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Determination of Mechanical Properties of the

Bones of the Skull

Paper is concerned with experimental procedures and


results obtained in tension, compression and shear tests
carried out on human skull bone

by D. H.. Robbins and J. L. Wood

ABSTRACT---This paper presents the initial results of a T h e p u b l i s h e d l i t e r a t u r e does not offer a com-
research project concerning the mechanism of head in- plete set of answers to these questions. T h e re-
jury. In order to begin to define the mechanism, it is
necessary to determine mechanical properties of the view sources 1-4 which are concerned in t o t a l or
various skull bones, organize them into constitutive equa- in p a r t with t h e m e c h a n i c a l p r o p e r t i e s of h a r d
tions, and develop a structural model of the skull. tissues refer o n l y once to t e s t s which h a v e been
The material presented is concerned primarily with the carried out on t h e bones of t h e h u m a n skull.
development of experimental procedures and the results
which have been obtained. The specimen-testing pro- E v a n s and L i s s n e P h a v e r e p o r t e d on t h e tensile a n d
gram has been split into four parts: (1) The procural of compressive s t r e n g t h s of e m b a l m e d h u m a n p a r i e t a l
3/4-in. and ll/2-in.-diam plugs from human skulls at bone. D e m p s t e r 6 has asserted on t h e basis of
autopsy and the precise determination of specimen loca- split-line analysis t h a t a large p o r t i o n of the skull
tion and orientation; (2) the fabrication and strain possesses a r a n d o m grain s t r u c t u r e .
gaging of small test specimens for basic tension, com-
pression, tension-compression, and shear tests; (3) the On t h e o t h e r h a n d e x p e r i m e n t a l studies of t h e
conducting of tests; and (4) the correlation of experi- m e c h a n i c a l p r o p e r t i e s of other skeletal c o m p o n e n t s
mental findings with microscopic structure by standard h a v e a long h i s t o r y d a t i n g b a c k to the early studies
and nonstandard techniques of histology. of W e r t h e i m 7 a n d R a u b e r 8 who used whole bones
a n d pieces of bone, respectively. M o s t tests h a v e
Introduction been carried o u t s t a t i c a l l y with t h e exception of t h e
A c u r r e n t research p r o j e c t at t h e H i g h w a y S a f e t y compression t e s t s of B i r d 9 a n d M c E l h a n e y l~ where
R e s e a r c h I n s t i t u t e is concerned w i t h t h e d e t e r m i n a - the effect of loading r a t e was studied. Techniques
t i o n of m a t e r i a l p r o p e r t i e s of t h e bones of t h e skull. of histology h a v e been used to s t u d y t h e micro-
T h i s is p a r t of an effort with t h e end o b j e c t i v e of s t r u c t u r e of bone in r e l a t i o n to the physical proper-
f a b r i c a t i n g p h y s i c a l a n d a n a l y t i c a l models which ties b y v a r i o u s investigators, some of whom are
can be used to s i m u l a t e h e a d - i n j u r y mechanisms. Dempster,11. 12 who p e r f o r m e d tests parallel a n d
S e v e r a l questions m u s t be considered in develop- p e r p e n d i c u l a r to t h e o r i e n t a t i o n of t h e grain struc-
ing a p r o g r a m for t e s t i n g m a t e r i a l of this t y p e . ture, Bird, ~ a n d Ascenzi 13 who has s t u d i e d t h e
W h a t sources are a v a i l a b l e for o b t a i n i n g m a t e r i a l ? p r o p e r t i e s of single osteons r e m o v e d from bone.
H o w is a m a t e r i a l s t o r e d which suffers p h y s i c a l a n d T h e only k n o w n a t t e m p t s to define a s t r e s s - s t r a i n
chemical changes w i t h time? H o w are conven- law other t h a n H o o k e s ' L a w h a v e been m a d e b y
t i o n a l or n o n c o n v e n t i o n a l m a t e r i a l t e s t p r o c e d u r e s M c E l h a n e y 14 who proposes linear and l o g a r i t h m i c
a d a p t e d for this m a t e r i a l ? D o t h e bones of t h e v a r i a t i o n s of stress with increasing s t r a i n r a t e a n d
skull b e h a v e as an isotropic, linear, elastic m a t e r i a l Sedlin ~5 who proposes a K e l v i n m a t e r i a l in series
and, if not, w h a t p r o p e r t i e s m u s t be a d d e d to t h e w i t h an elastic spring.
list for consideration?
Material Acquisition, Storage and Processing
D. H. Robbins is Research Engineer and J. L. Wood is Graduate Research
Assistant, Highway Safety Research Institute, University of M ichigan, A n n Before a n y extensive e x p e r i m e n t a l p r o g r a m could
Arbor, Mich.
be s t a r t e d , it was necessary to define sources for
Paper was presented at 1968 S E S A Spring Meeting held in Albany, N. Y.,
on M a y 7-10. skull m a t e r i a l . I t was found t h a t h u m a n m a t e r i a l

236 I May 1969


Fig. 1--Tension specimen

was available a t hospitals close to the Biomechanics on the bones of the skull and the c o m p o n e n t inner
Laboratories. Specimens have been removed at and outer tables as well as the spongy diplSe layer.
100 autopsies with a 3/4-in. or a l l/4-in.-diam The second objective was development of a speci-
Stryker bone plug cutter m o u n t e d in a Stryker men and gripping system which would allow com-
a u t o p s y saw. As m a n y as four plugs have been pressive as well as tensile forces to be applied to the
taken from a single skull using the smaller cutter. specimen for the purpose of finding a n y transition
T h e holes in the frontal bone are filled with dental modulus as a loading passes from tension to com-
acrylic. E m b a l m e d skullcaps were available from pression. An experimental design of this t y p e
the D e p a r t m e n t of A n a t o m y at the University. allows cyclic testing and the m e a s u r e m e n t of
These offer a source which is useful in determining hysteresis or energy absorbed b y the bone as the
regional differences in skull physical properties. loads are applied and released. T h e third objective
When material is obtained, a complete specimen of the program was the determination of the relation
record is made. The location of a specimen of bone of the physical properties to the skull a n a t o m y and,
is specified by measuring the distances of the speci- further, the relationship of the measured proper-
men from standard anatomical features such as ties to the skull microscopic-structure properties
suture lines. Orientation of a specimen in the t h r o u g h a series of histological studies.
skull, posterior-anterior and right-left, is indicated The specimen and gripping system are shown in
b y making a cross directly on the skull before the Fig. 1. The specimen is roughly 1/2-in. long and
specimen is removed. I n addition, a circular the cross-sectional area of the test sections about
paper spot representing each bone plug is placed on 2 • 10 -3 in. 2 Small blocks are cut from the
a reference skull kept in the laboratory to serve as a a u t o p s y bone plugs, these blanks milled true and,
tally and also to indicate locations for future speci- finally, a finished specimen produced b y mounting
mens. the blank in a template and using the U n i m a t lathe-
Bone specimens are stored in g]ass vials in a mill as a routing table. H e a t production is low.
freezer at - 1 0 ~ C to prevent moisture loss. I t is T h e solution to the problem of gripping a specimen
felt t h a t enough evidence has become available in for tension, compression, cyclic and d y n a m i c load-
research at The University of Michigan and else- ings which was adopted involved applying a positive
where to validate this technique for storage. pressure to the specimen tabs as well as pinning the
tab ends to prevent the specimen from slipping,
Tension-Compression Tests bending or breaking in the grips.
There were multiple objectives in the develop- I n order to measure strain, it was decided t h a t
ment of this series of experiments. T h e first was strain gages offered the greatest potential, although
the design of a tension test which could be con- it was found t h a t the mounting of gages on these
ducted statically or dynamically. T h e results were small specimens was difficult. E p o x y - b a c k e d foil
to be static and dynamic elastic moduli or func- gages with grid sizes ranging from 0.015 to 0.04 in.
tional stress-strain relationships and failure stresses. have been used. After the gage is aligned and
I t was necessary t h a t this test could be carried out cemented to the bone with E a s t m a n 910 adhesive,

Experimental Mechanics I 237


DIRECTION OF
LOAD APPLICATION
I0,000

5~000
Cycle
Loading
/ ~ LOADING HEADS
OF TESTING
MACHINE

RECTANGULAR
Bending Failure TEST BLOCK
Check

P
5
I
10
I
15 20 25
I
STRAIN
i (Thousands of microinches/inch)

Fig. 3~Compression-test setup


Fig. 2--Stress vs. strain for tension-compression test

the tabs are tinned and the lead wire is attached.


