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Erschienen in: European Radiology 1/2016

01.01.2016 | Molecular Imaging

Molecular MRI differentiation between primary central nervous system lymphomas and high-grade gliomas using endogenous protein-based amide proton transfer MR imaging at 3 Tesla

verfasst von: Shanshan Jiang, Hao Yu, Xianlong Wang, Shilong Lu, Yufa Li, Lyujin Feng, Yi Zhang, Hye-Young Heo, Dong-Hoon Lee, Jinyuan Zhou, Zhibo Wen

Erschienen in: European Radiology | Ausgabe 1/2016

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Abstract

Objectives

To show the ability of using the amide proton transfer-weighted (APTW) MRI signals as imaging biomarkers to differentiate primary central nervous system lymphomas (PCNSLs) from high-grade gliomas (HGGs).

Methods

Eleven patients with lymphomas and 21 patients with HGGs were examined. Magnetization-transfer (MT) spectra over an offset range of ±6 ppm and the conventional MT ratio (MTR) at 15.6 ppm were acquired. The APTW signals, total chemical-exchange-saturation-transfer signal (integral between 0 and 5 ppm, CESTtotal), and MTR signal were obtained and compared between PCNSLs and HGGs. The diagnostic performance was assessed with the receiver operating characteristic (ROC) curve analysis.

Results

The PCNSLs usually showed more homogeneous APTW hyperintensity (spatially compared to normal brain tissue) than the HGGs. The APTWmax, APTWmax-min and CESTtotal signal intensities were significantly lower (P < 0.05, 0.001 and 0.05, respectively), while the APTWmin and MTR were significantly higher (both P < 0.01) in PCNSL lesions than in HGG lesions. The APTW values in peritumoral oedema were significantly lower for PCNSLs than for HGGs (P < 0.01). APTWmax-min had the highest area under the ROC curve (0.963) and accuracy (94.1 %) in differentiating PCNSLs from HGGs.

Conclusions

The protein-based APTW signal would be a valuable MRI biomarker by which to identify PCNSLs and HGGs presurgically.

