(Stroke. 1997;28:2174-2179.)
© 1997 American Heart Association, Inc.
Articles |
Effect of Extracranial Carotid Artery Stenosis and Other Risk Factors for Stroke on Periventricular Hyperintensity
From the Third Division of Internal Medicine, Shimane Medical University, Izumo (T.A.), and Department of Neurology, Tokyo Saiseikai Central Hospital (M.T., H.H., T.I.) (Japan).
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Abstract |
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Background and Purpose The pathogenesis of periventricular hyperintensity (PVH) is still uncertain. We investigated the relationship between PVH and risk factors for cerebrovascular diseases, especially extracranial carotid artery stenosis (ECAS).
Methods We studied PVH and ECAS in 323 subjects between 1991 and 1994. Using 1.5-T MRI scan images, we measured PVH quantitatively at eight points and evaluated cerebral infarction. Duplex carotid sonography was performed on the carotid arteries bilaterally and used to divide the severity of ECAS into five grades. Risk factors for cerebrovascular diseases and atherosclerotic complications were assessed from the clinical history.
Results Age was significantly correlated with the size of frontal and whole PVH (P<.01). Frontal PVH was significantly more severe in subjects with hypertension (P<.05). Frontal, occipital, and whole PVH were significantly more severe in subjects with a history of cerebrovascular accident (P<.01). Other risk factors and atherosclerotic complications were not correlated with PVH. There were no significant differences in the severity of PVH among the five groups of ECAS. The severity of PVH in each region was not related to ECAS. There was no significant difference in the age of patients in relation to the five grades of ECAS. However, PVH was significantly more severe in subjects with lacunar infarction or infarction of the deep border zone (P<.05). There was no relationship between PVH and cortical infarction or infarction of the cortical border zone.
Conclusions PVH correlated with age, hypertension, and past history of cerebrovascular disease but not with ECAS. PVH was significantly more severe in lacunar infarction and infarction of the deep border zone. These results suggest that small-vessel disease may underlie the pathogenesis and development of PVH.
Key Words: carotid stenosis • small-vessel disease • leukoaraiosis • white matter
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Introduction |
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Periventricular hyperintensity is a frequent finding on brain MRI in the elderly.1 2 3 PVH is generally associated with increasing age,2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 the risk factors for stroke (especially hypertension),4 5 6 8 9 10 11 12 13 14 15 16 17 18 19 21 22 25 27 28 29 30 31 32 a history of stroke,8 9 16 17 18 20 22 29 and dementia.* Many reports suggest that PVH indicates ischemic changes in the cerebral white matter, which is supplied by deep penetrating arteries,4 6 25 27 31 34 35 36 37 38 39 but the pathogenesis of PVH is not fully understood. Since ECAS is a well-known risk factor for both stroke and TIA, it is conceivable that ECAS plays a role in the development of PVH. However, a correlation between ECAS and the severity of PVH is still uncertain. Previous studies reported contradictory findings concerning the relationship between the severity of either PVH or leukoaraiosis and ECAS.9 15 29 31 32 37 The purpose of this study is to clarify the relationship between the severity of PVH and risk factors for cerebrovascular disease and to examine the relationship of ECAS to PVH specifically.
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Subjects and Methods |
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We studied patients who were seen in the Tokyo Saiseikai Central Hospital because of cerebrovascular diseases, other neurological diseases, diabetes mellitus, ischemic heart disease, or medical examination of the brain between 1991 and 1994. The patients were given both a brain MRI and duplex carotid ultrasonography within a 3-month period for further examination of these diseases and cerebrovascular complications. We selected subjects who had unilateral or bilateral ECAS. The study included 323 subjects (237 men and 86 women; age range, 25 to 91 years; mean age, 68.2 years). We collected information about the subjects by retrospective review of patients' medical records. Patients with an obvious cause for their ECAS, such as Takayasu's disease, were excluded from the study.
