Analysis of arterial intimal hyperplasia: review and hypothesis

Vladimir M Subbotin, Vladimir M Subbotin

Abstract

Background: Despite a prodigious investment of funds, we cannot treat or prevent arteriosclerosis and restenosis, particularly its major pathology, arterial intimal hyperplasia. A cornerstone question lies behind all approaches to the disease: what causes the pathology?

Hypothesis: I argue that the question itself is misplaced because it implies that intimal hyperplasia is a novel pathological phenomenon caused by new mechanisms. A simple inquiry into arterial morphology shows the opposite is true. The normal multi-layer cellular organization of the tunica intima is identical to that of diseased hyperplasia; it is the standard arterial system design in all placentals at least as large as rabbits, including humans. Formed initially as one-layer endothelium lining, this phenotype can either be maintained or differentiate into a normal multi-layer cellular lining, so striking in its resemblance to diseased hyperplasia that we have to name it "benign intimal hyperplasia". However, normal or "benign" intimal hyperplasia, although microscopically identical to pathology, is a controllable phenotype that rarely compromises blood supply. It is remarkable that each human heart has coronary arteries in which a single-layer endothelium differentiates early in life to form a multi-layer intimal hyperplasia and then continues to self-renew in a controlled manner throughout life, relatively rarely compromising the blood supply to the heart, causing complications requiring intervention only in a small fraction of the population, while all humans are carriers of benign hyperplasia. Unfortunately, this fundamental fact has not been widely appreciated in arteriosclerosis research and medical education, which continue to operate on the assumption that the normal arterial intima is always an "ideal" single-layer endothelium. As a result, the disease is perceived and studied as a new pathological event caused by new mechanisms. The discovery that normal coronary arteries are morphologically indistinguishable from deadly coronary arteriosclerosis continues to elicit surprise.

Conclusion: Two questions should inform the priorities of our research: (1) what controls switch the single cell-layer intimal phenotype into normal hyperplasia? (2) how is normal (benign) hyperplasia maintained? We would be hard-pressed to gain practical insights without scrutinizing our premises.

References

    1. Booth FW, Gordon SE, Carlson CJ, Hamilton MT. Waging war on modern chronic diseases: primary prevention through exercise biology. J Appl Physiol. 2000;88:774–787.
    1. Boden WE, O'Rourke RA, Teo KK, Hartigan PM, Maron DJ, Kostuk WJ, Knudtson M, Dada M, Casperson P, Harris CL. et al.Optimal medical therapy with or without PCI for stable coronary disease. N Engl J Med. 2007;356:1503–1516. doi: 10.1056/NEJMoa070829.
    1. Booth FW, Chakravarthy MV, Gordon SE, Spangenburg EE. Waging war on physical inactivity: using modern molecular ammunition against an ancient enemy. J Appl Physiol. 2002;93:3–30.
    1. Booth FW, Neufer PD. Exercise Controls Gene Expression. American Scientist. 2005;93
    1. Iestra JA, Kromhout D, van der Schouw YT, Grobbee DE, Boshuizen HC, van Staveren WA. Effect size estimates of lifestyle and dietary changes on all-cause mortality in coronary artery disease patients: a systematic review. Circulation. 2005;112:924–934. doi: 10.1161/CIRCULATIONAHA.104.503995.
    1. Stary HC, Blankenhorn DH, Chandler AB, Glagov S, Insull W Jr, Richardson M, Rosenfeld ME, Schaffer SA, Schwartz CJ, Wagner WD. et al.A definition of the intima of human arteries and of its atherosclerosis-prone regions. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Arterioscler Thromb. 1992;12:120–134.
    1. Stary HC, Chandler AB, Dinsmore RE, Fuster V, Glagov S, Insull W Jr, Rosenfeld ME, Schwartz CJ, Wagner WD, Wissler RW. 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. Circulation. 1995;92:1355–1374.
    1. Cano A, Hermenegildo C, Oviedo P, Tarin JJ. The risk for cardiovascular disease in women: from estrogens to selective estrogen receptor modulators. Front Biosci. 2007;12:49–68. doi: 10.2741/2048.
    1. Shapiro WD. Coronary disease in the young. Dissertation. University of Wisconsin, Medicine. 1951.
    1. Stary HC, Blankenhorn DH, Chandler AB, Glagov S, Insull WJ, Richardson M, Rosenfeld ME, Schaffer SA, Schwartz CJ, Wagner WD. A definition of the intima of human arteries and of its atherosclerosis- prone regions. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Circulation. 1992;85:391–405.
    1. Stary HC, Chandler AB, Dinsmore RE, Fuster V, Glagov S, Insull W Jr, Rosenfeld ME, Schwartz CJ, Wagner WD, Wissler RW. 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.
    1. Desmouliere A, Darby IA, Gabbiani G. Normal and pathologic soft tissue remodeling: role of the myofibroblast, with special emphasis on liver and kidney fibrosis. Lab Invest. 2003;83:1689–1707. doi: 10.1097/01.LAB.0000101911.53973.90.
    1. Schurch W, Seemayer TA, Gabbiani G. The myofibroblast: a quarter century after its discovery. Am J Surg Pathol. 1998;22:141–147. doi: 10.1097/00000478-199802000-00001.
    1. Gilbert SF. Developmental Biology. 4. Sunderland: Sinauer Associates, Inc; 1994.
    1. Chandrasoma P, Taylor CR. Concise pathology. 2. Norwalk: Appleton & Lange; 1995.
    1. Daoud A, Jarmolych J, Zumbo A, Fani, Florentin R. Preatheroma Phase of Coronary Atherosclerosis in Man. Exp Mol Pathol. 1964;90:475–484. doi: 10.1016/0014-4800(64)90028-0.
    1. Bots ML, Baldassarre D, Simon A, de Groot E, O'Leary DH, Riley W, Kastelein JJ, Grobbee DE. Carotid intima-media thickness and coronary atherosclerosis: weak or strong relations? Eur Heart J. 2007;28:398–406. doi: 10.1093/eurheartj/ehl482.
    1. Hung MJ, Cherng WJ, Yang NI, Cheng CW, Li LF. Relation of high-sensitivity C-reactive protein level with coronary vasospastic angina pectoris in patients without hemodynamically significant coronary artery disease. Am J Cardiol. 2005;96:1484–1490. doi: 10.1016/j.amjcard.2005.07.055.
    1. Cin VG, Pekdemir H, Camsar A, Cicek D, Akkus MN, Parmaksyz T, Katyrcybay T, Doven O. Diffuse intimal thickening of coronary arteries in slow coronary flow. Jpn Heart J. 2003;44:907–919. doi: 10.1536/jhj.44.907.
    1. Miyao Y, Kugiyama K, Kawano H, Motoyama T, Ogawa H, Yoshimura M, Sakamoto T, Yasue H. Diffuse intimal thickening of coronary arteries in patients with coronary spastic angina. J Am Coll Cardiol. 2000;36:432–437. doi: 10.1016/S0735-1097(00)00729-4.
    1. Luo H, Nishioka T, Eigler NL, Forrester JS, Fishbein MC, Berglund H, Siegel RJ. Coronary artery restenosis after balloon angioplasty in humans is associated with circumferential coronary constriction. Arterioscler Thromb Vasc Biol. 1996;16:1393–1398.
    1. Yutani C, Imakita M, Ishibashi-Ueda H, Tsukamoto Y, Nishida N, Ikeda Y. Coronary atherosclerosis and interventions: pathological sequences and restenosis. Pathol Int. 1999;49:273–290. doi: 10.1046/j.1440-1827.1999.00861.x.
    1. Kipshidze N, Dangas G, Tsapenko M, Moses J, Leon MB, Kutryk M, Serruys P. Role of the endothelium in modulating neointimal formation: vasculoprotective approaches to attenuate restenosis after percutaneous coronary interventions. J Am Coll Cardiol. 2004;44:733–739.
    1. Krotz F, Sohn HY, Klauss V, Schiele TM. Intracoronary brachytherapy – clinical state and pathophysiological considerations. Curr Pharm Des. 2005;11:421–433. doi: 10.2174/1381612053382025.
    1. Sheppard R, Eisenberg MJ, Donath D, Meerkin D. Intracoronary brachytherapy for the prevention of restenosis after percutaneous coronary revascularization. Am Heart J. 2003;146:775–786. doi: 10.1016/S0002-8703(03)00389-2.
    1. Teirstein P, Reilly JP. Late stent thrombosis in brachytherapy: the role of long-term antiplatelet therapy. J Invasive Cardiol. 2002;14:109–114.
    1. Schiele TM, Krotz F, Klauss V. Vascular restenosis – striving for therapy. Expert Opin Pharmacother. 2004;5:2221–2232. doi: 10.1517/14656566.5.11.2221.
