A Novel Approach to Determining Tumor Progression Using a Three-Site Pilot Clinical Trial of Spectroscopic MRI-Guided Radiation Dose Escalation in Glioblastoma
Abstract
:1. Introduction
2. Materials and Methods
2.1. Clinical Trial Treatment Protocol
2.2. Follow-Up
2.3. Tumor Recurrence Determination
2.4. Survival Analysis
3. Results
3.1. Survival Analysis
3.2. Example Assessments of Recurrence Using Patient Follow-Up
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Gilbert, M.R.; Dignam, J.; Won, M.; Blumenthal, D.T.; Vogelbaum, M.A.; Aldape, K.D.; Colman, H.; Chakravarti, A.; Jeraj, R.; Armstrong, T.S.; et al. RTOG 0825: Phase III double-blind placebo-controlled trial evaluating bevacizumab (Bev) in patients (Pts) with newly diagnosed glioblastoma (GBM). J. Clin. Oncol. 2013, 31, 1. [Google Scholar] [CrossRef]
- Stupp, R.; Taillibert, S.; Kanner, A.; Read, W.; Steinberg, D.; Lhermitte, B.; Toms, S.; Idbaih, A.; Ahluwalia, M.S.; Fink, K.; et al. Effect of Tumor-Treating Fields Plus Maintenance Temozolomide vs Maintenance Temozolomide Alone on Survival in Patients With Glioblastoma: A Randomized Clinical Trial. JAMA 2017, 318, 2306–2316. [Google Scholar] [CrossRef] [PubMed]
- Tan, A.C.; Ashley, D.M.; López, G.Y.; Malinzak, M.; Friedman, H.S.; Khasraw, M. Management of glioblastoma: State of the art and future directions. CA Cancer J. Clin. 2020, 70, 299–312. [Google Scholar] [CrossRef] [PubMed]
- Ostrom, Q.T.; Gittleman, H.; Farah, P.; Ondracek, A.; Chen, Y.; Wolinsky, Y.; Stroup, N.E.; Kruchko, C.; Barnholtz-Sloan, J.S. CBTRUS statistical report: Primary brain and central nervous system tumors diagnosed in the United States in 2006–2010. Neuro-Oncol. 2013, 15 (Suppl. 2), ii1–ii56. [Google Scholar] [CrossRef] [PubMed]
- Kelly, P.J.; Daumas-Duport, C.; Kispert, D.B.; Kall, B.A.; Scheithauer, B.W.; Illig, J.J. Imaging-based stereotaxic serial biopsies in untreated intracranial glial neoplasms. J. Neurosurg. 1987, 66, 865–874. [Google Scholar] [CrossRef]
- Wernicke, A.G.; Smith, A.W.; Taube, S.; Mehta, M.P. Glioblastoma: Radiation treatment margins, how small is large enough? Pract. Radiat. Oncol. 2016, 6, 298–305. [Google Scholar] [CrossRef]
- Ramesh, K.; Mellon, E.A.; Gurbani, S.S.; Weinberg, B.D.; Schreibmann, E.; Sheriff, S.A.; Goryawala, M.; de le Fuente, M.; Eaton, B.R.; Zhong, J.; et al. A Multi-Institutional Pilot Clinical Trial of Spectroscopic MRI-guided Radiation Dose Escalation for Newly-Diagnosed Glioblastoma. Neuro-Oncol. Adv. 2022, 4, vdac006. [Google Scholar] [CrossRef]
- Nelson, S.J.; Vigneron, D.B.; Dillon, W.P. Serial evaluation of patients with brain tumors using volume MRI and 3D 1H MRSI. NMR Biomed. 1999, 12, 123–138. [Google Scholar] [CrossRef]
- Duijn, J.H.; Matson, G.B.; Maudsley, A.A.; Weiner, M.W. 3D phase encoding 1H spectroscopic imaging of human brain. Magn. Reson. Imaging 1992, 10, 315–319. [Google Scholar] [CrossRef]
- Horská, A.; Barker, P.B. Imaging of brain tumors: MR spectroscopy and metabolic imaging. Neuroimaging Clin. N. Am. 2010, 20, 293–310. [Google Scholar] [CrossRef] [Green Version]
