CC BY-NC-ND 4.0 · Asian J Neurosurg 2019; 14(01): 5-14
DOI: 10.4103/ajns.AJNS_302_17
Review Article

Convection-enhanced drug delivery for glioblastoma: A systematic review focused on methodological differences in the use of the convection-enhanced delivery method

Bo Halle
1   Department of Neurosurgery, Odense University Hospital and BRIDGE - Brain Research - Inter-Disciplinary Guided Excellence
2   Department of Clinical Research, University of Southern Denmark, Odense
,
Kristian Mongelard
1   Department of Neurosurgery, Odense University Hospital and BRIDGE - Brain Research - Inter-Disciplinary Guided Excellence
2   Department of Clinical Research, University of Southern Denmark, Odense
,
Frantz Poulsen
1   Department of Neurosurgery, Odense University Hospital and BRIDGE - Brain Research - Inter-Disciplinary Guided Excellence
2   Department of Clinical Research, University of Southern Denmark, Odense
› Author Affiliations

Glioblastoma (GBM) is a leading cause of brain cancer-related death. The blood–brain barrier (BBB) prevents the transport of most systemic delivered molecules to the brain. This constitutes a major problem in the therapy of brain tumors. In the last decade, numerous different drug-delivery approaches have been developed to overcome the BBB. The objective of this study is to provide an overview of the methodological aspects used in all preclinical and clinical studies published from 2011 to 2016 where convection-enhanced delivery (CED) was used for drug delivery in the treatment of GBM. A systematic review of English articles published in the past 5 years was undertaken using PubMed and Embase. The search terms (brain tumor [MeSH Terms]) AND (CED OR convection enhanced delivery) were used in PubMed and a similar search was carried out in Embase using their “multi-field search.” All studies using CED on an intracranial GBM model were included. The search resulted in 151 hits after duplicates were removed. In total, 30 studies were included in the review. Of these, two publications studied the technical aspects of the CED method. Furthermore, only one study was a clinical study. The research field is focused on preclinical drug development trials and less emphasis is placed on the CED technique itself. However, it is important that future studies focus on establishing optimal protocols for the use of CED in rodents as well as for big brain models to be able to use the CED method in patients with GBM.

Financial support and sponsorship

Nil.




Publication History

Article published online:
09 September 2022

© 2019. Asian Congress of Neurological Surgeons. This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commercial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/)

Thieme Medical and Scientific Publishers Pvt. Ltd.
A-12, 2nd Floor, Sector 2, Noida-201301 UP, India

