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Case 8 Bilateral Intracranial V4 Vertebral Artery Stenosis
166
creased flow velocities in both V4-VA segments, reaching a peak systolic flow velocity of 175cm/s (insonation depth: 61 mm) on the left side and 169 cm/s (insonation depth: 67 mm) on the right. The BA had a normal flow pattern (Figs.B8.8B8.10).
Degree of Neurosonologic Difculty: Low
Conclusion
Bilateral left-pronounced intracranial VA stenoses. Reste­nosis of the left VA after balloon dilatation. No evidence of reocclusion or stenosis of the BA.
Fig. B8.1 DSA, left VA injection, posteroanterior view. Left VA-V4 stenosis (arrowhead) and BA occlusion starting at the midbasilar region (arrow), (courtesy of Dr. Faiss, Asklepios FachklinikumTeupitz, Teu pitz , Ge rman y).
Fig. B8.3 Unenhanced CT, axial plane. Circumscribed right cerebel­lar infarction within the SCA territory (arrow), (courtesy of Dr. Faiss, Asklepios Fachklinikum Teupitz, Teupitz, Germany).
Fig. B8.2 DSA, left VA injection, posteroanterior view. Complete recanalization of the BA after intraarterial thrombolysis. Diminished left V4-VA stenosis after balloon dilatation (arrows), (courtesy of Dr. Faiss, Asklepios Fachklinikum Teupitz, Teupitz, Germany).
Fig. B8.4 Extracranial duplex, longitudinal plane. Left V2-VA diam­eter: 4.5 mm.
Initial Neurosonologic Findings (Day 42)
167
Degree of Neurosonologic Difculty: Low
Fig. B8.5 Extracranial duplex, longitudinal plane. Right V2-VA diam-
eter: 3.2 mm.
Fig. B8.7 Extracranial duplex, longitudinal plane. Doppler spectrum analysis of the right V2-VA with mildly increased pulsatility (flow velocity: 72/14 cm/s).
Fig. B8.6 Extracranial duplex, longitudinal plane. Doppler spectrum analysis of the left V2-VA with increased pulsatility (flow velocity: 46/ 11 cm/s). Note the mild retrograde flow component indicating rel­evant distal obstruction.
Fig. B8.8 TCCS (transforaminal approach). Turbulent and increased flow in the left V4-VA (flow velocity: 175/79 cm/s).
Fig. B8.9 TCCS (transforaminal approach). Turbulent and increased flow in the right V4-VA (flow velocity: 169/70 cm/s).
Fig. B8.10 TCCS (transforaminal approach). Normal flow in the BA.
Case 8 Bilateral Intracranial V4 Vertebral Artery Stenosis
168
Degree of Neurosonologic Difculty: Low
Fig. B8.11 CTA, coronal MIP: 4 weeks after thrombolysis and left-
sided balloon dilatation: Persisting bilateral intracranial VA stenosis with massive local calcification hindering graduation of stenoses (arrowheads). Note that there is a signal loss in the right distal V4-VA which is caused by an elongated vessel course and not by a distal vessel occlusion.

Neuroradiologic Findings

MRIcouldnotbeperformedbecausethepatientexperi­enced severe claustrophobia. Cerebral CT did not show any new ischemic lesion. CTA confirmed the bilateral intra­cranial VA stenoses with severe calcification in this area (Fig. B8.11).

Clinical Course (2)

During the next few days the patient experienced further recurrent episodes of vertigo and nausea which were closely related to episodes of low blood pressure. Clopi­dogrel was added as a second antiplatelet agent and at­tempts were made to keep the blood pressure within the upper normal range. Interventional treatment with stent placement was discussed but refused by the patient. Dur­ing 3 years of follow-up, no new ischemic event occurred and the neurosonologic findings remained unchanged.

Final Diagnosis

Successful intraarterial thrombolysis in distal BA occlu­sion, probably caused by artery-to-artery embolism from bilateral calcified intracranial VA stenoses. Suspected ad­ditional hemodynamic transient ischemic attacks (TIAs) originating from the vertebrobasilar circulation.

