Top

Published in:

01-04-2017 | Case Report

Hemodynamic changes in a middle cerebral artery aneurysm at follow-up times before and after its rupture: a case report and a review of the literature

Authors: A. Sejkorová, K. D. Dennis, H. Švihlová, O. Petr, G. Lanzino, A. Hejčl, D. Dragomir-Daescu

Published in: Neurosurgical Review | Issue 2/2017

Abstract

Hemodynamic parameters play a significant role in the development of cerebral aneurysms. Parameters such as wall shear stress (WSS) or velocity could change in time and may contribute to aneurysm growth and rupture. However, the hemodynamic changes at the rupture location remain unclear because it is difficult to obtain data prior to rupture. We analyzed a case of a ruptured middle cerebral artery (MCA) aneurysm for which we acquired imaging data at three time points, including at rupture. A patient with an observed MCA aneurysm was admitted to the emergency department with clinical symptoms of a subarachnoid hemorrhage. During three-dimensional (3D) digital subtraction angiography (DSA), the aneurysm ruptured again. Imaging data from two visits before rupture and this 3D DSA images at the moment of rupture were acquired, and computational fluid dynamic (CFD) simulations were performed. Results were used to describe the time-dependent changes of the hemodynamic variables associated with rupture. Time-dependent hemodynamic changes at the rupture location were characterized by decreased WSS and flow velocity magnitude. The impingement jet in the dome changed its position in time and the impingement area at follow-up moved near the rupture location. The results suggest that the increased WSS on the dome and increased low wall shear stress area (LSA) and decreased WSS on the daughter bleb with slower flow and slow vortex may be associated with rupture. CFD performed during the follow-up period may be part of diagnostic tools used to determine the risk of aneurysm rupture.

Bor AS, Tiel Groenestege AT, terBrugge KG, Agid R, Velthuis BK, Rinkel GJ, Wermer MJ (2015) Clinical, radiological, and flow-related risk factors for growth of untreated, unruptured intracranial aneurysms. Stroke; a journal of cerebral circulation 46:42–48CrossRef

Boussel L, Rayz V, McCulloch C, Martin A, Acevedo-Bolton G, Lawton M, Higashida R, Smith WS, Young WL, Saloner D (2008) Aneurysm growth occurs at region of low wall shear stress. Patient-Specific Correlation of Hemodynamics and Growth in a Longitudinal Study Stroke 39:2997–3002

Bowker TJ, Watton PN, Summers PE, Byrne JV, Ventikos Y (2010) Rest versus exercise hemodynamics for middle cerebral artery aneurysms: a computational study. AJNR Am J Neuroradiol 31:317–323CrossRefPubMed

Castro MA, Ahumada Olivares MC, Putman CM, Cebral JR (2014) Unsteady wall shear stress analysis from image-based computational fluid dynamic aneurysm models under Newtonian and Casson rheological models. Med Biol Eng Comput 52:827–839CrossRefPubMed

Castro MA, Putman CM, Cebral JR (2006) Computational fluid dynamics modeling of intracranial aneurysms: effects of parent artery segmentation on intra-aneurysmal hemodynamics. AJNR Am J Neuroradiol 27:1703–1709PubMed

Cebral JR, Castro MA, Appanaboyina S, Putman CM, Millan D, Frangi AF (2005) Efficient pipeline for image-based patient-specific analysis of cerebral aneurysm hemodynamics: technique and sensitivity. IEEE Trans Med Imaging 24:457–467CrossRefPubMed

Cebral JR, Castro MA, Burgess JE, Pergolizzi RS, Sheridan MJ, Putman CM (2005) Characterization of cerebral aneurysms for assessing risk of rupture by using patient-specific computational hemodynamics models. AJNR Am J Neuroradiol 26:2550–2559PubMed

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 32:145–151CrossRefPubMed

Cebral JR, Sheridan M, Putman CM (2010) Hemodynamics and bleb formation in intracranial aneurysms. AJNR Am J Neuroradiol 31:304–310CrossRefPubMed

10.

Chien A, Castro MA, Tateshima S, Sayre J, Cebral J, Vinuela F (2009) Quantitative hemodynamic analysis of brain aneurysms at different locations. AJNR Am J Neuroradiol 30:1507–1512CrossRefPubMed

11.

