Biomedical papers, 2018 (vol. 162), issue 1

Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2018, 162(1):10-17 | 10.5507/bp.2018.004

Vulnerable atherosclerotic plaque - a review of current concepts and advanced imaging

Miloslav Spaceka, David Zemanekb, Martin Hutyraa, Martin Slukaa, Milos Taborskya
a Department of Internal Medicine I - Cardiology, Faculty of Medicine and Dentistry, Palacky University Olomouc and University Hospital Olomouc, Olomouc, Czech Republic
b 2nd Department of Internal Medicine - Department of Cardiovascular Medicine, First Faculty of Medicine, Charles University in Prague and General University Hospital in Prague, Czech Republic

Atherosclerosis is the most common cause of both carotid and coronary steno-occlusive disease. Rupture of an atherosclerotic plaque may lead to the formation of an overlying thrombosis resulting in complete arterial occlusion or downstream embolism. Clinically, this may manifest as a stroke or acute myocardial infarction, the overall leading causes of mortality and disability in developed countries. In this article, we summarize current concepts of the development of vulnerable plaque and provide an overview of commonly used imaging methods that may suggest/indicate atherosclerotic plaque vulnerability.

Keywords: atherosclerosis, vulnerable plaque, carotid artery, coronary artery, imaging

Received: September 18, 2017; Accepted: February 6, 2018; Prepublished online: February 21, 2018; Published: March 27, 2018


References

  1. Lloyd-Jones D, Adams RJ, Brown TM, Carnethon M, Dai S, De Simone G, Ferguson TB, Ford E, Furie K, Gillespie C, Go A, Greenlund K, Haase N, Hailpern S, Ho PM, Howard V, Kissela B, Kittner S, Lackland D, Lisabeth L, Marelli A, McDermott MM, Meigs J, Mozaffarian D, Mussolino M, Nichol G, Roger VL, Rosamond W, Sacco R, Sorlie P, Stafford R, Thom T, Wasserthiel-Smoller S, Wong ND, Wylie-Rosett J; American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Executive summary: heart disease and stroke statistics-2010 update: a report from the American Heart Association. Circulation 2010;121(7):948-54. Go to original source... Go to PubMed...
  2. Anderson KM, Wilson PW, Odell PM, Kannel WB. An updated coronary risk profile. A statement for health professionals. Circulation 1991;83(1):356-62. Go to original source... Go to PubMed...
  3. Conroy RM, Pyorala K, Fitzgerald AP, Sans S, Menotti A, De Backer G, De Bacquer D, Ducimetiere P, Jousilahti P, Keil U, Njolstad I, Oganov RG, Thomsen T, Tunstall-Pedoe H, Tverdal A, Wedel H, Whincup P, Wilhelmsen L, Graham IM; SCORE project group. Estimation of ten-year risk of fatal cardiovascular disease in Europe: the SCORE project. Eur Heart J 2003;24(11):987-1003. Go to original source... Go to PubMed...
  4. Falk E, Shah PK, Fuster V. Coronary plaque disruption. Circulation 1995;92(6):657-71. Go to original source... Go to PubMed...
  5. Celeng C, Takx RA, Ferencik M, Maurovich-Horvat P. Non-invasive and invasive imaging of vulnerable coronary plaque. Trends Cardiovascular Med 2016;26(6):538-47. Go to original source...
  6. Humphries SE. Guidelines for the identification and management of patients with familial hypercholesterolemia (FH): are we coming to a consensus? Atheroscler Suppl 2011;12(2):217-20. Go to original source... Go to PubMed...
  7. Skalen K, Gustafsson M, Rydberg EK, Hulten LM, Wiklund O, Innerarity TL, Boren J. Subendothelial retention of atherogenic lipoproteins in early atherosclerosis. Nature 2002;417(6890):750-4. Go to original source... Go to PubMed...
  8. Jufri NF, Mohamedali A, Avolio A, Baker MS. Mechanical stretch: physiological and pathological implications for human vascular endothelial cells. Vasc Cell 2015;7(1):8. Go to original source... Go to PubMed...
