Proton magnetic resonance spectroscopy in patients with glial tumors: a multicenter study

Restricted access

✓ The authors represent a cooperative group of 15 institutions that examined the feasibility of using metabolic features observed in vivo with 1H-magnetic resonance (MR) spectroscopy to characterize brain tumors of the glial type. The institutions provided blinded, centralized MR spectroscopy data processing along with independent central review of MR spectroscopy voxel placement, composition and contamination by brain, histopathological typing using current World Health Organization criteria, and clinical data. Proton 1H-MR spectroscopy was performed using a spin-echo technique to obtain spectra from 8-cc voxels in the tumor and when feasible in the contralateral brain. Eighty-six cases were assessable, 41 of which had contralateral brain spectra. Glial tumors had significantly elevated intensities of choline signals, decreased intensities of creatine signals, and decreased intensities of N-acetylaspartate compared to brain. Choline signal intensities were highest in astrocytomas and anaplastic astrocytomas, and creatine signal intensities were lowest in glioblastomas. However, whether expressed relative to brain or as intratumoral ratios, these metabolic characteristics exhibited large variations within each subtype of glial tumor. The resulting overlaps precluded diagnostic accuracy in the distinction of low- and high-grade tumors. Although the extent of contamination of the 1HMR spectroscopy voxel by brain had a marked effect on metabolite concentrations and ratios, selection of cases with minimal contamination did not reduce these overlaps. Thus, each type and grade of tumor is a metabolically heterogeneous group. Lactate occurred infrequently and in all grades. Mobile lipids, on the other hand, occurred in 41% of high-grade tumors with higher mean amounts found in glioblastomas. This result, coupled with the recent demonstration that intratumoral mobile lipids correlate with microscopic tumor cell necrosis, leads to the hypothesis that mobile lipids observed in vivo in 1H-MR spectroscopy may correlate independently with prognosis of individual patients.

Article Information

Address reprint requests to: William G. Negendank, M.D., Department of NMR and Medical Spectroscopy, Fox Chase Cancer Center, 7701 Burholme Avenue, Philadelphia, Pennsylvania 19111.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Evaluation algorithm used in the study. MRI = magnetic resonance imaging; MRS = magnetic resonance spectroscopy; Q.C. = quality control.

  • View in gallery

    Magnetic resonance (MR) spectroscopy voxel locations and 1H-MR spectra in a patient with an astrocytic tumor in the right parietal lobe. Upper Left: A T2-weighted MR image showing the position of the 2 × 2 × 2 cm voxel centered in the tumor. Upper Right: A T2-weighted MR image showing the position of the 2 × 2 × 2 cm voxel in the contralateral brain. Lower Left and Right: Charts displaying 1H-MR spectra from the tumor (lower left) and the contralateral brain (lower right).

  • View in gallery

    Graph depicting the effect of voxel contamination by brain on ratios of metabolite signal intensities in tumors to those in contralateral brain. The fractions of tumor within the magnetic resonance spectroscopy voxels are indicated. Values are expressed as means ± standard error. CHOL = choline; CR = creatine; NAA = N-acetylaspartate.

  • View in gallery

    Graph displaying the means, standard deviations, and scatterplot of cholines, creatines, and N-acetylaspartate (NAA) region in astrocytic tumors expressed as ratios to the creatine peak intensities in contralateral brain. AA = anaplastic astrocytomas; AS = astrocytomas; B = brain; GB = glioblastomas multiforme. Significance of differences (p) compared to brain: for cholines, AS 0.0014, AA 0.0002, and GB 0.1905; for creatines, AS 0.9999, AA < 0.0001, and GB 0.0001; for NAA region, AS, AA, and GB < 0.0001.

  • View in gallery

    Examples of spectra with lipids or lactate. Left: Lactate-CH3 appears as an inverted doublet at 1.3 ppm (asterisk). Right: Lipids with the dominant fatty acyl-CH2 peak at 1.3 ppm and the -CH3 at 0.9 ppm (asterisks).

  • View in gallery

    Graph showing lipids in astrocytic tumors, expressed as the ratio of intensity of the 1.3 ppm methylene peak to that of cholines (Chol). AA = anaplastic astrocytomas; AS = astrocytomas; GBM = glioblastomas multiforme.

References

  • 1.

