Richard L. Lieber

FUNCTIONAL AND CLINICAL SIGNIFICANCE OF SKELETAL MUSCLE ARCHITECTURE

Skeletal muscle architecture is the structural property of whole muscles that dominates their function. This review describes the basic architectural properties of human upper and lower extremity muscles. The designs of various muscle groups in humans and other species are analyzed from the point of view of optimizing function. Muscle fiber arrangement and motor unit arrangement is discussed in terms of the control of movement. Finally, the ability of muscles to change their architecture in response to immobilization, eccentric exercise, and surgical tendon transfer is reviewed. Future integrative physiological studies will provide insights into the mechanisms by which such adaptations occur. It is likely that muscle fibers transduce both stress and strain and respond by modifying sarcomere number in a way more suited to the new biomechanical environment.

A Model of the Lower Limb for Analysis of Human Movement

Computer models that estimate the force generation capacity of lower limb muscles have become widely used to simulate the effects of musculoskeletal surgeries and create dynamic simulations of movement. Previous lower limb models are based on severely limited data describing limb muscle architecture (i.e., muscle fiber lengths, pennation angles, and physiological cross-sectional areas). Here, we describe a new model of the lower limb based on data that quantifies the muscle architecture of 21 cadavers. The model includes geometric representations of the bones, kinematic descriptions of the joints, and Hill-type models of 44 muscle–tendon compartments. The model allows calculation of muscle–tendon lengths and moment arms over a wide range of body positions. The model also allows detailed examination of the force and moment generation capacities of muscles about the ankle, knee, and hip and is freely available at www.simtk.org.

Structural and mechanical basis of exercise-induced muscle injury

It is well documented in both animal and human studies that unaccustomed, particularly eccentric, muscle exercise may cause damage of muscle fiber contractile and cytoskeletal components. These injuries typically include: Z-band streaming and dissolution, A-band disruption, disintegration of the intermediate filament system, and misalignment of the myofibrils. The mechanical basis for this damage is suggested to be due to the fiber strain magnitude rather than the absolute stress imposed on the fiber. We hypothesize that eccentric contraction-induced damage occurs early in the treatment period, i.e., within the first few minutes. The structural abnormalities predominate in the fast-twitch glycolytic fibers. In the final section of this paper, we hypothesize a damage scheme, based on the muscle fiber oxidative capacity as a determining factor.

Are Current Measurements of Lower Extremity Muscle Architecture Accurate

Skeletal muscle architecture is defined as the arrangement of fibers in a muscle and functionally defines performance capacity. Architectural values are used to model muscle-joint behavior and to make surgical decisions. The two most extensively used human lower extremity data sets consist of five total specimens of unknown size, gender, and age. Therefore, it is critically important to generate a high-fidelity human lower extremity muscle architecture data set. We disassembled 27 muscles from 21 human lower extremities to characterize muscle fiber length and physiologic cross-sectional area, which define the excursion and force-generating capacities of a muscle. Based on their architectural features, the soleus, gluteus medius, and vastus lateralis are the strongest muscles, whereas the sartorius, gracilis, and semitendinosus have the largest excursion. The plantarflexors, knee extensors, and hip adductors are the strongest muscle groups acting at each joint, whereas the hip adductors and hip extensors have the largest excursion. Contrary to previous assertions, two-joint muscles do not necessarily have longer fibers than single-joint muscles as seen by the similarity of knee flexor and extensor fiber lengths. These high-resolution data will facilitate the development of more accurate musculoskeletal models and challenge existing theories of muscle design; we believe they will aid in surgical decision making.

Architecture of selected muscles of the arm and forearm: anatomy and implications for tendon transfer.

The architectural features of twenty-one different forearm muscles (n = 154 total muscles) were studied. Muscles included the extensor digitorum communis to the index, middle, ring, and small fingers, the extensor digit quinti, the extensor indicis proprius, the extensor pollicis longus, the flexor digitorum superficialis, the flexor digitorum profundus, the flexor pollicis longus, the pronator quadratus, the palmaris longus, the pronator teres, and the brachioradialis. Muscle length, mass, fiber pennation angle, fiber length, and sarcomere length were determined with the use of laser diffraction techniques. From these values, physiologic cross-sectional area and fiber length/muscle length ratio were calculated. The individual digital extensor muscles were found to be relatively similar in architectural structure. Similarly, the deep and superficial digital flexors were very similar architecturally, with the exception of the small finger flexor digitorum superficialis, which was much smaller and shorter than the rest of the digital flexors. The brachioradialis and the pronator teres had dramatically different architectural properties. While the masses of the two muscles were nearly identical, the muscles had significantly different predicted contractile properties based on their different fiber arrangement. The brachioradialis, with its long fibers arranged at a small pennation angle, had a physiologic cross-sectional area that was only one third that of the pronator teres, with its short fibers that were more highly pennated. Using these architectural data and the statistical method of discriminant analysis, we provide additional information that might be useful in the selection of potential donor muscles to restore thumb flexion, thumb extension, finger extension, and finger flexion.