Key Points

PCNSLs overall showed more homogeneous APTW hyperintensity than HGGs.
Maximum APTW signals were lower in PCNSL lesions than in HGG lesions.
MTR signals were higher in PCNSLs than in HGGs.
APTW heterogeneity had the highest accuracy in differentiating PCNSLs from HGGs.
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Literatur
1.
Zurück zum Zitat Corn BW, Marcus SM, Topham A, Hauck W, Curran WJ Jr (1997) Will primary central nervous system lymphoma be the most frequent brain tumor diagnosed in the year 2000? Cancer 79:2409–2413CrossRefPubMed Corn BW, Marcus SM, Topham A, Hauck W, Curran WJ Jr (1997) Will primary central nervous system lymphoma be the most frequent brain tumor diagnosed in the year 2000? Cancer 79:2409–2413CrossRefPubMed
2.
Zurück zum Zitat DeAngelis LM, Seiferheld W, Schold SC, Fisher B, Schultz CJ (2002) Combination chemotherapy and radiotherapy for primary central nervous system lymphoma: Radiation Therapy Oncology Group study 93-10. J Clin Oncol 20:4643–4648CrossRefPubMed DeAngelis LM, Seiferheld W, Schold SC, Fisher B, Schultz CJ (2002) Combination chemotherapy and radiotherapy for primary central nervous system lymphoma: Radiation Therapy Oncology Group study 93-10. J Clin Oncol 20:4643–4648CrossRefPubMed
3.
Zurück zum Zitat Wen PY, Macdonald DR, Reardon DA et al (2010) Updated response assessment criteria for high-grade gliomas: response assessment in neuro-oncology working group. J Clin Oncol 28:1963–1972CrossRefPubMed Wen PY, Macdonald DR, Reardon DA et al (2010) Updated response assessment criteria for high-grade gliomas: response assessment in neuro-oncology working group. J Clin Oncol 28:1963–1972CrossRefPubMed
4.
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-Oncology 14:919–930PubMedCentralCrossRefPubMed 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-Oncology 14:919–930PubMedCentralCrossRefPubMed
5.
Zurück zum Zitat Go JL, Lee SC, Kim PE (2006) Imaging of primary central nervous system lymphoma. Neurosurg Focus 21, E4CrossRefPubMed Go JL, Lee SC, Kim PE (2006) Imaging of primary central nervous system lymphoma. Neurosurg Focus 21, E4CrossRefPubMed
6.
Zurück zum Zitat Lolli V, Tampieri D, Melancon D, Delpilar Cortes M (2010) Imaging in primary central nervous system lymphoma. Neuroradiol J 23:680–689CrossRefPubMed Lolli V, Tampieri D, Melancon D, Delpilar Cortes M (2010) Imaging in primary central nervous system lymphoma. Neuroradiol J 23:680–689CrossRefPubMed
7.
Zurück zum Zitat Tang YZ, Booth TC, Bhogal P, Malhotra A, Wilhelm T (2011) Imaging of primary central nervous system lymphoma. Clin Radiol 66:768–777CrossRefPubMed Tang YZ, Booth TC, Bhogal P, Malhotra A, Wilhelm T (2011) Imaging of primary central nervous system lymphoma. Clin Radiol 66:768–777CrossRefPubMed
8.
Zurück zum Zitat Wang S, Kim S, Chawla S et al (2011) Differentiation between glioblastomas, solitary brain metastases, and primary cerebral lymphomas using diffusion tensor and dynamic susceptibility contrast-enhanced MR imaging. AJNR Am J Neuroradiol 32:507–514CrossRefPubMed Wang S, Kim S, Chawla S et al (2011) Differentiation between glioblastomas, solitary brain metastases, and primary cerebral lymphomas using diffusion tensor and dynamic susceptibility contrast-enhanced MR imaging. AJNR Am J Neuroradiol 32:507–514CrossRefPubMed
9.
Zurück zum Zitat Doskaliyev A, Yamasaki F, Ohtaki M et al (2012) Lymphomas and glioblastomas: differences in the apparent diffusion coefficient evaluated with high b-value diffusion-weighted magnetic resonance imaging at 3 T. Eur J Radiol 81:339–344CrossRefPubMed Doskaliyev A, Yamasaki F, Ohtaki M et al (2012) Lymphomas and glioblastomas: differences in the apparent diffusion coefficient evaluated with high b-value diffusion-weighted magnetic resonance imaging at 3 T. Eur J Radiol 81:339–344CrossRefPubMed
