Biomechanical Basis of Traumatic Brain Injury

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Chapter 324 Biomechanical Basis of Traumatic Brain Injury

David F. Meaney, Stephen E. Olvey, Thomas A. Gennarelli

The complex pathophysiologic phenomena encountered in patients with traumatic brain injuries (TBIs) can ultimately be viewed as a response of the brain to an external mechanical force. Therefore, preventing and treating the consequences of these injuries require an understanding of the causative mechanical factors that induce TBIs. We review the primary mechanical forces that contribute to these brain injuries, how these mechanical forces cause movement and damage within the brain, and the available data on how to prevent these types of injuries. This information is provided as an introduction only, and more detailed investigations of these principles can be found in other publications.¹^–⁴

Clinical Classification of Brain Injuries

Clinically, head injuries can be classified into five distinct categories: skull fracture, focal injury, diffuse brain injury, penetrating injury, and blast injury. Skull fracture may or may not involve damage to the underlying brain, but the fracture is often not a direct cause of neurological disability. Focal injuries are defined simply as visible damage that is generally limited to a well-circumscribed region; examples of focal injuries include contusions to the cortex and subdural, epidural, and intracerebral hematomas. Focal injuries occur in nearly half of all patients with severe brain injury and are responsible for approximately two thirds of brain injury–related deaths.⁵ Diffuse brain injury differs from focal brain injury and skull fracture in that it can often occur without macroscopic structural damage, is associated with widespread brain dysfunction, and affects approximately 40% of patients with severe brain injury.^5,⁶ Although contributing to nearly a third of the deaths attributable to brain injury, the most important aspect of diffuse brain injury is that it is the most prevalent cause of disability in survivors of TBI. In its mildest form (concussion), diffuse brain damage may not necessarily be structural and may involve only alterations in neural excitability, neurotransmission, or long-term changes in receptor dysfunction and associated disabilities. In more severe cases, diffuse brain injury is manifested as prolonged coma without a mass lesion and involves some degree of structural derangement at the microscopic level. Diffuse brain injury may sometimes include secondary damage from both brain swelling and ischemic injury. However, the most commonly injured substrate in diffuse brain injury is the axons within the white matter or the neuronal cell body; for this reason, the prominent forms of diffuse brain injury are diffuse axonal injury (DAI) and ischemic brain damage.⁵

Mechanisms of Injury

The first descriptor for differentiating traumatic from nontraumatic loading to the head is whether the loading is static or dynamic in nature. Static or quasi-static loading is an uncommon occurrence and is used to describe a situation in which force is applied to the head very slowly, typically occurring over times longer than 200 msec. Squeezing or crushing of the skull commonly occurs as a result of this static or quasi-static loading, as seen in earthquakes, building collapses, or machinery accidents, and it involves fractures at the vault or basilar skull region. Remarkably, because the loading needed to cause this extensive fracture pattern is applied slowly, it is common that consciousness is preserved after such loading. At high levels of force, the severe compression of the brain can lead to herniation of the brain contents and frequently fatal brain damage.

Dynamic loading is the more common type of mechanical loading to the head, especially when one considers traumatic injury. Dynamic loading is applied rapidly, typically in durations of less than 50 msec. Dynamic loading can be of two types: impulsive or impact. Impulsive loading occurs when the head is set into motion indirectly by a blow to another body region, such as when a running back is hit in the midtorso by a heavy lineman in American football or the sudden motion of an unrestrained head when the torso is restrained during a vehicular crash. These conditions are not infrequent in that any blow to the torso or face can often set the head into violent motion without a direct impact to the skull. The resulting inertial force applied to the head causes the brain to move within the skull; the nature and interaction of this brain motion with the internal skull structures leads to injury along the brain surface and within the brain parenchyma. Fifty-one moderate to severe head injuries occurred during the period 1996 to 2003 in automobile racing drivers who were exposed to high acceleration during crashes without the head or face making direct contact. In the worst cases, fatal basilar skull fracture was seen with cranial-cervical distraction. Another example of impulse loading without the head sustaining direct contact is the brain injury that results from “shaken baby syndrome.”

Impact loading is the more frequent type of dynamic loading. Impact loading is complex and usually results in a combination of contact force and inertial (head motion) force. The response of the head to impact conditions depends on the object that strikes the head. For example, inertial effects may be minimal if the head is prevented from moving when it is struck. In this situation, the injuries that occur are the result of contact phenomena, or mechanical events that occur both near and distant from the point of impact. The effects of contact phenomena vary with the size of the impact object, the magnitude of force delivered, and the direction of the force. Factors contributing to the magnitude of the force include the mass, surface area, velocity, and hardness of the impacting object. For objects larger than approximately 2 square inches, localized skull bending occurs immediately beneath the impact point and peripheral to the impact sites. If the skull deformation exceeds the tolerance of the skull, a fracture occurs. Penetration, perforation, or localized depressed skull fractures are more likely if the object has a surface area of less than 2 square inches. Additionally, shock waves can travel through the skull and parenchyma from the point of impact; within the brain, these shock waves can cause localized changes in pressure, distortion, and injury in the form of small hemorrhages and contusion. Children are at greater risk for this type of injury because their skulls are more flexible than adult skulls. Fracture deformation is between 1.7 and 5 times greater in a child than in an adult, depending on the zone of the skull affected.⁷ The increase in deformability of the child’s skull can result in extensive diffuse brain damage if the child’s skull has received a significant impact, as well as in a greater propensity for the formation of epidural hematomas because of the dural stripping action of skull deformation.⁷ Children also appear to be at greater risk for diffuse brain injury because their skulls have a lower degree of calcification and thus a reduced capacity to absorb an impact. This results in greater transfer of the kinetic energy from the impact site to the brain tissue.⁷

