Enhancing drug delivery for boron neutron capture therapy of brain tumors with focused ultrasound

Neuro-Oncology

Volumn 15, Issue 9, 2013, Pages 1225-1235

  Alkins, Ryan D ^a,b   Brodersen, Peter M ^c   Sodhi, Rana N S ^c   Hynynen, Kullervo ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b Sunnybrook Health Sciences Centre   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

blood brain barrier; brain tumor barrier; imaging mass spectrometry; neutron capture; therapeutic ultrasound

Indexed keywords

4 BORONOPHENYLALANINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATOMIC EMISSION SPECTROMETRY; BLOOD BRAIN BARRIER; BLOOD VESSEL PERMEABILITY; CONCENTRATION (PARAMETERS); CONTRAST ENHANCEMENT; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; GLIOBLASTOMA; NEUTRON CAPTURE THERAPY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; RAT; ULTRASOUND TRANSDUCER;

BLOOD-BRAIN BARRIER; BRAIN-TUMOR BARRIER; IMAGING MASS SPECTROMETRY; NEUTRON CAPTURE; THERAPEUTIC ULTRASOUND;

ANIMALS; BORON COMPOUNDS; BORON NEUTRON CAPTURE THERAPY; BRAIN NEOPLASMS; CONTRAST MEDIA; DRUG DELIVERY SYSTEMS; FRUCTOSE; GLIOBLASTOMA; MAGNETIC RESONANCE IMAGING; MALE; MICROBUBBLES; RATS; RATS, INBRED F344; ULTRASONIC THERAPY;

EID: 84883201164     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/not052     Document Type: Article

References (56)

