A decade in prostate cancer: From NMR to metabolomics

Nature Reviews Urology

Volumn 8, Issue 6, 2011, Pages 301-311

  DeFeo, Elita M ^a   Wu, Chin Lee ^a   McDougal, W Scott ^a   Cheng, Leo L ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACCURACY; CANCER PATIENT; CLINICAL PRACTICE; EX VIVO STUDY; HUMAN; IN VIVO STUDY; METABOLOMICS; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PATIENT CARE; PRIORITY JOURNAL; PROSTATE CANCER; REVIEW; TECHNOLOGY;

ANIMALS; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MALE; METABOLOMICS; PROSTATIC NEOPLASMS;

EID: 79958856339     PISSN: 17594812     EISSN: 17594820     Source Type: Journal    
DOI: 10.1038/nrurol.2011.53     Document Type: Review

References (167)

1. Damadian, R. Tumor detection by nuclear magnetic resonance. Science 171, 1151-1153 (1971).
2. Mansfield, P., Grannell, P. K., Garroway, A. N. & Stalker, D. C. in Proceedings of the 1st Specialized AMPERE Colloquium 16-27 (Krakow, Poland, 1973).
3. Lauterbur, P. Image formation by induced local interations: examples employing nuclear magnetic resonance. Nature 242, 190-191 (1973).
4. Ambrose, J. & Hounsfield, G. Computerized transverse axial tomography. Br. J. Radiol. 46, 148-149 (1973).
5. Hounsfield, G. N. Computerized transverse axial scanning (tomography). 1. Description of system. Br. J. Radiol. 46, 1016-1022 (1973).
6. McCook, A. Life after fraud. The Scientist 23, 28 (2009).
7. Findings of Scientific Misconduct NIH Guide. 25 (1996).
8. Fossel, E. T., Carr, J. M. & McDonagh, J. Detection of malignant tumors. Water-suppressed proton nuclear magnetic resonance spectroscopy of plasma. N. Engl. J. Med. 315, 1369-1376 (1986).
9. Andrew, E., Bradbury, A. & Eades, R. Nuclear magnetic resonance spectra from a crystal rotated at high speed. Nature 182, 1695 (1958).
10. Cheng, L. L. et al. Enhanced resolution of proton NMR spectra of malignant lymph nodes using magic-angle spinning. Magn. Reson. Med. 36, 653-658 (1996).
11. Cheng, L. L. et al. Quantitative neuropathology by high resolution magic angle spinning proton magnetic resonance spectroscopy. Proc. Natl Acad. Sci. USA 94, 6408-6413 (1997).
12. Cheng, L. L. et al. Quantification of microheterogeneity in glioblastoma multiforme with ex vivo high-resolution magic-angle spinning (HRMAS) proton magnetic resonance spectroscopy. Neuro Oncol. 2, 87-95 (2000).
13. Cheng, L. L., Wu, C., Smith, M. R. & Gonzalez, R. G. Non-destructive quantitation of spermine in human prostate tissue samples using HRMAS 1H NMR spectroscopy at 9.4 T. FEBS Lett. 494, 112-116 (2001).
14. Cheng, L. L. & Pohl, U. in The Handbook of Metabonomics and Metabolomics (eds Lindon, J. C., Nicholls, J. K. & Holmes, E.) 345-374 (Elsevier, Amsterdam, 2007).
15. van der Graaf, M. et al. Proton MR spectroscopy of prostatic tissue focused on the detection of spermine, a possible biomarker of malignant behavior in prostate cancer. MAGMA 10, 153-159 (2000).
16. Smith, R., Litwin, M., Lu, Y. & Zetter, B. Identification of an endogenous inhibitor of prostate carcinoma cell growth. Nat. Med. 1, 1040-1045 (1995).
17. Swindle, P. et al. Pathologic characterization of human prostate tissue with proton MR spectroscopy. Radiology 228, 144-151 (2003).
18. Menard, C. et al. Magnetic resonance spectroscopy of the malignant prostate gland after radiotherapy: a histopathologic study of diagnostic validity. Int. J. Radiat. Oncol. Biol. Phys. 50, 317-323 (2001).
19. Costello, L. C., Franklin, R. B., Feng, P., Tan, M. & Bagasra, O. Zinc and prostate cancer: a critical scientific, medical, and public interest issue (United States). Cancer Causes Control 16, 901-915 (2005).
20. Serkova, N. J. et al. The metabolites citrate, myo-inositol, and spermine are potential age-independent markers of prostate cancer in human expressed prostatic secretions. Prostate 68, 620-628 (2008).
