Complex, Multidimensional Thumb Movements Generated by Individual Extrinsic Muscles

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1 Complex, Multidimensional Thumb Movements Generated by Individual Extrinsic Muscles Zong-Ming Li, Jie Tang, Matthew Chakan, Rodrigo Kaz Hand Research Laboratory, Departments of Orthopaedic Surgery and Bioengineering, University of Pittsburgh, 210 Lothrop Street, E1641 BST, Pittsburgh, Pennsylvania Received 9 October 2007; accepted 7 January 2008 Published online in Wiley InterScience ( DOI /jor ABSTRACT: The objective of this study was to investigate three-dimensional thumb joint movements produced by individual extrinsic thumb muscles. Ten cadaveric arms were dissected to expose the musculotendinous junctions of the flexor pollicis longus (FPL), abductor pollicis longus (APL), extensor pollicis brevis (EPB), and extensor pollicis longus (EPL). Each muscle/tendon was loaded to 10% of its maximal force capability whereas three-dimensional angular movements of the carpometacarpal (CMC), metacarpophalangeal (MCP), and interphalangeal (IP) joints were obtained simultaneously. We found that each extrinsic muscle produced unique joint angular trajectories in multiple directions. The FPL, APL, EBP, and EPL generated two, two, three, and six movements, respectively. The extrinsic muscles all together generated eight movements among the multiple thumb joints. High interjoint coordination was shown between the MCP joint flexion and IP joint flexion by FPL loading, as well as between the MCP joint extension and IP joint extension by EPL loading. High intrajoint coordination was observed between extension and supination at the CMC joint by the APL, EPL, and EPB. We concluded that each muscle produces movements in multiple joints and/or in multiple anatomical directions. The findings provide a novel insight into the biomechanical roles of the extrinsic muscles of the thumb. ß 2008 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. J Orthop Res 26: , 2008 Keywords: hand; thumb; kinematics; muscle The human thumb is exceptionally mobile, strong, and dexterous partially due to its sophisticated musculature. Kinematically, thumb motion results from complicated combinations of flexion/extension, abduction/ adduction, and pronation/supination (i.e., axial rotation) at the carpometacarpal (CMC), metacarpophalangeal (MCP), and interphalangeal (IP) joints. 1,2 The movement capability of the thumb was previously determined by measuring the linear distance between the thumb tip and the fingertips or other anatomical landmarks, 3,4 but thumb pathology can be characterized by examining the angular motion at the individual joints. Manual goniometry is commonly used in the clinic to evaluate statically joint mobility in a single plane. Electrogoniometers can be used to monitor dynamic joint motion, 5 but they can be too bulky to record simultaneous movements from multiple joints within the thumb and can interfere with delicate thumb movements. X-rays, 1,6 and CT 7 have been used to study in vivo thumb kinematics, but the amount of kinematic information is limited. Recently, noninvasive, marker-based video methods have been used to study advanced kinematic features thus providing a more accurate representation of thumb motion. 2,8 11 Marker-based motion analyses were applied to study thumb pathokinematics in individuals with cervical myelopathy 12 and lower median nerve block; 13 the authors reported aberrant thumb kinematics during pinch movements. Thus far, our understanding of thumb motion by each muscle remains dominated by basic functional anatomy using unidirectional, simplified nomenclature such as flexors or extensors. Therefore, this study was undertaken to elucidate thumb joint kinematics generated by Correspondence to: Zong-Ming Li (T: ; F: ; zmli@pitt.edu) ß 2008 Orthopaedic Research Society. Published by Wiley Periodicals, Inc. individual muscles. We used cadaveric hands to precisely simulate force production by a single muscle. We limited this study to the four extrinsic muscles because force simulation on an extrinsic muscle could be implemented without disrupting anatomical structure. We addressed two questions. First, what movements of the thumb joints are actuated by each extrinsic muscle? We hypothesized that each muscle generates multiple movements that occurred in multiple joints and/or in multiple anatomical planes. Second, assuming that a muscle generates multiple movements, what are their relationships within a given joint and across multiple joints. We hypothesized that a muscle generates coordinated multiple movements within a joint and across multiple joints. MATERIALS AND METHODS Fresh-frozen, right cadaveric arms were used, disarticulated at the