Molecular imaging of vascular inflammation

Current Pharmaceutical Design

Volumn 20, Issue 14, 2014, Pages 2439-2447

  Tahara, Nobuhiro ^a   Tahara, Atsuko ^a   Honda, Akihiro ^a   Nitta, Yoshikazu ^a   Kodama, Norihiro ^a   Yamagishi, Sho ichi ^a   Imaizumi, Tsutomu ^a  

^a KURUME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

18F labeled FDG PET; Atherosclerosis; Inflammation; Molecular imaging; Vulnerable plaque

Indexed keywords

FLUORODEOXYGLUCOSE F 18;

AORTA DISEASE; ARTERITIS; ARTERY DIAMETER; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CARDIOVASCULAR RISK; COMPUTER ASSISTED EMISSION TOMOGRAPHY; COMPUTER ASSISTED TOMOGRAPHY; CORONARY ARTERY DISEASE; DIAGNOSTIC TEST ACCURACY STUDY; DIAGNOSTIC VALUE; DRUG EFFICACY; DRUG UPTAKE; EXPERIMENTAL MODEL; FEASIBILITY STUDY; HUMAN; INFLAMMATION; MACROPHAGE; MOLECULAR BIOLOGY; MOLECULAR IMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; ONCOLOGY; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; REPRODUCIBILITY; VASCULITIS; ANIMAL; DIAGNOSTIC IMAGING; PATHOPHYSIOLOGY; PROCEDURES; TRENDS; VASCULAR DISEASES;

ANIMALS; ATHEROSCLEROSIS; DIAGNOSTIC IMAGING; HUMANS; INFLAMMATION; MOLECULAR IMAGING; VASCULAR DISEASES;

EID: 84903708769     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/13816128113199990479     Document Type: Article

References (92)

