Share:
Share this content in WeChat
X
Clinical Article
Value of arterial spin labeling and diffusion tensor imaging in evaluating IDH1 gene phenotype in gliomas
ZHANG Meng  GENG Ruiwen  BAI Yuan  DONG Yang 

Cite this article as: ZHANG M, GENG R W, BAI Y, et al. Value of arterial spin labeling and diffusion tensor imaging in evaluating IDH1 gene phenotype in gliomas[J]. Chin J Magn Reson Imaging, 2023, 14(10): 58-64. DOI:10.12015/issn.1674-8034.2023.10.011.


[Abstract] Objective To investigate the value of conventional MRI combined with arterial spin labeling (ASL) imaging and diffusion tensor imaging (DTI) in assessing the phenotype of isocitrate dehydrogenase 1 (IDH1) value in glioma.Materials and Methods Sixty-one cases of patients with pathologically confirmed glioma from September 2019 to December 2021 were collected retrospectively and divided into IDH1 mutant (IDH1mut) and IDH1 wild (IDH1wt) groups according to IDH1 phenotype by genetic or immunohistochemical detection. Routine cranial MRI examination, ASL and DTI examination were performed before surgery. Evaluate the conventional MRI features of IDH1mut and IDH1wt gliomas (size, location, margin, necrotic cystic changes, hemorrhage, edema, and enhancement), measure the anisotropy fraction (FA), apparent diffusion coefficient (ADC), maximum cerebral blood flow (CBFmax) and mean (CBFmean) of the solid tumor area and peritumor area, and the relative CBFmax (rCBFmax), relative cerebral CBFmean (rCBFmean) were computed. Statistical analysis was performed using SPSS 25.0. All inter-sample analyses were performed using independent samples t-tests or non-parametric tests. Multi-factor logistic regression models were developed and receiver operating characteristic (ROC) curves were plotted to predict diagnostic efficacy.Results A total of 61 cases of gliomas were included in this study: 19 cases of IDH1mut and 42 cases of IDH1wt. There were significant differences in the location, enhancement, edema, CBF in the solid tumor area, and ADC in the peritumor area between IDH1mut and IDH1wt gliomas (P<0.05). CBFmax, CBFmean, rCBFmax, and rCBFmean in the solid tumor area of IDH1wt were higher than those of IDH1mut (P<0.05), and the area under the curve (AUC) was 0.879, 0.832, 0.806, 0.875, respectively. The peritumoral ADC value of IDH1wt was higher than that of IDH1mut (P<0.05). The CBFmean in solid tumor area combined with ADC value in peritumor area had the highest diagnostic efficacy (AUC=0.892). Multi-factor logistic regression showed that CBF in the solid tumor area was an independent risk factor for predicting the IDH1 phenotype of glioma.Conclusions Multi-parametric MRI has important value in evaluating the IDH1 phenotype of gliomas. The combination of tumor parenchymal CBF and peritumoral ADC can further improve the diagnostic efficacy of the IDH1 phenotype of gliomas.
[Keywords] glioma;magnetic resonance imaging;arterial spin labeling;diffusion tensor imaging;isocitrate dehydrogenase 1;peritumoral

ZHANG Meng1, 2   GENG Ruiwen1   BAI Yuan1   DONG Yang1*  

1 Department of Radiology, the Second Hospital of Dalian Medical University, Dalian 116027, China

2 Dalian Medical University, Dalian 116027, China

Corresponding author: DONG Y, E-mail: 23121546@qq.com

Conflicts of interest   None.

ACKNOWLEDGMENTS Scientific Research Plan Project of Liaoning Provincial Department of Education (No. LZ2019030).
Received  2023-03-12
Accepted  2023-09-11
DOI: 10.12015/issn.1674-8034.2023.10.011
Cite this article as: ZHANG M, GENG R W, BAI Y, et al. Value of arterial spin labeling and diffusion tensor imaging in evaluating IDH1 gene phenotype in gliomas[J]. Chin J Magn Reson Imaging, 2023, 14(10): 58-64. DOI:10.12015/issn.1674-8034.2023.10.011.

