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- SUBJECTS AND METHODS
Osteoarthritis (OA) of the knee is associated with disability due to pain, quadriceps dysfunction, and impaired proprioception. OA patients have up to 4° of error in their ability to reposition their limb and to perceive movement (1–11). However, little is known about the distribution of this error in the range of motion of the knee. Such information would be clinically important because from the distribution of the error one could infer the type of malfunctioning receptors and improve the design of rehabilitation protocols. Joint receptors contribute to position sense primarily at the extremes of the joint range of motion and muscle receptors discharge to indicate limb position in the midrange; therefore, it is important to determine where in the range of motion the proprioceptive error is the largest (12, 13). Thus, one aim of the present study was to determine the distribution of error in knee joint proprioception in age- and sex-matched subjects with and without knee OA.
Injury to a joint affects the magnitude of maximal strength as well as the control of force produced by the muscles surrounding the joint (14, 15). Adequate control of submaximal muscle forces is especially important in activities of daily living (ADLs) that are normally executed at a fraction of the available maximal muscle strength in young and middle-aged adults (16). Accuracy and steadiness of force production are 2 forms of force control that have been used widely to assess the quality of force production in geriatric populations in a variety of muscles and tasks (17–19). However, it is unknown if the quantitative reduction of maximal strength of the quadriceps muscle in patients with knee OA is accompanied by a concomitant impairment of submaximal forces. Such information is clinically relevant for understanding locomotor deficits and improving currently used exercise rehabilitation programs.
Another hallmark symptom of knee OA is quadriceps weakness. Compared with age- and sex-matched healthy adults, patients with knee OA present with 10–60% less quadriceps muscle strength (8, 20–22). Quadriceps weakness is normally quantified as a reduction in maximal isometric and isokinetic concentric muscle strength. However, ADLs also comprise eccentric or lengthening contractions and it is unclear if quadriceps weakness is present to the same extent in this expression of maximal eccentric strength (23). This is an especially relevant issue for knee OA patients who have quadriceps weakness due partly to incomplete muscle activation (8, 24); even healthy young adults are often unable to fully activate their muscle during a maximal effort eccentric contraction (25). In addition, in eccentric contractions, some researchers observed a preferential recruitment of type II muscle fibers (26) and a greater selective atrophy of type II muscle fibers in muscles around joints with OA compared with muscles of age-matched controls (27, 28). Thus, it is reasonable to hypothesize that patients with knee OA would exhibit weakness in eccentric strength.
Taken together, the aim of the present study is to compare the distribution of error in knee joint proprioception, force accuracy and steadiness, and the force-velocity relationship in patients with grade II knee OA and age and sex-matched healthy adults. Special attention will be paid to eccentric strength. The characterization of these aberrations represents a shift from the traditional quantification of quadriceps dysfunction to the identification of novel control properties of quadriceps force production in patients with knee OA.
- Top of page
- SUBJECTS AND METHODS
The finding of 2.4° impairment of proprioception in patients with knee OA is consistent with the 1–4° error found using similar (2, 9) or other methods of assessing proprioception (2, 3, 10, 11). A new finding in the present study is that subjects with knee OA produce more joint position error at 2 of the 5 positions in which the knee is in the most extended positions. In contrast, healthy subjects have a similar magnitude of error at different knee positions throughout the range of motion. In addition, nearly 70% of the error in OA patients came from overshooting the target. So far it is unknown if the magnitude of knee joint proprioception error is evenly distributed in the range of motion. Previous studies determined the error at specific knee joint positions and reported the average error across the entire range of motion (2, 9–11). In a viscosupplementation study, knee OA patients, as in the present study, produced significantly more error in more extended knee joint positions (31). However, that study did not use a healthy control group and the OA patients were older and more debilitated than our OA patients.
