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Treatment-related changes in glioblastoma: a review on the controversies in response assessment criteria and the concepts of true progression, pseudoprogression, pseudoresponse and radionecrosis

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Abstract

The assessment of response to therapy in glioblastoma remains a challenge, because the surrogate measures of survival are subject to radiographic misinterpretation. A solid and reliable definition of progression is needed for both clinical decision-making and for evaluating response within the clinical trials. Historically, assessment criteria have used radiologic and clinical features aimed to correctly classify patients into progressive or non-progressive disease. The widely used RANO criteria are a valuable tool in disease evaluation, both in the clinical setting and in the clinical trials. However, assessment criteria have certain limitations that emerging image techniques have tried to overcome. Differentiating true progression from treatment-related changes (like pseudoprogression or pseudoresponse) is crucial in order not to prematurely discontinue adjuvant chemotherapy or redirect the patient to second-line options. This fact underscores the need for advanced radiologic techniques, like specific diffusion and perfusion MRI sequences, MR spectroscopy and PET, which seem to play a role in distinguishing these phenomena.

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References

  1. Wen PY, Kesari S. Malignant gliomas in adults. N Engl J Med. 2008;359(5):492–507.

    Article  PubMed  CAS  Google Scholar 

  2. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, 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;5:459–66.

    Article  CAS  Google Scholar 

  3. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352(10):987–96.

    Article  PubMed  CAS  Google Scholar 

  4. Ellingson BM, Wen PY, Cloughesy TF. Modified criteria for radiographic response assessment in glioblastoma clinical trials. Neurotherapeutics. 2017;14(2):307–20.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Chinot OL, Macdonald DR, Abrey LE, Zahlmann G, Kerloëguen Y, Cloughesy TF. Response assessment criteria for glioblastoma: practical adaptation and implementation in clinical trials of antiangiogenic therapy. Curr Neurol Neurosci Rep. 2013;13(5):347.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Lamborn KR, Yung WK, Chang SM, Wen PY, Cloughesy TF, DeAngelis LM, et al. Progression-free survival: an important end point in evaluating therapy for recurrent high-grade gliomas. Neuro Oncol. 2008;10(2):162–70.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Provenzale JM, Ison C, Delong D. Bidimensional measurements in brain tumors: assessment of interobserver variability. AJR Am J Roentgenol. 2009;193(6):W515–22.

    Article  PubMed  Google Scholar 

  8. 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 neurooncology working group. J Clin Oncol. 2010;28(11):1963–72.

    Article  PubMed  Google Scholar 

  9. Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, et al. The 2016 World Health Organization classification of tumors of the central nervous system: a summary. Acta Neuropathol. 2016;131(6):803–20.

    Article  PubMed  Google Scholar 

  10. Reardon DA, Ballman KV, Buckner JC, Chang SM, Ellingson BM. Impact of imaging measurements on response assessment in glioblastoma clinical trials. Neuro Oncol. 2014;16 suppl 7:Vii24–35.

    Article  PubMed  CAS  Google Scholar 

  11. Hygino da Cruz LC Jr, Rodriguez I, Domingues RC, Gasparetto EL, Sorensen AG. Pseudoprogression and pseudoresponse: imaging challenges in the assessment of posttreatment glioma. AJNR Am J Neuroradiol. 2011;32(11):1978–85.

    Article  PubMed  Google Scholar 

  12. Chang JH, Kim CY, Choi BS, Kim YJ, Kim JS, Kim IA. Pseudoprogression and pseudoresponse in the management of high-grade glioma : optimal decision timing according to the response assessment of the neuro-oncology working group. J Korean Neurosurg Soc. 2014;55(1):5–11.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Huang RY, Neagu MR, Reardon DA, Wen PY. Pitfalls in the neuroimaging of glioblastoma in the era of antiangiogenic and immuno/targeted therapy—detecting illusive disease, defining response. Front Neurol. 2015;6:33.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Parvez K, Parvez A, Zadeh G. The diagnosis and treatment of pseudoprogression, radiation necrosis and brain tumor recurrence. Int J Mol Sci. 2014;15(7):11832–46.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Yoo RE, Choi SH. Recent application of advanced MR imaging to predict pseudoprogression in high-grade glioma patients. Magn Reson Med Sci. 2016;15(2):165–77.

