2

BIOMECHANICS OF CLOSED
HEAD INJURY
A. J. McLean and Robert W. G. Anderson

This chapter discusses ways in which the brain is

thought to be injured by a blunt impact to the head.
The impacting object is assumed to be unlikely to
penetrate the skull in the manner of a bullet, for
example.
The chapter is also concentrated on injuries to the
brain, rather than lacerations and abrasions to the
scalp or fractures of the skull. Obviously, if the skull is
fractured and displaced inwards, then the part of the
brain underlying the fracture will be injured. However, the brain can be very severely injured without
the skull being fractured by the impact to the head
(Gennarelli, 1980). Other intracranial injuries, such as
subdural hematomas, are referred to briefly in relation
to theories of mechanisms of primary injury to the
brain. Secondary complications of head injury also
affect the brain but they are not considered in this
chapter.

2.1

Impact to the head

2.1.1

IMPACT AND IMPULSE

Closed head injury is, in the great majority of cases, a

consequence of an impact to the head. However, there
are references in the literature to the production of
diffuse axonal injury in non-impact experiments in
which the head of an animal was accelerated in a
manner that minimized the direct contact effects of an
impact to the head (Gennarelli and Thibault, 1982;
Adams, Graham and Gennarelli, 1981). There are also
reports of brain injury resulting from acceleration of
the upper torso of an animal without any direct
impact to the head (Ommaya, Hirsch and Martinez,
1966). These reports are discussed later in this chapter.
For the present, the readers attention is drawn to the
distinction between an impact to the head and an
impulse transmitted to the head through the neck.
Both an impact and an impulse, as described above,
can accelerate a stationary head (or decelerate a

moving one) but an impact will also produce contact

effects on the head, such as skull deformation or
fracture, with an associated risk of injury to the brain.
However, in practice it appears that injury to the
human brain is almost always the result of an impact
to the head, or to a protective helmet, rather than an
impulse transmitted through the neck (Tarriere, 1981;
McLean, 1995).
An impact to a given location on the head can be
characterized by the impact velocity and the physical
properties of the struck or striking object.
2.1.2

IMPACT VELOCITY

Some forensic pathology research literature implies

that the type of brain injury differs according to
whether the head is stationary and is struck by a
moving object, or is moving and strikes a stationary
object (Yanagida, Fujiwara and Mizoi, 1989). This
distinction can be of considerable legal significance in
cases of assault in which the victim sustains a head
injury which could have been caused either by a blow
to the head or from striking the head in the resulting
fall. However, as Holbourn (1943) observed, the
moving head typically strikes an object that is considerably more massive than the head, whereas the
stationary head is more often hit by objects which are
of similar mass to the head or even lighter, such as a
club.
In physical terms the difference between the head
moving or being stationary on impact is solely in the
frame of reference. Most readers will have experienced
the paradoxical sensation of not knowing which train
is moving when the train alongside theirs in the
station starts to move. There is no physical difference
between the forces involved in a stationary head being
hit or a moving head striking a fixed object, given that
other factors such as the velocity of the impact and the
characteristics of the object contacted by the head are
the same. Throughout this chapter the terms struck

Head Injury. Edited by Peter Reilly and Ross Bullock. Published in 1997 by Chapman & Hall, London. ISBN 0 412 58540 5

26

BIOMECHANICS OF CLOSED HEAD INJURY

and striking will therefore be used more or less

interchangeably.
In general, the head impact velocity will be greater
in, say, high-speed crashes on the road than in crashes
at low speed. However, that is not necessarily so. The
type of crash is a significant factor, with high speed
rollovers sometimes being relatively non-injurious
compared to collisions with another vehicle or a fixed
object at a much lower speed. Even in two apparently
similar crashes it is not at all uncommon for a person
in one crash to receive a severe impact to the head
when a person in the other crash may not be hit on the
head at all.

2.1.3 PHYSICAL PROPERTIES OF THE STRUCK OR

STRIKING OBJECT

(a)

Shape

As noted above, we have assumed that the impacting

object does not penetrate the skull in the manner of a
bullet, for example. The most important characteristics
of the struck or striking object are therefore its stiffness
and surface area, given that its shape is consistent with
it imparting a blunt impact to the head.

(a)

Local deformation of the skull at the point of impact

can be expected to result in direct contact injury to the
underlying brain tissue. This almost inevitably occurs
if the impact produces a displaced fracture of the
skull, but high-speed cine radiography has shown that
the skull can also be indented sufficiently in the first
few milliseconds of the impact to compress the
underlying brain and then return to its original shape
without residual evidence of such deformation in the
bone (Gurdjian, 1972; Shatsky et al., 1974).
Shatsky et al. (1974), in their studies using anesthetized monkeys, showed that in occipital impacts the
skull was not deformed and no underlying brain
lesions were observed. Impacts in the temporoparietal
region did show evidence of transient skull deformation and accompanying brain lesions. For a given
impact, the risk of underlying skull fracture will also
vary with the location of the impact on the head.
Nahum et al. (1968) estimated that for a contact area of
approximately 1 square inch (6.5 cm2) the force
required to produce a clinically significant skull
fracture in the frontal area of the cadaver skull was
twice that required in the temporoparietal area.

(b)
(b)

Stiffness

The term stiffness, as used here in the engineering

sense, is sometimes confused with hardness. The
property of stiffness is well illustrated by the compression of a spring. The less the spring deflects under a
given load the stiffer it is said to be. By comparison, a
thin sheet of glass is very hard on the surface but it
will bend, or deflect, easily when loaded. It has a low
level of stiffness, which, of course, decreases abruptly
to zero when the glass breaks.
A concrete floor is extremely stiff; almost infinitely
so in relation to the human head. A sheet metal panel
of a car, however, may be deformed several centimeters when struck by the head of a pedestrian or an
occupant of the car. Such differences in stiffness of the
object struck by the head have been shown to be
associated with differences in the type of the resulting
intracranial injury, as discussed below (Gennarelli,
1984; Willinger, Kopp and Cesari, 1991).

