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Intra-articular knee joint effusion induces quadriceps avoidance gait patterns1
Clinical Biomechanics 15 (2000) 147±159
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Clinical Biomechanics Award 1999
Intra-articular knee joint eusion induces quadriceps avoidance gait patterns 1 Michael R. Torry a,*, Michael J. Decker a, Randall W. Viola b, Dennis D. OÕConnor a, J. Richard Steadman b a
Steadman±Hawkins Sports Medicine Foundations, Vail, CO 81657, USA b Steadman±Hawkins Sports Medicine Clinic, Vail, CO, 81657, USA Received 1 September 1999; accepted 14 October 1999
Abstract Objectives. (1) To identify adaptations caused by intra-articular knee joint eusion during walking and (2) to determine if knee joint eusion may be a causative factor in promoting quadriceps avoidance gait patterns. Design. Gait testing of 14 healthy individuals who underwent incremental saline injections of the knee joint capsule. Background. Gait adaptations have been reported in the literature for knee injured and rehabilitating individuals. Knee joint capsular aerent activity can in¯uence knee joint function. Methods. Gait analysis was employed in a pre- and post-test, repeated measures design to determine lower extremity joint kinematics, kinetics, energetics and thigh EMG adaptations due to intra-articular knee joint eusion. Results. Knee eusion caused an increase in hip and knee ¯exion through the stance phase. Knee extensor torque, impulse and negative and positive work were diminished with increased eusion levels. Quadriceps activity decreased and hamstring activity increased due to intra-articular knee joint eusion. Discussion. These adaptations cannot be attributed to an injury, surgery or rehabilitation. Thus, the results of this experiment suggest knee joint capsular distention, via knee joint eusion, may be responsible for many gait adaptations reported for knee injured individuals in previous investigations. Conclusions. Knee joint eusion and the subsequent capsular distention can cause major alterations in the normal gait cycle and can be considered a causative factor promoting the acquisition of quadriceps avoidance gait patterns. Relevance This study provides reference data on the eects of intra-articular knee joint eusion on gait parameters by which future studies of injured or rehabilitating individuals can be compared. Ó 2000 Elsevier Science Ltd. All rights reserved. Keywords: Gait; Knee; Eusion; Torque; Power; EMG; ACL
1. Introduction Intra-articular knee joint eusion accompanies nearly all knee injuries or surgeries. Eusions develop not only after knee trauma, but because of many degenerative conditions as well [1,2]. In either case, eusion may inhibit rehabilitation, delay the return to functional activities or promote adaptations that may alter normal functional patterns. Understanding the in¯uence eu-
*
Corresponding author. E-mail address: [email protected] (M.R. Torry). 1 Presented at the XVII Congress of the International Society of Biomechanics, Calgares, Canada, 8±13 August 1999.
sion may have on lower extremity gait function may help clinicians more clearly understand a myriad of gait abnormalities. Investigators have demonstrated the existence of knee joint capsular mechanoreceptors and their in¯uence on quadriceps function by injecting ¯uids into the knee joint capsule of healthy individuals [3±5]. These studies report a reduction in the Homan re¯exes of the quadriceps musculature. Furthermore, these investigators observed that the vastus medialis sustained the most dramatic inhibitory eect compared to other quadriceps musculature. Other studies have reported substantial reductions in volitional isometric and isokinetic knee extensor torque, and in quadriceps EMG activity during knee extensor exercises [6±8]. It is the consensus of these
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investigators that the inhibitory eects observed in these studies were a result of inhibitory aerent impulses produced by joint capsular distention [3±8]. Extensor torque reduction has also been identi®ed in the gait patterns of knee injured individuals [9±11]. Speci®cally, anterior cruciate ligament (ACL) de®cient and ACL reconstructed individuals have been reported to walk with reduced knee extensor torque and power patterns and the source of their mechanical work is modi®ed [9±11]. These ®ndings are supported by observations of increased electromyographic (EMG) activity in the hamstrings and reduced EMG activity in the quadriceps [12±16]. Furthermore, quadriceps avoidance gait patterns have been shown to be related to the time since injury and thus, are considered a learned response [10,17]. Although hypotheses have been proposed, the mechanism of how individuals learn these adaptations has not been experimentally identi®ed [18,19]. Neuro-biological studies have supported an integrated role of joint capsular receptors during normal locomotion and distinct, parallel aerent spinal pathways have been identi®ed as having direct and indirect input into the three functional levels of the cerebellum [20±26]. In animal studies, increased anterior±posterior tibial displacement at the knee joint have been shown to elicit re¯ex arcs mediated by the multiple mechanoreceptors located in capsular tissue and ligament bundles [27±31]. The inhibitory eect of this aerent activity on eerent motor pathways has been well documented in various animals [32±37] and humans [38±41]. Cole et al. [28] reported that as little as 200±500 lm of tibial displacement relative to the femur in the cat knee produced marked joint aerent discharge, suggesting that clinically undetectable displacement may elicit mechanoreceptor responses. Correspondingly, Hasan et al. [42] showed that the human ACL de®cient knee experiences greater anterior±posterior tibio-femoral displacements during gait compared to healthy subjects. Thus, it is plausible that these small displacements occurring during gait can distend the joint capsule suciently to elicit aerent activity that eect and modify the locomotor program over time. The ®rst purpose of this study was to document the eects of experimentally induced eusion of the knee joint on the kinematic, kinetic, energetic and EMG pro®les of the lower extremity during walking. The results of this study provide baseline eects of eusion on knee joint function by which future gait analysis of injured or rehabilitating individuals may be compared. Furthermore, the existence of the quadriceps avoidance patterns and reduced extensor torque patterns has been observed in ACL de®cient and ACL reconstructed individuals, respectively. To date the neurological mechanism that in¯uences individuals to learn these adaptations has not been identi®ed. Thus, the second purpose was to determine if knee joint capsular dis-
tention could be a mechanism that induces quadriceps avoidance gait patterns. We propose that if the classic adaptations (increased knee ¯exion, decreased knee extensor torque, decreased knee power and work) are apparent due to injection of the knee joint capsule with saline, then knee joint capsular distention may be a causative factor promoting the acquisition of the quadriceps avoidance patterns. 2. Methods 2.1. Subjects Fourteen healthy subjects (9 male; 5 female) with no history of lower extremity pathology volunteered as the test group (mean age 29.5, SD 5.1 yr; mean mass 78.50, SD 4.0 kg; mean height 184.2, SD 4.2 cm). Prior to testing, each participant provided their written informed consent according to a protocol approved by an Institutional Review Board retained by the Vail Valley Medical Center. 2.2. Instrumentation and data processing Lower extremity performance during level ground walking were recorded using a three-dimensional motion analysis system (Motion Analysis, Santa Rosa, CA, USA). A four segment, rigid-link model of the lower limb was de®ned by 13 retro-re¯ective, spherical markers (diameter 25 mm) that delineated segment coordinate systems that were related to ®xed anatomic reference systems [43]. Five synchronized cameras captured the gait motion at a frequency of 120 Hz. The cameras were calibrated with mean residual errors in the range of 1.25±2.55 mm over a volumetric space of 1.50 ´ 1.10 ´ 1.50 m3 . The coordinate data for each marker trajectory were smoothed using a fourth-order Butterworth ®lter with a ®ve Hz cut-o frequency. The magnitude of the segmental masses and the mass center location of the lower extremity, along with their moment of inertia, were estimated using a mathematical model [44], and segmental masses reported by Dempster [45]. Force data were sampled at a frequency of 1200 Hz. Center of pressure were calculated from the sampled ground reaction forces [46]. Dynamic joint torque data were calculated by combining the anthropometric, kinematic and force data in an inverse dynamic analysis [46]. Net hip and knee sagittal plane joint moments were calculated throughout the stance phase, with a positive internal moment acting in the direction of hip and knee extension, respectively. Instantaneous mechanical power for each joint were calculated by taking the product of the joint torque and joint angular velocity and were reported as positive values representing energy generation
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and negative values representing energy absorption [46]. Calculating the area under the power curve represents work. Thus, area under the positive power curve indicates that the joint is acting concentrically to generate energy (positive work), while the area under the negative power curve indicates that the joint is acting eccentrically to absorb energy (negative work) [10,11,46]. The kinetic and energetic data were scaled by dividing each value in the time series by the product of the subjectÕs weight (BW) and height (HT), and multiplying by 100 [9,47]. Custom software utilizing a cubic spline function was used to time normalize the data based on the number of data points in the trial with the largest number of points to produce time series data expressed as 0±100% of the stance phase. Ensemble averages of time series data were averaged for the entire group (N 140 trials) for graphical purposes. To monitor muscular activity patterns, the skin of each electrode site was shaved and cleaned with alcohol. Pre-gelled, silver±silver/chloride bipolar surface electrodes (Medicotest A/S, Rugmaken, Denmark) were placed over the vastus medialis, vastus lateralis, biceps femoris, and the medial hamstrings (semitendinosus and semimembranosus) according to Basmajiian and Deluca [48] and Delagi et al. [49]. The electrodes were placed over each muscle belly in line with the direction of the ®bers and with a center to center distance of approximately 2.5 cm. Placement of electrodes was con®rmed for each muscle with manual muscle testing and visual biofeedback monitoring. A single ground electrode was placed over the anterior tibial spine. The input impedance of the EMG ampli®er was <10 MX, with a common mode of rejection ratio of 85 dB and a gain of 1000. Raw dynamic EMG and isometric, maximum voluntary contractions (MVCs) for each muscle were collected with an eight channel Noraxon Telemetry (Noraxon, Scottsdale, AZ, USA) unit on-line to the Motion Analysis A/D board, sampling at a frequency of 1200 Hz. Pre-test MVCs were collected using methods described previously by Lange et al. [50]. To ensure true MVC records, the subjects were allowed to practice the contractions for several minutes prior to testing. Visual biofeedback was used to help the subjects isolate and concentrate on the intended musculature during the practice session. MVC data were processed with a 50 ms root-mean square (RMS) moving window [51]. EMG reference values were calculated for each muscle using the average of the ®ve peak EMG signals and represented 100% MVC. The mean peak amplitude of the ®ve MVCs was used to scale the dynamic contractions recorded during each gait test. Stance phase trial data were processed with a 15 ms RMS moving window and were scaled by dividing by each subjectÕs representative MVC and multiplying by 100 [50,51]. Thus, EMG gait values are
