Patients with knee osteoarthritis (OA) self-report pain and functional limitations (20,34). The reductions in physical function have been associated with reduced muscle strength in the lower extremities (20,34,39), together with altered neuromuscular control thought to affect knee joint kinematics and kinetics during level gait and stair ascent/descent (11,14,16,17,32). However, it is not known whether these changes precede or follow because of knee OA.
Meniscectomized patients are at high risk of developing knee OA and thus constitute a good model to study OA onset (7,8). In a recent study on middle-aged meniscectomized patients, no reductions were reported in any muscle strength variables despite patients self-reporting more pain and reduced physical function compared with healthy controls ∼2 yr after meniscectomy (37). However, a clinically relevant difference of ∼10% was observed between meniscectomized patients and controls in clinical tests, indicating impairments in functional tasks with multiple degrees of freedom (37). Reduced functional capacity may reflect a movement strategy to minimize pain and to protect the knee joint by reducing joint range of motion (ROM) and movement speed and may, as such, be accompanied by altered patterns of neuromuscular activity. Changes in neuromuscular activity might involve increased muscle coactivation and altered medial versus lateral muscle activity, which have been previously reported in knee OA patients (11,14-17,19,32).
Changes in the neuromuscular activity pattern of prime mover thigh muscles in OA patients could potentially affect the focal concentration of bone-on-bone contact forces in the knee joint during locomotion. Further, long-term alterations in neuromuscular activity profile may precede future muscle strength deficits and either contribute per se to the development of OA or, alternatively, reflect an adoptive countermeasure strategy that is insufficient to prevent OA development. Stair descent constitutes a useful model to investigate such potential changes in neuromuscular control and loading, representing a demanding complex daily locomotor task with multiple degrees of freedom.
Several longitudinal training studies have demonstrated that resistance training and neuromuscular training can induce changes in the neuromuscular activity and control of muscles crossing the knee joint (1,9,27). Thus, it seems important to gain knowledge of specific changes in neuromuscular activity profile in meniscectomized patients at high risk of knee OA to design effective interventions to optimize knee joint loading and possibly prevent or postpone knee OA development in these patients.
The aim of the current study was to identify differences in knee ROM, movement speed, ground reaction forces (GRF) and neuromuscular activity including muscle coactivation and medial versus lateral muscle activation during stair descent in patients meniscectomized for symptomatic degenerative meniscal tears compared with healthy controls. We hypothesized that patients would display altered patterns of neuromuscular activity including alterations in agonist-antagonist muscle coactivation, accompanied by a decreased range of knee joint motion and reduced movement speed along with reduced GRF to adopt a movement strategy with minimized knee joint loading compared with the nonoperated leg and with healthy controls.
Patients, 35-55 yr old at the time of surgery, who had 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. The age criteria were set to include most patients with degenerative meniscal tears but without knee OA. Patients were excluded if they were misclassified by the surgical code system, if they had had a previous knee ligament injury or severe cartilage changes defined as deep clefts or visible bone at the time of meniscectomy, or if they self-reported comorbidities limiting participation in the study. A modified version of The Self-Administered Comorbidity Questionnaire developed by Sangha et al. (30) was used to identify comorbidities.
The controls (35-55 yr old), from the same geographic region as the patients, were identified through the Danish Civil Registration System. Subjects were excluded if they had had a previous knee ligament injury, knee surgery, or self-reported comorbidities limiting participation in the study. The study aimed at matching patients and controls (i.e., on age and sex) at a group level.
After the informed consent form was signed, knee pain was assessed using the Knee Injury and Osteoarthritis Outcome Score (KOOS) (29) followed by measurements of body height and weight. The KOOS also assesses knee-related quality of life, other symptoms, and function during activities of daily living and during sport and recreational activity. Only scores from the pain subscale are reported in this study. A normalized score is calculated for each subscale (0 indicating extreme symptoms and 100 indicating no symptoms). The KOOS has been validated for meniscectomized patients and has shown high test-retest reproducibility (28,29).
