Delayed Onset of Quadriceps Activity and Altered Knee Joint Kinematics During Stair Stepping in Individuals With Knee Osteoarthritis

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1 1080 Delayed Onset of Quadriceps Activity and Altered Knee Joint Kinematics During Stair Stepping in Individuals With Knee Osteoarthritis Rana S. Hinman, BPhysio, Kim L. Bennell, PhD, Ben R. Metcalf, BSci, Kay M. Crossley, BAppSci, GradDip ABSTRACT. Hinman RS, Bennell KL, Metcalf BR, Crossley KM. Delayed onset of quadriceps activity and altered knee joint kinematics during stair stepping in individuals with knee osteoarthritis. Arch Phys Med Rehabil 2002;83: Objective: To determine if the electromyographic onset of vastus lateralis and kinematic knee joint motion in individuals with knee osteoarthritis (OA) differs from that of asymptomatic persons, during the task of stair stepping. Design: Cross-sectional. Setting: University laboratory in Australia. Participants: Twenty-five participants with symptomatic knee OA and 33 asymptomatic controls. Interventions: Not applicable. Main Outcome Measures: Surface electromyography to determine the onset of vastus lateralis activity. Two-dimensional kinematic analysis of sagittal plane knee motion during stance phase of stair ascent and descent. Results: Participants with knee OA showed delayed onset of vastus lateralis activity during stair descent (P.05) but not ascent. Both groups displayed a similar total range of knee motion. However, during stair descent, participants with OA had less knee flexion during early stance (P.05) than controls. Conclusion: Individuals with knee OA display altered quadriceps function and knee joint kinematics during stair descent. These impairments may have implications for force attenuation across the knee joint and warrant future investigation. Key Words: Electromyography; Kinematics; Knee; Osteoarthritis; Rehabilitation by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation OSTEOARTHRITIS (OA) IS A COMMON, chronic joint disease characterized by pain, disability, and progressive loss of function. It is the most common musculoskeletal complaint worldwide and is associated with significant health and welfare costs. 1-3 The knee is the most frequently affected joint of the lower limb. Prevalence of knee OA increases with age 4 and thus is a leading cause of disability in the elderly. 5-7 Weight-bearing tasks are among the most difficult for individuals afflicted by knee OA; limitations in stair climbing and ambulation are commonly reported. 6,7 From the Centre for Sports Medicine Research and Education, School of Physiotherapy, University of Melbourne, Australia. Supported by the National Health and Medical Research Council (grant no ). No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. Reprint requests to Rana S. Hinman, Centre for Sports Medicine Research and Education, Schl of Physiotherapy, University of Melbourne, 200 Berkeley St, Carlton, 3010, Australia, r.hinman@pgrad.unimelb.edu.au /02/ $35.00/0 doi: /apmr Precise coordination of quadriceps activity and knee joint motion is essential to attenuate forces and control joint loading during locomotion Preactivation of quadriceps, relative to heel strike, aims to minimize impact shock by decelerating the lower leg and ensuring accurate foot placement on the ground. Controlled knee flexion, often described as loading response knee flexion (LRKF), occurs as weight is loaded onto the limb at heel strike and acts to dissipate the load. This is achieved by eccentric quadriceps contraction. Increased joint loading is associated with OA. 11,12 It has been proposed that impairments in quadriceps function and knee joint kinematics may be important in the pathogenesis and progression of knee OA Motor activity is time dependent. Delayed motor response of the quadriceps and hamstrings has been shown in individuals with other knee pathology. 17,18 Delayed onset of quadriceps activity may increase the force with which the foot hits the ground, exposing the knee to damaging jarring stresses. Knee OA is associated with weakness and arthrogenous inhibition of the quadriceps as well as proprioceptive deficits Additionally, joint effusion, pain, and fatigue, all common manifestations of knee OA, can inhibit the voluntary and reflexive motor output of the quadriceps As a result of these factors, it is possible that knee OA may be associated with delayed activity of the quadriceps, yet this possibility has not been investigated to date. Analysis of knee joint kinematics in the osteoarthritic population has primarily occurred during gait, whereas other ambulatory tasks have received little attention. Indeed, stair ascent and descent, tasks more demanding of the knee joint than level walking, 30 have been investigated in only 1 published study. 