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Neuromuscular Function during a Forward Lunge in Meniscectomized Patients

THORLUND, JONAS BLOCH; DAMGAARD, JACOB; ROOS, EWA M.; AAGAARD, PER

Medicine & Science in Sports & Exercise: July 2012 - Volume 44 - Issue 7 - p 1358–1365
doi: 10.1249/MSS.0b013e31824c315b
APPLIED SCIENCES
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Objective This study aimed to investigate differences in knee joint kinematics, ground reaction force kinetics and neuromuscular activity including muscle coactivation, and medial versus lateral muscle activity during a forward lunge between the operated and contralateral legs of meniscectomized patients. Such differences may represent early changes in neuromuscular function potentially contributing to the development of knee osteoarthritis.

Methods Twenty-two unilaterally meniscectomized patients (15 men and 7 women; age = 45.4 ± 5.1 yr, height = 174.3 ± 7.1 cm, weight = 77.3 ± 15.4 kg (mean ± SD)) were investigated on their operated and contralateral legs during a forward lunge using synchronous goniometer, force plate, and EMG recording (vastus lateralis, vastus medialis, biceps femoris, and semitendinosus).

Results During impact loading, an increased level of muscle coactivation (38.0% (29.8%–46.3%) vs 30.1% (23.6%–36.6%), P = 0.02; mean (95% confidence interval)), reduced range of motion (59.4° (54.5°–64.2°) vs 64.9 (60.8°–70.0°), P = 0.01), and increased loading rate (985% BW·s−1 (653–1317% BW·s−1) vs 696% BW·s−1 (525–868% BW·s−1), P = 0.01) were observed in the operated leg compared with the contralateral leg. In addition, different patterns of medial versus lateral neuromuscular activity were observed in the operated and contralateral legs, along with minor differences during the other phases of the forward lunge.

Conclusions The findings of increased muscle coactivation, reduced range of motion, and increased loading rate in the operated compared with the contralateral leg support the hypothesis that meniscectomized patients demonstrate modulations in kinetics, kinematics, and neuromuscular activity, which may represent early changes in neuromuscular function that precede and affect development of knee osteoarthritis. The results also indicate that the forward lunge test is a sensitive measure to identify leg-to-leg differences in neuromuscular function after surgical interventions.

Institute of Sports Science and Clinical Biomechanics, University of Southern Denmark, Odense, DENMARK

Address for correspondence: Jonas Bloch Thorlund, Ph.D., Institute ofSports Science and Clinical Biomechanics, University of Southern Denmark, Campusvej 55, 5230 Odense M, Denmark; E-mail: jthorlund@health.sdu.dk.

Submitted for publication September 2011.

Accepted for publication January 2012.

Knee osteoarthritis (OA) is considered a mechanically driven disease. The external knee adduction moment (KAM) (29), a surrogate measure of medial compartment knee joint loading, has been reported to be higher in patients with medial tibiofemoral knee OA (5). Furthermore, the KAM has been associated with progression (25) and severity (31) of the disease. Thus, altered and/or increased knee joint loading during normal ambulation have been suggested to play a role in the initiation of knee OA (4). Increased knee joint loading and altered kinematics during level walking and stair ascent/descent may be caused by altered neuromuscular function. Indeed, patients with knee OA have been reported to have impaired lower extremity muscle strength (19,22,24,32) and display alterations in neuromuscular activity. Changes in neuromuscular activity include elevated levels of muscle coactivation (7,15,16,21,30), which is thought to increase knee joint stability albeit also causing reduced range of motion (ROM). In addition, altered patterns of medial versus lateral muscle activity have also been reported in patients with knee OA (13,17,18), which may represent a compensatory strategy to reduce medial compartment loading. However, only limited knowledge exists on the possible neuromuscular deficits before onset of knee OA.

