Spectroscopic imaging through magnetic resonance for brain tumour diagnostics: Recent achievements, dilemmas and potential solutions via advances in signal processing

In the very recent period Magnetic Resonance Spectroscopy (MRS) and Spectroscopic Imaging (MRSI) have become key diagnostic modalities for neuro-oncology. MRS and MRSI are now applied extensively for initial detection of brain tumours, for histopathologic classification, tumour localization and grading, as well as for assessment of response to therapy and for follow-up surveillance, striving, in particular, for earlier identification of recurrence. In this paper we review the current state of the art of MRS and MRSI for brain tumour diagnostics, highlighting the achievements, as well as remaining dilemmas. Clearly, MRS and MRSI represent an important advance for the detection and characterisation of tumours of the brain. However, there are still important shortcomings of the present applications of MRS and MRSI in neuro-oncology. First of all, very few of the currently assessed metabolite concentrations or ratios unequivocally distinguish intra-cerebral tumours from normal brain tissue. Moreover, changes in each of the metabolite concentrations and ratios are non-specific for cancer of the brain. In other words, non-neoplastic processes such as infection, stroke, demyelinating disorders, inter alia, frequently show spectral changes that are identical to those seen in brain tumours. Histopathological characterization and tumour grading, both crucial for clinical decision-making, have been greatly aided by MRS and MRSI. However, there are numerous contradictory findings in the literature. We demonstrate in this paper that many of the shortcomings of MRS and MRSI for neuro-oncology are directly related to the reliance upon the conventional Fourier-based framework for data analysis. We review the distinct advantages of the Fast Pade Transform (FPT) relative to the Fast Fourier Transform (FFT). Our focus is on those salient features of the FPT that are of critical clinical relevance for achieving an overall improved diagnostic performance of MRS and MRSI. These features are extremely stable and rapid convergence, as well as highly accurate quantification estimates of spectra from in vivo MRS time signals, as presently illustrated for data from the brain of a healthy volunteer. The next, and urgently needed step, is to more widely apply the FPT to in vivo MRS and MRSI signals from patients with brain tumours with the aim of tackling, in actual practice, the diagnostic dilemmas still plaguing neuro-oncology.

[1]  Carles Arús,et al.  Adult primitive neuroectodermal tumor: proton MR spectroscopic findings with possible application for differential diagnosis. , 2002, Radiology.

[2]  Liliana Goumnerova,et al.  Biochemical characterization of pediatric brain tumors by using in vivo and ex vivo magnetic resonance spectroscopy. , 2002, Journal of neurosurgery.

[3]  K Kikuchi,et al.  Discrimination of brain abscess and cystic tumor by in vivo proton magnetic resonance spectroscopy. , 2001, Neurologia medico-chirurgica.

[4]  Karen Belkić,et al.  Magnetic Resonant Spectroscopy and Spectroscopic Imaging: A Review of Basic Principles and Recent Achievements in Oncology , 2003 .

[5]  Thomas Dierks,et al.  Determination of histopathological tumor grade in neuroepithelial brain tumors by using spectral pattern analysis of in vivo spectroscopic data. , 2003, Journal of neurosurgery.

[6]  W. Hall,et al.  Influence of 1.5-Tesla intraoperative MR imaging on surgical decision making. , 2003, Acta neurochirurgica. Supplement.

[7]  B. Ross,et al.  Short-Echo Time Proton MR Spectroscopy in the Presence of Gadolinium , 2001, Journal of computer assisted tomography.

[8]  A R Tate,et al.  The contribution of proton magnetic resonance spectroscopy ( 1 HMRS) to clinical brain tumour diagnosis , 2002, British journal of neurosurgery.

[9]  P. Black,et al.  Cellular-telephone use and brain tumors. , 2001, The New England journal of medicine.

[10]  N. Bulakbaşı,et al.  Combination of single-voxel proton MR spectroscopy and apparent diffusion coefficient calculation in the evaluation of common brain tumors. , 2003, AJNR. American journal of neuroradiology.

[11]  L. Martí-Bonmatí,et al.  [The contribution of magnetic resonance spectroscopy to the classification of high grade gliomas. The predictive value of macromolecules]. , 2002, Revista de neurologia.