2.1.4

LOCATION OF THE IMPACT ON THE HEAD

The location of the impact on the head can be related

to brain injury in a number of ways: such as by local
deformation of the skull and, more importantly, by
determining the relative levels of linear and angular
acceleration of the head.

Injury adjacent to the location of the impact

Injury remote from the location of the impact

The resulting injury can also be, and very often is,
remote from the location of the impact. This is so for
injuries to both the skull and the brain. A blunt impact
to the calvarium may result in remote linear fractures
in the base of the skull. This is thought to be a
consequence of the skull cap being strong enough to
withstand the force of the impact, which is therefore
transmitted to the much thinner bone found in parts of
the base of the skull. However, once a remote linear
fracture has been initiated in such a region, it can
propagate almost instantly back into the calvarium
which is still loaded by the force of the impact (Melvin
and Evans, 1971).
The term contrecoup has long been used to
characterize an injury to the brain which is on the far
side of the head to the impact. It has been postulated
that contrecoup injury to the brain is a consequence
of rapid and localized pressure changes near the
surface of the brain tissue due to cavitation effects
arising from the brain moving relative to the cranial
cavity in response to the impact (Courville, 1942).
However, Nusholtz et al. (1984) reported that, in
occipital impacts to the head of the Rhesus monkey,
contrecoup negative pressures greater than one
atmosphere did not appear to be associated with
injury to the brain.
In the case of an occipital impact it is possible that
relative motion between the brain and the often

RESPONSE OF THE HEAD TO IMPACT

irregular bony anatomy of the anterior fossa in the

human may play a role in the causation of contrecoup
injury to the brain (Shatsky et al., 1974).
(c)

Head impact location and brain injury severity

Finally, the location of the impact to the head can

determine the nature, pattern and severity of injury
throughout the brain. More than 200 years ago
Percivall Pott, Surgeon of the City of London,
remarked upon an apparent relationship between
impact location on the head and the severity of the
resulting brain injury:
I will not assert it to be a general fact, but as far
as my own experience and observation go, I
think that I have seen more patients get well,
whose injuries have been in or under the frontal
bone, than any other bones of the cranium. If this
should be found to be generally true, may not
the reason be worth inquiring into?

27

not, the skull may be crushed to a greater or lesser

degree and the injury to the head, and the brain, will
be directly related to the location and extent of the
skull deformation. An example of such an impact
would be a masonry block falling on the head of a
person lying on a concrete floor.
As noted above, most cases of closed head injury
result from a moving head coming into contact with
a stationary object or with an object moving at a
different velocity. Injuries to the brain are generally
thought to result from the acceleration of the brain in
response to the impact to the head, with the exception of direct contact injuries resulting from skull
fracture or motion of the brain relative to the cranial
cavity. The term acceleration is used here in the
absolute sense to refer both to cases in which the
stationary head is accelerated by an impacting object
and to cases in which the moving head is decelerated
when it hits a stationary object, or one moving at a
lower velocity.

The Chirurgical Works of Percivall Pott, FRS, 1779

Some 200 years later this matter has been inquired into
and the results are consistent with Percivall Potts
experience and observation. For example, the experimental work of Gennarelli, Thibault and Tomei (1987)
on subhuman primates demonstrated that a combination of linear and angular acceleration of the head in
the coronal plane (rotation of the head about a point in
the cervical spine, somewhat analogous to the motion
resulting from a lateral impact to the head) was more
injurious to the brain than similar acceleration in the
sagittal plane (as in a frontal impact). The results of
detailed investigation of a small number of cases of
fatal and severe head injury to car occupants were also
consistent with frontal impact to the head being less
injurious to the brain than lateral impact (Simpson et
al., 1991). However, animal experiments conducted in
Japan, discussed later in this chapter, indicate that the
relationship between impacts in the sagittal and
coronal planes and injury to the brain may be
considerably more complex than is commonly supposed (Ono et al., 1980; Kikuchi, Ono and Nakamura,
1982).

2.2

Response of the head to impact

Another factor which has a marked influence on the

severity of the resulting injury is whether or not the
head is free to move in response to the impact.
2.2.1

MOVEMENT OF THE HEAD

The mechanism of injury to the head depends on

whether or not the head is free to change its velocity
when struck (Denny-Brown and Russell, 1941). If it is

2.2.2

THE FORCE OF THE IMPACT

For a given head impact velocity, an impact with a

sheet metal panel of a car will result in a much smaller
impact force, and hence lower acceleration of the
head, than will an impact with a concrete floor. This is
because the moving head is brought to rest over a
greater distance in the former case, as indicated by the
considerable dent which is often seen in the panel
following a head impact. However, the lower acceleration means that the impact force, albeit at a lower
level, is acting on the head for a longer time.
As will be seen later, there is reason to believe that
the sensitivity of the brain to injury from an impact to
the head is time-dependent. A very high level of
acceleration of the head acting for a very short time
may be less injurious than a lower level of acceleration
acting over a relatively longer time period.