1. Halperin EC, Burger PC, Bullard DE. The fallacy of the localized supraten-torial malignant glioma. Int J Radiat Oncol Biol Phys. 1988;15:505-509.
2. Ohgaki H, Dessen P, Jourde B, et al. Genetic pathways to glioblastoma: a population-based study. Cancer Res. 2004;64:6892-6899. (Pubitemid 39330996)
3. Adamson C, Kanu OO, Mehta AI, et al. Glioblastomamultiforme:areview of where we have been and where we are going. Expert Opin Investig Drugs. 2009;18:1061-1083.
4. Stupp R, Mason WP, vandenBent MJ, et al. for the European organisation for research and treatmentofcancer braintumour and radiation oncology groups; National cancer institute of Canada clinical trials group. Radiotherapy plus concomitant and adjuvant temozolomide for glioblas-toma. N Engl J Med. 2005;352:987-996.
5. Stupp R, Hegi ME, Mason WP, et al. for the European organisation for research and treatment of cancer brain tumour and radiation oncology groups; National cancer institute of Canada clinical trials group. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 2009;10:459-466.
6. Szerlip N, Rutter C, Ram N, et al. Factors impacting volumetric white matter changes following whole brain radiation therapy. J Neurooncol. 2011;103:111-119.
7. Crossen JR, Garwood A, Glatstein E, Neuwelt EA. Neurobehavioral sequelae of cranial irradiation in adults: a review of radiation induced encepha-lopathy. J Clin Oncol. 1994;12:627-642. (Pubitemid 24079908)
8. Abbott NJ, Rönnbäck L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci. 2006;7:41-53. (Pubitemid 41828930)
9. Muldoon LL, Soussain C, Jahnke K, et al. Chemotherapy delivery issues in central nervous system malignancy: a reality check. J Clin Oncol. 2007;25:2295-2305. (Pubitemid 46954658)
10. Lockman PR, Mittapalli RK, Taskar KS, et al. Heterogeneous blood-tumor barrier permeability determines drug efficacy in experimental brain metastases of breast cancer. Clin Cancer Res. 2010;16:5664-5678.
11. Coderre JA, Morris GM. The radiation biology of boron neutron capture therapy. Radiat Res. 1999;151:1-18. (Pubitemid 29069340)
12. Barth RF, Coderre JA, Vicente MGH, Blue TE. Boron neutron capture therapy of cancer: current status and future prospects. Clin Cancer Res. 2005;11:3987-4002. (Pubitemid 40791562)
13. Yoshino K, Suzuki A, Mori Y, et al. Improvement of solubility of p-boronophenylalanine by complex formation with monosaccharides. Strahlenther Onkol. 1989;165:127-129. (Pubitemid 19073396)
14. Skold K, Gorlia T, Pellettieri L, Giusti V, H-Stenstam B, Hopewell JW. Boron neutron capture therapy for newly diagnosed glioblastoma multiforme: an assessment of clinical potential. Br J Radiol. 2010;83:596-603.
15. Diaz AZ. Assessment of the results from the phase I/II boron neutron capture therapy trials at the Brookhaven National Laboratory from a clinician's point of view. J Neurooncol. 2003;62:101-109. (Pubitemid 36553120)
16. Barth RF, Yang W, Coderre JA. Rat brain tumor models to assess the effi-cacyof boron neutron capture therapy:acritical evaluation.JNeurooncol. 2003;62:61-74. (Pubitemid 36559478)
17. Smith DR, Chandra S, Barth RF, Yang W, Joel DD, Coderre JA. Quantitative imaging and microlocalizationof boron-10in brain tumors and infiltrating tumorcellsbySIMS ion microscopy: relevancetoneutroncapture therapy. Cancer Res. 2001;61:8179-8187. (Pubitemid 33091610)
18. Joel DD, Coderre JA, Micca PL, Nawrocky MM. Effectofdoseand infusion time on the delivery of p-boronophenylalanine for neutron capture therapy. J Neurooncol. 1999;41:213-221. (Pubitemid 29209809)
19. Hynynen K, McDannold N, Vykhodtseva N, Jolesz FA. Noninvasive MR imaging-guided focal opening of the blood-brain barrier in rabbits. Radiology. 2001;220:640-646. (Pubitemid 32799969)
20. Hynynen K, McDannold N, Sheikov NA, Jolesz FA, Vykhodtseva N. Local and reversible blood-brain barrier disruption by noninvasive focused ultrasound at frequencies suitable for trans-skull sonications. NeuroImage. 2005;24:12-20. (Pubitemid 39611021)
21. w for targeted blood-brain barrier disruption: a feasibility study. Ultrasound Med Biol. 2007;33:584-590. (Pubitemid 46467079)
22. 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. (Pubitemid 39094314)
23. Green GH, Blincoe C, WeethBoron HJ. Boron contamination from borosi-licate glass. J Agric Food Chem. 1976;24:1245-1246.
24. Shibata Y, Zamenhof RG, Busse P, Patel H. Quality control of BPA-f for Harvard-MIT BNCT Clinical Trial [abstract]. 11th World Congress on Neutron Capture Therapy. October 11-15, 2004; Boston, MA.
25. Barth RF. Ratbrain tumor modelsinexperimentalneuro-oncology:the 9L, C6, T9, F98, RG2 (D74), RT-2 and CNS-1 Gliomas. J Neurooncol. 1998;36:91-102. (Pubitemid 28230658)
26. Ausserer WA, Ling YC, Chandra S, Morrison GH. Quantitative imaging of boron, calcium, magnesium, potassium, and sodium distributions in cultured cells with ion microscopy. Anal Chem. 1989;61:2690-2695. (Pubitemid 20065834)
27. Benabdellah F, Seyer A, Quinton L, Touboul D, Brunelle A, Laprévote O. Mass spectrometry imaging of rat brain sections: nanomolar sensitivity with MALDI versus nanometer resolution by TOF-SIMS. Anal Bioanal Chem. 2010;396:151-162.
28. Laakso J, Kulvik M, Ruokonen I, et al. Atomic emission method for total boron in blood during neutron-capture therapy. Clin Chem. 2001;47:1796-1803. (Pubitemid 32881192)