midhumerus and thawed at room temperature prior to testing. Specimens possessed a normal range of motion and were free from gross deformity. Two specimens were excluded: one with increased CMC joint laxity, and one with severe osteoarthritis at the CMC joint detected by radiographs and dissection. The remaining specimens (four male, six female) had mean (SD) age of 52.8 (6.4) years. A minimal dissection was performed on each specimen to expose the musculotendinous junctions of the flexor pollicis longus (FPL), abductor pollicis longus (APL), extensor pollicis brevis (EPB), and extensor pollicis longus (EPL) muscles. Tissue moisture was maintained by periodically applying a 0.9% saline solution (Baxter Healthcare, Deerfield, IL) during dissection and testing. Each tendon was sutured at a location slightly distal to its musculotendinous junction using a baseball stitch technique, leaving excess suture material to tie into a loop for subsequent force application. Proximal and distal anatomy of the muscles remained intact. The specimen was mounted on a custom apparatus to maximize the view of the dorsal surface of the thumb (Fig. 1A). The elbow was fixed in 908 of flexion by attaching a clamp to the end of the transected humerus, while the forearm was fixed in neutral pronation/supination by 1289

2 1290 LI ET AL. Figure 1. A specimen mounted in the fixation apparatus for muscle loading and thumb motion recording. (A) A global view of the entire arm with 9 markers visible. (B) A radial view of the hand with all 12 markers visible. [Color figure can be viewed in the online issue, which is available at inserting two 5.0-mm Schanz screws into the proximal radius and holding the screws with external fixator clamps (Trauma- Fix Universal System, Orthopaedic Innovation, Sheffield, UK). Digits two through five were attached to a flat, rigid support so that their MCP, PIP, and DIP joints were in neutral position. The finger support was oriented to align the axis of the second metacarpal with the radial axis, thus keeping the wrist in neutral posture. 3D thumb kinematics was obtained by optically tracking surface markers attached to the hand using double stick tape. T-shaped plates with 12 reflective markers (5-mm diam) were attached to the hand (Fig. 1B) to establish local coordinate frames (Fig. 2). Markers 10, 11, and 12 were attached to the dorsal aspect of the second and third to establish a reference frame representing the stationary distal radius. Before each trial, the thumb was randomly and manually moved for 15 s for preconditioning, then placed in a position with minimal resistance to motion (i.e., resting posture). The muscles were individually loaded in a random order by manually pulling on the suture loops. The force application was visually aligned to the muscle s line of action and directed toward the muscle origin. Force was monitored by a force transducer (Nano17, ATI Industrial Automation, Apex, NC) interfaced with a customized LabVIEW program (National Instruments, Austin, TX). Using a visual force display, a loading force was ramped to 10% of the maximum force capability of each muscle 14 over 10 s. Thumb motion via the surface markers was recorded using a motion analysis system (VICON 460, Oxford, UK). Force and motion data were recorded at 100 Hz and were synchronized by a step signal from the LabVIEW program to the motion analysis system. Three trials were performed for each muscle. Flexion/extension, abduction/adduction, and pronation/ supination angles at the CMC, MCP, and IP joints were determined using Euler angles based on the neighboring coordinate frame of joints 2 (Fig. 2). From the force and angle data, joint coordination patterns were analyzed using correlation and regression methods, and ranges of motion in individual movement planes of the individual joints were calculated. Range of motion was considered significant if its absolute value was significantly greater than 58, using a one-sample, onetailed t-test (a ¼ 0.05). RESULTS The extrinsic muscles generated characteristic angular trajectories in individual anatomical planes across individual joints (Fig. 3). Some curves remained flat in certain planes, but each muscle generated more than one movement in multiple planes and/or in multiple joints. For each movement, the trajectory ascended or descended monotonically with increasing force. For total movement in the 0 to 10% force range, most movement occurred within the initial 5% force and then tended to plateau in the 5 to 10% force range. However, a different pattern was observed for the abduction/adduction curve of the CMC joint by the APL (Fig. 3B). The joint Figure 2. Coordinate frames of the thumb and forearm established by the surface markers. The coordinate frame in the dotted circle is established by the markers attached to the dorsal aspect of the hand and is used to represent of the distal radius. Extension (þ) and flexion ( ) occur about the X-axis; abduction (þ) and adduction ( ) occur about the Y-axis; and pronation (þ) and supination ( ) occur about the Z-axis. [Color figure can be viewed in the online issue, which is available at

