Development of Carotid Intraplaque Hemorrhage Demonstrated by Serial Magnetic Resonance Imaging

Abstract

HomeCirculationVol. 120, No. 16Development of Carotid Intraplaque Hemorrhage Demonstrated by Serial Magnetic Resonance Imaging Free AccessReview ArticlePDF/EPUBAboutView PDFView EPUBSections ToolsAdd to favoritesDownload citationsTrack citationsPermissions ShareShare onFacebookTwitterLinked InMendeleyReddit Jump toFree AccessReview ArticlePDF/EPUBDevelopment of Carotid Intraplaque Hemorrhage Demonstrated by Serial Magnetic Resonance Imaging R.M. Kwee, MD, F.H.B.M. Schreuder, MD, W.H. Mess, MD, PhD, R.J. van Oostenbrugge, MD, PhD, V.H.J.M. Triebels, MD, L.H. van den Akker, MD, PhD, S. Heeneman, PhD, P.A.M. Hofman, MD, PhD, J.M.A. van Engelshoven, MD, PhD, J.E. Wildberger, MD, PhD and M.E. Kooi, PhD R.M. KweeR.M. Kwee From the Departments of Radiology (R.M.K., P.A.M.H., J.M.A.v.E., J.E.W., M.E.K.), Neurology (F.H.B.M.S., R.J.v.O.), Clinical Neurophysiology (W.H.M.), and Pathology (S.H.) and Cardiovascular Research Institute Maastricht (R.M.K., R.J.v.O., S.H., J.M.A.v.E., J.E.W., M.E.K.), Maastricht University Medical Center, Maastricht, Netherlands; and Departments of Neurology (V.H.J.M.T.) and Vascular Surgery (L.H.v.d.A.), Orbis Medical Center, Sittard, Netherlands. Search for more papers by this author , F.H.B.M. SchreuderF.H.B.M. Schreuder From the Departments of Radiology (R.M.K., P.A.M.H., J.M.A.v.E., J.E.W., M.E.K.), Neurology (F.H.B.M.S., R.J.v.O.), Clinical Neurophysiology (W.H.M.), and Pathology (S.H.) and Cardiovascular Research Institute Maastricht (R.M.K., R.J.v.O., S.H., J.M.A.v.E., J.E.W., M.E.K.), Maastricht University Medical Center, Maastricht, Netherlands; and Departments of Neurology (V.H.J.M.T.) and Vascular Surgery (L.H.v.d.A.), Orbis Medical Center, Sittard, Netherlands. Search for more papers by this author , W.H. MessW.H. Mess From the Departments of Radiology (R.M.K., P.A.M.H., J.M.A.v.E., J.E.W., M.E.K.), Neurology (F.H.B.M.S., R.J.v.O.), Clinical Neurophysiology (W.H.M.), and Pathology (S.H.) and Cardiovascular Research Institute Maastricht (R.M.K., R.J.v.O., S.H., J.M.A.v.E., J.E.W., M.E.K.), Maastricht University Medical Center, Maastricht, Netherlands; and Departments of Neurology (V.H.J.M.T.) and Vascular Surgery (L.H.v.d.A.), Orbis Medical Center, Sittard, Netherlands. Search for more papers by this author , R.J. van OostenbruggeR.J. van Oostenbrugge From the Departments of Radiology (R.M.K., P.A.M.H., J.M.A.v.E., J.E.W., M.E.K.), Neurology (F.H.B.M.S., R.J.v.O.), Clinical Neurophysiology (W.H.M.), and Pathology (S.H.) and Cardiovascular Research Institute Maastricht (R.M.K., R.J.v.O., S.H., J.M.A.v.E., J.E.W., M.E.K.), Maastricht University Medical Center, Maastricht, Netherlands; and Departments of Neurology (V.H.J.M.T.) and Vascular Surgery (L.H.v.d.A.), Orbis Medical Center, Sittard, Netherlands. Search for more papers by this author , V.H.J.M. TriebelsV.H.J.M. Triebels From the Departments of Radiology (R.M.K., P.A.M.H., J.M.A.v.E., J.E.W., M.E.K.), Neurology (F.H.B.M.S., R.J.v.O.), Clinical Neurophysiology (W.H.M.), and Pathology (S.H.) and Cardiovascular Research Institute Maastricht (R.M.K., R.J.v.O., S.H., J.M.A.v.E., J.E.W., M.E.K.), Maastricht University Medical Center, Maastricht, Netherlands; and Departments of Neurology (V.H.J.M.T.) and Vascular Surgery (L.H.v.d.A.), Orbis Medical Center, Sittard, Netherlands. Search for more papers by this author , L.H. van den AkkerL.H. van den Akker From the Departments of Radiology (R.M.K., P.A.M.H., J.M.A.v.E., J.E.W., M.E.K.), Neurology (F.H.B.M.S., R.J.v.O.), Clinical Neurophysiology (W.H.M.), and Pathology (S.H.) and Cardiovascular Research Institute Maastricht (R.M.K., R.J.v.O., S.H., J.M.A.v.E., J.E.W., M.E.K.), Maastricht University