Baboon Bone Structure

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Changes in the Fracture Toughness of Bone May Not Be

Reflected in Its Mineral Density, Porosity, andTensile Properties

X. D. WANG,1 N. S. MASILAMANI,1 J. D. MABREY,1 M. E. ALDER,2 and C. M. AGRAWAL1

1 Department of Orthopaedics and 2 Department of Dental Diagnostic Science, The University of Texas Health Science Center at San Antonio,

San Antonio, TX, USA

Age-related changes in the skeleton often lead to an increase

in the susceptibility of bone to fracture. Such changes most

likely occur in the constituents of bone, namely, the mineraland organic phases, and in their spatial arrangement mani-

fested as orientation and microstructure. In the past, how-

ever, bone loss or decline in bone mineral density has been

considered to be the major contributing factor for the in-

creased risk of bone fractures, and elastic modulus and

ultimate strength have been commonly used to assess bone

quality and strength. However, whether these properties

provide sufficient information regarding the likelihood of

bone to fracture remains debatable. Using a novel fracture

toughness test, which measures the energy or stress intensity

required to propagate a crack within a material, the objective

of this study was to investigate if the mineral density and

mechanical properties of bone can accurately predict bone

fragility as measured by fracture toughness. Changes infracture toughness ( K IC ), bone mineral density (BMD), elas-

tic modulus ( E), yield and ultimate strength ( y and s),

porosity ( P0

), and microhardness ( H v) of bone were examined

as a function of age in a baboon model. With increasing age,

the fracture toughness of bone decreased, and its microhard-

ness increased. However, no significant changes were found

in BMD, E, P0

, y, and s as a function of age. In addition,

simple regression analyses revealed no significant correlation

between bone fracture toughness and the other parameters,

except for microhardness of bone. The results of this study

indicate that changes in bone fracture toughness may not be

necessarily reflected in its mineral density, porosity, elastic

modulus, yield strength, and ultimate strength. (Bone 23:

67–72; 1998) © 1998 by Elsevier Science Inc. All rightsreserved.

Key Words: Bone; Bone mineral density; Fracture toughness;Tensile properties; Microhardness; Porosity.

Introduction

Age-related changes in the skeleton may lead to an increase in

the susceptibility of bone to fracture.22

Such changes most likelyoccur in the constituents of bone, namely, the mineral andorganic phases, and in their spatial arrangements, such as orien-tation and microstructure.15,23 Although decreased bone mineraldensity (BMD) has been shown to be a major contributing factorof fracture risk,9,12 the roles of other factors, such as bonemicrostructure and organic phase, are still not well understood.Some studies have investigated effects of these factors on bonefracture properties.3,16,18,28,29,33,34 For instance, a study by Mc-Calden and coworkers indicated that even without significantchanges in bone mineral density, the tensile strength of bone candecrease with age due to increased porosity.18 Similarly, Yeni etal. showed that the fracture toughness of bone significantlychanged with bone porosity, but had no correlation with mineralcontent.33,34 On the other hand, some studies have demonstrated

that the fracture toughness is correlated with bone density.3,32

Moreover, studies have also reported that variations in bonemicrostructure and osteon morphology result in significantchanges in bone fracture toughness.28,34 As far as the organicphase is concerned, Kovach and colleagues found that changes instructural characteristics of collagen network detected using alaser fluorescence technique significantly correlated with bonefracture toughness.16 In a recent study conducted by Wang et al.,collagen denaturation was found to correlate significantly withthe fracture toughness of bone,29 showing that besides bonemineral density, porosity, and bone microstructure, changes inthe collagen network can also lead to significant variations inbone fracture properties. All these results suggest that bonefracture properties are determined by multiple factors.

In the past, elastic modulus and ultimate strength have beencommonly used to assess bone quality and strength.18,21 How-ever, whether these properties can provide sufficient informationregarding the likelihood of bone to fracture is still debatable.Because in vivo bone fractures are often initiated and/or pro-moted by cracks,27 fracture toughness, a measure of the energyor stress intensity required to propagate a crack within a material,may provide a more meaningful assessment of the susceptibilityof bone to fracture. Based on this consideration, researchers havestarted to investigate bone fracture behavior using various frac-ture mechanics approaches. Although bone is neither homoge-neous nor isotropic, Norman et al. demonstrated that linearelastic fracture mechanics approaches are still valid for assessingthe fracture toughness of bone as long as the same type of bone

Address for correspondence and reprints: Xiaodu Wang, Ph.D., Ortho-

paedic Bioengineering, The University of Texas Health Science Center,

7703 Floyd Curl Drive, San Antonio, TX 78284-7774. E-mail:

[email protected]

