Cardiovascular Pathology
Volume 20, Issue 2 , Pages 114-123 , March 2011

Animal models of abdominal aortic aneurysm and their role in furthering management of human disease

Received 2 September 2009 ,Revised 2 November 2009 ,Accepted 4 January 2010.

References 

  1. Balestrieri ML, Giovane A, Mancini FP, Napoli C. Proteomics and cardiovascular disease: an update. Curr Med Chem. 2008;15:555–572
  2. Powell JT, Norman PE. Abdominal aortic aneurysm events in postmenopausal women. Br Med J. 2008;337
  3. Gillum RF. Epidemiology of aortic aneurysm in the United States. J Clin Epidemiol. 1995;48:1289–1298
  4. Thompson MM. Controlling the expansion of abdominal aortic aneurysms. Br J Surg. 2003;90:897–898
  5. Sakalihasan N, Limet R, Defawe OD. Abdominal aortic aneurysm. Lancet. 2005;365:1577–1589
  6. Harthun NL. Current issues in the treatment of women with abdominal aortic aneurysm. Gender Medicine. 2008;5:36–43
  7. Golledge J, Tsao PS, Dalman RL, Norman PE. Circulating markers of abdominal aortic aneurysm presence and progression. Circulation. 2008;118:2382–2392
  8. Timaran CH, Veith FJ, Rosero EB, Modrall JG, Arko FR, Clagett GP, et al. Endovascular aortic aneurysm repair in patients with the highest risk and in-hospital mortality in the United States. Arch Surg. 2007;142:520–524[discussion 524–5]
  9. Vardulaki KA, Walker NM, Day NE, Duffy SW, Ashton HA, Scott RAP. Quantifying the risks of hypertension, age, sex and smoking in patients with abdominal aortic aneurysm. Br J Surg. 2000;87:195–200
  10. Clancy P, Oliver L, Jayalath R, Buttner P, Golledge J. Assessment of a serum assay for quantification of abdominal aortic calcification. Arterioscler Thromb Vasc Biol. 2006;26:2574–2576
  11. Golledge J, Muller J, Daugherty A, Norman P. Abdominal aortic aneurysm: pathogenesis and implications for management. Arterioscler Thromb Vasc Biol. 2006;26:2605–2613
  12. Brady AR, Thompson SG, Fowkes FG, Greenhalgh RM, Powell JT UK Small Aneurysm Trial Participants. Abdominal aortic aneurysm expansion: risk factors and time intervals for surveillance. Circulation. 2004;110:16–21
  13. Powell JT. Familial clustering of abdominal aortic aneurysm—smoke signals, but no culprit genes. Br J Surg. 2003;90:1173–1174
  14. Golledge J, Karan M, Moran CS, Muller J, Clancy P, Dear AE, et al. Reduced expansion rate of abdominal aortic aneurysms in patients with diabetes may be related to aberrant monocyte–matrix interactions. Eur Heart J. 2008;29:665–672
  15. Norman PE, Davis TM, Le MT, Golledge J. Matrix biology of abdominal aortic aneurysms in diabetes: mechanisms underlying the negative association. Connect Tissue Res. 2007;48:125–131
  16. Johnston KW, Rutherford RB, Tilson MD, Shah DM, Hollier L, Stanley JC. Suggested standards for reporting on arterial aneurysms. Subcommittee on Reporting Standards for Arterial Aneurysms, Ad Hoc Committee on Reporting Standards, Society for Vascular Surgery and North American Chapter, International Society for Cardiovascular Surgery. J Vasc Surg. 1991;1991:3
  17. Humphery JD, Taylor CA. Intracranial and abdominal aortic aneurysms: similarities, differences and need for a new class of computational models. Ann Rev Biomed Eng. 2008;10:221–246
  18. Annambhotla S, Bourgeois S, Wang X, Lin PH, Yao Q, Chen C. Recent advances in molecular mechanisms of abdominal aortic aneurysm formation. World J Surg. 2008;32:976–986