    Alavi JBAlavi AChawluk Jet al: Positron emission tomography in patients with glioma. A predictor of prognosis. Cancer 62:107410781988Alavi JB Alavi A Chawluk J et al: Positron emission tomography in patients with glioma. A predictor of prognosis. Cancer 62:1074–1078 1988

    • Search Google Scholar
    • Export Citation
  • 2.

    Alger JRFrank JABizzi Aet al: Metabolism of human gliomas: assessment with H-1 MR spectroscopy and F-18 fluorodeoxyglucose PET. Radiology 177:6336411990Alger JR Frank JA Bizzi A et al: Metabolism of human gliomas: assessment with H-1 MR spectroscopy and F-18 fluorodeoxyglucose PET. Radiology 177:633–641 1990

    • Search Google Scholar
    • Export Citation
  • 3.

    Alger JRSymko SCBizzi Aet al: Absolute quantitation of short TE brain 1H-MR spectra and spectroscopic imaging data. J Comput Assist Tomogr 17:1911991993Alger JR Symko SC Bizzi A et al: Absolute quantitation of short TE brain 1H-MR spectra and spectroscopic imaging data. J Comput Assist Tomogr 17:191–199 1993

    • Search Google Scholar
    • Export Citation
  • 4.

    Arnold DLShoubridge EAVillemure JGet al: Proton and phosphorus magnetic resonance spectroscopy of human astrocytomas in vivo. Preliminary observations on tumor grading. NMR Biomed 3:1841891990Arnold DL Shoubridge EA Villemure JG et al: Proton and phosphorus magnetic resonance spectroscopy of human astrocytomas in vivo. Preliminary observations on tumor grading. NMR Biomed 3:184–189 1990

    • Search Google Scholar
    • Export Citation
  • 5.

    Aronen HJGazit IELouis DNet al: Cerebral blood volume maps of gliomas: comparison with tumor grade and histologic findings. Radiology 191:41511994Aronen HJ Gazit IE Louis DN et al: Cerebral blood volume maps of gliomas: comparison with tumor grade and histologic findings. Radiology 191:41–51 1994

    • Search Google Scholar
    • Export Citation
  • 6.

    Behar KLOgino T: Characterization of macromolecule resonances in the 1H NMR spectrum of rat brain. Magn Reson Med 30:38401993Behar KL Ogino T: Characterization of macromolecule resonances in the 1H NMR spectrum of rat brain. Magn Reson Med 30:38–40 1993

    • Search Google Scholar
    • Export Citation
  • 7.

    Bottomley PA: Spatial localization in NMR spectroscopy in vivo. Ann NY Acad Sci 508:3333481987Bottomley PA: Spatial localization in NMR spectroscopy in vivo. Ann NY Acad Sci 508:333–348 1987

    • Search Google Scholar
    • Export Citation
  • 8.

    Bruhn HFrahm JGyngell MLet al: Noninvasive differentiation of tumors with use of localized H-1 MR spectroscopy in vivo: initial experience in patients with cerebral tumors. Radiology 172:5415481989Bruhn H Frahm J Gyngell ML et al: Noninvasive differentiation of tumors with use of localized H-1 MR spectroscopy in vivo: initial experience in patients with cerebral tumors. Radiology 172:541–548 1989

    • Search Google Scholar
    • Export Citation
  • 9.

    Burger PCVogel FSGreen SBet al: Glioblastoma multiforme and anaplastic astrocytoma. Pathologic criteria and prognostic implications. Cancer 56:110611111985Burger PC Vogel FS Green SB et al: Glioblastoma multiforme and anaplastic astrocytoma. Pathologic criteria and prognostic implications. Cancer 56:1106–1111 1985

    • Search Google Scholar
    • Export Citation
  • 10.

    Daumas-Duport CScheithauer BO'Fallon Jet al: Grading of astrocytomas. A simple and reproducible method. Cancer 62:215221651988Daumas-Duport C Scheithauer B O'Fallon J et al: Grading of astrocytomas. A simple and reproducible method. Cancer 62:2152–2165 1988

    • Search Google Scholar
    • Export Citation
  • 11.

    Demaerel PJohannik KVan Hecke Pet al: Localized 1H NMR spectroscopy in fifty cases of newly diagnosed intracranial tumors. J Comput Assist Tomogr 15:67761991Demaerel P Johannik K Van Hecke P et al: Localized 1H NMR spectroscopy in fifty cases of newly diagnosed intracranial tumors. J Comput Assist Tomogr 15:67–76 1991

    • Search Google Scholar
    • Export Citation
  • 12.

