Identification of a dichotomy in morphological predictors of rupture status between sidewall- and bifurcation-type intracranial aneurysms

Clinical article

Merih I. Baharoglu M.D., Alexandra Lauric Ph.D., Bu-Lang Gao M.D., Ph.D. and Adel M. Malek M.D., Ph.D.
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  • Cerebrovascular and Endovascular Division, Department of Neurosurgery, Tufts Medical Center and Tufts University School of Medicine, Boston, Massachusetts
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Object

Prediction of aneurysm rupture likelihood is clinically valuable, given that more unruptured aneurysms are being discovered incidentally with the increased use of imaging. The authors set out to evaluate the relative performance of morphological features for rupture status discrimination in the context of the divergent geometrical and hemodynamic characteristics of sidewall- and bifurcation-type aneurysms.

Methods

Catheter 3D rotational angiographic images of 271 consecutive aneurysms (101 ruptured, 135 bifurcation type) were used to assess the following parameters in 3D: maximum diameter (Dmax), height, height/width ratio, aspect ratio, size ratio, nonsphericity index, and inflow angle. Univariate statistics applied to the bifurcation, sidewall, and combined (bifurcation + sidewall) sets identified significant features for inclusion in multivariate analysis yielding area under the curve (AUC) and optimal thresholds in the receiver-operating characteristic. Furthermore, a computational fluid dynamics analysis was performed to evaluate the flow and wall shear stress conditions inside sidewall and bifurcation aneurysms at different inflow angles.

Results

The mean Dmax, height, and inflow angle were significantly greater in ruptured sidewall aneurysms than in unruptured sidewall aneurysms, but showed no difference between ruptured and unruptured bifurcation lesions. There was a statistically significant difference between ruptured and unruptured aneurysms for all measured features in the combined set. Multivariate analysis identified the following: 1) nonsphericity index as the only rupture status discriminator in bifurcation lesions (AUC = 0.67); 2) height/width ratio, size ratio, and inflow angle as strong discriminators in sidewall lesions (AUC = 0.87); and 3) height/width ratio, inflow angle, and size ratio as intermediate discriminators in the combined group (AUC = 0.76). Computational fluid dynamics analysis showed that although increasing inflow angle in a sidewall model led to deeper penetration of flow, higher velocities, and higher wall shear stress inside the aneurysm dome, it produced the exact opposite results in a bifurcation model.

Conclusions

Retrospective morphological and hemodynamic analysis point to a dichotomy between sidewall and bifurcation aneurysms with respect to performance of shape and size parameters in identifying rupture status, suggesting the need for aneurysm type–based analyses in future studies. The current most commonly used clinical risk assessment metric, Dmax, was found to be of no value in differentiating between ruptured and unruptured bifurcation aneurysms.

Abbreviations used in this paper:AUC = area under the receiver-operating curve; CFD = computational fluid dynamics; Dmax = largest diameter of aneurysm dome; ICA = internal carotid artery; ISUIA = International Study of Unruptured Intracranial Aneurysms; PCoA = posterior communicating artery; ROC = receiver-operating curve or characteristic.

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Contributor Notes

Address correspondence to: Adel M. Malek, M.D., Ph.D., Department of Neurosurgery, Tufts Medical Center, 800 Washington Street, Boston, Massachusetts 02111. email: amalek@tuftsmedicalcenter.org.

Please include this information when citing this paper: published online January 13, 2012; DOI: 10.3171/2011.11.JNS11311.

  • 1

    Asari S, & Ohmoto T: Natural history and risk factors of unruptured cerebral aneurysms. Clin Neurol Neurosurg 95:205214, 1993

  • 2

    Baharoglu MI, , Schirmer CM, , Hoit DA, , Gao BL, & Malek AM: Aneurysm inflow-angle as a discriminant for rupture in sidewall cerebral aneurysms: morphometric and computational fluid dynamic analysis. Stroke 41:14231430, 2010

    • Search Google Scholar
    • Export Citation
  • 3

    Beck J, , Rohde S, , Berkefeld J, , Seifert V, & Raabe A: Size and location of ruptured and unruptured intracranial aneurysms measured by 3-dimensional rotational angiography. Surg Neurol 65:1827, 2006

    • Search Google Scholar
    • Export Citation
  • 4

    Broderick JP, , Brott TG, , Duldner JE, , Tomsick T, & Leach A: Initial and recurrent bleeding are the major causes of death following subarachnoid hemorrhage. Stroke 25:13421347, 1994