3 THUMB MOVEMENTS 1291 Figure 3. Angular trajectories generated by individual muscles. Each forceangle curve was averaged across the 10 specimens. The muscle loadings are expressed as the percentages of their respective maximum force potentials. Each panel shows the three angular movements in flexion ( )/extension (þ) ( ), abduction (þ)/adduction ( ) (), and pronation (þ)/ supination ( ) (- - -) of a specific joint by a specific muscle. abducted slightly within the first 2% force, and then moved towards adduction. The extrinsic muscles collectively generated significant joint movements across eight of the nine possible movements across the three joints and three angular directions (Fig. 4; p < 0.005). The FPL generated two dominant movements: MCP joint flexion and IP joint flexion. On average, the FPL flexed the MCP joint by 14.68, and flexed the IP joint in a much larger amount, The FPL did not generate any significant movements at the CMC joint. The APL generated two significant movements within the CMC joint, in extension and in supination. Surprisingly, the APL did not significantly abduct the CMC joint (p ¼ 0.996), and there were no significant movements at the MCP or IP joint. The EPB generated three significant movements at the CMC and MCP joints. The EPB extended the CMC and MCP joints by and 25.58, respectively, and supinated the CMC joint by The EPL generated as many as six movements across the CMC, MCP, and IP joints. The EPL extended the CMC, MCP, and IP joints by 18.48, 25.78, and 21.98, respectively. The EPL also adducted and supinated the CMC joint by and 19.08, respectively. In addition, the EPL generated small, but significant, MCP joint adduction of The multiple movements generated by a muscle occurred in a coordinated manner. The coordination was observed among multiple joints in a specific movement plane (i.e., interjoint coordination) or among multiple movement planes within a specific joint (i.e., intrajoint coordination) (Tables 1 and 2). The FPL generated interjoint coordination in flexion between the MCP and IP joints, with a correlation coefficient of 0.93 (Fig. 3; Table 1). The EPB generated coordinated

4 1292 LI ET AL. Figure 4. Ranges of motion (ROM, degrees) produced by individual muscles. A positive value denotes that the motion was generated toward extension, abduction, or pronation, while a negative value denotes the motion was generated toward flexion, adduction, or supination. extension between the CMC and MCP joints (R ¼ 0.78). The EPL generated coordinated extensions at the CMC, MCP, and IP joints, and coordinated adduction at the CMC and MCP joints. Intrajoint coordination occurred within the CMC and MCP joints (Table 2). The APL consistently generated highly correlated movements between extension and supination at the CMC joint (R 2 ¼ ). The slope of the regression was , meaning that an increase in extension was linearly coupled with an equal increase in supination. Likewise, the EPB and EPL generated highly coordinated movements between supination and extension at the CMC joint (Table 2), with supination to extension ratios of and

5 THUMB MOVEMENTS 1293 Table 1. Correlation Coefficients (Mean SD) for Interjoint Coordination (i.e., Coordination among Movement Trajectories across Joints) Muscle Joint Pair Movement Direction Correlation Coefficient FPL MCP IP Flexion EPB CMC MCP Extension EPL CMC MCP Extension MCP IP Extension CMC MCP Adduction , respectively. In addition, the EPL generated adduction extension coupling at the CMC joint and the MCP joint, with adduction to extension ratios of and , respectively. DISCUSSION Our first purpose was to identify the exact movements of the thumb joints generated by each extrinsic muscle. Each muscle produced movements in multiple joints and/or in multiple anatomical planes. The FPL, APL, EPB, and EPL generated two, two, three, and six movements, respectively. The FPL-generated movements were limited to flexion of the MCP and IP joints. The APL generated movements in multiple directions (i.e., extension and supination), but the movements were limited to the CMC joint. The EPB-generated movements in multiple directions (i.e., extension and supination) in multiple joints (i.e., CMC and MCP joints). The EPL generated the most complicated movements, influencing all joints and acting on multiple anatomical planes. Together, the four extrinsic