 
  • References

  • 1 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;352:987-96.
  • 2 Stupp R, Taillibert S, Kanner AA, Kesari S, Steinberg DM, Toms SA, et al. Maintenance therapy with tumor-treating fields plus temozolomide vs. temozolomide alone for glioblastoma: A Randomized Clinical Trial. JAMA 2015;314:2535-43.
  • 3 Fakhoury M. Drug delivery approaches for the treatment of glioblastoma multiforme. Artif Cells Nanomed Biotechnol 2016;44:1365-73.
  • 4 Bobo RH, Laske DW, Akbasak A, Morrison PF, Dedrick RL, Oldfield EH, et al. Convection-enhanced delivery of macromolecules in the brain. Proc Natl Acad Sci U S A 1994;91:2076-80.
  • 5 Garland L, Gitlitz B, Ebbinghaus S, Pan H, de Haan H, Puri RK, et al. Phase I trial of intravenous IL-4 pseudomonas exotoxin protein (NBI-3001) in patients with advanced solid tumors that express the IL-4 receptor. J Immunother 2005;28:376-81.
  • 6 Lidar Z, Mardor Y, Jonas T, Pfeffer R, Faibel M, Nass D, et al. Convection-enhanced delivery of paclitaxel for the treatment of recurrent malignant glioma: A phase I/II clinical study. J Neurosurg 2004;100:472-9.
  • 7 Laske DW, Youle RJ, Oldfield EH. Tumor regression with regional distribution of the targeted toxin TF-CRM107 in patients with malignant brain tumors. Nat Med 1997;3:1362-8.
  • 8 Weaver M, Laske DW. Transferrin receptor ligand-targeted toxin conjugate (Tf-CRM107) for therapy of malignant gliomas. J Neurooncol 2003;65:3-13.
  • 9 Sampson JH, Akabani G, Archer GE, Bigner DD, Berger MS, Friedman AH, et al. Progress report of a Phase I study of the intracerebral microinfusion of a recombinant chimeric protein composed of transforming growth factor (TGF)-alpha and a mutated form of the pseudomonas exotoxin termed PE-38 (TP-38) for the treatment of malignant brain tumors. J Neurooncol 2003;65:27-35.
  • 10 Weber F, Asher A, Bucholz R, Berger M, Prados M, Chang S, et al. Safety, tolerability, and tumor response of IL4-pseudomonas exotoxin (NBI-3001) in patients with recurrent malignant glioma. J Neurooncol 2003;64:125-37.
  • 11 Allard E, Passirani C, Benoit JP. Convection-enhanced delivery of nanocarriers for the treatment of brain tumors. Biomaterials 2009;30:2302-18.
  • 12 Kunwar S, Chang S, Westphal M, Vogelbaum M, Sampson J, Barnett G, et al. Phase III randomized trial of CED of IL13-PE38QQR vs. gliadel wafers for recurrent glioblastoma. Neuro Oncol 2010;12:871-81.
  • 13 Kunwar S, Chang SM, Prados MD, Berger MS, Sampson JH, Croteau D, et al. Safety of intraparenchymal convection-enhanced delivery of cintredekin besudotox in early-phase studies. Neurosurg Focus 2006;20:E15.
  • 14 Sampson JH, Archer G, Pedain C, Wembacher-Schröder E, Westphal M, Kunwar S, et al. Poor drug distribution as a possible explanation for the results of the PRECISE trial. J Neurosurg 2010;113:301-9.
  • 15 Bouras A, Kaluzova M, Hadjipanayis CG. Radiosensitivity enhancement of radioresistant glioblastoma by epidermal growth factor receptor antibody-conjugated iron-oxide nanoparticles. J Neurooncol 2015;124:13-22.
  • 16 Kaluzova M, Bouras A, Machaidze R, Hadjipanayis CG. Targeted therapy of glioblastoma stem-like cells and tumor non-stem cells using cetuximab-conjugated iron-oxide nanoparticles. Oncotarget 2015;6:8788-806.
  • 17 Wang W, Sivakumar W, Torres S, Jhaveri N, Vaikari VP, Gong A, et al. Effects of convection-enhanced delivery of bevacizumab on survival of glioma-bearing animals. Neurosurg Focus 2015;38:E8.
  • 18 Danhier F, Messaoudi K, Lemaire L, Benoit JP, Lagarce F. Combined anti-galectin-1 and anti-EGFR siRNA-loaded chitosan-lipid nanocapsules decrease temozolomide resistance in glioblastoma:In vivo evaluation. Int J Pharm 2015;481:154-61.
  • 19 Bernal GM, LaRiviere MJ, Mansour N, Pytel P, Cahill KE, Voce DJ, et al. Convection-enhanced delivery and in vivo imaging of polymeric nanoparticles for the treatment of malignant glioma. Nanomedicine 2014;10:149-57.
