Quadriceps strength (knee extensor torque) is an important correlate of physical function in individuals with hip osteoarthritis (OA). However, it remains unclear whether the ability to rapidly generate quadriceps torque in the early phase of muscle contraction (maximal rate of torque development [MRTD]) is also associated with physical function. The purpose of this study was to quantify the independent impact of quadriceps strength and quadriceps MRTD on self-report and physical performance measures of physical function in community-dwelling adults with hip OA.
Ninety-two adults with radiographically confirmed symptomatic hip OA (mean age 62 years) participated. Unilateral isometric quadriceps strength and MRTD were measured using a dynamometer. Self-report measure of physical function was assessed by the Short Form 36 (SF-36) questionnaire, and physical performance was assessed by the timed stair and step tests.
In the hierarchical regression models, high maximal quadriceps strength and high quadriceps MRTD uniquely covaried with high SF-36 physical function scores after accounting for demographic, anthropometric, and pain measures. For the timed stair test, all else being equal, in 2 participants with low but identical levels of quadriceps strength, the one with a higher MRTD had better stair-climbing function. For the step test, quadriceps MRTD was not associated with step test performance over and above that of quadriceps strength.
In individuals with hip OA, maximal quadriceps strength and quadriceps MRTD positively impact self-report and physical performance measures of physical function. These findings are of importance in developing intervention strategies, but they call for further study.
Osteoarthritis (OA) of the hip is a major contributor to physical function limitations in older adults (1). Specifically, hip OA, along with knee OA, affects the ability to walk and climb stairs more than any other diseases (2). Furthermore, compared with individuals with healthy hips, those with hip OA have lower quadriceps strength (3, 4), and available studies have shown that quadriceps strength is an important correlate of physical function (5, 6).
Common to all of the studies cited above was the measurement of quadriceps strength, which is the capacity of the quadriceps to produce torque. Nonetheless, quadriceps strength represents just one aspect of muscle performance; another aspect relates to the capacity of the quadriceps to develop torque rapidly in the initial phase of muscle contraction: the maximal rate of torque development (MRTD) (7). Ostensibly, the ability to rapidly generate muscular torque is important not only during time-critical events (7), e.g., recovering one's balance from a trip, but also during many tasks of daily living, e.g., stair climbing, where dynamic joint stability (8) is required. Furthermore, one recent study (9) showed that individuals with unilateral hip OA had lower quadriceps MRTD on the involved side than on their own uninvolved sides, and this finding appears to be explained by emerging pathophysiologic evidence that hip OA is associated with 1) muscle atrophy (4, 9–13), preferentially affecting the type II fibers (10–13); 2) reduced muscle density (9, 14), presumably caused by muscle infiltration with connective tissues and adipocytes (15); and 3) a decline in muscle activation during the early phase of muscle contractions (9).
Although considerable pathophysiologic evidence (4, 9–15) implicates the decline in quadriceps MRTD as a hip OA–related impairment, only one study to date has examined the relationship between quadriceps MRTD and physical function. Specifically, Suetta et al (16) parenthetically reported that quadriceps MRTD was associated with gait speed, but this conclusion was limited on 2 counts. First, the authors studied only 13 patients who subsequently underwent total hip arthroplasty, and the generalizability of their findings to individuals with less severe hip OA is uncertain. Second, Suetta et al (16) examined only gait speed, and it remains unknown whether their findings hold true for other measures of physical function.
To the extent that quadriceps strength and MRTD represent conceptually distinct aspects of muscle performance, we believe it is important to examine their associations with physical function which, in turn, could potentially lead to the development of new management strategies for individuals with hip OA. For this reason, we initiated this study to extend previous findings, enrolling a larger number of participants with hip OA and employing multivariable approaches to quantify the independent impact of quadriceps strength and quadriceps MRTD on both self-report and physical performance measures of physical function.
