Top

Published in:

01-01-2018 | Clinical Study

Myo-inositol concentration in MR spectroscopy for differentiating high grade glioma from primary central nervous system lymphoma

Authors: Hiroaki Nagashima, Takashi Sasayama, Kazuhiro Tanaka, Katsusuke Kyotani, Naoko Sato, Masahiro Maeyama, Masaaki Kohta, Junichi Sakata, Yusuke Yamamoto, Kohkichi Hosoda, Tomoo Itoh, Ryohei Sasaki, Eiji Kohmura

Published in: Journal of Neuro-Oncology | Issue 2/2018

Abstract

It is sometimes difficult to distinguish gliomas from other tumors on routine imaging. In this study, we assessed whether 3-T magnetic resonance spectroscopy (MRS) with LCModel software might be useful for discriminating glioma from other brain tumors, such as primary central nervous system lymphomas (PCNSLs) and metastatic tumors. A total of 104 cases of brain tumor (66 gliomas, 20 PCNSLs, 6 metastatic tumors, 12 other tumors) were preoperatively investigated with short echo time (35 ms) single-voxel 3-T MRS. LCModel software was used to evaluate differences in the absolute concentrations of choline, N-acetylaspartate, N-acetylaspartylglutamate, glutamate + glutamine, myo-inositol (mIns), and lipid. mIns levels were significantly increased in high-grade glioma (HGG) compared with PCNSL (p < 0.001). In multivariate logistic regression analysis, mIns was the best marker for differentiating HGG from PCNSL (p < 0.0001, odds ratio 1.9927, 95% confidence interval 1.3628–3.2637). Conventional MRS detection of mIns resulted in a high diagnostic accuracy (sensitivity, 64%; specificity, 90%; area under the receiver operator curve, 0.80) for HGG. The expression of inositol 3-phosphate synthase (ISYNA1) was significantly higher in gliomas than in PCNSLs (p < 0.05), suggesting that the increased level of mIns in glioma is due to high expression of ISYNA1, the rate-limiting enzyme in the mIns-producing pathway. In conclusion, noninvasive analysis of mIns using single-voxel MRS may be useful in distinguishing gliomas from other brain tumors, particularly PCNSLs.

Available only for authorised users

Stupp R, Pavlidis N, Jelic S (2005) ESMO minimum clinical recommendations for diagnosis, treatment and follow-up of malignant glioma. Ann Oncol 16 Suppl 1: i64–i65. https://doi.org/10.1093/annonc/mdi834 CrossRefPubMed

Stupp R (2007) Malignant glioma: ESMO clinical recommendations for diagnosis, treatment and follow-up. Ann Oncol 18(Suppl 2): ii69–ii70. https://doi.org/10.1093/annonc/mdm044 PubMed

Morris PG, Abrey LE (2009) Therapeutic challenges in primary CNS lymphoma. Lancet Neurol 8:581–592. https://doi.org/10.1016/s1474-4422(09)70091-2 CrossRefPubMed

Arrieta O, Saavedra-Perez D, Kuri R, Aviles-Salas A, Martinez L, Mendoza-Posada D, Castillo P, Astorga A, Guzman E, De la Garza J (2009) Brain metastasis development and poor survival associated with carcinoembryonic antigen (CEA) level in advanced non-small cell lung cancer: a prospective analysis. BMC Cancer 9:119. https://doi.org/10.1186/1471-2407-9-119 CrossRefPubMedPubMedCentral

Christensen TD, Spindler KL, Palshof JA, Nielsen DL (2016) Systematic review: brain metastases from colorectal cancer—incidence and patient characteristics. BMC Cancer 16:260. https://doi.org/10.1186/s12885-016-2290-5 CrossRefPubMedPubMedCentral

Haldorsen IS, Krossnes BK, Aarseth JH, Scheie D, Johannesen TB, Mella O, Espeland A (2007) Increasing incidence and continued dismal outcome of primary central nervous system lymphoma in Norway 1989–2003 : time trends in a 15-year national survey. Cancer 110:1803–1814. https://doi.org/10.1002/cncr.22989 CrossRefPubMed

Guo AC, MacFall JR, Provenzale JM (2002) Multiple sclerosis: diffusion tensor MR imaging for evaluation of normal-appearing white matter. Radiology 222:729–736. https://doi.org/10.1148/radiol.2223010311 CrossRefPubMed

Weber MA, Zoubaa S, Schlieter M, Juttler E, Huttner HB, Geletneky K, Ittrich C, Lichy MP, Kroll A, Debus J, Giesel FL, Hartmann M, Essig M (2006) Diagnostic performance of spectroscopic and perfusion MRI for distinction of brain tumors. Neurology 66:1899–1906. https://doi.org/10.1212/01.wnl.0000219767.49705.9c CrossRefPubMed

Yamasaki F, Kurisu K, Satoh K, Arita K, Sugiyama K, Ohtaki M, Takaba J, Tominaga A, Hanaya R, Yoshioka H, Hama S, Ito Y, Kajiwara Y, Yahara K, Saito T, Thohar MA (2005) Apparent diffusion coefficient of human brain tumors at MR imaging. Radiology 235:985–991. https://doi.org/10.1148/radiol.2353031338 CrossRefPubMed

10.

