Elastin and collagen fibre microstructure of the human aorta in ageing and disease: a review

Aortic disease is a significant cause of death in developed countries. The most common forms of aortic disease are aneurysm, dissection, atherosclerotic occlusion and ageing-induced stiffening. The microstructure of the aortic tissue has been studied with great interest, because alteration of the quantity and/or architecture of the connective fibres (elastin and collagen) within the aortic wall, which directly imparts elasticity and strength, can lead to the mechanical and functional changes associated with these conditions. This review article summarizes the state of the art with respect to characterization of connective fibre microstructure in the wall of the human aorta in ageing and disease, with emphasis on the ascending thoracic aorta and abdominal aorta where the most common forms of aortic disease tend to occur.

[1]  C. L. Cesar,et al.  Elastic fibers and collagen distribution in human aorta , 2011, BiOS.

[2]  J. Powell,et al.  Mechanical properties of the aneurysmal aorta , 1992, The British journal of surgery.

[3]  N. Stergiopulos,et al.  Arterial remodeling in response to increased blood flow using a constituent-based model. , 2008, Journal of biomechanics.

[4]  S Glagov,et al.  Comparison of Abdominal and Thoracic Aortic Medial Structure in Mammals , 1969, Circulation research.

[5]  N. Stergiopulos,et al.  Effect of elastin degradation on carotid wall mechanics as assessed by a constituent-based biomechanical model. , 2007, American journal of physiology. Heart and circulatory physiology.

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

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

[8]  M. Tilson Histochemistry of aortic elastin in patients with nonspecific abdominal aortic aneurysmal disease. , 1988, Archives of surgery.

[9]  J. Uitto,et al.  Marfan syndrome. Demonstration of abnormal elastin in aorta. , 1982, The Journal of clinical investigation.

[10]  Michael F. McNeeley,et al.  Aortic dissection in osteogenesis imperfecta: case report and review of the literature , 2012, Emergency Radiology.

[11]  K. Sueishi,et al.  Alterations of elastic architecture in human aortic dissecting aneurysm. , 1990, Laboratory investigation; a journal of technical methods and pathology.

[12]  A. Moragas,et al.  Mathematical morphologic analysis of the aortic medial structure. Biomechanical implications. , 1993, Analytical and quantitative cytology and histology.

[13]  Y. Soini,et al.  Increased amount of type III pN-collagen in human abdominal aortic aneurysms: evidence for impaired type III collagen fibrillogenesis. , 2000, Journal of vascular surgery.

[14]  B. Strauss,et al.  Vascular matrix remodeling in patients with bicuspid aortic valve malformations: implications for aortic dilatation. , 2003, The Journal of thoracic and cardiovascular surgery.

[15]  B. McManus,et al.  Localization of aortic disease is associated with intrinsic differences in aortic structure. , 1995, The Journal of surgical research.

[16]  S A Wickline,et al.  Decreased vascular smooth muscle cell density in medial degeneration of human abdominal aortic aneurysms. , 1997, The American journal of pathology.

[17]  S. Greenberg The association of medial collagenous tissue with atheroma formation in the aging human aorta as revealed by a special technique. , 1986, Histology and histopathology.

[18]  V. Duance,et al.  The distribution of collagen types I, III and V (AB) in normal and atherosclerotic human aorta , 1980, The Journal of pathology.

[19]  R. Béliveau,et al.  Differential regulation of matrix metalloproteinase activities in abdominal aortic aneurysms. , 2002, Journal of vascular surgery.

[20]  S. Takanashi,et al.  Efficacy and pitfalls of transapical cannulation for the repair of acute type A aortic dissection. , 2012, The Annals of thoracic surgery.

[21]  B T Baxter,et al.  Elastin is increased in abdominal aortic aneurysms. , 1994, The Journal of surgical research.

[22]  Z. Fayad,et al.  Associations between serum lipoprotein(a) levels and the severity of coronary and aortic atherosclerosis. , 2012, Atherosclerosis.

[23]  P. Hasleton,et al.  Collagen in dissecting aneurysms of the human thoracic aorta. Increased collagen content and decreased collagen concentration may be predisposing factors in dissecting aneurysms. , 1990, The American journal of cardiovascular pathology.

[24]  W. Hornebeck,et al.  Studies on elastic tissue of aorta in aortic dissections and Marfan syndrome. , 1981, Pathologie-biologie.

[25]  M. Faber,et al.  THE HUMAN AORTA , 2009 .

[26]  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.

[27]  R. Ogden,et al.  A New Constitutive Framework for Arterial Wall Mechanics and a Comparative Study of Material Models , 2000 .