    Article  PubMed  Google Scholar 

  16. Khan MN, Sharma AM, Pitz M, Loewen SK, Quon H, Poulin A, et al. High-grade glioma management and response assessment-recent advances and current challenges. Curr Oncol. 2016;23(4):e383–91.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Wick W, Platten M, Meisner C, Felsberg J, Tabatabai G, Simon M, et al. Temozolomide chemotherapy alone versus radiotherapy alone for malignant astrocytoma in the elderly: the NOA-08 randomised, phase 3 trial. Lancet Oncol. 2012;13(7):707–15.

    Article  PubMed  CAS  Google Scholar 

  18. Roa W, Brasher PM, Bauman G, Anthes M, Bruera E, Chan A, et al. Abbreviated course of radiation therapy in older patients with glioblastoma multiforme: a prospective randomized clinical trial. J Clin Oncol. 2004;22(9):1583–8.

    Article  PubMed  CAS  Google Scholar 

  19. Vredenburgh JJ, Desjardins A, Herndon JE 2nd, Marcello J, Reardon DA, Quinn JA, et al. Bevacizumab plus irinotecan in recurrent glioblastoma multiforme. J Clin Oncol. 2007;25(30):4722–9.

    Article  PubMed  CAS  Google Scholar 

  20. Malmström A, Grønberg BH, Marosi C, Stupp R, Frappaz D, Schultz H, et al. Temozolomide versus standard 6-week radiotherapy versus hypofractionated radiotherapy in patients older than 60 years with glioblastoma: the Nordic randomised, phase 3 trial. Lancet Oncol. 2012;13(9):916–26.

    Article  PubMed  CAS  Google Scholar 

  21. Gilbert MR, Wang M, Aldape KD, Stupp R, Hegi ME, Jaeckle KA, et al. Dose-dense temozolomide for newly diagnosed glioblastoma: a randomized phase III clinical trial. J Clin Oncol. 2013;31(32):4085–91.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. 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.

    Article  PubMed  CAS  Google Scholar 

  23. Roa W, Kepka L, Kumar N, Sinaika V, Matiello J, Lomidze D, et al. International atomic energy agency randomized phase III study of radiation therapy in elderly and/or frail patients with newly diagnosed glioblastoma multiforme. J Clin Oncol. 2015;33(35):4145–50.

    Article  PubMed  Google Scholar 

  24. Provenzale JM, Mancini MC. Assessment of intra-observer variability in measurement of high-grade brain tumors. J Neurooncol. 2012;108(3):477–83.

    Article  PubMed  Google Scholar 

  25. Levin VA, Crafts DC, Norman DM, Hoffer PB, Spire JP, Wilson CB. Criteria for evaluating patients undergoing chemotherapy for malignant brain tumors. J Neurosurg. 1977;47(3):329–35.

    Article  PubMed  CAS  Google Scholar 

  26. Miller AB, Hoogstraten B, Staquet M, Winkler A. Reporting results of cancer treatment. Cancer. 1981;47(1):207–14.

    Article  PubMed  CAS  Google Scholar 

  27. Quant EC, Wen PY. Response assessment in neuro-oncology. Curr Oncol Rep. 2011;13(1):50–6. https://doi.org/10.1007/s11912-010-0143-y.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  29. Cairncross JG, Pexman JH, Rathbone MP, DelMaestro RF. Postoperative contrast enhancement in patients with brain tumor. Ann Neurol. 1985;17(6):570–2.

    Article  PubMed  CAS  Google Scholar 

  30. Brandsma D, van den Bent MJ. Pseudoprogression and pseudoresponse in the treatment of gliomas. Curr Opin Neurol. 2009;22(6):633–8.

