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Intracavitary radioimmunotherapy of high-grade gliomas: present status and future developments

  • Review Article - Tumor - Glioma
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Abstract

There is a distinct need for new and second-line therapies to delay or prevent local tumor regrowth after current standard of care therapy. Intracavitary radioimmunotherapy, in combination with radiotherapy, is discussed in the present review as a therapeutic strategy of high potential. We performed a systematic literature search following the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA). The available body of literature on intracavitary radioimmunotherapy (iRIT) in glioblastoma and anaplastic astrocytomas is presented. Several past and current phase I and II clinical trials, using mostly an anti-tenascin monoclonal antibody labeled with I-131, have shown median overall survival of 19–25 months in glioblastoma, while adverse events remain low. Tenascin, followed by EGFR and variants, or smaller peptides have been used as targets, and most clinical studies were performed with I-131 or Y-90 as radionuclides while only recently Re-188, I-125, and Bi-213 were applied. The pharmacokinetics of iRIT, as well as the challenges encountered with this therapy, is comprehensively discussed. This promising approach deserves further exploration in future studies by incorporating several innovative modifications.

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References

  1. Aaslid R, Groger U, Patlak CS, Fenstermacher JD, Huber P, Reulen HJ (1990) Fluid flow rates in human peritumoural oedema. Acta Neurochir Suppl (Wien) 51:152–154

    CAS  Google Scholar 

  2. Akabani G, Reist CJ, Cokgor I, Friedman AH, Friedman HS, Coleman RE, Zhao XG, Bigner DD, Zalutsky MR (1999) Dosimetry of 131I-labeled 81C6 monoclonal antibody administered into surgically created resection cavities in patients with malignant brain tumors. J Nucl Med 40:631–638

    CAS  PubMed  Google Scholar 

  3. Akabani G, Cokgor I, Coleman RE, Gonzalez Trotter D, Wong TZ, Friedman HS, Friedman AH, Garcia-Turner A, Herndon JE, DeLong D, McLendon RE, Zhao XG, Pegram CN, Provenzale JM, Bigner DD, Zalutsky MR (2000) Dosimetry and dose-response relationships in newly diagnosed patients with malignant gliomas treated with iodine-131-labeled anti-tenascin monoclonal antibody 81C6 therapy. Int J Radiat Oncol Biol Phys 46:947–958

    Article  CAS  PubMed  Google Scholar 

  4. Akabani G, Reardon DA, Coleman RE, Wong TZ, Metzler SD, Bowsher JE, Barboriak DP, Provenzale JM, Greer KL, DeLong D, Friedman HS, Friedman AH, Zhao XG, Pegram CN, McLendon RE, Bigner DD, Zalutsky MR (2005) Dosimetry and radiographic analysis of 131I-labeled anti-tenascin 81C6 murine monoclonal antibody in newly diagnosed patients with malignant gliomas: a phase II study. J Nucl Med 46:1042–1051

    CAS  PubMed  Google Scholar 

  5. Albert FK, Forsting M, Sartor K, Adams HP, Kunze S (1994) Early postoperative magnetic resonance imaging after resection of malignant glioma: objective evaluation of residual tumor and its influence on regrowth and prognosis. Neurosurgery 34:45–60 discussion 60-41

    CAS  PubMed  Google Scholar 

  6. Arista A, Sturiale C, Riva P, Tison V, Frattarelli M, Moscatelli G, Franceschi G, Spinelli A (1995) Intralesional administration of I-131 labelled monoclonal antibodies in the treatment of malignant gliomas. Acta Neurochir 135:159–162

    Article  CAS  PubMed  Google Scholar 

  7. Bartolomei M, Mazzetta C, Handkiewicz-Junak D, Bodei L, Rocca P, Grana C, Maira G, Sturiale C, Villa G, Paganelli G (2004) Combined treatment of glioblastoma patients with locoregional pre-targeted 90Y-biotin radioimmunotherapy and temozolomide. Q J Nucl Med Mol Imaging 48:220–228

    CAS  PubMed  Google Scholar 

  8. Bashir R, Hochberg F, Oot R (1988) Regrowth patterns of glioblastoma multiforme related to planning of interstitial brachytherapy radiation fields. Neurosurgery 23:27–30

    Article  CAS  PubMed  Google Scholar 

  9. Beckford Vera DR, Eigner S, Eigner Henke K, Leyva Montana R, Melichar F, Beran M (2013) (177)Lu/ (90) Y intermediate-affinity monoclonal antibodies targeting EGFR and HER2/c-neu: preparation and preclinical evaluation. Recent Results Cancer Res 194:301–317. https://doi.org/10.1007/978-3-642-27994-2_16

    Article  CAS  PubMed  Google Scholar 

  10. Behling K, Maguire WF, Lopez Puebla JC, Sprinkle SR, Ruggiero A, O’Donoghue J, Gutin PH, Scheinberg DA, McDevitt MR (2016) Vascular targeted radioimmunotherapy for the treatment of glioblastoma. J Nucl Med 57:1576–1582. https://doi.org/10.2967/jnumed.115.171371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Bender H, Emrich JG, Eshelman J, Chu MA, Steplewski Z, Biersack HJ, Brady LW (1997) External beam radiation enhances antibody mediated radiocytotoxicity in human glioma cells in vitro. Anticancer Res 17:1797–1802

