Metabolite quantification in tumours by magnetic resonance spectroscopy: Objectives, results and perspectives

Current Medical Imaging Reviews

Volumn 5, Issue 2, 2009, Pages 110-127

  Canese, Rossella ^a,b   Iorio, Egidio ^a,b   Ricci, Alessandro ^a,b   Pisanu, Maria Elena ^a,b   Giannini, Massimo ^a,b   Podo, Franca ^a,b  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b Alleanza Contro il Cancro   (Italy)

Author keywords

Magnetic resonance spectroscopic imaging (MRSI); Magnetic resonance spectroscopy (MRS); Metabolism; Quantification; Tumours

Indexed keywords

CHOLINE; DOXORUBICIN; GLUTAMIC ACID; GLUTAMINE; GLUTATHIONE; N ACETYLASPARTIC ACID; PROSTATE SPECIFIC ANTIGEN;

BRAIN TUMOR; BREAST CANCER; CANCER ADJUVANT THERAPY; CANCER CLASSIFICATION; CANCER GRADING; CANCER RADIOTHERAPY; COLORECTAL CANCER; CONTRAST ENHANCEMENT; DIAGNOSTIC ACCURACY; DISEASE COURSE; FIBROSARCOMA; HUMAN; LIVER CANCER; MAGIC ANGLE SPINNING PROTON NUCLEAR MAGNETIC RESONANCE; MALIGNANT NEOPLASTIC DISEASE; METABOLITE; MULTIPLE MYELOMA; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OVARY CANCER; PRIORITY JOURNAL; PROSTATE CANCER; PROTON NUCLEAR MAGNETIC RESONANCE; QUANTITATIVE ANALYSIS; REVIEW; SENSITIVITY AND SPECIFICITY; SPECTROSCOPY; TREATMENT PLANNING; TREATMENT RESPONSE; WATER CONTENT;

EID: 68549083816     PISSN: 15734056     EISSN: None     Source Type: Journal    
DOI: 10.2174/157340509788185306     Document Type: Review

References (167)

1. 31P NMR using surface coils. Nature 1980; 283: 167-70.
2. Gadian DG, Radda GK. NMR studies of tissue metabolism. Annu Rev Biochem 1981; 50: 69-83.
3. Bottomley PA. Human in vivo NMR spectroscopy in diagnostic medicine: clinical tool or research probe? Radiology 1989; 170: 1-15.
4. Gadian DG. NMR and its Application to Living Systems. 2nd ed. Oxford: Oxford University Press 1995.
5. Leach MO, Le Moyec L, Podo F. MRS of Tumours: Basic Principles. In: de Certaines JD, Boveé WMMJ, Podo F, Eds. Magnetic Resonance Spectroscopy in Biology and Medicine. Oxford: Pergamon Press 1992; pp. 295-44.
6. Negendank W. Studies of human tumors by MRS: a review. NMR Biomed 1992; 5: 303-24.
7. Podo F. Tumour phospholipid metabolism. NMR Biomed 1999; 12: 413-39.
8. Gillies RJ, Bhujwalla ZM, Evelhoch J, et al. Applications of magnetic resonance in model systems: tumor biology and physiology. Neoplasia 2000; 2: 139-51.
9. He Q, Xu RZ, Shkarin P, et al. Magnetic resonance spectroscopic imaging of tumor metabolic markers for cancer diagnosis, metabolic phenotyping, and characterization of tumor microenvironment. Disease Markers 2004; 19: 69-94.
10. Gillies RJ, Morse DL. In vivo magnetic resonance spectroscopy in cancer. Annu Rev Biomed Eng 2005; 7: 287-326.
11. Leach MO. Magnetic resonance spectroscopy (MRS) in the investigation of cancer at the Royal Marsden Hospital and the Institute of Cancer Research. Phys Med Biol 2006; 51: R61-82.
12. Celda B, Monleon D, Martinez-Bisbal MC, et al. MRS as endogenous molecular imaging for brain and prostate tumors: FP6 project "eTUMOR". Adv Exp Med Biol 2006; 587: 285-02.
13. Podo F, Sardanelli F, Iorio E, et al. Abnormal choline phospholipid metabolism in breast and ovary cancer: molecular bases for noninvasive imaging approaches. Curr Med Imaging Rev 2007; 3: 123-37. Available from: http://www.ingentaconnect.com/content/ben/cmir/2007.
14. Chance B, Nakase Y, Bond M, Leigh JS Jr. McDonald G. Detection of 31P nuclear magnetic resonance signals in brain by in vivo and freeze-trapped assays. Proc Natl Acad Sci USA 1978; 75: 4925-9.
