Advertisement

Indications and Limitations of Conventional Imaging – Current Clinical Practice in the Context of Standard Therapy

  • Raymond Y. HuangEmail author
  • Patrick Y. Wen
Chapter

Abstract

Imaging has critical roles in the management of glioma; MRI is routinely performed for initial diagnostic evaluation, preoperative planning, and posttreatment monitoring for tumor recurrence. In this chapter, standard therapy for high- and low-grade gliomas is outlined with emphasis on how imaging contributes to various stages of treatment. Limitations of conventional imaging techniques for these roles are also discussed to highlight the need of developing advanced imaging methods to overcome these limitations.

Keywords

Glioblastoma HGG LGG Pseudoprogression Pseudoresponse MRI RANO 

References

  1. 1.
    Ostrom QT, Gittleman H, Truitt G, Boscia A, Kruchko C, Barnholtz-Sloan JS. CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2011–2015. Neuro-Oncology. 2018;20(suppl_4):iv1–86.PubMedCrossRefPubMedCentralGoogle Scholar
  2. 2.
    Schiff D, Lee EQ, Nayak L, Norden AD, Reardon DA, Wen PY. Medical management of brain tumors and the sequelae of treatment. Neuro-Oncology. 2015;17(4):488–504.PubMedCrossRefPubMedCentralGoogle Scholar
  3. 3.
    Louis D, Ohgaki H, Wiestler O, Cavenee W. WHO classification of tumours of the central nervous system [internet], vol. 1. 4th ed. France: International Agency for Research on Cancer; 2016. [cited 2018 May 9]. Available from: http://publications.iarc.fr/Book-And-Report-Series/Who-Iarc-Classification-Of-Tumours/Who-Classification-Of-Tumours-Of-The-Central-Nervous-System-2016.Google Scholar
  4. 4.
    Wen PY, Kesari S. Malignant Gliomas in adults. N Engl J Med. 2008;359(5):492–507.PubMedCrossRefPubMedCentralGoogle Scholar
  5. 5.
    Wangaryattawanich P, Hatami M, Wang J, Thomas G, Flanders A, Kirby J, et al. Multicenter imaging outcomes study of the cancer genome atlas glioblastoma patient cohort: imaging predictors of overall and progression-free survival. Neuro-Oncology. 2015;17(11):1525–37.PubMedCrossRefPubMedCentralGoogle Scholar
  6. 6.
    Dardis C, Milton K, Ashby L, Shapiro W. Leptomeningeal metastases in high-grade adult glioma: development, diagnosis, management, and outcomes in a series of 34 patients. Front Neurol. 2014;5:220.PubMedCrossRefPubMedCentralGoogle Scholar
  7. 7.
    Kelly PJ, Daumas-Duport C, Kispert DB, Kall BA, Scheithauer BW, Illig JJ. Imaging-based stereotaxic serial biopsies in untreated intracranial glial neoplasms. J Neurosurg. 1987;66(6):865–74.PubMedCrossRefPubMedCentralGoogle Scholar
  8. 8.
    Price SJ, Jena R, Burnet NG, Hutchinson PJ, Dean AF, Peña A, et al. Improved delineation of glioma margins and regions of infiltration with the use of diffusion tensor imaging: an image-guided biopsy study. AJNR Am J Neuroradiol. 2006;27(9):1969–74.PubMedPubMedCentralGoogle Scholar
  9. 9.
    Lacroix M, Abi-Said D, Fourney DR, Gokaslan ZL, Shi W, DeMonte F, et al. A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg. 2001;95(2):190–8.CrossRefGoogle Scholar
  10. 10.
    Ebisu T, Tanaka C, Umeda M, Kitamura M, Naruse S, Higuchi T, et al. Discrimination of brain abscess from necrotic or cystic tumors by diffusion-weighted echo planar imaging. Magn Reson Imaging. 1996;14(9):1113–6.PubMedCrossRefPubMedCentralGoogle Scholar
  11. 11.
    Butler AR, Horii SC, Kricheff II, Shannon MB, Budzilovich GN. Computed tomography in astrocytomas. A statistical analysis of the parameters of malignancy and the positive contrast-enhanced CT scan. Radiology. 1978;129(2):433–9.PubMedCrossRefPubMedCentralGoogle Scholar
  12. 12.