2.2.3 LINEAR AND ANGULAR ACCELERATION OF

THE HEAD

If the line of action (the vector) of the impact force

passes through the center of gravity of the head then
the head will be accelerated in a straight line. In other
words, it will be subjected to a linear acceleration. This
general statement ignores any restraining effect of the
neck, which is likely to be small in the time interval
during which injury to the brain is thought to occur.
However, if the force vector does not pass through the
center of gravity then the head will be subjected to
both linear and angular acceleration, with the latter
resulting in rotation about the center of gravity. In this
chapter the terms rotational and angular are used

28

BIOMECHANICS OF CLOSED HEAD INJURY

interchangeably. In some research papers a distinction

has been made between these two terms by defining
the former to mean rotation about the center of gravity
of the head and the latter to refer to rotation of the
head about some other point, such as in the cervical
spine, which results in a combination of linear and
angular motion of the center of gravity of the head.
The basic relationship between the force of the
impact and the resulting angular acceleration () of
the head is similar to that for linear acceleration except
that the offset (x) of the force vector from the center of
gravity of the head is taken into account along with
the moment of inertia (I) of the head:
F x = I .
The moment of inertia of a solid sphere, a very crude
approximation to the human head, about an axis
through the center of the sphere is:
I = 2/5 m r 2.
The force changes during the impact and so the
magnitude of the angular acceleration will change
with time during the impact.
If the human head was spherical, with its center of
gravity at the center of the sphere, then the force
vector of an impact perpendicular to the surface
would always pass through the center of gravity.
However, the human head is far from spherical and
so, for an impact perpendicular to the surface of the
skull, the distance of the force vector from the center of
gravity varies with the location of the impact on the
head. In general, regardless of differences in head
shape, the vector of an impact on the side of the
head is likely to be offset more from the center of
gravity than that of an impact on the frontal bone or
the occiput.
However, the human head does come in a wide
range of shapes and it is conceivable that the range of
this variability may be sufficient to influence the
response of the head to impact and hence the nature
and/or severity of the resulting injury to the brain
(McLean et al., 1990). For example, the force vector of
a lateral impact to the side of the frontal bone of a long
narrow head is likely to have a greater offset from the
center of gravity of the head than is a similar impact to
a rounder head, both viewed in the horizontal plane.
In practice, most impacts to the head will pocket
into the scalp to some degree. This may result in the
force vector not being at 90 to the surface of the skull,
which, in turn, will affect the distance between the
force vector and the center of gravity of the head.
However, any variation arising in this way is unlikely
to affect the general relationship between impacts on
the side of the head and greater offsets of the force
vector from the center of gravity. This means that, for
a given impact severity, lateral impacts are likely to

result in a higher level of angular acceleration of the

head than are frontal or occipital impacts (see, for
example, Vilenius et al., 1994).
If the level of angular acceleration increases with a
change in the location of the impact on the head, this
increase will be accompanied by a decrease in the level
of linear acceleration and vice versa. While it is possible
to envisage an impact to the head, such as an occipital
impact or one to the frontal bone, producing only
linear acceleration, it is most unlikely that any realistic
impact to the head will produce only angular acceleration about the center of gravity.
2.2.4

STRESS AND STRAIN

Stress (tensile or compressive) is measured in terms of

force per unit area. Strain describes the response of
the material which is being stressed. It is measured in
terms of the proportional change in length in the
direction of the tensile or compressive stress: hence
reference to, for example, a 10% strain. A compressive
strain will, of course, indicate a reduction in length,
whereas a tensile strain will indicate that the stressed
material has been stretched.
Another type of stress, and associated strain, which
is thought to be particularly relevant to injury to the
brain results from the action of a shear force. The effects
of shear stress are illustrated by the action of a pair of
scissors, or shears, cutting a thin stack of sheets of
paper. Shear stress is also measured in terms of force
per unit area but the area is measured in the plane in
which the force is acting (at right angles to the face of
the sheets of paper in the example given here).
Similarly, shear strain is the proportional displacement,
expressed in terms of the original thickness, resulting
from the action of the shear force.
(a)

Strain rate

The rate of application of a force is reflected in the rate

of the resulting strain, expressed in terms of strain per
unit of time. The response to physical loading of some
biological materials is strain-rate-dependent (Viano
and Lau, 1988).

2.3

Methods of investigation

Three types of investigative method have been used in

the study of brain injury biomechanics: experimental,
mathematical and observational.
2.3.1

EXPERIMENTAL STUDIES

Much of what is known, or postulated, about brain

injury mechanisms in living humans has come from
experimental studies. Test subjects have included

TOWARD AN UNDERSTANDING OF BRAIN INJURY MECHANISMS

human cadavers, anesthetized animals and animal

cadavers. Physical models of the head have also been
used. Experiments conducted on living humans have
defined the response of the head to non-injurious
impact.
The human cadaver head has the advantage of valid
anatomical, but not physiological, representation of
the head of the living human (although attempts have
been made to simulate vascular lesions by pressurizing the vascular system prior to impacting the head).
The anesthetized animal is, of course, a living subject
but differs anatomically from the human. Highly
sophisticated experimental techniques have been
developed in the course of the evolution of animalbased head injury studies (see, for example, Nusholtz,
Kaiker and Lehman, 1986). Although the anatomical
differences are least in the non-human primate, the
smaller size of the monkey skull and brain introduce
problems of dimensional scaling in attempts to relate
the results to the living human.
Experiments using physical models of the brain, or
skull and brain, have included measurements of
strain, recorded by measuring the distortion of an
impregnated grid or by photoelastic means, in accelerated gel-filled containers (Thibault, Gennarelli and
Margulies, 1987; Holbourn, 1943).
2.3.2

