315
Views
18
CrossRef citations to date
0
Altmetric
Review

NMR-based metabolomics of prostate cancer: a protagonist in clinical diagnostics

, &
Pages 651-661 | Received 02 Dec 2015, Accepted 07 Mar 2016, Published online: 25 Mar 2016

References

  • Siegel R, Millar K, Jemal A. Cancer statistics, 2016. CA Cancer J Clin. 2016;66:7–30 .
  • Cannon L. Genetic epidemiology of prostate cancer in Utah Morman genealogy. J Cancer Surviv. 1982;1:47–70.
  • Albright F, Teerlink C, Werner TL, et al. Significant evidence for a heritable contribution to cancer predisposition: a review of cancer familiality by site. BMC Cancer. 2012;12:138.
  • Stewart SB, Freedland SJ. Influence of obesity on the incidence and treatment of genitourinary malignancies. Urol Oncol. 2011;29:476–486.
  • Sonn GA, Aronson W, Litwin MS. Impact of diet on prostate cancer: a review. Prostate Cancer Prostatic Dis. 2005;8:304–310.
  • Levy-Lahad E, Friedman E. Cancer risks among BRCA1 and BRCA2 mutation carriers. Br J Cancer. 2007;96:11–15.
  • Agalliu I, Leanza SM, Smith L, et al. Contribution of HPC1 (RNASEL) and HPCX variants to prostate cancer in a founder population. Prostate. 2010;70:1716–1727.
  • Morgentaler A, Rhoden EL. Prevalence of prostate cancer among hypogonadal men with prostate specific antigen levels of 4.0 ng/mL or less. Urology. 2006;68:1263–1267.
  • Ikuerowo SO, Omisanjo OA, Bioku MJ, et al. Prevalence and characteristics of prostate cancer among participants of a community-based screening in Nigeria using serum prostate specific antigen and digital rectal examination. Pan Afr Med J. 2013;15:129–136.
  • Gleason D. Histologic grading and clinical staging of prostatic carcinoma. In: Tannenbaum M, editor. Urologic pathology: the prostate. Philadelphia, PA: Lea and Febiger; 1977. p. 171–198.
  • Langer DL, Van Der Kwast TH, Evans AJ, 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. 2009;30:327–334.
  • Panebianco V, Barchetti F, Sciarra A, et al. Multi-parametric magnetic resonance imaging vs. standard care in men being evaluated for prostate cancer: a randomized study. Urol Oncol. 2015;33(1):17.e1–e7.
  • Siddiqui MM, Rais-Bahrami S, Truong H, et al. Magnetic resonance imaging/ultrasound–fusion biopsy significantly upgrades prostate cancer versus systematic 12-core transrectal ultrasound biopsy. Eur Urol. 2013;64:713–719.
  • Smeenge M, Barentsz J, Cosgrove D, et al. Role of transrectal ultrasonography (TRUS) in focal therapy of prostate cancer: report from a consensus panel. BJU Int. 2009;110:942–948.
  • Thompson IM, Ankerst DP, Chi C, et al. Assessing prostate cancer risk: results from the prostate cancer prevention trial. J Natl Cancer Inst. 2006;98:529–534.
  • Pal RP, Maitra NU, Mellon JK, et al. Defining prostate cancer risk before prostate biopsy. Urol Oncol. 2013;31:1408–1418.
  • Ukimura O, Coleman JA, de la Taille A, et al. Contemporary role of systematic prostate biopsies: indications, techniques, and implications for patient care. Eur Urol. 2013;63:214–230.
  • Schröder FH, Carter HB, Wolters T, et al. Early detection of prostate cancer in 2007. Part 1: PSA and PSA kinetics. Eur Urol. 2008;53:468–477.
  • Catalona WL, Richie JP, Ahmann FR, et al. Comparison of digital rectal examination and serum prostate specific antigen in the early detection of prostate cancer: results of a multicenter clinical trial of 6,630 men. J Urol. 1994;151:1283–1290.
