Andrew A. Biewener

Muscle-tendon stresses and elastic energy storage during locomotion in the horse

The stresses acting in muscle-tendon units and ligaments of the forelimb and hindlimb of horses were determined over a range of speed and gait based on recordings of ground reaction forces and limb kinematics. Maximum stresses of 40-50 MPa were calculated to act in several of the principal forelimb (superficial digital flexor (SDF), deep digital flexor (DDF), ulnaris lateralis (UL) and flexor carpi ulnaris/radialis (FCU/R)) and hindlimb tendons (plantaris, DDF) at the fastest galloping speeds recorded (up to 7.4 m s-1). Smaller stresses were found for the gastrocnemius (GAST) tendon (30 MPa) and suspensory ligaments (S-Ligs) (18-25 MPa). Average peak muscle stresses reached 200-240 kPa during galloping. Tendon and muscle stresses increased more steeply with changes of gait and during galloping, than during trotting. Calculations of elastic strain energy storage based on tendon stress showed similar patterns of increase with change of speed and gait, with the greatest contribution to elastic savings by the DDF tendons of the forelimb and hindlimb. In general, the hindlimb contributed two-thirds and the forelimb one-third to overall energy storage. Comparison of tendon elastic energy savings with mechanical work showed a maximum 40% recovery of mechanical work by elastic savings when the horses changed gait from a walk to a slow trot. Percentage of recovery then decreased with increased trotting speed, but increased again with a change of gait to a gallop, reaching 36% recovery at the fastest measured galloping speed (7.4 m s-1). The long length of horse tendons in relation to extremely short pennate muscle fibers suggests a highly specialized design for economical muscle force generation and enhanced elastic energy savings. However, elastic energy savings in terms of percentage of recovery of mechanical work and metabolic energy is less than that observed in wallabies and kangaroos during hopping, but similar to that in humans during running, and greater than that for dogs during trotting and galloping.

Musculoskeletal design in relation to body size

Irrespective of body size and phylogenetic diversity, the skeletal systems of terrestrial mammals are built of tissue components having similar mechanical properties and material organization. Because of scale effects on skeletal form, therefore, larger mammals increase the effective mechanical advantage of their limbs to decrease mass-specific forces associated with the support of gravitational loads imposed during locomotion to maintain a similar safety factor. Larger animals accomplish this by adopting a more upright posture while running, which aligns their limb joints more closely with the resultant ground reaction force, thereby decreasing the mass-specific force that their muscles must generate to support externally applied joint moments. As a result, peak (compressive) bone stresses determined from in vivo bone strain recordings and force platform and kinematic analyses of the limb generally range from -40 to -80 MPa (mean: -55 +/- 23 MPa), corresponding to a safety factor to compressive bone failure of about three to four. The decrease in mass-specific muscle force indicates that the maximum stresses developed in limb muscles of different sized species are also similar at equivalent levels of performance. Stresses developed in the midshafts of most long bones are primarily the result of bending, often engendered by axial forces transmitted about the bones longitudinal curvature. The consistency of bending-induced skeletal strain over a range of physical activity and the associated expense of increased strain magnitude that this form of loading incurs suggest that functional strain patterns developed through bending may be a desirable architectural objective of most long bones. Alteration of a bones normal functional strain distribution, therefore, is likely a key factor underlying adaptive remodeling in response to changes in mechanical loading.

