Pseudoprogression, radionecrosis, inflammation or true tumor progression? challenges associated with glioblastoma response assessment in an evolving therapeutic landscape

Journal of Neuro-Oncology - Tập 134 Số 3 - Trang 495-504 - 2017
Benjamin M. Ellingson1, Caroline Chung2, Whitney B. Pope3, Jerrold L. Boxerman4, Timothy J. Kaufmann5
1UCLA Brain Tumor Imaging Laboratory (BTIL), David Geffen School of Medicine, Center for Computer Vision and Imaging, University of California Los Angeles, 924 Westwood Blvd., Suite 615, Los Angeles, CA, 90024, USA
2Department of Radiation Oncology, University of Texas MD Anderson Cancer Center, Houston, TX, USA
3Department of Radiological Sciences, David Geffen School of Medicine, University of California Los Angeles, Los Angeles, CA, USA
4Department of Diagnostic Imaging, Rhode Island Hospital and Alpert Medical School of Brown University, Providence, RI, USA
5Department of Radiology, Mayo Clinic, Rochester, MN, USA

Tóm tắt

Từ khóa


Tài liệu tham khảo

Leon SP, Folkerth RD, Black PM (1996) Microvessel density is a prognostic indicator for patients with astroglial brain tumors. Cancer 77:362–372

Wesseling P, van der Laak JA, Link M, Teepen HL, Ruiter DJ (1998) Quantitative analysis of microvascular changes in diffuse astrocytic neoplasms with increasing grade of malignancy. Hum Pathol 29:352–358

Folkman J (2002) Role of angiogenesis in tumor growth and metastasis. Semin Oncol 29:15–18

Kelly PJ, Daumas-Duport C, Kispert DB, Kall BA, Scheithauer BW, Illig JJ (1987) Imaging-based stereotaxic serial biopsies in untreated intracranial glial neoplasms. J Neurosurg 66:865–874

Macdonald DR, Cascino TL, Schold SC Jr, Cairncross JG (1990) Response criteria for phase II studies of supratentorial malignant glioma. J Clin Oncol 8:1277–1280

Wen PY, Cloughesy TF, Ellingson BM, Reardon DA, Fine HA, Abrey L, Ballman K, Bendszuz M, Buckner J, Chang SM, Prados MD, Pope WB, Gregory Sorensen A, van den Bent M, Yung WK (2014) Report of the Jumpstarting Brain Tumor Drug Development Coalition and FDA clinical trials neuroimaging endpoint workshop (January 30, 2014, Bethesda MD). Neuro Oncol 16 Suppl 7: vii 36-47

Therasse P, Arbuck SG, Eisenhauer EA, Wanders J, Kaplan RS, Rubinstein L, Verweij J, Van Glabbeke M, van Oosterom AT, Christian MC, Gwyther SG (2000) 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 92:205–216

Wen PY, Macdonald DR, Reardon DA, Cloughesy TF, Sorensen AG, Galanis E, Degroot J, Wick W, Gilbert MR, Lassman AB, Tsien C, Mikkelsen T, Wong ET, Chamberlain MC, Stupp R, Lamborn KR, Vogelbaum MA, van den Bent MJ, Chang SM (2010) Updated response assessment criteria for high-grade gliomas: response assessment in neuro-oncology working group. J Clin Oncol 28:1963–1972

Pope WB, Lai A, Nghiemphu P, Mischel P, Cloughesy TF (2006) MRI in patients with high-grade gliomas treated with bevacizumab and chemotherapy. Neurology 66:1258–1260

Chamberlain MC: MRI in patients with high-grade gliomas treated with bevacizumab and chemotherapy. Neurology 67: 2089; author reply 2089, 2006

Fajardo L-G LF, Berthrong M, Anderson RE (2001) Radiation pathology. Oxford University Press, New York