    Article  PubMed  Google Scholar 

  31. 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.

    Article  PubMed  CAS  Google Scholar 

  32. 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.

    Article  PubMed  CAS  Google Scholar 

  33. Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer. 2009;45(2):228–47.

    Article  PubMed  CAS  Google Scholar 

  34. Therasse P, Arbuck SG, Eisenhauer EA, Wanders J, Kaplan RS, Rubinstein L, et al. New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. J Natl Cancer Inst. 2000;92(3):205–16.

    Article  PubMed  CAS  Google Scholar 

  35. Gállego Pérez-Larraya J, Lahutte M, Petrirena G, Reyes-Botero G, González-Aguilar A, Houillier C, et al. Response assessment in recurrent glioblastoma treated with irinotecan-bevacizumab: comparative analysis of the Macdonald, RECIST, RANO, and RECIST + F criteria. Neuro Oncol. 2012;14(5):667–73.

    Article  PubMed  CAS  Google Scholar 

  36. Galanis E, Buckner JC, Maurer MJ, Sykora R, Castillo R, Ballman KV, et al. Validation of neuroradiologic response assessment in gliomas: measurement by RECIST, two-dimensional, computer-assisted tumor area, and computer-assisted tumor volume methods. Neuro Oncol. 2006;8(2):156–65.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Okada H, Weller M, Huang R, Finocchiaro G, Gilbert MR, et al. Immunotherapy response assessment in neurooncology: a report of the RANO working group. Lancet Oncol. 2015;16(15):e534–42.

    Article  PubMed  PubMed Central  Google Scholar 

  38. NCCN Guidelines. https://www.nccn.org/professionals/physician_gls/f_guidelines.asp#cns. Accessed 13 Sept 2017.

  39. Ellingson BM, Bendszus M, Boxerman J, Barboriak D, Erickson BJ, Smits M, et al. Consensus recommendations for a standardized brain tumor imaging protocol in clinical trials. Neuro Oncol. 2015;17(9):1188–98.

    PubMed  PubMed Central  Google Scholar 

  40. 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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Weller M, Yung WK. Angiogenesis inhibition for glioblastoma at the edge: beyond AVAGlio and RTOG 0825. Neuro Oncol. 2013;15(8):971.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Ellingson BM, Harris RJ, Woodworth DC, Leu K, Zaw O, Mason WP, et al. Baseline pretreatment contrast enhancing tumor volume including central necrosis is a prognostic factor in recurrent glioblastoma: evidence from single and multicenter trials. Neuro Oncol. 2017;19(1):89–98.

    Article  PubMed  Google Scholar 

  44. Minaya P, Baumstarck K, Berbis J, Goncalves A, Barlesi F, Michel G, et al. The caregiver oncology quality of life questionnaire (CarGOQoL): development and validation of an instrument to measure the quality of life of the caregivers of patients with cancer. Eur J Cancer. 2012;48(6):904–11.

    Article  PubMed  Google Scholar 

  45. Kumar AJ, Leeds NE, Fuller GN, Van Tassel P, Maor MH, Sawaya RE, et al. Malignant gliomas: MR imaging spectrum of radiation therapy- and chemotherapy-induced necrosis of the brain after treatment. Radiology. 2000;217(2):377–84.

    Article  PubMed  CAS  Google Scholar 

  46. Miyatake S, Nonoguchi N, Furuse M, Yoritsune E, Miyata T, Kawabata S, et al. Pathophysiology, diagnosis, and treatment of radiation necrosis in the brain. Neurol Med Chir (Tokyo). 2015;55(1):50–9.

