The Effect of Upper-Limb Motion on Lower-Limb Muscle Synchrony : Implications for Anterior Cruciate Ligament Injury

Cowling, E. J. BSc(Hons); Steele, J. R. PhD

Journal of Bone & Joint Surgery - American Volume:
Article
Abstract

Background: A high prevalence of rupture of the anterior cruciate ligament is associated with activities that incorporate both abrupt deceleration and catching a ball. In the present study, we examined whether the upper-limb motion involved in catching a ball affected the synchrony of the lower-limb muscles during tasks known to stress the anterior cruciate ligament-namely, abrupt decelerative landings.

Methods: Seven male and eleven female subjects decelerated abruptly to land in single-limb stance after catching a chest-height pass and after no catching. Ground-reaction force and electromyographic data for six lower-limb muscles were sampled while the subjects' landing technique was filmed. The joint-reaction forces and the sagittal planar net moments for the knee then were calculated to derive the tibiofemoral shear forces. The muscle onsets and peak muscle activities were temporally analyzed with respect to the time of initial foot-ground contact, the peak resultant ground-reaction force, and the peak tibiofemoral shear force.

Results: When catching a pass, the subjects demonstrated significantly (p < 0.05) earlier rectus femoris onset relative to the timing of the initial foot-ground contact and of the peak tibiofemoral shear force, and they showed delayed biceps femoris onset relative to the timing of the peak tibiofemoral shear force compared with the findings in the trials without catching.

Conclusions: We concluded that catching a ball during an abrupt landing could increase the potential for an anterior cruciate ligament injury by limiting the time available for the hamstring muscles to generate posterior tibial-drawer force before the onset of the quadriceps-induced anterior tibial translation.

Clinical Relevance: The integrity of the anterior cruciate ligament during landing relies on the proper coordination of the lower-limb muscles, particularly the quadriceps and the hamstrings. The present study demonstrated that motion of the upper-limbs may interfere with recruitment of these muscles, thereby predisposing the anterior cruciate ligament to injury.

Author Information

E.J. Cowling, BSc(Hons); J.R. Steele, PhD; Biomechanics Research Laboratory, Department of Biomedical Science, University of Wollongong, Wollongong NSW 2522, Australia. E-mail address for E.J. Cowling: ejc03@uow.edu.au. E-mail address for J.R. Steele: julie_steele@uow.edu.au

Article Outline

The most frequently occurring and debilitating knee injury in sports is rupture of the anterior cruciate ligament1,2. Typically, noncontact injury of the anterior cruciate ligament involves rapid deceleration3, quick changes in direction4, or abrupt landing, often accompanied by a poor landing technique5,6.

In a study of patients with a functionally deficient anterior cruciate ligament, one of us (J.R.S.) and Brown7 postulated that the upper-limb motion required to catch a ball may interfere with this muscle coordination during dynamic tasks, such as an abrupt landing, thereby compromising the preprogrammed synchrony of the lower-limb muscles required to ensure that the integrity of the anterior cruciate ligament is maintained. However, we found only one report in which the influence of upper-limb motion on the function of the lower-limb muscles during a dynamic task was examined. In that study, Miyatsu et al.8 compared the dynamic properties of the muscles in the knee joint as subjects jumped down from a 40-cm-high box while throwing a ball or while not throwing a ball. They reported that the forearm extension involved in throwing a ball compared with that involved in not throwing a ball resulted in greater knee extension and suppressed hamstring activity upon landing, thereby imposing greater tibiofemoral shear forces and increasing the potential for injury of the anterior cruciate ligament. Although they did not report trunk and hip angles in their study, Miyatsu et al. suggested that the forearm extension involved in the release of the ball was responsible for the observed increase in knee extension and the suppressed hamstring-muscle activity at the time of landing. However, we found no studies to confirm whether other upper-limb motion, such as catching a ball, affected the synchrony of the lower-limb muscles during tasks known to stress the anterior cruciate ligament-namely, abrupt decelerative landings. If upper-limb motion substantially alters the synchrony of the lower-limb muscles, there are immediate applications for this knowledge with regard to developing strategies to prevent injury of the anterior cruciate ligament and to developing rehabilitation programs. Therefore, the purpose of our study was to establish whether the upper-limb motion involved in catching a ball influenced the coordination of the muscles crossing the knee joint during abrupt deceleration on landing.

