Analysis of cancer metabolism by imaging hyperpolarized nuclei: prospects for translation to clinical research
Open accessAbstract
A major challenge in cancer biology is to monitor and understand cancer metabolism in vivo with the goal of improved diagnosis and perhaps therapy. Because of the complexity of biochemical pathways, tracer methods are required for detecting specific enzyme-catalyzed reactions. Stable isotopes such as (13)C or (15)N with detection by nuclear magnetic resonance provide the necessary information about tissue biochemistry, but the crucial metabolites are present in low concentration and therefore are beyond the detection threshold of traditional magnetic resonance methods. A solution is to improve sensitivity by a factor of 10,000 or more by temporarily redistributing the populations of nuclear spins in a magnetic field, a process termed hyperpolarization. Although this effect is short-lived, hyperpolarized molecules can be generated in an aqueous solution and infused in vivo where metabolism generates products that can be imaged. This discovery lifts the primary constraint on magnetic resonance imaging for monitoring metabolism-poor sensitivity-while preserving the advantage of biochemical information. The purpose of this report was to briefly summarize the known abnormalities in cancer metabolism, the value and limitations of current imaging methods for metabolism, and the principles of hyperpolarization. Recent preclinical applications are described. Hyperpolarization technology is still in its infancy, and current polarizer equipment and methods are suboptimal. Nevertheless, there are no fundamental barriers to rapid translation of this exciting technology to clinical research and perhaps clinical care.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Metabolic imaging using hyperpolarization of 13C and other stable isotopes has considerable translational potential in human disease because of its high sensitivity, integration with MRI, lack of the need for radioactive tracers, and ability to probe the flux of specific enzymatic reactions in vivo.
“metabolic imaging using hyperpolarization of 13C and other stable isotopes has considerable translational potential in human disease because of its high sensitivity, integration with MRI, lack of the need for radioactive tracers, and in particular its ability to probe the flux of specific enzymatic reactions in vivo (Kurhanewicz et al., 2011).”
From Cellular Metabolism and Disease: What Do Metabolic Outliers Teach Us? (2012) · cites this paper as Kurhanewicz et al., 2011
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Warburg, O. (1956) · Science · doi:10.1126/science.123.3191.309 · Cited by 13,425 · see citing works
An Integrated Genomic Analysis of Human Glioblastoma Multiforme
Parsons, D. W., Jones, S., Zhang, X., Lin, J. C.-H., Leary, R. J., Angenendt, P., Mankoo, P., Carter, H., Siu, I.-M., Gallia, G. L., et al. (2008) · Science · doi:10.1126/science.1164382 · Cited by 5,857 · see citing works
<i>IDH1</i> and <i>IDH2</i> Mutations in Gliomas
Yan, H., Parsons, D. W., Jin, G., McLendon, R., Rasheed, B. A., Yuan, W., Kos, I., Batinic-Haberle, I., Jones, S., Riggins, G. J., et al. (2009) · New England Journal of Medicine · doi:10.1056/nejmoa0808710 · Cited by 5,847 · see citing works
Cancer-associated IDH1 mutations produce 2-hydroxyglutarate
Dang, L., White, D. W., Gross, S., Bennett, B. D., Bittinger, M. A., Driggers, E. M., Fantin, V. R., Jang, H. G., Jin, S., Keenan, M. C., et al. (2009) · Nature · doi:10.1038/nature08617 · Cited by 4,154 · see citing works
Kim, J.-W., Tchernyshyov, I., Semenza, G. L., & Dang, C. V. (2006) · Cell Metabolism · doi:10.1016/j.cmet.2006.02.002 · Cited by 3,905 · see citing works
Increase in signal-to-noise ratio of > 10,000 times in liquid-state NMR
Ardenkjær‐Larsen, J. H., Fridlund, B., Gram, A., Hansson, G., Hansson, L., Lerche, M. H., Servin, R., Thaning, M., & Golman, K. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1733835100 · Cited by 2,870 · see citing works
The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth
Christofk, H. R., Vander Heiden, M. G., Harris, M. H., Ramanathan, A., Gerszten, R. E., Wei, R., Fleming, M. D., Schreiber, S. L., & Cantley, L. C. (2008) · Nature · doi:10.1038/nature06734 · Cited by 2,820 · see citing works
Recurring mutations found by sequencing an acute myeloid leukemia genome
Mardis, E. R., Ding, L., Dooling, D. J., Larson, D. E., McLellan, M. D., Chen, K., Koboldt, D. C., Fulton, R. S., Delehaunty, K. D., McGrath, S. D., et al. (2009) · New England Journal of Medicine · doi:10.1056/nejmoa0903840 · Cited by 2,219 · see citing works
Gao, P., Tchernyshyov, I., Chang, T.-C., Lee, Y.-S., Kita, K., Ochi, T., Zeller, K. I., De Marzo, A. M., Van Eyk, J. E., Mendell, J. T., et al. (2009) · Nature · doi:10.1038/nature07823 · Cited by 2,124 · see citing works
Succinate links TCA cycle dysfunction to oncogenesis by inhibiting HIF-α prolyl hydroxylase
Selak, M. A., Armour, S. M., MacKenzie, E. D., Boulahbel, H., Watson, D. G., Mansfield, K. D., Pan, Y., Simon, M. C., Thompson, C. B., & Gottlieb, E. (2005) · Cancer Cell · doi:10.1016/j.ccr.2004.11.022 · Cited by 2,108 · cited 2× · see citing works
