J Appl Biomed 13:69-78, 2015 | DOI: 10.1016/j.jab.2014.10.002

Multinuclear magnetic resonance evaluation of tumor tissue

Dorota Bartusika,*, David Aebisherb
a Southern Polytechnic State University, Department of Biology and Chemistry, Marietta, GA 30060, USA
b Shorter University, Natural Sciences Department, Rome, GA 30165, USA

Current biomedical research requires quantitative and qualitative studies of tissue metabolites. In this review, we discuss recent advances in multinuclear magnetic resonance (MR) technology that enhance biomedical research. The advances presented herein clearly show that MR is a diagnostic tool for the study of tumor tissue metabolism associated with changes in small molecule concentrations. Biomedical MR offers a non-invasive view of cancer cell metabolism by detection of resonance nuclei such as hydrogen-1, carbon-13, phosphorus-31 and fluorine-19. Due to current progress in MR technology, it is now possible to monitor changes in cancer cell metabolism before and after therapy.
Our criteria for the selection of research papers for this review were focused on those that show progress in biomedicine achieved by using MR. Our review demonstrates that small molecule detection in cancer tissue by MR has advanced biomedical research allowing for significant improvements in tumor detection and treatment.

Keywords: Cancer; Magnetic resonance imaging; Magnetic resonance spectroscopy; Cellular metabolism; Multimodal magnetic resonance

Received: July 7, 2014; Revised: October 20, 2014; Accepted: October 22, 2014; Published: May 1, 2015  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Bartusik D, Aebisher D. Multinuclear magnetic resonance evaluation of tumor tissue. J Appl Biomed. 2015;13(2):69-78. doi: 10.1016/j.jab.2014.10.002.
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Aboagye, E.O., Bhujwalla, Z.M., 1999. Malignant transformation alters membrane choline phospholipid metabolism of human mammary epithelial cells. Cancer Res. 59, 80-84.
    2. Abragam, A., Goldman, M., 1987. Principles of dynamic nuclear polarization. Rep. Prog. Phys. 41, 395-467. Go to original source...
    3. Abramov, Y., Carmi, S., Cohen, J.S., Anteby, S.O., Ringel, I., 2012. 31 P-magnetic resonance spectra of ovarian cancer cells exposed to chemotherapy within a three-dimensional Matrigel construct. Oncol. Rep. 2, 735-741. Go to original source... Go to PubMed...
    4. Adams, R.W., Aguilar, J.A., Atkinson, K.D., Cowley, M.J., Elliott, P. I., Duckett, S.B., Green, G.G., Khazal, I.G., Lopez-Serrano, J., Williamson, D.C., 2009. Reversible interactions with parahydrogen enhance NMR sensitivity by polarization transfer. Science 323, 1708-1711. Go to original source... Go to PubMed...
    5. Albert, M.S., Cates, G.D., Drienhuys, B., Rapper, W., Saam, B., Springer, O.S., Wishnia, A., 1994. Biological magnetic resonance imaging using laser polarized 129Xe. Nature 370, 199-201. Go to original source... Go to PubMed...
    6. Al-Saffar, N.M., Marshall, L.V., Jackson, L.E., Balarajah, G., Eykyn, T.R., Agliano, A., Clarke, P.A., Jones, C., Workman, P., Pearson, A.D., Leach, M.O., 2014. Lactate and choline metabolites detected in vitro by nuclear magnetic resonance spectroscopy are potential metabolic biomarkers for PI3K Inhibition in pediatric glioblastoma. PLoS ONE 9, e103835. Go to original source... Go to PubMed...
    7. Ardenkjaer-Larsen, J.H., Fridlund, B., Gram, A., Hansson, G., Hansson, L., Lerche, M.H., Servin, R., Thaning, M., Golman, K., 2003. Proc. Natl. Acad. Sci. U.S.A. 100, 10158-10163. Go to original source... Go to PubMed...
    8. Bartella, L., Thakur, S.B., Morris, E.A., Dershaw, D.D., Huang, W., Chough, E., Cruz, M.C., Liberman, L., 2007. Enhancing nonmass lesions in the breast: evaluation with proton 1H MR spectroscopy. Radiology 245, 80-87. Go to original source... Go to PubMed...
    9. Bartusik, D., Tomanek, B., Siluk, D., Kaliszan, R., 2010. 19F MRI of 3D CEM cells to study the effects of tocopherols and tocotrienols. J. Pharm. Biomed. Anal. 53, 599-602. Go to original source... Go to PubMed...
    10. Bartusik, D., Tomanek, B., 2010a. Detection of fluorine labeled Herceptin using cellular 19F MRI ex vivo. J. Pharm. Biomed. Anal. 51, 894-900. Go to original source... Go to PubMed...
    11. Bartusik, D., Tomanek, B., 2010b. Application of 19F magnetic resonance to study the efficacy of fluorine labeled drugs in the three-dimensional cultured. Arch. Biochem. Biophys. 493, 234-241. Go to original source... Go to PubMed...