Back to Top | Article Outline

Materials and Methods

Subjects

Seven male and eleven female recreational athletes with no history of lower-limb injury, disease, or trauma who participated in sports that were associated with a high prevalence of injury to the anterior cruciate ligament (for example, netball and basketball) were recruited to participate in the study. (Netball is somewhat similar to basketball and is played predominantly in the Commonwealth countries by females.) The subjects had a mean age (and standard deviation) of 22.6 ± 2.5 years, a mean height of 1.70 ± 0.07 m, and a mean body mass of 65.5 ± 12.0 kg. To ensure that the selection criteria were satisfied, each subject completed an informed consent form and a questionnaire regarding his or her history of injury. In addition, all testing was conducted in accordance with the National Health and Medical Research Council Statement on Human Experimentation9.

Back to Top | Article Outline
Experimental Protocol

Each subject was required to accelerate forward for approximately three paces, leap from the nondominant limb, and then abruptly decelerate by landing on the dominant (test) limb in single-limb stance on a force platform. Data were collected for a minimum of five successful trials (that is, landing with the foot centrally located on the force platform) under two test conditions: (1) catching a leather netball (Mitre, India) at chest height during landing (catch), and (2) refraining from use of any pronounced upper-limb motion upon landing (no catch). These two conditions were randomly presented to the subjects, and therefore the subjects did not know whether they would be required to catch a ball during landing until the moment that the ball was released by the thrower. Abrupt landing was selected as the deceleration task in the present study, as such landings have been implicated as a typical noncontact mechanism for injury of the anterior cruciate ligament. Before performing the deceleration task, each subject completed a standardized five-minute cycling warm-up on a wind-braked cycle ergometer (Monark, Varberg, Sweden) (set at a workload of 50 to 100W) to ensure that all subjects had a similar warm-up.

Back to Top | Article Outline
Data Collection
Film Data

The landing action of each subject was filmed in the plane of progression with use of a LOCAM (model 51; Redlake Imaging, Morgan Hill, California) 16-mm pin-registered high-speed motion-picture camera (200 Hz, 1/600-second exposure time) leveled on a tripod 0.95 m above the ground and 3.5 m from the subject to allow for later analysis of the landing technique. The camera placement and alignment were designed to minimize errors of perspective. A 1-m horizontal scaling ruler, placed directly over the force platform, was filmed before each set of trials to enable later conversion of the film images to the actual distance in meters. The high-speed camera was time-synchronized with the electromyographic and force data by marking the film with an ultrabright current-limited light-emitting diode system placed in the camera's field of view.

Back to Top | Article Outline
Ground-Reaction Force Data

Following familiarization with the task, each subject performed the test. Three orthogonal components and the point of application of the ground-reaction forces generated during landing were recorded over four seconds (1000 Hz) as the subject landed on a multicomponent force plate (type 9281B; Kistler Instrumente AG, Winterthur, Switzerland) interfaced with a multichannel charge amplifier (type 9865A; Kistler Instrumente AG). The force plate was secured on four steel mountings embedded on a concrete base and covered with a granulated rubber sports surface so that the landing surface was flush with a wooden walkway (7.26 by 2.42 by 0.11 m). Each subject's foot placement on landing was manually measured (in millimeters) from the point of the location of the anterior part of the subject's shoe corresponding to the second toe and from the point of the midline of the heel with respect to the short and long axes of the force plate. These foot-placement data were used in conjunction with the kinematic and force-plate data to locate the x and y coordinates of the center of pressure relative to the subject's landed foot10. The four vertical, two anteroposterior, and two mediolateral channels were summed and scaled to obtain force-time curves as input to later determine the tibiofemoral shear forces and the peak resultant ground-reaction force.

Back to Top | Article Outline
Muscle Activity Data

The skin-surface sites of the six superficial muscles crossing the knee joint (the rectus femoris, vastus lateralis, vastus medialis, semimembranosus, biceps femoris, and medial head of the gastrocnemius) were initially prepared by shaving, abrading, and swabbing with diluted ethanol to reduce skin impedance (less than 6 kW), measured with the Artifact Eliminator (model CE01; CardioMetrics, Taylors Lakes, Victoria, Australia), at the site of each electrode. Adhesive-backed bipolar silver-silver chloride disposable infant-monitoring surface electrodes (3M, Morden, Manitoba, Canada) then were placed over the relevant muscle bellies (with an inter-detection-surface spacing of 10 mm), and, after confirming correct placement of the electrodes by means of muscle palpation and a clear electromyographic signal, the electrode wires were taped to the subject's skin to minimize movement artifact. A reference electrode was placed on the lateral femoral epicondyle. The electromyographic signals were relayed from the electrodes to a battery-powered transmitter (Telemyo; Noraxon, Scottsdale, Arizona), with eight channels and a mass of 0.96 kg, strapped firmly to the subject's lower back, to the Telemyo receiver. The analogue output for the muscles from the receiver (±5 V for full scale) were sampled at 1000 Hz (bandwidth, 0 to 340 Hz) with use of Bioware software (version 3.06 for Windows 95; Kistler) and stored for later analysis.

