HR-MAS NMR Based Quantitative Metabolomics in Breast Cancer
Open accessAbstract
High resolution magic-angle spinning (HR-MAS) nuclear magnetic resonance (NMR) spectroscopy is increasingly used for profiling of breast cancer tissue, delivering quantitative information for approximately 40 metabolites. One unique advantage of the method is that it can be used to analyse intact tissue, thereby requiring only minimal sample preparation. Importantly, since the method is non-destructive, it allows further investigations of the same specimen using for instance transcriptomics. Here, we discuss technical aspects critical for a successful analysis—including sample handling, measurement conditions, pulse sequences for one- and two dimensional analysis, and quantification methods—and summarize available studies, with a focus on significant associations of metabolite levels with clinically relevant parameters.
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?
SS HRMAS-NMR facilitates sample preparation and has been used for metabolomic screening of cancer tissue, neurons, metabolic syndrome, and plants.
“This facilitates the sample preparation and has been used for the metabolomic screening of, e.g., cancer tissue,136,137 metabolite screening in neurons,138 metabolic syndrome,139 plants140 or other.”
From Connecting metabolome and phenotype: recent advances in functional metabolomics tools for the identification of bioactive natural products (2024) · cites this paper as [137]
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
Molecular portraits of human breast tumours
Perou, C., Sørlie, T., Eisen, M., van de Rijn, M., Jeffrey, S., Rees, C. A., Pollack, J., Ross, D., Johnsen, H., Akslen, L., et al. (2000) · Nature · doi:10.1038/35021093 · Cited by 16,551 · see citing works
Nishimura, R., Osako, T., Nishiyama, Y., Tashima, R., Nakano, M., Fujisue, M., Toyozumi, Y., & Arima, N. (2013) · Oncology · doi:10.1159/000353099 · Cited by 13,239 · see citing works
Sørlie, T., Perou, C., Tibshirani, R., Aas, T., Geisler, S., Johnsen, H., Hastie, T., Eisen, M., van de Rijn, M., Jeffrey, S., et al. (2001) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.191367098 · Cited by 11,695 · see citing works
A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer.
Paik, S., Shak, S., Tang, G., Kim, C., Baker, J., Cronin, M., Baehner, F., Walker, M. G., Watson, D., Park, T., et al. (2004) · New England Journal of Medicine · doi:10.1056/nejmoa041588 · Cited by 6,009 · see citing works
Cortazar, P., Zhang, L., Untch, M., Mehta, K. M., Costantino, J. P., Wolmark, N., Bonnefoi, H. R., Cameron, D., Gianni, L., Valagussa, P., et al. (2014) · The Lancet · doi:10.1016/s0140-6736(13)62422-8 · Cited by 4,777 · see citing works
Supervised Risk Predictor of Breast Cancer Based on Intrinsic Subtypes
Parker, J. S., Mullins, M., Cheang, M. C. U., Leung, S. C. Y., Voduc, D. K., Vickery, T. L., Davies, S. R., Fauron, C. M. ‐., He, X., Hu, Z., et al. (2009) · Journal of Clinical Oncology · doi:10.1200/jco.2008.18.1370 · Cited by 4,737 · see citing works
Ki67 expression in breast cancer
Elkablawy, M. A., Albasri, A. M., Mohammed, R. A., Hussainy, A. S., Nouh, M. M., & Alhujaily, A. S. (2016) · Saudi Medical Journal · doi:10.15537/smj.2016.2.12285 · Cited by 4,382 · see citing works
Estimation 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
Enhancement of nuclear magnetic resonance signals by polarization transfer
Morris, G. A., & Freeman, R. (1979) · Journal of the American Chemical Society · doi:10.1021/ja00497a058 · Cited by 2,009 · see citing works
Automatic quantitation of localized in vivo1H spectra with LCModel
Provencher, S. W. (2001) · NMR in Biomedicine · doi:10.1002/nbm.698 · Cited by 1,640 · see citing works
Emerging applications of metabolomics in drug discovery and precision medicine
Wishart, D. S. (2016) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2016.32 · Cited by 1,499 · see citing works
Curigliano, G., Burstein, H. J., Winer, E. P., Gnant, M., Dubsky, P. C., Loibl, S., Colleoni, M. A., Regan, M. M., Piccart, M. J., Senn, H.-J., et al. (2017) · Annals of Oncology · doi:10.1093/annonc/mdx308 · Cited by 1,208 · see citing works
