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Calcif Tissue Int (2001) 69:373–378

DOI: 10.1007/s00223-001-1006-1

© 2001 Springer-Verlag New York Inc.

Shear Strength and Fatigue Properties of Human Cortical Bone


Determined from Pure Shear Tests
C. H. Turner,1 T. Wang,1 D. B. Burr2
1
Departments of Orthopaedic Surgery and Mechanical Engineering, Indiana University Purdue University Indianapolis,
Indianapolis, Indiana 46202, USA
2
Department of Anatomy and Cell Biology, Indiana University Purdue University Indianapolis, Indianapolis, Indiana, 46202, USA

Received: 16 January 2001 / Accepted: 11 July 2001 / Online publication: 3 December 2001

Abstract. Shear properties of bone have been inferred from age develops within the bone tissue and with time can ac-
torsion tests. However, torsion often causes spiral fracture cumulate. The combination of the bone weakening effects
planes that correspond to tensile rather than shear failure. of microdamage accumulation and bone resorption that is
We measured the shear properties of human cortical bone in
both longitudinal and transverse directions using pure shear triggered by microdamage can lead to stress fracture [2].
tests. Shearing applied transverse to the bone long axis Microdamage may be caused by either tensile, compressive,
caused fracture along a 45° plane that coincided with maxi- or shear stresses. Since cortical bone is weak in shear [3],
mum tension. This fracture pattern is similar to spiral frac- particularly in the longitudinal plane, shear fatigue of bone
tures caused by torsion. Shear strength along the bone axis may be a key factor in stress fracture pathogenesis. Yet
was 51.6 MPa or about 35% less than that determined using
torsion tests. Fatigue tests of human cortical bone in pure there are no data available to test this possibility since the
shear were conducted. The results agreed well with previous fatigue properties of cortical bone in shear fatigue have not
measurements of cortical bone fatigue life in tension and been measured.
compression, when normalized to strength. Using tibial In previous studies, shear strength has been inferred
shear strain magnitudes measured previously for human from torsion tests applied to specimens of cortical bone. As
volunteers, we estimated the fatigue life of cortical bone for
different activities, and speculate that shear fatigue failure is noted above, torsion often causes tensile failure in bone,
a probable cause of tibial stress fractures resulting from rather than shear. An alternative to the torsion test is pure
impact loading. shear testing following protocols designed for composite
material testing. Additionally, pure shear testing can be used
Key words: Torsion — Human cortical bone — Shear fa- to determine the response of cortical bone to cyclic fatigue
tigue failure
loading in shear, a property of bone that has not been stud-
ied.
We measured shear strength of human cortical bone in
During normal activities, bone tissue is subjected to tensile, the longitudinal and transverse planes using the Iosipescu
compressive, and shear stresses. Usually shear stress mag- [4] and Arcan et al. [5] pure shear testing protocols. In
nitudes are relatively small, but can become substantial in addition, we conducted fatigue tests in pure shear.
long bones subjected to torsion. Severe torsion can result in
long bone fracture. Fracture surfaces produced by torsional
loads are helical [1], creating a spiral fracture. Torsional Methods
loading creates both transverse and longitudinal shear
Bone Specimens
stresses in the bone as well as tensile and compressive
stresses 45° from the shear direction (Fig. 1a). Bone will fail Cortical bone specimens were obtained from the midshafts of hu-
along the plane in which it is weakest. Often this fracture man femora from three males (63, 72, and 74 years old) and two
plane coincides with the maximum tensile stresses, which in females (71 and 83 years old). These bones were stored at −20°C
until the time of testing.
the case of torsional loading, falls along a helical plane 45°
from the long axis (the maximum compressive stress runs
along a perpendicular helical plane, see Fig. 1b), suggesting Pure Shear Tests
that torsion causes bone to fail in tension rather than shear.
Shearing tests were conducted using the Iosipescu [4] and Arcan et
When bone is subjected to cyclical loading, microdam- al. [5] pure shear protocols (Fig. 2). Before the shear testing, we
conducted finite element analyses to confirm that the tests pro-
duced pure shear stress in the test specimens. All the analyses were
done using Sun SPARCstation (Sun Microsystems, Inc.). Patran
Correspondence to: C. H. Turner 2.5 (PDA Engineering) was used to create geometry and mesh and
374 C. H. Turner et al.: Shear Strength of Cortical Bone

Fig. 1. (a) Torsional loading causes shear stress along and trans-
verse to the long axis of the bone (indicated by stripes). Tensile
stress is maximum in a plane +45° from the long axis and maxi-
mum compressive stress occurs at −45°. (b) Torsional loading
applied to a bone causes compressive stress (A) and tensile stress
(B) in perpendicular helical planes 45° from the long axis. This is
analogous to the effect of twisting a cardboard tube. If twisted in
the correct direction, the tube will come apart along the helical
seam, the result of tensile stresses created across the seam.

