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Superparamagnetic magnetite nanoparticles for cancer cells treatment via magnetic hyperthermia: effect of natural capping agent, particle size and concentration

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Abstract

Superparamagnetic iron oxide nanoparticles (SPMNPs) continue to emerge as one of the most potential candidates in biomedical applications. Their multiple functionalities arise from several advantages, such as their responsiveness to external magnetic stimuli, availability, biocompatibility, lack of toxicity, and easier to synthesize. Such MNPs can generate heat when they subjected to an alternating magnetic field, which can be used in tumor treatment if the released heat is as enough as to increase the tumor area temperature the tumor area from physiological temperature of 37 °C to 42–45 °C. In this regard, the size, distribution, magnetic properties of the magnetic nanoparticles play an important role. Thus, the Fe3O4 NPs were synthesized via a simple and inexpensive coprecipitation route with the assistance of natural extracts of Peppermint (P) and Dracocephalum (D) as capping agents. The structural, morphological, and magnetic properties were characterized through the XRD, HRTEM, and vibrating sample magnetometer, respectively.

Cytotoxic effect and IC50 values of the as-synthesized Fe3O4 NPs on K562 were evaluated using MTT assay, being of 106.3 and 146.0 of the IC50 values for NPs synthesized with P and D-capping agents, respectively. The growth inhibition was dependent on treatment time, dose of NPs, and type of the employed capping agent. Furthermore, the synthesized NPs with dracocephalum had a more inhibitory effect than that of the other sample. The heating efficiency of the Fe3O4 NPs was investigated via an induction heater generating alternating magnetic field at frequency of 92 kHz and amplitude of 10 kA/m. The temperature rise (ΔT) of the as-prepared ferrofluids in the AC magnetic field was studied on different concentrations of magnetic nanoparticles. The specific absorption rate (SAR), as an indicative of heating efficiency, was obtained from Box-Lucas equation and linear fitting of ΔT-time curve. The results showed that the ΔT sharply increases with increasing the concentration of NPs from 3 to 9 mg/mL, but it was dependent on the size, distribution, and magnetic properties of the samples synthesized with two different capping agents. The SAR values of 33 W/g at 9 mg/mL obtained, for the P SPIONPs, suggests the use of those MNPs as the potential materials in tumor treatment via magnetic fluid hyperthermia.

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References

  1. N.V. Jadhav, A.I. Prasad, A. Kumar, R. Mishra, S. Dhara, K. Babu, C. Prajapat, N. Misra, R. Ningthoujam, B. Pandey, Synthesis of oleic acid functionalized Fe3O4 magnetic nanoparticles and studying their interaction with tumor cells for potential hyperthermia applications. Colloids Surf. B Biointerfaces 108, 158–168 (2013)

    Article  CAS  Google Scholar 

  2. D. Tishkevich, I. Korolkov, A. Kozlovskiy, M. Anisovich, D. Vinnik, A. Ermekova, A. Vorobjova, E. Shumskaya, T. Zubar, S. Trukhanov, Immobilization of boron-rich compound on Fe3O4 nanoparticles: stability and cytotoxicity. J. Alloy. Compd. 797, 573–581 (2019)

    Article  CAS  Google Scholar 

  3. P. Nezhad-Mokhtari, F. Salahpour-Anarjan, A. Rezanezhad, A. Akbarzadeh, Magnetic Nanoparticles: An Emergent Platform for Future Cancer Theranostics, in Nanobiotechnology in Diagnosis, Drug Delivery, and Treatment. (Wiley, Hoboken, 2020), pp. 171–195

    Chapter  Google Scholar 

  4. H. Yang, Y. Chen, Z. Chen, Y. Geng, X. Xie, X. Shen, T. Li, S. Li, C. Wu, Y. Liu, Chemo-photodynamic combined gene therapy and dual-modal cancer imaging achieved by pH-responsive alginate/chitosan multilayer-modified magnetic mesoporous silica nanocomposites. Biomater. Sci. 5(5), 1001–1013 (2017)