21. Kline, E. E. et al. Citrate concentrations in human seminal fluid and expressed prostatic fluid determined via 1H nuclear magnetic resonance spectroscopy outperform prostate specific antigen in prostate cancer detection. J. Urol. 176, 2274-2279 (2006).
22. Averna, T. A., Kline, E. E., Smith, A. Y. & Sillerud, L. O. A decrease in 1H nuclear magnetic resonance spectroscopically determined citrate in human seminal fluid accompanies the development of prostate adenocarcinoma. J. Urol. 173, 433-438 (2005).
23. Swanson, M. G. et al. Proton HR-MAS spectroscopy and quantitative pathologic analysis of MRI/3D-MRSI-targeted postsurgical prostate tissues. Magn. Reson. Med. 50, 944-954 (2003).
24. van Asten, J. J. et al. High resolution magic angle spinning NMR spectroscopy for metabolic assessment of cancer presence and Gleason score in human prostate needle biopsies. MAGMA 21, 435-442 (2008).
25. Tessem, M. B. et al. Evaluation of lactate and alanine as metabolic biomarkers of prostate cancer using 1H HR-MAS spectroscopy of biopsy tissues. Magn. Reson. Med. 60, 510-516 (2008).
26. Stenman, K. et al. Detection of polyunsaturated omega-6 fatty acid in human malignant prostate tissue by 1D and 2D high-resolution magic angle spinning NMR spectroscopy. MAGMA 22, 327-331 (2009).
27. Swanson, M. G. et al. Quantification of choline and ethanolamine- containing metabolites in human prostate tissues using 1H HR-MAS total correlation spectroscopy. Magn. Reson. Med. 60, 33-40 (2008).
28. Swanson, M. G. et al. Quantitative analysis of prostate metabolites using 1H HR-MAS spectroscopy. Magn. Reson. Med. 55, 1257-1264 (2006).
29. Komoroski, R. A., Holder, J. C., Pappas, A. A. & Finkbeiner, A. E. (31)P NMR of phospholipid metabolites in prostate cancer and benign prostatic hyperplasia. Magn. Reson. Med. 65, 911-913 (2011).
30. Taylor, J. L. et al. High-resolution magic angle spinning proton NMR analysis of human prostate tissue with slow spinning rates. Magn. Reson. Med. 50, 627-632 (2003).
31. Burns, M. A. et al. Reduction of spinning sidebands in proton NMR of human prostate tissue with slow high-resolution magic angle spinning. Magn. Reson. Med. 54, 34-42 (2005).
32. Jordan, K. W., He, W., Halpern, E. F., Wu, C. L. & Cheng, L. L. Evaluation of tissue metabolites with high resolution magic angle spinning MR spectroscopy human prostate samples after three-year storage at -80°C. Biomark. Insights 2, 147-154 (2007).
33. Wu, C. L. et al. Proton high-resolution magic angle spinning NMR analysis of fresh and previously frozen tissue of human prostate. Magn. Reson. Med. 50, 1307-1311 (2003).
34. Zektzer, A. S. et al. Improved signal to noise in high-resolution magic angle spinning total correlation spectroscopy studies of prostate tissues using rotor-synchronized adiabatic pulses. Magn. Reson. Med. 53, 41-48 (2005).
35. Ratiney, H., Albers, M. J., Rabeson, H. & Kurhanewicz, J. Semi-parametric time-domain quantification of HR-MAS data from prostate tissue. NMR Biomed. 23, 1146-1157 (2010).
36. Burns, M. A., He, W., Wu, C. L. & Cheng, L. L. Quantitative pathology in tissue MR spectroscopy based human prostate metabolomics. Technol. Cancer Res. Treat. 3, 591-598 (2004).
37. Cheng, L. L. et al. Metabolic characterization of human prostate cancer with tissue magnetic resonance spectroscopy. Cancer Res. 65, 3030-3034 (2005).
38. Sciarra, A. Words of wisdom. Re: Retrospective analysis of prostate cancer recurrence potential with tissue metabolomic profiles. Maxeiner A, Adkins CB, Zhang Y. et al. Prostate 2010;70, 710-717.
39. Eur. Urol. 58, 315 (2010).
40. Maxeiner, A. et al. Retrospective analysis of prostate cancer recurrence potential with tissue metabolomic profiles. Prostate 70, 710-717 (2010).
41. Kurhanewicz, J. et al. Three-dimensional H-1 MR spectroscopic imaging of the in situ human prostate with high (0.24-07-cm3) spatial resolution. Radiology 198, 795-805 (1996).