Bone Vol. 23, No. 1July 1998:67–72

67© 1998 by Elsevier Science Inc. 8756-3282/98/$19.00All rights reserved. PII S8756-3282(98)00071-4


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is compared.20 Besides mode I fracture toughness,5,20 somerecent studies also investigated mode II (shear) and mode III(tear) fracture toughness of bone.13,19 However, most of thesetechniques are only suitable for testing large bone specimensfrom large species such as bovine. This drawback has strictlylimited the use of well controlled animal models in studying bone

fracture properties. To alleviate this problem, a novel “sandwich”technique has been recently developed to allow for testing of bone specimens from animals as small as rabbits.30

The hypothesis of the present study is that the measurementsof bone mineral density, porosity, and tensile properties alone donot necessarily reflect changes in the fracture toughness of bone.Using the sandwich technique and a baboon model, this studywas performed to investigate the correlation of bone fracturetoughness with bone mineral density, porosity, and tensile prop-erties. Changes in fracture toughness (K IC ), bone mineral density(BMD), elastic modulus ( E ), yield and ultimate strength ( y ands), porosity (P0), and microhardness ( H v) of bone were exam-ined as a function of age.

Materials and Methods

Femora from 18 baboons (8 males and 10 females), ranging from6 to 26 years of age, were obtained from the Southwest Foun-dation for Biomedical Research, San Antonio, Texas, and freshfrozen at 20°C until testing. All animals were carefullyscreened to avoid the influence of any pathologies on bone.Baboons commonly reach skeletal maturity at approximately 6years of age,2 and their life span is usually considered to be 20years. To cover the age ranges of young adults, middle aged, andthe elderly, these animals were divided into three age groups:6–9, 10–16, and over 16 years old, respectively (n 6 in eachgroup). Haversian bone was the dominant microstructure of thebaboon bone samples tested in this study. There were three malesand three females each in the young adult and elderly groups,whereas the middle aged group was comprised of two males andfour females.

The mid-diaphysis was extracted from each femur and usedfor preparing biomechanical test specimens. Before specimenpreparation, the BMD of these mid-diaphyseal samples wasmeasured using quantitative computed tomography (QCT). Ingeneral, it is desirable to measure the BMD directly on the testspecimens. However, the specimen size used in this study wastoo small to acquire accurate BMD measurements. To ensure thatthe measured BMD values were representative of the test spec-imens, all measurements were made at the cross section of thediaphysis from where the test specimens were subsequentlyobtained. An area of 2 2 mm was used for each measurement.A hydroxyapatite phantom with three known densities was usedto obtain a calibration curve: QCT measurements (in

hounsfields) vs. hydroxyapatite density (g/cm

3

). Values of BMDwere then calculated based on this calibration curve and QCTreadings.

A single-layer compact sandwich (SCS) specimen (Figure 1)was used to estimate the mode I fracture toughness (critical stressintensity factor, K IC ), which is a measure of the resistance of amaterial to crack growth.30 To fabricate this specimen, polym-ethylmethacrylate (PMMA) was used as the holder material.Longitudinal bone coupons (20 3.5 2 mm) were cut andmachined from the lateral aspect of each femoral diaphysis. Thebonding surfaces of the coupons were first cleaned and dehy-drated by acetone and dried for 5 sec using pressurized air. Thecoupons were then carefully cemented between two PMMAholders using a cyanoacrylate adhesive (Quicktite™, LoctiteCorp., Rocky Hill, CT). As shown in Figure 1, a starter notch was

cut in the middle of the bone interlayer using a circular saw and

then a precrack was introduced using a sharp razor blade. Thespecimens were kept moist throughout the preparation and test-ing process, which followed a procedure previously described.28

In this study, only longitudinal fracture toughness was measureddue to lack of bone stock for preparing test specimens in otherorientations. It has been demonstrated that bone fracture tough-ness alters with respect to crack orientations, and the longitudinaldirection is the weakest orientation in bone.4,6

The E , y, and s of bone were determined using a tensiletest. Flat dumb-bell shaped tensile test specimens were extractedfrom the lateral aspect of the same mid-diaphysis used for thefracture toughness test specimens. Because the bone stock at thelateral aspect was limited, the size of the tensile specimens wasdetermined by the available bone volume remaining after thefracture toughness test specimens were taken. The overall length,gage length, gage width, and gage thickness of the specimenswere 30, 10, 2, and 1 mm, respectively. These specimens wereloaded to failure in tension in an Instron machine at a constantloading speed (3 mm/min), and the resulting load-displacementcurve was used to calculate the elastic modulus and tensilestrength of bone.