  • 20 Chen PY, Ozawa T, Drummond DC, Kalra A, Fitzgerald JB, Kirpotin DB, et al. Comparing routes of delivery for nanoliposomal irinotecan shows superior anti-tumor activity of local administration in treating intracranial glioblastoma xenografts. Neuro Oncol 2013;15:189-97.
  • 21 Sonabend AM, Carminucci AS, Amendolara B, Bansal M, Leung R, Lei L, et al. Convection-enhanced delivery of etoposide is effective against murine proneural glioblastoma. Neuro Oncol 2014;16:1210-9.
  • 22 Stephen ZR, Kievit FM, Veiseh O, Chiarelli PA, Fang C, Wang K, et al. Redox-responsive magnetic nanoparticle for targeted convection-enhanced delivery of O6-benzylguanine to brain tumors. ACS Nano 2014;8:10383-95.
  • 23 Zamykal M, Martens T, Matschke J, Günther HS, Kathagen A, Schulte A, et al. Inhibition of intracerebral glioblastoma growth by targeting the insulin-like growth factor 1 receptor involves different context-dependent mechanisms. Neuro Oncol 2015;17:1076-85.
  • 24 Suzuki A, Leland P, Kobayashi H, Choyke PL, Jagoda EM, Inoue T, et al. Analysis of biodistribution of intracranially infused radiolabeled interleukin-13 receptor-targeted immunotoxin IL-13PE by SPECT/CT in an orthotopic mouse model of human glioma. J Nucl Med 2014;55:1323-9.
  • 25 Shultz MD, Wilson JD, Fuller CE, Zhang J, Dorn HC, Fatouros PP, et al. Metallofullerene-based nanoplatform for brain tumor brachytherapy and longitudinal imaging in a murine orthotopic xenograft model. Radiology 2011;261:136-43.
  • 26 Weng KC, Hashizume R, Noble CO, Serwer LP, Drummond DC, Kirpotin DB, et al. Convection-enhanced delivery of targeted quantum dot-immunoliposome hybrid nanoparticles to intracranial brain tumor models. Nanomedicine (Lond) 2013;8:1913-25.
  • 27 Halle B, Marcusson EG, Aaberg-Jessen C, Jensen SS, Meyer M, Schulz MK, et al. Convection-enhanced delivery of an anti-miR is well-tolerated, preserves anti-miR stability and causes efficient target de-repression: A proof of concept. J Neurooncol 2016;126:47-55.
  • 28 Mendiburu-Eliçabe M, Gil-Ranedo J. Combination therapy of intraperitoneal rapamycin and convection- enhanced delivery of nanoliposomal CPT-11 in rodent orthotopic brain tumor xenografts. Curr Cancer Drug Targets 2015;15:352-62.
  • 29 Cooper I, Last D, Guez D, Sharabi S, Elhaik Goldman S, Lubitz I, et al. Combined local blood-brain barrier opening and systemic methotrexate for the treatment of brain tumors. J Cereb Blood Flow Metab 2015;35:967-76.
  • 30 Yang W, Barth RF, Huo T, Nakkula RJ, Weldon M, Gupta N, et al. Radiation therapy combined with intracerebral administration of carboplatin for the treatment of brain tumors. Radiat Oncol 2014;9:25.
  • 31 Xi G, Robinson E, Mania-Farnell B, Vanin EF, Shim KW, Takao T, et al. Convection-enhanced delivery of nanodiamond drug delivery platforms for intracranial tumor treatment. Nanomedicine 2014;10:381-91.
  • 32 Yin D, Zhai Y, Gruber HE, Ibanez CE, Robbins JM, Kells AP, et al. Convection-enhanced delivery improves distribution and efficacy of tumor-selective retroviral replicating vectors in a rodent brain tumor model. Cancer Gene Ther 2013;20:336-41.
  • 33 Huo T, Barth RF, Yang W, Nakkula RJ, Koynova R, Tenchov B, et al. Preparation, biodistribution and neurotoxicity of liposomal cisplatin following convection enhanced delivery in normal and F98 glioma bearing rats. PLoS One 2012;7:e48752.
  • 34 Phillips WT, Goins B, Bao A, Vargas D, Guttierez JE, Trevino A, et al. Rhenium-186 liposomes as convection-enhanced nanoparticle brachytherapy for treatment of glioblastoma. Neuro Oncol 2012;14:416-25.
  • 35 Xi G, Rajaram V, Mania-Farnell B, Mayanil CS, Soares MB, Tomita T, et al. Efficacy of vincristine administered via convection-enhanced delivery in a rodent brainstem tumor model documented by bioluminescence imaging. Childs Nerv Syst 2012;28:565-74.
  • 36 Shi M, Fortin D, Sanche L, Paquette B. Convection-enhancement delivery of platinum-based drugs and lipoplatin (TM) to optimize the concomitant effect with radiotherapy in F98 glioma rat model. Invest New Drugs 2015;33:555-63.