[12]  M. Kundi,et al.  Mobile telephones and cancer: is there really no evidence of an association? (review). , 2003, International journal of molecular medicine.

[13]  Meng Law,et al.  Proton MR spectroscopy of tumefactive demyelinating lesions. , 2002, AJNR. American journal of neuroradiology.

[14]  S. Provencher Estimation of metabolite concentrations from localized in vivo proton NMR spectra , 1993, Magnetic resonance in medicine.

[15]  D. Hoffmann,et al.  Necrotic tumor versus brain abscess: importance of amino acids detected at 1H MR spectroscopy--initial results. , 1999, Radiology.

[16]  L. Astrakas,et al.  Spectroscopic and perfusion magnetic resonance imaging predictors of progression in pediatric brain tumors , 2004, Cancer.

[17]  J. Walecki,et al.  1H-MRS in vivo predicts the early treatment outcome of postoperative radiotherapy for malignant gliomas. , 2002, International journal of radiation oncology, biology, physics.

[18]  Current dilemmas and future perspectives for breast cancer screening with a focus on optimization of magnetic resonance spectroscopic imaging by advances in signal processing. , 2004, The Israel Medical Association journal : IMAJ.

[19]  Ewald Moser,et al.  High‐resolution 3D proton spectroscopic imaging of the human brain at 3 T: SNR issues and application for anatomy‐matched voxel sizes , 2003, Magnetic resonance in medicine.

[20]  Wolfgang Grodd,et al.  Parameterized evaluation of macromolecules and lipids in proton MR spectroscopy of brain diseases , 2003, Magnetic resonance in medicine.

[21]  M. Rijpkema,et al.  Characterization of oligodendrogliomas using short echo time 1H MR spectroscopic imaging , 2003, NMR in biomedicine.

[22]  V. Tugnoli,et al.  Characterization of lipids from human brain tissues by multinuclear magnetic resonance spectroscopy. , 2001, Biopolymers.

[23]  S. Provencher Automatic quantitation of localized in vivo 1H spectra with LCModel , 2001, NMR in biomedicine.

[24]  Douglas L Rothman,et al.  Magnetic resonance spectroscopy of neurotransmitters in human brain , 2003, Annals of neurology.

[25]  W El-Deredy,et al.  Tumour grading from magnetic resonance spectroscopy: a comparison of feature extraction with variable selection , 2003, Statistics in medicine.

[26]  Akira Matsumura,et al.  Quantification of cerebral metabolites in glioma patients with proton MR spectroscopy using T2 relaxation time correction. , 2002, Magnetic resonance imaging.

[27]  Damien Galanaud,et al.  Use of proton magnetic resonance spectroscopy of the brain to differentiate gliomatosis cerebri from low-grade glioma. , 2003, Journal of neurosurgery.

[28]  K. H. Mild,et al.  Case-control study on the use of cellular and cordless phones and the risk for malignant brain tumours , 2002, International journal of radiation biology.

[29]  C. Arús,et al.  Utility of proton MR spectroscopy in the diagnosis of radiologically atypical intracranial meningiomas , 2003, Neuroradiology.

[30]  J. Olsen,et al.  Acromegaly and cancer risk: a cohort study in Sweden and Denmark , 2002, Cancer Causes & Control.

[31]  C Gössl,et al.  Improved analysis of 1H‐MR spectra in the presence of mobile lipids , 2001, Magnetic resonance in medicine.

[32]  James B Murdoch,et al.  Proton MR spectroscopy of gliomatosis cerebri: case report of elevated myoinositol with normal choline levels. , 2003, AJNR. American journal of neuroradiology.

[33]  A. Auvinen,et al.  Incidence of cancer among Nordic airline pilots over five decades: occupational cohort study , 2002, BMJ : British Medical Journal.

[34]  G. Colditz,et al.  Sex steroid hormone exposures and risk for meningioma. , 2003, Journal of neurosurgery.

[35]  K. Belkic Magnetic resonance spectroscopic imaging in breast cancer detection: possibilities beyond the conventional theoretical framework for data analysis , 2004 .