    12. Beckonert, O., Monnerjahn, J., Bonk, U., Leibfritz, D., 2003. Visualizing metabolic changes in breast-cancer tissue using 1 H-NMR spectroscopy and self-organizing maps. NMR Biomed. 23, 1-11. Go to original source... Go to PubMed...
    13. Befroy, D.E., Rothman, D.L., Petersen, K.F., Shulman, G.I., 2012. 31 P-magnetization transfer magnetic resonance spectroscopy measurements of in vivo metabolism. Diabetes 61, 1927-1934. Go to original source... Go to PubMed...
    14. Bernstein, M.A., King, K.F., Zhou, X.J., 2004. Handbook of MRI Pulse Sequences. Elsevier Academic Press, New York, NY, USA. Go to original source...
    15. Cecil, K.M., Schnall, M.D., Siegelman, E.S., Lenkinski, R.E., 2001. The evaluation of human breast lesions with magnetic resonance imaging and proton magnetic resonance spectroscopy. Breast Cancer Res. Treat. 68, 45-54. Go to original source... Go to PubMed...
    16. Chen, A.P., Albers, M.J., Cunningham, C.H., Kohler, S.J., Yen, Y.F., Hurd, R.E., Tropp, J., Bok, R., Pauly, J.M., Nelson, S.J., Kurhanewicz, J., Vigneron, D.B., 2007. Hyperpolarized C-13 spectroscopic imaging of the TRAMP mouse at 3T-initial experience. Magn. Reson. Med. 58, 1099-1106. Go to original source... Go to PubMed...
    17. Chen, A.P., Kurhanewicz, J., Bok, R., Xu, D., Joun, D., Zhang, V., Nelson, S.J., Hurd, R.E., Vigneron, D.B., 2008. Feasibility of using hyperpolarized [1-13C] lactate as a substrate for in vivo metabolic 13C MRSI studies. Magn. Reson. Imaging 26, 721-726. Go to original source... Go to PubMed...
    18. Chen, J.H., Enloe, B.M., Weybright, P., Campbell, N., Dorfman, D., Fletcher, C.D., Cory, D.G., Singer, S., 2002. Biochemical correlates of thiazolidinedione-induced adipocyte differentiation by high-resolution magic angle spinning NMR spectroscopy. Magn. Reson. Med. 48, 602-610. Go to original source... Go to PubMed...
    19. Chen, R., Yu, H., An, Y.L., Yu-Jia, Z., Teng, G.J., 2014. Genetic immunotherapy for hepatocellular carcinoma by endothelial progenitor cells armed with cytosine deaminase. J. Biomed. Nanotechnol. 10, 271-277. Go to original source... Go to PubMed...
    20. Chen, W., Zu, Y., Huang, Q., Chen, F., Wang, G., Lan, W., Bai, C., Lu, S., Yue, Y., Deng, F., 2011. Study on metabonomic characteristics of human lung cancer using high resolution magic-angle spinning 1H NMR spectroscopy and multivariate data analysis. Magn. Reson. Med. 66, 1531-1540. Go to original source... Go to PubMed...
    21. Cheng, L.L., Chang, B.L., Smith, R.G., Gonzalez, J., 1998. Evaluating human breast ductal carcinomas with highresolution magic-angle spinning proton magnetic resonance spectroscopy. Magn. Reson. 135, 194-202. Go to original source... Go to PubMed...
    22. Cheng, L.L., Burns, M.A., Taylor, J.L., He, W., Halpern, E.F., McDougal, W.S., Wu, C.L., 2005. Metabolic characterization of human prostate cancer with tissue magnetic resonance spectroscopy. Cancer Res. 65, 3030-3034. Go to original source... Go to PubMed...
    23. Comment, A., van den Brandt, B., Uffmann, K., Kurdzesau, F., Jannin, S., Konter, J.A., Hautle, P., Wenckebach, W.T., Gruetter, R., van der Klink, J.J., 2007. Design and performance of a DNP prepolarizer coupled to a rodent MRI scanner. Concepts Magn. Reson. B 31, 255-269. Go to original source...
    24. Cox, I.J., Bell, J.D., Peden, C.J., Iles, R.A., Foster, C.S., Watanapa, P., Williamson, R.C., 1992. In vivo and in vitro 31P magnetic resonance spectroscopy of focal hepatic malignancies. NMR Biomed. 5, 114-120. Go to original source... Go to PubMed...
    25. Damadian, R., Goldsmith, M., Minkoff, L., 1977. NMR in cancer: XVI. Fonar image of the live human body. Physiol. Chem. Phys. 9, 97-100.
    26. Day, S.E., Kettunen, M.I., Gallagher, F.A., Hu, D.E., Lerche, M., Wolber, J., Golman, K., Ardenkjaer-Larsen, J.H., Brindle, K.M., 2007. Detecting tumor response to treatment using hyperpolarized 13C magnetic resonance imaging and spectroscopy. Nat. Med. 13, 1382-1387. Go to original source... Go to PubMed...
