In vivo imaging of glucose uptake and metabolism in tumors
Open accessAbstract
Tumors have a greater reliance on anaerobic glycolysis for energy production than normal tissues. We developed a noninvasive method for imaging glucose uptake in vivo that is based on magnetic resonance imaging and allows the uptake of unlabeled glucose to be measured through the chemical exchange of protons between hydroxyl groups and water. This method differs from existing molecular imaging methods because it permits detection of the delivery and uptake of a metabolically active compound in physiological quantities. We show that our technique, named glucose chemical exchange saturation transfer (glucoCEST), is sensitive to tumor glucose accumulation in colorectal tumor models and can distinguish tumor types with differing metabolic characteristics and pathophysiologies. The results of this study suggest that glucoCEST has potential as a useful and cost-effective method for characterizing disease and assessing response to therapy in the clinic.
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GlucoCEST signal arising from free glucose and products arising from its metabolism can be present in any of three tissue compartments: intravascular, extravascular-extracellular, and intracellular.
“However, the glucoCEST signal arising from free glucose and products arising from its metabolism can be present in any of three tissue compartments: intravascular, extravascular–extracellular, and intracellular (Chan et al., 2012, Nasrallah et al., 2013, Walker-Samuel et al., 2013).”
From In vivo imaging of tau pathology using multi-parametric quantitative MRI (2015) · cites this paper as Walker-Samuel et al., 2013
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Hanahan, D., & Weinberg, R. A. (2000) · Cell · doi:10.1016/s0092-8674(00)81683-9 · Cited by 29,219 · see citing works
Mutual-information-based registration of medical images: a survey
Pluim, J. P. W., Maintz, J. B. A., & Viergever, M. A. (2003) · IEEE Transactions on Medical Imaging · doi:10.1109/tmi.2003.815867 · Cited by 2,882 · see citing works
Guidelines for the welfare and use of animals in cancer research
Workman, P., Aboagye, E. O., Balkwill, F. R., Balmain, A., Bruder, G., Chaplin, D. J., Double, J. A., Everitt, J. I., Farningham, D. A. H., Glennie, M. J., et al. (2010) · British Journal of Cancer · doi:10.1038/sj.bjc.6605642 · Cited by 1,449 · see citing works
Using the amide proton signals of intracellular proteins and peptides to detect pH effects in MRI
Zhou, J., Payen, J., Wilson, D. A., Traystman, R. J., & van Zijl, P. C. M. (2003) · Nature Medicine · doi:10.1038/nm907 · Cited by 1,203 · see citing works
Java-based graphical user interface for the MRUI quantitation package
Naressi, A., Couturier, C., Devos, J. M., Janssen, M., Mangeat, C., de Beer, R., & Graveron‐Demilly, D. (2001) · Magnetic Resonance Materials in Physics Biology and Medicine · doi:10.1007/bf02668096 · Cited by 1,003 · see citing works
Evaluating the glucose tolerance test in mice
Andrikopoulos, S., Blair, A. R., DeLuca, N., Fam, B. C., & Proietto, J. (2008) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.90617.2008 · Cited by 824 · see citing works
Quantitative interpretation of magnetization transfer
Henkelman, R. M., Huang, X., Xiang, Q., Stanisz, G. J., Swanson, S. D., & Bronskill, M. J. (1993) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1910290607 · Cited by 734 · see citing works
Progress and Promise of FDG-PET Imaging for Cancer Patient Management and Oncologic Drug Development
Kelloff, G. J., Hoffman, J. M., Johnson, B. E., Scher, H. I., Siegel, B. A., Cheng, E. Y., Cheson, B. D., O’Shaughnessy, J., Guyton, K. Z., Mankoff, D. A., et al. (2005) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-04-2626 · Cited by 672 · see citing works
Amide proton transfer (APT) contrast for imaging of brain tumors
Zhou, J., Lal, B., Wilson, D. A., Laterra, J., & van Zijl, P. C. M. (2003) · Magnetic Resonance in Medicine · doi:10.1002/mrm.10651 · Cited by 660 · see citing works
Procedure guideline for tumor imaging with F-18 FDG PET/CT
Delbeke, D., Coleman, R. E., Guiberteau, M. J., Brown, M. L., Royal, H. D., Siegel, B. A., Townsend, D. W., Berland, L. L., Parker, J. A., Hübner, K. F., et al. (2006) · Cited by 620 · see citing works
Whole-Body Dual-Modality PET/CT and Whole-Body MRI for Tumor Staging in Oncology
Antoch, G. (2003) · JAMA · doi:10.1001/jama.290.24.3199 · Cited by 551 · see citing works
Naressi, A., Couturier, C., Castang, I., de Beer, R., & Graveron‐Demilly, D. (2001) · Computers in Biology and Medicine · doi:10.1016/s0010-4825(01)00006-3 · Cited by 461 · see citing works
31P-MRS measurements of extracellular pH of tumors using 3-aminopropylphosphonate
Gillies, R. J., Liu, Z., & Bhujwalla, Z. M. (1994) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1994.267.1.c195 · Cited by 351 · see citing works
McMahon, M. T., Gilad, A. A., Zhou, J., Sun, P. Z., Bulte, J. W. M., & van Zijl, P. C. M. (2006) · Magnetic Resonance in Medicine · doi:10.1002/mrm.20818 · Cited by 331 · see citing works
Procedure guideline for tumor imaging with 18F-FDG PET/CT 1.0.