  9. Hansson GK. Inflammation, atherosclerosis and coronary artery disease. N Engl J Med 2005;352(16):1685-95. Go to original source... Go to PubMed...
  10. Libby P. Inflammation in atherosclerosis. Arterioscler Thromb Vasc Biol 2012;32(9):2045-51. Go to original source... Go to PubMed...
  11. Andersson J, Libby P, Hansson GK. Adaptive immunity and atherosclerosis. Clin Immunol 2010;134(1):33-46. Go to original source... Go to PubMed...
  12. Saybolt MD, Lilly SM, Patel D, Hamamdzic D, Llano R, Fenning RS, Madden S, Wilensky RL. The vulnerable artery: early and rapid deposition of lipid in coronary arteries is associated with subsequent development of thin-cap fibroatheromas. EuroIntervention 2016;11(14):e1612-8. Go to original source... Go to PubMed...
  13. Janoudi A, Shamoun FE, Kalavakunta JK, Abela GS. Cholesterol crystal induced arterial inflammation and destabilization of atherosclerotic plaque. Eur Heart J. 2016;37(25):1959-67. Go to original source... Go to PubMed...
  14. Libby P. Mechanisms of the acute coronary syndromes and their implications for therapy. N Engl J Med 2013;368(21):2004-13. Go to original source... Go to PubMed...
  15. Moreno PR, Purushothaman KR, Fuster V, Echeverri D, Truszczynska H, Sharma SK, Badimon JJ, O'Connor WN. Plaque neovascularization is increased in ruptured atherosclerotic lesions of human aorta. Implications for plaque vulnerability. Circulation 2004;110(14):2032-8. Go to original source... Go to PubMed...
  16. Karunakaran D, Geoffrion M, Wei L, Gan W, Richards L, Shangari P, DeKemp EM, Beanlands RA, Perisic L, Maegdefessel L, Hedin U, Sad S, Guo L, Kolodgie FD, Virmani R, Ruddy T, Rayner KJ. Targeting macrophage necroptosis for therapeutic and diagnostic interventions in atherosclerosis. Sci Adv 2016;2(7):e1600224. Go to original source... Go to PubMed...
  17. Tuenter A, Selwaness M, Arias Lorza A, Schuurbiers JC, Speelman L, Cibis M, van der Lugt A, de Bruijne M, van der Steen AF, Franco OH, Vernooij MW, Wentzel JJ. High shear stress relates to intraplaque haemorrhage in asymptomatic carotid plaques. Atherosclerosis. 2016;251:348-54. Go to original source... Go to PubMed...
  18. Vergallo R, Ren X, Yonetsu T, Kato K, Uemura S, Yu B, Jia H, Abtahian F, Aguirre AD, Tian J, Hu S, Soeda T, Lee H, McNulty I, Park SJ, Jang Y, Prasad A, Lee S, Zhang S, Porto I, Biasucci LM, Crea F, Jang IK. Pancoronary plaque vulnerability in patients with acute coronary syndrome and ruptured culprit plaque: A 3-vessel optical coherence tomography study. Am Heart J 2014;167(1):59-67. Go to original source... Go to PubMed...
  19. Puri R, Nissen SE, Libby P, Shao M, Ballantyne CM, Barter PJ, Chapman MJ, Erbel R, Raichlen JS, Uno K, Kataoka Y, Nicholls SJ. C-reactive protein, but not low-density lipoprotein cholesterol levels, associate with coronary atheroma regression and cardiovascular events following maximally intensive statin therapy. Circulation 2013;128(22):2395-403. Go to original source... Go to PubMed...
  20. Coronary artery surgery study (CASS): a randomized trial of coronary artery bypass surgery. Survival data. Circulation 1983;68(5):939-50. Go to PubMed...
