Evaluation of a similarity anisotropic diffusion denoising approach for improving in vivo CEST-MRI tumor pH imaging.
CEST
MRI
anisotropic diffusion
denoising
iopamidol
pH imaging
Journal
Magnetic resonance in medicine
ISSN: 1522-2594
Titre abrégé: Magn Reson Med
Pays: United States
ID NLM: 8505245
Informations de publication
Date de publication:
06 2021
06 2021
Historique:
received:
10
01
2020
revised:
18
12
2020
accepted:
18
12
2020
pubmed:
27
1
2021
medline:
21
5
2021
entrez:
26
1
2021
Statut:
ppublish
Résumé
Chemical exchange saturation transfer MRI provides new approaches for investigating tumor microenvironment, including tumor acidosis that plays a key role in tumor progression and resistance to therapy. Following iopamidol injection, the detection of the contrast agent inside the tumor tissue allows measurements of tumor extracellular pH. However, accurate tumor pH quantifications are hampered by the low contrast efficiency of the CEST technique and by the low SNR of the acquired CEST images, hence in a reduced detectability of the injected agent. This work aims to investigate a novel denoising method for improving both tumor pH quantification and accuracy of CEST-MRI pH imaging. An hybrid denoising approach was investigated for CEST-MRI pH imaging based on the combination of the nonlocal mean filter and the anisotropic diffusion tensor method. The denoising approach was tested in simulated and in vitro data and compared with previously reported methods for CEST imaging and with established denoising approaches. Finally, it was validated with in vivo data to improve the accuracy of tumor pH maps. The proposed method outperforms current denoising methods in CEST contrast quantification and detection of the administered contrast agent at several increasing noise levels with simulated data. In addition, it achieved a better pH quantification in in vitro data and demonstrated a marked improvement in contrast detection and a substantial improvement in tumor pH accuracy in in vivo data. The proposed approach effectively reduces the noise in CEST images and increases the sensitivity detection in CEST-MRI pH imaging.
Substances chimiques
Iopamidol
JR13W81H44
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3479-3496Informations de copyright
© 2021 International Society for Magnetic Resonance in Medicine.
Références
Yadav NN, Xu J, Bar-Shir A, et al. Natural D-glucose as a biodegradable MRI relaxation agent. Magn Reson Med. 2014;72:823-828.
Cai K, Haris M, Singh A, et al. Magnetic resonance imaging of glutamate. Nat Med. 2012;18:302-306.
Walker-Samuel S, Ramasawmy R, Torrealdea F, et al. In vivo imaging of glucose uptake and metabolism in tumors. Nat Med. 2013;19:1067-1072.
Zhang L, Martins AF, Mai Y, et al. Imaging extracellular lactate in vitro and in vivo using CEST MRI and a paramagnetic shift reagent. Chemistry. 2017;23:1752-1756.
Harris RJ, Cloughesy TF, Liau LM, et al. pH-weighted molecular imaging of gliomas using amine chemical exchange saturation transfer MRI. Neuro Oncol. 2015;17:1514-1524.
Lim H, Albatany M, Martinez-Santiesteban F, Bartha R, Scholl TJ. Longitudinal measurements of intra- and extracellular pH gradient in a rat model of glioma. Tomography. 2018;4:46-54.
Sun PZ, Wang E, Cheung JS. Imaging acute ischemic tissue acidosis with pH-sensitive endogenous amide proton transfer (APT) MRI-correction of tissue relaxation and concomitant RF irradiation effects toward mapping quantitative cerebral tissue pH. Neuroimage. 2012;60:1-6.
Albatany M, Li A, Meakin S, Bartha R. In vivo detection of acute intracellular acidification in glioblastoma multiforme following a single dose of cariporide. Int J Clin Oncol. 2018;23:812-819.
Sun PZ, Xiao G, Zhou IY, Guo Y, Wu R. A method for accurate pH mapping with chemical exchange saturation transfer (CEST) MRI. Contrast Media Mol Imaging. 2016;11:195-202.
Anemone A, Consolino L, Arena F, Capozza M, Longo DL. Imaging tumor acidosis: a survey of the available techniques for mapping in vivo tumor pH. Cancer Metastasis Rev. 2019;38:25-49.
