Skip to main content

Advertisement

SpringerLink
Log in

Comparing efficacy of charged-particle therapy with brachytherapy in treatment of uveal melanoma

  • Article
  • Published:
Eye Submit manuscript

Abstract

Background

Uveal melanoma (UM) is the most common primary ocular tumour in adults. The most used eye-preserving treatments are charged-particle therapy (CPT) and brachytherapy. We performed a systematic review and meta-analysis to compare efficacies and complications of these two radiotherapies.

Methods

We searched EMBASE, PubMed, MEDLINE, and the Cochrane Library from January 2012 to December 2022. Two independent reviewers identified controlled studies comparing outcomes of CPT versus brachytherapy. Case series that utilize either treatment modality were also reviewed.

Results

One hundred fifty studies met the eligibility criteria, including 2 randomized control trials, 5 controlled cohort studies, and 143 case series studies. We found significant reduction in local recurrence rate among patients treated with CPT compared to brachytherapy (Odds ratio[OR] 0.38, 95% Confidence interval [CI] 0.24–0.60, p < 0.01). Analysis also showed a trend of increased risks of secondary glaucoma after CPT. No statistically significant differences were found in analyzing risks of mortality, enucleation, and cataract.

Conclusions

Our study suggested no difference in mortality, enucleation rate and cataract formation rate comparing the two treatments. Lower local recurrence rate and possibly higher secondary glaucoma incidence was noted among patients treated with CPT. Nevertheless, the overall level of evidence is limited, and further high-quality studies are necessary to provide a more definitive conclusion.

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

Fig. 1: Flow diagram.
Fig. 2: OR and 95% CI of efficacy comparing CPT to brachytherapy.

Similar content being viewed by others

Data availability

This study is registered was registered with PROSPERO (ID:399075.) Extracted data are available online(link); additional requests may be made to the corresponding author.

References

  1. Shields JA, Shields CL. Intraocular Tumors: A Text and Atlas. Saunders; 1992.

  2. Diener-West M, Earle J, Fine S, Hawkins B, Moy C, Reynolds S, et al. The COMS randomized trial of iodine 125 brachytherapy for choroidal melanoma, II: characteristics of patients enrolled and not enrolled. COMS Report No. 17. Arch Ophthalmol. 2001;119:951–65.

    Article  CAS  PubMed  Google Scholar 

  3. Group TCOMS. The COMS randomized trial of iodine 125 brachytherapy for choroidal melanoma, III: initial mortality findings: COMS Report No. 18. Arch Ophthalmol. 2001;119:969–82.

    Article  Google Scholar 

  4. Ghassemi F, Sheibani S, Arjmand M, Poorbaygi H, Kouhestani E, Sabour S, et al. Comparison of iodide-125 and ruthenium-106 brachytherapy in the treatment of choroidal melanomas. Clin Ophthalmol. 2020;14:339–46.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Mairani A, Mein S, Blakely E, Debus J, Durante M, Ferrari A, et al. Roadmap: helium ion therapy. Phys Med Biol. 2022;67:15TR02.

  6. Char DH, Phillips T, Daftari I. Proton teletherapy of uveal melanoma. Int Ophthalmol Clin. 2006;46:41–49.

    Article  PubMed  Google Scholar 

  7. Tommasino F, Scifoni E, Durante M. New ions for therapy. Int J Part Ther. 2016;2:428–38.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Damato BE. Treatment selection for uveal melanoma. Dev Ophthalmol. 2012;49:16–26.

    Article  PubMed  Google Scholar 

  9. Zemba M, Dumitrescu OM, Gheorghe AG, Radu M, Ionescu MA, Vatafu A, et al. Ocular complications of radiotherapy in uveal melanoma. Cancers. 2023;15:333.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Allen AM, Pawlicki T, Dong L, Fourkal E, Buyyounouski M, Cengel K, et al. An evidence based review of proton beam therapy: the report of ASTRO’s emerging technology committee. Radiother Oncol. 2012;103:8–11.

    Article  PubMed  Google Scholar 

  11. Park JM, Kim JI, Wu HG. Technological advances in charged-particle therapy. Cancer Res Treat. 2021;53:635–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Harbour JW, Char DH, Kroll S, Quivey JM, Castro J. Metastatic risk for distinct patterns of postirradiation local recurrence of posterior uveal melanoma. Ophthalmology. 1997;104:1785–92.

    Article  CAS  PubMed  Google Scholar 

  13. Lin AJ, Rao YJ, Acharya S, Schwarz J, Rao PK, Grigsby P. Patterns of care and outcomes of proton and eye plaque brachytherapy for uveal melanoma: review of the national cancer database. Brachytherapy. 2017;16:1225–31.