  21. Tonino PA, De Bruyne B, Pijls NH, Siebert U, Ikeno F, van't Veer M, Klauss V, Manoharan G, Engstrom T, Oldroyd KG, Var Lee PN, MacCarthy PA, Fearon WF; FAME Study Investigators. Fractional flow reserve versus angiography for guiding percutaneous coronary intervention. N Engl J Med 2009;360(3):213-24. Go to original source... Go to PubMed...
  22. North American Symptomatic Carotid Artery Trial Collaborators, Barnett HJM, Taylor DW, Haynes RB, Sackett DL, Peerless SJ, Ferguson GG, Fox AJ, Rankin RN, Hachinski VC, Wiebers DO, Eliasziw M. Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis. N Engl J Med 1991;325(7):445-53. Go to original source... Go to PubMed...
  23. European Carotid Surgery Trialists´ Collaborative Group. MRC European Carotid Surgery Trial: interim results for symptomatic patients with severe (70-99%) or mild (0-29%) carotid stenosis. Lancet 1991;337(8752):1235-43. Go to original source... Go to PubMed...
  24. Executive Committee for the Asymptomatic Carotid Atherosclerosis Study. Endarterectomy for asymptomatic carotid artery stenosis. JAMA 1995;273(18):1421-8. Go to original source... Go to PubMed...
  25. Halliday AW, Thomas D, Mansfield A. The Asymptomatic Carotid Surgery Trial (ACST). Rationale and design. Steering Committee. Eur J Vasc Surg 1994;8(6):703-10.
  26. Silvestrini M, Vernieri F, Pasqualetti P, Matteis M, Passarelli F, Troisi E, Caltagirone C. Impaired cerebral vasoreactivity and risk of stroke in patients with asymptomatic carotid artery stenosis. JAMA 2000;283(16):2122-7. Go to original source... Go to PubMed...
  27. Small GR, Chow BJW. CT imaging of the vulnerable plaque. Curr Treat Options Cardiovasc Med 2017;19(12):92. Go to original source... Go to PubMed...
  28. Ouhlos M, Flach HZ, de Weert TT, Hendriks JM, van Sambeek MR, Dippel DW, Pattynama PM, van der Lugt A. Carotid plaque composition and cerebral infarction: MR imaging study. Am J Neuroradiol 2005;26(5):1044-9. Go to PubMed...
  29. de Weert TT, Ouhlos M, Meijering E, Zondervan PE, Hendriks JM, van Sambeek MR, Dippel DW, van der Lugt A. In vivo characterization and quantication of atherosclerotic carotid plaque components with multi detector computed tomography and histopathological correlation. Arterioscler Thromb Vasc Biol 2006;26(10):2366-72. Go to original source... Go to PubMed...
  30. Hoffman U, Moselewski F, Nieman K, Jang IK, Ferencik M, Rahman AM, Cury RC, Abbara S, Joneidi-Jafari H, Achenbach S, Brady TJ. Noninvasive assessment of plaque morphology and composition in culprit and stable lesions in acute coronary syndrome and stable lesions in stable angina by multi detector computed tomography. J Am Coll Cardiol 2006;47(8):1655-62. Go to original source... Go to PubMed...
  31. Motoyama S, Sarai M, Harigaya H, Anno H, Inoue K, Hara T, Naruse H, Ishii J, Hishida H, Wong ND, Virmani R, Kondo T, Ozaki Y, Narula J. Computed tomographic angiography characteristics of atherosclerotic plaques subsequently resulting in acute coronary syndrome. J Am Coll Cardiol 2009;54(1):49-57. Go to original source... Go to PubMed...
  32. Tsutsumi M, Kodama T, Aikawa H, Onizuka M, iko M, Nii K, Hamaguchi S, Etou H, Sakamoto K, Inoue R, Nakau H, Kazekawa K. Fragmentation of calcified plaque after carotid artery stenting in heavily calcified circumferential stenosis. Neuroradiology 2010;52(9):831-6. Go to original source... Go to PubMed...
