Hybrid magnetic resonance and optoacoustic tomography (MROT) for preclinical neuroimaging

Zhenyue Chen; Irmak Gezginer; Mark-Aurel Augath; Wuwei Ren; Yu-Hang Liu; Ruiqing Ni; Xosé Luís Deán-Ben; Daniel Razansky

doi:10.1038/s41377-022-01026-w

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Hybrid magnetic resonance and optoacoustic tomography (MROT) for preclinical neuroimaging

Original Articles

- Hybrid magnetic resonance and optoacoustic tomography (MROT) for preclinical neuroimaging
- Light: Science & Applications Vol. 11, Issue 12, Pages: 2961-2971(2022)
- Affiliations：
  
  1.Institute for Biomedical Engineering and Institute of Pharmacology and Toxicology, Faculty of Medicine, University of Zurich, Zurich, Switzerland
  2.Institute for Biomedical Engineering, Department of Information Technology and Electrical Engineering, ETH Zurich, Zurich, Switzerland
  3.Zurich Neuroscience Center (ZNZ), Zurich, Switzerland
- Author bio：
  
  Daniel Razansky (daniel.razansky@uzh.ch)
- Funds：
- DOI：10.1038/s41377-022-01026-w
  CLC：
- Published：31 December 2022，
  
  Published Online：24 November 2022，
  
  Received：27 May 2022，
  
  Revised：13 October 2022，
  
  Accepted：24 October 2022
- Accepted：
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Chen, Z. Y. et al. Hybrid magnetic resonance and optoacoustic tomography (MROT) for preclinical neuroimaging. Light: Science & Applications, 11, 2961-2971 (2022).
DOI：

Chen, Z. Y. et al. Hybrid magnetic resonance and optoacoustic tomography (MROT) for preclinical neuroimaging. Light: Science & Applications, 11, 2961-2971 (2022). DOI： 10.1038/s41377-022-01026-w.

摘要

Abstract

Multi-modal imaging is essential for advancing our understanding of brain function and unraveling pathophysiological processes underlying neurological and psychiatric disorders. Magnetic resonance (MR) and optoacoustic (OA) imaging have been shown to provide highly complementary contrasts and capabilities for preclinical neuroimaging. True integration between these modalities can thus offer unprecedented capabilities for studying the rodent brain in action. We report on a hybrid magnetic resonance and optoacoustic tomography (MROT) system for concurrent noninvasive structural and functional imaging of the mouse brain. Volumetric OA tomography was designed as an insert into a high-field MR scanner by integrating a customized MR-compatible spherical transducer array

an illumination module

and a dedicated radiofrequency coil. A tailored data processing pipeline has been developed to mitigate signal crosstalk and accurately register image volumes acquired with T1-weighted

angiography

and blood oxygenation level-dependent (BOLD) sequences onto the corresponding vascular and oxygenation data recorded with the OA modality. We demonstrate the concurrent acquisition of dual-mode anatomical and angiographic brain images with the scanner

as well as real-time functional readings of multiple hemodynamic parameters from animals subjected to oxygenation stress. Our approach combines the functional and molecular imaging advantages of OA with the superb soft-tissue contrast of MR

further providing an excellent platform for cross-validation of functional readings by the two modalities.

关键词

Keywords

references

B. Ellenbroek , J. Youn . Rodent models in neuroscience research: is it a rat race? . Dis. Model. Mech. , 2016 . 9 1079 -1087 . DOI:10.1242/dmm.026120http://doi.org/10.1242/dmm.026120.

Q. Chen , 等 . Imaging neural activity using Thy1-GCaMP transgenic mice . Neuron , 2012 . 76 297 -308 . DOI:10.1016/j.neuron.2012.07.011http://doi.org/10.1016/j.neuron.2012.07.011.

T. M. Dawson , T. E. Golde , C. Lagier-Tourenne . Animal models of neurodegenerative diseases . Nat. Neurosci. , 2018 . 21 1370 -1379 . DOI:10.1038/s41593-018-0236-8http://doi.org/10.1038/s41593-018-0236-8.

B. Ballanger , 等 . A multi-atlas based method for automated anatomical Macaca fascicularis brain MRI segmentation and PET kinetic extraction . Neuroimage , 2013 . 77 26 -43 . DOI:10.1016/j.neuroimage.2013.03.029http://doi.org/10.1016/j.neuroimage.2013.03.029.