15. Grove TH, Ackerman JJ, Radda GK, Bore PJ. Analysis of rat heart in vivo by phosphorus nuclear magnetic resonance. Proc Natl Acad Sci USA 1980; 77: 299-02.
16. Boveé WMMJ. Quality assessment in in vivo NMR. In: de Certaines JD, Boveé WMMJ, Podo F, Eds. Magnetic Resonance Spectroscopy in Biology and Medicine. Oxford: Pergamon Press 1992; pp. 209-20.
17. Keevil SF, Barbiroli B, Brooks JC, et al. Absolute metabolite quantification by in vivo NMR spectroscopy: II. A multicentre trial of protocols for in vivo localised proton studies of human brain. Magn Reson Imaging 1998; 16: 1093-06.
18. Ott D, Hennig J, Ernst T. Human brain tumors: assessment with in vivo proton MR spectroscopy. Radiology 1993; 186: 745-52.
19. 1H magnetic resonance spectroscopy. Magn Reson Med 2003; 49: 223-32.
20. Vanhamme L, van den Boogaart A, Van Huffel S. Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. J Magn Reson 1997; 129: 35-43.
21. Provencher SW. Estimation of metabolite concentrations from localized in vivo proton NMR spectra. Magn Reson Med 1993; 30: 672-9.
22. Cavassila S, Deval S, Huegen C, van Ormondt D, Graveron-Demilly D. Cramer-Rao bounds: an evaluation tool for quantitation. NMR Biomed 2001; 14: 278-83.
23. 1H human brain spectra by LCModel and AMARES. Magn Reson Med 2004; 51: 904-12.
24. Sijens PE, van den Bent MJ, Nowak PJ, van Dijk P, Oudkerk M. 1H chemical shift imaging reveals loss of brain tumor choline signal after administration of Gd-contrast. Magn Reson Med 1997; 37: 222-5.
25. Gideon P, Sorensen PS, Thomsen C, Stahlberg F, Gjerris F, Henriksen O. Assessment of CSF dynamics and venous flow in the superior sagittal sinus by MRI in idiopathic intracranial hypertension: a preliminary study. Neuroradiology 1994; 36: 350-4.
26. 1H-magnetic resonance spectroscopy of breast cancer pre- and postgadolinium administration. Invest Radiol 2005; 40: 405-11.
27. Barker PB, Soher BJ, Blackband SJ, Chatham JC, Mathews VP, Bryan RN. Quantitation of proton NMR spectra of the human brain using tissue water as an internal concentration reference. NMR Biomed 1993; 6: 89-94.
28. 1H-MRS using water as an internal standard. Magn Reson Imaging 1993; 11: 107-18.
29. Toft PB, Christiansen P, Pryds O, Lou HC, Henriksen O. T1, T2, and concentrations of brain metabolites in neonates and adolescents estimated with H-1 MR spectroscopy. J Magn Reson Imaging 1994; 4: 1-5.
30. Christiansen P, Toft P, Larsson HB, Stubgaard M, Henriksen O. The concentration of N-acetyl aspartate, creatine + phosphocreatine, and choline in different parts of the brain in adulthood and senium. Magn Reson Imaging 1993; 11: 799-06.
31. Christiansen P, Schlosser A, Henriksen O. Reduced N-acetyl-aspartate content in the frontal part of the brain in patients with probable Alzheimer's disease. Magn Reson Imaging 1995; 13: 457-62.
32. Cady EB. Quantitative combined phosphorus and proton PRESS of the brains of newborn human infants. Magn Reson Med 1995; 33: 557-63.
33. 1H MR spectroscopy. Magn Reson Med 2003; 50: 1134-43.
34. 1H MRS. Magn Reson Med 2003; 49: 632-7.
35. 1H MR spectra: a comparison of classification using whole spectra versus metabolite quantification. NMR Biomed 2007; 20: 763-70.
36. Yerli H, Agildere AM, Ozen O, Geyik E, Atalay B, Elhan AH. Evaluation of cerebral glioma grade by using normal side creatine as an internal reference in multi-voxel 1H-MR spectroscopy. Diagn Interv Radiol 2007; 13: 3-9.
37. Matsumura A, Isobe T, Takano S, Kawamura H, Anno I. Non-invasive quantification of lactate by proton MR spectroscopy and its clinical applications. Clin Neurol Neurosurg 2005; 107: 379-84.
38. Payne GS, Leach MO. Applications of magnetic resonance spectroscopy in radiotherapy treatment planning. Br J Radiol 2006; 79 Spec No 1: S16-26.
