Multiplexed imaging in oncology.
Journal
Nature biomedical engineering
ISSN: 2157-846X
Titre abrégé: Nat Biomed Eng
Pays: England
ID NLM: 101696896
Informations de publication
Date de publication:
05 2022
05 2022
Historique:
received:
30
01
2019
accepted:
06
09
2021
entrez:
27
5
2022
pubmed:
28
5
2022
medline:
1
6
2022
Statut:
ppublish
Résumé
In oncology, technologies for clinical molecular imaging are used to diagnose patients, establish the efficacy of treatments and monitor the recurrence of disease. Multiplexed methods increase the number of disease-specific biomarkers that can be detected simultaneously, such as the overexpression of oncogenic proteins, aberrant metabolite uptake and anomalous blood perfusion. The quantitative localization of each biomarker could considerably increase the specificity and the accuracy of technologies for clinical molecular imaging to facilitate granular diagnoses, patient stratification and earlier assessments of the responses to administered therapeutics. In this Review, we discuss established techniques for multiplexed imaging and the most promising emerging multiplexing technologies applied to the imaging of isolated tissues and cells and to non-invasive whole-body imaging. We also highlight advances in radiology that have been made possible by multiplexed imaging.
Identifiants
pubmed: 35624151
doi: 10.1038/s41551-022-00891-5
pii: 10.1038/s41551-022-00891-5
doi:
Substances chimiques
Biomarkers
0
Types de publication
Journal Article
Review
Research Support, Non-U.S. Gov't
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
527-540Subventions
Organisme : NCI NIH HHS
ID : R33 CA202064
Pays : United States
Organisme : NCI NIH HHS
ID : UH2 CA202637
Pays : United States
Organisme : NIBIB NIH HHS
ID : R01 EB017748
Pays : United States
Organisme : NCI NIH HHS
ID : R01 CA222836
Pays : United States
Informations de copyright
© 2022. Springer Nature Limited.
Références
Heinzmann, K., Carter, L. M., Lewis, J. S. & Aboagye, E. O. Multiplexed imaging for diagnosis and therapy. Nat. Biomed. Eng. 1, 697–713 (2017).
pubmed: 31015673
doi: 10.1038/s41551-017-0131-8
Gerlinger, M. et al. Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N. Engl. J. Med. 366, 883–892 (2012).
pubmed: 22397650
pmcid: 4878653
doi: 10.1056/NEJMoa1113205
Janku, F. Tumor heterogeneity in the clinic: is it a real problem? Ther. Adv. Med. Oncol. 6, 43–51 (2014).
pubmed: 24587830
pmcid: 3932055
doi: 10.1177/1758834013517414
Giedt, R. J. et al. Single-cell barcode analysis provides a rapid readout of cellular signaling pathways in clinical specimens. Nat. Commun. 9, 4550 (2018).
pubmed: 30382095
pmcid: 6208406
doi: 10.1038/s41467-018-07002-6
Haun, J. B. et al. Micro-NMR for rapid molecular analysis of human tumor samples. Sci. Transl. Med. 3, 71ra16 (2011).
pubmed: 21346169
pmcid: 3086073
doi: 10.1126/scitranslmed.3002048
Nathan, E. Frenk et al. High-content biopsies facilitate molecular analyses and do not increase complication rates in patients with advanced solid tumors. JCO Precis. Oncol. 1, 1–9 (2017).
Kodack, D. P. et al. Primary patient-derived cancer cells and their potential for personalized cancer patient care. Cell Rep. 21, 3298–3309 (2017).
pubmed: 29241554
pmcid: 5745232
doi: 10.1016/j.celrep.2017.11.051
Whitley, M. J. et al. A mouse-human phase 1 co-clinical trial of a protease-activated fluorescent probe for imaging cancer. Sci. Transl. Med. 8, 320ra324 (2016).
doi: 10.1126/scitranslmed.aad0293
Liao, L. J., Lo, W. C., Hsu, W. L., Cheng, P. W. & Wang, C. P. Assessment of pain score and specimen adequacy for ultrasound-guided fine-needle aspiration biopsy of thyroid nodules. J. Pain. Res 11, 61–66 (2018).
pubmed: 29343981
doi: 10.2147/JPR.S148088
Umkehrer, C. et al. Isolating live cell clones from barcoded populations using CRISPRa-inducible reporters. Nat. Biotechnol. https://doi.org/10.1038/s41587-020-0614-0 (2020).
