The Effect of Endurance Exercise on the Morphology of Muscle Attachment Sites: An Experimental Study in Sheep (Ovis Aries)

The morphology of muscle attachment sites, or entheses, has long been assumed to directly reflect in vivo muscle activity. However, upon close consideration it becomes obvious that this idea is likely an over-simplification of what appears to be a complex functional relationship. It is clear from previous studies that muscle load does not always induce hypertrophy, and skeletal resorption has been reported at actively loaded attachment sites. This study is the first to document the relationship between known muscle load and the morphology and mineralization rates of the relevant attachment sites.

This study tests a number of hypotheses that are based on the idea that an increase in the number and magnitude of applied muscular forcfs will hypertrophy the muscles’ attachment sites in a number of ways. The size (2D area, 3D area and volume), rugosity (3D area: 2D area ratio and fractal dimension) and mineral apposition rates (MAR) at the sites of attachment are all predicted to increase in response to the increased load. 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 one hour/day for 90 days) and sedentary control animals.

Results of this study demonstrate no response to the exercise treatment used in this experiment in any measure of enthesis morphology or in MAR. Further tests examined the idea that attachment sites reflect differences in relative lifetime stress levels, but found no significant differences between such entheses. These results indicate that the attachment site parameters measured in this study do not reflect the forces produced by muscle contractions. Potential explanations of these surprising results include the mature age of the animals, inadequate experiment length, and inappropriate load for inducing morphological change. The results of this study reinforce the idea that the relationship between in vivo loads and attachment site morphology is not as straightforward as has long been assumed. Ideas for future studies that may help further elucidate this relationship are discussed