    Burger PC, Heinz ER, Shibata T, Kleihues P. Topographic anatomy and CT correlations in the untreated glioblastoma multiforme. J Neurosurg. 1988;68(5):698–704.PubMedCrossRefPubMedCentralGoogle Scholar
  13. 13.
    Dean BL, Drayer BP, Bird CR, Flom RA, Hodak JA, Coons SW, et al. Gliomas: classification with MR imaging. Radiology. 1990;174(2):411–5.PubMedCrossRefPubMedCentralGoogle Scholar
  14. 14.
    Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJB, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352(10):987–96.CrossRefGoogle Scholar
  15. 15.
    Stupp R, Taillibert S, Kanner A, Read W, Steinberg D, Lhermitte B, et al. Effect of tumor-treating fields plus maintenance temozolomide vs maintenance temozolomide alone on survival in patients with glioblastoma: arandomized clinical trial. JAMA. 2017;318(23):2306–16.PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Bloch O, Han SJ, Cha S, Sun MZ, Aghi MK, McDermott MW, et al. Impact of extent of resection for recurrent glioblastoma on overall survival: clinical article. J Neurosurg. 2012;117(6):1032–8.PubMedCrossRefPubMedCentralGoogle Scholar
  17. 17.
    Ellingson BM, Abrey LE, Nelson SJ, Kaufmann TJ, Garcia J, Chinot O, et al. Validation of postoperative residual contrast-enhancing tumor volume as an independent prognostic factor for overall survival in newly diagnosed glioblastoma. Neuro-Oncology. 2018;20(9):1240–50.PubMedCrossRefPubMedCentralGoogle Scholar
  18. 18.
    Tate MC. Surgery for gliomas. Cancer Treat Res. 2015;163:31–47.PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    Pillai JJ. The evolution of clinical functional imaging during the past 2 decades and its current impact on neurosurgical planning. AJNR Am J Neuroradiol. 2010;31(2):219–25.PubMedCrossRefPubMedCentralGoogle Scholar
  20. 20.
    Hegi ME, Diserens A-C, Gorlia T, Hamou M-F, de Tribolet N, Weller M, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med. 2005;352(10):997–1003.PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    Albert FK, Forsting M, Sartor K, Adams HP, Kunze S. Early postoperative magnetic resonance imaging after resection of malignant glioma: objective evaluation of residual tumor and its influence on regrowth and prognosis. Neurosurgery. 1994;34(1):45–60; discussion 60–61.PubMedPubMedCentralGoogle Scholar
  22. 22.
    Forsting M, Albert FK, Kunze S, Adams HP, Zenner D, Sartor K. Extirpation of glioblastomas: MR and CT follow-up of residual tumor and regrowth patterns. AJNR Am J Neuroradiol. 1993;14(1):77–87.PubMedPubMedCentralGoogle Scholar
  23. 23.
    Bette S, Gempt J, Huber T, Boeckh-Behrens T, Ringel F, Meyer B, et al. Patterns and time dependence of unspecific enhancement in postoperative magnetic resonance imaging after glioblastoma resection. World Neurosurg. 2016;90:440–7.PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    Lescher S, Schniewindt S, Jurcoane A, Senft C, Hattingen E. Time window for postoperative reactive enhancement after resection of brain tumors: less than 72 hours. Neurosurg Focus. 2014;37(6):E3.PubMedCrossRefPubMedCentralGoogle Scholar
  25. 25.
    Vogelbaum MA, Jost S, Aghi MK, Heimberger AB, Sampson JH, Wen PY, et al. Application of novel response/progression measures for surgically delivered therapies for gliomas: Response Assessment in Neuro-Oncology (RANO) Working Group. Neurosurgery. 2012;70(1):234–43; discussion 243–4.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Quigley MR. Early postoperative magnetic resonance imaging after resection of malignant glioma: objective evaluation of residual tumor and influence on regrowth and prognosis. Neurosurgery. 1994;34(6):1105.PubMedPubMedCentralGoogle Scholar
  27. 27.