After placement of EMG electrodes and electrogoniometers (more details given below), the subjects were asked to descend a four-step staircase at a self-chosen speed, without the use of hand rails and wearing their own comfortable walking shoes. At the bottom of the stairs, subjects continued walking performing a horizontal transition step down onto a force plate imbedded in the floor. The horizontal staircase position was adjusted relative to the position of the force plate so that the length of the horizontal transition step corresponded to one-third of the total leg length for each individual subject (measured from the midpoint of the greater trochanter to the midpoint of the lateral malleolus). Subjects were carefully instructed to continue walking until they reached a cone placed 2 m beyond the force plate. Subjects were allowed two to three stair descent trials for the purpose of familiarization before actual testing. Subsequently, two experimental trials were performed for each leg (i.e., the operated and nonoperated for the patients and the left and the right legs of the controls), and the average of these two trials was used for further analysis. Trials were repeated if visible hesitation, misplaced footing, or stumbles were observed. After the stair descent tests, the subjects conducted three isometric maximal voluntary contraction (MVC) trials for the quadriceps and hamstring muscles, respectively, for the purpose of EMG normalization. The staircase was designed with a rise of 16 cm, a depth of 23 cm, and a step width of 60 cm. The current study had experimental focus on the transition step between stair descent and subsequent level walking because this transition step involves high peak GRF (GRFpeak) and thus represents a demanding task for the knee joint during daily walking activities. The order of test leg was randomized for both groups, i.e., operated/nonoperated in the patients and left/right in the controls. In addition to the described test procedures, isokinetic muscle strength was also obtained as previously reported (37). The study was approved by the local ethics committee of the Region of Southern Denmark (ID S-20080044).
Knee angle recordings.
A flexible electrogoniometer (Biometrics SG150; Biometrics Ltd., Gwent, U.K.) was placed laterally across both knees of the subjects according to the manufacturer's manual to measure instantaneous knee joint angle during movement. Goniometer data were synchronously recorded with the EMG and force plate signals. During later offline analysis, the instants of foot strike and toe-off were determined from the GRF curve and used as temporal reference points. The goniometer was calibrated with the knee flexed at a 90° angle (0° = full extension).
Force plate analysis.
The methods used for data collection and processing are similar to those reported by Larsen et al. (18). In brief, a force plate (Kistler 9281 B; Kistler Instruments, Winterthur, Switzerland) was placed in the floor at a distance of one-third the leg length of the subject from the final step of the stairs to ensure that full foot contact was made as the person stepped down from the last step. The force plate was completely isolated from the staircase structure and the floor to avoid vibration artifacts. The vertical GRF signal (Fz) was recorded at 1000 Hz using a 12-bit A/D converter (DT 3010; Data Translation, Marlboro, MA) (18). Furthermore, two strain gauge-based load cells connected to a custom-made amplifier were integrated in the second and fourth steps of the staircase. The duration between contacts on the two load cells (steps) were determined from the load cell signals and used to calculate stride frequency. In the current study, analytical focus was given to the first part of the Fz signal (Fig. 1), which represents the vertical impact phase (i.e., weight acceptance) and thus comprises the phase of energy absorption and GRFpeak during ground contact and thus the phase most demanding for the knee joint. All Fz (GRF) signals were normalized as a percentage of body weight (%BW; Fig. 1) and rate of GRF rise during the initial stance phase (loading slope (Loadslope)) and the GRFpeak was calculated. GRFpeak occurred in the first half of the Fz signal (Fig. 1: Fz2). In some cases, an initial force peak (Fz1) was detected before Fz2, and if higher than Fz2, Fz1 was identified as GRFpeak. However, in most cases, Fz1 was lower than Fz2. Loadslope was defined as the mean rate of Fz rise in percentage of body weight (%BW·s−1) from the instant of foot strike to 80% of GRFpeak and reflects the ability to absorb GRF impacts during the initial phase of foot contact. Furthermore, the stride frequency (strides per minute) (Sfreq), average knee joint velocity (°·s−1) from foot strike to GRFpeak (Vmean), time from foot strike to GRFpeak (Tpeak GRF), and time for the entire stance phase (Tstance) were determined.
EMG recording and analysis.
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 stair descent and were subsequently normalized to the maximal EMG signal amplitude recorded during an MVC. MVC for the quadriceps and hamstring muscles were performed in a sitting position as maximal isometric extensor or flexor contractions, respectively. The hip was flexed at 90°, and the knee angle was in 60° of extension. Strong verbal encouragement was given during every contraction to promote maximal voluntary effort. EMG signals were obtained according to procedures reported elsewhere (18,38) and in agreement with SENIAM recommendations (www.SENIAM.org) using 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. 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 synchronously sampled at a 1000-Hz sampling rate along with the goniometer and force plate signals. During subsequent analysis, any potential DC offset was removed from the raw EMG signals by linear detrending, and subsequently, the signals were digitally high-pass-filtered at the 5-Hz cutoff frequency, followed by full-wave rectification and low-pass filtering at the 10-Hz cutoff frequency (2). All filtering routines used fourth-order zero-lag Butterworth filters. Finally, all EMG signals were normalized to their peak EMG amplitude during MVC. Neuromuscular activity was calculated as the mean normalized EMG amplitude during the loading slope phase (Actload) and at peak GRF (Actpeak GRF; mean in a 20-ms time interval before the instant of GRFpeak).