Although these definitions highlight the etiologic differences between impact and impulsive loading, the fundamental means of damaging the skull and brain are the same: distortion or straining of bone or soft tissues beyond their functional or structural tolerance. Strain, or deformation, is considered the proximal cause of tissue damage. This strain can cause alterations in the functioning of neural circuits and receptors and changes in the properties of neural tissue ^8,⁹ (for recent reviews, see Spaethling and colleagues¹⁰ and LaPlaca and coworkers¹¹). In general, strain can be considered the amount of deformation that the tissue experiences as a result of applied mechanical force. Strain is often described as compressive, tensile, dilational, or shear in nature (Fig. 324-1). Compressive strain is the amount of contraction observed when the material is compressed. For instance, if a stiff cylinder is placed upright on a tabletop and a stack of books is placed on the top circular face of the cylinder, the cylinder would shorten with respect to its original, unloaded length. If the cylinder were originally 10 cm in length and became 8 cm when the books were placed on top, the material is said to have a 20% compressive strain. In comparison, tensile strain is the amount of elongation that occurs when the material is stretched. If a column 10 cm in length becomes 11 cm long when stretched, it undergoes 10% tensile strain (stretched length minus original length divided by original length). Dilational strain, also referred to as volumetric strain, describes the change in volume that occurs when pressure is applied to all exposed faces of a material. Most material will show either negative or positive dilational strain when positive or negative pressure, respectively, is applied to the material. Finally, shear strain can be considered the amount of distortion that occurs in response to forces applied all along the surface of the material. A common illustration of shear strain is the distortional change that occurs in a deck of playing cards when one hand is moved across the top of the deck. None of the cards are compressed or stretched as a result of this motion, but the side profile of the deck changes to a slanted rectangle. The amount that the side profile varies from a normal rectangle indicates the state of its shear strain.

FIGURE 324-1 Visualization of the different strains (deformation) associated with traumatic intracranial damage. Dashed lines are the undeformed shape, whereas the shaded objects represent the deformed configuration. Tearing of vessels is often described as the tensile strain limit, where the limit is expressed as a fraction (usually percentage) of the original vessel length. Bone tissue can sustain both tensile and compressive loading, and the failure limit for each type of loading is normally distinct. Soft tissues, notably brain, are susceptible to shearing deformation. Axons within the tissue experience a more complex deformation. Pressure applied to all faces of a material will cause a dilational (volumetric) strain, which may be a mechanism to consider with very high loading rates (e.g., blast-induced pressure waves). The arrows in each diagram indicate the direction of the force applied to cause the resulting deformation.

The strain limit of bone and soft tissue before damage occurs depends not only on the force (e.g., direction, magnitude, duration) but also on the mechanical properties of the tissue. Materials such as concrete are ideal for sustaining large compressive loads, but they need reinforcement to sustain the same loads or deformation in tension. In comparison, rubber materials can often reach deformations 2 or 3 times their original length before breaking. However, these same rubber materials cannot sustain the tensile/compressive loads applied to concrete. Biologic materials are more complex than either rubber or concrete because tissues often show stiffening when the rate of applied force increases (i.e., dynamic loads will cause less deformation than the same force applied more slowly). Materials that show a change in stiffness with applied loading rate are termed viscoelastic. Perhaps the most recognizable viscoelastic material is Silly Putty. Silly Putty can easily be formed into various shapes with one’s hands. If pulled slowly, Silly Putty can deform substantially before breaking. If, however, this material is pulled very quickly, it breaks at a much smaller length. Biologic tissues typically display such viscoelastic behavior and can therefore withstand strain better if they are deformed slowly rather than quickly.

The three principal tissues involved in brain injury (bone, vascular tissue, and brain tissue) vary considerably in their tolerances to compression, tension, and shear. Bone, for example, is considerably stronger than either vascular or brain tissue; much more force is needed to induce damaging levels of stress. The amount of strain that bone can tolerate is actually less than that needed to injure brain tissue (for example, bone breaks at 1% to 2% strain, whereas brain and vascular tissue may not tear until 10% or 20% strain is applied). The key differences are the stiff mechanical properties of bone in comparison to either brain or vascular tissue—it takes considerable force to cause 1% to 2% strain in bone. Like vascular and brain tissue, bone also withstands compressive strain and shear strain, with a tensile strength tolerance somewhere in between. There is proportionately less difference among the three strain tolerances for bone, whereas there is a considerable difference in the damage limit for brain tissue in tension, shear, and compression.

Because the brain is virtually incompressible in vivo and has very low tolerance to tensile and shear strain, both tensile strain and shear strain are usually causes of brain damage. The same is true for vascular tissue. Whether damage to vascular or brain tissue takes place depends on the exact properties of these two tissues. As discussed later, vascular tissue tends to fail under more rapidly applied loads than brain tissue does. In addition, certain conditions can cause relatively pure injury to vascular elements in the neural structures within the head, depending on the type of injury.

Mechanistic Causes of Head Injuries

Most head injuries occur as a result of one of two basic mechanisms: contact or inertial (acceleration) loading. Contact injuries require that the head strike an object or be struck, regardless of whether the blow causes the head to move afterward. Inertial injuries are often called head motion or acceleration injuries because they result from violent head motion, regardless of whether the head moves because of a direct blow.

Contact Injuries

In general, contact injuries are caused by force during impact. These injuries result solely from contact phenomena and are not caused by head motion or acceleration. Contact injuries can therefore be considered trauma that would occur if the head were prevented from moving.