    Nabors LB, Portnow J, Ammirati M, Baehring J, Brem H, Butowski N, et al. NCCN guidelines insights: central nervous system cancers, version 1.2017. J Natl Compr Cancer Netw. 2017;15(11):1331–45.CrossRefGoogle Scholar
  28. 28.
    Macdonald DR, Cascino TL, Schold SC Jr, Cairncross JG. Response criteria for phase II studies of supratentorial malignant glioma. J Clin Oncol. 1990;8(7):1277–80.PubMedCrossRefPubMedCentralGoogle Scholar
  29. 29.
    Han K, Ren M, Wick W, Abrey L, Das A, Jin J, et al. Progression-free survival as a surrogate endpoint for overall survival in glioblastoma: a literature-based meta-analysis from 91 trials. Neuro-Oncology. 2014;16(5):696–706.PubMedCrossRefPubMedCentralGoogle Scholar
  30. 30.
    Wen PY, Macdonald DR, Reardon DA, Cloughesy TF, Sorensen AG, Galanis E, et al. Updated response assessment criteria for high-grade gliomas: response assessment in neuro-oncology working group. J Clin Oncol. 2010;28(11):1963–72.PubMedCrossRefPubMedCentralGoogle Scholar
  31. 31.
    Wick W, Chinot OL, Bendszus M, Mason W, Henriksson R, Saran F, et al. Evaluation of pseudoprogression rates and tumor progression patterns in a phase III trial of bevacizumab plus radiotherapy/temozolomide for newly diagnosed glioblastoma. Neuro-Oncology. 2016;18(10):1434–41.PubMedCrossRefPubMedCentralGoogle Scholar
  32. 32.
    Brandsma D, Stalpers L, Taal W, Sminia P, van den Bent MJ. Clinical features, mechanisms, and management of pseudoprogression in malignant gliomas. Lancet Oncol. 2008;9(5):453–61.PubMedCrossRefGoogle Scholar
  33. 33.
    Valtonen S, Timonen U, Toivanen P, Kalimo H, Kivipelto L, Heiskanen O, et al. Interstitial chemotherapy with carmustine-loaded polymers for high-grade gliomas: a randomized double-blind study. Neurosurgery. 1997;41(1):44–8; discussion 48–9.PubMedCrossRefPubMedCentralGoogle Scholar
  34. 34.
    Radbruch A, Fladt J, Kickingereder P, Wiestler B, Nowosielski M, Bäumer P, et al. Pseudoprogression in patients with glioblastoma: clinical relevance despite low incidence. Neuro-Oncology. 2015;17(1):151–9.PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Linhares P, Carvalho B, Figueiredo R, Reis RM, Vaz R. Early pseudoprogression following chemoradiotherapy in glioblastoma patients: the value of RANO evaluation. J Oncol. 2013;2013:690585.PubMedCrossRefPubMedCentralGoogle Scholar
  36. 36.
    Young RJ, Gupta A, Shah AD, Graber JJ, Zhang Z, Shi W, et al. Potential utility of conventional MRI signs in diagnosing pseudoprogression in glioblastoma. Neurology. 2011;76(22):1918–24.PubMedCrossRefPubMedCentralGoogle Scholar
  37. 37.
    Yoo R-E, Choi SH, Kim TM, Lee S-H, Park C-K, Park S-H, et al. Independent poor prognostic factors for true progression after radiation therapy and concomitant temozolomide in patients with glioblastoma: subependymal enhancement and low ADC value. AJNR Am J Neuroradiol. 2015;36(10):1846–52.PubMedCrossRefPubMedCentralGoogle Scholar
  38. 38.
    Weller M, Cloughesy T, Perry JR, Wick W. Standards of care for treatment of recurrent glioblastoma–are we there yet? Neuro-Oncology. 2013;15(1):4–27.PubMedCrossRefPubMedCentralGoogle Scholar
  39. 39.
    Friedman HS, Prados MD, Wen PY, Mikkelsen T, Schiff D, Abrey LE, et al. Bevacizumab alone and in combination with irinotecan in recurrent glioblastoma. J Clin Oncol. 2009;27(28):4733–40.PubMedCrossRefPubMedCentralGoogle Scholar
  40. 40.
