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 Table of Contents  
REVIEW ARTICLE
Year : 2016  |  Volume : 12  |  Issue : 2  |  Page : 520-525

Boron neutron capture therapy: Moving toward targeted cancer therapy


1 Department of Immunology, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran
2 Biotechnology Research Center, Mashhad University of Medical Sciences, Mashhad, Iran
3 Department of Genetics and Molecular Biology, School of Medicine, Isfahan University of Medical Science, Isfahan, Iran
4 Department of Microbiology and Virology, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
5 Department of Clinical Biochemistery, Biochemistry and Nutrition Research Center, Mashhad University of Medical Sciences, Mashhad, Iran
6 Nanotechnology Research Center, School of Pharmacy, Mashhad University of Medical Sciences, Mashhad, Iran
7 Department of Medical Biotechnology, School of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

Date of Web Publication25-Jul-2016

Correspondence Address:
Hamed Mirzaei
Department of Medical Biotechnology, School of Medicine, Mashhad University of Medical Sciences, Mashhad 91775-1365
Iran
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0973-1482.176167

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 > Abstract 


Boron neutron capture therapy (BNCT) occurs when a stable isotope, boton-10, is irradiated with low-energy thermal neutrons to yield stripped down helium-4 nuclei and lithium-7 nuclei. It is a binary therapy in the treatment of cancer in which a cytotoxic event is triggered when an atom placed in a cancer cell. Here, we provide an overview on the application of BNCT in cancer therapy as well as current preclinical and clinical evidence on the efficacy of BNCT in the treatment of melanoma, brain tumors, head and neck cancer, and thyroid cancer. Several studies have shown that BNCT is effective in patients who had been treated with a full dose of conventional radiotherapy, because of its selectivity. In addition, BNCT is dependent on the normal/tumor tissue ratio of boron distribution. Increasing evidence has shown that BNCT can be combined with different drug delivery systems to enhance the delivery of boron to cancer cells. The flexibility of BNCT to be used in combination with different tumor-targeting approaches has made this strategy a promising option for cancer therapy. This review aims to provide a state-of-the-art overview of the recent advances in the use of BNCT for targeted therapy of cancer.

Keywords: Boron neutron capture therapy, cancer, radiotherapy


How to cite this article:
Mirzaei HR, Sahebkar A, Salehi R, Nahand JS, Karimi E, Jaafari MR, Mirzaei H. Boron neutron capture therapy: Moving toward targeted cancer therapy. J Can Res Ther 2016;12:520-5

How to cite this URL:
Mirzaei HR, Sahebkar A, Salehi R, Nahand JS, Karimi E, Jaafari MR, Mirzaei H. Boron neutron capture therapy: Moving toward targeted cancer therapy. J Can Res Ther [serial online] 2016 [cited 2019 Dec 15];12:520-5. Available from: http://www.cancerjournal.net/text.asp?2016/12/2/520/176167




 > Introduction Top


Boron neutron capture therapy (BNCT) is based on the atomic response that happens when boron-10 is irradiated with low-energy thermal neutrons to yield high-direct energy exchange α particles and recoiling lithium-7 (7 Li) cores. The concept of BNCT was first introduced by Locher. They highlighted that neutrons have potentially promising application which could be used as therapeutic agents due to their biological effects.[1],[2] The advancement of the BNCT idea with details has precisely been explored by Barth in 2003.[3] In principle, BNCT enables targeted destruction of harmful cells.[4],[5],[6],[7] It is focused around the atomic catch and splitting responses that happen when boton-10 (10 B), which is a nonradioactive form of naturally occurring boron, is irradiated with low-energy thermal neutrons to yield high-linear energy transfer (LET) particles (helium-4) and withdrawing 7 Li cores.[8],[9] To improve the efficacy of BNCT, a sufficient dose of 10 B must be delivered to the tumor site (f20 Ag/g or f109 particles/cell), and enough thermal neutrons must be devoured by them to keep up a fatal 10 B (n, α)7 Li catch reaction. Since the high-LET particles have limited path lengths in tissue (5–9 µm), the hazardous effects of these high-energy particles are limited to boron holding cells. Clinical interest to use BNCT has been focused in the treatment of high-grade glioma,[3] cerebral metastases [10] and melanoma.[11] BNCT is known as a kind of radiation treatment. In this method,10 B and thermal neutrons are used for tumor tissues. Several studies examined BNCT as an effective method in cancer therapy. In a study, Busse et al. investigated the effect of BNCT on patients with primary and metastatic brain tumors. Their results indicated that tumor volume was reduced following BNCT.[3] This method has the potential for killing tumor cells by thermal energy and 10 B agent.[12],[13],[14] Increasing evidence has shown that BNCT can be combined with drug delivery system strategies such as polymeric particles, liposome and monoclonal antibody (mAb) to increase boron delivery to malignant tissues and cancer cells, particularly when combined with targeted agents (e.g., mAb). This review will cover state-of-the-art findings on radiobiological applications of BNCT, clinical results, and critical issues that must be addressed to increase the efficiency of this treatment modality.