Free Induction Decays of Rotating Solids
Lowe, I. J. (1959) · Physical Review Letters · doi:10.1103/physrevlett.2.285 · Cited by 1,172 · see citing works
Palmer, A. G. I., Cavanagh, J., Wright, P. E., & Rance, M. (1991) · Journal of Magnetic Resonance (1969) · doi:10.1016/0022-2364(91)90036-s · Cited by 948 · see citing works
Filipits, M., Rudas, M., Jakesz, R., Dubsky, P. C., Fitzal, F., Singer, C. F., Dietze, O., Greil, R., Jelen, A., Sevelda, P., et al. (2011) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-11-0926 · Cited by 732 · see citing works
Removal of Dipolar Broadening of Nuclear Magnetic Resonance Spectra of Solids by Specimen Rotation
Andrew, E. R., Bradbury, A., & Eades, R. G. (1959) · Nature · doi:10.1038/1831802a0 · Cited by 713 · see citing works
Concentration Measurement by Proton NMR Using the ERETIC Method
Akoka, S., Barantin, L., & Trierweiler, M. (1999) · Analytical Chemistry · doi:10.1021/ac981422i · Cited by 520 · see citing works
Measuring Protein Concentrations by NMR Spectroscopy
Wider, G., & Dreier, L. (2006) · Journal of the American Chemical Society · doi:10.1021/ja055336t · Cited by 462 · see citing works
High-resolution magic-angle-spinning NMR spectroscopy for metabolic profiling of intact tissues
Beckonert, O. P., Coen, M., Keun, H. C., Wang, Y., Ebbels, T. M. D., Holmes, E. C., Lindon, J. C., & Nicholson, J. K. (2010) · Nature Protocols · doi:10.1038/nprot.2010.45 · Cited by 380 · see citing works
Cheng, L. L., Ma, M. J., Becerra, L. R., Ptak, T., Tracey, I., Lackner, A. A., & González, R. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.12.6408 · Cited by 339 · see citing works
Breast cancer intra-tumor heterogeneity
Martelotto, L. G., Ng, C. K. Y., Piscuoglio, S., Weigelt, B., & Reis-Filho, J. S. (2014) · Breast Cancer Research · doi:10.1186/bcr3658 · Cited by 333 · see citing works
High‐resolution magic angle spinning MRS of breast cancer tissue
Sitter, B., Sonnewald, U., Spraul, M., Fjøsne, H. E., & Gribbestad, I. S. (2002) · NMR in Biomedicine · doi:10.1002/nbm.775 · Cited by 323 · see citing works
Barker, P. B., Soher, B. J., Blackband, S. J., Chatham, J. C., Mathews, V. P., & Bryan, R. N. (1993) · NMR in Biomedicine · doi:10.1002/nbm.1940060114 · Cited by 299 · see citing works
Spin echo NMR spectra without J modulation
Aguilar, J. A., Nilsson, M., Bodenhausen, G., & Morris, G. A. (2011) · Chemical Communications · doi:10.1039/c1cc16699a · Cited by 298 · see citing works
Two-Dimensional Sideband Separation in Magic-Angle-Spinning NMR
Antzutkin, O. N., Shekar, S. C., & Levitt, M. H. (1995) · Journal of Magnetic Resonance Series A · doi:10.1006/jmra.1995.1142 · Cited by 298 · see citing works
Shabihkhani, M., Lucey, G. M., Wei, B., Mareninov, S., Lou, J. J., Vinters, H. V., Singer, E. J., Cloughesy, T. F., & Yong, W. H. (2014) · Clinical Biochemistry · doi:10.1016/j.clinbiochem.2014.01.002 · Cited by 287 · see citing works
Quantitative analysis of prostate metabolites using 1H HR‐MAS spectroscopy
Swanson, M. G., Zektzer, A. S., Tabatabai, Z. L., Simko, J., Jarso, S., Keshari, K. R., Schmitt, L., Carroll, P. R., Shinohara, K., Vigneron, D. B., et al. (2006) · Magnetic Resonance in Medicine · doi:10.1002/mrm.20909 · Cited by 250 · see citing works
Two‐dimensional J‐resolved NMR spectroscopy: review of a key methodology in the metabolomics toolbox
Ludwig, C., & Viant, M. R. (2009) · Phytochemical Analysis · doi:10.1002/pca.1186 · Cited by 238 · see citing works
Can NMR solve some significant challenges in metabolomics?
Gowda, G. A. N., & Raftery, D. (2015) · Journal of Magnetic Resonance · doi:10.1016/j.jmr.2015.07.014 · Cited by 234 · see citing works
Comparison of HR MAS MR spectroscopic profiles of breast cancer tissue with clinical parameters
Sitter, B., Lundgren, S., Bathen, T. F., Halgunset, J., Fjøsne, H. E., & Gribbestad, I. S. (2005) · NMR in Biomedicine · doi:10.1002/nbm.992 · Cited by 234 · see citing works
Solvent peak saturation with single phase and quadrature fourier transformation
Hoult, D. I. (1976) · Journal of Magnetic Resonance (1969) · doi:10.1016/0022-2364(76)90081-0 · Cited by 227 · see citing works
Cheng, L. L., Chang, I. W., Louis, D. N., & González, R. G. (1998) · PubMed · Cited by 208 · see citing works