Van Mieghem E, Wozniak A, Geussens Y, Menten J, De Vleeschouwer S, Van Calenbergh F, Sciot R, Van Gool S, Bechter OE, Demaerel P, Wilms G, Clement PM (2013) Defining pseudoprogression in glioblastoma multiforme. Eur J Neurol 20:1335–1341

de Wit MC, de Bruin HG, Eijkenboom W, Sillevis Smitt PA, van den Bent MJ (2004) Immediate post-radiotherapy changes in malignant glioma can mimic tumor progression. Neurology 63:535–537

Parvez K, Parvez A, Zadeh G (2014) The diagnosis and treatment of pseudoprogression, radiation necrosis and brain tumor recurrence. Int J Mol Sci 15:11832–11846

Brandes AA, Tosoni A, Spagnolli F, Frezza G, Leonardi M, Calbucci F, Franceschi E (2008) Disease progression or pseudoprogression after concomitant radiochemotherapy treatment: pitfalls in neurooncology. Neuro Oncol 10:361–367

Taal W, Brandsma D, de Bruin HG, Bromberg JE, Swaak-Kragten AT, Smitt PA, van Es CA, van den Bent MJ (2008) Incidence of early pseudo-progression in a cohort of malignant glioma patients treated with chemoirradiation with temozolomide. Cancer 113:405–410

Radbruch A, Fladt J, Kickingereder P, Wiestler B, Nowosielski M, Baumer P, Schlemmer HP, Wick A, Heiland S, Wick W, Bendszus M (2015) Pseudoprogression in patients with glioblastoma: clinical relevance despite low incidence. Neuro Oncol 17:151–159

Gahramanov S, Varallyay C, Tyson RM, Lacy C, Fu R, Netto JP, Nasseri M, White T, Woltjer RL, Gultekin SH, Neuwelt EA (2014) Diagnosis of pseudoprogression using MRI perfusion in patients with glioblastoma multiforme may predict improved survival. CNS. Oncol 3:389–400

Ellingson BM, Wen PY, van den Bent MJ, Cloughesy TF (2014) Pros and cons of current brain tumor imaging. Neuro Oncol 16 Suppl 7: vii2-11

Brandes AA, Franceschi E, Tosoni A, Blatt V, Pession A, Tallini G, Bertorelle R, Bartolini S, Calbucci F, Andreoli A, Frezza G, Leonardi M, Spagnolli F, Ermani M (2008) 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

Sanghera P, Rampling R, Haylock B, Jefferies S, McBain C, Rees JH, Soh C, Whittle IR (2012) The concepts, diagnosis and management of early imaging changes after therapy for glioblastomas. Clin Oncol (R Coll Radiol) 24:216–227

Langleben DD, Segall GM (2000) PET in differentiation of recurrent brain tumor from radiation injury. J Nucl Med 41:1861–1867

Gerstner ER, McNamara MB, Norden AD, Lafrankie D, Wen PY (2009) Effect of adding temozolomide to radiation therapy on the incidence of pseudo-progression. J Neurooncol 94:97–101

Calvo W (1993) Experimental radiation damage of the central nervous system. Recent Results Cancer Res 130:175–188

Hopewell JW, Calvo W, Jaenke R, Reinhold HS, Robbins ME, Whitehouse EM (1993) Microvasculature and radiation damage. Recent Results Cancer Res 130:1–16

Roberts WG, Palade GE (1995) Increased microvascular permeability and endothelial fenestration induced by vascular endothelial growth factor. J Cell Sci 108(Pt 6):2369–2379

Li YQ, Ballinger JR, Nordal RA, Su ZF, Wong CS (2001) Hypoxia in radiation-induced blood-spinal cord barrier breakdown. Cancer Res 61:3348–3354

Brandsma D, Stalpers L, Taal W, Sminia P, van den Bent MJ (2008) Clinical features, mechanisms, and management of pseudoprogression in malignant gliomas. Lancet Oncol 9:453–461

Ellingson BM, Malkin MG, Rand SD, Connelly JM, Quinsey C, LaViolette PS, Bedekar DP, Schmainda KM (2010) Validation of functional diffusion maps (fDMs) as a biomarker for human glioma cellularity. J Magn Reson Imaging 31:538–548

