Email this article THE WAYS TO OPTIMIZE CLINICAL OUTCOMES OF PHOTODYNAMIC THERAPY BY OPTICAL IMAGING TECHNIQUES
- Authors: Gamayunov S.V.1,2, Skrebtsova R.R.3,4, Korchagina K.S.5,6, Sapunov D.A.7,8, Shakhova M.A.9,10, Shakhova N.M.11,12
-
Affiliations:
- Republican Clinical Oncologic Dispensary of Ministry of Health and Social Development of the Chuvash Republic
- 31 Gladkova ul., Cheboksary, 428020, Russian Federation
- Nizhny Novgorod Regional Oncologic Clinic
- 190 Rodionova ul., Nizhny Novgorod, 603126, Russian Federation
- Moscow State University of Medicine and Dentistry named after A.I. Evdokimov
- 20–1 Delegatskaya ul., Moscow, 127473, Russian Federation
- Nizhny Novgorod Regional State Hospital named after N.A. Semashko
- 190 Rodionova ul., Nizhny Novgorod, 603126, Russian Federation
- Nizhny Novgorod State Medical Academy
- 10/1 Minina i Pozharskogo ploshchad', Nizhny Novgorod, 603005, Russian Federation
- Institute of Applied Physics of the Russian Academy of Sciences
- 46 Ul'yanova ul., Nizhny Novgorod, 603950, Russian Federation
- Issue: Vol 44, No 2 (2016)
- Pages: 148-157
- Section: ARTICLES
- URL: https://almclinmed.ru/jour/article/view/331
- DOI: https://doi.org/10.18786/2072-0505-2016-44-2-148-157
- ID: 331
Cite item
Full Text
Abstract
Background: Photodynamic therapy (PDT) is a modern minimally invasive technique for treatment of a wide range of diseases, including malignancies. One of directions for PDT development is the individualization of exposure modes that can be achieved with effective treatment monitoring. There are a number of approaches employing imaging techniques, the most promising of them being optical ones. Aim: To analyze factors affecting clinical outcomes of PDT in non-melanoma skin tumors, and to evaluate the prospects of optical imaging techniques for PDT planning and monitoring. Materials and methods: We retrospectively analyzed various aspects of the results PDT obtained in 855 patients with non-melanoma skin tumors. PDT was performed with systemic chlorine photosensitizers. As a source of irradiation, the laser at a wavelength of 662 nm was used following exposure modes: mean power density 0.3 W/cm², the laser irradiation dose of 200 J/cm² for basal cancer and 300 J/cm² for squamous cell carcinoma. Clinical evaluation was performed based on tumor response according to RECIST criteria, by the presence or absence of recurrence during long term follow up and by the presence or absence of cosmetic defects. Fluorescence imaging and optical coherence tomography were used as non-invasive imaging techniques. Results: It was found that clinical predictors of treatment failure included tumor recurrence, squamous type of tumor, and advanced exophytic or infiltrative component. Fluorescence imaging showed an association between clinical outcomes of PDT and fluorescence characteristics of the photosensitizer. The best clinical outcomes were achieved in 147 patients with a combination of high contrast fluorescence (FC>1.2) and a high degree of photobleaching of the agent (ΔIt/IN >25%): the number of complete tumor responses was 94% (138 of 147), with recurrence seen in 3 (2%) patients only with the follow up from 6 to 53 month duration. Clinical predictors of PDT cosmetic failures are tumor recurrence and tumor stage above T2. The most vulnerable zones are the outer ear and nose wings; this fact is related to an involvement of the cartilage located directly beneath the thin skin in the photodynamic reaction. This was demonstrated by optical coherence tomography. Conclusion: Presence of clinical predictors of PDT failure justifies correction of light exposure modes that can be optimally implemented with techniques for objective evaluation of the tumor borders, photosensitizer accumulation and photobleaching. Dynamic non-invasive monitoring of PDT procedure with fluorescence imaging and optical coherence tomography seems promising for implementation of an individual approach resulting in optimal oncological and functional outcomes.
