Deformation of the human brain induced by mild angular head acceleration

https://doi.org/10.1016/j.jbiomech.2007.09.016Get rights and content

Abstract

Deformation of the human brain was measured in tagged magnetic resonance images (MRI) obtained dynamically during angular acceleration of the head. This study was undertaken to provide quantitative experimental data to illuminate the mechanics of traumatic brain injury (TBI). Mild angular acceleration was imparted to the skull of a human volunteer inside an MR scanner, using a custom MR-compatible device to constrain motion. A grid of MR “tag” lines was applied to the MR images via spatial modulation of magnetization (SPAMM) in a fast gradient echo imaging sequence. Images of the moving brain were obtained dynamically by synchronizing the imaging process with the motion of the head. Deformation of the brain was characterized quantitatively via Lagrangian strain. Consistent patterns of radial-circumferential shear strain occur in the brain, similar to those observed in models of a viscoelastic gel cylinder subjected to angular acceleration. Strain fields in the brain, however, are clearly mediated by the effects of heterogeneity, divisions between regions of the brain (such as the central fissure and central sulcus) and the brain's tethering and suspension system, including the dura mater, falx cerebri, and tentorium membranes.

Introduction

Every year there are over 1.5 million new cases of traumatic brain injuries (TBI) in the US. In addition to the devastating human costs, TBI causes over $56.3 billion in economic losses per year (Thurman, 2001). In spite of its importance and its many years of research interest, TBI is not well understood. It is clear that when the skull is accelerated, the brain deforms in response, but the details of the resulting strain fields are not known. It is widely accepted that skull acceleration can lead to brain injury if local strains and strain rates exceed a critical threshold (Gennarelli et al., 1989; Bain and Meaney, 2000), above which the neural fibers (axons) are affected.

Shear strains due to angular acceleration of the skull have been hypothesized to be especially important in TBI. Holbourn (1943) showed that rotation of the human skull could cause large deformations of a gel housed within its cranial cavity. Pudenz and Shelden (1946) supported Holbourn's claims through visualization of the surface of animal brains. They replaced the top half of a monkey skull with transparent plastic, and filmed the deformation of the brain during linear acceleration.

More recently, quantitative studies of brain deformation have been performed using high-speed filming of gel-filled skulls (Meaney et al., 1995; Margulies et al., 1990), high-speed bi-planar X-ray imaging of the cadaveric brain (Hardy et al., 2001), and MR imaging of the brain in human volunteers (Wedeen and Poncelet, 1996; Reese et al., 2002; Bayly et al., 2005). In studies done with high-speed filming, quantitative estimates of strain (0.20–0.30) were found in gel-filled pig skulls subjected to angular accelerations similar to those that produced axonal injury in the live animal. Because these studies used gel as a surrogate, they could not capture the effects of heterogeneity, anisotropy, vasculature, meninges, and cerebrospinal fluid on brain deformation. Hardy et al. (2001) performed high-speed (250–1000 frames/s) bi-planar X-ray studies of the displacement of 11 neutrally buoyant radio-opaque markers in cadaver brains during head acceleration. Spatial resolution was limited by the sparseness of the array of physical markers; also tissue properties and brain–skull interactions of the cadaver may differ significantly from those of a live subject. Zou et al. (2007) reported estimates of relative rigid-body rotation and translation of the brain and skull, obtained from the X-ray data of Hardy et al. (2001). Wedeen and Poncelet (1996) demonstrated the use of phase-contrast magnetic resonance images (MRI) to measure strains in the brain parenchyma of human subjects during physiological pulsatile motion and voluntary head shaking. Head accelerations during voluntary motion were not measured. Bayly et al. (2005) studied deformation of the human brain in vivo, during controlled linear head acceleration, using tagged MR imaging. This approach provides strain fields with good spatial (2×2×5 mm) and temporal (6 ms/frame) resolution. Results of this study suggest that tethering of the brain at the sellar and suprasellar region plays a central role in determining the mechanical response of the brain during linear skull accelerations (Bayly et al., 2005). Head accelerations were primarily posterior–anterior and were limited to values that are safe for the human test subjects (20–30 m/s2).

An important purpose for measurement of brain deformation is to generate quantitative data to validate computer models. Computer models of the brain (Ruan et al., 1991; Kleiven, 2006; Takhounts et al., 2003; Zhang et al., 2004) offer great potential for studying brain biomechanics, if they are shown to be accurate. For example, simulations could be used to provide estimates of brain deformation for accelerations that would be unsafe for human subjects (as in, for example, Kleiven and von Holst, 2002), or for studies that would be costly, difficult, or inconclusive with cadavers or animals. However, accurate computer simulations require accurate information about the brain's material properties, boundary conditions, and tissue connectivity. It is critically important for computer simulations to be verified by comparison to observations.

The current experimental study was performed to illuminate the mechanical response of the brain to mild angular acceleration. The brain was imaged using dynamic tagged, gated MRI during angular motion of the head in the transverse plane (rotation about the long axis of the neck). Deformation was quantified by computing the two-dimensional (2-D) Lagrangian strain tensor in four parallel axial planes.

Section snippets

Overview

Three adult male subjects of average height and weight (age 25–42 yrs; 70–80 kg; 1.7–1.8 m tall), performed controlled head rotation using a custom, MR-compatible device (Fig. 1) that imparted a repeatable mild angular acceleration of ∼250–300 rad/s2. These accelerations are about 10% of those experienced during heading of a soccer ball (Naunheim et al., 2003). The protocol was reviewed and approved by the Washington University Human Research Protection Office. Tagged MR images were acquired in

Results

Patterns of deformation are illustrated qualitatively by the reference and deformed grids of tag lines in Fig. 6, Fig. 7. In these figures, displacements are amplified by a factor of five, for visualization only. Fig. 6 illustrates the initial deformation as mobile brain tissue rotates clockwise relative to the skull, which has stopped. Because the brain is tethered to the skull by vessels and membraneous connections (e.g., arachnoid granulations) at its base and surface, the decelerating

Discussion

The theory that radial-circumferential shear strain dominates during angular acceleration was first proposed by Holbourn (1943). Holbourn used a gelatin phantom inside a simulated skull to examine strain fields. Results from the present study support his basic theory, though strain patterns differ because Holbourn's simple models lacked true material properties and boundary conditions.

In the current study, values of radial-circumferential shear strain exceeding 0.06 were observed in small

Conflict of interest

None.

Acknowledgments

The technical assistance of Richard Nagel and Linda Hood is gratefully acknowledged. Support from NIH grant NS-55951 is gratefully acknowledged. MRI facilities support was provided by National Cancer Institute Small Animal Imaging Resource (SAIR) Program grant R24-CA83060. This work was also funded in part by the US DOT (NHTSA) grant DTNH22-01-H-07551 and the FHA grant FHWA ICRC(1) via the Southern Consortium on Injury Biomechanics.

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