The measurements of porosity were performed on a cross

section of the diaphysis adjacent to the site from where thebiomechanical test specimens were taken. The cross section wasembedded in a plastic resin and polished following standardprocedures for engineering materials. Thereafter, an image of thecross section was digitized into a computer via a light micro-scope. Then an image processing and computational code writtenin the National Institutes of Health (NIH) Image macro program-ming language was used to calculate the ratio of the area of cavities (Haversian and vascular canals) with respect to thewhole area of the image. This ratio was defined as the porosityof bone.

Vickers microhardness was measured using a microhardnesstester (Micromet, Adolph I. Buehler, Inc., Evanston, IL) on thesame cross section utilized for measuring porosity. To be con-sistent, microhardness was measured only in the interstitial

regions. An average microhardness value was obtained from

Figure 1. Configuration of an SCS specimen for bone fracture toughnesstests. A bone coupon was sandwiched between two holders and a notchwith a precrack at its end was introduced in the middle of the bone layer.The specimen was loaded until the crack propagated through the bonelayer. The key dimensions of the specimen were W 17.5 mm, B 3.5mm, h 2 mm, and a 7.5 mm.

68 X. D. Wang et al. Bone Vol. 23, No. 1Fracture toughness vs. BMD, porosity, and tensile property July 1998:67–72


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three measurements at randomly selected locations on eachsample.

All experimental data were compiled as mean and standarddeviation (mean SD). A one-way analysis of variance(ANOVA) was employed to detect differences in all measuredparameters as a function of age. The parameters indicatingsignificant changes with age were considered to be the age-dependent parameters, and a simple regression analysis wasutilized to explore the correlation between the measuredparameters.

Results

The experimental results are summarized in Table 1. Althoughthe fracture toughness changed significantly as a function of age( p 0.05), no significant difference was observed between theyoung adult and middle-aged group (6–10 and 11–16 years,respectively). The mean fracture toughness values for these twoage groups were similar to that (2.17 0.27 MPam) obtainedin a previous study.31 However, the fracture toughness sharplydropped for the elderly group (16 years) as shown in Figure 2.

The microhardness of bone ( H v) was another parameter that

changed significantly with age ( p

0.05). In the ANOVAanalysis, the microhardness showed no significant changes foryoung adult and middle-aged groups, but in contrast to fracture

toughness, increased sharply for the elderly group as shown inFigure 3.

No statistically significant differences were found in E , BMD, y, s, and P0 between the three age groups ( p 0.05).

Simple regression analyses showed that no significant corre-lation existed between BMD, porosity, tensile properties, andfracture toughness of bone ( p 0.05). However, the regressionanalysis indicated that the fracture toughness decreased withincreasing microhardness (Figure 4), although there was only arelatively weak correlation between the two ( p 0.077).

Discussion

To evaluate the biomechanical competence of bone, two basicaspects have to be taken into account: morphometric and materialproperties. Morphometric properties provide information per-taining to the size, shape, and other structural characteristics of bone, while material properties are representative of its intrinsicmechanical properties. The strength of any given bone relies onboth these properties, and age-related changes in bone may occurexclusively in either of them or simultaneously in both. In thisstudy, only the material properties of baboon cortical bone were

examined as a function of age. Among the parameters measured,

Table 1. Summary of experimental data (n 6)

Age (years)K IC

(MPam) E (GPa) s (MPa) y (MPa) d m (g/cm3) H v (kg/mm

2) P0 (%)

6–10 2.25 .18 4.55 1.82 180 26.6 147 3.4 1.33 0.01 48.9 4.1 3.3 1.2

11–16 2.28

.29 4.89

0.80 164

12.1 139

11.6 1.29

0.01 51.3

5.2 3.6

1.316 1.73 .25 5.03 1.47 190 14.2 154 15.5 1.35 0.02 60.5 10.2 5.4 2.8ANOVA p 0.002 p 0.8 p 0.09 p 0.18 p 0.2 p 0.03 p 0.3

Differences are significant only when p 0.05. K IC : mode I fracture toughness; E : elastic modulus; s: ultimate strength; y: yield strength; d m: bonemineral density measured using QCT; H v: Vickers microhardness; and P0: porosity measured on the cross section of femora using an image processingtechnique.

Figure 2. Fracture toughness of bone as a function of age. Mode Ilongitudinal fracture toughness (K IC ) was measured using a single-layersandwich specimen. A significant decrease in K IC was found for the

elderly compared to younger groups ( p 0.05).

