Mri-Flair Intraventricular CSF Pulsation Artifacts (VCSFA) in UWS Patients

Jesús Perez-Nellar¹, Calixto Machado*², Rafael Rodríguez³, Yanin Machado², Mauricio Chinchilla ², Arthur Schiff ⁴, Beata Drobná Sániová ⁵, Michal Drobný ⁵

1. Hermanos Ameijeiras Hospital, Stroke Unit, Havana, Cuba.

2. Institute of Neurology and Neurosurgery, Department of Clinical Neurophysiology, Havana, Cuba

3. International Center for Neurological Restoration, Havana, Cuba

4. Emory University School of Medicine, 201 Dowman Dr, Atlanta, GA 30322

5. Comenius University in Bratislava, Slovak Republic

Corresponding Author: Calixto Machado, MD, Ph.D., FAAN, President, Cuban Society of Clinical Neurophysiology, Instituto de Neurología y Neurocirugía, 29 y D, Vedado, Apartado Postal 4268, La Habana 10400.

Copy Right: © 2022 Calixto Machado, MD, Ph.D., FAAN, This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Received Date: November 16, 2022

Published Date: December 01, 2022

Abstract

One of the major limitations of FLAIR imaging is the ventricular CSF pulsation artifact (VCSFA). This artifact could compromise the study of ventricular abnormalities by leading to false-negative or false-positive interpretations. We report four young unresponsive wakefulness syndrome (UWS) patients with severe ventriculomegaly and brain atrophy who showed VCSFA on MR imaging. FLAIR axial images showed the presence of a hyperintensity occupying the third, fourth lateral ventricles and the aqueduct of Sylvius. VCSFA was more prominent in the third and fourth ventricles compared with the lateral ventricles. In PVS, both severe ventriculomegaly and brain atrophy might induce non-appropriate CSF circulation nulling, which remains hyperintense on axial FLAIR images, leading to VCSFA coming out. This is the first report in the literature about the presence of VCSFA in UWS patients.

Keyword: MRI; FLAIR; ventricular CSF pulsation artifact (VCSFA); unresponsive wakefulness syndrome (UWS); cerebrospinal fluid; ventricles.

Introduction

The fast fluid-attenuated inversion recovery (FLAIR) magnetic resonance imaging (MRI) technique was first reported by Hajnal et al.[1, 2] Normal cerebral spinal fluid (CSF) has long T1 and long T2 times manifest as dark signals on T1-weighted images and bright signals on T2-weighted images. FLAIR imaging results in nulling and dark CSF signals. The ability to perform FLAIR imaging with fast spin-echo (FSE) sequences time nulls the CSF signal, providing heavy T2 weighting due to its very long echo time. [3-9]

The superiority of FLAIR imaging compared with T1- and T2-weighted Imaging has been suggested in evaluating various disorders, such as stroke, multiple sclerosis, infections, hypertensive encephalopathy, and cerebral hemorrhage. [4, 5, 9-21]

Nonetheless, one of the major limitations of FLAIR imaging is ventricular CSF pulsation artifact (VCSFA). This artifact could compromise the sensitivity and specificity of FLAIR images by leading to false-negative or false-positive interpretations of ventricular abnormalities. [22-25]

We report four young unresponsive wakefulness syndrome (UWS) patients with marked ventriculomegaly and brain atrophy who showed the VCSFA on FLAIR MRI. This is the first report in the literature about the presence of VCSFA in UWS patients.

Methods

We studied four patients (ranging from 12 to 31 years old) who suffered hypoxic-ischemic insult resulting in UWS of long-term clinical evolution (4-8 years). The patients fulfilled current diagnostic criteria for UWS 26-36: no evidence of awareness of self or environment, no interaction with others, and no comprehension or expression of language. Noxious stimuli frequently resulted in massive stretching or startle reactions without habituation, sometimes with massive flexor responses. They were occasionally grimacing following stimulation. Nonetheless, external stimuli did not evoke purposefully, sustained, and reproducible voluntary behavioral responses. Patients were assessed by the Coma Recovery Scale Revisited (CRS-R).27, 37-39 Patients' demographic features are summarized in table 1.

Patients were studied by a 1.5T MR scanner (Symphony, Siemens). FLAIR technique description is found elsewhere.40 Two independent observers reviewed MRI studies to detect the VCSFA in the aqueduct of Sylvius and the lateral, third, and fourth ventricles. VCSFA intensity was classified as slight, moderate, and high by the two independent observers.

The Institute of Neurology and Neurosurgery IRB, Havana, Cuba, approved this study.

Results

The VCSFA was found in all patients and was more prominent in the third and fourth ventricles than the lateral ventricles (Table 2).

Figure 1 presents MRI data sets on axial views from patient OC (A to F images). MRI FLAIR axial images showed the VCSFA in the fourth and third ventricles; meanwhile, this artifact was comparatively less pronounced in the lateral ventricles, visualized as small white spots. There was also parenchymal atrophy and white matter hyperintensity. MR T1 axial images of the same patient (D to F) revealed severe brain atrophy in both cerebral hemispheres, associated with dilated ventricles and wide cerebral sulci, but no intraventricular abnormalities were found. The VCSFA was found on axial images in one patient but was not detected on sagittal planes.

