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ISSN: 2329-6895
Journal of Neurological Disorders
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MRI Characterizations of Region Specific White Matter Hyperintensities and Vertebral Artery Stenosis

Liya Wang1,2, Adrian Lam3, John Oshinski1,2 , Xiaodong Zhong4, Chad A Holder1, Felicia Goldstein5, Diana Ge2 and Hui Mao1,2*
1Department of Radiology and Imaging Sciences, Emory University School of Medicine, Atlanta, Georgia, USA
2Center for Systems Imaging, Emory University, Atlanta, Georgia, USA
3Department of Biomedical Engineering, Georgia Institute of Technology, Atlanta, Georgia, USA
4MR R&D Collaborations, Siemens Healthcare, Atlanta, Georgia, USA
5Department of Neurology, Emory University School of Medicine, Atlanta, Georgia, USA
Corresponding Author : Hui Mao, PhD
Professor, Department of Radiology and Imaging Sciences
Emory University School of Medicine
Atlanta, Georgia, USA
Tel: 404-712-0357
E-mail: [email protected]
Received June 20, 2014; Accepted August 14, 2014; Published August 18, 2014
Citation: Wang L, Lam A, Oshinski J, Zhong X, Holder CA, et al. (2014) MRI Characterizations of Region Specific White Matter Hyperintensities and Vertebral Artery Stenosis. J Neurol Disord 5:178. doi: 10.4172/2329-6895.1000178
Copyright: © 2014 Wang L, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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Abstract

Cerebrovascular diseases cause brain degeneration and subsequent decline of cognitive functions. In this study, comprehensive magnetic resonance imaging approaches with both structural and blood flow imaging were used to characterize the white matter hyperintensity in the brain, cerebral blood flow, and obstruction of vertebral artery caused by stenosis in various cases of individuals with cerebral vascular and cardiovascular risks. It is demonstrated that vertebral artery stenosis characterized as vertebral artery narrowing and/or reduced blood flow velocity by MRI may be associated with the regional specific cerebral vascular comorbidities detected as white matter hyperintensity and reduction of cerebral blood flow. More specifically, unilateral vertebral artery stenosis led to asymmetric periventricular WMHs, while bilateral vertebral artery with lower blood flow led to symmetric periventricular WMHs. The comprehensive MRI protocol with functional and high resolution structural imaging sequences is capable of providing valuable information on blood flow supply in the vertebral artery and cerebrovascular ischemia in individuals having vertebral and cardiovascular abnormalities.

Abstract
Cerebrovascular diseases cause brain degeneration and subsequent decline of cognitive functions. In this study, comprehensive magnetic resonance imaging approaches with both structural and blood flow imaging were used to characterize the white matter hyperintensity in the brain, cerebral blood flow, and obstruction of vertebral artery caused by stenosis in various cases of individuals with cerebral vascular and cardiovascular risks. It is demonstrated that vertebral artery stenosis characterized as vertebral artery narrowing and/or reduced blood flow velocity by MRI may be associated with the regional specific cerebral vascular comorbidities detected as white matter hyperintensity and reduction of cerebral blood flow. More specifically, unilateral vertebral artery stenosis led to asymmetric periventricular WMHs, while bilateral vertebral artery with lower blood flow led to symmetric periventricular WMHs. The comprehensive MRI protocol with functional and high resolution structural imaging sequences is capable of providing valuable information on blood flow supply in the vertebral artery and cerebrovascular ischemia in individuals having vertebral and cardiovascular abnormalities.