Enhanced resolution of proton NMR spectra of malignant lymph nodes using magic‐angle spinning
Cheng, L. L., Lean, C. L., Bogdanova, A., Wright, S. C., Ackerman, J. L., Brady, T. J., & Garrido, L. (1996) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1910360502 · Cited by 195 · see citing works
Maniara, G., Rajamoorthi, K., Rajan, S. T., & Stockton, G. W. (1998) · Analytical Chemistry · doi:10.1021/ac980573i · Cited by 191 · see citing works
Keifer, P. A., Baltusis, L. M., Rice, D. M., Tymiak, A. A., & Shoolery, J. Ν. (1996) · Journal of Magnetic Resonance Series A · doi:10.1006/jmra.1996.0052 · Cited by 174 · see citing works
Cheng, L. L., Chang, I.-W., Smith, B. L., & González, R. G. (1998) · Journal of Magnetic Resonance · doi:10.1006/jmre.1998.1578 · Cited by 172 · see citing works
Recent Advances in Targeted and Untargeted Metabolomics by NMR and MS/NMR Methods
Bingol, K. (2018) · High-Throughput · doi:10.3390/ht7020009 · Cited by 172 · see citing works
Metabolic characterization of triple negative breast cancer
Cao, M. D., Lamichhane, S., Lundgren, S., Bofin, A. M., Fjøsne, H. E., Giskeødegård, G. F., & Bathen, T. F. (2014) · BMC Cancer · doi:10.1186/1471-2407-14-941 · Cited by 165 · see citing works
A new method for absolute quantitation MRS metabolites
Barantin, L., Pape, A. L., & Akoka, S. (1997) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1910380203 · Cited by 157 · see citing works
Sitter, B., Bathen, T. F., Singstad, T. E., Fjøsne, H. E., Lundgren, S., Halgunset, J., & Gribbestad, I. S. (2010) · NMR in Biomedicine · doi:10.1002/nbm.1478 · Cited by 154 · see citing works
Weybright, P., Millis, K. K., Campbell, N., Cory, D. G., & Singer, S. (1998) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1910390302 · Cited by 143 · see citing works
Quantitative NMR analysis of intra- and extracellular metabolism of mammalian cells: A tutorial
Kostidis, S., Addie, R. D., Morreau, H. M., Mayboroda, O. A., & Giera, M. A. (2017) · Analytica Chimica Acta · doi:10.1016/j.aca.2017.05.011 · Cited by 142 · see citing works
Hu, J. Z., Wang, W., Liu, F., Solum, M. S., Alderman, D. W., Pugmire, R. J., & Grant, D. M. (1995) · Journal of Magnetic Resonance Series A · doi:10.1006/jmra.1995.1082 · Cited by 141 · see citing works
Bathen, T. F., Jensen, L. R., Sitter, B., Fjøsne, H. E., Halgunset, J., Axelson, D. E., Gribbestad, I. S., & Lundgren, S. (2006) · Breast Cancer Research and Treatment · doi:10.1007/s10549-006-9400-z · Cited by 133 · see citing works
Waters, N. J., Garrod, S., Farrant, R. D., Haselden, J. N., Connor, S. C., Connelly, J. C., Lindon, J. C., Holmes, E. C., & Nicholson, J. K. (2000) · Analytical Biochemistry · doi:10.1006/abio.2000.4574 · Cited by 129 · see citing works
Multivariate Modeling and Prediction of Breast Cancer Prognostic Factors Using MR Metabolomics
Giskeødegård, G. F., Grinde, M. T., Sitter, B., Axelson, D. E., Lundgren, S., Fjøsne, H. E., Dahl, S., Gribbestad, I. S., & Bathen, T. F. (2009) · Journal of Proteome Research · doi:10.1021/pr9008783 · Cited by 128 · see citing works
Millis, K. K., Maas, W. E., Cory, D. G., & Singer, S. (1997) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1910380307 · Cited by 128 · see citing works
Moestue, S. A., Borgan, E., Huuse, E. M., Lindholm, E. M., Sitter, B., Børresen‐Dale, A., Engebraaten, O., Mælandsmo, G. M., & Gribbestad, I. S. (2010) · BMC Cancer · doi:10.1186/1471-2407-10-433 · Cited by 122 · see citing works
Cao, M. D., Sitter, B., Bathen, T. F., Bofin, A. M., Lønning, P. E., Lundgren, S., & Gribbestad, I. S. (2011) · NMR in Biomedicine · doi:10.1002/nbm.1762 · Cited by 120 · see citing works
He, Q. H., Shungu, D. C., van Zijl, P. C. M., Bhujwalla, Z. M., & Glickson, J. D. (1995) · Journal of Magnetic Resonance Series B · doi:10.1006/jmrb.1995.1035 · Cited by 117 · see citing works
Kriat, M., Sylviane Confort-gouny, A., Vion‐Dury, J., SCIAKY, M., Viout, P., & Cozzone, P. J. (1992) · NMR in Biomedicine · doi:10.1002/nbm.1940050404 · Cited by 116 · see citing works
