Magnetic Resonance Imaging in Studies of Perifocal Zone of Brain Gliomas (a Literature Review)
https://doi.org/10.52560/2713-0118-2024-1-20-36
Abstract
This review provides insight into application of modern MRI modalities including diffusion kurtosis imaging in assessment of perifocal glioma zone. Differentiation of “pure” perifocal vasogenic edema from edema infiltrated by glioma cells, as well as identification of peritumoral intact (on conventional MRI) brain matter infiltration make it possible to determine glial tumor borders more accurately. Analysis of diffusion and perfusion quantitative MR data allow determining glioma borders in areas with unaltered blood-brain barrier. There is a growing possibility to develop a personalized navigation algorithm for surgical removal of the tumor, followed by the determination of an individual plan for radiation and chemotherapy, as well as prediction of disease outcomes.
About the Authors
N. E. ZakharovaRussian Federation
Zakharova Natal’ya Evgen’evna, radiologist, PhD, professor RAS, Department of Neuroradiology
16, ul. 4-ya Tverskaya-Yamskaya, Moscow, 125047
+7 (499) 972-85-55
A. I. Batalov
Russian Federation
Batalov Artem Igorevich, radiologist, PhD, Department of Neuroradiology
16, ul. 4-ya Tverskaya-Yamskaya, Moscow, 125047
+7 (499) 972-85-55
E. L. Pogosbekyan
Russian Federation
Pogosbekyan Eduard Leonidovich, medical physicist, Department of Neuroradiology
16, ul. 4-ya Tverskaya-Yamskaya, Moscow, 125047
+7 (499) 972-85-55
S. A. Goryaynov
Russian Federation
Goryaynov Sergey Alexeevich, neurosurgeon, PhD
16, ul. 4-ya Tverskaya-Yamskaya, Moscow, 125047
+7 (499) 972-85-55
L. M. Fadeeva
Russian Federation
Fadeeva Liudmila Mikhaylovna, leading engineer, Department of Neuroradiology
16, ul. 4-ya Tverskaya-Yamskaya, Moscow, 125047
+7 (499) 972-85-55
A. E. Bykanov
Russian Federation
Bykanov Andrey Egorovich, neurosurgeon, PhD
16, ul. 4-ya Tverskaya-Yamskaya, Moscow, 125047
+7 (499) 972-85-55
A. N. Tyurina
Russian Federation
Tyurina Anastasia Nikolaevna, radiologist, PhD, Department of Neuroradiology
16, ul. 4-ya Tverskaya-Yamskaya, Moscow, 125047
+7 (499) 972-85-55
I. V. Chekhonin
Russian Federation
Chekhonin Ivan Vladimirovich, Ph. D. Med., radiologist, junior research associate, Department of Neuroradiology
16, ul. 4-ya Tverskaya-Yamskaya, Moscow, 125047
+7 (499) 972-85-55
S. A. Galstyan
Russian Federation
Galstyan Suzanna Andranikovna, pathologist
16, ul. 4-ya Tverskaya-Yamskaya, Moscow, 125047
+7 (499) 972-85-55
I. N. Pronin
Russian Federation
Pronin Igor Nikolaevich, М. D., D.Sci., Academician of the Russian Academy of Sciences, Head of Department of Neuroradiology
16, ul. 4-ya Tverskaya-Yamskaya, Moscow, 125047
+7 (499) 972-85-55
D. Yu. Usachev
Russian Federation
Usachev Dmitriy Yur’evich, MD, PhD, professor, academician of the Russian Academy of Sciences, director of the N. N. Burdenko National Medical Research Center of Neurosurgery of the Ministry of Health of the Russian Federation
16, ul. 4-ya Tverskaya-Yamskaya, Moscow, 125047
+7 (499) 972-85-55
References
1. Batalov A. I., Zakharova N. E., Pogosbekyan E. L., Fadeeva L. M., Goriaynov S. A., Baev A. A., Shul’ts E. I., Chelushkin D. M., Potapov A. A., Pronin I. N. Non-contrast ASL perfusion in preoperative diagnosis of supratentorial gliomas. Zhurnal Voprosy Neirokhirurgii Imeni N. N. Burdenko. 2018;82(6):15-22. (In Russ., in Engl.). https://doi.org/10.17116/neiro20188206115
2. Turkin A. M., Pogosbekyan E. L., Tonoyan A. S., Schults E. I., Maximov I. I., Dolgushin M. B., Khachanova N. V., Fadeeva L. M., Melnikova-Pitskhelauri T. V., Pitskhelauri D. I., Pronin I. N., Kornienko V. N. Diffusion kurtosis Imaging in the assessment of peritumoral brain edema in glioblastomas and brain metastases. Med. Vis. 2017;4:97-112. (In Russ., in Engl.). https://doi.org/10.24835/1607-0763-2017-4-97-112