 

Keywords
Magnetic resonance imaging; Brain; White matter; Vertebral artery stenosis; Vascular disease; Blood flow rate
Introduction
Increasing evidence has shown that cerebrovascular disease may contribute to the development of mild cognitive impairment (MCI) and dementia as well as the pathogenesis of Alzheimer's disease (AD) [1]. One indicator of cerebrovascular diseases is white matter hyperintensities (WMHs) observed by magnetic resonance imaging (MRI), which appear as high-signal foci within the subcortical white matter in T2-weighted spin-echo and fluid attenuated inversion recovery (FLAIR) images. Earlier reports have shown a greater severity of WMHs among patients with AD. Our recent work also suggests that WMH may be associated with the reduction of white matter integrity which is linked to the cognitive decline [2]. While WMHs are commonly found in patients with symptomatic cerebrovascular disease, they can also be seen in individuals with cardiovascular risk factors, such as hypertension and atherosclerosis. Therefore, it is important to examine the roles of multiple dimensions of vascular risk factors and how the progression of cerebrovascular disease facilitates the white matter degeneration and cognitive decline. One specific interest is to examine the association between cerebral vascular abnormalities and carotid and/or vertebral artery stenosis. Carotid and vertebral arteries channel oxygenated blood to the posterior part of the brain. Atherosclerosis, or hardening of the arteries, mostly due to fatty substance deposition and plaque formation, can lead to narrowing of the blood vessels. Several studies have assessed the relationship between WMHs and the risk of stroke, dementia, and carotid artery diseases [3-5]. However, the optimal management of vertebral artery stenosis has received limited attention, and is not well understood [6]. Unlike carotid diseases, the prognosis of symptomatic vertebral artery stenosis is also largely unknown [7]. This partly reflects difficulties in imaging of extracranial vertebral artery adequately.
MRI is sensitive for detecting anatomic and pathological abnormalities with exquisite soft tissue contrast and high spatial resolution. In addition to characterization of cerebral tissue integrity and infarcts, such as WMHs, MRI also offers capabilities to examine vascular structure and function. For example, relative cerebral blood flow (relCBF) and volume can be measured using Arterial Spin Labeling (ASL) perfusion imaging without administration of exogenous contrast agents. In ASL a radiofrequency pulse is used to tag the inflow blood in a section of the carotid artery and subsequently measure the amount of tagged blood in the brain [8]. By applying velocity-encoding gradients, Phase Contrast Magnetic Resonance Imaging (PCMR) acquires the phase information from the images to calculate the velocity of the blood flow in arterial vessels [9-10]. Furthermore, Magnetic Resonance Angiography (MRA) techniques can generate blood vessel images for identification of stenosis, occlusions, aneurysms or other vasculature obstructions from high-resolution images [11,12]. Therefore, it is possible to study cerebral vascular abnormalities and function as well as obstruction of proximal extracranial vertebral artery with these non-invasive and clinically feasible neuroimaging methods in the same imaging session.
Here we present various cases of MRI examinations of individuals with cerebral vascular and cardiovascular risks to demonstrate the association between extracranial vertebral artery stenosis evidenced by obstructed artery and blood flow velocity and cerebral vascular comorbidities, particularly WMHs and reduction of cerebral blood flow in specific brain regions.
Material and Methods
Subjects
This study was approved by the local Institutional Review Board for the human subject research. Written consents were obtained from fifteen consecutive participants (3 men, 12 women; average age of 60.1 ± 9.1 years old) before the study. Based on vertebral artery stenosis and the specific location of WMHs, 15 subjects were grouped into: 1) left vertebral artery stenosis with bilateral asymmetric periventricular WMHs (n=4), 2) right vertebral artery stenosis with bilateral asymmetric periventricular WMHs (n=7), and 3) bilateral vertebral arteries stenosis with similar caliber with bilateral symmetric periventricular WMHs (n=4). All participants did not have histories or findings suggestive of stroke as determined by reviewing their medical records and a neurologic exam.
MRI acquisition and data analysis
The MRI protocol included whole-brain T2 weighted fast spin echo imaging, FLAIR imaging, ASL perfusion imaging, PCMR, and MRA imaging. All images were acquired on a whole body 3T MRI scanner (Siemens Tim Trio, Siemens Healthcare, Erlangen, Germany) using a standard 12-channel head coil and a four-element phased array carotid coil (Machnet, Maastricht, The Netherlands) when needed.
T2 weighted fast spin echo images (TR=4900 ms and TE=110 ms) were collected with 60 slices, 2 mm thickness and no gap, followed by a FLAIR sequence, with TR=6000 ms and TE=81 ms with 27 slices and 4 mm slice thickness to detect WMHs. A 3D TOF sequence was then performed to provide bright blood signal, 60-slice region of interest (ROI) centered at the carotid bifurcation to obtain high signal-to-noise (SNR), high resolution images for evaluation of the vessel lumen.
