Donate Help Contact The AHA Sign In Home
American Heart Association
Circulation
Search: search_blue_button Advanced Search
Circulation. 2005;111:2768-2775
Published online before print May 23, 2005, doi: 10.1161/CIRCULATIONAHA.104.504167
This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow All Versions of this Article:
111/21/2768    most recent
CIRCULATIONAHA.104.504167v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowRequest Permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Takaya, N.
Right arrow Articles by Hatsukami, T. S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Takaya, N.
Right arrow Articles by Hatsukami, T. S.
Related Collections
Right arrow Pathophysiology
Right arrow Imaging
Right arrow Computerized tomography and Magnetic Resonance Imaging

(Circulation. 2005;111:2768-2775.)
© 2005 American Heart Association, Inc.


Imaging

Presence of Intraplaque Hemorrhage Stimulates Progression of Carotid Atherosclerotic Plaques

A High-Resolution Magnetic Resonance Imaging Study

Norihide Takaya, MD, PhD; Chun Yuan, PhD; Baocheng Chu, MD, PhD; Tobias Saam, MD; Nayak L. Polissar, PhD; Gail P. Jarvik, MD, PhD; Carol Isaac, RVT; Judith McDonough, BS; Cynthia Natiello, RN; Randy Small, HT; Marina S. Ferguson, MT; Thomas S. Hatsukami, MD

From the Departments of Radiology (N.T., C.Y., B.C., T.S., M.S.F.), Pathology (R.S.), and Medicine, Division of Medical Genetics (G.P.J.), University of Washington, Seattle; Department of Cardiology, Juntendo University School of Medicine, Tokyo, Japan (N.T.); Mountain-Whisper-Light Statistical Consulting, Seattle, Wash (N.L.P.); and Department of Surgery, University of Washington, and Veterans Affairs Puget Sound Health Care System, Seattle, Wash (C.I., J.M., C.N., T.S.H.).

Correspondence to Thomas S. Hatsukami, MD, Veterans Affairs Puget Sound Health Care System, Surgery and Perioperative Care (112), 1660 S Columbian Way, Seattle, WA 98108. E-mail tomhat{at}u.washington.edu

Received September 1, 2004; revision received January 25, 2005; accepted February 22, 2005.

Background— Previous studies suggest that erythrocyte membranes from intraplaque hemorrhage into the necrotic core are a source of free cholesterol and may become a driving force in the progression of atherosclerosis. We have shown that MRI can accurately identify carotid intraplaque hemorrhage and precisely measure plaque volume. We tested the hypothesis that hemorrhage into carotid atheroma stimulates plaque progression.

Methods and Results— Twenty-nine subjects (14 cases with intraplaque hemorrhage and 15 controls with comparably sized plaques without intraplaque hemorrhage at baseline) underwent serial carotid MRI examination with a multicontrast weighted protocol (T1, T2, proton density, and 3D time of flight) over a period of 18 months. The volumes of wall, lumen, lipid-rich necrotic core, calcification, and intraplaque hemorrhage were measured with a custom-designed image analysis tool. The percent change in wall volume (6.8% versus –0.15%; P=0.009) and lipid-rich necrotic core volume (28.4% versus –5.2%; P=0.001) was significantly higher in the hemorrhage group than in controls over the course of the study. Furthermore, those with intraplaque hemorrhage at baseline were much more likely to have new plaque hemorrhages at 18 months compared with controls (43% versus 0%; P=0.006).

Conclusions— Hemorrhage into the carotid atherosclerotic plaque accelerated plaque progression in an 18-month period. Repeated bleeding into the plaque may produce a stimulus for the progression of atherosclerosis by increasing lipid core and plaque volume and creating new destabilizing factors.


Key Words: magnetic resonance imaging • carotid arteries • hemorrhage • atherosclerosis • plaque




This article has been cited by other articles:


Home page
Arterioscler. Thromb. Vasc. Bio.Home page
H. Ota, W. Yu, H. R. Underhill, M. Oikawa, L. Dong, X. Zhao, N. L. Polissar, B. Neradilek, T. Gao, Z. Zhang, et al.
Hemorrhage and Large Lipid-Rich Necrotic Cores Are Independently Associated With Thin or Ruptured Fibrous Caps: An In vivo 3T MRI Study
Arterioscler Thromb Vasc Biol, October 1, 2009; 29(10): 1696 - 1701.
[Abstract] [Full Text] [PDF]


Home page
RadioGraphicsHome page
C. Oppenheim, O. Naggara, E. Touze, J.-C. Lacour, E. Schmitt, F. Bonneville, S. Crozier, E. Guegan-Massardier, E. Gerardin, X. Leclerc, et al.
High-Resolution MR Imaging of the Cervical Arterial Wall: What the Radiologist Needs to Know
RadioGraphics, September 1, 2009; 29(5): 1413 - 1431.
[Abstract] [Full Text] [PDF]


Home page
Cardiovasc ResHome page
J. Le Dall, B. Ho-Tin-Noe, L. Louedec, O. Meilhac, C. Roncal, P. Carmeliet, S. Germain, J.-B. Michel, and X. Houard
Immaturity of microvessels in haemorrhagic plaques is associated with proteolytic degradation of angiogenic factors
Cardiovasc Res, August 13, 2009; (2009) cvp253v2.
[Abstract] [Full Text] [PDF]


Home page
Eur Heart JHome page
K. Yunoki, T. Naruko, R. Komatsu, S. Ehara, N. Shirai, K. Sugioka, M. Nakagawa, C. Kitabayashi, Y. Ikura, A. Itoh, et al.
Enhanced expression of haemoglobin scavenger receptor in accumulated macrophages of culprit lesions in acute coronary syndromes
Eur. Heart J., August 1, 2009; 30(15): 1844 - 1852.
[Abstract] [Full Text] [PDF]


Home page
J Am Coll Cardiol ImgHome page
B. Chu, M. S. Ferguson, H. Chen, D. S. Hippe, W. S. Kerwin, G. Canton, C. Yuan, and T. S. Hatsukami
Cardiac Magnetic Resonance Features of the Disruption-Prone and the Disrupted Carotid Plaque
J. Am. Coll. Cardiol. Img., July 1, 2009; 2(7): 883 - 896.
[Abstract] [Full Text] [PDF]


Home page
RadiologyHome page
R. Bitar, A. R. Moody, G. Leung, S. Symons, S. Crisp, J. Butany, C. Rowsell, A. Kiss, A. Nelson, and R. Maggisano
In Vivo 3D High-Spatial-Resolution MR Imaging of Intraplaque Hemorrhage
Radiology, October 1, 2008; 249(1): 259 - 267.
[Abstract] [Full Text] [PDF]


Home page
J Am Coll Cardiol ImgHome page
P. M. Winter, S. D. Caruthers, H. Zhang, T. A. Williams, S. A. Wickline, and G. M. Lanza
Antiangiogenic synergism of integrin-targeted fumagillin nanoparticles and atorvastatin in atherosclerosis.
J. Am. Coll. Cardiol. Img., September 1, 2008; 1(5): 624 - 634.
[Abstract] [Full Text] [PDF]


Home page
RadiologyHome page
H. R. Underhill, V. L. Yarnykh, T. S. Hatsukami, J. Wang, N. Balu, C. E. Hayes, M. Oikawa, W. Yu, D. Xu, B. Chu, et al.
Carotid Plaque Morphology and Composition: Initial Comparison between 1.5- and 3.0-T Magnetic Field Strengths
Radiology, August 1, 2008; 248(2): 550 - 560.
[Abstract] [Full Text] [PDF]


Home page
RadiologyHome page
N. Altaf, P. S. Morgan, A. Moody, S. T. MacSweeney, J. R. Gladman, and D. P. Auer
Brain White Matter Hyperintensities Are Associated with Carotid Intraplaque Hemorrhage
Radiology, July 1, 2008; 248(1): 202 - 209.
[Abstract] [Full Text] [PDF]


Home page
StrokeHome page
J. N. Redgrave, P. Gallagher, J. K. Lovett, and P. M. Rothwell
Critical Cap Thickness and Rupture in Symptomatic Carotid Plaques: The Oxford Plaque Study
Stroke, June 1, 2008; 39(6): 1722 - 1729.
[Abstract] [Full Text] [PDF]


Home page
J Am Coll CardiolHome page
T. Saam, H. R. Underhill, B. Chu, N. Takaya, J. Cai, N. L. Polissar, C. Yuan, and T. S. Hatsukami
Prevalence of American Heart Association type VI carotid atherosclerotic lesions identified by magnetic resonance imaging for different levels of stenosis as measured by duplex ultrasound.
J. Am. Coll. Cardiol., March 11, 2008; 51(10): 1014 - 1021.
[Abstract] [Full Text] [PDF]


Home page
Arterioscler. Thromb. Vasc. Bio.Home page
E. Lancelot, V. Amirbekian, I. Brigger, J.-S. Raynaud, S. Ballet, C. David, O. Rousseaux, S. Le Greneur, M. Port, H. R. Lijnen, et al.
Evaluation of Matrix Metalloproteinases in Atherosclerosis Using a Novel Noninvasive Imaging Approach
Arterioscler Thromb Vasc Biol, March 1, 2008; 28(3): 425 - 432.
[Abstract] [Full Text] [PDF]