 > Application of novel Drug Delivery Systems to Boron Neutron Capture Therapy for Cancer Top


BNCT has been clinically used for the treatment of dangerous brain tumors, advanced melanomas, head and neck malignancy, and hepatoma.[15],[16] Sodium mercaptoundecahydrododecaborate (Na2 10b12 H11 SH: BSH) and boron phenylalanine (10 BPA) are at present being utilized clinically. Molecular compounds are effortlessly cleared from cancer cells and blood, so high-amassing and specific delivery of boron compounds into tumor tissues and malignancy cells are crucial to accomplish compelling BNCT and to dodge harm to nearby normal cells. With a specific goal to attain the particular delivery of atoms to malignant cells, an efficient drug delivery system is demanded.[17] [Figure 1] shows the schematic representation of various drug delivery systems used for BNCT of cancer.
Figure 1: Schematic of various drug delivery systems in boron neutron capture therapy of cancer

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Monoclonal antibody

mAb-based treatment of cancer has been secured as a standout among the best helpful techniques for both hematologic malignancies and solid tumors in the recent 20 years.[18],[19],[20],[21] Barth et al. first reported the application of a mAb for boron delivery systems, using boronated mAb 17-1A in potential neutron capture therapy for colorectal cancer.[22] In other study intended to expand the application of BNCT for the treatment of abdominal cancers, it was attempted to determine whether mAb against alpha-fetoprotein (AFP) could be a useful tool to deliver 10 B to AH-66 hepatoma cells for BNCT. Firstly, mAb was boronated by mixing with 10 B-compound (Cs2 10 B12 H11 SH) using N-succinimidyl 3(2-pyridyldithio) propionate. Numbers of 10 B atoms bound to an antibody molecule were proportional to the dose of 10 B-compound added, and the maximum number of 10 B atoms conjugated to an antibody molecule was approximately 1240. After irradiation with thermal neutron, boronated AH-66 cells showed decreasing uptake of (3H) TdR in comparison with the number of 10 B atoms bound to and/or incorporated into the tumor cells. These results indicate that 10 B atoms delivered by moAb exert cytotoxic effects on AH-66 cells in a dose-dependent manner by thermal neutron irradiation.[23] In another research, examined a targeting model of BNCT to hepatoma cells in vivo with a boronated anti (AFP) mAb. This studies shown that the 10 B-conjugated antitumor moAb could deliver a sufficient amount of 10 B atoms to the tumor cells to induce cytotoxic effects 72 h after injection upon thermal neutron irradiation.[24] Tamat et al., in other study, used boronated mAb 225.28S as neutron capture therapy in malignant melanoma.[25] Barth et al. study delivery of boronated epidermal growth factor (EGF) as a molecular targeting agent with utilizing neutron capture therapy in brain tumors. These data shown that the efficacy of BNCT was significantly increased (P < 0.006), following convection-enhanced delivery of boronated dendrimer-EGF compared to intratumoral injection that the survival data were equivalent to those previously reported by using the boronated antihuman-EGF moAb, C225 (cetuximab).[26] [Table 1] illustrates the application of mAbs for boron delivery systems.
Table 1: Application of monoclonal antibodies as delivery systems in boron neutron capture therapy of cancer

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Polymer

The polymers are known as new materials that can be used for drug targeting. Several studies indicated that these agents can be useful for targeting in several tumors such as melanoma, brain tumor, head and neck, and breast.[30] These agents can be produced chemically. They have several properties that increase the utilizing of them in cancer treatment.[17],[31],[32],[33],[34] In an exploration, Shukla et al. examined folic acid conjugates of boronated polyethylene glycol (PEG) containing 3rd generation polyamidoamine dendrimers to obtain 10 B concentrations necessary for BNCT in malignancy by lessening the uptake of these conjugates by the reticuloendothelial framework. Biodistribution studies with this conjugate in C57bl/6 mice bearing folate receptor (+) murine 24jk-FBP sarcomas obtained particular tumor uptake (6.0% ID/g tumor), high hepatic (38.8% ID/g), and renal (62.8% ID/g) uptake, demonstrating that this polymer can be used as delivery system for drug targeting in cancers.[35] In other study, Suzuki et al. studied intrablood vessel organization of sodium borocaptate (BSH)/lipiodol emulsion delivery 10 B to liver tumors exceptionally specifically as BNCT in the rodent liver model. They demonstrated that i.p. administration of BSH/lipiodol emulsion is a successful system for delivering of 10 B specifically to the liver tumors.[36] In other examination, Suzuki et al. examined the pharmacokinetics of BSH succeeding i.p. administration of BSH with other embolizing operator, degradable starch microspheres (DSM). These data showed that BSH/DSM-BNCT was not suitable for the treatment of distinctive liver tumors on account of the low-T/L 10 B fixation degree. Of course, the high-10 B gathering in the liver tumors succeeding intrablood vessel organization of BSH/DSM emulsion recommends that BSH/DSM-BNCT has the potential for procurement to perilous tumors in diverse areas.[37] [Table 2] illustrates the application of polymers as delivery systems of cancer.
Table 2: Application of polymers as delivery systems of cancer