PARTICIPANTS AND METHODS
This study forms part of a series of experiments to investigate the correlates of physical function in persons with hip OA. The study sample comprised community-dwelling adults living in Victoria, Australia. All participants were volunteers who had responded to advertisements in local papers. Participants were recruited if they had radiographic hip OA as confirmed by a radiologist, and had hip or groin pain on most days of the past month (17). Exclusion criteria included significant back or other joint pain; secondary hip OA due to trauma, inflammatory, or metabolic rheumatic diseases; lower extremity joint replacement; inability to understand English; and the presence of any medical conditions that would compromise physical function. This research was carried out with approval from the Radiation Safety Section at the Department of Human Services and the Human Research Ethics Committee at the University of Melbourne.
A total of 100 eligible participants participated in this research study. However, 7 participants did not have MRTD values due to unavailability of equipment and 1 participant declined the MRTD test; these 8 participants did not differ significantly from those with complete data in levels of quadriceps strength and physical function. We chose not to impute missing values primarily because the residualized MRTD (MRTDresid) variable was partially derived from the quadriceps strength results; therefore, we included participants in this study for whom MRTD data were complete (92 of 100).
Participants attended a test session at our facility after obtaining informed consent. Prior to the physical performance assessment, participants' height, waist circumference, and body mass were obtained. Waist circumference was taken midway between the inferior margin of the last rib and the crest of the ilium in a horizontal plane. Each participant also completed a set of questionnaires, with physical activity measured using the Physical Activity Scale for the Elderly (PASE) (18) and pain and physical function measured using the Short Form 36 (SF-36) general health survey (19).
Physical Activity Scale for the Elderly.
The PASE is a 12-item self-report questionnaire that inquires about the frequency of the participants' recreational and occupational physical activities undertaken over the previous 7 days (18). Total PASE scores range from 0 to >400, where higher scores indicate higher activity levels. For the PASE, previous studies have demonstrated its strong convergent validity and good test–retest reliability in older adults (18, 20).
Short Form 36.
The SF-36 (19) is a generic questionnaire designed to measure health-related quality of life in general and specific populations (21). The SF-36 comprises 36 items related to 8 subscales of health, of which we used the bodily pain and physical function subscales. Each subscale ranges from 0–100, with higher scores representing better health states. In this study, we used the Australian SF-36 version 2 (22), which directs participants to consider the previous 4 weeks for the bodily pain subscale; however, items in the physical function subscale indicate the present time.
Physical performance measures.
Participants had their symptomatic hips, or the more painful hip in the case of bilateral symptoms, tested. Participants were tested in the following order: step test, timed stair test, and quadriceps performance tests. Participants were provided with rest periods as requested.
Dynamic standing balance was assessed using the step test (23). Participants stood barefoot on the tested extremity 5 cm from a 15-cm step, and they were instructed to step the contralateral foot on and off the step as many times as possible over 15 seconds. The number of complete step repetitions was recorded, with higher scores indicating better balance. Although no empirical work has used the step test on individuals with hip OA, we have previously established its known group validity in 66 individuals with and without symptomatic knee OA (24).
Timed stair test.
Stair-climbing ability was assessed by the time taken to climb up and down 6 standardized stairs (step height 18 cm, step depth 30 cm). Handrails were on the right side of the stairs, and participants held them loosely for safety if necessary. During the test, participants were instructed to ascend and descend the stairs in their usual manner. No practice trial was given for this test. In the present study, timed stair measurements showed excellent reliability over a 1-week test–retest interval (n = 9; intraclass correlation coefficient [ICC2,1] 0.84, standard error of measurement [SEM] 0.53 seconds).
Maximal volitional isometric contraction of the quadriceps at 60° of knee flexion was obtained on a KinCom 125-AP isokinetic dynamometer (Chattecx, Chattanooga, TN). The participant was tested in a seated position with the hip at 90° of flexion, and strapping was placed across the waist and chest to stabilize the torso. The axis of rotation of the dynamometer lever arm was aligned with the femoral lateral condyle, and the lever arm was secured to the tibia just proximal to the medial malleolus via an ankle cuff. Before testing the knee extensors, the gravity compensation procedure was performed by measuring the participant's passive extremity weight at 30° of knee flexion. To measure torque, the distance from the ankle cuff to the dynamometer rotation axis was recorded as the lever arm length. The lever arm length (in meters [m]) was multiplied by the highest contraction force (in newtons [N]) to obtain muscle-generated torque (N × m). Following a warm-up comprising 1 submaximal and 1 maximal contraction, all participants performed 2 maximal trials for 5 seconds with a 1-minute rest interval. The higher measurement of 2 valid trials was analyzed. In the present study, stair measurements showed excellent reliability over a 1-week test–retest interval (n = 19; ICC2,1 0.93, SEM 8 N × m).
