Advertisement

Clinical Neuroradiology

, Volume 29, Issue 2, pp 285–293 | Cite as

Hemodynamics of Focal Versus Global Growth of Small Cerebral Aneurysms

  • Paolo Machi
  • Rafik Ouared
  • Olivier Brina
  • Pierre Bouillot
  • Hasan Yilmaz
  • Maria I Vargas
  • Renato Gondar
  • Philippe Bijlenga
  • Karl O Lovblad
  • Zsolt KulcsárEmail author
Original Article

Abstract

Background and Purpose

Hemodynamics play a driving role in the life cycle of brain aneurysms from initiation through growth until eventual rupture. The specific factors behind aneurysm growth, especially in small aneurysms, are not well elucidated. The goal of this study was to differentiate focal versus general growth and to analyze the hemodynamic microenvironment at the sites of enlargement in small cerebral aneurysms.

Materials and Methods

Small aneurysms showing growth during follow-up were identified from our prospective aneurysm database. Three dimensional rotational angiography (3DRA) studies before and after morphology changes were available for all aneurysms included in the study, allowing for detailed shape and computational fluid dynamic (CFD) based hemodynamic analysis. Six patients fulfilled the inclusion criteria.

Results

Two different types of change were observed: focal growth, with bleb or blister formation in three, and global aneurysm enlargement accompanied by neck broadening in other three patients. Areas of focal growth showed low shear conditions with increased oscillations at the site of growth (a low wall shear stress [WSS] and high oscillatory shear index [OSI]). Global aneurysm enlargement was associated with increased WSS coupled with a high spatial wall shear stress gradient (WSSG).

Conclusion

For different aneurysm growth types, distinctive hemodynamic microenvironment may be responsible and temporal–spatial changes of the pathologic WSS would have the inciting effect. We suggest the distinction of focal and global growth types in future hemodynamic and histological studies.

Keywords

Cerebral aneurysm Aneurysm growth Subarachnoid hemorrhage Computational flow Dynamics 

Abbreviations

3D

Three-dimensional

ICA

Internal carotid artery

MRA

Magnetic resonance angiography

CTA

Computed tomographic angiography

3DRA

Three-dimensional rotational angiography

WSS

Wall shear stress

WSSG

Wall shear stress gradient

OSI

Oscillatory shear index

GA

Growth area (of the aneurysm wall)

LVF

Low value fraction

HVF

High value fraction

DSA

Digital subtraction angiography

STL

STereoLithography

Notes

Funding

This study was supported by Swiss National Science Foundation grants (SNF 32003B_160222 and SNF 320030_156813).

Conflict of interest

P. Machi, R. Ouared, O. Brina, P. Bouillot, H. Yilmaz, M.I. Vargas, R. Gondar, P. Bijlenga, K.O. Lovblad and Z. Kulcsár declare that they have no competing interests.

Supplementary material

62_2017_640_MOESM1_ESM.docx (107 kb)
Materials and methods
62_2017_640_MOESM2_ESM.jpg (3.1 mb)
OSI, peak systolic WSSG (Pa/µm) and WSS (Pa) in aneurysms and growth areas for patients p2, p5, p6. Patient representation is row-like. Columns from left to right represent for each patient, the growth area, and the spatial frequency distribution of OSI, peak systolic WSSG and WSS, over the aneurysm (blue) and growth area (yellow), respectively. Medallions, cast the zoom on distributions in growth areas
62_2017_640_MOESM3_ESM.jpg (1.4 mb)
Columns B, D and F, show the histograms (spatial density distribution functions) of OSI, peak systolic WSSG (Pa/µm) and WSS (Pa) in aneurysms (blue) and growth areas (yellow) for patients p1, p3, p4. Medallions, cast the zoom on distributions in growth areas. Columns A, C and E represent the clusterization (in red) of OSI, peak systolic WSSG and WSS patterns in overall growth areas (green), respectively. Patient representation is row-like
62_2017_640_MOESM4_ESM.jpg (832 kb)
Streamlines (colored by velocity) at peak systolic for all cases. The white arrows show the regions of growth

