The Role of in vivo Proton Magnetic Resonance Spectroscopy (MRS) in the Evaluation of Breast and Prostate Cancers

Uma Sharma, Naranamangalam R Jagannathan

Abstract


In vivo proton (1H) magnetic resonance spectroscopy (MRS) has evolved as a non-invasive technique for the investigation of cancer biochemistry and metabolism. As an adjunct to magnetic resonance imaging,MRS plays a promising role in increasing the specificity of cancer diagnosis and assessment of treatment response in breast and prostate cancers. Various breast MRS studies have documented water-to-fat ratio(W-F) and a peak at 3.2 ppm corresponding to various choline (Cho) containing compounds as promising biomarkers for the diagnosis of breastcancer. Recent breast MRS studies have also documented the determinationof the absolute concentration of tCho metabolite, and cut-off valueswere determined for the discrimination of malignant, benign and normalbreast tissues. MRS parameters like W-F ratio and the concentration oftCho have also been evaluated as useful biomarkers for monitoring therapeuti cresponse of breast cancer patients. Prostate cancer (PCa) is themost common malignancy affecting men. The measurements of relative levels of citrate (Cit), creatine (Cr), Cho, and polyamines (PA) using 1HMRS have established lower Cit and high Cho levels as characteristics ofPCa. These parameters have also been used to monitor the therapeutic response of PCa patients. In this review, we present briefly the current status and the future potential of various 1H in vivo MRS methods in breast and prostate cancer research, and their potential in relation to diagnosis,monitoring of therapeutic response and metabolism.

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References


U. Sharma, R. Sharma and N. R. Jagannathan, Breast Magnetic Resonance Imaging (MRI), Encycloped. Magn. Reson., R. K. Harris and R. E. Wasylishen, Eds. John Wiley: Chichester, U.K., Published 15th March (2010). DOI:10.1002/9780470034590.emrstm0045.pub2.

D. D. Stark and W. G. Bradley, Magnetic Resonance Imaging, Mosby: New York, U.S.A., (1998).

N. R. Jagannathan, MR Imaging and Spectroscopy in Pharmaceutical and Clinical Research, Jaypee Brothers: New Delhi, India (2001).

U. Sharma and N. R. Jagannathan, Breast Magnetic Resonance Spectroscopy (MRS), Encycloped. Magn. Reson., R. K. Harris and R. E. Wasylishen Eds. John Wiley: Chichester, U.K., DOI: 10.1002/9780470034590.emrstm1167; Published 15th December (2009).

U. Sharma and N. R. Jagannathan, Potential of in vivo magnetic resonance spectroscopy (MRS) in medicine, Proc Indian Natl. Sci Acad., 70, 555–577 (2004).

E. R. Danielsen and B. D. Ross, Magnetic Resonance Spectroscopy Diagnosis of Neurological Diseases, Marcel Dekker:

New York, U.S.A., (1999).

D. G. Gadian, A. Connelly, J. S. Duncan, J. H. Cross, F. L. Kirknam, C. L. Johnson, F. Vargha-Khadem, B. G. Nevile

and G. D. Jackson, 1H magnetic resonance spectroscopy in the investigation of intractable epilepsy, Acta Neurol.

Scand., 152, 116–121 (1994).

S. K. Mukherji, Clinical Applications of Magnetic Resonance Spectroscopy, John Willey & Sons: New York, U.S.A.,

(1998).

R. T. Greenlee, M. B. Hill-Harmon, T. Murray and M. Thun, Cancer statistics, CA Cancer J. Clin., 51, 15–36

(2001).

U. Fischer, L. Kopka and E. Grabbe, Breast carcinoma: Effect of preoperative contrast-enhanced MR imaging

on the therapeutic approach, Radiology, 213, 881–888 (1999).

S. C. Rankin, MRI of the breast, Br. J. Radiol., 73, 806–818 (2000).

E. E. Deurloo, J. L. Peterse, E. J. Rutgers, A. P. Besnard, S. H. Muller and K. G. Gilhuijs, Additional breast lesions in patients eligible for breast-conserving therapy by MRI: Impact on pre-operative management and potential benefit of computerized analysis, Eur. J. Cancer, 41, 1393–1401 (2005).

