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Diffusion-Weighted Magnetic Resonance Imaging in Internal Carotid Artery Dissection
Sebastian Koch, MD;
Alejandro A. Rabinstein, MD;
Jose G. Romano, MD;
Alejandro Forteza, MD
Arch Neurol. 2004;61:510-512.
ABSTRACT
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Background Acute multiple brain infarction pattern on diffusion-weighted imaging is associated with arterial or cardiac sources of embolism.
Objectives To review the diffusion-weighted imaging characteristics of patients with strokes secondary to internal carotid artery (ICA) dissection and to gain further insights into the mechanisms of cerebral ischemia.
Design Patients with ICA dissection and ischemic stroke were identified by review of an angiographic database and hospital discharge codes. Patients were included if the diagnosis of ICA dissection was confirmed and diffusion-weighted imaging was obtained within 10 days of symptom onset. Infarct patterns were analyzed according to established templates of vascular territories.
Results Inclusion criteria were met by 14 patients. Internal carotid artery occlusion was present in 10. Acute multiple brain infarction was found in 10 (71%) of the 14 patients. Cortical involvement was found in 8 patients, while the infarct was restricted to the subcortical region in 6. In 9 (64%) of the 14 patients, ischemic lesions were located in 1 of the 3 border zones.
Conclusions Acute multiple brain infarction pattern with border zone involvement is frequently found in ICA dissection–related strokes. This finding may further support an interaction of hemodynamic and embolic mechanisms as a cause of cerebral ischemia in this condition.
INTRODUCTION
Analysis of infarct patterns on computed tomography and magnetic resonance (MR) imaging has led to deeper insights into the mechanisms of cerebral ischemia. Diffusion-weighted imaging (DWI) allows the identification of small ischemic lesions, which may not be detected by computed tomography or conventional MR imaging.1-2 Multiple acute ischemic lesions, also known as acute multiple brain infarction (AMBI), on DWI are associated with arterial or cardiac sources of embolism.3-4 This pattern is believed to arise from repeated embolism or the fragmentation of a single embolus, resulting in at least 2 noncontiguous areas of cerebral infarction.4-5
The mechanism of ischemia in internal carotid artery (ICA) dissection remains controversial. Sudden narrowing of the arterial lumen in dissections may result in rapid hemodynamic compromise, leading to infarction. Weiller et al6 found an equal role of hemodynamic and embolic mechanisms in ICA dissection. Two other studies7-8 highlighted the importance of embolism. If, indeed, embolism is the predominant mechanism of cerebral ischemia in ICA dissection, it is likely that DWI will detect the presence of AMBI in this setting. We therefore undertook this study to review the DWI characteristics of patients with ICA dissection.
METHODS
Patients admitted to Jackson Memorial Hospital, Miami, Fla, between August 1, 1999, and February 28, 2003, with a diagnosis of ICA dissection were identified by review of an angiographic database and of hospital discharge codes (International Classification of Diseases, Ninth Revision, Clinical Modification, codes 433 and 434). We reviewed the medical charts and radiological data (catheter cerebral angiograms, neck MR angiograms, and neck MR imaging with fat-suppressed images) of patients diagnosed as having ICA dissection by the treating physicians to confirm the primary diagnosis. Patients were included if DWI was obtained within 10 days of symptom onset. Penetrating injury to the neck as a cause of dissection was an exclusion criterion.
Diffusion-weighted imaging studies were reviewed for infarct patterns. Vascular territories were determined according to established vascular maps, and border zones were divided into the anterior, posterior, and deep internal watershed areas.9-10 Infarctions were examined for the presence of AMBI and border zone involvement. Acute multiple brain infarction was defined as 2 separate DWI-positive lesions within the same or different vascular territories. All DWIs were independently interpreted by 2 observers blinded to the clinical data. In cases of discrepancy, a consensus reading was obtained.
RESULTS
We identified 26 patients with ICA dissection. Diffusion-weighted imaging was obtained in 21 patients, and 14 had evidence of cerebral infarction. The clinical features, infarct patterns, and radiological data of this patient group are presented in Figure 1. The diagnosis of dissection was confirmed by intra-arterial angiography (n = 12) and MR angiography with axial MR imaging (n = 2). The mean patient age was 46 years (range, 28-59 years). Nine patients (64%) were men. Hypertension was present in 5 (36%) of the 14 patients. Neck pain or headache on presentation was noted in 4 (29%) of 14. Oculosympathetic paresis was found in 2 of 14.
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Diffusion-weighted imaging (DWI) and clinical findings in patients with internal carotid artery (ICA) dissection. HTN indicates hypertension.
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Internal carotid artery occlusion was present in 10 (71%) of the 14 patients. The right ICA was involved in 8 (57%) of 14 patients. One patient (patient 7) experienced bilateral ICA dissections.
