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Published in: European Radiology 3/2019

01-03-2019 | Neuro

MR imaging based fractal analysis for differentiating primary CNS lymphoma and glioblastoma

Authors: Shuai Liu, Xing Fan, Chuanbao Zhang, Zheng Wang, Shaowu Li, Yinyan Wang, Xiaoguang Qiu, Tao Jiang

Published in: European Radiology | Issue 3/2019

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Abstract

Objectives

The aim of this study was to differentiate primary central nervous system lymphoma (PCNSL) from glioblastomas (GBM) using the fractal analysis of conventional MRI data.

Materials and methods

Sixty patients with PCNSL and 107 patients with GBM with MRI data available were enrolled. Fractal dimension (FD) and lacunarity values of the tumour region were calculated using fractal analysis. A predictive model combining fractal parameters and anatomical characteristics was built using logistic regression. The role of FD, lacunarity and the predictive model in differential diagnosis was evaluated using receiver-operating characteristic (ROC) curve analysis. The association between fractal parameters and anatomical characteristics of tumours was also investigated.

Results

PCNSL had lower FD values (p < 0.001) and higher lacunarity values (p < 0.001) than GBM. ROC curve analysis revealed that FD, lacunarity, and the predictive model could distinguish PCNSL from GBM (area under the curve: 0.895, 0.776, and 0.969, respectively). The following associations were observed between fractal parameters and anatomical characteristics: multiple lesions were significantly associated with higher lacunarity (p = 0.024), necrosis with higher FD (p = 0.027), corpus callosum involvement with higher lacunarity (p < 0.001) in PCNSL and subventricular zone involvement with higher FD (p < 0.001) in GBM.

Conclusions

The findings of the study indicate that fractal analysis on conventional MRI performs well in distinguishing PCNSL from GBM.