    1. Kaluza GL, Raizner AE. Brachytherapy for restenosis after stenting for coronary artery disease: its role in the drug-eluting stent era. Curr Opin Cardiol. 2004;19:601–607. doi: 10.1097/01.hco.0000142069.39957.03.
    1. Costa MA, Simon DI. Molecular basis of restenosis and drug-eluting stents. Circulation. 2005;111:2257–2273. doi: 10.1161/01.CIR.0000163587.36485.A7.
    1. Teirstein PS, King S. Vascular radiation in a drug-eluting stent world: it's not over till it's over. Circulation. 2003;108:384–385. doi: 10.1161/01.CIR.0000080229.68147.4F.
    1. Valgimigli M, Malagutti P, van Mieghem CA, Vaina S, Ligthart JM, Sianos G, Serruys PW. Persistence of neointimal growth 12 months after intervention and occurrence of delayed restenosis in patients with left main coronary artery disease treated with drug-eluting stents. J Am Coll Cardiol. 2006;47:1491–1494. doi: 10.1016/j.jacc.2006.01.008.
    1. Callow AD. In: Intimal Hyperplasia. Dobrin PB, editor. Austin: R.G. Landes Co; 1994. Intimal Hyperplasia: The Clinical problem; pp. 3–12. [Medical intelligence unit]
    1. Fortunato JE, Glagov S, Bassiouny HS. Irradiation for the treatment of intimal hyperplasia. Ann Vasc Surg. 1998;12:495–503. doi: 10.1007/s100169900191.
    1. Serruys PW, Regar E, Carter AJ. Rapamycin eluting stent: the onset of a new era in interventional cardiology. Heart. 2002;87:305–307. doi: 10.1136/heart.87.4.305.
    1. Hafeez N. Prevention of coronary restenosis with radiation therapy: a review. Clin Cardiol. 2002;25:313–322. doi: 10.1002/clc.4950250703.
    1. de Winter RJ, Windhausen F, Cornel JH, Dunselman PH, Janus CL, Bendermacher PE, Michels HR, Sanders GT, Tijssen JG, Verheugt FW. Early invasive versus selectively invasive management for acute coronary syndromes. N Engl J Med. 2005;353:1095–1104. doi: 10.1056/NEJMoa044259.
    1. Hochman JS, Lamas GA, Buller CE, Dzavik V, Reynolds HR, Abramsky SJ, Forman S, Ruzyllo W, Maggioni AP, White H. et al.Coronary intervention for persistent occlusion after myocardial infarction. N Engl J Med. 2006;355:2395–2407. doi: 10.1056/NEJMoa066139.
    1. Katritsis DG, Ioannidis JP. Percutaneous coronary intervention versus conservative therapy in nonacute coronary artery disease: a meta-analysis. Circulation. 2005;111:2906–2912. doi: 10.1161/CIRCULATIONAHA.104.521864.
    1. Susser M, Susser E. Choosing a future for epidemiology: I. Eras and paradigms. Am J Public Health. 1996;86:668–673.
    1. Dean K. The role of methods in maintaining orthodox beliefs in health research. Soc Sci Med. 2004;58:675–685. doi: 10.1016/S0277-9536(03)00219-3.
    1. Gillett G. Beyond the orthodox: heresy in medicine and social science. Soc Sci Med. 1994;39:1125–1131. doi: 10.1016/0277-9536(94)90345-X.
    1. Mojon-Azzi SM, Jiang X, Wagner U, Mojon DS. Redundant publications in scientific ophthalmologic journals: the tip of the iceberg? Ophthalmology. 2004;111:863–866. doi: 10.1016/j.ophtha.2003.09.029.
    1. Armstrong RA, Cairns NJ, Lantos PL. Are pathological lesions in neurodegenerative disorders the cause or the effect of the degeneration? Neuropathology. 2002;22:133–146. doi: 10.1046/j.1440-1789.2002.00446.x.
    1. De Servi S, Mariani M, Mariani G, Mazzone A. C-reactive protein increase in unstable coronary disease cause or effect? J Am Coll Cardiol. 2005;46:1496–1502. doi: 10.1016/j.jacc.2005.05.083.
    1. Horsella M, Sindermann G. Aspects of scientific discourse: Conditional argumentation. English for Specific Purposes. 1992;11:129–139. doi: 10.1016/S0889-4906(05)80004-3.
    1. Biro JC. Seven fundamental, unsolved questions in molecular biology. Cooperative storage and bi-directional transfer of biological information by nucleic acids and proteins: an alternative to "central dogma". Med Hypotheses. 2004;63:951–962. doi: 10.1016/j.mehy.2004.06.024.
    1. Deng MC, Plenz G, Erren M, Wilhelm MJ, Moennig G, Rothenburger M, Baba HA. Transplant vasculopathy: a model for coronary artery disease? Herz. 2000;25:95–99. doi: 10.1007/PL00001959.
    1. Takahashi T, Lee RT. Dendritic cells in neointima formation: from where did you come, and what are you doing here? J Am Coll Cardiol. 2003;42:939–941. doi: 10.1016/S0735-1097(03)00840-4.
    1. Osada M, Takeda S, Ogawa R, Komori S, Tamura K. T lymphocyte activation and restenosis after percutaneous transluminal coronary angioplasty. J Interferon Cytokine Res. 2001;21:219–221. doi: 10.1089/107999001750169835.
    1. Bauriedel G, Jabs A, Skowasch D, Hutter R, Badimon JJ, Fuster V, Welsch U, Luderitz B. Dendritic cells in neointima formation after rat carotid balloon injury: coordinated expression withanti-apoptotic Bcl-2 and HSP47 in arterial repair. J Am Coll Cardiol. 2003;42:930–938. doi: 10.1016/S0735-1097(03)00828-3.
    1. Charlton BG. Boom or bubble? Is medical research thriving or about to crash? Med Hypotheses. 2006;66:1–2. doi: 10.1016/j.mehy.2005.10.004.
    1. Charlton BG, Andras P. Medical research funding may have over-expanded and be due for collapse. Qjm. 2005;98:53–55. doi: 10.1093/qjmed/hci003.
    1. Thoma R. Ueber die Abhängigkeit der Bindegewebsneubildung in der Arterienintima von den mechanischen Bedingungen des Blutumlaufes. Erste Mittheilung. Die Rückwirkung des Verschlusses der Nabelarterien und des arteriösen Ganges auf die Structur der Aortenwand. Archiv fur pathologische Anatomie und Physiologie und fur klinische Medicin (Virchows Archiv) 1883;93:443–505. doi: 10.1007/BF02324120.
    1. Thoma R. Über die Intima der Arterien. Virchows Archiv. 1921;230:1–45. doi: 10.1007/BF01948742.
    1. Wolkoff K. Über die histologische Struktur der Coronararterien des menschlichen Herzens. Virchows Archiv. 1923;241:42–58. doi: 10.1007/BF01942462.
    1. Fox H. In: Arteriosclerosis; a survey of the problem. Cowdry EV, editor. New York: The Macmillan Company; 1933. Arteriosclerosis in Low Mammals and Birds; Its Relation to the Disease in Man; pp. 153–194.
    1. Ward BC, Shively JN. Atherosclerosis in rat kangaroos. Arch Pathol. 1974;98:90–93.
    1. Velican C, Velican D. Coronary arteries in infants up to the age of ten years. I. Chronology of adaptive intimal changes. Rev Roum Med Intern. 1975;13:19–24.
    1. Velican C, Velican D. Coronary arteries in children up to the age of ten years II. Intimal thickening and its role in atherosclerotic involvement. Med Interne. 1976;14:17–24.
    1. Velican C, Velican D. Particular aspects of the children coronary artery remodelling. Med Interne. 1978;16:127–134.
    1. Velican C, Velican D. Some particular aspects of the microarchitecture of human coronary arteries. Atherosclerosis. 1979;33:191–200. doi: 10.1016/0021-9150(79)90116-3.
    1. Bohorquez F, Stout C. Arteriosclerosis in exotic mammals. Atherosclerosis. 1972;16:225–231. doi: 10.1016/0021-9150(72)90056-1.
    1. Bálint A. In: Arterial lesion and arteriosclerosis. Jellinek H, editor. London-New York: Plenium Press; 1974. The fine structure of the mammalian arterial wall.
    1. French JE. Atherosclerosis in relation to the structure and function of the arterial intima, with special reference to the endothelium. Int Rev Exp Pathol. 1966;5:253–353.
    1. Hirvonen J, Yla-Herttuala S, Laaksonen H, Mottonen M, Nikkari T, Pesonen E, Raekallio J, Akerblom HK. Coronary intimal thickenings and lipids in Finnish children who died violently. Acta Paediatr Scand Suppl. 1985;318:221–224.