Abaqus 5.5 (Hibbitt, Karlsson & Sorensen, Inc.) was used to ana-
lyze the models. The Arcan and Iosipescu tests were analyzed Fig. 2. (a) Iosipescu and (b) Arcan test methods for producing
using 8-node quadratic quadrilateral elements with 3574 and 1646 pure shear stresses in composite materials. The shaded region in
degrees of freedom, respectively. Bone was modeled as an isotro- (a) is under pure shear when a force F is applied. Iosipescu speci-
pic material with a Young’s modulus of 20 GPa and a Poisson’s mens are typically four times longer than they are wide with 90°
ratio of 0.3. Shear stress and principle stress angle were calculated notches in the center and a specimen thickness of at least 2.5 mm.
in the critical test region (shaded region in Fig. 2; this region For Arcan test specimens, the width of the test region is denoted h.
comprised 32 elements for the Arcan analysis and 20 elements for It is important that the notches have fillets otherwise stress con-
the Iosipescu analysis). centrations can be created which will cause premature failure of
Shear tests were performed on longitudinal test specimens, in the test specimen. From Turner C H., Burr D B. Bone 14:595–608,
which shearing occurred transverse to the long axis (transverse 1993. Used with permission from Elsevier Science.
shear), or on transverse test specimens where shearing was parallel
to the long axis (longitudinal shear). The Iosipescu test configu- Testing was done at room temperature. Ultimate load was mea-
ration was used for transverse shear tests, but size requirements sured for each specimen.
dictated that the Arcan configuration be used for longitudinal shear For both the Arcan and Iosipescu tests, shear stress in the test
tests because of the degree of radial curvature of the bone. For region was calculated as ␶ ⳱ F/ht. where F is the applied force, h
transverse shear tests, 6–7 cm sections from the femoral mid- is the height of the critical section (Fig. 2), and t is the specimen
diaphysis were cut into four quadrants. A milling machine (EMCO thickness.
Maximat Super 11, EMCO Maier Co, Columbus, OH) was used to
cut a rectangular piece (40 × 10 × 3 mm) from each quadrant, with
its long axis parallel to the femoral long axis. Two V-shaped Fatigue Tests
notches of 90° and 3 mm depth were cut using a milling machine
with a custom-made end mill cutter with a 0.5 mm tip radius (Fig. Five longitudinal shear specimens were made from each femur (for
3). The specimens (n ⳱ 11) were tested at room temperature (22 a total of 25). One specimen from each femur was loaded to
± 2 °C). The test apparatus was custom-made according to the fracture to determine the ultimate longitudinal shear stress. Then
specifications of Iosipescu et al. [4]. Specimens were loaded to the remaining four specimens were tested under cyclic load with
fracture in pure shear at a rate of 1 mm/sec using a servohydraulic peak load levels that created shear stresses that were 60%, 70%,
test system (MTS 810, MTS Systems Co., Eden Prairie, MN). A 80%, and 90% of the ultimate longitudinal shear stress. Tests were
plotter (HP 7090A, Hewlett Packard, Palo Alto) recorded the ul- performed using an apparatus according to the specification de-
timate loads. scribed by Arcan et al. [5] Universal joints were used to prevent
For longitudinal shear tests, a group of three to four specimens bending and torsion on the specimen. A haversine load waveform
were machined from each quadrant of the femoral cortex. These was applied to the specimen using the MTS servohydraulic testing
specimens (n ⳱ 14) came from the same mid-diaphyseal sections machine, with a frequency of 2 Hz. Specimens were kept wet by
as were used for the transverse shear tests. From the diaphyseal dripping 37°C physiological saline over them throughout the tests.
bone, a rectangular piece was machined to 10 mm × 10 mm × 3 Fatigue failure is defined as the complete fracture of the specimen.
mm, 90° notches 2.5 mm in depth were cut using the end mill
cutter described above (Fig. 3), and the test region of the specimen Results
was milled to a 1.5 mm thickness. Each specimen was mounted
into an aluminum grip and loaded as specified by Arcan et al. [5]. Finite element analyses confirmed that both the Arcan and
C. H. Turner et al.: Shear Strength of Cortical Bone 375

Fig. 4. Illustration of the fracture planes for transverse and longi-


tudinal shearing of cortical bone. The striped pattern shows the
direction of the ‘grain’ of the bone along the long axis. Shearing
aligned with the grain (longitudinal shear) caused a fracture plane
along the grain. Shearing across the grain (transverse shear) caused
a fracture plane 45° from the grain. This fracture plane corre-
sponded to the maximum tensile stress. Thus, transverse shearing
causes a tensile fracture rather than a shear fracture.

