S pontaneous dissection of the internal

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1 Pictorial Essay Dissections of the Internal Carotid Artery: Th ree- Dimensional Time-of-Flight M R Angiography and MR Imaging Features S pontaneous dissection of the internal carotid artery is now recognized as one of the most frequent causes of ischemic stroke in young patients; it accounts for as many as 20% of the ischemic strokes that occur in patients who are less than 45 years old I I 1. Approximately 80% of the strokes that are due to internal carotid artery dissection are preceded by warning signs 5-10 days before occurring [2]. Although the clinical signs might be nonspecific such as headache. the neurologic outcome can be grave, depending on the degree of cerebral ischemia. Three-dimensional time-of-flight (TOF) MR angiography and MR imaging are reported to be reliable. noninvasive methods of assessing internal carotid artery dissection [3-5]. Advantages include the availability of an infinite number of projections of the artery. the accessibility of images that allow direct visualization of intramural hematoma, and the ability to assess intracranial circulation and cerebral infarction. Technique MR evaluation of internal carotid artery dissection must include imaging of the head and neck. MR angiography and MR imaging were performed on a I.0-T system (Magnetom; Valerie Bousson1, Claude Levy, Laurent Brunereau, Hocine Ojouhri, J. M. Tubiana Siemens Medical Systems, Iselin, NJ) with an emitting-receiving quadrature head coil. MR angiograms were obtained in the coronal plane using a three-dimensional TOF technique. Acquisition parameters were as follows: TRII E, 40/10; flip angle. 20#{176}; imaging volume, 230 mm: and matrix, 160 x 256. A superior saturation band was used to suppress signal within veins. Additional axial three-dimensional TOF MR angiograms were used to better delineate a focal aneurysmal dilatation (35/10; flip angle, 20#{176}: imaging volume, 200 mm; matrix, 256 x 512). Axial three-dimensional TOF MR angiograms ofthe circle of Willis were obtained to evaluate blood flow within the intracranial arteries (45/10: flip angle, 20#{176}: imaging volume. 200 mm; matrix. 256 x 512). The sections acquired, termed source images or partitions. were used for the production of projection angiograms. These projection images were produced using a maximum-intensity-projection algorithm that retains the brightest pixels from the source images. Projection angiograms were viewed at 20#{176} rotations around the spinal axis. MR imaging of the neck was performed using axial TIweighted (500/15: number of excitations, two: imaging volume, 230 mm; matrix, 192 x 256) or T2-weighted (3500/93; number of excitations, one; imaging volume, 230 mm; matrix, 192 x 256) contiguous images of 6- mm thickness (or both) from the bifurcation of the common carotid artery to the siphon. Cerebral sequences, performed to assess intracranial consequences of the dissection, included axial T2-weighted images (3500/93; number of excitations, one; imaging volume, 230 mm; matrix, 192 x 256) and postcontrast TI-weighted images (500/15; number of excitations, two; imaging volume, 230 mm; matrix, 192x256). Our protocol used a common angiographic technique-the time-of-flight technique-and a common postprocessing algorithm-the maximum-intensity-projection algorithm. However, several angiographic techniques (and various algorithms) exist and are still evolving: phase-contrast techniques, blackblood techniques, and contrast-enhanced MR angiographic methods. Therefore, the equipment and software, as well as the protocols, may differ from one center to another, especially for those using dynamic contrast injection for MR angiography. Diagnosis Criteria of Internal Carotid Artery Dissection Internal carotid artery dissection is caused by the penetration of blood through the arterial wall with the development of an intramural Received July 27, 1998; accepted after revision December 17, All authors: Service de Radiologie, HOpital Saint-Antoine, 184 Rue du Faubourg Saint-Antoine, Paris Cedex 12, France. Address correspondence to V. Bousson. AJR1999;173: X199/ American Roentgen Ray Society AJft173, July