MATHEMATICAL STUDIES

Mathematical models of human and animal heads are

now at the stage which, with the ready availability of
powerful computers, justifies their use in attempts to
predict the likely impact-induced motion of the brain
relative to the skull and strains within the brain tissue
(Zhou, Khalil and King, 1994). The development of a
realistic mathematical model depends, inter alia, on
knowledge of the physical response of brain tissue to
impact loading, in addition to the response of the skull
and membranes (Melvin, Lighthall and Ueno, 1993).
Experimental data are available for use in the
validation of mathematical models of the animal
skull/brain system. Validation of mathematical models of the human head depends on the availability of
adequately detailed and accurate estimates of the
forces involved in impacts to the head of the living
human in events such as road crashes and the
resulting pathology, particularly the neuropathology.
2.3.3

OBSERVATIONAL STUDIES

The investigation of cases in which living humans

have sustained a closed head injury has the desirable
attribute that the phenomenon being investigated is
exactly that which is of interest. However, it is difficult
to obtain adequately detailed information on the
characteristics of the injury to the brain, and the

29

severity of the impact to the head can only be

estimated (Ryan et al., 1989; Gibson et al., 1985).
(a)

Neuropathology

In fatal cases the neuropathologist can provide information on injury to the brain at the microscopic level.
Even so, there are limitations imposed by the fact that
some brain lesions are not at present readily detectable
unless the fatally injured individual survives for some
hours after the incident which produced the injury. In
surviving cases, magnetic resonance imaging (MRI)
and computed tomography (CT) can be used to
identify and locate larger hemorrhagic lesions in the
brain.
(b)

Characteristics of the impact to the head

The location of the impact on the head can be

determined from the location of abrasions and contusions, depressed skull fractures and subgaleal hematomas at autopsy or in operative cases. In non-fatal cases
it can be difficult to determine the location of an
impact above the hairline.
Determining the object or objects struck by the head
usually depends on examining the setting in which
the injury occurred, such as the vehicle involved and
the crash site in the case of a road accident. The
stiffness of the struck object may be able to be deduced
from a simple description of the event, such as the
head striking a concrete floor as the result of a fall. In
a road crash the head impact is most likely to have
been with some part of the vehicle. Knowledge of the
stiffness of the struck part of the vehicle can be used to
estimate the force of the head impact, assuming that a
reasonably accurate estimate can be made of the
velocity with which the head struck the object. If a
record has been made of any residual deformation of
the struck object, an instrumented headform can be
used to measure the force required to reproduce the
dent observed in the actual impact.

2.4 Toward an understanding of brain

injury mechanisms
The study of the biomechanics of head injury has been
concentrated on the relationship between the forces
applied to the head and the resulting injury to the
brain. Some of the earlier studies used the presence or
absence of skull fracture as the outcome variable,
assuming that it would be positively related to the
severity of brain injury (see the following section on
the impact tolerance of the head). However, it was
soon recognized that the response of the whole head
to impact was likely to be the main determinant of the
nature and severity of injury to the brain.

30
2.4.1

BIOMECHANICS OF CLOSED HEAD INJURY

SETTING THE SCENE

The work of Holbourn (1943), a research physicist in

the University Department of Surgery in Oxford, UK,
set the scene for what has been the most widely
accepted theory of the mechanism of injury to the
brain: that rotational motion of the head is the
predominant causal factor.
Reasoning that the brain was effectively incompressible, Holbourn hypothesized that linear acceleration of the head could not deform the brain and so was
unlikely to result in injury to the brain tissue. Angular
acceleration, however, could be expected to set up
shear strains in the brain, and the relative displacement within the brain that is implied by the creation of
such strains would be expected to be a cause of
injury.
The bowl of porridge analogy is sometimes used to
illustrate Holbourns hypothesis (Figure 2.1).
If the stationary bowl is suddenly moved sideways
(linear acceleration) there will be no appearance of
relative motion in the porridge (apart from spilling
over the side, which is not possible with a closed
vessel such as the cranial cavity). If, however, the bowl
is rotated rapidly (angular acceleration), that part of
the porridge adjacent to the bowl will tend to move
with the bowl and the porridge in the center will tend
to remain stationary. This can only happen if there is
relative motion (shear strains) within the porridge.
Holbourn tested his hypothesis using the physical
model referred to above: a gel-filled two dimensional
model of the human head. The strains produced in the
gel by acceleration of the model in that plane were
revealed by photoelastic techniques. As he predicted,
the model was relatively insensitive to linear acceleration but the pattern of strains produced by angular
acceleration could readily be demonstrated.

of the bowl produces

Figure 2.1 Angular acceleration ()
shear strains in the contents, as illustrated by the layers
sliding across each other.

The other observation which he made was that for

very short blows the duration of application of the
accelerating force was an important factor in the
production of shear strains in his model brain,
whereas for blows of long duration the levels of
shear strain were independent of the time for which
the force acts. The change from short to long
duration was estimated to occur somewhere in the
range 2200 ms (Holbourn, 1943). He also noted that
interposing a deformable object, such as a crash
helmet, between the blow and the head has the effect
of extending the duration of the impact and thereby
reducing the average level of the force transmitted to
the head (Cairns and Holbourn, 1943).
Some 20 years elapsed before Holbourns hypothesis that angular acceleration of the head was likely to
be much more injurious to the brain than linear
acceleration was followed up by other investigators.
One very practical reason for this was that it was a
relatively straightforward matter to measure linear
acceleration but techniques to measure the angular
acceleration of the head in animal experiments were
not available.