Year	Entry
2002	Currey JD. Bones: Structure and Mechanics. Princeton, NJ: Princeton University Press; 2002.
1998	Benjamin M, Ralphs JR. Fibrocartilage in tendons and ligaments: an adaptation to compressive load. J Anat. 1998;193(4):481-494.
1978	Uhthoff HK, Jaworski ZF. Bone loss in response to long-term immobilisation. J Bone Joint Surg. August 1978;60B(3):420-429.
1987	Frost HM. The mechanostat: a proposed pathogenic mechanism of osteoporoses and the bone mass effects of mechanical and nonmechanical agents. Bone Miner. April 1987;2(2):73-85.
1992	Rubin CT, Bain SD, McLeod KJ. Suppression of the osteogenic response in the aging skeleton. Calcif Tiss Int. April 1992;50(4):306-313.
1994	Raab-Cullen DM, Thiede MA, Petersen DN, Kimmel DB, Recker RR. Mechanical loading stimulates rapid changes in periosteal gene expression. Calcif Tiss Int. December 1994;55(6):473-478.
1892	Wolff J. Das Gesetz der Transformation der Knochen. Berlin: Hirschwald; 1892.
1969	Frost HM. Tetracycline-based histological analysis of bone remodeling. Calcif Tiss Res. 1969;3(1):211-237.
1998	Martin RB, Burr DB, Sharkey NA. Skeletal Tissue Mechanics. New York, NY: Springer-Verlag; 1998.
1991	Bertram JEA, Swartz SM. The “law of bone transformation”: a case of crying Wolff? Biol Rev. August 1991;66(3):245-273.
2003	Lieberman DE, Pearson OM, Polk JD, Demes B, Crompton AW. Optimization of bone growth and remodeling in response to loading in tapered mammalian limbs. J Exp Biol. September 15, 2003;206(18):3125-3138.
1997	Judex S, Gross TS, Zernicke RF. Strain gradients correlate with sites of exercise‐induced bone‐forming surfaces in the adult skeleton. J Bone Miner Res. October 1997;12(10):1737-1745.
1995	Turner CH, Owan I, Takano Y. Mechanotransduction in bone: role of strain rate. Am J Physiol Endocrinol Metab. September 1995;269(3):E438-E442.
1981	Woo SL-Y, Gomez MA, Amiel D, Ritter MA, Gelberman RH, Akeson WH. The effects of exercise on the biomechanical and biochemical properties of swine digital flexor tendons. J Biomech Eng. February 1981;103(1):51-56.
1995	Matyas JR, Anton MG, Shrive NG, Frank CB. Stress governs tissue phenotype at the femoral insertion of the rabbit MCL. J Biomech. February 1995;28(2):147-157.
1970	Cooper RR, Misol S. Tendon and ligament insertion: a light and electron microscopic study. J Bone Joint Surg. January 1970;52A(1):1-20, 170.
1995	Newman E, Turner AS, Wark JD. The potential of sheep for the study of osteopenia: current status and comparison with other animal models. Bone. April 1, 1995;16(4)(suppl):S277-S284.
2004	Pearson OM, Lieberman DE. The aging of Wolff's “law”: ontogeny and responses to mechanical loading in cortical bone. Yearb Phys Anthropol. 2004;47:63-99.
2000	Judex S, Zernicke RF. High-impact exercise and growing bone: relation between high strain rates and enhanced bone formation. J Appl Physiol. June 2000;88(6):2183-2191.
1982	Lanyon LE, Goodship AE, Pye CJ, MacFie JH. Mechanically adaptive bone remodelling. J Biomech. 1982;15(3):141-154.
2001	Hsieh Y, Robling AG, Ambrosius WT, Burr DB, Turner CH. Mechanical loading of diaphyseal bone in vivo: the strain threshold for an osteogenic response varies with location. J Bone Miner Res. December 2001;16(10):2291-2297.
1995	Hillam RA, Skerry TM. Inhibition of bone resorption and stimulation of formation by mechanical loading of the modeling rat ulna in vivo. J Bone Miner Res. June 1995;10(5):683-689.
2004	Warden SJ, Turner CH. Mechanotransduction in the cortical bone is most efficient at loading frequencies of 5–10 hz. Bone. February 2004;34(2):261-270.
2000	Robling AG, Burr DB, Turner CH. Partitioning a daily mechanical stimulus into discrete loading bouts improves the osteogenic response to loading. J Bone Miner Res. August 2000;15(8):1596-1602.
1985	Rubin CT, Lanyon LE. Regulation of bone mass by mechanical strain magnitude. Calcif Tiss Int. 1985;37(4):411-417.
1984	Rubin CT, Lanyon LE. Regulation of bone formation by applied dynamic loads. J Bone Joint Surg. March 1984;66A(3):397-402.
2002	Burr DB, Robling AG, Turner CH. Effects of biomechanical stress on bones in animals. Bone. May 2002;30(5):781-786.
1995	Turner CH, Takano Y, Owan I. Aging changes mechanical loading thresholds for bone formation in rats. J Bone Miner Res. October 1995;10(10):1544-1549.
1981	Woo SL-Y, Kuei SC, Amiel D, Gomez MA, Hayes WC, White FC, Akeson WH. The effect of prolonged physical training on the properties of long bone: a study of Wolff's Law. J Bone Joint Surg. June 1981;63A(5):780-787.
1994	Forwood MR, Turner CH. The response of rat tibiae to incremental bouts of mechanical loading: a quantum concept for bone formation. Bone. November–December 1994;15(6):603.
1998	Turner CH. Three rules for bone adaptation to mechanical stimuli. Bone. November 1998;23(5):399-407.
1997	Mosley JR, March BM, Lynch J, Lanyon LE. Strain magnitude related changes in whole bone architecture in growing rats. Bone. March 1997;20(3):191-198.
1998	Mosley JR, Lanyon LE. Strain rate as a controlling influence on adaptive modeling in response to dynamic loading of the ulna in growing male rats. Bone. October 1998;23(4):313-318.
2002	Robling AG, Hinant FM, Burr DB, Turner CH. Improved bone structure and strength after long‐term mechanical loading is greatest if loading is separated into short bouts. J Bone Miner Res. August 2002;17(8):1545-1554.
2002	Robling AG, Hinant FM, Burr DB, Turner CH. Shorter, more frequent mechanical loading sessions enhance bone mass. Med Sci Sports Exer. February 2002;34(2):196-202.

Year

Entry

2002

Currey JD. Bones: Structure and Mechanics. Princeton, NJ: Princeton University Press; 2002.

1998

Benjamin M, Ralphs JR. Fibrocartilage in tendons and ligaments: an adaptation to compressive load. J Anat. 1998;193(4):481-494.

1978

Uhthoff HK, Jaworski ZF. Bone loss in response to long-term immobilisation. J Bone Joint Surg. August 1978;60B(3):420-429.

1987

Frost HM. The mechanostat: a proposed pathogenic mechanism of osteoporoses and the bone mass effects of mechanical and nonmechanical agents. Bone Miner. April 1987;2(2):73-85.

1992

Rubin CT, Bain SD, McLeod KJ. Suppression of the osteogenic response in the aging skeleton. Calcif Tiss Int. April 1992;50(4):306-313.