Because most impacts also cause head motion to some degree, contact injuries rarely occur clinically in pure form. Rather, contact injuries have superimposed acceleration injuries. Contact forces are of two types: those that produce effects at or near the impact site and those that produce effects remote from the area of impact. In both instances, contact forces cause focal injuries only; they do not cause diffuse brain injury.

Local Contact Effects

Examples of injuries caused by local contact effects include most linear and depressed skull fractures, some basilar skull fractures, epidural hematomas, and coup contusions. A linear skull fracture occurs as a result of local skull bending at the impact site that exceeds the local strain limit for the bony tissue (Fig. 324-2). Because strain tolerance is related to the inherent mechanical properties of the material, it is not surprising to find that skull fracture depends partly on the material properties of the skull and its thickness in the impact region. Additional factors include the magnitude and direction of impact and the size of the impacted area. Mechanistically, the local in-bending caused by the impact creates compressive strain on the outer skull surface and tensile strain on the inner surface (see Fig. 324-2). Bone, although naturally resistant to compressive force and strain, is less resistant to tensile force on the inner skull surface. Thus, the initial fracture begins at the inner table. Once initiated, the fracture follows the path of least resistance dictated by the geometric and strength characteristics of the surrounding skull. During the continuing fracture process, energy from the impacting object is transferred to the skull via the fracture. The linear fracture is complete when the impact energy is dissipated completely.

FIGURE 324-2 Local contact effects. During an impact, the scalp and underlying skull (A) will deform. With its stiff mechanical properties, bone will bend inward and create localized stress within the bone and adjacent brain tissue (B; stress indicated as lines emanating from the impact site). The stress within the bone is tensile on the inner table and compressive along the outer table. Most bony structures fail under tension before compression, and therefore the initial site of skull fracture occurs along the inner table (C).

Depressed skull fractures occur when the striking or struck object is small enough to cause concentration of strain and stress immediately beneath the impacting object. These concentrated strains produce a highly localized fracture pattern that does not emanate from the contact site. Unlike a linear skull fracture, energy is not absorbed by a fracture propagating away from the fracture point. Instead, the energy is dissipated by the localized bone failure. With highly concentrated contact force, these depressed skull fractures penetrate completely through the skull. Impact of the skull base or nearby regions can occur and cause basilar skull fractures from local contact effects. Direct impact on the occiput or mastoid is a common method for the development of this type of skull fracture.

The vascular damage caused by local contact effects (e.g., epidural hematoma and coup contusions) is intimately linked to the causative phenomena for the preceding skull fracture types. Epidural hematoma is a complication of skull bending that is usually associated with skull fracture. In the limiting case, dural vessels are torn as the fracture propagates and travels past a vessel. Mechanical failure of these vessels can occur without fracture if the skull deformation and bending are sufficient to cause vascular tears. Rapid return of the deforming skull after impact may strip away the underlying dura and thus form a potential space that slowly fills with blood, such as the so-called venous epidural hematoma, which is more often seen in younger persons.

Coup contusions occur beneath the site of impact under certain conditions. These contusions are due either to direct injury to the brain and its surface vessels that lie beneath the area of skull deformation or to the high negative pressure that develops in the area where the skull rapidly snaps back into place. The first mechanism causes highly focused compressive strain; the second subjects the brain to very high tensile stress. In either case, the strain is sufficient to cause tissue failure of the pial and cortical vessels of the brain and form localized contusions. Brain laceration is an extension of the same phenomenon but may also occur if skull in-bending is sufficient to actually perforate the pia.

Remote Contact Effects

Contact phenomena, which are equally important, can produce remote injuries as a result of either skull distortion or stress waves. These mechanisms contribute to vault fractures away from the impact site, to basilar skull fractures, and to contrecoup and intermediate coup contusions. Remote vault fracture can develop if the impact occurs over a thick portion of the skull or if the striking object is relatively broad. Because the thick skull can withstand the impact force, the local in-bending energy can travel away from the impact site to remote skull regions, which may sustain larger local bending as a result of their inherently weaker characteristics. If the strain tolerance is exceeded, remote skull fracture occurs. Once initiated, a fracture will usually propagate along the lines of least resistance. Typically, the basilar skull has thin sections that offer this path of least resistance. Consequently, various types of basilar skull fractures may occur as a result of remote contact loading.

Occasionally, head contact is severe enough to cause global changes in skull shape. These global changes are particularly apparent if the physical skull structure is compliant, such as in infants and developing children. This type of large skull deformation can cause rapid increases or decreases in intracranial volume. These changes are usually transient, and because of the elastic nature of the skull and its contents, the skull returns to its normal shape immediately after the force is removed. Two phenomena may occur at these large deformations—localized changes in pressure and fluctuations in intracranial volume—and cause a variety of injuries. The rapid changes in skull shape can be sufficient to produce levels of negative pressure at points where the skull has pulled away from the brain and cause contrecoup contusions. This localized pressure mechanism is proposed as a cause of the small petechiae surrounding the ventricles, presumably as they expand in response to the brief negative intracranial pressure. A sudden fluctuation or decrease in intracranial volume caused by global skull deformation can prompt herniation of the brain contents through the various foramina, primarily the foramen magnum. The action of herniation places an excessive amount of strain on structures of the lower brainstem and injures tissues remote from the impact site. These fluctuations in intracranial volume may explain part of the distinct neurological and pathologic findings observed in infants or children with TBI. However, the frequency with which trauma contributes to global skull deformation in adults is still debated, and these injuries are probably much more commonly due to inertial effects.

