Neurosurgical techniques for disruption of the blood–brain barrier for glioblastoma treatment

Pharmaceutics

Volumn 7, Issue 3, 2015, Pages 175-187

  Rodriguez, Analiz ^a   Tatter, Stephen B ^a   Debinski, Waldemar ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Blood brain barrier; Focused ultrasound; Glioblastoma; Intra arterial drug delivery; Laser interstitial thermotherapy; Non thermal irreversible electroporation

Indexed keywords

BEVACIZUMAB; CARMUSTINE; CETUXIMAB; CYCLOPHOSPHAMIDE; DOXORUBICIN; MANNITOL; METHOTREXATE; PROCARBAZINE; TEMOZOLOMIDE;

ANTINEOPLASTIC ACTIVITY; BLOOD BRAIN BARRIER; CANCER SURVIVAL; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG MECHANISM; DRUG PENETRATION; DRUG RESPONSE; DRUG SAFETY; DRUG TARGETING; GLIOBLASTOMA; HIGH INTENSITY FOCUSED ULTRASOUND; HUMAN; IRREVERSIBLE ELECTROPORATION DEVICE; LASER THERMOTHERAPY; MEMBRANE DAMAGE; NEUROSURGERY; NONHUMAN; OVERALL SURVIVAL; PROGRESSION FREE SURVIVAL; REVIEW; SURGICAL APPROACH; SURGICAL TECHNIQUE;

EID: 84940758944     PISSN: None     EISSN: 19994923     Source Type: Journal    
DOI: 10.3390/pharmaceutics7030175     Document Type: Review

References (70)

