Abstract
The initial process of atherosclerotic development has not been systematically evaluated. This study aimed to observe atherosclerotic progression from normal vessel wall (NVW) to atherosclerotic plaque and examine local factors associated with such progression using > 5-year long-term follow-up data obtained by serial optical coherence tomography (OCT). A total of 49 patients who underwent serial OCT for lesions with NVW over 5 years (average: 6.9 years) were enrolled. NVW was defined as a vessel wall with an OCT-detectable three-layer structure and intimal thickness ≤ 300 μm. Baseline and follow-up OCT images were matched, and OCT cross sections with NVW > 30° were enrolled. Cross sections were diagnosed as “progression” when the NVW in these cross sections was reduced by > 30° at > 5-year follow-up. Atherogenic progression from NVW to atherosclerotic plaque was observed in 40.8% of enrolled cross sections. The incidence of microchannels in an adjacent atherosclerotic plaque within the same cross section (6.7 vs. 3.3%; p = 0.046) and eccentric distribution of atherosclerotic plaque (25.0 vs. 12.6%; p < 0.001) at baseline was significantly higher in cross sections with progression than in those without. Cross sections with progression exhibited significantly higher NVW intimal thickness at baseline than cross sections without progression (200.1 ± 53.7 vs. 180.2 ± 59.6 μm; p < 0.001). Multivariate analysis revealed that the presence of microchannels in an adjacent atherosclerotic plaque, eccentric distribution of atherosclerotic plaque, and greater NVW intimal thickness at baseline were independently associated with progression at follow-up. The presence of microchannels in an adjacent atherosclerotic plaque, eccentric distribution of atherosclerotic plaque, and greater NVW intimal thickness were potentially associated with initial atherosclerotic development from NVW to atherosclerotic plaque.
Similar content being viewed by others
Abbreviations
- CAG:
-
Coronary angiography
- DIT:
-
Diffuse intimal thickening
- ESS:
-
Endothelial shear stress
- FD-OCT:
-
Frequency-domain optical coherence tomography
- hsCRP:
-
High-sensitivity C-reactive protein
- LDLc:
-
Low-density lipoprotein cholesterol
- NVW:
-
Normal vessel wall
- OCT:
-
Optical coherence tomography
- PCI:
-
Percutaneous coronary intervention
- SMCs:
-
Smooth muscle cells
- TD-OCT:
-
Time-domain optical coherence tomography
References
Dohi T, Maehara A, Moreno PR, Baber U, Kovacic JC, Limaye AM, Ali ZA, Sweeny JM, Mehran R, Dangas GD, Xu K, Sharma SK, Mintz GS, Kini AS (2015) The relationship among extent of lipid-rich plaque, lesion characteristics, and plaque progression/regression in patients with coronary artery disease: a serial near-infrared spectroscopy and intravascular ultrasound study. Eur Heart J Cardiovasc Imaging 16:81–87
Endo H, Dohi T, Miyauchi K, Kuramitsu S, Kato Y, Okai I, Yokoyama M, Yokoyama T, Ando K, Okazaki S, Shimada K, Suwa S, Daida H (2019) Clinical significance of non-culprit plaque regression following acute coronary syndrome: a serial intravascular ultrasound study. J Cardiol 74:102–108
Tearney GJ, Regar E, Akasaka T, Adriaenssens T, Barlis P, Bezerra HG, Bouma B, Bruining N, Cho JM, Chowdhary S, Costa MA, de Silva R, Dijkstra J, Di Mario C, Dudek D, Falk E, Feldman MD, Fitzgerald P, Garcia-Garcia HM, Gonzalo N, Granada JF, Guagliumi G, Holm NR, Honda Y, Ikeno F, Kawasaki M, Kochman J, Koltowski L, Kubo T, Kume T, Kyono H, Lam CC, Lamouche G, Lee DP, Leon MB, Maehara A, Manfrini O, Mintz GS, Mizuno K, Morel MA, Nadkarni S, Okura H, Otake H, Pietrasik A, Prati F, Raber L, Radu MD, Rieber J, Riga M, Rollins A, Rosenberg M, Sirbu V, Serruys PW, Shimada K, Shinke T, Shite J, Siegel E, Sonoda S, Suter M, Takarada S, Tanaka A, Terashima M, Thim T, Uemura S, Ughi GJ, van Beusekom HM, van der Steen AF, van Es GA, van Soest G, Virmani R, Waxman S, Weissman NJ, Weisz G, International Working Group for Intravascular Optical Coherence T (2012) Consensus standards for acquisition, measurement, and reporting of intravascular optical coherence tomography studies: a report from the International Working Group for Intravascular Optical Coherence Tomography Standardization and Validation. J Am Coll Cardiol 59:1058–1072
