Biomechanical determinants of abdominal aortic aneurysm rupture.

Rupture of abdominal aortic aneurysm (AAA) represents a significant clinical event, having a mortality rate of 90% and being currently ranked as the 13th leading cause of death in the US. The ability to reliably evaluate the susceptibility of a particular AAA to rupture on a case-specific basis could vastly improve the clinical management of these patients. Because AAA rupture represents a mechanical failure of the degenerated aortic wall, biomechanical considerations are important to understand this process and to improve our predictions of its occurrence. Presented here is an overview of research to date related to the biomechanics of AAA rupture. This includes a summary of results related to ex vivo and in vivo mechanical testing, noninvasive AAA wall stress estimations, and potential mechanisms of AAA wall weakening. We conclude with a demonstration of a biomechanics-based approach to predicting AAA rupture on a patient-specific basis, which may ultimately prove to be superior to the widely and currently used maximum diameter criterion.

[1]  A J Hall,et al.  Aortic Wall Tension as a Predictive Factor for Abdominal Aortic Aneurysm Rupture: Improving the Selection of Patients for Abdominal Aortic Aneurysm Repair , 2000, Annals of vascular surgery.

[2]  J. Eidt,et al.  Abdominal Aortic Aneurysm Repair , 2001, Vascular surgery.

[3]  E. Mangiarua,et al.  Increased intraluminal pressure induces DNA synthesis and c-fos expression in perfused rat aorta. , 1996, Archives of physiology and biochemistry.

[4]  B. Baxter,et al.  Macrophage Products Inhibit Human Aortic Smooth Muscle Cell Proliferation and Alter 1α(I) Procollagen Expression , 1997, Annals of vascular surgery.

[5]  Simon C Watkins,et al.  Cellular content and permeability of intraluminal thrombus in abdominal aortic aneurysm. , 1997, Journal of vascular surgery.

[6]  M. Matsumoto,et al.  150-kD oxygen-regulated protein is expressed in human atherosclerotic plaques and allows mononuclear phagocytes to withstand cellular stress on exposure to hypoxia and modified low density lipoprotein. , 1996, The Journal of clinical investigation.

[7]  N. Hertzer.  Outcome assessment in vascular surgery--results mean everything. , 1995, Journal of vascular surgery.

[8]  M. Koussa,et al.  Embolization of type II endoleaks after aortic stent-graft implantation: technique and immediate results. , 2001, Journal of vascular surgery.

[9]  P. Cahill,et al.  Effect of Pulse Pressure on Vascular Smooth Muscle Cell Migration: The Role of Urokinase and Matrix Metalloproteinase , 1999, Thrombosis and Haemostasis.

[10]  D A Vorp,et al.  Wall Strength and Stiffness of Aneurysmal and Nonaneurysmal Abdominal Aorta , 1996, Annals of the New York Academy of Sciences.

[11]  S. George,et al.  Surgical preparative injury and neointima formation increase MMP-9 expression and MMP-2 activation in human saphenous vein. , 1997, Cardiovascular research.

[12]  C. Liapis,et al.  Matrix metalloproteinases: contribution to pathogenesis, diagnosis, surveillance and treatment of abdominal aortic aneurysms , 2004, Current medical research and opinion.

[13]  David A. Vorp,et al.  Effect of intraluminal thrombus thickness and bulge diameter on the oxygen diffusion in abdominal aortic aneurysm. , 1998, Journal of biomechanical engineering.

[14]  W. Pearce,et al.  Size matters: the relationship between MMP-9 expression and aortic diameter. , 1997, Circulation.

[15]  D. J. Patel,et al.  Static Anisotropic Elastic Properties of the Aorta in Living Dogs , 1969, Circulation research.

[16]  J. Berk,et al.  Hypoxia downregulates tropoelastin gene expression in rat lung fibroblasts by pretranslational mechanisms. , 1999, American journal of physiology. Lung cellular and molecular physiology.

[17]  E. C. Xu,et al.  Biomechanical regulation of human monocyte/macrophage molecular function. , 2000, The American journal of pathology.

[18]  M. R. Roach,et al.  The composition and mechanical properties of abdominal aortic aneurysms. , 1994, Journal of vascular surgery.

[19]  T Länne,et al.  Abdominal aortic aneurysm wall mechanics and their relation to risk of rupture. , 1999, European journal of vascular and endovascular surgery : the official journal of the European Society for Vascular Surgery.

