Stereotactical Phenomena in Traumatic Brain Injury Biomechanics: Diffuse Axonal Injury and Brain Concussion

By Dr. C. OBREJA
NTCP@ - not-for-profit organization
211, rue Robespierre, 93170 Bagnolet, France
Email: ntcp@neurostaff.org
Web site: http://www.neurostaff.org

Traumatic Brain Injury (TBI) is the consequence of spatiotemporal pressure variations occuring inside the brain during head traumas. Spatial distribution of the pressure gradient (PG) is responsible for the locality of cerebral lesions and consequent neurological signs. Besides the skull's deformation caused by contact loading and the resulting skull vibrations and/or fractures, current biomechanical theories concern two inertial phenomena: linear acceleration and rotational head movement. The first theory explains superficial brain lesions and is widely accepted. The second theory better explains deep cerebral lesions and the concussion mechanism but is still controversial. The stereotactical approach mainly considers the approximately spherical shape of the skull-brain interface. The skull-brain relative movement, caused by acceleration phenomena (linear or rotational) and by skull vibrations, generate secondary pressure waves with approximately spherical wave fronts that concentrically propagate toward the deep cerebral structures. The wave front's spoke and its surface progressively decrease. According to the energy conservation law, the amplitude of the pressure waves progressively increases. Thus, the PG will be maximal in the geometrical center of the implied skull vault segment. Stereotactical phenomena can explain common posttraumatic neurological signs and cerebral lesions and is compatible with previously reported experimental findings. It complements other biomechanical theories, which could allow us to integrate TBI biomechanics in a common concept in order to better understand TBI pathophysiology and related pathological entities like boxers' chronic encephalopathy or even Alzheimer's disease. Further experimental and especially human observational research on TBI biomechanics is needed.

Introduction

Traumatic brain injury (TBI) is the main cause of death for patients under 45 (1). TBI biomechanics explores the mechanical phenomena that cause initial cranio-cerebral lesions and thus represents the starting point for the overall understanding of TBI pathophysiology. TBI is the consequence of spatiotemporal pressure variations occuring inside the brain during head traumas. Spatial distribution of the pressure gradient (PG) is responsible for tissue strains (compression, tensile, shear), cerebral lesion localisation and consequent neurological signs (2). Besides skull deformation caused by contact loading and the resulting skull vibrations and/or fractures, current biomechanical theories concern two inertial phenomena: linear acceleration and rotational head movement. The first theory explains superficial brain lesions. The second theory seems to better explain deep cerebral lesions and the concussion mechanism but is still controversial (3). Here is a new biomechanical approach that can explain deep cerebral lesions and common neurological signs observed after human head traumas.

Traumatic brain lesions

Focal and diffuse cerebral lesions are described. Focal lesions, also called cerebral contusions, are haemorrhagical and are visible on such frequently performed radiological exams as X-ray computed tomography. Focal lesions are often located in the superficial brain structures, close to the skull, but sometimes deep cerebral hematomas occur. Focal lesions always coexist with different degrees of diffuse cerebral lesions, also called "diffuse axonal injury" (DAI). DAI is concentrated in the deep cerebral regions and is not visible on radiological exams. Meanwhile, in accordance with its severity, DAI is mainly responsible for various degrees of consciousness disturbances and further clinical outcome (2). The clinical expression corresponding to the pathological term DAI is brain concussion.

Current Biomechanical Theories

The linear acceleration theory was first published about a century ago. Relative movements and secondary impacts occur between the skull and the brain during a head impact. The pressure increases in the superficial cerebral structures below the impact zone, proportionally to the head's linear acceleration (4). This theory explains the occurrence of superficial cerebral lesions. It cannot explain preferential localisation of DAI in the deep cerebral structures (8), nor deep traumatic cerebral hematomas. Nor can it explain why loss of consciousness and memory troubles are the most frequent clinical signs occurring after head trauma - despite the fact that the responsible cerebral structures are deeply located.