Figure 2. shows the FLAIR axial image of patient AG demonstrating fourth and third ventricular CSF pulsation artifacts (arrows). There is severe parenchymal atrophy.

Figure 3 presents the FLAIR axial image of patient JM, demonstrating a huge atrophy with ventriculomegaly. A severe ventricular CSF pulsation artifact (arrows) is visualized in the fourth ventricle (A-B), aqueduct (C), and third ventricle (D-E).

Discussion

The prominent hyperintensity occupying the cerebral ventricles in our patients most probably represents the VCSFA due to an inversion delay and ghosting effects. VCSFA might obscure or mimic intraventricular lesions, especially in the third and fourth ventricles. [1, 2, 23, 41-52]

The most important contributor to VCSFA is an inflow of non-nulled cerebral spinal fluid (CSF) from the superior or inferior areas. When CSF goes into the brain sections between the inversion pulse and the commencement of signal sampling, it is not appropriately nulled and remains hyperintense on axial FLAIR images. Hence, the causes of VCSFA seem to be multifactorial. [1, 2, 23, 43-49, 53-56]

This is analogous to the signal produced by the inflow of fresh blood on time-of-flight MR angiograms, and only instead of saturation effects, the VCSFA is due to the effects of inversion delay.[23, 57-60] CSF enters the brain sections between the inversion pulse and the beginning of signal sampling; hence, it is not correctly nulled and remains hyperintense on axial FLAIR images. [6, 19, 22, 23, 41, 46, 47, 61-63]

The increased severity and frequency of VCSFA in the third and fourth ventricles are most likely multifactorial. One likely cause is the reflux of spinal CSF into these inferior ventricles through the posterior fossa. A second factor is the increased velocity of CSF flow through the third and fourth ventricles, increasing the rate of superior entry of CSF from the lateral ventricles during the inversion delay. Ghost pulsation effects also appear to contribute to VCSFA. Because CSF is moving in the ventricles, any residual non-nulled CSF will cause pulsation artifacts in many places. One manifestation of this ghosting is the placement of redundant CSF signals across the phase-encoding axis in a manner that could obscure or mimic brain parenchymal lesions. Inflow and ghost pulsation effects are artifacts caused by flow and are thus related. The difference is that optimal gradient moment nulling (e.g., accounting for velocity, acceleration, jerk, etc.) might reduce the effect of ghosting but would not affect the inversion delay artifact. Conversely, wider inversion pulses might help reduce the signal from inflowing CSF, but any moving protons will still cause ghosting of whatever signal they contribute. [11, 23, 46, 47, 64-68]

Bakshi et al. reported that increasing ventricular size and, to a lesser extent, increasing age were significantly associated with VCSFA. [23] In UWS cases is frequent to find marked brain atrophy and ventriculomegaly. These morphological features put forth their maximal force on the CSF circulation. Ventriculomegaly may induce an increment of CSF flow velocity through the third and fourth ventricles. [34, 35, 69, 70]

Another possible mechanism could be the reflux of spinal CSF into the fourth and third ventricles from the cisterna magna. Some authors have shown increased passage of subarachnoid dye into the fourth ventricle from the cisterna magna in cases of ventriculomegaly due to brain volume loss, as occurs in hydrocephalus. [71-73] This reflux may also be enhanced in normal-pressure and pyogenic meningitis.[74-76]

Brain atrophy might produce a decrement in the compliance of periventricular tissues that may allow for the more vigorous transmission of systolic and diastolic pulsations to the ventricles, further increasing CSF velocity. These strong CSF pulsations that occur in synchrony with the systole and diastole set forth their maximal force at the base of the brain through the third ventricle, where CSF velocities are also maximal. Hence, marked ventriculomegaly and brain atrophy might explain the presence of the VCSFA in UWS cases because CSF circulation might not be appropriately nulled, remaining hyperintense on MR axial images. [23, 72, 74, 77-79] 

In one case, the VCSFA was found on axial images, but it was not detected on sagittal planes. This is likely because sagittal Imaging induces the required nulling of in-plane midline brain and cervical spinal CSF before the fluid arrives at the third and fourth ventricles during readout. (i.e., CSF flow remains in-plane, and no inflow of non-nulled CSF occurs). [23, 80]

Several authors have proposed technical variations to reduce this artifact, such as using a wider slice-selective inversion to increase the inversion of CSF outside the imaging section or using other section-selective inversion pulses to utilize cardiac synchronization during MRI acquisition.[81-83]  Other authors have recommended using a non-slice-selective inversion pulse to eliminate the VCSFA using the K-space reordered by Inversion-time for each Slice Position (KRISP) technique in order to achieve constant contrast in a multislice acquisition.[46, 47]

We conclude that it is extremely important to consider the possible presence of VCSFA in UWS patients because it may induce false-negative or false-positive diagnoses of intraventricular abnormalities.

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