Skip to main content
Top
Published in: Cancer Chemotherapy and Pharmacology 6/2019

01-12-2019 | Ultrasound | Original Article

Combined thermo-chemotherapy of cancer using 1 MHz ultrasound waves and a cisplatin-loaded sonosensitizing nanoplatform: an in vivo study

Authors: Rasoul Irajirad, Amirhossein Ahmadi, Bahareh Khalili Najafabad, Ziaeddin Abed, Roghayeh Sheervalilou, Samideh Khoei, M. Bagher Shiran, Habib Ghaznavi, Ali Shakeri-Zadeh

Published in: Cancer Chemotherapy and Pharmacology | Issue 6/2019

Login to get access

Abstract

Purpose

The aim of the present study was to develop a new strategy for combined thermo-chemotherapy of cancer. For this purpose, we used ultrasound waves [1 MHz; 1 W/cm2; 10 min] in combination with a sonosensitizing nanoplatform, named ACA, made of alginate co-loaded with cisplatin and gold nanoparticles (AuNPs).

Methods

Various combinatorial treatment regimens consisting of ultrasound, AuNPs, cisplatin, and ACA nanoplatform were studied in vivo. The CT26 colon adenocarcinoma cell line was used for tumor induction in BALB/c mice. During the ultrasound exposure, we monitored the temperature variations in each treatment group using infrared thermal imaging. Furthermore, tumor metabolism was assessed by [18F]FDG (2-deoxy-2-[18F]fluoro-d-glucose)-positron emission tomography (PET) imaging.

Results

The combination of ultrasound with nanoplatform showed an improved therapeutic efficacy than free cisplatin or ultrasound alone. It was revealed that the examined thermo-chemotherapy protocol has the potential to intensively decrease the metabolic activity of CT26 tumors.

