Non-Cancer Effects following Ionizing Irradiation Involving the Eye and Orbit
Juliette Thariat, Arnaud Martel, Alexandre Matet, Olivier Loria, Laurent Kodjikian, Anh-Minh Nguyen, Laurence Rosier, Joël Herault, Sacha Nahon-Estève, Thibaud Mathis, Juliette Thariat, Arnaud Martel, Alexandre Matet, Olivier Loria, Laurent Kodjikian, Anh-Minh Nguyen, Laurence Rosier, Joël Herault, Sacha Nahon-Estève, Thibaud Mathis
Abstract
The eye is an exemplarily challenging organ to treat when considering ocular tumors. It is at the crossroads of several major aims in oncology: tumor control, organ preservation, and functional outcomes including vision and quality of life. The proximity between the tumor and organs that are susceptible to radiation damage explain these challenges. Given a high enough dose of radiation, virtually any cancer will be destroyed with radiotherapy. Yet, the doses inevitably absorbed by normal tissues may lead to complications, the likelihood of which increases with the radiation dose and volume of normal tissues irradiated. Precision radiotherapy allows personalized decision-making algorithms based on patient and tumor characteristics by exploiting the full knowledge of the physics, radiobiology, and the modifications made to the radiotherapy equipment to adapt to the various ocular tumors. Anticipation of the spectrum and severity of radiation-induced complications is crucial to the decision of which technique to use for a given tumor. Radiation can damage the lacrimal gland, eyelashes/eyelids, cornea, lens, macula/retina, optic nerves and chiasma, each having specific dose-response characteristics. The present review is a report of non-cancer effects that may occur following ionizing irradiation involving the eye and orbit and their specific patterns of toxicity for a given radiotherapy modality.
Keywords: brachytherapy; ocular tumor; orbit; proton beam therapy; radiation-induced adverse events; radiotherapy; toxicities.
Conflict of interest statement
The authors declare no conflict of interest.
Figures
References
- Mathis T., Cassoux N., Tardy M., Piperno S., Gastaud L., Dendale R., Maschi C., Nguyen A.-M., Meyer L., Bonnin N., et al. Management of uveal melanomas, guidelines for oncologists. Bull. Cancer. 2018;105:967–980. doi: 10.1016/j.bulcan.2018.07.011.
- Thariat J., Herault J., Mouriaux F. Conservative Treatments of Ocular Melanomas: Technology Used Wisely. Int. J. Radiat. Oncol. Biol. Phys. 2017;98:501–503. doi: 10.1016/j.ijrobp.2017.02.212.
- Thariat J., Hannoun-Levi J.-M., Sun Myint A., Vuong T., Gérard J.-P. Past, Present, and Future of Radiotherapy for the Benefit of Patients. Nat. Rev. Clin. Oncol. 2013;10:52–60. doi: 10.1038/nrclinonc.2012.203.
- Courdi A., Caujolle J.P., Grange J.D., Diallo-Rosier L., Sahel J., Bacin F., Zur C., Gastaud P., Iborra-Brassart N., Hérault J., et al. Results of Proton Therapy of Uveal Melanomas Treated in Nice. Int. J. Radiat. Oncol. Biol. Phys. 1999;45:5–11. doi: 10.1016/S0360-3016(99)00147-9.
- Paganetti H., Blakely E., Carabe-Fernandez A., Carlson D.J., Das I.J., Dong L., Grosshans D., Held K.D., Mohan R., Moiseenko V., et al. Report of the AAPM TG-256 on the Relative Biological Effectiveness of Proton Beams in Radiation Therapy. Med. Phys. 2019;46:e53–e78. doi: 10.1002/mp.13390.
- Petringa G., Calvaruso M., Conte V., Bláha P., Bravatà V., Cammarata F.P., Cuttone G., Forte G.I., Keta O., Manti L., et al. Radiobiological Outcomes, Microdosimetric Evaluations and Monte Carlo Predictions in Eye Proton Therapy. Appl. Sci. 2021;11:8822. doi: 10.3390/app11198822.
- Thariat J., Racadot S., Pointreau Y., Boisselier P., Grange J.-D., Graff P., Weber D.C. Intensity-modulated radiotherapy of head and neck cancers: Dose effects on the ocular, orbital and eyelid structures. Cancer Radiother. 2016;20:467–474. doi: 10.1016/j.canrad.2016.07.079.
- Thariat J., Grange J.-D., Mosci C., Rosier L., Maschi C., Lanza F., Nguyen A.M., Jaspart F., Bacin F., Bonnin N., et al. Visual Outcomes of Parapapillary Uveal Melanomas Following Proton Beam Therapy. Int. J. Radiat. Oncol. Biol. Phys. 2016;95:328–335. doi: 10.1016/j.ijrobp.2015.12.011.
- Espensen C.A., Appelt A.L., Fog L.S., Gothelf A.B., Thariat J., Kiilgaard J.F. Predicting Visual Acuity Deterioration and Radiation-Induced Toxicities after Brachytherapy for Choroidal Melanomas. Cancers. 2019;11:1124. doi: 10.3390/cancers11081124.
- Mazal A., Prezado Y., Ares C., de Marzi L., Patriarca A., Miralbell R., Favaudon V. FLASH and Minibeams in Radiation Therapy: The Effect of Microstructures on Time and Space and Their Potential Application to Protontherapy. Br. J. Radiol. 2020;93:20190807. doi: 10.1259/bjr.20190807.