[36]  V. L. Doyle,et al.  Metabolic profiles of human brain tumors using quantitative in vivo 1H magnetic resonance spectroscopy , 2003, Magnetic resonance in medicine.

[37]  W. Hall,et al.  Improving diagnostic yield in brain biopsy: Coupling spectroscopic targeting with real‐time needle placement , 2001, Journal of magnetic resonance imaging : JMRI.

[38]  M. Harada,et al.  Brain abscess and glioblastoma identified by combined proton magnetic resonance spectroscopy and diffusion-weighted magnetic resonance imaging--two case reports. , 2002, Neurologia medico-chirurgica.

[39]  Kunio Tanaka,et al.  In vivo single‐voxel proton MR spectroscopy in brain lesions with ring‐like enhancement , 2001, NMR in biomedicine.

[40]  P. Black,et al.  Multiparametric MR assessment of pediatric brain tumors , 2002, Neuroradiology.

[41]  J K Smith,et al.  Correlation of myo-inositol levels and grading of cerebral astrocytomas. , 2000, AJNR. American journal of neuroradiology.

[42]  Roland G Henry,et al.  Characterization of untreated gliomas by magnetic resonance spectroscopic imaging. , 2002, Neuroimaging clinics of North America.

[43]  Risto A Kauppinen,et al.  Monitoring cytotoxic tumour treatment response by diffusion magnetic resonance imaging and proton spectroscopy , 2002, NMR in biomedicine.

[44]  D. Arnold,et al.  Proton Magnetic Resonance Spectroscopic Imaging Can Predict Length of Survival in Patients with Supratentorial Gliomas , 2003, Neurosurgery.

[45]  Dževad Belkić Exact Analytical Expressions for Any Lorentzian Spectrum in the Fast Padé Transform (FPT) , 2003 .

[46]  Edward E Graves,et al.  Metabolic imaging of low-grade gliomas with three-dimensional magnetic resonance spectroscopy. , 2002, International journal of radiation oncology, biology, physics.

[47]  T. Aburano,et al.  Diagnosis and treatment of progressive space-occupying radiation necrosis following stereotactic radiosurgery for brain metastasis: Value of proton magnetic resonance spectroscopy , 2003, Acta Neurochirurgica.

[48]  Mauricio Castillo,et al.  Clinical Applications of Proton MR Spectroscopy in Oncology , 2002, Technology in cancer research & treatment.

[49]  A. van den Boogaart,et al.  Quantitative data analysis of in vivo MRS data sets , 1997 .

[50]  L. Brandão,et al.  MR Spectroscopy of the Brain , 2003 .

[51]  V. Tugnoli,et al.  Cholesteryl esters in human malignant neoplasms. , 2003, International journal of molecular medicine.

[52]  Susan M. Chang,et al.  Three-dimensional magnetic resonance spectroscopic imaging of histologically confirmed brain tumors. , 2001, Magnetic resonance imaging.

[53]  J. Walecki,et al.  Hydrogen-1 MR spectroscopy of the peritumoral zone in patients with cerebral glioma: assessment of the value of the method. , 2003, Academic radiology.

[54]  D. Belkić Strikingly stable convergence of the Fast Padé Transform (FPT) for high-resolution parametric and non-parametric signal processing of Lorentzian and non-Lorentzian spectra , 2004 .

[55]  T. Mikkelsen,et al.  Correlation between Magnetic Resonance Spectroscopy Imaging and Image-guided Biopsies: Semiquantitative and Qualitative Histopathological Analyses of Patients with Untreated Glioma , 2001, Neurosurgery.

[56]  Mark A. Brown,et al.  MRI: Basic Principles and Applications , 1995 .

[57]  S. Nelson Multivoxel magnetic resonance spectroscopy of brain tumors. , 2003, Molecular cancer therapeutics.

[58]  Leo L. Cheng,et al.  Quantification of microheterogeneity in glioblastoma multiforme with ex vivo high-resolution magic-angle spinning (HRMAS) proton magnetic resonance spectroscopy. , 2000, Neuro-oncology.

[59]  H. Minn,et al.  Evaluation of brain tumor metabolism with [11C]choline PET and 1H-MRS , 2003, Journal of Neuro-Oncology.

