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Published in: Journal of Neuro-Oncology 3/2017

01-12-2017 | Clinical Study

Correlation between arterial spin-labeling perfusion and histopathological vascular density of pediatric intracranial tumors

Authors: Kazufumi Kikuchi, Akio Hiwatashi, Osamu Togao, Koji Yamashita, Koji Yoshimoto, Masahiro Mizoguchi, Satoshi O. Suzuki, Toru Iwaki, Yuriko Suzuki, Hiroshi Honda

Published in: Journal of Neuro-Oncology | Issue 3/2017

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Abstract

Traditional MRI methods for estimation of blood flow in brain tumors require high-flow injection of contrast agents through large-bore intravenous access, which limits their pediatric utility. In contrast, arterial spin-labeling (ASL) can be used without contrast media. This study aimed to evaluate the relationship between tumor blood flow (TBF) measured by ASL and histopathological vascular density in pediatric brain tumors. Nineteen consecutive children were evaluated (10 boys, 9 girls; median age: 6 years; 8 high-grade and 11 low-grade tumors). ASL was performed with a pseudocontinuous labeling time of 1650 ms and post-labeling delay of 1525 ms. The maximal absolute (aTBF) and relative (rTBF) tumor blood flows were measured. To evaluate the relative vascular area (%Vessel), the total stained vascular area was divided by the whole tissue area. Spearman’s rank-order correlation, the Mann–Whitney U test, and receiver operating characteristic analysis were used for statistical analysis. The absolute and relative TBF rates were 4.9–92.9 mL/100 g/min and 0.17–3.59 mL/100 g/min, respectively. The %Vessel was 0.6–30.2%. The %Vessel showed a significant positive correlation with TBF (aTBF: r = 0.87, P < 0.0001; rTBF: r = 0.89, P < 0.0001). The TBF rate of high-grade tumors was significantly higher than that of low-grade tumors (aTBF: P = 0.0050, rTBF: P = 0.0036). The rTBF had the best diagnostic performance (area under the curve: 0.89). ASL perfusion imaging without contrast material can be used for accurate evaluation of histopathological vascular density and may be helpful for tumor grading in children.
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Literature
1.
go back to reference Bleyer WA (1990) The impact of childhood cancer on the United States and the world. CA Cancer J Clin 40:355–367CrossRefPubMed Bleyer WA (1990) The impact of childhood cancer on the United States and the world. CA Cancer J Clin 40:355–367CrossRefPubMed
3.
go back to reference Sugahara T, Korogi Y, Kochi M, Ikushima I, Hirai T, Okuda T, Shigematsu Y, Liang L, Ge Y, Ushio Y, Takahashi M (1998) Correlation of MR imaging-determined cerebral blood volume maps with histologic and angiographic determination of vascularity of gliomas. Am J Roentgenol 171:1479–1486. doi:10.2214/ajr.171.6.9843274 CrossRef Sugahara T, Korogi Y, Kochi M, Ikushima I, Hirai T, Okuda T, Shigematsu Y, Liang L, Ge Y, Ushio Y, Takahashi M (1998) Correlation of MR imaging-determined cerebral blood volume maps with histologic and angiographic determination of vascularity of gliomas. Am J Roentgenol 171:1479–1486. doi:10.​2214/​ajr.​171.​6.​9843274 CrossRef
5.
go back to reference Tzika AA, Astrakas LG, Zarifi MK, Zurakowski D, Poussaint TY, Goumnerova L, Tarbell NJ, Black PM (2004) Spectroscopic and perfusion magnetic resonance imaging predictors of progression in pediatric brain tumors. Cancer 100:1246–1256. doi:10.1002/cncr.20096 CrossRefPubMed Tzika AA, Astrakas LG, Zarifi MK, Zurakowski D, Poussaint TY, Goumnerova L, Tarbell NJ, Black PM (2004) Spectroscopic and perfusion magnetic resonance imaging predictors of progression in pediatric brain tumors. Cancer 100:1246–1256. doi:10.​1002/​cncr.​20096 CrossRefPubMed
7.
go back to reference Lobel U, Sedlacik J, Reddick WE, Kocak M, Ji Q, Broniscer A, Hillenbrand CM, Patay Z (2011) Quantitative diffusion-weighted and dynamic susceptibility-weighted contrast-enhanced perfusion MR imaging analysis of T2 hypointense lesion components in pediatric diffuse intrinsic pontine glioma. Am J Neuroradiol 32:315–322. doi:10.3174/ajnr.A2277 CrossRefPubMed Lobel U, Sedlacik J, Reddick WE, Kocak M, Ji Q, Broniscer A, Hillenbrand CM, Patay Z (2011) Quantitative diffusion-weighted and dynamic susceptibility-weighted contrast-enhanced perfusion MR imaging analysis of T2 hypointense lesion components in pediatric diffuse intrinsic pontine glioma. Am J Neuroradiol 32:315–322. doi:10.​3174/​ajnr.​A2277 CrossRefPubMed
