Skip to main content

Advertisement

SpringerLink
Log in

Using X-rays in photodynamic therapy: an overview

  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

Abstract

Photodynamic therapy is a therapeutic option to treat cancer and other diseases. PDT is used every day in dermatology, and recent developments in the treatment of glioblastoma, mesothelioma or prostate have demonstrated the efficacy of this modality. In order to improve the efficacy of PDT, different strategies are under development, such as the use of targeted PS or nanoparticles to improve selectivity and the design of light devices to better monitor the light dose. Due to the low penetration of light into tissue, another way to improve the efficacy of PDT to treat deep tumors is the use of upconversion NPs or bi-photon absorption compounds. These compounds can be excited in the red part of the spectrum. A relatively new approach, which we will call PDTX, is the use of X-rays instead of UV-visible light for deeper penetration into tissue. The principle of this technique will be described, and the state-of-art literature concerning this modality will be discussed. First, we will focus on various photosensitizers that have been used in combination with X-ray irradiation. To improve the efficacy of this modality, nanoparticles have been designed that allow the conversion of high-energy ionizing radiation into UV-visible light; these are potential candidates for the PDTX approach. They will be discussed at the end of this review.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. X. Wen, Y. Li and M. R. Hamblin, Photodynamic therapy in dermatology beyond non-melanoma cancer: An update, Photodiagn. Photodyn. Ther., 2017, 19, 140–152.

    Article  CAS  Google Scholar 

  2. J. Akimoto, Photodynamic Therapy for Malignant Brain Tumors, Neurol. Med. Chir., 2016, 56, 151–157.

    Article  Google Scholar 

  3. J. S. Friedberg, Photodynamic therapy for malignant pleural mesothelioma, J. Natl. Compr. Cancer Network, 2012, 10, S75–S79.

    Article  Google Scholar 

  4. S. S. Taneja, Re: padeliporfin vascular-targeted photo-dynamic therapy versus active surveillance in men with low-risk prostate cancer (CLIN1001 PCM301): An open-label, phase 3, randomised controlled trial editorial comment, J. Urol., 2017, 198, 255–256.

    Article  PubMed  Google Scholar 

  5. H. Azaïs, C. Frochot, A. Grabarz, S. K. Bach, L. Colombeau, N. Delhem, S. Mordon and P. Collinet, Specific folic-acid targeted photosensitizer. The first step toward intraperitoneal photodynamic therapy for epi-thelial ovarian cancer, Gynecol. Obstet. Fertil. Senol., 2017, 45, 190–196.

    PubMed  Google Scholar 

  6. E. E. Kamarulzaman, R. Vanderesse, A. M. Gazzali, M. Barberi-Heyob, C. Boura, C. Frochot, O. Shawkataly, A. Aubry and H. A. Wahab, Molecular modelling, synthesis and biological evaluation of peptide inhibitors as anti-angiogenic agent targeting neuropilin-1 for anti-cancer application, J. Biomol. Struct. Dyn., 2017, 35, 26–45.

    Article  CAS  PubMed  Google Scholar 

  7. E. Thomas, L. Colombeau, M. Gries, T. Peterlini, C. Mathieu, N. Thomas, C. Boura, C. Frochot, R. Vanderesse, F. Lux, M. Barberi-Heyob and O. Tillement, Ultrasmall AGulX theranostic nanoparticles for vascular-targeted interstitial photodynamic therapy of glioblas-toma, Int. J. Nanomed., 2017, 12, 7075–7088.

    Article  CAS  Google Scholar 

  8. S. Mordon, C. Cochrane, J. B. Tylcz, N. Betrouni, L. Mortier and V. Koncar, Light emitting fabric techno-logies for photodynamic therapy, Photodiagn. Photodyn. Ther., 2015, 12, 1–8.

    Article  CAS  Google Scholar 

  9. L. Colombeau, S. Acherar, F. Baros, P. Arnoux, A. M. Gazzali, K. Zaghdoudi, M. Toussaint, R. Vanderesse and C. Frochot, in Light-Responsive Nanostructured Systems for Applications in Nanomedicine, ed. S. Sortino, 2016, vol. 370, pp. 113–134.

    Article  CAS  Google Scholar 

  10. W. Fan, P. Huang and X. Chen, Overcoming the Achilles' heel of photodynamic therapy, Chem. Soc. Rev., 2016, 45, 6488–6519.

    Article  CAS  PubMed  Google Scholar 

  11. D. K. Chatterjee, L. S. Fong and Y. Zhang, Nanoparticles in photodynamic therapy: An emerging paradigm, Adv. Drug Delivery Rev., 2008, 60, 1627–1637.

    Article  CAS  Google Scholar 

  12. W. Chen, Nanoparticle fluorescence based technology for biological applications, J. Nanosci. Nanotechnol., 2008, 8, 1019–1051.

    Article  CAS  PubMed  Google Scholar 

  13. J. A. Coulter, W. B. Hyland, J. Nicol and F. J. Currell, Radiosensitising nanoparticles as novel cancer thera-peutics-pipe dream or realistic prospect?, Clin. Oncol., 2013, 25, 593–603.

    Article  CAS  Google Scholar 

  14. J. Hu, Y. Tang, A. H. Elmenoufy, H. Xu, Z. Cheng and X. Yang, Nanocomposite-based photodynamic therapy strategies for deep tumor treatment, Small, 2015, 11, 5860–5887.

    Article  CAS  PubMed  Google Scholar 

  15. A. Kamkaew, F. Chen, Y. Zhan, R. L. Majewski and W. Cai, Scintillating nanoparticles as energy mediators for enhanced photodynamic therapy, ACS Nano, 2016, 10, 3918–3935.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. P. Retif, S. Pinel, M. Toussaint, C. Frochot, R. Chouikrat, T. Bastogne and M. Barberi-Heyob, Nanoparticles for radi-ation therapy enhancement: the key parameters, Theranostics, 2015, 5, 1030–1044.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. D. R. Cooper, D. Bekah and J. L. Nadeau, Gold nano-particles and their alternatives for radiation therapy enhancement, Front. Chem., 2014, 2, 86.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. W. Ngwa, R. Kumar, S. Sridhar, H. Korideck, P. Zygmanski, R. A. Cormack, R. Berbeco and G. M. Makrigiorgos, Targeted radiotherapy with gold nanoparticles: current status and future perspectives, Nanomedicine, 2014, 9, 1063–1082.

    Article  CAS  PubMed  Google Scholar 

  19. P. Juzenas, W. Chen, Y. P. Sun, M. A. Coelho, R. Generalov, N. Generalova and I. L. Christensen, Quantum dots and nanoparticles for photodynamic and radiation therapies of cancer, Adv. Drug Delivery Rev., 2008, 60, 1600–1614.

    Article  CAS  Google Scholar 

  20. K. Benstead and J. V. Moore, The effect of combined modality treatment with ionising radiation and TPPS-mediated photodynamic therapy on murine tail skin, Br.J. Cancer, 1990, 62, 48–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. A. Colasanti, A. Kisslinger, M. Quarto and P. Riccio, Combined effects of radiotherapy and photodynamic therapy on an in vitro human prostate model, Acta Biochim. Pol., 2004, 51, 1039–1046.

    CAS  PubMed  Google Scholar 

  22. J. Liu, Y. Yang, W. Zhu, X. Yi, Z. Dong, X. Xu, M. Chen, K. Yang, G. Lu, L. Jiang and Z. Liu, Nanoscale metal-organic frameworks for combined photodynamic & radi-ation therapy in cancer treatment, Biomaterials, 2016, 97, 1–9.

    Article  CAS  PubMed  Google Scholar 

  23. A. R. Montazerabadi, A. Sazgarnia, M. H. Bahreyni-Toosi, A. Ahmadi and A. Aledavood, The effects of combined treatment with ionizing radiation and indo-cyanine green-mediated photodynamic therapy on breast cancer cells, J. Photochem. Photobiol., B, 2012, 109, 42–49.