Back to Top | Article Outline
Data Analysis
Kinematic Data

After processing of the film, the two-dimensional coordinates for the adhesive skin-marker landmarks placed on the lateral aspect of each subject's foot, ankle, knee, hip, and shoulder were manually digitized (200 Hz) with use of a sonic digitizer (GP9; Science Accessories, Stratford, Connecticut) interfaced with a personal computer. The landmarks were selected to enable later computation of foot, leg, thigh, and trunk motion during landing. Three representative trials per subject were analyzed, commencing with the frame representing the initial contact between the shoe on the subject's test limb and the force plate and continuing until fifteen frames after the frame corresponding to the generation of the peak resultant ground-reaction force. After digitizing, a fourth-order zero-phase-shift Butterworth digital low-pass filter was applied to the data11 in order to filter out any high-frequency noise (a cutoff frequency of 11 Hz, determined with use of the residual analysis method11). The processed digitized film data then were used to determine the kinematic variables of interest during the landing task-namely, the hip and knee flexion angles and the trunk angle relative to the right-hand horizontal. Variables that were required to derive the joint-reaction forces and the moments of force about the knee joint also were calculated; these included the linear acceleration of the foot and leg mass centers (m/sec-2), the distance from the segmental center of mass to the point of application of the reaction forces (m), and the angular acceleration of the foot and leg in the sagittal plane (deg/sec-2).

Back to Top | Article Outline
Kinetic Data

The magnitude and timing of the peak of the summed vertical and anteroposterior ground-reaction forces and the time of initial contact and peak resultant ground-reaction forces were determined for each landing trial. All values were recorded both in newtons and as normalized for body weight. The joint-reaction forces and sagittal planar net moments of force for the knee then were calculated with use of newtonian equations of motion and inverse dynamics. The input for the analyses was derived from the kinematic and ground-reaction force data, combined with estimates of the mass and moment of inertia of each segment. The tibiofemoral shear force (FS), which acts parallel to the orientation of the tibial plateau, then was calculated, with use of the method of Kuster et al.12, as the sum of the shear component of the patellar tendon force (FP) and the shear component of the resultant joint-reaction force (R) (Fig. 1Fig. 1). The data pertaining to knee joint geometry-that is, the angle of the patellar tendon force (FP) relative to the knee flexion angle (b) and the angle of the tibial plateau relative to the long axis of the tibia (a) (Fig. 1Fig. 1)-used as input in these calculations were obtained from an article by Nisell13. The time to the peak tibiofemoral shear force was used to represent the time of maximal anterior loading of the knee joint during the landing task.

Back to Top | Article Outline
Muscle-Activation Patterns

To assess the temporal characteristics of the muscle bursts, the raw electromyographic data were visually inspected and any signal offset was removed with use of signal-processing software (PROG)14. The full-wave rectified data then were filtered with use of a fourth-order zero-phase-shift Butterworth low-pass filter11 (a cutoff frequency of 20 Hz), and the resultant linear envelopes were screened with a threshold detector. Cutoff frequencies ranging from 10 to 25 Hz (in 1-Hz increments) were initially tried, and 20 Hz was selected as it produced a smoothed representation of the raw electromyographic signals that closely resembled the shape of the muscle tension curves while retaining critical temporal components of the signal. Muscle burst onsets and offsets were deemed to have occurred when fourteen consecutive samples (a 1000-Hz sampling rate) of the linear envelope exceeded and passed back under, respectively, a threshold of 7% of the maximum amplitude of the linear envelope of the muscle burst of interest. A 7% threshold was chosen after thresholds ranging from 3% to 15% were tested in trials, and the output was compared with the muscle burst onsets and offsets manually derived from the filtered electromyographic data and the linear envelopes. This threshold value also has been used to calculate muscle burst onsets and offsets in a previous study in which lower-limb muscle synchrony was examined7. Each signal then was visually inspected to confirm the validity of the calculated results and to minimize the probability of a type-I error. The temporal characteristics (the duration, onset, and peak activity) of each muscle burst immediately prior to landing, for each of the six muscles, were analyzed relative to the timing of initial contact, the peak resultant ground-reaction force, and the peak tibiofemoral shear force. These variables were chosen to provide information pertaining to the effects of upper-limb motion on lower-limb muscle-activation patterns during the deceleration task. The muscle-activation patterns and kinematic variables were assessed relative to the times of initial contact, the peak resultant ground-reaction force, and the peak tibiofemoral shear force, as these times have been identified as the most critical in the landing task7.

