Skip to main content
SpringerLink
Log in

Structure, Mechanical Properties, and Mechanics of Intracranial Saccular Aneurysms

  • Published:
Journal of elasticity and the physical science of solids Aims and scope Submit manuscript

Abstract

Intracranial saccular aneurysms remain an enigma; it is not known why they form, why they enlarge, or why only some of them rupture. Nonetheless, there is general agreement that mechanics plays an essential role in each aspect of the natural history of these potentially deadly lesions. In this paper, we review recent findings that discount limit point instabilities under quasi-static increases in pressure and resonance under dynamic loading as possible mechanisms of enlargement of saccular aneurysms. Indeed, recent histopathological data suggest that aneurysms enlarge due to a stress-mediated process of growth and remodeling of collagen, the primary load-bearing constituent within the wall. We submit that advanced theoretical, experimental, and numerical studies of this process are essential to further progress in treating this class of pathologies. The purpose of this review is to provide background and direction that encourages elasticians to contribute to this important area of research.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. N. Akkas, Aneurysms as a biomechanical instability problem. In: F. Mosora (ed.), Biomechanical Transport Processes, Plenum Press (1990) pp. 303–311.

  2. G.D. Angelini, S.L. Passani, I.M. Breckenridge and A.C. Newby, Nature and pressure dependence of damage induced by distension of human saphenous vein coronary artery bypass grafts. Cardiovas. Res. 21 (1987) 902–907.

    Google Scholar 

  3. S. Asari and T. Ohmoto, Growth and rupture of unruptured cerebral aneurysms based on the intraoperative appearance. Acta Med. Okayama 48 (1994) 257–262.

    Google Scholar 

  4. J.I. Ausman, The New England Journal of Medicine report on unruptured intracranial aneurysms: A critique. Surg. Neurol. 51 (1999) 227–229.

    Article  Google Scholar 

  5. G.M. Austin, Biomathematical model of aneurysm of the Circle of Willis: The Duffing equation and some approximate solutions. Math. Biosci. 11 (1971) 163–172.

    Article  MATH  Google Scholar 

  6. G.M. Austin, W. Schievink and R. Williams, Controlled pressure-volume factors in the enlargement of intracranial saccular aneurysms. Neurosurg. 24 (1989) 722–730.

    Google Scholar 

  7. G.M. Austin, S. Fisher, D. Dickson, D. Anderson and S. Richardson, The significance of the extracellular matrix in intracranial aneurysms. Ann. Clin. Lab. Sci. 23 (1993) 97–105.

    Google Scholar 

  8. M.F. Beatty, Topics in finite elasticity: Hyperelasticity of rubber, elastomers, and biological tissues-with examples. Appl. Mech. Rev. 40 (1987) 1699–1734.

    Google Scholar 

  9. H.S. Bennett, The microscopical investigation of biological materials with polarized light. In: McClung's Handbook of Microscopical Technique, 3rd edn, Hafner Publishing Co., New York (1950).

    Google Scholar 

  10. P.J. Camarata, R.E. Latchaw, D.A. Rufenacht and R.C. Heros, State of the art in medicine: Intracranial aneurysms. Invest. Radiol. 28 (1993) 373–382.

    Google Scholar 

  11. G.J. Campbell and M.R. Roach, Fenestrations in the internal elastic lamina at bifurcations of the human cerebral arteries. Stroke 12 (1981) 489–495.

    Google Scholar 

  12. P.B. Canham and G.G. Ferguson, A mathematical model for the mechanics of saccular aneurysms Neurosurg. 17 (1985) 291–295.

    Google Scholar 

  13. P.B. Canham, H.M. Finlay, J.G. Dixon and S.Y. Tong, Aneurysmal fabric modelled by layered great circle trajectories of collagen. Acta Sterol. 11 (1992) 703–711.

    Google Scholar 

  14. P.B. Canham, H.M. Finlay and S.Y. Tong, Stereological analysis of the layered structure of human intracranial aneurysms. J. Microsc. 183 (1996) 170–180.