    1. Davies H. Atherogenesis and the coronary arteries of childhood. Int J Cardiol. 1990;28:283–291. doi: 10.1016/0167-5273(90)90310-2.
    1. Sims FH, Gavin JB, Vanderwee MA. The intima of human coronary arteries. Am Heart J. 1989;118:32–38. doi: 10.1016/0002-8703(89)90068-9.
    1. Greenwald SE, Berry CL. Improving vascular grafts: the importance of mechanical and haemodynamic properties. J Pathol. 2000;190:292–299. doi: 10.1002/(SICI)1096-9896(200002)190:3<292::AID-PATH528>;2-S.
    1. O'Brien ER, Bennett KL, Garvin MR, Zderic TW, Hinohara T, Simpson JB, Kimura T, Nobuyoshi M, Mizgala H, Purchio A, Schwartz SM. Beta ig-h3, a transforming growth factor-beta-inducible gene, is overexpressed in atherosclerotic and restenotic human vascular lesions. Arterioscler Thromb Vasc Biol. 1996;16:576–584.
    1. Garvin MR, Labinaz M, Pels K, Walley VM, Mizgala HF, O'Brien ER. Arterial expression of the plasminogen activator system early after cardiac transplantation. Cardiovasc Res. 1997;35:241–249. doi: 10.1016/S0008-6363(97)00088-6.
    1. Miller H, Poon S, Hibbert B, Rayner K, Chen YX, O'Brien ER. Modulation of estrogen signaling by the novel interaction of heat shock protein 27, a biomarker for atherosclerosis, and estrogen receptor beta: mechanistic insight into the vascular effects of estrogens. Arterioscler Thromb Vasc Biol. 2005;25:e10–14. doi: 10.1161/01.ATV.0000156536.89752.8e.
    1. Ikari Y, McManus BM, Kenyon J, Schwartz SM. Neonatal intima formation in the human coronary artery. Arterioscler Thromb Vasc Biol. 1999;19:2036–2040.
    1. Zhdanov VS, Sternby NH, Drobkova IP, Galakhov IE. Hyperplasia of coronary intima in young males in relation to development of coronary heart disease in adults. Int J Cardiol. 2000;76:57–64. doi: 10.1016/S0167-5273(00)00369-7.
    1. Matturri L, Lavezzi AM, Ottaviani G, Rossi L. Intimal preatherosclerotic thickening of the coronary arteries in human fetuses of smoker mothers. J Thromb Haemost. 2003;1:2234–2238. doi: 10.1046/j.1538-7836.2003.00409.x.
    1. Kusnetzowsky NJ. Arteriosklerose der Coronararterien des Herzens. Virchows Archiv. 1923;245:55–77. doi: 10.1007/BF01992098.
    1. Fukuchi M, Watanabe J, Kumagai K, Baba S, Shinozaki T, Miura M, Kagaya Y, Shirato K. Normal and oxidized low density lipoproteins accumulate deep in physiologically thickened intima of human coronary arteries. Lab Invest. 2002;82:1437–1447.
    1. Nakashima Y, Chen YX, Kinukawa N, Sueishi K. Distributions of diffuse intimal thickening in human arteries: preferential expression in atherosclerosis-prone arteries from an early age. Virchows Arch. 2002;441:279–288. doi: 10.1007/s00428-002-0605-1.
    1. Vink A, Schoneveld AH, Poppen M, de Kleijn DP, Borst C, Pasterkamp G. Morphometric and immunohistochemical characterization of the intimal layer throughout the arterial system of elderly humans. J Anat. 2002;200:97–103. doi: 10.1046/j.0021-8782.2001.00005.x.
    1. Rosamond W, Flegal K, Friday G, Furie K, Go A, Greenlund K, Haase N, Ho M, Howard V, Kissela B. et al.Heart disease and stroke statistics – 2007 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation. 2007;115:e69–171. doi: 10.1161/CIRCULATIONAHA.106.179918.
    1. Maier W, Abay M, Cook S, Togni M, Zeiher A, Meier B. The 2002 European registry of cardiac catheter interventions. Int J Cardiol. 2006;113:299–304. doi: 10.1016/j.ijcard.2005.11.026.
    1. Cooper R, Cutler J, Desvigne-Nickens P, Fortmann SP, Friedman L, Havlik R, Hogelin G, Marler J, McGovern P, Morosco G. et al.Trends and disparities in coronary heart disease, stroke, and other cardiovascular diseases in the United States: findings of the national conference on cardiovascular disease prevention. Circulation. 2000;102:3137–3147.
    1. Thomson KS. Morphogenesis and evolution. New York: Oxford University Press; 1988.
    1. Osborn GR. The incubation period of coronary thrombosis. London: Butterworths; 1963.
    1. Junqueira LC, Carneiro J. Basic Histology : Text & Atlas. 11th International Edition edn. The McGraw-Hill Companies; 2005.
    1. Ham AW. Histology. 9. Philadelphia: Lippincott; 1987.
    1. Dellmann HD. Textbook of Veterinary Histology. Lippincott Williams & Wilkins; 1998.
    1. Huttner I, Kocher O, Gabbani G. In: Diseases of the arterial wall. Camilleri J-P, Berry CL, Fiessinger J-N, Bariety J, editor. London: Springer-Verlag; 1989. Endothelial and Smooth-Muscle Cells; pp. 3–41.
    1. Friedman M. Pathogenesis of coronary artery disease. New York: Blakiston Division, McGraw-Hill; 1969.
    1. DiCorleto PE, Gimbrone MAJ. In: Atherosclerosis and coronary artery disease. 1. Fuster V, Ross R, Topol EJ, editor. Philadelphia: Lippincott-Raven; 1996. Vascular Endothelium; pp. 387–399.
    1. Goldberg ID. In: The Coronary Artery. Kalsner S, editor. New York: Oxford University Press; 1982. The endothelium: injury and repair of the arterial wall; pp. 417–432.
    1. Kuehnel W. Color Atlas of Cytology, Histology, and Microscopic Anatomy. 4. New York: Thieme Verlag; 2003.
    1. Bacon RL, Niles NR. Medical histology : a text-atlas with introductory pathology. New York: Springer-Verlag; 1983.
    1. Ross MH, Kaye GI, Pawlina W. Histology : a text and atlas. 4. Philadelphia: Lippincott Williams & Wilkins; 2003.
    1. Gartner LP, Hiatt JL. Color textbook of histology. 3. Philadelphia: Saunders/Elsevier; 2007. 11. Circulatory System; pp. 251–271.
    1. Histology for Pathologists. 2. Philadelphia Lippincott-Raven; 1997.
    1. Gallagher PJ. In: Histology for Pathologists. 2. Sternberg SS, editor. Philadelphia: Lippincott-Raven; 1997. Blood Vessels. Chapter 33; pp. 763–786.
    1. Stehbens WE. In: Vascular pathology. Stehbens WE, Lie JT, editor. London: Chapman & Hall Medical; 1995. General features, structures, topography and adaptation of the circulatory systems; pp. 1–20.
    1. O'Brien ER, deBlois D, Schwartz SM. In: Intimal Hyperplasia. Dobrin PB, editor. Austin: R.G. Landes Co; 1994. A critical examination of animal models of restenosis following angioplasty; pp. 229–256. [Medical intelligence unit]
    1. Schwartz SM, deBlois D, O'Brien ER. The intima. Soil for atherosclerosis and restenosis. Circ Res. 1995;77:445–465.
    1. Dobrin PB. Intimal hyperplasia. Austin: R.G. Landes Co; 1994.
    1. Demetris AJ, Murase N, Starzl TE, Fung JJ. Pathology of chronic rejection: an overview of common findings and observations about pathogenic mechanisms and possible prevention. Graft. 1998;I:52–59.
    1. Geraghty JG, Stoltenberg RL, Sollinger HW, Hullett DA. Vascular smooth muscle cells and neointimal hyperplasia in chronic transplant rejection. Transplantation. 1996;62:502–509. doi: 10.1097/00007890-199608270-00013.
    1. Miyagawa-Hayashino A, Tsuruyama T, Haga H, Oike F, Il-Deok K, Egawa H, Hiai H, Tanaka K, Manabe T. Arteriopathy in chronic allograft rejection in liver transplantation. Liver Transpl. 2004;10:513–519. doi: 10.1002/lt.20081.
    1. Oguma S, Belle S, Starzl TE, Demetris AJ. A histometric analysis of chronically rejected human liver allografts: insights into the mechanisms of bile duct loss: direct immunologic and ischemic factors. Hepatology. 1989;9:204–209. doi: 10.1002/hep.1840090207.
    1. Cagle PT, Brown RW, Frost A, Kellar C, Yousem SA. Diagnosis of chronic lung transplant rejection by transbronchial biopsy. Mod Pathol. 1995;8:137–142.
