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Research progress of amide proton transfer magnetic resonance imaging in Parkinson's disease
MIRIBAN·Maimaitikuerban   ZHANG Shuxian  MA Jingxu  WANG Hong 

Cite this article as: MIRIBAN·M M T K E B, ZHANG S X, MA J X, et al. Research progress of amide proton transfer magnetic resonance imaging in Parkinson's disease[J]. Chin J Magn Reson Imaging, 2023, 14(6): 94-98. DOI:10.12015/issn.1674-8034.2023.06.016.


[Abstract] Amide proton transfer (APT) imaging technology is a new and original MRI technology developed in recent years on the basis of chemical exchange saturation transfer (CEST) imaging, which is based on the non-invasive detection and evaluation of protein concentration and pH at the cellular and molecular level, indirectly reflects the metabolic changes and physiological and pathological information in living cells. Parkinson's disease (PD) is the second most common neurodegenerative disease, which has not been eradicated yet, patients take drugs to control symptoms and maintain daily life. Early detection and diagnosis of PD is the key to treatment, and patients benefit greatly. APT imaging technology can evaluate the protein metabolism status of various brain regions in patients with PD and help to realize the early diagnosis of PD. This article reviews the basic principles of APT MRI technology, research progress in PD, and challenges faced in its application, aiming to better understand the APT imaging technology and provide reference for future research.
[Keywords] Parkinson's disease；magnetic resonance imaging；amide proton transfer imaging；chemical exchange saturation transfer；research progress；early diagnosis；differential diagnosis

MIRIBAN·Maimaitikuerban    ZHANG Shuxian   MA Jingxu   WANG Hong*  

Imaging Center, the Second Affiliated Hospital of Xinjiang Medical University, Urumqi 830063, China

Corresponding author: Wang H, E-mail: wangh_xj@163.com

Conflicts of interest   None.

ACKNOWLEDGMENTS Natural Science Foundation of Xinjiang Uygur Autonomous Region (No. 2022D01C272, 2019D01C227).
Received  2023-02-03
Accepted  2023-04-20
DOI: 10.12015/issn.1674-8034.2023.06.016
Cite this article as: MIRIBAN·M M T K E B, ZHANG S X, MA J X, et al. Research progress of amide proton transfer magnetic resonance imaging in Parkinson's disease[J]. Chin J Magn Reson Imaging, 2023, 14(6): 94-98. DOI:10.12015/issn.1674-8034.2023.06.016.