Tzika, A. A., Cheng, L. L., Goumnerova, L., Madsen, J. R., Zurakowski, D., Astrakas, L. G., Zarifi, M. K., Scott, R. M., Anthony, D. C., González, R. G., et al. (2002) · Journal of neurosurgery · doi:10.3171/jns.2002.96.6.1023 · Cited by 113 · see citing works
Merging transcriptomics and metabolomics - advances in breast cancer profiling
Borgan, E., Sitter, B., Lingjærde, O. C., Johnsen, H., Lundgren, S., Bathen, T. F., Sørlie, T., Børresen‐Dale, A., & Gribbestad, I. S. (2010) · BMC Cancer · doi:10.1186/1471-2407-10-628 · Cited by 112 · see citing works
Prognostic value of metabolic response in breast cancer patients receiving neoadjuvant chemotherapy
Cao, M. D., Giskeødegård, G. F., Bathen, T. F., Sitter, B., Bofin, A. M., Lønning, P. E., Lundgren, S., & Gribbestad, I. S. (2012) · BMC Cancer · doi:10.1186/1471-2407-12-39 · Cited by 104 · see citing works
Magnetism in high-resolution NMR probe design. I: General methods
Doty, F. D., Entzminger, G., & Yang, Y. A. (1998) · Concepts in Magnetic Resonance · doi:10.1002/(sici)1099-0534(1998)10:3 · Cited by 103 · see citing works
Maximov, I. I., Tošner, Z., & Nielsen, N. C. (2008) · The Journal of Chemical Physics · doi:10.1063/1.2903458 · Cited by 102 · see citing works
Opstad, K. S., Bell, B. A., Griffiths, J. R., & Howe, F. A. (2008) · NMR in Biomedicine · doi:10.1002/nbm.1239 · Cited by 97 · see citing works
Classification of human liposarcoma and lipoma using ex vivo proton NMR spectroscopy
Millis, K. K., Weybright, P., Campbell, N., Fletcher, J. A., Fletcher, C. D. �., Cory, D. G., & Singer, S. (1999) · Magnetic Resonance in Medicine · doi:10.1002/(sici)1522-2594(199902)41:2 · Cited by 92 · see citing works
Barton, S. J., Howe, F. A., Tomlins, A. M., Cudlip, S., Nicholson, J. K., Bell, B. A., & Griffiths, J. R. (1999) · Magnetic Resonance Materials in Physics Biology and Medicine · doi:10.1007/bf02590529 · Cited by 86 · see citing works
Taylor, J. L., Wu, C., Cory, D. G., González, R., Bielecki, A., & Cheng, L. L. (2003) · Magnetic Resonance in Medicine · doi:10.1002/mrm.10562 · Cited by 85 · see citing works
Giskeødegård, G. F., Lundgren, S., Sitter, B., Fjøsne, H. E., Postma, G., Buydens, L. M. C., Gribbestad, I. S., & Bathen, T. F. (2012) · NMR in Biomedicine · doi:10.1002/nbm.2798 · Cited by 81 · see citing works
Bathen, T. F., Geurts, B., Sitter, B., Fjøsne, H. E., Lundgren, S., Buydens, L. M. C., Gribbestad, I. S., Postma, G., & Giskeødegård, G. F. (2013) · PLoS ONE · doi:10.1371/journal.pone.0061578 · Cited by 78 · see citing works
Metabolic clusters of breast cancer in relation to gene- and protein expression subtypes
Haukaas, T. H., Euceda, L. R., Giskeødegård, G. F., Lamichhane, S., Krohn, M., Jernström, S., Aure, M. R. R., Lingjærde, O. C., Schlichting, E., Garred, Ø., et al. (2016) · Cancer & Metabolism · doi:10.1186/s40170-016-0152-x · Cited by 76 · see citing works
Breast cancer intratumor genetic heterogeneity: causes and implications
Ng, C. K. Y., Pemberton, H. N., & Reis-Filho, J. S. (2012) · Expert Review of Anticancer Therapy · doi:10.1586/era.12.85 · Cited by 74 · see citing works
An HR-MAS MR Metabolomics Study on Breast Tissues Obtained with Core Needle Biopsy
Li, M.-L., Song, Y., Cho, N., Chang, J. M., Koo, H., Yi, A., Kim, H., Park, S., & Moon, W. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025563 · Cited by 74 · see citing works
DSA: A New Internal Standard for NMR Studies in Aqueous Solution
Nowick, J. S., Khakshoor, O., Hashemzadeh, M., & Brower, J. O. (2003) · Organic Letters · doi:10.1021/ol035347w · Cited by 74 · see citing works
Albers, M. J., Butler, T. N., Iman, R., Bao, N., Keshari, K. R., Swanson, M. G., & Kurhanewicz, J. V. (2009) · Magnetic Resonance in Medicine · doi:10.1002/mrm.21808 · Cited by 67 · see citing works
Magnetism in high-resolution NMR probe design. II: HR MAS
Doty, F. D., Entzminger, G., & Yang, Y. (1998) · Concepts in Magnetic Resonance · doi:10.1002/(sici)1099-0534(1998)10:4 · Cited by 61 · see citing works
Alum, M. F., Shaw, P. A., Sweatman, B. C., Ubhi, B. K., Haselden, J. N., & Connor, S. C. (2008) · Metabolomics · doi:10.1007/s11306-008-0103-9 · Cited by 60 · see citing works
Choi, J. S., Baek, H., Kim, S., Kim, M. J., Youk, J. H., Moon, H. J., Kim, E., Han, K., Kim, D., Kim, S. I., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0051712 · Cited by 57 · see citing works
