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Response to Letter Regarding Article, “HighResolution Magnetic Resonance Wall Imaging Findings of Moyamoya Disease”
We appreciate the constructive comments Shang et al1 provided on our report in Stroke,2 which evaluated high-resolution wall MRI (HR-MRI) findings of Moyamoya disease (MMD) compared with intracranial atherosclerotic disease. MMD exhibited distinct HR-MRI findings, concentric enhancement on bilateral distal internal carotid arteries, and shrinkage of middle cerebral artery, regardless of symptoms (presence or severity) or stage (Suzuki grade). As Shang et al pointed out, the wall enhancement observed in our patients may have been because of luminal (and not wall) enhancement from slow-moving blood adjacent to the wall of the vessel (slow flow artifact). The suppression of intravascular signals is important in vessel wall imaging and various blackblood imaging techniques are used to achieve this, including spatial presaturation (commonly used with T1 fluid-attenuated inversion recovery or volumetric isotropic turbo spin-echo acquisition) and double inversion recovery preparation. The double inversion recovery preparation sequence is used widely for black-blood imaging and generally provides good image quality. However, the multisection double inversion recovery turbo spin-echo sequence requires a complicated section-interleaving implementation, which can compromise black-blood imaging efficacy. Furthermore, the double inversion recovery method is not easily adaptable for large field-of-view 3-dimensional black-blood imaging because of outflow limitations. To address this problem, new techniques such as improved motionsensitized driven equilibrium and delay alternating with nutation for tailored excitation prepulse sequences have been developed.3 Recently, we switched from spatial presaturation to improved motion-sensitized driven equilibrium sequences for black-blood imaging, and further studies with this improved technique are ongoing. In addition, several findings of our study suggest that enhancement on distal internal carotid artery/middle cerebral artery was caused by true wall enhancement rather than slow flow artifacts. First, in patients with intracranial atherosclerotic disease, enhancement was rarely observed on the asymptomatic stenosed segment. Second, in patients with MMD, enhancement was often observed on the nonstenosed segment on time of flight MRA, usually with mild concentric wall thickening either on the asymptomatic side or on the nonstenosed distal internal carotid artery in conjunction with bright signal, which suggests fast arterial flow, not slow flow. The mechanisms of vessel wall enhancement in MMD remain controversial. Circumscribed enhancement of the distal internal carotid artery on symptomatic or asymptomatic segments may represent active angiogenesis or hyperproliferation of the vessel wall component, such as smooth muscle cell migration/proliferation or fine vascular networks.4,5 However, our data indicate that far advanced MMD (Suzuki grade 5 or 6) also exhibited a similar pattern of enhancement. Therefore, increased angiogenesis may not be the only cause of vessel wall enhancement in MMD. In addition, blood–brain barriers were fragile in patients
with MMD,6 and enhancement may be related to fragile blood– brain barriers. Further studies with histological confirmation are required. Shang et al also suggested studying the association between HR-MRI findings and ACTA2 mutation. Although ACTA2 mutation analysis was not performed in our study, it would be helpful to establish the mechanism of vessel enhancement in MMD in future studies. The diagnosis of MMD is reliant on angiography-based criteria, and this has inherent limitations, including the absence of basal collaterals in early or far advanced MMD and a lack of biomarkers. Our study revealed that HR-MRI could be an imaging biomarker specific to MMD. Further study is warranted to develop new diagnostic criteria for MMD using more objective and consistent factors such as HR-MRI findings and genetic variation (ongoing trial, NCT02074111).
Sources of Funding This study was supported by the National Research Foundation of Korea, Ministry of Science, ICT (Information, Communication, Technology) and Future Planning (2011-0019389).
Disclosures None.
Sookyung Ryoo, MD Department of Neurology, Samsung Medical Center Sungkyunkwan University School of Medicine Seoul, Korea Jihoon Cha, MD Department of Radiology, Samsung Medical Center Sungkyunkwan University School of Medicine Seoul, Korea Oh Young Bang, MD Department of Neurology, Samsung Medical Center Sungkyunkwan University School of Medicine Seoul, Korea 1. Shang T, Welch B, Pinho M. Letter by Shang et al regarding article, “High-resolution magnetic resonance wall imaging findings of Moyamoya disease.” Stroke. 2014;45:e299. 2. Ryoo S, Cha J, Kim SJ, Choi JW, Ki CS, Kim KH, et al. High-resolution magnetic resonance wall imaging findings of Moyamoya disease. Stroke. 2014;45:2457–2460. 3. Li L, Chai JT, Biasiolli L, Robson MD, Choudhury RP, Handa AI, et al. Black-blood multicontrast imaging of carotid arteries with DANTEprepared 2D and 3D MR imaging. Radiology. 2014:131717. 4. Lin R, Xie Z, Zhang J, Xu H, Su H, Tan X, et al. Clinical and immunopathological features of Moyamoya disease. PLoS One. 2012;7:e36386. 5. Kuroda S, Houkin K. Moyamoya disease: current concepts and future perspectives. Lancet Neurol. 2008;7:1056–1066. 6. Fujimura M, Watanabe M, Narisawa A, Shimizu H, Tominaga T. Increased expression of serum Matrix Metalloproteinase-9 in patients with moyamoya disease. Surg Neurol. 2009;72:476–480, discussion 480.
