header advert
Bone & Joint Research Logo

Receive monthly Table of Contents alerts from Bone & Joint Research

Comprehensive article alerts can be set up and managed through your account settings

View my account settings

Visit Bone & Joint Research at:

X (Twitter)
Instagram
Article alerts Social media
Current issue
Submit
Open Access

Biomaterials

Standardizing compression testing for measuring the stiffness of human bone

Download PDF

Abstract

Objectives

The ability to determine human bone stiffness is of clinical relevance in many fields, including bone quality assessment and orthopaedic prosthesis design. Stiffness can be measured using compression testing, an experimental technique commonly used to test bone specimens in vitro. This systematic review aims to determine how best to perform compression testing of human bone.

Methods

A keyword search of all English language articles up until December 2017 of compression testing of bone was undertaken in Medline, Embase, PubMed, and Scopus databases. Studies using bulk tissue, animal tissue, whole bone, or testing techniques other than compression testing were excluded.

Results

A total of 4712 abstracts were retrieved, with 177 papers included in the analysis; 20 studies directly analyzed the compression testing technique to improve the accuracy of testing. Several influencing factors should be considered when testing bone samples in compression. These include the method of data analysis, specimen storage, specimen preparation, testing configuration, and loading protocol.

Conclusion

Compression testing is a widely used technique for measuring the stiffness of bone but there is a great deal of inter-study variation in experimental techniques across the literature. Based on best evidence from the literature, suggestions for bone compression testing are made in this review, although further studies are needed to establish standardized bone testing techniques in order to increase the comparability and reliability of bone stiffness studies.

Cite this article: S. Zhao, M. Arnold, S. Ma, R. L. Abel, J. P. Cobb, U. Hansen, O. Boughton. Standardizing compression testing for measuring the stiffness of human bone. Bone Joint Res 2018;7:524–538. DOI: 10.1302/2046-3758.78.BJR-2018-0025.R1.

Article focus

  • To provide a comprehensive review on the experimental technique of compression testing of bone.

  • To provide recommendations on how best to perform compression testing of bone in the future.

Key messages

  • There is a great deal of inter-study variation in the experimental technique for compression testing of bone.

  • Factors such as specimen preparation, specimen geometry, testing configuration, and strain rate can affect the measurement of bone stiffness.

  • Further studies looking specifically at aspects of the compression testing technique are required in order to establish a standardized method for bone.

Strengths and limitations

  • This review followed guidelines suggested by the Cochrane and Preferred Reporting Items for Systematic Reviews and Meta-Analyses organizations.

  • This review of compression testing can help to develop a standardized experimental bone testing technique in the future.

Introduction

Stiffness can be defined as the resistance of a structure or material to deformation.1 This property is of great importance for understanding the relationship between the structure and function of bone, and is clinically relevant in areas such as orthopaedic prosthesis design and characterization of bone properties across anatomical locations.2-5 Thus, the ability to determine bone stiffness in an accurate and efficient way is crucial for enabling clinicians to understand the effect of factors such as disease, age, and medical intervention on bone quality.

Compression testing is a widely used experimental technique for determining the mechanical properties of bulk tissue specimens excised from cortical or cancellous regions of bone.6-10 It is relatively straightforward to perform, and is capable of producing quick measurements of apparent elastic modulus and other properties, such as ultimate strength.11 Other bulk tissue testing techniques for determining stiffness include three-point bending, tensile testing, and torsional testing.12,13 The apparent properties obtained from these tests are independent of the whole bone geometry, but include effects of porosity and anisotropy arising from osteon or trabecular orientation.14 Currently, there is wide variation in the literature about how compression testing of bone is performed, with no benchmark protocol. Differences between studies may be due to differing processes of extraction, machining, and preserving the bone samples.15 They may also be due to the method used to measure the strain in the bone as well as the strain rate used during testing.16

Currently, strict standards are universally established for the experimental testing of engineering materials. However, this is not the case for compression testing of bone specimens, where standardized material testing methods cannot always be applied due to restrictions related to using biological tissue. These include the heterogeneity and finite size of bone specimens, difficulties with gripping bone surfaces, as well as the relatively low loads that can be applied. Subsequently, there are variations in testing methodology and specimen preparation across the literature, and direct comparison of studies is difficult.15 Therefore, this paper aims to review systematically the literature surrounding compression testing of human bone and its reliability for measuring stiffness. Specifically, this systematic review aims to determine how best to perform compression testing of human bone in order to help develop a standardized testing technique for future studies.

Materials and Methods

A systematic review of published literature up until December 2017 relating to compression testing of human bone was undertaken using Medline, Embase, PubMed, and Scopus databases according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines.17 This was considered representative of the literature. A combination of the search terms, “compression test*” OR “compressive test*” OR “axial compression” AND “Bone*” OR “cortical bone*” OR “compact bone*” AND “stiffness” OR “rigidity” OR “elasticity” OR “elastic* modulus” OR “Young’s modulus” were used. Exclusion criteria included studies using non-human tissue, those that did not undergo compression testing (e.g. tensile testing or finite element modelling), non-bulk tissue testing (e.g. whole bone specimens), non-accessible or non-English papers, and those that did not measure stiffness directly from the compression test. Two authors (SZ and MA) were responsible for independent article extraction and inclusion. Any disagreements were resolved with discussion as recommended by Cochrane Collaboration guidelines.18

Results

Search results

Figure 1 shows the study extraction flowchart, according to PRISMA guidelines. A total of 4712 abstracts were retrieved. Following duplicate removal and abstract screening, a total of 807 eligible full-text articles remained. After review of these manuscripts, 177 papers were deemed to fit the inclusion criteria for compression testing of human bone and were consequently included in this review.

Fig. 1 Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow diagram of study selection.

Fig. 1

Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow diagram of study selection.

Qualitative assessment

Overall, there was a great deal of variation across the literature in terms of testing protocol. Supplementary tables i, ii, and iii show details of the testing protocol and experimental setup used in each study, with articles separated according to the type of bone used (cancellous, cortical, or mixed specimens). If the method of strain measurement was not specifically reported in the article, it was assumed that it was measured via the machine crosshead displacement. A total of 20 studies directly analyzed aspects of the compression testing technique,7,16,19-36 and provided recommendations for improving the accuracy and precision of future testing. A brief overview of the studies retrieved is provided in the results section of this review. The analysis of individual studies is in the discussion section.

Bone specimen preparation and storage

It was found that the most common method for storing and preserving bone specimens prior to testing was freezing and subsequent thawing before testing.5,6,8,10,16,20-22,24-31,33-139 The temperatures used varied across the literature and samples were commonly frozen in physiological (0.9%) saline solutions. Other solutions used for storage, or for thawing samples, include ethanol,5,22,32,70-72,140-145 Ringer’s solution,16,31,42,43,57,60,74,80,83,84,105,142,144,146 embalming fluid (commonly formalin-based solutions),31,102,118,141,147-152 and phosphate-buffered saline (PBS) solution.65,115,124,135,153 Some studies freeze-dried the samples.21,59,154-156

During the testing process, fresh wet specimens were most commonly used. Six studies used dried specimens in the compression test.33,51,135,138,157,158 The majority of studies tested bone specimens in unconfined conditions, but some tested in confined conditions using confinement chambers,22,98,159,160 a steel annulus,52 or polytetrafluoroethylene (PTFE) tape.130

Testing setup

The standard compression test traditionally involves compressing the bone specimen between two fixed parallel stainless-steel platens or anvils (Fig. 2). Certain studies used a combination of a fixed platen paired with an adjustable, rotating platen.38,43-45,69,101,104,107,113,118,119,146,157,161-163 A few studies used variations of the standard machine setup such as use of grooved platens,154 custom-built compression machines,82,122,132,164,165 and drop tower159 or hand-loaded testing machines.141 Some studies tested bone specimens in water baths filled with saline solution.53,66,70,72,87,107,122,166,167 Other solutions in which samples were immersed during testing included Ringer’s solution,168 Hank’s Balanced Salt Solution,166 and PBS with protease inhibitors.132

Images showing a) standard platens compression testing setup of a bone specimen, and b) a close-up schematic of a bone specimen placed between two polished platens.

Fig.

Images showing a) standard platens compression testing setup of a bone specimen, and b) a close-up schematic of a bone specimen placed between two polished platens.

Many studies used additional measures to improve accuracy of the testing technique, including the use of mineral oil to lubricate the specimen-platen interface22,24,26,34,61,88,103,127-129,133,147,148,162 and embedding the specimens in brass, aluminium alloy, or stainless-steel endcaps.4,8,19,28,29,34-36,39,40,49,73,76,77,90,99,113,118,119,131-133,142,144,153,159,164,167,169 Some studies used latex,33,38,69,132 Teflon plates,20,104 or poly(methyl methacrylate) (PMMA) cement22,27,32,166,170,171 on the specimen ends to help stabilize the severed trabecular free ends. Other studies glued specimens with cyanoacrylate or epoxy adhesive to the platen.51,55,116,172-174

Strain measurement

The most common method for strain measurement was using the machine crosshead displacement. The following studies applied machine compliance correction when using this method of strain measurement.34,37,46,47,51,52,57,75,88,160,166,168 Only one study37 gave specific details of the compliance correction algorithm. Other studies used extensometers3,8,16,22,24,26-32,35,40,47,49,50,53,60-62,65,68,76,77,81-84,90,97,103-105,111,112,119,127,129,131-133,135,136,142,144,147,148,168,170,171,173-181 and electric resistance wire strain gauges33,133,158,160 to measure strain. A few studies used Digital Image Correlation (DIC), an optical, non-contact technique.30,67,86,120,125,140,145,182 It was found that the majority of studies used physiological183 strain rates in the range of 0.005 s-1 to 0.08 s-1, with a few testing at substantially higher strain rates.16,26,68,159,161

Discussion

This systematic review set out to determine how best to perform compression testing of human bone, in order to suggest a standardized method for determining bone stiffness to be used in future studies. A total of 177 articles were retrieved which help to answer this question. The retrieved articles have been analyzed and, where possible, recommendations for compression testing have been made.

Determination of stiffness

The load-displacement curve and the resultant stress-strain curve can be divided into elastic and plastic deformation regions. Within the elastic region, the structure undergoes deformation, which returns to its original shape after the load is released.9 The pre-yield region of the stress-strain curve is usually linear and is considered, often incorrectly, to be elastic. The slope of the linear portion is taken by many researchers as the elastic modulus or Young’s modulus (Fig. 3). However, bone is a complex, anisotropic, and heterogeneous material that does not behave as a purely elastic material. Thus, it has been shown to demonstrate non-linear behaviour, particularly at the lower portion of the pre-yield elastic region of the stress-strain curve, likely due to factors such as irregularities in the specimen surface layers.25,29,34 Morgan et al29 thus used a second-order polynomial fit for strain ranges of up to 0.2% when calculating the slope to minimize systematic errors. For strain ranges up to 0.25% and 0.3%, they used third and fourth order polynomial fits, respectively.

Fig. 3 Stress-strain graph of a typical compression test with corresponding mechanical parameters measured.

Fig. 3

Stress-strain graph of a typical compression test with corresponding mechanical parameters measured.

Strictly speaking, the slope of the linear portion of the stress-strain curve is not the Young’s modulus of the bone specimen because this deformation is not purely elastic. Bones have complex hierarchical structures and contain many defects, including pores. Some degree of plastic deformation is present, even at a relatively low compressive stress or strain. An appropriate term used to describe the slope of the initial linear part is the apparent modulus, which is a useful stiffness parameter for comparison purposes.184 However, this parameter simply represents the ratio between stress and strain, and should not be confused with the elastic or Young’s modulus of the material. Many papers in the literature reported the apparent modulus as Young’s modulus.3-5,7,10,16,19,20-25,27,29,30-33,37,40-42,45,47,48,50-53,55,57-71,73-84,86-100,102-124,126-137,139,140,142-148,150,151,153-159,161-164,166-168,176-182,185-195 This likely explains why many reported Young’s modulus values are generally lower than expected, and with a wide range of variance.

The Young’s modulus of bone specimens ideally should be obtained by an intermittent loading-unloading procedure. Specifically, the stress is increased at a low strain rate to a level somewhat below the yield point, i.e. before the stress-strain curve deviates from the linear portion. It is then released and immediately increased again, forming a loading-unloading cycle.196 The unloading curve is steeper than the linear portion of the normal stress-strain curve, and its gradient can be used to generate a value for Young’s modulus.65 However, the complexity of bone material and variation between specimen and specimen may mean that this technique (which is commonly used in testing porous metals196) is not feasible. Thus, we suggest for pragmatic purposes that the technique outlined by Keaveny et al36 is used, whereby modulus is determined from a best fit line to the steepest portion of the stress-strain curve over a range of 0.2% strain. This is still technically measuring apparent modulus, but at a strain below 0.2% the amount of plastic deformation is likely to be small. Thus, this method may provide a value close to the true elastic modulus. However, care should be taken when interpreting the validity of data taken from studies using this method of calculation in the absence of endcaps or extensometers. This is because there is often a non-linear toe-in region present on the loading curve over this strain range if endcaps are not used.

All future studies should report the correct terminology, particularly where absolute values for modulus are concerned.

Other factors contributing to the variance in the literature regarding bone stiffness include patient demographic or health status, sample location, orientation, and testing conditions. It can be misleading to provide an authoritative reference range for moduli, as in reality this range would differ between studies due to these numerous aforementioned compounding factors. But as a guide, for wet, cortical femoral bone (the most commonly tested), one can expect the stiffness to fall approximately in the range of 15 GPa to 20 GPa.8,65,112,142 This range should be interpreted accordingly with the test conditions and sample origin. Lower values should be anticipated when using cancellous samples,197 when compressing in the transverse direction rather than the longitudinal,65 when testing metaphyseal bone, rather than diaphyseal bone,198 in a patient group of older age,61 or when extensometers and endcaps have not been used (i.e. structural end effects are not accounted for).36 Higher values may be anticipated when testing dry samples135,158 or at higher strain rates.16 These factors will be discussed in more detail in the subsequent sections of this paper.

Stiffness of animal bone is outside the scope of this review, but may be of interest to researchers. For example, where bovine bone is commonly used as a test material. For further discussion regarding other mechanical testing techniques and non-human bone, we recommend the broad review by Novitskaya et al197 as a good starting point.

Sample preparation

By far the most common method of specimen storage was shown to be freezing of wet bone specimens. Linde and Sørensen22 have shown that this method has minimal effect on stiffness. Therefore, freezing in physiological saline should be the standard method of storage as it is easily accessible and facilitates consistency and comparability between studies.

Although the majority of studies tested wet specimens, six studies tested dried specimens.33,51,135,138,157,158 Testing dry specimens may help facilitate coupling to the metal platens and hold the specimen in place. However, Carter et al51 found that specimens that had been dried then rewetted gave significantly greater moduli values than fresh specimens. This is consistent with studies by Bargren et al158 and Samuel et al,135 who found that bone specimens that had been dried had increased stiffness compared with the hydrated specimens. Therefore, studies using fresh specimens should not be compared with those using dry. When testing fresh specimens, care should be taken to ensure that the surface layers of the specimens do not dry out.

Bone can be considered a composite structure, with a solid phase (mineralized bone tissue) and a fluid phase (i.e. bone marrow, vessels, nerves, blood, and interstitial fluid).52 Thus, properties will change depending on whether or not specimens are tested with marrow in situ or ex situ,22,52 as well as depending on the hydration state of the tissue.135,199 Several studies have shown that defatting and removal of bone marrow from bone specimens prior to testing has significant effects on the mechanical properties measured.3,22,33,52 The storage method before testing is therefore important. It is recommended to freeze samples in saline with marrow intact. It not only has a minimal effect on the mechanical properties, but also is a widely accessible and commonly used technique.

Orientation and anatomical location

When compression testing anisotropic materials such as bone,200 care must be taken to control and specify orientation and axis of loading of the specimen. Not only is this important in studies wishing to replicate in vivo conditions, but it also helps ensure comparability between studies. Care must be taken to avoid misalignment of the principal material axes with the anatomical axes during the specimen machining process. This is because off-axis angulation can lead to errors in the mechanical properties measured, as demonstrated experimentally by Öhman et al.32 Schwiedrzik et al173 used bone specimens that were extracted perpendicular to the main trabecular orientation rather than parallel, which explained the lower yield stress values obtained in their study. Morgan and Keaveny99 quantified the degree of misalignment in their study to enable them to calculate the average estimated percentage error in their modulus measurements. They used microCT scanning, as did Perilli et al,144 to determine any off-axis angulation of the specimens. Bourgnon et al45 used a microscopy camera during their experiment to ensure correct alignment before testing. Although microCT and microscopy cameras can offer more accurate alignment information, they are not always available and can be time-consuming to use. Researchers should use cameras or visual inspection for checking orientation.

The orientation considerations can cause constraint in the sample extraction procedure. For example, in two studies by Wachter et al,127,129 the thin cortical shell in the donor patient’s femur only allowed for small cortical specimens to be extracted in one direction. If resources allow, it would be beneficial to take radiographs of specimens to ascertain the trabecular direction, and subsequently ensure correct orientation prior to testing.32,133,179,201 It is recommended that the misalignment angle is measured and considered when analyzing the outcomes.