    Article  CAS  Google Scholar 

  24. B. W. Pogue, J. A. O'Hara, E. Demidenko, C. M. Wilmot, I. A. Goodwin, B. Chen, H. M. Swartz and T. Hasan, Photodynamic therapy with verteporfin in the radiation-induced fibrosarcoma-1 tumor causes enhanced radiation sensitivity, Cancer Res., 2003, 63, 1025–1033.

    CAS  PubMed  Google Scholar 

  25. J. G. Post, J. A. te Poele, Y. Oussoren and F. A. Stewart, The influence of intravesical photodynamic therapy on sub-sequent bladder irradiation tolerance, Radiother. Oncol., 1995, 37, 124–130.

    Article  CAS  PubMed  Google Scholar 

  26. C. Prinsze, L. C. Penning, T. M. Dubbelman and J. VanSteveninck, Interaction of photodynamic treatment and either hyperthermia or ionizing radiation and of ionizing radiation and hyperthermia with respect to cell killing of L929 fibroblasts, Chinese hamster ovary cells, and T24 human bladder carcinoma cells, Cancer Res., 1992, 52, 117–120.

    CAS  PubMed  Google Scholar 

  27. J. Qiu, Q. Xiao, X. Zheng, L. Zhang, H. Xing, D. Ni, Y. Liu, S. Zhang, Q. Ren, Y. Hua, K. Zhao and W. Bu, Single W18O49 nanowires: A multifunctional nanoplatform for computed tomography imaging and photothermal/photo-dynamic/radiation synergistic cancer therapy, Nano Res., 2015, 8, 3580–3590.

    Article  CAS  Google Scholar 

  28. A. Sazgarnia, A. R. Montazerabadi, M. H. Bahreyni-Toosi and A. Ahmadi, Photosensitizing and radiosensitizing effects of mitoxantrone: combined chemo-, photo-, and radiotherapy of DFW human melanoma cells, Lasers Med. Sci., 2013, 28, 1533–1539.

    Article  PubMed  Google Scholar 

  29. J. Shi, Z. Chen, L. Wang, B. Wang, L. Xu, L. Hou and Z. Zhang, A tumor-specific cleavable nanosystem of PEG-modified C60@Au hybrid aggregates for radio frequency-controlled release, hyperthermia, photodynamic therapy and X-ray imaging, Acta Biomater., 2016, 29, 282–297.

    Article  CAS  PubMed  Google Scholar 

  30. J. Winther, J. Overgaard and N. Ehlers, The effect of photodynamic therapy alone and in combination with misonidazole or X-rays for management of a retinoblas-toma-like tumour, Photochem. Photobiol., 1988, 47, 419–423.

    Article  CAS  PubMed  Google Scholar 

  31. J. Xu, J. Gao and Q. Wei, Combination of photodynamic therapy with radiotherapy for cancer treatment, J. Nanomater., 2016, 2016, 7.

    Google Scholar 

  32. X. Yu, X. Tang, J. He, X. Yi, G. Xu, L. Tian, R. Zhou, C. Zhang and K. Yang, Polydopamine nanoparticle as a multifunctional nanocarrier for combined radiophotody-namic therapy of cancer, Part. Part. Syst. Charact., 2017, 34, 1600296.

    Article  CAS  Google Scholar 

  33. P. Hambsch, Y. P. Istomin, D. A. Tzerkovsky, I. Patties, J. Neuhaus, R. D. Kortmann, S. Schastak and A. Glasow, Efficient cell death induction in human glioblastoma cells by photodynamic treatment with Tetrahydroporphyrin-Tetratosylat (THPTS) and ionizing irradiation, Oncotarget., 2017, 8, 72411–72423.

    Article  PubMed  PubMed Central  Google Scholar 

  34. M. Zhang, Z. Cui, R. Song, B. Lv, Z. Tang, X. Meng, X. Chen, X. Zheng, J. Zhang, Z. Yao and W. Bu, SnWO4- based nanohybrids with full energy transfer for largely enhanced photodynamic therapy and radiotherapy, Biomaterials, 2017, 155, 135–144.

    Article  PubMed  CAS  Google Scholar 

  35. W. Fan, B. Shen, W. Bu, F. Chen, Q. He, K. Zhao, S. Zhang, L. Zhou, W. Peng, Q. Xiao, D. Ni, J. Liu and J. Shi, A smart upconversion-based mesoporous silica nanotheranostic system for synergetic chemo-/radio-/ photodynamic therapy and simultaneous MR/UCL imaging, Biomaterials, 2014, 35, 8992–9002.

    Article  CAS  PubMed  Google Scholar 

  36. D. Balland, R. Guillard and J. C. Andre, Industrial photo-chemistry.6. Light-distribution in photopolymerizable composite-materials and heterogeneities observed in light-source used for the photoreaction, Polym. Photochem., 1984, 4, 111–133.

    Article  CAS  Google Scholar 

  37. C. Braun and J. C. Andre, Industrial photochemistry.7. Light-distribution in a diffusing medium of titanium-dioxide in water, J. Photochem., 1985, 28, 13–29.

    Article  CAS  Google Scholar 

  38. P. Boissard, French thesis, Université de Toulouse III Paul Sabatier, 2012.

    Google Scholar 

  39. C. M. Yang, French thesis, Paris XI, 2014.

    Google Scholar 

  40. N. Y. Morgan, G. Kramer-Marek, P. D. Smith, K. Camphausen and J. Capala, Nanoscintillator conju-gates as photodynamic therapy-based radiosensitizers: calculation of required physical parameters, Radiat. Res., 2009, 171, 236–244.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. A. L. Bulin, A. Vasil'ev, A. Belsky, D. Amans, G. Ledoux and C. Dujardin, Modelling energy deposition in nanos-cintillators to predict the efficiency of the X-ray-induced photodynamic effect, Nanoscale, 2015, 7, 5744–5751.

    Article  CAS  PubMed  Google Scholar 

  42. J. C. Finlay, PDT driven by energy-converting materials: a theoretical analysis, in SPIE BiOS, 2009, vol. 7164, p. 7.

    Google Scholar 

  43. W. Hausmann, Die sensibilisierende wirkung des hemato-porphyrin, Biochem. Z., 1910, 30, 276–316.

    Google Scholar 

  44. M. R. Hamblin and P. Mróz, in Engineering in Medicine & Biology series, Artech House series, 2008.

    Google Scholar 

  45. R. Bonnet, in Advanced chemistry texts, Gordon and Breach Science Publishers, 2000, pp. 1029–3654.

    Google Scholar 

  46. R. L. Lipson and E. J. Baldes, The photodynamic pro-perties of a particular hematoporphyrin derivative, Arch. Dermatol., 1960, 82, 508–516.

    Article  CAS  PubMed  Google Scholar 

  47. M. Schaffer, B. Ertl-Wagner, P. M. Schaffer, U. Kulka, A. Hofstetter, E. Duhmke and G. Jori, Porphyrins as radio-sensitizing agents for solid neoplasms, Curr. Pharm. Des., 2003, 9, 2024–2035.

    Article  CAS  PubMed  Google Scholar 

  48. S. Schwartz, K. Absolon and H. Vermund, Some relation-ships of porphyrins, X-ray, and tumors, Univ. Minn. Med. Bull., 1955, 27, 1–37.

    Google Scholar 

  49. L. Cohen and S. Schwartz, Modification of radiosensitivity by porphyrins. II. Transplanted rhabdomyosarcoma in mice, Cancer Res., 1966, 26, 1769–1773.

    CAS  PubMed  Google Scholar 

  50. J. Moan and E. O. Pettersen, X-irradiation of human cells in culture in the presence of hematoporphyrin, Int. J. Radiat. Biol., 1981, 40, 107–109.

    Article  CAS  Google Scholar 

  51. G. Kavarnos, R. Nath and P. Bongiorni, Visible-light and X irradiations of chinese hamster lung cells treated with hematoporphyrin derivative, Radiat. Res., 1994, 137, 196–201.