[1]
YANG X J, YIN H F, LI Z, et al. Chinese version of simplified table of 2021 WHO Classification of Tumors of the Central Nervous System (fifth edition) and translational interpretations[J]. Chin J Contemp Neurol Neurosurg, 2021, 21(9): 746-750.
[2]
LOUIS D N, PERRY A, WESSELING P, et al. The 2021 WHO Classification of Tumors of the Central Nervous System: a summary[J]. Neuro Oncol, 2021, 23(8): 1231-1251. DOI: 10.1093/neuonc/noab106.
[3]
SPORIKOVA Z, SLAVKOVSKY R, TUCKOVA L, et al. IDH1/2 mutations in patients with diffuse gliomas: a single centre retrospective massively parallel sequencing analysis[J]. Appl Immunohistochem Mol Morphol, 2022, 30(3): 178-183. DOI: 10.1097/PAI.0000000000000997.
[4]
MONDESIR J, WILLEKENS C, TOUAT M, et al. IDH1 and IDH2 mutations as novel therapeutic targets: current perspectives[J]. J Blood Med, 2016, 7: 171-180. DOI: 10.2147/JBM.S70716.eCollection2016.
[5]
YAN H, PARSONS D W, JIN G, et al. IDH1 and IDH2 mutations in gliomas[J]. N Engl J Med, 2009, 360(8): 765-773. DOI: 10.1056/NEJMoa0808710.
[6]
KAUR B, KHWAJA F W, SEVERSON E A, et al. Hypoxia and the hypoxia-inducible-factor pathway in glioma growth and angiogenesis[J]. Neuro Oncol, 2005, 7(2): 134-153. DOI: 10.1215/s1152851704001115.
[7]
DANG L, WHITE D W, GROSS S, et al. Cancer-associated IDH1 mutations produce 2-hydroxyglutarate[J]. Nature, 2009, 462(7274): 739-744. DOI: 10.1038/nature08617.
[8]
PRENSNER J R, CHINNAIYAN A M. Metabolism unhinged: IDH mutations in cancer[J]. Nat Med, 2011, 17(3): 291-293. DOI: 10.1038/nm0311-291.
[9]
TAN Y, ZHANG H, WANG X, et al. Comparing the value of DKI and DTI in detecting isocitrate dehydrogenase genotype of astrocytomas[J]. Clin Radiol, 2019, 74(4): 314-320. DOI: 10.1016/j.crad.2018.12.004.
[10]
WANG N, XIE S Y, LIU H M, et al. Arterial Spin Labeling for Glioma Grade Discrimination: Correlations with IDH1 Genotype and 1p/19q Status[J]. Transl Oncol, 2019, 12(5): 749-756. DOI: 10.1016/j.tranon.2019.02.013.
[11]
HUNG N DUY, MINH DUC N, VAN ANH N T, et al. Diagnostic performance of diffusion tensor imaging for preo-perative glioma grading[J]. Clin Ter, 2021, 172(4): 315-321. DOI: 10.7417/ct.2021.2335.
[12]
ALIOTTA E, NOURZADEH H, BATCHALA P P, et al. Molecular Subtype Classification in Lower-Grade Glioma with Accelerated DTI[J]. AJNR Am J Neuroradiol, 2019, 40(9): 1458-1463. DOI: 10.3174/ajnr.A6162.
[13]
BATALOV A I, ZAKHAROVA N E, CHEKHONIN I V, et al. Arterial spin labeling perfusion in determining the IDH1 status and Ki-67 index in brain gliomas[J/OL]. Diagnostics (Basel), 2022, 12(6): 1444 [2023-03-12]. https://pubmed.ncbi.nlm.nih.gov/35741254/.10.3390/diagnostics12061444. DOI: 10.3390/diagnostics12061444.
[14]
AUGELLI R, CICERI E, GHIMENTON C, et al. Magnetic resonance diffusion-tensor imaging metrics in high grade gliomas: correlation with IDH1 gene status in WHO 2016 era[J]. Eur J Radiol, 2019, 116: 174-179. DOI: 10.1016/j.ejrad.2019.04.020.
[15]
WANG R, WANG S Y, ZHANG H P, et al. Application value of DCE-MRI in tumor body, peritumoral edema area in grading diffuse glioma[J]. Chin J Magn Reson Imaging, 2021, 12(6): 88-91. DOI: 10.12015/issn.1674-8034.2021.06.017.
[16]
DU N, SHU W, LI K, et al. An initial study on the predictive value using multiple MRI characteristics for Ki-67 labeling index in glioma[J/OL]. J Transl Med, 2023, 21(1): 119 [2023-03-12]. https://pubmed.ncbi.nlm.nih.gov/36774480/.10.1186/s12967-023-03950-w. DOI: 10.1186/s12967-023-03950-w.
[17]