Discussion

Clinical Aspects
Here we report of a 56-year-old man with bilateral intra­cranial VA stenoses. An artery-to-artery embolism origi­nated from one of these stenoses and subsequently led to a distal BA occlusion. Intraarterial thrombolysis was suc­cessfully performed and only a small right-sided cerebellar infarct within the SCA territory remained. The case repre­sents a special pathologic constellation within the verte­brobasilar territory because of the bilaterally affected V4­VA segments.
According to reports of several stroke databases, isch­emic events of the posterior circulation account for ap­proximately 20 % of strokes (Bogousslavsky et al. 1988, Moulin et al. 1997, Vemmos et al. 2000). The New England Medical Center Posterior Circulation Registry is the largest database comprising prospectively collected data of 407 patients (Caplan et al. 2004). Of these, 59 % had a stroke, 24 % TIA followed by stroke and 16 % sustained a TIA with subsequent stroke. Ischemic strokes of the posterior cir­culation was caused by embolic events in 40 % of cases when considering the single most likely mechanism. Of these, 60 % were thought to be of cardioembolic origin. Artery-to-artery embolic events originating from the pos­terior circulation accounted for 35 % and a mixed cause in the remaining 5 % of cases. Large artery occlusive lesions causing stroke (32 %), vessel branch occlusion (14 %), mi­graine (3 %) and others (10 %) were the next relevant causes (Caplan et al. 2004).
Stenoses of the posterior circulation are predominantly found at the VA origin followed by the BA and intracranial VA. Within the intracranial VA they are most frequently found in the distal segments, near the origin of the poste­rior inferior cerebellar artery (PICA). Bilateral stenoses, as in our case, are not rare (Bogousslavsky et al. 1988, Caplan 1983, Muller-Kuppers et al. 1997). The New England Med­ical Center Posterior Circulation Registry reported clinical and radiological findings of 42 patients (9.8 %) with bilat­eral intracranial VA involvement. Of these, 18 had bilateral stenosis, eight had bilateral occlusion, and 16 had unilat­eral occlusion and contralateral stenosis. Only six patients (14%) had isolated bilateral intracranial VA pathology. The others presented in addition occlusive vascular lesions in the BA (69 %), the extracranial VA (43 %), and also in the ICA (26 %). Most of the stenoses were of atherothrombotic origin (Shin et al. 1999).
In cases of chronic and slowly progressing occlusive processes, patients with distal VA stenoses develop differ­ent collateral pathways. Collateralization may occur from the anterior circulation via the posterior communicating artery (PCoA) or the posterior circulation via the cerebellar arteries, anterior spinal artery, and the leptomeningeal arteries. However, often this is not sufcient, which may lead to impaired perfusion in the dependent brain terri­tories. Subsequently, patients present with recurrent ste-
Discussion
169
reotyped TIAs. Vertigo, dysarthria, ataxia, and double vi­sion are the most frequent symptoms which may be aggravated by orthostasis or antihypertensive therapy (Caplan 1996). Shin and co-workers (1999) found 81 % of patients in the group having TIAs had bilateral VA pathol­ogy; 38% of the TIAs were isolated events, and the remain­deroccurredbeforeoraftermanifestationofstroke.In most TIAs a hemodynamic cause was suspected (Shin et al. 1999). As in our case, transient vertigo and ataxia were the most frequently found clinical symptoms. The main components of the vestibulocerebellar system, located in the cerebellum and brain stem, derive their blood supply from the distal VA via penetrating branches and the PICA andarequicklyaffectedbyareducedorthogradeperfu­sion.
If a completed stroke occurs, the infarctpattern depends on the site of the vascular pathology. Medullary infarctions or infarcts of the PICA territory are observed if the stenotic process is located proximal to, or directly at the origin of the PICA. Ischemia within the BA, SCA, and posterior ce­rebral artery (PCA) territory occur more often in stenotic processes distal to the PICA branch. Artery-to-artery em­bolic events from atheromatous plaques located in the intracranial VA may also result in distal patterns of infarc­tion. In our patient, a VA-derived thrombus caused a distal BA occlusion with clinically fluctuating signs of a top-of­the-basilar-syndrome(Caplan 1980, Mehler 1989). In cases of persisting occlusion this may lead to ischemic infarctions in upper pons, midbrain, cerebellum within the SCA territory, thalamus, and the PCA territory. How­ever, the extent may vary, as in our patient who only had a partial SCA infarction. From this we can assume that although the occlusion began at the mid-basilar level, it must have extended to the head of the BA. We can also conclude that our patientsclinicalsymptomswereindi­cative of distal BA involvement, as they were mainly com­prised of a mesencephalic dysfunction (transient third nerve palsy and fluctuation in consciousness). Because of the fluctuating symptoms, lack of ischemic signs on cere­bral CT, and verification of the BA occlusion by DSA, an intracranial thrombolysis was performed which led to complete recanalization 6 hours after the onset of his symptoms. Furthermore, balloon dilatation of the left high-grade VA stenosis was performed.
In general, the therapeutic options in thromboembolic occlusionsoftheBAaresimilartothoseintheanterior circulation. However, only case series addressing treat­ment of acute BA occlusion have so far been published; there are no randomized trials. Based on the results of the NINDS trial (The NINDS rt-PA Stroke Study Group 1995) some data exist about the intravenous application of thrombolytic substances in patients with vertebrobasilar occlusion within a 3 hour margin (Grond et al. 1998) within the first 7 hours (Montavont et al. 2004) and even up to 12 hours for patients with sudden disturbance of conscious­ness and tetraparesis and up to 48 hours for patients with gradually increasing brain stem symptoms (Lindsberg et al