[20]  W. Mower,et al.  Stress distributions in vascular aneurysms: factors affecting risk of aneurysm rupture. , 1993, The Journal of surgical research.

[21]  P. Harris,et al.  Realistic expectations for patients with stent-graft treatment of abdominal aortic aneurysms. Results of a European multicentre registry. , 1999, European journal of vascular and endovascular surgery : the official journal of the European Society for Vascular Surgery.

[22]  M. Thubrikar,et al.  Mechanical properties of abdominal aortic aneurysm wall , 2001, Journal of medical engineering & technology.

[23]  D A Vorp,et al.  Mechanical properties and microstructure of intraluminal thrombus from abdominal aortic aneurysm. , 2001, Journal of biomechanical engineering.

[24]  M. Webster,et al.  Wall stress distribution on three-dimensionally reconstructed models of human abdominal aortic aneurysm. , 2000, Journal of vascular surgery.

[25]  F. Veith,et al.  Endoleaks after endovascular graft treatment of aortic aneurysms: classification, risk factors, and outcome. , 1998, Journal of vascular surgery.

[26]  R G Stringfellow,et al.  The influence of aorta-aneurysm geometry upon stress in the aneurysm wall. , 1987, The Journal of surgical research.

[27]  Janet T Powell,et al.  Detection, management, and prospects for the medical treatment of small abdominal aortic aneurysms. , 2004, Arteriosclerosis, thrombosis, and vascular biology.

[28]  Per Eriksson,et al.  Influence of intraluminal thrombus on structural and cellular composition of abdominal aortic aneurysm wall. , 2003, Journal of vascular surgery.

[29]  D A Vorp,et al.  Association of intraluminal thrombus in abdominal aortic aneurysm with local hypoxia and wall weakening. , 2001, Journal of vascular surgery.

[30]  R. Green,et al.  An evaluation of new methods of expressing aortic aneurysm size: relationship to rupture. , 1992, Journal of vascular surgery.

[31]  H. Oral,et al.  Hemodynamic regulation of tumor necrosis factor-alpha gene and protein expression in adult feline myocardium. , 1997, Circulation research.

[32]  B. Baxter,et al.  Incidence and histologic characteristics of blebs in patients with abdominal aortic aneurysms. , 1996, Journal of vascular surgery.

[33]  Thoralf M. Sundt,et al.  Mechanical Properties of Dilated Human Ascending Aorta , 2002, Annals of Biomedical Engineering.

[34]  M J Fagan,et al.  A comparative study of aortic wall stress using finite element analysis for ruptured and non-ruptured abdominal aortic aneurysms. , 2004, European journal of vascular and endovascular surgery : the official journal of the European Society for Vascular Surgery.

[35]  Peter R Hoskins,et al.  The relationship between aortic wall distensibility and rupture of infrarenal abdominal aortic aneurysm. , 2003, Journal of vascular surgery.

[36]  M L Raghavan,et al.  Toward a biomechanical tool to evaluate rupture potential of abdominal aortic aneurysm: identification of a finite strain constitutive model and evaluation of its applicability. , 2000, Journal of biomechanics.

[37]  G. L’italien,et al.  Biaxial elastic properties of rat arteries in vivo: influence of vascular wall cells on anisotropy. , 1994, The American journal of physiology.

[38]  P. Hoskins,et al.  The relationship between abdominal aortic aneurysm wall compliance, maximum diameter and growth rate. , 1997, Cardiovascular surgery.

[39]  C. Levene,et al.  The effect of hypoxia on the synthesis of collagen and glycosaminoglycans by cultured pig aortic endothelium. , 1982, Atherosclerosis.

[40]  R Fumero,et al.  Biomechanical factors in abdominal aortic aneurysm rupture. , 1993, European journal of vascular surgery.

[41]  D. Brewster.  Presidential address: what would you do if it were your father? Reflections on endovascular abdominal aortic aneurysm repair. , 2001, Journal of vascular surgery.

[42]  P. Hoskins,et al.  The relationship between abdominal aortic aneurysm distensibility and serum markers of elastin and collagen metabolism. , 2001, European journal of vascular and endovascular surgery : the official journal of the European Society for Vascular Surgery.

[43]  P. Howard,et al.  Mechanical forces alter extracellular matrix synthesis by human periodontal ligament fibroblasts. , 2010, Journal of periodontal research.

[44]  S Glagov,et al.  Cyclic stretching stimulates synthesis of matrix components by arterial smooth muscle cells in vitro. , 2003, Science.