31 Altered walking pattern is reported in individuals with knee OA, with a reduction in rate and range of knee motion, gait velocity, and loading of the affected joint most commonly seen Decreased knee flexion during the stance phase of gait is characteristic of the disease and may represent an effort by the individual to reduce compressive forces across the loaded knee to minimize pain. Quadriceps weakness may also be a contributing factor 10 ; if the individual is unable to eccentrically control the range of knee flexion normally used, a reduction in range may be evident. Regardless of the cause, limitation of knee flexion significantly reduces the normal shock absorption action of the joint and leads to increased vertical ground reaction forces. 8,10,36 In summary, individuals with knee OA display altered knee joint kinematics during level walking, and those altered kinematics are associated with increased ground reaction forces and joint loading. Additionally, impairments in quadriceps function associated with the disease suggest that a delay in onset of quadriceps activity may exist, which may further compromise load attenuation across the knee. The purpose of the present study was to identify the onset of quadriceps activity (relative to foot strike) and to evaluate the kinematics of knee joint motion during the provocative activity of stair stepping in individuals with symptomatic knee OA and to compare those

2 ALTERED VASTUS LATERALIS ONSET AND KNEE MOTION IN OA, Hinman 1081 findings with the same data obtained from an asymptomatic group. METHODS Participants Twenty-five participants (14 men, 11 women) with knee OA and 33 asymptomatic controls (17 men, 16 women) over the age of 50 years were recruited by advertisements in local clubs, libraries, and the print and radio media. Diagnosis of OA was confirmed by a rheumatologist and was based on the American College of Rheumatology clinical and radiologic classification criteria. 37 Participants with OA were included if they had knee pain on most days of the previous month (average level, 3cm on a 10-cm visual analog scale [VAS]), showed osteophytes on radiograph, and experienced pain and/or difficulty on getting up from sitting or climbing stairs. All participants were independent in activities of daily living and had a stable intake of nonsteroidal anti-inflammatory drugs over the previous fortnight. Exclusion criteria included physiotherapy treatment for the knee (previous 12mo), knee surgery (previous 3mo), past history of lower-limb joint replacement, Synvisc (hyaluronate) or intraarticular steroid injection (previous 6mo), systemic arthritic condition, or severe medical condition precluding safe testing. Control participants were excluded if they reported any history of lower-limb pathology or joint disorder, injury to or pain in either knee in the past year (for which treatment was sought, or that interfered with function), or displayed abnormality on physical examination of the knee (flexion range of motion [ROM] 125, effusion, palpable warmth, ligamentous laxity). Because of ethical constraints, radiographs to exclude radiographic OA were not performed. The study was approved by the University of Melbourne Human Research Ethics Committee. All participants provided written informed consent. Procedure The affected limb (or most symptomatic in case of bilateral symptoms) of the OA group was tested; in controls, the left or right limb was randomly tested. Height and weight were obtained barefoot, and body mass index (BMI) calculated. Knee radiographs. Participants with OA had radiographs (skyline, weight-bearing anteroposterior and lateral) of the tested knee within the previous 12 months. Severity of OA was graded by a radiologist according to the Kellgren and Lawrence system. 38 Evaluation of each joint compartment (medial and lateral tibiofemoral, patellofemoral) was performed with regard to presence of joint space narrowing, osteophyte, subchondral sclerosis, attrition of articular surfaces, and subchondral cysts. Knee pain and disability. The Western Ontario and Mc- Master Universities Osteoarthritis Index (WOMAC) was used to evaluate knee pain and disability in the OA group. 39 A 10-cm horizontal VAS, 40 marked in 1-cm increments, was used to record average pain (on movement and at rest), activity restriction over the previous week, and severity of pain experienced during testing. We used the Human Activity Profile 41 (HAP) to measure physical activity patterns in both groups. Electromyographic recordings. Surface electromyographic activity of vastus lateralis was recorded. Previous investigations of knee muscular activity magnitudes during stair climbing have revealed that the vastus lateralis is the predominant force producer (and the most active) of the 4 components of the quadriceps during this task, 30,42 thus the onset of this muscle s activity was deemed most important. After skin preparation, Fig 1. Apparatus set-up, and electrode and marker placement for testing; participant is performing stair descent. Ag/AgCl electrodes a were placed over the muscle belly using the easily identifiable patella, as recommended by Basmajian and Blumenstein, 43 as a reference point (10cm superior and 6 8cm lateral to the superior border of the patella, and orientated 15 to the vertical 44 with an interelectrode distance of 22mm). The ground electrode was placed over the tibial tubercle. Figure 1 