Biomechanical implications of mineral content and microstructural variations in cortical bone of horse, elk, and sheep calcanei.
Abstract: Artiodactyl and perissodactyl calcanei have been recently introduced as models for examining bone for mechanically mediated adaptation. We have reported substantial regional variations in cortical bone microstructure and mineral content within the same cross-section of mule deer calcanei. In part, these variations may be adaptations accommodating the customary presence of predominantly tension, compression, and shear strain modes in mutually exclusive cortical locations. Calcanei from skeletally mature horses, elk, and sheep were examined in order to corroborate these previous findings. From each species, one calcaneus was obtained from each of 13 animals. Each bone was cut transversely near mid-shaft into two segments and examined for mineral (ash) content. From each species, an additional segment obtained from each of 7 of the original 13 bones was examined for microstructure using 50x backscattered electron images. Regions examined included the compression (cranial), tension (caudal), and medial and lateral (shear) cortices. Periosteal (P), middle (M), and endosteal (E) regions were also examined separately within the compression and tension cortices. Quantified microstructural parameters included: (1) secondary osteon population density (OPD), (2) fractional area of secondary bone (FASB), (3) porosity, (4) population density of new remodeling events (NRE = resorption spaces and newly forming secondary osteons), and (5) secondary osteon diameter and minimum-to-maximum chord ratio. Results in each species showed variations that are considered to be mechanically important and are similar to those reported in mule deer calcanei. Mineral content data suggest that remodeling activity in the compression, medial, and lateral cortices was occurring at a slower rate than remodeling in the tension cortex. In comparison to the tension cortices, the compression cortices have approximately 6.0% higher mineral content (P < 0.007) and 35% higher OPD (P < 0.01). Additionally, the compression cortices have more nearly perfectly round osteons and lower FASB, porosity, NRE, and osteon diameter (P < 0.05; except for FASB in horse where P = 0.087 and NRE in sheep where P = 0.520). However, patterns of microstructural variations between intracortical regions (P, M, E) are inconsistent when compared to data reported in mule deer calcanei. Microstructural characteristics between the medial and lateral cortices were similar although some significant differences were identified. In general, the microstructure of the medial and lateral cortices differ from the neighboring compression and tension cortices. Differences in mineral content and microstructure between opposing compression and tension cortices of these three species resemble differences previously reported in mule deer calcanei. The majority of the microstructural variations can be explained in the context of strain-magnitude-based rules of Frost's Mechanostat Theory of mechanically induced bone adaptation. These variations may also be strongly influenced by the strain mode predominating in each cortical location. The hypothesis that intracortical material adaptations are correlated with progressive transcortical strain magnitude variations is not supported by the inconsistent transcortical variations in material organization. These interpretations do not preclude the possibility that other specific strain features may contribute to a complex adaptive signal.
Publication Date: 1998-02-12 PubMed ID: 9372164DOI: 10.1002/(SICI)1097-0185(199711)249:3<297::AID-AR1>3.0.CO;2-SGoogle Scholar: Lookup
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- Journal Article
- Research Support
- U.S. Gov't
- Non-P.H.S.
Summary
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This research explores the variations in the microstructure and mineral content of horse, elk, and sheep calcanei (heel bones), particularly in different regions of the bone, to investigate if these variations adapt to mechanical strain. The results confirmed previous findings in mule deer and are significant for understanding how bones adapt to stress.
Study Overview
- The research investigates if the cortical bone microstructure and mineral content in the calcanei of horses, elk, and sheep show variations that could adapt to mechanical stress. The study aims to confirm the findings of similar studies on mule deer.
- In total, calcanei from 13 animals of each species were examined, with each bone being cut into two segments mid-shaft and analyzed for mineral content (ash).
- Different regions of the calcanei, including the compression (cranial), tension (caudal), and medial and lateral (shear) cortices, were examined. The periosteal, middle, and endosteal regions within the compression and tension cortices were also separately examined.
Microstructural Parameters
- The study analyzed a range of microstructural parameters, including the density of secondary osteons, the fractional area of secondary bone, porosity, the population density of new remodeling events, and the diameter and ratio of secondary osteon chords.
- These parameters allow an understanding of how the bone microstructure may adapt to mechanical strain.
Findings
- The findings revealed differences in the rates of bone remodeling between different regions of the calcanei, with those subjected to compression, and medial and lateral forces seeing slower remodeling than those under tension.
- The research also found that the compression cortices had a higher mineral content and secondary osteon population density compared to the tension cortices. The compression cortices were also found to have more round osteons and lower fractional areas of secondary bone, porosity, and new remodeling events.
- The research confirmed the findings of similar studies on mule deer, suggesting the changes identified are mechanically significant and imply a degree of mechanoadaptation.
Implications
- Understanding the biomechanical implications of mineral content and microstructural variations in cortical bone can inform how bones adapt to daily stress.
- The research challenges the hypothesis that intracortical material adaptations relate to progressive variations overall. While the authors acknowledge that some strain features may contribute to the complex adaptive signal, their findings do not back the original hypothesis.
Cite This Article
APA
Skedros JG, Su SC, Bloebaum RD.
(1998).