Ullal, A. V. et al. Cancer cell profiling by barcoding allows multiplexed protein analysis in fine-needle aspirates. Sci. Transl. Med. 6, 219ra219 (2014).
doi: 10.1126/scitranslmed.3007361
Chen, K. H., Boettiger, A. N., Moffitt, J. R., Wang, S. & Zhuang, X. RNA imaging. Spatially resolved, highly multiplexed RNA profiling in single cells. Science 348, aaa6090 (2015).
pubmed: 25858977
pmcid: 4662681
doi: 10.1126/science.aaa6090
Moffitt, J. R. et al. High-performance multiplexed fluorescence in situ hybridization in culture and tissue with matrix imprinting and clearing. Proc. Natl Acad. Sci. USA 113, 14456–14461 (2016).
pubmed: 27911841
pmcid: 5167177
doi: 10.1073/pnas.1617699113
Wang, G., Moffitt, J. R. & Zhuang, X. Multiplexed imaging of high-density libraries of RNAs with MERFISH and expansion microscopy. Sci. Rep. 8, 4847 (2018).
pubmed: 29555914
pmcid: 5859009
doi: 10.1038/s41598-018-22297-7
Wu, X., Mao, S., Ying, Y., Krueger, C. J. & Chen, A. K. Progress and challenges for live-cell imaging of genomic loci using CRISPR-based platforms. Genomics Proteom. Bioinform. https://doi.org/10.1016/j.gpb.2018.10.001 (2019).
Im, H. et al. Digital diffraction analysis enables low-cost molecular diagnostics on a smartphone. Proc. Natl Acad. Sci. USA 112, 5613–5618 (2015).
pubmed: 25870273
pmcid: 4426451
doi: 10.1073/pnas.1501815112
Pathania, D. et al. Holographic assessment of lymphoma tissue (HALT) for global oncology field applications. Theranostics 6, 1603–1610 (2016).
pubmed: 27446494
pmcid: 4955059
doi: 10.7150/thno.15534
Im, H. et al. Design and clinical validation of a point-of-care device for the diagnosis of lymphoma via contrast-enhanced microholography and machine learning. Nat. Biomed. Eng. 2, 666–674 (2018).
pubmed: 30555750
pmcid: 6291220
doi: 10.1038/s41551-018-0265-3
Min, J. et al. Computational optics enables breast cancer profiling in point-of-care settings. ACS Nano 12, 9081–9090 (2018).
pubmed: 30113824
pmcid: 6519708
doi: 10.1021/acsnano.8b03029
Fereidouni, F. et al. Microscopy with ultraviolet surface excitation for rapid slide-free histology. Nat. Biomed. Eng. 1, 957–966 (2017).
pubmed: 31015706
pmcid: 6223324
doi: 10.1038/s41551-017-0165-y
Orringer, D. A. et al. Rapid intraoperative histology of unprocessed surgical specimens via fibre-laser-based stimulated Raman scattering microscopy. Nat. Biomed. Eng. https://doi.org/10.1038/s41551-016-0027 (2017).
Glaser, A. K. et al. Light-sheet microscopy for slide-free non-destructive pathology of large clinical specimens. Nat. Biomed. Eng. https://doi.org/10.1038/s41551-017-0084 (2017).
Lin, J. R. et al. Highly multiplexed immunofluorescence imaging of human tissues and tumors using t-CyCIF and conventional optical microscopes. eLife https://doi.org/10.7554/eLife.31657 (2018).
Gerdes, M. J. et al. Highly multiplexed single-cell analysis of formalin-fixed, paraffin-embedded cancer tissue. Proc. Natl Acad. Sci. USA 110, 11982–11987 (2013).
pubmed: 23818604
pmcid: 3718135
doi: 10.1073/pnas.1300136110
Yang, B. et al. Single-cell phenotyping within transparent intact tissue through whole-body clearing. Cell 158, 945–958 (2014).
pubmed: 25088144
pmcid: 4153367
doi: 10.1016/j.cell.2014.07.017
Tanaka, N. et al. Three-dimensional single-cell imaging for the analysis of RNA and protein expression in intact tumour biopsies. Nat. Biomed. Eng. https://doi.org/10.1038/s41551-020-0576-z (2020).
Richardson, D. S. & Lichtman, J. W. Clarifying tissue clearing. Cell 162, 246–257 (2015).
pubmed: 26186186
pmcid: 4537058
doi: 10.1016/j.cell.2015.06.067
Liebmann, T. et al. Three-dimensional study of Alzheimer’s disease hallmarks using the iDISCO clearing method. Cell Rep. 16, 1138–1152 (2016).
pubmed: 27425620
pmcid: 5040352
doi: 10.1016/j.celrep.2016.06.060
Cuccarese, M. F. et al. Heterogeneity of macrophage infiltration and therapeutic response in lung carcinoma revealed by 3D organ imaging. Nat. Commun. 8, 14293 (2017).
pubmed: 28176769
pmcid: 5309815
doi: 10.1038/ncomms14293
Spraggins, J. M. et al. Next-generation technologies for spatial proteomics: integrating ultra-high speed MALDI-TOF and high mass resolution MALDI FTICR imaging mass spectrometry for protein analysis. Proteomics 16, 1678–1689 (2016).
pubmed: 27060368
pmcid: 5117945
doi: 10.1002/pmic.201600003
Castellino, S., Groseclose, M. R. & Wagner, D. MALDI imaging mass spectrometry: bridging biology and chemistry in drug development. Bioanalysis 3, 2427–2441 (2011).
pubmed: 22074284
doi: 10.4155/bio.11.232
Giesen, C. et al. Highly multiplexed imaging of tumor tissues with subcellular resolution by mass cytometry. Nat. Methods 11, 417–422 (2014).
