A study on the possibility of drug delivery approach through ultrasonic sensitive nanocarriers

Document Type : Review Paper

Authors

1 Nanobiotechnology Research Center, Baqiyatallah University of Medical Sciences, Tehran, Iran

2 Radiation Biology Research Center, Iran University of Medical Sciences (IUMS), Tehran, Iran

3 Department of Medical Nanotechnology, School of Advanced Technologies in Medicine, Iran University of Medical Sciences (IUMS), Tehran, Iran

4 Department of Medical Nanotechnology, School of Advanced Technologies in Medicine (SATiM), Tehran University of Medical Sciences (TUMS), Tehran, Iran

5 Department of Nursing, School of Nursing and Midwifery, Lorestan University of Medical Sciences, Boroujerd, Iran

6 Department of Physiotherapy, University of Social Welfare and Rehabilitation Sciences, Tehran, Iran

Abstract

Physical drug delivery through smart nanocarrier and external stimulus could lead to significant improvements of drug potency as well as noticeable decrease in unwanted side effects. Currently, many external energy sources such as light, magnetic fields, ultrasound, ...,  are under investigation as external stimulus for physical drug delivery. The purpose of this paper is to review most recent developments of triggered release of drugs and biomolecules under external ultrasound exposure. A special attention has also been paid to the metal nanostructures for ultrasound mediated drug delivery and also, other nanostructures were also considered. We briefly introduced ultrasound regulation and safety consideration. Further it is concluded that the use of nanostructures for delivery of active biomolecules in combination with ultrasound as a stimulus to trigger drug release from the nanocarriers and increased drug penetration has gained much attention for effective drug delivery and overcoming difficulties of multi-drug resistance of cancer.