Brain MRI was performed with a 1.5-T superconducting unit (Signa
Advantage, GE). Fast spin-echo sequences were performed with TR of 3500
ms and TE of 20 ms to produce proton density–weighted images.
Transaxial images of the brain were obtained with 5-mm thickness and
2-mm gap. Two-dimensional Fourier transformation of the images and a
256x256 data acquisition matrix were used. We evaluated the severity
of PVH using the modified method reported by Fukuda et
al.5 They reported that interrater reliability of
measurement of the severity of PVH was excellent5 ; they
used the same laboratory with which the first author was affiliated.
High signal intensity lesions adjacent to the lateral ventricles on
proton density–weighted images were defined as PVH. PVH size was
measured from the margin of the lateral ventricle to the end point of
the high-intensity lesion on axial images. Axial images were angled so
that they were parallel to the anterior commissure/posterior commissure
line. We measured PVH at eight points: bilaterally in the frontal
region on the slice that included basal ganglia and thalamus, and
bilaterally in frontal, middle, and occipital regions on the slice that
included the corona radiata (Fig 1
). The
individual values were summed for further analysis. Frontal PVH
was the sum in millimeters of numbers 1 through 4 in.
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Fig 1
. Similarly, lateral PVH was the sum of numbers 5 and 6, occipital
PVH was the sum of numbers 7and 8, and whole PVH was the sum of numbers
1 through 8. We did not measure a PVH when it was difficult to
differentiate the margin of the PVH from other white matter lesions or
cortical infarctions. All MRI images were reviewed by one observer who
had no knowledge of the clinical background of the subjects except for
age and sex so that the results were not influenced.
We also obtained T2-weighted images (TR, 3500 ms; TE, 120 ms) and T1-weighted images (TR, 350 ms; TE, 14 ms) to investigate cerebral infarction. Axial images were used to evaluate cerebral infarction. Cerebral infarctions was divided into four types based on their location: (1) lacunar infarction in the area of the penetrating artery; (2) territorial infarction in the cortex; (3) border zone infarction in the cortex; and (4) infarction of the deep white matter, including the border zone with the deep white matter.
The history of the subject was assessed for the presence of
cerebrovascular risk factors: age, sex, history of TIA, hypertension,
diabetes mellitus, hypercholesterolemia (total
cholesterol 
220 mg/dL), hypo-HDL
cholesterolemia (HDL cholesterol <35
mg/dL), smoking, and atrial fibrillation. Complications of
arteriosclerosis, such as
arteriosclerosis obliterans, coronary
artery disease, and past history of CVA, were also assessed. We
obtained these data from a retrospective chart review.
The degree of ECAS was evaluated with duplex carotid sonography with the use of 7.5- or 5-MHz probes (Quantam 2000, Siemens) at the carotid bifurcation and origin of the internal carotid artery bilaterally and was quantified with the use of the ratios of the diameter of the internal lumen to that of the vessel. The degree of ECAS was divided into five grades: grade 1, no lesions; grade 2, stenosis <30%; grade 3, stenosis between 30% and 75%; grade 4, stenosis >75%; and grade 5, total occlusion. Grade 1 was defined as no carotid lesion contralateral to the affected side. Subjects who had normal carotid arteries bilaterally were excluded from the study because our main interest was in the relationship between severity of ECAS and PVH. We compared the degree of PVH and ECAS on each side. To investigate the effect of bilateral ECAS on the degree of PVH, the subjects were divided into four groups on the basis of the grade of their ECAS: group 1, unilateral ECAS grade 2 or lower; group 2, bilateral grade 2 or unilateral grade 3; group 3, bilateral grade 3 or unilateral grade 4; and group 4, bilateral grade 4 or above or unilateral grade 5.32 Lesions of the large intracranial vessels were evaluated by MR angiography and rated as severe stenosis or occlusion of the middle cerebral artery. MR angiography was performed in all subjects for routine MRI studies at the same time. We defined severe stenosis as partial disappearance of the flow signal and occlusion as an interruption of the flow signal.