Sugahara T, Korogi Y, Kochi M, Ikushima I, Shigematu Y, Hirai T, Okuda T, Liang L, Ge Y, Komohara Y, Ushio Y, Takahashi M (1999) Usefulness of diffusion-weighted MRI with echo-planar technique in the evaluation of cellularity in gliomas. J Magn Reson Imaging 9:53–60

Hein PA, Eskey CJ, Dunn JF, Hug EB (2004) Diffusion-weighted imaging in the follow-up of treated high-grade gliomas: tumor recurrence versus radiation injury. AJNR Am J Neuroradiol 25:201–209

Rock JP, Scarpace L, Hearshen D, Gutierrez J, Fisher JL, Rosenblum M, Mikkelsen T (2004) Associations among magnetic resonance spectroscopy, apparent diffusion coefficients, and image-guided histopathology with special attention to radiation necrosis. Neurosurgery 54: 1111–1117; discussion 1117–1119

Sundgren PC, Fan X, Weybright P, Welsh RC, Carlos RC, Petrou M, McKeever PE, Chenevert TL (2006) Differentiation of recurrent brain tumor versus radiation injury using diffusion tensor imaging in patients with new contrast-enhancing lesions. Magn Reson Imaging 24:1131–1142

Fatterpekar GM, Galheigo D, Narayana A, Johnson G, Knopp E (2012) Treatment-related change versus tumor recurrence in high-grade gliomas: a diagnostic conundrum–use of dynamic susceptibility contrast-enhanced (DSC) perfusion MRI. AJR Am J Roentgenol 198:19–26

Prager AJ, Martinez N, Beal K, Omuro A, Zhang Z, Young RJ (2015) Diffusion and perfusion MRI to differentiate treatment-related changes including pseudoprogression from recurrent tumors in high-grade gliomas with histopathologic evidence. AJNR Am J Neuroradiol 36:877–885

Young RJ, Gupta A, Shah AD, Graber JJ, Chan TA, Zhang Z, Shi W, Beal K, Omuro AM (2013) MRI perfusion in determining pseudoprogression in patients with glioblastoma. Clin Imaging 37:41–49

Sugahara T, Korogi Y, Tomiguchi S, Shigematsu Y, Ikushima I, Kira T, Liang L, Ushio Y, Takahashi M (2000) Posttherapeutic intraaxial brain tumor: the value of perfusion-sensitive contrast-enhanced MR imaging for differentiating tumor recurrence from nonneoplastic contrast-enhancing tissue. AJNR Am J Neuroradiol 21:901–909

Hu LS, Baxter LC, Smith KA, Feuerstein BG, Karis JP, Eschbacher JM, Coons SW, Nakaji P, Yeh RF, Debbins J, Heiserman JE (2009) Relative cerebral blood volume values to differentiate high-grade glioma recurrence from posttreatment radiation effect: direct correlation between image-guided tissue histopathology and localized dynamic susceptibility-weighted contrast-enhanced perfusion MR imaging measurements. AJNR Am J Neuroradiol 30:552–558

Hoefnagels FW, Lagerwaard FJ, Sanchez E, Haasbeek CJ, Knol DL, Slotman BJ, Vandertop WP (2009) Radiological progression of cerebral metastases after radiosurgery: assessment of perfusion MRI for differentiating between necrosis and recurrence. J Neurol 256:878–887

Barajas RF, Chang JS, Sneed PK, Segal MR, McDermott MW, Cha S (2009) Distinguishing recurrent intra-axial metastatic tumor from radiation necrosis following gamma knife radiosurgery using dynamic susceptibility-weighted contrast-enhanced perfusion MR imaging. AJNR Am J Neuroradiol 30:367–372

Barajas RF Jr, Chang JS, Segal MR, Parsa AT, McDermott MW, Berger MS, Cha S (2009) Differentiation of recurrent glioblastoma multiforme from radiation necrosis after external beam radiation therapy with dynamic susceptibility-weighted contrast-enhanced perfusion MR imaging. Radiology 253:486–496