42. Kurhanewicz, J. et al. Citrate as an in vivo marker to discriminate prostate cancer from benign prostatic hyperplasia and normal prostate peripheral zone: detection via localized proton spectroscopy. Urology 45, 459-466 (1995).
43. Star-Lack, J., Nelson, S., Kurhanewicz, J., Huang, L. & Vigneron, D. Improved water and lipid suppression for 3D PRESS CSI using RF band selective inversion with gradient dephasing (BASING). Magn. Reson. Med. 38, 311-321 (1997).
44. Star-Lack, J., Vigneron, D. B., Pauly, J., Kurhanewicz, J. & Nelson, S. J. 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 7, 745-757 (1997).
45. Pucar, D. et al. Prostate cancer: correlation of MR imaging and MR spectroscopy with pathologic findings after radiation therapy - initial experience. Radiology 236, 545-553 (2005).
46. Villeirs, G. M. et al. Combined magnetic resonance imaging and spectroscopy in the assessment of high grade prostate carcinoma in patients with elevated PSA: a single-institution experience of 356 patients. Eur. J. Radiol. 77, 340-345 (2011).
47. Villeirs, G. M., Oosterlinck, W., Vanherreweghe, E. & De Meerleer, G. O. A qualitative approach to combined magnetic resonance imaging and spectroscopy in the diagnosis of prostate cancer. Eur. J. Radiol. 73, 352-356 (2008).
48. Mueller-Lisse, U. G. et al. Localized prostate cancer: effect of hormone deprivation therapy measured by using combined three-dimensional 1H MR spectroscopy and MR imaging: clinicopathologic case-controlled study. Radiology 221, 380-390 (2001).
49. Zakian, K. L. et al. Transition zone prostate cancer: metabolic characteristics at 1H MR spectroscopic imaging--initial results. Radiology 229, 241-247 (2003).
50. Fradet, V. et al. Prostate cancer managed with active surveillance: role of anatomic MR imaging and MR spectroscopic imaging. Radiology 256, 176-183 (2010).
51. Zhang, J. et al. Clinical stage T1c prostate cancer: evaluation with endorectal MR imaging and MR spectroscopic imaging. Radiology 253, 425-434 (2009).
52. Jung, J. A. et al. Prostate depiction at endorectal MR spectroscopic imaging: investigation of a standardized evaluation system. Radiology 233, 701-708 (2004).
53. Wetter, A. et al. Combined MRI and MR spectroscopy of the prostate before radical prostatectomy. AJR Am. J. Roentgenol. 187, 724-730 (2006).
54. Portalez, D. et al. Prospective comparison of T2w-MRI and dynamic-contrast-enhanced MRI, 3D-MR spectroscopic imaging or diffusion-weighted MRI in repeat TRUS-guided biopsies. Eur. Radiol. 20, 2781-2790 (2010).
55. Coakley, F. V. et al. Prostate cancer tumor volume: measurement with endorectal MR and MR spectroscopic imaging. Radiology 223, 91-97 (2002).
56. Hasumi, M. et al. The combination of multi-voxel MR spectroscopy with MR imaging improve the diagnostic accuracy for localization of prostate cancer. Anticancer Res. 23, 4223-4227 (2003).
57. Hom, J. J. et al. High-grade prostatic intraepithelial neoplasia in patients with prostate cancer: MR and MR spectroscopic imaging features--initial experience. Radiology 242, 483-489 (2007).
58. Chabanova, E. et al. Prostate cancer: 1.5 T endo-coil dynamic contrast-enhanced MRI and MR spectroscopy-correlation with prostate biopsy and prostatectomy histopathological data. Eur. J. Radiol. doi:10.1016/j.ejrad.2010. 07.004.
59. Xu, S. et al. Real-time MRI-TRUS fusion for guidance of targeted prostate biopsies. Comput. Aided Surg. 13, 255-264 (2008).
60. Testa, C. et al. Accuracy of MRI/MRSI-based transrectal ultrasound biopsy in peripheral and transition zones of the prostate gland in patients with prior negative biopsy. NMR Biomed. 23, 1017-1026 (2010).
61. Prando, A., Kurhanewicz, J., Borges, A. P., Oliveira, E. M. Jr & Figueiredo, E. Prostatic biopsy directed with endorectal MR spectroscopic imaging findings in patients with elevated prostate specific antigen levels and prior negative biopsy findings: early experience. Radiology 236, 903-910 (2005).
62. Kumar, V. et al. Transrectal ultrasound-guided biopsy of prostate voxels identified as suspicious of malignancy on three-dimensional (1)H MR spectroscopic imaging in patients with abnormal digital rectal examination or raised prostate specific antigen level of 4-10 ng/ml. NMR Biomed. 20, 11-20 (2007).
