{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,2]],"date-time":"2026-07-02T07:43:12Z","timestamp":1782978192017,"version":"3.54.5"},"reference-count":120,"publisher":"Journal of Neurosurgery Publishing Group (JNSPG)","issue":"1","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["FOC"],"published-print":{"date-parts":[[2010,1]]},"abstract":"\n Object<\/jats:title>\n \n The goal in this study was to determine if proton (\n 1<\/jats:sup>\n H) MR spectroscopy can differentiate meningioma grade and is associated with interpretations of biological behavior; the study was performed using ex vivo high-resolution spectra indicating metabolic characteristics.\n <\/jats:p>\n <\/jats:sec>\n \n Methods<\/jats:title>\n \n Sixty-eight resected tissue samples of meningiomas were examined using ex vivo\n 1<\/jats:sup>\n H MR spectroscopy. Of these meningiomas, 46 were WHO Grade I, 14 were WHO Grade II, and 8 were WHO Grade III. Fifty-nine were primary meningiomas and 9 were recurrences. Invasion of adjacent tissue (dura mater, bone, venous sinus, brain) was found in 32 cases. Thirty-nine meningiomas did not rapidly recur (as defined by expansion on MR imaging within a 5-year follow-up period), whereas rapid recurrence was confirmed in 24 meningiomas, and follow-up status was unknown in 5 cases.\n <\/jats:p>\n <\/jats:sec>\n \n Results<\/jats:title>\n The absolute concentrations of total alanine and creatine were decreased in high-grade compared with low-grade meningiomas, as was the ratio of glycine to alanine (all p < 0.05). Additionally, alanine and the glycine\/alanine ratio distinguished between primary and recurrent meningiomas (all p < 0.05). Finally, the absolute concentrations of alanine and creatine, and the glycine\/alanine and choline\/glutamate ratios were associated with rapid recurrence (p < 0.05).<\/jats:p>\n <\/jats:sec>\n \n Conclusions<\/jats:title>\n . These data indicate that meningioma tissue can be characterized by metabolic parameters that are not typically identified by histopathological analysis alone. Creatine, glycine, and alanine may be used as markers of meningioma grade, recurrence, and the likelihood of rapid recurrence. These data validate a previous study of a separate group of Grade I meningiomas.<\/jats:p>\n <\/jats:sec>","DOI":"10.3171\/2009.11.focus09216","type":"journal-article","created":{"date-parts":[[2009,12,31]],"date-time":"2009-12-31T11:26:33Z","timestamp":1262258793000},"page":"E12","source":"Crossref","is-referenced-by-count":22,"title":["Using ex vivo proton magnetic resonance spectroscopy to reveal associations between biochemical and biological features of meningiomas"],"prefix":"10.3171","volume":"28","author":[{"given":"Wolfgang K.","family":"Pfisterer","sequence":"first","affiliation":[{"name":"Divisions of Neurological Surgery,"},{"name":"Neurosurgical Department, Donauspital im Sozialmedizinisches Zentrum-Ost, Vienna, Austria"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ronald A.","family":"Nieman","sequence":"additional","affiliation":[{"name":"Nuclear Magnetic Resonance Core Facility, Department of Chemistry and Biochemistry, Arizona State University, Tempe, Arizona; and"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Adrienne C.","family":"Scheck","sequence":"additional","affiliation":[{"name":"Neuro-oncology Research, and"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stephen W.","family":"Coons","sequence":"additional","affiliation":[{"name":"Neuropathology, Barrow Neurological Institute, St. Joseph's Hospital and Medical Center, Phoenix;"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Robert F.","family":"Spetzler","sequence":"additional","affiliation":[{"name":"Divisions of Neurological Surgery,"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mark C.","family":"Preul","sequence":"additional","affiliation":[{"name":"Divisions of Neurological Surgery,"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1754","reference":[{"key":"b1-0280012","series-title":"J Neurosurg","first-page":"51","article-title":"The recurrence of intracranial meningiomas after surgical treatment","volume":"58","author":"Adegbite","year":"1983"},{"key":"b2-0280012","series-title":"J