Early Osteoarthritis of the Trapeziometacarpal Joint Is Not Associated With Joint Instability During Typical Isometric Loading Eni Halilaj,1 Douglas C. Moore,2 Tarpit K. Patel,2 Amy L. Ladd,3 Arnold-Peter C. Weiss,2 Joseph J. Crisco1,2 1 Center for Biomedical Engineering and School of Engineering, Brown University, Providence, Rhode Island 02912, 2Department of Orthopaedics, The Warren Alpert Medical School of Brown University and Rhode Island Hospital, Providence, Rhode Island 02903, 3Department of Orthopaedic Surgery, Robert A. Chase Hand & Upper Limb Center, Stanford School of Medicine, Stanford, California 94304

Received 11 November 2014; accepted 27 April 2015 Published online 12 June 2015 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/jor.22936

ABSTRACT: The saddle-shaped trapeziometacarpal (TMC) joint contributes importantly to the function of the human thumb. A balance between mobility and stability is essential in this joint, which experiences high loads and is prone to osteoarthritis (OA). Since instability is considered a risk factor for TMC OA, we assessed TMC joint instability during the execution of three isometric functional tasks (key pinch, jar grasp, and jar twist) in 76 patients with early TMC OA and 44 asymptomatic controls. Computed tomography images were acquired while subjects held their hands relaxed and while they applied 80% of their maximum effort for each task. Six degree-of-freedom rigid body kinematics of the metacarpal with respect to the trapezium from the unloaded to the loaded task positions were computed in terms of a TMC joint coordinate system. Joint instability was expressed as a function of the metacarpal translation and the applied force. We found that the TMC joint was more unstable during a key pinch task than during a jar grasp or a jar twist task. Sex, age, and early OA did not have an effect on TMC joint instability, suggesting that instability during these three tasks is not a predisposing factor in TMC OA. © 2015 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. J Orthop Res 33:1639–1645, 2015. Keywords: thumb carpometacarpal joint; joint instability; computed tomography; in vivo kinematics

Humans have a unique opposable thumb that exemplifies the necessity for balance between mobility and stability. Power grasping and precision handling maneuvers, which are required for the execution of most daily tasks, represent the diverse span of skillful manipulation that is associated with this digit.1 Much of the versatility of the thumb is due to the wide range of motion capability of the trapeziometacarpal (TMC) joint,2–4 as motions of the metacarpophalangeal (MCP) and the interphalangeal (IP) joints are largely restricted to flexion-extension—although a slight degree of abduction-adduction laxity exists in the former during a limited portion of its arc of motion.5–7 A saddleshaped articulation with six-degree-of-freedom capacity, the TMC joint also requires stability for adequate distribution of loads throughout the range of motion. Stability is often challenged in an anatomical joint that favors mobility and experiences high loads. Previous studies have shown that the loads applied at the tip of the thumb are amplified by up to 1200% at the TMC joint.8 If adequate support from soft tissue is lacking, the combination of high loads, high mobility, and incongruent surfaces9 can result in instability and high contact stresses, which in turn are known to negatively affect cartilage health and mediate osteoarthritis (OA).10–12 Several studies have demonstrated that limiting thumb motion with bracing and improv-

Conflict of interest: None. Grant sponsor: National Institute of Arthritis and Musculoskeletal; Grant number: AR059185. Grant sponsor: Skin Diseases of the National Institutes of Health; Grant number: AR059185. Correspondence to: Joseph J. Crisco (T: 401-444-4231; F: 401-4444418; E-mail: [email protected]) # 2015 Orthopaedic Research Society. Published by Wiley Periodicals, Inc.