    Article  CAS  Google Scholar 

  5. A. Hajalilou, S.A. Mazlan, S.T. Shilan, E. Abouzari-Lotf, Enhanced magnetorheology of soft magnetic carbonyl iron suspension with binary mixture of Ni-Zn ferrite and Fe 3 O 4 nanoparticle additive. Colloid Polym. Sci. 295(9), 1499–1510 (2017)

    Article  CAS  Google Scholar 

  6. S. Kanagesan, M. Hashim, S. Tamilselvan, N. Alitheen, I. Ismail, A. Hajalilou, K. Ahsanul, Synthesis, characterization, and cytotoxicity of iron oxide nanoparticles. Adv. Mater. Sci. Eng. 2013, 1–7 (2013)

    Article  CAS  Google Scholar 

  7. A. Yusoff, M. N. Salimi, M. F. Jamlos, In Synthesis and characterization of biocompatible Fe3O4 nanoparticles at different pH, AIP Conference Proceedings (AIP Publishing LLC, New York, 2017), p. 020010

  8. A. Hajalilou, L. Ferreira, M. Jorge, C. Reis, M. Cruz, Superparamagnetic Ag-Fe3O4 composites nanoparticles for magnetic fluid hyperthermia. J. Magn. Magn. Mater. 537, 168242 (2021)

    Article  CAS  Google Scholar 

  9. X. Yu, Y. Zhu, Preparation of magnetic mesoporous silica nanoparticles as a multifunctional platform for potential drug delivery and hyperthermia. Sci. Technol. Adv. Mater. 17(1), 229–238 (2016)

    Article  CAS  Google Scholar 

  10. L.-Z. Bai, D.-L. Zhao, Y. Xu, J.-M. Zhang, Y.-L. Gao, L.-Y. Zhao, J.-T. Tang, Inductive heating property of graphene oxide–Fe3O4 nanoparticles hybrid in an AC magnetic field for localized hyperthermia. Mater. Lett. 68, 399–401 (2012)

    Article  CAS  Google Scholar 

  11. S. Ebrahimisadr, B. Aslibeiki, R. Asadi, Magnetic hyperthermia properties of iron oxide nanoparticles: The effect of concentration. Phys. C Supercond. Appl. 549, 119–121 (2018)

    Article  CAS  Google Scholar 

  12. Y. Wang, X. Cao, G. Liu, R. Hong, Y. Chen, X. Chen, H. Li, B. Xu, D. Wei, Synthesis of Fe3O4 magnetic fluid used for magnetic resonance imaging and hyperthermia. J. Magn. Magn. Mater. 323(23), 2953–2959 (2011)

    Article  CAS  Google Scholar 

  13. B. Thiesen, A. Jordan, Clinical applications of magnetic nanoparticles for hyperthermia. Int. J. Hyperth. 24(6), 467–474 (2008)

    Article  CAS  Google Scholar 

  14. A. Jordan, R. Scholz, P. Wust, H. Fähling, R. Felix, Magnetic fluid hyperthermia (MFH): Cancer treatment with AC magnetic field induced excitation of biocompatible superparamagnetic nanoparticles. J. Magn. Magn. Mater. 201(1–3), 413–419 (1999)

    Article  CAS  Google Scholar 

  15. B. Aslibeiki, M. Ehsani, F. Nasirzadeh, M. Mohammadi, The effect of interparticle interactions on spin glass and hyperthermia properties of Fe3O4 nanoparticles. Mater. Res. Express 4(7), 075051 (2017)

    Article  CAS  Google Scholar 

  16. K. Petcharoen, A. Sirivat, Synthesis and characterization of magnetite nanoparticles via the chemical co-precipitation method. Mater. Sci. Eng. B 177(5), 421–427 (2012)

    Article  CAS  Google Scholar 

  17. D. Tishkevich, A. Vorobjova, D.A. Vinnik, Template Assisted Ni Nanowires Fabrication, Materials Science Forum (Trans Tech Publications, Stafa-Zurich, 2019), pp. 235–241

