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Case 23 Takayasu Arteritis with Subclavian Artery and Vertebral Artery Stenoses
286
1994, Grosset et al. 1992). In our patient, however, even this type of collateral flow was not possible because of bilaterallackoffunctionalPCoAs, a variation of the circle of Willis which is present in about 16 % of the population (Hoksbergen et al. 2000b). The coexistence of bilateral nonfunctional PCoAs and bilaterally impaired VA flow ex­plains the distinctly poststenotic altered flow pattern in both PCAs, which hardly demonstrated any arterial pulsa-
Degree of Neurosonologic Difculty: High
tility. It also explains why both PCAs appeared extremely small on DSA, which could havebeen interpreted as part of the arteritis even though involvement of the intracranial arteries is extremelyrare in Takayasu arteritis (Nasu1975). Aftersuccessfulbypasssurgery,bothPCAflowprofiles normalized, arguing against the hypothesis of an addi­tional vasculitic PCA involvement.
Case 24
Dissection of the Extracranial Internal Carotid Artery and Contralateral M1 Middle Cerebral Artery Stenosis

Clinical Presentation

Clinical Course (1)

A 34-year-old woman presented with a 1-year history of severe headaches that were thought to be caused by re­peated hypertensive episodes. She also reported a single episode of left-sided facialpain and ipsilateral conjunctival injection lasting for several hours approximately 1 year ago. After the initiation of antihypertensive treatment the headaches subsided. However, ambulatory examination of the optic fundi revealed retinal vessel narrowing. This finding prompted an ultrasound examination of the brain-supplying arteries. Transcranial Doppler (TCD) re­vealed a left M1 middle cerebral artery (MCA) stenosis. In addition to having hypertension, the patient was a smoker and used an oral contraceptive. An ambulatory cerebral computed tomography (CT) scan had been unremarkable. She was now admitted to our department for elective catheter angiography to search for extended intracranial vascular pathology.

Initial Neuroradiologic Findings

Two weeks later, the patient was readmitted to our hospi­tal for further evaluation. On admission she reported a right-sided neck pain during the catheter angiography that had been performed 2 weeks ago and a sore throat on the day following it. The neurologic examination was normal; in particular, she did not have Horner syndrome.

MRI and MR Angiography (10:00 Hours)

No parenchymal lesions were seen on magnetic resonance imaging (MRI). On conventional T2-weighted axial MRI images, a distinctly reduced flow void could be seen in the distal ICA on axial and coronal images. TOF MRA of the circle of Willis (CW) demonstrated the known left high­grade M1-MCA stenosis. A reduced signal was observed within the right terminal ICA. Cervical MRI and MRA of the extracranial vessels were not performed (Figs.B24.5–
B24.7).
287
Digital subtraction angiography (DSA) demonstrated mild bilateral extracranial internal carotid artery (ICA) elonga­tions and wide carotid sinuses, but there was no evidence of stenosis or atherosclerosis. Intracranially a left long­segmented high-grade stenosis of the proximal M1-MCA segment could be confirmed. Distal to the stenosis, the residual M1 segment was mildly dilated. Also, a delayed contrast filling of the distal MCA segments in relation to the distal ACA segments was seen indicating a high-grade stenosis of hemodynamic relevance. There were no signs of vasculitis (Figs. B24.1–B24.4).

Suspected Diagnosis

Asymptomatic left high-grade M1-MCA stenosis. In the absence of atherosclerotic vessel changes, and the pres­ence of a history of left-sided facial pain with associated conjunctival injection and headache 1 year previously, an MCA dissection was suspected.

Questions to Answer by Ultrasound Techniques

To confirm the left-sided MCA stenosis.
To search for evidence of other vascular pathology, e. g.,
dissection of the right ICA.

