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Radiomic analysis of magnetic resonance fingerprinting in adult brain tumors

  • Original Article
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European Journal of Nuclear Medicine and Molecular Imaging Aims and scope Submit manuscript

Abstract

Purpose

This is a radiomics study investigating the ability of texture analysis of MRF maps to improve differentiation between intra-axial adult brain tumors and to predict survival in the glioblastoma cohort.

Methods

Magnetic resonance fingerprinting (MRF) acquisition was performed on 31 patients across 3 groups: 17 glioblastomas, 6 low-grade gliomas, and 8 metastases. Using regions of interest for the solid tumor and peritumoral white matter on T1 and T2 maps, second-order texture features were calculated from gray-level co-occurrence matrices and gray-level run length matrices. Selected features were compared across the three tumor groups using Wilcoxon rank-sum test. Receiver operating characteristic curve analysis was performed for each feature. Kaplan-Meier method was used for survival analysis with log rank tests.

Results

Low-grade gliomas and glioblastomas had significantly higher run percentage, run entropy, and information measure of correlation 1 on T1 than metastases (p < 0.017). The best separation of all three tumor types was seen utilizing inverse difference normalized and homogeneity values for peritumoral white matter in both T1 and T2 maps (p < 0.017). In solid tumor T2 maps, lower values in entropy and higher values of maximum probability and high-gray run emphasis were associated with longer survival in glioblastoma patients (p < 0.05). Several texture features were associated with longer survival in glioblastoma patients on peritumoral white matter T1 maps (p < 0.05).

Conclusion

Texture analysis of MRF-derived maps can improve our ability to differentiate common adult brain tumors by characterizing tumor heterogeneity, and may have a role in predicting outcomes in patients with glioblastoma.

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Data availability

Upon reasonable request.

Abbreviations

AUC:

area under the curve

GLCM:

gray-level co-occurrence matrix

IMC1:

information measure of correlation 1

LGG:

lower grade glioma

MR:

magnetic resonance

MRF:

magnetic resonance fingerprinting

OS:

overall survival

ROC:

receiver operating characteristic

ROI:

region of interest

ST:

solid tumor

PW:

peritumoral white matter

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Funding

This work was supported by National Institutes of Health 1R01BB017219 award (Principal Investigator: Dr. Mark Griswold) and 1R01EB016728 award (Principal Investigators: Drs. Mark Griswold and Vikas Gulani). This project was also supported by the Clinical and Translational Science Collaborative (CTSC) of Cleveland which is funded by the National Institutes of Health (NIH), National Center for Advancing Translational Science (NCATS), Clinical and Translational Science Award (CTSA) grant, UL1TR002548 (Principal Investigator: Dr. Chaitra Badve). AES is supported by NIH CA217956, the Peter D Cristal Chair, the Center of Excellence for Translational Neuro-Oncology, the Gerald R. Kaufman Fund for Glioma Research at University Hospitals of Cleveland, the Kimble Family Foundation, and the Ferry Family Foundation at University Hospitals of Cleveland. The content is solely the responsibility of the authors and do not necessarily represent the official views of the NIH.

Author information

Author notes

  1. Sara Dastmalchian and Ozden Kilinc contributed equally to this work.

Authors and Affiliations

  1. Department of Radiology, Case Western Reserve University and University Hospitals of Cleveland, 11100 Euclid Ave, Cleveland, OH, 44106, USA

    Sara Dastmalchian, Ozden Kilinc, Mark Griswold, Jeffrey Sunshine & Chaitra Badve

  2. Case Western Reserve University School of Medicine, 11100 Euclid Ave, Cleveland, OH, 44106, USA

    Louisa Onyewadume & Charit Tippareddy

  3. Department of Biomedical Engineering, Case Western Reserve University, 11100 Euclid Ave, Cleveland, OH, 44106, USA

    Debra McGivney, Dan Ma & Mark Griswold

  4. Department of Radiology, University of Michigan, 1500 E. Medical Center Dr, B1G503, Ann Arbor, MI, 48109-5030, USA

    Vikas Gulani

  5. Department of Population and Quantitative Health Sciences, Case Western Reserve University School of Medicine, Wolstein Research Bldg. 2526, 2103 Cornell Rd, Cleveland, OH, 44106, USA

    Jill S. Barnholtz-Sloan

  6. Departments of Neurosurgery and Pathology, Case Western Reserve University, University Hospitals Cleveland Medical Center, 11100 Euclid Ave, Cleveland, OH, 44106, USA

    Andrew E. Sloan

  7. Seidman Cancer Center and Case Comprehensive Cancer Center, 11100 Euclid Ave, Cleveland, OH, 44106, USA

    Andrew E. Sloan

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  1. Sara Dastmalchian
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Contributions

All of the following authors have contributed substantially to the submitted work.