Delbeke, D., Coleman, R. E., Guiberteau, M. J., Brown, M. L., Royal, H. D., Siegel, B. A., Townsend, D. W., Berland, L. L., Parker, J. A., Hubner, K., et al. (2006) · PubMed · Cited by 297 · see citing works
Imaging of the Dynamics of Glucose Uptake in the Cytosol of COS-7 Cells by Fluorescent Nanosensors
Fehr, M., Lalonde, S., Lager, I., Wolff, M. W., & Frommer, W. B. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m301333200 · Cited by 295 · see citing works
Zhou, J., Wilson, D. A., Sun, P. Z., Klaus, J. A., & van Zijl, P. C. M. (2004) · Magnetic Resonance in Medicine · doi:10.1002/mrm.20048 · Cited by 293 · see citing works
Quantitative Analysis in Nuclear Medicine Imaging
Zaidi, H. (2006) · Springer eBooks · doi:10.1007/b107410 · Cited by 266 · see citing works
(1969) · Radiology · doi:10.1148/23.1.186b · Cited by 220 · see citing works
Pretsch, E., Bühlmann, P., & Badertscher, M. (2009) · Springer eBooks · doi:10.1007/978-3-540-93810-1_4 · Cited by 193 · see citing works
Whole-Body MRI Versus PET in Assessment of Multiple Myeloma Disease Activity
Shortt, C. P., Gleeson, T. G., Breen, K. A., McHugh, J. C., O'Connell, M. J., O’Gorman, P., & Eustace, S. J. (2009) · American Journal of Roentgenology · doi:10.2214/ajr.08.1633 · Cited by 184 · see citing works
High-resolution 13C nuclear magnetic resonance studies of glucose metabolism in Escherichia coli.
Uǧurbil, K., Brown, T. R., den Hollander, J. A., Glynn, P., & Shulman, R. G. (1978) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.75.8.3742 · Cited by 141 · see citing works
Hariharan, R., Bray, M. S., Ganim, R., Doenst, T., Goodwin, G. W., & Taegtmeyer, H. (1995) · Circulation · doi:10.1161/01.cir.91.9.2435 · Cited by 131 · see citing works
Walker‐Samuel, S., Leach, M. O., & Collins, D. J. (2006) · Physics in Medicine and Biology · doi:10.1088/0031-9155/51/14/021 · Cited by 129 · see citing works
Self-citationStancanello, J., Terreno, E., Castelli, D. D., Cabella, C., Uggeri, F., & Aime, S. (2008) · Contrast Media & Molecular Imaging · doi:10.1002/cmmi.240 · Cited by 126 · see citing works
Belle, V., Kahler, E., Waller, C., Rommel, E., Voll, S., Hiller, K., Bauer, W. R., & Haase, A. (1998) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.1880080610 · Cited by 121 · see citing works
Ali, M., Liu, G., Shah, T. V., Flask, C. A., & Pagel, M. D. (2009) · Accounts of Chemical Research · doi:10.1021/ar8002738 · Cited by 115 · see citing works
Tumor metabolic rates in sarcoma using FDG PET.
Eary, J. F., & Mankoff, D. A. (1998) · PubMed · Cited by 101 · see citing works
Predicting Response to Radioimmunotherapy from the Tumor Microenvironment of Colorectal Carcinomas
El‐Emir, E., Qureshi, U., Dearling, J. L. J., Boxer, G. M., Clatworthy, I., Folarin, A., Robson, M. P., Nagl, S., Konerding, M. A., & Pedley, R. B. (2007) · Cancer Research · doi:10.1158/0008-5472.can-07-2967 · Cited by 67 · see citing works
Self-citationKostenüberlegungen zur Ganzkörper-MRT und PET-CT im Rahmen des onkologischen Stagings
Plathow, C., Walz, M., Lichy, M. P., Aschoff, P., Pfannenberg, C., Bock, H., Eschmann, S. M., Claussen, C. D., & Schlemmer, H.-P. (2007) · Der Radiologe · doi:10.1007/s00117-007-1547-z · Cited by 57 · see citing works
Analysis of the regional uptake of radiolabeled deoxyglucose analogs in human tumor xenografts.
