Microtensile failure mechanisms in lamellar bone: Influence of fibrillar orientation, specimen size and hydration

Casari, Daniele; Kochetkova, Tatiana; Michler, Johann; Zysset, Philippe; Schwiedrzik, Jakob

doi:10.1016/j.actbio.2021.06.032

Cited by 11 publications

(9 citation statements)

References 62 publications

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“…Unfortunately, rehydration of dry bone tissue may lead to swelling, which alters the of testing. [ 24 ]…”

Section: Introductionmentioning

confidence: 99%

“…Unfortunately, rehydration of dry bone tissue may lead to swelling, which alters the of testing. [24] The goal of this study is to compare the tensile mechanical properties among bone biopsies from individuals with and without OI. Our first hypothesis is that a size-effect exists between the micro and macro mechanical properties leading to increased bone strength at the tissue level in both OI and healthy control bone.…”

Section: Introductionmentioning

confidence: 99%

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Tensile Mechanical Properties of Dry Cortical Bone Extracellular Matrix: A Comparison Among Two Osteogenesis Imperfecta and One Healthy Control Iliac Crest Biopsies

Indermaur,

Casari,

Kochetkova

et al. 2023

JBMR Plus

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Osteogenesis imperfecta (OI) is a genetic, collagen‐related bone disease that increases the incidence of bone fractures. Still, the origin of this brittle mechanical behavior remains unclear. The extracellular matrix (ECM) of OI bone exhibits a higher degree of bone mineralization (DBM), whereas compressive mechanical properties at the ECM level do not appear to be inferior to healthy bone. However, it is unknown if collagen defects alter ECM tensile properties. This study aims to quantify the tensile properties of healthy and OI bone ECM. In three transiliac biopsies (healthy n = 1, OI type I n = 1, OI type III n = 1), 23 microtensile specimens (gauge dimensions 10 × 5 × 2 μm3) were manufactured and loaded quasi‐statically under tension in vacuum condition. The resulting loading modulus and ultimate strength were extracted. Interestingly, tensile properties in OI bone ECM were not inferior compared to controls. All specimens revealed a brittle failure behavior. Fracture surfaces were graded according to their mineralized collagen fibers (MCF) orientation into axial, mixed, and transversal fracture surface types (FST). Furthermore, tissue mineral density (TMD) of the biopsy cortices was extracted from micro–computed tomogra[hy (μCT) images. Both FST and TMD are significant factors to predict loading modulus and ultimate strength with an adjusted R2 of 0.556 (p = 2.65e−05) and 0.46 (p = 2.2e−04), respectively. The influence of MCF orientation and DBM on the mechanical properties of the neighboring ECM was further verified with quantitative polarized Raman spectroscopy (qPRS) and site‐matched nanoindentation. MCF orientation and DBM were extracted from the qPRS spectrum, and a second mechanical model was developed to predict the indentation modulus with MCF orientation and DBM (R2 = 67.4%, p = 7.73e−07). The tensile mechanical properties of the cortical bone ECM of two OI iliac crest biopsies are not lower than the one from a healthy and are primarily dependent on MCF orientation and DBM. © 2023 The Authors. JBMR Plus published by Wiley Periodicals LLC on behalf of American Society for Bone and Mineral Research.

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“…Unfortunately, rehydration of dry bone tissue may lead to swelling, which alters the of testing. [ 24 ]…”

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Tensile Mechanical Properties of Dry Cortical Bone Extracellular Matrix: A Comparison Among Two Osteogenesis Imperfecta and One Healthy Control Iliac Crest Biopsies

Indermaur,

Casari,

Kochetkova

et al. 2023

JBMR Plus

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“…Hydration status of bone seems to be important during crack growth. Water presence leads to a stable crack growth parallel to the fibril orientation, indicating the combined role of collagen fibril orientation and hydration in crack initiation under tensile loading . In summary, the above-mentioned studies indicate a crucial role of the orientation of MCFs in response to the mechanical loading to resist the growth of cracks at the sub-micrometer scale …”

Section: Mcfs and The Mechanical Properties Of Bonementioning

confidence: 82%

“…Water presence leads to a stable crack growth parallel to the fibril orientation, indicating the combined role of collagen fibril orientation and hydration in crack initiation under tensile loading. 140 In summary, the above-mentioned studies indicate a crucial role of the orientation of MCFs in response to the mechanical loading to resist the growth of cracks at the sub-micrometer scale. 139 Microcracks at the microscale level were found to be highly dependent on the loading direction relative to the orientation of osteons and loading type.…”

Section: Intrinsic Toughening Mechanism Of Bone Originating From Mcfsmentioning

confidence: 91%

Mineralized Collagen Fibrils: An Essential Component in Determining the Mechanical Behavior of Cortical Bone

Al-Qudsy

et al. 2023

ACS Biomater. Sci. Eng.

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Bone comprises mechanically different materials in a specific hierarchical structure. Mineralized collagen fibrils (MCFs), represented by tropocollagen molecules and hydroxyapatite nanocrystals, are the fundamental unit of bone. The mechanical characterization of MCFs provides the unique adaptive mechanical competence to bone to withstand mechanical load. The structural and mechanical role of MCFs is critical in the deformation mechanisms of bone and the marvelous strength and toughness possessed by bone. However, the role of MCFs in the mechanical behavior of bone across multiple length scales is not fully understood. In the present study, we shed light upon the latest progress regarding bone deformation at multiple hierarchical levels and emphasize the role of MCFs during bone deformation. We propose the concept of hierarchical deformation of bone to describe the interconnected deformation process across multiple length scales of bone under mechanical loading. Furthermore, how the deterioration of bone caused by aging and diseases impairs the hierarchical deformation process of the cortical bone is discussed. The present work expects to provide insights on the characterization of MCFs in the mechanical properties of bone and lays the framework for the understanding of the multiscale deformation mechanics of bone.

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“…However, the effects of demineralization on enzymatic and non-enzymatic cross-links as well as to other organic components of the bone matrix were not investigated. Thus, while the collagen network within the mineral matrix accomplishes its function perfectly, altered mechanical properties are presented for both, native bone ( Casari et al, 2021 ; Gustafsson et al, 2018 ) and non-mineralized collagen fibrils ( Masic et al, 2015 ; Ping et al, 2022 ) when separated from each other. Investigating the deformation of mineral and collagen in bone by combining in situ testing of fibrolamellar bone with simultaneous SAXS and WAXD measuring tissue, fibrillar, and mineral strain of single fibrolamellar bone packets in a tensile testing setup revealed approximately constant fibril-to-tissue (0.41) and mineral-to-tissue (0.16) strain ratio in the elastic response (yield strain = 0.91 %) ( Gupta et al, 2006 ).…”

Section: Discussionmentioning

confidence: 99%

Bone collagen tensile properties of the aging human proximal femur

Bracher,

Voumard,

Simon

et al. 2024

Bone Reports

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Microtensile failure mechanisms in lamellar bone: Influence of fibrillar orientation, specimen size and hydration

Cited by 11 publications

References 62 publications

Tensile Mechanical Properties of Dry Cortical Bone Extracellular Matrix: A Comparison Among Two Osteogenesis Imperfecta and One Healthy Control Iliac Crest Biopsies

Tensile Mechanical Properties of Dry Cortical Bone Extracellular Matrix: A Comparison Among Two Osteogenesis Imperfecta and One Healthy Control Iliac Crest Biopsies

Mineralized Collagen Fibrils: An Essential Component in Determining the Mechanical Behavior of Cortical Bone

Bone collagen tensile properties of the aging human proximal femur

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