    Article  PubMed  Google Scholar 

  14. Char DH, Kroll S, Phillips TL, Quivey JM. Late radiation failures after iodine 125 brachytherapy for uveal melanoma compared with charged-particle (proton or helium ion) therapy. Ophthalmology. 2002;109:1850–4.

    Article  PubMed  Google Scholar 

  15. Char DH, Quivey JM, Castro JR, Kroll S, Phillips T. Helium ions versus iodine 125 brachytherapy in the management of uveal melanoma. A prospective, randomized, dynamically balanced trial. Ophthalmology. 1993;100:1547–54.

    Article  CAS  PubMed  Google Scholar 

  16. Cumpston M, Li T, Page MJ, Chandler J, Welch VA, Higgins JP, et al. Updated guidance for trusted systematic reviews: a new edition of the Cochrane Handbook for Systematic Reviews of Interventions. Cochrane Database Syst Rev. 2019;10:Ed000142.

    PubMed  Google Scholar 

  17. Sterne JA, Hernán MA, Reeves BC, Savović J, Berkman ND, Viswanathan M, et al. ROBINS-I: a tool for assessing risk of bias in non-randomised studies of interventions. BMJ. 2016;355:i4919.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Moola S, Munn Z, Tufanaru C, Aromataris E, Sears K, Sfetcu R, et al. Chapter 7: Systematic reviews of etiology and risk. Joanna briggs institute reviewer’s manual, vol 5. The Joanna Briggs Institute; 2021. pp. 217–69.

  19. Mishra KK, Quivey JM, Daftari IK, Weinberg V, Cole TB, Patel K, et al. Long-term results of the UCSF-LBNL randomized trial: charged particle with helium ion versus iodine-125 plaque therapy for choroidal and ciliary body melanoma. Int J Radiat Oncol Biol Phys. 2015;92:376–83.

    Article  PubMed  Google Scholar 

  20. Bolling JP, Dagan R, Rutenberg M, Mamalui-Hunter M, Buskirk SJ, Heckman MG, et al. Treatment of uveal melanoma with radioactive iodine 125 implant compared with proton beam radiotherapy. Mayo Clin Proc Innov Qual Outcomes. 2022;6:27–36.

    Article  PubMed  Google Scholar 

  21. Wilson MW, Hungerford JL. Comparison of episcleral plaque and proton beam radiation therapy for the treatment of choroidal melanoma. Ophthalmology. 1999;106:1579–87.

    Article  CAS  PubMed  Google Scholar 

  22. Kowal J, Markiewicz A, Dębicka-Kumela M, Bogdali A, Jakubowska B, Karska-Basta I, et al. Analysis of local recurrence causes in uveal melanoma patients treated with (125)I brachytherapy - a single institution study. J Contemp Brachytherapy. 2019;11:554–62.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Oxenreiter MM, Lane AM, Aronow MB, Shih H, Trofimov AV, Kim IK, et al. Proton beam irradiation of uveal melanoma involving the iris, ciliary body and anterior choroid without surgical localisation (light field). Br J Ophthalmol. 2022;106:518–21.

    Article  PubMed  Google Scholar 

  24. Hussain RN, Chiu A, Pittam B, Taktak A, Damato BE, Kacperek A, et al. Proton beam radiotherapy for choroidal and ciliary body melanoma in the UK-national audit of referral patterns of 1084 cases. Eye. 2022;37:1033–6.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Guleser UY, Sarici AM, Ucar D, Gonen B, Sengul Samanci N, Özgüroğlu M. Comparison of iodine-125 plaque brachytherapy and gamma knife stereotactic radiosurgery treatment outcomes for uveal melanoma patients. Graefes Arch Clin Exp Ophthalmol. 2022;260:1337–43.

    Article  CAS  PubMed  Google Scholar 

  26. Mazzini C, Pieretti G, Vicini G, Nicolosi C, Scoccianti S, Pertici M, et al. Clinical outcomes and secondary glaucoma after gamma-knife radiosurgery and Ruthenium-106 brachytherapy for uveal melanoma: a single institution experience. Melanoma Res. 2021;31:38–48.

    Article  CAS  PubMed  Google Scholar 

  27. Cennamo G, Montorio D, D’Andrea L, Farella A, Matano E, Giuliano M, et al. Long-term outcomes in uveal melanoma after ruthenium-106 brachytherapy. Front Oncol. 2021;11:754108.

    Article  CAS  PubMed  Google Scholar 

  28. Hauzinger JA, Blatsios G, Haas G, Zehetner C, Velez-Escola L, Nowosielski Y, et al. Proton beam radiation for iris melanoma: case series and review of literature. BMJ Open Ophthalmol. 2021;6:e000683.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Fili M, Astrahan M, Stålhammar G. Long-term outcomes after enucleation or plaque brachytherapy of choroidal melanomas touching the optic disc. Brachytherapy. 2021;20:1245–56.