1. World Health Organization. World Health Statistics 2012. Geneva: WHO, 2012.
2. Go AS, Mozaffarian D, Roger VL, et al. American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Executive summary: heart disease and stroke statistics--2013 update: a report from the American Heart Association. Circulation 2013; 127: 143-52.
3. Naghavi M, Libby P, Falk E, et al. From vulnerable plaque to vulnerable patient: a call for new definitions and risk assessment strategies: part I. Circulation 2003; 108: 1664-72.
4. Naghavi M, Libby P, Falk E, et al. From vulnerable plaque to vulnerable patient: a call for new definitions and risk assessment strategies: Part II. Circulation 2003; 108: 1772-8.
5. Fayad ZA, Fuster V. Clinical imaging of the high-risk or vulnerable atherosclerotic plaque. Circ Res 2001; 89: 305-16.
6. Moreno PR, Falk E, Palacios IF, Newell JB, Fuster V, Fallon JT. Macrophage infiltration in acute coronary syndromes. Implications for plaque rupture. Circulation 1994; 90: 775-8.
7. van der Wal AC, Becker AE, Koch KT, et al. Clinically stable angina pectoris is not necessarily associated with histologically stable atherosclerotic plaques. Heart 1996; 76: 312-6.
8. Jaffer FA, Libby P, Weissleder R. Molecular and cellular imaging of atherosclerosis: emerging applications. J Am Coll Cardiol 2006; 47: 1328-38.
9. Narula J, Garg P, Achenbach S, Motoyama S, Virmani R, Strauss HW. Arithmetic of vulnerable plaques for noninvasive imaging. Nat Clin Pract Cardiovasc Med 2008; 5: S2-S10.
10. Phelps ME. PET: the merging of biology and imaging into molecular imaging. J Nucl Med 2000; 41: 661-81.
11. Vallabhajosula S, Fuster V. Atherosclerosis: imaging techniques and the evolving role of nuclear medicine. J Nucl Med 1997; 38: 1788-96.
12. Jaffer FA, Weissleder R. Seeing within: molecular imaging of the cardiovascular system. Circ Res 2004; 94: 433-45.
13. Libby P. Inflammation in atherosclerosis. Nature 2002; 420: 868-74.
14. Rudd JH, Warburton EA, Fryer TD, et al. Imaging atherosclerotic plaque inflammation with [18F]-fluorodeoxyglucose positron emission tomography. Circulation 2002; 105: 2708-11.
15. 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 noninvasive measure of carotid plaque inflammation in patients. J Am Coll Cardiol 2006; 48: 1818-24.
16. Tahara N, Kai H, Ishibashi M, et al. Simvastatin attenuates plaque inflammation: evaluation by fluorodeoxyglucose positron emission tomography. J Am Coll Cardiol 2006; 48: 1825-31.
17. Tahara N, Kai H, Yamagishi S, et al. Vascular inflammation evaluated by [18F]-fluorodeoxyglucose positron emission tomography is associated with the metabolic syndrome. J Am Coll Cardiol 2007; 49: 1533-9.
18. Tahara N, Kai H, Nakaura H, et al. The prevalence of inflammation in carotid atherosclerosis: analysis with fluorodeoxyglucosepositron emission tomography. Eur Heart J 2007; 28: 2243-8.
19. Tahara N, Imaizumi T, Virmani R, Narula J. Clinical feasibility of molecular imaging of plaque inflammation in atherosclerosis. J Nucl Med 2009; 50: 331-4.
20. Tahara N, Yamagishi S, Takeuchi M, et al. Positive association between serum level of glyceraldehyde-derived advanced glycation end products and vascular inflammation evaluated by [(18)F]fluorodeoxyglucose positron emission tomography. Diabetes Care 2012; 35: 2618-25.
21. Rudd JH, Narula J, Strauss HW, et al. Imaging atherosclerotic plaque inflammation by fluorodeoxyglucose with positron emission tomography: ready for prime time? J Am Coll Cardiol 2010; 55: 2527-35.
22. Mizoguchi M, Tahara N, Tahara A, et al. Pioglitazone attenuates atherosclerotic plaque inflammation in patients with impaired glucose tolerance or diabetes a prospective, randomized, comparatorcontrolled study using serial FDG PET/CT imaging study of carotid artery and ascending aorta. JACC Cardiovasc Imaging 2011; 4: 1110-8.
23. Kolodgie FD, Burke AP, Farb A, et al. The thin-cap fibroatheroma: a type of vulnerable plaque: the major precursor lesion to acute coronary syndromes. Curr Opin Cardiol 2001; 16: 285-92.
24. Kagawa R, Moritake K, Shima T, Okada Y. Validity of B-mode ultrasonographic findings in patients undergoing carotid endarterectomy in comparison with angiographic and clinicopathologic features. Stroke 1996; 27: 700-5.
25. Golledge J, Greenhalgh RM, Davies AH. The symptomatic carotid plaque. Stroke 2000; 31: 774-81.
