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1 Department of Clinical Radiology, Graduate School of Medical Sciences, Kyushu
University, Maidashi 3-1-1, Higashi-ku, Fukuoka 812-8582, Japan.
2 Department of Neurosurgery, Graduate School of Medical Sciences, Kyushu
University, Higashi-ku, Fukuoka 812-8582, Japan.
3 Department of Neurosurgery, Hamanomachi Hospital, Maizuru 3-5-27, Chuo-ku,
Fukuoka 810-8539, Japan.
Received October 31, 2003;
accepted after revision January 30, 2004.
Address correspondence to O. Togao.
Abstract
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MATERIALS AND METHODS. Abdominal angiography was performed in 73 patients with idiopathic moyamoya disease. The findings of abdominal angiography were retrospectively reviewed for the presence and appearance of stenosis in the renal and other major abdominal arteries.
RESULTS. Four (5%) of 73 patients presented with unilateral renal artery stenosis. Three patients had moderate stenosis, and one patient had mild stenosis. In the three patients with moderate stenosis, the renal artery stenosis was located in the proximal region of the main branch. Two patients (3%) with moderate stenosis of the unilateral renal artery had renovascular hypertension. No statistically significant differences were observed in age, sex, and the cerebral angiographic stage between patients with and without renal artery stenosis. No stenosis was found in the abdominal aorta or celiac, superior mesenteric, common hepatic, splenic, and proximal common iliac arteries. No occlusions were found in any abdominal arteries.
CONCLUSION. The prevalence of renal artery stenosis in patients with moyamoya disease was 5% (4/73). Involvement of the proximal region of the renal artery was dominant. No stenosis was found in other abdominal arteries.
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We retrospectively evaluated the prevalence and findings of stenoocclusive lesions of the renal and other abdominal arteries in patients with moyamoya disease who underwent both cerebral and abdominal angiography as a routine protocol.
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All 73 patients underwent cerebral digital subtraction angiography, including bilateral internal carotid and external or common carotid arteriography, and unilateral or bilateral vertebral arteriography, using the transfemoral Seldinger catheterization technique. Both anteroposterior and lateral projection cerebral angiograms were obtained. In all angiograms, the same digital subtraction angiography equipment (FDP200A, Toshiba Medical Systems) was used. To evaluate the angiographic findings, we classified the stenoocclusive lesions of the intracranial internal carotid artery into the six angiographic stages defined by Suzuki and Takaku [1] and Suzuki and Kodama [2] and applied the stages to the 52 patients who had not undergone revascularization surgery.
Abdominal aortography or selective renal angiography was performed in all 73 patients during the same examination in which the cerebral angiography was performed to investigate the presence of renal artery stenosis for clinical purposes. Informed consent was obtained from all patients. This study was approved by our institutional review board. Of the 73 patients, abdominal aortography with or without selective renal angiography was performed in 54 patients, and selective renal angiography alone was performed in the remaining 19. The abdominal angiograms were obtained in anteroposterior projection, and the findings were reviewed for the presence, degree, and appearance of stenosis in the major abdominal vessels. We evaluated the abdominal aorta and the renal, celiac, common hepatic, splenic, superior mesenteric, and proximal common iliac arteries. The degree of maximal arterial stenosis was graded according to the classification used by Yamada et al. [4]: no stenosis, mild (< 50%) stenosis, moderate (50–75%) stenosis, marked (> 75%) stenosis, and occlusion.
Interpretation of all cerebral and abdominal angiograms was performed using film. Two board-certified radiologists met and discussed the angiography findings. Statistical analysis of the comparison of sex, age, and angiographic stage between patients with and without renal artery stenosis was performed using one of the following methods: Fisher's exact test, the unpaired Student's t test, or the Mann-Whitney U test. Values for p of less than 0.05 were considered statistically significant.
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Of 73 patients with moyamoya disease, four patients (5%; three male, one female) were found to have unilateral renal artery stenosis (Table 1). One patient had mild (< 50%) stenosis and three had moderate (50–75%) stenosis. In the three patients with moderate stenosis, the renal artery stenosis was located in the proximal third of the main branch. The other patient had mild stenosis in the mid portion of the main branch.
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Five (7%) of the 73 patients with moyamoya disease presented with hypertension. Two of these five patients had renal artery stenosis, but the remaining three did not. In two adult patients with moderate stenosis and hypertension, renovascular hypertension was confirmed by means of renal vein sampling, which revealed elevated plasma rennin activity on the affected side. All four patients with renal artery stenosis had stenosis or occlusion of the internal carotid artery and the proximal anterior cerebral artery and middle cerebral artery on both sides. Findings of their stages of cerebral angiography as defined by Suzuki and Takaku [1] and Suzuki and Kodama [2] were as follows: stage 3, two sides; stage 4, one side; stage 5, two sides; stage 6, one side. Images from one patient are shown in Figure 1A, 1B, 1C, 1D.