[28]  M. Gacko,et al.  Metalloproteinases, insulin‐like growth factor‐I and its binding proteins in aortic aneurysm , 2004, International journal of experimental pathology.

[29]  L. Chu,et al.  Vascular complications of Ehlers-Danlos syndrome: CT findings. , 2012, AJR. American journal of roentgenology.

[30]  F Radice,et al.  Alteration of elastin, collagen and their cross-links in abdominal aortic aneurysms. , 2002, European journal of vascular and endovascular surgery : the official journal of the European Society for Vascular Surgery.

[31]  J. Michel,et al.  Collagen is reduced and disrupted in human aneurysms and dissections of ascending aorta. , 2008, Human pathology.

[32]  B. Baxter,et al.  Elastin content, cross-links, and mRNA in normal and aneurysmal human aorta. , 1992, Journal of vascular surgery.

[33]  F. Yamasawa,et al.  Age-Dependent Changes of Collagen and Elastin Content in Human Aorta and Pulmonary Artery , 1984, Angiology.

[34]  G. Holzapfel,et al.  Stress-driven collagen fiber remodeling in arterial walls , 2007 .

[35]  R. Eisenstein,et al.  Aortic lesion in Marfan syndrome: the ultrastructure of cystic medial degeneration. , 1977, Archives of pathology & laboratory medicine.

[36]  D. Paik,et al.  Neovascularization in the Abdominal Aortic Aneurysm , 1996 .

[37]  N. Kouchoukos,et al.  Sensitive detection of abnormal aortic architecture in Marfan syndrome with high-frequency ultrasonic tissue characterization. , 1995, Circulation.

[38]  P. Palatini Cardiovascular Effects of Exercise in Young Hypertensives , 2012, International Journal of Sports Medicine.

[39]  Gerhard Sommer,et al.  Layer-Specific 3D Residual Deformations of Human Aortas with Non-Atherosclerotic Intimal Thickening , 2007, Annals of Biomedical Engineering.

[40]  J. Uitto,et al.  Marfan's syndrome: structural, biochemical, and mechanical studies of the aortic media. , 1985, The Journal of laboratory and clinical medicine.

[41]  SE Greenwald,et al.  Ageing of the conduit arteries , 2007, The Journal of pathology.

[42]  R. Ogden,et al.  Hyperelastic modelling of arterial layers with distributed collagen fibre orientations , 2006, Journal of The Royal Society Interface.

[43]  J. Michel,et al.  The translational science of Marfan syndrome , 2011, Heart.

[44]  A. Luttun,et al.  Loss of Matrix Metalloproteinase-9 or Matrix Metalloproteinase-12 Protects Apolipoprotein E–Deficient Mice Against Atherosclerotic Media Destruction but Differentially Affects Plaque Growth , 2004, Circulation.

[45]  Jeffrey A. Jones,et al.  Aortic dilatation with bicuspid aortic valves: cusp fusion correlates to matrix metalloproteinases and inhibitors. , 2012, The Annals of thoracic surgery.

[46]  E. Lakatta,et al.  Altered Regulation of Matrix Metalloproteinase-2 in Aortic Remodeling During Aging , 2002, Hypertension.

[47]  A. Della Corte,et al.  Different patterns of extracellular matrix protein expression in the convexity and the concavity of the dilated aorta with bicuspid aortic valve: preliminary results. , 2005, The Journal of thoracic and cardiovascular surgery.

[48]  T. Toda,et al.  Morphometrical analysis of the aging process in human arteries and aorta. , 1980, Acta anatomica.

[49]  P. Hasleton,et al.  Biochemical investigation of possible lesions in human aorta that predispose to dissecting aneurysms: pyridinoline crosslinks. , 1987, Cardiovascular research.

[50]  A. Lansing,et al.  Calcium and elastin in human arteriosclerosis. , 1950, Journal of gerontology.

[51]  Jay D Humphrey,et al.  Growth and remodeling in a thick-walled artery model: effects of spatial variations in wall constituents , 2008, Biomechanics and modeling in mechanobiology.

[52]  B. Clausen Influence of age on connective tissue. Hexosamine and hydroxyproline in human aorta, myocardium, and skin. , 1962, Laboratory investigation; a journal of technical methods and pathology.

[53]  T Christian Gasser,et al.  Spatial orientation of collagen fibers in the abdominal aortic aneurysm's wall and its relation to wall mechanics. , 2012, Acta biomaterialia.

[54]  J. Strong,et al.  Atherosclerosis in young white males: arterial collagen and cholesterol. , 1993, Matrix.

