Abstract

The fracture properties of cortical bone are directly coupled to its complex hierarchical structure. The limited availability of bone material from many anatomic locations creates challenges for assessing the effect of bone heterogeneity and anisotropy on fracture properties. The small punch technique was employed to examine the fracture behavior of cortical bone in terms of area under the curve values obtained from load–load point displacement behavior. Fracture toughness of cortical bone was also determined in terms of J-toughness values obtained using a compact tension (CT) test. Area under the curve values obtained from the small punch test were correlated with the J-toughness values of cortical bone. The effects of bone density and compositional parameters on area under the curve and Jtoughness values were also analyzed using linear and multiple regression analysis. Area under the curve and J-toughness values are strongly and positively correlated. Bone density and %mineral content are positively correlated with both area under the curve and J-toughness values. The multiple regression analysis outcomes support these results. Overall, the findings support the hypothesis that area under the curve values obtained from small punch tests can be used to assess the fracture behavior of cortical bone.

References

1.
Burr
,
D. B.
,
Forwood
,
M. R.
,
Fyhrie
,
D. P.
,
Martin
,
R. B.
,
Schaffler
,
M. B.
, and
Turner
,
C. H.
,
1997
, “
Bone Microdamage and Skeletal Fragility in Osteoporotic and Stress Fracture
,”
J. Bone Miner. Res.
,
12
(
1
), pp.
6
15
.10.1359/jbmr.1997.12.1.6
2.
Burr
,
D. B.
,
Martin
,
R. B.
,
Schaffler
,
M. B.
, and
Radin
,
E. L.
,
1985
, “
Bone Remodeling in Response to In Vivo Fatigue Microdamage
,”
J. Biomech.
,
18
(
3
), pp.
189
200
.10.1016/0021-9290(85)90204-0
3.
Doblare
,
M.
,
Garcia
,
J. M.
, and
Gomez
,
M. J.
,
2004
, “
Modeling Bone Tissue Fracture and Healing: A Review
,”
Eng. Fract. Mech.
,
71
, pp.
1809
1840
.10.1016/j.engfracmech.2003.08.003
4.
Fantner
,
G. E.
,
Hassenkam
,
T.
,
Kindt
,
J. H.
,
Weaver
,
J. C.
,
Birkedal
,
H.
,
Pechenik
,
L.
,
Cutroni
,
J. A.
,
Cidade
,
G. A. G.
,
Stucky
,
G. D.
,
Morse
,
D. E.
, and
Hansma
,
P. K.
,
2005
, “
Sacrificial Bonds and Hidden Length Dissipate Energy as Mineralized Fibrils Separate During Bone Fracture
,”
Nat. Mater.
,
4
(
8
), pp.
612
616
.10.1038/nmat1428
5.
Vashishth
,
D.
,
Tanner
,
K. E.
, and
Bonfield
,
W.
,
2003
, “
Experimental Validation of a Microcracking-Based Toughening Mechanism for Cortical Bone
,”
J. Biomech.
,
36
(
1
), pp.
121
124
.10.1016/S0021-9290(02)00319-6
6.
Brown
,
C. U.
,
Yeni
,
Y. N.
, and
Norman
,
T. L.
,
2000
, “
Fracture Toughness Is Dependent on Bone Location—A Study of the Femoral Neck, Femoral Shaft, and the Tibial Shaft
,”
J. Biomed. Mater. Res.
,
49
(
3
), pp.
380
389
.10.1002/(SICI)1097-4636(20000305)49:3<380::AID-JBM11>3.0.CO;2-W
7.
Nalla
,
R. K.
,
Kruzic
,
J. J.
, and
Ritchie
,
R. O.
,
2004
, “
On the Origin of the Toughness of Mineralized Tissue: Microcracking or Crack Bridging
,”
Bone
,
34
(
5
), pp.
790
798
.10.1016/j.bone.2004.02.001
8.
Sharma
,
N. K.
,
Pal
,
R.
,
Sehgal
,
D. K.
, and
Pandey
,
R. K.
,
2014
, “
Application of Elastic-Plastic Fracture Mechanics to Determine the Locational Variation in Fracture Properties of Cortical Bone
,”
Mater. Perform. Charact.
,
3
(3), pp.