U. Sharma, R. Sharma and N. R. Jagannathan, Characterization of Breast Lesions by Magnetic Resonance Imaging (MRI) and Spectroscopy (MRS), Curr. Med. Imaging Rev., 2, 329–340 (2006).

C. Kuhl, The current status of breast MR imaging, Part I: Choice of technique, image interpretation, diagnostic accuracy and transfer to clinical practice, Radiology, 244, 356–378 (2007).

N. R. Jagannathan, Ed. Breast MR, NMR Biomed., 22, 1–127 (2009).

N. R. Jagannathan, M. Singh, V. Govindaraju, P. Raghunathan, O. Coshic, P.K. Julka and G. K. Rath, Volume localized in vivo proton MR spectroscopy of breast carcinoma: variation of water-fat ratio in patients receiving chemotherapy, NMR Biomed., 11, 414–422 (1998).

N. R. Jagannathan, M. Kumar, P. Raghunathan, O. Coshic, P. K. Julka and G. K. Rath, Assessment of the therapeutic response of human breast carcinoma using in vivo volume localized proton magnetic resonance spectroscopy, Curr. Sci., 76, 777–782 (1999).

J. R. Roebuck, K. M. Cecil, M. D. Schnall and R. E. Lenkinski, Human breast lesions: Characterization with proton MR spectroscopy, Radiology, 209, 269–275 (1998).

K. M. Cecil, M. D. Schnall, E. S. Siegelman and R. E. Lenkinski, The evaluation of human breast lesions with magnetic resonance imaging and proton magnetic resonance spectroscopy, Breast Cancer Res. Treat., 68, 45–54 (2001).

D. K. Yeung, H. S. Cheung and G. M. Tse, Human breast lesions: Characterization with contrast-enhanced in vivo proton MR spectroscopy – initial results, Radiology, 220, 40–46 (2001).

R. Katz-Brull, P. T. Lavin and R. E. Lenkinski, Clinical utility of proton magnetic resonance spectroscopy in characterizing breast lesions, J. Natl. Cancer Inst., 94, 1197–1203 (2002).

J. Kurhanewicz, D. B. Vigneron, H. Hricak, P. Narayan, P. Carroll and S. J. Nelson, Three-dimensional 1H MR spectroscopic imaging of the in situ human prostate with high (0.24–0.7-cm3) spatial resolution, Radiology, 198, 795–805 (1996a).

J. Kurhanewicz, D. B. Vigneron, H. Hricak, F. Parivar, S. J. Nelson, K. Shinohara and P. R. Carroll, Prostate cancer: Metabolic response to cryosurgery as detected with 3D 1H MR spectroscopic imaging, Radiology, 200, 489–496 (1996b).

J. Frahm, K.D. Merbolt, and W. Hanicke, Localized proton spectroscopy using stimulated echoes, J. Magn. Reson. 72, 502–508 (1987).

R. J. Orididge, M. R. Bendall, R. E. Gordon, and A. Connelly, Volume selection for in vivo biological spectroscopy in ‘Magnetic Resonance in Biology and Medicine’, ed. G. Govil, C. L. Khetrapal, A. Saran, A.S. Tata, McGraw Hill, New Delhi, 387, 1985.

T. R. Brown, B. M. Kincaid, and K. Ugurbil, NMR chemical shift imaging in three dimensions, Proc. Natl. Sci. USA 79, 3523–3526 (1982).

A. A. Maudsley, S. K. Hilal, W. H. Perman, and H. E. Simon, Spatially resolved high resolution spectroscopy by ‘four dimensional’ NMR; J. Magn. Reson. 51, 147–152 (1983).

A. Haase, J. Frahm, W. Hanicke, and D. Matthei, 1H NMR chemical shift selective (CHESS) imaging, Phys. Med. Biol., 30, 341–344 (1985).

M. Mescher, A. Tannus, M.O’.N. Johnson, and M. Garwood, Solvent suppression using selective echo dephasing, J. Magn. Reson., 123, 226–229 (1996).

P. E. Sijens, H. K. Wijrdeman, M. A. Moerland, C. J. Bakker, J. W. Vermeulen and P. R. Luyten, Human breast cancer in vivo: 1H and 31P MR spectroscopy at 1.5 T, Radiology, 169, 615–620 (1988).

