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"Ivy Sign" in Childhood Moyamoya Disease: Depiction on FLAIR and Contrast-enhanced T1-weighted MR Images¹

¹ From the Departments of Radiology (H.K.Y., Y.W.C.) and Neurosurgery (H.J.S.), Samsung Medical Center, Sungkyunkwan University School of Medicine, 50 Irwon-dong, Kangnam-gu, Seoul 135-710, Korea. Received June 25, 2001; revision requested July 11; revision received October 12; accepted October 22. Address correspondence to H.J.S. (e-mail: hjshin@smc.samsung.co.kr).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
PURPOSE: To compare contrast material–enhanced T1-weighted and fluid-attenuated inversion recovery (FLAIR) magnetic resonance (MR) images with or without gadolinium in depicting the leptomeningeal ivy sign in children with moyamoya disease.

MATERIALS AND METHODS: Twenty-nine sets of FLAIR and postcontrast T1-weighted MR images were available in 19 consecutive children with primary moyamoya disease confirmed with conventional and MR angiography. Contrast-enhanced FLAIR MR images also were available in 15 sets. Two pediatric radiologists reviewed FLAIR and postcontrast T1-weighted images in separate sessions for the leptomeningeal ivy sign and assigned a rating of "present," "absent," or "equivocal" by consensus. Unenhanced and contrast-enhanced FLAIR MR images were compared side by side to determine which better depicted leptomeningeal high signal intensities.

RESULTS: Postcontrast T1-weighted MR images revealed the leptomeningeal ivy sign in 40 hemispheres (frequency of visualization, 71% [40 of 56 hemispheres]), whereas unenhanced FLAIR MR images depicted it in 26 hemispheres (frequency of visualization, 46% [26 of 56 hemispheres]). An equivocal rating was given in 21 hemispheres versus in 11 on FLAIR and postcontrast T1-weighted images, respectively. FLAIR and postcontrast T1-weighted images agreed in 40 hemispheres. There was no case with a positive rating on FLAIR images when postcontrast T1-weighted images were negative. Unenhanced FLAIR MR imaging was superior to contrast-enhanced FLAIR imaging in seven hemispheres, whereas enhanced FLAIR was better in four of 28 hemispheres. In the remaining 17, findings with each sequence were similar.

CONCLUSION: Contrast-enhanced T1-weighted images are better than FLAIR images for depicting the leptomeningeal ivy sign in moyamoya disease.

© RSNA, 2002

Index terms: Moyamoya disease, 17.7213 • Cerebral blood vessels, MR, 17.121416, 17.12142 • Cerebral blood vessels, stenosis or obstruction, 17.7213

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Moyamoya disease is an idiopathic cerebrovascular occlusive disorder characterized by progressive stenosis of the distal internal carotid arteries and by collateral vessel formation (1). There are three basic collateral pathways: basal moyamoya vessels from perforators, leptomeningeal collateral vessels from the posterior cerebral artery, and transdural collateral vessels from the external carotid artery. With high diagnostic accuracy, magnetic resonance (MR) imaging and MR angiography are very useful in assessing moyamoya disease in children (2–5). It has been observed that contrast material–enhanced MR images in patients with moyamoya disease show marked leptomeningeal enhancement and that there is a reduction in enhancement after bypass surgery. Some authors (6,7) call this leptomeningeal enhancement the "ivy sign," which is considered to represent the fine vascular network over the pial surface. Fluid-attenuated inversion recovery (FLAIR) MR images have been known as sensitive for the detection of leptomeningeal abnormalities (7–9). Since FLAIR imaging has been known to show arterial high signal intensity due to slow flow via leptomeningeal anastomosis in acute cerebral infarction (10), FLAIR imaging was expected to demonstrate the ivy sign of moyamoya disease. The purpose of our study was to compare contrast-enhanced T1-weighted and FLAIR MR images with or without gadolinium for depicting the leptomeningeal ivy sign in children with moyamoya disease.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Approval by the institutional review board was obtained, and patient informed consent was not required. Twenty-three pediatric patients who presented with transient ischemic attack (n = 22) or involuntary athetoid movement (n = 1) and were suspected of having moyamoya disease were studied with MR imaging over a 2-year period. At our hospital, the routine MR imaging protocol for moyamoya disease includes contrast-enhanced T1-weighted imaging, unenhanced FLAIR MR imaging, and, recently, contrast-enhanced FLAIR MR imaging. Moyamoya disease was diagnosed in 19 patients by using MR angiography, as well as conventional angiography. The diagnosis was made by using the criteria proposed by a research committee on spontaneous occlusion of the circle of Willis (2). None of the patients in the current study had underlying disease, including connective tissue disease, neurofibromatosis, or meningitis. In two, unilateral involvement of moyamoya disease was seen. There were 15 girls and four boys, with an age range of 3–14 years (average, 9 years). A total of 29 sets consisting of FLAIR and contrast-enhanced T1-weighted images were available in 19 children either before (n = 18) or after (n = 11) surgery. Because two patients had unilateral disease, 56 hemispheres were evaluated. Contrast-enhanced FLAIR MR images were available in 15 patients.