  19. Shimizu K, Mitchell RN, Libby P. Inflammation and cellular immune responses in abdominal aortic aneurysms. Arterioscler Thromb Vasc Biol. 2006;26:987–994
  20. Jones WB, Taylor SM, Kalbaugh CA, Joels CS, Blackhurst DW, Langan EM, et al. Lost to follow-up: a potential under-appreciated limitation of endovascular aneurysm repair. J Vas Surg. 2007;46:434–440
  21. Brox AC, Filion KB, Zhang X, Pilote M, Obrand D, Haider S, et al. In-hospital cost of abdominal aortic aneurysm repair in Canada and the United States. Arch Intern Med. 2003;163:2500–2504
  22. Scholz M, Mucke T, von During M, Pechlivanis I, Schmieder K, Harders AG. Microsurgically induced aneurysm models in rats: Part I. Techniques and histological examination. Minim Invasive Neurosurg. 2008;51:76–82
  23. Arends J, Perkins KD, Zhang J, Polyakov I, Lee F. A new technique for the surgical creation of aneurysms in an in vivo tortuous vessel model to test neurovascular devices. J Invest Surg. 2008;21:39–45
  24. Huynh H, Elkouri S, Beaudoin N, Brunea L, Guimond C, Daniel V, et al. Totally laparoscopic aortic surgery: comparison of the apron and retrocolic techniques in a porcine model. Vasc Endovascular Surg. 2007;41:230–238
  25. Daugherty A, Cassis LA. Mouse models of abdominal aortic aneurysms. Arterioscler Thromb Vasc Biol. 2004;24:429–434
  26. Geurts AM, Cost GJ, Freyvert Y, Zeitler B, Miller JC, Choi VM, et al. Knockout rats via embryo microinjection of zinc-finger nucleases. Science. 2009;325:433
  27. Conn MP. Sourcebook of models for biomedical research. Totowa, New Jersey 07512: Humana Press; 2008;
  28. Marinov GR, Marois Y, Paris E, Roby P, Formichi M, Douville Y, et al. Can the infusion of elastase in the abdominal aorta of the Yucatán miniature swine consistently produce experimental aneurysms?. J Invest Surg. 1997;10:129–150
  29. Powell JT. Models of arterial aneurysm: for the investigation of pathogenesis and pharmacotherapy — a review. Atherosclerosis. 1991;87:93–102
  30. Gresham GA, Howard AN. Aortic rupture in the turkey. J Atheroscler Res. 1961;1:17–80
  31. Abildgaard CF, Harrison J, JC A. Comparative study of blood coagulation in nonhuman primates. J Appl Physiol. 1971;30:400–405
  32. Anidjar S, Osborne-Pellegrin M, Coutard M, Michel JB. Arterial hypertension and aneurysmal dilation. Kidney Int. 1992;37:61–66
  33. Chiou AC, Chiu B, Pearce WH. Murine aortic aneurysm produced by periarterial application of calcium chloride. J Surg Res. 2001;99:371–376
  34. Rush C, Nyara M, Moxon JV, Trollope A, Cullen B, Golledge J. Whole genome expression analysis within the angiotensin II–apolipoprotein E deficient mouse model of abdominal aortic aneurysm. BMC Genomics. 2009;10:298
  35. Piedrahita JA, Zhang SH, Hagaman JR, Oliver PM, Maeda N. Generation of mice carrying a mutant apolipoprotein E gene inactivated by gene targeting in embryonic stem cells. PNAS. 1992;89:4471–4475
  36. Moláček J, Treska V, Kobr J, Certik B, Skalicky T, Kuntscher V, et al. Optimization of the model of abdominal aortic aneurysm—experiment in an animal model. J Vasc Res. 2009;46:1–5
  37. 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
  38. Allaire E, Forough R, Wang T, Clowes MM, Clowes AW. Tissue metalloproteinase inhibitor-1 (TIMP-1) overexpression prevents arterial rupture and dilatation in a xenograft model. FASEB J. 1996;10:A1134