ing dynamic stability through muscle exercise can reduce pain in the arthritic joint.13–16 These findings point to joint instability as a potential mediator of pathology. TMC OA is associated with hypermobility and idiopathic joint subluxation in the dorsal-radial direction (Fig. 1),17–23 which are believed to render the joint unstable, but instability in the active TMC joint has not been assessed. Women, who are more susceptible to TMC OA, generally score higher on generalized hypermobility tests24 and have a greater range of TMC motion than men.25 It is not known, however, if generalized joint hypermobility and TMC joint subluxation are concomitant with other systemic factors that contribute more directly to cartilage degradation and further joint destabilization, or if hypermobility plays a leading role in destabilizing the joint by creating suboptimal loading conditions and triggering a series of abnormal biological processes. The existing body of literature17–22 draws causal conclusions based on correlations between generalized hypermobility and TMC OA, or radiographic evidence of joint subluxation and TMC OA, but does not address the missing link between them—joint instability during loading. The aim of this study was to determine if populations that are more prone to TMC OA have greater joint instability during the execution of three highdemand functional tasks. TMC joint instability is defined here as a measure of compliance, i.e., the translation of the metacarpal over the trapezium for a given applied load. Since the female sex and OA onset are hypothesized to be associated with greater TMC joint instability, and age is a risk factor for TMC OA,26 we specifically sought to determine whether joint instability differed as a function of sex, age, and early OA. We hypothesized that during the execution of JOURNAL OF ORTHOPAEDIC RESEARCH NOVEMBER 2015

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Figure 1. Trapeziometacarpal (TMC) joint subluxation. Plain film X-ray illustrating dorsal subluxation in the TMC joint, which is associated with TMC OA.

these tasks joint instability would be significantly higher in women than in men, in older subjects than in younger subjects, and in arthritic patients than in age-matched controls.

METHODS Subjects Following approval from our institutional review board, 76 subjects with early stage TMC OA (31 men and 45 women) and 44 asymptomatic subjects (10 young men, 11 young women, 10 middle-aged men, and 13 middle-aged women) were recruited as part of a longitudinal study on TMC OA bimechanics27–31 (Table 1). Every subject was screened prior to enrollment to rule out any pre-existing conditions that are known to influence joint morphology or kinematics, such as traumatic injury, hand or thumb surgery, inflammatory arthritis, metabolic bone disease, etc. Radiographic (X-ray) examination for each subject included posterior-anterior and lateral views of the thumb, Robert’s view of the thumb,32,33 and a stress view of both thumbs simultaneously. The arthritic subjects were staged according to a modified Eaton staging system19 and only subjects who presented with pain at the base of the thumb and little or no radiographic evidence of TMC OA were included. Beighton scores for generalized joint laxity34 were collected for both the early OA subjects and the healthy controls. JOURNAL OF ORTHOPAEDIC RESEARCH NOVEMBER 2015

