Molecular Imaging of Brain Tumors and Drug Delivery Using CEST MRI: Promises and Challenges
Abstract
:1. Introduction
2. CEST Imaging of Brain Tumors
2.1. Endogenous Contrast
2.1.1. APT-Weighted (APTw) Contrast
2.1.2. NOE Contrast
2.2. Glioblastoma and Gliomas (Grade II, III)
Species | Tumor Type (Grade) | B0 (T) | Analysis Method | CEST Contrast | Molecular/Cellular Changes | Ref. |
---|---|---|---|---|---|---|
Rat | Glioma, C6 | 3 | DISC-CEST | APT | Cellular and nuclear atypia | Wu Y. et al., 2019 [92] |
Rat | Gliosarcoma, 9L | 4.7 | MTRasym | APTw | Cellular proteins and peptides | Zhou Z. et al., 2003 [3] |
Rat | Gliosarcoma, 9L | 4.7 | MTRasym | APTw | pH | Zhou Z. et al., 2003 [48] |
Rat | Gliosarcoma, 9L SF188/V + glioma | 4.7 | MTRasym | APTw | Treatment effects (radiation therapy), radiation necrosis, mobile cytosolic proteins, and peptides | Zhou J. et al., 2011 [70] |
Rat | Gliosarcoma, 9L | 4.7 | MTRasym | APTw NOE (−2.5 to −5 ppm) | Mobile proteins, peptides, lipids, and metabolites | Zhou J. et al., 2013 [43] |
Rat | U87 | 4.7 | MTRasym | APTw | Treatment effects (radiation therapy), radiation necrosis, cellularity, nuclear atypia, and vacuolation | Hong X. et al., 2014 [69] |
Rat | GBM | 4.7 | EMR | APT, NOE | Mobile proteins and peptides | Heo HY. et al., 2016 [87] |
Rat | GBM | 4.7 | MTRREX, AREX, CESTR, CESTRnr | APT, 2 ppm | APT: mobile proteins and peptides, 2 ppm: protein and peptide side-chain amide protons and various amine-related protons | Heo HY. et al., 2017 [89] |
Rat | U87 | 4.7 | MTRasym | APTw | Amide proton mobile amide proton content or the increased amide proton exchange rate | Lee DH. et al. 2017 [90] |
EMR | APT, NOE | |||||
Rat | Glioma | 4.7 | DISC-CEST | APT NOE | APT: intracellular mobile proteins/peptides concentration NOE: aliphatic and olefinic protons | Zhou IY. et al., 2017 [26] |
Rat | Gliosarcoma, 9L | 4.7 | MTRasym | APTw | NA | Heo H. et al., 2019 [91] |
EMR | APT, NOE | |||||
Rat | Gliosarcoma, 9L | 9.4 | AREX | APT, NOE | Protein contents | Xu J. et al., 2014 [93] |
Rat | Gliosarcoma, 9L | 9.4 | Lorentzian | APT (3.6 ppm) NOE (−3.2 ppm) | Amide proton | Cai K. et al., 2015 [115] |
2 ppm | Tumor progression and creatine | |||||
Rat | Gliosarcoma, 9L; glioma, F98 | 9.4 | Lorentzian | 2 ppm | Creatine and tumor aggressiveness | Cai K. et al., 2017 [116] |
Rat | Gliosarcoma, 9L | 9.4 | MTRasym, AREX | 3 ppm | Amine and protein | Zhang XY. et al., 2017 [117] |
Rat | ENU1564 (brain metastasis model) | 9.4 | APTR* | APT | Protein concentration and pH | Ray KJ. et al., 2019 [107] |
Rat | Gliosarcoma, 9L | 9.4 | Lorentzian | 3 ppm | Glutamate | Debnath A. et al., 2020 [118] |
Rat | Gliosarcoma, 9L | 9.4 | RPT | NOE (−1.6 ppm) | Phospholipids on cell membranes | Zu Z. et al., 2020 [101] |
Mouse | GBM, patient cells | 7 | MTRasym | APTw | Proliferation, cellular acidification, and treatment effect (TMZ) | Sagiyama K. et al., 2014 [40] |
Mouse | Glioma, GL261 | 7 | MTRasym | 3 ppm | Amine, pH, cellularity, and necrosis | Harris RJ. et al., 2015 [38] |
Mouse | U87MG | 9.4 | AACID | AACID (amide at 3.5 ppm, amine at 2.75 ppm) | Intracellular pH and treatment effect | Albatany M. et al., 2019 [66] |