“[24] Selak MA, Armour SM, MacKenzie ED, Boulahbel H, Watson DG, Mansfield”
BackgroundWise, D. R., DeBerardinis, R. J., Mancuso, A., Sayed, N., Zhang, X.-Y., Pfeiffer, H. K., Nissim, I., Daikhin, E., Yudkoff, M., McMahon, S. B., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810199105 · Cited by 2,001 · see citing works
Self-citationp53 Regulates Mitochondrial Respiration
Matoba, S., Kang, J.-G., Patino, W. D., Wragg, A., Boehm, M., Gavrilova, O., Hurley, P. J., Bunz, F., & Hwang, P. M. (2006) · Science · doi:10.1126/science.1126863 · Cited by 1,650 · see citing works
Mutations in <i>SDHD</i> , a Mitochondrial Complex II Gene, in Hereditary Paraganglioma
Baysal, B. E., Ferrell, R. E., Willett-Brozick, J. E., Lawrence, E. C., Myssiorek, D., Bosch, A., Mey, A. V. D., Taschner, P. E. M., Rubinstein, W. S., Myers, E. N., et al. (2000) · Science · doi:10.1126/science.287.5454.848 · Cited by 1,638 · see citing works
Fantin, V. R., St-Pierre, J., & Leder, P. (2006) · Cancer Cell · doi:10.1016/j.ccr.2006.04.023 · Cited by 1,635 · see citing works
Targeting lactate-fueled respiration selectively kills hypoxic tumor cells in mice
Sonveaux, P., Végran, F., Schroeder, T., Wergin, M., Verrax, J., Rabbani, Z. N., Saedeleer, C. J. D., Kennedy, K. M., Diepart, C., Jordan, B. F., et al. (2008) · Journal of Clinical Investigation · doi:10.1172/jci36843 · Cited by 1,633 · see citing works
Akt Stimulates Aerobic Glycolysis in Cancer Cells
Elstrom, R. L., Bauer, D. E., Buzzai, M., Karnauskas, R., Harris, M. H., Plas, D. R., Zhuang, H., Cinalli, R. M., Alavi, A., Rudin, C. M., et al. (2004) · Cancer Research · doi:10.1158/0008-5472.can-03-2904 · Cited by 1,454 · see citing works
c-Myc transactivation of <i>LDH-A</i> : Implications for tumor metabolism and growth
Shim, H., Dolde, C., Lewis, B. C., Wu, C.-S., Dang, G., Jungmann, R. A., Dalla-Favera, R., & Dang, C. V. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.13.6658 · Cited by 1,092 · see citing works
Astuti, D., Latif, F., Dallol, A., Dahia, P. L. M., Douglas, F., George, E., Sköldberg, F., Husebye, E. S., Eng, C., & Maher, E. R. (2001) · The American Journal of Human Genetics · doi:10.1086/321282 · Cited by 1,087 · see citing works
ATP citrate lyase inhibition can suppress tumor cell growth
Hatzivassiliou, G., Zhao, F., Bauer, D. E., Andreadis, C., Shaw, A. N., Dhanak, D., Hingorani, S. R., Tuveson, D. A., & Thompson, C. B. (2005) · Cancer Cell · doi:10.1016/j.ccr.2005.09.008 · Cited by 1,086 · see citing works
Biological magnetic resonance imaging using laser-polarized 129Xe
Albert, M. S., Cates, G. D., Driehuys, B., et al. (1994) · Nature · doi:10.1038/370199a0 · Cited by 1,059 · see citing works
Reversible Interactions with para-Hydrogen Enhance NMR Sensitivity by Polarization Transfer
Adams, R. W., Aguilar, J. A., Atkinson, K. D., et al. (2009) · Science · doi:10.1126/science.1168877 · Cited by 1,050 · see citing works
Parahydrogen and synthesis allow dramatically enhanced nuclear alignment
Bowers, C. R., & Weitekamp, D. P. (1987) · Journal of the American Chemical Society · doi:10.1021/ja00252a049 · Cited by 1,047 · see citing works
Brick by brick: metabolism and tumor cell growth
DeBerardinis, R. J., Sayed, N., Ditsworth, D., & Thompson, C. B. (2008) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2008.02.003 · Cited by 1,018 · see citing works
Self-citationPrinciples of dynamic nuclear polarisation
Abragam, A., & Goldman, M. (1978) · Reports on Progress in Physics · doi:10.1088/0034-4885/41/3/002 · Cited by 929 · see citing works
Citric acid cycle intermediates as ligands for orphan G-protein-coupled receptors
He, W., Miao, F. J.-P., Lin, D. C.-H., Schwandner, R. T., Wang, Z., Gao, J., Chen, J.-L., Tian, H., & Ling, L. (2004) · Nature · doi:10.1038/nature02488 · Cited by 909 · cited 2× · see citing works
“Furthermore, succinate can induce hypertension in animals when administered intravenously [145]; it is unclear whether this effect occurs in humans, but if it does, this may limit its clinical application.”
BackgroundDay, S. E., Kettunen, M. I., Gallagher, F. A., Hu, D., Lerche, M. H., Wolber, J., Golman, K., Ardenkjær‐Larsen, J. H., & Brindle, K. M. (2007) · Nature Medicine · doi:10.1038/nm1650 · Cited by 882 · see citing works
Self-citationMutations in SDHC cause autosomal dominant paraganglioma, type 3
Niemann, S., & Müller, U. (2000) · Nature Genetics · doi:10.1038/81551 · Cited by 875 · see citing works
Bowers, C. R., & Weitekamp, D. P. (1986) · Physical Review Letters · doi:10.1103/physrevlett.57.2645 · Cited by 871 · see citing works
Magnetic resonance imaging of pH in vivo using hyperpolarized 13C-labelled bicarbonate
Gallagher, F. A., Kettunen, M. I., Day, S. E., et al. (2008) · Nature · doi:10.1038/nature07017 · Cited by 851 · see citing works
Fatty-acid synthase and human cancer: new perspectives on its role in tumor biology
Kuhajda, F. P. (2000) · Nutrition · doi:10.1016/s0899-9007(99)00266-x · Cited by 789 · see citing works