2.4.2

THE WAYNE STATE TOLERANCE CURVE

At the same time that Holbourn was conducting his

experiments on physical models in England, Gurdjian
and Webster (1943) commenced studies at Wayne State
University in Detroit on the effect of impacts administered in various ways to the head of the dog. In 1955,
together with Lissner of the College of Engineering,
they reported their Observations on the mechanism of
brain concussion, contusion, and laceration (Gurdjian, Webster and Lissner, 1955). By applying air
pressure directly to the unopened dural sac for
various time periods they were able to show that the
severity of the concussive effect depended on both the
intensity of the pressure pulse and the duration of its
application. They concluded that Concussion occurs
as the result of brain stem injury either from increased
intracranial pressure at the time of impact, direct
injury by distortion, mass movement, shearing, or
destruction by a missile. Brief reference was made to
the possibility that rotation of the head might result in
the brain being injured by abutting against bony
projections within the skull.
Gurdjian and Lissner then conducted studies on a
physical model similar to Holbourns, but with the
inclusion of a simulation of the foramen magnum and
brain stem. These studies led them to conclude that
the mechanism of concussion is shear strain in the
brain stem caused by pressure gradients due to closed
system dynamics of impact (Gurdjian and Lissner,
1961).

TOWARD AN UNDERSTANDING OF BRAIN INJURY MECHANISMS

Lissner, Lebow and Evans (1960) also investigated

the relation between linear acceleration and intracranial pressure changes resulting from impacts to the
frontal bone of the embalmed human cadaver head.
The report on this work became notable for what was
almost a passing reference to the acceleration required
to produce a linear fracture of the frontal bone. The
plot of these results (Figure 2.2), later supplemented
by other data (Gurdjian et al., 1961), formed the basis
for the development of the Head Injury Criterion,
which is used almost universally today as the measure
of the risk of head injury in automobile crash injury
testing. This work, and the Head Injury Criterion, are
discussed at greater length in section 2.5.1.
Further investigations at Wayne State University
through the 1960s included occipital impacts to the
freely moving head of the anesthetized stumptail
monkey. In reporting on those experiments Hodgson
et al. (1969) commented that their results supported
the theory of Gurdjian and Lissner (1961). In particular, Hodgson et al. concluded that Although the
motion of the head involved both angular and
translational acceleration, the preponderance of affected cells found in the brain stem and the almost
complete absence of chromatolysis in the cortex,
makes it appear likely that translational acceleration is
the most important mechanism (Hodgson et al.,
1969).
However, in other studies of head injury mechanisms conducted in the 1960s, Ommaya and Hirsch
showed that in studies of whiplash injury the provision of a cervical collar neck support for monkeys
subjected to whole body acceleration almost eliminated the cases of concussion that were observed
when the head was free to rotate (Ommaya, Hirsch
and Martinez, 1966). In 1970, on the basis of further

Figure 2.2 The Wayne State tolerance curve. Points below

the curve are unlikely to be associated with severe brain
injury. (Source: reproduced from Gurdjian, Roberts and
Thomas, 1966, with permission.)

31

analysis of the results of these studies, they concluded

that no convincing evidence has to this date been
presented which relates brain injury and concussion to
translational motion of the head for short duration
force inputs, whether through whiplash or direct
impact (Hirsch and Ommaya, 1970).
2.4.3 FURTHER DEVELOPMENT OF EXPERIMENTS
USING HUMAN SURROGATES

In the early 1970s, Ommaya initiated work with

Gennarelli and Thibault on a series of head impact
experiments using monkeys (This work was later
continued by Gennarelli and Thibault at the University of Pennsylvania, in collaboration with Adams,
and then Graham, from the Institute for Neurological
Sciences in Glasgow.) They subjected the head of the
animal to predominately linear or angular acceleration
in a defined plane while at the same time minimizing
the direct contact effects of the impact on the head.
This was done by encasing the monkeys head in a
rigid skull cap and filling the space remaining
between the head and the cap with dental cement. The
skull cap was attached via a mechanical linkage to a
piston which, when actuated, accelerated the head
(Gennarelli and Thibault, 1982).
The rationale for attempting to minimize contact
effects of an impact to the head is clear. However, as
Gennarelli (1980) has noted, in the human there
appears to be little relationship between the presence
or absence of skull fracture and the severity of injury
to the brain. This could be interpreted to mean that the
concentrated forces of a localized impact act on the
brain in much the same way as the more uniformly
distributed forces of an impulse applied to the head as
a whole, apart from brain lesions due to local
deformation of the skull at the point of impact.
The linkage attached to the rigid skull cap constrained the motion of the head to a single plane with
the head rotating about a point in the region of the
lower part of the cervical spine. The movement of the
head was limited to an arc of 60 before the motion
was abruptly stopped. As the level of acceleration was
lower than the level of deceleration it was claimed that
the injurious event was the deceleration, although
there does seem to be reason to be concerned about the
injury potential of the acceleration phase. Physical
models subjected to the sequential accelerationdeceleration pulses showed marked distortion (strain) in
the brain tissue during the acceleration phase (Thibault, Gennarelli and Margulies, 1987; Margulies,
Thibault and Gennarelli, 1990).
Gennarelli and Thibault (1982) did find that to be
able to continue to produce subdural hematomas
when they increased the duration of the deceleration
phase they also had to increase the level of the

32

BIOMECHANICS OF CLOSED HEAD INJURY

deceleration itself. This contrasted with their finding

that axonal injury and concussion could be produced
at lower deceleration levels when the duration of the
deceleration phase was increased, a result which was
consistent with the acceleration/time relationship
shown in the Wayne State tolerance curve (Figure 2.2).
Their explanation for this difference was that the
bridging veins are sensitive to the rate at which the
acceleration is applied. However, there is now evidence that the bridging veins are not strain-ratesensitive (Lee and Haut, 1989).
Lee, Melvin and Ueno (1987), working with a twodimensional finite element model of the brain of the
Rhesus monkey, concluded that the subdural hematomas may actually have been produced during the
acceleration phase of the biphasic test device developed by Thibault and Gennarelli. This is because any
increase in the duration of the deceleration phase had
to be accompanied by a corresponding decrease in the
duration of the acceleration phase, and hence an
increase in the level of the acceleration was necessary
to maintain a given level of deceleration.
2.4.4

BRAIN INJURY WITHOUT HEAD IMPACT?