Neurosonologic Findings (12:00 Hours)

Extracranial Duplex Sonography
Therewerenoatheroscleroticvascularchanges.Theright ICA revealed a long-segmented lumen reduction that started 2 cm above the carotid bifurcation and continued over the whole visible distal vessel segment. There were no typical signs of a dissection. Flow velocity in the right ICA reached a systolic maximum of 200 cm/s. The right common carotid artery (CCA) showed a high-resistance flow signal with a reduced diastolic flow component. The left ICA, both external carotid arteries (ECAs), and the vertebral arteries (VAs) presented normal flow signals (not shown).
Case 24 Dissection of the Extracranial Internal Carotid Arter y and Contralateral M1 Middle Cerebral Arter y Stenosis
288
Transcranial Duplex Sonography
Within the left M1-MCA, transcranial color-coded sonog­raphy (TCCS) detected a turbulent stenotic flow (flow ve­locity: 383/267 cm/s). A poststenotic flow pattern was ob­served in the left M2-MCA branches. The flow signal of the right M1-MCA segment appeared normal. The right A1­ACA segment showed reversed flow while the left-sided A1-ACA segment demonstrated increased flow velocities without turbulence (flow velocity: 225/140 cm/s). Assess­ment of the posterior cerebral arteries, VAs, the basilar artery (BA) as well as the ophthalmic arteries (OAs) re­vealed overall normal orthograde flow signals without
Degree of Neurosonologic Difculty: High
signs of leptomeningeal or ophthalmic collateral support. TherewasapositiveoscillationeffectintherightM1-MCA segment with mild submandibular oscillation of the left ICAandthedominantleftVAattheatlasloop.Thisindi­cated collateral flow through the anterior communicating artery (ACoA) and right posterior communicating artery (PCoA) (Figs. B24.8–B24.14).
Conclusion
Hemodynamically relevant left high-grade M1-MCA stenosis. High-grade stenosis of the right extracranial ICA of hemodynamic relevance, suspicious of dissection, in­duced by the diagnostic DSA 2weeks previously. Collateral flow to the right MCA and ACA via the ACoA as well as the right PCoA.
was assumed to be most likely. After 6 months the patient was re-examined to evaluate the requirement for long­term secondary stroke prevention.

Questions to Answer by Ultrasound Techniques

Was there any regression of the right extracranial ICA stenosis under continuous anticoagulation with phen­procoumon?
Were there changes in the left M1-MCA stenosis?

Follow-up Neurosonologic Findings (6 Months)

Extracranial Duplex Sonography
No flow signal was observed in the right proximal ICA. The ipsilateral CCA revealed an increased pulsatility. The right ECA was normal revealing no indirect signs of collateral support (Figs. B24.18B24.21). The left-sided carotid ar­teries and the VAs were unremarkable.
Transcranial Duplex Sonography
Intracranially the flow pattern was unchanged in relation to the examination 6 months previously.

Conventional Angiography (16:00 Hours)

DSA performed on the same day demonstrated a conical lumen reduction of the right ICA directly above the carotid bifurcation with a filiform stenosis up to the base of the skull which was suggestive of ICA dissection. Collateraliza­tionviatheACoAwasdirectedtowardtherightMCAand ACA territory via the left ICA. The right PCoA flowed ante­riorly toward the MCA. There was no evidence of leptome­ningeal or ophthalmic collaterals. The known high-grade M1-MCA stenosis remained unchanged (Figs. B24.15– B24.17). In addition, renal angiography was performed, which excluded signs of fibromuscular dysplasia.

Clinical Course (2)

The dissection of the right ICA was considered to be of iatrogenic origin caused by the catheter during the initial DSA. Intravenous heparin treatment was started, aiming for a twofold rise in partial thromboplastin time. The pa­tient was then switched to oral anticoagulation with phen­procoumon for 6 months. The etiology of the left M1-MCA stenosis remained unclear. After exclusion of all other differential diagnoses, particularly vasculitis, a dissection
Conclusion
Unchanged high-grade stenosis of the left MCA. Secondary occlusion of the right extracranial proximal ICA with un­changed collateral blood flow via the ACoA and ipsilateral PCoA.
Conventional Angiography
A third angiography confirmed the occlusion of the right ICA with a smooth margin (Fig. B24.22).
Figure B24.23 shows a schematicdrawing of the extra- and intracranial brain-supplying arteries in this patient.

