Assessment of image-derived risk factors for natural course of unruptured cerebral aneurysms

Manasi Ramachandran Department of Biomedical Engineering, University of Iowa;

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Rohini Retarekar Department of Biomedical Engineering, University of Iowa;

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Madhavan L. Raghavan Department of Biomedical Engineering, University of Iowa;

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Benjamin Berkowitz Department of Biomedical Engineering, University of Iowa;

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Benjamin Dickerhoff Department of Biomedical Engineering, University of Iowa;

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Tatiana Correa Department of Biomedical Engineering, University of Iowa;

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Steve Lin Department of Biomedical Engineering, University of Iowa;

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Kevin Johnson Department of Neurosurgery, University of Iowa Hospitals and Clinics; and

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David Hasan Department of Neurosurgery, University of Iowa Hospitals and Clinics; and

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Christopher Ogilvy Department of Surgery, Division of Neurosurgery, Beth Israel Deaconess Medical Center; and

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Robert Rosenwasser Department of Neurosurgery, Jefferson University Hospital, Philadelphia;

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James Torner Department of Epidemiology, University of Iowa, Iowa City, Iowa;

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Einar Bogason Department of Neurosurgery, Penn State University, Hershey; and

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Christopher J. Stapleton Department of Neurosurgery, Massachusetts General Hospital, Boston, Massachusetts;

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Robert E. Harbaugh Department of Neurosurgery, Penn State University, Hershey; and
Department of Engineering Science and Mechanics, Pennsylvania State University, State College, Pennsylvania

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OBJECT

The goal of this prospective longitudinal study was to test whether image-derived metrics can differentiate unruptured aneurysms that will become unstable (grow and/or rupture) from those that will remain stable.

METHODS

One hundred seventy-eight patients harboring 198 unruptured cerebral aneurysms for whom clinical observation and follow-up with imaging surveillance was recommended at 4 clinical centers were prospectively recruited into this study. Imaging data (predominantly CT angiography) at initial presentation was recorded. Computational geometry was used to estimate numerous metrics of aneurysm morphology that described the size and shape of the aneurysm. The nonlinear, finite element method was used to estimate uniform pressure-induced peak wall tension. Computational fluid dynamics was used to estimate blood flow metrics. The median follow-up period was 645 days. Longitudinal outcome data on these aneurysm patients—whether their aneurysms grew or ruptured (the unstable group) or remained unchanged (the stable group)—was documented based on follow-up at 4 years after the beginning of recruitment.

RESULTS

Twenty aneurysms (10.1%) grew, but none ruptured. One hundred forty-nine aneurysms (75.3%) remained stable and 29 (14.6%) were lost to follow-up. None of the metrics—including aneurysm size, nonsphericity index, peak wall tension, and low shear stress area—differentiated the stable from unstable groups with statistical significance.

CONCLUSIONS

The findings in this highly selected group do not support the hypothesis that image-derived metrics can predict aneurysm growth in patients who have been selected for observation and imaging surveillance. If aneurysm shape is a significant determinant of invasive versus expectant management, selection bias is a key limitation of this study.

ABBREVIATIONS

CE = contrast enhanced; CTA = CT angiography; Dmax = maximum diameter; LSA = low shear area; MRA = MR angiography; NSI = nonsphericity index; PWT = peak wall tension; TOF = time of flight.
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  • 1

    Antiga L, , Ene-Iordache B, , Caverni L, , Cornalba GP, & Remuzzi A: Geometric reconstruction for computational mesh generation of arterial bifurcations from CT angiography. Comput Med Imaging Graph 26:227235, 2002

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Antiga L, , Ene-Iordache B, & Remuzzi A: Computational geometry for patient-specific reconstruction and meshing of blood vessels from MR and CT angiography. IEEE Trans Med Imaging 22:674684, 2003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Bacigaluppi S, , Piccinelli M, , Antiga L, , Veneziani A, , Passerini T, & Rampini P, et al.: Factors affecting formation and rupture of intracranial saccular aneurysms. Neurosurg Rev 37:114, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

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

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Boussel L, , Rayz V, , McCulloch C, , Martin A, , Acevedo-Bolton G, & Lawton M, et al.: Aneurysm growth occurs at region of low wall shear stress: patient-specific correlation of hemodynamics and growth in a longitudinal study. Stroke 39:29973002, 2008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Cebral JR, , Castro MA, , Burgess JE, , Pergolizzi RS, , Sheridan MJ, & Putman CM: Characterization of cerebral aneurysms for assessing risk of rupture by using patient-specific computational hemodynamics models. AJNR Am J Neuroradiol 26:25502559, 2005

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    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