Meniscectomized patients are a group of patients with a high risk of knee OA (10,12) and is therefore a useful model to study knee OA development including changes in neuromuscular activity and knee joint biomechanics possibly contributing to knee OA. Recently, we found no deficits in muscle strength in middle-age (35–55 yr) patients meniscectomized for symptomatic medial degenerative tears compared with healthy controls 2 yr after meniscectomy, despite patients’ self-reporting substantial pain and reduced physical function (36). Furthermore, neuromuscular activity, kinetics, and kinematics did not differ between patients and controls during stair descent (38). The relatively better muscle function and younger age in the meniscectomized patient group compared with patients with established OA may suggest that more demanding motor tasks are needed to detect early changes in knee joint kinetics/kinematics and/or neuromuscular activity in meniscectomized patients at high risk of knee OA.

The forward lunge represents a movement that is largely dependent on the quadriceps muscle (3) and requires more forceful and prolonged quadriceps contractions than horizontal gait owing to the high magnitude of impact loading and the prolonged stance phase, respectively. Furthermore, the forward lunge also requires high knee joint stability, for which the hamstrings muscles are known to play an important role (27). The forward lunge has been shown to be able to discriminate between anterior cruciate ligament–deficient subjects categorized as copers and noncopers (3) and subjects with and without experimentally induced knee pain (14). As such, the forward lunge may be a useful test to detect early subtle differences in neuromuscular activity and knee joint kinetics/kinematics, which may play a role in the initiation of knee OA.

The aim of this study was to investigate knee joint kinematics, ground reaction force (GRF) kinetics, and neuromuscular activity including muscle coactivation and the distribution of medial versus lateral muscle activity during a standardized forward lunge movement in meniscectomized patients at high risk of knee OA. We hypothesized that altered patterns of neuromuscular activity including increased muscle coactivation and reduced medial versus lateral activity would be observed in the operated compared with the contralateral leg, which would be accompanied by a decreased ROM in the knee joint and altered GRF. Such differences in neuromuscular activity and knee ROM have previously been observed in patients with knee OA (7,13,15,17).

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METHODS

The present study investigated 22 patients meniscectomized unilaterally for a medial meniscal tear in the posterior half of the meniscus (15 men and 7 women, age = 45.4 ± 5.1 yr, height = 174.3 ± 7.1 cm, weight = 77.3 ± 15.4 kg, body mass index = 25.4 ± kg·m−2 (mean ± SD)). These patients have been previously investigated during a stair decent test, as reported in detail elsewhere (38). In brief, patients 35–55 yr old at the time of surgery, who have undergone surgery for a medial meniscal tear in the posterior half of the meniscus in the years 2006 and 2007, were identified through the surgical code system from two different hospitals (mean ± time since surgery = 20.7 ± 6.6 months). The age criteria were set to include most patients with degenerative meniscal tears but without knee OA. Patients with previous knee ligament injury or severe cartilage changes defined as deep clefts or visible bone at the time of meniscectomy, or self-reported comorbidities limiting participation in the study (determined by the Self-administered Comorbidity Questionnaire [28]) were excluded from the study. After meniscectomy, patients were given a leaflet with standard rehabilitation exercises, which they were encouraged to perform at home. Information on compliance with the exercise recommendation was not collected. Specific details of the recruitment flow have been reported previously (36).

