Skip to main content
Erschienen in: European Radiology 2/2017

22.03.2016 | Magnetic Resonance

Grading diffuse gliomas without intense contrast enhancement by amide proton transfer MR imaging: comparisons with diffusion- and perfusion-weighted imaging

verfasst von: Osamu Togao, Akio Hiwatashi, Koji Yamashita, Kazufumi Kikuchi, Jochen Keupp, Koji Yoshimoto, Daisuke Kuga, Masami Yoneyama, Satoshi O. Suzuki, Toru Iwaki, Masaya Takahashi, Koji Iihara, Hiroshi Honda

Erschienen in: European Radiology | Ausgabe 2/2017

Einloggen, um Zugang zu erhalten

Abstract

Objectives

To investigate whether amide proton transfer (APT) MR imaging can differentiate high-grade gliomas (HGGs) from low-grade gliomas (LGGs) among gliomas without intense contrast enhancement (CE).

Methods

This retrospective study evaluated 34 patients (22 males, 12 females; age 36.0 ± 11.3 years) including 20 with LGGs and 14 with HGGs, all scanned on a 3T MR scanner. Only tumours without intense CE were included. Two neuroradiologists independently performed histogram analyses to measure the 90th-percentile (APT90) and mean (APTmean) of the tumours’ APT signals. The apparent diffusion coefficient (ADC) and relative cerebral blood volume (rCBV) were also measured. The parameters were compared between the groups with Student’s t-test. Diagnostic performance was evaluated with receiver operating characteristic (ROC) analysis.

Results

The APT90 (2.80 ± 0.59 % in LGGs, 3.72 ± 0.89 in HGGs, P = 0.001) and APTmean (1.87 ± 0.49 % in LGGs, 2.70 ± 0.58 in HGGs, P = 0.0001) were significantly larger in the HGGs compared to the LGGs. The ADC and rCBV values were not significantly different between the groups. Both the APT90 and APTmean showed medium diagnostic performance in this discrimination.

Conclusions

APT imaging is useful in discriminating HGGs from LGGs among diffuse gliomas without intense CE.