10.
Zurück zum Zitat Suh CH, Kim HS, Lee SS et al (2014) Atypical imaging features of primary central nervous system lymphoma that mimics glioblastoma: utility of intravoxel incoherent motion MR imaging. Radiology 272:504–513CrossRefPubMed Suh CH, Kim HS, Lee SS et al (2014) Atypical imaging features of primary central nervous system lymphoma that mimics glioblastoma: utility of intravoxel incoherent motion MR imaging. Radiology 272:504–513CrossRefPubMed
11.
Zurück zum Zitat Yamashita K, Yoshiura T, Hiwatashi A et al (2013) Differentiating primary CNS lymphoma from glioblastoma multiforme: assessment using arterial spin labeling, diffusion-weighted imaging, and (1)(8)F-fluorodeoxyglucose positron emission tomography. Neuroradiology 55:135–143CrossRefPubMed Yamashita K, Yoshiura T, Hiwatashi A et al (2013) Differentiating primary CNS lymphoma from glioblastoma multiforme: assessment using arterial spin labeling, diffusion-weighted imaging, and (1)(8)F-fluorodeoxyglucose positron emission tomography. Neuroradiology 55:135–143CrossRefPubMed
12.
Zurück zum Zitat Kickingereder P, Wiestler B, Sahm F et al (2014) Primary central nervous system lymphoma and atypical glioblastoma: multiparametric differentiation by using diffusion-, perfusion-, and susceptibility-weighted MR imaging. Radiology 272:843–850CrossRefPubMed Kickingereder P, Wiestler B, Sahm F et al (2014) Primary central nervous system lymphoma and atypical glioblastoma: multiparametric differentiation by using diffusion-, perfusion-, and susceptibility-weighted MR imaging. Radiology 272:843–850CrossRefPubMed
13.
Zurück zum Zitat Toh CH, Wei KC, Chang CN, Ng SH, Wong HF (2013) Differentiation of primary central nervous system lymphomas and glioblastomas: comparisons of diagnostic performance of dynamic susceptibility contrast-enhanced perfusion MR imaging without and with contrast-leakage correction. AJNR Am J Neuroradiol 34:1145–1149CrossRefPubMed Toh CH, Wei KC, Chang CN, Ng SH, Wong HF (2013) Differentiation of primary central nervous system lymphomas and glioblastomas: comparisons of diagnostic performance of dynamic susceptibility contrast-enhanced perfusion MR imaging without and with contrast-leakage correction. AJNR Am J Neuroradiol 34:1145–1149CrossRefPubMed
14.
Zurück zum Zitat Peters S, Knoss N, Wodarg F, Cnyrim C, Jansen O (2012) Glioblastomas vs. lymphomas: more diagnostic certainty by using susceptibility-weighted imaging (SWI). Röfo 184:713–718PubMed Peters S, Knoss N, Wodarg F, Cnyrim C, Jansen O (2012) Glioblastomas vs. lymphomas: more diagnostic certainty by using susceptibility-weighted imaging (SWI). Röfo 184:713–718PubMed
15.
Zurück zum Zitat Furtner J, Schopf V, Preusser M et al (2014) Non-invasive assessment of intratumoral vascularity using arterial spin labeling: a comparison to susceptibility-weighted imaging for the differentiation of primary cerebral lymphoma and glioblastoma. Eur J Radiol 83:806–810CrossRefPubMed Furtner J, Schopf V, Preusser M et al (2014) Non-invasive assessment of intratumoral vascularity using arterial spin labeling: a comparison to susceptibility-weighted imaging for the differentiation of primary cerebral lymphoma and glioblastoma. Eur J Radiol 83:806–810CrossRefPubMed
16.
Zurück zum Zitat Zhou J, Payen J, Wilson DA, Traystman RJ, van Zijl PCM (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 J, Wilson DA, Traystman RJ, van Zijl PCM (2003) Using the amide proton signals of intracellular proteins and peptides to detect pH effects in MRI. Nat Med 9:1085–1090CrossRefPubMed
17.