Due to the nature of human tissue collection, it may be difficult to determine the orientation and location of biopsied specimens relative to the donor’s host bone. The most commonly sampled locations throughout the relevant literature were the femur, followed by the vertebras and tibia. Variation in results due to anatomical variation12 can be minimized by sampling from the same precise anatomical site. Lv et al156 designed a personalized mould for each femoral head used in their study to ensure that biopsies were extracted from precisely the same anatomical location in each patient. While this method confers a higher level of precision and ensures standardized sample extraction, it is both time- and resource-consuming. It is hardly practical when a large number of samples are involved, and may not be as reproducible in other locations as the femoral head. In most cases, the use of anatomical landmarks to determine specimen extraction location would be sufficient.

Specimen geometry

In compression testing, the specimens are typically cylindrical or parallelepiped. A few studies used cross-sectional slices ranging from 8 mm to 20 mm in height.39,44,59,94 This is not recommended because the height-to-width ratio is too small, and it is also difficult to give an accurate measurement of the cross-sectional area. Thus, stiffness derived from studies using non-uniform specimen geometries should be interpreted with caution. Studies have found that modulus decreases with decreasing specimen cross-sectional area and length.24,34 Linde et al24 suggest a 6.5 mm cube or cylinder of 7.5 mm diameter and 6.5 mm length, and Keaveny et al202 recommended the use of cylindrical specimens over cubic in order to minimize errors related to Poisson’s ratio. However, this error is likely to be small. As long as an appropriate aspect ratio is maintained, geometry of the cross section, either cylindrical or cubic, should not matter much.

It is appreciated that it would be difficult to set a standardized specimen size for testing as this ultimately depends on the machine setup and volume of tissue available. However, given the literature and with guidance from current testing standards for similar engineering materials, the following aspects should be considered when selecting specimen geometry:

  • The aspect ratio (i.e. the height to width ratio of the specimen). This should be between 1 and 2 to avoid buckling of the specimen during the compression test and thus maintain axial load application.201,203

  • Cylindrical cross-section specimens should be used where possible. A 2:1 cylinder of minimum 5 mm diameter, as suggested by Keaveny et al,202 would be sufficient to satisfy the continuum assumption.

  • The method of strain measurement. In general, larger specimens should be used if using machine crosshead motion for strain measurement to minimize the effect of the structurally compromised free surface layers. Zhu et al34 recommended a minimum height of 10 mm and cross-sectional area of 100 mm2. If this cannot be achieved, regional strain measurement should be carried out.

Machining

It is important to maintain a standardized process for machining the top, bottom, and side surfaces of the bone specimen. This may be one of the most time-consuming steps of sample preparation but is imperative for ensuring a maximally ideal stress field and state during compression testing. Both ends of the specimen should be parallel to each other, with these surfaces also lying perfectly perpendicular to the long axis of the specimen.141

Irrigated, low-speed, low-force cutting devices should be used to prevent overheating of the specimens, and thus reduce thermal and mechanical damage.9,204 Diamond is a material that has been shown to be resistant to wear205 and is biocompatible.206 Thus, where possible, this should be used for tool materials. If cylindrical specimens are used, these are commonly cut using coring tools, by milling, or by lathing.9 Keaveny et al207 found that lathing their cylindrical specimens produced clean cut sides, and no additional damage compared with coring the specimens. Some studies recommend machining the samples while frozen to prevent damage,42,68 although there is little supporting evidence for this method. No matter how careful, any process of machining a heterogeneous tissue may lead to potential damage. We want to highlight a key step in the specimen preparation process, which is to inspect visually the specimen surfaces for any damage or unacceptable irregularities before proceeding to the compression test phase.

Testing configuration

It is possible to test bone specimens in confined or unconfined conditions. The latter allows the escape of bone marrow during testing, which reduces the influence of viscoelasticity. Confined testing not only keeps bone marrow in place but also restricts lateral deformation during testing. A study by Linde and Hvid27 looking at the effect of side constraint found that bone specimens tested in confined conditions produce increased values for stiffness compared with results obtained from the same specimen tested in unconfined conditions. Although, arguably, it is more representative to test specimens in constrained conditions, it is clearly difficult during testing to replicate the degree of constraint conferred by neighbouring tissue in vivo. It is thus recommended that, for measuring properties of the bone alone, unconfined testing remain the standard at least to facilitate comparability. This study highlights one of the potential limitations of ex situ techniques such as compression testing, where the results may have limited use clinically.

Platen setup

With traditional platens compression testing, the specimen can be placed between two fixed parallel platens, or a combination of a fixed platen paired with an adjustable platen. This adjustable platen, usually pivoted on a ball bearing, is often used to reduce the effects of specimen non-parallelism and misalignment. This would enable full engagement between the platen surface and specimen ends, and encourages evenly distributed loading during compression.69,77 Overall, with regard to the testing apparatus, the type of machine is unlikely to be a critical factor in relation to the testing results so long as the effects of specimen misalignment, friction, and slippage can be avoided or minimized.

Precautional measures (to improve accuracy)

The surface of the compression platens can be polished and/or lubricated with mineral oil to minimize friction between the platen surface and the specimen surface. This can help reduce the influence of “end effects” and allow for free transverse expansion of the specimen (Poisson’s effect).15,34,36,103 The disadvantage of this, however, is highlighted in preliminary studies by Linde et al26 where the presence of an oil film on the platen resulted in a significant load signal before the specimen had any contact with the compression column. Similarly, the use of latex, Teflon, PMMA cement, or glue to secure the specimens directly to the platen should generally be avoided, if possible, as it is unclear whether these additions have an effect on the mechanical properties measured.208

Endcaps may be made of brass, aluminium alloy, or stainless steel, and specimens are commonly secured within them using PMMA cement, cyanoacrylate glue or latex rubber. These may help to eliminate the effects of specimen slippage, while also providing a suitable homogeneous surface for the attachment of extensometers. This confers the advantage of increased precision.36 Furthermore, the process of embedding the specimens into the endcaps can introduce off-axis tilting or uncontrolled preloading.

Keaveny et al36 published a paper describing several systematic and random errors present when compression testing trabecular bone samples. They reported a systematic underestimation error in the range of 20% to 40% for compression testing of trabecular specimens. They suggested a testing technique aimed at minimizing end effects, which involves embedding the bone specimen in endcaps and using an extensometer to sample in four directions around the specimen. This study shows the beneficial effect of using an external method of strain measurement, and future studies should use this endcap-extensometer technique where possible.

One such case where it may not be possible to use extensometers is with small specimens. Speirs et al116 describe this issue in their study of the effect of sterilization techniques on ear ossicles. The naturally small size of these bones did not allow for use of endcaps or extensometers. They used data obtained from pre-testing on synthetic bone specimens of the same size and under similar conditions to help estimate the reproducibility of their testing technique. However, we suggest that, in these cases, alternative methods of strain measurement such as strain gauges or linear variable differential transformers (LVDTs) can be used to similar effect.

Temperature and environment

The temperature and testing environment can be controlled through use of temperature-controlled baths filled with solution (most commonly saline). These baths are commonly used to regulate the testing temperature to 37°C to emulate in vivo testing conditions. For most studies, the use of saline baths is not necessary, provided that the specimen is not left to dry out on the platen, and the test is carried out within a reasonable time frame.

It is appreciated that the machine setup and environmental condition depend not only on the objectives of the study but also on the resources available to the researcher. Thus, standardization is impractical in this aspect. We suggest that, where possible, any testing method used should be validated against an appropriate material standard with known properties (e.g. rigid plastic) in order to identify and quantify any systematic error present.14 This will enable adjustment to the testing technique to assure accuracy prior to testing.

Testing procedure

Preconditioning or preloading protocols are cyclic loading tests applied before the intended test is carried out. These are used to achieve a steady viscoelastic state and ensure that zero-strain during testing is reproducible by defining the zero-strain at a set preload.7 Preloading and preconditioning also help to ensure that the entire end surface of the bone specimen is uniformly in contact with the platen before testing. These multiple compression cycles may also be used to check for any substantial plastic damage to the specimens by identifying reductions in modulus between the cycles, provided that these cycles are within the elastic range.36

Preconditioning should be carried out if measures have not been taken to eliminate end effects.207 A cyclic, displacement-controlled preconditioning protocol of low strain levels in the range of 0.3% to 0.5%7,207 can be used to minimize irreversible damage to the specimens. Note that this threshold level of preload will differ between specimens and so, for more precision, a protocol where the specimen is cyclically loaded and unloaded until linearity may be used. This can be used to identify the zero-point, i.e. the effective starting point of zero-strain, where the specimen can then be subsequently reloaded for the test.36

Strain measurement

There are a wide variety of techniques for measuring strain, including machine crosshead displacement, strain extensometers, and strain gauges. With the traditional platens testing technique, strain can be easily measured via the motion of the test machine crosshead. This method works on the assumption that the displacement of the platen is identical to the deformation of the specimen. When measuring the relatively small deformations of bone specimens, this assumption introduces error due to deflection of the entire load frame of the machine when under stress. This effect is related to the stiffness of the test machine apparatus and is known as “machine compliance”.209 Thus, studies that use this method of strain measurement should correct for the machine compliance to ensure that they are measuring the strain of the specimen alone. The machine compliance may be determined directly by loading the system without a specimen or with a standard uniform material specimen such as steel with known properties. Augat et al3 reported systematic measurement errors in their study due to the measurement of strain across the machine platens, and not the specimen itself.

Although this method may be adequate, other methods of strain measurement with higher accuracy are necessary to obtain test values within an acceptable limit. Strain is often greater at boundary regions close to the platen than in the middle of cut specimens due to the severed struts of trabeculae on the outer surface. This can lead to overestimation of the average strain across the specimen, and thus a consequent underestimation of modulus.15,30,34 To minimize these end effects, strain is best measured at the middle region of the specimen. This can be achieved using an extensometer, which may be of a contact or non-contact type. Keaveny et al36 recommended an extensometer technique that sampled deformation data from all around the specimen, thus accounting for any potential architectural heterogeneity within the bone specimen. However, there are limitations to measuring strain using extensometers in such bone studies. First, the use of extensometers requires large specimen sizes due to technical difficulties with securing the arms of the extensometer on the surface of small or irregularly shaped specimens. The typically slippery and smooth surfaces of fresh bone specimens further exacerbate these fixation difficulties. Several studies reported errors stemming from slippage of the extensometer, particularly when dealing with wet bone specimens.77,142 Cotton et al168 reported that nearly 20% of their samples tested had unreliable extensometer readings, apparently due to slippage. There may have also been damage to specimens through transverse preload as a result of attaching contact-type extensometers.29

When strain gauges are suitably attached to the test material, the deformation of the strain gauge is assumed to be identical to the deformation of the material. The deformation of the strain gauge leads to changes in electrical resistance that allow digital calculation of strain.210 These can be used singularly for measuring strain in one direction or in the form of rosette strain gauges to measure strain multi-directionally. However, installation of these devices can be difficult when dealing with bone material in terms of specimen surface preparation and choice of adhesive. A common source of error lies in the bonding of the gauge to the test specimen and insufficient specimen surface preparation.210 By technical standards, the specimen surface should be chemically clean and degreased, appropriately rough, and of appropriate pH.211 As imagined, this is difficult or inappropriate when testing organic material such as fresh bone.

An innovative technique for strain measurement is digital image correlation (DIC), an optical, non-contact technique for measuring displacement. The specimen surface is usually painted or sprayed to produce a high-contrast speckle pattern. DIC works by tracking the pixels of serial digital photographs taken of the painted surface at different stages of deformation. Here, the DIC system is capable of taking the influences of end effects into account and has the potential for full-field strain measurement.210 However, measurements are limited to the accuracy and resolution of the DIC system and authors highlighted limitations with using acrylic paint for surface preparation.140 For example, paint that had penetrated into the pores could have been carrying applied loads or obstructing marrow flow, and thus could affect mechanical behaviour.140

Each method of strain measurement has its advantages and disadvantages and, ultimately, the method used should depend on the objective of the study. Where relative values are sought, traditional crosshead displacement measurement of strain is sufficient and is quick and simple to implement. It also places fewest restrictions on the specimen, with no need for large-sized specimens or surface preparation to facilitate attachment of extensometers or strain gauges. Although the effect of machine compliance may be negligible when testing relatively compliant orthopaedic samples, it is strongly recommended that investigators still correct for this error. If absolute values are of interest in the study, then extensometers should be used to improve the accuracy of strain measurement as discussed above. If localized strain changes are of interest to the researcher, strain gauges can be used. Digital image correlation is a method that would be most useful in studies interested in full-field strain measurements (e.g. whole bone fracture analysis).212 Further studies using DIC on ex vivo bone samples are required before reliability of this method can be assessed.

Strain rate

Strain rate is strain change (deformation) per unit of time. Testing strain rate is an important factor to consider when measuring the mechanical properties of biological materials. The strain rate used may vary depending on the nature of the experiment, i.e. within normal physiological range or higher strain rates for simulating trauma and impact.16 Physiological strain rates are considered to be within the range of 0.005 s-1 and 0.08 s-1, and the majority of studies use rates that fall within this range.183 The studies which tested at substantially higher strain rates16,26,68,159,161 were studying high-impact situations.

Wet bone exhibits “viscoelastic” or strain rate-dependent behaviour due to the complex, multi-phase, porous structure of bone where fluid present in the bone matrix effectively acts as a “shock absorber”.135,213 Internal friction between the fluid phase, i.e. bone marrow, and the solid phase, i.e. mineral matrix, leads to losses of elastic energy.14,52 This viscoelastic effect has been shown to have the greatest influence at higher strain rates (greater than 10 s-1) in confined boundary conditions where the marrow cannot move freely.26,52 Studies by Wells and Rawlings130 and Linde et al26 showed that the stiffness of trabecular bone increased as the testing strain rate increased. Hansen et al16 have experimentally demonstrated a similar effect when testing cortical bone. They tested at moderate to high strain rates, as this was more representative of the strain rates encountered during traumatic events that resulted in bone fractures.

Due to viscoelasticity, the most accurate modulus values are obtained at very low strain rates, i.e. rates that are considered “quasistatic”.25 It is suggested that a critical strain rate exists at which moduli values increase, although there is no definitive consensus in the literature.16,161 Clearly, compressing specimens at infinitely low strain rates would be impractical and inappropriate. At excessively slow loading durations over long periods of time, materials will suffer from creep deformation, a phenomenon which will also affect the measured modulus. Thus, we recommend a testing strain rate range of between 0.001 s-1 and 0.1 s-1 to be used where strain rate is not the studied factor. A strain rate within this range should be sufficient to minimize creep whilst still low enough to be considered quasistatic.214 Again, researchers should bear in mind their objectives as testing at these low strain rates may not be representative of the dynamic or physiological strains present in vivo,183 and many of the studies in the literature purposefully test at moderate or high strain rates. All studies should report the strain rate used to facilitate comparability.

In conclusion, variations in methodology for compression testing of bone across the literature due to lack of standardization in testing technique have made comparability and interpretation of current studies difficult.15 This paper aimed to review the literature systematically in order to determine how best to perform compression testing of human bone to help develop a standardized testing technique for future studies. The American Society for Testing Materials (ASTM) designations for compressive testing provide a current source of guidance for mechanical testing technique, but adaptations for use with bone tissue are necessary.203

We recommend that the testing protocol shown in Figure 4 should be used as a guide in conducting compression tests of human bone to obtain stiffness values. The following key factors in compression testing should be noted:

Fig. 4 Recommended testing protocol for measurement of bone modulus. DIC, Digital Image Correlation; LVDT, Linear Variable Differential Transformer.

Fig. 4

Recommended testing protocol for measurement of bone modulus. DIC, Digital Image Correlation; LVDT, Linear Variable Differential Transformer.

  • Orientation during extraction of the specimen must be carefully considered to ensure correct anatomical alignment.

  • Specimen geometry is important, and cylindrical bone cores with aspect ratios less than two are preferred.

  • Use of fresh, wet, and unconfined specimens stored in physiological saline is recommended.

  • The method of strain measurement should be carefully considered, taking into account the size and quality of the specimens.

  • The strain range and fit used to determine the apparent modulus must be carefully considered due to the non-linear and plastic nature of bone.

  • Strain rates of less than 0.1 s-1 should be used with preconditioning cycles.

  • Care should be taken with the testing configuration, with measures taken to minimize friction, specimen slippage, and misalignment.

  • Where possible, the testing protocol should be carried out on known materials to identify systematic errors, and for calibration purposes.

  • There should be clear and detailed reporting of the testing methodology and technique of data analysis.

It is important that any inter-study comparison take into account the specimen geometry, specimen-platen interface conditions, and specimen machining technique.15 Further studies are required to look specifically at the effect of factors such as specimen geometry, storage, boundary conditions, and strain rate on human bone apparent modulus. These will help to refine a standardized and optimal testing method for future compression testing of bone.

S. Zhao; email:
Author Contributions

S. Zhao: Study retrieval, Writing the manuscript.

M. Arnold: Study retrieval, Editing the manuscript.

S. Ma: Creating the figures, Editing the manuscript.

R. L. Abel: Editing the manuscript.

J. P. Cobb: Editing the manuscript.

U. Hansen: Editing the manuscript.

O. Boughton: Review proposal, Writing the manuscript.

Open access

This is an open-access article distributed under the terms of the Creative Commons Attributions licence (CC-BY-NC), which permits unrestricted use, distribution, and reproduction in any medium, but not for commercial gain, provided the original author and source are credited.