R. C. deCharms . Applications of real-time fMRI . Nat. Rev. Neurosci. , 2008 . 9 720 -729 . DOI:10.1038/nrn2414http://doi.org/10.1038/nrn2414.

F. Mandino , 等 . Animal functional magnetic resonance imaging: trends and path toward standardization . Front. Neuroinform. , 2020 . 13 78 DOI:10.3389/fninf.2019.00078http://doi.org/10.3389/fninf.2019.00078.

P. C. M. van Zijl , J. Hua , H. Z. Lu . The BOLD post-stimulus undershoot one of the most debated issues in fMRI . Neuroimage , 2012 . 62 1092 -1102 . DOI:10.1016/j.neuroimage.2012.01.029http://doi.org/10.1016/j.neuroimage.2012.01.029.

N. P. Blockley , 等 . A review of calibrated blood oxygenation level-dependent (BOLD) methods for the measurement of task-induced changes in brain oxygen metabolism . NMR Biomed. , 2013 . 26 987 -1003 . DOI:10.1002/nbm.2847http://doi.org/10.1002/nbm.2847.

M. Azimipour , 等 . Fluorescence laminar optical tomography for brain imaging: system implementation and performance evaluation . J. Biomed. Opt. , 2017 . 22 016003 DOI:10.1117/1.JBO.22.1.016003http://doi.org/10.1117/1.JBO.22.1.016003.

X. L. Deán-Ben , 等 . Advanced optoacoustic methods for multiscale imaging of in vivo dynamics . Chem. Soc. Rev. , 2017 . 46 2158 -2198 . DOI:10.1039/C6CS00765Ahttp://doi.org/10.1039/C6CS00765A.

E. C. Cho , 等 . Measuring the optical absorption cross sections of Au-Ag nanocages and Au nanorods by photoacoustic imaging . J. Phys. Chem. C. , 2009 . 113 9023 -9028 . DOI:10.1021/jp903343phttp://doi.org/10.1021/jp903343p.

G. Kim , 等 . Indocyanine-green-embedded PEBBLEs as a contrast agent for photoacoustic imaging . J. Biomed. Opt. , 2007 . 12 044020 DOI:10.1117/1.2771530http://doi.org/10.1117/1.2771530.

D. Razansky , 等 . Multispectral opto-acoustic tomography of deep-seated fluorescent proteins in vivo . Nat. Photonics , 2009 . 3 412 -417 . DOI:10.1038/nphoton.2009.98http://doi.org/10.1038/nphoton.2009.98.

S. Y. Nam , 等 . Combined ultrasound and photoacoustic imaging to noninvasively assess burn injury and selectively monitor a regenerative tissue-engineered construct . Tissue Eng. Part C Methods , 2015 . 21 557 -566 . DOI:10.1089/ten.tec.2014.0306http://doi.org/10.1089/ten.tec.2014.0306.

X. D. Wang , 等 . Noninvasive imaging of hemoglobin concentration and oxygenation in the rat brain using high-resolution photoacoustic tomography . J. Biomed. Opt. , 2006 . 11 024015 DOI:10.1117/1.2192804http://doi.org/10.1117/1.2192804.

X. D. Wang , 等 . Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain . Nat. Biotechnol. , 2003 . 21 803 -806 . DOI:10.1038/nbt839http://doi.org/10.1038/nbt839.

M. R. Tomaszewski , 等 . Oxygen-enhanced and dynamic contrast-enhanced optoacoustic tomography provide surrogate biomarkers of tumor vascular function hypoxia and necrosis . Cancer Res. , 2018 . 78 5980 -5991 . DOI:10.1158/0008-5472.CAN-18-1033http://doi.org/10.1158/0008-5472.CAN-18-1033.

Z. Y. Chen , 等 . Multimodal noninvasive functional neurophotonic imaging of murine brain-wide sensory responses . Adv. Sci. , 2022 . 9 2105588 DOI:10.1002/advs.202105588http://doi.org/10.1002/advs.202105588.

J. Weber , 等 . An activatable cancer-targeted hydrogen peroxide probe for photoacoustic and fluorescence imaging . Cancer Res. , 2019 . 79 5407 -5417 . DOI:10.1158/0008-5472.CAN-19-0691http://doi.org/10.1158/0008-5472.CAN-19-0691.

I. C. Sun , 等 . Photoacoustic imaging of cancer cells with glycol-chitosan-coated gold nanoparticles as contrast agents . J. Biomed. Opt. , 2019 . 24 121903 .

