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The Metabolic Epicenter of Supratentorial Gliomas: A 1H-MRSI Study

Published online by Cambridge University Press:  02 December 2014

Tejas Sankar
Affiliation:
Neurosurgery Research Laboratory, Division of Neurological Surgery, Barrow Neurological Institute, St. Joseph's Hospital and Medical Center, Phoenix, Arizona, USA
Yevgeniy E. Kuznetsov
Affiliation:
MR Spectroscopy Unit, McConnell Brain Imaging Centre, Departments of Neurology and Neurosurgery, McGill University, Montreal Neurological Institute, Montreal, Quebec, Canada
Robert W. Ryan
Affiliation:
Neurosurgery Research Laboratory, Division of Neurological Surgery, Barrow Neurological Institute, St. Joseph's Hospital and Medical Center, Phoenix, Arizona, USA
Zografos Caramanos
Affiliation:
MR Spectroscopy Unit, McConnell Brain Imaging Centre, Departments of Neurology and Neurosurgery, McGill University, Montreal Neurological Institute, Montreal, Quebec, Canada
Samson B. Antel
Affiliation:
MR Spectroscopy Unit, McConnell Brain Imaging Centre, Departments of Neurology and Neurosurgery, McGill University, Montreal Neurological Institute, Montreal, Quebec, Canada
Douglas L. Arnold
Affiliation:
MR Spectroscopy Unit, McConnell Brain Imaging Centre, Departments of Neurology and Neurosurgery, McGill University, Montreal Neurological Institute, Montreal, Quebec, Canada
Mark C. Preul*
Affiliation:
Neurosurgery Research Laboratory, Division of Neurological Surgery, Barrow Neurological Institute, St. Joseph's Hospital and Medical Center, Phoenix, Arizona, USA
*
Division of Neurological Surgery, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, 350 W. Thomas Road, Phoenix, Arizona, 85013, USA. Email: neuropub@chw.edu.
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Abstract

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Background:

Assessing the impact of glioma location on prognosis remains elusive. We approached the problem using multivoxel proton magnetic resonance spectroscopic imaging (1H-MRSI) to define a tumor “metabolic epicenter”, and examined the relationship of metabolic epicenter location to survival and histopathological grade.

Methods:

We studied 54 consecutive patients with a supratentorial glioma (astrocytoma or oligodendroglioma, WHO grades II-IV). The metabolic epicenter in each tumor was defined as the 1H-MRSI voxel containing maximum intra-tumoral choline on preoperative imaging. Tumor location was considered the X-Y-Z coordinate position, in a standardized stereotactic space, of the metabolic epicenter. Correlation between epicenter location and survival or grade was assessed.

Results:

Metabolic epicenter location correlated significantly with patient survival for all tumors (r2 = 0.30, p = 0.0002) and astrocytomas alone (r2 = 0.32, p = 0.005). A predictive model based on both metabolic epicenter location and histopathological grade accounted for 70% of the variability in survival, substantially improving on histology alone to predict survival. Location also correlated significantly with grade (r2 = 0.25, p = 0.001): higher grade tumors had a metabolic epicenter closer to the midpoint of the brain.

Conclusions:

The concept of the metabolic epicenter eliminates several problems related to existing methods of classifying glioma location. The location of the metabolic epicenter is strongly correlated with overall survival and histopathological grade, suggesting that it reflects biological factors underlying glioma growth and malignant dedifferentiation. These findings may be clinically relevant to predicting patterns of local glioma recurrence, and in planning resective surgery or radiotherapy.