  • Velonas VM, Woo HH, Remedios CG, et al. Current status of biomarkers for prostate cancer. Int J Mol Sci. 2013;14:11034–11060.
  • Engelbrecht MR, Jager GJ, Laheij RJ, et al. Local staging of prostate cancer using magnetic resonance imaging: a meta-analysis. Eur Radiol. 2002;12:2294–2302.
  • Kozlowski P, Chang SD, Jones EC, et al. Combined diffusion-weighted and dynamic contrast-enhanced MRI for prostate cancer diagnosis—correlation with biopsy and histopathology. J Magn Reson Imaging. 2006;24:108–113.
  • Turnbull LW, Buckley DL, Turnbull LS, et al. Differentiation of prostatic carcinoma and benign prostatic hyperplasia: correlation between dynamic Gd-DTPA-enhanced MR imaging and histopathology. J Magn Reson Imaging. 1999;9:311–316.
  • Barentsz JO, Engelbrecht M, Jager GJ, et al. Fast dynamic gadolinium-enhanced MR imaging of urinary bladder and prostate cancer. J Magn Reson Imaging. 1999;10:295–304.
  • Padhani AR, Gapinski CJ, Macvicar DA, et al. Dynamic contrast enhanced MRI of prostate cancer: correlation with morphology and tumor stage, histological grade and PSA. Clin Radiol. 2000;55:99–109.
  • Muramoto S, Uematsu H, Kimura H, et al. Differentiation of prostate cancer from benign prostate hypertrophy using dual-echo dynamic contrast MR imaging. Eur J Radiol. 2002;44:52–58.
  • Noworolski SM, Henry RG, Vigneron DB, et al. Dynamic contrast-enhanced MRI in normal and abnormal prostate tissues as defined by biopsy, MRI, and 3D MRSI. Magn Reson Med. 2005;53:249–255.
  • De Feo EM, Wu CL, McDougal WS, et al. A decade in prostate cancer: from NMR to metabolomics. Nat Rev Urol. 2011;8:301–311.
  • Eggleston JC, Saryan LA, Hollis DP. Nuclear magnetic resonance investigations of human neoplastic and abnormal nonneoplastic tissues. Cancer Res. 1975;35:1326–1332.
  • Andrew E, Bradbury A, Eades R. Nuclear magnetic resonance spectra from a crystal rotated at high speed. Nature. 1958;182:1695.
  • 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;36:653–658.
  • 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;94:6408–6413.
  • Swanson MG, Zektzer AS, Tabatabai ZL, et al. Quantitative analysis of prostate metabolites analysis of prostate using 1H HR-MAS spectroscopy. Magn Reson Med. 2006;55:1257–1264.
  • Cheng LL, Wu C, Smith MR, et al. Non-destructive quantitation of spermine in human prostate tissue samples using HR-MAS 1H NMR spectroscopy at 9.4 T. FEBS Lett. 2001;494:112–116.
  • Cheng LL, Pohl U. The handbook of metabonomics and metabolomics (Lindon JC, Nicholls JK, Holmes E, editors). Amsterdam: Elsevier; 2007. p. 345–374.
  • Schiebler ML, White M, Maygarden SJ, et al. In vitro high resolution 1H-spectroscopy of the human prostate: benign prostatic hyperplasia, normal peripheral zone and adenocarcinoma. Magn Reson Med. 1993;29:285–291.
  • Nelson SJ, Kurhanewicz J, Vigneron DB, et al. Metabolic imaging of patients with prostate cancer using hyperpolarized [1-C13] pyruvate. Sci Transl Med. 2013;5(198ra):108.
  • Albers MJ, Bok R, Chen AP, et al. Hyperpolarized 13C lactate, pyruvate, and alanine: non-invasive biomarkers for prostate cancer detection and grading. Cancer Res. 2008;68:8607–8861.