    1. Oguma S, Banner B, Zerbe T, Starzl T, Demetris AJ. Participation of dendritic cells in vascular lesions of chronic rejection of human allografts. Lancet. 1988;2:933–936. doi: 10.1016/S0140-6736(88)92600-1.
    1. Deng MC, Bell S, Huie P, Pinto F, Hunt SA, Stinson EB, Sibley R, Hall BM, Valantine HA. Cardiac allograft vascular disease. Relationship to microvascular cell surface markers and inflammatory cell phenotypes on endomyocardial biopsy. Circulation. 1995;91:1647–1654.
    1. Ciubotariu R, Liu Z, Colovai AI, Ho E, Itescu S, Ravalli S, Hardy MA, Cortesini R, Rose EA, Suciu-Foca N. Persistent allopeptide reactivity and epitope spreading in chronic rejection of organ allografts. J Clin Invest. 1998;101:398–405.
    1. Hornick PI, Mason PD, Baker RJ, Hernandez-Fuentes M, Frasca L, Lombardi G, Taylor K, Weng L, Rose ML, Yacoub MH. et al.Significant frequencies of T cells with indirect anti-donor specificity in heart graft recipients with chronic rejection. Circulation. 2000;101:2405–2410.
    1. Tejani A, Emmett L. Acute and chronic rejection. Semin Nephrol. 2001;21:498–507. doi: 10.1053/snep.2001.24945.
    1. Allan JS, Madsen JC. Recent advances in the immunology of chronic rejection. Curr Opin Nephrol Hypertens. 2002;11:315–321. doi: 10.1097/00041552-200205000-00008.
    1. Shirwan H, Mhoyan A, Kakoulidis TP, Yolcu ES, Ibrahim S. Prevention of chronic rejection with immunoregulatory cells induced by intrathymic immune modulation with class I allopeptides. Am J Transplant. 2003;3:581–589. doi: 10.1034/j.1600-6143.2003.00052.x.
    1. Rose ML. Activation of autoimmune B cells and chronic rejection. Transplantation. 2005;79:S22–24. doi: 10.1097/01.TP.0000153294.38939.5F.
    1. Libby P, Tanaka H. The pathogenesis of coronary arteriosclerosis ("chronic rejection") in transplanted hearts. Clin Transplant. 1994;8:313–318.
    1. Hansson GK. In: Transplant Vascular Scerosis. Orosz CG, Sedmak DD, Ferguson RM, editor. Ohio: R. G. Landes Company; 1995. Immune-vascular interaction in atherosclerosis and transplant arteriosclerosis; pp. 71–81.
    1. Lange V, Renner A, Sagstetter M, Harms H, Elert O. Cardiac allograft vasculopathy after cardiac transplantation and hormone therapy: positive effects? Transplantation. 2006;82:234–240. doi: 10.1097/01.tp.0000226179.16065.5e.
    1. Gill JS, Abichandani R, Kausz AT, Pereira BJ. Mortality after kidney transplant failure: the impact of non-immunologic factors. Kidney Int. 2002;62:1875–1883. doi: 10.1046/j.1523-1755.2002.00640.x.
    1. Tilney NL. Chronic rejection and its risk factors. Transplant Proc. 1999;31:41S–44S. doi: 10.1016/S0041-1345(98)02080-6.
    1. van Dam JG, Li F, Yin M, You XM, Grauls G, Steinhoff G, Bruggeman CA. Effects of cytomegalovirus infection and prolonged cold ischemia on chronic rejection of rat renal allografts. Transpl Int. 2000;13:54–63. doi: 10.1007/s001470050009.
    1. Mennander A, Tiisala S, Halttunen J, Yilmaz S, Paavonen T, Hayry P. Chronic rejection in rat aortic allografts. An experimental model for transplant arteriosclerosis. Arterioscler Thromb. 1991;11:671–680.
    1. Koulack J, McAlister VC, Giacomantonio CA, Bitter-Suermann H, MacDonald AS, Lee TD. Development of a mouse aortic transplant model of chronic rejection. Microsurgery. 1995;16:110–113. doi: 10.1002/micr.1920160213.
    1. Sun H, Valdivia LA, Subbotin V, Aitouche A, Fung JJ, Starzl TE, Rao AS. Improved surgical technique for the establishment of a murine model of aortic transplantation. Microsurgery. 1998;18:368–371. doi: 10.1002/(SICI)1098-2752(1998)18:6<368::AID-MICR5>;2-F.
    1. Mitchell RN, Libby P. Vascular remodeling in transplant vasculopathy. Circ Res. 2007;100:967–978. doi: 10.1161/01.RES.0000261982.76892.09.
    1. Wehner J, Morrell CN, Reynolds T, Rodriguez ER, Baldwin WM 3rd. Antibody and complement in transplant vasculopathy. Circ Res. 2007;100:191–203. doi: 10.1161/01.RES.0000255032.33661.88.
    1. Berman SS, Kirsch WM, Zhu YH, Anton L, Chai Y. Impact of nonpenetrating clips on intimal hyperplasia of vascular anastomoses. Cardiovasc Surg. 2001;9:540–547. doi: 10.1016/S0967-2109(01)00090-4.
    1. Sottiurai VS. Distal Anastomotic Intimal Hyperplasia: Histocytomorphology, Pathophysiology, Etiology, and Prevention. Int J Angiol. 1999;8:1–10. doi: 10.1007/BF01616834.
    1. Sottiurai VS. Can intimal hyperplasia and distal anastomotic intimal hyperplasia be controlled and prevented? Ann Vasc Surg. 2007;21:289–291.
    1. Sottiurai VS, Sue SL, Feinberg EL 2nd, Bringaze WL, Tran AT, Batson RC. Distal anastomotic intimal hyperplasia: biogenesis and etiology. Eur J Vasc Surg. 1988;2:245–256. doi: 10.1016/S0950-821X(88)80034-3.
    1. Hosono M, Ueda M, Suehiro S, Sasaki Y, Shibata T, Hattori K, Kinoshita H. Neointimal formation at the sites of anastomosis of the internal thoracic artery grafts after coronary artery bypass grafting in human subjects: an immunohistochemical analysis. J Thorac Cardiovasc Surg. 2000;120:319–328. doi: 10.1067/mtc.2000.106328.
    1. Purcell C, Tennant M, McGeachie J. Neo-intimal hyperplasia in vascular grafts and its implications for autologous arterial grafting. Ann R Coll Surg Engl. 1997;79:164–168.
    1. Purcell C, Tennant M, McGeachie J. Vascular tissue adaptations in end-to-end autologous arterial grafts in rats: a morphometric analysis. J Anat. 1998;192(Pt 1):37–43. doi: 10.1046/j.1469-7580.1998.19210037.x.
    1. Russell B. The History of Western Philosophy. New York: Simon and Schuster. Inc; 1972.
    1. Starzl TE. History of clinical transplantation. World J Surg. 2000;24:759–782. doi: 10.1007/s002680010124.
    1. Sayegh MH, Carpenter CB. Transplantation 50 years later – progress, challenges, and promises. N Engl J Med. 2004;351:2761–2766. doi: 10.1056/NEJMon043418.
    1. Hoerbelt R, Muniappan A, Madsen JC, Allan JS. New strategies for the treatment of chronic rejection. Curr Opin Investig Drugs. 2004;5:489–498.
    1. Goodman J, Mohanakumar T. Chronic rejection: failure of immune regulation. Front Biosci. 2003;8:s838–844. doi: 10.2741/1163.
    1. Houser S, Muniappan A, Allan J, Sachs D, Madsen J. Cardiac Allograft Vasculopathy: Real or a Normal Morphologic Variant? The Journal of Heart and Lung Transplantation. 2007;26:167–173. doi: 10.1016/j.healun.2006.11.012.
    1. Khan R, Agrotis A, Bobik A. Understanding the role of transforming growth factor-beta1 in intimal thickening after vascular injury. Cardiovasc Res. 2007;74:223–234. doi: 10.1016/j.cardiores.2007.02.012.
    1. Thoma R. Ueber die Abhangigkeit der Bindegewebsneubildung in der Arterienintima von den mechanischen Bedingungen des Blutumlaufes. Archiv fur pathologische Anatomie und Physiologie und fur klinische Medicin (Virchows Archiv) 1886;105:1–28. doi: 10.1007/BF01925196.
    1. Velican C, Velican D. The neglected coronary atherosclerosis. Atherosclerosis. 1983;47:215–229. doi: 10.1016/0021-9150(83)90053-9.
    1. Velican C, Velican D. Progression of coronary atherosclerosis from adolescents to mature adults. Atherosclerosis. 1983;47:131–144. doi: 10.1016/0021-9150(83)90150-8.
    1. Velican C, Velican D. Study of coronary intimal thickening. Atherosclerosis. 1985;56:331–344. doi: 10.1016/0021-9150(85)90008-5.
