0363-5465/102/3030-0483$02.00/0 THE AMERICAN JOURNAL OF SPORTS MEDICINE, Vol. 30, No. 4 © 2002 American Orthopaedic Society for Sports Medicine Motor Control of the Vastus Medialis Oblique and Vastus Lateralis Muscles Is Disrupted During Eccentric Contractions in Subjects with Patellofemoral Pain Tammy M. Owings,* MS, and Mark D. Grabiner,†‡ PhD From *the Department of Biomedical Engineering, The Cleveland Clinic Foundation, Cleveland, Ohio, and the †School of Kinesiology, University of Illinois at Chicago, Chicago, Illinois Background: Inappropriate control of the vastus medialis oblique and vastus lateralis muscles by the central nervous system can contribute to maltracking of the patella. Hypothesis: The activation timing and amplitude of the vastus medialis oblique and vastus lateralis muscles will be different between normal subjects and patients with patellofemoral pain. Study Design: Controlled laboratory study. Methods: Subjects with patellofemoral pain and asymptomatic control subjects performed maximum voluntary knee extension contractions initiated from a flexed and an extended position. The activation timing and amplitude of the vastus lateralis and vastus medialis oblique muscles were quantified from the recorded electromyographic signals. Results: There were no between-group differences in activation timing. The activation amplitude of the vastus medialis oblique and vastus lateralis muscles of the patellofemoral pain subjects was altered to the greatest extent during eccentric contractions and differed significantly from that of control subjects. Conclusions: The activation amplitudes of the vastus medialis oblique and vastus lateralis muscles of subjects with patellofemoral pain are consistent with a laterally tracking patella during eccentric contractions. Clinical Relevance: The findings suggest the clinical importance of determining whether altered activation patterns are sensitive to rehabilitation, and, if so, if subjective reports of knee joint pain and function parallel changes in the activation patterns as a result of rehabilitation. © 2002 American Orthopaedic Society for Sports Medicine can subsequently affect patellofemoral reaction forces and pressures. On the basis of this premise, an important functional role has been attributed to the vastus medialis oblique muscle in the causation of patellofemoral tracking disorders. Therefore, the vastus medialis oblique muscle is often targeted in rehabilitation protocols. However, supportive quantitative evidence for both the functional importance of the vastus medialis oblique muscle and for the effectiveness of rehabilitation that purportedly has a selective effect on it has not been conclusive. The rationale for an important biomechanical role of the vastus medialis oblique muscle in patellar tracking is substantiated by its physiologic and biomechanical properties. Compared with the vastus lateralis muscle, the vastus medialis oblique muscle has a smaller physiologic cross-sectional area13 and thus a smaller estimated max- Patellofemoral pain is the most prevalent knee disorder of children and young adults; however, the causative mechanisms remain imprecisely defined.10, 14 Aberrant patellar tracking is associated with some patellofemoral joint disorders. The position of the patella within the femoral trochlea, controlled by passive and dynamic mechanisms, influences patellofemoral joint reaction forces and pressures in cadaver specimens.7 Because the medially and laterally directed muscular forces applied to the patella influence the patellofemoral position in vivo, these forces ‡ Address correspondence and reprint requests to Mark D. Grabiner, PhD, School of Kinesiology (M/C 194), University of Illinois at Chicago, Chicago, IL 60608-1516. Funding was received from companies related to products used in this study. See “Acknowledgments” for funding information. 483 484 Owings and Grabiner imum contraction force. In addition, compared with the vastus lateralis muscle, the vastus medialis oblique is composed of a larger percentage of oxidative type I muscle fibers.4 This difference in fiber type would be expected to cause the vastus medialis oblique muscle to possess a slower maximum contraction velocity than the vastus lateralis muscle. Biomechanically, the pennation angle of the vastus medialis oblique muscle is well suited to apply a medially directed force to the patella. However, the larger contraction force and higher contraction velocity of the vastus lateralis muscle would be expected to dominate the movement of the patella unless the activation patterns of these muscles accounts for these differences. A plausible activation strategy of the central nervous system that could diminish the tendency of the vastus lateralis muscle to dominate the movement of the patella would be to activate the vastus medialis oblique muscle earlier than or to a greater relative extent than the vastus lateralis, or both earlier and to a greater extent. We designed a protocol that could test this hypothesis by exploiting the dependency of the potential for mediolateral patellar movement on the knee joint angle. With the knee flexed to 90°, the mediolateral movement