Neurosurg","first-page":"210","article-title":"Malignant progression in meningioma: documentation of a series and analysis of cytogenetic findings","volume":"101","author":"Al-Mefty","year":"2004"},{"key":"b3-0280012","series-title":"Acta Neurochir (Wien)","first-page":"333","article-title":"Angiogenesis and brain oedema in intracranial meningiomas: influence of vascular endothelial growth factor","volume":"140","author":"Bitzer","year":"1998"},{"key":"b4-0280012","series-title":"J Neurosurg","first-page":"765","article-title":"Quantitative imaging of estrogen and progesterone receptors, estrogen-regulated protein, and growth fraction: immunocytochemical assays in 52 meningiomas. Correlation with clinical and morphological data","volume":"81","author":"Bouillot","year":"1994"},{"key":"b5-0280012","series-title":"J Neuropathol Exp Neurol","first-page":"628","article-title":"Chromosome 1p and 14q FISH analysis in clinicopathologic subsets of meningioma: diagnostic and prognostic implications","volume":"60","author":"Cai","year":"2001"},{"key":"b6-0280012","series-title":"J Neurooncol","first-page":"99","article-title":"Histopathological and cytogenetic findings in benign, atypical and anaplastic human meningiomas: a study of 60 tumors","volume":"47","author":"Cerd\u00e1-Nicol\u00e1s","year":"2000"},{"key":"b7-0280012","series-title":"Cancer Res","first-page":"1825","article-title":"Correlation of high-resolution magic angle spinning proton magnetic resonance spectroscopy with histopathology of intact human brain tumor specimens","volume":"58","author":"Cheng","year":"1998"},{"key":"b8-0280012","series-title":"Acta Neurochir Suppl","first-page":"17","article-title":"Malignancy of brain tumors evaluated by proton magnetic resonance spectroscopy (1H-MRS) in vitro","volume":"76","author":"Czernicki","year":"2000"},{"key":"b9-0280012","series-title":"Nat Med","first-page":"1287","article-title":"A new approach for analyzing proton magnetic resonance spectroscopic images of brain tumors: nosologic images","volume":"6","author":"De Edelenyi","year":"2000"},{"key":"b10-0280012","series-title":"Ann Neurol","first-page":"273","article-title":"In vivo differentiation of astrocytic brain tumors and isolated demyelinating lesions of the type seen in multiple sclerosis using 1H magnetic resonance spectroscopic imaging","volume":"44","author":"De Stefano","year":"1998"},{"key":"b11-0280012","series-title":"J Biol Chem","first-page":"23830","article-title":"Genomic expression discovery predicts pathways and opposing functions behind 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phenotypes?","volume":"359","author":"Griffin","year":"2004"},{"key":"b16-0280012","series-title":"Magn Reson Med","first-page":"223","article-title":"Metabolic profiles of human brain tumors using quantitative in vivo 1H magnetic resonance spectroscopy","volume":"49","author":"Howe","year":"2003"},{"key":"b17-0280012","series-title":"Cancer","first-page":"360","article-title":"Loss of material from chromosome arm 1p during malignant progression of meningioma revealed by fluorescent in situ hybridization","volume":"83","author":"Ishino","year":"1998"},{"key":"b18-0280012","series-title":"Neurosurgery","first-page":"567","article-title":"Long-term outcome and growth rate of subtotally resected petroclival meningiomas: experience with 38 cases","volume":"46","author":"Jung","year":"2000"},{"key":"b19-0280012","series-title":"Neurosurgery","first-page":"2","article-title":"Factors affecting operative and excess long-term mortality in 935 patients with intracranial meningioma","volume":"31","author":"Kallio","year":"1992"},{"key":"b20-0280012","series-title":"J Neurosurg","first-page":"601","article-title":"Predictive value of progression-associated chromosomal aberrations for the prognosis of meningiomas: a retrospective study of 198 cases","volume":"95","author":"Ketter","year":"2001"},{"key":"b21-0280012","series-title":"Neurol Med Chir (Tokyo)","first-page":"350","article-title":"Proton magnetic resonance spectroscopy of astrocytic tumors: an in vitro study","volume":"33","author":"Kinoshita","year":"1993"},{"key":"b22-0280012","series-title":"Neurosurgery","first-page":"606","article-title":"Proton