- Email: [email protected]
Moyamoya Vessel Pathology Imaged by Ultra–High-Field Magnetic Resonance Imaging at 7.0 T
ARTICLE IN PRESS
Moyamoya Vessel Pathology Imaged by Ultra–High-Field Magnetic Resonance Imaging at 7.0 T Nora F. Dengler, MD,* Vince I. Madai, MD,†‡ Jens Wuerfel, MD,‡§‖¶** Federico C. von Samson-Himmelstjerna, PhD,‡‡‡ Petr Dusek, MD,‖†† Thoralf Niendorf, PhD,¶ Jan Sobesky, MD,†‡ and Peter Vajkoczy, MD*
Background: Prompt diagnosis of vessel pathology and appropriate treatment of moyamoya vasculopathy (MMV) are essential to improve long-term prognosis. The aims of our study were to explore the diagnostic value of ultra–high-field (UHF) magnetic resonance imaging at 7.0 T in MMV patients and to compare the applicability of two different 7.0 T vessel imaging modalities to 3.0 T magnetic resonance angiography (MRA) and digital subtraction angiography (DSA). Methods: In a World Health Organization-registered and prospective imaging trial, patients were investigated at 7.0 T magnetization-prepared rapid-acquisition gradient echo (MPRAGE)-MRA and time-of-flight (TOF)-MRA, 3.0 T TOF-MRA, and by DSA. Results: Six patients were included in our study and evaluated for MMV. 3.0 T TOF-MRA and 7.0 T MPRAGE-MRA were able to depict the complete major vascular tree and confirmed MMV-specific steno-occlusions of major intracranial arteries, as previously identified by DSA. 7.0 T TOF-MRA was limited to visualization of the circle of Willis as well as the internal carotid artery only. Donor vessels for bypass surgery (i.e., branches of superficial temporal artery) could be sufficiently visualized with all magnetic resonance modalities. Conclusions: Our results indicate that a specific 7.0 T vascular imaging protocol yields diagnostic information about vessel pathology in MMV that approximates conventional DSA. 7.0 T MPRAGE was superior to 7.0 T TOF-MRA due to shorter scanning times and better brain coverage. To date, however, limited availability of 7.0 T technology in medical facilities as well as technical and procedural constraints excludes a fair amount of patients from the clinical 7.0 T imaging process. Key Words: MRI—ultra–high-field MR—7.0 T—moyamoya—stroke—extracranial–intracranial bypass. © 2016 National Stroke Association. Published by Elsevier Inc. All rights reserved.
From the *Department of Neurosurgery, Charité Universitätsmedizin Berlin, Berlin, Germany; †Department of Neurology, Charité Universitätsmedizin Berlin, Berlin, Germany; ‡Center for Stroke Research Berlin (CSB), Charité Universitätsmedizin Berlin, Berlin, Germany; §Neurocure Clinical Research Centre, Charité Universitätsmedizin Berlin, Berlin, Germany; ‖Institute of Neuroradiology, University Göttingen, Göttingen, Germany; ¶Berlin Ultra-High Field Facility (B.U.F.F.), Max Delbrück Center for Molecular Medicine (MDC), Berlin, Germany; **Medical Image Analysis Center (MIAC AG), Basel, Switzerland; ††Department of Neurology and Center of Clinical Neuroscience, Charles University in Prague, First Faculty of Medicine and General University Hospital in Prague, Praha, Czech Republic; and ‡‡Fraunhofer MEVIS, Bremen, Germany. Received November 13, 2015; revision received January 20, 2016; accepted January 29, 2016. Conflict of interest: Thoralf Niendorf is founder and CEO of MRI.TOOLS GmbH, Berlin, Germany, and received speaker honoraria from Siemens Healthcare. Jens Wuerfel is CEO of the Medical Image Analysis Center (MIAC AG), Basel, Swizerland. He received research grants from Novartis and Biogen, and speaker honoraria from Bayer, Novartis, Teva, and Biogen. He served for advisory boards for Novartis and Biogen. He is supported by the German Ministry of Science (BMBF/KKNMS) and the German Ministry of Economy (BMWi). Apart from the scanner, no other resources of Siemens Healthcare, MRI.TOOLS GmbH, and MIAC AG were used, and the companies had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. Address correspondence to Peter Vajkoczy, MD, Department of Neurosurgery, Charité Universitätsmedizin Berlin, Augustenburger Platz 1, 13353 Berlin, Germany. E-mail: [email protected]. 1052-3057/$ - see front matter © 2016 National Stroke Association. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2016.01.041
Journal of Stroke and Cerebrovascular Diseases, Vol. ■■, No. ■■ (■■), 2016: pp ■■–■■
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Introduction Moyamoya vasculopathy (MMV) presents with mostly bilateral progressive stenosis of the terminal internal carotid artery (ICA). Affected patients develop pathognomonic collateral pathways that can lead to ischemic or hemorrhagic lesions and consecutive permanent or transient neurological deficits.1-4 To improve long-term prognosis of patients with MMV, prompt diagnosis of vessel pathology and appropriate treatment, for example, revascularization surgery, is mandatory.5-7 To date, digital subtraction angiography (DSA) is considered the “gold standard” for the diagnosis of MMV.8,9 DSA can be omitted when magnetic resonance imaging (MRI) and magnetic resonance angiography (MRA) with a field strength of 1.5 T or higher provide information about stenosis or occlusion of the terminal portion of the ICA or proximal portion of the anterior cerebral artery (ACA) and/or the middle cerebral artery (MCA) as well as abnormal vascular networks in the basal ganglia and collateral pathways.7,10,11 However, for preoperative planning, postoperative control, and follow-up of revascularizing procedures such as extracranial–intracranial bypass (EC– IC bypass), DSA is still the required standard. It would be beneficial for patients with MMV to undergo only MRI as a noninvasive diagnostic test that yields information about new ischemic lesions, high-resolution imaging of vessel dynamics, and bypass patency in contrast to a battery of examinations containing the combination of MRI and an invasive and radiation exposing DSA. The potential of ultra–high-field (UHF) MRI at 7.0 T in cerebrovascular disease has been shown recently.12-14 A major benefit is expected for MRA due to increased spatial resolution and novel contrast mechanisms.15,16 A 7.0 T MRA might therefore contribute substantial impact for the diagnosis of MMV. The aim of our study was to explore the diagnostic value of UHF MRA in MMV patients. We hypothesized that UHF MRA can yield preoperative diagnostic information equivalent to DSA for detection of MMV as well as for evaluation and planning of EC–IC bypass surgery.