Longo DL, Dastru W, Digilio G, et al. Iopamidol as a responsive MRI-chemical exchange saturation transfer contrast agent for pH mapping of kidneys: in vivo studies in mice at 7 T. Magn Reson Med. 2011;65:202-211.
Longo DL, Sun PZ, Consolino L, Michelotti FC, Uggeri F, Aime S. A general MRI-CEST ratiometric approach for pH imaging: demonstration of in vivo pH mapping with iobitridol. J Am Chem Soc. 2014;136:14333-14336.
Longo DL, Bartoli A, Consolino L, et al. In vivo imaging of tumor metabolism and acidosis by combining PET and MRI-CEST pH imaging. Cancer Res. 2016;76:6463-6470.
Chen M, Chen C, Shen Z, et al. Extracellular pH is a biomarker enabling detection of breast cancer and liver cancer using CEST MRI. Oncotarget. 2017;8:45759-45767.
Delli Castelli D, Ferrauto G, Cutrin JC, Terreno E, Aime S. In vivo maps of extracellular pH in murine melanoma by CEST-MRI. Magn Reson Med. 2014;71:326-332.
Chauvin T, Durand P, Bernier M, et al. Detection of enzymatic activity by PARACEST MRI: a general approach to target a large variety of enzymes. Angew Chem Int Ed Engl. 2008;47:4370-4372.
Hingorani DV, Yoo B, Bernstein AS, Pagel MD. Detecting enzyme activities with exogenous MRI contrast agents. Chemistry. 2014;20:9840-9850.
Anemone A, Consolino L, Conti L, et al. In vivo evaluation of tumour acidosis for assessing the early metabolic response and onset of resistance to dichloroacetate by using magnetic resonance pH imaging. Int J Oncol. 2017;51:498-506.
Goldenberg JM, Cardenas-Rodriguez J, Pagel MD. Preliminary results that assess metformin treatment in a preclinical model of pancreatic cancer using simultaneous [(18)F]FDG PET and acidoCEST MRI. Mol Imaging Biol. 2018;20:575-583.
Jones KM, Randtke EA, Yoshimaru ES, et al. Clinical translation of tumor acidosis measurements with AcidoCEST MRI. Mol Imaging Biol. 2017;19:617-625.
Muller-Lutz A, Khalil N, Schmitt B, et al. Pilot study of Iopamidol-based quantitative pH imaging on a clinical 3T MR scanner. MAGMA. 2014;27:477-485.
Knutsson L, Seidemo A, Rydhog Scherman A, et al. Arterial input functions and tissue response curves in dynamic glucose-enhanced (DGE) imaging: comparison between glucoCEST and blood glucose sampling in humans. Tomography. 2018;4:164-171.
Zaiss M, Anemone A, Goerke S, et al. Quantification of hydroxyl exchange of D-Glucose at physiological conditions for optimization of glucoCEST MRI at 3, 7 and 9.4 Tesla. NMR Biomed. 2019;32:e4113.
Anemone A, Consolino L, Longo DL. MRI-CEST assessment of tumour perfusion using X-ray iodinated agents: comparison with a conventional Gd-based agent. Eur Radiol. 2017;27:2170-2179.
Longo DL, Michelotti F, Consolino L, et al. In vitro and in vivo assessment of nonionic iodinated radiographic molecules as chemical exchange saturation transfer magnetic resonance imaging tumor perfusion agents. Invest Radiol. 2016;51:155-162.
Liu G, Song X, Chan KW, McMahon MT. Nuts and bolts of chemical exchange saturation transfer MRI. NMR Biomed. 2013;26:810-828.
Deshmane A, Zaiss M, Lindig T, et al. 3D gradient echo snapshot CEST MRI with low power saturation for human studies at 3T. Magn Reson Med. 2019;81:2412-2423.
Zaiss M, Ehses P, Snapshot-CEST SK. Optimizing spiral-centric-reordered gradient echo acquisition for fast and robust 3D CEST MRI at 9.4 T. NMR Biomed. 2018;31:e3879.
Perlman O, Herz K, Zaiss M, Cohen O, Rosen MS, Farrar CT. CEST MR-fingerprinting: practical considerations and insights for acquisition schedule design and improved reconstruction. Magn Reson Med. 2020;83:462-478.