  • Supplementary material

    Tables showing characteristics for all studies included in qualitative synthesis.

  • Funding Statement

    This work was supported by The UK National Institute for Health Research (NIHR) Imperial College Biomedical Research Centre (NIHR Imperial BRC) [RDB0479560], The Michael Uren Foundation [WSSU_NCN011], The Royal College of Surgeons of England [WSSU_P63898], and the Dunhill Medical Trust [WSSU_P63898].

  • Conflict of Interest Statement

    None declared

    • Follow us @BoneJointRes

    References

    1. Miles AW , Gheduzzi S . Basic biomechanics and biomaterials. Surg2012;30:86–91. Google Scholar

    2. Rubash HE , Sinha RK , Shanbhag AS , Kim SY . Pathogenesis of bone loss after total hip arthroplasty. Orthop Clin North Am1998;29:173–186.CrossrefPubMed Google Scholar

    3. Augat P , Link T , Lang TF et al. . Anisotropy of the elastic modulus of trabecular bone specimens from different anatomical locations. Med Eng Phys1998;20:124–131.CrossrefPubMed Google Scholar

    4. Nazarian A , Von Stechow D , Zurakowski D , Müller R , Snyder BD . Bone volume fraction explains the variation in strength and stiffness of cancellous bone affected by metastatic cancer and osteoporosis. Calcif Tissue Int2008;83:368–379.CrossrefPubMed Google Scholar

    5. Ciarallo A , Barralet J , Tanzer M , Kremer R . An approach to compare the quality of cancellous bone from the femoral necks of healthy and osteoporotic patients through compression testing and microcomputed tomography imaging. Mcgill J Med2006;9:102–107.PubMed Google Scholar

    6. El Masri F , Sapin de Brosses E , Rhissassi K , Skalli W , Mitton D . Apparent Young’s modulus of vertebral cortico-cancellous bone specimens. Comput Methods Biomech Biomed Engin2012;15:23–28. Google Scholar

    7. Linde F , Gøthgen CB , Hvid I , Pongsoipetch B . Mechanical properties of trabecular bone by a non-destructive compression testing approach. Eng Med1988;17:23–29.CrossrefPubMed Google Scholar

    8. Bayraktar HH , Morgan EF , Niebur GL et al. . Comparison of the elastic and yield properties of human femoral trabecular and cortical bone tissue. J Biomech2004;37:27–35.CrossrefPubMed Google Scholar

    9. An YH , Draughn RA . Mechanical Testing of Bone and the Bone-Implant Interface. First ed. Boca Raton: CRC Press, 1999. Google Scholar

    10. Røhl L , Larsen E , Linde F , Odgaard A , Jørgensen J . Tensile and compressive properties of cancellous bone. J Biomech1991;24:1143–1149.CrossrefPubMed Google Scholar

    11. Donnelly E . Methods for assessing bone quality: a review. Clin Orthop Relat Res2011;469:2128–2138.CrossrefPubMed Google Scholar

    12. Pal S . Mechanical properties of biological materials. In: PalS, ed. Design of Artificial Human Joints & Organs. USA: Springer, 2014:23–40. Google Scholar

    13. Ma S , Goh EL , Jin A et al. . Long-term effects of bisphosphonate therapy: perforations, microcracks and mechanical properties. Sci Rep2017;7:43399.CrossrefPubMed Google Scholar

    14. Turner CH , Burr DB . Basic biomechanical measurements of bone: a tutorial. Bone1993;14:595–608.CrossrefPubMed Google Scholar

    15. Keaveny TM , Borchers RE , Gibson LJ , Hayes WC . Theoretical analysis of the experimental artifact in trabecular bone compressive modulus. J Biomech1993;26:599–607.CrossrefPubMed Google Scholar

    16. Hansen U , Zioupos P , Simpson R , Currey JD , Hynd D . The effect of strain rate on the mechanical properties of human cortical bone. J Biomech Eng2008;130:011011.CrossrefPubMed Google Scholar

    17. Moher D , Liberati A , Tetzlaff J , Altman DG PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med2009;151:264–269.CrossrefPubMed Google Scholar

    18. Higgins JPT , Green S . Cochrane Handbook for Systematic Reviews of Interventions: Cochrane Book Series. Chichester: John Wiley & Sons, 2008. Google Scholar

    19. Bevill G , Eswaran SK , Farahmand F , Keaveny TM . The influence of boundary conditions and loading mode on high-resolution finite element-computed trabecular tissue properties. Bone2009;44:573–578.CrossrefPubMed Google Scholar

    20. Birnbaum K , Sindelar R , Gaertner JR , Wirtz DC . Material properties of trabecular bone structures. Surg Radiol Anat2001;23:399–407.CrossrefPubMed Google Scholar

    21. Conrad EU , Ericksen DP , Tencer AF , Strong DM , Mackenzie AP . The effects of freeze-drying and rehydration on cancellous bone. Clin Orthop Relat Res1993;290:279–284.PubMed Google Scholar

    22. Linde F , Sørensen HCF . The effect of different storage methods on the mechanical properties of trabecular bone. J Biomech1993;26:1249–1252.CrossrefPubMed Google Scholar

    23. Linde F , Pongsoipetch B , Frich LH , Hvid I . Three-axial strain controlled testing applied to bone specimens from the proximal tibial epiphysis. J Biomech1990;23:1167–1172.CrossrefPubMed Google Scholar

    24. Linde F , Hvid I , Madsen F . The effect of specimen geometry on the mechanical behaviour of trabecular bone specimens. J Biomech1992;25:359–368.CrossrefPubMed Google Scholar

    25. Linde F , Hvid I . Stiffness behaviour of trabecular bone specimens. J Biomech1987;20:83–89.CrossrefPubMed Google Scholar

    26. Linde F , Nørgaard P , Hvid I , Odgaard A , Søballe K . Mechanical properties of trabecular bone. Dependency on strain rate. J Biomech1991;24:803–809.CrossrefPubMed Google Scholar

    27. Linde F , Hvid I . The effect of constraint on the mechanical behaviour of trabecular bone specimens. J Biomech1989;22:485–490.CrossrefPubMed Google Scholar

    28. Morgan EF , Yeh OC , Keaveny TM . Damage in trabecular bone at small strains. Eur J Morphol2005;42:13–21.CrossrefPubMed Google Scholar

    29. Morgan EF , Yeh OC , Chang WC , Keaveny TM . Nonlinear behavior of trabecular bone at small strains. J Biomech Eng2001;123:1–9.CrossrefPubMed Google Scholar

    30. Odgaard A , Linde F . The underestimation of Young’s modulus in compressive testing of cancellous bone specimens. J Biomech1991;24:691–698. Google Scholar

    31. Öhman C , Dall’Ara E , Baleani M , Van Sint Jan S , Viceconti M . The effects of embalming using a 4% formalin solution on the compressive mechanical properties of human cortical bone. Clin Biomech (Bristol, Avon)2008;23:1294–1298.CrossrefPubMed Google Scholar

    32. Öhman C , Baleani M , Perilli E et al. . Mechanical testing of cancellous bone from the femoral head: experimental errors due to off-axis measurements. J Biomech2007;40:2426–2433.CrossrefPubMed Google Scholar

    33. Yahia LH , Drouin G , Duval P . A methodology for mechanical measurements of technical constants of trabecular bone. Eng Med1988;17:169–173.CrossrefPubMed Google Scholar

    34. Zhu M , Keller TS , Spengler DM . Effects of specimen load-bearing and free surface layers on the compressive mechanical properties of cellular materials. J Biomech1994;27:57–66.CrossrefPubMed Google Scholar

    35. Keaveny TM , Wachtel EF , Kopperdahl DL . Mechanical behavior of human trabecular bone after overloading. J Orthop Res1999;17:346–353.CrossrefPubMed Google Scholar

    36. Keaveny TM , Pinilla TP , Crawford RP , Kopperdahl DL , Lou A . Systematic and random errors in compression testing of trabecular bone. J Orthop Res1997;15:101–110.CrossrefPubMed Google Scholar

    37. Anderson MJ , Keyak JH , Skinner HB . Compressive mechanical properties of human cancellous bone after gamma irradiation. J Bone Joint Surg [Am]1992;74-A:747-752.PubMed Google Scholar

    38. Badiei A , Bottema MJ , Fazzalari NL . Influence of orthogonal overload on human vertebral trabecular bone mechanical properties. J Bone Miner Res2007;22:1690–1699.CrossrefPubMed Google Scholar

    39. Banse X , Delloye C , Cornu O , Bourgois R . Comparative left-right mechanical testing of cancellous bone from normal femoral heads. J Biomech1996;29:1247–1253.CrossrefPubMed Google Scholar

    40. Banse X , Sims TJ , Bailey AJ . Mechanical properties of adult vertebral cancellous bone: correlation with collagen intermolecular cross-links. J Bone Miner Res2002;17:1621–1628.CrossrefPubMed Google Scholar

    41. Baroud G , Nemes J , Ferguson SJ , Steffen T . Material changes in osteoporotic human cancellous bone following infiltration with acrylic bone cement for a vertebral cement augmentation. Comput Methods Biomech Biomed Engin2003;6:133–139.CrossrefPubMed Google Scholar

    42. Bentzen SM , Hvid I , Jørgensen J . Mechanical strength of tibial trabecular bone evaluated by X-ray computed tomography. J Biomech1987;20:743-752.CrossrefPubMed Google Scholar

    43. Bollerslev J , Mosekilde L , Nielsen HK , Mosekilde L . Biomechanical competence of iliac crest trabecular bone in autosomal dominant osteopetrosis type I. Bone1989;10:159–164.CrossrefPubMed Google Scholar

    44. Bosisio MR , Talmant M , Skalli W , Laugier P , Mitton D . Apparent Young’s modulus of human radius using inverse finite-element method. J Biomech2007;40:2022–2028. Google Scholar

    45. Bourgnon A , Sitzer A , Chabraborty A et al. . Impact of microscale properties measured by 50-MHz acoustic microscopy on mesoscale elastic and ultimate mechanical cortical bone properties. IEEE Int Ultrason Symp IUS, 2014;636–638. Google Scholar

    46. Brown TD , Ferguson AB Jr . Mechanical property distributions in the cancellous bone of the human proximal femur. Acta Orthop Scand1980;51:429–437.CrossrefPubMed Google Scholar

    47. Brown TD , Way ME , Ferguson AB Jr . Mechanical characteristics of bone in femoral capital aseptic necrosis. Clin Orthop Relat Res1981;156:240–247.PubMed Google Scholar

    48. Brown SJ , Pollintine P , Powell DE , Davie MWJ , Sharp CA . Regional differences in mechanical and material properties of femoral head cancellous bone in health and osteoarthritis. Calcif Tissue Int2002;71:227–234.CrossrefPubMed Google Scholar

    49. Burgers TA , Mason J , Niebur G , Ploeg HL . Compressive properties of trabecular bone in the distal femur. J Biomech2008;41:1077–1085.CrossrefPubMed Google Scholar

    50. Caler WE , Carter DR . Bone creep-fatigue damage accumulation. J Biomech1989;22:625–635.CrossrefPubMed Google Scholar

    51. Carter DR , Schwab GH , Spengler DM . Tensile fracture of cancellous bone. Acta Orthop1980;51:733–741.CrossrefPubMed Google Scholar

    52. Carter DR , Hayes WC . The compressive behavior of bone as a two-phase porous structure. J Bone Joint Surg [Am]1977;59-A:954–962.PubMed Google Scholar

    53. Cendre E , Mitton D , Roux J-P , Arlot ME , Duboeuf F , Burt-Pichat B , Rumelhart C , Peix G , Meunier PJ . High-resolution computed tomography for architectural characterization of human lumbar cancellous bone: relationships with histomorphometry and biomechanics. Osteoporos Int1999;10:353–360.CrossrefPubMed Google Scholar

    54. Cezayirlioglu H , Bahniuk E , Davy DT , Heiple KG . Anisotropic yield behavior of bone under combined axial force and torque. J Biomech1985;18:61–69.CrossrefPubMed Google Scholar

    55. Charlebois M , Pretterklieber M , Zysset PK . The role of fabric in the large strain compressive behavior of human trabecular bone. J Biomech Eng2010;132:121006.CrossrefPubMed Google Scholar

    56. Sneppen O , Christensen P , Larsen H , Vang PS . Mechanical testing of trabecular bone in knee replacement. Int Orthop1981;5:251–256.CrossrefPubMed Google Scholar

    57. Ciarelli MJ , Goldstein SA , Kuhn JL , Cody DD , Brown MB . Evaluation of orthogonal mechanical properties and density of human trabecular bone from the major metaphyseal regions with materials testing and computed tomography. J Orthop Res1991;9:674–682.CrossrefPubMed Google Scholar

    58. Cody DD , McCubbrey DA , Divine GW , Gross GJ , Goldstein SA . Predictive value of proximal femoral bone densitometry in determining local orthogonal material properties. J Biomech1996;29:753–761.CrossrefPubMed Google Scholar

    59. Cornu O , Boquet J , Nonclercq O et al. . Synergetic effect of freeze-drying and gamma irradiation on the mechanical properties of human cancellous bone. Cell Tissue Bank2011;12:281–288.CrossrefPubMed Google Scholar

    60. Deligianni DD , Maris A , Missirlis YF . Stress relaxation behaviour of trabecular bone specimens. J Biomech1994;27:1469–1476.CrossrefPubMed Google Scholar

    61. Ding M , Dalstra M , Danielsen CC et al. . Age variations in the properties of human tibial trabecular bone. J Bone Joint Surg [Br]1997;79-B:995–1002.CrossrefPubMed Google Scholar

    62. Ding M , Danielsen CC , Hvid I . Bone density does not reflect mechanical properties in early-stage arthrosis. Acta Orthop Scand2001;72:181–185. Google Scholar

    63. Ding M , Danielsen CC , Hvid I , Overgaard S . Three-dimensional microarchitecture of adolescent cancellous bone. Bone2012;51:953–960.CrossrefPubMed Google Scholar

    64. Ding M , Odgaard A , Linde F , Hvid I . Age-related variations in the microstructure of human tibial cancellous bone. J Orthop Res2002;20:615–621.CrossrefPubMed Google Scholar

    65. Dong XN , Acuna RL , Luo Q , Wang X . Orientation dependence of progressive post-yield behavior of human cortical bone in compression. J Biomech2012;45:2829–2834.CrossrefPubMed Google Scholar

    66. Du C , Ma H , Ruo M et al. . An experimental study on the biomechanical properties of the cancellous bones of distal femur. Biomed Mater Eng2006;16:215–222.PubMed Google Scholar

    67. Duchemin L , Bousson V , Raossanaly C et al. . Prediction of mechanical properties of cortical bone by quantitative computed tomography. Med Eng Phys2008;30:321–328.CrossrefPubMed Google Scholar

    68. Ducheyne P , Heymans L , Martens M et al. . The mechanical behaviour of intracondylar cancellous bone of the femur at different loading rates. J Biomech1977;10:747–762.CrossrefPubMed Google Scholar

    69. Fazzalari NL , Forwood MR , Smith K , Manthey BA , Herreen P . Assessment of cancellous bone quality in severe osteoarthrosis: bone mineral density, mechanics, and microdamage. Bone1998;22:381–388.CrossrefPubMed Google Scholar

    70. Follet H , Bruyère-Garnier K , Peyrin F et al. . Relationship between compressive properties of human os calcis cancellous bone and microarchitecture assessed from 2D and 3D synchrotron microtomography. Bone2005;36:340-351.CrossrefPubMed Google Scholar

    71. Follet H , Boivin G , Rumelhart C , Meunier PJ . The degree of mineralization is a determinant of bone strength: a study on human calcanei. Bone2004;34:783–789.CrossrefPubMed Google Scholar

    72. Follet H , Peyrin F , Vidal-Salle E et al. . Intrinsic mechanical properties of trabecular calcaneus determined by finite-element models using 3D synchrotron microtomography. J Biomech2007;40:2174–2183.CrossrefPubMed Google Scholar

    73. Follet H , Viguet-Carrin S , Burt-Pichat B et al. . Effects of preexisting microdamage, collagen cross-links, degree of mineralization, age, and architecture on compressive mechanical properties of elderly human vertebral trabecular bone. J Orthop Res2011;29:481–488.CrossrefPubMed Google Scholar

    74. Goldstein SA , Wilson DL , Sonstegard DA , Matthews LS . The mechanical properties of human tibial trabecular bone as a function of metaphyseal location. J Biomech1983;16:965–969.CrossrefPubMed Google Scholar

    75. Goulet RW , Goldstein SA , Ciarelli MJ et al. . The relationship between the structural and orthogonal compressive properties of trabecular bone. J Biomech1994;27:375-389.CrossrefPubMed Google Scholar

    76. Haddock SM , Yeh OC , Mummaneni PV , Rosenberg WS , Keaveny TM . Similarity in the fatigue behavior of trabecular bone across site and species. J Biomech2004;37:181–187.CrossrefPubMed Google Scholar

    77. Hernandez CJ , Lambers FM , Widjaja J , Chapa C , Rimnac CM . Quantitative relationships between microdamage and cancellous bone strength and stiffness. Bone2014;66:205–213.CrossrefPubMed Google Scholar