    CAS  PubMed  Google Scholar 

  12. Bigner DD, Brown MT, Friedman AH, Coleman RE, Akabani G, Friedman HS, Thorstad WL, McLendon RE, Bigner SH, Zhao XG, Pegram CN, Wikstrand CJ, Herndon JE 2nd, Vick NA, Paleologos N, Cokgor I, Provenzale JM, Zalutsky MR (1998) Iodine-131-labeled antitenascin monoclonal antibody 81C6 treatment of patients with recurrent malignant gliomas: phase I trial results. J Clin Oncol 16:2202–2212. https://doi.org/10.1200/JCO.1998.16.6.2202

    Article  CAS  PubMed  Google Scholar 

  13. Boiardi A, Eoli M, Salmaggi A, Lamperti E, Botturi A, Broggi G, Bartolomei M, Silvani A (2003) New approach in delivering chemotherapy: locoregional treatment for recurrent glioblastoma (rGBM). J Exp Clin Cancer Res 22:123–127

    CAS  PubMed  Google Scholar 

  14. Boskovitz A, Akabani GH, Pegram CN, Bigner DD, Zalutsky MR (2004) Human/murine chimeric 81C6 F (ab’)(2) fragment: preclinical evaluation of a potential construct for the targeted radiotherapy of malignant glioma. Nucl Med Biol 31:345–355. https://doi.org/10.1016/j.nucmedbio.2003.10.008

    Article  CAS  PubMed  Google Scholar 

  15. Brady LW, Markoe AM, Woo DV, Amendola BE, Karlsson UL, Rackover MA, Koprowski H, Steplewski Z, Peyster RG (1990) Iodine-125-labeled anti-epidermal growth factor receptor-425 in the treatment of glioblastoma multiforme. A pilot study. Front Radiat Ther Oncol 24:151–160 discussion 161-155

    Article  CAS  PubMed  Google Scholar 

  16. Brem H, Piantadosi S, Burger PC, Walker M, Selker R, Vick NA, Black K, Sisti M, Brem S, Mohr G et al (1995) Placebo-controlled trial of safety and efficacy of intraoperative controlled delivery by biodegradable polymers of chemotherapy for recurrent gliomas. The Polymer-brain Tumor Treatment Group. Lancet 345:1008–1012

    Article  CAS  PubMed  Google Scholar 

  17. Brown MT, Coleman RE, Friedman AH, Friedman HS, McLendon RE, Reiman R, Felsberg GJ, Tien RD, Bigner SH, Zalutsky MR, Zhao XG, Wikstrand CJ, Pegram CN, Herndon JE 2nd, Vick NA, Paleologos N, Fredericks RK, Schold SC Jr, Bigner DD (1996) Intrathecal 131I-labeled antitenascin monoclonal antibody 81C6 treatment of patients with leptomeningeal neoplasms or primary brain tumor resection cavities with subarachnoid communication: phase I trial results. Clin Cancer Res 2:963–972

    CAS  PubMed  Google Scholar 

  18. Casaco A, Lopez G, Garcia I, Rodriguez JA, Fernandez R, Figueredo J, Torres L, Perera A, Batista J, Leyva R, Pena Y, Amador Z, Gonzalez A, Estupinan B, Coca M, Hernandez A, Puig M, Iglesias M, Hernandez A, Ramos M, Rodriquez L, Suarez N (2008) Phase I single-dose study of intracavitary-administered nimotuzumab labeled with 188 Re in adult recurrent high-grade glioma. Cancer Biol Ther 7:333–339

    Article  CAS  PubMed  Google Scholar 

  19. Chang CN, Chen WC, Wei KC, Ng SH, Ho YS, Huang DY, Lee SP, Hong JH (2003) High-dose-rate stereotactic brachytherapy for patients with newly diagnosed glioblastoma multiformes. J Neuro-Oncol 61:45–55

    Article  Google Scholar 

  20. Chinot OL, Wick W, Mason W, Henriksson R, Saran F, Nishikawa R, Carpentier AF, Hoang-Xuan K, Kavan P, Cernea D, Brandes AA, Hilton M, Abrey L, Cloughesy T (2014) Bevacizumab plus radiotherapy-temozolomide for newly diagnosed glioblastoma. N Engl J Med 370:709–722. https://doi.org/10.1056/NEJMoa1308345

    Article  CAS  PubMed  Google Scholar 

  21. Cho KH, Hall WA, Lo SS, Dusenbery KE (2004) Stereotactic radiosurgery versus fractionated stereotactic radiotherapy boost for patients with glioblastoma multiforme. Technol Cancer Res Treat 3:41–49. https://doi.org/10.1177/153303460400300105

    Article  PubMed  Google Scholar 

  22. Cokgor I, Akabani G, Kuan CT, Friedman HS, Friedman AH, Coleman RE, McLendon RE, Bigner SH, Zhao XG, Garcia-Turner AM, Pegram CN, Wikstrand CJ, Shafman TD, Herndon JE 2nd, Provenzale JM, Zalutsky MR, Bigner DD (2000) Phase I trial results of iodine-131-labeled antitenascin monoclonal antibody 81C6 treatment of patients with newly diagnosed malignant gliomas. J Clin Oncol 18:3862–3872. https://doi.org/10.1200/JCO.2000.18.22.3862

    Article  CAS  PubMed  Google Scholar 

  23. Cordier D, Forrer F, Kneifel S, Sailer M, Mariani L, Macke H, Muller-Brand J, Merlo A (2010) Neoadjuvant targeting of glioblastoma multiforme with radiolabeled DOTAGA-substance P--results from a phase I study. J Neuro-Oncol 100:129–136. https://doi.org/10.1007/s11060-010-0153-5

    Article  CAS  Google Scholar 

  24. Curran WJ Jr, Scott CB, Horton J, Nelson JS, Weinstein AS, Fischbach AJ, Chang CH, Rotman M, Asbell SO, Krisch RE et al (1993) Recursive partitioning analysis of prognostic factors in three Radiation Therapy Oncology Group malignant glioma trials. J Natl Cancer Inst 85:704–710