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Statistical analysis of the comparison of sex, age, and cerebral angiographic stage between patients with and without renal artery stenosis is summarized in Table 2. Renal artery stenosis was more frequent in males than females. The mean age of the four patients with renal artery stenosis was slightly higher than that of the other 69 patients. The average cerebral angiographic stage of the bilateral sides of the patients with renal artery stenosis was higher than that of the other patients, but the difference was not statistically significant.
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No patients were found to have stenosis in the abdominal aorta or celiac, common hepatic, splenic, superior mesenteric, or proximal common iliac arteries. No occlusions were present in abdominal arteries.
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Extracranial involvements of moyamoya disease have been most often reported in the renal artery [16–22]. In our study, four (5%) of 73 patients with moyamoya disease had renal artery stenosis. This prevalence is similar to that reported by Yamada et al. [4]. However, because of the paucity of population-based studies, the prevalence of renal artery stenosis in the general population is unknown. We compared patients with and without renal artery stenosis on the basis of their age, sex, and cerebral angiographic stage but found no statistically significant differences. These results are in accordance with those of Yamada et al.
The angiographic appearance of renal artery stenosis was not described in detail in the study by Yamada et al. [4]. In our study, renal artery stenosis tended to be located in the proximal region of the main branch. In previous reports in which a histopathologic diagnosis of stenosed renal arteries was confirmed, an obvious tendency for proximal involvement in the renal artery was shown [6, 7, 12, 19]. This finding is different from that of fibromuscular dysplasia, which shows relatively distal involvement and a typical string-of-beads appearance. In atherosclerosis and Takayasu's arteritis, which are the other major differential diagnoses, the proximal region of the renal artery is often involved [23, 24]. However, it would be difficult to differentiate by angiographic appearance alone.
Renal artery stenosis in moyamoya disease may cause renovascular hypertension. Suzuki and Kodama [2] noted hypertension in eight of 54 adult patients, but in none of 46 pediatric patients. Choi et al. [7] reported that six (8%) of 72 patients with moyamoya disease had renovascular hypertension. In our study, five (7%) of 73 patients with moyamoya disease had hypertension. Two adult patients (3%) with a moderate stenosis of the renal artery presented with renovascular hypertension. Therefore, we considered it necessary to examine the presence of renal artery stenosis in patients with moyamoya disease who have hypertension.
In previous reports, renovascular hypertension in moyamoya disease was treated with balloon angioplasty [4, 7, 16], stent implantation [17], or an operation, including renal autotransplantation [6, 7, 12]. Balloon angioplasty is a common therapy for the treatment of renovascular hypertension. However, the effectiveness of balloon angioplasty for the treatment of renal artery stenosis in moyamoya disease has not yet been established. Our patients with renovascular hypertension were successfully treated with medication.
In addition to the renal artery, the coronary [8], pulmonary [5, 11], hepatic [9], splenic [9], superior mesenteric [6, 7], pancreatic [5], iliac [7], and peripheral [10] arteries have also been reported to be involved in moyamoya disease in clinical or autopsy studies. Ikeda [5] proved intimal thickening of the pulmonary, renal, and pancreatic arteries in their pathologic study. Kawakita et al. [9] reported the autopsy of a 12-year-old boy with moyamoya disease presenting with thickenings of the intima in the hepatic and splenic arteries. Shoskes and Novick [6] and Choi et al. [7] reported stenosis of the superior mesenteric and renal arteries on abdominal angiography. No reports have determined the prevalence of involvement of major abdominal vessels except for the renal artery in patients with moyamoya disease. Our results revealed no stenoocclusive change in the abdominal aorta, celiac, splenic, common hepatic, superior mesenteric, or proximal common iliac arteries. This result suggests that the involvement of abdominal vessels other than the renal artery in moyamoya disease is quite rare. Although the reason for the selective involvement of the renal artery is unknown, some association may exist between the intracranial arteries and the renal artery in susceptibility to systemic factors that cause coarctation of these vessels.
Our study has some limitations. First, the number of patients studied was small. Second, because of the retrospective nature of the study, a possible bias in patient selection could not be completely excluded. We included only patients who had cerebral angiography, which was often performed preoperatively or postoperatively. Patients who had been diagnosed on MR angiography alone were excluded. Therefore, some bias may have appeared toward more advanced cases. Third, the histopathologic diagnosis of stenosed renal arteries was not confirmed because none of the patients with renal artery stenosis had surgery or had undergone autopsy. However, no clinical evidence suggested other possible diagnoses, such as atherosclerosis, fibromuscular dysplasia, or Takayasu's arteritis, so we considered the renal artery stenosis to be a systemic manifestation of moyamoya disease.
In conclusion, four (5%) of 73 patients with idiopathic moyamoya disease presented with renal artery stenosis. Two patients (3%) with moderate stenosis in the renal arteries had renovascular hypertension. Renal artery stenosis was predominantly located in the proximal region of the main branch. We found no statistically significant differences in age, sex, and cerebral angiographic stages between patients with and without renal artery stenosis. No stenosis or occlusion was found in the other major abdominal arteries. Renal artery involvement in moyamoya disease is an important clinical manifestation that may result in renovascular hypertension. Involvement of abdominal vessels other than the renal artery is considered less common.
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