R. Do, L. Moy, N. Salibi, C. L. Mercado, K. McGorty, M. Kitazono E. Hech, Can MRS improve our ability to distinguish between benign and malignant lesions? Proc. Intl. Soc. Magn. Reson. Med., 14, 2876 (2006).

P. J. Bolan, S. Meisamy, E. H. Baker, J. Lin, T. Emory, M. Nelson, L. I. Everson, D. Yee and M. Garwood, In vivo quantification of choline compounds in the breast with 1H MR spectroscopy, Magn. Reson. Med., 50, 1134–1143 (2003).

P. J. Bolan, P. G. Henry, E. H. Baker, S. Meisamy and M. Garwood, Measurement and correction of respiration-induced B0 variations in breast 1H MRS at 4 Tesla, Magn. Reson. Med., 52, 1239–1245 (2004).

S. Meisamy, P. J. Bolan, E. H. Baker, R. L. Bliss, E. Gulbahce, L. I. Everson, M. T. Nelson, T. H. Emory, T. M. Tuttle, D. Yee and M. Garwood, Neoadjuvant chemotherapy of locally advanced breast cancer: Predicting response with in vivo 1H MR spectroscopy – a pilot study at 4 T, Radiology, 233, 424–431 (2004).

S. Meisamy, P. J. Bolan, E. H. Baker, M. G. Pollema, C. T. Le, F. Kelcz, M. C. Lechner, B. A. Luikens, R. A. Carlson, K. R. Brandt, K. K. Amrami, M. T. Nelson, L. I. Everson, T. H. Emory, T. M. Tuttle, D. Yee and M. Garwood, Adding in vivo quantitative 1H MR spectroscopy to improve diagnostic accuracy of breast MR imaging: Preliminary results of observer performance study at 4.0 T, Radiology, 236, 465–475 (2005).

P. J. Bolan, C. J. Snyder, L. J. DelaBarre, L. Bolinger, M. Garwood and J. T. Vaughan, Preliminary experience with breast 1H MRS at 7 Tesla, Proceedings of the 14th Annual Proc. Intl. Soc. Magn. Reson. Med., 14, 580 (2006). 37. U. Sharma, M. Kumar, R. G. Sah and N. R. Jagannathan, Study of normal breast tissue by in vivo volume localized proton MR spectroscopy: variation of water-fat ratio in relation to the heterogeneity of the breast and the menstrual cycle, Magn. Reson. Imaging, 27, 785–791 (2009).

M. Kumar, N. R. Jagannathan, V. Seenu, S. N. Dwivedi, P. K. Julka and G. K. Rath, Monitoring the therapeutic response of locally advanced breast cancer patients: Sequential in vivo proton MR spectroscopy study, J. Magn. Reson. Imaging, 24, 325–332 (2006).

M. A. Thomas, N. Binesh, K. Yue and N. DeBruhl, Volumelocalized two-dimensional correlated magnetic resonance spectroscopy of human breast cancer, J. Magn. Reson. Imaging, 14, 181–186 (2001).

K. A. Kvistad, I.J. Bakken, I. S. Gribbestad, B. Ehrnholm, S. Lundgren, H. E. Fjøsne, and O. Haraldseth, Characterization of neoplastic and normal human breast tissues with in vivo 1H MR spectroscopy, J. Magn. Reson. Imaging, 10, 159–164 (1999).

N. R. Jagannathan, M. Kumar, V. Seenu, O. Coshic, S. N. Dwivedi, P. K. Julka, A. Srivastava and G. K. Rath, 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 (2001).

K. Glunde, C. Jie, and Z. M. Bhujwalla, Molecular causes of the aberrant choline phospholipid metabolism in breast cancer, Cancer Res., 64, 4270–4276 (2004).

L. Bartella, S. B. Thakur, E. A. Morris, D. D. Dershaw, W. Huang, E. Chough, M. C. Cruz and L. Liberman, Enhancing non-mass lesions in the breast: Evaluation with proton (1H) MR spectroscopy, Radiology, 245, 80–87 (2007).

