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The inferomedial femoral neck is compromised by age but not disease: Fracture toughness and the multifactorial mechanisms comprising reference point microindentation

The inferomedial femoral neck is compromised by age but not disease: Fracture toughness and the multifactorial mechanisms comprising reference point microindentation
The inferomedial femoral neck is compromised by age but not disease: Fracture toughness and the multifactorial mechanisms comprising reference point microindentation
The influence of ageing on the fracture mechanics of cortical bone tissue is well documented, though little is known about if and how related material properties are further affected in two of the most prominent musculoskeletal diseases, osteoporosis and osteoarthritis (OA). The femoral neck, in close proximity to the most pertinent osteoporotic fracture site and near the hip joint affected by osteoarthritis, is a site of particular interest for investigation. We have recently shown that Reference Point micro-Indentation (RPI) detects differences between cortical bone from the femoral neck of healthy, osteoporotic fractured and osteoarthritic hip replacement patients. RPI is a new technique with potential for in vivo bone quality assessment. However, interpretation of RPI results is limited because the specific changes in bone properties with pathology are not well understood and, further, because it is not conclusive what properties are being assessed by RPI. Here, we investigate whether the differences previously detected between healthy and diseased cortical bone from the femoral neck might reflect changes in fracture toughness. Together with this, we investigate, which additional properties are reflected in RPI measures. RPI (using the Biodent device) and fracture toughness tests were conducted on samples from the inferomedial neck of bone resected from donors with: OA (41 samples from 15 donors), osteoporosis (48 samples from 14 donors) and non age-matched cadaveric controls (37 samples from 10 donoros) with no history of bone disease. Further, a subset of indented samples were imaged using micro-computed tomography (3 osteoporotic and 4 control samples each from different donors) as well as fluorescence microscopy in combination with serial sectioning after basic fuchsin staining (7 osteoporotic and 5 control samples from 5 osteoporotic and 5 control donors). In this study, the bulk indentation and fracture resistance properties of the inferomedial femoral neck in osteoporotic fracture, severe OA and control bone were comparable (p > 0.05 for fracture properties and <10% difference for indentation) but fracture toughness reduced with advancing age (7.0% per decade, r = −0.36, p = 0.029). Further, RPI properties (in particular, the indentation distance increase, IDI) showed partial correlation with fracture toughness (r = −0.40, p = 0.023) or derived elastic modulus (r = −0.40, p = 0.023). Multimodal indent imaging revealed evidence of toughening mechanisms (i.e. crack deflection, bridging and microcracking), elastoplastic response (in terms of the non-conical imprint shape and presence of pile-up) and correlation of RPI with damage extent (up to r = 0.79, p = 0.034) and indent size (up to r = 0.82, p < 0.001). Therefore, crack resistance, deformation resistance and, additionally, micro-structure (porosity: r = 0.93, p = 0.002 as well as pore proximity: r = −0.55, p = 0.027 for correlation with IDI) are all contributory to RPI. Consequently, it becomes clear that RPI measures represent a multitude of properties, various aspects of bone quality, but are not necessarily strongly correlated to a single mechanical property. In addition, osteoporosis or osteoarthritis do not seem to further influence fracture toughness of the inferomedial femoral neck beyond natural ageing. Since bone is highly heterogeneous, whether this finding can be extended to the whole femoral neck or whether it also holds true for other femoral neck quadrants or other material properties remains to be shown.
1751-6161
399-412
Jenkins, T.
e8110e1f-0b08-41ac-932a-46647c6845f3
Katsamenis, O.L.
8553e7c3-d860-4b7a-a883-abf6c0c4b438
Andriotis, O.G.
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Coutts, L.V.
90c9e532-5400-4ef8-853f-0e3c311b4f27
Carter, B.
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Dunlop, D.G.
eb03bdad-6a88-4057-acd8-70a9271f629d
Oreffo, R.O.C.
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Cooper, C.
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Harvey, N.C.
ce487fb4-d360-4aac-9d17-9466d6cba145
Thurner, P.J.
ab711ddd-784e-48de-aaad-f56aec40f84f
Arden, Nigel
23af958d-835c-4d79-be54-4bbe4c68077f
the OStEO group
Jenkins, T.
e8110e1f-0b08-41ac-932a-46647c6845f3
Katsamenis, O.L.
8553e7c3-d860-4b7a-a883-abf6c0c4b438
Andriotis, O.G.
d88047ee-bc23-4b1b-9d98-184685fefb65
Coutts, L.V.
90c9e532-5400-4ef8-853f-0e3c311b4f27
Carter, B.
263c07ad-1212-421d-9246-6a5daa6a7ad5
Dunlop, D.G.
eb03bdad-6a88-4057-acd8-70a9271f629d
Oreffo, R.O.C.
ff9fff72-6855-4d0f-bfb2-311d0e8f3778
Cooper, C.
e05f5612-b493-4273-9b71-9e0ce32bdad6
Harvey, N.C.
ce487fb4-d360-4aac-9d17-9466d6cba145
Thurner, P.J.
ab711ddd-784e-48de-aaad-f56aec40f84f
Arden, Nigel
23af958d-835c-4d79-be54-4bbe4c68077f

