European Radiology

, Volume 26, Issue 10, pp 3737–3743 | Cite as

Diffusion measurement of intraplaque hemorrhage and intramural hematoma using diffusion weighted MRI at 3T in cervical artery

  • Bin Yao
  • Li Yang
  • Guangbin Wang
  • Honglu Shi
  • Shanshan Wang
  • Huihua Li
  • Weibo Chen
  • Queenie Chan
Magnetic Resonance



To assess the difference between carotid haemorrhagic plaque and non-haemorrhagic plaque by using diffusion-weighted imaging (DWI) and to evaluate carotid intraplaque haemorrhage (IPH) and intramural hematoma (IMH) of cervical artery dissection with apparent diffusion coefficient (ADC) measurement.


Fifty-one symptomatic patients underwent 3.0-T carotid MR imaging, including conventional sequences, three-dimensional (3D) magnetization-prepared rapid acquisition gradient-echo (MPRAGE) sequence, and DWI. Thirty-nine patients with carotid plaque and eight patients with IMH of cervical artery dissection were finally included. The groups of hemorrhagic plaque, non-hemorrhagic plaque and IMH were divided according to 3D MPRAGE sequence. ADC values of different groups were measured, and t tests were performed.


The mean ADC values of hemorrhagic plaques, non-hemorrhagic plaque and IMH were (1.284 ± 0.327) × 10-3mm2/s, (1.766 ± 0.477) × 10-3mm2/s, and (0.563 ± 0.119) × 10-3mm2/s, respectively. The mean ADC values of hemorrhagic and non-hemorrhagic regions in the hemorrhagic plaque group were (0.985 ± 0.376) × 10-3mm2/s and (1.480 ± 0.465) × 10-3mm2/s, respectively. The differences between the hemorrhagic plaque and non-hemorrhagic plaque, hemorrhagic region and non-hemorrhagic region in hemorrhagic plaque, and the hemorrhagic region in the hemorrhagic plaque and IMH of artery dissection were significant (P < 0.05).


DWI may be a useful complement to conventional MR imaging for identifying haemorrhage of carotid plaques and differentiate IMHs from IPH.

Key Points

ADC values of IPH are lower than the plaque without IPH.

DWI might be a useful complement to identify IPH.

IMH may be differentiated from IPH by using DWI.


MRI Diffusion-weighted imaging Carotid intraplaque haemorrhage Cervical artery dissection Intramural hematoma ADC 



Apparent diffusion coefficient


Diffusion-weighted imaging


Intraplaque haemorrhage


Intramural hematoma


Lipid-rich necrotic core


Magnetic resonance angiography


Magnetic resonance imaging


Magnetization-prepared rapid acquisition gradient-echo





The scientific guarantor of this publication is Guangbin Wang. The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article. The authors state that this work has not received any funding.

No complex statistical methods were necessary for this paper. Institutional review board approval was obtained. Written informed consent was obtained from all subjects (patients) in this study. Methodology: prospective, experimental, performed at one institution.