29. Chandra S, Ausserer WA, Morrison GH. Evaluationofmatrix effectsinion microscopic analysis of freeze-fractured, freeze-dried cultured cells. J Microsc. 1987;148:223-239. (Pubitemid 18094888)
30. 23Na MR imaging. Radiology. 2003;227:529-537. (Pubitemid 36514773)
31. Henriksson R, Capala J, Michanek A, et al. Boron neutron capture therapy (BNCT) for glioblastoma multiforme: A phase II study evaluating a prolonged high-dose of boronophenylalanine (BPA). Radiother Oncol. 2008;88:183-191.
32. Kroll RA, Neuwelt EA. Outwitting the blood-brain barrier for therapeutic purposes: osmotic opening and other means. Neurosurgery. 1998;42:1083-1099.
33. Dean RL, Emerich DF, Hasler BP, Bartus RT. Cereport (RMP-7) increases carboplatin levels in brain tumors after pretreatment with dexametha-sone. Neuro Oncol. 1999;1:268-274.
34. Sampson JH, Brady ML, Petry NA, et al. Intracerebral infusate distribution by convection-enhanced deliveryin humans with malignant gliomas: descriptive effects of target anatomy and catheter positioning. Neurosurgery. 2007;60(suppl):ONS89-ONS98.
35. Rainov NG, Sö ling A. Clinical studies with targeted toxins in malignant glioma. Rev Recent Clin Trials. 2006;1:119-131.
36. Kunwar S, Chang S, Westphal M, et al. Phase III randomizedtrialofCEDof IL13-PE38QQR vs Gliadel wafers for recurrent glioblastoma. Neuro Oncol. 2010;12:871-881.
37. Treat LH, McDannold N, Vykhodtseva N, Zhang Y, Tam K, Hynynen K. Targeted delivery of doxorubicin to the rat brain at therapeutic levels using MRI-guided focused ultrasound. Int J Cancer. 2007;121:901-907. (Pubitemid 47106223)
38. Escoffre JM, Piron J, Novell A, Bouakaz A. Doxorubicin delivery into tumor cells with ultrasound and microbubbles. Mol Pharm. 2011;8:799-806.
39. Liu HL, Hua MY, Chen PY, et al. Blood-brain barrier disruption with focused ultrasound enhances deliveryofchemotherapeutic drugs for glio-blastoma treatment. Radiology. 2010;255:415-425.
40. Kinoshita M, McDannold N, Jolesz FA, Hynynen K. Targeted delivery of antibodies through the blood-brain barrier by MRI-guided focused ultrasound. Biochem Biophys Res Commun. 2006;340:1085-1090. (Pubitemid 43083389)
41. Barth RF, Yang W, Rotaru JH, et al. Boron neutron capture therapy of brain tumors: enhanced survival following intracarotid injection of either sodium borocaptateor boronophenylalaninewith orwithout blood-brain barrier disruption. Cancer Res. 1997;57:1129-1136. (Pubitemid 27138613)
42. McDannold N, Arvanitis CD, Vykhodtseva N, Livingstone MS. Temporary disruption of the blood-brain barrier by use of ultrasound and microbub-bles: safety and efficacy evaluation in rhesus macaques. Cancer Res. 2012;72:3652-3663.
43. Xie F, Boska MD, Lof J. Effects of transcranial ultrasound and intravenous microbubbles on blood brain barrier permeability in a large animal model. Ultrasound Med Biol. 2008;34:2028-2034.
44. Jeanmonod D, Werner B, Morel A, et al. Transcranial magnetic resonance imaging-guided focused ultrasound: noninvasive central lateral thalamotomy for chronic neuropathic pain. Neurosurg Focus. 2012;32:E1.
45. Elias WJ, Huss D, Khaled M, et al. ResultsofaphaseIstudyof MR-guided focused ultrasound thalamotomy for essential tremor [abstract]. American Association of Neurological Surgeons 80th Annual Scientific Meeting, April 14-18, 2012, Miami Beach, FL.
46. Detta A, Cruickshank GS. L-amino acid transporter-1 and boronophenylalanine-based boron neutron capture therapy of human brain tumors. Cancer Res. 2009;69:2126-2132.
47. Elowitz EH, Bergland RM, Coderre JA, Joel DD, Chadha M, Chanana AD. Biodistribution of p-boronophenylalanine in patients with glioblastoma multiforme for use in boron neutron capture therapy. Neurosurgery. 1998;42(3):463-468.
48. Morris GM, Micca PL, Coderre JA. The effect of dexamethasone on the uptake of p-boronophenylalanine in the rat brain and intracranial 9L glio-sarcoma. Appl Radiat Isot. 2004;61(5):917-921. (Pubitemid 39092640)
49. Rascher G, Fischmann A, Krö ger S, Duffner F, Grote EH, Wolburg H. Extracellular matrix and the blood-brain barrier in glioblastoma multiforme: spatial segregation of tenascin and agrin. Acta Neuropathol. 2002;104:85-91. (Pubitemid 36075363)
50. Schneider SW, Ludwig T, Tatenhorst L, et al. Glioblastoma cells release factors that disrupt blood-brain barrier features. Acta Neuropathologica. 2004;107:272-276. (Pubitemid 38263418)
51. Ohl CD, Ikink R. Shock-Wave-Induced Jetting of Micron-Size Bubbles. Phys Rev Lett. 2003;90:214502.
52. Kodama T, Tatsuno M, Sugimoto S, Uenohara H, Yoshimoto T, Takayama K. Liquid jets, accelerated thrombolysis:astudy for revascularizationofce-rebral embolism. Ultrasound Med Biol. 1999;25:977-983. (Pubitemid 29325773)
53. Dalecki D. Mechanical bioeffects of ultrasound. Annu Rev Biomed Eng. 2004;6:229-248. (Pubitemid 39209498)
54. Czarnota GJ, Karshafian R, Burns PN, et al. Tumor radiation response en-hancementbyacoustical stimulationofthe vasculature. Proc Natl Acad Sci U S A. 2012;109:E2033-E2041.
55. Hynynen K, Jolesz FA. Demonstration of potential noninvasive ultrasound brain therapy through intact skull. Ultrasound Med Biol. 1998;24:275-283. (Pubitemid 28145716)
56. O'Reilly MA, Hynynen K. Blood-brain barrier: real-time feedback-controlled focused ultrasound disruption by using an acoustic emissions-based controller. Radiology. 2012;263:96-106.