pubmed: 24584193
doi: 10.1038/nmeth.2869
Angelo, M. et al. Multiplexed ion beam imaging of human breast tumors. Nat. Med. 20, 436–442 (2014).
pubmed: 24584119
pmcid: 4110905
doi: 10.1038/nm.3488
Shen, C. et al. 2D and 3D CT radiomics features prognostic performance comparison in non-small cell lung cancer. Transl. Oncol. 10, 886–894 (2017).
pubmed: 28930698
pmcid: 5605492
doi: 10.1016/j.tranon.2017.08.007
Echegaray, S. et al. A rapid segmentation-insensitive “digital biopsy” method for radiomic feature extraction: method and pilot study using CT images of non-small cell lung cancer. Tomography 2, 283–294 (2016).
pubmed: 28612050
pmcid: 5466872
doi: 10.18383/j.tom.2016.00163
Coursey, C. A. et al. Dual-energy multidetector CT: how does it work, what can it tell us, and when can we use it in abdominopelvic imaging? Radiographics 30, 1037–1055 (2010).
pubmed: 20631367
doi: 10.1148/rg.304095175
McCollough, C. H., Leng, S., Yu, L. & Fletcher, J. G. Dual- and multi-energy CT: principles, technical approaches, and clinical applications. Radiology 276, 637–653 (2015).
pubmed: 26302388
doi: 10.1148/radiol.2015142631
Yeh, B. M. et al. Opportunities for new CT contrast agents to maximize the diagnostic potential of emerging spectral CT technologies. Adv. Drug Deliv. Rev. 113, 201–222 (2017).
pubmed: 27620496
doi: 10.1016/j.addr.2016.09.001
Beels, L. et al. Dose-length product of scanners correlates with DNA damage in patients undergoing contrast CT. Eur. J. Radiol. 81, 1495–1499 (2012).
pubmed: 21596504
doi: 10.1016/j.ejrad.2011.04.063
Pathe, C. et al. The presence of iodinated contrast agents amplifies DNA radiation damage in computed tomography. Contrast Media Mol. Imaging 6, 507–513 (2011).
pubmed: 22144029
doi: 10.1002/cmmi.453
Piechowiak, E. I., Peter, J. F., Kleb, B., Klose, K. J. & Heverhagen, J. T. Intravenous iodinated contrast agents amplify DNA radiation damage at CT. Radiology 275, 692–697 (2015).
pubmed: 25654667
doi: 10.1148/radiol.14132478
Rothkamm, K., Balroop, S., Shekhdar, J., Fernie, P. & Goh, V. Leukocyte DNA damage after multi-detector row CT: a quantitative biomarker of low-level radiation exposure. Radiology 242, 244–251 (2007).
pubmed: 17185671
doi: 10.1148/radiol.2421060171
Momose, A., Takeda, T., Itai, Y. & Hirano, K. Phase-contrast X-ray computed tomography for observing biological soft tissues. Nat. Med. 2, 473–475 (1996).
pubmed: 8597962
doi: 10.1038/nm0496-473
Baran, P. et al. Optimization of propagation-based X-ray phase-contrast tomography for breast cancer imaging. Phys. Med. Biol. 62, 2315–2332 (2017).
pubmed: 28140377
doi: 10.1088/1361-6560/aa5d3d
Symons, R. et al. Photon-counting CT for simultaneous imaging of multiple contrast agents in the abdomen: an in vivo study. Med. Phys. 44, 5120–5127 (2017).
pubmed: 28444761
doi: 10.1002/mp.12301
Trueb, P., Zambon, P. & Broennimann, C. Assessment of the spectral performance of hybrid photon counting X-ray detectors. Med. Phys. 44, e207–e214 (2017).
pubmed: 28901620
doi: 10.1002/mp.12323
Taguchi, K. & Iwanczyk, J. S. Vision 20/20: single photon counting x-ray detectors in medical imaging. Med. Phys. 40, 100901 (2013).
pubmed: 24089889
pmcid: 3786515
doi: 10.1118/1.4820371
Carter, L. M., Poty, S., Sharma, S. K. & Lewis, J. S. Preclinical optimization of antibody-based radiopharmaceuticals for cancer imaging and radionuclide therapy—model, vector, and radionuclide selection. J. Labelled Comp. Radiopharm. https://doi.org/10.1002/jlcr.3612 (2018).
Cornelis, F. H. et al. Long-half-life (89)Zr-labeled radiotracers can guide percutaneous biopsy within the PET/CT suite without reinjection of radiotracer. J. Nucl. Med. 59, 399–402 (2018).
pubmed: 28818992
pmcid: 5868497
doi: 10.2967/jnumed.117.194480
Phillips, E. et al. Clinical translation of an ultrasmall inorganic optical-PET imaging nanoparticle probe. Sci. Transl. Med. 6, 260ra149 (2014).
pubmed: 25355699
pmcid: 4426391
doi: 10.1126/scitranslmed.3009524
Black, N. F., McJames, S. & Kadrmas, D. J. Rapid multi-tracer PET tumor imaging with F-FDG and secondary shorter-lived tracers. IEEE Trans. Nucl. Sci. 56, 2750–2758 (2009).