  33. Braunwald E. Noninvasive detection of vulnerable coronary plaques. Locking the barn door before the horse is stolen. J Am Coll Cardiol 2009;54(1):58-59. Go to original source... Go to PubMed...
  34. Teng Z, Brown AJ, Gillard JH. From ultrasonography to high resolution magnetic resonance imaging: towards an optimal management strategy for vulnerable carotid atherosclerotic plaques. EBioMedicine 2016;3:2-3. Go to original source... Go to PubMed...
  35. Hatsukami TS, Ross R, Polissar NL, Yuan C. Visualization of fibrous cap thickness and rupture in human atherosclerotic carotid plaque in vivo with high-resolution magnetic resonance imaging. Circulation 2000;102(9):959-64. Go to original source... Go to PubMed...
  36. Demarco JK, Ota H, Underhill HR, Zhu DC, Reeves MJ, Potchen MJ, Majid A, Collar A, Talsma JA, Potru S, Oikawa M, Dong L, Zhao X, Yarnych VL, Yuan C. MR carotid plaque imaging and contrast-enhanced MR angiography identifies lesions associated with recent ipsilateral thromboembolic symptoms: an in vivo study at 3T. AJNR Am J Neuroradiol 2010;31(8):1395-402. Go to original source... Go to PubMed...
  37. Chu B, Kampschulte A, Ferguson MS, Kerwin WS, Yarnych VL, O'Brien KD, Polissar NL, Hatsukami TS, Yuan C. Hemorrhage in the atherosclerotic carotid plaque: a high resolution MRI study. Stroke 2004;35(5):1079-84. Go to original source... Go to PubMed...
  38. Brinjikji W, Rabinstein AA, Lanzino G, Murad MH, Williamson EE, DeMarco JK, Huston J 3rd. Ultrasound characteristics of symptomatic carotid plaques: a systematic review and meta-analysis. Cerebrovasc Dis 2015;40(3-4):165-74. Go to original source... Go to PubMed...
  39. Gupta A, Kesavabhotla K, Baradaran H, Kamel H, Pandya A, Giambrone AE, Wright D, Pain KJ, Mtui EE, Suri JS, Sanelli PC, Mushlin AL. Plaque echolucency and stroke risk in asymptomatic carotid stenosis: a systematic review and meta- analysis. Stroke 2015;46(1):91-7. Go to original source... Go to PubMed...
  40. Eliasziw M, Steriler JY, Fox AJ, Hachinski VC, Fergusson GG, Barnett HJ. Significance of plaque ulceration in symptomatic patients with high grade carotid stenosis: North American Symptomatic Carotid Endarterectomy Trial. Stroke 1994;25(2):304-8. Go to original source... Go to PubMed...
  41. Geroulakos G, Ramaswani G, Nicolaides A, James K, Labropoulos N, Belcaro G, Holloway M. Characterization of symptomatic and asymptomatic carotid plaques using high resolution real time ultrasound. Br J Surg 1993;80(10):1274-7. Go to original source... Go to PubMed...
  42. Staub D, Partovi S, Schinkel AF, Coll B, Uthoff H, Achwanden M, Jaegeer KA, Feinstein SB. Correlation of carotid artery atherosclerotic lesion echogenicity and severity at standard US with intraplaque neovascularization detected at contrast enhanced US. Radiology 2011;258(2):618-26. Go to original source... Go to PubMed...
  43. Millon A, Boussel L, Brevet M, Mathevet JL Canet-Soulas E, Mory C, Scoazec JY, Douek P. Clinical and histological significance of gadolinium enhancement in carotid atherosclerotic plaque. Stroke 2012;43(11):3023-8. Go to original source... Go to PubMed...
  44. Johri AM, Herr JE, Li TY, Yau O, Nambi V. Novel Ultrasound Methods to Investigate Carotid Artery Plaque Vulnerability. J Am Soc Echocardiogr 2017;30(2):139-48. Go to original source... Go to PubMed...
