H3K27-altered diffuse midline glioma: a paradigm shifting opportunity in direct delivery of targeted therapeutics

References

• Ostrom QT, Cioffi G, Waite K, et al. CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2014–2018. Neuro Oncol. 2021 Oct 5;23(12Suppl 2):iii1–iii105.
   PubMedGoogle Scholar
• Warren KE. Diffuse intrinsic pontine glioma: poised for progress. Front Oncol. 2012;2:205.
   PubMedGoogle Scholar
• Jaimes C, Poussaint TY. Primary neoplasms of the pediatric brain. Radiol Clin North Am. 2019 Nov;57(6):1163–1175.
   PubMed Web of Science ®Google Scholar
• Smith MA, Freidlin B, Ries LA, et al. Trends in reported incidence of primary malignant brain tumors in children in the United States. J Natl Cancer Inst. 1998 Sep 2;90(17):1269–1277.
   PubMedGoogle Scholar
• Cohen KJ, Jabado N, Grill J. Diffuse intrinsic pontine gliomas-current management and new biologic insights. Is there a glimmer of hope? Neuro Oncol. 2017 Aug 1;19(8):1025–1034.
   PubMed Web of Science ®Google Scholar
• Albright AL, Guthkelch AN, Packer RJ, et al. Prognostic factors in pediatric brain-stem gliomas. J Neurosurg. 1986 Dec;65(6):751–755.
   PubMed Web of Science ®Google Scholar
• Yoshimura J, Onda K, Tanaka R, et al. Clinicopathological study of diffuse type brainstem gliomas: analysis of 40 autopsy cases. Neurol Med Chir (Tokyo). 2003 Aug;43(8):375–382. discussion 382
   PubMed Web of Science ®Google Scholar
• Epstein F, Constantini S. Practical decisions in the treatment of pediatric brain stem tumors. Pediatr Neurosurg. 1996;24(1):24–34.
   PubMed Web of Science ®Google Scholar
• Gururangan S, McLaughlin CA, Brashears J, et al. Incidence and patterns of neuraxis metastases in children with diffuse pontine glioma. J Neurooncol. 2006 Apr;77(2):207–212.
   PubMed Web of Science ®Google Scholar
• Himes BT, Zhang L, Daniels DJ. Treatment strategies in diffuse midline gliomas with the H3K27M mutation: the role of convection-enhanced delivery in overcoming anatomic challenges. Front Oncol. 2019;9:31.
   PubMed Web of Science ®Google Scholar
• Rechberger JS, Lu VM, Zhang L, et al. Clinical trials for diffuse intrinsic pontine glioma: the current state of affairs. Childs Nerv Syst. 2020 Jan;36(1):39–46.
   PubMed Web of Science ®Google Scholar
• Frazier JL, Lee J, Thomale UW, et al. Treatment of diffuse intrinsic brainstem gliomas: failed approaches and future strategies. J Neurosurg Pediatr. 2009 Apr;3(4):259–269.
   PubMed Web of Science ®Google Scholar
• Walker DA, Liu J, Kieran M, et al. A multi-disciplinary consensus statement concerning surgical approaches to low-grade, high-grade astrocytomas and diffuse intrinsic pontine gliomas in childhood (CPN Paris 2011) using the Delphi method. Neuro Oncol. 2013 Apr;15(4):462–468.
   PubMed Web of Science ®Google Scholar
• Roujeau T, Machado G, Garnett MR, et al. Stereotactic biopsy of diffuse pontine lesions in children. J Neurosurg. 2007 Jul;107(1 Suppl):1–4.
   PubMed Web of Science ®Google Scholar
• Dawes W, Marcus HJ, Tisdall M, et al. Robot-assisted stereotactic brainstem biopsy in children: prospective cohort study. J Robot Surg. 2019 Aug;13(4):575–579.
   PubMed Web of Science ®Google Scholar
• Hamisch C, Kickingereder P, Fischer M, et al. Update on the diagnostic value and safety of stereotactic biopsy for pediatric brainstem tumors: a systematic review and meta-analysis of 735 cases. J Neurosurg Pediatr. 2017 Sep;20(3):261–268.
   PubMed Web of Science ®Google Scholar
• Williams JR, Young CC, Vitanza NA, et al. Progress in diffuse intrinsic pontine glioma: advocating for stereotactic biopsy in the standard of care. Neurosurg Focus. 2020 Jan 1;48(1):E4.