Acute multiple brain infarction was found in 10 (71%) of 14 (patients 1-10). A single infarct was detected in 4 (29%) (patients 11-14). Cortical involvement was found in 8 (57%) (patients 1-3, 8-10, 12, and 14). The infarct was restricted to the subcortical region in 6 (43%) (patients 4-7, 11, and 13). In 9 (64%) (patients 1-8 and 10), ischemic lesions were located in 1 of the 3 border zones. The ICA was occluded in 6 (60%) of 10 patients with AMBI pattern and in 4 (100%) of 4 with a single infarct on DWI. In patients with border zone involvement, 7 of 9 patients had an occluded ICA, compared with 4 of 5 patients without border zone lesions.
COMMENT
In our series of patients with ICA dissection, DWI detected AMBI in 10 (71%) of the 14 patients. Border zone involvement was present in 9 (64%) of 14. Two previous studies7-8 described computed tomography and conventional MR infarct patterns in patients with ICA dissection. Steinke et al8 found evidence of embolic infarcts, defined as territorial middle cerebral artery or large striatocapsular infarcts, in 70% of patients with ICA dissection. In 16% of patients, the area of infarction was located in a border zone. Lucas et al7 found areas of low-flow involvement in 8% of patients with ICA dissection and a stroke pattern suggestive of embolism, using criteria identical to those of Steinke et al, in 92%. Both groups of authors speculated that the incidence of border zone infarction was overestimated because of variability in the vascular anatomy and the misclassification of branch artery occlusion as watershed infarcts.
In the present study, the high incidence of AMBI confirms the importance of embolism in ICA dissection–related strokes. However, we found an increased frequency of border zone involvement compared with the previous series.7-8 In fact, at least 1 lesion of the AMBI was located in a border zone in 9 (64%) of 14 patients. The discrepancy between this finding and those noted by the other 2 author groups may be partially explained by differences in imaging techniques. The 2 previous studies used computed tomography and conventional MR imaging, which have less sensitivity in the detection of small ischemic lesions compared with DWI.1-2 In addition, differences in methods and definition of low-flow infarction, as well as severity of the underlying steno-occlusive vascular disease, with a high number of ICA occlusions being present in this series (71% of patients), may contribute to the discrepancy.
We are not aware of any previous studies analyzing DWI infarct patterns in ICA dissection. Therefore, it may be instructive to compare our findings with those of DWI series of strokes related to atherosclerotic ICA disease. In this condition, an AMBI infarct pattern has been reported to be present in at least 58% to 83% of patients.11-13 These findings are similar to the results of the present study.
Szabo et al12 noted small lesions in hemodynamic risk zones in 33 (32%) of 102 patients. Kang et al13 found border zone involvement, with or without the presence of a territorial lesion, in 10 (29%) of 35 patients. The latter study used methods similar to ours, allowing for a more direct comparison of infarct pattern. The incidence of border zone involvement in that study is lower than the 64% noted in our series, despite the presence of high-grade (>90%) ICA stenosis or occlusion in 86% of patients.
It is likely that in ICA dissection hemodynamic factors assume greater importance as diminished perfusion and embolism interact to cause cerebral infarction. This interaction has been well described recently.14 Decreased perfusion in low-flow zones may fail to wash out emboli. Cerebral infarction may occur more readily in these areas when cerebral embolism takes place.14 Indeed, unilateral watershed infarcts have been associated with embolism,15-16 and following cardiac surgery, territorial and border zone lesions are present simultaneously.17 In addition, border zone infarcts diagnosed by DWI are associated with transcranial Doppler–detected microemboli in patients with middle cerebral artery stenosis.18
The higher frequency of border zone involvement in strokes secondary to ICA dissection, compared with ICA atherosclerotic disease, may be related to a more sudden compromise of cerebral blood flow. Collateral flow may not establish itself as rapidly, leading to greater perfusion loss and increased susceptibility to embolism in the border zone areas.
In summary, ICA dissection should be added to the list of stroke etiologies associated with an AMBI pattern on DWI. Acute multiple brain infarction was found in 71% of patients with ICA dissection. At least 1 ischemic lesion was seen in a border zone area in 64% of patients. These findings may be further evidence for an interaction of hemodynamic and embolic mechanisms in strokes related to ICA dissection.
AUTHOR INFORMATION
Corresponding author and reprints: Sebastian Koch, MD, Department of Neurology, University of Miami School of Medicine, Professional Arts Center, 1150 NW 14th St, Suite 304, Miami, FL 33136 (e-mail: skoch{at}med.miami.edu).
Accepted for publication October 31, 2003.