    Article  Google Scholar 

  15. P.B. Canham, H.M. Finlay, J.A. Kiernan and G.G. Ferguson, Layered structure of saccular aneurysms assessed by collagen birefringence. Neurol. Res. 21 (1999) 618–626.

    Google Scholar 

  16. A.M. Coll, J.F.D. Corral, S. Yazawa and M. Falcon, Intra-aneurysmal pressure differences in human saccular aneurysms. Neurol. 6 (1976) 93–96.

    Google Scholar 

  17. M.R. Crompton, The pathology of ruptured middle-cerebral aneurysms with special reference to differences between the sexes. Lancet 2 (1962) 421–425.

    Article  Google Scholar 

  18. M.R. Crompton, Mechanism of growth and rupture in cerebral berry aneurysms. Br. Med. J. 1 (1966) 1138–1142.

    Article  Google Scholar 

  19. J. Cronin, Biomathematical model of aneurysm of the Circle of Willis: A qualitative analysis of the differential equation of Austin. Math. Biosci. 16 (1973) 209–225.

    Article  MATH  MathSciNet  Google Scholar 

  20. S.M. de la Monte, G.W. Moore, M.A. Monk and G.M. Hutchins, Risk factors for development and rupture of intracranial berry aneurysms. Am. J. Med. 78 (1985) 957–964.

    Article  Google Scholar 

  21. C.J. Doillon, M.G. Dunn, E. Bender and F.H. Silver, Collagen fiber formation in repair tissue: Development of strength and toughness. Collagen Rel. Res. 5 (1985) 481–492.

    Google Scholar 

  22. J.H. Evans and J.C. Barbenel, Structure and mechanical properties of tendon related to function. Equine Vet. J. 7 (1974) 1–8.

    MATH  Google Scholar 

  23. G.G. Ferguson, Turbulence in human intracranial saccular aneurysms. J. Neurosurg. 33 (1970) 485–497.

    Google Scholar 

  24. G.G Ferguson, Physical factors in the initiation, growth, and rupture of human intracranial aneurysms. J. Neurosurg. 37 (1972) 666–677.

    Google Scholar 

  25. G.G. Ferguson, Direct measurement of mean and pulsatile blood pressure at operation in human intracranial saccular aneurysms. J. Neurosurg. 36 (1972) 560–563.

    Google Scholar 

  26. G.G. Ferguson, Intracranial arterial aneurysms-a surgical perspective. In: Handbook of Clinical Neurology 11(55) (1989), pp. 41–87.

    Google Scholar 

  27. H.M. Finlay, P. Whittaker and P.B. Canham, Collagen organization in the branching region of human brain arteries. Stroke 29 (1998) 1595–1601.

    Google Scholar 

  28. W.D. Forbus, On the origin of miliary aneurysms of the superficial cerebral arteries. Bull. Johns Hopkins Hosp. 47 (1930) 239–284.

    Google Scholar 

  29. G.N. Foutrakis, H. Yonas and R.J. Sclabassi, Finite element methods in the simulation and analysis of intracranial blood flow: Saccular aneurysm formation in curved and bifurcating arteries. Tech Rep 6, Univ of Pitt Comp Neurosci (1994).

  30. D.L. Fry, Acute vascular endothelial changes associated with increased blood velocity gradients. Circ. Res. 22 (1968) 165–167.

    Google Scholar 

  31. P. Gaetani, F. Tartara, F. Tancioni, R. Rodriguez y Baena, E. Casari, M. Alfano and V. Grazioli, Deficiency of total collagen content and of deoxypyridinoline in intracranial aneurysm walls. FEBS Letters 404 (1997) 303–306.

    Article  Google Scholar 

  32. G.H. Gibbons and V.J. Dzau, The emerging concept of vascular remodeling. Mech. of Disease 330(20) (1994) 1431–1438.

    Google Scholar 

  33. Y.P. Gobin, J.L. Counord, P. Flaud and J. Duffaux, In vitro study of hemodynamics in a giant saccular aneurysm model: Influence of flow dynamics in the parent vessel and effects of coil embolization. Interven. NeuroRadiol. 36 (1994) 530–536.

