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Hemodynamic findings associated with intraoperative appearances of intracranial aneurysms

  • Pengjun Jiang
  • Qingyuan Liu
  • Jun Wu
  • Xin Chen
  • Maogui Li
  • Fan Yang
  • Zhengsong Li
  • Shuzhe Yang
  • Rui Guo
  • Bin Gao
  • Yong Cao
  • Rong Wang
  • Fei DiEmail author
  • Shuo WangEmail author
Original Article
  • 120 Downloads

Abstract

Intracranial aneurysms can be classified into thick-walled aneurysms and thin-walled aneurysms according to their intraoperative appearances; previous publications have revealed that different kinds of intraoperative appearances were associated with intraoperative rupture and postoperative complications. Here, we tried to evaluate the association between hemodynamic features and aneurysm wall appearance using computational fluid dynamics (CFD) method. Forty-one consecutive patients with unruptured middle cerebral artery (MCA) bifurcation aneurysms were included in our study. Based on the appearances observed under the microscope, aneurysms were classified into two different types: thick-walled and thin-walled aneurysms. Preoperative computed tomographic angiography (CTA) was used for geometry reconstruction and CFD analysis. Morphological and hemodynamic parameters were compared between the two groups. Eighteen aneurysms were classified as thick-walled atherosclerotic ones according to their intraoperative appearances. Compared with thin-walled aneurysms, aneurysms with atherosclerotic changes had larger geometry parameters (aneurysm depth, maximum height, diameter, aspect ratio, size ratio), lower wall shear stress (WSS), and larger low WSS area ratio (LSAR). Thick-walled aneurysms characterized by atherosclerotic changes are associated with low WSS and larger LSAR. CFD may be a useful tool for discriminating the intraoperative appearance of cerebral aneurysms.

Keywords

Cerebral aneurysm Hemodynamics Wall shear stress Intraoperative appearance Atherosclerotic change 

Notes

Funding

This work was supported by the National Key Research and Development Program of National Key Basic Research Development of China (Grant No. 2016YFC1301800) and the projects of National Natural Science Foundation of China (Grant No. 81471210 and 81671129).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Informed consent

The need for written informed consent was waived, due to the retrospective nature of this study.

Ethical approval

This study has been approved by the ethics committee of Beijing Tiantan Hospital, Capital Medical University.