    27. Degani, H., Horowitz, A., Itzchak, Y., 1986. Breast tumors: evaluation with P-31 MR spectroscopy. Radiology 161, 53-55. Go to original source... Go to PubMed...
    28. Degani, H., Ronen, S.M., Furman-Haran, E., 1994. Breast cancer: spectroscopy and imaging of cells and tumors. In: Gillies, R.J. (Ed.), NMR in Physiology and Biomedicine. Academic Press, San Diego, pp. 329-352. Go to original source...
    29. Fox, M.S., Ouriado, A., Thind, K., Hegarty, E., Wong, E., Hope, A., Santyr, G.E., 2014. Detection of radiation induced lung injury in rats using dynamic hyperpolarized 129Xe magnetic resonance spectroscopy. Med. Phys. 41, 072302. Go to original source... Go to PubMed...
    30. Friesen-Waldner, L.J., Wade, T.P., Thind, K., Chen, A.P., Gomori, J.M., Sosna, J., McKenzie, C.A., Katz-Brull, R., 2014. Hyperpolarized choline as an MR imaging molecular probe: feasibility of in vivo imaging in a rat model. J. Magn. Reson. Imaging (Epub ahead of print). Go to original source... Go to PubMed...
    31. Gallagher, F.A., Kettunen, M.I., Hu, D.E., Jensen, P.R., Zandt, R., Karlsson, M., Gisselsson, A., Nelson, S.K., Golman, K., Zandt, R., Lerche, M., Perhson, R., Ardenkjaer-Larsen, H., 2006. Metabolic imaging by hyperpolarized 13C magnetic resonance imaging for in vivo tumor diagnosis. Cancer Res. 66, 10855-10860. Go to original source... Go to PubMed...
    32. Gallagher, F.A., Kettunen, M.I., Day, S.E., Hu, D.E., ArdenkjaerLarsen, J.H., Zandt, R., Jensen, P.R., Karlsson, M., Golman, K., Lerche, M.H., Brindle, K.M., 2008. Magnetic resonance imaging of pH in vivo using hyperpolarized 13C-labelled bicarbonate. Nature 453, 940-943. Go to original source... Go to PubMed...
    33. Gallagher, F.A., Kettunen, M.I., Hu, D.E., Jensen, P.R., Zandt, R., Karlsson, M., Gisselsson, A., Nelson, S.K., Witney, T.H., Bohndiek, S.E., Hansson, G., Peitersen, T., Lerche, M.H., Brindle, K.M., 2009. Production of hyperpolarized [1,4-13C2] malate from [1,4-13C2] fumarate is a marker of cell necrosis an treatment response in tumors. Proc. Natl. Acad. Sci. U.S.A. 106, 19801-19806. Go to original source... Go to PubMed...
    34. Gillies, R.J., Bhujwalla, Z.M., Evelhoch, J., Garwood, M., Neeman, M., Robinson, S.P., Sotak, C.H., Van der Sanden, B., 2000. Applications of magnetic resonance in model systems: tumor biology and physiology. Neoplasia 2, 139-151. Go to original source... Go to PubMed...
    35. Gillies, R.J., Morse, D.L., 2005. In vivo magnetic resonance spectroscopy in cancer. Ann. Rev. Biomed. Eng. 7, 287-326. Go to original source... Go to PubMed...
    36. Gomez-Iturriaga, A., Crook, J., Casquero, F., Carvajal, C., Urresola, A., Canteli, B., Ezquerro, A., Hortelano, E., Cacicedo, J., Espinosa, J.M., Perez, F., Minguez, P., Bilbao, P., 2014. Impact of intraoperative MRI/TRUS fusion on dosimetric parameters in cT3a prostate cancer patients treated with high-dose-rate real-time brachytherapy. J. Contemp. Brachytherapy 6, 154-160. Go to original source... Go to PubMed...
    37. Goodson, B.M., 2002. Nuclear magnetic resonance of laserpolarized noble gases in molecules, materials, and organisms. J. Magn. Reson. 155, 157-216. Go to original source... Go to PubMed...
    38. Gribbestad, I.S., Fjosne, H.E., Haugen, O.A., Nilsen, G., Krane, J., Petersen, S.B., Kvinnsland, S., 1993. In vitro proton NMR spectroscopy of extracts from human breast tumours and non-involved breast tissue. Anticancer Res. 13, 1973-1980.
    39. Gribbestad, I.S., Petersen, S.B., Fjosne, H.E., Kvinnsland, S., Krane, J., 1994. 1H NMR spectroscopic characterization of perchloric acid extracts from breast carcinomas and noninvolved breast tissue. NMR Biomed. 7, 181-194. Go to original source... Go to PubMed...
    40. Gribbestad, I.S., Sitter, B., Lundgren, S., Krane, J., Axelson, D., 1999. Metabolite composition in breast tumors examined by proton nuclear magnetic resonance spectroscopy. Anticancer Res. 99, 1736-1737.
