Atherosclerosis in Animals is a Separate Type of Atherosclerosis that has Nothing to do with the Two Types of Atherosclerosis in Humans

Main Article Content

Sergey Rusanov

Abstract

The article is presented in the form of a review and analysis of the literature, which additionally helps to reveal the mechanisms of the pathogenesis of the development of atherosclerosis in humans. A contemporary vision is refuted that animal models of atherosclerosis are completely similar to the two types of human atherosclerotic lesions. The use of incorrect information about the etiology and pathogenesis of atherosclerotic lesions in humans reduces and even completely interferes with the possibility to carry out effective treatment and prevention of cardiovascular diseases associated with atherosclerosis. The two types of human atherosclerotic plaques have very different characteristics compared to atherosclerotic plaques in animals. They have a completely different etiology, pathogenesis, have a completely different appearance and location relative to the artery wall, have a different structure of the fibrous cap, a different pathway of LDL and macrophages, a different location of lipid core, a different way and time of arterial occlusion, a different type of endothelial dysfunction, they interact in totally different way with the walls of the artery and still have many additional differences that make both human atherosclerotic lesions completely different from atherosclerotic lesion in animals. Types IV atherosclerotic lesions consist of one lipid core with molten extracellular lipid. Type V atherosclerotic lesions type is a long, concentric, soft, strong, elastic, yellow, uniform structure. Due to the large number of inconsistencies between atherosclerotic lesions in animals and the two types of atherosclerotic lesions in humans, it is neither possible nor reasonable to use animal models to study the development of atherosclerotic lesions in humans. The plaques appear in the lumen of the artery in just a few days, in places of a sharp narrowing of the artery caused by hyperstimulation of the nervous system. The plaques consist of LDL, which were glued together with fibrin filaments. It also doesn't allow to detect a very simple mechanism accountable for the pathological increase in LDL levels in people who do not have genetic abnormalities. This mechanism proposed by the author is described in the first article dedicated to the type V atherosclerotic lesions (“Cylindrical cholesterol plaque”).

Keywords: Atherosclerosis, LDL, Atherosclerotic plaque, Heart attack, Stroke, Artery dissection, Stress, Atherosclerosis in animals, Atherosclerosis in humans

Article Details

How to Cite
RUSANOV, Sergey. Atherosclerosis in Animals is a Separate Type of Atherosclerosis that has Nothing to do with the Two Types of Atherosclerosis in Humans. Medical Research Archives, [S.l.], v. 10, n. 4, apr. 2022. ISSN 2375-1924. Available at: <https://esmed.org/MRA/mra/article/view/2760>. Date accessed: 21 dec. 2024. doi: https://doi.org/10.18103/mra.v10i4.2760.
Section
Review Articles

References

1. Buja LM. Nikolai N. Anitschkow and the lipid hypothesis of atherosclerosis. Cardiovasc Pathol. 2014 May-Jun;23(3):183-4. doi: 10.1016/j.carpath.2013.12.004. Epub 2014 Jan 3. PMID: 24484612.
2. Steinberg D. Thematic review series: the pathogenesis of atherosclerosis. An interpretive history of the cholesterol controversy, part V: the discovery of the statins and the end of the controversy. J Lipid Res. 2006 Jul;47(7):1339-51. doi: 10.1194/jlr.R600009-JLR200. Epub 2006 Apr 3. PMID: 16585781.
3. Forouzanfar MH, Afshin A, Alexander LT, et al, and GBD 2015 Risk Factors Collaborators. Global, regional, and national comparative risk assessment of 79 behavioural, environmental and occupational, and metabolic risks or clusters of risks, 1990-2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet. 2016; 388:1659 724. https://doi.org/10.1016/S0140-6736(16)31679-8
4. Nakashima Y, Plump AS, Raines EW, Breslow JL, Ross R. ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arterioscler Thromb. 1994 Jan;14(1):133-40. doi: 10.1161/01.atv.14.1.133. PMID: 8274468.
5. Steinberg D. Thematic review series: the pathogenesis of atherosclerosis. An interpretive history of the cholesterol controversy: part I. J Lipid Res. 2004 Sep;45(9):1583-93. doi: 10.1194/jlr.R400003-JLR200. Epub 2004 Apr 21. PMID: 15102877.
6. Orekhov AN, Sobenin IA. Modified lipoproteins as biomarkers of atherosclerosis. Front Biosci (Landmark Ed). 2018 Mar 1;23(8):1422-1444. doi: 10.2741/4653. PMID: 29293443.
7. Gordon T, Castelli WP, Hjortland MC, Kannel WB, Dawber TR. High density lipoprotein as a protective factor against coronary heart disease. The Framingham Study. Am J Med. 1977 May;62(5):707-14. doi: 10.1016/0002-9343(77)90874-9. PMID: 193398.
8. Ross R. Atherosclerosis-an inflammatory disease. N Engl J Med. 1999; 340:115-26. https://doi.org/10.1056/NEJM199901143400207
9. Libby P, Ridker PM, Hansson GK; Leducq Transatlantic Network on Atherothrombosis. Inflammation in atherosclerosis: from pathophysiology to practice. J Am Coll Cardiol. 2009 Dec 1;54(23):2129-38. doi: 10.1016/j.jacc.2009.09.009. PMID: 19942084; PMCID: PMC2834169.