Key Points

Amide proton transfer (APT) imaging helps in grading non-enhancing gliomas
High-grade gliomas showed higher APT signal than low-grade gliomas
APT imaging showed better diagnostic performance than diffusion- and perfusion-weighted imaging
Literatur
1.
Zurück zum Zitat Daumas-Duport C, Scheithauer B, O'Fallon J, Kelly P (1988) Grading of astrocytomas. A simple and reproducible method. Cancer 62:2152–2165CrossRefPubMed Daumas-Duport C, Scheithauer B, O'Fallon J, Kelly P (1988) Grading of astrocytomas. A simple and reproducible method. Cancer 62:2152–2165CrossRefPubMed
2.
Zurück zum Zitat Law M, Yang S, Babb JS et al (2004) Comparison of cerebral blood volume and vascular permeability from dynamic susceptibility contrast-enhanced perfusion MR imaging with glioma grade. AJNR Am J Neuroradiol 25:746–755PubMed Law M, Yang S, Babb JS et al (2004) Comparison of cerebral blood volume and vascular permeability from dynamic susceptibility contrast-enhanced perfusion MR imaging with glioma grade. AJNR Am J Neuroradiol 25:746–755PubMed
3.
Zurück zum Zitat Hilario A, Sepulveda JM, Perez-Nunez A et al (2014) A prognostic model based on preoperative MRI predicts overall survival in patients with diffuse gliomas. AJNR Am J Neuroradiol 35:1096–1102CrossRefPubMed Hilario A, Sepulveda JM, Perez-Nunez A et al (2014) A prognostic model based on preoperative MRI predicts overall survival in patients with diffuse gliomas. AJNR Am J Neuroradiol 35:1096–1102CrossRefPubMed
4.
Zurück zum Zitat Pierallini A, Bonamini M, Bozzao A et al (1997) Supratentorial diffuse astrocytic tumours: proposal of an MRI classification. Eur Radiol 7:395–399CrossRefPubMed Pierallini A, Bonamini M, Bozzao A et al (1997) Supratentorial diffuse astrocytic tumours: proposal of an MRI classification. Eur Radiol 7:395–399CrossRefPubMed
5.
Zurück zum Zitat Mihara F, Numaguchi Y, Rothman M, Sato S, Fiandaca MS (1995) MR imaging of adult supratentorial astrocytomas: an attempt of semi-automatic grading. Radiat Med 13:5–9PubMed Mihara F, Numaguchi Y, Rothman M, Sato S, Fiandaca MS (1995) MR imaging of adult supratentorial astrocytomas: an attempt of semi-automatic grading. Radiat Med 13:5–9PubMed
6.
Zurück zum Zitat Fan GG, Deng QL, Wu ZH, Guo QY (2006) Usefulness of diffusion/perfusion-weighted MRI in patients with non-enhancing supratentorial brain gliomas: a valuable tool to predict tumour grading? Br J Radiol 79:652–658CrossRefPubMed Fan GG, Deng QL, Wu ZH, Guo QY (2006) Usefulness of diffusion/perfusion-weighted MRI in patients with non-enhancing supratentorial brain gliomas: a valuable tool to predict tumour grading? Br J Radiol 79:652–658CrossRefPubMed
7.
Zurück zum Zitat McKnight TR, Lamborn KR, Love TD et al (2007) Correlation of magnetic resonance spectroscopic and growth characteristics within Grades II and III gliomas. J Neurosurg 106:660–666CrossRefPubMed McKnight TR, Lamborn KR, Love TD et al (2007) Correlation of magnetic resonance spectroscopic and growth characteristics within Grades II and III gliomas. J Neurosurg 106:660–666CrossRefPubMed
8.
Zurück zum Zitat Lee EJ, Lee SK, Agid R, Bae JM, Keller A, Terbrugge K (2008) Preoperative grading of presumptive low-grade astrocytomas on MR imaging: diagnostic value of minimum apparent diffusion coefficient. AJNR Am J Neuroradiol 29:1872–1877CrossRefPubMed Lee EJ, Lee SK, Agid R, Bae JM, Keller A, Terbrugge K (2008) Preoperative grading of presumptive low-grade astrocytomas on MR imaging: diagnostic value of minimum apparent diffusion coefficient. AJNR Am J Neuroradiol 29:1872–1877CrossRefPubMed
9.
Zurück zum Zitat Falk A, Fahlstrom M, Rostrup E et al (2014) Discrimination between glioma grades II and III in suspected low-grade gliomas using dynamic contrast-enhanced and dynamic susceptibility contrast perfusion MR imaging: a histogram analysis approach. Neuroradiology 56:1031–1038CrossRefPubMed Falk A, Fahlstrom M, Rostrup E et al (2014) Discrimination between glioma grades II and III in suspected low-grade gliomas using dynamic contrast-enhanced and dynamic susceptibility contrast perfusion MR imaging: a histogram analysis approach. Neuroradiology 56:1031–1038CrossRefPubMed