Conclusions

The data obtained in this study confirmed a potent anti-tumor efficacy caused by the ACA nanoplatform and ultrasound combination. It may provide a beneficial cancer therapy strategy in which the thermal and mechanical effects of ultrasound can intensify the therapeutic ratio of conventional chemotherapy methods.
Literature
1.
go back to reference Cho K, Wang X, Nie S, Shin DM (2008) Therapeutic nanoparticles for drug delivery in cancer. Clin Cancer Res 14(5):1310–1316CrossRef Cho K, Wang X, Nie S, Shin DM (2008) Therapeutic nanoparticles for drug delivery in cancer. Clin Cancer Res 14(5):1310–1316CrossRef
2.
go back to reference de Solorzano IO, Alejo T, Abad M, Bueno-Alejo C, Mendoza G, Andreu V, Irusta S, Sebastian V, Arruebo M (2019) Cleavable and thermo-responsive hybrid nanoparticles for on-demand drug delivery. J Colloid Interface Sci 533:171–181CrossRef de Solorzano IO, Alejo T, Abad M, Bueno-Alejo C, Mendoza G, Andreu V, Irusta S, Sebastian V, Arruebo M (2019) Cleavable and thermo-responsive hybrid nanoparticles for on-demand drug delivery. J Colloid Interface Sci 533:171–181CrossRef
3.
go back to reference Hashemian A, Eshghi H, Mansoori G, Shakeri-Zadeh A, Mehdizadeh A (2009) Folate-conjugated gold nanoparticles (synthesis, characterization and design for cancer cells nanotechnology-based targeting). Int J Nanosci Nanotechnol 5(1):25–34 Hashemian A, Eshghi H, Mansoori G, Shakeri-Zadeh A, Mehdizadeh A (2009) Folate-conjugated gold nanoparticles (synthesis, characterization and design for cancer cells nanotechnology-based targeting). Int J Nanosci Nanotechnol 5(1):25–34
4.
go back to reference Shakeri-Zadeh A, Eshghi H, Mansoori G, Hashemian A (2009) Gold nanoparticles conjugated with folic acid using mercaptohexanol as the linker. J Nanotechnol Progress Int 1:13–23 Shakeri-Zadeh A, Eshghi H, Mansoori G, Hashemian A (2009) Gold nanoparticles conjugated with folic acid using mercaptohexanol as the linker. J Nanotechnol Progress Int 1:13–23
5.
go back to reference Beik J, Khademi S, Attaran N, Sarkar S, Shakeri-Zadeh A, Ghaznavi H, Ghadiri H (2017) A nanotechnology based strategy to increase the efficiency of cancer diagnosis and therapy: folate conjugated gold nanoparticles. Curr Med Chem 24(39):4399–4416CrossRef Beik J, Khademi S, Attaran N, Sarkar S, Shakeri-Zadeh A, Ghaznavi H, Ghadiri H (2017) A nanotechnology based strategy to increase the efficiency of cancer diagnosis and therapy: folate conjugated gold nanoparticles. Curr Med Chem 24(39):4399–4416CrossRef
6.
go back to reference Mirrahimi M, Hosseini V, Kamrava SK, Attaran N, Beik J, Kooranifar S, Ghaznavi H, Shakeri-Zadeh A (2018) Selective heat generation in cancer cells using a combination of 808 nm laser irradiation and the folate-conjugated Fe2O3@ Au nanocomplex. Artif Cells Nanomed Biotechnol 46:241–253CrossRef Mirrahimi M, Hosseini V, Kamrava SK, Attaran N, Beik J, Kooranifar S, Ghaznavi H, Shakeri-Zadeh A (2018) Selective heat generation in cancer cells using a combination of 808 nm laser irradiation and the folate-conjugated Fe2O3@ Au nanocomplex. Artif Cells Nanomed Biotechnol 46:241–253CrossRef
7.
go back to reference Shakeri-Zadeh A, Kamrava SK, Farhadi M, Hajikarimi Z, Maleki S, Ahmadi A (2014) A scientific paradigm for targeted nanophotothermolysis; the potential for nanosurgery of cancer. Lasers Med Sci 29(2):847–853CrossRef Shakeri-Zadeh A, Kamrava SK, Farhadi M, Hajikarimi Z, Maleki S, Ahmadi A (2014) A scientific paradigm for targeted nanophotothermolysis; the potential for nanosurgery of cancer. Lasers Med Sci 29(2):847–853CrossRef
8.
go back to reference Beik J, Abed Z, Shakeri-Zadeh A, Nourbakhsh M, Shiran MB (2016) Evaluation of the sonosensitizing properties of nano-graphene oxide in comparison with iron oxide and gold nanoparticles. Phys E 81:308–314CrossRef Beik J, Abed Z, Shakeri-Zadeh A, Nourbakhsh M, Shiran MB (2016) Evaluation of the sonosensitizing properties of nano-graphene oxide in comparison with iron oxide and gold nanoparticles. Phys E 81:308–314CrossRef
9.
go back to reference Beik J, Abed Z, Ghadimi-Daresajini A, Nourbakhsh M, Shakeri-Zadeh A, Ghasemi MS, Shiran MB (2016) Measurements of nanoparticle-enhanced heating from 1 MHz ultrasound in solution and in mice bearing CT26 colon tumors. J Therm Biol 62:84–89CrossRef Beik J, Abed Z, Ghadimi-Daresajini A, Nourbakhsh M, Shakeri-Zadeh A, Ghasemi MS, Shiran MB (2016) Measurements of nanoparticle-enhanced heating from 1 MHz ultrasound in solution and in mice bearing CT26 colon tumors. J Therm Biol 62:84–89CrossRef
10.
go back to reference Ghaznavi H, Hosseini-Nami S, Kamrava SK, Irajirad R, Maleki S, Shakeri-Zadeh A, Montazerabadi A (2018) Folic acid conjugated PEG coated gold–iron oxide core–shell nanocomplex as a potential agent for targeted photothermal therapy of cancer. Artif Cells Nanomed Biotechnol 46(8):1594–1604PubMed Ghaznavi H, Hosseini-Nami S, Kamrava SK, Irajirad R, Maleki S, Shakeri-Zadeh A, Montazerabadi A (2018) Folic acid conjugated PEG coated gold–iron oxide core–shell nanocomplex as a potential agent for targeted photothermal therapy of cancer. Artif Cells Nanomed Biotechnol 46(8):1594–1604PubMed