shows the electrode placement on a participant s leg. The stair apparatus consisted of a 64-cm platform with 2 steps 15-cm high and 32-cm deep on each side. A handrail ran along the length of 1 side. Participants stood 2m from the lower step apparatus and performed stair ascent and descent at a self-selected speed. Initially, attempts were made to control speed using a metronome, but this proved impossible in this population. At least 3 practice trials ensured familiarity with the procedure. Participants wore comfortable walking shoes and were permitted to use the handrail for support, if necessary. Electromyographic activity was recorded during stance phase on the middle step during ascent and descent, for 5 consecutive trials. Electromyographic data were telemetered, b band-pass filtered between 20 and 500Hz, sampled at 1000Hz, and 12-bit analog-to-digital converted. Data were full-wave rectified and low-pass filtered at 50Hz. A computer algorithm identified onset of activity at the point at which the electromyographic signal deviated by more than 3 standard deviations (SDs), for a minimum of 25ms above baseline (averaged over the 200ms preceding commencement of the trial). The rectified unfiltered electromyographic data were visually checked to verify the electromyographic onsets identified by the computer. The sampling rate allowed a resolution of 1ms. Before analysis, 100 traces were randomly selected, and several algorithms were compared with visually identified electromyographic onsets. The 25ms 3 SD combination was found to deviate least from the visually identified onset of muscle activity and thus to be the most accurate (r 1, intercept 2.25, P.001). Intratester reliability of visual determination of electromyographic onset was established by repeat analysis of data 1 week later. The mean SD of the difference was ms, indicating a high level of accuracy.

3 1082 ALTERED VASTUS LATERALIS ONSET AND KNEE MOTION IN OA, Hinman tested using the Spearman coefficient. In all subjects, associations between muscle onset and kinematic variables were also determined. To ensure that all data were comparable, participants unable to ascend and descend stairs by the step-over-step method were excluded. Three members of the OA group were excluded from analysis of stair ascent and 4 from stair descent. No controls were excluded. Fig 2. Knee joint kinematics during stance phase of stair ascent and descent. Legend: a, total stance knee ROM (e d); b, early stance knee ROM (c d); c, peak loading response knee flexion (KF) angle; d, knee angle at foot strike; e, knee angle at toe-off. Muscle activity onset (electromyographic onset) was identified from individual trials and was quantified by subtracting it from foot strike onset. Onset of foot strike was determined by visual analysis of videotape. A synchronization pulse, common to both electromyography and video acquisition systems, allowed temporal comparison of the 2 measures. Results were averaged for 5 trials of stair ascent and descent. Kinematic analysis. Sagittal plane knee joint movement was measured using a Peak movement analysis system. c Reflective skin markers c were placed over the lateral malleolus, neck of fibula, iliotibial band (at superior border of the patella), and lateral thigh (junction of proximal one third and distal two thirds of a line joining the greater trochanter to the lateral knee joint line). 45 Figure 1 shows the marker placement on a participant s leg. Movement data of stance phase (initial foot strike to toe-off) during ascent and descent were recorded by a single camera d and digitized at a frequency of 50Hz. The obtained raw data, representing the spatial location of the 4 reference markers, were then filtered using a robust nonlinear leastsquares fourth-order (Butterworth) filter. c Three angular variables were of interest (fig 2): (1) peak LRKF (maximal flexion obtained after initial reduction after foot strike); (2) total stance knee ROM (calculated by subtracting knee angle at foot strike from that at toe-off); and (3) early stance knee ROM (calculated by subtracting knee angle at foot strike from that of peak LRKF). Temporal variables of interest were (1) duration of stance phase, (2) time to peak LRKF (expressed as a percentage of total stance phase), and (3) time to complete stair ascent and descent (initial contact of first step to toe-off of second step). Results were averaged over 5 trials of stair ascent and descent. Statistical Analysis Data were analyzed using the Statistical Package for the Social Sciences. e A univariate analysis of covariance compared differences between groups for each variable measured. Because speed of stair ascent and descent differed significantly between groups (and influences kinematic parameters of gait 10,32,35 ), it was controlled for statistically by inclusion as a covariate during analyses. Values of P less than.05 were regarded as statistically significant. In the OA group, associations between pain, disability, and the measured variables were RESULTS Participant characteristics are presented in table 1. Groups were similar in