3. Abdalla G., Dixon L., Sanverdi E., Machado P., Kwong J., Panovska-Griffiths J., Rojas-García A., Yoneoka D., Veraart J., Van Cauter S., Abdelkhalek A., Settein M., Yousry T., Bisdas S. The diagnostic role of diffusional kurtosis imaging in glioma grading and differentiation of gliomas from other intra-axial brain tumours: a systematic review with critical appraisal and meta-analysis. Neuroradiology. 2020; 62(7):791-802. https://doi.org/10.1007/S00234-020-02425-9
4. Akbari H., Macyszyn L., Da X., Bilello M., Wolf R., Martinez-Lage M., Biros G., Alonso-Basanta M., O’Rourke D., Davatzikos C. Imaging surrogates of infiltration obtained via multiparametric imaging pattern analysis predict subsequent location of recurrence of glioblastoma. Neurosurgery. 2016;78(4): 572-580. https://doi.org/10.1227/NEU.0000000000001202
5. Batalov A. I., Zakharova N. E., Pronin I. N., Belyaev A. Yu., Pogosbekyan E. L., Goryaynov S. A., Bykanov A. E., Tyurina pCASL-perfusion in preoperative assessment of brain gliomas in large cohort of patients. Sci. Rep. 2022;12:2121. https:// doi.org/10.1038/s41598-022-05992-4
6. Batalov A. I., Afandiev R. M., Zakharova N. E., Pogosbekyan E. L., Shulgina A. A., Kobyakov G. L., Potapov A. A., Pronin I. N. 3D pseudo-continuous arterial spin labeling-MRI (3D PCASL-MRI) in the differential diagnosis between glioblastomas and primary central nervous system lymphomas. Neuroradiology. 2022; 64:1539-1545. https://doi.org/10.1007/s00234-021-02888-4
7. Blystad I., Warntjes J. B. M., Smedby Ö., Lundberg P., Larsson E.-M., Tisell A. Quantitative MRI for analysis of peritumoral edema in malignant gliomas. PLoS ONE. 2017;12(5):e0177135. https:/ /doi.org/10.1371/journal.pone.0177135
8. Delgado A. F., Fahlström M., Nilsson M., Berntsson S. G., Zetterling M., Libard S., Alafuzoff I., van Westen D., Lätt J., Smits A., Larsson E. M. Diffusion kurtosis imaging of gliomas grades II and III — a study of perilesional tumor infiltration, tumor grades and subtypes at clinical presentation. Radiol. Oncol. 2017;51(2):121-129. https://doi.org/10.1515/raon-2017-0010
9. Eisele S. C., Wen P. Y., Lee E. Q. Assessment of brain tumor response: RANO and its offspring. Curr. Treat. Oncol. 2016;17(7):35. https://doi.org/10.1007/s11864-016-0413-5
10. Gates E. D. H., Lin J. S., Weinberg J. S., Prabhu S. S., Hamilton J., Hazle J. D., Fuller G. N., Baladandayuthapani V., Fuen tes D. T., Schellingerhout D. Imaging-based algorithm for the local grading of glioma. AJNR Am. J. Neuroradiol. 2020. V. 41, no. 3. P. 400–407. https://doi.org/10.3174/ajnr.A6405
11. Grossman E. J., Kirov I. I., Gonen O., Novikov D. S., Davitz M. S., Lui Y. W., Grossman R. I., Inglese M., Fieremans E. N-acetyl-aspartate levels correlate with intra-axonal compartment parameters from diffusion MRI. NeuroImage. 2015; 118:334-343. https://doi.org/10.1016/j.neuroimage.2015.05.061
12. Guo J., Yao C., Chen H., Zhuang D., Tang W., Ren G., Wang Y., Wu J., Huang F., Zhou L. The relationship between Cho/ NAA and glioma metabolism: implementation for margin delineation of cerebral gliomas. Acta Neurochir (Wien). 2012;154(8): 1361-1370. https://doi.org/10.1007/s00701-012-1418-x
13. Hansen B., Jespersen S. N. Kurtosis fractional anisotropy, its contrast and estimation by proxy. Sci. Rep. 2016;6:23999. https://doi.org/10.1038/ srep23999
14. Hempel J.-M., Schittenhelm J., Bisdas S., Brendle C., Bender B., Bier G. Skardelly M., Tabatabai G., Castaneda Vega S., Ernemann U., Klose U. In vivo assessment of tumor heterogeneity in WHO 2016 glioma grades using diffusion kurtosis imaging: diagnostic performance and improvement of feasibility in routine clinical practice. J. Neuroradiol. 2018;45(1): 32-40. https://doi.org/10.1016/j.neurad.2017.07.005