63. Manenti, G. et al. Magnetic resonance imaging of the prostate with spectroscopic imaging using a surface coil. Initial clinical experience. Radiol. Med. 111, 22-32 (2006).
64. Hata, N. et al. MR imaging-guided prostate biopsy with surgical navigation software: device validation and feasibility. Radiology 220, 263-268 (2001).
65. Lagerburg, V., Moerland, M. A., van Vulpen, M. & Lagendijk, J. J. A new robotic needle insertion method to minimise attendant prostate motion. Radiother. Oncol. 80, 73-77 (2006).
66. Rodriguez, O. et al. Contrast-enhanced in vivo imaging of breast and prostate cancer cells by MRI. Cell Cycle 5, 113-119 (2006).
67. Krieger, A. et al. Design of a novel MRI compatible manipulator for image guided prostate interventions. IEEE Trans. Biomed. Eng. 52, 306-313 (2005).
68. Mozer, P. C., Partin, A. W. & Stoianovici, D. Robotic image-guided needle interventions of the prostate. Rev. Urol. 11, 7-15 (2009).
69. Zelefsky, M. J. et al. Intraoperative conformal optimization for transperineal prostate implantation using magnetic resonance spectroscopic imaging. Cancer J. 6, 249-255 (2000).
70. DiBiase, S. J. et al. Magnetic resonance spectroscopic imaging-guided brachytherapy for localized prostate cancer. Int. J. Radiat. Oncol. Biol. Phys. 52, 429-438 (2002).
71. Kirilova, A. et al. 3D MR-Spectroscopic Imaging assessment of metabolic activity in the prostate during the PSA "bounce" following (125)Iodine brachytherapy. Int. J. Radiat. Oncol. Biol. Phys. 79, 371-378 (2011).
72. Kim, Y. et al. Class solution in inverse planned HDR prostate brachytherapy for dose escalation of DIL defined by combined MRI/MRSI. Radiother. Oncol. 88, 148-155 (2008).
73. Kazi, A., Godwin, G., Simpson, J. & Sasso, G. MRS-guided HDR brachytherapy boost to the dominant intraprostatic lesion in high risk localised prostate cancer. BMC Cancer 10, 472 (2010).
74. Mueller-Lisse, U. G. 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. 46, 49-57 (2001).
75. Pickett, B. et al. Use of MRI and spectroscopy in evaluation of external beam radiotherapy for prostate cancer. Int. J. Radiat. Oncol. Biol. Phys. 60, 1047-1055 (2004).
76. Coakley, F. V. et al. Endorectal MR imaging and MR spectroscopic imaging for locally recurrent prostate cancer after external beam radiation therapy: preliminary experience. Radiology 233, 441-448 (2004).
77. Pucar, D. et al. Preliminary assessment of magnetic resonance spectroscopic imaging in predicting treatment outcome in patients with prostate cancer at high risk for relapse. Clin. Prostate Cancer 3, 174-181 (2004).
78. Sciarra, A. et al. Role of dynamic contrast-enhanced magnetic resonance (MR) imaging and proton MR spectroscopic imaging in the detection of local recurrence after radical prostatectomy for prostate cancer. Eur. Urol. 54, 589-600 (2008).
79. Zakian, K. L. et al. An exploratory study of endorectal magnetic resonance imaging and spectroscopy of the prostate as preoperative predictive biomarkers of biochemical relapse after radical prostatectomy. J. Urol. 184, 2320-2327 (2010).
80. Weinreb, J. C. et al. Prostate cancer: sextant localization at MR imaging and MR spectroscopic imaging before prostatectomy - results of ACRIN prospective multi-institutional clinicopathologic study. Radiology 251, 122-133 (2009).
81. Chen, A. P. et al. High-resolution 3D MR spectroscopic imaging of the prostate at 3 T with the MLEV-PRESS sequence. Magn. Reson. Imaging 24, 825-832 (2006).
82. Futterer, J. J. et al. Initial experience of 3 tesla endorectal coil magnetic resonance imaging and 1H-spectroscopic imaging of the prostate. Invest. Radiol. 39, 671-680 (2004).
83. Futterer, J. J. et al. Prostate cancer: local staging at 3-T endorectal MR imaging - early experience. Radiology 238, 184-191 (2006).
84. Crehange, G. et al. Tumor volume and metabolism of prostate cancer determined by proton magnetic resonance spectroscopic imaging at 3T without endorectal coil reveal potential clinical implications in the context of radiation oncology. Int. J. Radiat. Oncol. Biol. Phys. doi:10.1016/j.ijrobp. 2010.03.007.