    Article  PubMed  Google Scholar 

  30. Sobti MM, Edington M, Connolly J, McLernon DJ, Schipani S, Ritchie D, et al. Outcomes following notched ruthenium-106 plaque brachytherapy for juxtapapillary choroidal melanomas. Ocul Oncol Pathol. 2021;7:411–7.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Marinkovic M, Pors LJ, van den Berg V, Peters FP, Schalenbourg A, Zografos L, et al. Clinical outcomes after international referral of uveal melanoma patients for proton therapy. Cancers. 2021;13:6241.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Meidenbauer K, Richards Z, Yupari RJ, Bena JF, Wilkinson A, Suh J, et al. Outcomes for posterior uveal melanoma: validation of american brachytherapy society guidelines. Brachytherapy. 2021;20:1226–34.

    Article  PubMed  Google Scholar 

  33. Zhou N, Zhang R, Liu Y, Wei W. Clinical characteristics of UM and association of metastasis of uveal melanoma with congenital oculocutaneous melanosis in asian patients: analysis of 1151 consecutive eyes. Ophthalmol Retina. 2021;5:1164–72.

    Article  PubMed  Google Scholar 

  34. Yupari RJ, Bena J, Wilkinson A, Suh J, Singh A. Small choroidal melanoma: outcomes following apical height dose brachytherapy. Br J Ophthalmol. 2021;105:1161–5.

    Article  PubMed  Google Scholar 

  35. Xu TT, Pulido JS, Deufel CL, Corbin KS, Petersen IA, Dalvin LA. Clinical outcomes of Modified Collaborative Ocular Melanoma Study IRIS plaques for treatment of iris, iridociliary, and ciliary body melanoma. Eye. 2021;35:2754–62.

    Article  PubMed  Google Scholar 

  36. Jampol LM, Moy CS, Murray TG, Reynolds SM, Albert DM, Schachat AP, et al. The COMS randomized trial of iodine 125 brachytherapy for choroidal melanoma: IV. Local treatment failure and enucleation in the first 5 years after brachytherapy. COMS Report No. 19. Ophthalmology. 2020;127:S148–s157.

    Article  PubMed  Google Scholar 

  37. Jung SK, Park YH, Shin DH, Kim HS, Jung JH, Kim TH, et al. Visual outcomes of proton beam therapy for choroidal melanoma at a single institute in the Republic of Korea. PLoS ONE. 2020;15:e0242966.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Filì M, Trocme E, Bergman L, See TRO, André H, Bartuma K, et al. Ruthenium-106 versus iodine-125 plaque brachytherapy of 571 choroidal melanomas with a thickness of ≥5.5 mm. Br J Ophthalmol. 2020;104:26–32.

    Article  PubMed  Google Scholar 

  39. Jiang P, Purtskhvanidze K, Kandzia G, Neumann D, Luetzen U, Siebert FA, et al. (106)Ruthenium eye plaque brachytherapy in the management of medium sized uveal melanoma. Radiat Oncol. 2020;15:183.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Riechardt AI, Stroux A, Seibel I, Heufelder J, Zeitz O, Böhmer D, et al. Side effects of proton beam therapy of choroidal melanoma in dependence of the dose to the optic disc and the irradiated length of the optic nerve. Graefes Arch Clin Exp Ophthalmol. 2020;258:2523–33.

    Article  PubMed  Google Scholar 

  41. Stålhammar G. Forty-year prognosis after plaque brachytherapy of uveal melanoma. Sci Rep. 2020;10:11297.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Toutée A, Angi M, Dureau S, Lévy-Gabriel C, Rouic LL, Dendale R, et al. Long-term visual outcomes for small uveal melanoma staged T1 treated by proton beam radiotherapy. Cancers. 2019;11:1047.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Espensen CA, Appelt AL, Fog LS, Gothelf AB, Thariat J, Kiilgaard JF. Predicting visual acuity deterioration and radiation-induced toxicities after brachytherapy for choroidal melanomas. Cancers. 2019;11:1124.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. King BA, Awh C, Gao BT, Wang J, Kocak M, Morales-Tirado VM, et al. Iodine-125 episcleral plaque brachytherapy for AJCC T4 posterior uveal melanoma: clinical outcomes in 158 patients. Ocul Oncol Pathol. 2019;5:340–9.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Stålhammar G, See TR, Filì M, Seregard S. No gender differences in long-term survival after brachytherapy of 1,541 patients with uveal melanoma. Ocul Oncol Pathol. 2019;5:432–9.