Medical Center, Maastricht, Netherlands; and Departments of Neurology (V.H.J.M.T.) and Vascular Surgery (L.H.v.d.A.), Orbis Medical Center, Sittard, Netherlands. Search for more papers by this author , S. HeenemanS. Heeneman From the Departments of Radiology (R.M.K., P.A.M.H., J.M.A.v.E., J.E.W., M.E.K.), Neurology (F.H.B.M.S., R.J.v.O.), Clinical Neurophysiology (W.H.M.), and Pathology (S.H.) and Cardiovascular Research Institute Maastricht (R.M.K., R.J.v.O., S.H., J.M.A.v.E., J.E.W., M.E.K.), Maastricht University Medical Center, Maastricht, Netherlands; and Departments of Neurology (V.H.J.M.T.) and Vascular Surgery (L.H.v.d.A.), Orbis Medical Center, Sittard, Netherlands. Search for more papers by this author , P.A.M. HofmanP.A.M. Hofman From the Departments of Radiology (R.M.K., P.A.M.H., J.M.A.v.E., J.E.W., M.E.K.), Neurology (F.H.B.M.S., R.J.v.O.), Clinical Neurophysiology (W.H.M.), and Pathology (S.H.) and Cardiovascular Research Institute Maastricht (R.M.K., R.J.v.O., S.H., J.M.A.v.E., J.E.W., M.E.K.), Maastricht University Medical Center, Maastricht, Netherlands; and Departments of Neurology (V.H.J.M.T.) and Vascular Surgery (L.H.v.d.A.), Orbis Medical Center, Sittard, Netherlands. Search for more papers by this author , J.M.A. van EngelshovenJ.M.A. van Engelshoven From the Departments of Radiology (R.M.K., P.A.M.H., J.M.A.v.E., J.E.W., M.E.K.), Neurology (F.H.B.M.S., R.J.v.O.), Clinical Neurophysiology (W.H.M.), and Pathology (S.H.) and Cardiovascular Research Institute Maastricht (R.M.K., R.J.v.O., S.H., J.M.A.v.E., J.E.W., M.E.K.), Maastricht University Medical Center, Maastricht, Netherlands; and Departments of Neurology (V.H.J.M.T.) and Vascular Surgery (L.H.v.d.A.), Orbis Medical Center, Sittard, Netherlands. Search for more papers by this author , J.E. WildbergerJ.E. Wildberger From the Departments of Radiology (R.M.K., P.A.M.H., J.M.A.v.E., J.E.W., M.E.K.), Neurology (F.H.B.M.S., R.J.v.O.), Clinical Neurophysiology (W.H.M.), and Pathology (S.H.) and Cardiovascular Research Institute Maastricht (R.M.K., R.J.v.O., S.H., J.M.A.v.E., J.E.W., M.E.K.), Maastricht University Medical Center, Maastricht, Netherlands; and Departments of Neurology (V.H.J.M.T.) and Vascular Surgery (L.H.v.d.A.), Orbis Medical Center, Sittard, Netherlands. Search for more papers by this author and M.E. KooiM.E. Kooi From the Departments of Radiology (R.M.K., P.A.M.H., J.M.A.v.E., J.E.W., M.E.K.), Neurology (F.H.B.M.S., R.J.v.O.), Clinical Neurophysiology (W.H.M.), and Pathology (S.H.) and Cardiovascular Research Institute Maastricht (R.M.K., R.J.v.O., S.H., J.M.A.v.E., J.E.W., M.E.K.), Maastricht University Medical Center, Maastricht, Netherlands; and Departments of Neurology (V.H.J.M.T.) and Vascular Surgery (L.H.v.d.A.), Orbis Medical Center, Sittard, Netherlands. Search for more papers by this author Originally published20 Oct 2009https://doi.org/10.1161/CIRCULATIONAHA.109.873513Circulation. 2009;120:1637–1639A 68-year-old man presented with a sudden onset of weakness and paresthesia of the left arm. He had a history of myocardial infarction 4 years earlier and a known renal artery stenosis. A nonenhanced computed tomographic scan of the brain showed no signs of hemorrhage or infarction. The patient underwent intravenous thrombolysis with alteplase (0.9 mg/kg body wt, 10% initial bolus dose over 1 minute, followed by infusion of the remaining 90% of the dose over 60 minutes). Soon after, the symptoms completely disappeared except for the persistence of a slight paresthesia of the left arm. Doppler ultrasonography revealed a hypoechoic plaque proximally in the right internal carotid artery causing a 50% to 69% stenosis. ECG showed sinus rhythm with complete right bundle-branch block without ST-segment or T-wave abnormalities. Transcranial