Data Acquisition The wrists and thumbs on the affected hands of the arthritic subjects and the dominant hands of the asymptomatic subjects were CT-scanned (GE LightSpeed 16, General Electric, Milwaukee, WI) in a splinted neutral position and during the execution of three functional tasks: lateral key pinch, jar grasp, and jar twist, at a resolution of 0.4 mm  0.4 mm  0.625 mm. The mean total effective dose of radiation to each study participant for these seven scans was approximately 0.35 mSv,35 equivalent to approximately 20 days of background radiation in the United States.36 Positioning of the wrist and thumb during the scans was standardized across subjects using a modified thumb spica brace (Rolyan1 Original, Patterson Medical, Bolingbrook, IL) for the neutral position and custom-made mechanical fixtures for the three tasks.28 A compression load cell (0-50lb, Model D, Honeywell International Inc., Morristown, NJ) was integrated into the fixtures and connected to a customwritten LabVIEW (National Instruments, Austin, Texas) data acquisition and display program. The key pinch fixture, which consisted of mating flat and concave polycarbonate platens designed to accept the load cell, was placed between the middle and distal phalanges of the index finger (Fig. 2, Left). The total height of the two platens was 12.3 mm. The jar grasp and jar twist tasks were executed using a polycarbonate cylinder with a diameter of 66 mm. During the jar grasp activity subjects were positioned with their wrist in slight extension, while their thumb pressed on a platen that was placed on the side of the cylinder, to cover the load cell and support the thumb. The platen rendered the total diameter of the fixture 67.5 mm (Fig. 2, Middle). During the jar twist activity subjects placed their hand on top of the cylinder, twisting an adjustable “lid,” which was paired with the load cell, in the direction that caused the wrist to deviate ulnarly (clockwise for the right hand/counter-clockwise for the left hand) (Fig. 2, Right). During the execution of the functional tasks subjects were scanned while they held their hands relaxed in the prescribed positions and while they applied 80% of their maximum pre-recorded effort for each specific task. Visual feedback from the LabVIEW program assisted them in maintaining a constant load. Each scan lasted 30–45s. The recorded load profile during this time was averaged and the average value was used as the applied load (F) during the isometric-loading task. Joint Kinematics and Instability The trapezium and first metacarpal were segmented from the neutral CT volumes using Mimics v.13.1 (Materialise, Leuven, Belgium) and exported as polygon meshes. The positions of the bones in the functional-task scans were determined automatically with a markerless bone registration algorithm.37 Motion of the metacarpal with respect to the trapezium from the unloaded to the loaded position of a given task was computed using metacarpal and trapezial segment coordinate systems (SCS).27 These SCS’s were aligned with the principal directions of curvature on the trapezial and metacarpal articular surfaces, which are oriented in the ulnar-radial (UR) and dorsal-volar (DV) directions. Metacarpal translation was defined as the displacement of the origin of the metacarpal SCS, which corresponded to the inflection point of the metacarpal articular surface, with respect to the trapezial SCS.27 Only translation in the plane of the articular surfaces was considered, since the proximaldistal component of translation in the TMC joint is typically minimal and not related to joint instability. In the articular

THUMB CARPOMETACARPAL JOINT STABILITY

Table 1. Mean Ages ( SD) of the Subjects in Each Study Group (In Yrs.) Young Healthy Men (n ¼ 10)

Women (n ¼ 11)

Older Healthy Men (n ¼ 10)

Women (n ¼ 13)

Early OA Men (n ¼ 31)

Women (n ¼ 45)

22.5  2.5 23.5  1.4 56.7  9.5 55.4  7.6 61.0  7.6 53.0  6.6

plane, the DV and UR components of translation, along with the magnitude of translation (d), were analyzed. Instability was defined as the ratio of the metacarpal translation to the applied load ðFdÞ. Statistical Analysis The outcome measures were the DV and UR components of metacarpal translation, the magnitude of translation, the applied load, and joint instability for each task, as well as the Beighton score. Correlated error general linear models were used to determine the effects of sex, age, early OA on all of the outcome measures. A cell-means model approach was taken, with all the hypotheses set a priori and carried out as orthogonal linear estimates. Sex group comparisons were made between: (1) healthy young men and women; (2) healthy older men and women; and (3) arthritic men and women. Age group comparisons were made between: (1) healthy young and older men; and (2) healthy young and older women. Health group comparisons were made between: (1) healthy older men and arthritic men; and (2) healthy older women and arthritic women. The Holm test was used to determine statistical significance, which was set at .05, after adjusting for multiplicity. Only the adjusted p values are reported here. Based on inspection of model residuals, a normal distribution was selected for the DV and UR components of translation, while a lognormal distribution was selected for the applied load, magnitude of translation, joint instability, and Beighton score. Results are presented as means and standard deviations (SD) for the normally distributed variables and as geometric means and 95% confidence intervals (CI) for the lognormal variables. Repeated measures analyses of variance, with Dunn’s multiple comparison tests, were used to determine if the applied load, the magnitude of translation, and instability were significantly different among the three tasks.