Le Bihan D, Breton E, Lallemand D, Grenier P, Cabanis E, Laval-Jeantet M (1986) MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 161:401–407. https://doi.org/10.1148/radiology.161.2.3763909 CrossRefPubMed

11.

Yamashita K, Hiwatashi A, Togao O, Kikuchi K, Kitamura Y, Mizoguchi M, Yoshimoto K, Kuga D, Suzuki SO, Baba S, Isoda T, Iwaki T, Iihara K, Honda H (2016) Diagnostic utility of intravoxel incoherent motion mr imaging in differentiating primary central nervous system lymphoma from glioblastoma multiforme. J Magn Reson Imaging 44:1256–1261. https://doi.org/10.1002/jmri.25261 CrossRefPubMed

12.

Jiang S, Yu H, Wang X, Lu S, Li Y, Feng L, Zhang Y, Heo HY, Lee DH, Zhou J, Wen Z (2016) Molecular MRI differentiation between primary central nervous system lymphomas and high-grade gliomas using endogenous protein-based amide proton transfer MR imaging at 3 T. Eur Radiol 26:64–71. https://doi.org/10.1007/s00330-015-3805-1 CrossRefPubMed

13.

Aburano H, Ueda F, Yoshie Y, Matsui O, Nakada M, Hayashi Y, Gabata T (2015) Differences between glioblastomas and primary central nervous system lymphomas in 1H-magnetic resonance spectroscopy. Jpn J Radiol 33:392–403. https://doi.org/10.1007/s11604-015-0430-5 CrossRefPubMed

14.

Yamasaki F, Takayasu T, Nosaka R, Amatya VJ, Doskaliyev A, Akiyama Y, Tominaga A, Takeshima Y, Sugiyama K, Kurisu K (2015) Magnetic resonance spectroscopy detection of high lipid levels in intraaxial tumors without central necrosis: a characteristic of malignant lymphoma. J Neurosurg 122:1370–1379. https://doi.org/10.3171/2014.9.jns14106 CrossRefPubMed

15.

Provencher SW (2001) Automatic quantitation of localized in vivo 1H spectra with LCModel. NMR Biomed 14:260–264CrossRefPubMed

16.

Nagashima H, Tanaka K, Sasayama T, Irino Y, Sato N, Takeuchi Y, Kyotani K, Mukasa A, Mizukawa K, Sakata J, Yamamoto Y, Hosoda K, Itoh T, Sasaki R, Kohmura E (2016) Diagnostic value of glutamate with 2-hydroxyglutarate in magnetic resonance spectroscopy for IDH1 mutant glioma. Neuro-oncology 18:1559–1568. https://doi.org/10.1093/neuonc/now090 PubMedPubMedCentral

17.

Graveron-Demilly D (2014) Quantification in magnetic resonance spectroscopy based on semi-parametric approaches. MAGMA 27:113–130CrossRefPubMed

18.

Tanaka K, Sasayama T, Mizukawa K, Takata K, Sulaiman NS, Nishihara M, Kohta M, Sasaki R, Hirose T, Itoh T, Kohmura E (2015) Combined IDH1 mutation and MGMT methylation status on long-term survival of patients with cerebral low-grade glioma. Clin Neurol Neurosurg 138:37–44. https://doi.org/10.1016/j.clineuro.2015.07.019 CrossRefPubMed

19.

Tanaka K, Sasayama T, Irino Y, Takata K, Nagashima H, Satoh N, Kyotani K, Mizowaki T, Imahori T, Ejima Y, Masui K, Gini B, Yang H, Hosoda K, Sasaki R, Mischel PS, Kohmura E (2015) Compensatory glutamine metabolism promotes glioblastoma resistance to mTOR inhibitor treatment. J Clin Invest 125:1591–1602. https://doi.org/10.1172/jci78239 CrossRefPubMedPubMedCentral

20.

Berridge MJ, Lipp P, Bootman MD (2000) Signal transduction. The calcium entry pas de deux. Science 287:1604–1605CrossRefPubMed

21.

Saiardi A, Bhandari R, Resnick AC, Snowman AM, Snyder SH (2004) Phosphorylation of proteins by inositol pyrophosphates. Science 306:2101–2105. https://doi.org/10.1126/science.1103344 CrossRefPubMed

22.

Shen X, Xiao H, Ranallo R, Wu WH, Wu C (2003) Modulation of ATP-dependent chromatin-remodeling complexes by inositol polyphosphates. Science 299:112–114. https://doi.org/10.1126/science.1078068 CrossRefPubMed

23.

