Skip to main content

Advertisement

Log in

Applying protein-based amide proton transfer MR imaging to distinguish solitary brain metastases from glioblastoma

  • Molecular Imaging
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objectives

To determine the utility of amide proton transfer-weighted (APTw) MR imaging in distinguishing solitary brain metastases (SBMs) from glioblastomas (GBMs).

Methods

Forty-five patients with SBMs and 43 patients with GBMs underwent conventional and APT-weighted sequences before clinical intervention. The APTw parameters and relative APTw (rAPTw) parameters in the tumour core and the peritumoral brain zone (PBZ) were obtained and compared between SBMs and GBMs. The receiver-operating characteristic (ROC) curve was used to assess the best parameter for distinguishing between the two groups.

Results

The APTwmax, APTwmin, APTwmean, rAPTwmax, rAPTwmin or rAPTwmean values in the tumour core were not significantly different between the SBM and GBM groups (P = 0.141, 0.361, 0.221, 0.305, 0.578 and 0.448, respectively). However, the APTwmax, APTwmin, APTwmean, rAPTwmax, rAPTwmin or rAPTwmean values in the PBZ were significantly lower in the SBM group than in the GBM group (P < 0.001). The APTwmin values had the highest area under the ROC curve 0.905 and accuracy 85.2% in discriminating between the two neoplasms.

Conclusion

As a noninvasive imaging method, APT-weighted MR imaging can be used to distinguish SBMs from GBMs.

Key Points

APTw values in the tumour core were not different between SBMs and GBMs.

APTw values in peritumoral brain zone were lower in SBMs than in GBMs.

The APTw min was the best parameter to distinguish SBMs from GBMs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

GBM:

Glioblastoma

SBM:

Solitary brain metastases

APT:

Amide proton transfer

APTw:

APT-weighted

rAPTw:

Relative APTw

CEST:

Chemical exchange-based saturation transfer

CNAWM:

Contralateral normal-appearing white matter

Gd:

Gadolinium

H&E:

Haematoxylin and eosin

PBZ:

Peritumoral brain zone

References

  1. Wang X, Chen JX, Zhou Q et al (2016) Statistical report of central nervous system tumors histologically diagnosed in the Sichuan Province of China from 2008 to 2013: a West China Glioma Center Report. Ann Surg Oncol. doi:10.1245/s10434-016-5410-1

    Article  PubMed  PubMed Central  Google Scholar 

  2. Ostrom QT, Gittleman H, Fulop J et al (2015) CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2008-2012. Neuro-Oncology 17:v1–iv62

    Article  Google Scholar 

  3. Blanchet L, Krooshof PW, Postma GJ et al (2011) Discrimination between metastasis and glioblastoma multiforme based on morphometric analysis of MR images. AJNR Am J Neuroradiol 32:67–73

    Article  CAS  Google Scholar 

  4. Yuh WT, Engelken JD, Muhonen MG, Mayr NA, Fisher DJ, Ehrhardt JC (1992) Experience with high-dose gadolinium MR imaging in the evaluation of brain metastases. AJNR Am J Neuroradiol 13:335–345

    CAS  PubMed  Google Scholar 

  5. Owonikoko TK, Arbiser J, Zelnak A et al (2014) Current approaches to the treatment of metastatic brain tumours. Nat Rev Clin Oncol 11:203–222

    Article  CAS  Google Scholar 

  6. Wen PY, Kesari S (2008) Malignant gliomas in adults. N Engl J Med 359:492–507

    Article  CAS  Google Scholar 

  7. Lee EJ, Ahn KJ, Lee EK, Lee YS, Kim DB (2013) Potential role of advanced MRI techniques for the peritumoural region in differentiating glioblastoma multiforme and solitary metastatic lesions. Clin Radiol 68:e689–e697

    Article  CAS  Google Scholar 

  8. Han CK, Huang SM, Guo JF, Zhuang XJ, Han HW (2015) Use of a high b-value for diffusion weighted imaging of peritumoral regions to differentiate high-grade gliomas and solitary metastases. J Magn Reson Imaging 42:80–86

    Article  Google Scholar 

  9. Abe T, Mizobuchi Y, Sako W et al (2015) Clinical significance of discrepancy between arterial spin labeling images and contrast-enhanced images in the diagnosis of brain tumors. Magn Reson Med Sci 14:313–319

    Article  Google Scholar 

  10. Caivano R, Lotumolo A, Rabasco P et al (2013) 3 Tesla magnetic resonance spectroscopy: cerebral gliomas vs. metastatic brain tumors. Our experience and review of the literature. Int J Neurosci 123:537–543