  1. 1.
    Levy EI, Mocco J, Samuelson RM, Ecker RD, Jahromi BS, Hopkins LN (2008) Optimal treatment of carotid artery disease. J Am Coll Cardiol 51:979–985CrossRefPubMedGoogle Scholar
  2. 2.
    Teng Z, Sadat U, Brown AJ, Gillard JH (2014) Plaque hemorrhage in carotid artery disease: pathogenesis, clinical and biomechanical considerations. J Biomech 47:847–858CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Kolodgie FD, Gold HK, Burke AP et al (2003) Intraplaque hemorrhage and progression of coronary atheroma. N Engl J Med 349:2316–2325CrossRefPubMedGoogle Scholar
  4. 4.
    Michel JB, Virmani R, Arbustini E, Pasterkamp G (2011) Intraplaque haemorrhages as the trigger of plaque vulnerability. Eur Heart J 32:1977–1985CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Sadat U, Teng Z, Young VE et al (2010) Association between biomechanical structural stresses of atherosclerotic carotid plaques and subsequent ischaemic cerebrovascular events–a longitudinal in vivo magnetic resonance imaging-based finite element study. Eur J Vasc Endovasc Surg 40:485–491CrossRefPubMedGoogle Scholar
  6. 6.
    Saam T, Hetterich H, Hoffmann V et al (2013) Meta-analysis and systematic review of the predictive value of carotid plaque hemorrhage on cerebrovascular events by magnetic resonance imaging. J Am Coll Cardiol 62:1081–1091CrossRefPubMedGoogle Scholar
  7. 7.
    Bartsch T, Palaschewski M, Thilo B et al (2009) Internal carotid artery dissection and stroke after SCUBA diving: a case report and review of the literature. J Neurol 256:1916–1919CrossRefPubMedGoogle Scholar
  8. 8.
    Patel RR, Adam R, Maldjian C, Lincoln CM, Yuen A, Arneja A (2012) Cervical carotid artery dissection: current review of diagnosis and treatment. Cardiol Rev 20:145–152CrossRefPubMedGoogle Scholar
  9. 9.
    Schievink WI (2001) Spontaneous dissection of the carotid and vertebral arteries. N Engl J Med 344:898–906CrossRefPubMedGoogle Scholar
  10. 10.
    Moody AR, Murphy RE, Morgan PS et al (2003) Characterization of complicated carotid plaque with magnetic resonance direct thrombus imaging in patients with cerebral ischemia. Circulation 107:3047–3052CrossRefPubMedGoogle Scholar
  11. 11.
    Chu B, Kampschulte A, Ferguson MS et al (2004) Hemorrhage in the atherosclerotic carotid plaque: a high-resolution MRI study. Stroke 35:1079–1084CrossRefPubMedGoogle Scholar
  12. 12.
    Saam T, Ferguson MS, Yarnykh VL et al (2005) Quantitative evaluation of carotid plaque composition by in vivo MRI. Arterioscler Thromb Vasc Biol 25:234–239CrossRefPubMedGoogle Scholar
  13. 13.
    Rodallec MH, Marteau V, Gerber S, Desmottes L, Zins M (2008) Craniocervical arterial dissection: spectrum of imaging findings and differential diagnosis. Radiographics 28:1711–1728CrossRefPubMedGoogle Scholar
  14. 14.
    Provenzale JM, Sarikaya B, Hacein-Bey L, Wintermark M (2011) Causes of misinterpretation of cross-sectional imaging studies for dissection of the craniocervical arteries. AJR Am J Roentgenol 196:45–52CrossRefPubMedGoogle Scholar
  15. 15.
    Flis CM, Jäger HR, Sidhu PS (2007) Carotid and vertebral artery dissections: clinical aspects, imaging features and endovascular treatment. Eur Radiol 17:820–834CrossRefPubMedGoogle Scholar
  16. 16.
    Heinz ER, Yeates AE, Djang WT (1989) Significant extracranial carotid stenosis: detection on routine cerebral MR images. Radiology 170:843–848CrossRefPubMedGoogle Scholar
  17. 17.
    Nörenberg D, Ebersberger HU, Diederichs G, Hamm B, Botnar RM, Makowski MR (2015) Molecular magnetic resonance imaging of atherosclerotic vessel wall disease. Eur Radiol. doi: 10.1007/s00330-015-3881-2 PubMedGoogle Scholar
  18. 18.
    Chawla S, Kim S, Wang S, Poptani H (2009) Diffusion-weighted imaging in head and neck cancers. Future Oncol l5:959–975CrossRefGoogle Scholar
  19. 19.
    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 17:542–546CrossRefPubMedGoogle Scholar
  20. 20.
    Clarke SE, Hammond RR, Mitchell JR, Rutt BK (2003) Quantitative assessment of carotid plaque composition using multicontrast MRI and registered histology. Magn Reson Med 50:1199–1208CrossRefPubMedGoogle Scholar
  21. 21.