    Google Scholar 

  18. D. Tishkevich, A. Vorobjova, D.A. Vinnik, Formation and Corrosion Behavior of Nickel/Alumina Nanocomposites, Solid State Phenomena (Trans Tech Publications, Stafa-Zurich, 2020), pp. 100–106

    Google Scholar 

  19. A. Vorobjova, D. Tishkevich, D. Shimanovich, M. Zdorovets, A. Kozlovskiy, T. Zubar, D. Vinnik, M. Dong, S. Trukhanov, A. Trukhanov, Electrochemical behaviour of Ti/Al2O3/Ni nanocomposite material in artificial physiological solution: prospects for biomedical application. Nanomaterials 10(1), 173 (2020)

    Article  CAS  Google Scholar 

  20. A. Yan, X. Liu, G. Qiu, H. Wu, R. Yi, N. Zhang, J. Xu, Solvothermal synthesis and characterization of size-controlled Fe3O4 nanoparticles. J. Alloy. Compd. 458(1–2), 487–491 (2008)

    Article  CAS  Google Scholar 

  21. H. Hu, H. Yang, P. Huang, D. Cui, Y. Peng, J. Zhang, F. Lu, J. Lian, D. Shi, Unique role of ionic liquid in microwave-assisted synthesis of monodisperse magnetite nanoparticles. Chem. Commun. 46(22), 3866–3868 (2010)

    Article  CAS  Google Scholar 

  22. R. Kavkhani, M. Pourzaki, A. Kianvash, A. Hajalilou, R.G. Adli, Effect of sintering temperature and soaking time on the magnetic properties and transmission behavior of nano crystalline Mg0. 8Mn0. 2Al0. 1Fe1. 9O4. J. Sol-Gel Sci. Technol. 99, 1–11 (2021)

    Article  CAS  Google Scholar 

  23. P. Liu, Z. Yao, J. Zhou, Z. Yang, L.B. Kong, Small magnetic Co-doped NiZn ferrite/graphene nanocomposites and their dual-region microwave absorption performance. J. Mater. Chem. C 4(41), 9738–9749 (2016)

    Article  CAS  Google Scholar 

  24. P. Liu, V.M.H. Ng, Z. Yao, J. Zhou, L.B. Kong, Ultrasmall Fe3O4 nanoparticles on MXenes with high microwave absorption performance. Mater. Lett. 229, 286–289 (2018)

    Article  CAS  Google Scholar 

  25. P. Liu, Z. Yao, V.M.H. Ng, J. Zhou, L.B. Kong, K. Yue, Facile synthesis of ultrasmall Fe3O4 nanoparticles on MXenes for high microwave absorption performance. Compos. A Appl. Sci. Manuf. 115, 371–382 (2018)

    Article  CAS  Google Scholar 

  26. J. Ding, T. Reynolds, W. Miao, P. McCormick, R. Street, High magnetic performance in mechanically alloyed Co-substituted Fe3O4. Appl. Phys. Lett. 65(24), 3135–3136 (1994)

    Article  CAS  Google Scholar 

  27. A. Hajalilou, S.A. Mazlan, A review on preparation techniques for synthesis of nanocrystalline soft magnetic ferrites and investigation on the effects of microstructure features on magnetic properties. Appl. Phys. A 122(7), 1–15 (2016)

    Article  CAS  Google Scholar 

  28. A. Hajalilou, A. Kianvash, H. Lavvafi, K. Shameli, Nanostructured soft magnetic materials synthesized via mechanical alloying: a review. J. Mater. Sci. Mater. Electron. 29(2), 1690–1717 (2018)

    Article  CAS  Google Scholar 

  29. A. Hajalilou, S.A. Mazlan, H. Lavvafi, K. Shameli, Field Responsive Fluids as Smart Materials (Springer, Berlin, 2016)

    Book  Google Scholar 

  30. R. Etemadifar, A. Kianvash, N. Arsalani, E. Abouzari-Lotf, A. Hajalilou, Green synthesis of superparamagnetic magnetite nanoparticles: effect of natural surfactant and heat treatment on the magnetic properties. J. Mater. Sci. Mater. Electron. 29(20), 17144–17153 (2018)