Flier, J. S., Mueckler, M., Usher, P., & Lodish, H. F. (1987) · Science · doi:10.1126/science.3103217 · Cited by 778 · see citing works
Genes of glycolysis are ubiquitously overexpressed in 24 cancer classes
Altenberg, B., & Greulich, K. O. (2004) · Genomics · doi:10.1016/j.ygeno.2004.08.010 · Cited by 662 · see citing works
Golman, K., Zandt, R. I. ‘., & Thaning, M. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601319103 · Cited by 661 · see citing works
p53 regulates glucose metabolism through an IKK-NF-κB pathway and inhibits cell transformation
Kawauchi, K., Araki, K., Tobiume, K., & Tanaka, N. (2008) · Nature Cell Biology · doi:10.1038/ncb1724 · Cited by 635 · see citing works
Increased lipogenesis in cancer cells: new players, novel targets
Swinnen, J. V., Brusselmans, K., & Verhoeven, G. (2006) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/01.mco.0000232894.28674.30 · Cited by 610 · see citing works
Albers, M. J., Bok, R., Chen, A. P., Cunningham, C. H., Zierhut, M. L., Zhang, V. Y., Kohler, S. J., Tropp, J. S., Hurd, R. E., Yen, Y., et al. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-0749 · Cited by 521 · see citing works
Self-citationBuchmann, I., Henze, M., Engelbrecht, S., et al. (2007) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-007-0450-1 · Cited by 507 · see citing works
Simultaneous spatial and spectral selective excitation
Meyer, C. H., Pauly, J. M., Macovskiand, A., et al. (1990) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1910150211 · Cited by 502 · see citing works
New approaches for imaging tumour responses to treatment
Brindle, K. M. (2008) · Nature reviews. Cancer · doi:10.1038/nrc2289 · Cited by 447 · see citing works
Self-citationMolecular imaging with endogenous substances
Golman, K., Ardenkjær‐Larsen, J. H., Petersson, J. S., et al. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1733836100 · Cited by 427 · see citing works
Hypoxia Inhibits G1/S Transition through Regulation of p27 Expression
Gardner, L. B., Li, Q., Park, M. S., Flanagan, W. M., Semenza, G. L., & Dang, C. V. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m010189200 · Cited by 390 · see citing works
Beyond the T1 Limit: Singlet Nuclear Spin States in Low Magnetic Fields
Carravetta, M., Johannessen, O. G., & Levitt, M. H. (2004) · Physical Review Letters · doi:10.1103/physrevlett.92.153003 · Cited by 388 · see citing works
Blodgett, T. M., Meltzer, C. C., & Townsend, D. W. (2007) · Radiology · doi:10.1148/radiol.2422051113 · Cited by 387 · see citing works
Über den Stoffwechsel von Tumoren im Körper
Warburg, O. H., Wind, F., & Negelein, E. (1926) · Journal of Molecular Medicine · doi:10.1007/bf01726240 · Cited by 360 · see citing works
Gillies, R. J., Raghunand, N., García‐Martín, M. L., & Gatenby, R. A. (2004) · IEEE Engineering in Medicine and Biology Magazine · doi:10.1109/memb.2004.1360409 · Cited by 351 · see citing works
A definition of molecular imaging.
Mankoff, D. A. (2007) · PubMed · Cited by 324 · see citing works
Enhancement of chemotherapy by manipulation of tumour pH
Raghunand, N., He, X., van Sluis, R., Mahoney, B. P., Baggett, B. K., Taylor, C. W., Paine-Murrieta, G. D., Roe, D. J., Bhujwalla, Z. M., & Gillies, R. J. (1999) · British Journal of Cancer · doi:10.1038/sj.bjc.6690455 · Cited by 318 · see citing works
Gallagher, F. A., Kettunen, M. I., Hu, D., Jensen, P. R., Zandt, R. I. ‘., Karlsson, M. G., Gisselsson, A., Nelson, S. K., Witney, T. H., Bohndiek, S. E., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911447106 · Cited by 303 · see citing works
Self-citationHyperpolarized 13 C allows a direct measure of flux through a single enzyme-catalyzed step by NMR
Merritt, M. E., Harrison, C. E., Storey, C. J., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0706235104 · Cited by 278 · see citing works
Langbein, S., Zerilli, M., Hausen, A. Z., Staiger, W., Rensch-Boschert, K., Lukán, N., Popa, J., Ternullo, M. P., Steidler, A., Weiss, C., et al. (2006) · British Journal of Cancer · doi:10.1038/sj.bjc.6602962 · Cited by 261 · see citing works
In Vivo Magnetic Resonance Spectroscopy in Cancer
Gillies, R. J., & Morse, D. L. (2005) · Annual Review of Biomedical Engineering · doi:10.1146/annurev.bioeng.7.060804.100411 · Cited by 261 · see citing works
Schroeder, M., Cochlin, L. E., Heather, L. C., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0805953105 · Cited by 249 · see citing works
Harris, T., Eliyahu, G., Frydman, L., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0909049106 · Cited by 227 · see citing works
Adams, R. W., Duckett, S. B., Green, R. A., et al. (2009) · The Journal of Chemical Physics · doi:10.1063/1.3254386 · Cited by 225 · see citing works
Schroeder, M., Atherton, H. J., Ball, D. R., Cole, M. A., Heather, L. C., Griffin, J. L., Clarke, K., Radda, G. K., & Tyler, D. J. (2009) · The FASEB Journal · doi:10.1096/fj.09-129171 · Cited by 221 · see citing works
Cardiac metabolism measured noninvasively by hyperpolarized 13C MRI
Golman, K., Petersson, J. S., Magnusson, P. O., et al. (2008) · Magnetic Resonance in Medicine · doi:10.1002/mrm.21460 · Cited by 216 · see citing works
