Non-invasive detection of 2-hydroxyglutarate and other metabolites in IDH1 mutant glioma patients using magnetic resonance spectroscopy
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Mutations of the isocitrate dehydrogenase 1 and 2 genes (IDH1 and IDH2) are commonly found in primary brain cancers. We previously reported that a novel enzymatic activity of these mutations results in the production of the putative oncometabolite, R(-)-2-hydroxyglutarate (2-HG). Here we investigated the ability of magnetic resonance spectroscopy (MRS) to detect 2-HG production in order to non-invasively identify patients with IDH1 mutant brain tumors. Patients with intrinsic glial brain tumors (n = 27) underwent structural and spectroscopic magnetic resonance imaging prior to surgery. 2-HG levels from MRS data were quantified using LC-Model software, based upon a simulated spectrum obtained from a GAMMA library added to the existing prior knowledge database. The resected tumors were then analyzed for IDH1 mutational status by genomic DNA sequencing, Ki-67 proliferation index by immunohistochemistry, and concentrations of 2-HG and other metabolites by liquid chromatography-mass spectrometry (LC-MS). MRS detected elevated 2-HG levels in gliomas with IDH1 mutations compared to those with wild-type IDH1 (P = 0.003). The 2-HG levels measured in vivo with MRS were significantly correlated with those measured ex vivo from the corresponding tumor samples using LC-MS (r (2) = 0.56; P = 0.0001). Compared with wild-type tumors, those with IDH1 mutations had elevated choline (P = 0.01) and decreased glutathione (P = 0.03) on MRS. Among the IDH1 mutated gliomas, quantitative 2-HG values were correlated with the Ki-67 proliferation index of the tumors (r ( 2 ) = 0.59; P = 0.026). In conclusion, water-suppressed proton ((1)H) MRS provides a non-invasive measure of 2-HG in gliomas, and may serve as a potential biomarker for patients with IDH1 mutant brain tumors. In addition to 2-HG, alterations in several other metabolites measured by MRS correlate with IDH1 mutation status.
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1H magnetic resonance spectroscopy can be applied for 2HG detection in vivo for glioma.
“recent data have suggested that 1H magnetic resonance spectroscopy can be applied for 2HG detection in vivo for glioma (Andronesi et al., 2012; Choi et al., 2012; Gross et al., 2010; Pope et al., 2012)”
From Metabolic Reprogramming: A Cancer Hallmark Even Warburg Did Not Anticipate (2012) · cites this paper as Pope et al., 2012
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Cites
Verhaak, R. G. W., Hoadley, K. A., Purdom, E., Wang, V., Qi, Y., Wilkerson, M. D., Miller, C. R., Ding, L., Golub, T., Mesirov, J. P., et al. (2010) · Cancer Cell · doi:10.1016/j.ccr.2009.12.020 · Cited by 7,575 · 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
Self-citationEstimation of metabolite concentrations from localized in vivo proton NMR spectra
Provencher, S. W. (1993) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1910300604 · Cited by 3,659 · see citing works
Xu, W., Yang, H., Liu, Y., Yang, Y., Wang, P., Kim, S.-H., Ito, S., Yang, C., Wang, P., Xiao, M.-T., et al. (2011) · Cancer Cell · doi:10.1016/j.ccr.2010.12.014 · Cited by 2,875 · see citing works
WISEMAN, H., & HALLIWELL, B. (1996) · Biochemical Journal · doi:10.1042/bj3130017 · Cited by 2,345 · see citing works
Ward, P. S., Patel, J., Wise, D. R., Abdel-Wahab, O., Bennett, B. D., Coller, H. A., Cross, J. R., Fantin, V. R., Hedvat, C. V., Perl, A. E., et al. (2010) · Cancer Cell · doi:10.1016/j.ccr.2010.01.020 · Cited by 2,020 · see citing works
Self-citationSpatial Localization in NMR Spectroscopy in Vivo
Bottomley, P. A. (1987) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1987.tb32915.x · Cited by 1,382 · see citing works
Hartmann, C. J., Meyer, J., Balß, J., Capper, D., Mueller, W. C., Christians, A., Felsberg, J., Wolter, M., Mawrin, C., Wick, W., et al. (2009) · Acta Neuropathologica · doi:10.1007/s00401-009-0561-9 · Cited by 1,163 · see citing works
Analysis of the IDH1 codon 132 mutation in brain tumors
Balss, J., Meyer, J., Mueller, W., Korshunov, A., Hartmann, C., & von Deimling, A. (2008) · Acta Neuropathologica · doi:10.1007/s00401-008-0455-2 · Cited by 1,036 · see citing works
IDH1 mutations are early events in the development of astrocytomas and oligodendrogliomas