- Farche, M.K.; Fachinetti, N.O.; da Silva, L.R.; Matos, L.A.; Appenzeller, S.; Cendes, F.; Reis, F. Revisiting the use of proton magnetic resonance spectroscopy in distinguishing between primary and secondary malignant tumors of the central nervous system. Neuroradiol. J. 2022, 35, 619–626. [Google Scholar] [CrossRef]
- Pirzkall, A.; Li, X.; Oh, J.; Chang, S.; Berger, M.S.; Larson, D.A.; Verhey, L.J.; Dillon, W.P.; Nelson, S.J. 3D MRSI for resected high-grade gliomas before RT: Tumor extent according to metabolic activity in relation to MRI. Int. J. Radiat. Oncol. Biol. Phys. 2004, 59, 126–137. [Google Scholar] [CrossRef]
- Narayana, A.; Chang, J.; Thakur, S.; Huang, W.; Karimi, S.; Hou, B.; Kowalski, A.; Perera, G.; Holodny, A.; Gutin, P.H. Use of MR spectroscopy and functional imaging in the treatment planning of gliomas. Br. J. Radiol. 2007, 80, 347–354. [Google Scholar] [CrossRef]
- Cordova, J.S.; Shu, H.K.; Liang, Z.; Gurbani, S.S.; Cooper, L.A.; Holder, C.A.; Olson, J.J.; Kairdolf, B.; Schreibmann, E.; Neill, S.G.; et al. Whole-brain spectroscopic MRI biomarkers identify infiltrating margins in glioblastoma patients. Neuro-Oncol. 2016, 18, 1180–1189. [Google Scholar] [CrossRef]
- Gilbert, M.R.; Dignam, J.J.; Armstrong, T.S.; Wefel, J.S.; Blumenthal, D.T.; Vogelbaum, M.A.; Colman, H.; Chakravarti, A.; Pugh, S.; Won, M.; et al. A Randomized Trial of Bevacizumab for Newly Diagnosed Glioblastoma. N. Engl. J. Med. 2014, 370, 699–708. [Google Scholar] [CrossRef]
- Gilbert, M.R.; Wang, M.; Aldape, K.D.; Stupp, R.; Hegi, M.; Jaeckle, K.A.; Armstrong, T.S.; Wefel, J.S.; Won, M.; Blumenthal, D.T.; et al. RTOG 0525: A randomized phase III trial comparing standard adjuvant temozolomide (TMZ) with a dose-dense (dd) schedule in newly diagnosed glioblastoma (GBM). J. Clin. Oncol. 2011, 29, 2006. [Google Scholar] [CrossRef]
- Stupp, R.; Hegi, M.E.; Mason, W.P.; van den Bent, M.J.; Taphoorn, M.J.; Janzer, R.C.; Ludwin, S.K.; Allgeier, A.; Fisher, B.; Belanger, K.; et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 2009, 10, 459–466. [Google Scholar] [CrossRef]
- Lawrence, Y.R.; Li, X.A.; el Naqa, I.; Hahn, C.A.; Marks, L.B.; Merchant, T.E.; Dicker, A.P. Radiation dose-volume effects in the brain. Int. J. Radiat. Oncol. Biol. Phys. 2010, 76, S20–S27. [Google Scholar] [CrossRef]
- Zikou, A.; Sioka, C.; Alexiou, G.A.; Fotopoulos, A.; Voulgaris, S.; Argyropoulou, M.I. Radiation Necrosis, Pseudoprogression, Pseudoresponse, and Tumor Recurrence: Imaging Challenges for the Evaluation of Treated Gliomas. Contrast Media Mol. Imaging 2018, 2018, 6828396. [Google Scholar] [CrossRef]
- Fulham, M.J.; Bizzi, A.; Dietz, M.J.; Shih, H.H.; Raman, R.; Sobering, G.S.; Frank, J.A.; Dwyer, A.J.; Alger, J.R.; Di Chiro, G. Mapping of brain tumor metabolites with proton MR spectroscopic imaging: Clinical relevance. Radiology 1992, 185, 675–686. [Google Scholar] [CrossRef]
- Gurbani, S.; Weinberg, B.; Cooper, L.; Mellon, E.; Schreibmann, E.; Sheriff, S.; Maudsley, A.; Goryawala, M.; Shu, H.K.; Shim, H. The Brain Imaging Collaboration Suite (BrICS): A Cloud Platform for Integrating Whole-Brain Spectroscopic MRI into the Radiation Therapy Planning Workflow. Tomography 2019, 5, 184–191. [Google Scholar] [CrossRef] [PubMed]