Keywords

References

1.Hill C. Medical ultrasonics: an historical review. BJR. 1973; 46(550): 899-905.
2.Feril LB, Jr., Tachibana K. Use of ultrasound in drug delivery systems: emphasis on experimental methodology and mechanisms. Int J Hyperthermia. 2012; 28(4): 282-289.
3.Mitragotri S. Healing sound: the use of ultrasound in drug delivery and other therapeutic applications. Nat Rev Drug Discov. 2005; 4(3): 255-260.
4.Liu Y, Miyoshi H, Nakamura M. Encapsulated ultrasound microbubbles: therapeutic application in drug/gene delivery. J Control Release. 2006; 114(1): 89-99.
5.Nabili M, Patel H, Mahesh SP, Liu J, Geist C, Zderic V. Ultrasound-Enhanced Delivery of Antibiotics and Anti-Inflammatory Drugs Into the Eye. Ultrasound Med Biol. 2013; 39(4): 638-646.
6.Qiu-Lan Zhou, Zhi-Yi Chen, Yi-Xiang Wang, Feng Yang, Yan Lin, and Yang-Ying Liao, “Ultrasound-Mediated Local Drug and Gene Delivery Using Nanocarriers,” BioMed Research International, 2014, Epub.
7.Cho K, Wang X, Nie S, Shin DM. Therapeutic nanoparticles for drug delivery in cancer. Clin. Cancer Res. 2008; 14(5): 1310-1316.
8.Lavon I, Kost J. Ultrasound and transdermal drug delivery. Drug Discov Today. 2004; 9(15): 670-676.
9.Paliwal S, Menon GK, Mitragotri S. Low-frequency sonophoresis: ultrastructural basis for stratum corneum permeability assessed using quantum dots. J Investig Dermatol. 2006; 126(5): 1095-1101.
10.Yang F, Zhang M, He W, Chen P, Cai X, Yang L, Ning G,  Junru W. Controlled release of Fe3O4 nanoparticles in encapsulated microbubbles to tumor cells via sonoporation and associated cellular bioeffects. Small. 2011; 7(7): 902-910.
11.Jing Y, Zhu Y, Yang X, Shen J, Li C. Ultrasound-triggered smart drug release from multifunctional core− shell capsules one-step fabricated by coaxial electrospray method. Langmuir. 2010; 27(3): 1175-1180.
12.Hoskins PR, Martin K, Thrush A. Diagnostic ultrasound: physics and equipment: Cambridge University Press; 2010.
13.Yagi N, Oshiro Y, Ishikawa T, Hata Y, editors. Ultrasonic image synthesis in fourier transform. World Automation Congress (WAC), 2012; 2012: IEEE.
14.Beutel J, Kundel HL, Van Metter RL. Handbook of Medical Imaging, volume 1: Physics and Psychophysics. 2000.
15.Kennedy JE. High-intensity focused ultrasound in the treatment of solid tumours. Nat Rev Cancer. 2005; 5(4): 321-327.
16.Wells P. Absorption and dispersion of ultrasound in biological tissue. Ultrasound Med Biol. 1975; 1(4): 369-376.
17.Mo S, Coussios C-C, Seymour L, Carlisle R. Ultrasound-enhanced drug delivery for cancer. Expert Opin Drug Deliv. 2012; 9(12): 1525-1538.
18.Alippi A, Galbato A, Cataldo F. Ultrasound cavitation in sonochemistry: decomposition of carbon tetrachloride in aqueous solutions of potassium iodide. Ultrasonics. 1992; 30(3): 148-151.
19.Barnett S, Ter Haar G, Ziskin M, Nyborg W, Maeda K, Bang J. Current status of research on biophysical effects of ultrasound. Ultrasound Med Biol. 1994; 20(3): 205-218.
20.Liu RH, Lenigk R, Druyor-Sanchez RL, Yang J, Grodzinski P. Hybridization enhancement using cavitation microstreaming. Anal. Chem. 2003; 75(8): 1911-1917.
21.Husseini GA, Pitt WG. Micelles and nanoparticles for ultrasonic drug and gene delivery. Adv. Drug Deliv. Rev. 2008; 60(10): 1137-1152.
22.Pitt WG, Husseini GA, Staples BJ. Ultrasonic drug delivery–a general review. Expert Opin Drug Deliv. 2004; 1(1): 37-56.
23.Suzuki R, Oda Y, Utoguchi N, Maruyama K. Progress in the development of ultrasound-mediated gene delivery systems utilizing nano-and microbubbles. J Control Release. 2011; 149(1): 36-41.
24.Apfel RE, Holland CK. Gauging the likelihood of cavitation from short-pulse, low-duty cycle diagnostic ultrasound. Ultrasound Med Biol. 1991; 17(2): 179-185.
25.ter Haar G. High intensity ultrasound. Surgical Innovation. 2001; 8(1): 77-89.
26.Wu F, Wang Z-B, Chen W-Z, Zou J-Z, Bai J, Zhu H, et al. Extracorporeal focused ultrasound surgery for treatment of human solid carcinomas: early Chinese clinical experience. Ultrasound Med Biol. 2004; 30(2): 245-260.
27.Dromi S, Frenkel V, Luk A, Traughber B, Angstadt M, Bur M, et al. Pulsed-high intensity focused ultrasound and low temperature–sensitive liposomes for enhanced targeted drug delivery and antitumor effect. Clin Cancer Res. 2007; 13(9) :2722-2727.
28.Linet MS, pyo Kim K, Rajaraman P. Children’s exposure to diagnostic medical radiation and cancer risk: epidemiologic and dosimetric considerations. Pediatric radiology. 2009; 39(1): 4-26.
29.Suslick KS. Ultrasound: its chemical, physical, and biological effects: VCH Publishers; 1988.
30.Lubbers J, Hekkenberg RT, Bezemer RA. Time to threshold (< i> TT), a safety parameter for heating by diagnostic ultrasound. Ultrasound Med Biol. 2003; 29(5): 755-764.
31.Williams AR. Ultrasound: biological effects and potential hazards: Academic Press New York; 1983.
32.Mitragotri S, Edwards DA, Blankschtein D, Langer R. A mechanistic study of ultrasonically‐enhanced transdermal drug delivery. J Pharm Sci. 1995; 84(6): 697-706.
33.Levy D, Kost J, Meshulam Y, Langer R. Effect of ultrasound on transdermal drug delivery to rats and guinea pigs. J Clin Invest. 1989; 83(6): 2074.
34.Mitragotri S, Blankschtein D, Langer R. Ultrasound-mediated transdermal protein delivery. SCIENCE-NEW YORK THEN WASHINGTON-. 1995:850-.
35.Mitragotri S, Blankschtein D, Langer R. Transdermal drug delivery using low-frequency sonophoresis. Pharm. Res. 1996; 13(3): 411-420.
36.Mitragotri S, Kost J. Transdermal delivery of heparin and low-molecular weight heparin using low-frequency ultrasound. Pharm. Res. 2001; 18(8): 1151-1156.
37.Yamashita N, Tachibana K, Ogawa K, Tsujita N, Tomita A. Scanning electron microscopic evaluation of the skin surface after ultrasound exposure. Anat. Rec. 1997;247(4):455-61.
38.Illing R, Kennedy J, Wu F, Ter Haar G, Protheroe A, Friend P, et al. The safety and feasibility of extracorporeal high-intensity focused ultrasound (HIFU) for the treatment of liver and kidney tumours in a Western population. Br J Cancer. 2005; 93(8): 890-895.
39.Kennedy J, Ter Haar G, Cranston D. High intensity focused ultrasound: surgery of the future? BJR. 2003; 76(909): 590-599.
40.Oosterhof G, Cornel E, Smits G, Debruyne F, Schalken J. Influence of high-intensity focused ultrasound on the development of metastases. Eur Urol. 1996; 32(1): 91-95.
41.Hancock H, Dreher MR, Crawford N, Pollock CB, Shih J, Wood BJ. Evaluation of pulsed high intensity focused ultrasound exposures on metastasis in a murine model. Clin Exp Metastasis. 2009; 26(7): 729-738.
42.Lindner JR, Kaul S. Delivery of drugs with ultrasound. Echocardiography. 2001; 18(4): 329-337.
43.Grayburn PA. Current and future contrast agents. Echocardiography. 2002; 19(3): 259-65.
44.Klibanov AL. Microbubble contrast agents: targeted ultrasound imaging and ultrasound-assisted drug-delivery applications. Invest Radiol. 2006; 41(3): 354-362.
45.Schroeder A, Kost J, Barenholz Y. Ultrasound, liposomes, and drug delivery: principles for using ultrasound to control the release of drugs from liposomes. Chem Phys Lipids. 2009; 162(1): 1-16.