Home page
StrokeHome page
B. A. Wasserman, A. R. Sharrett, S. Lai, A. S. Gomes, M. Cushman, A. R. Folsom, D. E. Bild, R. A. Kronmal, S. Sinha, and D. A. Bluemke
Risk Factor Associations With the Presence of a Lipid Core in Carotid Plaque of Asymptomatic Individuals Using High-Resolution MRI: The Multi-Ethnic Study of Atherosclerosis (MESA)
Stroke, February 1, 2008; 39(2): 329 - 335.
[Abstract] [Full Text] [PDF]


Home page
J. Neurol. Neurosurg. PsychiatryHome page
T. Y Tang, S. P S Howarth, S. R Miller, M. J Graves, J.-M. U-King-Im, R. A Trivedi, Z. Y. Li, S. R Walsh, A. P Brown, P. J Kirkpatrick, et al.
Comparison of the inflammatory burden of truly asymptomatic carotid atheroma with atherosclerotic plaques contralateral to symptomatic carotid stenosis: an ultra small superparamagnetic iron oxide enhanced magnetic resonance study
J. Neurol. Neurosurg. Psychiatry, December 1, 2007; 78(12): 1337 - 1343.
[Abstract] [Full Text] [PDF]


Home page
J. Leukoc. Biol.Home page
A. Leclercq, X. Houard, M. Philippe, V. Ollivier, U. Sebbag, O. Meilhac, and J.-B. Michel
Involvement of intraplaque hemorrhage in atherothrombosis evolution via neutrophil protease enrichment
J. Leukoc. Biol., December 1, 2007; 82(6): 1420 - 1429.
[Abstract] [Full Text] [PDF]


Home page
JNMHome page
L. G. Spagnoli, E. Bonanno, G. Sangiorgi, and A. Mauriello
Role of Inflammation in Atherosclerosis
J. Nucl. Med., November 1, 2007; 48(11): 1800 - 1815.
[Abstract] [Full Text] [PDF]


Home page
J Am Coll CardiolHome page
F. D. Kolodgie, J. Narula, C. Yuan, A. V. Finn, H. K. Gold, and R. Virmani
Reply
J. Am. Coll. Cardiol., October 9, 2007; 50(15): 1521 - 1521.
[Full Text] [PDF]


Home page
RadiologyHome page
T. Saam, T. S. Hatsukami, N. Takaya, B. Chu, H. Underhill, W. S. Kerwin, J. Cai, M. S. Ferguson, and C. Yuan
The Vulnerable, or High-Risk, Atherosclerotic Plaque: Noninvasive MR Imaging for Characterization and Assessment
Radiology, July 1, 2007; 244(1): 64 - 77.
[Abstract] [Full Text] [PDF]


Home page
Arterioscler. Thromb. Vasc. Bio.Home page
Y. Qiao, I. Ronen, J. Viereck, F. L. Ruberg, and J. A. Hamilton
Identification of Atherosclerotic Lipid Deposits by Diffusion-Weighted Imaging
Arterioscler Thromb Vasc Biol, June 1, 2007; 27(6): 1440 - 1446.
[Abstract] [Full Text] [PDF]


Home page
J Am Coll CardiolHome page
F. D. Kolodgie, J. Narula, C. Yuan, A. P. Burke, A. V. Finn, and R. Virmani
Elimination of Neoangiogenesis for Plaque Stabilization: Is There a Role for Local Drug Therapy?
J. Am. Coll. Cardiol., May 29, 2007; 49(21): 2093 - 2101.
[Abstract] [Full Text] [PDF]


Home page
StrokeHome page
N. Altaf, S. T. MacSweeney, J. Gladman, and D. P. Auer
Carotid Intraplaque Hemorrhage Predicts Recurrent Symptoms in Patients With High-Grade Carotid Stenosis
Stroke, May 1, 2007; 38(5): 1633 - 1635.
[Abstract] [Full Text] [PDF]


Home page
J Am Coll CardiolHome page
X. Houard, A. Leclercq, V. Fontaine, M. Coutard, J.-L. Martin-Ventura, B. Ho-Tin-Noe, Z. Touat, O. Meilhac, and J.-B. Michel
Retention and Activation of Blood-Borne Proteases in the Arterial Wall: Implications for Atherothrombosis
J. Am. Coll. Cardiol., October 27, 2006; 48(9_Suppl_A): A3 - A9.
[Abstract] [Full Text] [PDF]