11.
go back to reference Hauck TS, Jennings TL, Yatsenko T, Kumaradas JC, Chan WC (2008) Enhancing the toxicity of cancer chemotherapeutics with gold nanorod hyperthermia. Adv Mater 20(20):3832–3838CrossRef Hauck TS, Jennings TL, Yatsenko T, Kumaradas JC, Chan WC (2008) Enhancing the toxicity of cancer chemotherapeutics with gold nanorod hyperthermia. Adv Mater 20(20):3832–3838CrossRef
12.
go back to reference Beik J, Shiran MB, Abed Z, Shiri I, Ghadimi-Daresajini A, Farkhondeh F, Ghaznavi H, Shakeri-Zadeh A (2018) Gold nanoparticle-induced sonosensitization enhances the antitumor activity of ultrasound in colon tumor-bearing mice. Med Phys 45(9):4306–4314CrossRef Beik J, Shiran MB, Abed Z, Shiri I, Ghadimi-Daresajini A, Farkhondeh F, Ghaznavi H, Shakeri-Zadeh A (2018) Gold nanoparticle-induced sonosensitization enhances the antitumor activity of ultrasound in colon tumor-bearing mice. Med Phys 45(9):4306–4314CrossRef
13.
go back to reference Mirrahimi M, Abed Z, Beik J, Shiri I, Dezfuli AS, Mahabadi VP, Kamrava SK, Ghaznavi H, Shakeri-Zadeh A (2019) A thermo-responsive alginate nanogel platform co-loaded with gold nanoparticles and cisplatin for combined cancer chemo-photothermal therapy. Pharmacol Res 143:178–185CrossRef Mirrahimi M, Abed Z, Beik J, Shiri I, Dezfuli AS, Mahabadi VP, Kamrava SK, Ghaznavi H, Shakeri-Zadeh A (2019) A thermo-responsive alginate nanogel platform co-loaded with gold nanoparticles and cisplatin for combined cancer chemo-photothermal therapy. Pharmacol Res 143:178–185CrossRef
14.
go back to reference Sviridov A, Andreev V, Ivanova E, Osminkina L, Tamarov K, Timoshenko VY (2013) Porous silicon nanoparticles as sensitizers for ultrasonic hyperthermia. Appl Phys Lett 103(19):193110CrossRef Sviridov A, Andreev V, Ivanova E, Osminkina L, Tamarov K, Timoshenko VY (2013) Porous silicon nanoparticles as sensitizers for ultrasonic hyperthermia. Appl Phys Lett 103(19):193110CrossRef
15.
go back to reference Wen D (2013) Nanoparticle-related heat transfer phenomenon and its application in biomedical fields. Heat Transfer Eng 34(14):1171–1179CrossRef Wen D (2013) Nanoparticle-related heat transfer phenomenon and its application in biomedical fields. Heat Transfer Eng 34(14):1171–1179CrossRef
16.
go back to reference Dąbek L, Hornowski T, Józefczak A, Skumiel A (2013) Ultrasonic properties of magnetic nanoparticles with an additional biocompatible dextran layer. Arch Acoust 38(1):93–98CrossRef Dąbek L, Hornowski T, Józefczak A, Skumiel A (2013) Ultrasonic properties of magnetic nanoparticles with an additional biocompatible dextran layer. Arch Acoust 38(1):93–98CrossRef
17.
go back to reference Mehtala JG, Torregrosa-Allen S, Elzey BD, Jeon M, Kim C, Wei A (2014) Synergistic effects of cisplatin chemotherapy and gold nanorod-mediated hyperthermia on ovarian cancer cells and tumors. Nanomedicine 9(13):1939–1955CrossRef Mehtala JG, Torregrosa-Allen S, Elzey BD, Jeon M, Kim C, Wei A (2014) Synergistic effects of cisplatin chemotherapy and gold nanorod-mediated hyperthermia on ovarian cancer cells and tumors. Nanomedicine 9(13):1939–1955CrossRef
18.
go back to reference Raoof M, Corr SJ, Zhu C, Cisneros BT, Kaluarachchi WD, Phounsavath S, Wilson LJ, Curley SA (2014) Gold nanoparticles and radiofrequency in experimental models for hepatocellular carcinoma. Nanomed Nanotechnol Biol Med 10(6):1121–1130CrossRef Raoof M, Corr SJ, Zhu C, Cisneros BT, Kaluarachchi WD, Phounsavath S, Wilson LJ, Curley SA (2014) Gold nanoparticles and radiofrequency in experimental models for hepatocellular carcinoma. Nanomed Nanotechnol Biol Med 10(6):1121–1130CrossRef
19.
go back to reference Xu Y, Karmakar A, Heberlein WE, Mustafa T, Biris AR, Biris AS (2012) Multifunctional magnetic nanoparticles for synergistic enhancement of cancer treatment by combinatorial radio frequency thermolysis and drug delivery. Adv Healthcare Mater 1(4):493–501CrossRef Xu Y, Karmakar A, Heberlein WE, Mustafa T, Biris AR, Biris AS (2012) Multifunctional magnetic nanoparticles for synergistic enhancement of cancer treatment by combinatorial radio frequency thermolysis and drug delivery. Adv Healthcare Mater 1(4):493–501CrossRef
20.
go back to reference Chol S, Estman J (1995) Enhancing thermal conductivity of fluids with nanoparticles. ASME Publ Fed 231:99–106 Chol S, Estman J (1995) Enhancing thermal conductivity of fluids with nanoparticles. ASME Publ Fed 231:99–106
Metadata
Title
Combined thermo-chemotherapy of cancer using 1 MHz ultrasound waves and a cisplatin-loaded sonosensitizing nanoplatform: an in vivo study
Authors
Rasoul Irajirad
Amirhossein Ahmadi
Bahareh Khalili Najafabad
Ziaeddin Abed
Roghayeh Sheervalilou
Samideh Khoei
M. Bagher Shiran
Habib Ghaznavi
Ali Shakeri-Zadeh
Publication date
01-12-2019
Publisher
Springer Berlin Heidelberg
Published in
Cancer Chemotherapy and Pharmacology / Issue 6/2019
Print ISSN: 0344-5704
Electronic ISSN: 1432-0843
DOI
https://doi.org/10.1007/s00280-019-03961-9

Other articles of this Issue 6/2019

Cancer Chemotherapy and Pharmacology 6/2019 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine