MECHANICAL
PROPERTIES
OF CRANIAL SUTURES
CAROLYNRENZULLI JASLOW* The University
of Chicago,
Department
of Anatomy.
1025 E. 57th St., Chicago,
IL 60637, U.S.A.
Abstract -Many bones in mammalian skulls are linked together by cranial sutures. connective tissue joints that are morpholodcally variable and show different levels of interdigitation among and within species. The goal of this invest&ion was to determine whether sections of skull with cranial sutures have different mechanical propertIes than adjacent sections without sutures. and if these properties are enhanced with increased interdipitation. To test these hypotheses. bending strength and impact energy absorption were measured for samples of goat (Capra hircus) cranial bone without sutures and with sutures of different degrees of interdigitation. Bending strength was measured under both dynamic (9.7 mm displacement s- ‘) and relatively static (0.8 mm s - ‘) conditions, and at either speed. increased sutural interdigitation provided increased strength during three-point bending. However,except for very highly interdigitated sutures loaded slowly. sutures were not as strong in bending as bone. In contrast, sutures absorbed from 16% to loO?G more energy pr unit volume during impact loading than did bone. This five-fold increase in energy absorption by the sutures was significantly correlated with increased sutural interdigitation.
ISTRODl_‘CTION
forces e.xerted on the skull and sutures (Massler Schour,
The frequency inspired
of head injuries among
numerous
investipations
properties of the cranium.
has
of the cranial
hypothesize
bone.
phologies
might contribute
of canccllous
tures with mechanical
investigators bone
(McElhaney focused
as a
layered
‘sandwich’
et ul.. 1970: liubbard,
on
compacta
some
have studied whole sections of cranial
modeled
the mechanical
or the dipI&
baenid
1971). others have
properties
of just
associating
highly
advantages
reptiles
mastication
the
1960.
no data
anics is necessary to improve
the mechanical
properties and functional
more information
only ofskull
role of the cranium, little attention has been directed at
of the cranial humans.
the skull. the cranial
variable feature of
sutures. Hubbard
observed that in humans, cranial compliant
than the surrounding
rr 01. (1971)
bone, and that bone
and suture had equal bending strengths. However, neither this, nor any other study. has an attempt made to assess the mechanical
mine
in
response
how
the
are
increased
with
conditions, to virtually
bending strength
together (for descriptions
displacement
of sutures and fiber orient-
ation see Moss, 1957; Koskincn rr ul., 1976; Johansen 1986). Generally,
sutures are relatively simple, straight-edged sutural morphology
as the bones overlap or interdigitate. believed
to be associated
at birth.
were
static
trauma
may change
in
were to deter-
properties
of bending
differ between pure
suturat
loading
during
was measured
rates. In addition.
measured
sutures
not
sutures, and in sutures
interdigitation.
under a range of loading
tween age and mechanical
structures,
mcch-
from rapid loading during an impact blow
the collagenous connective tissue fibers that link them
but during growth,
greater
Because sutures function
suture is a joint between the bones of the
1982; Kokich.
to mechanical
mechanical
skull, consisting of the adjacent edges of the bones plus
and Hall,
sutural
to test the hypothesis that these properties
consequences of vari-
there
our understanding
cranial bone and cranial bone containing
ation in sutural morphology. A cranial
concerning
strength and energy absorption
been
and
1972). and
these hypotheses.
The purposes of this investigation
sutures were more
in amphis-
rooting
function in many diverse species, but also
an important
and morphologically
1974).
to support
Clearly
in spite of these etTorts to
su-
when the skull is
in sheep (Jaslow. 1989). However,
are currently
Wood.
understand
on sutural
interdigitated
in pigs and peccaries (Herring,
head-butting
structural
(Cans.
elements (Evans and Lissner. 1957; Melvin ef 01.. 1969; 1971). However.
skull func-
loaded during activities such as burrowing
structure
as independent
to particular
tions. These studies have focused primarily interdigitation,
While
to
ways in which sutures with certain mor-
compact bone (compaccta) that enclose a middle layer the diplo?.
vari-
ation among sutures, have led some investigators
bone is composed of inner and outer layers of bone called
and
1982). This
assertion, and observations of the morphological
of the mechanical
and much of this work has
focused on the characteristics Cranial
humans
1951; Moss, 1957. 1961: Oudhof,
to account
independent
of
growth,
sutural
under two direrent the correlations
properties
be-
of the sutures
for age effects on the changes
in
sutural
interdigitation.
Such changes are
with extrinsic
mechanical
MATERIAIS AND METHODS
Sumple preparation
Rzwid it1 jirul /,m~ 5 July 1989. *Current Address: Biology Department. Rhodes College. 2000 N. Parkway, Memphis. TN 381 I$, U.S.A.
