Beneficial Effects of Dual Frequency Sonodynamic Therapy and Hematoporphyrin Mesoporous Silica Nanoparticles in the Treatment of Mice Breast Adenocarcinoma

Document Type : Original Article

Authors

Department of Medical Physics, Semnan University of Medical Sciences, Semnan, Iran

Abstract

Background: Sonodynamic therapy (SDT) may be a new hopeful non-invasive method for cancer treatment, which incorporates a combination of low-intensity ultrasound and a sonosensitive chemical. The goal of this study was to evaluate the effect of dual-frequency sonication (1 and 3 MHz) and injected Hematoporphyrin encapsulated in mesoporous silica nanoparticles (HP-MSNs) as a sensitizer in the treatment of mice grafted with breast adenocarcinoma.
Methods: In this research, one hundred and thirty-two female mice with grafted breast adenocarcinoma were separated into 22 groups including control, sham, 4 groups of sonication 1 or 3 MHz (1 and 2 W/cm2), and 16 groups of SDT with Hematoporphyrin (HP) and HP-MSNs (2.5 and 5 mg/kg). The tumor growth factors and tumor grading were used to assess the treatment management.
Results: The results indicate that dual-frequency sonication has a delayed effect on tumor growth. The required time of T5 to the initial volume in all groups of SDT with HP (5 mg/kg) was greater than that in the control group (P<0.05). It was observed that SDT with an injection of HP-MSNs was effective in delaying tumor growth and the time of T2 and T5 was higher than that of other groups (P<0.05). This group had Grade II (intermediate), while others had Grade III (high) malignancy in the histological study of mice breast adenocarcinoma.
Conclusion: Our results reveal that dual-frequency SDT therapy with HP-MSN has a delaying tumor growth effect on mice breast adenocarcinoma. Hence, the expansion of minimally invasive methods such as SDT is necessary.

