Advertisement

Translational Stroke Research

, Volume 5, Issue 2, pp 167–173 | Cite as

Cerebral Aneurysms: Formation, Progression, and Developmental Chronology

  • Nima EtminanEmail author
  • Bruce A. Buchholz
  • Rita Dreier
  • Peter Bruckner
  • James C. Torner
  • Hans-Jakob Steiger
  • Daniel Hänggi
  • R. Loch Macdonald
Original Article

Abstract

The prevalence of unruptured intracranial aneurysms (UIAs) in the general population is up to 3 %. Existing epidemiological data suggests that only a small fraction of UIAs progress towards rupture over the lifetime of an individual, but the surrogates for subsequent rupture and the natural history of UIAs are discussed very controversially at present. In case of rupture of an UIA, the case fatality is up to 50 %, which therefore continues to stimulate interest in the pathogenesis of cerebral aneurysm formation and progression. Actual data on the chronological development of cerebral aneurysm has been especially difficult to obtain and, until recently, the existing knowledge in this respect is mainly derived from animal or mathematical models or short-term observational studies. Here, we review the current data on cerebral aneurysm formation and progression as well as a novel approach to investigate the developmental chronology of cerebral aneurysms.

Keywords

Intracranial aneurysms Aneurysm progression Aneurysm formation Developmental chronology 

Notes

Acknowledgments

NE and RLM receive grant support from the Physicians Services Incorporated Foundation. RLM receives grant support from the Brain Aneurysm Foundation, Canadian Institutes of Health Research, and the Heart and Stroke Foundation of Ontario. RLM is a consultant for Actelion Pharmaceuticals and Chief Scientific Officer of Edge Therapeutics, Inc. NE, DH, and RLM are scientific advisors/officers for Edge Therapeutics, Inc.

Support was also provided by NIH/NIGMS 8P41GM103483. This work was performed in part under the auspices of the US Department of Energy by Lawrence Livermore National Laboratory under Contract DE-AC52-07NA27344.

Conflict of Interest

None.