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Liposomes

Liposomes are widely utilized as carriers for various pharmaceuticals. Furthermore, these carriers can be used for encapsulation to develop delivery systems that can entangle unsteady mixes (for instance, antimicrobials, cell reinforcements, flavors, and bioactive components) and shield their usefulness.[46],[47] Liposomes can trap both hydrophobic and hydrophilic compounds. Hence, they can be used as powerful tools for drug delivery. This system provides suitable environment for different drugs. Liposomes provide effective properties for drugs such as drug targeting, increase half-life, and escape of immune system.[48],[49],[50] Other properties such as biocompatibility, biodegradability, low harmful quality, and bowed to trap both hydrophilic and lipophilic drugs [51] increase the utilizing of these carriers for site-specific drug delivery to tumor tissues.[52],[53],[54] Therefore, liposomes have extended rate both as an investigational system and financially as a drug delivery system.[48],[55],[56] Various studies have been controlled on liposomes with the target of decreasing drug or concentrating on particular cells.[57],[58],[59] Yanagie et al. studied BNCT utilizing 10 B entangled anticarcinoembryonic antigen (CEA) immunoliposome. Their information demonstrated that the immunoliposomes could deliver 10 B molcules to the tumor cells and push cytotoxic impact by thermal neutron. BNCT with immunoliposome may be valuable to the nonresectable threatening tumors in clinical requisition.[60] In other study, Yanagië et al. explored the utilizing of boronated CEA immunoliposome to tumor cell development restraint in vitro by BNCT model. The consequences of this study proposed that immunoliposomes containing the 10 B-compound could go about as a particular and effective transporter of 10 B atoms to target tumor cells by BNCT.[61] In other research, examined inhibition of growth of human breast cancer cells in culture by utilizing of liposomes containing 10 B. This information demonstrated that boronated liposomes can along this line of breast cancer cells in culture to impact cytotoxicity and concealment of development after thermal neutron irradiation.[61] Yanagie et al. examined the using of boron-ensnared stealth liposomes to the hindrance of the development of tumor cells for BNCT in vivo. Their results indicated that intravenous infusion of 10 B-PEG-liposomes can expand the maintenance of 10 B atoms by tumor cells.[62] In other exploration, Maruyama et al. studied intracellular focusing of BSH to suppression tumors by transferrin-PEG liposomes, for BNCT. Their results demonstrated that BSH-typifying TF-PEG liposomes may be helpful as another intracellular targeting carrier in BNCT treatment of diseases.[63] [Table 3] illustrates the application of liposomes and modified liposomes as delivery systems of cancer.
Table 3: Application of liposomes and modified liposomes as delivery systems of cancer

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 > Clinical Studies of Boron Neutron Capture Therapy for Cancer Top


Clinical researches BNCT has centered on the treatment of high-grade glioma and either cutaneous primaries or cerebral metastases of melanoma, head and neck and liver tumor.[78],[79],[80] Neutron sources for BNCT as of now are restricted to atomic reactors, and these are accessible in the United States, Japan, a few European countries and Argentina. [Figure 2] illustrates BNCT therapy for different cancer.[30] Various studies indicated that BNCT can be used as a suitable approach in clinical applications. These studies showed that BNCT have a potential for using in clinical.[30] For example, Sköld et al. explored the capability of BNCT, with L-BPA, as first line radiotherapy (RT) for glioblastoma multiforme (GBM). The survival of patients with recently diagnosed GBM from a Stage II BNCT study was contrasted and those from the two arms of a Stage III study with expected RT versus RT in addition to be associative and adjuvant drug with temozolomide (TMZ). A little subgroup, for which the methylation status of the O(6)-methylguanine-DNA methyltransferase (MGMT) DNA-repair gene was known, was additionally considered. The results showed that the utilization of BNCT with BPA ought to be investigated in a stratified randomized Stage II trial in which patients with the unmethylated MGMT DNA-repair gene are offered BNCT versus RT in addition to TMZ.[81]
Figure 2: Boron neutron capture therapy for different cancer

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 > Conclusion Top


Clinical researches in BNCT have focused primarily on the therapy of high-grade glioma and either cutaneous melanoma, head and neck, thyroid, and liver cancer. BNCT is known as a novel approach for the treatment of various cancers. In addition, this approach may provide suitable and powerful tools in combination with other therapies such as surgery and chemotherapy. With emergence novel drug delivery systems such as polymers, liposomes, and mAbs open new views in treatment cancer with BNCT. These approaches provide effective treatment of BNCT and overcoming to limitations other methods. Finally, two important issues regarding utilizing of BNCT as an approach in cancer therapy remains to be addressed: (i) Insufficient uptake of 10 B-labelled compound within tumor cells and (ii) the lack of efficient imaging methods to monitor the spatial bio-distribution of 10 B-labelled compounds and their pharmacokinetics. BNCT have enhanced because it may become the major modality for the next generation of radiation therapy, cell-selective charged-particle therapy.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
 > References Top