Keywords


  1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin. 2015; 65(1):5-29. doi: 10.3322/caac.21254.
  2. Harirchi I, Karbakhsh M, Kashefi A, Momtahen AJ. Breast cancer in Iran: results of a multi-center study. Asian Pac J Cancer Prev. 2004;5(1):24-7. PMID: 15075000.
  3. Chen H, Zhou X, Gao Y, Zheng B, Tang F, Huang J. Recent progress in development of new sonosensitizers for sonodynamic cancer therapy. Drug Discov Today. 2014; 19(4):502-9. doi: 10.1016/j.drudis.2014.01.010.
  4. Wan GY, Liu Y, Chen BW, Liu YY, Wang YS, Zhang N. Recent advances of sonodynamic therapy in cancer treatment. Cancer Biol Med. 2016 ;13(3):325-38. doi: 10.20892/j.issn.2095-3941.2016.0068.
  5. McHale AP, Callan JF, Nomikou N, Fowley C, Callan B. Sonodynamic Therapy: Concept, Mechanism and Application to Cancer Treatment. Adv Exp Med Biol. 2016; 880:429-50. doi: 10.1007/978-3-319-22536-4_22.
  6. Rosenthal I, Sostaric JZ, Riesz P. Sonodynamic therapy--a review of the synergistic effects of drugs and ultrasound. Ultrason Sonochem. 2004; 11(6):349-63. doi: 10.1016/j.ultsonch.2004.03.004.
  7. Shibaguchi H, Tsuru H, Kuroki M, Kuroki M. Sonodynamic cancer therapy: A non-invasive and repeatable approach using low-intensity ultrasound with a sonosensitizer. Anticancer Res. 2011; 31(7):2425-9. PMID: 21873154.
  8. Hasanzadeh H, Mokhtari-Dizaji M, Zahra Bathaie S, Hassan ZM, Shahbazfar AA. Dual-frequency ultrasound activation of nanomicellar doxorubicin in targeted tumor chemotherapy. J Med Ultrason (2001). 2014; 41(2):139-50. doi: 10.1007/s10396-013-0484-x.
  9. Suslick KS, McNamara WB, Didenko Y. Hot Spot conditions during multi-bubble cavitation. In: Crum LA, Mason TJ, Reisse JL, Suslick KS. (eds). Sonochemistry and sonoluminescence. NATO ASI Series, vol 524. Dordrecht: Springer; 1999. doi: 10.1007/978-94-015-9215-4_16.
  10. Hasanzadeh H, Mokhtari-Dizaji M, Bathaie SZ, Hassan ZM. Effect of local dual frequency sonication on drug distribution from polymeric nanomicelles. Ultrason Sonochem. 2011; 18(5):1165-71. doi: 10.1016/j.ultsonch.2011.03.018.
  11. Yumita N, Nishigaki R, Umemura K, Umemura S. Hematoporphyrin as a sensitizer of cell-damaging effect of ultrasound. Jpn J Cancer Res. 1989; 80(3):219-22. doi: 10.1111/j.1349-7006.1989.tb02295.x.
  12. Umemura S, Yumita N, Nishigaki R, Umemura K. Sonochemical activation of hematoporphyrin: a potential modality for cancer treatment. IEEE Ultrasonics Symposium; 1989, pp. 955-60 vol.2, doi: 10.1109/ULTSYM.1989.67130.
  13. Wang T, Zhang L, Su Z, Wang C, Liao Y, Fu Q. Multifunctional hollow mesoporous silica nanocages for cancer cell detection and the combined chemotherapy and photodynamic therapy. ACS Appl Mater Interfaces. 2011; 3(7):2479-86. doi: 10.1021/am200364e.
  14. Paris JL, Cabanas MV, Manzano M, Vallet-Regi Polymer-grafted mesoporous silica nanoparticles as ultrasound-responsive drug carriers. ACS Nano. 2015; 9(11): 11023-33. doi: 10.1021/acsnano.5b04378.
  15. Mekaru H, Lu J, Tamanoi F. Development of mesoporous silica-based nanoparticles with controlled release capability for cancer therapy. Adv Drug Deliv Rev. 2015; 95:40-9. doi: 10.1016/j.addr.2015.09.009.
  16. Zheng Y, Zhang Y, Ao M, Zhang P, Zhang H, Li P, et al. Hematoporphyrin encapsulated PLGA microbubble for contrast enhanced ultrasound imaging and sonodynamic therapy. J Microencapsul. 2012; 29(5):437-44. doi: 10.3109/02652048.2012.655333.
  17. Yang KN, Zhang CQ, Wang W, Wang PC, Zhou JP, Liang XJ. pH-responsive mesoporous silica nanoparticles employed in controlled drug delivery systems for cancer treatment. Cancer Biol Med. 2014; 11(1):34-43. doi: 10.7497/j.issn.2095-3941.2014.01.003.
  18. Xu Z, Liu S, Kang Y, Wang M. Glutathione-and pH-responsive nonporous silica prodrug nanoparticles for controlled release and cancer therapy. Nanoscale. 2015; 7(13): 5859-68. doi:10.1039/C5NR00297D.
  19. Feng R, Zhao Y, Zhu C, Mason T. Enhancement of ultrasonic cavitation yield by multi-frequency sonication. Ultrasonics sonochemistry 2002; 9(5): 231-6. doi: 10.1016/S1350-4177(02)00083-4.
  20. Alamolhoda M, Mokhtari-Dizaji M, Barati AH, Hasanzadeh H. Comparing the in vivo sonodynamic effects of dual- and single-frequency ultrasound in breast adenocarcinoma. J Med Ultrason. 2012; 39(3):115-25. doi: 10.1007/s10396-012-0348-9.
