Evidence of woven bone formation in carotid artery plaques
Article Sidebar
Main Article Content
Abstract
Objective: Plaque morphology plays an important prognostic role in the occurrence of cerebrovascular events. Echolucent and heterogeneous plaques, in particular, carry an increased risk of subsequent stroke. Depending on the quality of the plaque echogenicity based on B-mode ultrasound examination, carotid plaques divide into a soft lipid-rich plaque and a hard plaque with calcification. The aim of this study was to investigate structural changes in the basement membrane of different carotid artery plaque types.
Patients and methods: Biopsies were taken from 10 male patients (average age; 75 + 1 years) and 7 females (68 + 3 years). The study population included patients suffering from a filiform stenosis of the carotid artery, 8 patients with acute cerebrovascular events and 9 with asymptomatic stenosis. Scanning electron and polarised light microscopic investigations were carried out on explanted plaques to determine the morphology of calcified areas in vascular lesions.
Results: By means of scanning electron microscopy, multiple foci of local calcification were identified. The endothelial layer was partially desquamated from the basement membrane and showed island-like formations. Polarised light microscopy allows us to distinguish between soft plaques with transparent structure and hard plaques with woven bone formation.
Conclusion: The major finding of our study is the presence of woven bone tissue in hard plaques of carotid arteries, which may result from pathological strains or mechanical overloading of the collagen fibers. These data suggest a certain parallel with sclerosis of human aortic valves due to their similar morphological characteristics.
Article Details
Copyright (c) 2021 Masoud M, et al.
This work is licensed under a Creative Commons Attribution 4.0 International License.
Moroni F, Ammirati E, Norata GD, Magnoni M, Camici PG. The role of monocytes and macrophages in human atherosclerosis, plaque neoangiogenesis, and atherothrombosis Mediators Inflamm. 2019; 7434376. PubMed: https://pubmed.ncbi.nlm.nih.gov/31089324/ DOI: https://doi.org/10.1155/2019/7434376
Zhu G, Hom J, Li Y, Jiang B, Rodriguez F, et al. Carotid plaque imaging and the risk of atherosclerotic cardiovascular disease. Cardiovasc Diagn Ther. 2020; 10: 1048–1067. PubMed: https://pubmed.ncbi.nlm.nih.gov/32968660/ DOI: https://doi.org/10.21037/cdt.2020.03.10
Johri AM, Nambi V, Naqvi TZ, Feinstein SB, Kim ESH, et al. Recommendations for the assessment of carotid arterial plaque by ultrasound for the characterization of atherosclerosis and evaluation of cardiovascular risk. JASE. 2020; 33: 917-933. PubMed: https://pubmed.ncbi.nlm.nih.gov/32600741/ DOI: https://doi.org/10.1016/j.echo.2020.04.021
Momjian, S, Lalive, P, Sztajzel, R. Carotid plaque: comparison between visual and grey-scale median analysis. Ultrasound Med Biol. 2003; 29: 961-966. PubMed: https://pubmed.ncbi.nlm.nih.gov/12878241/ DOI: https://doi.org/10.1016/S0301-5629(03)00905-0
Mughal MM, Khan MK, DeMarco JK. Symptomatic and asymptomatic carotid artery plaque, Expert Rev Cardiovasc Ther. 2011; 9: 1315–1330. PubMed: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3243497/ DOI: https://doi.org/10.1586/erc.11.120
Mirzaie M, Schultz M, Schwartz P. Evidence of woven bone formation in heart valve disease. Ann Thorac Cardiovasc Surg. 2003; 9: 163-169. PubMed: https://pubmed.ncbi.nlm.nih.gov/12875637/
Von Hagens G. Impregnation of soft biological specimens with thermostetting resins and elastomers. Anat Rec. 1979; 94: 247–255. PubMed: https://pubmed.ncbi.nlm.nih.gov/464325/ DOI: https://doi.org/10.1002/ar.1091940206
Schultz M, Drommer R. Possibilities of preparation production from the craniofacial area for macroscopic and microscopic examination using new plastics techniques. Exp Mund-KieferGesichts Chir. 1983; 28: 95–97.
Meershoek A, van Dijk RA, Verhage S. Hamming JF, van den Bogaerdt AJ, et al. Histological evaluation disqualifies IMT and calcification scores as surrogates for grading coronary and aortic atherosclerosis. Int J Cardiol. 2016; 224: 328-334. PubMed: https://pubmed.ncbi.nlm.nih.gov/27668706/ DOI: https://doi.org/10.1016/j.ijcard.2016.09.043
Nambi V, Chambless L, Folsom AR. He M, Hu Y, et al. Carotid intima-media thickness and presence or absence of plaque improves prediction of coronary heart disease risk: The ARIC (Atherosclerosis risk in communities) study. J Am Coll Cardiol. 2010; 55: 1600-1607. PubMed: https://pubmed.ncbi.nlm.nih.gov/20378078/ DOI: https://doi.org/10.1016/j.jacc.2009.11.075
Toutouzas, K, Karanasos, A, Tousoulis, D. Optical coherence tomography for the detection of the vulnerable plaque. Eur Cardiol. 2016; 11: 90–95. PubMed: https://pubmed.ncbi.nlm.nih.gov/30310454/ DOI: https://doi.org/10.15420/ecr.2016:29:2
Hua Y. Chinese guidance on vascular ultrasound examination in stroke. Chin J Med Ultrasound. 2015; 8: 599-610.