Jenkins, T., Katsamenis, O.L., Andriotis, O.G., Coutts, L.V., Carter, B., Dunlop, D.G., Oreffo, R.O.C., Cooper, C., Harvey, N.C., Thurner, P.J. and Arden, Nigel , the OStEO group (2017) The inferomedial femoral neck is compromised by age but not disease: Fracture toughness and the multifactorial mechanisms comprising reference point microindentation. Journal of the Mechanical Behavior of Biomedical Materials, 75, 399-412. (doi:10.1016/j.jmbbm.2017.06.036).

Record type: Article

Abstract

The influence of ageing on the fracture mechanics of cortical bone tissue is well documented, though little is known about if and how related material properties are further affected in two of the most prominent musculoskeletal diseases, osteoporosis and osteoarthritis (OA). The femoral neck, in close proximity to the most pertinent osteoporotic fracture site and near the hip joint affected by osteoarthritis, is a site of particular interest for investigation. We have recently shown that Reference Point micro-Indentation (RPI) detects differences between cortical bone from the femoral neck of healthy, osteoporotic fractured and osteoarthritic hip replacement patients. RPI is a new technique with potential for in vivo bone quality assessment. However, interpretation of RPI results is limited because the specific changes in bone properties with pathology are not well understood and, further, because it is not conclusive what properties are being assessed by RPI. Here, we investigate whether the differences previously detected between healthy and diseased cortical bone from the femoral neck might reflect changes in fracture toughness. Together with this, we investigate, which additional properties are reflected in RPI measures. RPI (using the Biodent device) and fracture toughness tests were conducted on samples from the inferomedial neck of bone resected from donors with: OA (41 samples from 15 donors), osteoporosis (48 samples from 14 donors) and non age-matched cadaveric controls (37 samples from 10 donoros) with no history of bone disease. Further, a subset of indented samples were imaged using micro-computed tomography (3 osteoporotic and 4 control samples each from different donors) as well as fluorescence microscopy in combination with serial sectioning after basic fuchsin staining (7 osteoporotic and 5 control samples from 5 osteoporotic and 5 control donors). In this study, the bulk indentation and fracture resistance properties of the inferomedial femoral neck in osteoporotic fracture, severe OA and control bone were comparable (p > 0.05 for fracture properties and <10% difference for indentation) but fracture toughness reduced with advancing age (7.0% per decade, r = −0.36, p = 0.029). Further, RPI properties (in particular, the indentation distance increase, IDI) showed partial correlation with fracture toughness (r = −0.40, p = 0.023) or derived elastic modulus (r = −0.40, p = 0.023). Multimodal indent imaging revealed evidence of toughening mechanisms (i.e. crack deflection, bridging and microcracking), elastoplastic response (in terms of the non-conical imprint shape and presence of pile-up) and correlation of RPI with damage extent (up to r = 0.79, p = 0.034) and indent size (up to r = 0.82, p < 0.001). Therefore, crack resistance, deformation resistance and, additionally, micro-structure (porosity: r = 0.93, p = 0.002 as well as pore proximity: r = −0.55, p = 0.027 for correlation with IDI) are all contributory to RPI. Consequently, it becomes clear that RPI measures represent a multitude of properties, various aspects of bone quality, but are not necessarily strongly correlated to a single mechanical property. In addition, osteoporosis or osteoarthritis do not seem to further influence fracture toughness of the inferomedial femoral neck beyond natural ageing. Since bone is highly heterogeneous, whether this finding can be extended to the whole femoral neck or whether it also holds true for other femoral neck quadrants or other material properties remains to be shown.

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More information

Accepted/In Press date: 28 June 2017
e-pub ahead of print date: 30 June 2017
Published date: November 2017

Identifiers

Local EPrints ID: 412252
URI: http://eprints.soton.ac.uk/id/eprint/412252
ISSN: 1751-6161
PURE UUID: ee18558a-300d-4cdd-bc29-ca9d7ef75357
ORCID for O.L. Katsamenis: ORCID iD orcid.org/0000-0003-4367-4147
ORCID for R.O.C. Oreffo: ORCID iD orcid.org/0000-0001-5995-6726
ORCID for C. Cooper: ORCID iD orcid.org/0000-0003-3510-0709
ORCID for N.C. Harvey: ORCID iD orcid.org/0000-0002-8194-2512
ORCID for P.J. Thurner: ORCID iD orcid.org/0000-0001-7588-9041

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Date deposited: 14 Jul 2017 16:30
Last modified: 08 Oct 2020 04:11

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