Methods Study Protocol Patients were imaged within an ongoing World Health Organization-registered and prospective imaging trial (7UP, World Health Organization register No. DRKS00003193) before EC–IC bypass. Screening was performed between June 2012 and April 2014. Fully developed MMV was defined by bilateral stenosis or occlusion of the ICA or proximal portions of the ACA and/or the MCA as well as bilateral abnormal vascular networks, and was referred to as moyamoya disease (MMD). Unilateral MMV was referred to as “probable MMD” according to current guidelines.7 Inclusion criteria were confirmed or proba-
ble MMV, subacute/chronic ischemia or transient ischemic attack, age 18-80 years, ability to give informed consent, and legal competence. Exclusion criteria were any electronic and metallic implants, pregnancy or breast-feeding period, claustrophobia, chronic or episodic vertigo, retinal diseases, and dental bridges and/or more than 2 metallic dental crowns in a row. Neurological status was assessed at the time of admission. MRI was performed first at 3.0 T, immediately followed by MRI at 7.0 T. A neurologist specialized in stroke supervised the patients during the MRI examination. All patients gave informed written consent before the study. The study was approved by the authorized ethical review board, the governmental Berlin state ethical review board, and the relevant German state authority, the Federal Institute for Drugs and Medical Devices. Cerebral blood flow and reserve capacity in each patient were detected by positron emission tomography or singlephoton emission computed tomography (before and after forced vessel dilation by diamox).
MRI Hardware MRI was performed on a 3.0 T whole-body system (Magnetom Verio; Siemens Healthcare, Erlangen, Germany). A body coil was used for excitation and a 12-channel radio frequency (RF) receive coil (Siemens Healthcare) tailored for head imaging was employed for reception. At 7.0 T, a whole-body system (Magnetom 7.0 T, Siemens Healthcare) equipped with a 90 cm bore magnet (Magnex Scientific, Oxfordshire, United Kingdom) and an Avanto gradient system (Siemens Healthcare) was used together with a 1/24channel transmit/receive coil (Model NM 008-23-7S; NovaMedical, Wakefield, MA) designed for head imaging.
MRI Parameters The imaging protocol included MRA using 3D magnetization-prepared rapid-acquisition gradient echo (MPRAGE), time-of-flight (TOF)-MRA, T 2 -weighted imaging, and susceptibility-weighted imaging (SWI) at 7.0 T. A 3.0 T TOF-MRA and T2*-weighted imaging were conducted. Detailed parameters of the angiographic imaging techniques were as follows:
• 7.0 T T1-weighted 3D-MPRAGE: repetition time (TR): 2750 ms, echo time (TE): 1.81 ms, acceleration factor: 3 (Grappa), bandwidth: 350 Hz/pixel, voxel size: 0.7 × 0.7 × 0.7 mm3, matrix size: 384 × 384, flip angle: 10°, acquisition time: 5 minutes and 40 seconds, number of slabs: 1 (240 slices), and whole-brain coverage. • 7.0 T 3D TOF-MRA: TR: 32 ms, TE: 3.53 ms, no acceleration factor, bandwidth: 305 Hz/pixel, voxel size: 0.4 × 0.4 × 0.4 mm3, matrix size: 512 × 512, flip angle: 25°, acquisition time: 8 minutes and 16 seconds, number of slabs: 1 (128 slices), and 5.1 cm vertical coverage.
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• 3.0 T 3D TOF-MRA: TR: 24 ms, TE: 3.60 ms, acceleration factor: 2 (Grappa), bandwidth: 186 Hz/ pixel, voxel size: 0.6 × 0.6 × 0.6 mm3, matrix size: 384 × 384, flip angle: 18°, acquisition time: 5 minutes and 54 seconds, number of slabs: 4 (40 slices per slab), and 8.2 cm vertical coverage. Detailed parameters of the other imaging techniques were as follows:
• 7.0 T 3D SWI: TR: 22 ms, TE: 15.0 ms, acceleration factor: 2 (Grappa reconstruction), bandwidth: 120 Hz/ pixel, voxel size: 0.6 × 0.6 × 0.6 mm3, matrix size: 384 × 384, flip angle: 15°, and acquisition time: 10 minutes and 25 seconds. • 3.0 T 2D T2*-weighted imaging: TR: 800 ms, TE: 3.60 ms, no acceleration factor, bandwidth: 260 Hz/pixel, voxel size: 1.1 × 0.7 × 4.0 mm3, matrix size 256 × 230, flip angle: 25°, and acquisition time: 2 minutes and 35 seconds.
Analysis All 3.0 and 7.0 T images of our patients were evaluated independently by 2 reviewers (N.F.D. and V.I.M.) for determination of magnetic resonance (MR) MMV grades10 as well as DSA images for Suzuki grades.1
Results Patient Characteristics Forty-two patients admitted for evaluation of MMV to our neurosurgical department were screened for the study. Two patients refused informed consent, 34 patients were excluded due to metallic implants (n = 30) or tattoos (n = 4). In total, 6 patients with unilateral (n = 2) or bilateral (n = 4) MMV could be included in the study (4 females, 2 males) (Table 1). The median age was 28 years (interquartile range: 19.5-34). All 6 patients presented with recurrent transient neurological deficits, 1 patient also suffered from permanent left-sided hemiparesis. In all patients, typical collateral pathways were present and could be identified by DSA (Table 1). Four patients were classified as Suzuki grade 2°, 1 patient as Suzuki grade 3°, and 1 patient as Suzuki grade 4°. None of our patients showed signs of hemorrhages (e.g., microbleeds) at any of the 2 field strengths. Three patients underwent bilateral and 1 patient unilateral EC– IC bypass surgery in accordance with proven severely restricted reserve capacity.
Major Cerebral Artery and Small-Vessel Pathology In all 6 patients, 3.0 T TOF-MRA and 7.0 T MPRAGEMRA were able to depict the complete major vascular tree and showed MMV-specific steno-occlusions of major cerebral arteries, matching the results obtained by DSA. In contrast, identification of MMV pathologies by 7.0 T TOF-MRA was limited to the circle of Willis as well as
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the ICA (Fig 1). Motion artifacts were present in 3 out of 6 7.0 T TOF image series, due mainly to long scan times evoked by RF power deposition constraints. The overall impression of 7.0 T images (MPRAGE and TOF) was a more detailed depiction of small moyamoyaspecific vessels in comparison with 3.0 T MR images (Figs 2, 3). MR grading according to Houkin et al17 was performed for 3.0 T TOF-MRA, 7.0 T MPRAGE-MRA, and 7.0 T TOF-MRA. In differentiation between stenosis, discontinuity or invisible ICA or MCA similar results were obtained with only slight differences present between the 3 modalities (Table 1). Imaging with 7.0 T technology tended to show higher grades as the differentiation between an invisible, discontinuous or stenotic vessel was easier at 7.0 T MRI. (Figs 2, 3). Collateral vessels were not consistently identified in all MR modalities.
Donor Vessel Imaging In 4 patients, the MRI field of view was expanded to visualize possible donor vessels for EC–IC bypass surgery (superficial temporal artery). In all 4 patients, donor vessels were adequately identified with all MR modalities (7.0 T MPRAGE, 7.0 T TOF-MRA, and 3.0 T TOF-MRA) and were comparable to DSA visualization quality (Figs 2, 3).