(Stroke. 2014;45:e300.) © 2014 American Heart Association, Inc. Stroke is available at http://stroke.ahajournals.org
DOI: 10.1161/STROKEAHA.114.007219
Downloaded from http://stroke.ahajournals.org/ e300 at East Tennessee State University on June 11, 2015
Response to Letter Regarding Article, ''High-Resolution Magnetic Resonance Wall Imaging Findings of Moyamoya Disease'' Sookyung Ryoo, Jihoon Cha and Oh Young Bang Stroke. 2014;45:e300; originally published online October 14, 2014; doi: 10.1161/STROKEAHA.114.007219 Stroke is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231 Copyright © 2014 American Heart Association, Inc. All rights reserved. Print ISSN: 0039-2499. Online ISSN: 1524-4628
The online version of this article, along with updated information and services, is located on the World Wide Web at: http://stroke.ahajournals.org/content/45/12/e300
Permissions: Requests for permissions to reproduce figures, tables, or portions of articles originally published in Stroke can be obtained via RightsLink, a service of the Copyright Clearance Center, not the Editorial Office. Once the online version of the published article for which permission is being requested is located, click Request Permissions in the middle column of the Web page under Services. Further information about this process is available in the Permissions and Rights Question and Answer document. Reprints: Information about reprints can be found online at: http://www.lww.com/reprints Subscriptions: Information about subscribing to Stroke is online at: http://stroke.ahajournals.org//subscriptions/
Downloaded from http://stroke.ahajournals.org/ at East Tennessee State University on June 11, 2015
Response to Letter Regarding Article, “HighResolution Magnetic Resonance Wall Imaging Findings of Moyamoya Disease”
We appreciate the constructive comments Shang et al1 provided on our report in Stroke,2 which evaluated high-resolution wall MRI (HR-MRI) findings of Moyamoya disease (MMD) compared with intracranial atherosclerotic disease. MMD exhibited distinct HR-MRI findings, concentric enhancement on bilateral distal internal carotid arteries, and shrinkage of middle cerebral artery, regardless of symptoms (presence or severity) or stage (Suzuki grade). As Shang et al pointed out, the wall enhancement observed in our patients may have been because of luminal (and not wall) enhancement from slow-moving blood adjacent to the wall of the vessel (slow flow artifact). The suppression of intravascular signals is important in vessel wall imaging and various blackblood imaging techniques are used to achieve this, including spatial presaturation (commonly used with T1 fluid-attenuated inversion recovery or volumetric isotropic turbo spin-echo acquisition) and double inversion recovery preparation. The double inversion recovery preparation sequence is used widely for black-blood imaging and generally provides good image quality. However, the multisection double inversion recovery turbo spin-echo sequence requires a complicated section-interleaving implementation, which can compromise black-blood imaging efficacy. Furthermore, the double inversion recovery method is not easily adaptable for large field-of-view 3-dimensional black-blood imaging because of outflow limitations. To address this problem, new techniques such as improved motionsensitized driven equilibrium and delay alternating with nutation for tailored excitation prepulse sequences have been developed.3 Recently, we switched from spatial presaturation to improved motion-sensitized driven equilibrium sequences for black-blood imaging, and further studies with this improved technique are ongoing. In addition, several findings of our study suggest that enhancement on distal internal carotid artery/middle cerebral artery was caused by true wall enhancement rather than slow flow artifacts. First, in patients with intracranial atherosclerotic disease, enhancement was rarely observed on the asymptomatic stenosed segment. Second, in patients with MMD, enhancement was often observed on the nonstenosed segment on time of flight MRA, usually with mild concentric wall thickening either on the asymptomatic side or on the nonstenosed distal internal carotid artery in conjunction with bright signal, which suggests fast arterial flow, not slow flow. The mechanisms of vessel wall enhancement in MMD remain controversial. Circumscribed enhancement of the distal internal carotid artery on symptomatic or asymptomatic segments may represent active angiogenesis or hyperproliferation of the vessel wall component, such as smooth muscle cell migration/proliferation or fine vascular networks.4,5 However, our data indicate that far advanced MMD (Suzuki grade 5 or 6) also exhibited a similar pattern of enhancement. Therefore, increased angiogenesis may not be the only cause of vessel wall enhancement in MMD. In addition, blood–brain barriers were fragile in patients
with MMD,6 and enhancement may be related to fragile blood– brain barriers. Further studies with histological confirmation are required. Shang et al also suggested studying the association between HR-MRI findings and ACTA2 mutation. Although ACTA2 mutation analysis was not performed in our study, it would be helpful to establish the mechanism of vessel enhancement in MMD in future studies. The diagnosis of MMD is reliant on angiography-based criteria, and this has inherent limitations, including the absence of basal collaterals in early or far advanced MMD and a lack of biomarkers. Our study revealed that HR-MRI could be an imaging biomarker specific to MMD. Further study is warranted to develop new diagnostic criteria for MMD using more objective and consistent factors such as HR-MRI findings and genetic variation (ongoing trial, NCT02074111).