Doppler imaging revealed no stenosis of the right middle cerebral artery. Serum lipid profile was within normal limits. In addition to the aspirin (100 mg once per day) and atorvastatin (40 mg once per day) he was already using, the patient was prescribed dipyridamole (200 mg twice per day) for secondary stroke prevention.Fifteen days after the initial onset of symptoms, the patient was enrolled in a clinical study investigating the natural history of carotid artery plaques. Magnetic resonance imaging scans of the brain and right carotid artery plaque were obtained, which revealed a recent discrete infarction of the right sensory region (Figure 1A and 1B) and a plaque with a large lipid-rich necrotic core with no or little hemorrhage (Figure 2A through 2D), respectively. Download figureDownload PowerPointFigure 1. Cross-sectional magnetic resonance images of the brain. Baseline fluid-attenuated inversion recovery (A) and diffusion-weighted (B) images show a very small hyperintense area in the right sensory region (arrows), indicating recent discrete infarction. Compared with baseline magnetic resonance images, follow-up fluid-attenuated inversion recovery (C) and diffusion-weighted images (D) clearly show a new hyperintense area in the right motor region (arrows), indicating recent infarction.Download figureDownload PowerPointFigure 2. High-spatial-resolution magnetic resonance image, with cross-sectional coregistered images through plaque in the internal carotid artery. Baseline T2-weighted image (A) and precontrast (B) and postcontrast (C) T1-weighted images and plaque contours (D) (white: carotid artery lumen; light gray: vessel wall area) are shown. T2-weighted image (A) shows isointense plaque, precontrast T1-weighted image (B) shows hyperintense plaque, and postcontrast T1-weighted image (C) shows no enhancement of the plaque, which matches the criteria of a lipid-rich necrotic core with no or little hemorrhage. Follow-up T2-weighted (E) and precontrast (F) and postcontrast (G) T1-weighted images and plaque contours (F) (white: carotid artery lumen; light gray: vessel wall area; dark gray: hemorrhage) are shown. T2-weighted image (E) shows a striking hyperintense area within the plaque, adjacent to the lumen (dark gray area in H). This area is hyperintense at the precontrast T1-weighted image (F) and does not enhance at the postcontrast T1-weighted image (G). These findings indicate recent intraplaque hemorrhage.Three months after the initial event, the patient once more presented with sudden onset of weakness and a numb feeling of the left arm. The patient again underwent intravenous thrombolysis with alteplase. However, the symptoms persisted. A nonenhanced computed tomographic scan, performed 24 hours after thrombolysis, revealed a hypodense area in the right motor region. Repeated Doppler ultrasonography showed no change in carotid plaque echogenicity and degree of luminal narrowing of the right internal carotid artery. Ten days after the onset of the second event, the patient underwent repeated magnetic resonance imaging scans of the brain and right internal carotid artery plaque. These scans confirmed recent infarction in the right motor region (Figure 1C and 1D) and revealed recent intraplaque hemorrhage (Figure 2E through 2H).Because of recurrent symptoms, the patient underwent carotid endarterectomy 20 days after the onset of the second event. Histological analysis of the excised plaque demonstrated large intraplaque hemorrhage (Figure 3A and 3B), confirming the magnetic resonance imaging findings. According to the American Heart Association, it was a type VI plaque (complex plaque with possible surface defect, hemorrhage, or thrombus).1Download figureDownload PowerPointFigure 3. Cross section