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Title: Mechanical Competence and Bone Quality Develop During Skeletal Growth

Journal Article · · Journal of Bone and Mineral Research
DOI:https://doi.org/10.1002/jbmr.3730· OSTI ID:1581747
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  1. Univ. Medical Center, Hamburg (Germany). Dept. of Osteology and Biomechancis
  2. European Synchrotron Radiation Facility (ESRF), Grenoble (France). Beamline ID 10
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Advanced Light Source (ALS), Experimental Systems Group
  4. Univ. of New South Wales (UNSW), Sydney, NSW (Australia). School of Mechanical and Manufacturing Engineering
  5. Univ. Medical Center, Hamburg (Germany). Dept. of Medical Biometry and Epidemiology
  6. Univ. Medical Center, Hamburg (Germany). Dept. of Forensic Medicine
  7. Univ. of California, Berkeley, CA (United States). Dept. of Materials Science and Engineering; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Materials Sciences Division

Bone fracture risk is influenced by bone quality, which encompasses bone's composition as well as its multiscale organization and architecture. Aging and disease deteriorate bone quality, leading to reduced mechanical properties and higher fracture incidence. Largely unexplored is how bone quality and mechanical competence progress during longitudinal bone growth. In this study, human femoral cortical bone was acquired from fetal (n = 1), infantile (n = 3), and 2- to 14-year-old cases (n = 4) at the mid-diaphysis. Bone quality was assessed in terms of bone structure, osteocyte characteristics, mineralization, and collagen orientation. The mechanical properties were investigated by measuring tensile deformation at multiple length scales via synchrotron X-ray diffraction. We find dramatic differences in mechanical resistance with age. Specifically, cortical bone in 2- to 14-year-old cases exhibits a 160% greater stiffness and 83% higher strength than fetal/infantile cases. The higher mechanical resistance of the 2- to 14-year-old cases is associated with advantageous bone quality, specifically higher bone volume fraction, better micronscale organization (woven versus lamellar), and higher mean mineralization compared with fetal/infantile cases. Our study reveals that bone quality is superior after remodeling/modeling processes convert the primary woven bone structure to lamellar bone. In this cohort of female children, the microstructural differences at the femoral diaphysis were apparent between the 1- to 2-year-old cases. Indeed, the lamellar bone in 2- to 14-year-old cases had a superior structural organization (collagen and osteocyte characteristics) and composition for resisting deformation and fracture than fetal/infantile bone. Mechanistically, the changes in bone quality during longitudinal bone growth lead to higher fracture resistance because collagen fibrils are better aligned to resist tensile forces, while elevated mean mineralization reinforces the collagen scaffold. Thus, our results reveal inherent weaknesses of the fetal/infantile skeleton signifying its inferior bone quality. These results have implications for pediatric fracture risk, as bone produced at ossification centers during children's longitudinal bone growth could display similarly weak points.

Research Organization:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22). Scientific User Facilities Division, Washtington, DC (United States); Alexander von Humboldt Foundation, Bonn (Germany); German Research Foundation (DFG), Bonn (Germany)
Grant/Contract Number:
AC02-05CH11231; BU-2562/3‐1/5‐1
OSTI ID:
1581747
Journal Information:
Journal of Bone and Mineral Research, Vol. 34, Issue 8; ISSN 0884-0431
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 35 works
Citation information provided by
Web of Science

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Platelet‐rich fibrin and collagen membrane in the preservation of the alveolar bone: Feasibility of the elemental inorganic composition and scanning electron microscopy analysis journal August 2019
Sexually Dimorphic Influence of Neonatal Antibiotics on Bone journal June 2019
Compositional and mechanical properties of growing cortical bone tissue: a study of the human fibula journal November 2019
Multiscale bone quality analysis in osteoarthritic knee joints reveal a role of the mechanosensory osteocyte network in osteophytes journal January 2020
Compositional and mechanical properties of growing cortical bone tissue: a study of the human fibula text January 2019