A Comparative Study Between Tumor Blood Vessels and Dynamic Contrast-enhanced MRI for Identifying Isocitrate Dehydrogenase Gene 1 (IDH1) Mutation Status in Glioma

Shi-hui Li , Nan-xi Shen , Di Wu , Ju Zhang , Jia-xuan Zhang , Jing-jing Jiang , Wen-zhen Zhu

Current Medical Science ›› 2022, Vol. 42 ›› Issue (3) : 650 -657.

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Current Medical Science ›› 2022, Vol. 42 ›› Issue (3) : 650 -657. DOI: 10.1007/s11596-022-2563-y
Article

A Comparative Study Between Tumor Blood Vessels and Dynamic Contrast-enhanced MRI for Identifying Isocitrate Dehydrogenase Gene 1 (IDH1) Mutation Status in Glioma

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Abstract

Objective

Isocitrate dehydrogenase gene (IDH) mutations are associated with tumor angiogenesis and therefore play an important role in glioma management. This study compared the performance of tumor blood vessels counted from contrast-enhanced 3D brain volume (3D-BRAVO) sequence and dynamic contrast-enhanced (DCE) MRI in differentiating IDH1 status in gliomas.

Methods

Forty-four glioma patients [16 with IDH1 mutant-type (IDH1-MT), 28 with IDH1 wild-type (IDH1-WT)] were retrospectively analyzed. A blood vessel entering a tumor was defined as an intratumoral vessel; a blood vessel adjacent to the edge of a tumor was defined as a peritumoral vessel. Combined vessels were defined as the sum of the intratumoral and peritumoral vessels. DCE-derived metrics of tumor were normalized to the contralateral normal-appearing white matter.

Results

Intratumoral, peritumoral, and combined tumor blood vessels were all significantly different between IDH1-MT and IDH1-WT gliomas, and the range of area under curves (AUCs) was 0.816–0.855. For DCE-derived parameters, cerebral blood volume, cerebral blood flow, mean transit time, and volume transfer constant were significantly different between IDH1-MT and IDH1-WT gliomas, and the range of AUCs was 0.703–0.756. Combined vessels possessed the best performance for identifying IDH1 mutations in gliomas (AUC: 0.855, sensitivity: 0.857, specificity: 0.812, P<0.001).

Conclusion

The number of tumor blood vessels has comparable diagnostic performance with DCE-derived parameters for differentiating IDH1 mutations and can serve as a potential imaging biomarker to reflect IDH1 mutations in gliomas.

Keywords

dynamic contrast-enhanced perfusion / glioma / isocitrate dehydrogenase gene / tumor blood vessel

Cite this article

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Shi-hui Li, Nan-xi Shen, Di Wu, Ju Zhang, Jia-xuan Zhang, Jing-jing Jiang, Wen-zhen Zhu. A Comparative Study Between Tumor Blood Vessels and Dynamic Contrast-enhanced MRI for Identifying Isocitrate Dehydrogenase Gene 1 (IDH1) Mutation Status in Glioma. Current Medical Science, 2022, 42(3): 650-657 DOI:10.1007/s11596-022-2563-y

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References

[1]

BelloL, GiussaniC, CarrabbaG, et al.. Angiogenesis and invasion in gliomas. Cancer Treat Res, 2004, 117: 263-284

[2]

BurgerPC, VogelFS, GreenSB, et al.. Glioblastoma multiforme and anaplastic astrocytoma. Pathologic criteria and prognostic implications. Cancer, 1985, 56(5): 1106-1111

[3]

Daumas-DuportC, TuckerML, KollesH, et al.. Oligodendrogliomas. Part II: A new grading system based on morphological and imaging criteria. J Neurooncol, 1997, 34(1): 61-78

[4]

AbdulraufSI, EdvardsenK, HoKL, et al.. Vascular endothelial growth factor expression and vascular density as prognostic markers of survival in patients with low-grade astrocytoma. J Neurosurg, 1998, 88(3): 513-520