- Favaudon V., Caplier L., Monceau V., Pouzoulet F., Sayarath M., Fouillade C., Poupon M.-F., Brito I., Hupé P., Bourhis J., et al. Ultrahigh Dose-Rate FLASH Irradiation Increases the Differential Response between Normal and Tumor Tissue in Mice. Sci. Transl. Med. 2014;6:245ra93. doi: 10.1126/scitranslmed.3008973.
- Labarbe R., Hotoiu L., Barbier J., Favaudon V. A Physicochemical Model of Reaction Kinetics Supports Peroxyl Radical Recombination as the Main Determinant of the FLASH Effect. Radiother. Oncol. 2020;153:303–310. doi: 10.1016/j.radonc.2020.06.001.
- Purdy J.A. Current ICRU Definitions of Volumes: Limitations and Future Directions. Semin. Radiat. Oncol. 2004;14:27–40. doi: 10.1053/j.semradonc.2003.12.002.
- Mathis T., Jardel P., Loria O., Delaunay B., Nguyen A.-M., Lanza F., Mosci C., Caujolle J.-P., Kodjikian L., Thariat J. New Concepts in the Diagnosis and Management of Choroidal Metastases. Prog. Retin. Eye Res. 2019;68:144–176. doi: 10.1016/j.preteyeres.2018.09.003.
- Via R., Hennings F., Fattori G., Pica A., Lomax A., Weber D.C., Baroni G., Hrbacek J. Technical Note: Benchmarking Automated Eye Tracking and Human Detection for Motion Monitoring in Ocular Proton Therapy. Med. Phys. 2020;47:2237–2241. doi: 10.1002/mp.14087.
- Antonioli L., Pella A., Ricotti R., Rossi M., Fiore M.R., Belotti G., Magro G., Paganelli C., Orlandi E., Ciocca M., et al. Convolutional Neural Networks Cascade for Automatic Pupil and Iris Detection in Ocular Proton Therapy. Sensors. 2021;21:4400. doi: 10.3390/s21134400.
- Jeganathan V.S.E., Wirth A., MacManus M.P. Ocular Risks from Orbital and Periorbital Radiation Therapy: A Critical Review. Int. J. Radiat. Oncol. Biol. Phys. 2011;79:650–659. doi: 10.1016/j.ijrobp.2010.09.056.
- Finger P.T. Radiation Therapy for Orbital Tumors: Concepts, Current Use, and Ophthalmic Radiation Side Effects. Surv. Ophthalmol. 2009;54:545–568. doi: 10.1016/j.survophthal.2009.06.004.
- Durkin S.R., Roos D., Higgs B., Casson R.J., Selva D. Ophthalmic and Adnexal Complications of Radiotherapy. Acta Ophthalmol. Scand. 2007;85:240–250. doi: 10.1111/j.1600-0420.2006.00822.x.
- Marwaha G., Macklis R., Singh A.D. Radiation Therapy: Orbital Tumors. Dev. Ophthalmol. 2013;52:94–101. doi: 10.1159/000351084.
- Espensen C.A., Kiilgaard J.F., Appelt A.L., Fog L.S., Herault J., Maschi C., Caujolle J.-P., Thariat J. Dose-Response and Normal Tissue Complication Probabilities after Proton Therapy for Choroidal Melanoma. Ophthalmology. 2021;128:152–161. doi: 10.1016/j.ophtha.2020.06.030.
- O’Neil E.C., Henderson M., Massaro-Giordano M., Bunya V.Y. Advances in Dry Eye Disease Treatment. Curr. Opin. Ophthalmol. 2019;30:166–178. doi: 10.1097/ICU.0000000000000569.
- Kennerdell J.S., Flores N.E., Hartsock R.J. Low-Dose Radiotherapy for Lymphoid Lesions of the Orbit and Ocular Adnexa. Ophthalmic Plast. Reconstr. Surg. 1999;15:129–133. doi: 10.1097/00002341-199903000-00012.
- Kim S.E., Yang H.J., Yang S.-W. Effects of Radiation Therapy on the Meibomian Glands and Dry Eye in Patients with Ocular Adnexal Mucosa-Associated Lymphoid Tissue Lymphoma. BMC Ophthalmol. 2020;20:24. doi: 10.1186/s12886-019-1301-0.
- Mombaerts I., Cameron J.D., Chanlalit W., Garrity J.A. Surgical Debulking for Idiopathic Dacryoadenitis: A Diagnosis and a Cure. Ophthalmology. 2014;121:603–609. doi: 10.1016/j.ophtha.2013.09.010.
- Koaik M., Baig K. Corneal Neurotization. Curr. Opin. Ophthalmol. 2019;30:292–298. doi: 10.1097/ICU.0000000000000578.
- Wakamatsu T.H., Sant’Anna A.E.B.P.P., Cristovam P.C., Alves V.A.F., Wakamatsu A., Gomes J.A.P. Minor Salivary Gland Transplantation for Severe Dry Eyes. Cornea. 2017;36((Suppl. 1)):S26–S33. doi: 10.1097/ICO.0000000000001358.
- Ainsbury E.A., Dalke C., Hamada N., Benadjaoud M.A., Chumak V., Ginjaume M., Kok J.L., Mancuso M., Sabatier L., Struelens L., et al. Radiation-Induced Lens Opacities: Epidemiological, Clinical and Experimental Evidence, Methodological Issues, Research Gaps and Strategy. Environ. Int. 2021;146:106213. doi: 10.1016/j.envint.2020.106213.