References

  1. 1.
    Morita A, Kirino T, Hashi K, Aoki N, Fukuhara S, Hashimoto N, Nakayama T, Sakai M, Teramoto A, Tominari S, Yoshimoto T. The natural course of unruptured cerebral aneurysms in a Japanese cohort. N Engl J Med. 2012;366:2474–82.CrossRefPubMedGoogle Scholar
  2. 2.
    Wiebers DO, Whisnant JP, Huston J 3rd, Meissner I, Brown RD Jr, Piepgras DG, Forbes GS, Thielen K, Nichols D, O’Fallon WM, Peacock J, Jaeger L, Kassell NF, Kongable-Beckman GL, Torner JC; International Study of Unruptured Intracranial Aneurysms Investigators. Unruptured intracranial aneurysms: natural history, clinical outcome, and risks of surgical and endovascular treatment. Lancet. 2003;362:103–10.CrossRefPubMedGoogle Scholar
  3. 3.
    Greving JP, Wermer MJH, Brown RD, Morita A, Juvela S, Yonekura M, Ishibashi T, Torner JC, Nakayama T, Rinkel GJE, Algra A. Development of the PHASES score for prediction of risk of rupture of intracranial aneurysms: a pooled analysis of six prospective cohort studies. Lancet Neurol. 2014;13:59–66.CrossRefPubMedGoogle Scholar
  4. 4.
    Brinjikji W, Zhu YQ, Lanzino G, Cloft HJ, Murad MH, Wang Z, Kallmes DF. Risk factors for growth of intracranial aneurysms: a systematic review and meta-analysis. AJNR Am J Neuroradiol. 2016;37:615–20.CrossRefPubMedGoogle Scholar
  5. 5.
    Meng H, Wang Z, Hoi Y, Gao L, Metaxa E, Swartz DD, Kolega J. Complex hemodynamics at the apex of an arterial bifurcation induces vascular remodeling resembling cerebral aneurysm initiation. Stroke. 2007;38:1924–31.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Metaxa E, Tremmel M, Natarajan SK, Xiang J, Paluch RA, Mandelbaum M, Siddiqui AH, Kolega J, Mocco J, Meng H. Characterization of critical hemodynamics contributing to aneurysmal remodeling at the basilar terminus in a rabbit model. Stroke. 2010;41:1774–82.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Gondar R, Gautschi OP, Cuony J, Perren F, Jägersberg M, Corniola MV, Schatlo B, Molliqaj G, Morel S, Kulcsár Z, Mendes Pereira V, Rüfenacht D, Schaller K, Bijlenga P. Unruptured intracranial aneurysm follow-up and treatment after morphological change is safe: observational study and systematic review. J Neurol Neurosurg Psychiatr. 2016;87:1277–82.CrossRefGoogle Scholar
  8. 8.
    Backes D, Vergouwen MD, Tiel Groenestege AT, Bor AS, Velthuis BK, Greving JP, Algra A, Wermer MJ, van Walderveen MA, terBrugge KG, Agid R, Rinkel GJ. PHASES score for prediction of Intracranial aneurysm growth. Stroke. 2015;46:1221–6.CrossRefPubMedGoogle Scholar
  9. 9.
    Reymond P, Merenda F, Perren F, Rüfenacht D, Stergiopulos N. Validation of a one-dimensional model of the systemic arterial tree. Am J Physiol Heart Circ Physiol. 2009;297:H208–H22.CrossRefPubMedGoogle Scholar
  10. 10.
    Pereira VM, Brina O, Gonzales MA, Narata AP, Bijlenga P, Schaller K, Lovblad KO, Ouared R. Evaluation of the influence of inlet boundary conditions on computational fluid dynamics for intracranial aneurysms: a virtual experiment. J Biomech. 2013;46:1531–9.CrossRefPubMedGoogle Scholar