    41. Griffiths, J.R., Glickson, J.D., 2000. Monitoring pharmacokinetics of anticancer drugs: non-invasive investigation using magnetic resonance spectroscopy. Adv. Drug Deliv. Rev. 41, 75-89. Go to original source... Go to PubMed...
    42. Haddadin, I.S., McIntosh, A., Meisamy, S., Corum, C., Styczynski, Snyder, A.L., Powell, N.J., Nelson, M.T., Yee, D., Garwood, M., Bolan, P.J., 2009. Metabolite quantification and high-field MRS in breast cancer. NMR Biomed. 22, 65-76. Go to original source... Go to PubMed...
    43. Harris, T., Degani, H., Frydman, L., 2013. Hyperpolarized 13C NMR studies of glucose metabolism in living breast cancer cell cultures. NMR Biomed. 26, 1831-1843. Go to original source... Go to PubMed...
    44. Hersman, F.W., Ruset, I.C., Ketel, S., Muradian, I., Covrig, S.D., Distelbrink, J., Porter, W., Watt, D., Ketel, J., Brackett, J., Hope, A., Patz, S., 2008. Large production system for hyperpolarized 129Xe for human lung imaging studies. Acad. Radiol. 15, 292-683. Go to original source... Go to PubMed...
    45. Heywang, S.H., Hahn, D., Schmid, H., Krischke, I., Eiermann, W., Bassermann, R., Lissner, J., 1986. MR imaging of the breast using gadolinium-DTPA. J. Comput. Assist Tomogr. 10, 199-204. Go to original source... Go to PubMed...
    46. Hunjan, S., Zhao, D., Canstandtinescu, A., Hahan, E.W., Antich, P.P., Mason, R.P., 2001. Tumor oximetry: demonstration of an enhanced dynamic mapping procedure using fluorine-19 echo planar magnetic resonance imaging in the Dunning prostate R3327-AT1 rat tumor. Int. J. Radiat. Biol. Phys. 49, 1097-1108. Go to original source... Go to PubMed...
    47. Jagannathan, N.R., Kumar, M., Seenu, V., Coshic, O., Dwivedi, S. N., Julka, P.K., Srivastava, A., Rath, G.K., 2001. Evaluation of total choline from in-vivo volume localized proton MR spectroscopy and its response to neoadjuvant chemotherapy in locally advanced breast cancer. Br. J. Cancer 84, 1016-1022. Go to original source... Go to PubMed...
    48. Jensen, P.R., Karlsson, M., Meier, S., Duus, M.O., Lerche, M.H., 2009. Hyperpolarized amino acids for in vivo assays of transaminase activity. Chem. Eur. J. 15, 10010-10012. Go to original source... Go to PubMed...
    49. Jiang, Z.X., Feng, Y., Yu, B.Y., 2011. Fluorinated paramagnetic chelates as potential multi-chromic 19F tracer agents. Chem. Commun. 4, 7233-7235. Go to original source... Go to PubMed...
    50. Joseph, P.M., Fishman, J.E., Mukherji, B., Sloviter, H.A.J., 1985. In vivo 19F NMR imaging of the cardiovascular system. Comput. Assisted Tomogr. 9, 1012-1029. Go to original source... Go to PubMed...
    51. Jung, J., Jung, Y., Bang, E.J., Cho, S.I., Jang, Y.J., Kwak, J.M., Ryu, D. H., Park, S., Hwang, G.S., 2014. Noninvasive diagnosis and evaluation of curative surgery for gastric cancer by using NMR-based metabolomic profiling. Ann. Surg. Oncol., http://dx.doi.org/10.1245/s10434-014-3886-0. Go to original source... Go to PubMed...
    52. Kalra, R., Wade, K.E., Hands, L., Styles, P., Camplejohn, R., Greenall, M., Adams, G.E., Harris, A.L., Radda, G.K., 1993. Phosphomonoester is associated with proliferation in human breast cancer: a 31P MRS study. Br. J. Cancer 67, 1145-1153. Go to original source... Go to PubMed...
    53. Katz-Brull, R., Seger, D., Rivenson-Segal, D., Rushkin, E., Degani, H., 2002. Metabolic markers of breast cancer: enhanced choline metabolism and reduced choline-etherphospholipid synthesis. Cancer Res. 62, 1966-1970.
    54. Keshari, K.R., Wilson, D.M., 2014. Chemistry and biochemistry of 13 C hyperpolarized magnetic resonance using dynamic nuclear polarization. Chem. Soc. Rev. 43, 1627-1659. Go to original source... Go to PubMed...
    55. Kobus, T., Bitz, A.K., van Uden, M.J., Lagemaa, M.W., Rothgang, E., Orzada, S., Heerschap, A., Scheenen, T.W., 2012. In vivo 31P MR spectroscopic imaging of the human prostate at 7 T: safety and feasibility. Magn. Reson. Med. 68, 1683-1695. Go to original source... Go to PubMed...
