2 BIOMECHANICS OF CLOSEDHEAD INJURY

A. J. McLean and Robert W. G. Anderson

This chapter discusses ways in which the brain isthought to be injured by a blunt impact to the head.The impacting object is assumed to be unlikely topenetrate the skull in the manner of a bullet, forexample.

The chapter is also concentrated on injuries to thebrain, rather than lacerations and abrasions to thescalp or fractures of the skull. Obviously, if the skull isfractured and displaced inwards, then the part of thebrain underlying the fracture will be injured. How-ever, the brain can be very severely injured withoutthe skull being fractured by the impact to the head(Gennarelli, 1980). Other intracranial injuries, such assubdural hematomas, are referred to briefly in relationto theories of mechanisms of primary injury to thebrain. Secondary complications of head injury alsoaffect the brain but they are not considered in thischapter.

2.1 Impact to the head

2.1.1 IMPACT AND IMPULSE

Closed head injury is, in the great majority of cases, aconsequence of an impact to the head. However, thereare references in the literature to the production ofdiffuse axonal injury in ‘non-impact’ experiments inwhich the head of an animal was accelerated in amanner that minimized the direct contact effects of animpact to the head (Gennarelli and Thibault, 1982;Adams, Graham and Gennarelli, 1981). There are alsoreports of brain injury resulting from acceleration ofthe upper torso of an animal without any directimpact to the head (Ommaya, Hirsch and Martinez,1966). These reports are discussed later in this chapter.For the present, the reader’s attention is drawn to thedistinction between an impact to the head and animpulse 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 contacteffects on the head, such as skull deformation orfracture, with an associated risk of injury to the brain.However, in practice it appears that injury to thehuman brain is almost always the result of an impactto the head, or to a protective helmet, rather than animpulse transmitted through the neck (Tarriere, 1981;McLean, 1995).

An impact to a given location on the head can becharacterized by the impact velocity and the physicalproperties of the struck or striking object.

2.1.2 IMPACT VELOCITY

Some forensic pathology research literature impliesthat the type of brain injury differs according towhether the head is stationary and is struck by amoving object, or is moving and strikes a stationaryobject (Yanagida, Fujiwara and Mizoi, 1989). Thisdistinction can be of considerable legal significance incases of assault in which the victim sustains a headinjury which could have been caused either by a blowto the head or from striking the head in the resultingfall. However, as Holbourn (1943) observed, themoving head typically strikes an object that is con-siderably more massive than the head, whereas thestationary head is more often hit by objects which areof similar mass to the head or even lighter, such as aclub.

In physical terms the difference between the headmoving or being stationary on impact is solely in theframe of reference. Most readers will have experiencedthe paradoxical sensation of not knowing which trainis moving when the train alongside theirs in thestation starts to move. There is no physical differencebetween the forces involved in a stationary head beinghit or a moving head striking a fixed object, given thatother factors such as the velocity of the impact and thecharacteristics of the object contacted by the head arethe 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 lessinterchangeably.

In general, the head impact velocity will be greaterin, say, high-speed crashes on the road than in crashesat low speed. However, that is not necessarily so. Thetype of crash is a significant factor, with high speedrollovers sometimes being relatively non-injuriouscompared to collisions with another vehicle or a fixedobject at a much lower speed. Even in two apparentlysimilar crashes it is not at all uncommon for a personin one crash to receive a severe impact to the headwhen a person in the other crash may not be hit on thehead at all.

2.1.3 PHYSICAL PROPERTIES OF THE STRUCK ORSTRIKING OBJECT

(a) Shape

As noted above, we have assumed that the impactingobject does not penetrate the skull in the manner of abullet, for example. The most important characteristicsof the struck or striking object are therefore its stiffnessand surface area, given that its shape is consistent withit imparting a blunt impact to the head.

(b) Stiffness

The term ‘stiffness’, as used here in the engineeringsense, is sometimes confused with hardness. Theproperty of stiffness is well illustrated by the compres-sion of a spring. The less the spring deflects under agiven load the stiffer it is said to be. By comparison, athin sheet of glass is very hard on the surface but itwill bend, or deflect, easily when loaded. It has a lowlevel of stiffness, which, of course, decreases abruptlyto zero when the glass breaks.

A concrete floor is extremely stiff; almost infinitelyso in relation to the human head. A sheet metal panelof a car, however, may be deformed several cen-timeters when struck by the head of a pedestrian or anoccupant of the car. Such differences in stiffness of theobject struck by the head have been shown to beassociated with differences in the type of the resultingintracranial 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 relatedto brain injury in a number of ways: such as by localdeformation of the skull and, more importantly, bydetermining the relative levels of linear and angularacceleration of the head.

(a) Injury adjacent to the location of the impact

Local deformation of the skull at the point of impactcan be expected to result in direct contact injury to theunderlying brain tissue. This almost inevitably occursif the impact produces a displaced fracture of theskull, but high-speed cine radiography has shown thatthe skull can also be indented sufficiently in the firstfew milliseconds of the impact to compress theunderlying brain and then return to its original shapewithout residual evidence of such deformation in thebone (Gurdjian, 1972; Shatsky et al., 1974).