Dearling, J. L. J., Flynn, A. A., Sutcliffe-Goulden, J., Petrie, I. A., Boden, R. W., Green, A. J., Boxer, G. M., Beǵent, R. H. J., & Pedley, R. B. (2004) · PubMed · Cited by 56 · see citing works
Self-citationVallabhajosula, S. (2009) · Springer eBooks · doi:10.1007/978-3-540-76735-0 · Cited by 55 · see citing works
John, S., Ottolia, M., Weiss, J. N., & Ribalet, B. (2007) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-007-0395-z · Cited by 48 · see citing works
Hor, K. N., Mazur, W. M., Taylor, M. D., Al‐Khalidi, H. R., Cripe, L. H., Jefferies, J. L., Raman, S. V., Chung, E. S., Kinnett, K., Williams, K., et al. (2011) · Journal of Cardiovascular Magnetic Resonance · doi:10.1186/1532-429x-13-60 · Cited by 48 · see citing works
Kalderon, B., Korman, S. H., Gutman, A., & Lapidot, A. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.12.4690 · Cited by 46 · see citing works
Campbell‐Washburn, A. E., Price, A. N., Wells, J. A., Thomas, D. L., Ordidge, R. J., & Lythgoe, M. F. (2012) · Magnetic Resonance in Medicine · doi:10.1002/mrm.24243 · Cited by 39 · see citing works
Self-citationWalker‐Samuel, S., Orton, M. R., Boult, J. K. R., & Robinson, S. P. (2010) · Magnetic Resonance in Medicine · doi:10.1002/mrm.22572 · Cited by 28 · see citing works
Self-citationNon‐invasive in vivo imaging of vessel calibre in orthotopic prostate tumour xenografts
Walker‐Samuel, S., Boult, J. K. R., McPhail, L. D., Box, G., Eccles, S. A., & Robinson, S. P. (2011) · International Journal of Cancer · doi:10.1002/ijc.26112 · Cited by 19 · see citing works
Self-citationTyler, D. J., & Gowland, P. A. (2004) · Magnetic Resonance in Medicine · doi:10.1002/mrm.20323 · Cited by 19 · see citing works
Gloor, M., Scheffler, K., & Bieri, O. (2010) · Magnetic Resonance in Medicine · doi:10.1002/mrm.22694 · Cited by 15 · see citing works
Burrell, J. S., Walker‐Samuel, S., Baker, L. C. J., Boult, J. K. R., Ryan, A. J., Waterton, J. C., Halliday, J., & Robinson, S. P. (2011) · Magnetic Resonance in Medicine · doi:10.1002/mrm.22779 · Cited by 10 · see citing works
Self-citationMagnetization transfer with echo planar imaging
Ranjeva, J., Franconi, J., MANELFE, C., & Berry, I. (1997) · Magnetic Resonance Materials in Physics Biology and Medicine · doi:10.1007/bf02595043 · Cited by 7 · see citing works
Walker‐Samuel, S., Johnson, S. P., Pedley, B. R., Lythgoe, M. F., & Golay, X. (2011) · NMR in Biomedicine · doi:10.1002/nbm.1798 · Cited by 6 · see citing works
Self-citationProcedure guideline for general imaging: 1.0. Society of Nuclear Medicine.
Parker, J. A., Yester, M. V., Daube-Witherspoon, E., Todd-Pokropek, A. E., & Royal, H. J. (1996) · PubMed · Cited by 6 · see citing works
Equilibrium contrast CMR for the detection of amyloidosis in mice
Campbell‐Washburn, A. E., Price, A. N., Ellmerich, S., Simons, J. P., Al‐Shawi, R., Hawkins, P. N., Ordidge, R. J., Pepys, M. B., Moon, J., & Lythgoe, M. F. (2011) · Journal of Cardiovascular Magnetic Resonance · doi:10.1186/1532-429x-13-s1-o60 · Cited by 5 · see citing works
Self-citationAlberti (1998) · doi:10.1002/(sici)1096-9136(199807)15:7
Wheeler-Kingshott (2000) · doi:10.1002/1522-2594(200011)44:5
Basser (2000) · doi:10.1002/1522-2594(200010)44:4
Flagged first, then by citations
3 of the 51 references couldn’t be matched to a known paper.
Research works printed but not linked: 4
- [1]Ward KM Balaban RS Determination of pH using water protons and chemical exchange dependent saturation transfer (CEST) Magn Reson Med 2000 44 799 802 11064415
- [11]Kunnecke B Kustermann E Seelig J Simultaneous in vivo monitoring of hepatic glucose and glucose-6-phosphate by (13)C-NMR spectroscopy Magn Reson Med 2000 44 556 562 11025511
- [30]Plathow C Cost considerations for whole-body MRI and PET/CT as part of oncologic staging Der Radiologe 2008 48 384 396 17891370
- [34]Walker-Samuel S Johnson SP Pedley B Lythgoe MF Golay X Extracranial measurements of amide proton transfer using exchange-modulated point-resolved spectroscopy (EXPRESS) NMR Biomed 2012 25 829 834 22135248
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Wahsner, J., Gale, E. M., Rodríguez‐Rodríguez, A., & Caravan, P. D. (2018) · Chemical Reviews · doi:10.1021/acs.chemrev.8b00363 · Cited by 1,615 · see citing works
Tumor metastasis: moving new biological insights into the clinic
Wan, L., Pantel, K., & Kang, Y. (2013) · Nature Medicine · doi:10.1038/nm.3391 · Cited by 746 · see citing works
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Xie, N., Tan, Z., Banerjee, S., Cui, H., Ge, J., Liu, R.-M., Bernard, K., Thannickal, V. J., & Liu, G. (2015) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/rccm.201504-0780oc · Cited by 582 · see citing works
