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 clo...

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Veröffentlicht in:Journal of the mechanical behavior of biomedical materials 2017-11, Vol.75, p.399-412
Hauptverfasser: 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, The OStEO Group
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container_title Journal of the mechanical behavior of biomedical materials
container_volume 75
creator 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
The OStEO Group
description 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
doi_str_mv 10.1016/j.jmbbm.2017.06.036
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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 &gt; 0.05 for fracture properties and &lt;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 &lt; 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.</description><identifier>ISSN: 1751-6161</identifier><identifier>EISSN: 1878-0180</identifier><identifier>DOI: 10.1016/j.jmbbm.2017.06.036</identifier><identifier>PMID: 28803114</identifier><language>eng</language><publisher>Netherlands</publisher><subject>Adult ; Age Factors ; Aged ; Aged, 80 and over ; Biomechanical Phenomena ; Bone Density ; Female ; Femur ; Femur Neck - pathology ; Fractures, Bone - pathology ; Humans ; Male ; Middle Aged ; Osteoporosis - pathology ; X-Ray Microtomography</subject><ispartof>Journal of the mechanical behavior of biomedical materials, 2017-11, Vol.75, p.399-412</ispartof><rights>Copyright © 2017 The Authors. Published by Elsevier Ltd.. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c405t-80cccb5eae8b45edb789178cfc22c744978e039660f3500118ad731184ffbb4d3</citedby><cites>FETCH-LOGICAL-c405t-80cccb5eae8b45edb789178cfc22c744978e039660f3500118ad731184ffbb4d3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28803114$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Jenkins, T</creatorcontrib><creatorcontrib>Katsamenis, O L</creatorcontrib><creatorcontrib>Andriotis, O G</creatorcontrib><creatorcontrib>Coutts, L V</creatorcontrib><creatorcontrib>Carter, B</creatorcontrib><creatorcontrib>Dunlop, D G</creatorcontrib><creatorcontrib>Oreffo, R O C</creatorcontrib><creatorcontrib>Cooper, C</creatorcontrib><creatorcontrib>Harvey, N C</creatorcontrib><creatorcontrib>Thurner, P J</creatorcontrib><creatorcontrib>The OStEO Group</creatorcontrib><title>The inferomedial femoral neck is compromised by age but not disease: Fracture toughness and the multifactorial mechanisms comprising reference point microindentation</title><title>Journal of the mechanical behavior of biomedical materials</title><addtitle>J Mech Behav Biomed Mater</addtitle><description>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 &gt; 0.05 for fracture properties and &lt;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 &lt; 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.</description><subject>Adult</subject><subject>Age Factors</subject><subject>Aged</subject><subject>Aged, 80 and over</subject><subject>Biomechanical Phenomena</subject><subject>Bone Density</subject><subject>Female</subject><subject>Femur</subject><subject>Femur Neck - pathology</subject><subject>Fractures, Bone - pathology</subject><subject>Humans</subject><subject>Male</subject><subject>Middle Aged</subject><subject>Osteoporosis - pathology</subject><subject>X-Ray Microtomography</subject><issn>1751-6161</issn><issn>1878-0180</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVUU1v1DAQjSoq-gG_oBLykUvCOB-OwwEJVZQiVeqlnC3bmex6ie0ldir1B_E_maVLBacZ-c28eX6vKK44VBy4-LCrdt4YX9XA-wpEBY04Kc657GUJXMIr6vuOl4ILflZcpLQDEABSvi7Oaimh4bw9L349bJG5MOESPY5Oz2xCHxeqAe0P5hKz0e8JdAlHZp6Y3iAza2YhZjbSo074kd0s2uZ1QZbjutkGTInpMLJM3H6ds5sIjsuB3aPd6uCSPxK75MKGLUgCMFhk--hCZt7ZhZoRQ9bZxfCmOJ30nPDtsV4W32--PFzflnf3X79df74rbQtdLiVYa02HGqVpOxxNLwfeSzvZurZ92w69RGgGIWBqOgDOpR578kG202RMOzaXxadn3v1qyA5L98kKRTK9Xp5U1E79jwS3VZv4qDrBB9F2RPD-SLDEnyumrMg4i_OsA8Y1KT7UlE8jmoFGm-dR-mpK5MDLGQ7qELDaqT8Bq0PACoSigGnr3b8KX3b-Jtr8Bsm4qYg</recordid><startdate>20171101</startdate><enddate>20171101</enddate><creator>Jenkins, T</creator><creator>Katsamenis, O