    1. Velican C, Velican D. Coronary atherosclerosis: where are we now? Med Interne. 1988;26:5–13.
    1. Velican C, Velican D, Tancu I. Intimal thickening and atherosclerotic involvement of the left main coronary artery. Med Interne. 1985;23:95–101.
    1. Velican D, Petrescu C, Velican C. A light microscopic study on coronary atherosclerosis in an unselected population sample of Bucharest aged 41–50 years. Med Interne. 1983;21:161–167.
    1. Velican D, Petrescu C, Velican C. Prevalence of the "normal" aspect of the coronary arteries in an unselected population sample of Bucharest aged 1–60 years. Med Interne. 1987;25:113–119.
    1. Velican D, Velican C. Atherosclerotic involvement of the coronary arteries of adolescents and young adults. Atherosclerosis. 1980;36:449–460. doi: 10.1016/0021-9150(80)90238-5.
    1. Velican D, Velican C. Coronary anatomy and microarchitecture as related to coronary atherosclerotic involvement. Med Interne. 1989;27:257–262.
    1. Maladies de la paroi arterielle. Paris: Flammarion; 1987.
    1. Berry CL. In: Diseases of the arterial wall. Camilleri J-P, Berry CL, Fiessinger J-N, Bariety J, editor. London-New York: Springer-Verlag; 1989. Organogenesis of the arterial wall; pp. 56–70.
    1. Arteriosclerosis; a survey of the problem. 1. New York: The Macmillan Company; 1933.
    1. Anitschkow N. In: Arteriosclerosis; a survey of the problem. Cowdry EV, editor. New York: The Macmillan Company; 1933. Experimental arteriosclerosis in animals; pp. 271–322.
    1. Anitschkow N. Über die experimentelle Atherosklerose der Herzklappen. Virchows Archiv. 1915;220:233–256. doi: 10.1007/BF01949104.
    1. Anitschkow N. Zur Ätiologie der Atherosklerose. Virchows Archiv. 1924;249:73–82. doi: 10.1007/BF01891331.
    1. Mehta NJ, Khan IA. Cardiology's 10 greatest discoveries of the 20th century. Tex Heart Inst J. 2002;29:164–171.
    1. Friedman M, Friedland GW. Medicine's 10 greatest discoveries. New Haven: Yale University Press; 1998.
    1. Subotin M. Personal communication. 2007.
    1. Davies PF, Dewey CF Jr, Bussolari SR, Gordon EJ, Gimbrone MA Jr. Influence of hemodynamic forces on vascular endothelial function. In vitro studies of shear stress and pinocytosis in bovine aortic cells. J Clin Invest. 1984;73:1121–1129.
    1. Glagov S. Relation of structure to function in arterial walls. Artery. 1979;5:295–304.
    1. Hoshina K, Sho E, Sho M, Nakahashi TK, Dalman RL. Wall shear stress and strain modulate experimental aneurysm cellularity. J Vasc Surg. 2003;37:1067–1074.
    1. Ingber DE, Folkman J. Mechanochemical switching between growth and differentiation during fibroblast growth factor-stimulated angiogenesis in vitro: role of extracellular matrix. J Cell Biol. 1989;109:317–330. doi: 10.1083/jcb.109.1.317.
    1. Langille BL, O'Donnell F. Reductions in arterial diameter produced by chronic decreases in blood flow are endothelium-dependent. Science. 1986;231:405–407. doi: 10.1126/science.3941904.
    1. Masuda H, Kawamura K, Tohda K, Shozawa T, Sageshima M, Kamiya A. Increase in endothelial cell density before artery enlargement in flow-loaded canine carotid artery. Arteriosclerosis. 1989;9:812–823.
    1. Olesen SP, Clapham DE, Davies PF. Haemodynamic shear stress activates a K+ current in vascular endothelial cells. Nature. 1988;331:168–170. doi: 10.1038/331168a0.
    1. Sho E, Komatsu M, Sho M, Nanjo H, Singh TM, Xu C, Masuda H, Zarins CK. High flow drives vascular endothelial cell proliferation during flow-induced arterial remodeling associated with the expression of vascular endothelial growth factor. Exp Mol Pathol. 2003;75:1–11. doi: 10.1016/S0014-4800(03)00032-7.
    1. Sho E, Nanjo H, Sho M, Kobayashi M, Komatsu M, Kawamura K, Xu C, Zarins CK, Masuda H. Arterial enlargement, tortuosity, and intimal thickening in response to sequential exposure to high and low wall shear stress. J Vasc Surg. 2004;39:601–612. doi: 10.1016/j.jvs.2003.10.058.
    1. Sho E, Sho M, Singh TM, Nanjo H, Komatsu M, Xu C, Masuda H, Zarins CK. Arterial enlargement in response to high flow requires early expression of matrix metalloproteinases to degrade extracellular matrix. Exp Mol Pathol. 2002;73:142–153. doi: 10.1006/exmp.2002.2457.
    1. Sho E, Sho M, Singh TM, Xu C, Zarins CK, Masuda H. Blood flow decrease induces apoptosis of endothelial cells in previously dilated arteries resulting from chronic high blood flow. Arterioscler Thromb Vasc Biol. 2001;21:1139–1145. doi: 10.1161/hq0701.092118.
    1. Sho M, Sho E, Singh TM, Komatsu M, Sugita A, Xu C, Nanjo H, Zarins CK, Masuda H. Subnormal shear stress-induced intimal thickening requires medial smooth muscle cell proliferation and migration. Exp Mol Pathol. 2002;72:150–160. doi: 10.1006/exmp.2002.2426.
    1. Wolinsky H, Glagov S. A lamellar unit of aortic medial structure and function in mammals. Circ Res. 1967;20:99–111.
    1. Xu C, Lee S, Singh TM, Sho E, Li X, Sho M, Masuda H, Zarins CK. Molecular mechanisms of aortic wall remodeling in response to hypertension. J Vasc Surg. 2001;33:570–578. doi: 10.1067/mva.2001.112231.
    1. Yamauchi M, Takahashi M, Kobayashi M, Sho E, Nanjo H, Kawamura K, Masuda H. Normalization of high-flow or removal of flow cannot stop high-flow induced endothelial proliferation. Biomed Res. 2005;26:21–28. doi: 10.2220/biomedres.26.21.
    1. Karino T, Motomiya M, Goldsmith HL. Flow patterns at the major T-junctions of the dog descending aorta. J Biomech. 1990;23:537–548. doi: 10.1016/0021-9290(90)90047-7.
    1. Karino T, Goldsmith HL, Motomiya M, Mabuchi S, Sohara Y. Flow patterns in vessels of simple and complex geometries. Ann N Y Acad Sci. 1987;516:422–441. doi: 10.1111/j.1749-6632.1987.tb33063.x.
    1. Fukushima T, Karino T, Goldsmith HL. Disturbances of flow through transparent dog aortic arch. Heart Vessels. 1985;1:24–28. doi: 10.1007/BF02066483.
    1. Karino T, Goldsmith HL. Particle flow behavior in models of branching vessels. II. Effects of branching angle and diameter ratio on flow patterns. Biorheology. 1985;22:87–104.
    1. Karino T, Goldsmith HL. Disturbed flow in models of branching vessels. Trans Am Soc Artif Intern Organs. 1980;26:500–506.
    1. Karino T, Kwong HH, Goldsmith HL. Particle flow behaviour in models of branching vessels: I. Vortices in 90 degrees T-junctions. Biorheology. 1979;16:231–248.
    1. Endo S, Karino T, Goldsmith HL. Flow patterns in the dog descending aorta under a steady flow condition stimulating mid-systole. JSME International Journal, Series C. 2004;47:1000–1009. doi: 10.1299/jsmec.47.1000.
    1. Asakura T, Karino T. Flow patterns and spatial distribution of atherosclerotic lesions in human coronary arteries. Circ Res. 1990;66:1045–1066.
    1. Glagov S. Intimal hyperplasia, vascular modeling, and the restenosis problem. Circulation. 1994;89:2888–2891.
    1. Kamiya A, Bukhari R, Togawa T. Adaptive regulation of wall shear stress optimizing vascular tree function. Bull Math Biol. 1984;46:127–137.
    1. Kamiya A, Togawa T. Adaptive regulation of wall shear stress to flow change in the canine carotid artery. Am J Physiol. 1980;239:H14–21.
    1. Patterson C. Event Flow. Shear Stress Cues Vascular Development. Editorial. Arterioscler Thromb Vasc Biol. 2005;25:1761–1762. doi: 10.1161/01.ATV.0000175755.93591.56.