J. K. Begley, T. W. Redpath, P. J. Bolan and F. J. Gilbert, In vivo proton magnetic resonance spectroscopy of breast cancer: A review of the literature, Breast Cancer Res., 14, 207–216 (2012).

M. A. Jacobs, P. B. Barker, P. A. Bottomley, Z. Bhujwalla and D. A. Bluemke, Proton magnetic resonance spectroscopic imaging of human breast cancer: a preliminary study, J. Magn. Reson. Imaging, 19, 68–75 (2004).

M. A. Jacobs, P. B. Barker, P. Argani, R. Ouwerkerk, Z. M. Bhujwalla and D. A. Bluemke, Combined dynamic contrast enhanced breast MR and proton spectroscopic imaging: A feasibility study, J. Magn. Reson. Imaging, 21, 23–28 (2005).

H. M. Baik, M. Y. Su, H. J. Yu, and Nalcioglu O, Proton chemical shift imaging for monitoring early treatment response of breast cancer to neoadjuvant chemotherapy. Proceedings of the 13th Annual Intl. Soc. Mag. Reson. Med., 13, p1879, (2005).

F. Sardanelli, A. Fausto and F. Podo, MR spectroscopy of the breast, Radiol. Med. (Torino), 113, 56–64 (2008).

F. Sardanelli, A. Fausto, G. Di Leo, R. de Nijs, M. Vorbuchner and F. Podo, In vivo proton MR spectroscopy of the breast using the total choline peak integral as a marker of malignancy, AJR Am. J. Roentgenol., 192, 1608–1617 (2009).

L. Bartella, E. A. Morris, D. D. Dershaw, L. Liberman, S.B. Thakur, C. Moskowitz, J. Guido and W. Huang, Proton MR spectroscopy with choline peak as malignancy marker improves positive predictive value for breast cancer diagnosis: Preliminary study, Radiology, 239, 686–692 (2006).

H. M. Baek, J. H. Chen, H. J. Yu, R. Mehta, O. Nalcioglu, and M. Y. Su, Detection of choline signal in human breast lesions with chemical-shift imaging, J. Magn. Reson. Imaging, 27, 1114–1121 (2008).

H. M. Baik, M. Y. Su, H. Yu, R. Mehta and O. Nalcioglu, Quantification of choline-containing compounds in malignant breast tumors by 1H MR spectroscopy using water as an internal reference at 1.5 T, Magn. Reson. Mater. Phy., 19, 96–104 (2006).

R. G. Sah, U. Sharma, R. Parshad, V. Seenu, S. R. Mathur and N. R. Jagannathan, Association of estrogen receptor, progesterone receptor, and human epidermal growth factor receptor 2 status with total choline concentration and tumor volume in breast cancer patients: An MRI and in vivo proton MRS study, Magn. Reson. Med., 68, 1039–1047 (2012).

P. Stanwell, L. Gluch, D. Clark, B. Tomanek, L. Baker, B. Giuffre, C. Lean, P. Malycha and C.E. Mountford, Specificity of choline metabolites for in vivo diagnosis of breast cancer using 1H MRS at 1.5 T, Eur. Radiol., 15, 1037–1043 (2005).

R. G. Sah, K. Agarwal, U. Sharma, R. Parshad, V. Seenu, and N. R. Jagannathan, Characterization of malignant breast tissue of breast cancer patients and the normal breast tissue of healthy lactating women volunteers using diffusion MRI and in vivo 1H MR spectroscopy, J. Magn. Reson. Imaging, (2013) Nov 22, doi: 10.1002/jmri.24507. [Epub ahead of print].

G. M. Tse, H. S. Cheung, L. M. Pang, W. C. Chu, B. K. Law, F. Y. Kung and D. K. Yeung, Characterization of lesions of the breast with proton MR spectroscopy: Comparison of carcinomas, benign lesions, and phyllodes tumors, AJR Am. J. Roentgenol., 181, 1267–1273 (2003).

U. Sharma, H. M. Baek, M. Y. Su and N. R. Jagannathan, In vivo 1H MRS in the assessment of the therapeutic response of breast cancer patients, NMR Biomed., 24, 700–711 (2011).