The findings that proprioception errors occurred in the more extended knee positions and were due to overshooting the target indicate a reduction in the sensitivity of the proprioreceptors in OA subjects' knee joints. These receptors could include the quick-adapting Pacinian corpuscles, which sense joint motion, and the slow-adapting Ruffini receptors, which sense joint position. In the more extended knee positions, the quadriceps muscle is at a short length and the source of the proprioceptive dysfunction would be less likely to emanate from the Ia afferent muscle receptors, which primarily contribute to proprioception at longer lengths of muscle (11–13). Another possibility is that in the extended knee positions, reciprocal inhibition from the quadriceps to stretched hamstrings is not as effective in knee OA, contributing to the proprioception errors (32, 33).
This study is the first to demonstrate a link between knee proprioception error in knee OA and performance in ADLs (3). We observed a moderate relationship of r = 0.57 (P < 0.01; Table 6) between the average proprioception error at the 2 most extended knee positions and the time to execute ADLs, without a significant association between knee pain and proprioception errors. OA patients must select a configuration of joint positions for gait that produces the least discomfort. Slow gait facilitates this selection. The argument was made that an error of only 1–1.5° in knee joint position at heel strike and the late phase of swing during gait could contribute to OA subjects' altered gait and to the exacerbation of knee OA (8, 34). Although knee joint position at heel strike during gait may not differ between OA and healthy individuals (35), the amount of maximal flexion is smaller by 3–4°, resulting in a more extended limb during stance (36, 37). In addition, OA subjects compared with healthy adults had up to 2-fold greater variability in knee joint flexion while executing ADLs (35). Impaired proprioception can contribute to this increased variability. Taken together, OA patients have an aberrant proprioception system that increases the potential for positional errors in ADLs and reduces the potential to sense and correct such errors. Proprioception errors manifest in ADLs by increasing the variability around the correct limb position and contributing to altered gait (8, 34).
Force accuracy and steadiness describe the quality of submaximal force production. There is strong evidence to suggest that muscle force accuracy and steadiness decline with age (17–19), but it is unknown if such an impairment would also occur in knee OA. Our expectation that OA subjects do exhibit such impairment is based on the observation that individuals with a joint malfunction or injury present with some form of impaired force control (8, 11, 14, 24, 38). Indeed, our data indicate that OA patients had 89% more error in a force-matching task and had 155% greater variation in producing force smoothly. These data document a novel qualitative aberration in the quadriceps muscle of knee OA subjects and expand on the findings of many studies that reported quantitatively reduced maximal voluntary strength in knee OA (8, 20–23, 38–40).
The error in accurately matching the 50-N and 100-N target forces resulted from overshooting the target. Force accuracy generally improves with increasing force levels but when it is present, the error is almost always in the positive direction (17, 19). The OA group also followed this pattern and exerted more force than was necessary to reach the target under dynamic conditions.
We also observed significantly less steady force production of the quadriceps muscles in patients with knee OA compared with healthy subjects. Force steadiness was similar at the 2 target forces of 50N and 100N, even after the steadiness data were normalized for force and expressed as coefficient of variation (data not shown). By coincidence, the 50-N target force in the OA patients and the 100-N target force in healthy subjects represented about the same relative force of the maximal eccentric (∼17%) and concentric (∼24%) voluntary contraction, and the large differences in steadiness still persisted at the same relative force levels. These data suggest that the impaired ability of the quadriceps muscle to control force in OA patients is not the result of OA patients' reduced maximal quadriceps strength.
In previous reports, force steadiness improved with increasing force levels in old adults (for review see reference 18), but we found that OA patients' force steadiness was equally impaired at low and moderate force levels. Thus, the possibility exists that OA patients have difficulty in producing force smoothly with their quadriceps muscle over a broader range of forces than healthy age-matched adults (Table 5) and old adults (18, 19). Compared with healthy subjects, force steadiness in OA patients was especially impaired during eccentric contraction, less impaired during concentric, and unimpaired during isometric contraction. Coupled with their reduced ability to produce maximal eccentric force, the poor eccentric force steadiness and accuracy in OA patients suggest a generalized impairment of generating and controlling maximal and submaximal eccentric quadriceps force. This conclusion is strengthened by the observation that the variability in OA patients' joint torques in ADLs was up to 3.9-fold greater (35).