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reported as a percentage of the MVC. The scaled data were further quanti®ed by dividing the stance phase into four equal time intervals and averaging the data at 25% increments (0±25%, 26±50%, 51±75%, 76±100%) totaling 0±100% of the normalization base. These 25% intervals were analyzed to allow direct comparisons to be made in conjunction with knee power transition periods that delineate speci®c energy absorption (K1, Fig. 6) and energy generation (K2, Fig. 6) phases within the stance phase. 2.3. Walking protocol The subjects were allowed to familiarize themselves with the walkway and testing apparatus prior to testing. Each participant practiced walking on the six meter walkway at a self-selected speed until they could provide a consistent foot strike on the force platform. During data collection, each subject completed 10 walking trials. Only trials within 2.5% of the self-selected speed, and where full foot placement was achieved on the force platform, were considered acceptable for analysis. 2.4. Knee eusion and test protocol After 10 pre-eusion gait trials were collected, a series of saline injections were administered to simulate knee joint eusion and cause joint capsular distention. A physician (RMV) administered all injections using an aseptic sterile technique. The entire knee area was shaved and cleaned with alcohol and then bathed with a sterile 10% betadine solution. The injection site was then wiped with Povidone±Iodine in a sterile fashion. Immediately following each injection, the site was cleaned with alcohol and a sterile dressing applied. This procedure was carried out before and after each injection. The subject was placed in a seated position with their test limb fully extended. The ®rst injection consisted of a 3.0 cm3 mixture of 1% Lidocaine (1.5 cm3 ) and 25% Marcaine (1.5 cm3 ) introduced into the skin and subcutaneous tissue at the lateral supra patellar position with a 25 gauge needle. Care was taken not to penetrate the joint capsule during the numbing injection. After super®cial numbing had occurred, an 18 gauge needle was used to administer an infusion of 0.9% saline [4]. The ®rst saline injection accounted for 20 cm3 of ¯uid. Each successive injection accounted for an additional 30 cm3 saline added intra-articularly. At the time of each injection, an intra-articular pressure reading (mm Hg) was recorded via a pressure transducer aligned in parallel with the syringe [4,52]. A two-way stopcock located on the end of the syringe could be turned quickly to negate saline back-¯ow and allow for immediate pressure readings after the injection. The subject was then helped to stand upright and instructed to put full weight bearing pressure on the injected knee, and a weight
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bearing joint capsular pressure reading was recorded. The needle was withdrawn, a sterile dressing was applied and the individual performed 10 gait trials. The stretch-relax cycle for the human knee joint capsule has been estimated to be approximately 10 min [33,52]. Thus, all gait tests were completed in under a 10min time frame. After the fourth injection and subsequent gait test, the saline was aspirated from the knee joint. The total amount of saline removed for each subject was recorded. A ®nal sterile dressing was applied to the injection site and the subject performed the last set of 10 gait trials. The subjects were examined by a physician at 24, 48 h, and 7 days post-testing to ascertain recovery. 2.5. Statistical analysis The kinematic analysis yielded mean hip and knee joint angles at heel contact and mean hip and knee joint angles through the stance phase (0±100%). The kinetic analysis yielded peak knee extensor joint torque, extensor hip and knee joint angular impulse over the stance phase and hip and knee joint extensor angular impulse from 0% to 50% of the stance phase. Energetic variables included total positive hip work and total positive and negative knee work through the stance phase (0±100%), positive hip work at 0±30%, and total positive and negative knee work between 0% and 25% of the stance phase. These phases correspond to speci®c power transition periods described by Winter, 1990 and have been previously reported in ACL injured individuals [10,11]. EMG variables included the EMG data calculated over the 0±25% and 26±50% intervals of stance phase. Dierences in the kinematic, kinetic, work and EMG parameters between test conditions were analyzed in a repeated measures analysis of variance design (alpha 0.05) with a Bonferroni adjusted post hoc test to identify speci®c contrasts between conditions. To determine the relationship between the amount of ¯uid in the knee and the degree that it aected torque output, a product-moment correlation between the peak knee extensor torque and the knee joint extensor angular impulse and the weight bearing intra-articular pressures were also conducted. 3. Results 3.1. Kinematics The general eect of eusion on hip and knee joint kinematics was to cause a more ¯exed position at heel contact and throughout the stance phase (Table 1). Compared to pre-eusion values, individuals increased hip ¯exion angle at heel contact 1.1% at 20 cm3
(P 0:673), and 7.6% with 80 cm3 (P < 0:001) knee joint injection. Compared to pre-eusion trials, average hip ¯exion angle through the stance phase increased 5.0% (P 0:180), 28.4% (P < 0:001), and 48.0% (P < 0:001) for eusion levels of 20, 50 and 80 cm3 , respectively (Fig. 1). Hip angle at heel contact and average hip ¯exion angle through stance returned to within 3.1% and 6.1% of pre-eusion values after aspiration of the ¯uid (P > 0.10). Knee angle at heel contact increased in ¯exion 16.2% (P 0.312), 40.1% (P < 0.001) and 63.6% (P < 0.001) for eusion levels of 20, 50 and 80 cm3 , respectively. Average knee ¯exion angle through stance increased 6% for 20 cm3 (P 0.013), and 11.3% (P < 0.001) and 25.2% (P < 0.001) for 50 and 80 cm3 conditions (Fig. 2). Knee kinematics returned to within 1.2% of the pre-eusion values after aspiration (P > 0.05). 3.2. Kinetics Hip joint torque values and ensemble hip joint torque time series data for all conditions are presented in Table 1 and Fig. 3. Hip extensor impulse in the ®rst half of stance (0±50%) increased 2.0% (P 0.60), 7.2% (P 0.052) and 20.1% (P < 0.001) for eusion levels of 20, 50 and 80 cm3 , respectively. These values returned to within 0.56% of the pre-eusion values after aspiration (P 0.86). The general eect of eusion on stance phase knee joint torque patterns was a reduction in the extensor peak torque, extensor impulse in the ®rst half (0±50%) of stance and a shift toward an extensor torque in the latter half (55±80%) of stance (Table 1 and Fig. 4). Peak knee extensor torque decreased 12.3% (P < 0.001), 12.7% (P < 0.001), and 19.5% (P < 0.001) for eusion levels of 20, 50 and 80 cm3 , and returned to within 1.7% of preeusion values after aspiration (P 0.384). Knee extensor angular impulse calculated over the ®rst half of stance decreased 12.6% (P < 0.001), 20.2% (P < 0.001), and 30.2% (P < 0.001) at eusion levels of 20, 50 and 80 cm3 , respectively. Knee joint angular impulse returned to within 5.9% of pre-eusion values after aspiration (P 0.017). Knee joint ¯exor impulse was unchanged at 20 cm3 (P 0.563), but reduced 56.0% (P < 0.001) at 50 cm3 and was eliminated in most subjects with 80 cm3 of eusion. Knee joint ¯exor impulse returned to within 4.0% of pre-eusion values after aspiration (P 0.641). Mean intra-articular weight-bearing pressure increased 42.7% between 20 and 80 cm3 eusion levels (Table 1). Correlation of the weight bearing intra-articular pressure and the peak knee extensor torque and knee extensor angular impulse occurring during the ®rst half of stance were r ÿ0:44 (P 0.003) and r ÿ0:68 (P < 0.0001), respectively; indicating that as intra-articular pressure increased, peak knee extensor torque and
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Table 1 Mean values and {SD} across test conditions for kinematic, kinetic and energetic variablesa Variable
Kinematics Hip angle at heel contact Knee angle at heel contact Average hip angle through stance Average knee angle through stance Kinetics Hip extensor impulse (0±50%) Knee extensor impluse (0±50%) Peak extensor knee torque Knee ¯exion impulse (50±100%) Work Total positive hip Total positive knee Positive hip (0±50%) Negative knee (0±25%) Positive knee (26±50%)
Weight bearing intra-articular pressure a *
Condition Pre-eusion
20 cm3
50 cm3
80 cm3
Aspiration
ÿ21.38 {3.91} ÿ3.45 {2.67} ÿ5.77 {1.41} ÿ19.52 {2.37}
ÿ21.62 {4.15} ÿ4.12 {3.39} ÿ6.08 {1.92} ÿ20.64 {2.34}
ÿ20.6 {5.05} ÿ5.76 {2.05} ÿ8.06 {2.25} ÿ22.01 {2.12}
ÿ23.16 {4.56} ÿ9.49 {1.92} ÿ11.18 {1.59} ÿ26.13 {2.54}
ÿ20.67 {3.63} ÿ3.46 {2.67} ÿ6.15 {1.64} ÿ19.28 {2.35}
0.52 {0.26} 0.89 {0.18} 5.69 {0.63} ÿ0.35 {0.15}
0.53 {0.21} 0.78 {0.23} 4.99 {0.78} ÿ0.36 {0.09}
0.56 {0.21} 0.71 {0.21} 4.97 {0.84} ÿ0.15 {0.09}
0.66 {0.28} 0.62 {0.11} 4.58 {0.97} ÿ0.01 {0.01}
0.53 {0.26} 0.83 {0.17} 5.59 {0.61} ÿ0.33 {0.10}
0.31 {0.25} 0.73 {0.25} 0.52 {0.26} ÿ0.66 {0.22} 0.36 {0.12}
0.32 {0.21} 0.68 {0.22} 0.53 {0.21} ÿ0.61 {0.20} 0.34 {0.11}
0.35 {0.22} 0.67 {0.22} 0.56 {0.21} ÿ0.59 {0.24} 0.31 {0.07}
0.49 {0.35} 0.51 {0.18} 0.66 {0.28} ÿ0.43 {0.15} 0.21 {0.07}
0.30 {0.29} 0.72 {0.23} 0.53 {0.26} ÿ0.65 {0.21} 0.36 {0.11}
0 {0.00}
32.84 {15.09}
68.50 {22.174}
102.82 {30.56}
NA
Kinematics in degrees; torque in %BW.HT; impulse in %BW.HTs; work in %BW.HT; pressure in mm Hg. Values signi®cantly dier from pre-eusion condition; P < 0.015.