    1. Wang H, Riha GM, Yan S, Li M, Chai H, Yang H, Yao Q, Chen C. Shear stress induces endothelial differentiation from a murine embryonic mesenchymal progenitor cell line. Arterioscler Thromb Vasc Biol. 2005;25:1817–1823. doi: 10.1161/01.ATV.0000175840.90510.a8.
    1. Yamamoto K, Sokabe T, Watabe T, Miyazono K, Yamashita JK, Obi S, Ohura N, Matsushita A, Kamiya A, Ando J. Fluid shear stress induces differentiation of Flk-1-positive embryonic stem cells into vascular endothelial cells in vitro. Am J Physiol Heart Circ Physiol. 2005;288:H1915–1924. doi: 10.1152/ajpheart.00956.2004.
    1. Yamamoto K, Takahashi T, Asahara T, Ohura N, Sokabe T, Kamiya A, Ando J. Proliferation, differentiation, and tube formation by endothelial progenitor cells in response to shear stress. J Appl Physiol. 2003;95:2081–2088.
    1. Long ER. In: Cowdry's arteriosclerosis; a survey of the problem. 2. Blumenthal HT, editor. Springfield, Ill.: Thomas; 1967. Development of our Knowledge of Arteriosclerosis; pp. 5–20.
    1. Virchow R. In: Gesammelte Abhandlungen zur Wissenschaftlichen Medicin. Virchow R, editor. Frankfurt: Von Medinger Sohn; 1856. Phlogose und Thrombose in Gefägermanbsystem; pp. 458–636.
    1. Kuhn TS. The Structure of Scientific Revolutions. Chicago: University of Chicago Press; 1962.
    1. Kastelein JJ, van Leuven SI, Burgess L, Evans GW, Kuivenhoven JA, Barter PJ, Revkin JH, Grobbee DE, Riley WA, Shear CL. et al.Effect of Torcetrapib on Carotid Atherosclerosis in Familial Hypercholesterolemia. N Engl J Med. 2007;356(16):1620–30. doi: 10.1056/NEJMoa071359.
    1. Nissen SE, Tardif JC, Nicholls SJ, Revkin JH, Shear CL, Duggan WT, Ruzyllo W, Bachinsky WB, Lasala GP, Tuzcu EM. Effect of torcetrapib on the progression of coronary atherosclerosis. N Engl J Med. 2007;356:1304–1316. doi: 10.1056/NEJMoa070635.
    1. Tall AR. CETP Inhibitors to Increase HDL Cholesterol Levels. N Engl J Med. 2007;356
    1. Stehbens WE. Coronary heart disease, hypercholesterolemia, and atherosclerosis. I. False premises. Exp Mol Pathol. 2001;70:103–119. doi: 10.1006/exmp.2000.2340.
    1. Stehbens WE. Coronary heart disease, hypercholesterolemia, and atherosclerosis. II. Misrepresented data. Exp Mol Pathol. 2001;70:120–139. doi: 10.1006/exmp.2000.2339.
    1. Stehbens WE. The hypothetical epidemic of coronary heart disease and atherosclerosis. Med Hypotheses. 1995;45:449–454. doi: 10.1016/0306-9877(95)90219-8.
    1. Martin J. The idea is more important than the experiment. Lancet. 2000;356:934–937. doi: 10.1016/S0140-6736(00)02691-X.
    1. Romer AS. The vertebrate body. 6. Philadelphia: Saunders College Pub; 1986.
    1. Bergwerff M, DeRuiter MC, Gittenberger-de Groot AC. Comparative anatomy and ontogeny of the ductus arteriosus, a vascular outsider. Anat Embryol (Berl) 1999;200:559–571. doi: 10.1007/s004290050304.
    1. Augsburger HR, Kurzi M. Histomorphologic and morphometric evaluation of the uterine horns in nulliparous and multiparous Beagles. Am J Vet Res. 2004;65:552–558. doi: 10.2460/ajvr.2004.65.552.
    1. Blankenship TN, Enders AC. Modification of uterine vasculature during pregnancy in macaques. Microsc Res Tech. 2003;60:390–401. doi: 10.1002/jemt.10277.
    1. Obayashi S, Aso T, Sato J, Hamasaki H, Azuma H. Intimal hyperplasia in human uterine arteries accompanied by impaired synergism between prostaglandin I2 and nitric oxide. Br J Pharmacol. 1996;119:1072–1078.
    1. Cipolla M, Osol G. Hypertrophic and hyperplastic effects of pregnancy on the rat uterine arterial wall. Am J Obstet Gynecol. 1994;171:805–811.
    1. Kamiya S, Daigo M. Effect of pregnancy on gravid sclerosis of bovine uterine arteries. Nippon Juigaku Zasshi. 1989;51:1179–1184.
    1. Beppu M, Obayashi S, Aso T, Goto M, Azuma H. Endogenous nitric oxide synthase inhibitors in endothelial cells, endothelin-1 within the vessel wall, and intimal hyperplasia in perimenopausal human uterine arteries. J Cardiovasc Pharmacol. 2002;39:192–200. doi: 10.1097/00005344-200202000-00005.
    1. Crawford BS, Davis J, Harrigill K. Uterine artery atherosclerotic disease: histologic features and clinical correlation. Obstet Gynecol. 1997;90:210–215. doi: 10.1016/S0029-7844(97)00225-1.
    1. Heidger PM Jr, Van Orden DE, Farley DB. Electron microscopic and histochemical characterization of intra-arterial cushions of the rat and porcine uterine vascular bed. Acta Anat (Basel) 1983;117:239–247.
    1. Kardon RH, Farley DB, Heidger PM Jr, Van Orden DE. Intraarterial cushions of the rat uterine artery: a scanning electron microscope evaluation utilizing vascular casts. Anat Rec. 1982;203:19–29. doi: 10.1002/ar.1092030103.
    1. Whyte JO, Cisneros AI, Alvarez M, Alconchel MD, Yus C, Torres A, Sarrat R. Contributions to the study of the foetal development of physiological intimal thickening in the human uterine artery. Folia Morphol (Warsz) 2001;60:199–204.
    1. Loyaga-Rendon RY, Sakamoto S, Beppu M, Aso T, Ishizaka M, Takahashi R, Azuma H. Accumulated endogenous nitric oxide synthase inhibitors, enhanced arginase activity, attenuated dimethylarginine dimethylaminohydrolase activity and intimal hyperplasia in premenopausal human uterine arteries. Atherosclerosis. 2005;178:231–239. doi: 10.1016/j.atherosclerosis.2004.09.006.
    1. Newby AC, Zaltsman AB. Molecular mechanisms in intimal hyperplasia. J Pathol. 2000;190:300–309. doi: 10.1002/(SICI)1096-9896(200002)190:3<300::AID-PATH596>;2-I.
    1. Asmussen I. Ultrastructure of human umbilical arteries. Studies on arteries from newborn children delivered by nonsmoking, white group D, diabetic mothers. Circ Res. 1980;47:620–626.
    1. Takagi T, Toda T, Leszczynski D, Kummerow F. Ultrastructure of aging human umbilical artery and vein. Acta Anat (Basel) 1984;119:73–79.
    1. Stehbens WE, Wakefield JS, Gilbert-Barness E, Zuccollo JM. Histopathology and ultrastructure of human umbilical blood vessels. Fetal Pediatr Pathol. 2005;24:297–315. doi: 10.1080/15227950500503660.
    1. Osika W, Dangardt F, Gronros J, Lundstam U, Myredal A, Johansson M, Volkmann R, Gustavsson T, Gan LM, Friberg P. Increasing peripheral artery intima thickness from childhood to seniority. Arterioscler Thromb Vasc Biol. 2007;27:671–676. doi: 10.1161/01.ATV.0000256468.95403.6f.
    1. Simpson CF. Comparative morphology of intimal and adventitial hyperplasia of the arteriosclerotic turkey aorta. Exp Mol Pathol. 1972;17:65–76. doi: 10.1016/0014-4800(72)90058-5.
    1. Lindsay S, Chaikoff IL. In: Atherosclerosis and its origin. Sandler M, Bourne GH, editor. New York: Academic Press; 1963. Naturally occuring arteriosclerosis in animals: a comparison with experimentally induced lesions; pp. 349–437.
    1. Friedl R, Li J, Schumacher B, Hanke H, Waltenberger J, Hannekum A, Stracke S. Intimal hyperplasia and expression of transforming growth factor-beta1 in saphenous veins and internal mammary arteries before coronary artery surgery. Ann Thorac Surg. 2004;78:1312–1318. doi: 10.1016/j.athoracsur.2004.02.066.
    1. Weninger WJ, Muller GB, Reiter C, Meng S, Rabl SU. Intimal hyperplasia of the infant parasellar carotid artery: a potential developmental factor in atherosclerosis and SIDS. Circ Res. 1999;85:970–975.