Shatsky et al. (1974), in their studies using anesthe-tized monkeys, showed that in occipital impacts theskull was not deformed and no underlying brainlesions were observed. Impacts in the temporoparietalregion did show evidence of transient skull deforma-tion and accompanying brain lesions. For a givenimpact, the risk of underlying skull fracture will alsovary with the location of the impact on the head.Nahum et al. (1968) estimated that for a contact area ofapproximately 1 square inch (6.5 cm2) the forcerequired to produce a clinically significant skullfracture in the frontal area of the cadaver skull wastwice that required in the temporoparietal area.

(b) 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 forinjuries to both the skull and the brain. A blunt impactto the calvarium may result in remote linear fracturesin the base of the skull. This is thought to be aconsequence of the skull cap being strong enough towithstand the force of the impact, which is thereforetransmitted to the much thinner bone found in parts ofthe base of the skull. However, once a remote linearfracture has been initiated in such a region, it canpropagate almost instantly back into the calvariumwhich is still loaded by the force of the impact (Melvinand Evans, 1971).

The term ‘contrecoup’ has long been used tocharacterize an injury to the brain which is on the farside of the head to the impact. It has been postulatedthat contrecoup injury to the brain is a consequenceof rapid and localized pressure changes near thesurface of the brain tissue due to cavitation effectsarising from the brain moving relative to the cranialcavity in response to the impact (Courville, 1942).However, Nusholtz et al. (1984) reported that, inoccipital impacts to the head of the Rhesus monkey,contrecoup negative pressures greater than oneatmosphere did not appear to be associated withinjury to the brain.

In the case of an occipital impact it is possible thatrelative motion between the brain and the often

RESPONSE OF THE HEAD TO IMPACT 27

irregular bony anatomy of the anterior fossa in thehuman may play a role in the causation of contrecoupinjury to the brain (Shatsky et al., 1974).

(c) Head impact location and brain injury severity

Finally, the location of the impact to the head candetermine the nature, pattern and severity of injurythroughout the brain. More than 200 years agoPercivall Pott, Surgeon of the City of London,remarked upon an apparent relationship betweenimpact location on the head and the severity of theresulting brain injury:

I will not assert it to be a general fact, but as faras my own experience and observation go, Ithink that I have seen more patients get well,whose injuries have been in or under the frontalbone, than any other bones of the cranium. If thisshould be found to be generally true, may notthe reason be worth inquiring into?

The Chirurgical Works of Percivall Pott, FRS, 1779

Some 200 years later this matter has been inquired intoand the results are consistent with Percivall Pott’s‘experience and observation’. For example, the experi-mental work of Gennarelli, Thibault and Tomei (1987)on subhuman primates demonstrated that a combina-tion of linear and angular acceleration of the head inthe coronal plane (rotation of the head about a point inthe cervical spine, somewhat analogous to the motionresulting from a lateral impact to the head) was moreinjurious to the brain than similar acceleration in thesagittal plane (as in a frontal impact). The results ofdetailed investigation of a small number of cases offatal and severe head injury to car occupants were alsoconsistent with frontal impact to the head being lessinjurious to the brain than lateral impact (Simpson etal., 1991). However, animal experiments conducted inJapan, discussed later in this chapter, indicate that therelationship between impacts in the sagittal andcoronal planes and injury to the brain may beconsiderably more complex than is commonly sup-posed (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 theseverity of the resulting injury is whether or not thehead is free to move in response to the impact.

2.2.1 MOVEMENT OF THE HEAD

The mechanism of injury to the head depends onwhether or not the head is free to change its velocitywhen struck (Denny-Brown and Russell, 1941). If it is

not, the skull may be crushed to a greater or lesserdegree and the injury to the head, and the brain, willbe directly related to the location and extent of theskull deformation. An example of such an impactwould be a masonry block falling on the head of aperson lying on a concrete floor.

As noted above, most cases of closed head injuryresult from a moving head coming into contact witha stationary object or with an object moving at adifferent velocity. Injuries to the brain are generallythought to result from the acceleration of the brain inresponse to the impact to the head, with the excep-tion of direct contact injuries resulting from skullfracture or motion of the brain relative to the cranialcavity. The term ‘acceleration’ is used here in theabsolute sense to refer both to cases in which thestationary head is accelerated by an impacting objectand to cases in which the moving head is deceleratedwhen it hits a stationary object, or one moving at alower velocity.

2.2.2 THE FORCE OF THE IMPACT

For a given head impact velocity, an impact with asheet metal panel of a car will result in a much smallerimpact force, and hence lower acceleration of thehead, than will an impact with a concrete floor. This isbecause the moving head is brought to rest over agreater distance in the former case, as indicated by theconsiderable dent which is often seen in the panelfollowing a head impact. However, the lower accelera-tion means that the impact force, albeit at a lowerlevel, is acting on the head for a longer time.

As will be seen later, there is reason to believe thatthe sensitivity of the brain to injury from an impact tothe head is time-dependent. A very high level ofacceleration of the head acting for a very short timemay be less injurious than a lower level of accelerationacting over a relatively longer time period.

2.2.3 LINEAR AND ANGULAR ACCELERATION OFTHE HEAD

If the line of action (the vector) of the impact forcepasses through the center of gravity of the head thenthe head will be accelerated in a straight line. In otherwords, it will be subjected to a linear acceleration. Thisgeneral statement ignores any restraining effect of theneck, which is likely to be small in the time intervalduring which injury to the brain is thought to occur.However, if the force vector does not pass through thecenter of gravity then the head will be subjected toboth linear and angular acceleration, with the latterresulting in rotation about the center of gravity. In thischapter the terms ‘rotational’ and ‘angular’ are used

28 BIOMECHANICS OF CLOSED HEAD INJURY

interchangeably. In some research papers a distinctionhas been made between these two terms by definingthe former to mean rotation about the center of gravityof the head and the latter to refer to rotation of thehead about some other point, such as in the cervicalspine, which results in a combination of linear andangular motion of the center of gravity of the head.

