Abstract
Digital subtraction angiography (DSA) assesses the necessity of preoperative embolization in meningioma cases but entails complication risks. Previous studies evaluating meningiomas’ angiographic vascularity using perfusion-weighted imaging (PWI) have performed subjective visual assessments, not managing to assess the need for preoperative embolization. We objectively assessed the angiographic stain of meningiomas and examined the usefulness of two parameters of dynamic susceptibility contrast (DSC)-PWI, normalized cerebral blood volume (nCBV) and cerebral blood flow (nCBF), in predicting vascularity and the necessity of preoperative embolization. We retrospectively examined 52 patients who underwent surgery for primary meningioma and preoperative DSA and DSC-PWI. We calculated the normalized luminance (nLum) of the tumor stain in DSA. In 29 meningioma cases with a single feeding artery, we determined the DSC-PWI parameter that correlated with meningioma angiographic vascularity and predicted the necessity of preoperative embolization. We also compared vascularity between meningiomas with single and multiple feeding arteries and between convexity and skull-base meningiomas. nCBF (cut off: 3.66, P = 0.03, area under the curve [AUC] = 0.80) alone could predict the necessity of preoperative embolization and was more significantly correlated with the nLum than nCBV (P = 0.08, AUC = 0.73). Vascularity did not differ between meningiomas with single and multiple feeding arteries; skull-base meningiomas were more vascularized than convexity meningiomas (P = 0.0027). Our objective, quantitative assessments revealed nCBF as the most suitable parameter for evaluating meningioma vascularity. Tumor vascularity assessment using nCBF values and CBF images may aid predicting the necessity of preoperative DSA.
Similar content being viewed by others
References
Adachi K, Hayakawa M, Ishihara K, Ganaha T, Nagahisa S, Hasegawa M, Hirose Y (2016) Study of changing intracranial venous drainage patterns in petroclival meningioma. World Neurosurg 92:339–348. https://doi.org/10.1016/j.wneu.2016.05.019
Adachi K, Hayakawa M, Sadato A, Hayashi T, Maeda S, Nagahisa S, Hasegawa M (2016) Modified balloon protection technique for preoperative embolization of feeder arteries from internal carotid artery branches to skull-base tumor: technical note. J Neurol Surg A Cent Eur Neurosurg 77:161–166. https://doi.org/10.1055/s-0034-1543961
Adachi K, Hasegawa M, Hirose Y (2017) Evaluation of venous drainage patterns for skull base meningioma surgery. Neurol Med Chir (Tokyo) 57:505–512. https://doi.org/10.2176/nmc.ra.2016-0336
Adachi K, Hasegawa M, Tateyama S, Kawazoe Y, Hirose Y (2018) Surgical strategy for and anatomic locations of petroapex and petroclival meningiomas based on evaluation of the feeding artery. World Neurosurg 116:e611–e623. https://doi.org/10.1016/j.wneu.2018.05.052
Adachi K, Hasegawa M, Hirose Y (2020) Prediction of trigeminal nerve position based on the main feeding artery in petroclival meningioma. Neurosurg Rev. https://doi.org/10.1007/s10143-020-01313-3
Bitzer M, Opitz H, Popp J, Morgalla M, Gruber A, Heiss E, Voigt K (1998) Angiogenesis and brain oedema in intracranial meningiomas: influence of vascular endothelial growth factor. Acta Neurochir 140:333–340. https://doi.org/10.1007/s007010050106
Boxerman JL, Schmainda KM, Weisskoff RM (2006) Relative cerebral blood volume maps corrected for contrast agent extravasation significantly correlate with glioma tumor grade, whereas uncorrected maps do not. AJNR Am J Neuroradiol 27:859–867
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 30:317–320. https://doi.org/10.1161/01.str.30.2.317
Dawkins AA, Evans AL, Wattam J, Romanowski CA, Connolly DJ, Hodgson TJ, Coley SC (2007) Complications of cerebral angiography: a prospective analysis of 2,924 consecutive procedures. Neuroradiology 49:753–759. https://doi.org/10.1007/s00234-007-0252-y
Ginat DT, Mangla R, Yeaney G, Schaefer PW, Wang H (2012) Correlation between dynamic contrast-enhanced perfusion MRI relative cerebral blood volume and vascular endothelial growth factor expression in meningiomas. Acad Radiol 19:986–990. https://doi.org/10.1016/j.acra.2012.04.006
Heiserman JE, Dean BL, Hodak JA, Flom RA, Bird CR, Drayer BP, Fram EK (1994) Neurologic complications of cerebral angiography. AJNR Am J Neuroradiol 15:1401–1407; discussion 1408-1411