  39. Zatina MA, Zarins CK, Gewertz BL, Glagov S. Role of medial lamellar architecture in the pathogenesis of aortic aneurysms. J Vas Surg. 1984;1:442–448
  40. Schmoker JD, Lee CH, Taylor RG, Chung A, Trombley L, Hardin N, et al. A novel model of blunt thoracic aortic injury: a mechanism confirmed?. J Trauma. 2008;64:923–931
  41. German WJ, Black SPW. Experimental production of carotid aneurysms. N Engl J Med. 1954;250:104–106
  42. Kajimoto M, Shimono T, Hirano K, Miyake Y, Kato N, Imanaka-Yoshida K, et al. Basic fibroblast growth factor slow release stent graft for endovascular aortic aneurysm repair: a canine model experiment. J Vas Surg. 2008;48:1306–1314
  43. Murphy EH, Johnson ED, Arko FR. Device-specific resistance to in vivo displacement of stent-grafts implanted with maximum iliac fixation. J Endovasc Ther. 2007;14:585–592
  44. Lerouge S, Raymond J, Salazkin I, Qin Z, Gaboury L, Cloutier G, et al. Endovascular aortic aneurysm repair with stent-grafts: experimental models can reproduce endoleaks. J Vasc Interv Radiol. 2004;15:971–979
  45. Soulez G, Lerouge S, Salazkin I, Darsaut T, Oliva VL, Raymond J. Type I and collateral flow in experimental aneurysm models treated with stent-grafts. J Vasc Interv Radiol. 2007;18:265–272
  46. Gao L, Hoi Y, Swartz DD, Kolega J, Siddiqui A, Meng H. Nascent aneurysm formation at the basilar terminus induced by hemodynamics. Stroke. 2008;39:2085–2090
  47. Yoshino Y, Niimi Y, Song JK, Khoyama S, Shin YS, Berenstein A. Preventing spontaneous thrombosis of experimental sidewall aneurysms: the oblique cut. AJNR. 2005;26:1363–1365
  48. Mucke T, Scholz M, Kesting MR, Wolff KD, Schmieder K, Harders AG. Microsurgically induced aneurysm models in rats: Part II. Clipping, shrinking and micro-Doppler sonography. Minim Invasive Neurosurg. 2008;51:6–10
  49. Turk AS, Aagaard-Kienitz B, Niemann D, Consigny D, Rappe A, Grinde J, et al. Natural history of the canine vein pouch aneurysm model. AJNR. 2007;28:531–532
  50. Dobrin PB. Poststenotic dilatation. Surg Gynaecol Obstet. 1991;172:503–508
  51. Dobrin PB. Animal models of aneurysms. Ann Vasc Surg. 1999;13:641–648
  52. Allaire E, Muscatelli-Groux B, Mandet C, Guinault AM, Bruneval P, Desgranges P, et al. Paracrine effect of vascular smooth muscle cells in the prevention of aortic aneurysm formation. J Vasc Surg. 2002;36:1018–1026
  53. Allaire E, Hasenstab D, Kenagy RD, Starcher B, Clowes MM, Clowes AW. Prevention of aneurysm development and rupture by local overexpression of plasminogen activator inhibitor-1. Circulation. 1998;98:249–255
  54. Allaire E, Mandet C, Bruneval P, Bensenane S, Becquemin JP, Michel JB. Cell and extracellular matrix rejection in arterial concordant and discordant xenografts in the rat. Transplantation. 1996;62:794–803
  55. Allaire E, Forough R, Clowes M, Starcher B, Clowes AW. Local overexpression of TIMP-1 prevents aortic aneurysm degeneration and rupture in a rat model. J Clin Invest. 1998;102:1413–1420
  56. Zhang J, Schmidt J, Ryschich E, Schumacher H, Allenberg JR. Increased apoptosis and decreased density of medial smooth muscle cells in human abdominal aortic aneurysms. Chin Med J (Engl). 2003;116:1549–1552
  57. Ross R, Klebanoff SJ. The smooth muscle cell: I. In vivo synthesis of connective tissue proteins. J Cell Biol. 1971;40:159–171