2 Bousson et al. Fig. 1.-Subacute double internal carotid artery dissection in 53-year-old man with bilateral lower cranial nerve palsies. Axial Ti-weighted MR image shows typical semilunar-shaped or crescentic hyperintense thrombus within wall of both internal carotid arteries (black arrows). High signal intensity is caused by methemoglobin within thrombus. Hematomas are responsible for narrowing of both lumens (white arrows), which is marked on left side, and for increased external diameter of arteries. Increased external diameters might compress lower cranial nerves in carotid space, thus explaining palsies. hematoma. Blood can dissect subintimally or extend into the subadventitial plane. Criteria of dissection seen at MR angiography and MR imaging are direct visibility of the hematoma and increased external diameter of the artery and narrowing of its lumen [4]. Mural Hematoma On MR imaging, the mural hematoma typically appears as tissue with an abnormal signal intensity adjacent to the vessel lumen. Sometimes annular, the mural hematoma more typically has a semilunar shape. The signal intensity depends on the age of the hematoma. In the acute stage (1-4 days), the signal intensity is low on both TI- and T2- weighted images. In the subacute stage. the signal is hyperintense because of the presence of methemoglobin, making diagnosis less difficult (Figs. 1-5). On MR angiography with the TOF technique, subacute mural hematoma is included in the projection image that is created. Because methemoglobin has a short TI. methemoglobin cannot be saturated, as other stationary tissues are. by the rapid application of multiple RF pulses. Using a maximum-intensity-projection algorithm. the brightest pixels are extracted to create a projection image. and thus the subacute hematoma is included (Figs. 2-5). Fig. 2.-Subacute stenosis of right extracranial internal carotid artery dissection in 45-year-old woman with painful incomplete right Homer s syndrome (postganglionic syndrome including ptosis and miosis on same side, but not anahydrosis). A, Coronal three-dimensional time-of-flight MR angiogram shows marked increase in external diameter of artery, beginning approximately 2 cm above common carotid artery bifurcation (white arrow) and extending close to entry into petrous carotid canal (black arrow). Arrowhead points to left internal carotid artery redundancy. B, Corresponding axial Ti-weighted MR image shows predominantly subadventitial hematoma (arrowhead). Note narrowed but still patent lumen (arrow). However, flow within the true lumen usually gives a more intense signal than does mural hematoma [4] (Figs. 3 and 4). Abnormal signal intensity of flow-related phenomena can mimic dissecting hemorrhage on MR imaging. However, flow-related phenomena generally produce signal abnormalities that are located centrally (within the lumen), rather than peripherally, and that are not crescentic. The homogeneity of the hyperintense signal of mural hematoma on all slices and sequences [6] and the two following criteria (especially arterial expansion) provide evidence of dissection rather than slow flow. Increased External Diameter ofthe Internal Carotid Artery An intramural hematoma typically results in an increase in the diameter of the internal carotid artery (Figs. 2-4). Levy et al. [4] showed that this finding was the best indicator of internal carotid artery dissection at three-dimensional TOF MR angiography, with respective sensitivity and specificity of 95% and 99%. Narrowing ofthe Lumen ofthe Internal CarotidArtery The degree ofnarrowing ofthe lumen is highly variable. Lumen stenosis or occlusion is most likely caused by subintimal hematoma (Fig. 5). Visualization of a double lumen, which is common in cases of aortic dissection, is rarely observed in cases of internal carotid artery dissection [7]. Angiographic observations of intimal flaps (separating true lumen from false lumen) reveal that the flaps are of variable length and are usually seen near the proximal end of the dissection. A thin band of low signal intensity can sometimes be seen between the residual lumen and the hematoma on sagittal or coronal reconstructions of MR angiograms. This finding might represent the intimal flap. but comparison with axial Ti- or T2-weighted images or with the source image of an axial MR angiogram reveals that, in most cases, this finding instead represents the interface between two regions of different signal intensity. Location and Extent of the Dissection Longitudinal Extension Internal carotid artery dissections usually involve the extracranial part of the artery, sparing the carotid bulb and beginning approximately 2 cm distal to the common carotid bifurcation (Figs. 2 and 3). The dissections extend cephalad for a variable length. usually terminating proximal to the petrous carotid canal (Fig. 2). Less commonly, 140 AJR:i73, July 1999