muscles generated eight movements: CMC joint extension, adduction, and supination; MCP joint flexion, extension, and adduction; and IP joint flexion and extension. Among the eight movements, some can be contributed by multiple extrinsic muscles, some by a single extrinsic muscle, yet some cannot be realized by any extrinsic muscles. Our second purpose was to examine the coordination pattern of the multiple movements by each muscle. We found consistent inter- and intrajoint coordination patterns generated by the muscles. The FPL generated Table 2. Correlation Coefficients (Mean SD) for Intrajoint Coordination (i.e., Coordination among Movement Trajectories within Specific Joints) Joint Muscle Direction Pair Correlation Coefficient CMC joint APL Extension supination EPB Extension supination EPL Extension supination EPL Extension adduction MCP joint EPL Extension adduction MCP IP joint coordination in flexion. The EPB generated CMC MCP joint coordination in extension. The EPL generated CMC MCP IP joint coordination in extension and CMC MCP joint coordination in adduction. Intrajoint coordination occurred at the CMC and MCP joints. The APL and EPB generated extension supination coordination at the CMC joint. The EPL generated extension adduction supination coordination at the CMC joint and extension adduction coordination at the MCP joint. A specific movement could be generated by multiple muscles because of the overlapping kinematic function of the individual muscles. For example, extension and supination at the CMC joint can be achieved by the APL, EPB, and EPL. Extension of the MCP joint can be realized by the EPB and EPL. The EPB and APL had similar motion effects of CMC joint extension and supination, but the EPB also extended the MCP joint. The functional consortium of the muscles may allow the thumb to meet task requirements when some of the muscles are deficient. Indeed, loss of the APL and EPB has minimal adverse effects on the 3D thumb movement in patients. 15 However, some muscles are more indispensable for thumb and hand function. For example, a congenital absence of the FPL was accompanied with a total loss of IP joint flexion because no other extrinsic or intrinsic muscles could compensate for this deficiency. 16 Although our results are generally consistent with functional anatomy and with experimental data of the moment potentials of thumb muscles, 17 the kinematic consequences by the extrinsic muscles are more complicated than or even different from the known muscle function. In our study, the FPL generated flexion at the MCP and IP joints, but did not generate flexion movement at the CMC joint despite its obvious moment potential in flexion. The FPL initially flexes the IP joint, then the MCP joint, and finally in a weak manner the CMC joint. 3 The disparity between the moment potentials of a muscle and the actual joint movements by the muscle might result from joint surface configuration and soft tissue constraints. Our finding of the extension and supination roles of the APL confirms previous observations that the APL plays a weak role in abduction, 18,19 and it was consistently active during thumb opening. 20 The lack of abduction at the CMC joint by the APL is inconsistent with functional anatomy and is inconsistent with the abduction moment potential of the APL. 17 Also, our results provide a novel insight into the biomechanical role of the APL, EPB, and EPL in supinating the CMC joint, whereas moment potentials in pronation/ supination were not considered in the previous study. 17 Our findings signify the inadequacy of conventional anatomical nomenclature in conveying biomechanical functions of thumb muscles. The kinematics generated by a muscle are more complex than its anatomically implied function because a single muscle can generate movements in multiple directions across multiple joints. For example, the EPL not only extended the CMC, MCP, and IP joints, but also adducted and supinated the CMC

6 1294 LI ET AL. joint and adducted the MCP joint. More surprisingly, the movement outputs by a muscle may not even correspond to its anatomically implied function. For example, the APL, an abductor by name, produces extension and supination at the CMC joint, but little abduction. This result agrees with the observation that the APL is an effective thumb extensor, but a weak abductor, 18 and it is recruited with increasing thumb abduction to assist the primary abductors, the abductor pollicis brevis and opponens pollicis. 21 The APL functions as a stabilizer enabling the abductor pollicis brevis to be more effective in thumb abduction. 