Watanabe, T., Nobusawa, S., Kleihues, P., & Ohgaki, H. (2009) · The American Journal of Pathology · doi:10.2353/ajpath.2009.080958 · Cited by 1,027 · see citing works
Gross, S., Cairns, R. A., Minden, M. D., Driggers, E. M., Bittinger, M. A., Jang, H. G., Sasaki, M., Jin, S., Schenkein, D. P., Su, S. M., et al. (2010) · Journal of Experimental Medicine · doi:10.1084/jem.20092506 · Cited by 736 · see citing works
Self-citationWET, a T1- and B1-Insensitive Water-Suppression Method for in Vivo Localized 1H NMR Spectroscopy
Ogg, R. J., Kingsley, R. B., & Taylor, J. S. (1994) · Journal of Magnetic Resonance Series B · doi:10.1006/jmrb.1994.1048 · Cited by 734 · see citing works
Computer Simulations in Magnetic Resonance. An Object-Oriented Programming Approach
Smith, S. A., Levante, T. O., Meier, B. H., & Ernst, R. R. (1994) · Journal of Magnetic Resonance Series A · doi:10.1006/jmra.1994.1008 · Cited by 711 · see citing works
Profiling the effects of isocitrate dehydrogenase 1 and 2 mutations on the cellular metabolome
Reitman, Z. J., Jin, G., Karoly, E. D., Spasojevic, I., Yang, J., Kinzler, K. W., He, Y., Bigner, D. D., Vogelstein, B., & Yan, H. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1019393108 · Cited by 449 · see citing works
van den Bent, M. J., Dubbink, H. J., Marie, Y., Brandes, A. A., TAPHOORN, M. J. B., Wesseling, P., Frénay, M., Tijssen, C. C., Lacombe, D. A., Idbaïh, A., et al. (2010) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-09-2902 · Cited by 379 · see citing works
Dowling, C., Bollen, A. W., Noworolski, S. M., McDermott, M. W., Barbaro, N. M., Day, M. R., Henry, R. G., Chang, S. M., Dillon, W. P., Nelson, S. J., et al. (2001) · PubMed Central · Cited by 378 · see citing works
IDH mutations in glioma and acute myeloid leukemia
Dang, L., Jin, S., & Su, S.-S. M. (2010) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2010.07.002 · Cited by 368 · see citing works
Self-citationBleeker, F. E., Lamba, S., Leenstra, S., Troost, D., Hulsebos, T. J. M., Vandertop, W. P., Frattini, M., Molinari, F., Knowles, M. A., Cerrato, A., et al. (2009) · Human Mutation · doi:10.1002/humu.20937 · Cited by 365 · see citing works
Cramér–Rao bounds: an evaluation tool for quantitation
Cavassila, S., Deval, S., Huegen, C., ORMONDT, D. V., & Graveron‐Demilly, D. (2001) · NMR in Biomedicine · doi:10.1002/nbm.701 · Cited by 333 · see citing works
Tedeschi, G., Lundbom, N. M. I., Raman, R., Bonavita, S., Duyn, J. H., Alger, J. R., & Chiro, G. D. (1997) · Journal of neurosurgery · doi:10.3171/jns.1997.87.4.0516 · Cited by 269 · see citing works
Chou, W., Hou, H., Chen, C., Tang, J., Yao, M., Tsay, W., Ko, B.-S., Wu, S., Huang, S., Hsu, S.-C., et al. (2010) · Blood · doi:10.1182/blood-2009-11-253070 · Cited by 204 · see citing works
IDH1 mutations in low-grade astrocytomas predict survival but not response to temozolomide
Dubbink, H. J., Taal, W., van Marion, R., Kros, J. M., van Heuvel, I., Bromberg, J. E. C., Zonnenberg, B. A., Zonnenberg, C. B. L., Postma, T. J., Gijtenbeek, J. M. M., et al. (2009) · Neurology · doi:10.1212/wnl.0b013e3181c34ace · Cited by 186 · see citing works
Hydroxyglutaric aciduria and malignant brain tumor: a case report and literature review
Aghili, M., Zahedi, F., & Rafiee, E. (2009) · Journal of Neuro-Oncology · doi:10.1007/s11060-008-9706-2 · Cited by 159 · see citing works
IDH1andIDH2Mutations in Gliomas
Carli, E. D., Wang, X.-W., & Puget, S. (2009) · New England Journal of Medicine · doi:10.1056/nejmc090593 · Cited by 134 · see citing works
Jin, G., Reitman, Z. J., Spasojevic, I., Batinic-Haberle, I., Yang, J., Schmidt-Kittler, O., Bigner, D. D., & Yan, H. (2011) · PLoS ONE · doi:10.1371/journal.pone.0016812 · Cited by 112 · see citing works
van, Dubbink, Hj, Mariê, Brandes, Aa, TAPHOORN, M. J. B., Mj, Wesseling, P., Frenay, et al. (2010) · 中国神经肿瘤杂志 · Cited by 104 · see citing works
Molecular signatures classify astrocytic gliomas by IDH1 mutation status
Toedt, G., Barbus, S., Wolter, M., Felsberg, J., Tews, B., Blond, F., Sabel, M., Hofmann, S., Becker, N., Hartmann, C. J., et al. (2010) · International Journal of Cancer · doi:10.1002/ijc.25448 · Cited by 78 · see citing works
The principles of quantification applied to in vivo proton MR spectroscopy
Helms, G. (2008) · European Journal of Radiology · doi:10.1016/j.ejrad.2008.02.034 · Cited by 59 · see citing works
Proton magnetic resonance spectroscopy imaging in the study of human brain cancer.