The basic relationship between the force of theimpact and the resulting angular acceleration (�) ofthe head is similar to that for linear acceleration exceptthat the offset (x) of the force vector from the center ofgravity of the head is taken into account along withthe moment of inertia (I) of the head:

F x = I �.

The moment of inertia of a solid sphere, a very crudeapproximation to the human head, about an axisthrough the center of the sphere is:

I = 2/5 m r2.

The force changes during the impact and so themagnitude of the angular acceleration will changewith time during the impact.

If the human head was spherical, with its center ofgravity at the center of the sphere, then the forcevector of an impact perpendicular to the surfacewould always pass through the center of gravity.However, the human head is far from spherical andso, for an impact perpendicular to the surface of theskull, the distance of the force vector from the center ofgravity varies with the location of the impact on thehead. In general, regardless of differences in headshape, the vector of an impact on the side of thehead is likely to be offset more from the center ofgravity than that of an impact on the frontal bone orthe occiput.

However, the human head does come in a widerange of shapes and it is conceivable that the range ofthis variability may be sufficient to influence theresponse of the head to impact and hence the natureand/or severity of the resulting injury to the brain(McLean et al., 1990). For example, the force vector ofa lateral impact to the side of the frontal bone of a longnarrow head is likely to have a greater offset from thecenter of gravity of the head than is a similar impact toa rounder head, both viewed in the horizontal plane.

In practice, most impacts to the head will pocketinto the scalp to some degree. This may result in theforce vector not being at 90° to the surface of the skull,which, in turn, will affect the distance between theforce vector and the center of gravity of the head.However, any variation arising in this way is unlikelyto affect the general relationship between impacts onthe side of the head and greater offsets of the forcevector from the center of gravity. This means that, fora given impact severity, lateral impacts are likely to

result in a higher level of angular acceleration of thehead than are frontal or occipital impacts (see, forexample, Vilenius et al., 1994).

If the level of angular acceleration increases with achange in the location of the impact on the head, thisincrease will be accompanied by a decrease in the levelof linear acceleration and vice versa. While it is possibleto envisage an impact to the head, such as an occipitalimpact or one to the frontal bone, producing onlylinear acceleration, it is most unlikely that any realisticimpact to the head will produce only angular accelera-tion about the center of gravity.

2.2.4 STRESS AND STRAIN

Stress (tensile or compressive) is measured in terms offorce per unit area. Strain describes the response ofthe material which is being stressed. It is measured interms of the proportional change in length in thedirection of the tensile or compressive stress: hencereference to, for example, a 10% strain. A compressivestrain will, of course, indicate a reduction in length,whereas a tensile strain will indicate that the stressedmaterial has been stretched.

Another type of stress, and associated strain, whichis thought to be particularly relevant to injury to thebrain results from the action of a shear force. The effectsof shear stress are illustrated by the action of a pair ofscissors, or shears, cutting a thin stack of sheets ofpaper. Shear stress is also measured in terms of forceper unit area but the area is measured in the plane inwhich the force is acting (at right angles to the face ofthe sheets of paper in the example given here).Similarly, shear strain is the proportional displacement,expressed in terms of the original thickness, resultingfrom the action of the shear force.

(a) Strain rate

The rate of application of a force is reflected in the rateof the resulting strain, expressed in terms of strain perunit of time. The response to physical loading of somebiological materials is strain-rate-dependent (Vianoand Lau, 1988).

2.3 Methods of investigation

Three types of investigative method have been used inthe study of brain injury biomechanics: experimental,mathematical and observational.

2.3.1 EXPERIMENTAL STUDIES

Much of what is known, or postulated, about braininjury mechanisms in living humans has come fromexperimental studies. Test subjects have included

TOWARD AN UNDERSTANDING OF BRAIN INJURY MECHANISMS 29

human cadavers, anesthetized animals and animalcadavers. Physical models of the head have also beenused. Experiments conducted on living humans havedefined the response of the head to non-injuriousimpact.

The human cadaver head has the advantage of validanatomical, but not physiological, representation ofthe head of the living human (although attempts havebeen made to simulate vascular lesions by pressuriz-ing the vascular system prior to impacting the head).The anesthetized animal is, of course, a living subjectbut differs anatomically from the human. Highlysophisticated experimental techniques have beendeveloped in the course of the evolution of animal-based head injury studies (see, for example, Nusholtz,Kaiker and Lehman, 1986). Although the anatomicaldifferences are least in the non-human primate, thesmaller size of the monkey skull and brain introduceproblems of dimensional scaling in attempts to relatethe results to the living human.

Experiments using physical models of the brain, orskull and brain, have included measurements ofstrain, recorded by measuring the distortion of animpregnated grid or by photoelastic means, in accel-erated gel-filled containers (Thibault, Gennarelli andMargulies, 1987; Holbourn, 1943).

2.3.2 MATHEMATICAL STUDIES

Mathematical models of human and animal heads arenow at the stage which, with the ready availability ofpowerful computers, justifies their use in attempts topredict the likely impact-induced motion of the brainrelative to the skull and strains within the brain tissue(Zhou, Khalil and King, 1994). The development of arealistic mathematical model depends, inter alia, onknowledge of the physical response of brain tissue toimpact loading, in addition to the response of the skulland membranes (Melvin, Lighthall and Ueno, 1993).