Carravetta, M., & Levitt, M. H. (2005) · The Journal of Chemical Physics · doi:10.1063/1.1893983 · Cited by 204 · see citing works
Hyperpolarized C‐13 spectroscopic imaging of the TRAMP mouse at 3T—Initial experience
Chen, A. P., Albers, M. J., Cunningham, C. H., et al. (2007) · Magnetic Resonance in Medicine · doi:10.1002/mrm.21256 · Cited by 199 · see citing works
Self-citationSpontaneous Transfer of Parahydrogen Derived Spin Order to Pyridine at Low Magnetic Field
Atkinson, K. D., Cowley, M. J., Elliott, P. I. P., et al. (2009) · Journal of the American Chemical Society · doi:10.1021/ja903601p · Cited by 199 · see citing works
Liver and adipose tissue contributions to newly formed fatty acids in an ascites tumor
Ookhtens, M., Kannan, R., Lyon, I., & Baker, N. (1984) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1984.247.1.r146 · Cited by 199 · see citing works
Kaelin, W. G., & Thompson, C. B. (2010) · Nature · doi:10.1038/465562a · Cited by 198 · see citing works
Increasing Hyperpolarized Spin Lifetimes Through True Singlet Eigenstates
Warren, W. S., Jenista, E. R., Branca, R. T., et al. (2009) · Science · doi:10.1126/science.1167693 · Cited by 192 · see citing works
Self-citationHyperpolarized 13C magnetic resonance metabolic imaging: application to brain tumors
Park, I., Larson, P. E. Z., Zierhut, M. L., Hu, S., Bok, R., Ozawa, T., Kurhanewicz, J. V., Vigneron, D. B., VandenBerg, S. R., James, C. D., et al. (2010) · Neuro-Oncology · doi:10.1093/neuonc/nop043 · Cited by 192 · see citing works
Self-citationMetabolic Imaging and Other Applications of Hyperpolarized 13C1
Golman, K., & Petersson, J. S. (2006) · Academic Radiology · doi:10.1016/j.acra.2006.06.001 · Cited by 191 · see citing works
In vivo 13carbon metabolic imaging at 3T with hyperpolarized 13C‐1‐pyruvate
Kohler, S. J., Yen, Y., Wolber, J., Chen, A. P., Albers, M. J., Bok, R., Zhang, V., Tropp, J., Nelson, S. J., Vigneron, D. B., et al. (2007) · Magnetic Resonance in Medicine · doi:10.1002/mrm.21253 · Cited by 191 · see citing works
Self-citationWorkman, P., Aboagye, E. O., Chung, Y., Griffiths, J. R., Hart, R., Leach, M. O., Maxwell, R. J., McSheehy, P. M. J., Price, P., & Zweit, J. (2006) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djj162 · Cited by 189 · see citing works
Self-citationCompressed sensing for resolution enhancement of hyperpolarized 13C flyback 3D-MRSI
Hu, S., Lustig, M. S., Chen, A. P., et al. (2008) · Journal of Magnetic Resonance · doi:10.1016/j.jmr.2008.03.003 · Cited by 187 · see citing works
Nuclear magnetic resonance imaging with hyperpolarised helium-3
Ebert, M., Grossmann, T., Heil, W., et al. (1996) · The Lancet · doi:10.1016/s0140-6736(96)90940-x · Cited by 187 · see citing works
PASADENA Hyperpolarization of Succinic Acid for MRI and NMR Spectroscopy
Chekmenev, E. Y., Hövener, J., Norton, V. A., et al. (2008) · Journal of the American Chemical Society · doi:10.1021/ja7101218 · Cited by 184 · see citing works
Self-citationIn vivo molecular imaging for planning radiation therapy of gliomas: An application of 1H MRSI
Nelson, S. J., Graves, E. E., Pirzkall, A., et al. (2002) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.10183 · Cited by 179 · see citing works
Hyperpolarization of 13C through order transfer from parahydrogen: A new contrast agent for MRI
Goldman, M., Jóhannesson, H., Axelsson, O., et al. (2005) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2004.11.031 · Cited by 177 · see citing works
Kinetic modeling of hyperpolarized 13C1-pyruvate metabolism in normal rats and TRAMP mice
Zierhut, M. L., Yen, Y., Chen, A. P., Bok, R., Albers, M. J., Zhang, V. Y., Tropp, J., Park, I., Vigneron, D. B., Kurhanewicz, J. V., et al. (2009) · Journal of Magnetic Resonance · doi:10.1016/j.jmr.2009.10.003 · Cited by 166 · see citing works
Self-citationMultiband excitation pulses for hyperpolarized 13C dynamic chemical-shift imaging
Larson, P. E. Z., Kerr, A. B., Chen, A. P., et al. (2008) · Journal of Magnetic Resonance · doi:10.1016/j.jmr.2008.06.010 · Cited by 160 · see citing works
Gallagher, F. A., Kettunen, M. I., Day, S. E., Lerche, M. H., & Brindle, K. M. (2008) · Magnetic Resonance in Medicine · doi:10.1002/mrm.21650 · Cited by 157 · see citing works
Self-citationGenerating highly polarized nuclear spins in solution using dynamic nuclear polarization
Wolber, J., Ellner, F., Fridlund, B., et al. (2004) · Nuclear Instruments and Methods in Physics Research Section A Accelerators Spectrometers Detectors and Associated Equipment · doi:10.1016/j.nima.2004.03.171 · Cited by 156 · see citing works
Double spin-echo sequence for rapid spectroscopic imaging of hyperpolarized 13C
Cunningham, C. H., Chen, A. P., Albers, M. J., et al. (2007) · Journal of Magnetic Resonance · doi:10.1016/j.jmr.2007.05.014 · Cited by 155 · see citing works
Self-citationMetabolite quantification and high‐field MRS in breast cancer
Haddadin, I., McIntosh, A., Meisamy, S., et al. (2007) · NMR in Biomedicine · doi:10.1002/nbm.1217 · Cited by 155 · see citing works
Amino acid, glucose, and lactic acid utilization in vivo by rat tumors.