    Frahm JBruhn HHänicke Wet al: Localized proton NMR spectroscopy of brain tumors using short-echo time STEAM sequences. J Comput Assist Tomogr 15:9159221991Frahm J Bruhn H Hänicke W et al: Localized proton NMR spectroscopy of brain tumors using short-echo time STEAM sequences. J Comput Assist Tomogr 15:915–922 1991

    • Search Google Scholar
    • Export Citation
  • 13.

    Freitas IPontiggia PBarni Set al: Histochemical probes for the detection of hypoxic tumour cells. Anticancer Res 10:6136221990Freitas I Pontiggia P Barni S et al: Histochemical probes for the detection of hypoxic tumour cells. Anticancer Res 10:613–622 1990

    • Search Google Scholar
    • Export Citation
  • 14.

    Fulham MJBizzi ADietz MJet al: Mapping of brain tumor metabolites with proton MR spectroscopic imaging: clinical relevance. Radiology 185:6756861992Fulham MJ Bizzi A Dietz MJ et al: Mapping of brain tumor metabolites with proton MR spectroscopic imaging: clinical relevance. Radiology 185:675–686 1992

    • Search Google Scholar
    • Export Citation
  • 15.

    Furuya SNaruse SIde Met al: [The clinical application of multi-voxel 1H-CSI (chemical shift imaging) in brain tumors.] Nippon Igaku Hoshasen Gakkai Zasshi 51:8368381991 (Jpn)Furuya S Naruse S Ide M et al: [The clinical application of multi-voxel 1H-CSI (chemical shift imaging) in brain tumors.] Nippon Igaku Hoshasen Gakkai Zasshi 51:836–838 1991 (Jpn)

    • Search Google Scholar
    • Export Citation
  • 16.

    Gill SSThomas DGTVan Bruggen Net al: Proton MR spectroscopy of intracranial tumours: in vivo and in vitro studies. J Comput Assist Tomogr 14:4975041990Gill SS Thomas DGT Van Bruggen N et al: Proton MR spectroscopy of intracranial tumours: in vivo and in vitro studies. J Comput Assist Tomogr 14:497–504 1990

    • Search Google Scholar
    • Export Citation
  • 17.

    Haase AFrahm JHänicke Wet al: 1H NMR chemical shift selective (CHESS) imaging. Phys Med Biol 30:3413441985Haase A Frahm J Hänicke W et al: 1H NMR chemical shift selective (CHESS) imaging. Phys Med Biol 30:341–344 1985

    • Search Google Scholar
    • Export Citation
  • 18.

    Haase AFrahm JMatthaei Det al: FLASH imaging. Rapid NMR imaging using low flip-angle pulses. J Magn Reson 67:2582661986Haase A Frahm J Matthaei D et al: FLASH imaging. Rapid NMR imaging using low flip-angle pulses. J Magn Reson 67:258–266 1986

    • Search Google Scholar
    • Export Citation
  • 19.

    Hasso AN: Current status of enhanced magnetic resonance imaging in neuroradiology. Invest Radiol 28 (Suppl 1):S3S201993Hasso AN: Current status of enhanced magnetic resonance imaging in neuroradiology. Invest Radiol 28 (Suppl 1):S3–S20 1993

    • Search Google Scholar
    • Export Citation
  • 20.

    Heesters MAAMKamman RLMooyaart ELet al: Localized proton spectroscopy of inoperable brain gliomas. Response to radiation therapy. J Neurooncol 17:27351993Heesters MAAM Kamman RL Mooyaart EL et al: Localized proton spectroscopy of inoperable brain gliomas. Response to radiation therapy. J Neurooncol 17:27–35 1993

    • Search Google Scholar
    • Export Citation
  • 21.

    Henriksen OWieslander SGjerris Fet al: In vivo 1H-spectroscopy of human intracranial tumors at 1.5 Tesla. Preliminary experience at a clinical installation. Acta Radiol 32:95991991Henriksen O Wieslander S Gjerris F et al: In vivo1H-spectroscopy of human intracranial tumors at 1.5 Tesla. Preliminary experience at a clinical installation. Acta Radiol 32:95–99 1991

    • Search Google Scholar
    • Export Citation
  • 22.