According to the rotational movement theory published in 1943 by Holbourn (5), DAI and deep cerebral hematoma are caused by tensile strains occurring between the superficial and deep cerebral structures during circular head movement. In a large series of experiments on primates, Thibault and Gennarelli particularly supported the role of rotational movements in the occurrence of DAI (6).

The consequences of skull vibrations are poorly understood. It is probable that low-frequency skull vibrations (below 200 Hz) mainly cause deep cerebral lesions, while high-frequency vibrations have more consequences to the superficial cerebral structures (7).

In real-life head trauma all these phenomena coexist. In the mean time, DAI and brain concussion also occur in purely linear acceleration head-trauma experiments (5) Even, under the current approach, the linear acceleration theory cannot explain how deep cerebral structures can be injured while superficial cerebral structures are uninjured.

The Stereotactical Theory

The stereotactical approach considers the geometrical shape of the skull-brain interface, the close interactions between the two structures during their relative movements, and the resultant pressure waves propagation.

The shape of the skull-brain interface is approximately spherical. Skull-brain relative movements, caused by acceleration phenomena (linear or rotational) and by skull vibrations, generate secondary pressure waves with an approximately spherical wave front. Because brain tissue is isotropic on concentric planes, the wave propagation velocity toward the deep cerebral structures is spatially homogenous.

C = (E/r)0,5
C = wave propagation velocity; E = resilience; r = density

The spherical shape of the wave front is thus preserved. Its spoke and its surface progressively decrease. Despite attenuation phenomenon and, according to the law of energy conservation, the amplitude of the pressure waves, and thus the pressure gradient, progressively increase toward the deep cerebral structures. It will be maximal in the geometrical center of the implied skull vault segment (figure 1), particularly if no prior significant energy consumption process occurs in the superficial cerebral structures. If such a superficial cerebral contusion occurs, a pressure wave "shadow cone" is delimited towards the deep cerebral structures and thus stereotactical summation phenomena are partly disturbed.

Figure 1: The stereotactical concept illustrated on a sagital MRI view

In low or medium-energy impacts, skull vibrations play a significant role in generating successive wave fronts. Cumulative effects related to temporal summation phenomena thus add to the spatial (stereotactical) ones.

In high-energy impacts, acceleration phenomena are predominant. Because of skull fractures that often occur, skull vibrations are disturbed and their stereotactical consequences reduced. Therefore, high-acceleration effects diminish the relative consequences of skull vibrations.

Discussion

Stereotactical phenomena explain common neurological signs

Stereotactical phenomena explain why initial and reversible loss of consciousness (IRLC) is the most common posttraumatic neurological sign, even if the involved structure - the ascendant reticulate matter (ARM) - is located in the deep cerebral regions. It can also explain why, after IRLC, most patients don't have any focal neurological deficit (motor, sensate or visual) related to superficial cerebral-structure lesions, or functional impairment.

Functional recovery is faster for neuronal circuits with fewer infrastructure lesions so if superficial lesions were more important than deep ones, recovery from focal deficits would be longer than recovery of consciousness.

Stereotactical phenomena also explain the high incidence of memory disturbances after a head trauma as the result of functional impairment or lesions of the periventricular neuronal circuits. To our best knowledge, this is the first theory to explain these clinical phenomena. The isolated functional impairment of the ARM could also be explained by the fact that its neuronal fibers are less resistant because they are nonmyelinated. This argument is not applicable to myelinated neuronal fibers whose functional impairment or lesions generate frequent posttraumatic memory disturbances.

Stereotactical phenomena explain the deep cerebral lesions

The stereotactical approach can also explain preferential localisation of DAI in the corona radiata, corpus callosum, fornix and upper brainstem (8). These anatomical regions correspond to geometrical centers of different skull vault segments. Deep traumatic cerebral hematomas can also be better understood since they occur close to the geometrical center of the skull vault.