  45. Markus HS, King A, Shipley M, Topakian R, Cullinane M, Reihill S, Bornstein NM, Schaafsma A. Asymptomatic embolisation for prediction of stroke in the Asymptomatic Carotid Emboli Study (ACES): a prospective observational study. Lancet Neurol 2010;9(7):663-71. Go to original source... Go to PubMed...
  46. Spence JD. Transcranial Doppler monitoring for microemboli: a marker of a high-risk carotid plaque. Semin Vasc Surg 2017;30(1):62-6. Go to original source... Go to PubMed...
  47. Tawakol A, Migrino RQ, Bashian GG, Bedri S, Vermylen D, Cury RC, Yates D, LaMuraglia GM, Furie K, Houser S, Gewirtz H, Muller JE, Brady TJ, Fischman AJ. In vivo 18F-fluorodeoxyglucose positron emission tomography imaging provides a non-invasive measure of carotid plaque inflammation in patients. J Am Coll Cardiol 2006;48(9):1818-24. Go to original source... Go to PubMed...
  48. Liu J, Kervin WS, Caldwell JH, Fergusson MS, Hippe DS, Alessio AM, Martinez-Malo V, Pimentel K, Miyaoka RS, Kohler TR, Hatsukami TS, Yuan C. High-resolution FDG-microPET of carotid atherosclerosis: plaque components underlying enhanced FDG uptake. Int J Cardiovasc Imaging 2016;32(1):145-52. Go to original source... Go to PubMed...
  49. Tahata N, Kai H, Ishibashi M, Nakaur H, Kaida H, Baba K, Hayabuchi N, Imaizumi T. Simvastatin attenuates plaque inflammation. Evaluation by fluorodeoxyglucose positron emission tomography. J Am Coll Cardiol 2006;48(9):1825-31. Go to original source... Go to PubMed...
  50. Fujimoto S, Hartung D, Ohshima S, Edwards DS, Zhou J, Yalamanchili P, Azure M, Fujimoto A, Isobe S, Matsumoto Y, Boersma H, Wong N, Yamazaki J, Narula N, Petrov A, Narula J. Molecular imaging of matrix metalloproteinase in atherosclerotic lesions. Resolution with dietary modification and statin therapy. J Am Coll Cardiol 2008;52(23):1847-57. Go to original source... Go to PubMed...
  51. Yamagishi M, Tereshima M, Awano K, Kijima M, Nakatani S, Daikoku S, Ito K, Yasamura Y, Miyatake K. Morphology of vulnerable coronary plaque: insights from follow-up of patients examined by intravascular ultrasound before an acute coronary syndrome. J Am Coll Cardiol 2000;35(1):106-11. Go to original source... Go to PubMed...
  52. Kotani J, Mintz GS, Castagna MT, Pinnow E, Berzingi CO, Bui AB, Pichard AD, Satler LF, Suddath WO, Waksman R, Laird JR Jr, Kent KM, Weissman NJ. Intravascular ultrasound analysis of infarct-related and non-infarct related arteries in patients who presented with an acute myocardial infarction. Circulation 2003;107(23):2889-93. Go to original source... Go to PubMed...
  53. Ehara S, Kobayashi Y, Yoshiama M, Shimada K, Shimada Y, Fukuda D, Nakamura Y, Yamashita H, Yamagishi H, Takeuchi K, Naruko T, Haze K, Becker AE, Yoshikawa J, Ueda M. Spotty calcification typifies the culprit plaque in patients with acute myocardial infarction: an intravascular ultrasound study. Circulation 2004;110(22):3424-9. Go to original source... Go to PubMed...
  54. Nair A, Kuban BD, Tuzcu EM, Schoenhagen P, Nissen SE, Vince DG. Coronary plaque classification with intravascular ultrasound radiofrequency data analysis. Circulation 2002;106(17):2200-6. Go to original source... Go to PubMed...
  55. Mehta SK, McCary JR, Frutkin AD, Dolla WJ, Marso SP. Intravascular ultrasound radiofrequency analysis of coronary atherosclerosis: an emerging technology for the assessment of vulnerable plaque. Eur Heart J 2007;28(11):1283-8. Go to original source... Go to PubMed...