The second mechanism for remote damage from contact loading is the effect of stress waves originating at the point of impact. Radiating in a three-dimensional manner from the loading point at an exceedingly rapid speed, stress waves spread through the skull to cause local skull distortions that if excessive, produce basilar and remote vault fractures. Stress waves also spread throughout the brain and, like waves in water, reflect from the opposite side of the head and reverberate within the brain. The manner in which these waves reverberate within the brain depends on, among other factors, the ability of the brain tissue to dissipate the disturbances at the impact site. If the stress waves in the brain are amplified by this reverberation or local skull bending, high-intensity localized differences in pressure occur. If the strains induced by these stress waves exceed the tolerance of the tissue or vessel, damage will result. In theory, the areas of stress concentration secondary to reverberating shock waves occur deep within the brain and not at its surface. Therefore, shock waves have been used to explain the formation of intermediate coup contusions (a name sometimes used to describe hemorrhages occurring on surfaces that are not convex), scattered deep intracranial hemorrhages, and traumatic intracerebral hematomas. However, because these waves travel so rapidly and are quickly dissipated, this mechanism remains a matter of debate.

Head Motion (Inertial) Injuries

Inertial loading of the head, whether from impact or from impulsive loading, causes a broad variety of clinically relevant injuries. They are commonly called acceleration-deceleration injuries because acceleration is an important physical measure for loading. Other parameters may be equally important (e.g., head velocity), and although this category should perhaps be called “head motion injuries,” the term “acceleration injuries” remains in common use. From a mechanical point of view, acceleration and deceleration are the same physical phenomena and differ only in direction. For example, the effects of accelerating the head in the sagittal plane from the posterior to anterior direction act the same as decelerating the head from anterior to posterior.

Similar to contact injuries, head motion results in strain within brain tissue that can cause either functional or structural damage (Fig. 324-3). First, differential movement of the skull and brain can be produced by head acceleration or motion. This relative movement occurs because the brain is free to move to some degree within the skull and the brain lags behind the skull for a brief moment after acceleration begins as a result of inertia. When combined, these factors allow the skull and dura to move relative to the brain surface, thereby potentially causing localized strain at the surface. Particularly susceptible in this situation are the parasagittal bridging veins between the brain surface and dura, which may tear if the strain exceeds the tolerance of the vessels, and such tears cause about 60% of acute subdural hematomas. Furthermore, movement of the brain away from the skull creates a region of low pressure that if sufficiently intense, causes contrecoup contusions. Second, head acceleration can produce strain within the brain parenchyma and therefore result in widespread disturbances in brain function or structures. Strain within the brain parenchyma can be manifested as classic “cerebral concussion,” DAI and associated hemorrhages from tearing of tissue, and intermediate coup contusions. In each type of injury, the severity and extent of damage are intimately linked to the magnitude, rate, duration, direction, and type of inertial loading.

FIGURE 324-3 Head motion injuries. Impact can cause local contact effects, but two additional effects contribute to the lesions observed clinically. Because of its inertial properties, the brain slides relative to the inner skull surface, and cortical vessels connecting the brain to the dural membrane may tear. Additionally, the inertial loading delivered to the brain, coupled with its soft material properties, leads to deformation of the brain contents. This deformation is visualized with a superimposed grid pattern that deforms from the acceleration imparted during impact (shown as an arrow).

Types of Head Acceleration

Three types of acceleration can occur: translational, rotational, and angular (Fig. 324-4). Translational acceleration occurs when the center of gravity of the brain (which is approximately in the pineal region) moves in a straight line. Purely translational acceleration is uncommon because the physiologic articulation of the head and neck limits this pure movement. Exceptions occur when the head moves in a translational manner for brief periods or the head becomes arrested with other motions. An exception may be vertex impact, during which superior to inferior motions can occur. The brain motions that take place during translational acceleration are primarily due to the relative brain skull motions previously described and not to strain produced deep within the brain. Concussive injuries do not occur when the head experiences a purely translational acceleration.¹² For concussion or DAI to develop, the brain must undergo angular acceleration. Therefore, translational acceleration does not cause diffuse brain injuries, but it can produce focal injuries, including contrecoup contusions and intracerebral and subdural hematomas.

FIGURE 324-4 Types of head acceleration. Translational acceleration will move the head in a linear path. Alternatively, rotational acceleration will induce rotation about the head’s center of mass, which is located approximately in the pineal region. It is rare to find instances of pure translational or rotational acceleration in “real-world” injury situations. Rather, angular motion is more common. The angular motion leads to combined translational and rotational acceleration, thereby creating injury patterns that arise from both acceleration types.

Rotational acceleration occurs when there is rotation about the center of gravity of the brain without the center of gravity itself moving. Because the center of gravity of the brain is in the pineal area, pure rotational acceleration is a virtual impossibility in nearly all clinical situations. For the brain to rotate around an axis that goes through the pineal area, the entire body would have to swing around it. A notable exception is when the head is rotated solely in the horizontal plane, in which case pure rotation may occur about a vertical axis running through the pineal area.

Rotational acceleration is a very important and highly injurious mechanism because not only does it produce the high surface strain seen in translational motions but it is also the only mechanism capable of producing high levels of strain deep within the brain itself. However, because of the infrequency of pure rotational motions in clinical situations, the effects of rotational acceleration are usually seen after angular acceleration of the head.