knee extensor impulse decreased. Average ¯uid removed during aspiration was 62 cm3 (77.6%). 3.3. Energetics Time series hip and knee joint power patterns are presented in Figs. 5 and 6, and hip and knee work estimates are listed in Table 1. Compared to pre-effusion values, total positive work at the hip increased 2.1% (P 0.89), 8.7% (P 0.46) and 29.0% (P 0.001) for injection levels 20, 50 and 80 cm3 , respectively. Hip positive work during the ®rst half of stance, increased 38.5% (P 0.02), 48.5% (P < 0.001), and 56.6% (P < 0.001) for the successive eusion levels. Hip positive work returned to near normal values after aspiration (P 0.77). Total positive knee work decreased 5.2% (P 0.32), 9.0% (P 0.20), and 29.7% (P < 0.001) over the entire stance phase for 20, 50 and
80 cm3 eusion levels. Total positive knee work returned to within 2.0% of pre-eusion values after aspiration (P 0.773). To investigate speci®c changes in knee work during the stance phase, discrete intervals de®ned by transition periods in the knee joint power curves were also analyzed. The kneeÕs ability to absorb force was reduced as negative knee work occurring between 0% and 25% of stance (K1) decreased 8.3% (P 0.22), 11.3% (P 0.10), and 34.1% (P < 0.001) for the successive eusion levels, and returned to within 1.9% after aspiration (P 0.772). The kneeÕs ability to generate force was also reduced as positive knee power calculated between 26% and 50% (K2) decreased 6.2% (P 0.405), 14.3% (P 0.05), 42.5% (P < 0.001) for eusion levels of 20, 50 and 80 cm3 , respectively. Positive knee power in this interval returned to within 2.1% of pre-eusion levels after aspiration (P 0.751).
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Fig. 1. Stance phase hip position curves. Positive and negative values represent extended and ¯exed positions.
3.4. Electromyography In general, quadriceps activity was inhibited and hamstring activity was facilitated during the energy absorption phase (K1) of the knee during stance. Quadriceps and hamstring EMG activity responses due to eusion during the ®rst 25% of stance are depicted in Fig. 7a and b. Vastus medialis activity during K1 decreased 13.0% (P < 0.001), 20.6% (P < 0.001) and 31.4% (P < 0.001) for 20, 50 and 80 cm3 levels of eusion and remained 4.2% below pre-eusion values after aspiration (P 0.152). Vastus lateralis activity during this same time period decreased 9.2% (P 0.011), 27.7%
(P < 0.001) and 42.2% (P < 0.001) at each successive effusion level and remained 5.7% below pre-eusion levels after aspiration (P 0.13). Rectus femoris activity was less aected by eusion but still decreased 4.1% (P 0.063), 3.4% (P 0.125) and 17.2% (P < 0.001) with 20, 50 and 80 cm3 and returned to within 1.0% of preeusion values (P 0.882). Medial hamstring activity increased 4.1% (P 0.16), 10.5% (P < 0.001) and 22.5% (P < 0.001) for successive eusion levels. Medial hamstring activity returned to within 5.0% of pre-eusion levels after aspiration (P 0.883). Biceps femoris activity increased 0.6% (P 0.83) at 20 cm3 , 6.9% (P 0.02) at 50 cm3 and 13.7% (P < 0.001) at 80 cm3 of eusion,
Fig. 2. Stance phase knee position curves. Negative values represent a ¯exed knee.
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Fig. 3. Stance phase hip torque (internal moment). Positive and negative values represent net extensor and ¯exor torques.
respectively. Biceps femoris activity returned to within 2.3% of pre-eusion values after aspiration (P 0.465). Similar to the EMG results during the K1 interval, quadriceps activity decreased while hamstring activity increased during the major energy generation phase (K2) of the knee during stance. The quadriceps and hamstring EMG values for this phase are depicted in Fig. 7c and d. Vastus medialis activity decreased 8.8%, 16.4%, and 25.0% (all P < 0.001) for eusion levels of 20, 50 and 80 cm3 , respectively and returned to 3.4% of preeusion values after aspiration (P 0.140). Vastus lateralis EMG decreased 3.5% (P 0.29), 21.3% (P < 0.001), and 41.2% (P < 0.001) for the successive ef-
fusion levels and returned to within 4.0% after aspiration (P 224). Rectus femoris activity decreased 3.8% (P 0.43), 28.7% (P < 0.001) and 50.4% (P < 0.001) with increased eusion in the knee and returned to within 6.6% (P 0.882) of pre-eusion values after aspiration. Medial hamstring activity increased 2.5% (p 0.20), 6.6% (P < 0.001) and 14.9% (P < 0.001) for the successive eusion levels and returned to within 2.7% (P 0.172) of pre-eusion values. Biceps femoris activity increased 0.4% (P 0.87), 8.5% (P < 0.001), and 16.6% (P < 0.001) for eusion levels of 20, 50 and 80 cm3 , and returned to within 4.3% of pre-eusion values after aspiration (P 0.068).
Fig. 4. Stance phase knee torque (internal moment). Positive and negative values represent net extensor and ¯exor torques.
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Fig. 5. Stance phase hip power curves. Positive and negative values indicate energy generation and absorption.
4. Discussion The general eect of eusion on walking patterns was a more crouched style of gait, a decrease in torque, power and work produced at the knee joint and increased extensor torque, power and work produced at the hip joint. As the knee extensor function diminished in early stance, the subjects adapted by increasing hip extensor torque and positive work to help maintain total support for the limb and to provide forward progression to the walking motion. This compensatory pattern has been observed in knee injured individuals [10,11].
The reduction in energy absorption and generation at the knee are supported by the EMG parameters investigated in this study. EMG of all quadriceps muscular activity was reduced with intra-articular knee joint effusion. The vastus medialis was signi®cantly inhibited at 20 cm3 while larger eusion volumes were needed to produce the same results in the vastus lateralis and rectus femoris. The rectus femoris was least aected and we attribute this result to its bi-articulate nature and its in¯uence on the hip joint. Nonetheless, the rectus femoris was inhibited 17% at 80 cm3 ; indicating other hip ¯exors, such as the iliopsoas, may adapt to create a
Fig. 6. Stance phase knee power curves. Positive and negative values indicate energy generation and absorption.
Fig. 7. Electromyographic activity reported as a percent of MVC for all muscles and all conditions. Graph (a) Quadriceps activity during 0±25% (K1) period of stance; (b) Hamstring activity during 0±25% (K1) period of stance; (c) Quadriceps activity during 26±50% (K2) period of stance; (d) Hamstring activity during 26±50% (K2) period of stance. Solid icons represent values that are signi®cantly dierent then pre-eusion values (P < 0.015).