429
447
.10.1520/MPC20130069
9.
Zioupos
,
P.
, and
Currey
,
J. D.
,
1998
, “
Changes in the Stiffness, Strength and Toughness of Human Cortical Bone With Age
,”
Bone
,
22
(
1
), pp.
57
66
.10.1016/S8756-3282(97)00228-7
10.
Giannoudis
,
P.
,
Tzioupis
,
C.
,
Almalki
,
T.
, and
Buckley
,
R.
,
2007
, “
Fracture Healing in Osteoporotic Fractures: Is It Really Different? A Basic Science Perspective
,”
Injury
,
38
(
1
), pp.
S90
S99
.10.1016/j.injury.2007.02.014
11.
Burstein
,
A. H.
,
Reilly
,
D. T.
, and
Martens
,
M.
,
1976
, “
Aging of Bone Tissue: Mechanical Properties
,”
J. Bone Jt. Surg.
,
58
(
1
), pp.
82
86
.10.2106/00004623-197658010-00015
12.
Nalla
,
R. K.
,
Kruzic
,
J. J.
,
Kinney
,
J. H.
, and
Ritchie
,
R. O.
,
2004
, “
Effect of Aging on the Toughness of Human Cortical Bone: Evaluation by R-Curves
,”
Bone
,
35
(
6
), pp.
1240
1246
.10.1016/j.bone.2004.07.016
13.
Behiri
,
J. C.
, and
Bonfield
,
W.
,
1989
, “
Orientation Dependence of the Fracture Mechanics of Cortical Bone
,”
J. Biomech.
,
22
(
8–9
), pp.
863
867
.10.1016/0021-9290(89)90070-5
14.
Wright
,
T. M.
, and
Hayes
,
W. C.
,
1977
, “
Fracture Mechanics Parameters for Cortical Bone-Effects of Density and Specimen Thickness
,”
J. Biomech.
,
10
(
7
), pp.
419
425
.10.1016/0021-9290(77)90019-7
15.
Nalla
,
R. K.
,
Kinney
,
J. H.
, and
Ritchie
,
R. O.
,
2003
, “
Mechanistic Fracture Criteria for the Failure of Human Cortical Bone
,”
Nat. Mater.
,
2
(
3
), pp.
164
168
.10.1038/nmat832
16.
Yan
,
J.
,
Mecholsky
,
J.
, and
Clifton
,
K. B.
,
2007
, “
How Tough Is Bone? Application of Elastic-Plastic Fracture Mechanics to Bone
,”
Bone
,
40
(
2
), pp.
479
484
.10.1016/j.bone.2006.08.013
17.
Koester
,
K. J.
,
Ager
,
J. W.
, III
, and
Ritchie
,
R. O.
,
2008
, “
How Tough Is Cortical Human Bone? In-Situ Measurements on Realistically Short Cracks
,”
Nat. Mater.
,
7
(
8
), pp.
672
677
.10.1038/nmat2221
18.
Nalla
,
R. K.
,
Kruzic
,
J. J.
,
Kinney
,
J. H.
, and
Ritchie
,
R. O.
,
2005
, “
Mechanistic Aspects of Fracture and R-Curve Behavior in Human Cortical Bone
,”
Biomaterials
,
26
(
2
), pp.
217
231
.10.1016/j.biomaterials.2004.02.017
19.
Vashishth
,
D.
,
Behiri
,
J. C.
, and
Bonfield
,
W.
,
1997
, “
Crack Growth Resistance in Cortical Bone: Concept of Micro-Crack Toughening
,”
J. Biomech.
,
30
(
8
), pp.
763
769
.10.1016/S0021-9290(97)00029-8
20.
Malik
,
C. L.
,
Stover
,
S. M.
,
Martin
,
R. B.
, and
Gibeling
,
J. C.
,
2003
, “
Equine Cortical Bone Exhibits Rising R-Curve Fracture Mechanics
,”
J. Biomech.
,
36
(
2
), pp.
191
198
.10.1016/S0021-9290(02)00362-7
21.
Yang
,
Q. D.
,
Cox
,
B. N.
,
Nalla
,
R. K.
, and
Ritchie
,
R. O.
,
2006
, “
Re-Evaluating the Toughness of Human Cortical Bone
,”
Bone
,
38
(
6
), pp.
