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Synergetic and Antagonist Muscle Strength and Activity in Women With Knee Osteoarthritis

Patsika, Glykeria MSc; Kellis, Eleftherios PhD; Kofotolis, Nikolaos PhD; Salonikidis, Konstantinos PhD; Amiridis, Ioannis G. PhD

Journal of Geriatric Physical Therapy: January/March 2014 - Volume 37 - Issue 1 - p 17–23
doi: 10.1519/JPT.0b013e31828fccc1
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Background and Purpose: People with knee osteoarthritis (OA) display limitations in daily activities and a lower quality of life. The purpose of this study was to investigate the differences in strength balance and activation during maximum strength efforts between women with knee OA and asymptomatic women.

Methods: Twelve women with knee OA (age 60.33 ± 6.66 years) and 11 controls (age 56.54 ± 5.46 years) performed maximum isokinetic eccentric and concentric knee extension and flexion tests at 60°/s, 120°/s, and 150°/s. Surface electromyography (EMG) was recorded from the biceps femoris (BF), vastus lateralis (VL), and vastus medialis (VM). Hamstrings-to-quadriceps moment ratios (H/Q), the synergetic (VL/VM), and co-contraction (BF/[VM + VL]) EMG ratios were calculated.

Results: Analysis-of-variance designs showed that women experiencing knee OA had significantly higher H/Q moment ratios and VM/VL EMG ratios than controls (P < 0.05). The co-contraction index was significantly lower in the OA group only during knee flexion (P < 0.05).

Conclusions: Women with knee OA showed a higher H/Q moment ratios probably because of the need for better joint stability or a lower quadriceps capacity. This deficiency was accompanied by a higher VM activation, which probably serves to stabilize the patella upon maximum contraction as well as a higher activation of antagonist muscles.

Laboratory of Neuromechanics, Department of Physical Education and Sports Science of Serres, Aristotle University of Thessaloniki, Greece.

Address correspondence to: Glykeria Patsika, MSc, Laboratory of Neuromechanics, Aristotle University of Thessaloniki, Department of Physical Education and Sport Sciences at Serres, 62110, Serres, Greece (gpatsika@phed-sr.auth.gr).

There are no conflicts of interest and no source of funding.

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INTRODUCTION

Osteoarthritis (OA) is the most common form of arthritis1 and the leading cause of chronic functional disability,2,3 especially in older people. People with knee OA display limitations in daily activities4,5 and a lower quality of life6 because of increased pain3,7 and muscle weakness.3,8 Women display a higher rate of OA symptoms at all ages1 and a greater risk of developing OA than men.9 Therefore, examination of muscle function in women with knee OA is worthwhile.

During joint movements, antagonistic muscle groups exert forces in opposite directions. The maximum strength capacity of the antagonist muscles relative to the corresponding maximum strength of the agonists is frequently considered as an index of muscle strength balance around a joint.10 For the knee joint, such balance has been traditionally examined using the concentric hamstrings to concentric quadriceps moment (Hcon/Qcon) ratio.11 The functional eccentric hamstring-to-concentric quadriceps (Hecc/Qcon) moment ratio and the concentric hamstring-to-eccentric quadriceps (Hcon/Qecc) ratio have been proposed as being more valid for describing strength balances during dynamic movements.12 During dynamic movements, hamstrings and quadriceps muscle groups simultaneously contract concentrically and eccentrically to promote joint stability. Functional ratio is more valid during dynamic activities because it contains information about agonist and antagonist strength balance. Furthermore, such balance may be an indirect indicator of the capacity of hamstrings to counteract the anterior shear force of the tibia relative to the femur.10 Previous studies suggest a conventional ratio between 0.6 and 0.8, which increases with the isokinetic angular velocity,13,14 while the functional ratio of 1.0 demonstrates a significant ability of hamstring muscles to provide more knee joint stability.12 Although quadriceps strength is often reduced in people with OA,4,15,16 the results for the flexion maximum moment are conflicting.5,16,17 Only 1 study15 has shown that people with knee OA show no differences in Hcon/Qcon ratio compared with controls. Such evidence is insufficient to conclude that knee OA is accompanied by no strength imbalances because functional ratios (Hecc/Qcon and Hcon/Qecc) have not been thoroughly examined in this population.