Statistical analyses were performed with the use of nonparametric methods because the sampled data were not normally distributed and were unbalanced. The influences of risk factors for cerebrovascular disease, complications of arteriosclerosis, extracranial carotid lesions, and intracranial vascular lesions on PVH were analyzed with the Wilcoxon rank sum test and Kruskal-Wallis ANOVA. The correlation between PVH and age was determined by the Spearman's r test. A commercial software package (Statview, version 4.1.1) was used for the statistical analyses.
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Results |
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Age was significantly correlated with frontal (P<.0001) and whole PVH (P<.0001) (Fig 2
). Table 1
shows the influence of risk factors on PVH. Frontal PVH was
significantly more severe in patients with hypertension
(P=.048). Frontal, occipital, and whole PVH were
significantly larger in patients with a history of CVA and in women.
However, women were significantly older than men (men, 67.1±10.3
years; women, 71.2±10.1 years; P=.0019). Frontal and whole
PVH were significantly less severe in patients who smoked. Similarly,
patients who smoked were younger than those who did not smoke (smokers,
66.9±10.4 years; nonsmokers, 70.6±9.8 years; P=.008).
Other risk factors such as
hypercholesterolemia, hypo-HDL
cholesterolemia, atrial fibrillation, diabetes
mellitus, TIA, and atherosclerotic complications such as
coronary artery disease and
arteriosclerosis obliterans were not correlated
with PVH. There was no significant difference in the age of subjects
and the five grades of ECAS (Table 2).
The relationship between the severity of PVH and ECAS is shown in Fig 3. There were no significant differences
in severity of PVH in any region between groups with differing severity
of ECAS. The severity of PVH was not affected by severe
stenosis and occlusion of the middle cerebral artery (Table 3). Regarding the relationship between
the type of ischemic stroke and PVH, PVH was significantly more
severe in patients with lacunar infarction and infarction of the deep
border zone (Table 4). There was no
relationship between PVH and cortical infarction or infarction of the
cortical border zone.
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Discussion |
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There are many reports on the relationship between PVH and risk factors for cerebrovascular disease. These reports find that the severity of PVH increases with age,2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 hypertension,4 5 6 8 9 10 11 12 13 14 15 16 17 18 19 21 22 25 27 28 29 30 31 32 and a history of cerebrovascular disease.8 9 16 17 18 20 22 29 Several studies reported that diabetes mellitus,11 14 17 18 19 27 32 hyperlipidemia,14 16 and heart disease9 10 14 15 27 32 34 were also related to the severity of PVH, but these correlations were weaker than those between PVH and age and hypertension.11 14 17 32 In this study frontal PVH was correlated with both age and hypertension, while whole PVH was correlated only with age. History of cerebrovascular disease and female sex were also significantly associated with severe frontal, occipital, and whole PVH, and smoking was significantly associated with weak frontal and whole PVH. Other risk factors for cerebrovascular disease were not related to the severity of PVH. PVH was significantly larger in women, but women were older than men. Similarly, smokers were younger than nonsmokers. Therefore, PVH was larger in women and nonsmokers because of older age. These results are consistent with previous reports. We considered that age and hypertension were contributing factors for progression of PVH, but other risk factors were not. In connection with aging, it is conceivable that brain atrophy may contribute to the severity of PVH through anterograde wallerian degeneration. Some previous reports suggested that brain atrophy is related to PVH or leukoaraiosis23 24 33 through anterograde wallerian degeneration.