Angular acceleration occurs when components of translational and rotational acceleration are combined. In this situation, the center of gravity moves in an angular manner. Because of the neck’s anatomy, angular acceleration is the most common head motion encountered clinically. Frequently, the center of rotation occurs in the lower cervical region. The exact location of this rotation point, in conjunction with the magnitude of the impact force, determines the proportion of translation and rotation that the brain experiences. As the rotation point moves higher up the cervical spine, there is a proportionally greater rotational component; moving the rotation point lower introduces proportionally more translational acceleration. As might be expected, angular acceleration is the most damaging brain injury mechanism because it combines the injurious mechanism of both translational and rotational movements, especially the latter. Virtually every known type of head injury can be produced by angular acceleration, except for skull fracture and epidural hematoma. Several studies have now documented the in vivo motion of the brain during angular motions ^13,¹⁴ and have investigated the head motions associated with sports and concussive impacts.¹⁵^–²⁰

In helmeted sports, it is important to note that the helmet can and will accentuate angular accelerations when the head does not receive a direct impact because of the added mass of the helmet. Angular acceleration is greatly increased as a helmet’s mass increases and moves away from the center of rotation. This is especially important in children’s sports because of the inertial loading of a child’s head. If a child’s head is 1 kg lighter and 2 cm smaller in diameter than the typical 6.2-kg adult head, the inertia of a child’s head is approximately half that of an adult head, thereby allowing these greater accelerations.^7,²¹ In a study conducted to determine a recommended standard for youth helmets, it was found that boys aged 6 to 11 years have an average head mass 0.9 kg lighter than that of an average adult man with a head circumference approximately 2.5 cm less than the adult average circumference.²² Thus, modern helmet design must take mass into consideration.

Determinants of Acceleration Injury

The amount of inertially induced damage depends not only on the type of acceleration imparted to the head but also on several other factors. The magnitude of acceleration can be viewed as being proportional to the amount of strain delivered to the brain, and the acceleration rate is proportional to the strain rate. Both strain and the strain rate are factors contributing to the structural or functional limit of intracranial tissues. If the magnitude of acceleration is constant, the rate of acceleration varies inversely with the duration for which the acceleration is applied. Conversely, if the duration of acceleration is constant, the acceleration rate varies directly with the magnitude of the acceleration.

If one applies a constant amount of acceleration and varies only the duration over which the acceleration occurs, three zones of clinical interest are encountered (Fig. 324-5). The exact relationships between mechanical loading (magnitude, type, and direction of acceleration) and injury patterns are becoming increasingly more refined with computational models of the head/brain structure.²³^–²⁶ First, with very brief accelerations, many of the inertial effects within the brain are damped, and as a result the brain actually experiences very little strain. Consequently, extremely high accelerations are required to produce injury. Second, if the duration of acceleration is slightly longer, strain begins to appear within the brain but is primarily restricted to the periphery. Moreover, the brain surface can slide relative to the skull/dura surface. Injuries produced in these circumstances are confined to the brain periphery and vessels (e.g., bridging veins). Third, as the duration of acceleration increases even more, strain propagates deeper within the brain and can cause DAI, which in its severe form is manifested as prolonged traumatic coma.

FIGURE 324-5 Zones of clinical injury. An abbreviated format to describe human tolerance to specific head motions often uses both the magnitude and duration of acceleration. A range of both parameters is associated with either injury or no injury. For rotational motions, there are three general zones. In zone I, very brief durations of acceleration are highly unlikely to cause injury because the strains do not propagate to deeper brain structures and the relative motion between the brain and skull is small. In zone II, slightly longer acceleration durations allow strains to penetrate the periphery but do not significantly move into the deep region of the brain. Therefore, injuries to the brain periphery and cortical vessels are more common. In zone III, with even longer durations of acceleration, the strains propagate throughout the brain and injuries can occur to both the peripheral and deep parts of the brain.

It is thus extremely complex to try to map acceleration profiles into exact patterns of damage within the brain. Several simple descriptors of acceleration—the amount and type of acceleration, its duration, and the rate at which the acceleration is applied to the head—are interrelated and together contribute to the pattern of injury observed within each individual. Certainly, these parameters are linked; for example, with a constant level of acceleration, as the duration increases, head velocity and movement also increase. Past efforts to describe the tolerance of the head to different forms of TBI have used two primary measures—acceleration and head velocity/duration of acceleration—to reflect this complex relationship between motion and the resulting injury. Structural damage to superficial vascular tissue, especially to bridging veins and pial vessels, occurs in high-acceleration, short-duration conditions, whereas damage to brain tissue occurs in circumstances in which high accelerations are present with longer pulse durations and thus higher velocities.

Blast-Induced Brain Injuries

The effects of blast loading on humans originated with the term “shell shock” from World War I, which was used to describe a collection of symptoms that included a temporary altered mental state or confusion immediately after the blast.²⁷ In more severe forms, unconsciousness would occur. Despite being periodically addressed since its recognition as a clinical syndrome, only very recent studies have better described the conditions of blast-induced brain injury.²⁸^–³⁰ Although blast injury is formally defined in four phases, the bulk of blast-induced traumatic brain injury (bTBI) occurs in the primary, secondary, and tertiary phases. The primary injury phase consists of the response of brain tissue to the blast wave (an intense overpressurization impulse component of the blast). The secondary injury phase results from penetration of shrapnel into the head. The tertiary injury phase is due to head contact/acceleration as the body is moved by the “blast wind” (forced super-heated airflow).