About the authors
S. V. Gamayunov
Republican Clinical Oncologic Dispensary of Ministry of Health and Social Development of the Chuvash Republic; 31 Gladkova ul., Cheboksary,428020, Russian Federation
Email: natalia.shakhova@gmail.com
MD, PhD, Deputy Chief Physician on Surgery Россия
R. R. Skrebtsova
Nizhny Novgorod Regional Oncologic Clinic;190 Rodionova ul., Nizhny Novgorod, 603126, Russian Federation
Email: natalia.shakhova@gmail.com
MD, Oncologist (Surgeon) Россия
K. S. Korchagina
Moscow State University of Medicine and Dentistry named after A.I. Evdokimov; 20–1 Delegatskaya ul., Moscow, 127473, Russian Federation
Email: natalia.shakhova@gmail.com
MD, PhD Student, Chair of Pathological Anatomy Россия
D. A. Sapunov
Nizhny Novgorod Regional State Hospital named after N.A. Semashko; 190 Rodionova ul., Nizhny Novgorod, 603126, Russian Federation
Email: natalia.shakhova@gmail.com
MD, Otolaryngologist Россия
M. A. Shakhova
Nizhny Novgorod State Medical Academy; 10/1 Minina i Pozharskogo ploshchad', Nizhny Novgorod, 603005, Russian Federation
Email: natalia.shakhova@gmail.com
MD, Assistant, Chair of ENT Diseases Россия
N. M. Shakhova
Institute of Applied Physics of the Russian Academy of Sciences; 46 Ul'yanova ul., Nizhny Novgorod, 603950, Russian Federation
Author for correspondence.
Email: natalia.shakhova@gmail.com
MD, PhD, Leading Research Fellow, Laboratory of Biophotonics Россия
References
- Celli JP, Spring BQ, Rizvi I, Evans CL, Samkoe KS, Verma S, Pogue BW, Hasan T. Imaging and photodynamic therapy: mechanisms, monitoring, and optimization. Chem Rev. 2010;110(5):2795–838. doi: 10.1021/ cr900300p.
- Agostinis P, Berg K, Cengel KA, Foster TH, Girotti AW, Gollnick SO, Hahn SM, Hamblin MR, Juzeniene A, Kessel D, Korbelik M, Moan J, Mroz P, Nowis D, Piette J, Wilson BC, Golab J. Photodynamic therapy of cancer: an update. CA Cancer J Clin. 2011;61(4):250–81. doi: 10.3322/caac.20114.
- Гельфонд МЛ, Арсеньев АИ, Левченко ЕВ, Гельфонд ВМ, Мамонтов ОЮ, Моисеенко ВМ, Балдуева ИА, Новик АВ, Нехаева ТЛ, Данилова АБ, Данилов АО, Сенчик КЮ, Трунов ВА, Кульвелис ЮВ, Суханова ТЕ. Фотодинамическая терапия в комбинированном лечении злокачественных новообразований: настоящее и будущее. Лазерная медицина. 2012;16(2):25–30.
- Странадко ЕФ, Титова ВА, Петровский ВЮ. Фотодинамическая терапия: полимодальные программы лечения рака различных локализаций. Лазерная медицина. 2012;16(3):4–7.
- Allison RR, Moghissi K. Oncologic photodynamic therapy: clinical strategies that modulate mechanisms of action. Photodiagnosis Photodyn Ther. 2013;10(4):331–41. doi: 10.1016/j.pdpdt.2013.03.011.
- Allison RR, Moghissi K. Photodynamic Therapy (PDT): PDT Mechanisms. Clin Endosc. 2013;46(1):24–9. doi: 10.5946/ce.2013.46.1.24.
- Azzouzi AR, Lebdai S, Benzaghou F, Stief C. Vascular-targeted photodynamic therapy with TOOKAD® Soluble in localized prostate cancer: standardization of the procedure. World J Urol. 2015;33(7):937–44. doi: 10.1007/s00345-015- 1535-2.