References

  1. 1.
    Aoki T, Kataoka H, Ishibashi R, Nozaki K, Egashira K, Hashimoto N (2009) Impact of monocyte chemoattractant protein-1 deficiency on cerebral aneurysm formation. Stroke 40:942–951CrossRefGoogle Scholar
  2. 2.
    Aoki T, Yamamoto K, Fukuda M, Shimogonya Y, Fukuda S, Narumiya S (2016) Sustained expression of MCP-1 by low wall shear stress loading concomitant with turbulent flow on endothelial cells of intracranial aneurysm. Acta Neuropathol Commun 4(48):48CrossRefGoogle Scholar
  3. 3.
    Asari S, Ohmoto T (1994) Growth and rupture of unruptured cerebral aneurysms based on the intraoperative appearance. Acta Med Okayama 48:257–262PubMedGoogle Scholar
  4. 4.
    Boulouis G, Rodriguez-Regent C, Rasolonjatovo EC, Ben Hassen W, Trystram D, Edjlali-Goujon M, Meder JF, Oppenheim C, Naggara O (2017) Unruptured intracranial aneurysms: an updated review of current concepts for risk factors detection and management. Rev Neurol (Paris) 173:542–551CrossRefGoogle Scholar
  5. 5.
    Byrne G, Mut F, Cebral J (2014) Quantifying the large-scale hemodynamics of intracranial aneurysms. AJNR Am J Neuroradiol 35:333–338CrossRefGoogle Scholar
  6. 6.
    Can A, Du R (2016) Association of hemodynamic factors with intracranial aneurysm formation and rupture: systematic review and meta-analysis. Neurosurgery 78:510–520CrossRefGoogle Scholar
  7. 7.
    Cebral J, Ollikainen E, Chung BJ, Mut F, Sippola V, Jahromi BR, Tulamo R, Hernesniemi J, Niemelä M, Robertson A (2016) Flow conditions in the intracranial aneurysm lumen are associated with inflammation and degenerative changes of the aneurysm wall. AJNR Am J Neuroradiol 38Google Scholar
  8. 8.
    Cebral JR, Mut F, Weir J, Putman C (2011) Quantitative characterization of the hemodynamic environment in ruptured and unruptured brain aneurysms. AJNR Am J Neuroradiol 32:145–151CrossRefGoogle Scholar
  9. 9.
    Cebral JR, Mut F, Weir J, Putman CM (2011) Association of hemodynamic characteristics and cerebral aneurysm rupture. AJNR Am J Neuroradiol 32:264–270CrossRefGoogle Scholar
  10. 10.
    Chalouhi N, Ali MS, Jabbour PM, Tjoumakaris SI, Gonzalez LF, Rosenwasser RH, Koch WJ, Dumont AS (2012) Biology of intracranial aneurysms: role of inflammation. J Cereb Blood Flow Metab 32:1659–1676CrossRefGoogle Scholar
  11. 11.
    Chen XL, Chen Y, Ma L, Burkhardt JK, Wardell T, Wang C, Guo G, Wang S, Zhao YL (2017) Translucent appearance of middle cerebral artery bifurcation aneurysms is a risk factor for intraoperative aneurysm rupture during clipping. World Neurosurg 101:149–154CrossRefGoogle Scholar
  12. 12.
    Etminan N, Rinkel GJ (2017) Unruptured intracranial aneurysms: development rupture and preventive management. Nat Rev Neurol 13:126–126CrossRefGoogle Scholar
  13. 13.
    Feigin VL, Rinkel GJ, Lawes CM, Algra A, Bennett DA, Van GJ, Anderson CS (2005) Risk factors for subarachnoid hemorrhage: an updated systematic review of epidemiological studies. Stroke 36:2773–2780CrossRefGoogle Scholar
  14. 14.
    Frösen J, Piippo A, Paetau A, Kangasniemi M, Niemelä M, Hernesniemi J, Jääskeläinen J (2004) Remodeling of saccular cerebral artery aneurysm wall is associated with rupture histological analysis of 24 unruptured and 42 ruptured cases. Stroke 35:2287–2293CrossRefGoogle Scholar
  15. 15.
    Frösen J, Tulamo R, Paetau A, Laaksamo E, Korja M, Laakso A, Niemelä M, Hernesniemi J (2012) Saccular intracranial aneurysm: pathology and mechanisms. Acta Neuropathol 123:773–786CrossRefGoogle Scholar
  16. 16.
    Geng Z, Zhu Y, Yin Y, Ming S, Li M (2017) Association of wall shear stress with intracranial aneurysm rupture: systematic review and meta-analysis. Sci Rep 7:5331CrossRefGoogle Scholar
  17. 17.
    Greving JP, Wermer MJ, Jr BR, Morita A, Juvela S, Yonekura M, Ishibashi T, Torner JC, Nakayama T, Rinkel GJ (2014) Development of the PHASES score for prediction of risk of rupture of intracranial aneurysms: a pooled analysis of six prospective cohort studies. Lancet Neurol 13:59–66CrossRefGoogle Scholar
  18. 18.
    Himburg HA, Grzybowski DM, Hazel AL, Lamack JA, Li XM, Friedman MH (2004) Spatial comparison between wall shear stress measures and porcine arterial endothelial permeability. Am J Physiol Heart Circ Physiol 286:H1916–H1922CrossRefGoogle Scholar
  19. 19.
    Jing L, Fan J, Wang Y, Li H, Wang S, Yang X, Zhang Y (2015) Morphologic and hemodynamic analysis in the patients with multiple intracranial aneurysms: ruptured versus unruptured. PLoS One 10:e0132494CrossRefGoogle Scholar
  20. 20.
    Jou L, Lee DH, Mawad M (2008) Wall shear stress on ruptured and unruptured intracranial aneurysms at the internal carotid artery. AJNR Am J Neuroradiol 29:1761–1767CrossRefGoogle Scholar
  21. 21.
    Juvela S, Poussa K, Lehto H, Porras M (2013) Natural history of unruptured intracranial aneurysms: a long-term follow-up study. Stroke 93:2414–2421CrossRefGoogle Scholar
  22. 22.