10. Gerhardt T, Ley K. Monocyte trafficking across the vessel wall. Cardiovasc Res. 2015 Aug 1;107(3):321-30. doi: 10.1093/cvr/cvv147. Epub 2015 May 19. PMID: 25990461; PMCID: PMC4592323.
11. Williams KJ, Tabas I. The response-to-retention hypothesis of early atherogenesis. Arterioscler Thromb Vasc Biol1995;15:551–561. doi: 10.1161/01.atv.15.5.551 Google Scholar Crossref PubMed
12. Liu X, Fan Y, Deng X. Effect of the endothelial glycocalyx layer on arterial LDL transport under normal and high pressure. J Theor Biol2011;283:71–81. doi: 10.1016/j.jtbi.2011.05.030 Google Scholar Crossref PubMed
13. Egawa G, Nakamizo S, Natsuaki Y, Doi H, Miyachi Y, Kabashima K. Intravital analysis of vascular permeability in mice using two-photon microscopy. Sci Rep2013;3:1932. Google Scholar Crossref PubMed
14. Chappell J, Harman JL, Narasimhan VM,, et al, Extensive Proliferation of a Subset of Differentiated, yet Plastic, Medial Vascular Smooth Muscle Cells Contributes to Neointimal Formation in Mouse Injury and Atherosclerosis Models. Circ Res. 2016 Dec 9;119(12):1313-1323. doi: 10.1161/CIRCRESAHA.116.309799. Epub 2016 Sep 28. PMID: 27682618; PMCID: PMC5149073.
15. Yu ZM, Deng XT, Qi RM, Xiao LY, Yang CQ, Gong T. Mechanism of Chronic Stress-induced Reduced Atherosclerotic Medial Area and Increased Plaque Instability in Rabbit Models of Chronic Stress. Chin Med J (Engl). 2018 Jan 20;131(2):161-170. doi: 10.4103/0366-6999.222322. PMID: 29336364; PMCID: PMC5776846.
16. Shiomi M, Ito T, Hasegawa M, Yoshida K, Gould KL. Novel insights into coronary lumen preservation during progression of coronary atherosclerosis in coronary atherosclerosis-prone rabbits. Coron Artery Dis. 2004 Nov;15(7):419-26. doi: 10.1097/00019501-200411000-00009. PMID: 15492591.
17. Zhang X, Chen X, Liang Z, Nie M, Yan Y, Zhao Q. Atorvastatin Promotes Macrocalcification, But Not Microcalcification in Atherosclerotic Rabbits: An 18F-NaF PET/CT Study. J Cardiovasc Pharmacol. 2021 Oct 1;78(4):544-550. doi: 10.1097/FJC.0000000000001088. PMID: 34651601.
18. Aldrighi JM, Lanz JR, Mansur AP, Martinez TL, Ramires JA. Effect of sexual steroids on the calcium content of aortic atherosclerotic plaque of oophorectomized rabbits. Braz J Med Biol Res. 2005 May;38(5):705-11. doi: 10.1590/s0100-879x2005000500007. Epub 2005 May 25. PMID: 15917951.
19. Aboshady I, Cody DD, Johnson EM, et al, Flat-panel versus 64-channel computed tomography for in vivo quantitative characterization of aortic atherosclerotic plaques. Int J Cardiol. 2012 May 3;156(3):295-302. doi: 10.1016/j.ijcard.2010.11.011. Epub 2010 Dec 24. PMID: 21185613; PMCID: PMC3074048.
20. Rusanov SE. The affection of the disturbance of the hydrodynamics of blood in case of stress on pathological increase of level of low density lipoproteins in blood. The formation of cylindrical plaques, and their participation in the development of acute ischemic disorders of heart and brain. Med Hypotheses. 2017 Sep;106:61-70. doi: 10.1016/j.mehy.2017.07.001. Epub 2017 Jul 3. PMID: 28818274.
21. Rusanov S (2021) New in the etiology, pathogenesis, prevention and treatment of atherosclerosis. The two different types of cholesterol plaques have nothing to do with each other. Ann Circ 6(1): 004-011. doi: https://dx.doi.org/10.17352/ac.000018
22. Stary HC, Chandler AB, Dinsmore RE, et al. A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Arterioscler Thromb Vasc Biol 1995; 15: 1512– 1531. Crossref PubMed Web of Science®Google Scholar
23. YouTube [Internet]. [place unknown]: The Neurosurgical Atlas by Aaron CohenGadol, M.D. [Video], Carotid Endarterectomy: Technical Pearls and Pitfalls. Link: https://bit.ly/3iiARiZ
24. YouTube [Internet]. [place unknown]: Dr. Sandeep Burathoki. [Video], Carotid Artery Stenting video. Link: https://bit.ly/3m5yJfH
25. YouTube [Internet]. [place unknown]: Alvin Wang. [Video], Carotid endarterectomy. Link: https://bit.ly/2YaVC9B
26. YouTube [Internet]. [place unknown]: NSPC Brain & Spine Surgery. [Video], Carotid surgery. Link: https://bit.ly/3kS6LVs
27. YouTube [Internet]. [place unknown]: Covenant Health. [Video], Carotid Endarterectomy. Link: https://bit.ly/2XV8Q9V
28. Rаsslаivаûŝаâ аnevrizmа аorty (translation - “Aortic dissecting aneurysm.”) g. Krasnodar 06 09 12. Link: https://bit.ly/39Mf6U9