Zurück zum Zitat Zhou J, Lal B, Wilson DA, Laterra J, van Zijl PCM (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 PCM (2003) Amide proton transfer (APT) contrast for imaging of brain tumors. Magn Reson Med 50:1120–1126CrossRefPubMed
18.
Zurück zum Zitat Ward KM, Aletras AH, Balaban RS (2000) A new class of contrast agents for MRI based on proton chemical exchange dependent saturation transfer (CEST). J Magn Reson 143:79–87CrossRefPubMed Ward KM, Aletras AH, Balaban RS (2000) A new class of contrast agents for MRI based on proton chemical exchange dependent saturation transfer (CEST). J Magn Reson 143:79–87CrossRefPubMed
19.
Zurück zum Zitat Zhou J, van Zijl PC (2006) Chemical exchange saturation transfer imaging and spectroscopy. Progr NMR Spectrosc 48:109–136CrossRef Zhou J, van Zijl PC (2006) Chemical exchange saturation transfer imaging and spectroscopy. Progr NMR Spectrosc 48:109–136CrossRef
20.
Zurück zum Zitat Zaiss M, Bachert P (2013) Chemical exchange saturation transfer (CEST) and MR Z-spectroscopy in vivo: a review of theoretical approaches and methods. Phys Med Biol 58:R221–R269CrossRefPubMed Zaiss M, Bachert P (2013) Chemical exchange saturation transfer (CEST) and MR Z-spectroscopy in vivo: a review of theoretical approaches and methods. Phys Med Biol 58:R221–R269CrossRefPubMed
21.
Zurück zum Zitat Henkelman RM, Stanisz GJ, Graham SJ (2001) Magnetization transfer in MRI: a review. NMR Biomed 14:57–64CrossRefPubMed Henkelman RM, Stanisz GJ, Graham SJ (2001) Magnetization transfer in MRI: a review. NMR Biomed 14:57–64CrossRefPubMed
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 51:616–622PubMedCentralCrossRefPubMed Wen Z, Hu S, Huang F et al (2010) MR imaging of high-grade brain tumors using endogenous protein and peptide-based contrast. Neuroimage 51:616–622PubMedCentralCrossRefPubMed
23.
Zurück zum Zitat Zhou J, Tryggestad E, Wen Z et al (2011) Differentiation between glioma and radiation necrosis using molecular magnetic resonance imaging of endogenous proteins and peptides. Nat Med 17:130–134PubMedCentralCrossRefPubMed Zhou J, Tryggestad E, Wen Z et al (2011) Differentiation between glioma and radiation necrosis using molecular magnetic resonance imaging of endogenous proteins and peptides. Nat Med 17:130–134PubMedCentralCrossRefPubMed
24.
Zurück zum Zitat Zhou J, Zhu H, Lim M et al (2013) Three-dimensional amide proton transfer MR imaging of gliomas: initial experience and comparison with gadolinium enhancement. J Magn Reson Imaging 38:1119–1128CrossRefPubMed Zhou J, Zhu H, Lim M et al (2013) Three-dimensional amide proton transfer MR imaging of gliomas: initial experience and comparison with gadolinium enhancement. J Magn Reson Imaging 38:1119–1128CrossRefPubMed
25.
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 16:441–448PubMedCentralCrossRefPubMed Togao O, Yoshiura T, Keupp J et al (2014) Amide proton transfer imaging of adult diffuse gliomas: correlation with histopathological grades. Neuro Oncol 16:441–448PubMedCentralCrossRefPubMed
26.
Zurück zum Zitat Hong X, Liu L, Wang M et al (2014) Quantitative multiparametric MRI assessment of glioma response to radiotherapy in a rat model. Neuro Oncol 16:856–867PubMedCentralCrossRefPubMed Hong X, Liu L, Wang M et al (2014) Quantitative multiparametric MRI assessment of glioma response to radiotherapy in a rat model. Neuro Oncol 16:856–867PubMedCentralCrossRefPubMed
27.
Zurück zum Zitat Sagiyama K, Mashimo T, Togao O et al (2014) In vivo chemical exchange saturation transfer imaging allows early detection of a therapeutic response in glioblastoma. Proc Natl Acad Sci U S A 111:4542–4547PubMedCentralCrossRefPubMed Sagiyama K, Mashimo T, Togao O et al (2014) In vivo chemical exchange saturation transfer imaging allows early detection of a therapeutic response in glioblastoma. Proc Natl Acad Sci U S A 111:4542–4547PubMedCentralCrossRefPubMed