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majority of the compensatory (positive) work output for the hip joint. The secondary purpose of this investigation was to determine if knee joint capsular distention, via intraarticular knee joint eusion, could cause healthy individuals to walk with knee joint position, torque and power patterns similar to those that have been reported for ACL injured and rehabilitating individuals. Anterior cruciate ligament injuries have been shown to cause neuromuscular adaptations aecting the entire lower extremity [9±11]. It has been suggested that these adaptations may be mediated by: (1) brace wear [53], (2) training eects produced by rehabilitation [18,54], or (3) altered neuromuscular strategies due to the initial injury [18,19]. The results of the present study are not constrained by these factors as only healthy individuals were tested. Thus, rival adaptive mechanisms (i.e. injury, surgery or rehabilitation) could not have caused these patterns. The hip and knee kinematic and kinetic patterns observed in the present study are characteristic of the gait patterns reported for ACL de®cient and ACL reconstructed individuals [9±11,17]. DeVita et al. [10] investigated the time course of development of the quadriceps avoidance gait pattern by testing ACL injured individuals two weeks after injury but before surgery, and at three weeks post-reconstruction surgery. Results of that study indicated that at two weeks postinjury, ACL injured individuals maintained an extensor torque pattern at the knee. The knee joint torque and power patterns reported by DeVita et al. [10] are very similar to the joint torque and power patterns observed for the 50 and 80 cm3 conditions in the present study. DeVita et al. [10] also analyzed the gait patterns of ACL reconstructed patients at ®ve weeks post-reconstruction. At this time period, the authors noted that the extensor torque was still suppressed but showed trends of returning toward a normal bi-phasic, extensor±¯exor pattern. Again, these patterns bear close resemblance to the patterns observed with mild eusion (20 cm3 ) of the knee joint in the present study. Although eusion was not reported, it is reasonable to assume that the subjects utilized by DeVita et al. [10] experienced residual knee joint eusion after their surgery that may have contributed to those ®ndings. Birac et al. [17] reported that the development of the quadriceps avoidance pattern in ACL de®cient patients was related to the time since injury. Hurwitz et al. [18] and Hogervorst and Brand [19] proposed that the learning of the quadriceps avoidance pattern was most likely due to repetitive experiences that alter the locomotor system. However, to date, the aerent input responsible for this neuro-modulation has not been identi®ed. The present study supports the premise that joint capsular distention and mechanoreceptor aerent responses are the primary structures that provide this
information to the central nervous system. We propose that in ACL de®cient and reconstructed individuals, joint capsular distention, caused by excessive displacement of the tibia relative to the femur, stimulates capsular aerent activity in response to capsular stretching. The aerent information is passed to the spinal cord via the dorsal root ganglion. The dorsal and ventral spinocerebellar tracts convey the peripheral aerent information from the trunk and legs to the cerebellar cortex where this information is fractionated and relayed to the higher and lower motor cortices [55±57]. We base this mechanism on the following observations: (1) the results of the present study and previous investigations outlining distinct EMG and mechanical de®cits due to joint capsular distention and subsequent aerent responses [31±41], (2) previous research supporting excessive translation of the tibia relative to the femur during the gait cycle in ACL de®cient patients [42] and (3) evidence that a minimal amount of joint capsular distention has been shown to stimulate aerent responses [29,30]. Ultimately, the basis of this mechanism depends on the degree of tibio-femoral knee joint displacement and, as mentioned above, applies well to ACL de®cient persons. It is plausible that this mechanism may also apply to ACL reconstructed individuals as well. Successfully ACL reconstructed individuals are assumed to be structurally and mechanically sound after surgery. Nevertheless, there is considerable empirical evidence (KT-1000 scores [58,59]) and subjective clinical criteria [59,60] to argue that even in a surgically well reconstructed knee, there would exist some tibio-femoral displacement that was not inherent to that knee prior to injury or surgery. This ``clinically insigni®cant'' laxity may also distend the knee joint during impact activities, causing sucient tibio-femoral displacement and joint capsular distention. However, scienti®c evidence of tibio-femoral displacement during walking or other dynamic activities, to our knowledge, has not been reported in ACL reconstructed individuals. It is well documented that ACL injured and ACL reconstructed individuals tend to have residual quadriceps weakness (particularly vastus medialis) long after their injury or surgery. This weakness has been shown to aect the lower extremity gait in these individuals [54]. Hurley et al. (1992), utilizing a superimposed twitch technique, reported a signi®cant quadriceps strength de®cit in ACL injured individuals prior to participating in a rehabilitation program. Subsequent analysis after completion of an intensive rehabilitation program also demonstrated a residual quadriceps strength de®cit despite the absence of pain or eusion during testing [61]. The authors concluded that excessive joint motion together with aerent responses may limit the central nervous system drive to the quadriceps. In agreement with previous studies [4,5], the present study observed that the vastus medialis was most inhibited by knee joint
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eusion. Vastus medialis insuciency due to aerent inhibition would contribute to aberrant patellar tracking and possibly retro-patellar pain. This study supports the notion that residual or re-current bouts of knee joint eusion after knee injury may account for some of this residual weakness that may lead to extensor mechanism dysfunction. Several researchers have reported that biceps femoris activity is increased in ACL de®cient and ACL reconstructed patients [13,14,16]. These authors suggest that this is a protective mechanism that prevents anterior tibial translation and limits internal rotation thus protecting the knee from a pivoting motion. All hamstring EMG activity increased in the present study despite no inherent joint structural injury or laxity. This suggests that the increased hamstring activity observed by previous investigators [13,14,16] may be a result of ¯exor± extensor muscle synergy brought about by aerent neuro-modulation in order to reduce knee stress. The hamstring muscles have been demonstrated to assume a joint stabilizing role in the ACL de®cient individual [14,62]. However, the hamstrings are ineective at reducing anterior displacement at knee angles between 0° and 15° of ¯exion [63]. With eusion, knee ¯exion angle through stance was increased and subjects walked in a more ¯exed position. This position range allows greater hamstring synergy for knee joint stability [62]. Furthermore, the inhibition of the quadriceps and facilitation of the hamstring musculature in the present study would act to stabilize the knee joint by balancing the knee agonists and antagonists during the gait cycle. Solomonow et al. [62] suggested that these knee stabilizing factors are a function of an ACL-hamstring re¯ex arc. This study supports the existence of a joint capsular aerent±eerent pathway strong enough to induce immediate quadriceps and hamstring EMG alterations acting to stabilize the knee joint. Alternatively, the EMG observations in the present study may simply be a result of muscle force±length relationships due to positional changes. Several authors have reported quadriceps muscular inhibition to be a factor of hip and knee joint angle [64,65]. Although no subject complained of pain, seven subjects did comment on the ``tightness'' or ``pressure'' sensations in the knee with 80 cm3 of eusion. At the higher volume levels, pressure may have stimulated the nociceptive system surrounding the knee joint. Thus, the subjects may have changed their walking pattern in an attempt to reduce this pressure by selectively altering knee ¯exion angle to around 30°; an angle shown to reduce intra-articular knee pressure [52]. Correspondingly, this study does not discount possible in¯uences of the nociceptive system on stimulating the ¯exor withdrawal response [66,67]. However, compelling experimental evidence of painfree, ¯exor facilitation exists in the literature [41,56,68]. Moreover, in the present study,
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vastus medialis inhibition was observed at low pressure levels of eusion despite no change in knee joint ¯exion, suggesting that the nociceptive ¯exor withdrawal response was not stimulated. Speci®c limitations associated with this study are recognized. In this study design, an acute knee eusion was created and then aspirated. At most, 40 min would have passed before the aspiration was completed. Levick et al. (1983), reported that intra-articular pressure is a complex function of volume, joint angle, age, intra-articular ¯uid distribution, muscle action and time. Thus, it is not known whether the gait adaptations reported in the present study would have persisted after prolonged exposure to knee joint eusion. We also chose to use saline instead of other solutions that have been used in previous studies. Saline can absorb through the joint capsule whereas, other, heavier solutions cannot. Thus, intra-articular pressures may have diminished over time. However, we conducted all gait trials in under ten minutes. We statistically investigated the eect of time in a trials eect, post hoc test. There were no dierences in the eusion eects due to trials (P 0.12), indicating that the eects were consistent over the 10 trials collected for each eusion condition. Furthermore, we chose to control the amount of ¯uid injected into the knee joint rather than control for volume of ¯uid based on knee joint pressure. Our rationale in selecting this methodology was based upon the premise that physicians grade knee eusion categorically (mild, moderate and severe) during clinical exams, and document ¯uid extraction by volume and not pressure when clinical aspirations are performed. Related to this, we chose volumes of 20, 50 and 80 cm3 as they constitute a clinical representation of knee eusions encountered in the clinical setting due to acute injury, surgery or experienced by patients who are rehabilitating from a myriad of knee injuries [1,2]. 5. Summary It was hypothesized that intra-articular knee joint eusion would cause healthy individuals to walk with joint torque and power patterns similar to those previously reported for ACL injured and reconstructed individuals. With mild eusion (20 cm3 ) subjects walked with proper phasic torque, power and work relationships but exhibited a reduction in the magnitude of peak knee extensor torque, knee extensor angular impulse and vastus medialis EMG. With moderate (50 cm3 ) and severe (80 cm3 ) levels of eusion, the subjects walked in a more crouched style of gait with increased torque and power at the hip joint and decreased torque, power and work at the knee. EMG was diminished in all quadriceps muscles. All subjects showed the same directional response due to the eusion. The results of this study
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support the hypothesis that knee joint eusion may be considered a causative factor in promoting ``quadriceps avoidance like'' gait patterns. We believe these results are due to joint capsular aerent responses in conjunction with the joint capsule being distended. Because no rival adaptive mechanisms due to injury, surgery or rehabilitation could have caused the alterations observed in the gait patterns in the present study, these results may be a useful reference by which future gait studies of knee injured or rehabilitating individuals may be compared.
Acknowledgements The authors gratefully acknowledge Henry B. Ellis and Anne Morgan, B.S., for their contributions to the data reduction process. We also thank Drs. Savio L.-Y Woo, Ph.D., Chuck Dillman, Ph.D., and Paul DeVita, Ph.D., for their contributions to data interpretation and manuscript review.
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Clinical Biomechanics Award 1999
Intra-articular knee joint eusion induces quadriceps avoidance gait patterns 1 Michael R. Torry a,*, Michael J. Decker a, Randall W. Viola b, Dennis D. OÕConnor a, J. Richard Steadman b a
Steadman±Hawkins Sports Medicine Foundations, Vail, CO 81657, USA b Steadman±Hawkins Sports Medicine Clinic, Vail, CO, 81657, USA Received 1 September 1999; accepted 14 October 1999
Abstract Objectives. (1) To identify adaptations caused by intra-articular knee joint eusion during walking and (2) to determine if knee joint eusion may be a causative factor in promoting quadriceps avoidance gait patterns. Design. Gait testing of 14 healthy individuals who underwent incremental saline injections of the knee joint capsule. Background. Gait adaptations have been reported in the literature for knee injured and rehabilitating individuals. Knee joint capsular aerent activity can in¯uence knee joint function. Methods. Gait analysis was employed in a pre- and post-test, repeated measures design to determine lower extremity joint kinematics, kinetics, energetics and thigh EMG adaptations due to intra-articular knee joint eusion. Results. Knee eusion caused an increase in hip and knee ¯exion through the stance phase. Knee extensor torque, impulse and negative and positive work were diminished with increased eusion levels. Quadriceps activity decreased and hamstring activity increased due to intra-articular knee joint eusion. Discussion. These adaptations cannot be attributed to an injury, surgery or rehabilitation. Thus, the results of this experiment suggest knee joint capsular distention, via knee joint eusion, may be responsible for many gait adaptations reported for knee injured individuals in previous investigations. Conclusions. Knee joint eusion and the subsequent capsular distention can cause major alterations in the normal gait cycle and can be considered a causative factor promoting the acquisition of quadriceps avoidance gait patterns. Relevance This study provides reference data on the eects of intra-articular knee joint eusion on gait parameters by which future studies of injured or rehabilitating individuals can be compared. Ó 2000 Elsevier Science Ltd. All rights reserved. Keywords: Gait; Knee; Eusion; Torque; Power; EMG; ACL
1. Introduction Intra-articular knee joint eusion accompanies nearly all knee injuries or surgeries. Eusions develop not only after knee trauma, but because of many degenerative conditions as well [1,2]. In either case, eusion may inhibit rehabilitation, delay the return to functional activities or promote adaptations that may alter normal functional patterns. Understanding the in¯uence eu-
*
Corresponding author. E-mail address: [email protected] (M.R. Torry). 1 Presented at the XVII Congress of the International Society of Biomechanics, Calgares, Canada, 8±13 August 1999.
sion may have on lower extremity gait function may help clinicians more clearly understand a myriad of gait abnormalities. Investigators have demonstrated the existence of knee joint capsular mechanoreceptors and their in¯uence on quadriceps function by injecting ¯uids into the knee joint capsule of healthy individuals [3±5]. These studies report a reduction in the Homan re¯exes of the quadriceps musculature. Furthermore, these investigators observed that the vastus medialis sustained the most dramatic inhibitory eect compared to other quadriceps musculature. Other studies have reported substantial reductions in volitional isometric and isokinetic knee extensor torque, and in quadriceps EMG activity during knee extensor exercises [6±8]. It is the consensus of these
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investigators that the inhibitory eects observed in these studies were a result of inhibitory aerent impulses produced by joint capsular distention [3±8]. Extensor torque reduction has also been identi®ed in the gait patterns of knee injured individuals [9±11]. Speci®cally, anterior cruciate ligament (ACL) de®cient and ACL reconstructed individuals have been reported to walk with reduced knee extensor torque and power patterns and the source of their mechanical work is modi®ed [9±11]. These ®ndings are supported by observations of increased electromyographic (EMG) activity in the hamstrings and reduced EMG activity in the quadriceps [12±16]. Furthermore, quadriceps avoidance gait patterns have been shown to be related to the time since injury and thus, are considered a learned response [10,17]. Although hypotheses have been proposed, the mechanism of how individuals learn these adaptations has not been experimentally identi®ed [18,19]. Neuro-biological studies have supported an integrated role of joint capsular receptors during normal locomotion and distinct, parallel aerent spinal pathways have been identi®ed as having direct and indirect input into the three functional levels of the cerebellum [20±26]. In animal studies, increased anterior±posterior tibial displacement at the knee joint have been shown to elicit re¯ex arcs mediated by the multiple mechanoreceptors located in capsular tissue and ligament bundles [27±31]. The inhibitory eect of this aerent activity on eerent motor pathways has been well documented in various animals [32±37] and humans [38±41]. Cole et al. [28] reported that as little as 200±500 lm of tibial displacement relative to the femur in the cat knee produced marked joint aerent discharge, suggesting that clinically undetectable displacement may elicit mechanoreceptor responses. Correspondingly, Hasan et al. [42] showed that the human ACL de®cient knee experiences greater anterior±posterior tibio-femoral displacements during gait compared to healthy subjects. Thus, it is plausible that these small displacements occurring during gait can distend the joint capsule suciently to elicit aerent activity that eect and modify the locomotor program over time. The ®rst purpose of this study was to document the eects of experimentally induced eusion of the knee joint on the kinematic, kinetic, energetic and EMG pro®les of the lower extremity during walking. The results of this study provide baseline eects of eusion on knee joint function by which future gait analysis of injured or rehabilitating individuals may be compared. Furthermore, the existence of the quadriceps avoidance patterns and reduced extensor torque patterns has been observed in ACL de®cient and ACL reconstructed individuals, respectively. To date the neurological mechanism that in¯uences individuals to learn these adaptations has not been identi®ed. Thus, the second purpose was to determine if knee joint capsular dis-
tention could be a mechanism that induces quadriceps avoidance gait patterns. We propose that if the classic adaptations (increased knee ¯exion, decreased knee extensor torque, decreased knee power and work) are apparent due to injection of the knee joint capsule with saline, then knee joint capsular distention may be a causative factor promoting the acquisition of the quadriceps avoidance patterns. 2. Methods 2.1. Subjects Fourteen healthy subjects (9 male; 5 female) with no history of lower extremity pathology volunteered as the test group (mean age 29.5, SD 5.1 yr; mean mass 78.50, SD 4.0 kg; mean height 184.2, SD 4.2 cm). Prior to testing, each participant provided their written informed consent according to a protocol approved by an Institutional Review Board retained by the Vail Valley Medical Center. 2.2. Instrumentation and data processing Lower extremity performance during level ground walking were recorded using a three-dimensional motion analysis system (Motion Analysis, Santa Rosa, CA, USA). A four segment, rigid-link model of the lower limb was de®ned by 13 retro-re¯ective, spherical markers (diameter 25 mm) that delineated segment coordinate systems that were related to ®xed anatomic reference systems [43]. Five synchronized cameras captured the gait motion at a frequency of 120 Hz. The cameras were calibrated with mean residual errors in the range of 1.25±2.55 mm over a volumetric space of 1.50 ´ 1.10 ´ 1.50 m3 . The coordinate data for each marker trajectory were smoothed using a fourth-order Butterworth ®lter with a ®ve Hz cut-o frequency. The magnitude of the segmental masses and the mass center location of the lower extremity, along with their moment of inertia, were estimated using a mathematical model [44], and segmental masses reported by Dempster [45]. Force data were sampled at a frequency of 1200 Hz. Center of pressure were calculated from the sampled ground reaction forces [46]. Dynamic joint torque data were calculated by combining the anthropometric, kinematic and force data in an inverse dynamic analysis [46]. Net hip and knee sagittal plane joint moments were calculated throughout the stance phase, with a positive internal moment acting in the direction of hip and knee extension, respectively. Instantaneous mechanical power for each joint were calculated by taking the product of the joint torque and joint angular velocity and were reported as positive values representing energy generation
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and negative values representing energy absorption [46]. Calculating the area under the power curve represents work. Thus, area under the positive power curve indicates that the joint is acting concentrically to generate energy (positive work), while the area under the negative power curve indicates that the joint is acting eccentrically to absorb energy (negative work) [10,11,46]. The kinetic and energetic data were scaled by dividing each value in the time series by the product of the subjectÕs weight (BW) and height (HT), and multiplying by 100 [9,47]. Custom software utilizing a cubic spline function was used to time normalize the data based on the number of data points in the trial with the largest number of points to produce time series data expressed as 0±100% of the stance phase. Ensemble averages of time series data were averaged for the entire group (N 140 trials) for graphical purposes. To monitor muscular activity patterns, the skin of each electrode site was shaved and cleaned with alcohol. Pre-gelled, silver±silver/chloride bipolar surface electrodes (Medicotest A/S, Rugmaken, Denmark) were placed over the vastus medialis, vastus lateralis, biceps femoris, and the medial hamstrings (semitendinosus and semimembranosus) according to Basmajiian and Deluca [48] and Delagi et al. [49]. The electrodes were placed over each muscle belly in line with the direction of the ®bers and with a center to center distance of approximately 2.5 cm. Placement of electrodes was con®rmed for each muscle with manual muscle testing and visual biofeedback monitoring. A single ground electrode was placed over the anterior tibial spine. The input impedance of the EMG ampli®er was <10 MX, with a common mode of rejection ratio of 85 dB and a gain of 1000. Raw dynamic EMG and isometric, maximum voluntary contractions (MVCs) for each muscle were collected with an eight channel Noraxon Telemetry (Noraxon, Scottsdale, AZ, USA) unit on-line to the Motion Analysis A/D board, sampling at a frequency of 1200 Hz. Pre-test MVCs were collected using methods described previously by Lange et al. [50]. To ensure true MVC records, the subjects were allowed to practice the contractions for several minutes prior to testing. Visual biofeedback was used to help the subjects isolate and concentrate on the intended musculature during the practice session. MVC data were processed with a 50 ms root-mean square (RMS) moving window [51]. EMG reference values were calculated for each muscle using the average of the ®ve peak EMG signals and represented 100% MVC. The mean peak amplitude of the ®ve MVCs was used to scale the dynamic contractions recorded during each gait test. Stance phase trial data were processed with a 15 ms RMS moving window and were scaled by dividing by each subjectÕs representative MVC and multiplying by 100 [50,51]. Thus, EMG gait values are