    • Search Google Scholar
    • Export Citation
  • 5

    Cebral JR, , Mut F, , Weir J, & Putman C: Quantitative characterization of the hemodynamic environment in ruptured and unruptured brain aneurysms. AJNR Am J Neuroradiol 32:145151, 2011

    • Search Google Scholar
    • Export Citation
  • 6

    Dhar S, , Tremmel M, , Mocco J, , Kim M, , Yamamoto J, & Siddiqui AH, : Morphology parameters for intracranial aneurysm rupture risk assessment. Neurosurgery 63:185197, 2008

    • Search Google Scholar
    • Export Citation
  • 7

    Fogelholm R, , Hernesniemi J, & Vapalahti M: Impact of early surgery on outcome after aneurysmal subarachnoid hemorrhage. A population-based study. Stroke 24:16491654, 1993

    • Search Google Scholar
    • Export Citation
  • 8

    Forget TR Jr, , Benitez R, , Veznedaroglu E, , Sharan A, , Mitchell W, & Silva M, : A review of size and location of ruptured intracranial aneurysms. Neurosurgery 49:13221326, 2001

    • Search Google Scholar
    • Export Citation
  • 9

    Foutrakis GN, , Yonas H, & Sclabassi RJ: Saccular aneurysm formation in curved and bifurcating arteries. AJNR Am J Neuroradiol 20:13091317, 1999

    • Search Google Scholar
    • Export Citation
  • 10

    Griffith TM, & Edwards DH: Basal EDRF activity helps to keep the geometrical configuration of arterial bifurcations close to the Murray optimum. J Theor Biol 146:545573, 1990

    • Search Google Scholar
    • Export Citation
  • 11

    Hassan T, , Timofeev EV, , Saito T, , Shimizu H, , Ezura M, & Matsumoto Y, : A proposed parent vessel geometry-based categorization of saccular intracranial aneurysms: computational flow dynamics analysis of the risk factors for lesion rupture. J Neurosurg 103:662680, 2005

    • Search Google Scholar
    • Export Citation
  • 12

    Hoh BL, , Sistrom CL, , Firment CS, , Fautheree GL, , Velat GJ, & Whiting JH, : Bottleneck factor and height-width ratio: association with ruptured aneurysms in patients with multiple cerebral aneurysms. Neurosurgery 61:716723, 2007

    • Search Google Scholar
    • Export Citation
  • 13

    International Study of Unruptured Intracranial Aneurysms Investigators: Unruptured intracranial aneurysms—risk of rupture and risks of surgical intervention. N Engl J Med 339:17251733, 1998

    • Search Google Scholar
    • Export Citation
  • 14

    Juvela S, , Porras M, & Heiskanen O: Natural history of unruptured intracranial aneurysms: a long-term follow-up study. J Neurosurg 79:174182, 1993

    • Search Google Scholar
    • Export Citation
  • 15

    Juvela S, , Porras M, & Poussa K: Natural history of unruptured intracranial aneurysms: probability of and risk factors for aneurysm rupture. J Neurosurg 93:379387, 2000

    • Search Google Scholar
    • Export Citation
  • 16

    Kataoka K, , Taneda M, , Asai T, & Yamada Y: Difference in nature of ruptured and unruptured cerebral aneurysms. Lancet 355:203, 2000. (Letter)

    • Search Google Scholar
    • Export Citation
  • 17

    Kupersmith MJ, , Hurst R, , Berenstein A, , Choi IS, , Jafar J, & Ransohoff J: The benign course of cavernous carotid artery aneurysms. J Neurosurg 77:690693, 1992

    • Search Google Scholar
    • Export Citation
  • 18

    Lanzer P, & Topol EJ: PanVascular Medicine: Integrated Clinical Management Berlin, Springer-Verlag, 2002

  • 19

    Prestigiacomo CJ, , He W, , Catrambone J, , Chung S, , Kasper L, & Pasupuleti L, : Predicting aneurysm rupture probabilities through the application of a computed tomography angiography–derived binary logistic regression model. Clinical article. J Neurosurg 110:16, 2009

    • Search Google Scholar
    • Export Citation
  • 20

    Raghavan ML, , Ma B, & Harbaugh RE: Quantified aneurysm shape and rupture risk. J Neurosurg 102:355362, 2005

