Journal of Korean Neurosurgical Society

The Korean Neurosurgical Society (대한신경외과학회)
권호 표지
DOI QR코드

DOI QR Code

Pseudoprogression and Pseudoresponse in the Management of High-Grade Glioma : Optimal Decision Timing According to the Response Assessment of the Neuro-Oncology Working Group

  • Chang, Ji Hyun (Department of Radiation Oncology, Seoul National University Bundang Hospital) ;
  • Kim, Chae-Yong (Department of Neurosurgery, Seoul National University Bundang Hospital) ;
  • Choi, Byung Se (Department of Radiology, Seoul National University Bundang Hospital) ;
  • Kim, Yu Jung (Department of Internal Medicine, Seoul National University Bundang Hospital) ;
  • Kim, Jae Sung (Department of Radiation Oncology, Seoul National University Bundang Hospital) ;
  • Kim, In Ah (Department of Radiation Oncology, Seoul National University Bundang Hospital)
  • Received : 2013.03.19
  • Accepted : 2013.12.16
  • Published : 2014.01.28
Download PDF
⟨ Previous Next ⟩

Abstract

Objective : We evaluated pseudoprogression (PsPD) following radiation therapy combined with concurrent temozolomide (TMZ), and we assessed pseudoresponse following anti-angiogenic therapy for patients with recurrent disease using the Response Assessment of the Neuro-Oncology Working Group. Methods : Patients who were pathologically confirmed as having high-grade glioma received radiotherapy with concurrent TMZ followed by adjuvant TMZ. Bevacizumab (Avastin) with CPT-11 were used as a salvage option for cases of radiologic progression. Magnetic resonance imaging (MRI) was routinely performed 1 month after concurrent radiochemotherapy (CRT) and every 3 months thereafter. For cases treated with the bevacizumab-containing regimen for progressive disease, MRI was performed every 2 months. Results : Of 55 patients, 21 (38%) showed radiologic progression within 4 weeks after CRT. Of these patients, 16 (29%) showed progression at second post-CRT MRI (etPD) and five (9%) showed improvement (PsPD). Seven of thirty-four initially non-progressed patients showed progression at the second post-CRT MRI (ltPD). No difference in survival was observed between the etPD and ltPD groups (p=0.595). Five (50%) of ten patients showed a radiological response after salvage bevacizumab therapy. Four of those patients exhibited rapid progression immediately after discontinuation of the drug (drug holiday). Conclusion : Twelve weeks following treatment could be the optimal timing to determine PsPD or true progression. MRI with gadolinium enhancement alone is not sufficient to characterize tumor response or growth. Clinical correlation with adequate follow-up duration and histopathologic validation may be helpful in discriminating PsPD from true progression.