29. Brinjikji W, Huston J, Rabinstein AA, Kim G, Lerman A, et al. (2016) Contemporary carotid imaging: from degree of stenosis to plaque vulnerability. Journal of Neurosurgery 124: 27-42. Link: https://bit.ly/2Y7cBcR
30. YouTube [Internet]. [Place unknown]: The Austin Diagnostic Clinic (ADCHealth). [Video], You and Your Stent: Link: https://bit.ly/3zLkZvv
31. YouTube [Internet]. [place unknown]: Galina Skokova. [Video], Endarterectomy; Link: https://bit.ly/3AVsrp5
32. YouTube [Internet]. [Place unknown]: Tech Insider. [Video], Devices ‘eat’ bad cholesterol. Link: https://bit.ly/3AT0rCD
33. YouTube [Internet]. [Place unknown]: Nejrokhirurgiya. [Video], Operatsiya - karotidnaya ehndarterehktomiya 2 (translation - “Operation – carotid endarterectomy 2”); Link: https://bit.ly/3ihaGt4
34. YouTube [Internet]. [Place unknown]: Surgery Department. [Video], 1 Аngioplastika: stentirovanie podklûčičnoj arterii 2. Karotidnaâ èndarterèktomiâ (translation - “1. Angioplasty: stenting of the subclavian artery 2. Carotid endarterectomy”); Link: https://bit.ly/39MfCkZ
35. YouTube [Internet]. [place unknown]: CTSNetVideo. [Video], Triple Coronary Endarterectomy in a Patient Undergoing CABG 2019 Link: https://bit.ly/3kSyGVf
36. YouTube [Internet]. [place unknown]: CTSNetVideo. [Video], CoronaryEndarterectomy of the Left Anterior Descending Artery. Link:https://bit.ly/3ARPvVM
37. YouTube [Internet]. [place unknown]: TAUVOD. [Video], Eradication of Atherosclerosis. Link: https://bit.ly/3kPQJLB
38. Diagnosis of calcinosis of coronary arteries by multispiral computed tomography. Link: https://bit.ly/3ulNQoR
39. YouTube [Internet]. [place unknown]: UCLA Health. [Video], Carotid Artery Disease & Stroke Angioplasty - Dr. May Nour | UCLAMDChat. Link: https://bit.ly/3iiPa7n
40. YouTube [Internet]. [place unknown]: Surg Spot. [Video], Karotidnaya endarterektomiya: hirurgicheskoe lechenie kak profi laktika ishemicheskogo insulta (translation - “Carotid endarterectomy: surgical treatment as prevention of ischemic stroke”); Link: https://bit.ly/3ii9NAn
41. File: Carotid Plaque.jpg Link: https://bit.ly/3igKkaq
42. YouTube [Internet]. [place unknown]: Natus Neuro. [Video], Natus TCD Webinar: TCD Continuous Monitoring during Carotid Endarterectomy Surgery. Link: https://bit.ly/3BpPHfh
43. Zhang F, Zhang R, Zhang X, et al, Comprehensive analysis of circRNA expression pattern and circRNA-miRNA-mRNA network in the pathogenesis of atherosclerosis in rabbits. Aging (Albany NY). 2018 Sep 6;10(9):2266-2283. doi: 10.18632/aging.101541. PMID: 30187887; PMCID: PMC6188486.
44. Niimi M, Keyamura Y, Nozako M, et al, Probucol inhibits the initiation of atherosclerosis in cholesterol-fed rabbits. Lipids Health Dis. 2013 Nov 4;12:166. doi: 10.1186/1476-511X-12-166. PMID: 24188322; PMCID: PMC4228370.
45. Tian J, Hu S, Sun Y, et al, A novel model of atherosclerosis in rabbits using injury to arterial walls induced by ferric chloride as evaluated by optical coherence tomography as well as intravascular ultrasound and histology. J Biomed Biotechnol. 2012;2012:121867. doi: 10.1155/2012/121867. Epub 2012 May 14. PMID: 22665979; PMCID: PMC3361737.
46. Prathap K. Diet-induced aortic atherosclerosis in Malaysian long-tailed monkeys (Macaca irus). J Pathol. 1975 Mar;115(3):163-74. doi: 10.1002/path.1711150306. PMID: 1151525.
47. Terpstra AH, Schutte JB, West CE. Prevention of hypercholesterolemia in cholesterol-fed chickens by high-casein and high-soybean protein diets. Atherosclerosis. 1983 Jan;46(1):95-104. doi: 10.1016/0021-9150(83)90168-5. PMID: 6682328.
48. Hedin U, Matic LP. Recent advances in therapeutic targeting of inflammation in atherosclerosis. J Vasc Surg. 2019 Mar;69(3):944-951. doi: 10.1016/j.jvs.2018.10.051. Epub 2018 Dec 24. PMID: 30591299.
49. Li B, Li W, Li X, Zhou H. Inflammation: A Novel Therapeutic Target/Direction in Atherosclerosis. Curr Pharm Des. 2017;23(8):1216-1227. doi: 10.2174/1381612822666161230142931. PMID: 28034355; PMCID: PMC6302344.
50. Soehnlein O, Libby P. Targeting inflammation in atherosclerosis - from experimental insights to the clinic. Nat Rev Drug Discov. 2021 Aug;20(8):589-610. doi: 10.1038/s41573-021-00198-1. Epub 2021 May 11. PMID: 33976384; PMCID: PMC8112476.
51. Hansson GK, Robertson AK, Söderberg-Nauclér C. Inflammation and atherosclerosis. Annu Rev Pathol. 2006;1:297-329. doi: 10.1146/annurev.pathol.1.110304.100100. PMID: 18039117.