Type
Other
Copyright
Copyright © The Canadian Journal of Neurological 2009

References

1.Apuzzo, MLJ.Commentary: epidemiology and data analysis. In: Apuzzo, MLJ, editor. Malignant cerebral glioma. Park Ridge, Ill: American Association of Neurological Surgeons; 1990. p. 111.Google Scholar
2.Ahlbom, A, Rodvall, Y.Brain tumour trends. Lancet. 1989;334: 12723.Google Scholar
3.Salcman, M.Epidemiology and factors affecting survival. In: Apuzzo, MLJ, editor. Malignant cerebral glioma. Park Ridge, Ill: 9; 1990. p. 95109.Google Scholar
4.Cohadon, F, Aouad, N, Rougier, A, Vital, C, Rivel, J, Dartigues, JF.Histologic and non-histologic factors correlated with survival time in supratentorial astrocytic tumors. J Neurooncol. 1985;3: 10511.Google Scholar
5.Curran, WJ Jr, Scott, CB, Horton, J, Nelson, JS, Weinstein, AS, Fischbach, AJ, et al.Recursive partitioning analysis of prognostic factors in three Radiation Therapy Oncology Group malignant glioma trials. J Natl Cancer Inst. 1993;85:70410.Google Scholar
6.Miller, PJ, Hassanein, RS, Giri, PG, Kimler, BF, O’Boynick, P, Evans, RG.Univariate and multivariate statistical analysis of high-grade gliomas: the relationship of radiation dose and other prognostic factors. Int J Radiat Oncol Biol Phys. 1990;19:27580.CrossRefGoogle Scholar
7.Kim, TS, Halliday, AL, Hedley-Whyte, ET, Convery, K.Correlates of survival and the Daumas-Duport grading system for astrocytomas. J Neurosurg. 1991;74:2737.Google Scholar
8.Chang, CH, Horton, J, Schoenfeld, D, Salazer, O, Perez-Tamayo, R, Kramer, S, et al.Comparison of postoperative radiotherapy and combined postoperative radiotherapy and chemotherapy in the multidisciplinary management of malignant gliomas. A joint Radiation Therapy Oncology Group and Eastern Cooperative Oncology Group study. Cancer. 1983;52:9971007.Google Scholar
9.Green, SB, Byar, DP, Walker, MD, Pistenmaa, DA, Alexander, E Jr, Batzdorf, U, et al.Comparisons of carmustine, procarbazine, and high-dose methylprednisolone as additions to surgery and radiotherapy for the treatment of malignant glioma. Cancer Treat Rep. 1983;67:12132.Google Scholar
10.Kinsella, TJ, Collins, J, Rowland, J, Klecker, Jr R, Wright, D, Katz, D, et al.Pharmacology and phase I/II study of continuous intravenous infusions of iododeoxyuridine and hyperfractionated radiotherapy in patients with glioblastoma multiforme. J Clin Oncol. 1988;6:8719.Google Scholar
11.Coffey, RJ, Lunsford, LD, Taylor, FH.Survival after stereotactic biopsy of malignant gliomas. Neurosurgery. 1988;22:46573.Google Scholar
12.Nelson, DF, Nelson, JS, Davis, DR, Chang, CH, Griffin, TW, Pajak, TF.Survival and prognosis of patients with astrocytoma with atypical or anaplastic features. J Neurooncol. 1985;3:99103.Google Scholar
13.Jeremic, B, Milicic, B, Grujicic, D, Dagovic, A, Aleksandrovic, J, Nikolic, N.Clinical prognostic factors in patients with malignant glioma treated with combined modality approach. Am J Clin Oncol. 2004;27:195204.Google Scholar
14.Mikkelsen, T, Enam, SA, Rosenblum, ML.Invasion in malignant glioma. In: Winn, HR, Youmans, JR, editors. Youmans Neurological Surgery. Philadelphia: Saunders; 2004. p. 75770.Google Scholar
