Progressing Bevacizumab-Induced Diffusion Restriction Is Associated with Coagulative Necrosis Surrounded by Viable Tumor and Decreased Overall Survival in Patients with Recurrent Glioblastoma

References

1. 1.↵
   2. Stupp R,
   3. Mason WP,
   4. van den Bent MJ, et al

   ; European Organisation for Research and Treatment of Cancer Brain Tumor and Radiotherapy Groups, National Cancer Institute of Canada Clinical Trials Group. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005;352:987–96 doi:10.1056/NEJMoa043330 pmid:15758009

   CrossRefPubMedWeb of Science
2. 2.↵
   2. Iwamoto FM,
   3. Abrey LE,
   4. Beal K, et al

   . Patterns of relapse and prognosis after bevacizumab failure in recurrent glioblastoma. Neurology 2009;73:1200–06 doi:10.1212/WNL.0b013e3181bc0184 pmid:19822869

   Abstract/FREE Full Text
3. 3.↵
   2. Wong ET,
   3. Hess KR,
   4. Gleason MJ, et al

   . Outcomes and prognostic factors in recurrent glioma patients enrolled onto phase II clinical trials. J Clin Oncol 1999;17:2572–78 pmid:10561324

   Abstract/FREE Full Text
4. 4.↵
   2. Lamborn KR,
   3. Yung WK,
   4. Chang SM, et al

   ; North American Brain Tumor Consortium. Progression-free survival: an important end point in evaluating therapy for recurrent high-grade gliomas. Neuro Oncol 2008;10:162–70 doi:10.1215/15228517-2007-062 pmid:18356283

   Abstract/FREE Full Text
5. 5.↵
   2. Cohen MH,
   3. Shen YL,
   4. Keegan P, et al

   . FDA drug approval summary: bevacizumab (Avastin) as treatment of recurrent glioblastoma multiforme. Oncologist 2009;14:1131–38 doi:10.1634/theoncologist.2009-0121 pmid:19897538

   Abstract/FREE Full Text
6. 6.↵
   2. Friedman HS,
   3. Prados MD,
   4. Wen PY, et al

   . Bevacizumab alone and in combination with irinotecan in recurrent glioblastoma. J Clin Oncol 2009;27:4733–40 doi:10.1200/JCO.2008.19.8721 pmid:19720927

   Abstract/FREE Full Text
7. 7.↵
   2. Chinot OL,
   3. Wick W,
   4. Mason W, et al

   . Bevacizumab plus radiotherapy-temozolomide for newly diagnosed glioblastoma. N Engl J Med 2014;370:709–22 doi:10.1056/NEJMoa1308345 pmid:24552318

   CrossRefPubMedWeb of Science
8. 8.↵
   2. Gilbert MR,
   3. Dignam JJ,
   4. Armstrong TS, et al

   . A randomized trial of bevacizumab for newly diagnosed glioblastoma. N Engl J Med 2014;370:699–708 doi:10.1056/NEJMoa1308573 pmid:24552317

   CrossRefPubMedWeb of Science
9. 9.↵
   2. de Groot JF,
   3. Fuller G,
   4. Kumar AJ, et al

   . Tumor invasion after treatment of glioblastoma with bevacizumab: radiographic and pathologic correlation in humans and mice. Neuro Oncol 2010;12:233–42 doi:10.1093/neuonc/nop027 pmid:20167811

   Abstract/FREE Full Text
10. 10.↵
    2. Wen PY,
    3. Macdonald DR,
    4. Reardon DA, et al

    . Updated response assessment criteria for high-grade gliomas: Response Assessment in Neuro-Oncology Working Group. J Clin Oncol 2010;28:1963–72 doi:10.1200/JCO.2009.26.3541 pmid:20231676

    Abstract/FREE Full Text
11. 11.↵
    2. LaViolette PS,
    3. Cohen AD,
    4. Prah MA, et al

    . Vascular change measured with independent component analysis of dynamic susceptibility contrast MRI predicts bevacizumab response in high-grade glioma. Neuro Oncol 2013;15:442–50 doi:10.1093/neuonc/nos323 pmid:23382287

    Abstract/FREE Full Text
12. 12.↵
    2. Schmainda KM,
    3. Prah M,
    4. Connelly J, et al

    . Dynamic-susceptibility contrast agent MRI measures of relative cerebral blood volume predict response to bevacizumab in recurrent high-grade glioma. Neuro Oncol 2014;16:880–88 doi:10.1093/neuonc/not216 pmid:24431219

    Abstract/FREE Full Text
13. 13.↵
    2. Sawlani RN,
    3. Raizer J,
    4. Horowitz SW, et al

    . Glioblastoma: a method for predicting response to antiangiogenic chemotherapy by using MR perfusion imaging–pilot study. Radiology 2010;255:622–28 doi:10.1148/radiol.10091341 pmid:20413772