   Web of Science ®Google Scholar
• Wu G, Broniscer A, McEachron TA, et al. Somatic histone H3 alterations in pediatric diffuse intrinsic pontine gliomas and non-brainstem glioblastomas. Nat Genet. 2012 Jan 29;44(3):251–253.
   PubMed Web of Science ®Google Scholar
• Schwartzentruber J, Korshunov A, Liu XY, et al. Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature. 2012 Jan 29;482(7384):226–231.
   PubMed Web of Science ®Google Scholar
• Khuong-Quang DA, Buczkowicz P, Rakopoulos P, et al. K27M mutation in histone H3.3 defines clinically and biologically distinct subgroups of pediatric diffuse intrinsic pontine gliomas. Acta Neuropathol. 2012 Sep;124(3):439–447.
   PubMed Web of Science ®Google Scholar
• Saratsis AM, Kambhampati M, Snyder K, et al. Comparative multidimensional molecular analyses of pediatric diffuse intrinsic pontine glioma reveals distinct molecular subtypes. Acta Neuropathol. 2014;127(6):881–895.
   PubMed Web of Science ®Google Scholar
• Lulla RR, Saratsis AM, Hashizume R. Mutations in chromatin machinery and pediatric high-grade glioma. Sci Adv. 2016 Mar;2(3):e1501354.
   PubMed Web of Science ®Google Scholar
• Jones C, Karajannis MA, Jones DTW, et al. Pediatric high-grade glioma: biologically and clinically in need of new thinking. Neuro Oncol. 2017 Feb 1;19(2):153–161.
   PubMed Web of Science ®Google Scholar
• Louis DN, Perry A, Wesseling P, et al. The 2021 WHO classification of tumors of the central nervous system: a summary. Neuro Oncol. 2021 Aug 2;23(8):1231–1251.
   PubMed Web of Science ®Google Scholar
• Lewis PW, Muller MM, Koletsky MS, et al. Inhibition of PRC2 activity by a gain-of-function H3 mutation found in pediatric glioblastoma. Science. 2013 May 17;340(6134):857–861.
   PubMed Web of Science ®Google Scholar
• Chan KM, Fang D, Gan H, et al. The histone H3.3K27M mutation in pediatric glioma reprograms H3K27 methylation and gene expression. Genes Dev. 2013 May 1;27(9):985–990.
   PubMed Web of Science ®Google Scholar
• Bender S, Tang Y, Lindroth AM, et al. Reduced H3K27me3 and DNA hypomethylation are major drivers of gene expression in K27M mutant pediatric high-grade gliomas. Cancer Cell. 2013 Nov 11;24(5):660–672.
   PubMed Web of Science ®Google Scholar
• Venneti S, Garimella MT, Sullivan LM, et al. Evaluation of histone 3 lysine 27 trimethylation (H3K27me3) and enhancer of Zest 2 (EZH2) in pediatric glial and glioneuronal tumors shows decreased H3K27me3 in H3F3A K27M mutant glioblastomas. Brain Pathol. 2013 Sep;23(5):558–564.
   PubMed Web of Science ®Google Scholar
• Krug B, De Jay N, Harutyunyan AS, et al. Pervasive H3K27 acetylation leads to ERV expression and a therapeutic vulnerability in H3K27M gliomas. Cancer Cell. 2019 May 13;35(5):782–797.e8.
   PubMed Web of Science ®Google Scholar
• Larson JD, Kasper LH, Paugh BS, et al. Histone H3.3 K27M accelerates spontaneous brainstem glioma and drives restricted changes in bivalent gene expression. Cancer Cell. 2019 Jan 14;35(1):140–155.e7.
   PubMed Web of Science ®Google Scholar
• Kruidenier L, Chung CW, Cheng Z, et al. A selective jumonji H3K27 demethylase inhibitor modulates the proinflammatory macrophage response. Nature. 2012 Aug 16;488(7411):404–408.
   PubMed Web of Science ®Google Scholar
• Hashizume R, Andor N, Ihara Y, et al. Pharmacologic inhibition of histone demethylation as a therapy for pediatric brainstem glioma. Nat Med. 2014 Dec;20(12):1394–1396.
   PubMed Web of Science ®Google Scholar
• Brown ZZ, Müller MM, Jain SU, et al. Strategy for “detoxification” of a cancer-derived histone mutant based on mapping its interaction with the methyltransferase PRC2. J Am Chem Soc. 2014 Oct 1;136(39):13498–13501.