    Article  CAS  PubMed  Google Scholar 

  52. F. Bistolfi, Red radioluminescence and radiochemilumi-nescence: premises for a photodynamic tumour therapy with X-rays and haematoporphyrin derivatives. A working hypothesis, Panminerva Med., 2000, 42, 69–75.

    CAS  PubMed  Google Scholar 

  53. C. Austerlitz, V. L. Bormann de Souza, D. M. T. Campos, C. Kurachi, V. Bagnato and C. Sibata, Enhanced response of the Fricke solution doped with hematoporphyrin under X-rays irradiation, Braz. Arch. Biol. Technol., 2008, 51, 271–279.

    Article  CAS  Google Scholar 

  54. C. J. Byrne, L. V. Marshallsay and A. D. Ward, The compo-sition of Photofrin II, J. Photochem. Photobiol., B, 1990, 6, 13–27.

    Article  CAS  Google Scholar 

  55. T. J. Dougherty, C. J. Gomer, B. W. Henderson, G. Jori, D. Kessel, M. Korbelik, J. Moan and Q. Peng, Photodynamic therapy, J. Natl. Cancer Inst., 1998, 90, 889–905.

    Article  CAS  PubMed  Google Scholar 

  56. L. W. Ma, V. Iani and J. Moan, Combination therapy: photochemotherapy; electric current; and ionizing radi-ation. Different combinations studied in a WiDr human colon adenocarcinoma cell line, J. Photochem. Photobiol., B, 1993, 21, 149–154.

    Article  CAS  Google Scholar 

  57. M. Schaffer, P. M. Schaffer, L. Corti, G. Sotti, A. Hofstetter, G. Jori and E. Duhmke, Photofrin II as an efficient radio-sensitizing agent in an experimental tumor, Onkologie, 2001, 24, 482–485.

    CAS  PubMed  Google Scholar 

  58. M. Schaffer, P. M. Schaffer, M. Vogesser, B. Ertl-Wagner, J. Rauch, R. Oberneder, G. Jori, A. Hofstetter and E. Duhmke, Application of Photofrin II as a specific radio-sensitising agent in patients with bladder cancer-a report of two cases, Photochem. Photobiol. Sci., 2002, 1, 686–689.

    Article  CAS  PubMed  Google Scholar 

  59. M. Schaffer, P. M. Schaffer, L. Corti, M. Gardiman, G. Sotti, A. Hofstetter, G. Jori and E. Duhmke, Photofrin as a specific radiosensitizing agent for tumors: studies in comparison to other porphyrins, in an experimental in vivo model, J. Photochem. Photobiol., B, 2002, 66, 157–164.

    Article  CAS  Google Scholar 

  60. U. Kulka, M. Schaffer, A. Siefert, P. M. Schaffer, A. Olsner, K. Kasseb, A. Hofstetter, E. Duhmke and G. Jori, Photofrin as a radiosensitizer in an in vitro cell survival assay, Biochem. Biophys. Res. Commun., 2003, 311, 98–103.

    Article  CAS  PubMed  Google Scholar 

  61. M. Schaffer, B. Ertl-Wagner, P. M. Schaffer, U. Kulka, G. Jori, E. Duhmke and A. Hofstetter, The Application of Photofrin II as a sensitizing agent for ionizing radiation: A new approach in tumor therapy?, Curr. Med. Chem., 2005, 12, 1209–1215.

    Article  CAS  PubMed  Google Scholar 

  62. M. Schaffer, P. M. Schaffer, A. Hofstetter, E. Duhmke and G. Jori, On the double role of Photofrin as a photo-and a radio-sensitising agent: A possible new combination therapy for tumours, Photochem. Photobiol. Sci., 2002, 1, 438–439.

    Article  CAS  PubMed  Google Scholar 

  63. A. B. Ormond and H. S. Freeman, Dye Sensitizers for Photodynamic Therapy, Materials, 2013, 6, 817–840.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. K. Berg, Z. Luksiene, J. H. Moan and L. W. Ma, Combined treatment of ionizing-radiation and photosensitization by 5-aminolevulinic acid-indiced protoporphyrin-IX, Radiat. Res., 1995, 142, 340–346.

    Article  CAS  PubMed  Google Scholar 

  65. J. Takahashi and M. Misawa, Characterization of reactive oxygen species generated by protoporphyrin IX under X-ray irradiation, Radiat. Phys. Chem., 2009, 78, 889–898.

    Article  CAS  Google Scholar 

  66. J. Yamamoto, S. I. Ogura, T. Tanaka, T. Kitagawa, Y. Nakano, T. Saito, M. Takahashi, D. Akiba and S. Nishizawa, Radiosensitizing effect of 5-aminolevulinic acid-induced protoporphyrin IX in glioma cells in vitro, Oncol. Rep., 2012, 27, 1748–1752.

    CAS  PubMed  Google Scholar 

  67. J. Takahashi, M. Misawa, M. Murakami, T. Mori, K. Nomura and H. Iwahashi, 5-Aminolevulinic acid enhances cancer radiotherapy in a mouse tumor model, SpringerPlus, 2013, 2, 602.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  68. J. Takahashi, M. Misawa and H. Iwahashi, Gene expression profiling can predict the fate of HeLa cells exposed to X-ray irradiation with or without protopor-phyrin accumulation, Genomics Data, 2015, 5, 192–194.

    Article  PubMed  PubMed Central  Google Scholar 

  69. J. Takahashi, M. Misawa and H. Iwahashi, Transcriptome analysis of porphyrin-accumulated and X-ray-irradiated cell cultures under limited proliferation and non-lethal conditions, Microarrays, 2015, 4, 25–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. J. Takahashi, M. Misawa and H. Iwahashi, Combined treatment with X-ray irradiation and 5-aminolevulinic acid elicits better transcriptomic response of cell cycle-related factors than X-ray irradiation alone, Int. J. Radiat. Biol., 2016, 92, 774–789.

    Article  CAS  PubMed  Google Scholar 

  71. R. M. Acheson, Acridines, John Wiley & Sons, Inc., New York, 1956.

    Google Scholar 

  72. K. Kusuzaki, H. Murata, T. Matsubara, H. Satonaka, T. Wakabayashi, A. Matsumine and A. Uchida, Acridine orange could be an innovative anticancer agent under photon energy, In Vivo, 2007, 21, 205–214.

    CAS  PubMed  Google Scholar 

  73. S. Hashiguchi, K. Kusuzaki, H. Murata, H. Takeshita, M. Hashiba, T. Nishimura, T. Ashihara and Y. Hirasawa, Acridine orange excited by low-dose radiation has a strong cytocidal effect on mouse osteosarcoma, Oncology, 2002, 62, 85–93.

    Article  CAS  PubMed  Google Scholar 

  74. K. Kusuzaki, S. Hosogi, E. Ashihara, T. Matsubara, H. Satonaka, T. Nakamura, A. Matsumine, A. Sudo, A. Uchida, H. Murata, N. Baldini, S. Fais and Y. Marunaka, Translational research of photodynamic therapy with acridine orange which targets cancer acidity, Curr. Pharm. Des., 2012, 18, 1414–1420.

    Article  CAS  PubMed  Google Scholar 

  75. K. Kusuzaki, H. Murata, T. Matsubara, S. Miyazaki, K. Shintani, M. Seto, A. Matsumine, H. Hosoi, T. Sugimoto and A. Uchida, Clinical outcome of a novel photodynamic therapy technique using acridine orange for synovial sarcomas, Photochem. Photobiol., 2005, 81, 705–709.

    Article  CAS  PubMed  Google Scholar 

  76. T. Matsubara, K. Kusuzaki, A. Matsumine, H. Murata, Y. Marunaka, S. Hosogi, A. Uchida and A. Sudo, Photodynamic therapy with acridine orange in musculos-keletal sarcomas, J. Bone Jt. Surg., Br. Vol., 2010, 92, 760–762.

