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Cancer Chemotherapy and Pharmacology

, Volume 84, Issue 6, pp 1315–1321 | Cite as

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

  • Rasoul Irajirad
  • Amirhossein Ahmadi
  • Bahareh Khalili Najafabad
  • Ziaeddin Abed
  • Roghayeh Sheervalilou
  • Samideh Khoei
  • M. Bagher Shiran
  • Habib GhaznaviEmail author
  • Ali Shakeri-ZadehEmail author
Original Article
  • 57 Downloads

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.

Keywords

Cancer Chemotherapy Nanotechnology Hyperthermia Combination therapy 

Notes

Funding

All financial supports received from Iran University of Medical Sciences (Grant no. 29865) and Zahedan University of Medical Sciences (Grant no. 7970) are acknowledged.

Compliance with Ethical Standards

Conflicts of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in this study were in accordance with the ethical standards of Iran University of Medical Sciences (IUMS ethics committee, Permit number: IR.IUMS.REC 1395.95-03-30-27720).

References

  1. 1.
    Cho K, Wang X, Nie S, Shin DM (2008) Therapeutic nanoparticles for drug delivery in cancer. Clin Cancer Res 14(5):1310–1316CrossRefGoogle Scholar
  2. 2.
    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 533:171–181CrossRefGoogle Scholar
  3. 3.
    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):25–34Google Scholar
  4. 4.
    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 1:13–23Google Scholar
  5. 5.
    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):4399–4416CrossRefGoogle Scholar
  6. 6.
    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 46:241–253CrossRefGoogle Scholar
  7. 7.
    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):847–853CrossRefGoogle Scholar
  8. 8.
    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 81:308–314CrossRefGoogle Scholar
  9. 9.
    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 62:84–89CrossRefGoogle Scholar
  10. 10.
    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):1594–1604PubMedGoogle Scholar
  11. 11.
    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):3832–3838CrossRefGoogle Scholar
  12. 12.
    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):4306–4314CrossRefGoogle Scholar
  13. 13.
    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 143:178–185CrossRefGoogle Scholar
  14. 14.
    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):193110CrossRefGoogle Scholar
  15. 15.
    Wen D (2013) Nanoparticle-related heat transfer phenomenon and its application in biomedical fields. Heat Transfer Eng 34(14):1171–1179CrossRefGoogle Scholar
  16. 16.
    Dąbek L, Hornowski T, Józefczak A, Skumiel A (2013) Ultrasonic properties of magnetic nanoparticles with an additional biocompatible dextran layer. Arch Acoust 38(1):93–98CrossRefGoogle Scholar
  17. 17.
    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):1939–1955CrossRefGoogle Scholar
  18. 18.
    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):1121–1130CrossRefGoogle Scholar
  19. 19.
    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):493–501CrossRefGoogle Scholar
  20. 20.
    Chol S, Estman J (1995) Enhancing thermal conductivity of fluids with nanoparticles. ASME Publ Fed 231:99–106Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Medical Physics Department, School of MedicineIran University of Medical Sciences (IUMS), Hemmat Exp.TehranIran
  2. 2.Faculty of Pharmacy, Pharmaceutical Sciences Research CenterMazandaran University of Medical SciencesSariIran
  3. 3.Cellular and Molecular Research CenterZahedan University of Medical Sciences (ZaUMS)ZahedanIran

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