Share:
Share this content in WeChat
X
Review
Research progress of MRI on pathological changes and cognitive impairment of radiation-induced brain injury
ZHANG Danni  ZOU Qiaoqiao  WANG Mingliang  LI Wenbin 

Cite this article as: ZHANG D N, ZOU Q Q, WANG M L, et al. Research progress of MRI on pathological changes and cognitive impairment of radiation-induced brain injury[J]. Chin J Magn Reson Imaging, 2023, 14(5): 155-160. DOI:10.12015/issn.1674-8034.2023.05.027.


[Abstract] Cognitive function impairment is the most common clinical manifestation of radiation-induced brain injury. The diagnosis is mainly based on clinical features and neuropsychological scales. The process of cognitive function impairment after radiotherapy is related to the pathological changes. This article reviews the latest progress in the pathological processes related to cognitive function impairment after radiotherapy and the application of MRI. It summarizes the early imaging manifestations and corresponding pathological changes of radiation-induced brain injury in different sequences, and the application of artificial intelligence and radiomics based on MRI in predicting patients with cognitive function impairment after radiotherapy. Based on this, the research direction of artificial intelligence and radiomics combined with multi-sequence MRI for early diagnosis of cognitive function impairment after radiotherapy is proposed, which is helpful for early and accurate identification of patients with cognitive function impairment after radiotherapy and early intervention to improve the quality of life of patients.
[Keywords] radiation-induced brain injury;pathological changes;cognitive impairment;magnetic resonance imaging

ZHANG Danni   ZOU Qiaoqiao   WANG Mingliang   LI Wenbin*  

Department of Radiology, Shanghai Sixth People's Hospital Affiliated to Shanghai Jiao Tong University School of Medicine, Shanghai 200030, China

Corresponding author: Li WB, E-mail: liwenbin@sh163.net

Conflicts of interest   None.

ACKNOWLEDGMENTS National Natural Science Foundation of China (No. 81901727).
Received  2022-11-29
Accepted  2023-05-06
DOI: 10.12015/issn.1674-8034.2023.05.027
Cite this article as: ZHANG D N, ZOU Q Q, WANG M L, et al. Research progress of MRI on pathological changes and cognitive impairment of radiation-induced brain injury[J]. Chin J Magn Reson Imaging, 2023, 14(5): 155-160. DOI:10.12015/issn.1674-8034.2023.05.027.

[1]
FERLAY J, SOERJOMATARAM I, DIKSHIT R, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012[J/OL]. Int J Cancer, 2015, 136(5): E359-86 [2022-11-28]. https://pubmed.ncbi.nlm.nih.gov/25220842/. DOI: 10.1002/ijc.29210">10.1002/ijc.29210">10.1002/ijc.29210.
[2]
LI Y, PENG Y. Interpretation of Chinese expert consensus on diagnosis and treatment of radiation-induced brain injury[J]. J Intern Med Concepts Pract, 2019, 14(5): 269-270. DOI: 10.16138/j.1673-6087.2019.05.001">10.16138/j.1673-6087.2019.05.001">10.16138/j.1673-6087.2019.05.001.
[3]
VOON N S, ABDUL MANAN H, YAHYA N. Cognitive Decline following Radiotherapy of Head and Neck Cancer: Systematic Review and Meta-Analysis of MRI Correlates[J]. Cancers, 2021, 13(24): 6191. DOI: 10.3390/cancers13246191">10.3390/cancers13246191">10.3390/cancers13246191.
[4]
ZHANG D P, CHEN N Y, HUANG Y, et al. Research progress on the effect and mechanism of brain radiotherapy on cognitive function[J]. Chin J Neuroanat, 2020, 36(3): 345-348. DOI: 10.16557/j.cnki.1000-7547.2020.03.019">10.16557/j.cnki.1000-7547.2020.03.019">10.16557/j.cnki.1000-7547.2020.03.019.
[5]
ZHENG Z, WANG B, ZHAO Q, et al. Research progress on mechanism and imaging of temporal lobe injury induced by radiotherapy for head and neck cancer[J]. Eur Radiol, 2022, 32(1): 319-330. DOI: 10.1007/s00330-021-08164-6">10.1007/s00330-021-08164-6">10.1007/s00330-021-08164-6.