    Article  PubMed  Google Scholar 

  25. D’Souza NM, Fang P, Logan J, Yang J, Jiang W, Li J (2016) Combining radiation therapy with immune checkpoint blockade for central nervous system malignancies. Front Oncol 6:212. https://doi.org/10.3389/fonc.2016.00212

    Article  PubMed  PubMed Central  Google Scholar 

  26. De Bonis P, Lofrese G, Anile C, Pompucci A, Vigo V, Mangiola A (2013) Radioimmunotherapy for high-grade glioma. Immunotherapy 5:647–659. https://doi.org/10.2217/imt.13.43

    Article  CAS  PubMed  Google Scholar 

  27. De Santis R, Albertoni C, Petronzelli F, Campo S, D’Alessio V, Rosi A, Anastasi AM, Lindstedt R, Caroni N, Arseni B, Chiodi P, Verdoliva A, Cassani G, Chinol M, Paganelli G, Carminati P (2006) Low and high tenascin-expressing tumors are efficiently targeted by ST2146 monoclonal antibody. Clin Cancer Res 12:2191–2196. https://doi.org/10.1158/1078-0432.CCR-05-2526

    Article  PubMed  Google Scholar 

  28. Dewaraja YK, Frey EC, Sgouros G, Brill AB, Roberson P, Zanzonico PB, Ljungberg M (2012) MIRD pamphlet no. 23: quantitative SPECT for patient-specific 3-dimensional dosimetry in internal radionuclide therapy. J Nucl Med 53:1310–1325

    Article  CAS  PubMed  Google Scholar 

  29. Di Fede G, Bronte G, Rizzo S, Rolfo Cervetto C, Cocorullo G, Gulotta G, Bazan V, Russo A (2011) Monoclonal antibodies and antibody fragments: state of the art and future perspectives in the treatment of non-haematological tumors. Expert Opin Biol Ther 11:1433–1445. https://doi.org/10.1517/14712598.2011.594436

    Article  CAS  PubMed  Google Scholar 

  30. Elschot M, Vermolen BJ, Lam MG, de Keizer B, van den Bosch MA, de Jong HW (2013) Quantitative comparison of PET and Bremsstrahlung SPECT for imaging the in vivo yttrium-90 microsphere distribution after liver radioembolization. PLoS One 8:e55742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Emami B, Lyman J, Brown A, Coia L, Goitein M, Munzenrider JE, Shank B, Solin LJ, Wesson M (1991) Tolerance of normal tissue to therapeutic irradiation. Int J Radiat Oncol Biol Phys 21:109–122

    Article  CAS  PubMed  Google Scholar 

  32. Fiedler L, Kellner M, Gosewisch A, Oos R G, Böning G, Linder S, et al (2018) Evaluation of 177Lu- CHX-A´´-DTPA-6A10 Fab as a radioimmunotherapy agent targeting carbonic anhydrase XII. Europ J Nucl Med Mol Imag 60:55–62

  33. Fiedler L, Kellner M, Gosewisch A, Oos RG, Böning G, Linder S, Albert N, Bartenstein P, Reulen HJ, Zeidler R, Gildehaus FJ (2018) Evaluation of 177Lu- CHX-A″-DTPA-6A10 Fab as a radioimmunotherapy agent targeting carbonic anhydrase XII. Eur J Nucl Med Mol Imaging 60:55–62. https://doi.org/10.1016/j.nucmedbio.2018.02.004

    Article  CAS  Google Scholar 

  34. Gan HK, van den Bent M, Lassman AB, Reardon DA, Scott AM (2017) Antibody-drug conjugates in glioblastoma therapy: the right drugs to the right cells. Nat Rev Clin Oncol 14:695–707. https://doi.org/10.1038/nrclinonc.2017.95

    Article  CAS  PubMed  Google Scholar 

  35. Giese A, Bjerkvig R, Berens ME, Westphal M (2003) Cost of migration: invasion of malignant gliomas and implications for treatment. J Clin Oncol 21:1624–1636. https://doi.org/10.1200/JCO.2003.05.063

    Article  CAS  PubMed  Google Scholar 

  36. Gildehaus FJ, Rachinger W, Decker M, Stocker S, Poepperl G, Tatsch K, et al (2003) Migration properties of a radiolabeled intact antibody and Fab-fragment after locoregional application in C6 glioma of the rat. J Nucl Med 44:36 (abstract)

  37. Goetz C, Rachinger W, Poepperl G, Decker M, Gildehaus FJ, Stocker S, Jung G, Tatsch K, Tonn JC, Reulen HJ (2003) Intralesional radioimmunotherapy in the treatment of malignant glioma: clinical and experimental findings. Acta Neurochir Suppl 88:69–75

    Article  CAS  PubMed  Google Scholar 

  38. Goetz C, Riva P, Poepperl G, Gildehaus FJ, Hischa A, Tatsch K, Reulen HJ (2003) Locoregional radioimmunotherapy in selected patients with malignant glioma: experiences, side effects and survival times. J Neuro-Oncol 62:321–328

    Article  CAS  Google Scholar 

  39. Goetz CM, Rachinger W, Decker M, Gildehaus FJ, Stocker S, Jung G, Tatsch K, Tonn JC, Reulen HJ (2005) Distribution of labelled anti-tenascin antibodies and fragments after injection into intact or partly resected C6-gliomas in rats. Cancer Immunol Immunother 54:337–344. https://doi.org/10.1007/s00262-004-0608-7