RESULTS The mean thumb loads applied during key pinch, jar grasp, jar twist activities were 34 N (CI: 31–36 N), 36 N (CI: 32–41 N), and 43 N (CI: 40–47 N), respectively. The

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load applied during the key pinch activity was lower than the loads applied during the jar grasp or jar twist activities (p < 0.001). On average, women applied less load than men, but the differences were statistically significant only in arthritic subjects during the jar twist task (p ¼ 0.040, p > 0.059 for all other sex-group comparisons) (Fig. 3). Age did not have a significant effect on the loads applied in any of the tasks (p > 0.436). On average, arthritic women applied 30% less force than healthy women of the same age group during the jar grasp task (p ¼ 0.006) (Fig. 3). There was a trend toward arthritic men applying less load than healthy men of the same age group, but the difference between the two groups was not statistically significant (p ¼ 0.058). The mean loads applied during key pinch and jar twist tasks were not significantly different between arthritic patients and healthy controls (p > 0.216). The mean magnitudes of metacarpal translation for the key pinch, jar grasp, and jar twist tasks were 1.3 mm (CI: 1.1–1.4 mm), 0.8 mm (CI: 0.7–0.9 mm), and 0.8 mm (CI: 0.6–0.9 mm), respectively (Fig. 4). Translation was significantly larger during the key pinch task than during the jar grasp and jar twist tasks (p < 0.001). Within each task, the magnitude of metacarpal translation was not significantly different among sex, age, and health groups (p > 0.694) (Table 2). There were also no significant differences in the DV and UR components of translation with sex, age, or early OA (p > 0.693) (Tables 3 and 4). Across all the subjects, the metacarpal translated significantly in the volar (VD) direction by a mean ( SD) of 0.9  1.2 mm during key pinch; in the ulnar (UR) direction by a mean ( SD) of 0.7  0.6 mm and in the volar direction by a mean ( SD) of 0.2  0.5 mm during jar grasp; the direction of metacarpal translation was highly variable, and therefore not statistically significant, during the jar twist task. On average, TMC joint instability during the execution of key pinch, jar grasp, and jar twist tasks was 0.038 mm/N (CI: 0.033–0.043 mm/N), 0.022 mm/N (CI: 0.019–0.025 mm/N), 0.017 mm/N (CI: 0.014–0.021 mm/N), respectively. Instability was significantly higher during the key pinch task than during the jar grasp and jar twist tasks (p < 0.001). Within each task, instability was not significantly different between sex

Figure 2. Functional tasks. 3D renderings of the hand of one subject during the functional task positions of key pinch, jar grasp, and jar twist, with the Labview interface that visually assisted the subjects in maintaining 80% of the maximum load for each task during imaging. JOURNAL OF ORTHOPAEDIC RESEARCH NOVEMBER 2015

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Figure 3. The applied loads. The mean loads (with 95% confidence interval bars) applied during the key pinch, jar grasp, and jar twist tasks. Subject groups included young healthy (YH) and older healthy (OH) men (M) and women (W), as well as patients with early stage osteoarthritis (OA).

Figure 4. Metacarpal translation. The statistically significant directions of motion in the TMC joint during the execution of the functional tasks were volar translation in key pinch and ulnar and volar translation in jar grasp. Translation of the metacarpal during jar twist did not occur in consistent directions.

groups, age groups, or between arthritic subjects and healthy controls (p > 0.074) (Fig. 5). Beighton scores on generalized laxity were also not significantly different among groups (p > 0.191), but trends indicated that generalized laxity decreased with age and that it may be higher in arthritic subjects than in healthy subjects of the same age group (Fig. 6). On average, Beighton scores for each group were below the threshold of 4, which is the value that is considered indicative of generalized joint laxity.38,39