Human (n = 10) | GBM (IV), oligodendroglioma (III), LGO (II), LGA (II), Meningioma | 3 | MTRasym | APTw | Cellular protein/peptide and intracellular pH | Jones CK. et al., 2006 [4] |
Human (n = 9) | GMB (IV), AO (III), AA (III), LGO (II), LGA (II) | 3 | MTRasym | APTw | Glioma grading, cytosolic protein and peptide, and intracellular pH | Zhou J. et al., 2008 [60] |
Human (n = 12) | GBM (IV), astrocytoma (III), oligodendroglioma (III) | 3 | MTRasym | APTw | Viable tumor core, edema, necrosis, mobile protein, and peptide | Wen Z. et al., 2010 [45] |
Human (n = 14) | GBM (IV), AA (III), LGO (II), LGA (II), LGOA (II) | 3 | MTRasym | APTw | Protein content | Zhou J. et al., 2013 [42] |
Human (n = 36) | GBM (IV), AO (III), AA (III), AOA (III), LGA (II), LGO (II), LGOA (II) | 3 | MTRasym | APTw | Glioma grading, necrosis, cell density, and proliferation | Togao O. et al., 2014 [39] |
Human (n = 25) | Glioma (II–IV) | 3 | MTRasym | 3 ppm | An acidic signature, treatment effect (CRT), and PFS | Harris RJ. et al., 2015 [38] |
Human (n = 26) | GBM (IV), AA (III), AO (III), LGO (II), LGOA (II) | 3 | MTRasym | APTw | Glioma grading | Sakata A. et al., 2015 [65] |
Human (n = 13) | GBM (IV), Gliomas (low–grade), meningiomas, lymphoma | 3 | MTRasym | APTw | NA | Togao O. et al., 2015 [36] |
Human (n = 11) | High–grade glioma | 3 | EMR | APT, NOE | NA | Heo HY. et al., 2016 [119] |
Human (n = 32) | High–grade glioma Lymphomas | 3 | MTRasym | APTw | Differentiate lymphomas from high-grade glioma and protein | Jiang S. et al., 2016 [64] |
Human (n = 65) | Glioma (II–IV) | 3 | MTRasym | APTw | Proliferation | Park J. et al., 2016 [32] |
Human (n = 32) | GBM (IV), AA (III), gliomas (low–grade) | 3 | MTRasym | APTw | Cellularity | Ma B. et al., 2016 [68] |
Human (n = 65) | Glioma (II–IV) | 3 | MTRasym | APTw | Proliferation | Park J. et al., 2016 [32] |
Human (n = 32) | GBM (IV), AA (III), gliomas (low–grade) | 3 | MTRasym | APTw | Cellularity | Ma B. et al., 2016 [68] |
Human (n = 7) | AA (III), LGO (II), LGA (II) | 3 | MTRasym | APTw | NA | Zhang Y. et al., 2016 [88] |
Human (n = 44) | Glioma (II–IV) | 3 | MTRasym | APTw | Glioma grading and proliferation | Bai Y. et al., 2017 [63] |
Human (n = 46) | Glioma (II–IV) | 3 | MTRasym | APTw | Glioma grading, protein, and peptide | Choi YS. et al., 2017 [31] |
Human (n = 24) | Glioma (II–IV), edema | 3 | MTRasym | APTw | Cellularity, proliferation, and glioma grading | Jiang S. et al., 2017 [30] |
Human (n = 27) | Glioma (II) | 3 | MTRasym | APTw | IDH mutation | Jiang S. et al., 2017 [29] |
Human (n = 42) | Glioma (II–IV) | 3 | MTRasym | APTw | Glioma grading, proliferation, choline, and N-acetylaspartate | Su C. et al., 2017 [27] |
Human (n = 18) | GBM (IV) | 3 | MTRasym | APTw | MGMT promoter methylation status | Jiang S. et al., 2018 [24] |
Human (n = 57) | Meningioma | 3 | MTRasym | APTw | Intracellular proteins and peptides | Joo B. et al., 2018 [23] |
Human (n = 42) | Glioma (II–IV) | 3 | MTRasym | APTw | MGMT prediction | Su L. et al., 2018 [20] |