  58. Cohen JR, Sarfati I, Danna D, Wise L. Smooth muscle cell elastase, atherosclerosis, and abdominal aortic aneurysms. Ann Surg. 1992;216:327–330
  59. Patel MI, Melrose J, Ghosh P, Appleberg M. Increased synthesis of matrix metalloproteinases by aortic smooth muscle cells is implicated in the etiopathogenesis of abdominal aortic aneurysms. J Vasc Surg. 1996;24:82–92
  60. Powell JT, Greenhalgh RM. Cellular, enzymatic and genetic factors in the pathogenesis of abdominal aortic aneurysms. J Vasc Surg. 1989;9:297–304
  61. Thompson RW, Geraghty PJ, Lee JK. Abdominal aortic aneurysms: basic mechanisms and clinical implications. Curr Probl Surg. 2002;39:110–230
  62. Blumenthal HT, Lansing AI, Wheeler PA. Calcification of the media of the human aorta and its relation to intimal arteriosclerosis, ageing and disease. Am J Pathol. 1944;20:665–687
  63. Economou SG, Taylor CB, Beattie EJ, Davis CB. Persistent experimental aortic aneurysms in dogs. Surgery. 1960;47:21–28
  64. Nabseth DC, Martin DE, Rowe MI, Gotlieb LS, Deterling RA. Enzymatic destruction of aortic elastic tissue and possible relationship to experimental atherosclerosis. J Cardiovasc Surg (Torino). 1963;4:11–17
  65. Anidjar S, Salzmann JL, Gentric D, Lagneau P, Camilleri JP, Michel JB. Elastase-induced experimental aneurysms in rats. Circulation. 1990;82:973–978
  66. Azuma J, Asagami T, Dalman R, Tsao PS. Creation of murine experimental abdominal aortic aneurysms with elastase. J Vis Exp. 2009;23:1280
  67. Yamaguchi T, Yokokawa M, Suzuki M, Higashide S, et al. Morphologic changes in the aorta during elastase infusion in the rat aneurysm model. J Surg Res. 2001;95:161–166
  68. Halpern VJ, Nackman GB, Gandhi RH, Irizany E, et al. The elastase infusion model of experimental aortic aneurysms: synchrony of induction of endogenous proteinases with matrix destruction and inflammatory cell response. J Vasc Surg. 1994;20:51–60
  69. Pyo R, Lee JK, Shipley M, Curci JA, Mao D, Ziporin SJ, et al. Targeted gene disruption of matrix metalloproteinase-9 (gelatinase B) suppresses development of experimental abdominal aortic aneurysms. J Clin Invest. 2000;105:1641–1649
  70. Yamaguchi T, Yamaguchi T, Suzuki M, Higashide S, et al. The time course of elastin fiber degeneration in a rat aneurysm model. Surg Today. 2000;30:727–731
  71. Ponseti IVBW, Baird WA. Scoliosis and dissecting aneurysm of the aorta in rats fed with Lathyrus odoratus seeds. Am J Pathol. 1952;28:1059–1077
  72. Yu SY, Blumenthal HT. The calcification of elastic fiber: Part 4. Epinephrine and beta-aminopropionitrile-induced calcification in animal aortas. Atherosclerosis. 1965;5:159–173
  73. Gertz SD, Kurgan A, Eisenberg D. Aneurysm of the rabbit common carotid artery induced by periarterial application of calcium chloride in vivo. J Clin Invest. 1988;81:649–656
  74. Freestone T, Turner RJ, Higman DJ, Lever MJ, Powell JT. Influence of hypercholesterolemia and adventitial inflammation on the development of aortic aneurysm in rabbits. Arterioscler Thromb Vasc Biol. 1997;17:10–17
  75. Daugherty A. Mouse models of atherosclerosis. Am J Med Sci. 2002;323:3–10
  76. Daugherty A, Manning MW, Cassis LA. Antagonism of AT2 receptors augments Angiotensin II-induced abdominal aortic aneurysms and atherosclerosis. Br J Pharmacol. 2001;134:865–870