    Google Scholar 

  34. G.J. Hademenos, T. Massoud, D.J. Valentino, G. Duckwiler and F. Vinuela, A nonlinear mathematical model for the development and rupture of intracranial saccular aneurysms. Neurol. Res. 16 (1994) 376–384.

    Google Scholar 

  35. G.J. Hademenos, T.F. Massoud, F. Turjman and J.W. Sayre, Anatomical and morphological factors correlating with rupture of intracranial aneurysms in patients referred for endovascular treatment. Neuroradiol. 40 (1998) 755–760.

    Article  Google Scholar 

  36. A. Hara, N. Yoshimi and H. Mori, Evidence for apoptosis in human intracranial aneurysms. Neurol. Res. 20 (1998) 127–130.

    Google Scholar 

  37. T. Hasimoto, Dynamic measurement of pressure and flow velocities in glass and silastic model berry aneurysms. Neurol. Res. 6 (1984) 22–28.

    Google Scholar 

  38. N. Hashimoto and H. Handa, The size of cerebral aneurysms in relation to repeated rupture. Surg. Neurol. 19 (1983) 107–111.

    Article  Google Scholar 

  39. O. Hassler, Morphological studies on the large cerebral arteries, with reference to the aetiology of subarachnoid haemorrhage. Acta Psychiatr. Neurol. Scand. (suppl) 154 (1961) 1–145.

    Google Scholar 

  40. O. Hassler, The windows of the internal elastic lamella of the cerebral arteries. Virchows Arch. Path. Anat. 335 (1962) 127–132.

    Article  Google Scholar 

  41. K. Hegedus, Some observations on reticular fibers in the media of the major cerebral arteries. Surg. Neurol. 22 (1984) 301–307.

    Article  Google Scholar 

  42. F.P.K. Hsu, C. Schwab, D. Rigamonti and J.D. Humphrey, Identification of response functions for nonlinear membranes via axisymmetric inflation tests: Implications for biomechanics. Int. J. Sol. Struct. 31 (1994) 3375–3386.

    Article  MATH  Google Scholar 

  43. F.P.K. Hsu, A.M.C. Liu, J. Downs, D. Rigamonti and J.D. Humphrey, A triplane videobased experimental system for studying axisymmetrically inflated biomembranes, IEEE Trans. Biomed. Engr. 42 (1995) 442–450.

    Article  Google Scholar 

  44. J.D. Humphrey, R.K. Strumpf and F.C.P. Yin, A constitutive theory for biomembranes: Application to epicardium. ASME J. Biomech. Engr. 114 (1992) 461–466.

    Google Scholar 

  45. J.D. Humphrey, Arterial wall mechanics: Review and directions. Crit. Rev. Biomed. Engr. 23(1/2) (1995) 1–162.

    Google Scholar 

  46. J.D. Humphrey and S.K. Kyriacou, The use of Laplace's equation in aneurysm mechanics. Neurol. Res. 18 (1996) 204–208.

    Google Scholar 

  47. J.D. Humphrey, Computer methods in membrane biomechanics. Comp. Meth. Biomech. Biomed. Engr. 1 (1998) 171–210.

    Google Scholar 

  48. J.D. Humphrey, Remodeling of a collagenous tissue at fixed lengths. ASME J. Biomech. Engr. 121 (1999) 591–597.

    Google Scholar 

  49. E.J.N. Hung and M.R. Botwin, Mechanics of rupture of cerebral saccular aneurysms. J. Biomech. 8 (1975) 385–392.

    Article  Google Scholar 

  50. K.K. Jain, Mechanism of rupture of intracranial saccular aneurysms. Surg. (1963) 347–350.

  51. H. Kamitani, H. Masuzawa, I. Kanazawa and T. Kubo, Bleeding risk in unruptured and residual cerebral aneurysms-angiographic annual growth rate in nineteen patients. Acta Neurochir. (Wein) 141 (1999) 153–159.

    Article  Google Scholar 

  52. N.F. Kassel and J.C. Torner, Size of intracranial aneurysms. Neurosurg. 12 (1983) 291–297.

    Article  Google Scholar 

  53. C. Kim, J. Cervos-Navarro, H. Kikuchi, N. Hashimoto and F. Hazama, Alterations in cerebral vessels in experimental animals and their possible relationship to the development of aneurysms. Surg. Neurol. 38 (1992) 331–337.

