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The utility of arterial spin labeling imaging for predicting prognosis after a recurrence of high-grade glioma in patients under bevacizumab treatment

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Abstract

Background and purpose

Currently, the antiangiogenic agent bevacizumab (BVZ) is used as a treatment option for high-grade glioma (HGG) patients. However, BVZ restores disruptions of the blood–brain barrier, which leads to the disappearance of contrast enhancement during radiological examinations and therefore complicates evaluations of treatment efficacy. This study aimed to investigate the radio-morphological features of recurrent lesions that newly appeared under BVZ therapy, as well as the utility of arterial spin labeling (ASL) perfusion imaging for evaluating treatment response and prognosis in HGG patients receiving BVZ.

Methods

Thirty-two patients (20 males, 12 females; age range, 35–84 years) with HGG who experienced a recurrence under BVZ therapy were enrolled. We measured the relative cerebral blood flow (rCBF) values of each recurrent lesion using ASL, and retrospectively investigated the correlation between rCBF values and prognosis.

Results

The optimal rCBF cut-off value for predicting prognosis was defined as 1.67 using receiver operating characteristic curve analysis. The patients in the rCBF < 1.67 group had significantly longer overall survival (OS) and post-progression survival (PPS) than those in the rCBF ≥ 1.67 group (OS: 34.0 months vs. 13.0 months, p = 0.03 and PPS: 13.0 months vs. 6.0 months, p < 0.001, respectively).

Conclusion

The ASL-derived rCBF values of recurrent lesions may serve as an effective imaging biomarker for prognosis in HGG patients undergoing BVZ therapy. Low rCBF values may indicate that BVZ efficacy is sustainable, which will influence BVZ treatment strategies in HGG patients.

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Data availability

The data used in this study are available to researchers on request. Requests for data can be sent to the corresponding author.

References

  1. No authors listed (2017) Brain Tumor Registry of Japan (2005–2008). Neurol Med Chir (Tokyo) 57:9–102. https://doi.org/10.2176/nmc.sup.2017-0001

    Article  Google Scholar 

  2. Henriksen OM, Del Mar Álvarez-Torres M, Figueiredo P et al (2022) High-Grade Glioma Treatment Response monitoring biomarkers: a position Statement on the evidence supporting the Use of Advanced MRI techniques in the Clinic, and the latest bench-to-Bedside developments. Part 1: perfusion and diffusion techniques. Front Oncol 12:810263. https://doi.org/10.3389/fonc.2022.810263

    Article  PubMed  PubMed Central  Google Scholar 

  3. Seyedmirzaei H, Shobeiri P, Turgut M et al (2020) VEGF levels in patients with glioma: a systematic review and meta-analysis. Rev Neurosci 32:191–202. https://doi.org/10.1515/revneuro-2020-0062

    Article  PubMed  CAS  Google Scholar 

  4. Hegi ME, Diserens AC, Gorlia T et al (2005) MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 352:997–1003. https://doi.org/10.1056/NEJMoa043331

    Article  PubMed  CAS  Google Scholar 

  5. Hutterer M, Hattingen E, Palm C et al (2015) Current standards and new concepts in MRI and PET response assessment of antiangiogenic therapies in high-grade glioma patients. Neuro Oncol 17:784–800. https://doi.org/10.1093/neuonc/nou322

    Article  PubMed  CAS  Google Scholar 

  6. Lyu Y, Liu S, You H et al (2017) Evaluation of recurrent high-grade gliomas treated with bevacizumab: a preliminary report of 3D pseudocontinuous artery spin labeling. Magn Reson Imaging 46:565–573. https://doi.org/10.1002/jmri.25558

    Article  Google Scholar 

  7. 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 28:1963–1972. https://doi.org/10.1200/JCO.2009.26.3541

    Article  PubMed  Google Scholar 

  8. Schmainda KM, Zhang Z, Prah M et al (2015) Dynamic susceptibility contrast MRI measures of relative cerebral blood volume as a prognostic marker for overall survival in recurrent glioblastoma: results from the ACRIN 6677/RTOG 0625 multicenter trial. Neuro Oncol 17:1148–1156. https://doi.org/10.1093/neuonc/nou364

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Kickingereder P, Wiestler B, Burth S et al (2015) Relative cerebral blood volume is a potential predictive imaging biomarker of bevacizumab efficacy in recurrent glioblastoma. Neuro Oncol 17:1139–1147. https://doi.org/10.1093/neuonc/nov028

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  10. Beppu T, Sato Y, Sasaki T et al (2019) Comparisons between PET with 11 C-Methyl-L-Methionine and arterial spin labeling perfusion imaging in recurrent glioblastomas treated with Bevacizumab. Clin Nucl Med 44:186–193. https://doi.org/10.1097/RLU.0000000000002417