39. 1H-MR spectroscopy. J Magn Reson Imaging 2007; 26: 1390-8.
40. Frahm J, Bruhn H, Gyngell ML, Merboldt KD, Hanicke W, Sauter R. Localized proton NMR spectroscopy in different regions of the human brain in vivo. Relaxation times and concentrations of cerebral metabolites. Magn Reson Med 1989; 11: 47-63.
41. Toyooka M, Kimura H, Uematsu H, Kawamura Y, Takeuchi H, Itoh H. Tissue characterization of glioma by proton magnetic resonance spectroscopy and perfusion-weighted magnetic resonance imaging: glioma grading and histological correlation. Clin Imaging 2008; 32: 251-8.
42. 201TlCl single-photon emission computerized tomography, and gadolinium-enhanced magnetic resonance imaging. J Neurosurg 2004; 100: 835-41.
43. 1H-MRSI metabolites in gliomas. Neuroimage 2004; 23: 454-61.
44. Roebuck JR, Cecil KM, Schnall MD, Lenkinski RE. Human breast lesions: characterization with proton MR spectroscopy. Radiology 1998; 209: 269-75.
45. Li CW, Kuo YC, Chen CY, et al. Quantification of choline compounds in human hepatic tumors by proton MR spectroscopy at 3 T. Magn Reson Med 2005; 53: 770-6.
46. Chen CY, Li CW, Kuo YT, et al. Early response of hepatocellular carcinoma to transcatheter arterial chemoembolization: choline levels and MR diffusion constants - initial experience. Radiology 2006; 239: 448-56.
47. Bakken IJ, Gribbestad IS, Singstad TE, Kvistad KA. External standard method for the in vivo quantification of choline-containing compounds in breast tumors by proton MR spectroscopy at 1.5 tesla. Magn Res Med 2001; 46: 189-92.
48. Ernst T, Kreis R, Ross BD. Absolute quantitation of water and metabolites in the human brain. I. Compartments and water. J Magn Res Ser B 1993; 102: 1-8.
49. Kreis R, Ernst T, Ross BD. Absolute quantitation of water and metabolites in the human brain. I. Metabolite concentrations. J Magn Reson Ser B 1993; 102: 9-19.
50. 1H MR spectroscopy of brain tumours and masses. NMR Biomed 2003; 16: 123-31.
51. 1HMRS) to clinical brain tumour diagnosis. Br J Neurosurg 2002; 16: 329-34.
52. Preul MC, Caramanos Z, Collins DL, et al. Accurate, noninvasive diagnosis of human brain tumors by using proton magnetic resonance spectroscopy. Nat Med 1996; 2: 323-5.
53. Peet AC, Arvanitis TN, Auer DP, et al. The value of magnetic resonance spectroscopy in tumour imaging. Arch Dis Child 2008; 93: 725-7.
54. 1H MRSI. J Magn Reson Imaging 2002; 16: 464-76.
55. Burtscher IM, Skagerberg G, Geijer B, Englund E, Stahlberg F, Holtas S. Proton MR spectroscopy and preoperative diagnostic accuracy: an evaluation of intracranial mass lesions characterized by stereotactic biopsy findings. AJNR Am J Neuroradiol 2000; 21: 84-93.
56. Dowling C, Bollen AW, Noworolski SM, et al. Preoperative proton MR spectroscopic imaging of brain tumors: correlation with histopathologic analysis of resection specimens. AJNR Am J Neuroradiol 2001; 22: 604-12.
57. Stadlbauer A, Gruber S, Nimsky C, et al. Preoperative grading of gliomas by using metabolite quantification with high-spatial-resolution proton MR spectroscopic imaging. Radiology 2006; 238: 958-69.
58. 1H-MRSI of cerebral gray and white matter. Magn Reson Med 2000; 44: 401-11.
59. Matsumura A, Isobe T, Anno I, Takano S, Kawamura H. Correlation between choline and MIB-1 index in human gliomas. A quantitative in proton MR spectroscopy study. J Clin Neurosci 2005; 12: 416-20.
60. Isobe T, Matsumura A, Anno I, et al. Quantification of cerebral metabolites in glioma patients with proton MR spectroscopy using T2 relaxation time correction. Magn Reson Imaging 2002; 20: 343-9.
61. Stubbs M, Veech RL, Griffiths JR. Tumor metabolism: the lessons of magnetic resonance spectroscopy. Adv Enzyme Regul 1995; 35: 101-15.
62. 1H tumor spectra quantification from acquisitions without water suppression. Magn Reson Imaging 2006; 24: 1271-9.