  • 37 Zhang R, Saito R, Mano Y, Sumiyoshi A, Kanamori M, Sonoda Y, et al. Convection-enhanced delivery of SN-38-loaded polymeric micelles (NK012) enables consistent distribution of SN-38 and is effective against rodent intracranial brain tumor models. Drug Deliv 2016;23:2780-6.
  • 38 Hiramatsu R, Kawabata S, Tanaka H, Sakurai Y, Suzuki M, Ono K, et al. Tetrakis (p-carboranylthio-tetrafluorophenyl) Chlorin (TPFC): Application for photodynamic therapy and boron neutron capture therapy. J Pharm Sci 2015;104:962-70.
  • 39 Shi M, Fortin D, Paquette B, Sanche L. Convection-enhancement delivery of liposomal formulation of oxaliplatin shows less toxicity than oxaliplatin yet maintains a similar median survival time in F98 glioma-bearing rat model. Invest New Drugs 2016;34:269-76.
  • 40 Barth RF, Wu G, Meisen WH, Nakkula RJ, Yang W, Huo T, et al. Design, synthesis, and evaluation of cisplatin-containing EGFR targeting bioconjugates as potential therapeutic agents for brain tumors. Onco Targets Ther 2016;9:2769-81.
  • 41 Saucier-Sawyer JK, Seo YE, Gaudin A, Quijano E, Song E, Sawyer AJ, et al. Distribution of polymer nanoparticles by convection-enhanced delivery to brain tumors. J Control Release 2016;232:103-12.
  • 42 Yang X, Saito R, Nakamura T, Zhang R, Sonoda Y, Kumabe T, et al. Peri-tumoral leakage during intra-tumoral convection-enhanced delivery has implications for efficacy of peri-tumoral infusion before removal of tumor. Drug Deliv 2016;23:781-6.
  • 43 Thisgaard H, Halle B, Aaberg-Jessen C, Olsen BB, Therkelsen AS, Dam JH, et al. Highly effective auger-electron therapy in an orthotopic glioblastoma xenograft model using convection-enhanced delivery. Theranostics 2016;6:2278-91.
  • 44 Surapaneni K, Kennedy BC, Yanagihara TK, DeLaPaz R, Bruce JN. Early cerebral blood volume changes predict progression after convection-enhanced delivery of topotecan for recurrent malignant glioma. World Neurosurg 2015;84:163-72.
  • 45 Bruce JN, Fine RL, Canoll P, Yun J, Kennedy BC, Rosenfeld SS, et al. Regression of recurrent malignant gliomas with convection-enhanced delivery of topotecan. Neurosurgery 2011;69:1272-9.
  • 46 Barua NU, Woolley M, Bienemann AS, Johnson DE, Lewis O, Wyatt MJ, et al. Intermittent convection-enhanced delivery to the brain through a novel transcutaneous bone-anchored port. J Neurosci Methods 2013;214:223-232.
  • 47 Selek L, Seigneuret E, Nugue G, Wion D, Nissou MF, Salon C, et al. Imaging and histological characterization of a human brain xenograft in pig: The first induced glioma model in a large animal. J Neurosci Methods 2014;221:159-65.
  • 48 Barua NU, Gill SS, Love S. Convection-enhanced drug delivery to the brain: Therapeutic potential and neuropathological considerations. Brain Pathol 2014;24:117-27.
  • 49 Allen M, Bjerke M, Edlund H, Nelander S, Westermark B. Origin of the U87MG glioma cell line: Good news and bad news. Sci Transl Med 2016;8:1-4.
  • 50 White E, Bienemann A, Malone J, Megraw L, Bunnun C, Wyatt M, et al. An evaluation of the relationships between catheter design and tissue mechanics in achieving high-flow convection-enhanced delivery. J Neurosci Methods 2011;199:87-97.
  • 51 Krauze MT, Saito R, Noble C, Tamas M, Bringas J, Park JW, et al. Reflux-free cannula for convection-enhanced high-speed delivery of therapeutic agents. J Neurosurg 2005;103:923-9.
  • 52 Boucher Y, Baxter LT, Jain RK. Interstitial pressure gradients in tissue-isolated and subcutaneous tumors: Implications for therapy. Cancer Res 1990;50:4478-84.
  • 53 Schomberg D, Wang A, Marshall H, Miranpuri G, Sillay K. Ramped-rate vs. continuous-rate infusions: An in vitro comparison of convection enhanced delivery protocols. Ann Neurosci 2013;20:59-64.
  • 54 Hadjipanayis CG, Machaidze R, Kaluzova M, Wang L, Schuette AJ, Chen H, et al. EGFRvIII antibody-conjugated iron oxide nanoparticles for magnetic resonance imaging-guided convection-enhanced delivery and targeted therapy of glioblastoma. Cancer Res 2010;70:6303-12.
  • 55 Zhou J, Atsina KB, Himes BT, Strohbehn GW, Saltzman WM. Novel delivery strategies for glioblastoma. Cancer J 2012;18:89-99.