PICCA A, BERZERO G, DI STEFANO A L, et al. The clinical use of IDH1 and IDH2 mutations in gliomas[J]. Expert Rev Mol Diagn, 2018, 18(12): 1041-1051. DOI: 10.1080/14737159.2018.1548935.
[18]
QI S, YU L, LI H, et al. Isocitrate dehydrogenase mutation is associated with tumor location and magnetic resonance imaging characteristics in astrocytic neoplasms[J]. Oncol Lett, 2014, 7(6): 1895-1902. DOI: 10.3892/ol.2014.2013.
[19]
XING Z, ZHANG H, SHE D, et al. IDH genotypes differentiation in glioblastomas using DWI and DSC-PWI in the enhancing and peri-enhancing region[J]. Acta Radiol, 2019, 60(12): 1663-1672. DOI: 10.1177/0284185119842288.
[20]
HARTMANN C, MEYER J, BALSS J, et al. Type and frequency of IDH1 and IDH2 mutations are related to astrocytic and oligodendroglial differentiation and age: a study of 1, 010 diffuse gliomas[J]. Acta Neuropathol, 2009, 118(4): 469-474. DOI: 10.1007/s00401-009-0561-9.
[21]
KLOOSTERHOF N K, BRALTEN L B, DUBBINK H J, et al. Isocitrate dehydrogenase-1 mutations: a fundamentally new understanding of diffuse glioma?[J]. Lancet Oncol, 2011, 12(1): 83-91. DOI: 10.1016/s1470-2045(10)70053-x.
[22]
DUBINSKI D, WON S Y, RAUCH M, et al. Association of isocitrate dehydrogenase (IDH) status with edema to tumor ratio and its correlation with immune infiltration in glioblastoma[J/OL]. Front Immunol, 2021, 12: 627650 [2023-03-12]. https://pubmed.ncbi.nlm.nih.gov/33868245/.10.3389/fimmu.2021.627650. DOI: 10.3389/fimmu.2021.627650.
[23]
YANG J, ZHANG X, GAO X, et al. Fiber density and structural brain connectome in glioblastoma are correlated with glioma cell infiltration[J]. Neurosurgery, 2023, 92(6): 1234-1242. DOI: 10.1227/neu.0000000000002356.
[24]
LI Y, QIN Q, ZHANG Y, et al. Noninvasive determination of the IDH status of gliomas using MRI and MRI-Based radiomics: impact on diagnosis and prognosis[J]. Curr Oncol, 2022, 29(10): 6893-6907. DOI: 10.3390/curroncol29100542.
[25]
YAN J, ZHANG B, ZHANG S, et al. Quantitative MRI-based radiomics for noninvasively predicting molecular subtypes and survival in glioma patients[J/OL]. NPJ Precis Oncol, 2021, 5(1): 72 [2023-03-12]. https://pubmed.ncbi.nlm.nih.gov/34312469/. DOI: 10.1038/s41698-021-00205-z.
[26]
DASGUPTA A, GERAGHTY B, MARALANI P J, et al. Quantitative mapping of individual voxels in the peritumoral region of IDH-wildtype glioblastoma to distinguish between tumor infiltration and edema[J]. J Neurooncol, 2021, 153(2): 251-261. DOI: 10.1007/s11060-021-03762-2.
[27]
SHIMIZU T, MATSUSHIMA S, FUKASAWA N, et al. Differentiating between glioblastomas with and without isocitrate dehydrogenase gene mutation by findings on conventional magnetic resonance images[J]. J Clin Neurosci, 2020, 76: 140-144. DOI: 10.1016/j.jocn.2020.04.016.
[28]
HYARE H, RICE L, THUST S, et al. Modelling MR and clinical features in grade Ⅱ/Ⅲ astrocytomas to predict IDH mutation status[J]. Eur J Radiol, 2019, 114: 120-127. DOI: 10.1016/j.ejrad.2019.03.003.
[29]
SHIN S, KIM K, NAM H Y, et al. Sex difference in cerebral blood flow and cerebral glucose metabolism: an activation-likelihood estimation meta-analysis[J]. Nucl Med Commun, 2021, 42(4): 410-415. DOI: 10.1097/mnm.0000000000001343.
[30]
WANG K, WANG Y, FAN X, et al. Radiological features combined with IDH1 status for predicting the survival outcome of glioblastoma patients[J]. Neuro Oncol, 2016, 18(4): 589-597. DOI: 10.1093/neuonc/nov239.
[31]
GUO D, JIANG B. Noninvasively evaluating the grade and IDH mutation status of gliomas by using mono-exponential, bi-exponential diffusion-weighted imaging and three-dimensional pseudo-continuous arterial spin labeling[J/OL]. Eur J Radiol, 2023, 160: 110721 [2023-03-12]. https://pubmed.ncbi.nlm.nih.gov/36738600/.10.1016/j.ejrad.2023.110721. DOI: 10.1016/j.ejrad.2023.110721.