  • Thomas MA, Nagarajan RK, Huda A, et al. Multidimensional MR spectroscopic imaging of prostate cancer in vivo. NMR Biomed. 2014;27:53–66.
  • Schick F, Bogers H, Kurz S, et al. Localized proton MR spectroscopy of citrate in vitro and of the human prostate in vivo at 1.5 T. Magn Reson Med. 1993;29:38–43.
  • Lynch MJ, Nicholson JK. Proton MRS of human prostatic fluid: correlations between citrate, spermine, and myo-inositol levels and changes with disease. Prostate. 1997;30:248–255.
  • Thomas MA, Narayan P, Kurhanewicz J, et al. 1HMR spectroscopy of normal and malignant human prostates in vivo. J Magn Reson. 1990;87:610–619.
  • Kurhanewicz J, Vigneron DB, Nelson SJ, 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. 1995;3:459–466.
  • Gupta A, Bansal N, Houstaon B. Metabolomics of urinary tract infection: a new uroscope in town. Expert Rev Mol Diagn. 2012;12:361–369.
  • Krojanski HG, Lambert J, Garikalan Y, et al. Microslot NMR probe for metabolomics studies. Anal Chem. 2008;80:8668–8672.
  • Wensink H, Lopez FB, Hermes DC, et al. Measuring reaction kinetics in a lab-on-chip by micro-coil. NMR Lab Chip. 2005;5:280–284.
  • Bart J, Kolkman AJ, Oosthoek-de Vries AJ, et al. A microfluidic high-resolution NMR flow probe. J Am Chem Soc. 2009;131:5014–5015.
  • Ardenkjaer-Larson JH, Friedlund B, Gram A, et al. Increase in signal to noise ratio of >10,000 times in liquid state NMR. Proc Natl Acad Sci USA. 2003;100:10158–10163.
  • Rider OJ, Tyler DJ. Clinical implications of cardiac hyperpolarized magnetic resonance imaging. J Cardiovasc Magn Reson. 2013;15:93.
  • Robey IF, Baggett BK, Kirkpatrick ND, et al. Bicarbonate increases tumor pH and inhibits spontaneous metastases. Cancer Res. 2009;69:2260–2268.
  • Nath K, Nelson DS, Ho AM, et al. 31P and 1H MRS of DB-1 melanoma xenografts: lonidamine selectively decreases tumor intracellular pH and energy status and sensitizes tumors to melphalan. NMR Biomed. 2013;26:98–105.
  • Nath K, Nelson DS, Heitian DF, et al. Lonidamine induces intracellular tumor acidification and ATP depletion in breast, prostate and ovarian cancer xenografts and potentiates response to doxorubicin. NMR Biomed. 2015;28:281–290.
  • Kim JH, Kim SH, Altieri A, et al. Lonidamine: a hyperthermic sensitizer of HeLa cells in culture and of the Meth-A tumor in vivo. Oncology. 1984;41:30–35.
  • Kim JH, Alfieri AA, Kim SH, et al. Potentiation of radiation effects on 2 murine tumors by lonidamine. Cancer Res. 1986;46:1120–1123.
  • Costello LC, Franklin RB. Prostatic fluid electrolyte composition for the screening of prostate cancer: a potential solution to a major problem. Prostate Cancer Prostatic Dis. 2009;12:17–24.
  • Lynch MJ, Masters J, Pryor JP, et al. Ultra high field NMR spectroscopic studies on human seminal fluid, seminal vesicles and prostatic secretions. J Pharm Biomed Anal. 1994;12:5–19.
  • Teahan O, Bevan CL, Waxman J, et al. Metabolic signatures of malignant progression in prostate epithelium cells. Int J Biochem Cell Biol. 2011;43:1002–1009.
  • Liney GP, Turnbull LW, Martin L, et al. In vivo quantification of citrate concentration and water T2 relaxation time of the pathogenic prostate gland using 1H MRS and MRI. Magn Reson Imaging. 1997;15:1177–1186.