Chien A, Sayre J (2014) Morphologic and hemodynamic risk factors in ruptured aneurysms imaged before and after rupture. Am J Neuroradiol 35:2130–2135CrossRefPubMed

12.

Cloft HJ, Joseph GJ, Dion JE (1999) Risk of cerebral angiography in patients with subarachnoid hemorrhage, cerebral aneurysm, and arteriovenous malformation: a meta-analysis. Stroke 30:317–320CrossRefPubMed

13.

Cornelissen BMW, Schneiders JJ, Potters WV, Van Den Berg R, Velthuis BK, Rinkel GJE, Slump CH, VanBavel E, Majoie CBLM, Marquering HA (2015) Hemodynamic differences in intracranial aneurysms before and after rupture. Am J Neuroradiol 36:1927–1933CrossRefPubMed

14.

D’Arcangelo D, Ambrosino V, Giannuzzo M, Gaetano C, Capogrossi MC (2006) Axl receptor activation mediates laminar shear stress anti-apoptotic effects in human endothelial cells. Cardiovasc Res 71:754–763CrossRefPubMed

15.

Dhar S, Tremmel M, Mocco J, Kim M, Yamamoto J, Siddiqui AH, Hopkins LN, Meng H (2008) Morphology parameters for intracranial aneurysm rupture risk assessment. Neurosurgery 63:185–197CrossRefPubMedPubMedCentral

16.

Duan G, Lv N, Yin J, Xu J, Hong B, Xu Y, Liu J, Huang Q (2016) Morphological and hemodynamic analysis of posterior communicating artery aneurysms prone to rupture: a matched case-control study. Journal of NeuroInterventional Surgery 8:47–51CrossRefPubMed

17.

Fukazawa K, Ishida F, Umeda Y, Miura Y, Shimosaka S, Matsushima S, Taki W, Suzuki H (2015) Using computational fluid dynamics analysis to characterize local hemodynamic features of middle cerebral artery aneurysm rupture points. World Neurosurg 83:80–86CrossRefPubMed

18.

Geers AJ, Larrabide I, Radaelli AG, Bogunovic H, Kim M, Gratama van Andel HA, Majoie CB, VanBavel E, Frangi AF (2011) Patient-specific computational hemodynamics of intracranial aneurysms from 3d rotational angiography and ct angiography: an in vivo reproducibility study. AJNR Am J Neuroradiol 32:581–586CrossRefPubMed

19.

Goubergrits L, Schaller J, Kertzscher U, van den Bruck N, Poethkow K, Petz C, Hege HC, Spuler A (2012) Statistical wall shear stress maps of ruptured and unruptured middle cerebral artery aneurysms. J R Soc Interface 9:677–688CrossRefPubMed

20.

Grzyska U, Freitag J, Zeumer H (1990) Selective cerebral intraarterial DSA: complication rate and control of risk factors. Neuroradiology 32:296–299CrossRefPubMed

21.

Hassan T, Timofeev EV, Saito T, Shimizu H, Ezura M, Matsumoto Y, Takayama K, Tominaga T, Takahashi A (2005) A proposed parent vessel geometry-based categorization of saccular intracranial aneurysms: computational flow dynamics analysis of the risk factors for lesion rupture.[erratum appears in j neurosurg. 2005 dec;103(6):1110]. J Neurosurg 103:662–680CrossRefPubMed

22.

He X, Ku DN (1996) Pulsatile flow in the human left coronary artery bifurcation: average conditions. J Biomech Eng 118:74–82CrossRefPubMed

23.

Himburg HA, Grzybowski DM, Hazel AL, LaMack JA, Li X-M, Friedman MH (2004) Spatial comparison between wall shear stress measures and porcine arterial endothelial permeability. Am J Physiol Heart Circ Physiol 286:H1916–H1922CrossRefPubMed

24.

Hodis S, Uthamaraj S, Lanzino G, Kallmes DF, Dragomir-Daescu D (2014) Computational fluid dynamics simulation of an anterior communicating artery ruptured during angiography. J Neurointerv Surg 6:e14CrossRefPubMed

25.