Overheating results in crazing of the cement under 125

the gage, in damage to the bone, and in a failure of


the gage to adhere. Microscopic examination of
strain-gaged specimens reveals t h a t there is no pro-
fusion of the bone with cement.
T h e testing machines being used are a 10,000-1b-
capacity I n s t r o n floor-model testing machine with
reversible-loading design and a PlasTech testing
machine capable of inducing a strain rate of a b o u t
0.01 /
5000/sec for specimens of this size. For the s~atic DEFORMATION (inches)
tests, load vs. strain curves are obtained by running
the load and strain signals t h r o u g h Honeywell
bridge - excitation - balance units into an X-Y re-
125
corder. For the limited number of dynamic tests
which have been carried out, load, deformation
rate and strain are recorded on a storage oscillo-
scope and photographed.
A drawing of a typical plot of a test is shown in
Fig. 2. A series of three tests is actually performed
on each specimen. A bending test which is carried
out first shows whether the specimen is properly 0.01
lined up in the gripping system. I f alignment is DEFORMATION (inches)
perfect, no strain appears.
T h e next series of tests involves performing a
series of cycles from tension to compression for the
purpose of finding energy-absorption properties of
125
bone, tension elastic modulus, compression modulus,
and the modulus which exists as loading proceeds
from tension to compression and back. I t has
been found t h a t the hysteresis properties of bone
seem to be large, i.e., a relatively large a m o u n t of
energy is absorbed during cyclic loading from ten-
sion to compression.
Finally, the specimens are loaded in tension to
I
0.01
failure. The curves seem nearly linear for a b o u t
DEFORMATION(inches)
two-thirds of the load range indicating t h a t a Fig. 4--Load vs. deformation for compression test

238 I May 1969


Young's modulus defining a linear material is a widths were 0.20 in. or smaller and height varied
good approximation in the case of skull bone. from 0.16 to 0.23 in.
Also, it has been noted t h a t bone is a brittle ma- , The testing of the specimens was done on a
terial as there is little yielding or permanent de- 10,000-1b capacity I n s t r o n floor-model testing ma-
formation induced before failure. A final property, chine. T h e specimens were placed between a
which is observed when the specimen does not compression load cell and the traveling crosshead
fracture t h r o u g h a strain gage destroying the elec- and the rate of loading adjusted to the desired level.
trical circuit, is the recovery which takes place in L o a d was recorded on a strip chart.
the material when the load is released. The The most typical curves obtained are shown in
a m o u n t of strain induced is large, indicating the Fig. 4. The first curve was the most frequent.
viscoelastic behavior of bone. Observations have After the specimen was judged to have failed, the
shown t h a t the bone assumes its initial strain level test was stopped. There were several criteria for
in about 15 min after the test has concluded. failure. Whenever the curve looked like the por-
The average Y o u n g ' s modulus of 2.11 • 106 psi tion ABC in Fig. 4, it was inevitable t h a t the speci-
and failure stress of 9500 psi are based on about 50 men had failed cataclysmically. All the failures
tests and are in line with other published figures for were in the diplSe. When no cataclysmic failure
static tests on other types of bone. The fact t h a t was observed, then either the failure was indicated
the tension-compression loop closes upon itself and b y a sharp rise in the loading curve or b y a constant
t h a t it is linear for a large portion of both the ten- horizontal loading curve as shown in the last two
sion and compression sections indicates t h a t tension drawings in Fig. 4.
and compression moduli are the same and t h a t A structural modulus was obtained b y comparing
there is a smooth transition when loading passes axial deformation with load. The mean value was
from tension to compression. 2.02 • 105 psi with high and low values being 5.3
Variations in breaking stress seem to be related • 105 psi and 0.104 X 105 psi. A range of values
to the homogeneity of the bone. Low breaking this large contrasts greatly with the moduli ob-
stresses occur when there is some spongy bone, tained in the tension-compression tests where the
blood vessels, etc., present to initiate early failure. bone was compact. Failure stresses are also m u c h
These same features probably have something to do lower indicating the collapse of the weblike struc-
with the variation in values obtained for the tension tural network of the dipl5e layer. T h e mean value
modulus. T h u s far, no differences in physical is 5300 psi with high and low values of 15,700 psi
properties have been identified which correlate well and 768 psi.
with the observed osteon directional patterns or
with specimen location and orientation in the skull. Shear Tests
This is not surprising due to the more r a n d o m pat-
T h e purpose of the shear test is to measure the
tern of microstructure found in m a n y parts of the
shear strength of the diplSe in h u m a n skull bone
skull.
when it is subjected to a simple shear force. F,m-
A few dynamic stress-strain tests have been
balmed h u m a n skullcaps are being used for this
carried out. Preliminary results indicate t h a t
test because of ready availability and the desire to
there is a small increase in elastic modulus with no
determine any regional variation of properties with
increase in breaking stress which is c o m m o n for
specimen location in the skull.
brittle materials.

