Photodynamic therapy in neurooncology

Literature review reflects the current status and development status of intraoperative photodynamic therapy in neurooncology and discusses the results of the most important studies on photodynamic  therapy (PDT). We searched the Pubmed, EMBASE, Cochrane Library and eLibrary data-bases for publications  published  between January 2000 and December 2022. Found 204 publications  in foreign sources and 59 publications  in domestic editions, dealing with the issues of photodynamic  therapy in neurooncology. An analysis of the literature has shown that intraoperative PDT in neurooncology is an important tool that contributes to increasing the radicality of the operation and local control. The basic rationale for the effectiveness of PDT lies in the study of the pathways leading to the complete devitalization of a malignant tumor, the study of the mechanisms of the local and systemic immune response. In addition, subcellular targets in PDT are determined by the properties of photosensitizers (PS). Second generation PSs have already been introduced into clinical practice. The effectiveness of PDT using photoditazine, 5-aminolevulinic acid has been demonstrated. The mechanisms of action and targets of these PS have been established. In Russia, a number of studies have repeatedly shown and proved the clinical effectiveness of PDT in groups of neurooncological patients with glial tumors and secondary metastatic tumors, but so far, the method has not been included in the clinical guidelines for the provision of high-tech neurosurgical care. There is certainly a need for further development of PTD techniques in neurooncology, especially in patients at high risk of recurrence and aggressive CNS tumors.

1. Urbanska K., et al. Glioblastoma multiforme – an overview // Contemp. Oncol, 2014, vol. 18 (5), рр. 307-312. doi: 10.5114/wo.2014.40559

2. Schneider T. et al. Gliomas in adults, Dtsch. Arzteblatt Int, 2010, vol. 107 (45), рр. 799-807. doi: 10.3238/arztebl.2010.0799

3. Gerrard G.E., et al. Neuro-oncology practice in the U.K., Clin. Oncol, 2003, vol. 15(8), рр. 478-484. doi: 10.1016/s0936-6555(03)00150-x

4. Tigliev G.S., Chesnokova E.A., Olyushin V.E., et al. A method of treating malignant brain tumors with a multifocal growth pattern, Patent RF, 2004, vol. 2236270, (In Russian)

5. Comfort A.V., Olyushin V.E., Ruslyakova I.A., et al. Method of photodynamic therapy for the treatment of glial tumors of the cerebral hemispheres, Patent RF, 2008, vol. 2318542 (In Russian)

6. Noske D.P., Wolbers J.G., Sterenborg H.J. Photodynamic therapy of malignant glioma. A review of literature, Clin Neurol Neurosurg, 1991, vol. 93(4), рр. 293-307. doi: 10.1016/03038467(91)90094-6. PMID: 1665763

7. Akimotо J. Photodynamic therapy for malignant brain tumors, Neurol. Med. Chir, 2016, vol. 56 (4), рр. 151-157. doi: 10.2176/nmc.ra.2015-0296

8. Ostrom Q.T. et al. CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2009-2013, Neuro-Oncology, 2016. vol. 18 (5), рр. 1-75. doi: 10.1093/neuonc/now207

9. Quirk B.J. et al. Photodynamic therapy (PDT) in malignant brain tumors – Where do we stand? Photodiagnosis Photodyn. Ther, 2015, vol. 12(3), рр. 530-544. doi: 10.1016/j.pdpdt.2015.04.009

10. Castano A.P., et al. Mechanisms in photodynamic therapy: Part one – Photosensitizers, photochemistry and cellular localization, Photodiagnosis Photodyn. Ther, 2004. vol. 1 (4), рр.279-293. doi: 10.1016/s1572-1000(05)00007-4

11. Josefsen L.B. and Boyle R.W. Photodynamic therapy: Novel third-generation photosensitizers one step closer? Br. J. Pharmacol, 2008, vol. 154(1), рр. 1-3.