Key Points

• Fractal dimension and lacunarity were capable of differentiating PCNSL from GBM.
• PCNSL and GBM exhibited different anatomical characteristics.
• Fractal parameters were associated with some of these anatomical characteristics.
Literature
2.
go back to reference Hoang-Xuan K, Bessell E, Bromberg J et al (2015) Diagnosis and treatment of primary CNS lymphoma in immunocompetent patients: guidelines from the European Association for Neuro-Oncology. Lancet Oncol 16:e322–e332CrossRefPubMed Hoang-Xuan K, Bessell E, Bromberg J et al (2015) Diagnosis and treatment of primary CNS lymphoma in immunocompetent patients: guidelines from the European Association for Neuro-Oncology. Lancet Oncol 16:e322–e332CrossRefPubMed
3.
go back to reference Wang S, Kim S, Chawla S et al (2011) Differentiation between glioblastomas, solitary brain metastases, and primary cerebral lymphomas using diffusion tensor and dynamic susceptibility contrast-enhanced MR imaging. AJNR Am J Neuroradiol 32:507–514CrossRef Wang S, Kim S, Chawla S et al (2011) Differentiation between glioblastomas, solitary brain metastases, and primary cerebral lymphomas using diffusion tensor and dynamic susceptibility contrast-enhanced MR imaging. AJNR Am J Neuroradiol 32:507–514CrossRef
4.
go back to reference Yamashita K, Yoshiura T, Hiwatashi A et al (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 55:135–143CrossRefPubMed Yamashita K, Yoshiura T, Hiwatashi A et al (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 55:135–143CrossRefPubMed
5.
go back to reference Lin X, Lee M, Buck O et al (2017) Diagnostic Accuracy of T1-Weighted Dynamic Contrast-Enhanced-MRI and DWI-ADC for Differentiation of Glioblastoma and Primary CNS Lymphoma. AJNR Am J Neuroradiol 38:485–491CrossRefPubMed Lin X, Lee M, Buck O et al (2017) Diagnostic Accuracy of T1-Weighted Dynamic Contrast-Enhanced-MRI and DWI-ADC for Differentiation of Glioblastoma and Primary CNS Lymphoma. AJNR Am J Neuroradiol 38:485–491CrossRefPubMed
6.
go back to reference Kickingereder P, Sahm F, Wiestler B et al (2014) Evaluation of microvascular permeability with dynamic contrast-enhanced MRI for the differentiation of primary CNS lymphoma and glioblastoma: radiologic-pathologic correlation. AJNR Am J Neuroradiol 35:1503–1508CrossRefPubMed Kickingereder P, Sahm F, Wiestler B et al (2014) Evaluation of microvascular permeability with dynamic contrast-enhanced MRI for the differentiation of primary CNS lymphoma and glioblastoma: radiologic-pathologic correlation. AJNR Am J Neuroradiol 35:1503–1508CrossRefPubMed
7.
go back to reference Nakajima S, Okada T, Yamamoto A et al (2015) Differentiation between primary central nervous system lymphoma and glioblastoma: a comparative study of parameters derived from dynamic susceptibility contrast-enhanced perfusion-weighted MRI. Clin Radiol 70:1393–1399CrossRefPubMed Nakajima S, Okada T, Yamamoto A et al (2015) Differentiation between primary central nervous system lymphoma and glioblastoma: a comparative study of parameters derived from dynamic susceptibility contrast-enhanced perfusion-weighted MRI. Clin Radiol 70:1393–1399CrossRefPubMed
8.
go back to reference Jiang S, Yu H, Wang X et al (2016) Molecular MRI differentiation between primary central nervous system lymphomas and high-grade gliomas using endogenous protein-based amide proton transfer MR imaging at 3 Tesla. Eur Radiol 26:64–71CrossRef Jiang S, Yu H, Wang X et al (2016) Molecular MRI differentiation between primary central nervous system lymphomas and high-grade gliomas using endogenous protein-based amide proton transfer MR imaging at 3 Tesla. Eur Radiol 26:64–71CrossRef
9.
go back to reference Okada Y, Nihashi T, Fujii M et al (2012) Differentiation of newly diagnosed glioblastoma multiforme and intracranial diffuse large B-cell Lymphoma using (11)C-methionine and (18)F-FDG PET. Clin Nucl Med 37:843–849CrossRefPubMed Okada Y, Nihashi T, Fujii M et al (2012) Differentiation of newly diagnosed glioblastoma multiforme and intracranial diffuse large B-cell Lymphoma using (11)C-methionine and (18)F-FDG PET. Clin Nucl Med 37:843–849CrossRefPubMed
11.
go back to reference Fernandez E, Jelinek HF (2001) Use of fractal theory in neuroscience: methods, advantages, and potential problems. Methods 24:309–321CrossRefPubMed Fernandez E, Jelinek HF (2001) Use of fractal theory in neuroscience: methods, advantages, and potential problems. Methods 24:309–321CrossRefPubMed
12.
go back to reference Plotnick RE, Gardner RH, O'Neill RV (1993) Lacunarity indices as measures of landscape texture. Landscape ecology 8:201–211CrossRef Plotnick RE, Gardner RH, O'Neill RV (1993) Lacunarity indices as measures of landscape texture. Landscape ecology 8:201–211CrossRef
13.
go back to reference Di Ieva A, Le Reste PJ, Carsin-Nicol B, Ferre JC, Cusimano MD (2016) Diagnostic Value of Fractal Analysis for the Differentiation of Brain Tumors Using 3-Tesla Magnetic Resonance Susceptibility-Weighted Imaging. Neurosurgery 79:839–846CrossRefPubMed Di Ieva A, Le Reste PJ, Carsin-Nicol B, Ferre JC, Cusimano MD (2016) Diagnostic Value of Fractal Analysis for the Differentiation of Brain Tumors Using 3-Tesla Magnetic Resonance Susceptibility-Weighted Imaging. Neurosurgery 79:839–846CrossRefPubMed
14.
go back to reference Smitha KA, Gupta AK, Jayasree RS (2015) Fractal analysis: fractal dimension and lacunarity from MR images for differentiating the grades of glioma. Phys Med Biol 60:6937–6947CrossRefPubMed Smitha KA, Gupta AK, Jayasree RS (2015) Fractal analysis: fractal dimension and lacunarity from MR images for differentiating the grades of glioma. Phys Med Biol 60:6937–6947CrossRefPubMed
15.
go back to reference Nyúl LG, Udupa JK (1999) On standardizing the MR image intensity scale. Magn Reson Med 42:1072–1081CrossRefPubMed Nyúl LG, Udupa JK (1999) On standardizing the MR image intensity scale. Magn Reson Med 42:1072–1081CrossRefPubMed
