on the ACL during knee extension(5,20,32,37,40). O'Connor(37) used a computer model to estimate the capacity of knee flexors to unload the cruciate ligaments throughout the knee joint range. He found that when both flexors (hamstrings and gastrocnemius) are used simultaneously against the quadriceps, they can unload the anterior and posterior cruciate ligaments throughout the range of knee motion except at near full extension. It has been postulated that this function may be compromised by a loss of afferent neural activity from traumatic or surgical denervation of the anterior cruciate ligament(20,27,30,31,38). Beard et al.(9) found a significantly increased reflex latency in the hamstrings of ACL-deficient subjects compared with the uninjured contralateral extremity. They also reported that functional instability of the knee was directly related to the increase in reflex latency (8). Di Fabio et al. (17) recorded the automatic postural response from the tibialis anterior, quadriceps, and hamstring muscles in a group of subjects with ACL deficiency. They found that an externally induced backward body sway induced selective activation of the hamstrings in the ACL-deficient limb as an apparent addition to the synergistic structure of the lower extremity. It was postulated that a capsular-hamstring reflex may be integrated into the existing structure of a preprogrammed postural synergy in ACL-deficient limbs to compensate for ligamentous laxity. A recent study(38) showed that eccentric hamstring electromyographic(EMG) activity during rapid knee extension was significantly less in the limbs of subjects who had undergone ACL reconstructive surgery compared with the limbs of uninjured counterparts. It was postulated that the injured subjects may have suffered denervation of ligamentous tissue from trauma or operative repair, thus reducing afferent activity and neural control(27,30). Such asymmetry in eccentric knee flexor coactivation may indicate an attenuation of the restraining role these muscles play in ACL dysfunctional limbs.
Electromyography is a useful but indefinite indicator of nonisometric muscle force (7,10,44), and more direct measures of eccentric torque are needed to better understand the interplay of knee muscles in dynamic activity among healthy and post-surgical subjects. The purposes of this study were to compare eccentric knee flexor torque and muscle activation in right and left limbs of normal (NOR) subjects and in subjects who had undergone unilateral ACL autograft surgical reconstruction (INJ), and to assess the effect of movement speed on EMG/torque ratios and eccentric-concentric action relationships.
Sixteen subjects were originally recruited for this study. One post-surgical subject was unable to complete participation and the total number of participants was adjusted to 14. The INJ group consisted of seven subjects (4 males, 3 females; mean age = 32.15 ± 8.13 yr) who had sustained a unilateral ACL injury within the 4-yr period prior to the study. All of these post-surgical subjects had undergone arthroscopic patellar tendon autograft reconstruction of the ACL at least 1 yr prior to testing. None of the INJ group had contralateral knee dysfunction or multiple surgical procedures. The normal (NOR) group consisted of seven subjects (4 males, 3 females; mean age = 30.45 ± 6.61 yr) who had no history of knee impairment. All subjects in both groups were fully ambulatory and physically active. The subjects gave their consent in accordance with the policy statement of the American College of Sports Medicine.
Separate tests on each of the subjects' contralateral limbs were conducted using a modified Orthotron isokinetic dynamometer. Measurements of maximum eccentric knee flexor torque during resisted knee extension and simultaneous knee flexor (hamstrings and gastrocnemius) and knee extensor (quadriceps) EMG activity were recorded at speeds of 15°, 30°, 45°, and 60°·s-1 (0.26-1.05 rads·s-1). Pilot testing revealed 60°·s-1 to be the upper speed limit safely tolerated by the subjects in this protocol. The order of bilateral testing was counterbalanced across subjects (28). Each subject was positioned prone on a padded table with the pelvis and thighs secured with straps and the dynamometer axis of rotation aligned with the knee's frontal axis. The tested leg was secured to the dynamometer lever arm and the knee was flexed to 90°. The lever arm was weighted distally and released, thereby imposing a knee extension moment at the present speed against which the subject resisted as forcefully as possible with the knee flexor musculature. Weight magnitude was adjusted to exceed the capacity of the subject to voluntarily slow knee extension throughout the measured joint range. Subjects were allowed unlimited submaximal warm-ups until they felt comfortable with the apparatus and testing procedure. The warm-ups ranged from three to five trials at each speed. Only the isokinetic portion of the movement, 70° to 20° of knee flexion, was used to analyze data. All subjects performed three trials of maximum eccentric exercise with each contralateral extremity at each speed. Separate trials of maximum concentric knee flexion and extension were also performed for data normalization purposes. Simultaneous recordings of eccentric torque, angular displacement, and EMG activity from the hamstrings, gastrocnemius, and vastus lateralis musculature were collected using an ARIEL performance analysis system (APAS; analog module). Angular displacement of knee motion and eccentric