[6]
BÁLENTOVÁ S, HNILICOVÁ P, KALENSKÁ D, et al. Effect of fractionated whole-brain irradiation on brain and plasma in a rat model: Metabolic, volumetric and histopathological changes[J]. Neurochem Int, 2021, 145: 104985. DOI: 10.1016/j.neuint.2021.104985">10.1016/j.neuint.2021.104985">10.1016/j.neuint.2021.104985.
[7]
HART E, ODÉ Z, DERIEPPE M P P, et al. Blood-brain barrier permeability following conventional photon radiotherapy-A systematic review and meta-analysis of clinical and preclinical studies[J]. Clin Transl Radiat Oncol, 2022, 35: 44-55. DOI: 10.1016/j.ctro.2022.04.013">10.1016/j.ctro.2022.04.013">10.1016/j.ctro.2022.04.013.
[8]
FARJAM R, PRAMANIK P, ARYAL M P, et al. A Radiation-Induced Hippocampal Vascular Injury Surrogate Marker Predicts Late Neurocognitive Dysfunction[J]. Int J Radiat Oncol Biol Phys, 2015, 93(4): 908-915. DOI: 10.1016/j.ijrobp.2015.08.014">10.1016/j.ijrobp.2015.08.014">10.1016/j.ijrobp.2015.08.014.
[9]
CAO Y, TSIEN C I, SUNDGREN P C, et al. Dynamic contrast-enhanced magnetic resonance imaging as a biomarker for prediction of radiation-induced neurocognitive dysfunction[J]. Clin Cancer Res, 2009, 15(5): 1747-1754. DOI: 10.1158/1078-0432.Ccr-08-1420">10.1158/1078-0432.Ccr-08-1420">10.1158/1078-0432.Ccr-08-1420.
[10]
LEE R X, TANG F R. Radiation-induced neuropathological changes in the oligodendrocyte lineage with relevant clinical manifestations and therapeutic strategies[J]. Int J Radiat Biol, 2022, 98(10): 1519-1531. DOI: 10.1080/09553002.2022.2055804">10.1080/09553002.2022.2055804">10.1080/09553002.2022.2055804.
[11]
CHEN Q, LV X, ZHANG S, et al. Altered properties of brain white matter structural networks in patients with nasopharyngeal carcinoma after radiotherapy[J]. Brain Imaging Behav, 2020, 14(6): 2745-2761. DOI: 10.1007/s11682-019-00224-2">10.1007/s11682-019-00224-2">10.1007/s11682-019-00224-2.
[12]
YANG Z, GONG M, JIAN T, et al. Engrafted glial progenitor cells yield long-term integration and sensory improvement in aged mice[J]. Stem Cell Res Ther, 2022, 13(1): 285. DOI: 10.1186/s13287-022-02959-0">10.1186/s13287-022-02959-0">10.1186/s13287-022-02959-0.
[13]
FENG H C, CHEN N Y, CUI Y H, et al. Astrocyte activity and autophagy after radiation-induced brain injury in rats[J] . Chin J Physiol, 2019, 35(1): 99-105. DOI: 10.3969/j.issn.1000-4718.2019.01.016">10.3969/j.issn.1000-4718.2019.01.016">10.3969/j.issn.1000-4718.2019.01.016.
[14]
PIAO J, MAJOR T, AUYEUNG G, et al. Human embryonic stem cell-derived oligodendrocyte progenitors remyelinate the brain and rescue behavioral deficits following radiation[J]. Cell Stem Cell, 2015, 16(2): 198-210. DOI: 10.1016/j.stem.2015.01.004">10.1016/j.stem.2015.01.004">10.1016/j.stem.2015.01.004.
[15]
HUANG R R, DING G R. The role and mechanism of microglia in radiation induced brain injury[J]. Int J Radiat Med Nucl Med, 2021, 45(2): 124-131. DOI: 10.3760/cma.j.cn121381-202005040-00018">10.3760/cma.j.cn121381-202005040-00018">10.3760/cma.j.cn121381-202005040-00018.