Sauer, L. A., Stayman, J. W., & Dauchy, R. T. (1982) · PubMed · Cited by 152 · see citing works
Ward, C. S., Venkatesh, H. S., Chaumeil, M. M., Brandes, A., Criekinge, M. V., Dafni, H., Sukumar, S., Nelson, S. J., Vigneron, D. B., Kurhanewicz, J. V., et al. (2010) · Cancer Research · doi:10.1158/0008-5472.can-09-2251 · Cited by 152 · see citing works
Self-citationCholine Phospholipid Metabolism in Cancer: Consequences for Molecular Pharmaceutical Interventions
Glunde, K., Ackerstaff, E., Mori, N., et al. (2006) · Molecular Pharmaceutics · doi:10.1021/mp060067e · Cited by 143 · see citing works
Dynamic Nuclear Polarization of [1-13C]pyruvic acid at 4.6 tesla
Jóhannesson, H., Macholl, S., & Ardenkjær‐Larsen, J. H. (2008) · Journal of Magnetic Resonance · doi:10.1016/j.jmr.2008.12.016 · Cited by 142 · see citing works
McKnight, T. R., Lamborn, K. R., Love, T. D., Berger, M. S., Chang, S. M., Dillon, W. P., Bollen, A. W., & Nelson, S. J. (2007) · Journal of neurosurgery · doi:10.3171/jns.2007.106.4.660 · Cited by 139 · see citing works
Hyperpolarized xenon in NMR and MRI
Oros, A. M., & Shah, N. J. (2004) · Physics in Medicine and Biology · doi:10.1088/0031-9155/49/20/r01 · Cited by 137 · see citing works
Hu, S., Lustig, M. S., Balakrishnan, A., et al. (2009) · Magnetic Resonance in Medicine · doi:10.1002/mrm.22233 · Cited by 137 · see citing works
Talbot, J., Gutman, F., Fartoux, L., et al. (2006) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-006-0164-9 · Cited by 132 · see citing works
Noworolski, S. M., Henry, R. G., Vigneron, D. B., et al. (2005) · Magnetic Resonance in Medicine · doi:10.1002/mrm.20374 · Cited by 131 · see citing works
Self-citationThe Long-Lived Nuclear Singlet State of 15N-Nitrous Oxide in Solution
Pileio, G., Carravetta, M., Hughes, E., et al. (2008) · Journal of the American Chemical Society · doi:10.1021/ja803601d · Cited by 131 · see citing works
Therapeutic Target Metabolism Observed Using Hyperpolarized 15N Choline
Gabellieri, C., Reynolds, S., Lavie, A., et al. (2008) · Journal of the American Chemical Society · doi:10.1021/ja8001293 · Cited by 130 · see citing works
Pulse sequence for dynamic volumetric imaging of hyperpolarized metabolic products
Cunningham, C. H., Chen, A. P., Lustig, M. S., et al. (2008) · Journal of Magnetic Resonance · doi:10.1016/j.jmr.2008.03.012 · Cited by 130 · see citing works
Self-citationQuantitative13C NMR studies of metabolic compartmentation in the adult mammalian brain
Cruz, F., & Cerdán, S. (1999) · NMR in Biomedicine · doi:10.1002/(sici)1099-1492(199911)12:7 · Cited by 128 · see citing works
αvβ3-integrin imaging: a new approach to characterise angiogenesis?
Haubner, R. (2006) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-006-0136-0 · Cited by 127 · see citing works
Cerebral Blood Volume Measurements and Proton MR Spectroscopy in Grading of Oligodendroglial Tumors
Spampinato, M. V., Smith, J. K., Kwock, L., et al. (2006) · American Journal of Roentgenology · doi:10.2214/ajr.05.1177 · Cited by 124 · see citing works
Hurd, R. E., Yen, Y., Mayer, D., et al. (2010) · Magnetic Resonance in Medicine · doi:10.1002/mrm.22364 · Cited by 124 · see citing works
Hyperpolarized [2-13C]-Fructose: A Hemiketal DNP Substrate for In Vivo Metabolic Imaging
Keshari, K. R., Wilson, D. M., Chen, A. P., Bok, R., Larson, P. E. Z., Hu, S., Criekinge, M. V., Macdonald, J. M., Vigneron, D. B., & Kurhanewicz, J. V. (2009) · Journal of the American Chemical Society · doi:10.1021/ja9049355 · Cited by 119 · see citing works
Self-citationA 140GHz prepolarizer for dissolution dynamic nuclear polarization
Jannin, S., Comment, A., Kurdzesau, F., et al. (2008) · The Journal of Chemical Physics · doi:10.1063/1.2951994 · Cited by 116 · see citing works
Self-citationWitney, T. H., Kettunen, M. I., Day, S. E., Hu, D., Neves, A., Gallagher, F. A., Fulton, S. M., & Brindle, K. M. (2009) · Neoplasia · doi:10.1593/neo.09254 · Cited by 114 · see citing works
Self-citationProton NMR of15N-Choline Metabolites Enhanced by Dynamic Nuclear Polarization
Sarkar, R., Comment, A., Vasos, P. R., et al. (2009) · Journal of the American Chemical Society · doi:10.1021/ja9021304 · Cited by 113 · see citing works
Self-citationSilicon Nanoparticles as Hyperpolarized Magnetic Resonance Imaging Agents
Aptekar, J. W., Cassidy, M. C., Johnson, A. C., Barton, R. A., Lee, M., Ogier, A. C., Vo, C.-T., Anahtar, M. N., Ren, Y., Bhatia, S. N., et al. (2009) · ACS Nano · doi:10.1021/nn900996p · Cited by 112 · see citing works
Raghunand, N., Mahoney, B. P., van Sluis, R., Baggett, B. K., & Gillies, R. J. (2001) · Neoplasia · doi:10.1038/sj.neo.7900151 · Cited by 111 · see citing works
Pileio, G., & Levitt, M. H. (2009) · The Journal of Chemical Physics · doi:10.1063/1.3139064 · Cited by 110 · see citing works
Kettunen, M. I., Hu, D., Witney, T. H., et al. (2010) · Magnetic Resonance in Medicine · doi:10.1002/mrm.22276 · Cited by 110 · see citing works
Hyperpolarized water as an authentic magnetic resonance imaging contrast agent
McCarney, E. R., Armstrong, B. D., Lingwood, M. D., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610540104 · Cited by 109 · see citing works
Chen, A. P., Kurhanewicz, J. V., Bok, R., et al. (2008) · Magnetic Resonance Imaging · doi:10.1016/j.mri.2008.01.002 · Cited by 108 · see citing works
Self-citationCurrent and Potential Applications of Clinical 13C MR Spectroscopy