Muscle balance between the vastus medialis (VM) and the vastus lateralis (VL) muscle groups contributes to patellofemoral joint balance as well as patellar stability.18 An imbalance of these stabilizing muscles may reduce sensory joint innervations19 or proprioception.16 Abnormalities between the medial and the lateral compartments of the knee joint result in increased joint stress and damage of articular cartilage.20 However, research findings on the role of vastii muscle activity in women with OA are few and conflicting.21,22 Particularly, Wu et al.23 showed no imbalance between VM oblique and VL activation in people with knee OA during maximal isokinetic contractions, while those with knee OA and patellar malalignment exhibited an imbalance of quadriceps muscles. Moreover, Mairet et al.21 found higher agonist VM activation during isometric tests in the unaffected knee compared with the affected one; however, VL activity did not differ between the 2 limbs. In contrast, Hubley-Kozey et al.22 found that people with knee OA demonstrated higher VL muscle activation than controls during walking. Therefore, the question whether VM to VL (VM/VL) activation ratios are altered in people with knee OA remains unclear.

Coactivation is defined as the simultaneous activity of agonist and antagonist muscles surrounding a joint.24 The primary role of coactivity is to increase joint stiffness and thus to stabilize the knee joint.25,26 Several studies have shown that people with knee OA exhibit higher antagonist coactivation during walking than those without OA.4,27 While coactivation may be beneficial for stabilizing and controlling the motion of the knee joint,28,29 a higher coactivation might cause further pain,30 increase joint loading,31 and possibly contribute to further loss of articular cartilage.32 However, it has been found that coactivation during isometric knee extension efforts is not associated with reductions in isometric extension moment in people with OA.33 Whether such coactivity is higher in persons with OA during maximum isokinetic strength tests is not clear.

The purpose of this study was to investigate the differences in strength balance and muscle coactivity during maximum isokinetic strength efforts between women with knee OA and controls without OA. We hypothesized that women with knee OA would display a lower strength balance and higher synergetic and antagonistic coactivation than controls.

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SUBJECT AND METHODS

Subjects

The participants were recruited from a local center for the elderly care. Particularly, in consultation with the medical staff, women who experienced medical conditions that precluded safe participation (eg, stroke, cardiovascular or pulmonary diseases), history of previous hip or knee fracture, clinical or radiological hip OA, bilateral knee OA, and surgery of spine or lower extremities were excluded from the study. Subsequently, 12 women with knee OA [mean age 60.33 (SD = 6.66) years; mean height 1.61 (SD = 0.05) m; mean body mass 77.08 (SD = 9.2) kg; body mass index 29.49 (SD = 3.39) kg/m2] and 11 controls [(mean age 56.54 (SD = 5.46) years, mean height 1.64 (SD = 0.05) m, mean mass 77.36 (SD = 13.34) kg, mean body mass index 28.60 (SD = 4.11) kg/m2] agreed to participate in this study. Women with knee OA had grade II (5 women) or III (7 women) unilateral disease, in tibiofemoral compartment, as evidenced by radiographic assessment using Kellgren and Lawrence criteria.34 They also exhibited radiographic signs of hypertrophic changes, marginal spur formation, subchondral sclerosis, or cyst formation or nonuniform joint space narrowing. In contrast, healthy subjects had no pain or any injury of the knee or hip joint. All participants signed a written informed consent form, approved by the Aristotle University ethics committee.

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Instrumentation

Maximum isokinetic tests were performed on a Cybex isokinetic dynamometer (CYBEX Division of Lumex, Ronkonkoma, New York). Electromyographic (EMG) measurements were recorded using a remote EMG (Biopac Systems Inc, Goleta, California). A 2-axis electrogoniometer (Model TSD 130B, Biopac Systems, Inc, Goleta, California) was used to record the angular position of the knee. A Biopac MP100 Acquisition Unit (Biopac Systems Inc, Goleta, California), sampling at 1000 Hz, was used to collect angular position, moment, and EMG signals.

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Procedure

The skin was shaved and then cleaned with alcohol wipes to remove any dead cells. The bipolar Ag-Ag/Cl surface EMG electrodes (diameter 2 cm, distance 1 cm) were placed according to S.E.N.I.A.M. recommendations.35 Electrodes were placed over the long head of the biceps femoris (BF), half way on the line between the ischial tuberosity and the head of the fibula. Electrodes were also located on the VL and VM of the quadriceps. The exact position for the VL was on the bulk of the muscle, half way between the lateral femoral epicondyle and greater trochanter and for the VM was over the distal position of the muscle, 10 cm more and medially from the superior border of patella. The ground electrode was placed on a bony prominence and its position was not altered during any of the testing procedures.