Biomechanical implications of mineral content and microstructural variations in cortical bone of horse, elk, and sheep calcanei.
Anat Rec, 249(3), 297-316.
https://doi.org/10.1002/(SICI)1097-0185(199711)249:3<297::AID-AR1>3.0.CO;2-S Publication
Researcher Affiliations
- Bone and Joint Research Laboratory, VA Medical Center, Salt Lake City, Utah 84148, USA.
MeSH Terms
- Animals
- Biomechanical Phenomena
- Bone Remodeling / physiology
- Calcaneus / anatomy & histology
- Calcaneus / metabolism
- Calcaneus / physiology
- Calcification, Physiologic / physiology
- Deer / anatomy & histology
- Deer / physiology
- Female
- Horses / anatomy & histology
- Horses / physiology
- Male
- Sheep / anatomy & histology
- Sheep / physiology
Citations
This article has been cited 18 times.- Jannello JM, Chinsamy A. Osteohistology and palaeobiology of giraffids from the Mio-Pliocene Langebaanweg (South Africa).. J Anat 2023 May;242(5):953-971.
- Karydi C, García-Donas JG, Tsiminikaki K, Bonicelli A, Moraitis K, Kranioti EF. Estimation of Age-at-Death Using Cortical Bone Histomorphometry of the Rib and Femur: A Validation Study on a British Population.. Biology (Basel) 2022 Nov 4;11(11).
- Tits A, Plougonven E, Blouin S, Hartmann MA, Kaux JF, Drion P, Fernandez J, van Lenthe GH, Ruffoni D. Local anisotropy in mineralized fibrocartilage and subchondral bone beneath the tendon-bone interface.. Sci Rep 2021 Aug 16;11(1):16534.
- Taguchi T, Lopez MJ. An overview of de novo bone generation in animal models.. J Orthop Res 2021 Jan;39(1):7-21.
- Nguyen JT, Barak MM. Secondary osteon structural heterogeneity between the cranial and caudal cortices of the proximal humerus in white-tailed deer.. J Exp Biol 2020 Jun 11;223(Pt 11).
- Skedros JG, Su SC, Knight AN, Bloebaum RD, Bachus KN. Advancing the deer calcaneus model for bone adaptation studies: ex vivo strains obtained after transecting the tension members suggest an unrecognized important role for shear strains.. J Anat 2019 Jan;234(1):66-82.
- Miszkiewicz JJ, Mahoney P. Histomorphometry and cortical robusticity of the adult human femur.. J Bone Miner Metab 2019 Jan;37(1):90-104.
- Montoya-Sanhueza G, Chinsamy A. Long bone histology of the subterranean rodent Bathyergus suillus (Bathyergidae): ontogenetic pattern of cortical bone thickening.. J Anat 2017 Feb;230(2):203-233.
- Miszkiewicz JJ. Investigating histomorphometric relationships at the human femoral midshaft in a biomechanical context.. J Bone Miner Metab 2016 Mar;34(2):179-92.
- Goldman HM, Hampson NA, Guth JJ, Lin D, Jepsen KJ. Intracortical remodeling parameters are associated with measures of bone robustness.. Anat Rec (Hoboken) 2014 Oct;297(10):1817-28.
- Skedros JG, Knight AN, Farnsworth RW, Bloebaum RD. Do regional modifications in tissue mineral content and microscopic mineralization heterogeneity adapt trabecular bone tracts for habitual bending? Analysis in the context of trabecular architecture of deer calcanei.. J Anat 2012 Mar;220(3):242-55.
- Britz HM, Jokihaara J, Leppänen OV, Järvinen TL, Cooper DM. The effects of immobilization on vascular canal orientation in rat cortical bone.. J Anat 2012 Jan;220(1):67-76.
- Skedros JG, Sybrowsky CL, Anderson WE, Chow F. Relationships between in vivo microdamage and the remarkable regional material and strain heterogeneity of cortical bone of adult deer, elk, sheep and horse calcanei.. J Anat 2011 Dec;219(6):722-33.
- Skedros JG, Clark GC, Sorenson SM, Taylor KW, Qiu S. Analysis of the effect of osteon diameter on the potential relationship of osteocyte lacuna density and osteon wall thickness.. Anat Rec (Hoboken) 2011 Sep;294(9):1472-85.
- Fratzl-Zelman N, Roschger P, Gourrier A, Weber M, Misof BM, Loveridge N, Reeve J, Klaushofer K, Fratzl P. Combination of nanoindentation and quantitative backscattered electron imaging revealed altered bone material properties associated with femoral neck fragility.. Calcif Tissue Int 2009 Oct;85(4):335-43.
- Renders GA, Mulder L, van Ruijven LJ, van Eijden TM. Porosity of human mandibular condylar bone.. J Anat 2007 Mar;210(3):239-48.
- Goldman HM, Thomas CD, Clement JG, Bromage TG. Relationships among microstructural properties of bone at the human midshaft femur.. J Anat 2005 Feb;206(2):127-39.
- Goldman HM, Bromage TG, Boyde A, Thomas CD, Clement JG. Intrapopulation variability in mineralization density at the human femoral mid-shaft.. J Anat 2003 Aug;203(2):243-55.
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