2004). In this larger series including 43 patients with a BA occlusion receiving systemic rt-PA thrombolysis, 52 % demonstrated a BA recanalization. The mortality after 3 months was 40 %, and 22 % of patients achieved a good clinical outcome, being independent in all functions of daily life (Lindsberg et al. 2004). Improved recanalization rates and clinical outcomes were also reported for intra­arterial thrombolysis when compared with medical ther­apy with an antiplatelet agent. Intraarterial thrombolysis is to date the most accepted therapy in BA occlusion. A recent metaanalysis compared the results of intravenous and intraarterial thrombolysis within the posterior circu­lation. It demonstrated that recanalization rates were sig­nificantly better if intraarterial thrombolysis was used instead of intravenous thrombolysis (65 % vs. 53 %). How­ever, survival rates and clinical outcome did not differ significantly in the two groups (45 % vs. 50 %), but both groups had a similar proportion of good clinical outcome (24 % vs. 22 %) (Lindsberg and Mattle 2006). Independently of the applied treatment strategy, the proportion of pa­tients with a good clinical outcome was higher if recanal­ization occurred (38 % vs. 2 %). Contrary to the anterior circulation, no clear time window for thrombolysis in the posterior circulation has been established. In patients with a stuttering course and no early infarct signs, the time window for intraarterial and systemic thrombolysis may be extended at least to up to 48 hours after onset of symptoms (Lindsberg and Mattle 2006).
In addition to the above-mentioned treatment regi­mens, a new combination of therapies, bridging ther­apy,has been proposed for the posterior circulation. Eck­ert and coworkers demonstrated that the combination of intraarterial rt-PA, intravenous abciximab, and, if applica­ble, a balloon dilatation or stent, placement in 47 patients, led to similar recanalization rates (72 % vs. 68 %), a better clinical outcome (34 % vs. 17 %) and a significant lower mortality (38 % vs. 68 %) than with intravenous rt-PA alone (Eckertetal.2005).
In our patient balloon dilatation was performed in the left intracranial VA. A restenosis of the dilated vessel oc­curred. Restenosis has been reported in approximately one-third of cases after intracranial stenting (Jiang et al. 2007, SSYLVIA Study Investigators 2004). Stenting seems nottobesuperiortoballoondilatationwithrespectto restenosis rates, but stroke rates at follow-up might be lower after stenting procedures (Eberhardt et al. 2006) (for further information on intracranial stenting, see also Case 5, p.149).
Angiologic and Anatomic Aspects
In our case, the transcranial color-coded sonography (TCCS) assessment of both intracranial V4-VA stenoses was uncomplicated. The cut-off for a 100 % confident de­tection of a 50 % stenosis is 120 cm/s (Baumgartner et al.
1999). Both VAs in our patient revealed systolic flow ve­locities of around 170–180cm/s, well above these cut-off
Degree of Neurosonologic Difculty: Low
Case 8 Bilateral Intracranial V4 Vertebral Artery Stenosis
170
values. There are no published data for a more detailed grading. In ultrasound examination, a flow profile analysis of pre- and poststenotic vessel segments can give valuable additional information. The extracranial VA profiles in our patient revealed a left-pronounced increased pulsatility, ontheleftsidewithasmallretrogradeflowcomponent. The BA itself did not show an obvious poststenotic flow pattern. Taking this information into account, a stenosis of beginning hemodynamic relevance, approximately of 80 % withintheleftV4-VAsegmentandof70%intherightV4­VA segment, can be assumed. Ultrasound assessment of the intracranial VA segment may be limited in uncooper-
Degree of Neurosonologic Difculty: Low
ative patients or those with a large neck circumference. Furthermore, V4-VA segment elongations, frequently found in the elderly might hinder an unequivocal vessel identification and lead to confusion between VA and, for example, a prominent PICA. In contrast with the extracra­nial ICA insonation, calcified plaques seem not to hinder flow signal detection. This is probably due to the lower insonation frequencies used for transforaminal insonation and also to a lesser extent of VA of calcification. If VA evaluation is difcult, in the acute posterior stroke setting it is important to avoid delays and proceed to the next step of neuroradiologic examination, for example, a CTA or MRA.
However, analysis of the intracranial VA and the transi­tional segment between V3 and V4 may also prove difcult with both techniques. As seen in our patient, a distinct and long circumferential calcification can hinder CTA to assess a V4-VA stenosis. In such cases, the detailed analysis of the axial source images or a combined approach with MRA can be helpful (Hirai et al. 2002). Analysis of the time-of-flight (TOF)MRAtechniqueincomparisonwithDSAbytwo readers has demonstrated a lower sensitivity and specific­ity in detection of intracranialVA stenoses (84 and 93 %; 74 and82%)comparedwithextracranialocclusiveVApro­cesses (92 and 96 %; 100 and 90 %). TOF MRA accurately diagnosed only 43 % of intracranial and 75 % of extracranial VA stenosis (Bhadelia et al. 2001). Because of the increas­ing availability of fast gradient MR systems, the TOF MRA is gradually being substituted by contrast-enhanced MRA techniques which display better image contrast, require less time, and are therefore less susceptible to movement artifacts (Ersoy et al. 2003). Compared with the analysis of the carotid arteries, contrast-enhanced MRA, however, is less sensitive and specific in detecting steno-occlusive processes of the vertebrobasilar circulation (Yang et al.
2005). In equivocal or conflicting situations catheter an­giography may be required (for further information on assessment of intracranial stenoses, see also Case 5, p. 149).
Case 9
Moyamoya Disease with Bilateral Carotid-T Stenosis
171