    Kreisl TN, Kim L, Moore K, Duic P, Royce C, Stroud I, et al. Phase II trial of single-agent bevacizumab followed by bevacizumab plus irinotecan at tumor progression in recurrent glioblastoma. J Clin Oncol. 2009;27(5):740–5.PubMedCrossRefPubMedCentralGoogle Scholar
  41. 41.
    Gilbert MR, Dignam JJ, Armstrong TS, Wefel JS, Blumenthal DT, Vogelbaum MA, et al. A randomized trial of bevacizumab for newly diagnosed glioblastoma. N Engl J Med. 2014;370(8):699–708.PubMedCrossRefPubMedCentralGoogle Scholar
  42. 42.
    Chinot OL, Wick W, Mason W, Henriksson R, Saran F, Nishikawa R, et al. Bevacizumab plus radiotherapy-temozolomide for newly diagnosed glioblastoma. N Engl J Med. 2014;370(8):709–22.CrossRefGoogle Scholar
  43. 43.
    Batchelor TT, Duda DG, di Tomaso E, Ancukiewicz M, Plotkin SR, Gerstner E, et al. Phase II study of cediranib, an oral pan-vascular endothelial growth factor receptor tyrosine kinase inhibitor, in patients with recurrent glioblastoma. J Clin Oncol. 2010;28(17):2817–23.PubMedCrossRefPubMedCentralGoogle Scholar
  44. 44.
    Batchelor TT, Sorensen AG, di Tomaso E, Zhang W-T, Duda DG, Cohen KS, et al. AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell. 2007;11(1):83–95.PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Norden AD, Drappatz J, Muzikansky A, David K, Gerard M, McNamara MB, et al. An exploratory survival analysis of anti-angiogenic therapy for recurrent malignant glioma. J Neuro-Oncol. 2009;92(2):149–55.CrossRefGoogle Scholar
  46. 46.
    Huang RY, Rahman R, Ballman KV, Felten S, Anderson K, Ellingson BM, et al. The impact of T2/FLAIR evaluation per RANO criteria on response assessment of recurrent glioblastoma patients treated with bevacizumab. Clin Cancer Res. 2015;22(3):575–81.PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    Radbruch A, Lutz K, Wiestler B, Bäumer P, Heiland S, Wick W, et al. Relevance of T2 signal changes in the assessment of progression of glioblastoma according to the response assessment in neurooncology criteria. Neuro-Oncology. 2012;14(2):222–9.PubMedCrossRefGoogle Scholar
  48. 48.
    Nowosielski M, Ellingson BM, Chinot OL, Garcia J, Revil C, Radbruch A, et al. Radiologic progression of glioblastoma under therapy – an exploratory analysis of AVAglio. NeuroOncol. 2017;20(4):557–66.Google Scholar
  49. 49.
    Nowosielski M, Wiestler B, Goebel G, Hutterer M, Schlemmer HP, Stockhammer G, et al. Progression types after antiangiogenic therapy are related to outcome in recurrent glioblastoma. Neurology. 2014;82(19):1684–92.PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    Cachia D, Elshafeey NA, Kamiya-Matsuoka C, Hatami M, Alfaro-Munoz KD, Mandel JJ, et al. Radiographic patterns of progression with associated outcomes after bevacizumab therapy in glioblastoma patients. J Neurooncol. 2017;135(1):75–81.PubMedCrossRefPubMedCentralGoogle Scholar
  51. 51.
    Gahrmann R, van den Bent M, van der Holt B, Vernhout RM, Taal W, Vos M, et al. Comparison of 2D (RANO) and volumetric methods for assessment of recurrent glioblastoma treated with bevacizumab-a report from the BELOB trial. Neuro-Oncology. 2017;19(6):853–61.PubMedCrossRefPubMedCentralGoogle Scholar
  52. 52.
    Buckner JC, Shaw EG, Pugh SL, Chakravarti A, Gilbert MR, Barger GR, et al. Radiation plus Procarbazine, CCNU, and vincristine in low-grade Glioma. N Engl J Med. 2016;374(14):1344–55.PubMedCrossRefPubMedCentralGoogle Scholar
  53. 53.
    Smith JS, Chang EF, Lamborn KR, Chang SM, Prados MD, Cha S, et al. Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J Clin Oncol. 2008;26(8):1338–45.PubMedCrossRefPubMedCentralGoogle Scholar
  54. 54.
