DOI QR코드

DOI QR Code

Application of photodynamic therapy in gastrointestinal disorders: an outdated or re-emerging technique?

  • Lee, Han Hee (Division of Gastroenterology, Department of Internal Medicine, College of Medicine, The Catholic University of Korea) ;
  • Choi, Myung-Gyu (Division of Gastroenterology, Department of Internal Medicine, College of Medicine, The Catholic University of Korea) ;
  • Hasan, Tayyaba (Wellman Center for Photomedicine, Massachusetts General Hospital, Harvard Medical School)
  • Received : 2016.05.11
  • Accepted : 2016.12.19
  • Published : 2017.01.01

Abstract

Photodynamic therapy (PDT) is a promising therapeutic modality that involves the administration of a photosensitizer followed by local illumination with a specific wavelength of light in the presence of oxygen. PDT is minimally invasive, has high selectivity for cancer, and has good patient compliance due to the simplicity of the procedure; therefore, PDT is widely used as a palliative and salvage treatment in patients with various gastrointestinal malignancies. When used as a salvage treatment for locoregional failures after definitive chemoradiotherapy for esophageal cancer, favorable results have been reported. PDT in conjunction with biliary stenting is a promising palliative treatment for unresectable cholangiocarcinoma, and can be used as an advanced diagnostic and therapeutic strategy in peritoneal dissemination of gastric cancer. Recent clinical reports of PDT for treating non-resectable pancreatic cancer also show promising results. To widen the application of PDT, the integration of PDT with molecular imaging and nanotechnology is being extensively studied. Based on these new developments, PDT is likely to re-emerge as a valuable technique in the treatment of diverse gastrointestinal diseases.

Keywords

Acknowledgement

Supported by : National Research Foundation of Korea (NRF), Catholic Medical Center Research Foundation, National Institutes of Health/National Cancer Institute (NIH/NCI)