Experimental data are available for use in thevalidation of mathematical models of the animalskull/brain system. Validation of mathematical mod-els of the human head depends on the availability ofadequately detailed and accurate estimates of theforces involved in impacts to the head of the livinghuman in events such as road crashes and theresulting pathology, particularly the neuropathology.

2.3.3 OBSERVATIONAL STUDIES

The investigation of cases in which living humanshave sustained a closed head injury has the desirableattribute that the phenomenon being investigated isexactly that which is of interest. However, it is difficultto obtain adequately detailed information on thecharacteristics of the injury to the brain, and the

severity of the impact to the head can only beestimated (Ryan et al., 1989; Gibson et al., 1985).

(a) Neuropathology

In fatal cases the neuropathologist can provide infor-mation on injury to the brain at the microscopic level.Even so, there are limitations imposed by the fact thatsome brain lesions are not at present readily detectableunless the fatally injured individual survives for somehours after the incident which produced the injury. Insurviving cases, magnetic resonance imaging (MRI)and computed tomography (CT) can be used toidentify and locate larger hemorrhagic lesions in thebrain.

(b) Characteristics of the impact to the head

The location of the impact on the head can bedetermined from the location of abrasions and contu-sions, depressed skull fractures and subgaleal hemato-mas at autopsy or in operative cases. In non-fatal casesit can be difficult to determine the location of animpact above the hairline.

Determining the object or objects struck by the headusually depends on examining the setting in whichthe injury occurred, such as the vehicle involved andthe crash site in the case of a road accident. Thestiffness of the struck object may be able to be deducedfrom a simple description of the event, such as thehead striking a concrete floor as the result of a fall. Ina road crash the head impact is most likely to havebeen with some part of the vehicle. Knowledge of thestiffness of the struck part of the vehicle can be used toestimate the force of the head impact, assuming that areasonably accurate estimate can be made of thevelocity with which the head struck the object. If arecord has been made of any residual deformation ofthe struck object, an instrumented headform can beused to measure the force required to reproduce thedent observed in the actual impact.

2.4 Toward an understanding of braininjury mechanismsThe study of the biomechanics of head injury has beenconcentrated on the relationship between the forcesapplied to the head and the resulting injury to thebrain. Some of the earlier studies used the presence orabsence of skull fracture as the outcome variable,assuming that it would be positively related to theseverity of brain injury (see the following section onthe impact tolerance of the head). However, it wassoon recognized that the response of the whole headto impact was likely to be the main determinant of thenature and severity of injury to the brain.

30 BIOMECHANICS OF CLOSED HEAD INJURY

2.4.1 SETTING THE SCENE

The work of Holbourn (1943), a research physicist inthe University Department of Surgery in Oxford, UK,set the scene for what has been the most widelyaccepted theory of the mechanism of injury to thebrain: that rotational motion of the head is thepredominant causal factor.

Reasoning that the brain was effectively incom-pressible, Holbourn hypothesized that linear accelera-tion of the head could not deform the brain and so wasunlikely to result in injury to the brain tissue. Angularacceleration, however, could be expected to set upshear strains in the brain, and the relative displace-ment within the brain that is implied by the creation ofsuch strains would be expected to be a cause ofinjury.

The bowl of porridge analogy is sometimes used toillustrate Holbourn’s hypothesis (Figure 2.1).

If the stationary bowl is suddenly moved sideways(linear acceleration) there will be no appearance ofrelative motion in the porridge (apart from spillingover the side, which is not possible with a closedvessel such as the cranial cavity). If, however, the bowlis rotated rapidly (angular acceleration), that part ofthe porridge adjacent to the bowl will tend to movewith the bowl and the porridge in the center will tendto remain stationary. This can only happen if there isrelative motion (shear strains) within the porridge.

Holbourn tested his hypothesis using the physicalmodel referred to above: a gel-filled two dimensionalmodel of the human head. The strains produced in thegel by acceleration of the model in that plane wererevealed by photoelastic techniques. As he predicted,the model was relatively insensitive to linear accelera-tion but the pattern of strains produced by angularacceleration could readily be demonstrated.

The other observation which he made was that for‘very short blows’ the duration of application of theaccelerating force was an important factor in theproduction of shear strains in his model brain,whereas for ‘blows of long duration’ the levels ofshear strain were independent of the time for whichthe force acts. The change from ‘short’ to ‘long’duration was estimated to occur somewhere in therange 2–200 ms (Holbourn, 1943). He also noted thatinterposing a deformable object, such as a crashhelmet, between the blow and the head has the effectof extending the duration of the impact and therebyreducing the average level of the force transmitted tothe head (Cairns and Holbourn, 1943).

Some 20 years elapsed before Holbourn’s hypoth-esis that angular acceleration of the head was likely tobe much more injurious to the brain than linearacceleration was followed up by other investigators.One very practical reason for this was that it was arelatively straightforward matter to measure linearacceleration but techniques to measure the angularacceleration of the head in animal experiments werenot available.