R. G. Sah, U. Sharma, R. Parshad and N. R. Jagannathan, Choline as a biomarker a better predictor of early response of breast cancer than tumor volume? Sequential study of the therapeutic response of locally advanced breast cancer patients undergoing neo-adjuvant chemotherapy (NACT), Proceedings of the 18th Annual Intl. Soc. Mag. Reson. Med., p 3137 (2010).

K. A. Danishad, U. Sharma, R. G. Sah, V. Seenu, R. Parshad and N. R. Jagannathan, Assessment of therapeutic response of locally advanced breast cancer (LABC) patients undergoing neoadjuvant chemotherapy (NACT) monitored using sequential magnetic resonance spectroscopic imaging (MRSI), NMR Biomed., 23, 233–241 (2010).

N. R. Jagannathan, V. Kumar, R. Kumar and S. Thulkar, Role of magnetic resonance methods in the evaluation of prostate cancer: an Indian perspective. MAGMA, 21, 393–407 (2008); Erratum 21, 409 (2008).

J. L. Gulley, M. Emberton, J. Kurhanewicz and P. Choyke, Progress in prostate cancer imaging, Urol. Oncol. 30, 938–39 (2012).

A. Sciarra, J. Barentsz, A. Bjartell, J. Eastham, H. Hricak, V. Panebianco and J. A. Witjes, Advances in magnetic resonance imaging: How they are changing the management of prostate cancer? Eur. Urol., 59, 962–77 (2011).

V. Kumar, N. R. Jagannathan, S. Thulkar and R. Kumar, Pre-biopsy magnetic resonance spectroscopy and imaging in the diagnosis of prostate cancer, Int. J. Urol., 19, 602–13 (2012).

N. R. Jagannathan, Prostate MR: Current status, challenges and future directions, NMR Biomed., 27, 1–2 (2014) and other articles in this special issue.

L. O. Sillerud, K. R. Halliday, R. H. Griffey, C. Fenoglio- Preiser and S. Sheppard, In vivo 13C NMR spectroscopy of the human prostate, Magn. Reson. Med., 8, 224–230 (1988).

P. Narayan, D. B. Vigneron, P. Jajodia, C. M. Anderson, M. W. Hedgcock, E. A. Tanagho and T. L. James, Transrectal probe for 1H MRI and 31P MR spectroscopy of the prostate gland, Magn. Reson. Med., 11, 209–220 (1989).

M. A. Thomas, P. Narayan, J. Kurhanewicz, P. Jajodia and M. W. Weiner, 1H MR spectroscopy of normal malignant human prostates in vivo, J. Magn. Reson., 87, 610–619 (1990).

J. Kurhanewicz, A. Thomas, P. Jajodia, M. W. Weiner, T. L. James, D. B. Vigneron and P. Narayan, 31P spectroscopy of the human prostate gland in vivo using a transrectal probe, Magn. Reson. Med., 22, 404–413 (1991).

J. Kurhanewicz, R. Dahiya, J. M. Macdonald, L. H. Chang, T. L. James and P. Narayan, Citrate alterations in primary and metastatic human prostatic adenocarcinomas: 1H magnetic resonance spectroscopy and biochemical study, Magn. Reson. Med., 29, 149–157 (1993).

A. Shukla-Dave, H. Hricak, C. Moskowitz, N. Ishill, O. Akin, K. Kuroiwa, J. Spector, M. Kumar, V. E. Reuter, J. A. Koutcher and K. L. Zakian, Detection of prostate cancer with MR spectroscopic imaging: An expanded paradigm incorporating polyamines, Radiology, 245, 499–506 (2007).

D. W. Klomp, T. W. Scheenen, C. S. Arteaga, J. van Asten, V. O. Boer and P. R. Luijten, Detection of fully refocused polyamine spins in prostate cancer at 7 T, NMR Biomed., 24, 299–306 (2011).

L. L. Cheng, C. Wu, M. R. Smith and R. G. Gonzalez, Nondestructive quantitation of spermine in human prostate tissue samples using HRMAS 1H NMR spectroscopy at 9.4 T, FEBS Lett., 494, 112–116 (2001).

J. A. Jung, F. V. Coakley, D. B. Vigneron, M. G. Swanson, A. Qayyum, V. Weinberg, K. D. Jones, P. R. Carroll and J. Kurhanewicz, Prostate depiction at endorectal MR spectroscopic imaging: Investigation of a standardized evaluation system, Radiology, 233, 701–708 (2004).