Before the testing protocol, subjects were familiarized with the isokinetic dynamometer. The subjects were positioned on the chair with hip flexion angle at 115° (hip full extension = 180°). The thigh, pelvis, and trunk were stabilized with straps. The axis of knee rotation was aligned with the lateral femoral condyle. The familiarization and warm-up contained 3 maximal concentric and eccentric repetitions at each angular velocity of the protocol. The range of motion was from 0° (full extension) to 90° (of knee flexion). During testing, the subjects performed 5 maximal concentric and eccentric efforts of the knee extensors and knee flexors at angular velocities of 150°/s, 120°/s, and 60°/s. These angular velocities were selected because the knee joint operates at similar speeds during daily life activities.4,36 Isokinetic testing at higher angular velocities is prone to errors due to the effects of inertia.37

An interval of 20 seconds between tests was used to minimize fatigue effect. Three maximal isometric knee extension and flexion efforts at 65° and 30° were used to normalize the raw EMG signals. These angles were selected because they are characterized by a greater moment and EMG activity by the respective muscle groups during isokinetic tests.38,39 The position of the electrodes did not change during the test, and all tests were performed by the same investigator. The subjects were instructed to resist maximally through the whole range of motion during the test.

The data were analyzed using AcqKnowledge (Version 3.9.1., Biopac Systems Inc, Goleta, California). The gravity-corrected moment, angular position, and angular velocity were collected at frequency of 1000 Hz. The EMG signal was amplified (gain × 1000) with an input impedance of 10 MΩ and a common rejection ratio of 130 dB. The signal was filtered using a band pass filter (low 15 Hz and high 450 Hz) to avoid noise from other electrical devices and movement artifacts. Following full wave rectification, the root mean square (RMS) was calculated with a step of 10 samples.

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DATA ANALYSIS

The repetition with the maximum joint moment was analyzed from the 5 repetitions. The range of motion was restricted from 10° to 80° to avoid inertial effects.40 All isokinetic signals were averaged from 10° to 80° of knee flexion. The conventional Hcon/Qcon and the functional ratios Hecc/Qcon and Hcon/Qecc10,41 were calculated.

All isokinetic EMG signals of agonist muscles were normalized as a percentage of the RMS activity during isometric effort. The antagonist RMS was normalized as a percentage of the same muscle EMG when acting as agonist at the same angular velocity. In addition, 2 types of coactivation were analyzed. First, we calculated the VM/VL EMG ratios, during knee flexion and extension. Second, we calculated the coactivation ratio, as the ratio of agonist to antagonist muscles during knee flexion (2BF/[VL + VM]) and extension ([VL + VM]/2BF), separately.

A higher co-contraction index indicates more activation of the agonists relative to the antagonists.

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STATISTICAL ANALYSIS

Two-way analysis-of-variance (2 × 3) designs were used to examine group differences of conventional and functional ratios, at each of 3 angular velocities (60°/s, 120°/s, and 150°/s). Furthermore, a 3-way (2 × 2 × 3) analysis of variance was applied to examine group differences in VL/VM and coactivation EMG ratios for each type of muscle action (concentric and eccentric) and angular velocity (60°/s, 120°/s, and 150°/s). Significant F values were followed by Tukey's post hoc tests to determine which pair means were significantly different.

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RESULTS

H/Q Moment Ratios

The Hcon/Qcon moment ratios are presented in Table 1. The ANOVA did not show a statistically significant interaction between group and velocity on Hcon/Qcon moment ratios (F2,21 = 1.98; P = 0.151). However, a significant main effect was found for group (F1,21 = 36.45; P = 0.000); women with knee OA had a greater Hcon/Qcon moment ratio. The actual Hecc/Qcon and Hcon/Qecc moment ratios are presented in Table 2. There was also a main effect of group; women with knee OA also had significantly higher Hecc/Qcon (F2,21 = 9.702; P = 0.005) and Hcon/Qecc moment ratios (F1,21 = 18.171; P = 0.000 < 0.05).

Table 1

Table 1

Table 2

Table 2

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VM/VL EMG Ratio

The VM/VL EMG ratio values are presented in Figure 1A. The ANOVAs showed a significant 3-way interaction effect (group × muscle action × angular velocity) during extension (F2,21 = 9.063; P = 0.001) and flexion (F2,21 = 3.250; P = 0.05). Post hoc Tukey's tests showed a higher VM/VL EMG ratio at the eccentric 120°/s (extension) and concentric 60°/s (flexion) test in women with OA. Furthermore, there was a significant main effect for group either in extension or in flexion, as women with knee OA demonstrated a higher VM/VL EMG ratio (collapsed across testing conditions) than controls.

Figure 1

Figure 1

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Coactivation EMG Ratios

The coactivation EMG ratios are presented in Figure 2. The ANOVA results showed a statistically significant 3-way interaction effect (F2,21 = 6.31; P = 0.004) during knee extension (Figure 2A). Post hoc Tukey's tests indicated that women with OA had smaller coactivation ratios than controls at the 150°/s concentric test while the opposite was found for the eccentric 120°/s test (P < 0.05). For knee flexion (Figure 2B), no statistically interaction effect was found between group, muscle action, and angular velocity (F2,21 = 1.02, P = 0.34). However, there was a significant main effect for group; women with OA demonstrated smaller coactivation ratios (collapsed across testing conditions) than controls (F1,21 = 9.16; P = 0.006).