Discussion We present the first comparison of 3.0 T, 7.0 T, and DSA vessel imaging of patients with MMV. Our results indicate that major vessel pathology and donor vessel visualization are adequate with all 3 modalities. The quality of 7.0 T MPRAGE-MRA, however, was superior to 3.0 T TOF images in detecting moyamoya-specific smallvessel pathology and seems to offer a better resolution for assessment of MRA grades. The highest spatial resolution was shown by 7.0 T TOF, but brain coverage was limited and motion artifacts were frequent. For major arteries of the circle of Willis, the diagnostic value of 7.0 T MPRAGE-MRA and 7.0 T TOF-MRA was at least equivalent to 3.0 T TOF-MRA. Steno-occlusive changes were similarly detected with both modalities and were in line with DSA findings. Differentiation of ICA or MCA pathologies for MRA grading10,17 was more precise with 7.0 T MPRAGE-MRA and 7.0 T TOF-MRA images. Only 7.0 T MPRAGE-MRA and 7.0 T TOF-MRA were able to depict MMV-specific small-vessel pathologies comparable with DSA. Considering previous MR studies of MMV, higher magnetic field strength seems to correlate with more precise results of MRA.11,12,16,18-20 Isotropic spatial resolution of conventional angiography has been described to be 0.4 mm, which is theoretically comparable to the 0.4 mm isotropic resolution of our 7.0 T TOF-MRA images. However, at the current stage of development, the brain coverage of 7.0 T TOF-MRA is severely limited due to RF power deposition constraints, and the resulting long scan times render the MRA
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Table 1. Clinical, MRI and angiographic findings in our patient series evaluated for suspected MMV Patient
Sex Age Side Pathology TIA Permanent nD Bypass T2 MRI findings 7.0 T microbleeds 3.0 T microbleeds MRI grades 3.0 T TOF ICA R 3.0 T TOF MCA R 3.0 T TOF ACA R 3.0 T TOF PCA R 3.0 T TOF ICA L 3.0 T TOF MCA L 3.0 T TOF ACA L 3.0 T TOF PCA L 7.0 T MPR ICA R 7.0 T MPR MCA R 7.0 T MPR ACA R 7.0 T MPR PCA R 7.0 T MPR ICA L 7.0 T MPR MCA L 7.0 T MPR ACA L 7.0 T MPR PCA L 7.0 T TOF ICA R 7.0 T TOF MCA R 7.0 T TOF ACA R 7.0 T TOF PCA R 7.0 T TOF ICA L 7.0 T TOF MCA L 7.0 T TOF ACA L 7.0 T TOF PCA L Suzuki left Suzuki right Collateralization Motion artifacts Complete CoW
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2
3
4
5
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Female 28 Left ICA occlusion Yes No Left Left atrophy
Female 18 Bilateral ICA occlusion Yes No Bilateral Right ACA infarction No No
Male 28 Right MCA occlusion Yes No None No
Female 21 Bilateral MCA stenosis Yes Yes None No
Female 33 Bilateral MCA occlusion Yes No Bilateral No
No No
Male 40 Bilateral MCA occlusion Yes No Bilateral Right ACA infarction No No
No No
No No
No No
0 0 0 0 1 3 0 0 0 0 0 0 1 2 0 0 0 0 0 0 1 2 0 0 3 — lm, vb, eth, Acha No Yes
0 3 0 0 0 3 0 0 1 3 0 0 0 2 0 0 n.d. 2 0 n.d. n.d. 3 0 n.d. 2 2 ACA, PCA, Acha No No
1 2 1 0 1 2 1 0 1 1 2 0 1 2 2 0 0 2 0 0 0 2 0 0 4 3 eth, PCA, Acha, ls, lm Yes Yes
0 2 0 0 0 0 0 0 0 2 0 0 0 0 0 0 0 1 0 0 0 0 0 0 — 2 ACA, PCA, eth Yes Yes
0 2 0 0 0 2 0 0 1 1 0 0 1 1 0 0 0 2 0 0 0 1 0 0 2 2 ACA, PCA, eth, lm No Yes
0 2 0 0 0 3 0 0 1 1 0 0 0 2 0 0 0 1 0 0 0 1 0 0 2 2 ACA, PCA, eth, lm Yes Yes
Abbreviations: ACA, anterior cerebral artery; Acha, anterior choroidal artery; CoW, circle of Willis; EC–IC, extracranial–intracranial; eth, ethmoidal; ICA, internal carotid artery; L, left; lm, leptomeningeal; MCA, middle cerebral artery; MMV, moyamoya vasculopathy; MPRAGE, magnetization-prepared rapid-acquisition gradient echo; MRI, magnetic resonance imaging; n.d., not detected; nD, neurological deficit; PCA, posterior cerebral artery; R, right; SWI, susceptibility-weighted imaging; TIA, transient ischemic attack; TOF, time of flight; vb, vertebrobasilar. Clinical findings are displayed with respect to sex, age, side of vessel pathology, type of vessel pathology (occlusion or high-grade stenosis), presence of TIA, presence of permanent nD, and indication for EC–IC bypass surgery. T2 MRI findings such as infarction or atrophy are depicted as well as occurrence of microbleeds in 3.0 T SWI and 7.0 T SWI. MRI grades of vascular pathology were evaluated for 3.0 T TOF, 7.0 T MPRAGE, and 7.0 T TOF. Angiographic Suzuki grades were evaluated for both sides. Patients with motion artifacts in MR images as well as patients without complete depiction of the CoW are indicated.
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Figure 1. Spatial resolution and coverage of the MR modalities used: 3.0 T TOF-MRA (A), 7.0 T TOF-MRA (B), and 7.0 T MPRAGE-MRA (C). 3.0 T TOF-MRA displayed 8.2-cm vertical coverage (acquisition time: 5 minutes and 54 seconds), 7.0 T TOF-MRA 5.1 cm (scanning time of 8 minutes and 16 seconds), whereas 7.0 T MPRAGEMRA allowed for whole-brain coverage (acquisition time: 5 minutes and 40 seconds). Abbreviations: DSA, digital subtraction angiography; MPRAGE, magnetization-prepared rapid-acquisition gradient echo; MR, magnetic resonance; MRA, magnetic resonance angiography; TOF, time of flight.