With respect to the relationship between PVH and the type of ischemic stroke, PVH was significantly more severe in patients with lacunar infarction and infarction of the deep border zone. Hijdra et al18 reported that leukoaraiosis on brain CT was significantly more severe in patients with lacunar infarction but less common in patients with cortical infarction. They suggested that leukoaraiosis was associated with small-vessel disease in cerebrovascular disorders. Although infarction of the deep border zone is generally associated with lesions of the large vessels, lacunar infarctions and deep white matter infarctions are associated with arteriosclerosis of deep penetrating arteries. Pathological studies of the white matter showed that arteriosclerotic changes in the long penetrating arteries in the deep white matter were more severe in patients with leukoaraiosis.4 6 25 27 31 34 35 36 37 38 39 Small-vessel disease is generally thought to be caused by arteriosclerosis that results from aging and hypertension. There are also many reports that PVH represents ischemic changes in the white matter that result from arteriosclerosis of the long penetrating arteries.6 25 27 31 34 35 36 37 38 39 Our results support the observation that PVH strongly correlates with arteriosclerosis of deep penetrating arteries.
ECAS is a well-known risk factor for cerebral infarction and TIA. It is thought that severe stenosis or occlusion of the carotid artery leads to decreased cerebral blood flow.26 It is conceivable that the alteration of cerebral blood flow resulting from ECAS leads to the development of PVH,23 24 32 34 36 but the relationship between ECAS and the degree of PVH is still uncertain. Several studies reported contradictory findings concerning this relationship between the degree of PVH and ECAS.9 15 29 31 32 37 Leukoaraiosis on CT was not associated with severe carotid artery stenosis in the North American Symptomatic Carotid Endarterectomy Trial.9 Bogousslavsky et al29 also reported that leukoencephalopathy was not observed in patients with >50% stenosis or occlusion of the extracranial internal carotid arteries. While PVH was evaluated with a grading method in previous studies, we quantified PVH by measuring the distance it extended from the wall of the lateral ventricle. This enabled us to evaluate PVH in detail. Our quantitative analysis also demonstrated that there was no statistical difference between the severity of PVH and ECAS as shown in the previous studies. Therefore, we concluded that there is no relationship between the severity of PVH and carotid stenosis but rather that PVH is linked to small-vessel disease. Generally, it is thought that factors that accelerate the growth of carotid lesions are the same as risk factors for cerebrovascular disease, eg, age, hypertension, diabetes mellitus, and hyperlipidemia.40 41 42 43 44 45 46 However, our results suggest that these risk factors for cerebrovascular disease produce distinct effects on carotid lesions and deep white matter lesions.
We demonstrated that ECAS was not related to severity of PVH in this study, but several points regarding the interpretation of these results should be noted. First, there was a bias in terms of the patient population. Most subjects had CVA or risk factors of CVA such as diabetes and ischemic heart disease, while the number of healthy subjects was small. This type of study should be conducted on healthy subjects in the future. Second, we used the modified method reported by Fukuda et al5 for quantifying PVH They reported that the interrater reliability of measurement of the severity of PVH was excellent, and therefore we believed that the validity of the method was constant. However, we cannot exclude the possibility that measurement of PVH varies according to the condition of obtained images. Third, our sampled data were unbalanced. We therefore used nonparametric methods for statistical analysis. It may be necessary to add subjects to resolve the problem of an unbalanced number of subjects.
In conclusion, the severity of PVH was correlated with age, hypertension, and history of cerebrovascular complications. ECAS was not significantly related to severity of PVH. PVH was significantly greater in cases with lacunar infarction and infarction of the deep border zone. These results suggest that lesions in small vessels rather than large vessels underlie the pathogenesis and development of PVH.
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Selected Abbreviations and Acronyms |
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Acknowledgments |
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The authors wish to thank Dr Syuhei Yamaguchi (Third Division of Internal Medicine, Shimane Medical University) for careful review of the manuscript and Dr Hiroshi Segawa (Division of Rehabilitation, Keio University School of Medicine) for assistance. We also acknowledge the help of the staff of the MRI unit at Tokyo Saiseikai Central Hospital.
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Footnotes |
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Reprint requests to Tomohide Adachi, MD, Third Division of Internal Medicine, Shimane Medical University, 89-1 Enya-cho, Izumo 693, Japan.
References 2, 5, 8, 11-13, 22, 23, 29, 33, 34.
Received May 2, 1997; revision received July 11, 1997; accepted August 6, 1997.
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