Figure 2

Figure 2

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DISCUSSION

The main findings of this study are that, compared with controls, women with knee OA demonstrated higher H/Q moment ratios. Moreover, OA women showed higher VM/VL EMG activation ratios, but lower coactivation ratios than controls.

We have found that Hecc/Qcon and Hcon/Qecc moment ratios were higher in women with knee OA (Table 2). To our knowledge, the functional ratio in people with knee OA has not been previously investigated. Our results could be mainly attributed to a lower strength of the quadriceps relative to the hamstrings, as evidenced in previous studies.9,16,42 In fact, Slemenda et al.16 reported that OA weakness around the knee joint does not involve the flexors but largely involves the extensors muscles. This may be associated with quadriceps muscle atrophy43 or a shorter quadriceps moment arm display by people with knee OA.33 Lower strength capacity, during walking, has been found to have an association with high loads at the knee joint.44 Therefore, it is reasonable to suggest that a high Hecc/Qcon ratio may increase the potential of muscles to counter the anterior displacement of the tibia relative to the femur and to improve the dynamic joint stability in people with knee OA, when necessary.

In this study, women with knee OA showed higher VM/VL EMG ratios than controls (Figure 1). Increased activation of VM in women with knee OA in this study (Tables 1 and 2) may be needed to stabilize the patella in the medial compartment of the knee joint. In addition, people with knee OA may adopt an alternative activation strategy of the vastii muscles to decrease the loads from the opposite compartment of the knee. We assume that women with knee OA in this study have activated the VM muscle to decrease the loads in the medial compartment. Our results are in contrast with those reported by Wu et al.23 during isokinetic efforts in people with symptomatic knee OA, while they are in agreement with people with knee OA with patellar malalignment. These different results may indicate the importance to separate the long head from the oblique head of VM muscle, which may be activated differently. Moreover, different angular velocities, grade of OA, and different samples are the reasons that we may have altered muscle activation.

In this study, we found inconsistent evidence regarding group differences in coactivation ratios (Figure 2A) during knee extension and a smaller coactivation ratio during knee flexion (Figure 2B). This finding is in line with previous studies that have shown that people with knee OA exhibit higher levels of antagonist activation in daily activities than typical individuals.4,27 While this mechanism protects the knee by providing more stability, higher levels of coactivity increase articular loads.45 This may alter knee joint function by increasing the degeneration of the articular cartilage46 via alterations in the line of action of muscle force.47 We can, therefore, assume that a higher antagonist activation by women with knee OA may help them reduce joint pain by increasing joint stiffness but it may increase joint loads.32 Such a strategy is not observed when the knee extends but also when the knee flexes (Figure 2B).

Many factors may explain the present findings. For example, people who display knee muscle weakness, such as people with knee OA, are characterized by fiber type II atrophy.48,49 In contrast, an increase in type I muscle fibers may increase muscle stiffness.50 This mechanism is adopted so that people with knee OA may decrease pain, although the relationship between muscle strength and pain is not always linear.51 Proprioceptive information is provided by the articular mechanoreceptors to the central nervous system,52 and it is necessary for neuromuscular control during dynamic efforts.53 Therefore, injury that results in loss of mechanoreceptors could decrease the reflex response and information transmission to the central nervous system, thus leading to changes in coactivation of quadriceps and hamstrings muscles.54–57 Previous research studies have showed that coactivation might be affected by age,58,59 gender32 and grade of OA,60 contraction velocity,24 type of muscle action28 and level of training.61 Future research could examine the individual and combined effects of these factors on muscle synergetic and antagonist activity in people with knee OA.

Isokinetic tests have a low relationship with muscle function during daily activities, such as walking, climbing stairs, or standing up from a chair. This is because maximum strength represents only 1 factor that determines functional performance. In previous studies, conventional strength ratios were found to be unsatisfactory predictors of functional capacity,5,62 functional ratios might be better predictors for stair climbing and descending in people with knee OA.5

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CONCLUSION

Women with knee OA showed a higher H/Q moment ratio, higher VM/VL EMG ratio, and higher antagonist activation than asymptomatic individuals. Altered muscle activation during isokinetic tests may be a strategy that, used by people with knee OA, maintains knee joint integrity. In addition to quadriceps muscle strengthening, training programs could include exercises that enhance synergetic activity of the vastii muscles, better mobilize the patella, and provide improved coactivation balance of the antagonist muscle groups surrounding the knee.

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Keywords:

arthritis; coactivation; hamstrings; moment ratios; quadriceps

© 2014 Academy of Geriatric Physical Therapy, APTA