52. Freigang S, Ampenberger F, Spohn G, et al, Nrf2 is essential for cholesterol crystal-induced inflammasome activation and exacerbation of atherosclerosis. Eur J Immunol. 2011 Jul;41(7):2040-51. doi: 10.1002/eji.201041316. Epub 2011 Jun 8. PMID: 21484785.
53. Poznyak A, Grechko AV, Poggio P, et al, The Diabetes Mellitus-Atherosclerosis Connection: The Role of Lipid and Glucose Metabolism and Chronic Inflammation. Int J Mol Sci. 2020 Mar 6;21(5):1835. doi: 10.3390/ijms21051835. PMID: 32155866; PMCID: PMC7084712.
54. Cornelissen A, Guo L, Sakamoto A, Virmani R, Finn AV. New insights into the role of iron in inflammation and atherosclerosis. EBioMedicine. 2019 Sep;47:598-606. doi: 10.1016/j.ebiom.2019.08.014. Epub 2019 Aug 12. PMID: 31416722; PMCID: PMC6796517.
55. Ding Z, Pothineni NVK, Goel A, Lüscher TF, Mehta JL. PCSK9 and inflammation: role of shear stress, pro-inflammatory cytokines, and LOX-1. Cardiovasc Res. 2020 Apr 1;116(5):908-915. doi: 10.1093/cvr/cvz313. Erratum in: Cardiovasc Res. 2021 Dec 14;: PMID: 31746997.
56. Zhong Y, Liu J, Huo WM, Duan WL, Wang X, Shang J. β-Elemene reduces the progression of atherosclerosis in rabbits. Chin J Nat Med. 2015 Jun;13(6):415-20. doi: 10.1016/S1875-5364(15)30034-0. PMID: 26073337.
57. Koike T, Koike Y, Yang D, et al, Human apolipoprotein A-II reduces atherosclerosis in knock-in rabbits. Atherosclerosis. 2021 Jan;316:32-40. doi: 10.1016/j.atherosclerosis.2020.11.028. Epub 2020 Nov 28. PMID: 33296791; PMCID: PMC7770079.
58. Zhang Y, Yuan M, Li HM, Lao M, Xu Z, Li GP. Testin on Atherosclerosis in Rabbits. Chin Med J (Engl). 2015 Jun 20;128(12):1662-5. doi: 10.4103/0366-6999.158370. PMID: 26063370; PMCID: PMC4733733.
59. Zimmer S, Grebe A, Bakke SS, et al, Cyclodextrin promotes atherosclerosis regression via macrophage reprogramming. Sci Transl Med. 2016 Apr 6;8(333):333ra50. doi: 10.1126/scitranslmed.aad6100. PMID: 27053774; PMCID: PMC4878149.
60. Yao J, Ho D, Calingasan NY, Pipalia NH, Lin MT, Beal MF. Neuroprotection by cyclodextrin in cell and mouse models of Alzheimer disease. J Exp Med. 2012 Dec 17;209(13):2501-13. doi: 10.1084/jem.20121239. Epub 2012 Dec 3. PMID: 23209315; PMCID: PMC3526350.
61. Zimmer S, Grebe A, Siril S. Bakke et al., Cyclodextrin promotes atherosclerosis regression via macrophage reprogramming. Science Translational Medicine: 8(333), 333ra50 doi:10.1126/scitranslmed.aad6100
62. Meng LB, Shan MJ, Qiu Y, Qi R, Yu ZM, Guo P, Di CY, Gong T. TPM2 as a potential predictive biomarker for atherosclerosis. Aging (Albany NY). 2019 Sep 5;11(17):6960-6982. doi: 10.18632/aging.102231. Epub 2019 Sep 5. PMID: 31487691; PMCID: PMC6756910.
63. Izidoro MA, Cecconi A, Panadero MI, et al, Plasma Metabolic Signature of Atherosclerosis Progression and Colchicine Treatment in Rabbits. Sci Rep. 2020 Apr 27;10(1):7072. doi: 10.1038/s41598-020-63306-y. PMID: 32341369; PMCID: PMC7184732.
64. Wang N, Xu X, Li H, Feng Q, Wang H, Kang YJ. Atherosclerotic lesion-specific copper delivery suppresses atherosclerosis in high-cholesterol-fed rabbits. Exp Biol Med (Maywood). 2021 Dec;246(24):2671-2678. doi: 10.1177/15353702211046541. Epub 2021 Sep 16. PMID: 34525859; PMCID: PMC8669168.
65. Li M, Zhang Y, Ren H, Zhang Y, Zhu X. Effect of clopidogrel on the inflammatory progression of early atherosclerosis in rabbits model. Atherosclerosis. 2007 Oct;194(2):348-56. doi: 10.1016/j.atherosclerosis.2006.11.006. Epub 2006 Dec 6. PMID: 17156785.
66. Bao L, Zhang Y, Wei G, et al, The anti-atherosclerotic effects of puerarin on induced-atherosclerosis in rabbits. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2015 Mar;159(1):53-9. doi: 10.5507/bp.2013.096. Epub 2014 Jan 27. PMID: 24510110.
67. Aghebati T, Badiee A, Mohammadpour AH, et al, Anti-atherosclerosis effect of different doses of CETP vaccine in rabbit model of atherosclerosis. Biomed Pharmacother. 2016 Jul;81:468-473. doi: 10.1016/j.biopha.2016.04.035. Epub 2016 Apr 30. PMID: 27261627.