References

  1. 1.
    Weir B. Unruptured intracranial aneurysms: a review. J Neurosurg. 2002;96:3–42.PubMedCrossRefGoogle Scholar
  2. 2.
    Vernooij MW, Ikram MA, Tanghe HL, Vincent AJ, Hofman A, Krestin GP, et al. Incidental findings on brain MRI in the general population. N Engl J Med. 2007;357:1821–8.PubMedCrossRefGoogle Scholar
  3. 3.
    Vlak MH, Algra A, Brandenburg R, Rinkel GJ. Prevalence of unruptured intracranial aneurysms, with emphasis on sex, age, comorbidity, country, and time period: a systematic review and meta-analysis. Lancet Neurol. 2011;10:626–36.PubMedCrossRefGoogle Scholar
  4. 4.
    Krischek B, Inoue I. The genetics of intracranial aneurysms. J Hum Genet. 2006;51:587–94.PubMedCrossRefGoogle Scholar
  5. 5.
    Morita A, Fujiwara S, Hashi K, Ohtsu H, Kirino T. Risk of rupture associated with intact cerebral aneurysms in the Japanese population: a systematic review of the literature from Japan. J Neurosurg. 2005;102:601–6.PubMedCrossRefGoogle Scholar
  6. 6.
    Morita A, Kirino T, Hashi K, Aoki N, Fukuhara S, Hashimoto N, et al. The natural course of unruptured cerebral aneurysms in a Japanese cohort. N Engl J Med. 2012;366:2474–82.PubMedCrossRefGoogle Scholar
  7. 7.
    Wiebers DO, Whisnant JP, Huston 3rd J, Meissner I, Brown Jr RD, Piepgras DG, et al. Unruptured intracranial aneurysms: natural history, clinical outcome, and risks of surgical and endovascular treatment. Lancet. 2003;362:103–10.PubMedCrossRefGoogle Scholar
  8. 8.
    Lasheras JC. The biomechanics of arterial aneurysms. Annu Rev Fluid Mech. 2007;39:293–319.CrossRefGoogle Scholar
  9. 9.
    Fang H. A comparison of blood vessels of the brain and peripheral blood vessels. In: Wright IS, Millikan CH, editors. Cerebrovascular diseases. New York: Grune and Stratton; 1958. p. 17–22.Google Scholar
  10. 10.
    Chatziprodromou I, Tricoli A, Poulikakos D, Ventikos Y. Hemodynamics and wall remodeling of a growing cerebral aneurysm: a computational model. J Biomech. 2007;40:412–26.PubMedCrossRefGoogle Scholar
  11. 11.
    Steiger HJ. Pathophysiology of development and rupture of cerebral aneurysms. Acta Neurochir Suppl. 1990;48:1–57.PubMedGoogle Scholar
  12. 12.
    Chang HS. Simulation of the natural history of cerebral aneurysms based on data from the international study of unruptured intracranial aneurysms. J Neurosurg. 2006;104:188–94.PubMedCrossRefGoogle Scholar
  13. 13.
    Chatziprodromou I, Poulikakos D, Ventikos Y. On the influence of variation in hemodynamic conditions on the generation and growth of cerebral aneurysms and atherogenesis: a computational model. J Biomech. 2007;40:3626–40.PubMedCrossRefGoogle Scholar
  14. 14.
    Watton PN, Ventikos Y, Holzapfel GA. Modeling the growth and stabilization of cerebral aneurysms. Math Med Biol J IMA. 2009;26:133–64.CrossRefGoogle Scholar
  15. 15.
    Aoki T, Kataoka H, Shimamura M, Nakagami H, Wakayama K, Moriwaki T, et al. Nf-kappaB is a key mediator of cerebral aneurysm formation. Circulation. 2007;116:2830–40.PubMedCrossRefGoogle Scholar
  16. 16.
    Chalouhi N, Points L, Pierce GL, Ballas Z, Jabbour P, Hasan D. Localized increase of chemokines in the lumen of human cerebral aneurysms. Stroke 2013Google Scholar
  17. 17.
    Kanematsu Y, Kanematsu M, Kurihara C, Tada Y, Tsou TL, van Rooijen N, et al. Critical roles of macrophages in the formation of intracranial aneurysm. Stroke. 2011;42:173–8.PubMedCentralPubMedCrossRefGoogle Scholar
  18. 18.
    Starke RM, Chalouhi N, Ali MS, Jabbour PM, Tjoumakaris SI, Gonzalez LF, et al. The role of oxidative stress in cerebral aneurysm formation and rupture. Curr Neurovasc Res. 2013;10:247–55.PubMedCentralPubMedCrossRefGoogle Scholar
  19. 19.
    Zhang HF, Zhao MG, Liang GB, Song ZQ, Li ZQ. Expression of pro-inflammatory cytokines and the risk of intracranial aneurysm. Inflammation 2013Google Scholar
  20. 20.