12. doi: 10.1038/bjp.2008.98

13. Dolmans D.E., et al. Photodynamic therapy for cancer, Nature, 2003. vol. 3, рр. 380-387. doi: 10.1038/nrc1071

14. Allison R.R. and Sibata C.H. Oncologic photodynamic therapy photosensitizers: A clinical review, Photodiagnosis Photodyn. Ther, 2010, vol. 7(2), рр. 61-75. doi: 10.1016/j.pdpdt.2010.02.001

15. Stepp H. and Stummer W. 5-ALA in the management of malignant glioma, Lasers Surg. Med, 2018, vol. 50(5), рр. 399-419. doi: 10.1002/lsm.22933

16. Bechet D., et al. Photodynamic therapy of malignant brain tumours: A complementary approach to conventional therapies, Cancer Treat. Rev, 2014, vol. 40(2), рр. 229-241. doi: 10.1016/j.ctrv.2012.07.004

17. Abramova O.B., Drozhzhina V.V., Churikova T.P., et al. Photodynamic therapy of experimental tumors of various morphological types with liposomal borated chlorin e6, Biomedical Photonics, 2021, vol. 10(3), рр. 12-22. (In Russian)

18. Hiramatsu R. et al. Application of a novel boronated porphyrin (H₂OCP) as a dual sensitizer for both PDT and BNCT, Lasers Surg. Med, 2011, vol. 43(1), рр. 52-58. doi: 10.1002/lsm.21026

19. Bechet D. Neuropilin-1 targeting photosensitization-induced early stages of thrombosis via tissue factor release, Pharm Res, 2010, vol. 27(3), рр.468-79. doi: 10.1007/s11095-009-0035-8

20. Rajora A. K., et al. Recent Advances and Impact of Chemotherapeutic and Antiangiogenic Nanoformulations for Combination Cancer Therapy, Pharmaceutics, 2020, vol. 12, р. 592. doi: 10.3390/pharmaceutics12060592

21. Yudintceva N.M., Mikhrina, A.L., Nechaeva, A.S., Shevtsov, M.A. Assessment of heat-shock protein Hsp70 colocalization with markers of tumor stem-like cells, Cell and Tissue Biology, 2022, vol. 16(5), рр. 459-464. doi:10.1134/S1990519X22050108

22. Tagaeva R.B., Bobkov D.E., Nechaeva A.S., et al. Membranebound heat shock protein mHsp70 as a marker of malignant brain tumors, Russian Neurosurgical Journal named after Professor A. L. Polenov, 2023, vol. 15(2), рр. 98-101. (In Russian)

23. Deng C.X. Targeted drug delivery across the blood-brain barrier using ultrasound technique, Ther. Deliv, 2010, vol. 1(6), рр. 819-848. doi: 10.4155/tde.10.66

24. Banks W.A. From blood-brain barrier to blood-brain interface: New opportunities for CNS drug delivery, Nat. Rev. Drug Discov, 2016, vol. 15, рр. 275-292. doi: 10.1038/nrd.2015.21

25. Fecci P.E., et al. Viruses in the treatment of brain tumors, Neuroimaging Clin. of North America, 2002, vol. 12(4), рр. 553-570. doi: 10.1016/s1052-5149(02)00028-x

26. Patel M. M. and Patel B. M. Crossing the Blood-Brain Barrier: Recent Advances in Drug Delivery to the Brain, CNS Drugs, 2017, vol. 31, рр. 109-133. doi: 10.1007/s40263-016-0405-9

27. Roet M., et al. Progress in euromodulation of the brain: A role for magnetic nanoparticles? Prog. Neurobiol, 2019, vol. 177, рр. 1-14. doi: 10.1016/j.pneurobio.2019.03.002

28. Baek S.K., et al. Photothermal treatment of glioma; an in vitro study of macrophage-mediated delivery of gold nanoshells, Journal of Neuro-Oncology, 2011, vol. 104(2), 439-448. doi:10.1007/s11060-010-0511-3

29. Male D., et al. Gold Nanoparticles for Imaging and Drug Transport to the CNS, Int. Rev. Neurobiol, 2016, vol. 130, рр. 155-198. doi: 10.1016/bs.irn.2016.05.003

30. Pass H. I. Photodynamic therapy in oncology: Mechanisms and clinical use, J. Natl. Cancer Inst, 1993, vol. 85, рр. 443-456. doi.org/10.1093/jnci/85.6.443

31. Lukšienë, Ž. Photodynamic therapy: Mechanism of action and ways to improve the efficiency of treatment, Medicina, 2003, vol. 39, рр. 1137-1150.