63. Sijens PE, Wijrdeman HK, Moerland MA, Bakker CJ, Vermeulen JW, Luyten PR. Human breast cancer in vivo: H-1 and P-31 MR spectroscopy at 1.5 T. Radiology 1988; 169: 615-20.
64. Jacobs MA, Barker PB, Bottomley PA, Bhujwalla Z, Bluemke DA. Proton magnetic resonance spectroscopic imaging of human breast cancer: a preliminary study. J Magn Reson Imaging 2004; 19: 68-75.
65. Sharma U, Sah RG, Jagannathan NR. Magnetic Resonance Imaging (MRI) and Spectroscopy (MRS) in breast cancer. Magn Reson Insights 2008; 2: 93-103.
66. Kumar M, Jagannathan NR, Seenu V, Dwivedi SN, Julka PK, Rath GK. Monitoring the therapeutic response of locally advanced breast cancer patients: sequential in vivo proton MR spectroscopy study. J Magn Reson Imaging 2006; 24: 325-32.
67. Haddadin IS, McIntosh A, Meisamy S, et al. Metabolite quantification and high-field MRS in breast cancer. NMR Biomed 2009; 22: 65-76.
68. Sardanelli F, Fausto A, Podo F. MR spectroscopy of the breast. Radiol Med 2008; 113: 56-64.
69. 1H spectroscopy without solvent suppression: characterization of signal modulations at short echo times. J Magn Reson 2001; 153: 203-9.
70. 1H-MRS of the brain at 3 T: the effects of physiological motion. Magn Reson Med 2004; 51: 184-7.
71. 1H MR spectroscopy using water as an internal reference at 1.5 T. MAGMA 2006; 19: 96-104.
72. Graham SJ, Stanchev PL, Lloyd-Smith JO, Bronskill MJ, Plewes DB. Changes in fibroglandular volume and water content of breast tissue during the menstrual cycle observed by MR imaging at 1.5 T. J Magn Reson Imaging 1995; 5: 695-701.
73. Manton DJ, Chaturvedi A, Hubbard A, et al. Neoadjuvant chemotherapy in breast cancer: early response prediction with quantitative MR imaging and spectroscopy. Br J Cancer 2006; 94: 427-35.
74. 1H MR spectroscopy to improve diagnostic accuracy of breast MR imaging: preliminary results of observer performance study at 4.0 T. Radiology 2005; 236: 465-75.
75. Huang W, Fisher PR, Dulaimy K, Tudorica LA, O'Hea B, Button TM. Detection of breast malignancy: diagnostic MR protocol for improved specificity. Radiology 2004; 232: 585-91.
76. Sardanelli F, Fausto A, Di Leo G, de Nijs R, Vorbuchner M, Podo F. In vivo Proton MR Spectroscopy of the Breast Using the Total Choline Peak Integral as a Marker of Malignancy. Am J Roentgenol 2008; in press.
77. Jagannathan NR, Kumar M, Seenu V, et al. 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 2001; 84: 1016-22.
78. 1H MR spectroscopy. J Magn Reson Imaging 1999; 10: 159-64.
79. 1H MR spectroscopy-a pilot study at 4 T. Radiology 2004; 233: 424-31.
80. Baek HM, Chen JH, Nalcioglu O, Su MY. Proton MR spectroscopy for monitoring early treatment response of breast cancer to neoadjuvant chemotherapy. Ann Oncol 2008; 19: 1022-4.
81. Tan PC, Pickles MD, Lowry M, Manton DJ, Turnbull LW. Lesion T(2) relaxation times and volumes predict the response of malignant breast lesions to neoadjuvant chemotherapy. Magn Reson Imaging 2008; 26: 26-34.
82. Al-Saffar NM, Troy H, Ramirez de Molina A, et al. Noninvasive magnetic resonance spectroscopic pharmacodynamic markers of the choline kinase inhibitor MN58b in human carcinoma models. Cancer Res 2006; 66: 427-34.
83. Morse DL, Raghunand N, Sadarangani P, et al. Response of choline metabolites to docetaxel therapy is quantified in vivo by localized (31)P MRS of human breast cancer xenografts and in vitro by high-resolution (31)P NMR spectroscopy of cell extracts. Magn Reson Med 2007; 58: 270-80.
84. Chen M, Dang HD, Wang JY, et al. Prostate cancer detection: comparison of T2-weighted imaging, diffusion-weighted imaging, proton magnetic resonance spectroscopic imaging, and the three techniques combined. Acta Radiol 2008; 49: 602-10.