    Hasan D, Chalouhi N, Jabbour P, Hashimoto T. Macrophage imbalance (M1 vs. M2) and upregulation of mast cells in wall of ruptured human cerebral aneurysms: preliminary results. J Neuroinflammation. 2012;9:222.PubMedCentralPubMedCrossRefGoogle Scholar
  21. 21.
    Hoh BL, Hosaka K, Downes DP, Nowicki KW, Fernandez CE, Batich CD, et al. Monocyte chemotactic protein-1 promotes inflammatory vascular repair of murine carotid aneurysms via a macrophage inflammatory protein-1alpha and macrophage inflammatory protein-2-dependent pathway. Circulation. 2011;124:2243–52.PubMedCentralPubMedCrossRefGoogle Scholar
  22. 22.
    Frenzel T, Lee CZ, Kim H, Quinnine NJ, Hashimoto T, Lawton MT, et al. Feasibility of minocycline and doxycycline use as potential vasculostatic therapy for brain vascular malformations: pilot study of adverse events and tolerance. Cerebrovasc Dis. 2008;25:157–63.PubMedCentralPubMedCrossRefGoogle Scholar
  23. 23.
    Makino H, Tada Y, Wada K, Liang EI, Chang M, Mobashery S, et al. Pharmacological stabilization of intracranial aneurysms in mice: a feasibility study. Stroke. 2012;43:2450–6.PubMedCentralPubMedCrossRefGoogle Scholar
  24. 24.
    Hasan DM, Chalouhi N, Jabbour P, Dumont AS, Kung DK, Magnotta VA, et al. Evidence that acetylsalicylic acid attenuates inflammation in the walls of human cerebral aneurysms: preliminary results. J Am Heart Assoc. 2013;2:e000019.PubMedCentralPubMedCrossRefGoogle Scholar
  25. 25.
    Hasan DM, Mahaney KB, Brown Jr RD, Meissner I, Piepgras DG, Huston J, et al. Aspirin as a promising agent for decreasing incidence of cerebral aneurysm rupture. Stroke. 2011;42:3156–62.PubMedCentralPubMedCrossRefGoogle Scholar
  26. 26.
    Caranci F, Briganti F, Cirillo L, Leonardi M, Muto M. Epidemiology and genetics of intracranial aneurysms. European journal of radiology. 2013Google Scholar
  27. 27.
    Grobelny TJ. Brain aneurysms: Epidemiology, treatment options, and milestones of endovascular treatment evolution. Dis Mon DM. 2011;57:647–55.CrossRefGoogle Scholar
  28. 28.
    Krischek B, Tatagiba M. The influence of genetics on intracranial aneurysm formation and rupture: current knowledge and its possible impact on future treatment. Adv Tech Stand Neurosurg. 2008;33:131–47.PubMedCrossRefGoogle Scholar
  29. 29.
    Onda H, Kasuya H, Yoneyama T, Takakura K, Hori T, Takeda J, et al. Genome wide-linkage and haplotype-association studies map intracranial aneurysm to chromosome 7q11. Am J Hum Genet. 2001;69:804–19.PubMedCentralPubMedCrossRefGoogle Scholar
  30. 30.
    Ruigrok YM, Rinkel GJ. Genetics of intracranial aneurysms. Stroke. 2008;39:1049–55.PubMedCrossRefGoogle Scholar
  31. 31.
    Ruigrok YM, Rinkel GJ, Wijmenga C, Kasuya H, Tajima A, Takahashi T, et al. Association analysis of genes involved in the maintenance of the integrity of the extracellular matrix with intracranial aneurysms in a Japanese cohort. Cerebrovasc Dis. 2009;28:131–4.PubMedCrossRefGoogle Scholar
  32. 32.
    Kissela BM, Sauerbeck L, Woo D, Khoury J, Carrozzella J, Pancioli A, et al. Subarachnoid hemorrhage: a preventable disease with a heritable component. Stroke. 2002;33:1321–6.PubMedCrossRefGoogle Scholar
  33. 33.
    Schievink WI, Schaid DJ, Michels VV, Piepgras DG. Familial aneurysmal subarachnoid hemorrhage: a community-based study. J Neurosurg. 1995;83:426–9.PubMedCrossRefGoogle Scholar
  34. 34.
    Brown Jr RD, Huston J, Hornung R, Foroud T, Kallmes DF, Kleindorfer D, et al. Screening for brain aneurysm in the familial intracranial aneurysm study: frequency and predictors of lesion detection. J Neurosurg. 2008;108:1132–8.PubMedCrossRefGoogle Scholar
  35. 35.
    Aoki T, Kataoka H, Ishibashi R, Nozaki K, Morishita R, Hashimoto N. Reduced collagen biosynthesis is the hallmark of cerebral aneurysm: contribution of interleukin-1beta and nuclear factor-kappaB. Arterioscler Thromb Vasc Biol. 2009;29:1080–6.PubMedCrossRefGoogle Scholar
  36. 36.