PCMR images encoded for through-plane blood velocity were acquired at the inlet of the common carotid artery (CCA) at the same location as the proximal slice of the 3D-TOF image stack. The imaging parameters included 30 cardiac phases, pixel size=1.1X1.1 mm2, slice thickness=6 mm, and VENC=100 cm/s. The proximal extracranial vertebral arteries and the internal carotid arteries were processed offline using Segment (Medviso AB, Lund, Sweden) [13]. Vessel borders were drawn on magnitude images and contours were transferred directly to the corresponding phase images. Pixel-by-pixel velocity values were then integrated over the region of interest (ROI) to obtain flow rates for each time point. Net flow over the cardiac cycle was quantified from these time dependent flow rate data.
ASL images were acquired using single-shot echo-planar imaging (EPI) [14,15], consisting of five 8-mm-thick slices with 2-mm gaps with an in-plane resolution of 2.3X2.3 mm2 oriented 10° up from the anterior-posterior commissural line and covered the volume above this line. Other acquisition parameters were as follows: TR/TE=2500/15 ms, TI1 (start time of the periodic saturation pulses)=700 ms, TI2 (time from labeling pulse to the excitation pulse)=1800 ms, saturation stop time=1600 ms, and flow limit=100 cm/s. Relative cerebral blood flow (relCBF) was generated inline on the scanner by the ASL sequence for assessing possible cerebral hypoperfusion [16,17].
Results
The demographics and specific findings of all subjects are summarized in Table 1. Unfortunately, no diagnostic records were collected, therefore the pathology information of the patients were unknown.
Unilateral vertebral artery stenosis led to asymmetric periventricular WMHs
Among 15 cases collected in this study, seven presented right vertebral artery stenosis with asymmetric periventricular WMHs in the occipital horns, which was more pronounced in the ipsilateral occipital region. These WMHs observed in both T2 weighted (Figure 1A) and FLAIR (Figure 1B) images appear as a hyperintense band with variable thickness located along the dorsolateral angles of the ventricles close to the ependymal surface. The reduction of relCBF was found in the bilateral occipital lobes, but predominantly in the right occipital lobe, as shown in Figure 1C, which was consistent with the significant narrowing of right extracranial vertebral artery (>80%) observed in 3D TOF MRA (Figure 1D). However, the sizes of the bilateral carotid arteries were similar as shown in Figure 1D and 1E. The internal diameter of the right vertebral artery was measured at 2.4 mm. In comparison, the internal diameters of the left vertebral artery, right carotid artery, and left carotid artery were 4.6 mm, 7.2 mm, and 8.4 mm, respectively (Figure 1F). PCMR confirmed there was decreased blood flow velocity in the right vertebral artery (arrow, Figure 1G), comparing to the left one (Figure 1H).
Figure 2 presents another example about unilateral vertebral artery stenosis leading to ipsilateral periventricular WMHs. In four cases with left vertebral artery stenosis, they all exhibited unilateral vertebral artery stenosis that can be associated with bilateral asymmetrical periventricular WMHs, which was more pronounced in the left occipital horns in T2 weighted imaging (Figure 2A). Furthermore, the FLAIR image revealed such asymmetrical appearances of WMHs in the occipital horn along with punctuate and confluent lesion adjacent to the occipital horn of the anterior periventricular areas (Figure 2B). In this case, the FLAIR image was found to have a better sensitivity to WMHs than T2 weighted imaging, especially for those at periventricular locations. Besides identifying infarcts from structural imaging, relCBF map calculated from the ASL images demonstrated decreased relCBF in the left rostral occipital cortex and parietal cortex, including angular gyrus, supramarginal gyrus, and postcentral gyrus (Figure 2C). MRA of head and neck generated from 3D TOF MRI (Figures 2D and 2E) showed marked narrowing of the left proximal extracranial vertebral artery (>70%) with the internal diameter measured at 3.2 mm, comparing to 5.7 mm diameter of the right vertebral artery. The diameters of carotid arteries were 6.5 mm (left) and 7.7 mm (right), respectively (Figure 2F). The flow velocity calculation based on PCMR (Figure 2G) suggested that there was a decrease in blood flow rate in the left proximal extracranial vertebral artery, but not in the right extracranial vertebral artery and bilateral carotid artery as shown in Figure 2H. These findings suggest that periventricular WMHs in the occipital horn might be caused by ipsilateral vertebral artery stenosis.