    1. Elzenga NJ, Gittenberger-de Groot AC. Localised coarctation of the aorta. An age dependent spectrum. Br Heart J. 1983;49:317–323. doi: 10.1136/hrt.49.4.317.
    1. Head CE, Jowett VC, Sharland GK, Simpson JM. Timing of presentation and postnatal outcome of infants suspected of having coarctation of the aorta during fetal life. Heart. 2005;91:1070–1074. doi: 10.1136/hrt.2003.033027.
    1. Ohkubo M, Takahashi K, Kishiro M, Akimoto K, Yamashiro Y. Histological findings after angioplasty using conventional balloon, radiofrequency thermal balloon, and stent for experimental aortic coarctation. Pediatr Int. 2004;46:39–47. doi: 10.1111/j.1328-0867.2004.t01-1-.x.
    1. Navas-Acien A, Selvin E, Sharrett AR, Calderon-Aranda E, Silbergeld E, Guallar E. Lead, cadmium, smoking, and increased risk of peripheral arterial disease. Circulation. 2004;109:3196–3201. doi: 10.1161/01.CIR.0000130848.18636.B2.
    1. Ridker PM, Stampfer MJ, Rifai N. Novel risk factors for systemic atherosclerosis: a comparison of C-reactive protein, fibrinogen, homocysteine, lipoprotein(a), and standard cholesterol screening as predictors of peripheral arterial disease. Jama. 2001;285:2481–2485. doi: 10.1001/jama.285.19.2481.
    1. Inoue S, Koyama H, Miyata T, Shigematsu H. Pathogenetic heterogeneity of in-stent lesion formation in human peripheral arterial disease. J Vasc Surg. 2002;35:672–678. doi: 10.1067/mva.2002.122021.
    1. Opie SR, Dib N. Local endovascular delivery, gene therapy, and cell transplantation for peripheral arterial disease. J Endovasc Ther. 2004;11(Suppl 2):II151–162.
    1. Sidawy AN, Weiswasser JM, Waksman R. Peripheral vascular brachytherapy. J Vasc Surg. 2002;35:1041–1047. doi: 10.1067/mva.2002.123751.
    1. Cappell MS. Intestinal (mesenteric) vasculopathy. II. Ischemic colitis and chronic mesenteric ischemia. Gastroenterol Clin North Am. 1998;27:827–860. doi: 10.1016/S0889-8553(05)70034-0.
    1. Jarvinen O, Sisto T, Laurikka J, Tarkka M. Intimal thickening and fragmentation of the internal elastic lamina in the mesenteric arteries. Apmis. 1996;104:395–400.
    1. Stokes JB, Bonsib SM, McBride JW. Diffuse intimal fibromuscular dysplasia with multiorgan failure. Arch Intern Med. 1996;156:2611–2614. doi: 10.1001/archinte.156.22.2611.
    1. Zochodne D. Von Recklinghausen's vasculopathy. Am J Med Sci. 1984;287:64–65. doi: 10.1097/00000441-198401000-00021.
    1. Walpoth BH, Rogulenko R, Tikhvinskaia E, Gogolewski S, Schaffner T, Hess OM, Althaus U. Improvement of patency rate in heparin-coated small synthetic vascular grafts. Circulation. 1998;98:II319–323. discussion II324.
    1. Walpoth BH, Pavlicek M, Celik B, Nicolaus B, Schaffner T, Althaus U, Hess OM, Carrel T, Morris RE. Prevention of neointimal proliferation by immunosuppression in synthetic vascular grafts. Eur J Cardiothorac Surg. 2001;19:487–492. doi: 10.1016/S1010-7940(01)00582-6.
    1. Herring M, Smith J, Dalsing M, Glover J, Compton R, Etchberger K, Zollinger T. Endothelial seeding of polytetrafluoroethylene femoral popliteal bypasses: the failure of low-density seeding to improve patency. J Vasc Surg. 1994;20:650–655.
    1. Jensen N, Lindblad B, Bergqvist D. Endothelial cell seeded dacron aortobifurcated grafts: platelet deposition and long-term follow-up. J Cardiovasc Surg (Torino) 1994;35:425–429.
    1. Sapienza P, di Marzo L, Cucina A, Corvino V, Mingoli A, Giustiniani Q, Ziparo E, Cavallaro A. Release of PDGF-BB and bFGF by human endothelial cells seeded on expanded polytetrafluoroethylene vascular grafts. J Surg Res. 1998;75:24–29. doi: 10.1006/jsre.1997.5260.
    1. Schmidt SP, Meerbaum SO, Anderson JM, Clarke RE, Zellers RA, Sharp WV. Evaluation of expanded polytetrafluoroethylene arteriovenous access grafts onto which microvessel-derived cells were transplanted to "improve" graft performance: preliminary results. Ann Vasc Surg. 1998;12:405–411. doi: 10.1007/s100169900176.
    1. Kumar A, Lindner V. Remodeling with neointima formation in the mouse carotid artery after cessation of blood flow. Arterioscler Thromb Vasc Biol. 1997;17:2238–2244.
    1. Ahn HS, Chackalamannil S, Boykow G, Graziano MP, Foster C. Development of proteinase-activated receptor 1 antagonists as therapeutic agents for thrombosis, restenosis and inflammatory diseases. Curr Pharm Des. 2003;9:2349–2365. doi: 10.2174/1381612033453884.
    1. Donners MM, Daemen MJ, Cleutjens KB, Heeneman S. Inflammation and restenosis: implications for therapy. Ann Med. 2003;35:523–531. doi: 10.1080/07853890310014876.
    1. Ferns GA, Raines EW, Sprugel KH, Motani AS, Reidy MA, Ross R. Inhibition of neointimal smooth muscle accumulation after angioplasty by an antibody to PDGF. Science. 1991;253:1129–1132. doi: 10.1126/science.1653454.
    1. Kitamoto S, Egashira K, Takeshita A. Stress and vascular responses: anti-inflammatory therapeutic strategy against atherosclerosis and restenosis after coronary intervention. J Pharmacol Sci. 2003;91:192–196. doi: 10.1254/jphs.91.192.
    1. Ross R. Atherosclerosis – an inflammatory disease. N Engl J Med. 1999;340:115–126. doi: 10.1056/NEJM199901143400207.
    1. Schillinger M, Minar E. Restenosis after percutaneous angioplasty: the role of vascular inflammation. Vasc Health Risk Manag. 2005;1:73–78. doi: 10.2147/vhrm.1.1.73.58932.
    1. Versaci F, Gaspardone A. Prevention of restenosis after stenting: the emerging role of inflammation. Coron Artery Dis. 2004;15:307–311. doi: 10.1097/00019501-200409000-00002.
    1. Klitkou J, Jensen LO, Hansen HS, Thayssen P. High sensitive C-reactive protein and interleukin 6 are not related to neointimal hyperplasia in paclitaxel eluting stents or bare metal stents. An intravascular ultrasound study. Int J Cardiol. 2007;119:114–116. doi: 10.1016/j.ijcard.2006.07.073.
    1. Sartore S, Chiavegato A, Faggin E, Franch R, Puato M, Ausoni S, Pauletto P. Contribution of adventitial fibroblasts to neointima formation and vascular remodeling: from innocent bystander to active participant. Circ Res. 2001;89:1111–1121. doi: 10.1161/hh2401.100844.
    1. Arciniegas E, Ponce L, Hartt Y, Graterol A, Carlini RG. Intimal thickening involves transdifferentiation of embryonic endothelial cells. Anat Rec. 2000;258:47–57. doi: 10.1002/(SICI)1097-0185(20000101)258:1<47::AID-AR6>;2-W.
    1. Skowasch D, Jabs A, Andrie R, Dinkelbach S, Luderitz B, Bauriedel G. Presence of bone-marrow- and neural-crest-derived cells in intimal hyperplasia at the time of clinical in-stent restenosis. Cardiovasc Res. 2003;60:684–691. doi: 10.1016/j.cardiores.2003.09.001.
    1. Carmeliet P, Moons L, Stassen JM, De Mol M, Bouche A, van den Oord JJ, Kockx M, Collen D. Vascular wound healing and neointima formation induced by perivascular electric injury in mice. Am J Pathol. 1997;150:761–776.
    1. Subbotin V, Sun H, Aitouche A, Salam A, Valdivia LA, Fung JJ, Starzl TE, Rao AS. Marked mitigation of transplant vascular sclerosis in FasLgld (CD95L) mutant recipients. The role of alloantibodies in the development of chronic rejection. Transplantation. 1999;67:1295–1300. doi: 10.1097/00007890-199905270-00001.
    1. Subbotin V, Sun H, Aitouche A, Valdivia LA, Fung JJ, Starzl TE, Rao AS. Abrogation of chronic rejection in a murine model of aortic allotransplantation by prior induction of donor-specific tolerance. Transplantation. 1997;64:690–695. doi: 10.1097/00007890-199709150-00005.