    Kadasi LM, Dent WC, Malek AM (2013) Cerebral aneurysm wall thickness analysis using intraoperative microscopy: effect of size and gender on thin translucent regions. J Neurointerv Surg 5:201–206CrossRefGoogle Scholar
  23. 23.
    Kadasi LM, Dent WC, Malek AM (2013) Colocalization of thin-walled dome regions with low hemodynamic wall shear stress in unruptured cerebral aneurysms. J Neurosurg 119:172–179CrossRefGoogle Scholar
  24. 24.
    Kanematsu Y, Kanematsu M, Kurihara C, Tada Y, Tsou TL, Van RN, Lawton MT, Young WL, Liang EI, Nuki Y (2011) Critical roles of macrophages in the formation of intracranial aneurysm. Stroke 42:173–178CrossRefGoogle Scholar
  25. 25.
    Kleinloog R, Verweij BH, Van dVP, Deelen P, Swertz MA, De ML, Van DP, Giuliani F, Regli L, Van dZA (2016) RNA sequencing analysis of intracranial aneurysm walls reveals involvement of lysosomes and immunoglobulins in rupture. Stroke 47:1286–1293CrossRefGoogle Scholar
  26. 26.
    Lall RR, Eddleman CS, Bendok BR, Batjer HH (2009) Unruptured intracranial aneurysms and the assessment of rupture risk based on anatomical and morphological factors: sifting through the sands of data. Neurosurg Focus 26:E2CrossRefGoogle Scholar
  27. 27.
    Li L, Yang X, Fan J, Dusting GJ, Wu Z (2009) Transcriptome-wide characterization of gene expression associated with unruptured intracranial aneurysms. Eur Neurol 62:330–337CrossRefGoogle Scholar
  28. 28.
    Listed N (1998) Unruptured intracranial aneurysms--risk of rupture and risks of surgical intervention. International study of unruptured intracranial aneurysms investigators. N Engl J Med 339:1725CrossRefGoogle Scholar
  29. 29.
    Malek AM, Alper SL, Izumo S (1999) Hemodynamic shear stress and its role in atherosclerosis. Jama 282:2035–2042CrossRefGoogle Scholar
  30. 30.
    Mathiesen T, Armonda RA, Lawton MT (2013) Anatomic risk factors for middle cerebral artery aneurysm rupture: computed tomography angiography study of 1009 consecutive patients. COMMENTS. Neurosurgery 73:836–837Google Scholar
  31. 31.
    Ollikainen E, Tulamo R, Lehti S, Leerueckert M, Hernesniemi J, Niemelä M, Yläherttuala S, Kovanen PT, Frösen J (2016) Smooth muscle cell foam cell formation, apolipoproteins, and ABCA1 in intracranial aneurysms: implications for lipid accumulation as a promoter of aneurysm wall rupture. J Neuropathol Exp Neurol 75:689–699CrossRefGoogle Scholar
  32. 32.
    Sforza DM, Putman CM, Cebral JR (2009) Hemodynamics of cerebral aneurysms. Annu Rev Fluid Mech 41:91–107CrossRefGoogle Scholar
  33. 33.
    Shojima M, Oshima M, Takagi K, Torii R, Hayakawa M, Katada K, Morita A, Kirino T (2004) Magnitude and role of wall shear stress on cerebral aneurysm: computational fluid dynamic study of 20 middle cerebral artery aneurysms. Stroke 35:2500–2505CrossRefGoogle Scholar
  34. 34.
    Song J, Park JE, Kim HR, Yong SS (2015) Observation of cerebral aneurysm wall thickness using intraoperative microscopy: clinical and morphological analysis of translucent aneurysm. Neurol Sci 36:907–912CrossRefGoogle Scholar
  35. 35.
    Sugiyama S, Niizuma K, Nakayama T, Shimizu H, Endo H, Inoue T, Fujimura M, Ohta M, Takahashi A, Tominaga T (2013) Relative residence time prolongation in intracranial aneurysms: a possible association with atherosclerosis. Neurosurgery 73:767–776CrossRefGoogle Scholar
  36. 36.
    Suzuki T, Takao H, Suzuki T, Kambayashi Y, Watanabe M, Sakamoto H, Kan I, Nishimura K, Kaku S, Ishibashi T (2016) Determining the presence of thin-walled regions at high-pressure areas in unruptured cerebral aneurysms by using computational fluid dynamics. Neurosurgery 79:589–595CrossRefGoogle Scholar
  37. 37.
    Szelényi A, Beck J, Strametz R, Blasel S, Oszvald A, Raabe A, Seifert V (2011) Is the surgical repair of unruptured atherosclerotic aneurysms at a higher risk of intraoperative ischemia? Clin Neurol Neurosurg 113:129–135CrossRefGoogle Scholar
  38. 38.
    Tateshima S, Tanishita K, Omura H, Sayre J, Villablanca JP, Martin N, Vinuela F (2008) Intra-aneurysmal hemodynamics in a large middle cerebral artery aneurysm with wall atherosclerosis. Surg Neurol 70:454–462CrossRefGoogle Scholar
  39. 39.
    Xiang J, Natarajan SK, Tremmel M, Ma D, Mocco J, Hopkins LN, Siddiqui AH, Levy EI, Meng H (2011) Hemodynamic-morphologic discriminants for intracranial aneurysm rupture. Stroke 42:144–152CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Neurosurgery, Beijing Tiantan HospitalCapital Medical UniversityBeijingPeople’s Republic of China
  2. 2.China National Clinical Research Center for Neurological DiseasesBeijingPeople’s Republic of China
  3. 3.Center of Stroke, Beijing Institute for Brain DisordersBeijingPeople’s Republic of China
  4. 4.Beijing Key Laboratory of Translational Medicine for Cerebrovascular DiseasesBeijingPeople’s Republic of China
  5. 5.School of Life Science and BioEngineeringBeijing University of TechnologyBeijingPeople’s Republic of China

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