STRUCTURAL AND FUNCTIONAL CHANGES IN SPASTIC SKELETAL MUSCLE

This review summarizes current information regarding the changes in structure or function that occur in skeletal muscle secondary to spasticity. Most published studies have reported an increase in fiber size variability in spastic muscle. There is no general agreement regarding any shift in fiber type distribution secondary to spasticity. Mechanical studies in whole limbs as well as in isolated single cells support the notion of an intrinsic change in the passive mechanical properties of muscle after spasticity in addition to the more widely reported neural changes that occur. Evidence is presented for changes within both the muscle cell and extracellular matrix that contribute to the overall changes in the tissue. Taken together, the literature supports the notion that, although spasticity is multifactorial and neural in origin, significant structural alterations in muscle also occur. An understanding of the specific changes that occur in the muscle and extracellular matrix may facilitate the development of new conservative or surgical therapies for this problem. Muscle Nerve 29: 615–627, 2004

Structure and Function of the Skeletal Muscle Extracellular Matrix

The skeletal muscle extracellular matrix (ECM) plays an important role in muscle fiber force transmission, maintenance, and repair. In both injured and diseased states, ECM adapts dramatically, a property that has clinical manifestations and alters muscle function. Here we review the structure, composition, and mechanical properties of skeletal muscle ECM; describe the cells that contribute to the maintenance of the ECM; and, finally, overview changes that occur with pathology. New scanning electron micrographs of ECM structure are also presented with hypotheses about ECM structure–function relationships. Detailed structure–function relationships of the ECM have yet to be defined and, as a result, we propose areas for future study. Muscle Nerve 44: 318–331, 2011

Spastic muscle cells are shorter and stiffer than normal cells

The mechanical properties of isolated single muscle fiber segments were measured in muscle cells obtained from patients undergoing surgery for correction of flexion contractures secondary to static perinatal encephalopathy (cerebral palsy). “Normal” muscle cells from patients with intact neuromuscular function were also mechanically tested. Fiber segments taken from subjects with spasticity developed passive tension at significantly shorter sarcomere lengths (1.84 ± 0.05 μm, n = 15) than fibers taken from normal subjects (2.20 ± 0.04 μm, n = 35). Elastic modulus of the stress–strain relationship in fibers from patients with spasticity (55.00 ± 6.61 kPa) was almost double that measured in normal fibers (28.25 ± 3.31 kPa). The fact that these muscle cells from patients with spasticity have a shorter resting sarcomere length and increased modulus compared with normal muscle cells suggests dramatic remodeling of intracellular or extracellular muscle structural components such as titin and collagen. Such changes in muscles of patients with spasticity may have implications for therapy. Muscle Nerve, 27: 157–164 ,2003

Corrective Shoes and Inserts as Treatment for Flexible Flatfoot in Infants and Children

We performed a prospective study to determine whether flexible flatfoot in children can be influenced by treatment. One hundred and twenty-nine children who had been referred by pediatricians, and for whom the radiographic findings met the criteria for flatfoot, were randomly assigned to one of four groups: Group I, controls; Group II, treatment with corrective orthopaedic shoes; Group III, treatment with a Helfet heel-cup; or Group IV, treatment with a custom-molded plastic insert. All of the patients in Groups II, III, and IV had a minimum of three years of treatment, and ninety-eight patients whose compliance with the protocol was documented completed the study. Analysis of radiographs before treatment and at the most recent follow-up demonstrated a significant improvement in all groups (p less than 0.01), including the controls, and no significant difference between the controls and the treated patients (p greater than 0.4). We concluded that wearing corrective shoes or inserts for three years does not influence the course of flexible flatfoot in children.

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 calculated. 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 discriminant 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.