    56. 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., 2011. Analysis of cancer metabolism by imaging hyperpolarized nuclei: prospects for translation to clinical research. Neoplasia 13, 81-97. Go to original source... Go to PubMed...
    57. Lauterbur, P.C., 1974. Magnetic resonance zeugmatography. Pure Appl. Chem. 40, 149-157. Go to original source...
    58. Larson, P.E.Z., Kerr, A.B., Chen, A.P., Lustig, M.S., Zierhut, M.L., Hu, S., Cunningham, C.H., Pauly, J.M., Kurhanewicz, J., Vigneron, D.B.J., 2008. Multiband excitation pulses for hyperpolarized 13C dynamic chemical-shift imaging. Magn. Reson. 194, 121-127. Go to original source... Go to PubMed...
    59. Leach, M.O., Verrill, M., Glaholm, J., Smith, T.A., Collins, D.J., Payne, G.S., Sharp, J.C., Ronen, S.M., McCready, V.R., Powles, T.J., Smith, I.E., 1998. Measurements of human breast cancer using magnetic resonance spectroscopy: a review of clinical measurements and a report of localized 31P measurements of response to treatment. NMR Biomed. 11, 314-340. Go to original source... Go to PubMed...
    60. Li, B.S.Y., Babb, J.S., Soher, B.J., Maudsley, A.A., Gonen, O., 2002. Reproducibility of 3D proton spectroscopy in the human brain. Magn. Reson. Med. 47, 39-44. Go to original source... Go to PubMed...
    61. Lilburn, D.M.L., Pavlovskaya, G.E., Meersmann, T., 2013. Perspectives of hyperpolarized noble gas MRI beyond 3He. J. Magn. Reson. 229C, 173-186. Go to original source... Go to PubMed...
    62. Mackinnon, W.B., Barry, P.A., Malycha, P.L., Gillett, D.J., Russell, P., Lean, C.L., Doran, S.T., Barraclough, B.H., Bilous, M., Mountford, C.E., 1997a. Fine-needle biopsy specimens of benign breast lesions distinguished from invasive cancer ex vivo with proton MR spectroscopy. Radiology 204, 661-666. Go to original source... Go to PubMed...
    63. Mackinnon, W.B., Barry, P.A., Malycha, P.L., Gillett, D.J., Russell, P., Lean, C.L., Barraclough, B.H., Bilous, M., Mountford, C.E., 1997b. Fine-needle biopsy specimens of benign breast lesions distinguished from invasive cancer ex vivo with proton MR spectroscopy. Radiology 204, 661-666. Go to original source... Go to PubMed...
    64. Mahon, M.M., Cox, I.J., Dina, R., Soutter, W.P., McIndoe, G.A., Williams, A.D., deSouza, N.M., 2004. 1H magnetic resonance spectroscopy of preinvasive and invasive cervical cancer: in vivo-ex vivo profiles and effect of tumor load. J. Magn. Reson. Imaging 19, 356-364. Go to original source... Go to PubMed...
    65. Martinez-Bisbal, M.C., Marti-Bonmati, L., Piquer, J., Revert, A., Ferrer, P., Lacer, J.L., Piotto, M., Assemat, O., Celda, B., 2004. 1 H and 13C HR-MAS spectroscopy of intact biopsy samples ex vivo and in vivo 1H MRS study of human high grade gliomas. NMR Biomed. 17, 191-205. Go to original source... Go to PubMed...
    66. Maudsley, A.A., Domenig, C., Govind, V., Darkazanli, A., Studholme, C., Arheart, K., Bloomer, C., 2009. Mapping of brain metabolite distributions by volumetric proton MR spectroscopic imaging (MRSI). Magn. Reson. Med. 61, 548-559. Go to original source... Go to PubMed...
    67. McKnight, T.R., 2004a. Proton magnetic resonance spectroscopic evaluation of brain tumor metabolism. Semin. Onol. 31, 605-617. Go to original source... Go to PubMed...
    68. McKnight, T.R., 2004b. Proton magnetic resonance spectroscopic evaluation of brain tumor metabolism. Semin. Oncol. 31, 605-617. Go to original source... Go to PubMed...
    69. McLean, M.A., Priest, A.N., Joubert, I., Lomas, D.J., Kataoka, M.Y., Earl, H., Crawford, R., Brenton, J.D., Griffiths, J.R., Sala, E., 2009. Metabolic characterization of primary and metastatic ovarian cancer by 1H-MRS in vivo at 3 T. Magn. Reson. Med. 62, 855-861. Go to original source... Go to PubMed...
    70. Meng, X., Huang, Z., Wang, R., Yu, J., 2014. Prediction of response to preoperative chemoradiotherapy in patients with locally advanced rectal cancer. Biosci. Trends 8, 11-23. Go to original source... Go to PubMed...
    71. Mentore, K., Froh, D.K., de Lange, E.E., Brookeman, J.R., PagetBrown, A.O., Altes, T.A., 2005. Hyperpolarized HHe 3 MRI of the lung in cystic fibrosis: assessment at baseline and after bronchodilator and airway clearance treatment. Acad. Radiol. 12, 1423-1429. Go to original source... Go to PubMed...
