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Sonodynamic and sono-photodynamic therapy in oncology

https://doi.org/10.24931/2413-9432-2019-8-2-31-46

Abstract

In the present publication, authors have analyzed the results of using sonodynamic and sono-photodynamic therapy with photosensitizing agents of various classes (hematoporphyrin, 5-aminolevulinic acid, chlorin derivatives, etc.) in experimental oncology. In a number of in vitro and in vivo studies, the high antitumor efficacy of the above treatment methods has been proven. Ultrasonic treatment with a pulse frequency of 1–3 MHz and an intensity of 0.7 to 5 W/cm2 , independently and in combination with photo-irradiation of experimental tumors, can significantly improve the cytotoxic properties of photosensitizers. This became the basisfor testing the methodsin patients with malignant neoplasms of various localizations. Scientists fromSouth-East Asia presented the preliminary results of the use of sonodynamic and sono-photodynamic therapy with photosensitizers in the treatment of malignant pathology of the mammary gland, stomach, esophagus, prostate, lung and brain. Analysis of the obtained data indicates the absence of serious adverse events and an increase in the antitumor efficacy of treatment, which included these treatment methods with chlorin-type photosensitizers. 

About the Authors

D. A. Tzerkovsky
N.N. Alexandrov National Cancer Centre of Belarus
Belarus
Lesnoy


E. L. Protopovich
N.N. Alexandrov National Cancer Centre of Belarus
Belarus
Lesnoy


D. S. Stupak
N.N. Alexandrov National Cancer Centre of Belarus
Belarus
Lesnoy


References

1. Escoffre J.M. and Bouakaz A.B. Therapeutic ultrasound. Switzerland, Springer, 2016. 459 p.

2. Ulashchik V.S., Chirkin A.A. Ultrazvukovaya terapiya [Ultrasound therapy].Minsk, Belarus Publ., 1983. 254 p.

3. Couture O., Foley J., Kassel N.F., Larrat B., Aubry J.-F. Review of ultrasound mediated drug delivery for cancer treatment: updates from pre-clinical studies, Transl. Cancer Res., 2014, vol. 3, no. 5, pp. 494–511.

4. Costley D., McEwan C., Fowleym C., McHale A.P., Atchison J., Nomikou N., Callan J.F. Treating cancer with sonodynamic therapy: A review,Int. J. Hyperthermia, 2015, vol. 32, no. 2, pp. 107–117.

5. Nikolaev A.L., Gopin A.V., Bozhevolnov V.E., Treshalina H.M., Andronova N.V., Melikhov I.V., Filonenko E.V., Mazina S.E., Gerasimova G.K., Khorosheva E.V., Mikhailova I.N., Demidov L.V., Bokhyan B.Yu., Kogan B.Ya., Kaliya O.L. Combined method of ultrasound therapy of oncological diseases, Rus. J.Gen. Chem., 2015, vol. 85, no. 1, pp. 303–320.

6. Liu X. H., Li S., Wang M., Dai Z.J. Current status and future perspectives of sonodynamic therapy and sonosensitiers, Asian Pac. J. Cancer Prev., 2015, vol. 16, no. 11, pp. 4489–4492.

7. Rosenthal I., Sostaric J.Z., Riesz P. Sonodynamic therapy – a review of the synergistic effects of drugs and ultrasound, Ultrasonics Sonochem., 2004, vol. 11, pp. 349–363.

8. Yumita Т., Nishigaki T., Umemura K., Umemura S.-I. Synergetic effect of ultrasound and hematoporphyrin on sarcoma 180, J. Jpn. Cancer Res., vol. 81, 1990, p. 304.

9. McHale A.P., Callan J.F., Nomikou N., Fowley C., Callan B. Sonodynamic therapy: concept, mechanism and application to cancer treatment, Adv. Exp. Med. Biol., 2016, vol. 880, pp. 429–450.

10. Xiong W., Wang P., Hu J., Jia Y., Wu L., Chen X., Liu Q., Wang X. A new sensitizer DVDMS combined with multiple focused ultrasound treatments: an effective antitumor strategy, Sci. Rep., 2015, vol. 5, e17485.