torque were monitored, respectively, by a rotational potentiometer and a hydraulic force transducer adapted to the dynamometer. Direct electrical current provided power to the potentiometer and transducer, and output signals from these devices were transmitted to the computer via an analog-to-digital converter. Data were downloaded from the APAS and processed with custom software. The unresisted torque generated by the weighted lever arm was calibrated regularly throughout the individual testing sessions at each speed. The torque recorded during resisted knee extension was subtracted from the unresisted torque to calculate the eccentric knee flexor torque produced by the subject. All torque values were averaged across the joint range tested. Electromyographic signals were sampled at 1 MHz with preamplified surface electrodes positioned directly over the bellies of the biceps femoris, medial gastrocnemius, and vastus lateralis muscles. The surface sites were shaved and cleaned, and electrode gel was applied between the skin and electrode to ensure low impedance (<5 kohms). Electromyographic recordings were full-wave rectified, integrated, and divided by the time of trial to provide EMG activity per unit time. Eccentric EMG activity was normalized to the percentage of activity recorded from the same muscle during maximum concentric knee flexion. EMG/torque ratio comparisons were determined by calculating EMG (nonnormalized) activity per unit torque for eccentric and concentric actions (45). Pairedt-tests and analyses of variance (ANOVA) were used to identify significant differences (P < 0.05), if any, in torque and EMG activity between contralateral limbs and between speeds.
Eccentric and concentric knee flexor torque values and normalized knee flexor EMG data are summarized, respectively, in Tables 1 and 2. The results revealed that the post-surgical limb (ACL) of the INJ group produced significantly less (P < 0.05) eccentric torque, and significantly less flexor EMG activity (gastrocnemius), at 60°·s-1 than the uninjured contralateral limb. No significant differences were found for the same comparisons at all speeds between normal (NOR) group contralateral limbs.
Figures 1 and 2 illustrate the change in eccentric and concentric flexor torque across testing speeds. Eccentric torque rose steadily with speed in both groups. This rise was significant as speed increased from 45° to 60°·s-1 for the uninjured limbs of the surgical (INJ) group and the left and right limbs of the NOR group. Eccentric flexor/concentric extensor torque ratios shown inFigure 3 indicate that eccentric flexor torque increased with speed for both groups and approximated equality with concentric extensor torque at 60°·s-1 for the ACL and UNI limbs of the INJ group. Flexor muscle EMG/torque ratios were 30-191% greater for concentric than eccentric muscle actions across groups and speeds(Figs. 4 and 5).
A number of reports have indicated that eccentric knee flexor coactivation stiffens the knee during voluntary extension, thereby attenuating strain to joint ligaments (5,20,32,42). This function is considered crucial to the dynamic stability of the knee joint(5,42). In this study, mean eccentric flexor torque and EMG (gastrocnemius) in the post-surgical limb were, respectively, 13% and 25% less than the contralateral uninjured extremity (P < 0.05), for the fastest speed tested (60°·s-1). This finding suggests that an association exists between EMG eccentric flexor torque and flexor EMG; however, the magnitude of torque may not be directly estimated from EMG data.
Although the hamstrings and gastrocnemius are both knee flexors, in this study only the gastrocnemius muscle of the ACL limb exhibited a significant EMG decrease compared with the UNI limb. Since the role of the hamstrings in unloading the cruciate ligaments in considered to be distinct from that of the gastrocnemius (37), a direct comparison to studies of hamstring activity is limited. Little research has been conducted on the role of the gastrocnemius as a knee joint stabilizer. O'Connor(37) and Collins (16) produced models indicating that the gastrocnemius, as well as the hamstrings, can restrain extensor torque and may unload cruciate ligaments. Their calculations assumed isometric (37) or closed chain activity(16), and direct application of the quantitative results requires further study. The finding of significant ACL/uninjured limb differences in gastrocnemius but not hamstring musculature may be related to speed of motion. Hagood et al. (21) reported that as knee extension velocity increased to 240°·s-1 there was a substantial EMG rise in the antagonist musculature, suggesting an increase in joint stiffness and reduction in laxity. It has also been shown that eccentric hamstring EMG activity during rapid knee extension is significantly less in the limbs of subjects who had undergone ACL reconstructive surgery compared with the uninjured contralateral counterpart (38). The significant difference was more pronounced as speed of motion was increased from 100° to 300°·s-1. It was suggested that the variation in eccentric hamstring coactivation may indicate a reduction in the restraining role these muscles play in ACL dysfunctional limbs. Since the speeds of motion were considerably higher than in the present study, it is possible that 60°·s-1 was not fast enough to evoke differences in hamstring activation. However, the increase to 60°·s-1 may have been sufficient to elicit gastrocnemius differences between the ACL and uninjured counterpart.