of the patella is limited, in part by the geometry of the intercondylar groove. In contrast, with the knee extended, the extent to which the patella can move medially and laterally is increased because the patella then resides in a more shallow aspect of the intercondylar groove. The purpose of the study was to determine whether the activation timing and activation amplitude of the vastus medialis oblique and vastus lateralis muscles are related to the extent to which the patella can move medially and laterally within the intercondylar groove. In addition, we determined whether the activation timing and the activation amplitude of the vastus medialis oblique and vastus lateralis muscles are altered by the presence of patellofemoral pain. Two experimental questions were addressed in the study. First, is the vastus medialis oblique muscle activated earlier or to a greater extent than the vastus lateralis muscle to accommodate knee joint angles at which the potential for mediolateral patellar movement is increased? Second, does the activation timing and the amplitude of the vastus medialis and vastus lateralis muscles of subjects with patellofemoral pain differ from those of asymptomatic subjects? MATERIALS AND METHODS Subjects volunteered to participate in this study and were placed into an experimental group (N ⫽ 20) or a control group (N ⫽ 14) based on the presence of symptoms of patellofemoral pain in either one or both knees. The experimental group consisted of 12 women with a mean age of 33.7 ⫾ 6.9 years, height of 1.65 ⫾ 0.06 meters, and weight of 670.8 ⫾ 156.5 N, and 8 men with a mean age of 29.1 ⫾ 10.7 years, height of 1.77 ⫾ 0.08 meters, and weight of 884.8 ⫾ 220.3 N. When subjects had bilateral knee pain, the knee with the greatest subjectively reported pain was tested. The control group was composed of 4 women with a mean age of 22.3 ⫾ 1.6 years, height of American Journal of Sports Medicine 1.63 ⫾ 0.07 meters, and weight of 667.5 ⫾ 146.7 N, and 10 men with a mean age of 24.5 ⫾ 2.3 years, height of 1.81 ⫾ 0.06 meters, and weight of 752.1 ⫾ 124.2 N. They were healthy, recreationally active, and reported no history of knee injury to the right leg. The protocol prescribed maximum voluntary concentric and eccentric knee extension contractions. However, because of the potential for discomfort of the subjects with patellofemoral pain, especially during eccentric contractions, these subjects performed fewer repetitions and at a slower isokinetic velocity than did the control subjects. The control subjects performed three concentric and three eccentric contractions at 60 deg/sec with their right knee. The patellofemoral pain subjects performed two concentric and two eccentric contractions at 15 deg/sec with the painful knee. The order of concentric and eccentric contractions was randomized. The knee extension contractions were performed on a Kin-Com isokinetic dynamometer (Chattanooga Corporation, Chattanooga, Tennessee). Subjects were seated upright in the dynamometer with their waist and distal thigh stabilized with straps. The hip-trunk angle was fixed at approximately 100°. All contractions were performed through a 60° range of motion. Concentric and eccentric contractions were initiated from a knee flexion angle of 80° and 20°, respectively (full extension, 0°). Bipolar silver-silver chloride surface electrodes (recording diameter, 8 mm; center-to-center distance, 20 mm) were placed over the vastus lateralis, vastus medialis oblique, and biceps femoris muscles of the tested leg. Electrode site preparation, which included shaving, light abrasion, and cleaning with isopropyl alcohol, generally reduced interelectrode resistance to less than 5 and 10 k⍀ for men and women, respectively. The long axis of the electrodes was positioned over each muscle in the assumed direction of the underlying muscle fibers. A reference electrode was placed over the fibular head of the tested leg. The detected EMG signals were amplified using a Noraxon telemetered EMG system (gain, 1000; CMRR, 130 dB; bandpass, 15 to 500 Hz; Noraxon USA, Inc., Scottsdale, Arizona). The transmitted signals were input to an analog-to-digital circuit (Data Translation, 2801A, Marlboro, Massachusetts), digitized at 1 kHz, and stored. The same analog-to-digital circuit was used to digitize the force, speed, and position signals from the Kin-Com dynamometer. Two dependent variables, representing activation timing and activation amplitude, were extracted from the digitized EMG data. The time at which the vastus lateralis and vastus medialis oblique muscles became active was determined with use of a custom interactive graphics and analysis package. The onset and offset times were provided by the software package after the investigator visually positioned a vertical cursor at the location. The muscles were deemed active when the EMG signal surpassed the resting values. Because the contractions were vigorously performed, the onset of activation was unambiguous. The relative timing of the vastus lateralis and the vastus medialis oblique muscles, expressed in millisec- Vol. 30, No. 4, 2002 onds, was determined by subtracting the onset time of the vastus medialis