References

  1. McCaughan JS Jr, Guy JT, Hawley P, et al. Hematoporphyrin-derivative and photoradiation therapy of malignant tumors. Lasers Surg Med 1983;3:199-209. https://doi.org/10.1002/lsm.1900030302
  2. Yoshida K, Suzuki S, Mimura S, et al. Photodynamic therapy for superficial esophageal cancer: a phase III study using PHE and excimer dye laser. Gan To Kagaku Ryoho 1993;20:2063-2066.
  3. Soetikno R, Kaltenbach T, Yeh R, Gotoda T. Endoscopic mucosal resection for early cancers of the upper gastrointestinal tract. J Clin Oncol 2005;23:4490-4498. https://doi.org/10.1200/JCO.2005.19.935
  4. Dolmans DE, Fukumura D, Jain RK. Photodynamic therapy for cancer. Nat Rev Cancer 2003;3:380-387. https://doi.org/10.1038/nrc1071
  5. Barr H, Dix AJ, Kendall C, Stone N. Review article: the potential role for photodynamic therapy in the management of upper gastrointestinal disease. Aliment Pharmacol Ther 2001;15:311-321. https://doi.org/10.1046/j.1365-2036.2001.00936.x
  6. Pogue BW, Sheng C, Benevides J, et al. Protoporphyrin IX fluorescence photobleaching increases with the use of fractionated irradiation in the esophagus. J Biomed Opt 2008;13:034009. https://doi.org/10.1117/1.2937476
  7. Laukka MA, Wang KK. Initial results using low-dose photodynamic therapy in the treatment of Barrett's esophagus. Gastrointest Endosc 1995;42:59-63. https://doi.org/10.1016/S0016-5107(95)70245-8
  8. Overholt BF, Panjehpour M. Barrett's esophagus: photodynamic therapy for ablation of dysplasia, reduction of specialized mucosa, and treatment of superficial esophageal cancer. Gastrointest Endosc 1995;42:64-70. https://doi.org/10.1016/S0016-5107(95)70246-6
  9. Overholt BF, Panjehpour M, Haydek JM. Photodynamic therapy for Barrett's esophagus: follow-up in 100 patients. Gastrointest Endosc 1999;49:1-7. https://doi.org/10.1016/S0016-5107(99)70437-2
  10. Overholt BF, Lightdale CJ, Wang KK, et al. Photodynamic therapy with porfimer sodium for ablation of high-grade dysplasia in Barrett's esophagus: international, partially blinded, randomized phase III trial. Gastrointest Endosc 2005;62:488-498. https://doi.org/10.1016/j.gie.2005.06.047
  11. Yano T, Muto M, Yoshimura K, et al. Phase I study of photodynamic therapy using talaporfin sodium and diode laser for local failure after chemoradiotherapy for esophageal cancer. Radiat Oncol 2012;7:113. https://doi.org/10.1186/1748-717X-7-113
  12. Yano T, Muto M, Minashi K, et al. Long-term results of salvage photodynamic therapy for patients with local failure after chemoradiotherapy for esophageal squamous cell carcinoma. Endoscopy 2011;43:657-663. https://doi.org/10.1055/s-0030-1256373
  13. Nakamura T, Fukui H, Shirakawa K, Fujii Y, Fujimori T, Terano A. Photodynamic therapy of superficial esophageal cancer with a transparent hood. Gastrointest Endosc 2004;60:120-124. https://doi.org/10.1016/S0016-5107(04)01525-1
  14. Tanaka T, Matono S, Nagano T, et al. Photodynamic therapy for large superficial squamous cell carcinoma of the esophagus. Gastrointest Endosc 2011;73:1-6. https://doi.org/10.1016/j.gie.2010.08.049
  15. Yano T, Muto M, Minashi K, Ohtsu A, Yoshida S. Photodynamic therapy as salvage treatment for local failures after definitive chemoradiotherapy for esophageal cancer. Gastrointest Endosc 2005;62:31-36. https://doi.org/10.1016/S0016-5107(05)00545-6
  16. Hatogai K, Yano T, Kojima T, et al. Salvage photodynamic therapy for local failure after chemoradiotherapy for esophageal squamous cell carcinoma. Gastrointest Endosc 2016;83:1130-1139. https://doi.org/10.1016/j.gie.2015.11.016
  17. Litle VR, Luketich JD, Christie NA, et al. Photodynamic therapy as palliation for esophageal cancer: experience in 215 patients. Ann Thorac Surg 2003;76:1687-1692. https://doi.org/10.1016/S0003-4975(03)01299-2
  18. Lindenmann J, Matzi V, Neuboeck N, et al. Individualized, multimodal palliative treatment of inoperable esophageal cancer: clinical impact of photodynamic therapy resulting in prolonged survival. Lasers Surg Med 2012;44:189-198. https://doi.org/10.1002/lsm.22006
  19. Yoon HY, Cheon YK, Choi HJ, Shim CS. Role of photodynamic therapy in the palliation of obstructing esophageal cancer. Korean J Intern Med 2012;27:278-284. https://doi.org/10.3904/kjim.2012.27.3.278