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reported as a percentage of the MVC. The scaled data were further quanti®ed by dividing the stance phase into four equal time intervals and averaging the data at 25% increments (0±25%, 26±50%, 51±75%, 76±100%) totaling 0±100% of the normalization base. These 25% intervals were analyzed to allow direct comparisons to be made in conjunction with knee power transition periods that delineate speci®c energy absorption (K1, Fig. 6) and energy generation (K2, Fig. 6) phases within the stance phase. 2.3. Walking protocol The subjects were allowed to familiarize themselves with the walkway and testing apparatus prior to testing. Each participant practiced walking on the six meter walkway at a self-selected speed until they could provide a consistent foot strike on the force platform. During data collection, each subject completed 10 walking trials. Only trials within 2.5% of the self-selected speed, and where full foot placement was achieved on the force platform, were considered acceptable for analysis. 2.4. Knee eusion and test protocol After 10 pre-eusion gait trials were collected, a series of saline injections were administered to simulate knee joint eusion and cause joint capsular distention. A physician (RMV) administered all injections using an aseptic sterile technique. The entire knee area was shaved and cleaned with alcohol and then bathed with a sterile 10% betadine solution. The injection site was then wiped with Povidone±Iodine in a sterile fashion. Immediately following each injection, the site was cleaned with alcohol and a sterile dressing applied. This procedure was carried out before and after each injection. The subject was placed in a seated position with their test limb fully extended. The ®rst injection consisted of a 3.0 cm3 mixture of 1% Lidocaine (1.5 cm3 ) and 25% Marcaine (1.5 cm3 ) introduced into the skin and subcutaneous tissue at the lateral supra patellar position with a 25 gauge needle. Care was taken not to penetrate the joint capsule during the numbing injection. After super®cial numbing had occurred, an 18 gauge needle was used to administer an infusion of 0.9% saline [4]. The ®rst saline injection accounted for 20 cm3 of ¯uid. Each successive injection accounted for an additional 30 cm3 saline added intra-articularly. At the time of each injection, an intra-articular pressure reading (mm Hg) was recorded via a pressure transducer aligned in parallel with the syringe [4,52]. A two-way stopcock located on the end of the syringe could be turned quickly to negate saline back-¯ow and allow for immediate pressure readings after the injection. The subject was then helped to stand upright and instructed to put full weight bearing pressure on the injected knee, and a weight
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bearing joint capsular pressure reading was recorded. The needle was withdrawn, a sterile dressing was applied and the individual performed 10 gait trials. The stretch-relax cycle for the human knee joint capsule has been estimated to be approximately 10 min [33,52]. Thus, all gait tests were completed in under a 10min time frame. After the fourth injection and subsequent gait test, the saline was aspirated from the knee joint. The total amount of saline removed for each subject was recorded. A ®nal sterile dressing was applied to the injection site and the subject performed the last set of 10 gait trials. The subjects were examined by a physician at 24, 48 h, and 7 days post-testing to ascertain recovery. 2.5. Statistical analysis The kinematic analysis yielded mean hip and knee joint angles at heel contact and mean hip and knee joint angles through the stance phase (0±100%). The kinetic analysis yielded peak knee extensor joint torque, extensor hip and knee joint angular impulse over the stance phase and hip and knee joint extensor angular impulse from 0% to 50% of the stance phase. Energetic variables included total positive hip work and total positive and negative knee work through the stance phase (0±100%), positive hip work at 0±30%, and total positive and negative knee work between 0% and 25% of the stance phase. These phases correspond to speci®c power transition periods described by Winter, 1990 and have been previously reported in ACL injured individuals [10,11]. EMG variables included the EMG data calculated over the 0±25% and 26±50% intervals of stance phase. Dierences in the kinematic, kinetic, work and EMG parameters between test conditions were analyzed in a repeated measures analysis of variance design (alpha 0.05) with a Bonferroni adjusted post hoc test to identify speci®c contrasts between conditions. To determine the relationship between the amount of ¯uid in the knee and the degree that it aected torque output, a product-moment correlation between the peak knee extensor torque and the knee joint extensor angular impulse and the weight bearing intra-articular pressures were also conducted. 3. Results 3.1. Kinematics The general eect of eusion on hip and knee joint kinematics was to cause a more ¯exed position at heel contact and throughout the stance phase (Table 1). Compared to pre-eusion values, individuals increased hip ¯exion angle at heel contact 1.1% at 20 cm3
(P 0:673), and 7.6% with 80 cm3 (P < 0:001) knee joint injection. Compared to pre-eusion trials, average hip ¯exion angle through the stance phase increased 5.0% (P 0:180), 28.4% (P < 0:001), and 48.0% (P < 0:001) for eusion levels of 20, 50 and 80 cm3 , respectively (Fig. 1). Hip angle at heel contact and average hip ¯exion angle through stance returned to within 3.1% and 6.1% of pre-eusion values after aspiration of the ¯uid (P > 0.10). Knee angle at heel contact increased in ¯exion 16.2% (P 0.312), 40.1% (P < 0.001) and 63.6% (P < 0.001) for eusion levels of 20, 50 and 80 cm3 , respectively. Average knee ¯exion angle through stance increased 6% for 20 cm3 (P 0.013), and 11.3% (P < 0.001) and 25.2% (P < 0.001) for 50 and 80 cm3 conditions (Fig. 2). Knee kinematics returned to within 1.2% of the pre-eusion values after aspiration (P > 0.05). 3.2. Kinetics Hip joint torque values and ensemble hip joint torque time series data for all conditions are presented in Table 1 and Fig. 3. Hip extensor impulse in the ®rst half of stance (0±50%) increased 2.0% (P 0.60), 7.2% (P 0.052) and 20.1% (P < 0.001) for eusion levels of 20, 50 and 80 cm3 , respectively. These values returned to within 0.56% of the pre-eusion values after aspiration (P 0.86). The general eect of eusion on stance phase knee joint torque patterns was a reduction in the extensor peak torque, extensor impulse in the ®rst half (0±50%) of stance and a shift toward an extensor torque in the latter half (55±80%) of stance (Table 1 and Fig. 4). Peak knee extensor torque decreased 12.3% (P < 0.001), 12.7% (P < 0.001), and 19.5% (P < 0.001) for eusion levels of 20, 50 and 80 cm3 , and returned to within 1.7% of preeusion values after aspiration (P 0.384). Knee extensor angular impulse calculated over the ®rst half of stance decreased 12.6% (P < 0.001), 20.2% (P < 0.001), and 30.2% (P < 0.001) at eusion levels of 20, 50 and 80 cm3 , respectively. Knee joint angular impulse returned to within 5.9% of pre-eusion values after aspiration (P 0.017). Knee joint ¯exor impulse was unchanged at 20 cm3 (P 0.563), but reduced 56.0% (P < 0.001) at 50 cm3 and was eliminated in most subjects with 80 cm3 of eusion. Knee joint ¯exor impulse returned to within 4.0% of pre-eusion values after aspiration (P 0.641). Mean intra-articular weight-bearing pressure increased 42.7% between 20 and 80 cm3 eusion levels (Table 1). Correlation of the weight bearing intra-articular pressure and the peak knee extensor torque and knee extensor angular impulse occurring during the ®rst half of stance were r ÿ0:44 (P 0.003) and r ÿ0:68 (P < 0.0001), respectively; indicating that as intra-articular pressure increased, peak knee extensor torque and
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Table 1 Mean values and {SD} across test conditions for kinematic, kinetic and energetic variablesa Variable
Kinematics Hip angle at heel contact Knee angle at heel contact Average hip angle through stance Average knee angle through stance Kinetics Hip extensor impulse (0±50%) Knee extensor impluse (0±50%) Peak extensor knee torque Knee ¯exion impulse (50±100%) Work Total positive hip Total positive knee Positive hip (0±50%) Negative knee (0±25%) Positive knee (26±50%)
Weight bearing intra-articular pressure a *
Condition Pre-eusion
20 cm3
50 cm3
80 cm3
Aspiration
ÿ21.38 {3.91} ÿ3.45 {2.67} ÿ5.77 {1.41} ÿ19.52 {2.37}
ÿ21.62 {4.15} ÿ4.12 {3.39} ÿ6.08 {1.92} ÿ20.64 {2.34}
ÿ20.6 {5.05} ÿ5.76 {2.05} ÿ8.06 {2.25} ÿ22.01 {2.12}
ÿ23.16 {4.56} ÿ9.49 {1.92} ÿ11.18 {1.59} ÿ26.13 {2.54}
ÿ20.67 {3.63} ÿ3.46 {2.67} ÿ6.15 {1.64} ÿ19.28 {2.35}
0.52 {0.26} 0.89 {0.18} 5.69 {0.63} ÿ0.35 {0.15}
0.53 {0.21} 0.78 {0.23} 4.99 {0.78} ÿ0.36 {0.09}
0.56 {0.21} 0.71 {0.21} 4.97 {0.84} ÿ0.15 {0.09}
0.66 {0.28} 0.62 {0.11} 4.58 {0.97} ÿ0.01 {0.01}
0.53 {0.26} 0.83 {0.17} 5.59 {0.61} ÿ0.33 {0.10}
0.31 {0.25} 0.73 {0.25} 0.52 {0.26} ÿ0.66 {0.22} 0.36 {0.12}
0.32 {0.21} 0.68 {0.22} 0.53 {0.21} ÿ0.61 {0.20} 0.34 {0.11}
0.35 {0.22} 0.67 {0.22} 0.56 {0.21} ÿ0.59 {0.24} 0.31 {0.07}
0.49 {0.35} 0.51 {0.18} 0.66 {0.28} ÿ0.43 {0.15} 0.21 {0.07}
0.30 {0.29} 0.72 {0.23} 0.53 {0.26} ÿ0.65 {0.21} 0.36 {0.11}
0 {0.00}
32.84 {15.09}
68.50 {22.174}
102.82 {30.56}
NA
Kinematics in degrees; torque in %BW.HT; impulse in %BW.HTs; work in %BW.HT; pressure in mm Hg. Values signi®cantly dier from pre-eusion condition; P < 0.015.