  • Costello LC, Feng P, Milon B, et al. Role of zinc in the pathogenesis and treatment of prostate cancer: critical issues to resolve. Prostate Cancer Prostatic Dis. 2004;7:111–117.
  • Costello LC, Franklin RB, Feng P. Mitochondrial function, zinc, and intermediary metabolism relationships in normal prostate and prostate cancer. Mitochondrion. 2005;5:143–153.
  • Franklin RB, Costello LC. Zinc as an anti-tumor agent in prostate cancer and in other cancers. Arch Biochem Biophys. 2007;463:211–217.
  • Franz MC, Anderle P, Burzle M, et al. Zinc transporters in prostate cancer. Mol Aspects Med. 2013;34:735–741.
  • Dakubo GD, Parr RL, Costello LC, et al. Altered metabolism and mitochondrial genome in prostate cancer. J Clin Pathol. 2006;59:10–16.
  • Robert MJ, Schirra HJ, Lavin MF, et al. Metabolomics; a novel approach to early and noninvasive prostate cancer detection. Korean J Urol. 2011;52:79–89.
  • Yacoe ME, Sommer G, Peehl D. In vitro proton spectroscopy of normal and abnormal prostate. Magn Reson Med. 1991;19:429–438.
  • Hahn P, Smith IC, Leboldus L, et al. The classification of benign and malignant human prostate tissue by multivariate analysis of 1H magnetic resonance spectra. Cancer Res. 1997;57:3398–3401.
  • Halliday KR, Fenoglio-Preiser C, Sillerud LO. Differentiation of human tumors from nonmalignant tissue by natural-abundance 13C NMR spectroscopy. Magn Reson Med. 1988;7:384–411.
  • Sillerud LO, Halliday KR, Griffey RH, et al. In vivo 13C NMR spectroscopy of the human prostate. Magn Reson Med. 1988;8:224–230.
  • Fowler AH, Pappas AA, Holder JC, et al. Differentiation of human prostate cancer from benign hypertrophy by in vitro 1H NMR. Magn Reson Med. 1992;25:140–147.
  • Schiebler ML, Miyamoto KK, White M, et al. In vitro high resolution 1H-spectroscopy of the human prostate: benign prostatic hyperplasia, normal peripheral zone and adenocarcinoma. Magn Reson Med. 1993;29:285–291.
  • Cornel EB, Smits GA, Oosterhof GO, et al. Characterization of human prostate cancer, benign prostatic hyperplasia and normal prostate by in vitro 1H and 31P magnetic resonance spectroscopy. J Urol. 1993;150:2019–2024.
  • Vander GM, Schipper RG, Oosterhof GON, et al. Proton MR spectroscopy of prostatic tissue focused on the detection of spermine, a possible biomarker of malignant behavior in prostate cancer. Magn Reson Mater Phys. 2000;10:153–159.
  • Swindle P, McCredie S, Russell P, et al. Pathologic characterization of human prostate tissue with proton MR spectroscopy. Radiology. 2003;228:144–151.
  • Swindle P, Ramadan S, Stanwel P, et al. Proton magnetic resonance spectroscopy of the central, transition and peripheral zones of the prostate: assignments and correlation with histopathology. Magn Reson Mater Phys. 2008;21:423–434.
  • Komoroski RA, Holder JC, Pappas AA, et al. 31P NMR of phospholipid metabolites in prostate cancer and benign prostatic hyperplasia. Magn Reson Med. 2011;65:911–913.
  • Tessem MB, Swanson MG, Keshari KR, et al. Evaluation of lactate and alanine as metabolic biomarkers of prostate cancer using 1H HR-MAS spectroscopy of biopsy tissues. Magn Reson Med. 2008;60:510–516.