15.Preul, MC, Caramanos, Z, Collins, DL, Villemure, JG, Leblanc, R, Olivier, A, et al.Accurate, noninvasive diagnosis of human brain tumors by using proton magnetic resonance spectroscopy. Nat Med. 1996;2:3235.Google Scholar
16.Preul, MC, Caramanos, Z, Leblanc, R, Villemure, JG, Arnold, DL.Using pattern analysis of in vivo proton MRSI data to improve the diagnosis and surgical management of patients with brain tumors. NMR Biomed. 1998;11: 192200.Google Scholar
17.McBride, DQ, Miller, BL, Nikas, DL, Buchthal, S, Chang, L, Chiang, F, et al.Analysis of brain tumors using 1H magnetic resonance spectroscopy. Surg Neurol. 1995;44: 13744.CrossRefGoogle ScholarPubMed
18.Meyerand, ME, Pipas, JM, Mamourian, A, Tosteson, TD, Dunn, JF.Classification of biopsy-confirmed brain tumors using single-voxel MR spectroscopy. AJNR Am J Neuroradiol. 1999;20: 11723.Google Scholar
19.Castillo, M, Kwock, L, Scatliff, J, Mukherji, SK.Proton MR spectroscopy in neoplastic and non-neoplastic brain disorders. Magn Reson Imaging Clin N Am. 1998;6: 120.Google Scholar
20.Alger, JR, Frank, JA, Bizzi, A, Fulham, MJ, DeSouza, BX, Duhaney, MO, et al.Metabolism of human gliomas: assessment with H-1 MR spectroscopy and F-18 fluorodeoxyglucose PET. Radiology. 1990;177: 63341.Google Scholar
21.Fulham, MJ, Bizzi, A, Dietz, MJ, Shih, HH, Raman, R, Sobering, GS, et al.Mapping of brain tumor metabolites with proton MR spectroscopic imaging: clinical relevance. Radiology. 1992;185: 67586.Google Scholar
22.Fountas, KN, Kapsalaki, EZ, Gotsis, SD, Kapsalakis, JZ, Smisson, HF III, Johnston, KW, et al.In vivo proton magnetic resonance spectroscopy of brain tumors. Stereotact Funct Neurosurg. 2000;74: 8394.Google Scholar
23.Tamiya, T, Kinoshita, K, Ono, Y, Matsumoto, K, Furuta, T, Ohmoto, T.Proton magnetic resonance spectroscopy reflects cellular proliferative activity in astrocytomas. Neuroradiol. 2000;42: 3338.CrossRefGoogle ScholarPubMed
24.Wilken, B, Dechent, P, Herms, J, Maxton, C, Markakis, E, Hanefeld, F, et al.Quantitative proton magnetic resonance spectroscopy of focal brain lesions. Pediatr Neurol. 2000;23: 2231.Google Scholar
25.Shimizu, H, Kumabe, T, Tominaga, T, Kayama, T, Hara, K, Ono, Y, et al.Noninvasive evaluation of malignancy of brain tumors with proton MR spectroscopy. AJNR Am J Neuroradiol. 1996;17: 73747.Google ScholarPubMed
26.Dowling, C, Bollen, AW, Noworolski, SM, McDermott, MW, Barbaro, NM, Day, MR, et al.Preoperative proton MR spectroscopic imaging of brain tumors: correlation with histopathologic analysis of resection specimens. AJNR. 2001;22: 60412.Google Scholar
27.Tedeschi, G, Lundbom, N, Raman, R, Bonavita, S, Duyn, JH, Alger, JR, et al.Increased choline signal coinciding with malignant degeneration of cerebral gliomas: a serial proton magnetic resonance spectroscopy imaging study. J Neurosurg. 1997;87: 51624.Google Scholar
28.McKnight, TR, Lamborn, KR, Love, TD, Berger, MS, Chang, S, Dillon, WP, et al.Correlation of magnetic resonance spectroscopic and growth characteristics within Grades II and III gliomas. J Neurosurg. 2007;106: 6606.CrossRefGoogle ScholarPubMed
29.Matsumura, A, Isobe, T, Anno, I, Takano, S, Kawamura, H.Correlation between choline and MIB-1 index in human gliomas. A quantitative proton MR spectroscopy study. J Clin Neurosci. 2005;12: 41620.CrossRefGoogle ScholarPubMed
