An In-Vivo Study of Sonodynamic Therapy with Encapsulated Hematoporphyrin
,
Abstract
Purpose: According to the side effects of invasive cancer treatments, Sonodynamic Therapy (SDT) as a noninvasive method for breast adenocarcinoma was considered. Sonosensitizer agents’ encapsulation can improve the accumulation of these drugs in the tumor tissue and reduce treatment side effects. Hence, mice breast adenocarcinoma SDT with Hematoporphyrin (HP) and HP-encapsulated Mesoporous Silica Nanoparticles (HP-MSNs) was carried out.
Materials and Methods: Ninety-six female breast adenocarcinoma grafted Balb/C mice were randomly divided into 16 groups (n = 6): control, sham, HP, HP-MSN, Ultrasound (US), SDT+HP, and SDT+HP-MSN groups. Sonosensitizer agents were injected intraperitoneally (2.5 or 5 mg/kg, 0.2 ml) 24h before an US radiation (1MHz, 1 or 2 W/cm2, 60 sec). The tumor growth parameters were evaluated 30 days after SDT.
Results: The inhibition ratio was enhanced by 23, 18, 18, and 16% relative to the control group in HP-MSN (5 mg/kg), HP-MSN (2.5 mg/kg) HP (5 mg/kg) and US (2 W/cm2) groups, respectively, at 18 days after the injection time; whereas, the analysis of findings revealed an antitumor effect in SDT with HP-MSN groups. The Tumor Growth Inhibition (TGI) percentages were 45, 42, and 42% for the SDT (2 W/cm2) + HP-MSN (5 mg/kg), SDT (1 W/cm2) + HP-MSN (5 mg/kg), and SDT (2 W/cm2) + HP (2.5 mg/kg) groups, respectively, on the 18th day post-injection, and T2 and T5 times were higher than that of control and sham groups (P<0.05). The estimated 44-day survival time in the Kaplan-Meier test was 95% in the SDT (2 W/ cm2) + HP-MSN (5 mg/kg) treated group, which had moderately differentiated cells in tumor grading.
Conclusion: Based on the findings, SDT with HP-encapsulated MSNs (5 mg/kg) has an antitumor effect on breast adenocarcinoma.
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22- S. Jafari, M. Jadidi, H. Hasanzadeh, T. Khani, R. Nasr, and V. Semnani, "Sonodynamic therapy of mice breast adenocarcinoma with HP-MSN." Iran J Sci Technol Trans Sci, (2020).
23- Naiara I Vazquez, Zoilo Gonzalez, Begona Ferrari, and Yolanda Castro, "Synthesis of mesoporous silica nanoparticles by sol–gel as nanocontainer for future drug delivery applications." Boletín de la Sociedad Española de Cerámica y Vidrio, Vol. 56 (No. 3), pp. 139-45, (2017).
24- M.A. Shahbazi, B. Herranz, and H.A. Santos, "Nanostructured porous Si-based nanoparticles for targeted drug delivery." Biomatter, Vol. 2 (No. 4), pp. 1-17, (2012).
25- X. Yu, I. Trase, M. Ren, K. Duval, X. Guo, and Z. Chen, "Design of nanoparticle-based carriers for targeted drug delivery." Journal Nanomaterials, (2016).
26- M. Alamolhoda and M. Mokhtari-Dizaji, "Evaluation of fractionated and repeated sonodynamic therapy by using dual frequency for murine model of breast adenocarcinoma." Journal Therapeutic Ultrasound, Vol. 3 (No. 10), pp. 1-9, (2015).
27- M. Alamolhoda, M. Mokhtari-Dizaji, A.H. Barati, and H. Hasanzadeh, "Comparing the in vivo sonodynamic effects of dual and single frequency ultrasound in breast adenocarcinoma." Journal Medical Ultrasonics, Vol. 39 (No. 3), pp. 115-25, (2012).
28- H.J. Bloom and W.W. Richardson, "Histological grading and prognosis in breast cancer: a study of 1409 cases of which 359 have been followed for 15 years." Br J Cancer, Vol. 11pp. 359-77, (1957).
29- N. Yumita, R. Nishigaki, K. Umemura, and Si. Umemura, "Hematoporphyrin as a sensitizer of cell‐damaging effect of ultrasound." Japanese Journal Cancer Research, Vol. 80 (No. 3), pp. 219-22, (1989).
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31- L. Osminkina et al., "Silicon nanoparticles as amplifiers of the ultrasonic effect in sonodynamic therapy." Bulletin Experimental Biology Medicine, Vol. 161 (No. 2), pp. 296-99, (2016).