Bilateral vertebral artery with lower blood flow led to symmetric periventricular WMHs
We also found four cases that showed symmetrical minor WMHs in the areas of bilateral periventricular occipital horns seen in T2 weighted images (Figure 3A), which were more pronounced in the FLAIR image (Figure 3B). The lesions mostly appeared as punctuate WMHs adjacent to the bilateral occipital horns. No juxtacortical or posterior fossa lesions were observed. The relCBF map revealed decreased CBF in bilateral occipital regions (Figure 3C), although no significant major vessel stenosis or occlusion was observed in bilateral proximal extracranial vertebral artery (Figure 3D and 3E). The internal diameter of the right vertebral artery, left vertebral artery, right carotid artery, and left carotid artery were 4.9 mm, 5.2 mm, 6.7 mm and 6.4 mm, respectively (Figure 3F). However, blood flow velocity appeared to be slow in the bilateral proximal extracranial vertebral artery detected in PCMR (Figure 3G). The relevant changes were plotted in Figure 3H. These findings suggest that low blood flow velocity might contribute to the cause of WMHs in the periventricular occipital horns even though no apparent bilateral extracranial vertebral artery narrowing was observed. From the neuroimaging technique perspective, PCMR with information on flow velocity seems to provide more sensitive and specific detection of vasculature abnormalities in the extracranial vertebral arteries than 3D TOF MRI due to its quantitative capability.
Discussion
WMHs commonly seen on MR images are related to various neurological disorders, including cerebrovascular diseases, cardiovascular diseases, dementia, and psychiatric disorders[18]. Although the pathogenic mechanisms of periventricular WMHs are still under investigation [19], it has been increasingly believed that ischemic cerebrovascular disease, not only from carotid artery disease, but also due to vertebral artery stenosis, is one of the common causes of posterior circulation ischemia and leads to cerebral WMHs.
Extracranial vertebral artery is affected by several pathological processes. Stenosis of the vertebral artery can occur in either its extra‐ or intracranial portions, and may account for up to 20% of posterior circulation ischemic strokes [20-23]. Some studies have reported that atherosclerotic disease at the first part of the vertebral artery was commonly associated with similar disease in the internal carotid artery [24,25] because both vertebral arteries feed into one basilar artery. However, none of the isolated vertebral artery stenosis develops into posterior circulation infarction [26]. The findings of this study demonstrated that the vertebral artery obstruction due to either unilateral or bilateral stenosis may cause reduction of cerebral blood supply and subsequent periventricular white matter damage in the occipital area. More specifically, we found unilateral vertebral artery stenosis without bilateral carotid artery ischemia contributed to WMHs in either ipsilateral or bi-periventricular occipital horns (Figures 1 and 2). On the other hand, symmetric WMHs could be found in bi-periventricular occipital horns in FLAIR or T2 weighted imaging (Figure 3), when extracranial vertebral artery had symmetric narrowing but without carotid artery blood flow reduction.
In addition to report the findings of possible association between extracranial vertebral artery and cerebral white matter ischemic damage, we presented a MRI protocol combining T2 weighted imaging, FLAIR, 3D TOF MRA, and PCMR to characterize extracranial vertebral artery stenosis, vertebral artery the blood flow velocity change and related structural and vascular abnormaities in the brain. This neuroimaging protocol provides comprehensive and multi-dimensional assessment of "function-structure" relationships of the brain and vasculature. It is translational and clinically feasible when there is a need for obtaining a systematic characterization of cerebral vascular diseases.
We recognize that the current study is limited by the sample size, making it difficult to perform typical statistical analysis. A quantitative correlation between the degree of WMHs and the severity of extracranial vertebral artery stenosis would greatly enhance and validate the preliminary findings presented here. Thus, the results from this study will need to be further validated with more extensive and quantitative investigations in the future.
Conclusions
We demonstrated that vertebral artery stenosis characterized as vertebral artery narrowing and/or reduced blood flow velocity by MRI may be associated with the regional specific cerebral vascular comorbidities detected as white matter hyperintensity and reduction of cerebral blood flow. This comprehensive MRI protocol with functional and high resolution structural imaging sequences is capable of providing valuable information on blood flow supply in the vertebral artery and cerebrovascular ischemia in individuals having vertebral and cardiovascular abnormalities.
Acknowledgement
This study was supported in part by a seed grant from a NIH Program Project Grant P50AG025688 to Emory Alzheimer's Disease Research Center (ADRC).
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