    1. Alroy J. Cope's rule and the dynamics of body mass evolution in North American fossil mammals. Science. 1998;280:731–734. doi: 10.1126/science.280.5364.731.
    1. Damuth J. Cope's rule, the island rule and the scaling of mammalian population density. Nature. 1993;365:748–750. doi: 10.1038/365748a0.
    1. Shah M, Jeffery RW, Hannan PJ, Onstad L. Relationship between socio-demographic and behaviour variables, and body mass index in a population with high-normal blood pressure: Hypertension Prevention Trial. Eur J Clin Nutr. 1989;43:583–596.
    1. Nuzzo V, Tauchmanova L, Fonderico F, Trotta R, Fittipaldi MR, Fontana D, Rossi R, Lombardi G, Trimarco B, Lupoli G. Increased intima-media thickness of the carotid artery wall, normal blood pressure profile and normal left ventricular mass in subjects with primary hyperparathyroidism. Eur J Endocrinol. 2002;147:453–459. doi: 10.1530/eje.0.1470453.
    1. Freitag MH, Vasan RS. What is normal blood pressure? Curr Opin Nephrol Hypertens. 2003;12:285–292. doi: 10.1097/00041552-200305000-00010.
    1. Czarnecka D, Bilo G. A patient with high normal blood pressure – Should we treat? Blood Press. 2005;14(Suppl 2):50–52. doi: 10.1080/08038020500424715.
    1. Bolande RP, Leistikow EA, Wartman FS 3rd, Louis TM. The development of preatherosclerotic coronary artery lesions in perinatal piglets. Biol Neonate. 1996;69:109–118.
    1. Boucek RJ, Fojaco R, Takashita R. Anatomic Considerations for Regional Intimal Changes in the Coronary Arteries (Dog) Anat Rec. 1964;148:161–169. doi: 10.1002/ar.1091480206.
    1. Cohen MP, Yu-Wu V. Age-related changes in non-enzymatic glycosylation of human basement membranes. Exp Gerontol. 1983;18:461–469. doi: 10.1016/0531-5565(83)90025-6.
    1. Gerrity RG, Cliff WJ. The aortic tunica intima in young and aging rats. Exp Mol Pathol. 1972;16:382–402. doi: 10.1016/0014-4800(72)90012-3.
    1. Krus S, Turjman MW, Flejka E. Comparative morphology of the hepatic and coronary artery walls. Part II. The relation between the internal elastic membrane, non- atherosclerotic intimal thickening and atherosclerosis. Med Sci Monit. 2000;6:249–252.
    1. Yoro T, Burnstock G. Fine structure of "intimal cushions" at branching sites in coronary arteries of vertebrates. A scanning and transmission electron microscopic study. Z Anat Entwicklungsgesch. 1973;140:187–202. doi: 10.1007/BF00520330.
    1. Masuda H, Kawamura K, Nanjo H, Sho E, Komatsu M, Sugiyama T, Sugita A, Asari Y, Kobayashi M, Ebina T. et al.Ultrastructure of endothelial cells under flow alteration. Microsc Res Tech. 2003;60:2–12. doi: 10.1002/jemt.10237.
    1. Nanjo H, Sho E, Komatsu M, Sho M, Zarins CK, Masuda H. Intermittent short-duration exposure to low wall shear stress induces intimal thickening in arteries exposed to chronic high shear stress. Exp Mol Pathol. 2006;80:38–45.
    1. Tohda K, Masuda H, Kawamura K, Shozawa T. Difference in dilatation between endothelium-preserved and -desquamated segments in the flow-loaded rat common carotid artery. Arterioscler Thromb. 1992;12:519–528.
    1. Sunamura M, Ishibashi H, Karino T. Flow patterns and preferred sites of intimal thickening in diameter-mismatched vein graft interpositions. Surgery. 2007;141:764–776. doi: 10.1016/j.surg.2006.12.019.
    1. Moore JE Jr, Ku DN, Zarins CK, Glagov S. Pulsatile flow visualization in the abdominal aorta under differing physiologic conditions: implications for increased susceptibility to atherosclerosis. J Biomech Eng. 1992;114:391–397.
    1. Niebauer J, Cooke JP. Cardiovascular effects of exercise: role of endothelial shear stress. J Am Coll Cardiol. 1996;28:1652–1660. doi: 10.1016/S0735-1097(96)00393-2.
    1. Vermot-Desroches C, Marchand D, Roy C, Wijdenes J. Heterogeneity of antigen expression among human umbilical cord vascular endothelial cells: identification of cell subsets by co-expression of haemopoietic antigens. Immunol Lett. 1995;48:1–9. doi: 10.1016/0165-2478(95)02432-8.
    1. Baron M. Induction of embryonic hematopoietic and endothelial stem/progenitor cells by hedgehog-mediated signals. Differentiation. 2001;68:175–185. doi: 10.1046/j.1432-0436.2001.680405.x.
    1. Dickson MC, Martin JS, Cousins FM, Kulkarni AB, Karlsson S, Akhurst RJ. Defective haematopoiesis and vasculogenesis in transforming growth factor-beta 1 knock out mice. Development. 1995;121:1845–1854.
    1. Downs KM. Florence Sabin and the mechanism of blood vessel lumenization during vasculogenesis. Microcirculation. 2003;10:5–25.
    1. Sanchez M, Gottgens B, Sinclair AM, Stanley M, Begley CG, Hunter S, Green AR. An SCL 3' enhancer targets developing endothelium together with embryonic and adult haematopoietic progenitors. Development. 1999;126:3891–3904.
    1. Wood HB, May G, Healy L, Enver T, Morriss-Kay GM. CD34 expression patterns during early mouse development are related to modes of blood vessel formation and reveal additional sites of hematopoiesis. Blood. 1997;90:2300–2311.
    1. Bergwerff M, DeRuiter MC, Hall S, Poelmann RE, Gittenberger-de Groot AC. Unique vascular morphology of the fourth aortic arches: possible implications for pathogenesis of type-B aortic arch interruption and anomalous right subclavian artery. Cardiovasc Res. 1999;44:185–196. doi: 10.1016/S0008-6363(99)00186-8.
    1. Brand T. Heart development: molecular insights into cardiac specification and early morphogenesis. Dev Biol. 2003;258:1–19. doi: 10.1016/S0012-1606(03)00112-X.
    1. Fitzgerald MC, Schwarzbauer JE. Importance of the basement membrane protein SPARC for viability and fertility in Caenorhabditis elegans. Curr Biol. 1998;8:1285–1288. doi: 10.1016/S0960-9822(07)00540-4.
    1. Paralkar VM, Vukicevic S, Reddi AH. Transforming growth factor beta type 1 binds to collagen IV of basement membrane matrix: implications for development. Dev Biol. 1991;143:303–308. doi: 10.1016/0012-1606(91)90081-D.
    1. Aird WC. Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circ Res. 2007;100:158–173. doi: 10.1161/01.RES.0000255691.76142.4a.
    1. Ballermann BJ, Dardik A, Eng E, Liu A. Shear stress and the endothelium. Kidney Int Suppl. 1998;67:S100–108. doi: 10.1046/j.1523-1755.1998.06720.x.
    1. Gloe T, Sohn HY, Meininger GA, Pohl U. Shear stress-induced release of basic fibroblast growth factor from endothelial cells is mediated by matrix interaction via integrin alpha(v)beta3. J Biol Chem. 2002;277:23453–23458. doi: 10.1074/jbc.M203889200.
    1. Ковалевский AO. Избранные Работы. Ленинград: Академия Наук СССР; 1951.
    1. Garcia-Fernandez J, Holland PW. Archetypal organization of the amphioxus Hox gene cluster. Nature. 1994;370:563–566. doi: 10.1038/370563a0.
    1. Dobzhansky T. Nothing in Biology Makes Sense Except in the Light of Evolution. The American Biology Teacher. 1973;35:125–129.
    1. Lee MSY. Divergent evolution, hierarchy and cladistics. Zoologica Scripta. 2002;31:217–219. doi: 10.1046/j.1463-6409.2002.00101.x.
    1. Brown TL. Making Truth. The Roles of Metaphor in Science. Urbana: University of Illinois Press; 2003.
    1. Wallitt EJ, Jevon M, Hornick PI. Therapeutics of vein graft intimal hyperplasia: 100 years on. Ann Thorac Surg. 2007;84:317–323. doi: 10.1016/j.athoracsur.2007.02.035.
    1. Islam S, Ribeiro AA, Loesch A. Basilar artery of the capybara (Hydrochaeris hydrochaeris): an ultrastructural study. Anat Histol Embryol. 2004;33:81–89. doi: 10.1111/j.1439-0264.2003.00519.x.

Source: PubMed

3
Abonneren