Back to Top | Article Outline
Statistical Analysis

The means and standard deviations for the kinematic, kinetic, and electromyographic dependent variables were calculated for each of the two landing conditions. Normality was confirmed for the data with use of a Kolmogorov-Smirnov test with the Lilliefors correction, and equal variance was confirmed with a Levene median test. The p value to reject normality and/or equal variance was set at p £ 0.05. The dependent means were analyzed with use of paired t tests. The main purpose of this design was to establish whether upper-limb motion significantly (p £ 0.05) affected synchrony of the lower-limb muscles during the dynamic deceleration task.

Back to Top | Article Outline

Results

Kinetic Data

No significant differences between the catch and no-catch test conditions were found with respect to any of the kinetic variables displayed at landing (Table ITable I)-that is, the subjects generated peak forces at landing of a similar magnitude and at a consistent time after initial contact, irrespective of whether they were required to catch a ball.

Back to Top | Article Outline
Kinematic Data

No significant difference between the catch and no-catch test conditions was detected with respect to knee angle at either initial contact or peak resultant ground-reaction force, suggesting that catching a ball upon landing did not alter knee-joint kinematics throughout the landing phase. In contrast, paired t tests indicated significant differences between the catch and no-catch conditions with respect to both the mean hip angle and the mean trunk angle at initial contact and at peak resultant ground-reaction force (Table IITable II). Although significant (p £ 0.05), the difference in the means between the two conditions at both initial contact and peak resultant ground-reaction force ranged from only 3.5° to 4.5°. As the error inherent in measuring joint angles is often considered to be as much as 5°, the difference between the two conditions with respect to the hip and trunk angles in the present study was not considered to be meaningful. Furthermore, in view of the findings of one of us (J.R.S.) and colleagues15, this small change in hip angle was not expected to substantially alter the ability of the hamstring muscles to restrain anterior tibial translation.

Back to Top | Article Outline
Muscle-Activation Patterns

The burst onset time of the rectus femoris muscle and the burst peak time of the gastrocnemius muscle, relative to the time of initial contact, were significantly earlier in the catch condition than in the no-catch condition (Fig. 2Fig. 2) (Table IIITable III). Furthermore, the burst onset time of the rectus femoris muscle, relative to the time of the peak tibiofemoral shear force, was significantly earlier for the catch condition than for the no-catch condition. However, the burst onset time of the biceps femoris muscle, relative to the time of the peak tibiofemoral shear force, was significantly later for the catch condition than for the no-catch condition (Fig. 3Fig. 3).

Back to Top | Article Outline

Discussion

Compared with that in the no-catch condition, the upper-limb motion involved in catching a ball resulted in significantly earlier onset of rectus femoris muscle activity relative to the time of the initial contact and relative to the time of the peak tibiofemoral shear force. With the exception of vastus medialis onset relative to the timing of the peak tibiofemoral shear force, a similar trend was noted for earlier burst onset of the vastus muscles relative to the time of initial contact and relative to the time of the peak tibiofemoral shear force. This finding suggests that upper-limb motion caused earlier activation of the anterior thigh muscles. Although not significant, the power of these trends for the vastus muscles was low (5% to 10%), and therefore they warrant further investigation. Miyatsu et al.8 reported that the moment of ball release by a subject who performed a throwing action before landing from a jump from a box was accompanied by increased vastus medialis activity and suppressed semimembranosus activity. They suggested that the upper-limb action of throwing a ball resulted in overcontraction of the quadriceps muscles relative to the hamstring muscles. Our study supports this theory, as we found that earlier quadriceps muscle contraction may promote anterior tibial translation, particularly if the hamstring muscles are not activated sufficiently to generate an antagonistic posterior tibial-drawer force.