Safety Factors in Bone Strength

SummaryFunctionalin vivo strain data are examined in relation to bone material properties in an attempt to evaluate the relative importance of osteoporotic bone loss versus fatigue damage accumulation as factors underlying clinical bone fragility. Specifically, does the skeleton have a sufficiently large safety factor (ratio of bone failure strain to maximum functional strain) to require that fatigue damage accumulation is the main factor contributing to increased risk of fracture in the elderly? Existing methods limitin vivo strain measurements to the surfaces of cortical bone. Peak principal compressive strains measured at cortical sites during strenuous activity in various mammalian and avian species range from −1700 to −5200 με, averaging - 2500 με (−0.0025 strain). Much of this threefold variation reflects differences in the intensity of physical activity, as well as differences among species and bones that have been studied. Peak strains can also vary as much as tenfold at different cortical sites within the same bone. No data exist for cortical bone strain during strenuous activity in humans, but it is likely that human bones experience a similar range of peak strain levels. Compact bone fails in longitudinal compression at strains as high as −14,000 to −21,000 με, but begins to yield at strains between −6000 and −8000 με. Given that yielding involves rapid accumulation of microdamage within the bone, it seems prudent to base skeletal safety factors on the yield strain, rather than the ultimate failure strain of bone tissue. Safety factors to yield failure therefore range from 1.4 to 4.1. This safety factor range is likely diminished further by age-related increases in mineralization and secondary remodeling that reduce the strength and energy-absorbing capacity of bone. Although no one safety factor applies to all skeletal sites within an individual, it seems clear that osteoporotic bone loss of 40 to 50% of normal constitutes a causative factor of clinical bone fragility, particularly if bone loss is high at sites of high functional strain. Theoretical consideration of the statistical distribution of bone strength in relation to functional loading events within a population over a lifetime of use further supports this interpretation, by indicating an increased probability of fracture with increasing age. Fatigue damage accumulation will serve to exacerbate these trends. Bone loss and fatigue damage accumulation therefore, should be viewed as mutually reinforcing agents of bone fragility. Improved correlation of peak functional strain patterns with localized bone loss and bone turnover dynamics at sites of high fracture risk, together with assessment of microdamage, is needed to resolve the relative contribution of these factors to osteoporotic bone fragility.

Bone modeling during growth: dynamic strain equilibrium in the chick tibiotarsus.

SummaryBone loading was quantified, usingin vivo strain recordings, in the tibiotarsus of growing chicks at 4,8, 12, and 17 weeks of age. The animals were exercised on a treadmil at 35% of their maximum running speed for 15 minutes/day.In vivo bone strains were recorded at six sites on the tibiotarsus. Percentages of the bones length and a percentage of top running speed were used to define functionally equivalent sites on the bone, and a consistent exercise level over the period of growth was studied. The pattern of bone strain defined in terms of strain magnitude, sign, and orientation remained unchanged from 4–17 weeks of age, a period when bone mass and length increased 10-fold and threefold, respectively. Our findings support the hypothesis that bones model (and remodel) during growth to achieve and maintain a similar distribution of dynamic strains at functionally equivalent sites. Because strain magnitude and sign (tensile versus compressive) differed among recording sites, these data also suggest that cellular responses to strain-mediated stimuli differ from site to site within a bone.

Gravity, posture and locomotion in primates

An animals physical environment greatly influences its form and function. Therefore, it is not surprising to expect that forces generated by Earths gravity would exert similar mechanical constraints and yield similar principles of structural design and biomechanical function for most terrestrial species. This is more the case when groups of animals are constructed of tissues having similar mechanical properties. As reflected by its title, the goal of this book, and the 1986 symposium upon which it is based (sponsored by the Centre National de la Recherche Scientifique, France), is to identify common themes underlying the biomechanics of locomotor support in primates, to clarify those aspects in which primates may differ from other mammalian species, and to evaluate the usefulness of primates as model species for investigating the influence of gravity on locomotor systems more generally. The book reflects two decades of research in the fields of physical anthropology and biomechanics, which have benefited from the development of new technologies for carrying out important experimental studies of animal locomotion. The success of an edited symposium volume, such as this, depends ultimately on the cohesion and synthesis of the concepts and data presented by the various contributors. Overall, the book makes a fairly good attempt to present a broad, critical perspective of the many topics that are covered and to outline future directions for research. However, it suffers from chapters that are uneven in the effectiveness with which they achieve these goals. Primates are shown to follow fairly general patterns of locomotor design and function, on the one hand (chapters by Alexander, Jungers, and Preuschoft); yet, at the same time, considerable variation is observed among different primate species (Jouffrey et al., Berge and Yamazaki), as well as between primates and humans (Kimura) and primates and mammals (De-