- Hamada N., Azizova T.V., Little M.P. An Update on Effects of Ionizing Radiation Exposure on the Eye. Br. J. Radiol. 2020;93:20190829. doi: 10.1259/bjr.20190829.
- Finger P.T. Tumour Location Affects the Incidence of Cataract and Retinopathy after Ophthalmic Plaque Radiation Therapy. Br. J. Ophthalmol. 2000;84:1068–1070. doi: 10.1136/bjo.84.9.1068.
- Seibel I., Cordini D., Hager A., Riechardt A.I., Rehak M., Böker A., Böhmer D., Heufelder J., Joussen A.M. Cataract Development in Patients Treated with Proton Beam Therapy for Uveal Melanoma. Graefe’s Arch. Clin. Exp. Ophthalmol. 2016;254:1625–1630. doi: 10.1007/s00417-016-3356-4.
- Mathis T., Rosier L., Meniai F., Baillif S., Maschi C., Herault J., Caujolle J.-P., Kodjikian L., Salleron J., Thariat J. The Lens Opacities Classification System III Grading in Irradiated Uveal Melanomas to Characterize Proton Therapy-Induced Cataracts. Am. J. Ophthalmol. 2019;201:63–71. doi: 10.1016/j.ajo.2019.01.025.
- Thariat J., Jacob S., Caujolle J.-P., Maschi C., Baillif S., Angellier G., Mathis T., Rosier L., Carnicer A., Hérault J., et al. Cataract Avoidance with Proton Therapy in Ocular Melanomas. Investig. Ophthalmol. Vis. Sci. 2017;58:5378–5386. doi: 10.1167/iovs.17-22557.
- Gragoudas E.S., Egan K.M., Arrigg P.G., Seddon J.M., Glynn R.J., Munzenrider J.E. Cataract Extraction after Proton Beam Irradiation for Malignant Melanoma of the Eye. Arch. Ophthalmol. 1992;110:475–479. doi: 10.1001/archopht.1992.01080160053029.
- The Collaborative Ocular Melanoma Study Group Incidence of Cataract and Outcomes after Cataract Surgery in the First 5 Years after Iodine 125 Brachytherapy in the Collaborative Ocular Melanoma Study: COMS Report No. 27. Ophthalmology. 2007;114:1363–1371. doi: 10.1016/j.ophtha.2006.10.039.
- Archer D.B., Amoaku W.M.K., Gardiner T.A. Radiation Retinopathy—Clinical, Histopathological, Ultrastructural and Experimental Correlations. Eye. 1991;5:239–251. doi: 10.1038/eye.1991.39.
- Mathis T., Levron A., Pommier P., Denis P., Thariat J., Kodjikian L. Intra- and Subretinal Neovascularization Following Radiation Therapy: Contribution of OCT-Angiography. J. Fr. Ophtalmol. 2018;41:e481–e483. doi: 10.1016/j.jfo.2018.04.007.
- Parsons J.T., Bova F.J., Fitzgerald C.R., Mendenhall W.M., Million R.R. Radiation Retinopathy after External-Beam Irradiation: Analysis of Time-Dose Factors. Int. J. Radiat. Oncol. Biol. Phys. 1994;30:765–773. doi: 10.1016/0360-3016(94)90347-6.
- Kaushik M., Pulido J.S., Schild S.E., Stafford S. Risk of Radiation Retinopathy in Patients with Orbital and Ocular Lymphoma. Int. J. Radiat. Oncol. Biol. Phys. 2012;84:1145–1150. doi: 10.1016/j.ijrobp.2011.12.097.
- Horgan N., Shields C.L., Mashayekhi A., Teixeira L.F., Materin M.A., Shields J.A. Early Macular Morphological Changes Following Plaque Radiotherapy for Uveal Melanoma. Retina. 2008;28:263–273. doi: 10.1097/IAE.0b013e31814b1b75.
- Marin L., Toumi E., Caujolle J.-P., Doyen J., Martel A., Nahon-Esteve S., Maschi C., Baillif S. OCT-Angiography for the Diagnosis of Radiation Maculopathy in Patients Treated with Proton Beam Therapy: A 2-Year Prospective Study. Eur. J. Ophthalmol. 2021 doi: 10.1177/11206721211067331.
- Hayreh S.S. Post-Radiation Retinopathy. A Fluorescence Fundus Angiographic Study. Br. J. Ophthalmol. 1970;54:705–714. doi: 10.1136/bjo.54.11.705.
- Shields C.L., Say E.A.T., Samara W.A., Khoo C.T.L., Mashayekhi A., Shields J.A. Optical Coherence Tomography Angiography of the Macula after Plaque Radiotherapy of Choroidal Melanoma: Comparison of Irradiated Versus Nonirradiated Eyes in 65 Patients. Retina. 2016;36:1493–1505. doi: 10.1097/IAE.0000000000001021.
- Sellam A., Coscas F., Lumbroso-Le Rouic L., Dendale R., Lupidi M., Coscas G., Desjardins L., Cassoux N. Optical Coherence Tomography Angiography of Macular Features After Proton Beam Radiotherapy for Small Choroidal Melanoma. Am. J. Ophthalmol. 2017;181:12–19. doi: 10.1016/j.ajo.2017.06.008.
- Spaide R.F., Fujimoto J.G., Waheed N.K., Sadda S.R., Staurenghi G. Optical Coherence Tomography Angiography. Prog. Retin. Eye Res. 2018;64:1–55. doi: 10.1016/j.preteyeres.2017.11.003.
- Finger P.T., Kurli M. Laser Photocoagulation for Radiation Retinopathy after Ophthalmic Plaque Radiation Therapy. Br. J. Ophthalmol. 2005;89:730–738. doi: 10.1136/bjo.2004.052159.
- Horgan N., Shields C.L., Mashayekhi A., Shields J.A. Classification and Treatment of Radiation Maculopathy. Curr. Opin. Ophthalmol. 2010;21:233–238. doi: 10.1097/ICU.0b013e3283386687.
- Veverka K.K., AbouChehade J.E., Iezzi R., Pulido J.S. NONINVASIVE GRADING OF RADIATION RETINOPATHY: The Use of Optical Coherence Tomography Angiography. Retina. 2015;35:2400–2410. doi: 10.1097/IAE.0000000000000844.
- Kinyoun J.L., Lawrence B.S., Barlow W.E. Proliferative Radiation Retinopathy. Arch. Ophthalmol. 1996;114:1097–1100. doi: 10.1001/archopht.1996.01100140299007.
- Hykin P.G., Shields C.L., Shields J.A., Arevalo J.F. The Efficacy of Focal Laser Therapy in Radiation-Induced Macular Edema. Ophthalmology. 1998;105:1425–1429. doi: 10.1016/S0161-6420(98)98023-X.
- Finger P.T., Chin K.J., Semenova E.A. Intravitreal Anti-VEGF Therapy for Macular Radiation Retinopathy: A 10-Year Study. Eur. J. Ophthalmol. 2016;26:60–66. doi: 10.5301/ejo.5000670.
- Finger P.T., Chin K.J. Intravitreous Ranibizumab (Lucentis) for Radiation Maculopathy. Arch. Ophthalmol. 2010;128:249–252. doi: 10.1001/archophthalmol.2009.376.
- Fallico M., Reibaldi M., Avitabile T., Longo A., Bonfiglio V., Chronopoulos A., Caltabiano R., Spatola C., Russo A. Intravitreal Aflibercept for the Treatment of Radiation-Induced Macular Edema after Ruthenium 106 Plaque Radiotherapy for Choroidal Melanoma. Graefe’s Arch. Clin. Exp. Ophthalmol. 2019;257:1547–1554. doi: 10.1007/s00417-019-04347-6.
- Murray T.G., Latiff A., Villegas V.M., Gold A.S. Aflibercept for Radiation Maculopathy Study: A Prospective, Randomized Clinical Study. Ophthalmol. Retin. 2019;3:561–566. doi: 10.1016/j.oret.2019.02.009.
- Frizziero L., Parrozzani R., Trainiti S., Pilotto E., Miglionico G., Pulze S., Midena E. Intravitreal Dexamethasone Implant in Radiation-Induced Macular Oedema. Br. J. Ophthalmol. 2017;101:1699–1703. doi: 10.1136/bjophthalmol-2017-310220.
- Baillif S., Maschi C., Gastaud P., Caujolle J.P. Intravitreal Dexamethasone 0.7-Mg Implant for Radiation Macular Edema after Proton Beam Therapy for Choroidal Melanoma. Retina. 2013;33:1784–1790. doi: 10.1097/IAE.0b013e31829234fa.
- Caminal J.M., Flores-Moreno I., Arias L., Gutiérrez C., Piulats J.M., Català J., Rubio M.J., Cobos E., García P., Pera J., et al. Intravitreal Dexamethasone Implant for Radiation Maculopathy Secondary to Plaque Brachytherapy in Choroidal Melanoma. Retina. 2015;35:1890–1897. doi: 10.1097/IAE.0000000000000537.
- Seibel I., Hager A., Riechardt A.I., Davids A.M., Böker A., Joussen A.M. Antiangiogenic or Corticosteroid Treatment in Patients with Radiation Maculopathy After Proton Beam Therapy for Uveal Melanoma. Am. J. Ophthalmol. 2016;168:31–39. doi: 10.1016/j.ajo.2016.04.024.
- Russo A., Reibaldi M., Avitabile T., Uva M.G., Franco L.M., Gagliano C., Bonfiglio V., Spatola C., Privitera G., Longo A. Dexamethasone Intravitreal Implant vs. Ranibizumab in the Treatment of Macular Edema Secondary to Brachytherapy for Choroidal Melanoma. Retina. 2018;38:788–794. doi: 10.1097/IAE.0000000000001585.
- Russo A., Laguardia M., Damato B. Eccentric Ruthenium Plaque Radiotherapy of Posterior Choroidal Melanoma. Graefe’s Arch. Clin. Exp. Ophthalmol. 2012;250:1533–1540. doi: 10.1007/s00417-012-1962-3.
- Caujolle J.-P., Paoli V., Chamorey E., Maschi C., Baillif S., Herault J., Gastaud P., Hannoun-Levi J.M. Local Recurrence after Uveal Melanoma Proton Beam Therapy: Recurrence Types and Prognostic Consequences. Int. J. Radiat. Oncol. Biol. Phys. 2013;85:1218–1224. doi: 10.1016/j.ijrobp.2012.10.005.
- Kim I.K., Lane A.M., Jain P., Awh C., Gragoudas E.S. Ranibizumab for the Prevention of Radiation Complications in Patients Treated with Proton Beam Irradiation for Choroidal Melanoma. Trans. Am. Ophthalmol. Soc. 2016;114:T2.