    Article  PubMed  Google Scholar 

  47. Shaw PJ, Bates D. Conservative treatment of delayed cerebral radiation necrosis. J Neurol Neurosurg Psychiatry. 1984;47(12):1338–41.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Levin VA, Bidaut L, Hou P, Kumar AJ, Wefel JS, Bekele BN, et al. Randomized double-blind placebo-controlled trial of bevacizumab therapy for radiation necrosis of the central nervous system. Int J Radiat Oncol Biol Phys. 2011;79(5):1487–95.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Delishaj D, Ursino S, Pasqualetti F, Cristaudo A, Cosottini M, Fabrini MG, et al. Bevacizumab for the treatment of radiation-induced cerebral necrosis: a systematic review of the literature. J Clin Med Res. 2017;9(4):273–80.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Furuse M, Nonoguchi N, Kuroiwa T, Miyamoto S, Arakawa Y, Shinoda J, et al. A prospective, multicentre, single-arm clinical trial of bevacizumab for patients with surgically untreatable, symptomatic brain radiation necrosis. Neurooncol Pract. 2016;3(4):272–80.

    PubMed  PubMed Central  Google Scholar 

  51. Siu A, Wind JJ, Iorgulescu JB, Chan TA, Yamada Y, Sherman JH. Radiation necrosis following treatment of high grade glioma–a review of the literature and current understanding. Acta Neurochir (Wien). 2012;154(2):191–201.

    Article  PubMed  Google Scholar 

  52. Happold C, Ernemann U, Roth P, Wick W, Weller M, Schmidt F. Anticoagulation for radiation-induced neurotoxicity revisited. J Neurooncol. 2008;90(3):357–62.

    Article  PubMed  Google Scholar 

  53. Kohshi K, Imada H, Nomoto S, Yamaguchi R, Abe H, Yamamoto H. Successful treatment of radiation-induced brain necrosis by hyperbaric oxygen therapy. J Neurol Sci. 2003;209(1–2):115–7.

    Article  PubMed  Google Scholar 

  54. Rahmathulla G, Recinos PF, Valerio JE, Chao S, Barnett GH. Laser interstitial thermal therapy for focal cerebral radiation necrosis: a case report and literature review. Stereotact Funct Neurosurg. 2012;90(3):192–200.

    Article  PubMed  Google Scholar 

  55. Williamson R, Kondziolka D, Kanaan H, Lunsford LD, Flickinger JC. Adverse radiation effects after radiosurgery may benefit from oral vitamin E and pentoxifylline therapy: a pilot study. Stereotact Funct Neurosurg. 2008;86(6):359–66.

    Article  PubMed  Google Scholar 

  56. 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.

    Article  PubMed  Google Scholar 

  57. Chaskis C, Neyns B, Michotte A, De Ridder M, Everaert H. Pseudoprogression after radiotherapy with concurrent temozolomide for high-grade glioma: clinical observations and working recommendations. Surg Neurol. 2009;72(4):423–8.

    Article  PubMed  Google Scholar 

  58. Taal W, Brandsma D, de Bruin HG, Bromberg JE, Swaak-Kragten AT, Smitt PA, et al. Incidence of early pseudo-progression in a cohort of malignant glioma patients treated with chemoirradiation with temozolomide. Cancer. 2008;113(2):405–10.

    Article  PubMed  CAS  Google Scholar 

  59. Pouleau HB, Sadeghi N, Balériaux D, Mélot C, De Witte O, Lefranc F. High levels of cellular proliferation predict pseudoprogression in glioblastoma patients. Int J Oncol. 2012;40(4):923–8.

    Article  PubMed  Google Scholar 

  60. Gahramanov S, Raslan AM, Muldoon LL, Hamilton BE, Rooney WD, Varallyay CG, et al. Potential for differentiation of pseudoprogression from true tumor progression with dynamic susceptibility-weighted contrast-enhanced magnetic resonance imaging using ferumoxytol vs. gadoteridol: a pilot study. Int J Radiat Oncol Biol Phys. 2011;79(2):514–23.