68. Kong L, Luo C, Li X, Zhou Y, He H. The anti-inflammatory effect of kaempferol on early atherosclerosis in high cholesterol fed rabbits. Lipids Health Dis. 2013 Jul 29;12:115. doi: 10.1186/1476-511X-12-115. PMID: 23895132; PMCID: PMC3735477.
69. Zheng H, Li N, Ding Y, Miao P. Losartan alleviates hyperuricemia-induced atherosclerosis in a rabbit model. Int J Clin Exp Pathol. 2015 Sep 1;8(9):10428-35. PMID: 26617751; PMCID: PMC4637566.
70. Davis HR Jr, Lowe RS, Neff DR. Effects of ezetimibe on atherosclerosis in preclinical models. Atherosclerosis. 2011 Apr;215(2):266-78. doi: 10.1016/j.atherosclerosis.2011.02.010. Epub 2011 Feb 17. PMID: 21397230.
71. Herrero-Beaumont G, Marcos ME, Sánchez-Pernaute O, et al, Effect of chondroitin sulphate in a rabbit model of atherosclerosis aggravated by chronic arthritis. Br J Pharmacol. 2008 Jun;154(4):843-51. doi: 10.1038/bjp.2008.113. Epub 2008 Apr 21. PMID: 18536737; PMCID: PMC2439856.
72. Zha S, Wang F, Li Z, Ma Z, Yang L, Liu F. PJ34, a PARP1 inhibitor, promotes endothelial repair in a rabbit model of high fat diet-induced atherosclerosis. Cell Cycle. 2019 Sep;18(17):2099-2109. doi: 10.1080/15384101.2019.1640008. Epub 2019 Jul 15. PMID: 31276434; PMCID: PMC6986555.
73. van der Heijden T, Kritikou E, Venema W, et al, NLRP3 Inflammasome Inhibition by MCC950 Reduces Atherosclerotic Lesion Development in Apolipoprotein E-Deficient Mice-Brief Report. Arterioscler Thromb Vasc Biol. 2017 Aug;37(8):1457-1461. doi: 10.1161/ATVBAHA.117.309575. Epub 2017 Jun 8. PMID: 28596375.
74. Bode N, Grebe A, Kerksiek A, et al, Ursodeoxycholic acid impairs atherogenesis and promotes plaque regression by cholesterol crystal dissolution in mice. Biochem Biophys Res Commun. 2016 Sep 9;478(1):356-362. doi: 10.1016/j.bbrc.2016.07.047. Epub 2016 Jul 11. PMID: 27416761.
75. Adorni MP, Zimetti F, Billheimer JT, et al, The roles of different pathways in the release of cholesterol from macrophages. J Lipid Res. 2007 Nov;48(11):2453-62. doi: 10.1194/jlr.M700274-JLR200. Epub 2007 Aug 29. PMID: 17761631.
76. Tertov VV, Kaplun VV, Sobenin IA, Orekhov AN. Low-density lipoprotein modification occurring in human plasma possible mechanism of in vivo lipoprotein desialylation as a primary step of atherogenic modification. Atherosclerosis. 1998 May;138(1):183-95. doi: 10.1016/s0021-9150(98)00023-9. PMID: 9678784.
77. Ouchi Y, Sasaki J, Arai H, et al, Ito H. Ezetimibe Lipid-Lowering Trial on Prevention of Atherosclerotic Cardiovascular Disease in 75 or Older (EWTOPIA 75): A Randomized, Controlled Trial. Circulation. 2019 Sep 17;140(12):992-1003. doi: 10.1161/CIRCULATIONAHA.118.039415. Epub 2019 Aug 22. PMID: 31434507.
78. Ota H, Omori H, Kawasaki M, Hirakawa A, Matsuo H. Clinical impact of PCSK9 inhibitor on stabilization and regression of lipid-rich coronary plaques: a near-infrared spectroscopy study. Eur Heart J Cardiovasc Imaging. 2022 Jan 24;23(2):217-228. doi: 10.1093/ehjci/jeab034. PMID: 33637979.
79. Tommaso Gori & Thomas Münzel (2011) Oxidative stress and endothelial dysfunction: Therapeutic implications, Annals of Medicine, 43:4, 259-272, DOI: 10.3109/07853890.2010.543920
80. Hamaad A, Lip GY, MacFadyen RJ. Unheralded sudden cardiac death: do autonomic tone and thrombosis interact as key factors in aetiology? Ann Med. 2003;35(8):592-604. doi: 10.1080/07853890310016351. PMID: 14708969.
81. Chevalier P, Dacosta A, Defaye P, et al. (1998) Arrythmic cardiac arrest due to isolated coronary artery spasm: Long-term outcome of seven resuscitated patients. J Am Coll Cardiol 31:57–61 PubMedWeb of ScienceGoogle Scholar
82. Connelly KA, MacIsaac AI, Jelinek VM. Stress, myocardial infarction, and the "tako-tsubo" phenomenon. Heart. 2004 Sep;90(9):e52. doi: 10.1136/hrt.2004.038851. PMID: 15310721; PMCID: PMC1768425.
83. Lowenstein CJ, Dinerman JL, Snyder SH (1994) Nitric oxide: a physiologic messenger. Ann Intern Med 120:227–237.CrossRefPubMedWeb of ScienceGoogle Scholar
84. Leor J, Poole WK, Kloner RA. Sudden cardiac death triggered by an earthquake. N Engl J Med. 1996 Feb 15;334(7):413-9. doi: 10.1056/NEJM199602153340701. PMID: 8552142.