The fresh heads of female domestic hircus) were used to obtain 313
goats (Capra
test specimens of cranial
314
C. R.
JASLOW
bones and sutures. Two sutures were studied: (1) the internasal suture, which remains straight-edged. ing a butt-joint, frontoparietal
throughout among
tain samples of crania) nasal
form-
and (2) the
suture, which exhibits variable amounts
of interdigitation bones
containing
development,
and
most
parietal
individuals
(Fig. 1). To ob-
bone and these sutures. the of the
and frontal
posterior
braincase
bones were removed
from each goat head. These sections of the cranium were stripped
of periosteum.
and frozen
at
-5°C.
They were then cut with a band saw into test specimens while
still frozen
to minimize
heating
of the
bone. Samples with frontoparietal
sutures or samples
of just
about
frontal
bone
were
cut
x 4-S cm long. Samples with internasal about
1 cm wide sutures were
1 cm wide x 2.5 cm long. Specimen
ranged from about samples
were irregularly
specimen
curved,
were individually
the ends of each
embedded
resin and cured at room temperature 2 h. During
thickness
2 to 5 mm. Because most of the in fiberglass
for no more than
this time, the bone or suture
moist with physiological
was kept
saline. After curing, the resin
blocks on the ends of each sample were trimmed produce
relatively
uniform
samples
to
that approxim-
ated straight beams. Sample beam width (w) and mean thickness(h)
at the suture (Fig. 2) were measured with
calipers (kO.05
mm) and thcsc values wcrc used later
to standardize
for diffcrcnces
in cross-sectional
arca
among test specimens. The dcgrcc of intcrdigitation each suture, a dimension& tracing
of
value. was cstimatcd
the path of the external
Fig. 1. Dorsal view of ;I goat skull showing the simple internasal (inJ and inlcrdigilalcd fronioparictal (fp) sutures. Rectangular openings in the skull show thcgcncral shape and orientation of typical test samples that wcrc cut from lurgcr sections that had been removed from the skull (dashcd lines).
by
suture surface. and I
Y
dividing that length by the straight lint distance from start to end of the suture. By this method, the straightedged internasal
sutures always
-x-
had intcrdigitation
values of 1, and the more convoluted
Y
a l
frontoparietal
I
I
sutures ranged from about 2 to about 6.5. The samples were stored in plastic bags at - 5 ‘C for up to 6 weeks, then placed in physiological
saline at 5°C to hydrate
for at least 12 h prior to testing. Bcforc testing. samples were brought during
to room temperature
(within
all tests, the samples were kept
I h) and
moist
with
saline.
The test specimens were loaded as beams in symmetrical
three-point
someter
modified
bending using a Monsanto to permit
electronic
imposed loads and deformations. formed such that the internal
Fig. 2. (a) Diagram of a test sample showing width (w) and thickness (h) measurements. (b) Diagram of the technique used to load the test samples in symmetrical three-point bending and impact. In both cases ths force was directed onto the external surLce of the suture or bone (ex). The span length (x) was 19.42 mm during three-point bending and approximately 25 mm during impact loading. The diameter of the force application platen during bending was I.59 mm with a radius OF curvature of 3.17 mm. On average, the span of collagen between the two bones was about 0.2 mm.
bone surface was sup-
suture surface to roughly
ditions that might accompany
of
The tests were per-
ported, and the force was applied at mid-span external
ten-
recording
b
simulate
on the
the con-
an external load on the
acceptable.
Bending tests of the frontoparietal
skull and sutures (Fig. 2). The total span length was
were performed
19.42 mm, therefore
displacement
thickness
the ratio
of span length
to the
(= depth) of the samples ranged from about
s-r
‘fast’ displacement
(henceforth
regarded as ‘slow’ and
rates, respectively). The internasal
4: I to over 9: 1. Sample beams were loaded until the
sutures were only loaded at 9.7 mm s-
recorded
To
force returned
to zero (the starting
level);
standardize
failure was defined as the peak force applied. Only test
strength
specimens that broke
culated
at the suture were considered
(peak
sutures
at crosshead speeds of 0.8 and 9.7 mm
for
size
differences,
’ displacement. the
bending
stress) of each test sample was calelastic beam theory according to
Xlechanlcul
[equation
315
properues of cramal sutures
(I b]: MC um*.=I
(1)
absorption
before failure.
supported.
unfixed, at either end while a pendulum
The
test specimens were
head swung through the unsupported
middle, striking
the external surface of the suture as in the three-point bending tests (Fig. 2). The
where
pendulum
apparatus
was
calibrated for energy losses of 14%. caused mainly by
M=Fd
maximum
/=(Hh’);l2
second moment
bending moment
(Nm)
friction
of area (m”)
at the axis of rotation
potentiometer
when a single-turn
was attached to the axis to record the
c
l/2 mean sample thickness (ml
angular displacement of the pendulum.
a mar
bending strength (Pa)
the height of the pendulum
By measuring
before and after loading
F
peak force (N)
the sample. the amount of energy absorbed by the test
d
l/2 span length (ml
specimen was calculated as:
\1
sample width (m)
h
mean sample thickness (m).