    Article  Google Scholar 

  54. M. Kojima, H. Handa, N. Hashimoto, C. Kim and F. Hazima, Early changes of experimentally induced cerebral aneurysms in rats: Scanning electron microscopy study. Stroke 17 (1986) 835–841.

    Google Scholar 

  55. T.M. Kosierkiewicz, S.M. Factor and D.W. Dickson, Immunocytochemical studies of atherosclerotic lesions of cerebral berry aneurysms. J. Neuropath. Exp. Neurol. 53 (1994) 399–406.

    Google Scholar 

  56. H. Kraus, Thin Elastic Shells, J. Wiley, New York (1967).

    MATH  Google Scholar 

  57. S.K. Kyriacou and J.D. Humphrey, Influence of size, shape and properties on the mechanics of axisymmetric saccular aneurysms. J. Biomech. 29 (1996) 1015–1022. Erratum 30 (1997) 761.

    Article  Google Scholar 

  58. S.K. Kyriacou, C. Schwab and J.D. Humphrey, Finite element analysis of nonlinear orthotropic hyperelastic membranes. Comp. Mech. 18 (1996) 269–278.

    MATH  ADS  Google Scholar 

  59. S.K. Kyriacou, A. Shah and J.D. Humphrey, Inverse finite element characterization of nonlinear hyperelastic membranes. J. Appl. Mech. 64 (1997) 257–262.

    MATH  Google Scholar 

  60. E.R. Lang and M. Kidd, Electron microscopy of human cerebral aneurysms. J. Neurosurg. 22 (1965) 554–562.

    Google Scholar 

  61. B.L. Langille, Remodeling of developing and mature arteries: Endothelium, smooth muscle, and matrix. J. Cardiovasc. Pharmacol. 21 (1993) S11-S17.

    Google Scholar 

  62. Y. Lanir, Constitutive equations for fibrous connective tissues. J. Biomechanics 16 (1983) 1–12.

    Article  ADS  Google Scholar 

  63. J.M. Lee and D.R. Boughner, Tissue mechanics of canine pericardium in different test environments. Evidence for time-dependent accommodation, absence of placticity, and new roles for collagen and elastin. Circ. Res. 49 (1981) 533–544.

    Google Scholar 

  64. K.O. Lim and D.R. Boughner, Low frequency dynamic viscoelastic properties of human mitral valve tissue. Cardiovasc. Res. 10 (1976) 459–465.

    Article  Google Scholar 

  65. M. Low, K. Perktold and R. Raunig, Hemodynamics in rigid and distensible saccular aneurysms: A numerical study of pulsatile flow characteristics. Biorheol. 30 (1993) 287–298.

    Google Scholar 

  66. D.J. MacDonald, H.M. Finlay and P.B. Canham, Directional wall strength in saccular brain aneurysms from polarized light microscopy. Ann. Biomed. Eng. 28 (2000) 533–542.

    Article  Google Scholar 

  67. F.B. Meyer, J. Huston and S.S. Riederer, Pulsatile increases in aneurysm size determined by cine phase-contrast MR angiography. J. Neurosurg. 78 (1993) 879–883.

    Google Scholar 

  68. W.R. Milnor, Hemodynamics, Williams and Wilkens, Baltimore (1989).

    Google Scholar 

  69. C. Mimata, M. Kitaoka, S. Nagahiro, K. Iyama, H. Hori, H. Yoshioka and Y. Ushio, Differential distribution and expressions of collagens in the cerebral aneurysmal wall. Acta Neuropathol. 94 (1997) 197–206.

    Article  Google Scholar 

  70. G. Neil-Dwyer, J.R. Bartlett, A.C. Nicholls, P. Narcisi and F.M. Pope, Collagen deficiency and ruptured cerebral aneurysms. J. Neurosurg. 59 (1983) 16–20.

    Google Scholar 

  71. D.A. Nichols, F.B. Meyer, D.G. Piepgras and P.L. Smith, Endovascular treatment of intracranial aneurysms. Mayo Clinic Proceedings 69 (1994) 272–285.