- Shields C.L., Dalvin L.A., Chang M., Mazloumi M., Fortin P., McGarrey M., Martin A., Yaghy A., Yang X., Vichitvejpaisal P., et al. Visual Outcome at 4 Years Following Plaque Radiotherapy and Prophylactic Intravitreal Bevacizumab (Every 4 Months for 2 Years) for Uveal Melanoma: Comparison with Nonrandomized Historical Control Individuals. JAMA Ophthalmol. 2020;138:136–146. doi: 10.1001/jamaophthalmol.2019.5132.
- Eandi C.M., Polito M.S., Schalenbourg A., Zografos L. Eighteen-Months Results of Intravitreal Anti-Vascular Endothelial Growth Factor on Vision and Microcirculation in Radiation Maculopathy. Retina. 2021;41:1883. doi: 10.1097/IAE.0000000000003105.
- Van der Kogel A.J. Radiation-Induced Damage in the Central Nervous System: An Interpretation of Target Cell Responses. Br. J. Cancer Suppl. 1986;7:207–217.
- Hopewell J.W., van der Kogel A.J. Pathophysiological Mechanisms Leading to the Development of Late Radiation-Induced Damage to the Central Nervous System. Front. Radiat. Ther. Oncol. 1999;33:265–275. doi: 10.1159/000061239.
- Danesh-Meyer H.V. Radiation-Induced Optic Neuropathy. J. Clin. Neurosci. 2008;15:95–100. doi: 10.1016/j.jocn.2007.09.004.
- Omary R.A., Berr S.S., Kamiryo T., Lanzino G., Kassell N.F., Lee K.S., Lopes M.B., Hillman B.J. 1995 AUR Memorial Award. Gamma Knife Irradiation-Induced Changes in the Normal Rat Brain Studied with 1H Magnetic Resonance Spectroscopy and Imaging. Acad. Radiol. 1995;2:1043–1051. doi: 10.1016/S1076-6332(05)80511-2.
- Levin L.A., Gragoudas E.S., Lessell S. Endothelial Cell Loss in Irradiated Optic Nerves. Ophthalmology. 2000;107:370–374. doi: 10.1016/S0161-6420(99)00054-8.
- Groenewald C., Konstantinidis L., Damato B. Effects of Radiotherapy on Uveal Melanomas and Adjacent Tissues. Eye. 2013;27:163–171. doi: 10.1038/eye.2012.249.
- Kline L.B., Kim J.Y., Ceballos R. Radiation Optic Neuropathy. Ophthalmology. 1985;92:1118–1126. doi: 10.1016/S0161-6420(85)33898-8.
- Yousef Y.A., Finger P.T. Optical Coherence Tomography of Radiation Optic Neuropathy. Ophthalmic Surg. Lasers Imaging. 2012;43:6–12. doi: 10.3928/15428877-20111129-09.
- Chien J.L., Sioufi K., Ferenczy S.R., Say E.A.T., Shields C.L. Optical Coherence Tomography Angiography Detects Subclinical Radial Peripapillary Capillary Density Reduction after Plaque Radiotherapy for Choroidal Melanoma. Retina. 2020;40:1774–1782. doi: 10.1097/IAE.0000000000002680.
- Kim I.K., Lane A.M., Egan K.M., Munzenrider J., Gragoudas E.S. Natural History of Radiation Papillopathy after Proton Beam Irradiation of Parapapillary Melanoma. Ophthalmology. 2010;117:1617–1622. doi: 10.1016/j.ophtha.2009.12.015.
- Martel M.K., Sandler H.M., Cornblath W.T., Marsh L.H., Hazuka M.B., Roa W.H., Fraass B.A., Lichter A.S. Dose-Volume Complication Analysis for Visual Pathway Structures of Patients with Advanced Paranasal Sinus Tumors. Int. J. Radiat. Oncol. Biol. Phys. 1997;38:273–284. doi: 10.1016/S0360-3016(97)00029-1.
- Meyer A., Lévy C., Blondel J., D’Hermies F., Frau E., Schlienger P., Mammar H., Delacroix S., Nauraye C., Desblancs C., et al. Optic neuropathy after proton-beam therapy for malignant choroidal melanoma. J. Fr. Ophtalmol. 2000;23:543–553.
- Gragoudas E.S., Li W., Lane A.M., Munzenrider J., Egan K.M. Risk Factors for Radiation Maculopathy and Papillopathy after Intraocular Irradiation. Ophthalmology. 1999;106:1571–1577; discussion 1577–1578. doi: 10.1016/S0161-6420(99)90455-4.
- Cicinelli M.V., Di Nicola M., Gigliotti C.R., Battista M., Miserocchi E., Del Vecchio A., Mortini P., Bandello F., Modorati G.M. Predictive Factors of Radio-Induced Complications in 194 Eyes Undergoing Gamma Knife Radiosurgery for Uveal Melanoma. Acta Ophthalmol. 2021;99:e1458–e1466. doi: 10.1111/aos.14814.
- De Potter P., Shields C.L., Shields J.A., Cater J.R., Brady L.W. Plaque Radiotherapy for Juxtapapillary Choroidal Melanoma. Visual Acuity and Survival Outcome. Arch. Ophthalmol. 1996;114:1357–1365. doi: 10.1001/archopht.1996.01100140557006.
- Omoti A.E., Omoti C.E. Ocular Toxicity of Systemic Anticancer Chemotherapy. Pharm. Pract. 2006;4:55–59.
- Monroe A.T., Bhandare N., Morris C.G., Mendenhall W.M. Preventing Radiation Retinopathy with Hyperfractionation. Int. J. Radiat. Oncol. Biol. Phys. 2005;61:856–864. doi: 10.1016/j.ijrobp.2004.07.664.