Martínez‐Bisbal, M. C., & Celda, B. (2009) · PubMed · Cited by 35 · see citing works
Labussière, M., Wang, X.-W., Idbaïh, A., Ducray, F., & Sanson, M. (2010) · Future Oncology · doi:10.2217/fon.10.25 · Cited by 22 · see citing works
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Ward, P. S., & Thompson, C. B. (2012) · Cancer Cell · doi:10.1016/j.ccr.2012.02.014 · Cited by 3,233 · see citing works
Metabolic pathways promoting cancer cell survival and growth
Boroughs, L. K., & DeBerardinis, R. J. (2015) · Nature Cell Biology · doi:10.1038/ncb3124 · Cited by 1,459 · see citing works
Glioma Subclassifications and Their Clinical Significance
Chen, R., Smith-Cohn, M., Cohen, A. L., & Colman, H. (2017) · Neurotherapeutics · doi:10.1007/s13311-017-0519-x · Cited by 812 · see citing works
Glutathione levels in human tumors
Gamcsik, M. P., Kasibhatla, M. S., Teeter, S. D., & Colvin, O. M. (2012) · Biomarkers · doi:10.3109/1354750x.2012.715672 · Cited by 608 · see citing works
Emerging insights into the molecular and cellular basis of glioblastomaPreprint
Dunn, G. P., Rinne, M. L., Wykosky, J., Genovese, G., Quayle, S. N., Dunn, I. F., Agarwalla, P. K., Chheda, M. G., Campos, B., Wang, A., et al. (2012) · Genes & Development · doi:10.1101/gad.187922.112 · Cited by 559 · see citing works
IDH1andIDH2Mutations in Tumorigenesis: Mechanistic Insights and Clinical Perspectives
Yang, H., Ye, D., Guan, K., & Xiong, Y. (2012) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-12-1773 · Cited by 459 · see citing works
Oncometabolites: linking altered metabolism with cancer
Yang, M. H., Soga, T., & Pollard, P. J. (2013) · Journal of Clinical Investigation · doi:10.1172/jci67228 · Cited by 424 · see citing works
Chang, K., Bai, H. X., Zhou, H., Su, C., Bi, W. L., Agbodza, E., Kavouridis, V. K., Senders, J. T., Boaro, A., Beers, A. L., et al. (2017) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-17-2236 · Cited by 392 · see citing works
McBrayer, S. K., Mayers, J. R., DiNatale, G. J., Shi, D. D., Khanal, J., Chakraborty, A. A., Sarosiek, K. A., Briggs, K. J., Robbins, A. K., Sewastianik, T., et al. (2018) · Cell · doi:10.1016/j.cell.2018.08.038 · Cited by 368 · see citing works
Multimodal MRI features predict isocitrate dehydrogenase genotype in high-grade gliomas
Zhang, B., Chang, K., Ramkissoon, S. H., Tanguturi, S. K., Bi, W. L., Reardon, D. A., Ligon, K. L., Alexander, B. M., Wen, P. Y., & Huang, R. Y. (2016) · Neuro-Oncology · doi:10.1093/neuonc/now121 · Cited by 262 · see citing works
Intraoperative mass spectrometry mapping of an onco-metabolite to guide brain tumor surgery
Santagata, S., Eberlin, L. S., Norton, I. H., Calligaris, D., Feldman, D. R., Ide, J. L., Liu, X., Wiley, J. S., Vestal, M. L., Ramkissoon, S. H., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1404724111 · Cited by 259 · see citing works
Kalyanaraman, B., Cheng, G., Hardy, M., Ouari, O., López, M., Joseph, J., Zielonka, J., & Dwinell, M. B. (2017) · Redox Biology · doi:10.1016/j.redox.2017.09.020 · Cited by 236 · see citing works
The role of neuropathology in the management of patients with diffuse low grade glioma
Cahill, D. P., Sloan, A. E., Nahed, B. V., Aldape, K., Louis, D. N., Ryken, T. C., Kalkanis, S. N., & Olson, J. J. (2015) · Journal of Neuro-Oncology · doi:10.1007/s11060-015-1909-8 · Cited by 230 · see citing works
Noninvasive IDH1 mutation estimation based on a quantitative radiomics approach for grade II glioma
Yu, J., Shi, Z., Lian, Y., Li, Z., Liu, T., Gao, Y., Wang, Y., Chen, L., & Mao, Y. Q. (2016) · European Radiology · doi:10.1007/s00330-016-4653-3 · Cited by 213 · see citing works
Mountz, J. M., Ahmed, R., Oborski, M. J., Lieberman, F. S., & Hwang, M. (2014) · Cancer Management and Research · doi:10.2147/cmar.s54726 · Cited by 210 · see citing works
Choi, C., Raisanen, J. M., Ganji, S. K., Zhang, S., McNeil, S. S., An, Z., Madan, A., Hatanpaa, K. J., Vemireddy, V., Sheppard, C. A., et al. (2016) · Journal of Clinical Oncology · doi:10.1200/jco.2016.67.1222 · Cited by 201 · see citing works
Combining molecular and imaging metrics in cancer: radiogenomics
Gullo, R. L., Naranjo, I. D., Morris, E. A., & Pinker, K. (2020) · Insights into Imaging · doi:10.1186/s13244-019-0795-6 · Cited by 181 · see citing works
Imaging Correlates of Adult Glioma Genotypes
Smits, M., & van den Bent, M. J. (2017) · Radiology · doi:10.1148/radiol.2017151930 · Cited by 180 · see citing works
2016 Updates to the WHO Brain Tumor Classification System: What the Radiologist Needs to Know
Johnson, D. R., Guerin, J. B., Giannini, C., Morris, J. M., Eckel, L. J., & Kaufmann, T. J. (2017) · Radiographics · doi:10.1148/rg.2017170037 · Cited by 177 · see citing works
Detection of oncogenic IDH1 mutations using magnetic resonance spectroscopy of 2-hydroxyglutarate
Andronesi, O. C., Rapalino, O., Gerstner, E. R., Chi, A. S., Batchelor, T. T., Cahill, D. P., Sorensen, A. G., & Rosen, B. R. (2013) · Journal of Clinical Investigation · doi:10.1172/jci67229 · Cited by 174 · see citing works
Predicting IDH mutation status in grade II gliomas using amide proton transfer‐weighted (APTw) MRI
Jiang, S., Zou, T., Eberhart, C. G., Villalobos, M. A. V., Heo, H., Zhang, Y., Wang, Y., Wang, X., Yu, H., Du, Y., et al. (2017) · Magnetic Resonance in Medicine · doi:10.1002/mrm.26820 · Cited by 172 · see citing works
Emerging Therapies for Glioblastoma
Thomas, A. A., Brennan, C., DeAngelis, L. M., & Omuro, A. M. P. (2014) · JAMA Neurology · doi:10.1001/jamaneurol.2014.1701 · Cited by 167 · see citing works
Paech, D., Windschuh, J., Oberhollenzer, J., Dreher, C., Sahm, F., Meissner, J., Goerke, S., Schuenke, P., Zaiß, M., Regnery, S., et al. (2018) · Neuro-Oncology · doi:10.1093/neuonc/noy073 · Cited by 166 · see citing works
Isocitrate dehydrogenase‐mutant glioma: Evolving clinical and therapeutic implications
Miller, J. J., Shih, H. A., Andronesi, O. C., & Cahill, D. P. (2017) · Cancer · doi:10.1002/cncr.31039 · Cited by 152 · see citing works
Andronesi, O. C., Loebel, F., Bogner, W., Marjańska, M., Heiden, M. G. V., Iafrate, A. J., Dietrich, J., Batchelor, T. T., Gerstner, E. R., Kaelin, W. G., et al. (2015) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-15-0656 · Cited by 153 · see citing works
Non-invasive in vivo assessment of IDH1 mutational status in glioma
Chaumeil, M. M., Larson, P. E. Z., Yoshihara, H. A. I., Danforth, O. M., Vigneron, D. B., Nelson, S. J., Pieper, R. O., Phillips, J. J., & Ronen, S. M. (2013) · Nature Communications · doi:10.1038/ncomms3429 · Cited by 139 · see citing works
Yogananda, C. G. B., Shah, B., Vejdani‐Jahromi, M., Nalawade, S. S., Murugesan, G. K., Yu, F. F., Pinho, M. C., Wagner, B., Mickey, B., Patel, T., et al. (2019) · Neuro-Oncology · doi:10.1093/neuonc/noz199 · Cited by 138 · see citing works
RetractedRadiogenomic Analysis of Oncological Data: A Technical Survey
Incoronato, M., Aiello, M., Infante, T., Cavaliere, C., Grimaldi, A., Mirabelli, P., Monti, S., & Salvatore, M. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18040805 · Cited by 136 · see citing works
IDH1/2 mutations target a key hallmark of cancer by deregulating cellular metabolism in glioma
Zhang, C., Moore, L. M., Li, X., Yung, W. K. A., & Zhang, W. (2013) · Neuro-Oncology · doi:10.1093/neuonc/not087 · Cited by 132 · see citing works
Zhou, H., Chang, K., Bai, H. X., Xiao, B., Su, C., Bi, W. L., Zhang, P. J., Senders, J. T., Vallières, M., Kavouridis, V. K., et al. (2019) · Journal of Neuro-Oncology · doi:10.1007/s11060-019-03096-0 · Cited by 130 · see citing works
Suh, C. H., Kim, H. S., Jung, S. C., Choi, C. G., & Kim, S. J. (2018) · Neuro-Oncology · doi:10.1093/neuonc/noy113 · Cited by 128 · see citing works
New Molecular Considerations for Glioma: IDH, ATRX, BRAF, TERT, H3 K27M
Karsy, M. J., Guan, J., Cohen, A. L., Jensen, R. L., & Colman, H. (2017) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-017-0722-5 · Cited by 125 · see citing works
<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
Alterations of metabolic genes and metabolites in cancer
Oermann, E. K., Wu, J., Guan, K., & Xiong, Y. (2012) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2012.01.013 · Cited by 122 · see citing works
Imaging genomics in cancer research: limitations and promises
Bai, H. X., Lee, A. M., Yang, L., Zhang, P. J., Davatzikos, C. A., Maris, J. M., & Diskin, S. J. (2016) · British Journal of Radiology · doi:10.1259/bjr.20151030 · Cited by 112 · see citing works
Zhang, J., Liu, H., Tong, H., Wang, S., Yang, Y., Liu, G., & Zhang, W. (2017) · Contrast Media & Molecular Imaging · doi:10.1155/2017/7064120 · Cited by 111 · see citing works