- Ramesh, K.; Gurbani, S.S.; Mellon, E.A.; Huang, V.; Goryawala, M.; Barker, P.B.; Kleinberg, L.; Shu, H.G.; Shim, H.; Weinberg, B.D. The Longitudinal Imaging Tracker (BrICS-LIT): A Cloud Platform for Monitoring Treatment Response in Glioblastoma Patients. Tomography 2020, 6, 93–100. [Google Scholar] [CrossRef] [PubMed]
- Cramer, J.A.; Eisenmenger, L.B.; Pierson, N.S.; Dhatt, H.S.; Heilbrun, M.E. Structured and templated reporting: An overview. Appl. Radiol. 2014, 43, 18–21. [Google Scholar] [CrossRef] [PubMed]
- Ganeshan, D.; Duong, P.T.; Probyn, L.; Lenchik, L.; McArthur, T.A.; Retrouvey, M.; Ghobadi, E.H.; Desouches, S.L.; Pastel, D.; Francis, I.R. Structured Reporting in Radiology. Acad. Radiol. 2018, 25, 66–73. [Google Scholar] [CrossRef]
- Gore, A.; Hoch, M.J.; Shu, H.G.; Olson, J.J.; Voloschin, A.D.; Weinberg, B.D. Institutional Implementation of a Structured Reporting System: Our Experience with the Brain Tumor Reporting and Data System. Acad. Radiol. 2019, 26, 974–980. [Google Scholar] [CrossRef]
- Weinberg, B.D.; Gore, A.; Shu, H.G.; Olson, J.J.; Duszak, R.; Voloschin, A.D.; Hoch, M.J. Management-Based Structured Reporting of Posttreatment Glioma Response with the Brain Tumor Reporting and Data System. J. Am. Coll. Radiol. JACR 2018, 15, 767–771. [Google Scholar] [CrossRef]
- Zhang, J.Y.; Weinberg, B.D.; Hu, R.; Saindane, A.; Mullins, M.; Allen, J.; Hoch, M.J. Quantitative Improvement in Brain Tumor MRI through Structured Reporting (BT-RADS). Acad. Radiol. 2020, 27, 780–784. [Google Scholar] [CrossRef]
- Maudsley, A.A.; Darkazanli, A.; Alger, J.R.; Hall, L.O.; Schuff, N.; Studholme, C.; Yu, Y.; Ebel, A.; Frew, A.; Goldgof, D.; et al. Comprehensive processing, display and analysis for in vivo MR spectroscopic imaging. NMR Biomed. 2006, 19, 492–503. [Google Scholar] [CrossRef]
- Stupp, R.; Mason, W.P.; van den Bent, M.J.; Weller, M.; Fisher, B.; Taphoorn, M.J.; Belanger, K.; Brandes, A.A.; Marosi, C.; Bogdahn, U.; et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 2005, 352, 987–996. [Google Scholar] [CrossRef]
- Davidson-Pilon, C. Lifelines: Survival analysis in Python. J. Open Source Softw. 2019, 4, 1317. [Google Scholar] [CrossRef] [Green Version]
- Bland, J.M.; Altman, D.G. Survival probabilities (the Kaplan-Meier method). BMJ 1998, 317, 1572–1580. [Google Scholar] [CrossRef]
- Shu, H.; Mellon, E.A.; Kleinberg, L.R.; Gurbani, S.S.; Ramesh, K.K.; Goryawala, M.; Sheriff, S.A.; Huang, V.; Barker, P.B.; Maudsley, A.; et al. A multisite clinical trial of spectroscopic MRI-guided radiation dose escalation for newly-diagnosed glioblastomas. In Proceedings of the American Society of Clinical Oncology Virtual, Online, 4–8 June 2021. [Google Scholar]
- Gondi, V.; Pugh, S.; Tsien, C.; Chenevert, T.; Gilbert, M.; Omuro, A.; Mcdonough, J.; Aldape, K.; Srinivasan, A.; Rogers, C. Radiotherapy (RT) Dose-intensification (DI) Using Intensity-modulated RT (IMRT) versus Standard-dose (SD) RT with Temozolomide (TMZ) in Newly Diagnosed Glioblastoma (GBM): Preliminary Results of NRG Oncology BN001. Int. J. Radiat. Oncol. Biol. Phys. 2020, 108, S22–S23. [Google Scholar] [CrossRef]