1. Dyrna, F.; Hanske, S.; Krueger, M.; Bechmann, I. The blood-brain barrier. J. Neuroimmune Pharmacol. 2013, 8, 763-773.
2. Cardoso, F.L.; Brites, D.; Brito, M.A. Looking at the blood-brain barrier: molecular anatomy and possible investigation approaches. Brain Res. Rev. 2010, 64, 328-363.
3. Winkler, E.A.; Bell, R.D.; Zlokovic, B.V. Central nervous system pericytes in health and disease. Nat. Neurosci. 2011, 14, 1398-1405.
4. Mikitsh, J.L.; Chacko, A.-M. Pathways for small molecule delivery to the central nervous system across the blood-brain barrier. Perspect. Medicin. Chem. 2014, 6, 11-24.
5. Bauer, H.-C.; Krizbai, I.A.; Bauer, H.; Traweger, A. "You Shall Not Pass"-tight junctions of the blood brain barrier. Front. Neurosci. 2014, 8, 392.
6. Jovčevska, I.; Kočevar, N.; Komel, R. Glioma and glioblastoma - how much do we (not) know? Mol. Clin. Oncol. 2013, 1, 935-941.
7. Paw, I.; Carpenter, R.C.; Watabe, K.; Debinski, W.; Lo, H.-W. Mechanisms regulating glioma invasion. Cancer Lett. 2015, 362, 1-7.
8. Woodworth, G.F.; Dunn, G.P.; Nance, E.A.; Hanes, J.; Brem, H. Emerging insights into barriers to effective brain tumor therapeutics. Front. Oncol. 2014, 4, 126.
9. Aiken, R. Molecular neuro-oncology and the challenge of the blood-brain barrier. Semin. Oncol. 2014, 41, 438-445.
10. Zhang, R.D.; Price, J.E.; Fujimaki, T.; Bucana, C.D.; Fidler, I.J. Differential permeability of the blood-brain barrier in experimental brain metastases produced by human neoplasms implanted into nude mice. Am. J. Pathol. 1992, 141, 1115-1124.
11. Watkins, S.; Robel, S.; Kimbrough, I.F.; Robert, S.M.; Ellis-Davies, G.; Sontheimer, H. Disruption of astrocyte-vascular coupling and the blood-brain barrier by invading glioma cells. Nat. Commun. 2014, 5, 4196.
12. Davies, D.C. Blood-brain barrier breakdown in septic encephalopathy and brain tumours. J. Anat. 2002, 200, 639-646.
13. Papadopoulos, M.C.; Saadoun, S.; Binder, D.K.; Manley, G.T.; Krishna, S.; Verkman, A.S. Molecular mechanisms of brain tumor edema. Neuroscience 2004, 129, 1011-1020.
14. Dubois, L.G.; Campanati, L.; Righy, C.; D'Andrea-Meira, I.; de Sampaio e Spohr, T.C.L.; Porto-Carreiro, I.; Pereira, C.M.; Balça-Silva, J.; Kahn, S.A.; DosSantos, M.F.; et al. Gliomas and the vascular fragility of the blood brain barrier. Front. Cell. Neurosci. 2014, 8, 418.
15. Thompson, E.M.; Frenkel, E.P.; Neuwelt, E.A. The paradoxical effect of bevacizumab in the therapy of malignant gliomas. Neurology 2011, 76, 87-93.
16. Van Vulpen, M.; Kal, H.B.; Taphoorn, M.J.B.; El-Sharouni, S.Y. Changes in blood-brain barrier permeability induced by radiotherapy: implications for timing of chemotherapy? Oncol. Rep. 2002, 9, 683-688.
17. Burkhardt, J.-K.; Riina, H.; Shin, B.J.; Christos, P.; Kesavabhotla, K.; Hofstetter, C.P.; Tsiouris, A.J.; Boockvar, J.A. Intra-arterial delivery of bevacizumab after blood-brain barrier disruption for the treatment of recurrent glioblastoma: Progression-free survival and overall survival. World Neurosurg. 2012, 77, 130-134.
18. Bidros, D.S.; Vogelbaum, M.A. Novel drug delivery strategies in neuro-oncology. Neurotherapeutics 2009, 6, 539-546.
19. Miller, G. Drug targeting. Breaking down barriers. Science 2002, 297, 1116-1118.
20. Chi, O.Z.; Wei, H.M.; Lu, X.; Weiss, H.R. Increased blood-brain permeability with hyperosmolar mannitol increases cerebral O2 consumption and O2 supply/consumption heterogeneity. J. Cereb. Blood Flow Metab. 1996, 16, 327-333.
21. Joshi, S.; Ellis, J.A.; Emala, C.W. Revisiting intra-arterial drug delivery for treating brain diseases or is it "déjà-vu, all over again"? J. Neuroanaesth. Crit. Care 2014, 1, 108-115.