  • Averna TA, Kline EE, Smith AY, et al. A decrease in 1H nuclear magnetic resonance spectroscopically determined citrate in human seminal fluid accompanies the development of prostate adenocarcinoma. J Urol. 2005;173:433–438.
  • Kline EE, Treat EG, Averna TA, 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. 2006;176:2274–2279.
  • Serkova NJ, Gamito EJ, Jones RH, et al. The metabolites citrate, myo-Inositol, and spermine are potential age-independent markers of prostate cancer in human expressed prostatic secretions. Prostate. 2008;68:620–628.
  • Kumar D, Gupta A, Mandhani A, et al. Metabolomics-derived prostate cancer biomarkers: fact or fiction? J. Proteome Res. 2015;14:1455–1464.
  • Kotzerke J, Gschwend JE, Neumaier B. PET for prostate cancer imaging: still a quandary or the ultimate solution? J Nucl Med. 2002;43:200–202.
  • Zaheer A, Cho SY, Pomper MG. New agents and techniques for imaging prostate cancer. J Nucl Med. 2009;50:1387–1390.
  • Farsad M, Schiavina R, Franceschelli A, et al. Positron-emission tomography in imaging and staging prostate cancer. Cancer Biomark. 2008;4:277–284.
  • Apolo AB, Pandit-Taskar N, Morris MJ. Novel tracers and their development for the imaging of metastatic prostate cancer. J Nucl Med. 2008;49:2031–2041.
  • Fox JJ, Schoder H, Larson SM. Molecular imaging of prostate cancer. Curr Opin Urol. 2012;22:320–327.
  • Jadvar H. Molecular imaging of prostate cancer: PET radiotracers. AJR Am J Roentgenol. 2012;199:278–291.
  • Lutje S, Boerman OC, Van Rij CM, et al. Prospects in radionuclide imaging of prostate cancer. Prostate. 2012;72:1262–1272.
  • Oyama N, Miller TR, Dehdashti F, et al. 11C-acetate PET imaging of prostate cancer: detection of recurrent disease at PSA relapse. J Nucl Med. 2003;44:549–555.
  • Schiepers C, Hoh CK, Nuyts J, et al. 11C-acetate kinetics of prostate cancer. J Nucl Med. 2008;49:206–215.
  • Picchio M, Treiber U, Beer AJ, et al. Value of11C-choline PET and contrast-enhanced CT for staging of bladder cancer: correlation with histopathologic findings. J Nucl Med. 2006;47:938–944.
  • Reske SN, Blumstein NM, Neumaier B, et al. Imaging prostate cancer with11C-choline PET/CT. J Nucl Med. 2006;47:1249–1254.
  • Hara T, Kosaka N, Kishi H. Development of 18F-fluoroethylcholine for cancer imaging with PET: synthesis, biochemistry, and prostate cancer imaging. J Nucl Med. 2002;43:187–199.
  • Degrado TR, Coleman RE, Wang S, et al. Synthesis and evaluation of 18F-labeled choline as an oncologic tracer for positron emission tomography: initial findings in prostate cancer. Cancer Res. 2000;61:110–117.
  • Jadvar H. Prostate cancer: PET with 18F-FDG, 18F- or 11C-acetate, and 18F- or 11C-choline. J Nucl Med. 2011;52:81–89.
  • Dimitrakopoulou-Strauss A, Strauss LG. PET imaging of prostate cancer with 11C-acetate. J Nucl Med. 2003;44:556–558.
  • Schuster DM, Savir-Baruch D, Nieh P, et al. Detection of recurrent prostate carcinoma with anti-3-18F-fluorocyclobutane-1-carboxylic acid PET/CT and 111In-capromab pendetide SPECT/CT. Radiology. 2011;259:852–861.
  • Schiavina R, Brunocilla E, Martorana G. The new promise of FACBC position emission tomography/computed tomography in the localization of disease relapse after radical treatment for prostate cancer: are we turning to the right radiotracer? Eur Urol. 2014;65:255–256.