DISCUSSION Mechanical instability is thought to be a predisposing risk factor for TMC OA. In the absence of conclusive evidence to support this hypothesis, we designed a study to assess instability during isometric loading of the TMC joint. The specific aim of the study was to determine if the female sex, older age, and the onset of TMC OA are associated with TMC joint instability during the execution of high demand functional tasks

that are known to load the TMC joint. We found that sex, age, and early OA do not significantly affect TMC joint stability during key pinch, jar grasp, and jar twist activities, although thumb strength during a jar grasp activity was lower in arthritic subjects than in healthy controls and trends indicate that men generally apply higher loads than women across the three tasks. We also found that a key pinch activity renders the TMC joint more unstable than jar grasp and jar twist activities. Our findings on thumb strength—based on both statistically significant results and observed trends— are consistent with conventional knowledge and findings reported in the literature. It has been previously shown that thumb strength is greater in men than women and relatively constant between the ages of 20 and 60 years, after which it decreases rapidly.40 The mean age of the older subjects we analyzed was less than 60 years, which might explain the lack of differences with age. The finding that arthritic women

Table 2. The Mean (95% CI) Magnitude of Metacarpal Translation (In Millimeter)

Key Pinch Jar Grasp Jar Twist

YM

YW

OM

OW

OAM

OAW

1.7 (1.1–2.5) 0.8 (0.6–1.1) 0.7 (0.5–1.2)

1.0 (0.7–1.5) 1.0 (0.8–1.1) 0.8 (0.4–1.3)

1.1 (0.6–2.1) 1.0 (0.7–1.4) 0.6 (0.3–1.3)

1.5 (1.1–2.1) 0.8 (0.7–1.0) 0.9 (0.5–1.4)

1.2 (1.0–1.6) 0.7 (0.6–0.9) 0.9 (0.7–1.1)

1.2 (1.0–1.5) 0.8 (0.7–0.9) 0.7 (0.5–0.9)

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Table 3. The Mean ( SD) Dorsal-Volar (D-/Vþ) Component of Metacarpal Translation (In Millimeter)

Key Pinch Jar Grasp Jar Twist

YM

YW

OM

OW

OAM

OAW

0.9  2.0 0.3  0.3 0.2  0.6

0.6  1.2 0.3  0.4 0.5  0.7

1.0  1.3 0.1  0.9 0.2  1.0

0.9  1.4 0.1  0.3 0.0  0.9

1.1  0.8 0.2  0.4 0.0  0.7

0.9  1.0 0.2  0.6 0.0  0.7

Table 4. The Mean ( SD) Ulnar-Radial (U-/Rþ) Component of Metacarpal Translation (In Millimeter)

Key Pinch Jar Grasp Jar Twist

YM

YW

OM

OW

OAM

OAW

0.1  1.4 0.8  0.8 0.5  0.7

0.2  0.9 0.8  0.3 0.0  1.0

0.4  1.3 0.6  0.7 0.1  1.0

0.3  1.0 0.7  0.5 0.3  1.5

0.2  1.1 0.7  0.3 0.3  1.0

0.4  1.2 0.6  0.8 0.2  0.8

Figure 5. Joint instability. Mean TMC joint instability (with 95% confidence interval bars) during key pinch, jar grasp, and jar twist tasks. Subject groups included young healthy (YH) and older healthy (OH) men (M) and women (W), as well as subjects with early stage osteoarthritis (OA).

applied lower loads during the jar grasp activity was expected, as reduction in grip strength is one of the leading symptoms associated with TMC OA. Our findings of no group differences in TMC joint instability during joint loading were surprising and contradict our initial hypotheses, which were based on the currently accepted beliefs that joint instability may be a predisposing factor in TMC OA, and therefore that it may be associated with the female sex, older age, and OA onset. The theory that translational instability leads to TMC OA18 emanates from studies reporting a correlation between the stage of OA and the integrity of the anterior oblique ligament (AOL),41 by the Framingham study that reported that radial subluxation measured in X-ray stress views predicts later onset of TMC OA in men,20 and by reports of a relationship between generalized joint hypermobility and TMC OA.21,22 The arthritic group tested here did not exhibit excessive translation when compared to asymptomatic subjects of the same age during the execution of the functional tasks. While this seems counterintuitive, it is possible that cocontraction of opposing muscles stabilize the joint during high demand tasks, obscuring the presence of instability that occurs with passive or lower-demand loading. However, Beighton scores on passive generalized laxity were also not significantly higher in arthritic patients than in healthy controls (Fig. 7).