Jang IK, Bouma BE, Kang DH, Park SJ, Park SW, Seung KB, Choi KB, Shishkov M, Schlendorf K, Pomerantsev E, Houser SL, Aretz HT, Tearney GJ (2002) Visualization of coronary atherosclerotic plaques in patients using optical coherence tomography: comparison with intravascular ultrasound. J Am Coll Cardiol 39:604–609
Bezerra HG, Costa MA, Gualiumi G, Rollins AM, Simon DI (2009) Intracoronary optical coherence tomography: a comprehensive review: clinical and research applications. JACC Cardiovasc Interv 2:1035–1046
Berry C, L’Allier PL, Gre ́Goire Lespe ́Rance Levesque Ibrahim Tardif JJSRJC (2007) Comparison with intravascular ultrasound Comparison of intravascular ultrasound and quantitative coronary angiography for the assessment of coronary artery progression. Circulation 115:1851–1857
Matsumoto D, Shite J, Shinke T, Otake H, Tanino Y, Ogasawara D, Sawada T, Paredes OL, Hirata K, Yokoyama M (2007) Neointimal coverage of sirolimus-eluting stents at 6-month follow-up: evaluated by optical coherence tomography. Eur Heart J 28:961–967
Golinvaux N, Maehara A, Mintz GS, Lansky AJ, McPherson J, Farhat N, Marso S, De Bruyne B, Serruys PW, Templin B, Cheong WF, Aaskar R, Fahy M, Mehran R, Leon M, Stone GW (2012) An intravascular ultrasound appraisal of atherosclerotic plaque distribution in diseased coronary arteries. Am Heart J 163:624–631
Nakashima Y, Chen YX, Kinukawa N, Sueishi K (2002) Distributions of diffuse intimal thickening in human arteries: preferential expression in atherosclerosis-prone arteries from an early age. Virchows Arch 441:279–288
Kitabata H, Tanaka A, Kubo T, Takarada D, Kashiwagi M, Tsujioka H, Ikejima H, Kuroi A, Kataiwa H, Ishibashi K, Komukai K, Tanimoto T, Ino Y, Hirata K, Nakamura N, Mizukoshi M, ImanishibT AT (2010) Relation of microchannel structure identified by optical coherence tomography to plaque vulnerability in patients with coronary artery disease. Am J Cardiol 105:1673–1678
Tearney GJ, Yabushita H, Houser SL, Aretz HT, Jang IK, Schlendorf KH, Kauffman CR, Shishkov M, Halpern EF, Bouma BE (2003) Quantification of macrophage content in atherosclerotic plaques by optical coherence tomography. Circulation 107:113–119
Kaprio J, Norio R, Pesonen E, Sarna S (1993) Intimal thickening of the coronary arteries in infants in relation to family history of coronary artery disease. Circulation 87:1960–1968
Aikawa M, Sivam PN, Kuro-o M, Kimura K, Nakahara K, Takewaki S, Ueda M, Yamaguchi H, Yazaki Y, Periasamy M, Nagai R (1993) Human smooth muscle myosin heavy chain isoforms as molecular markers for vascular development and atherosclerosis. Circ Res 73:1000–1012
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 20:1262–1275
Otsuka F, Kramer MCA, Woudstra P, Yahagi K, Ladich E, Finn AV, De Winter RJ, Kolodgie FD, Wight TN, Davis HR, Joner M, Virmani R (2015) Natural progression of atherosclerosis from pathologic intimal thickening to late fibroatheroma in human coronary arteries: a pathology study. Atherosclerosis 241:772–782
Nakata A, Miyagawa J, Yamashita S, Nishida M, Tamura R, Yamamori K, Nakamura T, Nozaki S, Kameda-Takemura K, Kawata S, Taniguchi N, Higashiyama S, Matsuzawa Y (1996) Localization of heparin-binding epidermal growth factor-like growth factor in human coronary arteries. Possible roles of HB-EGF in the formation of coronary atherosclerosis. Circulation 94:2778–2786
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 53:1517–1527