    Herholz KHeindel WLuyten PRet al: In vivo imaging of glucose consumption and lactate concentration in human gliomas. Ann Neurol 31:3193271992Herholz K Heindel W Luyten PR et al: In vivo imaging of glucose consumption and lactate concentration in human gliomas. Ann Neurol 31:319–327 1992

    • Search Google Scholar
    • Export Citation
  • 23.

    H”lzer THerholz KJeske Jet al: FDG-PET as a prognostic indicator in radiochemotherapy of glioblastoma. J Comput Assist Tomogr 17:6816871993H”lzer T Herholz K Jeske J et al: FDG-PET as a prognostic indicator in radiochemotherapy of glioblastoma. J Comput Assist Tomogr 17:681–687 1993

    • Search Google Scholar
    • Export Citation
  • 24.

    Husted CADuijn JHMatson GBet al: Molar quantitation of in vivo proton metabolites in human brain with 3D magnetic resonance spectroscopic imaging. Magn Reson Imaging 12:6616671994Husted CA Duijn JH Matson GB et al: Molar quantitation of in vivo proton metabolites in human brain with 3D magnetic resonance spectroscopic imaging. Magn Reson Imaging 12:661–667 1994

    • Search Google Scholar
    • Export Citation
  • 25.

    Kim CKAlavi JBAlavi Aet al: New grading system of cerebral gliomas using positron emission tomography with F-18 fluorodeoxyglucose. J Neurooncol 10:85911991Kim CK Alavi JB Alavi A et al: New grading system of cerebral gliomas using positron emission tomography with F-18 fluorodeoxyglucose. J Neurooncol 10:85–91 1991

    • Search Google Scholar
    • Export Citation
  • 26.

    Kinoshita YKajiwara HYokota Aet al: Proton magnetic resonance spectroscopy of brain tumors: an in vitro study. Neurosurgery 35:6066131994Kinoshita Y Kajiwara H Yokota A et al: Proton magnetic resonance spectroscopy of brain tumors: an in vitro study. Neurosurgery 35:606–613 1994

    • Search Google Scholar
    • Export Citation
  • 27.

    Kleihues PBurger PCScheithauer BW: Histological Typing of Tumours of the Central Nervous Systemed 2. Berlin: Springer-Verlag1993Kleihues P Burger PC Scheithauer BW: Histological Typing of Tumours of the Central Nervous System ed 2. Berlin: Springer-Verlag 1993

    • Search Google Scholar
    • Export Citation
  • 28.

    Klose U: In vivo proton spectroscopy in presence of eddy currents. Magn Reson Med 14:26301990Klose U: In vivo proton spectroscopy in presence of eddy currents. Magn Reson Med 14:26–30 1990

    • Search Google Scholar
    • Export Citation
  • 29.

    Kreis RErnst TRoss BD: Absolute quantitation of water and metabolites in the human brain. II. Metabolite concentrations. J Magn Reson (B) 102:9191993Kreis R Ernst T Ross BD: Absolute quantitation of water and metabolites in the human brain. II. Metabolite concentrations. J Magn Reson (B) 102:9–19 1993

    • Search Google Scholar
    • Export Citation
  • 30.

    Kuesel ACDonnelly SMHalliday Wet al: Mobile lipids and metabolic heterogeneity of brain tumours as detectable by ex vivo 1H MR spectroscopy. NMR Biomed 7:1721801994Kuesel AC Donnelly SM Halliday W et al: Mobile lipids and metabolic heterogeneity of brain tumours as detectable by ex vivo1H MR spectroscopy. NMR Biomed 7:172–180 1994

    • Search Google Scholar
    • Export Citation
  • 31.

    Kuesel ACSutherland GRHalliday Wet al: 1H MR spectroscopy of high grade astrocytomas: mobile lipid accumulation in necrotic tissue. NMR Biomed 7:1491551994Kuesel AC Sutherland GR Halliday W et al: 1H MR spectroscopy of high grade astrocytomas: mobile lipid accumulation in necrotic tissue. NMR Biomed 7:149–155 1994

    • Search Google Scholar
    • Export Citation
  • 32.

    Kugel HHeindel WErnestus RIet al: Human brain tumors: spectral patterns detected with localized H-1 MR spectroscopy. Radiology 183:7017091992Kugel H Heindel W Ernestus RI et al: Human brain tumors: spectral patterns detected with localized H-1 MR spectroscopy. Radiology 183:701–709 1992

    • Search Google Scholar
    • Export Citation
  • 33.