    Article  PubMed  Google Scholar 

  11. Golay X, Hendrikse J, Lim TC (2004) Perfusion imaging using arterial spin labeling. Top Magn Reson Imaging 15:10–27

    Article  PubMed  Google Scholar 

  12. Falk Delgado A, De Luca F, van Westen D et al (2018) Arterial spin labeling MR imaging for differentiation between high- and low-grade glioma-a meta-analysis. Neuro Oncol 20:1450–1461. https://doi.org/10.1093/neuonc/noy095

    Article  PubMed  PubMed Central  Google Scholar 

  13. Yang S, Zhao B, Wang G et al (2016) Improving the Grading Accuracy of Astrocytic Neoplasms noninvasively by combining timing information with cerebral blood Flow: a Multi-TI arterial spin-labeling MR Imaging Study. AJNR Am J Neuroradiol 37:2209–2216. https://doi.org/10.3174/ajnr.A4907

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Batalov AI, Afandiev RM, Zakharova NE et al (2022) 3D pseudo-continuous arterial spin labeling-MRI (3D PCASL-MRI) in the differential diagnosis between glioblastomas and primary central nervous system Lymphomas. Neuroradiology 64:1539–1545. https://doi.org/10.1007/s00234-021-02888-4

    Article  PubMed  CAS  Google Scholar 

  15. Xi YB, Kang XW, Wang N et al (2019) Differentiation of primary central nervous system Lymphoma from high-grade glioma and brain Metastasis using arterial spin labeling and dynamic contrast-enhanced magnetic resonance imaging. Eur J Radiol 112:59–64. https://doi.org/10.1016/j.ejrad.2019.01.008

    Article  PubMed  Google Scholar 

  16. Choi YJ, Kim HS, Jahng GH et al (2013) Pseudoprogression in patients with glioblastoma: added value of arterial spin labeling to dynamic susceptibility contrast perfusion MR imaging. Acta Radiol 54:448–454. https://doi.org/10.1177/0284185112474916

    Article  PubMed  Google Scholar 

  17. Manning P, Daghighi S, Rajaratnam MK et al (2020) Differentiation of Progressive Disease from pseudoprogression using 3D PCASL and DSC perfusion MRI in patients with glioblastoma. J Neurooncol 147:681–690. https://doi.org/10.1007/s11060-020-03475-y

    Article  PubMed  Google Scholar 

  18. Takano S, Kato Y, Yamamoto T et al (2012) Immunohistochemical detection of IDH1 mutation, p53, and internexin as prognostic factors of glial tumors. J Neurooncol 108:361–373. https://doi.org/10.1007/s11060-012-0837-0

    Article  PubMed  CAS  Google Scholar 

  19. Schmainda KM, Prah MA, Marques H et al (2021) Value of dynamic contrast perfusion MRI to predict early response to bevacizumab in newly diagnosed glioblastoma: results from ACRIN 6686 multicenter trial. Neuro Oncol 23:314–323. https://doi.org/10.1093/neuonc/noaa167

    Article  PubMed  CAS  Google Scholar 

  20. Zhang W, Kreisl T, Solomon J et al (2009) Acute effects of bevacizumab on glioblastoma vascularity assessed with DCE-MRI and relation to patient survival. Proc Intl Soc Magn Reson Med 17:282

    CAS  Google Scholar 

  21. Kickingereder P, Wiestler B, Graf M et al (2015) Evaluation of dynamic contrast-enhanced MRI derived microvascular permeability in recurrent glioblastoma treated with bevacizumab. J Neurooncol 121:373–380. https://doi.org/10.1007/s11060-014-1644-6

    Article  PubMed  CAS  Google Scholar 

  22. Essig M, Shiroishi MS, Nguyen TB et al (2013) Perfusion MRI: the five most frequently asked technical questions. AJR Am J Roentgenol 200:24–34. https://doi.org/10.2214/AJR.12.9543

    Article  PubMed  PubMed Central  Google Scholar 

  23. Galldiks N, Rapp M, Stoffels G et al (2013) Earlier diagnosis of Progressive Disease during bevacizumab treatment using O-(2-18F-fluorethyl)-L-tyrosine positron emission tomography in comparison with magnetic resonance imaging. Mol Imaging 12:273–276

    Article  PubMed  Google Scholar 

  24. Galldiks N, Rapp M, Stoffels G et al (2013) Response assessment of bevacizumab in patients with recurrent malignant glioma using [18F] Fluoroethyl-L-tyrosine PET in comparison to MRI. Eur J Nucl Med Mol Imaging 40:22–33. https://doi.org/10.1007/s00259-012-2251-4