1.
Michiue H, Sakurai Y, Kondo N, Kitamatsu M, Bin F, Nakajima K, et al. The acceleration of boron neutron capture therapy using multi-linked mercaptoundecahydrododecaborate (BSH) fused cell-penetrating peptide. Biomaterials 2014;35:3396-405.  Back to cited text no. 1
    
2.
Kueffer PJ, Maitz CA, Khan AA, Schuster SA, Shlyakhtina NI, Jalisatgi SS, et al. Boron neutron capture therapy demonstrated in mice bearing EMT6 tumors following selective delivery of boron by rationally designed liposomes. Proc Natl Acad Sci U S A 2013;110:6512-7.  Back to cited text no. 2
    
3.
Barth RF. A critical assessment of boron neutron capture therapy: An overview. J Neurooncol 2003;62:1-5.  Back to cited text no. 3
    
4.
Masunaga SI, Sakurai Y, Tano K, Tanaka H, Suzuki M, Kondo N, et al. Effect of bevacizumab combined with boron neutron capture therapy on local tumor response and lung metastasis. Exp Ther Med 2014;8:291-301.  Back to cited text no. 4
    
5.
Miyatake S, Furuse M, Kawabata S, Maruyama T, Kumabe T, Kuroiwa T, et al. Bevacizumab treatment of symptomatic pseudoprogression after boron neutron capture therapy for recurrent malignant gliomas. Report of 2 cases. Neuro Oncol 2013;15:650-5.  Back to cited text no. 5
    
6.
Curran WJ Jr, Scott CB, Horton J, Nelson JS, Weinstein AS, Fischbach AJ, et al. Recursive partitioning analysis of prognostic factors in three Radiation Therapy Oncology Group malignant glioma trials. J Natl Cancer Inst 1993;85:704-10.  Back to cited text no. 6
    
7.
Lacroix M, Abi-Said D, Fourney DR, Gokaslan ZL, Shi W, DeMonte F, et al. A multivariate analysis of 416 patients with glioblastoma multiforme: Prognosis, extent of resection, and survival. J Neurosurg 2001;95:190-8.  Back to cited text no. 7
    
8.
Genady AR, Ioppolo JA, Azaam MM, El-Zaria ME. New functionalized mercaptoundecahydrododecaborate derivatives for potential application in boron neutron capture therapy: Synthesis, characterization and dynamic visualization in cells. Eur J Med Chem 2015;93:574-83.  Back to cited text no. 8
    
9.
Hanaoka K, Watabe T, Naka S, Kanai Y, Ikeda H, Horitsugi G, et al. FBPA PET in boron neutron capture therapy for cancer: Prediction of (10) B concentration in the tumor and normal tissue in a rat xenograft model. EJNMMI Res 2014;4:70.  Back to cited text no. 9
    
10.
Busse PM, Harling OK, Palmer MR, Kiger WS 3rd, Kaplan J, Kaplan I, et al. A critical examination of the results from the Harvard-MIT NCT program phase I clinical trial of neutron capture therapy for intracranial disease. J Neurooncol 2003;62:111-21.  Back to cited text no. 10
    
11.
Mishima Y, Ichihashi M, Nakanishi T, Tsuji M, Nakagawa T. Selective thermal neutron capture therapy of cancer cells using their specific metabolic activity. In: Mishima Y, editor. Cancer Neutron Capture Therapy, 1st ed. New York, Springer; 1996. p. 21-36.  Back to cited text no. 11
    
12.
Alberti D, Protti N, Toppino A, Deagostino A, Lanzardo S, Bortolussi S, et al. A theranostic approach based on the use of a dual boron/Gd agent to improve the efficacy of Boron Neutron Capture Therapy in the lung cancer treatment. Nanomedicine 2015;11:741-50.  Back to cited text no. 12
    
13.
Wongthai P, Hagiwara K, Miyoshi Y, Wiriyasermkul P, Wei L, Ohgaki R, et al. Boronophenylalanine, a boron delivery agent for boron neutron capture therapy, is transported by ATB0,+, LAT1 and LAT2. Cancer Sci 2015;106:279-86.  Back to cited text no. 13
    
14.
Seki K, Kinashi Y, Takahashi S. Influence of p53 status on the effects of boron neutron capture therapy in glioblastoma. Anticancer Res 2015;35:169-74.  Back to cited text no. 14
    