    72. Miwa, K., Matsuo, M., Ogawa, S.I., Shinoda, J., Yokoyama, K., Yamada, J., Yano, H., Iwama, T., 2014. Re-irradiation of recurrent glioblastoma multiforme using 11C-methionine PET/CT/MRI image fusion for hypofractionated stereotactic radiotherapy by intensity modulated radiation therapy. Radiat. Oncol. 9, 181. Go to original source... Go to PubMed...
    73. Morawski, A.M., Winter, P.M., Yu, X., Fuhrhop, R.W., Scott, M.J., Hockett, F., Robertson, J.D., Gaffney, P.J., Lanza, G.M., Wickline, S.A., 2004. Quantitative ''magnetic resonance immunohistochemistry'' with ligand-targeted 19F nanoparticles. Magn. Reson. Med. 52, 1255-1266. Go to original source... Go to PubMed...
    74. Morse, D.L., Gillies, R.J., 2005. Choline containing compounds as diagnostic, prognostic and therapeutic response indicators for breast cancer. In: Jagannathan, N.R. (Ed.), Recent Advances in MR Imaging and Spectroscopy. Jaypee Brothers Medical Publishers (P) Ltd., New Delhi, pp. 345-397. Go to original source...
    75. Morse, D.L., Gray, H., Payne, C.M., Gillies, R.J., 2005. Docetaxel induces cell death through mitotic catastrophe in human breast cancer cells. Mol. Cancer Ther. 4, 1495-1504. Go to original source... Go to PubMed...
    76. Mountford, C.E., Doran, S., Lean, C., Russell, P., 2004. Proton MRS can determine the pathology of human cancers with a high level of accuracy. Chem. Rev. 104, 3677-3704. Go to original source... Go to PubMed...
    77. Natterer, J., Bargon, J., 1997. Parahydrogen induced polarization. Prog. Nucl. Magn. Reson. Spectrosc. 31, 293-315. Go to original source...
    78. Negendank, W., 1992. Studies of human tumors by MRS: a review. NMR Biomed. 5, 303-324. Go to original source... Go to PubMed...
    79. Negendank, W.G., Padavic-Shaller, K.A., Li, C.W., MurphyBoesch, J., Stoyanova, R., Krigel, R.L., Schilder, R.J., Smith, M. R., Brown, T.R., 1995. Metabolic characterization of human non-Hodgkin's lymphomas in vivo with the use of protondecoupled phosphorus magnetic resonance spectroscopy. Cancer Res. 55, 3286-3294. Go to PubMed...
    80. Park, J.M., Park, J.H., 2001. Human in-vivo 31P MR spectroscopy of benign and malignant breast tumors. Korean J. Radiol. 2, 80-86. Go to original source... Go to PubMed...
    81. Perou, C.M., Sorlie, T., Eisen, M.B., van de Rijn, M., Jeffrey, S.S., Rees, C.A., Pollack, J.R., Ross, D.T., Johnsen, H., Akslen, L.A., Fluge, O., Pergamenschikov, A., Williams, C., Zhu, S.X., Lonning, P.E., Borresen-Dale, A.-L., Brown, P.O., Botstein, D., 2000. Molecular portraits of human breast tumours. Nature 406, 747-752. Go to original source... Go to PubMed...
    82. Podo, F., 1999. Tumour phospholipid metabolism. NMR Biomed. 12, 413-439. Go to original source... Go to PubMed...
    83. Qi, J., Shukla-Dave, A., Fong, Y., Gönen, M., Schwartz, L.H., Jarnagin, W.M., Koutcher, J.A., Zakian, K.L., 2011. 31P MR spectroscopic imaging detects regenerative changes in human liver stimulated by portal vein embolization. J. Magn. Reson. Imaging 34, 336-344. Go to original source... Go to PubMed...
    84. Ratner, A.V., Quay, S., Muller, H.H., Simpson, B.B., Hurd, R., Young, S.W., 1989. 19F relaxation rate enhancement and frequency shift with Gd-DTPA. Invest. Radiol. 24, 224-227. Go to original source... Go to PubMed...
    85. Reeder, S.B., Brittain, J.H., Grist, T.M., Yen, Y.F., 2007. Leastsquares chemical shift separation for 13C metabolic imaging. J. Magn. Reson. Imaging 26, 1145-2115. Go to original source... Go to PubMed...
    86. Reo, N.V., Adinehzadeh, M., Foy, B.D., 2002. Kinetic analyses of liver phosphatidylcholine and phosphatidylethanolamine biosynthesis using 13C NMR spectroscopy. Biochim. Biophys. Acta 1580, 171-188. Go to original source... Go to PubMed...
    87. Rivera, D.S., Wijnen, J.P., van der Kemp, W.J., Raaijmakers, A.J., Luijten, P.R., Klomp, D.W., 2014. MRI and 31 P magnetic resonance spectroscopy hardware for axillary lymph node investigation at 7 T. Magn. Reson. Med., http://dx.doi.org/10.1002/mrm.25304. Go to original source... Go to PubMed...