Juratli, T. A., Tummala, S. S., Riedl, A., Daubner, D., Hennig, S., Penson, T., Zolal, A., Thiede, C., Schackert, G., Krex, D., et al. (2018) · Journal of Neuro-Oncology · doi:10.1007/s11060-018-03034-6 · Cited by 112 · see citing works
Detection of IDH1 mutation in the plasma of patients with glioma
Boisselier, B., Pérez‐Larraya, J. G., Rossetto, M., Labussière, M., Ciccarino, P., Marie, Y., Delattre, J., & Sanson, M. (2012) · Neurology · doi:10.1212/wnl.0b013e31826e9b0a · Cited by 110 · see citing works
Salamanca-Cardona, L., Shah, H., Poot, A. J., Correa, F. M., Di Gialleonardo, V., Lui, H., Miloushev, V. Z., Granlund, K. L., Tee, S. S., Cross, J. R., et al. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.10.001 · Cited by 106 · see citing works
Imaging signatures of glioblastoma molecular characteristics: A radiogenomics review
Kazerooni, A. F., Bakas, S., Rad, H. S., & Davatzikos, C. A. (2019) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.26907 · Cited by 104 · see citing works
Lee, S., Choi, S. H., Ryoo, I., Yoon, T. J., Kim, T. M., Lee, S., Park, C., Kim, J., Sohn, C., Park, S., et al. (2014) · Journal of Neuro-Oncology · doi:10.1007/s11060-014-1614-z · Cited by 104 · see citing works
IDH inhibition in gliomas: from preclinical models to clinical trials
Rudà, R., Horbinski, C., van den Bent, M. J., Preusser, M., & Soffietti, R. (2024) · Nature Reviews Neurology · doi:10.1038/s41582-024-00967-7 · Cited by 104 · see citing works
GC/MS-based metabolomic analysis of cerebrospinal fluid (CSF) from glioma patients
Nakamizo, S., Sasayama, T., Shinohara, M., Irino, Y., Nishiumi, S., Nishihara, M., Tanaka, H., Tanaka, K., Mizukawa, K., Itoh, T., et al. (2013) · Journal of Neuro-Oncology · doi:10.1007/s11060-013-1090-x · Cited by 101 · see citing works
Conventional and advanced magnetic resonance imaging in patients with high-grade glioma
Pope, W. B., & Brandal, G. (2018) · The Quarterly Journal of Nuclear Medicine and Molecular Imaging · doi:10.23736/s1824-4785.18.03086-8 · Cited by 98 · see citing works
Self-citationGenetics and Epigenetics of Glioblastoma: Applications and Overall Incidence of IDH1 Mutation
Liu, A., Hou, C., Chen, H., Zong, X., & Zong, P. (2016) · Frontiers in Oncology · doi:10.3389/fonc.2016.00016 · Cited by 99 · see citing works
Tietze, A., Choi, C., Mickey, B., Maher, E. A., Ulhøi, B. P., Sangill, R., Lassen–Ramshad, Y., Lukacova, S., Østergaard, L., & von Öettingen, G. (2017) · Journal of neurosurgery · doi:10.3171/2016.10.jns161793 · Cited by 90 · see citing works
Hyperpolarized [1-13C] Glutamate: A Metabolic Imaging Biomarker of IDH1 Mutational Status in Glioma
Chaumeil, M. M., Larson, P. E. Z., Woods, S. M., Cai, L., Eriksson, P., Robinson, A. E., Lupo, J., Vigneron, D. B., Nelson, S. J., Pieper, R. O., et al. (2014) · Cancer Research · doi:10.1158/0008-5472.can-14-0680 · Cited by 87 · see citing works
Highly specific determination of IDH status using edited in vivo magnetic resonance spectroscopy
Branzoli, F., Stefano, A. L. D., Capelle, L., Ottolenghi, C., Valabrègue, R., Deelchand, D. K., Bielle, F., Villa, C., Baussart, B., Lehéricy, S., et al. (2017) · Neuro-Oncology · doi:10.1093/neuonc/nox214 · Cited by 88 · see citing works
Garrett, M. C., Sperry, J., Braas, D., Yan, W., Le, T. M., Mottahedeh, J., Ludwig, K., Eskin, A., Qin, Y., Levy, R., et al. (2018) · Cancer & Metabolism · doi:10.1186/s40170-018-0177-4 · Cited by 83 · see citing works
Self-citationGenetically-defined metabolic reprogramming in cancer
Mullen, A. R., & DeBerardinis, R. J. (2012) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2012.06.009 · Cited by 87 · see citing works
IDH1 R132H Mutation Generates a Distinct Phospholipid Metabolite Profile in Glioma
Esmaeili, M., Hamans, B. C., Navis, A. C., van Horssen, R., Bathen, T. F., Gribbestad, I. S., Leenders, W. P. J., & Heerschap, A. (2014) · Cancer Research · doi:10.1158/0008-5472.can-14-0008 · Cited by 86 · see citing works
MRI radiomics analysis of molecular alterations in low-grade gliomas
Shofty, B., Artzi, M., Bashat, D. B., Liberman, G., Haim, O., Kashanian, A., Bokstein, F., Blumenthal, D. T., Ram, Z., & Shahar, T. (2017) · International Journal of Computer Assisted Radiology and Surgery · doi:10.1007/s11548-017-1691-5 · Cited by 86 · see citing works