pubmed: 20046800
pmcid: 2799294
doi: 10.1109/TNS.2009.2026417
Kadrmas, D. J., Rust, T. C. & Hoffman, J. M. Single-scan dual-tracer FLT+FDG PET tumor characterization. Phys. Med. Biol. 58, 429–449 (2013).
pubmed: 23296314
pmcid: 3553659
doi: 10.1088/0031-9155/58/3/429
Weissleder, R., Schwaiger, M. C., Gambhir, S. S. & Hricak, H. Imaging approaches to optimize molecular therapies. Sci. Transl. Med. 8, 355ps316 (2016).
doi: 10.1126/scitranslmed.aaf3936
Black, K. C. et al. Dual-radiolabeled nanoparticle SPECT probes for bioimaging. Nanoscale 7, 440–444 (2015).
pubmed: 25418982
pmcid: 4268305
doi: 10.1039/C4NR05269B
Sharir, T. & Slomka, P. Dual-isotope myocardial perfusion SPECT imaging: past, present, and future. J. Nucl. Cardiol. https://doi.org/10.1007/s12350-017-0966-0 (2017).
doi: 10.1007/s12350-017-0966-0
pubmed: 28975548
Berg, E., Roncali, E., Kapusta, M., Du, J. & Cherry, S. R. A combined time-of-flight and depth-of-interaction detector for total-body positron emission tomography. Med. Phys. 43, 939–950 (2016).
pubmed: 26843254
pmcid: 4733082
doi: 10.1118/1.4940355
Zhang, X., Zhou, J., Cherry, S. R., Badawi, R. D. & Qi, J. Quantitative image reconstruction for total-body PET imaging using the 2-meter long EXPLORER scanner. Phys. Med. Biol. 62, 2465–2485 (2017).
pubmed: 28240215
pmcid: 5524562
doi: 10.1088/1361-6560/aa5e46
Cherry, S. R. et al. Total-body PET: maximizing sensitivity to create new opportunities for clinical research and patient care. J. Nucl. Med. 59, 3–12 (2018).
pubmed: 28935835
pmcid: 5750522
doi: 10.2967/jnumed.116.184028
Wibmer, A. G., Hricak, H., Ulaner, G. A. & Weber, W. Trends in oncologic hybrid imaging. Eur. J. Hybrid. Imaging 2, 1 (2018).
pubmed: 29782605
doi: 10.1186/s41824-017-0019-6
Sanguedolce, F. et al. Baseline multiparametric MRI for selection of prostate cancer patients suitable for active surveillance: which features matter? Clin. Genitourin. Cancer https://doi.org/10.1016/j.clgc.2017.10.020 (2017).
Kesch, C. et al. Multiparametric MRI fusion-guided biopsy for the diagnosis of prostate cancer. Curr. Opin. Urol. https://doi.org/10.1097/mou.0000000000000461 (2017).
Brembilla, G. et al. Preoperative multiparametric MRI of the prostate for the prediction of lymph node metastases in prostate cancer patients treated with extended pelvic lymph node dissection. Eur. Radiol. https://doi.org/10.1007/s00330-017-5229-6 (2017).
Ma, D. et al. Magnetic resonance fingerprinting. Nature 495, 187–192 (2013).
pubmed: 23486058
pmcid: 3602925
doi: 10.1038/nature11971
European Society of, R. Magnetic resonance fingerprinting - a promising new approach to obtain standardized imaging biomarkers from MRI. Insights Imaging 6, 163–165 (2015).
doi: 10.1007/s13244-015-0403-3
Harisinghani, M. G. et al. Noninvasive detection of clinically occult lymph-node metastases in prostate cancer. N. Engl. J. Med. 348, 2491–2499 (2003).
pubmed: 12815134
doi: 10.1056/NEJMoa022749
Kircher, M. F. et al. In vivo high resolution three-dimensional imaging of antigen-specific cytotoxic T-lymphocyte trafficking to tumors. Cancer Res. 63, 6838–6846 (2003).
pubmed: 14583481
Miller, M. A., Arlauckas, S. & Weissleder, R. Prediction of anti-cancer nanotherapy efficacy by imaging. Nanotheranostics 1, 296–312 (2017).
pubmed: 29071194
pmcid: 5646731
doi: 10.7150/ntno.20564
Weissleder, R., Saini, S., Stark, D. D., Wittenberg, J. & Ferrucci, J. T. Dual-contrast MR imaging of liver cancer in rats. AJR Am. J. Roentgenol. 150, 561–566 (1988).
pubmed: 3257610
doi: 10.2214/ajr.150.3.561
Anderson, C. E. et al. Dual contrast - magnetic resonance fingerprinting (DC-MRF): a platform for simultaneous quantification of multiple MRI contrast agents. Sci. Rep. 7, 8431 (2017).
pubmed: 28814732
pmcid: 5559598
doi: 10.1038/s41598-017-08762-9
Hurd, R. E., Yen, Y. F., Chen, A. & Ardenkjaer-Larsen, J. H. Hyperpolarized 13C metabolic imaging using dissolution dynamic nuclear polarization. J. Magn. Reson. Imaging 36, 1314–1328 (2012).
pubmed: 23165733
doi: 10.1002/jmri.23753
Nelson, S. J. et al. Metabolic imaging of patients with prostate cancer using hyperpolarized [1-(1)(3)C]pyruvate. Sci. Transl. Med. 5, 198ra108 (2013).