15. Kim J. Y., Yoon M. J., Park J. E., Choi E. J., Lee J., Kim H. S. Radiomics in peritumoral non-enhancing regions: fractional anisotropy and cerebral blood volume improve prediction of local progression and overall survival in patients with glioblastoma. Neuroradiology. 2019; 61(11):1261-1272. https://doi.org/10.1007/s00234-019-02255-4
16. Lemercier P., Paz M. S., Patrie J. T., Flors L., Leiva-Salinas C. Gradient of apparent diffusion coefficient values in peritumoral edema helps in differentiation of glioblastoma from solitary metastatic lesions. AJR Am. J. Roentgenol. 2014;203(1); 163-169. https://doi.org/10.2214/AJR.13.11186
17. Martín-Noguerol T., Mohan S., Santos-Armentia E., Cabrera-Zubizarreta A., Luna A. Advanced MRI assessment of non-enhancing peritumoral signal abnormality in brain lesions. European Journal of Radiology. 2021;143:109900
18. Maximov I. I., Tonoyan A. S., Pronin I. N. Differentiation of glioma malignancy grade using diffusion MRI. Phys Med. 2017;40:24–32. https://doi.org/10.1016/j.ejmp.2017.07.002
19. Pogosbekian E. L., Pronin I. N., Zakharova N. E., Batalov A. I., Turkin A. M., Konakova T.A., Maximov I. I. Feasibility of generalised diffusion kurtosis imaging approach for brain glioma grading. Neuroradiology. 2021. V. 63, no. 8. P. 1241-1251. https://doi.org/10.1007/s00234-020-02613-7
20. Qiu J., Deng K., Wang P., Chen C., Luo Y., Yuan S., Wen J. Application of diffusion kurtosis imaging to the study of edema in solid and peritumoral areas of glioma. Magn Reson Imaging. 2022;86610-16. https://doi.org/10.1016/j.mri.2021.11.001
21. Sanai N., Polley M. Y., McDermott M. W., Parsa A. T., Berger M. S. An extent of resection threshold for newly diagnosed glioblastomas. J. Neurosurg. 2011;115(1):3-8. https://doi.org/10.3171/2011.2.jns10998
22. Solozhentseva K., Batalov A., Zakharova N., Goryaynov S., Pogosbekyan E., Pronin I. The Role of 3D-pCASL MRI in the Differential Diagnosis of Glioblastoma and Brain Metastases. Front. Oncol. 2022;12:874924. https://doi.org/10.3389/fonc.2022.874924
23. Steven A. J., Zhuo J., Melhem E. R. Diffusion kurtosis imaging: An emerging technique for evaluating the microstructural environment of the brain. Am. J. Roentgenol. 2014;202(1):26-33. https://doi.org/10.2214/AJR.13.11365
24. Tan Y., Wang X.-C., Zhang H., Wang J., Qin J.-B., Wu X.-F., Zhang L., Wang L. Differentiation of high-gradeastrocytomas from solitary-brain-metastases: comparing diffusion kurtosis imaging and diffusion tensor imaging. Eur. J. Radiol. 2015;84(12): 2618-2624. https://doi.org/10.1016/j.ejrad.2015.10.007
25. Yamahara T., Numay, Oishi T., Kawaguchi T., Seno T., Asai A., Kawamoto K. Morphological and flow cytometric glioblastoma: a comparison of autopsy brain and neuroimaging. Brain and Tumor Pathol. 2010;27:81-87. https://doi.org/10.1007/s10014-010-0275-7
26. Zakharova N. E., Batalov A. I., Pogosbekian E. L., Chekhonin I. V., Goryaynov S. A., Bykanov A. E., Tyurina A. N., Galstyan S. A., Nikitin P. V., Fadeeva L. M., Usachev D. Yu., Pronin I. N. Perifocal Zone of Brain Gliomas: Application of Diffusion Kurtosis and Perfusion MRI Values for Tumor Invasion Border Determination. Cancers. 2023;15(10):2760. https://doi.org/10.3390/cancers15102760
27. Zetterling M., Roodakker K. R., Berntsson S. G., Edqvist P. H., Latini F., Landtblom A. M., Pontén F., Alafuzoff I., Larsson E. M., Smits A. Extension of diffuse low-grade gliomas beyond radiological borders as shown by the coregistration of histopathological and magnetic resonance imaging data. J. Neurosurg. 2016;125 (5):1155-1166. https://doi.org/10.3171/2015.10.JNS15583
Supplementary files
Review
For citations:
Zakharova N.E., Batalov A.I., Pogosbekyan E.L., Goryaynov S.A., Fadeeva L.M., Bykanov A.E., Tyurina A.N., Chekhonin I.V., Galstyan S.A., Pronin I.N., Usachev D.Yu. Magnetic Resonance Imaging in Studies of Perifocal Zone of Brain Gliomas (a Literature Review). Radiology - Practice. 2024;(1):20-36. (In Russ.) https://doi.org/10.52560/2713-0118-2024-1-20-36