As described by Larsen et al. (18), the magnitude of agonist-antagonist muscle coactivation was calculated as the magnitude of relative normalized signal overlapping (common EMG − signal area) for two EMG signals, namely, EMGa and EMGb, relative to the total EMG signal area calculated in a given time interval.
Muscle coactivation was calculated for the whole thigh and separately for the lateral and medial parts of the thigh, respectively, during the loading slope phase (Coactload: from the instant of foot strike to 80% GRFpeak) and at peak GRF (CoactpeakGRF; mean in a 20-ms time interval before the instant of GRFpeak).
In addition, to investigate the distribution of medial versus lateral muscle activity, we also calculated mean medial ((VM + ST)/2) and mean lateral ((VL + BF)/2) neuromuscular activity, respectively, in the leg operated on and nonoperated leg of the patients and for the left/right leg of the controls during the initial weight acceptance phase (loading slope phase) and at GRFpeak (mean in a 20-ms time interval before the instant of GRFpeak).
The Student's unpaired t-test and the Mann-Whitney test were used to compare subject characteristics between patients and controls as appropriate. Furthermore, the Student's paired t-test was used to evaluate differences between medial and lateral muscle activity within the different legs (i.e., operated on, nonoperated, and control legs). A mixed linear model (26) was used to evaluate differences between legs in the kinematic, kinetic, and EMG variables of interest with "subject" as random effect and "leg" (i.e., leg operated on and nonoperated leg for the patients and the left and the right legs of the controls) as fixed effect. If data did not follow the Gaussian distribution, they were log-transformed before analysis but are still presented as non-log-transformed means. Correlation analysis was performed using Spearman ρ to examine the relationship between the magnitude of self-reported pain in patients and the outcome variables obtained in the leg operated on that were significantly different from those of the nonoperated leg or controls. Stata 10.1 (Statacorp, College Station, TX) was used for all statistical analyses, with a prespecified level of significance = 0.05.
A total of 31 patients and 31 controls were ultimately examined. A detailed explanation of the recruitment flow has previously been published (37). Because of equipment malfunction on two consecutive testing days, five patients and five controls had to be excluded from this analysis. Furthermore, four patients reported knee injuries to the contralateral knee (which had previously not been reported). These patients were also excluded. Thus, data are presented for the remaining 22 patients and 26 controls. The characteristics of the participants are shown in Table 1. Patients and controls were similar in all variables, except patients reported more knee pain than controls (P < 0.001; Table 1).
Kinematic and kinetic variables.
No differences were observed between patients and controls in ROM, movement speed, and GRF variables. However, patients showed a reduced stance phase (Tstance) when stepping out on the force plate on the operated leg compared with the nonoperated leg (post hoc test, P = 0.01). In support, there was a tendency for increased stride frequency (Sfreq) in trials where patients performed the stair descent transition step using the operated leg compared with the nonoperated leg (Table 2).
Neuromuscular activity and muscle coactivation.
No differences were observed in level of activation among the operated, nonoperated, and control legs (Fig. 2). Patients displayed less activity in the medial hamstring muscle (ST) compared with the lateral (BF) hamstrings muscles in the operated and nonoperated legs. This pattern of lower medial versus hamstring muscle activity was also observed in controls. Furthermore, patients showed increased medial (VM) versus lateral (VL) muscle activity at peak GRF (Actpeak GRF) in the nonoperated leg (P ≤ 0.05), along with a tendency toward reduced medial (VM) versus lateral activity (VL) in the operated leg (Fig. 2). No differences in medial versus lateral muscle activity were observed for the quadriceps muscle in controls. The magnitude of muscle coactivation was similar in patients and controls. However, controls showed a tendency to a higher level of coactivation compared with patients in the medial part of the thigh during the loading slope phase (Fig. 3).
Medial versus lateral leg muscle activity.
No differences were observed in mean medial (VM + ST) versus mean lateral (VL + BF) muscle activity among the operated, nonoperated, and control legs (Fig. 4). However, in meniscectomized legs, the mean neuromuscular activity was lower in the medial compared with the lateral thigh muscles during the loading slope phase (P ≤ 0.05) and at GRFpeak (P ≤ 0.01) (Fig. 4). In contrast, no mediolateral differences in overall thigh muscle activity were observed for the nonoperated leg or in control legs (Fig. 4).