  21. Kanthale P M, Brotchie A, Ashokkumar M, Grieser F. Experimental and theoretical investigations on sonoluminescenceunder dual frequency conditions. Ultrasonics Sonochemistry. 2008; 15(4):629-35. doi: 10.1016/j.ultsonch.2007.08.006.
  22. Vazquez N I, Gonzalez Z, Ferrari B, Castro Y. Synthesis of mesoporous silica nanoparticles by sol-gel as nanocontainer for future drug delivery applications. BoletinSociedad Espanola Ceramica Vidrio. 2017; 56(3): 139-45. doi: 10.1016/j.bsecv.2017.03.002.
  23. Shahbazi MA, Herranz B, Santos HA. Nanostructured porous Si-based nanoparticles for targeted drug delivery. Biomatter. 2012; 2(4):296-312. doi: 10.4161/biom.22347.
  24. Bharti C, Nagaich U, Pal AK, Gulati N. Mesoporous silica nanoparticles in target drug delivery system: A review. Int J Pharm Investig. 2015; 5(3):124-33. doi: 10.4103/2230-973X.160844.
  25. Yu X, Trase I, Ren M, Duval K, Guo X, Chen Z. Design of nanoparticle-based carriers for targeted drug delivery. Journal Nanomaterials. 2016; 2016:1087250. doi: 10.1155/2016/1087250.
  26. Alamolhoda M, Mokhtari-Dizaji M. Evaluation of fractionated and repeated sonodynamic therapy by using dual frequency for murine model of breast adenocarcinoma. J Ther Ultrasound. 2015; 3:10. doi: 10.1186/s40349-015-0031-x.
  27. Bloom HJ, and Richardson WW. Histological grading and prognosis in breast cancer; a study of 1409 cases of which 359 have been followed for 15 years. Br J Cancer. 1957; 11(3):359-77. doi: 10.1038/bjc.1957.43.
  28. Barati AH, Mokhtari-Dizaji M, Mozdarani H, Bathaie Z, Hassan ZM. Effect of exposure parameters on cavitation induced by low-level dual-frequency ultrasound. Ultrason Sonochem. 2007; 14(6):783-9. doi: 10.1016/j.ultsonch.2006.12.016.
  29. Guan L, Xu G. Damage effect of high-intensity focused ultrasound on breast cancer tissues and their vascularities. World J Surg Oncol. 2016; 14(1):153. doi: 10.1186/s12957-016-0908-3.
  30. Yue W, Chen L, Yu L, Zhou B, Yin H, Ren W, et al. Checkpoint blockade and nanosonosensitizer augmented noninvasive sonodynamic therapy combination reduces tumor growth and metastases in mice. NatCommun. 2019; 10:2025. doi: 10.1038/s41467-019-09760-3.
  31. Quan-hong L, Shi-hui S, Ya-ping X, Hao Q, Jin-xuan Z, Yao-hui R, et al. Synergistic anti-tumor effect of ultrasound and hematoporphyrin on sarcoma180 cells with special reference to the changes of morphology and cytochrome oxidase activity of tumor cells. J Exp Clin Cancer Res. 2004; 23(2):333-41. PMID: 15354420.
  32. Lv Y, Zheng J, Zhou Q, Jia L, Wang C, Liu N, et al. Antiproliferative and apoptosis-inducing effect of exo-Protoporphyrin IX based sonodynamic therapy on human oral squamous cell carcinoma. Sci Rep. 2017; 7:40967. doi:1038/srep40967.
  33. Jafari S, Jadidi M, Hasanzadeh H, Khani T, Nasr R, Semnani V. Sonodynamic therapy of mice breast adenocarcinoma with HP-MSN. Iran J Sci Technol Trans Sci. 2020; 44, 651–60. doi.org/10.1007/s40995-020-00893-5.
  34. Lee S, Yun HS, Kim SH. The comparative effects of mesoporous silica nanoparticles and colloidal silica on inflammation and apoptosis. Biomaterials. 2011; 32(35):9434-43. doi: 10.1016/j.biomaterials.2011.08.042.
  35. Ebrahim Niya A, Mokhtari M, Toliyat T. Evaluating the effects of dual frequency sonication parameters on acoustic cavitation by chemical dosimeter using iodide. Journal of Kerman University of Medical Sciences 2013; 20(2): 179-91.
  36. Wang J, Jiao Y, Shao Y. Mesoporous silica nanoparticles for dual-mode chemo-sonodynamic therapy by low-energy ultrasound. Materials (Basel). 2018; 11(10):2041. doi: 10.3390/ma11102041.
  37. Yu T, Wang Z, Mason TJ. A review of research into the uses of low level ultrasound in cancer therapy. Ultrason Sonochem. 2004; 11(2):95-103. doi: 10.1016/S1350-4177(03)00157-3.
  38. Canavese G, Ancona A, Racca L, Canta M, Dumontel B, Barbaresco F, et al. Nanoparticle-assisted ultrasound: A special focus on sonodynamic therapy against cancer. Chemical Engineering Journal. 2018; 340: 155-72. doi:10.1016/j.cej.2018.01.060.
  39. Horise Y, Maeda M, Konishi Y, Okamoto J, Ikuta S, Okamoto Y, et al. Sonodynamic therapy with anticancer micelles and hgh-intensity focused ultrasound in treatment of canine cancer. Front Pharmacol. 2019; 10:545. PMID: 31164823.