MR imaging was performed at 1.5 T (Signa; GE Medical Systems, Milwaukee, Wis). All patients underwent FLAIR and contrast-enhanced T1-weighted imaging. FLAIR imaging was performed by using a fast FLAIR sequence with a repetition time msec/effective echo time msec/inversion time msec of 10,000/133/2,200 and a 16-kHz bandwidth. Contrast-enhanced T1-weighted MR images were obtained shortly after administration of 0.2 mmol per kilogram of body weight gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany), by using a spin-echo (repetition time msec/echo time msec, 517/10; 256 x 256 matrix; 2-minute 20-second acquisition time) sequence. In those patients in whom contrast-enhanced FLAIR imaging was performed, it was performed immediately after contrast-enhanced T1-weighted imaging. The approximate time interval of contrast-enhanced FLAIR imaging was 4 minutes after injection of gadopentetate dimeglumine.

The "ivy sign" was defined as continuous or discontinuous linear high signal intensities along the cortical sulci and subarachnoid space. First, two pediatric radiologists (H.K.Y., Y.W.C.), by consensus, reviewed contrast-enhanced T1-weighted MR images for the leptomeningeal ivy sign and then reviewed unenhanced FLAIR images at a different session. A rating of "absent," "equivocal," or "present" was assigned. Unenhanced and contrast-enhanced FLAIR MR images were compared side by side to determine which were better for depiction of leptomeningeal high signal intensities.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
The results of rating are summarized in Table 1. Contrast-enhanced T1-weighted images revealed the leptomeningeal ivy sign in 40 hemispheres (frequency of visualization, 71% [40 of 56 hemispheres]) (Figs 1, 2). The frequency of visualization became 91% (51 of 56 hemispheres) when 11 hemispheres with an equivocal rating on postcontrast T1-weighted images were included. Unenhanced FLAIR MR images depicted the ivy sign in 26 hemispheres (frequency of visualization, 46% [26 of 56 hemispheres]). FLAIR and contrast-enhanced T1-weighted images agreed in 40 hemispheres (Table 2). There were four cases with a rating of "absent" on FLAIR and "present" or "equivocal" on postcontrast T1-weighted images. In 12 hemispheres, FLAIR images had a rating of "equivocal," while postcontrast T1-weighted images had a rating of "present." There was no positive rating on FLAIR images when contrast-enhanced T1-weighted images showed a negative result.

View larger version (144K): [in this window] [in a new window] [Download PPT slide]   Figure 1a. Bilateral moyamoya disease in an 8-year-old girl. (a) Transverse postcontrast T1-weighted (517/10) MR image shows diffuse leptomeningeal enhancement, with some enhancement of perforating arteries (arrowheads) in basal ganglia. Areas supplied by the posterior cerebral artery are relatively spared. (b) Transverse unenhanced FLAIR (10,000/133[effective]/2,200) MR image shows subtle high signal intensities (arrowheads) along leptomeninges in bilateral frontal regions and was interpreted as equivocal.

View larger version (154K): [in this window] [in a new window] [Download PPT slide]   Figure 1b. Bilateral moyamoya disease in an 8-year-old girl. (a) Transverse postcontrast T1-weighted (517/10) MR image shows diffuse leptomeningeal enhancement, with some enhancement of perforating arteries (arrowheads) in basal ganglia. Areas supplied by the posterior cerebral artery are relatively spared. (b) Transverse unenhanced FLAIR (10,000/133[effective]/2,200) MR image shows subtle high signal intensities (arrowheads) along leptomeninges in bilateral frontal regions and was interpreted as equivocal.

View larger version (163K): [in this window] [in a new window] [Download PPT slide]   Figure 2a. Bilateral moyamoya disease in a 14-year-old girl. (a) Transverse postcontrast T1-weighted (517/10) MR image shows diffuse enhancement along leptomeningeal surfaces (arrowheads), predominantly in right hemisphere. (b) Transverse unenhanced FLAIR (10,000/133 [effective]/2,200) MR image reveals multiple areas of high signal intensity (arrowheads) in leptomeninges. Both a and b were interpreted as depicting the leptomeningeal ivy sign. (c) Transverse gadolinium-enhanced FLAIR (10,000/133[effective]/2,200) MR image shows high signal intensities (arrowheads) in leptomeninges of left frontal and right frontoparietal regions, which are less apparent than those in b. Unenhanced FLAIR imaging is better for depicting the leptomeningeal ivy sign.