(I) overestimates
Equation
the absolute
strength of bone by as much as 50-100% plastic yielding
E=[tflK(i--j)]-f., bending
1970; Burstein cat(II., 1972). However,
(Currey,
this was not a
problem here since values of bone and sutural strength were compared
relative to one another.
values of absolute culated according
bending strength,
In contrast to the values cal-
(I) correspond to what
to equation
Currcy calls ‘the modulus of rupture’
(1970, p. 222).
Least squares regressions (LSR) were used to dctcrmint
if
the strength
of the
where
because of
in the bone before failure
Irontoparietal
samples varied with the dcgroc of sutural
sulurc
intcrdigit-
energy absorbed (J)
E m
mass of the pendulum (kg)
R
gravitational initial
L
Values of energy absorption
were divided by the cross-
sectional area of the beam (mean thickness x width) to normalize for size differences among the test samples. Cross-sectional
gun content and orientation
same for
in the suture may occur
height (m) height (m)
energy loss (J).
frictional
ation
regressions were performed initially
acceleration (9.81 m sd2)
pendulum
final pendulum
;
ation for each bending rate. Because changes in collawith age, multi@
(2)
arca was sullicicnt
bccausc the third all
for this standardiz-
dimension
the test spccimcns.
bctwocn energy
absorption
(Icngth) was the The
relationship
and degree of sutural
to assess the potential elTccts on sutural strength of the
interdigitation
goat’s age alone or with the changes in interdigitation.
regression.
The age of each goat was estimated
using the tooth-
using age and sutural
wear criteria
(19X2). A more
test for the potential e!Tccts of age on energy absorp-
of Deniz
and
Payne
general test of the elTect of age on sutural obtained
by regressing
age against
strength was the values
of
tion.
was dctormincd
using
Again, a preliminary
Only
samples
intcrdigitation that
least-squares
multiple
broke
regression
was executed to
at the suture
were
included in these analyses.
strength for the internasal sutures, which lacked interdigitation.
These
test
animals ranging from
samples
were
taken
from
RESUI.TS
I to 9 years of age. a range that
Test results of 88 cranial samples from 33 goats were
covers most of the lifespan of a domestic goat.
used in the different approximately Samples of cranial
bone or frontoparietal
suture
tested (Table
65%
regressions;
these represented
of the total number
I). Age had no significant
of samples
etTect on the
were subjected to impact loading using a pendulum
bending strength
impact
sutures across the age range used in this study. The
testing
apparatus
to measure
their
energy
of the cranial
samples containing
T;~blc I. Descriptive summary ol Ihc numhcr (,I) and percentage (%) of goal cranial suture samples that failed succcss~ully in the ditTerent mechanical
” (%I used Goals Range
tesls
(1) Fast bending strength (FP suture)
(2) Slow bending strength (FP sulurc)
(3) Fast bending strength (IN sulure)
(4) Energy absorption (FP suture)
22 (63%) IO IA
21 (70”/,) 6 3-I
27 (68%) II 2-4
18 (60%) 9 l-4
‘Success’ was defined as failure across the SUIUTC. The tests include: (I) fast bending strcnglh and (2) slow bending strength of the fronlopariclal suture (FP). (3) fast bending strength ol the internasal sulurc (IN), and (4) energy absorption of the frontoparictal sulurc. For each test. additional values show the number ol ditTcrent goat skulls from which the successful test specimens were obtained (goats), and the range of successlid lest specimens used per goat skull (range).
316
C. R. 40.
a 3
JASLOW
Table 2. Multiple regression significance tests of age and interdigitation as predictor variables for rapid bending strength(R). slow bending strength(S), and energy absorption of frontoparietal sutures
30.
.
Regression coefficient
: 20. P ::
.
Bending strength (R)
z
Interdigitation Age
.o
‘O-
I
0
10
4
AGE (yearm)
Bending strength (S) Interdigitation Age
Fig. 3. Mean bending strengfh of internasal sutures for samples of diRerent ages. Lines indicate _+ I SE. R =0.288. p z= 0.05. Slope =0.9. intercept = 17.5 (n = 27).
regression of age against (which
lack
strength
8.23 0.56
2.37’ 0.09
33.69
4.26t
12.90
1.34
1.01 1.76
2.62’ 1.64
Energy absorption Interdigitation Age
lp