    Lowry OHBerger SJChi MYet al: Diversity of metabolic patterns in human brain tumors—I. High energy phosphate compounds and basic composition. J Neurochem 29:9599771977Lowry OH Berger SJ Chi MY et al: Diversity of metabolic patterns in human brain tumors—I. High energy phosphate compounds and basic composition. J Neurochem 29:959–977 1977

    • Search Google Scholar
    • Export Citation
  • 34.

    Majors AXue MNg TCet al: Short echo time proton spectroscopy of human brain using a gradient head coil. Magn Reson Imaging 10:6496541992Majors A Xue M Ng TC et al: Short echo time proton spectroscopy of human brain using a gradient head coil. Magn Reson Imaging 10:649–654 1992

    • Search Google Scholar
    • Export Citation
  • 35.

    Michaelis TMerboldt KDBruhn Het al: Absolute concentrations of metabolites in the adult human brain in vivo: quantification of localized proton MR spectra. Radiology 187:2192271993Michaelis T Merboldt KD Bruhn H et al: Absolute concentrations of metabolites in the adult human brain in vivo: quantification of localized proton MR spectra. Radiology 187:219–227 1993

    • Search Google Scholar
    • Export Citation
  • 36.

    Michaelis TMerboldt KDHänicke Wet al: On the identification of cerebral metabolites in localized 1H NMR spectra of human brain in vivo. NMR Biomed 4:90981991Michaelis T Merboldt KD Hänicke W et al: On the identification of cerebral metabolites in localized 1H NMR spectra of human brain in vivo. NMR Biomed 4:90–98 1991

    • Search Google Scholar
    • Export Citation
  • 37.

    Moonen CTWvon Keinlin Mvan Zijl PCMet al: Comparison of single-shot localization methods (STEAM and PRESS) for in vivo proton NMR spectroscopy. NMR Biomed 2:2012081989Moonen CTW von Keinlin M van Zijl PCM et al: Comparison of single-shot localization methods (STEAM and PRESS) for in vivo proton NMR spectroscopy. NMR Biomed 2:201–208 1989

    • Search Google Scholar
    • Export Citation
  • 38.

    Morantz RA: The management of the patient with low-grade cerebral astrocytomas in Morantz RAWalsh JW (eds): Brain Tumors. A Comprehensive Text. New York: Marcel-Dekker1994 pp 387415Morantz RA: The management of the patient with low-grade cerebral astrocytomas in Morantz RA Walsh JW (eds): Brain Tumors. A Comprehensive Text. New York: Marcel-Dekker 1994 pp 387–415

    • Search Google Scholar
    • Export Citation
  • 39.

    Negendank WSauter RBrown Tet al: Intratumoral lipids and lactate in 1H MRS in vivo in astrocytic tumors. Proc Soc Magn Reson Med 3:12961994 (Abstract)Negendank W Sauter R Brown T et al: Intratumoral lipids and lactate in 1H MRS in vivo in astrocytic tumors. Proc Soc Magn Reson Med 3:1296 1994 (Abstract)

    • Search Google Scholar
    • Export Citation
  • 40.

    Negendank WZimmerman RGotsis Eet al: A cooperative group study of 1H MRS of primary brain tumors. Proc Soc Magn Reson Med 3:15211993 (Abstract)Negendank W Zimmerman R Gotsis E et al: A cooperative group study of 1H MRS of primary brain tumors. Proc Soc Magn Reson Med 3:1521 1993 (Abstract)

    • Search Google Scholar
    • Export Citation
  • 41.

    Nelson JSTsukada YSchoenfeld Det al: Necrosis as a prognostic criterion in malignant supratentorial, astrocytic gliomas. Cancer 52:5505541983Nelson JS Tsukada Y Schoenfeld D et al: Necrosis as a prognostic criterion in malignant supratentorial astrocytic gliomas. Cancer 52:550–554 1983

    • Search Google Scholar
    • Export Citation
  • 42.

    Ordidge RJCresshull ID: The correction of transient Bo field shifts following the application of pulsed gradients by phase correction in the time domain. J Magn Reson 69:1511551986Ordidge RJ Cresshull ID: The correction of transient Bo field shifts following the application of pulsed gradients by phase correction in the time domain. J Magn Reson 69:151–155 1986

    • Search Google Scholar
    • Export Citation
  • 43.