In many of the publications on this very extensive

series of experiments at the University of Pennsylvania, reference has been made to the non-impact
nature of the acceleration of the head of the animal
(see, for example, Gennarelli and Thibault, 1982). The
intent may have been to draw attention to the fact that
contact phenomena, such as deformation of the skull,
were minimized by distributing the accelerative load
over a wide area of the head. A motorcyclists crash
helmet performs a similar function, while also absorbing some of the energy of the impact.
However, the term non-impact can, of course, be
interpreted to mean that the head was not subjected to
an impact. Such an interpretation can be a matter of
considerable forensic significance. For example, in
cases of alleged child abuse it is not uncommon for the
defense to allege that the infant was shaken vigorously rather than the head being struck by, or against,
some object. The probable validity of such an assertion
was investigated by Duhaime et al. (1987) who
concluded that vigorous shaking of the torso of an
infant was most unlikely to result in injury to the
childs brain in the absence of an impact to the head.
They estimated that the head acceleration level produced by such shaking was probably about one-50th
of the level resulting from an impact. This finding is
consistent with the results from our investigation of
brain injury in road crashes, although the force which
can be imparted to the torso, and hence to the head, by
an adult shaking an infant is likely to be considerably
less than can occur in a road crash.

Meaney, Thibault and Gennarelli (1994), at the

University of Pennsylvania, used a mathematical
model of the human body to investigate the likelihood
of that occurring to a car occupant subjected to a
severe lateral impact. They concluded that the acceleration of the head is unlikely to reach a level which
would be injurious to the brain. This is consistent with
McLeans finding, referred to earlier, that there were
no cases of brain injury without head impact in a
series of more than 400 fatally injured road users
(McLean, 1995).
2.4.5 THE ROLE OF LINEAR AND ANGULAR
ACCELERATION

Ommaya and Gennarelli (1974) reported that linear

acceleration of the head of the squirrel monkey in the
sagittal plane was associated with focal lesions but
was unlikely to produce cerebral concussion. However, cerebral concussion was produced in each case
when the head of the monkey was subjected to
predominantly angular acceleration. Concussion was
assessed with reference to measures of the sensory
responses at the level of the cortical neuronal pool
(Gennarelli, Thibault and Ommaya, 1972).
Later work by Gennarelli et al. (1982) emphasized
the importance of the plane in which the angular
acceleration acts. They concluded that angular acceleration of the head causes axonal injury in the brain
proportional to the degree of coronal motion.
Ono et al. (1980), from the Japan Automobile
Research Institute and Jikei University Medical
School, conducted experiments on non-human primates to examine brain injury mechanisms. Their
observations were consistent with the conclusions of
Ommaya, Hirsch and Martinez (1966) and Gennarelli,
Thibault and Ommaya (1972) that an angular acceleration component must be present to induce brain
contusion in the sagittal plane. Ono et al. further
concluded that another important mechanism for the
occurrence of contusions is deformation of the skull as
governed by the contact area of the striker.
However, the results of these tests in Japan also
showed that the occurrence of concussion, as distinct
from brain contusion, in the monkeys could not be
correlated with angular acceleration but was highly
correlated with the linear acceleration of the head.
Their definition of the severity of concussion was
based on observation of the duration of apnea, loss of
the corneal reflex and blood pressure disturbances.
The acceleration/time curve marking the threshold for
skull fracture was found to lie above the corresponding tolerance curve for concussion (Figure 2.3).
These results were scaled from the monkeys head to
that of the human, using the technique of dimensional
analysis. The scaled results were validated by compar-

TOWARD AN UNDERSTANDING OF BRAIN INJURY MECHANISMS

Figure 2.3 JARI human head tolerance curve (JHTC).

(Source: reproduced from Ono et al., 1980, with permission.)

ing them with the acceleration/time curve for the

production of fracture in the human cadaver skull.
In a subsequent series of experiments in which the
animals head was subjected to lateral impact, Kikuchi,
Ono and Nakamura (1982) found that the acceleration/
time tolerance curve for concussion was higher than
the corresponding curve established for impacts that
accelerated the head in the sagittal plane. This finding
ran counter to the conclusion drawn by Gennarelli et al.
(1982) that the tolerance of the brain to acceleration, in
terms of duration of coma, was substantially less in the
coronal than in the sagittal plane.
Kikuchi, Ono and Nakamura acknowledged that
their results differed from the concept that lateral
impact to the head was more injurious than frontal or
occipital impact. They deduced that the difference
arose from the fact that the relative threshold levels for
skull fracture, brain concussion and various pathological brain injuries differ for impacts in the sagittal
and coronal planes.