S. Gargiulo , S. Albanese , M. Mancini . State-of-the-art preclinical photoacoustic imaging in oncology: recent advances in cancer theranostics . Contrast Media Mol. Imaging , 2019 . 2019 5080267 .

Q. Guo , D. Wang , G. L. Yang . Photoacoustic imaging guided photothermal and chemodynamic combined therapy for cancer using "All in One" W18O49 nanorod agent . J. Biomed. Nanotechnol. , 2019 . 15 2090 -2099 . DOI:10.1166/jbn.2019.2832http://doi.org/10.1166/jbn.2019.2832.

E. Amidi , 等 . Classification of human ovarian cancer using functional spectral and imaging features obtained from in vivo photoacoustic imaging . Biomed. Opt. Express , 2019 . 10 2303 -2317 . DOI:10.1364/BOE.10.002303http://doi.org/10.1364/BOE.10.002303.

J. Rebling , 等 . Dual-wavelength hybrid optoacoustic-ultrasound biomicroscopy for functional imaging of large-scale cerebral vascular networks . J. Biophotonics , 2018 . 11 e201800057 DOI:10.1002/jbio.201800057http://doi.org/10.1002/jbio.201800057.

X. L. Deán-Ben , E. Merčep , D. Razansky . Hybrid-array-based optoacoustic and ultrasound (OPUS) imaging of biological tissues . Appl. Phys. Lett. , 2017 . 110 203703 DOI:10.1063/1.4983462http://doi.org/10.1063/1.4983462.

B. Lafci , 等 . Noninvasive multiparametric characterization of mammary tumors with transmission-reflection optoacoustic ultrasound . Neoplasia , 2020 . 22 770 -777 . DOI:10.1016/j.neo.2020.10.008http://doi.org/10.1016/j.neo.2020.10.008.

H. Estrada , 等 . High-resolution fluorescence-guided transcranial ultrasound mapping in the live mouse brain . Sci. Adv. , 2021 . 7 eabi5464 DOI:10.1126/sciadv.abi5464http://doi.org/10.1126/sciadv.abi5464.

Z. Y. Chen , 等 . Hybrid system for in vivo epifluorescence and 4D optoacoustic imaging . Opt. Lett. , 2017 . 42 4577 -4580 . DOI:10.1364/OL.42.004577http://doi.org/10.1364/OL.42.004577.

Z. Y. Chen , 等 . Concurrent fluorescence and volumetric optoacoustic tomography of nanoagent perfusion and bio-distribution in solid tumors . Biomed. Opt. Express , 2019 . 10 5093 -5102 . DOI:10.1364/BOE.10.005093http://doi.org/10.1364/BOE.10.005093.

T. Berer , 等 . Multimodal noncontact photoacoustic and optical coherence tomography imaging using wavelength-division multiplexing . J. Biomed. Opt. , 2015 . 20 046013 DOI:10.1117/1.JBO.20.4.046013http://doi.org/10.1117/1.JBO.20.4.046013.

W. Zhang , 等 . High-resolution in vivo multimodal photoacoustic microscopy optical coherence tomography and fluorescence microscopy imaging of rabbit retinal neovascularization . Light Sci. Appl. , 2018 . 7 103 DOI:10.1038/s41377-018-0093-yhttp://doi.org/10.1038/s41377-018-0093-y.

Z. Chen , 等 . Non-invasive multimodal optical coherence and photoacoustic tomography for human skin imaging . Sci. Rep. , 2017 . 7 17975 DOI:10.1038/s41598-017-18331-9http://doi.org/10.1038/s41598-017-18331-9.

W. W. Ren , 等 . Automated registration of magnetic resonance imaging and optoacoustic tomography data for experimental studies . Neurophotonics , 2019 . 6 025001 .

Y. Wang , 等 . In Vivo Photoacoustic/Single-Photon Emission Computed Tomography Imaging for Dynamic Monitoring of Aggregation-Enhanced Photothermal Nanoagents . Anal. Chem. , 2019 . 91 2128 -2134 . DOI:10.1021/acs.analchem.8b04585http://doi.org/10.1021/acs.analchem.8b04585.

W. W. Ren , 等 . Development of concurrent magnetic resonance imaging and volumetric optoacoustic tomography: a phantom feasibility study . J. Biophotonics , 2021 . 14 e202000293 .