    Ott DHennig JErnst T: Human brain tumors: assessment with in vivo proton MR spectroscopy. Radiology 186:7457521993Ott D Hennig J Ernst T: Human brain tumors: assessment with in vivo proton MR spectroscopy. Radiology 186:745–752 1993

    • Search Google Scholar
    • Export Citation
  • 44.

    Patronas NJDi Chiro GKufta Cet al: Prediction of survival in glioma patients by means of positron emission tomography. J Neurosurg 62:8168221985Patronas NJ Di Chiro G Kufta C et al: Prediction of survival in glioma patients by means of positron emission tomography. J Neurosurg 62:816–822 1985

    • Search Google Scholar
    • Export Citation
  • 45.

    Peeling JSutherland G: High-resolution 1H NMR spectroscopy studies of extracts of human cerebral neoplasms. Magn Reson Med 24:1231361992Peeling J Sutherland G: High-resolution 1H NMR spectroscopy studies of extracts of human cerebral neoplasms. Magn Reson Med 24:123–136 1992

    • Search Google Scholar
    • Export Citation
  • 46.

    Posse SSchuknecht BSmith MEet al: Short echo time proton MR spectroscopic imaging. J Comput Assist Tomogr 17:1141993Posse S Schuknecht B Smith ME et al: Short echo time proton MR spectroscopic imaging. J Comput Assist Tomogr 17:1–14 1993

    • Search Google Scholar
    • Export Citation
  • 47.

    Preul MCCaramanos ZCollins JGet al: Linear discriminant analysis based on proton MR spectroscopic imaging of human brain tumours improves pre-operative diagnosis. Proc Soc Magn Reson 2:1251994 (Abstract)Preul MC Caramanos Z Collins JG et al: Linear discriminant analysis based on proton MR spectroscopic imaging of human brain tumours improves pre-operative diagnosis. Proc Soc Magn Reson 2:125 1994 (Abstract)

    • Search Google Scholar
    • Export Citation
  • 48.

    Radlbauer RLangenberger KWMoser E: Qualitätskontrolle für die lokalisierte In-vivo-Protonenspektroskopie an klinischen MR-Geräten. Roto Fortschr Geb Rontgenstr Neuen Bildgeb Verfahr 160:2542591994Radlbauer R Langenberger KW Moser E: Qualitätskontrolle für die lokalisierte In-vivo-Protonenspektroskopie an klinischen MR-Geräten. Roto Fortschr Geb Rontgenstr Neuen Bildgeb Verfahr 160:254–259 1994

    • Search Google Scholar
    • Export Citation
  • 49.

    Remy CArús CZiegler Aet al: in vivo, ex vivo and in vitro one- and two-dimensional nuclear magnetic resonance spectroscopy of an intracerebral glioma in rat brain: assignment of resonances. J Neurochem 62:1661791994Remy C Arús C Ziegler A et al: in vivoex vivo and in vitro one- and two-dimensional nuclear magnetic resonance spectroscopy of an intracerebral glioma in rat brain: assignment of resonances. J Neurochem 62:166–179 1994

    • Search Google Scholar
    • Export Citation
  • 50.

    Russell DSRubinstein LJ: Pathology of Tumors of the Nervous Systemed 4. Baltimore: Williams & Wilkins1977Russell DS Rubinstein LJ: Pathology of Tumors of the Nervous System ed 4. Baltimore: Williams & Wilkins 1977

    • Search Google Scholar
    • Export Citation
  • 51.

    Rutter AHugenholtz HSaunders JKet al: Classification of brain tumors by ex vivo 1H NMR spectroscopy. J Neurochem 64:165516611995Rutter A Hugenholtz H Saunders JK et al: Classification of brain tumors by ex vivo 1H NMR spectroscopy. J Neurochem 64:1655–1661 1995

    • Search Google Scholar
    • Export Citation
  • 52.

    Salcman M (ed): Neurobiology of Brain Tumors. Baltimore: Williams & Wilkins Vol 41991Salcman M (ed): Neurobiology of Brain Tumors. Baltimore: Williams & Wilkins Vol 4 1991

    • Search Google Scholar
    • Export Citation
  • 53.

