Skip to main content
Log in

Quantifying H&E staining results, grading and predicting IDH mutation status of gliomas using hybrid multi-dimensional MRI

  • Research Article
  • Published:
Magnetic Resonance Materials in Physics, Biology and Medicine Aims and scope Submit manuscript

Abstract

Objective

To assess the performance of hybrid multi-dimensional magnetic resonance imaging (HM-MRI) in quantifying hematoxylin and eosin (H&E) staining results, grading and predicting isocitrate dehydrogenase (IDH) mutation status of gliomas.

Materials and methods

Included were 71 glioma patients (mean age, 50.17 ± 13.38 years; 35 men). HM-MRI images were collected at five different echo times (80–200 ms) with seven b-values (0–3000 s/mm2). A modified three-compartment model with very-slow, slow and fast diffusion components was applied to calculate HM-MRI metrics, including fractions, diffusion coefficients and T2 values of each component. Pearson correlation analysis was performed between HM-MRI derived fractions and H&E staining derived percentages. HM-MRI metrics were compared between high-grade and low-grade gliomas, and between IDH-wild and IDH-mutant gliomas. Using receiver operational characteristic (ROC) analysis, the diagnostic performance of HM-MRI in grading and genotyping was compared with mono-exponential models.

Results

HM-MRI metrics FDvery-slow and FDslow demonstrated a significant correlation with the H&E staining results (p < .05). Besides, FDvery-slow showed the highest area under ROC curve (AUC = 0.854) for grading, while Dslow showed the highest AUC (0.845) for genotyping. Furthermore, a combination of HM-MRI metrics FDvery-slow and T2Dslow improved the diagnostic performance for grading (AUC = 0.876).

Discussion

HM-MRI can aid in non-invasive diagnosis of gliomas.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

For ethical considerations, the data supporting the study's conclusions are not publicly available; however, they are available from the corresponding author upon appropriate request. 

Abbreviations

CNS:

Central nervous system

DWI:

Diffusion weighted imaging

IDH:

Isocitrate dehydrogenase

ADC:

Apparent diffusion coefficient

LGG:

Low-grade glioma

HGG:

High-grade glioma

IDH-MUT:

IDH-mutant glioma

IDH-WILD:

IDH-wild glioma

HM-MRI:

Hybrid multi-dimensional MRI

GRE:

Gradient echo

TR:

Repetition time

TE:

Echo time

FOV:

Field of view

FSE:

Fast spin echo

FLAIR:

Fluid-attenuated inversion recovery

EES:

Extravascular extracellular space

BBB:

Brain-blood barrier

ROI:

Regions of interest

IHC:

Immune-histochemical

ROC:

Receiver operating characteristic

AUC:

Area under the receiver operating characteristic curve

LR:

Logistic regression

WHO:

World Health Organization

H&E:

Hematoxylin and eosin 

AQP4:

aquaporin-4

References

  1. Burgenske DM, Yang J, Decker PA et al (2019) Molecular profiling of long-term IDH-wildtype glioblastoma survivors. Neuro Oncol. https://doi.org/10.1093/neuonc/noz129

    Article  PubMed  PubMed Central  Google Scholar 

  2. Gritsch S, Batchelor TT, Gonzalez Castro LN (2022) Diagnostic, therapeutic, and prognostic implications of the 2021 World Health Organization classification of tumors of the central nervous system. Cancer. https://doi.org/10.1002/cncr.33918

    Article  PubMed  Google Scholar 

  3. Komori T (2022) Grading of adult diffuse gliomas according to the 2021 WHO classification of tumors of the central nervous system. Lab Invest. https://doi.org/10.1038/s41374-021-00667-6

    Article  PubMed  Google Scholar 

  4. Louis DN, Perry A, Wesseling P et al (2021) The 2021 WHO classification of tumors of the central nervous system: a summary. Neuro Oncol. https://doi.org/10.1093/neuonc/noab106

    Article  PubMed  PubMed Central  Google Scholar 

  5. Uribe-Cardenas R, Giantini-Larsen AM, Garton A, Juthani RG, Schwartz TH (2022) Innovations in the diagnosis and surgical management of low-grade gliomas. World Neurosurg. https://doi.org/10.1016/j.wneu.2022.06.070

    Article  PubMed  Google Scholar 

  6. Szychot E, Youssef A, Ganeshan B et al (2021) Predicting outcome in childhood diffuse midline gliomas using magnetic resonance imaging based texture analysis. J Neuroradiol. https://doi.org/10.1016/j.neurad.2020.02.005