Cohen O, Huang S, McMahon MT, Rosen MS, Farrar CT. Rapid and quantitative chemical exchange saturation transfer (CEST) imaging with magnetic resonance fingerprinting (MRF). Magn Reson Med. 2018;80:2449-2463.
Kim J, Wu Y, Guo Y, Zheng H, Sun PZ. A review of optimization and quantification techniques for chemical exchange saturation transfer MRI toward sensitive in vivo imaging. Contrast Media Mol Imaging. 2015;10:163-178.
Mohan J, Krishnaveni V, Guo Y. A survey on the magnetic resonance image denoising methods. Biomed Signal Proces. 2014;9:56-69.
Krissian K, Malandain G, Ayache N, Vaillant R, Trousset Y. Model-based detection of tubular structures in 3D images. Comput Vis Image Underst. 2000;80:130-171.
Kroon DJ, Slump CH, Maal TJ. Optimized anisotropic rotational invariant diffusion scheme on cone-beam CT. Med Image Comput Comput Assist Interv. 2010;13(Pt 3):221-228.
Perona P, Malik J. Scale-space and edge-detection using anisotropic diffusion. IEEE Trans Pattern Anal. 1990;12:629-639.
Romdhane F, Benzarti F, Amiri H. 3D medical images denoising. In: Proceedings of the First International Image Processing, Applications and Systems Conference, Hammamet, Tunisia, 2014.
Rudin LI, Osher S, Fatemi E. Nonlinear total variation based noise removal algorithms. Physica D. 1992;60:259-268.
Weickert J. Coherence-enhancing diffusion filtering. Int J Comput Vis. 1999;31:111-127.
Buades A, Coll B, Morel JM. A review of image denoising algorithms, with a new one. Multiscale Model Sim. 2005;4:490-530.
Dabov K, Foi A, Katkovnik V, Egiazarian K. Image denoising by sparse 3-D transform-domain collaborative filtering. IEEE Trans Image Process. 2007;16:2080-2095.
Baselice F, Ferraioli G, Pascazio V. A 3D MRI denoising algorithm based on Bayesian theory. Biomed Eng Online. 2017;16:25.
Baselice F, Ferraioli G, Pascazio V, Sorriso A. Bayesian MRI denoising in complex domain. Magn Reson Imaging. 2017;38:112-122.
Gonzalez JE, Thompson PM, Zhao A, Tu Z. Modeling diffusion-weighted MRI as a spatially variant gaussian mixture: application to image denoising. Med Phys. 2011;38:4350-4364.
Manjon JV, Coupe P, Buades A, Louis Collins D, Robles M. New methods for MRI denoising based on sparseness and self-similarity. Med Image Anal. 2012;16:18-27.
Bhujle HV, Vadavadagi BH. NLM based magnetic resonance image denoising-a review. Biomed Signal Proces. 2019;47:252-261.
Liu H, Yang C, Pan N, Song E, Green R. Denoising 3D MR images by the enhanced non-local means filter for Rician noise. Magn Reson Imaging. 2010;28:1485-1496.
Wu X, Liu SJ, Wu M, et al. Nonlocal denoising using anisotropic structure tensor for 3D MRI. Med Phys. 2013;40:101904.
Decker CM, Zollner FG, Konstandin S, Schad LR. Comparing anisotropic diffusion filters for the enhancement of sodium magnetic resonance images. Magn Reson Imaging. 2012;30:1192-1200.
Zollner FG, Emblem KE, Schad LR. SVM-based glioma grading: optimization by feature reduction analysis. Z Med Phys. 2012;22:205-214.
Terreno E, Stancanello J, Longo D, et al. Methods for an improved detection of the MRI-CEST effect. Contrast Media Mol Imaging. 2009;4:237-247.
Randtke EA, Granados JC, Howison CM, Pagel MD, Cardenas-Rodriguez J. Multislice CEST MRI improves the spatial assessment of tumor pH. Magn Reson Med. 2017;78:97-106.
Breitling J, Deshmane A, Goerke S, et al. Adaptive denoising for chemical exchange saturation transfer MR imaging. NMR Biomed. 2019:e4133.
Yuan J, Mok GSP, Zhang Q, Wang Y, Zhou J. Improved quantification of chemical exchange saturation transfer (CEST) MRI using nonlocal means. In: Proceedings of the IEEE Nuclear Science Symposium and Medical Imaging Conference, Seattle, Washington, 2014.