19 Our results allow us to infer the kinesiological functions of the intrinsic muscles. At the CMC joint, the extrinsic muscles in concert are capable of generating joint motion in extension, adduction, and supination. The intrinsic muscles must play a critical role in contributing to CMC joint motion in flexion, abduction, and pronation since these movements exist. The compound motion of the CMC joint in flexion, abduction, and pronation during opposition is one of the most important functions of the thumb. Therefore, the intrinsic muscles are primary contributors to the opposition movement, whereas the extrinsic muscles (except for the FPL) are responsible for moving the thumb in the counteropposition direction to release grip. 3 This dichotomy helps explain the commonly observed functional impairment to opposition in patients with median neuropathy, because the median nerve is neuroanatomically associated with the thenar muscles. The intrinsic and extrinsic muscles may jointly contribute to a specific direction of force or motion. For example, the adductor pollicis longus is a strong adductor of the CMC joint even though the EPL also provides adduction. In addition, the adductor pollicis has a strong flexion potential at the CMC joint, 17 which is synergistic with the FPL. This functional overlap explains the Froment s sign caused by ulnar nerve palsy, as the FPL is overly activated to compensate for the impaired adductor pollicis for pinch tasks, causing hyperflexion of the IP joint. We found that extrinsic muscles were capable of generating flexion (by the FPL), extension (by the EPB and EPL), and slight adduction (by the FPL) at the MCP joint. Likewise, the intrinsic muscles are called upon for other movements (e.g., abduction and pronation 2 at the MCP joint). The IP joint is commonly considered a hinge joint with only flexion and extension, which can be achieved by the FPL and EPL, respectively. Still, the intrinsic muscles provide assistance to IP joint extension via the extensor mechanisms. 22 Interjoint coordination is expected because of the multiarticular nature of the extrinsic muscles, and because a tensioned muscle creates mechanical torques over all the spanned joints. For example, the EPL originates in the forearm, and its tendon crosses the CMC, MCP, and IP joints before it inserts into the base of the distal phalanx of the thumb. Contraction of this muscle has mechanical effects on all the joints it crosses. The interjoint coordination patterns are also commonly observed among thumb joints (during pinch movements 2,23 ) and finger joints. 24 A consistent pattern of intrajoint coordination was observed at the CMC and MCP joints. The coordinated motion between extension and supination at the CMC joint complements our previous finding of in vivo flexionpronation coordination at the CMC joint during thumb opposition. 2 These intrajoint coordination patterns agree with the notion that axial rotation at the CMC joint does not occur independently, but as part of the conjunct movement of flexion/extension. 1,23 The coordination within the CMC joint may be attributable to the line of tendon force, 17,25 joint surface configuration, 23 and ligament constraint. 26 Hollister and colleagues 23 argued that the intrajoint coordination at the CMC and MCP joints is mainly due to the thumb joints having axes of rotation that are offset from the anatomical planes, leading to conjunct movements. 23 We found that the APL, EPB, and EPL generated axial rotation (i.e., supination) at the CMC joint, although the rotation was coupled with movements in other planes. Our previous study also showed substantial axial rotations at the CMC joint as well as at the MCP joint during thumb opposition, although the rotation was coupled with flexion/extension. 2 We acknowledge several limitations of this study. First, the relationship between a muscle force and joint movements is dependent upon the mechanical properties of the joint. The joint resistance in a cadaveric hand (e.g., joint lubrication and nominal tendon tension) may be different from in vivo, limiting the generalization of our results. The discrepancy could be assessed by evaluating the change of passive resistance. It is advantageous to identify the biomechanical outputs of a single muscle using a cadaveric model, 27 but future in vivo studies using electrical stimulation may be performed to validate the biomechanical role of individual thumb muscles. Second, each tendon was loaded to 10% of its maximum force capacity, so the joint movements should be interpreted only in this force range. Nevertheless, a 10% force level is realistic because thumb movements require submaximal muscle activations. The motion trajectories confirm that a large portion of joint movement ranges were attained within 5% force. The thumb only uses a small portion (<35%) of its available ranges of motion to perform activities of daily living. 