    78. Hvid I . Cancellous bone at the knee: a comparison of two methods of strength measurement. Arch Orthop Trauma Surg1985;104:211–217.CrossrefPubMed Google Scholar

    79. Hvid I , Christensen P , Søondergaard J , Christensen PB , Larsen CG . Compressive strength of tibial cancellous bone: Instron and osteopenetrometer measurements in an autopsy material. Acta Orthop Scand1983;54:819–825. Google Scholar

    80. Hvid I , Jensen J . Cancellous bone strength at the proximal human tibia. Eng Med1984;13:21–25.CrossrefPubMed Google Scholar

    81. Hvid I , Bentzen SM , Linde F , Mosekilde L , Pongsoipetch B . X-ray quantitative computed tomography: the relations to physical properties of proximal tibial trabecular bone specimens. J Biomech1989;22:837–844.CrossrefPubMed Google Scholar

    82. Imbert L , Aurégan J-C , Pernelle K , Hoc T . Microstructure and compressive mechanical properties of cortical bone in children with osteogenesis imperfecta treated with bisphosphonates compared with healthy children. J Mech Behav Biomed Mater2015;46:261–270.CrossrefPubMed Google Scholar

    83. Jensen NC , Hvid I , Krøner K . Strength pattern of cancellous bone at the ankle joint. Eng Med1988;17:71–76.CrossrefPubMed Google Scholar

    84. Jensen NC , Madsen LP , Linde F . Topographical distribution of trabecular bone strength in the human os calcanei. J Biomech1991;24:49–55.CrossrefPubMed Google Scholar

    85. Jones AA , Dougherty PJ , Sharkey NA , Benson DR . Iliac crest bone graft. Osteotome versus saw. Spine1993;18(Suppl):2048–2052.CrossrefPubMed Google Scholar

    86. Kalouche I , Crépin J , Abdelmoumen S et al. . Mechanical properties of glenoid cancellous bone. Clin Biomech (Bristol, Avon)2010;25:292–298.CrossrefPubMed Google Scholar

    87. Karim L , Vashishth D . Heterogeneous glycation of cancellous bone and its association with bone quality and fragility. PLoS One2012;7:e35047.CrossrefPubMed Google Scholar

    88. Keller TS . Predicting the compressive mechanical behavior of bone. J Biomech1994;27:1159–1168.CrossrefPubMed Google Scholar

    89. Keyak JH , Lee IY , Nath DS , Skinner HB . Postfailure compressive behavior of tibial trabecular bone in three anatomic directions. J Biomed Mater Res1996;31:373–378.CrossrefPubMed Google Scholar

    90. Kopperdahl DL , Keaveny TM . Yield strain behavior of trabecular bone. J Biomech1998;31:601–608.CrossrefPubMed Google Scholar

    91. Leichter I , Bivas A , Margulies JY , Roman I , Simkin A . Acoustic emission from trabecular bone during mechanical testing: the effect of osteoporosis and osteoarthritis. Proc Inst Mech Eng Part H1990;204:123–127.CrossrefPubMed Google Scholar

    92. Li Z-C , Dai L-Y , Jiang L-S , Qiu S . Difference in subchondral cancellous bone between postmenopausal women with hip osteoarthritis and osteoporotic fracture: implication for fatigue microdamage, bone microarchitecture, and biomechanical properties. Arthritis Rheum2012;64:3955–3962.CrossrefPubMed Google Scholar

    93. Linde F , Hvid I , Jensen NC . Material properties of cancellous bone in repetitive axial loading. Eng Med1985;14:173–177.CrossrefPubMed Google Scholar

    94. Macneil JA , Boyd SK . Bone strength at the distal radius can be estimated from high-resolution peripheral quantitative computed tomography and the finite element method. Bone2008;42:1203–1213.CrossrefPubMed Google Scholar

    95. Martens M , Van Audekercke R , Delport P , De Meester P , Mulier JC . The mechanical characteristics of cancellous bone at the upper femoral region. J Biomech1983;16:971–983.CrossrefPubMed Google Scholar

    96. Martin H , Werner J , Andresen R , Schober H-C , Schmitz K-P . Noninvasive assessment of stiffness and failure load of human vertebrae from CT-data. Biomed Tech (Berl)1998;43:82–88.CrossrefPubMed Google Scholar

    97. Matsuura M , Eckstein F , Lochmüller E-M , Zysset PK . The role of fabric in the quasi-static compressive mechanical properties of human trabecular bone from various anatomical locations. Biomech Model Mechanobiol2008;7:27–42.CrossrefPubMed Google Scholar

    98. Misch CE , Qu Z , Bidez MW . Mechanical properties of trabecular bone in the human mandible: implications for dental implant treatment planning and surgical placement. J Oral Maxillofac Surg1999;57:700–706.CrossrefPubMed Google Scholar

    99. Morgan EF , Keaveny TM . Dependence of yield strain of human trabecular bone on anatomic site. J Biomech2001;34:569–577.CrossrefPubMed Google Scholar

    100. Murdoch AH , Mathias KJ , Shepherd DET . Investigation into the material properties of beech wood and cortical bone. Biomed Mater Eng2004;14:1–4.PubMed Google Scholar

    101. Nicholson PHF , Cheng XG , Lowet G et al. . Structural and material mechanical properties of human vertebral cancellous bone. Med Eng Phys1997;19:729–737.CrossrefPubMed Google Scholar

    102. Njeh CF , Kuo CW , Langton CM , Atrah HI , Boivin CM . Prediction of human femoral bone strength using ultrasound velocity and BMD: an in vitro study. Osteoporos Int1997;7:471–477.CrossrefPubMed Google Scholar

    103. Odgaard A , Hvid I , Linde F . Compressive axial strain distributions in cancellous bone specimens. J Biomech1989;22:829–835.CrossrefPubMed Google Scholar

    104. O’Mahony AM , Williams JL , Katz JO , Spencer P . Anisotropic elastic properties of cancellous bone from a human edentulous mandible. Clin Oral Implants Res2000;11:415–421.CrossrefPubMed Google Scholar

    105. Ouyang J , Yang GT , Wu WZ , Zhu QA , Zhong SZ . Biomechanical characteristics of human trabecular bone. Clin Biomech (Bristol, Avon)1997;12:522–524.CrossrefPubMed Google Scholar

    106. Pattin CA , Caler WE , Carter DR . Cyclic mechanical property degradation during fatigue loading of cortical bone. J Biomech1996;29:69–79.CrossrefPubMed Google Scholar

    107. Portero-Muzy NR , Chavassieux PM , Mitton D et al. . Euler(strut.cavity), a new histomorphometric parameter of connectivity reflects bone strength and speed of sound in trabecular bone from human os calcis. Calcif Tissue Int2007;81:92–98.CrossrefPubMed Google Scholar

    108. Poukalova M , Yakacki CM , Guldberg RE et al. . Pullout strength of suture anchors: effect of mechanical properties of trabecular bone. J Biomech2010;43:1138–1145.CrossrefPubMed Google Scholar

    109. Poumarat G , Squire P , Dabonneville M . Comparison of mechanical properties of human, bovine bone and a new processed bone xenograft. Biomaterials1993;14:337–340.CrossrefPubMed Google Scholar

    110. Rauh J , Despang F , Baas J et al. . Comparative biomechanical and microstructural analysis of native versus peracetic acid-ethanol treated cancellous bone graft. Biomed Res Int2014;2014:784702.CrossrefPubMed Google Scholar

    111. Reilly DT , Burstein AH . The elastic and ultimate properties of compact bone tissue. J Biomech1975;8:393-405.CrossrefPubMed Google Scholar

    112. Reilly DT , Burstein AH , Frankel VH . The elastic modulus for bone. J Biomech1974;7:271-275. Google Scholar

    113. Rincón-Kohli L , Zysset PK . Multi-axial mechanical properties of human trabecular bone. Biomech Model Mechanobiol2009;8:195–208.CrossrefPubMed Google Scholar

    114. Rodrigues AM , Caetano-Lopes J , Vale AC et al. . Low osteocalcin/collagen type I bone gene expression ratio is associated with hip fragility fractures. Bone2012;51:981–989.CrossrefPubMed Google Scholar

    115. Sierpowska J , Hakulinen M , Töyräs J et al. . Prediction of mechanical properties of human trabecular bone by electrical measurements. Physiol Meas2005;26:S119–S131.CrossrefPubMed Google Scholar

    116. Speirs AD , Hotz MA , Oxland TR , Häusler R , Nolte L-P . Biomechanical properties of sterilized human auditory ossicles. J Biomech1999;32:485–491.CrossrefPubMed Google Scholar

    117. Steinhauser E , Diehl P , Hadaller M et al. . Biomechanical investigation of the effect of high hydrostatic pressure treatment on the mechanical properties of human bone. J Biomed Mater Res B Appl Biomater2006;76:130–135.CrossrefPubMed Google Scholar

    118. Stoppie N , Pattijn V , Van Cleynenbreugel T et al. . Structural and radiological parameters for the characterization of jawbone. Clin Oral Implants Res2006;17:124–133.CrossrefPubMed Google Scholar

    119. Stoppie N , Van Cleynenbreugel T , Wevers M , Vander Sloten J , Naert I . The validation of a compression testing method for cancellous human jawbone by high-resolution finite element modeling. Int J Oral Maxillofac Implants2007;22:436–445.PubMed Google Scholar

    120. Sugita H , Oka M , Toguchida J et al. . Anisotropy of osteoporotic cancellous bone. Bone1999;24:513–516.CrossrefPubMed Google Scholar

    121. Sun S-S , Ma H-L , Liu C-L et al. . Difference in femoral head and neck material properties between osteoarthritis and osteoporosis. Clin Biomech (Bristol, Avon)2008;23:S39–S47.CrossrefPubMed Google Scholar

    122. Thurner PJ , Erickson B , Turner P et al. . The effect of NaF in vitro on the mechanical and material properties of trabecular and cortical bone. Adv Mater2009;21:451–457. Google Scholar

    123. Vale AC , Aleixo IP , Lúcio M et al. . At the moment of occurrence of a fragility hip fracture, men have higher mechanical properties values in comparison with women. BMC Musculoskelet Disord2013;14:295.CrossrefPubMed Google Scholar

    124. Vale AC , Pereira MFC , Maurício A et al. . Micro-computed tomography and compressive characterization of trabecular bone. Colloids Surf A Physicochem Eng Asp2013;438:199–205. Google Scholar

    125. Vardakastani V , Saletti D , Skalli W et al. . Increased intra-cortical porosity reduces bone stiffness and strength in pediatric patients with osteogenesis imperfecta. Bone2014;69:61–67.CrossrefPubMed Google Scholar

    126. Vastel L , Meunier A , Siney H , Sedel L , Courpied J-P . Effect of different sterilization processing methods on the mechanical properties of human cancellous bone allografts. Biomaterials2004;25:2105–2110.CrossrefPubMed Google Scholar

    127. Wachter NJ , Augat P , Krischak GD et al. . Prediction of strength of cortical bone in vitro by microcomputed tomography. Clin Biomech (Bristol, Avon)2001;16:252–256.CrossrefPubMed Google Scholar

    128. Wachter NJ , Augat P , Mentzel M et al. . Predictive value of bone mineral density and morphology determined by peripheral quantitative computed tomography for cancellous bone strength of the proximal femur. Bone2001;28:133–139.CrossrefPubMed Google Scholar

    129. Wachter NJ , Krischak GD , Mentzel M et al. . Correlation of bone mineral density with strength and microstructural parameters of cortical bone in vitro. Bone2002;31:90–95.CrossrefPubMed Google Scholar

    130. Wells JG , Rawlings RD . Acoustic emission and mechanical properties of trabecular bone. Biomaterials1985;6:218–224.CrossrefPubMed Google Scholar

    131. Wu Z , Laneve AJ , Niebur GL . In vivo microdamage is an indicator of susceptibility to initiation and propagation of microdamage in human femoral trabecular bone. Bone2013;55:208–215.CrossrefPubMed Google Scholar

    132. Yamamoto E , Paul Crawford R , Chan DD , Keaveny TM . Development of residual strains in human vertebral trabecular bone after prolonged static and cyclic loading at low load levels. J Biomech2006;39:1812–1818.CrossrefPubMed Google Scholar

    133. Zhou B , Liu XS , Wang J et al. . Dependence of mechanical properties of trabecular bone on plate-rod microstructure determined by individual trabecula segmentation (ITS). J Biomech2014;47:702–708.CrossrefPubMed Google Scholar

    134. Cesar R , Leivas TP , Augusto C et al. . Axial compressive strength of human vertebrae trabecular bones classified as normal, osteopenic and osteoporotic by quantitative ultrasonometry of calcaneus. Res Biomed Eng2017;33:91–96. Google Scholar

    135. Samuel J , Park JS , Almer J , Wang X . Effect of water on nanomechanics of bone is different between tension and compression. J Mech Behav Biomed Mater2016;57:128–138.CrossrefPubMed Google Scholar

    136. Mirzaali MJ , Schwiedrzik JJ , Thaiwichai S et al. . Mechanical properties of cortical bone and their relationships with age, gender, composition and microindentation properties in the elderly. Bone2015;93:196–211.CrossrefPubMed Google Scholar

    137. Ozan F , Pekedis M , Koyuncu S¸ et al. . Micro-computed tomography and mechanical evaluation of trabecular bone structure in osteopenic and osteoporotic fractures. J Orthop Surg (Hong Kong)2017;25:2309499017692718.CrossrefPubMed Google Scholar

    138. Erivan R , Villatte G , Cueff R , Boisgard S , Descamps BS . Rehydration improves the ductility of dry bone allografts. Cell Tissue Bank2017;18:307-312.CrossrefPubMed Google Scholar

    139. Li J , Huang S , Tang Y , Wang X , Pan T . Biomechanical analysis of the posterior bony column of the lumbar spine. J Orthop Surg Res2017;12:132.CrossrefPubMed Google Scholar

    140. Cyganik Ł , Binkowski M , Kokot G et al. . Prediction of Young’s modulus of trabeculae in microscale using macro-scale’s relationships between bone density and mechanical properties. J Mech Behav Biomed Mater2014;36:120–134. Google Scholar

    141. Jia-ju S , Jie G , Fu-Zhao H . The compressive properties of long bones. Appl Math Mech1981;2:733–742. Google Scholar

    142. Öhman C , Baleani M , Pani C et al. . Compressive behaviour of child and adult cortical bone. Bone2011;49:769–776.CrossrefPubMed Google Scholar

    143. Rao S , McKellop H , Chao D et al. . Biomechanical comparison of bone graft used in anterior spinal reconstruction. Freeze-dried demineralized femoral segments versus fresh fibular segments and tricortical iliac blocks in autopsy specimens. Clin Orthop Relat Res1993;289:131–135.PubMed Google Scholar

    144. Perilli E , Baleani M , Öhman C et al. . Dependence of mechanical compressive strength on local variations in microarchitecture in cancellous bone of proximal human femur. J Biomech2008;41:438–446.CrossrefPubMed Google Scholar

    145. Cyganik Ł , Binkowski M , Kokot G et al. . Microscale’s relationship between Young’s modulus and tissue density. Prediction of displacements. Comput Methods Biomech Biomed Engin2017;20:1658-1668. Google Scholar

    146. Mosekilde L , Mosekilde L , Danielsen CC . Biomechanical competence of vertebral trabecular bone in relation to ash density and age in normal individuals. Bone1987;8:79–85.CrossrefPubMed Google Scholar

    147. Giesen EB , Ding M , Dalstra M , van Eijden TM . Reduced mechanical load decreases the density, stiffness, and strength of cancellous bone of the mandibular condyle. Clin Biomech (Bristol, Avon)2003;18:358–363.CrossrefPubMed Google Scholar

    148. Giesen EB , Ding M , Dalstra M , van Eijden TM . Mechanical properties of cancellous bone in the human mandibular condyle are anisotropic. J Biomech2001;34:799–803.CrossrefPubMed Google Scholar

    149. Kurutz M , Donáth J , Gálos M , Varga P , Fornet B . Age- and sex-related regional compressive strength characteristics of human lumbar vertebrae in osteoporosis. J Multidiscip Healthc2008;1:105–121.CrossrefPubMed Google Scholar

    150. McElhaney JH , Fogle JL , Melvin JW et al. . Mechanical properties on cranial bone. J Biomech1970;3:495-511.CrossrefPubMed Google Scholar

    151. Seo SH , Lee J , Park IH . Efficacy of dual energy x-ray absorptiometry for evaluation of biomechanical properties: bone mineral density and actual bone strength. J Bone Metab2014;21:205–212.CrossrefPubMed Google Scholar

    152. Topolin´ski T , Cichan´ski A , Mazurkiewicz A , Nowicki K . Applying a stepwise load for calculation of the S-N curve for trabecular bone based on the linear hypothesis for fatigue damage accumulation. Mater Sci Forum2012;726:39–42. Google Scholar

    153. Lambers FM , Bouman AR , Tkachenko EV , Keaveny TM , Hernandez CJ . The effects of tensile-compressive loading mode and microarchitecture on microdamage in human vertebral cancellous bone. J Biomech2014;47:3605–3612.CrossrefPubMed Google Scholar