   PubMed Web of Science ®Google Scholar
• Grasso CS, Tang Y, Truffaux N, et al. Functionally defined therapeutic targets in diffuse intrinsic pontine glioma. Nat Med. 2015 Jun;21(6):555–559.
   PubMed Web of Science ®Google Scholar
• Vitanza NA, Biery MC, Myers C, et al. Optimal therapeutic targeting by HDAC inhibition in biopsy-derived treatment-naïve diffuse midline glioma models. Neuro Oncol. 2021 Mar 25;23(3):376–386.
   PubMed Web of Science ®Google Scholar
• Mohammad F, Weissmann S, Leblanc B, et al. EZH2 is a potential therapeutic target for H3K27M-mutant pediatric gliomas. Nat Med. 2017 Apr;23(4):483–492.
   PubMed Web of Science ®Google Scholar
• Lavarone E, Barbieri CM, Pasini D. Dissecting the role of H3K27 acetylation and methylation in PRC2 mediated control of cellular identity. Nat Commun. 2019 Apr 11;10(1):1679.
   PubMedGoogle Scholar
• Zhang Y, Dong W, Zhu J, et al. Combination of EZH2 inhibitor and BET inhibitor for treatment of diffuse intrinsic pontine glioma. Cell Biosci. 2017;7:56.
   PubMed Web of Science ®Google Scholar
• Piunti A, Hashizume R, Morgan MA, et al. Therapeutic targeting of polycomb and BET bromodomain proteins in diffuse intrinsic pontine gliomas. Nat Med. 2017 Apr;23(4):493–500.
   PubMed Web of Science ®Google Scholar
• Argersinger DP, Rivas SR, Shah AH, et al. New developments in the pathogenesis, therapeutic targeting, and treatment of H3K27M-mutant diffuse midline glioma. Cancers (Basel). 2021 Oct;13(21):21.
   Web of Science ®Google Scholar
• Zhou Z, Luther N, Ibrahim GM, et al. B7-H3, a potential therapeutic target, is expressed in diffuse intrinsic pontine glioma. J Neurooncol. 2013 Feb;111(3):257–264.
   PubMed Web of Science ®Google Scholar
• Souweidane MM, Kramer K, Pandit-Taskar N, et al. Convection-enhanced delivery for diffuse intrinsic pontine glioma: a single-centre, dose-escalation, phase 1 trial. Lancet Oncol. 2018 Aug;19(8):1040–1050.
   PubMed Web of Science ®Google Scholar
• Bander ED, Ramos AD, Wembacher-Schroeder E, et al. Repeat convection-enhanced delivery for diffuse intrinsic pontine glioma. J Neurosurg Pediatr. 2020;25:1–6.
   Google Scholar
• Debinski W, Gibo DM, Hulet SW, et al. Receptor for interleukin 13 is a marker and therapeutic target for human high-grade gliomas. Clin Cancer Res. 1999 5;May(5):985–990.
   Google Scholar
• Debinski W, Obiri NI, Pastan I, et al. A novel chimeric protein composed of interleukin 13 and Pseudomonas exotoxin is highly cytotoxic to human carcinoma cells expressing receptors for interleukin 13 and interleukin 4. J Biol Chem. 1995 Jul 14;270(28):16775–16780.
   PubMed Web of Science ®Google Scholar
• Debinski W, Obiri NI, Powers SK, et al. Human glioma cells overexpress receptors for interleukin 13 and are extremely sensitive to a novel chimeric protein composed of interleukin 13 and pseudomonas exotoxin. Clin Cancer Res. 1995 Nov;1(11):1253–1258.
   PubMed Web of Science ®Google Scholar
• Heiss JD, Jamshidi A, Shah S, et al. Phase I trial of convection-enhanced delivery of IL13-Pseudomonas toxin in children with diffuse intrinsic pontine glioma. J Neurosurg Pediatr. 2018 Dec 7;23(3):333–342.
   PubMed Web of Science ®Google Scholar
• Mount CW, Majzner RG, Sundaresh S, et al. Potent antitumor efficacy of anti-GD2 CAR T cells in H3-K27M(+) diffuse midline gliomas. Nat Med. 2018 May;24(5):572–579.
   PubMed Web of Science ®Google Scholar
• Majzner RG, Ramakrishna S, Yeom KW, et al. GD2-CAR T cell therapy for H3K27M-mutated diffuse midline gliomas. Nature. 2022 Mar;603(7903):934–941.