    Article  CAS  PubMed  Google Scholar 

  40. Hdeib A, Sloan A (2012) Targeted radioimmunotherapy: the role of (1)(3)(1)I-chTNT-1/B mAb (Cotara) for treatment of high-grade gliomas. Future Oncol 8:659–669. https://doi.org/10.2217/fon.12.58

    Article  CAS  PubMed  Google Scholar 

  41. Hens M, Vaidyanathan G, Welsh P, Zalutsky MR (2009) Labeling internalizing anti-epidermal growth factor receptor variant III monoclonal antibody with (177)Lu: in vitro comparison of acyclic and macrocyclic ligands. Nucl Med Biol 36:117–128. https://doi.org/10.1016/j.nucmedbio.2008.11.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Hens M, Vaidyanathan G, Zhao XG, Bigner DD, Zalutsky MR (2010) Anti-EGFRvIII monoclonal antibody armed with 177Lu: in vivo comparison of macrocyclic and acyclic ligands. Nucl Med Biol 37:741–750. https://doi.org/10.1016/j.nucmedbio.2010.04.020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Herold-Mende C, Mueller MM, Bonsanto MM, Schmitt HP, Kunze S, Steiner HH (2002) Clinical impact and functional aspects of tenascin-C expression during glioma progression. Int J Cancer 98:362–369

    Article  CAS  PubMed  Google Scholar 

  44. Hindié E, Zanotti-Fregonara P, Quinto MA, Morgat C, Champion C (2016) Dose deposits from 90Y, 177Lu, 111In, and 161Tb in micrometastases of various sizes: implications for radiopharmaceutical therapy. J Nucl Med 57:759–764

    Article  PubMed  Google Scholar 

  45. Hindorf C, Glatting G, Chiesa C, Linden O, Flux G, Committee ED (2010) EANM Dosimetry Committee guidelines for bone marrow and whole-body dosimetry. Eur J Nucl Med Mol Imaging 37:1238–1250. https://doi.org/10.1007/s00259-010-1422-4

    Article  PubMed  Google Scholar 

  46. Hockaday DC, Shen S, Fiveash J, Raubitschek A, Colcher D, Liu A, Alvarez V, Mamelak AN (2005) Imaging glioma extent with 131I-TM-601. J Nucl Med 46:580–586

    CAS  PubMed  Google Scholar 

  47. Hopkins K, Chandler C, Bullimore J, Sandeman D, Coakham H, Kemshead JT (1995) A pilot study of the treatment of patients with recurrent malignant gliomas with intratumoral yttrium-90 radioimmunoconjugates. Radiother Oncol 34:121–131

    Article  CAS  PubMed  Google Scholar 

  48. Hopkins K, Papanastassiou V, Kemshead JT (1996) The treatment of patients with recurrent malignant gliomas with intratumoral radioimmunoconjugates. Recent Results Cancer Res 141:159–175

    Article  CAS  PubMed  Google Scholar 

  49. Jones FS, Jones PL (2000) The tenascin family of ECM glycoproteins: structure, function, and regulation during embryonic development and tissue remodeling. Dev Dyn 218:235–259. https://doi.org/10.1002/(SICI)1097-0177(200006)218:2<235::AID-DVDY2>3.0.CO;2-G

    Article  CAS  PubMed  Google Scholar 

  50. Kneifel S, Cordier D, Good S, Ionescu MC, Ghaffari A, Hofer S, Kretzschmar M, Tolnay M, Apostolidis C, Waser B, Arnold M, Mueller-Brand J, Maecke HR, Reubi JC, Merlo A (2006) Local targeting of malignant gliomas by the diffusible peptidic vector 1,4,7,10-tetraazacyclododecane-1-glutaric acid-4,7,10-triacetic acid-substance p. Clin Cancer Res 12:3843–3850. https://doi.org/10.1158/1078-0432.CCR-05-2820

    Article  CAS  PubMed  Google Scholar 

  51. Kostron H, Obwegeser A, Jakober R (1996) Photodynamic therapy in neurosurgery: a review. J Photochem Photobiol B 36:157–168

    Article  CAS  PubMed  Google Scholar 

  52. Kubben PL, Wesseling P, Lammens M, Schijns OE, Ter Laak-Poort MP, van Overbeeke JJ, van Santbrink H (2012) Correlation between contrast enhancement on intraoperative magnetic resonance imaging and histopathology in glioblastoma. Surg Neurol Int 3:158. https://doi.org/10.4103/2152-7806.105097

    Article  PubMed  PubMed Central  Google Scholar 

  53. Kunwar S, Prados MD, Chang SM, Berger MS, Lang FF, Piepmeier JM, Sampson JH, Ram Z, Gutin PH, Gibbons RD, Aldape KD, Croteau DJ, Sherman JW, Puri RK, Cintredekin Besudotox Intraparenchymal Study G (2007) Direct intracerebral delivery of cintredekin besudotox (IL13-PE38QQR) in recurrent malignant glioma: a report by the Cintredekin Besudotox Intraparenchymal Study Group. J Clin Oncol 25:837–844. https://doi.org/10.1200/JCO.2006.08.1117

    Article  CAS  PubMed  Google Scholar 

  54. Larson SM, Carrasquillo JA, Cheung NK, Press OW (2015) Radioimmunotherapy of human tumours. Nat Rev Cancer 15:347–360. https://doi.org/10.1038/nrc3925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Leins A, Riva P, Lindstedt R, Davidoff MS, Mehraein P, Weis S (2003) Expression of tenascin-C in various human brain tumors and its relevance for survival in patients with astrocytoma. Cancer 98:2430–2439. https://doi.org/10.1002/cncr.11796