    154. Balsly CR , Cotter AT , Williams LA et al. . Effect of low dose and moderate dose gamma irradiation on the mechanical properties of bone and soft tissue allografts. Cell Tissue Bank2008;9:289–298.CrossrefPubMed Google Scholar

    155. Grieb TA , Forng R-Y , Stafford RE et al. . Effective use of optimized, high-dose (50 kGy) gamma irradiation for pathogen inactivation of human bone allografts. Biomaterials2005;26:2033–2042.CrossrefPubMed Google Scholar

    156. Lv H , Zhang L , Yang F et al. . Comparison of microstructural and mechanical properties of trabeculae in femoral head from osteoporosis patients with and without cartilage lesions: a case-control study. BMC Musculoskelet Disord2015;16:72.CrossrefPubMed Google Scholar

    157. Pothuaud L , Van Rietbergen B , Mosekilde L et al. . Combination of topological parameters and bone volume fraction better predicts the mechanical properties of trabecular bone. J Biomech2002;35:1091–1099.CrossrefPubMed Google Scholar

    158. Bargren JH , Andrew C , Bassett L , Gjelsvik A . Mechanical properties of hydrated cortical bone. J Biomech1974;7:239-245.CrossrefPubMed Google Scholar

    159. Finlay JB , Repo RU . Cartilage impact in vitro: effect of bone and cement. J Biomech1978;11:379–388.CrossrefPubMed Google Scholar

    160. Aiyangar AK , Vivanco J , Au AG et al. . Dependence of anisotropy of human lumbar vertebral trabecular bone on quantitative computed tomography-based apparent density. J Biomech Eng2014;136:091003.CrossrefPubMed Google Scholar

    161. Han S , Medige J , Faran K , Feng Z , Ziv I . The ability of quantitative ultrasound to predict the mechanical properties of trabecular bone under different strain rates. Med Eng Phys1997;19:742–747.CrossrefPubMed Google Scholar

    162. Liu JF , Shim VPW , Lee PVS . Quasi-static compressive and tensile tests on cancellous bone in human cervical spine. Conf Proc Soc Exp Mech Ser2013;5:109–118. https://link.springer.com/chapter/10.1007/978-1-4614-4427-5_16 (date last accessed 13 August 2018). Google Scholar

    163. Díaz León JL , Lesso Arroyo R , RodrÍguez Castro R , López Vázquez A . Mechanical characterization of bone allografts, enriched with mesenchymal cells. Int J Des Nat Ecodynamics2016;11:722–730. https://www.witpress.com/elibrary/dne-volumes/11/4/1282 (date last accessed 13 August 2018). Google Scholar

    164. Nazarian A , Muller J , Zurakowski D , Müller R , Snyder BD . Densitometric, morphometric and mechanical distributions in the human proximal femur. J Biomech2007;40:2573–2579.CrossrefPubMed Google Scholar

    165. Townsend PR , Raux P , Rose RM , Miegel RE , Radin EL . The distribution and anisotropy of the stiffness of cancellous bone in the human patella. J Biomech1975;8:363-367.CrossrefPubMed Google Scholar

    166. Rapillard L , Charlebois M , Zysset PK . Compressive fatigue behavior of human vertebral trabecular bone. J Biomech2006;39:2133–2139.CrossrefPubMed Google Scholar

    167. Tang SY , Zeenath U , Vashishth D . Effects of non-enzymatic glycation on cancellous bone fragility. Bone2007;40:1144–1151.CrossrefPubMed Google Scholar

    168. Cotton JR , Winwood K , Zioupos P , Taylor M . Damage rate is a predictor of fatigue life and creep strain rate in tensile fatigue of human cortical bone samples. J Biomech Eng2005;127:213–219.CrossrefPubMed Google Scholar

    169. Wegrzyn J , Roux JP , Arlot ME et al. . Determinants of the mechanical behavior of human lumbar vertebrae after simulated mild fracture. J Bone Miner Res2011;26:739–746.CrossrefPubMed Google Scholar

    170. Stauber M , Rapillard L , van Lenthe GH , Zysset P , Müller R . Importance of individual rods and plates in the assessment of bone quality and their contribution to bone stiffness. J Bone Miner Res2006;21:586–595.CrossrefPubMed Google Scholar

    171. van Lenthe GH , Stauber M , Müller R . Specimen-specific beam models for fast and accurate prediction of human trabecular bone mechanical properties. Bone2006;39:1182–1189.CrossrefPubMed Google Scholar

    172. Chevalier Y , Pahr D , Allmer H , Charlebois M , Zysset P . Validation of a voxel-based FE method for prediction of the uniaxial apparent modulus of human trabecular bone using macroscopic mechanical tests and nanoindentation. J Biomech2007;40:3333–3340.CrossrefPubMed Google Scholar

    173. Schwiedrzik J , Gross T , Bina M et al. . Experimental validation of a nonlinear μFE model based on cohesive-frictional plasticity for trabecular bone. Int J Numer Methods Biomed Eng2016;32:e02739.CrossrefPubMed Google Scholar

    174. Schwiedrzik JJ , Kaudela K-H , Burner U , Zysset PK . Fabric-mechanical property relationships of trabecular bone allografts are altered by supercritical CO2 treatment and gamma sterilization. Bone2011;48:1370–1377. Google Scholar

    175. Boustani HN , Zander T , Disch AC , Rohlmann A . Pedicle-screw-based dynamic implants may increase posterior intervertebral disc bulging during flexion. Biomed Tech (Berl)2011;56:327–331.CrossrefPubMed Google Scholar

    176. Frich LH , Jensen NC , Odgaard A et al. . Bone strength and material properties of the glenoid. J Shoulder Elb Surg1997;6:97–104.CrossrefPubMed Google Scholar

    177. Hans D , Wu C , Njeh CF et al. . Ultrasound velocity of trabecular cubes reflects mainly bone density and elasticity. Calcif Tissue Int1999;64:18–23.CrossrefPubMed Google Scholar

    178. Majumdar S , Kothari M , Augat P et al. . High-resolution magnetic resonance imaging: three-dimensional trabecular bone architecture and biomechanical properties. Bone1998;22:445–454.CrossrefPubMed Google Scholar

    179. Majumdar S , Lin J , Link T et al. . Fractal analysis of radiographs: assessment of trabecular bone structure and prediction of elastic modulus and strength. Med Phys1999;26:1330–1340.CrossrefPubMed Google Scholar

    180. Ouyang X , Majumdar S , Link TM et al. . Morphometric texture analysis of spinal trabecular bone structure assessed using orthogonal radiographic projections. Med Phys1998;25:2037–2045.CrossrefPubMed Google Scholar

    181. Ojanen X , Tanska P Malo MKH,et al.. Tissue viscoelasticity is related to tissue composition but may not fully predict the apparent-level viscoelasticity in human trabecular bone - An experimental and finite element study. J Biomech2017;65:96–105. Google Scholar

    182. Cyganik L , Binkowski M , Popik P et al. . Experimental verification of the relationships between Young’s modulus and bone density using DIC. In: KleiberM, BurczynskiT, WildeK, GoskiJ, eds. Advances in Mechanics: Theoretical, Computational and Interdisciplinary Issues: Proceedings of the 3rd Polish Congress of Mechanics (PCM) and 21st International Conference on Computer Methods in Mechanics (CMM). Gdansk: CRC Press, 2016:133-136. Google Scholar

    183. Langton CM , Njeh CF . The Physical Measurement of Bone. USA: CRC Press, 2003. Google Scholar

    184. García-Rodríguez S , Smith EL , Ploeg H-L . A calibration procedure for a bone loading system. J J Med Device2008;2:11006. Google Scholar

    185. Ouyang X , Lin JC , Link T et al. . Biomechanical strength versus spinal trabecular bone structure assessed using contact radiography and texture analysis. Proc SPIE - Int Soc Opt Eng1997;3034:165–174. Google Scholar

    186. Bone MC , Dold P , Flohr M et al. . The influence of the strength of bone on the deformation of acetabular shells: a laboratory experiment in cadavers. Bone Joint J2015;97–B:473–477.CrossrefPubMed Google Scholar

    187. Christensen P , Larsen HS , Lian R , Vang PS . Mechanical testing of the trabecular bone of the knee in knee alloplasty. Ugeskr Laeger1981;143:3127–3130. (in Danish) Google Scholar

    188. Nicholson PHF , Strelitzki R . On the prediction of Young’s modulus in calcaneal cancellous bone by ultrasonic bulk and bar velocity measurements. Clin Rheumatol1999;18:10–16. Google Scholar

    189. Rho JY , Flaitz D , Swarnakar V , Acharya RS . The characterization of broadband ultrasound attenuation and fractal analysis by biomechanical properties. Bone1997;20:497–504.CrossrefPubMed Google Scholar

    190. Shim VPW , Yang LM , Liu JF , Lee VS . Characterisation of the dynamic compressive mechanical properties of cancellous bone from the human cervical spine. Int J Impact Eng2006;32:525–540. Google Scholar

    191. Zhang Z-M , Li Z-C , Jiang L-S , Jiang S-D , Dai L-Y . Micro-CT and mechanical evaluation of subchondral trabecular bone structure between postmenopausal women with osteoarthritis and osteoporosis. Osteoporos Int2010;21:1383–1390.CrossrefPubMed Google Scholar

    192. Jankowska-Kuchta E , Kasprzak H , Fechner G . Comparison of mechanical properties of the bone investigated by compression test and holographic interferometry. Proc SPIE - Mic Hol Interf Bio1994;2083:319-321. https://www.spiedigitallibrary.org/conference-proceedings-of-spie/2083/0000/Comparison-of-mechanical-properties-of-the-bone-investigated-by-compression/10.1117/12.167405.short (date last accessed 13 August 2018). Google Scholar

    193. Parsch D , Breitwieser T , Breusch SJ . Mechanical stability of structured bone grafts from the anterior iliac crest. Clin Biomech (Bristol, Avon)2008;23:955–960.CrossrefPubMed Google Scholar

    194. Stein ID , Granik G . Human vertebral bone: relation of strength, porosity, and mineralization to fluoride content. Calcif Tissue Int1980;32:189–194.CrossrefPubMed Google Scholar

    195. Evans FG , Wood JL . Mechanical properties and density of bone in a case of severe endemic fluorosis. Acta Orthop Scand1976;47:489–495.CrossrefPubMed Google Scholar

    196. Ashby MF , Evans AG , Fleck NA et al. . Metal Foams: A Design Guide. First ed. Boston, Massachusetts: Butterworth-Heinemann, 2000. Google Scholar

    197. Novitsakaya E , Chen P-Y , Hamed E et al. . Recent advances on the measurement and calculation of the elastic moduli of cortical and trabecular bone: a review. Theoret Appl Mech2011;38:209-297. Google Scholar

    198. Lotz JC , Gerhart TN , Hayes WC . Mechanical properties of metaphyseal bone in the proximal femur. J Biomech1991;24:317-329.CrossrefPubMed Google Scholar

    199. Nyman JS , Roy A , Shen X et al. . The influence of water removal on the strength and toughness of cortical bone. J Biomech2006;39:931–938.CrossrefPubMed Google Scholar

    200. Mayeur O , Haugou G , Chaâri F et al. . Quasi-static and dynamic behaviour of the bone structures with fine geometric and materials modelling aspects. EPJ Web Conf2012;26:3008. https://www.epj-conferences.org/articles/epjconf/abs/2012/08/epjconf_dymat2012_03008/epjconf_dymat2012_03008.html (date last accessed 25 May 2018). Google Scholar

    201. Wang X , Nyman JS , Dong X , Leng H , Reyes M . Fundamental Biomechanics in Bone Tissue Engineering: Synthesis Lectures on Tissue Engineering. San Rafael, California: Morgan & Claypool Publishers, 2010. Google Scholar

    202. Keaveny TM , Borchers RE , Gibson LJ , Hayes WC . Trabecular bone modulus and strength can depend on specimen geometry. J Biomech1993;26:991-1000.CrossrefPubMed Google Scholar

    203. No authors listed. Standard Test Method for Compressive Properties of Rigid Plastics. ASTM D695-15. ASTM International, 2015. https://www.astm.org/Standards/D695.htm (date last accessed 25 May 2018). Google Scholar

    204. Tawy GF , Rowe PJ , Riches PE . Thermal damage done to bone by burring and sawing with and without irrigation in knee arthroplasty. J Arthroplasty2016;31:1102–1108.CrossrefPubMed Google Scholar

    205. Butler-Smith PW , Axinte DA , Daine M . Solid diamond micro-grinding tools: from innovative design and fabrication to preliminary performance evaluation in Ti–6Al–4V. Int J Mach Tools Manuf2012;59:55–64. Google Scholar

    206. Tang L , Tsai C , Gerberich WW , Kruckeberg L , Kania DR . Biocompatibility of chemical-vapour-deposited diamond. Biomaterials1995;16:483–488.CrossrefPubMed Google Scholar

    207. Keaveny TM , Guo XE , Wachtel EF , McMahon TA , Hayes WC . Trabecular bone exibits fully linear elastic behavior and yields at low strains. J Biomech1994;27:1127–1136. Google Scholar

    208. Dong XN , Yeni YN , Les CM , Fyhrie DP . Effects of end boundary conditions and specimen geometry on the viscoelastic properties of cancellous bone measured by dynamic mechanical analysis. J Biomed Mater Res A2004;68:573–583.CrossrefPubMed Google Scholar

    209. Kalidindi SR , Abusafieh A , Ei-Danaf E . Accurate characterization of machine compliance for simple compression testing. Exp Mech1997;37:210-215. Google Scholar

    210. Grassi L , Isaksson H . Extracting accurate strain measurements in bone mechanics: A critical review of current methods. J Mech Behav Biomed Mater2015;50:43–54.CrossrefPubMed Google Scholar

    211. No authors listed. Surface preparation for strain gage bonding. instruction bulletin B-129-8. Micro measurements. http://www.vishaypg.com/docs/11129/11129B129.pdf (date last accessed 29 May 2018). Google Scholar

    212. Grassi L , Väänänen SP , Yavari SA et al. . Full-field strain measurement during mechanical testing of the human femur at physiologically relevant strain rates. J Biomech Eng2014;136:111010.CrossrefPubMed Google Scholar

    213. Lakes RS , Katz JL , Sternstein SS . Viscoelastic properties of wet cortical bone-I. Torsional and biaxial studies. Biomechanics1979;12:657–678. Google Scholar

    214. Bunshah RF . Techniques of Metals Research: Measurement of Mechanical Properties. Ann Arbor, Michigan: Interscience Publishers, 1971. Google Scholar

    Information

    Journal

    Bone & Joint Research

    Volume

    7 No.8 | Pages 524 - 538

    Section

    Biomaterials

    Published

    01 August 2018

    DOI

    Expand all

    Doctor

    The MSk Lab, Imperial College London, Charing Cross Hospital, London, UK

    sarah.zhao12@imperial.ac.uk

    Search for more articles by this author

    Doctor

    The MSk Lab, Imperial College London, Charing Cross Hospital, London, UK

    Search for more articles by this author

    Research Postgraduate

    The MSk Lab, Imperial College London, Charing Cross Hospital, London, UK and Department of Mechanical Engineering, Imperial College London, South Kensington Campus, London, UK

    Search for more articles by this author

    Lecturer in Musculoskeletal Sciences

    The MSk Lab, Imperial College London, Charing Cross Hospital, London, UK

    Search for more articles by this author

    Chair in Orthopaedic Surgery

    The MSk Lab, Imperial College London, Charing Cross Hospital, London, UK

    Search for more articles by this author

    Senior Lecturer in Medical Engineering

    Department of Mechanical Engineering, Imperial College London, London, UK

    Search for more articles by this author

    Clinical Research Fellow and Specialist Registrar

    The MSk Lab, Imperial College London, Charing Cross Hospital, London, UK and Department of Mechanical Engineering, Imperial College London, London, UK

    Search for more articles by this author
    Compression testing
    Bone
    Stiffness
    Orthopaedic
    Submit Letter to the Editor

    Share

    Share article on social media
    Facebook
    X (Twitter)
    LinkedIn
    Email

    Figures

    Fig. 1 Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow diagram of study selection.

    Fig. 1

    Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow diagram of study selection.
    Go to Article
    Images showing a) standard platens compression testing setup of a bone specimen, and b) a close-up schematic of a bone specimen placed between two polished platens.

    Fig.

    Images showing a) standard platens compression testing setup of a bone specimen, and b) a close-up schematic of a bone specimen placed between two polished platens.
    Go to Article
    Fig. 3 Stress-strain graph of a typical compression test with corresponding mechanical parameters measured.

    Fig. 3

    Stress-strain graph of a typical compression test with corresponding mechanical parameters measured.
    Go to Article
    Fig. 4 Recommended testing protocol for measurement of bone modulus. DIC, Digital Image Correlation; LVDT, Linear Variable Differential Transformer.

    Fig. 4

    Recommended testing protocol for measurement of bone modulus. DIC, Digital Image Correlation; LVDT, Linear Variable Differential Transformer.
    Go to Article

    Metrics

    Downloaded 6792 times

    References

    1. Find in article

    Miles AW , Gheduzzi S . Basic biomechanics and biomaterials. Surg2012;30:86–91.

    Google Scholar
    2. Find in article

    Rubash HE , Sinha RK , Shanbhag AS , Kim SY . Pathogenesis of bone loss after total hip arthroplasty. Orthop Clin North Am1998;29:173–186.