[1]
CHEN Z J, MA J, TANG N, et al. Disease burden trend analysis and prediction of Parkinson's disease in China[J]. Chin J Prev Contr Chron Dis, 2022, 30(9): 649-654. DOI: 10.16386/j.cjpccd.issn.1004-6194.2022.09.003.
[2]
DORSEY E R, SHERER T, OKUN M S, et al. The Emerging Evidence of the Parkinson Pandemic[J]. J Parkinsons Dis, 2018, 8(s1): S3-S8. DOI: 10.3233/JPD-181474.
[3]
LI G, MA J, CUI S, et al. Parkinson's disease in China: a forty-year growing track of bedside work[J]. Transl Neurodegener, 2019, 8: 22. DOI: 10.1186/s40035-019-0162-z.
[4]
MA X, LI S, LI C, et al. Diffusion Tensor Imaging Along the Perivascular Space Index in Different Stages of Parkinson's Disease[J]. Front Aging Neurosci, 2021, 15(13): 773951. DOI: 10.3389/fnagi.2021.773951.
[5]
HALLER S, HAACKE E M, THURNHER M M, et al. Susceptibility-weighted Imaging: Technical Essentials and Clinical Neurologic Applications[J]. Radiology, 2021, 299(1): 3-26. DOI: 10.1148/radiol.2021203071.
[6]
LE H, ZENG W, ZHANG H, et al. Mean apparent propagator MRI is better than conventional diffusion tensor imaging for the evaluation of Parkinson's disease: a prospective pilot study[J]. Front Aging Neurosci, 2020, 12: 563595. DOI: 10.3389/fnagi.2020.563595.
[7]
CHENG L, WU X, GUO R, et al. Discriminative pattern of reduced cerebral blood flow in Parkinson's disease and Parkinsonism-plus syndrome: an ASL-MRI study[J]. BMC Med Imaging, 2020, 20(1): 78. DOI: 10.1186/s12880-020-00479-y.
[8]
THOMAS G E C, LEYLAND L A, SCHRAG A E, et al. Brain iron deposition is linked with cognitive severity in Parkinson's disease[J]. J Neurol Neurosurg Psychiatry, 2020, 91(4): 418-425. DOI: 10.1136/jnnp-2019-322042.
[9]
DONAHUE E K, BUI V, FOREMAN R P, et al. Magnetic resonance spectroscopy shows associations between neurometabolite levels and perivascular space volume in Parkinson's disease: a pilot and feasibility study[J]. Neuroreport, 2022, 33(7): 291-296. DOI: 10.1097/WNR.0000000000001781.
[10]
SUNG S, FARRELL M, VIJIARATNAM N, et al. Pain and dyskinesia in Parkinson's disease may share common pathophysiological mechanisms-An fMRI study[J]. J Neurol Sci, 2020, 15(416): 116905. DOI: 10.1016/j.jns.2020.116905.
[11]
HUANG X P, HAN H Y, WANG M, et al. Clinical research of NODDI technology in deep brain nucleus of Parkinson's disease[J]. Chin J Magn Reson Imaging, 2021, 12(3): 6-9, 19. DOI: 10.12015/issn.1674-8034.2021.03.002.
[12]
PATHAK N, VIMAL S K, TANDON I, et al. Neurodegenerative Disorders of Alzheimer, Parkinsonism, Amyotrophic Lateral Sclerosis and Multiple Sclerosis: An Early Diagnostic Approach for Precision Treatment[J]. Metab Brain Dis, 2022, 37(1): 67-104. DOI: 10.1007/s11011-021-00800-w.
[13]
VAN ZIJL P C, ZHOU J, MORI N, et al. Mechanism of magnetization transfer during on-resonance water saturation. A new approach to detect mobile proteins, peptides, and lipids[J]. Magn Reson Med, 2003, 49(3): 440-449. DOI: 10.1002/mrm.10398.
[14]
WARD K M, ALETRAS A H, BALABAN R S. A new class of contrast agents for MRI based on proton chemical exchange dependent saturation transfer (CEST)[J]. J Magn Reson, 2000, 143: 79-87. DOI: 10.1006/jmre.1999.1956.
[15]
KOGAN F, HARIHARAN H, REDDY R. Chemical exchange saturation transfer (CEST) imaging: description of technique and potential clinical applications[J]. Curr Radiol Rep, 2013, 1: 102-114. DOI: 10.1007/s40134-013-0010-3.
[16]
VAN ZIJL P C, YADAV N N. Chemical exchange saturation transfer (CEST): what is in a name and what isn't?[J]. Magn Reson Med, 2011, 65(4): 927-948. DOI: 10.1002/mrm.22761.
[17]
CEMBER A T J, NANGA R P R, REDDY R. Glutamate-weighted CEST (gluCEST) imaging for mapping neurometabolism: An update on the state of the art and emerging findings from in vivo applications[J]. NMR Biomed, 2022, 31: 4780. DOI: 10.1002/nbm.4780.
[18]
LIU Z, YANG Q, LUO H, et al. Demonstration of fast and equilibrium human muscle creatine CEST imaging at 3 T[J]. Magn Reson Med, 2022, 88(1): 322-331. DOI: 10.1002/mrm.29223.