26. Grønholdt ML, Nordestgaard BG, Schroeder TV, Vorstrup S, Sillesen H. Ultrasonic echolucent carotid plaques predict future strokes. Circulation 2001; 104: 68-73.
27. Valgimigli M, Agostoni P, Serruys PW. Acute coronary syndromes: an emphasis shift from treatment to prevention; and the enduring challenge of vulnerable plaque detection in the cardiac catheterization laboratory. J Cardiovasc Med (Hagerstown) 2007; 8: 221-9.
28. Motoyama S, Kondo T, Sarai M, et al. Multislice computed tomographic characteristics of coronary lesions in acute coronary syndromes. J Am Coll Cardiol. 2007; 50: 319-26.
29. Motoyama S, Sarai M, Harigaya H, et al. Computed tomographic angiography characteristics of atherosclerotic plaques subsequently resulting in acute coronary syndrome. J Am Coll Cardiol 2009; 54: 49-57.
30. Nakazawa G, Tanabe K, Onuma Y, et al. Efficacy of culprit plaque assessment by 64-slice multidetector computed tomography to predict transient no-reflow phenomenon during percutaneous coronary intervention. Am Heart J 2008; 155: 1150-7.
31. Tanaka A, Shimada K, Yoshida K, et al. Non-invasive assessment of plaque rupture by 64-slice multidetector computed tomography--comparison with intravascular ultrasound. Circ J 2008; 72: 1276-81.
32. Kashiwagi M, Tanaka A, Kitabata H, et al. Feasibility of noninvasive assessment of thin-cap fibroatheroma by multidetector computed tomography. JACC Cardiovasc Imaging 2009; 2: 1412-9.
33. Tanaka A, Kawasaki T, Noguchi T, et al. Hyperintense plaque with noncontrast T1-weighted magnetic resonance coronary plaque imaging leading to acute coronary syndrome. Circulation 2009; 120: 2400-1.
34. Kawasaki T, Koga S, Koga N, et al. Characterization of hyperintense plaque with noncontrast T(1)-weighted cardiac magnetic resonance coronary plaque imaging: comparison with multislice computed tomography and intravascular ultrasound. JACC Cardiovasc Imaging 2009; 2: 720-8.
35. Noguchi T, Yamada N, Higashi M, Goto Y, Naito H. Highintensity signals in carotid plaques on T1-weighted magnetic resonance imaging predict coronary events in patients with coronary artery disease. J Am Coll Cardiol 2011; 58: 416-22.
36. Virgolini I, Müller C, Fitscha P, et al. Radiolabelling autologous monocytes with 111-indium-oxine for reinjection in patients with atherosclerosis. Prog Clin Biol Res 1990; 355: 271-80.
37. Lees RS, Lees AM, Strauss HW. External imaging of human atherosclerosis. J Nucl Med. 1983; 24: 154-6.
38. Fischman AJ, Rubin RH, Khaw BA, et al. Radionuclide imaging of experimental atherosclerosis with nonspecific polyclonal immunoglobulin G. J Nucl Med 1989; 30: 1095-100.
39. Hartung D, Petrov A, Haider N, et al. Radiolabeled Monocyte Chemotactic Protein 1 for the detection of inflammation in experimental atherosclerosis. J Nucl Med 2007; 48: 1816-21.
40. Sadeghi MM, Schechner JS, Krassilnikova S, et al. Vascular cell adhesion molecule-1-targeted detection of endothelial activation in human microvasculature. Transplant Proc 2004; 36: 1585-91.
41. Fujimoto S, Hartung D, Ohshima S, et al. Molecular imaging of matrix metalloproteinase in atherosclerotic lesions: resolution with dietary modification and statin therapy. J Am Coll Cardiol 2008; 52: 1847-57.
42. Delbeke D. Oncological applications of FDG PET Imaging. J Nucl Med 1999; 40: 1706-15.
43. Kubota R, Yamada S, Kubota K, Ishiwata K, Tamahashi N, Ido T. Intratumoral distribution of fluorine-18-fluorodeoxyglucose in vivo: high accumulation in macrophages and granulation tissues studied by microautoradiography. J Nucl Med 1992; 33: 1972-80.
44. Kubota R, Kubota K, Yamada S, Tada M, Ido T, Tamahashi N. Microautoradiographic study for the differentiation of intratumoral macrophages, granulation tissues and cancer cells by the dynamics of fluorine-18-fluorodeoxyglucose uptake. J Nucl Med 1994; 35: 104-12.
45. Folco EJ, Sheikine Y, Rocha VZ, et al. Hypoxia but not inflammation augments glucose uptake in human macrophages: Implications for imaging atherosclerosis with 18fluorine-labeled 2-deoxy-Dglucose positron emission tomography. J Am Coll Cardiol 2011; 58: 603-14.
46. Ogawa M, Nakamura S, Saito Y, Kosugi M, Magata Y. What can be seen by 18F-FDG PET in atherosclerosis imaging? The effect of foam cell formation on 18F-FDG uptake to macrophages in vitro. J Nucl Med 2012; 53: 55-8.
47. Rosenbaum D, Millon A, Fayad ZA. Molecular imaging in atherosclerosis: FDG PET. Curr Atheroscler Rep 2012; 14: 429-37.