    Article  CAS  PubMed  Google Scholar 

  56. Li L, Quang TS, Gracely EJ, Kim JH, Emrich JG, Yaeger TE, Jenrette JM, Cohen SC, Black P, Brady LW (2010) A phase II study of anti-epidermal growth factor receptor radioimmunotherapy in the treatment of glioblastoma multiforme. J Neurosurg 113:192–198. https://doi.org/10.3171/2010.2.JNS091211

    Article  PubMed  Google Scholar 

  57. Li J, Wang M, Won M, Shaw EG, Coughlin C, Curran WJ Jr, Mehta MP (2011) Validation and simplification of the Radiation Therapy Oncology Group recursive partitioning analysis classification for glioblastoma. Int J Radiat Oncol Biol Phys 81:623–630. https://doi.org/10.1016/j.ijrobp.2010.06.012

    Article  PubMed  Google Scholar 

  58. Luther N, Zhou Z, Zanzonico P, Cheung NK, Humm J, Edgar MA, Souweidane MM (2014) The potential of theragnostic (1)(2)(4)I-8H9 convection-enhanced delivery in diffuse intrinsic pontine glioma. Neuro-Oncology 16:800–806. https://doi.org/10.1093/neuonc/not298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Mamelak AN, Rosenfeld S, Bucholz R, Raubitschek A, Nabors LB, Fiveash JB, Shen S, Khazaeli MB, Colcher D, Liu A, Osman M, Guthrie B, Schade-Bijur S, Hablitz DM, Alvarez VL, Gonda MA (2006) Phase I single-dose study of intracavitary-administered iodine-131-TM-601 in adults with recurrent high-grade glioma. J Clin Oncol 24:3644–3650. https://doi.org/10.1200/JCO.2005.05.4569

    Article  CAS  PubMed  Google Scholar 

  60. Mirimanoff RO, Gorlia T, Mason W, Van den Bent MJ, Kortmann RD, Fisher B, Reni M, Brandes AA, Curschmann J, Villa S, Cairncross G, Allgeier A, Lacombe D, Stupp R (2006) Radiotherapy and temozolomide for newly diagnosed glioblastoma: recursive partitioning analysis of the EORTC 26981/22981-NCIC CE3 phase III randomized trial. J Clin Oncol 24:2563–2569. https://doi.org/10.1200/JCO.2005.04.5963

    Article  CAS  PubMed  Google Scholar 

  61. Moher D, Liberati A, Tetzlaff J, Altman DG, Group P (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 339:b2535. https://doi.org/10.1136/bmj.b2535

    Article  PubMed  PubMed Central  Google Scholar 

  62. Moher D, Liberati A, Tetzlaff J, Altman DG, Group P (2010) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg 8:336–341. https://doi.org/10.1016/j.ijsu.2010.02.007

    Article  PubMed  Google Scholar 

  63. Muller A, Jurcoane A, Kebir S, Ditter P, Schrader F, Herrlinger U, Tzaridis T, Madler B, Schild HH, Glas M, Hattingen E (2017) Quantitative T1-mapping detects cloudy-enhancing tumor compartments predicting outcome of patients with glioblastoma. Cancer Med 6:89–99. https://doi.org/10.1002/cam4.966

    Article  CAS  PubMed  Google Scholar 

  64. Nestler U, Lutz K, Pichlmeier U, Stummer W, Franz K, Reulen HJ, Bink A, Group ALAGS (2015) Anatomic features of glioblastoma and their potential impact on survival. Acta Neurochir 157:179–186. https://doi.org/10.1007/s00701-014-2271-x

    Article  CAS  PubMed  Google Scholar 

  65. Nicholas MK, Lukas RV, Jafri NF, Faoro L, Salgia R (2006) Epidermal growth factor receptor - mediated signal transduction in the development and therapy of gliomas. Clin Cancer Res 12:7261–7270. https://doi.org/10.1158/1078-0432.CCR-06-0874

    Article  CAS  PubMed  Google Scholar 

  66. Oh S, Tsai AK, Ohlfest JR, Panoskaltsis-Mortari A, Vallera DA (2011) Evaluation of a bispecific biological drug designed to simultaneously target glioblastoma and its neovasculature in the brain. J Neurosurg 114:1662–1671. https://doi.org/10.3171/2010.11.JNS101214

    Article  PubMed  Google Scholar 

  67. Paganelli G, Bartolomei M, Ferrari M, Cremonesi M, Broggi G, Maira G, Sturiale C, Grana C, Prisco G, Gatti M, Caliceti P, Chinol M (2001) Pre-targeted locoregional radioimmunotherapy with 90Y-biotin in glioma patients: phase I study and preliminary therapeutic results. Cancer Biother Radiopharm 16:227–235. https://doi.org/10.1089/10849780152389410

    Article  CAS  PubMed  Google Scholar 

  68. Papanastassiou V, Pizer BL, Coakham HB, Bullimore J, Zananiri T, Kemshead JT (1993) Treatment of recurrent and cystic malignant gliomas by a single intracavity injection of 131I monoclonal antibody: feasibility, pharmacokinetics and dosimetry. Br J Cancer 67:144–151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Patel SJ, Shapiro WR, Laske DW, Jensen RL, Asher AL, Wessels BW, Carpenter SP, Shan JS (2005) Safety and feasibility of convection-enhanced delivery of Cotara for the treatment of malignant glioma: initial experience in 51 patients. Neurosurgery 56:1243–1252 discussion 1252-1243

