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Clinical significance of microvessels detected by in vivo optical coherence tomography within human atherosclerotic coronary arterial intima: a study with multimodality intravascular imagings

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Abstract

The significance of microvessels within atherosclerotic plaques is not yet fully clarified. Associated with plaque vulnerability. The aim of this study is to examine tissue characteristics of plaque with microvessels detected by optical coherence tomography (OCT) by use of a commercially available color-coded intravascular ultrasound (IVUS) and coronary angioscopy (CAS). The subjects examined comprised of 44 patients with stable angina pectoris who underwent percutaneous coronary intervention. Microvessels were defined as a tiny tubule with a diameter of 50–300 µm detected over three or more frames in OCT. We compared the total volume of microvessels with tissue component such as fibrotic, lipidic, necrotic, and calcified volume and the number of yellow plaque. In IVUS analysis, % necrotic volume and % lipidic volume were significantly correlated and % fibrotic volume was inversely significantly correlated with the total volume of microvessel (r = 0.485, p = 0.0009; r = 0.401, p = 0.007; r = − 0.432, p = 0.003, respectively). The number of plaque with an angioscopic yellow grade of two or more was significantly correlated with the total volume of microvessel (r = 0.461, p = 0.002). The greater the luminal volume of microvessels, the more the percent content of necrotic/lipidic tissue volume within plaque and the more the number of yellow plaques. These data suggested that microvessels within coronary plaque might be related to plaque vulnerability.

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References

  1. Davies MJ, Thomas A (1984) Thrombosis and acute coronary-artery lesions in sudden cardiac ischemic death. N Engl J Med 310(18):1137–1140

    Article  CAS  PubMed  Google Scholar 

  2. Fuster V, Badimon L, Badimon JJ, Chesebro JH (1992) The pathogenesis of coronary artery disease and the acute coronary syndromes. N Engl J Med 326(5):310–318

    Article  CAS  PubMed  Google Scholar 

  3. Falk E, Shah PK, Fuster V (1995) Coronary plaque disruption. Circulation 92(3):657–671

    Article  CAS  PubMed  Google Scholar 

  4. Little WC, Constantinescu M, ApplegateRJ KMA, Burrows MT, Kahl FR, Santamore WP (1988) Can coronary angiography predict the site of a subsequent myocardial infarction in patients with mild-to-moderate coronary artery disease? Circulation 78(5Pt 1):1157–1166

    Article  CAS  PubMed  Google Scholar 

  5. 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  CAS  PubMed  Google Scholar 

  6. Nissen SE, Yock P (2001) Intravascular ultrasound: novel pathophysiological insights and current clinical applications. Circulation 103(4):604–616

    Article  CAS  PubMed  Google Scholar 

  7. Gertz SD, Roberts WC (1990) Hemodynamic shear force in rupture of coronary arterial atherosclerotic plaques. Am J Cardiol 66(19):1368–1372

    Article  CAS  PubMed  Google Scholar 

  8. 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  CAS  PubMed  Google Scholar 

  9. Davies MJ, Richardson PD, Woolf N, Katz DR, Mann J (1993) Risk of thrombosis in human atherosclerotic plaques: role of extracellular lipid, macrophage, and smooth muscle cell content. Br Heart J 69(5):377–381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Lendon CL, Davies MJ, Born GV, Richardson PD (1991) Atherosclerotic plaque caps are locally weakened when macrophages density is increased. Atherosclerosis 87(1):87–90

    Article  CAS  PubMed  Google Scholar 

  11. Ehara S, Kobayashi Y, Yoshiyama 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 (2004) Spotty calcification typifies the culprit plaque in patients with acute myocardial infarction: anintravascular ultrasound study. Circulation 110(22):3424–3429

    Article  PubMed  Google Scholar 

  12. Kitabata H, Tanaka A, Kubo T, Takarada S, Kashiwagi M, Tsujioka H, Ikejima H, Kuroi A, Kataiwa H, Ishibashi K, Komukai K, Tanimoto T, Ino Y, Hirata K, Nakamura N, Mizukoshi M, Imanishi T, Akasaka T (2010) Relation of microchannel structure identified by optical coherence tomography to plaque vulnerability in patients with coronary artery disease. Am J Cardiol 105(12):1673–1678

    Article  PubMed  Google Scholar 

  13. Uemura S, Ishigami K, Soeda T, Okayama S, Sung JH, NakagawaH SS, Takeda Y, Kawata H, Horii M, Saito Y (2012) Thin-capfibroatheroma and microchannel findings in optical coherence tomography correlate with subsequent progression of coronary atheromatous plaques. Eur Heart J 33(1):78–85

    Article  PubMed  Google Scholar 

  14. KolodgieFD GHK, Burke AP, Fowler DR, Kruth HS, Weber DK, Farb A, Guerrero LJ, Hayase M, Kutys R, Narula J, Finn AV, Virmani R (2003) Intraplaque hemorrhage and progression of coronary atheroma. N Engl J Med 349(24):2316–2325

    Article  Google Scholar 

  15. Purushothaman KR, Sanz J, Zias E, Fuster V, Moreno PR (2006) Atherosclerosis neovascularization and imaging. Curr Mol Med 6(5):549–556