878
887
.10.1016/j.bone.2005.10.014
22.
Ural
,
A.
, and
Vashishth
,
D.
,
2006
, “
Cohesive Finite Element Modeling of Age-Related Toughness Loss in Human Cortical Bone
,”
J. Biomech.
,
39
(
16
), pp.
2974
2982
.10.1016/j.jbiomech.2005.10.018
23.
Manahan
,
M. P.
,
Argon
,
A. S.
, and
Harling
,
O. K.
,
1981
, “
The Development of Miniaturized Disk Based Test for the Determination of Post Irradiation Mechanical Properties
,”
J. Nucl. Mater.
,
103–104
, pp.
1545
1550
.10.1016/0022-3115(82)90820-0
24.
Huang
,
F. M.
,
Hamilton
,
M. L.
, and
Wire
,
G. L.
,
1982
, “
Bend Testing for Miniature Disk
,”
Nucl. Technol.
,
57
(
2
), pp.
234
242
.10.13182/NT82-A26286
25.
Baik
,
J. M.
,
Kameda
,
J.
, and
Buck
,
O.
,
1983
, “
Small Punch Testing Test Evaluation of Inter-Granular Embrittlement of an Alloy Steel
,”
Scr. Metall.
,
17
(
12
), pp.
1443
1447
.10.1016/0036-9748(83)90373-3
26.
Manahan
,
M. P.
,
1983
, “
A New Post-Irradiation Mechanical Behavior Test: The Miniature Disk Bend Test
,”
Nucl. Technol.
,
63
, pp.
275
295
.10.13182/NT83-A33289
27.
Manahan
,
M. P.
,
Browning
,
A. E.
,
Argon
,
A. S.
, and
Harling
,
O. K.
,
1986
, “
Miniaturized Disk Bend Test Technique Development and Application: The Use of Small Scale Specimen for Testing Irradiated Material
,”
American Society for Testing and Materials
, Philadelphia, PA, Standard No. STP 888.
28.
Kurtz
,
S. M.
,
Foulds
,
J. R.
,
Jewett
,
C. W.
,
Srivastav
,
S.
, and
Edidin
,
A. A.
,
1997
, “
Validation of Small Punch Testing Technique to Characterize the Mechanical Behavior of Ultra High Molecular Weight Polyethylene
,”
Biomaterials
,
18
(
24
), pp.
1659
1663
.10.1016/S0142-9612(97)00124-5
29.
Kurtz
,
S. M.
,
Foulds
,
J. R.
,
Jewett
,
C. W.
, and
Edidin
,
A. A.
,
1999
, “
Miniature Specimen Mechanical Testing Technique Scaled to the Articulated Surface of Polyethylene Components for Total Joint Replacement for Arthoplasty
,”
J. Biomed. Mater. Res.
,
48
(
1
), pp.
75
81
.10.1002/(SICI)1097-4636(1999)48:1>75::AID-JBM13>3.0.CO;2-H
30.
Giddings
,
V. I.
,
Kurdz
,
S. M.
,
Foulds
,
J. R.
,
Jewett
,
C. W.
,
Srivastav
,
S.
, and
Edidin
,
A. A.
,
2001
, “
Small Punch Test Technique for Characterizing the Elastic Modulus and Fracture Behavior of PMMA Bone Cement Used in Total Joint Replacement
,”
Biomaterials
,
22
(
13
), pp.
1875
1881
.10.1016/S0142-9612(00)00372-0
31.
Mao
,
X.
,
Saito
,
M.
, and
Takahashi
,
H.
,
1991
, “
Small Punch Test to Predict Ductile Fracture Toughness JIC and Brittle Fracture Toughness KIC
,”
Scr. Metall. Mater.
,
25
(
11
), pp.
2481
2485
.10.1016/0956-716X(91)90053-4
32.
Mao
,
X.
,
Shoji
,
T.
, and
Takahashi
,
H.
,
1987
, “
Characterization of Fracture Behavior in Small Punch Test by Combined Recrystallization Etch Method and Rigid Plastic Analysis
,”
J. Test. Eval.
,
15
, pp.
30
37
.10.1520/JTE11549J
33.
Edidin
,
A. A.
,
Pruitt
,
L.