Fig. 3. Protocol for specimen preparation. A section was cut from


the femoral midshaft and divided into four quadrants. Each quad-
rant was machined into a flat bar approximately 10 mm wide and
3 mm thick. The flat bar was machined into an Iosipescu shear
specimen (shown on the left) for transverse shear tests by cutting
notches in the top of the bottom, or into four Arcan shear speci-
mens (shown on the right) by notching the sides.

Iosipescu devices achieved an excellent pure shear stress


state within the critical section. The principal angle was 45°
± 0.5° for the Arcan device and 45° ± 1.3° for the Iosipescu
device, demonstrating excellent agreement with theory (a
principal angle of 45° was expected). The equation ␶ ⳱ F/ht
underestimated the average nodal shear stress within the
critical section by < 4%. Shear stress was virtually uniform
across the 4 mm critical section for both the Iosipescu and Fig. 5. S-N curve for fatigue of cortical bone in shear. Regression
Arcan specimens. of the data on a log-log scale yielded a good fit (r2 ⳱ 0.89, P <
The shear strength under longitudinal shear was 51.6 ± 0.00001).
1.9 MPa, which was significantly less than shear strength
under transverse shear, 65.3 ± 2.5 MPa (p < 0.001). For
transverse shearing, the fracture plane was always 45° from ␥failure = 8900N−0.06 (2)
the direction of loading, whereas longitudinal shear always
produced a fracture along the shear plane (Fig. 4). The where ␶failure is the longitudinal shear stress (in MPa), ␥failure
fracture plane caused by transverse shearing always coin- is the longitudinal shear strain (in microstrain), and N is the
cided with the maximum tensile stress, hence transverse number of loading cycles until failure. Peak shear strain was
shearing caused failure due to tension not shear. calculated as peak stress divided by the shear modulus of
Of the 20 specimens prepared for fatigue testing, 16 the femur in the longitudinal-circumferential plane (6.23
were tested successfully. Four specimens were not used due GPa [6]).
to either mistakes in specimen preparation or premature
shutdown of the testing machine during the fatigue test. Discussion
Results from shear fatigue tests are summarized as peak
stress vs cycles (S-N curve, Fig. 5) or peak strain vs cycles. We report the shear strength of human cortical bone in its
The data closely fit the equation: weakest plane (longitudinal) and the shear fatigue properties
of femoral bone. The longitudinal shear strength measured
␶failure = 55N−0.06 (1) in our study (51.6 MPa) was similar to that measured pre-
viously (50.4 MPa) for embalmed human femurs [7]. Table
or 1 shows the tensile, compressive, and shear strengths for
376 C. H. Turner et al.: Shear Strength of Cortical Bone

Table 1. Tensile, compressive, and shear strengths of human


femoral midshaft
Longitudinal Transverse
Tensile strength [8] 133.0 MPa 51.0 MPa
Compressive strength [8] 193.0 MPa 133.0 MPa
Shear strength (torsion) [8] 68.0 MPa
Shear strength [7] 50.4 MPa
Shear strength (current study) 51.6 MPa 65.3 MPaa
a
Transverse shear specimens failed in tesion rather than shear