Pelisek J, Wendorff H, Wendorff C. Age-associated changes in human carotid atherosclerotic plaques. Ann Med. 2016; 48: 541-551. PubMed: https://pubmed.ncbi.nlm.nih.gov/27595161/ DOI: https://doi.org/10.1080/07853890.2016.1204468
Jinnouchi H, Sato Y, Sakamoto A, Cornelissen A, Mori M, et al. Calcium deposition within coronary atherosclerotic lesion: Implications for plaque stability. Finn Atherosclerosis. 2020; 306: 85-95. PubMed: https://pubmed.ncbi.nlm.nih.gov/32654790/ DOI: https://doi.org/10.1016/j.atherosclerosis.2020.05.017
Antipova D, Eadie L, Makin S. The use of transcranial ultrasound and clinical assessment to diagnose ischaemic stroke due to large vessel occlusion in remote and rural areas, PLoS One. 2020; 15: e0239653. PubMed: https://pubmed.ncbi.nlm.nih.gov/33007053/ DOI: https://doi.org/10.1371/journal.pone.0239653
Ahluwalia N, Genoux A, Ferrieres J, Perret B, Carayol M, et al. Iron status is associated with carotid atherosclerotic plaques in middle-aged adults. J Nutr. 2010; 140: 812–816. PubMed: https://pubmed.ncbi.nlm.nih.gov/20181783/ DOI: https://doi.org/10.3945/jn.109.110353
Sun B, Zhao H, Liu X, Lu Q, Zhao X, et al. Elevated hemoglobin A1c is associated with carotid plaque vulnerability: Novel findings from magnetic resonance imaging study in hypertensive stroke patients. Sci Rep. 2016; 6: 33246. PubMed: https://pubmed.ncbi.nlm.nih.gov/27629481/ DOI: https://doi.org/10.1038/srep33246
Brophy ML, Dong Y, Wu H, Rahman HNA, Song K, et al. Eating the dead to keep atherosclerosis at bay. Front Cardiovasc Med. 2017; 4: 2. PubMed: https://pubmed.ncbi.nlm.nih.gov/28194400/ DOI: https://doi.org/10.3389/fcvm.2017.00002
Vaidya K, Martínez G, Patel S. The role of colchicine in acute coronary syndromes. Clin Ther. 2019; 41: 11-20. PubMed: https://pubmed.ncbi.nlm.nih.gov/30185392/ DOI: https://doi.org/10.1016/j.clinthera.2018.07.023
Ruddy JM, Ikonomidis JS, Jones JA. Multidimensional contribution of matrix metalloproteinases to atherosclerotic plaque vulnerability: Multiple mechanisms of inhibition to promote stability. J Vasc Res. 2016; 53: 1-16. PubMed: https://pubmed.ncbi.nlm.nih.gov/27327039/ DOI: https://doi.org/10.1159/000446703
Alhendi AMN, Patrikakis M, Daub CO, Kawaji H, Itoh M, et al. Promoter usage and dynamics in vascular smooth muscle cells Exposed to fibroblast growth factor-2 or interleukin-1β. Sci Rep. 2018; 8: 13164. PubMed: https://pubmed.ncbi.nlm.nih.gov/30177712/ DOI: https://doi.org/10.1038/s41598-018-30702-4
Veseli BE, Perrotta P, De Meyer GRA, Roth L, der Donckt CV, et al. Animal models of atherosclerosis. Eur J Pharmacol. 2017; 816: 3-13. PubMed: https://pubmed.ncbi.nlm.nih.gov/28483459/ DOI: https://doi.org/10.1016/j.ejphar.2017.05.010
Nikkari ST, O'Brien KD, Ferguson M, Hatsukami T, Welgus HG, et al. Interstitial collagenase (MMP-1) expression in human carotid atherosclerosis. Circulation. 1995; 92: 1393-1398. PubMed: https://pubmed.ncbi.nlm.nih.gov/7664418/ DOI: https://doi.org/10.1161/01.CIR.92.6.1393
Chen X, Cao X, Jiang H, Che X, Xu X, et al. SIKVAV-modified chitosan hydrogel as a skin substitutes for wound closure in mice. Molecules. 2018; 23: 2611. PubMed: https://pubmed.ncbi.nlm.nih.gov/30314388/ DOI: https://doi.org/10.3390/molecules23102611