33

Further investigations at the University of Pennsylvania by Thibault et al. led to the suggestion that a
single parameter, such as the value of the peak angular
acceleration, may not be an adequate predictor of the
deformation of the brain tissue and hence of the
severity of intracerebral injury (Thibault, Gennarelli
and Margulies, 1987). They proposed that the change
in angular velocity and possibly the total displacement may also be important parameters. This led on to
the development of a hypothesis by Margulies and
Thibault (1992) that the level of strain in the brain
tissue due to an impact to the head might be a function
of the peak change in rotational velocity, the peak
rotational acceleration and the mass of the head.
2.4.6

RELATIVE MOTION CONCEPT OF BRAIN INJURY

As mentioned previously, Holbourn (1943) argued

that rotational motion of the head was a significant
causal factor in the production of injury to the brain.
Pudenz and Sheldon (1946) were able to demonstrate
relative motion between the brain and the skull of the
monkey by means of a Lucite calvarium. They found
that the extent of such relative motion was influenced
by the direction of the impact to the head, being
greater in the sagittal than in the coronal plane.
The emphasis placed by many research workers on
rotational motion as a critical factor in the production of
injury to the brain is not universally accepted. For
example, Willinger et al. (1994) claim that knowledge of
the angular and linear components of the response of
the head to an impact is not a sufficient basis for accurate prediction of the mechanisms of any intracerebral
lesions. Applying the technique known as modal
analysis to the human head, both in vivo (Figure 2.4)

Figure 2.4 The signals measured by a load sensing hammer and an accelerometer (held against the head by the left forefinger)
are processed by modal analysis to determine the effective masses comprising the head (e.g. skull and brain) and their relative
motion for a given rate of change of acceleration of the head (which is related to the stiffness of the object struck).

34

BIOMECHANICS OF CLOSED HEAD INJURY

and in vitro, Willinger et al. (1992) have noted that measurement of the acceleration response to impact of the
head of the living human indicates that in an impact
with a hard object, such as a concrete floor, the brain
appears to move relative to the skull, whereas in an
impact with a relatively soft object, such as a sheet
metal panel of a car, the brain appears to move with the
skull.
This suggests that an impact with a hard object is
likely to be accompanied by peripheral injuries, such
as ruptured bridging veins, due to relative movement
between the brain and the skull. By comparison, when
the head hits a softer object the brain tends to move
with the skull and so it is subjected to similar forces,
and the resulting accelerations, to those acting on the
skull. An impact with a soft object is therefore likely
to be characterized by damage to the tissue deep
within the brain, such as axonal injury. The results
from modal analysis of the human head suggest that
these differences in the response of the brain to impact
are independent of the severity of the impact.
Willinger et al. (1992) demonstrated that this
hypothesis was consistent with the findings from the
detailed investigations conducted by the NHMRC
Road Accident Research Unit in Adelaide of cases of
impact to the head of the living human in road crashes
and falls.
Willinger later showed that the extensive series of
experiments on non-human primates conducted by
Gennarelli and Thibault to explore the sensitivity of
the brain to linear and angular acceleration also
yielded results that were consistent with his hypothesis (Willinger et al., 1994). He has therefore suggested
that the postulated roles of these two types of
acceleration in the causation of brain injury might
simply be a correlate of underlying differences in the
characteristics of the rate of change of the acceleration
of the head. Meaney, in commenting on Willingers
hypothesis, has noted that other factors, such as the
apparent dependence of the brain on the direction of
the applied force (or, resulting acceleration) may be
equally important in predicting the occurrence of
injury to the brain (Meaney, 1994).
Viano (1987) had earlier argued that acceleration,
per se, is not the cause of injury (to the brain). Rather
rapid motion of the skull causes displacement of the
hard bony structures of the head against the soft
tissues of the brain, which lag in their motion due to
inertia and loose coupling to the skull. This argument
differs from that of Willinger et al. (1992), who claim
that there is evidence from modal analysis that in
some impact situations the brain remains closely
coupled to the skull. At Vianos suggestion, a method
was developed to facilitate the comparison of the bony
anatomy of the cranial cavity with the presence or
absence of lesions on or near the surface of the brain

(McLean et al., 1990). However, apart from lesions

adjacent to skull fractures, there was no clear evidence
of a relationship between the shape of the cranial
cavity and lesions on the surface of the brain
(unpublished).
At the time of writing, the NHMRC Road Accident
Research Unit at the University of Adelaide is collaborating with the Bioengineering Center at Wayne State
University in a comparison of the pattern of brain
lesions observed in fatal road crashes with the strains
predicted in the brain using a three-dimensional finite
element model of the skull and brain subjected to
similar estimated impact conditions. If, in due course,
such a mathematical model can be validated it will be
possible to resolve many of the conflicting theories of
the mechanisms of impact injury to the brain.

2.5

Tolerance of the head to impact

Whatever the actual mechanism or mechanisms of

injury to the brain may be in cases of blunt impact to
the head, there is a need for some quantitative
measure relating characteristics of the impact to the
risk of head injury. The designer of a crash helmet, or
of those parts of a passenger car that are likely to be
struck by the head of an occupant, needs to know
what head acceleration levels are likely to result in
severe or fatal head injuries. Without such a measure,
or criterion, the development of devices aimed at
minimizing the severity of the head injury resulting
from a given impact can be based on little more than
an assumption that some of the energy of the impact
should be absorbed before it reaches the head.
The acceleration of the head has been, and continues
to be, used as a measure of the tolerance of the head to
impact. However, as noted above, the duration of the
impact is also related to the risk of a severe head
injury. Several measures have been developed in an
attempt to quantify the tolerance of the head to impact
in terms of the magnitude of both the resulting
acceleration of the head and the duration of the
impact. Of these, the Head Injury Criterion, commonly referred to by the acronym HIC, is by far the
most widely used. For the present purpose the
derivation of HIC is outlined as a basis for consideration of some of the criticisms which have been levied
against it. The discussion concludes with a review of
the reasons why HIC continues to be used, almost
universally, as the measure of the tolerance of the
brain to blunt impact to the head.
2.5.1

HIC: THE HEAD INJURY CRITERION

The first attempt to measure the tolerance of the head

to blunt impact was carried out by researchers at
Wayne State University in Detroit, notably Gurdjian