J. Scheidler, H. Hricak, D. B. Vigneron, K. K. Yu, D. L. Sokolov, L. R. Huang, C. J. Zaloudek, S. J. Nelson, P. R. Carroll and J. Kurhanewicz, Prostate cancer: Localization with three-dimensional proton MR spectroscopic imaging—Clinicopathologic study, Radiology, 213, 473–480 (1999).

A. E.Wefer, H. Hricak, D. B. Vigneron, F. V. Coakley, Y. Lu, J. Wefer, U. Mueller-Lisse, P. R. Carroll and J. Kurhanewicz, Sextant localization of prostate cancer: Comparison of sextant biopsy, magnetic resonance imaging and magnetic resonance spectroscopic imaging with step section histology, J. Urol., 164, 400–404 (2000).

M. Hasumi, K. Suzuki, A. Taketomi, H. Matsui, T. Yamamoto, K. Ito, K. Kurokawa, J. Aoki, K. Endo and H. Yamanaka, 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).

K. Saito, T. Kaminaga, S. Muto, H. Ide, K. Nishio, Y. Kamiyama, H. Okada, Y. Terado, S. Furui and S. Horie, Clinical efficacy of proton magnetic resonance spectroscopy (1H-MRS) in the diagnosis of localized prostate cancer, Anticancer Res., 28, 1899–1904 (2008).

G. M. Villeirs, W. Oosterlinck, E. Vanherreweghe and G. O. De Meerleer, A qualitative approach to combined magnetic resonance imaging and spectroscopy in the diagnosis of prostate cancer, Eur. J. Radiol., 73, 352–356 (2010).

S. Klijn, P. J. De Visschere, G. O. De Meerleer and G. M. Villeirs, Comparison of qualitative and quantitative approach to prostate MR spectroscopy in peripheral zone cancer detection. Eur. J. Radiol. doi:10.1016/j.ejrad.2010.12.017 (2011).

C. Testa, R. Schiavina, R. Lodi, E. Salizzoni, B. Corti, M. Farsad, J. Kurhanewicz, F. Manferrari, E. Brunocilla, C. Tonon, N. Monetti, P. Castellucci, S. Fanti, M. Coe, W. F. Grigioni, G. Martorana, R. Canini and B. Barbiroli, Prostate cancer: Sextant localization with MR imaging, MR spectroscopy, and 11C-choline PET/CT, Radiology, 244, 797–806 (2007).

R. Dhingsa, A. Qayyum, F. V. Coakley, Y. Lu, K. D. Jones, M. G. Swanson, P. R. Carroll, H. Hricak and J. Kurhanewicz, Prostate cancer localization with endorectal MR imaging and MR spectroscopic imaging: Effect of clinical data on reader accuracy, Radiology, 230, 215–220 (2004).

K. L. Zakian, K. Sircar, H. Hricak, H. N. Chen, A. Shukla- Dave, S. Eberhardt, M. Muruganandham, L. Ebora, M. W. Kattan, V. E. Reuter, P. T. Scardino and J. A. Koutcher, Correlation of proton MR spectroscopic imaging with Gleason score based on step-section pathologic analysis after radical prostatectomy, Radiology, 234, 804–814 (2005).

C. Testa, R. Schiavina, R. Lodi, E. Salizzoni, C. Tonon, A. D’Errico, B. Corti, A. M. Morselli-Labate, A. Franceschelli, A. Bertaccini, F. Manferrarik, W. F. Grigioni, R. Canini, G. Martorana and B. Barbiroli, 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).

J. S. Yuen, C. H. Thng, P. H. Tan, L.W. Khin, S. J. Phee, D. Xiao, W. K. Lau, W. S. Ng and C.W. Cheng, Endorectal magnetic resonance imaging and spectroscopy for the detection of tumor foci in men with prior negative transrectal ultrasound prostate biopsy, J. Urol., 171, 1482–1486 (2004).