Miloushev, V. Z. et al. Metabolic Imaging of the Human Brain with Hyperpolarized 13C Pyruvate Demonstrates 13C Lactate Production in Brain Tumor Patients. Cancer Res. https://doi.org/10.1158/0008-5472.can-18-0221 (2018).
Wilson, D. M. et al. Multi-compound polarization by DNP allows simultaneous assessment of multiple enzymatic activities in vivo. J. Magn. Reson. 205, 141–147 (2010).
pubmed: 20478721
pmcid: 2885774
doi: 10.1016/j.jmr.2010.04.012
Klippel, S., Freund, C. & Schroder, L. Multichannel MRI labeling of mammalian cells by switchable nanocarriers for hyperpolarized xenon. Nano Lett. 14, 5721–5726 (2014).
pubmed: 25247378
doi: 10.1021/nl502498w
Koch, M. & Ntziachristos, V. Advancing surgical vision with fluorescence imaging. Annu. Rev. Med. 67, 153–164 (2016).
pubmed: 26768238
doi: 10.1146/annurev-med-051914-022043
Yun, S. H. & Kwok, S. J. J. Light in diagnosis, therapy and surgery. Nat. Biomed. Eng. https://doi.org/10.1038/s41551-016-0008 (2017).
Kobayashi, H. et al. Simultaneous multicolor imaging of five different lymphatic basins using quantum dots. Nano Lett. 7, 1711–1716 (2007).
pubmed: 17530812
doi: 10.1021/nl0707003
Erogbogbo, F. et al. In vivo targeted cancer imaging, sentinel lymph node mapping and multi-channel imaging with biocompatible silicon nanocrystals. ACS Nano 5, 413–423 (2011).
pubmed: 21138323
doi: 10.1021/nn1018945
Behrooz, A. et al. Multispectral open-air intraoperative fluorescence imaging. Opt. Lett. 42, 2964–2967 (2017).
pubmed: 28957220
doi: 10.1364/OL.42.002964
Keating, J. et al. Identification of breast cancer margins using intraoperative near-infrared imaging. J. Surg. Oncol. 113, 508–514 (2016).
pubmed: 26843131
doi: 10.1002/jso.24167
Keating, J. J. et al. Intraoperative molecular imaging of lung adenocarcinoma can identify residual tumor cells at the surgical margins. Mol. Imaging Biol. 18, 209–218 (2016).
pubmed: 26228697
pmcid: 5474117
doi: 10.1007/s11307-015-0878-9
Zeng, C. et al. Intraoperative identification of liver cancer microfoci using a targeted near-infrared fluorescent probe for imaging-guided surgery. Sci. Rep. 6, 21959 (2016).
pubmed: 26923919
pmcid: 4770417
doi: 10.1038/srep21959
van den Berg, N. S., Buckle, T., KleinJan, G. H., van der Poel, H. G. & van Leeuwen, F. W. B. Multispectral fluorescence imaging during robot-assisted laparoscopic sentinel node biopsy: a first step towards a fluorescence-based anatomic roadmap. Eur. Urol. 72, 110–117 (2017).
pubmed: 27345689
doi: 10.1016/j.eururo.2016.06.012
Miampamba, M. et al. Sensitive in vivo visualization of breast cancer using ratiometric protease-activatable fluorescent imaging agent, AVB-620. Theranostics 7, 3369–3386 (2017).
pubmed: 28900516
pmcid: 5595138
doi: 10.7150/thno.20678
Lamberts, L. E. et al. Tumor-specific uptake of fluorescent Bevacizumab-IRDye800CW microdosing in patients with primary breast cancer: a phase I feasibility study. Clin. Cancer Res. 23, 2730–2741 (2017).
pubmed: 28119364
doi: 10.1158/1078-0432.CCR-16-0437
Carney, B., Kossatz, S. & Reiner, T. Molecular imaging of PARP. J. Nucl. Med. 58, 1025–1030 (2017).
pubmed: 28473593
pmcid: 5493005
doi: 10.2967/jnumed.117.189936
van Dam, G. M. et al. Intraoperative tumor-specific fluorescence imaging in ovarian cancer by folate receptor-alpha targeting: first in-human results. Nat. Med. 17, 1315–1319 (2011).
pubmed: 21926976
doi: 10.1038/nm.2472
Stummer, W. et al. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol. 7, 392–401 (2006).
pubmed: 16648043
doi: 10.1016/S1470-2045(06)70665-9
Georges, J. F. et al. Delta-aminolevulinic acid-mediated photodiagnoses in surgical oncology: a historical review of clinical trials. Front. Surg. 6, 45 (2019).
pubmed: 31555659
pmcid: 6737001
doi: 10.3389/fsurg.2019.00045
Haider, S. A., Lim, S., Kalkanis, S. N. & Lee, I. Y. The impact of 5-aminolevulinic acid on extent of resection in newly diagnosed high grade gliomas: a systematic review and single institutional experience. J. Neurooncol. 141, 507–515 (2019).
pubmed: 30506501
doi: 10.1007/s11060-018-03061-3
Lanahan, C. R. et al. Real-time, intraoperative detection of residual breast cancer in lumpectomy cavity margins using the LUM imaging system: results of a feasibility study. Cancer Res. 78 (4 Suppl.), abstr. P2-12-05 (2018).