85. 1H-MRS) in the diagnosis of localized prostate cancer. Anticancer Res 2008; 28: 1899-904.
86. Swindle P, Ramadan S, Stanwell P, McCredie S, Russell P, Mountford C. Proton magnetic resonance spectroscopy of the central, transition and peripheral zones of the prostate: assignments and correlation with histopathology. MAGMA 2008; 21: 423-34.
87. Wang P, Guo YM, Liu M, et al. A meta-analysis of the accuracy of prostate cancer studies which use magnetic resonance spectroscopy as a diagnostic tool. Korean J Radiol 2008; 9: 432-8.
88. Kurhanewicz J, Swanson MG, Nelson SJ, Vigneron DB. Combined magnetic resonance imaging and spectroscopic imaging approach to molecular imaging of prostate cancer. J Magn Reson Imaging 2002; 16: 451-63.
89. Kurhanewicz J, Vigneron DB, Males RG, Swanson MG, Yu KK, Hricak H. The prostate: MR imaging and spectroscopy. Present and future. Radiol Clin North Am 2000; 38: 115-38, viii-ix.
90. Lowry M, Liney GP, Turnbull LW, Manton DJ, Blackband SJ, Horsman A. Quantification of citrate concentration in the prostate by proton magnetic resonance spectroscopy: zonal and age-related differences. Magn Reson Med 1996; 36: 352-8.
91. Pels P, Ozturk-Isik E, Swanson MG, et al. Quantification of prostate MRSI data by model-based time domain fitting and frequency domain analysis. NMR Biomed 2006; 19: 188-97.
92. Weis J, Ahlstrom H, Hlavcak P, Haggman M, Ortiz-Nieto F, Bergman A. Two-dimensional spectroscopic imaging for pretreatment evaluation of prostate cancer: comparison with the step-section histology after radical prostatectomy. Magn Reson Imaging 2009; 27: 87-93.
93. Heerschap A, Jager GJ, van der Graaf M, et al. In vivo proton MR spectroscopy reveals altered metabolite content in malignant prostate tissue. Anticancer Res 1997; 17: 1455-60.
94. 1H MRS and MRI. Magn Reson Imaging 1997; 15: 1177-86.
95. Kim JK, Kim DY, Lee YH, et al. In vivo differential diagnosis of prostate cancer and benign prostatic hyperplasia: localized proton magnetic resonance spectroscopy using external-body surface coil. Magn Reson Imaging 1998; 16: 1281-8.
96. Schricker AA, Pauly JM, Kurhanewicz J, Swanson MG, Vigneron DB. Dualband spectral-spatial RF pulses for prostate MR spectroscopic imaging. Magn Reson Med 2001; 46: 1079-87.
97. Star-Lack J, Vigneron DB, Pauly J, Kurhanewicz J, Nelson SJ. Improved solvent suppression and increased spatial excitation bandwidths for three-dimensional PRESS CSI using phase-compensating spectral/spatial spin-echo pulses. J Magn Reson Imaging 1997; 7: 745-57.
98. Swanson MG, Vigneron DB, Tabatabai ZL, et al. Proton HR-MAS spectroscopy and quantitative pathologic analysis of MRI/3DMRSI-targeted postsurgical prostate tissues. Magn Reson Med 2003; 50: 944-54.
99. Schiebler ML, Tomaszewski JE, Bezzi M, et al. Prostatic carcinoma and benign prostatic hyperplasia: correlation of high-resolution MR and histopathologic findings. Radiology 1989; 172: 131-7.
100. 3) spatial resolution. Radiology 1996; 198: 795-805.
101. Yu KK, Scheidler J, Hricak H, et al. Prostate cancer: prediction of extracapsular extension with endorectal MR imaging and three-dimensional proton MR spectroscopic imaging. Radiology 1999; 213: 481-8.
102. Casciani E, Polettini E, Bertini L, et al. Prostate cancer: evaluation with endorectal MR imaging and three-dimensional proton MR spectroscopic imaging. Radiol Med 2004; 108: 530-41.
103. 1H MR spectroscopic imaging. Radiology 1996; 200: 489-96.
104. Heijmink SW, Scheenen TW, Futterer JJ, et al. Prostate and lymph node proton magnetic resonance (MR) spectroscopic imaging with external array coils at 3 T to detect recurrent prostate cancer after radiation therapy. Invest Radiol 2007; 42: 420-7.
105. Mueller-Lisse UG, Swanson MG, Vigneron DB, et al. Time-dependent effects of hormone-deprivation therapy on prostate metabolism as detected by combined magnetic resonance imaging and 3D magnetic resonance spectroscopic imaging. Magn Reson Med 2001; 46: 49-57.