View larger version (169K): [in this window] [in a new window] [Download PPT slide]   Figure 2b. Bilateral moyamoya disease in a 14-year-old girl. (a) Transverse postcontrast T1-weighted (517/10) MR image shows diffuse enhancement along leptomeningeal surfaces (arrowheads), predominantly in right hemisphere. (b) Transverse unenhanced FLAIR (10,000/133 [effective]/2,200) MR image reveals multiple areas of high signal intensity (arrowheads) in leptomeninges. Both a and b were interpreted as depicting the leptomeningeal ivy sign. (c) Transverse gadolinium-enhanced FLAIR (10,000/133[effective]/2,200) MR image shows high signal intensities (arrowheads) in leptomeninges of left frontal and right frontoparietal regions, which are less apparent than those in b. Unenhanced FLAIR imaging is better for depicting the leptomeningeal ivy sign.

View larger version (167K): [in this window] [in a new window] [Download PPT slide]   Figure 2c. Bilateral moyamoya disease in a 14-year-old girl. (a) Transverse postcontrast T1-weighted (517/10) MR image shows diffuse enhancement along leptomeningeal surfaces (arrowheads), predominantly in right hemisphere. (b) Transverse unenhanced FLAIR (10,000/133 [effective]/2,200) MR image reveals multiple areas of high signal intensity (arrowheads) in leptomeninges. Both a and b were interpreted as depicting the leptomeningeal ivy sign. (c) Transverse gadolinium-enhanced FLAIR (10,000/133[effective]/2,200) MR image shows high signal intensities (arrowheads) in leptomeninges of left frontal and right frontoparietal regions, which are less apparent than those in b. Unenhanced FLAIR imaging is better for depicting the leptomeningeal ivy sign.

View larger version (169K): [in this window] [in a new window] [Download PPT slide]   Figure 3a. Bilateral moyamoya disease in a 10-year-old boy. (a) Transverse unenhanced FLAIR (10,000/133[effective]/2,200) MR image shows bilateral areas of high signal intensity (arrowheads) along leptomeninges. (b) Transverse gadolinium-enhanced FLAIR (10,000/133[effective]/2,200) MR image also demonstrates bilateral high signal intensities (arrowheads), which were depicted slightly better than those in a.

View larger version (165K): [in this window] [in a new window] [Download PPT slide]   Figure 3b. Bilateral moyamoya disease in a 10-year-old boy. (a) Transverse unenhanced FLAIR (10,000/133[effective]/2,200) MR image shows bilateral areas of high signal intensity (arrowheads) along leptomeninges. (b) Transverse gadolinium-enhanced FLAIR (10,000/133[effective]/2,200) MR image also demonstrates bilateral high signal intensities (arrowheads), which were depicted slightly better than those in a.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

Conventional MR imaging and MR angiography have been widely used in assessing moyamoya disease and have become an essential part of preoperative evaluation, as well as postoperative follow-up (2–5). MR imaging findings of moyamoya disease are well known; MR imaging can reveal stenosis or occlusion of the distal internal carotid artery and moyamoya vessels with signal voids in the basal ganglia, as well as ischemia, infarction, atrophy, and ventriculomegaly (5). A variety of pulse sequences are used for MR imaging, including FLAIR imaging, diffusion-weighted imaging, perfusion MR imaging, and contrast-enhanced MR imaging. Contrast-enhanced T1-weighted images show marked leptomeningeal enhancement along the cortical sulci, as well as enhancement of the moyamoya vessels in cases with advanced moyamoya disease. As shown in some reports of studies dealing with postoperative changes (5,7,11), moyamoya vessels and leptomeningeal enhancement diminished after bypass surgery, with development of new transdural collateral vessels. Therefore, leptomeningeal enhancement and moyamoya vessels seem to be reciprocal to the transdural collateral formation from the external carotid artery.

In normal subjects, intracranial structures including venous sinuses, cortical veins, and choroids plexus are commonly but not always enhanced on gadolinium-enhanced MR images, but there is no apparent leptomeningeal enhancement (11). Leptomeningeal enhancement on postcontrast MR images has been described in association with meningoencephalitis (8,12), meningeal carcinomatosis (9,13), and vasculitis (14).