Sources of Funding This study was supported by the National Research Foundation of Korea, Ministry of Science, ICT (Information, Communication, Technology) and Future Planning (2011-0019389).
Disclosures None.
Sookyung Ryoo, MD Department of Neurology, Samsung Medical Center Sungkyunkwan University School of Medicine Seoul, Korea Jihoon Cha, MD Department of Radiology, Samsung Medical Center Sungkyunkwan University School of Medicine Seoul, Korea Oh Young Bang, MD Department of Neurology, Samsung Medical Center Sungkyunkwan University School of Medicine Seoul, Korea 1. Shang T, Welch B, Pinho M. Letter by Shang et al regarding article, “High-resolution magnetic resonance wall imaging findings of Moyamoya disease.” Stroke. 2014;45:e299. 2. Ryoo S, Cha J, Kim SJ, Choi JW, Ki CS, Kim KH, et al. High-resolution magnetic resonance wall imaging findings of Moyamoya disease. Stroke. 2014;45:2457–2460. 3. Li L, Chai JT, Biasiolli L, Robson MD, Choudhury RP, Handa AI, et al. Black-blood multicontrast imaging of carotid arteries with DANTEprepared 2D and 3D MR imaging. Radiology. 2014:131717. 4. Lin R, Xie Z, Zhang J, Xu H, Su H, Tan X, et al. Clinical and immunopathological features of Moyamoya disease. PLoS One. 2012;7:e36386. 5. Kuroda S, Houkin K. Moyamoya disease: current concepts and future perspectives. Lancet Neurol. 2008;7:1056–1066. 6. Fujimura M, Watanabe M, Narisawa A, Shimizu H, Tominaga T. Increased expression of serum Matrix Metalloproteinase-9 in patients with moyamoya disease. Surg Neurol. 2009;72:476–480, discussion 480.
(Stroke. 2014;45:e300.) © 2014 American Heart Association, Inc. Stroke is available at http://stroke.ahajournals.org
DOI: 10.1161/STROKEAHA.114.007219
Downloaded from http://stroke.ahajournals.org/ e300 at East Tennessee State University on June 11, 2015
Response to Letter Regarding Article, ''High-Resolution Magnetic Resonance Wall Imaging Findings of Moyamoya Disease'' Sookyung Ryoo, Jihoon Cha and Oh Young Bang Stroke. 2014;45:e300; originally published online October 14, 2014; doi: 10.1161/STROKEAHA.114.007219 Stroke is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231 Copyright © 2014 American Heart Association, Inc. All rights reserved. Print ISSN: 0039-2499. Online ISSN: 1524-4628
The online version of this article, along with updated information and services, is located on the World Wide Web at: http://stroke.ahajournals.org/content/45/12/e300
Permissions: Requests for permissions to reproduce figures, tables, or portions of articles originally published in Stroke can be obtained via RightsLink, a service of the Copyright Clearance Center, not the Editorial Office. Once the online version of the published article for which permission is being requested is located, click Request Permissions in the middle column of the Web page under Services. Further information about this process is available in the Permissions and Rights Question and Answer document. Reprints: Information about reprints can be found online at: http://www.lww.com/reprints Subscriptions: Information about subscribing to Stroke is online at: http://stroke.ahajournals.org//subscriptions/
Downloaded from http://stroke.ahajournals.org/ at East Tennessee State University on June 11, 2015