    Article  PubMed  Google Scholar 

  70. Pichlmeier U, Bink A, Schackert G, Stummer W, Group ALAGS (2008) Resection and survival in glioblastoma multiforme: an RTOG recursive partitioning analysis of ALA study patients. Neuro-Oncology 10:1025–1034. https://doi.org/10.1215/15228517-2008-052

    Article  PubMed  PubMed Central  Google Scholar 

  71. Popperl G, Gotz C, Gildehaus FJ, Yousry TA, Reulen HJ, Hahn K, Tatsch K (2002) Initial experiences with adjuvant locoregional radioimmunotherapy using 131I-labeled monoclonal antibodies against tenascin (BC-4) for treatment of glioma (WHO III and IV). Nuklearmedizin 41:120–128

    Article  CAS  PubMed  Google Scholar 

  72. Popperl G, Gotz C, Rachinger W, Schnell O, Gildehaus FJ, Tonn JC, Tatsch K (2006) Serial O-(2-[(18)F]fluoroethyl)-L: -tyrosine PET for monitoring the effects of intracavitary radioimmunotherapy in patients with malignant glioma. Eur J Nucl Med Mol Imaging 33:792–800. https://doi.org/10.1007/s00259-005-0053-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Radbruch A, Lutz K, Wiestler B, Baumer P, Heiland S, Wick W, Bendszus M (2012) Relevance of T2 signal changes in the assessment of progression of glioblastoma according to the response assessment in neuroncology criteria. Neuro-Oncology 14:222–229. https://doi.org/10.1093/neuonc/nor200

    Article  CAS  PubMed  Google Scholar 

  74. Rainov NG (2000) A phase III clinical evaluation of herpes simplex virus type 1 thymidine kinase and ganciclovir gene therapy as an adjuvant to surgical resection and radiation in adults with previously untreated glioblastoma multiforme. Hum Gene Ther 11:2389–2401. https://doi.org/10.1089/104303400750038499

    Article  CAS  PubMed  Google Scholar 

  75. Ravic M (2003) Intracavitary treatment of malignant gliomas: radioimmunotherapy targeting fibronectin. Acta Neurochir Suppl 88:77–82

    CAS  PubMed  Google Scholar 

  76. Reardon DA, Akabani G, Coleman RE, Friedman AH, Friedman HS, Herndon JE 2nd, Cokgor I, McLendon RE, Pegram CN, Provenzale JM, Quinn JA, Rich JN, Regalado LV, Sampson JH, Shafman TD, Wikstrand CJ, Wong TZ, Zhao XG, Zalutsky MR, Bigner DD (2002) Phase II trial of murine (131)I-labeled antitenascin monoclonal antibody 81C6 administered into surgically created resection cavities of patients with newly diagnosed malignant gliomas. J Clin Oncol 20:1389–1397. https://doi.org/10.1200/JCO.2002.20.5.1389

    Article  CAS  PubMed  Google Scholar 

  77. Reardon DA, Akabani G, Coleman RE, Friedman AH, Friedman HS, Herndon JE 2nd, RE ML, Pegram CN, Provenzale JM, Quinn JA, Rich JN, Vredenburgh JJ, Desjardins A, Gururangan S, Badruddoja M, Dowell JM, Wong TZ, Zhao XG, Zalutsky MR, Bigner DD (2006) Salvage radioimmunotherapy with murine iodine-131-labeled antitenascin monoclonal antibody 81C6 for patients with recurrent primary and metastatic malignant brain tumors: phase II study results. J Clin Oncol 24:115–122. https://doi.org/10.1200/JCO.2005.03.4082

    Article  CAS  PubMed  Google Scholar 

  78. Reardon DA, Quinn JA, Akabani G, Coleman RE, Friedman AH, Friedman HS, Herndon JE 2nd, RE ML, Pegram CN, Provenzale JM, Dowell JM, Rich JN, Vredenburgh JJ, Desjardins A, Sampson JH, Gururangan S, Wong TZ, Badruddoja MA, Zhao XG, Bigner DD, Zalutsky MR (2006) Novel human IgG2b/murine chimeric antitenascin monoclonal antibody construct radiolabeled with 131I and administered into the surgically created resection cavity of patients with malignant glioma: phase I trial results. J Nucl Med 47:912–918

    CAS  PubMed  Google Scholar 

  79. Reardon DA, Zalutsky MR, Bigner DD (2007) Antitenascin-C monoclonal antibody radioimmunotherapy for malignant glioma patients. Expert Rev Anticancer Ther 7:675–687. https://doi.org/10.1586/14737140.7.5.675

    Article  CAS  PubMed  Google Scholar 

  80. Reardon DA, Zalutsky MR, Akabani G, Coleman RE, Friedman AH, Herndon JE 2nd, McLendon RE, Pegram CN, Quinn JA, Rich JN, Vredenburgh JJ, Desjardins A, Guruangan S, Boulton S, Raynor RH, Dowell JM, Wong TZ, Zhao XG, Friedman HS, Bigner DD (2008) A pilot study: 131I-antitenascin monoclonal antibody 81c6 to deliver a 44-Gy resection cavity boost. Neuro-Oncology 10:182–189. https://doi.org/10.1215/15228517-2007-053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Reulen HJ (2010) Bulk flow and diffusion revisited, and clinical applications. Acta Neurochir Suppl 106:3–13. https://doi.org/10.1007/978-3-211-98811-4_1

    Article  PubMed  Google Scholar 

  82. Reulen HJ, Graham R, Spatz M, Klatzo I (1977) Role of pressure gradients and bulk flow in dynamics of vasogenic brain edema. J Neurosurg 46:24–35. https://doi.org/10.3171/jns.1977.46.1.0024