No individual model can mimic the clinical and mechanical complexity resulting from bTBI. For injuries in the civilian population, the mechanical factors are often grouped into either the focal/contact or acceleration/inertial forces that produce the different mixture of clinical injuries ranging from concussion to skull fracture, contusions, and DAI. However, blast injuries are grouped by injuries resulting from the different physical aspects of the blast phenomenon; in short, primary bTBI is caused by the shock wave, secondary bTBI is caused by shrapnel, tertiary bTBI is due to the blast wind, and quaternary bTBI covers the remaining mitigating factors. These groupings apply to the study of not only brain injuries but also other body regions susceptible to injury from blast. This distinct method of grouping blast injuries may seem inconsistent with the classifications often used for civilian TBI resulting from falls/assaults or motor vehicle accidents; however, the fair level of knowledge gained from civilian TBI studies can be used to study the military problem.

Primary blast injury is limited to injuries caused by the rapidly expanding blast wave.³¹ Past work identified typical pressure wave profiles generated during blast events³² and how this pressure wave propagates through air and biologic tissues.³³^–³⁵ Shock waves from a blast are typically characterized as a rapid rise and fall of high pressures.³⁶ The shock wave passes on the order of milliseconds, although the exact profile and range are dependent on the size, type, and shape of the explosive. In air, the shock wave oscillates between overpressure and underpressure segments, but these waves dampen out quickly. In water, the shock wave maintains a normal pressure profile over a longer range. The presence of structures and fluid interfaces complicates this pressure profile.

Most structural damage occurs when the shock wave travels from water to air. For this reason, a large number of studies have focused on the fluid-air interfaces in the body because they are highly vulnerable to the passing pressure waves. Studies in these areas have generated injury thresholds for both the pulmonary system and the gut/bowel.³⁷ As this pressure wave travels through the organs, there are stress concentrations that arise at tissue-air interfaces, reflections of stress waves at tissue interfaces, and possibly constructive stress wave interference within internal points of tissue that can further complicate the pattern of injury.³⁶ Models to study the primary injury phase should account for both the blast pressure transmitted through the organ of interest and shock wave reflection/transmission behavior at tissue interfaces.

Secondary blast injury covers both the penetrating and nonpenetrating injuries that occur when high-velocity projectiles/fragments impact the head.³¹ Certainly, these injuries share some common ground with the ballistic wounds in civilians (for recent publications, see elsewhere³⁶^–³⁹ but are considerably more complex because of the nonuniform size and number of impacting fragments. Nevertheless, the mechanics of these penetrating lesions is becoming clearer, given the frequency of gunshot wounds in the civilian population.³⁸ A projectile moving through soft tissue at high speed will cause rapid expansion and subsequent collapse of tissue along the penetration track. This induces cavitation damage along the path of the projectile, as well as primary laceration damage along the path of the fragment. At the mechanistic level, these injuries are best modeled as a tissue laceration, with the obvious complicating mechanisms related to blood in the extracellular space and the potential for secondary brain injuries such as hypoxia.

Tertiary blast injury occurs when the primary blast wind causes the victim to collide with fixed or mobile objects. These types of injuries share the most in common with contact/acceleration injuries in civilians, where both the contact and acceleration forces can contribute to the different intracranial injuries that occur. Helmets worn by troops reduce the likelihood of injuries from direct contact for most of the head. However, current military helmets are not designed to specifically reduce rotational acceleration after a helmeted impact.^19,³⁹ The Head Acceleration Neutralization System (HANS) worn by race car drivers has been dramatically successful in mitigating this rotational acceleration damage (Fig. 324-6). There is still high potential for inertially based injuries, including subdural hematoma and DAI. As a result, the predominant mechanism of tertiary blast injuries in helmeted troops is the intracranial deformations caused by the head striking an object or the head being struck by an object with sufficient mass to cause a significant inertial load. In nonhelmeted victims, tertiary blast injuries can also include skull fracture or contusions from focal contact forces when the unprotected head strikes an object or surface.

FIGURE 324-6 Driver wearing a modern Head Acceleration Neutralization System device tethered to the helmet.

Injuries and Their Mechanisms

This section uses the preceding concepts to explain the mechanisms responsible for frequently observed primary head injuries. It is clear that many of these injuries can occur in combination, and isolated occurrences of these types of damage, particularly after severe head injuries, are rare. As a result, it is common to find particular brain damage mechanisms associated primarily with motor vehicle accidents and other patterns of damage associated more frequently with falls or assaults or with pedestrian-versus-vehicle accidents.

Skull Fracture

Focal Brain Injury

Epidural Hematoma

Epidural hematoma can be considered a more complex case of linear skull fracture. During the fracture initiation or propagation period, vessels in the underlying dural membrane are torn and bleeding ensues into the epidural space. Subdural bleeding is also possible without skull fracture because the local skull bending caused by an impact may be sufficient to tear dural vessels without exceeding the failure limit of the bone. Head motion or inertial effects do not generally cause an epidural hematoma.

Coup Contusions

Immediately under the impact point, coup contusions arise principally from the local skull bending or fracture caused by an impact from a relatively small, hard object. These phenomena in turn subject the underlying cortical and pial vascular network to strains that if excessive, cause bleeding at or near the brain surface. Damage is likely to occur when the skull is “rebounding” from the impact and the vessels are experiencing tensile strain. For cases of skull fracture, the localized strain from the skull contacting the cortical surface provides a means for the vascular damage noted in the pia and cortex.