Doyle WK, Budinger TF, Valk PE, Levin VA, Gutin PH (1987) Differentiation of cerebral radiation necrosis from tumor recurrence by [18F]FDG and 82Rb positron emission tomography. J Comput Assist Tomogr 11:563–570

Kim EE, Chung SK, Haynie TP, Kim CG, Cho BJ, Podoloff DA, Tilbury RS, Yang DJ, Yung WK, Moser RP Jr., et al (1992) Differentiation of residual or recurrent tumors from post-treatment changes with F-18 FDG PET. Radiographics 12:269–279

Terakawa Y, Tsuyuguchi N, Iwai Y, Yamanaka K, Higashiyama S, Takami T, Ohata K (2008) Diagnostic accuracy of 11 C-methionine PET for differentiation of recurrent brain tumors from radiation necrosis after radiotherapy. J Nucl Med 49:694–699

Chen W, Silverman DH, Delaloye S, Czernin J, Kamdar N, Pope W, Satyamurthy N, Schiepers C, Cloughesy T (2006) 18F-FDOPA PET imaging of brain tumors: comparison study with 18F-FDG PET and evaluation of diagnostic accuracy. J Nucl Med 47:904–911

Popperl G, Gotz C, Rachinger W, Gildehaus FJ, Tonn JC, Tatsch K (2004) Value of O-(2-[18F]fluoroethyl)- L-tyrosine PET for the diagnosis of recurrent glioma. Eur J Nucl Med Mol Imaging 31:1464–1470

Rachinger W, Goetz C, Popperl G, Gildehaus FJ, Kreth FW, Holtmannspotter M, Herms J, Koch W, Tatsch K, Tonn JC: Positron emission tomography with O-(2-[18F]fluoroethyl)-l-tyrosine versus magnetic resonance imaging in the diagnosis of recurrent gliomas. Neurosurgery 57: 505–511; discussion 505–511, 2005

Albert NL, Weller M, Suchorska B, Galldiks N, Soffietti R, Kim MM, la Fougere C, Pope W, Law I, Arbizu J, Chamberlain MC, Vogelbaum M, Ellingson BM, Tonn JC (2016) Response Assessment in Neuro-Oncology working group and European Association for Neuro-Oncology recommendations for the clinical use of PET imaging in gliomas. Neuro Oncol 18:1199–1208

Galldiks N, Dunkl V, Stoffels G, Hutterer M, Rapp M, Sabel M, Reifenberger G, Kebir S, Dorn F, Blau T, Herrlinger U, Hau P, Ruge MI, Kocher M, Goldbrunner R, Fink GR, Drzezga A, Schmidt M, Langen KJ (2015) Diagnosis of pseudoprogression in patients with glioblastoma using O-(2-[18F]fluoroethyl)-L-tyrosine PET. Eur J Nucl Med Mol Imaging 42:685–695

Herrmann K, Czernin J, Cloughesy T, Lai A, Pomykala KL, Benz MR, Buck AK, Phelps ME, Chen W (2014) Comparison of visual and semiquantitative analysis of 18F-FDOPA-PET/CT for recurrence detection in glioblastoma patients. Neuro Oncol 16:603–609

Yamamoto Y, Nishiyama Y, Toyama Y, Kunishio K, Satoh K, Ohkawa M (2002) 99mTc-MIBI and 201Tl SPET in the detection of recurrent brain tumours after radiation therapy. Nucl Med Commun 23:1183–1190

Schwartz RB, Carvalho PA, Alexander E 3rd, Loeffler JS, Folkerth R, Holman BL (1991) Radiation necrosis vs high-grade recurrent glioma: differentiation by using dual-isotope SPECT with 201TI and 99mTc-HMPAO. AJNR Am J Neuroradiol 12:1187–1192