  11. 11.
    Backes D, Rinkel GJ, Laban KG, Algra A, Vergouwen MD. Patient- and aneurysm-specific risk factors for Intracranial aneurysm growth: a systematic review and meta-analysis. Stroke. 2016;47:951–7.CrossRefPubMedGoogle Scholar
  12. 12.
    Bor AS, Groenestege TT, terBrugge KG, Agid R, Velthuis BK, Rinkel GJ, Wermer MJ. Clinical, radiological, and flow-related risk factors for growth of untreated. Stroke. 2015;46:42–8.CrossRefPubMedGoogle Scholar
  13. 13.
    Burns JD, Huston J, Layton KF, Piepgras DG, Brown RD. Intracranial aneurysm enlargement on serial magnetic resonance angiography: frequency and risk factors. Stroke. 2009;40:406–11.CrossRefPubMedGoogle Scholar
  14. 14.
    Inoue T, Shimizu H, Fujimura M, Saito A, Tominaga T. Annual rupture risk of growing unruptured cerebral aneurysms detected by magnetic resonance angiography: clinical article. J Neurosurg. 2012;117:20–5.CrossRefPubMedGoogle Scholar
  15. 15.
    Villablanca JP, Duckwiler GR, Jahan R, Tateshima S, Martin NA, Frazee J, Gonzalez NR, Sayre J, Vinuela FV. Natural history of asymptomatic unruptured cerebral aneurysms evaluated at CT angiography: growth and rupture incidence and correlation with epidemiologic risk factors. Radiology. 2013;269:258–65.CrossRefPubMedGoogle Scholar
  16. 16.
    Kolega J, Gao L, Mandelbaum M, Mocco J, Siddiqui AH, Natarajan SK, Meng H. Cellular and molecular responses of the basilar terminus to hemodynamics during intracranial aneurysm initiation in a rabbit model. J Vasc Res. 2011;48:429–42.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Kulcsár Z, Ugron A, Marosfo IM, Berentei Z, Paál G, Szikora I. Hemodynamics of cerebral aneurysm initiation: the role of wall shear stress and spatial wall shear stress gradient. AJNR Am J Neuroradiol. 2011;32:587–94.CrossRefPubMedGoogle Scholar
  18. 18.
    Szikora I, Paal G, Ugron A, Nasztanovics F, Marosfoi M, Berentei Z, Kulcsar Z, Lee W, Bojtar I, Nyary I. Impact of aneurysmal geometry on intraaneurysmal flow: a computerized flow simulation study. Neuroradiology. 2008;50:411–21.CrossRefPubMedGoogle Scholar
  19. 19.
    Cebral JR, Sheridan M, Putman CM. Hemodynamics and bleb formation in intracranial aneurysms. AJNR Am J Neuroradiol. 2010;31:304–10.CrossRefPubMedGoogle Scholar
  20. 20.
    Shojima M, Nemoto S, Morita A, Oshima M, Watanabe E, Saito N. Role of shear stress in the blister formation of cerebral aneurysms. Neurosurgery. 2010;67:1268–74. discussion 1274–5.CrossRefPubMedGoogle Scholar
  21. 21.
    Tanoue T, Tateshima S, Villablanca JP, Vinuela F, Tanishita K. Wall shear stress distribution inside growing cerebral aneurysm. AJNR Am J Neuroradiol. 2011;32:1732–7.CrossRefPubMedGoogle Scholar
  22. 22.
    Sugiyama S, Meng H, Funamoto K, Inoue T, Fujimura M, Nakayama T, Omodaka S, Shimizu H, Takahashi A, Tominaga T. Hemodynamic analysis of growing intracranial aneurysms arising from a posterior inferior cerebellar artery. World Neurosurg. 2012;78:462–8.CrossRefPubMedGoogle Scholar
  23. 23.
