Case 9 A 32-year-old white man was admitted after suffering a mild brachiofacial weakness, aphasia, and a homonymous hemianopia to the right side. He was a smoker. No further vascular risk factors were present. On admission, no sensorimotor deficit was detected but he had a right homonymous hemianopia and mild fluent aphasia (National Institute of Health Stroke Scale [NIHSS] score: 3). Immediately performed MRI demonstrated on diffusion-weighted images a large acute territorial left occipital ischemia in the posterior cerebral artery (PCA) territory as well as a small territorial left parietal precentral infarction in the left middle cerebral artery (MCA) territory. FLAIR-weighted images unmasked a right frontal territorial infarction in the anterior cerebral artery (ACA) territory. Furthermore bilateral small internal border zone infarctions (BZI) and dilated leptomeningeal vessels pronounced on the left hemisphere were detected. Also, a moderate parietal accentuated hemiatrophy was seen on the right side. Contrast-enhanced MR angiography (ce-MRA) showed signs of bilateral distal carotid artery occlusion in otherwise normal extracranial brain-supplying arteries. The MCA and ACA were undetectable on both sides. Instead, multiple small vessels were seen. Otherwise, the insular and cortical branches appeared normal. Intracranial time-of-flight (TOF) MRA was also suspicious for bilateral proximal MCA and ACA occlusion. However, on T2-weighted images both M1-MCAs could be depicted by their signal voids, indicating real flow in these vessels (Fig. B9.1, Fig. B9.2, Fig. B9.3, Fig. B9.4). Because of the large infarcted areas no thrombolysis was performed. Bilateral territorial and hemodynamic infarctions in bilateral severe steno-occlusive distal internal carotid artery (ICA) pathology compatible with moyamoya disease (MMD). Selective ICA contrast filling demonstrated bilateral terminal ICA occlusion. Furthermore, a network of small capillary collateral vessels was visible in the region of the distal ICA and proximal MCA. The distal branches of both MCAs and ACAs, seen in the late arterial phase, showed regular contrast. In addition, a collateral leptomeningeal flow was seen via the posterior communicating artery (PCoA) and dural anastomoses on the right side. Selective left vertebral artery (VA) filling yielded a prominent right PCA and the suspicion of a left distal PCA occlusion. Similar to the anterior circulation, a network of small vessels indicating collateral pathways was seen in the area of the proximal PCA (Fig. B9.5, Fig. B9.6, Fig. B9.7, Fig. B9.8). Moyamoya disease stage IV with acute left MCA and PCA territorial strokes in severe carotid-T pathology and left-sided PCA occlusion. The neurologic deficits partially regressed and the patient was started on aspirin for secondary stroke prevention. For further occupational and physiotherapeutic treatment he was transferred to a rehabilitation center and an extracranial–intracranial (EC–IC) bypass was recommended to be performed after rehabilitation. A first detailed ultrasound examination was performed in the rehabilitation center. B-mode and color-mode imaging revealed no atherosclerotic vascular changes. The lumen of both ICAs appeared reduced compared with the diameter especially of the right VA. Doppler spectrum analysis showed normal and symmetric flow signals, but volume flow measurements showed mildly reduced flow in the ICAs and compensatory increased flow in the VAs (Fig. B9.9 and Fig. B9.10). Fig. B9.1 (A,B) MR diffusion-weighted image, axial plane. Hyperintense signals indicating acute territorial infarctions in the left PCA calcarine artery territory and left MCA prerolandic artery territories. Note the old right-sided ACA infarction (arrow) and the spared occipital pole (arrowhead). (Courtesy of Prof. Schramm, Neuroradiological Department, University Hospital Lübeck, Germany.) Fig. B9.2 MR FLAIR image, axial plane. (A) Mild parietal atrophy on the right side. Note the dilated leptomeningeal vessels (arrowheads) indicating increased and delayed flow. (B) Besides the post-central MCA infarction, small bilateral internal BZI can be seen (arrows). (Courtesy of Prof. Schramm, Neuroradiological Department, University Hospital Lübeck, Germany.) Fig. B9.3 Contrast-enhanced MRA showing a steno-occlusive pathology in both distal ICAs. Instead of MCA and ACA main stems, multiple bilateral small vessels can be seen, but the insular branches appear normal. Note the large diameter of the right VA, exceeding that of the right ICA. (Courtesy of Prof. Schramm, Neuroradiological Department, University Hospital