11. Sun H., Ge W., Gao X., Wang S., Jiang S., Hu Y., Yu M., Hu S. Apoptosis-promoting effects of hematoporphyrin monomethyl ethersonodynamic therapy (HMME-SDT) on endometrial cancer, PLoS One, 2015, vol. 10, no. 9, e0137980.

12. Li Y.N., Zhou Q., Yang B., Hu Z., Wang J.H., Li Q.S., Cao W.W. Mechanism of rat osteosarcoma cell apoptosis induced by a combination of low-intensity ultrasound and 5-aminolevulinic acid in vitro, Genet. Mol. Res., 2015, vol. 14, no. 3, pp. 9604–9613.

13. Hu Z., Fan H., Lu G., Zhou Q., Yang B., Zheng J., Cao W. 5-Aminolevulinic acid-mediated sonodynamic therapy induces antitumor effects in malignant melanoma via p53-miR-34a-Sirt1 axis, J. Dermatol. Sci., 2015, vol. 79, no. 2, pp. 155–162.

14. Liu X., Li W., Geng S., Meng Q.G., Bi Z.G. Apoptosis induced by sonodynamic therapy in human osteosarcoma cells in vitro, Mol. Med. Rep., 2015, vol. 12, no. 1, pp. 1183–1188.

15. Wang X.J., Luo J., Leung A.W., Li Y., Zhang H., Xu C. Hypocrellin B in hepatocellular carcinoma cells: Subcellular localization and sonodynamic damage, Int. J. Radiat. Biol., 2015, vol. 91, no. 5, pp. 399–406.

16. Xiang J., Leung A.W., Xu C. Effect of ultrasound sonication on clonogenic survival and mitochondria of ovarian cancer cells in the presence of methylene blue, J. Ultrasound Med., 2014, vol. 33, no. 10, pp. 1755–1761.

17. Dai S., Xu C.Q., Tien Y., Cheng W., Li B. In vitro stimulation of calcium overload and apoptosis by sonodynamic therapy combined with hematoporphyrin monomethyl ether in C6 glioma cells, Oncol. Lett., 2014, vol. 8, no. 4, pp. 1675–1681.

18. Li Y.J., Huang P., Jiang C.L., Jia de X., Du X.X., Zhou J.H., Han Y., Sui H., Wei X.L., Liu L., Yuan H.H., Zhang T.T., Zhang W.J., Xie R., Lang X.H., Wang L.Y., Liu T., Bai Y.X., Tian Y. Sonodynamically induced anti-tumor effect of 5-aminolevulinic acid on pancreatic cancer cells, Ultrasound Med. Biol., 2014, vol. 40, no. 11, pp. 2671–2679.

19. Su X., Li Y., Wang P., Wang X., Liu Q. Protoporphyrin IX-mediated sonodynamic action induces apoptosis of K562 cells, Ultrasonics, 2014, vol. 54, pp. 275–284.

20. Chen B., Zheng R., Liu D., Li B., Lin J., Zhang W. The tumor affinity of chlorin e6 and its sonodynamic effects on non-small cell lung cancer, Ultrason. Sonochem., 2013, vol. 20, no. 2, pp. 667–673.

21. Su X., Wang P., Wang X., Cao B., Li L., Liu Q. Apoptosis of U937 cells Induced by hematoporphyrin monomethyl ether-mediated sonodynamic action, Cancer Biother. Radiopharm., 2013, vol. 28, no. 3, pp. 207–217.

22. Foglietta F., Canaparo R., Francovich A., Arena F., Civera S., Cravotto G., Frairia R., Serpe L. Sonodynamic treatment as an innovative bimodal anticancer approach: shock wave-mediated tumor growth inhibition in a syngeneic breast cancer model, Discov. Med., 2015, vol. 20, no. 110, pp. 197–205.

23. Li Y., Zhou Q., Hu Z., Yang B., Li Q., Wang J., Zheng J., Cao W. 5-Aminolevulinic acid-based sonodynamic therapy induces the apoptosis of osteosarcoma in mice, PLoS One., 2015, vol. 10, no. 7, e0132074.

24. 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, vol. 3, p. 10.

25. Hu Z., Fan H., Lu G., Zhou Q., Yang B., Zheng J., Cao W. 5-Aminolevulinic acid-mediated sonodynamic therapy induces anti-tumor effects in malignant melanoma via p53-miR-34a-Sirt1 axis, J.Dermatol. Sci., 2015, vol. 79, no. 2, pp. 155–162.