28 Third, the starting joint positions were somewhat variable, especially for the flexion angles at the IP joint. This variation might have been caused by accidental tension prior to muscle loading because the starting joint position was shifted towards the movement, that is, more flexed starting position for the FPL and more extended starting position for the EPL. This systematic (not random) error for estimating range of motion was negligible for the CMC and MCP joints and relatively small (<88) for the more variable IP joint. Fourth, we only investigated the kinematics of extrinsic muscles. It is challenging to examine thumb kinematics by tensioning intrinsic muscles, as they may have broad insertion areas, and muscle forces cannot be simply represented by a simple resultant force. The manipulation of the intrinsic muscles may disrupt local

7 THUMB MOVEMENTS 1295 anatomy and alter thumb kinematics, yet the force by an extrinsic muscle can be conveniently simulated with the thumb anatomy preserved, yielding a force motion relationship with a high degree of fidelity. In conclusion, our results showed that each muscle produces movements in multiple joints and/or in multiple anatomical directions, thus providing a novel insight into the biomechanical roles of the extrinsic muscles of the thumb. ACKNOWLEDGMENTS This study was supported by the Frank E. Raymond Memorial Research Grant from the OREF. REFERENCES 1. Cooney WP 3rd, Lucca MJ, Chao EY, et al The kinesiology of the thumb trapeziometacarpal joint. J Bone Joint Surg Am 63: Li ZM, Tang J Coordination of thumb joints during opposition. J Biomech : Kapandji IA Biomechanics of the thumb. In: Tubiana R, editor. The hand, vol. 1. Philadelphia, PA: Saunders; p Kapandji AI Clinical evaluation of the thumb s opposition. J Hand Ther 5: Chao EY Justification of triaxial goniometer for the measurement of joint rotation. J Biomech 13: Kuo LC, Su FC, Chiu HY, et al Feasibility of using a video-based motion analysis system for measuring thumb kinematics. J Biomech 35: Cheema TA, Cheema NI, Tayyab R, et al Measurement of rotation of the first metacarpal during opposition using computed tomography. J Hand Surg Am 31: Coert JH, van Dijke HG, Hovius SE, et al Quantifying thumb rotation during circumduction utilizing a video technique. J Orthop Res 21: Kuo LC, Cooney WP 3rd, Kaufman KR, et al A quantitative method to measure maximal workspace of the trapeziometacarpal joint normal model development. J Orthop Res 22: Lee SW, Zhang X Development and evaluation of an optimization-based model for power-grip posture prediction. J Biomech 38: Su FC, Kuo LC, Chiu HY, et al Video-computer quantitative evaluation of thumb function using workspace of the thumb. J Biomech 36: Sakai N Finger motion analysis of the patients with cervical myelopathy. Spine 30: Li ZM, Nimbarte AD Peripheral median nerve block impairs precision pinch movement. Clin Neurophysiol 117: Brand PW, Beach RB, Thompson DE Relative tension and potential excursion of muscles in the forearm and hand. J Hand Surg Am 6: Britto JA, Elliot D Thumb function without the abductor pollicis longus and extensor pollicis brevis. J Hand Surg Br 27: Thomas C, Mathivanan T Congenital absence of flexor pollicis longus without hypoplasia of the thenar muscles. J Hand Surg Br 24: Smutz WP, Kongsayreepong A, Hughes RE, et al Mechanical advantage of the thumb muscles. J Biomech 31: Cooney WP, Linscheid RL, An KN Opposition of the thumb: an anatomic and biomechanical study of tendon transfers. J Hand Surg Am 9: van Oudenaarde E, Brandsma JW, Oostendorp RA The influence of forearm, hand and thumb positions on extensor carpi ulnaris and abductor pollicis longus activity. Acta Anat 158: Johanson ME, Skinner SR, Lamoreux LW Phasic relationships of the intrinsic and extrinsic thumb musculature. Clin Orthop Relat Res 322: Cooney WP 3rd, An KN, Daube JR, et al Electromyographic analysis of the thumb: a study of isometric forces in pinch and grasp. J Hand Surg Am 10: von Schroeder HP, Botte MJ The dorsal aponeurosis, intrinsic, hypothenar, and thenar musculature of the hand. Clin Orthop Relat Res 383: Hollister A, Giurintano DJ Thumb movements, motions, and moments. J Hand Ther 8: Darling WG, Cole KJ, Miller GF Coordination of index finger movements. J Biomech 27: Brand PW, Hollister AM Clinical mechanics of the hand, 3rd ed. St. Louis, MO: Mosby, Inc. 26. Zancolli EA, Ziadenberg C, Zancolli E Jr Biomechanics of the trapeziometacarpal joint. Clin Orthop 220: Pearlman JL, Roach SS, Valero-Cuevas FJ The fundamental thumb-tip force vectors produced by the muscles of the thumb. J Orthop Res 22: Hume MC, Gellman H, McKellop H, et al Functional range of motion of the joints of the hand. J Hand Surg Am 15: