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Quantitative MR Analysis for the Assessment of Carotid Atherosclerosis

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Multi-Modality Atherosclerosis Imaging and Diagnosis
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Abstract

In recent years in vivo carotid black blood MRI (bb-MRI) has evolved to be a promising method for imaging atherosclerotic disease of the cervical arteries. Advantages such as noninvasiveness, lack of radiation exposure, excellent soft tissue contrast, accuracy, and reproducibility have contributed to its acceptance. Recent developments of bb-MRI enable to reliably identify and quantify plaque components and to detect features of the vulnerable plaque, such as a thin or ruptured fibrous cap, large necrotic core, intraplaque hemorrhage, macrophage infiltration, and neovascularization. In addition, carotid bb-MRI allows evaluating mechanical forces and the biological activity of atherosclerotic plaques. The ability to quantitatively evaluate a variety of these markers paves the way for a broad application of carotid bb-MRI and permits studies aimed at understanding atherosclerotic disease development, treatment studies, and patient risk stratification. This book chapter will discuss the capabilities of bb-MRI for quantitative assessment of the composition and morphology of atherosclerotic lesions. Technical requirements, such as hardware, software, and sequence considerations will be discussed. Studies, which evaluated the accuracy and reproducibility of carotid bb-MRI, will be shown. In addition, clinical studies will be shown which used bb-MRI to compare symptomatic and asymptomatic plaques, to study the natural history of atherosclerosis, and to evaluate the effect of anti-atherosclerotic drugs on the regression/progression of atherosclerosis.

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Abbreviations

bb-MRI:

Black-blood magnetic resonance imaging

CNR:

Contrast-to-noise ratio

DCE:

Dynamic contrast enhanced

DIR:

Double inversion recovery

FC:

Fibrous cap

ICC:

Intraclass correlation coefficient

IOSB:

Inflow/outflow saturation band

IPH:

Intraplaque hemorrhage

IS:

Inflow saturation

LR/NC:

Lipid-rich/necrotic core

MACE:

Major cardiovascular or cerebrovascular event

MP-RAGE:

Magnetization-prepared rapid acquisition gradient echo

MSDE:

Motion-sensitized driven equilibrium

NWI:

Normalized wall index

PWS:

Plaque wall stress

REX-DIR:

Rapid extended coverage double inversion recovery

SNR:

Signal-to-noise ratio

TI:

Time of inversion

TOF:

Time of flight

USPIO:

Ultrasmall superparamagnetic iron oxide

WSS:

Wall shear stress

References

  1. Virmani R, Kolodgie FD, Burke AP, Farb A, Schwartz SM (2000) Lessons from sudden coronary death: a comprehensive morphological classification scheme for atherosclerotic lesions. Arterioscler Thromb Vasc Biol 20(5):1262–1275

    Article  PubMed  CAS  Google Scholar 

  2. Naghavi M, Libby P, Falk E, Casscells SW, Litovsky S, Rumberger J, Badimon JJ et al (2003) From vulnerable plaque to vulnerable patient: a call for new definitions and risk assessment strategies: part II. Circulation 108(15):1772–1778. doi:10.1161/01.CIR.0000087481.55887.C9

    Article  PubMed  Google Scholar 

  3. Naghavi M, Libby P, Falk E, Casscells SW, Litovsky S, Rumberger J, Badimon JJ et al (2003) From vulnerable plaque to vulnerable patient: a call for new definitions and risk assessment strategies: part I. Circulation 108(14):1664–1672. doi:10.1161/01.CIR.0000087480.94275.97

    Article  PubMed  Google Scholar 

  4. Saam T, Hatsukami TS, Takaya N, Chu B, Underhill H, Kerwin WS, Cai J, Ferguson MS, Yuan C (2007) The vulnerable, or high-risk, atherosclerotic plaque: noninvasive MR imaging for characterization and assessment. Radiology 244(1):64–77. doi:10.1148/radiol.2441051769, 244/1/64 [pii]

    Article  PubMed  Google Scholar 

  5. Yarnykh VL, Terashima M, Hayes CE, Shimakawa A, Takaya N, Nguyen PK, Brittain JH, McConnell MV, Yuan C (2006) Multicontrast black-blood MRI of carotid arteries: comparison between 1.5 and 3 tesla magnetic field strengths. J Magn Reson Imaging 23(5):691–698. doi:10.1002/jmri.20562

    Article  PubMed  Google Scholar 

  6. Koktzoglou I, Chung YC, Mani V, Carroll TJ, Morasch MD, Mizsei G, Simonetti OP, Fayad ZA, Li D (2006) Multislice dark-blood carotid artery wall imaging: a 1.5T and 3.0T comparison. J Magn Reson Imaging 23(5):699–705. doi:10.1002/jmri.20563

    Article  PubMed  Google Scholar 

  7. Underhill HR, Yarnykh VL, Hatsukami TS, Wang J, Balu N, Hayes CE, Oikawa M et al (2008) Carotid plaque morphology and composition: initial comparison between 1.5- and 3.0-T magnetic field strengths. Radiology 248(2):550–560. doi:10.1148/radiol.2482071114, 2482071114 [pii]

    Article  PubMed  Google Scholar 

  8. Kerwin WS, Liu F, Yarnykh V, Underhill H, Oikawa M, Yu W, Hatsukami TS, Yuan C (2008) Signal features of the atherosclerotic plaque at 3.0 Tesla versus 1.5 Tesla: impact on automatic classification. J Magn Reson Imaging 28(4):987–995. doi:10.1002/jmri.21529

    Article  PubMed  Google Scholar 

  9. Hayes CE, Mathis CM, Yuan C (1996) Surface coil phased arrays for high-resolution imaging of the carotid arteries. J Magn Reson Imaging 6(1):109–112

    Article  PubMed  CAS  Google Scholar 

  10. Saam T, Raya JG, Cyran CC, Bochmann K, Meimarakis G, Dietrich O, Clevert DA et al (2009) High resolution carotid black-blood 3T MR with parallel imaging and dedicated 4-channel surface coils. J Cardiovasc Magn Reson 11:41. doi:10.1186/1532-429X-11-41

    Article  PubMed  Google Scholar 

  11. Underhill HR, Yuan C (2011) Carotid MRI: a tool for monitoring individual response to cardiovascular therapy? Expert Rev Cardiovasc Ther 9(1):63–80. doi:10.1586/erc.10.172

    Article  PubMed  Google Scholar 

  12. Serfaty JM, Chaabane L, Tabib A, Chevallier JM, Briguet A, Douek PC (2001) Atherosclerotic plaques: classification and characterization with T2-weighted high-spatial-resolution MR imaging – an in vitro study. Radiology 219(2):403–410

    PubMed  CAS  Google Scholar 

  13. Cappendijk VC, Cleutjens KB, Heeneman S, Schurink GW, Welten RJ, Kessels AG, van Suylen RJ, Daemen MJ, van Engelshoven JM, Kooi ME (2004) In vivo detection of hemorrhage in human atherosclerotic plaques with magnetic resonance imaging. J Magn Reson Imaging 20(1):105–110. doi:10.1002/jmri.20060

    Article  PubMed  Google Scholar 

  14. Corti R, Osende JI, Fayad ZA, Fallon JT, Fuster V, Mizsei G, Dickstein E, Drayer B, Badimon JJ (2002) In vivo noninvasive detection and age definition of arterial thrombus by MRI. J Am Coll Cardiol 39(8):1366–1373

    Article  PubMed  Google Scholar 

  15. Clarke SE, Hammond RR, Mitchell JR, Rutt BK (2003) Quantitative assessment of carotid plaque composition using multicontrast MRI and registered histology. Magn Reson Med 50(6):1199–1208. doi:10.1002/mrm.10618

    Article  PubMed  Google Scholar 

  16. Wang J, MS Ferguson, N Balu, C Yuan, TS Hatsukami, P Bornert. 2010b. Improved carotid intraplaque hemorrhage imaging using a slab-selective phase-sensitive inversion-recovery (SPI) sequence. Magn Reson Med 64(5): 1332-1340.doi:10.1002/mrm.22539