oblique from that of the vastus lateralis. Thus, a negative value indicates that activation of the vastus lateralis muscle preceded activation of the vastus medialis oblique muscle. The activation signals of the vastus lateralis and vastus medialis oblique muscles were full-wave rectified and integrated for 100 ms after activation onset to derive a measure of activation amplitude. This period of time generally preceded the onset of the dynamometer motion that was set, in software, as a threshold of knee extension force required to trigger motion of the Kin-Com dynamometer. Because the analysis window preceded motion of the dynamometer, the EMG signal during this period was not influenced by afferent feedback that signals changes in muscle length and muscle shortening velocity. Furthermore, the initial muscle force generated to trigger motion of the Kin-Com dynamometer is always isometric, regardless of whether the contraction that followed triggering of the dynamometer motion was concentric or eccentric.3 The integrated values for each muscle were expressed as a percentage of the averaged value from the contraction initiated with the knee flexed. A two-by-two (knee joint angle by group) analysis of variance with repeated measures for the knee joint angle was used to analyze activation timing for the two knee joint angles from which the contractions were initiated. Post hoc single-sample t-tests were used to compare the activation timing to the value zero, effectively testing the null hypothesis that between-muscle differences were not significant. Because the activation amplitude during the contraction initiated with the knee extended was normalized to the value derived during the contraction initiated with the knee flexed, single-sample t-tests were used to compare knee joint angles to the value 1. A two-by-two (muscle by group) repeated-measures analysis of variance was used to compare the activation amplitude of the vastus lateralis and the vastus medialis oblique muscles. Statistical analysis was performed with SPSS Version 7.0 (SPSS, Chicago, Illinois), and a P value of 0.05 was accepted as reflecting statistical significance. Motor Control in Subjects with Patellofemoral Pain 485 TABLE 1 Activation Timing (in milliseconds) in the Control Subjects and Subjects with Patellofemoral Pain as a Function of Knee Joint Angle from Which the Contraction was Initiateda Group Flexed Extended Control Patellofemoral pain 5.5 ⫾ 11.0 ⫺1.4 ⫾ 16.7 4.5 ⫾ 10.9 ⫺6.7 ⫾ 18.9 a Activation timing is expressed as a difference (vastus lateralis muscle ⫺ vastus medialis oblique muscle) for which a negative value indicates that the activation of the vastus lateralis muscle preceded that of the vastus medialis oblique muscle. ralis muscle by 5 ⫾ 9 ms (pooled across initial knee joint angles). In contrast, in the patellofemoral pain subjects, activation of the vastus medialis oblique muscle preceded that of the vastus lateralis muscle by 4 ⫾ 15 ms. However, although the analysis of variance revealed significant between-group differences (P ⫽ 0.05) (Table 1), the subsequent post hoc analysis revealed that the activation timing values of the control and patellofemoral pain groups were not significantly different from zero (P ⫽ 0.06 and 0.23, respectively). The vastus medialis oblique muscle was not activated to a greater extent than the vastus lateralis muscle when contractions were initiated with the knee extended, which, compared with the flexed knee position, increased RESULTS The vastus medialis oblique muscle was not activated earlier relative to the vastus lateralis muscle during contractions initiated with the knee extended, a position that, compared with the flexed-knee position, increases the extent to which the patella can move medially and laterally within the intercondylar groove. The effect of the knee joint angle at which contractions were initiated on the activation timing of the vastus medialis oblique and vastus lateralis muscles was not significant (P ⫽ 0.30) (Table 1). In addition, the knee joint angle by group interaction term was not significant (P ⫽ 0.48). The activation timing of the vastus medialis oblique and vastus lateralis muscles was not affected in the subjects with patellofemoral pain, compared with control subjects. Among the control group subjects, activation of the vastus medialis oblique muscle followed that of the vastus late- Figure 1. The normalized activation amplitude of the vastus lateralis muscle was significantly greater than that of the vastus medialis oblique muscle during maximum voluntary knee extensions initiated with the knee in extension in control subjects (N ⫽ 14) and patellofemoral pain subjects (N ⫽ 20). The initial activation amplitude of the vastus medialis oblique and vastus lateralis muscles was significantly greater in the patellofemoral pain subjects compared with the control subjects. The activation levels are normalized to the activation values observed during maximum voluntary knee extension initiated with the knee flexed and that are represented by the value 1 on the vertical axis. 486 Owings and Grabiner the extent to which the patella can move medially and laterally within the