    Crossref PubMed Google Scholar
    3. Find in article

    Augat P , Link T , Lang TF et al. . Anisotropy of the elastic modulus of trabecular bone specimens from different anatomical locations. Med Eng Phys1998;20:124–131.

    Crossref PubMed Google Scholar
    4. Find in article

    Nazarian A , Von Stechow D , Zurakowski D , Müller R , Snyder BD . Bone volume fraction explains the variation in strength and stiffness of cancellous bone affected by metastatic cancer and osteoporosis. Calcif Tissue Int2008;83:368–379.

    Crossref PubMed Google Scholar
    5. Find in article

    Ciarallo A , Barralet J , Tanzer M , Kremer R . An approach to compare the quality of cancellous bone from the femoral necks of healthy and osteoporotic patients through compression testing and microcomputed tomography imaging. Mcgill J Med2006;9:102–107.

    PubMed Google Scholar
    6. Find in article

    El Masri F , Sapin de Brosses E , Rhissassi K , Skalli W , Mitton D . Apparent Young’s modulus of vertebral cortico-cancellous bone specimens. Comput Methods Biomech Biomed Engin2012;15:23–28.

    Google Scholar
    7. Find in article

    Linde F , Gøthgen CB , Hvid I , Pongsoipetch B . Mechanical properties of trabecular bone by a non-destructive compression testing approach. Eng Med1988;17:23–29.

    Crossref PubMed Google Scholar
    8. Find in article

    Bayraktar HH , Morgan EF , Niebur GL et al. . Comparison of the elastic and yield properties of human femoral trabecular and cortical bone tissue. J Biomech2004;37:27–35.

    Crossref PubMed Google Scholar
    9. Find in article

    An YH , Draughn RA . Mechanical Testing of Bone and the Bone-Implant Interface. First ed. Boca Raton: CRC Press, 1999.

    Google Scholar
    10. Find in article

    Røhl L , Larsen E , Linde F , Odgaard A , Jørgensen J . Tensile and compressive properties of cancellous bone. J Biomech1991;24:1143–1149.

    Crossref PubMed Google Scholar
    11. Find in article

    Donnelly E . Methods for assessing bone quality: a review. Clin Orthop Relat Res2011;469:2128–2138.

    Crossref PubMed Google Scholar
    12. Find in article

    Pal S . Mechanical properties of biological materials. In: PalS, ed. Design of Artificial Human Joints & Organs. USA: Springer, 2014:23–40.

    Google Scholar
    13. Find in article

    Ma S , Goh EL , Jin A et al. . Long-term effects of bisphosphonate therapy: perforations, microcracks and mechanical properties. Sci Rep2017;7:43399.

    Crossref PubMed Google Scholar
    14. Find in article

    Turner CH , Burr DB . Basic biomechanical measurements of bone: a tutorial. Bone1993;14:595–608.

    Crossref PubMed Google Scholar
    15. Find in article

    Keaveny TM , Borchers RE , Gibson LJ , Hayes WC . Theoretical analysis of the experimental artifact in trabecular bone compressive modulus. J Biomech1993;26:599–607.

    Crossref PubMed Google Scholar
    16. Find in article

    Hansen U , Zioupos P , Simpson R , Currey JD , Hynd D . The effect of strain rate on the mechanical properties of human cortical bone. J Biomech Eng2008;130:011011.

    Crossref PubMed Google Scholar
    17. Find in article

    Moher D , Liberati A , Tetzlaff J , Altman DG PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med2009;151:264–269.

    Crossref PubMed Google Scholar
    18. Find in article

    Higgins JPT , Green S . Cochrane Handbook for Systematic Reviews of Interventions: Cochrane Book Series. Chichester: John Wiley & Sons, 2008.

    Google Scholar
    19. Find in article

    Bevill G , Eswaran SK , Farahmand F , Keaveny TM . The influence of boundary conditions and loading mode on high-resolution finite element-computed trabecular tissue properties. Bone2009;44:573–578.

    Crossref PubMed Google Scholar
    20. Find in article

    Birnbaum K , Sindelar R , Gaertner JR , Wirtz DC . Material properties of trabecular bone structures. Surg Radiol Anat2001;23:399–407.

    Crossref PubMed Google Scholar
    21. Find in article

    Conrad EU , Ericksen DP , Tencer AF , Strong DM , Mackenzie AP . The effects of freeze-drying and rehydration on cancellous bone. Clin Orthop Relat Res1993;290:279–284.

    PubMed Google Scholar
    22. Find in article

    Linde F , Sørensen HCF . The effect of different storage methods on the mechanical properties of trabecular bone. J Biomech1993;26:1249–1252.

    Crossref PubMed Google Scholar
    23. Find in article

    Linde F , Pongsoipetch B , Frich LH , Hvid I . Three-axial strain controlled testing applied to bone specimens from the proximal tibial epiphysis. J Biomech1990;23:1167–1172.

    Crossref PubMed Google Scholar
    24. Find in article

    Linde F , Hvid I , Madsen F . The effect of specimen geometry on the mechanical behaviour of trabecular bone specimens. J Biomech1992;25:359–368.

    Crossref PubMed Google Scholar
    25. Find in article

    Linde F , Hvid I . Stiffness behaviour of trabecular bone specimens. J Biomech1987;20:83–89.

    Crossref PubMed Google Scholar
    26. Find in article

    Linde F , Nørgaard P , Hvid I , Odgaard A , Søballe K . Mechanical properties of trabecular bone. Dependency on strain rate. J Biomech1991;24:803–809.

    Crossref PubMed Google Scholar
    27. Find in article

    Linde F , Hvid I . The effect of constraint on the mechanical behaviour of trabecular bone specimens. J Biomech1989;22:485–490.

    Crossref PubMed Google Scholar
    28. Find in article

    Morgan EF , Yeh OC , Keaveny TM . Damage in trabecular bone at small strains. Eur J Morphol2005;42:13–21.

    Crossref PubMed Google Scholar
    29. Find in article

    Morgan EF , Yeh OC , Chang WC , Keaveny TM . Nonlinear behavior of trabecular bone at small strains. J Biomech Eng2001;123:1–9.

    Crossref PubMed Google Scholar
    30. Find in article

    Odgaard A , Linde F . The underestimation of Young’s modulus in compressive testing of cancellous bone specimens. J Biomech1991;24:691–698.

    Google Scholar
    31. Find in article

    Öhman C , Dall’Ara E , Baleani M , Van Sint Jan S , Viceconti M . The effects of embalming using a 4% formalin solution on the compressive mechanical properties of human cortical bone. Clin Biomech (Bristol, Avon)2008;23:1294–1298.

    Crossref PubMed Google Scholar
    32. Find in article

    Öhman C , Baleani M , Perilli E et al. . Mechanical testing of cancellous bone from the femoral head: experimental errors due to off-axis measurements. J Biomech2007;40:2426–2433.

    Crossref PubMed Google Scholar
    33. Find in article

    Yahia LH , Drouin G , Duval P . A methodology for mechanical measurements of technical constants of trabecular bone. Eng Med1988;17:169–173.

    Crossref PubMed Google Scholar
    34. Find in article

    Zhu M , Keller TS , Spengler DM . Effects of specimen load-bearing and free surface layers on the compressive mechanical properties of cellular materials. J Biomech1994;27:57–66.

    Crossref PubMed Google Scholar
    35. Find in article

    Keaveny TM , Wachtel EF , Kopperdahl DL . Mechanical behavior of human trabecular bone after overloading. J Orthop Res1999;17:346–353.

    Crossref PubMed Google Scholar
    36. Find in article

    Keaveny TM , Pinilla TP , Crawford RP , Kopperdahl DL , Lou A . Systematic and random errors in compression testing of trabecular bone. J Orthop Res1997;15:101–110.

    Crossref PubMed Google Scholar
    37. Find in article

    Anderson MJ , Keyak JH , Skinner HB . Compressive mechanical properties of human cancellous bone after gamma irradiation. J Bone Joint Surg [Am]1992;74-A:747-752.

    PubMed Google Scholar
    38. Find in article

    Badiei A , Bottema MJ , Fazzalari NL . Influence of orthogonal overload on human vertebral trabecular bone mechanical properties. J Bone Miner Res2007;22:1690–1699.

    Crossref PubMed Google Scholar
    39. Find in article

    Banse X , Delloye C , Cornu O , Bourgois R . Comparative left-right mechanical testing of cancellous bone from normal femoral heads. J Biomech1996;29:1247–1253.

    Crossref PubMed Google Scholar
    40. Find in article

    Banse X , Sims TJ , Bailey AJ . Mechanical properties of adult vertebral cancellous bone: correlation with collagen intermolecular cross-links. J Bone Miner Res2002;17:1621–1628.

    Crossref PubMed Google Scholar
    41. Find in article

    Baroud G , Nemes J , Ferguson SJ , Steffen T . Material changes in osteoporotic human cancellous bone following infiltration with acrylic bone cement for a vertebral cement augmentation. Comput Methods Biomech Biomed Engin2003;6:133–139.

    Crossref PubMed Google Scholar
    42. Find in article

    Bentzen SM , Hvid I , Jørgensen J . Mechanical strength of tibial trabecular bone evaluated by X-ray computed tomography. J Biomech1987;20:743-752.

    Crossref PubMed Google Scholar
    43. Find in article

    Bollerslev J , Mosekilde L , Nielsen HK , Mosekilde L . Biomechanical competence of iliac crest trabecular bone in autosomal dominant osteopetrosis type I. Bone1989;10:159–164.

    Crossref PubMed Google Scholar
    44. Find in article

    Bosisio MR , Talmant M , Skalli W , Laugier P , Mitton D . Apparent Young’s modulus of human radius using inverse finite-element method. J Biomech2007;40:2022–2028.

    Google Scholar
    45. Find in article

    Bourgnon A , Sitzer A , Chabraborty A et al. . Impact of microscale properties measured by 50-MHz acoustic microscopy on mesoscale elastic and ultimate mechanical cortical bone properties. IEEE Int Ultrason Symp IUS, 2014;636–638.

    Google Scholar
    46. Find in article

    Brown TD , Ferguson AB Jr . Mechanical property distributions in the cancellous bone of the human proximal femur. Acta Orthop Scand1980;51:429–437.

    Crossref PubMed Google Scholar
    47. Find in article

    Brown TD , Way ME , Ferguson AB Jr . Mechanical characteristics of bone in femoral capital aseptic necrosis. Clin Orthop Relat Res1981;156:240–247.

    PubMed Google Scholar
    48. Find in article

    Brown SJ , Pollintine P , Powell DE , Davie MWJ , Sharp CA . Regional differences in mechanical and material properties of femoral head cancellous bone in health and osteoarthritis. Calcif Tissue Int2002;71:227–234.

    Crossref PubMed Google Scholar
    49. Find in article

    Burgers TA , Mason J , Niebur G , Ploeg HL . Compressive properties of trabecular bone in the distal femur. J Biomech2008;41:1077–1085.

    Crossref PubMed Google Scholar
    50. Find in article

    Caler WE , Carter DR . Bone creep-fatigue damage accumulation. J Biomech1989;22:625–635.

    Crossref PubMed Google Scholar
    51. Find in article

    Carter DR , Schwab GH , Spengler DM . Tensile fracture of cancellous bone. Acta Orthop1980;51:733–741.

    Crossref PubMed Google Scholar
    52. Find in article

    Carter DR , Hayes WC . The compressive behavior of bone as a two-phase porous structure. J Bone Joint Surg [Am]1977;59-A:954–962.

    PubMed Google Scholar
    53. Find in article

    Cendre E , Mitton D , Roux J-P , Arlot ME , Duboeuf F , Burt-Pichat B , Rumelhart C , Peix G , Meunier PJ . High-resolution computed tomography for architectural characterization of human lumbar cancellous bone: relationships with histomorphometry and biomechanics. Osteoporos Int1999;10:353–360.

    Crossref PubMed Google Scholar
    54. Find in article

    Cezayirlioglu H , Bahniuk E , Davy DT , Heiple KG . Anisotropic yield behavior of bone under combined axial force and torque. J Biomech1985;18:61–69.

    Crossref PubMed Google Scholar
    55. Find in article

    Charlebois M , Pretterklieber M , Zysset PK . The role of fabric in the large strain compressive behavior of human trabecular bone. J Biomech Eng2010;132:121006.

    Crossref PubMed Google Scholar
    56. Find in article

    Sneppen O , Christensen P , Larsen H , Vang PS . Mechanical testing of trabecular bone in knee replacement. Int Orthop1981;5:251–256.

    Crossref PubMed Google Scholar
    57. Find in article

    Ciarelli MJ , Goldstein SA , Kuhn JL , Cody DD , Brown MB . Evaluation of orthogonal mechanical properties and density of human trabecular bone from the major metaphyseal regions with materials testing and computed tomography. J Orthop Res1991;9:674–682.

    Crossref PubMed Google Scholar
    58. Find in article

    Cody DD , McCubbrey DA , Divine GW , Gross GJ , Goldstein SA . Predictive value of proximal femoral bone densitometry in determining local orthogonal material properties. J Biomech1996;29:753–761.

    Crossref PubMed Google Scholar
    59. Find in article

    Cornu O , Boquet J , Nonclercq O et al. . Synergetic effect of freeze-drying and gamma irradiation on the mechanical properties of human cancellous bone. Cell Tissue Bank2011;12:281–288.

    Crossref PubMed Google Scholar
    60. Find in article

    Deligianni DD , Maris A , Missirlis YF . Stress relaxation behaviour of trabecular bone specimens. J Biomech1994;27:1469–1476.

    Crossref PubMed Google Scholar
    61. Find in article

    Ding M , Dalstra M , Danielsen CC et al. . Age variations in the properties of human tibial trabecular bone. J Bone Joint Surg [Br]1997;79-B:995–1002.

    Crossref PubMed Google Scholar
    62. Find in article

    Ding M , Danielsen CC , Hvid I . Bone density does not reflect mechanical properties in early-stage arthrosis. Acta Orthop Scand2001;72:181–185.

    Google Scholar
    63. Find in article

    Ding M , Danielsen CC , Hvid I , Overgaard S . Three-dimensional microarchitecture of adolescent cancellous bone. Bone2012;51:953–960.

    Crossref PubMed Google Scholar
    64. Find in article

    Ding M , Odgaard A , Linde F , Hvid I . Age-related variations in the microstructure of human tibial cancellous bone. J Orthop Res2002;20:615–621.

    Crossref PubMed Google Scholar
    65. Find in article

    Dong XN , Acuna RL , Luo Q , Wang X . Orientation dependence of progressive post-yield behavior of human cortical bone in compression. J Biomech2012;45:2829–2834.

    Crossref PubMed Google Scholar
    66. Find in article

    Du C , Ma H , Ruo M et al. . An experimental study on the biomechanical properties of the cancellous bones of distal femur. Biomed Mater Eng2006;16:215–222.

    PubMed Google Scholar
    67. Find in article

    Duchemin L , Bousson V , Raossanaly C et al. . Prediction of mechanical properties of cortical bone by quantitative computed tomography. Med Eng Phys2008;30:321–328.

    Crossref PubMed Google Scholar
    68. Find in article

    Ducheyne P , Heymans L , Martens M et al. . The mechanical behaviour of intracondylar cancellous bone of the femur at different loading rates. J Biomech1977;10:747–762.

    Crossref PubMed Google Scholar
    69. Find in article

    Fazzalari NL , Forwood MR , Smith K , Manthey BA , Herreen P . Assessment of cancellous bone quality in severe osteoarthrosis: bone mineral density, mechanics, and microdamage. Bone1998;22:381–388.

    Crossref PubMed Google Scholar
    70. Find in article

    Follet H , Bruyère-Garnier K , Peyrin F et al. . Relationship between compressive properties of human os calcis cancellous bone and microarchitecture assessed from 2D and 3D synchrotron microtomography. Bone2005;36:340-351.

    Crossref PubMed Google Scholar
    71. Find in article

    Follet H , Boivin G , Rumelhart C , Meunier PJ . The degree of mineralization is a determinant of bone strength: a study on human calcanei. Bone2004;34:783–789.

    Crossref PubMed Google Scholar
    72. Find in article

    Follet H , Peyrin F , Vidal-Salle E et al. . Intrinsic mechanical properties of trabecular calcaneus determined by finite-element models using 3D synchrotron microtomography. J Biomech2007;40:2174–2183.

    Crossref PubMed Google Scholar
    73. Find in article

    Follet H , Viguet-Carrin S , Burt-Pichat B et al. . Effects of preexisting microdamage, collagen cross-links, degree of mineralization, age, and architecture on compressive mechanical properties of elderly human vertebral trabecular bone. J Orthop Res2011;29:481–488.

    Crossref PubMed Google Scholar
    74. Find in article

    Goldstein SA , Wilson DL , Sonstegard DA , Matthews LS . The mechanical properties of human tibial trabecular bone as a function of metaphyseal location. J Biomech1983;16:965–969.

    Crossref PubMed Google Scholar
    75. Find in article

    Goulet RW , Goldstein SA , Ciarelli MJ et al. . The relationship between the structural and orthogonal compressive properties of trabecular bone. J Biomech1994;27:375-389.