sequence prone to bulk motion artifacts. Therefore, further developments need to reduce the specific absorption rate of 7.0 T TOF-MRA. MPRAGE-MRA is an alternative angiography technique at 7.0 T that provides whole-brain coverage and has been shown to provide superior quality
DSA
3.0 T TOF-MRA
compared to routine 3.0 T TOF-MRA imaging20,21. Our study suggests that a resolution of approximately 0.7 mm used for 7.0 T MPRAGE-MRA is sufficient to provide the information necessary in patients with MMV. This also applies to visualization of the extracranial donor vessel
7.0 T MPRAGE
7.0 T TOF-MRA
Figure 2. This 21-year-old female patient presented with transitory hypesthesia of the right-side extremities. She was diagnosed with bilateral MCA stenosis (left: high grade, right: middle grade) and MMD. DSA, 3.0 T TOF-MRA, 7.0 T MPRAGE-MRA, and 7.0 T TOF-MRA displayed high-grade stenosis of the left-sided MCA sufficiently. 7.0 T MPRAGE-MRA and 7.0 T TOF-MRA depicted moyamoya-specific collateral vessels in more detail than 3.0 T TOF-MRA. MR images are presented in 3D (first row) and as axial slices at the level of ICA bifurcation. Bottom line: Depiction of the left-sided external carotid artery in the same patient. Here, we present all 4 modalities (DSA, 3.0 T TOF-MRA, 7.0 T MPRAGE, and 7.0 T TOF-MRA) with special focus on the STA to display the potential donor vessel for EC–IC bypass. Due to limited coverage, 3.0 T TOF-MRA and 7.0 T TOF-MRA did not display the complete vessel. Abbreviations: DSA, digital subtraction angiography; EC–IC, extracranial–intracranial; ICA, internal carotid artery; MCA, middle cerebral artery; MMD, moyamoya disease; MPRAGE, magnetization-prepared rapid-acquisition gradient echo; MRA, magnetic resonance angiography; STA, superficial temporal artery; TOF, time of flight.
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A
DSA
3.0 T TOF
7.0 T MPR
7.0 T TOF
B
DSA
3.0 T TOF
7.0 T MPR
3.0 T TOF
C
DSA
3.0 T TOF
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7.0 T TOF
D
DSA
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3.0 T TOF
7.0 T MPR
E
DSA
3.0 T TOF
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Figure 3. DSA images of all patients included in our study. (A) This 28-year-old female patient (patient 1, Table 1) suffered from TIAs with right-sided brachiofacial palsy. DSA depicted a left-sided occlusion of the ICA. The first 4 columns show the different 2D modalities: DSA, 3.0 T TOF-MRA (3 T TOF), 7.0 T MPRAGE-MRA (7 T MPR), and 7.0 T TOF-MRA (7 T TOF). On the right, a sagittal DSA with depiction of collateral vessels and a 3D 7.0 T TOF-MRA of the same patient is presented. (B) A 40-year-old male patient with bilateral MCA occlusion presented with recurrent TIAs including left-sided brachial palsy (patient 2, Table 1). DSA, axial 3.0 T TOF-MRA, and 7.0 T MPRAGE-MRA as well as 3D reconstruction are presented. The placement of the 7.0 T TOF-MRA region of interest did not include the ICA bifurcation and representable images could not be generated. (C) Bilateral ICA occlusion in this 18-year-old female patient is identified with all 4 modalities (patient 3, Table 1). She suffered aphasia and TIAs presenting with right-sided hemiparesis. On the right, a sagittal view of collateralization is depicted with DSA images (top) and a 3D image of the major cerebral vessels with 7.0 T TOF-MRA (bottom). (D) Right-sided high-grade MCA stenosis was responsible for intermittent aphasia and right-sided hemiparesis in this 28-year-old male patient (patient 4, Table 1). We present DSA images as well as 3.0 T TOF-MRA and 7.0 T MPRAGE-MRA images in 2D and 3D. (E) A left-sided MCA occlusion and high-grade stenosis of the right MCA was present in this 33-year-old female patient. We show DSA images of the rightsided MCA stenosis as well as 2D and 3D 3.0 T TOF-MRA and 7.0 T MPRAGE-MRA images. 7.0 T images were more sensitive to patient movement during the examination and motion artifacts can be identified. Abbreviations: DSA, digital subtraction angiography; ICA, internal carotid artery; MCA, middle cerebral artery; MPRAGE, magnetization-prepared rapid-acquisition gradient echo; MRA, magnetic resonance angiography; TIA, transient ischemic attack; TOF, time of flight.
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in preparation for bypass surgery. Given the better visualization of small vessels compared to 3.0 T imaging, our results strengthen the notion that 7.0 T MPRAGEMRA is superior to 3.0 T TOF-MRA and 7.0 T TOFMRA imaging, while providing high resolution and wholebrain coverage at the same time. However, the limited availability of 7.0 T MPRAGE-MRA reduces the clinical relevance of this technique at the current state. In future studies, 7.0 T MPRAGE-MRA may be considered as a viable alternative to the current gold-standard DSA, which is associated with considerable risk for the patients. Another imaging technique is the less invasive computed tomography angiography, which proved to be a solid diagnostic tool in MMD 22 and was shown to provide a high image quality for postoperative bypass assessment,9 as there will be medical facilities that will never use UHF MR technology. Also, for patients with metallic implants or other contraindications for MRI, computed tomography angiography remains a sound diagnostic option with an acceptable risk profile. One remaining advantage of DSA, however, is the dynamics of the acquired image series, which allows assessment of the status of collateralization for the individual patient. TOF techniques as investigated in the present study do not offer dynamic information about flow and thus do not allow investigation of the extent of perfusion compensation via collaterals. However, collateral status can be assessed using MRI, by applying either rapid gadolinium-based techniques23 or arterial spin-labeling approaches,24 and both can be combined with MRA in a single session. Our study is limited since only MRA source images were compared, as the generation of maximum intensity projection images for MPRAGE angiography is currently not yet standardized. A major limitation of our study is that only few patients (14%) screened for participation in our study were eligible due to the very strict safety and regulatory measures required for study clearance by the appropriate authorities. This was experienced as well by other groups performing 7.0 T imaging.25 Therefore, our study is a pilot study showing the potential advantages of UHF imaging for patients with MMV. It can be expected that with future clinically approved 7.0 T MRIsystems and metallic implants certified for UHF MRI, more patients will be eligible for 7.0 T MRI imaging and studies on UHF MRI. In conclusion, our results indicate that a specific 7.0 T vascular imaging protocol yields diagnostic information about vessel pathology in MMV that approximates conventional DSA. 7.0 T MPRAGE-MRA was superior to 7.0 T TOF-MRA due to shorter scanning times and better brain coverage. To date, however, motion artifacts, a limited availability of 7.0 T technology in medical facilities, and contraindications such as metallic implants exclude a fair amount of patients from the clinical 7.0 T imaging process.
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ARTICLE IN PRESS 8 18. Maderwald S, Ladd SC, Gizewski ER, et al. To TOF or not to TOF: strategies for non-contrast-enhanced intracranial MRA at 7.0 T. MAGMA 2008;21:159-167. 19. Monninghoff C, Maderwald S, Theysohn JM, et al. Evaluation of intracranial aneurysms with 7.0 T versus 1.5 T time-of-flight MR angiography—initial experience. Rofo 2009;181:16-23. 20. Wrede KH, Dammann P, Monninghoff C, et al. Nonenhanced MR imaging of cerebral aneurysms: 7 Tesla versus 1.5 Tesla. PLoS ONE 2014;9:e84562. 21. Madai VI, von Samson-Himmelstjerna FC, Sandow N, et al. Ultrahigh-field MPRAGE magnetic resonance angiography at 7.0T in patients with cerebrovascular disease. Eur J Radiol 2015;84:2613-2617.