- Yang, Y.; Yang, Y.; Wu, X.; Pan, Y.; Zhou, D.; Zhang, H.; Chen, Y.; Zhao, J.; Mo, Z.; Huang, B. Adding DSC PWI and DWI to BT-RADS can help identify postoperative recurrence in patients with high-grade gliomas. J. Neuro-Oncol. 2020, 146, 363–371. [Google Scholar] [CrossRef]
- da Cruz, L.C.H., Jr.; Rodriguez, I.; Domingues, R.C.; Gasparetto, E.L.; Sorensen, A.G. Pseudoprogression and pseudoresponse: Imaging challenges in the assessment of posttreatment glioma. AJNR Am. J. Neuroradiol. 2011, 32, 1978–1985. [Google Scholar] [CrossRef] [Green Version]
Patient | PFS (Months) | IDH | MGMT | EOR (cc) | Progression Type |
---|---|---|---|---|---|
1 | 19.0 | 1 | 1 | 1.6 | In-Field |
2 | 14.3 | 0 | 0 | 2.6 | In-Field |
3 | 16.6 | 0 | 0 | 0.3 | Out-of-Field |
4 | 12.6 | 0 | 1 | 2.2 | In-Field |
5 | 13.9 | 0 | 0 | 0.5 | In-Field |
6 | 8.4 | 0 | 0 | 1.4 | In-Field |
7 | 8.1 | 0 | 0 | 12.1 | Multifocal |
8 | 6.2 | 0 | 0 | 3.9 | Multifocal |
9 | 10.2 | 0 | 1 | 7 | Out-of-Field |
10 | 7.1 | 0 | 0 | 0.4 | Multifocal |
11 | 11.0 | 0 | 1 | 5 | Multifocal |
12 | 11.5 | 0 | 0 | 2 | In-Field |
13 | 16.2 | 0 | 0 | 0.5 | In-Field |
14 | 29.6 | 0 | 1 | 2.9 | Out-of-Field |
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Ramesh, K.K.; Huang, V.; Rosenthal, J.; Mellon, E.A.; Goryawala, M.; Barker, P.B.; Gurbani, S.S.; Trivedi, A.G.; Giuffrida, A.S.; Schreibmann, E.; et al. A Novel Approach to Determining Tumor Progression Using a Three-Site Pilot Clinical Trial of Spectroscopic MRI-Guided Radiation Dose Escalation in Glioblastoma. Tomography 2023, 9, 362-374. https://doi.org/10.3390/tomography9010029
Ramesh KK, Huang V, Rosenthal J, Mellon EA, Goryawala M, Barker PB, Gurbani SS, Trivedi AG, Giuffrida AS, Schreibmann E, et al. A Novel Approach to Determining Tumor Progression Using a Three-Site Pilot Clinical Trial of Spectroscopic MRI-Guided Radiation Dose Escalation in Glioblastoma. Tomography. 2023; 9(1):362-374. https://doi.org/10.3390/tomography9010029
Chicago/Turabian StyleRamesh, Karthik K., Vicki Huang, Jeffrey Rosenthal, Eric A. Mellon, Mohammed Goryawala, Peter B. Barker, Saumya S. Gurbani, Anuradha G. Trivedi, Alexander S. Giuffrida, Eduard Schreibmann, and et al. 2023. "A Novel Approach to Determining Tumor Progression Using a Three-Site Pilot Clinical Trial of Spectroscopic MRI-Guided Radiation Dose Escalation in Glioblastoma" Tomography 9, no. 1: 362-374. https://doi.org/10.3390/tomography9010029
APA StyleRamesh, K. K., Huang, V., Rosenthal, J., Mellon, E. A., Goryawala, M., Barker, P. B., Gurbani, S. S., Trivedi, A. G., Giuffrida, A. S., Schreibmann, E., Han, H., de le Fuente, M., Dunbar, E. M., Holdhoff, M., Kleinberg, L. R., Shu, H. -K. G., Shim, H., & Weinberg, B. D. (2023). A Novel Approach to Determining Tumor Progression Using a Three-Site Pilot Clinical Trial of Spectroscopic MRI-Guided Radiation Dose Escalation in Glioblastoma. Tomography, 9(1), 362-374. https://doi.org/10.3390/tomography9010029