Author contributions: Study concept and design (Drs Koch and Rabinstein); acquisition of data (Drs Koch, Rabinstein, and Forteza); analysis and interpretation of data (Drs Koch, Rabinstein, Romano, and Forteza); drafting of the manuscript (Dr Koch); critical revision of the manuscript for important intellectual content (Drs Koch, Rabinstein, Romano, and Forteza); administrative, technical, and material support (Dr Koch); study supervision (Drs Koch, Romano, and Forteza).
From the Department of Neurology, University of Miami School of Medicine, Miami, Fla.
REFERENCES
1. Warach S, Chien D, Li W, Ronthal M, Edelman RR. Fast magnetic resonance diffusion-weighted imaging of acute human stroke. Neurology. 1992;42:1717-1723.
FREE FULL TEXT
2. Lutsep HL, Albers GW, de Crespigny A, Kamat GN, Marks MP, Moseley ME. Clinical utility of diffusion-weighted magnetic resonance imaging in the assessment of ischemic stroke. Ann Neurol. 1997;41:574-580.
FULL TEXT
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ISI
| PUBMED
3. Koennecke HC, Bernarding J, Braun J, et al. Scattered brain infarction pattern of diffusion-weighted magnetic resonance imaging in patients with acute ischemic stroke. Cerebrovasc Dis. 2001;11:157-163.
FULL TEXT
|
ISI
| PUBMED
4. Baird AE, Loevblad KO, Schlau G, Edelman RR, Warach S. Multiple acute stroke syndrome: marker of embolic disease? Neurology. 2000;54:674-678.
FREE FULL TEXT
5. Roh JK, Kang DW, Lee SH, Yoon BW, Chang KH. Significance of acute multiple brain infarction on diffusion-weighted imaging. Stroke. 2000;31:688-694.
FREE FULL TEXT
6. Weiller C, Mullges W, Ringelstein EB, Buell U, Reiche W. Pattern of brain infarction in internal carotid artery dissection. Neurosurg Rev. 1991;14:111-113.
FULL TEXT
|
ISI
| PUBMED
7. Lucas C, Moulin T, Deplanque D, Tatu L, Chavot D. Stroke patterns of internal carotid artery dissection. Stroke. 1998;29:2646-2648.
FREE FULL TEXT
8. Steinke W, Schwartz A, Hennerici M. Topography of cerebral infarction associated with carotid artery dissection. J Neurol. 1996;243:323-328.
FULL TEXT
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ISI
| PUBMED
9. Ringelstein EB, Stögbauer F. Border-zone infarcts. In: Bogousslavsky J, Caplan L, eds. Stroke Syndromes. 2nd ed. New York, NY: Cambridge University Press; 2001:564-582.
10. Tatu L, Moulin T, Bogousslavsky J, Duvernoy H. Arterial territories of the human brain: cerebral hemisphere. Neurology. 1998;50:1699-1708.
ABSTRACT
11. Kastrup A, Schulz JB, Mader I, Dichgans J, Kuker W. Diffusion-weighted MRI in patients with symptomatic internal carotid artery disease. J Neurol. 2002;249:1168-1174.
FULL TEXT
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ISI
| PUBMED
12. Szabo K, Kern R, Gass A, Hirsch J, Hennerici M. Acute stroke patterns in patients with internal carotid artery disease: a diffusion-weighted magnetic resonance imaging study. Stroke. 2001;32:1323-1329.
FREE FULL TEXT
13. Kang DW, Chu K, Ko SB, Kwon SJ, Yoon BW, Roh JK. Lesion patterns and mechanism of ischemia in internal carotid artery disease: a diffusion-weighted imaging study. Arch Neurol. 2002;59:1577-1582.
FREE FULL TEXT
14. Caplan LR, Hennerici M. Impaired clearance of emboli (washout) is an important link between hypoperfusion, embolism, and ischemic stroke. Arch Neurol. 1998;55:1475-1482.
FREE FULL TEXT
15. Jorgensen L, Torvik A. Ischemic cerebrovascular diseases in an autopsy series: part 2: prevalence, location, pathogenesis, and clinical course of cerebral infarcts. J Neurol Sci. 1969;9:285-320.
FULL TEXT
|
ISI
| PUBMED
16. Belden JR, Caplan LR, Pessin MS, Kwan E. Mechanisms and clinical features of posterior border-zone infarcts. Neurology. 1999;53:1312-1318.
FREE FULL TEXT
17. Wityk RJ, Goldsborough MA, Hillis A, et al. Diffusion- and perfusion-weighted brain magnetic resonance imaging in patients with neurologic complications after cardiac surgery. Arch Neurol. 2001;58:571-576.
FREE FULL TEXT
18. Wong KS, Gao S, Chan YL, et al. Mechanisms of acute cerebral infarctions in patients with middle cerebral artery stenosis: a diffusion-weighted imaging and microemboli monitoring study. Ann Neurol. 2002;52:74-81.
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