Neuroimaging of Adult Hydrocephalus

Ventricle expansion and disproportionately enlarged subarachnoid-space hydrocephalus (DESH) are the hallmark features of idiopathic normal-pressure hydrocephalus, which has recently also been referred to as Hakim’s disease. DESH refers to the unbalanced distribution of CSF in the subarachnoid space characterized by tightened sulci in the high convexities and Sylvian fissure dilation. The ventricles and Sylvian fissure expand in the parietal direction. This process compresses the brain and subarachnoid space around the parietal region. In addition to 2-dimensional imaging indicators, this study describes new 3-dimensional and 4-dimensional imaging indicators.

Key points

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Idiopathic normal pressure hydrocephalus is not characterized solely by ventricular enlargement.
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The most important imaging finding is disproportionately enlarged subarachnoid-space hydrocephalus (DESH).
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The callosal angle and brain–ventricle ratio are the most useful for quantitatively determining DESH.

Abbreviations

BVR	brain–ventricle ratio
CA	callosal angle
CAPPAH	convexity apparent hyperperfusion
CSF	cerebrospinal fluid
CT	computed tomography
DAT	dopamine transporter
DESH	disproportionately enlarged subarachnoid-space hydrocephalus
iNPH	idiopathic normal-pressure hydrocephalus
IVIM	intravoxel incoherent motion
PC	phase-contrast
PVH	periventricular hypodensity
ROI	region of interest
SFD	Sylvian fissure dilation
SINPHONI	study of idiopathic normal-pressure hydrocephalus on neurologic improvement
THC	tightened high-convexity
Time-SLIP	Time-spatial labeling inversion pulse

Introduction

Neuroimaging is essential for the diagnosis of hydrocephalus. Typically, the ventricles are enlarged in patients with hydrocephalus. However, the mechanism underlying ventricular enlargement remains largely unknown, partly because of a significant paradigm shift in the hypothesis underlying cerebrospinal fluid (CSF) dynamics in the last decade. Chronic hydrocephalus in adults is believed to be caused by the chronic accumulation of CSF in the cranial cavity because of aging and various risk factors. Importantly, the ventricles and subarachnoid space, which account for the majority of CSF, expand simultaneously. However, many physicians still believe that “hydrocephalus is a disease characterized by the enlargement of the ventricles within the brain,” which often leads to misinterpretations as “cerebral atrophy” and misdiagnoses as Alzheimer’s disease. A key imaging finding for differentiating idiopathic normal-pressure hydrocephalus (iNPH) from cerebral atrophy is disproportionately enlarged subarachnoid-space hydrocephalus (DESH), as described later. This article delineates the imaging findings and indices characteristic of iNPH using computed tomography (CT) scans and MRI.

Evans Index

The most famous global index for ventricular enlargement is the Evans Index, proposed by Dr William A. Evans Jr. in 1942. When it was first proposed, it was measured on a pneumoencephalography frontal view (an X ray taken after injecting air into the ventricles via the lumbar region). The Evans Index was defined as the ratio of the maximum width of the frontal horns of the lateral ventricles to the maximum internal diameter of the skull. Values of 0.20 to 0.25 are considered normal, values of 0.25 to 0.30 indicate a tendency toward ventricular enlargement, and values greater than 0.30 indicate ventricular enlargement. With the advent of CT scan and MRI, pneumoencephalography is no longer performed. The Evans Index is now defined as the maximum width of the frontal horns of the lateral ventricles divided by the maximum intracranial diameter in the same section of the axial slice in which the frontal horns are most enlarged, obtained from either CT or MRI ( Fig. 1 ). The Evans Index is useful as an indicator of ventricular enlargement in many types of hydrocephalus but is unsuitable for iNPH. The Evans Index has a long history as an indicator of ventricular enlargement and is widely known even among nonspecialists. However, the anterior horn of the lateral ventricle is not easily enlarged in iNPH horizontally in the lateral X -axis direction. ^, Even after shunt surgery, this index least likely changes compared with the following indices. ^, It is not suitable for assessing ventricular enlargement in iNPH. Furthermore, healthy elderly individuals over the age of 65 years also experience ventricular enlargement because of age-related brain atrophy, with an Evans Index greater than 0.3 being considered within the normal range. Furthermore, the average Evans Index for 80-year-old men has been reported to be 0.3. Therefore, there is a risk of overestimating ventricular enlargement in healthy elderly individuals who do not have pathologic ventricular enlargement, making the Evans Index generally unsuitable for assessing ventricular enlargement in the elderly. Then, what should we use as an index of ventricular enlargement instead of the Evans Index? The most reliable method for quantitatively assessing ventricular enlargement is 3-dimensional (3D) measurement; however, we present and recommend some 2-dimensional (2D) indices that can be easily measured.