Relationship between patient-reported pain and selected variables.
Correlation analysis was performed between KOOS pain score and duration of the stance phase (Tstance) and mean medial (VM + ST) muscle activity during the loading slope phase and at GRFpeak, respectively. A negative relationship was observed between KOOS pain and Tstance (rs = −0.47, P = 0.03), whereas no relationship was observed between self-reported pain and medial muscle activity.
The aim of the current study was to examine whether altered patterns of neuromuscular activity and agonist-antagonist muscle coactivation could be identified in middle-aged meniscectomized patients at high risk of future knee OA between the operated and nonoperated legs and compared with healthy controls. Such alterations could potentially affect knee joint kinetics and kinematics and hence influence the development of OA. We did not observe the hypothesized differences between patients and controls, but we observed a shorter stance phase (Tstance) in the meniscectomized leg compared with the nonoperated leg in patients. Furthermore, lower neuromuscular activity was observed in the medial (mean VM + ST) compared with the lateral (mean VL + BF) thigh muscles in the meniscectomized leg of patients. This may represent early changes in neuromuscular control in the initial state of knee OA development.
Previous studies on patients with knee OA have reported increased levels of leg muscle coactivation (14,15,19,32), altered medial versus lateral muscle activation (11,16,17), and increased knee adduction moment (3,19) during gait and stair ascent/descent. It is not clear whether these changes are a consequence of knee OA or precede the disease. Several studies have been conducted on the biomechanics of gait and stair ascent/descent (4,6,21,22,35,36) and changes in neuromuscular activity (6,10,21,22) in meniscectomized patients. However, the above studies either involved younger patients with traumatic meniscal tears (4,6,21,22) and/or patients soon after surgery, thus representing early postsurgical recovery (6,10,22,35,36). Observed deficiencies, therefore, might not only have been due to the meniscal tear per se but may also have been due to the surgical procedure itself (6,22,35,36). In the current study, middle-aged patients were examined ∼21 months after meniscectomy of degenerative tears to represent patients in a "preosteoarthritis" state (7,8) while considered to be fully rehabilitated after surgery.
In contrast to our expectations, no differences in any knee joint kinetic and kinematic variables were observed between patients and controls. Likewise, no differences emerged in knee ROM (ROMstance and ROMweight), knee joint position (Anglefoot strike and Angletoe-off), or GRF between the operated and nonoperated legs of the patients (Table 2). Nevertheless, a reduced Tstance (∼3%) was observed in meniscectomized legs compared with nonoperated legs. Thus, our hypotheses of an altered kinetic and kinematic profile in meniscectomized patients were only partially confirmed by the current data, but differences were only evident between the operated and nonoperated legs of the patients. The finding of a 3% reduced Tstance during the stair-to-ground transition phase in the meniscectomized leg compared with nonoperated leg is probably of limited clinical significance, although it potentially reflects a greater reliance on the unaffected limb during stair descent. However, the finding of a negative relationship between pain and the duration of the stance phase in the operated leg (i.e., more pain was associated with a longer stance phase) indicates that a useful strategy to minimize pain during stair descent in this population is by producing a given amount of kinetic impulse (momentum) using an extended time of contact (t) and thereby reduce the magnitude of contact force (F) exerted in the knee joint (since Δmomentum = Ft). Thus, the above relationship may be a sign of pain contributing to an asymmetric movement pattern in an attempt to reduce knee joint load.
It was expected that meniscectomized patients would demonstrate altered patterns of neuromuscular control including increased muscle coactivation, which have been suggested to affect knee ROM. However, contrary to our expectations, knee ROM did not differ between patients and controls, but patients tended to have lower muscle coactivation in the medial part of the thigh than controls during the weight acceptance phase (Fig. 3).
In the current study, neuromuscular activity was generally lower (∼50%) in the medial (ST) versus lateral (BF) hamstring muscles in both legs of the patients. A similar pattern was observed in controls (∼40% lower medial activity), indicating that this represents a general and normal pattern of hamstring activity during stair descent (Fig. 2). Clinicians often observe medial quadriceps (VM) atrophy and neuromuscular deficits after knee injury and delayed VM versus VL muscle activity onset has been reported in patients with patellofemoral pain (5). Our results seems to support this notion because neuromuscular activity tended to be lower in the medial (VM) compared with the lateral (VL) quadriceps in meniscectomized legs at GRFpeak.