85. McLean, M. A. et al. Prostate cancer metabolite quantification relative to water in (1)H-MRSI in vivo at 3 Tesla. Magn. Reson. Med. 65, 914-919 (2011).
86. Near, J. et al. High-field MRSI of the prostate using a transmit/receive endorectal coil and gradient modulated adiabatic localization. J. Magn. Reson. Imaging 30, 335-343 (2009).
87. Pinkerton, R. G., Near, J. P., Barberi, E. A., Menon, R. S. & Bartha, R. Transceive surface coil array for MRI of the human prostate at 4T. Magn. Reson. Med. 57, 455-458 (2007).
88. Klomp, D. W., Bitz, A. K., Heerschap, A. & Scheenen, T. W. Proton spectroscopic imaging of the human prostate at 7 T. NMR Biomed. 22, 495-501 (2009).
89. Choi, H. & Ma, J. Use of perfluorocarbon compound in the endorectal coil to improve MR spectroscopy of the prostate. AJR Am. J. Roentgenol. 190, 1055-1059 (2008).
90. Rosen, Y. et al. 3T MR of the prostate: reducing susceptibility gradients by inflating the endorectal coil with a barium sulfate suspension. Magn. Reson. Med. 57, 898-904 (2007).
91. Scheidler, J., Vogel, M., Gross, P. & Heuck, A. Combined MRI and MRS in prostate cancer: improvement of spectral quality by susceptibility matching. Rofo 181, 531-535 (2009).
92. Males, R. G. et al. Clinical application of BASING and spectral/spatial water and lipid suppression pulses for prostate cancer staging and localization by in vivo 3D 1H magnetic resonance spectroscopic imaging. Magn. Reson. Med. 43, 17-22 (2000).
93. Pels, P. et al. Quantification of prostate MRSI data by model-based time domain fitting and frequency domain analysis. NMR Biomed. 19, 188-197 (2006).
94. Kelm, B. M., Menze, B. H., Zechmann, C. M., Baudendistel, K. T. & Hamprecht, F. A. Automated estimation of tumor probability in prostate magnetic resonance spectroscopic imaging: pattern recognition vs quantification. Magn. Reson. Med. 57, 150-159 (2007).
95. Tiwari, P., Rosen, M. & Madabhushi, A. A hierarchical spectral clustering and nonlinear dimensionality reduction scheme for detection of prostate cancer from magnetic resonance spectroscopy (MRS). Med. Phys. 36, 3927-3939 (2009).
96. Ahmed, H. U. et al. Is it time to consider a role for MRI before prostate biopsy? Nat. Rev. Clin. Oncol. 6, 197-206 (2009).
97. Wu, C. L. et al. Metabolomic imaging for human prostate cancer detection. Sci. Transl. Med. 2, 16ra8 (2010).
98. Ackerstaff, E., Pflug, B. R., Nelson, J. B. & Bhujwalla, Z. M. Detection of increased choline compounds with proton nuclear magnetic resonance spectroscopy subsequent to malignant transformation of human prostatic epithelial cells. Cancer Res. 61, 3599-3603 (2001).
99. Ippolito, J. E. et al. Linkage between cellular communications, energy utilization, and proliferation in metastatic neuroendocrine cancers. Proc. Natl Acad. Sci. USA 103, 12505-12510 (2006).
100. Dyke, J. P. et al. Metabolic response of the CWR22 prostate tumor xenograft after 20 Gy of radiation studied by 1H spectroscopic imaging. Clin. Cancer Res. 9, 4529-4536 (2003).
101. Rantalainen, M. et al. Statistically integrated metabonomic-proteomic studies on a human prostate cancer xenograft model in mice. J. Proteome Res. 5, 2642-2655 (2006).
102. Milkevitch, M., Jeitner, T. M., Beardsley, N. J. & Delikatny, E. J. Lovastatin enhances phenylbutyrate-induced MR-visible glycerophosphocholine but not apoptosis in DU145 prostate cells. Biochim. Biophys. Acta 1771, 1166-1176 (2007).
103. Gabellieri, C. et al. Modulation of choline kinase activity in human cancer cells observed by dynamic 31P NMR. NMR Biomed. 22, 456-461 (2009).
104. Levin, Y. S. et al. Methods for metabolic evaluation of prostate cancer cells using proton and (13)C HR-MAS spectroscopy and [3-(13)C] pyruvate as a metabolic substrate. Magn. Reson. Med. 62, 1091-1098 (2009).