[19]
ANEMONE A, CAPOZZA M, ARENA F, et al. In vitro and in vivo comparison of MRI chemical exchange saturation transfer (CEST) properties between native glucose and 3-O-Methyl-D-glucose in a murine tumor model[J/OL]. NMR Biomed, 2021, 34(12): e4602 [2023-02-02]. https://pubmed.ncbi.nlm.nih.gov/34423470/. DOI: 10.1002/nbm.4602.
[20]
GILAD A A, BAR-SHIR A, BRICCO A R, et al. Protein and peptide engineering for chemical exchange saturation transfer imaging in the age of synthetic biology[J]. NMR Biomed, 2022, 11: 4712. DOI: 10.1002/nbm.4712.
[21]
ZHOU J, HEO H Y, KNUTSSON L, et al. APT-weighted MRI: Techniques, current neuro applications, and challenging issues[J]. J Magn Reson Imaging, 2019, 50(2): 347-364. DOI: 10.1002/jmri.26645.
[22]
ZHOU J, PAYEN J F, WILSON D A, et al. Using the amide proton signals of intracellular proteins and peptides to detect pH effects in MRI[J]. Nat Med, 2003, 9(8): 1085-1090. DOI: 10.1038/nm907.
[23]
LU J, ZHOU J, CAI C, et al. Observation of true and pseudo NOE signals using CEST-MRI and CEST-MRS sequences with and without lipid suppression[J]. Magn Reson Med, 2015, 73: 1615-1622. DOI: 10.1002/mrm.25277.
[24]
GOERKE S, SOEHNGEN Y, DESHMANE A, et al. Relaxation-compensated APT and rNOE CEST-MRI of human brain tumors at 3 T[J]. Magn Reson Med, 2019, 82(2): 622-632. DOI: 10.1002/mrm.27751.
[25]
MUELLER S, STIRNBERG R, AKBEY S, et al. Whole brain snapshot CEST at 3T using 3D-EPI: Aiming for speed, volume, and homogeneity[J]. Magn Reson Med, 2020, 84(5): 2469-2483. DOI: 10.1002/mrm.28298.
[26]
HEO H Y, ZHANG Y, LEE D H, et al. Quantitative assessment of amide proton transfer (APT) and nuclear Overhauser enhancement (NOE) imaging with extrapolated semi‐solid magnetization transfer reference (EMR) signals: application to a rat glioma model at 4.7 Tesla[J]. Magn Reson Med, 2016, 75(1): 137-149. DOI: 10.1002/mrm.25581.
[27]
CHEN L, BARKER P B, WEISS R G, et al. Creatine and phosphocreatine mapping of mouse skeletal muscle by a polynomial and Lorentzian line-shape fitting CEST method[J]. Magn Reson Med, 2019, 81(1): 69-78. DOI: 10.1002/mrm.27514.
[28]
RAY K J, SIMARD M A, LARKIN J R, et al. Tumor pH and protein concentration contribute to the signal of amide proton transfer magnetic resonance imaging[J]. Cancer Res, 2019, 79(7): 1343-1352. DOI: 10.1158/0008-5472.CAN-18-2168.
[29]
ZHOU J, ZAISS M, KNUTSSON L, et al. Review and consensus recommendations on clinical APT-weighted imaging approaches at 3T: Application to brain tumors[J]. Magn Reson Med, 2022, 88(2): 546-574. DOI: 10.1002/mrm.29241.
[30]
KOIKE H, MORIKAWA M, ISHIMARU H, et al. Amide proton transfer MRI differentiates between progressive multifocal leukoencephalopathy and malignant brain tumors: a pilot study[J]. BMC Med Imaging, 2022, 22(1): 227. DOI: 10.1186/s12880-022-00959-3.
[31]
YU L, LI C, LUO X, et al. Differentiation of malignant and benign head and neck tumors with amide proton transfer-weighted mr imaging[J]. Mol Imaging Biol, 2019, 21(2): 348-355. DOI: 10.1007/s11307-018-1248-1.
[32]
NAKAJO M, BOHARA M, KAMIMURA K, et al. Correlation between amide proton transfer-related signal intensity and diffusion and perfusion magnetic resonance imaging parameters in high-grade glioma[J]. Sci Rep, 2021, 11: 11223. DOI: 10.1038/s41598-021-90841-z.
[33]
FOO L S, HARSTON G, MEHNDIRATTA A, et al. Clinical translation of amide proton transfer (APT) MRI for ischemic stroke: a systematic review (2003-2020)[J]. Quant Imaging Med Surg, 2021, 11(8): 3797-3811. DOI: 10.21037/qims-20-1339.
[34]
CHEN S, LIU X, LIN J, et al. Application of amide proton transfer imaging for the diagnosis of neonatal hypoxic-ischemic encephalopathy[J]. Front Pediatr, 2022, 11(10): 996949. DOI: 10.3389/fped.2022.996949.
[35]
ZHANG H, ZHOU J, PENG Y. Amide Proton Transfer-Weighted MR Imaging of Pediatric Central Nervous System Diseases[J]. Magn Reson Imaging Clin N Am, 2021, 29(4): 631-641. DOI: 10.1016/j.mric.2021.06.012.