York JD, Odom AR, Murphy R, Ives EB, Wente SR (1999) A phospholipase C-dependent inositol polyphosphate kinase pathway required for efficient messenger RNA export. Science 285:96–100CrossRefPubMed

24.

Haris M, Cai K, Singh A, Hariharan H, Reddy R (2011) In vivo mapping of brain myo-inositol. Neuroimage 54:2079–2085. https://doi.org/10.1016/j.neuroimage.2010.10.017 CrossRefPubMed

25.

Castillo M, Smith JK, Kwock L (2000) Correlation of myo-inositol levels and grading of cerebral astrocytomas. AJNR 21:1645–1649PubMed

26.

Hattingen E, Raab P, Franz K, Zanella FE, Lanfermann H, Pilatus U (2008) Myo-inositol: a marker of reactive astrogliosis in glial tumors? NMR Biomed 21:233–241. https://doi.org/10.1002/nbm.1186 CrossRefPubMed

27.

Koguchi T, Tanikawa C, Mori J, Kojima Y, Matsuda K (2016) Regulation of myo-inositol biosynthesis by p53-ISYNA1 pathway. Int J Oncol 48:2415–2424. https://doi.org/10.3892/ijo.2016.3456 CrossRefPubMed

28.

Seelan RS, Lakshmanan J, Casanova MF, Parthasarathy RN (2009) Identification of myo-inositol-3-phosphate synthase isoforms: characterization, expression, and putative role of a 16-kDa gamma(c) isoform. J Biol Chem 284:9443–9457. https://doi.org/10.1074/jbc.M900206200 CrossRefPubMedPubMedCentral

29.

Wei L, Hong S, Yoon Y, Hwang SN, Park JC, Zhang Z, Olson JJ, Hu XP, Shim H (2012) Early prediction of response to Vorinostat in an orthotopic rat glioma model. NMR Biomed 25:1104–1111. https://doi.org/10.1002/nbm.2776 CrossRefPubMedPubMedCentral

30.

Eisenberg F Jr, Parthasarathy R (1987) Measurement of biosynthesis of myo-inositol from glucose 6-phosphate. Methods Enzymol 141:127–143CrossRefPubMed

31.

Mora P, Majos C, Castaner S, Sanchez JJ, Gabarros A, Muntane A, Aguilera C, Arus C (2014) (1)H-MRS is useful to reinforce the suspicion of primary central nervous system lymphoma prior to surgery. Eur Radiol 24:2895–2905. https://doi.org/10.1007/s00330-014-3308-5 CrossRefPubMed

32.

Kimura T, Sako K, Gotoh T, Tanaka K, Tanaka T (2001) In vivo single-voxel proton MR spectroscopy in brain lesions with ring-like enhancement. NMR Biomed 14:339–349CrossRefPubMed

33.

Opstad KS, Ladroue C, Bell BA, Griffiths JR, Howe FA (2007) Linear discriminant analysis of brain tumour (1)H MR spectra: a comparison of classification using whole spectra versus metabolite quantification. NMR Biomed 20:763–770. https://doi.org/10.1002/nbm.1147 CrossRefPubMed

34.

Choi C, Ganji SK, DeBerardinis RJ, Dimitrov IE, Pascual JM, Bachoo R, Mickey BE, Malloy CR, Maher EA (2011) Measurement of glycine in the human brain in vivo by 1H-MRS at 3T: application in brain tumors. Magn Reson Med 66:609–618. https://doi.org/10.1002/mrm.22857 CrossRefPubMedPubMedCentral

Title: Myo-inositol concentration in MR spectroscopy for differentiating high grade glioma from primary central nervous system lymphoma
Authors: Hiroaki Nagashima
Takashi Sasayama
Kazuhiro Tanaka
Katsusuke Kyotani
Naoko Sato
Masahiro Maeyama
Masaaki Kohta
Junichi Sakata
Yusuke Yamamoto
Kohkichi Hosoda
Tomoo Itoh
Ryohei Sasaki
Eiji Kohmura
Publication date: 01-01-2018
Publisher: Springer US
Published in: Journal of Neuro-Oncology / Issue 2/2018
Print ISSN: 0167-594X
Electronic ISSN: 1573-7373
DOI: https://doi.org/10.1007/s11060-017-2655-x

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Myo-inositol concentration in MR spectroscopy for differentiating high grade glioma from primary central nervous system lymphoma

Abstract

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 2/2018

Impact of WHO 2016 update of brain tumor classification, molecular markers and clinical outcomes in pleomorphic xanthoastrocytoma

Addition of chemotherapy to hypofractionated radiotherapy for glioblastoma: practice patterns, outcomes, and predictors of survival

Glioblastoma and acute myeloid leukemia: malignancies with striking similarities

Pittsburgh compound B (PiB) PET imaging of meningioma and other intracranial tumors

An immune-related lncRNA signature for patients with anaplastic gliomas

Local control and overall survival for adjuvant stereotactic radiosurgery in patients with residual or recurrent disease