105. Robey, I. F. et al. Bicarbonate increases tumor pH and inhibits spontaneous metastases. Cancer Res. 69, 2260-2268 (2009).
106. Ackerstaff, E., Artemov, D., Gillies, R. J. & Bhujwalla, Z. M. Hypoxia and the presence of human vascular endothelial cells affect prostate cancer cell invasion and metabolism. Neoplasia 9, 1138-1151 (2007).
107. Al-Saffar, N. M. et al. The phosphoinositide 3-kinase inhibitor PI-103 downregulates choline kinase alpha leading to phosphocholine and total choline decrease detected by magnetic resonance spectroscopy. Cancer Res. 70, 5507-5517 (2010).
108. Raina, K., Serkova, N. J. & Agarwal, R. Silibinin feeding alters the metabolic profile in TRAMP prostatic tumors: 1H-NMRS-based metabolomics study. Cancer Res. 69, 3731-3735 (2009).
109. Larson, P. E. et al. Investigation of tumor hyperpolarized [1-13C]-pyruvate dynamics using time-resolved multiband RF excitation echo-planar MRSI. Magn. Reson. Med. 63, 582-591 (2010).
110. Albers, M. J. et al. Hyperpolarized 13C lactate, pyruvate, and alanine: noninvasive biomarkers for prostate cancer detection and grading. Cancer Res. 68, 8607-8615 (2008).
111. Cunningham, C. H. et al. Sequence design for magnetic resonance spectroscopic imaging of prostate cancer at 3 T. Magn. Reson. Med. 53, 1033-1039 (2005).
112. Scheenen, T. W. et al. Optimal timing for in vivo 1H-MR spectroscopic imaging of the human prostate at 3T. Magn. Reson. Med. 53, 1268-1274 (2005).
113. Trabesinger, A. H., Meier, D., Dydak, U., Lamerichs, R. & Boesiger, P. Optimizing PRESS localized citrate detection at 3 Tesla. Magn. Reson. Med. 54, 51-58 (2005).
114. Gambarota, G., van der Graaf, M., Klomp, D., Mulkern, R. V. & Heerschap, A. Echo-time independent signal modulations using PRESS sequences: a new approach to spectral editing of strongly coupled AB spin systems. J. Magn. Reson. 177, 299-306 (2005).
115. Lange, T., Trabesinger, A. H., Schulte, R. F., Dydak, U. & Boesiger, P. Prostate spectroscopy at 3 Tesla using two-dimensional S.-PRESS. Magn. Reson. Med. 56, 1220-1228 (2006).
116. Chen, A. P. et al. High-speed 3T MR spectroscopic imaging of prostate with flyback echo-planar encoding. J. Magn. Reson. Imaging 25, 1288-1292 (2007).
117. Weis, J. et al. Two-dimensional spectroscopic imaging for pretreatment evaluation of prostate cancer: comparison with the step-section histology after radical prostatectomy. Magn. Reson. Imaging 27, 87-93 (2009).
118. Thomas, M. A. et al. Two-dimensional MR spectroscopy of healthy and cancerous prostates in vivo. MAGMA 21, 443-458 (2008).
119. Near, J., Romagnoli, C. & Bartha, R. Reduced power magnetic resonance spectroscopic imaging of the prostate at 4.0 Tesla. Magn. Reson. Med. 61, 273-281 (2009).
120. Thakur, S. B., Yaligar, J. & Koutcher, J. A. In vivo lactate signal enhancement using binomial spectral-selective pulses in selective MQ coherence (SS-SelMQC) spectroscopy. Magn. Reson. Med. 62, 591-598 (2009).
121. Bertilsson, H. et al. A new method to provide a fresh frozen prostate slice suitable for gene expression study and MR spectroscopy. Prostate 71, 461-469 (2011).
122. Lenkinski, R. E. et al. An illustration of the potential for mapping MRI/MRS parameters with genetic over-expression profiles in human prostate cancer. MAGMA 21, 411-421 (2008).
123. Santos, C. F. et al. Metabolic, pathologic, and genetic analysis of prostate tissues: quantitative evaluation of histopathologic and mRNA integrity after HR-MAS spectroscopy. NMR Biomed. 23, 391-398 (2010).
124. Shukla-Dave, A. et al. Correlation of MR imaging and MR spectroscopic imaging findings with Ki-67, phospho-Akt, and androgen receptor expression in prostate cancer. Radiology 250, 803-812 (2009).
125. Kaul, D. et al. Assessing prostate cancer growth with mRNA of spermine metabolic enzymes. Cancer Biol. Ther. 9, 736-742 (2010).