15.
Barth RF, Soloway AH, Fairchild RG. Boron neutron capture therapy of cancer. Cancer Res 1990;50:1061-70.  Back to cited text no. 15
    
16.
Barth RF, Vicente MG, Harling OK, Kiger WS 3rd, Riley KJ, Binns PJ, et al. Current status of boron neutron capture therapy of high grade gliomas and recurrent head and neck cancer. Radiat Oncol 2012;7:146.  Back to cited text no. 16
    
17.
Yanagië H, Ogata A, Sugiyama H, Eriguchi M, Takamoto S, Takahashi H. Application of drug delivery system to boron neutron capture therapy for cancer. Expert Opin Drug Deliv 2008;5:427-43.  Back to cited text no. 17
    
18.
Suzuki M, Kato I, Aihara T, Hiratsuka J, Yoshimura K, Niimi M, et al. Boron neutron capture therapy outcomes for advanced or recurrent head and neck cancer. J Radiat Res 2014;55:146-53.  Back to cited text no. 18
    
19.
Croce M, Corrias MV, Rigo V, Ferrini S. New immunotherapeutic strategies for the treatment of neuroblastoma. Immunotherapy 2015;7:285-300.  Back to cited text no. 19
    
20.
Coulson A, Levy A, Gossell-Williams M. Monoclonal Antibodies in Cancer Therapy: Mechanisms, Successes and Limitations. West Indian Med J 2014;63:650-4.  Back to cited text no. 20
    
21.
Kazemi T, Younesi V, Jadidi-Niaragh F, Yousefi M. Immunotherapeutic approaches for cancer therapy: An updated review. Artif Cells Nanomed Biotechnol; 2015. p. 1-11. [Epub ahead of print].  Back to cited text no. 21
    
22.
Barth RF, Alam F, Soloway AH, Adams DM, Steplewski Z. Boronated monoclonal antibody 17-1A for potential neutron capture therapy of colorectal cancer. Hybridoma 1986;5 Suppl 1:S43-50.  Back to cited text no. 22
    
23.
Takahashi T, Fujii Y, Fujii G, Nariuchi H. Preliminary study for application of anti-alpha-fetoprotein monoclonal antibody to boron-neutron capture therapy. Jpn J Exp Med 1987;57:83-91.  Back to cited text no. 23
    
24.
Yanagië H, Fujii Y, Sekiguchi M, Nariuchi H, Kobayashi T, Kanda K. A targeting model of boron neutron-capture therapy to hepatoma cells in vivo with a boronated anti-(alpha-fetoprotein) monoclonal antibody. J Cancer Res Clin Oncol 1994;120:636-40.  Back to cited text no. 24
    
25.
Tamat SR, Moore DE, Patwardhan A, Hersey P. Boronated monoclonal antibody 225.28S for potential use in neutron capture therapy of malignant melanoma. Pigment Cell Res 1989;2:278-80.  Back to cited text no. 25
    
26.
Barth RF, Wu G, Yang W, Binns PJ, Riley KJ, Patel H, et al. Neutron capture therapy of epidermal growth factor (+) gliomas using boronated cetuximab (IMC-C225) as a delivery agent. Appl Radiat Isot 2004;61:899-903.  Back to cited text no. 26
    
27.
Ranadive GN, Rosenzweig HS, Epperly MW, Bloomer WD. A technique to prepare boronated B72.3 monoclonal antibody for boron neutron capture therapy. Nucl Med Biol 1993;20:1-6.  Back to cited text no. 27
    
28.
Liu L, Barth RF, Adams DM, Soloway AH, Reisfeld RA. Bispecific antibodies as targeting agents for boron neutron capture therapy of brain tumors. J Hematother 1995;4:477-83.  Back to cited text no. 28
    
29.
Yang W, Barth RF, Wu G, Kawabata S, Sferra TJ, Bandyopadhyaya AK, et al. Molecular targeting and treatment of EGFRvIII-positive gliomas using boronated monoclonal antibody L8A4. Clin Cancer Res 2006;12:3792-802.  Back to cited text no. 29
    
30.
Barth RF, Coderre JA, Vicente MG, Blue TE. Boron neutron capture therapy of cancer: Current status and future prospects. Clin Cancer Res 2005;11:3987-4002.  Back to cited text no. 30
    
31.
Scialabba C, Licciardi M, Mauro N, Rocco F, Ceruti M, Giammona G. Inulin-based polymer coated SPIONs as potential drug delivery systems for targeted cancer therapy. Eur J Pharm Biopharm 2014;88:695-705.  Back to cited text no. 31
    
32.
Chiang YT, Lo CL. pH-responsive polymer-liposomes for intracellular drug delivery and tumor extracellular matrix switched-on targeted cancer therapy. Biomaterials 2014;35:5414-24.  Back to cited text no. 32
    
33.
Amin M, Badiee A, Jaafari MR. Improvement of pharmacokinetic and antitumor activity of PEGylated liposomal doxorubicin by targeting with N-methylated cyclic RGD peptide in mice bearing C-26 colon carcinomas. Int J Pharm 2013;458:324-33.  Back to cited text no. 33
    