32- S. Gelperina, K. Kisich, M.D. Iseman, and L. Heifets, "The potential advantages of nanoparticle drug delivery systems in chemotherapy of tuberculosis." Am J Respir Crit Care Med, Vol. 172 (No. 12), pp. 1487-90, (2005).
33- A.H. Barati, M. Mokhtari-Dizaji, H. Mozdarani, Z. Bathaie, and M.H. Hassan, "Effect of exposure parameters on cavitation induced by low-level dual-frequency ultrasound." Ultrasonics Sonochemistry, Vol. 14 (No. 6), pp. 783-89, (2007).
34- Wenwen Yue et al., "Checkpoint blockade and nanosonosensitizer-augmented noninvasive sonodynamic therapy combination reduces tumour growth and metastases in mice." Nature communications, Vol. 10 (No. 1), pp. 1-15, (2019).
35- Y. Lv et al., "Antiproliferative and apoptosis-inducing effect of exo-Protoporphyrin IX based sonodynamic therapy on human oral Squamous cell carcinoma." Scientific Reports, Vol. 7 (No. 40967), (2017).
36- Hui Gao et al., "pH-Responsive Nanoparticles for Enhanced Antitumor Activity by High-Intensity Focused Ultrasound Therapy Combined with Sonodynamic Therapy." International Journal of Nanomedicine, Vol. 17p. 333, (2022).
37- X. Huang, N.P. Young, and H. Townley, "Characterization and comparison of Mesoporous silica particles for optimized drug delivery regular." Nanomater Nanotechnol, Vol. 4 (No. 2), pp. 1-15, (2014).
38- T. Wang, L. Zhang, Z. Su, C. Wang, Y. Liao, and Q. Fu, "Multifunctional hollow mesoporous silica nanocages for cancer cell detection and the combined chemotherapy and photodynamic therapy." ACS Appl Mater Interfaces, pp. 2479-86, (2011).
39- Q. Liu, X. Li, L. Xiao, P. Wang, X. Wang, and W. Tang, "Sonodynamically induced antitumor effect of hematoporphyrin on Hepatoma 22." Ultrason Sonochem, Vol. 15 (No. 6), pp. 943-48, (2008).
40- Shengjie Sun and Meiying Wu, "Sonodynamic Therapy: another “light” in tumor treatment by exogenous stimulus." Smart Materials in Medicine, Vol. 2pp. 145-49, (2021).
41- Y. Zheng et al., "Hematoporphyrin encapsulated PLGA microbubble for contrast enhanced ultrasound imaging and sonodynamic therapy." Journal Microencapsulation, Vol. 29 (No. 5), pp. 437-44., (2012).
42- G. Canavese et al., "Nanoparticle-assisted ultrasound: A special focus on sonodynamic therapy against cancer." Chem Eng J, Vol. 15 (No. 340), pp. 155-72, (2018).
43- Yuki Horise et al., "Sonodynamic therapy with anticancer micelles and high-intensity focused ultrasound in treatment of canine cancer." Frontiers in Pharmacology, p. 545, (2019).
2- B.M. Rabatic, "Experimental therapies in breast cancer." Breast Cancer Biology Radiation Oncologist, pp. 81-90, (2014).
3- T.J. Dougherty et al., "Photodynamic therapy." Journal National Cancer Institute, Vol. 90pp. 889-905, (1998).
4- H. Chen, X. Zhou, Y. Gao, B. Zheng, F. Tang, and J. Huang, "Recent progress in development of new sonosensitizers for sonodynamic cancer therapy." Drug Discovery Today, Vol. 19pp. 502-09, (2014).
5- M. Intra et al., "A new option for early breast cancer patients previously irradiated for Hodgkin's disease: intraoperative radiotherapy with electrons (ELIOT)." Breast Cancer Research, Vol. 7 (No. 5), pp. R828-R32, (2005).
6- M. Rezaei-Tavirani, E. Dolat, H. Hasanzadeh, S.S. Seyyedi, V. Semnani, and Sobhi S., "TiO2 nanoparticle as a sensitizer drug in radiotherapy: in vitro study." Iranian Journal Cancer Prevention, Vol. 6pp. 37-44, (2013).
7- K. Tachibana, Jr. LB. Feril, and Y. Ikeda-Dantsuji, "Sonodynamic therapy " Ultrasonics, Vol. 48pp. 253-59, (2008).
8- A.P. McHale, J.F. Callan, N. Nomikou, C. Fowley, and B. Callan, "Sonodynamic therapy: concept, mechanism and application to cancer treatment." Therapeutic Ultrasound, Vol. 880pp. 429-50, (2016).