Participants were positioned as per the quadriceps strength test. Without any preceding countermovement and in response to an acoustic signal, participants were instructed to extend their knee as fast and forcefully as possible for at least 2 seconds. Two submaximal practice trials and 3 test trials with a 1-minute rest interval were performed. During testing, strong verbal encouragement was given and visual feedback was provided using a real-time display of the force time curves on a computer screen.
Dynamometer force signals were sampled at 1 kHz using a Micro 1401 Mk. II data acquisition system with Spike 2 software, version 5 (Cambridge Electronic Design, Cambridge, UK), and then uploaded into Microsoft Excel (Microsoft, Redmond, WA). Quadriceps force signals were multiplied by lever arm length to calculate torque, and MRTD was the maximum first derivative of the torque time curve, determined over overlapping 30-msec moving windows. Although other variants of isometric rapid muscle performance exist, e.g., torque time integrals over different time periods (7, 25), varying compliance of the shin force transducer interface between participants can introduce additional variability in these measurements (26). Furthermore, we chose MRTD because it 1) avoids the arbitrariness associated with determining torque onset, and 2) is sensitive to the effects of aging (27–31), hip OA (9), and muscle training (7, 16, 32). In the present study, MRTD measurements showed fair reliability over a 1-week test–retest interval (n = 19; ICC2,1 0.63, SEM 237 N × m/second).
The dependent variables step test, stair-climb time, and SF-36 physical function scores were examined as continuous variables, given their normal distributions. Because the distribution of the PASE was positively skewed, its scores were log-transformed before analyses. Given the available sample size, we determined a priori 5 potential covariates, specifically sex, age, waist circumference, self-reported physical activity, and pain levels, on the basis of previously reported associations with physical function or plausible prior hypotheses. We did not include in our analyses body mass and body mass index because they were highly correlated with waist circumference (r = 0.85 and 0.87, respectively) and would have led to adverse multicollinearity effects. Pearson's and point biserial correlations described the bivariable relationships between all variables. Because quadriceps strength correlated highly with MRTD (r = 0.83), the MRTDresid variable was created to reduce the potential problem of multicollinearity. Specifically, MRTD was regressed on quadriceps strength and the residuals were saved to produce MRTDresid; therefore, each MRTDresid value represented the extent to which the actual MRTD value exceeded or fell below what would be predicted from quadriceps strength.
Separate hierarchical models were used to determine whether quadriceps performance was associated with the 3 physical function measures. In step 1, we entered age, sex, physical activity level (assessed by the PASE), pain level (assessed by the SF-36 bodily pain subscale), and waist circumference. In step 2, we entered the 2 measures of quadriceps performance, quadriceps strength and MRTDresid. Because previous literature (33–38) and partial scatterplots suggested a potential nonlinear association between quadriceps strength and physical function, we entered the quadratic (squared) term of quadriceps strength in step 3. The sequential process of hierarchical regression examined the change in explained variation by the variables entered in each step; therefore, a significant quadratic component would indicate a nonlinear aspect of the relationship between strength and function. Finally, possible effect modifications of the relationship between MRTDresid and physical function by quadriceps strength were examined by entering MRTDresid × strength in step 4. To elucidate the form of a significant interactive effect, we repeated the regression analyses to assess the relationship between MRTDresid and function when the quadriceps strength level was high (1 SD above its mean) and low (1 SD below its mean), respectively.
Goodness-of-fit was evaluated by testing the residuals for normality and homoscedasticity, and examining partial regression residual plots for all variables. For all analyses, P values less than 0.05 (2-tailed) were considered to be significant.