[36]
WANG D, WANG X N, GAO P, et al. Application of Amide Proton Transfer Magnetic Resonance Imaging in Alzheimer's Disease and Mild Cognitive Impairment[J]. Chinese Journal of Medical Imaging, 2022, 30(5): 430-434. DOI: 10.3969/j.issn.1005-5185.2022.05.003.
[37]
SARTORETTI E, SARTORETTI T, WYSS M, et al. Amide proton transfer weighted imaging shows differences in multiple sclerosis lesions and white matter hyperintensities of presumed vascular origin[J]. Front Neurol, 2019, 10: 1307. DOI: 10.3389/fneur.2019.01307.
[38]
WANG W, ZHANG H, LEE D H, et al. Using functional and molecular MRI techniques to detect neuroinflammation and neuroprotection after traumatic brain injury[J]. Brain Behav Immun, 2017, 64: 344-353. DOI: 10.1016/j.bbi.2017.04.019.
[39]
ZIMMERMANN F, KORZOWSKI A, BREITLING J, et al. A novel normalization for amide proton transfer CEST MRI to correct for fat signal-induced artifacts: application to human breast cancer imaging[J]. Magn Reson Med, 2020, 83(3): 920-934. DOI: 10.1002/mrm.27983.
[40]
LIN Y, LUO X, YU L, et al. Amide proton transfer-weighted MRI for predicting histological grade of hepatocellular carcinoma: comparison with diffusion-weighted imaging[J]. Quant Imaging Med Surg, 2019, 9(10): 1641-1651. DOI: 10.21037/qims.2019.08.07.
[41]
WANG H J, CAI Q, HUANG Y P, et al. Amide Proton Transfer-weighted MRI in Predicting Histologic Grade of Bladder Cancer[J]. Radiology, 2022, 305(1): 127-134. DOI: 10.1148/radiol.211804.
[42]
WEI Q, YUAN W, JIA Z, et al. Preoperative MR radiomics based on high-resolution T2-weighted images and amide proton transfer-weighted imaging for predicting lymph node metastasis in rectal adenocarcinoma[J]. Abdom Radiol (NY), 2022. DOI: 10.1007/s00261-022-03731-x.
[43]
TIAN S, CHEN A, LI Y, et al. The combined application of amide proton transfer imaging and diffusion kurtosis imaging for differentiating stage Ia endometrial carcinoma and endometrial polyps[J/OL]. Magn Reson Imaging, 2023, 2(22): S0730-725X00241-7 [2023-02-02]. https://pubmed.ncbi.nlm.nih.gov/36603780/. DOI: 10.1016/j.mri.2022.12.026.
[44]
HE Y L, LI Y, LIN C Y, et al. Three-dimensional turbo-spin-echo amide proton transfer-weighted MRI for cervical cancer: a preliminary study[J]. J Magn Reson Imaging, 2019, 50(4): 1318-1325. DOI: 10.1002/jmri.26710.
[45]
YIN H, WANG D, YAN R, et al. Comparison of Diffusion Kurtosis Imaging and Amide Proton Transfer Imaging in the Diagnosis and Risk Assessment of Prostate Cancer[J]. Front Oncol, 2021, 11: 640906. DOI: 10.3389/fonc.2021.640906.
[46]
ZHANG P Y, TANG Y X, JIANG H Y, et al. Feasibility study of three-dimensional amide proton transfer imaging in differentiating prostate cancer with and without bone metastasis[J]. Chin J Magn Reson Imaging, 2022, 13(12): 100-103, 110. DOI: 10.12015/issn.1674-8034.2022.12.017.
[47]
MANCINI L, CASAGRANDA S, GAUTIER G, et al. CEST MRI provides amide/amine surrogate biomarkers for treatment-naïve glioma sub-typing[J]. Eur J Nucl Med Mol Imaging, 2022, 49(7): 2377-2391. DOI: 10.1007/s00259-022-05676-1.
[48]
TOLOSA E, GARRIDO A, SCHOLZ S W, et al. Challenges in the diagnosis of Parkinson's disease[J]. Lancet Neurol, 2021, 20(5): 385-397. DOI: 10.1016/S1474-4422(21)00030-2.
[49]
DI MAIO R, HOFFMAN E K, ROCHA E M, et al. LRRK2 activation in idiopathic Parkinson's disease[J]. Sci Transl Med, 2018, 25(10): 451. DOI: 10.1126/scitranslmed.aar5429.
[50]
BLOEM B R, OKUN M S, KLEIN C. Parkinson's disease[J]. Lancet, 2021, 397(10291): 2284-2303. DOI: 10.1016/S0140-6736(21)00218-X.
[51]
KWON E H, TENNAGELS S, GOLD R, et al. Update on CSF Biomarkers in Parkinson's Disease[J]. Biomolecules, 2022, 12(2): 329. DOI: 10.3390/biom12020329.
[52]
LI C, PENG S, WANG R, et al. Chemical exchange saturation transfer MR imaging of Parkinson's disease at 3 Tesla[J]. Eur Radiol, 2014, 24(10): 2631-2639. DOI: 10.1007/s00330-014-3241-7.