Clinical Course (3)

Secondary stroke prevention was changed to antiplatelet therapy. During 4 years of follow-up no cerebral ischemia occurred and no changes in vascular pathology were ob­served.
Clinical Course (3)
289
Degree of Neurosonologic Difculty: High
Fig. B24.1 DSA, left ICA injection, left anterior oblique (LAO) pro-
jection. Mild elongation of the ICA and wide carotid sinus without evidence of atherosclerosis.
Fig. B24.3 DSA, left ICA injection, posteroanterior view. Long-seg­mented high-grade stenosis of the proximal left M1-MCA (arrow). Note the dilation of the MCA distal of the stenosis. Also note the delayed filling of the distal MCA segments in comparison to distal ACA segments.
Fig. B24.2 DSA, right ICA injection, right anterior oblique (RAO) projection. Identical mild elongation of the ICA and wide carotid sinus without evidence of atherosclerosis.
Fig. B24.4 DSA, left ICA injection, posteroanterior view. Magnified view of Figure B24.3 demonstrating a filiform MCA stenosis (arrows) and poststenotic vessel dilation.
Case 24 Dissection of the Extracranial Internal Carotid Arter y and Contralateral M1 Middle Cerebral Arter y Stenosis
290
Degree of Neurosonologic Difculty: High
Fig. B24.5 MRI T2-weighted image, axial plane. Regular findings
without evidence of parenchymal lesions. Note, that the prominent right PCoA is already visible (arrow).
Fig. B24.7 3D TOF MRA, axial MIP. Reduced signal in the left M1­MCA (single arrow), indicating high-grade stenosis. Note that the right-sided distinct PCoA is not visualized. Note also a reduced signal in the intracranial right ICA (arrows).
Fig. B24.6 MR T2-weighted image, axial plane. Attenuated flow void in the right ICA (arrow) indicating a significantly reduced blood flow.
Fig. B24.8 TCCS, transtemporal approach, midbrain plane. In­creased flow velocity in the left M1-MCA indicating high-grade stenosis (flow velocity: 383/267 cm/s).
Clinical Course (3)
291
Degree of Neurosonologic Difculty: High
Fig. B24.9 TCCS, transtemporal approach, midbrain plane. Normal
flow pattern in theright M1-MCA (flow velocity: 97/52cm/s) despite the proximal extracranial high-grade ICA stenosis. Note the limited quality of the right temporal bone window.
Fig. B24.11 TCCS, transtemporal approach, midbrain plane, left- sided insonation. Positive oscillation effect on the right M1-MCA
(arrows) caused by oscillation of the dominant left VA, indicating collateralization via the PCoA. Note also the prominent blue-coded right PCoA (arrow).
Fig. B24.10 TCCS, transtemporal approach, midbrain plane, left- sided insonation. Positive oscillation effect on the right M1-MCA
(arrows) caused by mild oscillation of the left extracranial ICA, indicating cross-flow via the ACoA.
Fig. B24.12 TCCS, transtemporal approach, midbrain plane, left­sided insonation. Increased flow velocity in the left A1-ACA without turbulence, suggesting collateralization of the contralateral anterior circulation via the ACoA but also for the ipsilateral MCA territory (flow velocity: 225/140 cm/s).
Fig. B24.13 TCCS, transtemporal approach, midbrain plane, right­sidedinsonation.TherightA1-ACApresentedwithreversedflow direction (flow velocity: 192/116 cm/s).
Fig. B24.14 TCCS, transtemporal approach, midbrain plane, left­sided insonation. Turbulent flow and increased flow velocity within the ACoA (functional stenosis) causedby intracranialcross-flow from the left ICA.
Case 24 Dissection of the Extracranial Internal Carotid Arter y and Contralateral M1 Middle Cerebral Arter y Stenosis
292
Degree of Neurosonologic Difculty: High
Fig. B24.15 DSA, right ICA injection, lateral view. Conical lumen
reduction of the right ICA directly above the carotid bifurcation with a long-segmented filiform stenosis up to the base of the skull (arrows).
Fig. B24.16 DSA, left ICA injection, posteroanterior view. Collateral blood flow into the right MCA and ACA via ACoA and retrograde right A1-ACA. Symmetric filling of both MCAs without delay between the right and left sides indicating well developed cross-flow (arrow­heads). Also note the known long-segmental left M1-MCA stenosis (arrow).
Fig. B24.17 DSA, left VA injection, posteroanterior view. Collateral blood flow via the prominent PCoA (arrow) solely into the right MCA.
Fig. B24.18 Extracranial duplex, longitudinal plane. Normal flow in the left CCA (flow velocity: 122/49 cm/s).
Clinical Course (3)
293
Degree of Neurosonologic Difculty: High
Fig. B24.19 Extracranial duplex, longitudinal plane. High-resistance
flow signal in the right CCA demonstrating increased pulsatility, i. e., a reduced diastolic flow component (flow velocity: 127/ 22 cm/s).
Fig. B24.21 Extracranial duplex, longitudinal plane. Absent flow signal in the right ICA.
Fig. B24.20 Extracranial duplex, longitudinal plane. Normal flow in the left ICA (flow velocity: 65/30 cm/s).
Fig. B24.22 Follow-up DSA, right ICA injection, lateral views. Initial DSA: Normalright ICA (A). Two weeks later: High-grade ICA stenosis due to dissection (B). Af ter 6 months: Complete ICA occlusion with a rounded margin resembling occlusion in atherosclerosis (C).
Fig. B24.23 Schematic drawing of the extra- and intracranial brain­supplying arteries of the patient in Case 24. Right proximal ICA occlusion (large circle). Left M1-MCA stenosis (small circle). Collat­eralization of the right MCA territory from the left ICA via ACoA and retrograde A1-ACA as well as from the PCA via the right PCoA. Collateralization of the left MCA territory via leptomeningeal collat­erals from the lef t ACA.
Case 24 Dissection of the Extracranial Internal Carotid Arter y and Contralateral M1 Middle Cerebral Arter y Stenosis
294
coincidence and the subsequently discovery of typical an-