[5]

HardeeME, ZagzagD. Mechanisms of glioma-associated neovascularization. Am J Pathol, 2012, 181(4): 1126-1141

[6]

LouisDN, PerryA, ReifenbergerG, et al.. The 2016 World Health Organization Classification of Tumors of the Central Nervous System: a summary. Acta Neuropathologica, 2016, 131(6): 803-820

[7]

LaiA, KharbandaS, PopeWB, et al.. Evidence for sequenced molecular evolution of IDH1 mutant glioblastoma from a distinct cell of origin. J Clin Oncol, 2011, 29(34): 4482-4490

[8]

YanH, ParsonsDW, JinG, et al.. IDH1 and IDH2 mutations in gliomas. N Engl J Med, 2009, 360(8): 765-773

[9]

BalssJ, MeyerJ, MuellerW, et al.. Analysis of the IDH1 codon 132 mutation in brain tumors. Acta Neuropathol, 2008, 116(6): 597-602

[10]

DangL, WhiteD W, GrossS, et al.. Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature, 2009, 462(7274): 739-744

[11]

YeD, MaS, XiongY, et al.. R-2-hydroxyglutarate as the key effector of IDH mutations promoting oncogenesis. Cancer Cell, 2013, 23(3): 274-276

[12]

KoivunenP, LeeS, DuncanCG, et al.. Transformation by the (R)-enantiomer of 2-hydroxyglutarate linked to EGLN activation. Nature, 2012, 483(7390): 484-488

[13]

KickingerederP, SahmF, RadbruchA, et al.. IDH mutation status is associated with a distinct hypoxia/angiogenesis transcriptome signature which is non-invasively predictable with rCBV imaging in human glioma. Sci Rep, 2015, 5: 16238

[14]

TurkalpZ, KaramchandaniJ, DasS. IDH mutation in glioma: new insights and promises for the future. JAMA Neurol, 2014, 71(10): 1319-1325

[15]

FriedmanHS, PradosMD, WenPY, et al.. Bevacizumab alone and in combination with irinotecan in recurrent glioblastoma. J Clin Oncol, 2009, 27(28): 4733-4740

[16]

ToviM, LiljaA, BergstromM, et al.. Delineation of gliomas with magnetic resonance imaging using Gd-DTPA in comparison with computed tomography and positron emission tomography. Acta Radiol, 1990, 31(5): 417-429

[17]

JahngGH, LiKL, OstergaardL, et al.. Perfusion magnetic resonance imaging: a comprehensive update on principles and techniques. Korean J Radiol, 2014, 15(5): 554-577

[18]

BrendleC, HempelJM, SchittenhelmJ, et al.. Glioma Grading and Determination of IDH Mutation Status and ATRX loss by DCE and ASL Perfusion. Clin Neuroradiol, 2018, 28(3): 421-428

[19]

YouSH, ChoiSH, KimTM, et al.. Differentiation of High-Grade from Low-Grade Astrocytoma: Improvement in Diagnostic Accuracy and Reliability of Pharmacokinetic Parameters from DCE MR Imaging by Using Arterial Input Functions Obtained from DSC MR Imaging. Radiology, 2018, 286(3): 981-991

[20]

PatelSH, PoissonLM, BratDJ, et al.. T2—FLAIR Mismatch, an Imaging Biomarker for IDH and 1p/19q Status in Lower-grade Gliomas: A TCGA/TCIA Project. Clin Cancer Res, 2017, 23(20): 6078-6085

[21]

XiY, KangX, WangN, et al.. Differentiation of primary central nervous system lymphoma from high-grade glioma and brain metastasis using arterial spin labeling and dynamic contrast-enhanced magnetic resonance imaging. Eur J Radiol, 2019, 112: 59-64

[22]

ToftsPS. Modeling tracer kinetics in dynamic Gd-DTPA MR imaging. J Magn Reson Imaging, 1997, 7(1): 91-101

[23]