106. Mueller-Lisse UG, Swanson MG, Vigneron DB, Kurhanewicz J. Magnetic resonance spectroscopy in patients with locally confined prostate cancer: association of prostatic citrate and metabolic atrophy with time on hormone deprivation therapy, PSA level, and biopsy Gleason score. Eur Radiol 2007; 17: 371-8.
107. Thomas MA, Lange T, Velan SS, et al. Two-dimensional MR spectroscopy of healthy and cancerous prostates in vivo. MAGMA 2008; 21: 443-58.
108. Choi H, Ma J. Use of perfluorocarbon compound in the endorectal coil to improve MR spectroscopy of the prostate. AJR Am J Roentgenol 2008; 190: 1055-9.
109. Okada T, Harada M, Matsuzaki K, Nishitani H, Aono T. Evaluation of female intrapelvic tumors by clinical proton MR spectroscopy. J Magn Reson Imaging 2001; 13: 912-7.
110. Hascalik S, Celik O, Sarac K, Meydanli MM, Alkan A, Mizrak B. Metabolic changes in pelvic lesions: findings at proton MR spectroscopic imaging. Gynecol Obstet Invest 2005; 60: 121-7.
111. Stanwell P, Russell P, Carter J, Pather S, Heintze S, Mountford C. Evaluation of ovarian tumors by proton magnetic resonance spectroscopy at three Tesla. Invest Radiol 2008; 43: 745-51.
112. 1H-magnetic resonance spectroscopy of the serial development of hepatocarcinogenesis in an experimental animal model. Biochim Biophys Acta 2001; 1526: 230-6.
113. 1H-NMR spectroscopy in a rat model. Toxicol Appl Pharmacol 2005; 207: 237-44.
114. 1H MR spectroscopy in the evaluation of the serial development of hepatocarcinogenesis in an experimental rat model. Acad Radiol 2006; 13: 1532-7.
115. Zhao WD, Guan S, Zhou KR, et al. In vivo detection of metabolic changes by 1H-MRS in the DEN-induced hepatocellular carcinoma in Wistar rat. J Cancer Res Clin Oncol 2005; 131: 597-602.
116. Kuo YT, Li CW, Chen CY, Jao J, Wu DK, Liu GC. In vivo proton magnetic resonance spectroscopy of large focal hepatic lesions and metabolite change of hepatocellular carcinoma before and after transcatheter arterial chemoembolization using 3.0-T MR scanner. J Magn Reson Imaging 2004; 19: 598-604.
117. 1H magnetic resonance spectroscopy in evaluation of hepatocellular carcinoma and its early response to transcatheter arterial chemoembolization. Chin Med Sci J 2006; 21: 258-64.
118. 1H magnetic resonance spectroscopy. Mol Cancer 2008; 7: 33.
119. 1H-MR spectra in vivo at 1.5 T. Magn Reson Med 2002; 47: 809-11.
120. Seierstad T, Roe K, Olsen DR. Noninvasive monitoring of radiation-induced treatment response using proton magnetic resonance spectroscopy and diffusion-weighted magnetic resonance imaging in a colorectal tumor model. Radiother Oncol 2007; 85: 187-94.
121. Chung YL, Troy H, Kristeleit R, et al. Noninvasive magnetic resonance spectroscopic pharmacodynamic markers of a novel histone deacetylase inhibitor, LAQ824, in human colon carcinoma cells and xenografts. Neoplasia 2008; 10: 303-13.
122. Beauregard DA, Pedley RB, Hill SA, Brindle KM. Differential sensitivity of two adenocarcinoma xenografts to the anti-vascular drugs combretastatin A4 phosphate and 5,6-dimethylxanthenone-4-acetic acid, assessed using MRI and MRS. NMR Biomed 2002; 15: 99-105.
123. McPhail LD, Chung YL, Madhu B, et al. Tumor dose response to the vascular disrupting agent, 5,6-dimethylxanthenone-4-acetic acid, using in vivo magnetic resonance spectroscopy. Clin Cancer Res 2005; 11: 3705-13.
124. Kamm YJ, Peters GJ, Hull WE, Punt CJ, Heerschap A. Correlation between 5-fluorouracil metabolism and treatment response in two variants of C26 murine colon carcinoma. Br J Cancer 2003; 89: 754-62.
125. McSheehy PM, Seymour MT, Ojugo AS, et al. A pharmacokinetic and pharmacodynamic study in vivo of human HT29 tumours using 19F and 31P magnetic resonance spectroscopy. Eur J Cancer 1997; 33: 2418-27.