34.
Rastgoo M, Hosseinzadeh H, Alavizadeh H, Abbasi A, Ayati Z, Jaafari MR. Antitumor activity of PEGylated nanoliposomes containing crocin in mice bearing C26 colon carcinoma. Planta Med 2013;79:447-51.  Back to cited text no. 34
    
35.
Shukla S, Wu G, Chatterjee M, Yang W, Sekido M, Diop LA, et al. Synthesis and biological evaluation of folate receptor-targeted boronated PAMAM dendrimers as potential agents for neutron capture therapy. Bioconjug Chem 2003;14:158-67.  Back to cited text no. 35
    
36.
Suzuki M, Masunaga S, Kinashi Y, Nagata K, Sakurai Y, Nakamatsu K, et al. Intra-arterial administration of sodium borocaptate (BSH)/lipiodol emulsion delivers B-10 to liver tumors highly selectively for boron neutron capture therapy: Experimental studies in the rat liver model. Int J Radiat Oncol Biol Phys 2004;59:260-6.  Back to cited text no. 36
    
37.
Suzuki M, Nagata K, Masunaga S, Kinashi Y, Sakurai Y, Maruhashi A, et al. Biodistribution of 10B in a rat liver tumor model following intra-arterial administration of sodium borocaptate (BSH)/degradable starch microspheres (DSM) emulsion. Appl Radiat Isot 2004;61:933-7.  Back to cited text no. 37
    
38.
Yanagië H, Sato T, Nishi H, Okahata Y, Fujii Y, Eriguchi M. Boron delivery to tumors mediated by polyethylene glycol-binding BSA. Proceeding of 7th international symposium on neutron capture therapy for cancer. In: Larsson B, Carpenter DE, Soloway AH, editors. Advances in Neutron Capture Therapy. New York: Elsevier Science; 1997.  Back to cited text no. 38
    
39.
Kanematsu T, Inokuchi K, Sugimachi K, Furuta T, Sonoda T, Tamura S, et al. Selective effects of lipiodolized antitumor agents. Eur J Surg Oncol 1984;25:218-26.  Back to cited text no. 39
    
40.
Ozawa T, Afzal J, Lamborn KR, Bollen AW, Bauer WF, Koo MS, et al. Toxicity, biodistribution, and convection-enhanced delivery of the boronated porphyrin BOPP in the 9L intracerebral rat glioma model. Int J Radiat Oncol Biol Phys 2005;63:247-52.  Back to cited text no. 40
    
41.
Matsumura A, Shibata Y, Yamamoto T, Yoshida F, Isobe T, Nakai K, et al. A new boronated porphyrin (STA-BX909) for neutron capture therapy: An in vitro survival assay and in vivo tissue uptake study. Cancer Lett 1999;141:203-9.  Back to cited text no. 41
    
42.
Azab AK, Srebnik M, Doviner V, Rubinstein A. Targeting normal and neoplastic tissues in the rat jejunum and colon with boronated, cationic acrylamide copolymers. J Control Release 2005;106:14-25.  Back to cited text no. 42
    
43.
Fukumori Y, Ichikawa H, Nakatani Y. Gadolinium-loaded Chitosan Nanoparticles for Cancer Neutron-capture Therapy: Pharmaceutical Characteristics andIn Vitro Antitumor Effect. AIChE Spring National Meeting – 5th World Congress on Particle Technology; 2006.  Back to cited text no. 43
    
44.
Lai CH, Lin YC, Chou FI, Liang CF, Lin EW, Chuang YJ, et al. Design of multivalent galactosyl carborane as a targeting specific agent for potential application to boron neutron capture therapy. Chem Commun (Camb) 2012;48:612-4.  Back to cited text no. 44
    
45.
Ciani L, Bortolussi S, Postuma I, Cansolino L, Ferrari C, Panza L, et al. Rational design of gold nanoparticles functionalized with carboranes for application in Boron Neutron Capture Therapy. Int J Pharm 2013;458:340-6.  Back to cited text no. 45
    
46.
Nakamura H. Boron lipid-based liposomal boron delivery system for neutron capture therapy: Recent development and future perspective. Future Med Chem 2013;5:715-30.  Back to cited text no. 46
    
47.
Akbarzadeh A, Rezaei-Sadabady R, Davaran S, Joo SW, Zarghami N, Hanifehpour Y, et al. Liposome: Classification, preparation, and applications. Nanoscale Res Lett 2013;8:102.  Back to cited text no. 47
    
48.
Alavizadeh SH, Badiee A, Golmohammadzadeh S, Jaafari MR. The influence of phospholipid on the physicochemical properties and anti-tumor efficacy of liposomes encapsulating cisplatin in mice bearing C26 colon carcinoma. Int J Pharm 2014;473:326-33.  Back to cited text no. 48
    