KellnerE, BreyerT, GallP, et al.. MR evaluation of vessel size imaging of human gliomas: Validation by histopathology. J Magn Reson Imaging, 2015, 42(4): 1117-1125

[24]

LemassonB, ValableS, FarionR, et al.. In vivo imaging of vessel diameter, size, and density: a comparative study between MRI and histology. Magn Reson Med, 2013, 69(1): 18-26

[25]

KiselevV G, StreckerR, ZiyehS, et al.. Vessel size imaging in humans. Magn Reson Med, 2005, 53(3): 553-563

[26]

TropresI, GrimaultS, VaethA, et al.. Vessel size imaging. Magn Reson Med, 2001, 45(3): 397-408

[27]

GuoH, KangH, TongH, et al.. Microvascular characteristics of lower-grade diffuse gliomas: investigating vessel size imaging for differentiating grades and subtypes. Eur Radiol, 2019, 29(4): 1893-1902

[28]

StadlbauerA, ZimmermannM, KitzwogererM, et al.. MR Imaging-derived Oxygen Metabolism and Neovascularization Characterization for Grading and IDH Gene Mutation Detection of Gliomas. Radiology, 2017, 283(3): 799-809

[29]

KleihuesP, SoylemezogluF, SchaubleB, et al.. Histopathology, classification, and grading of gliomas. Glia, 1995, 15(3): 211-221

[30]

Jafari-KhouzaniK, LoebelF, BognerW, et al.. Volumetric relationship between 2-hydroxyglutarate and FLAIR hyperintensity has potential implications for radiotherapy planning of mutant IDH glioma patients. Neuro Oncol, 2016, 18(11): 1569-1578

[31]

MurP, MollejoM, Hernández-IglesiasT, et al.. Molecular Classification Defines 4 Prognostically Distinct Glioma Groups Irrespective of Diagnosis and Grade. J Neuropathol Exp Neurol, 2015, 74(3): 241-249

[32]

BeikoJ, SukiD, HessK R, et al.. IDH1 mutant malignant astrocytomas are more amenable to surgical resection and have a survival benefit associated with maximal surgical resection. Neuro Oncol, 2014, 16(1): 81-91

[33]

PellegattaS, VallettaL, CorbettaC, et al.. Effective immuno-targeting of the IDH1 mutation R132H in a murine model of intracranial glioma. Acta Neuropathol Commun, 2015, 3: 4

[34]

RohleD, Popovici-MullerJ, PalaskasN, et al.. An inhibitor of mutant IDH1 delays growth and promotes differentiation of glioma cells. Science, 2013, 340(6132): 626-630

[35]

TurcanS, FabiusAW, BorodovskyA, et al.. Efficient induction of differentiation and growth inhibition in IDH1 mutant glioma cells by the DNMT Inhibitor Decitabine. Oncotarget, 2013, 4(10): 1729-1736

[36]

Gomez-ManzanoC, HolashJ, FueyoJ, et al.. VEGF Trap induces antiglioma effect at different stages of disease. Neuro Oncol, 2008, 10(6): 940-945

[37]

HolashJ, DavisS, PapadopoulosN, et al.. VEGF-Trap: a VEGF blocker with potent antitumor effects. Proc Natl Acad Sci U S A, 2002, 99(17): 11393-11398

[38]

Cortes-SantiagoN, HossainMB, GabrusiewiczK, et al.. Soluble Tie2 overrides the heightened invasion induced by anti-angiogenesis therapies in gliomas. Oncotarget, 2016, 7(13): 16146-16157

[39]

HuangH, BhatA, WoodnuttG, et al.. Targeting the ANGPT-TIE2 pathway in malignancy. Nat Rev Cancer, 2010, 10(8): 575-585

[40]

ChaeSS, KamounWS, FarrarCT, et al.. Angiopoietin-2 interferes with anti-VEGFR2-induced vessel normalization and survival benefit in mice bearing gliomas. Clin Cancer Res, 2010, 16(14): 3618-3627

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