Miyatsu et al.8 did not examine the effects of upper-limb motion on biceps femoris or gastrocnemius activity, so comparisons with our study are limited. However, they noted that subjects who were required to release a ball when they landed from a jump from a box had suppressed semimembranosus activity just before landing. We also noted a later biceps femoris onset relative to the timing of the peak tibiofemoral shear force in the catch test condition, suggesting that upper-limb motion significantly (p £ 0.05) delayed the onset of biceps femoris muscle activity. Despite the difference between our study and that of Miyatsu et al.8 with respect to the landing techniques, the findings of both studies suggested that motion of the upper-limbs delayed or suppressed the activation of the muscles that act as synergists to the anterior cruciate ligament.

The activity of the gastrocnemius muscle was found to reach a peak significantly earlier in the catch test condition than in the no-catch test condition. However, because of the large window of time proposed for electromechanical delay of the lower-limb muscles (20 to 100 msec)16, it could not be established whether this earlier peak positively or negatively affected the onset of gastrocnemius mechanical force generation relative to the timing of the peak tibiofemoral shear force. As the gastrocnemius muscle can act as a synergist to the anterior cruciate ligament by imparting a posterior drawer on the proximal part of the tibia, additional research is warranted to establish the precise electromechanical delay associated with the gastrocnemius muscle so that the effects of upper-limb motion on gastrocnemius muscle activity can be more clearly interpreted.

The time-interval between the onset of biceps femoris muscle activity and the onset of rectus femoris muscle activity in the no-catch condition was longer than that in the catch condition (Fig. 3Fig. 3). It has been postulated that the increased interval between the biceps femoris and rectus femoris onset times in the no-catch condition provides greater protection to the anterior cruciate ligament by allowing more time for a posterior tibial-drawer force to be generated by the biceps femoris before the onset of the rectus-femoris-induced anterior tibial translation17. Therefore, the significant alterations in the biceps femoris and rectus femoris onset times in the catch condition may predispose the anterior cruciate ligament to less protection from the hamstring muscles during landing.

Reflex contraction of the hamstring muscles occurs too slowly to protect the knee effectively from injury in dynamic landing tasks18,19. All six muscles examined in the present study consistently showed onset times before initial contact, suggesting that the activity of the lower-limb muscles was preprogrammed before landing20. As subjects did not know whether the upper-limb motion of catching was required until the ball was released by the thrower, the significant differences observed in lower-limb muscle-activation patterns between the catch and no-catch conditions suggest that upper-limb motion was responsible for altering the preprogrammed activity of the lower-limb muscles. The mechanism by which this was possible is currently unknown, but, as the changes appear to predispose the anterior cruciate ligament to increased potential for injury, additional investigation is warranted.

Our results suggest that upper-limb motion is not accompanied by any significant change in knee-joint angle at the time of either initial contact or the peak resultant ground-reaction force. Therefore, any changes in lower-limb muscle-activation patterns in the present study were not considered to have resulted from changes in lower-limb or trunk kinematics during the landing task. These results are in contrast to the findings of Miyatsu et al.8, who reported that subjects who threw a ball while jumping from a 40-cm-high box had less knee flexion than subjects who jumped without throwing a ball. This extended knee position was accompanied by suppressed hamstring activity. Trunk and hip angles were not reported by Miyatsu et al.; however, they suggested that forearm extension may have been responsible for the decreased knee flexion angles and the suppressed hamstring muscle recruitment at the time of landing. The findings in the study by Miyatsu et al. suggest a link between upper-limb motion and an increased potential for knee-joint injury, as the hamstring muscles act synergistically with the anterior cruciate ligament in restraining anterior tibial translation.

We detected no significant differences between the catch and no-catch conditions with respect to either the timing or the magnitude of the forces generated by the subjects upon landing. Therefore, we concluded that the upper-limb motion involved in catching a ball did not alter the kinetics of landing.

Although the upper-limb motion involved in catching a ball did not alter the kinetics or joint angles displayed at landing, it resulted in significantly later hamstring muscle activity and significantly earlier quadriceps muscle activity (p £ 0.05). We concluded that upper-limb motion involved in catching a ball during an abrupt decelerative landing can increase the potential for anterior cruciate ligament injury by limiting the time available for a posterior tibial-drawer force to be generated by the hamstring muscles before the onset of the quadriceps-muscle-induced anterior tibial translation. The exact mechanism by which upper-limb motion can alter lower-limb muscle-activation patterns remains a question for further investigation.

