Trabecular bone in the calcaneus of runners

RESEARCH ARTICLE Trabecular bone in the calcaneus of runners Andrew Best1*, Brigitte Holt1, Karen Troy2, Joseph Hamill3 1 Department of Anthropology, University of Massachusetts, Amherst, Massachusetts, United States of America, 2 Department of Biomedical Engineering, Worcester Polytechnic Institute, Worcester, Massachusetts, United States of America, 3 Department of Kinesiology, University of Massachusetts, Amherst, Massachusetts, United States of America * Abstract a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Best A, Holt B, Troy K, Hamill J (2017) Trabecular bone in the calcaneus of runners. PLoS ONE 12(11): e0188200. https://doi.org/10.1371/ journal.pone.0188200 Editor: Alena Grabowski, University of Colorado Boulder, UNITED STATES Received: February 28, 2017 Accepted: November 2, 2017 Published: November 15, 2017 Copyright: © 2017 Best et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: Joseph Hamill provided funding for participant transportation to and from WPI. Competing interests: The authors have declared that no competing interests exist. Trabecular bone of the human calcaneus is subjected to extreme repetitive forces during endurance running and should adapt in response to this strain. To assess possible bone functional adaptation in the posterior region of the calcaneus, we recruited forefoot-striking runners (n = 6), rearfoot-striking runners (n = 6), and non-runners (n = 6), all males aged 20–41 for this institutionally approved study. Foot strike pattern was confirmed for each runner using a motion capture system. We obtained high resolution peripheral computed tomography scans of the posterior calcaneus for both runners and non-runners. No statistically significant differences were found between runners and nonrunners or forefoot strikers and rearfoot strikers. Mean trabecular thickness and mineral density were greatest in forefoot runners with strong effect sizes (<0.80). Trabecular thickness was positively correlated with weekly running distance (r2 = 0.417, p<0.05) and years running (r2 = 0.339, p<0.05) and negatively correlated with age at onset of running (r2 = 0.515, p<0.01) Trabecular thickness, mineral density and bone volume ratio of nonrunners were highly correlated with body mass (r2 = 0.824, p<0.05) and nonrunners were significantly heavier than runners (p<0.05). Adjusting for body mass revealed significantly thicker trabeculae in the posterior calcaneus of forefoot strikers, likely an artifact of greater running volume and earlier onset of running in this subgroup; thus, individuals with the greatest summative loading stimulus had, after body mass adjustment, the thickest trabeculae. Further study with larger sample sizes is necessary to elucidate the role of footstrike on calcaneal trabecular structure. To our knowledge, intraspecific body mass correlations with measures of trabecular robusticity have not been reported elsewhere. We hypothesize that early adoption of running and years of sustained moderate volume running stimulate bone modeling in trabeculae of the posterior calcaneus. Introduction Trabecular bone forms porous networks in long bone epiphyses, joint articulations, and throughout the internal volumes of the foot bones. Elastic properties of trabecular bone are a function of several characteristics, including the average thickness of each trabecular strut (trabeculae), the number of struts per unit area, the total volume of trabecular bone per unit area PLOS ONE | https://doi.org/10.1371/journal.pone.0188200 November 15, 2017 1 / 14 Trabecular bone in the calcaneus of runners (bone volume fraction: a function of trabecular number and thickness), orientation and connectivity of struts, and mineral density. Density of trabecular bone was first correlated with mechanical properties 50 years ago [1, 2], and by the 1970’s and 1980’s architectural properties were as well [3, 4, 5, 6]. Computed tomography, an x-ray imaging tool, now allows for precise and nondestructive analysis of trabecular architecture. Diederichs et al. [7] found that CTderived trabecular properties are highly predictive of mechanical strength in the calcaneus, particularly bone mineral density (r2 = 60%), bone volume fraction, (r2 = 63%) and average thickness of trabeculae (r2 = 53%). Trabeculae are usually aligned with the principle direction of strain [8], and degree of anisotropy- a measure of trabecular alignment- is positively correlated with mechanical strength in the prevailing direction of trabeculation [9]. The process by which bone adapts to stress was first described by Wolff [10] and others [11] and later refined and termed bone functional adaptation (BFA) by Ruff et al. [12]. While BFA has been debated in its details and mechanisms, it is generally accepted that long bone diaphyseal shape and bending strength respond to loading [12], although some researchers have argued that cross-sectional shape does not reflect loading history (e.g. [13]). Recent work has clearly shown a similar adaptive response in trabecular bone. Animal experiments demonstrate increases in trabecular thickness, mineral density, bone volume fraction, and anisotropy in response to loading [14, 15, 16, 17, 18], and trabecular bone measures are frequently used to infer physical behavior, including locomotor patterns, in hominin and primate skeletal material [19, 20, 21, 22, 23, 24, 25, 26, 27]. Loading-induced increases in trabecular number are seen in young animal experiments [18, 15]; this variable is thought to be malleable early in life and does not comprise a significant part of bone adaptation in adults. However, some evidence suggests that attenuation of trabecular bone volume with ageing differs between the sexes, with women losing trabecular number and men losing trabecular thickness, perhaps leading to increased number of (now thinner) trabeculae in men [28]. The purpose of the present study is to investigate possible trabecular bone adaptation resultant from a common activity that subjects bone to a regime of repetitive and high strain: endurance running. Previous work has identified cortical and trabecular bone adaptation in the tibia of endurance runners [29, 30, 31]. We chose to study the calcaneus, not just because it endures tremendous forces during endurance running but also because its function differs based on foot strike. Foot strike patterns during running include forefoot striking (FFS), where the forefoot makes initial contact; midfoot striking (MFS), where the forefoot and heel make ground contact simultaneously; and rearfoot striking (RFS), where the heel strikes first before the body’s center of mass mov (...truncated)