age, weight, height, and BMI (P.05). According to the HAP, groups were doing similar maximal levels of activity (P.05), but OA participants had ceased a greater number of activities (P.001). Gender distribution was comparable across groups, with the OA group comprising 56% men and the control group 52%. Of the OA group, 68% reported bilateral symptoms. The dominant leg (the leg used to kick a ball) was tested in 40% of participants in each of the OA and control groups. In the OA group, 88% were graded radiographically as either moderate or severe (grade 3 or 4) and all displayed evidence of patellofemoral as well as tibiofemoral joint OA. Pain and disability characteristics of the OA group are presented in table 2. Pain experienced by OA participants during the testing procedure ranged from 0 to 7cm as measured on a VAS, with a mean of cm. While participants with OA took longer to ascend (table 3) and descend (table 4) the stairs (P.05), this was not accounted for by either pain or disability (r.38, P.08 and r.10, P.66, respectively, during ascent; r.33, P.14 and r.12, P.61, respectively, during descent). Onset of Vastus Lateralis Activity Relative to Foot Strike Mean SD onset of activity of vastus lateralis preceded foot strike in the control group during stair ascent (table 3) and both groups during descent (table 4). A significant delay in onset of vastus lateralis activity (P.05) was seen during stair descent but not ascent in participants with OA when compared with controls (fig 3). In the OA group, participants with more pain during testing displayed a greater delay in onset of muscle activity during stair ascent but not descent (r.42, P.05). Knee Joint Kinematics During Stance Kinematic data from both groups during stair stepping are presented in table 3 (stair ascent) and table 4 (stair descent). Although the OA group displayed greater knee flexion at toe-off during stair ascent and at foot strike during stair descent (P.001), no differences were detected in total stance knee ROM between the groups. No differences were seen in peak Table 1: Presenting Characteristics of Participants Characteristic OA (n 25) Control (n 33) Age (y) Height (m) Weight (kg) BMI (kg/m 2 ) HAP MCA NII * NOTE. Values are mean SD. Abbreviations: MCA, maximal current activity (defined as the highest activity marked as still doing); NII, normative impairment index (obtained by subtracting from the MCA the number of activities marked as stopped doing). * P.05.

4 ALTERED VASTUS LATERALIS ONSET AND KNEE MOTION IN OA, Hinman 1083 Table 2: Pain and Disability Characteristics of OA Participants Characteristic Mean SD Range Duration of symptoms (y) Average pain on movement in last week (VAS) (cm) Average pain at rest in last week (VAS) (cm) Average restriction of activity in last week (VAS) (cm) Severity of pain in last 48 hours (WOMAC max score, 20) Severity of difficulty with physical functioning in last 48 hours (WOMAC max score, 68) LRKF between groups. However, participants with OA used less knee flexion from foot strike to peak LRKF (early stance knee ROM) during stair descent (P.012). No differences were detected between groups during stair ascent. Peak LRKF occurred at a similar stage of the stance phase in both groups during ascent and descent. In the OA group during descent, participants with more pain at rest over the previous week (r.46, P.05) and greater disability over the previous 48 hours (r.46, P.05) displayed a greater reduction in total stance knee ROM. Those with greater restriction of activity over the previous week (r.55, P.05) and disability over the previous 48 hours (r.50, P.05) displayed a greater reduction in early stance knee ROM during descent. In all participants, individuals with greater flexion at foot strike during descent showed a greater delay in onset of muscle activity (r.29, P.05). DISCUSSION Stair stepping was chosen because it is a functional, weightbearing task that is difficult and painful for individuals with knee OA. 5,6 Support moment magnitudes are greater in stair stepping than level walking and require greater muscle strength and control. 30 After controlling for their slower walking speed, the present study found that individuals with knee OA had a delayed onset of quadriceps activity during descent and used less knee flexion in early stance. These findings have implications for the pathogenesis, progression, and management of individuals with knee OA. Delayed Onset of Quadriceps Activity During stair descent, participants with knee OA activated their quadriceps significantly later (ie, closer to foot strike) than control subjects. This finding suggests that knee OA is associated with altered temporal control of the quadriceps. In both groups, muscle activity occurred before foot strike, constituting a feed-forward element of motor control. This preactivation may be seen as an anticipatory postural adjustment to ready the motor system for anticipated forces applied across the knee at foot strike. 