C. Bhatia, S. Phongkitkarun, D. Booranapitaksonti, W. Kochakarn and P. Chaleumsanyakorn, Diagnostic accuracy of MRI/MRSI for patients with persistently high PSA levels and negative TRUS-guided biopsy results, J. Med. Assoc. Thai., 90, 1391–1399 (2007).

C. K. Naughton, D. S. Smith, P. A. Humphrey, W. J. Catalona and D. W. Keetch, Clinical and pathologic tumor characteristics of prostate cancer as a function of the number of biopsy cores: A retrospective study, Urology, 52, 808–813 (1998).

V. Kumar, N. R. Jagannathan, R. Kumar, S. Thulkar, S. D. Gupta, A. K. Hemal and N. P. Gupta, Transrectal ultrasound-guided biopsy of prostate voxels identified as suspicious of malignancy on three-dimensional spectroscopic imaging in patients with abnormal digital rectal examination or raised prostate specific antigen level of 4–10 ng mL−1, NMR Biomed., 20, 11–20 (2007).

M. Chen, H. D. Dang, J. Y. Wang, C. Zhou, S. Y. Li, W. C. Wang, W. F. Zhao, Z. H. Yang, C. Y. Zhong and G. Z. Li, 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).

H. U. Ahmed, A. Kirkham, M. Arya, R. Illing, A. Freeman, C. Allen and M. Emberton, Is it time to consider a role for MRI before prostate biopsy?, Nature Rev. Clin. Oncol., 6, 197–206 (2009).

J. C. Vilanova, J. Comet, C. Barcelo-Vidal, J. Barceló, E. López-Bonet, A. Maroto, M. Arzoz, A. Moreno and J. Areal, 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).

G. M. Villeirs, G. O. De Meerleer, P. J. De Visschere, V. H. Fonteyne, A. C. Verbaeys and W. Oosterlinck, 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).

I. M. Thompson, D. K. Pauler, P. J. Goodman, C.M. Tangen, M. S. Lucia, H. L. Parnes, L. M. Minasian, L. G. Ford, S. M. Lippman, E. D. Crawford, J. J. Crowley and C. A. Jr Coltman, Prevalence of prostate cancer among men with a prostate-specific antigen level ≤4.0 ng per milliliter, N. Engl. J. Med., 350, 2239–2246 (2004).

A. Prando, J. Kurhanewicz, A. P. Borges, E. M. Jr Oliveira, and E. Figueiredo, 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).

A. Wetter, F. Hubner, T. Lehnert, K. Fliessbach, M. Vorbuchner, S. Roell, S. Zangos, W. Luboldt and T. J. Vogl, Three-dimensional 1H magnetic resonance spectroscopy of the prostate in clinical practice: Technique and results in patients with elevated prostate-specific antigen

and negative or no previous prostate biopsies, Eur. Radiol.,15, 645–652 (2005).

A. G. Anastasiadis, M. P. Lichy, U. Nagele, M. A. Kuczyk, A. S. Merseburger, J. Hennenlotter, S. Corvin, K. D. Sievert, C. D. Claussen, A. Stenzl and H. P. Schlemmer, MRI-guided biopsy of the prostate increases diagnostic performance in men with elevated or increasing PSA levels after previous negative trus biopsies, Eur. Urol., 50,738–48 & 748–749 (2006).

N. Lawrentschuk and N. Fleshner, The role of magnetic resonance imaging in targeting prostate cancer in patients with previous negative biopsies and elevated prostatespecific antigen levels, BJU Int., 103, 730–733 (2009).

M. Schmuecking, C. Boltze, H. Geyer, H. Salz, B. Schilling, T.G. Wendt, K.H. Kloetzer and C. Marx, 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).

A. Sciarra, V. Panebianco, M. Ciccariello, S. Salciccia, S. Cattarino, D. Lisi, A. Gentilucci, A. Alfarone, S. Bernardo, R. Passariello and V. Gentile, 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).

V. Kumar, N. R. Jagannathan, R. Kumar, R. Nayyar, S. Thulkar, S. D. Gupta, A. K. Hemal and N. P. Gupta, Potential of 1H 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).

R. Kumar, R. Nayyar, V. Kumar, N. P. Gupta, A. K. Hemal, N. R. Jagannathan, S. Dattagupta and S. Thulkar, Potential of magnetic resonance spectroscopic imaging in predicting absence of prostate cancer in men with serum prostate-specific antigen between 4 and 10 ng mL−1: A follow-up study, Urology, 72, 859–863 (2008).

