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Diffusion-weighted imaging and arterial spin labeling radiomics features may improve differentiation between radiation-induced brain injury and glioma recurrence

  • Magnetic Resonance
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objectives

To determine whether radiomics features derived from diffusion-weighted imaging (DWI) and arterial spin labeling (ASL) can improve the differentiation between radiation-induced brain injury (RIBI) and tumor recurrence (TR) in glioma patients.

Methods

A total of 4199 radiomics features were extracted from conventional MRI, apparent diffusion coefficient (ADC), and cerebral blood flow (CBF) maps, obtained from 96 pathologically confirmed WHO grade 2~4 gliomas with enhancement after standard treatment. The intraclass correlation coefficient (ICC) was used to test segmentation stability between two doctors. Radiomics features were selected using the Mann–Whitney U test, LASSO regression, and RFE algorithms. Four machine learning classifiers were adopted to establish radiomics models. The diagnostic performance of multiparameter, conventional, and single-parameter MRI radiomics models was compared using the area under the curve (AUC). The models were evaluated in the subsequent independent validation set (n = 30).

Results

Eight important radiomics features (3 from conventional MRI, 1 from ADC, and 4 from CBF) were selected. Support vector machine (SVM) was chosen as the optimal classifier. The diagnostic performance of the multiparameter MRI radiomics model (AUC 0.96) was higher than that of the conventional MRI (AUC 0.88), ADC (AUC 0.91), and CBF (AUC 0.95) radiomics models. For subgroup analysis, the multiparameter MRI radiomics model showed similar performance, with AUCs of 0.98 in WHO grade 2~3 and 0.96 in WHO grade 4.

Conclusion

The incorporation of noninvasive DWI and ASL into the MRI radiomics model improved the diagnostic performance in differentiating RIBI from TR; ASL, especially, played a significant role.

Key Points

• The multiparameter MRI radiomics model was superior to the conventional MRI radiomics model in differentiating glioma recurrence from radiation-induced brain injury.

• Diffusion and perfusion MRI could improve the ability of the radiomics model in predicting the progression in patients with glioma.

• Arterial spin labeling played an important role in predicting glioma progression using radiomics models.

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Abbreviations

ADC:

Apparent diffusion coefficient

ASL:

Arterial spin labeling

AUC:

Area under the receiver operating characteristics curve

BBB:

Blood–brain barrier

CBF:

Cerebral blood flow

CE:

Contrast-enhanced

DSC:

Dynamic susceptibility contrast-enhanced

DWI:

Diffusion-weighted imaging

GLCM:

Gray-level co-occurrence matrix

GLRLM:

Gray-level run-length matrix

GLSZM:

Gray-level size zone matrix

ICC:

Intraclass correlation coefficient

IDH:

Isocitrate dehydrogenase

KNN:

K-nearest neighbor

LASSO:

Least absolute shrinkage and selection operator

LR:

Logistic regression

MRS:

Magnetic resonance spectroscopy

NB:

Naive Bayes

PsP:

Pseudoprogression

RFE:

Recursive feature elimination

RIBI:

Radiation-induced brain injury

RN:

Radiation necrosis

ROC:

Receiver operating characteristic curves

ROI :

Regions of interest

SVM:

Support vector machine

TMZ:

Temozolomide

TR:

Tumor recurrence

References

  1. Ostrom QT, Cioffi G, Waite K, Kruchko C, Barnholtz-Sloan JS (2021) CBTRUS Statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2014-2018. Neuro Oncol 23:i1–i105

    Article  Google Scholar 

  2. Weller M, van den Bent M, Preusser M et al (2021) EANO guidelines on the diagnosis and treatment of diffuse gliomas of adulthood. Nat Rev Clin Oncol 18:170–186

    Article  PubMed  Google Scholar 

  3. Stupp R, Mason WP, van den Bent MJ et al (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996

    Article  CAS  PubMed  Google Scholar 

  4. Parvez K, Parvez A, Zadeh G (2014) The diagnosis and treatment of pseudoprogression, radiation necrosis and brain tumor recurrence. Int J Mol Sci 15:11832–11846

    Article  PubMed  PubMed Central  Google Scholar 

  5. Radbruch A, Fladt J, Kickingereder P et al (2015) Pseudoprogression in patients with glioblastoma: clinical relevance despite low incidence. Neuro Oncol 17:151–159

    Article  PubMed  Google Scholar 

  6. Wilson CB, Crafts D, Levin V (1977) Brain tumors: criteria of response and definition of recurrence. Natl Cancer Inst Monogr 46:197–203

    CAS  PubMed  Google Scholar 

  7. Furuse M, Nonoguchi N, Kawabata S, Miyatake S, Kuroiwa T (2015) Delayed brain radiation necrosis: pathological review and new molecular targets for treatment. Med Mol Morphol 48:183–190