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Testing Procedure

Knee joint kinematics, GRF kinetics, and neuromuscular activity were assessed during a forward lunge. Please refer to Figure 1 for an example of the EMG, goniometer, and GRF measurements during the forward lunge. The subjects were instructed to start in an upright position, facing the force plate with the feet shoulder width apart, at a distance to the force plate equal to the length of the subjects leg (i.e., defined from the midpoint of the greater trochanter to the midpoint of the lateral malleolus). The subject was then asked to perform a single long step onto the force plate with the leading leg while keeping the upper body perpendicular to the ground and both with hands on the hips. The foot of the leading leg was to hit the middle of the force plate, and the knee should be flexed to a 90° angle, before immediately pushing backward to the starting position without moving the foot of the posterior stance leg. Subject instructions were standardized using a manuscript, and representative pictures of the movement were shown to the subject. Practice trials (about two to four trials) were conducted until the subjects felt confident with the movement, and sufficient rest was allowed between trials to avoid fatigue. The subjects wore shorts and their own shoes during the experiment. Three forward lunges were performed for each leg, and these were analyzed separately. A mean of the three trials was calculated for the different variables of interest as recommended by Alkjaer et al. (2). The starting leg (i.e., operated/contralateral) was randomized for each subject. All subjects provided written informed consent, and the study was approved by the Ethics Committee of the Region of Southern Denmark (ID: S-20080044).

FIGURE 1

FIGURE 1

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Knee Angle Recordings

A flexible electrogoniometer (Biometrics SG150; Biometrics Ltd., Gwent, UK) was placed laterally across both knees of the subjects to measure instantaneous knee joint angle during movement. Goniometer data were recorded synchronously with the EMG and force plate signals. During later offline analysis, the instant of foot strike and toe-off, respectively, were determined from the vertical GRF curve and were used as temporal reference points. Further, the following variables were obtained: knee angle at foot strike (Anglefoot strike), knee angle at toe-off (Angletoe-off), knee angle at peak knee flexion (Anglepeak flex), knee ROM from foot strike to peak knee flexion (ROMpeak flex), knee ROM during the loading phase (ROMload), and knee ROM during the unloading phase (ROMunload). The goniometer was calibrated with the knee flexed at a 90° angle (0° = full extension).

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Force Plate Analysis

GRF data were collected using a force plate (Kistler 9281 B; Winterthur, Switzerland), which was integrated into the floor. The vertical GRF signal (Fz) was recorded at 1000 Hz using a 12-bit A/D converter (DT 3010; Data Translation, Marlboro, MA).

During subsequent analysis of the GRF signal, the following variables were calculated and expressed as a percentage of body weight (%BW): the loading slope (GRFload) defined as the rate of GRF rise in the initial weight acceptance phase from foot strike to 80% of peak GRF (GRFpeak), the unloading slope (GRFunload) defined as the GRF slope from 80% GRF to toe-off, and the mean GRF (GRFmean) defined as the average GRF during the entire stance phase. During the forward lunge, the temporal occurrence of the peak GRF may vary substantially between trials. Thus, in accordance with previous reports (20,33,38), we chose to use 80% of GRF as a reference point rather than peak GRF to minimize the effect of this on the calculations of the loading and unloading slope. Furthermore, the duration of the loading phase (Tload: time from foot strike to 80% GRFpeak), unloading phase (Tunload: time from 80% of GRFpeak to toe-off), and the entire stance phase (Tstance: time from foot strike to toe-off) were determined. A representative curve of the GRF signal and the determined variables are shown in Figure 2.

FIGURE 2

FIGURE 2

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EMG

Testing.

Bipolar surface EMG signals were obtained from selected knee extensor and flexor muscles (vastus lateralis (VL), vastus medialis (VM), biceps femoris (BF), and semitendinosus (ST)) during the forward lunge and were subsequently normalized to the maximal EMG signal amplitude recorded during a standardized maximal voluntary contraction (MVC) maneuver. Quadriceps and hamstring MVC were performed in a sitting position as maximal isometric knee extensor or flexor contractions, respectively. The hip was flexed at 90°, and the knee angle was in 60° extension. Strong verbal encouragement was given during every contraction to promote maximal voluntary effort. EMG signals were obtained according to procedures reported elsewhere (20,37) and in agreement with SENIAM recommendations (www.SENIAM.org) using bipolar Ag/AgCl surface electrodes (Blue Sensor M, M-00-S/50; Ambu, Ballerup, Denmark) with a 20-mm interelectrode distance. Before placing the electrodes, the skin was shaved and cleaned with alcohol to reduce electrode–skin impedance.