85. Kark JD, Goldman S, Epstein L. Iraqi missile attacks on Israel. JAMA1995;273:1208–10. CrossRefPubMedWeb of ScienceGoogle Scholar
86. Witte DR, Bots ML, Hoes AW, et al. Cardiovascular mortality in Dutch men during 1996 European football championship: longitudinal population study. BMJ 2000;321:1552–4. Abstract/FREE Full TextGoogle Scholar
87. Allegra JR, Mostashari F, Rothman J, Milano P, Cochrane DG. Cardiac events in
New Jersey after the September 11, 2001, terrorist attack. J Urban Health 2005;82(3):358–63. http://dx.doi.org/10.1093/jurban/jti087. Epub 2005 Jul 6. PMID:16000653. PMCID:PMC3456051.
88. Feng J, Lenihan DJ, Johnson MM, Karri V, Reddy CV. Cardiac sequelae in Brooklyn after the September 11 terrorist attacks. Clin Cardiol. 2006 Jan;29(1):13-7. doi: 10.1002/clc.4960290105. PMID: 16477772; PMCID: PMC6654218.
89. Rosengren A, Hawken S, Ounpuu S, et al, INTERHEART investigators. Association of psychosocial risk factors with risk of acute myocardial infarction in 11119 cases and 13648 controls from 52 countries (the INTERHEART study): case-control study. Lancet. 2004 Sep 11-17;364(9438):953-62. doi: 10.1016/S0140-6736(04)17019-0. PMID: 15364186.
90. Shen BJ, Avivi YE, Todaro JF, et al, Anxiety characteristics independently and prospectively predict myocardial infarction in men: the unique contribution of anxiety among psychologic factors. J Am Coll Cardiol, 51 (2008), pp. 113-119 ArticleDownload PDFView Record in ScopusGoogle Scholar
91. Mittleman MA, Maclure M, Sherwood JB, et al, Triggering of acute myocardial infarction onset by episodes of anger. Determinants of Myocardial Infarction Onset Study Investigators. Circulation. 1995 Oct 1;92(7):1720-5. doi: 10.1161/01.cir.92.7.1720. PMID: 7671353.
92. Allison TG. Identification and treatment of psychosocial risk factors for coronary artery disease. Mayo Clin Proc. 1996 Aug;71(8):817-9. doi: 10.1016/S0025-6196(11)64849-0. PMID: 8691905.
93. Tsouna-Hadjis ED, Mitsibounas DN, Kallergis GE, Sideris DA. Autonomic nervous system responses to personal stressful events in patients with acute myocardial infarction. Preliminary results. Psychother Psychosom. 1998;67(1):31-6. doi: 10.1159/000012256. PMID: 9491438.
94. Thombs BD, Bass EB, Ford DE, et al, Prevalence of depression in survivors of acute myocardial infarction. J Gen Intern Med 2006; 21:30–38 Crossref, Medline, Google Scholar
95. Kaptein KI, de Jonge P, van den Brink RH, Korf J. Course of depressive symptoms after myocardial infarction and cardiac prognosis: a latent class analysis. Psychosom Med. 2006 Sep-Oct;68(5):662-8. doi: 10.1097/01.psy.0000233237.79085.57. Epub 2006 Sep 20. PMID: 16987947.
96. van Melle JP, de Jonge P, Spijkerman TA, Tijssen JG, Ormel J, van Veldhuisen DJ, van den Brink RH, van den Berg MP. Prognostic association of depression following myocardial infarction with mortality and cardiovascular events: a meta-analysis. Psychosom Med. 2004 Nov-Dec;66(6):814-22. doi: 10.1097/01.psy.0000146294.82810.9c. PMID: 15564344.
97. Kaptein KI, de Jonge P, van den Brink RH, Korf J. Course of depressive symptoms after myocardial infarction and cardiac prognosis: a latent class analysis. Psychosom Med. 2006 Sep-Oct;68(5):662-8. doi: 10.1097/01.psy.0000233237.79085.57. Epub 2006 Sep 20. PMID: 16987947.
98. Dai MX, Zheng XH, Yu J, et al, The impact of intermittent and repetitive cold stress exposure on endoplasmic reticulum stress and instability of atherosclerotic plaques. Cell Physiol Biochem. 2014;34(2):393-404. doi: 10.1159/000363008. Epub 2014 Jul 11. PMID: 25059288.
99. Lu XT, Liu YF, Zhang L, et al, Unpredictable chronic mild stress promotes atherosclerosis in high cholesterol-fed rabbits. Psychosom Med. 2012 Jul-Aug;74(6):604-11. doi: 10.1097/PSY.0b013e31825d0b71. Epub 2012 Jun 28. PMID: 22753638.
100. Lin Y, Feng M, Lu CW, Lei YP, He ZM, Xiong Y. Preservation of vascular DDAH activity contributes to the protection of captopril against endothelial dysfunction in hyperlipidemic rabbits. Eur J Pharmacol. 2017 Mar 5;798:43-48. doi: 10.1016/j.ejphar.2017.01.041. Epub 2017 Feb 3. PMID: 28163022.
101. Drolet MC, Plante E, Battistini B, Couet J, Arsenault M. Early endothelial dysfunction in cholesterol-fed rabbits: a non-invasive in vivo ultrasound study. Cardiovasc Ultrasound. 2004 Jul 21;2:10. doi: 10.1186/1476-7120-2-10. PMID: 15268763; PMCID: PMC514529.