    Juvela S, Poussa K, Porras M. Factors affecting formation and growth of intracranial aneurysms: a long-term follow-up study. Stroke. 2001;32:485–91.PubMedCrossRefGoogle Scholar
  37. 37.
    Koffijberg H, Buskens E, Algra A, Wermer MJ, Rinkel GJ. Growth rates of intracranial aneurysms: exploring constancy. J Neurosurg. 2008;109:176–85.PubMedCrossRefGoogle Scholar
  38. 38.
    Nuki Y, Tsou TL, Kurihara C, Kanematsu M, Kanematsu Y, Hashimoto T. Elastase-induced intracranial aneurysms in hypertensive mice. Hypertension. 2009;54:1337–44.PubMedCentralPubMedCrossRefGoogle Scholar
  39. 39.
    Sprengers ME, van Rooij WJ, Sluzewski M, Rinkel GJ, Velthuis BK, de Kort GA, et al. MR angiography follow-up 5 years after coiling: frequency of new aneurysms and enlargement of untreated aneurysms. AJNR Am J neuroradiol. 2009;30:303–7.PubMedCrossRefGoogle Scholar
  40. 40.
    Wermer MJ, van der Schaaf IC, Velthuis BK, Algra A, Buskens E, Rinkel GJ. Follow-up screening after subarachnoid haemorrhage: frequency and determinants of new aneurysms and enlargement of existing aneurysms. Brain J Neurol. 2005;128:2421–9.CrossRefGoogle Scholar
  41. 41.
    Juvela S, Porras M, Poussa K. Natural history of unruptured intracranial aneurysms: probability of and risk factors for aneurysm rupture. J Neurosurg. 2000;93:379–87.PubMedCrossRefGoogle Scholar
  42. 42.
    David CA, Vishteh AG, Spetzler RF, Lemole M, Lawton MT, Partovi S. Late angiographic follow-up review of surgically treated aneurysms. J Neurosurg. 1999;91:396–401.PubMedCrossRefGoogle Scholar
  43. 43.
    Ferns SP, Sprengers ME, van Rooij WJ, van den Berg R, Velthuis BK, de Kort GA, et al. De novo aneurysm formation and growth of untreated aneurysms: A 5-year MRA follow-up in a large cohort of patients with coiled aneurysms and review of the literature. Stroke. 2011;42:313–8.PubMedCrossRefGoogle Scholar
  44. 44.
    Tsutsumi K, Ueki K, Morita A, Usui M, Kirino T. Risk of aneurysm recurrence in patients with clipped cerebral aneurysms: results of long-term follow-up angiography. Stroke. 2001;32:1191–4.PubMedCrossRefGoogle Scholar
  45. 45.
    Etminan N, Dreier R, Buchholz BA, Bruckner P, Steiger HJ, Hanggi D, et al. Exploring the age of intracranial aneurysms using carbon birth dating: preliminary results. Stroke. 2013;44:799–802.PubMedCentralPubMedCrossRefGoogle Scholar
  46. 46.
    Vogel JS, Love AH. Quantitating isotopic molecular labels with accelerator mass spectrometry. Methods Enzymol. 2005;402:402–22.PubMedCrossRefGoogle Scholar
  47. 47.
    Vogel JS, Turteltaub KW, Finkel R, Nelson DE. Accelerator mass spectrometry. Anal Chem. 1995;67:353A–9.PubMedCrossRefGoogle Scholar
  48. 48.
    Stuiver M, Reimer PJ, Braziunas TF. High-precision radiocarbon age calibration for terrestrial and marine samples. Radiocarbon. 1998;40:1127–51.Google Scholar
  49. 49.
    Graven HD, Guilderson TP, Keeling RF. Observations of radiocarbon in CO2 at La Jolla, California, USA 1992–2007: analysis of the long-term trend. J Geophys Res-Atmos. 2012;117Google Scholar
  50. 50.
    Hua Q, Barbetti M. Review of tropospheric bomb C-14 data for carbon cycle modeling and age calibration purposes. Radiocarbon. 2004;46:1273–98.Google Scholar
  51. 51.
    Levin I, Hammer S, Kromer B, Meinhardt F. Radiocarbon observations in atmospheric CO2: determining fossil fuel CO2 over Europe using Jungfraujoch observations as background. Sci Total Environ. 2008;391:211–6.PubMedCrossRefGoogle Scholar
  52. 52.
    Levin I, Naegler T, Kromer B, Diehl M, Francey RJ, Gomez-Pelaez AJ, et al. Observations and modeling of the global distribution and long-term trend of atmospheric 14CO2. Tellus. 2010:26–46Google Scholar
  53. 53.
    Harkness DD. Further investigations of the transfer of bomb 14C to man. Nature. 1972;240:302–3.PubMedCrossRefGoogle Scholar
  54. 54.
    Harkness DD, Walton A. Carbon-14 in the biosphere and humans. Nature. 1969;223:1216–8.PubMedCrossRefGoogle Scholar
