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Advances in diffusion MRI based on oscillating gradient spin echo
ZHANG Xinli  WANG Jing 

ZHANG X L, WANG J. Advances in diffusion MRI based on oscillating gradient spin echo[J]. Chin J Magn Reson Imaging, 2023, 14(9): 198-202. DOI:10.12015/issn.1674-8034.2023.09.036.


[Abstract] Diffusion magnetic resonance imaging (dMRI) is one of the most promising methods for microstructural imaging of biological tissues, which has made great progress in tumor and neuroimaging. Oscillating gradient spin echo (OGSE) sequence is a new dMRI technique, which shortens the measurable effective diffusion time of water molecules by applying oscillating gradients. By establishing a mathematical model, the microstructure characteristics such as cell diameter, extracellular water molecular diffusion coefficient, intracellular water molecular volume fraction and cellularity can be measured. It shows the prospect of clinical application in tumor cell diameter measurement, tumor heterogeneity evaluation and nerve axon diameter measurement. This paper reviewed the imaging principle of OGSE, the research status of OGSE in tumors and nerve axons, and the current limitations of OGSE, aiming to provide reference for scholars interested in this technology, promote further research on OGSE, and accelerate the application of OGSE in clinical diagnosis and treatment.
[Keywords] diffusion magnetic resonance imaging；microstructure imaging；oscillating gradient spin echo；tumor imaging；neuroimaging

ZHANG Xinli1, 2   WANG Jing1, 2*  

1 Department of Radiology, Union hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, China

2 Hubei Province Key Laboratory of Molecular Imaging, Wuhan 430030, China

Corresponding author: Wang J, E-mail: xhwangjing@hust.edu.cn

Conflicts of interest   None.

ACKNOWLEDGMENTS Natural Science Foundation of Hubei Province (No. 2021CFB447).
Received  2023-05-06
Accepted  2023-07-27
DOI: 10.12015/issn.1674-8034.2023.09.036
ZHANG X L, WANG J. Advances in diffusion MRI based on oscillating gradient spin echo[J]. Chin J Magn Reson Imaging, 2023, 14(9): 198-202. DOI:10.12015/issn.1674-8034.2023.09.036.

