Abstract
Introduction
This study was conducted to compare the association of Gaussian and non-Gaussian magnetic resonance imaging (MRI)-derived parameters with histologic grade and MIB-1 (Ki-67 labeling) index (MI) in brain glioma.
Methods
Sixty-five patients with pathologically confirmed glioma, who underwent diffusion-weighted MRI with 2 b values (0, 1000 s/mm2) and 22 b values (≤5000 s/mm2), respectively, were divided into three groups of grade II (n = 35), grade III (n = 8), and grade IV (n = 22). Comparisons by two groups were made for apparent diffusion coefficient (ADC), slow diffusion coefficient (Dslow), distributed diffusion coefficient (DDC), and heterogeneity index α. Analyses of receiver operating characteristic (ROC) curve were performed to maximize the area under the curve (AUC) for differentiating grade III + IV (high-grade glioma, HGG) from grade II (low-grade glioma, LGG) and grade IV (glioblastoma multiforme, GBM) from grade II + III (other grade glioma, OGG). Correlations with MI were analyzed for the MRI parameters.
Results
On tumor regions, the values of ADC, Dslow, DDC, and α were significantly higher in grade II [(1.37 ± 0.29, 0.70 ± 0.11, 1.39 ± 0.34) (×10−3 mm2/s) and 0.88 ± 0.05, respectively] than in grade III [(0.99 ± 0.13, 0.55 ± 0.07, 1.04 ± 0.20) (×10−3 mm2/s) and 0.80 ± 0.03, respectively] and grade IV [(1.03 ± 0.14, 0.50 ± 0.05, 1.02 ± 0.16) (×10−3 mm2/s) and 0.76 ± 0.04, respectively] (all P < 0.001). The parameter α showed the highest AUCs of 0.950 and 0.922 in discriminating HGG from LGG and GBM from OGG, respectively. Significant correlations with histologic grade and MI were observed for the MRI parameters.
Conclusion
The non-Gaussian MRI-derived parameters α and Dslow are superior to ADC in glioma grading, which are comparable with ADC as reliable biomarkers in noninvasively predicting the proliferation level of glioma malignancy.
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References
Nitta M, Muragaki Y, Maruyama T, Ikuta S, Komori T, Maebayashi K et al (2015) Proposed therapeutic strategy for adult low-grade glioma based on aggressive tumor resection. Neurosurg Focus 38, E7
Weller M, van den Bent M, Hopkins K, Tonn JC, Stupp R, Falini A et al (2014) EANO guideline for the diagnosis and treatment of anaplastic gliomas and glioblastoma. Lancet Oncol 15:e395–e403
Chen R, Ravindra VM, Cohen AL, Jensen RL, Salzman KL, Prescot AP et al (2015) Molecular features assisting in diagnosis, surgery, and treatment decision making in low-grade gliomas. Neurosurg Focus 38, E2
Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A et al (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114:97–109
Maris D, Nica D, Mohan D, Moisa H, Ciurea AV (2014) Multidisciplinary management of adult low grade gliomas. Chirurgia (Bucur) 109:590–599
Le Bihan D (2013) Apparent diffusion coefficient and beyond: what diffusion MR imaging can tell us about tissue structure. Radiology 268:318–322
Kang Y, Choi SH, Kim YJ, Kim KG, Sohn CH, Kim JH et al (2011) Gliomas: histogram analysis of apparent diffusion coefficient maps with standard- or high-b-value diffusion-weighted MR imaging—correlation with tumor grade. Radiology 261:882–890
Grinberg F, Farrher E, Ciobanu L, Geffroy F, Le Bihan D, Shah NJ (2014) Non-Gaussian diffusion imaging for enhanced contrast of brain tissue affected by ischemic stroke. PLoS One 9, e89225
Kristoffersen A (2011) Statistical assessment of non-Gaussian diffusion models. Magn Reson Med 66:1639–1648
Iima M, Reynaud O, Tsurugizawa T, Ciobanu L, Li JR, Geffroy F et al (2014) Characterization of glioma microcirculation and tissue features using intravoxel incoherent motion magnetic resonance imaging in a rat brain model. Invest Radiol 49:485–490
Kwee TC, Galban CJ, Tsien C, Junck L, Sundgren PC, Ivancevic MK et al (2010) Intravoxel water diffusion heterogeneity imaging of human high-grade gliomas. NMR Biomed 23:179–187
Bisdas S, Koh TS, Roder C, Braun C, Schittenhelm J, Ernemann U et al (2013) Intravoxel incoherent motion diffusion-weighted MR imaging of gliomas: feasibility of the method and initial results. Neuroradiology 55:1189–1196
Bennett KM, Schmainda KM, Bennett RT, Rowe DB, Lu H, Hyde JS (2003) Characterization of continuously distributed cortical water diffusion rates with a stretched-exponential model. Magn Reson Med 50:727–734