Lübeck, Germany.) Fig. B9.4 (A) 3D TOF-MRA. Circle of Willis, coronal oblique maximal intensity projection (MIP). Absent flow signal in the M1-MCA (arrows) and A1-ACA on both sides as well as in the left PCA (arrow). Note the fine network-like collateral vessels surrounding the circle of Willis (arrowheads) (B) T2-weighted image, axial plane. In contrast to TOF-MRA, visible MCA signal voids indicate that both vessels remained open, even at its proximal site. Note that the T2-weighted images better delineate the multiple small collateral vessels surrounding the MCA, ACA, and PCA (arrowheads). (Courtesy of Prof. Schramm, Neuroradiological Department, University Hospital Lübeck, Germany.) Fig. B9.5 DSA, right selective ICA injection, lateral view. The DSA shows a right terminal ICA occlusion (dotted arrow). Collateral flow derives in part from the PCA via the PCoA (arrowhead). Note the typical network-like anastomoses in the area of the proximal MCA, which itself is not visualized (arrows). Small dural anastomoses are also visible (arrowheads). (Courtesy of Prof. Schramm, Neuroradiological Department, University Hospital Lübeck, Germany.) Fig. B9.6 DSA, right selective ICA injection, posteroanterior view. (A) Early arterial phase: No visible MCA but PCA leptomeningeal filling through the PCoA (arrows). Note a dural anastomosis (arrowheads). (B) Late arterial phase with visible insular and leptomeningeal branches of the right MCA and both ACA. As retrograde filling via the PCoA seemed unlikely, antegrade filling via the proximal MCA and ACA in addition to the collateral network has to be assumed, even if the M1-MCA and A1-ACA are not directly visible. (Courtesy of Prof. Schramm, Neuroradiological Department, University Hospital Lübeck, Germany.) Fig. B9.7 DSA, left selective VA injection, posteroanterior view. (A) Early arterial phase: Suspected stenosis of both proximal PCAs (arrowheads). Similar to the anterior circulation, a fine network can be seen surrounding both PCAs. (B) Late arterial phase: The right MCA territory is partially perfused by the PCA (arrow). (Courtesy of Prof. Schramm, Neuroradiological Department, University Hospital Lübeck, Germany.) Fig. B9.8 DSA, left selective VA injection, lateral view. (A) Early arterial phase: Better delineation of the fine collateral network compared with the posteroanterior view (arrows). (B) The late arterial phase demonstrates the posterior pericallosal artery connecting via the pericallosal artery with the anterior circulation (arrowhead). (Courtesy of Prof. Schramm, Neuroradiological Department, University Hospital Schleswig-Holstein, Lübeck, Germany.) Despite good insonation conditions, the distal ICA could not be detected on both sides. Using color-mode imaging, a network of small arteries was visible in both perimesencephalic cisterns. Both M1-MCAs revealed a poststenotic flow pattern, severely affected on the right side and moderate affected on the left side. Bilateral flow velocities were markedly reduced. A similar flow profile was observed in the right A1-ACA and no signal could be depicted in the left A1-ACA. The left PCA was patent. Turbulent flow and markedly raised flow velocities were observed in both P1/P2-PCA segments and also in cortical PCA branches, i.e., in the anterior temporal artery (ATA) and in the occipitotemporal artery (OTA). The ubiquity phenomenon in all accessible PCA segments was suggestive for increased collateral flow but did not rule out the presence of additional stenoses (Figs. B9.11–B9.18; see also Video B9.1). Fig. B9.9 Extracranial duplex, longitudinal plane. The right ICA appears small showing a decreased blood volume flow (BVF 210 mL/min). Fig. B9.10 Extracranial duplex, longitudinal plane. The right V2-VA has a large diameter and an unusually high blood volume flow (BVF 310 mL/min). Fig. B9.11 TCCS (transtemporal approach), right-sided insonation, midbrain plane. Severely poststenotic flow pattern with a marked decreased flow in the right M1-MCA (flow velocity 21/16 cm/s). Note the color signals in the perimesencephalic cistern corresponding to the small collaterals seen in the T2-weighted MR image (arrow). Fig. B9.12 TCCS (transtemporal approach), left-sided insonation, midbrain plane. Moderate poststenotic flow pattern with a decreased flow in the left M1-MCA (flow velocity 34/20 cm/s).
Moyamoya Disease
Clinical Presentation
Initial Neuroradiologic Findings
Suspected Diagnosis
Conventional Angiography (Day 3)
Conclusion
Clinical Course (1)
Questions to Answer by Ultrasound Techniques
Initial Neurosonologic Findings (Week 6)
Extracranial Duplex Sonography
Transcranial Duplex Sonography