Clinical Presentation

A 34-year-old Caucasian woman presented after three separate episodes of transient left-sided brachiofacial hemiparesis within the last 4 weeks, each lasting a few minutes. Since the birth of her first child 4 years previ­ously, she had suffered from a pregnancy-induced hyper­tension. No further vascular risk factors were present. Initially she was admitted to a district general hospital. Transient ischemic attacks (TIAs) were suspected, and a cranial magnetic resonance (MR) scan and an MR angio­gram were performed revealing bilateral middle cerebral artery (MCA) stenosis more pronounced on the right side. The patient was started on antiplatelet treatment with aspirin and dipyridamole and was referred to our depart­ment for further evaluation.

Initial Neuroradiologic Findings

The externally performed MRI did not show ischemic brain lesions (not shown). Intracranial time-of-flight (TOF) MRA, however, was suspicious of bilateral proximal MCA and anterior cerebral artery (ACA) stenoses with a right-sided accentuation (Fig. B9.1).

Initial Neurosonologic Findings (Day 1)

Extracranial Duplex Sonography
B-mode and color-mode imaging revealed no atheroscle­rotic vascular changes. Doppler spectrum analysis showed normal and symmetric flow signals. Assessment of the vertebral arteries (VAs) was also normal.
Transcranial Duplex Sonography
A mildly elevated flow velocity was seen in the right distal internal carotid artery (ICA) reaching 160 cm/s. Both M1­MCA segments were markedly affected reaching a peak systolic flow of 380 cm/s on the right side and 210cm/s on the left side. The right M2-MCA segments presented a poststenotic flow pattern. Flow in the right A1-ACA seg­ment demonstrated normal velocities but with a clearly reduced pulsatility, probably indicating an additional col­lateral flow toward the MCA territory. The left A1-ACA segment presented elevated flow velocities reaching 175 cm/s peak systolic flow without turbulence, corre­sponding to either a low-grade ACA stenosis or collateral flow. Normal flow velocities were detected in both poste­rior cerebral arteries (PCAs) (Figs. B9.2–B9.8).