    Article  PubMed  PubMed Central  Google Scholar 

  46. AlMahmoud T, Quinlan-Davidson S, Pond GR, Deschênes J. Outcome analysis of visual acuity and side effect after ruthenium-106 plaque brachytherapy for medium-sized choroidal melanoma. Middle East Afr J Ophthalmol. 2018;25:103–7.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Danish H, Ferris MJ, Balagamwala E, Switchenko JM, Patel KR, Choudhary M, et al. Comparative outcomes and toxicities for ruthenium-106 versus palladium-103 in the treatment of choroidal melanoma. Melanoma Res. 2018;28:120–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Seibel I, Riechardt AI, Erb-Eigner K, Böker A, Cordini D, Heufelder J, et al. Proton beam irradiation: a safe procedure in postequatorial extraocular extension from uveal melanoma. Am J Ophthalmol. 2018;191:49–53.

    Article  PubMed  Google Scholar 

  49. Le BHA, Kim JW, Deng H, Rayess N, Jennelle RL, Zhou SY, et al. Outcomes of choroidal melanomas treated with eye physics plaques: A 25-year review. Brachytherapy. 2018;17:981–9.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Miguel D, de Frutos-Baraja JM, López-Lara F, Saornil MA, García-Álvarez C, Alonso P, et al. Radiobiological doses, tumor, and treatment features influence on outcomes after epiescleral brachytherapy. A 20-year retrospective analysis from a single-institution: part II. J Contemp Brachytherapy. 2018;10:347–59.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Oellers P, Mowery YM, Perez BA, Stinnett S, Mettu P, Vajzovic L, et al. Efficacy and safety of low-dose iodine plaque brachytherapy for juxtapapillary choroidal melanoma. Am J Ophthalmol. 2018;186:32–40.

    Article  PubMed  Google Scholar 

  52. Pagliara MM, Tagliaferri L, Azario L, Lenkowicz J, Lanza A, Autorino R, et al. Ruthenium brachytherapy for uveal melanomas: Factors affecting the development of radiation complications. Brachytherapy. 2018;17:432–8.

    Article  PubMed  Google Scholar 

  53. Shields CL, Sioufi K, Srinivasan A, Di Nicola M, Masoomian B, Barna LE, et al. Visual outcome and millimeter incremental risk of metastasis in 1780 patients with small choroidal melanoma managed by plaque radiotherapy. JAMA Ophthalmol. 2018;136:1325–33.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Aziz HA, Al Zahrani YA, Bena J, Lorek B, Wilkinson A, Suh J, et al. Episcleral brachytherapy of uveal melanoma: role of intraoperative echographic confirmation. Br J Ophthalmol. 2017;101:747–51.

    Article  PubMed  Google Scholar 

  55. Bellerive C, Aziz HA, Bena J, Wilkinson A, Suh JH, Plesec T, et al. Local failure after episcleral brachytherapy for posterior uveal melanoma: patterns, risk factors, and management. Am J Ophthalmol. 2017;177:9–16.

    Article  PubMed  Google Scholar 

  56. Hegde JV, McCannel TA, McCannel CA, Lamb J, Wang PC, Veruttipong D, et al. Juxtapapillary and circumpapillary choroidal melanoma: globe-sparing treatment outcomes with iodine-125 notched plaque brachytherapy. Graefes Arch Clin Exp Ophthalmol. 2017;255:1843–50.

    Article  PubMed  Google Scholar 

  57. Papakostas TD, Lane AM, Morrison M, Gragoudas ES, Kim IK. Long-term outcomes after proton beam irradiation in patients with large choroidal melanomas. JAMA Ophthalmol. 2017;135:1191–6.

    Article  PubMed  PubMed Central  Google Scholar 

  58. Patel KR, Prabhu RS, Switchenko JM, Chowdhary M, Craven C, Mendoza P, et al. Visual acuity, oncologic, and toxicity outcomes with (103)Pd vs. (125)I plaque treatment for choroidal melanoma. Brachytherapy. 2017;16:646–53.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Riechardt AI, Karle B, Cordini D, Heufelder J, Budach V, Joussen AM, et al. Proton therapy of iris melanoma with 50 CGE : Influence of target volume on clinical outcome. Strahlenther Onkol. 2017;193:943–50.

    Article  PubMed  Google Scholar 

  60. Rospond-Kubiak I, Wróblewska-Zierhoffer M, Twardosz-Pawlik H, Kocięcki J. Ruthenium brachytherapy for uveal melanoma - single institution experience. J Contemp Brachytherapy. 2017;9:548–52.