9- I. Rosenthal, J.Z. Sostaric, and P. Riesz, "Sonodynamic therapy- a review of the synergistic effects of drugs and ultrasound." Ultrasonics Sonochemistry, Vol. 11pp. 349-63, (2004).
10- T. Yu, Z. Wang, and Mason T.J., "A review of research into the uses of low level ultrasound in cancer therapy." Ultrasonics Sonochemistry, Vol. 11pp. 95-103, (2004).
11- H. Shibaguchi, H. Tsuru, M. Kuroki, and M. Kuroki, "Sonodynamic cancer therapy: a non-invasive and repeatable approach using low-intensity ultrasound with a sonosensitizer." Anticancer Research, Vol. 31pp. 2425-29, (2011).
12- W.K. Bai, E. Shen, and B. Hu, "Induction of the apoptosis of cancer cell by sonodynamic therapy: a review." Chinese Journal Cancer Research, Vol. 24pp. 368-73, (2012).
13- G.Y. Wan, Y. Liu, B.W. Chen, Y.Y. Liu, Y.S. Wang, and N. Zheng, "Recent advances of sonodynamic therapy in cancer treatment " Cancer Biol Med, Vol. 13 (No. 3), (2016).
14- M. Kuroki et al., "Sonodynamic therapy of cancer using novel sonosensitizers." Anticancer research, Vol. 27 (No. 5), pp. 3673-78, (2017).
15- N. Yumita, R. Nishigaki, and S.I. Umemura, "Sonodynamically induced antitumor effect of Photofrin II on colon 26 carcinoma." Journal Cancer Research Clinical Oncology, (2000).
16- P. Tharkar, R. Varanasi, W.S.F. Wong, C.T. Jin, and W. Chrzanowski, "Nano-enhanced drug delivery and therapeutic ultrasound for cancer treatment and beyond." Frontiers in Bioengineering and Biotechnology, (2019).
17- B.G. Trewyn, S. Giri, I.I. Slowing, and VS-Y. Lin, "Mesoporous silica nanoparticle based controlled release, drug delivery, and biosensor systems." Chem Commun, Vol. 31pp. 3236-345, (2017).
18- J.L. Paris, M.V. Cabañas, M. Manzano, and M. Vallet-Regí, "Polymer-grafted mesoporous silica nanoparticles as ultrasound-responsive drug carriers." ACS Nano, Vol. 9pp. 11023-33, (2015).
19- P. Dogra et al., "Establishing the effects of mesoporous silica nanoparticle properties on in vivo disposition using imaging-based pharmacokinetics." Nature communications, Vol. 9 (No. 4551), pp. 1-14, (2018).
20- C. Beharti, U. Nagaich, A.K. Pal, and N. Gulati, "Mesoporous silica nanoparticles in target drug delivery system: A review." International Journal Pharmaceutical Investigation, Vol. 5 (No. 3), pp. 124-33, (2015).
21- A. Khaleghian, H. Hasanzadeh, A. Moshtaghian, R. Nasr, A. Emadi, and S. Moshfegh, "Inhibitory effects of silica nanoparticles loaded with hematoporphyrin on breast cancer cell line." Middle East J Rehabil Health Stud, Vol. 5 (No. 3), (2018).
22- S. Jafari, M. Jadidi, H. Hasanzadeh, T. Khani, R. Nasr, and V. Semnani, "Sonodynamic therapy of mice breast adenocarcinoma with HP-MSN." Iran J Sci Technol Trans Sci, (2020).
23- Naiara I Vazquez, Zoilo Gonzalez, Begona Ferrari, and Yolanda Castro, "Synthesis of mesoporous silica nanoparticles by sol–gel as nanocontainer for future drug delivery applications." Boletín de la Sociedad Española de Cerámica y Vidrio, Vol. 56 (No. 3), pp. 139-45, (2017).
24- M.A. Shahbazi, B. Herranz, and H.A. Santos, "Nanostructured porous Si-based nanoparticles for targeted drug delivery." Biomatter, Vol. 2 (No. 4), pp. 1-17, (2012).
25- X. Yu, I. Trase, M. Ren, K. Duval, X. Guo, and Z. Chen, "Design of nanoparticle-based carriers for targeted drug delivery." Journal Nanomaterials, (2016).
26- M. Alamolhoda and M. Mokhtari-Dizaji, "Evaluation of fractionated and repeated sonodynamic therapy by using dual frequency for murine model of breast adenocarcinoma." Journal Therapeutic Ultrasound, Vol. 3 (No. 10), pp. 1-9, (2015).