    Kim SE, Jeong EK, Shi XF, Morrell G, Treiman GS, Parker DL (2009) Diffusion-weighted imaging of human carotid artery using 2D single-shot interleaved multislice inner volume diffusion-weighted echo planar imaging (2D ss-IMIV-DWEPI) at 3T_ diffusion measurement in atherosclerotic plaque. J Magn Reson Imaging 30:1068–1077CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Qiao Y, Ronen I, Viereck J, Ruberg FL, Hamilton JA (2007) Identification of atherosclerotic lipid deposits by diffusion-weighted imaging. Arterioscler Thromb Vasc Biol 27:1440–1446CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Young VE, Patterson AJ, Sadat U et al (2010) Diffusion-weighted magnetic resonance imaging for the detection of lipid-rich necrotic core in carotid atheroma in vivo. Neuroradiology 52:929–936CrossRefPubMedGoogle Scholar
  24. 24.
    Kim SE, Treiman GS, Roberts JA et al (2011) In vivo and ex vivo measurements of the mean ADC values of lipid necrotic core and hemorrhage obtained from diffusion-weighted imaging in human atherosclerotic plaques. J Magn Reson Imaging 34:1167–1175CrossRefPubMedGoogle Scholar
  25. 25.
    Haussen DC, Henninger N, Selim M (2013) Diffusion-weighted imaging of intramural hematoma in internal carotid artery dissection. Acta Neurol Belg 113:109–110CrossRefPubMedGoogle Scholar
  26. 26.
    Ota H, Yarnykh VL, Ferguson MS (2010) Carotid intraplaque hemorrhage imaging at 3.0-T MR imaging: comparison of the diagnostic performance of three T1-weighted sequences. Radiology 254:551–563CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Zhu DC, Ferguson MS, DeMarco JK (2008) An optimized 3D inversion recovery prepared fast spoiled gradient recalled sequence for carotid plaque hemorrhage imaging at 3.0 T. Magn Reson Imaging 26:1360–1366CrossRefPubMedGoogle Scholar
  28. 28.
    Fryer JA, Myers PC, Appleberg M (1987) Carotid intraplaque hemorrhage: the significance of neovascularity. J Vasc Surg 6:341–349CrossRefPubMedGoogle Scholar
  29. 29.
    Meyrier A (2006) Cholesterol crystal embolism: diagnosis and treatment. Kidney Int 69:1308–1312CrossRefPubMedGoogle Scholar
  30. 30.
    Virmani R, Kolodgie FD, Burke AP (2005) Atherosclerotic plaque progression and vulnerability to rupture: angiogenesis as a source of intraplaque hemorrhage. Arterioscler Thromb Vasc Biol 25:2054–2061CrossRefPubMedGoogle Scholar
  31. 31.
    Michel JB, Martin-Ventura JL, Nicoletti A, Ho-Tin-Noé B (2014) Pathology of human plaque vulnerability: mechanisms and consequences of intraplaque haemorrhages. Atherosclerosis 234:311–319CrossRefPubMedGoogle Scholar
  32. 32.
    Derksen WJ, Peeters W, van Lammeren GW (2011) Different stages of intraplaque hemorrhage are associated with different plaque phenotypes: a large histopathological study in 794 carotid and 276 femoral endarterectomy specimens. Atherosclerosis 218:369–377CrossRefPubMedGoogle Scholar
  33. 33.
    Altaf N, Beech A, Goode SD, Gladman JR et al (2007) Carotid intraplaque hemorrhage detected by magnetic resonance imaging predicts embolization during carotid endarterectomy. J Vasc Surg 46:31–36CrossRefPubMedGoogle Scholar
  34. 34.
    Wolf O, Heider P, Heinz M et al (2004) Microembolic signals detected by transcranial Doppler sonography during carotid endarterectomy and correlation with serial diffusion-weighted imaging. Stroke 35:e373–e375CrossRefPubMedGoogle Scholar
  35. 35.
    Markus HS, Droste DW, Kaps M (2005) Dual antiplatelet therapy with clopidogrel and aspirin in symptomatic carotid stenosis evaluated using Doppler embolic signal detection: the clopidogrel and aspirin for reduction of emboli in symptomatic carotid stenosis (CARESS) trial. Circulation 111:2233–2240CrossRefPubMedGoogle Scholar
  36. 36.
    Lennard NS, Vijayasekar C, Tiivas C, Chan CW, Higman DJ, Imray CH (2003) Control of emboli in patients with recurrent or crescendo transient ischaemic attacks using preoperative transcranial Doppler-directed Dextran therapy. Br J Surg 90:166–170CrossRefPubMedGoogle Scholar
  37. 37.
    Menon R, Kerry S, Norris JW, Markus HS (2008) Treatment of cervical artery dissection: a systematic review and meta-analysis. J Neurol Neurosurg Psychiatry 79:1122–1127CrossRefPubMedGoogle Scholar

Copyright information

© European Society of Radiology 2015

Authors and Affiliations

  • Bin Yao
    • 1
  • Li Yang
    • 2
  • Guangbin Wang
    • 3
  • Honglu Shi
    • 3
  • Shanshan Wang
    • 3
  • Huihua Li
    • 3
  • Weibo Chen
    • 4
  • Queenie Chan
    • 4
  1. 1.The Second Affiliated Hospital of Nanchang UniversityNanchangChina
  2. 2.Department of Radiology, Shanghai Institute of Medical Imaging, Zhongshan HospitalFudan UniversityShanghaiPeople’s Republic of China
  3. 3.Shandong Medical Imaging Research InstituteShandong UniversityJinanPeople’s Republic of China
  4. 4.Philips HealthcareShanghaiPeople’s Republic of China

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