Structural and mechanical adaptation of immature bone to strenuous exercise

Matsuda, Junji; Zernicke, Ronald F.; Vailas, A. C.; Pedrini, V.; Pedrini-Mille, A.; Maynard, Jerry A.

doi:10.1152/jappl.1986.60.6.2028

Cited by 93 publications

(36 citation statements)

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“…Younger animals (4-6 weeks old) continuously ran for 30 minutes, older animals 45-60 minutes. Details of the exercise program are reported elsewhere (15). Fumarase activity was significantly increased in the proximal lateral gastrocnemius of runners, indicating that our exercise program was producing the effects of endurance training (15).…”

Section: Methodsmentioning

confidence: 93%

Response of immature chicken meniscus to strenuous exercise: Biochemical studies of proteoglycan and collagen

Pedrini-Mille

Pedrini

Maynard

et al. 1988

Journal Orthopaedic Research

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Male white Leghorn chickens were exercised on a treadmill at 70-80% of their maximal oxygen consumption starting at 4 weeks and continuing up to 20 weeks of age. The effect of the strenuous exercise regime on the extracellular matrix of menisci was followed through studies of proteoglycans and collagen. Avian menisci contain type I collagen, chondroitin sulfate proteoglycans, which increase with age in amount and degree of aggregation, and dermatan sulfate proteoglycans, which decrease with age. Five weeks of exercise cause a premature decrease of dermatan sulfate proteoglycans, while the chondroitin sulfate-containing molecules become significantly more aggregated than those of the tissue of age-matched controls. Strenuous exercise also causes a significant decrease in the number of pyridinoline crosslinks per mole of collagen in the menisci of young runners. The exercise-induced changes of proteoglycan and collagen occur only during the period of active growth, and all parameters return to normal when the animals reach skeletal maturity. The early proteoglycan aggregation and dermatan sulfate decrease induced by exercise are probably an adaptation to the increased loading. Although the mechanism by which strenuous exercise reduces or delays the formation of collagen pyridinoline crosslinks in menisci of skeletally immature animals is unknown, their decrease could negatively affect the mechanical properties of the tissue during the period of active growth.

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Section: Methodsmentioning

confidence: 93%

Response of immature chicken meniscus to strenuous exercise: Biochemical studies of proteoglycan and collagen

Pedrini-Mille

Pedrini

Maynard

et al. 1988

Journal Orthopaedic Research

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“…Additionally, the degree to which attachment sites respond to external loads is poorly understood and certainly more complex than most interpretations of their morphology would suggest. Bone does not respond to all stimuli, and when it does, it responds differently in different conditions (Burr et al, 2002;Cullen et al, 2001;Currey, 2002;Judex and Zernicke, 2000b;Kontulainen, 2002;Lanyon et al, 1982;Matsuda et al, 1986;McLeod et al, 1998;Robling et al, 2000;Rubin and Lanyon, 1985;Turner, 1998;Turner et al, 1995a;Zernicke et al, 2001). Muscle attachments are sometimes, but not always, associated with osteogenesis at their points of attachment, and sometimes a muscle may attach to an area that is both depositional and resorptive in different locations at the same time (Hoyte and Enlow, 1966).…”

Section: Introductionmentioning

confidence: 99%

The effect of endurance exercise on the morphology of muscle attachment sites

Zumwalt

2006

Journal of Experimental Biology

138

188

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SUMMARY The morphology of muscle attachment sites, or entheses, has long been assumed to directly reflect in vivo muscle activity. The purpose of this study is to examine whether variations in muscle activity that are within normal physiological limits are reflected in variations in external attachment site morphology. This study tests the hypothesis that increased muscle activity (magnitude, number and frequency of loading cycles) results in the hypertrophy of muscle attachment sites. The attachment sites of six limb muscles and one muscle of mastication (control) in mature female sheep were measured and compared in exercised (weighted treadmill running for 1 h per day for 90 days) and sedentary control animals. Attachment site surface morphology was assessed by quantifying the size (3D surface area) and complexity (fractal dimension parallel and perpendicular to soft tissue attachment) of the surfaces. The results of this study demonstrate no effect of the exercise treatment used in this experiment on any measure of enthesis morphology. Potential explanations for the lack of exercise response include the mature age of the animals, inappropriate stimulus type for inducing morphological change, or failure to surpass a hypothetical threshold of load for inducing morphological change. However, further tests also demonstrate no relationship between muscle size and either attachment site size or complexity in sedentary control animals. The results of this study indicate that the attachment site morphological parameters measured in this study do not reflect muscle size or activity. In spite of decades of assumption otherwise, there appears to be no direct causal relationship between muscle size or activity and attachment site morphology, and reconstructions of behavior based on these features should be viewed with caution.

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“…Second, it is unclear how the rate and distribution of bone deposition is affected along the proximodistal axis. Data from previous investigations are somewhat contradictory (Woo et al, 1981;Matsuda et al, 1986;Lieberman et al, 2003;O'Neill and Ruff, 2004;Drapeau and Streeter, 2006), but indicate that bone may primarily be added periosteally to increase resistance to bending with new growth diminishing distally along the proximodistal axis (Lieberman et al, 2003). By adding bone periosteally and hence farther from the bending axis, the reduction of tissue strains from bending may be maximized.…”

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confidence: 99%

Bone modeling response to voluntary exercise in the hindlimb of mice

Plochocki

Rivera

Zhang

et al. 2007

Journal of Morphology

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The functional adaptation of juvenile mammalian limb bone to mechanical loading is necessary to maintain bone strength. Diaphyseal size and shape are modified during growth through the process of bone modeling. Although bone modeling is a well-documented response to increased mechanical stress on growing diaphyseal bone, the effect of proximodistal location on bone modeling remains unclear. Distal limb elements in cursorial mammals are longer and thinner, most likely to conserve energy during locomotion because they require less energy to move. Therefore, distal elements are hypothesized to experience greater mechanical loading during locomotion and may be expected to exhibit a greater modeling response to exercise. In this study, histomorphometric comparisons are made between femora and tibiae of mice treated with voluntary exercise and a control group (N = 20). We find that femora of exercised mice exhibit both greater bone growth rates and growth areas than do controls (P < 0.05). The femora of exercised mice also have significantly greater cortical area, bending rigidity, and torsional rigidity (P < 0.05), although bending and torsional rigidity are comparable when standardized by bone length. Histomorphometric and cross-section geometric properties of the tibial midshaft of exercised and control mice did not differ significantly, although tibial length was significantly greater in exercised mice (P < 0.05). Femora of exercised mice were able to adapt to increased mechanical loading through increases in compressive, bending, and torsional rigidity. No such adaptations were found in the tibia. It is unclear if this is a biomechanical adaptation to greater stress in proximal elements or if distal elements are ontogenetically constrained in a tradeoff of bone strength of distal elements for bioenergetic efficiency during locomotion.

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Structural and mechanical adaptation of immature bone to strenuous exercise

Cited by 93 publications

References 0 publications

Response of immature chicken meniscus to strenuous exercise: Biochemical studies of proteoglycan and collagen

Response of immature chicken meniscus to strenuous exercise: Biochemical studies of proteoglycan and collagen

The effect of endurance exercise on the morphology of muscle attachment sites

Bone modeling response to voluntary exercise in the hindlimb of mice

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