N.F. DENGLER ET AL. 22. Tsuchiya K, Makita K, Furui S. Moyamoya disease: diagnosis with three-dimensional CT angiography. Neuroradiology 1994;36:432-434. 23. Kim SJ, Son JP, Ryoo S, et al. A novel magnetic resonance imaging approach to collateral flow imaging in ischemic stroke. Ann Neurol 2014;76:356-369. 24. Zaharchuk G, Do HM, Marks MP, et al. Arterial spinlabeling MRI can identify the presence and intensity of collateral perfusion in patients with moyamoya disease. Stroke 2011;42:2485-2491. 25. Fischer A, Maderwald S, Johst S, et al. Initial evaluation of non-contrast-enhanced magnetic resonance angiography in patients with peripheral arterial occlusive disease at 7.0 T. Invest Radiol 2014;49:331-338.
Moyamoya Vessel Pathology Imaged by Ultra–High-Field Magnetic Resonance Imaging at 7.0 T Nora F. Dengler, MD,* Vince I. Madai, MD,†‡ Jens Wuerfel, MD,‡§‖¶** Federico C. von Samson-Himmelstjerna, PhD,‡‡‡ Petr Dusek, MD,‖†† Thoralf Niendorf, PhD,¶ Jan Sobesky, MD,†‡ and Peter Vajkoczy, MD*
Background: Prompt diagnosis of vessel pathology and appropriate treatment of moyamoya vasculopathy (MMV) are essential to improve long-term prognosis. The aims of our study were to explore the diagnostic value of ultra–high-field (UHF) magnetic resonance imaging at 7.0 T in MMV patients and to compare the applicability of two different 7.0 T vessel imaging modalities to 3.0 T magnetic resonance angiography (MRA) and digital subtraction angiography (DSA). Methods: In a World Health Organization-registered and prospective imaging trial, patients were investigated at 7.0 T magnetization-prepared rapid-acquisition gradient echo (MPRAGE)-MRA and time-of-flight (TOF)-MRA, 3.0 T TOF-MRA, and by DSA. Results: Six patients were included in our study and evaluated for MMV. 3.0 T TOF-MRA and 7.0 T MPRAGE-MRA were able to depict the complete major vascular tree and confirmed MMV-specific steno-occlusions of major intracranial arteries, as previously identified by DSA. 7.0 T TOF-MRA was limited to visualization of the circle of Willis as well as the internal carotid artery only. Donor vessels for bypass surgery (i.e., branches of superficial temporal artery) could be sufficiently visualized with all magnetic resonance modalities. Conclusions: Our results indicate that a specific 7.0 T vascular imaging protocol yields diagnostic information about vessel pathology in MMV that approximates conventional DSA. 7.0 T MPRAGE was superior to 7.0 T TOF-MRA due to shorter scanning times and better brain coverage. To date, however, limited availability of 7.0 T technology in medical facilities as well as technical and procedural constraints excludes a fair amount of patients from the clinical 7.0 T imaging process. Key Words: MRI—ultra–high-field MR—7.0 T—moyamoya—stroke—extracranial–intracranial bypass. © 2016 National Stroke Association. Published by Elsevier Inc. All rights reserved.
From the *Department of Neurosurgery, Charité Universitätsmedizin Berlin, Berlin, Germany; †Department of Neurology, Charité Universitätsmedizin Berlin, Berlin, Germany; ‡Center for Stroke Research Berlin (CSB), Charité Universitätsmedizin Berlin, Berlin, Germany; §Neurocure Clinical Research Centre, Charité Universitätsmedizin Berlin, Berlin, Germany; ‖Institute of Neuroradiology, University Göttingen, Göttingen, Germany; ¶Berlin Ultra-High Field Facility (B.U.F.F.), Max Delbrück Center for Molecular Medicine (MDC), Berlin, Germany; **Medical Image Analysis Center (MIAC AG), Basel, Switzerland; ††Department of Neurology and Center of Clinical Neuroscience, Charles University in Prague, First Faculty of Medicine and General University Hospital in Prague, Praha, Czech Republic; and ‡‡Fraunhofer MEVIS, Bremen, Germany. Received November 13, 2015; revision received January 20, 2016; accepted January 29, 2016. Conflict of interest: Thoralf Niendorf is founder and CEO of MRI.TOOLS GmbH, Berlin, Germany, and received speaker honoraria from Siemens Healthcare. Jens Wuerfel is CEO of the Medical Image Analysis Center (MIAC AG), Basel, Swizerland. He received research grants from Novartis and Biogen, and speaker honoraria from Bayer, Novartis, Teva, and Biogen. He served for advisory boards for Novartis and Biogen. He is supported by the German Ministry of Science (BMBF/KKNMS) and the German Ministry of Economy (BMWi). Apart from the scanner, no other resources of Siemens Healthcare, MRI.TOOLS GmbH, and MIAC AG were used, and the companies had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. Address correspondence to Peter Vajkoczy, MD, Department of Neurosurgery, Charité Universitätsmedizin Berlin, Augustenburger Platz 1, 13353 Berlin, Germany. E-mail: [email protected]. 1052-3057/$ - see front matter © 2016 National Stroke Association. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jstrokecerebrovasdis.2016.01.041
Journal of Stroke and Cerebrovascular Diseases, Vol. ■■, No. ■■ (■■), 2016: pp ■■–■■
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Introduction Moyamoya vasculopathy (MMV) presents with mostly bilateral progressive stenosis of the terminal internal carotid artery (ICA). Affected patients develop pathognomonic collateral pathways that can lead to ischemic or hemorrhagic lesions and consecutive permanent or transient neurological deficits.1-4 To improve long-term prognosis of patients with MMV, prompt diagnosis of vessel pathology and appropriate treatment, for example, revascularization surgery, is mandatory.5-7 To date, digital subtraction angiography (DSA) is considered the “gold standard” for the diagnosis of MMV.8,9 DSA can be omitted when magnetic resonance imaging (MRI) and magnetic resonance angiography (MRA) with a field strength of 1.5 T or higher provide information about stenosis or occlusion of the terminal portion of the ICA or proximal portion of the anterior cerebral artery (ACA) and/or the middle cerebral artery (MCA) as well as abnormal vascular networks in the basal ganglia and collateral pathways.7,10,11 However, for preoperative planning, postoperative control, and follow-up of revascularizing procedures such as extracranial–intracranial bypass (EC– IC bypass), DSA is still the required standard. It would be beneficial for patients with MMV to undergo only MRI as a noninvasive diagnostic test that yields information about new ischemic lesions, high-resolution imaging of vessel dynamics, and bypass patency in contrast to a battery of examinations containing the combination of MRI and an invasive and radiation exposing DSA. The potential of ultra–high-field (UHF) MRI at 7.0 T in cerebrovascular disease has been shown recently.12-14 A major benefit is expected for MRA due to increased spatial resolution and novel contrast mechanisms.15,16 A 7.0 T MRA might therefore contribute substantial impact for the diagnosis of MMV. The aim of our study was to explore the diagnostic value of UHF MRA in MMV patients. We hypothesized that UHF MRA can yield preoperative diagnostic information equivalent to DSA for detection of MMV as well as for evaluation and planning of EC–IC bypass surgery.