    Article  CAS  PubMed  Google Scholar 

  16. 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

    Article  CAS  PubMed  Google Scholar 

  17. Finn AV, Nakano M, Narula J, Kolodgie FD, Virmani R (2010) Concept of vulnerable/unstable plaque. Arterioscler Thromb Vasc Biol 30(7):1282–1292

    Article  CAS  PubMed  Google Scholar 

  18. Moulton KS, Vakili K, Zurakowski D, Soliman M, Butterfield C, Sylvin E, Lo KM, Gillies S, Javaherian K, Folkman J (2003) Inhibition of plaque neovascularization reduces macrophage accumulation and progression of advanced atherosclerosis. Proc Natl Acad Sci U S A 100(8):4736–4741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Badimon JJ, Fuster V, Chesebro JH, Badimon L (1993) Coronary atherosclerosis. A multifactorial disease. Circulation 87(3 Suppl):113–116

    Google Scholar 

  20. Virmani R, Burke AP, Kolodgie FD, Farb A (2003) Pathology of the thin-cap fibroatheroma: a type of vulnerable plaque. J Interv Cardiol 16(3):267–272

    Article  PubMed  Google Scholar 

  21. Sluimer JC, Kolodgie FD, Bijnens AP, Maxfield K, Pacheco E, Kutys B, Duimel H, Frederik PM, van Hinsbergh VW, Virmani R, Daemen MJ (2009) Thin-walled microvessels in human coronary atherosclerotic plaques show incomplete endothelial junctions relevance of compromised structural integrity for intraplaque microvascular leakage. J Am Coll Cardiol 53(17):1517–1527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Lu J, Duan W, Qiao A (2015) Finite element analysis of mechanics of neovessels with intraplaque hemorrhage in carotid atherosclerosis. Biomed Eng Online 14(Suppl 1):S3

    Article  PubMed  PubMed Central  Google Scholar 

  23. Horie N, Morofuji Y, Morikawa M, Tateishi Y, Izumo T, Hayashi K, Tsujino A, Nagata I (2015) Communication of inwardly projecting neovessels with the lumen contributes to symptomatic intraplaque hemorrhage in carotid artery stenosis. J Neurosurg 123(5):1125–1132

    Article  CAS  PubMed  Google Scholar 

  24. Alviar CL, Tellez A, Wallace-Bradley D, Lopez-Berestein G, Sanguino A, Schulz DG, Builes A, Ballantyne CM, Yang CY, Kaluza GL, Granada JF (2010) Impact of adventitial neovascularisation on atherosclerotic plaque composition and vascular remodelling in a porcine model of coronary atherosclerosis. EuroIntervention 5(8):981–988

    Article  PubMed  Google Scholar 

  25. Vorpahl M, Nakano M, Virmani R (2010) Small black holes in optical frequency domain imaging matches intravascular neoangiogenesis formation in histology. Eur Heart J 31(15):1889.

  26. Jang IK, Tearney GJ, MacNeill B, Takano M, Moselewski F, Iftima N, Shishkov M, Houser S, Aretz HT, Halpern EF, Bouma BE (2005) In vivo characterization of coronary atherosclerotic plaque by use of optical coherence tomography. Circulation 111(12):1551–1555

    Article  PubMed  PubMed Central  Google Scholar 

  27. Hirayama A, Saito S, Ueda Y, Takayama T, Honye J, Komatsu S, Yamaguchi O, Li Y, Yajima J, Nanto S, Takazawa K, Kodama K (2009) Qualitative and quantitative changes in coronary plaque associated with atorvastatin therapy. Circ J 73(4):718–725

    Article  CAS  PubMed  Google Scholar 

  28. Kodama K, Komatsu S, Ueda Y, Takayama T, Yajima J, Nanto S, Matsuoka H, Saito S, Hirayama A (2010) Stabilization and regression of coronary plaques treated with pitavastatin proven by angioscopy and intravascular ultrasound–the TOGETHAR trial. Circ J74(9):1922–1928

    Article  Google Scholar 

  29. Ueda Y, Asakura M, Yamaguchi O, Hirayama A, Hori M, Kodama K (2001) The healing process of infarct-related plaques Insights from 18 months of serial angioscopic follow-up. J Am Coll Cardiol 38(7):1916–1922

    Article  CAS  PubMed  Google Scholar 

  30. Moreno PR, Purushothaman KR, Zias E, Sanz J, Fuster V (2006) Neovascularization in human atherosclerosis. Curr Mol Med 6(5):457–477

    Article  CAS  PubMed  Google Scholar 

  31. Fittipaldi S, Vasuri F, Degiovanni A, Pini R, Mauro R, Faggioli G, D’Errico-Grigioni A, Stella A, Pasquinelli G (2014) Nestin and WT1 expression in atheromathous plaque neovessels: association with vulnerability. Histol Histopathol 29(12):1565–1573

    PubMed  Google Scholar 

  32. Slevin M, Krupinski J, Badimon L (2009) Controlling the angiogenic switch in developing atherosclerotic plaques: possible targets for therapeutic intervention. J Angiogenes Res 1:4