Pros and cons of ultra-high-field MRI/MRS for human application
Ladd, M. E., Bachert, P., Meyerspeer, M., Moser, E., Nagel, A. M., Norris, D. G., Schmitter, S., Speck, O., Straub, S., & Zaiß, M. (2018) · Progress in Nuclear Magnetic Resonance Spectroscopy · doi:10.1016/j.pnmrs.2018.06.001 · Cited by 550 · see citing works
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Feyter, H. M. D., Behar, K. L., Corbin, Z. A., Fulbright, R. K., Brown, P. B., McIntyre, S., Nixon, T. W., Rothman, D. L., & de Graaf, R. A. (2018) · Science Advances · doi:10.1126/sciadv.aat7314 · Cited by 378 · see citing works
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Gao, G., Sun, X., & Liang, G. (2021) · Advanced Functional Materials · doi:10.1002/adfm.202100738 · Cited by 363 · see citing works
van Zijl, P. C. M., Lam, W. W., Xu, J., Knutsson, L., & Stanisz, G. J. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.04.045 · Cited by 343 · see citing works
Advances in neuro-oncology imaging
Langen, K., Galldiks, N., Hattingen, E., & Shah, N. J. (2017) · Nature Reviews Neurology · doi:10.1038/nrneurol.2017.44 · Cited by 339 · see citing works
Tan, Z., Xie, N., Cui, H., Moellering, D. R., Abraham, E. H., Thannickal, V. J., & Liu, G. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1402469 · Cited by 320 · see citing works
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Lerch, J. P., van der Kouwe, A. J. W., Raznahan, A., Paus, T., Johansen‐Berg, H., Miller, K. L., Smith, S. M., Fischl, B. R., & Sotiropoulos, S. N. (2017) · Nature Neuroscience · doi:10.1038/nn.4501 · Cited by 313 · see citing works
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Jones, K. M., Pollard, A. C., & Pagel, M. D. (2017) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.25838 · Cited by 288 · see citing works
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Wu, B. H., Warnock, G., Zaiß, M., Lin, C., Chen, M., Zhou, Z., Mu, L., Nanz, D., Tuura, R., & Delso, G. (2016) · EJNMMI Physics · doi:10.1186/s40658-016-0155-2 · Cited by 277 · see citing works
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Mitchell, M. J., Jain, R. K., & Langer, R. (2017) · Nature Reviews Cancer · doi:10.1038/nrc.2017.83 · Cited by 273 · see citing works
Yuan, Y., Zhang, J., Qi, X., Li, S., Liu, G., Siddhanta, S., Barman, I., Song, X., McMahon, M. T., & Bulte, J. W. M. (2019) · Nature Materials · doi:10.1038/s41563-019-0503-4 · Cited by 250 · see citing works
Zaiß, M., Windschuh, J., Paech, D., Meissner, J., Burth, S., Schmitt, B., Kickingereder, P., Wiestler, B., Wick, W., Bendszus, M., et al. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.02.040 · Cited by 220 · see citing works
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Zheng, X., Mao, H., Huo, D., Wu, W., Liu, B., & Jiang, X. (2017) · Nature Biomedical Engineering · doi:10.1038/s41551-017-0057 · Cited by 210 · see citing works
A review of responsive MRI contrast agents: 2005–2014
Hingorani, D. V., Bernstein, A. S., & Pagel, M. D. (2014) · Contrast Media & Molecular Imaging · doi:10.1002/cmmi.1629 · Cited by 199 · see citing works
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Zhang, L., Shi, L., Shen, Y., Miao, Y., Wei, M., Qian, N., Liu, Y., & Min, W. (2019) · Nature Biomedical Engineering · doi:10.1038/s41551-019-0393-4 · Cited by 197 · see citing works
Xu, X., Yadav, N. N., Knutsson, L., Hua, J., Kalyani, R. R., Hall, E., Laterra, J., Blakeley, J. O., Strowd, R. E., III, Pomper, M. G., et al. (2015) · Tomography · doi:10.18383/j.tom.2015.00175 · Cited by 184 · see citing works
Imaging brain deoxyglucose uptake and metabolism by glucoCEST MRI
Nasrallah, F. A., Pagès, G., Kuchel, P. W., Golay, X., & Chuang, K.-H. (2013) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2013.79 · Cited by 179 · see citing works
Self-citationHu, F., Chen, Z., Zhang, L., Shen, Y., Wei, L., & Min, W. (2015) · Angewandte Chemie International Edition · doi:10.1002/anie.201502543 · Cited by 161 · see citing works
The Oncogenic Action of NRF2 Depends on De-glycation by Fructosamine-3-Kinase
Sanghvi, V. R., Leibold, J., Mina, M., Mohan, P., Berishaj, M., Li, Z., Miele, M. M., Lailler, N., Zhao, C., de Stanchina, E., et al. (2019) · Cell · doi:10.1016/j.cell.2019.07.031 · Cited by 155 · see citing works
Heo, H., Zhang, Y., Lee, D., Hong, X., & Zhou, J. (2015) · Magnetic Resonance in Medicine · doi:10.1002/mrm.25581 · Cited by 154 · see citing works