Kurhanewicz, J. V., Bok, R., Nelson, S. J., et al. (2008) · Journal of Nuclear Medicine · doi:10.2967/jnumed.107.045112 · Cited by 107 · see citing works
Self-citationProgress in Hyperpolarized Ultrafast 2D NMR Spectroscopy
Mishkovsky, M., & Frydman, L. (2008) · ChemPhysChem · doi:10.1002/cphc.200800461 · Cited by 105 · see citing works
Regulation of cytoplasmic pH in phagocytic cell function and dysfunction
Grinstein, S., Swallow, C. J., & Rotstein, O. D. (1991) · Clinical Biochemistry · doi:10.1016/0009-9120(91)80014-t · Cited by 101 · see citing works
Advances in MR Spectroscopy of the Prostate
Kurhanewicz, J. V., & Vigneron, D. B. (2008) · Magnetic Resonance Imaging Clinics of North America · doi:10.1016/j.mric.2008.07.005 · Cited by 101 · see citing works
Self-citationLarson, P. E. Z., Bok, R., Kerr, A. B., et al. (2010) · Magnetic Resonance in Medicine · doi:10.1002/mrm.22264 · Cited by 97 · see citing works
Mata, J. F., Altes, T. A., Cai, J. Y., et al. (2006) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00418.2006 · Cited by 96 · see citing works
Molecular imaging : principles and practice
Weissleder, R. (2010) · Medical Entomology and Zoology · Cited by 91 · see citing works
Friedlos, F., Lehouritis, P., Ogilvie, L. M., Hedley, D., Davies, L. C., Bermudes, D. G., King, I., Martin, J., Marais, R., & Springer, C. J. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-07-4800 · Cited by 91 · see citing works
Breeuwsma, A. J., Pruim, J., van den Bergh, A. C. M., et al. (2009) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2009.04.090 · Cited by 90 · see citing works
Mayer, D., Yen, Y., Tropp, J. S., et al. (2009) · Magnetic Resonance in Medicine · doi:10.1002/mrm.22041 · Cited by 89 · see citing works
Merritt, M. E., Harrison, C. E., Storey, C. J., et al. (2008) · Magnetic Resonance in Medicine · doi:10.1002/mrm.21760 · Cited by 88 · see citing works
Jensen, P. R., Peitersen, T., Karlsson, M. G., Zandt, R. I. ‘., Gisselsson, A., Hansson, G., Meier, S., & Lerche, M. H. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.066407 · Cited by 86 · see citing works
DNP-Hyperpolarized 13C Magnetic Resonance Metabolic Imaging for Cancer Applications
Nelson, S. J., Vigneron, D. B., Kurhanewicz, J. V., et al. (2008) · Applied Magnetic Resonance · doi:10.1007/s00723-008-0136-2 · Cited by 85 · see citing works
Self-citationPiert, M., Park, H., Khan, A. S., Siddiqui, J., Hussain, H. K., Chenevert, T. L., Wood, D. P., Johnson, T. D., Shah, R. B., & Meyer, C. R. (2009) · Journal of Nuclear Medicine · doi:10.2967/jnumed.109.063396 · Cited by 83 · see citing works
Hyperpolarized 1H NMR Employing Low γ Nucleus for Spin Polarization Storage
Chekmenev, E. Y., Norton, V. A., Weitekamp, D. P., et al. (2009) · Journal of the American Chemical Society · doi:10.1021/ja809634u · Cited by 81 · see citing works
Self-citationFast metabolic imaging of systems with sparse spectra: Application for hyperpolarized 13C imaging
Mayer, D., Levin, Y. S., Hurd, R. E., et al. (2006) · Magnetic Resonance in Medicine · doi:10.1002/mrm.21025 · Cited by 81 · see citing works
Keshari, K. R., Kurhanewicz, J. V., Jeffries, R. E., Wilson, D. M., Dewar, B. J., Criekinge, M. V., Zierhut, M. L., Vigneron, D. B., & Macdonald, J. M. (2010) · Magnetic Resonance in Medicine · doi:10.1002/mrm.22225 · Cited by 79 · see citing works
Self-citationHyperpolarized MR Imaging: Neurologic Applications of Hyperpolarized Metabolism
Ross, B. D., Bhattacharya, P. K., Wagner, S. R., et al. (2009) · American Journal of Neuroradiology · doi:10.3174/ajnr.a1790 · Cited by 75 · see citing works
Self-citationBeloueche‐Babari, M., Chung, Y.-L., Al-Saffar, N. M. S., et al. (2009) · British Journal of Cancer · doi:10.1038/sj.bjc.6605457 · Cited by 71 · see citing works
Krockenberger, M., Hönig, A., Rieger, L., et al. (2007) · International Journal of Gynecological Cancer · doi:10.1111/j.1525-1438.2007.00799.x · Cited by 71 · see citing works
Hu, S., Chen, A. P., Zierhut, M. L., et al. (2009) · Molecular Imaging and Biology · doi:10.1007/s11307-009-0218-z · Cited by 71 · see citing works
Imaging of branched chain amino acid metabolism in tumors with hyperpolarized 13 C ketoisocaproate
Karlsson, M. G., Jensen, P. R., Zandt, R. I. ‘., et al. (2009) · International Journal of Cancer · doi:10.1002/ijc.25072 · Cited by 70 · see citing works
Innovations in Radiotherapy Planning of Head and Neck Cancers: Role of PET
Troost, E. G. C., Schinagl, D. A. X., Bussink, J., et al. (2009) · Journal of Nuclear Medicine · doi:10.2967/jnumed.108.061499 · Cited by 69 · see citing works
Hyperpolarized Long-T1 Silicon Nanoparticles for Magnetic Resonance ImagingPreprint
Aptekar, J. W., Cassidy, M. C., Johnson, A. C., et al. (2009) · arXiv (Cornell University) · doi:10.48550/arxiv.0902.0269 · Cited by 69 · see citing works
Single‐acquisition sequence for the measurement of oxygen partial pressure by hyperpolarized gas MRI
Fischer, M. C., Spector, Z. Z., Ishii, M., Yu, J., Emami, K., Itkin, M. G., & Rizi, R. R. (2004) · Magnetic Resonance in Medicine · doi:10.1002/mrm.20239 · Cited by 68 · see citing works
Self-citationExtending the Scope of Singlet‐State Spectroscopy
Sarkar, R., Ahuja, P., Moskau, D., et al. (2007) · ChemPhysChem · doi:10.1002/cphc.200700545 · Cited by 68 · see citing works
Clinical Applications of Proton MR Spectroscopy in Oncology