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

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

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Fillinger MF, , Marra SP, , Raghavan ML, & Kennedy FE: Prediction of rupture risk in abdominal aortic aneurysm during observation: wall stress versus diameter. J Vasc Surg 37:724732, 2003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Ford MD, , Alperin N, , Lee SH, , Holdsworth DW, & Steinman DA: Characterization of volumetric flow rate waveforms in the normal internal carotid and vertebral arteries. Physiol Meas 26:477488, 2005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Ford MD, , Hoi Y, , Piccinelli M, , Antiga L, & Steinman DA: An objective approach to digital removal of saccular aneurysms: technique and applications. Br J Radiol 82:S55S61, 2009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Jou LD, , Lee DH, , Morsi H, & Mawad ME: Wall shear stress on ruptured and unruptured intracranial aneurysms at the internal carotid artery. AJNR Am J Neuroradiol 29:17611767, 2008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Laaksamo E, , Ramachandran M, , Frösen J, , Tulamo R, , Baumann M, & Friedlander RM, et al.: Intracellular signaling pathways and size, shape, and rupture history of human intracranial aneurysms. Neurosurgery 70:15651573, 2012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Lauric A, , Hippelheuser J, , Cohen AD, , Kadasi LM, & Malek AM: Wall shear stress association with rupture status in volume matched sidewall aneurysms. J Neurointerv Surg 6:466473, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Lauric A, , Miller EL, , Baharoglu MI, & Malek AM: 3D shape analysis of intracranial aneurysms using the writhe number as a discriminant for rupture. Ann Biomed Eng 39:14571469, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Lauric A, , Miller EL, , Baharoglu MI, & Malek AM: Rupture status discrimination in intracranial aneurysms using the centroid-radii model. IEEE Trans Biomed Eng 58:28952903, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Ma B, , Harbaugh RE, & Raghavan ML: Three-dimensional geometrical characterization of cerebral aneurysms. Ann Biomed Eng 32:264273, 2004

  • 18

    Ma B, , Lu J, , Harbaugh RE, & Raghavan ML: Nonlinear anisotropic stress analysis of anatomically realistic cerebral aneurysms. J Biomech Eng 129:8896, 2007

  • 19

    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 366:24742482, 2012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Piccinelli M, , Steinman DA, , Hoi Y, , Tong F, , Veneziani A, & Antiga L: Automatic neck plane detection and 3D geometric characterization of aneurysmal sacs. Ann Biomed Eng 40:21882211, 2012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Piccinelli M, , Veneziani A, , Steinman DA, , Remuzzi A, & Antiga L: A framework for geometric analysis of vascular structures: application to cerebral aneurysms. IEEE Trans Med Imaging 28:11411155, 2009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Qian Y, , Takao H, , Umezu M, & Murayama Y: Risk analysis of unruptured aneurysms using computational fluid dynamics technology: preliminary results. AJNR Am J Neuroradiol 32:19481955, 2011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

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

  • 24

    Ramachandran M: On the Role of Intracranial Aneurysm Morphology in Stable Versus Unstable Lesions [dissertaton] Iowa City, IA, University of Iowa, 2012

  • 25

    Ramachandran M, , Laakso A, , Harbaugh RE, & Raghavan ML: On the role of modeling choices in estimation of cerebral aneurysm wall tension. J Biomech 45:29142919, 2012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Ramachandran M, , Retarekar R, , Harbaugh RE, , Hasan D, , Policeni B, & Rosenwasser R, et al.: Sensitivity of quantified intracranial aneurysm geometry to imaging modality. Cardiovasc Eng Technol 4:7586, 2013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Retarekar R: Hemodynamics and Natural History Outcome in Unruptured Intracranial Aneurysms [dissertation] Iowa City, IA, University of Iowa, 2012

  • 28

    Retarekar R, , Ramachandran M, , Berkowitz B, , Harbaugh RE, , Hasan D, & Rosenwasser RH, et al.: Stratification of a population of intracranial aneurysms using blood flow metrics. Comput Methods Biomech Biomed Engin 18:10721082, 2015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Saloner D, , Martin A, , Hurwit D, , Sohrabi S, , Lee A, & Rayz V, et al.: MRI/A in the evaluation of changes over time in untreated aneurysms. Proc Intl Soc Mag Reson Med 21:2995, 2013. (Abstract)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Shapiro SS, & Wilk MB: An analysis of variance test for normality (complete samples). Biometrika 52:591611, 1965

  • 31

    Shojima M, , Oshima M, , Takagi K, , Torii R, , Hayakawa M, & Katada K, et al.: Magnitude and role of wall shear stress on cerebral aneurysm: computational fluid dynamic study of 20 middle cerebral artery aneurysms. Stroke 35:25002505, 2004

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Takao H, , Murayama Y, , Otsuka S, , Qian Y, , Mohamed A, & Masuda S, et al.: Hemodynamic differences between unruptured and ruptured intracranial aneurysms during observation. Stroke 43:14361439, 2012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Tremmel M, , Dhar S, , Levy EI, , Mocco J, & Meng H: Influence of intracranial aneurysm-to-parent vessel size ratio on hemodynamics and implication for rupture: results from a virtual experimental study. Neurosurgery 64:622631, 2009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Valen-Sendstad K, , Piccinelli M, & Steinman DA: High-resolution computational fluid dynamics detects flow instabilities in the carotid siphon: implications for aneurysm initiation and rupture?. J Biomech 47:32103216, 2014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Valencia C, , Villa-Uriol MC, , Pozo JM, & Frangi AF: Morphological descriptors as rupture indicators in middle cerebral artery aneurysms. Conf Proc IEEE Eng Med Biol Soc 2012:60466049, 2010

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

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

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37

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

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