  77. Tangirala RK, Rubin EM, Palinski W. Quantitation of atherosclerosis in murine models: correlation between lesions in the aortic origin and in the entire aorta, and differences in the extent of lesions between sexes in LDL receptor-deficient and apolipoprotein E-deficient mice. J Lipid Res. 1995;36:2320–2328
  78. Yoshimura K, Aoki H, Ikeda Y, Furutani A, Hamano K, Matsuzaki M. Development of pharmacological therapy for abdominal aortic aneurysms based on animal studies. In:  Sakalihasan N,  Kuivaniemi H,  Michel JB editor. Aortic aneurysms — new insights into an old problem. Liege, Belgium: Les Editions de l'Universite de Liege; 2008;
  79. Inoue N, Muramatsu M, Jin D, Takai T, Katayama H, Kitaura Y, et al. Involvement of vascular angiotensin II-forming enzymes in the progression of aortic abdominal aneurysms in angiotensin II-infused ApoE-deficient mice. J Atheroscler Thromb. 2009;16:164–171
  80. Cassis LA, Gupte M, Thayer S, Zhang X, Charnigo R, Howatt DA, et al. Angiotensin II infusion promotes abdominal aortic aneurysms independent of increased blood pressure in hypercholesterolemic mice. Am J Physiol Heart Circ Physiol. 2009;296:H1660–H1665
  81. Qin Z. Newly developed angiotensin II-infused experimental models in vascular biology. Regul Pept. 2008;150:1–6
  82. Carrell TWG, Smith A, Burnand KG. Experimental techniques and models in the study of the development and treatment of abdominal aortic aneurysm. Br J Surg. 1999;86:305–312
  83. Borioni R, Garofalo M, De Paulis R, Nardi P, Scaffa R, Chiariello L. Abdominal aortic dissections anatomic and clinical features and therapeutic options. Tex Heart Inst J. 2005;32:70–73
  84. Saraff K, Babamusta F, Cassis LA, Daugherty A. Aortic dissection precedes formation of aneurysms and atherosclerosis in angiotensin II-infused, apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2003;23:1621–1626
  85. Manning MW, Cassi LA, Huang J, Szilvassy SJ, Daugherty A. Abdominal aortic aneurysms: fresh insights from a novel animal model of the disease. Vasc Med. 2002;1:45–54
  86. Aziz F, Kuivaniemi H. Role of matrix metalloproteinase inhibitors in preventing abdominal aortic aneurysm. Ann Vasc Surg. 2007;21:392–401
  87. Silence J, Collen D, Lijen HR. Reduced atherosclerotic plaque but enhanced aneurysm formation in mice with inactivation of the tissue inhibitor of metalloproteinase-1 (TIMP-1) gene. Circ Res. 2002;90:897–903
  88. Ahluwalia N, Lin AY, Tager AM, Pruitt IE, Anderson TJ, Kristo F, et al. Inhibited aortic aneurysm formation in BLT1-deficient mice. J Immunol. 2007;179:691–697
  89. Sanchez-Galan E, Gomez-Hernandez A, Vidal C, Martin-Ventura JL, Blanco-Colio LM, Munoz-Garcia B, et al. Leukotriene B4 enhances the activity of nuclear factor-kappaB pathway through BLT1 and BLT2 receptors in atherosclerosis. Cardiovasc Res. 2009;81:216–225
  90. Zhou YJ, Wang JH, Li L, Yang HW, Wen de L, He QC. Expanding expression of the 5-lipoxygenase/leukotriene B4 pathway in atherosclerotic lesions of diabetic patients promotes plaque instability. Biochem Biophys Res Commun. 2007;363:30–36
  91. Sun J, Sukhova GK, Yang M, Wolters PJ, MacFarlane LA, Libby P, et al. Mast cells modulate the pathogenesis of elastase-induced abdominal aortic aneurysms in mice. J Clin Invest. 2007;117:3359–3368