It has been postulated that regulation of agonist-antagonist muscle coactivation may be influenced by afferent discharge from ligament mechanoreceptors (20,23,24,40,41) and that ligament disruption and post-injury surgical reconstructions may disrupt knee mechanoreceptors and affect consequent extremity function(6,20,27,30,31). It is possible that trauma or surgical intervention may have denervated ligamentous tissue in the surgical knee resulting in reduced flexor responses at faster speeds of motion. In order to directly measure eccentric flexor torque in this study, the extensor moment was applied by a weighted lever arm against which the subjects were required to resist. Therefore, there are limitations in comparisons of the present data with those studies in which the extensor moment was applied by the action of the quadriceps muscles, an action that has been shown to load the ACL (20,37,39).
Movement speed appeared to have an effect on the eccentric muscular responses in the contralateral limbs of both groups of subjects. The steady rise in eccentric torque with speed found in this study is congruous with the early work of Katz (26), who, using prepared muscle specimens, calculated that force in lengthening contractions increase with velocity of stretch. Later work with human muscle(2,4) demonstrated that eccentric contractions produced greater force as lengthening velocity increased up to high velocities where force leveled off. Abbott and Aubert (1) reported that when stretch at constant speed is imposed on a muscle the rate of tension rise increases with the speed of stretch, but the tension has an upper limitation value independent of speed. More recent reports on human eccentric force-velocity relationships using isokinetic exercise, however, have yielded variable results. In these studies, whether peak torque rose or remained stable across increasing speeds appeared to be dependent upon training condition (24), subject gender (15), and joint position (46). Since average torque across the joint range rather than peak torque was used in this study, direct comparisons to those measuring peak torque are limited.
It has been suggested that the leveling off of peak torque with increasing eccentric speed found in some studies may be due to a reduction in neural drive, which may protect the neurologically intact muscle from injury at high velocities of lengthening (46,47). It is possible that the velocities in this study were not fast enough to invoke inhibitory stimuli and that torque continued to increase with speed of lengthening. This rise was attenuated in the surgical limb of the INJ group as only the uninjured limb of the INJ group and the contralateral limbs of the NOR group demonstrated a significant increase in torque from 45° to 60°·s-1. This attenuation may similarly be due to afferent receptor dysfunction resulting from trauma or surgery(30), thereby reducing flexor responses at faster speeds of motion.
The ratio of eccentric flexor torque to concentric extensor torque increased with speed for both groups and approximated equality at 60°·s-1 for the ACL and UNI limbs of the INJ group. This suggests that as speed increases the restraining action of the eccentrically contracting hamstrings may have an increasing capacity to counter the tibial anterior shear moment created by forcefully contracting knee extensors. In a recent computer modeling study of knee function, O'Connor(37) indicated that the coactivating knee flexors can generate sufficient isometric resistance to unload the cruciate ligaments over a specified range of motion. The present data suggest that knee flexor muscles may function similarly under conditions of dynamic loading as well. It is interesting to note that the eccentric flexor/concentric extensor ratio for both the ACL and UNI limbs of the INJ group significantly (P < 0.05) exceeded that of the left and right NOR group contralateral limbs for the 45° and 60°·s-1 conditions (Fig. 3). The ACL subjects may have accommodated their injuries and surgeries by more highly developing the flexor eccentric function relative to the antagonist quadriceps, thus potentially reducing anterior tibial shear. To maintain contralateral symmetry, this eccentric development may have been cross transferred to the uninjured extremity(19,33).
The finding that knee flexor eccentric actions generated less EMG activation per unit force than concentric actions is consistent with other studies (12,32,45). It has been postulated that eccentric contractions reflect reduced energy costs compared with concentric contractions since for a given load fewer muscle fibers are recruited for voluntary lengthening actions than with shortening actions(11,44). The results of this study suggest that speed of movement may influence the relative energy cost of eccentric muscle action as the eccentric EMG/torque ratio as a percentage of the concentric EMG/torque ratio tended to decrease across speeds.