Suspected Diagnosis

Recurrent left-sided TIAs in bilateral high-grade proximal MCA and ACA stenoses of unknown origin.

Questions to Answer by Ultrasound Techniques

Was there any evidence of pathologic vascular changes in the cervical vessels?
What was the grading of the intracranial stenoses?
Were there any other intracranial stenotic processes or
collateral blood flow?
Conclusion
Bilateral carotid-T pathology with right high-grade M1­MCA stenosis and moderate M1-MCA stenosis on the left side. Moderate stenosis of the right terminal ICA. Indirect signs of partial leptomeningeal collateralization via both A1-ACA segments and possible additional low-grade A1­ACA stenosis.

Conventional Angiography (Day 2)

Selective right ICA contrast filling demonstrated a moder­ate stenosis of the terminal ICA continuing into a long segmental high-grade M1-MCA stenosis. Furthermore, a network of small capillary collateral vessels was visible in the region of the distal ICA and proximal MCA. The distal branches of the right MCA showed regular contrast. The proximal A1-ACA segment demonstrated moderate steno­sis. Selective left ICA filling yielded a mild caliber reduction from the distal ICA to the M1-MCA segment and to a lesser
Case 9 Moyamoya Disease with Bilateral Carotid-T Stenosis
172
Degree of Neurosonologic Difculty: Low
Fig. B9.1 Intracranial 3D TOF MRA, coronal MIP. Bilateral stenosis of
the MCA and ACA at their respective origins with a right-sided accentuation (arrows).
Fig. B9.3 TCCS (transtemporal approach), right-sided insonation, midbrain plane. Distinct flow increase in the right M1-MCA (flow velocity: 379/220 cm/s).
Fig. B9.2 TCCS (transtemporal approach), right-sided insonation, upper pontine plane. Moderately increased flow in the right C2­ICA (flow velocity: 160/90 cm/s).
Fig. B9.4 TCCS (transtemporal approach), right-sided insonation, midbrain plane. Poststenotic flow pattern in the right M2-MCA.
Fig. B9.5 TCCS (transtemporal approach), right-sided insonation, midbrain plane. The right A1-ACA shows a reduced pulsatility due to an increased diastolic flow (flow velocity: 95/63 cm/s).
Fig. B9.6 TCCS (transtemporal approach), left-sided insonation, midbrain plane. Raised flow velocity in the left M1-MCA (peak systolic flow velocity: 212 cm/s).

Discussion

173
Degree of Neurosonologic Difculty: Low
Fig. B9.7 TCCS (transtemporal approach), left-sided insonation,
midbrain plane. Normal flow in a left M2-MCA.
extent in the A1-ACA segment. Again, a network of small vessels indicating collateral pathways was seen. The pos­terior circulation was normal (Fig. B9.9).

Clinical Course

The finding of bilateral stenotic carotid-T processes includ­ing both MCAs, ACAs, and in part the distal ICAs as well as small-caliber collateral pathways were suggestive of the diagnosis of a yet indistinct moyamoya disease.The absent vascular risk factors and the normal status of extracranial vessels further supported this diagnosis. As the patient complained of a daily, dull headache, her medication was changed from dipyridamole plus aspirin to aspirin alone. The headaches disappeared and no further ischemic events occurred. The patient was referred to the depart­ment of neurosurgery to evaluate the possibility of an extra-intracranial vascular bypass. Thereafter she was lost to follow-up.
Fig. B9.8 TCCS (transtemporal approach), left-sided insonation, midbrain plane. Increased but not turbulent flow in the left A1­ACA (peak systolic flow velocity: 175 cm/s).
Fig. B9.9 DSA, superimposed right and left selective ICA injection, posteroanterior view. Right-sided moderate terminal ICA stenosis continuing into a proximal high-grade M1-MCA and moderate A1­ACA stenosis. Note the poststenotic dilatation of the distal M1-MCA and the M2-MCA branches. Similar but milder stenoses are seen on the left side. Bilateral networks of small vessels within the region of the distal ICA and proximal MCA.