28.
Zurück zum Zitat Jia G, Abaza R, Williams JD et al (2011) Amide proton transfer MR imaging of prostate cancer: a preliminary study. J Magn Reson Imaging 33:647–654PubMedCentralCrossRefPubMed Jia G, Abaza R, Williams JD et al (2011) Amide proton transfer MR imaging of prostate cancer: a preliminary study. J Magn Reson Imaging 33:647–654PubMedCentralCrossRefPubMed
29.
Zurück zum Zitat Klomp DW, Dula AN, Arlinghaus LR et al (2013) Amide proton transfer imaging of the human breast at 7 T: development and reproducibility. NMR Biomed 26:1271–1277PubMedCentralCrossRefPubMed Klomp DW, Dula AN, Arlinghaus LR et al (2013) Amide proton transfer imaging of the human breast at 7 T: development and reproducibility. NMR Biomed 26:1271–1277PubMedCentralCrossRefPubMed
30.
Zurück zum Zitat Dula AN, Arlinghaus LR, Dortch RD et al (2013) Amide proton transfer imaging of the breast at 3 T: establishing reproducibility and possible feasibility assessing chemotherapy response. Magn Reson Med 70:216–224PubMedCentralCrossRefPubMed Dula AN, Arlinghaus LR, Dortch RD et al (2013) Amide proton transfer imaging of the breast at 3 T: establishing reproducibility and possible feasibility assessing chemotherapy response. Magn Reson Med 70:216–224PubMedCentralCrossRefPubMed
31.
Zurück zum Zitat Yuan J, Chen S, King AD et al (2014) Amide proton transfer-weighted imaging of the head and neck at 3 T: a feasibility study on healthy human subjects and patients with head and neck cancer. NMR Biomed 27:1239–1247PubMedCentralCrossRefPubMed Yuan J, Chen S, King AD et al (2014) Amide proton transfer-weighted imaging of the head and neck at 3 T: a feasibility study on healthy human subjects and patients with head and neck cancer. NMR Biomed 27:1239–1247PubMedCentralCrossRefPubMed
32.
Zurück zum Zitat Zhao X, Wen Z, Huang F et al (2011) Saturation power dependence of amide proton transfer image contrasts in human brain tumors and strokes at 3 T. Magn Reson Med 66:1033–1041PubMedCentralCrossRefPubMed Zhao X, Wen Z, Huang F et al (2011) Saturation power dependence of amide proton transfer image contrasts in human brain tumors and strokes at 3 T. Magn Reson Med 66:1033–1041PubMedCentralCrossRefPubMed
33.
Zurück zum Zitat Tietze A, Blicher J, Mikkelsen IK et al (2014) Assessment of ischemic penumbra in patients with hyperacute stroke using amide proton transfer (APT) chemical exchange saturation transfer (CEST) MRI. NMR Biomed 27:163–174PubMedCentralCrossRefPubMed Tietze A, Blicher J, Mikkelsen IK et al (2014) Assessment of ischemic penumbra in patients with hyperacute stroke using amide proton transfer (APT) chemical exchange saturation transfer (CEST) MRI. NMR Biomed 27:163–174PubMedCentralCrossRefPubMed
34.
Zurück zum Zitat Tee YK, Harston GW, Blockley N et al (2014) Comparing different analysis methods for quantifying the MRI amide proton transfer (APT) effect in hyperacute stroke patients. NMR Biomed 27:1019–1029CrossRefPubMed Tee YK, Harston GW, Blockley N et al (2014) Comparing different analysis methods for quantifying the MRI amide proton transfer (APT) effect in hyperacute stroke patients. NMR Biomed 27:1019–1029CrossRefPubMed
35.
36.
Zurück zum Zitat Franconi F, Roux J, Garric X, Lemaire L (2014) Early postsurgical visualization of composite mesh used in ventral hernia repair by amide proton transfer MRI. Magn Reson Med 71:313–317CrossRefPubMed Franconi F, Roux J, Garric X, Lemaire L (2014) Early postsurgical visualization of composite mesh used in ventral hernia repair by amide proton transfer MRI. Magn Reson Med 71:313–317CrossRefPubMed
37.
