Understanding Entheses: Bridging the Gap Between Clinical and Anthropological Perspectives

Abstract

An enthesis is the interface where tendon meets bone, providing both muscle anchorage and stress dissipation. Previous anthropological research suggests size and complexity of entheses observable in osteological material, are indicative of the strain magnitude resulting from repetitive muscle contractions during the performance of daily routines. These proposed ''musculoskeletal stress markers'' are routinely incorporated into bioarcheological studies as evidence of general activity patterns past human populations participated in. However, much of how this complex osteotendinous interface develops and responds to mechanical strains is poorly understood. The following review seeks to shed light on this structural enigma by synthesizing current findings in both the clinical and anthropological literature, in the interest of generating new conversations in how entheses respond to contractual forces and the systemic influences (i.e., genetics, hormones), that surround their morphological development. Only once we truly understand the etiology of tendon insertion sites, will the value of enthesial research in reconstructing human behavior be determined. Anat Rec, 295:1239Rec, 295: -1251Rec, 295: , 2012. V C 2012 Wiley Periodicals, Inc. Keywords: musculoskeletal stress markers (MSM); fibrocartilaginous; tendon anatomy; tendon insertion; bone morphology Anthropologists regularly implement bone remodeling principles in response to mechanical loads to infer a causal relationship between muscle tendon insertions and activity levels. Previous research suggests size and complexity of tendon insertions are indicative of strain magnitude resulting from habitual physical activity (Lane, 1887;Kennedy, 1989;Hawkey and Merbs, 1995;Churchill and Morris, 1998;Hawkey, 1998;Steen and Lane, 1998;Stirland, 1998;Wilczak and Kennedy, 1998;Capasso et al., 1999;Weiss, 2003Weiss, , 2004Weiss, , 2007 alOumaoui et al., 2004;Molnar, 2006;Cardoso and Henderson, 2010;Thara et al., 2010;Havelkova et al., 2011). Using both qualitative and quantitative data to assess the expression of insertion morphology along long bone diaphyses, inferences are frequently made regarding both generalized and specific activities past humans participated in throughout their daily lives. Recognition of this potential relationship between mechanical strain and the osteotendinous interface has led many to refer to tendon insertions sites as musculoskeletal stress markers (MSM). However, more empirical analyses exploring the factors responsible for these proposed MSM are needed before we can confidently begin to assess individual behavior and draw population-based inferences from series of skeletal remains. With this lack of understanding in the etiology of periosteal tendon insertion morphology, particularly in the mechanical and structural relationship between soft and hard tissues, this interface should be referred to by the clinical term, enthesis.

Bone microarchitecture at muscle attachment sites: The relationship between macroscopic scores of entheses and their cortical and trabecular microstructural design

“…The authors suggested that "moderate exercise" did not affect the subchondral bone volume at the enthesis, however, the tendon thickness was increased in trained rats (Frizziero et al, 2011). This raises one of the most crucial questions in the field of bone structural adaptation: what is the osteogenic potential of high intermittent stresses vs. habitual moderate stress, i.e., which type and magnitude of stress drives bone structural adaptation (Frost, 2000;Zumwalt, 2006;Ruff et al, 2006;Schlecht, 2012b)? Following this question, another arises as to whether the structural adaptation to muscle loads is different across lifespan?…”

“…Following this question, another arises as to whether the structural adaptation to muscle loads is different across lifespan? Does the entheseal morphology mostly reflect the activities in youth, or do the activities in advanced age also determine the appearance of attachment sites, or are both the case (Ruff et al, 2006;Schlecht, 2012b)? In that sense, it seems too simplistic to just observe the general occupation of an individual when analyzing entheses morphology, and correct interpretations may require a more precise investigation of loading activities.…”

“…Although muscle activity was frequently linked to overall bone cross-sectional geometry (Ruff et al, 2006;Niinim€ aki, 2012;Niinim€ aki et al, 2013), further experimental or simulation studies are necessary to check whether or how mechanical strains derived from the muscle contraction dissipate along the diaphysis, or if they mostly concentrate at the insertion sites (Schlecht, 2012b). To this goal, the comparison of cortical thickness between muscle attachments sites and the surrounding bone might offer some clues.…”

“…Specifically, in order to profoundly understand the relevance of macroscopic scoring of entheses (in the form of entheseal changes), we have to understand several more issues which are important for stress transfer, such as: different histological types of entheses (Currey, 2002;Schlecht, 2012b), the angle of muscle attachment to the bone surface and the pennation angle (Alexander and Vernon, 1975;Thomopoulos et al, 2007), the skeletal region where the enthesis is located, the movement of the enthesis location during growth, caused by constant resorption and new deposition (Hoyte and Enlow, 1966;Wang et al, 2013), the difference in body size, and the embryological development of the entheses. Although differences in body size may also be important for entheseal morphology, we observed in our sample that an individual can present different macroscopic stages at different insertion sites even on the same bone.…”

‘You must keep going’ – Musculoskeletal system stress indicators of prehistoric mobile pastoralists in Western China

“…As alternative causes for EC, inflammatory or metabolic diseases are mentioned, such as seronegative spondyloarthropathies (Resnick and Niwayama, 1995;Freemont, 2002) or diffuse idiopathic skeletal hyperostosis (DISH) (Cammisa et al, 1998;Hannallah et al, 2007;van der Merve et al, 2012). Additionally, a dependency on the type of entheses, fibrous or fibrocartilaginous (Benjamin et al, 1986(Benjamin et al, , 2002Villotte, 2006;Villotte et al, 2010;Schlecht, 2012), a stature dependency on the morphology of entheses (Zumwalt et al, 2000;Weiss, 2003Weiss, , 2004Weiss, , 2007, and particularly age dependency (Kennedy, 1989;Robb, 1998;Weiss, 2003Weiss, , 2004Weiss, , 2007Mariotti et al, 2004;Molnar, 2006;Alves Cardoso and Henderson, 2010;Villotte et al, 2010;Milella et al, 2012) are discussed in many recent articles.…”