Z-Evans Index

In chronic hydrocephalus in adults, excluding iNPH disease, the ventricles usually enlarge in all directions, making it possible to detect ventricular enlargement, regardless of the site or direction of measurement within the ventricles. However, in iNPH, the increased CSF tends to expand into intracranial CSF spaces that are easier to enlarge, leading to a wide variation in ventricular enlargement. Furthermore, the Sylvian fissures, which are located laterally to the lateral ventricles, often enlarge simultaneously, making it difficult for the lateral ventricles to enlarge in the lateral X -axis direction. Therefore, whether the lateral ventricles are more likely to expand antero-posteriorly in the Y -axis direction or vertically in the Z -axis direction was investigated. We found that they are more likely to expand in the Z -axis direction. Therefore, in analogy to the Evans Index, the Z-Evans Index was defined as the ratio of the maximum width of the frontal horns of the lateral ventricles in the Z -axis direction to the median cranial diameter on a coronal section passing through the anterior commissure to posterior commissure line (AC–PC line) using CT or MRI ( Fig. 2 ). A useful cutoff value for detecting ventricular enlargement in iNPH was reported to be 0.42. The median cranial diameter on the coronal section passing through the AC was used as the denominator. In 2 individuals in this figure, it passed through the sella turcica; however, it has been pointed out that the median coronal section can sometimes pass through the anterior or posterior clinoid processes because of individual differences in the inclination of the AC–PC line.

Callosal angle

The corpus callosum is a bundle of fibers that connect the left and right cerebral hemispheres, located just above the bilateral ventricles. In iNPH, expansion of the lateral ventricles in the Z -axis direction causes strong compression of the corpus callosum, resulting in thinning and V-shaped deformation of the corpus callosum. The reasons for this V-shaped deformation are believed to be that the corpus callosum is pushed upward due to the rigid falx cerebri that separates the 2 cerebral hemispheres, and it is compressed from both sides toward the median superior direction because of the expansion of the Sylvian fissures. The falx moves deeper toward the posterior region, where it connects to the tentorium cerebelli, which separates the cerebrum from the cerebellum, making the posterior region more prone to strong V-shaped deformations. The degree of V-shaped deformation of the corpus callosum is indicated by a narrowing callosal angle (CA). The upper walls of the bilateral ventricles vary more toward the posterior than toward the anterior. The measurement is defined on a coronal CT or MRI that intersects the AC–PC line perpendicularly and passes through the PC ( Fig. 3 ). A useful cutoff value for detecting ventricular enlargement in iNPH was reported to be 90° with an accuracy of greater than 90%. This cutoff value is also useful as an indicator of improvement after surgery. ^, The CA is globally recognized as a useful indicator for diagnosing iNPH. In patients with iNPH, in whom the ventricles are elongated in the superior direction, creating holes in the septum pellucidum and blunting the CA, or in patients with a cavum septum pellucidum or cavum vergae, the CA can be blunted and exceed 90°.

Brain–ventricle ratio

We hypothesized that the compression of the brain and subarachnoid space at the high parietal convexity region due to the superior Z -axis expansion of the lateral ventricles is the reason for the morphologic changes specific to iNPH and thus devised the brain–ventricle ratio (BVR), which is defined as the ratio of the maximum Z -axis width of the brain immediately above the lateral ventricles to the maximum Z -axis width of the frontal horns of the lateral ventricles on the coronal section passing through the AC ( Fig. 4 ), similar to the Z-Evans Index. The cutoff value is reported to be less than 1.0 (ie, the width of the ventricles is greater than the width of the brain). The BVR at the AC level is measured as the maximum z -axial length of the brain just above the lateral ventricles (yellow line) divided by the maximum length of the lateral ventricles (cyan line). When the coronary plane passes through the AC, the value will be greater than 1.0, and when the plane passes through the PC, it is less than 1.5. This figure shows that z -EI = 46.7/95.0 = 0.49 >0.42 and BVR at the AC level = 28.1/46.7 = 0.6 <1.0.

Disproportionately enlarged subarachnoid-space hydrocephalus

The term DESH was first reported by Hashimoto and colleagues as the first paper of the multicenter collaborative prospective cohort study of idiopathic normal-pressure hydrocephalus on neurologic improvement (SINPHONI) in 2010. However, before this report, in 1998, Kitagaki and colleagues noted the signs of high-convexity/midline subarachnoid space tightness in addition to mild–moderate ventricular enlargement in an MRI volumetry-based study. Recently, many experts have agreed that DESH is the most important imaging feature for detecting or avoiding misdiagnosis of iNPH ( Fig. 5 ). ^, DESH refers to the unbalanced distribution of CSF in the subarachnoid space characterized by the presence of tightened sulci in the high convexities (THC) and Sylvian fissure dilation (SFD). A possible hypothesis for the characteristic CSF distribution in DESH is as follows: the CSF volume increases slowly with aging. The CSF spreads sequentially to spaces that are easier to enlarge, such as the ventricles and subarachnoid spaces, and finally connects directly to alternative pathways other than the foramina of Magendie and Luschka, resulting in iNPH. An alternative CSF pathway is the inferior choroidal point of the choroidal fissure, in which the inferior horn of the lateral ventricles and ambient cistern are separated by a thin membrane called tenia at the choroid plexus base attachment, and arteries and veins run through this thin membrane, which is connected by the tenia extension of the hippocampal fimbria ( Fig. 6 ). The superior wall of the third ventricle also has a choroid plexus bordering the velum interpositum, which interfaces with the third ventricle and quadrigeminal cistern. This also serves as an alternative direct CSF pathway. We also considered that the subarachnoid spaces, with reduced arachnoid columns lining the basal cistern and Sylvian fissure, would likely enlarge similarly to the ventricles. In iNPH, the ventricles, basal cistern, and Sylvian fissure expand in unison similar to a single sink that stores CSF and is more likely to expand depending on the density of the arachnoid columns.