human femoral bone as reported by Saha [7] and Reilly and


Burstein [8], compared to the shear strengths reported here.
The data compiled in Table 1 illustrate two things: (1) cor-
tical bone is weak in both tension and shear, and (2) the Fig. 6. S-N curve comparing fatigue of cortical bone in shear
longitudinal shear strength of cortical bone is substantially (closed circles) with fatigue measured in tension, compression,
reversed loading, or bending. Open circles [14]; open squares [11];
lower than shear strength determined using torsion tests. open triangles [15]; open upside down triangles [12]; closed tri-
Cortical bone shear strength has been reported to be be- angles [17] (tension); closed upside down triangles [17] (compres-
tween 68 and 70 MPa based upon data from torsion tests [8, sion); closed squares (large) [13]; closed squares (small) [16].
9]. These values are about 35% higher than the longitudinal
shear strength reported here (but similar to transverse shear
strength). [11, 12, 14, 15] (open symbols in Fig. 6) than under tensile
The transverse shear test created a failure plane 45° from [16] compressive [13, 17], or uniaxial tensile-compressive
the long axis, coincidental with the plane of maximum ten- loading [16] (closed symbols). This comparison may be
sion. This fracture pattern is analogous to the spiral fracture misleading, however, since bending and flexural tests were
resulting from torsion. The similarity of these results dem- conducted at high frequencies (30–125 Hz) and uniaxial
onstrates that the transverse pure shear test provides results tests were conducted at lower frequencies (0.5–2 Hz). Caler
similar to the more widely accepted torsion test. As illus- and Carter [18] have shown that there is a time-dependent
trated in Figure 1a, transverse shear loads cause shear component for damage accumulation in cortical bone,
stresses in both the transverse and longitudinal directions. hence, fatigue testing of bone at higher frequencies could
Since longitudinal shear strength was substantially less than inadvertently extend the fatigue life, in terms of cycles to
transverse shear strength, it is difficult to understand why failure. Also, testing temperature has significant effects on
the transverse shear specimens did not fail in the longitu- fatigue life of bone. Carter and Hayes [14] found that a
dinal direction, i.e., along the grain of the bone. Had the decrease from 45°C to 21°C tripled fatigue life of cortical
specimens failed in longitudinal shear, they would have bone. This is significant since most of the previous studies
split down the long axis instead of failing at a 45° angle. that used bending or flexural tests were conducted at room
Clearly the bone tissue could have failed along either of its temperature (20–22 °C) rather than body temperature (37
weakest planes—longitudinal shear or tension—but failure °C) [11, 12, 15]. The fatigue life for a given shear stress
occurred in tension. Perhaps the constraints placed upon the magnitude was considerably less than fatigue life at similar
specimen by the Iosipescu test apparatus did not allow fail- stress magnitudes, determined using uniaxial tension, com-
ure in longitudinal shear. Nevertheless, there are clinical pression, or bending loading. However, as noted in Table 1,
examples of longitudinal shear fractures. The most common cortical bone is much weaker in longitudinal shear than in
is the ‘boot top’ fracture resulting from a skiing accident. tension or compression. Consequently, we chose to further
This fracture typically results from the combination of tor- compare the S-N curves after normalizing peak stress by
sion and three-point bending at the boot top. Both torsion cortical bone strength in shear, tension, and compression.
and bending cause transverse shear loading to the tibia, We used the tensile and compressive fatigue data from Pat-
resulting in longitudinal shear stress. The fracture often in- tin et al. [17] to compare with shear fatigue data, since
cludes a spiral fracture plane combined with longitudinal Pattin et al. used similar testing conditions (bone type, test
fracture planes [10]. type, frequency), as in the current study. After normaliza-
The fatigue properties of cortical bone in shear deter- tion, there were no significant differences between the shear
mined in this study were compared with previous studies S-N curve and the tensile or compressive S-N curves (Fig.
from the literature (Fig. 6). Table 2 lists the previous studies 7), suggesting that fatigue of cortical bone occurs at similar
used for this comparison. (This list includes only studies rates in tension, compression, and shear.
that reported an S-N curve, allowing comparison with the The study results demonstrate that cortical bone is very
data in Fig. 5). Cortical bone exhibited better fatigue prop- weak in shear and is subject to fatigue failure when repet-
erties under rotating bending or reversed flexural loading itively loaded in shear. These findings may help explain the
C. H. Turner et al.: Shear Strength of Cortical Bone 377

Table 2. Previous fatigue studies used for comparison with shear fatigue data
Reference Bone type Test type Temperature Frequency (Hz)
King and Evans [11] Embalmed human Reversed flexural Room temperature 30
Swanson et al. [12] Human Rotating bending Room temperature 70
Gray and Korbacher [13] Bovine Uniaxial compression Room temperature 30
Carter et al. [14] Bovine Rotating bending 37°C 125
Lafferty and Raju [15] Bovine Rotating bending 21°C 30
Carter et al. [16] Human Uniaxial reversed 37°C 0.5–1.0
Pattin et al. [17] Human Uniaxial compression 37°C 2
Pattin et al. [17] Human Uniaxial tension 37°C 2
Current study Human Pure shear 37°Ca 2
a
37°C saline was dripped on the specimens during the test

true when it comes to stress fracture of the human tibia;