    88. Ronen, S.M., Leach, M.O., 2001. Breast imaging technology: imaging biochemistry - applications to breast cancer. Breast Cancer Res. 3, 36-40. Go to original source... Go to PubMed...
    89. Ronen, S.M., Volk, A., Mispelter, J., 1994. Comparative NMR study of a differentiated rat hepatoma and its dedifferentiated subclone cultured as spheroids and as implanted tumors. NMR Biomed. 7, 278-282. Go to original source... Go to PubMed...
    90. Ronen, S.M., DiStefano, F., McCoy, C.L., Robertson, D., Smith, T. A.D., Al-Saffar, N.M., Titley, J., Cunningham, D.C., Griffiths, J. R., Leach, M.O., Clarke, P.A., 1999. Magnetic resonance detects metabolic changes associated with chemotherapyinduced apoptosis. Br. J. Cancer 80, 1035-1041. Go to original source... Go to PubMed...
    91. Robinson, S.P., McCoy, C.L., Griffiths, J.R., 1996. Animal tumor models. In: Grant, D.M., Harris, R.K. (Eds.), Encyclopedia of Nuclear Magnetic Resonance, vol. 2. Wiley, New York, pp. 828-833.
    92. Ruiz-Cabello, J., Barnett, B.P., Bottomley, P.A., Bulte, J.W.M., 2011. Fluorine 19F MRS and MRI in biomedicine. NMR Biomed. 24, 114-129. Go to original source... Go to PubMed...
    93. Schreiber, W.G., Morbach, A.E., Stavngaard, T., Gast, K.K., Herweling, A., Søgaard, L.V., Windirsch, M., Schmiedeskamp, J., Heussel, C.P., Kauczor, H.U., 2005. Assessment of lung microstructure with magnetic resonance imaging of hyperpolarized helium-3. Respir. Physiol. Neurobiol. 148, 23-42. Go to original source... Go to PubMed...
    94. Schlemmer, H.P., Becker, M., Bachert, P., Dietz, A., Rudat, V., Vanselow, B., Wollensack, P., Zuna, I., Knopp, M.V., Weidauer, H., Wannenmacher, M., van Kaick, G., 1999. Alterations of intratumoral pharmacokinetics of 5-fluorouracil in head and neck carcinoma during simultaneous radiochemotherapy. Cancer Res. 59, 2363-2369.
    95. Shchepin, R.V., Coffey, A.M., Waddell, K.W., Chekmenev, E.Y., 2014a. Parahydrogen induced polarization of 1-13Cphospholactate-d2 for biomedical imaging with >30,000,000fold NMR signal enhancement in water. Anal. Chem. 86, 5601-5605. Go to original source... Go to PubMed...
    96. Shchepin, R.V., Pham, W., Chekmenev, E., 2014b. Dephosphorylation and biodistribution of 1-13Cphospholactate in vivo. J. Labelled Comp. Radiopharm. 57, 517-524. Go to original source... Go to PubMed...
    97. Sijens, P.E., 1998. Phosphorus MR spectroscopy in the treatment of human extremity sarcomas. NMR Biomed. 11, 341-353. Go to original source... Go to PubMed...
    98. Silberhumer, G.R., Zakian, K., Malhotra, S., Brader, P., Gönen, M., Koutcher, J., Fong, Y., 2009. Relationship between 31P metabolites and oncolytic viral therapy sensitivity in human colorectal cancer xenografts. Br. J. Surg. 96, 809-816. Go to original source... Go to PubMed...
    99. Smith, T.A.D., Bush, C., Jameson, C., Titley, J.C., Leach, M.O., Wilman, D.E.V., McCready, V.R., 1993. Phospholipid metabolites, prognosis and proliferation in human breast carcinoma. NMR Biomed. 6, 318-323. Go to original source... Go to PubMed...
    100. Smith, T.A., Appleyard, M.V., Sharp, S., Fleming, I.N., Murray, K., Thompson, A.M., 2013. Response to trastuzumab by Her-2 expressing breast tumour xenografts is accompanied by decreased Hexokinase II, glut1 and [18F]-FDG incorporation and changes in 31P-NMR-detectable phosphomonoesters. Cancer Chemother. Pharmacol. 71, 473-480. Go to original source... Go to PubMed...
    101. Srinivas, M., Morel, P.A., Ernst, L.A., Laidlaw, D.H., Ahrens, E.T., 2007. Fluorine-19 MRI for visualization and quantification of cell migration in a diabetes model. Magn. Reson. Med. 58, 725-734. Go to original source... Go to PubMed...
    102. Srivastava, S., Roy, R., Singh, S., Kumar, P., Dalela, D., Sankhwar, S.N., Goel, A., Sonkar, A.A., 2010. Taurine - a possible fingerprint biomarker in non-muscle invasive bladder cancer: a pilot study by 1H NMR spectroscopy. Cancer Biomark. 6, 11-20. Go to original source... Go to PubMed...