    Article  CAS  Google Scholar 

  77. K. Kusuzaki, H. Murata, T. Matsubara, S. Miyazaki, A. Okamura, M. Seto, A. Matsumine, H. Hosoi, T. Sugimoto and A. Uchida, Clinical trial of photodynamic therapy using acridine orange with/without low dose radi-ation as new limb salvage modality in musculoskeletal sarcomas, Anticancer Res., 2005, 25, 1225–1235.

    CAS  PubMed  Google Scholar 

  78. T. Nakamura, K. Kusuzaki, T. Matsubara, A. Matsumine, H. Murata and A. Uchida, A new limb salvage surgery in cases of high-grade soft tissue sarcoma using photo-dynamic surgery, followed by photo-and radiodynamic therapy with acridine orange, J. Surg. Oncol., 2008, 97, 523–528.

    Article  PubMed  Google Scholar 

  79. T. Matsubara, K. Kusuzaki, A. Matsumine, H. Murata, H. Satonaka, K. Shintani, T. Nakamura, H. Hosoi, T. Iehara, T. Sugimoto and A. Uchida, A new therapeutic modality involving acridine orange excitation by photon energy used during reduction surgery for rhabdomyosar-comas, Oncol. Rep., 2009, 21, 89–94.

    Article  PubMed  CAS  Google Scholar 

  80. T. Matsubara, K. Kusuzaki, A. Matsumine, H. Murata, T. Nakamura, A. Uchida and A. Sudo, Clinical outcomes of minimally invasive surgery using acridine orange for musculoskeletal sarcomas around the forearm, compared with conventional limb salvage surgery after wide resec-tion, J. Surg. Oncol., 2010, 102, 271–275.

    Article  PubMed  Google Scholar 

  81. K. Kusuzaki, T. Takai, H. Yoshimura, K. Inoue, S. Takai and N. Baldini, Clinical trial of radiotherapy after intrave-nous injection of acridine orange for patients with cancer, Anticancer Res., 2018, 38, 481–489.

    CAS  PubMed  Google Scholar 

  82. J. A. O'Hara, E. B. Douple, M. J. Abrams, D. J. Picker, C. M. Giandomenico and J. F. Vollano, Potentiation of radiation-induced cell kill by synthetic matalllo-porphyrins, Int. J. Radiat. Oncol., Biol., Phys., 1989, 16, 1049–1052.

    Article  CAS  Google Scholar 

  83. M. A. Capella and S. Menezes, Synergism between electro-lysis and methylene blue photodynamic action in Escherichia coli, Int. J. Radiat. Biol., 1992, 62, 321–326.

    Article  CAS  PubMed  Google Scholar 

  84. T. Matsubara, K. Kusuzaki, A. Matsumine, H. Satonaka, K. Shintani, T. Nakamura and A. Uchida, Methylene blue in place of acridine orange as a photosensitizer in photo-dynamic therapy of osteosarcoma, In Vivo, 2008, 22, 297–303.

    CAS  PubMed  Google Scholar 

  85. S. Douillard, D. Olivier and T. Patrice, In vitro and in vivo evaluation of Radachlorin (R) sensitizer for photodynamic therapy, Photochem. Photobiol. Sci., 2009, 8, 405–413.

    Article  CAS  PubMed  Google Scholar 

  86. R. Ghoodarzi, V. Changizi, A. R. Montazerabadi and N. Eyvazzadaeh, Assessing of integration of ionizing radi-ation with Radachlorin-PDT on MCF-7 breast cancer cell treatment, Lasers Med. Sci., 2016, 31, 213–219.

    Article  CAS  PubMed  Google Scholar 

  87. A. Kumar and A. Dhawan, Genotoxic and carcinogenic potential of engineered nanoparticles: an update, Arch. Toxicol., 2013, 87, 1883–1900.

    Article  CAS  PubMed  Google Scholar 

  88. P. Boffetta, A. Soutar, J. W. Cherrie, F. Granath, A. Andersen, A. Anttila, M. Blettner, V. Gaborieau, S. J. Klug, S. Langard, D. Luce, F. Merletti, B. Miller, D. Mirabelli, E. Pukkala, H. O. Adami and E. Weiderpass, Mortality among workers employed in the titanium dioxide production industry in Europe, Cancer Causes Control, 2004, 15, 697–706.

    Article  PubMed  Google Scholar 

  89. T. A. Kuhlbusch, C. Asbach, H. Fissan, D. Göhler and M. Stintz, Nanoparticle exposure at nanotechnology work-places: A review, Part. Fibre Toxicol., 2011, 8, 22.

    Article  PubMed  PubMed Central  Google Scholar 

  90. G. Oberdörster, A. Maynard, K. Donaldson, V. Castranova, J. Fitzpatrick, K. Ausman, J. Carter, B. Karn, W. Kreyling, D. Lai, S. Olin, N. Monteiro-Riviere, D. Warheit and H. Yang, Principles for characterizing the potential human health effects from exposure to nanomaterials: elements of a screening strategy, Part. Fibre Toxicol., 2005, 2, 8.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  91. E. Gaffet, Nanomaterials: A review of the definitions, applications, health effects. How to implement secure development, C. R. Phys., 2011, 12, 648–658.

    Article  CAS  Google Scholar 

  92. M. E. Samberg, S. J. Oldenburg and N. A. Monteiro-Riviere, Evaluation of silver nanoparticle toxicity in skin in vivo and keratinocytes in vitro, Environ. Health Perspect., 2010, 118, 407–413.

    Article  CAS  PubMed  Google Scholar 

  93. Y. Wang, Z. Chen, T. Ba, J. Pu, T. Chen, Y. Song, Y. Gu, Q. Qian, Y. Xu, K. Xiang, H. Wang and G. Jia, Susceptibility of young and adult rats to the oral toxicity of titanium dioxide nanoparticles, Small, 2013, 9, 1742–1752.

    Article  CAS  PubMed  Google Scholar 

  94. M. Hofmann-Amtenbrink, D. W. Grainger and H. Hofmann, Nanoparticles in medicine: Current chal-lenges facing inorganic nanoparticle toxicity assessments and standardizations, Nanomed. Nanotechnol. Biol. Med., 2015, 11, 1689–1694.

    Article  CAS  Google Scholar 

  95. S. K. Murthy, Nanoparticles in modern medicine: State of the art and future challenges, Int. J. Nanomed., 2007, 2, 129–141.

    CAS  Google Scholar 

  96. K. Shubhika, Nanotechnology and medicine-The upside and the downside, Int. J. Drug Dev. Res., 2012, 5, 1–10.

    Google Scholar 

  97. E. Vlachou, E. Chipp, E. Shale, Y. T. Wilson, R. Papini and N. S. Moiemen, The safety of nanocrystalline silver dres-sings on burns: a study of systemic silver absorption, Burns, 2007, 33, 979–985.

    Article  PubMed  Google Scholar 

  98. C. W. Lam, J. T. James, R. McCluskey, S. Arepalli and R. L. Hunter, A review of carbon nanotube toxicity and assessment of potential occupational and environmental health risks, Crit. Rev. Toxicol., 2006, 36, 189–217.

    Article  CAS  PubMed  Google Scholar 

  99. R. A. Baan, Carcinogenic hazards from inhaled carbon black, titanium dioxide, and talc not containing asbestos or asbestiform fibers: recent evaluations by an IARC Monographs Working Group, Inhalation Toxicol., 2007, 19 (Suppl 1), 213–228.

    Article  CAS  Google Scholar 

  100. D. H. M. Dam, K. S. B. Culver, I. Kandela, R. C. Lee, K. Chandra, H. Lee, C. Mantis, A. Ugolkov, A. P. Mazar and T. W. Odom, Biodistribution and in vivo toxicity of aptamer-loaded gold nanostars, Nanomed. Nanotechnol. Biol. Med., 2015, 11, 671–679.