Kimura H, Takeuchi H, Koshimoto Y, Arishima H, Uematsu H, Kawamura Y, Kubota T, Itoh H (2006) Perfusion imaging of meningioma by using continuous arterial spin-labeling: comparison with dynamic susceptibility-weighted contrast-enhanced MR images and histopathologic features. AJNR Am J Neuroradiol 27:85–93
Knopp EA, Cha S, Johnson G, Mazumdar A, Golfinos JG, Zagzag D, Miller DC, Kelly PJ, Kricheff II (1999) Glial neoplasms: dynamic contrast-enhanced T2*-weighted MR imaging. Radiology 211:791–798. https://doi.org/10.1148/radiology.211.3.r99jn46791
Koizumi S, Sakai N, Kawaji H, Takehara Y, Yamashita S, Sakahara H, Baba S, Hiramatsu H, Sameshima T, Namba H (2015) Pseudo-continuous arterial spin labeling reflects vascular density and differentiates angiomatous meningiomas from non-angiomatous meningiomas. J Neuro-Oncol 121:549–556. https://doi.org/10.1007/s11060-014-1666-0
Lu Y, Xiong J, Yin B, Wen J, Liu L, Geng D (2018) The role of three-dimensional pseudo-continuous arterial spin labelling in grading and differentiating histological subgroups of meningiomas. Clin Radiol 73:176–184. https://doi.org/10.1016/j.crad.2017.08.005
Maia AC Jr, Malheiros SM, da Rocha AJ, da Silva CJ, Gabbai AA, Ferraz FA, Stavale JN (2005) MR cerebral blood volume maps correlated with vascular endothelial growth factor expression and tumor grade in nonenhancing gliomas. AJNR Am J Neuroradiol 26:777–783
Raper DM, Starke RM, Henderson F Jr, Ding D, Simon S, Evans AJ, Jane JA Sr, Liu KC (2014) Preoperative embolization of intracranial meningiomas: efficacy, technical considerations, and complications. AJNR Am J Neuroradiol 35:1798–1804. https://doi.org/10.3174/ajnr.A3919
Sughrue ME, Kane AJ, Shangari G, Rutkowski MJ, McDermott MW, Berger MS, Parsa AT (2010) The relevance of Simpson grade I and II resection in modern neurosurgical treatment of World Health Organization grade I meningiomas. J Neurosurg 113:1029–1035. https://doi.org/10.3171/2010.3.Jns091971
Thiex R, Norbash AM, Frerichs KU (2010) The safety of dedicated-team catheter-based diagnostic cerebral angiography in the era of advanced noninvasive imaging. AJNR Am J Neuroradiol 31:230–234. https://doi.org/10.3174/ajnr.A1803
Toh CH, Wei KC, Chang CN, Peng YW, Ng SH, Wong HF, Lin CP (2014) Assessment of angiographic vascularity of meningiomas with dynamic susceptibility contrast-enhanced perfusion-weighted imaging and diffusion tensor imaging. AJNR Am J Neuroradiol 35:263–269. https://doi.org/10.3174/ajnr.A3651
Wanibuchi M, Komatsu K, Akiyama Y, Mikami T, Iihoshi S, Miyata K, Mikuni N (2016) Quantitative assessment of flow reduction after feeder embolization in meningioma by using pseudocontinuous arterial spin labeling. World Neurosurg 93:237–245. https://doi.org/10.1016/j.wneu.2016.06.004
Willinsky RA, Taylor SM, TerBrugge K, Farb RI, Tomlinson G, Montanera W (2003) Neurologic complications of cerebral angiography: prospective analysis of 2,899 procedures and review of the literature. Radiology 227:522–528. https://doi.org/10.1148/radiol.2272012071
Yoo RE, Yun TJ, Cho YD, Rhim JH, Kang KM, Choi SH, Kim JH, Kim JE, Kang HS, Sohn CH, Park SW, Han MH (2016) Utility of arterial spin labeling perfusion magnetic resonance imaging in prediction of angiographic vascularity of meningiomas. J Neurosurg 125:536–543. https://doi.org/10.3171/2015.8.Jns151211
Zhang H, Rodiger LA, Shen T, Miao J, Oudkerk M (2008) Preoperative subtyping of meningiomas by perfusion MR imaging. Neuroradiology 50:835–840. https://doi.org/10.1007/s00234-008-0417-3
Acknowledgments
We would like to thank Editage for proofreading our work.
Funding
Canon provided the Olea Sphere V3.0 for this study.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee (institutional review board at Fujita health university, Protocol Number: HM19-287) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Consent to participate, consent for publication
For this type of study formal consent is not required, and an opt-out method was used for all potential study cases.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Adachi, K., Murayama, K., Hayakawa, M. et al. Objective and quantitative evaluation of angiographic vascularity in meningioma: parameters of dynamic susceptibility contrast-perfusion-weighted imaging as clinical indicators of preoperative embolization. Neurosurg Rev 44, 2629–2638 (2021). https://doi.org/10.1007/s10143-020-01431-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10143-020-01431-y