    Article  PubMed  PubMed Central  Google Scholar 

  61. Tagliaferri L, Pagliara MM, Masciocchi C, Scupola A, Azario L, Grimaldi G, et al. Nomogram for predicting radiation maculopathy in patients treated with Ruthenium-106 plaque brachytherapy for uveal melanoma. J Contemp Brachytherapy. 2017;9:540–7.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Zewar A, Nawaiseh I, Jaradat I, Khzouz J, Alrawashdeh K, Abdeen G, et al. Management and outcome of uveal melanoma in a single tertiary cancer center in Jordan. Turk Patoloji Derg. 2016;32:186–92.

    PubMed  Google Scholar 

  63. Belaïd A, Nasr C, Jmour O, Cherif A, Kochbati L, Bouguila H, et al. Brachytherapy of uveal melanomas with ruthenium-106 plaques. Asian Pac J Cancer Prev. 2016;17:5281–5.

    PubMed  PubMed Central  Google Scholar 

  64. Bensoussan E, Thariat J, Maschi C, Delas J, Schouver ED, Hérault J, et al. Outcomes after proton beam therapy for large choroidal melanomas in 492 patients. Am J Ophthalmol. 2016;165:78–87.

    Article  PubMed  Google Scholar 

  65. Caminal JM, Padrón-Pérez N, Arias L, Masuet-Aumatell C, Gutiérrez C, Piulats JM, et al. Transscleral resection without hypotensive anaesthesia vs iodine-125 plaque brachytherapy in the treatment of choroidal melanoma. Eye. 2016;30:833–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Thariat J, Grange JD, Mosci C, Rosier L, Maschi C, Lanza F, et al. Visual outcomes of parapapillary uveal melanomas following proton beam therapy. Int J Radiat Oncol Biol Phys. 2016;95:328–35.

    Article  PubMed  Google Scholar 

  67. Marinkovic M, Horeweg N, Fiocco M, Peters FP, Sommers LW, Laman MS, et al. Ruthenium-106 brachytherapy for choroidal melanoma without transpupillary thermotherapy: Similar efficacy with improved visual outcome. Eur J Cancer. 2016;68:106–13.

    Article  CAS  PubMed  Google Scholar 

  68. Naseripour M, Jaberi R, Sedaghat A, Azma Z, Nojomi M, Falavarjani KG, et al. Ruthenium-106 brachytherapy for thick uveal melanoma: reappraisal of apex and base dose radiation and dose rate. J Contemp Brachytherapy. 2016;8:66–73.

    Article  PubMed  PubMed Central  Google Scholar 

  69. Wisely CE, Hadziahmetovic M, Reem RE, Hade EM, Nag S, Davidorf FH, et al. Long-term visual acuity outcomes in patients with uveal melanoma treated with 125I episcleral OSU-Nag plaque brachytherapy. Brachytherapy. 2016;15:12–22.

    Article  PubMed  PubMed Central  Google Scholar 

  70. Weber B, Paton K, Ma R, Pickles T. Outcomes of proton beam radiotherapy for large non-peripapillary choroidal and ciliary body melanoma at TRIUMF and the BC cancer agency. Ocul Oncol Pathol. 2015;2:29–35.

    Article  PubMed  PubMed Central  Google Scholar 

  71. Browne AW, Dandapani SV, Jennelle R, Stevanovic M, Lee TC, Murphree AL, et al. Outcomes of medium choroidal melanomas treated with ruthenium brachytherapy guided by three-dimensional pretreatment modeling. Brachytherapy. 2015;14:718–25.

    Article  PubMed  Google Scholar 

  72. Fili M, Lundell G, Lundell M, Seregard S. High dose rate and low dose rate ruthenium brachytherapy for uveal melanoma. No association with ocular outcome. Br J Ophthalmol. 2014;98:1349–54.

    Article  CAS  PubMed  Google Scholar 

  73. Jancar B, Budihna M, Drnovsek-Olup B, Andrejcic KN, Zupancic IB, Pahor D. Prognostic factors of choroidal melanoma in Slovenia, 1986-2008. Radio Oncol. 2016;50:104–12.

    Article  Google Scholar 

  74. Seibel I, Cordini D, Rehak M, Hager A, Riechardt AI, Böker A, et al. Local recurrence after primary proton beam therapy in uveal melanoma: risk factors, retreatment approaches, and outcome. Am J Ophthalmol. 2015;160:628–36.

    Article  PubMed  Google Scholar 

  75. Sikuade MJ, Salvi S, Rundle PA, Errington DG, Kacperek A, Rennie IG. Outcomes of treatment with stereotactic radiosurgery or proton beam therapy for choroidal melanoma. Eye. 2015;29:1194–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Tarmann L, Wackernagel W, Avian A, Mayer C, Schneider M, Winkler P, et al. Ruthenium-106 plaque brachytherapy for uveal melanoma. Br J Ophthalmol. 2015;99:1644–9.