46.Pong M, Umchid S, Guarino AJ, Lewin PA, Litniewski J, Nowicki A, et al. In vitro ultrasound-mediated leakage from phospholipid vesicles. Ultrasonics. 2006; 45(1): 133-145.
47.Kimura A, Sakai A, Tsukishiro S-i, BEPPU S, FuJIwARA H. Preparation and characterization of echogenic liposome as an ultrasound contrast agent: size-dependency and stabilizing effect of cholesterol on the echogenicity of gas-entrapping liposome. Chem Pharm Bull. 1998; 46(10): 1493-1496.
48.Huang S-L. Liposomes in ultrasonic drug and gene delivery. Adv. Drug Deliv. Rev. 2008;60(10):1167-76.
49.Kheirolomoom A, Dayton PA, Lum AF, Little E, Paoli EE, Zheng H,. Acoustically-active microbubbles conjugated to liposomes: characterization of a proposed drug delivery vehicle. J Control Release. 2007; 118(3): 275.
50.Huang S-L, McPherson DD, MacDonald RC. A method to co-encapsulate gas and drugs in liposomes for ultrasound-controlled drug delivery. Ultrasound Med Biol. 2008; 34(8): 1272-1280.
51.Husseini GA, Pitt WG. Ultrasonic‐activated micellar drug delivery for cancer treatment. J Pharm Sci. 2009; 98(3): 795-811.
52.Rapoport N, Christensen D, Fain H, Barrows L, Gao Z. Ultrasound-triggered drug targeting of tumors in vitro and in vivo. Ultrasonics. 2004; 42(1-9): 943-950.
53.Miller DW, Batrakova EV, Waltner TO, Alakhov VY, Kabanov AV. Interactions of pluronic block copolymers with brain microvessel endothelial cells: evidence of two potential pathways for drug absorption. Bioconjug Chem. 1997; 8(5): 649-657.
54.You J, Zhang G, Li C. Exceptionally high payload of doxorubicin in hollow gold nanospheres for near-infrared light-triggered drug release. ACS nano. 2010; 4(2):1033-1041.
55.Amini SM, Kharrazi S, Hadizadeh M, Fateh M, Saber R. Effect of gold nanoparticles on photodynamic efficiency of 5-aminolevolenic acid photosensitiser in epidermal carcinoma cell line: an in vitro study. IET Nanobiotechnol [Internet]. 2013; 7(4): 151-156.
56.Darabpour E, Kashef N, Amini SM, Kharrazi S, Djavid GE. Fast and effective photodynamic inactivation of 4-day-old biofilm of methicillin-resistant Staphylococcus aureus using methylene blue-conjugated gold nanoparticles. J Drug Deliv Sci Technol. 2017; 37: 134-140.
57.Khademi S, Sarkar S, Kharrazi S, Amini SM, Shakeri-Zadeh A, Ay MR, et al. Evaluation of size, morphology, concentration, and surface effect of gold nanoparticles on X-ray attenuation in computed tomography. Phys Med. 2018; 45: 127-133.
58.Shirkhanloo H, Safari M, Amini SM, Rashidi M. Novel Semisolid Design Based on Bismuth Oxide (Bi2O3) nanoparticles for radiation protection. Nanomed Res J. 2017; 2(4): 230-238.
59.Amini SM, Kharrazi S, Rezayat SM, Gilani K. Radiofrequency electric field hyperthermia with gold nanostructures: role of particle shape and surface chemistry. Artif Cells Nanomed Biotechnol. 2017:1-11.
60.Amini SM, Kharrazi S, Jaafari MR. Radio frequency hyperthermia of cancerous cells with gold nanoclusters: an in vitro investigation. Gold Bull. 2017; 50(1): 43-50.
61.Amstad E, Kohlbrecher J, Müller E, Schweizer T, Textor M, Reimhult E. Triggered release from liposomes through magnetic actuation of iron oxide nanoparticle containing membranes. Nano lett. 2011; 11(4): 1664-1670.
62.Fatemi F, Amini SM, Kharrazi S, Rasaee MJ, Mazlomi MA, Asadi-Ghalehni M, et al. Construction of genetically engineered M13K07 helper phage for simultaneous phage display of gold binding peptide 1 and nuclear matrix protein 22 ScFv antibody. Colloids Surf B Biointerfaces. 2017; 159(Supplement C): 770-780.
