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.