Proton MRS of the breast in the clinical setting
Mountford, C. E., Ramadan, S. A., Stanwell, P., & Malycha, P. L. (2008) · NMR in Biomedicine · doi:10.1002/nbm.1301 · Cited by 57 · see citing works
Impact of Freezing Delay Time on Tissue Samples for Metabolomic Studies
Haukaas, T. H., Moestue, S. A., Vettukattil, R., Sitter, B., Lamichhane, S., Segura, R., Giskeødegård, G. F., & Bathen, T. F. (2016) · Frontiers in Oncology · doi:10.3389/fonc.2016.00017 · Cited by 55 · see citing works
Interplay of choline metabolites and genes in patient-derived breast cancer xenografts
Grinde, M. T., Skrbo, N., Moestue, S. A., Rødland, E. A., Borgan, E., Kristian, A., Sitter, B., Bathen, T. F., Børresen‐Dale, A., Mælandsmo, G. M., et al. (2014) · Breast Cancer Research · doi:10.1186/bcr3597 · Cited by 54 · see citing works
Martínez‐Bisbal, M. C., Monleón, D., Assemat, O., Piotto, M., Piquer, J., Llácer, J. L., & Celda, B. (2008) · NMR in Biomedicine · doi:10.1002/nbm.1304 · Cited by 51 · see citing works
Bertilsson, H., Angelsen, A., Viset, T., Skogseth, H., Tessem, M., & Halgunset, J. (2010) · The Prostate · doi:10.1002/pros.21260 · Cited by 50 · see citing works
Choi, J. S., Baek, H., Kim, S., Kim, M. J., Youk, J. H., Moon, H. J., Kim, E., & Nam, Y. K. (2013) · PLoS ONE · doi:10.1371/journal.pone.0083866 · Cited by 43 · see citing works
The effect of sample freezing on proton magic‐angle spinning NMR spectra of biological tissue
Middleton, D. A., Bradley, D. P., Connor, S. C., Mullins, P. G., & Reid, D. G. (1998) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1910400122 · Cited by 38 · see citing works
Slow-spinning low-sideband HR-MAS NMR spectroscopy: delicate analysis of biological samples
Renault, M., Shintu, L., Piotto, M., & Caldarelli, S. (2013) · Scientific Reports · doi:10.1038/srep03349 · Cited by 36 · see citing works
André, M., Dumez, J., Rezig, L., Shintu, L., Piotto, M., & Caldarelli, S. (2014) · Analytical Chemistry · doi:10.1021/ac502792u · Cited by 36 · see citing works
Adiabatic TOCSY MAS in Liquids
Kupče, Ē., Keifer, P. A., & Delepierre, M. (2001) · Journal of Magnetic Resonance · doi:10.1006/jmre.2000.2224 · Cited by 33 · see citing works
Chae, E. Y., Shin, H. J., Kim, S., Baek, H., Yoon, D., Kim, S., Shim, Y. E., Kim, H. H., Cha, J. H., Choi, W. J., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0161038 · Cited by 29 · see citing works
Gogiashvili, M., Edlund, K., Gianmoena, K., Marchan, R., Brik, A., Andersson, J. T., Lambert, J., Madjar, K., Hellwig, B., Rahnenführer, J., et al. (2016) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-016-0100-1 · Cited by 29 · see citing works
Self-citationEuceda, L. R., Haukaas, T. H., Giskeødegård, G. F., Vettukattil, R., Engel, J., Silwal‐Pandit, L., Lundgren, S., Borgen, E., Garred, Ø., Postma, G., et al. (2017) · Metabolomics · doi:10.1007/s11306-017-1168-0 · Cited by 29 · see citing works
Jordan, K. W., He, W., Halpern, E. F., Wu, C., & Cheng, L. L. (2007) · Biomarker Insights · doi:10.1177/117727190700200006 · Cited by 29 · see citing works
Gogiashvili, M., Horsch, S., Marchan, R., Gianmoena, K., Cadenas, C., Tanner, B., Naumann, S., Ersova, D., Lippek, F., Rahnenführer, J., et al. (2017) · NMR in Biomedicine · doi:10.1002/nbm.3862 · Cited by 27 · see citing works
Self-citationWieruszeski, J., Montagne, G., Chessari, G., Rousselot‐Pailley, P., & Lippens, G. M. (2001) · Journal of Magnetic Resonance · doi:10.1006/jmre.2001.2394 · Cited by 26 · see citing works
Chen, J., Enloe, B. M., Xiao, Y., Cory, D. G., & Singer, S. (2003) · Magnetic Resonance in Medicine · doi:10.1002/mrm.10569 · Cited by 25 · see citing works
High-Resolution Magic-Angle-Spinning NMR Spectroscopy of Intact Tissue
Giskeødegård, G. F., Cao, M. D., & Bathen, T. F. (2015) · Methods in molecular biology · doi:10.1007/978-1-4939-2377-9_4 · Cited by 25 · see citing works
Yoon, H., Yoon, D., Yun, M., Choi, J. S., Park, V. Y., Kim, E., Jeong, J., Koo, J. S., Yoon, J. H., Moon, H. J., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0159949 · Cited by 25 · see citing works
HR‐MAS of cells: A “cellular water shift” due to water‐protein interactions?