Skjulsvik AJ, Mork JN, Torp MO, Torp SH (2014) Ki-67/MIB-1 immunostaining in a cohort of human gliomas. Int J Clin Exp Pathol 7:8905–8910
Wakimoto H, Aoyagi M, Nakayama T, Nagashima G, Yamamoto S, Tamaki M et al (1996) Prognostic significance of Ki-67 labeling indices obtained using MIB-1 monoclonal antibody in patients with supratentorial astrocytomas. Cancer 77:373–380
Gempt J, Soehngen E, Forster S, Ryang YM, Schlegel J, Zimmer C et al (2014) Multimodal imaging in cerebral gliomas and its neuropathological correlation. Eur J Radiol 83:829–834
Bossuyt PM, Reitsma JB, Bruns DE, Gatsonis CA, Glasziou PP, Irwig LM et al (2003) Towards complete and accurate reporting of studies of diagnostic accuracy: the STARD Initiative. Radiology 226:24–28
Fudaba H, Shimomura T, Abe T, Matsuta H, Momii Y, Sugita K et al (2014) Comparison of multiple parameters obtained on 3T pulsed arterial spin-labeling, diffusion tensor imaging, and MRS and the Ki-67 labeling index in evaluating glioma grading. AJNR Am J Neuroradiol 35:2091–2098
Le Bihan D, Breton E, Lallemand D, Aubin ML, Vignaud J, Laval-Jeantet M (1988) Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. Radiology 168:497–505
Kwee TC, Galban CJ, Tsien C, Junck L, Sundgren PC, Ivancevic MK et al (2010) Comparison of apparent diffusion coefficients and distributed diffusion coefficients in high-grade gliomas. J Magn Reson Imaging 31:531–537
Tao H, Li H, Hua Y, Chen Z, Feng X, Chen S (2015) Quantitative magnetic resonance imaging (MRI) evaluation of cartilage repair after microfracture treatment for full-thickness cartilage defect models in rabbit knee joints: correlations with histological findings. Skeletal Radiol 44:393–402
Woo S, Lee JM, Yoon JH, Joo I, Han JK, Choi BI (2014) Intravoxel incoherent motion diffusion-weighted MR imaging of hepatocellular carcinoma: correlation with enhancement degree and histologic grade. Radiology 270:758–767
Youden WJ (1950) Index for rating diagnostic tests. Cancer 3:32–35
Bisdas S, Braun C, Skardelly M, Schittenhelm J, Teo TH, Thng CH et al (2014) Correlative assessment of tumor microcirculation using contrast-enhanced perfusion MRI and intravoxel incoherent motion diffusion-weighted MRI: is there a link between them? NMR Biomed 27:1184–1191
Federau C, Meuli R, O’Brien K, Maeder P, Hagmann P (2014) Perfusion measurement in brain gliomas with intravoxel incoherent motion MRI. AJNR Am J Neuroradiol 35:256–262
Hu YC, Yan LF, Wu L, Du P, Chen BY, Wang L et al (2014) Intravoxel incoherent motion diffusion-weighted MR imaging of gliomas: efficacy in preoperative grading. Sci Rep 4:7208
Higano S, Yun X, Kumabe T, Watanabe M, Mugikura S, Umetsu A et al (2006) Malignant astrocytic tumors: clinical importance of apparent diffusion coefficient in prediction of grade and prognosis. Radiology 241:839–846
Cui Y, Ma L, Chen X, Zhang Z, Jiang H, Lin S (2014) Lower apparent diffusion coefficients indicate distinct prognosis in low-grade and high-grade glioma. J Neurooncol 119:377–385
Togao O, Hiwatashi A, Yamashita K, Kikuchi K, Mizoguchi M, Yoshimoto K et al (2015) Differentiation of high-grade and low-grade diffuse gliomas by intravoxel incoherent motion MR imaging. Neuro Oncol. doi:10.1093/neuonc/nov147
Chandarana H, Lee VS, Hecht E, Taouli B, Sigmund EE (2011) Comparison of biexponential and monoexponential model of diffusion weighted imaging in evaluation of renal lesions: preliminary experience. Invest Radiol 46:285–291
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We declare that all human studies have been approved by the Huashan Hospital Ethics Committee and have therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. We declare that all patients gave informed consent prior to inclusion in this study.
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RY and PH contributed equally to this study and are joint first authors.
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Yan, R., Haopeng, P., Xiaoyuan, F. et al. Non-Gaussian diffusion MR imaging of glioma: comparisons of multiple diffusion parameters and correlation with histologic grade and MIB-1 (Ki-67 labeling) index. Neuroradiology 58, 121–132 (2016). https://doi.org/10.1007/s00234-015-1606-5
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DOI: https://doi.org/10.1007/s00234-015-1606-5