  • Nanni C, Schiavina R, Boschi S, et al. Comparison of 18F-FACBC and 11C-choline PET/CT in patients with radically treated prostate cancer and biochemical relapse: preliminary results. Eur J Nucl Med Mol Imaging. 2013;40(Suppl. 1):11–17.
  • Even-Sapir E, Metser U, Mishani E, et al. The detection of bone metastases in patients with high-risk prostate cancer: 99mTc-MDP planar bone scintigraphy, single- and multi-field-of-view SPECT, 18F-fluoride PET, and 18F-fluoride PET/CT. J Nucl Med. 2006;47:287–297.
  • Jadvar H. PSMA PET in prostate cancer. J Nucl Med. 2015;56:1131–1132.
  • Baum RP, Kulkarni H, Weineisen M, et al. Advancing personalized nuclear medicine by theranostics of prostate cancer using Ga-68 and Lu-177 labeled PSMA small molecules. J Nucl Med. 2015;56(Suppl. 1):22.
  • Holland JP, Divilov V, Bander NH, et al. 89Zr-DFO-J591 for immunoPET of prostate-specific membrane antigen expression in vivo. J Nucl Med. 2010;51:1293–1300.
  • Afshar-Oromieh A, Malcher A, Eder M, et al. PET imaging with a [68Ga]gallium-labelled PSMA ligand for the diagnosis of prostate cancer: biodistribution in humans and first evaluation of tumour lesions. Eur J Nucl Med Mol Imaging. 2013;40:486–495.
  • Mease RC, Dusich CL, Foss CA, et al. N-[N-[(S)-1,3-dicarboxypropyl]carbamoyl]-4-[18F]fluorobenzyl-L-cysteine, [18F]DCFBC: a new imaging probe for prostate cancer. Clin Cancer Res. 2008;14:3036–3043.
  • Ulmert D, Evans MJ, Holland JP, et al. Imaging androgen receptor signaling with a radiotracer targeting free prostate-specific antigen. Cancer Discov. 2012;2:320–327.
  • Wu AM. Antibodies and antimatter: the resurgence of immuno-PET. J Nucl Med. 2009;50:2–5.
  • Wu AM. Engineered antibodies for molecular imaging of cancer. Methods. 2014;65:139–147.
  • Murphy G, Haider M, Ghai S, et al. The expanding role of MRI in prostate cancer. AJR Am J Roentgenol. 2013;201:1229–1238.
  • Turkbey B, Mani H, Shah V, et al. Multiparametric 3T prostate magnetic resonance imaging to detect cancer: histopathological correlation using prostatectomy specimens processed in customizedmagnetic resonance imaging based molds. J Urol. 2011;186:1818–1824.
  • Isebaert S, Bergh LV, Haustermans K, et al. Multiparametric MRI for prostate cancer localization in correlation to whole-mount histopathology. J Magn Reson Imaging. 2013;37:1392–1401.
  • Siddiqui MM, Rais-Bahrami S, Turkbey B, et al. Comparison of MR/ultrasound fusion-guided biopsy with ultrasound-guided biopsy for the diagnosis of prostate cancer. JAMA. 2015;313(4):390–397.
  • Valerio M, Ahmed HU, Emberton M, et al. The role of focal therapy in the management of localised prostate cancer: a systematic review. Eur Urol. 2014;66(4):732–751.
  • Sankineni S, Wood BJ, Rais-Bahrami S, et al. Image guided focal therapy for prostate cancer. Diagn Interv Radiol. 2014;20(6):492–497.
  • Park BH, Jeon HG, Choo SH, et al. Role of multiparametric 3.0-Tesla magnetic resonance imaging in patients with prostate cancer eligible for active surveillance. BJU Int. 2014;113(6):864–870.
  • Barchetti F, Panebianco V. Multiparametric MRI for recurrent prostate cancer post radical prostatectomy and postradiation therapy. Biomed Res Int. 2014;2014:1–23.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.