    Article  CAS  Google Scholar 

  101. J. Zhao, P. Lee, M. J. Wallace and M. P. Melancon, Gold Nanoparticles in Cancer Therapy: Efficacy, Biodistribution, and Toxicity, Curr. Pharm. Des., 2015, 21, 4240–4251.

    Article  CAS  PubMed  Google Scholar 

  102. E. Boisselier and D. Astruc, Gold nanoparticles in nano-medicine: preparations, imaging, diagnostics, therapies and toxicity, Chem. Soc. Rev., 2009, 38, 1759–1782.

    Article  CAS  PubMed  Google Scholar 

  103. W. H. De Jong and P. J. A. Borm, Drug delivery and nano-particles: Applications and hazards, Int. J. Nanomed., 2008, 3, 133–149.

    Article  Google Scholar 

  104. M. R. Gwinn and V. Vallyathan, Nanoparticles: Health effects-Pros and cons, Environ. Health Perspect., 2006, 114, 1818–1825.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. M. A. Maurer-Jones, K. C. Bantz, S. A. Love, B. J. Marquis and C. L. Haynes, Toxicity of therapeutic nanoparticles, Nanomedicine, 2009, 4, 219–241.

    Article  CAS  PubMed  Google Scholar 

  106. L. Zhang, F. X. Gu, J. M. Chan, A. Z. Wang, R. S. Langer and O. C. Farokhzad, Nanoparticles in medicine: thera-peutic applications and developments, Clin. Pharmacol. Ther., 2008, 83, 761–769.

    Article  CAS  PubMed  Google Scholar 

  107. S. Nazir, T. Hussain, A. Ayub, U. Rashid and A. J. MacRobert, Nanomaterials in combating cancer: Therapeutic applications and developments, Nanomed. Nanotechnol. Biol. Med., 2014, 10, 19–34.

    Article  CAS  Google Scholar 

  108. P. Zhao, S. Y. Dong, J. Bhattacharyya and M. N. Chen, iTEP Nanoparticle-Delivered Salinomycin Displays an Enhanced Toxicity to Cancer Stem Cells in Orthotopic Breast Tumors, Mol. Pharm., 2014, 11, 2703–2712.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Y. F. Wang, P. F. Liu, L. H. Qiu, Y. Sun, M. J. Zhu, L. Y. Gu, W. Di and Y. R. Duan, Toxicity and therapy of cisplatin-loaded EGF modified mPEG-PLGA-PLL nanoparticles for SKOV3 cancer in mice, Biomaterials, 2013, 34, 4068–4077.

    Article  CAS  PubMed  Google Scholar 

  110. A. Shafei, W. El-Bakly, A. Sobhy, O. Wagdy, A. Reda, O. Aboelenin, A. Marzouk, K. Habak, R. Mostafa, M. A. Ali and M. Ellithy, A review on the efficacy and toxicity of different doxorubicin nanoparticles for targeted therapy in metastatic breast cancer, Biomed. Pharmacother., 2017, 95, 1209–1218.

    Article  CAS  PubMed  Google Scholar 

  111. Y. S. R. Elnaggar, S. M. Etman, D. A. Abdelmonsif and O. Y. Abdallah, Intranasal piperine-loaded chitosan nano-particles as brain-targeted therapy in Alzheimer’s disease: Optimization, biological efficacy, and potential toxicity, J. Pharm. Sci., 2015, 104, 3544–3556.

    Article  CAS  PubMed  Google Scholar 

  112. H. L. Chen, W. B. Nan, X. J. Wei, Y. Wang, F. Lv, H. B. Tang, Y. H. Li, C. Y. Zhou, J. T. Lin, W. L. Zhu and Q. Q. Zhang, Toxicity, pharmaco-kinetics, and in vivo efficacy of biotinylated chitosan surface-modified PLGA nanoparticles for tumor therapy, Artif. Cells, Nanomed., Biotechnol., 2017, 45, 1115–1122.

    Article  CAS  Google Scholar 

  113. L. Chen, L. Wu, F. Liu, X. Y. Qi, Y. R. Ge and S. Shen, Azo-functionalized Fe3O4 nanoparticles: a near-infrared light triggered drug delivery system for combined therapy of cancer with low toxicity, J. Mater. Chem. B, 2016, 4, 3660–3669.

    Article  CAS  PubMed  Google Scholar 

  114. H. I. Hung, O. J. Klein, S. W. Peterson, S. R. Rokosh, S. Osseiran, N. H. Nowell and C. L. Evans, PLGA nano-particle encapsulation reduces toxicity while retaining the therapeutic efficacy of EtNBS-PDT in vitro, Sci. Rep., 2016, 6, 33234.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. H. X. Wang, J. P. Wu, L. Xu, K. Xie, C. Chen and Y. H. Dong, Albumin nanoparticle encapsulation of potent cytotoxic therapeutics shows sustained drug release and alleviates cancer drug toxicity, Chem. Commun., 2017, 53, 2618–2621.

    Article  CAS  Google Scholar 

  116. A. W. Dunn, S. M. Ehsan, D. Mast, G. M. Pauletti, H. Xu, J. M. Zhang, R. C. Ewing and D. L. Shi, Photothermal effects and toxicity of Fe3O4 nanoparticles via near infra-red laser irradiation for cancer therapy, Mater. Sci. Eng., C, 2015, 46, 97–102.

    Article  CAS  Google Scholar 

  117. B. Samanta, H. Yan, N. O. Fischer, J. Shi, D. J. Jerry and V. M. Rotello, Protein-passivated Fe3O4 nanoparticles: low toxicity and rapid heating for thermal therapy, J. Mater. Chem., 2008, 18, 1204–1208.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. D. Q. Wang, L. J. Meng, Z. F. Fei, C. Hou, J. G. Long, L. Zeng, P. J. Dyson and P. Huang, Multi-layered tumor-targeting photothermal-doxorubicin releasing nanotubes eradicate tumors in vivo with negligible systemic toxicity, Nanoscale, 2018, 10, 8536–8546.

    Article  CAS  PubMed  Google Scholar 

  119. H. Y. Jiang, D. Chen, D. B. Guo, N. Wang, Y. Su, X. Jin, G. S. Tong and X. Y. Zhu, Zwitterionic gold nanorods: low toxicity and high photothermal efficacy for cancer therapy, Biomater. Sci., 2017, 5, 686–697.

    Article  CAS  PubMed  Google Scholar 

  120. Y. Luo, H. Wu, C. Feng, K. Xiao, X. Yang, Q. Liu, T. Lin, H. Zhang, J. H. Walton, Y. Ajena, Y. Hu, K. S. Lam and Y. Li, “One-Pot” Fabrication of Highly Versatile and Biocompatible Poly(vinyl alcohol)-porphyrin-based Nanotheranostics, Theranostics, 2017, 7, 3901–3914.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. A. Uppal, B. Jain, P. K. Gupta and K. Das, Photodynamic action of Rose Bengal silica nanoparticle complex on breast and oral cancer cell lines, Photochem. Photobiol., 2011, 87, 1146–1151.

    Article  CAS  PubMed  Google Scholar 

  122. Y. Zhang, N. Li, H. Suh and D. J. Irvine, Nanoparticle anchoring targets immune agonists to tumors enabling anti-cancer immunity without systemic toxicity, Nat. Commun., 2018, 9, 6.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  123. A. Jafarizad, A. Aghanejad, M. Sevim, O. Metin, J. Barar, Y. Omidi and D. Ekinci, Gold nanoparticles and reduced graphene oxide-gold nanoparticle composite materials as covalent drug delivery systems for breast cancer treatment, ChemistrySelect, 2017, 2, 6663–6672.

    Article  CAS  Google Scholar 

  124. S. S. Lee, P. J. R. Roche, P. N. Giannopoulos, E. J. Mitmaker, M. Tamilia, M. Paliouras and M. A. Trifiro, Prostate-specific membrane antigen-directed nanoparticle targeting for extreme nearfield ablation of prostate cancer cells, Tumor Biol., 2017, 39, 1–12.