Methods Study Protocol Patients were imaged within an ongoing World Health Organization-registered and prospective imaging trial (7UP, World Health Organization register No. DRKS00003193) before EC–IC bypass. Screening was performed between June 2012 and April 2014. Fully developed MMV was defined by bilateral stenosis or occlusion of the ICA or proximal portions of the ACA and/or the MCA as well as bilateral abnormal vascular networks, and was referred to as moyamoya disease (MMD). Unilateral MMV was referred to as “probable MMD” according to current guidelines.7 Inclusion criteria were confirmed or proba-
ble MMV, subacute/chronic ischemia or transient ischemic attack, age 18-80 years, ability to give informed consent, and legal competence. Exclusion criteria were any electronic and metallic implants, pregnancy or breast-feeding period, claustrophobia, chronic or episodic vertigo, retinal diseases, and dental bridges and/or more than 2 metallic dental crowns in a row. Neurological status was assessed at the time of admission. MRI was performed first at 3.0 T, immediately followed by MRI at 7.0 T. A neurologist specialized in stroke supervised the patients during the MRI examination. All patients gave informed written consent before the study. The study was approved by the authorized ethical review board, the governmental Berlin state ethical review board, and the relevant German state authority, the Federal Institute for Drugs and Medical Devices. Cerebral blood flow and reserve capacity in each patient were detected by positron emission tomography or singlephoton emission computed tomography (before and after forced vessel dilation by diamox).
MRI Hardware MRI was performed on a 3.0 T whole-body system (Magnetom Verio; Siemens Healthcare, Erlangen, Germany). A body coil was used for excitation and a 12-channel radio frequency (RF) receive coil (Siemens Healthcare) tailored for head imaging was employed for reception. At 7.0 T, a whole-body system (Magnetom 7.0 T, Siemens Healthcare) equipped with a 90 cm bore magnet (Magnex Scientific, Oxfordshire, United Kingdom) and an Avanto gradient system (Siemens Healthcare) was used together with a 1/24channel transmit/receive coil (Model NM 008-23-7S; NovaMedical, Wakefield, MA) designed for head imaging.
MRI Parameters The imaging protocol included MRA using 3D magnetization-prepared rapid-acquisition gradient echo (MPRAGE), time-of-flight (TOF)-MRA, T 2 -weighted imaging, and susceptibility-weighted imaging (SWI) at 7.0 T. A 3.0 T TOF-MRA and T2*-weighted imaging were conducted. Detailed parameters of the angiographic imaging techniques were as follows:
• 7.0 T T1-weighted 3D-MPRAGE: repetition time (TR): 2750 ms, echo time (TE): 1.81 ms, acceleration factor: 3 (Grappa), bandwidth: 350 Hz/pixel, voxel size: 0.7 × 0.7 × 0.7 mm3, matrix size: 384 × 384, flip angle: 10°, acquisition time: 5 minutes and 40 seconds, number of slabs: 1 (240 slices), and whole-brain coverage. • 7.0 T 3D TOF-MRA: TR: 32 ms, TE: 3.53 ms, no acceleration factor, bandwidth: 305 Hz/pixel, voxel size: 0.4 × 0.4 × 0.4 mm3, matrix size: 512 × 512, flip angle: 25°, acquisition time: 8 minutes and 16 seconds, number of slabs: 1 (128 slices), and 5.1 cm vertical coverage.
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• 3.0 T 3D TOF-MRA: TR: 24 ms, TE: 3.60 ms, acceleration factor: 2 (Grappa), bandwidth: 186 Hz/ pixel, voxel size: 0.6 × 0.6 × 0.6 mm3, matrix size: 384 × 384, flip angle: 18°, acquisition time: 5 minutes and 54 seconds, number of slabs: 4 (40 slices per slab), and 8.2 cm vertical coverage. Detailed parameters of the other imaging techniques were as follows:
• 7.0 T 3D SWI: TR: 22 ms, TE: 15.0 ms, acceleration factor: 2 (Grappa reconstruction), bandwidth: 120 Hz/ pixel, voxel size: 0.6 × 0.6 × 0.6 mm3, matrix size: 384 × 384, flip angle: 15°, and acquisition time: 10 minutes and 25 seconds. • 3.0 T 2D T2*-weighted imaging: TR: 800 ms, TE: 3.60 ms, no acceleration factor, bandwidth: 260 Hz/pixel, voxel size: 1.1 × 0.7 × 4.0 mm3, matrix size 256 × 230, flip angle: 25°, and acquisition time: 2 minutes and 35 seconds.
Analysis All 3.0 and 7.0 T images of our patients were evaluated independently by 2 reviewers (N.F.D. and V.I.M.) for determination of magnetic resonance (MR) MMV grades10 as well as DSA images for Suzuki grades.1
Results Patient Characteristics Forty-two patients admitted for evaluation of MMV to our neurosurgical department were screened for the study. Two patients refused informed consent, 34 patients were excluded due to metallic implants (n = 30) or tattoos (n = 4). In total, 6 patients with unilateral (n = 2) or bilateral (n = 4) MMV could be included in the study (4 females, 2 males) (Table 1). The median age was 28 years (interquartile range: 19.5-34). All 6 patients presented with recurrent transient neurological deficits, 1 patient also suffered from permanent left-sided hemiparesis. In all patients, typical collateral pathways were present and could be identified by DSA (Table 1). Four patients were classified as Suzuki grade 2°, 1 patient as Suzuki grade 3°, and 1 patient as Suzuki grade 4°. None of our patients showed signs of hemorrhages (e.g., microbleeds) at any of the 2 field strengths. Three patients underwent bilateral and 1 patient unilateral EC– IC bypass surgery in accordance with proven severely restricted reserve capacity.
Major Cerebral Artery and Small-Vessel Pathology In all 6 patients, 3.0 T TOF-MRA and 7.0 T MPRAGEMRA were able to depict the complete major vascular tree and showed MMV-specific steno-occlusions of major cerebral arteries, matching the results obtained by DSA. In contrast, identification of MMV pathologies by 7.0 T TOF-MRA was limited to the circle of Willis as well as
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the ICA (Fig 1). Motion artifacts were present in 3 out of 6 7.0 T TOF image series, due mainly to long scan times evoked by RF power deposition constraints. The overall impression of 7.0 T images (MPRAGE and TOF) was a more detailed depiction of small moyamoyaspecific vessels in comparison with 3.0 T MR images (Figs 2, 3). MR grading according to Houkin et al17 was performed for 3.0 T TOF-MRA, 7.0 T MPRAGE-MRA, and 7.0 T TOF-MRA. In differentiation between stenosis, discontinuity or invisible ICA or MCA similar results were obtained with only slight differences present between the 3 modalities (Table 1). Imaging with 7.0 T technology tended to show higher grades as the differentiation between an invisible, discontinuous or stenotic vessel was easier at 7.0 T MRI. (Figs 2, 3). Collateral vessels were not consistently identified in all MR modalities.