    Article  CAS  Google Scholar 

  11. Mouthuy N, Cosnard G, Abarca-Quinones J, Michoux N (2012) Multiparametric magnetic resonance imaging to differentiate high-grade gliomas and brain metastases. J Neuroradiology Journal de neuroradiologie 39:301–307

    Article  Google Scholar 

  12. 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 50:1120–1126

    Article  Google Scholar 

  13. 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 9:1085–1090

    Article  CAS  Google Scholar 

  14. van Zijl PCM, Yadav NN (2011) Chemical exchange saturation transfer (CEST): what is in a name and what Isn't? Magn Reson Med 65:927–948

    Article  Google Scholar 

  15. Jiang SS, Yu H, Wang XL et al (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 Tesla. Eur Radiol 26:64–71

    Article  Google Scholar 

  16. 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 38:1119–1128

    Article  Google Scholar 

  17. Togao O, Kessinger CW, Huang G et al (2013) Characterization of lung cancer by amide proton transfer (APT) imaging: an in-vivo study in an orthotopic mouse model. Plos One 8:e77019

    Article  CAS  Google Scholar 

  18. Wen ZB, Hu SG, Huang FH et al (2010) MR imaging of high-grade brain tumors using endogenous protein and peptide-based contrast. Neuroimage 51:616–622

    Article  Google Scholar 

  19. Togao O, Hiwatashi A, Yamashita K et al (2016) Grading diffuse gliomas without intense contrast enhancement by amide proton transfer MR imaging: comparisons with diffusion- and perfusion-weighted imaging. Eur Radiol. doi:10.1007/s00330-016-4328-0:1-11

    Article  PubMed  Google Scholar 

  20. Sakata A, Okada T, Yamamoto A et al (2015) Grading glial tumors with amide proton transfer MR imaging: different analytical approaches. J Neuro-Oncol 122:339–348

    Article  CAS  Google Scholar 

  21. Jia G, Abaza R, Williams JD et al (2011) Amide proton transfer MR imaging of prostate cancer: a preliminary study. J Magn Reson Imaging 33:647–654

    Article  Google Scholar 

  22. Klomp DWJ, Dula AN, Arlinghaus LR et al (2013) Amide proton transfer imaging of the human breast at 7T: development and reproducibility. NMR Biomed 26:1271–1277

    Article  CAS  Google Scholar 

  23. 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 70:216–224

    Article  CAS  Google Scholar 

  24. Wang J, Weygand J, Hwang KP et al (2016) Magnetic resonance imaging of glucose uptake and metabolism in patients with head and neck cancer. Scientific reports 6:30618

    Article  CAS  Google Scholar 

  25. 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 27:1239–1247

    Article  Google Scholar 

  26. Zhou JY, Tryggestad E, Wen ZB et al (2011) Differentiation between glioma and radiation necrosis using molecular magnetic resonance imaging of endogenous proteins and peptides. Nat Med 17:130–U308

    Article  CAS  Google Scholar 

  27. Ma B, Blakeley JO, Hong X et al (2016) Applying amide proton transfer-weighted MRI to distinguish pseudoprogression from true progression in malignant gliomas. J Magn Reson Imaging 44:456–462

    Article  Google Scholar 

  28. 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 27:163–174

    Article  Google Scholar 

  29. Tee YK, Harston GWJ, Blockley N et al (2014) Comparing different analysis methods for quantifying the MRI amide proton transfer (APT) effect in hyperacute stroke patients. NMR Biomed 27:1019–1029

    Article  CAS  Google Scholar 

  30. Zhao XN, Wen ZB, Huang FH et al (2011) Saturation power dependence of amide proton transfer image contrasts in human brain tumors and strokes at 3 T. Magn Reson Med 66:1033–1041

    Article  Google Scholar 

  31. Li CM, Peng S, Wang R et al (2014) Chemical exchange saturation transfer MR imaging of Parkinson's disease at 3 Tesla. Eur Radiol 24:2631–2639

    Article  Google Scholar 

  32. Zhang Y, Heo HY, Lee DH et al (2016) Selecting the reference image for registration of CEST series. J Magn Reson Imaging 43:756–761

    Article  Google Scholar 

  33. Zhang H, Kang H, Zhao X et al (2016) Amide proton transfer (APT) MR imaging and magnetization transfer (MT) MR imaging of pediatric brain development. Eur Radiol 26:3368–3376