intercondylar groove (Fig. 1). In the control subjects, the activation amplitude of the vastus medialis oblique muscle during the contractions initiated with the knee extended was significantly decreased compared with the contractions initiated with the knee flexed (P ⫽ 0.02). However, the decreased activation amplitude of the vastus lateralis muscle was not significant (P ⫽ 0.07). In the patellofemoral pain subjects, activation amplitude of the vastus lateralis muscle during the contractions initiated with the knee extended increased compared with the contractions initiated with the knee flexed (P ⫽ 0.01). However, the increased activation amplitude of the vastus medialis oblique muscle was not significant (P ⫽ 0.18). For both groups of subjects the activation amplitude of the vastus lateralis muscle was significantly larger than that of the vastus medialis oblique muscle during the contraction initiated with the knee extended (P ⫽ 0.02). The muscle-by-group interaction term was not significant (P ⫽ 0.31). Subjects with patellofemoral pain had activation amplitude profiles that were functionally different from those of the asymptomatic control subjects. For the contractions initiated with the knee extended, the activation amplitudes of the vastus medialis oblique and vastus lateralis muscles of the patellofemoral pain subjects were significantly greater than those of the control subjects (P ⬍ 0.01) (Fig. 1). DISCUSSION The protocol used in the current study exploited the dependency on knee joint angle of the extent to which the patella can normally move medially and laterally within the intercondylar groove. We found that the activation timing of the vastus medialis oblique and vastus lateralis muscles of the subjects with patellofemoral pain was not significantly different from that of control subjects. In addition, we found that the activation amplitude patterns for the subjects with patellofemoral pain were significantly different from those of control subjects. We originally reasoned that the central nervous system could adjust for the smaller contractile force and contractile velocity of the vastus medialis muscle by activating it earlier than the vastus lateralis muscle. We also reasoned that such an activation strategy would be evident to a greater extent when contractions were initiated with the knee joint extended, a position that increases the extent to which the patella can normally move medially and laterally within the intercondylar groove. Computer simulation has suggested that activation of the vastus medialis oblique muscle 5 ms earlier than the vastus lateralis muscle can reduce both the laterally directed motion of the patella and the initial peak patellofemoral contact force.8 The results implied that causing the vastus lateralis muscle to be activated 5 ms before the vastus medialis oblique muscle would increase lateralization of the patella and the patellofemoral contact force in excess of that observed when the muscles were activated simultaneously. The results show that, for the open kinetic chain task used in American Journal of Sports Medicine the present study, these two muscles are activated simultaneously in both asymptomatic control subjects and subjects with patellofemoral joint pain. The statistically significant between-group differences with respect to activation amplitude are biomechanically meaningful. First, for the control subjects, the vastus medialis and vastus lateralis muscle activation levels were generally diminished during contractions initiated with the knee joint extended compared with those when the knee joint was flexed, reflecting the differences in the way the central nervous system activates motor units during concentric and eccentric contractions.3 In contrast, the activation levels of patellofemoral pain subjects were generally increased. In particular, compared with the activation level during the contraction initiated with the knee flexed, the increase in vastus lateralis muscle activation level, but not vastus medialis, was significant for the patellofemoral pain subjects. The functional importance of these differences is that, after the onset of motion of the dynamometer, the contraction initiated with the knee extended was eccentric. The significant increase in vastus lateralis muscle activation and the associated increase in contraction force were not paralleled by an increase in vastus medialis muscle activation. This finding raises the testable hypothesis that the subsequent eccentric contraction conditions are accompanied by increased lateralization of the patella and increased patellofemoral pressures and forces. The experimental approach used in the present study in conjunction with a computational model will be required to truly test this hypothesis in vivo. Consistent with our findings, the latency between the vastus medialis oblique and vastus lateralis muscle activation during voluntary concentric contractions by control subjects and patellofemoral pain subjects has previously been reported as not significantly different.5 However, the reflex activation of the vastus medialis oblique muscle occurs significantly later than that of the vastus lateralis in subjects