102. El-Awady MS, Suddek GM. Agmatine ameliorates atherosclerosis progression and endothelial dysfunction in high cholesterol-fed rabbits. J Pharm Pharmacol. 2014 Jun;66(6):835-43. doi: 10.1111/jphp.12204. Epub 2014 Jan 7. PMID: 24393128.
103. Shechter M, Matetzky S, Prasad M, et al. Endothelial function predicts 1-year adverse clinical outcome in patients hospitalized in the emergency department chest pain unit. Int. J. Cardiol. 2017;240:14–19. doi: 10.1016/j.ijcard.2017.04.101.
104. AlBadri A, Bairey Merz CN, Johnson BD, et al. Impact of abnormal coronary reactivity on long-term clinical outcomes in women. J. Am. Coll. Cardiol. 2019;73(6):684–693. doi: 10.1016/j.jacc.2018.11.040.
105. Cannon RO, III, Cattau EL, Jr, Yakshe PN, et al. Coronary flow reserve, esophageal motility, and chest pain in patients with angiographically normal coronary arteries. Am. J. Med. 1990;88(3):217–222. doi: 10.1016/0002-9343(90)90145-4.
106. Merz CNB, Kelsey SF, Pepine CJ, et al. The Women’s Ischemia Syndrome Evaluation (WISE) study: protocol design, methodology and feasibility report. J. Am. Coll. Cardiol. 1999;33(6):1453–1461. doi: 10.1016/S0735-1097(99)00082-0.
107. Ahmadi N, Ruiz-Garcia J, Hajsadeghi F, et al, Impaired coronary artery distensibility is an endothelium-dependent process and is associated with vulnerable plaque composition. Clin Physiol Funct Imaging. 2016 Jul;36(4):261-8. doi: 10.1111/cpf.12220. Epub 2014 Dec 18. PMID: 25524149.
108. De Bruyne B, Oldroyd KG, Pijls NHJ. Microvascular (Dys)function and clinical outcome in stable coronary disease. J. Am. Coll. Cardiol. 2016;67(10):1170–1172. doi: 10.1016/j.jacc.2015.11.066.
109. Layland J, Carrick D, Lee M, Oldroyd K, Berry C. Adenosine: physiology, pharmacology, and clinical applications. JACC Cardiovasc. Interv. 2014;7(6):581–591. doi: 10.1016/j.jcin.2014.02.009.
110. Wieneke H, von Birgelen C, Haude M, et al. Determinants of coronary blood flow in humans: Quantification by intracoronary Doppler and ultrasound. J. Appl. Physiol. 2005;98(3):1076–1082. doi: 10.1152/japplphysiol.00724.2004.
111. Doucette JW, Corl PD, Payne HM, et al. Validation of a Doppler guide wire for intravascular measurement of coronary artery flow velocity. Circulation. 1992;85(5):1899–1911. doi: 10.1161/01.CIR.85.5.1899.
112. Stuijfzand WJ, Schumacher SP, Driessen RS, et al. Myocardial Blood Flow and Coronary Flow Reserve During 3 Years Following Bioresorbable Vascular Scaffold Versus Metallic Drug-Eluting Stent Implantation: The VANISH Trial. JACC Cardiovasc Interv. 2019 May 27;12(10):967-979. doi: 10.1016/j.jcin.2019.03.004. Epub 2019 Apr 24. PMID: 31029616.
113. Suwaidi JA, Hamasaki S, Higano ST, Nishimura RA, Holmes DR, Jr, Lerman A. Long-term follow-up of patients with mild coronary artery disease and endothelial dysfunction. Circulation. 2000;101(9):948–954. doi: 10.1161/01.CIR.101.9.948.
114. Herscovici R, Sedlak T, Wei J, Pepine CJ, Handberg E, Bairey Merz CN. Ischemia and no obstructive coronary artery disease (INOCA): What is the risk? J. Am. Heart Assoc. 2018;7(17):e008868. doi: 10.1161/JAHA.118.008868.
115. Lanza GA. Diagnostic Approach to Patients with Stable Angina and No Obstructive Coronary Arteries. Eur Cardiol. 2019 Jul 11;14(2):97-102. doi: 10.15420/ecr.2019.22.2. PMID: 31360230; PMCID: PMC6659043.
116. Lanza GA, Camici PG, Galiuto L, et al. Gruppo di Studio di Fisiopatologia Coronarica e Microcircolazione, Società Italiana di Cardiologia. Methods to investigate coronary microvascular function in clinical practice. J. Cardiovasc. Med. (Hagerstown) 2013;14(1):1–18. doi: 10.2459/JCM.0b013e328351680f.
117. Lanza GA. Diagnostic approach to patients with stable angina and no obstructive coronary arteries. Eur. Cardiol. 2019;14(2):97–102. doi: 10.15420/ecr.2019.22.2.
118. Ford TJ, Corcoran D, Berry C. Stable coronary syndromes: pathophysiology, diagnostic advances and therapeutic need. Heart. 2018 Feb;104(4):284-292. doi: 10.1136/heartjnl-2017-311446. Epub 2017 Oct 13. PMID: 29030424; PMCID: PMC5861393.
119. Hofma SH, van der Giessen WJ, van Dalen BM, et al. Indication of long-term endothelial dysfunction after sirolimus-eluting stent implantation. Eur. Heart J. 2006;27(2):166–170. doi: 10.1093/eurheartj/ehi571.
