Loss of mural cells leads to wall degeneration, aneurysm growth, and eventual rupture in a rat aneurysm model

Stroke

Volumn 45, Issue 1, 2014, Pages 248-254

  Marbacher, Serge ^a   Marjamaa, Johan ^a   Bradacova, Katerina ^a   Von Gunten, Michael ^b   Honkanen, Petri ^a   Abo Ramadan, Usama ^c   Hernesniemi, Juha ^a   Niemelä, Mika ^a   Frösen, Juhana ^a  

^a HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^b Institute of Pathology Länggasse   (Switzerland)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Aneurysm rupture; Degeneration; Inflammation; Intracranial aneurysm; Smooth muscle cells; Thrombosis

Indexed keywords

DODECYL SULFATE SODIUM;

ABDOMINAL AORTA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ARTERY ANEURYSM RUPTURE; BRAIN DEGENERATION; BRAIN PERICYTE; CONTRAST ENHANCEMENT; CONTROLLED STUDY; ENCEPHALITIS; FIBROSIS; HISTOLOGY; IMAGE ANALYSIS; MAGNETIC RESONANCE ANGIOGRAPHY; MALE; NEUROENDOSCOPY; NEUTROPHIL; NONHUMAN; OCCLUSIVE CEREBROVASCULAR DISEASE; PRIORITY JOURNAL; RAT; RECANALIZATION; SACCULAR ANEURYSM; SACCULAR INTRACRANIAL ANEURYSM RUPTURE; SUBARACHNOID HEMORRHAGE; THORACIC AORTA;

EID: 85027947089     PISSN: 00392499     EISSN: 15244628     Source Type: Journal    
DOI: 10.1161/STROKEAHA.113.002745     Document Type: Article

References (30)