32. Vrouenraets M.B., et al. Basic principles, applications in oncology and improved selectivity of photodynamic therapy, Anticancer Res, 2003, vol. 23, рр. 505-522.

33. Allison R.R. Photodynamic therapy: Oncologic horizons, Future Oncology, 2014, vol. 10(1), рр. 123-142. doi: 10.2217/fon.13.176

34. Scheffer G.L., et al. Specific detection of multidrug resistance proteins MRP1, MRP2, MRP3, MRP5 and MDR3 P-glycoprotein with panel of monoclonal antibodies, Cancer Res, 2000, Vol. 60, рр. 5269-5277.

35. Schipmann S., et al. Combination of ALA-induced fluorescence-guided resection and intraoperative open photodynamic therapy for recurrent glioblastoma: case series on a promising dual strategy for local tumor control, J. Neurosurg, 2020, vol. 134, рр. 426-436.

36. Akimoto J., et al. First autopsy analysis of the efficacy of intraoperative additional photodynamic therapy for patients with glioblastoma, Brain Tumor Pathol, 2019, vol. 36, рр. 144-151.

37. Vermandel M., et al. Standardized intraoperative 5-ALA photodynamic therapy for newly diagnosed glioblastoma patients: a preliminary analysis of the INDYGO clinical trial, J. Neurooncol, 2021, vol. 152, рр. 501-514.

38. Ricchelli F. Photophysical properties of porphyrins in biological membranes, J. Photochem. Photobiol. B Biol, 1995, vol. 29, рр. 109-118. doi.org/10.1016/1011-1344(95)07155-U

39. Castano A.P., et al. Mechanisms in photodynamic therapy: Part three – Photosensitizer pharma-cokinetics, biodistribution, tumor localization and modes of tumor destruction, Photodiagnosis. Photodyn. Ther, 2005, vol. 2, рр. 91-106. doi.org/10.1016/S1572-1000(05)00060-8

40. Bartusik-Aebisher D., et al. The Use of Photodynamic Therapy in the Treatment of Brain Tumors – A Review of the Literature, Molecules, 2022, vol. 27, рр. 6847. doi.org/10.3390/molecules27206847

41. Efendiev K., Alekseeva P., Shiryaev A., at al. Near-infrared phototheranostics of tumors with protoporphyrin IX and chlorin e6 photosensitizers, Photodiagnosis and Photodynamic Therapy, 2023, vol. 42, р. 103566. doi: 10.1016/j.pdpdt.2023.103566

42. Tserkovsky D.A., Maslakov E.A., Bagrintsev D.A. et al. The role of photodynamic therapy in the treatment of primary, recurrent and metastatic malignant brain tumors, Biomedical Photonics, 2018, vol. 7(2), рр. 37-49 (In Russian)

43. Stummer W. et al. Technical principles of microsurgical resection of malignant glioma tissue controlled by protoporphyrin-IX-fluorescence, Acta Neurochir, 1998. vol. 140, рр. 995-1000. doi: 10.1007/s007010050206

44. Stummer W. et al. Long-sustaining response in a patient with non-resectable, distant recurrence of glioblastoma multiforme treated by interstitial photodynamic therapy using 5-ALA: Case report, J. Neurooncol, 2008, vol. 87. рр. 103-109. doi.org/10.1007/s11060-007-9497-x

45. Schwartz C. et al. Interstitial photodynamic therapy for de-novo multiforme glioblastoma. WHO IV, Neurooncology, 2015, vol. 17, рр. 214-220. doi.org/10.1093/neuonc/nov235.25

46. Rynda A.Yu., Olyushin V.E., Rostovtsev D.M., et al. The use of intraoperative photodynamic therapy in the structure of complex treatment of malignant gliomas, Journal “Problems of Neurosurgery” named after N.N. Burdenko, 2023, vol. 87(1), рр. 25-34 (In Russian)

47. Stummer W., Pitchimeier U., Meinel T., Wiestler O.D., Zanella F., Reulen H.J. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomized controlled multicentre phase III trial, Lancet Oncol, 2006, vol.7, рр. 392-401.