    Russell JH, Kelson N, Barry M, Pearcy M, Fletcher DF, Winter CD. Computational fluid dynamic analysis of intracranial aneurysmal bleb formation. Neurosurgery. 2013;73:1061–8. discussion 1068–9.CrossRefPubMedGoogle Scholar
  24. 24.
    Sugiyama SI, Endo H, Omodaka S, Endo T, Niizuma K, Rashad S, Nakayama T, Funamoto K, Ohta M, Tominaga T. Daughter sac formation related to blood inflow jet in an intracranial aneurysm. World Neurosurg. 2016;96:396–402.CrossRefPubMedGoogle Scholar
  25. 25.
    Boussel L, Rayz V, McCulloch C, Martin A, Acevedo-Bolton G, Lawton M, Higashida R, Smith WS, Young WL, Saloner D. Aneurysm growth occurs at region of low wall shear stress: patient-specific. Stroke. 2008;39:2997–3002.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Brinjikji W, Chung BJ, Jimenez C, Putman C, Kallmes DF, Cebral JR. Hemodynamic differences between unstable and stable unruptured aneurysms independent of size and location: a pilot study. J Neurointerv Surg. 2016;9:376–80.CrossRefPubMedGoogle Scholar
  27. 27.
    Sforza DM, Kono K, Tateshima S, Vinuela F, Putman C, Cebral JR. Hemodynamics in growing and stable cerebral aneurysms. J Neurointerv Surg. 2016;8:407–12.CrossRefPubMedGoogle Scholar
  28. 28.
    Koffijberg H, Buskens E, Algra A, Wermer MJ, Rinkel GJ. Growth rates of intracranial aneurysms: exploring constancy. J Neurosurg. 2008;109:176–85.CrossRefPubMedGoogle Scholar
  29. 29.
    Zhang Y, Mu S, Chen J, Wang S, Li H, Yu H, Jiang F, Yang X. Hemodynamic analysis of intracranial aneurysms with daughter blebs. Eur Neurol. 2011;66:359–67.CrossRefPubMedGoogle Scholar
  30. 30.
    Meng H, Tutino VM, Xiang J, Siddiqui A. High WSS or low WSS? Complex interactions of hemodynamics with intracranial. AJNR Am J Neuroradiol. 2014;35:1254–62.CrossRefPubMedGoogle Scholar
  31. 31.
    Zhu YQ, Li MH, Yan L, Tan HQ, Cheng YS. Arterial wall degeneration plus hemodynamic insult cause arterial wall remodeling. J Neuropathol Exp Neurol. 2014;73:808–19.CrossRefPubMedGoogle Scholar
  32. 32.
    Cebral J, Ollikainen E, Chung BJ, Mut F, Sippola V, Jahromi BR, Tulamo R, Hernesniemi J, Niemelä M, Robertson A, Frösen J. Flow conditions in the intracranial aneurysm lumen are associated with inflammation and degenerative changes of the aneurysm wall. AJNR Am J Neuroradiol. 2017;38:119–26.CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Paolo Machi
    • 1
  • Rafik Ouared
    • 1
  • Olivier Brina
    • 1
  • Pierre Bouillot
    • 1
    • 2
  • Hasan Yilmaz
    • 1
  • Maria I Vargas
    • 1
  • Renato Gondar
    • 3
  • Philippe Bijlenga
    • 3
  • Karl O Lovblad
    • 1
  • Zsolt Kulcsár
    • 1
    • 4
    Email author
  1. 1.Neuroradiology Division, Department of Radiology and Medical InformaticsGeneva University HospitalsGenevaSwitzerland
  2. 2.Laboratory for Hydraulic MachinesÉcole Polytechnique Fédérale de LausanneLausanneSwitzerland
  3. 3.Neurosurgery Division, Department of Clinical NeurosciencesGeneva University HospitalsGenevaSwitzerland
  4. 4.Department of NeuroradiologyUniversity Hospital of ZurichZürichSwitzerland

Personalised recommendations