Kwock, L., Smith, J. K., Castillo, M., et al. (2002) · Technology in Cancer Research & Treatment · doi:10.1177/153303460200100103 · Cited by 65 · see citing works
Levin, Y. S., Mayer, D., Yen, Y., et al. (2007) · Magnetic Resonance in Medicine · doi:10.1002/mrm.21327 · Cited by 64 · see citing works
Proton magnetic resonance spectroscopy of brain tumors correlated with pathology1
Magalhães, Á., Godfrey, W. A., Shen, Y., et al. (2004) · Academic Radiology · doi:10.1016/j.acra.2004.10.057 · Cited by 60 · see citing works
Hyperpolarized lithium‐6 as a sensor of nanomolar contrast agents
van Heeswijk, R. B., Uffmann, K., Comment, A., et al. (2009) · Magnetic Resonance in Medicine · doi:10.1002/mrm.21952 · Cited by 60 · see citing works
Self-citationSardanelli, F., Fausto, A., & Podo, F. (2008) · La radiologia medica · doi:10.1007/s11547-008-0228-y · Cited by 57 · see citing works
In vivo proton magnetic resonance spectroscopy of breast lesions: an update
Tse, G. M.-K., Yeung, D. K. Y., King, A. D., et al. (2006) · Breast Cancer Research and Treatment · doi:10.1007/s10549-006-9412-8 · Cited by 57 · see citing works
Proton MRS of the breast in the clinical setting
Mountford, C. E., Ramadan, S. A., Stanwell, P., et al. (2008) · NMR in Biomedicine · doi:10.1002/nbm.1301 · Cited by 57 · see citing works
Merritt, M. E., Harrison, C. E., Kovács, Z., et al. (2007) · Journal of the American Chemical Society · doi:10.1021/ja075768z · Cited by 55 · see citing works
Generation of hyperpolarized substrates by secondary labeling with [1,1- 13 C] acetic anhydride
Wilson, D. M., Hurd, R. E., Keshari, K. R., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810190106 · Cited by 54 · see citing works
Molecular imaging of proliferation in vivo: Positron emission tomography with [18F]fluorothymidine
Buck, A. K., Herrmann, K., Shen, C., et al. (2009) · Methods · doi:10.1016/j.ymeth.2009.03.009 · Cited by 52 · see citing works
Accelerated spectroscopic imaging of hyperpolarized C‐13 pyruvate using SENSE parallel imaging
Arunachalam, A., Whitt, D. B., Fish, K. M., et al. (2009) · NMR in Biomedicine · doi:10.1002/nbm.1401 · Cited by 48 · see citing works
Chen, J., Huang, S., Li, T., et al. (2006) · Neuroradiology · doi:10.1007/s00234-006-0066-3 · Cited by 46 · see citing works
Producing over 100ml of highly concentrated hyperpolarized solution by means of dissolution DNP
Comment, A., Rentsch, J., Kurdzesau, F., et al. (2008) · Journal of Magnetic Resonance · doi:10.1016/j.jmr.2008.06.003 · Cited by 45 · see citing works
Self-citationLee, C. P., Payne, G. S., Oregioni, A., et al. (2009) · British Journal of Cancer · doi:10.1038/sj.bjc.6605425 · Cited by 38 · see citing works
In vivo hyperpolarized 13C MR spectroscopic imaging with 1H decoupling
Chen, A. P., Tropp, J. S., Hurd, R. E., et al. (2008) · Journal of Magnetic Resonance · doi:10.1016/j.jmr.2008.12.004 · Cited by 38 · see citing works
Hyperpolarized 13C magnetic resonance detection of carboxypeptidase G2 activity
Jamin, Y., Gabellieri, C., Smyth, L. A., et al. (2009) · Magnetic Resonance in Medicine · doi:10.1002/mrm.22049 · Cited by 38 · see citing works
Cardiovascular Applications of Hyperpolarized Contrast Media and Metabolic Tracers
Bhattacharya, P. K., Ross, B. D., & Bünger, R. (2009) · Experimental Biology and Medicine · doi:10.3181/0904-mr-135 · Cited by 34 · see citing works
Self-citationKubota, K., Furumoto, S., Iwata, R., et al. (2006) · Annals of Nuclear Medicine · doi:10.1007/bf03026816 · Cited by 30 · see citing works
Chuang, C., Chan, A. A., Larson, D., et al. (2007) · Technology in Cancer Research & Treatment · doi:10.1177/153303460700600502 · Cited by 29 · see citing works
In vivo monitoring of fluoropyrimidine metabolites
Findlay, M. P. N., & Leach, M. O. (1994) · Anti-Cancer Drugs · doi:10.1097/00001813-199406000-00002 · Cited by 28 · see citing works
Self-citationAgents for Polarization Enhancement in MRI
Aime, S., Dastrù, W., Gobetto, R., et al. (2008) · Handbook of experimental pharmacology · doi:10.1007/978-3-540-72718-7_12 · Cited by 26 · see citing works
Geraghty, P. R., van den Bosch, M. A. A. J., Spielman, D. M., et al. (2008) · The Breast Journal · doi:10.1111/j.1524-4741.2008.00650.x · Cited by 24 · see citing works
Matsumoto, S., Espey, M. G., Utsumi, H., Devasahayam, N., Matsumoto, K., Matsumoto, A., Hirata, H., Wink, D. A., Kuppusamy, P., Subramanian, S., et al. (2008) · Magnetic Resonance in Medicine · doi:10.1002/mrm.21500 · Cited by 20 · see citing works
MRI of hyperpolarized 3He gas in human paranasal sinuses
Rizi, R. R., Dimitrov, I. E., Thompson, A. K., et al. (1998) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1910390603 · Cited by 19 · see citing works
Self-citationErratum: Targeting the protein kinase C family: are we there yet?
MacKay, H. J., & Twelves, C. (2008) · Nature reviews. Cancer · doi:10.1038/nrc2350 · Cited by 16 · see citing works
The Translational Research Working Group Developmental Pathway for Image-Based Assessment Modalities
Dorfman, G. S., Sullivan, D. C., Schnall, M. D., et al. (2008) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-08-1264 · Cited by 13 · see citing works
Hou, X., & Gao, P. (2009) · PubMed · Cited by 2 · see citing works
Flagged first, then by citations
Research works printed but not linked: 9
- Kaelin WG Jr and Thompson CB (2010). Q&A: cancer: clues from cell metabo- lism. Nature 465(7298), 562-564.