Heo, H., Zhang, Y., Jiang, S., Lee, D., & Zhou, J. (2015) · Magnetic Resonance in Medicine · doi:10.1002/mrm.25795 · Cited by 153 · see citing works
Zaiß, M., Zu, Z., Xu, J., Schuenke, P., Gochberg, D. F., Gore, J. C., Ladd, M. E., & Bachert, P. (2014) · NMR in Biomedicine · doi:10.1002/nbm.3237 · Cited by 151 · see citing works
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Shen, Y., Hu, F., & Min, W. (2019) · Annual Review of Biophysics · doi:10.1146/annurev-biophys-052118-115500 · Cited by 140 · see citing works
Downfield‐NOE‐suppressed amide‐CEST‐MRI at 7 Tesla provides a unique contrast in human glioblastoma
Zaiß, M., Windschuh, J., Goerke, S., Paech, D., Meissner, J., Burth, S., Kickingereder, P., Wick, W., Bendszus, M., Schlemmer, H., et al. (2016) · Magnetic Resonance in Medicine · doi:10.1002/mrm.26100 · Cited by 132 · see citing works
Kim, J., Wu, Y., Guo, Y., Zheng, H., & Sun, P. Z. (2015) · Contrast Media & Molecular Imaging · doi:10.1002/cmmi.1628 · Cited by 129 · see citing works
Cohen, O., Huang, S., McMahon, M. T., Rosen, M. S., & Farrar, C. T. (2018) · Magnetic Resonance in Medicine · doi:10.1002/mrm.27221 · Cited by 128 · see citing works
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Kim, M. M., Parolia, A., Dunphy, M. P., & Venneti, S. (2016) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2016.108 · Cited by 119 · see citing works
Heo, H., Jones, C. K., Hua, J., Yadav, N. N., Agarwal, S., Zhou, J., van Zijl, P. C. M., & Pillai, J. J. (2015) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.25108 · Cited by 117 · see citing works
d’Esposito, A., Sweeney, P. W., Ali, M., Saleh, M., Ramasawmy, R., Roberts, T. A., Agliardi, G., Desjardins, A. E., Lythgoe, M. F., Pedley, R. B., et al. (2018) · Nature Biomedical Engineering · doi:10.1038/s41551-018-0306-y · Cited by 115 · see citing works
Self-citationXu, X., Chan, K. W. Y., Knutsson, L., Artemov, D., Xu, J., Liu, G., Katō, Y., Lal, B., Laterra, J., McMahon, M. T., et al. (2015) · Magnetic Resonance in Medicine · doi:10.1002/mrm.25995 · Cited by 114 · see citing works
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Molecular magnetic resonance imaging in cancer
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Zaiß, M., Ehses, P., & Scheffler, K. (2018) · NMR in Biomedicine · doi:10.1002/nbm.3879 · Cited by 106 · see citing works
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Huang, J., van Zijl, P. C. M., Han, X., Dong, C. M., Cheng, G. W., Tse, K., Knutsson, L., Chen, L., Lai, J. H. C., Wu, E. X., et al. (2020) · Science Advances · doi:10.1126/sciadv.aba3884 · Cited by 103 · see citing works
Zhou, I. Y., Wang, E., Cheung, J. S., Zhang, X., Fulci, G., & Sun, P. Z. (2017) · Scientific Reports · doi:10.1038/s41598-017-00167-y · Cited by 101 · see citing works
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Zhang, X., Wang, F., Afzal, A., Xu, J., Gore, J. C., Gochberg, D. F., & Zu, Z. (2016) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2016.05.002 · Cited by 98 · see citing works
Mapping Brain Glucose Uptake with Chemical Exchange-Sensitive Spin-Lock Magnetic Resonance Imaging
Jin, T., Mehrens, H. S., Hendrich, K. S., & Kim, S. (2014) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.2014.97 · Cited by 97 · see citing works
Imaging metabolic heterogeneity in cancer
Sengupta, D., & Pratx, G. (2016) · Molecular Cancer · doi:10.1186/s12943-015-0481-3 · Cited by 94 · see citing works
In vivo imaging of tau pathology using multi-parametric quantitative MRI
Wells, J. A., O'Callaghan, J. M., Holmes, H. E., Powell, N. M., Johnson, R. A., Siow, B., Torrealdea, F., Ismail, O., Walker-Samuel, S., Golay, X., et al. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.02.023 · Cited by 93 · see citing works
Self-citationT1ρ-weighted Dynamic Glucose-enhanced MR Imaging in the Human Brain
Paech, D., Schuenke, P., Koehler, C., Windschuh, J., Mundiyanapurath, S., Bickelhaupt, S., Bonekamp, D., Bäumer, P., Bachert, P., Ladd, M. E., et al. (2017) · Radiology · doi:10.1148/radiol.2017162351 · Cited by 93 · see citing works
Ye, J.-Z., Lin, X., Cheng, Z.-X., Su, Y., Li, W., Ali, F., Zheng, J., & Peng, B. (2018) · Journal of Proteomics · doi:10.1016/j.jprot.2018.05.006 · Cited by 92 · see citing works
Label-free CEST MRI Detection of Citicoline-Liposome Drug Delivery in Ischemic Stroke
Liu, H., Jabłońska, A., Li, Y., Cao, S., Liu, D., Chen, H., van Zijl, P. C. M., Bulte, J. W. M., Janowski, M., Walczak, P., et al. (2016) · Theranostics · doi:10.7150/thno.15492 · Cited by 92 · see citing works