    Crossref PubMed Google Scholar
    76. Find in article

    Haddock SM , Yeh OC , Mummaneni PV , Rosenberg WS , Keaveny TM . Similarity in the fatigue behavior of trabecular bone across site and species. J Biomech2004;37:181–187.

    Crossref PubMed Google Scholar
    77. Find in article

    Hernandez CJ , Lambers FM , Widjaja J , Chapa C , Rimnac CM . Quantitative relationships between microdamage and cancellous bone strength and stiffness. Bone2014;66:205–213.

    Crossref PubMed Google Scholar
    78. Find in article

    Hvid I . Cancellous bone at the knee: a comparison of two methods of strength measurement. Arch Orthop Trauma Surg1985;104:211–217.

    Crossref PubMed Google Scholar
    79. Find in article

    Hvid I , Christensen P , Søondergaard J , Christensen PB , Larsen CG . Compressive strength of tibial cancellous bone: Instron and osteopenetrometer measurements in an autopsy material. Acta Orthop Scand1983;54:819–825.

    Google Scholar
    80. Find in article

    Hvid I , Jensen J . Cancellous bone strength at the proximal human tibia. Eng Med1984;13:21–25.

    Crossref PubMed Google Scholar
    81. Find in article

    Hvid I , Bentzen SM , Linde F , Mosekilde L , Pongsoipetch B . X-ray quantitative computed tomography: the relations to physical properties of proximal tibial trabecular bone specimens. J Biomech1989;22:837–844.

    Crossref PubMed Google Scholar
    82. Find in article

    Imbert L , Aurégan J-C , Pernelle K , Hoc T . Microstructure and compressive mechanical properties of cortical bone in children with osteogenesis imperfecta treated with bisphosphonates compared with healthy children. J Mech Behav Biomed Mater2015;46:261–270.

    Crossref PubMed Google Scholar
    83. Find in article

    Jensen NC , Hvid I , Krøner K . Strength pattern of cancellous bone at the ankle joint. Eng Med1988;17:71–76.

    Crossref PubMed Google Scholar
    84. Find in article

    Jensen NC , Madsen LP , Linde F . Topographical distribution of trabecular bone strength in the human os calcanei. J Biomech1991;24:49–55.

    Crossref PubMed Google Scholar
    85. Find in article

    Jones AA , Dougherty PJ , Sharkey NA , Benson DR . Iliac crest bone graft. Osteotome versus saw. Spine1993;18(Suppl):2048–2052.

    Crossref PubMed Google Scholar
    86. Find in article

    Kalouche I , Crépin J , Abdelmoumen S et al. . Mechanical properties of glenoid cancellous bone. Clin Biomech (Bristol, Avon)2010;25:292–298.

    Crossref PubMed Google Scholar
    87. Find in article

    Karim L , Vashishth D . Heterogeneous glycation of cancellous bone and its association with bone quality and fragility. PLoS One2012;7:e35047.

    Crossref PubMed Google Scholar
    88. Find in article

    Keller TS . Predicting the compressive mechanical behavior of bone. J Biomech1994;27:1159–1168.

    Crossref PubMed Google Scholar
    89. Find in article

    Keyak JH , Lee IY , Nath DS , Skinner HB . Postfailure compressive behavior of tibial trabecular bone in three anatomic directions. J Biomed Mater Res1996;31:373–378.

    Crossref PubMed Google Scholar
    90. Find in article

    Kopperdahl DL , Keaveny TM . Yield strain behavior of trabecular bone. J Biomech1998;31:601–608.

    Crossref PubMed Google Scholar
    91. Find in article

    Leichter I , Bivas A , Margulies JY , Roman I , Simkin A . Acoustic emission from trabecular bone during mechanical testing: the effect of osteoporosis and osteoarthritis. Proc Inst Mech Eng Part H1990;204:123–127.

    Crossref PubMed Google Scholar
    92. Find in article

    Li Z-C , Dai L-Y , Jiang L-S , Qiu S . Difference in subchondral cancellous bone between postmenopausal women with hip osteoarthritis and osteoporotic fracture: implication for fatigue microdamage, bone microarchitecture, and biomechanical properties. Arthritis Rheum2012;64:3955–3962.

    Crossref PubMed Google Scholar
    93. Find in article

    Linde F , Hvid I , Jensen NC . Material properties of cancellous bone in repetitive axial loading. Eng Med1985;14:173–177.

    Crossref PubMed Google Scholar
    94. Find in article

    Macneil JA , Boyd SK . Bone strength at the distal radius can be estimated from high-resolution peripheral quantitative computed tomography and the finite element method. Bone2008;42:1203–1213.

    Crossref PubMed Google Scholar
    95. Find in article

    Martens M , Van Audekercke R , Delport P , De Meester P , Mulier JC . The mechanical characteristics of cancellous bone at the upper femoral region. J Biomech1983;16:971–983.

    Crossref PubMed Google Scholar
    96. Find in article

    Martin H , Werner J , Andresen R , Schober H-C , Schmitz K-P . Noninvasive assessment of stiffness and failure load of human vertebrae from CT-data. Biomed Tech (Berl)1998;43:82–88.

    Crossref PubMed Google Scholar
    97. Find in article

    Matsuura M , Eckstein F , Lochmüller E-M , Zysset PK . The role of fabric in the quasi-static compressive mechanical properties of human trabecular bone from various anatomical locations. Biomech Model Mechanobiol2008;7:27–42.

    Crossref PubMed Google Scholar
    98. Find in article

    Misch CE , Qu Z , Bidez MW . Mechanical properties of trabecular bone in the human mandible: implications for dental implant treatment planning and surgical placement. J Oral Maxillofac Surg1999;57:700–706.

    Crossref PubMed Google Scholar
    99. Find in article

    Morgan EF , Keaveny TM . Dependence of yield strain of human trabecular bone on anatomic site. J Biomech2001;34:569–577.

    Crossref PubMed Google Scholar
    100. Find in article

    Murdoch AH , Mathias KJ , Shepherd DET . Investigation into the material properties of beech wood and cortical bone. Biomed Mater Eng2004;14:1–4.

    PubMed Google Scholar
    101. Find in article

    Nicholson PHF , Cheng XG , Lowet G et al. . Structural and material mechanical properties of human vertebral cancellous bone. Med Eng Phys1997;19:729–737.

    Crossref PubMed Google Scholar
    102. Find in article

    Njeh CF , Kuo CW , Langton CM , Atrah HI , Boivin CM . Prediction of human femoral bone strength using ultrasound velocity and BMD: an in vitro study. Osteoporos Int1997;7:471–477.

    Crossref PubMed Google Scholar
    103. Find in article

    Odgaard A , Hvid I , Linde F . Compressive axial strain distributions in cancellous bone specimens. J Biomech1989;22:829–835.

    Crossref PubMed Google Scholar
    104. Find in article

    O’Mahony AM , Williams JL , Katz JO , Spencer P . Anisotropic elastic properties of cancellous bone from a human edentulous mandible. Clin Oral Implants Res2000;11:415–421.

    Crossref PubMed Google Scholar
    105. Find in article

    Ouyang J , Yang GT , Wu WZ , Zhu QA , Zhong SZ . Biomechanical characteristics of human trabecular bone. Clin Biomech (Bristol, Avon)1997;12:522–524.

    Crossref PubMed Google Scholar
    106. Find in article

    Pattin CA , Caler WE , Carter DR . Cyclic mechanical property degradation during fatigue loading of cortical bone. J Biomech1996;29:69–79.

    Crossref PubMed Google Scholar
    107. Find in article

    Portero-Muzy NR , Chavassieux PM , Mitton D et al. . Euler(strut.cavity), a new histomorphometric parameter of connectivity reflects bone strength and speed of sound in trabecular bone from human os calcis. Calcif Tissue Int2007;81:92–98.

    Crossref PubMed Google Scholar
    108. Find in article

    Poukalova M , Yakacki CM , Guldberg RE et al. . Pullout strength of suture anchors: effect of mechanical properties of trabecular bone. J Biomech2010;43:1138–1145.

    Crossref PubMed Google Scholar
    109. Find in article

    Poumarat G , Squire P , Dabonneville M . Comparison of mechanical properties of human, bovine bone and a new processed bone xenograft. Biomaterials1993;14:337–340.

    Crossref PubMed Google Scholar
    110. Find in article

    Rauh J , Despang F , Baas J et al. . Comparative biomechanical and microstructural analysis of native versus peracetic acid-ethanol treated cancellous bone graft. Biomed Res Int2014;2014:784702.

    Crossref PubMed Google Scholar
    111. Find in article

    Reilly DT , Burstein AH . The elastic and ultimate properties of compact bone tissue. J Biomech1975;8:393-405.

    Crossref PubMed Google Scholar
    112. Find in article

    Reilly DT , Burstein AH , Frankel VH . The elastic modulus for bone. J Biomech1974;7:271-275.

    Google Scholar
    113. Find in article

    Rincón-Kohli L , Zysset PK . Multi-axial mechanical properties of human trabecular bone. Biomech Model Mechanobiol2009;8:195–208.

    Crossref PubMed Google Scholar
    114. Find in article

    Rodrigues AM , Caetano-Lopes J , Vale AC et al. . Low osteocalcin/collagen type I bone gene expression ratio is associated with hip fragility fractures. Bone2012;51:981–989.

    Crossref PubMed Google Scholar
    115. Find in article

    Sierpowska J , Hakulinen M , Töyräs J et al. . Prediction of mechanical properties of human trabecular bone by electrical measurements. Physiol Meas2005;26:S119–S131.

    Crossref PubMed Google Scholar
    116. Find in article

    Speirs AD , Hotz MA , Oxland TR , Häusler R , Nolte L-P . Biomechanical properties of sterilized human auditory ossicles. J Biomech1999;32:485–491.

    Crossref PubMed Google Scholar
    117. Find in article

    Steinhauser E , Diehl P , Hadaller M et al. . Biomechanical investigation of the effect of high hydrostatic pressure treatment on the mechanical properties of human bone. J Biomed Mater Res B Appl Biomater2006;76:130–135.

    Crossref PubMed Google Scholar
    118. Find in article

    Stoppie N , Pattijn V , Van Cleynenbreugel T et al. . Structural and radiological parameters for the characterization of jawbone. Clin Oral Implants Res2006;17:124–133.

    Crossref PubMed Google Scholar
    119. Find in article

    Stoppie N , Van Cleynenbreugel T , Wevers M , Vander Sloten J , Naert I . The validation of a compression testing method for cancellous human jawbone by high-resolution finite element modeling. Int J Oral Maxillofac Implants2007;22:436–445.

    PubMed Google Scholar
    120. Find in article

    Sugita H , Oka M , Toguchida J et al. . Anisotropy of osteoporotic cancellous bone. Bone1999;24:513–516.

    Crossref PubMed Google Scholar
    121. Find in article

    Sun S-S , Ma H-L , Liu C-L et al. . Difference in femoral head and neck material properties between osteoarthritis and osteoporosis. Clin Biomech (Bristol, Avon)2008;23:S39–S47.

    Crossref PubMed Google Scholar
    122. Find in article

    Thurner PJ , Erickson B , Turner P et al. . The effect of NaF in vitro on the mechanical and material properties of trabecular and cortical bone. Adv Mater2009;21:451–457.

    Google Scholar
    123. Find in article

    Vale AC , Aleixo IP , Lúcio M et al. . At the moment of occurrence of a fragility hip fracture, men have higher mechanical properties values in comparison with women. BMC Musculoskelet Disord2013;14:295.

    Crossref PubMed Google Scholar
    124. Find in article

    Vale AC , Pereira MFC , Maurício A et al. . Micro-computed tomography and compressive characterization of trabecular bone. Colloids Surf A Physicochem Eng Asp2013;438:199–205.

    Google Scholar
    125. Find in article

    Vardakastani V , Saletti D , Skalli W et al. . Increased intra-cortical porosity reduces bone stiffness and strength in pediatric patients with osteogenesis imperfecta. Bone2014;69:61–67.

    Crossref PubMed Google Scholar
    126. Find in article

    Vastel L , Meunier A , Siney H , Sedel L , Courpied J-P . Effect of different sterilization processing methods on the mechanical properties of human cancellous bone allografts. Biomaterials2004;25:2105–2110.

    Crossref PubMed Google Scholar
    127. Find in article

    Wachter NJ , Augat P , Krischak GD et al. . Prediction of strength of cortical bone in vitro by microcomputed tomography. Clin Biomech (Bristol, Avon)2001;16:252–256.

    Crossref PubMed Google Scholar
    128. Find in article

    Wachter NJ , Augat P , Mentzel M et al. . Predictive value of bone mineral density and morphology determined by peripheral quantitative computed tomography for cancellous bone strength of the proximal femur. Bone2001;28:133–139.

    Crossref PubMed Google Scholar
    129. Find in article

    Wachter NJ , Krischak GD , Mentzel M et al. . Correlation of bone mineral density with strength and microstructural parameters of cortical bone in vitro. Bone2002;31:90–95.

    Crossref PubMed Google Scholar
    130. Find in article

    Wells JG , Rawlings RD . Acoustic emission and mechanical properties of trabecular bone. Biomaterials1985;6:218–224.

    Crossref PubMed Google Scholar
    131. Find in article

    Wu Z , Laneve AJ , Niebur GL . In vivo microdamage is an indicator of susceptibility to initiation and propagation of microdamage in human femoral trabecular bone. Bone2013;55:208–215.

    Crossref PubMed Google Scholar
    132. Find in article

    Yamamoto E , Paul Crawford R , Chan DD , Keaveny TM . Development of residual strains in human vertebral trabecular bone after prolonged static and cyclic loading at low load levels. J Biomech2006;39:1812–1818.

    Crossref PubMed Google Scholar
    133. Find in article

    Zhou B , Liu XS , Wang J et al. . Dependence of mechanical properties of trabecular bone on plate-rod microstructure determined by individual trabecula segmentation (ITS). J Biomech2014;47:702–708.

    Crossref PubMed Google Scholar
    134. Find in article

    Cesar R , Leivas TP , Augusto C et al. . Axial compressive strength of human vertebrae trabecular bones classified as normal, osteopenic and osteoporotic by quantitative ultrasonometry of calcaneus. Res Biomed Eng2017;33:91–96.

    Google Scholar
    135. Find in article

    Samuel J , Park JS , Almer J , Wang X . Effect of water on nanomechanics of bone is different between tension and compression. J Mech Behav Biomed Mater2016;57:128–138.

    Crossref PubMed Google Scholar
    136. Find in article

    Mirzaali MJ , Schwiedrzik JJ , Thaiwichai S et al. . Mechanical properties of cortical bone and their relationships with age, gender, composition and microindentation properties in the elderly. Bone2015;93:196–211.

    Crossref PubMed Google Scholar
    137. Find in article

    Ozan F , Pekedis M , Koyuncu S¸ et al. . Micro-computed tomography and mechanical evaluation of trabecular bone structure in osteopenic and osteoporotic fractures. J Orthop Surg (Hong Kong)2017;25:2309499017692718.

    Crossref PubMed Google Scholar
    138. Find in article

    Erivan R , Villatte G , Cueff R , Boisgard S , Descamps BS . Rehydration improves the ductility of dry bone allografts. Cell Tissue Bank2017;18:307-312.

    Crossref PubMed Google Scholar
    139. Find in article

    Li J , Huang S , Tang Y , Wang X , Pan T . Biomechanical analysis of the posterior bony column of the lumbar spine. J Orthop Surg Res2017;12:132.

    Crossref PubMed Google Scholar
    140. Find in article

    Cyganik Ł , Binkowski M , Kokot G et al. . Prediction of Young’s modulus of trabeculae in microscale using macro-scale’s relationships between bone density and mechanical properties. J Mech Behav Biomed Mater2014;36:120–134.

    Google Scholar
    141. Find in article

    Jia-ju S , Jie G , Fu-Zhao H . The compressive properties of long bones. Appl Math Mech1981;2:733–742.

    Google Scholar
    142. Find in article

    Öhman C , Baleani M , Pani C et al. . Compressive behaviour of child and adult cortical bone. Bone2011;49:769–776.

    Crossref PubMed Google Scholar
    143. Find in article

    Rao S , McKellop H , Chao D et al. . Biomechanical comparison of bone graft used in anterior spinal reconstruction. Freeze-dried demineralized femoral segments versus fresh fibular segments and tricortical iliac blocks in autopsy specimens. Clin Orthop Relat Res1993;289:131–135.

    PubMed Google Scholar
    144. Find in article

    Perilli E , Baleani M , Öhman C et al. . Dependence of mechanical compressive strength on local variations in microarchitecture in cancellous bone of proximal human femur. J Biomech2008;41:438–446.

    Crossref PubMed Google Scholar
    145. Find in article

    Cyganik Ł , Binkowski M , Kokot G et al. . Microscale’s relationship between Young’s modulus and tissue density. Prediction of displacements. Comput Methods Biomech Biomed Engin2017;20:1658-1668.

    Google Scholar
    146. Find in article

    Mosekilde L , Mosekilde L , Danielsen CC . Biomechanical competence of vertebral trabecular bone in relation to ash density and age in normal individuals. Bone1987;8:79–85.

    Crossref PubMed Google Scholar
    147. Find in article

    Giesen EB , Ding M , Dalstra M , van Eijden TM . Reduced mechanical load decreases the density, stiffness, and strength of cancellous bone of the mandibular condyle. Clin Biomech (Bristol, Avon)2003;18:358–363.