[1]
JANG H, DU J. Optimizing diffusion-weighted MRI of peripheral nerves[J]. Radiology, 2022, 302(1): 162-163. DOI: 10.1148/radiol.2021211907.
[2]
ZHU A T, SHIH R, HUANG R Y, et al. Revealing tumor microstructure with oscillating diffusion encoding MRI in pre-surgical and post-treatment glioma patients[J/OL]. Magn Reson Med, 2023 [2023-05-05]. https://pubmed.ncbi.nlm.nih.gov/37335831/. DOI: 10.1002/mrm.29758.
[3]
XU Y H, DING L. A review of brain tissue microstructural imaging based on diffusion magnetic resonance[J]. Chin J Biomed Eng, 2021, 40(3): 354-363. DOI: 10.3969/j.issn.0258-8021.2021.03.11.
[4]
XU J Z. Probing neural tissues at small scales: recent progress of oscillating gradient spin echo (OGSE) neuroimaging in humans[J/OL]. J Neurosci Methods, 2021, 349: 109024 [2023-05-05]. https://pubmed.ncbi.nlm.nih.gov/33333089/. DOI: 10.1016/j.jneumeth.2020.109024.
[5]
GROSS B, KOSFELD R. Application of spin-echo method in measurement of auto-diffusion[J]. MESSTECHNIK, 1969, 77(7-8): 171.
[6]
ZHANG H X, LIU K Y, BA R C, et al. Histological and molecular classifications of pediatric glioma with time-dependent diffusion MRI-based microstructural mapping[J]. Neuro Oncol, 2023, 25(6): 1146-1156. DOI: 10.1093/neuonc/noad003.
[7]
JIANG X Y, LI H, XIE J P, et al. Quantification of cell size using temporal diffusion spectroscopy[J]. Magn Reson Med, 2016, 75(3): 1076-1085. DOI: 10.1002/mrm.25684.
[8]
GORE J C, XU J Z, COLVIN D C, et al. Characterization of tissue structure at varying length scales using temporal diffusion spectroscopy[J]. NMR Biomed, 2010, 23(7): 745-756. DOI: 10.1002/nbm.1531.
[9]
WU J, KANG T S, LAN X L, et al. IMPULSED model based cytological feature estimation with U-Net: application to human brain tumor at 3T[J]. Magn Reson Med, 2023, 89(1): 411-422. DOI: 10.1002/mrm.29429.
[10]
NILSSON M, ENGLUND E, SZCZEPANKIEWICZ F, et al. Imaging brain tumour microstructure[J/OL]. NeuroImage, 2018, 182: 232-250 [2023-05-05]. https://pubmed.ncbi.nlm.nih.gov/29751058/. DOI: 10.1016/j.neuroimage.2018.04.075.
[11]
JIANG X Y, LI H, XIE J P, et al. In vivo imaging of cancer cell size and cellularity using temporal diffusion spectroscopy[J]. Magn Reson Med, 2017, 78(1): 156-164. DOI: 10.1002/mrm.26356.
[12]
XU J Z, DOES M D, GORE J C. Sensitivity of MR diffusion measurements to variations in intracellular structure: effects of nuclear size[J]. Magn Reson Med, 2009, 61(4): 828-833. DOI: 10.1002/mrm.21793.
[13]
VITALE I, SHEMA E, LOI S, et al. Intratumoral heterogeneity in cancer progression and response to immunotherapy[J]. Nat Med, 2021, 27(2): 212-224. DOI: 10.1038/s41591-021-01233-9.
[14]
COLVIN D C, YANKEELOV T E, DOES M D, et al. New insights into tumor microstructure using temporal diffusion spectroscopy[J]. Cancer Res, 2008, 68(14): 5941-5947. DOI: 10.1158/0008-5472.CAN-08-0832.
[15]
CHAWLA S, BUKHARI S, AFRIDI O M, et al. Metabolic and physiologic magnetic resonance imaging in distinguishing true progression from pseudoprogression in patients with glioblastoma[J/OL]. NMR Biomed, 2022, 35(7): e4719 [2023-05-05]. https://pubmed.ncbi.nlm.nih.gov/35233862/. DOI: 10.1002/nbm.4719.
[16]
AREVALO O D, SOTO C, RABIEI P, et al. Assessment of glioblastoma response in the era of bevacizumab: longstanding and emergent challenges in the imaging evaluation of pseudoresponse[J/OL]. Front Neurol, 2019, 10: 460 [2023-05-05]. https://pubmed.ncbi.nlm.nih.gov/31133966/. DOI: 10.3389/fneur.2019.00460.
[17]
BONGERS A, HAU E, SHEN H. Short diffusion time diffusion-weighted imaging with oscillating gradient preparation as an early magnetic resonance imaging biomarker for radiation therapy response monitoring in glioblastoma: a preclinical feasibility study[J]. Int J Radiat Oncol Biol Phys, 2018, 102(4): 1014-1023. DOI: 10.1016/j.ijrobp.2017.12.280.
[18]
COLVIN D C, LOVELESS M E, DOES M D, et al. Earlier detection of tumor treatment response using magnetic resonance diffusion imaging with oscillating gradients[J]. Magn Reson Imaging, 2011, 29(3): 315-323. DOI: 10.1016/j.mri.2010.10.003.