[16]
LIU Q, HUANG Y, DUAN M, et al. Microglia as Therapeutic Target for Radiation-Induced Brain Injury[J]. Int J Mol Sci, 2022, 23(15): 8286. DOI: 10.3390/ijms23158286">10.3390/ijms23158286">10.3390/ijms23158286.
[17]
BELOV O V, BATMUNKH M, INCERTI S, et al. Radiation damage to neuronal cells: Simulating the energy deposition and water radiolysis in a small neural network[J]. Phys Med2016, 32(12): 1510-1520. DOI: 10.1016/j.ejmp.2016.11.004">10.1016/j.ejmp.2016.11.004">10.1016/j.ejmp.2016.11.004.
[18]
GREENE-SCHLOESSER D, MOORE E, ROBBINS M E. Molecular pathways: radiation-induced cognitive impairment[J]. Clin Cancer Res, 2013, 19(9): 2294-2300. DOI: 10.1158/1078-0432.Ccr-11-2903">10.1158/1078-0432.Ccr-11-2903">10.1158/1078-0432.Ccr-11-2903.
[19]
PARIHAR V K, PASHA J, TRAN K K, et al. Persistent changes in neuronal structure and synaptic plasticity caused by proton irradiation[J]. Brain Struct Funct, 2015, 220(2): 1161-1171. DOI: 10.1007/s00429-014-0709-9">10.1007/s00429-014-0709-9">10.1007/s00429-014-0709-9.
[20]
NEU M A, TANYILDIZI Y, WINGERTER A, et al. Susceptibility-weighted magnetic resonance imaging of cerebrovascular sequelae after radiotherapy for pediatric brain tumors[J]. Radiother Oncol, 2018, 127(2): 280-286. DOI: 10.1016/j.radonc.2018.03.010">10.1016/j.radonc.2018.03.010">10.1016/j.radonc.2018.03.010.
[21]
PHILLIPS N S, HILLENBRAND C M, MITREA B G, et al. Cerebral microbleeds in adult survivors of childhood acute lymphoblastic leukemia treated with cranial radiation[J]. Sci Rep, 2020, 10(1): 692. DOI: 10.1038/s41598-020-57682-8">10.1038/s41598-020-57682-8">10.1038/s41598-020-57682-8.
[22]
SHEN Q, LIN F, RONG X, et al. Temporal Cerebral Microbleeds Are Associated With Radiation Necrosis and Cognitive Dysfunction in Patients Treated for Nasopharyngeal Carcinoma[J]. Int J Radiat Oncol Biol Phys, 2016, 94(5): 1113-1120. DOI: 10.1016/j.ijrobp.2015.11.037">10.1016/j.ijrobp.2015.11.037">10.1016/j.ijrobp.2015.11.037.
[23]
RODDY E, SEAR K, FELTON E, et al. Presence of cerebral microbleeds is associated with worse executive function in pediatric brain tumor survivors[J]. Neuro Oncol, 2016, 18(11): 1548-1558. DOI: 10.1093/neuonc/now163">10.1093/neuonc/now163">10.1093/neuonc/now163.
[24]
MORRISON M A, MUELLER S, FELTON E, et al. Rate of radiation-induced microbleed formation on 7T MRI relates to cognitive impairment in young patients treated with radiation therapy for a brain tumor[J]. Radiother Oncol, 2021, 154: 145-153. DOI: 10.1016/j.radonc.2020.09.028">10.1016/j.radonc.2020.09.028">10.1016/j.radonc.2020.09.028.
[25]
KŁOS J, VAN LAAR P J, SINNIGE P F, et al. Quantifying effects of radiotherapy-induced microvascular injury; review of established and emerging brain MRI techniques[J]. Radiother Oncol, 2019, 140: 41-53. DOI: 10.1016/j.radonc.2019.05.020">10.1016/j.radonc.2019.05.020">10.1016/j.radonc.2019.05.020.
[26]
SHAN M Y, YANG G Q, QIN J B, et al. Preliminary study of DSC-MRI and IVIM in differentiating postoperative recurrence and radiation brain injury of high-grade glioma[J]. Chin J Magn Reson Imaging, 2020, 11(5): 326-331. DOI: 10.12015/issn.1674-8034.2020.05.002">10.12015/issn.1674-8034.2020.05.002">10.12015/issn.1674-8034.2020.05.002.