Keywords

References

  1. Brandes AA, Franceschi E, Tosoni A, Blatt V, Pession A, Tallini G : MGMT promoter methylation status can predict the incidence and outcome of pseudoprogression after concomitant radiochemotherapy in newly diagnosed glioblastoma patients. J Clin Oncol 26 : 2192-2197, 2008 https://doi.org/10.1200/JCO.2007.14.8163
  2. Caroline I, Rosenthal MA : Imaging modalities in high-grade gliomas : pseudoprogression, recurrence, or necrosis? J Clin Neurosci 19 : 633-637, 2012 https://doi.org/10.1016/j.jocn.2011.10.003
  3. Chamberlain MC : Bevacizumab for the treatment of recurrent glioblastoma. Clin Med Insights Oncol 5 : 117-129, 2011
  4. 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 72 : 423-428, 2009 https://doi.org/10.1016/j.surneu.2008.09.023
  5. Easaw JC, Mason WP, Perry J, Laperrière N, Eisenstat DD, Del Maestro R, et al. : Canadian recommendations for the treatment of recurrent or progressive glioblastoma multiforme. Curr Oncol 18 : e126-e136, 2011
  6. Fauquette W, Amourette C, Dehouck MP, Diserbo M : Radiation-induced blood-brain barrier damages : an in vitro study. Brain Res 1433 : 114-126, 2012 https://doi.org/10.1016/j.brainres.2011.11.022
  7. 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 27 : 4733-4740, 2009 https://doi.org/10.1200/JCO.2008.19.8721
  8. Gallego Perez-Larraya J, Lahutte M, Petrirena G, Reyes-Botero G, Gonzalez-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 14 : 667-673, 2012 https://doi.org/10.1093/neuonc/nos070
  9. Joo JD, Chang JH, Kim JH, Hong YK, Kim YH, Kim CY : Temozolomide during and after radiotherapy for newly diagnosed glioblastomas : a prospective multicenter study of Korean patients. J Korean Neurosurg Soc 52 : 92-97, 2012 https://doi.org/10.3340/jkns.2012.52.2.92
  10. Kang HC, Kim CY, Han JH, Choe GY, Kim JH, Kim JH, et al. : Pseudoprogression in patients with malignant gliomas treated with concurrent temozolomide and radiotherapy : potential role of p53. J Neurooncol 102 : 157-162, 2011 https://doi.org/10.1007/s11060-010-0305-7
  11. 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 27 : 740-745, 2009 https://doi.org/10.1200/JCO.2008.16.3055
  12. 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 10 : 162-170, 2008 https://doi.org/10.1215/15228517-2007-062
  13. Laymon CM, Oborski MJ, Lee VK, Davis DK, Wiener EC, Lieberman FS, et al. : Combined imaging biomarkers for therapy evaluation in glioblastoma multiforme : correlating sodium MRI and F-18 FLT PET on a voxel-wise basis. Magn Reson Imaging 30 : 1268-1278, 2012 https://doi.org/10.1016/j.mri.2012.05.011
  14. Lutz K, Radbruch A, Wiestler B, Bäumer P, Wick W, Bendszus M : Neuroradiological response criteria for high-grade gliomas. Clin Neuroradiol 21 : 199-205, 2011 https://doi.org/10.1007/s00062-011-0080-7
  15. Macdonald DR, Cascino TL, Schold SC Jr, Cairncross JG : Response criteria for phase II studies of supratentorial malignant glioma. J Clin Oncol 8 : 1277-1280, 1990
  16. Mangla R, Singh G, Ziegelitz D, Milano MT, Korones DN, Zhong J, et al. : Changes in relative cerebral blood volume 1 month after radiation-temozolomide therapy can help predict overall survival in patients with glioblastoma. Radiology 256 : 575-584, 2010 https://doi.org/10.1148/radiol.10091440
  17. Miyatake S, Furuse M, Kawabata S, Maruyama T, Kumabe T, Kuroiwa T, et al. : Bevacizumab treatment of symptomatic pseudoprogression after boron neutron capture therapy for recurrent malignant gliomas. Report of 2 cases. Neuro Oncol 15 : 650-655, 2013 https://doi.org/10.1093/neuonc/not020
  18. 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 92 : 149-155, 2009 https://doi.org/10.1007/s11060-008-9745-8
  19. Pan E, Tsai JS, Mitchell SB : Retrospective study of venous thromboembolic and intracerebral hemorrhagic events in glioblastoma patients. Anticancer Res 29 : 4309-4313, 2009
  20. Rosso L, Brock CS, Gallo JM, Saleem A, Price PM, Turkheimer FE, et al. : A new model for prediction of drug distribution in tumor and normal tissues : pharmacokinetics of temozolomide in glioma patients. Cancer Res 69 : 120-127, 2009 https://doi.org/10.1158/0008-5472.CAN-08-2356
  21. Sanghera P, Perry J, Sahgal A, Symons S, Aviv R, Morrison M, et al. : Pseudoprogression following chemoradiotherapy for glioblastoma multiforme. Can J Neurol Sci 37 : 36-42, 2010 https://doi.org/10.1017/S0317167100009628
  22. Sanghera P, Rampling R, Haylock B, Jefferies S, McBain C, Rees JH, et al. : The concepts, diagnosis and management of early imaging changes after therapy for glioblastomas. Clin Oncol (R Coll Radiol) 24 : 216-227, 2012 https://doi.org/10.1016/j.clon.2011.06.004
  23. Scherrmann JM : Expression and function of multidrug resistance transporters at the blood-brain barriers. Expert Opin Drug Metab Toxicol 1 : 233-246, 2005 https://doi.org/10.1517/17425255.1.2.233
  24. 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 113 : 405-410, 2008 https://doi.org/10.1002/cncr.23562
  25. Thompson EM, Frenkel EP, Neuwelt EA : The paradoxical effect of bevacizumab in the therapy of malignant gliomas. Neurology 76 : 87-93, 2011 https://doi.org/10.1212/WNL.0b013e318204a3af
  26. 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 70 : 234-243; discussion 243-244, 2012 https://doi.org/10.1227/NEU.0b013e318223f5a7
  27. Vredenburgh JJ, Desjardins A, Herndon JE 2nd, Dowell JM, Reardon DA, Quinn JA, et al. : Phase II trial of bevacizumab and irinotecan in recurrent malignant glioma. Clin Cancer Res 13 : 1253-1259, 2007 https://doi.org/10.1158/1078-0432.CCR-06-2309
  28. 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 28 : 1963-1972, 2010 https://doi.org/10.1200/JCO.2009.26.3541
  29. Young RJ, Gupta A, Shah AD, Graber JJ, Chan TA, Zhang Z, et al. : MRI perfusion in determining pseudoprogression in patients with glioblastoma. Clin Imaging 37 : 41-49, 2013 https://doi.org/10.1016/j.clinimag.2012.02.016