   PubMed Web of Science ®Google Scholar
• Hall MD, Odia Y, Allen JE, et al. First clinical experience with DRD2/3 antagonist ONC201 in H3 K27M-mutant pediatric diffuse intrinsic pontine glioma: a case report. J Neurosurg Pediatr. 2019 Apr 5;23(6):719–725.
   PubMed Web of Science ®Google Scholar
• Chi AS, Tarapore RS, Hall MD, et al. Pediatric and adult H3 K27M-mutant diffuse midline glioma treated with the selective DRD2 antagonist ONC201. J Neurooncol. 2019 Oct;145(1):97–105.
   PubMed Web of Science ®Google Scholar
• Duchatel RJ, Mannan A, Woldu AS, et al. Preclinical and clinical evaluation of German-sourced ONC201 for the treatment of H3K27M-mutant diffuse intrinsic pontine glioma. Neurooncol Adv. 2021 January-December;3(1):vdab169.
   PubMedGoogle Scholar
• Gardner SL, Tarapore RS, Allen J, et al. Phase I dose escalation and expansion trial of single agent ONC201 in pediatric diffuse midline gliomas following radiotherapy. Neurooncol Adv. 2022 January-December;4(1):vdac143.
   PubMedGoogle Scholar
• Mueller S, Polley MY, Lee B, et al. Effect of imaging and catheter characteristics on clinical outcome for patients in the PRECISE study. J Neurooncol. 2011 Jan;101(2):267–277.
   PubMed Web of Science ®Google Scholar
• Rechberger JS, Porath KA, Zhang L, et al. IL-13Rα2 status predicts GB-13 (IL13.E13K-PE4E) efficacy in high-grade glioma. Pharmaceutics. 2022 Apr 24;14(5):922.
   PubMed Web of Science ®Google Scholar
• Saunders NA, Simpson F, Thompson EW, et al. Role of intratumoural heterogeneity in cancer drug resistance: molecular and clinical perspectives. EMBO Mol Med. 2012 Aug;4(8):675–684.
   PubMed Web of Science ®Google Scholar
• Greene JM, Levy D, Fung KL, et al. Modeling intrinsic heterogeneity and growth of cancer cells. J Theor Biol. 2015 Feb;21(367):262–277.
   Google Scholar
• Pardridge WM. The blood-brain barrier: bottleneck in brain drug development. NeuroRx. 2005 Jan;2(1):3–14.
   PubMedGoogle Scholar
• Warren KE. Beyond the blood:brain barrier: the importance of Central Nervous System (CNS) pharmacokinetics for the treatment of CNS tumors, including diffuse intrinsic pontine glioma. Front Oncol. 2018;8:239.
   PubMed Web of Science ®Google Scholar
• Bailey S, Howman A, Wheatley K, et al. Diffuse intrinsic pontine glioma treated with prolonged temozolomide and radiotherapy–results of a United Kingdom phase II trial (CNS 2007 04). Eur J Cancer. 2013 Dec;49(18):3856–3862.
   PubMed Web of Science ®Google Scholar
• Subashi E, Cordero FJ, Halvorson KG, et al. Tumor location, but not H3.3K27M, significantly influences the blood-brain-barrier permeability in a genetic mouse model of pediatric high-grade glioma. J Neurooncol. 2016 Jan;126(2):243–251.
   PubMed Web of Science ®Google Scholar
• Zhao R, Pollack GM. Regional differences in capillary density, perfusion rate, and P-glycoprotein activity: a quantitative analysis of regional drug exposure in the brain. Biochem Pharmacol. 2009 Oct 15;78(8):1052–1059.
   PubMed Web of Science ®Google Scholar
• El-Khouly FE, van Vuurden DG, Stroink T, et al. Effective drug delivery in diffuse intrinsic pontine glioma: a theoretical model to identify potential candidates. Front Oncol. 2017;7:254.
   PubMed Web of Science ®Google Scholar
• Griffith JI, Rathi S, Zhang W, et al. Addressing BBB Heterogeneity: a new paradigm for drug delivery to brain tumors. Pharmaceutics. 2020 Dec 11;12(12)1205.
   PubMed Web of Science ®Google Scholar
• Power EA, Rechberger JS, Gupta S, et al. Drug delivery across the blood-brain barrier for the treatment of pediatric brain tumors - An update. Adv Drug Deliv Rev. 2022;185:114303.