Schuenke, P., Koehler, C., Korzowski, A., Windschuh, J., Bachert, P., Ladd, M. E., Mundiyanapurath, S., Paech, D., Bickelhaupt, S., Bonekamp, D., et al. (2016) · Magnetic Resonance in Medicine · doi:10.1002/mrm.26370 · Cited by 89 · see citing works
Chemical exchange saturation transfer MR imaging of Parkinson’s disease at 3 Tesla
Li, C., Peng, S., Wang, R., Chen, H., Su, W., Zhao, X., Zhou, J., & Chen, M. (2014) · European Radiology · doi:10.1007/s00330-014-3241-7 · Cited by 88 · see citing works
3D gradient echo snapshot CEST MRI with low power saturation for human studies at 3T
Deshmane, A., Zaiß, M., Lindig, T. M., Herz, K., Schuppert, M., Gandhi, C., Bender, B., Ernemann, U., & Scheffler, K. (2018) · Magnetic Resonance in Medicine · doi:10.1002/mrm.27569 · Cited by 88 · see citing works
Heo, H., Han, Z., Jiang, S., Schär, M., van Zijl, P. C. M., & Zhou, J. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.01.034 · Cited by 87 · see citing works
Kaggie, J. D., Khan, A. S., Matys, T., Schulte, R. F., Locke, M. J., Grimmer, A., Frary, A. J., Menih, I. H., Latimer, E., Graves, M. J., et al. (2022) · NeuroImage · doi:10.1016/j.neuroimage.2022.119284 · Cited by 86 · see citing works
Assessments of tumor metabolism with CEST MRI
Goldenberg, J. M., & Pagel, M. D. (2018) · NMR in Biomedicine · doi:10.1002/nbm.3943 · Cited by 85 · see citing works
Lee, D., Heo, H., Zhang, K., Zhang, Y., Jiang, S., Zhao, X., & Zhou, J. (2016) · Magnetic Resonance in Medicine · doi:10.1002/mrm.26131 · Cited by 85 · see citing works
Magnetic Resonance Imaging of Glucose Uptake and Metabolism in Patients with Head and Neck Cancer
Wang, J., Weygand, J., Hwang, K., Mohamed, A., Ding, Y., Fuller, C. D., Lai, S. Y., Frank, S. J., & Zhou, J. (2016) · Scientific Reports · doi:10.1038/srep30618 · Cited by 84 · see citing works
In vivo methods for imaging blood–brain barrier function and dysfunction
Harris, W. J., Asselin, M., Hinz, R., Parkes, L. M., Allan, S. M., Schießl, I., Boutin, H., & Dickie, B. (2022) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-022-05997-1 · Cited by 87 · see citing works
Comparison of divalent transition metal ion paraCEST MRI contrast agents
Dorazio, S. J., Olatunde, A. O., Tsitovich, P. B., & Morrow, J. R. (2013) · JBIC Journal of Biological Inorganic Chemistry · doi:10.1007/s00775-013-1059-4 · Cited by 82 · see citing works
Lactate Chemical Exchange Saturation Transfer (LATEST) Imaging in vivo: A Biomarker for LDH Activity
DeBrosse, C., Nanga, R. P. R., Bagga, P., Nath, K., Haris, M., Marincola, F. M., Schnall, M. D., Hariharan, H., & Reddy, R. D. (2016) · Scientific Reports · doi:10.1038/srep19517 · Cited by 82 · see citing works
Wang, M., Hong, X., Chang, C.-F., Li, Q., Ma, B., Zhang, H., Xiang, S., Heo, H., Zhang, Y., Lee, D., et al. (2015) · Magnetic Resonance in Medicine · doi:10.1002/mrm.25690 · Cited by 81 · see citing works
Towards the complex dependence of MTRasym on T1w in amide proton transfer (APT) imaging
Zu, Z. (2018) · NMR in Biomedicine · doi:10.1002/nbm.3934 · Cited by 81 · see citing works
Label-free in vivo molecular imaging of underglycosylated mucin-1 expression in tumour cells
Song, X., Airan, R. D., Arifin, D. R., Bar‐Shir, A., Kadayakkara, D. K. K., Liu, G., Gilad, A. A., van Zijl, P. C. M., McMahon, M. T., & Bulte, J. W. M. (2015) · Nature Communications · doi:10.1038/ncomms7719 · Cited by 80 · see citing works
Ray, K. J., Simard, M. A., Larkin, J. R., Coates, J. T. T., Kinchesh, P., Smart, S., Higgins, G. S., Chappell, M. A., & Sibson, N. R. (2019) · Cancer Research · doi:10.1158/0008-5472.can-18-2168 · Cited by 80 · see citing works
Fang, Z., Wang, C., Yang, J., Song, Z., Xie, C., Ji, Y., Wang, Z., Du, X., Zheng, Q., Chen, C., et al. (2023) · Nature Nanotechnology · doi:10.1038/s41565-023-01501-4 · Cited by 80 · see citing works
Natural D‐glucose as a biodegradable MRI relaxation agent
Yadav, N. N., Xu, J., Bar‐Shir, A., Qin, Q., Chan, K. W. Y., Grgac, K., Li, W., McMahon, M. T., & van Zijl, P. C. M. (2014) · Magnetic Resonance in Medicine · doi:10.1002/mrm.25329 · Cited by 79 · see citing works
Rivlin, M., Tsarfaty, I., & Navon, G. (2014) · Magnetic Resonance in Medicine · doi:10.1002/mrm.25467 · Cited by 77 · see citing works
Dou, W., Lin, C.-Y. E., Ding, H., Shen, Y., Dou, C., Qian, L., Wen, B., & Wu, B. H. (2019) · Quantitative Imaging in Medicine and Surgery · doi:10.21037/qims.2019.10.03 · Cited by 77 · see citing works
Microenvironment-triggered multimodal precision diagnostics
Hao, L., Rohani, N., Zhao, R. T., Pulver, E. M., Mak, H. H., Kelada, O. J., Ko, H., Fleming, H. E., Gertler, F. B., & Bhatia, S. N. (2021) · Nature Materials · doi:10.1038/s41563-021-01042-y · Cited by 76 · see citing works