Cited by

  1. Advanced Magnetic Resonance Imaging Methods for Planning and Monitoring Radiation Therapy in Patients With High-Grade Glioma vol.24, pp.4, 2014, https://doi.org/10.1016/j.semradonc.2014.06.008
  2. Pseudoprogression in children, adolescents and young adults with non-brainstem high grade glioma and diffuse intrinsic pontine glioma vol.129, pp.1, 2016, https://doi.org/10.1007/s11060-016-2151-8
  3. Treatment-related changes in glioblastoma: a review on the controversies in response assessment criteria and the concepts of true progression, pseudoprogression, pseudoresponse and radionecrosis vol.20, pp.8, 2014, https://doi.org/10.1007/s12094-017-1816-x
  4. Noninvasive Glioblastoma Testing: Multimodal Approach to Monitoring and Predicting Treatment Response vol.2018, pp.None, 2014, https://doi.org/10.1155/2018/2908609
  5. Current concepts in radiologic assessment of pediatric brain tumors during treatment, part 1 vol.48, pp.13, 2018, https://doi.org/10.1007/s00247-018-4194-9
  6. The Path Toward PET-Guided Radiation Therapy for Glioblastoma in Laboratory Animals: A Mini Review vol.6, pp.None, 2014, https://doi.org/10.3389/fmed.2019.00005
  7. Blood Biomarkers of Glioma in Response Assessment Including Pseudoprogression and Other Treatment Effects: A Systematic Review vol.10, pp.None, 2014, https://doi.org/10.3389/fonc.2020.01191
  8. Pseudoprogression versus true progression in glioblastoma patients: A multiapproach literature review. Part 2 – Radiological features and metric markers vol.159, pp.None, 2014, https://doi.org/10.1016/j.critrevonc.2021.103230
  9. A Clinical PET Imaging Tracer ([18F]DASA-23) to Monitor Pyruvate Kinase M2–Induced Glycolytic Reprogramming in Glioblastoma vol.27, pp.23, 2014, https://doi.org/10.1158/1078-0432.ccr-21-0544