[60]  S. Shibata,et al.  Diagnostic potential of short echo time MR spectroscopy of gliomas with single-voxel and point-resolved spatially localised proton spectroscopy of brain , 2001, Neuroradiology.

[61]  Carles Arús,et al.  Proton magnetic resonance spectroscopy (1H MRS) of human brain tumours: assessment of differences between tumour types and its applicability in brain tumour categorization , 2003, European Radiology.

[62]  A R Tate,et al.  Magnetic resonance spectroscopy of brain hemangiopericytomas: high myoinositol concentrations and discrimination from meningiomas. , 2001, Journal of neurosurgery.

[63]  G. Reifenberger,et al.  Diagnostic difficulties in childhood bilateral thalamic astrocytomas. , 2003, Neuropediatrics.

[64]  M. Berger,et al.  Histopathological validation of a three-dimensional magnetic resonance spectroscopy index as a predictor of tumor presence. , 2002, Journal of neurosurgery.

[65]  L Verhey,et al.  Serial proton MR spectroscopic imaging of recurrent malignant gliomas after gamma knife radiosurgery. , 2001, AJNR. American journal of neuroradiology.

[66]  V. Govindaraju,et al.  Proton NMR chemical shifts and coupling constants for brain metabolites , 2000, NMR in biomedicine.

[67]  Mario Forjaz Secca,et al.  MRI Principles of the Head, Skull Base and Spine , 2002, Springer Paris.

[68]  Ying Lu,et al.  Analysis of the spatial characteristics of metabolic abnormalities in newly diagnosed glioma patients , 2002, Journal of magnetic resonance imaging : JMRI.

[69]  An efficient chemical shift imaging scheme for magnetic resonance‐guided neurosurgery , 2001, Journal of magnetic resonance imaging : JMRI.

[70]  B. Barbiroli,et al.  Gliomatosis cerebri: clinical, neurochemical and neuroradiological response to temozolomide administration. , 2003, Magnetic resonance imaging.

[71]  Z. Wu,et al.  In vivo single-voxel proton MR spectroscopy in the differentiation of high-grade gliomas and solitary metastases. , 2004, Clinical radiology.

[72]  Gi-Hwan Choi,et al.  (1)H-MRS metabolic patterns for distinguishing between meningiomas and other brain tumors. , 2003, Magnetic resonance imaging.

[73]  H. Lanfermann,et al.  Clinical application of proton magnetic resonance spectroscopy in the diagnosis of intracranial mass lesions , 2002, Neuroradiology.

[74]  Karen Belkić,et al.  The Need for Quantitative Biomedical Spectroscopic Imaging through Magnetic Resonance in Oncology beyond the Conventional Fourier-Based Signal Processing , 2003 .

[75]  R. Floris,et al.  Diffusion-weighted MR Imaging: clinical applications in neuroradiology. , 2003, La Radiologia medica.

[76]  L. Kwock,et al.  Proton magnetic resonance spectroscopy of brain-stem lesions , 2002, Neuroradiology.

[77]  E. A. Chiocca,et al.  In vivo 3-T MR spectroscopy in the distinction of recurrent glioma versus radiation effects: initial experience. , 2002, Radiology.

[78]  D. Birchall,et al.  Use of serial proton magnetic resonance spectroscopy to differentiate low grade glioma from tumefactive plaque in a patient with multiple sclerosis. , 2003, The British journal of radiology.

[79]  F. Howe,et al.  Detection of elevated glutathione in meningiomas by quantitative in vivo 1H MRS , 2003, Magnetic resonance in medicine.

[80]  M. Leach,et al.  Could assessment of glioma methylene lipid resonance by in vivo (1)H-MRS be of clinical value? , 2003, The British journal of radiology.

[81]  D. Belkić Fast Padé transform for magnetic resonance imaging and computerized tomography , 2001 .

[82]  P. Bottomley,et al.  The trouble with spectroscopy papers , 1992, Journal of magnetic resonance imaging : JMRI.

[83]  J. Walecki,et al.  Malignancy of brain tumors evaluated by proton magnetic resonance spectroscopy (1H-MRS) in vitro. , 2000, Acta neurochirurgica. Supplement.