through the carotid endarterectomy specimen, corresponding to the level of the magnetic resonance images (Figure 2). Hematoxylin-eosin staining; magnification ×125 (A) and ×1000 (B). There are large areas of intraplaque hemorrhage (asterisks in A). At the right shoulder region, the fibrous cap is very thin and shows recent reendothelialization (arrows in A and B). Many erythrocytes are present within the fibrous cap (B).To our knowledge, this is the first report showing the in vivo development of carotid intraplaque hemorrhage and the coincidence of ipsilateral ischemic stroke. The findings of this case are in accordance with results of previous studies, which showed that carotid intraplaque hemorrhage on magnetic resonance imaging is associated with cerebral ischemic events.2–4Sources of FundingThis study was supported by a Dutch Heart Foundation grant (2006B061).DisclosuresNone.FootnotesReprint requests to Robert M. Kwee, MD, Department of Radiology, Cardiovascular Research Institute Maastricht, Maastricht University Medical Center, PO Box 5800, 6202 AZ Maastricht, the Netherlands. E-mail [email protected]References1 Stary HC, Chandler AB, Dinsmore RE, Fuster V, Glagov S, Insull W Jr, Rosenfeld ME, Schwartz CJ, Wagner WD, Wissler RW. A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis: a report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Arterioscler Thromb Vasc Biol. 1995; 15: 1512–1531.CrossrefMedlineGoogle Scholar2 Murphy RE, Moody AR, Morgan PS, Martel AL, Delay GS, Allder S, MacSweeney ST, Tennant WG, Gladman J, Lowe J, Hunt BJ. Prevalence of complicated carotid atheroma as detected by magnetic resonance direct thrombus imaging in patients with suspected carotid artery stenosis and previous acute cerebral ischemia. Circulation. 2003; 107: 3053–3058.LinkGoogle Scholar3 Altaf N, Daniels L, Morgan PS, Auer D, MacSweeney ST, Moody AR, Gladman JR. Detection of intraplaque hemorrhage by magnetic resonance imaging in symptomatic patients with mild to moderate carotid stenosis predicts recurrent neurological events. J Vasc Surg. 2008; 47: 337–342.CrossrefMedlineGoogle Scholar4 Takaya N, Yuan C, Chu B, Saam T, Underhill H, Cai J, Tran N, Polissar NL, Isaac C, Ferguson MS, Garden GA, Cramer SC, Maravilla KR, Hashimoto B, Hatsukami TS. Association between carotid plaque characteristics and subsequent ischemic cerebrovascular events: a prospective assessment with MRI—initial results. Stroke. 2006; 37: 818–823.LinkGoogle Scholar Previous Back to top Next FiguresReferencesRelatedDetailsCited By Appel A, Chou C, Larson J, Zhong Z, Schoen F, Johnston C, Brey E and Anastasio M (2013) An initial evaluation of analyser-based phase-contrast X-ray imaging of carotid plaque microstructure, The British Journal of Radiology, 10.1259/bjr.20120318, 86:1021, (20120318-20120318), Online publication date: 1-Jan-2013. Hoeks A and Kooi M (2011) Wear and Tear⁎⁎Editorials published in JACC: Cardiovascular Imaging reflect the views of the authors and do not necessarily represent the views of JACC: Cardiovascular Imaging or the American College of Cardiology., JACC: Cardiovascular Imaging, 10.1016/j.jcmg.2011.03.003, 4:5, (478-480), Online publication date: 1-May-2011. Kwee R, van Oostenbrugge R, Mess W, Prins M, van der Geest R, ter Berg J, Franke C, Korten A, Meems B, van Engelshoven J, Wildberger J and Kooi M (2010) Carotid Plaques in Transient Ischemic Attack and Stroke Patients, Investigative Radiology, 10.1097/RLI.0b013e3181ed15ff, 45:12, (803-809), Online publication date: 1-Dec-2010. October 20, 2009Vol 120, Issue 16 Advertisement Article InformationMetrics https://doi.org/10.1161/CIRCULATIONAHA.109.873513PMID: 19841310 Originally publishedOctober 20, 2009 PDF download Advertisement SubjectsComputerized Tomography (CT)ImagingStenosis