    Sauter R: Cerebral single volume proton spectroscopy on healthy volunteers. A multicenter pilot study. Proc Soc Magn Reson Med 12:15311993 (Abstract)Sauter R: Cerebral single volume proton spectroscopy on healthy volunteers. A multicenter pilot study. Proc Soc Magn Reson Med 12:1531 1993 (Abstract)

    • Search Google Scholar
    • Export Citation
  • 54.

    Scherer HJ: Cerebral astrocytomas and their derivatives. Am J Cancer 40:1591981940Scherer HJ: Cerebral astrocytomas and their derivatives. Am J Cancer 40:159–198 1940

    • Search Google Scholar
    • Export Citation
  • 55.

    Schick FNägele TKlose Uet al: Lactate quantification by means of PRESS spectroscopy—influence of refocusing pulses and timing scheme. Magn Reson Imaging 13:3093191995Schick F Nägele T Klose U et al: Lactate quantification by means of PRESS spectroscopy—influence of refocusing pulses and timing scheme. Magn Reson Imaging 13:309–319 1995

    • Search Google Scholar
    • Export Citation
  • 56.

    Schifter THoffman JMHanson MWet al: Serial FDG-PET studies in the prediction of survival in patients with primary brain tumors. J Comput Assist Tomogr 17:5095161993Schifter T Hoffman JM Hanson MW et al: Serial FDG-PET studies in the prediction of survival in patients with primary brain tumors. J Comput Assist Tomogr 17:509–516 1993

    • Search Google Scholar
    • Export Citation
  • 57.

    Segebarth CMBalériaux DFLuyten PRet al: Detection of metabolic heterogeneity of human intracranial tumors in vivo by 1H NMR spectroscopic imaging. Magn Reson Med 13:62761990Segebarth CM Balériaux DF Luyten PR et al: Detection of metabolic heterogeneity of human intracranial tumors in vivo by 1H NMR spectroscopic imaging. Magn Reson Med 13:62–76 1990

    • Search Google Scholar
    • Export Citation
  • 58.

    Sutton LNWang ZGusnard Det al: Proton magnetic resonance spectroscopy of pediatric brain tumors. Neurosurgery 31:1952021992Sutton LN Wang Z Gusnard D et al: Proton magnetic resonance spectroscopy of pediatric brain tumors. Neurosurgery 31:195–202 1992

    • Search Google Scholar
    • Export Citation
  • 59.

    Sutton LNWehrli SLGennarelli Let al: High-resolution 1Hmagnetic resonance spectroscopy of pediatric posterior fossa tumors in vitro. J Neurosurg 81:4434481994Sutton LN Wehrli SL Gennarelli L et al: High-resolution 1Hmagnetic resonance spectroscopy of pediatric posterior fossa tumors in vitro. J Neurosurg 81:443–448 1994

    • Search Google Scholar
    • Export Citation
  • 60.

    Tzika AAVigneron DBBall WS Jret al: Localized proton MR spectroscopy of the brain in children. J Magn Reson Imaging 3:7197291993Tzika AA Vigneron DB Ball WS Jr et al: Localized proton MR spectroscopy of the brain in children. J Magn Reson Imaging 3:719–729 1993

    • Search Google Scholar
    • Export Citation
  • 61.

    Usenius JPRKauppinen RAVainio PAet al: Quantitative metabolite patterns of human brain tumors: detection by 1H NMR spectroscopy in vivo and in vitro. J Comput Assist Tomogr 18:7057131994Usenius JPR Kauppinen RA Vainio PA et al: Quantitative metabolite patterns of human brain tumors: detection by 1H NMR spectroscopy in vivo and in vitro. J Comput Assist Tomogr 18:705–713 1994

    • Search Google Scholar
    • Export Citation
  • 62.

    Winger MJMacdonald DRCairncross JG: Supratentorial anaplastic gliomas in adults. The prognostic importance of extent of resection and prior low-grade glioma. J Neurosurg 71:4874931989Winger MJ Macdonald DR Cairncross JG: Supratentorial anaplastic gliomas in adults. The prognostic importance of extent of resection and prior low-grade glioma. J Neurosurg 71:487–493 1989

    • Search Google Scholar
    • Export Citation

TrendMD

Cited By

Metrics

Metrics

All Time Past Year Past 30 Days
Abstract Views 147 146 13
Full Text Views 130 130 0
PDF Downloads 90 90 0
EPUB Downloads 0 0 0

PubMed

Google Scholar