Aoki T, Rodriguez-Porcel M, Matsuo Y, Cassar A, Kwon TG, Franchi F, Gulati R, Kushwaha SS, Lennon RJ, Lerman LO, Ritman EL, Lerman A (2015) Evaluation of coronary adventitial vasa vasorum using 3D optical coherence tomography—animal and human studies. Atherosclerosis 239:203–208
Taruya A, Tanaka A, Nishiguchi T, Matsuo Y, Ozaki Y, Kashiwagi M, Shiono Y, Orii M, Yamano T, Ino Y, Hirata K, Kubo T, Akasaka T (2015) Vasa vasorum restructuring in human atherosclerotic Plaque Vulnerability. J Am College of Cardiol 65:2469–2477
Subbotin VM (2016) Excessive intimal hyperplasia in human coronary arteries before intimal lipid depositions is the initiation of coronary atherosclerosis and constitutes a therapeutic target. Drug Discov Today 21:1578–1595
Nakashima Y, Fujii H, Sumiyoshi S, Wight TN, Sueishi K (2007) Early human atherosclerosis: accumulation of lipid and proteoglycans in intimal thickenings followed by macrophage infiltration. Arterioscler Thromb Vasc Biol 27:1159–1165
Yamagishi M, Umeno T, Hongo Y, Tsutsui H, Goto Y, Nakatani S, Miyatake K (1997) Intravascular ultrasonic evidence for importance of plaque distribution (eccentric vs circumferential) in determining distensibility of the left anterior descending artery. Am J Cardiol 79:1596–1600
Ge J, Chirillo F, Schwedtmann J, Görge G, Haude M, Baumgart D, Shah V, Von Birgelen C, Sack S, Boudoulas H, Erbel R (1999) Screening of ruptured plaques in patients with coronary artery disease by intravascular ultrasound. Heart 81:621–627
Von Birgelen C, Klinkhart W, Mintz GS, Papatheodorou A, Herrmann J, Baumgart D, Haude M, Wieneke H, Ge J, Erbel R (2001) Plaque distribution and vascular remodeling of ruptured and nonruptured coronary plaques in the same vessel: an intravascular ultrasound study in vivo. J Am Coll Cardiol 37:1864–1870
Davies PF (2008) Hemodynamic shear stress and the endothelium in cardiovascular pathophysiology. Nat Clin Pract Cardiovasc Med 6:16–26
Wentzel JJ, Chatzizisis YS, Gijsen FJH, Giannoglou GD, Feldman CL, Stone PH (2012) Endothelial shear stress in the evolution of coronary atherosclerotic plaque and vascular remodelling: current understanding and remaining questions. Cardiovasc Res 96:234–243
Papafaklis MI, Takahashi S, Antoniadis AP, Coskun AU, Tsuda M, Mizuno S, Andreou I, Nakamura S, Makita Y, Hirohata A, Saito S, Feldman CL, Stone PH (2015) Effect of the local hemodynamic environment on the de novo development and progression of eccentric coronary atherosclerosis in humans: insights from PREDICTION. Atherosclerosis 240:205–211
Acknowledgements
The OCT core laboratory in Kobe University, Japan served as the independent core lab for data analysis.
Funding
No grants were received from any funding agency in the public, commercial, or not-for-profit sectors.
Author information
Authors and Affiliations
Contributions
RT: conceptualization, resources, formal analysis, investigation, Methodology, writing—original draft, visualization. HO: conceptualization, methodology, writing—review and editing, supervision. HK: data curation. TT: resources. YN: resources. YT: resources. KY: resources. HY: resources. AN: investigation. HO: resources. YS: investigation. SN: resources. YM: resources. KT: resources. KH: project administration, supervision.
Corresponding author
Ethics declarations
Conflict of interest
H.O. and T.T. received a lecture fee from Abbott Vascular. K.H. received grant support from Abbott Vascular. Other authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Takeshige, R., Otake, H., Kawamori, H. et al. Progression from normal vessel wall to atherosclerotic plaque: lessons from an optical coherence tomography study with follow-up of over 5 years. Heart Vessels 37, 1–11 (2022). https://doi.org/10.1007/s00380-021-01889-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00380-021-01889-w