  56. Nasu K, Tsuchikane E, Katoh O, Vince DG, Virmani R, Surmely JF, Murata A, Takeda Y, Ito T, Ehara M, Matsubara T, Tereshima M, Suzuki T. Accuracy of in vivo coronary plaque morphology assessment: a validation study of in vivo virtual histology compared with in vitro histopatology. J Am Coll Cardiol 2006;47(12):2405-12. Go to original source... Go to PubMed...
  57. Stone GW, Maehara A, Lansky AJ, de Bruyne B, Cristae E, Mintz GS, Mehran R, McPherson J, Farhat N, Marso SP, Parise H, Templin B, White R, Zhang Z, Serruys PW; PROSPECT Investigators. A prospective natural-history study of coronary atherosclerosis. N Engl J Med 2011;364(21):226-35. Go to original source... Go to PubMed...
  58. McPherson JA, Maehara A, Weisz G, Mintz GS, Cristae E, Mehran R, Foster M, Verheye S, Rabbani L, Xu K, Fahy M, Templin B, Zhang Z, Lansky AJ, de Bruyne B, Serruys PW, Stone GW. Residual plaque burden in patients with acute coronary syndromes after successful percutaneous coronary intervention. JACC Cardiovas Imaging 2012;5(3):S95-S105. Go to original source... Go to PubMed...
  59. Kume T, Uemura S. Current clinical applications of coronary optical coherence tomography. Cardiovasc Interv Ther 2017. doi: 10.1007/s12928-017-0483-8. [Epub ahead of print]. Go to original source... Go to PubMed...
  60. Tearney GJ, Yabushita H, Houser SL, Aretz HT, Jang IK, Schlendorf KH, Kauffman CR, Shishkov M, Halpern EF, Bouma BE. Quantification of macrophages content in atherosclerotic plaques by optical coherence tomography. Circulation 2003;107(1):113-9. Go to original source... Go to PubMed...
  61. Rathore S, Tereshima M, Matsuo H, Kinoshita Y, Kimura M, Tsuchikane E, Nasu K, Ehara M, Asakura Y, Katoh O, Suzuki T. Association of coronary plaque composition and arterial remodelling: a optical coherence study. Atherosclerosis 2012;221(2):405-15. Go to original source... Go to PubMed...
  62. Kato K, Yonetsu K, Kim SJ, Xing L, Lee H, McNulty I, Yeh RW, Sakhuja R, Zhang S, Uemura S, Yu B, Mizuno K, Jang IK. Comparison of nonculprit coronary plaque characteristics between patients with and without diabetes: a 3-vessel optical coherence tomography study. JACC Cardiovasc Interv 2012;5(11):1150-8. Go to original source... Go to PubMed...
  63. Hattori K, Ozaki Y, Ismail TF, Okumura M, Naruse H, Kan S, Ishikawa M, Kawai T, Ohta M, Kawai H, Hashimoto T, Takagi Y, Ishii J, Serruys PW, Narula J. Impact of statin therapy on plaque characteristics as assessed by serial OCT, greyscale and integrated backscatter-IVUS. JACC Cardiovasc Imaging 2012;5(2):169-77. Go to original source... Go to PubMed...
  64. Kang SJ, Mintz GS, Pu J, Sum ST, Madden SP, Burke AP, Xu K, Goldstein JA, Stone GW, Muller JE, Virmani R, Maehara A. Combined IVUS and NIRS detection of fibroateheromas: histopatological validation in human coronary arteries. J Am Coll Cardiol Img 2015;8(2):184-94. Go to original source...
  65. Fard AM, Vacas-Jacques P, Hamidi E, Wang H, Carruth RW, Gardecki JA, Tearney GJ. Optical coherence tomography - near infrared spectroscopy system and catheter for intravascular imaging. Opt Express 2013;21(25):30849-58. Go to original source... Go to PubMed...