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

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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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References

  1. Bleyer WA (1990) The impact of childhood cancer on the United States and the world. CA Cancer J Clin 40:355–367

    Article  CAS  PubMed  Google Scholar 

  2. Pollack IF (1994) Brain tumors in children. N Engl J Med 331:1500–1507. doi:10.1056/NEJM199412013312207

    Article  CAS  PubMed  Google Scholar 

  3. 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

    Article  CAS  Google Scholar 

  4. Cha S (2006) Dynamic susceptibility-weighted contrast-enhanced perfusion MR imaging in pediatric patients. Neuroimaging Clin N Am 16:137–147. doi:10.1016/j.nic.2005.11.006 ix

    Article  PubMed  Google Scholar 

  5. 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

    Article  PubMed  Google Scholar 

  6. Thompson EM, Guillaume DJ, Dosa E, Li X, Nazemi KJ, Gahramanov S, Hamilton BE, Neuwelt EA (2012) Dual contrast perfusion MRI in a single imaging session for assessment of pediatric brain tumors. J Neurooncol 109:105–114. doi:10.1007/s11060-012-0872-x

    Article  PubMed  PubMed Central  Google Scholar 

  7. 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

    Article  CAS  PubMed  Google Scholar 

  8. Kanda T, Nakai Y, Oba H, Toyoda K, Kitajima K, Furui S (2016) Gadolinium deposition in the brain. Magn Reson Imaging 34:1346–1350. doi:10.1016/j.mri.2016.08.024

    Article  CAS  PubMed  Google Scholar 

  9. Dai W, Garcia D, de Bazelaire C, Alsop DC (2008) Continuous flow-driven inversion for arterial spin labeling using pulsed radio frequency and gradient fields. Magn Reson Med 60:1488–1497. doi:10.1002/mrm.21790

    Article  PubMed  PubMed Central  Google Scholar 

  10. 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 27:85–93

    CAS  PubMed  Google Scholar 

  11. 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

    Article  PubMed  Google Scholar 

  12. 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

    Article  PubMed  Google Scholar 

  13. 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

    Article  PubMed  Google Scholar 

  14. 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

    Article  PubMed  Google Scholar 

  15. Yeom KW, Mitchell LA, Lober RM, Barnes PD, Vogel H, Fisher PG, Edwards MS (2014) Arterial spin-labeled perfusion of pediatric brain tumors. Am J Neuroradiol 35:395–401. doi:10.3174/ajnr.A3670

    Article  CAS  PubMed  Google Scholar 

  16. 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

    Google Scholar 

  17. 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

    Article  PubMed  Google Scholar 

  18. Garcia DM, Duhamel G, Alsop DC (2005) Efficiency of inversion pulses for background suppressed arterial spin labeling. Magn Reson Med 54:366–372. doi:10.1002/mrm.20556

    Article  PubMed  Google Scholar 

  19. Maleki N, Dai W, Alsop DC (2012) Optimization of background suppression for arterial spin labeling perfusion imaging. MAGMA 25:127–133. doi:10.1007/s10334-011-0286-3

    Article  PubMed  Google Scholar 

  20. DeLong ER, DeLong DM, Clarke-Pearson DL (1988) Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 44:837–845

    Article  CAS  PubMed  Google Scholar 

  21. Aronen HJ, Gazit IE, Louis DN, Buchbinder BR, Pardo FS, Weisskoff RM, Harsh GR, Cosgrove GR, Halpern EF, Hochberg FH et al (1994) Cerebral blood volume maps of gliomas: comparison with tumor grade and histologic findings. Radiology 191:41–51. doi:10.1148/radiology.191.1.8134596

    Article  CAS  PubMed  Google Scholar 

  22. 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 6:91–97

    Article  PubMed  Google Scholar 

  23. 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

    Article  PubMed  Google Scholar 

  24. 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

    Article  CAS  PubMed  Google Scholar 

  25. 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

    Article  PubMed  Google Scholar 

  26. Tien RD, Felsberg GJ, Friedman H, Brown M, MacFall J (1994) MR imaging of high-grade cerebral gliomas: value of diffusion-weighted echoplanar pulse sequences. Am J Roentgenol 162:671–677. doi:10.2214/ajr.162.3.8109520

    Article  CAS  Google Scholar 

  27. Risberg J, Ancri D, Ingvar DH (1969) Correlation between cerebral blood volume and cerebral blood flow in the cat. Exp Brain Res 8:321–326

    Article  CAS  PubMed  Google Scholar 

  28. Ito H, Kanno I, Ibaraki M, Hatazawa J, Miura S (2003) Changes in human cerebral blood flow and cerebral blood volume during hypercapnia and hypocapnia measured by positron emission tomography. J Cereb Blood Flow Metab 23:665–670. doi:10.1097/01.WCB.0000067721.64998.F5

    Article  PubMed  Google Scholar 

  29. 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 13:17–27

    Article  PubMed  Google Scholar 

  30. Catafau AM (2001) Brain SPECT in clinical practice. Part I: perfusion. J Nucl Med 42:259–271

    CAS  PubMed  Google Scholar 

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Funding

This work was supported by JSPS KAKENHI Grant Number 26461828.

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Correspondence to Akio Hiwatashi.

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The authors declare that they have no conflict of interest.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. This cross-sectional study was approved by an institutional review board (approval #26-138).

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Kikuchi, K., Hiwatashi, A., Togao, O. et al. Correlation between arterial spin-labeling perfusion and histopathological vascular density of pediatric intracranial tumors. J Neurooncol 135, 561–569 (2017). https://doi.org/10.1007/s11060-017-2604-8

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  • DOI: https://doi.org/10.1007/s11060-017-2604-8

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