Aime, S., Bruno, E., Cabella, C., Colombatto, S., Digilio, G., & Mainero, V. (2005) · Magnetic Resonance in Medicine · doi:10.1002/mrm.20707 · Cited by 23 · see citing works
Jordan, K. W., He, W., Halpern, E. F., et al. (2007) · PubMed · Cited by 22 · see citing works
Ye, T., Zheng, C., Zhang, S., Gowda, G. A. N., Olga Vitek, A., & Raftery, D. (2011) · Analytical Chemistry · doi:10.1021/ac202548n · Cited by 22 · see citing works
Esmaeili, M., Bathen, T. F., Engebråten, O., Mælandsmo, G. M., Gribbestad, I. S., & Moestue, S. A. (2013) · Magnetic Resonance in Medicine · doi:10.1002/mrm.24869 · Cited by 19 · see citing works
Park, V. Y., Yoon, D., Koo, J. S., Kim, E., Kim, S. I., Choi, J. S., Park, S., Park, H. S., Kim, S., & Kim, M. J. (2016) · Medicine · doi:10.1097/md.0000000000003398 · Cited by 19 · see citing works
Metabolic Response to Everolimus in Patient-Derived Triple-Negative Breast Cancer Xenografts
Euceda, L. R., Hill, D. K., Stokke, E., Hatem, R., Botty, R. E., Bièche, I., Marangoni, E., Bathen, T. F., & Moestue, S. A. (2017) · Journal of Proteome Research · doi:10.1021/acs.jproteome.6b00918 · Cited by 19 · see citing works
Optimized selective lactate excitation with a refocused multiple-quantum filter
Holbach, M., Lambert, J., Johst, S., Ladd, M. E., & Suter, D. (2015) · Journal of Magnetic Resonance · doi:10.1016/j.jmr.2015.03.004 · Cited by 14 · see citing works
Self-citationMartin, R. W., Jachmann, R. C., Sakellariou, D., Nielsen, U. G., & Pines, A. (2005) · Magnetic Resonance in Medicine · doi:10.1002/mrm.20585 · Cited by 11 · see citing works
Optimized multiple-quantum filter for robust selective excitation of metabolite signals
Holbach, M., Lambert, J., & Suter, D. (2014) · Journal of Magnetic Resonance · doi:10.1016/j.jmr.2014.03.007 · Cited by 10 · see citing works
Self-citationPitfalls to be considered on the metabolomic analysis of biological samples by HR-MAS
Esteve, V., MartÃnez-Granados, B., & Martínez‐Bisbal, M. C. (2014) · Frontiers in Chemistry · doi:10.3389/fchem.2014.00033 · Cited by 10 · see citing works
A two-dimensional NMR experiment for the correlation of spin-locked and free-precession frequencies
Ravikumar, M., & Bothner‐By, A. A. (1993) · Journal of the American Chemical Society · doi:10.1021/ja00069a077 · Cited by 6 · see citing works
Prognostic gene expression assays in breast cancer: are two better than one?
Sparano, J. A. (2018) · npj Breast Cancer · doi:10.1038/s41523-018-0063-9 · Cited by 6 · see citing works
Righi, V., Schenetti, L., Maiorana, A., Libertini, E., Bettelli, S. R., Bonetti, L. R., & Mucci, A. (2014) · Metabolomics · doi:10.1007/s11306-014-0709-z · Cited by 3 · see citing works
Flagged first, then by citations
2 of the 104 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Analytical Techniques for Metabolomic Studies: A Review
Segers, K., Declerck, S., Mangelings, D., Heyden, Y. V., & Eeckhaut, A. V. (2019) · Bioanalysis · doi:10.4155/bio-2019-0014 · Cited by 230 · see citing works
Quantitative NMR-Based Biomedical Metabolomics: Current Status and Applications
Crook, A. A., & Powers, R. (2020) · Molecules · doi:10.3390/molecules25215128 · Cited by 183 · see citing works
Phosphatidylcholine-Derived Lipid Mediators: The Crosstalk Between Cancer Cells and Immune Cells
Saito, R. D. F., Andrade, L. N. D. S., Bustos, S. O., & Chammas, R. J. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.768606 · Cited by 183 · see citing works
Metabolomics as a tool for the early diagnosis and prognosis of diabetic kidney disease
Pereira, P., Carrageta, D. F., Oliveira, P. F., Rodrigues, A. S., Alves, M. G., & Monteiro, M. P. (2022) · Medicinal Research Reviews · doi:10.1002/med.21883 · Cited by 167 · see citing works
Letertre, M. P. M., Giraudeau, P., & Tullio, P. D. (2021) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2021.698337 · Cited by 147 · see citing works
Vitale, G. A., Geibel, C., Minda, V., Wang, M., Aron, A. T., & Petras, D. (2024) · Natural Product Reports · doi:10.1039/d3np00050h · Cited by 66 · see citing works
Silva, A., Cardoso, M. R., Rezende, L. M., Lin, J. Q., Guimarães, F., Silva, G. R. D. P., Murgu, M., Priolli, D. G., Eberlin, M. N., Tata, A., et al. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21103611 · Cited by 39 · see citing works
Grading of endometrial cancer using 1H HR-MAS NMR-based metabolomics
Skorupa, A., Poński, M., Ciszek, M., Cichoń, B., Klimek, M. M., Witek, A., Pakuło, S., Boguszewicz, Ł., & Sokol, M. B. (2021) · Scientific Reports · doi:10.1038/s41598-021-97505-y · Cited by 33 · see citing works