    Article  CAS  PubMed  Google Scholar 

  83. Reulen HJ, Poepperl G, Goetz C, Gildehaus FJ, Schmidt M, Tatsch K, Pietsch T, Kraus T, Rachinger W (2015) Long-term outcome of patients with WHO grade III and IV gliomas treated by fractionated intracavitary radioimmunotherapy. J Neurosurg 123:760–770. https://doi.org/10.3171/2014.12.JNS142168

    Article  CAS  PubMed  Google Scholar 

  84. Riva P, Tison V, Arista A, Sturiale C, Franceschi G, Riva N, Casi M, Moscatelli G, Campori F, Spinelli A (1993) Radioimmunotherapy of gastrointestinal cancer and glioblastomas. Int J Biol Markers 8:192–197

    Article  CAS  PubMed  Google Scholar 

  85. Riva P, Arista A, Sturiale C, Tison V, Lazzari S, Franceschi G, Spinelli A, Casi M, Sarti G, Campori F et al (1994) Glioblastoma therapy by direct intralesional administration of I-131 radioiodine labeled antitenascin antibodies. Cell Biophys 24-25:37–43

    Article  CAS  PubMed  Google Scholar 

  86. Riva P, Arista A, Tison V, Sturiale C, Franceschi G, Spinelli A, Riva N, Casi M, Moscatelli G, Frattarelli M (1994) Intralesional radioimmunotherapy of malignant gliomas. An effective treatment in recurrent tumors. Cancer 73:1076–1082

    Article  CAS  PubMed  Google Scholar 

  87. Riva P, Arista A, Franceschi G, Frattarelli M, Sturiale C, Riva N, Casi M, Rossitti R (1995) Local treatment of malignant gliomas by direct infusion of specific monoclonal antibodies labeled with 131I: comparison of the results obtained in recurrent and newly diagnosed tumors. Cancer Res 55:5952s–5956s

    CAS  PubMed  Google Scholar 

  88. Riva P, Franceschi G, Arista A, Frattarelli M, Riva N, Cremonini AM, Giuliani G, Casi M (1997) Local application of radiolabeled monoclonal antibodies in the treatment of high grade malignant gliomas: a six-year clinical experience. Cancer 80:2733–2742

    Article  CAS  PubMed  Google Scholar 

  89. Riva P, Franceschi G, Frattarelli M, Lazzari S, Riva N, Giuliani G, Casi M, Sarti G, Guiducci G, Giorgetti G, Gentile R, Santimaria M, Jermann E, Maeke HR (1999) Loco-regional radioimmunotherapy of high-grade malignant gliomas using specific monoclonal antibodies labeled with 90Y: a phase I study. Clin Cancer Res 5:3275s–3280s

    CAS  PubMed  Google Scholar 

  90. Riva P, Franceschi G, Frattarelli M, Riva N, Guiducci G, Cremonini AM, Giuliani G, Casi M, Gentile R, Jekunen AA, Kairemo KJ (1999) 131I radioconjugated antibodies for the locoregional radioimmunotherapy of high-grade malignant glioma--phase I and II study. Acta Oncol 38:351–359

    Article  CAS  PubMed  Google Scholar 

  91. Riva P, Franceschi G, Riva N, Casi M, Santimaria M, Adamo M (2000) Role of nuclear medicine in the treatment of malignant gliomas: the locoregional radioimmunotherapy approach. Eur J Nucl Med 27:601–609

    Article  CAS  PubMed  Google Scholar 

  92. Sandstrom M, Garske-Roman U, Granberg D, Johansson S, Widstrom C, Eriksson B, Sundin A, Lundqvist H, Lubberink M (2013) Individualized dosimetry of kidney and bone marrow in patients undergoing 177Lu-DOTA-octreotate treatment. J Nucl Med 54:33–41. https://doi.org/10.2967/jnumed.112.107524

    Article  CAS  PubMed  Google Scholar 

  93. Sauerwein W, Zurlo A, Group EBNCT (2002) The EORTC Boron Neutron Capture Therapy (BNCT) Group: achievements and future projects. Eur J Cancer 38(Suppl 4):S31–S34

    Article  PubMed  Google Scholar 

  94. Schlegel J In preparation

  95. Shapiro WR, Carpenter SP, Roberts K, Shan JS (2006) (131)I-chTNT-1/B mAb: tumour necrosis therapy for malignant astrocytic glioma. Expert Opin Biol Ther 6:539–545. https://doi.org/10.1517/14712598.6.5.539

    Article  CAS  PubMed  Google Scholar 

  96. Stummer W, Stocker S, Novotny A, Heimann A, Sauer O, Kempski O, Plesnila N, Wietzorrek J, Reulen HJ (1998) In vitro and in vivo porphyrin accumulation by C6 glioma cells after exposure to 5-aminolevulinic acid. J Photochem Photobiol B 45:160–169

    Article  CAS  PubMed  Google Scholar 

  97. Stummer W, Stocker S, Wagner S, Stepp H, Fritsch C, Goetz C, Goetz AE, Kiefmann R, Reulen HJ (1998) Intraoperative detection of malignant gliomas by 5-aminolevulinic acid-induced porphyrin fluorescence. Neurosurgery 42:518–525 discussion 525-516

    Article  CAS  PubMed  Google Scholar 

  98. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO, European Organisation for R, Treatment of Cancer Brain T, Radiotherapy G, National Cancer Institute of Canada Clinical Trials G (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996. https://doi.org/10.1056/NEJMoa043330