    Article  CAS  PubMed  Google Scholar 

  8. Abbasi AW, Westerlaan HE, Holtman GA, Aden KM, van Laar PJ, van der Hoorn A (2018) Incidence of tumour progression and pseudoprogression in high-grade gliomas: a systematic review and meta-analysis. Clin Neuroradiol 28:401–411

    Article  PubMed  Google Scholar 

  9. van West SE, de Bruin HG, van de Langerijt B, Swaak-Kragten AT, van den Bent MJ, Taal W (2017) Incidence of pseudoprogression in low-grade gliomas treated with radiotherapy. Neuro Oncol 19:719–725

    PubMed  Google Scholar 

  10. Zhou H, Vallieres M, Bai HX et al (2017) MRI features predict survival and molecular markers in diffuse lower-grade gliomas. Neuro Oncol 19:862–870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Prager AJ, Martinez N, Beal K, Omuro A, Zhang Z, Young RJ (2015) Diffusion and perfusion MRI to differentiate treatment-related changes including pseudoprogression from recurrent tumors in high-grade gliomas with histopathologic evidence. AJNR Am J Neuroradiol 36:877–885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Kim JY, Park JE, Jo Y et al (2019) Incorporating diffusion- and perfusion-weighted MRI into a radiomics model improves diagnostic performance for pseudoprogression in glioblastoma patients. Neuro Oncol 21:404–414

    Article  PubMed  Google Scholar 

  13. Grade M, Hernandez TJ, Pizzini FB, Achten E, Golay X, Smits M (2015) A neuroradiologist’s guide to arterial spin labeling MRI in clinical practice. Neuroradiology 57:1181–1202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Thust SC, van den Bent MJ, Smits M (2018) Pseudoprogression of brain tumors. J Magn Reson Imaging 48:571–589

  15. Jovanovic M, Radenkovic S, Stosic-Opincal T et al (2017) Differentiation between progression and pseudoprogresion by arterial spin labeling MRI in patients with glioblastoma multiforme. J BUON 22:1061–1067

    PubMed  Google Scholar 

  16. Manning P, Daghighi S, Rajaratnam MK et al (2020) Differentiation of progressive disease from pseudoprogression using 3D PCASL and DSC perfusion MRI in patients with glioblastoma. J Neurooncol 147:681–690

    Article  PubMed  Google Scholar 

  17. Razek A, El-Serougy L, Abdelsalam M, Gaballa G, Talaat M (2018) Differentiation of residual/recurrent gliomas from postradiation necrosis with arterial spin labeling and diffusion tensor magnetic resonance imaging-derived metrics. Neuroradiology 60:169–177

    Article  PubMed  Google Scholar 

  18. Ozsunar Y, Mullins ME, Kwong K et al (2010) Glioma recurrence versus radiation necrosis? A pilot comparison of arterial spin-labeled, dynamic susceptibility contrast enhanced MRI, and FDG-PET imaging. Acad Radiol 17:282–290

    Article  PubMed  Google Scholar 

  19. Lambin P, Leijenaar R, Deist TM et al (2017) Radiomics: the bridge between medical imaging and personalized medicine. Nat Rev Clin Oncol 14:749–762

    Article  PubMed  Google Scholar 

  20. Wen PY, Macdonald DR, Reardon DA et al (2010) Updated response assessment criteria for high-grade gliomas: response assessment in neuro-oncology working group. J Clin Oncol 28:1963–1972

    Article  PubMed  Google Scholar 

  21. Chukwueke UN, Wen PY (2019) Use of the Response Assessment in Neuro-Oncology (RANO) criteria in clinical trials and clinical practice. CNS Oncol 8:S28

    Article  Google Scholar 

  22. Hepp T, Schmid M, Gefeller O, Waldmann E, Mayr A (2016) Approaches to regularized regression - a comparison between gradient boosting and the Lasso. Methods Inf Med 55:422–430

    Article  PubMed  Google Scholar 

  23. Cha J, Kim ST, Kim HJ et al (2014) Differentiation of tumor progression from pseudoprogression in patients with posttreatment glioblastoma using multiparametric histogram analysis. AJNR Am J Neuroradiol 35:1309–1317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Kong DS, Kim ST, Kim EH et al (2011) Diagnostic dilemma of pseudoprogression in the treatment of newly diagnosed glioblastomas: the role of assessing relative cerebral blood flow volume and oxygen-6-methylguanine-DNA methyltransferase promoter methylation status. AJNR Am J Neuroradiol 32:382–387