[19]
JIANG X Y, XU J Z, GORE J C. Quantitative temporal diffusion spectroscopy as an early imaging biomarker of radiation therapeutic response in gliomas: a preclinical proof of concept[J]. Adv Radiat Oncol, 2018, 4(2): 367-376. DOI: 10.1016/j.adro.2018.11.003.
[20]
XU J Z, LI K, SMITH R A, et al. Characterizing tumor response to chemotherapy at various length scales using temporal diffusion spectroscopy[J/OL]. PLoS One, 2012, 7(7): e41714 [2023-05-05]. https://pubmed.ncbi.nlm.nih.gov/22911846/. DOI: 10.1371/journal.pone.0041714.
[21]
TISON A, GARAUD S, CHICHE L, et al. Immune-checkpoint inhibitor use in patients with cancer and pre-existing autoimmune diseases[J]. Nat Rev Rheumatol, 2022, 18(11): 641-656. DOI: 10.1038/s41584-022-00841-0.
[22]
BAGCHI S, YUAN R, ENGLEMAN E G. Immune checkpoint inhibitors for the treatment of cancer: clinical impact and mechanisms of response and resistance[J/OL]. Annu Rev Pathol, 2021, 16: 223-249 [2023-05-05]. https://pubmed.ncbi.nlm.nih.gov/33197221/. DOI: 10.1146/annurev-pathol-042020-042741.
[23]
JIANG X Y, DUDZINSKI S, BECKERMANN K E, et al. MRI of tumor T cell infiltration in response to checkpoint inhibitor therapy[J/OL]. J Immunother Cancer, 2020, 8(1): e000328 [2023-05-05]. https://pubmed.ncbi.nlm.nih.gov/32581044/. DOI: 10.1136/jitc-2019-000328.
[24]
HOFFMANN E, GERWING M, NILAND S, et al. Profiling specific cell populations within the inflammatory tumor microenvironment by oscillating-gradient diffusion-weighted MRI[J/OL]. J Immunother Cancer, 2023, 11(3): e006092 [2023-05-05]. https://pubmed.ncbi.nlm.nih.gov/36918222/. DOI: 10.1136/jitc-2022-006092.
[25]
JIANG X Y, MCKINLEY E T, XIE J P, et al. In vivo magnetic resonance imaging of treatment-induced apoptosis[J/OL]. Sci Rep, 2019, 9(1): 9540 [2023-05-05]. https://pubmed.ncbi.nlm.nih.gov/31266982/. DOI: 10.1038/s41598-019-45864-y.
[26]
PORTNOY S, FICHTNER N D, DZIEGIELEWSKI C, et al. In vitro detection of apoptosis using oscillating and pulsed gradient diffusion magnetic resonance imaging[J]. NMR Biomed, 2014, 27(4): 371-380. DOI: 10.1002/nbm.3070.
[27]
JIANG X Y, LI H, ZHAO P, et al. Early detection of treatment-induced mitotic arrest using temporal diffusion magnetic resonance spectroscopy[J]. Neoplasia, 2016, 18(6): 387-397. DOI: 10.1016/j.neo.2016.04.006.
[28]
XU J Z, JIANG X Y, LI H, et al. Magnetic resonance imaging of mean cell size in human breast tumors[J]. Magn Reson Med, 2020, 83(6): 2002-2014. DOI: 10.1002/mrm.28056.
[29]
BA R C, WANG X X, ZHANG Z L, et al. Diffusion-time dependent diffusion MRI: effect of diffusion-time on microstructural mapping and prediction of prognostic features in breast cancer[J]. Eur Radiol, 2023, 33(9): 6226-6237. DOI: 10.1007/s00330-023-09623-y.
[30]
IIMA M, YAMAMOTO A, KATAOKA M, et al. Time-dependent diffusion MRI to distinguish malignant from benign head and neck tumors[J]. J Magn Reson Imaging, 2019, 50(1): 88-95. DOI: 10.1002/jmri.26578.
[31]
IIMA M, KATAOKA M, HONDA M, et al. The rate of apparent diffusion coefficient change with diffusion time on breast diffusion-weighted imaging depends on breast tumor types and molecular prognostic biomarker expression[J]. Invest Radiol, 2021, 56(8): 501-508. DOI: 10.1097/RLI.0000000000000766.
[32]
WU D, JIANG K W, LI H, et al. Time-dependent diffusion MRI for quantitative microstructural mapping of prostate cancer[J]. Radiology, 2022, 303(3): 578-587. DOI: 10.1148/radiol.211180.
[33]
MAEKAWA T, HORI M, MURATA K, et al. Differentiation of high-grade and low-grade intra-axial brain tumors by time-dependent diffusion MRI[J/OL]. Magn Reson Imaging, 2020, 72: 34-41 [2023-05-05]. https://pubmed.ncbi.nlm.nih.gov/32599021/. DOI: 10.1016/j.mri.2020.06.018.
[34]
MAEKAWA T, HORI M, MURATA K, et al. Investigation of time-dependent diffusion in extra-axial brain tumors using oscillating-gradient spin-echo[J/OL]. Magn Reson Imaging, 2023, 96: 67-74 [2023-05-05]. https://pubmed.ncbi.nlm.nih.gov/36423796/. DOI: 10.1016/j.mri.2022.11.010.
[35]
