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Table 1. Information regarding the male donors (age, height, weight, cause of death) and their femoral bones
Age (yr)
35
42
46
48
50
52
56
60
70
92
Cause of death
Height
(m)
Weight
(kg)
Anatomical
height
Outer
diameter
(mm)
Inner
diameter
(mm)
Cortical
thickness
(mm)
Drowning
Road traffic accident
Coronary
Cerebral hemorrhage
Acute pericarditis
Coronary
Coronary
Coronary
Respiratory failure
Toxemia
1.68
1.67
1.62
1.60
1.78
1.71
1.64
1.64
1.66
1.64
63.5
65.5
69.5
57.0
86.0
76.5
78.0
79.5
43.3
44.0
md
m
pm
pm
md
m
md
md
m
md
28.8
29.9
26.8
32.0
30.5
27.8
29.4
27.8
27.1
30.3
14.9
14.9
14.8
16.7
16.7
14.7
12.7
12.5
15.5
17.2
6.9
7.0
5.9
7.6
6.8
6.5
8.3
7.6
5.8
6.5
Anatomical height: m 5 medial, pm and md 5 cut towards the proximal or distal end, respectively. The inner and outer diameters of the cylinders and
the maximum apparent cortical thickness were measured along the anterio-posterior and medio-lateral planes and then averaged.
Figure 1. Specimens were cut from the anterior, lateral, and posterior
sectors of the femora. The plate-like specimen for 3-point bending (E, sf)
was always in the middle of each sector and the Wf and KCJ specimens
were cut right and left on either side of it. Fracture in all three cases
proceeded in a direction across the structural elements driven either by
the direction of bending (E, sf), the chevron notch (Wf), or the sharp
notch (KCJ).
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60
Figure 4. Plots for (E, sf, KC, Wf, J) vs. age. A, L, P indicate the anterior,
lateral, and posterior sectors, respectively. The filled symbols are the
average of the previous three values at a certain age. The solid lines are
least squares linear regressions and their 95% confidence intervals. (b)
Dotted line indicates the results compiled by Yamada30 on relatively wet
human femoral bone at room temperature. In (c), the dotted data and lines
are mixed male/female results obtained by Bonfield and Behiri3 at room
temperature on relatively wet human tibial CT specimens along the
longitudinal direction. In (e), the dotted line shows results for a mode-I
critical strain energy release rate obtained for tibia, mixed male/female, by
Norman et al.20 on CT specimens in the longitudinal direction at room
temperature.
(1)
(2)
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Table 2. Relationships between material properties and age ($ 35 years old) observed in the present tests; linear and loglog relationships
E (GPa)
sf (MPa)
KC (MPa m1/2)
Wf (kJ m22)
J-integral (kJ m22)
Log E
Log sf
Log KC
Log Wf
Log J-integral
516.36 (0.75)a
21.81/0.000b
5191.1 (10.72)
17.82/0.000
57.33 (0.345)
21.23/0.000
54.42 (0.526)
8.40/0.000
51.34 (0.090)
14.90/0.000
51.41 (0.094)
15.0/0.000
52.62 (0.116)
22.52/0.000
51.25 (0.087)
14.42/0.000
51.61 (0.332)
4.85/0.000
50.38 (0.144)
2.63/0.028
20.0354 (0.013)
22.70/0.027
20.625 (0.188)
23.33/0.010
20.0264 (0.006)
24.37/0.002
20.0295 (0.009)
23.21/0.012
20.0036 (0.0016)
22.31/0.049
20.147 (0.054)
22.71/0.027
20.248 (0.067)
23.69/0.006
20.280 (0.050)
25.59/0.000
20.682 (0.192)
23.55/0.008
20.187 (0.083)
22.25/0.054
age (yr)
R2 5 48%
age (yr)
R2 5 58%
age (yr)
R2 5 71%
age (yr)
R2 5 57%
age (yr)
R2 5 40%
R2 5 48%
R2 5 63%
R2 5 80%
R2 5 61%
R2 5 39%
SD in parentheses.
t and p values are given underneath each coefficient, probabilities of 0.000 indicate p , 0.001.
(3)
also did not hold true. Our specimens had thicknesses in the
2.9 4.9 mm range. Formula (1) produces a minimum thickness
requirement of 7.7 8.5 mm, a restriction that can not be satisfied
given the cortical thickness in human bone (Table 1). Our
mechanical observations were indicative of significant plastic
deformations being present and these were a result of the preinitiation microcracking seen in the vicinity of the notch. The
measurements for KC fracture toughness can, therefore, only be
estimates and not KIC ASTM standard values.
The J-integral was calculated by a graphical method.10 It
estimates fracture toughness through measuring the energy
needed to propagate a crack and its critical value is at the point
where the crack first started growing. The method applies
equally well from the elastic to fully plastic behavior. Each
load/displacement curve is integrated to produce the energy
(work) input in the system up to a certain displacement value.
Each work value is scaled (up or down by using each specimens thickness) to a common value of thickness for all
specimens. For each displacement a plot is made of the scaled
work values vs. each specimens crack length (manmade
notch). The negative slope of this relationship (2]U/]a) when
normalized for the average thickness value is the value of the
J-integral function. The critical value of J is subsequently
determined for the critical displacement value at which the
(manmade-) notch started growing during each test.
Our method followed 4 steps: (i) the work under the load/
displacement curve was determined at a set of seven preselected
displacements (di, i 5 17, Figure 2) for all 30 specimens. (The
displacements were chosen so as to encompass both the linear
behavior and the region of the critical load point for all specimens.) Each of the energy values was scaled to the average
thickness value of 3.66 mm. (ii) For each displacement (i.e., d1),
the scaled energy values (U1,j, j 5 130) were plotted (7
graphs in total) vs. the initial notch length of each specimen.