    Article  PubMed  PubMed Central  Google Scholar 

  25. Song YS, Choi SH, Park CK et al (2013) True progression versus pseudoprogression in the treatment of glioblastomas: a comparison study of normalized cerebral blood volume and apparent diffusion coefficient by histogram analysis. Korean J Radiol 14:662–672

    Article  PubMed  PubMed Central  Google Scholar 

  26. Lee WJ, Choi SH, Park CK et al (2012) Diffusion-weighted MR imaging for the differentiation of true progression from pseudoprogression following concomitant radiotherapy with temozolomide in patients with newly diagnosed high-grade gliomas. Acad Radiol 19:1353–1361

    Article  PubMed  Google Scholar 

  27. Thomsen H, Steffensen E, Larsson EM (2012) Perfusion MRI (dynamic susceptibility contrast imaging) with different measurement approaches for the evaluation of blood flow and blood volume in human gliomas. Acta Radiol 53:95–101

    Article  CAS  PubMed  Google Scholar 

  28. Patel M, Zhan J, Natarajan K et al (2021) Machine learning-based radiomic evaluation of treatment response prediction in glioblastoma. Clin Radiol 76:617–628

    Article  Google Scholar 

  29. Reimer C, Deike K, Graf M et al (2017) Differentiation of pseudoprogression and real progression in glioblastoma using ADC parametric response maps. PLoS One 12:e174620

    Article  Google Scholar 

  30. Choi YJ, Kim HS, Jahng GH, Kim SJ, Suh DC (2013) Pseudoprogression in patients with glioblastoma: added value of arterial spin labeling to dynamic susceptibility contrast perfusion MR imaging. Acta Radiologica 54:448–454

    Article  PubMed  Google Scholar 

  31. Wang YL, Chen S, Xiao HF et al (2018) Differentiation between radiation-induced brain injury and glioma recurrence using 3D pCASL and dynamic susceptibility contrast-enhanced perfusion-weighted imaging. Radiother Oncol 129:68–74

    Article  PubMed  Google Scholar 

  32. Gutsche R, Scheins J, Kocher M et al (2021) Evaluation of FET PET radiomics feature repeatability in glioma patients. Cancers (Basel) 13

  33. Chang PD, Malone HR, Bowden SG et al (2017) A multiparametric model for mapping cellularity in glioblastoma using radiographically localized biopsies. AJNR Am J Neuroradiol 38:890–898

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Materka A, Strzelecki M (1998) Texture analysis methods - a review. Institute of Electronics Technical University of Lodz

    Google Scholar 

  35. Su C, Jiang J, Zhang S et al (2019) Radiomics based on multicontrast MRI can precisely differentiate among glioma subtypes and predict tumour-proliferative behaviour. Eur Radiol 29:1986–1996

    Article  PubMed  Google Scholar 

  36. Ion-Margineanu A, Van Cauter S, Sima DM et al (2016) Classifying glioblastoma multiforme follow-up progressive vs. responsive forms using multi-parametric MRI features. Front Neurosci 10:615

  37. Hashido T, Saito S, Ishida T (2020) A radiomics-based comparative study on arterial spin labeling and dynamic susceptibility contrast perfusion-weighted imaging in gliomas. Sci Rep 10:6121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Tan Y, Zhang ST, Wei JW et al (2019) A radiomics nomogram may improve the prediction of IDH genotype for astrocytoma before surgery. Eur Radiol 29:3325–3337

    Article  PubMed  Google Scholar 

  39. Akbari H, Bakas S, Pisapia JM et al (2018) In vivo evaluation of EGFRvIII mutation in primary glioblastoma patients via complex multiparametric MRI signature. Neuro Oncol 20:1068–1079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by the National Key R&D Program of China (2019YFB1311600) and the National Natural Science Foundation of China (62072358).

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Correspondence to Liang Zhang or Lin Ma.

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Guarantor

The scientific guarantor of this publication is Lin Ma, MD.

Conflict of interests

The authors of this manuscript declare no relationship with any companies whose products or services may be related to the subject matter of the article.

Statistics and biometry

One of the authors has significant statistical expertise (Guangming Zhu, 8 years of experience).

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Written informed consent was waived by the Institutional Review Board.

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Institutional Review Board approval was obtained.

Methodology

• Retrospective

• Cross-sectional study

• Performed at one institution

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Jun Zhang and Yue Wu are co-first authors.

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Zhang, J., Wu, Y., Wang, Y. et al. Diffusion-weighted imaging and arterial spin labeling radiomics features may improve differentiation between radiation-induced brain injury and glioma recurrence. Eur Radiol 33, 3332–3342 (2023). https://doi.org/10.1007/s00330-022-09365-3

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  • DOI: https://doi.org/10.1007/s00330-022-09365-3

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