    Crossref PubMed Google Scholar
    148. Find in article

    Giesen EB , Ding M , Dalstra M , van Eijden TM . Mechanical properties of cancellous bone in the human mandibular condyle are anisotropic. J Biomech2001;34:799–803.

    Crossref PubMed Google Scholar
    149. Find in article

    Kurutz M , Donáth J , Gálos M , Varga P , Fornet B . Age- and sex-related regional compressive strength characteristics of human lumbar vertebrae in osteoporosis. J Multidiscip Healthc2008;1:105–121.

    Crossref PubMed Google Scholar
    150. Find in article

    McElhaney JH , Fogle JL , Melvin JW et al. . Mechanical properties on cranial bone. J Biomech1970;3:495-511.

    Crossref PubMed Google Scholar
    151. Find in article

    Seo SH , Lee J , Park IH . Efficacy of dual energy x-ray absorptiometry for evaluation of biomechanical properties: bone mineral density and actual bone strength. J Bone Metab2014;21:205–212.

    Crossref PubMed Google Scholar
    152. Find in article

    Topolin´ski T , Cichan´ski A , Mazurkiewicz A , Nowicki K . Applying a stepwise load for calculation of the S-N curve for trabecular bone based on the linear hypothesis for fatigue damage accumulation. Mater Sci Forum2012;726:39–42.

    Google Scholar
    153. Find in article

    Lambers FM , Bouman AR , Tkachenko EV , Keaveny TM , Hernandez CJ . The effects of tensile-compressive loading mode and microarchitecture on microdamage in human vertebral cancellous bone. J Biomech2014;47:3605–3612.

    Crossref PubMed Google Scholar
    154. Find in article

    Balsly CR , Cotter AT , Williams LA et al. . Effect of low dose and moderate dose gamma irradiation on the mechanical properties of bone and soft tissue allografts. Cell Tissue Bank2008;9:289–298.

    Crossref PubMed Google Scholar
    155. Find in article

    Grieb TA , Forng R-Y , Stafford RE et al. . Effective use of optimized, high-dose (50 kGy) gamma irradiation for pathogen inactivation of human bone allografts. Biomaterials2005;26:2033–2042.

    Crossref PubMed Google Scholar
    156. Find in article

    Lv H , Zhang L , Yang F et al. . Comparison of microstructural and mechanical properties of trabeculae in femoral head from osteoporosis patients with and without cartilage lesions: a case-control study. BMC Musculoskelet Disord2015;16:72.

    Crossref PubMed Google Scholar
    157. Find in article

    Pothuaud L , Van Rietbergen B , Mosekilde L et al. . Combination of topological parameters and bone volume fraction better predicts the mechanical properties of trabecular bone. J Biomech2002;35:1091–1099.

    Crossref PubMed Google Scholar
    158. Find in article

    Bargren JH , Andrew C , Bassett L , Gjelsvik A . Mechanical properties of hydrated cortical bone. J Biomech1974;7:239-245.

    Crossref PubMed Google Scholar
    159. Find in article

    Finlay JB , Repo RU . Cartilage impact in vitro: effect of bone and cement. J Biomech1978;11:379–388.

    Crossref PubMed Google Scholar
    160. Find in article

    Aiyangar AK , Vivanco J , Au AG et al. . Dependence of anisotropy of human lumbar vertebral trabecular bone on quantitative computed tomography-based apparent density. J Biomech Eng2014;136:091003.

    Crossref PubMed Google Scholar
    161. Find in article

    Han S , Medige J , Faran K , Feng Z , Ziv I . The ability of quantitative ultrasound to predict the mechanical properties of trabecular bone under different strain rates. Med Eng Phys1997;19:742–747.

    Crossref PubMed Google Scholar
    162. Find in article

    Liu JF , Shim VPW , Lee PVS . Quasi-static compressive and tensile tests on cancellous bone in human cervical spine. Conf Proc Soc Exp Mech Ser2013;5:109–118. (date last accessed 13 August 2018).

    https://link.springer.com/chapter/10.1007/978-1-4614-4427-5_16 Google Scholar
    163. Find in article

    Díaz León JL , Lesso Arroyo R , RodrÍguez Castro R , López Vázquez A . Mechanical characterization of bone allografts, enriched with mesenchymal cells. Int J Des Nat Ecodynamics2016;11:722–730. (date last accessed 13 August 2018).

    https://www.witpress.com/elibrary/dne-volumes/11/4/1282 Google Scholar
    164. Find in article

    Nazarian A , Muller J , Zurakowski D , Müller R , Snyder BD . Densitometric, morphometric and mechanical distributions in the human proximal femur. J Biomech2007;40:2573–2579.

    Crossref PubMed Google Scholar
    165. Find in article

    Townsend PR , Raux P , Rose RM , Miegel RE , Radin EL . The distribution and anisotropy of the stiffness of cancellous bone in the human patella. J Biomech1975;8:363-367.

    Crossref PubMed Google Scholar
    166. Find in article

    Rapillard L , Charlebois M , Zysset PK . Compressive fatigue behavior of human vertebral trabecular bone. J Biomech2006;39:2133–2139.

    Crossref PubMed Google Scholar
    167. Find in article

    Tang SY , Zeenath U , Vashishth D . Effects of non-enzymatic glycation on cancellous bone fragility. Bone2007;40:1144–1151.

    Crossref PubMed Google Scholar
    168. Find in article

    Cotton JR , Winwood K , Zioupos P , Taylor M . Damage rate is a predictor of fatigue life and creep strain rate in tensile fatigue of human cortical bone samples. J Biomech Eng2005;127:213–219.

    Crossref PubMed Google Scholar
    169. Find in article

    Wegrzyn J , Roux JP , Arlot ME et al. . Determinants of the mechanical behavior of human lumbar vertebrae after simulated mild fracture. J Bone Miner Res2011;26:739–746.

    Crossref PubMed Google Scholar
    170. Find in article

    Stauber M , Rapillard L , van Lenthe GH , Zysset P , Müller R . Importance of individual rods and plates in the assessment of bone quality and their contribution to bone stiffness. J Bone Miner Res2006;21:586–595.

    Crossref PubMed Google Scholar
    171. Find in article

    van Lenthe GH , Stauber M , Müller R . Specimen-specific beam models for fast and accurate prediction of human trabecular bone mechanical properties. Bone2006;39:1182–1189.

    Crossref PubMed Google Scholar
    172. Find in article

    Chevalier Y , Pahr D , Allmer H , Charlebois M , Zysset P . Validation of a voxel-based FE method for prediction of the uniaxial apparent modulus of human trabecular bone using macroscopic mechanical tests and nanoindentation. J Biomech2007;40:3333–3340.

    Crossref PubMed Google Scholar
    173. Find in article

    Schwiedrzik J , Gross T , Bina M et al. . Experimental validation of a nonlinear μFE model based on cohesive-frictional plasticity for trabecular bone. Int J Numer Methods Biomed Eng2016;32:e02739.

    Crossref PubMed Google Scholar
    174. Find in article

    Schwiedrzik JJ , Kaudela K-H , Burner U , Zysset PK . Fabric-mechanical property relationships of trabecular bone allografts are altered by supercritical CO2 treatment and gamma sterilization. Bone2011;48:1370–1377.

    Google Scholar
    175. Find in article

    Boustani HN , Zander T , Disch AC , Rohlmann A . Pedicle-screw-based dynamic implants may increase posterior intervertebral disc bulging during flexion. Biomed Tech (Berl)2011;56:327–331.

    Crossref PubMed Google Scholar
    176. Find in article

    Frich LH , Jensen NC , Odgaard A et al. . Bone strength and material properties of the glenoid. J Shoulder Elb Surg1997;6:97–104.

    Crossref PubMed Google Scholar
    177. Find in article

    Hans D , Wu C , Njeh CF et al. . Ultrasound velocity of trabecular cubes reflects mainly bone density and elasticity. Calcif Tissue Int1999;64:18–23.

    Crossref PubMed Google Scholar
    178. Find in article

    Majumdar S , Kothari M , Augat P et al. . High-resolution magnetic resonance imaging: three-dimensional trabecular bone architecture and biomechanical properties. Bone1998;22:445–454.

    Crossref PubMed Google Scholar
    179. Find in article

    Majumdar S , Lin J , Link T et al. . Fractal analysis of radiographs: assessment of trabecular bone structure and prediction of elastic modulus and strength. Med Phys1999;26:1330–1340.

    Crossref PubMed Google Scholar
    180. Find in article

    Ouyang X , Majumdar S , Link TM et al. . Morphometric texture analysis of spinal trabecular bone structure assessed using orthogonal radiographic projections. Med Phys1998;25:2037–2045.

    Crossref PubMed Google Scholar
    181. Find in article

    Ojanen X , Tanska P Malo MKH,et al.. Tissue viscoelasticity is related to tissue composition but may not fully predict the apparent-level viscoelasticity in human trabecular bone - An experimental and finite element study. J Biomech2017;65:96–105.

    Google Scholar
    182. Find in article

    Cyganik L , Binkowski M , Popik P et al. . Experimental verification of the relationships between Young’s modulus and bone density using DIC. In: KleiberM, BurczynskiT, WildeK, GoskiJ, eds. Advances in Mechanics: Theoretical, Computational and Interdisciplinary Issues: Proceedings of the 3rd Polish Congress of Mechanics (PCM) and 21st International Conference on Computer Methods in Mechanics (CMM). Gdansk: CRC Press, 2016:133-136.

    Google Scholar
    183. Find in article

    Langton CM , Njeh CF . The Physical Measurement of Bone. USA: CRC Press, 2003.

    Google Scholar
    184. Find in article

    García-Rodríguez S , Smith EL , Ploeg H-L . A calibration procedure for a bone loading system. J J Med Device2008;2:11006.

    Google Scholar
    185. Find in article

    Ouyang X , Lin JC , Link T et al. . Biomechanical strength versus spinal trabecular bone structure assessed using contact radiography and texture analysis. Proc SPIE - Int Soc Opt Eng1997;3034:165–174.

    Google Scholar
    186. Find in article

    Bone MC , Dold P , Flohr M et al. . The influence of the strength of bone on the deformation of acetabular shells: a laboratory experiment in cadavers. Bone Joint J2015;97–B:473–477.

    Crossref PubMed Google Scholar
    187. Find in article

    Christensen P , Larsen HS , Lian R , Vang PS . Mechanical testing of the trabecular bone of the knee in knee alloplasty. Ugeskr Laeger1981;143:3127–3130. (in Danish)

    Google Scholar
    188. Find in article

    Nicholson PHF , Strelitzki R . On the prediction of Young’s modulus in calcaneal cancellous bone by ultrasonic bulk and bar velocity measurements. Clin Rheumatol1999;18:10–16.

    Google Scholar
    189. Find in article

    Rho JY , Flaitz D , Swarnakar V , Acharya RS . The characterization of broadband ultrasound attenuation and fractal analysis by biomechanical properties. Bone1997;20:497–504.

    Crossref PubMed Google Scholar
    190. Find in article

    Shim VPW , Yang LM , Liu JF , Lee VS . Characterisation of the dynamic compressive mechanical properties of cancellous bone from the human cervical spine. Int J Impact Eng2006;32:525–540.

    Google Scholar
    191. Find in article

    Zhang Z-M , Li Z-C , Jiang L-S , Jiang S-D , Dai L-Y . Micro-CT and mechanical evaluation of subchondral trabecular bone structure between postmenopausal women with osteoarthritis and osteoporosis. Osteoporos Int2010;21:1383–1390.

    Crossref PubMed Google Scholar
    192. Find in article

    Jankowska-Kuchta E , Kasprzak H , Fechner G . Comparison of mechanical properties of the bone investigated by compression test and holographic interferometry. Proc SPIE - Mic Hol Interf Bio1994;2083:319-321. (date last accessed 13 August 2018).

    https://www.spiedigitallibrary.org/conference-proceedings-of-spie/2083/0000/Comparison-of-mechanical-properties-of-the-bone-investigated-by-compression/10.1117/12.167405.short Google Scholar
    193. Find in article

    Parsch D , Breitwieser T , Breusch SJ . Mechanical stability of structured bone grafts from the anterior iliac crest. Clin Biomech (Bristol, Avon)2008;23:955–960.

    Crossref PubMed Google Scholar
    194. Find in article

    Stein ID , Granik G . Human vertebral bone: relation of strength, porosity, and mineralization to fluoride content. Calcif Tissue Int1980;32:189–194.

    Crossref PubMed Google Scholar
    195. Find in article

    Evans FG , Wood JL . Mechanical properties and density of bone in a case of severe endemic fluorosis. Acta Orthop Scand1976;47:489–495.

    Crossref PubMed Google Scholar
    196. Find in article

    Ashby MF , Evans AG , Fleck NA et al. . Metal Foams: A Design Guide. First ed. Boston, Massachusetts: Butterworth-Heinemann, 2000.

    Google Scholar
    197. Find in article

    Novitsakaya E , Chen P-Y , Hamed E et al. . Recent advances on the measurement and calculation of the elastic moduli of cortical and trabecular bone: a review. Theoret Appl Mech2011;38:209-297.

    Google Scholar
    198. Find in article

    Lotz JC , Gerhart TN , Hayes WC . Mechanical properties of metaphyseal bone in the proximal femur. J Biomech1991;24:317-329.

    Crossref PubMed Google Scholar
    199. Find in article

    Nyman JS , Roy A , Shen X et al. . The influence of water removal on the strength and toughness of cortical bone. J Biomech2006;39:931–938.

    Crossref PubMed Google Scholar
    200. Find in article

    Mayeur O , Haugou G , Chaâri F et al. . Quasi-static and dynamic behaviour of the bone structures with fine geometric and materials modelling aspects. EPJ Web Conf2012;26:3008. (date last accessed 25 May 2018).

    https://www.epj-conferences.org/articles/epjconf/abs/2012/08/epjconf_dymat2012_03008/epjconf_dymat2012_03008.html Google Scholar
    201. Find in article

    Wang X , Nyman JS , Dong X , Leng H , Reyes M . Fundamental Biomechanics in Bone Tissue Engineering: Synthesis Lectures on Tissue Engineering. San Rafael, California: Morgan & Claypool Publishers, 2010.

    Google Scholar
    202. Find in article

    Keaveny TM , Borchers RE , Gibson LJ , Hayes WC . Trabecular bone modulus and strength can depend on specimen geometry. J Biomech1993;26:991-1000.

    Crossref PubMed Google Scholar
    203. Find in article

    No authors listed. Standard Test Method for Compressive Properties of Rigid Plastics. ASTM D695-15. ASTM International, 2015. (date last accessed 25 May 2018).

    https://www.astm.org/Standards/D695.htm Google Scholar
    204. Find in article

    Tawy GF , Rowe PJ , Riches PE . Thermal damage done to bone by burring and sawing with and without irrigation in knee arthroplasty. J Arthroplasty2016;31:1102–1108.

    Crossref PubMed Google Scholar
    205. Find in article

    Butler-Smith PW , Axinte DA , Daine M . Solid diamond micro-grinding tools: from innovative design and fabrication to preliminary performance evaluation in Ti–6Al–4V. Int J Mach Tools Manuf2012;59:55–64.

    Google Scholar
    206. Find in article

    Tang L , Tsai C , Gerberich WW , Kruckeberg L , Kania DR . Biocompatibility of chemical-vapour-deposited diamond. Biomaterials1995;16:483–488.

    Crossref PubMed Google Scholar
    207. Find in article

    Keaveny TM , Guo XE , Wachtel EF , McMahon TA , Hayes WC . Trabecular bone exibits fully linear elastic behavior and yields at low strains. J Biomech1994;27:1127–1136.

    Google Scholar
    208. Find in article

    Dong XN , Yeni YN , Les CM , Fyhrie DP . Effects of end boundary conditions and specimen geometry on the viscoelastic properties of cancellous bone measured by dynamic mechanical analysis. J Biomed Mater Res A2004;68:573–583.

    Crossref PubMed Google Scholar
    209. Find in article

    Kalidindi SR , Abusafieh A , Ei-Danaf E . Accurate characterization of machine compliance for simple compression testing. Exp Mech1997;37:210-215.

    Google Scholar
    210. Find in article

    Grassi L , Isaksson H . Extracting accurate strain measurements in bone mechanics: A critical review of current methods. J Mech Behav Biomed Mater2015;50:43–54.

    Crossref PubMed Google Scholar
    211. Find in article

    No authors listed. Surface preparation for strain gage bonding. instruction bulletin B-129-8. Micro measurements. (date last accessed 29 May 2018).

    http://www.vishaypg.com/docs/11129/11129B129.pdf Google Scholar
    212. Find in article

    Grassi L , Väänänen SP , Yavari SA et al. . Full-field strain measurement during mechanical testing of the human femur at physiologically relevant strain rates. J Biomech Eng2014;136:111010.

    Crossref PubMed Google Scholar
    213. Find in article

    Lakes RS , Katz JL , Sternstein SS . Viscoelastic properties of wet cortical bone-I. Torsional and biaxial studies. Biomechanics1979;12:657–678.

    Google Scholar
    214. Find in article

    Bunshah RF . Techniques of Metals Research: Measurement of Mechanical Properties. Ann Arbor, Michigan: Interscience Publishers, 1971.

    Google Scholar