knee extensor impulse decreased. Average ¯uid removed during aspiration was 62 cm3 (77.6%). 3.3. Energetics Time series hip and knee joint power patterns are presented in Figs. 5 and 6, and hip and knee work estimates are listed in Table 1. Compared to pre-effusion values, total positive work at the hip increased 2.1% (P 0.89), 8.7% (P 0.46) and 29.0% (P 0.001) for injection levels 20, 50 and 80 cm3 , respectively. Hip positive work during the ®rst half of stance, increased 38.5% (P 0.02), 48.5% (P < 0.001), and 56.6% (P < 0.001) for the successive eusion levels. Hip positive work returned to near normal values after aspiration (P 0.77). Total positive knee work decreased 5.2% (P 0.32), 9.0% (P 0.20), and 29.7% (P < 0.001) over the entire stance phase for 20, 50 and
80 cm3 eusion levels. Total positive knee work returned to within 2.0% of pre-eusion values after aspiration (P 0.773). To investigate speci®c changes in knee work during the stance phase, discrete intervals de®ned by transition periods in the knee joint power curves were also analyzed. The kneeÕs ability to absorb force was reduced as negative knee work occurring between 0% and 25% of stance (K1) decreased 8.3% (P 0.22), 11.3% (P 0.10), and 34.1% (P < 0.001) for the successive eusion levels, and returned to within 1.9% after aspiration (P 0.772). The kneeÕs ability to generate force was also reduced as positive knee power calculated between 26% and 50% (K2) decreased 6.2% (P 0.405), 14.3% (P 0.05), 42.5% (P < 0.001) for eusion levels of 20, 50 and 80 cm3 , respectively. Positive knee power in this interval returned to within 2.1% of pre-eusion levels after aspiration (P 0.751).
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Fig. 1. Stance phase hip position curves. Positive and negative values represent extended and ¯exed positions.
3.4. Electromyography In general, quadriceps activity was inhibited and hamstring activity was facilitated during the energy absorption phase (K1) of the knee during stance. Quadriceps and hamstring EMG activity responses due to eusion during the ®rst 25% of stance are depicted in Fig. 7a and b. Vastus medialis activity during K1 decreased 13.0% (P < 0.001), 20.6% (P < 0.001) and 31.4% (P < 0.001) for 20, 50 and 80 cm3 levels of eusion and remained 4.2% below pre-eusion values after aspiration (P 0.152). Vastus lateralis activity during this same time period decreased 9.2% (P 0.011), 27.7%
(P < 0.001) and 42.2% (P < 0.001) at each successive effusion level and remained 5.7% below pre-eusion levels after aspiration (P 0.13). Rectus femoris activity was less aected by eusion but still decreased 4.1% (P 0.063), 3.4% (P 0.125) and 17.2% (P < 0.001) with 20, 50 and 80 cm3 and returned to within 1.0% of preeusion values (P 0.882). Medial hamstring activity increased 4.1% (P 0.16), 10.5% (P < 0.001) and 22.5% (P < 0.001) for successive eusion levels. Medial hamstring activity returned to within 5.0% of pre-eusion levels after aspiration (P 0.883). Biceps femoris activity increased 0.6% (P 0.83) at 20 cm3 , 6.9% (P 0.02) at 50 cm3 and 13.7% (P < 0.001) at 80 cm3 of eusion,
Fig. 2. Stance phase knee position curves. Negative values represent a ¯exed knee.
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Fig. 3. Stance phase hip torque (internal moment). Positive and negative values represent net extensor and ¯exor torques.
respectively. Biceps femoris activity returned to within 2.3% of pre-eusion values after aspiration (P 0.465). Similar to the EMG results during the K1 interval, quadriceps activity decreased while hamstring activity increased during the major energy generation phase (K2) of the knee during stance. The quadriceps and hamstring EMG values for this phase are depicted in Fig. 7c and d. Vastus medialis activity decreased 8.8%, 16.4%, and 25.0% (all P < 0.001) for eusion levels of 20, 50 and 80 cm3 , respectively and returned to 3.4% of preeusion values after aspiration (P 0.140). Vastus lateralis EMG decreased 3.5% (P 0.29), 21.3% (P < 0.001), and 41.2% (P < 0.001) for the successive ef-
fusion levels and returned to within 4.0% after aspiration (P 224). Rectus femoris activity decreased 3.8% (P 0.43), 28.7% (P < 0.001) and 50.4% (P < 0.001) with increased eusion in the knee and returned to within 6.6% (P 0.882) of pre-eusion values after aspiration. Medial hamstring activity increased 2.5% (p 0.20), 6.6% (P < 0.001) and 14.9% (P < 0.001) for the successive eusion levels and returned to within 2.7% (P 0.172) of pre-eusion values. Biceps femoris activity increased 0.4% (P 0.87), 8.5% (P < 0.001), and 16.6% (P < 0.001) for eusion levels of 20, 50 and 80 cm3 , and returned to within 4.3% of pre-eusion values after aspiration (P 0.068).
Fig. 4. Stance phase knee torque (internal moment). Positive and negative values represent net extensor and ¯exor torques.
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Fig. 5. Stance phase hip power curves. Positive and negative values indicate energy generation and absorption.
4. Discussion The general eect of eusion on walking patterns was a more crouched style of gait, a decrease in torque, power and work produced at the knee joint and increased extensor torque, power and work produced at the hip joint. As the knee extensor function diminished in early stance, the subjects adapted by increasing hip extensor torque and positive work to help maintain total support for the limb and to provide forward progression to the walking motion. This compensatory pattern has been observed in knee injured individuals [10,11].
The reduction in energy absorption and generation at the knee are supported by the EMG parameters investigated in this study. EMG of all quadriceps muscular activity was reduced with intra-articular knee joint effusion. The vastus medialis was signi®cantly inhibited at 20 cm3 while larger eusion volumes were needed to produce the same results in the vastus lateralis and rectus femoris. The rectus femoris was least aected and we attribute this result to its bi-articulate nature and its in¯uence on the hip joint. Nonetheless, the rectus femoris was inhibited 17% at 80 cm3 ; indicating other hip ¯exors, such as the iliopsoas, may adapt to create a
Fig. 6. Stance phase knee power curves. Positive and negative values indicate energy generation and absorption.
Fig. 7. Electromyographic activity reported as a percent of MVC for all muscles and all conditions. Graph (a) Quadriceps activity during 0±25% (K1) period of stance; (b) Hamstring activity during 0±25% (K1) period of stance; (c) Quadriceps activity during 26±50% (K2) period of stance; (d) Hamstring activity during 26±50% (K2) period of stance. Solid icons represent values that are signi®cantly dierent then pre-eusion values (P < 0.015).