    Article  PubMed  Google Scholar 

  77. Takiar V, Voong KR, Gombos DS, Mourtada F, Rechner LA, Lawyer AA, et al. A choice of radionuclide: Comparative outcomes and toxicity of ruthenium-106 and iodine-125 in the definitive treatment of uveal melanoma. Pract Radiat Oncol. 2015;5:e169–e176.

    Article  PubMed  Google Scholar 

  78. Vonk DT, Kim Y, Javid C, Gordon JD, Stea B. Prescribing to tumor apex in episcleral plaque iodine-125 brachytherapy for medium-sized choroidal melanoma: a single-institutional retrospective review. Brachytherapy. 2015;14:726–33.

    Article  PubMed  Google Scholar 

  79. Petrovic A, Bergin C, Schalenbourg A, Goitein G, Zografos L. Proton therapy for uveal melanoma in 43 juvenile patients: long-term results. Ophthalmology. 2014;121:898–904.

    Article  PubMed  Google Scholar 

  80. Rahmi A, Mammar H, Thariat J, Angellier G, Herault J, Chauvel P, et al. Proton beam therapy for presumed and confirmed iris melanomas: a review of 36 cases. Graefes Arch Clin Exp Ophthalmol. 2014;252:1515–21.

    Article  CAS  PubMed  Google Scholar 

  81. Badiyan SN, Rao RC, Apicelli AJ, Acharya S, Verma V, Garsa AA, et al. Outcomes of iodine-125 plaque brachytherapy for uveal melanoma with intraoperative ultrasonography and supplemental transpupillary thermotherapy. Int J Radiat Oncol Biol Phys. 2014;88:801–5.

    Article  PubMed  Google Scholar 

  82. Barker CA, Francis JH, Cohen GN, Marr BP, Wolden SL, McCormick B, et al. (106)Ru plaque brachytherapy for uveal melanoma: factors associated with local tumor recurrence. Brachytherapy. 2014;13:584–90.

    Article  PubMed  PubMed Central  Google Scholar 

  83. Perez BA, Mettu P, Vajzovic L, Rivera D, Alkaissi A, Steffey BA, et al. Uveal melanoma treated with iodine-125 episcleral plaque: an analysis of dose on disease control and visual outcomes. Int J Radiat Oncol Biol Phys. 2014;89:127–36.

    Article  PubMed  PubMed Central  Google Scholar 

  84. Sagoo MS, Shields CL, Emrich J, Mashayekhi A, Komarnicky L, Shields JA. Plaque radiotherapy for juxtapapillary choroidal melanoma: treatment complications and visual outcomes in 650 consecutive cases. JAMA Ophthalmol. 2014;132:697–702.

    Article  PubMed  Google Scholar 

  85. Salkola S, Heikkonen J, Eskelin S, Kivelä T. Management of choroidal melanomas less than 10 mm in largest basal diameter with a 10-mm ruthenium plaque. Retina. 2014;34:2110–20.

    Article  PubMed  Google Scholar 

  86. Sandinha MT, Kacperek A, Errington RD, Coupland SE, Damato B. Recurrence of iris melanoma after proton beam therapy. Br J Ophthalmol. 2014;98:484–7.

    Article  PubMed  Google Scholar 

  87. Wagner A, Chen A, Cook T, Faber D, Winward K, Sause W. Outcomes and control rates for I-125 plaque brachytherapy for uveal melanoma: a community-based institutional experience. ISRN Ophthalmol. 2014;2014:950975.

    Article  PubMed  PubMed Central  Google Scholar 

  88. Berry JL, Dandapani SV, Stevanovic M, Lee TC, Astrahan M, Murphree AL, et al. Outcomes of choroidal melanomas treated with eye physics: a 20-year review. JAMA Ophthalmol. 2013;131:1435–42.

    Article  PubMed  Google Scholar 

  89. Caminal JM, Mejia K, Masuet-Aumatell C, Arias L, Piulats JM, Gutierrez C, et al. Endoresection versus iodine-125 plaque brachytherapy for the treatment of choroidal melanoma. Am J Ophthalmol. 2013;156:334–42.e331.

    Article  PubMed  Google Scholar 

  90. Caujolle JP, Paoli V, Chamorey E, Maschi C, Baillif S, Herault J, et al. Local recurrence after uveal melanoma proton beam therapy: recurrence types and prognostic consequences. Int J Radiat Oncol Biol Phys. 2013;85:1218–24.

    Article  PubMed  Google Scholar 

  91. Konstantinidis L, Roberts D, Errington RD, Kacperek A, Damato B. Whole anterior segment proton beam radiotherapy for diffuse iris melanoma. Br J Ophthalmol. 2013;97:471–4.