TOLERANCE OF THE HEAD TO IMPACT

and Lissner, from the 1940s through to the 1960s (see,

for example, Gurdjian and Lissner, 1944). As noted
earlier in this chapter, they subjected cadaver heads to
a blow to the forehead and related the linear acceleration of the head to whether or not the impact
produced fractures in the frontal bone. Eight skulls
were hit and the results of six of the eight cases were
plotted on a graph having the linear (straight line)
acceleration of the head on the vertical axis and time
(measured in milliseconds) on the horizontal axis
(McElhaney, Roberts and Hilyard, 1976). These points
mostly lay on that part of the curve (shown in Figure
2.2) which lies between about 1 ms and about 7 ms
after initial contact. Additional data points from other
experimental head impact studies on animals in which
the duration of the impact was longer were added
later, together with the results of cases in which
human volunteers were subjected to non-injurious
relatively low-level accelerations acting for a comparatively long time. The slope of the extended curve
approached the horizontal asymptotically after about
10 ms (Figure 2.2).
The curve defined by the data points from the
original cadaver studies, supplemented by the additional data, became known as the Wayne State
tolerance curve (Figure 2.2). It was thought to provide
an indication of the tolerance of the brain to impact, in
terms of the time history of the acceleration imparted
to the head. This was a considerable extrapolation
from the original tests, in which the outcome measure
had been simply the presence or absence of skull
fracture. The validity of the Wayne State tolerance
curve (WSTC) depended primarily on the assumption
that, if the skull of a living human was fractured, then
that injury would probably be accompanied by
concussion.
(a)

The Gadd Severity Index

In 1966, at the Stapp Car Crash Conference, Gadd of

General Motors proposed a head injury severity
index based on the Wayne State tolerance curve
(Gadd, 1966). Gadd reasoned that some measure of
the area under the acceleration/time curve for a
given impact could form the basis for such an index.
However it was apparent that a low level of acceleration lasting for a long time was not injurious whereas
a higher level of acceleration acting for a shorter time
was much more likely to be so, even though the area
under the acceleration/time curve could be the
same.
Gadd therefore decided to weight the area measure
in favor of the acceleration component. He did this by
raising the acceleration value to the power of 2.5. He
chose this number, 2.5, because it happened to be the
absolute slope of the Wayne State curve when plotted

35

on logarithmic axes. The mathematical expression for

the Gadd Severity Index (SI) is:
SI =

a

2.5

dt

where a is the effective acceleration (thought to have

been the average linear acceleration) of the head
measured in terms of g, the acceleration of gravity, and
t is the time in milliseconds from the start of the
impact.
The Gadd Severity Index or, as it was initially called,
the Severity Index, was thought by some still not to
deal adequately with long-duration, low-acceleration
impacts. In 1971, Versace, of the Ford Motor Company,
proposed a modification of the Gadd Severity Index,
which became known as the Head Injury Criterion
(HIC). The change was proposed to focus the severity
index on that part of the impact that was likely to be
relevant to the risk of injury to the brain. This was
done by averaging the integration of the resultant
acceleration/time curve over whatever time interval
yielded the maximum value of HIC. Because this
varies from one impact to another, the expression for
Versaces modified index simply refers to times t1 and
t2. The expression for HIC is:
HIC = (t2 t1 )

t2

a/(t2 t1 ) dt 2.5

t1

where an algorithm selects t1 and t2 to yield the

maximum value.
Since then, the desirability of restricting the time
interval (t2 t1) to as low as 15 ms has been noted to
avoid the possibility of obtaining high HIC values
from long-duration, low-acceleration cases (see, for
example, Prasad and Mertz, 1985).
After the analysis of impact accelerations experienced by American football players, human volunteer
impacts with air-bags and impact tests with windscreens, Hodgson and Thomas (1972) hypothesized
that a linear acceleration/time concussion tolerance
curve may not exist and that only impacts of very
short duration (e.g. with hard surfaces) may be
important. They suggested that if the impact does not
contain a critical HIC interval of less than 15 ms, the
impact should be considered safe. As noted above,
there is observational evidence that, in fact, head
injury without head contact is so rare that it is never
seen in the clinical setting (Tarriere, 1981; McLean,
1995).
HIC has been shown to relate well to the probability
that an impact will fracture the skull of a cadaver
(Hertz, 1994), which is perhaps not surprising given
the derivation of the original points on the Wayne
State curve. However, the Head Injury Criterion bears,
at best, a crude relationship to those factors now
thought to be important in brain injury causation.

36

BIOMECHANICS OF CLOSED HEAD INJURY

(b)

The JARI human head tolerance curve

Of the various other tolerance criteria which have

been proposed, the JARI human head tolerance curve
(Ono et al., 1980; Kikuchi, Ono and Nakamura, 1982)
is closest in general concept to the Wayne State curve.
The JARI tolerance curve is more soundly based than
the Wayne State tolerance curve but is nevertheless
almost identical to it. There are other head injury
criteria that have been proposed but, despite the
acknowledged inadequacies of HIC, it continues to
be by far the most widely used measure of the risk of
injury to the brain from a blunt impact to the head.
This is largely because it is specified in vehicle safety
legislation in the United States and also because there
is not yet any demonstrably superior criterion in
terms of relevance to the severity of head injury to
humans.

2.6 The state of the art of head injury

biomechanics
In conclusion, the following comment made by Goldsmith in 1981 is still a reasonable assessment of the
present situation: The state of knowledge concerning
trauma of the human head is so scant that the
community cannot agree on new and improved
criteria even though it is generally admitted that
present designations are not satisfactory.
Nevertheless, current work on mathematical models, when combined with the results of detailed
investigation of the response of the living human
brain to impact to the head, shows promise of
contributing substantially to our understanding of
brain injury mechanisms and the tolerance of the head
to impact.

2.7

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