Choi, C., Ganji, S., Hulsey, K., Madan, A., Kovács, Z. Z., Dimitrov, I. E., Zhang, S., Pichumani, K., Mendelsohn, D. B., Mickey, B., et al. (2013) · NMR in Biomedicine · doi:10.1002/nbm.2943 · Cited by 83 · see citing works
Kalinina, J., Carroll, A., Wang, L., Yu, Q., Mancheno, D. E., Wu, S., Liu, F., Ahn, J. Y., He, M., Mao, H. Z., et al. (2012) · Journal of Molecular Medicine · doi:10.1007/s00109-012-0888-x · Cited by 84 · see citing works
Chen, L., Voronovich, Z. A., Clark, K., Hands, I., Mannas, J., Walsh, M., Nikiforova, M. N., Durbin, E. B., Weiss, H. L., & Horbinski, C. (2014) · Neuro-Oncology · doi:10.1093/neuonc/nou097 · Cited by 82 · see citing works
Metabolic Reprogramming in Mutant IDH1 Glioma Cells
Izquierdo-García, J. L., Viswanath, P., Eriksson, P., Chaumeil, M. M., Pieper, R. O., Phillips, J. J., & Ronen, S. M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0118781 · Cited by 84 · see citing works
Metabolic Profiling of IDH Mutation and Malignant Progression in Infiltrating Glioma
Jalbert, L. E., Elkhaled, A., Phillips, J. J., Neill, E., Williams, A. A., Crane, J. C., Olson, M. P., Molinaro, A. M., Berger, M. S., Kurhanewicz, J. V., et al. (2017) · Scientific Reports · doi:10.1038/srep44792 · Cited by 79 · see citing works
Platt, T., Ladd, M. E., & Paech, D. (2021) · Investigative Radiology · doi:10.1097/rli.0000000000000820 · Cited by 81 · see citing works
Nagashima, H., Tanaka, K., Sasayama, T., Irino, Y., Sato, N., Takeuchi, Y., Kyotani, K., Mukasa, A., Mizukawa, K., Sakata, J., et al. (2016) · Neuro-Oncology · doi:10.1093/neuonc/now090 · Cited by 76 · see citing works
The Role of Extent of Resection in IDH1 Wild-Type or Mutant Low-Grade Gliomas
Patel, T., Bander, E. D., Venn, R. A., Powell, T. M., Cederquist, G., Schaefer, P. M., Puchi, L. A., Akhmerov, A., Ogilvie, S. Q., Reiner, A. S., et al. (2017) · Neurosurgery · doi:10.1093/neuros/nyx265 · Cited by 67 · see citing works
Chaumeil, M. M., Radoul, M., Najac, C., Eriksson, P., Viswanath, P., Blough, M. D., Chesnelong, C., Luchman, H. A., Cairncross, J. G., & Ronen, S. M. (2016) · NeuroImage Clinical · doi:10.1016/j.nicl.2016.06.018 · Cited by 67 · see citing works
Jansen, R. W., van Amstel, P., Martens, R. M., Kooi, I. E., Wesseling, P., de Langen, A. J., Menke-Van der Houven van Oordt, C. W., Jansen, B. H. E., Moll, A. C., Dorsman, J. C., et al. (2018) · Oncotarget · doi:10.18632/oncotarget.24893 · Cited by 63 · see citing works
Glycine by MR spectroscopy is an imaging biomarker of glioma aggressiveness
Tiwari, V., Daoud, E. V., Hatanpaa, K. J., Gao, A., Zhang, S., An, Z., Ganji, S., Raisanen, J. M., Lewis, C. M., Askari, P., et al. (2020) · Neuro-Oncology · doi:10.1093/neuonc/noaa034 · Cited by 65 · see citing works
Diseases of the Brain, Head and Neck, Spine 2020–2023
Hodler, J., Huch, R., & von Schulthess, G. K. (2020) · IDKD Springer series · doi:10.1007/978-3-030-38490-6 · Cited by 65 · see citing works
Natsumeda, M., Igarashi, H., Nomura, T., Ogura, R., Tsukamoto, Y., Kobayashi, T., Aoki, H., Okamoto, K., Kakita, A., Takahashi, H., et al. (2014) · Acta Neuropathologica Communications · doi:10.1186/s40478-014-0158-y · Cited by 64 · see citing works
Leather, T., Jenkinson, M. D., Das, K., & Poptani, H. (2017) · Metabolites · doi:10.3390/metabo7020029 · Cited by 65 · see citing works
Batsios, G., Viswanath, P., Subramani, E., Najac, C., Gillespie, A. M., Santos, R. D., Molloy, A. R., Pieper, R. O., & Ronen, S. M. (2019) · Scientific Reports · doi:10.1038/s41598-019-47021-x · Cited by 60 · see citing works
Tan, W., Huang, W., Yin, B., Xiong, J., Wu, J., & Geng, D. (2014) · American Journal of Neuroradiology · doi:10.3174/ajnr.a3803 · Cited by 63 · see citing works
Tan, W., Xiong, J., Huang, W., Wu, J., Zhan, S., & Geng, D. (2016) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.25358 · Cited by 63 · see citing works
Isocitrate Dehydrogenase Mutations in Glioma: Genetics, Biochemistry, and Clinical Indications
Liu, Y., Lang, F., Chou, F.-J., Zaghloul, K. A., & Yang, C. (2020) · Biomedicines · doi:10.3390/biomedicines8090294 · Cited by 61 · see citing works
IDH Mutations in Tumorigenesis and Their Potential Role As Novel Therapeutic Targets
Krell, D., Mulholland, P. J., Frampton, A. E., Krell, J., Stebbing, J., & Bardella, C. (2013) · Future Oncology · doi:10.2217/fon.13.143 · Cited by 62 · see citing works