Investigation performed at the Biomechanics Research Laboratory, Department of Biomedical Science, University of Wollongong, Wollongong, New South Wales, Australia

No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. Funds were received in total or partial support of the research or clinical study presented in this article. The funding source was the Sporting Injuries Committee, New South Wales, Australia.

1. Johnson RJ. The anterior cruciate ligament problem. Clin Orthop, 1983;172: 14-8.
2. Malone TR, Hardaker WT, Garrett WE, Feagin JA, Bassett FH. Relationship of gender to anterior cruciate ligament injuries in intercollegiate basketball players. J South Orthop Assoc, 1993;2: 36-9.
3. Miller MDM, Cooper DE, Warner JJP. Review of sports medicine and arthroscopy. Philadelphia: WB Saunders; 1995
4. Bartold SJ. Injury driven change to the fundamental design parameters of the Australian Rules Football boot. In: Abstracts of the Australian Conference of Science and Medicine in Sport. Bruce, Australian Capital Territory: Sports Medicine Australia; 1997. p 52-3
5. Hopper D, Elliott B. Lower-limb and back injury patterns of elite netball players. Sports Med, 1993;16: 148-62.
6. Hume PA, Steele JR. Injury prevention strategies in netball: are Australian players heeding the advice?. J Sci Med Sport, 2000;3: 392-9.
7. Steele JR, Brown JM. Effects of chronic anterior cruciate ligament deficiency on muscle activation patterns during an abrupt deceleration task. Clin Biomech, 1999;14: 247-57.
8. Miyatsu M, Onozawa T, Atsuta Y, Watakabe M, Ishimaru A, Suzuki N, Sugawara O, Asano Y, Yamashita I, Takemitsu Y. Dynamic properties of muscles regulating the knee joint in basketball. In: de Groot G, Hollander AP, Huijing PA, van Ingen Schenau GJ, editors. Biomechanics XI-B. Amsterdam: Free University Press; 1988. p 831-5
9. National Health and Medical Research Council. NHMRC Statement on Human Experimentation. Canberra, Australia: National Health and Medical Research Council; 1994
10. Bobbert MF, Schamhardt HC. Accuracy of determining the point of force of application with piezoelectric force plates. J Biomech, 1990;23: 705-10.
11. Winter DA. Biomechanics and motor control of human movement. 2nd ed. New York: Wiley; 1990
12. Kuster M, Wood GA, Sakurai S, Blatter G. Downhill walking: a stressful task for the anterior cruciate ligament? A biomechanical study with clinical implications. Knee Surg Sports Traumatol Arthrosc, 1994;2: 2-7.
13. Nisell R. Mechanics of the knee. A study of joint and muscle load with clinical implications. Acta Orthop Scand, 1985;56(Suppl): 1-42.
14. Andrews M. PROG [computer program]. Department of Biomedical Science, University of Wollongong, Wollongong, New South Wales, Australia, 1996
15. Steele JR, Milburn PD, Roger GJ. Effect of torso position on arthrometric assessment of anterior knee laxity. Clin Biomech, 1995;10: 421-7.
16. Zhou S, Lawson DL, Morrison WE,, Fairweather I. Electromechanical delay of knee extensors: the normal range and the effects of age and gender. J Human Movement Studies, 1995;28: 127-46.
17. Kain CC, McCarthy JA, Arms S, Pope MH, Steadman JR, Manske PA, Shively RA. An in vivo analysis of the effect of transcutaneous electrical stimulation of the quadriceps and hamstrings on anterior cruciate ligament deformation. Am J Sports Med., 1988;16: 147-52.
18. Grabiner MD, Weiker GG. Anterior cruciate ligament injury and hamstrings coactivation. Clin Biomech, 1993;8: 215-9.
19. Solomonow M, Baratta R, Zhou BH, Shoji E, Bose W, Beck C, D'Ambrosia R. The synergistic action of the anterior cruciate ligament and thigh muscles in maintaining joint stability. Am J Sports Med, 1987;15: 207-13.
20. Andriacchi TP. Dynamics of pathological motion: applied to the anterior cruciate deficient knee. J Biomech, 1990;23(Suppl 1): 99-105.
Copyright 2001 by The Journal of Bone and Joint Surgery, Incorporated