    McGirt MJ, Chaichana KL, Attenello FJ, Weingart JD, Than K, Burger PC, et al. Extent of surgical resection is independently associated with survival in patients with hemispheric infiltrating low-grade gliomas. Neurosurgery. 2008;63(4):700–7; author reply 707–8.PubMedCrossRefPubMedCentralGoogle Scholar
  55. 55.
    Wijnenga MMJ, French PJ, Dubbink HJ, Dinjens WNM, Atmodimedjo PN, Kros JM, et al. The impact of surgery in molecularly defined low-grade glioma: an integrated clinical, radiological, and molecular analysis. Neuro-Oncology. 2018;20(1):103–12.PubMedCrossRefPubMedCentralGoogle Scholar
  56. 56.
    Beiko J, Suki D, Hess KR, Fox BD, Cheung V, Cabral M, et al. IDH1 mutant malignant astrocytomas are more amenable to surgical resection and have a survival benefit associated with maximal surgical resection. Neuro-Oncology. 2014;16(1):81–91.PubMedCrossRefPubMedCentralGoogle Scholar
  57. 57.
    Kawaguchi T, Sonoda Y, Shibahara I, Saito R, Kanamori M, Kumabe T, et al. Impact of gross total resection in patients with WHO grade III glioma harboring the IDH 1/2 mutation without the 1p/19q co-deletion. J Neuro-Oncol. 2016;129(3):505–14.CrossRefGoogle Scholar
  58. 58.
    Claus EB, Horlacher A, Hsu L, Schwartz RB, Dello-Iacono D, Talos F, et al. Survival rates in patients with low-grade glioma after intraoperative magnetic resonance image guidance. Cancer. 2005;103(6):1227–33.PubMedCrossRefPubMedCentralGoogle Scholar
  59. 59.
    Ius T, Isola M, Budai R, Pauletto G, Tomasino B, Fadiga L, et al. Low-grade glioma surgery in eloquent areas: volumetric analysis of extent of resection and its impact on overall survival. A single-institution experience in 190 patients. J Neurosurg. 2012;117(6):1039–52.PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Krishnan R, Raabe A, Hattingen E, Szelényi A, Yahya H, Hermann E, et al. Functional magnetic resonance imaging-integrated neuronavigation: correlation between lesion-to-motor cortex distance and outcome. Neurosurgery. 2004;55(4):904–14; discusssion 914–5.PubMedCrossRefPubMedCentralGoogle Scholar
  61. 61.
    Nimsky C, Fujita A, Ganslandt O, Von Keller B, Fahlbusch R. Volumetric assessment of glioma removal by intraoperative high-field magnetic resonance imaging. Neurosurgery. 2004;55(2):358–70; discussion 370–1.PubMedCrossRefPubMedCentralGoogle Scholar
  62. 62.
    Duffau H. Mapping the connectome in awake surgery for gliomas: an update. J Neurosurg Sci. 2017;61(6):612–30.PubMedPubMedCentralGoogle Scholar
  63. 63.
    Shaw EG, Berkey B, Coons SW, Bullard D, Brachman D, Buckner JC, et al. Recurrence following neurosurgeon-determined gross-total resection of adult supratentorial low-grade glioma: results of a prospective clinical trial. J Neurosurg. 2008;109(5):835–41.PubMedCrossRefPubMedCentralGoogle Scholar
  64. 64.
    van den Bent MJ, Afra D, de Witte O, Ben Hassel M, Schraub S, Hoang-Xuan K, et al. Long-term efficacy of early versus delayed radiotherapy for low-grade astrocytoma and oligodendroglioma in adults: the EORTC 22845 randomised trial. Lancet. 2005;366(9490):985–90.PubMedCrossRefPubMedCentralGoogle Scholar
  65. 65.
    Karim ABMF, Afra D, Cornu P, Bleehan N, Schraub S, De Witte O, et al. Randomized trial on the efficacy of radiotherapy for cerebral low-grade glioma in the adult: European Organization for Research and Treatment of Cancer Study 22845 with the Medical Research Council study BRO4: an interim analysis. Int J Radiat Oncol Biol Phys. 2002;52(2):316–24.PubMedCrossRefPubMedCentralGoogle Scholar
  66. 66.