Hodis S, Uthamaraj S, Smith AL, Dennis KD, Kallmes DF, Dragomir-Daescu D (2012) Grid convergence errors in hemodynamic solution of patient-specific cerebral aneurysms. J Biomech 45:2907–2913CrossRefPubMed

26.

Investigators TISoUIA (1998) Unruptured intracranial aneurysms—risk of rupture and risks of surgical intervention. N Engl J Med 339:1725–1733CrossRef

27.

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:e0132494CrossRefPubMedPubMedCentral

28.

Jou LD, Lee DH, Morsi H, Mawad ME (2008) Wall shear stress on ruptured and unruptured intracranial aneurysms at the internal carotid artery. AJNR Am J Neuroradiol 29:1761–1767CrossRefPubMed

29.

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 119:172–179CrossRefPubMed

30.

Li ML, Wang YC, Liou TM, Lin CA (2014) The hemodynamics in intracranial aneurysm ruptured region with active contrast leakage during computed tomography angiography. Comput Mech 54:987–997CrossRef

31.

Li Y-SJ, Haga JH, Chien S (2005) Molecular basis of the effects of shear stress on vascular endothelial cells. J Biomech 38:1949–1971CrossRefPubMed

32.

Liu J, Fan J, Xiang J, Zhang Y, Yang X (2016) Hemodynamic characteristics of large unruptured internal carotid artery aneurysms prior to rupture: a case control study. Journal of Neurointerventional Surgery 8:367–372CrossRefPubMed

33.

Meng H, Tutino VM, Xiang J, Siddiqui A (2014) High WSS or low WSS? Complex interactions of hemodynamics with intracranial aneurysm initiation, growth, and rupture: toward a unifying hypothesis. Am J Neuroradiol 35:1254–1262CrossRefPubMed

34.

Meng H, Wang Z, Hoi Y, Gao L, Metaxa E, Swartz DD, Kolega J (2007) Complex hemodynamics at the apex of an arterial bifurcation induces vascular remodeling resembling cerebral aneurysm initiation. Stroke 38:1924–1931CrossRefPubMedPubMedCentral

35.

Miura Y, Ishida F, Umeda Y, Tanemura H, Suzuki H, Matsushima S, Shimosaka S, Taki W (2013) Low wall shear stress is independently associated with the rupture status of middle cerebral artery aneurysms. Stroke 44:519–521CrossRefPubMed

36.

Mut F, Lohner R, Chien AC, Tateshima S, Vinuela F, Putman C, Cebral JR (2011) Computational hemodynamics framework for the analysis of cerebral aneurysms. Int J Numer Method Biomed Eng 27:822–839CrossRefPubMedPubMedCentral

37.

Nixon AM, Gunel M, Sumpio BE (2010) The critical role of hemodynamics in the development of cerebral vascular disease. J Neurosurg 112:1240–1253CrossRefPubMed

38.

Omodaka S, Inoue T, Funamoto K, Sugiyama S, Shimizu H, Hayase T, Takahashi A, Tominaga T (2012) Influence of surface model extraction parameter on computational fluid dynamics modeling of cerebral aneurysms. J Biomech 45:2355–2361CrossRefPubMed

39.

Omodaka S, Sugiyama S, Inoue T, Funamoto K, Fujimura M, Shimizu H, Hayase T, Takahashi A, Tominaga T (2012) Local hemodynamics at the rupture point of cerebral aneurysms determined by computational fluid dynamics analysis. Cerebrovasc Dis 34:121–129CrossRefPubMed

40.

Qian Y, Takao H, Umezu M, Murayama Y (2011) Risk analysis of unruptured aneurysms using computational fluid dynamics technology: preliminary results. AJNR Am J Neuroradiol 32:1948–1955CrossRefPubMed

41.

Raghavan ML, Ma B, Harbaugh RE (2005) Quantified aneurysm shape and rupture risk. J Neurosurg 102:355–362CrossRefPubMed

42.

Shojima M, Nemoto S, Morita A, Oshima M, Watanabe E, Saito N (2010) Role of shear stress in the blister formation of cerebral aneurysms. Neurosurgery 67:1268–1274CrossRefPubMed

43.