[53]
LI C, CHEN M, ZHAO X, et al. Chemical Exchange Saturation Transfer MRI Signal Loss of the Substantia Nigra as an Imaging Biomarker to Evaluate the Diagnosis and Severity of Parkinson's Disease[J]. Front Neurosci, 2017, 11: 489. DOI: 10.3389/fnins.2017.00489.
[54]
LI C, WANG R, CHEN H, et al. Chemical exchange saturation transfer MR imaging is superior to diffusion-tensor imaging in the diagnosis and severity evaluation of Parkinson's disease: a study on substantia nigra and striatum[J]. Front Aging Neurosci, 2015, 7: 198. DOI: 10.3389/fnagi.2015.00198.
[55]
MENNECKE A, KHAKZAR K M, GERMAN A, et al. 7 tricks for 7 T CEST: Improving the reproducibility of multipool evaluation provides insights into the effects of age and the early stages of Parkinson's disease[J]. NMR Biomed, 2022, 22: 4717. DOI: 10.1002/nbm.4717.
[56]
LI S, CHAN P, LI C, et al. Changes of Amide Proton Transfer Imaging in Multiple System Atrophy Parkinsonism Type[J]. Front Aging Neurosci, 2020, 30(12): 572421. DOI: 10.3389/fnagi.2020.572421.
[57]
WAMELINK I J H G, KUIJER J P A, PADRELA B E, et al. Reproducibility of 3 T APT-CEST in Healthy Volunteers and Patients With Brain Glioma[J]. J Magn Reson Imaging, 2023, 57(1): 206-215. DOI: 10.1002/jmri.28239.
[58]
LEE J B, PARK J E, JUNG S C, et al. Repeatability of amide proton transfr-weighted signals in the brain according to clinical condition and anatomical location[J]. Eur Radiol, 2020, 30(1): 346-356. DOI: 10.1007/s00330-019-06285-7.
[59]
ZHOU J, ZHU H, LIM M, et al. Three-dimensional amide proton transfer MR imaging of gliomas: Initial experience and comparison with gadolinium enhancement[J]. J Magn Reson Imaging, 2013, 38(5): 1119-1128. DOI: 10.1002/jmri.24067.
[60]
WADA T, TOKUNAGA C, TOGAO O, et al. Three-dimensional chemical exchange saturation transfer imaging using compressed SENSE for full z-spectrum acquisition[J]. Magn Reson Imaging, 2022, 92: 58-66. DOI: 10.1016/j.mri.2022.05.014.
[61]
LIEBERT A, TKOTZ K, HERRLER J, et al. Whole-brain quantitative CEST MRI at 7T using parallel transmission methods and correction[J]. Magn Reson Med, 2021, 86(1): 346-362. DOI: 10.1002/mrm.28745.
[62]
LIEBERT A, ZAISS M, GUMBRECHT R, et al. Multiple interleaved mode saturation (MIMOSA) for B1+ inhomogeneity mitigation in chemical exchange saturation transfer[J]. Magn Reson Med, 2019, 82(2): 693-705. DOI: 10.1002/mrm.27762.
[63]
ZAISS M, HERZ K, DESHMANE A, et al. Possible artifacts in dynamic CEST MRI due to motion and field alterations[J]. J Magn Reson, 2019, 298: 16-22. DOI: 10.1016/j.jmr.2018.11.002.
[64]
SUI R, CHEN L, LI Y, et al. Whole-brain amide CEST imaging at 3T with a steady-state radial MRI acquisition[J]. Magn Reson Med, 2021, 86(2): 893-906. DOI: 10.1002/mrm.28770.
[65]
SUN P Z. Quasi–steady-state amide proton transfer (QUASS APT) MRI enhances pH-weighted imaging of acute stroke[J]. Magn Reson Med, 2022, 88: 2633-2644. DOI: 10.1002/mrm.29408.
[66]
PERLMAN O, ITO H, HERZ K, et al. Quantitative imaging of apoptosis following oncolytic virotherapy by magnetic resonance fingerprinting aided by deep learning[J]. Nat Biomed Eng, 2022, 6(5): 648-657. DOI: 10.1038/s41551-021-00809-7.
[67]
ZAISS M, EHSES P, SCHEFFLER K. Snapshot-CEST: Optimizing spiral-centric-reordered gradient echo acquisition for fast and robust 3D CEST MRI at 9.4 T[J]. NMR Biomed, 2018, 31(4): 3879. DOI: 10.1002/nbm.3879.
[68]
KIM B, SCHÄR M, PARK H, et al. A deep learning approach for magnetization transfer contrast MR fingerprinting and chemical exchange saturation transfer imaging[J]. Neuroimage, 2020, 1(221): 117165. DOI: 10.1016/j.neuroimage.2020.117165.
[69]
KANG B, KIM B, SCHÄR M, et al. Unsupervised learning for magnetization transfer contrast MR fingerprinting: Application to CEST and nuclear Overhauser enhancement imaging[J]. Magn Reson Med, 2021, 85: 2040-2054. DOI: 10.1002/mrm.28573.

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