The current study also investigated the distribution of overall medial versus lateral muscle activity because skewed patterns of medial versus lateral muscle activity could potentially affect knee control/function and joint stability. No differences were observed between mean medial (VM + ST) and mean lateral (VL + BF) muscle activity among the operated, nonoperated, and control legs. However, we observed reduced (∼20%) medial compared with lateral mean muscle activity in meniscectomized legs. In contrast, no differences in medial versus lateral muscle activity were observed in the nonoperated legs of patients or in controls. Increased levels of lateral muscle activity have previously been observed in patients with knee OA compared with controls (11,16), increasing with OA severity (17). This likely represents a neuromuscular strategy to reduce knee adduction moment and decrease medial knee joint compartment loading (11). Thus, the reduction in medial muscle activity currently observed in meniscectomized legs could reflect a strategy to decrease compression forces in the medial compartment of the knee joint. The specific effect of attenuated medial muscle activity on biomechanical knee joint loading profile and specifically on the knee adduction moment, which is often used as a surrogate measure for medial knee compartment joint loading (24,31,40) and is associated with medial knee OA severity (33), currently remains unknown. Recently, Netravali et al. (23) reported that patients meniscectomized for medial meniscal tears in the posterior part of the meniscus (similar to the present patients) showed increased external rotation of the tibia throughout the stance phase during walking. The presence of such a gait pattern is likely to affect knee joint stability and could be an alternative explanation for the altered medial versus lateral muscle activity in the meniscectomized legs in this study.
The patients examined in the current study self-reported elevated levels of knee pain compared with population-based controls. Increased pain feedback may be a contributor to the reduced medial muscle activity. Pain has also been suggested to be a contributing factor in arthrogenic muscle inhibition (AMI) (25) resulting in reduced motor drive to the muscles surrounding an injured joint (13). Henriksen et al. (12) recently reported reduced levels of muscle activity in response to experimentally induced VM muscle pain during a forward lunge. However, in the present study, we observed no relationship between pain and reduced medial muscle activity indicating that pain was probably not the main cause of the observed alterations in neuromuscular activity during stair descent.
We recently reported no differences in maximal muscle strength between the operated and nonoperated legs of the same patients as the present study (37), indicating that changes/asymmetries in neuromuscular activity potentially precede the occurrence of future strength deficits/asymmetries in this population of patients. In the current study, the relatively modest limb-to-limb differences observed in patients may be due to the relatively short time interval between surgery and testing (i.e., ∼2 yr), and thus, the potential development of knee OA may not have progressed as much as in patients studied at later time points. Furthermore, this may also explain the current lack of gross systematic differences in neuromuscular activity and kinetic gait profile between patients and controls since early changes may manifest first as asymmetries between the operated and nonoperated leg of the patients, potentially leading to bilateral differences at more progressed stages toward knee OA.
The current study has limitations. First, this was a cross-sectional study. Thus, the underlying cause of the observed changes and the effect on knee OA development remains speculative. Second, in the current study, we used GRF as an indicator of knee joint loading; however, this measure may not reflect the actual magnitude of bone-on-bone contact forces exerted in the knee joint. Third, five patients and five controls were excluded because of equipment malfunction. These participants may have performed differently from the included participants. However, this is unlikely because both the excluded patients and the controls were highly similar to the rest of the participants (i.e., age, height, weight).
The hypothesized reduction in knee ROM, movement speed, and altered GRF kinetics and neuromuscular activity between patients and controls could not be confirmed. However, we observed a shorter stance phase in meniscectomized legs during the transition step between stair descent and level walking along with lower medial leg muscle activity in the meniscectomized leg. These findings support the hypothesis that meniscectomized patients demonstrate early modulations in kinematics and neuromuscular activity, which may represent a strategy to reduce knee joint pain. Further, the present study findings also indicate that training/rehabilitation of meniscectomized patients should focus also on neuromuscular control of the hamstring and quadriceps muscles and not rely entirely on muscle strength development alone. The current findings may represent an initial stage in the possible chain of events leading to knee OA in meniscectomized patients. The exact mechanisms of these changes and their effect on knee adduction moment and knee OA development remain unknown and warrant further investigation. Future studies should examine whether the observed biomechanical and neuromuscular changes are exacerbated in patients with a longer postsurgery time interval (i.e., representing patients at a more progressed state of knee OA development).
This study was supported by The Danish Rheumatism Association and the Region of Southern Denmark.
The results of the present study do not constitute any endorsement by the American College of Sports Medicine.
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Keywords:© 2011 American College of Sports Medicine
KNEE JOINT; OSTEOARTHRITIS; MENISCECTOMY; BIOMECHANICS; EMG