[45]  Heterogeneous, Variable Wall-Thickness Modeling of a Ruptured Abdominal Aortic Aneurysm , 2004 .

[46]  P B Dobrin,et al.  Pathophysiology and pathogenesis of aortic aneurysms. Current concepts. , 1989, The Surgical clinics of North America.

[47]  J. Powell,et al.  Mechanical properties of the aneurysmal aorta , 1993 .

[48]  E. Campbell,et al.  Hypoxic injury to human alveolar macrophages accelerates release of previously bound neutrophil elastase. Implications for lung connective tissue injury including pulmonary emphysema. , 1983, The American review of respiratory disease.

[49]  RAP Scott,et al.  The Multicentre Aneurysm Screening Study (MASS) into the effect of abdominal aortic aneurysm screening on mortality in men: a randomised controlled trial , 2002, The Lancet.

[50]  K. Pietilä,et al.  Effect of hypoxia on the synthesis of glycosaminoglycans and collagen by rabbit aortic smooth muscle cells in culture. , 1984, Atherosclerosis.

[51]  V. Bernhard,et al.  Aortic blebs: possible site of aneurysm rupture. , 1989, Journal of vascular surgery.

[52]  D. Vorp,et al.  Age-related differences in the biaxial biomechanical behavior of human abdominal aorta , 2002 .

[53]  M. Webster,et al.  Ex vivo biomechanical behavior of abdominal aortic aneurysm: Assessment using a new mathematical model , 1996, Annals of Biomedical Engineering.

[54]  F J Schoen,et al.  Circumferential stress and matrix metalloproteinase 1 in human coronary atherosclerosis. Implications for plaque rupture. , 1996, Arteriosclerosis, thrombosis, and vascular biology.

[55]  H. Itoh,et al.  Prostaglandin F(2alpha), cytokines and cyclic mechanical stretch augment matrix metalloproteinase-1 secretion from cultured human uterine cervical fibroblast cells. , 2002, Molecular human reproduction.

[56]  D E Strandness,et al.  Stress-strain characteristics and collagen-elastin content of abdominal aortic aneurysms. , 1970, Surgery, gynecology & obstetrics.

[57]  Michael S Sacks,et al.  A planar biaxial constitutive relation for the luminal layer of intra-luminal thrombus in abdominal aortic aneurysms. , 2006, Journal of biomechanics.

[58]  A. Banes,et al.  Modulation of endothelial cell phenotype by cyclic stretch: inhibition of collagen production. , 1990, The Journal of surgical research.

[59]  M. Davies,et al.  Atherosclerotic plaque caps are locally weakened when macrophages density is increased. , 1991, Atherosclerosis.

[60]  H. W. Weizsäcker,et al.  Biomechanical behavior of the arterial wall and its numerical characterization , 1998, Comput. Biol. Medicine.

[61]  David A. Vorp,et al.  In Vivo Three-Dimensional Surface Geometry of Abdominal Aortic Aneurysms , 1999, Annals of Biomedical Engineering.

[62]  R Fumero,et al.  Biomechanics of abdominal aortic aneurysm in the presence of endoluminal thrombus: experimental characterisation and structural static computational analysis. , 1998, European journal of vascular and endovascular surgery : the official journal of the European Society for Vascular Surgery.

[63]  M I Patel,et al.  Current views on the pathogenesis of abdominal aortic aneurysms. , 1995, Journal of the American College of Surgeons.

[64]  Elena S. Di Martino,et al.  Development and 3D Finite Element Implementation of a Multiaxial Constitutive Relation for Abdominal Aortic Aneurysms , 2004 .

[65]  T Länne,et al.  Abdominal aortic aneurysm: a general defect in the vasculature with focal manifestations in the abdominal aorta? , 1997, Journal of vascular surgery.

[66]  J D Humphrey,et al.  Influence of size, shape and properties on the mechanics of axisymmetric saccular aneurysms. , 1996, Journal of biomechanics.

[67]  Janet T. Powell,et al.  Mechanical properties of th aneurysmal aorta , 1992 .

[68]  M. Webster,et al.  Effect of intraluminal thrombus on wall stress in patient-specific models of abdominal aortic aneurysm. , 2002, Journal of vascular surgery.

[69]  Samuel E. Wilson,et al.  Immediate repair compared with surveillance of small abdominal aortic aneurysms. , 2002, The New England journal of medicine.

[70]  Y. Sasaguri,et al.  Ambient pressure stimulates immortalized human aortic endothelial cells to increase DNA synthesis and matrix metalloproteinase 1 (tissue collagenase) production , 2004, Virchows Archiv.