2.4.2 THE WAYNE STATE TOLERANCE CURVE

At the same time that Holbourn was conducting hisexperiments on physical models in England, Gurdjianand Webster (1943) commenced studies at Wayne StateUniversity in Detroit on the effect of impacts admin-istered 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 ofbrain concussion, contusion, and laceration’ (Gurdj-ian, Webster and Lissner, 1955). By applying airpressure directly to the unopened dural sac forvarious time periods they were able to show that theseverity of the concussive effect depended on both theintensity of the pressure pulse and the duration of itsapplication. They concluded that ‘Concussion occursas the result of brain stem injury either from increasedintracranial pressure at the time of impact, directinjury by distortion, mass movement, shearing, ordestruction by a missile’. Brief reference was made tothe possibility that rotation of the head might result inthe brain being injured by ‘abutting against bonyprojections within the skull’.

Gurdjian and Lissner then conducted studies on aphysical model similar to Holbourn’s, but with theinclusion of a simulation of the foramen magnum andbrain stem. These studies led them to conclude that‘the mechanism of concussion is shear strain in thebrain stem caused by pressure gradients due to closedsystem dynamics of impact’ (Gurdjian and Lissner,1961).

Figure 2.1 Angular acceleration (�̇) of the bowl producesshear strains in the contents, as illustrated by the layerssliding across each other.

•

TOWARD AN UNDERSTANDING OF BRAIN INJURY MECHANISMS 31

Lissner, Lebow and Evans (1960) also investigatedthe relation between linear acceleration and intra-cranial pressure changes resulting from impacts to thefrontal bone of the embalmed human cadaver head.The report on this work became notable for what wasalmost a passing reference to the acceleration requiredto produce a linear fracture of the frontal bone. Theplot of these results (Figure 2.2), later supplementedby other data (Gurdjian et al., 1961), formed the basisfor the development of the Head Injury Criterion,which is used almost universally today as the measureof the risk of head injury in automobile crash injurytesting. This work, and the Head Injury Criterion, arediscussed at greater length in section 2.5.1.

Further investigations at Wayne State Universitythrough the 1960s included occipital impacts to thefreely moving head of the anesthetized stumptailmonkey. In reporting on those experiments Hodgsonet al. (1969) commented that their results supportedthe theory of Gurdjian and Lissner (1961). In partic-ular, Hodgson et al. concluded that ‘Although themotion of the head involved both angular andtranslational acceleration, the preponderance of affec-ted cells found in the brain stem and the almostcomplete absence of chromatolysis in the cortex,makes it appear likely that translational acceleration isthe most important mechanism’ (Hodgson et al.,1969).

However, in other studies of head injury mecha-nisms conducted in the 1960s, Ommaya and Hirschshowed that in studies of whiplash injury the provi-sion of a cervical collar neck support for monkeyssubjected to whole body acceleration almost elimi-nated the cases of concussion that were observedwhen the head was free to rotate (Ommaya, Hirschand Martinez, 1966). In 1970, on the basis of further

analysis of the results of these studies, they concludedthat ‘no convincing evidence has to this date beenpresented which relates brain injury and concussion totranslational motion of the head for short durationforce inputs, whether through whiplash or directimpact’ (Hirsch and Ommaya, 1970).

2.4.3 FURTHER DEVELOPMENT OF EXPERIMENTSUSING HUMAN SURROGATES

In the early 1970s, Ommaya initiated work withGennarelli and Thibault on a series of head impactexperiments using monkeys (This work was latercontinued by Gennarelli and Thibault at the Uni-versity of Pennsylvania, in collaboration with Adams,and then Graham, from the Institute for NeurologicalSciences in Glasgow.) They subjected the head of theanimal to predominately linear or angular accelerationin a defined plane while at the same time minimizingthe direct contact effects of the impact on the head.This was done by encasing the monkey’s head in arigid skull cap and filling the space remainingbetween the head and the cap with dental cement. Theskull cap was attached via a mechanical linkage to apiston which, when actuated, accelerated the head(Gennarelli and Thibault, 1982).

The rationale for attempting to minimize contacteffects of an impact to the head is clear. However, asGennarelli (1980) has noted, in the human thereappears to be little relationship between the presenceor absence of skull fracture and the severity of injuryto the brain. This could be interpreted to mean that theconcentrated forces of a localized impact act on thebrain in much the same way as the more uniformlydistributed forces of an impulse applied to the head asa whole, apart from brain lesions due to localdeformation of the skull at the point of impact.

The linkage attached to the rigid skull cap con-strained the motion of the head to a single plane withthe head rotating about a point in the region of thelower part of the cervical spine. The movement of thehead was limited to an arc of 60° before the motionwas abruptly stopped. As the level of acceleration waslower than the level of deceleration it was claimed thatthe injurious event was the deceleration, althoughthere does seem to be reason to be concerned about theinjury potential of the acceleration phase. Physicalmodels subjected to the sequential acceleration–decel-eration pulses showed marked distortion (strain) inthe ‘brain’ tissue during the acceleration phase (Thi-bault, Gennarelli and Margulies, 1987; Margulies,Thibault and Gennarelli, 1990).

Gennarelli and Thibault (1982) did find that to beable to continue to produce subdural hematomaswhen they increased the duration of the decelerationphase they also had to increase the level of the

Figure 2.2 The Wayne State tolerance curve. Points belowthe curve are unlikely to be associated with severe braininjury. (Source: reproduced from Gurdjian, Roberts andThomas, 1966, with permission.)