Figure 3. Microhardness of bone as a function of age. The microhard-ness ( H v) of the interstitial regions was measured on the cross section of each femoral diaphysis using a Vickers microhardness tester. A signifi-cant increase in H v was found for the elderly compared to younger groups

( p 0.05).

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age-related changes were detected only in the fracture toughnessand interstitial microhardness of bone, while the BMD, porosity,and tensile properties exhibited no significant changes. Theseresults indicate that: (1) the fracture toughness of bone decreaseswith age; (2) bone fracture toughness varies even though nochanges occur in its BMD, porosity, and tensile properties; and(3) besides BMD and porosity, other factors may be responsiblefor the decreased fracture toughness of bone.

Baboon bone samples tested in this study exhibited no sig-nificant changes in both porosity and BMD with increasing age,which is not in good agreement with the results obtained fromhuman cortical bone in the literature.18,33,34 This is probably dueto the differences between the two species. For instance, theporosity value of baboon cortical bone obtained in this studyvaried between 3% and 8%, which is extremely small comparedto reported values (between 5% and 30%) of human corticalbone.18,34 Given this small range, normal limitations associatedwith data measurements, and other non-age-related differencesbetween the specimens, it is quite likely that tests in the presentstudy were unable to detect age-related changes in the porosity of baboon bone. A further, more detailed, study with a large number

of specimens will be required to explore this issue. However, itshould be pointed out that the intent of the present study was toinvestigate the correlation of fracture toughness of bone with itsmineral density, porosity, and tensile properties. Although age-related changes in baboon bone may not closely mimic similarchanges in human bone, it is unlikely that this difference wouldsignificantly influence the correlation between bone properties.

It is noteworthy that in the present study the mean elasticmodulus values were within the range of 4.55–5.03 GPa for thedifferent age groups, and were much smaller compared to thevalue (15.4 GPa) obtained in a three-point bending test in aprevious study.31 This is probably due to the effects of a smallspecimen size. It has been found that a small specimen size canlead to decreased bone stiffness values due to the weakeningeffects of osteons.10 In addition, all testing systems have an

inherent error caused by system deformation and play in their

moving parts. Such errors can lead to an underestimation of elastic modulus if the deformation of test specimens is very smalland of the same order of magnitude as the errors. However, sucherrors would be expected to have little influence on detectingrelative differences between the specimens as long as the spec-imen size and test condition are consistent. Moreover, due to the

restrictions imposed by limited bone stock and the test method-ologies used, the failure planes in fracture toughness and tensiletests were different. In the fracture toughness test, cracks travelin a longitudinal plane, whereas in the tensile test failure occursat the transverse plane of the femoral diaphysis. Thus, these twotests would reflect age-related changes in bone at differentorientations. Finally, it should be pointed out that due to limitedspecimen sizes the measurements of BMD, porosity, and micro-hardness were not performed directly on the biomechanical testspecimens. However, since all these measurements were per-formed at a similar anatomical location, the values obtainedwould be expected to be representative of the test specimens.

Baboon bone samples tested in this study exhibited no sig-nificant changes in both porosity and BMD with increasing age,which is not in agreement with the results obtained from human

cortical bone in the literature.18,33,34 This is probably due to thediscrepancy between the two species. For instance, the porosityvalue of baboon cortical bone obtained in this study varied in arange between 3% and 8%, which is extremely small comparedto that (between 5% and 30%) of human cortical bone reportedin the literature.18,34 Considering non-age-related differencesbetween the samples and errors associated with the measurement,it is possible that the sample size used in this study was too smallto detect age-related changes in such a small range (a fewpercent) for the baboon bone samples tested. However, it shouldbe pointed out that the intent in the present study was toinvestigate the correlation of the fracture toughness of bone withits mineral density, porosity, and tensile properties. Althoughage-related changes in baboon bone may be more or less differ-ent from humans, it is unlikely that such a discrepancy may causemisleading conclusions to be made when the correlation betweenthe bone properties is explored in this baboon model.

Age-related changes in the longitudinal fracture toughness of bone have been reported by several investigators.6,8,19 The re-sults of their studies on human bone indicated that the fracturetoughness of bone decreased with age for both genders. Theresults of our study exhibited the same trend in baboon bone,suggesting that bone becomes more susceptible to crack growthwith increasing age.