[84]  Daniel B Vigneron,et al.  In vivo molecular imaging for planning radiation therapy of gliomas: An application of 1H MRSI , 2002, Journal of magnetic resonance imaging : JMRI.

[85]  W P Dillon,et al.  Preoperative proton MR spectroscopic imaging of brain tumors: correlation with histopathologic analysis of resection specimens. , 2001, AJNR. American journal of neuroradiology.

[86]  Vanhamme,et al.  Improved method for accurate and efficient quantification of MRS data with use of prior knowledge , 1997, Journal of magnetic resonance.

[87]  Brian D. Ross,et al.  Magnetic Resonance Spectroscopy Diagnosis of Neurological Diseases , 1999 .

[88]  M. Oudkerk,et al.  1H chemical shift imaging characterization of human brain tumor and edema , 2002, European Radiology.

[89]  P. Brown,et al.  Properly Selected Patients with Multiple Brain Metastases May Benefit from Aggressive Treatment of their Intracranial Disease , 2004, Journal of Neuro-Oncology.

[90]  G. van Kaick,et al.  Differentiation of radiation necrosis from tumor progression using proton magnetic resonance spectroscopy , 2002, Neuroradiology.

[91]  Walter Heindel,et al.  Phosphorus‐31 MR spectroscopy of normal adult human brain and brain tumours , 2002, NMR in biomedicine.

[92]  W. Schlote,et al.  Preoperative Proton-MR Spectroscopy of Gliomas – Correlation with Quantitative Nuclear Morphology in Surgical Specimen , 2003, Journal of Neuro-Oncology.

[93]  Glyn Johnson,et al.  High-grade gliomas and solitary metastases: differentiation by using perfusion and proton spectroscopic MR imaging. , 2002, Radiology.

[94]  B. Kupelnick,et al.  Dietary cured meat and the risk of adult glioma: a meta-analysis of nine observational studies. , 2003, Journal of environmental pathology, toxicology and oncology : official organ of the International Society for Environmental Toxicology and Cancer.

[95]  G Friedmann,et al.  Human brain tumors: spectral patterns detected with localized H-1 MR spectroscopy. , 1992, Radiology.

[96]  A. Villringer,et al.  Stroke Magnetic Resonance Imaging Is Accurate in Hyperacute Intracerebral Hemorrhage: A Multicenter Study on the Validity of Stroke Imaging , 2004, Stroke.

[97]  Carles Arús,et al.  Automated classification of short echo time in in vivo 1H brain tumor spectra: A multicenter study , 2003, Magnetic resonance in medicine.

[98]  H. Zeeb,et al.  Mortality from cancer and other causes among male airline cockpit crew in Europe , 2003, International journal of cancer.

[99]  R. Sener Astroblastoma: diffusion MRI, and proton MR spectroscopy. , 2002, Computerized medical imaging and graphics : the official journal of the Computerized Medical Imaging Society.

[100]  A. Falini,et al.  Anatomical and biochemical investigation of primary brain tumours , 2001, European Journal of Nuclear Medicine.

[101]  J A Sorenson,et al.  Localized 2D J‐resolved H MR spectroscopy of human brain tumors in vivo , 1996, Journal of magnetic resonance imaging : JMRI.

[102]  M. Lim,et al.  Cosmic rays: are air crew at risk? , 2002, Occupational and environmental medicine.

[103]  F. Floeth,et al.  Comparative follow-up of enhancement phenomena with MRI and Proton MR Spectroscopic Imaging after intralesional immunotherapy in glioblastoma--Report of two exceptional cases. , 2002, Zentralblatt fur Neurochirurgie.

[104]  L. G. Astrakas,et al.  Proton magnetic spectroscopic imaging of the child's brain: the response of tumors to treatment , 2001, Neuroradiology.

[105]  H. Urbach,et al.  1H-MR-Spektroskopie von Hirntumoren im Verlauf der Strahlentherapie: Anwendung von schneller spektroskopischer Bildgebung und Einzelvolumen-MRS in der Rezidivdiagnostik , 2002 .