32 BIOMECHANICS OF CLOSED HEAD INJURY

deceleration itself. This contrasted with their findingthat axonal injury and concussion could be producedat lower deceleration levels when the duration of thedeceleration phase was increased, a result which wasconsistent with the acceleration/time relationshipshown in the Wayne State tolerance curve (Figure 2.2).Their explanation for this difference was that thebridging veins are sensitive to the rate at which theacceleration is applied. However, there is now evi-dence that the bridging veins are not strain-rate-sensitive (Lee and Haut, 1989).

Lee, Melvin and Ueno (1987), working with a two-dimensional finite element model of the brain of theRhesus monkey, concluded that the subdural hemato-mas may actually have been produced during theacceleration phase of the biphasic test device devel-oped by Thibault and Gennarelli. This is because anyincrease in the duration of the deceleration phase hadto be accompanied by a corresponding decrease in theduration of the acceleration phase, and hence anincrease in the level of the acceleration was necessaryto maintain a given level of deceleration.

2.4.4 BRAIN INJURY WITHOUT HEAD IMPACT?

In many of the publications on this very extensiveseries of experiments at the University of Pennsylva-nia, 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). Theintent may have been to draw attention to the fact thatcontact phenomena, such as deformation of the skull,were minimized by distributing the accelerative loadover a wide area of the head. A motorcyclist’s crashhelmet performs a similar function, while also absorb-ing some of the energy of the impact.

However, the term ‘non-impact’ can, of course, beinterpreted to mean that the head was not subjected toan impact. Such an interpretation can be a matter ofconsiderable forensic significance. For example, incases of alleged child abuse it is not uncommon for thedefense to allege that the infant was shaken vigor-ously rather than the head being struck by, or against,some object. The probable validity of such an assertionwas investigated by Duhaime et al. (1987) whoconcluded that vigorous shaking of the torso of aninfant was most unlikely to result in injury to thechild’s brain in the absence of an impact to the head.They estimated that the head acceleration level pro-duced by such shaking was probably about one-50thof the level resulting from an impact. This finding isconsistent with the results from our investigation ofbrain injury in road crashes, although the force whichcan be imparted to the torso, and hence to the head, byan adult shaking an infant is likely to be considerablyless than can occur in a road crash.

Meaney, Thibault and Gennarelli (1994), at theUniversity of Pennsylvania, used a mathematicalmodel of the human body to investigate the likelihoodof that occurring to a car occupant subjected to asevere lateral impact. They concluded that the accel-eration of the head is unlikely to reach a level whichwould be injurious to the brain. This is consistent withMcLean’s finding, referred to earlier, that there wereno cases of brain injury without head impact in aseries of more than 400 fatally injured road users(McLean, 1995).

2.4.5 THE ROLE OF LINEAR AND ANGULARACCELERATION

Ommaya and Gennarelli (1974) reported that linearacceleration of the head of the squirrel monkey in thesagittal plane was associated with focal lesions butwas unlikely to produce cerebral concussion. How-ever, cerebral concussion was produced in each casewhen the head of the monkey was subjected topredominantly angular acceleration. Concussion wasassessed with reference to measures of the sensoryresponses at the level of the cortical neuronal pool(Gennarelli, Thibault and Ommaya, 1972).

Later work by Gennarelli et al. (1982) emphasizedthe importance of the plane in which the angularacceleration acts. They concluded that ‘angular accel-eration of the head causes axonal injury in the brainproportional to the degree of coronal motion’.

Ono et al. (1980), from the Japan AutomobileResearch Institute and Jikei University MedicalSchool, conducted experiments on non-human pri-mates to examine brain injury mechanisms. Theirobservations were consistent with the conclusions ofOmmaya, Hirsch and Martinez (1966) and Gennarelli,Thibault and Ommaya (1972) that an angular accelera-tion component must be present to induce braincontusion in the sagittal plane. Ono et al. furtherconcluded that another important mechanism for theoccurrence of contusions is deformation of the skull asgoverned by the contact area of the striker.

However, the results of these tests in Japan alsoshowed that the occurrence of concussion, as distinctfrom brain contusion, in the monkeys could not becorrelated with angular acceleration but was highlycorrelated with the linear acceleration of the head.Their definition of the severity of concussion wasbased on observation of the duration of apnea, loss ofthe corneal reflex and blood pressure disturbances.The acceleration/time curve marking the threshold forskull fracture was found to lie above the correspond-ing tolerance curve for concussion (Figure 2.3).

These results were scaled from the monkey’s head tothat of the human, using the technique of dimensionalanalysis. The scaled results were validated by compar-

TOWARD AN UNDERSTANDING OF BRAIN INJURY MECHANISMS 33

ing them with the acceleration/time curve for theproduction of fracture in the human cadaver skull.

In a subsequent series of experiments in which theanimal’s head was subjected to lateral impact, Kikuchi,Ono and Nakamura (1982) found that the acceleration/time tolerance curve for concussion was higher thanthe corresponding curve established for impacts thataccelerated the head in the sagittal plane. This findingran counter to the conclusion drawn by Gennarelli et al.(1982) that the tolerance of the brain to acceleration, interms of duration of coma, was substantially less in thecoronal than in the sagittal plane.

Kikuchi, Ono and Nakamura acknowledged thattheir results differed from the concept that lateralimpact to the head was more injurious than frontal oroccipital impact. They deduced that the differencearose from the fact that the relative threshold levels forskull fracture, brain concussion and various patho-logical brain injuries differ for impacts in the sagittaland coronal planes.