Because of the separate age effect, the required slope (]U1/]a,
for i 5 1) was derived from a regression of the energy values
(U1,j) vs. both age and notch length. In this way the age effect
Table 3. Correlation coefficients between the mechanical variables
and age
N 5 10
E
sf
KC
Wf
J
N 5 30
E
sf
KC
Wf
J
Age (yr)
sf
KC
Wf
20.690a
20.763a
20.839a
20.750a
20.633a
0.842a
0.676a
0.572
0.378
0.775a
0.761a
0.218
0.709a
0.605
0.572
20.471a
20.602a
20.640a
20.573a
20.406a
0.828a
0.449a
0.458a
0.151
0.533a
0.544a
0.153
0.505a
0.554a
0.252
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was factored out at this stage of the method. (iii) The slopes
produced (]Ui/]a, i 5 17) were plotted vs. the preselected
displacement values (di) to produce a J-calibration curve
(Figure 3). (iv) From this calibration curve the critical value
for the J-integral for each specimen is derived at the point of
critical displacement (dC in Figures 2 and 3), where the notch
started propagating.
To reiterate, the various tests have the following characteristics: E measures material stiffness; sf measures flexural strength
and overestimates it to a greater extent the more postyield
deformation the specimen shows, whereas the actual damage is
confined to a mm-wide area; KC is an expression of the intensity
of the stress field necessary to start a crack growing, and assumes
that nonlinear effects are minimal and confined to an area very
63
Figure 5. Photos of LSCM in front of the crack tip: (a) brittle; (b) deflected; and (c) zigzag behavior. The notch site is noted as N; thin arrows
show the path of the major crack. Note that the crack has circumvented the large osteons (r); the diffuse interlamellar damage in some cases (i); and
the fanning out of microdamage (f) in a direction opposite to the notch (which did not, however, cause a secondary macrocrack).
64
Anterior
Lateral
Posterior
35
42
46
48
50
52
56
60
70
92
(db-db)
(db-b)
d-zd
(b-b)
(dz-bdz)
d-dz
d-z
(bz-z)
d-d
(dz-bdz)
(db-b)
(b-z)
(bd-z)
(b-d)
(bz-z)
zd-zd
d-z
(bz-zb)
(bd-d)
(d-bd)
(b-b)
d-d a
d-zd
(d-bd)
d-d
d-d
(d-bd)
(dz-db)
d-dz
dz-dz
ous fracture toughness tests focused almost exclusively on longitudinal cracks), the bones were screened for diseases and
deteriorative effects and, most importantly, all the mechanical
measures came from one set of bones only. Therefore, we know
now not only what the effect of age is on the mechanical
measures, but also, for instance, that a 2.3% reduction in stiffness
is accompanied by a 3.7% reduction in flexural strength, a 4.1%
reduction in fracture toughness KC, and so on. Such relationships
cannot be inferred from the tests reported in previous papers.
Ordinary strength tests may, particularly if the material is
brittle, give values that are misleading, because in materials with
a hierarchical architecture (such as bone), there is a size effect:
smaller specimens may have calculated strengths that are greater
than those of large specimens. Fracture mechanics tests, on the
other hand, attempt to measure material properties on carefully
prepared specimens by either confining damage to a small,
predictable part of the specimen (unlike the situation in real life,
where damage may occur almost randomly throughout the specimen), or by having a shape and size of a notch such that the
stress field around it is mathematically tractable. In this respect,
the present study also brings together measurements of strength
and toughness of the material. In homogeneous metallic materials, the two measures have an inverse relationship,4 whereas
fiber reinforced composites show a positive relationship.11 In the
first case, KC offers information, additional to that provided by
strength, about the conditions that lead to the production of a
macrocrack. However, KC is not useful for predictions of
strength and, in fact, events that initiate a macrocrack are irrelevant to the final fracture or coherence of the structure. In the
second case, the load that creates the first macrocrack is also the
maximum, because afterwards the material simply disintegrates
more or less easily. KC (a variable derived by elastic field theory
equations) is useful, but it is well correlated with the more easily
acquired material strength. KC can therefore be used for strength
predictions, but one should question whether it is conceptually
correct to use it.
Our data and observations of the course of a major crack
partially clarify the fracture process in human bone. All the
3-point bending tests showed that human bone has some postfailure load integrity (failure is at the point where a major
macrocrack is initiated and the material strength is defined) and
therefore cannot be characterized as a brittle material. Fracture
mechanics was originally introduced into bone studies to explain
the differences in stiffness, strength, and toughness observed in
wet and dry bone, and similar though less marked differences in
the properties of fresh and embalmed bone.19 However, in these
cases there is a quantum transformation of the condition of at
least one component of bone (collagen), which can directly affect
its role in bone toughness. Dehydration of bone causes a transition from quasibrittle (wet bone) to a brittle material (dry
bone). Embalming also has a hardening effect that affects the
strength and toughness of the material differently. By contrast,
aging constitutes a simple deteriorative, gradual process, which
only affects the quality of bone material.
All types of bone experience the generation of microcracks
(damage) prior to failure. Microcracks start at yield32 and,
depending on the size, amount, and interaction of such microcracking, bone can be tough to a greater or lesser degree by being
able to prolong its postyield deformation. It is reasonable, therefore, to expect that the decrease in toughness of human bone with
age is related to the kind and amount of microcracking (prefailure damage). However, the clear relationship between toughness
and extent of postyield deformation in normal bone does not
necessarily mean that this is the only possible explanation. The
brittleness of biological materials is a factor of many quantities.
It depends on the amount of prefailure damage,32 on the magni-
65
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