[27]
ZHANG J, WANG Y, WANG Y, et al. Perfusion magnetic resonance imaging in the differentiation between glioma recurrence and pseudoprogression: a systematic review, meta-analysis and meta-regression[J]. Quant Imaging Med Surg, 2022, 12(10): 4805-4822. DOI: 10.21037/qims-22-32">10.21037/qims-22-32">10.21037/qims-22-32.
[28]
FU R, SZIDONYA L, BARAJAS R F, et al. Diagnostic performance of DSC perfusion MRI to distinguish tumor progression and treatment-related changes: a systematic review and meta-analysis[J/OL]. Neurooncol Adv, 2022, 4(1): vdac027 [2022-11-28]. https://pubmed.ncbi.nlm.nih.gov/35386567/. DOI: 10.1093/noajnl/vdac027">10.1093/noajnl/vdac027">10.1093/noajnl/vdac027.
[29]
WANG Y L, CHEN S, XIAO H F, et al. Differentiation between radiation-induced brain injury and glioma recurrence using 3D pCASL and dynamic susceptibility contrast-enhanced perfusion-weighted imaging[J]. Radiother Oncol, 2018, 129(1): 68-74. DOI: 10.1016/j.radonc.2018.01.009">10.1016/j.radonc.2018.01.009">10.1016/j.radonc.2018.01.009.
[30]
YANG J, XU Z, GAO J, et al. Evaluation of early acute radiation-induced brain injury: Hybrid multifunctional MRI-based study[J]. Magn Reson Imaging, 2018, 54: 101-108. DOI: 10.1016/j.mri.2018.08.012">10.1016/j.mri.2018.08.012">10.1016/j.mri.2018.08.012.
[31]
DÜNDAR T T, CETINKAYA E, YURTSEVER İ, et al. Follow-Up of High-Grade Glial Tumor; Differentiation of Posttreatment Enhancement and Tumoral Enhancement by DCE-MR Perfusion[J]. Contrast Media Mol Imaging, 2022, 2022: 6948422. DOI: 10.1155/2022/6948422">10.1155/2022/6948422">10.1155/2022/6948422.
[32]
WANG M L, LI W B. A review of the application of MRI techniques in cognitive impairment after traumatic brain injury[J]. Chin J Magn Reson Imaging, 2016, 7(4): 310-314. DOI: 10.12015/issn.1674-8034.2016.04.013">10.12015/issn.1674-8034.2016.04.013">10.12015/issn.1674-8034.2016.04.013
[33]
SONG X H, YANG J R, WANG L J. Research progress of functional magnetic resonance imaging in radiation-induced brain injury after radiotherapy of nasopharyngeal carcinoma[J]. Chin J Magn Reson Imaging, 2021, 12(1): 96-99. DOI: 10.12015/issn.1674-8034.2021.01.022">10.12015/issn.1674-8034.2021.01.022">10.12015/issn.1674-8034.2021.01.022.
[34]
LIN X, TANG L, LI M, et al. Irradiation-related longitudinal white matter atrophy underlies cognitive impairment in patients with nasopharyngeal carcinoma[J]. Brain Imaging Behav, 2021, 15(5): 2426-2435. DOI: 10.1007/s11682-020-00441-0">10.1007/s11682-020-00441-0">10.1007/s11682-020-00441-0.
[35]
DUAN F, CHENG J, JIANG J, et al. Whole-brain changes in white matter microstructure after radiotherapy for nasopharyngeal carcinoma: a diffusion tensor imaging study[J]. Eur Arch Otorhinolaryngol, 2016, 273(12): 4453-4459. DOI: 10.1007/s00405-016-4127-x">10.1007/s00405-016-4127-x">10.1007/s00405-016-4127-x.
[36]
LIU J, WANG W, ZHOU Y, et al. Early-Onset Micromorphological Changes of Neuronal Fiber Bundles During Radiotherapy[J]. J Magn Reson Imaging, 2022, 56(1): 210-218. DOI: 10.1002/jmri.28018">10.1002/jmri.28018">10.1002/jmri.28018.