- Gillies RJ, Raghunand N, Garcia-Martin ML, and Gatenby RA (2004). pH imaging. A review of pH measurement methods and applications in cancers. IEEE Eng Med Biol Mag 23(5), 57-64.
- Kurhanewicz J, Bok R, Nelson SJ, and Vigneron DB (2008). Current and poten- tial applications of clinical 13 C MR spectroscopy. J Nucl Med 49(3), 341-344.
- Jamin Y, Gabellieri C, Smyth L, Reynolds S, Robinson SP, Springer CJ, Leach MO, Payne GS, and Eykyn TR (2009). Hyperpolarized (13)C magnetic reso- nance detection of carboxypeptidase G2 activity. Magn Reson Med 62(5), 1300-1304.
- Golman K, in 't Zandt R, and Thaning M (2006). Real-time metabolic im- aging. Proc Natl Acad Sci USA 103(30), 11270-11275.
- Golman K, Petersson JS, Magnusson P, Johansson E, Akeson P, Chai CM, Hansson G, and Månsson S (2008). Cardiac metabolism measured noninva- sively by hyperpolarized (13)C MRI. Magn Reson Med 59(5), 1005-1013.
- Harris T, Eliyahu G, Frydman L, and Degani H (2009). Kinetics of hyper- polarized 13 C1-pyruvate transport and metabolism in living human breast can- cer cells. Proc Natl Acad Sci USA 106(43), 18131-18136.
- Jensen PR, Peitersen T, Karlsson M, In't Zandt R, Gisselsson A, Hansson G, Meier S, and Lerche MH (2009). Tissue-specific short chain fatty acid metab- olism and slow metabolic recovery after ischemia from hyperpolarized NMR in vivo. J Biol Chem 284(52), 36077-36082.
- Podo F (1999). Tumour phospholipid metabolism. NMR Biomed 12(7), 413-439.
Cited by
Sorted by citations
The return of metabolism: biochemistry and physiology of the pentose phosphate pathway
Stincone, A., Prigione, A., Cramer, T., Wamelink, M. M. C., Campbell, K., Cheung, E., Olin‐Sandoval, V., Grüning, N., Krüger, A., Tauqeer Alam, M., et al. (2015) · Biological Reviews · doi:10.1111/brv.12140 · Cited by 1,576 · see citing works
Self-citationGlutamine and cancer: cell biology, physiology, and clinical opportunities
Hensley, C. T., Wasti, A. T., & DeBerardinis, R. J. (2013) · Journal of Clinical Investigation · doi:10.1172/jci69600 · Cited by 1,262 · see citing works
Self-citationCellular Metabolism and Disease: What Do Metabolic Outliers Teach Us?
DeBerardinis, R. J., & Thompson, C. B. (2012) · Cell · doi:10.1016/j.cell.2012.02.032 · Cited by 858 · see citing works
Self-citationMarin-Valencia, I., Yang, C., Mashimo, T., Cho, S., Baek, H., Yang, X.-L., Rajagopalan, K. N., Maddie, M., Vemireddy, V., Zhao, Z., et al. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.05.001 · Cited by 529 · see citing works
Self-citation<i>IDH1</i> Mutation Induces Reprogramming of Pyruvate Metabolism
Izquierdo-Garcia, J. L., Viswanath, P., Eriksson, P., Cai, L., Radoul, M., Chaumeil, M. M., Blough, M., Luchman, H. A., Weiss, S., Cairncross, J. G., et al. (2015) · Cancer Research · doi:10.1158/0008-5472.can-15-0840 · Cited by 123 · see citing works
- Authors
- Kurhanewicz, J., Vigneron, D. B., Brindle, K., Chekmenev, E. Y., Comment, A., Cunningham, C. H., DeBerardinis, R. J., Green, G. G., Leach, M. O., Rajan, S. S., Rizi, R. R., Ross, B. D., Warren, W. S., & Malloy, C. R.
- Affiliations
- University of California, San Francisco (US)
- University of Cambridge (GB)
- Vanderbilt University (US)
- École Polytechnique Fédérale de Lausanne (CH)
- Sunnybrook Health Science Centre (CA)
- The University of Texas Southwestern Medical Center (US)
- University of York (GB)
- Institute of Cancer Research (GB)
- United States Food and Drug Administration (US)
- University of Pennsylvania (US)
- Huntington Medical Research Institutes (US)
- Duke University (US)
- Corresponding author
- Kurhanewicz, John
- ORCID
- Venue
- Neoplasia
- Publisher
- Elsevier BV
- Published
- 2011-02
- Volume
- 13
- Issue
- 2
- Pages
- 81-97
- ISSN
- 1476-5586 (ISSN-L)
- PMC
- PMC3033588
- OpenAlex
- W1912319529
- Cited by
- 681
- References
- 156
- Citations by year
- 2026: 14 · 2025: 13 · 2024: 12 · 2023: 25 · 2022: 20 · 2021: 21 · 2020: 40 · 2019: 40 · 2018: 59 · 2017: 67 · 2016: 78 · 2015: 58 · 2014: 83 · 2013: 64 · 2012: 58
- FWCI
- 33.70
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Neoplasia (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
- Funders
- University of Pennsylvania
- National Institutes of Health
- National Institute of Standards and Technology
- National Heart, Lung, and Blood Institute
- National Cancer Institute
- National Institute of Diabetes and Digestive and Kidney Diseases
- National Institute of Biomedical Imaging and Bioengineering (R01EB002122)
- National Center for Research Resources (P41RR002584)
- Topics
- Physical Sciences › Chemistry › Spectroscopy › Advanced NMR Techniques and Applications
- Physical Sciences › Physics and Astronomy › Atomic and Molecular Physics, and Optics › Atomic and Subatomic Physics Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
- Keywords
- cancer metabolism, hyperpolarization, magnetic resonance imaging, metabolic imaging, clinical translation, preclinical applications
- MeSH terms
- Carbon Isotopes, Fumarates, Humans, Magnetic Resonance Imaging, Neoplasms, Biomarkers, Tumor, Pyruvic Acid, Positron-Emission Tomography, Metabolic Networks and Pathways
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