    103. Süllentrop, F., Hahn, J., Moka, D., 2012. In vitro and in vivo 1H-MR spectroscopic examination of the renal cell carcinoma. Int. J. Biomed. Sci. 8, 94-108. Go to original source...
    104. Swanson, M.G., Vigneron, D.B., Tabatab, Z.L., Males, R.G., Schmitt, Carroll, P.R., James, J.K., Hurd, R.E., Kurhanewicz, J., 2003. Proton HR-MAS spectroscopy and quantitative pathologic analysis of MRI/3D-MRSI-targeted postsurgical prostate tissues. Magn. Reson. Med. 50, 944-954. Go to original source... Go to PubMed...
    105. Sze, G., Shin, J., Krol, G., Johnson, C., Liu, D., Deck, M.D., 1998. Intraparenchymal brain metastases: MR imaging versus contrast-enhanced CT. Radiology 168, 187-194. Go to original source... Go to PubMed...
    106. Tate, A.R., Foxall, P.J.D., Holmes, E., Moka, D., Spraul, M., Nicholson, J.K., Lindon, J.C., 2000. Distinction between normal and renal cell carcinoma kidney cortical biopsy samples using pattern recognition of 1H magic angle spinning (MAS) NMR spectra. NMR Biomed. 13, 64-71. Go to original source... Go to PubMed...
    107. Terreno, E., Castelli, D.D., Cabella, C., Dastru, W., Sanino, A., Stancanello, J., Tei, L., Aime, S., 2008. Paramagnetic liposomes as innovative contrast agents for magnetic resonance (MR) molecular imaging applications. Chem. Biodivers. 5, 1901-1902. Go to original source... Go to PubMed...
    108. Twelves, C.J., Porter, D.A., Lowryl, M., Dobbs, N.A., Graves, P.A., Smith, M.A., Rubens, R.D., Richards, M.A., 1994. Phosphorus31 metabolism of post-menopausal breast cancer studied in vivo by magnetic resonance spectroscopy. Br. J. Cancer 69, 1151-2115. Go to original source... Go to PubMed...
    109. Thompson, C.J., Goertzen, A.L., Thiessen, J.D., Bishop, D., Stortz, G., Kozlowski, P., Retière, F., Zhang, X., Sossi, V., 2014. Development of a PET scanner for simultaneously imaging small animals with MRI and PET. Sensors (Basel) 14, 14654-14671. Go to original source... Go to PubMed...
    110. Tugnoli, V., Mucci, A., Schenetti, L., Righi, V., Calabrese, C., Fabbri, A., Di, F.G., Tosi, M.R., 2006. Ex vivo HR-MAS magnetic resonance spectroscopy of human gastric adenocarcinomas: a comparison with healthy gastric mucosa. Oncol. Rep. 16, 543-553. Go to original source... Go to PubMed...
    111. Van der Sanden, B.P.J., Heerschap, A., Hoofd, L., Simonetti, A.W., Nicolay, K., van der Toorn, A., Colier, W.N.J.M., van der Koge, A.J., 1999. Effect of carbogen breathing on the physiological profile of human glioma xenograf. Magn. Reson. Med. 42, 490-499. Go to original source... Go to PubMed...
    112. Von Brand, E., Cisterna, M., Merino, G., Uribe, E., Palma-Rojas, C., Rosenblitt, M., Albornoz, J.L., 2009. Non-destructive method to study the internal anatomy of the Chilean scallop Argopecten purpuratus. J. Shellfish Res. 28, 325-327. Go to original source...
    113. Walker, T.G., Happer, W., 1997. Spin-exchange optical pumping of noble-gas nuclei. Rev. Mod. Phys. 69, 629-642. Go to original source...
    114. Walter, G., Barton, E.R., Sweeney, H.L., 2000. Noninvasive measurement of gene expression in skeletal muscle. Proc. Natl. Acad. Sci. U.S.A. 97, 5151-5155. Go to original source... Go to PubMed...
    115. Wang, H., Wang, L., Zhang, H., Deng, P., Chen, J., Zhou, B., Hu, J., Zou, J., Lu, W., Xiang, P., Wu, T., Shao, X., Li, Y., Zhou, Z., Zhao, Y.L., 2013. 1H NMR-based metabolic profiling of human rectal cancer tissue. Mol. Cancer 12, 121. Go to original source... Go to PubMed...
    116. Warren, W.S., Jenista, E., Branca, R.T., Chen, X., 2009. Increasing hyperpolarized spin lifetimes through true singlet eigenstates. Science 323, 1711-1714. Go to original source... Go to PubMed...
    117. Yeung, D.K.W., Yang, W.T., Tse, G.M., 2002. Breast cancer: in vivo proton MR spectroscopy in the characterization of histopathologic subtypes and preliminary observations in axillary node metastases. Radiology 225, 190-197. Go to original source... Go to PubMed...

    Return to the content