Donor Vessel Imaging In 4 patients, the MRI field of view was expanded to visualize possible donor vessels for EC–IC bypass surgery (superficial temporal artery). In all 4 patients, donor vessels were adequately identified with all MR modalities (7.0 T MPRAGE, 7.0 T TOF-MRA, and 3.0 T TOF-MRA) and were comparable to DSA visualization quality (Figs 2, 3).
Discussion We present the first comparison of 3.0 T, 7.0 T, and DSA vessel imaging of patients with MMV. Our results indicate that major vessel pathology and donor vessel visualization are adequate with all 3 modalities. The quality of 7.0 T MPRAGE-MRA, however, was superior to 3.0 T TOF images in detecting moyamoya-specific smallvessel pathology and seems to offer a better resolution for assessment of MRA grades. The highest spatial resolution was shown by 7.0 T TOF, but brain coverage was limited and motion artifacts were frequent. For major arteries of the circle of Willis, the diagnostic value of 7.0 T MPRAGE-MRA and 7.0 T TOF-MRA was at least equivalent to 3.0 T TOF-MRA. Steno-occlusive changes were similarly detected with both modalities and were in line with DSA findings. Differentiation of ICA or MCA pathologies for MRA grading10,17 was more precise with 7.0 T MPRAGE-MRA and 7.0 T TOF-MRA images. Only 7.0 T MPRAGE-MRA and 7.0 T TOF-MRA were able to depict MMV-specific small-vessel pathologies comparable with DSA. Considering previous MR studies of MMV, higher magnetic field strength seems to correlate with more precise results of MRA.11,12,16,18-20 Isotropic spatial resolution of conventional angiography has been described to be 0.4 mm, which is theoretically comparable to the 0.4 mm isotropic resolution of our 7.0 T TOF-MRA images. However, at the current stage of development, the brain coverage of 7.0 T TOF-MRA is severely limited due to RF power deposition constraints, and the resulting long scan times render the MRA
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Table 1. Clinical, MRI and angiographic findings in our patient series evaluated for suspected MMV Patient
Sex Age Side Pathology TIA Permanent nD Bypass T2 MRI findings 7.0 T microbleeds 3.0 T microbleeds MRI grades 3.0 T TOF ICA R 3.0 T TOF MCA R 3.0 T TOF ACA R 3.0 T TOF PCA R 3.0 T TOF ICA L 3.0 T TOF MCA L 3.0 T TOF ACA L 3.0 T TOF PCA L 7.0 T MPR ICA R 7.0 T MPR MCA R 7.0 T MPR ACA R 7.0 T MPR PCA R 7.0 T MPR ICA L 7.0 T MPR MCA L 7.0 T MPR ACA L 7.0 T MPR PCA L 7.0 T TOF ICA R 7.0 T TOF MCA R 7.0 T TOF ACA R 7.0 T TOF PCA R 7.0 T TOF ICA L 7.0 T TOF MCA L 7.0 T TOF ACA L 7.0 T TOF PCA L Suzuki left Suzuki right Collateralization Motion artifacts Complete CoW
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2
3
4
5
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Female 28 Left ICA occlusion Yes No Left Left atrophy
Female 18 Bilateral ICA occlusion Yes No Bilateral Right ACA infarction No No
Male 28 Right MCA occlusion Yes No None No
Female 21 Bilateral MCA stenosis Yes Yes None No
Female 33 Bilateral MCA occlusion Yes No Bilateral No
No No
Male 40 Bilateral MCA occlusion Yes No Bilateral Right ACA infarction No No
No No
No No
No No
0 0 0 0 1 3 0 0 0 0 0 0 1 2 0 0 0 0 0 0 1 2 0 0 3 — lm, vb, eth, Acha No Yes
0 3 0 0 0 3 0 0 1 3 0 0 0 2 0 0 n.d. 2 0 n.d. n.d. 3 0 n.d. 2 2 ACA, PCA, Acha No No
1 2 1 0 1 2 1 0 1 1 2 0 1 2 2 0 0 2 0 0 0 2 0 0 4 3 eth, PCA, Acha, ls, lm Yes Yes
0 2 0 0 0 0 0 0 0 2 0 0 0 0 0 0 0 1 0 0 0 0 0 0 — 2 ACA, PCA, eth Yes Yes
0 2 0 0 0 2 0 0 1 1 0 0 1 1 0 0 0 2 0 0 0 1 0 0 2 2 ACA, PCA, eth, lm No Yes
0 2 0 0 0 3 0 0 1 1 0 0 0 2 0 0 0 1 0 0 0 1 0 0 2 2 ACA, PCA, eth, lm Yes Yes
Abbreviations: ACA, anterior cerebral artery; Acha, anterior choroidal artery; CoW, circle of Willis; EC–IC, extracranial–intracranial; eth, ethmoidal; ICA, internal carotid artery; L, left; lm, leptomeningeal; MCA, middle cerebral artery; MMV, moyamoya vasculopathy; MPRAGE, magnetization-prepared rapid-acquisition gradient echo; MRI, magnetic resonance imaging; n.d., not detected; nD, neurological deficit; PCA, posterior cerebral artery; R, right; SWI, susceptibility-weighted imaging; TIA, transient ischemic attack; TOF, time of flight; vb, vertebrobasilar. Clinical findings are displayed with respect to sex, age, side of vessel pathology, type of vessel pathology (occlusion or high-grade stenosis), presence of TIA, presence of permanent nD, and indication for EC–IC bypass surgery. T2 MRI findings such as infarction or atrophy are depicted as well as occurrence of microbleeds in 3.0 T SWI and 7.0 T SWI. MRI grades of vascular pathology were evaluated for 3.0 T TOF, 7.0 T MPRAGE, and 7.0 T TOF. Angiographic Suzuki grades were evaluated for both sides. Patients with motion artifacts in MR images as well as patients without complete depiction of the CoW are indicated.