Ozbek, A., Dean-Ben, X. L. & Razansky, D. Realtime parallel back-projection algorithm for three-dimensional optoacoustic imaging devices. In Proc. Opto-Acoustic Methods and Applications. 88000I (SPIE, 2013).

X. L. Deán-Ben , A. Özbek , D. Razansky . Accounting for speed of sound variations in volumetric hand-held optoacoustic imaging . Front. Optoelectron. , 2017 . 10 280 -286 . DOI:10.1007/s12200-017-0739-zhttp://doi.org/10.1007/s12200-017-0739-z.

SPM12. https://www.fil.ion.ucl.ac.uk/spm/software/spm12https://www.fil.ion.ucl.ac.uk/spm/software/spm12 (2022).

D. Bulte , 等 . Measurement of cerebral blood volume in humans using hyperoxic MRI contrast . J. Magn. Reson. Imaging , 2007 . 26 894 -899 . DOI:10.1002/jmri.21096http://doi.org/10.1002/jmri.21096.

R. F. Kilcoyne , 等 . Magnetic resonance imaging of soft tissue masses . Clin. Orthop. Relat. Res. , 1988 . 13 -19. .

S. Gottschalk , 等 . Noninvasive real-time visualization of multiple cerebral hemodynamic parameters in whole mouse brains using five-dimensional optoacoustic tomography . J. Cereb. Blood Flow. Metab. , 2015 . 35 531 -535 . DOI:10.1038/jcbfm.2014.249http://doi.org/10.1038/jcbfm.2014.249.

Bruker. BioSpec 70/20 and 94/20. https://www.bruker.com/en/products-and-solutions/preclinical-imaging/mri/biospec/biospec-70-20-and-94-20.htmlhttps://www.bruker.com/en/products-and-solutions/preclinical-imaging/mri/biospec/biospec-70-20-and-94-20.html (2022).

M. Uecker , 等 . Real-time MRI at a resolution of 20 ms . NMR Biomed. , 2010 . 23 986 -994 . DOI:10.1002/nbm.1585http://doi.org/10.1002/nbm.1585.

C. Hoyer , 等 . Advantages and challenges of small animal magnetic resonance imaging as a translational tool . Neuropsychobiology , 2014 . 69 187 -201 . DOI:10.1159/000360859http://doi.org/10.1159/000360859.

Rudin, M. Molecular Imaging: Basic Principles and Applications in Biomedical Research 2nd edn. (World Scientific, 2012).

G. P. Howles , 等 . High-resolution magnetic resonance angiography in the mouse using a nanoparticle blood-pool contrast agent . Magn. Reson. Med. , 2009 . 62 1447 -1456 . DOI:10.1002/mrm.22154http://doi.org/10.1002/mrm.22154.

Ç. Özsoy , 等 . Ultrafast four-dimensional imaging of cardiac mechanical wave propagation with sparse optoacoustic sensing . Proc. Natl Acad. Sci.e USA , 2021 . 118 e2103979118 DOI:10.1073/pnas.2103979118http://doi.org/10.1073/pnas.2103979118.

W. Y. Li , 等 . Broadband model-based optoacoustic mesoscopy enables deep-tissue imaging beyond the acoustic diffraction limit . Laser Photonics Rev. , 2022 . 16 2100381 DOI:10.1002/lpor.202100381http://doi.org/10.1002/lpor.202100381.

Deán-Ben, X. L. et al. Noninvasive three-dimensional optoacoustic localization microangiography of deep tissues. Preprint at arXiv https://arxiv.org/abs/2007.00372https://arxiv.org/abs/2007.00372 (2020).

E. Merčep , X. L. Deán-Ben , D. Razansky . Combined pulse-echo ultrasound and multispectral optoacoustic tomography with a multi-segment detector array . IEEE Trans. Med. Imaging , 2017 . 36 2129 -2137 . DOI:10.1109/TMI.2017.2706200http://doi.org/10.1109/TMI.2017.2706200.

J. Robin , 等 . Hemodynamic response to sensory stimulation in mice: comparison between functional ultrasound and optoacoustic imaging . NeuroImage , 2021 . 237 118111 DOI:10.1016/j.neuroimage.2021.118111http://doi.org/10.1016/j.neuroimage.2021.118111.

F. Schmitt . Echo-planar imaging . Brain Mapp. , 2015 . 1 53 -74. .

R. Hochuli , 等 . Estimating blood oxygenation from photoacoustic images: can a simple linear spectroscopic inversion ever work? . J. Biomed. Opt. , 2019 . 24 121914 .

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