Metabolomics and metabolites in cancer diagnosis and treatment
Cai, M., Liu, H., Shao, C., Li, T., Jin, J., Liang, Y., Wang, J., Cao, J., Yang, B. K., He, Q., et al. (2025) · Molecular Biomedicine · doi:10.1186/s43556-025-00362-8 · Cited by 32 · see citing works
Yao, C., Qi, L., Zhong, F., Li, N., & Ma, Y. (2021) · Journal of Chromatography B · doi:10.1016/j.jchromb.2021.123056 · Cited by 31 · see citing works
Cakmakci, D., Karakaslar, E. O., Ruhland, E., Chenard, M., Proust, F., Piotto, M., Namer, I. J., & Çiçek, A. E. (2020) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1008184 · Cited by 24 · see citing works
Annunziato, M., Eeza, M. N. H., Bashirova, N., Lawson, A., Matysik, J., Benetti, D. D., Grosell, M., Stieglitz, J. D., Alia, A., & Berry, J. P. (2021) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2021.149858 · Cited by 24 · see citing works
NMR spectroscopy as a “green analytical method” in metabolomics and proteomics studies
Mielko, K. A., Pudełko‐Malik, N., Tarczewska, A., & Młynarz, P. (2021) · Sustainable Chemistry and Pharmacy · doi:10.1016/j.scp.2021.100474 · Cited by 23 · see citing works
Ali, S., Rech, K. S., Badshah, G., Soares, F. L. F., & Barison, A. (2021) · Journal of Natural Products · doi:10.1021/acs.jnatprod.0c01094 · Cited by 18 · see citing works
Alwahsh, M., Knitsch, R., Marchan, R., Lambert, J., Hoerner, C., Zhang, X.-N., Schalke, B. C. G., Lee, D.-H., Bulut, E. L., Graeter, T. P., et al. (2022) · Cancers · doi:10.3390/cancers14061564 · Cited by 18 · see citing works
Self-citationThe magic angle view to food: magic-angle spinning (MAS) NMR spectroscopy in food science
Jensen, H. M., & Bertram, H. C. (2019) · Metabolomics · doi:10.1007/s11306-019-1504-7 · Cited by 16 · see citing works
Metabolomic analysis of endometrial cancer by high-resolution magic angle spinning NMR spectroscopy
Düz, S. A., Mumcu, A., Doğan, B., Yılmaz, E., Çoşkun, E. İ., Sarıdogan, E., Tuncay, G., & Karaer, A. (2022) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-022-06587-0 · Cited by 14 · see citing works
Bitencourt, A. G. V., Goldberg, J., Pinker, K., & Thakur, S. B. (2019) · Metabolomics · doi:10.1007/s11306-019-1611-5 · Cited by 13 · see citing works
Wang, S., Shi, W., Guo, P., Liu, H., Feng, J., & Huang, H. (2020) · Journal of Pharmaceutical and Biomedical Analysis · doi:10.1016/j.jpba.2020.113546 · Cited by 11 · see citing works
Metabolomics techniques: A brief update
Tyagi, R., Kumar, P., & Sharma, U. (2021) · Elsevier eBooks · doi:10.1016/b978-0-323-85652-2.00007-5 · Cited by 10 · see citing works
Kaynar, G., Cakmakci, D., Bund, C., Todeschi, J., Namer, I. J., & Çiçek, A. E. (2023) · Bioinformatics · doi:10.1093/bioinformatics/btad684 · Cited by 10 · see citing works
Eeza, M. N. H., Singer, R., Höfling, C., Matysik, J., de Groot, H. J. M., Roβner, S., & Alia, A. (2021) · Journal of Alzheimer s Disease · doi:10.3233/jad-201575 · Cited by 9 · see citing works
Al-Douri, N. A., Al-Jaidi, B. A., Hammad, H. M., Shakya, A. K., Alkhalailah, T. J. M., Shilbayeh, S. A. R., Ibrahim, A. A. M., Venugopala, K. N., & Kamal, Y. T. (2022) · Indian Journal of Pharmaceutical Education and Research · doi:10.5530/ijper.56.3s.156 · Cited by 8 · see citing works
Skorupa, A., Ciszek, M., Turska-d’Amico, M., Stobiecka, E., Chmielik, E., Szumniak, R., d’Amico, A., Boguszewicz, Ł., & Sokol, M. B. (2023) · Cancers · doi:10.3390/cancers15041283 · Cited by 8 · see citing works
Eraslan, Z., Cascante, M., & Günther, U. L. (2022) · Handbook of experimental pharmacology · doi:10.1007/164_2022_619 · Cited by 8 · see citing works
Migdadi, L., Telfah, A., Hergenröder, R., & Wöhler, C. (2022) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2022.05.050 · Cited by 7 · see citing works
Self-citationNuclear Magnetic Resonance Based Metabolomics—A Rising Star in Traditional Chinese Medicine Research
Hu, Y., Liu, L., Yan, G., Bai, L., Yang, L., Kong, L. D., Sun, H., Liu, C., Sun, Y., Han, Y., et al. (2025) · Pharmaceuticals · doi:10.3390/ph18081186 · Cited by 6 · see citing works
Hameed, R., Naseer, A., Saxena, A., Akbar, M., Toppo, P., Sarkar, A., Shukla, S. K., & Nazir, A. (2024) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-024-05179-2 · Cited by 6 · see citing works
Düz, S. A., Mumcu, A., Doğan, B., Sarıdoğan, E., Tuncay, G., Onat, T., & Karaer, A. (2025) · Analytical Biochemistry · doi:10.1016/j.ab.2025.115885 · Cited by 5 · see citing works
Nuclear magnetic resonance in metabolomics
Emwas, A.-H. M., Szczepski, K., Poulson, B. G., McKay, R. T., Tenori, L., Saccenti, E., Lachowicz, J. I., & Jaremko, M. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-85062-9.00005-2 · Cited by 5 · see citing works