126. Jhavar, S. G. et al. Processing of radical prostatectomy specimens for correlation of data from histopathological, molecular biological, and radiological studies: a new whole organ technique. J. Clin. Pathol. 58, 504-508 (2005).
127. Zhan, Y., Feldman, M., Tomaszeweski, J., Davatzikos, C. & Shen, D. Registering histological and MR images of prostate for image-based cancer detection. Med. Image Comput. Comput. Assist. Interv. 9, 620-628 (2006).
128. Alterovitz, R., Goldberg, K., Kurhanewicz, J., Pouliot, J. & Hsu, I. C. Image registration for prostate MR spectroscopy using modeling and optimization of force and stiffness parameters. Conf. Proc. IEEE Eng. Med. Biol. Soc. 3, 1722-1725 (2004).
129. Park, H. et al. Registration methodology for histological sections and in vivo imaging of human prostate. Acad. Radiol. 15, 1027-1039 (2008).
130. McGrath, D. M., Vlad, R. M., Foltz, W. D. & Brock, K. K. Technical note: fiducial markers for correlation of whole-specimen histopathology with MR imaging at 7 tesla. Med. Phys. 37, 2321-2328 (2010).
131. Shah, V. et al. A method for correlating in vivo prostate magnetic resonance imaging and histopathology using individualized magnetic resonance-based molds. Rev. Sci. Instrum. 80, 104301 (2009).
132. Mazaheri, Y. et al. Semi-automatic deformable registration of prostate MR images to pathological slices. J. Magn. Reson. Imaging 32, 1149-1157 (2010).
133. Ozer, S. et al. Supervised and unsupervised methods for prostate cancer segmentation with multispectral MRI. Med. Phys. 37, 1873-1883 (2010).
134. Sciarra, A. et al. Value of magnetic resonance spectroscopy imaging and dynamic contrast-enhanced imaging for detecting prostate cancer foci in men with prior negative biopsy. Clin. Cancer Res. 16, 1875-1883 (2010).
135. Wang, X. Z. et al. 1H-MRSI of prostate cancer: the relationship between metabolite ratio and tumor proliferation. Eur. J. Radiol. 73, 345-351 (2010).
136. Westphalen, A. C. et al. Peripheral zone prostate cancer: accuracy of different interpretative approaches with MR and MR spectroscopic imaging. Radiology 246, 177-184 (2008).
137. Vilanova, J. C. et al. Peripheral zone prostate cancer in patients with elevated PSA levels and low free-to-total PSA ratio: detection with MR imaging and MR spectroscopy. Radiology 253, 135-143 (2009).
138. Kumar, V. et al. Potential of (1)H MR spectroscopic imaging to segregate patients who are likely to show malignancy of the peripheral zone of the prostate on biopsy. J. Magn. Reson. Imaging 30, 842-848 (2009).
139. Cazares, L. H. et al. Imaging mass spectrometry of a specific fragment of mitogen-activated protein kinase/extracellular signal-regulated kinase kinase kinase 2 discriminates cancer from uninvolved prostate tissue. Clin. Cancer Res. 15, 5541-5551 (2009).
140. Eberlin, L. S. et al. Cholesterol sulfate imaging in human prostate cancer tissue by desorption electrospray ionization mass spectrometry. Anal. Chem. 82, 3430-3434 (2010).
141. Schwamborn, K. et al. Identifying prostate carcinoma by MALDI-Imaging. Int. J. Mol. Med. 20, 155-159 (2007).
142. Sreekumar, A. et al. Metabolomic profiles delineate potential role for sarcosine in prostate cancer progression. Nature 457, 910-914 (2009).
143. Jentzmik, F. et al. Sarcosine in prostate cancer tissue is not a differential metabolite for prostate cancer aggressiveness and biochemical progression. J. Urol. 185, 706-711 (2011).
144. Jiang, Y., Cheng, X., Wang, C. & Ma, Y. Quantitative determination of sarcosine and related compounds in urinary samples by liquid chromatography with tandem mass spectrometry. Anal. Chem. 82, 9022-9027 (2010).
145. Jentzmik, F. et al. Sarcosine in urine after digital rectal examination fails as a marker in prostate cancer detection and identification of aggressive tumours. Eur. Urol. 58, 12-18 (2010).
146. Delongchamps, N. B. et al. Multiparametric magnetic resonance imaging for the detection and localization of prostate cancer: combination of T2-weighted, dynamic contrast-enhanced and diffusion-weighted imaging. BJU Int. doi:10.1111/j.1464410X.2010.09808.x.