- Bhandare N., Monroe A.T., Morris C.G., Bhatti M.T., Mendenhall W.M. Does Altered Fractionation Influence the Risk of Radiation-Induced Optic Neuropathy? Int. J. Radiat. Oncol. Biol. Phys. 2005;62:1070–1077. doi: 10.1016/j.ijrobp.2004.12.009.
- Borruat F.-X., Schatz N.J., Giaser J.S., Matos L., Feuer W. Radiation Optic Neuropathy: Report of Cases, Role of Hyperbaric Oxygen Therapy, and Literature Review. Neuro-Ophthalmol. 1996;16:255–266. doi: 10.3109/01658109609044633.
- Finger P.T., Chin K.J. Antivascular Endothelial Growth Factor Bevacizumab for Radiation Optic Neuropathy: Secondary to Plaque Radiotherapy. Int. J. Radiat. Oncol. Biol. Phys. 2012;82:789–798. doi: 10.1016/j.ijrobp.2010.11.075.
- Roelofs K.A., Larocque M.P., Murtha A., Weis E. The Use of Intravitreal Anti-VEGF and Triamcinolone in the Treatment of Radiation Papillopathy. Ocul. Oncol. Pathol. 2018;4:395–400. doi: 10.1159/000487543.
- Shields C.L., Demirci H., Marr B.P., Mashayekhi A., Dai V.V., Materin M.A., Shields J.A. Intravitreal Triamcinolone Acetonide for Acute Radiation Papillopathy. Retina. 2006;26:537–544. doi: 10.1097/00006982-200605000-00007.
- Eckstein D., Riechardt A.I., Heufelder J., Zeitz O., Böker A., Brockmann C., Joussen A.M., Seibel I. Radiation-Induced Optic Neuropathy: Observation versus Intravitreal Treatment: Can Visual Acuity Be Maintained by Intravitreal Treatment? Am. J. Ophthalmol. 2019;208:289–294. doi: 10.1016/j.ajo.2019.07.004.
- Bensoussan E., Thariat J., Maschi C., Delas J., Schouver E.D., Hérault J., Baillif S., Caujolle J.-P. Outcomes after Proton Beam Therapy for Large Choroidal Melanomas in 492 Patients. Am. J. Ophthalmol. 2016;165:78–87. doi: 10.1016/j.ajo.2016.02.027.
- Damato B. Local Resection of Uveal Melanoma. Dev. Ophthalmol. 2012;49:66–80. doi: 10.1159/000328261.
- Konstantinidis L., Groenewald C., Coupland S.E., Damato B. Trans-Scleral Local Resection of Toxic Choroidal Melanoma after Proton Beam Radiotherapy. Br. J. Ophthalmol. 2014;98:775–779. doi: 10.1136/bjophthalmol-2013-304501.
- Mantel I., Schalenbourg A., Bergin C., Petrovic A., Weber D.C., Zografos L. Prophylactic Use of Bevacizumab to Avoid Anterior Segment Neovascularization Following Proton Therapy for Uveal Melanoma. Am. J. Ophthalmol. 2014;158:693–701.e2. doi: 10.1016/j.ajo.2014.07.002.
- Houston S.K., Shah N.V., Decatur C., Lonngi M., Feuer W., Markoe A.M., Murray T.G. Intravitreal Bevacizumab Combined with Plaque Brachytherapy Reduces Melanoma Tumor Volume and Enhances Resolution of Exudative Detachment. Clin. Ophthalmol. 2013;7:193–198. doi: 10.2147/OPTH.S37938.
- Parrozzani R., Pilotto E., Dario A., Miglionico G., Midena E. Intravitreal Triamcinolone versus Intravitreal Bevacizumab in the Treatment of Exudative Retinal Detachment Secondary to Posterior Uveal Melanoma. Am. J. Ophthalmol. 2013;155:127–133.e2. doi: 10.1016/j.ajo.2012.06.026.
- Malclès A., Nguyen A.-M., Mathis T., Grange J.-D., Kodjikian L. Intravitreal Dexamethasone Implant (Ozurdex®) for Exudative Retinal Detachment after Proton Beam Therapy for Choroidal Melanoma. Eur. J. Ophthalmol. 2017;27:596–600. doi: 10.5301/ejo.5000940.
- Campochiaro P.A., Hafiz G., Mir T.A., Scott A.W., Sophie R., Shah S.M., Ying H.S., Lu L., Chen C., Campbell J.P., et al. Pro-Permeability Factors After Dexamethasone Implant in Retinal Vein Occlusion; the Ozurdex for Retinal Vein Occlusion (ORVO) Study. Am. J. Ophthalmol. 2015;160:313–321.e19. doi: 10.1016/j.ajo.2015.04.025.
- Campochiaro P.A., Hafiz G., Mir T.A., Scott A.W., Zimmer-Galler I., Shah S.M., Wenick A.S., Brady C.J., Han I., He L., et al. Pro-Permeability Factors in Diabetic Macular Edema; the Diabetic Macular Edema Treated with Ozurdex Trial. Am. J. Ophthalmol. 2016;168:13–23. doi: 10.1016/j.ajo.2016.04.017.
- Kodjikian L., Bellocq D., Mathis T. Pharmacological Management of Diabetic Macular Edema in Real-Life Observational Studies. BioMed Res. Int. 2018;2018:8289253. doi: 10.1155/2018/8289253.
