Acute pressure changes in the brain are correlated with MR elastography stiffness measurements: initial feasibility in an in vivo large animal model

Abstract

Purpose: The homeostasis of intracranial pressure (ICP) is of paramount importance for maintaining normal brain function. A noninvasive technique capable of making direct measurements of ICP currently does not exist. MR elastography (MRE) is capable of noninvasively measuring brain tissue stiffness in vivo, and may act as a surrogate to measure ICP. The objective of this study was to investigate the impact of changing ICP on brain stiffness using MRE in a swine model.

Methods: Baseline MRE measurements were obtained, and then catheters were surgically placed into the left and right lateral ventricles of three animals. ICP was systematically increased over the range of 0 to 55 millimeters mercury (mmHg), and stiffness measurements were made using brain MRE at vibration frequencies of 60 hertz (Hz), 90 Hz, 120 Hz, and 150 Hz.

Results: A significant linear correlation between stiffness and ICP in the cross-subject comparison was observed for all tested vibrational frequencies (P ≤ 0.01). The 120 Hz (0.030 ± 0.004 kilopascal (kPa)/mmHg, P < 0.0001) and 150 Hz (0.031 ± 0.008 kPa/mmHg, P = 0.01) vibrational frequencies had nearly identical slopes, which were approximately two- to three-fold higher than the 90 Hz (0.017 ± 0.002 kPa/mmHg, P < 0.0001) and 60 Hz (0.009 ± 0.002 kPa/mmHg, P = 0.001) slopes, respectively.

Conclusion: In this study, MRE demonstrated the potential for noninvasive measurement of changes in ICP. Magn Reson Med 79:1043-1051, 2018. © 2017 The Authors Magnetic Resonance in Medicine published by Wiley Periodicals, Inc. on behalf of International Society for Magnetic Resonance in Medicine. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.

Keywords: brain stiffness; intracranial pressure; magnetic resonance elastography; viscoelasticity.

Figure 1

(A) Schematic diagram of surgical dental cement cap and catheter placement through the skull. (B‐D) Catheter trajectory planning using high‐resolution T₁‐weighted images. (B) Oblique‐coronal and (C) axial reconstructed image of pig brain, with the prescribed catheter placements shown in red. (D) Postsurgical axial reconstructed image after catheter placement. One catheter was used to increase ICP, whereas the other catheter was used to continuously monitor ICP. ICP, intracranial pressure.

Figure 2

MRI schematic diagram of postsurgical MR elastography, imaging, and pressure‐monitoring setup. Hz, hertz.

Figure 3

Anatomical images of ventricles under different pressure levels postcatheter implantation in pig 1 (top row). The black dashed boxes in the top row have been magnified in the bottom row. For comparison purposes, the ventricles at 0 mmHg have been overlaid in red in all three magnified images. mmHg, millimeters mercury.

Figure 4

Median |G*| (kPa) as a function of intracranial pressure at 60 Hz, 90 Hz, 120 Hz, and 150 Hz vibration frequencies, and for all three pigs. Hz, hertz; kPA, kilopascal; mmHg, millimeters mercury.

Figure 5

Cross‐subject median change in |G*| as a function of frequency and intracranial pressure for all three pigs. The linear regression lines for each vibration frequency have been plotted. Hz, hertz; kPA, kilopascal; mmHg, millimeters mercury.

Figure 6

Elastograms (|G*|) of presurgery and postsurgery at baseline and postsurgery at maximum ICP in three pigs and at a 120 hertz vibration frequency. ICP, intracranial pressure; kPA, kilopascal; mmHg, millimeters mercury.

Figure 7

Schematic of hypothetical stress‐strain curve (top‐right axes, red dashed line) as a possible explanation for the observed stiffness‐pressure measurements (bottom‐left axes, solid black squares) in pig 1 (120 Hz). At each pressure, the slope of the stress‐strain curve corresponds to the stiffness of the brain parenchyma. In the linear region, the slope of the stress‐strain curve is constant across all pressures; that is, the stiffness remains constant. In the nonlinear region, the slope is continually increasing, thus giving rise to increasing stiffness. Assuming that pressure is the dominant factor, the presurgical baseline‐stiffness measurement (black dashed line) suggests that normal brain function occurs in the nonlinear region of the stress‐strain curve. >Hz, hertz; kPA, kilopascal; mmHg, millimeters mercury.