- Galbán S, Brisset JC, Rehemtulla A, Chenevert TL, Ross BD, Galbán CJ. Diffusion-weighted MRI for assessment of early cancer treatment response. Curr Pharm Biotechnol. 2010;11(6):701–8. doi: 10.2174/138920110792246627.
- Fei B, Wang H, Wu C, Chiu SM. Choline PET for monitoring early tumor response to photodynamic therapy. J Nucl Med. 2010;51(1):130–8. doi: 10.2967/jnumed.109.067579.
- Madar-Balakirski N, Tempel-Brami C, Kalchenko V, Brenner O, Varon D, Scherz A, Salomon Y. Permanent occlusion of feeding arteries and draining veins in solid mouse tumors by vascular targeted photodynamic therapy (VTP) with Tookad. PLoS One. 2010;5(4):e10282. doi: 10.1371/journal.pone.0010282.
- Lee TK, Baron ED, Foster TH. Monitoring Pc 4 photodynamic therapy in clinical trials of cutaneous T-cell lymphoma using noninvasive spectroscopy. J Biomed Opt. 2008;13(3):030507. doi: 10.1117/1.2939068.
- Khurana M, Moriyama EH, Mariampillai A, Wilson BC. Intravital high-resolution optical imaging of individual vessel response to photodynamic treatment. J Biomed Opt. 2008;13(4):040502. doi: 10.1117/1.2965545.
- Standish BA, Lee KK, Jin X, Mariampillai A, Munce NR, Wood MF, Wilson BC, Vitkin IA, Yang VX. Interstitial Doppler optical coherence tomography as a local tumor necrosis predictor in photodynamic therapy of prostatic carcinoma: an in vivo study. Cancer Res. 2008;68(23):9987–95. doi: 10.1158/0008-5472. CAN-08-1128.
- Mallidi S, Watanabe K, Timerman D, Schoenfeld D, Hasan T. Prediction of tumor recurrence and therapy monitoring using ultrasound-guided photoacoustic imaging. Theranostics. 2015;5(3):289–301. doi: 10.7150/thno.10155.
- Tyrrell JS, Campbell SM, Curnow A. The relationship between protoporphyrin IX photobleaching during real-time dermatological methyl-aminolevulinate photodynamic therapy (MAL-PDT) and subsequent clinical outcome. Lasers Surg Med. 2010;42(7):613–9. doi: 10.1002/lsm.20943.
- Baran TM, Foster TH. Fluence rate-dependent photobleaching of intratumorally administered Pc 4 does not predict tumor growth delay. Photochem Photobiol. 2012;88(5):1273–9. doi: 10.1111/j.1751-1097.2012.01171.x.
- Anbil S, Rizvi I, Celli JP, Alagic N, Hasan T. A photobleaching-based PDT dose metric predicts PDT efficacy over certain BPD concentration ranges in a three-dimensional model of ovarian cancer. Proc. SPIE 8568, Optical Methods for Tumor Treatment and Detection: Mechanisms and Techniques in Photodynamic Therapy XXII, 85680S (March 13, 2013). doi: 10.1117/12.2010840. Доступно на: http://dx. doi.org/10.1117/12.2010840
- Гамаюнов СВ, Гребенкина ЕВ, Ермилина АА, Каров ВА, König K, Корчагина КС, Скребцова РР, Терехов ВМ, Терентьев ИГ, Турчин ИВ, Шахова НМ. Флюоресцентный мониторинг фотодинамической терапии рака кожи в клинической практике. Современные технологии в медицине. 2015;7(2):75–83. doi: http://dx.doi.org/10.17691/stm2015.7.2.10.
- Kruijt B, de Bruijn HS, van der Ploeg-van den Heuvel A, de Bruin RW, Sterenborg HJ, Amelink A, Robinson DJ. Monitoring ALA-induced PpIX photodynamic therapy in the rat esophagus using fluorescence and reflectance spectroscopy. Photochem Photobiol. 2008;84(6):1515–27. doi: 10.1111/j.1751- 1097.2008.00379.x.