Final Diagnosis

Recurrent TIAs, presumably of hemodynamic origin in the right MCA territory caused by bilateral right-pronounced high-grade carotid-T stenoses on the basis of presumed moyamoya disease.
Discussion
Clinical Aspects
Here we discuss a 34-year-old Caucasian woman who presented with bilateral intracranial stenotic processes within the distal ICA as well as the proximal MCA and ACA. Apart from mild hypertension, no classic vascular risk factors were present. Correspondingly, no atheroscle-
rotic lesions were found in the extracranial arteries. Age and location of the stenotic processes were suggestive of rare causes of ischemic stroke. Based on the angiographic finding of bilateral intracranial ICA stenoses, additional involvement of circle of Willis (CW) arteries and the typ­ical formation of small collateral vessels, moyamoya dis­ease was considered.
Moyamoya disease was first described by Takeuchi and Shimizu in 1957 and is predominantly found in Japan. The annual incidence is 0.35% per 100 000 inhabitants (Fukui and Kawano 1996). Precise epidemiological data for Eu­rope and North America are not available. Until 1996 the total number of reported moyamoya cases was 239 in North America (Chiu et al. 1998). Within the Asian and, in particular, within the Japanese population the incidence
Case 9 Moyamoya Disease with Bilateral Carotid-T Stenosis
174
is tenfold higher than in Europe or in North America (Yo­nekawa 1997). Generally young women seem to be more frequently affected than men. A clustering within families is seen in up to 10% of affected patients. The disease may manifest at any age. However, there are peaks in presen­tation in those aged < 10 years and between 30 and 40 years.
Inthecourseofthedisease,thereisaslow,spontaneous, and progressive development of stenoses in the CW. Gen­erally the affected vessels are the ICA, MCA, and ACA. Concomitantly, a network of intracerebral and extracere­bral collaterals can be found. The collaterals in the region
Degree of Neurosonologic Difculty: Low
of the CW appear in DSA imaging as fog or smokelike structures, which give the disease its name (moyamoya is Japanese for smoke or fog).
Macroanatomically, a stenosed or occluded vessel lu­men is found in the affected arteries caused by an intimal thickening of the vessel. On histologic examination, mural thrombi are frequently found with the stenosed regions, which are thought to be responsible for the eccentric reductionofthevessellumen(Hosodaetal.1997).How­ever, until now the exact cause of the disease remains unclear despite continuing effort. The predominance among the Asian population and the reported inheritance in some families argue in favour of a multifactorial, heredi­tary etiology.
Clinically moyamoya frequently manifests itself by re­occurring TIAs. Atypical reported symptoms are chronic headaches and focal or generalized epileptic seizures. In Asia an increased incidence of intracranial bleeding has been reported as a further first manifestation of moya­moya in the adult population, whereas TIAs prevail in the juvenile form. In Europe this difference between age groups does not seem to exist. In our presented patient, age, gender, and the clinical presentation with supposedly hemodynamic TIAs corresponded well with the suspected diagnosis of moyamoya disease.
As moyamoya is a rare disease of unknown etiology, a number of focal and systemic diseases have tobe excluded, including chronic meningitis or atherosclerotic vascular disease. In some middle-aged patients, the latter may lead to a picture similar tothe moyamoyafindings. This group of patients, however, demonstrates additional macroangio­pathic changes in the extracranial brain-supplying arteries (Hinshaw et al. 1976). As the foglike collateral network can also be foundin these patients, it hasto be interpreted asan unspecific compensatory reaction to a slowly progressing stenotic process. Finally, radiation may also cause moya­moya-like vascular changes as a side effect.
To date, there is no medical treatment to stop or delay the disease progression although antiplatelet agents and anticoagulation are frequently used. The only effective treatment is surgical revascularization of the malperfused brain regions. Several surgical techniques are used. The most common is direct revascularization with an extrac­ranial–intracranial (EC–IC) bypass between the superficial temporal artery and a cortical MCA branch (STA–MCA