126. 1H magnetic resonance spectroscopy of bone marrow. MAGMA 2007; 20: 93-101.
127. Doyle VL, Payne GS, Collins DJ, Verrill MW, Leach MO. Quantification of phosphorus metabolites in human calf muscle and soft-tissue tumours from localized MR spectra acquired using surface coils. Phys Med Biol 1997; 42: 691-706.
128. Rodrigues LM, Maxwell RJ, McSheehy PM, et al. In vivo detection of ifosfamide by 31P-MRS in rat tumours: increased uptake and cytotoxicity induced by carbogen breathing in GH3 prolactinomas. Br J Cancer 1997; 75: 62-8.
129. Rodrigues LM, Robinson SP, McSheehy PM, Stubbs M, Griffiths JR. Enhanced uptake of ifosfamide into GH3 prolactinomas with hypercapnic hyperoxic gases monitored in vivo by (31)P MRS. Neoplasia 2002; 4: 539-43.
130. 1H nuclear magnetic resonance spectroscopy: effect of 5-fluorouracil on lactate levels in radiation-induced fibrosarcoma 1 tumors. Cancer Res 1998; 58: 1063-7.
131. Bhujwalla ZM, Shungu DC, Glickson JD. Effects of blood flow modifiers on tumor metabolism observed in vivo by proton magnetic resonance spectroscopic imaging. Magn Reson Med 1996; 36: 204-11.
132. Bhujwalla ZM, Glickson JD. Detection of tumor response to radiation therapy by in vivo proton MR spectroscopy. Int J Radiat Oncol Biol Phys 1996; 36: 635-9.
133. Shungu DC, Bhujwalla ZM, Li SJ, Rose LM, Wehrle JP, Glickson JD. Determination of absolute phosphate metabolite concentrations in RIF-1 tumors in vivo by 31P-1H-2H NMR spectroscopy using water as an internal intensity reference. Magn Reson Med 1992; 28: 105-21.
134. Andrew ER, Bradbury A, Eades RG. Removal of dipolar brodadening of nuclear magnetic resonance spectra of solids by specimen rotation. Nature 1959; 183: 1802-3.
135. Lowe IJ. Free induction decays of rotating solids. Phys Rev Lett 1959; 2: 285-287.
136. Cheng LL, Lean CL, Bogdanova A, et al. Enhanced resolution of proton NMR spectra of malignant lymph nodes using magic-angle spinning. Magn Reson Med 1996; 36: 653-8.
137. Cheng LL, Ma MJ, Becerra L, et al. Quantitative neuropathology by high resolution magic angle spinning proton magnetic resonance spectroscopy. Proc Natl Acad Sci USA 1997; 94: 6408-13.
138. Sjobakk TE, Johansen R, Bathen TF, et al. Characterization of brain metastases using high-resolution magic angle spinning MRS. NMR Biomed 2008; 21: 175-85.
139. 1H MRS study of human high grade gliomas. NMR Biomed 2004; 17: 191-205.
140. Sitter B, Sonnewald U, Spraul M, Fjosne HE, Gribbestad IS. High-resolution magic angle spinning MRS of breast cancer tissue. NMR Biomed 2002; 15: 327-37.
141. 1H HR-MAS spectroscopy. Magn Reson Med 2006; 55: 1257-64.
142. Bathen TF, Jensen LR, Sitter B, et al. MR-determined metabolic phenotype of breast cancer in prediction of lymphatic spread, grade, and hormone status. Breast Cancer Res Treat 2007; 104: 181-9.
143. 1H MR spectroscopy for assessment of apoptosis in cervical carcinomas. BMC Cancer 2007; 7: 11.
144. Tzika AA, Astrakas L, Cao H, et al. Combination of high-resolution magic angle spinning proton magnetic resonance spectroscopy and microscale genomics to type brain tumor biopsies. Int J Mol Med 2007; 20: 199-208.
145. Cheng LL, Anthony DC, Comite AR, Black PM, Tzika AA, Gonzalez RG. Quantification of microheterogeneity in glioblastoma multiforme with ex vivo high-resolution magic-angle spinning (HRMAS) proton magnetic resonance spectroscopy. Neuro Oncol 2000; 2: 87-95.
146. 1H NMR spectroscopy reveals different responses in choline-containing metabolites upon gene therapy-induced programmed cell death in rat brain glioma. NMR Biomed 2005; 18: 252-9.
147. 1H MR spectra. Int J Mol Med 2006; 18: 859-69.
