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.

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

2.1
2.1.1

Impact to the head

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

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

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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.

(a)

Injury adjacent to the location of the impact

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.

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).

Injury remote from the location of the impact

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.

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

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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? 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).

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.

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

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

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

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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

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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

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

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 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.

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

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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.

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 2 200 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

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

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).

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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

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

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.)

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 acceleration deceleration 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

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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?

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

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.

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

33

Figure 2.3 JARI human head tolerance curve (JHTC). (Source: reproduced from Ono et al., 1980, with permission.)

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

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.

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 Willinger s 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

35

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

on logarithmic axes. The mathematical expression for the Gadd Severity Index (SI) is: SI =

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

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

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
(b)

BIOMECHANICS OF CLOSED HEAD INJURY

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

References

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responses to rotational and translational accelerations of the head, in Proceedings of the 16th Stapp Car Crash Conference, Society of Automotive Engineers, New York, pp. 296 308. Gennarelli, T. A., Thibault, L. E. and Tomei, G. (1987) Directional dependence of axonal brain injury due to centroidal and non-centroidal acceleration, in Proceedings of the 31st Stapp Car Crash Conference, Society of Automotive Engineers, Warrendale, PA, pp. 49 53. Gennarelli, T. A., Thibault, L. E., Adams, J. H. et al. (1982) Diffuse axonal injury and traumatic coma in the primate. Annals of Neurology, 12, 564 574. Gibson, T. J., McCaul, K. A., McLean, A. J. and Blumbergs, P. C. (1985) Investigation of head injury mechanisms in motor vehicle accidents a multidisciplinary approach. Society of Automotive Engineers Technical Paper Series 850093, Society of Automotive Engineers, Warrendale, PA. Goldsmith, W. (1981) Current controversies in the stipulation of head injury criteria letter to the editor. 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(1955) Observations on the mechanism of brain concussion, contusion and laceration, Surgery, Gynecology, and Obstetrics, 101, 680 690. Gurdjian, E. S., Lissner, H. R., Evans, F. G. et al. (1961) Intracranial pressure and acceleration accompanying head impacts in human cadavers. Surgery, Gynecology, and Obstetrics, 112, 185 190. Hertz, E. (1993) A note on the head injury criterion (HIC) as a predictor of the risk of skull fracture, in 37th Annual Proceedings of the Association for the Advancement of Automotive Medicine, Association for the Advancement of Automotive Medicine, Des Plaines, IL, pp. 303 312. Hirsch, A. E. and Ommaya, A. K. (1970) Protection from brain injury: the relative significance of translational and rotational motions of the head after impact, in Proceedings of the 14th Stapp Car Crash Conference, Society of Automotive Engineers, New York, pp. 144 151. Hodgson, V. R. and Thomas, L. M. (1972) Effect of long-duration impact on the head, in Proceedings of the 16th Stapp Car Crash Conference, Society of Automotive Engineers, New York, pp. 292 295. Hodgson, V. R., Thomas, L. M., Gurdjian, E. S. et al. (1969) Advances in understanding of experimental concussion mechanisms, in Proceedings of the 13th Stapp Car Crash Conference, Society of Automotive Engineers, New York, pp. 18 37. Holbourn, A. H. S. (1943) Mechanics of head injuries. Lancet, ii, 438 441. Kikuchi, A., Ono, K. and Nakamura, N. (1982) Human head tolerance to lateral impact deduced from experimental head injuries using primates, Society of Automotive Engineers Technical Paper Series 826035, Society of Automotive Engineers, Warrendale, PA. Lee, M. C. and Haut, R. C. (1989) Insensitivity of tensile failure properties of human bridging veins to strain rate: implications in biomechanics of subdural haematoma. Journal of Biomechanics, 22, 537 542. Lee, M. C., Melvin, J. W. and Ueno, K. (1987) Finite element analysis of traumatic subdural hematoma, in Proceedings of the 31st Stapp Car Crash Conference, Society of Automotive Engineers, Warrendale, PA, pp. 6777. Lissner, H. R., Lebow, M. and Evans, F. G. (1960) Experimental studies on the relation between acceleration and intracranial pressure changes in man. Surgery, Gynecology, and Obstetrics, 111, 329 338. McElhaney, J. H., Roberts, V. L. and Hilyard, F. (1976) Handbook of Human Tolerance, Japan Automobile Research Institute, Tsukuba, Japan. McLean, A. J. (1995) Brain injury without head impact? Journal of Neurotrauma, 12(4), 621 625. McLean, A. J., Blumbergs, P. C., Kloeden, C. N. et al. (1990) The relative motion concept of brain injury, in Proceedings of the International Research Council on the Biomechanics of Impacts, IRCOBI, Bron, France, pp. 181190. Margulies, S. S. and Thibault, L. E. (1992) A proposed tolerance criterion for diffuse axonal injury in man. Journal of Biomechanics, 25(8), 917 923. 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