Further investigations at the University of Pennsyl-vania by Thibault et al. led to the suggestion that asingle parameter, such as the value of the peak angularacceleration, may not be an adequate predictor of thedeformation of the brain tissue and hence of theseverity of intracerebral injury (Thibault, Gennarelliand Margulies, 1987). They proposed that the changein angular velocity and possibly the total displace-ment may also be important parameters. This led on tothe development of a hypothesis by Margulies andThibault (1992) that the level of strain in the braintissue due to an impact to the head might be a functionof the peak change in rotational velocity, the peakrotational acceleration and the mass of the head.

2.4.6 RELATIVE MOTION CONCEPT OF BRAIN INJURY

As mentioned previously, Holbourn (1943) arguedthat rotational motion of the head was a significantcausal factor in the production of injury to the brain.Pudenz and Sheldon (1946) were able to demonstraterelative motion between the brain and the skull of themonkey by means of a Lucite calvarium. They foundthat the extent of such relative motion was influencedby the direction of the impact to the head, beinggreater in the sagittal than in the coronal plane.

The emphasis placed by many research workers onrotational motion as a critical factor in the production ofinjury to the brain is not universally accepted. Forexample, Willinger et al. (1994) claim that knowledge ofthe angular and linear components of the response ofthe head to an impact is not a sufficient basis for accu-rate prediction of the mechanisms of any intracerebrallesions. Applying the technique known as modalanalysis to the human head, both in vivo (Figure 2.4)

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

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 relativemotion 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 meas-urement of the acceleration response to impact of thehead of the living human indicates that in an impactwith a hard object, such as a concrete floor, the brainappears to move relative to the skull, whereas in animpact with a relatively soft object, such as a sheetmetal panel of a car, the brain appears to move with theskull.

This suggests that an impact with a hard object islikely to be accompanied by peripheral injuries, suchas ruptured bridging veins, due to relative movementbetween the brain and the skull. By comparison, whenthe head hits a softer object the brain tends to movewith the skull and so it is subjected to similar forces,and the resulting accelerations, to those acting on theskull. An impact with a ‘soft’ object is therefore likelyto be characterized by damage to the tissue deepwithin the brain, such as axonal injury. The resultsfrom modal analysis of the human head suggest thatthese differences in the response of the brain to impactare independent of the severity of the impact.

Willinger et al. (1992) demonstrated that thishypothesis was consistent with the findings from thedetailed investigations conducted by the NHMRCRoad Accident Research Unit in Adelaide of cases ofimpact to the head of the living human in road crashesand falls.

Willinger later showed that the extensive series ofexperiments on non-human primates conducted byGennarelli and Thibault to explore the sensitivity ofthe brain to linear and angular acceleration alsoyielded results that were consistent with his hypoth-esis (Willinger et al., 1994). He has therefore suggestedthat the postulated roles of these two types ofacceleration in the causation of brain injury mightsimply be a correlate of underlying differences in thecharacteristics of the rate of change of the accelerationof the head. Meaney, in commenting on Willinger’shypothesis, has noted that other factors, such as theapparent dependence of the brain on the direction ofthe applied force (or, resulting acceleration) may beequally important in predicting the occurrence ofinjury to the brain (Meaney, 1994).

Viano (1987) had earlier argued that ‘acceleration,per se, is not the cause of injury’ (to the brain). ‘Ratherrapid motion of the skull causes displacement of thehard bony structures of the head against the softtissues of the brain, which lag in their motion due toinertia and loose coupling to the skull’. This argumentdiffers from that of Willinger et al. (1992), who claimthat there is evidence from modal analysis that insome impact situations the brain remains closelycoupled to the skull. At Viano’s suggestion, a methodwas developed to facilitate the comparison of the bonyanatomy of the cranial cavity with the presence orabsence of lesions on or near the surface of the brain

(McLean et al., 1990). However, apart from lesionsadjacent to skull fractures, there was no clear evidenceof a relationship between the shape of the cranialcavity and lesions on the surface of the brain(unpublished).

At the time of writing, the NHMRC Road AccidentResearch Unit at the University of Adelaide is collabo-rating with the Bioengineering Center at Wayne StateUniversity in a comparison of the pattern of brainlesions observed in fatal road crashes with the strainspredicted in the brain using a three-dimensional finiteelement model of the skull and brain subjected tosimilar estimated impact conditions. If, in due course,such a mathematical model can be validated it will bepossible to resolve many of the conflicting theories ofthe mechanisms of impact injury to the brain.

2.5 Tolerance of the head to impact

Whatever the actual mechanism or mechanisms ofinjury to the brain may be in cases of blunt impact tothe head, there is a need for some quantitativemeasure relating characteristics of the impact to therisk of head injury. The designer of a crash helmet, orof those parts of a passenger car that are likely to bestruck by the head of an occupant, needs to knowwhat head acceleration levels are likely to result insevere or fatal head injuries. Without such a measure,or criterion, the development of devices aimed atminimizing the severity of the head injury resultingfrom a given impact can be based on little more thanan assumption that some of the energy of the impactshould be absorbed before it reaches the head.

The acceleration of the head has been, and continuesto be, used as a measure of the tolerance of the head toimpact. However, as noted above, the duration of theimpact is also related to the risk of a severe headinjury. Several measures have been developed in anattempt to quantify the tolerance of the head to impactin terms of the magnitude of both the resultingacceleration of the head and the duration of theimpact. Of these, the Head Injury Criterion, com-monly referred to by the acronym HIC, is by far themost widely used. For the present purpose thederivation of HIC is outlined as a basis for considera-tion of some of the criticisms which have been leviedagainst it. The discussion concludes with a review ofthe reasons why HIC continues to be used, almostuniversally, as the measure of the tolerance of thebrain to blunt impact to the head.