Zurück zum Zitat Kalakunja A, Hardwicke F (2003) Non-Hodgkin's lymphoma occurring as pure central nervous system pathology. Clin Adv Hematol Oncol 1:554–555PubMed Kalakunja A, Hardwicke F (2003) Non-Hodgkin's lymphoma occurring as pure central nervous system pathology. Clin Adv Hematol Oncol 1:554–555PubMed
38.
Zurück zum Zitat Commins DL (2006) Pathology of primary central nervous system lymphoma. Neurosurg Focus 21, E2CrossRefPubMed Commins DL (2006) Pathology of primary central nervous system lymphoma. Neurosurg Focus 21, E2CrossRefPubMed
39.
Zurück zum Zitat Rubenstein J, Ferreri AJ, Pittaluga S (2008) Primary lymphoma of the central nervous system: epidemiology, pathology and current approaches to diagnosis, prognosis and treatment. Leuk Lymphoma 49:S43–S51CrossRef Rubenstein J, Ferreri AJ, Pittaluga S (2008) Primary lymphoma of the central nervous system: epidemiology, pathology and current approaches to diagnosis, prognosis and treatment. Leuk Lymphoma 49:S43–S51CrossRef
40.
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 60:842–849PubMedCentralCrossRefPubMed 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 60:842–849PubMedCentralCrossRefPubMed
41.
Zurück zum Zitat Murakami R, Hirai T, Sugahara T et al (2009) Grading astrocytic tumors by using apparent diffusion coefficient parameters: superiority of a one- versus two-parameter pilot method. Radiology 251:838–845CrossRefPubMed Murakami R, Hirai T, Sugahara T et al (2009) Grading astrocytic tumors by using apparent diffusion coefficient parameters: superiority of a one- versus two-parameter pilot method. Radiology 251:838–845CrossRefPubMed
42.
Zurück zum Zitat Zhou J, Yan K, Zhu H (2012) A simple model for understanding the origin of the amide proton transfer MRI signal in tissue. Appl Magn Reson 42:393–402PubMedCentralCrossRefPubMed Zhou J, Yan K, Zhu H (2012) A simple model for understanding the origin of the amide proton transfer MRI signal in tissue. Appl Magn Reson 42:393–402PubMedCentralCrossRefPubMed
43.
Zurück zum Zitat Imai H, Shimada K, Shimada S et al (2009) Comparative clinicopathological study of primary CNS diffuse large B-cell lymphoma and intravascular large B-cell lymphoma. Pathol Int 59:431–437CrossRefPubMed Imai H, Shimada K, Shimada S et al (2009) Comparative clinicopathological study of primary CNS diffuse large B-cell lymphoma and intravascular large B-cell lymphoma. Pathol Int 59:431–437CrossRefPubMed
44.
Zurück zum Zitat Preusser M, Woehrer A, Koperek O et al (2010) Primary central nervous system lymphoma: a clinicopathological study of 75 cases. Pathology 42:547–552CrossRefPubMed Preusser M, Woehrer A, Koperek O et al (2010) Primary central nervous system lymphoma: a clinicopathological study of 75 cases. Pathology 42:547–552CrossRefPubMed
45.
Zurück zum Zitat Scott JN, Brasher PM, Sevick RJ, Rewcastle NB, Forsyth PA (2002) How often are nonenhancing supratentorial gliomas malignant? A population study. Neurology 59:947–949CrossRefPubMed Scott JN, Brasher PM, Sevick RJ, Rewcastle NB, Forsyth PA (2002) How often are nonenhancing supratentorial gliomas malignant? A population study. Neurology 59:947–949CrossRefPubMed
Metadaten
Titel
Molecular MRI differentiation between primary central nervous system lymphomas and high-grade gliomas using endogenous protein-based amide proton transfer MR imaging at 3 Tesla
verfasst von
Shanshan Jiang
Hao Yu
Xianlong Wang
Shilong Lu
Yufa Li
Lyujin Feng
Yi Zhang
Hye-Young Heo
Dong-Hoon Lee
Jinyuan Zhou
Zhibo Wen
Publikationsdatum
01.01.2016
Verlag
Springer Berlin Heidelberg
Erschienen in
European Radiology / Ausgabe 1/2016
Print ISSN: 0938-7994
Elektronische ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-015-3805-1

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