3 Fig. 3.-Subacute stenosis of extra- and intracranial right internal carotid artery caused by dissection in 37- year-old man. A, Coronal three-dimensional time-offiight (TOF) MR angiogram shows right internal carotid artery dissection, beginning above bulb (arrowhead) and extending to horizontal portion of petrous internal carotid artery (open arrow). Intramural thrombus (solid thin arrow) is hypointense relative to intraluminal flow (solid thick arrow) but hyperintense relative to surrounding saturated tissue because of short longitudinal relaxation constant of methemoglobin. B, Source image from coronal three-dimensional TOF MR angiogram shows hyperintense mural hematoma (solid thin arrow) and flow within patent lumen (solid thick arrow), which is more hyperintense than hematoma. Intramural hematoma is also seen within horizontal petrous carotid artery (open arrow). C. Axial Ti-weighted MR image at level of petrous bones depicts thrombus within wall of horizontal petrous artery (thin arrows). Thick arrow points to normal left petrous internal carotid artery. D, Follow-up three-dimensional TOF MR angiogram performed 2 months later shows that mural hematoma seen on initial MR angiogram has disappeared but without complete resolution of narrowing of lumen (arrow). Fig. 4.-Right stenosis of cervical internal carotid artery dissection in 30-year-old woman. A, Coronal three-dimensional time-of-flight (TOF) MR angiogram shows subacute right cervical internal carotid artery hematoma (arrowheads). Arrow points to flow within patent lumen. B, Source image from axial three-dimensional TOF MR angiogram shows that outer diameter of right internal carotid artery is enlarged, with intramural thrombus (arrowheads) that is hypointense relative to intraluminal flow (arrow) but hyperintense relative to surrounding saturated tissue. Open arrow points to normal left internal carotid artery. Note difference of size of lumen of both internal carotid arteries. C, Axial Ti-weighted MR image at same level as that in B shows hyperintense mural hematoma (arrowheads) surrounding signal void of blood flow (arrow). Open arrow points to normal left internal carotid artery. AJR:173, July

4 Bousson et al. extension is seen within the petrous canal (Fig. 3) and can involve the intracavernous segments of the artery. Some dissections involve only a limited part of the internal carotid artery (Figs. 4 and 5). Axial Extension Consequences on the blood flow depend on the location of-either subintimal or subadventitial-and axial extension of the hematoma. Lumen narrowing can be subtle or severe (Fig. 5) up to the point of complete occlusion of the artery. If the intramural hematoma extends into the subadventitial plane. a focal aneurysmal dilatation of the artery may be formed. Such dissections with saclike outpouching are termed aneurysmal dissections. Therefore. internal carotid artery dissections are systematically divided into stenotic, occlusive, and aneurysmal dissections [7]. Other Arteries Concomitant or delayed bilateral internal carotid artery dissections can be observed (Figs. I and 6). as well as involvement of vertebral arteries. Intracranial Consequences Transient ischemic attack or stroke may resuit from two phenomena: either a local thrombus that develops as a result of lumen stenosis and causes embolic complications or a severe stenosis or occlusion of the artery that is responsible for decreased cerebral blood flow. Intracranial consequences depend on the ability of developing collateral blood circulation. The most commonly affected territory is that of the middle cerebral artery (Fig. 6), but anterior and posterior intracranial circulation may be affected. Fig. 5.