  92. Tsuruda T, Kato J, Hatakeyama K, Kojima K, Mitsuhiro , Yano Y, et al. Adventitial mast cells contribute to pathogenesis in the progression of abdominal aortic aneurysm. Circ Res. 2008;102:1368–1377
  93. Pereira L, Andrikopopulos K, Tian J, Lee SY, Keene DR, Ono R, et al. Targetting of the gene encoding fibrillin-1 recapitulates the vascular aspect of Marfan syndrome. Nat Genet. 1997;17:218–222
  94. Ammash NM, Sundt TM, Connolly HM. Marfan syndrome — Diagnosis and management. Curr Probl Cardiol. 2008;33:7–39
  95. Pereira L, Lee SY, Gayraud B, Andrikopopulos K, Shapiro SD, Bunton T, et al. Pathogenic sequence for aneurysm revealed in mice underexpressing fibrillin-1. PNAS. 1999;96:3819–3823
  96. Xiong W, Knispel RA, C; DH, F; R, BB T. Doxycycline delays aneurysm rupture in a mouse model of Marfan syndrome. J Vas Surg. 2008;47:166–172
  97. Brophy PM, Tilson JE, Tilson MD. Propanolol delays the formation of aneurysms in the male blotchy mouse. J Surg Res. 1988;44:687–689
  98. Dietz HC, Pyeritz RE. Mutations in the human gene for fibrillin-1 (FBN1) in the Marfan syndrome and related disorders. Mol Hum Genet. 1995;4:1799–1809
  99. Andrews EJ, White W, Bullock LP. Spontaneous aortic aneurysms in blotchy mice. Am J Pathol. 1974;78:199–210
  100. Faca VM, Song KS, Wang H, Zhang Q, Krasnoselsky AL, Newcomb LF, et al. A mouse to human search for plasma proteome changes associated with pancreatic tumour development. PLOS Medicine. 2008;e123:5
  101. Cox B, Kotlyar M, Evangelou AI, Ignatchenko V, Ignatchenko A, Whiteley K, et al. Comparative systems biology of human and mouse as a tool to guide the modeling of human placental pathology. Mol Syst Biol. 2009;5:279
  102. Kruger M, Moser M, Ussar S, Thievessen I, Lubar CA, Forner F, et al. SILAC mouse for quantitative proteomics uncovers kindlin-3 as an essential factor for red blood cell function. Cell. 2008;134:353–364
  103. McClatchy DB, Dong MQ, Wu C, Venable JD, Yates JR. 15N Metabolic labeling of mammalian tissue with slow protein turnover. J Proteome Res. 2007;6:2005–2010
  104. Wu CC, MacCoss MJ, Howell KE, Matthews DE, Yates JR. Metabolic labeling of mammalian organisms with stable isotopes for quantitative proteomic analysis. Anal Chem. 2004;76:4951–4959
  105. Judge AD, Robbins M, Tavakoli I, Levi J, Hu L, Fronda A, et al. Confirming the RNAi-mediated mechanism of action of siRNA-based cancer therapeutics in mice. J Clin Invest. 2009;119:661–673
  106. Sadek M, Hynecek RL, Goldenberg S, Kent KC, Marin ML, Faries PL. Gene expression analysis of a porcine native abdominal aortic aneurysm model. Surgery. 2008;144:252–258
  107. Chun HJ, Ali ZA, Kojima Y, Kundu RK, Sheikh AY, Agrawal R, et al. Apelin signaling antagonizes Ang II effects in mouse models of atherosclerosis. J Clin Invest. 2008;118:3343–3354
  108. Golledge J, Norman PE. Pathophysiology of abdominal aortic aneurysm relevant to improvements in patients' management. Curr Opin Cardiol. 2009;24:532–538

 Financial support: This work was supported by funding from the National Health and Medical Research Council, Australia (project grant number 540405). Jonathan Golledge holds a Practitioner's Fellowship from the National Health and Medical Research Council, Australia (grant number 431503).

PII: S1054-8807(10)00002-5

doi: 10.1016/j.carpath.2010.01.001

Cardiovascular Pathology
Volume 20, Issue 2 , Pages 114-123 , March 2011

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