Hence, conclusions about a causal relationship between hypermobility and TMC OA should be made cautiously. Their coexistence in later stage TMC OA may not be indicative of a causative relationship. When interpreting the findings presented here, it is important to consider the following limitations of this study. First, the effects of aging and early OA were inferred with a cross-sectional study design, and a follow-up longitudinal study may be required to deter-

Figure 6. Generalized joint laxity. Mean Beighton scores for generalized joint laxity (with 95% confidence interval bars). Subject groups included young healthy (YH) and older healthy (OH) men (M) and women (W), as well as subject with early stage osteoarthritis (OA). JOURNAL OF ORTHOPAEDIC RESEARCH NOVEMBER 2015

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Figure 7. Generalized joint laxity and TMC joint instability. Trends indicate that there is no relationship between the Beighton scores for generalized joint laxity and TMC joint instability during the execution of key pinch, jar grasp, and jar twist tasks.

mine these effects more conclusively. Second, we analyzed only three functional tasks, which were emulated using standard fixed-size mechanical fixtures, but there may be other tasks that could elicit instability in the TMC joint. We selected these three common tasks that cover both power-grasping and precision-handling type of activities because they are commonly reported as pain inducing in the arthritic joint. Third, there may be differences that we were unable to capture with our sample sizes. Post hoc power analyses (>95%) indicate that the group-wise comparisons within each task were powered to detect differences in translation of 1.1 mm, on average (range 0.3 to 2.4), and differences in instability of 0.07 mm/N, on average (range 0.02 to 0.5). Last, we used the load applied at the tip of the thumb since this is the best approximation that we could get for the force experienced by the metacarpal, but we ensured that the postures of the distal and proximal phalanges were consistent across subjects and therefore believe that the thumb-tip force amplifications down the kinematic chain were consistent. This cross-sectional study on three functional tasks that rely heavily on support from the thumb provides important insight on the role of joint instability on TMC OA, suggesting that individuals who develop TMC OA do not have joints that are inherently less stable during high-demand tasks and that joint instability alone may not be a primary etiological factor in TMC OA. Further insight into cartilage biology—the genetic, hormonal, and metabolic factors that influence it—and other mechanical factors implicated in joint health is needed to improve the current understanding of this multifactorial disease. In particular, elucidating the role of joint mechanics should shape the discussion on TMC OA pathogenesis and inform strategies for disease-modifying treatment.

AUTHORS’ CONTRIBUTIONS Eni Halilaj was involved with data processing, analysis, and interpretation, as well as drafting of the paper. Douglas C. Moore was involved with data acquisition, interpretation, as well as critical revising of the paper. Tarpit K. Patel was involved with data acquisition and data processing. Amy L. JOURNAL OF ORTHOPAEDIC RESEARCH NOVEMBER 2015

Ladd, Arnold-Peter C. Weiss, and Joseph J. Crisco were involved with data interpretation and critical revising of the paper. All the authors have read and approved the final submitted manuscript.

ACKNOWLEDGMENTS The authors would like to thank Jason T. Machan, Arlene J. Garcia, Deborah E. Kenny, Robert Chang, James C. Tarrant, Joel B. Schwartz, Bethany J. Wilcox, and Braden C. Fleming for their contributions. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

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JOURNAL OF ORTHOPAEDIC RESEARCH NOVEMBER 2015

Early osteoarthritis of the trapeziometacarpal joint is not associated with joint instability during typical isometric loading.

The saddle-shaped trapeziometacarpal (TMC) joint contributes importantly to the function of the human thumb. A balance between mobility and stability ...
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