30.Kwan, RK, Evans, AC, Pike, GB.MRI simulation-based evaluation of image-processing and classification methods. IEEE Trans Med Imaging. 1999;18: 108597.Google Scholar
31.Jeremic, B, Grujicic, D, Antunovic, V, Djuric, L, Stojanovic, M, Shibamoto, Y.Hyperfractionated radiation therapy (HFX RT) followed by multiagent chemotherapy (CHT) in patients with malignant glioma: a phase II study. Int J Radiat Oncol Biol Phys. 1994;30: 117985.CrossRefGoogle ScholarPubMed
32.Jeremic, B, Grujicic, D, Antunovic, V, Djuric, L, Shibamoto, Y.Accelerated hyperfractionated radiation therapy for malignant glioma. A phase II study. Am J Clin Oncol. 1995;18: 44953.Google Scholar
33.Jeremic, B, Shibamoto, Y, Grujicic, D, Milicic, B, Stojanovic, M, Nikolic, N, et al.Pre-irradiation carboplatin and etoposide and accelerated hyperfractionated radiation therapy in patients with high-grade astrocytomas: a phase II study. Radiother Oncol. 1999;51: 2733.Google Scholar
34.Jeremic, B, Shibamoto, Y, Grujicic, D, Stojanovic, M, Milicic, B, Nikolic, N, et al.Concurrent accelerated hyperfractionated radiation therapy and carboplatin/etoposide in patients with malignant glioma: long-term results of a phase II study. J Neurooncol. 2001;51: 13341.Google Scholar
35.Simpson, JR, Horton, J, Scott, C, Curran, WJ, Rubin, P, Fischbach, J, et al.Influence of location and extent of surgical resection on survival of patients with glioblastoma multiforme: results of three consecutive Radiation Therapy Oncology Group (RTOG) clinical trials. Int J Radiat Oncol Biol Phys. 1993;26:23944.CrossRefGoogle ScholarPubMed
36.Curran, WJ Jr, Scott, CB, Horton, J, Nelson, JS, Weinstein, AS, Nelson, DF.Does extent of surgery influence outcome for astrocytoma with atypical or anaplastic foci (AAF)? A report from three Radiation Therapy Oncology Group (RTOG) trials. J Neurooncol. 1992;12: 21927.CrossRefGoogle ScholarPubMed
37.Gehan, EA, Walker, MD.Prognostic factors for patients with brain tumors. Natl Cancer Inst Monogr. 1977;46: 18995.Google ScholarPubMed
38.Phuphanich, S, Ferrall, S, Greenberg, H.Long-term survival in malignant glioma. Prognostic factors. J Fla Med Assoc. 1993;80: 1814.Google Scholar
39.Kowalczuk, A, Macdonald, RL, Amidei, C, Dohrmann, G III, Erickson, RK, Hekmatpanah, J, et al.Quantitative imaging study of extent of surgical resection and prognosis of malignant astrocytomas. Neurosurgery. 1997;41: 102836.CrossRefGoogle ScholarPubMed
40.Jelsma, R, Bucy, PC.Glioblastoma multiforme: its treatment and some factors affecting survival. Arch Neurol. 1969;20: 16171.Google Scholar
41.Jelsma, R, Bucy, PC.The treatment of glioblastoma multiforme of the brain. J Neurosurg. 1967;27: 388400.Google Scholar
42.Winger, MJ, Macdonald, DR, Cairncross, JG.Supratentorial anaplastic gliomas in adults. The prognostic importance of extent of resection and prior low-grade glioma. J Neurosurg. 1989;71: 48793.Google Scholar
43.Devaux, BC, O’Fallon, JR, Kelly, PJ.Resection, biopsy, and survival in malignant glial neoplasms. A retrospective study of clinical parameters, therapy, and outcome. J Neurosurg. 1993;78: 76775.Google Scholar
44.Shinoda, J, Sakai, N, Murase, S, Yano, H, Matsuhisa, T, Funakoshi, T.Selection of eligible patients with supratentorial glioblastoma multiforme for gross total resection. J Neurooncol. 2001;52: 16171.CrossRefGoogle ScholarPubMed