    Article  PubMed  Google Scholar 

  61. Brandes AA, Franceschi E, Tosoni A, Blatt V, Pession A, Tallini G, et al. MGMT promoter methylation status can predict the incidence and outcome of pseudoprogression after concomitant radiochemotherapy in newly diagnosed glioblastoma patients. J Clin Oncol. 2008;26(13):2192–7.

    Article  PubMed  Google Scholar 

  62. Ulmer S, Spalek K, Nabavi A, Schultka S, Mehdorn HM, Kesari S, et al. Temporal changes in magnetic resonance imaging characteristics of Gliadel wafers and of the adjacent brain parenchyma. Neuro Oncol. 2012;14(4):482–90.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Colen RR, Zinn PO, Hazany S, Do-Dai D, Wu JK, Yao K, et al. Magnetic resonance imaging appearance and changes on intracavitary Gliadel wafer placement: a pilot study. World J Radiol. 2011;3(11):266–72.

    Article  PubMed  PubMed Central  Google Scholar 

  64. 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 Oncol. 2016;18(10):1434–41.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. Batchelor TT, Sorensen AG, di Tomaso E, Zhang WT, 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. 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 Neurooncol. 2009;92(2):149–55.

    Article  PubMed  CAS  Google Scholar 

  67. Sorensen AG, Batchelor TT, Zhang WT, Chen PJ, Yeo P, Wang M, et al. A “vascular normalization index” as potential mechanistic biomarker to predict survival after a single dose of cediranib in recurrent glioblastoma patients. Cancer Res. 2009;69(13):5296–300.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  68. Lescher S, Jurcoane A, Veit A, Bähr O, Deichmann R, Hattingen E. Quantitative T1 and T2 mapping in recurrent glioblastomas under bevacizumab: earlier detection of tumor progression compared to conventional MRI. Neuroradiology. 2015;57(1):11–20.

    Article  PubMed  Google Scholar 

  69. Ellingson BM, Kim HJ, Woodworth DC, Pope WB, Cloughesy JN, Harris RJ, et al. Recurrent glioblastoma treated with bevacizumab: contrast-enhanced T1-weighted subtraction maps improve tumor delineation and aid prediction of survival in a multicenter clinical trial. Radiology. 2014;271(1):200–10.

    Article  PubMed  Google Scholar 

  70. Mascalchi M, Filippi M, Floris R, Fonda C, Gasparotti R, Villari N. Diffusion-weighted MR of the brain: methodology and clinical application. Radiol Med. 2005;109(3):155–97.

    PubMed  Google Scholar 

  71. Hein PA, Eskey CJ, Dunn JF, Hug EB. Diffusion-weighted imaging in the follow-up of treated high-grade gliomas: tumor recurrence versus radiation injury. AJNR Am J Neuroradiol. 2004;25(2):201–9.

    PubMed  Google Scholar 

  72. Asao C, Korogi Y, Kitajima M, Hirai T, Baba Y, Makino K, et al. Diffusion-weighted imaging of radiation-induced brain injury for differentiation from tumor recurrence. AJNR Am J Neuroradiol. 2005;26(6):1455–60.

    PubMed  Google Scholar 

  73. Song YS, Choi SH, Park CK, Yi KS, Lee WJ, Yun TJ, et al. True progression versus pseudoprogression in the treatment of glioblastomas: a comparison study of normalized cerebral blood volume and apparent diffusion coefficient by histogram analysis. Korean J Radiol. 2013;14(4):662–72.

    Article  PubMed  PubMed Central  Google Scholar 

  74. Chu HH, Choi SH, Ryoo I, Kim SC, Yeom JA, Shin H, et al. Differentiation of true progression from pseudoprogression in glioblastoma treated with radiation therapy and concomitant temozolomide: comparison study of standard and high-b-value diffusion-weighted imaging. Radiology. 2013;269(3):831–40.

    Article  PubMed  Google Scholar 

  75. Boxerman JL, Ellingson BM, Jeyapalan S, Elinzano H, Harris RJ, Rogg JM, et al. Longitudinal DSC-MRI for distinguishing tumor recurrence from pseudoprogression in patients with a high-grade glioma. Am J Clin Oncol. 2017;40(3):228–34.