  20. Pennathur A, Farkas A, Krasinskas AM, et al. Esophagectomy for T1 esophageal cancer: outcomes in 100 patients and implications for endoscopic therapy. Ann Thorac Surg 2009;87:1048-1054. https://doi.org/10.1016/j.athoracsur.2008.12.060
  21. Tachibana M, Hirahara N, Kinugasa S, Yoshimura H. Clinicopathologic features of superficial esophageal cancer: results of consecutive 100 patients. Ann Surg Oncol 2008;15:104-116. https://doi.org/10.1245/s10434-007-9604-4
  22. Miyata H, Yamasaki M, Takiguchi S, et al. Salvage esophagectomy after definitive chemoradiotherapy for thoracic esophageal cancer. J Surg Oncol 2009;100:442-446. https://doi.org/10.1002/jso.21353
  23. Heier SK, Rothman KA, Heier LM, Rosenthal WS. Photodynamic therapy for obstructing esophageal cancer: light dosimetry and randomized comparison with Nd:YAG laser therapy. Gastroenterology 1995;109:63-72. https://doi.org/10.1016/0016-5085(95)90269-4
  24. Lightdale CJ, Heier SK, Marcon NE, et al. Photodynamic therapy with porfimer sodium versus thermal ablation therapy with Nd:YAG laser for palliation of esophageal cancer: a multicenter randomized trial. Gastrointest Endosc 1995;42:507-512. https://doi.org/10.1016/S0016-5107(95)70002-1
  25. Soderlund C, Linder S. Covered metal versus plastic stents for malignant common bile duct stenosis: a prospective, randomized, controlled trial. Gastrointest Endosc 2006;63:986-995. https://doi.org/10.1016/j.gie.2005.11.052
  26. O'Brien S, Hatfield AR, Craig PI, Williams SP. A three year follow up of self expanding metal stents in the endoscopic palliation of longterm survivors with malignant biliary obstruction. Gut 1995;36:618-621. https://doi.org/10.1136/gut.36.4.618
  27. Kahaleh M, Mishra R, Shami VM, et al. Unresectable cholangiocarcinoma: comparison of survival in biliary stenting alone versus stenting with photodynamic therapy. Clin Gastroenterol Hepatol 2008;6:290-297. https://doi.org/10.1016/j.cgh.2007.12.004
  28. Ortner ME, Caca K, Berr F, et al. Successful photodynamic therapy for nonresectable cholangiocarcinoma: a randomized prospective study. Gastroenterology 2003;125:1355-1363. https://doi.org/10.1016/j.gastro.2003.07.015
  29. Zoepf T, Jakobs R, Arnold JC, Apel D, Riemann JF. Palliation of nonresectable bile duct cancer: improved survival after photodynamic therapy. Am J Gastroenterol 2005;100:2426-2430. https://doi.org/10.1111/j.1572-0241.2005.00318.x
  30. Witzigmann H, Berr F, Ringel U, et al. Surgical and palliative management and outcome in 184 patients with hilar cholangiocarcinoma: palliative photodynamic therapy plus stenting is comparable to r1/r2 resection. Ann Surg 2006;244:230-239. https://doi.org/10.1097/01.sla.0000217639.10331.47
  31. Quyn AJ, Ziyaie D, Polignano FM, Tait IS. Photodynamic therapy is associated with an improvement in survival in patients with irresectable hilar cholangiocarcinoma. HPB (Oxford) 2009;11:570-577. https://doi.org/10.1111/j.1477-2574.2009.00102.x
  32. Cheon YK, Lee TY, Lee SM, Yoon JY, Shim CS. Longterm outcome of photodynamic therapy compared with biliary stenting alone in patients with advanced hilar cholangiocarcinoma. HPB (Oxford) 2012;14:185-193. https://doi.org/10.1111/j.1477-2574.2011.00424.x
  33. Lee TY, Cheon YK, Shim CS, Cho YD. Photodynamic therapy prolongs metal stent patency in patients with unresectable hilar cholangiocarcinoma. World J Gastroenterol 2012;18:5589-5594. https://doi.org/10.3748/wjg.v18.i39.5589
  34. Huggett MT, Jermyn M, Gillams A, et al. Phase I/II study of verteporfin photodynamic therapy in locally advanced pancreatic cancer. Br J Cancer 2014;110:1698-1704. https://doi.org/10.1038/bjc.2014.95
  35. Bown SG, Rogowska AZ, Whitelaw DE, et al. Photodynamic therapy for cancer of the pancreas. Gut 2002;50:549-557. https://doi.org/10.1136/gut.50.4.549
  36. Kelty CJ, Brown NJ, Reed MW, Ackroyd R. The use of 5-aminolaevulinic acid as a photosensitiser in photodynamic therapy and photodiagnosis. Photochem Photobiol Sci 2002;1:158-168. https://doi.org/10.1039/b201027p
  37. Isomoto H, Nanashima A, Senoo T, et al. In vivo fluorescence navigation of gastric and upper gastrointestinal tumors by 5-aminolevulinic acid mediated photodynamic diagnosis with a laser-equipped video image endoscope. Photodiagnosis Photodyn Ther 2015;12:201-208. https://doi.org/10.1016/j.pdpdt.2015.03.006