    Article  PubMed  CAS  Google Scholar 

  25. Schwarzenberg J, Czernin J, Cloughesy TF et al (2014) Treatment response evaluation using 18F-FDOPA PET in patients with recurrent malignant glioma on bevacizumab therapy. Clin Cancer Res 20:3550–3559. https://doi.org/10.1158/1078-0432.CCR-13-1440

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Hughes KL, O’Neal CM, Andrews BJ et al (2021) A systematic review of the utility of amino acid PET in assessing treatment response to bevacizumab in recurrent high-grade glioma. Neurooncol Adv 3:vdab003. https://doi.org/10.1093/noajnl/vdab003

    Article  PubMed  PubMed Central  Google Scholar 

  27. Gaddamanugu S, Shafaat O, Sotoudeh H et al (2022) Clinical applications of diffusion-weighted sequence in brain imaging: beyond Stroke. Neuroradiology 64:15–30. https://doi.org/10.1007/s00234-021-02819-3

    Article  PubMed  Google Scholar 

  28. Nguyen HS, Milbach N, Hurrell SL et al (2016) Progressing Bevacizumab-Induced Diffusion Restriction is Associated with Coagulative Necrosis surrounded by viable Tumor and decreased overall survival in patients with recurrent glioblastoma. AJNR Am J Neuroradiol 37:2201–2208. https://doi.org/10.3174/ajnr.A4898

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Zakhari N, Taccone MS, Torres C et al (2018) Diagnostic accuracy of centrally restricted diffusion in the differentiation of treatment-related necrosis from Tumor Recurrence in High-Grade Gliomas. AJNR Am J Neuroradiol 39:260–264. https://doi.org/10.3174/ajnr.A5485

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Rieger J, Bähr O, Müller K et al (2010) Bevacizumab-induced diffusion-restricted lesions in malignant glioma patients. J Neurooncol 99:49–56. https://doi.org/10.1007/s11060-009-0098-8

    Article  PubMed  CAS  Google Scholar 

  31. Farid N, Almeida-Freitas DB, White NS et al (2013) Restriction-Spectrum Imaging of Bevacizumab-Related Necrosis in a patient with GBM. Front Oncol 3:258. https://doi.org/10.3389/fonc.2013.00258

    Article  PubMed  PubMed Central  Google Scholar 

  32. Mong S, Ellingson BM, Nghiemphu PL et al (2012) Persistent diffusion-restricted lesions in bevacizumab-treated malignant gliomas are associated with improved survival compared with matched controls. AJNR Am J Neuroradiol 33:1763–1770. https://doi.org/10.3174/ajnr.A3053

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Cachia D, Elshafeey NA, Kamiya-Matsuoka C et al (2017) Radiographic patterns of progression with associated outcomes after bevacizumab therapy in glioblastoma patients. J Neurooncol 135:75–81. https://doi.org/10.1007/s11060-017-2550-5

    Article  PubMed  CAS  Google Scholar 

  34. Gupta A, Young RJ, Karimi S et al (2011) Isolated diffusion restriction precedes the development of enhancing Tumor in a subset of patients with glioblastoma. AJNR Am J Neuroradiol 32:1301–1306. https://doi.org/10.3174/ajnr.A2479

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

We thank Yudai Ohta and Kyohei Okuda for their technical support in data acquisition.

Funding

This study was supported by JSPS KAKENHI grant number JP20K08135 (A.K.).

Author information

Authors and Affiliations

  1. Department of Brain and Neurosciences, Division of Neurosurgery, Faculty of Medicine, Tottori University, Tottori, Japan

    Atsushi Kambe, Tomohiro Hosoya & Masamichi Kurosaki

  2. Department of Multidisciplinary Internal Medicine, Division of Radiology, Faculty of Medicine, Tottori University, Tottori, Japan

    Shinichiro Kitao, Ryoya Ochiai & Shinya Fujii

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  1. Atsushi Kambe
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Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analyses were performed by Atsushi Kambe, Shinichiro Kitao and Ryoya Ochiai. The first draft of the manuscript was written by Atsushi Kambe, and all authors commented on previous versions of the manuscript. All authors have read and approved the final version of the manuscript.

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Correspondence to Atsushi Kambe.

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Ethics approval

This retrospective study was approved by our Institutional Review Board, and the requirement for informed consent was waived because of the retrospective nature of this study (approval no. 23A018).

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The authors have no relevant financial or non-financial interests to disclose.

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Kambe, A., Kitao, S., Ochiai, R. et al. The utility of arterial spin labeling imaging for predicting prognosis after a recurrence of high-grade glioma in patients under bevacizumab treatment. J Neurooncol 166, 175–183 (2024). https://doi.org/10.1007/s11060-023-04550-w

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