[71]  David A. Vorp,et al.  Mechanical wall stress in abdominal aortic aneurysm: influence of diameter and asymmetry. , 1998, Journal of vascular surgery.

[72]  S S Gambhir,et al.  Effect of intraluminal thrombus on abdominal aortic aneurysm wall stress. , 1997, Journal of vascular surgery.

[73]  C. Lewis,et al.  Hypoxia-induced gene expression in human macrophages: implications for ischemic tissues and hypoxia-regulated gene therapy. , 2003, The American journal of pathology.

[74]  R N Vaishnav,et al.  Incremental formulations in vascular mechanics. , 1984, Journal of biomechanical engineering.

[76]  D. Brewster,et al.  Autopsy Study of Unoperated Abdominal Aortic Aneurysms: The Case for Early Resection , 1977, Circulation.

[77]  J Swedenborg,et al.  Growth of thrombus may be a better predictor of rupture than diameter in patients with abdominal aortic aneurysms. , 2000, European journal of vascular and endovascular surgery : the official journal of the European Society for Vascular Surgery.

[78]  R. Budwig,et al.  The influence of shape on the stresses in model abdominal aortic aneurysms. , 1996, Journal of biomechanical engineering.

[79]  David A. Vorp,et al.  Gene Expression Is Altered in Perfused Arterial Segments Exposed to Cyclic Flexure Ex Vivo , 1999, Annals of Biomedical Engineering.

[80]  Mark F Fillinger,et al.  Prediction of rupture risk in abdominal aortic aneurysm during observation: wall stress versus diameter. , 2003, Journal of vascular surgery.

[81]  D Bergqvist,et al.  Incidence and Prevalence of Abdominal Aortic Aneurysms, Estimated by Necropsy Studies and Population Screening by Ultrasound a , 1996, Annals of the New York Academy of Sciences.

[82]  Mark F Fillinger,et al.  In vivo analysis of mechanical wall stress and abdominal aortic aneurysm rupture risk. , 2002, Journal of vascular surgery.

[83]  Michael S Sacks,et al.  Age dependency of the biaxial biomechanical behavior of human abdominal aorta. , 2004, Journal of biomechanical engineering.

[84]  David A. Vorp,et al.  Potential influence of intraluminal thrombus on abdominal aortic aneurysm as assessed by a new non-invasive method. , 1996, Cardiovascular surgery.

[85]  D. Vorp,et al.  The effects of aneurysm on the biaxial mechanical behavior of human abdominal aorta. , 2006, Journal of biomechanics.

[86]  J. Reilly,et al.  Possible key role for plasmin in the pathogenesis of abdominal aortic aneurysms. , 1994, Surgery.

[87]  S. Carr,et al.  Minimal incision aortic surgery. , 2001, Journal of vascular surgery.

[88]  N. Sakalihasan,et al.  Modifications of the extracellular matrix of aneurysmal abdominal aortas as a function of their size. , 1993, European journal of vascular surgery.

[89]  R. Mecham,et al.  Hypoxia-induced inhibition of tropoelastin synthesis by neonatal calf pulmonary artery smooth muscle cells. , 1991, American journal of respiratory cell and molecular biology.

[90]  T. Gatanaga,et al.  Hypoxia induces a human macrophage cell line to release tumor necrosis factor-alpha and its soluble receptors in vitro. , 1993, The Journal of surgical research.

[91]  Rodney A. White,et al.  Endoleak as a predictor of outcome after endovascular aneurysm repair: AneuRx multicenter clinical trial. , 2000, Journal of vascular surgery.

[92]  Robert A. Brown,et al.  Mechanical loading regulates protease production by fibroblasts in three‐dimensional collagen substrates , 2000, Wound repair and regeneration : official publication of the Wound Healing Society [and] the European Tissue Repair Society.

[93]  D. J. Patel,et al.  Nonlinear anisotropic viscoelastic properites of canine arterial segments. , 1977, Journal of biomechanics.

[94]  D Bergqvist,et al.  Literature review of surgical management of abdominal aortic aneurysm. , 2001, European journal of vascular and endovascular surgery : the official journal of the European Society for Vascular Surgery.

[95]  Y C Fung,et al.  The degree of nonlinearity and anisotropy of blood vessel elasticity. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[96]  D Bergqvist,et al.  Diameter and compliance in the male human abdominal aorta: influence of age and aortic aneurysm. , 1992, European journal of vascular surgery.