    Mandonnet E, Delattre J-Y, Tanguy M-L, Swanson KR, Carpentier AF, Duffau H, et al. Continuous growth of mean tumor diameter in a subset of grade II gliomas. Ann Neurol. 2003;53(4):524–8.PubMedCrossRefPubMedCentralGoogle Scholar
  67. 67.
    Rees J, Watt H, Jäger HR, Benton C, Tozer D, Tofts P, et al. Volumes and growth rates of untreated adult low-grade gliomas indicate risk of early malignant transformation. Eur J Radiol. 2009;72(1):54–64.PubMedCrossRefPubMedCentralGoogle Scholar
  68. 68.
    van den Bent MJ, Wefel JS, Schiff D, Taphoorn MJB, Jaeckle K, Junck L, et al. Response assessment in neuro-oncology (a report of the RANO group): assessment of outcome in trials of diffuse low-grade gliomas. Lancet Oncol. 2011;12(6):583–93.PubMedCrossRefPubMedCentralGoogle Scholar
  69. 69.
    White ML, Zhang Y, Kirby P, Ryken TC. Can tumor contrast enhancement be used as a criterion for differentiating tumor grades of oligodendrogliomas? AJNR Am J Neuroradiol. 2005;26(4):784–90.PubMedPubMedCentralGoogle Scholar
  70. 70.
    Brasil Caseiras G, Ciccarelli O, Altmann DR, Benton CE, Tozer DJ, Tofts PS, et al. Low-grade gliomas: six-month tumor growth predicts patient outcome better than admission tumor volume, relative cerebral blood volume, and apparent diffusion coefficient. Radiology. 2009;253(2):505–12.PubMedCrossRefPubMedCentralGoogle Scholar
  71. 71.
    Hlaihel C, Guilloton L, Guyotat J, Streichenberger N, Honnorat J, Cotton F. Predictive value of multimodality MRI using conventional, perfusion, and spectroscopy MR in anaplastic transformation of low-grade oligodendrogliomas. J Neuro-Oncol. 2010;97(1):73–80.CrossRefGoogle Scholar
  72. 72.
    Provenzale JM, Ison C, Delong D. Bidimensional measurements in brain tumors: assessment of interobserver variability. AJR Am J Roentgenol. 2009;193(6):W515–22.PubMedCrossRefGoogle Scholar
  73. 73.
    Provenzale JM, Mancini MC. Assessment of intra-observer variability in measurement of high-grade brain tumors. J Neuro-Oncol. 2012;108(3):477–83.CrossRefGoogle Scholar
  74. 74.
    Ertl-Wagner BB, Blume JD, Peck D, Udupa JK, Herman B, Levering A, et al. Reliability of tumor volume estimation from MR images in patients with malignant glioma. Results from the American College of Radiology Imaging Network (ACRIN) 6662 Trial. Eur Radiol. 2009;19(3):599–609.PubMedCrossRefPubMedCentralGoogle Scholar
  75. 75.
    van den Bent MJ, Baumert B, Erridge SC, Vogelbaum MA, Nowak AK, Sanson M, et al. Interim results from the CATNON trial (EORTC study 26053-22054) of treatment with concurrent and adjuvant temozolomide for 1p/19q non-co-deleted anaplastic glioma: a phase 3, randomised, open-label intergroup study. Lancet. 2017;390(10103):1645–53.PubMedCrossRefPubMedCentralGoogle Scholar
  76. 76.
    Naftel RP, Pollack IF, Zuccoli G, Deutsch M, Jakacki RI. Pseudoprogression of low-grade gliomas after radiotherapy. Pediatr Blood Cancer. 2015;62(1):35–9.PubMedCrossRefPubMedCentralGoogle Scholar
  77. 77.
    van West SE, de Bruin HG, van de Langerijt B, Swaak-Kragten AT, van den Bent MJ, Taal W. Incidence of pseudoprogression in low-grade gliomas treated with radiotherapy. Neuro-Oncology. 2017;19(5):719–25.PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Department of RadiologyBrigham and Women’s HospitalBostonUSA
  2. 2.Dana-Farber Cancer InstituteBostonUSA

Personalised recommendations