8,46 Because the present study is the first to investigate onset of quadriceps activity in a population with knee OA, no comparison with other studies is possible. Although a delay in the activation of the quadriceps in individuals with knee OA has been noted, the cross-sectional nature of the present study does not enable us to elucidate mechanisms behind this finding. Several mechanisms may be postulated, however. Knee OA is associated with proprioceptive deficits, an integral component of motor control. Impairment in afferent proprioceptive information to the supraspinal centers may result in slowing of centrally driven quadriceps activity. Quadriceps weakness and arthrogenous inhibition 20,22,23 are associated with knee OA. Weak muscles fatigue more readily, and fatigue is associated with slowing and inhibition of voluntary and reflex motor control. 27,28,47,48 In healthy individuals, fatigue of the quadriceps has been shown to result in delayed onset of activity. 49 In addition, aging is associated with increased muscle reaction time, as well as slowing in voluntary mechanisms of postural control. 50,51 Presence of pain or effusion have also been associated with alterations in temporal patterns of muscle recruitment In the present study, we found a relationship between pain and muscle activity during ascent, in that subjects with greater pain showed a greater delay in quadriceps onset, lending credence to this hypothesis. It is unclear why no statistically significant differences were seen between groups during stair ascent. Both groups naturally descended stairs at a faster rate than that used during ascent. The slower speed of ascent may explain this lack of difference between groups. Neuromuscular activity is time dependent, and Table 3: Unadjusted Electromyographic and Kinematic Data Obtained During Stair Ascent Variable OA (n 22) Control (n 33) Vastus lateralis onset before foot strike (ms) KF at foot strike (deg) Peak LRKF (deg) KF at toe-off (deg) * Total stance knee ROM (deg) Early stance knee ROM (deg) E Time to peak LRKF (% stance phase) Time to complete (s) NOTE. Values are mean SD. Abbreviation: KF, knee flexion. * P.01 (statistically adjusted for speed). P.001. Table 4: Unadjusted Electromyographic and Kinematic Data Obtained During Stair Descent Variable OA (n 21) Control (n 33) Vastus lateralis onset before foot strike (ms) * KF at foot strike (deg) Peak LRKF (deg) KF at toe-off (deg) Total stance knee ROM (deg) Early stance knee ROM (deg) * Time to peak LRKF (% stance phase) Time to complete (s) NOTE. Values are mean SD. * P.05 (statistically adjusted for speed). P.001 (statistically adjusted for speed). P.001.

5 1084 ALTERED VASTUS LATERALIS ONSET AND KNEE MOTION IN OA, Hinman Fig 3. Representative electromyographic data of vastus lateralis activity during stair descent. Note that the onset of vastus lateralis occurs later in the OA participant than in the control (ie, closer to foot strike). the faster speed of stair descent may not have allowed sufficient time for individuals with OA to activate quadriceps appropriately, thus resulting in a delayed onset not seen during ascent. Additionally, the load placed on the knee is less during stair ascent than descent. 56 The quadriceps may be assisted by leaning the trunk forward and by using the hand rail to pull the body upward. It may be that the anticipated load during stair ascent is insufficient to delay onset of quadriceps activity when compared with descent. While the delayed preactivation of the quadriceps may be associated with proprioceptive deficits, altered muscle function, pain, and/or effusion, findings of the present study suggest that individuals with knee OA may have an impaired ability to attenuate impact forces during stair descent. Delayed onset of quadriceps activity may result in insufficient time to adequately retard lower limb descent, leading to increased impact at foot strike. Reduced Knee Flexion in Early Stance But No Difference in Total Stance ROM During stair ascent and descent, individuals with knee OA used a similar range of sagittal knee motion during the stance phase, when compared with controls. The present study is the first to evaluate knee joint kinematics of the stance phase of stair stepping in a population with knee OA. Only 1 published study 31 has analyzed the impact of OA on knee joint kinematics during stair stepping. However, because the authors evaluated only the maximum knee flexion angle obtained during the task, observed during swing phase, comparison between the earlier study and ours is not possible. Previously, investigations of walking have revealed a reduction in total stance knee motion in this population This gait alteration is believed to be a compensatory strategy used to minimize pain. It is likely that the absence of a difference between groups in stair stepping is because of the constraining nature of the task itself. Stair stepping requires greater knee ROM than does level gait 30 ;itis likely that to complete the task, subjects were unable to limit their knee motion to a significant degree. The finding by Kaufman et al 31 of similar maximum knee flexion between patients with OA and controls during stair climbing supports this hypothesis. Despite the