magnetic resonance spectroscopy of brain tumors: an in vitro study","volume":"35","author":"Kinoshita","year":"1994"},{"key":"b23-0280012","series-title":"NMR Biomed","first-page":"2","article-title":"Absolute concentrations of metabolites in human brain tumors using in vitro proton magnetic resonance 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resonance spectroscopy ((1) H MRS) of human brain tumours: assessment of differences between tumour types and its applicability in brain tumour categorization","volume":"13","author":"Maj\u00f3s","year":"2003"},{"key":"b32-0280012","series-title":"NMR Biomed","first-page":"104","article-title":"Determination of proton metabolite concentrations and relaxation parameters in normal human brain and intracranial tumours","volume":"8","author":"Manton","year":"1995"},{"key":"b33-0280012","series-title":"Surg Neurol","first-page":"436","article-title":"Recurrence of meningiomas after operation","volume":"25","author":"Marks","year":"1986"},{"key":"b34-0280012","series-title":"Neurosurgery","first-page":"478","article-title":"Immunohistochemical detection of progesterone receptors and the correlation with Ki-67 labeling indices in paraffin-embedded sections of meningiomas","volume":"37","author":"Nagashima","year":"1995"},{"key":"b35-0280012","series-title":"Radiology","first-page":"745","article-title":"Human brain tumors: assessment with in vivo proton MR spectroscopy","volume":"186","author":"Ott","year":"1993"},{"key":"b36-0280012","series-title":"Magn Reson Med","first-page":"123","article-title":"High-resolution 1H NMR spectroscopy studies of extracts of human cerebral neoplasms","volume":"24","author":"Peeling","year":"1992"},{"key":"b37-0280012","series-title":"Cancer","first-page":"2046","article-title":"\u201cMalignancy\u201d in meningiomas: a clinicopathologic study of 116 patients, with grading implications","volume":"85","author":"Perry","year":"1999"},{"key":"b38-0280012","series-title":"Am J Surg Pathol","first-page":"1455","article-title":"Meningioma grading: an analysis of histologic parameters","volume":"21","author":"Perry","year":"1997"},{"key":"b39-0280012","series-title":"Cancer","first-page":"2262","article-title":"The prognostic significance of MIB-1, p53, and DNA flow cytometry in completely resected primary meningiomas","volume":"82","author":"Perry","year":"1998"},{"key":"b40-0280012","series-title":"J Neurooncol","first-page":"43","article-title":"Implicating chromosomal aberrations with meningioma growth and recurrence: results from FISH and MIB-I analysis of grades I and II meningioma tissue","volume":"87","author":"Pfisterer","year":"2008"},{"key":"b41-0280012","series-title":"Neuro-oncol","first-page":"290","article-title":"Diagnostic and prognostic significance of genetic regional heterogeneity in meningiomas","volume":"6","author":"Pfisterer","year":"2004"},{"key":"b42-0280012","series-title":"Neurosurgery","first-page":"1048","article-title":"Fluorescent in situ hybridization and ex vivo 1H magnetic resonance spectroscopic examinations of meningioma tumor tissue: is it possible to identify a clinically-aggressive subset of benign meningiomas?","volume":"61","author":"Pfisterer","year":"2007"},{"key":"b43-0280012","series-title":"J Cancer Res Clin Oncol","first-page":"343","article-title":"Diagnostic assessment of brain tumours and non-neoplastic brain disorders in vivo using proton nuclear magnetic resonance spectroscopy and artificial neural networks","volume":"125","author":"Poptani","year":"1999"},{"key":"b44-0280012","series-title":"Nat Med","first-page":"323","article-title":"Accurate, noninvasive diagnosis of human brain tumors by using proton magnetic resonance spectroscopy","volume":"2","author":"Preul","year":"1996"},{"key":"b45-0280012","series-title":"NMR Biomed","first-page":"192","article-title":"Using pattern analysis of in vivo proton MRSI data to improve the diagnosis and surgical management of patients with brain tumors","volume":"11","author":"Preul","year":"1998"},{"key":"b46-0280012","series-title":"Can J Neurol Sci","first-page":"13","article-title":"Magnetic resonance spectroscopy guided brain tumor resection: differentiation between recurrent glioma and radiation change in two diagnostically difficult cases","volume":"25","author":"Preul","year":"1998"},{"key":"b47-0280012","series-title":"Acta Neurochir (Wien)","first-page":"1231","article-title":"Suprasellar meningiomas\u2014neurological and visual outcome at long-term follow-up in a homogeneous series of patients treated microsurgically","volume":"140","author":"Puchner","year":"1998"},{"key":"b48-0280012","series-title":"Magn Reson Q","first-page":"191","article-title":"Clinical applications of magnetic resonance spectroscopy","volume":"10","author":"Ross","year":"1994"},{"key":"b49-0280012","series-title":"J Neurooncol","first-page":"63","article-title":"Prospective serial proton MR spectroscopic assessment of response to tamoxifen for recurrent malignant glioma","volume":"90","author":"Sankar","year":"2008"},{"key":"b50-0280012","series-title":"Can J Neurol Sci","first-page":"696","article-title":"The metabolic epicenter of supratentorial gliomas: a 1H-MRSI study","volume":"36","author":"Sankar","year":"2009"},{"key":"b51-0280012","series-title":"Acta Neurochir (Wien)","first-page":"493","article-title":"Biology of meningiomas","volume":"142","author":"Sanson","year":"2000"},{"key":"b52-0280012","series-title":"Cytometry","first-page":"153","article-title":"Incidence of numerical chromosome aberrations in meningioma tumors as revealed by fluorescence in situ hybridization using 10 chromosome-specific probes","volume":"50","author":"Sayagu\u00e9s","year":"2002"},{"key":"b53-0280012","series-title":"J Neurol Neurosurg Psychiatry","first-page":"22","article-title":"The recurrence of intracranial meningiomas after surgical treatment","volume":"20","author":"Simpson","year":"1957"},{"key":"b54-0280012","series-title":"Magn Reson Med","first-page":"29","article-title":"Automated classification of short echo time in in vivo 1H brain tumor spectra: a multicenter study","volume":"49","author":"Tate","year":"2003"},{"key":"b55-0280012","series-title":"J Comput Assist Tomogr","first-page":"705","article-title":"Quantitative metabolite patterns of human brain tumors: detection by 1H NMR spectroscopy in vivo and in vitro","volume":"18","author":"Usenius","year":"1994"},{"key":"b56-0280012","series-title":"Neuroreport","first-page":"1597","article-title":"Automated classification of human brain tumours by neural network analysis using in vivo 1H magnetic resonance spectroscopic metabolite phenotypes","volume":"7","author":"Usenius","year":"1996"},{"key":"b57-0280012","series-title":"J Neurochem","first-page":"1538","article-title":"Choline-containing compounds in human astrocytomas studied by 1H NMR spectroscopy in vivo and in vitro","volume":"63","author":"Usenius","year":"1994"},{"key":"b58-0280012","series-title":"Am J Pathol","first-page":"665","article-title":"Molecular characterization of human meningiomas by gene expression profiling using high-density oligonucleotide microarrays","volume":"161","author":"Watson","year":"2002"},{"key":"b59-0280012","series-title":"Teratog Carcinog Mutagen","first-page":"217","article-title":"Evaluation of relationship between chromosome 22 and p53 gene alterations and the subtype of meningiomas by the interphase-FISH technique","volume":"22","author":"Yakut","year":"2002"},{"key":"b60-0280012","series-title":"Cytogenet Cell Genet","first-page":"207","article-title":"Meningioma: a cytogenetic model of a complex benign human tumor, including data on 394 karyotyped cases","volume":"93","author":"Zang","year":"2001"},{"key":"b1-0280012","series-title":"J Neurosurg","first-page":"51","article-title":"The recurrence of intracranial meningiomas after surgical treatment","volume":"58","author":"Adegbite","year":"1983"},{"key":"b2-0280012","series-title":"J Neurosurg","first-page":"210","article-title":"Malignant progression in meningioma: documentation of a series and analysis of cytogenetic findings","volume":"101","author":"Al-Mefty","year":"2004"},{"key":"b3-0280012","series-title":"Acta Neurochir (Wien)","first-page":"333","article-title":"Angiogenesis and brain oedema in intracranial meningiomas: influence of vascular endothelial growth factor","volume":"140","author":"Bitzer","year":"1998"},{"key":"b4-0280012","series-title":"J Neurosurg","first-page":"765","article-title":"Quantitative imaging of estrogen and progesterone receptors, estrogen-regulated protein, and growth fraction: immunocytochemical assays in 52 meningiomas. 