Structural Compression Tests


The objective of this test series was the de-
termination of the crush failure characteristics of
the diplSe layer of the skull and the measurement of
an average structural compression modulus of
elasticity for rectangular blocks of skull bone. The
compressive load was applied to the block in a
direction perpendicular to the surface of the skull.
A schematic of the test setup is shown in Fig. 3.
A series of seventy tests has been carried out to
date on bone removed at autopsy and frozen until
the test date.
The test specimens were made from bone plugs
removed at a u t o p s y b y first machining the circular
disks flat on a milling machine while using a jig for
clamping the specimen. This piece was then sawed
into smaller pieces and finished specimens were in
the shape of very small blocks with all planes
mutually perpendicular to each other. Specimen Fig. 5--Skullcap with shear specimens drilled out

Experimental Mechanics I 239


Fig. 6--Shear-test fixture

For each of the three skullcaps used so far, 5. W h e n the diplSe layer of the skull is subjected
circular plugs are cut using a 8/s-in. bone-plug to a shearing force, the failure stresses are lower
cutter. W a t e r is generously applied to the blade than those developed in tension or compression.
of the cutter during the drilling procedure to act as
a lubricant and to prevent burning of the plug. Acknowledgments
A reference system was designed to identify the This project is being sponsored by the National
location of bone plugs removed from the calvarium. Institute of Neurological Diseases and Blindness
This system is an a d a p t a t i o n of M c E l h a n e y 16 based under C o n t r a c t PH-43-67-1136. I n addition, the
on the coronal and sagittal suture lines of the skull- authors wish to t h a n k Drs. Gikas and Hendrix of
cap. A cut skullcap is shown in Fig. 5. the University of Michigan for help in specimen
A total of 370 tests have been carried out on the acquisition.
I n s t r o n testing machine using the shear grips shown
in Fig. 6. The failure load is recorded in order to References
determine the simple shear-failure stress, the 1. Fung, Y . C., "Biomechanics,'" Appl. Mech. Rev., 21 (1), 1-20
average value of which is 1900 psi. I t should be (1968).
2. Evans, F . G., Stress and Strain in Bones, Springfield, Ill., C. C.
observed t h a t this value is lower t h a n the failure Thomas (1957).
3. Evans, F. G., and Catron, A. R., "'Bibliography on the Physical
stresses obtained in the compression tests. N o Properties of the Skeletal System," Highway Safety Research Inst., Th
clearly defined relation between strength and loca- University of Michigan (1967).
4. Kraus, H., "'On the Mechanical Properties and Behavior of Human
tion or between strength and rate of loading has Compact Bone," Advances in Biomedical Engineering and Medical Physics
yet been determined. (1967).
5. Evans, F. G., and Lissner, H. R., "Tensile and Compressive Strength
of Human Parietal Bone," Jnl. Appl. Physiol., 10, 493-497 (1957).
6. Dempster, W . T., "'Correlation of Types of Cortical Grain Structure
Conclusions with Architectural Features of the Human Skull," Amer. dnl. Anat., 120
(1), 7-31 (1967).
Based oll the above results, the following con- 7. Wertheim, M. G., "Memoire sur l'Elasticitd et la Cohesion des
Principaux Tissues du Corps Humain," Ann. Chim. et Phys., 21, 385-414
clusions m a y be drawn: (1847).
1. Skullcap compact bone has a static elastic 8. Rauber, A. A., Elasticit~tt und Festigkeit der Knochen, Leipzig,
Engelmann (1876).
modulus in tension and compression on the average 9. Bird, F., Becket, H., Healer, J., and Messer, M., "Experimental
of 2.1 X 108psi. Determination of the Mechanical Properties of Bone," Aerospace Medicine,
39 (1), 44-48 (1968).
2. The breaking stress in tension is about 9500 10. McElhaney, J. H., "'Dynamic Response of Bone and Muscle Tissue,"
psi. Jnl. Appl. Physiol., 21, 1231-1236 (1966).
11. Dempster, W . T., and Liddicoat, R. T., "'Compact Bone as a Non-
3. The large hysteresis loop and the large a m o u n t Isotropic Material," Amer. Jnl. Anat., 91,331-362 (1952).
12. Dempster, W . T., and Coleman, R. F., "Tensile Strength of Bone
of recoverable strain induced in a specimen stressed Along and Across the Grain," Jnl. Appl. Physiol., 16, 355-360 (1961).
to failure points out that skull bone is a highly 13. Ascenzi, A., Bonucci, E., and Checcucci, A., "'The Tensile Properties
of Single Osteons Studied Using a Microwave Extensimeter," Studies on the
viscoelastic, brittle material. Anatomy and Function of Bone and Joints, Springer-Verlag, Heidelberg
4. The nature of the compression test results indi- (1966).
14. McElhaney, J. H., and Byars, E. F., "Dynamic Response of Biologi-
cates t h a t the skull can be t h o u g h t of as a sandwich cal Materials," A S M E Paper No. 6 5 - W A / H U F - 9 (1965).
shell possessing transverse orthotropy, the middle 15. Sedlin, E. D., " A Rheological Model for Cortical Bone," Acta
Orthop. Scandinav., Suppl. 83 (1965).
layer being an energy absorber. 16. McElhaney, J. H., unpublished note.

240 I May 1969

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