Human (n = 21) | GBM (IV), glioma (II), metastases, meningoma, chronic infarction | 3 | MTRasym | APTw | Proteins and peptides | Sun H. et al., 2018 [120] |
Human (n = 32) | Glioma (II–IV) | 3 | Z-spectral fitted, | APT | Glioma grading and proliferation | Zhang J. et al., 2018 [19] |
MTRasym | APTw | |||||
Human (n = 51) | Glioma (II–IV) | 3 | MTRasym | APTw | Glioma grading and mobile cellular proteins | Zou T. et al., 2018 [62] |
Human (n = 21) | GBM (IV), gliosarcoma (IV), AA (III), | 3 | MTRasym | APTw | Cellularity, proliferation, tumor recurrence, and a marker for active glioma | Jiang S. et al., 2019 [18] |
Human (n = 71) | Glioma (III and IV) | 3 | MTRasym | APTw | Overall survival, PFS, and IDH mutation | Joo B. et al., 2019 [17] |
Human (n = 14) | GBM (IV) | 3 | MTRasym | APTw | IDH and pH | Schure JR. et al., 2019 [108] |
Lorentzian | APT | |||||
Human (n = 90) | Glioma (II–IV) | 3 | MTRasym | 3 ppm | Cerebral blood volume and IDH mutation | Wang YL. et al., 2019 [72] |
Human (n = 26) | Glioma (II, IV) Metastasis | 3 | MTRasym | APTw (3.5±0.4 ppm) | Glioma grading, MGMT, and IDH | Durmo F. et al., 2020 [61] |
Human (n = 59) | Glioma (II, III) | 3 | MTRasym, machine learning | APTw | IDH1 mutation | Han Y. et al., 2020 [71] |
Human (n = 54) | GBM (IV) | 3 | MTRasym | APTw | Treatment effect (bevacizumab), 12-month progression, PFS, and CBV | Park J. et al., 2020 [13] |
Human (n = 30) | Glioma (III, IV) | 3 | MTRasym | APTw | Treatment effect (radiotherapy or CRT), tumor recurrence, and protein | Liu J. et al., 2020 [14] |
Human (n = 46) | Glioma (II–IV) | 3 | MTRasym | APTw | Cellularity and CBV glioma grading | Schon S. et al., 2020 [59] |
Human (n = 18) | GBM (IV), AA (III), astrocytoma (III), LGO (II), LGA (II) | 3 | MTRasym | APTw | Cytosolic protein content, mobile proteins, and semisolid macromolecules | Warnert EAH. et al., 2021 [11] |
Lorentzian | APT | |||||
Human (n = 51) | Glioma (II–IV) | 3 | MTRasym | APTw | Glioma grading (peptide or protein concentrations), cellularity, proliferation, and IDH mutation | Xu Z. et al., 2021 [9] |
Human (n = 48) | Glioma (II–IV), Brain metastases | 3 | MTRasym, machine learning | APTw | Protein content | Sartoretti E. et al., 2021 [12] |
Human (n = 19) | GBM, meningioma, brain metastasis | 3 | QUASS | APT, MT&NOE (−1.5 ppm) | −1.5 ppm: proliferation | Wu Y. et al., 2021 [10] |
Human (n = 48) | High–grade glioma (III,IV) Low–grade glioma (I,II) | 3 | CESTRnr, EMR | APT | Glioma grading (proteins and peptides) | Zhang H. et al., 2021 [8] |
Human (n = 81) | H3K27M–mutant associated brainstem glioma | 3 | MTRasym | APTw | H3K27M mutation, proliferation, pH, and protein and peptide metabolism | Zhuo Z. et al., 2021 [6] |
Human (n = 113) | Glioma (II–IV) | 3 | Lorentzian | APT | Glioma grading (cellularity, mobile protein, and peptides), and IDH mutation | Su C. et al., 2022 [5] |
2 ppm | Creatine and 1p/19q co-deletion | |||||
Human (n = 1) | AA (III) | 7 | MTRasym | −3.5 ppm | Cellular density | Jones CK. et al., 2013 [44] |
Lorentzian | APT (3.3 to 3.7 ppm) NOE (−2 to −5 ppm) | |||||