    Article  PubMed  Google Scholar 

  7. Narvaez O, Svenningsson L, Yon M, Sierra A, Topgaard D (2022) Massively multi-dimensional diffusion-relaxation correlation MRI. Front Phys. https://doi.org/10.3389/fphy.2021.793966

    Article  Google Scholar 

  8. Jalnefjord O, Andersson M, Montelius M et al (2018) Comparison of methods for estimation of the intravoxel incoherent motion (IVIM) diffusion coefficient (D) and perfusion fraction (f). MAGMA. https://doi.org/10.1007/s10334-018-0697-5

    Article  PubMed  Google Scholar 

  9. Hu LS, Hawkins-Daarud A, Wang L, Li J, Swanson KR (2020) Imaging of intratumoral heterogeneity in high-grade glioma. Cancer Lett. https://doi.org/10.1016/j.canlet.2020.02.025

    Article  PubMed  PubMed Central  Google Scholar 

  10. Guo D, Jiang B (2023) 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. Eur J Radiol. https://doi.org/10.1016/j.ejrad.2023.110721

    Article  PubMed  Google Scholar 

  11. Maynard J, Okuchi S, Wastling S et al (2020) World Health Organization grade II/III glioma molecular status: prediction by MRI morphologic features and apparent diffusion coefficient. Radiology. https://doi.org/10.1148/radiol.2020191832

    Article  PubMed  Google Scholar 

  12. Gu W, Fang S, Hou X, Ma D, Li S (2021) Exploring diagnostic performance of T2 mapping in diffuse glioma grading. Quant Imaging Med Surg. https://doi.org/10.21037/qims-20-916

    Article  PubMed  PubMed Central  Google Scholar 

  13. Kern M, Auer TA, Picht T, Misch M, Wiener E (2020) T2 mapping of molecular subtypes of WHO grade II/III gliomas. BMC Neurol. https://doi.org/10.1186/s12883-019-1590-1

    Article  PubMed  PubMed Central  Google Scholar 

  14. Cao M, Ding W, Han X et al (2019) Brain T1ρ mapping for grading and IDH1 gene mutation detection of gliomas: a preliminary study. J Neurooncol. https://doi.org/10.1007/s11060-018-03033-7

    Article  PubMed  Google Scholar 

  15. Springer E, Cardoso PL, Strasser B et al (2022) MR fingerprinting—a radiogenomic marker for diffuse gliomas. Cancers (Basel). https://doi.org/10.3390/cancers14030723

    Article  PubMed  PubMed Central  Google Scholar 

  16. Auer TA, Kern M, Fehrenbach U et al (2021) T2 mapping of the peritumoral infiltration zone of glioblastoma and anaplastic astrocytoma. Neuroradiol J. https://doi.org/10.1177/1971400921989325

    Article  PubMed  PubMed Central  Google Scholar 

  17. Bontempi P, Rozzanigo U, Amelio D et al (2021) Quantitative multicomponent T2 relaxation showed greater sensitivity than flair imaging to detect subtle alterations at the periphery of lower grade gliomas. Front Oncol. https://doi.org/10.3389/fonc.2021.651137

    Article  PubMed  PubMed Central  Google Scholar 

  18. Toh CH, Chen YL, Hsieh TC et al (2006) Glioblastoma multiforme with diffusion-weighted magnetic resonance imaging characteristics mimicking primary brain lymphoma. case report. J Neurosurg. https://doi.org/10.3171/jns.2006.105.1.132

    Article  PubMed  Google Scholar 

  19. Kim Y, Lee SK, Kim JY, Kim JH (2023) Pitfalls of diffusion-weighted imaging: clinical utility of T2 shine-through and T2 black-out for musculoskeletal diseases. Diagnostics (Basel). https://doi.org/10.3390/diagnostics13091647

    Article  PubMed  PubMed Central  Google Scholar 

  20. Chatterjee A, Mercado C, Bourne RM et al (2022) Validation of prostate tissue composition by using hybrid multi-dimensional MRI: correlation with histologic findings. Radiology. https://doi.org/10.1148/radiol.2021204459

    Article  PubMed  Google Scholar 

  21. Chatterjee A, Antic T, Gallan AJ et al (2022) Histological validation of prostate tissue composition measurement using hybrid multi-dimensional MRI: agreement with pathologists’ measures. Abdom Radiol (NY). https://doi.org/10.1007/s00261-021-03371-7