63.Emami T, Madani R, Golchinfar F, Shoushtary A, Amini SM. Comparison of gold nanoparticle conjugated secondary antibody with non-gold secondary antibody in an ELISA kit model. Monoclon Antib Immunodiagn Immunother. 2015; 34(5): 366-370.
64.Shaabani E, Amini SM, Kharrazi S, Tajerian R. Curcumin coated gold nanoparticles: synthesis, characterization, cytotoxicity, antioxidant activity and its comparison with citrate coated gold nanoparticles. Nanomed J. 2017; 4(2): 115-125.
65.Esmaeili-bandboni A, Amini SM, Faridi-majidi R, Bagheri J, Mohammadnejad J, Sadroddiny E. A cross- linking gold nanoparticles aggregation method based on localized surface plasmon resonance for quantitative detection of miR-155. IET Nanobiotechnol [Internet]. 2017. Available from: http://digital-library.theiet.org/content/journals/10.1049/iet-nbt. 2017. 0174.
66.Fujimoto T, Terauchi S-y, Umehara H, Kojima I, Henderson W. Sonochemical preparation of single-dispersion metal nanoparticles from metal salts. Chem. Mater. 2001; 13(3): 1057-1060.
67.Gedanken A. Using sonochemistry for the fabrication of nanomaterials. Ultrason Sonochem. 2004; 11(2): 47-55.
68.Gedanken A, Mastai Y. Sonochemistry and other novel methods developed for the synthesis of nanoparticles. The Chemistry of Nanomaterials: Synthesis, Properties and Applications. 2005: 113-169.
69.Suslick KS, Choe S-B, Cichowlas AA, Grinstaff MW. Sonochemical synthesis of amorphous iron. nature. 1991; 353(6343): 414-416.
70.Prozorov T, Prozorov R, Suslick KS. High velocity interparticle collisions driven by ultrasound. JACS. 2004; 126(43): 13890-13891.
71.Okitsu K, Ashokkumar M, Grieser F. Sonochemical synthesis of gold nanoparticles: effects of ultrasound frequency. J Phys Chem B. 2005; 109(44): 20673-20675.
72.Watt J, Austin MJ, Simocko CK, Pete DV, Chavez J, Ammerman LM. Formation of Metal Nanoparticles Directly from Bulk Sources Using Ultrasound and Application to E‐Waste Upcycling. Small. 2018: 1703615.
73.Lea-Banks H, Teo B, Stride E, Coussios CC. The effect of particle density on ultrasound-mediated transport of nanoparticles. Phys Med Biol. 2016; 61(22): 7906.
74.Mo S, Carlisle R, Laga R, Myers R, Graham S, Cawood R. Increasing the density of nanomedicines improves their ultrasound-mediated delivery to tumours. J Control Release. 2015; 210: 10-8.
75.Mannaris C, Teo BM, Seth A, Bau L, Coussios C, Stride E. Gas‐Stabilizing Gold Nanocones for Acoustically Mediated Drug Delivery. Adv Healthc Mater. 2018: 1800184.
76.Shchukin DG, Gorin DA, Möhwald H. Ultrasonically induced opening of polyelectrolyte microcontainers. Langmuir. 2006; 22(17): 7400-7404.
77.Skirtach AG, De Geest BG, Mamedov A, Antipov AA, Kotov NA, Sukhorukov GB. Ultrasound stimulated release and catalysis using polyelectrolyte multilayer capsules. J. Mater. Chem. 2007;17(11): 1050-1054.
78.Kolesnikova TA, Gorin DA, Fernandes P, Kessel S, Khomutov GB, Fery A, et al. Nanocomposite microcontainers with high ultrasound sensitivity. Adv Funct Mater. 2010; 20(7): 1189-1195.
79.Pavlov AM, Saez V, Cobley A, Graves J, Sukhorukov GB, Mason TJ. Controlled protein release from microcapsules with composite shells using high frequency ultrasound—potential for in vivo medical use. Soft Matter. 2011; 7(9): 4341-4347.
80.Zarchi AAK, Amini SM, Salimi A, kharrazi S. Synthesis and Characterization of Liposomal Doxorubicin with Loaded Gold Nanoparticles. IET Nanobiotechnol [Internet]. 2018. Available from: http://digital-library.theiet.org/content/journals/10.1049/iet-nbt.2017.0321.
81.Li Y, He D, Tu J, Wang R, Zu C, Chen Y, et al. The comparative effect of wrapping solid gold nanoparticles and hollow gold nanoparticles with doxorubicin-loaded thermosensitive liposomes for cancer thermo-chemotherapy. Nanoscale. 2018.
82.Liu Y, Miyoshi H, Nakamura M. Encapsulated ultrasound microbubbles: therapeutic application in drug/gene delivery. J Control Release. 2006; 114(1): 89-99.
83.Tachibana K, Uchida T, Ogawa K, Yamashita N, Tamura K. Induction of cell-membrane porosity by ultrasound. Lancet. 1999; 353(9162): 1409.
84.Juffermans L, Dijkmans PA, Musters R, Visser CA, Kamp O. Transient permeabilization of cell membranes by ultrasound-exposed microbubbles is related to formation of hydrogen peroxide. Am J Physiol Heart Circ Physiol. 2006; 291(4): H1595-H1601.
85.Miller DL, Gies RA. The interaction of ultrasonic heating and cavitation in vascular bioeffects on mouse intestine. Ultrasound Med Biol. 1998; 24(1): 123-128.
86.Van Wamel A, Kooiman K, Emmer M, Ten Cate F, Versluis M, de Jong N. Ultrasound microbubble induced endothelial cell permeability. J Control. Release. 2006; 116(2): e100-e2.
87.Bekeredjian R, Chen S, Frenkel PA, Grayburn PA, Shohet RV. Ultrasound-targeted microbubble destruction can repeatedly direct highly specific plasmid expression to the heart. Circulation. 2003; 108(8): 1022-1026.
88.Aoi A, Watanabe Y, Mori S, Takahashi M, Vassaux G, Kodama T. Herpes simplex virus thymidine kinase-mediated suicide gene therapy using nano/microbubbles and ultrasound. Ultrasound Med Biol. 2008; 34(3): 425-434.
89.Hynynen K. Ultrasound for drug and gene delivery to the brain. Adv Drug Deliv Rev. 2008; 60(10): 1209-1217.
90.Huang S-L, MacDonald RC. Acoustically active liposomes for drug encapsulation and ultrasound-triggered release. Biochim Biophys Acta: Biomembranes. 2004; 1665(1): 134-141.
91.Ahmed SE, Moussa HG, Martins AM, Al-Sayah MH, Husseini GA. Effect of pH, ultrasound frequency and power density on the release of calcein from stealth liposomes. Eur J Nanomed. 2016; 8(1): 31-43.
92.Huang S-L, Kee PH, Kim H, Moody MR, Chrzanowski SM, MacDonald RC, et al. Nitric oxide-loaded echogenic liposomes for nitric oxide delivery and inhibition of intimal hyperplasia. J Am Coll Cardiol. 2009; 54(7): 652-659.
93.Marin A, Muniruzzaman M, Rapoport N. Mechanism of the ultrasonic activation of micellar drug delivery. J Control Release. 2001; 75(1): 69-81.
94.Gao Z-G, Fain HD, Rapoport N. Controlled and targeted tumor chemotherapy by micellar-encapsulated drug and ultrasound. J Control Release. 2005; 102(1): 203-222.
95.Husseini GA, Myrup GD, Pitt WG, Christensen DA, Rapoport NY. Factors affecting acoustically triggered release of drugs from polymeric micelles. J Control Release. 2000; 69(1): 43-52.
96.Rapoport N. Combined cancer therapy by micellar-encapsulated drug and ultrasound. Int. J. Pharm. 2004; 277(1): 155-162.
97.Husseini GA, El-Fayoumi RI, O'Neill KL, Rapoport NY, Pitt WG. DNA damage induced by micellar-delivered doxorubicin and ultrasound: comet assay study. Cancer lett. 2000; 154(2): 211-216.
98.Husseini GA, de la Rosa MAD, Gabuji T, Zeng Y, Christensen DA, Pitt WG. Release of doxorubicin from unstabilized and stabilized micelles under the action of ultrasound. J. Nanosci. Nanotechnol 2007; 7(3): 1028.
99.Cavalli R, Bisazza A, Rolfo A, Balbis S, Madonnaripa D, Caniggia I, et al. Ultrasound-mediated oxygen delivery from chitosan nanobubbles. Int. J. Pharm. 2009; 378(1): 215-217.
Nanomedicine Journal
Volume 5, Issue 3
July 2018
Pages 127-137

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