48. Saam T, Cai J, Ma L, et al. Comparison of symptomatic and asymptomatic atherosclerotic carotid plaque features with in vivo MR imaging. Radiology 2006; 240: 464-72.
49. Sadat U, Weerakkody RA, Bowden DJ, et al. Utility of high resolution MR imaging to assess carotid plaque morphology: a comparison of acute symptomatic, recently symptomatic and asymptomatic patients with carotid artery disease. Atherosclerosis 2009; 207: 434-9.
50. 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: 959-64.
51. Yuan C, Mitsumori LM, Ferguson MS, et al. In vivo accuracy of multispectral magnetic resonance imaging for identifying lipid-rich necrotic cores and intraplaque hemorrhage in advanced human carotid plaques. Circulation 2001; 104: 2051-6.
52. Cai J, Hatsukami TS, Ferguson MS, et al. 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 2005; 112: 3437-44.
53. Bini J, Izquierdo-Garcia D, Mateo J, et al. Preclinical Evaluation of MR Attenuation Correction Versus CT Attenuation Correction on a Sequential Whole-Body MR/PET Scanner. Invest Radiol. 2013; 48: 313-22.
54. Berker Y, Franke J, Salomon A, et al. MRI-based attenuation correction for hybrid PET/MRI systems: a 4-class tissue segmentation technique using a combined ultrashort-echo-time/Dixon MRI sequence. J Nucl Med. 2012; 53: 796-804.
55. Rudd JH, Myers KS, Bansilal S, et al. (18)Fluorodeoxyglucose positron emission tomography imaging of atherosclerotic plaque inflammation is highly reproducible: implications for atherosclerosis therapy trials. J Am Coll Cardiol 2007; 50: 892-6.
56. Numano F, Okawara M, Inomata H, Kobayashi Y. Takayasu's arteritis. Lancet 2000; 356: 1023-25.
57. Arend WP, Michel BA, Bloch DA, et al. The American College of Rheumatology 1990 criteria for the classification of Takayasu arteritis. Arthritis Rheum 1990; 33: 1129-34.
58. Webb M, Chambers A, AL-Nahhas A, et al. The role of 18F-FDG PET in characterising disease activity in Takayasu arteritis. Eur J Nucl Med Mol Imaging 2004; 31: 627-34.
59. Kobayashi Y, Ishii K, Oda K, et al. Aortic wall inflammation due to Takayasu arteritis imaged with 18F-FDG PET coregistered with enhanced CT. J Nucl Med 2005; 46: 917-22.
60. Tezuka D, Haraguchi G, Ishihara T, et al. Role of FDG PET-CT in Takayasu arteritis: sensitive detection of recurrences. JACC Cardiovasc Imaging 2012; 5: 422-9.
61. Sakalihasan N, Delvenne P, Nusgens BV, Limet R, Lapière CM. Activated forms of MMP2 and MMP9 in abdominal aortic aneurysms. J Vasc Surg 1996; 24: 127-33.
62. Sangiorgi G, Trimarchi S, Mauriello A, et al. Plasma levels of metalloproteinases-9 and-2 in the acute and subacute phases of type A and type B aortic dissection. J Cardiovasc Med (Hagerstown) 2006; 7: 307-15.
63. Karapanagiotidis GT, Antonitsis P, Charokopos N, et al. Serum levels of matrix metalloproteinases-1,-2,-3 and-9 in thoracic aortic diseases and acute myocardial ischemia. J Cardiothorac Surg 2009; 4: 59.
64. Lindholt JS, Vammen S, Fasting H, Henneberg EW, Heickendorff L. The plasma level of matrix metalloproteinase 9 may predict the natural history of small abdominal aortic aneurysms. A preliminary study. Eur J Vasc Endovasc Surg 2000; 20: 281-5.
65. Sakalihasan N, Van Damme H, Gomez P, et al. Positron emission tomography (PET) evaluation of abdominal aortic aneurysm (AAA). Eur J Vasc Endovasc Surg 2002; 23: 431-6.
66. Kato K, Nishio A, Kato N, Usami H, Fujimaki T, Murohara T. Uptake of 18F-FDG in acute aortic dissection: a determinant of unfavorable outcome. J Nucl Med 2010; 51: 674-81.
67. Reeps C, Pelisek J, Bundschuh RA, et al. Imaging of acute and chronic aortic dissection by 18F-FDG PET/CT. J Nucl Med 2010; 51: 686-91.
68. Vallabhajosula S, Machac K, Knesaurek J. Imaging atherosclerotic macrophage density by positron emission tomography using F-18 fluorodeoxyglucose (FDG) (abstr). J Nucl Med 1996; 37 Suppl: 38P.
69. Lederman RJ, Raylman RR, Fisher SJ, et al. Detection of atherosclerosis using a novel positron-sensitive probe and 18-fluorodeoxyglucose (FDG). Nucl Med Commun 2001; 22: 747-53.
70. Ogawa M, Ishino S, Mukai T, et al. (18)F-FDG accumulation in atherosclerotic plaques: immunohistochemical and PET imaging study. J Nucl Med 2004; 45: 1245-50.
71. Tawakol A, Migrino RQ, Hoffmann U, et al. Noninvasive in vivo measurement of vascular inflammation with F-18 fluorodeoxyglucose positron emission tomography. J Nucl Cardiol 2005; 12: 294-301.
72. Yun M, Yeh D, Araujo LI, et al. F-18 FDG uptake in the large arteries: a new observation. Clin Nucl Med 2001; 26: 314-9.