  38. Kishi K, Fujiwara Y, Yano M, et al. Diagnostic laparoscopy with 5-aminolevulinic-acid-mediated photodynamic diagnosis enhances the detection of peritoneal micrometastases in advanced gastric cancer. Oncology 2014;87:257-265. https://doi.org/10.1159/000365356
  39. Kishi K, Fujiwara Y, Yano M, et al. Staging laparoscopy using ALA-mediated photodynamic diagnosis improves the detection of peritoneal metastases in advanced gastric cancer. J Surg Oncol 2012;106:294-298. https://doi.org/10.1002/jso.23075
  40. Mari E, Floriani I, Tinazzi A, et al. Efficacy of adjuvant chemotherapy after curative resection for gastric cancer: a meta-analysis of published randomised trials. A study of the GISCAD (Gruppo Italiano per lo Studio dei Carcinomi dell'Apparato Digerente). Ann Oncol 2000;11:837-843. https://doi.org/10.1023/A:1008377101672
  41. Yan TD, Black D, Sugarbaker PH, et al. A systematic review and meta-analysis of the randomized controlled trials on adjuvant intraperitoneal chemotherapy for resectable gastric cancer. Ann Surg Oncol 2007;14:2702-2713. https://doi.org/10.1245/s10434-007-9487-4
  42. Baeza MR, Giannini TO, Rivera SR, et al. Adjuvant radiochemotherapy in the treatment of completely resected, locally advanced gastric cancer. Int J Radiat Oncol Biol Phys 2001;50:645-650. https://doi.org/10.1016/S0360-3016(01)01467-5
  43. Kishi K, Yano M, Inoue M, et al. Talaporfin-mediated photodynamic therapy for peritoneal metastasis of gastric cancer in an in vivo mouse model: drug distribution and efficacy studies. Int J Oncol 2010;36:313-320.
  44. Tsujimoto H, Morimoto Y, Takahata R, et al. Photodynamic therapy using nanoparticle loaded with indocyanine green for experimental peritoneal dissemination of gastric cancer. Cancer Sci 2014;105:1626-1630. https://doi.org/10.1111/cas.12553
  45. Miller JD, Baron ED, Scull H, et al. Photodynamic therapy with the phthalocyanine photosensitizer Pc 4: the case experience with preclinical mechanistic and early clinical-translational studies. Toxicol Appl Pharmacol 2007;224:290-299. https://doi.org/10.1016/j.taap.2007.01.025
  46. Barolet D. Light-emitting diodes (LEDs) in dermatology. Semin Cutan Med Surg 2008;27:227-238. https://doi.org/10.1016/j.sder.2008.08.003
  47. Juzeniene A, Juzenas P, Ma LW, Iani V, Moan J. Effectiveness of different light sources for 5-aminolevulinic acid photodynamic therapy. Lasers Med Sci 2004;19:139-149. https://doi.org/10.1007/s10103-004-0314-x
  48. Mang TS. Lasers and light sources for PDT: past, present and future. Photodiagnosis Photodyn Ther 2004;1:43-48. https://doi.org/10.1016/S1572-1000(04)00012-2
  49. Henderson BW, Busch TM, Vaughan LA, et al. Photofrin photodynamic therapy can significantly deplete or preserve oxygenation in human basal cell carcinomas during treatment, depending on fluence rate. Cancer Res 2000;60:525-529.
  50. Curnow A, Haller JC, Bown SG. Oxygen monitoring during 5-aminolaevulinic acid induced photodynamic therapy in normal rat colon. Comparison of continuous and fractionated light regimes. J Photochem Photobiol B 2000;58:149-155. https://doi.org/10.1016/S1011-1344(00)00120-2
  51. Goetz M, Wang TD. Molecular imaging in gastrointestinal endoscopy. Gastroenterology 2010;138:828.e1-833.e1.
  52. Kim JH, Roh YJ, Kim IW, et al. Targeted photodynamic therapy with colon cancer-specific peptide conjugated photosensitizer. Photodiagnosis Photodyn Ther 2015;12:340.
  53. Bae BC, Yang SG, Jeong S, et al. Polymeric photosensitizer-embedded self-expanding metal stent for repeatable endoscopic photodynamic therapy of cholangiocarcinoma. Biomaterials 2014;35:8487-8495. https://doi.org/10.1016/j.biomaterials.2014.07.001
  54. Min D, Jeong D, Choi MG, Na K. Photochemical tissue penetration via photosensitizer for effective drug penetration in a non-vascular tumor. Biomaterials 2015;52:484-493. https://doi.org/10.1016/j.biomaterials.2015.02.060
  55. Spring BQ, Bryan Sears R, Zheng LZ, et al. A photoactivable multi-inhibitor nanoliposome for tumour control and simultaneous inhibition of treatment escape pathways. Nat Nanotechnol 2016;11:378-387. https://doi.org/10.1038/nnano.2015.311