   PubMed Web of Science ®Google Scholar
• Bartus RT, Elliott P, Hayward N, et al. Permeability of the blood brain barrier by the bradykinin agonist, RMP-7: evidence for a sensitive, auto-regulated, receptor-mediated system. Immunopharmacology. 1996 Jun;33(1–3):270–278.
   PubMedGoogle Scholar
• Englander ZK, Wei HJ, Pouliopoulos AN, et al. Focused ultrasound mediated blood-brain barrier opening is safe and feasible in a murine pontine glioma model. Sci Rep. 2021 Mar 22;11(1):6521.
   PubMed Web of Science ®Google Scholar
• McCrea HJ, Ivanidze J, O’Connor A, et al. Intraarterial delivery of bevacizumab and cetuximab utilizing blood-brain barrier disruption in children with high-grade glioma and diffuse intrinsic pontine glioma: results of a phase I trial. J Neurosurg Pediatr. 2021;6:1–9.
   Google Scholar
• Kunigelis KE, Vogelbaum MA. Therapeutic delivery to central nervous system. Neurosurg Clin N Am. 2021 Apr;32(2):291–303.
   PubMed Web of Science ®Google Scholar
• Drapeau A, Fortin D. Chemotherapy delivery strategies to the central nervous system: neither optional nor superfluous. Curr Cancer Drug Targets. 2015;15(9):752–768.
   PubMed Web of Science ®Google Scholar
• Patel JP, Spiller SE, Barker ED. Drug penetration in pediatric brain tumors: challenges and opportunities. Pediatr Blood Cancer. 2021 Mar 15:e28983.
   Google Scholar
• Jagannathan J, Walbridge S, Butman JA, et al. Effect of ependymal and pial surfaces on convection-enhanced delivery. J Neurosurg. 2008 Sep;109(3):547–552.
   PubMed Web of Science ®Google Scholar
• Bobo RH, Laske DW, Akbasak A, et al. Convection-enhanced delivery of macromolecules in the brain. Proc Natl Acad Sci U S A. 1994 Mar 15;91(6):2076–2080.
   PubMed Web of Science ®Google Scholar
• Lonser RR, Sarntinoranont M, Morrison PF, et al. Convection-enhanced delivery to the central nervous system. J Neurosurg. 2015 Mar;122(3):697–706.
   PubMed Web of Science ®Google Scholar
• Vogelbaum MA, Sampson JH, Kunwar S, et al. Convection-enhanced delivery of cintredekin besudotox (interleukin-13-PE38QQR) followed by radiation therapy with and without temozolomide in newly diagnosed malignant gliomas: phase 1 study of final safety results. Neurosurgery. 2007 Nov;61(5):1031–1037. discussion 1037–8
   PubMed Web of Science ®Google Scholar
• Zhou Z, Singh R, Souweidane MM. Convection-enhanced delivery for diffuse intrinsic pontine glioma treatment. Curr Neuropharmacol. 2017;15(1):116–128.
   PubMed Web of Science ®Google Scholar
• Morgenstern PF, Zhou Z, Wembacher-Schröder E, et al. Clinical tolerance of corticospinal tracts in convection-enhanced delivery to the brainstem. J Neurosurg. 2018 Dec 21;131(6):1812–1818.
   PubMed Web of Science ®Google Scholar
• Rechberger JS, Power EA, Lu VM, et al. Evaluating infusate parameters for direct drug delivery to the brainstem: a comparative study of convection-enhanced delivery versus osmotic pump delivery. Neurosurg Focus. 2020 Jan 1;48(1):E2.
   PubMed Web of Science ®Google Scholar
• Sampson JH, Brady ML, Petry NA, et al. Intracerebral infusate distribution by convection-enhanced delivery in humans with malignant gliomas: descriptive effects of target anatomy and catheter positioning. Neurosurgery. 2007 Feb;60(2Suppl 1):ONS89–98. discussion ONS98–9
   PubMedGoogle Scholar
• Allard E, Passirani C, Benoit JP. Convection-enhanced delivery of nanocarriers for the treatment of brain tumors. Biomaterials. 2009 Apr;30(12):2302–2318.
   PubMed Web of Science ®Google Scholar
• Singleton WGB, Bienemann AS, Woolley M, et al. The distribution, clearance, and brainstem toxicity of panobinostat administered by convection-enhanced delivery. J Neurosurg Pediatr. 2018 Sep;22(3):288–296.