    Article  PubMed  CAS  Google Scholar 

  76. Hu LS, Eschbacher JM, Heiserman JE, Dueck AC, Shapiro WR, Liu S, et al. Reevaluating the imaging definition of tumor progression: perfusion MRI quantifies recurrent glioblastoma tumor fraction, pseudoprogression, and radiation necrosis to predict survival. Neuro Oncol. 2012;14(7):919–30.

    Article  PubMed  PubMed Central  Google Scholar 

  77. Mangla R, Kolar B, Zhu T, Zhong J, Almast J, Ekholm S. Percentage signal recovery derived from MR dynamic susceptibility contrast imaging is useful to differentiate common enhancing malignant lesions of the brain. AJNR Am J Neuroradiol. 2011;32(6):1004–10.

    Article  PubMed  CAS  Google Scholar 

  78. Hilario A, Sepulveda JM, Hernandez-Lain A, Salvador E, Koren L, Manneh R, et al. Leakage decrease detected by dynamic susceptibility-weighted contrast-enhanced perfusion MRI predicts survival in recurrent glioblastoma treated with bevacizumab. Clin Transl Oncol. 2017;19(1):51–7.

    Article  PubMed  CAS  Google Scholar 

  79. Yun TJ, Park CK, Kim TM, Lee SH, Kim JH, Sohn CH, et al. Glioblastoma treated with concurrent radiation therapy and temozolomide chemotherapy: differentiation of true progression from pseudoprogression with quantitative dynamic contrast-enhanced MR imaging. Radiology. 2015;274(3):830–40.

    Article  PubMed  Google Scholar 

  80. Cha J, Kim ST, Kim HJ, Kim BJ, Kim YK, Lee JY, et al. Differentiation of tumor progression from pseudoprogression in patients with posttreatment glioblastoma using multiparametric histogram analysis. AJNR Am J Neuroradiol. 2014;35(7):1309–17.

    Article  PubMed  CAS  Google Scholar 

  81. Galldiks N, Dunkl V, Stoffels G, Hutterer M, Rapp M, Sabel M, et al. Diagnosis of pseudoprogression in patients with glioblastoma using O-(2-[18F] fluoroethyl)-l-tyrosine PET. Eur J Nucl Med Mol Imaging. 2015;42(5):685–95.

    Article  PubMed  CAS  Google Scholar 

  82. Kebir S, Khurshid Z, Gaertner FC, Essler M, Hattingen E, Fimmers R, et al. Unsupervised consensus cluster analysis of [18F]-fluoroethyl-l-tyrosine positron emission tomography identified textural features for the diagnosis of pseudoprogression in high-grade glioma. Oncotarget. 2017;8(5):8294–304.

    Article  PubMed  Google Scholar 

  83. Galldiks N, Langen KJ, Pope WB. From the clinician’s point of view—what is the status quo of positron emission tomography in patients with brain tumors? Neuro Oncol. 2015;17(11):1434–44.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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  1. Servicio de Neurocirugía, Hospital Universitario de Burgos, Avda Islas Baleares 3, 09006, Burgos, Spain

    P. D. Delgado-López

  2. Servicio de Radiología, Departamento de Neurorradiología, Hospital Universitario de Burgos, Burgos, Spain

    E. Riñones-Mena

  3. Servicio de Oncología Radioterápica, Hospital Universitario de Burgos, Burgos, Spain

    E. M. Corrales-García

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Delgado-López, P.D., Riñones-Mena, E. & Corrales-García, E.M. Treatment-related changes in glioblastoma: a review on the controversies in response assessment criteria and the concepts of true progression, pseudoprogression, pseudoresponse and radionecrosis. Clin Transl Oncol 20, 939–953 (2018). https://doi.org/10.1007/s12094-017-1816-x

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