Cited by

  1. Ethnopharmacological Approaches for Therapy of Jaundice: Part I vol.8, pp.None, 2017, https://doi.org/10.3389/fphar.2017.00518
  2. Leveraging Engineering of Indocyanine Green-Encapsulated Polymeric Nanocomposites for Biomedical Applications vol.8, pp.6, 2017, https://doi.org/10.3390/nano8060360
  3. Status and future directions in the management of pancreatic cancer: potential impact of nanotechnology vol.144, pp.7, 2017, https://doi.org/10.1007/s00432-018-2651-3
  4. Experience of using photodynamic therapy in the treatment of esophageal cancer vol.8, pp.2, 2017, https://doi.org/10.24931/2413-9432-2019-8-2-19-24
  5. Experience of using photodynamic therapy in the treatment of esophageal cancer vol.8, pp.2, 2017, https://doi.org/10.24931/2413-9432-2019-8-2-19-24
  6. Photodynamic enhancement of the activity of antibiotics used in urinary tract infections vol.34, pp.8, 2017, https://doi.org/10.1007/s10103-019-02730-7
  7. Antimicrobial Biophotonic Treatment of Ampicillin-Resistant Pseudomonas aeruginosa with Hypericin and Ampicillin Cotreatment Followed by Orange Light vol.11, pp.12, 2019, https://doi.org/10.3390/pharmaceutics11120641
  8. Quinoline- and Benzoselenazole-Derived Unsymmetrical Squaraine Cyanine Dyes: Design, Synthesis, Photophysicochemical Features and Light-Triggerable Antiproliferative Effects against Breast Cancer Cell vol.13, pp.11, 2017, https://doi.org/10.3390/ma13112646
  9. Cell Membrane-Inspired Polymeric Vesicles for Combined Photothermal and Photodynamic Prostate Cancer Therapy vol.12, pp.38, 2020, https://doi.org/10.1021/acsami.0c11636
  10. Considerations and Technical Pitfalls in the Employment of the MTT Assay to Evaluate Photosensitizers for Photodynamic Therapy vol.11, pp.6, 2017, https://doi.org/10.3390/app11062603
  11. Antimicrobial and antimycotic photodynamic therapy (review of literature) vol.10, pp.1, 2017, https://doi.org/10.24931/2413-9432-2021-10-1-25-31
  12. In the Search for Photocages Cleavable with Visible Light: An Overview of Recent Advances and Chemical Strategies vol.5, pp.4, 2017, https://doi.org/10.1002/cptc.202000253