Nuclear Magnetic Resonance Spectroscopy in Analyses of Biological Samples
Stanišić, D., Martins, L. G., & Tasić, L. (2021) · Springer eBooks · doi:10.1007/978-3-030-82381-8_9 · Cited by 5 · see citing works
Targeted metabolomics analyses for brain tumor margin assessment during surgery
Cakmakci, D., Kaynar, G., Bund, C., Piotto, M., Proust, F., Namer, I. J., & Çiçek, A. E. (2022) · Bioinformatics · doi:10.1093/bioinformatics/btac309 · Cited by 4 · see citing works
García-Mañas, C., Montes, M. D. J., Abreu, A. C., Maresca, M. Á. R., Fernández, I., & Alonso, A. M. F. (2026) · PLoS ONE · doi:10.1371/journal.pone.0339292 · Cited by 2 · see citing works
Bahti, A., Telfah, A., Hergenröder, R., & Suter, D. (2025) · Analytical Chemistry · doi:10.1021/acs.analchem.3c05226 · Cited by 2 · see citing works
Self-citationMumcu, A. (2021) · Journal of the Turkish Chemical Society Section A Chemistry · doi:10.18596/jotcsa.986523 · Cited by 2 · see citing works
Sivanesan, I., Kannan, E. P., Venkatachalam, P., Ortiz, C. T., Gopal, J., & Muthu, M. (2025) · TrAC Trends in Analytical Chemistry · doi:10.1016/j.trac.2025.118492 · Cited by 1 · see citing works
Phenotype Classification of Intact Cells by NMR Spectroscopy through Machine Learning Approaches
Mengucci, C., Dell’Amico, C., Giudice, S. D., Barbieri, L., Mariottini, A., Onorati, M., Massacesi, L., Luchinat, E., & Banci, L. (2026) · Journal of the American Chemical Society · doi:10.1021/jacs.6c01100 · Cited by 1 · see citing works
NMR-Based Mitochondria Metabolomic Profiling: A New Approach To Reveal Cancer-Associated Alterations
Domingo-Ortí, I., Ferrer-Torres, P., Armiñán, A., Vicent, M. J., Pineda‐Lucena, A., & Palomino‐Schätzlein, M. (2023) · Analytical Chemistry · doi:10.1021/acs.analchem.3c02432 · Cited by 1 · see citing works
Liu, H., Wang, Y., Han, Y.-Q., Yang, G., Wang, L., Jin, P., Liang, H., Huang, H., Deng, P., Lu, C. D., et al. (2021) · Research Square · doi:10.21203/rs.3.rs-753667/v1
Presset, A. (2022) · theses.fr (ABES) · doi:10.70675/dcdf978cz83d8z4a59z99afzcc06e380823b
Gdowicz‐Kłosok, A., Boguszewicz, Ł., Skorupa, A., Ciszek, M., Turska-d’Amico, M., Krześniak, M., Łasut-Szyszka, B., Sokól, M., & Wydmański, J. (2026) · Scientific Reports · doi:10.1038/s41598-026-58204-8
Use of Nuclear Magnetic Resonance (NMR) to Study Cancer Metabolism
Freitas-Dias, C., & Gonçalves, L. G. (2026) · Advances in experimental medicine and biology · doi:10.1007/978-3-032-12166-0_18
NMR spectroscopy for precision medicine and clinical translation
Gupta, U., Mishra, J., Singh, A., Pandey, S., Marwari, D., Siddiqui, M. A., & Sinha, N. (2026) · Annual reports on NMR spectroscopy · doi:10.1016/bs.arnmr.2026.04.003
GarcÃa-Bocanegra, I., Urbano‐Gámez, J. D., Pérez-Cardona, A., Barrios, L., Somoza‐Ramírez, M. I., Vicioso, L., Susacasa, E. P., Córdoba, G. D., Acebal‐Blanco, M. M., Sendra‐Portero, F., et al. (2026) · NMR in Biomedicine · doi:10.1002/nbm.70386
- Authors
- Gogiashvili, M., Nowacki, J., Hergenröder, R., Hengstler, J. G., Lambert, J., & Edlund, K.
- Affiliations
- Leibniz Institute for Analytical Sciences - ISAS (DE)
- Leibniz Research Centre for Working Environment and Human Factors (DE)
- Corresponding author
- Gogiashvili, Mikheil
- ORCID
- Venue
- Metabolites
- Publisher
- MDPI AG
- Published
- 2019-01-22
- Volume
- 9
- Issue
- 2
- Pages
- 19
- ISSN
- 2218-1989 (ISSN-L)
- PMC
- PMC6410210
- OpenAlex
- W2911544468
- Cited by
- 44
- References
- 104
- Citations by year
- 2026: 5 · 2025: 5 · 2024: 2 · 2023: 3 · 2022: 10 · 2021: 12 · 2020: 4 · 2019: 3
- FWCI
- 0.64
- Type
- journal article
- Language
- en
- Open access
- gold
- dx.doi.org
- Licence
- Locations
- Metabolites (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Technische Universität Dortmund Eldorado (Technische Universität Dortmund) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Informationszentrum Lebenswissenschaften (ZB MED) (submittedVersion, cc-by)
- Technische Universität Dortmund Eldorado (Technische Universität Dortmund) (cc-by)
- Funders
- Bundesministerium für Bildung und Forschung
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolomics and Mass Spectrometry Studies
- Physical Sciences › Chemistry › Spectroscopy › Advanced NMR Techniques and Applications
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced MRI Techniques and Applications
- Keywords
- breast cancer, quantitative metabolomics, sample handling, pulse sequences, metabolite quantification
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