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Sampling.

EMG electrodes were directly connected to small custom-built preamplifiers taped to the skin. The EMG signals were transmitted through shielded wires to a custom-built differential instrumentation amplifier with a frequency response of 10–10,000 Hz and a common mode rejection ratio >100 dB. An amplifier gain of 400 (=52 dB) was used and included analog high-pass (10 Hz) and low-pass filtering (550 Hz), respectively. Signal-to-noise ratio exceeded 55 dB. All EMG signals were sampled synchronously (1000 Hz) with the goniometer and force plate signals. During subsequent analysis, EMG signals were digitally high-pass-filtered at a 5-Hz cutoff frequency, followed by full-wave rectification and low-pass filtering at a 10-Hz cutoff frequency (1). All filtering routines used fourth-order zero-lag Butterworth filters. All EMG signals in the forward lunge analysis were normalized to their peak EMG amplitude during MVC. Neuromuscular activity was calculated as the mean normalized EMG amplitude during the loading slope phase, the unloading slope phase, and as the average during the entire stance phase.

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Analysis.

As previously described (20), agonist–antagonist muscle coactivation was quantified as the magnitude of normalized signal overlapping for two given EMG signals (intersection of EMGa (agonist) and EMGb (antagonist)), relative to the union of the two EMG signals in a given time interval (i.e., percentage overlap between agonist and antagonist muscle EMG signals).

Muscle coactivation was calculated for the knee extensors versus flexors during the loading phase, the unloading phase, and the entire stance phase, respectively. In addition, the relative distribution of medial ((VM + ST) / 2) versus lateral ((VL + BF) / 2) muscle activity was calculated for, the operated and contralateral legs, respectively, during the initial weight acceptance phase (loading phase), during the unloading phase, and during the entire stance phase (38). Before all coactivation analyses, all EMG signals were normalized relative to the maximal EMG amplitude recorded during an MVC maneuver (see details above).

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Statistical Analysis

Student’s paired t-test was used to evaluate differences in kinematics, kinetics, and EMG variables between the operated and contralateral legs. Furthermore, Student’s paired t-test was used to evaluate medial versus lateral muscle activity within the operated and contralateral legs, respectively. Stata 11.0 (StataCorp, College Station, TX) was used for all statistical analyses, with a prespecified level of significance = 0.05. Corrections for multiple comparisons were not performed because of the exploratory nature of the study.

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RESULTS

The patients performed the forward lunge close to the intended 90° peak knee flexion angle for both the operated and the contralateral legs (Table 1). Kinetic, kinematic, and neuromuscular differences were observed between the operated and contralateral legs, particularly, but not solely confined to, the loading phase of the forward lunge. These differences were manifested as a 30% (P = 0.01) shorter loading phase (Tload), a 42% (P = 0.01), higher loading rate (Loadslope), and a tendency (P = 0.07) for a reduced rate of unloading (Unloadslope) in the operated compared with the contralateral leg. Consistent with the shorter loading phase, we also observed a 22% (P = 0.01) reduced knee ROM during the loading phase (ROMload) along with an 8% (P = 0.01) reduction in ROM from foot strike to peak knee flexion (ROMpeak flex) in the operated compared with the contralateral leg (Table 1).

TABLE 1

TABLE 1

Hamstring muscle activity was 39% higher in the operated leg for BF during the loading phase (15.3 ± 2.4% MVC vs 11.0 ± 1.7% MVC (mean ± SE), P = 0.03) and 46% higher during the unloading phase (8.3 ± 1.7% MVC vs 5.7 ± 0.9%MVC, P = 0.03) compared with the contralateral leg. In addition, ST activity was higher in the operated leg during the unloading phase (7.1 ± 2.0% MVC vs 3.8 ± 0.6% MVC, P = 0.04) compared with the contralateral leg. Moreover, a tendency for elevated muscle activity was observed during the entire stance phase for BF (P = 0.07) and during the loading phase for ST (P = 0.06) in the operated compared with the contralateral leg (Fig. 3). No differences were observed in quadriceps (VL and VM) neuromuscular activity between legs.