Romdhane F, Benzarti F, Amiri H. A new method for three-dimensional magnetic resonance images denoising. Int J Comput Vis Robot. 2018;8:1-17.
Romdhane F, Benzarti F, Amiri H. 3D CT denoising by new combination between Nl-mean filter and diffusion tensor. Adv Intell Syst. 2017;552:233-243.
Coupe P, Yger P, Barillot C. Fast non local means denoising for 3D MR images. Med Image Comput Comput Assist Interv. 2006;9(Pt 2):33-40.
Coupe P, Manjon JV, Gedamu E, Arnold D, Robles M, Collins DL. An object-based method for Rician noise estimation in MR images. Med Image Comput Comput Assist Interv. 2009;12(Pt 2):601-608.
Pop S, Olivier L, Romulus T, Monica B. A new partial differential equation-based approach for 3D data denoising and edge preserving. Revue Roumaine des Sciences Techniques - Serie Électrotechnique et Énergétique. 2007;52:407-418.
Moon BF, Jones KM, Chen LQ, et al. A comparison of iopromide and iopamidol, two acidoCEST MRI contrast media that measure tumor extracellular pH. Contrast Media Mol Imaging. 2015;10:446-455.
Stancanello J, Terreno E, Castelli DD, Cabella C, Uggeri F, Aime S. Development and validation of a smoothing-splines-based correction method for improving the analysis of CEST-MR images. Contrast Media Mol Imaging. 2008;3:136-149.
Zaiss M. CEST-sources.org. https://www.cest-sources.org/doku.php. Accessed March 11, 2019.
Zaiss M, Schmitt B, Bachert P. Quantitative separation of CEST effect from magnetization transfer and spillover effects by Lorentzian-line-fit analysis of z-spectra. J Magn Reson. 2011;211:149-155.
Isa IS, Sulaiman SN, Mustapha M, Darus S. Evaluating denoising performances of fundamental filters for T2-weighted MRI images. Procedia Comput Sci. 2015;60:760-768.
Wang Z, Bovik AC. A universal image quality index. IEEE Signal Process Let. 2002;9:81-84.
Wang Z, Bovik AC, Sheikh HR, Simoncelli EP. Image quality assessment: from error visibility to structural similarity. IEEE Trans Image Process. 2004;13:600-612.
Zhou J, Payen JF, Wilson DA, Traystman RJ, van Zijl PC. Using the amide proton signals of intracellular proteins and peptides to detect pH effects in MRI. Nat Med. 2003;9:1085-1090.
Zhou IY, Wang E, Cheung JS, Zhang X, Fulci G, Sun PZ. Quantitative chemical exchange saturation transfer (CEST) MRI of glioma using Image Downsampling Expedited Adaptive Least-squares (IDEAL) fitting. Sci Rep. 2017;7:84.
Kujawa A, Kim M, Demetriou E, et al. Assessment of a clinically feasible Bayesian fitting algorithm using a simplified description of Chemical Exchange Saturation Transfer (CEST) imaging. J Magn Reson. 2019;300:120-134.
Dopfert J, Witte C, Kunth M, Schroder L. Sensitivity enhancement of (Hyper-)CEST image series by exploiting redundancies in the spectral domain. Contrast Media Mol Imaging. 2014;9:100-107.
Chen L, Cao S, Koehler RC, Zijl PCM, Xu J. High-sensitivity CEST mapping using a spatiotemporal correlation-enhanced method. Magn Reson Med. 2020;84:3342-3350.
Villano D, Romdhane F, Irrera P, et al. A fast multislice sequence for 3D MRI-CEST pH imaging. Magn Reson Med. 2021;85:1335-1349.
Paech D, Dreher C, Regnery S, et al. Relaxation-compensated amide proton transfer (APT) MRI signal intensity is associated with survival and progression in high-grade glioma patients. Eur Radiol. 2019;29:4957-4967.
Lee DH, Heo HY, Zhang K, et al. Quantitative assessment of the effects of water proton concentration and water T1 changes on amide proton transfer (APT) and nuclear Overhauser enhancement (NOE) MRI: the origin of the APT imaging signal in brain tumor. Magn Reson Med. 2017;77:855-863.