Cheng S, Wang D, Jin Ke J, Ma L, Zhou J, et al. Improved in vitro angiogenic behavior of human umbilical vein endothelial cells with oxidized polydopamine coating. Colloid Surface B. 2020; 194: 111176. PubMed: https://pubmed.ncbi.nlm.nih.gov/32540767/ DOI: https://doi.org/10.1016/j.colsurfb.2020.111176
Chia JS, Du JL, Hsu WB, Sun A, Chiang CP, et al. Inhibition of metastasis, angiogenesis, and tumor growth by Chinese herbal cocktail Tien-Hsien Liquid. BMC Cancer. 2010; 10: 175. PubMed: https://pubmed.ncbi.nlm.nih.gov/20429953/ DOI: https://doi.org/10.1186/1471-2407-10-175
Latha S, Samiappan D, Kumar R. Carotid artery ultrasound image analysis: A review of the literature. Proc Inst Mech Eng H. 2020; 234: 417-443. PubMed: https://pubmed.ncbi.nlm.nih.gov/31960771/ DOI: https://doi.org/10.1177/0954411919900720
Saxena A, Kwee Ng EY, Teik S. Imaging modalities to diagnose carotid artery stenosis: progress and prospect, Bio Med Eng. 2019; 18: 66. PubMed: https://pubmed.ncbi.nlm.nih.gov/31138235/ DOI: https://doi.org/10.1186/s12938-019-0685-7
Banaei A. The comparison between digital subtraction angiography, CT angiography, and doppler ultrasonography in evaluation and assessment of carotid artery stenosis. Ann Mil Health Sci Res. 2017; 15: e61661. DOI: https://doi.org/10.5812/amh.61661
Correia M, Maresca D, Goudot G, Villemain O, Bizé A, et al. Quantitative imaging of coronary flows using 3D ultrafast doppler coronary angiography. Phys Med Biol. 2020; 65: 105013. PubMed: https://pubmed.ncbi.nlm.nih.gov/32340010/ DOI: https://doi.org/10.1088/1361-6560/ab8d78
Morbiducci U, Kok AM, Kwak BR. Atherosclerosis at arterial bifurcations: Evidence for the role of haemodynamics and geometry. Thrombosis and Haemostasis. 2016; 115: 484492. PubMed: https://pubmed.ncbi.nlm.nih.gov/26740210/ DOI: https://doi.org/10.1160/th15-07-0597
Monckeberg JG. Normal histological construction and sclerosis of aortic valves. Virchows Archiv Pathol Anat Physiol. 1904; 176: 472-514. DOI: https://doi.org/10.1007/BF02041318
Virchow R. Cellular pathology: as based upon physiological and pathological histology. Nutr Rev. 1989; 47: 23-25. PubMed: https://pubmed.ncbi.nlm.nih.gov/2649802/ DOI: https://doi.org/10.1111/j.1753-4887.1989.tb02747.x
Yang P, Troncone L, Augur ZM, Kim SSJ, McNeil ME, et al. The role of bone morphogenetic protein signaling in vascular calcification. Bone. 2020; 115542. PubMed: https://pubmed.ncbi.nlm.nih.gov/32736145/ DOI: https://doi.org/10.1016/j.bone.2020.115542
Sun M, Chang Q, Xin M. Endogenous bone morphogenetic protein 2 plays a role in vascular smooth muscle cell calcification induced by interleukin 6 in vitro. Int J Immunopathol Pharmacol. 2017; 30: 227–237. PubMed: https://pubmed.ncbi.nlm.nih.gov/28134597/ DOI: https://doi.org/10.1177/0394632016689571
Nagy E, Eriksson P, Yousry M, Caidahl K, Ingelsson E, et al. Valvular osteoclasts in calcification and aortic valve stenosis severity. Int J Cardiol. 2013; 168: 2264-2271. PubMed: https://pubmed.ncbi.nlm.nih.gov/23452891/ DOI: https://doi.org/10.1016/j.ijcard.2013.01.207
Low EL, Baker AH, Bradshaw AC. TGFβ, smooth muscle cells and coronary artery disease: a review. Cell Signal. 2019; 53: 90-101. PubMed: https://pubmed.ncbi.nlm.nih.gov/30227237/ DOI: https://doi.org/10.1016/j.cellsig.2018.09.004
Shioi A, Ikari Y. Plaque calcification during atherosclerosis progression and regression. J Atheroscler Thromb. 2018; 25: 294–303. PubMed: https://pubmed.ncbi.nlm.nih.gov/29238011/ DOI: https://doi.org/10.5551/jat.RV17020