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

Abstract

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.

Understanding Entheses: Bridging the Gap Between Clinical and Anthropological Perspectives

“…Activity reconstructions using entheses profiles are frequently conducted using subjective macroscopic methods that may be irrelevant and/or inaccurate in assessing enthesis morphology (Bryant and Seymour, 1990;Robb, 1998;Wilczak, 1998;Knü sel, 2002). Further concerns arise with the regular failure to account for potential nuances that may affect entheses response to applied load, such as body mass, age, genetic precursors, skeletal maturity, and muscle contractile rates (Stirland, 1998;Wilczak, 1998;Zumwalt, 2006). Moreover, previous studies frequently lack explicit biological justification for why particular parameters are initially chosen for profile assessment (Robb, 1998;Wilczak, 1998;Zumwalt, 2005Zumwalt, , 2006.…”

“…This technological progression in the assessment of entheses may allow for statistical correlations between skeletal morphology and activity, potentially allowing for the delineation of more meaningful macroscopic methodology in accounting for morphological development. There continues to be a lack of sound research exploring the etiology of tendon insertion scarification, and whether it is truly indicative, or at least primarily representative, of habitually applied mechanical loads (Robb, 1998;Wilczak, 1998;Jurmain, 1999;Schlecht, 2004;Pearson and Buikstra, 2006;Zumwalt, 2006;Schlecht, 2008;Weiss et al, 2012).…”

“…However, few investigators attempting behavior reconstructions question the lack of direct evidence for such a relationship. Several researchers note that most activityrelated studies fail to consider other mechanical and systemic influences on osteotendinous responsiveness to load, such as body mass or genetics or both (Robb, 1998;Wilczak, 1998;Weiss, 2003;Schlecht, 2004;Zumwalt, 2006;Schlecht, 2008). Additionally, previous studies rarely account for muscle activity intensity, an individual's skeletal maturity, or the time frame in which a proposed activity may have taken place during one's lifetime.…”

“…On the basis of the findings of Chamay and Tschantz (1972) and Woo et al (1981), many anthropologists propose that repetitive muscular activity strengthens the tendon-anchoring mechanism as bone cell proliferation increases via capillary expansion, stimulating periosteal modeling and remodeling activity (Torg et al, 1972;Hawkey and Merbs, 1995;Zumwalt, 2006). Weiss (2003Weiss ( , 2004Weiss ( , 2007 has found statistically significant correlations between the robusticity, geometrical properties, and MSMs of long bones, suggesting that tendon insertion development is at least partially dependent on mechanical influences, since it is well established that cross-sectional structure is indicative of such a relationship (Larsen and Ruff, 1990;Ruff et al, 2006).…”

“…Pearson and Buikstra (2006) attribute this to a lack of interest among clinicians since osteophyte formation rarely has a detrimental effect in living humans. To date, Ann Zumwalt (2006) has conducted the most thorough study assessing longitudinal development of entheses in exercised sheep. However, there remains a need for additional well designed experiments assessing enthesial development and what, if any, contribution these markers have in occupation-based research.…”