   PubMed Web of Science ®Google Scholar
• Chen MY, Hoffer A, Morrison PF, et al. Surface properties, more than size, limiting convective distribution of virus-sized particles and viruses in the central nervous system. J Neurosurg. 2005 Aug;103(2):311–319.
   PubMed Web of Science ®Google Scholar
• Healy AT, Vogelbaum MA. Convection-enhanced drug delivery for gliomas. Surg Neurol Int. 2015;6(Suppl 1):S59–67.
   PubMedGoogle Scholar
• Luther N, Zhou Z, Zanzonico P, et al. The potential of theragnostic 124I-8H9 convection-enhanced delivery in diffuse intrinsic pontine glioma. Neuro Oncol. 2014 Jun;16(6):800–806.
   PubMed Web of Science ®Google Scholar
• Louis N, Liu S, He X, et al. New therapeutic approaches for brainstem tumors: a comparison of delivery routes using nanoliposomal irinotecan in an animal model. J Neurooncol. 2018 Feb;136(3):475–484.
   PubMed Web of Science ®Google Scholar
• Sandberg DI, Kharas N, Yu B, et al. High-dose MTX110 (soluble panobinostat) safely administered into the fourth ventricle in a nonhuman primate model. J Neurosurg Pediatr. 2020 May 1;26(2):127–135.
   PubMed Web of Science ®Google Scholar
• Kunwar S, Prados MD, Chang SM, et al. Direct intracerebral delivery of cintredekin besudotox (IL13-PE38QQR) in recurrent malignant glioma: a report by the cintredekin besudotox intraparenchymal study group. J Clin Oncol. 2007 Mar 1;25(7):837–844.
   PubMed Web of Science ®Google Scholar
• Kunwar S, Chang S, Westphal M, et al. Phase III randomized trial of CED of IL13-PE38QQR vs Gliadel wafers for recurrent glioblastoma. Neuro Oncol. 2010 Aug;12(8):871–881.
   PubMed Web of Science ®Google Scholar
• Ivasyk I, Morgenstern PF, Wembacher-Schroeder E, et al. Influence of an intratumoral cyst on drug distribution by convection-enhanced delivery: case report. J Neurosurg Pediatr. 2017 Sep;20(3):256–260.
   PubMed Web of Science ®Google Scholar
• Brady ML, Raghavan R, Mata J, et al. Large-volume infusions into the brain: a comparative study of catheter designs. Stereotact Funct Neurosurg. 2018;96(3):135–141.
   PubMed Web of Science ®Google Scholar
• Brady ML, Grondin R, Zhang Z, et al. In-vitro and in-vivo performance studies of a porous infusion catheter designed for intraparenchymal delivery of therapeutic agents of varying size. J Neurosci Methods. 2022 Aug;1(378):109643.
   Google Scholar
• Lewis O, Woolley M, Johnson D, et al. Chronic, intermittent convection-enhanced delivery devices. J Neurosci Methods. 2016 Feb;1(259):47–56.
   Google Scholar
• Lewis O, Woolley M, Johnson DE, et al. Maximising coverage of brain structures using controlled reflux, convection-enhanced delivery and the recessed step catheter. J Neurosci Methods. 2018 Oct;1(308):337–345.
   Google Scholar
• Wembacher-Schroeder E, Kerstein N, Bander ED, et al. Evaluation of a patient-specific algorithm for predicting distribution for convection-enhanced drug delivery into the brainstem of patients with diffuse intrinsic pontine glioma. J Neurosurg Pediatr. 2021;14:1–9.
   Google Scholar
• Barua NU, Lowis SP, Woolley M, et al. Robot-guided convection-enhanced delivery of carboplatin for advanced brainstem glioma. Acta Neurochir (Wien). 2013 Aug;155(8):1459–1465.
   PubMed Web of Science ®Google Scholar
• Barua NU, Woolley M, Bienemann AS, et al. Intermittent convection-enhanced delivery to the brain through a novel transcutaneous bone-anchored port. J Neurosci Methods. 2013 Apr 15;214(2):223–232.
   PubMed Web of Science ®Google Scholar
• Barua NU, Hopkins K, Woolley M, et al. A novel implantable catheter system with transcutaneous port for intermittent convection-enhanced delivery of carboplatin for recurrent glioblastoma. Drug Deliv. 2016;23(1):167–173.