10.
Zurück zum Zitat Zhou J, Payen JF, Wilson DA, Traystman RJ, van Zijl PC (2003) Using the amide proton signals of intracellular proteins and peptides to detect pH effects in MRI. Nat Med 9:1085–1090CrossRefPubMed Zhou J, Payen JF, Wilson DA, Traystman RJ, van Zijl PC (2003) Using the amide proton signals of intracellular proteins and peptides to detect pH effects in MRI. Nat Med 9:1085–1090CrossRefPubMed
11.
Zurück zum Zitat Zhou J, Lal B, Wilson DA, Laterra J, van Zijl PC (2003) Amide proton transfer (APT) contrast for imaging of brain tumors. Magn Reson Med 50:1120–1126CrossRefPubMed Zhou J, Lal B, Wilson DA, Laterra J, van Zijl PC (2003) Amide proton transfer (APT) contrast for imaging of brain tumors. Magn Reson Med 50:1120–1126CrossRefPubMed
12.
Zurück zum Zitat Zhou J, Blakeley JO, Hua J et al (2008) Practical data acquisition method for human brain tumor amide proton transfer (APT) imaging. Magn Reson Med 60:842–849CrossRefPubMedPubMedCentral Zhou J, Blakeley JO, Hua J et al (2008) Practical data acquisition method for human brain tumor amide proton transfer (APT) imaging. Magn Reson Med 60:842–849CrossRefPubMedPubMedCentral
13.
Zurück zum Zitat Togao O, Yoshiura T, Keupp J et al (2014) Amide proton transfer imaging of adult diffuse gliomas: correlation with histopathological grades. Neuro Oncol 16:441–448CrossRefPubMed Togao O, Yoshiura T, Keupp J et al (2014) Amide proton transfer imaging of adult diffuse gliomas: correlation with histopathological grades. Neuro Oncol 16:441–448CrossRefPubMed
14.
Zurück zum Zitat Sakata A, Okada T, Yamamoto A et al (2015) Grading glial tumors with amide proton transfer MR imaging: different analytical approaches. J Neurooncol 122:339–348CrossRefPubMed Sakata A, Okada T, Yamamoto A et al (2015) Grading glial tumors with amide proton transfer MR imaging: different analytical approaches. J Neurooncol 122:339–348CrossRefPubMed
15.
Zurück zum Zitat Keupp J, Baltes C, Harvey P, Van den Brink J (2011) Parallel RF transmission based MRI technique for highly sensitive detection of amide proton transfer in the human brain at 3T. Proc Int Soc Magn Reson Med 19:710 Keupp J, Baltes C, Harvey P, Van den Brink J (2011) Parallel RF transmission based MRI technique for highly sensitive detection of amide proton transfer in the human brain at 3T. Proc Int Soc Magn Reson Med 19:710
16.
Zurück zum Zitat Togao O, Hiwatashi A, Keupp J et al (2015) Scan-rescan reproducibility of parallel transmission based amide proton transfer imaging of brain tumors. J Magn Reson Imaging 42:1346–1353CrossRefPubMed Togao O, Hiwatashi A, Keupp J et al (2015) Scan-rescan reproducibility of parallel transmission based amide proton transfer imaging of brain tumors. J Magn Reson Imaging 42:1346–1353CrossRefPubMed
17.
Zurück zum Zitat Boxerman JL, Schmainda KM, Weisskoff RM (2006) Relative cerebral blood volume maps corrected for contrast agent extravasation significantly correlate with glioma tumor grade, whereas uncorrected maps do not. AJNR Am J Neuroradiol 27:859–867PubMed Boxerman JL, Schmainda KM, Weisskoff RM (2006) Relative cerebral blood volume maps corrected for contrast agent extravasation significantly correlate with glioma tumor grade, whereas uncorrected maps do not. AJNR Am J Neuroradiol 27:859–867PubMed
18.
Zurück zum Zitat Hu LS, Eschbacher JM, Heiserman JE et al (2012) Reevaluating the imaging definition of tumor progression: perfusion MRI quantifies recurrent glioblastoma tumor fraction, pseudoprogression, and radiation necrosis to predict survival. Neuro Oncol 14:919–930CrossRefPubMedPubMedCentral Hu LS, Eschbacher JM, Heiserman JE et al (2012) Reevaluating the imaging definition of tumor progression: perfusion MRI quantifies recurrent glioblastoma tumor fraction, pseudoprogression, and radiation necrosis to predict survival. Neuro Oncol 14:919–930CrossRefPubMedPubMedCentral
19.