Advanced MR Techniques for Preoperative Glioma Characterization: Part 2
Hangel, G. J., Schmitz‐Abecassis, B., Sollmann, N., Pinto, J., Arzanforoosh, F., Barkhof, F., Booth, T. C., Calvo‐Imirizaldu, M., Cassia, G. D. S. E., Chmelík, M., et al. (2023) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.28663 · Cited by 60 · see citing works
From genomics to the clinic: biological and translational insights of mutant IDH1/2 in glioma
Dunn, G. P., Andronesi, O. C., & Cahill, D. P. (2013) · Neurosurgical FOCUS · doi:10.3171/2012.12.focus12355 · Cited by 59 · see citing works
IDH1/2 mutation detection in gliomas
Arita, H., Narita, Y., Yoshida, A., Hashimoto, N., Yoshimine, T., & Ichimura, K. (2014) · Brain Tumor Pathology · doi:10.1007/s10014-014-0197-x · Cited by 58 · see citing works
Mutant IDH in Gliomas: Role in Cancer and Treatment Options
Solomou, G., Finch, A., Asghar, A., & Bardella, C. (2023) · Cancers · doi:10.3390/cancers15112883 · Cited by 57 · see citing works
The clinical use of IDH1 and IDH2 mutations in gliomas
Pïcca, A., Berzero, G., Stefano, A. L. D., & Sanson, M. (2018) · Expert Review of Molecular Diagnostics · doi:10.1080/14737159.2018.1548935 · Cited by 55 · see citing works
Molecular subtypes, stem cells and heterogeneity: Implications for personalised therapy in glioma
Morokoff, A. P., Ng, W., Gogos, A., & Kaye, A. H. (2015) · Journal of Clinical Neuroscience · doi:10.1016/j.jocn.2015.02.008 · Cited by 54 · see citing works
Genotype-targeted local therapy of glioma
Shankar, G. M., Kirtane, A. R., Miller, J. J., Mazdiyasni, H., Rogner, J., Tai, T., Williams, E. A., Higuchi, F., Juratli, T. A., Tateishi, K., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1805751115 · Cited by 54 · see citing works
Elkhaled, A., Jalbert, L. E., Constantin, A., Yoshihara, H. A. I., Phillips, J. J., Molinaro, A. M., Chang, S. M., & Nelson, S. J. (2014) · NMR in Biomedicine · doi:10.1002/nbm.3097 · Cited by 52 · see citing works
Chen, R., Ravindra, V. M., Cohen, A. L., Jensen, R. L., Salzman, K. L., Prescot, A. P., & Colman, H. (2015) · Neurosurgical FOCUS · doi:10.3171/2015.1.focus14745 · Cited by 50 · see citing works
Ganji, S., An, Z., Tiwari, V., McNeil, S. S., Pinho, M. C., Pan, E., Mickey, B., Maher, E. A., & Choi, C. (2016) · Magnetic Resonance in Medicine · doi:10.1002/mrm.26190 · Cited by 50 · see citing works
Jiang, S., Wen, Z., Ahn, S. S., Cai, K., Paech, D., Eberhart, C. G., & Zhou, J. (2022) · NMR in Biomedicine · doi:10.1002/nbm.4731 · Cited by 48 · see citing works
Xin, H., Lai, Q., Zhou, Y., He, J., Song, Y., Liao, M., Sun, J., Li, M., Zhang, M., Liang, W., et al. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1134521 · Cited by 48 · see citing works
Zhou, M., Zhou, Y., Liao, H. V., Rowland, B. C., Kong, X., Arvold, N. D., Reardon, D. A., Wen, P. Y., Lin, A., & Huang, R. Y. (2018) · Neuro-Oncology · doi:10.1093/neuonc/noy022 · Cited by 48 · see citing works
Verma, G., Mohan, S., Nasrallah, M. P., Brem, S. S., Lee, J. Y. K., Chawla, S., Wang, S., Nagarajan, R., Thomas, M. A., & Poptani, H. (2016) · Journal of Translational Medicine · doi:10.1186/s12967-016-1035-1 · Cited by 47 · see citing works
Self-citationMetabolomic profiling of hormone-dependent cancers: a bird's eye view
Lloyd, S. M., Arnold, J. M., & Sreekumar, A. (2015) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2015.07.001 · Cited by 46 · see citing works
Oeltzschner, G., Saleh, M. G., Rimbault, D., Mikkelsen, M. E., Chan, K. L., Puts, N. A. J., & Edden, R. A. E. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.10.002 · Cited by 46 · see citing works
A computer-aided grading of glioma tumor using deep residual networks fusion
Tripathi, P. C., & Bag, S. (2021) · Computer Methods and Programs in Biomedicine · doi:10.1016/j.cmpb.2021.106597 · Cited by 47 · see citing works
Klink, B., Miletić, H., Stieber, D., Huszthy, P. C., Valenzuela, J. A. C., Balß, J., Wang, J., Schubert, M., Sakariassen, P. Ø., Sundstrøm, T., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0059773 · Cited by 44 · see citing works
Imaging Genomics of Glioblastoma
Elbanan, M., Amer, A. M., Zinn, P. O., & Colen, R. R. (2014) · Neuroimaging Clinics of North America · doi:10.1016/j.nic.2014.09.010 · Cited by 44 · see citing works