26. Song D., Yue W., Li Z., Li J., Zhao J., Zhang N. Study of the mechanism of sonodynamic therapy in a rat glioma model, Onco Targets Ther., 2014, vol. 7, pp. 1801–1810.

27. Li C., Zhang K., Wang P., Hu J., Liu Q., Wang X. Sonodynamic antitumor effect of a novel sonosensitizer on S180 solid tumor, Biopharm. Drug Dispos., 2014, vol. 35, no. 1, pp. 50–59.

28. Wang S., Hu Z., Wang X., Gu C., Gao Z., Cao W., Zheng J. 5-Aminolevulinic acid-mediated sonodynamic therapy reverses macrophage and dendritic cell passivity in murine melanoma xenografts, Ultrasound Med. Biol., 2014, vol. 40, no. 9, pp. 2125–2133.

29. Gao Z., Zheng J., Yang B., Wang Z., Fan H., Lv Y., Li H., Jia L., Cao W. Sonodynamic therapy inhibits angiogenesis and tumor growth in a xenograft mouse model, Cancer Lett., 2013, vol. 335, pp. 93–99.

30. Chen B., Zheng R., Liu D., Li B., Lin J., Zhang W. The tumor affinity of chlorin e6 and its sonodynamic effects on non-small cell lung cancer, Ultrason. Sonochem., 2013, vol. 20, no. 2, pp. 667–673.

31. Yamaguchi S., Endo S., Kudo N., Sumiyoshi K., Motegi H., Kobayashi H., Terasaka S., Houkin K. Porphyrin derivates-mediated sonodynamic therapy for malignant gliomas in vitro, Ultrasound Med. Biol., 2015, vol. 41, no. 9, pp. 2458–2465.

32. Tserkovsky D.A. Sono-photodynamic therapy – a new direction in the treatment of malignant brain tumors, Oncolog. Jurn., 2015, vol. 9, no. 1, pp. 94–106.

33. Kenyon J.N., Fulle R.J., Lewis T.J. Activated cancer therapy using light and ultrasound – a case series of sonodynamic photodynamic therapy in 115 patients over a 4 year period, Current Drug. Ther., 2009, vol. 4, pp. 179–193.

34. Rengeng L., Qianyu Z., Yuehong L., Zhongzhong P., Libo L. Sonodynamic therapy, a treatment developing from photodynamic therapy, Photodiagnosis Photodyn. Ther., 2017, vol. 19, pp. 159–166.

35. Bakhshizadeh M., Moshirian T., Esmaily H., Rajabi O., Nassirli H., Sazgarnia A. Sonophotodynamic therapy mediated by liposomal zinc phthalocyanine in a colon carcinoma tumor model: Role of irradiating arrangement, Iran J. Basic Med. Sci., 2017, vol. 20, no. 10, pp. 1088–1092.

36. Wang P., Li C., Wang X., Xiong W., Feng X., Liu Q., Leung A.W., Xu C. Anti-metastatic and pro-apoptotic effects elicited by combination photodynamic therapy with sonodynamic therapy on breast cancer both in vitro and in vivo, Ultrasonics Sonochem., 2015, vol. 23, pp. 116–127.

37. Tomankova K., Kolarova H., Vachutka J., Zapletalova J., Hanakova A., Kaplova E. Study of photodynamic, sonodynamic and antioxidative influence on HeLa cell line, Ind. J. Biochem. Biophys., 2014, vol. 51, pp. 19–28.

38. Li Q., Wang X., Wang P., Zhang K., Wang H., Feng X., Liu Q. Efficacy of chlorin e6-mediated sono-photodynamic therapy on 4T1 cells, Cancer Biother. Radiopharmac., 2014, vol. 29, no. 1, pp. 42–52.

39. Wang H., Wang X., Wang P., Zhang K., Yang S., Liu Q. Ultrasound enhances the efficacy of chlorin e6-mediated photodynamic therapy in MDA-MB-231 cells, Ultrasound Med. Biol., 2013, vol. 39, no. 9, pp. 1713–1724.