    Google Scholar 

  72. S.H.M. Nyström, Development of intracranial aneurysms as revealed by electron microscopy. J. Neurosurg. 20 (1963) 329–337.

    Google Scholar 

  73. J.R. Ostergaard, Risk factors in intracranial saccular aneurysms. Acta. Neurol. Scand. 80 (1989) 81–98.

    Article  Google Scholar 

  74. J.R. Ostergaard, E. Reske-Nielsen and H. Oxlund, Histological and morphometric observations on the reticular fibers in the arterial beds of patients with ruptured intracranial saccular aneurysms. Neurosurg. 20 (1987) 554–558.

    Google Scholar 

  75. L. Parlea, R. Fahrig, D.W. Holdsworth and S.P. Lownie, An analysis of the geometry of saccular intracranial aneurysms. Am. J. Neuroradiol. 20 (1999) 1079–1089.

    Google Scholar 

  76. W.R. Phillips, Mineral Optics: Principles and Techniques, W.H. Freeman, San Francisco (1971), pp. 171–190.

    Google Scholar 

  77. C. Richardson and O. Kofman, Cranial bruit with intracranial saccular aneurysms. Trans. Am. Neurol. Assoc. 76 (1951) 151–154.

    Google Scholar 

  78. J.M. Ryan and J.D. Humphrey, Finite element based predictions of preferred material symmetries in saccular aneurysms. Ann. Biomed. Engr. 27 (1999) 641–647.

    Article  Google Scholar 

  79. A.L. Sahs, Observations on the pathology of saccular aneurysms. J. Neurosurg. 24 (1966) 792–806.

    Google Scholar 

  80. L.N. Sekhar and R.C. Heros, Origin, growth and rupture of saccular aneurysms: A review. Neurosurg. 8 (1981) 248–260.

    Google Scholar 

  81. L.N. Sekhar, R.P. Sclabassi, M. Sun, H.B. Blue and J.F. Wasserman, Intra-aneurysmal pressure measurements in experimental saccular aneurysms in dogs. Stroke 19 (1988) 353–356.

    Google Scholar 

  82. P. Seshaiyer, A.D. Shah, S.K. Kyriacou and J.D. Humphrey, Multiaxial mechanical behavior of human saccular aneurysms. Comp. Meth. Biomech. Biomed. Engr. 4 (2001) 281–290.

    Google Scholar 

  83. S. Scott, G.G. Ferguson and M.R. Roach, Comparison of the elastic properties of human intracranial arteries and aneurysms. Can. J. Physiol. and Pharmacol. 50 (1972) 328–332.

    Google Scholar 

  84. A.D. Shah, J.L. Harris, S.K. Kyriacou and J.D. Humphrey, Further roles of geometry and properties in saccular aneurysm mechanics. Comp. Meth. Biomech. Biomed. Engr. 1 (1997) 109–121.

    Google Scholar 

  85. A.D. Shah and J.D. Humphrey, Finite strain elastodynamics of saccular aneurysms. J. Biomech. 32 (1999) 593–599.

    Article  Google Scholar 

  86. T.E. Simkins and W.E. Stehbens, Vibrational behavior of arterial aneurysms. Lett. Appl. Engr. Sci. 1 (1973) 85–100.

    Google Scholar 

  87. J.H.F. Smith, P.B. Canham and J. Starkey, Orientation of collagen in the tunica adventitia of the human cerebral artery measured with polarized light and the universal stage. J. Ultrastruct. Res. 77 (1981) 133–145.

    Article  Google Scholar 

  88. J. Starkey, The analysis of three-dimensional orientation data. Can. J. Earth Sci. 30 (1993) 1355–1362.

    Google Scholar 

  89. W.E. Stehbens, Histopathology of cerebral aneurysms. Arch. Neurol. 8 (1963) 272–285.

    Google Scholar 

  90. W.E. Stehbens, Ultrastructure of aneurysms. Arch. Neurol. 32 (1975) 798–807.

    Google Scholar 

  91. W.E. Stehbens, The pathology of intracranial arterial aneurysms and their complications. In: J.L. Fox (ed.), Intracranial Aneurysms, Springer-Verlag, New York (1983).