    Article  Google Scholar 

  34. Allen JS, Bruss J, Brown CK, Damasio H (2005) Normal neuroanatomical variation due to age: the major lobes and a parcellation of the temporal region. Neurobiol Aging 26:1245–1260

    Article  Google Scholar 

  35. Tan Y, Wang XC, Zhang H et al (2015) Differentiation of high-grade-astrocytomas from solitary-brain-metastases: comparing diffusion kurtosis imaging and diffusion tensor imaging. Eur J Radiol 84:2618–2624

    Article  Google Scholar 

  36. Crisi G, Orsingher L, Filice S (2013) Lipid and macromolecules quantitation in differentiating glioblastoma from solitary metastasis: a short-echo time single-voxel magnetic resonance spectroscopy study at 3 T. J Comput Assist Tomogr 37:265–271

    Article  Google Scholar 

  37. Lee EJ, terBrugge K, Mikulis D et al (2011) Diagnostic value of peritumoral minimum apparent diffusion coefficient for differentiation of glioblastoma multiforme from solitary metastatic lesions. AJR Am J Roentgenol 196:71–76

    Article  Google Scholar 

  38. Ramalho J, Castillo M, AlObaidy M et al (2015) High signal intensity in globus pallidus and dentate nucleus on unenhanced T1-weighted MR images: evaluation of two linear gadolinium-based contrast agents. Radiology 276:836–844

    Article  Google Scholar 

  39. Collidge TA, Thomson PC, Mark PB et al (2007) Gadolinium-enhanced MR imaging and nephrogenic systemic fibrosis: retrospective study of a renal replacement therapy cohort. Radiology 245:168–175

    Article  Google Scholar 

  40. Lemee JM, Clavreul A, Aubry M et al (2015) Characterizing the peritumoral brain zone in glioblastoma: a multidisciplinary analysis. J Neuro-Oncol 122:53–61

    Article  Google Scholar 

  41. Oh J, Cha S, Aiken AH et al (2005) Quantitative apparent diffusion coefficients and T2 relaxation times in characterizing contrast enhancing brain tumors and regions of peritumoral edema. J Magn Reson Imaging 21:701–708

    Article  Google Scholar 

  42. Goplen D, Bougnaud S, Rajcevic U et al (2010) Alpha B-Crystallin is elevated in highly infiltrative apoptosis-resistant glioblastoma cells. Am J Pathol 177:1618–1628

    Article  CAS  Google Scholar 

  43. Parney IF, Waldron JS, Parsa AT (2009) Flow cytometry and in vitro analysis of human glioma-associated macrophages. Laboratory investigation Journal of neurosurgery 110:572–582

    CAS  PubMed  Google Scholar 

  44. Frieboes HB, Zheng X, Sun CH, Tromberg B, Gatenby R, Cristini V (2006) An integrated computational/experimental model of tumor invasion. Cancer Res 66:1597–1604

    Article  CAS  Google Scholar 

  45. Fazi B, Felsani A, Grassi L et al (2015) The transcriptome and miRNome profiling of glioblastoma tissues and peritumoral regions highlights molecular pathways shared by tumors and surrounding areas and reveals differences between short-term and long-term survivors. Oncotarget 6:22526–22552

    Article  Google Scholar 

Download references

Acknowledgements

This study was partially supported by grants from National Natural Science Foundation of China (81171322), Guangdong Provincial Natural Science Foundation (2014A030313271, S2012010009114), Guangdong Provincial Science and Technology Project (2014A020212726), Southern Medical University clinical research project (LC2016ZD028) and the National Institutes of Health (R01EB009731, R01CA166171).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhibo Wen.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Zhibo Wen, MD.

Conflict of interest

The authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article.

Funding

This study is partially supported by grants from National Natural Science Foundation of China (81171322), Natural Science Foundation of Guangdong Province (2014A030313271), Guangdong Provincial Science and Technology Project (2014A020212726), Natural Science Foundation of Guangdong Province (S2012010009114), Southern Medical University clinical research project (LC2016ZD028) and the National Institutes of Health (R01EB009731, R01CA166171).

Statistics and biometry

No complex statistical methods were necessary for this article.

Informed consent

Written informed consent was obtained from all subjects (patients) in this study.

Ethical approval

Institutional Review Board approval was obtained.

Methodology

• retrospective

• diagnostic or prognostic study

• performed at one institution

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yu, H., Lou, H., Zou, T. et al. Applying protein-based amide proton transfer MR imaging to distinguish solitary brain metastases from glioblastoma. Eur Radiol 27, 4516–4524 (2017). https://doi.org/10.1007/s00330-017-4867-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-017-4867-z

Keywords

Navigation