120. Ghiadoni L, Salvetti M, Muiesan ML, Taddei S. Evaluation of endothelial function by flow mediated dilation: Methodological issues and clinical importance. High Blood Press. Cardiovasc. Prev. 2015;22(1):17–22. doi: 10.1007/s40292-014-0047-2.
121. Zalos G, Finkel T, Hill JM, et al. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. Obstet. Gynecol. Surv. 2004;58(7):467–468. doi: 10.1097/01.ogx.00000716.62998.d7
122. Gómez-Hospital JA Tenas MS, Cequier Fillat A, et al. Endothelial function in coronary segments previously treated with balloon angioplasty. Rev. Esp. Cardiol. 2000;53(11):1467–1473. PubMed
123. Van der Heiden K, Gijsen FJ, Narracott A, et al, The effects of stenting on shear stress: relevance to endothelial injury and repair. Cardiovasc Res. 2013 Jul 15;99(2):269-75. doi: 10.1093/cvr/cvt090. Epub 2013 Apr 15. PMID: 23592806.
124. Shiomi M, Fan J. Unstable coronary plaques and cardiac events in myocardial infarction-prone Watanabe heritable hyperlipidemic rabbits: questions and quandaries. Curr Opin Lipidol. 2008 Dec;19(6):631-6. doi: 10.1097/MOL.0b013e3283189c18. PMID: 18957890.
125. Yamada S, Koike T, Nakagawa T, et al, Morphological features of coronary plaques in WHHLMI rabbits (Oryctolagus cuniculus), an animal model for familial hypercholesterolemia. Exp Anim. 2017 May 3;66(2):145-157. doi: 10.1538/expanim.16-0078. Epub 2016 Dec 27. PMID: 28025424; PMCID: PMC5411301.
126. Bi L, Wacker BK, Bueren E, Ham E, Dronadula N, Dichek DA. A Rabbit Model for Testing Helper-Dependent Adenovirus-Mediated Gene Therapy for Vein Graft Atherosclerosis. Mol Ther Methods Clin Dev. 2017 Sep 28;7:96-111. doi: 10.1016/j.omtm.2017.09.004. PMID: 29296626; PMCID: PMC5744068.
127. Schachner T, Laufer G, Bonatti J. In vivo (animal) models of vein graft disease. Eur J Cardiothorac Surg. 2006 Sep;30(3):451-63. doi: 10.1016/j.ejcts.2006.06.015. Epub 2006 Jul 25. PMID: 16870461.
128. Rai S, Zulli A. Lack of cell stress markers in fibrous cap cells in the left main coronary artery. Histol Histopathol. 2013 Apr;28(4):505-11. doi: 10.14670/HH-28.505. Epub 2013 Feb 11. PMID: 23397141.
129. Torres G, Czernuszewicz TJ, Homeister JW, Farber MA, Caughey MC, Gallippi CM. Carotid Plaque Fibrous Cap Thickness Measurement by ARFI Variance of Acceleration: In Vivo Human Results. IEEE Trans Med Imaging. 2020 Dec;39(12):4383-4390. doi: 10.1109/TMI.2020.3019184. Epub 2020 Nov 30. PMID: 32833633; PMCID: PMC7725192.
130. Sakakura K, Nakano M, Otsuka F, Ladich E, Kolodgie FD, Virmani R. Pathophysiology of atherosclerosis plaque progression. Heart Lung Circ. 2013 Jun;22(6):399-411. doi: 10.1016/j.hlc.2013.03.001. Epub 2013 Mar 29. Erratum in: Heart Lung Circ. 2014 Apr;23(4):387. PMID: 23541627.
131. Cardoso L, Weinbaum S. Microcalcifications, Their Genesis, Growth, and Biomechanical Stability in Fibrous Cap Rupture. Adv Exp Med Biol. 2018;1097:129-155. doi: 10.1007/978-3-319-96445-4_7. PMID: 30315543.
132. Saba L, Potters F, van der Lugt A, Mallarini G. Imaging of the fibrous cap in atherosclerotic carotid plaque. Cardiovasc Intervent Radiol. 2010 Aug;33(4):681-9. doi: 10.1007/s00270-010-9828-8. Epub 2010 Mar 17. PMID: 20237780.
133. Ruehm SG. Magnetresonanztomographische Bildgebung der atherosklerotischen Plaque [Magnetic resonance imaging of atherosclerotic plaque]. Herz. 2003 Sep;28(6):513-20. German. doi: 10.1007/s00059-003-2489-5. PMID: 14564414.
134. Galdin NS (2006) Osnovy gidravliki i gidroprivoda. Uchebnoe posobie translation - “Fundamentals of hydraulics and hydraulic drive. Textbook”). Omsk: Sibirskaja gosudarstvennaja avtomobil’no-dorozhnaja akademija (SibADI); 145.
135. Shterenliht DV (1984) Gidravlika (translation - “Hydraulics”). Moskva: Jenergoatomizdat 640.
136. Chugaev RR (1982) Gidravlika (Tehnicheskaja mehanika zhidkosti) (translation “Hydraulics (Technical fl uid mechanics)”). Moskva: Jenergoizdat 67
137. Getz GS, Reardon CA. Animal models of atherosclerosis. Arterioscler Thromb Vasc Biol. 2012 May;32(5):1104-15. doi: 10.1161/ATVBAHA.111.237693. Epub 2012 Mar 1. PMID: 22383700; PMCID: PMC3331926.