49.
Benech RO, Kheadr EE, Laridi R, Lacroix C, Fliss I. Inhibition of Listeria innocua in cheddar cheese by addition of nisin Z in liposomes or by in situ production in mixed culture. Appl Environ Microbiol 2002;68:3683-90.  Back to cited text no. 49
    
50.
Shehata T, Ogawara K, Higaki K, Kimura T. Prolongation of residence time of liposome by surface-modification with mixture of hydrophilic polymers. Int J Pharm 2008;359:272-9.  Back to cited text no. 50
    
51.
Johnston MJ, Semple SC, Klimuk SK, Ansell S, Maurer N, Cullis PR. Characterization of the drug retention and pharmacokinetic properties of liposomal nanoparticles containing dihydrosphingomyelin. Biochim Biophys Acta 2007;1768:1121-7.  Back to cited text no. 51
    
52.
Hofheinz RD, Gnad-Vogt SU, Beyer U, Hochhaus A. Liposomal encapsulated anti-cancer drugs. Anticancer Drugs 2005;16:691-707.  Back to cited text no. 52
    
53.
Kalat SA, Khamesipour A, Bavarsad N, Fallah M, Khashayarmanesh Z, Feizi E, et al. Use of topical liposomes containing meglumine antimoniate (Glucantime) for the treatment of L. major lesion in BALB/c mice. Int J Parasitol 2014;143:5-10.  Back to cited text no. 53
    
54.
Shariat S, Badiee A, Jalali SA, Mansourian M, Yazdani M, Mortazavi SA, et al. P5 HER2/neu-derived peptide conjugated to liposomes containing MPL adjuvant as an effective prophylactic vaccine formulation for breast cancer. Cancer Lett 2014;355:54-60.  Back to cited text no. 54
    
55.
Shariat S, Badiee A, Jaafari MR, Mortazavi SA. Optimization of a method to prepare liposomes containing HER2/Neu- derived peptide as a vaccine delivery system for breast cancer. Iran J Pharm Res 2014;13:15-25.  Back to cited text no. 55
    
56.
Mansourian M, Badiee A, Jalali SA, Shariat S, Yazdani M, Amin M, et al. Effective induction of anti-tumor immunity using p5 HER-2/neu derived peptide encapsulated in fusogenic DOTAP cationic liposomes co-administrated with CpG-ODN. Immunol Lett 2014;162 (1 Pt A):87-93.  Back to cited text no. 56
    
57.
Omri A, Suntres ZE, Shek PN. Enhanced activity of liposomal polymyxin B against Pseudomonas aeruginosa in a rat model of lung infection. Biochem Pharmacol 2002;64:1407-13.  Back to cited text no. 57
    
58.
Schiffelers RM, Storm G, Bakker-Woudenberg IA. Host factors influencing the preferential localization of sterically stabilized liposomes in Klebsiella pneumoniae-infected rat lung tissue. Pharm Res 2001;18:780-7.  Back to cited text no. 58
    
59.
Stano P, Bufali S, Pisano C, Bucci F, Barbarino M, Santaniello M, et al. Novel camptothecin analogue (gimatecan)-containing liposomes prepared by the ethanol injection method. J Liposome Res 2004;14:87-109.  Back to cited text no. 59
    
60.
Yanagie H, Fujii Y, Takahashi T, Tomita T, Fukano Y, Hasumi K, et al. Boron neutron capture therapy using 10B entrapped anti-CEA immunoliposome. Hum Cell 1989;2:290-6.  Back to cited text no. 60
    
61.
Yanagië H, Tomita T, Kobayashi H, Fujii Y, Takahashi T, Hasumi K, et al. Application of boronated anti-CEA immunoliposome to tumour cell growth inhibition in in vitro boron neutron capture therapy model. Br J Cancer 1991;63:522-6.  Back to cited text no. 61
    
62.
Yanagie H, Maruyama K, Takizawa T, Ishida O, Ogura K, Matsumoto T, et al. Application of boron-entrapped stealth liposomes to inhibition of growth of tumour cells in the in vivo boron neutron-capture therapy model. Biomed Pharmacother 2006;60:43-50.  Back to cited text no. 62
    
63.
Maruyama K, Ishida O, Kasaoka S, Takizawa T, Utoguchi N, Shinohara A, et al. Intracellular targeting of sodium mercaptoundecahydrododecaborate (BSH) to solid tumors by transferrin-PEG liposomes, for boron neutron-capture therapy (BNCT). J Control Release 2004;98:195-207.  Back to cited text no. 63
    
64.
Yanagië H, Kobayashi H, Takeda Y, Yoshizaki I, Nonaka Y, Naka S, et al. Inhibition of growth of human breast cancer cells in culture by neutron capture using liposomes containing 10B. Biomed Pharmacother 2002;56:93-9.  Back to cited text no. 64
    