    Google Scholar 

  92. W.E. Stehbens, Pathology and pathogenesis of intracranial berry aneurysms. Neurol. Res. 12 (1990) 29–34.

    Google Scholar 

  93. H.J. Steiger, R. Aaslid, S. Keller and H.J. Reulen, Strength, elasticity and viscoelastic properties of cerebral aneurysms. Heart Vessels 5 (1986) 41–46.

    Article  Google Scholar 

  94. H.J. Steiger, D.W. Liepsch, A. Poll and H.J. Reulen, Hemodynamic stress in terminal saccular aneurysms: A laser doppler study. Heart Vessels 4 (1988) 162–169.

    Article  Google Scholar 

  95. H.J. Steiger, Pathophysiology of development and rupture of cerebral aneurysms. Acta Neurochir. Suppl. 48 (1990) 1–57.

    ADS  Google Scholar 

  96. J. Suzuki and H. Ohara, Clinicopathological study of cerebral aneurysms. J. Neurosurg. 48 (1978) 505–514.

    Article  Google Scholar 

  97. M. Toth, G.L. Nadasy, I. Nyary, T. Kerenyi, M. Orosz, G. Molnarka and E. Monos, Sterically inhomogeneous viscoelastic behavior of human saccular cerebral aneurysms. J. Vasc. Res. 35 (1998) 345–355.

    Article  Google Scholar 

  98. H. Ujiie, K. Sato, H. Onda, A. Oikkawa, M. Kagawa, K. Atakakura and N. Kobayashi, Clinical analysis of incidentally discovered unruptured aneurysms. Stroke 24 (1993) 1850–1856.

    Google Scholar 

  99. H. Ujiie et al., Effects of size and shape (aspect ratio) on the hemodynamics of saccular aneurysms: A possible index for surgical treatment of intracranial aneurysms. Neurosurg. 45 (1999) 119–130.

    Article  Google Scholar 

  100. R. Vilarta and B.C. Vidal, Anisotropic and biomechanical properties of tendons modified by exercise and denervation: Aggregation and macromolecular order in collagen bundles. Matrix 9 (1989) 55–61.

    Google Scholar 

  101. S.A. Wainwright, W.D. Biggs, J.D. Currey and J.M. Gosline, Mechanical Design in Organisms, Princeton University Press (1976), pp. 88–93.

  102. D.O. Wiebers, J.P. Whisnant, T.M. Sundt and W.M. O'Fallon, The significance of unruptured intracranial aneurysms. J. Neurosurg. 66 (1987) 23–29.

    Article  Google Scholar 

  103. D.O. Wiebers et al., Unruptured in tracranial aneurysms-risk of rupture and risks of surgical intervention. International study of unruptured intracranial aneurysms investigators. N. Engl. J. Med. 339 (1998) 1725–1733.

    Article  Google Scholar 

  104. P. Whittaker, M.E. Schwab and P.B. Canham, The molecular organization of collagen in saccular aneurysms assessed by polarized light microscopy. Conn. Tiss. Res. 17 (1988) 43–54.

    Google Scholar 

  105. P. Whittaker, D.R. Boughner and R.A. Kloner, Role of collagen in acute myocardial infarct expansion. Circulation 84 (1991) 3123–3134.

    Google Scholar 

  106. M. Wolman and T.A. Gillman, A polarized light study of collagen in dermal wound healing. Br. J. Exp. Path. 53 (1972) 85–89.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Biomedical Engineering, Texas A&M University, College Station, TX, U.S.A.

    J.D. Humphrey

  2. Medical Biophysics, University of Western Ontario, London, Ontario, Canada

    P.B. Canham

Authors
  1. J.D. Humphrey
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P.B. Canham
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Humphrey, J., Canham, P. Structure, Mechanical Properties, and Mechanics of Intracranial Saccular Aneurysms. Journal of Elasticity 61, 49–81 (2000). https://doi.org/10.1023/A:1010989418250

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1010989418250

Search

Navigation