16.
go back to reference Hellier P (2003) Consistent intensity correction of MR imagesImage Processing, 2003 ICIP 2003 Proceedings 2003 International Conference on. IEEE, pp I-1109 Hellier P (2003) Consistent intensity correction of MR imagesImage Processing, 2003 ICIP 2003 Proceedings 2003 International Conference on. IEEE, pp I-1109
18.
go back to reference Miwa K, Inubushi M, Wagatsuma K et al (2014) FDG uptake heterogeneity evaluated by fractal analysis improves the differential diagnosis of pulmonary nodules. Eur J Radiol 83:715–719CrossRef Miwa K, Inubushi M, Wagatsuma K et al (2014) FDG uptake heterogeneity evaluated by fractal analysis improves the differential diagnosis of pulmonary nodules. Eur J Radiol 83:715–719CrossRef
19.
go back to reference Hayano K, Yoshida H, Zhu AX, Sahani DV (2014) Fractal analysis of contrast-enhanced CT images to predict survival of patients with hepatocellular carcinoma treated with sunitinib. Dig Dis Sci 59:1996–2003CrossRefPubMed Hayano K, Yoshida H, Zhu AX, Sahani DV (2014) Fractal analysis of contrast-enhanced CT images to predict survival of patients with hepatocellular carcinoma treated with sunitinib. Dig Dis Sci 59:1996–2003CrossRefPubMed
20.
go back to reference Hayano K, Lee SH, Yoshida H, Zhu AX, Sahani DV (2014) Fractal analysis of CT perfusion images for evaluation of antiangiogenic treatment and survival in hepatocellular carcinoma. Acad Radiol 21:654–660CrossRefPubMed Hayano K, Lee SH, Yoshida H, Zhu AX, Sahani DV (2014) Fractal analysis of CT perfusion images for evaluation of antiangiogenic treatment and survival in hepatocellular carcinoma. Acad Radiol 21:654–660CrossRefPubMed
21.
go back to reference Breki CM, Dimitrakopoulou-Strauss A, Hassel J et al (2016) Fractal and multifractal analysis of PET/CT images of metastatic melanoma before and after treatment with ipilimumab. EJNMMI Res 6:61 Breki CM, Dimitrakopoulou-Strauss A, Hassel J et al (2016) Fractal and multifractal analysis of PET/CT images of metastatic melanoma before and after treatment with ipilimumab. EJNMMI Res 6:61
22.
go back to reference Cha S (2006) Update on brain tumor imaging: from anatomy to physiology. AJNR Am J Neuroradiol 27:475–487 Cha S (2006) Update on brain tumor imaging: from anatomy to physiology. AJNR Am J Neuroradiol 27:475–487
23.
go back to reference Inda MM, Bonavia R, Seoane J (2014) Glioblastoma multiforme: a look inside its heterogeneous nature. Cancers (Basel) 6:226–239CrossRef Inda MM, Bonavia R, Seoane J (2014) Glioblastoma multiforme: a look inside its heterogeneous nature. Cancers (Basel) 6:226–239CrossRef
24.
go back to reference Yasar F, Akgünlü F (2005) Fractal dimension and lacunarity analysis of dental radiographs. Dentomaxillofac Radiol 34:261–267CrossRef Yasar F, Akgünlü F (2005) Fractal dimension and lacunarity analysis of dental radiographs. Dentomaxillofac Radiol 34:261–267CrossRef
25.
go back to reference Karperien A, Jelinek H, Milosevic N (2011) Reviewing lacunarity analysis and classification of microglia in neuroscience. 8th European Conference on Mathematical and Theoretical Biology, Poland Karperien A, Jelinek H, Milosevic N (2011) Reviewing lacunarity analysis and classification of microglia in neuroscience. 8th European Conference on Mathematical and Theoretical Biology, Poland
26.
go back to reference Haldorsen IS, Kråkenes J, Krossnes BK, Mella O, Espeland A (2009) CT and MR imaging features of primary central nervous system lymphoma in Norway, 1989-2003. AJNR Am J Neuroradiol 30:744–751CrossRefPubMed Haldorsen IS, Kråkenes J, Krossnes BK, Mella O, Espeland A (2009) CT and MR imaging features of primary central nervous system lymphoma in Norway, 1989-2003. AJNR Am J Neuroradiol 30:744–751CrossRefPubMed
27.
go back to reference Küker W, Nägele T, Korfel A et al (2005) Primary central nervous system lymphomas (PCNSL): MRI features at presentation in 100 patients. J Neurooncol 72:169–177CrossRefPubMed Küker W, Nägele T, Korfel A et al (2005) Primary central nervous system lymphomas (PCNSL): MRI features at presentation in 100 patients. J Neurooncol 72:169–177CrossRefPubMed
28.
go back to reference Malikova H, Koubska E, Weichet J et al (2016) Can morphological MRI differentiate between primary central nervous system lymphoma and glioblastoma? Cancer Imaging 16:40CrossRefPubMedPubMedCentral Malikova H, Koubska E, Weichet J et al (2016) Can morphological MRI differentiate between primary central nervous system lymphoma and glioblastoma? Cancer Imaging 16:40CrossRefPubMedPubMedCentral
30.
go back to reference Rubenstein J, Ferreri AJ, Pittaluga S (2008) Primary lymphoma of the central nervous system: epidemiology, pathology and current approaches to diagnosis, prognosis and treatment. Leuk Lymphoma 49(Suppl 1):43–51CrossRefPubMedPubMedCentral Rubenstein J, Ferreri AJ, Pittaluga S (2008) Primary lymphoma of the central nervous system: epidemiology, pathology and current approaches to diagnosis, prognosis and treatment. Leuk Lymphoma 49(Suppl 1):43–51CrossRefPubMedPubMedCentral
31.
go back to reference Li H, Giger ML, Olopade OI, Lan L (2007) Fractal analysis of mammographic parenchymal patterns in breast cancer risk assessment. Acad Radiol 14:513–521CrossRefPubMed Li H, Giger ML, Olopade OI, Lan L (2007) Fractal analysis of mammographic parenchymal patterns in breast cancer risk assessment. Acad Radiol 14:513–521CrossRefPubMed
Metadata
Title
MR imaging based fractal analysis for differentiating primary CNS lymphoma and glioblastoma
Authors
Shuai Liu
Xing Fan
Chuanbao Zhang
Zheng Wang
Shaowu Li
Yinyan Wang
Xiaoguang Qiu
Tao Jiang
Publication date
01-03-2019
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 3/2019
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-018-5658-x

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