similar total stance ROM and peak LRKF seen in both groups, participants with OA used less knee flexion in early stance during stair descent than the controls (11.5 and 16.7 of knee flexion, respectively). Limitation of flexion at this early point of the stance phase is perhaps more critical than limitation of the stance phase as a whole. Perry 10 reported that knee flexion during early stance represents the point of the gait cycle where muscular demands and joint forces are greatest. Eccentric quadriceps action during this phase of gait acts as the primary dynamic shock absorbing mechanism. Individuals with OA may use less knee flexion in early stance for several reasons. A reduction in motor control of the lower limb, or quadriceps weakness, may lead to greater knee flexion at foot strike (12.1 in OA group, 7.7 in controls), thus limiting the range of flexion available for use during early stance. The presence of a mild flexion deformity as a result of the disease process would have similar consequences. There was no correlation between pain and early stance knee ROM in the OA group, but an association did exist between pain and total knee ROM. A correlation was also evident between early stance knee ROM and self-reported disability. Given these associations, and the knowledge that pain is an important determinant of disability in this population, 7,57 it is likely that the finding of reduced early stance knee ROM represents a compensatory strategy used to minimize eccentric quadriceps demand and to reduce compressive forces across the knee. No major differences in knee joint kinematics were detected between groups during stair ascent probably because of the nature of the task. Compressive forces are less than those seen in descent 56 and may not demand compensatory gait adjustments to accommodate impairments associated with joint disease. Additionally, concentric quadriceps activity is required to extend the knee in order to elevate the body from 1 step to the next. This action requires very little knee flexion in early stance, as evidenced by the results of the control group (mean, ), rendering it unlikely that the osteoarthritic process can have much effect on this parameter. The consequences of the kinematic changes evident in this study warrant future investigation. A reduction in knee flexion during early stance diminishes the normal shock absorption mechanism of the knee. 8,36 In a normal population, restricted stance phase knee flexion during gait results in greater vertical ground reaction forces and rates of lower-limb loading. 36 The present investigation did not measure force production across the knee joint; therefore, the relations between the observed kinematic alterations and knee joint forces cannot be evaluated. It is possible that stair descent may be associated with increased joint forces in individuals with OA, but further investigation with forceplate analysis is required to establish any such association. Clinical Implications Findings of the present study have important clinical implications. The impairments in quadriceps activity and knee joint kinematics observed during stair descent in individuals with

6 ALTERED VASTUS LATERALIS ONSET AND KNEE MOTION IN OA, Hinman 1085 knee OA may be associated with alterations in joint loading. Further investigation, directed at evaluating the impact of these findings on joint loading, is required to elucidate the mechanisms behind, and implications of, these impairments. Treatment strategies in this patient population should be directed not only toward improving the strength of the quadriceps, but also toward improving the speed of its motor response. While this strategy may entail specific quadriceps retraining, the enhancement of sensory feedback, including proprioception, should not be neglected. Strategies aimed at increasing knee flexion during the initial stages of loading are warranted and require future investigation in this population. CONCLUSIONS The present investigation provided evidence that temporal quadriceps control and knee joint kinematics are disturbed in individuals with knee OA during stair descent, but not ascent. These findings sustain a growing belief among health professionals that impairments in motor control and joint motion have important associations with knee OA. Our results suggest that knee OA may be associated with an alteration in force production across the knee during stair descent. Future investigation is warranted to determine the effect of these changes on joint loading. Acknowledgments: We thank Professor Rachelle Buchbinder and Dr. Joylene Rentsch for their assistance in screening study participants, Dr. Mike Smith for assistance with radiographic evaluations, and Sallie Cowan and Dr. Trevor Allen for their technical and scientific assistance. References 1. Gabriel SE, Crowson CS, Campion ME, O Fallon WM. Indirect and non-medical costs among people with rheumatoid arthritis and osteoarthritis compared with non-arthritic controls. J Rheumatol 1997;24: Jacobsson L, Lindgärde F, Manthorpe R. 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