1. Taylor TN, Davis PH, Torner JC, Holmes J, Meyer JW, Jacobson MF. Lifetime cost of stroke in the United States. Stroke. 1996;27:1459-1466.
2. Morita A, Kirino T, Hashi K, Aoki N, Fukuhara S, Hashimoto N, et al; UCAS Japan Investigators. The natural course of unruptured cerebral aneurysms in a Japanese cohort. N Engl J Med. 2012;366:2474-2482.
3. Wiebers DO, Whisnant JP, Huston J III, Meissner I, Brown RD Jr, Piepgras DG, et al; International Study of Unruptured Intracranial Aneurysms Investigators. Unruptured intracranial aneurysms: natural history, clinical outcome, and risks of surgical and endovascular treatment. Lancet. 2003;362:103-110.
4. Frösen J, Piippo A, Paetau A, Kangasniemi M, Niemelä M, Hernesniemi J, et al. Remodeling of saccular cerebral artery aneurysm wall is associated with rupture: histological analysis of 24 unruptured and 42 ruptured cases. Stroke. 2004;35:2287-2293.
5. Kataoka K, Taneda M, Asai T, Kinoshita A, Ito M, Kuroda R. Structural fragility and inflammatory response of ruptured cerebral aneurysms. A comparative study between ruptured and unruptured cerebral aneurysms. Stroke. 1999;30:1396-1401.
6. Frösen J, Marjamaa J, Myllärniemi M, Abo-Ramadan U, Tulamo R, Niemelä M, et al. Contribution of mural and bone marrow-derived neointimal cells to thrombus organization and wall remodeling in a microsurgical murine saccular aneurysm model. Neurosurgery. 2006;58:936-944, discussion 936.
7. Nakajima N, Nagahiro S, Sano T, Satomi J, Satoh K. Phenotypic modulation of smooth muscle cells in human cerebral aneurysmal walls. Acta Neuropathol. 2000;100:475-480.
8. Frösen J, Tulamo R, Paetau A, Laaksamo E, Korja M, Laakso A, et al. Saccular intracranial aneurysm: pathology and mechanisms. Acta Neuropathol. 2012;123:773-786.
9. Chalouhi N, Ali MS, Jabbour PM, Tjoumakaris SI, Gonzalez LF, Rosenwasser RH, et al. Biology of intracranial aneurysms: role of inflammation. J Cereb Blood Flow Metab. 2012;32:1659-1676.
10. Krings T, Mandell DM, Kiehl TR, Geibprasert S, Tymianski M, Alvarez H, et al. Intracranial aneurysms: from vessel wall pathology to therapeutic approach. Nat Rev Neurol. 2011;7:547-559.
11. Kulcsár Z, Houdart E, Bonafé A, Parker G, Millar J, Goddard AJ, et al. Intraaneurysmal thrombosis as a possible cause of delayed aneurysm rupture after flow-diversion treatment. AJNR Am J Neuroradiol. 2011;32:20-25.
12. Marjamaa J, Tulamo R, Frösen J, Abo-Ramadan U, Hernesniemi JA, Niemelä MR, et al. Occlusion of neck remnant in experimental rat aneurysms after treatment with platinum-or polyglycolic-polylactic acidcoated coils. Surg Neurol. 2009;71:458-465, discussion 465.
13. Yoshino Y, Niimi Y, Song JK, Khoyama S, Shin YS, Berenstein A. Preventing spontaneous thrombosis of experimental sidewall aneurysms: the oblique cut. AJNR Am J Neuroradiol. 2005;26:1363-1365.
14. Black SP, German WJ. Observations on the relationship between the volume and the size of the orifice of experimental aneurysms. J Neurosurg. 1960;17:984-990.
15. Allaire E, Guettier C, Bruneval P, Plissonnier D, Michel JB. Cell-free arterial grafts: morphologic characteristics of aortic isografts, allografts, and xenografts in rats. J Vasc Surg. 1994;19:446-456.
16. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9:671-675.
17. Marjamaa J, Antell H, Abo-Ramadan U, Hernesniemi JA, Niemelä MR, Kangasniemi M. High-resolution TOF MR angiography at 4.7 Tesla for volumetric and morphologic evaluation of coiled aneurysm neck remnants in a rat model. Acta Radiol. 2011;52:340-348.
18. Yushkevich PA, Piven J, Hazlett HC, Smith RG, Ho S, Gee JC, et al. User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage. 2006;31:1116-1128.
19. Lee D, Yuki I, Murayama Y, Chiang A, Nishimura I, Vinters HV, et al. Thrombus organization and healing in the swine experimental aneurysm model. Part I. A histological and molecular analysis. J Neurosurg. 2007;107:94-108.
20. Kuijper PH, Gallardo Torres HI, Lammers JW, Sixma JJ, Koenderman L, Zwaginga JJ. Platelet and fibrin deposition at the damaged vessel wall: cooperative substrates for neutrophil adhesion under flow conditions. Blood. 1997;89:166-175.
21. Houard X, Touat Z, Ollivier V, Louedec L, Philippe M, Sebbag U, et al. Mediators of neutrophil recruitment in human abdominal aortic aneurysms. Cardiovasc Res. 2009;82:532-541.
22. Koole D, Zandvoort HJ, Schoneveld A, Vink A, Vos JA, van den Hoogen LL, et al. Intraluminal abdominal aortic aneurysm thrombus is associated with disruption of wall integrity. J Vasc Surg. 2013;57:77-83.
23. Fontaine V, Jacob MP, Houard X, Rossignol P, Plissonnier D, Angles-Cano E, et al. Involvement of the mural thrombus as a site of protease release and activation in human aortic aneurysms. Am J Pathol. 2002;161:1701-1710.
24. Martin-Ventura JL, Madrigal-Matute J, Martinez-Pinna R, Ramos-Mozo P, Blanco-Colio LM, Moreno JA, et al. Erythrocytes, leukocytes and platelets as a source of oxidative stress in chronic vascular diseases: detoxifying mechanisms and potential therapeutic options. Thromb Haemost. 2012;108:435-442.
25. Mack CP. Signaling mechanisms that regulate smooth muscle cell differentiation. Arterioscler Thromb Vasc Biol. 2011;31:1495-1505.
26. Churchman AT, Anwar AA, Li FY, Sato H, Ishii T, Mann GE, et al. Transforming growth factor-beta1 elicits Nrf2-mediated antioxidant responses in aortic smooth muscle cells. J Cell Mol Med. 2009;13: 2282-2292.
27. Folkesson M, Silveira A, Eriksson P, Swedenborg J. Protease activity in the multi-layered intra-luminal thrombus of abdominal aortic aneurysms. Atherosclerosis. 2011;218:294-299.
28. Dahl SL, Koh J, Prabhakar V, Niklason LE. Decellularized native and engineered arterial scaffolds for transplantation. Cell Transplant. 2003;12:659-666.
29. Hashimoto N, Handa H, Hazama F. Experimentally induced cerebral aneurysms in rats. Surg Neurol. 1978;10:3-8.
30. Nuki Y, Tsou TL, Kurihara C, Kanematsu M, Kanematsu Y, Hashimoto T. Elastase-induced intracranial aneurysms in hypertensive mice. Hypertension. 2009;54:1337-1344.