147. Scherr, M. K. et al. MR-perfusion (MRP) and diffusion-weighted imaging (DWI) in prostate cancer: quantitative and model-based gadobenate dimeglumine MRP parameters in detection of prostate cancer. Eur. J. Radiol. 76, 359-366 (2010).
148. Schmuecking, M. et al. Dynamic MRI and CAD vs. choline MRS: where is the detection level for a lesion characterisation in prostate cancer? Int. J. Radiat. Biol. 85, 814-824 (2009).
149. Langer, D. L. et al. Prostate cancer detection with multi-parametric MRI: logistic regression analysis of quantitative T2, diffusion-weighted imaging, and dynamic contrast-enhanced MRI. J. Magn. Reson. Imaging 30, 327-334 (2009).
150. Chen, M. 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. 49, 602-610 (2008).
151. Carlani, M., Mancino, S., Bonanno, E., Finazzi Agro, E. & Simonetti, G. Combined morphological, [1H]-MR spectroscopic and contrast-enhanced imaging of human prostate cancer with a 3-Tesla scanner: preliminary experience. Radiol. Med. 113, 670-688 (2008).
152. Testa, C. et al. Prostate cancer: sextant localization with MR imaging, MR spectroscopy, and 11C-choline PET/CT. Radiology 244, 797-806 (2007).
153. Yamaguchi, T. et al. Prostate cancer: a comparative study of 11C-choline PET and MR imaging combined with proton MR spectroscopy. Eur. J. Nucl. Med. Mol. Imaging 32, 742-748 (2005).
154. Schreibmann, E. & Xing, L. Narrow band deformable registration of prostate magnetic resonance imaging, magnetic resonance spectroscopic imaging, and computed tomography studies. Int. J. Radiat. Oncol. Biol. Phys. 62, 595-605 (2005).
155. Grosu, A. L., Wiedenmann, N. & Molls, M. Biological imaging in radiation oncology. Z. Med. Phys. 15, 141-145 (2005).
156. Eggleston, J. C., Saryan, L. A. & Hollis, D. P. Nuclear magnetic resonance investigations of human neoplastic and abnormal nonneoplastic tissues. Cancer Res. 35, 1326-1332 (1975).
157. Steyn, J. H. & Smith, F. W. Nuclear magnetic resonance imaging of the prostate. Br. J. Urol. 54, 726-728 (1982).
158. Sillerud, L., Halliday, K., Griffey, R., Fenoglio-Preiser, C. & Sheppard, S. In vivo 13C NMR spectroscopy of the human prostate. Magn. Reson. Med. 8, 224-230 (1988).
159. Narayan, P. et al. Characterization of prostate cancer, benign prostatic hyperplasia and normal prostates using transrectal 31phosphorus magnetic resonance spectroscopy: a preliminary report. J. Urol. 146, 66-74 (1991).
160. Schick, F. et al. Localized proton MR spectroscopy of citrate in vitro and of the human prostate in vivo at 1.5 T. Magn. Reson. Med. 29, 38-43 (1993).
161. Schiebler, M. L., Miyamoto, K. K., White, M., Maygarden, S. J. & Mohler, J. L. In vitro high resolution 1H-spectroscopy of the human prostate: benign prostatic hyperplasia, normal peripheral zone and adenocarcinoma. Magn. Reson. Med. 29, 285-291 (1993).
162. Lynch, M. & Nicholson, J. Proton MRS of human prostatic fluid: correlations between citrate, spermine, and myo-inositol levels and changes with disease. Prostate 30, 248-255 (1997).
163. Hahn, P. et al. The classification of benign and malignant human prostate tissue by multivariate analysis of 1H magnetic resonance spectra. Cancer Res. 57, 3398-3401 (1997).
164. van Dorsten, F. A. et al. Combined quantitative dynamic contrast-enhanced MR imaging and (1)H MR spectroscopic imaging of human prostate cancer. J. Magn. Reson. Imaging 20, 279-287 (2004).
165. Wang, L. et al. Prediction of organ-confined prostate cancer: incremental value of MR imaging and MR spectroscopic imaging to staging nomograms. Radiology 238, 597-603 (2006).
166. Coakley, F. V. et al. Validity of prostate-specific antigen as a tumour marker in men with prostate cancer managed by watchful-waiting: correlation with findings at serial endorectal magnetic resonance imaging and spectroscopic imaging. BJU Int. 99, 41-45 (2007).
167. Shukla-Dave, A. et al. Prediction of prostate cancer recurrence using magnetic resonance imaging and molecular profiles. Clin. Cancer Res. 15, 3842-3849 (2009).