Final Diagnosis

Asymptomatic high-grade left M1-MCA stenosis caused by dissection ofunknown etiology. Iatrogenicdissection ofthe right extracranialICA caused by catheter angiography with initial high-grade stenosis and secondary ICA occlusion.

Discussion

Clinical Aspects
Here we report of a 34-year-old woman with a suspected
Degree of Neurosonologic Difculty: High
left intracranial MCA dissection and an iatrogenic dissec­tion of the right ICA.
Dissections are an important cause of stroke, especially in young patients. Most dissections, however, occur within the extracranial brain-supplying arteries. In these cases, diagnosis is mainly made by MRI visualization of the intra­mural hematoma. Other supporting indicators are the typical angiographic morphology, missing atherosclerotic vessel wall changes, and the presence of an intima flap or a false lumen, in combination with a corresponding clinical picture (for further discussion on extracranial dissection, see Case 11, p.183).
Diagnosis of intracranial dissections is more difcult. Often it is based on an angiographically diagnosed intra­cranial stenosis in a young patient suffering from a stroke accompanied by pain. In cases of a concomitant intracra­nial aneurysm or recent subarachnoid haemorrhage (SAH) the diagnosis becomes even more likely. However, in the group of patients aged over 40 a reliable diagnosis be­comes more difcult as atherosclerosis might be seen as a confounding factor and as headaches might also occur in normal-type stroke. With regard to isolated MCA dissec­tions only 23 patients have been reported (Lin et al. 2005), of which 88% had cerebral infarction and 12 % had SAH. All the infarctions wereterritorial and none within the border zones, so that embolic events and not hemodynamic causes are thought to be the underlying mechanism (for further discussion on intracranial dissection, see also Case 21, p. 261.
In our case a MCA dissection was considered to be the most likely cause. In favor of this hypothesis were the reported left-sided facial pains and headaches, the young age of the patient, and the absence of atherosclerotic ves­sel wall changes. The angiographic finding of an irregular segmental long-segmental stenosis was also compatible with the hypothesis. However, no ischemia occurred and, unusual for dissection, the stenosis remained unchanged over the following years.
During catheter angiography for etiological clarification of the MCA stenosis our patient experienced an extracra­nial ICA dissection with initial high-grade ICA stenosis and subsequent ICA occlusion. Clinically this corresponded to neck pains which the patient had experienced during and shortly after thefirst angiography. Because of the temporal
giologic ICA alterations, an iatrogenic cause seemed ob­vious. Although rarely reported, the question was raised whether our patient had a particular predisposition to develop adissection during selective catheter angiography because of the already present intracranial spontaneous dissection. An inherited or acquired abnormality of the intimalormedialvessellayersoroftheelasticconnective tissue, as for instance in Marfan syndrome, Ehlers–Danlos syndrome, and pseudoxanthoma elasticum, could result in increased spontaneous vessel wall vulnerability (Schie­vink 2001) and possibly also an increased vulnerability, for example, to mechanical manipulations. Brandt and coworkers (1988) reported ultrastructural collagen alter­ations and alterations of the extracellular matrix in skin specimens of patients with extracranial dissections, which then may lead to generalized arteriopathy, associated in­tracranial pseudoaneurysms, an aortic dilatation, and/or hyper-distensibility of arterial walls (Guillon et al. 2000, Hausser et al. 2004). However, none of these conditions were found in our patient, and she had no suggestive family history. Therefore, the assumption of a particular predisposition to vessel wall injuries in our patient re­mains speculative.