Mohan, J. F. et al. Imaging the emergence and natural progression of spontaneous autoimmune diabetes. Proc. Natl Acad. Sci. USA 114, E7776–E7785 (2017).
pubmed: 28839093
pmcid: 5604023
doi: 10.1073/pnas.1707381114
Wang, Y. W., Reder, N. P., Kang, S., Glaser, A. K. & Liu, J. T. C. Multiplexed optical imaging of tumor-directed nanoparticles: a review of imaging systems and approaches. Nanotheranostics 1, 369–388 (2017).
pubmed: 29071200
pmcid: 5647764
doi: 10.7150/ntno.21136
Ntziachristos, V. & Razansky, D. Molecular imaging by means of multispectral optoacoustic tomography (MSOT). Chem. Rev. 110, 2783–2794 (2010).
pubmed: 20387910
doi: 10.1021/cr9002566
Ntziachristos, V. Going deeper than microscopy: the optical imaging frontier in biology. Nat. Methods 7, 603–614 (2010).
pubmed: 20676081
doi: 10.1038/nmeth.1483
Stoffels, I. et al. Metastatic status of sentinel lymph nodes in melanoma determined noninvasively with multispectral optoacoustic imaging. Sci. Transl. Med. 7, 317ra199 (2015).
pubmed: 26659573
doi: 10.1126/scitranslmed.aad1278
Neuschmelting, V., Lockau, H., Ntziachristos, V., Grimm, J. & Kircher, M. F. Lymph node micrometastases and in-transit metastases from melanoma: in vivo detection with multispectral optoacoustic imaging in a mouse model. Radiology 280, 137–150 (2016).
pubmed: 27144537
doi: 10.1148/radiol.2016160191
Schwarz, M., Buehler, A., Aguirre, J. & Ntziachristos, V. Three-dimensional multispectral optoacoustic mesoscopy reveals melanin and blood oxygenation in human skin in vivo. J. Biophoton. 9, 55–60 (2016).
doi: 10.1002/jbio.201500247
Neuschmelting, V. et al. WST11 vascular targeted photodynamic therapy effect monitoring by multispectral optoacoustic tomography (MSOT) in mice. Theranostics 8, 723–734 (2018).
pubmed: 29344301
pmcid: 5771088
doi: 10.7150/thno.20386
Johnson, S. P., Ogunlade, O., Lythgoe, M. F., Beard, P. & Pedley, R. B. Longitudinal photoacoustic imaging of the pharmacodynamic effect of vascular targeted therapy on tumors. Clin. Cancer Res. 25, 7436–7447 (2019).
pubmed: 31551349
pmcid: 7611302
doi: 10.1158/1078-0432.CCR-19-0360
Reshetnyak, Y. K. Imaging tumor acidity: pH-low insertion peptide probe for optoacoustic tomography. Clin. Cancer Res. 21, 4502–4504 (2015).
pubmed: 26224874
pmcid: 4609264
doi: 10.1158/1078-0432.CCR-15-1502
Xie, B. et al. Optoacoustic detection of early therapy-induced tumor cell death using a targeted imaging agent. Clin. Cancer Res. 23, 6893–6903 (2017).
pubmed: 28821560
doi: 10.1158/1078-0432.CCR-17-1029
Yin, W. et al. Tumor specific liposomes improve detection of pancreatic adenocarcinoma in vivo using optoacoustic tomography. J. Nanobiotechnol. 13, 90 (2015).
doi: 10.1186/s12951-015-0139-8
Banala, S. et al. Quinone-fused porphyrins as contrast agents for photoacoustic imaging. Chem. Sci. 8, 6176–6181 (2017).
pubmed: 28989649
pmcid: 5628350
doi: 10.1039/C7SC01369H
Roberts, S. A. et al. Sonophore-enhanced nanoemulsions for optoacoustic imaging of cancer. Chem. Sci. https://doi.org/10.1039/C8SC01706A (2018).
Aguirre, J. et al. Precision assessment of label-free psoriasis biomarkers with ultra-broadband optoacoustic mesoscopy. Nat. Biomed. Eng. https://doi.org/10.1038/s41551-017-0068 (2017).