,
Jewett
,
C. W.
,
Crane
,
D. J.
,
Roberts
,
D.
, and
Kurtz
,
S. M.
,
1999
, “
Plasticity Induced Damage Layer Is a Precursor to Wear in Radiation Cross Linked UHMWPE Acetabular Components for Total Hip Replacement
,”
J. Arthroplasty
,
14
(
5
), pp.
616
627
.10.1016/S0883-5403(99)90086-4
34.
Husain
,
A.
,
Sehgal
,
D. K.
, and
Pandey
,
R. K.
,
2002
, “
Design of a Simple, Versatile, Small Specimen Punch Test Setup for Determination of the Mechanical Behavior of Materials
,”
Exp. Tech.
,
26
(
5
), pp.
33
38
.10.1111/j.1747-1567.2002.tb00082.x
35.
Kruzic
,
J. J.
,
Kim
,
D. K.
,
Koester
,
K. J.
, and
Ritchie
,
R. O.
,
2009
, “
Indentation Techniques for Evaluating the Fracture Toughness of Biomaterials and Hard Tissues
,”
J. Mech. Behav. Biomed. Mater.
,
2
(
4
), pp.
384
395
.10.1016/j.jmbbm.2008.10.008
36.
Chantikul
,
P.
,
Anstis
,
G. R.
,
Lawn
,
B. R.
, and
Marshall
,
D. B.
,
1981
, “
A Critical Evaluation of Indentation Techniques for Measuring Fracture Toughness—Part II: Strength Method
,”
J. Am. Ceram. Soc.
,
64
(
9
), pp.
539
543
.10.1111/j.1151-2916.1981.tb10321.x
37.
Rasoulian
,
R.
,
Raeisi Najafi
,
A.
,
Chittenden
,
M.
, and
Jasiuk
,
I.
,
2013
, “
Reference Point Indentation Study of Age-Related Changes in Porcine Femoral Cortical Bone
,”
J. Biomech.
,
46
(
10
), pp.
1689
1696
.10.1016/j.jbiomech.2013.04.003
38.
Gallant
,
M. A.
,
Brown
,
D. M.
,
Organ
,
J. M.
,
Allen
,
M. R.
, and
Burr
,
D. R.
,
2013
, “
Reference-Point Indentation Correlates With Bone Toughness Assessed Using Whole-Bone Traditional Mechanical Testing
,”
Bone
,
53
(
1
), pp.
301
305
.10.1016/j.bone.2012.12.015
39.
Libonati
,
F.
, and
Vergani
,
L.
,
2016
, “
Understanding the Structure-Property Relationship in Cortical Bone to Design a Biomimetic Composite
,”
Compos. Struct.
,
139
, pp.
188
198
.10.1016/j.compstruct.2015.12.003
40.
Yang
,
Q. D.
,
Cox
,
B. N.
,
Nalla
,
R. K.
, and
Ritchie
,
R. O.
,
2006
, “
Fracture Length Scales in Human Cortical Bone: The Necessity of Nonlinear Fracture Models
,”
Biomaterials
,
27
(
9
), pp.
2095
2113
.10.1016/j.biomaterials.2005.09.040
41.
Gupta
,
H. S.
,
Krauss
,
S.
,
Kerschnitzki
,
M.
,
Karunaratne
,
A.
,
Dunlop
,
J. W.
,
Barber
,
A. H.
,
Boesecke
,
P.
,
Funari
,
S. S.
, and
Fratzl
,
P.
,
2013
, “
Intrafibrillar Plasticity Through Mineral/Collagen Sliding Is the Dominant Mechanism for the Extreme Toughness of Antler Bone
,”
J. Mech. Behav. Biomed. Mater.
,
28
, pp.
366
382
.10.1016/j.jmbbm.2013.03.020
42.
Peterlik
,
H.
,
Roschger
,
P.
,
Klaushofer
,
K.
, and
Fratzl
,
P.
,
2006
, “
From Brittle to Ductile Fracture of Bone
,”
Nat. Mater.
,
5
(
1
), pp.
52
55
.10.1038/nmat1545
43.
Sharma
,
N. K.
,
Sehgal
,
D. K.
, and
Pandey
,
R. K.
,
2014
, “
Studies on Deformational Behavior of Miniaturized Cortical Bone Specimens Using Finite Element Simulation
,”
AIP Conf. Proc.
