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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
 [1];  [1];  [1];  [1];  [2];  [3];  [4];  [5];  [2];  [6]; ORCiD logo [1];  [7]; ORCiD logo [1]
  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 Laboratory (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: 37 works
Citation information provided by
Web of Science

References (59)

Beginning endochondral ossification in embryonic mouse radii journal January 1973
Tibial compression is anabolic in the adult mouse skeleton despite reduced responsiveness with aging journal September 2011
The genetics of bone mass and susceptibility to bone diseases journal April 2016
Collagen orientation in compact bone: II. Distribution of lamellae in the whole of the human femoral shaft with reference to its mechanical properties journal January 1984
Muscle force regulates bone shaping for optimal load-bearing capacity during embryogenesis journal July 2011
Vitamin D Deficiency Induces Early Signs of Aging in Human Bone, Increasing the Risk of Fracture journal July 2013
Mechanical adaptability of the Bouligand-type structure in natural dermal armour journal October 2013
Modifications to Nano- and Microstructural Quality and the Effects on Mechanical Integrity in Paget's Disease of Bone: NANO/MICROSTRUCTURE EFFECTS ON MECHANICAL INTEGRITY IN PDB journal January 2015
The quantitative study of the orientation of collagen in compact bone slices journal January 1990
A SAXS/WAXS/GISAXS Beamline with Multilayer Monochromator journal October 2010
Aging and Bone journal October 2010
The Development of Metaphyseal Cortex-Implications for Distal Radius Fractures During Growth journal August 2001
Spatial and temporal variations of mechanical properties and mineral content of the external callus during bone healing journal August 2009
Age-related changes in the plasticity and toughness of human cortical bone at multiple length scales journal August 2011
Spiral twisting of fiber orientation inside bone lamellae journal March 2006
Human fetal bone development: histomorphometric evaluation of the proximal femoral metaphysis journal June 2002
The epidemiology of fractures in England journal February 2008
Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture journal July 2005
Bone histomorphometry: a concise review for endocrinologists and clinicians journal March 2010
Aging diminishes lamellar and woven bone formation induced by tibial compression in adult C57BL/6 journal August 2014
Intracortical remodelling and porosity in the distal radius and post-mortem femurs of women: a cross-sectional study journal May 2010
Trends in trabecular architecture and bone mineral density distribution in 152 individuals aged 30–90years journal September 2014
Normative data on mineralization density distribution in iliac bone biopsies of children, adolescents and young adults journal June 2009
Bone Biology journal January 1995
Size-Corrected BMD Decreases During Peak Linear Growth: Implications for Fracture Incidence During Adolescence journal December 2006
Lehre und Forschung an Verstorbenen: „Mortui vivos docent“ journal March 2016
Nika : software for two-dimensional data reduction journal March 2012
Mechanical and structural properties of bone in non-critical and critical healing in rat journal September 2014
Dilatational band formation in bone journal November 2012
The true toughness of human cortical bone measured with realistically short cracks journal June 2008
How Tough Is Brittle Bone? Investigating Osteogenesis Imperfecta in Mouse Bone: FRACTURE TOUGHNESS OF OIM BONE journal May 2014
A study of the relationship between mineral content and mechanical properties of turkey gastrocnemius tendon journal June 1995
Decreasing incidence of fractures in children: An epidemiological analysis of 1,673 fractures in Malmö, Sweden, 1993–1994 journal January 1999
The fracture mechanics of human bone: influence of disease and treatment journal September 2015
Bone as a Structural Material journal April 2015
Epidemiology of fractures in children and adolescents: Increased incidence over the past decade: a population-based study from northern Sweden journal February 2010
Preferred collagen fiber orientation in the human mid-shaft femur journal April 2003
Evidence of structural and material adaptation to specific strain features in cortical bone journal September 1996
Mechanistic fracture criteria for the failure of human cortical bone journal February 2003
Epidemiology of Childhood Fractures in Britain: A Study Using the General Practice Research Database journal September 2004
Challenges in the Acquisition and Analysis of Bone Microstructure During Growth journal November 2016
Nanoscale Deformation Mechanisms in Bone journal October 2005
Bone histomorphometry and bone quality journal May 2009
Circularly polarized light standards for investigations of collagen fiber orientation in bone journal September 2003
Bone Mineral Density in Girls with Forearm Fractures journal January 1998
The effects of ageing and changes in mineral content in degrading the toughness of human femora journal February 1996
Standardized nomenclature, symbols, and units for bone histomorphometry: A 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee journal December 2012
The mechanical properties of bone tissue in children journal January 1975
Epidemiology of fractures of the distal end of the radius in children as associated with growth. journal January 1989
Influence of mineral content and composition on graylevels in backscattered electron images of bone journal January 1993
Mineral maturity and crystallinity index are distinct characteristics of bone mineral journal January 2010
FT-IR imaging of native and tissue-engineered bone and cartilage journal May 2007
Long bone maturation is driven by pore closing: A quantitative tomography investigation of structural formation in young C57BL/6 mice journal August 2015
Periosteal Bone Formation — A Neglected Determinant of Bone Strength journal July 2003
Developing bones are differentially affected by compromised skeletal muscle formation journal May 2010
Bone Biology journal January 1995
The effects of ageing and changes in mineral content in degrading the toughness of human femora journal September 1997
Erratum: The genetics of bone mass and susceptibility to bone diseases journal July 2016
Nanoscale deformation mechanisms in bone journal May 2009

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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

Figures / Tables (13)