Table 1 shows the participants' descriptive characteristics, whereas Table 2 provides the descriptive statistics for the self-report and physical measures. Among the participants, there was a 3.1–9.5-fold range in their SF-36 physical function scores, step test repetitions, and stair-climb time. One participant was unable to perform the timed stair test, and this participant was excluded from the analyses involving the stair variable. Table 3 shows the correlation coefficients between the measures used in this study. Quadriceps strength and MRTD correlated with all measures of physical function. As expected, no correlation existed between quadriceps strength and MRTDresid, indicating that both variables can exert their own effects in the hierarchical models without mutual influence.
Table 2. Self-report and physical performance measures*
Mean ± SD
PASE = Physical Activity Scale for the Elderly; N = newtons; m = meters; MRTD = maximal rate of torque development; MRTDresid = residualized MRTD; SF-36 = Medical Outcomes Study 36-Item Short Form Health Survey.
169 ± 80
Isometric strength, N × m
139 ± 52
MRTD, N × m − 103/second
1.55 ± 0.67
MRTDresid, N × m − 103/ second
0 ± 0.38
Timed stair test, seconds (n = 91)
9.8 ± 2.5
17 ± 3.7
54.8 ± 19
54.2 ± 21
Table 3. Correlation matrix for age, sex, PASE, SF-36 bodily pain and physical function, waist circumference, quadriceps strength, quadriceps MRTD and MRTDresid, stair-climb test, and step test*
Sex (1 = men, 2 = women); PASE = Physical Activity Scale for the Elderly; SF-36 = Medical Outcomes Study 36-Item Short Form Health Survey; MRTD = maximal rate of torque development; MRTDresid = residualized MRTD.
Tables 4 and 5 show the hierarchical models for the self-report and physical performance measures of physical function, respectively. The combinations of age, sex, physical activity, pain level, waist circumference, and quadriceps performance explained between 42% and 55% of the variation in physical function. In all models, only waist circumference was consistently associated with physical function. For quadriceps strength, when second-order polynomial curves were fitted, a trend toward a nonlinear effect was observed for the step and stair-climb tests, with the improvement in model fit approaching significance (model 3 ΔR2 = 0.03, P = 0.06 and ΔR2 = 0.02, P = 0.05, respectively) (Table 5).
Table 4. Hierarchical regression analysis for variables predicting SF-36 physical function (dependent variable)*
Values are the unstandardized regression coefficient b (SE) unless otherwise indicated. Sex (1 = men, 2 = women); SF-36 = Medical Outcomes Study 36-Item Short Form Health Survey; PASE = Physical Activity Scale for the Elderly; MRTDresid = residualized maximal rate of torque development.
Table 5. Hierarchical regression analysis for variables predicting stair-climb test and step test (dependent variables)*
Values are the unstandardized regression coefficient b (SE) unless otherwise indicated. Sex (1 = men, 2 = women); PASE = Physical Activity Scale for the Elderly; SF-36= Medical Outcomes Study 36-Item Short Form Health Survey; MRTDresid = residualized maximal rate of torque development.
For SF-36 physical function, the results (Table 4) revealed statistically significant main (additive) effects for quadriceps strength and MRTDresid (b = 0.19, P < 0.01 and b = 0.01, P < 0.05, respectively). The first-order interaction between quadriceps strength and MRTDresid was not statistically significant. In contrast to the analysis of SF-36 physical function, no main effects for MRTDresid were evident for the stair and step tests; however, there was an MRTDresid × strength interaction for the stair test: the magnitude of association of MRTDresid with stair time increased (i.e., became more negative) as quadriceps strength decreased (b = −0.39 × 10−4; P < 0.001) (Table 5). Figure 1 depicts the interactive effect by showing the relationship between MRTDresid and stair time for 2 levels of quadriceps strength: high (1 SD above the mean) and low (1 SD below the mean).