65.
Feakes DA, Shelly K, Knobler CB, Hawthorne MF. Na3[B20H17NH3]: Synthesis and liposomal delivery to murine tumors. Proc Natl Acad Sci U S A 1994;91:3029-33.  Back to cited text no. 65
    
66.
Shelly K, Feakes DA, Hawthorne MF, Schmidt PG, Krisch TA, Bauer WF. Model studies directed toward the boron neutron-capture therapy of cancer: Boron delivery to murine tumors with liposomes. Proc Natl Acad Sci U S A 1992;89:9039-43.  Back to cited text no. 66
    
67.
Ishida O, Maruyama K, Tanahashi H, Iwatsuru M, Sasaki K, Eriguchi M, et al. Liposomes bearing polyethyleneglycol-coupled transferrin with intracellular targeting property to the solid tumors in vivo. Pharm Res 2001;18:1042-8.  Back to cited text no. 67
    
68.
Doi A, Kawabata S, Iida K, Yokoyama K, Kajimoto Y, Kuroiwa T, et al. Tumor-specific targeting of sodium borocaptate (BSH) to malignant glioma by transferrin-PEG liposomes: A modality for boron neutron capture therapy. J Neurooncol 2008;87:287-94.  Back to cited text no. 68
    
69.
Pan XQ, Wang H, Lee RJ. Boron delivery to a murine lung carcinoma using folate receptor-targeted liposomes. Anticancer Res 2002;22:1629-33.  Back to cited text no. 69
    
70.
Pan XQ, Wang H, Shukla S, Sekido M, Adams DM, Tjarks W, et al. Boron-containing folate receptor-targeted liposomes as potential delivery agents for neutron capture therapy. Bioconjug Chem 2002;13:435-42.  Back to cited text no. 70
    
71.
Kullberg EB, Wei Q, Capala J, Giusti V, Malmström PU, Gedda L. EGF-receptor targeted liposomes with boronated acridine: Growth inhibition of cultured glioma cells after neutron irradiation. Int J Radiat Biol 2005;81:621-9.  Back to cited text no. 71
    
72.
Peacock GF, Ji B, Wang CK, Lu DR. Cell culture studies of a carborane cholesteryl ester with conventional and PEG liposomes. Drug Deliv 2003;10:29-34.  Back to cited text no. 72
    
73.
Miyajima Y, Nakamura H, Kuwata Y, Lee JD, Masunaga S, Ono K, et al. Transferrin-loaded nido-carborane liposomes: Tumor-targeting boron delivery system for neutron capture therapy. Bioconjug Chem 2006;17:1314-20.  Back to cited text no. 73
    
74.
Nakamura H, Miyajima Y, Kuwata Y, Maruyama K, Masunaga S, Ono K. Transferrin-loaded nido-carborane liposomes. Synthesis and intracellular targeting to solid tumors for boron neutron capture therapy. Proc Natl Acad Sci U S A 1999;96:238-41.  Back to cited text no. 74
    
75.
Heber EM, Hawthorne MF, Kueffer PJ, Garabalino MA, Thorp SI, Pozzi EC, et al. Therapeutic efficacy of boron neutron capture therapy mediated by boron-rich liposomes for oral cancer in the hamster cheek pouch model. Proc Natl Acad Sci U S A 2014;111:16077-81.  Back to cited text no. 75
    
76.
Tachikawa S, Miyoshi T, Koganei H, El-Zaria ME, Viñas C, Suzuki M, et al. Spermidinium closo-dodecaborate-encapsulating liposomes as efficient boron delivery vehicles for neutron capture therapy. Chem Commun (Camb) 2014;50:12325-8.  Back to cited text no. 76
    
77.
Gifford I, Vreeland W, Grdanovska S, Burgett E, Kalinich J, Vergara V, et al. Liposome-based delivery of a boron-containing cholesteryl ester for high-LET particle-induced damage of prostate cancer cells: A boron neutron capture therapy study. Int J Radiat Biol 2014;90:480-5.  Back to cited text no. 77
    
78.
Miyatake S, Kawabata S, Hiramatsu R, Furuse M, Kuroiwa T, Suzuki M. Boron neutron capture therapy with bevacizumab may prolong the survival of recurrent malignant glioma patients: Four cases. Radiat Oncol 2014;9:6.  Back to cited text no. 78
    
79.
Nakai K, Yamamoto T, Kumada H, Matsumura A. Boron neutron capture therapy for glioblastoma: A Phase-I/II clinical trial at JRR-4. Eur Assoc Neurooncol Mag 2014;2010:4.  Back to cited text no. 79
    
80.
Pisarev MA, Dagrosa MA, Thomasz L, Juvenal G. Boron neutron capture therapy applied to undifferentiated thyroid carcinoma. Medicina (B Aires) 2006;66:569-73.  Back to cited text no. 80
    
81.
Sköld 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.  Back to cited text no. 81
    


    Figures

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    Tables

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