10.
go back to reference 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. Am J Neuroradiol 27:85–93PubMed 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. Am J Neuroradiol 27:85–93PubMed
11.
go back to reference Warmuth C, Gunther M, Zimmer C (2003) Quantification of blood flow in brain tumors: comparison of arterial spin labeling and dynamic susceptibility-weighted contrast-enhanced MR imaging. Radiology 228:523–532. doi:10.1148/radiol.2282020409 CrossRefPubMed Warmuth C, Gunther M, Zimmer C (2003) Quantification of blood flow in brain tumors: comparison of arterial spin labeling and dynamic susceptibility-weighted contrast-enhanced MR imaging. Radiology 228:523–532. doi:10.​1148/​radiol.​2282020409 CrossRefPubMed
12.
go back to reference Jarnum H, Steffensen EG, Knutsson L, Frund ET, Simonsen CW, Lundbye-Christensen S, Shankaranarayanan A, Alsop DC, Jensen FT, Larsson EM (2010) Perfusion MRI of brain tumours: a comparative study of pseudo-continuous arterial spin labelling and dynamic susceptibility contrast imaging. Neuroradiology 52:307–317. doi:10.1007/s00234-009-0616-6 CrossRefPubMed Jarnum H, Steffensen EG, Knutsson L, Frund ET, Simonsen CW, Lundbye-Christensen S, Shankaranarayanan A, Alsop DC, Jensen FT, Larsson EM (2010) Perfusion MRI of brain tumours: a comparative study of pseudo-continuous arterial spin labelling and dynamic susceptibility contrast imaging. Neuroradiology 52:307–317. doi:10.​1007/​s00234-009-0616-6 CrossRefPubMed
13.
go back to reference Wolf RL, Wang J, Wang S, Melhem ER, O’Rourke DM, Judy KD, Detre JA (2005) Grading of CNS neoplasms using continuous arterial spin labeled perfusion MR imaging at 3 T. J Magn Reson Imaging 22:475–482. doi:10.1002/jmri.20415 CrossRefPubMed Wolf RL, Wang J, Wang S, Melhem ER, O’Rourke DM, Judy KD, Detre JA (2005) Grading of CNS neoplasms using continuous arterial spin labeled perfusion MR imaging at 3 T. J Magn Reson Imaging 22:475–482. doi:10.​1002/​jmri.​20415 CrossRefPubMed
14.
go back to reference Yamashita K, Yoshiura T, Hiwatashi A, Togao O, Yoshimoto K, Suzuki SO, Abe K, Kikuchi K, Maruoka Y, Mizoguchi M, Iwaki T, Honda H (2013) Differentiating primary CNS lymphoma from glioblastoma multiforme: assessment using arterial spin labeling, diffusion-weighted imaging, and (1)(8)F-fluorodeoxyglucose positron emission tomography. Neuroradiology 55:135–143. doi:10.1007/s00234-012-1089-6 CrossRefPubMed Yamashita K, Yoshiura T, Hiwatashi A, Togao O, Yoshimoto K, Suzuki SO, Abe K, Kikuchi K, Maruoka Y, Mizoguchi M, Iwaki T, Honda H (2013) Differentiating primary CNS lymphoma from glioblastoma multiforme: assessment using arterial spin labeling, diffusion-weighted imaging, and (1)(8)F-fluorodeoxyglucose positron emission tomography. Neuroradiology 55:135–143. doi:10.​1007/​s00234-012-1089-6 CrossRefPubMed
16.
go back to reference Louis D, Ohgaki H, Wiestler O, Cavenee W, Ellison D, Figarella-Branger D, Perry A, Reifenberger G, von Deimling A (2016) WHO classification of tumours of the central nervous system, revised. IARC Press, Lyon Louis D, Ohgaki H, Wiestler O, Cavenee W, Ellison D, Figarella-Branger D, Perry A, Reifenberger G, von Deimling A (2016) WHO classification of tumours of the central nervous system, revised. IARC Press, Lyon
17.
go back to reference Alsop DC, Detre JA, Golay X, Gunther M, Hendrikse J, Hernandez-Garcia L, Lu H, MacIntosh BJ, Parkes LM, Smits M, van Osch MJ, Wang DJ, Wong EC, Zaharchuk G (2015) Recommended implementation of arterial spin-labeled perfusion MRI for clinical applications: A consensus of the ISMRM perfusion study group and the European consortium for ASL in dementia. Magn Reson Med 73:102–116. doi:10.1002/mrm.25197 CrossRefPubMed Alsop DC, Detre JA, Golay X, Gunther M, Hendrikse J, Hernandez-Garcia L, Lu H, MacIntosh BJ, Parkes LM, Smits M, van Osch MJ, Wang DJ, Wong EC, Zaharchuk G (2015) Recommended implementation of arterial spin-labeled perfusion MRI for clinical applications: A consensus of the ISMRM perfusion study group and the European consortium for ASL in dementia. Magn Reson Med 73:102–116. doi:10.​1002/​mrm.​25197 CrossRefPubMed
20.
go back to reference DeLong ER, DeLong DM, Clarke-Pearson DL (1988) Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 44:837–845CrossRefPubMed DeLong ER, DeLong DM, Clarke-Pearson DL (1988) Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 44:837–845CrossRefPubMed
21.
22.
go back to reference Noguchi T, Yoshiura T, Hiwatashi A, Togao O, Yamashita K, Kobayashi K, Mihara F, Honda H (2007) Quantitative perfusion imaging with pulsed arterial spin labeling: a phantom study. Magn Reson Med Sci 6:91–97CrossRefPubMed Noguchi T, Yoshiura T, Hiwatashi A, Togao O, Yamashita K, Kobayashi K, Mihara F, Honda H (2007) Quantitative perfusion imaging with pulsed arterial spin labeling: a phantom study. Magn Reson Med Sci 6:91–97CrossRefPubMed
23.
go back to reference Dangouloff-Ros V, Deroulers C, Foissac F, Badoual M, Shotar E, Grevent D, Calmon R, Pages M, Grill J, Dufour C, Blauwblomme T, Puget S, Zerah M, Sainte-Rose C, Brunelle F, Varlet P, Boddaert N (2016) Arterial spin labeling to predict brain tumor grading in children: correlations between histopathologic vascular density and perfusion MR imaging. Radiology 281:553–566. doi:10.1148/radiol.2016152228 CrossRefPubMed Dangouloff-Ros V, Deroulers C, Foissac F, Badoual M, Shotar E, Grevent D, Calmon R, Pages M, Grill J, Dufour C, Blauwblomme T, Puget S, Zerah M, Sainte-Rose C, Brunelle F, Varlet P, Boddaert N (2016) Arterial spin labeling to predict brain tumor grading in children: correlations between histopathologic vascular density and perfusion MR imaging. Radiology 281:553–566. doi:10.​1148/​radiol.​2016152228 CrossRefPubMed
24.
go back to reference Tural S, Gercek A, Konya D, Ozgen S, Toplamoglu H, Ozek MM (2009) Microvessel density and vascular endothelial growth factor expression as predictors of childrens’ survival from cerebellar medulloblastoma. J Clin Neurosci 16:1199–1202. doi:10.1016/j.jocn.2008.10.026 CrossRefPubMed Tural S, Gercek A, Konya D, Ozgen S, Toplamoglu H, Ozek MM (2009) Microvessel density and vascular endothelial growth factor expression as predictors of childrens’ survival from cerebellar medulloblastoma. J Clin Neurosci 16:1199–1202. doi:10.​1016/​j.​jocn.​2008.​10.​026 CrossRefPubMed
25.
go back to reference Guo Y, Cai YQ, Cai ZL, Gao YG, An NY, Ma L, Mahankali S, Gao JH (2002) Differentiation of clinically benign and malignant breast lesions using diffusion-weighted imaging. J Magn Reson Imaging 16:172–178. doi:10.1002/jmri.10140 CrossRefPubMed Guo Y, Cai YQ, Cai ZL, Gao YG, An NY, Ma L, Mahankali S, Gao JH (2002) Differentiation of clinically benign and malignant breast lesions using diffusion-weighted imaging. J Magn Reson Imaging 16:172–178. doi:10.​1002/​jmri.​10140 CrossRefPubMed
26.
27.
go back to reference Risberg J, Ancri D, Ingvar DH (1969) Correlation between cerebral blood volume and cerebral blood flow in the cat. Exp Brain Res 8:321–326CrossRefPubMed Risberg J, Ancri D, Ingvar DH (1969) Correlation between cerebral blood volume and cerebral blood flow in the cat. Exp Brain Res 8:321–326CrossRefPubMed
29.
go back to reference Wolf RL, Alsop DC, McGarvey ML, Maldjian JA, Wang J, Detre JA (2003) Susceptibility contrast and arterial spin labeled perfusion MRI in cerebrovascular disease. J Neuroimaging 13:17–27CrossRefPubMed Wolf RL, Alsop DC, McGarvey ML, Maldjian JA, Wang J, Detre JA (2003) Susceptibility contrast and arterial spin labeled perfusion MRI in cerebrovascular disease. J Neuroimaging 13:17–27CrossRefPubMed
30.
go back to reference Catafau AM (2001) Brain SPECT in clinical practice. Part I: perfusion. J Nucl Med 42:259–271PubMed Catafau AM (2001) Brain SPECT in clinical practice. Part I: perfusion. J Nucl Med 42:259–271PubMed
Metadata
Title
Correlation between arterial spin-labeling perfusion and histopathological vascular density of pediatric intracranial tumors
Authors
Kazufumi Kikuchi
Akio Hiwatashi
Osamu Togao
Koji Yamashita
Koji Yoshimoto
Masahiro Mizoguchi
Satoshi O. Suzuki
Toru Iwaki
Yuriko Suzuki
Hiroshi Honda
Publication date
01-12-2017
Publisher
Springer US
Published in
Journal of Neuro-Oncology / Issue 3/2017
Print ISSN: 0167-594X
Electronic ISSN: 1573-7373
DOI
https://doi.org/10.1007/s11060-017-2604-8

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