27- M. Alamolhoda, M. Mokhtari-Dizaji, A.H. Barati, and H. Hasanzadeh, "Comparing the in vivo sonodynamic effects of dual and single frequency ultrasound in breast adenocarcinoma." Journal Medical Ultrasonics, Vol. 39 (No. 3), pp. 115-25, (2012).
28- H.J. Bloom and W.W. Richardson, "Histological grading and prognosis in breast cancer: a study of 1409 cases of which 359 have been followed for 15 years." Br J Cancer, Vol. 11pp. 359-77, (1957).
29- N. Yumita, R. Nishigaki, K. Umemura, and Si. Umemura, "Hematoporphyrin as a sensitizer of cell‐damaging effect of ultrasound." Japanese Journal Cancer Research, Vol. 80 (No. 3), pp. 219-22, (1989).
30- L. Quan-hong 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." Journal Experimental Clinical Cancer Research, Vol. 23 (No. 2), pp. 333-41, (2004).
31- L. Osminkina et al., "Silicon nanoparticles as amplifiers of the ultrasonic effect in sonodynamic therapy." Bulletin Experimental Biology Medicine, Vol. 161 (No. 2), pp. 296-99, (2016).
32- S. Gelperina, K. Kisich, M.D. Iseman, and L. Heifets, "The potential advantages of nanoparticle drug delivery systems in chemotherapy of tuberculosis." Am J Respir Crit Care Med, Vol. 172 (No. 12), pp. 1487-90, (2005).
33- A.H. Barati, M. Mokhtari-Dizaji, H. Mozdarani, Z. Bathaie, and M.H. Hassan, "Effect of exposure parameters on cavitation induced by low-level dual-frequency ultrasound." Ultrasonics Sonochemistry, Vol. 14 (No. 6), pp. 783-89, (2007).
34- Wenwen Yue et al., "Checkpoint blockade and nanosonosensitizer-augmented noninvasive sonodynamic therapy combination reduces tumour growth and metastases in mice." Nature communications, Vol. 10 (No. 1), pp. 1-15, (2019).
35- Y. Lv et al., "Antiproliferative and apoptosis-inducing effect of exo-Protoporphyrin IX based sonodynamic therapy on human oral Squamous cell carcinoma." Scientific Reports, Vol. 7 (No. 40967), (2017).
36- Hui Gao et al., "pH-Responsive Nanoparticles for Enhanced Antitumor Activity by High-Intensity Focused Ultrasound Therapy Combined with Sonodynamic Therapy." International Journal of Nanomedicine, Vol. 17p. 333, (2022).
37- X. Huang, N.P. Young, and H. Townley, "Characterization and comparison of Mesoporous silica particles for optimized drug delivery regular." Nanomater Nanotechnol, Vol. 4 (No. 2), pp. 1-15, (2014).
38- T. Wang, L. Zhang, Z. Su, C. Wang, Y. Liao, and Q. Fu, "Multifunctional hollow mesoporous silica nanocages for cancer cell detection and the combined chemotherapy and photodynamic therapy." ACS Appl Mater Interfaces, pp. 2479-86, (2011).
39- Q. Liu, X. Li, L. Xiao, P. Wang, X. Wang, and W. Tang, "Sonodynamically induced antitumor effect of hematoporphyrin on Hepatoma 22." Ultrason Sonochem, Vol. 15 (No. 6), pp. 943-48, (2008).
40- Shengjie Sun and Meiying Wu, "Sonodynamic Therapy: another “light” in tumor treatment by exogenous stimulus." Smart Materials in Medicine, Vol. 2pp. 145-49, (2021).
41- Y. Zheng et al., "Hematoporphyrin encapsulated PLGA microbubble for contrast enhanced ultrasound imaging and sonodynamic therapy." Journal Microencapsulation, Vol. 29 (No. 5), pp. 437-44., (2012).
42- G. Canavese et al., "Nanoparticle-assisted ultrasound: A special focus on sonodynamic therapy against cancer." Chem Eng J, Vol. 15 (No. 340), pp. 155-72, (2018).
43- Yuki Horise et al., "Sonodynamic therapy with anticancer micelles and high-intensity focused ultrasound in treatment of canine cancer." Frontiers in Pharmacology, p. 545, (2019).
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| Issue | Vol 10 No 2 (2023) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/fbt.v10i2.12218 | |
| Keywords | ||
| Breast Adenocarcinoma Sonodynamic Therapy Hematoporphyrin Mesoporous Silica Nanoparticles | ||
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How to Cite
1.
Souri S, Jadidi M, Hasanzadeh H, Khani T, Semnani V. An In-Vivo Study of Sonodynamic Therapy with Encapsulated Hematoporphyrin. Frontiers Biomed Technol. 2022;10(2):140-149.