Samnick S, Bader JB, Hellwig D, Moringlane JR, Alexander C, Romeike BF, Feiden W, Kirsch CM (2002) Clinical value of iodine-123-alpha-methyl-L-tyrosine single-photon emission tomography in the differential diagnosis of recurrent brain tumor in patients pretreated for glioma at follow-up. J Clin Oncol 20:396–404

Zeng QS, Li CF, Liu H, Zhen JH, Feng DC (2007) Distinction between recurrent glioma and radiation injury using magnetic resonance spectroscopy in combination with diffusion-weighted imaging. Int J Radiat Oncol Biol Phys 68:151–158

Bashir MR, Bhatti L, Marin D, Nelson RC (2015) Emerging applications for ferumoxytol as a contrast agent in MRI. J Magn Reson Imaging 41:884–898

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 6: 33, 2015

Okada H, Weller M, Huang R, Finocchiaro G, Gilbert MR, Wick W, Ellingson BM, Hashimoto N, Pollack IF, Brandes AA, Franceschi E, Herold-Mende C, Nayak L, Panigrahy A, Pope WB, Prins R, Sampson JH, Wen PY, Reardon DA (2015) Immunotherapy response assessment in neuro-oncology: a report of the RANO working group. Lancet Oncol 16:e534–e542

Okada H, Kalinski P, Ueda R, Hoji A, Kohanbash G, Donegan TE, Mintz AH, Engh JA, Bartlett DL, Brown CK, Zeh H, Holtzman MP, Reinhart TA, Whiteside TL, Butterfield LH, Hamilton RL, Potter DM, Pollack IF, Salazar AM, Lieberman FS (2011) Induction of CD8 + T-cell responses against novel glioma-associated antigen peptides and clinical activity by vaccinations with {alpha}-type 1 polarized dendritic cells and polyinosinic-polycytidylic acid stabilized by lysine and carboxymethylcellulose in patients with recurrent malignant glioma. J Clin Oncol 29:330–336

Sampson JH, Heimberger AB, Archer GE, Aldape KD, Friedman AH, Friedman HS, Gilbert MR, Herndon JE 2nd, McLendon RE, Mitchell DA, Reardon DA, Sawaya R, Schmittling RJ, Shi W, Vredenburgh JJ, Bigner DD (2010) Immunologic escape after prolonged progression-free survival with epidermal growth factor receptor variant III peptide vaccination in patients with newly diagnosed glioblastoma. J Clin Oncol 28:4722–4729

Vrabec M, Van Cauter S, Himmelreich U, Van Gool SW, Sunaert S, De Vleeschouwer S, Suput D, Demaerel P (2011) MR perfusion and diffusion imaging in the follow-up of recurrent glioblastoma treated with dendritic cell immunotherapy: a pilot study. Neuroradiology 53:721–731

Stenberg L, Englund E, Wirestam R, Siesjo P, Salford LG, Larsson EM (2006) Dynamic susceptibility contrast-enhanced perfusion magnetic resonance (MR) imaging combined with contrast-enhanced MR imaging in the follow-up of immunogene-treated glioblastoma multiforme. Acta Radiol 47:852–861

Chiba Y, Kinoshita M, Okita Y, Tsuboi A, Isohashi K, Kagawa N, Fujimoto Y, Oji Y, Oka Y, Shimosegawa E, Morita S, Hatazawa J, Sugiyama H, Hashimoto N, Yoshimine T (2012) Use of (11)C-methionine PET parametric response map for monitoring WT1 immunotherapy response in recurrent malignant glioma. J Neurosurg 116:835–842

Tumeh PC, Radu CG, Ribas A (2008) PET imaging of cancer immunotherapy. J Nucl Med 49:865–868

Stuplich M, Hadizadeh DR, Kuchelmeister K, Scorzin J, Filss C, Langen KJ, Schafer N, Mack F, Schuller H, Simon M, Glas M, Pietsch T, Urbach H, Herrlinger U (2012) Late and prolonged pseudoprogression in glioblastoma after treatment with lomustine and temozolomide. J Clin Oncol 30:e180–e183