    Article  CAS  PubMed  Google Scholar 

  99. Stupp R, Taillibert S, Kanner AA, Kesari S, Steinberg DM, Toms SA, Taylor LP, Lieberman F, Silvani A, Fink KL, Barnett GH, Zhu JJ, Henson JW, Engelhard HH, Chen TC, Tran DD, Sroubek J, Tran ND, Hottinger AF, Landolfi J, Desai R, Caroli M, Kew Y, Honnorat J, Idbaih A, Kirson ED, Weinberg U, Palti Y, Hegi ME, Ram Z (2015) Maintenance therapy with tumor-treating fields plus temozolomide vs temozolomide alone for glioblastoma: a randomized clinical trial. JAMA 314:2535–2543. https://doi.org/10.1001/jama.2015.16669

    Article  CAS  PubMed  Google Scholar 

  100. Torres LA, Coca MA, Batista JF, Casaco A, Lopez G, Garcia I, Perera A, Pena Y, Hernandez A, Sanchez Y, Romero S, Leyva R, Prats A, Fernandez R (2008) Biodistribution and internal dosimetry of the 188Re-labelled humanized monoclonal antibody anti-epidemal growth factor receptor, nimotuzumab, in the locoregional treatment of malignant gliomas. Nucl Med Commun 29:66–75. https://doi.org/10.1097/MNM.0b013e3282f1bbce

    Article  CAS  PubMed  Google Scholar 

  101. Veeravagu A, Liu Z, Niu G, Chen K, Jia B, Cai W, Jin C, Hsu AR, Connolly AJ, Tse V, Wang F, Chen X (2008) Integrin alphavbeta3-targeted radioimmunotherapy of glioblastoma multiforme. Clin Cancer Res 14:7330–7339. https://doi.org/10.1158/1078-0432.CCR-08-0797

    Article  CAS  PubMed  Google Scholar 

  102. Ventimiglia JB, Wikstrand CJ, Ostrowski LE, Bourdon MA, Lightner VA, Bigner DD (1992) Tenascin expression in human glioma cell lines and normal tissues. J Neuroimmunol 36:41–55

    Article  CAS  PubMed  Google Scholar 

  103. von Neubeck C, Seidlitz A, Kitzler HH, Beuthien-Baumann B, Krause M (2015) Glioblastoma multiforme: emerging treatments and stratification markers beyond new drugs. Br J Radiol 88:20150354. https://doi.org/10.1259/bjr.20150354

    Article  Google Scholar 

  104. Westphal M, Hilt DC, Bortey E, Delavault P, Olivares R, Warnke PC, Whittle IR, Jaaskelainen J, Ram Z (2003) A phase 3 trial of local chemotherapy with biodegradable carmustine (BCNU) wafers (Gliadel wafers) in patients with primary malignant glioma. Neuro-Oncology 5:79–88. https://doi.org/10.1093/neuonc/5.2.79

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Westphal M, Yla-Herttuala S, Martin J, Warnke P, Menei P, Eckland D, Kinley J, Kay R, Ram Z, Group AS (2013) Adenovirus-mediated gene therapy with sitimagene ceradenovec followed by intravenous ganciclovir for patients with operable high-grade glioma (ASPECT): a randomised, open-label, phase 3 trial. Lancet Oncol 14:823–833. https://doi.org/10.1016/S1470-2045(13)70274-2

    Article  CAS  PubMed  Google Scholar 

  106. Wygoda Z, Kula D, Bierzynska-Macyszyn G, Larysz D, Jarzab M, Wlaszczuk P, Bazowski P, Wojtacha M, Rudnik A, Stepien T, Kaspera W, Etmanska A, Skladowski K, Tarnawski R, Kokocinska D, Jarzab B (2006) Use of monoclonal anti-EGFR antibody in the radioimmunotherapy of malignant gliomas in the context of EGFR expression in grade III and IV tumors. Hybridoma (Larchmt) 25:125–132. https://doi.org/10.1089/hyb.2006.25.125

    Article  CAS  Google Scholar 

  107. Yamamoto T, Nakai K, Matsumura A (2008) Boron neutron capture therapy for glioblastoma. Cancer Lett 262:143–152. https://doi.org/10.1016/j.canlet.2008.01.021

    Article  CAS  PubMed  Google Scholar 

  108. Zalutsky MR (2005) Current status of therapy of solid tumors: brain tumor therapy. J Nucl Med 46(Suppl 1):151S–156S

    PubMed  Google Scholar 

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Acknowledgements

Figures 1 and 2 were originally published in JNM. Akabani et al. [2]. J Nucl Med. 1999;40: 631-638, © by the Society of Nuclear Medicine and Molecular Imaging, Inc.

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  1. Hans-Jürgen Reulen and Eric Suero Molina contributed equally to this work.

Authors and Affiliations

  1. Neurosurgical Department, LMU Munich, Munich, Germany

    Hans-Jürgen Reulen

  2. Department of Neurosurgery, University Hospital of Münster, Münster, Germany

    Eric Suero Molina & Walter Stummer

  3. Helmholtz-Zentrum Munich, German Research Center for Environmental Health, Research Group Gene Vectors, Munich, Germany

    Reinhard Zeidler

  4. Department of Otorhinolaryngology, Head and Neck Surgery, University Hospital, LMU Munich, Munich, Germany

    Reinhard Zeidler

  5. Department of Nuclear Medicine, University Hospital, LMU Munich, Munich, Germany

    Franz Josef Gildehaus, Guido Böning & Astrid Gosewisch

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Reulen, HJ., Suero Molina, E., Zeidler, R. et al. Intracavitary radioimmunotherapy of high-grade gliomas: present status and future developments. Acta Neurochir 161, 1109–1124 (2019). https://doi.org/10.1007/s00701-019-03882-9

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