    Article  PubMed  Google Scholar 

  92. Krema H, Heydarian M, Beiki-Ardakani A, Weisbrod D, Xu W, Laperriere NJ, et al. Dosimetric and late radiation toxicity comparison between iodine-125 brachytherapy and stereotactic radiation therapy for juxtapapillary choroidal melanoma. Int J Radiat Oncol Biol Phys. 2013;86:510–5.

    Article  PubMed  Google Scholar 

  93. Marconi DG, de Castro DG, Rebouças LM, Bernardes Gil GO, Fogaroli RC, Conte Maia MA, et al. Tumor control, eye preservation, and visual outcomes of ruthenium plaque brachytherapy for choroidal melanoma. Brachytherapy. 2013;12:235–9.

    Article  PubMed  Google Scholar 

  94. Mishra KK, Daftari IK, Weinberg V, Cole T, Quivey JM, Castro JR, et al. 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.

    Article  PubMed  Google Scholar 

  95. Murray TG, Markoe AM, Gold AS, Ehlies F, Bermudez E, Wildner A, et al. Long-term followup comparing two treatment dosing strategies of (125) I plaque radiotherapy in the management of small/medium posterior uveal melanoma. J Ophthalmol. 2013;2013:517032.

    Article  PubMed  PubMed Central  Google Scholar 

  96. Quinlan-Davidson S, AlMahmoud T, Shenouda G, Evans M, Mansour M, Edelstein C, et al. Intraoperative sonographically assisted radioactive iodine 125 plaque brachytherapy for choroidal melanoma: visual acuity outcome. J Ultrasound Med. 2013;32:995–1001.

    Article  PubMed  Google Scholar 

  97. Toyama S, Tsuji H, Mizoguchi N, Nomiya T, Kamada T, Tokumaru S, et al. Long-term results of carbon ion radiation therapy for locally advanced or unfavorably located choroidal melanoma: usefulness of CT-based 2-port orthogonal therapy for reducing the incidence of neovascular glaucoma. Int J Radiat Oncol Biol Phys. 2013;86:270–6.

    Article  PubMed  Google Scholar 

  98. Desjardins L, Lumbroso-Le Rouic L, Levy-Gabriel C, Cassoux N, Dendale R, Mazal A, et al. Treatment of uveal melanoma by accelerated proton beam. Dev Ophthalmol. 2012;49:41–57.

    Article  PubMed  Google Scholar 

  99. Finger PT, Chin KJ, Tena LB. A five-year study of slotted eye plaque radiation therapy for choroidal melanoma: near, touching, or surrounding the optic nerve. Ophthalmology. 2012;119:415–22.

    Article  PubMed  Google Scholar 

  100. García-Álvarez C, Saornil MA, López-Lara F, Almaraz A, Muñoz MF, Frutos-Baraja J, et al. Episcleral brachytherapy for uveal melanoma: analysis of 136 cases. Clin Transl Oncol. 2012;14:350–5.

    Article  PubMed  Google Scholar 

  101. Perri P, Fiorica F, D’Angelo S, Lamberti G, Parmeggiani F, Martini A, et al. Ruthenium-106 eye plaque brachytherapy in the conservative treatment of uveal melanoma: a mono-institutional experience. Eur Rev Med Pharm Sci. 2012;16:1919–24.

    CAS  Google Scholar 

  102. Russo A, Laguardia M, Damato B. Eccentric ruthenium plaque radiotherapy of posterior choroidal melanoma. Graefes Arch Clin Exp Ophthalmol. 2012;250:1533–40.

    Article  PubMed  Google Scholar 

  103. Tran E, Ma R, Paton K, Blackmore E, Pickles T. Outcomes of proton radiation therapy for peripapillary choroidal melanoma at the BC Cancer Agency. Int J Radiat Oncol Biol Phys. 2012;83:1425–31.

    Article  PubMed  Google Scholar 

  104. Yarovoy AA, Magaramov DA, Bulgakova ES. The comparison of ruthenium brachytherapy and simultaneous transpupillary thermotherapy of choroidal melanoma with brachytherapy alone. Brachytherapy. 2012;11:224–9.

    Article  PubMed  Google Scholar 

  105. Karlovits B, Trombetta MG, Verstraeten T, Johnson M, Wong M, Karlovits S. Local control and visual acuity following treatment of medium-sized ocular melanoma using a contact eye plaque: a single surgeon experience. Brachytherapy. 2011;10:228–31.

    Article  PubMed  Google Scholar 

  106. Lane AM, Kim IK, Gragoudas ES. Proton irradiation for peripapillary and parapapillary melanomas. Arch Ophthalmol. 2011;129:1127–30.