L</creator><creator>Andriotis, O G</creator><creator>Coutts, L V</creator><creator>Carter, B</creator><creator>Dunlop, D G</creator><creator>Oreffo, R O C</creator><creator>Cooper, C</creator><creator>Harvey, N C</creator><creator>Thurner, P J</creator><creator>The OStEO Group</creator><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20171101</creationdate><title>The inferomedial femoral neck is compromised by age but not disease: Fracture toughness and the multifactorial mechanisms comprising reference point microindentation</title><author>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 ; The OStEO Group</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c405t-80cccb5eae8b45edb789178cfc22c744978e039660f3500118ad731184ffbb4d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Adult</topic><topic>Age Factors</topic><topic>Aged</topic><topic>Aged, 80 and over</topic><topic>Biomechanical Phenomena</topic><topic>Bone Density</topic><topic>Female</topic><topic>Femur</topic><topic>Femur Neck - pathology</topic><topic>Fractures, Bone - pathology</topic><topic>Humans</topic><topic>Male</topic><topic>Middle Aged</topic><topic>Osteoporosis - pathology</topic><topic>X-Ray Microtomography</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Jenkins, T</creatorcontrib><creatorcontrib>Katsamenis, O L</creatorcontrib><creatorcontrib>Andriotis, O G</creatorcontrib><creatorcontrib>Coutts, L V</creatorcontrib><creatorcontrib>Carter, B</creatorcontrib><creatorcontrib>Dunlop, D G</creatorcontrib><creatorcontrib>Oreffo, R O C</creatorcontrib><creatorcontrib>Cooper, C</creatorcontrib><creatorcontrib>Harvey, N C</creatorcontrib><creatorcontrib>Thurner, P J</creatorcontrib><creatorcontrib>The OStEO Group</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of the mechanical behavior of biomedical materials</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Jenkins, T</au><au>Katsamenis, O L</au><au>Andriotis, O G</au><au>Coutts, L V</au><au>Carter, B</au><au>Dunlop, D G</au><au>Oreffo, R O C</au><au>Cooper, C</au><au>Harvey, N C</au><au>Thurner, P J</au><au>The OStEO Group</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The inferomedial femoral neck is compromised by age but not disease: Fracture toughness and the multifactorial mechanisms comprising reference point microindentation</atitle><jtitle>Journal of the mechanical behavior of biomedical materials</jtitle><addtitle>J Mech Behav Biomed Mater</addtitle><date>2017-11-01</date><risdate>2017</risdate><volume>75</volume><spage>399</spage><epage>412</epage><pages>399-412</pages><issn>1751-6161</issn><eissn>1878-0180</eissn><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 &gt; 0.05 for fracture properties and &lt;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 &lt; 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.</abstract><cop>Netherlands</cop><pmid>28803114</pmid><doi>10.1016/j.jmbbm.2017.06.036</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record>
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subjects Adult
Age Factors
Aged
Aged, 80 and over
Biomechanical Phenomena
Bone Density
Female
Femur
Femur Neck - pathology
Fractures, Bone - pathology
Humans
Male
Middle Aged
Osteoporosis - pathology
X-Ray Microtomography
title The inferomedial femoral neck is compromised by age but not disease: Fracture toughness and the multifactorial mechanisms comprising reference point microindentation
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