In the present study, the BMD measured is actually anapparent mineral density, which represents the amount of mineralin a unit volume of bone. Thus, its value is primarily influencedby two factors: true mineral density and porosity. No significantage-related changes were found in both BMD and porosity in this

study, thereby indicating no significant changes in the truemineral density as well. Because elastic modulus of bone isdetermined primarily by bone mineral content (or true densi-ty),11,17,25 similar elastic modulus values would be expected forall age groups tested. This result is in agreement with reports onhuman bone by McCalden et al.18 and Yeni et al.33 Moreover, theresults of our study indicate that the ultimate strength wasrelatively constant over the different ages. Considering the factthat there was little variation in BMD and porosity in the bonespecimens tested (Table 1), no significant changes in bonestrength would be expected because the ultimate strength of boneis primarily determined by these factors.18,26 However, the frac-ture toughness of these bone specimens changed significantly,suggesting that the ultimate strength of bone may not adequatelyreflect its fracture toughness. This is not surprising because these

two parameters describe different aspects of the biomechanical

Figure 4. Correlation of the fracture toughness of bone with its micro-hardness. A relatively weak correlation ( p 0.077) was found betweenthe two parameters in a simple regression analysis. The dotted linedepicts the linear regression of the data (r 2 0.26).



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behavior of bone; fracture toughness measures the ability of amaterial to resist fractures associated with crack propagation,1

while the ultimate strength does not take cracks into account.Additionally, these two tests actually reflect bone fracture prop-erties in different orientations (e.g., longitudinal and transverse).Because bone is anisotropic in nature, bone fracture properties

may vary significantly in different orientations.4,28 In a recentstudy, Zioupos and Currey reported that the transverse fracturetoughness of human cortical bone had a strong correlation withthe stiffness and strength obtained in the same orientation.35

Thus, the correlation between bone fracture properties is orien-tation dependent.

Bone is a composite material comprising mineral and organicphases.7,14 Changes in any of these components and their spatialarrangement may contribute to the fracture toughness of bone.Among the relevant parameters, bone density has been reportedto be significantly correlated with mode I (tension) fracturetoughness of bone.6,32 Similarly, Yeni et al. reported that themode I fracture toughness of human femora significantly corre-lated with bone density, but exhibited little correlation with bone

mineral content.33

In another study, Yeni et al. found that bonefracture toughness decreased with increasing porosity as a func-tion of age.34 In the present study, the fracture toughness of baboon bone showed significant changes irrespective of rela-tively constant BMD and porosity. These results suggest thatbone fracture toughness may be affected not only by mineraldensity and porosity but by some other factors as well. In somerecent studies relevant to this issue, it was determined that theintegrity of the collagen network (90% of organic phase of bone)also plays a role in determining bone fracture properties.16,29

Also it was reported that bone fracture toughness had a signifi-cant correlation with osteon morphology (e.g., size, area, anddensity, etc.).34 Thus, it is possible that without significantchanges in bone mineral phase and porosity, bone fracture

toughness can change due to the variation in osteon morphologyand the organic phase.In general, microhardness is a material property that reflects

a combination of the elastic modulus ( E ) and yield strength( y).

24 The linear regression analyses, however, did not showsignificant correlation between interstitial microhardness andelastic modulus or yield strength of bone for the animals tested( p 0.05). In this study, we only measured interstitial micro-hardness. Because Haversian systems also play a role in deter-mining bone mechanical properties, it is possible that an increasein the interstitial microhardness may not lead to significantchanges in mechanical properties of the entire tissue. Moreover,although both the microhardness and fracture toughness of bonechanged as a function of age, there was only a relatively weak correlation between the interstitial microhardness and fracture

toughness of bone ( p 0.077). Because the measured micro-hardness only reflects material properties of interstitial region, astronger correlation may become obvious if the influence of Haversian systems is taken into consideration. The underlyingmechanisms for the relationship between fracture toughness andmicrohardness are not clear and further studies are needed toaddress this issue.

In summary, the results of this study indicate that interstitialmicrohardness and longitudinal fracture toughness of baboonbone significantly change with age. However, these changes arenot reflected in the elastic modulus and tensile strength and areindependent from the apparent bone mineral density and poros-ity. This suggests that apparent mineral density, porosity, andtensile properties alone do not always reflect changes in the

fracture toughness of bone.

Acknowledgments: Special thanks are due to Dr. G. B. Hubbert, S.McAnn, and M. Silva, Southwest Foundation for Biomedical Science,San Antonio, TX, for providing the baboon tissue.

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Date Received: September 18, 1997

Date Revised: March 30, 1998

Date Accepted: March 31, 1998


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Baboon Bone Structure