M. Zaider, M. J. Zelefsky, E. K. Lee, K. L. Zakian, H. I. Amols, J. Dyke, G. Cohen, Y. Hu, A. K. Endi, C. Chui and J. A. Koutcher, Treatment planning for prostate implants using magnetic resonance spectroscopy imaging, Int. J. Radiat. Oncol. Biol. Phys. 47, 1085–1096 (2000).

S. J. DiBiase, K. Hosseinzadeh, R. P. Gullapalli, S. C. Jacobs, M. J. Naslund, G. N. Sklar, R. B. Alexander and C. Yu, Magnetic resonance spectroscopic imaging-guided brachy therapy for localized prostate cancer, Int. J. Radiat. Oncol. Biol. Phys., 52, 429–438 (2002).

A. Kazi, G. Godwin, J. Simpson and G. Sasso, MRS-guided HDR brachytherapy boost to the dominant intraprostatic lesion in high risk localised prostate cancer, BMC Cancer, 10, 472 (2010).

F. Parivar, H. Hricak, K. Shinohara, J. Kurhanewicz, D. B. Vigneron, S. J. Nelson and P. R. Carroll, Detection of locally recurrent prostate cancer after cryosurgery: Evaluation by transrectal ultrasound, magnetic resonance imaging, and three-dimensional proton magnetic resonance spectroscopy, Urology, 48, 594–599 (1996).

D. Pucar, A. Shukla-Dave, H. Hricak, C. S. Moskowitz, K. Kuroiwa, S. Olgac, L. E. Ebora, P. T. Scardino, J. A. Koutcher and K. L. Zakian, Prostate cancer: Correlation of MR imaging and MR spectroscopy with pathologic findings after radiation therapy-initial experience, Radiology, 236, 545–553 (2005).

C. Menard, I. C. Smith, R. L. Somorjai, L. Leboldus, R. Patel, C. Littman, S. J. Robertson, and T. Bezabeh, 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).

F. V. Coakley, H. S. Teh, A. Qayyum, M. G. Swanson, Y. Lu, M3rd. Roach, B. Pickett, K. Shinohara, D. B. Vigneron and J. Kurhanewicz, Endorectal MR imaging and MR spectroscopic imaging for locally recurrent prostate cancer after external beam radiation therapy: Preliminary experience, Radiology, 233, 441–448 (2004).

B. Pickett, J. Kurhanewicz, F. Coakley, K. Shinohara, B. Fein and M.3rd Roach, Use of MRI and spectroscopy in evaluation of external beam radiotherapy for prostate cancer, Int. J. Radiat. Oncol. Biol. Phys., 60, 1047–1055 (2004).

A. Sciarra, V. Panebianco, S. Salciccia, M. Osimani, D. Lisi, M. Ciccariello, R. Passariello, F. Di Silverio and V. Gentile, 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).

S. Cirillo, M. Petracchini, L. D’Urso, P. Dellamonica, R. Illing, D. Regge and G. Muto. Endorectal magnetic resonance imaging and magnetic resonance spectroscopy to monitor the prostate for residual disease or local cancer recurrence after transrectal high-intensity focused ultrasound, BJU Int., 102, 452–458 (2008).

V. Panebianco, A. Sciarra, D. Lisi, F. Galati, V. Buonocore, C. Catalano, V. Gentile, A. Laghi and R. Passariello, Prostate cancer: 1H MRS-DCEMR at 3T versus [18F] choline PET/CT in the detection of local prostate cancer recurrence in men with biochemical progression after radical retropubic prostatectomy (RRP), Eur. J. Radiol., 81, 700– 708 (2012).

A. Sciarra, V. Panebianco, S. Salciccia, D. Lisi, A. Alfarone, A. Gentilucci, U. Parente, S. Cattarino, R. Passariello and V. Gentile, Determination of the time for maximal response to neoadjuvant hormone therapy for prostate cancer using magnetic resonance with spectroscopy (MRSI) and dynamic contrast enhancement (DCEMR), Urol. Oncol., 30, 614–619 (2012).


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