[55]  P. Moreau,et al.  Evolution and modulation of age-related medial elastocalcinosis: impact on large artery stiffness and isolated systolic hypertension. , 2005, Cardiovascular research.

[56]  A. Comerota,et al.  Adventitial elastolysis is a primary event in aneurysm formation. , 1993, Journal of vascular surgery.

[57]  Stephen W. K. Cheng,et al.  Expression of integrin alpha5beta1 and the relationship to collagen and elastin content in human suprarenal and infrarenal aortas. , 2005, Vascular and endovascular surgery.

[58]  M. D. Tilson,et al.  Analysis of elastin cross-linking and the connective tissue matrix of abdominal aortic aneurysms. , 1994, Surgery.

[59]  A. Rachev,et al.  Theoretical study on the effects of pressure-induced remodeling on geometry and mechanical non-homogeneity of conduit arteries , 2011, Biomechanics and modeling in mechanobiology.

[60]  R. John,et al.  Chemical compositions of elastins isolated from aortas and pulmonary tissues of humans of different ages. , 1972, The Biochemical journal.

[61]  Hirst Ae,et al.  DISSECTING ANEURYSM OF THE AORTA: A REVIEW OF 505 CASES , 1958, Medicine.

[62]  K. Sobolewski,et al.  Collagen, elastin and glycosaminoglycans in aortic aneurysms. , 1995, Acta biochimica Polonica.

[63]  J. Schwarzbauer,et al.  Elastic Fibers: Building Bridges Between Cells and Their Matrix , 2002, Current Biology.

[64]  D. Simionescu,et al.  Involvement of matrix metalloproteinases and tenascin-C in elastin calcification. , 2004, Cardiovascular pathology : the official journal of the Society for Cardiovascular Pathology.

[65]  E. B. Smith THE INFLUENCE OF AGE AND ATHEROSCLEROSIS ON THE CHEMISTRY OF AORTIC INTIMA.2. COLLAGEN AND MUCOPOLYSACCHARIDES. , 1965, Journal of atherosclerosis research.

[66]  N. Stergiopulos,et al.  A Structure-Based Model of Arterial Remodeling in Response to Sustained Hypertension , 2009 .

[67]  S. Lyonnet,et al.  Vascular Wall Remodeling in Patients with Supravalvular Aortic Stenosis and Williams Beuren Syndrome , 2005, Journal of Vascular Research.

[68]  Plasma and tissue levels of collagen types I and III markers in patients with abdominal aortic aneurysms. , 2000, International angiology : a journal of the International Union of Angiology.

[69]  K. Murata,et al.  Collagen types in various layers of the human aorta and their changes with the atherosclerotic process. , 1986, Atherosclerosis.

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

[71]  A. Attili,et al.  Congenital bicuspid aortic valve first presenting as an aortic aneurysm. , 2012, The American journal of medicine.

[72]  J. Blankensteijn,et al.  Matrix metalloproteinase inhibition reduces intimal hyperplasia in a porcine arteriovenous-graft model. , 2004, Journal of vascular surgery.

[73]  K. Hamaoui,et al.  Massive spontaneous diaphragmatic rupture in Ehlers-Danlos syndrome. , 2012, Annals of the Royal College of Surgeons of England.

[74]  Juan-Pablo Maureira,et al.  Failure of Marfan anatomic criteria to predict risk of aortic dissection in Turner syndrome: necessity of specific adjusted risk thresholds. , 2012, Interactive cardiovascular and thoracic surgery.

[75]  M. Cho,et al.  Departments of Pathology and , 2022 .

[76]  G. Sterrantino,et al.  Aortic Connective Tissue in Ageing—A Biochemical Study , 1985, Angiology.

[77]  D. Paik,et al.  Neovascularization in the abdominal aortic aneurysm. Endothelial nitric oxide synthase, nitric oxide, and elastolysis. , 1996, Annals of the New York Academy of Sciences.

[78]  J. Uitto,et al.  DEMONSTRATION OF ABNORMAL ELASTIN IN AORTA , 1982 .

[79]  A. Avolio,et al.  Quantification of alterations in structure and function of elastin in the arterial media. , 1998, Hypertension.

[80]  G. Jondeau,et al.  Genetics of Thoracic Aortic Aneurysms , 2012, Current Atherosclerosis Reports.

[81]  G. Pals,et al.  Osteogenesis Imperfecta: A Review with Clinical Examples , 2011, Molecular Syndromology.

[82]  A. Leask Emerging targets for the treatment of scleroderma , 2012, Expert opinion on emerging drugs.

[83]  J. Powell,et al.  Elastin degradation in abdominal aortic aneurysms. , 1987, Atherosclerosis.