The results suggest that ACL dysfunction may result in reduced eccentric flexor torque at rapid movement speeds, eccentric flexor torque increases with speed of movement and may have the capacity to counter forceful extensor concentric torque, and eccentric muscle actions produce less muscle activation per unit force than concentric actions which may reflect reduced energy cost(11,44,45).
1. Abbott, B. and X. Aubert. Changes in energy in a muscle during very slow stretches. Proc. R. Soc.
B 139:104-117, 1951.
2. Abbott, B., B. Bigland, and J. Ritchie. The physiological cost of negative work. J. Physiol.
3. Andriacchi, T., P. Sabiston, and K. Dehaven. Ligament: injury and repair. In: Injury and Repair of the Musculoskeletal Soft Tissues
, S. L. Woo and J. A. Buckwalter (Eds.). Park Ridge, IL: American Academy of Orthopaedic Surgeons, 1987, pp. 103-128.
4. Asmussen, E. Positive and negative muscular work.Acta Physiol. Scand.
5. Baratta, R., M. Solomonow, B. H. Zhou, E. D. Letson, R. Chuinard, and R. D'ambrosia. Muscular coactivation. the role of the antagonist musculature in maintaining knee stability. Am. J. Sports Med.
6. Barrack, R. L., H. B. Skinner, and S. L. Buckley. Proprioception in the anterior cruciate ligament dificient knee. Am. J. Sports Med.
7. Basmajian, J. and C. Deluca. Muscles Alive: Their Functions Revealed by Electromyography
, 5th Ed. Baltimore: Williams & Wilkins, 1985, pp. 187-220.
8. Beard, D., R. Kyberd, C. Fergusson, and C. Dodd. Proprioception after rupture of the anterior cruciate ligament. J. Bone Joint Surg.
9. Beard, D., R. Kyberd, J. O'Connor, C. Fergusson, and C. Dodd. Reflex hamstring contraction latency in anterior cruciate ligament deficiency. J. Orthop. Res.
10. Bigland-Ritchie, B. EMG/force relations and fatigue of human voluntary contractions. Exerc. Sport Sci. Rev.
11. Bigland-Ritchie, B. and J. Woods. Integrated EMG and O2
uptake during positive and negative work. J. Physiol.
12. Bigland-Ritchie, B. and O. Lippold. The relation between force, velocity, and integrated electrical activity in human muscles.J. Physiol.
13. Brandt, K. Transection of the anterior cruciate ligament in the dog: a model of osteoarthritis. Semin. Arthritis Rheum.
21(Suppl. 2):22-32, 1991.
14. Brandt, K., S. Myers, D. Burr, and M. Albrecht. Osteoarthritic changes in canine articular cartilage, subchondral bone, and synovium fifty-four months after transection of the anterior cruciate ligament. Arthritis Rheum.
15. Colliander, E. and P. Tesch. Bilateral eccentric and concentric torque of quadriceps and hamstring muscles in females and males.Eur. J. Appl. Physiol.
16. Collins, J. J. Antagonistic-synergistic muscle action at the knee during competitive weightlifting. Med. Biol. Eng. Comput.
17. Di Fabio, R. P., B. Graf, M. B. Badke, A. Breunig, and K. Jensen. Effect of knee joint laxity on long-loop postural reflexes: evidence for a human capsular-hamstring reflex. Exp. Brain Res.
18. Draganich, L. F., R. J. Jaeger, and A. R. Krali. Coactivation of the hamstrings and quadriceps during extension of the knee.J. Bone Joint Surg. 71A:1075-1081, 1989.
19. Enoka R. M. Muscle strength and its development.Sports Med.
20. Harter, R. A., L. R. Osternig, and K. M. Singer. Knee joint proprioception following anterior cruciate ligament reconstruction.J. Sports Rehabil.
21. Hagood, S., M. Solomonow, R. Baratta, B. J. Zhou, and R. D'Ambrosia. The effect of joint velocity on the contribution of the antagonist musculature to knee stiffness and laxity. Am. J. Sports Med.
22. Hortobagyi, T. and F. Katch. Eccentric and concentric torquevelocity relationships during arm flexion and extension. Eur. J. Appl. Physiol.
23. Johansson, H., P. Sjolander, and P. Sojka. Receptors in the knee joint ligaments and their role in the biomechanics of the joint.Crit. Rev. Biomed. Eng.
24. Johansson, H. Role of knee ligaments in proprioception and regulation of muscle stiffness. J. Electromyography Kinesiol.