45.Larjavaara, S, Mantyla, R, Salminen, T, Haapasalo, H, Raitanen, J, Jaaskelainen, J, et al.Incidence of gliomas by anatomic location. Neuro Oncol. 2007;9: 31925.Google Scholar
46.Duffau, H, Capelle, L.Preferential brain locations of low-grade gliomas: comparison with glioblastomas and review of hypothesis. Cancer. 2004;100: 26226.CrossRefGoogle Scholar
47.Walker, MD, Green, SB, Byar, DP, Alexander, E Jr, Batzdorf, U, Brooks, WH, et al.Randomized comparisons of radiotherapy and nitrosoureas for the treatment of malignant glioma after surgery. N Engl J Med. 1980;303: 13239.Google Scholar
48.Sanai, N, Berger, MS.Glioma extent of resection and its impact on patient outcome. Neurosurgery. 2008;62: 75366.Google Scholar
49.Scherer, HJ.Structural development in gliomas. Am J Cancer. 1938;34: 33351.Google Scholar
50.Matsukado, Y, MacCarty, CS, Kernohan, JW.The growth of glioblastoma multiforme (astrocytomas, grades 3 and 4) in neurosurgical practice. J Neurosurg. 1961;18: 63644.Google Scholar
51.Rosenblum, ML, Eisenberg, AD, Norman, D.Brain tumor invasion: clinical patterns of malignant astrocytoma spread [abstract]. J Neurosurg. 1992;76: 383A.Google Scholar
52.Enam, SA, Eisenberg, AD, Norman, D, Rosenblum, ML.Patterns of spread and recurrence of glioma: studies by neuroimaging. In: Mikkelsen, T, Bjerkvig, R, Laerum, OD, Rosenblum, ML, editors. Brain tumor invasion: biological, clinical, and therapeutic considerations. New York: Wiley-Liss; 1998. p. 13359.Google Scholar
53.Salazar, OM, Rubin, P.The spread of glioblastoma multiforme as a determining factor in the radiation treated volume. Int J Radiat Oncol Biol Phys. 1976;1: 62737.Google Scholar
54.Piepmeier, JM.Observations on the current treatment of low-grade astrocytic tumors of the cerebral hemispheres. J Neurosurg. 1987;67: 17781.Google Scholar
55.McCormack, BM, Miller, DC, Budzilovich, GN, Voorhees, GJ, Ransohoff, J.Treatment and survival of low-grade astrocytoma in adults—1977-1988. Neurosurgery. 1992;31: 63642.Google Scholar
56.Laws, ER Jr, Taylor, WF, Clifton, MB, Okazaki, H.Neurosurgical management of low-grade astrocytoma of the cerebral hemispheres. J Neurosurg. 1984;61: 66573.Google Scholar
57.Muller, W, Afra, D, Schroder, R.Supratentorial recurrences of gliomas. Morphological studies in relation to time intervals with astrocytomas. Acta Neurochir (Wien). 1977;37: 7591.Google Scholar
58.North, CA, North, RB, Epstein, JA, Piantadosi, S, Wharam, MD.Lowgrade cerebral astrocytomas. Survival and quality of life after radiation therapy. Cancer. 1990;66: 614.Google Scholar
59.Soffietti, R, Chio, A, Giordana, MT, Vasario, E, Schiffer, D.Prognostic factors in well-differentiated cerebral astrocytomas in the adult. Neurosurgery. 1989;24: 68692.CrossRefGoogle ScholarPubMed
60.Vertosick, FT Jr, Selker, RG, Arena, VC.Survival of patients with well-differentiated astrocytomas diagnosed in the era of computed tomography. Neurosurgery. 1991;28: 496501.Google Scholar
61.Lim, DA, Cha, S, Mayo, MC, Chen, M-H, Keles, E, VandenBerg, S, et al.Relationship of glioblastoma multiforme to neural stem cell regions predicts invasive and multifocal tumor phenotype. Neurooncol. 2007;9: 4249.Google Scholar