48. Eljamel, S. Photodynamic applications in brain tumors: A comprehensive review of the literature, Photodiagnosis Photodyn. Ther, 2010, vol.7, рр. 76-85. doi.org/10.1016/j.pdpdt.2010.02.002

49. Stylli S.S., Kaye A.H., MacGregor L., Howes M., Rajendra P. Photodynamic therapy of high-grade glioma – long term survival, J. Clin. Neurosci, 2005, vol.12(4), рр. 389-398.

50. Kostron H., Fiegele T., Akatuna E. Combination of «FOSCAN» mediated fluorescence guided resection and photodynamic treatment as new therapeutic concept for malignant brain tumors // Med. Laser Applic. – 2006. – Vol. 21. – P. 285-290.

51. Muller P., Wilson B. Photodynamic therapy of brain tumors--a work in progress, Lasers Surg Med, 2006, vol. 38(5), рр. 384-389

52. MuragakiY., Akimoto J., Maruyama T., et al. Phase II clinical studyon intraoperative photodynamic therapy with talaporfin sodium and semiconductor laser in patients with malignant brain tumors, J. Neurosurg, 2013, vol. 119(4), рр. 845-852.

53. Akimoto, J., et al. First autopsy analysis of the efficacy of intraoperative additional photodynamic therapy for patients with glioblastoma, Brain Tumor Pathol, 2019, vol. 36, рр. 144-151.

54. Shimizu K., Nitta M., Komori T. et al. Intraoperative Photodynamic Diagnosis Using Talaporfin Sodium Simultaneously Applied for Photodynamic Therapy against Malignant Glioma: A Prospective Clinical Study, Frontiers in Neurology, 2018, vol. 9, рр. 1-9. doi.org/10.3389/fneur.2018.00024

55. Nitta M., Muragaki Y., Maruyama T., et al. T. Role of photodynamic therapy using talaporfin sodium and a semiconductor laser in patients with newly diagnosed glioblastoma, J Neurosurg, 2018, vol. 7, рр. 1-8. doi.org/10.3171/2018.7.JNS18422.

56. Tatsuya K., Nitta М., Kazuhide S., et al. Therapeutic Options for Recurrent Glioblastoma-Efficacy of Talaporfin Sodium Mediated Photodynamic Therapy, Pharmaceutics, 2022, vol. 14(2), р. 353. doi.org/10.3390/pharmaceutics14020353.

57. Teng C.W., Amirshaghaghi A., Cho S.S., et al. Combined fluorescence-guided surgery and photodynamic therapy for glioblastoma multiforme using cyanine and chlorin nanocluster, J Neurooncol, 2020, vol.149, рр. 243-252. doi.org/10.1007/s11060-020-03618-1

58. Maruyama T., Muragaki Y., Nitta M., et al. Photodynamic therapy for malignant brain tumors, Japanese J Neurosurg, 2016, vol.25, р. 895.

59. Kozlikina E.I. et al. The Combined Use of 5-ALA and Chlorin e6 Photosensitizers for Fluorescence-Guided Resection and Photodynamic Therapy under Neurophysiological Control for Recurrent Glioblastoma in the Functional Motor Area after Ineffective Use of 5-ALA: Preliminary Results, Bioengineering, 2022, vol.9, р.104. doi.org/10.3390/bioengineering9030104

60. Hamid S.A., Zimmermann W., et al. In vitro study for photodynamic therapy using Fotolon in glioma treatment. Proc. SPIE, 2015, vol. 9542, р. 13. doi.org/10.1117/12.2183884

61. Akimoto J., Fukami S., Ichikawa M. et al Intraoperative Photodiagnosis for Malignant Glioma Using Photosensitizer Talaporfin Sodium, Frontiers in Surgery, 2019, vol. 21, рр. 6-12. doi.org/10.3389/fsurg.2019.00012

62. Stummer W., Pichlmeier U., Meinel T. Fluorescence-guided surgery with 5 –aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial, Lancet Oncol, 2006, vol. 7, рр. 392-401.