Contrecoup Contusions

Two phenomena have been attributed to the pathogenesis of countercoup contusions: cavitation effects and inertial loading. Of the two, the more likely mechanism of contrecoup damage is translational or angular head motion. On impact, the brain moves toward the impact site and creates an area of negative pressure directly opposite the loading point. This negative pressure may in turn cause damage by exceeding the tensile strength of water or, alternatively, cause small gas bubbles to appear within the parenchyma. The return to normal or positive pressure will cause the small bubbles to collapse and is termed cavitation. However, it is difficult to conduct experiments that clearly support the cavitation mechanism, and this mechanism does not easily explain contusions located outside the region considered opposite the impact. Instead, it appears that the regions of vascular disruption and cortical damage and contrecoup regions are due primarily to acceleration effects and can result from either translation or angular head motions. Each head motion, particularly angular movement, is capable of producing tensile strain throughout the brain. If the tensile strain is greater than the vascular tolerance in a given region, contusion occurs. However, because these injuries are inertial and can therefore be caused by impulsive loading only, impact is not necessary for contrecoup contusions to occur. The term “contrecoup” can therefore be considered misleading because the critical mechanism is most often acceleration and not the contact effects from impact. In situations in which the head experiences impulsive loading, contrecoup contusions occur solely because of the strain generated in the cortical brain region during the acceleration period. Strain concentrations may occur in specific regions of the brain because of geometric effects and are responsible in part for the high incidence of frontal and temporal lobe contusions observed clinically. Although global skull deformation caused by impact may create tensile stress and contusion damage in regions remote from the impact, the predominant mechanism of contrecoup contusions is rotational acceleration.

Because of their macroscopic and easily identifiable nature, contusions are periodically used to characterize the biomechanical input to the head. However, several points deserve mention when using contusions as a tool in this manner. First, the line of action of an impact force cannot be ascertained simply by connecting a line between the coup and contrecoup damage sites. The discussion in the preceding paragraphs highlights the significance of inertial loading producing the pattern of contrecoup damage versus the role of local contact effects. Thus, coup and contrecoup injuries, although differing only slightly in name, arise from fundamentally different mechanisms. Contrecoup contusions are frequently not exactly opposite the point of impact. In fact, the most frequently occurring contusions of the temporal and frontal poles are contrecoup in almost every instance, regardless of the impact site. In view of these differences, it is more appropriate to consider a contrecoup contusion as one that is simply not immediately below the impact site; it should not be considered to appear immediately opposite the point of impact. Second, in a similar manner, coup and contrecoup contusions should not be viewed as arising from acceleration and deceleration of the head, respectively. Rather, the relative proportion of coup versus contrecoup contusions depends solely on the response of the head to impact. Because of its pathogenesis, the acceleration of the head caused by a concentrated blow to the head has led to the proposal that acceleration causes coup contusions. However, the hard, small object that causes impact in these typical cases tends to produce focal skull deformation with an underlying coup contusion, and a large portion of the energy is dissipated at the impact site. Local skull deformation produces a noticeable coup contusion, and the lack of substantial head motion produces slight or very limited contrecoup contusion. Conversely, a softer or larger impact object is commonly seen in cases of deceleration injury, such as in a vehicle accident victim, in whom the injuries are caused less by local injury beneath the point of impact because a proportional increase in energy is used in setting the head into motion or stopping it from moving. In this case, a large contrecoup region occurs and the coup contusion is smaller or nonexistent because of the soft, wide padded surfaces within modern automobiles.

Intermediate Coup Contusions

This designation has been given to vascular disruption in brain surfaces that are not adjacent to the skull. Although the mechanism of these lesions has not been studied extensively, it is likely that they are due to strain concentrations resulting from impact-generated stress waves or from inertially generated brain movements. In the latter case, the brain is thought to strike or be pulled away from adjacent, relatively immobile structures, a mechanism that results in focal or compressive strain, respectively. Alternatively, intermediate contusions of the cingulate gyrus can be due to interactions with the falx, and similarly, those of the inferomedial temporal lobe can result from involvement with the tentorium of the petrous ridge.

Intracerebral Hematoma

Large traumatic intracerebral hematomas are uncommon and are most often associated with extensive cortical contusions. They can therefore be considered contusions in which larger, deeper vessels have been disrupted. Smaller, single hematomas that are not associated with contusion probably occur because of stress concentrations resulting from impact or because of acceleration-induced tissue strains deep within the brain. Intracerebral hematomas are poorly studied but may represent a form of the tissue tear/vessel shear hemorrhages that accompany DAI.

Tissue Tear Hemorrhages (Microhemorrhages)

Tissue tear hemorrhages are multiple areas of damage to blood vessels and axons occurring in association with DAI. Accordingly, these hemorrhages are considered to be due to inertial or head motion effects and are therefore not related to contact phenomena. They are distinct from the intracerebral hematomas just described and are actually a part of the pathologic picture of a severe form of DAI that results in immediate prolonged coma. Tissue tear hemorrhages are typically numerous, small, and located parasagittally and in the central third of the brain.

Tissue tear hemorrhages appear in small areas where the brain’s tolerance to shear forces has been exceeded, thereby allowing the tissue to separate sufficiently to tear both axons and small vessels. Their locations are characteristically in the superior medial frontoparietal white matter, corpus callosum, centrum semiovale, periventricular white and gray matter (“gliding contusions”), internal capsule, and basal ganglia. In the brainstem, they appear in dorsal area of the midbrain and upper pons (“dorsolateral quadrant brainstem contusions”). Several factors contribute to these multiple foci of damage, including the presence of intracranial partitioning membranes, the geometric irregularities of the skull, and the plane of motion experienced by the head. Tissue tear hemorrhages represent areas of maximum strain-acceleration–induced brain damage, and these lesions denote severe DAI on computed tomography or at postmortem examination of the brain.