    Article  PubMed  PubMed Central  Google Scholar 

  33. Turu MM, Slevin M, Matou S, West D, Rodriguez C, Luque A, Grau-Olivares M, Badimon L, Martinez-Gonzalez J, Krupinski J (2008) C-reactive protein exerts angiogenic effects on vascular endothelial cells and modulates associated signalling pathways and gene expression. BMC Cell Biol 9:47

    Article  PubMed  PubMed Central  Google Scholar 

  34. Williams KJ, Feig JE, Fisher EA (2008) Rapid regression of atherosclerosis:insights from the clinical and experimental literature. Nat Clin Pract Cardiovasc Med 5(2):91–102

    Article  CAS  PubMed  Google Scholar 

  35. Stone GW, Maehara A, Lansky AJ, de Bruyne B, Cristea E, Mintz GS, Mehran R, McPherson J, Farhat N, Marso SP, Parise H, Templin B, White R, Zhang Z, Serruys PW (2011) A prospective natural-history study of coronary atherosclerosis. N Engl J Med 364(3):226–235

    Article  CAS  PubMed  Google Scholar 

  36. Schoenhagen P, Ziada KM, Kapadia SR, Crowe TD, Nissen SE, Tuzcu EM (2000) Extent and direction of arterial remodeling in stable versus unstable coronary syndromes : an intravascular ultrasound study. Circulation 101(6):598–603

    Article  CAS  PubMed  Google Scholar 

  37. Naghavi M, Libby P, Falk E, Casscells SW, Litovsky S, Rumberger J, Badimon JJ, Stefanadis C, Moreno P, Pasterkamp G, Fayad Z, Stone PH, Waxman S, Raggi P, Madjid M, Zarrabi A, Burke A, Yuan C, Fitzgerald PJ, Siscovick DS, de Korte CL, Aikawa M, Juhani Airaksinen KE, Assmann G, Becker CR, Chesebro JH, Farb A, Galis ZS, Jackson C, Jang IK, Koenig W, Lodder RA, March K, Demirovic J, Navab M, Priori SG, Rekhter MD, Bahr R, Grundy SM, Mehran R, Colombo A, Boerwinkle E, Ballantyne C, Insull W Jr, Schwartz RS, Vogel R, Serruys PW, Hansson GK, Faxon DP, Kaul S, Drexler H, Greenland P, Muller JE, Virmani R, Ridker PM, Zipes DP, Shah PK, Willerson JT (2003) From vulnerable plaqueto vulnerable patient: a call for new definitions and risk assessment strategies: part I. Circulation 108(14):1664–1672

    Article  PubMed  Google Scholar 

  38. Olson FJ, Stromberg S, Hjelmgren O, Kjelldahl J, Fagerberg B, Bergstrom GM (2011) Increased vascularization of shoulder regionsofcarotid atherosclerotic plaques from patients with diabetes. J Vasc Surg 54(5):1324-1331.e5

    Article  PubMed  Google Scholar 

  39. Arderiu G, PenaE AR, Juan-Babot O, Badimon L (2011) Tissue factor regulates microvessel formation and stabilization by induction of chemokine (C-C motif) ligand 2 expression. Arterioscler Thromb Vasc Biol 31(11):2607–2615

    Article  CAS  PubMed  Google Scholar 

  40. Purushothaman KR, Purushothaman M, Muntner P, Lento PA, O’Connor WN, Sharma SK, Fuster V, Moreno PR (2011) Inflammation, neovascularization and intra-plaque hemorrhage are associated with increased reparative collagen content: implication for plaque progression in diabetic atherosclerosis. Vasc Med 16(2):103–108

    Article  PubMed  Google Scholar 

  41. Ohtani T, Ueda Y, Mizote I, Oyabu J, Okada K, Hirayama A, Kodama K (2006) Number of yellow plaques detected in a coronary artery is associated with future risk of acute coronary syndrome: detection of vulnerable patients by angioscopy. J Am Coll Cardiol 47(11):2194–2200

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Division of Cardiology, Department of Medicine, Nihon University School of Medicine, 30-1 Oyaguchi-kamicho, Itabashi-ku, Tokyo, 173-8610, Japan

    Toshihiko Nishida, Takafumi Hiro, Tadateru Takayama, Mitsumasa Sudo, Hironori Haruta, Daisuke Fukamachi, Atsushi Hirayama & Yasuo Okumura

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  1. Toshihiko Nishida
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  2. Takafumi Hiro
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Correspondence to Takafumi Hiro.

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Hiro T and Hirayama A also work for Department of Advanced Cardiovascular Imaging, Nihon University School of Medicine, endowed by Boston Scientific Japan, Co. Ltd.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee (Nihon University Itabashi Hospital, Clinical Research Judging Committee, RK-160112–12) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Nishida, T., Hiro, T., Takayama, T. et al. Clinical significance of microvessels detected by in vivo optical coherence tomography within human atherosclerotic coronary arterial intima: a study with multimodality intravascular imagings. Heart Vessels 36, 756–765 (2021). https://doi.org/10.1007/s00380-020-01756-0

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