[84]  I. Tanboğa,et al.  Aortic elastic properties and left ventricular diastolic function in patients with isolated bicuspid aortic valve. , 2012, Journal of Heart Valve Disease.

[85]  N. Stergiopulos,et al.  Arterial remodeling in response to hypertension using a constituent-based model. , 2007, American journal of physiology. Heart and circulatory physiology.

[86]  Hasleton Ps,et al.  Increased elastin content and decreased elastin concentration may be predisposing factors in dissecting aneurysms of human thoracic aorta , 1993 .

[87]  Nikos Stergiopulos,et al.  Structural strain energy function applied to the ageing of the human aorta. , 2007, Journal of biomechanics.

[88]  P. Hasleton,et al.  Increased elastin content and decreased elastin concentration may be predisposing factors in dissecting aneurysms of human thoracic aorta. , 1993, Cardiovascular research.

[89]  R. Bank,et al.  Distinct defects in collagen microarchitecture underlie vessel-wall failure in advanced abdominal aneurysms and aneurysms in Marfan syndrome , 2009, Proceedings of the National Academy of Sciences.

[90]  R. Busuttil,et al.  Elastase activity: the role of elastase in aortic aneurysm formation. , 1982, The Journal of surgical research.

[91]  N. Stergiopulos,et al.  A constituent-based model of age-related changes in conduit arteries. , 2011, American journal of physiology. Heart and circulatory physiology.

[92]  Jay D Humphrey,et al.  A 2D constrained mixture model for arterial adaptations to large changes in flow, pressure and axial stretch. , 2005, Mathematical medicine and biology : a journal of the IMA.

[93]  Jay D. Humphrey,et al.  Time Courses of Growth and Remodeling of Porcine Aortic Media During Hypertension: A Quantitative Immunohistochemical Examination , 2008, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[94]  B. Voss,et al.  Localization of collagen types I, III, IV and V, fibronectin and laminin in human arteries by the indirect immunofluorescence method. , 1986, Pathology, research and practice.

[95]  X. Niu,et al.  Pioglitazone Attenuates Vascular Fibrosis in Spontaneously Hypertensive Rats , 2012, PPAR research.

[96]  N. Yokoyama,et al.  Prevalence and Predictors of Coexistent Silent Atherosclerotic Cardiovascular Disease in Patients With Abdominal Aortic Aneurysm Without Previous Symptomatic Cardiovascular Diseases , 2012, Angiology.

[97]  Stephen W. K. Cheng,et al.  Expression of Integrin •5•1 and the Relationship to Collagen and Elastin Content in Human Suprarenal and Infrarenal Aortas , 2005 .

[98]  Elspeth B. Smith,et al.  The influence of age and atherosclerosis on the chemistry of aortic intima , 1965 .

[99]  M. Spina,et al.  Age-related chemical changes in human elastins from non-atherosclerotic areas of thoracic aorta. , 1976, Atherosclerosis.

[100]  Peter Regitnig,et al.  Determination of the layer-specific distributed collagen fibre orientations in human thoracic and abdominal aortas and common iliac arteries , 2012, Journal of The Royal Society Interface.

[101]  U. Laufs,et al.  Aneurysms of the ascending aorta. , 2012, Deutsches Arzteblatt international.

[102]  R. Attaran,et al.  Ascending aortic aneurysm in a man with scleroderma , 2007, Clinical Rheumatology.

[103]  J. Cerveira,et al.  Reduced capacity to inhibit elastase in abdominal aortic aneurysm. , 1999, The Journal of surgical research.

[104]  G. Langewouters,et al.  The static elastic properties of 45 human thoracic and 20 abdominal aortas in vitro and the parameters of a new model. , 1984, Journal of biomechanics.

[105]  J. Humphrey,et al.  Biomechanics of the Porcine Basilar Artery in Hypertension , 2006, Annals of Biomedical Engineering.

[106]  M. Faber,et al.  The human aorta. V. Collagen and elastin in the normal and hypertensive aorta. , 1952, Acta pathologica et microbiologica Scandinavica.

[107]  V. C. Myers,et al.  Some chemical changes in the human thoracic aorta accompanying the aging process. , 1946, Journal of gerontology.

[108]  H. Lai,et al.  Bilateral versus unilateral antegrade cerebral perfusion in arch reconstruction for aortic dissection. , 2012, The Annals of thoracic surgery.

[109]  N. Fukunaga,et al.  Dissecting aneurysm in a patient with autosomal dominant polycystic kidney disease. , 2012, Annals of thoracic and cardiovascular surgery : official journal of the Association of Thoracic and Cardiovascular Surgeons of Asia.

[110]  J. Dillon,et al.  The nitrite/elastin reaction: implications for in vivo degenerative effects. , 1997, Connective tissue research.

[111]  A. Becker,et al.  Histologic changes in the normal aging aorta: implications for dissecting aortic aneurysm. , 1977, The American journal of cardiology.

[112]  T. Savunen,et al.  Elastin and collagen in the aortic wall: changes in the Marfan syndrome and annuloaortic ectasia. , 1985, Experimental and molecular pathology.

[113]  Dimitrios P Sokolis,et al.  Biomechanical response of ascending thoracic aortic aneurysms: association with structural remodelling , 2012, Computer methods in biomechanics and biomedical engineering.

[114]  A. Della Corte,et al.  Spatial patterns of matrix protein expression in dilated ascending aorta with aortic regurgitation: congenital bicuspid valve versus Marfan's syndrome. , 2006, The Journal of heart valve disease.

[115]  H. Bouissou,et al.  Interstitial collagens and ageing in human aorta , 2004, Virchows Archiv A.

[116]  F L Wuyts,et al.  Elastic properties of human aortas in relation to age and atherosclerosis: a structural model. , 1995, Physics in medicine and biology.

[117]  L. Kuller,et al.  Aortic stiffness and calcification in men in a population-based international study. , 2012, Atherosclerosis.

[118]  H. Sariola,et al.  Histological pattern and changes in extracellular matrix in aortic dissections. , 1986, Journal of clinical pathology.

[119]  E. M. Pedersen,et al.  Dilation of the ascending aorta in Turner syndrome - a prospective cardiovascular magnetic resonance study , 2011, Journal of cardiovascular magnetic resonance : official journal of the Society for Cardiovascular Magnetic Resonance.

[120]  D. Keller Caution regarding testosterone therapy. , 2012, The American journal of medicine.

[121]  T. Guy,et al.  Surgical treatment of ischemic mitral regurgitation might not influence ventricular remodeling. , 2005, The Journal of thoracic and cardiovascular surgery.

[122]  D. Mendrinos,et al.  Hypertension in the elderly. , 2012, World journal of cardiology.

[123]  L Guize,et al.  Pulse pressure: a predictor of long-term cardiovascular mortality in a French male population. , 1997, Hypertension.

[124]  Kozaburo Hayashi,et al.  A strain energy function for arteries accounting for wall composition and structure. , 2004, Journal of biomechanics.

[125]  J. S. Yao,et al.  Collagen types and matrix protein content in human abdominal aortic aneurysms. , 1989, Journal of vascular surgery.

[126]  E. Kanabrocki,et al.  Calcium, cholesterol, and collagen levels in human aortas. , 1960, Journal of gerontology.

[127]  D. Fujimoto Aging and cross-linking in human aorta. , 1982, Biochemical and biophysical research communications.

[128]  Y. Hosoda,et al.  Elastin Content of the Aorta and the Pulmonary Artery in the Japanese , 1965, Angiology.

[129]  Z. Fayad,et al.  The LDL-cholesterol to HDL-cholesterol ratio and the severity of coronary and aortic atherosclerosis. , 2012, Atherosclerosis.

[130]  T. Ohishi,et al.  Quantitation of the crosslinks, pyridinoline, deoxypyridinoline and pentosidine, in human aorta with dystrophic calcification. , 1995, Atherosclerosis.

[131]  Salvatore Pasta,et al.  Effect of aneurysm on the mechanical dissection properties of the human ascending thoracic aorta. , 2012, The Journal of thoracic and cardiovascular surgery.

[132]  J. Coselli,et al.  Decreased expression of fibulin-5 correlates with reduced elastin in thoracic aortic dissection. , 2005, Surgery.

[133]  E. Nanba,et al.  Relationships between matrix metalloproteinases and tissue inhibitor of metalloproteinases in the wall of abdominal aortic aneurysms. , 2003, International angiology : a journal of the International Union of Angiology.

[134]  Bradley S. Fleenor,et al.  Sodium nitrite de-stiffening of large elastic arteries with aging: Role of normalization of advanced glycation end-products , 2012, Experimental Gerontology.

[135]  G. London,et al.  Arterial stiffness: pathophysiology and clinical impact. , 2004, Clinical and experimental hypertension.

[136]  K. Sueishi,et al.  Dissecting aneurysm: a clinicopathologic and histopathologic study of 111 autopsied cases. , 1990, Human pathology.

[137]  A. Khoynezhad,et al.  Current management of type B aortic dissection , 2008, Vascular health and risk management.