73. Yun M, Jang S, Cucchiara A, Newberg AB, Alavi A. 18F FDG uptake in the large arteries: a correlation study with the atherogenic risk factors. Semin Nucl Med 2002; 32: 70-6.
74. Tatsumi M, Cohade C, Nakamoto Y, Wahl RL. Fluorodeoxyglucose uptake in the aortic wall at PET/CT: possible finding for active atherosclerosis. Radiology. 2003; 229: 831-7.
75. Ben-Haim S, Kupzov E, Tamir A, Israel O. Evaluation of 18F-FDG uptake and arterial wall calcifications using 18F-FDG PET/CT. J Nucl Med 2004; 45: 1816-21.
76. Dunphy MP, Freiman A, Larson SM, Strauss HW. Association of vascular 18F-FDG uptake with vascular calcification. J Nucl Med 2005; 46: 1278-84.
77. Yun M, Jang S, Cucchiara A, Newberg AB, Alavi A. 18F FDG uptake in the large arteries: a correlation study with the atherogenic risk factors. Semin Nucl Med 2002; 32: 70-6.
78. Tahara N, Yamagishi SI, Mizoguchi M, et al. Demonstration of the efficacy of statins in resolution of plaque inflammation by serial FDG imaging. Immun, Endoc & Metab Agents in Med Chem 2008; 8: 183-8.
79. Crisby M, Nordin-Fredriksson G, Shah PK, Yano J, Zhu J, Nilsson J. Pravastatin treatment increases collagen content and decreases lipid content, inflammation, metalloproteinases, and cell death in human carotid plaques: implications for plaque stabilization. Circulation 2001; 103: 926-33.
80. Sukhova GK, Williams JK, Libby P. Statins reduce inflammation in atheroma of nonhuman primates independent of effects on serum cholesterol. Arterioscler Thromb Vasc Biol 2002; 22: 1452-8.
81. Nissen SE, Nicholls SJ, Sipahi I, et al; ASTEROID Investigators. Effect of very high-intensity statin therapy on regression of coronary atherosclerosis: the ASTEROID trial. JAMA 2006; 295: 1556-65.
82. Nissen SE, Nicholls SJ, Wolski K, et al; PERISCOPE Investigators. Comparison of pioglitazone vs glimepiride on progression of coronary atherosclerosis in patients with type 2 diabetes: the PERISCOPE randomized controlled trial. JAMA. 2008; 299: 1561-73.
83. Miyazaki Y, Mahankali A, Matsuda M, et al. Improved glycemic control and enhanced insulin sensitivity in type 2 diabetic subjects treated with pioglitazone. Diabetes Care 2001; 24: 710-9.
84. Satoh N, Ogawa Y, Usui T, et al. Antiatherogenic effect of pioglitazone in type 2 diabetic patients irrespective of the responsiveness to its antidiabetic effect. Diabetes Care 2003; 26: 2493-9.
85. Pfützner A, Marx N, Lübben G, et al. Improvement of cardiovascular risk markers by pioglitazone is independent from glycemic control: results from the pioneer study. J Am Coll Cardiol 2005; 45: 1925-31.
86. Dormandy JA, Charbonnel B, Eckland DJ, et al; PROactive investigators. Secondary prevention of macrovascular events in patients with type 2 diabetes in the PROactive Study (PROspective pioglitAzone Clinical Trial In macroVascular Events): a randomised controlled trial. Lancet 2005; 366: 1279-89.
87. Wilcox R, Bousser MG, Betteridge DJ, et al; PROactive Investigators. Effects of pioglitazone in patients with type 2 diabetes with or without previous stroke: results from PROactive (PROspective pioglitAzone Clinical Trial In macroVascular Events 04). Stroke 2007; 38: 865-73.
88. Erdmann E, Dormandy JA, Charbonnel B, Massi-Benedetti M, Moules IK, Skene AM; PROactive Investigators. The effect of pioglitazone on recurrent myocardial infarction in 2,445 patients with type 2 diabetes and previous myocardial infarction: results from the PROactive (PROactive 05) Study. J Am Coll Cardiol 2007; 49: 1772-80.
89. Mazzone T, Meyer PM, Feinstein SB, et al. Effect of pioglitazone compared with glimepiride on carotid intima-media thickness in type 2 diabetes: a randomized trial. JAMA 2006; 296: 2572-81.
90. Alexanderson E, Slomka P, Cheng V, et al. Fusion of positron emission tomography and coronary computed tomographic angiography identifies fluorine 18 fluorodeoxyglucose uptake in the left main coronary artery soft plaque. J Nucl Cardiol 2008; 15: 841-3.
91. Rogers IS, Nasir K, Figueroa AL, et al. Feasibility of FDG imaging of the coronary arteries: comparison between acute coronary syndrome and stable angina. JACC Cardiovasc Imaging 2010; 3: 388-97.
92. Paulmier B, Duet M, Khayat R, et al. Arterial wall uptake of fluorodeoxyglucose on PET imaging in stable cancer disease patients indicates higher risk for cardiovascular events. J Nucl Cardiol 2008; 15: 209-17.