The purpose of this study was to assess cross-sectional associations of self-report and physical performance measures of physical function with quadriceps performance in individuals with symptomatic hip OA. At the simplest, our results are consistent with those from all but a few reports suggesting that quadriceps strength is an important correlate of physical function in hip OA (5, 6). In contrast to these studies, our results further showed that MRTDresid measures covaried with SF-36 physical function measures and stair-climbing performance above and beyond maximal quadriceps strength and demographic, anthropometric, and pain measures.
Before a discussion of the results, the theoretical construct of MRTDresid deserves consideration. Although maximal quadriceps strength and MRTD are often described as distinct characteristics of quadriceps performance, several studies (29, 39), including our own (Table 3), are consistent in showing a close association between the 2 variables. In this context, our analytic approach in creating MRTDresid scores is defensible both mathematically and conceptually: this approach not only removes the intercorrelation of variables, but it also produces a quadriceps strength measure independent of rapid muscle function. To the extent that several neuromuscular factors, including percentage of muscle fiber area of type II fibers (30, 40–42) and the capacity for fast neural activation (7, 25), correlate closely with strength-independent MRTD and not necessarily with maximal quadriceps strength, we believe the use of MRTDresid (together with quadriceps strength) permits a more comprehensive and clearer examination of quadriceps performance with physical function than would have occurred if the raw MRTD had been used.
Turning to our multivariable results, quadriceps strength and MRTDresid were linearly and independently associated with SF-36 physical function. In contrast, for the stair-climbing test, not only was a nonlinear trend observed with quadriceps strength, but a significant quadriceps strength × MRTDresid interaction was also observed. These latter observations are, however, not surprising, because the concept of functional threshold (35) provides a unifying explanation. Specifically, the concept suggests a nonlinear association between muscle strength and physical function (particularly for tasks requiring submaximal strength), such that there is a functional strength threshold below which strength and function are closely related, but beyond which the association between strength and function substantially attenuates or no longer exists. Mechanistically, when maximal quadriceps strength exceeds the functional threshold, it follows that an increase in MRTD or MRTDresid would not appreciably improve stair performance.
Our data showing a relationship between MRTDresid and physical function cannot be directly related to those of Juhakoski et al (43), who reported on 118 individuals with hip OA. Although the authors found that leg extensor power correlated with RAND-36 physical function, leg extensor power was measured in a multi-joint movement, which precluded direct inference about quadriceps performance. Nonetheless, our results agree with those of other previous studies reporting on older adults with and without hip OA. Specifically, Suetta et al (16) found cross-sectional and longitudinal associations between strength-normalized MRTD and gait speed in 13 strength-trained individuals with end-stage hip OA (r = 0.55 and 0.86, respectively), whereas 2 small cross-sectional studies (n = 13 and 17, respectively) (28, 29) reported positive correlations between absolute or body mass–adjusted isometric quadriceps MRTD and jump height in older adults with healthy hips. Whereas previous studies (16, 28, 29) were limited by small sample sizes, mandating the use of bivariable models, our study extends them by enrolling a larger sample of adults with a wider range of OA severity, and by examining other types of physical function, specifically stair-climbing performance and SF-36 physical functioning.
In contrast to our results, Seynnes et al (44) reported on 19 older women and found no association between quadriceps RTD and stair-climbing power (calculated from body mass, total stair height, and stair ascent time). Although the discrepant results may be explained by differences in sample sizes or study samples, differences in measurements could also be responsible. Specifically, Seynnes et al (44) measured quadriceps RTD from torque onset to the first plateau on the torque time curve, and it remains unclear, although unlikely, whether this measurement captures the very initial phase of torque development. In contrast, our MRTD, as also reported by others (27, 30), occurred early in the torque time curve, i.e., before 50% of maximal torque was reached. Given that strength-normalized RTD obtained in the early phase of torque development is more sensitive to the effects of aging (27, 30) and neuromuscular training (7, 8, 16, 32) than are measures obtained over longer phases, it may be anticipated that the former would correlate more closely with physical function measures.