There is extensive documentation in the literature that individuals with knee OA have a large deficit in isometric and concentric quadriceps muscle strength (8, 20, 21, 24). The results of the present study expand on these findings and suggest that the ability of OA patients to produce force while the quadriceps muscle lengthens is significantly more impaired than force production under isometric and concentric conditions.
The eccentric weakness in knee OA is probably of neural origin. Slemenda et al reported that quadriceps weakness was independent of muscle size in knee OA (21), and others reported that OA subjects were unable to fully activate the quadriceps during maximal isometric contractions (8, 20). Indeed, healthy individuals also have difficulty in fully activating their muscles during a maximal voluntary eccentric contraction due to neural inhibition associated with the high forces (25, 41). It is likely that eccentric weakness in knee OA is the combined effect of the natural inhibition associated with an eccentric contraction and the arthrogenous muscle inhibition uniquely present in knee OA. A parallel mechanism could be related to motor unit recruitment. In eccentric contractions, a preferential recruitment of type II muscle fibers occurs (26). Even though total quadriceps muscle size may be similar between individuals with and without knee OA (21), selective atrophy of type II muscle fibers has been observed in muscles around joints with OA (27, 28). This could partly account for the low eccentric strength in patients with knee OA.
The present data suggest that clinicians should evaluate proprioception in knee OA at multiple points in the range of motion, with special attention to errors in the more extended knee joint positions. Reduced knee joint proprioception in OA patients indicates the need to incorporate proprioception training in OA patients' exercise program to slow disease progression. It is unknown whether exercise can improve joint proprioception in patients with knee OA. Proprioception training of the ankle or knee after a ligament injury produced mixed results, probably due to the low specificity of the proprioception training in relation to the high loading rates of the joints used in the target tasks (42–45). Conceptually, OA patients are ideal candidates for training that uses a combination of weight-bearing and non–weight-bearing tasks for proprioception training because they are free of ligamentous injury and the loading rate of the knee joint during their slowed gait is also low (42). Although not a causative relationship, the correlation between proprioception errors and function suggests that improved proprioception may lead to improved function by improving the awareness of limb position in space, reducing pain, and increasing muscle strength (15, 42).
There was a moderate (r = 0.62) correlation between the time to execute ADLs and variability of force (steadiness), suggesting clinical relevance of impaired force control for daily function. Accurate scaling of eccentric force of the quadriceps is vital for successful execution of ADLs and it affects our ability to achieve the necessary force and alters the kinematics of the limb. For example, stair descent is dominated by eccentric quadriceps contractions (46), and this ADL is associated with the highest rate of falling (47). In addition, the magnitude of force fluctuation may vary between steps of gait (18), and this fluctuation can be exacerbated by errors due to proprioception. Clinicians should consider using low-intensity and very low-intensity resistance exercise, which are known to improve force steadiness in old adults (18, 19). These low-intensity exercise programs are appropriate precursors to moderate-intensity exercise using accentuated exercise with eccentric contractions, longer in duration or higher in load, to combat eccentric weakness in knee OA (48, 49).
One limitation of the study is that we included relatively young individuals with moderate knee OA who were also free from other medical conditions, making our subjects somewhat unusual compared with subjects in many other studies. Another limitation is that the force accuracy and steadiness measurements were assessed at relatively low force levels, and it is unknown how these force levels compare with forces that occur during ADLs. We also tested force accuracy and steadiness in a single-joint test and not in a multijoint movement, as in ADLs.
In conclusion, the present study produced 3 new findings related to individuals with knee OA. We found that knee joint proprioception error is greater in the more extended than flexed knee joint positions. We also found that OA patients have an impaired ability to accurately and steadily produce submaximal quadriceps forces. Finally, we observed a preferentially large reduction in maximal eccentric strength. In total, the data suggest that quadriceps weakness in knee OA includes not only an impaired ability to produce maximal strength, but also an impaired ability to control submaximal force. These results have implications for designing exercise and rehabilitation programs for patients with knee osteoarthritis.