    Article  CAS  Google Scholar 

  31. A.B. Ogholbeyg, A. Kianvash, A. Hajalilou, E. Abouzari-Lotf, A. Zarebkohan, Cytotoxicity characteristics of green assisted-synthesized superparamagnetic maghemite (γ-Fe 2 O 3) nanoparticles. J. Mater. Sci. Mater. Electron. 29(14), 12135–12143 (2018)

    Article  CAS  Google Scholar 

  32. L. Huang, X. Weng, Z. Chen, M. Megharaj, R. Naidu, Synthesis of iron-based nanoparticles using oolong tea extract for the degradation of malachite green. Spectrochim. Acta Part A Mol. Biomol. Spectrosc. 117, 801–804 (2014)

    Article  CAS  Google Scholar 

  33. S.M. Ghaseminezhad, S.A. Shojaosadati, Evaluation of the antibacterial activity of Ag/Fe3O4 nanocomposites synthesized using starch. Carbohydr. Polym. 144, 454–463 (2016)

    Article  CAS  Google Scholar 

  34. W. Chen, W. Cai, L. Zhang, G. Wang, L. Zhang, Sonochemical processes and formation of gold nanoparticles within pores of mesoporous silica. J. Colloid Interface Sci. 238(2), 291–295 (2001)

    Article  CAS  Google Scholar 

  35. S. Sengupta, D. Eavarone, I. Capila, G. Zhao, N. Watson, T. Kiziltepe, R. Sasisekharan, Temporal targeting of tumour cells and neovasculature with a nanoscale delivery system. Nature 436(7050), 568–572 (2005)

    Article  CAS  Google Scholar 

  36. K. Do Kim, D.N. Han, H.T. Kim, Optimization of experimental conditions based on the Taguchi robust design for the formation of nano-sized silver particles by chemical reduction method. Chem. Eng. J. 104(1–3), 55–61 (2004)

    Article  CAS  Google Scholar 

  37. A.M. El Badawy, K.G. Scheckel, M. Suidan, T. Tolaymat, The impact of stabilization mechanism on the aggregation kinetics of silver nanoparticles. Sci. Total Environ. 429, 325–331 (2012)

    Article  CAS  Google Scholar 

  38. P. Raveendran, J. Fu, S.L. Wallen, Completely “green” synthesis and stabilization of metal nanoparticles. J. Am. Chem. Soc. 125(46), 13940–13941 (2003)

    Article  CAS  Google Scholar 

  39. J.N. Kuhn, C.-K. Tsung, W. Huang, G.A. Somorjai, Effect of organic capping layers over monodisperse platinum nanoparticles upon activity for ethylene hydrogenation and carbon monoxide oxidation. J. Catal. 265(2), 209–215 (2009)

    Article  CAS  Google Scholar 

  40. M. Maham, H. Akbari, A. Delazar, Chemical composition and antinociceptive effect of the essential oil of dracocephalum moldavica L. Pharm Sci 18(4), 187–192 (2013)

    Google Scholar 

  41. N. Galeotti, L.D.C. Mannelli, G. Mazzanti, A. Bartolini, C. Ghelardini, Menthol: a natural analgesic compound. Neurosci. Lett. 322(3), 145–148 (2002)

    Article  CAS  Google Scholar 

  42. N.H. Abdullah, K. Shameli, E.C. Abdullah, L.C. Abdullah, A facile and green synthetic approach toward fabrication of starch-stabilized magnetite nanoparticles. Chin. Chem. Lett. 28(7), 1590–1596 (2017)

    Article  CAS  Google Scholar 

  43. E. Rezaie, A. Rezanezhad, A. Hajalilou, L.S. Ghadimi, E. Abouzari-Lotf, N. Arsalani, Electrochemical behavior of SrFe12O19/CoFe2O4 composite nanoparticles synthesized via one-pot hydrothermal method. J. Alloy. Compd. 789, 40–47 (2019)

    Article  CAS  Google Scholar 

  44. A. Raghavender, N. Biliškov, Ž Skoko, XRD and IR analysis of nanocrystalline Ni–Zn ferrite synthesized by the sol–gel method. Mater. Lett. 65(4), 677–680 (2011)