  • 21

    Rahman M, , Ogilvy CS, , Zipfel GJ, , Derdeyn CP, , Siddiqui AH, & Bulsara KR, : Unruptured cerebral aneurysms do not shrink when they rupture: multicenter collaborative aneurysm study group. Neurosurgery 68:155161, 2011

    • Search Google Scholar
    • Export Citation
  • 22

    Rahman M, , Smietana J, , Hauck E, , Hoh B, , Hopkins N, & Siddiqui A, : Size ratio correlates with intracranial aneurysm rupture status: a prospective study. Stroke 41:916920, 2010

    • Search Google Scholar
    • Export Citation
  • 23

    Sadatomo T, , Yuki K, , Migita K, , Taniguchi E, , Kodama Y, & Kurisu K: Morphological differences between ruptured and unruptured cases in middle cerebral artery aneurysms. Neurosurgery 62:602609, 2008

    • Search Google Scholar
    • Export Citation
  • 24

    Ujiie H, , Tachibana H, , Hiramatsu O, , Hazel AL, , Matsumoto T, & Ogasawara Y, : Effects of size and shape (aspect ratio) on the hemodynamics of saccular aneurysms: a possible index for surgical treatment of intracranial aneurysms. Neurosurgery 45:119130, 1999

    • Search Google Scholar
    • Export Citation
  • 25

    Ujiie H, , Tamano Y, , Sasaki K, & Hori T: Is the aspect ratio a reliable index for predicting the rupture of a saccular aneurysm?. Neurosurgery 48:495503, 2001

    • Search Google Scholar
    • Export Citation
  • 26

    van Gijn J, , Kerr RS, & Rinkel GJE: Subarachnoid haemorrhage. Lancet 369:306318, 2007

  • 27

    Vernooij MW, , Ikram MA, , Tanghe HL, , Vincent AJ, , Hofman A, & Krestin GP, : Incidental findings on brain MRI in the general population. N Engl J Med 357:18211828, 2007

    • Search Google Scholar
    • Export Citation
  • 28

    Wardlaw JM, & White PM: The detection and management of unruptured intracranial aneurysms. Brain 123:205221, 2000

  • 29

    Wiebers DO: Patients with small, asymptomatic, unruptured intracranial aneurysms and no history of subarachnoid hemorrhage should generally be treated conservatively: for. Stroke 36:408409, 2005

    • Search Google Scholar
    • Export Citation
  • 30

    Wiebers DO, , Whisnant JP, , Huston J III, , Meissner I, , Brown RD Jr, & Piepgras DG, : Unruptured intracranial aneurysms: natural history, clinical outcome, and risks of surgical and endovascular treatment. Lancet 362:103110, 2003

    • Search Google Scholar
    • Export Citation
  • 31

    Wiebers DO, , Whisnant JP, & O'Fallon WM: The natural history of unruptured intracranial aneurysms. N Engl J Med 304:696698, 1981

  • 32

    Wiebers DO, , Whisnant JP, , Sundt TM Jr, & O'Fallon WM: The significance of unruptured intracranial saccular aneurysms. J Neurosurg 66:2329, 1987

    • Search Google Scholar
    • Export Citation
  • 33

    Winn HR, , Almaani WS, , Berga SL, , Jane JA, & Richardson AE: The long-term outcome in patients with multiple aneurysms. Incidence of late hemorrhage and implications for treatment of incidental aneurysms. J Neurosurg 59:642651, 1983

    • Search Google Scholar
    • Export Citation
  • 34

    Womersley JR: Method for the calculation of velocity, rate of flow and viscous drag in arteries when the pressure gradient is known. J Physiol 127:553563, 1955

    • Search Google Scholar
    • Export Citation
  • 35

    Xiang J, , Natarajan SK, , Tremmel M, , Ma D, , Mocco J, & Hopkins LN, : Hemodynamic-morphologic discriminants for intracranial aneurysm rupture. Stroke 42:144152, 2011

    • Search Google Scholar
    • Export Citation
  • 36

    Yasui N, , Magarisawa S, , Suzuki A, , Nishimura H, , Okudera T, & Abe T: Subarachnoid hemorrhage caused by previously diagnosed, previously unruptured intracranial aneurysms: a retrospective analysis of 25 cases. Neurosurgery 39:10961101, 1996

    • Search Google Scholar
    • Export Citation

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