bypass) (for further information on EC–IC bypass, see Case 25, p.297). An indirect form of revascularization is the placement of the STA on the dura, muscle, or pia (encephaloduroarteriosynangiosis, encephalomyosynan­giosis, or pial synangiosis). All approaches improve the perfusion of the poststenotic brain regions and are able to minimize or even to stop clinical events. The indirect approach is more frequently applied in children and the direct approach in adults.
Angiologic and Anatomic Aspects
Diagnosis of moyamoya is based on morphological vascu­lar aspects depicted by the angiologic imaging methods. An additional diagnostic criterion is the bilateral occur­rence of stenotic processes. Bilateral involvement confirms the suspected diagnosis; in unilateral cases, a possible moyamoya has to be postulated.
First-line techniques are the noninvasive CT and CTA as well as MRI and MRA. In suspected cases, these are fol­lowed by DSA. Conventional CT findings are variable and often unspecific. They range from mild brain atrophy with frontal accentuation to multiple hypodense ischemic areas within the regions of the vascular border zones. Although rare, even a subarachnoid hemorrhage can occur. If con­trast CT is performed, the lenticulostriatal collateral net­work might be seen. MRI is more sensitive in identifying ischemic lesions if diffusion and perfusion sequences are applied. These techniques are helpful in representing the regionsatriskaswellasconfirmingthepostoperative perfusion improvements. The described typical collateral vessels can sometimes be seen in the form of flow artifacts (flow voidphenomenon). On post contrast sequences, a leptomeningeal enhancement (ivy sign)mightbeob­served which is caused by multiple fine leptomeningeal anastomoses (Ohta et al. 1995). MRA is able to detect collateral vessels at the basal skull level in cases with advanced disease. The overall diagnostic sensitivity of MRAincomparisontoDSAis73%andthespecificityis 100 % (Yamada et al. 1995). There have been no systematic analyses of CTA results.
For final confirmation of moyamoya, DSA is required, which should at the latest be performed before planning an intervention. The technique shows stenoses or occlu­sions of the distal intracranial ICA and the proximal MCA and/or ACA in addition to the collateral vascular network adjacent to the stenotic process (see also chapter 6, Fig. 7C). An angiographically determined definition of six stages of the disease has been reported by Suzuki and Takaku (1969). The chronologic stages of the disease are: I. Narrowing of the carotid siphon. II. Initiation. III. Intensification. IV. Minimization. V. Reduction. VI. Disappearance of moyamoya vessels.
Discussion
175
Our patient’s findings correspond with stage II (early dis- ease)demonstrating carotid-T stenoses, the fine collat­eral network, and a poststenotic dilatation of the distal intracranial arteries.
Doppler and duplex ultrasound may also contribute important diagnostic information in patients with moya­moya disease. TCCS permits identification and quantifica­tion of intracranial stenosis. More importantly, ultrasound allows the evaluation of collateral pathways. For example, raised flow velocities in the P1- and P2-PCA segments seldom affected in moyamoya disease are indirect indica­tors of leptomeningeal collateralization in cases with af­fected proximal MCA. As the A1-ACA segments can be affected by the disease, it may be impossible, as it was in our case, to sonographically differentiate between com­pensatory collateral flow and raised flow velocity caused by a stenosis. The same is true for the criterion of turbulent flow, as turbulence is not pathognomonic for a stenosis and can frequently occur in regions with tortuous vessels even without the presence of a stenosis. Other indirect
sonographic signs of collateral involvement are a reduced pulsatility as a result of a peripheral vascular dilatation.
A number of recent ultrasound studies have systemati­cally analyzed flow patterns in moyamoya disease. These studies have found reduced flow velocities and raised pulsatility indices in the extracranial CCA and ICA which frequently revealed a narrowed lumen. Intracranially, the aforementioned multilocular stenoses can be detected. Furthermore, low flow velocities with low pulsatility (due to low resistance) can be detected within the distal, poststenotic basal cerebral arteries, which in the case of a severe flow alteration, might appear occluded on catheter angiography (Muttaqin et al. 1993, Ruan et al. 2006). Fi­nally, the small fine moyamoya collaterals can be depicted as scattered colored dots in about half of cases, comprising low flow velocities and reduced pulsatility indices on Doppler spectrum analysis (Ruan et al. 2006). In our pre­sumed case of early-stage moyamoya disease, these sig­nals were not found.
Degree of Neurosonologic Difculty: Low