HUANG S Y, TIAN Q Y, FAN Q Y, et al. High-gradient diffusion MRI reveals distinct estimates of axon diameter index within different white matter tracts in the in vivo human brain[J]. Brain Struct Funct, 2020, 225(4): 1277-1291. DOI: 10.1007/s00429-019-01961-2.
[36]
FAN Q Y, TIAN Q Y, OHRINGER N A, et al. Age-related alterations in axonal microstructure in the corpus callosum measured by high-gradient diffusion MRI[J/OL]. Neuroimage, 2019, 191: 325-336 [2023-05-05]. https://pubmed.ncbi.nlm.nih.gov/30790671/. DOI: 10.1016/j.neuroimage.2019.02.036.
[37]
XU J Z, LI H, LI K, et al. Fast and simplified mapping of mean axon diameter using temporal diffusion spectroscopy[J]. NMR Biomed, 2016, 29(4): 400-410. DOI: 10.1002/nbm.3484.
[38]
XU J Z, LI H, HARKINS K D, et al. Mapping mean axon diameter and axonal volume fraction by MRI using temporal diffusion spectroscopy[J/OL]. Neuroimage, 2014, 103: 10-19 [2023-05-05]. https://pubmed.ncbi.nlm.nih.gov/25225002/. DOI: 10.1016/j.neuroimage.2014.09.006.
[39]
HERRERA S L, SHEFT M, MERCREDI M E, et al. Axon diameter inferences in the human corpus callosum using oscillating gradient spin echo sequences[J/OL]. Magn Reson Imaging, 2022, 85: 64-70 [2023-05-05]. https://pubmed.ncbi.nlm.nih.gov/34662703/. DOI: 10.1016/j.mri.2021.10.014.
[40]
DROBNJAK I, ZHANG H, IANUŞ A, et al. PGSE, OGSE, and sensitivity to axon diameter in diffusion MRI: insight from a simulation study[J]. Magn Reson Med, 2016, 75(2): 688-700. DOI: 10.1002/mrm.25631.
[41]
KAKKAR L S, BENNETT O F, SIOW B, et al. Low frequency oscillating gradient spin-echo sequences improve sensitivity to axon diameter: an experimental study in viable nerve tissue[J/OL]. Neuroimage, 2018, 182: 314-328 [2023-05-05]. https://pubmed.ncbi.nlm.nih.gov/28774648/. DOI: 10.1016/j.neuroimage.2017.07.060.
[42]
MERCREDI M, MARTIN M. Toward faster inference of micron-scale axon diameters using Monte Carlo simulations[J]. Magma, 2018, 31(4): 511-530. DOI: 10.1007/s10334-018-0680-1.
[43]
TÉTREAULT P, HARKINS K D, BARON C A, et al. Diffusion time dependency along the human corpus callosum and exploration of age and sex differences as assessed by oscillating gradient spin-echo diffusion tensor imaging[J/OL]. Neuroimage, 2020, 210: 116533 [2023-05-05]. https://pubmed.ncbi.nlm.nih.gov/31935520/. DOI: 10.1016/j.neuroimage.2020.116533.
[44]
HARKINS K D, BEAULIEU C, XU J Z, et al. A simple estimate of axon size with diffusion MRI[J/OL]. Neuroimage, 2021, 227: 117619 [2023-05-05]. https://pubmed.ncbi.nlm.nih.gov/33301942/. DOI: 10.1016/j.neuroimage.2020.117619.
[45]
LI H, JIANG X Y, XIE J P, et al. Impact of transcytolemmal water exchange on estimates of tissue microstructural properties derived from diffusion MRI[J]. Magn Reson Med, 2017, 77(6): 2239-2249. DOI: 10.1002/mrm.26309.
[46]
MAEKAWA T, HORI M, MURATA K, et al. Choroid plexus cysts analyzed using diffusion-weighted imaging with short diffusion-time[J/OL]. Magn Reson Imaging, 2019, 57: 323-327 [2023-05-05]. https://pubmed.ncbi.nlm.nih.gov/30605722/. DOI: 10.1016/j.mri.2018.12.010.
[47]
MAZZOLI V, MOULIN K, KOGAN F, et al. Diffusion tensor imaging of skeletal muscle contraction using oscillating gradient spin echo[J/OL]. Front Neurol, 2021, 12: 608549 [2023-05-05]. https://pubmed.ncbi.nlm.nih.gov/33658976/. DOI: 10.3389/fneur.2021.608549.
[48]
ANDICA C, HORI M, KAMIYA K, et al. Spatial restriction within intracranial epidermoid cysts observed using short diffusion-time diffusion-weighted imaging[J]. Magn Reson Med Sci, 2018, 17(3): 269-272. DOI: 10.2463/mrms.cr.2017-0111.
[49]
JIANG X Y, XU J Z, GORE J C. Mapping hepatocyte size in vivo using temporal diffusion spectroscopy MRI[J]. Magn Reson Med, 2020, 84(5): 2671-2683. DOI: 10.1002/mrm.28299.
[50]
WAGNER M, DOBLAS S, POTÉ N, et al. Comparison of pulsed and oscillating gradient diffusion-weighted MRI for characterizing hepatocellular nodules in liver cirrhosis: ex vivo study in a rat model[J]. J Magn Reson Imaging, 2020, 51(4): 1065-1074. DOI: 10.1002/jmri.26919.

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