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majority of the compensatory (positive) work output for the hip joint. The secondary purpose of this investigation was to determine if knee joint capsular distention, via intraarticular knee joint eusion, could cause healthy individuals to walk with knee joint position, torque and power patterns similar to those that have been reported for ACL injured and rehabilitating individuals. Anterior cruciate ligament injuries have been shown to cause neuromuscular adaptations aecting the entire lower extremity [9±11]. It has been suggested that these adaptations may be mediated by: (1) brace wear [53], (2) training eects produced by rehabilitation [18,54], or (3) altered neuromuscular strategies due to the initial injury [18,19]. The results of the present study are not constrained by these factors as only healthy individuals were tested. Thus, rival adaptive mechanisms (i.e. injury, surgery or rehabilitation) could not have caused these patterns. The hip and knee kinematic and kinetic patterns observed in the present study are characteristic of the gait patterns reported for ACL de®cient and ACL reconstructed individuals [9±11,17]. DeVita et al. [10] investigated the time course of development of the quadriceps avoidance gait pattern by testing ACL injured individuals two weeks after injury but before surgery, and at three weeks post-reconstruction surgery. Results of that study indicated that at two weeks postinjury, ACL injured individuals maintained an extensor torque pattern at the knee. The knee joint torque and power patterns reported by DeVita et al. [10] are very similar to the joint torque and power patterns observed for the 50 and 80 cm3 conditions in the present study. DeVita et al. [10] also analyzed the gait patterns of ACL reconstructed patients at ®ve weeks post-reconstruction. At this time period, the authors noted that the extensor torque was still suppressed but showed trends of returning toward a normal bi-phasic, extensor±¯exor pattern. Again, these patterns bear close resemblance to the patterns observed with mild eusion (20 cm3 ) of the knee joint in the present study. Although eusion was not reported, it is reasonable to assume that the subjects utilized by DeVita et al. [10] experienced residual knee joint eusion after their surgery that may have contributed to those ®ndings. Birac et al. [17] reported that the development of the quadriceps avoidance pattern in ACL de®cient patients was related to the time since injury. Hurwitz et al. [18] and Hogervorst and Brand [19] proposed that the learning of the quadriceps avoidance pattern was most likely due to repetitive experiences that alter the locomotor system. However, to date, the aerent input responsible for this neuro-modulation has not been identi®ed. The present study supports the premise that joint capsular distention and mechanoreceptor aerent responses are the primary structures that provide this
information to the central nervous system. We propose that in ACL de®cient and reconstructed individuals, joint capsular distention, caused by excessive displacement of the tibia relative to the femur, stimulates capsular aerent activity in response to capsular stretching. The aerent information is passed to the spinal cord via the dorsal root ganglion. The dorsal and ventral spinocerebellar tracts convey the peripheral aerent information from the trunk and legs to the cerebellar cortex where this information is fractionated and relayed to the higher and lower motor cortices [55±57]. We base this mechanism on the following observations: (1) the results of the present study and previous investigations outlining distinct EMG and mechanical de®cits due to joint capsular distention and subsequent aerent responses [31±41], (2) previous research supporting excessive translation of the tibia relative to the femur during the gait cycle in ACL de®cient patients [42] and (3) evidence that a minimal amount of joint capsular distention has been shown to stimulate aerent responses [29,30]. Ultimately, the basis of this mechanism depends on the degree of tibio-femoral knee joint displacement and, as mentioned above, applies well to ACL de®cient persons. It is plausible that this mechanism may also apply to ACL reconstructed individuals as well. Successfully ACL reconstructed individuals are assumed to be structurally and mechanically sound after surgery. Nevertheless, there is considerable empirical evidence (KT-1000 scores [58,59]) and subjective clinical criteria [59,60] to argue that even in a surgically well reconstructed knee, there would exist some tibio-femoral displacement that was not inherent to that knee prior to injury or surgery. This ``clinically insigni®cant'' laxity may also distend the knee joint during impact activities, causing sucient tibio-femoral displacement and joint capsular distention. However, scienti®c evidence of tibio-femoral displacement during walking or other dynamic activities, to our knowledge, has not been reported in ACL reconstructed individuals. It is well documented that ACL injured and ACL reconstructed individuals tend to have residual quadriceps weakness (particularly vastus medialis) long after their injury or surgery. This weakness has been shown to aect the lower extremity gait in these individuals [54]. Hurley et al. (1992), utilizing a superimposed twitch technique, reported a signi®cant quadriceps strength de®cit in ACL injured individuals prior to participating in a rehabilitation program. Subsequent analysis after completion of an intensive rehabilitation program also demonstrated a residual quadriceps strength de®cit despite the absence of pain or eusion during testing [61]. The authors concluded that excessive joint motion together with aerent responses may limit the central nervous system drive to the quadriceps. In agreement with previous studies [4,5], the present study observed that the vastus medialis was most inhibited by knee joint
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eusion. Vastus medialis insuciency due to aerent inhibition would contribute to aberrant patellar tracking and possibly retro-patellar pain. This study supports the notion that residual or re-current bouts of knee joint eusion after knee injury may account for some of this residual weakness that may lead to extensor mechanism dysfunction. Several researchers have reported that biceps femoris activity is increased in ACL de®cient and ACL reconstructed patients [13,14,16]. These authors suggest that this is a protective mechanism that prevents anterior tibial translation and limits internal rotation thus protecting the knee from a pivoting motion. All hamstring EMG activity increased in the present study despite no inherent joint structural injury or laxity. This suggests that the increased hamstring activity observed by previous investigators [13,14,16] may be a result of ¯exor± extensor muscle synergy brought about by aerent neuro-modulation in order to reduce knee stress. The hamstring muscles have been demonstrated to assume a joint stabilizing role in the ACL de®cient individual [14,62]. However, the hamstrings are ineective at reducing anterior displacement at knee angles between 0° and 15° of ¯exion [63]. With eusion, knee ¯exion angle through stance was increased and subjects walked in a more ¯exed position. This position range allows greater hamstring synergy for knee joint stability [62]. Furthermore, the inhibition of the quadriceps and facilitation of the hamstring musculature in the present study would act to stabilize the knee joint by balancing the knee agonists and antagonists during the gait cycle. Solomonow et al. [62] suggested that these knee stabilizing factors are a function of an ACL-hamstring re¯ex arc. This study supports the existence of a joint capsular aerent±eerent pathway strong enough to induce immediate quadriceps and hamstring EMG alterations acting to stabilize the knee joint. Alternatively, the EMG observations in the present study may simply be a result of muscle force±length relationships due to positional changes. Several authors have reported quadriceps muscular inhibition to be a factor of hip and knee joint angle [64,65]. Although no subject complained of pain, seven subjects did comment on the ``tightness'' or ``pressure'' sensations in the knee with 80 cm3 of eusion. At the higher volume levels, pressure may have stimulated the nociceptive system surrounding the knee joint. Thus, the subjects may have changed their walking pattern in an attempt to reduce this pressure by selectively altering knee ¯exion angle to around 30°; an angle shown to reduce intra-articular knee pressure [52]. Correspondingly, this study does not discount possible in¯uences of the nociceptive system on stimulating the ¯exor withdrawal response [66,67]. However, compelling experimental evidence of painfree, ¯exor facilitation exists in the literature [41,56,68]. Moreover, in the present study,
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vastus medialis inhibition was observed at low pressure levels of eusion despite no change in knee joint ¯exion, suggesting that the nociceptive ¯exor withdrawal response was not stimulated. Speci®c limitations associated with this study are recognized. In this study design, an acute knee eusion was created and then aspirated. At most, 40 min would have passed before the aspiration was completed. Levick et al. (1983), reported that intra-articular pressure is a complex function of volume, joint angle, age, intra-articular ¯uid distribution, muscle action and time. Thus, it is not known whether the gait adaptations reported in the present study would have persisted after prolonged exposure to knee joint eusion. We also chose to use saline instead of other solutions that have been used in previous studies. Saline can absorb through the joint capsule whereas, other, heavier solutions cannot. Thus, intra-articular pressures may have diminished over time. However, we conducted all gait trials in under ten minutes. We statistically investigated the eect of time in a trials eect, post hoc test. There were no dierences in the eusion eects due to trials (P 0.12), indicating that the eects were consistent over the 10 trials collected for each eusion condition. Furthermore, we chose to control the amount of ¯uid injected into the knee joint rather than control for volume of ¯uid based on knee joint pressure. Our rationale in selecting this methodology was based upon the premise that physicians grade knee eusion categorically (mild, moderate and severe) during clinical exams, and document ¯uid extraction by volume and not pressure when clinical aspirations are performed. Related to this, we chose volumes of 20, 50 and 80 cm3 as they constitute a clinical representation of knee eusions encountered in the clinical setting due to acute injury, surgery or experienced by patients who are rehabilitating from a myriad of knee injuries [1,2]. 5. Summary It was hypothesized that intra-articular knee joint eusion would cause healthy individuals to walk with joint torque and power patterns similar to those previously reported for ACL injured and reconstructed individuals. With mild eusion (20 cm3 ) subjects walked with proper phasic torque, power and work relationships but exhibited a reduction in the magnitude of peak knee extensor torque, knee extensor angular impulse and vastus medialis EMG. With moderate (50 cm3 ) and severe (80 cm3 ) levels of eusion, the subjects walked in a more crouched style of gait with increased torque and power at the hip joint and decreased torque, power and work at the knee. EMG was diminished in all quadriceps muscles. All subjects showed the same directional response due to the eusion. The results of this study
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support the hypothesis that knee joint eusion may be considered a causative factor in promoting ``quadriceps avoidance like'' gait patterns. We believe these results are due to joint capsular aerent responses in conjunction with the joint capsule being distended. Because no rival adaptive mechanisms due to injury, surgery or rehabilitation could have caused the alterations observed in the gait patterns in the present study, these results may be a useful reference by which future gait studies of knee injured or rehabilitating individuals may be compared.
Acknowledgements The authors gratefully acknowledge Henry B. Ellis and Anne Morgan, B.S., for their contributions to the data reduction process. We also thank Drs. Savio L.-Y Woo, Ph.D., Chuck Dillman, Ph.D., and Paul DeVita, Ph.D., for their contributions to data interpretation and manuscript review.
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