Demaerel et al (15) observed marked meningeal enhancement in a girl with moyamoya disease. The ivy sign was described by Ohta et al (6), referring to the diffuse leptomeningeal enhancement that resembles creeping ivy on stones in patients with moyamoya disease. The ivy sign can be found on FLAIR images, as well as on contrast-enhanced MR images (7). Characteristic enhancement is caused by an engorged pial network via leptomeningeal anastomosis and is confirmed at surgery (7). In other reports (7,16–18), surgical findings of engorged pial vessels with thickened arachnoid membranes and edema are described, which may explain the leptomeningeal enhancement on contrast-enhanced MR images. Dilated pial vessels were preexisting rather than newly formed (17,18). The source of leptomeningeal high signal intensity on FLAIR images may be complex and is not clear. As for the leptomeningeal enhancement on postcontrast T1-weighted images mentioned earlier, it seems largely due to slow-flowing vessels of the engorged pial network (7). Thickening with congestion of the leptomeninges can take part in the mechanism causing high signal intensity. Thus, the mechanism of the leptomeningeal ivy sign can be explained mainly by an engorged pial network and possibly by congested leptomeninges.

Encephaloduroarteriosynangiosis, a method of indirect bypass, is the treatment of choice in pediatric moyamoya disease. It has been observed that moyamoya and leptomeningeal collateral vessels decrease after effective surgery (5,16). Leptomeningeal enhancement at gadolinium-enhanced MR imaging became less prominent following surgery, and MR imaging may thus play a role in evaluating surgical outcome (11). Leptomeningeal enhancement in moyamoya disease is not seen over the brainstem or cerebellum, because posterior circulation is relatively normal in most patients with moyamoya disease (11).

FLAIR is an inversion-recovery MR imaging pulse sequence that nulls the high signal intensity of cerebrospinal fluid. FLAIR images, as well as T2-weighted images, may show secondary findings of moyamoya disease, including brain infarction and resultant gliosis with atrophy (2). T2-weighted images seem to be better for visualizing the stenotic arteries directly, but FLAIR images are better for showing subtle parenchymal changes. Since fluid signal is effectively suppressed, FLAIR is very useful in the diagnosis of leptomeningeal or subarachnoid space disease (8,9). The question of which is better for evaluation of leptomeningeal disease is still controversial, but for the ivy sign in moyamoya disease, leptomeningeal abnormality is more extensive on contrast-enhanced T1-weighted images than on FLAIR images (7–9). In the current study, contrast-enhanced T1-weighted images depicted the leptomeningeal ivy sign in a larger number of patients than did FLAIR images, and, albeit subjectively, we observed that contrast-enhanced T1-weighted images were better for visualizing the ivy sign than were FLAIR images in most cases.

Contrast-enhanced FLAIR MR imaging has been described as a promising technique in patients with cerebral glioma and metastases (19). Other studies (20,21) have demonstrated that gadolinium-enhanced T1-weighted imaging was superior to enhanced FLAIR imaging in revealing intraparenchymal lesions. Nevertheless, it was expected that postcontrast FLAIR images might be useful for evaluating meningeal disease because they do not show vessel enhancement, as do T1-weighted images. According to our results, gadolinium-enhanced FLAIR MR imaging was not better than unenhanced FLAIR imaging for visualizing leptomeningeal high signal intensities in patients with moyamoya disease.

It is expected that leptomeningeal enhancement fades as time elapses after injection of contrast material. According to the study by Komiyama et al (11), the enhancement was most prominent soon after administration of gadolinium-based contrast material, fading rapidly thereafter. We obtained contrast-enhanced T1-weighted images within a few minutes after contrast material injection, and contrast-enhanced T1-weighted images were of good quality in all cases. Contrast-enhanced FLAIR images were obtained approximately 4 minutes after contrast material injection; this delay might have influenced the results.

In summary, the leptomeningeal ivy sign seen on postcontrast T1-weighted images is a relatively common and characteristic finding in patients with moyamoya disease. Gadolinium-enhanced T1-weighted images are superior to FLAIR MR images for depicting the ivy sign in patients with moyamoya disease.

	FOOTNOTES

 
Abbreviation: FLAIR = fluid-attenuated inversion recovery

Author contributions: Guarantor of integrity of entire study, H.J.S.; study concepts and design, H.K.Y.; literature research, H.K.Y.; clinical studies, H.J.S., H.K.Y.; data acquisition, H.K.Y.; data analysis/interpretation, H.K.Y., Y.W.C.; manuscript preparation, H.K.Y.; manuscript definition of intellectual content, H.J.S., H.K.Y.; manuscript editing and revision/review, H.K.Y., Y.W.C.; manuscript final version approval, H.K.Y., H.J.S., Y.W.C.

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This Article Abstract Figures Only Full Text (PDF) All Versions of this Article: 2232011094v1 223/2/384    most recent Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Yoon, H.-K. Articles by Chang, Y. W. Search for Related Content PubMed PubMed Citation Articles by Yoon, H.-K. Articles by Chang, Y. W.