148. Ackerstaff E, Glunde K, Bhujwalla ZM. Choline phospholipid metabolism: a target in cancer cells? J Cell Biochem 2003; 90: 525-33.
149. Katz-Brull R, Lavin PT, Lenkinski RE. Clinical utility of proton magnetic resonance spectroscopy in characterizing breast lesions. J Natl Cancer Inst 2002; 94: 1197-203.
150. 1H NMR spectroscopy of colon tumors and normal mucosal biopsies; elevated taurine levels and reduced polyethyleneglycol absorption in tumors may have diagnostic significance. NMR Biomed 1993; 6: 111-8.
151. Cheng LL, Chang IW, Smith BL, Gonzalez RG. Evaluating human breast ductal carcinomas with high-resolution magic-angle spinning proton magnetic resonance spectroscopy. J Magn Reson 1998; 135: 194-202.
152. Wu CL, Taylor JL, He W, et al. Proton high-resolution magic angle spinning NMR analysis of fresh and previously frozen tissue of human prostate. Magn Reson Med 2003; 50: 1307-11.
153. Sitter B, Lundgren S, Bathen TF, Halgunset J, Fjosne HE, Gribbestad IS. Comparison of HR MAS MR spectroscopic profiles of breast cancer tissue with clinical parameters. NMR Biomed 2006; 19: 30-40.
154. 1H HR-MAS spectroscopy of biopsy tissues. Magn Reson Med 2008; 60: 510-6.
155. Martinez-Bisbal MC, Monleon D, Assemat O, et al. Determination of metabolite concentrations in human brain tumour biopsy samples using HR-MAS and ERETIC measurements. NMR Biomed 2009; 22: 199-206.
156. Tyagi RK, Azrad A, Degani H, Salomon Y. Simultaneous extraction of cellular lipids and water-soluble metabolites: evaluation by NMR spectroscopy. Magn Reson Med 1996; 35: 194-200.
157. Podo F, Carpinelli G, Di Vito M, et al. Nuclear magnetic resonance analysis of tumor necrosis factor-induced alterations of phospholipid metabolites and pH in Friend leukemia cell tumors and fibrosarcomas in mice. Cancer Res 1987; 47: 6481-9.
158. 1HNMR spectroscopy. NMR Biomed 2002; 15: 37-44.
159. Henke J, Willker W, Engelmann J, Leibfritz D. Combined extraction techniques of tumour cells and lipid/phospholipid assignment by two dimensional NMR spectroscopy. Anticancer Res 1996; 16: 1417-27.
160. Podo F, Ferretti A, Knijn A, et al. Detection of phosphatidylcholine-specific phospholipase C in NIH-3T3 fibroblasts and their H-ras transformants: NMR and immunochemical studies. Anticancer Res 1996; 16: 1399-412.
161. Iorio E, Mezzanzanica D, Alberti P, et al. Alterations of choline phospholipid metabolism in ovarian tumor progression. Cancer Res 2005; 65: 9369-76.
162. Wevers RA, Engelke UF, Moolenaar SH, et al. 1H-NMR spectroscopy of body fluids: inborn errors of purine and pyrimidine metabolism. Clin Chem 1999; 45: 539-48.
163. Moolenaar SH, Gohlich-Ratmann G, Engelke UF, et al. Beta-ureidopropionase deficiency: a novel inborn error of metabolism discovered using NMR spectroscopy on urine. Magn Reson Med 2001; 46: 1014-7.
164. Street JC, Mahmood U, Matei C, Koutcher JA. in vivo and in vitro studies of cyclophosphamide chemotherapy in a mouse mammary carcinoma by 31P NMR spectroscopy. NMR Biomed 1995; 8: 149-58.
165. Lenz EM, Wilson ID, Wright B, et al. A comparison of quantitative NMR and radiolabelling studies of the metabolism and excretion of Statil (3-(4-bromo-2-fluorobenzyl)-4-oxo-3H-phthalazin-1-ylacetic acid) in the rat. J Pharm Biomed Anal 2002; 28: 31-43.
166. Monte SY, Ismail I, Mallett DN, Matthews C, Tanner RJ. The minimal metabolism of inhaled 1,1,1,2-tetrafluoroethane to trifluoroacetic acid in man as determined by high sensitivity 19F nuclear magnetic resonance spectroscopy of urine samples. J Pharm Biomed Anal 1994; 12: 1489-93.
167. Busse D, Busch FW, Bohnenstengel F, et al. Dose escalation of cyclophosphamide in patients with breast cancer: consequences for pharmacokinetics and metabolism. J Clin Oncol 1997; 15: 1885-96.