22. Shin, B.J.; Burkhardt, J.-K.; Riina, H.A.; Boockvar, J.A. Superselective intra-arterial cerebral infusion of novel agents after blood-brain disruption for the treatment of recurrent glioblastoma multiforme: A technical case series. Neurosurg. Clin. N. Am. 2012, 23, 323-329.
23. Boockvar, J.A.; Tsiouris, A.J.; Hofstetter, C.P.; Kovanlikaya, I.; Fralin, S.; Kesavabhotla, K.; Seedial, S.M.; Pannullo, S.C.; Schwartz, T.H.; Stieg, P.; et al. Safety and maximum tolerated dose of superselective intraarterial cerebral infusion of bevacizumab after osmotic blood-brain barrier disruption for recurrent malignant glioma. J. Neurosurg. 2011, 114, 624-632.
24. Riina, H.A.; Knopman, J.; Greenfield, J.P.; Fralin, S.; Gobin, Y.P.; Tsiouris, A.J.; Souweidane, M.M.; Boockvar, J.A. Balloon-assisted superselective intra-arterial cerebral infusion of bevacizumab for malignant brainstem glioma. A technical note. Interv. Neuroradiol. 2010, 16, 71-76.
25. Yamane, T.; Kaneko, A.; Mohri, M. The technique of ophthalmic arterial infusion therapy for patients with intraocular retinoblastoma. Int. J. Clin. Oncol. 2004, 9, 69-73.
26. Jabbour, P.; Chalouhi, N.; Tjoumakaris, S.; Gonzalez, L.F.; Dumont, A.S.; Chitale, R.; Rosenwasser, R.; Bianciotto, C.G.; Shields, C. Pearls and pitfalls of intraarterial chemotherapy for retinoblastoma. J. Neurosurg. Pediatr. 2012, 10, 175-181.
27. Hynynen, K. Ultrasound for drug and gene delivery to the brain. Adv. Drug Deliv. Rev. 2008, 60, 1209-1217.
28. Holt, R.G.; Roy, R.A. Measurements of bubble-enhanced heating from focused, MHz-frequency ultrasound in a tissue-mimicking material. Ultrasound Med. Biol. 2001, 27, 1399-1412.
29. Kim, Y.; Rhim, H.; Choi, M.J.; Lim, H.K.; Choi, D. High-intensity focused ultrasound therapy: An overview for radiologists. Korean J. Radiol. 2008, 9, 291-302.
30. Hynynen, K.; McDannold, N.; Vykhodtseva, N.; Jolesz, F.A. Noninvasive MR imaging-guided focal opening of the blood-brain barrier in rabbits. Radiology 2001, 220, 640-646.
31. McDannold, N.J.; Vykhodtseva, N.I.; Hynynen, K. Microbubble contrast agent with focused ultrasound to create brain lesions at low power levels: MR imaging and histologic study in rabbits. Radiology 2006, 241, 95-106.
32. Sheikov, N.; McDannold, N.; Vykhodtseva, N.; Jolesz, F.; Hynynen, K. Cellular mechanisms of the blood-brain barrier opening induced by ultrasound in presence of microbubbles. Ultrasound Med. Biol. 2004, 30, 979-989.
33. Chen, H.; Konofagou, E.E. The size of blood-brain barrier opening induced by focused ultrasound is dictated by the acoustic pressure. J. Cereb. Blood Flow Metab. 2014, 34, 1197-1204.
34. Yang, F.-Y.; Ko, C.-E.; Huang, S.-Y.; Chung, I.-F.; Chen, G.-S. Pharmacokinetic changes induced by focused ultrasound in glioma-bearing rats as measured by dynamic contrast-enhanced MRI. PLoS ONE 2014, 9, e92910.
35. Aryal, M.; Vykhodtseva, N.; Zhang, Y.-Z.; Park, J.; McDannold, N. Multiple treatments with liposomal doxorubicin and ultrasound-induced disruption of blood-tumor and blood-brain barriers improve outcomes in a rat glioma model. J. Control. Release 2013, 169, 103-111.
36. Liu, H.-L.; Huang, C.-Y.; Chen, J.-Y.; Wang, H.-Y.J.; Chen, P.-Y.; Wei, K.-C. Pharmacodynamic and therapeutic investigation of focused ultrasound-induced blood-brain barrier opening for enhanced temozolomide delivery in glioma treatment. PLoS ONE 2014, 9, e114311.
37. Yang, F.-Y.; Wong, T.-T.; Teng, M.-C.; Liu, R.-S.; Lu, M.; Liang, H.-F.; Wei, M.-C. Focused ultrasound and interleukin-4 receptor-targeted liposomal doxorubicin for enhanced targeted drug delivery and antitumor effect in glioblastoma multiforme. J. Control. Release 2012, 160, 652-658.