Home page
Arterioscler. Thromb. Vasc. Bio.Home page
S. Choudhary, C. L. Higgins, I. Y. Chen, M. Reardon, G. Lawrie, G. W. Vick III, C. Karmonik, D. P. Via, and J. D. Morrisett
Quantitation and Localization of Matrix Metalloproteinases and Their Inhibitors in Human Carotid Endarterectomy Tissues
Arterioscler Thromb Vasc Biol, October 1, 2006; 26(10): 2351 - 2358.
[Abstract] [Full Text] [PDF]


Home page
J. Lipid Res.Home page
J. R. Crouse III
Thematic review series: Patient-Oriented Research. Imaging atherosclerosis: state of the art
J. Lipid Res., August 1, 2006; 47(8): 1677 - 1699.
[Abstract] [Full Text] [PDF]


Home page
RadiologyHome page
T. Saam, J. Cai, L. Ma, Y.-Q. Cai, M. S. Ferguson, N. L. Polissar, T. S. Hatsukami, and C. Yuan
Comparison of Symptomatic and Asymptomatic Atherosclerotic Carotid Plaque Features with in Vivo MR Imaging.
Radiology, August 1, 2006; 240(2): 464 - 472.
[Abstract] [Full Text] [PDF]


Home page
J Am Coll CardiolHome page
S. B. Feinstein
Contrast Ultrasound Imaging of the Carotid Artery Vasa Vasorum and Atherosclerotic Plaque Neovascularization
J. Am. Coll. Cardiol., July 18, 2006; 48(2): 236 - 243.
[Abstract] [Full Text] [PDF]


Home page
CirculationHome page
C. Cheng, D. Tempel, R. van Haperen, A. van der Baan, F. Grosveld, M. J.A.P. Daemen, R. Krams, and R. de Crom
Atherosclerotic Lesion Size and Vulnerability Are Determined by Patterns of Fluid Shear Stress
Circulation, June 13, 2006; 113(23): 2744 - 2753.
[Abstract] [Full Text] [PDF]


Home page
Am. J. Pathol.Home page
E. D. MacDougall, F. Kramer, P. Polinsky, S. Barnhart, B. Askari, F. Johansson, R. Varon, M. E. Rosenfeld, K. Oka, L. Chan, et al.
Aggressive Very Low-Density Lipoprotein (VLDL) and LDL Lowering by Gene Transfer of the VLDL Receptor Combined with a Low-Fat Diet Regimen Induces Regression and Reduces Macrophage Content in Advanced Atherosclerotic Lesions in LDL Receptor-Deficient Mice
Am. J. Pathol., June 1, 2006; 168(6): 2064 - 2073.
[Abstract] [Full Text] [PDF]


Home page
Arterioscler. Thromb. Vasc. Bio.Home page
C. M. Matter, M. T. Wyss, P. Meier, N. Spath, T. von Lukowicz, C. Lohmann, B. Weber, A. R. de Molina, J. C. Lacal, S. M. Ametamey, et al.
18F-Choline Images Murine Atherosclerotic Plaques Ex Vivo
Arterioscler Thromb Vasc Biol, March 1, 2006; 26(3): 584 - 589.
[Abstract] [Full Text] [PDF]


Home page
StrokeHome page
N. Takaya, C. Yuan, B. Chu, T. Saam, H. Underhill, J. Cai, N. Tran, N. L. Polissar, C. Isaac, M. S. Ferguson, et al.
Association Between Carotid Plaque Characteristics and Subsequent Ischemic Cerebrovascular Events: A Prospective Assessment With MRI--Initial Results
Stroke, March 1, 2006; 37(3): 818 - 823.
[Abstract] [Full Text] [PDF]


Home page
StrokeHome page
W. A. Willinek
Looking Beyond the Lumen to Predict Cerebrovascular Events: "The Road Less Travelled By"
Stroke, March 1, 2006; 37(3): 759 - 760.
[Full Text] [PDF]


Home page
StrokeHome page
N. Nighoghossian, L. Derex, and P. Douek
The Vulnerable Carotid Artery Plaque: Current Imaging Methods and New Perspectives
Stroke, December 1, 2005; 36(12): 2764 - 2772.
[Abstract] [Full Text] [PDF]


Home page
Arterioscler. Thromb. Vasc. Bio.Home page
R. Virmani, F. D. Kolodgie, A. P. Burke, A. V. Finn, H. K. Gold, T. N. Tulenko, S. P. Wrenn, and J. Narula
Atherosclerotic Plaque Progression and Vulnerability to Rupture: Angiogenesis as a Source of Intraplaque Hemorrhage
Arterioscler Thromb Vasc Biol, October 1, 2005; 25(10): 2054 - 2061.
[Abstract] [Full Text] [PDF]