2.5.1 HIC: THE HEAD INJURY CRITERION

The first attempt to measure the tolerance of the headto blunt impact was carried out by researchers atWayne 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 notedearlier in this chapter, they subjected cadaver heads toa blow to the forehead and related the linear accelera-tion of the head to whether or not the impactproduced fractures in the frontal bone. Eight skullswere hit and the results of six of the eight cases wereplotted 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 pointsmostly lay on that part of the curve (shown in Figure2.2) which lies between about 1 ms and about 7 msafter initial contact. Additional data points from otherexperimental head impact studies on animals in whichthe duration of the impact was longer were addedlater, together with the results of cases in whichhuman volunteers were subjected to non-injuriousrelatively low-level accelerations acting for a compar-atively long time. The slope of the extended curveapproached the horizontal asymptotically after about10 ms (Figure 2.2).

The curve defined by the data points from theoriginal cadaver studies, supplemented by the addi-tional data, became known as the Wayne Statetolerance curve (Figure 2.2). It was thought to providean indication of the tolerance of the brain to impact, interms of the time history of the acceleration impartedto the head. This was a considerable extrapolationfrom the original tests, in which the outcome measurehad been simply the presence or absence of skullfracture. The validity of the Wayne State tolerancecurve (WSTC) depended primarily on the assumptionthat, if the skull of a living human was fractured, thenthat injury would probably be accompanied byconcussion.

(a) The Gadd Severity Index

In 1966, at the Stapp Car Crash Conference, Gadd ofGeneral Motors proposed a head injury severityindex based on the Wayne State tolerance curve(Gadd, 1966). Gadd reasoned that some measure ofthe area under the acceleration/time curve for agiven impact could form the basis for such an index.However it was apparent that a low level of accelera-tion lasting for a long time was not injurious whereasa higher level of acceleration acting for a shorter timewas much more likely to be so, even though the areaunder the acceleration/time curve could be thesame.

Gadd therefore decided to weight the area measurein favor of the acceleration component. He did this byraising the acceleration value to the power of 2.5. Hechose this number, 2.5, because it happened to be theabsolute slope of the Wayne State curve when plotted

on logarithmic axes. The mathematical expression forthe Gadd Severity Index (SI) is:

SI = � a2.5 dt

where a is the ‘effective’ acceleration (thought to havebeen the average linear acceleration) of the headmeasured in terms of g, the acceleration of gravity, andt is the time in milliseconds from the start of theimpact.

The Gadd Severity Index or, as it was initially called,the Severity Index, was thought by some still not todeal adequately with long-duration, low-accelerationimpacts. 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 severityindex on that part of the impact that was likely to berelevant to the risk of injury to the brain. This wasdone by averaging the integration of the resultantacceleration/time curve over whatever time intervalyielded the maximum value of HIC. Because thisvaries from one impact to another, the expression forVersace’s modified index simply refers to times t1 andt2. The expression for HIC is:

HIC = (t2 – t1) � t2

t1

a/(t2 – t1) dt2.5

where an algorithm selects t1 and t2 to yield themaximum value.

Since then, the desirability of restricting the timeinterval (t2 – t1) to as low as 15 ms has been noted toavoid the possibility of obtaining high HIC valuesfrom long-duration, low-acceleration cases (see, forexample, Prasad and Mertz, 1985).

After the analysis of impact accelerations experi-enced by American football players, human volunteerimpacts with air-bags and impact tests with wind-screens, Hodgson and Thomas (1972) hypothesizedthat a linear acceleration/time concussion tolerancecurve may not exist and that only impacts of veryshort duration (e.g. with hard surfaces) may beimportant. They suggested that if the impact does notcontain a critical HIC interval of less than 15 ms, theimpact should be considered safe. As noted above,there is observational evidence that, in fact, headinjury without head contact is so rare that it is neverseen in the clinical setting (Tarriere, 1981; McLean,1995).

HIC has been shown to relate well to the probabilitythat an impact will fracture the skull of a cadaver(Hertz, 1994), which is perhaps not surprising giventhe derivation of the original points on the WayneState curve. However, the Head Injury Criterion bears,at best, a crude relationship to those factors nowthought 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 havebeen 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 thanthe Wayne State tolerance curve but is neverthelessalmost identical to it. There are other head injurycriteria that have been proposed but, despite theacknowledged inadequacies of HIC, it continues tobe by far the most widely used measure of the risk ofinjury to the brain from a blunt impact to the head.This is largely because it is specified in vehicle safetylegislation in the United States and also because thereis not yet any demonstrably superior criterion interms of relevance to the severity of head injury tohumans.

2.6 The state of the art of head injurybiomechanics

In conclusion, the following comment made by Gold-smith in 1981 is still a reasonable assessment of thepresent situation: ‘The state of knowledge concerningtrauma of the human head is so scant that thecommunity cannot agree on new and improvedcriteria even though it is generally admitted thatpresent designations are not satisfactory’.

Nevertheless, current work on mathematical mod-els, when combined with the results of detailedinvestigation of the response of the living humanbrain to impact to the head, shows promise ofcontributing substantially to our understanding ofbrain injury mechanisms and the tolerance of the headto impact.

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