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phenotypes","volume":"278","author":"Fathallah-Shaykh","year":"2003"},{"key":"b12-0280012","series-title":"Stereotact Funct Neurosurg","first-page":"83","article-title":"In vivo proton magnetic resonance spectroscopy of brain tumors","volume":"74","author":"Fountas","year":"2000"},{"key":"b13-0280012","series-title":"Neurosurgery","first-page":"1269","article-title":"Brain edema in meningiomas is associated with increased vascular endothelial growth factor expression","volume":"40","author":"Goldman","year":"1997"},{"key":"b14-0280012","series-title":"Magn Reson Med","first-page":"1011","article-title":"Measurement of chemical shifts and coupling constants for glutamate and glutamine","volume":"39","author":"Govindaraju","year":"1998"},{"key":"b15-0280012","series-title":"Philos Trans R Soc Lond B Biol Sci","first-page":"857","article-title":"Metabolic profiles to define the genome: can we hear the 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meningioma","volume":"31","author":"Kallio","year":"1992"},{"key":"b20-0280012","series-title":"J Neurosurg","first-page":"601","article-title":"Predictive value of progression-associated chromosomal aberrations for the prognosis of meningiomas: a retrospective study of 198 cases","volume":"95","author":"Ketter","year":"2001"},{"key":"b21-0280012","series-title":"Neurol Med Chir (Tokyo)","first-page":"350","article-title":"Proton magnetic resonance spectroscopy of astrocytic tumors: an in vitro study","volume":"33","author":"Kinoshita","year":"1993"},{"key":"b22-0280012","series-title":"Neurosurgery","first-page":"606","article-title":"Proton magnetic resonance spectroscopy of brain tumors: an in vitro study","volume":"35","author":"Kinoshita","year":"1994"},{"key":"b23-0280012","series-title":"NMR Biomed","first-page":"2","article-title":"Absolute concentrations of metabolites in human brain tumors using in vitro proton magnetic resonance spectroscopy","volume":"10","author":"Kinoshita","year":"1997"},{"key":"b24-0280012","series-title":"Acta Neurochir (Wien)","first-page":"87","article-title":"Invasion of the cavernous sinus by medial sphenoid meningioma\u2014\u201cradical\u201d surgery and recurrence","volume":"103","author":"Kleinpeter","year":"1990"},{"key":"b25-0280012","series-title":"NMR Biomed","first-page":"149","article-title":"1H MRS of high grade astrocytomas: mobile lipid accumulation in necrotic tissue","volume":"7","author":"Kuesel","year":"1994"},{"key":"b26-0280012","series-title":"Curr Opin Neurol","first-page":"882","article-title":"Meningioma","volume":"6","author":"Kujas","year":"1993"},{"key":"b27-0280012","series-title":"NMR Biomed","first-page":"307","article-title":"1H- and (31)P-MR spectroscopy of primary and recurrent human brain tumors in vitro: malignancy-characteristic profiles of water soluble and lipophilic spectral components","volume":"14","author":"Lehnhardt","year":"2001"},{"key":"b28-0280012","series-title":"Cancer Genet Cytogenet","first-page":"119","article-title":"Loss of 1p in recurrent meningiomas: a comparative study in successive recurrences by cytogenetics and fluorescence in situ hybridization","volume":"125","author":"L\u00f3pez-Gin\u00e9s","year":"2001"},{"key":"b29-0280012","series-title":"Pathology and Genetics of Tumours of the Nervous System: World Health Organisation Classification of Tumours","first-page":"176","article-title":"Meningiomas","author":"Louis","year":"2000"},{"key":"b30-0280012","series-title":"Cancer","first-page":"377","article-title":"Gains of chromosome 22 by fluorescence in situ hybridization in the context of an hyperdiploid karyotype are associated with aggressive clinical features in meningioma patients","volume":"92","author":"Ma\u00edllo","year":"2001"},{"key":"b31-0280012","series-title":"Eur Radiol","first-page":"582","article-title":"Proton magnetic 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