[37]
LENG X, FANG P, LIN H, et al. Structural MRI research in patients with nasopharyngeal carcinoma following radiotherapy: A DTI and VBM study[J]. Oncol Lett, 2017, 14(5): 6091-6096. DOI: 10.3892/ol.2017.6968">10.3892/ol.2017.6968">10.3892/ol.2017.6968.
[38]
DING Z, ZHANG H, LV X F, et al. Radiation-induced brain structural and functional abnormalities in presymptomatic phase and outcome prediction[J]. Hum Brain Mapp, 2018, 39(1): 407-427. DOI: 10.1002/hbm.23852">10.1002/hbm.23852">10.1002/hbm.23852.
[39]
QIU Y, GUO Z, LIN X, et al. Standard radiotherapy for patients with nasopharyngeal carcinoma results in progressive tract-specific brain white matter alterations: A one-year follow-up via diffusion tensor imaging[J]. Radiother Oncol, 2021, 159: 255-264. DOI: 10.1016/j.radonc.2021.03.039">10.1016/j.radonc.2021.03.039">10.1016/j.radonc.2021.03.039.
[40]
LV X, HE H, YANG Y, et al. Radiation-induced hippocampal atrophy in patients with nasopharyngeal carcinoma early after radiotherapy: a longitudinal MR-based hippocampal subfield analysis[J]. Brain Imaging Behav, 2019, 13(4): 1160-1171. DOI: 10.1007/s11682-018-9931-z">10.1007/s11682-018-9931-z">10.1007/s11682-018-9931-z.
[41]
CHAPMAN C H, NAGESH V, SUNDGREN P C, et al. Diffusion tensor imaging of normal-appearing white matter as biomarker for radiation-induced late delayed cognitive decline[J]. Int J Radiat Oncol Biol Phys, 2012, 82(5): 2033-2040. DOI: 10.1016/j.ijrobp.2011.01.068">10.1016/j.ijrobp.2011.01.068">10.1016/j.ijrobp.2011.01.068.
[42]
WU G, LUO S S, BALASUBRAMANIAN P S, et al. Early Stage Markers of Late Delayed Neurocognitive Decline Using Diffusion Kurtosis Imaging of Temporal Lobe in Nasopharyngeal Carcinoma Patients[J]. J Cancer, 2020, 11(20): 6168-6177. DOI: 10.7150/jca.48759">10.7150/jca.48759">10.7150/jca.48759.
[43]
WU G, LI R R, BALASUBRAMANIAN P S, et al. Temporal lobe microstructural abnormalities in patients with nasopharyngeal carcinoma quantitatively evaluated by high-resolution DWI and DKI after concurrent chemoradiotherapy[J]. Clin Transl Radiat Oncol, 2020, 21: 36-43. DOI: 10.1016/j.ctro.2019.12.003">10.1016/j.ctro.2019.12.003">10.1016/j.ctro.2019.12.003.
[44]
MORRISON M A, WALTER S, MUELLER S, et al. Functional network alterations in young brain tumor patients with radiotherapy-induced memory impairments and vascular injury[J]. Front Neurol, 2022, 13: 921984. DOI: 10.3389/fneur.2022.921984">10.3389/fneur.2022.921984">10.3389/fneur.2022.921984.
[45]
ZHANG Y M, GAO J M, ZHOU H, et al. Pre-symptomatic local brain activity and functional connectivity alterations in nasopharyngeal carcinoma patients who developed radiation encephalopathy following radiotherapy[J]. Brain Imaging Behav, 2020, 14(5): 1964-1978. DOI: 10.1007/s11682-019-00145-0">10.1007/s11682-019-00145-0">10.1007/s11682-019-00145-0.
[46]
MA Q, ZENG L L, QIN J, et al. Radiation-induced cerebellar-cerebral functional connectivity alterations in nasopharyngeal carcinoma patients[J]. Neuroreport, 2017, 28(12): 705-711. DOI: 10.1097/wnr.0000000000000813">10.1097/wnr.0000000000000813">10.1097/wnr.0000000000000813.
[47]
ZHAO L M, KANG Y F, GAO J M, et al. Functional Connectivity Density for Radiation Encephalopathy Prediction in Nasopharyngeal Carcinoma[J]. Front Oncol, 2021, 11: 687127. DOI: 10.3389/fonc.2021.687127">10.3389/fonc.2021.687127">10.3389/fonc.2021.687127.