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Figure 1. Spatial resolution and coverage of the MR modalities used: 3.0 T TOF-MRA (A), 7.0 T TOF-MRA (B), and 7.0 T MPRAGE-MRA (C). 3.0 T TOF-MRA displayed 8.2-cm vertical coverage (acquisition time: 5 minutes and 54 seconds), 7.0 T TOF-MRA 5.1 cm (scanning time of 8 minutes and 16 seconds), whereas 7.0 T MPRAGEMRA allowed for whole-brain coverage (acquisition time: 5 minutes and 40 seconds). Abbreviations: DSA, digital subtraction angiography; MPRAGE, magnetization-prepared rapid-acquisition gradient echo; MR, magnetic resonance; MRA, magnetic resonance angiography; TOF, time of flight.
sequence prone to bulk motion artifacts. Therefore, further developments need to reduce the specific absorption rate of 7.0 T TOF-MRA. MPRAGE-MRA is an alternative angiography technique at 7.0 T that provides whole-brain coverage and has been shown to provide superior quality
DSA
3.0 T TOF-MRA
compared to routine 3.0 T TOF-MRA imaging20,21. Our study suggests that a resolution of approximately 0.7 mm used for 7.0 T MPRAGE-MRA is sufficient to provide the information necessary in patients with MMV. This also applies to visualization of the extracranial donor vessel
7.0 T MPRAGE
7.0 T TOF-MRA
Figure 2. This 21-year-old female patient presented with transitory hypesthesia of the right-side extremities. She was diagnosed with bilateral MCA stenosis (left: high grade, right: middle grade) and MMD. DSA, 3.0 T TOF-MRA, 7.0 T MPRAGE-MRA, and 7.0 T TOF-MRA displayed high-grade stenosis of the left-sided MCA sufficiently. 7.0 T MPRAGE-MRA and 7.0 T TOF-MRA depicted moyamoya-specific collateral vessels in more detail than 3.0 T TOF-MRA. MR images are presented in 3D (first row) and as axial slices at the level of ICA bifurcation. Bottom line: Depiction of the left-sided external carotid artery in the same patient. Here, we present all 4 modalities (DSA, 3.0 T TOF-MRA, 7.0 T MPRAGE, and 7.0 T TOF-MRA) with special focus on the STA to display the potential donor vessel for EC–IC bypass. Due to limited coverage, 3.0 T TOF-MRA and 7.0 T TOF-MRA did not display the complete vessel. Abbreviations: DSA, digital subtraction angiography; EC–IC, extracranial–intracranial; ICA, internal carotid artery; MCA, middle cerebral artery; MMD, moyamoya disease; MPRAGE, magnetization-prepared rapid-acquisition gradient echo; MRA, magnetic resonance angiography; STA, superficial temporal artery; TOF, time of flight.
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A
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E
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Figure 3. DSA images of all patients included in our study. (A) This 28-year-old female patient (patient 1, Table 1) suffered from TIAs with right-sided brachiofacial palsy. DSA depicted a left-sided occlusion of the ICA. The first 4 columns show the different 2D modalities: DSA, 3.0 T TOF-MRA (3 T TOF), 7.0 T MPRAGE-MRA (7 T MPR), and 7.0 T TOF-MRA (7 T TOF). On the right, a sagittal DSA with depiction of collateral vessels and a 3D 7.0 T TOF-MRA of the same patient is presented. (B) A 40-year-old male patient with bilateral MCA occlusion presented with recurrent TIAs including left-sided brachial palsy (patient 2, Table 1). DSA, axial 3.0 T TOF-MRA, and 7.0 T MPRAGE-MRA as well as 3D reconstruction are presented. The placement of the 7.0 T TOF-MRA region of interest did not include the ICA bifurcation and representable images could not be generated. (C) Bilateral ICA occlusion in this 18-year-old female patient is identified with all 4 modalities (patient 3, Table 1). She suffered aphasia and TIAs presenting with right-sided hemiparesis. On the right, a sagittal view of collateralization is depicted with DSA images (top) and a 3D image of the major cerebral vessels with 7.0 T TOF-MRA (bottom). (D) Right-sided high-grade MCA stenosis was responsible for intermittent aphasia and right-sided hemiparesis in this 28-year-old male patient (patient 4, Table 1). We present DSA images as well as 3.0 T TOF-MRA and 7.0 T MPRAGE-MRA images in 2D and 3D. (E) A left-sided MCA occlusion and high-grade stenosis of the right MCA was present in this 33-year-old female patient. We show DSA images of the rightsided MCA stenosis as well as 2D and 3D 3.0 T TOF-MRA and 7.0 T MPRAGE-MRA images. 7.0 T images were more sensitive to patient movement during the examination and motion artifacts can be identified. Abbreviations: DSA, digital subtraction angiography; ICA, internal carotid artery; MCA, middle cerebral artery; MPRAGE, magnetization-prepared rapid-acquisition gradient echo; MRA, magnetic resonance angiography; TIA, transient ischemic attack; TOF, time of flight.
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in preparation for bypass surgery. Given the better visualization of small vessels compared to 3.0 T imaging, our results strengthen the notion that 7.0 T MPRAGEMRA is superior to 3.0 T TOF-MRA and 7.0 T TOFMRA imaging, while providing high resolution and wholebrain coverage at the same time. However, the limited availability of 7.0 T MPRAGE-MRA reduces the clinical relevance of this technique at the current state. In future studies, 7.0 T MPRAGE-MRA may be considered as a viable alternative to the current gold-standard DSA, which is associated with considerable risk for the patients. Another imaging technique is the less invasive computed tomography angiography, which proved to be a solid diagnostic tool in MMD 22 and was shown to provide a high image quality for postoperative bypass assessment,9 as there will be medical facilities that will never use UHF MR technology. Also, for patients with metallic implants or other contraindications for MRI, computed tomography angiography remains a sound diagnostic option with an acceptable risk profile. One remaining advantage of DSA, however, is the dynamics of the acquired image series, which allows assessment of the status of collateralization for the individual patient. TOF techniques as investigated in the present study do not offer dynamic information about flow and thus do not allow investigation of the extent of perfusion compensation via collaterals. However, collateral status can be assessed using MRI, by applying either rapid gadolinium-based techniques23 or arterial spin-labeling approaches,24 and both can be combined with MRA in a single session. Our study is limited since only MRA source images were compared, as the generation of maximum intensity projection images for MPRAGE angiography is currently not yet standardized. A major limitation of our study is that only few patients (14%) screened for participation in our study were eligible due to the very strict safety and regulatory measures required for study clearance by the appropriate authorities. This was experienced as well by other groups performing 7.0 T imaging.25 Therefore, our study is a pilot study showing the potential advantages of UHF imaging for patients with MMV. It can be expected that with future clinically approved 7.0 T MRIsystems and metallic implants certified for UHF MRI, more patients will be eligible for 7.0 T MRI imaging and studies on UHF MRI. In conclusion, our results indicate that a specific 7.0 T vascular imaging protocol yields diagnostic information about vessel pathology in MMV that approximates conventional DSA. 7.0 T MPRAGE-MRA was superior to 7.0 T TOF-MRA due to shorter scanning times and better brain coverage. To date, however, motion artifacts, a limited availability of 7.0 T technology in medical facilities, and contraindications such as metallic implants exclude a fair amount of patients from the clinical 7.0 T imaging process.
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