Human (n = 2) | GBM (IV), glioma (II or III) | 7 | MTRasym | −3 ppm | Necrosis and the structural integrity of proteins in cells (protein folding) | Zaiss M. et al., 2013 [121] |
Human (n = 12) | GBM (IV) | 7 | MTRasym | 3.3 ppm | Protein structures proliferation | Paech D. et al., 2014 [41] |
Human (n = 15) | GBM (IV) | 7 | MTRasym | 3.3 ppm | Cell density and edema | Paech D. et al., 2015 [37] |
Human (n = 1) | LGO (II) | 7 | AREX | APT, NOE | NA | Windschuh J. et al., 2015 [35] |
Human (n = 10) | GBM (IV) | 7 | AREX | 3.5 ppm, NOE | Protein and lipid | Zaiss M. et al., 2015 [34] |
Human (n = 10) | Gliomas (II–IV) | 7 | MTRasym | APTw | Glioma grading | Heo HY. et al., 2016 [33] |
EMR | APT (3.3 to 3.7 ppm) NOE (−3.3 to −3.7 ppm) | |||||
Human (n = 11) | GBM (IV) | 7 | MTRasym, dnsAREX | 3.5 ppm | Amide proton and pH | Zaiss M. et al., 2017 [25] |
Human (n = 31) | Glioma (II–IV) | 7 | MTRasym, dnsAREX | APT (3.5 ppm) | Glioma grading, IDH mutation, and MGMT promoter methylation status | Paech D. et al., 2018 [22] |
Human (n = 20) | GBM (IV) | 7 | Lorentzian | NOE | Treatment effect (First-line therapy) | Regnery S. et al., 2018 [21] |
MTRasym | APTw | |||||
dnsAREX | APT | |||||
Human (n = 12) | GBM (IV), LGO (II), LGA (II) | 7 | AREX | NOE | Treatment effect (CRT) | Meissner JE. et al., 2019 [67] |
dnsAREX | APT | |||||
Human (n = 26) | GBM (IV), AA (III) | 7 | AREX, dnsAREX | APT | Overall survival and PFS, amino acid, and protein | Paech D. et al., 2019 [16] |
Human (n = 1) | GBM | 9.4 | Lorentzian | 3.5 ppm, NOE (−1.6, −3.5 ppm), 2 ppm, 2.7 ppm | Proteins and lipids | Zaiss M. et al., 2018 [98] |
2.3. Multiple CEST Contrast in Brain Tumors
3. Non-Metallic CEST Contrast Agents for Brain Tumor Imaging
4. Imaging Drugs and Drug Delivery
4.1. Imaging Drugs and Drug Delivery Using CEST MRI
4.2. Theranostic Applications
5. Technical Part
5.1. CEST Acquisition
5.2. CEST Post-Processing
5.2.1. Z-Spectra and B0/B1 Correction
5.2.2. Z-Spectra Analysis
- (1)
- MTRasym analysis
- (2)
- Lorentzian difference analysis (LDA)
- (3)
- Multi-pool Lorentzian fitting
- (4)
- Polynomial and Lorentzian line-shape fitting (PLOF)
- (5)
- Three-offset method
5.2.3. Inverse Z-Spectra Analysis
5.2.4. Deep Learning-Based Analysis Methods
- (1)
- Deep learning-based Z-spectra analysis
- (2)
- Deep learning-based CEST fingerprinting
6. Promises and Challenges
7. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Huang, J.; Chen, Z.; Park, S.-W.; Lai, J.H.C.; Chan, K.W.Y. Molecular Imaging of Brain Tumors and Drug Delivery Using CEST MRI: Promises and Challenges. Pharmaceutics 2022, 14, 451. https://doi.org/10.3390/pharmaceutics14020451
Huang J, Chen Z, Park S-W, Lai JHC, Chan KWY. Molecular Imaging of Brain Tumors and Drug Delivery Using CEST MRI: Promises and Challenges. Pharmaceutics. 2022; 14(2):451. https://doi.org/10.3390/pharmaceutics14020451
Chicago/Turabian StyleHuang, Jianpan, Zilin Chen, Se-Weon Park, Joseph H. C. Lai, and Kannie W. Y. Chan. 2022. "Molecular Imaging of Brain Tumors and Drug Delivery Using CEST MRI: Promises and Challenges" Pharmaceutics 14, no. 2: 451. https://doi.org/10.3390/pharmaceutics14020451