[48]
FU G, XIE Y, PAN J, et al. Longitudinal study of irradiation-induced brain functional network alterations in patients with nasopharyngeal carcinoma[J]. Radiother Oncol, 2022, 173: 277-284. DOI: 10.1016/j.radonc.2022.06.008">10.1016/j.radonc.2022.06.008">10.1016/j.radonc.2022.06.008.
[49]
ATWOOD T, PAYNE V S, ZHAO W, et al. Quantitative magnetic resonance spectroscopy reveals a potential relationship between radiation-induced changes in rat brain metabolites and cognitive impairment[J]. Radiat Res, 2007, 168(5): 574-581. DOI: 10.1667/rr0735.1">10.1667/rr0735.1">10.1667/rr0735.1.
[50]
CHEN W S, LI J J, HONG L, et al. Diagnostic Value of Magnetic Resonance Spectroscopy in Radiation Encephalopathy Induced by Radiotherapy for Patients with Nasopharyngeal Carcinoma: A Meta-Analysis[J]. Biomed Res Int, 2016, 2016: 5126074. DOI: 10.1155/2016/5126074">10.1155/2016/5126074">10.1155/2016/5126074.
[51]
ALIREZAEI Z, AMOUHEIDARI A, HASSANPOUR M, et al. Early Detection of Radiation-Induced Injury and Prediction of Cognitive Deficit by MRS Metabolites in Radiotherapy of Low-Grade Glioma[J]. Biomed Res Int, 2021, 2021: 6616992. DOI: 10.1155/2021/6616992">10.1155/2021/6616992">10.1155/2021/6616992.
[52]
LENG X, FANG P, LIN H, et al. Application of a machine learning method to whole brain white matter injury after radiotherapy for nasopharyngeal carcinoma[J]. Cancer Imaging, 2019, 19(1): 19. DOI: 10.1186/s40644-019-0203-y">10.1186/s40644-019-0203-y">10.1186/s40644-019-0203-y.
[53]
ZHANG B, LIAN Z, ZHONG L, et al. Machine-learning based MRI radiomics models for early detection of radiation-induced brain injury in nasopharyngeal carcinoma[J]. BMC Cancer, 2020, 20(1): 502. DOI: 10.1186/s12885-020-06957-4">10.1186/s12885-020-06957-4">10.1186/s12885-020-06957-4.
[54]
BAO D, ZHAO Y, LI L, et al. A MRI-based radiomics model predicting radiation-induced temporal lobe injury in nasopharyngeal carcinoma[J]. Eur Radiol, 2022, 32(10): 6910-6921. DOI: 10.1007/s00330-022-08853-w">10.1007/s00330-022-08853-w">10.1007/s00330-022-08853-w.
[55]
HOU J, LI H, ZENG B, et al. MRI-based radiomics nomogram for predicting temporal lobe injury after radiotherapy in nasopharyngeal carcinoma[J]. Eur Radiol, 2022, 32(2): 1106-1114. DOI: 10.1007/s00330-021-08254-5">10.1007/s00330-021-08254-5">10.1007/s00330-021-08254-5.
[56]
BIN X, ZHU C, TANG Y, et al. Nomogram Based on Clinical and Radiomics Data for Predicting Radiation-induced Temporal Lobe Injury in Patients with Non-metastatic Stage T4 Nasopharyngeal Carcinoma[J/OL]. Clin Oncol (R Coll Radiol), 2022, 34(12): e482-e492 [2022-11-28]. https://pubmed.ncbi.nlm.nih.gov/36008245/. DOI: 10.1016/j.clon.2022.07.007">10.1016/j.clon.2022.07.007">10.1016/j.clon.2022.07.007.
[57]
NIU J L. Application of radiomics model in predicting radiation encephalopathy after radiotherapy for nasopharynheal carcinoma[D]. Hangzhou: Zhejiang Chinese Medical University, 2022.

PREV Research progress of brain structural and functional magnetic resonance imaging in patients with chronic pruritus disease
NEXT Advances in cerebellar neuroimaging in autism spectrum disorders
  



Tel & Fax: +8610-67113815    E-mail: editor@cjmri.cn