FIGURE 3

FIGURE 3

During the loading phase, elevated levels (26%) of quadriceps–hamstrings muscle coactivation were observed for the entire thigh (i.e., VL + VM vs BF + ST) in the operated compared with the contralateral leg (38.0 ± 4.0% MVC vs 30.1 ± 3.1% MVC, P = 0.02). In contrast, muscle coactivation did not differ between the operated and contralateral legs during the unloading phase or in the entire stance phase (Fig. 4).

FIGURE 4

FIGURE 4

Overall medial (VM + ST) muscle activity was 15% higher than lateral (VL + BF) muscle activity in the contralateral leg during the loading phase (26.1 ± 2.3% MVC vs 22.6 ± 2.0% MVC, P = 0.048) as well as 15% higher during the entire stance phase (41.1 ± 4.0% MVC vs 35.6 ± 2.5% MVC, P = 0.03; Fig. 5). Such a pattern was not observed in the operated leg, where overall medial and lateral muscle activities did not differ.

FIGURE 5

FIGURE 5

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DISCUSSION

In the present study, we observed kinetic, kinematic, and neuromuscular activity differences during the loading phase of a standardized forward lunge movement between the operated and contralateral legs of meniscectomized patients at high risk of knee OA. Specifically, increased levels of muscle coactivation, reduced ROM, and increased rate of loading were observed in the operated leg compared with the contralateral leg, along with different patterns of medial versus lateral muscle activity in meniscectomized legs during a forward lunge.

Patients with knee OA have been reported to show impaired neuromuscular function expressed as reduced lower extremity muscle strength (19,22,24,32) and altered patterns of neuromuscular activity, including higher levels of muscle coactivation (7,15,16,21,30) and altered medial versus lateral muscle activity (13,17,18), which are thought to affect knee joint loading and kinematics. Nevertheless, little is known about the initial changes in neuromuscular activity and knee joint biomechanics that may precede knee OA. Some studies have been conducted on neuromuscular activity and gait and stair/ascent biomechanics in the patients (6,8,23,26,34,35). However, these studies either involved younger patients with traumatic meniscal tears (6,8,23,26) or early postmeniscectomy patients (8,26,34,35), representing early postsurgical recovery. In the latter case, deficiencies may not be due to the meniscal tear per se but may be caused by the surgical procedure itself. Thus, in the present study, we examined a homogenous group of middle-age patients 21 months after meniscectomy representing a “pre-OA” state (9,11).

Recently, we observed reduced medial versus lateral neuromuscular activity during stair descent in the operated leg of the present group of patients (38). However, GRF, ROM, and muscle coactivation did not differ between patients and controls or between the operated and contralateral legs of meniscectomized patients (38). Thus, in the present study, we examined knee joint kinematics, GRF kinetics, and neuromuscular activity during a more demanding task (i.e., a standardized forward lunge). This movement requires high neuromuscular activity of prolonged duration in the quadriceps muscle together with high transversal knee joint stability, in which the hamstrings muscles also play an important role (27). Thus, we expected this test to be sensitive for detecting differences between meniscectomized and unaffected legs, respectively. Indeed, differences in impact loading were observed between the operated and contralateral legs. The observations of elevated muscle coactivation (i.e., increased overlap of normalized quadriceps and hamstrings EMG activity) and reduced ROM in the meniscectomized legs during the loading phase led to a reduced loading phase (shorter Tload), which was accompanied by an increased loading rate (higher Loadslope). Increased muscle coactivation and reduced ROM have previously been observed in patients with knee OA and has been suggested to cause a “stiffening” of the knee joint, which not only reduces the exposure time but also reduces the control of impact load absorption (7). Furthermore, a tendency toward a lower rate of unloading (i.e., reduced Unloadslope) was observed in the operated leg compared with the contralateral leg. These findings underline that the dynamic loading and unloading phases of the forward lunge are most sensitive for detecting differences between the operated and contralateral legs of meniscectomized patients.