Zurück zum Zitat Paulson ES, Schmainda KM (2008) Comparison of dynamic susceptibility-weighted contrast-enhanced MR methods: recommendations for measuring relative cerebral blood volume in brain tumors. Radiology 249:601–613CrossRefPubMedPubMedCentral Paulson ES, Schmainda KM (2008) Comparison of dynamic susceptibility-weighted contrast-enhanced MR methods: recommendations for measuring relative cerebral blood volume in brain tumors. Radiology 249:601–613CrossRefPubMedPubMedCentral
20.
Zurück zum Zitat Thevenaz P, Ruttimann UE, Unser M (1998) A pyramid approach to subpixel registration based on intensity. IEEE Trans Image Process 7:27–41CrossRefPubMed Thevenaz P, Ruttimann UE, Unser M (1998) A pyramid approach to subpixel registration based on intensity. IEEE Trans Image Process 7:27–41CrossRefPubMed
21.
Zurück zum Zitat Shrout PE, Fleiss JL (1979) Intraclass correlations: uses in assessing rater reliability. Psychol Bull 86:420–428CrossRefPubMed Shrout PE, Fleiss JL (1979) Intraclass correlations: uses in assessing rater reliability. Psychol Bull 86:420–428CrossRefPubMed
22.
Zurück zum Zitat Wen Z, Hu S, Huang F et al (2010) MR imaging of high-grade brain tumors using endogenous protein and peptide-based contrast. Neuroimage 51:616–622CrossRefPubMedPubMedCentral Wen Z, Hu S, Huang F et al (2010) MR imaging of high-grade brain tumors using endogenous protein and peptide-based contrast. Neuroimage 51:616–622CrossRefPubMedPubMedCentral
23.
Zurück zum Zitat Salhotra A, Lal B, Laterra J, Sun PZ, van Zijl PC, Zhou J (2008) Amide proton transfer imaging of 9L gliosarcoma and human glioblastoma xenografts. NMR Biomed 21:489–497CrossRefPubMedPubMedCentral Salhotra A, Lal B, Laterra J, Sun PZ, van Zijl PC, Zhou J (2008) Amide proton transfer imaging of 9L gliosarcoma and human glioblastoma xenografts. NMR Biomed 21:489–497CrossRefPubMedPubMedCentral
24.
Zurück zum Zitat Xu J, Zaiss M, Zu Z et al (2014) On the origins of chemical exchange saturation transfer (CEST) contrast in tumors at 9.4 T. NMR Biomed 27:406–416CrossRefPubMedPubMedCentral Xu J, Zaiss M, Zu Z et al (2014) On the origins of chemical exchange saturation transfer (CEST) contrast in tumors at 9.4 T. NMR Biomed 27:406–416CrossRefPubMedPubMedCentral
25.
Zurück zum Zitat Heo HY, Zhang Y, Lee DH, Hong X, Zhou J (2015) Quantitative assessment of amide proton transfer (APT) and nuclear overhauser enhancement (NOE) imaging with extrapolated semi-solid magnetization transfer reference (EMR) signals: application to a rat glioma model at 4.7 tesla. Magn Reson Med. doi:10.1002/mrm.25581 Heo HY, Zhang Y, Lee DH, Hong X, Zhou J (2015) Quantitative assessment of amide proton transfer (APT) and nuclear overhauser enhancement (NOE) imaging with extrapolated semi-solid magnetization transfer reference (EMR) signals: application to a rat glioma model at 4.7 tesla. Magn Reson Med. doi:10.​1002/​mrm.​25581
26.
Zurück zum Zitat Togao O, Yoshiura T, Keupp J et al (2012) Effect of saturation pulse length on parallel transmission based Amide Proton Transfer (APT) imaging of different brain tumor types. Proc Int Soc Magn Reson Med 21:744 Togao O, Yoshiura T, Keupp J et al (2012) Effect of saturation pulse length on parallel transmission based Amide Proton Transfer (APT) imaging of different brain tumor types. Proc Int Soc Magn Reson Med 21:744
Metadaten
Titel
Grading diffuse gliomas without intense contrast enhancement by amide proton transfer MR imaging: comparisons with diffusion- and perfusion-weighted imaging
verfasst von
Osamu Togao
Akio Hiwatashi
Koji Yamashita
Kazufumi Kikuchi
Jochen Keupp
Koji Yoshimoto
Daisuke Kuga
Masami Yoneyama
Satoshi O. Suzuki
Toru Iwaki
Masaya Takahashi
Koji Iihara
Hiroshi Honda
Publikationsdatum
22.03.2016
Verlag
Springer Berlin Heidelberg
Erschienen in
European Radiology / Ausgabe 2/2017
Print ISSN: 0938-7994
Elektronische ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-016-4328-0

Weitere Artikel der Ausgabe 2/2017

European Radiology 2/2017 Zur Ausgabe

Update Radiologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.