Contrary to the results for the stair-climbing and SF-36 measures, MRTDresid did not covary with step test performance (Table 5, model 2). Because MRTDresid represents the increase or decrease in MRTD relative to those predicted by quadriceps strength, and thus are not the actual MRTD values, our multivariable results should be interpreted cautiously, as suggesting that MRTD did not wield an influence on step test over and above that of quadriceps strength. Furthermore, at the bivariable level (Table 3), essentially identical correlations were observed for quadriceps MRTD and quadriceps strength with the step test (r = −0.38 for both), indicating that both variables have similar explanatory power.
As such, our results do not necessarily disagree with those of Pijnappels et al (29), who found that quadriceps strength and body mass–adjusted MRTD were equally discriminating in identifying elderly patients at risk of falling. Furthermore, they are consistent with those of Bellew (45), who showed no association between strength-adjusted RTD and standing postural sway measures in 27 older adults. Nevertheless, the question remains: how do we explain the null finding with MRTDresid? One possibility is that because the step test requires no intense or rapid movements of the involved knee, its movement demand may be insufficient for MRTDresid to wield an effect. For example, our significant findings for MRTDresid with SF-36 physical function and stair-climb tests, physical tasks that impose relatively higher demands on the knee, may be interpreted as supporting our explanation. Furthermore, Izquierdo et al (46) showed that their RTD measures, obtained from a bilateral isometric squat, correlated more closely with computerized posturographic tasks that were more dynamic rather than static in nature. Although their method used to quantify RTD was appreciably different from ours, the results overall suggest that the associations of physical function with MRTD and MRTDresid may be dependent on the movement demand of the physical task.
Our results have implications. First, viewed in the context of the accumulating evidence for the qualitative muscle changes in hip OA, perhaps the most compelling finding of our study is that quadriceps MRTD is an independent correlate of physical function. Thus far, conservative management guidelines for hip OA (47) have emphasized muscle strengthening, and our finding, if replicated, implies that interventions that improve quadriceps MRTD, e.g., neuromuscular training (8) or resistance training comprising a high-velocity component in the repetitions (16), could potentially further enhance physical function. Second, although common in the gerontologic literature (33–38), few or no studies in the OA literature have explored possible nonlinear associations between muscle performance and physical function. Nonetheless, where nonlinear associations exist, our results indicate that a failure to consider quadriceps strength level can mask subgroup-specific associations. In the non-moderated regression model where MRTDresid was assessed against stair-climbing performance across all levels of quadriceps strength, the main effects of MRTDresid were effectively attenuated (Table 5, model 2). Nonlinear quadriceps performance associations with physical function may be more common than previously assumed and future studies should delineate possible strength thresholds below which a significant association between MRTDresid and function occurs.
Our study has limitations. First, our results may be affected by reverse causation due to their cross-sectional nature, i.e., physical function limitations could adversely affect quadriceps performance, and intervention studies are clearly needed to establish the presence and direction of causation. Second, although our study is one of the largest studies thus far conducted of quadriceps MRTD and physical function, the sample size was suboptimal to allow stratified analyses by sex. Third, we cannot rule out the possibility of residual confounding from other unknown factors or from factors for which we have accounted imperfectly. For instance, physical activity level was self-reported; therefore, inaccurate measurements were possible (48), which in turn could undermine associations. Finally, although MRTDresid is reportedly related to the properties of the muscle tendon complex (30, 40–42) and the level of muscle activation (49, 50), our study design does not allow us to disambiguate their relative contributions to physical function. Accordingly, future studies should address this issue to refine our understanding of the association between MRTD and function.
In conclusion, we demonstrated that in adults with symptomatic hip OA, maximal quadriceps strength and MRTD exerted independent influence on SF-36 physical function over and above that of demographic, anthropometric, and pain measures. When adjusted for quadriceps strength, MRTD was neither associated with step test performance nor with stair-climbing performance at high quadriceps strength levels. Because of the cross-sectional nature of our findings, intervention studies are necessary to determine whether improvements in quadriceps MRTD enhance functional status in individuals with hip OA.
Mr. Pua had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.
Study design. Pua, Wrigley, Cowan, Bennell.
Acquisition of data. Pua, Wrigley.
Analysis and interpretation of data. Pua, Wrigley, Cowan, Bennell.