tibial strains have been measured in several human volun-
teers during a variety of activities [22–24]. Activities that
cause impact loading (e.g., running) cause higher tibial
strains than activities involving smooth movements (e.g.,
cycling). In activities that do not involve impact loading, the
predicted fatigue failure of the cortical bone exceeds the
human lifetime (108 cycles or about 100 years) (Table 3).
However, for impact activities like running, the predicted
fatigue life in shear can be as much as 3 orders of magnitude
shorter than in compression.
The current study was limited to bone specimens from
only a few elderly individuals. It is possible that bone
samples from younger individuals would have a longer fa-
Fig. 7. S-N curves comparing fatigue properties after peak stress tigue life under similar loading conditions. The results are
were normalized by the ultimate strength (defined as the peak
stress value at one cycle to failure extrapolated from the S-N also limited to bone specimens from the femoral midshaft.
curve). Shear fatigue data taken from the current study were nor- We chose this anatomical site because it was the site for
malized by longitudinal shear strength (52 MPa). Tensile fatigue samples in most previous studies, thus allowing valid com-
data from Pattin et al. [17] were normalized by longitudinal tensile
strength (111 MPa). Compressive fatigue data from Pattin et al. parison of results. Of course cortical bone mechanical prop-
was normalized by longitudinal compressive strength (182 MPa). erties vary with anatomical site. Evans and Lebow [24]
Analysis of covariance (with load type as a main effect and (log) found that the fatigue life of human tibial bone specimens
cycles to failure as a covariate) showed that there were not sig-
nificant differences between the normalized shear fatigue S-N was greatest at the midshaft, but 37% less in the distal third
curve (circles) and the normalized tensile S-N curve (triangles of the cortex and 67% less in the proximal third. The varia-
[17]), or the normalized compressive S-N curve (upside down tion in fatigue life may be due to site-specific differences in
triangles [17]) (P > 0.9).
bone microstructure. The density and Young’s modulus of
femoral and tibial cortical bone are both less in distal and
proximal locations compared with the midshaft [25]. Carter
high incidence of stress fractures during certain strenuous et al. [16] showed that fatigue life decreases with decreasing
exercises. Cortical bone strain has been measured in vivo in Young’s modulus and/or increasing porosity. Hence, the
a number of animal species and humans during various shear fatigue properties presented here are valid only for the
exercises. Bone strains for dogs and horses while they run human femoral midshaft and might vary with proximodistal
show that the tibiae and radii are loaded primarily in bend- location along the femur, or in other anatomical sites.
ing, such that shear strains are fairly low [19]. These results In conclusion, we found that the longitudinal shear
imply that stress fractures are mainly the result of large strength measured using pure shear testing was about 35%
tensile and compressive strains/stresses, rather than shear- less than that previously determined using torsion tests.
ing. Fatigue failure of the third metacarpal bone in thor- Thus, human cortical bone is considerably weaker in lon-
oughbred racehorses is associated with peak compressive gitudinal shear compared with transverse shear. This study
strain magnitude in the bone during training [20]. Yet others is the first investigation of the fatigue behavior of human
have argued that fatigue fracture may be the result of shear cortical bone under pure shear loading. Based upon in vivo
strains, even if they are considerably less than tensile or bone strain measurements from human volunteers, we be-
compressive strains, due to the weakness of cortical bone in lieve that shear stresses may play an important role in the
shear [21]. There is growing evidence that the latter may be pathogenesis of stress fractures in the tibia.
378 C. H. Turner et al.: Shear Strength of Cortical Bone

Table 3. Measured tibial strains in human volunteers participating in different activities [22,
23]
Activity Peak strain Predicted time to failure
Comp. Tensile Shear Comp. Tensile Shear
8 8
Cycling [23] 291 271 628 >10 >10 >108
Walking [22] 544 437 871 >108 >108 >108
Jogging [22] 879 625 1444 >108 >108 >108
Running Sprint [22] 968 646 1583 >108 >108 >108
Zigzag running Uphill [23] 1226 743 1966 5.9 × 107 >108 >108
Running 17 km/h [23] 1675 1378 5027 5.4 × 106 >108 9.0 × 103
a
The number of loading cycles until failure were estimated based upon the current results
(shear) or the results from Pattin et al. [17] for tension or compression. Strains are in units of
microstrain The stress fatigue data from Pattin et al. [17] were converted to strains by dividing
by the Young’s modulus of human femoral bone (20 GPa [6])

Acknowledgments. This work was supported by USPHS Research (ed) Digest of the Seventh International Conference on Medi-
Grants P01-AG05793 and R01-AR43730 from the National Insti- cal and Biological Engineering. , Stockholm, pp 514
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