Real-Time Multifrequency MR Elastography of the Human Brain Reveals Rapid Changes in Viscoelasticity in Response to the Valsalva Maneuver.

Helge Herthum,Heiko Tzschätzsch,Ingolf Sack,Steffen Görner,Josef Pfeuffer,Jürgen Braun,Stefan Hetzer,Mehrgan Shahryari,Carsten Warmuth,Hennes Neubauer,Felix Schrank

doi:10.3389/fbioe.2021.666456

Abstract

Modulation of cerebral blood flow and vascular compliance plays an important role in the regulation of intracranial pressure (ICP) and also influences the viscoelastic properties of brain tissue. Therefore, magnetic resonance elastography (MRE), the gold standard for measuring in vivo viscoelasticity of brain tissue, is potentially sensitive to cerebral autoregulation. In this study, we developed a multifrequency MMRE technique that provides serial maps of viscoelasticity at a frame rate of nearly 6 Hz without gating, i.e., in quasi-real time (rt-MMRE). This novel method was used to monitor rapid changes in the viscoelastic properties of the brains of 17 volunteers performing the Valsalva maneuver (VM). rt-MMRE continuously sampled externally induced vibrations comprising three frequencies of 30.03, 30.91, and 31.8 Hz were over 90 s using a steady-state, spiral-readout gradient-echo sequence. Data were processed by multifrequency dual elasto-visco (MDEV) inversion to generate maps of magnitude shear modulus | G∗| (stiffness) and loss angle φ at a frame rate of 5.4 Hz. As controls, the volunteers were examined to study the effects of breath-hold following deep inspiration and breath-hold following expiration. We observed that | G∗| increased while φ decreased due to VM and, less markedly, due to breath-hold in inspiration. Group mean VM values showed an early overshoot of | G∗| 2.4 ± 1.2 s after the onset of the maneuver with peak values of 6.7 ± 4.1% above baseline, followed by a continuous increase in stiffness during VM. A second overshoot of | G∗| occurred 5.5 ± 2.0 s after the end of VM with peak values of 7.4 ± 2.8% above baseline, followed by 25-s sustained recovery until the end of image acquisition. φ was constantly reduced by approximately 2% during the entire VM without noticeable peak values. This is the first report of viscoelasticity changes in brain tissue induced by physiological maneuvers known to alter ICP and detected by clinically applicable rt-MMRE. Our results show that apnea and VM slightly alter brain properties toward a more rigid-solid behavior. Overshooting stiffening reactions seconds after onset and end of VM reveal rapid autoregulatory processes of brain tissue viscoelasticity.

Highlights

A balance of intracranial mechanical properties is of crucial importance for normal brain function (Linninger et al, 2005; Guyton and Hall, 2006; Wagshul et al, 2006; Schmid Daners et al, 2012)
Using rt-MMRE, we investigate rapid viscoelastic changes during cerebral autoregulation associated with the Valsalva maneuver (VM)
A slight increase in | G∗| was visible in the late VM response, whereas no response of φ was apparent in individual maps

Summary

Introduction

A balance of intracranial mechanical properties is of crucial importance for normal brain function (Linninger et al, 2005; Guyton and Hall, 2006; Wagshul et al, 2006; Schmid Daners et al, 2012). It is likely that regulation of ICP, which is one of the most important vital functions of intracranial mechanics, affects shear viscoelasticity (Perrinez et al, 2009; McGarry et al, 2015; Lilaj et al, 2020). This mechanical component of cerebral autoregulation is largely unstudied due to a lack of imaging techniques that can measure cerebral shear modulus in vivo with high spatial and temporal resolution

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Results

Conclusion