Subdural Hematoma

Three varieties of acute subdural hematoma are found clinically. The first two are associated with contusion and laceration and are sometimes called complicated subdural hematomas. Complicated subdural hematomas result from the contact or acceleration effects that cause the primary lesion. The third type of subdural hematoma is the most common form of vascular disruption; it involves tearing of parasagittal bridging veins located along the interhemispheric fissure and sagittal sinus. It results entirely from inertial and not from contact forces. Based on their superficial location, parasagittal bridging veins are susceptible to damage during short-duration angular acceleration of the head. Common situations in which this acceleration condition occurs include falls in which the head strikes a broad, hard surface and assaults in which a majority of the impact energy is used to set the head in motion. Under these loading conditions, the strain within the brain is concentrated along the outer margins where the parasagittal bridging veins reside. If vascular tolerance is surpassed, subdural bleeding occurs. Because of its similar mechanism, subdural hematoma may coexist with underlying hemispheric brain damage, usually DAI. This explains the frequency of cases in which the subdural hematoma is small but the brain damage underlying it is more than expected because of compression of the brain from the hematoma.

Diffuse Brain Injury

Cerebral Concussion

All gradations of concussion (transient reversible neurological dysfunction as a result of trauma) are produced entirely by inertial loading and not from contact phenomena effects. Experimentally, it is now possible to produce concussion in small animals with acceleration.^40,⁴¹ It is probable, however, that concussion is observed in concert with injuries arising from the contact phenomena, simply because the contact loading will produce both contact effects and head acceleration. Unlike subdural hematoma, concussion does not occur with purely translational motion of the head. Angular rotational head motion causes the deeper structures within the brain to deform and results in the classic widespread disruption of brain function that underlies concussion. For a concussive injury, most of the strain is insufficient to cause structural damage. Instead, damage to the structures may be either partially or completely reversible, depending on the severity of the inertial loading. The precise location of the functional derangement in a concussion continues to be debated. It remains uncertain whether the effects of angular acceleration are principally seen in the brainstem, the cerebral hemispheres, or both regions.

Diffuse Axonal Injury

Axonal damage appears to be one of the two most important pathologic substrates producing prolonged traumatic coma not attributable to mass lesions and, like cerebral concussion, is caused only by angular rotational acceleration and not by contact phenomena (the second pathologic substrate being ischemic/hypoxic neuronal damage). DAI nearly always coincides with other forms of contact or inertial injuries.⁴² Furthermore, recent evidence has suggested that the magnitude of rotational acceleration needed to produce DAI requires the head to strike an object or surface, a requirement that raises the likelihood of superimposed contact injuries.^24,⁴³ In high-g vehicular crashes, as seen frequently in modern motor sports, DAI does occur without direct impact to the helmeted head. The amount and location of axonal damage as a consequence of rotational acceleration probably determine the severity (depth and duration) of the injury, as well as the quality of recovery. Critical factors in estimating the amount and extent of axonal damage include the magnitude, duration, and onset rate of the angular acceleration, in addition to the direction of motion and the role of the intracranial membranes.⁴⁴^–⁴⁶ In particular, DAI is produced by a longer duration of acceleration loading, as opposed to the relatively brief loading duration that usually produces acute subdural hematoma. DAI is most likely to occur when the head is impulsively loaded or when the impact involves a relatively soft, broad object, as in an occupant involved in a motor vehicle accident. The former is not common clinically because of the levels of rotational acceleration needed for it; instead, the latter is the most frequent circumstance producing DAI.

The direction that the head moves plays an important role in the amount and distribution of axonal damage in a given situation. For equivalent levels of angular acceleration, the brain is most vulnerable to axonal damage if it is moved laterally. The brain tolerates sagittal movement best, and horizontal motions are somewhere between lateral and sagittal movements. However, sagittal motions are the most effective in producing vascular injuries in the superior margin of the brain because the motion of the brain in this plane is not severely restricted by intracranial membranes. To this end, the full-blown picture of widely scattered damage to the cerebral hemispheres and brainstem, along with tissue tear hemorrhages, most likely occurs because of the spatial changes in the strain pattern induced by the falx and tentorium during lateral motions. Furthermore, the gyral geometry of the cerebrum and brainstem plays an important role in the response of the brain to rotational motions. In response to a lateral head motion, small centers of rotation occur in the superior frontal and temporal lobe. Although the induced clockwise motion is the same for all centers of rotation, at the periphery of the rotation, the brain tissue is moving in opposite directions. The combination of three main factors—the complex gyral geometry, the white/gray matter mechanical properties, and the intracranial membranes—leads to a complex deformation pattern within the brain that correlates well with areas showing damage. Until recently there has not been an effective way to measure head accelerations directly in real time in humans. A method using custom-fitted ear plugs with implanted triaxial accelerometers to measure head acceleration in the x-, y-, and z- axes with 5 degrees of freedom was developed in 2002 (Fig. 324-8).⁴⁷ Current technology will allow these systems to record data and to transmit that data wirelessly to the sidelines or other remote location (Fig. 324-9). Studies including automobile racing drivers, football players, rodeo cowboys, and aerobatic pilots have currently been or are being contemplated. In-ear accelerometers have an advantage over other methods that instrument the helmet because they are not affected by the independent movement of the helmet on impact. This movement is usually in the direction opposite the force applied and not proportional to the resultant motion of the head (crash test results at Wayne State University, Melvin J, personal communications). It is anticipated that data from these studies will help gain a better understanding of what degree and direction of force will cause what specific types of severe TBI. Additionally, it is anticipated that a threshold level of acceleration will be recognized that if exceeded, will identify an athlete or combatant who should be immediately pulled out of competition or conflict because of a concussion. Having accurate head acceleration data should also help validate various head injury models.