    Article  CAS  Google Scholar 

  45. S.D. Abkenar, M. Khoobi, R. Tarasi, M. Hosseini, A. Shafiee, M.R. Ganjali, Fast removal of methylene blue from aqueous solution using magnetic-modified Fe 3 O 4 nanoparticles. J. Environ. Eng. 141(1), 04014049 (2015)

    Article  CAS  Google Scholar 

  46. M.I. Khalil, Co-precipitation in aqueous solution synthesis of magnetite nanoparticles using iron (III) salts as precursors. Arab. J. Chem. 8(2), 279–284 (2015)

    Article  CAS  Google Scholar 

  47. R.A. Varin, A.S. Bidabadi, M. Polanski, M. Biglari, L. Stobinski, The effects of filamentary Ni, graphene and lithium amide (LiNH2) additives on the dehydrogenation behavior of mechano-chemically synthesized crystalline manganese borohydride (Mn (BH4) 2) and its solvent filtration/extraction. Mater. Res. Bull. 100, 394–406 (2018)

    Article  CAS  Google Scholar 

  48. Y.-S. Li, J.S. Church, A.L. Woodhead, Infrared and Raman spectroscopic studies on iron oxide magnetic nano-particles and their surface modifications. J. Magn. Magn. Mater. 324(8), 1543–1550 (2012)

    Article  CAS  Google Scholar 

  49. T.T.T. Mai, P.T. Ha, H.N. Pham, T.T.H. Le, H.L. Pham, T.B.H. Phan, X.P. Nguyen, Chitosan and O-carboxymethyl chitosan modified Fe3O4 for hyperthermic treatment. Adv. Nat. Sci Nanosci. Nanotechnol. 3(1), 015006 (2012)

    Article  CAS  Google Scholar 

  50. J.-N. Park, P. Zhang, Y.-S. Hu, E.W. McFarland, Synthesis and characterization of sintering-resistant silica-encapsulated Fe3O4 magnetic nanoparticles active for oxidation and chemical looping combustion. Nanotechnology 21(22), 225708 (2010)

    Article  CAS  Google Scholar 

  51. X. Zhang, Y. Niu, X. Meng, Y. Li, J. Zhao, Structural evolution and characteristics of the phase transformations between α-Fe 2 O 3, Fe 3 O 4 and γ-Fe 2 O 3 nanoparticles under reducing and oxidizing atmospheres. CrystEngComm 15(40), 8166–8172 (2013)

    Article  CAS  Google Scholar 

  52. G. Li, J. Lan, G. Li, Chrysanthemum-like 3D hierarchical magnetic γ-Fe 2 O 3 and Fe 3 O 4 superstructures: facile synthesis and application in adsorption of organic pollutants from water. RSC Adv. 5(3), 1705–1711 (2015)

    Article  CAS  Google Scholar 

  53. C. Guo, Y. Hu, H. Qian, J. Ning, S. Xu, Magnetite (Fe3O4) tetrakaidecahedral microcrystals: synthesis, characterization, and micro-Raman study. Mater. Charact. 62(1), 148–151 (2011)

    Article  CAS  Google Scholar 

  54. X.-D. Liu, H. Chen, S.-S. Liu, L.-Q. Ye, Y.-P. Li, Hydrothermal synthesis of superparamagnetic Fe3O4 nanoparticles with ionic liquids as stabilizer. Mater. Res. Bull. 62, 217–221 (2015)

    Article  CAS  Google Scholar 

  55. Y.V. Kolen’ko, M. Bañobre-López, C. Rodríguez-Abreu, E. Carbó-Argibay, A. Sailsman, Y. Piñeiro-Redondo, M.F. Cerqueira, D.Y. Petrovykh, K. Kovnir, O.I. Lebedev, Large-scale synthesis of colloidal Fe3O4 nanoparticles exhibiting high heating efficiency in magnetic hyperthermia. J. Phys. Chem. C 118(16), 8691–8701 (2014)