Dynamic Imaging of Glucose and Lactate Metabolism by 13C-MRS without Hyperpolarization
Brender, J., Kishimoto, S., Merkle, H., Reed, G. D., Hurd, R. E., Chen, A. P., Ardenkjær‐Larsen, J. H., Munasinghe, J., Saito, K., Seki, T., et al. (2019) · Scientific Reports · doi:10.1038/s41598-019-38981-1 · Cited by 75 · see citing works
Functional polymers as metal-free magnetic resonance imaging contrast agents
Fu, C., Yu, Y., Xu, X., Wang, Q., Chang, Y.-X., Zhang, C., Zhao, J., Peng, H., & Whittaker, A. K. (2020) · Progress in Polymer Science · doi:10.1016/j.progpolymsci.2020.101286 · Cited by 75 · see citing works
Fast and Quantitative T1ρ-weighted Dynamic Glucose Enhanced MRI
Schuenke, P., Paech, D., Koehler, C., Windschuh, J., Bachert, P., Ladd, M. E., Schlemmer, H.-P., Radbruch, A., & Zaiß, M. (2017) · Scientific Reports · doi:10.1038/srep42093 · Cited by 75 · see citing works
Emerging Technologies to Image Tissue Metabolism
Ntziachristos, V., Pleitez, M. A., Aime, S., & Brindle, K. M. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2018.09.004 · Cited by 74 · see citing works
Zhang, J., Yuan, Y., Gao, M., Han, Z., Chu, C., Li, Y., van Zijl, P. C. M., Ying, M., Bulte, J. W. M., & Liu, G. (2019) · Angewandte Chemie International Edition · doi:10.1002/anie.201904722 · Cited by 73 · see citing works
Zhou, Y., Bie, C., van Zijl, P. C. M., & Yadav, N. N. (2022) · NMR in Biomedicine · doi:10.1002/nbm.4778 · Cited by 73 · see citing works
Anemone, A., Consolino, L., Conti, L., Reineri, F., Cavallo, F., Aime, S., & Longo, D. L. (2017) · International Journal of Oncology · doi:10.3892/ijo.2017.4029 · Cited by 73 · see citing works
Liu, G., Banerjee, S. R., Yang, X., Yadav, N. N., Lisok, A., Jabłońska, A., Xu, J., Li, Y., Pomper, M. G., & van Zijl, P. C. M. (2017) · Nature Biomedical Engineering · doi:10.1038/s41551-017-0168-8 · Cited by 70 · see citing works
Huang, J., Lai, J. H. C., Tse, K., Cheng, G. W., Liu, Y., Chen, Z., Han, X., Chen, L., Xu, J., & Chan, K. W. Y. (2021) · Magnetic Resonance in Medicine · doi:10.1002/mrm.29044 · Cited by 70 · see citing works
Glucosamine and N-acetyl glucosamine as new CEST MRI agents for molecular imaging of tumors
Rivlin, M., & Navon, G. (2016) · Scientific Reports · doi:10.1038/srep32648 · Cited by 70 · see citing works
Imaging Cancer Metabolism: Underlying Biology and Emerging Strategies
Pantel, A. R., Ackerman, D., Lee, S., Mankoff, D. A., & Gade, T. P. F. (2018) · Journal of Nuclear Medicine · doi:10.2967/jnumed.117.199869 · Cited by 70 · see citing works
Zaiß, M., Anemone, A., Goerke, S., Longo, D. L., Herz, K., Pohmann, R., Aime, S., Rivlin, M., Navon, G., Golay, X., et al. (2019) · NMR in Biomedicine · doi:10.1002/nbm.4113 · Cited by 69 · see citing works
Self-citationMapping human brain capillary water lifetime: high‐resolution metabolic neuroimaging
Rooney, W. D., Li, X., Sammi, M. K., BOURDETTE, D. N., Neuwelt, E. A., & SPRINGER, C. S. J. (2015) · NMR in Biomedicine · doi:10.1002/nbm.3294 · Cited by 69 · see citing works
Advances in Magnetic Resonance Imaging Contrast Agents for Biomarker Detection
Sinharay, S., & Pagel, M. D. (2016) · Annual Review of Analytical Chemistry · doi:10.1146/annurev-anchem-071015-041514 · Cited by 68 · see citing works
Jin, T., & Kim, S. (2014) · NMR in Biomedicine · doi:10.1002/nbm.3191 · Cited by 67 · see citing works
Mahajan, A., Goh, V., Basu, S. K., Vaish, R., Weeks, A. J., Thakur, M., & Cook, G. (2015) · Clinical Radiology · doi:10.1016/j.crad.2015.06.082 · Cited by 66 · see citing works
Wehner, J., Weissler, B., Dueppenbecker, P. M., Gebhardt, P., Goldschmidt, B., Schug, D., Kiessling, F. M., & Schulz, V. (2015) · Physics in Medicine and Biology · doi:10.1088/0031-9155/60/6/2231 · Cited by 65 · see citing works
Chan, K. W. Y., Jiang, L., Cheng, M., Wijnen, J. P., Liu, G., Huang, P., van Zijl, P. C. M., McMahon, M. T., & Glunde, K. (2016) · NMR in Biomedicine · doi:10.1002/nbm.3526 · Cited by 65 · see citing works
Creatine CEST MRI for Differentiating Gliomas with Different Degrees of Aggressiveness
Cai, K., Tain, R., Zhou, X. J., Damen, F. C., Scotti, A., Hariharan, H., Poptani, H., & Reddy, R. D. (2016) · Molecular Imaging and Biology · doi:10.1007/s11307-016-0995-0 · Cited by 64 · see citing works
MR imaging of a novel NOE-mediated magnetization transfer with water in rat brain at 9.4 T
Zhang, X., Wang, F., Jin, T., Xu, J., Xie, J., Gochberg, D. F., Gore, J. C., & Zu, Z. (2016) · Magnetic Resonance in Medicine · doi:10.1002/mrm.26396 · Cited by 64 · see citing works
Two decades of dendrimers as versatile MRI agents: a tale with and without metals
McMahon, M. T., & Bulte, J. W. M. (2017) · Wiley Interdisciplinary Reviews Nanomedicine and Nanobiotechnology · doi:10.1002/wnan.1496 · Cited by 64 · see citing works
Lee, H., Choi, Y. H., Sung, H. H., Han, D. H., Jeon, H. G., Jeong, B. C., Seo, S. I., Jeon, S. S., Lee, H. M., & Choi, H. Y. (2016) · Clinical Genitourinary Cancer · doi:10.1016/j.clgc.2016.08.023 · Cited by 63 · see citing works
Yuan, J., Chen, S., King, A. D., Zhou, J., Bhatia, K. S. S., Zhang, Q., Yeung, D. K. W., Wei, J., Mok, G. S. P., & Wáng, Y. X. J. (2014) · NMR in Biomedicine · doi:10.1002/nbm.3184 · Cited by 62 · see citing works
Xu, X., Sehgal, A. A., Yadav, N. N., Laterra, J., Blair, L., Blakeley, J. O., Seidemo, A., Coughlin, J. M., Pomper, M. G., Knutsson, L., et al. (2019) · Magnetic Resonance in Medicine · doi:10.1002/mrm.28124 · Cited by 62 · see citing works
A diaCEST MRI approach for monitoring liposomal accumulation in tumors
Chan, K. W. Y., Yu, T., Qiao, Y., Liu, Q., Yang, M., Patel, H. V., Liu, G., Kinzler, K. W., Vogelstein, B., Bulte, J. W. M., et al. (2014) · Journal of Controlled Release · doi:10.1016/j.jconrel.2014.02.005 · Cited by 61 · see citing works
Developing imidazoles as CEST MRI pH sensors
Yang, X., Song, X., Banerjee, S. R., Li, Y., Byun, Y., Liu, G., Bhujwalla, Z. M., Pomper, M. G., & McMahon, M. T. (2016) · Contrast Media & Molecular Imaging · doi:10.1002/cmmi.1693 · Cited by 61 · see citing works
A Comprehensive View on MRI Techniques for Imaging Blood-Brain Barrier Integrity.
Elschot, E. P., Backes, W., Postma, A., van Oostenbrugge, R. V., Staals, J., Rouhl, R., & Jansen, J. (2020) · Investigative Radiology · doi:10.1097/rli.0000000000000723 · Cited by 54 · see citing works
Magnetic Resonance Imaging of Liver Metastasis
Karaosmanoğlu, A. D., Onur, M. R., Ozmen, M. N., Akata, D., & Karçaaltıncaba, M. (2016) · Seminars in Ultrasound CT and MRI · doi:10.1053/j.sult.2016.08.005 · Cited by 60 · see citing works
Multiscale profiling of protease activity in cancer
Amini, A. P., Kirkpatrick, J. D., Wang, C. S., Jaeger, A. M., Su, S., Naranjo, S., Zhong, Q., Cabana, C. M., Jacks, T., & Bhatia, S. N. (2022) · Nature Communications · doi:10.1038/s41467-022-32988-5 · Cited by 60 · see citing works
Possible artifacts in dynamic CEST MRI due to motion and field alterations
Zaiß, M., Herz, K., Deshmane, A., Kim, M., Golay, X., Lindig, T. M., Bender, B., Ernemann, U., & Scheffler, K. (2018) · Journal of Magnetic Resonance · doi:10.1016/j.jmr.2018.11.002 · Cited by 59 · see citing works
Self-citationAdaptive denoising for chemical exchange saturation transfer MR imaging
Breitling, J., Deshmane, A., Goerke, S., Korzowski, A., Herz, K., Ladd, M. E., Scheffler, K., Bachert, P., & Zaiß, M. (2019) · NMR in Biomedicine · doi:10.1002/nbm.4133 · Cited by 59 · see citing works
- Authors
- Walker-Samuel, S., Ramasawmy, R., Torrealdea, F., Rega, M., Rajkumar, V., Johnson, S. P., Richardson, S., Gonçalves, M., Parkes, H. G., Årstad, E., Thomas, D. L., Pedley, R. B., Lythgoe, M. F., & Golay, X.
- Affiliations
- University College London (GB)
- UCL Queen Square Institute of Neurology (GB)
- Engineering and Physical Sciences Research Council (GB)
- ORCID
- Venue
- Nature Medicine
- Published
- 2013-07-07
- Volume
- 19
- Issue
- 8
- Pages
- 1067-1072
- ISSN
- 1078-8956 (ISSN-L)
- 1546-170X
- PMC
- PMC5275770
- OpenAlex
- W2011581245
- Cited by
- 479
- References
- 51
- Citations by year
- 2026: 20 · 2025: 25 · 2024: 21 · 2023: 36 · 2022: 34 · 2021: 37 · 2020: 32 · 2019: 58 · 2018: 45 · 2017: 49 · 2016: 48 · 2015: 43 · 2014: 24 · 2013: 6
- FWCI
- 28.71
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Medicine (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- Cancer Research UK (16463, A10331, 16464)
- National Institute for Health and Care Research (C309/A8274, C16412/A6269, C1519/A10331, C1060/A10334)
- British Heart Foundation
- Home Office
- Topics
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Physical Sciences › Chemistry › Spectroscopy › Advanced NMR Techniques and Applications
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Medical Imaging Techniques and Applications
- Keywords
- tumor glucose metabolism, hydroxyl groups, colorectal neoplasia, anaerobic glycolysis, tumor metabolic heterogeneity
- MeSH terms
- Amino Acids, Animals, Autoradiography, Carbon Isotopes, Female, Glucose, Humans, Magnetic Resonance Imaging, Microscopy, Fluorescence, Neoplasms, Perfusion, Cell Hypoxia, Fluorodeoxyglucose F18, Xenograft Model Antitumor Assays, Mice
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