- Sunar U, Rohrbach D, Rigual N, Tracy E, Keymel K, Cooper MT, Baumann H, Henderson BH. Monitoring photobleaching and hemodynamic responses to HPPH-mediated photodynamic therapy of head and neck cancer: a case report. Opt Express. 2010;18(14):14969–78. doi: 10.1364/OE.18.014969.
- Maas AL, Carter SL, Wileyto EP, Miller J, Yuan M, Yu G, Durham AC, Busch TM. Tumor vascular microenvironment determines responsiveness to photodynamic therapy. Cancer Res. 2012;72(8):2079–88. doi: 10.1158/0008-5472. CAN-11-3744.
- Mallidi S, Spring BQ, Chang S, Vakoc B, Hasan T. Optical Imaging, Photodynamic Therapy and Optically Triggered Combination Treatments. Cancer J. 2015;21(3):194–205. doi: 10.1097/ PPO.0000000000000117.
- Yan X, Hu H, Lin J, Jin AJ, Niu G, Zhang S, Huang P, Shen B, Chen X. Optical and photoacoustic dual-modality imaging guided synergistic photodynamic/photothermal therapies. Nanoscale. 2015;7(6):2520–6. doi: 10.1039/ c4nr06868h.
- Shanbhogue AK, Karnad AB, Prasad SR. Tumor response evaluation in oncology: current update. J Comput Assist Tomogr. 2010;34(4):479– 84. doi: 10.1097/RCT.0b013e3181db2670.
- Странадко ЕФ, Волгин ВН, Рябов МВ. Фото-динамическая терапия базально-клеточного рака кожи с применением фотогема. Клиническая дерматология и венерология. 2008;(6):28–33.
- Lee Y, Baron ED. Photodynamic therapy: current evidence and applications in dermatology. Semin Cutan Med Surg. 2011;30(4):199– 209. doi: 10.1016/j.sder.2011.08.001.
- Shirmanova MV, Gavrina AI, Aksenova NA, Glagolev NN, Solovieva AB, Shakhov BE, Zagaynova EV. Comparative study of tissue distribution of chlorin e6 complexes with amphiphilic polymers in mice with cervical carcinoma. J Anal Bioanal Tech. 2014;S1:008. doi: 10.4172/2155-9872.S1-008.
- Sliakhtsin SV, Trukhachova TV, Petrov PT, Isaakov GA, Istomin YP. Investigation of tissue biodistribution and plasma pharmacokinetics of Photolon® (Fotolon®) in intact and tumor-bearing rats. Evaluation of the ability of the photosensitizer to pass through intact histohematogenous barriers. Photodiagnosis Photodyn Ther. 2008;5 Suppl 1:S6–S7. doi: http://dx.doi. org/10.1016/S1572-1000(08)70019-X.
- Странадко ЕФ, Волгин ВН, Ламоткин ИА, Рябов МВ, Садовская МВ. Фотодинамическая терапия базально-клеточного рака кожи с фотосенсибилизатором фотодитазином. Российский биотерапевтический журнал. 2008;7(4):7–11.
- Капинус ВН, Каплан МА, Спиченкова ИС, Шубина АМ, Ярославцева-Исаева ЕВ. Фотодинамическая терапия с фотосенсибилизатором Фотолон плоскоклеточного рака кожи. Лазерная медицина. 2012;16(2):31–4.
- Mackenzie GD, Dunn JM, Selvasekar CR, Mosse CA, Thorpe SM, Novelli MR, Bown SG, Lovat LB. Optimal conditions for successful ablation of high-grade dysplasia in Barrett's oesophagus using aminolaevulinic acid photodynamic therapy. Lasers Med Sci. 2009;24(5):729–34. doi: 10.1007/s10103-008-0630-7.
- Liu B, Farrell TJ, Patterson MS. Comparison of noninvasive photodynamic therapy dosimetry methods using a dynamic model of ALA-PDT of human skin. Phys Med Biol. 2012;57(3):825– 41. doi: 10.1088/0031-9155/57/3/825. 33. Taub AF. Cosmetic clinical indications for photodynamic therapy. J Cosmet Dermatol. 2012;25(5):218–24.
Supplementary files