    Google Scholar 

  125. L. Tao, K. Zhang, Y. J. Sun, B. Q. Jin, Z. J. Zhang and K. Yang, Anti-epithelial cell adhesion molecule mono-clonal antibody conjugated fluorescent nanoparticle bio-sensor for sensitive detection of colon cancer cells, Biosens. Bioelectron., 2012, 35, 186–192.

    Article  CAS  PubMed  Google Scholar 

  126. Y. Cheng, A. C. Samia, J. Li, M. E. Kenney, A. Resnick and C. Burda, Delivery and Efficacy of a Cancer Drug as a Function of the Bond to the Gold Nanoparticle Surface, Langmuir, 2010, 26, 2248–2255.

    Article  CAS  PubMed  Google Scholar 

  127. W. Chen and J. Zhang, Using nanoparticles to enable sim-ultaneous radiation and photodynamic therapies for cancer treatment, J. Nanosci. Nanotechnol., 2006, 6, 1159–1166.

    Article  CAS  PubMed  Google Scholar 

  128. V. V. Bakhmetyev, T. S. Minakova, S. V. Mjakin, L. A. Lebedev, A. B. Vlasenko, A. A. Nikandrova, I. A. Ekimova, N. S. Eremina, M. M. Sychov and A. Ringuede, Synthesis and surface characterization of nanosized Y2O3:Eu and YAG:Eu luminescent phosphors which are useful in photodynamic therapy of cancer, Eur. J. Nanomed., 2016, 8, 173–184.

    Article  CAS  Google Scholar 

  129. W. Chen and J. Zhang, Nanoparticles based photo-dynamic therapy and methods of making and using some, US 20070218049, 2007.

    Google Scholar 

  130. W. Chen, Nanoparticle self-lighting photodynamic therapy for cancer teatment, J. Biomed. Nanotechnol., 2008, 4, 369–376.

    Article  CAS  Google Scholar 

  131. S. Kascakova, M. Refregiers and A. Guiliani, Radioluminescent compound for radiotherapy and deep photodynamic therapy and device for deep photodynamic therapy, France Pat., WO2015/059379, 2016.

    Google Scholar 

  132. W. Lin, C. He and K. Lu, Nanoparticles for photodynamic therapy, X-ray induced photodynamic therapy, radio-therapy, chemotherapy, immunotherapy, and any combination thereof, USA Pat., WO2016061256A1, 2016.

    Google Scholar 

  133. J. Takahashi and M. Misawa, Analysis of potential radio-sensitizing materials for X-ray-induced photodynamic therapy, NanoBiotechnology, 2007, 3, 116–126.

    Article  CAS  Google Scholar 

  134. Z. Liu, L. Xiong, G. Ouyang, L. Ma, S. Sahi, K. Wang, L. Lin, H. Huang, X. Miao, W. Chen and Y. Wen, Investigation of copper cysteamine nanoparticles as a new type of radiosensitiers for colorectal carcinoma treatment, Sci. Rep., 2017, 7, 9290.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  135. L. Ma, X. Zou and W. Chen, A new X-ray activated nano-particle photosensitizer for cancer treatment, J. Biomed. Nanotechnol., 2014, 10, 1501–1508.

    Article  CAS  PubMed  Google Scholar 

  136. C. C. Yang, Y. J. Sun, P. H. Chung, W. Y. Chen, W. Swieszkowski, W. M. Tian and F. H. Lin, Development of Ce-doped TiO2 activated by X-ray irradiation for alterna-tive cancer treatment, Ceram. Int., 2017, 43, 12675–12683.

    Article  CAS  Google Scholar 

  137. J. P. Scaffidi, M. K. Gregas, B. Lauly, Y. Zhang and T. Vo-Dinh, Activity of psoralen-functionalized nanoscintillators against cancer cells upon X-ray excitation, ACS Nano, 2011, 5, 4679–4687.

    Article  CAS  PubMed  Google Scholar 

  138. L. Ma, X. Zou, B. Bui, W. Chen, K. H. Song and T. Solberg, X-ray excited ZnS:Cu,Co afterglow nanoparticles for photodynamic activation, Appl. Phys. Lett., 2014, 105, 013702.

    Article  CAS  Google Scholar 

  139. L. Ma, X. Zou, M. Hossu and W. Chen, Synthesis of ZnS: Ag,Co water-soluble blue afterglow nanoparticles and application in photodynamic activation, Nanotechnology, 2016, 27, 315602.

    Article  PubMed  CAS  Google Scholar 

  140. S. Sadjadpour, S. Safarian, S. J. Zargar and N. Sheibani, Antiproliferative effects of ZnO, ZnO-MTCP, and ZnO-CuMTCP nanoparticles with safe intensity UV and X-ray irradiation, Biotechnol. Appl. Biochem., 2016, 63, 113–124.

    Article  CAS  PubMed  Google Scholar 

  141. W.-J. Kuo, Y.-C. Wang, M.-H. Chen, F.-I. Tung and T.-Y. Liu, Study of a novel vehicle developed for enhancing the efficacy of radiation therapy, Ceram. Int., 2017, 43, S789–S796.

    Article  CAS  Google Scholar 

  142. Z. Mohammadi, A. Sazgarnia, O. Rajabi and M. Seilanian Toosi, Comparative study of X-ray treatment and photo-dynamic therapy by using 5-aminolevulinic acid conju-gated gold nanoparticles in a melanoma cell line, Artif. Cells, Nanomed., Biotechnol., 2017, 45, 467–473.

    Article  CAS  Google Scholar 

  143. H. Chen, X. Sun, G. D. Wang, K. Nagata, Z. Hao, A. Wang, Z. Li, J. Xie and B. Shen, LiGa5O8:Cr-based theranostic nanoparticles for imaging-guided X-ray induced photo-dynamic therapy of deep-seated tumors, Mater. Horiz., 2017, 4, 1092–1101.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. K. Popovich, L. Prochazkova, I. T. Pelikanova, M. Vlk, M. Palkovsky, V. Jary, M. Nikl, V. Mucka, E. Mihokova and V. Cuba, Preliminary study on singlet oxygen production using CeF3:Tb3+@SiO2-PpIX, Radiat. Meas., 2016, 90, 325–328.

    Article  CAS  Google Scholar 

  145. S. L. Yefimova, T. N. Tkacheva, P. O. Maksimchuk, I. I. Bespalova, K. O. Hubenko, V. K. Klochkov, A. V. Sorokin and Y. V. Malyukin, GdVO4:Eu3+ nano-particles-Methylene Blue complexes for PDT: Electronic excitation energy transfer study, J. Lumin., 2017, 192, 975–981.

    Article  CAS  Google Scholar 

  146. E. Abliz, J. E. Collins, H. Bell and D. B. Tata, Novel appli-cations of diagnostic X-rays in activating a clinical photo-dynamic drug: Photofrin II through X-ray induced visible luminescence from “rare-earth” formulated particles, J. X-Ray Sci. Technol., 2011, 19, 521–530.

    CAS  Google Scholar 

  147. S. Clement, W. Deng, E. Camilleri, B. C. Wilson and E. M. Goldys, X-ray induced singlet oxygen generation by nanoparticle-photosensitizer conjugates for photo-dynamic therapy: determination of singlet oxygen quantum yield, Sci. Rep., 2016, 6, 19954.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Y. Tang, J. Hu, A. H. Elmenoufy and X. Yang, Highly efficient FRET system capable of deep photodynamic therapy established on X-ray excited mesoporous LaF3:Tb scintillating nanoparticles, ACS Appl. Mater. Interfaces, 2015, 7, 12261–12269.