    CrossRefPubMedWeb of Science
14. 14.↵
    2. Sugahara T,
    3. Korogi Y,
    4. Kochi M, et al

    . Usefulness of diffusion-weighted MRI with echo-planar technique in the evaluation of cellularity in gliomas. J Magn Reson Imaging 1999;9:53–60 pmid:10030650

    CrossRefPubMedWeb of Science
15. 15.↵
    2. Ellingson BM,
    3. Malkin MG,
    4. Rand SD, et al

    . Validation of functional diffusion maps (fDMs) as a biomarker for human glioma cellularity. J Magn Reson Imaging 2010;31:538–48 doi:10.1002/jmri.22068 pmid:20187195

    CrossRefPubMedWeb of Science
16. 16.↵
    2. Moffat BA,
    3. Chenevert TL,
    4. Lawrence TS, et al

    . Functional diffusion map: a noninvasive MRI biomarker for early stratification of clinical brain tumor response. Proc Natl Acad Sci U S A 2005;102:5524–29 doi:10.1073/pnas.0501532102 pmid:15805192

    Abstract/FREE Full Text
17. 17.↵
    2. Hamstra DA,
    3. Galbán CJ,
    4. Meyer CR, et al

    . Functional diffusion map as an early imaging biomarker for high-grade glioma: correlation with conventional radiologic response and overall survival. J Clin Oncol 2008;26:3387–94 doi:10.1200/JCO.2007.15.2363 pmid:18541899

    Abstract/FREE Full Text
18. 18.↵
    2. Ellingson BM,
    3. Cloughesy TF,
    4. Zaw T, et al

    . Functional diffusion maps (fDMs) evaluated before and after radiochemotherapy predict progression-free and overall survival in newly diagnosed glioblastoma. Neuro Oncol 2012;14:333–43 doi:10.1093/neuonc/nor220 pmid:22270220

    Abstract/FREE Full Text
19. 19.↵
    2. Ellingson BM,
    3. Cloughesy TF,
    4. Lai A, et al

    . Graded functional diffusion map-defined characteristics of apparent diffusion coefficients predict overall survival in recurrent glioblastoma treated with bevacizumab. Neuro Oncol 2011;13:1151–61 doi:10.1093/neuonc/nor079 pmid:21856685

    Abstract/FREE Full Text
20. 20.↵
    2. Ellingson BM,
    3. Kim E,
    4. Woodworth DC, et al

    . Diffusion MRI quality control and functional diffusion map results in ACRIN 6677/RTOG 0625: a multicenter, randomized, phase II trial of bevacizumab and chemotherapy in recurrent glioblastoma. Int J Oncol 2015;46:1883–92 doi:10.3892/ijo.2015.2891 pmid:25672376

    CrossRefPubMed
21. 21.↵
    2. Mong S,
    3. Ellingson BM,
    4. Nghiemphu PL, et al

    . Persistent diffusion-restricted lesions in bevacizumab-treated malignant gliomas are associated with improved survival compared with matched controls. AJNR Am J Neuroradiol 2012;33:1763–70 doi:10.3174/ajnr.A3053 pmid:22538078

    Abstract/FREE Full Text
22. 22.↵
    2. Hwang EJ,
    3. Cha Y,
    4. Lee AL, et al

    . Early response evaluation for recurrent high grade gliomas treated with bevacizumab: a volumetric analysis using diffusion-weighted imaging. J Neurooncol 2013;112:427–35 doi:10.1007/s11060-013-1072-z pmid:23417358

    CrossRefPubMed
23. 23.↵
    2. Zhang M,
    3. Gulotta B,
    4. Thomas A, et al

    . Large-volume low apparent diffusion coefficient lesions predict poor survival in bevacizumab-treated glioblastoma patients. Neuro Oncol 2016;18:735–43 doi:10.1093/neuonc/nov268 pmid:26538618

    Abstract/FREE Full Text
24. 24.↵
    2. Gupta A,
    3. Young RJ,
    4. Karimi S, et al

    . Isolated diffusion restriction precedes the development of enhancing tumor in a subset of patients with glioblastoma. AJNR Am J Neuroradiol 2011;32:1301–06 doi:10.3174/ajnr.A2479 pmid:21596805

    Abstract/FREE Full Text
25. 25.↵
    2. Gerstner ER,
    3. Frosch MP,
    4. Batchelor TT

    . Diffusion magnetic resonance imaging detects pathologically confirmed, nonenhancing tumor progression in a patient with recurrent glioblastoma receiving bevacizumab. J Clin Oncol 2010;28:e91–93 doi:10.1200/JCO.2009.25.0233 pmid:19933906