Magnetic Resonance (MR) Metabolic Imaging in Glioma
Chaumeil, M. M., Lupo, J., & Ronen, S. M. (2015) · Brain Pathology · doi:10.1111/bpa.12310 · Cited by 44 · see citing works
Aragón, M., Marcé, R. M., & Borrull, F. (2013) · Talanta · doi:10.1016/j.talanta.2013.07.010 · Cited by 44 · see citing works
A New Specific Succinate-Glutamate Metabolomic Hallmark in Sdhx-Related Paragangliomas
Impériale, A., Moussallieh, F., Sebag, F. A., Brunaud, L., Barlier, A., Elbayed, K., Bachellier, P., Goichot, B., Pacák, K., Namer, I. J., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0080539 · Cited by 43 · see citing works
Analyzing Tumor Metabolism In Vivo
Faubert, B., & DeBerardinis, R. J. (2016) · Annual Review of Cancer Biology · doi:10.1146/annurev-cancerbio-050216-121954 · Cited by 43 · see citing works
Verma, G., Chawla, S., Mohan, S., Wang, S., Nasrallah, M. P., Sheriff, S., Desai, A. S., Brem, S. S., O’Rourke, D. M., Wolf, R. L., et al. (2018) · NMR in Biomedicine · doi:10.1002/nbm.4042 · Cited by 43 · see citing works
Lumata, L., Yang, C., Ragavan, M., Carpenter, N., DeBerardinis, R. J., & Merritt, M. E. (2015) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/bs.mie.2015.04.006 · Cited by 42 · see citing works
Lazović, J., Soto, H., Piccioni, D. E., Ru, J. R. L., Li, S., Mirsadraei, L., Yong, W. H., Prins, R. M., Liau, L. M., Ellingson, B. M., et al. (2012) · Neuro-Oncology · doi:10.1093/neuonc/nos258 · Cited by 42 · see citing works
Self-citationBisdas, S., Chadzynski, G. L., Braun, C., Schittenhelm, J., Skardelly, M., Hagberg, G. E., Ethofer, T., Pohmann, R., Shajan, G., Engelmann, J., et al. (2016) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.25221 · Cited by 41 · see citing works
Radiomic Phenotyping in Brain Cancer to Unravel Hidden Information in Medical Images
Abrol, S., Kotrotsou, A., Salem, A., Zinn, P. O., & Colen, R. R. (2017) · Topics in Magnetic Resonance Imaging · doi:10.1097/rmr.0000000000000117 · Cited by 41 · see citing works
IDH Inhibitors and Beyond: The Cornerstone of Targeted Glioma Treatment
Gatto, L., Franceschi, E., Tosoni, A., Nunno, V. D., Maggio, I., Lodi, R., & Brandes, A. A. (2021) · Molecular Diagnosis & Therapy · doi:10.1007/s40291-021-00537-3 · Cited by 43 · see citing works
- Authors
- Pope, W. B., Prins, R. M., Albert Thomas, M., Nagarajan, R., Yen, K. E., Bittinger, M. A., Salamon, N., Chou, A. P., Yong, W. H., Soto, H., Wilson, N., Driggers, E., Jang, H. G., Su, S. M., Schenkein, D. P., Lai, A., Cloughesy, T. F., Kornblum, H. I., Wu, H., Fantin, V. R., & Liau, L. M.
- Affiliations
- University of California, Los Angeles (US)
- Agios Pharmaceuticals (United States) (US)
- Corresponding author
- Liau, Linda M.
- ORCID
- Venue
- Journal of Neuro-Oncology
- Published
- 2011-10-21
- Volume
- 107
- Issue
- 1
- Pages
- 197-205
- ISSN
- 0167-594X (ISSN-L)
- 1573-7373
- PMC
- PMC3650613
- OpenAlex
- W2083820071
- Cited by
- 318
- References
- 32
- Citations by year
- 2026: 14 · 2025: 8 · 2024: 12 · 2023: 22 · 2022: 15 · 2021: 23 · 2020: 26 · 2019: 27 · 2018: 27 · 2017: 32 · 2016: 29 · 2015: 27 · 2014: 24 · 2013: 17 · 2012: 13
- FWCI
- 8.64
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Journal of Neuro-Oncology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (UL1TR000124)
- National Cancer Institute (R01CA121131, R01CA123396, K01CA111402, R01CA112358)
- National Institute of Neurological Disorders and Stroke (R01NS052563)
- National Center for Advancing Translational Sciences
- Topics
- Health Sciences › Medicine › Genetics › Glioma Diagnosis and Treatment
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
- Keywords
- 2-hydroxyglutarate, IDH1 mutation, glioma, oncometabolites, magnetic resonance spectroscopy, non-invasive cancer detection, choline, glutathione, Ki-67 proliferation index, tumor metabolites, biomarkers
- MeSH terms
- Adult, Aged, Aged, 80 and over, Brain Neoplasms, Chromatography, Liquid, DNA, Neoplasm, Female, Follow-Up Studies, Glioma, Glutarates, Humans, Isocitrate Dehydrogenase, Magnetic Resonance Imaging, Male, Middle Aged, Mutation, Magnetic Resonance Spectroscopy, Prognosis, Prospective Studies, Mass Spectrometry, Biomarkers, Tumor, Polymerase Chain Reaction, Young Adult
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