    Article  CAS  Google Scholar 

  56. A. Hajalilou, E. Abouzari-Lotf, R. Etemadifar, V. Abbasi-Chianeh, A. Kianvash, Fabrication by electrophoretic deposition of nano-Fe 3 O 4 and Fe 3 O 4@ SiO 2 3D structure on carbon fibers as supercapacitor materials. JOM 70(8), 1404–1410 (2018)

    Article  CAS  Google Scholar 

  57. H. Abdollah, H. Mansor, E.-K. Reza, M.M. Taghi, Effect of milling atmosphere on structural and magnetic properties of Ni–Zn ferrite nanocrystalline. Chin Phys B 24(4), 048102 (2015)

    Article  CAS  Google Scholar 

  58. S. Balakrishnan, M.J. Bonder, G.C. Hadjipanayis, Particle size effect on phase and magnetic properties of polymer-coated magnetic nanoparticles. J. Magn. Magn. Mater. 321(2), 117–122 (2009)

    Article  CAS  Google Scholar 

  59. X. Batlle, P. Guardia, O. Iglesias, A. Labarta, A.G. Roca, M. Puerto Morales, C.J. Serna, Magnetite Nanoparticles with Almost Bulk Magnetic Properties: The Role of the Surfactant (APS March Meeting Abstracts, Chicago, 2007), pp. P14-013

    Google Scholar 

  60. V. Šepelák, K. Becker, Mössbauer studies in the mechanochemistry of spinel ferrites. J. Mater. Synth. Process. 8(3), 155–166 (2000)

    Article  Google Scholar 

  61. A. Hajalilou, M. Hashim, R. Ebrahimi-Kahrizsangi, N. Sarami, Influence of CaO and SiO2 co-doping on the magnetic, electrical properties and microstructure of a Ni–Zn ferrite. J. Phys. D Appl. Phys. 48(14), 145001 (2015)

    Article  CAS  Google Scholar 

  62. S. El-Dek, M.A. Ali, S.M. El-Zanaty, S.E. Ahmed, Comparative investigations on ferrite nanocomposites for magnetic hyperthermia applications. J. Magn. Magn. Mater. 458, 147–155 (2018)

    Article  CAS  Google Scholar 

  63. G. Kandasamy, S. Khan, J. Giri, S. Bose, N.S. Veerapu, D. Maity, One-pot synthesis of hydrophilic flower-shaped iron oxide nanoclusters (IONCs) based ferrofluids for magnetic fluid hyperthermia applications. J. Mol. Liq. 275, 699–712 (2019)

    Article  CAS  Google Scholar 

  64. D.-L. Zhao, X.-W. Zeng, Q.-S. Xia, J.-T. Tang, Preparation and coercivity and saturation magnetization dependence of inductive heating property of Fe3O4 nanoparticles in an alternating current magnetic field for localized hyperthermia. J. Alloy. Compd. 469(1–2), 215–218 (2009)

    Article  CAS  Google Scholar 

  65. A. Mallick, A. Mahapatra, A. Mitra, J.-M. Greneche, R. Ningthoujam, P. Chakrabarti, Magnetic properties and bio-medical applications in hyperthermia of lithium zinc ferrite nanoparticles integrated with reduced graphene oxide. J. Appl. Phys 123(5), 055103 (2018)

    Article  CAS  Google Scholar 

  66. B. Mehdaoui, A. Meffre, J. Carrey, S. Lachaize, L.M. Lacroix, M. Gougeon, B. Chaudret, M. Respaud, Optimal size of nanoparticles for magnetic hyperthermia: a combined theoretical and experimental study. Adv. Funct. Mater. 21(23), 4573–4581 (2011)

    Article  CAS  Google Scholar 

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Rezanezhad, A., Hajalilou, A., Eslami, F. et al. Superparamagnetic magnetite nanoparticles for cancer cells treatment via magnetic hyperthermia: effect of natural capping agent, particle size and concentration. J Mater Sci: Mater Electron 32, 24026–24040 (2021). https://doi.org/10.1007/s10854-021-06865-8

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