[32]
AHN S H, AHN S S, PARK Y W, et al. Association of dynamic susceptibility contrast- and dynamic contrast-enhanced magnetic resonance imaging parameters with molecular marker status in lower-grade gliomas: A retrospective study[J]. Neuroradiol J, 2023, 36(1): 49-58. DOI: 10.1177/19714009221098369.
[33]
PANG H, DANG X, REN Y, et al. 3D-ASL perfusion correlates with VEGF expression and overall survival in glioma patients: Comparison of quantitative perfusion and pathology on accurate spatial location-matched basis[J]. J Magn Reson Imaging, 2019, 50(1): 209-220. DOI: 10/.10.1002/jmri.26562.
[34]
LI S H, SHEN N X, WU D, et al. A comparative study between tumor blood vessels and dynamic contrast-enhanced MRI for identifying isocitrate dehydrogenase gene 1 (IDH1) mutation status in glioma[J]. Curr Med Sci, 2022, 42(3): 650-657. DOI: 10.1007/s11596-022-2563-y.
[35]
ZHAO J, WANG Y L, LI X B, et al. Comparative analysis of the diffusion kurtosis imaging and diffusion tensor imaging in grading gliomas, predicting tumour cell proliferation and IDH-1 gene mutation status[J]. J Neurooncol, 2019, 141(1): 195-203. DOI: 10.1007/s11060-018-03025-7.
[36]
XIONG J, TAN W, WEN J, et al. Combination of diffusion tensor imaging and conventional MRI correlates with isocitrate dehydrogenase 1/2 mutations but not 1p/19q genotyping in oligodendroglial tumours[J]. Eur Radiol, 2016, 26(6): 1705-1715. DOI: 10.1007/s00330-015-4025-4.
[37]
TAN W L, HUANG W Y, YIN B, et al. Can diffusion tensor imaging noninvasively detect IDH1 gene mutations in astrogliomas? A retrospective study of 112 cases[J]. AJNR Am J Neuroradiol, 2014, 35(5): 920-927. DOI: 10.3174/ajnr.A3803.
[38]
ZHU W, GAO Y, WANG P J. The Research of Multimodal Functional MRI in the Evaluation of IDH1 mutation Status of Glioma[J]. Chin Comput Med Imag, 2021, 27(3): 179-184. DOI: 10.19627/j.cnki.cn31-1700/th.2021.03.001.
[39]
METZ M C, MOLINA-ROMERO M, LIPKOVA J, et al. Predicting glioblastoma recurrence from preoperative MR scans using fractional-anisotropy maps with free-water suppression[J/OL]. Cancers (Basel), 2020, 12(3): 728 [2023-03-12]. https://pubmed.ncbi.nlm.nih.gov/32204544/.10.3390/cancers12030728. DOI: 10.3390/cancers12030728.
[40]
WAQAR M, LEWIS D, AGUSHI E, et al. Cerebral and tumoral blood flow in adult gliomas: a systematic review of results from magnetic resonance imaging[J/OL]. Br J Radiol, 2021, 94(1125): 20201450 [2023-03-12]. https://pubmed.ncbi.nlm.nih.gov/34106749/. DOI: 10.1259/bjr.20201450.
[41]
YOO R E, YUN T J, HWANG I, et al. Arterial spin labeling perfusion-weighted imaging aids in prediction of molecular biomarkers and survival in glioblastomas[J]. Eur Radiol, 2020, 30(2): 1202-1211. DOI: 10.1007/s00330-019-06379-2.
[42]
XIONG J, TAN W L, PAN J W, et al. Detecting isocitrate dehydrogenase gene mutations in oligodendroglial tumors using diffusion tensor imaging metrics and their correlations with proliferation and microvascular density[J]. J Magn Reson Imaging, 2016, 43(1): 45-54. DOI: 10.1002/jmri.24958.

PREV The value of multi-parametric MRI-based radiomics models in distinguishing primary central nervous system lymphoma from high-grade glioma
NEXT Application value of 3.0 T MAGIC relaxation time quantitative technique in neonates with acute bilirubin encephalopathy
  



Tel & Fax: +8610-67113815    E-mail: editor@cjmri.cn