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.
The femoral enthesis of the human anterior cruciate ligament (ACL) is known to be more susceptible to injury than the tibial enthesis. To determine whether anatomic differences might help explain this difference, we quantified the microscopic appearance of both entheses in 15 unembalmed knee specimens using light microscopy, toluidine blue stain and image analysis. The amount of calcified fibrocartilage and uncalcified fibrocartilage, and the ligament entheseal attachment angle were then compared between the femoral and tibial entheses via linear mixed-effects models. The results showed marked differences in anatomy between the two entheses. The femoral enthesis exhibited a 3.9-fold more acute ligament attachment angle than the tibial enthesis (p < 0.001), a 43% greater calcified fibrocartilage tissue area (p < 0.001), and a 226% greater uncalcified fibrocartilage depth (p < 0.001), with the latter differences being particularly pronounced in the central region. We conclude that the ACL femoral enthesis has more fibrocartilage and a more acute ligament attachment angle than the tibial enthesis, which provides insight into why it is more vulnerable to failure.
Background: Nearly three-quarters of anterior cruciate ligament (ACL) injuries occur as “noncontact” failures from routine athletic maneuvers. Recent in vitro studies revealed that repetitive strenuous submaximal knee loading known to especially strain the ACL can lead to its fatigue failure, often at the ACL femoral enthesis. Hypothesis: ACL failure can be caused by accumulated tissue fatigue damage: specifically, chemical and structural evidence of this fatigue process will be found at the femoral enthesis of ACLs from tested cadaveric knees, as well as in ACL explants removed from patients undergoing ACL reconstruction. Study Design: Controlled laboratory study. Methods: One knee from each of 7 pairs of adult cadaveric knees were repetitively loaded under 4 times–body weight simulated pivot landings known to strain the ACL submaximally while the contralateral, unloaded knee was used as a comparison. The chemical and structural changes associated with this repetitive loading were characterized at the ACL femoral enthesis at multiple hierarchical collagen levels by employing atomic force microscopy (AFM), AFM–infrared spectroscopy, molecular targeting with a fluorescently labeled collagen hybridizing peptide, and second harmonic imaging microscopy. Explants from ACL femoral entheses from the injured knee of 5 patients with noncontact ACL failure were also characterized via similar methods. Results: AFM–infrared spectroscopy and collagen hybridizing peptide binding indicate that the characteristic molecular damage was an unraveling of the collagen molecular triple helix. AFM detected disruption of collagen fibrils in the forms of reduced topographical surface thickness and the induction of ~30- to 100-nm voids in the collagen fibril matrix for mechanically tested samples. Second harmonic imaging microscopy detected the induction of ~10- to 100-µm regions where the noncentrosymmetric structure of collagen had been disrupted. These mechanically induced changes, ranging from molecular to microscale disruption of normal collagen structure, represent a previously unreported aspect of tissue fatigue damage in noncontact ACL failure. Confirmatory evidence came from the explants of 5 patients undergoing ACL reconstruction, which exhibited the same pattern of molecular, nanoscale, and microscale structural damage detected in the mechanically tested cadaveric samples. Conclusion: The authors found evidence of accumulated damage to collagen fibrils and fibers at the ACL femoral enthesis at the time of surgery for noncontact ACL failure. This tissue damage was similar to that found in donor knees subjected in vitro to repetitive 4 times–body weight impulsive 3-dimensional loading known to cause a fatigue failure of the ACL. Clinical Relevance: These findings suggest that some ACL injuries may be due to an exacerbation of preexisting hierarchical tissue damage from activities known to place larger-than-normal loads on the ACL. Too rapid an increase in these activities could cause ACL tissue damage to accumulate across length scales, thereby affecting ACL structural integrity before it has time to repair. Prevention necessitates an understanding of how ACL loading magnitude and frequency are anabolic, neutral, or catabolic to the ligament.
Understanding the functional integration of skeletal traits and how they naturally vary within and across populations will benefit assessments of functional adaptation directed towards interpreting bone stiffness in contemporary and past humans. Moreover, investigating how these traits intraskeletally vary will guide us closer towards predicting fragility from a single skeletal site. Using an osteological collection of 115 young adult male and female African-Americans, we assessed the functional relationship between bone robustness (i.e. total area/length), cortical tissue mineral density (Ct.TMD), and cortical area (Ct.Ar) for the upper and lower limbs. All long bones demonstrated significant trait covariance (p < 0.005) independent of body size, with slender bones having 25-50% less Ct.Ar and 5-8% higher Ct.TMD compared to robust bones. Robustness statistically explained 10.2-28% of Ct.TMD and 26.6-64.6% of Ct.Ar within male and female skeletal elements. This covariance is systemic throughout the skeleton, with either the slender or robust phenotype consistently represented within all long bones for each individual. These findings suggest that each person attains a unique trait set by adulthood that is both predictable by robustness and partially independent of environmental influences. The variation in these functionally integrated traits allows for the maximization of tissue stiffness and minimization of mass so that regardless of which phenotype is present, a given bone is reasonably stiff and strong, and sufficiently adapted to perform routine, habitual loading activities. Covariation intrinsic to functional adaptation suggests that whole bone stiffness depends upon particular sets of traits acquired during growth, presumably through differing levels of cellular activity, resulting in differing tissue morphology and composition. The outcomes of this intraskeletal examination of robustness and its correlates may have significant value in our progression towards improved clinical assessments of bone strength and fragility.
Traits of the skeletal system are coordinately adjusted to establish mechanical homeostasis in response to genetic and environmental factors. Prior work demonstrated that this `complex adaptive' process is not perfect, revealing a two-fold difference in whole bone stiffness of the tibia across a population. Robustness (specifically, total cross-sectional area relative to length) varies widely across skeletal sites and between sexes. However, it is unknown whether the natural variation in whole bone stiffness and strength also varies across skeletal sites and between men and women. We tested the hypotheses that: 1) all major long bones of the appendicular skeleton demonstrate inherent, systemic constraints in the degree to which morphological and compositional traits can be adjusted for a given robustness; and 2) these traits covary in a predictable manner independent of body size and robustness. We assessed the functional relationships among robustness, cortical area (Ct.Ar), cortical tissue mineral density (Ct.TMD), and bone strength index (BSI) across the long bones of the upper and lower limbs of 115 adult men and women. All bones showed a significant (p < 0.001) positive regression between BSI and robustness after adjusting for body size, with slender bones being 1.7–2.3 times less stiff and strong in men and 1.3–2.8 times less stiff and strong in women compared to robust bones. Our findings are the first to document the natural inter-individual variation in whole bone stiffness and strength that exist within populations and that is predictable based on skeletal robustness for all major long bones. Documenting and further understanding this natural variation in strength may be critical for differentially diagnosing and treating skeletal fragility.
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