38. Diaz, R.J.; McVeigh, P.Z.; O'Reilly, M.A.; Burrell, K.; Bebenek, M.; Smith, C.; Etame, A.B.; Zadeh, G.; Hynynen, K.; Wilson, B.C.; et al. Focused ultrasound delivery of Raman nanoparticles across the blood-brain barrier: Potential for targeting experimental brain tumors. Nanomedicine 2014, 10, 1075-1087.
39. Huber, P.E.; Pfisterer, P. In vitro and in vivo transfection of plasmid DNA in the Dunning prostate tumor R3327-AT1 is enhanced by focused ultrasound. Gene Ther. 2000, 7, 1516-1525.
40. Kinoshita, M.; McDannold, N.; Jolesz, F.A.; Hynynen, K. Targeted delivery of antibodies through the blood-brain barrier by MRI-guided focused ultrasound. Biochem. Biophys. Res. Commun. 2006, 340, 1085-1090.
41. Alonso, A. Ultrasound-induced blood-brain barrier opening for drug delivery. Front. Neurol. Neurosci. 2015, 36, 106-115.
42. McDannold, N.; Clement, G.T.; Black, P.; Jolesz, F.; Hynynen, K. Transcranial magnetic resonance imaging-guided focused ultrasound surgery of brain tumors: Initial findings in 3 patients. Neurosurgery 2010, 66, 323-332.
43. Coluccia, D.; Fandino, J.; Schwyzer, L.; O'Gorman, R.; Remonda, L.; Anon, J.; Martin, E.; Werner, B. First noninvasive thermal ablation of a brain tumor with MR-guided focused ultrasound. J. Ther. Ultrasound 2014, 2, 17.
44. Iancu, C.; Mocan, L. Advances in cancer therapy through the use of carbon nanotube-mediated targeted hyperthermia. Int. J. Nanomedicine 2011, 6, 1675-1684.
45. Stafford, R.J.; Fuentes, D.; Elliott, A.A.; Weinberg, J.S.; Ahrar, K. Laser-induced thermal therapy for tumor ablation. Crit. Rev. Biomed. Eng. 2010, 38, 79-100.
46. Jethwa, P.R.; Barrese, J.C.; Gowda, A.; Shetty, A.; Danish, S.F. Magnetic resonance thermometryguided laser-induced thermal therapy for intracranial neoplasms: Initial experience. Neurosurgery 2012, 71, 133-145.
47. Sloan, A.E.; Ahluwalia, M.S.; Valerio-Pascua, J.; Manjila, S.; Torchia, M.G.; Jones, S.E.; Sunshine, J.L.; Phillips, M.; Griswold, M.A.; Clampitt, M.; et al. Results of the NeuroBlate System first-in-humans Phase I clinical trial for recurrent glioblastoma: Clinical article. J. Neurosurg. 2013, 118, 1202-1219.
48. Torres-Reveron, J.; Tomasiewicz, H.C.; Shetty, A.; Amankulor, N.M.; Chiang, V.L. Stereotactic laser induced thermotherapy (LITT): A novel treatment for brain lesions regrowing after radiosurgery. J. Neurooncol. 2013, 113, 495-503.
49. Carpentier, A.; McNichols, R.J.; Stafford, R.J.; Itzcovitz, J.; Guichard, J.-P.; Reizine, D.; Delaloge, S.; Vicaut, E.; Payen, D.; Gowda, A.; et al. Real-time magnetic resonance-guided laser thermal therapy for focal metastatic brain tumors. Neurosurgery 2008, 63, 21-29.
50. Carpentier, A.; Chauvet, D.; Reina, V.; Beccaria, K.; Leclerq, D.; McNichols, R.J.; Gowda, A.; Cornu, P.; Delattre, J.-Y. MR-guided laser-induced thermal therapy (LITT) for recurrent glioblastomas. Lasers Surg. Med. 2012, 44, 361-368.
51. Lee Titsworth, W.; Murad, G.J.A.; Hoh, B.L.; Rahman, M. Fighting fire with fire: The revival of thermotherapy for gliomas. Anticancer Res. 2014, 34, 565-574.
52. Hawasli, A.H.; Ray, W.Z.; Murphy, R.K.J.; Dacey, R.G.; Leuthardt, E.C. Magnetic resonance imaging-guided focused laser interstitial thermal therapy for subinsular metastatic adenocarcinoma: Technical case report. Neurosurgery 2012, 70, 332-338.
53. Mohammadi, A.M.; Hawasli, A.H.; Rodriguez, A.; Schroeder, J.L.; Laxton, A.W.; Elson, P.; Tatter, S.B.; Barnett, G.H.; Leuthardt, E.C. The Role of Laser Interstitial Thermal Therapy in Enhancing Progression Free Survival of Difficult-to-Access High Grade Gliomas: A Multi-Center Study. Cancer 2014, 3, 971-979.
54. Schober, R.; Bettag, M.; Sabel, M.; Ulrich, F.; Hessel, S. Fine structure of zonal changes in experimental Nd:YAG laser-induced interstitial hyperthermia. Lasers Surg. Med. 1993, 13, 234-241.