25. Johnson, R., B. Beynnon, C. Nichols, and P. Renstrom. The treatment of injuries of the anterior cruciate ligament. J. Bone Joint Surg.
26. Katz, B. The relation between force and speed in muscular contraction. J. Physiol.
27. Kennedy, J. C., I. J. Alexander, and K. C. Hayes. Nerve supply of the human knee and its functional importance. Am. J. Sports Med.
28. Keppel, G. Design and Analysis.
Englewood Cliffs, NJ: Prentice Hall, 1991, pp. 335-339.
29. Komi, P. V., M. Kaneko, and O. Aura. EMG activity of the leg extensor muscles with special reference to mechanical efficiency in concentric and eccentric exercise. Int. J. Sports Med.
8(Suppl. 1):22-29, 1987.
30. Krauspe, R., M. Schmidt, and H. Schable. Sensory innervation of the anterior cruciate ligament. J. Bone Joint Surg.
31. Lephart, S. M., M. S. Kocher, F. H. Fu, P. Borsa, and C. D. Harner. Proprioception following anterior cruciate ligament reconstruction.J. Sports Rehabil.
32. More, R. C., B. T. Karras, R. Neiman, D. Fritschy, S. Woo, and D. M. Daniel. Hamstrings: an anterior cruciate ligament protagonist.Am. J. Sports Med.
33. Moritani, T. and H. A. deVries. Neural factors versus hypertrophy in the time course of muscle strength gain. Am. J. Phys. Med.
34. Myers, S., K. Brandt, B. O'Connor, D. Visco, and M. Albrecht. Synovitis and osteoarthritic changes in canine articular cartilage after anterior cruciate ligament transaction. Arthritis Rheum.
35. Noyes, F., P. Mooar, D. Matthews, and D. Butler. The symptomatic anterior cruciate-deficient knee. Part I: the long-term functional disability in athletically active individuals. J. Bone Joint Surg.
36. Noyes, F., D. Matthews, P. Mooar, and E. Grood. The symptomatic anterior cruciate-deficient knee. Part II: the results of rehabilitation, activity modification, and counseling on functional disability. J. Bone Joint Surg.
37. O'Connor, J. Can muscle co-contraction protect knee ligaments after injury or repair? J. Bone Joint Surg.
38. Osternig, L., B. Caster, and C. James. Contralateral hamstring (biceps femoris) coactivation patterns and anterior cruciate ligament dysfunction. Med. Sci. Sports Exerc.
39. Renstrom, P., S. W. Arms, T. S. Stanwyck, R. J. Johnson, and M. H. Pope. Strain within the anterior cruciate ligament during hamstring and quadriceps activity. Am. J. Sports Med.
40. Sojka, R., P. Sjolander, H. Johansson, and M. Djupsjobacka. Influence from stretch-sensitive receptors in the collateral ligaments of the knee joint on the gamma-muscle-spindle systems of flexor and extensor muscles. Neurosci. Res.
41. Sojka, P., H. Johansson, P. Sjolander, R. Lorentzon, and M. Djupsjobacka. Fusimotor neurons can be reflexly influenced by activity in receptor afferents from the posterior cruciate ligament. Brain Res.
42. Solomonow, M., R. Baratta, and B. H. Zghou. The synergistic action of the anterior cruciate ligament and thigh muscles in maintaining joint stability. Am. J. Sports Med.
43. Solomonow, M., R. Baratta, and R. D'Ambrosia. The EMG-force relationships of skeletal muscle: dependence on contraction rate and motor units control strategy. Electromyogr. Clin. Neurophysiol.
44. Stauber, W. T. Eccentric action of muscles: physiology, injury and adaptations. Exerc. Sport Sci. Rev.
45. Tesch, P., G. Dudley, M. Duvoisin, B. Hather, and R. Harris. Force and EMG signal patterns during repeated bouts of concentric and eccentric muscle actions. Acta Physiol. Scand.
46. Westing, S., J. Seger, E. Karlson, and E. Ekblom. Eccentric and concentric torque-velocity characteristics of the quadriceps femoris in man. Eur. J. App. Physiol.
47. Westing, S., A. Cresswell, and A. Thorstensson. Muscle activation during maximal voluntary eccentric and concentric knee extension.Eur. J. App. Physiol.
ECCENTRIC EXERCISE; ANTERIOR CRUCIATE LIGAMENT; ELECTROMYOGRAPHY
©1996The American College of Sports Medicine
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