    Article  PubMed  Google Scholar 

  22. Lee GH, Chatterjee A, Karademir I et al (2022) Comparing radiologist performance in diagnosing clinically significant prostate cancer with multiparametric versus hybrid multi-dimensional MRI. Radiology. https://doi.org/10.1148/radiol.211895

    Article  PubMed  PubMed Central  Google Scholar 

  23. Zeng Q, Shi F, Zhang J, Ling C, Dong F, Jiang B (2018) A modified tri-exponential model for multi-b-value diffusion-weighted imaging: a method to detect the strictly diffusion-limited compartment in brain. Front Neurosci. https://doi.org/10.3389/fnins.2018.00102

    Article  PubMed  PubMed Central  Google Scholar 

  24. Cao M, Wang X, Liu F, Xue K, Dai Y, Zhou Y (2023) A three-component multi-b-value diffusion-weighted imaging might be a useful biomarker for detecting microstructural features in gliomas with differences in malignancy and IDH-1 mutation status. Eur Radiol. https://doi.org/10.1007/s00330-022-09212-5

    Article  PubMed  PubMed Central  Google Scholar 

  25. Yushkevich PA, Piven J, Hazlett HC et al (2006) User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage. https://doi.org/10.1016/j.neuroimage.2006.01.015

    Article  PubMed  Google Scholar 

  26. Boruah D, Deb P, Srinivas V, Mani NS (2014) Morphometric study of nuclei and microvessels in gliomas and its correlation with grades. Microvasc Res. https://doi.org/10.1016/j.mvr.2014.03.002

    Article  PubMed  Google Scholar 

  27. Zaccagna F, Riemer F, Priest AN et al (2019) Non-invasive assessment of glioma microstructure using VERDICT MRI: correlation with histology. Eur Radiol. https://doi.org/10.1007/s00330-019-6011-8

    Article  PubMed  PubMed Central  Google Scholar 

  28. Raja R, Rosenberg GA, Caprihan A (2018) MRI measurements of blood-brain barrier function in dementia: a review of recent studies. Neuropharmacology. https://doi.org/10.1016/j.neuropharm.2017.10.034

    Article  PubMed  Google Scholar 

  29. Yan H, Parsons DW, Jin G et al (2009) IDH1 and IDH2 mutations in gliomas. N Engl J Med. https://doi.org/10.1056/NEJMoa0808710

    Article  PubMed  PubMed Central  Google Scholar 

  30. Furtado FS, Mercaldo ND, Vahle T et al (2023) Simultaneous multislice diffusion-weighted imaging versus standard diffusion-weighted imaging in whole-body PET/MRI. Eur Radiol. https://doi.org/10.1007/s00330-022-09275-4

    Article  PubMed  Google Scholar 

  31. Slator PJ, Palombo M, Miller KL et al (2021) Combined diffusion-relaxometry microstructure imaging: current status and future prospects. Magn Reson Med. https://doi.org/10.1002/mrm.28963

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was partly supported by the National NSFC International (regional) Cooperation and Exchange Project (Grant No. 82111530204), partly supported by Swedish Foundation for International Cooperation in Research and Higher Education (Grant No. CH2020-8775), and partly supported by Hubei Provincial Natural Science Foundation of China (Grant No. 2021CFB099).

Author information

Authors and Affiliations

Authors

Contributions

Wenbo Sun: investigation; data curation; validation; writing—original draft; visualization; formal analysis. Dan Xu: investigation; data curation; validation; writing—original draft; visualization; formal analysis. Huan Li: data curation; project administration. Sirui Li: investigation; methodology. QingJia Bao: writing—review & editing; resources. Xiaopeng Song: software; resources. Daniel Topgaard: supervision; conceptualization; funding acquisition; writing-review & editing. Haibo Xu: supervision; conceptualization; funding acquisition; writing—review & editing.

Corresponding authors

Correspondence to Daniel Topgaard or Haibo Xu.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Ethical statement

All enrolled subjects provided informed consent, and the ethics committee of our hospital approved this prospective study (Ethics number 2020109). 

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sun, W., Xu, D., Li, H. et al. Quantifying H&E staining results, grading and predicting IDH mutation status of gliomas using hybrid multi-dimensional MRI. Magn Reson Mater Phy (2024). https://doi.org/10.1007/s10334-024-01154-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10334-024-01154-x

Keywords

Navigation