    Article  CAS  PubMed  Google Scholar 

  149. H. Chen, G. D. Wang, Y. J. Chuang, Z. Zhen, X. Chen, P. Biddinger, Z. Hao, F. Liu, B. Shen, Z. Pan and J. Xie, Nanoscintillator-mediated X-ray inducible photodynamic therapy for in vivo cancer treatment, Nano Lett., 2015, 15, 2249–2256.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. G. D. Wang, H. T. Nguyen, H. Chen, P. B. Cox, L. Wang, K. Nagata, Z. Hao, A. Wang, Z. Li and J. Xie, X-ray induced photodynamic therapy: A combination of radiotherapy and photodynamic therapy, Theranostics, 2016, 6, 2295–2305.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. M. H. Chen, Y. J. Jenh, S. K. Wu, Y. S. Chen, N. Hanagata and F. H. Lin, Non-invasive Photodynamic Therapy in Brain Cancer by Use of Tb3+-Doped LaF3 Nanoparticles in Combination with Photosensitizer Through X-ray Irradiation: A Proof-of-Concept Study, Nanoscale Res. Lett., 2017, 12, 62.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  152. Y. Liu, W. Chen, S. Wang and A. G. Joly, Investigation of water-soluble X-ray luminescence nanoparticles for photo-dynamic activation, Appl. Phys. Lett., 2008, 92, 043901.

    Article  CAS  Google Scholar 

  153. F. Rossi, E. Bedogni, F. Bigi, T. Rimoldi, L. Cristofolini, S. Pinelli, R. Alinovi, M. Negri, S. C. Dhanabalan, G. Attolini, F. Fabbri, M. Goldoni, A. Mutti, G. Benecchi, C. Ghetti, S. Lannotta and G. Salviati, Porphyrin conju-gated SiC/SiOx nanowires for X-ray-excited photodynamic therapy, Sci. Rep., 2015, 5, 7606.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. R. Tatti, M. Timpel, M. V. Nardi, F. Fabbri, R. Rossi, L. Pasquardini, A. Chiasera, L. Aversa, K. Koshmak, A. Giglia, L. Pasquali, T. Rimoldi, L. Cristofolini, G. Attolini, S. Varas, S. Iannotta, R. Verucchi and G. Salviati, Functionalization of SiC/SiOx nanowires with a porphyrin derivative: a hybrid nanosystem for X-ray induced singlet oxygen generation, Mol. Syst. Des. Eng., 2017, 2, 165–172.

    Article  CAS  Google Scholar 

  155. C. L. Pan, M. H. Chen, F. I. Tung and T. Y. Liu, A nanove-hicle developed for treating deep-seated bacteria using low-dose X-ray, Acta Biomater., 2017, 47, 159–169.

    Article  CAS  PubMed  Google Scholar 

  156. H. T. Kim, K. H. Kim, G. H. Choi, S. Jheon, S. H. Park, B. I. Kim, K. Hyodo, M. Ando and J. K. Kim, in 12th World Congress of the International Photodynamic Association: Photodynamic Therapy: Back to the Future, ed. D. H. Kessel, 2009, vol. 7380.

  157. S. A. Osseni, S. Lechevallier, M. Verelst, C. Dujardin, J. Dexpert-Ghys, D. Neumeyer, M. Leclercq, H. Baaziz, D. Cussac, V. Santran and R. Mauricot, New nanoplatform based on Gd2O2S:Eu3+ core: synthesis, characterization and use for in vitro bio-labelling, J. Mater. Chem., 2011, 21, 18365–18372.

    Article  CAS  Google Scholar 

  158. A. Kleinauskas, S. Rocha, S. Sahu, Y. P. Sun and P. Juzenas, Carbon-core silver-shell nanodots as sensi-tizers for phototherapy and radiotherapy, Nanotechnology, 2013, 24, 325103.

    Article  PubMed  CAS  Google Scholar 

  159. C. Zhang, K. Zhao, W. Bu, D. Ni, Y. Liu, J. Feng and J. Shi, Marriage of scintillator and semiconductor for synchro-nous radiotherapy and deep photodynamic therapy with diminished oxygen dependence, Angew. Chem., Int. Ed., 2015, 54, 1770–1774.

    Article  CAS  Google Scholar 

  160. K. Kirakci, P. Kubat, K. Fejfarova, J. Martincik, M. Nikl and K. Lang, X-ray inducible luminescence ands inglet oxygen sensitization by an octahedral molybdenum cluster compound: A new class of nanoscintillators, Inorg. Chem., 2016, 55, 803–809.

    Article  CAS  PubMed  Google Scholar 

  161. Z. Guo, S. Zhu, Y. Yong, X. Zhang, X. Dong, J. Du, J. Xie, Q. Wang, Z. Gu and Y. Zhao, Synthesis of BSA-coated BiOI@Bi2S3 semiconductor heterojunction nanoparticles and their applications for radio/photodynamic/photother-mal synergistic therapy of tumor, Adv. Mater., 2017, 29, 1704136.

    Article  CAS  Google Scholar 

  162. A. L. Bulin, C. Truillett, R. Chouikrat, F. Lux, C. Frochot, D. Amans, G. Ledoux, O. Tillement, P. Perriat, M. Barberi-Heyob and C. Dujardin, X-ray-induced singlet oxygen acti-vation with nanoscintillator-coupled porphyrins, J. Phys. Chem. C, 2013, 117, 21583–21589.

    Article  CAS  Google Scholar 

  163. X. Zou, M. Yao, L. Ma, M. Hossu, X. Han, P. Juzenas and W. Chen, X-ray-induced nanoparticle-based photodynamic therapy of cancer, Nanomedicine, 2014, 9, 2339–2351.

    Article  CAS  PubMed  Google Scholar 

  164. S. Kascáková, A. Giuliani, S. Lacerda, A. Pallier, P. Mercere, É. Tóth and M. Réfrégiers, X-ray-induced radiophotodynamic therapy (RPDT) using lanthanide micelles: Beyond depth limitations, Nano Res., 2015, 8, 2373–2379.

    Article  CAS  Google Scholar 

  165. W. Fan, B. Shen, W. Bu, X. Zheng, Q. He, Z. Cui, D. Ni, K. Zhao, S. Zhang and J. Shi, Intranuclear biophotonics by smart design of nuclear-targeting photo-/radio-sensitizers co-loaded upconversion nanoparticles, Biomaterials, 2015, 69, 89–98.

    Article  CAS  PubMed  Google Scholar 

  166. H.-P. Chen, F.-I. Tung, M.-H. Chen and T.-Y. Liu, A mag-netic vehicle realized tumor cell-targeted radiotherapy using low-dose radiation, J. Controlled Release, 2016, 226, 182–192.

    Article  CAS  Google Scholar 

  167. K. Kudinov, D. Bekah, D. Cooper, S. Shastry, C. Hill, S. Bradforth and J. Nadeau, Presented in part at the SPIE BiOS, 2016.

    Google Scholar 

  168. M. Zahedifar, E. Sadeghi, M. M. Shanei, A. Sazgarnia and M. Mehrabi, Afterglow properties of CaF2:Tm nano-particles and its potential application in photodynamic therapy, J. Lumin., 2016, 171, 254–258.

    Article  CAS  Google Scholar 

  169. H. Homayoni, L. Ma, J. Zhang, S. K. Sahi, L. H. Rashidi, B. Bui and W. Chen, Synthesis and conjugation of Sr2MgSi2O7:Eu2+, Dy3+ water soluble afterglow nano-particles for photodynamic activation, Photodiagn. Photodyn. Ther., 2016, 16, 90–99.

    Article  CAS  Google Scholar 

  170. R. Chouikrat, F. Baros, J. C. Andre, R. Vanderesse, B. Viana, A. L. Bulin, C. Dujardin, P. Arnoux, M. Verelst and C. Frochot, A photosensitizer lanthanide nanoparticle formulation that induces singlet oxygen with direct light excitation, but not by photon or X-ray energy transfer, Photochem. Photobiol., 2017, 93, 1439–1448.

    Article  CAS  PubMed  Google Scholar 

  171. S. Clement, W. Chen, A. G. Anwer and E. M. Goldys, Verteprofin conjugated to gold nanoparticles for fluo-rescent cellular bioimaging and X-ray mediated photo-dynamic therapy, Microchim. Acta, 2017, 184, 1765–1771.