55. Hawasli, A.H.; Kim, A.H.; Dunn, G.P.; Tran, D.D.; Leuthardt, E.C. Stereotactic laser ablation of high-grade gliomas. Neurosurg. Focus 2014, 37, E1.
56. Nakagawa, M.; Matsumoto, K.; Higashi, H.; Furuta, T.; Ohmoto, T. Acute effects of interstitial hyperthermia on normal monkey brain--magnetic resonance imaging appearance and effects on blood-brain barrier. Neurol. Med. Chir. 1994, 34, 668-675.
57. Tsong, T.Y. Electroporation of cell membranes. Biophys. J. 1991, 60, 297-306.
58. Golberg, A.; Yarmush, M.L. Nonthermal irreversible electroporation: Fundamentals, applications, and challenges. IEEE Trans. Biomed. Eng. 2013, 60, 707-714.
59. Ellis, T.L.; Garcia, P.A.; Rossmeisl, J.H.; Henao-Guerrero, N.; Robertson, J.; Davalos, R.V. Nonthermal irreversible electroporation for intracranial surgical applications. Laboratory investigation. J. Neurosurg. 2011, 114, 681-688.
60. Hjouj, M.; Last, D.; Guez, D.; Daniels, D.; Sharabi, S.; Lavee, J.; Rubinsky, B.; Mardor, Y. MRI study on reversible and irreversible electroporation induced blood brain barrier disruption. PLoS ONE 2012, 7, e42817.
61. Garcia, P.A.; Rossmeisl, J.H.; Robertson, J.L.; Olson, J.D.; Johnson, A.J.; Ellis, T.L.; Davalos, R.V. 7.0-T magnetic resonance imaging characterization of acute blood-brain-barrier disruption achieved with intracranial irreversible electroporation. PLoS ONE 2012, 7, e50482.
62. Rossmeisl, J.H.; Garcia, P.A.; Roberston, J.L.; Ellis, T.L.; Davalos, R.V. Pathology of non-thermal irreversible electroporation (N-TIRE)-induced ablation of the canine brain. J. Vet. Sci. 2013, 14, 433-440.
63. Garcia, P.A.; Pancotto, T.; Rossmeisl, J.H.; Henao-Guerrero, N.; Gustafson, N.R.; Daniel, G.B.; Robertson, J.L.; Ellis, T.L.; Davalos, R.V. Non-thermal irreversible electroporation (N-TIRE) and adjuvant fractionated radiotherapeutic multimodal therapy for intracranial malignant glioma in a canine patient. Technol. Cancer Res. Treat. 2011, 10, 73-83.
64. Gidwani, M.; Singh, A.V. Nanoparticle enabled drug delivery across the blood brain barrier: In vivo and in vitro models, opportunities and challenges. Curr. Pharm. Biotechnol. 2014, 14, 1201-1212.
65. Gong, W.; Wang, Z.; Liu, N.; Lin, W.; Wang, X.; Xu, D.; Liu, H.; Zeng, C.; Xie, X.; Mei, X.; et al. Improving efficiency of adriamycin crossing blood brain barrier by combination of thermosensitive liposomes and hyperthermia. Biol. Pharm. Bull. 2011, 34, 1058-1064.
66. Foley, C.P.; Rubin, D.G.; Santillan, A.; Sondhi, D.; Dyke, J.P.; Pierre Gobin, Y.; Crystal, R.G.; Ballon, D.J. Intra-arterial delivery of AAV vectors to the mouse brain after mannitol mediated blood brain barrier disruption. J. Control. Release 2014, 196, 71-78.
67. Ben-Zvi, A.; Lacoste, B.; Kur, E.; Andreone, B.J.; Mayshar, Y.; Yan, H.; Gu, C. Mfsd2a is critical for the formation and function of the blood-brain barrier. Nature 2014, 509, 507-511.
68. Al-Shehri, A.; Favretto, M.E.; Ioannou, P.V.; Romero, I.A.; Couraud, P.-O.; Weksler, B.B.; Parker, T.L.; Kallinteri, P. Permeability of PEGylated Immunoarsonoliposomes Through In Vitro Blood Brain Barrier-Medulloblastoma Co-culture Models for Brain Tumor Therapy. Pharm. Res. 2015, 32, 1072-1083.
69. Bicker, J.; Alves, G.; Fortuna, A.; Falcão, A. Blood-brain barrier models and their relevance for a successful development of CNS drug delivery systems: A review. Eur. J. Pharm. Biopharm. 2014, 87, 409-432.
70. Chassidim, Y.; Vazana, U.; Prager, O.; Veksler, R.; Bar-Klein, G.; Schoknecht, K.; Fassler, M.; Lublinsky, S.; Shelef, I. Analyzing the blood-brain barrier: The benefits of medical imaging in research and clinical practice. Semin. Cell Dev. Biol. 2015, 38, 43-52.