,
1618
, pp.
819
822
.10.1063/1.4897858
44.
Sharma
,
N. K.
,
Sharma
,
S.
,
Sehgal
,
D. K.
, and
Pandey
,
R. K.
,
2013
, “
Studies on Deformational Behavior of Cortical Bone Using Small Punch Testing and Finite Element Simulation
,”
World Congress on Engineering and Computer Science
, San Francisco, CA, Oct. 23–25, pp.
920
924
.
45.
Sharma
,
N. K.
,
Sharma
,
S.
,
Sehgal
,
D. K.
, and
Pandey
,
R. K.
,
2014
, “
Detailed Analysis of Deformational Behavior of Plexiform Bone Using Small Specimen Testing and Finite Element Simulation
,”
Transactions on Engineering and Technology
,
Springer
,
Dordrecht, The Netherlands
, pp.
661
673
.
46.
Sharma
,
N. K.
,
Sehgal
,
D. K.
, and
Pandey
,
R. K.
,
2014
, “
Deformational Behavior of Cortical Bone Under Small Punch Testing
,”
International Conference on Material Science and Material Engineering
, Chicago, IL, Mar. 15–16, pp.
354
361
.
47.
ASTM International
,
2001
, “
Standard Test Method for Measurement of Fracture Toughness
,” American Society for Testing Materials, West Conshohocken, PA, Standard No. E1820-99a.
48.
Lucksanasombool
,
P.
,
Higgs
,
W. A. J.
,
Higgs
,
R. J. E. D.
, and
Swain
,
M. V.
,
2001
, “
Fracture Toughness of Bovine Bone: Influence of Orientation and Storage Media
,”
Biomaterials
,
22
(
23
), pp.
3127
3132
.10.1016/S0142-9612(01)00062-X
49.
Behiri
,
J. C.
, and
Bonfield
,
W.
,
1984
, “
Fracture Mechanics of Bone—The Effect of Density, Specimen Thickness and Crack Velocity on Longitudinal Fracture
,”
J. Biomech.
,
17
(
1
), pp.
25
34
.10.1016/0021-9290(84)90076-9
50.
Vashishth
,
D.
,
2004
, “
Rising Crack-Growth-Resistance Behavior in Cortical Bone: Implications for Toughness Measurements
,”
J. Biomech.
,
37
(
6
), pp.
943
946
.10.1016/j.jbiomech.2003.11.003
51.
Nalla
,
R. K.
,
Stolken
,
J. S.
,
Kinney
,
J. H.
, and
Ritchie
,
R. O.
,
2005
, “
Fracture in Human Cortical Bone: Local Fracture Criteria and Toughening Mechanisms
,”
J. Biomech.
,
38
(
7
), pp.
1517
1525
.10.1016/j.jbiomech.2004.07.010
52.
Launey
,
M. E.
,
Buehler
,
M. J.
, and
Ritchie
,
R. O.
,
2010
, “
On the Mechanistic Origins of Toughness in Bone
,”
Annu. Rev. Mater. Res.
,
40
(
1
), pp.
25
53
.10.1146/annurev-matsci-070909-104427
53.
Singh
,
J.
,
Sharma
,
N. K.
, and
Sehgal
,
S. S.
,
2017
, “
Small Punch Testing: An Alternative Technique to Evaluate Tensile Behavior of Cortical Bone
,”
J. Mech. Med. Biol.
,
17
(6), pp.
1
14
.10.1142/S0219519417501020
54.
Sharma
,
N. K.
,
Sharma
,
S.
,
Sehgal
,
D. K.
, and
Pandey
,
R. K.
,
2014
, “
Effect of Bone Composition and Apparent Density on Inhomogeneity in Energy Dissipation During Tension
,”
World Congress on Engineering
, London, July 2–4, pp.
1399
1403
.
55.
Sharma
,
N. K.
,
2014
, “
Studies on Orientation Effect and Locational Variation in Mechanical and Fracture Properties of Cortical Bone
,” Ph.D. dissertation, Department of Applied Mechanics, IIT Delhi, New Delhi, India, pp.
1
270
.
You do not currently have access to this content.