-Severe stenosis of intrapetrous right internal carotid artery caused by dissection in 47-year-old woman complaining of right-sided tinnitus that had been present for 15 days at presentation. A, Coronal three-dimensional time-of-flight (TOF) MR angiogram shows right internal carotid artery dissection involving horizontal petrous portion of right internal carotid artery (thick arrow). Blood flow below level of dissection is difficult to see (thin arrow) because of saturation phenomenon caused by slow flow. Blood flow above dissection is highly reduced (arrowhead) and not visible on this coronal three-dirn mensional TOF MR sequence. B, Axial Ti-weighted MR image depicts mural hematoma at end of horizontal petrous portion of carotid artery (short arrows(. Arrowhead points to left internal carotid artery at same level. Note severe narrowing of lumen (long arrow). Underlying Factors Internal carotid artery redundancy and fibromuscular dysplasia are known to substantially increase risk of internal carotid artery dissection. Redundancy is easily depicted by MR angiography unlike fibromuscular dysplasia. fbr which the technique has poor sensitivity. Follow-Up Variable recovery of dissected internal carotid artery is observed. from restitution ad integrun to persistent residual stenosis or occlusion of the artery (Fig. 6). Stenoses and occlusions are often transient. and recanalization occurs during the first 2 months in two thirds of patients (Fig. 3). Complete recanalization occurs in approximately 60% of initial occlusions and 90% of initial stenoses [8]. Focal aneurysmal dilatation may be seen at initial presentation of internal carotid ar- Fig. 6.-Follow-up MR angiogram obtained 6 months after dissection shows residual left occlusion and right pseudoaneurysm in 46-year-old man with initial bilateral internal carotid artery dissection (occlusive dissection of left internal carotid artery and aneurysmal dissection of right internal carotid artery) and residual right hemiplegia. A, Coronal three-dimensional time-of-flight MR angiogram (oblique view) depicts residual occlusion of left internal carotid artery, beginning just above bulb (open arrow) and small pseudoaneurysm of subpetrous right internal carotid artery (solid arrow(. B, Axial T2-weighted MR image shows left middle cerebral artery territory infarction (asterisk). 142 AJR:173, July 1999

5 MR Angiography and MR Imaging of the Internal Carotid Artery Fig. 7.-Persistent aneurysmal dilatation on 6-month follow-up was detected by MR angiography of 47-year-old man with initial left internal carotid artery dissection. A, Axial three-dimensional time-of-flight (TOF) MR angiogram depicts small aneurysm of subpetrous left internal carotid artery (arrow). B, Source image from axial three-dimensional TOF MR angiogram shows small aneurysm (arrow) with signal intensity similar to that of circulating blood flow within subpetrous left internal carotid artery (arrowhead). tery dissection or on follow-up images (Figs. 6 and 7). At the early stage. diagnosis is difficult because the distinction between hematoma and flow within the aneurysm is poor. Focused attention is needed on followup imaging. although the treatment of these aneurysms is not clear. The overall prognosis is related to the presence of brain ischemia (Fig. 6)-that is, patients without focal neurologic deficits have an improved outcome compared with those with such deficits. Conclusion MR angiography and MR imaging are useful noninvasive tools for diagnosis of internal carotid artery dissection and its intracranial consequences and for follow-up examinations. Acknowledgment We thank Daniel Rochet for his photographic References assistance. I. Bogousslavsky J, Pierre P. Ischemic stnke in patients under age 45. Neurol Cliii 1992: 10: Biousse V. d Anglejan-Chatillon J. Touboul JP. Amarenco P. Bousser MG. Time course of symptoms in extracranial carotid artery dissections: a series of 80 patients. Stroke 1995:26: Goldberg HI. Grossman RI. Gomori JM. Asbury AK. Bilaniuk LT. Zimmerman RA. Cervical internal carotid artery dissecting hemorrhage: diagnosis using MR. Radiology 1986:158: Levy c, ip. Raveau V. et al. Cantid and vertebral artery dissections: three-dimensional tune-of-flight MR angiography and MR imaging versus conventional angiography. Radiology 1994:190: Klufas RA, Hsu L Barnes PD, Patel MR. Schwartz RB. Dissection of the carotid and vertebral arteries: imaging with MR angiography. AiR 1995:164: Stnngans K, Liberopoulos K. Giaka E. et al. Threedimensional time-of-flight MR angiography and MR imaging versus conventional angiography in Carotid artery dissections. IniAngiol 1996:15: Houser OW, Mokri B. Sundt TM. Baker HL, Reese DF. Spontaneous cervical cephalic arterial dissection and its residuum: angiographic spectrum. AJNR 1984:5: Sturzenegger M, Maule HP, Rivoir A. Baumgartner RW. Ultrasound findings in carotid artery dissection: analysis of 43 patients. Neurology 1995:45: AJR:173, July