Shojima M, Oshima M, Takagi K, Hayakawa M, Katada K, Morita A, Kirino T (2006) Numerical simulation of the intra-aneurysmal flow dynamics. Interv Neuroradiol 12:49–52CrossRefPubMedPubMedCentral

44.

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 35:2500–2505CrossRefPubMed

45.

Shojima M, Oshima M, Takagi K, Torii R, Nagata K, Shirouzu I, Morita A, Kirino T (2005) Role of the bloodstream impacting force and the local pressure elevation in the rupture of cerebral aneurysms. Stroke 36:1933–1938CrossRefPubMed

46.

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 73:767–776CrossRefPubMed

47.

Sun Q, Groth A, Aach T (2012) Comprehensive validation of computational fluid dynamics simulations of in-vivo blood flow in patient-specific cerebral aneurysms. Med Phys 39:742–754CrossRefPubMed

48.

Szikora I, Paal G, Ugron A, Nasztanovics F, Marosfoi M, Berentei Z, Kulcsar Z, Lee W, Bojtar I, Nyary I (2008) Impact of aneurysmal geometry on intraaneurysmal flow: a computerized flow simulation study. Neuroradiology 50:411–421CrossRefPubMed

49.

Takao H, Murayama Y, Otsuka S, Qian Y, Mohamed A, Masuda S, Yamamoto M, Abe T (2012) Hemodynamic differences between unruptured and ruptured intracranial aneurysms during observation. Stroke 43:1436–1439CrossRefPubMed

50.

Ujiie H, Tachibana H, Hiramatsu O, Hazel AL, Matsumoto T, Ogasawara Y, Nakajima H, Hori T, Takakura K, Kajiya F (1999) Effects of size and shape (aspect ratio) on the hemodynamics of saccular aneurysms: a possible index for surgical treatment of intracranial aneurysms. Neurosurgery 45:119PubMed

51.

Valen-Sendstad K, Mardal KA, Mortensen M, Reif BA, Langtangen HP (2011) Direct numerical simulation of transitional flow in a patient-specific intracranial aneurysm. J Biomech 44:2826–2832CrossRefPubMed

52.

Valen-Sendstad K, Mardal KA, Steinman DA (2013) High-resolution CFD detects high-frequency velocity fluctuations in bifurcation, but not sidewall, aneurysms. J Biomech 46:402–407CrossRefPubMed

53.

Wang SZ, Chen JL, Ding GH, Lu G, Zhang XL (2010) Non-newtonian computational hemodynamics in two patient-specific cerebral aneurysms with daughter saccules. J Hydrodyn 22:639–646CrossRef

54.

Wiebers DO (2003) Unruptured intracranial aneurysms: natural history, clinical outcome, and risks of surgical and endovascular treatment. Lancet 362:103–110CrossRefPubMed

55.

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 42:144–152CrossRefPubMed

Title: Hemodynamic changes in a middle cerebral artery aneurysm at follow-up times before and after its rupture: a case report and a review of the literature
Authors: A. Sejkorová
K. D. Dennis
H. Švihlová
O. Petr
G. Lanzino
A. Hejčl
D. Dragomir-Daescu
Publication date: 01-04-2017
Publisher: Springer Berlin Heidelberg
Published in: Neurosurgical Review / Issue 2/2017
Print ISSN: 0344-5607
Electronic ISSN: 1437-2320
DOI: https://doi.org/10.1007/s10143-016-0795-7

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Hemodynamic changes in a middle cerebral artery aneurysm at follow-up times before and after its rupture: a case report and a review of the literature

Abstract

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 2/2017

Cerebrospinal fluid leaks in extended endoscopic transsphenoidal surgery: covering all the angles

Assessment of the cortical artery using computed tomography angiography for bypass surgery in moyamoya disease

Surgical safety of cervical pedicle screw placement with computer navigation system

Intradiploic pseudomeningocele and ossified occipitocervical pseudomeningocele after decompressive surgery for Chiari I malformation: report of two cases and literature review

Flow reversal bypass surgery: a treatment option for giant serpentine and dolichoectatic aneurysms—internal maxillary artery bypass with an interposed radial artery graft followed by parent artery occlusion

Posterior fossa decompression with and without duraplasty for the treatment of Chiari malformation type I—a systematic review and meta-analysis