Architecture of selected wrist flexor and extensor muscles ‘The architectural features of 25 wrist flexor and extensor muscles were studied. Muscles included the flexor carpi ulnaris, the flexor carpi radialis, the extensor carpi ulnaris, the extensor capri radialis brevis, and the extensor carpi radialis longus. Muscle length, mass, fiber pennation angle, fiber length, and sarcomere length (by use of laser diffraction techniques) were determined, In addition, physiological cross-sectional area and fiber length/muscle length ratio were caleu- lated. The muscles were found to be highly specialized, with architectural features of same muscles very similar. The fiber length/muscle length ratio, muscle length, and pennation angle represented the major differences between muscles, Thus using these parameters in discrim- inant analysis permitted correct identification of each of the 25 muscles. In terms of size and intrinsic design, these individual muscles were highly specialized for their function, (J Hap SuRG 1990;15A:244-50.) Richard L. Lieber, PhD, Babak M. Fazeli, and Michael J. Botte, MD, San Diego, Calif. Siecisnt mince arinoctue is dafined as the arrangement of the muscle fibers relative to the axis of force generation.' Architectural features include muscle fiber length (FL), orientation of muscle fibers relative to the axis of force generation (pennation angle, 6), and physiological cross-sectional area (CSA). Mus- cle architecture has a profound influence on its function. Many previous studies of skeletal muscle anatomy em- phasize fiber type differences between different mus- cles.? However, architectural differences can be more functionally significant. For example, it is believed that fast skeletal muscle fibers are slightly stronger and From the Division of Orthopaedics and Rehabiitetion, Veterans ‘Administration Medical Center; and University of California, San Diego, Calif ‘Supported by the UCSD Academic Senate, and NIH Grant AR3S192. Part of this work was presented atthe 1989 Orthopaedic Research Society and the 1989 UCSD Undergraduate Research Symposium. Received for publication Feb. 13, 1989; accepted in revised form ‘April 4, 1989. No benefits in any form have been received or will be received from ‘a commercial party related directly or indirectly to the subject of this articles, Reprint requests: Richard L. Lieber, PhD, Division of Orthopaedics and Rehabilitation (V-151), V.A. Medical Center and U.C. San Diego School of Medicine, 3350 La Jolla Village De., San Diego, CA 92161 3/1/13349 244° THE JOURNAL OF HAND SURGERY shorten approximately twice as fast as slow skeletal muscle fibers."? However, muscles of different archi- tecture, but similar fiber type, may differ in strength and speed by factors of 10 or 20."'*” In terms of gross functional properties, skeletal muscle architecture plays a greater role than fiber type distribution. Numerous muscle architecture studies have docu- mented significant differences between functional groups. For example, it has been demonstrated that the hamstring muscles of human beings,’ cats,° rabbits, and guinea pigs* are characterized by relatively long fiber lengths and small physiological cross-sectional areas compared to quadriceps muscles. Similar differ- ences exist between dorsifiexors and plantarflexors of various species. These data suggest that skeletal muscle architecture is matched to the functional requirements of the particular muscle groups. That is, the antigravity muscles (quadriceps and plantarflexors) generate rela- tively large forces due to their high pennation angles and large CSA, whereas the hamstring muscles and dorsiflexors produce large displacements and velocities because of their relatively long muscle fibers. Ina recent study of muscle architecture in the rabbit hindlimb,* we used the statistical method of discrimi- nant analysis to define the parameters that most power- fully discriminated between functional muscle groups. Our objective was to objectively identify unique dif- ferences between hamstring muscles and quadriceps,Vol. 15A, No. 2 March 1990 and dorsiflexors and plantarflexors. Numerous signifi- cant intrinsic and extrinsic differences between muscle groups were documented. This suggested that muscle groups differed not only in absolute size and shape but also in design. Few muscle architecture studies have been done in human subjects.”"° Selection of muscles for surgical transfer is based on, among other things, muscle ex- cursion and tension generating capacity.’ These func- tional parameters are a direct function of muscle fiber length and physiological cross-sectional area, respec- tively.''* Such architectural information may be of use in deciding which muscle is appropriate to perform a particular function after surgical transfer. The objective of this preliminary study, therefore, was to quantify architectural properties of selected forearm muscles in human subjects to determine the degree of specializa- tion of these muscles and the implications of such spe- cialization for tendon transfer procedures. Materials and methods Five muscles from each of five human cadaver spec- imens were studied (n = 25 muscles). On initial dis- section, it became obvious that forearm muscles of hu- ‘man subjects were more complex in arrangement and interconnection than similar muscles of animal hind- limbs. It was thus not possible to accurately isolate and perform architectural measurements (see below) on all of the human forearm muscles without destruction of adjacent muscles. Therefore, we chose to limit this study to the major wrist flexors and extensors: the flexor carpi ulnaris (KCU), the flexor carpi radialis (FCR), the extensor carpi radialis brevis (ECRB), the extensor carpi radialis longus (ECRL), and the extensor carpi ulnaris (ECU). Although these muscles are not com- ‘monly involved in a particular transfer, we believed that they represented the general nature of the wrist mus- culature and planned a second study, which would spe- cifically concentrate on muscles involved in particular transfers Architectural determination. Muscle architecture was determined according to the methods developed by Sacks and Roy.* Cadaver specimens were amputated above the elbow, arms were skinned and mounted to a board by inserting 3.2 mm Steinmann pins through the distal humerus and through the index, long, and ring metacarpals. The elbow was fixed at 90 degrees of flexion and the wrist and forearm in the neutral position. The fingers were not immobilized and thus assumed a flexed position during fixation. Each specimen was im- mersed in 10% phosphate-buffered formalin for 24 to Architecture of selected wrist flexor and extensor muscles 248 Fig. 1. Laser diffraction pattern from a muscle fiber bundle. ‘The long axis of the bundle lies in the plane of the paper. Any of the four diffraction orders (labeled 1, 2, 3, 4) can be used to calculate sarcomere length; however, in practice, only the first order was used. In practice, the diffraction angle (labeled @ in the figure) was measured using photodiode array interfaced to a computer.” 48 hours to fix the muscle tissue. The specimen was then rinsed in phosphate buffer for another 24 hours. ‘The muscles were removed, weighed (WT) and muscle length (ML) was measured as the distance from the origin of the most proximal muscle fibers to the inser- tion of the most distal muscle fibers. As much tendon as possible was removed before weighing. The muscles were then placed in 15% sulfuric acid to partially digest both the connective tissues surrounding the muscles and especially the endomysium around the muscle fibers. In pilot experiments, digestion times ranging from 12 to 72 hours in 12-hour increments were investigated to determine optimal digestion time. When digestion time ‘was too short, it was not possible (o isolate intact muscle fiber bundles (with fibers running from origin to inser- tion) while digestion times that were too long resulted in digestion of the fibers themselves. Average digestion time was 48 hours. After the digestion period, muscle fiber surface pennation angle was determined with a goniometer. Pennation angle varied along the length of the muscle (by about 4 degrees) and, therefore, mea- surements were obtained from the proximal, middle, and distal muscle portions and averaged to yield one value per muscle. Muscle fiber bundles (consisting of 5 to 50 muscle fibers) were isolated from the proximal, middle, and distal muscle regions and fiber bundle length (FL) was measured with dial calibers. Sarcomere length (SL) of the isolated fiber bundles was dctcrmined * by laser diffraction according to the method describedLieber, Fazeli, and Botte ‘The Journal of HAND SURGERY Fig, 2. Wrist flexors analyzed in the present study. Table I. Architectural features of selected human wrist muscles* Muscle Fiber Pennation (Cross-sectional Muscle mass ‘Muscle length length ‘angle ‘area studied (8) (mm) (um) (degrees) (mm) FLIML ratio FCR 109 +17 163.7 + 3.9 $12 = 19 34 #12 199 = 27 0.31 = 0.01 FCU 134 13 WIBS159 415 +23 21 +06 342 23 0.19 = 0.01 ECRB Bs +09 12722100 477237 89 = 20 213 = 18 0.38 = 0.03, ECRL, 18 + 1.2 81+ 74 163 = 59 25207 M46 + 11 0.82 = 0.04 ECU 136 +33 181.6 + 06 50.7 * 2.5 35203 260 = 71 0.28 + 0.01 “ean = SEM fora = Sof each ippe of muscle. See text Tor calculation of physiological cross-sectional are, by Lieber and associates." The muscle fiber bundle was mounted on a glass slide and transilluminated by a He-Ne laser (Model 05-LHR-171, Melles-Griot, Ir- vine, Calif.) (Fig. 1). SL was then calculated by use of the grating equation: nh = d-sin@ where n is the diffraction order (+1, +2, +3, ete.), Dis the laser wavelength (0.632 1m), d is the grating spacing (which equals SL), and @ is the diffraction angle measured by use of a photodiode array.” In all cases, the first order diffraction line was used for SL mea- surements (Fig. 1). In addition to the measured parameters, the following parameters were calculated: FL/ML ratio, FL/WT, and CSA/WT. Physiological cross-sectional area (CSA) ‘was determined according to the following equation": WT = cos0) CSA = 1 056 FL where 8 = the surface pennation angle and 1.056 = muscle density in gm/cm’." Proximal, middle, and distal FLs and SLs were averaged for each muscle to yield a representative muscle FL and SL. ML and FL were normalized to SL = 2.2 um to compensate for variations in limb position during fixation. Statistical analysis. Data were entered onto a PDP- 11/73 computer and analyzed with use of the BMDP software package. Initially, data were screened to in- sure that the parametric statistical test assumptions were satisfied (i. that the data were normally distributed ‘and that the variance between groups was equal). Next, ‘2 two-way analysis of variance was performed (two- way ANOVA; BMDP program P7D) to determine whether there was a significant difference between wrist flexors and extensors and between ulnarly placed and radially placed muscles for each parameter calculated (BMDP program P7D). Finally, discriminant analysis ‘was performed between flexors and extensors, ulnarly placed muscles and radially placed muscles, and be-Vol. 15A, No. 2 March 1990 Architecture of selected wrist flexor and extensor muscles 287 Fig. 3. Wrist extensors analyzed in the present study. tween each individual muscle to identify the parame- ters that best discriminated between groups (BMDP program P7M using F-to-enter = 5.000 and F-to- remove = 4.996). The significance level was set to p = 0.05. Data are expressed in the text as mean = SEM unless otherwise noted. Results Data were acquired from 25 muscles from 5 fore- arms. In several cases (6 of 75 measurements in four different muscles, 2 ECRLs, 1 FCU, and 2 ECUs) it ‘was not possible to obtain usable diffraction patterns from the proximal, middle, and distal portions of mus- cles and therefore SLs were not obtained. In these cases, average SL was determined from the remaining usable SL values. In all cases, at least two SL values were obtained from each muscle. Intramuscular sarcomere length values differed by an average of 2.1 * 0.5%. General features. The fibers of the FCU arose from the proximal portion of the muscle to a distance about 75% along the muscle length (Fig. 2). The individual fibers were relatively short (only about 20% ML Table 1). The FCU insertion tendon was actually en- closed by the muscle fibers so that, in cross section, the muscle took on the shape of an airplane wing, with the insertion tendon placed in the center of the “wing.” A relatively stout fascial sheath enclosed the FCU from its origin almost along the entire ML (Fig. 2). In con- trast, the FCR ML was shorter than the FCU and yet the muscles fibers were longer (Fig. 2, Table I). The insertion tendon extended out from the muscle mass a distance equivalent to approximately 75% of the ML. ‘The muscle fibers of the ECU extended the entire length of the musculotendinous unit (Fig. 3), which made it easy to identify by inspection of the distal tendon. The ECRL and ECRB were impossible to entirely separate at the lateral epicondyle (Fig. 3). Whereas the ML of the ECRB was longer than the ML of the ECRL, the ECRL fibers were clearly longer than the ECRB fibers, hence its name. As with the wrist flexors, the ulnarly placed extensor had almost no bare tendon extending out from the muscle mass, and both the ECRL and ECRB had a large, flattened