40. Li J. H., Chen Z. Q., Huang Z., Zhan Q., Ren F.B., Liu J.Y., Yue W., Wang Z. In vitro study of low intensity ultrasound combined with different doses of PDT: effects on C6 glioma cells, Oncol. Lett., 2013, vol. 5, no. 2, pp. 702–706.

41. Tzerkovsky D., Grachev Yu., Artsemyeva T., Istomin Yu. Sono-photodynamic therapy with a photolon of the recurrent form of the Grade IV glioblastoma multiforme: preliminary results of the first phase of a clinical study, Fotodinamicheskaya terapiya i fotodiagnostika, 2015, vol. 4, no. 1, pp. 32–33.

42. Tserkovsky D. A., Alexandrova E. N., Chalau V.N., Istomin Y.P. Effects of combined sonodynamic and photodynamic therapies with photolon on a glioma C6 tumor model, Exp. Oncol., 2012, vol. 34, no. 4, pp. 332–335.

43. Abder-Kader M.H. Photodynamic therapy. From theory to application. Verlag, Berlin, Heidelberg, Springer, 2014. 317 p.

44. Gomer C.J. Photodynamic therapy. Methods and protocols. New York, Humana Press, 2010. 299 p.

45. Rapozzi V. and Jori G. Resistance to photodynamic therapy in cancer. Switzerland, Springer, 2015. 251 p.

46. Couture O., Foley J., Kassel N.F., Larrat B., Aubry J.-F.Review of ultrasound mediated drug delivery for cancer treatment: updates from pre-clinical studies, Transl. Cancer Res., 2014, vol. 3, no. 5, pp. 494–511.

47. Huang Z., Moseley H., Bown S. Rationale of combined PDT and SDT modalities for treating cancer patients in terminal stage: the proper use of photosensitizer, Integr. Cancer Ther., 2010, vol. 9, no. 4. pp. 317–319.

48. Inui T., Makita K., Miura H., Matsuda A., Kuchiike D., Kubo K., Mette M., Uto Y., Nishikata T., Hori H., Sakamoto N. Case report: a breast cancer patient treated with GcMAF, sonodynamic therapy and hormone therapy, Anticancer Res., 2014, vol. 34, pp. 4589–4594.

49. Li L.Q., Wang X., Zhang I.W., Mitchell D. Primary clinical use of the sono-photo-dynamic therapy for advanced esophagocadiac and gastric adenocarcinoma, J. Clin. Oncol., 2014, vol. 32 (suppl.), e15024.

50. Wang X., Zhang W., Xu Z., Luo Y., Mitchell D., Moss R.W. Sonodynamic and photodynamic therapy in advanced breast carcinoma: a report of 3 cases, Integr. Cancer. Ther., 2009, vol. 8, no. 3, pp. 283–287.

51. Wang X.J., Mitchell D., Lewis T.J. Primary clinical use of sonodynamic therapy (SDT) for advanced breast cancer, J. Clin. Oncol., Abstracts ASCO Annual Meeting Proceedings, 2008, vol. 26, no. 15 (Suppl.), Abstract 12029.

52. Murphy D., Meade B., Sali A. Prostate cancer treated by sonodynamic and photodynamic therapies (SPDT, NGPDT), in 66th Annual Meeting «USANZ 2013», Melbourne, 13–16 April, 2013. Poster № 089.

53. Zhang W., Li K., Lu J., Peng Z., Wang X., Li Q., Zhao G., Hao J., Luo Y., Zhao Y., Yin X., O’Brien K.A. Sonodynamic and photodynamic therapy in breast cancer: a pilot study, Int. J. Complement. Alt. Med., 2017, vol. 9, no. 5, pp. 00313.

54. Istomin Yu., Tzerkovsky D., Grachev Yu., Artsemyeva T., Borichevsky F., Maslakov E., Semak I., Bagrintsev D. Intraoperative sono-photodynamic therapy with photolon in animal experiments and promising results of phase I clinical study in patients with recurrent malignant gliomas, J. Neuro-Oncol., 2016. vol. 2, no. 2, 16, pp. 1–9.


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Tzerkovsky D.A., Protopovich E.L., Stupak D.S. Sonodynamic and sono-photodynamic therapy in oncology. Biomedical Photonics. 2019;8(2):31-46. https://doi.org/10.24931/2413-9432-2019-8-2-31-46

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