- Desjardins L., Lumbroso-Le Rouic L., Levy-Gabriel C., Dendale R., Delacroix S., Nauraye C., Estève M., Plancher C., Asselain B. Combined Proton Beam Radiotherapy and Transpupillary Thermotherapy for Large Uveal Melanomas: A Randomized Study of 151 Patients. Ophthalmic Res. 2006;38:255–260. doi: 10.1159/000094834.
- Konstantinidis L., Groenewald C., Coupland S.E., Damato B. Long-Term Outcome of Primary Endoresection of Choroidal Melanoma. Br. J. Ophthalmol. 2014;98:82–85. doi: 10.1136/bjophthalmol-2013-304022.
- Cassoux N., Cayette S., Plancher C., Lumbroso-Le Rouic L., Levy-Gabriel C., Asselain B., Sastre X., Couturier J., Arrufat S., Piperno-Neumann S., et al. Choroidal Melanoma: Does Endoresection Prevent Neovascular Glaucoma in Patient Treated with Proton Beam Irradiation? Retina. 2013;33:1441–1447. doi: 10.1097/IAE.0b013e31827f65c8.
- Van Beek J.G.M., Ramdas W.D., Angi M., van Rij C.M., Naus N.C., Kacperek A., Errington R.D., Damato B., Heimann H., Kiliç E. Local Tumour Control and Radiation Side Effects for Fractionated Stereotactic Photon Beam Radiotherapy Compared to Proton Beam Radiotherapy in Uveal Melanoma. Radiother. Oncol. 2021;157:219–224. doi: 10.1016/j.radonc.2021.01.030.
- Egan K.M., Gragoudas E.S., Seddon J.M., Glynn R.J., Munzenreider J.E., Goitein M., Verhey L., Urie M., Koehler A. The Risk of Enucleation after Proton Beam Irradiation of Uveal Melanoma. Ophthalmology. 1989;96:1377–1382; discussion 1382–1383. doi: 10.1016/S0161-6420(89)32738-2.
- Egger E., Zografos L., Schalenbourg A., Beati D., Böhringer T., Chamot L., Goitein G. Eye Retention after Proton Beam Radiotherapy for Uveal Melanoma. Int. J. Radiat. Oncol. Biol. Phys. 2003;55:867–880. doi: 10.1016/S0360-3016(02)04200-1.
- Mishra K.K., Daftari I.K., Weinberg V., Cole T., Quivey J.M., Castro J.R., Phillips T.L., Char D.H. Risk Factors for Neovascular Glaucoma after Proton Beam Therapy of Uveal Melanoma: A Detailed Analysis of Tumor and Dose-Volume Parameters. Int. J. Radiat. Oncol. Biol. Phys. 2013;87:330–336. doi: 10.1016/j.ijrobp.2013.05.051.
- Shields C.L., Shields J.A., Shields M.B., Augsburger J.J. Prevalence and Mechanisms of Secondary Intraocular Pressure Elevation in Eyes with Intraocular Tumors. Ophthalmology. 1987;94:839–846. doi: 10.1016/S0161-6420(87)33537-7.
- Ly L.V., Bronkhorst I.H.G., van Beelen E., Vrolijk J., Taylor A.W., Versluis M., Luyten G.P.M., Jager M.J. Inflammatory Cytokines in Eyes with Uveal Melanoma and Relation with Macrophage Infiltration. Investig. Ophthalmol. Vis. Sci. 2010;51:5445–5451. doi: 10.1167/iovs.10-5526.
- Boyd S.R., Tan D., Bunce C., Gittos A., Neale M.H., Hungerford J.L., Charnock-Jones S., Cree I.A. Vascular Endothelial Growth Factor Is Elevated in Ocular Fluids of Eyes Harbouring Uveal Melanoma: Identification of a Potential Therapeutic Window. Br. J. Ophthalmol. 2002;86:448–452. doi: 10.1136/bjo.86.4.448.
- Missotten G.S.O., Notting I.C., Schlingemann R.O., Zijlmans H.J., Lau C., Eilers P.H.C., Keunen J.E.E., Jager M.J. Vascular Endothelial Growth Factor a in Eyes with Uveal Melanoma. Arch. Ophthalmol. 2006;124:1428–1434. doi: 10.1001/archopht.124.10.1428.
- Daftari I.K., Char D.H., Verhey L.J., Castro J.R., Petti P.L., Meecham W.J., Kroll S., Blakely E.A. Anterior Segment Sparing to Reduce Charged Particle Radiotherapy Complications in Uveal Melanoma. Int. J. Radiat. Oncol. Biol. Phys. 1997;39:997–1010. doi: 10.1016/S0360-3016(97)00557-9.
- Hirasawa N., Tsuji H., Ishikawa H., Koyama-Ito H., Kamada T., Mizoe J.-E., Ito Y., Naganawa S., Ohnishi Y., Tsujii H. Risk Factors for Neovascular Glaucoma after Carbon Ion Radiotherapy of Choroidal Melanoma Using Dose–Volume Histogram Analysis. Int. J. Radiat. Oncol. Biol. Phys. 2007;67:538–543. doi: 10.1016/j.ijrobp.2006.08.080.
- Char D.H., Quivey J.M., Castro J.R., Kroll S., Phillips T. Helium Ions versus Iodine 125 Brachytherapy in the Management of Uveal Melanoma. A Prospective, Randomized, Dynamically Balanced Trial. Ophthalmology. 1993;100:1547–1554. doi: 10.1016/S0161-6420(93)31446-6.