Knee extensor neuromuscular activity was similar between the operated and contralateral legs, whereas hamstring muscle activity generally was higher in the operated leg. These findings suggest that the increased levels of muscle coactivation observed in the operated limb was mainly caused by elevated hamstring activity, which may reflect an increased need for transversal knee joint stability. Moreover, different patterns of medial (VM + ST) versus lateral (VL + BF) neuromuscular activity were observed in the operated and contralateral legs. No differences in medial versus lateral muscle activity were observed in the operated leg. In contrast, higher levels of medial versus lateral muscle activity were observed during the loading phase and entire stance phase in the contralateral leg, suggesting that high medial muscle activity is important during a forward lunge. Previous studies in knee OA patients have reported low levels of medial versus lateral muscle activity (13,17), which have been suggested to represent a strategy to reduce the KAM (i.e., reducing medial knee joint compartment loading) (13). Thus, the presently observed lack in elevated medial versus lateral muscle activity in the operated leg during the forward lunge along with previous reports of reduced medial versus lateral muscle activity in the operated leg during stair descent (38) may reflect a strategy to decrease compression forces in the medial knee joint compartment via lowered medial muscle activity. However, the specific association between the different patterns of neuromuscular activity on the external KAM (i.e., a surrogate measure of medial knee compartment loading [29,39]) could not be investigated with the methods applied in the present study.

The present findings confirmed the hypothesis that the forward lunge represents a more challenging and sensitive motor task than stair descent in identifying leg-to-leg differences in neuromuscular function and impact loading between operated and contralateral legs in middle-age meniscectomized patients 21 months after surgery. Furthermore, together with our previous results obtained during stair descent (38), the present data support the notion that impairments in neuromuscular function in meniscectomized patients at high risk of knee OA initially are manifested by asymmetries between the operated and contralateral legs, which may potentially become augmented at more progressed stages of knee OA development.

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Limitations.

Owing to the cross-sectional study design, the potential implications of the present findings for future knee OA development remain speculative. Furthermore, detailed GRF analysis was used as a surrogate measure of knee joint loading; however, this measure may not reflect actual bone-on-bone knee joint contact forces. Another limitation in the present study is the lack of information about postsurgery rehabilitation, which may affect neuromuscular function. However, given that patients were assessed 21 months after surgery and all patients received the same instructions regarding postsurgery rehabilitation (i.e., a home exercise program), the importance of this is probably limited.

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CONCLUSIONS

The present findings support the hypothesis that meniscectomized patients show early modulations in knee joint kinematics, GRF kinetics, and neuromuscular activity, which may precede and potentially affect long-term knee OA development. These modulations were manifested as increased muscle coactivation, reduced ROM, and increased rate of GRF loading during a forward lunge in the operated leg compared with the healthy contralateral leg of meniscectomized patients at high risk of knee OA. Furthermore, different patterns of medial versus lateral neuromuscular activity were observed in the operated and contralateral legs. The present data support that the forward lunge test provides a sensitive motor task for identifying leg-to-leg differences in neuromuscular function in middle-age meniscectomized patients. The implications of the present findings on medial knee joint compartment loading (i.e., KAM) and medial compartment knee OA development warrant further investigation.

This study was supported by funding from The Danish Rheumatism Association and the Region of Southern Denmark. The sponsors had no role in any part of the study.

None of the authors have any conflict of interest to declare.

The results of the present study do not constitute any endorsement by the American College of Sports Medicine.

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Keywords:

KNEE JOINT; OSTEOARTHRITIS; MENISCECTOMY; BIOMECHANICS; EMG

©2012The American College of Sports Medicine