Sara Dastmalchian:

• Contributed equally to this work as: Ozden Kilinc.

• Substantial contributions to the conception and design of the work; the acquisition, analysis, and interpretation of data for the work;

• Drafting the manuscript and revising it critically for important intellectual content;

• Final approval of the version to be published;

• Agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Ozden Kilinc:

• Contributed equally to this work as: Sara Dastmalchian.

• Substantial contributions to the conception and design of the work; the acquisition, analysis, and interpretation of data for the work;

• Drafting the manuscript and revising it critically for important intellectual content;

• Final approval of the version to be published;

• Agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Louisa Onyewadume:

• Substantial contributions to the analysis and interpretation of data for the work;

• Revising the manuscript critically for important intellectual content;

• Final approval of the version to be published;

• Agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Charit Tippareddy:

• Substantial contributions to the analysis and interpretation of data for the work;

• Drafting the manuscript and revising it critically for important intellectual content;

• Final approval of the version to be published;

• Agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Debra McGivney:

• Substantial contributions to the conception and design of the work, analysis, and interpretation of data for the work;

• Revising the manuscript critically for important intellectual content;

• Final approval of the version to be published;

• Agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Dan Ma:

• Substantial contributions to the conception and design of the work; and the acquisition and analysis of data for the work;

• Revising the manuscript critically for important intellectual content;

• Final approval of the version to be published;

• Agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Mark Griswold:

• Substantial contributions to the conception and design of the work; and the acquisition of data for the work;

• Revising the manuscript critically for important intellectual content;

• Final approval of the version to be published;

• Agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Jeffrey Sunshine:

• Substantial contributions to the conception and design of the work;

• Revising the manuscript critically for important intellectual content;

• Final approval of the version to be published;

• Agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Vikas Gulani:

• Substantial contributions to the conception and design of the work; and the acquisition of data for the work;

• Revising the manuscript critically for important intellectual content;

• Final approval of the version to be published;

• Agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Jill S. Barnholtz-Sloan:

• Substantial contributions to the conception and design of the work; analysis, and interpretation of data for the work;

• Revising the manuscript critically for important intellectual content;

• Final approval of the version to be published;

• Agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Andrew E. Sloan:

• Substantial contributions to the conception and design of the work; and the acquisition of data for the work;

• Revising the manuscript critically for important intellectual content;

• Final approval of the version to be published;

• Agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Chaitra Badve:

• Substantial contributions to the conception and design of the work; the acquisition, analysis, and interpretation of data for the work;

• Drafting the manuscript and revising it critically for important intellectual content;

• Final approval of the version to be published;

• Agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Corresponding author

Correspondence to Chaitra Badve.

Ethics declarations

Conflict of interest

Case Western Reserve University and University Hospitals receive research support from Siemens. Chaitra Badve, Dan Ma, Andrew E. Sloan, Jeffrey Sunshine, Mark Griswold, and Vikas Gulani have patent applications on MRF applications in brain tumors.

Sara Dastmalchian, Ozden Kilinc, Louisa Onyewadume, Charit Tippareddy, Debra McGivney, Jill Barnholtz-Sloan do not have any relevant conflicts of interest to disclose.

Ethics approval

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.

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Informed consent was obtained from all individual participants included in the study.

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Not applicable.

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Dastmalchian, S., Kilinc, O., Onyewadume, L. et al. Radiomic analysis of magnetic resonance fingerprinting in adult brain tumors. Eur J Nucl Med Mol Imaging 48, 683–693 (2021). https://doi.org/10.1007/s00259-020-05037-w

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