- Foss A.J., Whelehan I., Hungerford J.L., Anderson D.F., Errington R.D., Kacperek A., Restori M., Kongerud J., Sheen M. Predictive Factors for the Development of Rubeosis Following Proton Beam Radiotherapy for Uveal Melanoma. Br. J. Ophthalmol. 1997;81:748–754. doi: 10.1136/bjo.81.9.748.
- Hayreh S.S. Neovascular Glaucoma. Prog. Retin. Eye Res. 2007;26:470–485. doi: 10.1016/j.preteyeres.2007.06.001.
- Bianciotto C., Shields C.L., Pirondini C., Mashayekhi A., Furuta M., Shields J.A. Proliferative Radiation Retinopathy after Plaque Radiotherapy for Uveal Melanoma. Ophthalmology. 2010;117:1005–1012. doi: 10.1016/j.ophtha.2009.10.015.
- Park U.C., Park K.H., Kim D.M., Yu H.G. Ahmed Glaucoma Valve Implantation for Neovascular Glaucoma after Vitrectomy for Proliferative Diabetic Retinopathy. J. Glaucoma. 2011;20:433–438. doi: 10.1097/IJG.0b013e3181f3eb06.
- Leszczyński R., Domański R., Formińska-Kapuścik M., Mrukwa-Kominek E., Rokita-Wala I. Contact Transscleral Cyclophotocoagulation in the Treatment of Neovascular Glaucoma: A Five-Year Follow-Up. Med. Sci. Monit. 2009;15:BR84–BR87.
- Pokroy R., Greenwald Y., Pollack A., Bukelman A., Zalish M. Visual Loss after Transscleral Diode Laser Cyclophotocoagulation for Primary Open-Angle and Neovascular Glaucoma. Ophthalmic Surg. Lasers Imaging. 2008;39:22–29. doi: 10.3928/15428877-20080101-09.
- Wakabayashi T., Oshima Y., Sakaguchi H., Ikuno Y., Miki A., Gomi F., Otori Y., Kamei M., Kusaka S., Tano Y. Intravitreal Bevacizumab to Treat Iris Neovascularization and Neovascular Glaucoma Secondary to Ischemic Retinal Diseases in 41 Consecutive Cases. Ophthalmology. 2008;115:1571–1580.e3. doi: 10.1016/j.ophtha.2008.02.026.
- Caujolle J.P., Maschi C., Freton A., Pages G., Gastaud P. Treatment of Neovascular Glaucoma after Proton Therapy for Uveal Melanomas with Ranibizumab Injection: Preliminary Results. Ophthalmic Res. 2012;47:57–60. doi: 10.1159/000328633.
- Grisanti S., Biester S., Peters S., Tatar O., Ziemssen F., Bartz-Schmidt K.U. Tuebingen Bevacizumab Study Group Intracameral Bevacizumab for Iris Rubeosis. Am. J. Ophthalmol. 2006;142:158–160. doi: 10.1016/j.ajo.2006.02.045.
- Mahdjoubi A., Najean M., Lemaitre S., Dureau S., Dendale R., Levy C., Rouic L.L.-L., Desjardins L., Cassoux N. Intravitreal Bevacizumab for Neovascular Glaucoma in Uveal Melanoma Treated by Proton Beam Therapy. Graefe’s Arch. Clin. Exp. Ophthalmol. 2018;256:411–420. doi: 10.1007/s00417-017-3834-3.
- Takihara Y., Inatani M., Kawaji T., Fukushima M., Iwao K., Iwao M., Tanihara H. Combined Intravitreal Bevacizumab and Trabeculectomy with Mitomycin C versus Trabeculectomy with Mitomycin C Alone for Neovascular Glaucoma. J. Glaucoma. 2011;20:196–201. doi: 10.1097/IJG.0b013e3181d9ce12.
- Saito Y., Higashide T., Takeda H., Ohkubo S., Sugiyama K. Beneficial Effects of Preoperative Intravitreal Bevacizumab on Trabeculectomy Outcomes in Neovascular Glaucoma. Acta Ophthalmol. 2010;88:96–102. doi: 10.1111/j.1755-3768.2009.01648.x.
- Puyo L., Paques M., Fink M., Sahel J.-A., Atlan M. Choroidal Vasculature Imaging with Laser Doppler Holography. Biomed. Opt. Express. 2019;10:995–1012. doi: 10.1364/BOE.10.000995.
- Zoberi J.E., Garcia-Ramirez J., Hedrick S., Rodriguez V., Bertelsman C.G., Mackey S., Hu Y., Gach H.M., Rao P.K., Grigsby P.W. MRI-Based Treatment Planning and Dose Delivery Verification for Intraocular Melanoma Brachytherapy. Brachytherapy. 2018;17:31–39. doi: 10.1016/j.brachy.2017.07.011.
- Fleury E., Trnková P., Erdal E., Hassan M., Stoel B., Jaarma-Coes M., Luyten G., Herault J., Webb A., Beenakker J.-W., et al. Three-Dimensional MRI-Based Treatment Planning Approach for Non-Invasive Ocular Proton Therapy. Med. Phys. 2021;48:1315–1326. doi: 10.1002/mp.14665.
- Powell B.E., Finger P.T. Anti-VEGF Therapy Immediately after Plaque Radiation Therapy Prevents or Delays Radiation Maculopathy. Ophthalmol. Retina. 2020;4:547–550. doi: 10.1016/j.oret.2020.01.010.
Source: PubMed