Cheng, J. X. & Xie, X. S. Vibrational spectroscopic imaging of living systems: an emerging platform for biology and medicine. Science 350, aaa8870 (2015).
pubmed: 26612955
doi: 10.1126/science.aaa8870
Fu, D., Yang, W. & Xie, X. S. Label-free imaging of neurotransmitter acetylcholine at neuromuscular junctions with stimulated raman scattering. J. Am. Chem. Soc. 139, 583–586 (2017).
pubmed: 28027644
doi: 10.1021/jacs.6b10727
Lu, F. K. et al. Label-free DNA imaging in vivo with stimulated Raman scattering microscopy. Proc. Natl Acad. Sci. USA 112, 11624–11629 (2015).
pubmed: 26324899
pmcid: 4577158
doi: 10.1073/pnas.1515121112
Zhang, R. R. & Kuo, J. S. Detection of human brain tumor infiltration with quantitative stimulated Raman scattering microscopy. Neurosurgery 78, N9–N11 (2016).
pubmed: 26986648
doi: 10.1227/01.neu.0000481982.43612.7b
Freudiger, C. W. et al. Label-free biomedical imaging with high sensitivity by stimulated Raman scattering microscopy. Science 322, 1857–1861 (2008).
pubmed: 19095943
pmcid: 3576036
doi: 10.1126/science.1165758
Evans, C. L. et al. Chemically-selective imaging of brain structures with CARS microscopy. Opt. Express 15, 12076–12087 (2007).
pubmed: 19547572
doi: 10.1364/OE.15.012076
Andreou, C., Kishore, S. A. & Kircher, M. F. Surface-enhanced Raman spectroscopy: a new modality for cancer imaging. J. Nucl. Med. 56, 1295–1299 (2015).
pubmed: 26182971
doi: 10.2967/jnumed.115.158196
Xia, Q., Chen, Z., Zhou, Y. & Liu, R. Near-infrared organic fluorescent nanoparticles for long-term monitoring and photodynamic therapy of cancer. Nanotheranostics 3, 156–165 (2019).
pubmed: 31008024
pmcid: 6470342
doi: 10.7150/ntno.33536
Reichel, D., Tripathi, M., Butte, P., Saouaf, R. & Perez, J. M. Tumor-activatable clinical nanoprobe for cancer imaging. Nanotheranostics 3, 196–211 (2019).
pubmed: 31183314
pmcid: 6536784
doi: 10.7150/ntno.34921
Wei, L. et al. Fabrication of positively charged fluorescent polymer nanoparticles for cell imaging and gene delivery. Nanotheranostics 2, 157–167 (2018).
pubmed: 29577019
pmcid: 5865269
doi: 10.7150/ntno.22988
Li, J. et al. Two-color-based nanoflares for multiplexed micrornas imaging in live cells. Nanotheranostics 2, 96–105 (2018).
pubmed: 29291166
pmcid: 5743841
doi: 10.7150/ntno.22960
Choi, D. et al. Iodinated echogenic glycol chitosan nanoparticles for X-ray CT/US dual imaging of tumor. Nanotheranostics 2, 117–127 (2018).
pubmed: 29577016
pmcid: 5865266
doi: 10.7150/ntno.18643
Pallaoro, A., Braun, G. B. & Moskovits, M. Biotags based on surface-enhanced Raman can be as bright as fluorescence tags. Nano Lett. 15, 6745–6750 (2015).
pubmed: 26317146
doi: 10.1021/acs.nanolett.5b02594
Andreou, C. et al. Imaging of liver tumors using surface-enhanced raman scattering nanoparticles. ACS Nano 10, 5015–5026 (2016).
pubmed: 27078225
pmcid: 4884645
doi: 10.1021/acsnano.5b07200
Harmsen, S. et al. Rational design of a chalcogenopyrylium-based surface-enhanced resonance Raman scattering nanoprobe with attomolar sensitivity. Nat. Commun. 6, 6570 (2015).
pubmed: 25800697
doi: 10.1038/ncomms7570
Harmsen, S. et al. Surface-enhanced resonance Raman scattering nanostars for high-precision cancer imaging. Sci. Transl. Med. 7, 271ra277 (2015).
doi: 10.1126/scitranslmed.3010633
Nayak, T. R. et al. Tissue factor-specific ultra-bright SERRS nanostars for Raman detection of pulmonary micrometastases. Nanoscale 9, 1110–1119 (2017).
pubmed: 27991632
pmcid: 5438878
doi: 10.1039/C6NR08217C
Ye, L. et al. Comparing semiconductor nanocrystal toxicity in pregnant mice and non-human primates. Nanotheranostics 3, 54–65 (2019).
pubmed: 30662823
pmcid: 6328306
doi: 10.7150/ntno.27452
Karabeber, H. et al. Guiding brain tumor resection using surface-enhanced Raman scattering nanoparticles and a hand-held Raman scanner. ACS Nano 8, 9755–9766 (2014).
pubmed: 25093240
pmcid: 4212801
doi: 10.1021/nn503948b
Kircher, M. F. et al. A brain tumor molecular imaging strategy using a new triple-modality MRI-photoacoustic-Raman nanoparticle. Nat. Med. 18, 829–834 (2012).
pubmed: 22504484
pmcid: 3422133
doi: 10.1038/nm.2721
Zavaleta, C. L. et al. Multiplexed imaging of surface enhanced Raman scattering nanotags in living mice using noninvasive Raman spectroscopy. Proc. Natl Acad. Sci. USA 106, 13511–13516 (2009).
pubmed: 19666578
pmcid: 2726370
doi: 10.1073/pnas.0813327106
Oseledchyk, A., Andreou, C., Wall, M. A. & Kircher, M. F. Folate-targeted surface-enhanced resonance raman scattering nanoprobe ratiometry for detection of microscopic ovarian cancer. ACS Nano 11, 1488–1497 (2017).
pubmed: 27992724
pmcid: 5502101
doi: 10.1021/acsnano.6b06796
Wang, Y. W. et al. Raman-encoded molecular imaging with topically applied SERS nanoparticles for intraoperative guidance of lumpectomy. Cancer Res. 77, 4506–4516 (2017).
pubmed: 28615226
doi: 10.1158/0008-5472.CAN-17-0709
Wang, Y. W. et al. Multiplexed molecular imaging of fresh tissue surfaces enabled by convection-enhanced topical staining with SERS-coded nanoparticles. Small 12, 5612–5621 (2016).
pubmed: 27571395
doi: 10.1002/smll.201601829
Nicolson, F. et al. Non-invasive in vivo imaging of cancer using Surface-Enhanced Spatially Offset Raman Spectroscopy (SESORS). Theranostics 9, 5899–5913 (2019).
Bohndiek, S. E. et al. A small animal Raman instrument for rapid, wide-area, spectroscopic imaging. Proc. Natl Acad. Sci. USA 110, 12408–12413 (2013).
pubmed: 23821752
pmcid: 3725059
doi: 10.1073/pnas.1301379110
Thomas, G. et al. Evaluating feasibility of an automated 3-dimensional scanner using Raman spectroscopy for intraoperative breast margin assessment. Sci. Rep. 7, 13548 (2017).
pubmed: 29051521
pmcid: 5648832
doi: 10.1038/s41598-017-13237-y
Garai, E. et al. A real-time clinical endoscopic system for intraluminal, multiplexed imaging of surface-enhanced Raman scattering nanoparticles. PLoS ONE 10, e0123185 (2015).
pubmed: 25923788
pmcid: 4414592
doi: 10.1371/journal.pone.0123185
Thakor, A. S. et al. The fate and toxicity of Raman-active silica-gold nanoparticles in mice. Sci. Transl. Med. 3, 79ra33 (2011).
pubmed: 21508310
doi: 10.1126/scitranslmed.3001963
Dubey, R. D. et al. Novel hyaluronic acid conjugates for dual nuclear imaging and therapy in CD44-expressing tumors in mice in vivo. Nanotheranostics 1, 59–79 (2017).
pubmed: 29071179
pmcid: 5646725
doi: 10.7150/ntno.17896
Zhang, S., Gupta, S., Fitzgerald, T. J. & Bogdanov, A. A.Jr. Dual radiosensitization and anti-STAT3 anti-proliferative strategy based on delivery of gold nanoparticle—oligonucleotide nanoconstructs to head and neck cancer cells. Nanotheranostics 2, 1–11 (2018).
pubmed: 29291159
pmcid: 5743834
doi: 10.7150/ntno.22335
Zhang, Q. et al. Construction of multifunctional Fe3O4-MTX@HBc nanoparticles for MR imaging and photothermal therapy/chemotherapy. Nanotheranostics 2, 87–95 (2018).
pubmed: 29291165
pmcid: 5743840
doi: 10.7150/ntno.21942
Liu, R., Tang, J., Xu, Y., Zhou, Y. & Dai, Z. Nano-sized indocyanine green J-aggregate as a one-component theranostic agent. Nanotheranostics 1, 430–439 (2017).
pubmed: 29188176
pmcid: 5704008
doi: 10.7150/ntno.19935
Liu, L., Ruan, Z., Yuan, P., Li, T. & Yan, L. Oxygen self-sufficient amphiphilic polypeptide nanoparticles encapsulating BODIPY for potential near infrared imaging-guided photodynamic therapy at low energy. Nanotheranostics 2, 59–69 (2018).
pubmed: 29291163
pmcid: 5743838
doi: 10.7150/ntno.22754
Lin, S. Y., Huang, R. Y., Liao, W. C., Chuang, C. C. & Chang, C. W. Multifunctional PEGylated albumin/IR780/iron oxide nanocomplexes for cancer photothermal therapy and MR imaging. Nanotheranostics 2, 106–116 (2018).
pubmed: 29577015
pmcid: 5865265
doi: 10.7150/ntno.19379
Gupta, M. K. et al. Recent strategies to design vascular theranostic nanoparticles. Nanotheranostics 1, 166–177 (2017).
pubmed: 29071185
pmcid: 5646719
doi: 10.7150/ntno.18531
Thurber, G. M., Figueiredo, J. L. & Weissleder, R. Multicolor fluorescent intravital live microscopy (FILM) for surgical tumor resection in a mouse xenograft model. PLoS ONE 4, e8053 (2009).
pubmed: 19956597
pmcid: 2779447
doi: 10.1371/journal.pone.0008053
Herzog, E. et al. Optical imaging of cancer heterogeneity with multispectral optoacoustic tomography. Radiology 263, 461–468 (2012).
pubmed: 22517960
doi: 10.1148/radiol.11111646