Due to the recent advances in noninvasive vascular di­agnostics of the brain-supplying arteries, angiography has lost its importance. However, it has, without doubt, a place in special indications such as the diagnosis of vascular malformations, vasculitis, or in any case where endovas­cular treatment is a potential therapeutic option. But its use has always been open to criticism because of the potential side effects. Although the applied techniques are constantly being improved by using smaller catheters, hydrophilic guidewires, and digital imaging systems, an­giography-related neurologic complications still occur. Complication rates are usually reported asincidents occur­ring within 24 hours postintervention (so our case would not have been included).
A prospective analysis in 2899 angiographic interven­tions revealed a combined rate of transient and reversible neurologic deficits of 1.3%. In 14 of these patients (0.5 %), persisting neurologic deficits occurred (Willinsky et al.
2003). In an older reportincluding eight prospective stud­ies the general neurologic complication rate was 4.1 % and the rate of persisting neurologic deficits was 1 % (Hankey et al. 1990). Complication rates are influenced by patient as well as procedure-related factors. A significantly higher complication rate has been observed in patients aged 55 years or older (1.8% vs. 0.9 %) (Willinsky et al. 2003). Other authors,whohavereportednoneurologiccomplications in those < 50 years or those < 30 years of age, support this finding (Dion et al. 1987, Heiserman et al. 1994). Other factors are the angiography duration, the number of ves­sels catheterized, the experience of the investigator, and the studied vascular pathology. Thus, a four-vessel angiog­raphy is not a routine procedure and vessel intubation has to be justified on the basis of the very clinical question. If a
Discussion
295
patient with anterior circulation pathology had a dissec­tion during VA intubation, the neuroradiologist would be at risk of being sued for malpractice. Mani and Eisenberg (1978) reported an overall complication rate of 3.9 % in a teaching hospital, compared with 0.9 % in a non-teaching hospital. When patients with and without occlusive artery diseasewerecompared,thecomplicationratesinateach­ing hospital were 4.3 % and 1.2 %, and in a non-teaching hospital they were 2.6 % and 0.5 %, respectively (Mani et al.
1978). The above finding corresponds well with the fact that the rate of complications is higher instroke patients in general than in those with other vascular pathology. A metaanalysis that compared stroke patients and patients with intracranial malformations, aneurysms, or vaso­spasm found a complication rate of 35 % in the former and 0.8 % in the latter group (Cloft et al. 1999).
In addition to manifest neurologic deficits, angiography may also cause asymptomatic injuries to the brain. Bend­szus and coworkers (1999) analyzed 91 patients who underwent a total of 100 mostly diagnostic angiographies. MRI including diffusion-weighted images before and after angiography revealed 42 postinterventional new lesions in 23 patients, mostly of embolic appearance. Fortunately, none of these patients demonstrated aclinically detectable neurologic deficit. Patients with vascular risk factors and known vasculopathy were at higher risk of developing lesions than those without vascular pathology (44 % vs. 13%). The lesion size was small in the majority of cases but seven of them exceeded 10mm (Bendszus et al. 1999). This study illustrates that angiography-related embolic events are frequent but are not sufciently reflected by the reported clinical complication rates. Considering the distribution pattern of the observed cerebral lesions, a thromboembolic event originating from the catheter itself or from mechanically dislocated atherosclerotic plaque fragments seems to be the most likely mechanism.