tendon extending out from the muscle mass. The ECRL bare tendon was about twice as long as the ML, whereas the ECRB bare tendon extended from the muscle only about 25% of the ML. Architectural analysis. Two-way ANOVA revealed that the flexors and extensors did not differ significantly in WT, i.e., they contained roughly the same amount of contractile material; (p > 0.9, Table 1). Average extensor SL was significantly greater than the average flexor SL (p < 0.01), indicating that the extensors were fixed in a slightly lengthened position relative to the flexors. However, because muscle length and fiber length were normalized to a constant sarcomere length of 2.2 uum, this fixation artifact had no influence on subsequent data analysis. ML varied significantly be- tween the flexors and extensors (p < 0.001) and ul- narly placed and radially placed muscle (p < 0.001), with the flexors being longer than extensors and ulnarly placed muscles larger than radially placed muscles (Fig. 4). FL/ML ratio differed significantly between flexors and extensors (p <0.05) and ulnarly and radially‘The Journal of 248° Lieber, Fazeli, and Botte HAND SURGERY L4| ECU ECRL ECRB Fou FCR Extensors Flexors Fig. 4, Muscle length (normalized to a sarcomere length of 2.2 pm) for the five muscles studied. Each bar represents the mean + SEM for five samples. Note that muscle lengths differ between flexors and extensors as well as radially placed and ulnarly placed muscles. Abbreviations: FCU, Flexor carpi ulnaris; FCR, flexor carpi radialis; ECRB, extensor carpi radialis brevis; ECRL, extensor carpi radialis longus; ECU, extensor carpi ulnar, r 30.75 2 2 0.80 > x 5 x gos = = 0.00 ECU ECRL ECRB FOU FOR Extensors Flexors Fig. 5. Fiber length/muscle length ratio for the five muscles studied. Each bar represents the mean * SEM for five samples. Note that the ECRL has the largest ratio in spite of being the shortest muscle (c,f. Fig. 1). Abbreviations same as Fig. 4. placed muscle (p < 0.05, Fig. 5). However, this main ECRL with fibers (FL = 76 mm) that ran over 80% effect was primarily due to the high ratio of the ECRL of the muscle length at a very low pennation angle as opposed to pronounced gross differences between (8 = 2.5 degrees, Table I). On the opposite side of the groups. The muscle with the longest fibers was the spectrum, the FCU had the highest cross-sectional areaVol. 1A, No. 2 March 1990 Architecture of selected wrist flexor and extensor muscles 249 { Prnaen Angi (Sores) Fig. 6. Three-dimensional representation of the best discriminators between muscles (see Results). By plotting cach muscle in terms of its discriminators, each muscle occupies a different region of space. This is a reflection of the distinct properties of each muscle. (CSA = 342. mm’) and largest pennation angle (@ = 12 degrees) of any muscles studied. In terms of design, therefore, the FCU and ECRL were at opposite ends of the spectrum. Discriminant analysis showed that the best diserim- inator between flexors and extensors was ML. Use of the discriminating function to retrospectively classify the flexors and extensors was successful for approxi- mately 85% of the muscles. When trying to discriminate between ulnarly placed muscles and radially placed muscles, the two best discriminators were ML and WT. Again, the success rate for retrospective classification of the radially placed and ulnarly placed muscles was about 85%. Interestingly, although only one or two discriminators were entered into the discriminating equation for flexors versus extensors, and radially ver- sus ulnarly placed muscles, when trying to discriminate between all five muscles, three discriminators were en- tered into the equation. These were, in order from best to worst discriminator, FL/ML ratio, ML, and pen- nation angle. Thus the five muscles differed signifi- cantly in one intrinsic measure (FL/MIL ratio) and two extrinsic properties (ML and pennation angle). Sur- prisingly, it was possible to retrospectively classify all 25 muscles (100% correct classification) as FCU, ECU, ECRB, ECRL, or FCR using the discriminating func- tion, five times better than would be achieved by chance classification. Plotting each muscle as a function of its discriminators results in a graph where the various mus- cles occupy distinct regions of “architectural” space (Fig. 6). Muscles that are closest to one another are ‘most architecturally similar. “ussion This study demonstrated that the major wrist muscles differ significantly in their muscle architecture. In terms of absolute size and intrinsic design, the individual mus- cles are highly specialized for different functions. This is not necessarily the case when considering only the wrist flexors versus extensors or radially versus ulnarly placed muscles. That is, there docs not appear to be a general difference between wrist flexors and wrist ex- tensors except that perhaps the wrist flexors are some- what larger and generate greater tension (have greater CSA) than do the wrist extensors (Table 1). In com- parison, with our previous study of limb muscle archi- tecture,* it is apparent that there are much more dramatic differences between these five muscles of the wrist than between the antagonists in the lower limb. This is some- what surprising, since the primary purpose of the limb250 Lieber, Fazeli, and Botte ‘muscles is to provide locomotion and balance, whercas the wrist muscles have numerous functions, Our data agree qualitatively with the data of Brand and associates,” who showed that the FCU is the strong- est wrist flexor and the ECRL has extremely long mus- cle fibers. At the quantitative level, we differ with them somewhat in the absolute size and absolute fiber length of the various muscles studied, although it does not appear that these differences are of great consequence. ‘The fact that al five muscles were able to be classified on the basis of FL/ML ratio, ML, and pennation angle with 100% accuracy, underlines the highly specialized nature of each muscle. It is apparent that the five mus- cles are not simply interchangeable. For example, the very long fibers of the ECRL permit it to have a large range over which it generates tension, whereas, the same is not true with the FCU. It is interesting to note the relative relationship be~ ‘tween ECRL and ECRB. The juxtaposition of a muscle with long fibers to a muscle with short fibers is not unprecedented. For example, in hindlimbs of human beings,’ rabbits, and cats,* the synergistic pair of tib- ialis anterior and extensor digitorum longus differ greatly in their absolute fiber lengths and fiber length and muscle ratio. This suggests, for example, that the “TA can shorten over a greater range while maintaining tension or will be able to shorten at a higher absolute velocity while still maintaining tension." Of course, conclusive statements regarding function can only be ‘made in light of established joint kinematics. Therefore, in the case of the ECRL/ECRB synergism, it is possible that both muscles perform nearly identical functions, but that the ECRL simply uses a much larger moment arm at the wrist and therefore requires a greater range of motion. Such a situation is not the case in the TAVEDL synergism or MG/SOL synergism. For ex- ample the ‘TA has longer muscle fibers but a shorter moment arm and the MG and SOL both have identical moment arms as they insert on the Achilles tendon.* Future studies will be directed toward elucidation of the relationship between muscle architecture and joint kinematics in the human wrist for various types of motion. Architectural data, such as described in this article, performed on muscles specifically involved with tendon transfers, may ultimately provide additional informa- tion useful for such procedures. Tendon transfers are well accepted as a means to restore function due to injury of the radial, median, and ulnar nerves.'*"* Of- ten, multiple donors or different combinations of trans- fers are available. Factors influencing the selection of specific donors for transfer include availability, strength, amplitude, and integrity of the specific donor, ‘The Journal of HAND SURGERY the expendability of the donor, synergism, the route and direction of the transfer, the quality of soft tissue traversed by the transfer, and the experience or pref- erence of the surgeon. A knowledge of the muscle ar- chitecture may assist in this selection process. As the architecture of the upper limb muscles is defined, one may be able to select a transfer donor, based partially on architectural similarities to the muscle that normally performs the needed function, or based on the particular needs of the patient.? REFERENCES 1. Gans C. Fiber architecture and muscle function. Exerc Sport Sci Rev 1982;10:160-207. 2. Close RI. Dynamic properties of mammalian skeletal muscles. Physiol Rev 1972;52:129-97, 3. Bodine SC, Roy RR, Eldred E, Edgerton VR. 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