    Article  PubMed  Google Scholar 

  17. Yuan C, Mitsumori LM, Ferguson MS, Polissar NL, Echelard D, Ortiz G, Small R, Davies JW, Kerwin WS, Hatsukami TS (2001) In vivo accuracy of multispectral magnetic resonance imaging for identifying lipid-rich necrotic cores and intraplaque hemorrhage in advanced human carotid plaques. Circulation 104(17):2051–2056

    Article  PubMed  CAS  Google Scholar 

  18. Yuan C, Mitsumori LM, Beach KW, Maravilla KR (2001) Carotid atherosclerotic plaque: noninvasive MR characterization and identification of vulnerable lesions. Radiology 221(2):285–299

    Article  PubMed  CAS  Google Scholar 

  19. Lin W, Abendschein DR, Haacke EM (1997) Contrast-enhanced magnetic resonance angiography of carotid arterial wall in pigs. J Magn Reson Imaging 7(1):183–190

    Article  PubMed  CAS  Google Scholar 

  20. Dumoulin CL, Hart HR Jr (1986) Magnetic resonance angiography. Radiology 161(3):717–720

    PubMed  CAS  Google Scholar 

  21. Yuan C, Kerwin WS, Yarnykh VL, Cai J, Saam T, Chu B, Takaya N et al (2006) MRI of atherosclerosis in clinical trials. NMR Biomed 19(6):636–654. doi:10.1002/nbm.1065

    Article  PubMed  Google Scholar 

  22. Edelman RR, Mattle HP, Wallner B, Bajakian R, Kleefield J, Kent C, Skillman JJ, Mendel JB, Atkinson DJ (1990) Extracranial carotid arteries: evaluation with “black blood” MR angiography. Radiology 177(1):45–50

    PubMed  CAS  Google Scholar 

  23. Edelman RR, Chien D, Kim D (1991) Fast selective black blood MR imaging. Radiology 181(3):655–660

    PubMed  CAS  Google Scholar 

  24. Wang J, Yarnykh VL, Hatsukami T, Chu B, Balu N, Yuan C (2007) Improved suppression of plaque-mimicking artifacts in black-blood carotid atherosclerosis imaging using a multislice motion-sensitized driven-equilibrium (MSDE) turbo spin-echo (TSE) sequence. Magn Reson Med 58(5):973–981. doi:10.1002/mrm.21385

    Article  PubMed  Google Scholar 

  25. Steinman DA, Rutt BK (1998) On the nature and reduction of plaque-mimicking flow artifacts in black blood MRI of the carotid bifurcation. Magn Reson Med 39(4):635–641

    Article  PubMed  CAS  Google Scholar 

  26. Watanabe Y, Nagayama M (2010) MR plaque imaging of the carotid artery. Neuroradiology 52(4):253–274. doi:10.1007/s00234-010-0663-z

    Article  PubMed  Google Scholar 

  27. Simonetti OP, Finn JP, White RD, Laub G, Henry DA (1996) “Black blood” T2-weighted inversion-recovery MR imaging of the heart. Radiology 199(1):49–57

    PubMed  CAS  Google Scholar 

  28. Fayad ZA, Fuster V (2002) Atherothrombotic plaques and the need for imaging. Neuroimaging Clin N Am 12(3):351–364

    Article  PubMed  Google Scholar 

  29. Yarnykh VL, Yuan C (2003) Multislice double inversion-recovery black-blood imaging with simultaneous slice reinversion. J Magn Reson Imaging 17(4):478–483. doi:10.1002/jmri.10278

    Article  PubMed  Google Scholar 

  30. Yarnykh VL, Yuan C (2002) T1-insensitive flow suppression using quadruple inversion-recovery. Magn Reson Med 48(5):899–905. doi:10.1002/mrm.10292

    Article  PubMed  Google Scholar 

  31. Balu N, Wang J, Dong L, Baluyot F, Chen H, Yuan C (2009) Current techniques for MR imaging of atherosclerosis. Top Magn Reson Imaging 20(4):203–215. doi:10.1097/RMR.0b013e3181ea287d00002142-200908000-00001 [pii]

    Article  PubMed  Google Scholar 

  32. Koktzoglou I, Li D (2007) Diffusion-prepared segmented steady-state free precession: application to 3D black-blood cardiovascular magnetic resonance of the thoracic aorta and carotid artery walls. J Cardiovasc Magn Reson 9(1):33–42. doi:10.1080/10976640600843413

    Article  PubMed  Google Scholar 

  33. Wang J, Balu N, Canton G, Yuan C (2010) Imaging biomarkers of cardiovascular disease. J Magn Reson Imaging 32(3):502–515. doi:10.1002/jmri.22266

    Article  PubMed  Google Scholar 

  34. Yim YJ, Choe YH, Ko Y, Kim ST, Kim KH, Jeon P, Byun HS, Kim DI (2008) High signal intensity halo around the carotid artery on maximum intensity projection images of time-of-flight MR angiography: a new sign for intraplaque hemorrhage. J Magn Reson Imaging 27(6):1341–1346. doi:10.1002/jmri.21284

    Article  PubMed  Google Scholar 

  35. Yuan C, Petty C, O’Brien KD, Hatsukami TS, Eary JF, Brown BG (1997) In vitro and in situ magnetic resonance imaging signal features of atherosclerotic plaque-associated lipids. Arterioscler Thromb Vasc Biol 17(8):1496–1503

    Article  PubMed  CAS  Google Scholar 

  36. Takaya N, Cai J, Ferguson MS, Yarnykh VL, Chu B, Saam T, Polissar NL et al (2006) Intra- and interreader reproducibility of magnetic resonance imaging for quantifying the lipid-rich necrotic core is improved with gadolinium contrast enhancement. J Magn Reson Imaging 24(1):203–210. doi:10.1002/jmri.20599

    Article  PubMed  Google Scholar 

  37. Wasserman BA, Smith WI, Trout HH 3rd, Cannon RO 3rd, Balaban RS, Arai AE (2002) Carotid artery atherosclerosis: in vivo morphologic characterization with gadolinium-enhanced double-oblique MR imaging initial results. Radiology 223(2):566–573

    Article  PubMed  Google Scholar 

  38. Balu N, Wang J, Dong L, Baluyot F, Chen H, Yuan C (2009) Current techniques for MR imaging of atherosclerosis. Top Magn Reson Imaging 20(4):203–215. doi:10.1097/RMR.0b013e3181ea287d

    Article  PubMed  Google Scholar 

  39. Cai J, Hatsukami TS, Ferguson MS, Kerwin WS, Saam T, Chu B, Takaya N, Polissar NL, Yuan C (2005) In vivo quantitative measurement of intact fibrous cap and lipid-rich necrotic core size in atherosclerotic carotid plaque: comparison of high-resolution, contrast-enhanced magnetic resonance imaging and histology. Circulation 112(22):3437–3444. doi:10.1161/CIRCULATIONAHA.104.528174, CIRCULATIONAHA.104.528174 [pii]

    Article  PubMed  Google Scholar 

  40. Armitage FE, Richardson DE, Li KC (1990) Polymeric contrast agents for magnetic resonance imaging: synthesis and characterization of gadolinium diethylenetriaminepentaacetic acid conjugated to polysaccharides. Bioconjug Chem 1(6): 365–374

    Article  PubMed  CAS  Google Scholar 

  41. Flacke S, Fischer S, Scott MJ, Fuhrhop RJ, Allen JS, McLean M, Winter P et al (2001) Novel MRI contrast agent for molecular imaging of fibrin: implications for detecting vulnerable plaques. Circulation 104(11):1280–1285

    Article  PubMed  CAS  Google Scholar 

  42. Winter PM, Morawski AM, Caruthers SD, Fuhrhop RW, Zhang H, Williams TA, Allen JS et al (2003) Molecular imaging of angiogenesis in early-stage atherosclerosis with alpha(v)beta3-integrin-targeted nanoparticles. Circulation 108(18):2270–2274. doi:10.1161/01.CIR.0000093185.16083.95

    Article  PubMed  CAS  Google Scholar 

  43. Barkhausen J, Ebert W, Heyer C, Debatin JF, Weinmann HJ (2003) Detection of atherosclerotic plaque with Gadofluorine-enhanced magnetic resonance imaging. Circulation 108(5):605–609. doi:10.1161/01.CIR.0000079099.36306.10

    Article  PubMed  CAS  Google Scholar 

  44. Kerwin W, Xu D, Liu F, Saam T, Underhill H, Takaya N, Chu B, Hatsukami T, Yuan C (2007) Magnetic resonance imaging of carotid atherosclerosis: plaque analysis. Top Magn Reson Imaging 18(5):371–378. doi:10.1097/rmr.0b013e3181598d9d

    Article  PubMed  Google Scholar 

  45. Dong L, Kerwin WS, Ferguson MS, Li R, Wang J, Chen H, Canton G, Hatsukami TS, Yuan C (2009) Cardiovascular magnetic resonance in carotid atherosclerotic disease. J Cardiovasc Magn Reson 11:53. doi:10.1186/1532-429X-11-53, 1532-429X-11-53 [pii]

    Article  PubMed  Google Scholar 

  46. Kerwin WS, Yuan C (2001) Active edge maps for medical image registration. Proc SPIE 4322:4516–4526

    Google Scholar 

  47. Fei B, Suri JS, Wilson DL (2005) Three-dimensional volume registration of carotid MR images. Stud Health Technol Inform 113:394–411

    PubMed  Google Scholar 

  48. Chu B, Ferguson MS, Chen H, Hippe DS, Kerwin WS, Canton G, Yuan C, Hatsukami TS (2009) Magnetic [corrected] resonance imaging [corrected] features of the disruption-prone and the disrupted carotid plaque. JACC Cardiovasc Imaging 2(7):883–896. doi:10.1016/j.jcmg.2009.03.013, S1936-878X(09)00343-X [pii]

    Article  PubMed  Google Scholar 

  49. Greenland P, LaBree L, Azen SP, Doherty TM, Detrano RC (2004) Coronary artery calcium score combined with Framingham score for risk prediction in asymptomatic individuals. JAMA 291(2):210–215. doi:10.1001/jama.291.2.210

    Article  PubMed  CAS  Google Scholar 

  50. Ebrahim S, Papacosta O, Whincup P, Wannamethee G, Walker M, Nicolaides AN, Dhanjil S et al (1999) Carotid plaque, intima media thickness, cardiovascular risk factors, and prevalent cardiovascular disease in men and women: the British Regional Heart Study. Stroke 30(4):841–850

    Article  PubMed  CAS  Google Scholar 

  51. Glagov S, Weisenberg E, Zarins CK, Stankunavicius R, Kolettis GJ (1987) Compensatory enlargement of human atherosclerotic coronary arteries. N Engl J Med 316(22):1371–1375. doi:10.1056/NEJM198705283162204

    Article  PubMed  CAS  Google Scholar 

  52. Takaya N, Yuan C, Chu B, Saam T, Underhill H, Cai J, Tran N et al (2006) Association between carotid plaque characteristics and subsequent ischemic cerebrovascular events: a prospective assessment with MRI – initial results. Stroke 37(3):818–823. doi:10.1161/01.STR.0000204638.91099.91, 01.STR.000020463 8.91099.91 [pii]

    Article  PubMed  Google Scholar 

  53. Mani V, Muntner P, Gidding SS, Aguiar SH, El Aidi H, Weinshelbaum KB, Taniguchi H et al (2009) Cardiovascular magnetic resonance parameters of atherosclerotic plaque burden improve discrimination of prior major adverse cardiovascular events. J Cardiovasc Magn Reson 11:10. doi:10.1186/1532-429X- 11-10

    Article  PubMed  Google Scholar 

  54. Underhill HR, Kerwin WS, Hatsukami TS, Yuan C (2006) Automated measurement of mean wall thickness in the common carotid artery by MRI: a comparison to intima-media thickness by B-mode ultrasound. J Magn Reson Imaging 24(2):379–387. doi:10.1002/jmri.20636

    Article  PubMed  Google Scholar 

  55. Cao JJ, Thach C, Manolio TA, Psaty BM, Kuller LH, Chaves PH, Polak JF et al (2003) C-reactive protein, carotid intima-media thickness, and incidence of ischemic stroke in the elderly: the Cardiovascular Health Study. Circulation 108(2):166–170. doi:10.1161/01.CIR.0000079160.07364.6A

    Article  PubMed  CAS  Google Scholar 

  56. Zhao X, Underhill HR, Zhao Q, Cai J, Li F, Oikawa M, Dong L et al (2011) Discriminating carotid atherosclerotic lesion severity by luminal stenosis and plaque burden: a comparison utilizing high-resolution magnetic resonance imaging at 3.0 Tesla. Stroke 42(2):347–353. doi:10.1161/STROKEAHA.110.597328

    Article  PubMed  Google Scholar 

  57. Luo Y, Polissar N, Han C, Yarnykh V, Kerwin WS, Hatsukami TS, Yuan C (2003) Accuracy and uniqueness of three in vivo measurements of atherosclerotic carotid plaque morphology with black blood MRI. Magn Reson Med 50(1):75–82. doi:10.1002/mrm.10503

    Article  PubMed  Google Scholar 

  58. Yuan C, Beach KW, Smith LH Jr, Hatsukami TS (1998) Measurement of atherosclerotic carotid plaque size in vivo using high resolution magnetic resonance imaging. Circulation 98(24):2666–2671

    Article  PubMed  CAS  Google Scholar 

  59. Zhang S, Hatsukami TS, Polissar NL, Han C, Yuan C (2001) Comparison of carotid vessel wall area measurements using three different contrast-weighted black blood MR imaging techniques. Magn Reson Imaging 19(6):795–802, doi:S0730725X01004088 [pii]

    Article  PubMed  CAS  Google Scholar 

  60. Balu N, Chu B, Hatsukami TS, Yuan C, Yarnykh VL (2008) Comparison between 2D and 3D high-resolution black-blood techniques for carotid artery wall imaging in clinically significant atherosclerosis. J Magn Reson Imaging 27(4):918–924. doi:10.1002/jmri.21282

    Article  PubMed  Google Scholar 

  61. Saam T, Hatsukami TS, Yarnykh VL, Hayes CE, Underhill H, Chu B, Takaya N et al (2007) Reader and platform reproducibility for quantitative assessment of carotid atherosclerotic plaque using 1.5T Siemens, Philips, and General Electric scanners. J Magn Reson Imaging 26(2):344–352. doi:10.1002/jmri.21004

    Article  PubMed  Google Scholar 

  62. Duivenvoorden R, de Groot E, Elsen BM, Lameris JS, van der Geest RJ, Stroes ES, Kastelein JJ, Nederveen AJ (2009) In vivo quantification of carotid artery wall dimensions: 3.0-Tesla MRI versus B-mode ultrasound imaging. Circ Cardiovasc Imaging 2(3):235–242. doi:10.1161/CIRCIMAGING.108.788059

    Article  PubMed  CAS  Google Scholar 

  63. Alizadeh Dehnavi R, Doornbos J, Tamsma JT, Stuber M, Putter H, van der Geest RJ, Lamb HJ, de Roos A (2007) Assessment of the carotid artery by MRI at 3T: a study on reproducibility. J Magn Reson Imaging 25(5):1035–1043. doi:10.1002/jmri.20904

    Article  PubMed  Google Scholar 

  64. Saam T, Kerwin WS, Chu B, Cai J, Kampschulte A, Hatsukami TS, Zhao XQ et al (2005) Sample size calculation for clinical trials using magnetic resonance imaging for the quantitative assessment of carotid atherosclerosis. J Cardiovasc Magn Reson 7(5):799–808

    Article  PubMed  Google Scholar 

  65. Saam T, Raya JG, Cyran CC, Bochmann K, Meimarakis G, Dietrich O, Clevert DA et al (2009) High resolution carotid black-blood 3T MR with parallel imaging and dedicated 4-channel surface coils. J Cardiovasc Magn Reson 11:41. doi:10.1186/1532-429X-11-41, 1532-429X-11-41 [pii]

    Article  PubMed  Google Scholar 

  66. Toussaint JF, LaMuraglia GM, Southern JF, Fuster V, Kantor HL (1996) Magnetic resonance images lipid, fibrous, calcified, hemorrhagic, and thrombotic components of human atherosclerosis in vivo. Circulation 94(5):932–938

    Article  PubMed  CAS  Google Scholar 

  67. Hatsukami TS, Ross R, Polissar NL, Yuan C (2000) Visualization of fibrous cap thickness and rupture in human atherosclerotic carotid plaque in vivo with high-resolution magnetic resonance imaging. Circulation 102(9):959–964

    Article  PubMed  CAS  Google Scholar 

  68. Trivedi RA, U-King-Im J, Graves MJ, Horsley J, Goddard M, Kirkpatrick PJ, Gillard JH (2004) Multi-sequence in vivo MRI can quantify fibrous cap and lipid core components in human carotid atherosclerotic plaques. Eur J Vasc Endovasc Surg 28(2):207–213. doi:10.1016/j.ejvs.2004.05.001 S1078588404002199 [pii]

    PubMed  CAS  Google Scholar 

  69. Chu B, Kampschulte A, Ferguson MS, Kerwin WS, Yarnykh VL, O’Brien KD, Polissar NL, Hatsukami TS, Yuan C (2004) Hemorrhage in the atherosclerotic carotid plaque: a high-resolution MRI study. Stroke 35(5):1079–1084. doi:10.1161/01.STR.0000125856.25309.86 01.STR.000012585 6.25309.86 [pii]

    Article  PubMed  Google Scholar 

  70. Moody AR, Murphy RE, Morgan PS, Martel AL, Delay GS, Allder S, MacSweeney ST et al (2003) Characterization of complicated carotid plaque with magnetic resonance direct thrombus imaging in patients with cerebral ischemia. Circulation 107(24):3047–3052. doi:10.1161/01.CIR.0000074222.61572.44, 01.CIR.0000074222.61572.44 [pii]

    Article  PubMed  Google Scholar 

  71. Virmani R, Kolodgie FD, Burke AP, Finn AV, Gold HK, Tulenko TN, Wrenn SP, Narula J (2005) Atherosclerotic plaque progression and vulnerability to rupture: angiogenesis as a source of intraplaque hemorrhage. Arterioscler Thromb Vasc Biol 25(10):2054–2061. doi:10.1161/01.ATV.0000178991.71605.18

    Article  PubMed  CAS  Google Scholar 

  72. Davies MJ, Thomas AC (1985) Plaque fissuring – the cause of acute myocardial infarction, sudden ischaemic death, and crescendo angina. Br Heart J 53(4):363–373

    Article  PubMed  CAS  Google Scholar 

  73. Ota H, Yarnykh VL, Ferguson MS, Underhill HR, Demarco JK, Zhu DC, Oikawa M et al (2010) Carotid intraplaque hemorrhage imaging at 3.0-T MR imaging: comparison of the diagnostic performance of three T1-weighted sequences. Radiology 254(2):551–563. doi:10.1148/radiol.09090535, 254/2/551 [pii]

    Article  PubMed  Google Scholar 

  74. Wang J, Ferguson MS, Balu N, Yuan C, Hatsukami TS, Bornert P (2010) Improved carotid intraplaque hemorrhage imaging using a slab-selective phase-sensitive inversion-recovery (SPI) sequence. Magn Reson Med 64(5):1332–1340. doi:10.1002/mrm.22539

    Article  PubMed  Google Scholar 

  75. Arapoglou B, Kondi-Pafiti A, Katsenis K, Dimakakos P (1994) The clinical significance of carotid plaque haemorrhage. Int Angiol 13(4):323–326

    PubMed  CAS  Google Scholar 

  76. Ammar AD, Wilson RL, Travers H, Lin JJ, Farha SJ, Chang FC (1984) Intraplaque hemorrhage: its significance in cerebrovascular disease. Am J Surg 148(6):840–843

    Article  PubMed  CAS  Google Scholar 

  77. Altaf N, Daniels L, Morgan PS, Auer D, MacSweeney ST, Moody AR, Gladman JR (2008) Detection of intraplaque hemorrhage by magnetic resonance imaging in symptomatic patients with mild to moderate carotid stenosis predicts recurrent neurological events. J Vasc Surg 47(2):337–342. doi:10.1016/j.jvs.2007.09.064

    Article  PubMed  Google Scholar 

  78. Singh N, Moody AR, Gladstone DJ, Leung G, Ravikumar R, Zhan J, Maggisano R (2009) Moderate carotid artery stenosis: MR imaging-depicted intraplaque hemorrhage predicts risk of cerebrovascular ischemic events in asymptomatic men. Radiology 252(2):502–508. doi:10.1148/radiol.2522080792, 2522080792 [pii]

    Article  PubMed  Google Scholar 

  79. Saam T, Underhill HR, Chu B, Takaya N, Cai J, Polissar NL, Yuan C, Hatsukami TS (2008) 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 51(10):1014–1021. doi:10.1016/j.jacc.2007.10.054, S0735-1097(07)03882-X [pii]

    Article  PubMed  Google Scholar 

  80. Kolodgie FD, Gold HK, Burke AP, Fowler DR, Kruth HS, Weber DK, Farb A et al (2003) Intraplaque hemorrhage and progression of coronary atheroma. N Engl J Med 349(24):2316–2325. doi:10.1056/NEJMoa035655

    Article  PubMed  CAS  Google Scholar 

  81. Libby P (2002) Inflammation in atherosclerosis. Nature 420(6917):868–874. doi:10.1038/nature01323

    Article  PubMed  CAS  Google Scholar 

  82. Bornstein NM, Krajewski A, Lewis AJ, Norris JW (1990) Clinical significance of carotid plaque hemorrhage. Arch Neurol 47(9):958–959

    Article  PubMed  CAS  Google Scholar 

  83. Underhill HR, Yuan C, Yarnykh VL, Chu B, Oikawa M, Polissar NL, Schwartz SM, Jarvik GP, Hatsukami TS (2009) Arterial remodeling in [corrected] subclinical carotid artery disease. JACC Cardiovasc Imaging 2(12):1381–1389. doi:10.1016/j.jcmg.2009.08.007

    Article  PubMed  Google Scholar 

  84. Underhill HR, Hatsukami TS, Fayad ZA, Fuster V, Yuan C (2010) MRI of carotid atherosclerosis: clinical implications and future directions. Nat Rev Cardiol 7(3):165–173. doi:10.1038/nrcardio.2009.246, nrcardio.2009.246 [pii]

    Article  PubMed  Google Scholar 

  85. Takaya N, Yuan C, Chu B, Saam T, Polissar NL, Jarvik GP, Isaac C et al (2005) Presence of intraplaque hemorrhage stimulates progression of carotid atherosclerotic plaques: a high-resolution magnetic resonance imaging study. Circulation 111(21):2768–2775. doi:10.1161/CIRCULATIONAHA.104.504167, CIRCULATIONAHA.104.504167 [pii]

    Article  PubMed  Google Scholar 

  86. Teng Z, Sadat U, Huang Y, Young VE, Graves MJ, Lu J, Gillard JH (2011) In vivo MRI-based 3D mechanical stress–strain profiles of carotid plaques with juxtaluminal plaque haemorrhage: an exploratory study for the mechanism of subsequent cerebrovascular events. Eur J Vasc Endovasc Surg 42(4):427–433. doi:10.1016/j.ejvs.2011.05.009

    Article  PubMed  CAS  Google Scholar 

  87. Toussaint JF, Southern JF, Fuster V, Kantor HL (1997) Water diffusion properties of human atherosclerosis and thrombosis measured by pulse field gradient nuclear magnetic resonance. Arterioscler Thromb Vasc Biol 17(3):542–546

    Article  PubMed  CAS  Google Scholar 

  88. Kampschulte A, Ferguson MS, Kerwin WS, Polissar NL, Chu B, Saam T, Hatsukami TS, Yuan C (2004) Differentiation of intraplaque versus juxtaluminal hemorrhage/thrombus in advanced human carotid atherosclerotic lesions by in vivo magnetic resonance imaging. Circulation 110(20):3239–3244. doi:10.1161/01.CIR.0000147287.23741.9A, 01.CIR.0000147287.23741.9A [pii]

    Article  PubMed  CAS  Google Scholar 

  89. Saam T, Cai J, Ma L, Cai YQ, Ferguson MS, Polissar NL, Hatsukami TS, Yuan C (2006) Comparison of symptomatic and asymptomatic atherosclerotic carotid plaque features with in vivo MR imaging. Radiology 240(2):464–472. doi:10.1148/radiol.2402050390, 240/2/464 [pii]

    Article  PubMed  Google Scholar 

  90. Stary HC, Chandler AB, Dinsmore RE, Fuster V, Glagov S, Insull W Jr, Rosenfeld ME, Schwartz CJ, Wagner WD, Wissler RW (1995) 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 15(9):1512–1531

    Article  PubMed  CAS  Google Scholar 

  91. Underhill HR, Yuan C, Yarnykh VL, Chu B, Oikawa M, Dong L, Polissar NL, Garden GA, Cramer SC, Hatsukami TS (2010) Predictors of surface disruption with MR imaging in asymptomatic carotid artery stenosis. AJNR Am J Neuroradiol 31(3):487–493. doi:10.3174/ajnr.A1842, ajnr.A1842 [pii]

    Article  PubMed  CAS  Google Scholar 

  92. Toussaint JF, Southern JF, Fuster V, Kantor HL (1995) T2-weighted contrast for NMR characterization of human atherosclerosis. Arterioscler Thromb Vasc Biol 15(10):1533–1542

    PubMed  CAS  Google Scholar 

  93. Fabiano S, Mancino S, Stefanini M, Chiocchi M, Mauriello A, Spagnoli LG, Simonetti G (2008) High-resolution multicontrast-weighted MR imaging from human carotid endarterectomy specimens to assess carotid plaque components. Eur Radiol 18(12):2912–2921. doi:10.1007/s00330-008-1091-x

    Article  PubMed  Google Scholar 

  94. Shinnar M, Fallon JT, Wehrli S, Levin M, Dalmacy D, Fayad ZA, Badimon JJ, Harrington M, Harrington E, Fuster V (1999) The diagnostic accuracy of ex vivo MRI for human atherosclerotic plaque characterization. Arterioscler Thromb Vasc Biol 19(11):2756–2761

    Article  PubMed  CAS  Google Scholar 

  95. Yuan C, Kerwin WS, Ferguson MS, Polissar N, Zhang S, Cai J, Hatsukami TS (2002) Contrast-enhanced high resolution MRI for atherosclerotic carotid artery tissue characterization. J Magn Reson Imaging 15(1):62–67. doi:10.1002/jmri.10030 [pii]

    Article  PubMed  Google Scholar 

  96. Berliner JA, Navab M, Fogelman AM, Frank JS, Demer LL, Edwards PA, Watson AD, Lusis AJ (1995) Atherosclerosis: basic mechanisms. Oxidation, inflammation, and genetics. Circulation 91(9):2488–2496

    Article  PubMed  CAS  Google Scholar 

  97. Mauriello A, Servadei F, Sangiorgi G, Anemona L, Giacobbi E, Liotti D, Spagnoli LG (2011) Asymptomatic carotid plaque rupture with unexpected thrombosis over a non-canonical vulnerable lesion. Atherosclerosis 218(2):356–362. doi:10.1016/j.atherosclerosis.2011.06.056

    Article  PubMed  CAS  Google Scholar 

  98. Yuan C, Zhang SX, Polissar NL, Echelard D, Ortiz G, Davis JW, Ellington E, Ferguson MS, Hatsukami TS (2002) Identification of fibrous cap rupture with magnetic resonance imaging is highly associated with recent transient ischemic attack or stroke. Circulation 105(2):181–185

    Article  PubMed  Google Scholar 

  99. Redgrave JN, Gallagher P, Lovett JK, Rothwell PM (2008) Critical cap thickness and rupture in symptomatic carotid plaques: the oxford plaque study. Stroke 39(6):1722–1729. doi:10.1161/STROKEAHA.107.507988, STROKEAHA.107.507988 [pii]

    Article  PubMed  Google Scholar 

  100. Mitsumori LM, Hatsukami TS, Ferguson MS, Kerwin WS, Cai J, Yuan C (2003) In vivo accuracy of multisequence MR imaging for identifying unstable fibrous caps in advanced human carotid plaques. J Magn Reson Imaging 17(4):410–420. doi:10.1002/jmri.10264

    Article  PubMed  Google Scholar 

  101. Kwee RM, van Engelshoven JM, Mess WH, ter Berg JW, Schreuder FH, Franke CL, Korten AG et al (2009) Reproducibility of fibrous cap status assessment of carotid artery plaques by contrast-enhanced MRI. Stroke 40(9):3017–3021. doi:10.1161/STROKEAHA.109.555052, STROKEAHA.109.555052 [pii]

    Article  PubMed  Google Scholar 

  102. Schmermund A, Erbel R (2001) Unstable coronary plaque and its relation to coronary calcium. Circulation 104(14):1682–1687

    Article  PubMed  CAS  Google Scholar 

  103. Huang H, Virmani R, Younis H, Burke AP, Kamm RD, Lee RT (2001) The impact of calcification on the biomechanical stability of atherosclerotic plaques. Circulation 103(8):1051–1056

    Article  PubMed  CAS  Google Scholar 

  104. Kwee RM (2010) Systematic review on the association between calcification in carotid plaques and clinical ischemic symptoms. J Vasc Surg 51(4):1015–1025. doi:10.1016/j.jvs.2009.08.072, S0741-5214(09)01788-1 [pii]

    Article  PubMed  Google Scholar 

  105. Li ZY, Howarth S, Tang T, Graves M, U-King-Im J, Gillard JH (2007) Does calcium deposition play a role in the stability of atheroma? Location may be the key. Cerebrovasc Dis 24(5):452–459. doi:10.1159/000108436

    Article  PubMed  Google Scholar 

  106. Deguchi JO, Aikawa M, Tung CH, Aikawa E, Kim DE, Ntziachristos V, Weissleder R, Libby P (2006) Inflammation in atherosclerosis: visualizing matrix metalloproteinase action in macrophages in vivo. Circulation 114(1):55–62. doi:10.1161/CIRCULATIONAHA.106.619056

    Article  PubMed  Google Scholar 

  107. Jeziorska M, Woolley DE (1999) Local neovascularization and cellular composition within vulnerable regions of atherosclerotic plaques of human carotid arteries. J Pathol 188(2):189–196. doi:10.1002/(SICI)1096-9896(199906)188:2<189::AID-PATH33 6>3.0.CO;2-N

    Article  PubMed  CAS  Google Scholar 

  108. Milei J, Parodi JC, Alonso GF, Barone A, Grana D, Matturri L (1998) Carotid rupture and intraplaque hemorrhage: immunophenotype and role of cells involved. Am Heart J 136(6):1096–1105

    Article  PubMed  CAS  Google Scholar 

  109. Papini GD, Di Leo G, Tritella S, Nano G, Cotticelli B, Clemente C, Tealdi DG, Sardanelli F (2011) Evaluation of inflammatory status of atherosclerotic carotid plaque before thromboendarterectomy using delayed contrast-enhanced subtracted images after magnetic resonance angiography. Eur J Radiol 80(3):e373–e380. doi:10.1016/j.ejrad.2011.01.029

    Article  PubMed  Google Scholar 

  110. Tang TY, Howarth SP, Miller SR, Graves MJ, U-King-Im JM, Li ZY, Walsh SR, Hayes PD, Varty K, Gillard JH (2008) Comparison of the inflammatory burden of truly asymptomatic carotid atheroma with atherosclerotic plaques in patients with asymptomatic carotid stenosis undergoing coronary artery bypass grafting: an ultrasmall superparamagnetic iron oxide enhanced magnetic resonance study. Eur J Vasc Endovasc Surg 35(4):392–398. doi:10.1016/j.ejvs.2007.10.019, S1078-5884(07)00683-1 [pii]

    Article  PubMed  CAS  Google Scholar 

  111. Moreno PR, Purushothaman KR, Sirol M, Levy AP, Fuster V (2006) Neovascularization in human atherosclerosis. Circulation 113(18):2245–2252. doi:10.1161/CIRCULATIONAHA.105.578955

    Article  PubMed  Google Scholar 

  112. Calcagno C, Mani V, Ramachandran S, Fayad ZA (2010) Dynamic contrast enhanced (DCE) magnetic resonance imaging (MRI) of atherosclerotic plaque angiogenesis. Angiogenesis 13(2):87–99. doi:10.1007/s10456-010-9172-2

    Article  PubMed  Google Scholar 

  113. Moreno PR, Purushothaman KR, Fuster V, Echeverri D, Truszczynska H, Sharma SK, Badimon JJ, O’Connor WN (2004) Plaque neovascularization is increased in ruptured atherosclerotic lesions of human aorta: implications for plaque vulnerability. Circulation 110(14):2032–2038. doi:10.1161/01.CIR.0000143233.87854.23

    Article  PubMed  Google Scholar 

  114. Mofidi R, Crotty TB, McCarthy P, Sheehan SJ, Mehigan D, Keaveny TV (2001) Association between plaque instability, angiogenesis and symptomatic carotid occlusive disease. Br J Surg 88(7):945–950. doi:10.1046/j.0007-1323.2001.01823.x

    Article  PubMed  CAS  Google Scholar 

  115. Kerwin WS, O’Brien KD, Ferguson MS, Polissar N, Hatsukami TS, Yuan C (2006) Inflammation in carotid atherosclerotic plaque: a dynamic contrast-enhanced MR imaging study. Radiology 241(2):459–468. doi:10.1148/radiol.2412051336

    Article  PubMed  Google Scholar 

  116. Choudhury RP, Fuster V, Fayad ZA (2004) Molecular, cellular and functional imaging of atherothrombosis. Nat Rev Drug Discov 3(11):913–925. doi:10.1038/nrd1548

    Article  PubMed  CAS  Google Scholar 

  117. Griffioen AW, Molema G (2000) Angiogenesis: potentials for pharmacologic intervention in the treatment of cancer, cardiovascular diseases, and chronic inflammation. Pharmacol Rev 52(2):237–268

    PubMed  CAS  Google Scholar 

  118. Choyke PL, Dwyer AJ, Knopp MV (2003) Functional tumor imaging with dynamic contrast-enhanced magnetic resonance imaging. J Magn Reson Imaging 17(5):509–520. doi:10.1002/jmri.10304

    Article  PubMed  Google Scholar 

  119. Kerwin WS, Oikawa M, Yuan C, Jarvik GP, Hatsukami TS (2008) MR imaging of adventitial vasa vasorum in carotid atherosclerosis. Magn Reson Med 59(3):507–514. doi:10.1002/mrm.21532

    Article  PubMed  CAS  Google Scholar 

  120. Yankeelov TE, Gore JC (2009) Dynamic contrast enhanced magnetic resonance imaging in oncology: theory, data acquisition, analysis, and examples. Curr Med Imaging Rev 3(2):91–107. doi:10.2174/157340507780619179

    Article  PubMed  Google Scholar 

  121. Kerwin W, Hooker A, Spilker M, Vicini P, Ferguson M, Hatsukami T, Yuan C (2003) Quantitative magnetic resonance imaging analysis of neovasculature volume in carotid atherosclerotic plaque. Circulation 107(6):851–856

    Article  PubMed  Google Scholar 

  122. Walker-Samuel S, Leach MO, Collins DJ (2006) Evaluation of response to treatment using DCE-MRI: the relationship between initial area under the gadolinium curve (IAUGC) and quantitative pharmacokinetic analysis. Phys Med Biol 51(14):3593–3602. doi:10.1088/0031-9155/51/14/021

    Article  PubMed  CAS  Google Scholar 

  123. Dong L, Kerwin WS, Chen H, Chu B, Underhill HR, Neradilek MB, Hatsukami TS, Yuan C, Zhao XQ (2011) Carotid artery atherosclerosis: effect of intensive lipid therapy on the vasa vasorum – evaluation by using dynamic contrast-enhanced MR imaging. Radiology 260(1):224–231. doi:10.1148/radiol.11101264, radiol.11101264 [pii]

    Article  PubMed  Google Scholar 

  124. Trivedi RA, Mallawarachi C, U-King-Im JM, Graves MJ, Horsley J, Goddard MJ, Brown A et al (2006) Identifying inflamed carotid plaques using in vivo USPIO-enhanced MR imaging to label plaque macrophages. Arterioscler Thromb Vasc Biol 26(7):1601–1606. doi:10.1161/01.ATV.0000222920.59760.df, 01.ATV.0000222920.59760.df [pii]

    Article  PubMed  CAS  Google Scholar 

  125. Tang TY, Muller KH, Graves MJ, Li ZY, Walsh SR, Young V, Sadat U, Howarth SP, Gillard JH (2009) Iron oxide particles for atheroma imaging. Arterioscler Thromb Vasc Biol 29(7):1001–1008. doi:10.1161/ATVBAHA.108.165514, ATVBAHA.108.165514 [pii]

    Article  PubMed  CAS  Google Scholar 

  126. Trivedi RA, U-King-Im JM, Graves MJ, Cross JJ, Horsley J, Goddard MJ, Skepper JN et al (2004) In vivo detection of macrophages in human carotid atheroma: temporal dependence of ultrasmall superparamagnetic particles of iron oxide-enhanced MRI. Stroke 35(7):1631–1635. doi:10.1161/01.STR.0000131268.50418.b7

    Article  PubMed  Google Scholar 

  127. Winter PM, Caruthers SD, Yu X, Song SK, Chen J, Miller B, Bulte JW et al (2003) Improved molecular imaging contrast agent for detection of human thrombus. Magn Reson Med 50(2):411–416. doi:10.1002/mrm.10532

    Article  PubMed  CAS  Google Scholar 

  128. Rausch M, Hiestand P, Baumann D, Cannet C, Rudin M (2003) MRI-based monitoring of inflammation and tissue damage in acute and chronic relapsing EAE. Magn Reson Med 50(2):309–314. doi:10.1002/mrm.10541

    Article  PubMed  CAS  Google Scholar 

  129. Ruehm SG, Corot C, Vogt P, Kolb S, Debatin JF (2001) Magnetic resonance imaging of atherosclerotic plaque with ultrasmall superparamagnetic particles of iron oxide in hyperlipidemic rabbits. Circulation 103(3):415–422

    Article  PubMed  CAS  Google Scholar 

  130. Kooi ME, Cappendijk VC, Cleutjens KB, Kessels AG, Kitslaar PJ, Borgers M, Frederik PM, Daemen MJ, van Engelshoven JM (2003) Accumulation of ultrasmall superparamagnetic particles of iron oxide in human atherosclerotic plaques can be detected by in vivo magnetic resonance imaging. Circulation 107(19):2453–2458. doi:10.1161/01.CIR.0000068315.98705.CC

    Article  PubMed  CAS  Google Scholar 

  131. Tang TY, Howarth SP, Miller SR, Graves MJ, U-King-Im JM, Trivedi RA, Li ZY et al (2007) 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 78(12):1337–1343. doi:10.1136/jnnp.2007.118901

    Article  PubMed  Google Scholar 

  132. Ku DN, Giddens DP, Zarins CK, Glagov S (1985) Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress. Arteriosclerosis 5(3):293–302

    Article  PubMed  CAS  Google Scholar 

  133. Steinman DA, Thomas JB, Ladak HM, Milner JS, Rutt BK, Spence JD (2002) Reconstruction of carotid bifurcation hemodynamics and wall thickness using computational fluid dynamics and MRI. Magn Reson Med 47(1):149–159

    Article  PubMed  Google Scholar 

  134. Kerwin WS, Canton G (2009) Advanced techniques for MRI of atherosclerotic plaque. Top Magn Reson Imaging 20(4):217–225. doi:10.1097/RMR.0b013e3181ea285300002142-200908000-00002 [pii]

    Article  PubMed  Google Scholar 

  135. Gnasso A, Irace C, Carallo C, De Franceschi MS, Motti C, Mattioli PL, Pujia A (1997) In vivo association between low wall shear stress and plaque in subjects with asymmetrical carotid atherosclerosis. Stroke 28(5):993–998

    Article  PubMed  CAS  Google Scholar 

  136. Lovett JK, Rothwell PM (2003) Site of carotid plaque ulceration in relation to direction of blood flow: an angiographic and pathological study. Cerebrovasc Dis 16(4):369–375. doi:10.1159/000072559

    Article  PubMed  Google Scholar 

  137. Malek AM, Alper SL, Izumo S (1999) Hemodynamic shear stress and its role in atherosclerosis. JAMA 282(21):2035–2042

    Article  PubMed  CAS  Google Scholar 

  138. Cheng C, Tempel D, van Haperen R, van der Baan A, Grosveld F, Daemen MJ, Krams R, de Crom R (2006) Atherosclerotic lesion size and vulnerability are determined by patterns of fluid shear stress. Circulation 113(23):2744–2753. doi:10.1161/CIRCULATIONAHA.105.590018

    Article  PubMed  Google Scholar 

  139. Richardson PD, Davies MJ, Born GV (1989) Influence of plaque configuration and stress distribution on fissuring of coronary atherosclerotic plaques. Lancet 2(8669):941–944

    Article  PubMed  CAS  Google Scholar 

  140. Cheng GC, Loree HM, Kamm RD, Fishbein MC, Lee RT (1993) Distribution of circumferential stress in ruptured and stable atherosclerotic lesions. A structural analysis with histopathological correlation. Circulation 87(4):1179–1187

    Article  PubMed  CAS  Google Scholar 

  141. Tang D, Yang C, Kobayashi S, Zheng J, Woodard PK, Teng Z, Billiar K, Bach R, Ku DN (2009) 3D MRI-based anisotropic FSI models with cyclic bending for human coronary atherosclerotic plaque mechanical analysis. J Biomech Eng 131(6):061010. doi:10.1115/1.3127253

    Article  PubMed  Google Scholar 

  142. Li ZY, Howarth S, Trivedi RA, U-King-Im JM, Graves MJ, Brown A, Wang L, Gillard JH (2006) Stress analysis of carotid plaque rupture based on in vivo high resolution MRI. J Biomech 39(14):2611–2622. doi:10.1016/j.jbiomech.2005.08.022

    Article  PubMed  Google Scholar 

  143. Loree HM, Kamm RD, Stringfellow RG, Lee RT (1992) Effects of fibrous cap thickness on peak circumferential stress in model atherosclerotic vessels. Circ Res 71(4):850–858

    Article  PubMed  CAS  Google Scholar 

  144. Vengrenyuk Y, Carlier S, Xanthos S, Cardoso L, Ganatos P, Virmani R, Einav S, Gilchrist L, Weinbaum S (2006) A hypothesis for vulnerable plaque rupture due to stress-induced debonding around cellular microcalcifications in thin fibrous caps. Proc Natl Acad Sci USA 103(40):14678–14683. doi:10.1073/pnas.0606310103

    Article  PubMed  CAS  Google Scholar 

  145. Yang C, Canton G, Yuan C, Ferguson M, Hatsukami TS, Tang D (2011) Impact of flow rates in a cardiac cycle on correlations between advanced human carotid plaque progression and mechanical flow shear stress and plaque wall stress. Biomed Eng Online 10(1):61. doi:10.1186/1475-925X-10-61

    Article  PubMed  Google Scholar 

  146. Teng Z, Canton G, Yuan C, Ferguson M, Yang C, Huang X, Zheng J, Woodard PK, Tang D (2010) 3D Critical plaque wall stress is a better predictor of carotid plaque rupture sites than flow shear stress: an in vivo MRI-based 3D FSI study. J Biomech Eng 132(3):031007. doi:10.1115/1.4001028

    Article  PubMed  Google Scholar 

  147. Gao H, Long Q, Das SK, Sadat U, Graves M, Gillard JH, Li ZY (2011) Stress analysis of carotid atheroma in transient ischemic attack patients: evidence for extreme stress-induced plaque rupture. Ann Biomed Eng 39(8):2203–2212. doi:10.1007/s10439-011-0314-5

    Article  PubMed  Google Scholar 

  148. Zhu C, Teng Z, Sadat U, Young VE, Graves MJ, Li ZY, Gillard JH (2010) Normalized wall index specific and MRI-based stress analysis of atherosclerotic carotid plaques: a study comparing acutely symptomatic and asymptomatic patients. Circ J 74(11):2360–2364

    Article  PubMed  Google Scholar 

  149. Sadat U, Teng Z, Young VE, Zhu C, Tang TY, Graves MJ, Gillard JH (2011) Impact of plaque haemorrhage and its age on structural stresses in atherosclerotic plaques of patients with carotid artery disease: an MR imaging-based finite element simulation study. Int J Cardiovasc Imaging 27(3):397–402. doi:10.1007/s10554-010-9679-z

    Article  PubMed  Google Scholar 

  150. Teng Z, Sadat U, Ji G, Zhu C, Young VE, Graves MJ, Gillard JH (2011) Lumen irregularity dominates the relationship between mechanical stress condition, fibrous-cap thickness, and lumen curvature in carotid atherosclerotic plaque. J Biomech Eng 133(3):034501. doi:10.1115/1.4003439

    Article  PubMed  Google Scholar 

  151. Syed MA, Oshinski JN, Kitchen C, Ali A, Charnigo RJ, Quyyumi AA (2009) Variability of carotid artery measurements on 3-Tesla MRI and its impact on sample size calculation for clinical research. Int J Cardiovasc Imaging 25(6):581–589. doi:10.1007/s10554-009-9468-8

    Article  PubMed  Google Scholar 

  152. (1998) Prevention of cardiovascular events and death with pravastatin in patients with coronary heart disease and a broad range of initial cholesterol levels. The Long-Term Intervention with Pravastatin in Ischaemic Disease (LIPID) Study Group. N Engl J Med 339(19):1349–1357. doi:10.1056/NEJM199811053391902

  153. Libby P, Aikawa M (2003) Mechanisms of plaque stabilization with statins. Am J Cardiol 91(4A):4B–8B

    Article  PubMed  CAS  Google Scholar 

  154. Duivenvoorden R, de Groot E, Stroes ES, Kastelein JJ (2009) Surrogate markers in clinical trials – challenges and opportunities. Atherosclerosis 206(1):8–16. doi:10.1016/j.atherosclerosis.2008.12.009, S0021-9150(08)00899-X [pii]

    Article  PubMed  CAS  Google Scholar 

  155. Zhao XQ, Yuan C, Hatsukami TS, Frechette EH, Kang XJ, Maravilla KR, Brown BG (2001) Effects of prolonged intensive lipid-lowering therapy on the characteristics of carotid atherosclerotic plaques in vivo by MRI: a case–control study. Arterioscler Thromb Vasc Biol 21(10):1623–1629

    Article  PubMed  CAS  Google Scholar 

  156. Saam T, Yuan C, Chu B, Takaya N, Underhill H, Cai J, Tran N et al (2007) Predictors of carotid atherosclerotic plaque progression as measured by noninvasive magnetic resonance imaging. Atherosclerosis 194(2):e34–e42. doi:10.1016/j.atherosclerosis.2006.08.016

    Article  PubMed  CAS  Google Scholar 

  157. Kwee RM, van Oostenbrugge RJ, Mess WH, Prins MH, van der Geest RJ, ter Berg JW, Franke CL et al (2010) Carotid plaques in transient ischemic attack and stroke patients: one-year follow-up study by magnetic resonance imaging. Invest Radiol 45(12):803–809. doi:10.1097/RLI.0b013e3181ed15ff

    Article  PubMed  Google Scholar 

  158. Corti R, Fayad ZA, Fuster V, Worthley SG, Helft G, Chesebro J, Mercuri M, Badimon JJ (2001) Effects of lipid-lowering by simvastatin on human atherosclerotic lesions: a longitudinal study by high-resolution, noninvasive magnetic resonance imaging. Circulation 104(3):249–252

    Article  PubMed  CAS  Google Scholar 

  159. Corti R, Fuster V, Fayad ZA, Worthley SG, Helft G, Smith D, Weinberger J et al (2002) Lipid lowering by simvastatin induces regression of human atherosclerotic lesions: two years’ follow-up by high-resolution noninvasive magnetic resonance imaging. Circulation 106(23):2884–2887

    Article  PubMed  CAS  Google Scholar 

  160. Underhill HR, Yuan C, Zhao XQ, Kraiss LW, Parker DL, Saam T, Chu B et al (2008) Effect of rosuvastatin therapy on carotid plaque morphology and composition in moderately hypercholesterolemic patients: a high-resolution magnetic resonance imaging trial. Am Heart J 155(3):584.e581–584.e588. doi:10.1016/j.ahj.2007.11.018

    Article  CAS  Google Scholar 

  161. Zhao XQ, Phan BA, Chu B, Bray F, Moore AB, Polissar NL, Dodge JT Jr, Lee CD, Hatsukami TS, Yuan C (2007) Testing the hypothesis of atherosclerotic plaque lipid depletion during lipid therapy by magnetic resonance imaging: study design of carotid plaque composition study. Am Heart J 154(2):239–246. doi:10.1016/j.ahj.2007.04.035

    Article  PubMed  CAS  Google Scholar 

  162. Zhao XQ, Dong L, Hatsukami T, Phan BA, Chu B, Moore A, Lane T et al (2011) MR imaging of carotid plaque composition during lipid-lowering therapy a prospective assessment of effect and time course. JACC Cardiovasc Imaging 4(9):977–986. doi:10.1016/j.jcmg.2011.06.013

    Article  PubMed  Google Scholar 

  163. Migrino RQ, Bowers M, Harmann L, Prost R, Ladisa JF (2011) Carotid plaque regression following 6-month statin therapy assessed by 3T cardiovascular magnetic resonance: comparison with ultrasound intima media thickness. J Cardiovasc Magn Reson 13(1):37. doi:10.1186/1532-429X-13-37

    Article  PubMed  Google Scholar 

  164. Tang TY, Howarth SP, Miller SR, Graves MJ, Patterson AJ, U-King-Im JM, Li ZY et al (2009) The ATHEROMA (Atorvastatin therapy: effects on reduction of macrophage activity) study. Evaluation using ultrasmall superparamagnetic iron oxide-enhanced magnetic resonance imaging in carotid disease. J Am Coll Cardiol 53(22):2039–2050. doi:10.1016/j.jacc.2009.03.018

    Article  PubMed  CAS  Google Scholar 

  165. Patterson AJ, Tang TY, Graves MJ, Muller KH, Gillard JH (2011) In vivo carotid plaque MRI using quantitative T2* measurements with ultrasmall superparamagnetic iron oxide particles: a dose–response study to statin therapy. NMR Biomed 24(1):89–95. doi:10.1002/nbm.1560

    Article  PubMed  Google Scholar 

  166. Chu B, Zhao XQ, Saam T, Yarnykh VL, Kerwin WS, Flemming KD, Huston J 3rd et al (2005) Feasibility of in vivo, multicontrast-weighted MR imaging of carotid atherosclerosis for multicenter studies. J Magn Reson Imaging 21(6):809–817. doi:10.1002/jmri.20308

    Article  PubMed  Google Scholar 

  167. Underhill HR, Hatsukami TS, Cai J, Yu W, DeMarco JK, Polissar NL, Ota H et al (2010) A noninvasive imaging approach to assess plaque severity: the carotid atherosclerosis score. AJNR Am J Neuroradiol 31(6):1068–1075. doi:10.3174/ajnr.A2007, ajnr.A2007 [pii]

    Article  PubMed  CAS  Google Scholar 

  168. Macedo R, Chen S, Lai S, Shea S, Malayeri AA, Szklo M, Lima JA, Bluemke DA (2008) MRI detects increased coronary wall thickness in asymptomatic individuals: the multi-ethnic study of atherosclerosis (MESA). J Magn Reson Imaging 28(5):1108–1115. doi:10.1002/jmri.21511

    Article  PubMed  Google Scholar 

  169. Wasserman BA, Sharrett AR, Lai S, Gomes AS, Cushman M, Folsom AR, Bild DE, Kronmal RA, Sinha S, Bluemke DA (2008) 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 39(2):329–335. doi:10.1161/STROKEAHA.107.498634, STROKEAHA.107.498634 [pii]

    Article  PubMed  Google Scholar 

  170. Maderwald S, Ladd SC, Gizewski ER, Kraff O, Theysohn JM, Wicklow K, Moenninghoff C, Wanke I, Ladd ME, Quick HH (2008) To TOF or not to TOF: strategies for non-contrast-enhanced intracranial MRA at 7T. MAGMA 21(1–2):159–167. doi:10.1007/s10334-007-0096-9

    Article  PubMed  Google Scholar 

  171. Rominger A, Saam T, Wolpers S, Cyran CC, Schmidt M, Foerster S, Nikolaou K, Reiser MF, Bartenstein P, Hacker M (2009) 18F-FDG PET/CT identifies patients at risk for future vascular events in an otherwise asymptomatic cohort with neoplastic disease. J Nucl Med 50(10):1611–1620. doi:10.2967/jnumed.109.065151

    Article  PubMed  Google Scholar 

  172. Rudd JH, Warburton EA, Fryer TD, Jones HA, Clark JC, Antoun N, Johnstrom P et al (2002) Imaging atherosclerotic plaque inflammation with [18F]-fluorodeoxyglucose positron emission tomography. Circulation 105(23):2708–2711

    Article  PubMed  CAS  Google Scholar 

  173. Hadley JR, Roberts JA, Goodrich KC, Buswell HR, Parker DL (2005) Relative RF coil performance in carotid imaging. Magn Reson Imaging 23(5):629–639. doi:10.1016/j.mri.2005.04.009

    Article  PubMed  Google Scholar 

  174. Balu N, Yarnykh VL, Scholnick J, Chu B, Yuan C, Hayes C (2009) Improvements in carotid plaque imaging using a new eight-element phased array coil at 3T. J Magn Reson Imaging 30(5):1209–1214. doi:10.1002/jmri.21890

    Article  PubMed  Google Scholar 

  175. Boussel L, Herigault G, de la Vega A, Nonent M, Douek PC, Serfaty JM (2006) Swallowing, arterial pulsation, and breathing induce motion artifacts in carotid artery MRI. J Magn Reson Imaging 23(3):413–415. doi:10.1002/jmri.20525

    Article  PubMed  Google Scholar 

  176. Crowe LA, Keegan J, Gatehouse PD, Mohiaddin RH, Varghese A, Symmonds K, Cannell TM, Yang GZ, Firmin DN (2005) 3D volume-selective turbo spin echo for carotid artery wall imaging with navigator detection of swallowing. J Magn Reson Imaging 22(4):583–588. doi:10.1002/jmri.20424

    Article  PubMed  Google Scholar 

  177. Chan CF, Gatehouse PD, Hughes R, Roughton M, Pennell DJ, Firmin DN (2009) Novel technique used to detect swallowing in volume-selective turbo spin-echo (TSE) for carotid artery wall imaging. J Magn Reson Imaging 29(1):211–216. doi:10.1002/jmri.21607

    Article  PubMed  Google Scholar 

  178. Boussel L, Arora S, Rapp J, Rutt B, Huston J, Parker D, Yuan C, Bassiouny H, Saloner D (2009) Atherosclerotic plaque progression in carotid arteries: monitoring with high-spatial-resolution MR imaging – multicenter trial. Radiology 252(3):789–796. doi:10.1148/radiol.2523081798

    Article  PubMed  Google Scholar 

  179. Parmar JP, Rogers WJ, Mugler JP 3rd, Baskurt E, Altes TA, Nandalur KR, Stukenborg GJ et al (2010) Magnetic resonance imaging of carotid atherosclerotic plaque in clinically suspected acute transient ischemic attack and acute ischemic stroke. Circulation 122(20):2031–2038. doi:10.1161/CIRCULATIONAHA.109.866053

    Article  PubMed  Google Scholar 

  180. Saam T, Underhill HR, Chu B, Takaya N, Cai J, Polissar NL, Yuan C, Hatsukami TS (2008) 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 51(10):1014–1021. doi:10.1016/j.jacc.2007.10.054

    Article  PubMed  Google Scholar 

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Schindler, A., Saam, T. (2014). Quantitative MR Analysis for the Assessment of Carotid Atherosclerosis. In: Saba, L., Sanches, J., Pedro, L., Suri, J. (eds) Multi-Modality Atherosclerosis Imaging and Diagnosis. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-7425-8_4

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