63. Cramer S.W., Chen C.C. Photodynamic Therapy for the Treatment of Glioblastoma, Front. Surg, 2020, vol.6, р. 81. doi.org/10.3389/fsurg.2019.00081.

64. Schipmann S., et al. Combination of ALA-induced fluorescence-guided resection and intraoperative open photodynamic therapy for recurrent glioblastoma: case series on a promising dual strategy for local tumor control, J. Neurosurg, 2020, vol. 134, рр. 426-436.

65. Stummer W., et al. Long-sustaining response in a patient with non-resectable, distant recurrence of glioblastoma multiforme treated by interstitial photodynamic therapy using 5-ALA: Case report, J. Neurooncol, 2008, vol. 87, рр. 103-109. doi.org/10.1007/s11060-007-9497-x

66. Schwartz C. et al. Interstitial photodynamic therapy for de-novo multiforme glioblastoma WHO IV, Neurooncology, 2015, vol.17, рр. 214-220. doi.org/10.1093/neuonc/nov235.25

67. Mahmoudi K,. et al. 5-Aminolevulinic Acid Photodynamic Therapy for the Treatment of High-Grade Gliomas, J. Neurooncol, 2019, vol. 141, рр. 595-607. doi.org/10.1007/s11060-019-03103-4

68. Chen R., Aghi M.K. Atypical meningiomas, Handb Clin Neurol, 2020, vol. 170, рр. 233-244. doi.org/10.1016/B978-0-12-822198-3.00043-4

69. Kiesel B., et al. G. 5-ALA in suspected low-grade gliomas: Current Role, limitations, and new approaches // Front. Oncol. – 2021. – Vol. 11. – P.699301. doi.org/10.3389/fonc.2021.699301

70. Reshetov I.V., Korenev S.V., Romanko Yu.S. Forms of cell death and targets during photodynamic therapy, Siberian Oncology Journal, 2022, vol. 21(5), рр. 149-154. (In Russian)

71. Kukanov K.K., Vorobyova O.M., Zabrodskaya Yu.M. et al. Intracranial meningiomas: clinical, intrascopic and pathomorphological causes of recurrence, taking into account modern treatment methods (literature review), Siberian Oncology Journal, 2022, vol. 21 (4), рр. 110-123. (In Russian)

72. Rynda A.Yu., Rostovtsev D.M., Olyushin V.E., et al. Therapeutic pathomorphosis in malignant glioma tissues after photodynamic therapy with chlorin e6 (report of two clinical cases), Biomedical Photonics, 2020, vol. 9(2), рр. 45-54. (In Russian)

73. Rynda A.Yu., Rostovtsev D.M., Olyushin V.E. Fluorescence-guided resection of astrocytic brain tumors – a review of the literature, Russian Neurosurgical Journal named after Professor A.L. Polenova, 2018, vol. 10(1), рр. 97-110. (In Russian)

74. Rynda A.Yu., Olyushin V.E., Rostovtsev D.M., et al. Fluorescence diagnostics with chlorin e6 in the surgery of low-grade gliomas, Biomedical Photonics, 2021, vol. 10(4), рр. 35-43. (In Russian)

75. Rynda A.Yu., Olyushin V.E., Rostovtsev D.M., et al. Results of using intraoperative fluorescent control with chlorin E6 during resection of glial brain tumors, Journal of Neurosurgery named after N.N. Burdenko, 2021, vol. 85(4), рр.20-28. (In Russian)

76. Rynda A.Yu., Olyushin V.E., Rostovtsev D.M., et al. Comparative analysis of fluorescent navigation in surgery of malignant gliomas using 5-ALA and chlorin E6, Surgery. Journal named after N.I. Pirogov, 2022, vol. 1, рр. 5-14. (In Russian)

77. Rynda A.Yu., Olyushin V.E., Rostovtsev D.M., et al. Possibilities of intraoperative fluorescent bioimaging of nerves in neurosurgical practice, Russian Neurosurgical Journal named after. prof. A. L. Polenova, 2023, vol. 15(1), р. 12. (In Russian)