  55. 55.
    Libby WF, Berger R, Mead JF, Alexander GV, Ross JF. Replacement rates for human tissue from atmospheric radiocarbon. Science. 1964;146:1170–2.PubMedCrossRefGoogle Scholar
  56. 56.
    Lovell MA, Robertson JD, Buchholz BA, Xie C, Markesbery WR. Use of bomb pulse carbon-14 to age senile plaques and neurofibrillary tangles in Alzheimer's disease. Neurobiol Aging. 2002;23:179–86.PubMedCrossRefGoogle Scholar
  57. 57.
    Stewart DN, Lango J, Nambiar KP, Falso MJ, FitzGerald PG, Rocke DM, et al. Carbon turnover in the water-soluble protein of the adult human lens. Mol Vis. 2013;19:463–75.PubMedCentralPubMedGoogle Scholar
  58. 58.
    Arner P, Bernard S, Salehpour M, Possnert G, Liebl J, Steier P, et al. Dynamics of human adipose lipid turnover in health and metabolic disease. Nature. 2011;478:110–3.PubMedCentralPubMedCrossRefGoogle Scholar
  59. 59.
    Bergmann O, Bhardwaj RD, Bernard S, Zdunek S, Barnabe-Heider F, Walsh S, et al. Evidence for cardiomyocyte renewal in humans. Science. 2009;324:98–102.PubMedCentralPubMedCrossRefGoogle Scholar
  60. 60.
    Bergmann O, Liebl J, Bernard S, Alkass K, Yeung MS, Steier P, et al. The age of olfactory bulb neurons in humans. Neuron. 2012;74:634–9.PubMedCrossRefGoogle Scholar
  61. 61.
    Perl S, Kushner JA, Buchholz BA, Meeker AK, Stein GM, Hsieh M, et al. Significant human beta-cell turnover is limited to the first three decades of life as determined by in vivo thymidine analog incorporation and radiocarbon dating. J Clin Endocrin Metab. 2010;95:E234–9.CrossRefGoogle Scholar
  62. 62.
    Spalding KL, Arner E, Westermark PO, Bernard S, Buchholz BA, Bergmann O, et al. Dynamics of fat cell turnover in humans. Nature. 2008;453:783–7.PubMedCrossRefGoogle Scholar
  63. 63.
    Spalding KL, Bhardwaj RD, Buchholz BA, Druid H, Frisen J. Retrospective birth dating of cells in humans. Cell. 2005;122:133–43.PubMedCrossRefGoogle Scholar
  64. 64.
    Hagg S, Salehpour M, Noori P, Lundstrom J, Possnert G, Takolander R, et al. Carotid plaque age is a feature of plaque stability inversely related to levels of plasma insulin. PloS One. 2011;6:e18248.PubMedCentralPubMedCrossRefGoogle Scholar
  65. 65.
    Brown TA, Nelson DE, Vogel JS, Southon JR. Improved collagen extraction by modified Longin method. Radiocarbon. 1988;30:171–7.Google Scholar
  66. 66.
    Reimer PJ, Brown TA, Reimer RW. Discussion: reporting and calibration of post-bomb C-14 data. Radiocarbon. 2004;46:1299–304.Google Scholar
  67. 67.
    Bhardwaj RD, Curtis MA, Spalding KL, Buchholz BA, Fink D, Bjork-Eriksson T, et al. Neocortical neurogenesis in humans is restricted to development. Proc Natl Acad Sci U S A. 2006;103:12564–8.PubMedCentralPubMedCrossRefGoogle Scholar
  68. 68.
    Spalding KL, Bergmann O, Alkass K, Bernard S, Salehpour M, Huttner HB, et al. Dynamics of hippocampal neurogenesis in adult humans. Cell. 2013;153:1219–27.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Nima Etminan
    • 1
    Email author
  • Bruce A. Buchholz
    • 2
  • Rita Dreier
    • 3
  • Peter Bruckner
    • 3
  • James C. Torner
    • 4
  • Hans-Jakob Steiger
    • 1
  • Daniel Hänggi
    • 1
  • R. Loch Macdonald
    • 5
  1. 1.Department of Neurosurgery, Medical FacultyHeinrich-Heine-UniversityDusseldorfGermany
  2. 2.Center for Accelerator Mass Spectrometry, Lawrence Livermore National LaboratoryLivermoreUSA
  3. 3.Institute for Physiological Chemistry and PathobiochemistryWestfalian Wilhelms-UniversityMuensterGermany
  4. 4.Department of EpidemiologyUniversity of IowaIowa CityUSA
  5. 5.Division of Neurosurgery, St. Michael’s Hospital, Labatt Family Centre of Excellence in Brain Injury and Trauma Research, Keenan Research Centre of the Li Ka Shing Knowledge Institute of St. Michael’s Hospital, Department of SurgeryUniversity of TorontoTorontoCanada

Personalised recommendations