with patellofemoral pain.12, 15 This contrast suggests that the activation timing during reflex and voluntary contractions may not be related in a functionally intuitive manner. The differences we observed in activation amplitude between the control subjects and those with patellofemoral pain are difficult to directly compare with the findings of others. The difficulty arises because our method of EMG analysis is different from those used by other authors. The analyses of EMG data reported by others during dynamic muscle contractions have not generally been independent of the effects of muscle lengthening and shortening, for example, during level gait, stair climbing, and ramp walking.9, 11 Our analysis of the initial 100 ms of activation, a period during which the contraction is essentially isometric, precludes influence by afferent activity related to muscle length changes. However, we can make one betweenstudy comparison. In asymptomatic control subjects in the present study, the normalized activation amplitude of the vastus medialis oblique muscle was, on average, about 14% smaller than that of the vastus lateralis muscle. This between-muscle difference is similar to the 11% difference previously reported for uninjured subjects.2 Thus, by our Vol. 30, No. 4, 2002 methods, the vastus lateralis muscle of asymptomatic control subjects consistently has a larger initial activation amplitude than does the vastus medialis muscle. In other studies in which isolated knee extension was performed on a dynamometer, analysis of the EMG data is often reported as an activation ratio of vastus medialis oblique:vastus lateralis muscle.1, 6 In the present study, the ratios for the control and patellofemoral pain subjects were 0.82 and 0.77, respectively. These values are quite different from the ratios reported by Laprade et al.,6 Sheehy et al.,11 and Boucher et al.,1 which ranged from 1.3 to 2.0 and 1.1 to 2.25 for control subjects and patellofemoral pain subjects, respectively. These differences reflect, in part, the very different contraction conditions during which the EMG data were collected and the analysis window used to quantify the signal. However, we believe that the use of activation ratios, which presume a linear force: EMG relationship for each muscle, can be problematic if the relationships demonstrate nonlinearity. We recognize that a number of limitations were present in our experimental design. First, the subjects in the patellofemoral pain group were a convenience sample, recruited using criteria of activity-related patellofemoral pain but without a history of knee surgery. The subjects’ symptoms of patellofemoral pain varied both in intensity and duration, and thus, in some respects, were heterogeneous. Nevertheless, as a group, these subjects were associated with a pattern of activation amplitude that was different from that of control subjects. Another potential limitation of the study relates to the different isokinetic speeds used to test the control subjects (60 deg/sec) and the patellofemoral pain subjects (15 deg/sec). The slow speed was selected for the patellofemoral pain subjects in an effort to reduce any pain or discomfort that they may have experienced or anticipated. However, because all of our measurements were acquired before the onset of dynamometer motion and because we were not interested in the muscle strength differences between the groups of subjects, the speed and strength disparities were not considered to have been experimental confounds. In retrospect, it would have been valuable to make bilateral measurements, especially on the patellofemoral pain subjects. The absence of bilateral measurements is not actually a limitation of the study. However, bilateral measurements would have allowed discrimination of a localized unilateral outcome associated with the pathologic condition from that of a general influence. The activation levels of the vastus medialis and vastus lateralis muscles of the subjects with patellofemoral pain were consistent with a laterally tracking patella. The unexpectedly large activation amplitudes of both muscles in the patellofemoral pain subjects compared with the control subjects are notable. This finding provides evidence that patellofemoral pain is associated with a disruption in Motor Control in Subjects with Patellofemoral Pain 487 the control of the knee extensor muscles during the initial activation of eccentric contractions. Although it is not possible to ascribe a causal effect of the altered activation timing and amplitude to the presence of patellofemoral pain, these findings raise follow-up questions. Are the altered activation patterns sensitive to rehabilitation? Do subjective reports of knee joint pain and function parallel changes in the activation patterns as a result of rehabilitation? ACKNOWLEDGMENTS The authors gratefully acknowledge funding for the study from the Chattanooga Corporation, Chattanooga, Tennessee, and Bauerfiend USA, Corporation, Atlanta, Georgia. The authors also thank Michele E. George and Thomas M. Lundin for their assistance in the data collection and analysis. REFERENCES 1. 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