    FREE Full Text
26. 26.↵
    2. Rieger J,
    3. Bähr O,
    4. Müller K, et al

    . Bevacizumab-induced diffusion-restricted lesions in malignant glioma patients. J Neurooncol 2010;99:49–56 doi:10.1007/s11060-009-0098-8 pmid:20035366

    CrossRefPubMed
27. 27.↵
    2. Rieger J,
    3. Bähr O,
    4. Ronellenfitsch MW, et al

    . Bevacizumab-induced diffusion restriction in patients with glioma: tumor progression or surrogate marker of hypoxia? J Clin Oncol 2010;28:e477; author reply e478 doi:10.1200/JCO.2010.29.2029 pmid:20585096

    FREE Full Text
28. 28.↵
    2. Farid N,
    3. Almeida-Freitas DB,
    4. White NS, et al

    . Restriction-spectrum imaging of bevacizumab-related necrosis in a patient with GBM. Front Oncol 2013;3:258 doi:10.3389/fonc.2013.00258 pmid:24137566

    CrossRefPubMed
29. 29.↵
    2. LaViolette PS,
    3. Mickevicius NJ,
    4. Cochran EJ, et al

    . Precise ex vivo histological validation of heightened cellularity and diffusion-restricted necrosis in regions of dark apparent diffusion coefficient in 7 cases of high-grade glioma. Neuro Oncol 2014;16:1599–606 doi:10.1093/neuonc/nou142 pmid:25059209

    Abstract/FREE Full Text
30. 30.↵
    2. Farid N,
    3. Almeida-Freitas DB,
    4. White NS, et al

    . Combining diffusion and perfusion differentiates tumor from bevacizumab-related imaging abnormality (bria). J Neurooncol 2014;120:539–46 doi:10.1007/s11060-014-1583-2 pmid:25135423

    CrossRefPubMed
31. 31.↵
    2. Robbins SL,
    3. Cotran RS,
    4. Kumar V

    . Robbins and Cotran Pathologic Basis of Disease. Philadelphia: Saunders/Elsevier; 2010
32. 32.↵
    2. Hegi ME,
    3. Diserens AC,
    4. Gorlia T, et al

    . MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005;352:997–1003 doi:10.1056/NEJMoa043331 pmid:15758010

    CrossRefPubMedWeb of Science
33. 33.↵
    2. Pellatt B,
    3. Mickevicius NJ,
    4. Cochran EJ, et al

    . 3D-printed MRI-based custom brain molds for minimizing tissue distortion and precisely slicing tissue for co-registration with clinically acquired MRI in glioma patients. Neuro-Oncology 2014;16(suppl 5):v152 doi:10.1093/neuonc/nou264.62

    Abstract/FREE Full Text
34. 34.↵
    2. Pope WB,
    3. Kim HJ,
    4. Huo J, et al

    . Recurrent glioblastoma multiforme: ADC histogram analysis predicts response to bevacizumab treatment. Radiology 2009;252:182–89 doi:10.1148/radiol.2521081534 pmid:19561256

    CrossRefPubMedWeb of Science
35. 35.↵
    2. Reiger J,
    3. Bähr O,
    4. Müller K, et al

    . Bevacizumab-induced diffusion-restricted lesions in malignant glioma patients. J Neurooncol 2010;99:49–56 doi:10.1007/s11060-009-0098-8 pmid:20035366

    CrossRefPubMed
36. 36.↵
    2. Rahman R,
    3. Hamdan A,
    4. Zweifler R, et al

    . Histogram analysis of apparent diffusion coefficient within enhancing and nonenhancing tumor volumes in recurrent glioblastoma patients treated with bevacizumab. J Neurooncol 2014;119:149–58 doi:10.1007/s11060-014-1464-8 pmid:24805151

    CrossRefPubMed
37. 37.↵
    2. Bähr O,
    3. Harter P,
    4. Weise L, et al

    . Sustained focal antitumor activity of bevacizumab in recurrent glioblastoma. Neurology 2014;83:227–34 doi:10.1212/WNL.0000000000000594 pmid:24928118

    Abstract/FREE Full Text
38. 38.↵
    2. Jeyaretna DS,
    3. Curry WT Jr.,
    4. Batchelor TT, et al

    . Exacerbation of cerebral radiation necrosis by bevacizumab. J Clin Oncol 2011;29:e159–62 doi:10.1200/JCO.2010.31.4815 pmid:21149667

    FREE Full Text
39. 39.↵
    2. Rivera AL,
    3. Pelloski CE,
    4. Gilbert MR, et al

    . MGMT promoter methylation is predictive of response to radiotherapy and prognostic in the absence of adjuvant alkylating chemotherapy for glioblastoma. Neuro Oncol 2010;12:116–21 doi:10.1093/neuonc/nop020 pmid:20150378

    Abstract/FREE Full Text