Side effects related to the contrast agents used and, as in our case, a dissection of the studied vessel occur less frequently. A retrospective analysis of 2437 diagnostic angiographies and 675 neurointerventional procedures reported 12 dissections (0.4 %). Nine of these were in the VA, one in the CCA, and two in the ICA (Cloft et al. 2000). Seven of these patients reported symptoms during con­trast injection. In the remaining five the dissection oc­curred during catheter manipulation. Except for one pa­tient who developed aclinically silent territorialinfarction all the others had a benign clinical course.
Because of the symptom onset during angiography in our patient the diagnosis of a carotid dissection was be­yond doubt. Interestingly, the patient did not mention her symptoms at the time of investigationwhich was ambu­latory. It was therefore missed and only noted when she was readmitted for further diagnostics and ultrasound depicted the new vessel pathology. This clinical pattern indicates that a number of dissections, and also those of spontaneous nature, might occur silently, leaving a poten­tially high number of unreported cases.
Angiologic and Anatomic Aspects
The primary ultrasound analysis yielded a long-seg­mented ICA narrowing with local systolic flow velocities of up to 200 cm/s but no typical direct signs of dissection. Typically a more distally located conical-shaped stenosis or occlusion can be found. Even if the stenosis itself is not visible, a high-resistance flow signal might indicate the relevant distal flow obstruction. The latter constellation alone, however, is not sufcient to diagnose dissection, as distal stenosis caused by fibromuscular dysplasia (FMD) or a distal vessel kinking might also result in similar findings. If atherosclerotic vessel wall changes are completely ab­sent, a dissection, however, becomes more likely. When­ever the patient shows additional head or facial pain and/ or had Horner syndrome the presence of a dissection is practically evident.
On the contrary, normal ultrasound findings do not ex­clude a dissection as a distal vessel narrowing less than 70 to 80 % will not result in relevant proximal blood flow alterations and distal dissecting aneurysms might domi­nate the morphologic picture. However, in our experience, if patients are symptomatic, a distal hemodynamically relevant stenosis is a frequent finding. In patients without ischemia, extracranial ultrasound examination is normal in approximately 29 % of cases. In those with ischemia, normal ultrasound findings occur in 5 % only (Baumgart­ner et al. 2001). An analysis of purely hemodynamic ultra­sound criteriain patients withcerebral ischemia caused by a dissection found a sensitivity, specificity, and positive and negative predictive values of 96 %, 92 %, 94 %, and 97 %, respectively (Benninger et al. 2006). Hence, ultra­sound is especially useful as a screening tool in patients with stroke. Further neuroradiologic examination will be needed for confirmation of diagnosis in equivocal cases (for further discussion on ultrasound findings in extracra­nial ICA dissection, see also Case 11, p.183).
During oral anticoagulation, our patient developed a secondary ICA occlusion which, in contrast with the pa­tient in Case 11, did not result in an additional intracranial hemodynamic compromise (for further discussion on sec­ondaryvesselocclusion,seealsoCase11,p.183).DSA demonstrated the hemodynamic effect of the MCA steno­sisbyadelayedMCAvesselfillingwhencomparedwith the ACA contrast filling pattern. Similar to DSA, ultrasound is also able to reveal flow alterations induced by hemody­namically relevant stenoses. The ultrasound correlate of the delayed vessel filling is the presence of a poststenotic flow pattern which was observed in an M2 branch of our patient. Whenever a poststenotic flow pattern is detected, astenosisofatleast80%canbeassumed.However,de­tailed grading, such as in extracranial ICA stenosis, is cur­rently not possible (for further discussion on grading of intracranial stenoses, see Chapter 5, “Stenoses and Occlu- sions,p. 81).
Another interesting hemodynamic aspect was revealed by DSA. On selective VA filling, the PCoA on the side of the
Degree of Neurosonologic Difculty: High