    Article  CAS  Google Scholar 

  172. S. Kokotov, A. Lewis, R. Neumann and S. Amrusi, X-ray induced visible luminescence of porphyrins, Photochem. Photobiol., 1994, 59, 385–387.

    Article  CAS  PubMed  Google Scholar 

  173. G. Lan, K. Ni, R. Xu, K. Lu, Z. Lin, C. Chan and W. Lin, Nanoscale metal-organic layers for deeply penetrating X-ray-induced photodynamic therapy, Angew. Chem., Int. Ed., 2017, 56, 12102–12106.

    Article  CAS  Google Scholar 

  174. J. Douglas, ICRU Report 50—Prescribing, recording and reporting photon beam therapy, Med. Phys., 1994, 21, 833–834.

    Article  Google Scholar 

  175. K. C. Wei, K. C. Yang, L. W. Chen, W. C. Liu, W. C. Chen, W. Y. Chiou and P. C. Lai, Management of fluoroscopy-induced radiation ulcer: One-stage radical excision and immediate reconstruction, Sci. Rep., 2016, 6, 35875.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  176. R. Waksman, P. E. McEwan, T. I. Moore, R. Pakala, F. D. Kolodgie, D. G. Hellinga, R. C. Seabron, S. J. Rychnovsky, J. Vasek, R. W. Scott and R. Virmani, PhotoPoint photodynamic therapy promotes stabilization of atherosclerotic plaques and inhibits plaque pro-gression, J. Am. Coll. Cardiol., 2008, 52, 1024–1032.

    Article  CAS  PubMed  Google Scholar 

  177. S. Michels and U. Schmidt-Erfurth, Photodynamic therapy with verteporfin: a new treatment in ophthalmology, Semin. Ophthalmol., 2001, 16, 201–206.

    Article  CAS  PubMed  Google Scholar 

  178. J. N. Silva, P. Filipe, P. Morliere, J. C. Maziere, J. P. Freitas, M. M. Gomes and R. Santus, Photodynamic therapy: Dermatology and ophthalmology as main fields of current applications in clinic, Biomed. Mater. Eng., 2008, 18, 319–327.

    CAS  PubMed  Google Scholar 

  179. Y. Lee and E. D. Baron, Photodynamic therapy: current evidence and applications in dermatology, Semin. Cutaneous Med. Surg., 2011, 30, 199–209.

    Article  CAS  Google Scholar 

  180. R. M. Szeimies, S. Lischner, W. Philipp-Dormston, T. Walker, D. Hiepe-Wegener, K. Feise, M. Podda, W. Prager, E. Kohl and S. Karrer, Photodynamic therapy for skin rejuvenation: treatment options-results of a con-sensus conference of an expert group for aesthetic photo-dynamic therapy, J. Dtsch. Dermatol. Ges., 2013, 11, 632–636.

    PubMed  Google Scholar 

  181. P. Babilas, S. Schreml, M. Landthaler and R. M. Szeimies, Photodynamic therapy in dermatology: state-of-the-art, Photodermatol., Photoimmunol. Photomed., 2010, 26, 118–132.

    Article  CAS  Google Scholar 

  182. P. Meisel and T. Kocher, Photodynamic therapy for peri-odontal diseases: state of the art, J. Photochem. Photobiol., B, 2005, 79, 159–170.

    Article  CAS  Google Scholar 

  183. K. Konopka and T. Goslinski, Photodynamic therapy in dentistry, J. Dent. Res., 2007, 86, 694–707.

    Article  CAS  PubMed  Google Scholar 

  184. T. G. Cotter, Apoptosis and cancer: the genesis of a research field, Nat. Rev. Cancer, 2009, 9, 501–507.

    Article  CAS  PubMed  Google Scholar 

  185. G. Bozzini, P. Colin, N. Betrouni, P. Nevoux, A. Ouzzane, P. Puech, A. Villers and S. Mordon, Photodynamic therapy in urology: what can we do now and where are we heading?, Photodiagn. Photodyn. Ther., 2012, 9, 261–273.

    Article  CAS  Google Scholar 

  186. L. Costa, M. A. Faustino, M. G. Neves, A. Cunha and A. Almeida, Photodynamic inactivation of mammalian viruses and bacteriophages, Viruses, 2012, 4, 1034–1074.

    Article  PubMed  PubMed Central  Google Scholar 

  187. M. Wainwright, Local treatment of viral disease using photodynamic therapy, Int. J. Antimicrob. Agents, 2003, 21, 510–520.

    Article  CAS  PubMed  Google Scholar 

  188. F. Pereira Gonzales and T. Maisch, Photodynamic inacti-vation for controlling Candida albicans infections, Fungal Biol., 2012, 116, 1–10.

    Article  PubMed  CAS  Google Scholar 

  189. P. Calzavara-Pinton, M. T. Rossi, R. Sala and M. Venturini, Photodynamic antifungal chemotherapy, Photochem. Photobiol., 2012, 88, 512–522.

    Article  CAS  PubMed  Google Scholar 

  190. M. P. Paz-Cristobal, D. Royo, A. Rezusta, E. Andres-Ciriano, M. C. Alejandre, J. F. Meis, M. J. Revillo, C. Aspiroz, S. Nonell and Y. Gilaberte, Photodynamic fun-gicidal efficacy of hypericin and dimethyl methylene blue against azole-resistant Candida albicans strains, Mycoses, 2014, 57, 35–42.

    Article  CAS  PubMed  Google Scholar 

  191. Y. Arenas, S. Monro, G. Shi, A. Mandel, S. McFarland and L. Lilge, Photodynamic inactivation of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus with Ru(II)-based type I/type II photosensitizers, Photodiagn. Photodyn. Ther., 2013, 10, 615–625.

    Article  CAS  Google Scholar 

  192. F. F. Sperandio, Y. Y. Huang and M. R. Hamblin, Antimicrobial photodynamic therapy to kill Gram-negative bacteria, Recent Pat. Antiinfect Drug Discov., 2013, 8, 108–120.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  193. M. Magaraggia, F. Faccenda, A. Gandolfi and G. Jori, Treatment of microbiologically polluted aquaculture waters by a novel photochemical technique of potentially low environmental impact, J. Environ. Monit., 2006, 8, 923–931.

    Article  CAS  PubMed  Google Scholar 

  194. R. Bonnett, M. A. Krysteva, I. G. Lalov and S. V. Artarsky, Water disinfection using photosensitizers immobilized on chitosan, Water Res., 2006, 40, 1269–1275.

    Article  CAS  PubMed  Google Scholar 

  195. L. Brovko, Photodynamic treatment: a new efficient alternative for surface sanitation, Adv. Food Nutr. Res., 2010, 61, 119–147.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to acknowledge Régis Vanderesse for his kind help in writing this manuscript.

Author information

Authors and Affiliations

  1. Laboratoire Réactions et Génie des Procédés (LRGP), UMR 7274, Université de Lorraine, CNRS, Nancy, France

    L. Larue, Z. Youssef, L. Colombeau, J. C. André, P. Arnoux, F. Baros & C. Frochot

  2. Laboratoire de Chimie Physique Macromoléculaire (LCPM), UMR 7375, Université de Lorraine, CNRS, Nancy, France

    A. Ben Mihoub, L. Colombeau & S. Acherar

  3. Image Assisted Laser Therapy for Oncology (ONCO-THAI), U 1189, Université de Lille, INSERM, CHU Lille, Lille, France

    M. Vermandel

Authors
  1. L. Larue
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Ben Mihoub
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Z. Youssef
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. L. Colombeau
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. Acherar
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. J. C. André
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. P. Arnoux
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. F. Baros
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. M. Vermandel
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. C. Frochot
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to C. Frochot.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Larue, L., Ben Mihoub, A., Youssef, Z. et al. Using X-rays in photodynamic therapy: an overview. Photochem Photobiol Sci 17, 1612–1650 (2018). https://doi.org/10.1039/c8pp00112j

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/c8pp00112j

Search

Navigation