   PubMed Web of Science ®Google Scholar
• Lopez KA, Tannenbaum AM, Assanah MC, et al. Convection-enhanced delivery of topotecan into a PDGF-driven model of glioblastoma prolongs survival and ablates both tumor-initiating cells and recruited glial progenitors. Cancer Res. 2011 Jun 1;71(11):3963–3971.
   PubMed Web of Science ®Google Scholar
• Sonabend AM, Stuart RM, Yun J, et al. Prolonged intracerebral convection-enhanced delivery of topotecan with a subcutaneously implantable infusion pump. Neuro Oncol. 2011 Aug;13(8):886–893.
   PubMed Web of Science ®Google Scholar
• D’Amico RS, Neira JA, Yun J, et al. Validation of an effective implantable pump-infusion system for chronic convection-enhanced delivery of intracerebral topotecan in a large animal model. J Neurosurg. 2019;2:1–10.
   Google Scholar
• Occhiogrosso G, Edgar MA, Sandberg DI, et al. Prolonged convection-enhanced delivery into the rat brainstem. Neurosurgery. 2003 Feb;52(2):388–393. discussion 393–4
   PubMed Web of Science ®Google Scholar
• Zacharoulis S, Szalontay L, CreveCoeur T, et al. DDEL-07. A Phase I study examining the feasibility of intermittent convection-enhanced delivery (CED) of MTX110 for the treatment of children with newly diagnosed diffuse midline gliomas (DMGs). Neuro Oncol. 2022;24(Supplement_1):i35–i35.
   Google Scholar
• Asthagiri AR, Walbridge S, Heiss JD, et al. Effect of concentration on the accuracy of convective imaging distribution of a gadolinium-based surrogate tracer. J Neurosurg. 2011 Sep;115(3):467–473.
   PubMed Web of Science ®Google Scholar
• Chittiboina P, Heiss JD, Warren KE, et al. Magnetic resonance imaging properties of convective delivery in diffuse intrinsic pontine gliomas. J Neurosurg Pediatr. 2014 Mar;13(3):276–282.
   PubMed Web of Science ®Google Scholar
• Park EJ, Choi J, Lee KC, et al. Emerging PEGylated non-biologic drugs. Expert Opin Emerg Drugs. 2019 Jun;24(2):107–119.
   PubMed Web of Science ®Google Scholar
• Oberoi RK, Mittapalli RK, Elmquist WF. Pharmacokinetic assessment of efflux transport in sunitinib distribution to the brain. J Pharmacol Exp Ther. 2013 Dec;347(3):755–764.
   PubMed Web of Science ®Google Scholar
• Gampa G, Kenchappa RS, Mohammad AS, et al. Enhancing brain retention of a KIF11 inhibitor significantly improves its efficacy in a mouse model of glioblastoma. Sci Rep. 2020 Apr 16;10(1):6524.
   PubMed Web of Science ®Google Scholar
• Koog L, Gandek TB, Nagelkerke A. Liposomes and extracellular vesicles as drug delivery systems: a comparison of composition, pharmacokinetics, and functionalization. Adv Healthc Mater. 2022 March 01;11(5):2100639.
   Web of Science ®Google Scholar
• Song E, Gaudin A, King AR, et al. Surface chemistry governs cellular tropism of nanoparticles in the brain. Nat Commun. 2017 May;19(8):15322.
   Google Scholar
• Chen EM, Quijano AR, Seo YE, et al. Biodegradable PEG-poly(ω-pentadecalactone-co-p-dioxanone) nanoparticles for enhanced and sustained drug delivery to treat brain tumors. Biomaterials. 2018;178:193–203.
   PubMed Web of Science ®Google Scholar
• Panahi Y, Farshbaf M, Mohammadhosseini M, et al. Recent advances on liposomal nanoparticles: synthesis, characterization and biomedical applications. Artif Cells Nanomed Biotechnol. 2017 Jun;45(4):788–799.
   PubMed Web of Science ®Google Scholar
• Antimisiaris SG, Mourtas S, Marazioti A. Exosomes and exosome-inspired vesicles for targeted drug delivery. Pharmaceutics. 2018 Nov 6;10:4.
   Web of Science ®Google Scholar
• Gallitto M, Lazarev S, Wasserman I, et al. Role of radiation therapy in the management of diffuse intrinsic pontine glioma: a systematic review. Adv Radiat Oncol. 2019 July-September;4(3):520–531.
   PubMedGoogle Scholar