    Article  PubMed  Google Scholar 

  107. Leonard KL, Gagne NL, Mignano JE, Duker JS, Bannon EA, Rivard MJ. A 17-year retrospective study of institutional results for eye plaque brachytherapy of uveal melanoma using (125)I, (103)Pd, and (131)Cs and historical perspective. Brachytherapy. 2011;10:331–9.

    Article  PubMed  Google Scholar 

  108. Macdonald EC, Cauchi P, Kemp EG. Proton beam therapy for the treatment of uveal melanoma in Scotland. Br J Ophthalmol. 2011;95:1691–5.

    Article  PubMed  Google Scholar 

  109. Papageorgiou KI, Cohen VM, Bunce C, Kinsella M, Hungerford JL. Predicting local control of choroidal melanomas following 106Ru plaque brachytherapy. Br J Ophthalmol. 2011;95:166–70.

    Article  CAS  PubMed  Google Scholar 

  110. Bianciotto C, Shields CL, Pirondini C, Mashayekhi A, Furuta M, Shields JA. Proliferative radiation retinopathy after plaque radiotherapy for uveal melanoma. Ophthalmology. 2010;117:1005–12.

    Article  PubMed  Google Scholar 

  111. Caujolle JP, Mammar H, Chamorey E, Pinon F, Herault J, Gastaud P. Proton beam radiotherapy for uveal melanomas at nice teaching hospital: 16 years’ experience. Int J Radiat Oncol Biol Phys. 2010;78:98–103.

    Article  PubMed  Google Scholar 

  112. Daftari IK, Mishra KK, O’Brien JM, Tsai T, Park SS, Sheen M, et al. Fundus image fusion in EYEPLAN software: an evaluation of a novel technique for ocular melanoma radiation treatment planning. Med Phys. 2010;37:5199–207.

    Article  PubMed  Google Scholar 

  113. Gündüz K, Kurt RA, Akmeşe HE, Köse K, Uçakhan-Gündüz O. Ruthenium-106 plaque radiotherapy alone or in combination with transpupillary thermotherapy in the management of choroidal melanoma. Jpn J Ophthalmol. 2010;54:338–43.

    Article  PubMed  Google Scholar 

  114. Gündüz AK, Mirzayev I. Secondary endoresection for previously treated choroidal melanomas with a non-responsive course and persistent exudative retinal detachment. Int J Ophthalmol. 2022;15:276–83.

    Article  PubMed  PubMed Central  Google Scholar 

  115. Saconn PA, Gee CJ, Greven CM, McCoy TP, Ekstrand KE, Greven KM. Alternative dose for choroidal melanoma treated with an iodine-125 radioactive plaque: a single-institution retrospective study. Int J Radiat Oncol Biol Phys. 2010;78:844–8.

    Article  CAS  PubMed  Google Scholar 

  116. Verschueren KM, Creutzberg CL, Schalij-Delfos NE, Ketelaars M, Klijsen FL, Haeseker BI, et al. Long-term outcomes of eye-conserving treatment with Ruthenium(106) brachytherapy for choroidal melanoma. Radiother Oncol. 2010;95:332–8.

    Article  PubMed  Google Scholar 

  117. Aziz S, Taylor A, McConnachie A, Kacperek A, Kemp E. Proton beam radiotherapy in the management of uveal melanoma: clinical experience in Scotland. Clin Ophthalmol. 2009;3:49–55.

    PubMed  PubMed Central  Google Scholar 

  118. Correa R, Pera J, Gómez J, Polo A, Gutiérrez C, Caminal JM, et al. (125)I episcleral plaque brachytherapy in the treatment of choroidal melanoma: a single-institution experience in Spain. Brachytherapy. 2009;8:290–6.

    Article  PubMed  Google Scholar 

  119. Frenkel S, Hendler K, Pe’er J. Uveal melanoma in Israel in the last two decades: characterization, treatment and prognosis. Isr Med Assoc J. 2009;11:280–5.

    PubMed  Google Scholar 

  120. Kaiserman N, Kaiserman I, Hendler K, Frenkel S, Pe’er J. Ruthenium-106 plaque brachytherapy for thick posterior uveal melanomas. Br J Ophthalmol. 2009;93:1167–71.

    Article  CAS  PubMed  Google Scholar 

  121. Mosci C, Mosci S, Barla A, Squarcia S, Chauvel P, Iborra N. Proton beam radiotherapy of uveal melanoma: Italian patients treated in Nice, France. Eur J Ophthalmol. 2009;19:654–60.

    Article  PubMed  Google Scholar 

  122. Krohn J, Monge OR, Skorpen TN, Mørk SJ, Dahl O. Posterior uveal melanoma treated with I-125 brachytherapy or primary enucleation. Eye. 2008;22:1398–403.

    Article  CAS  PubMed  Google Scholar 

  123. Sagoo MS, Shields CL, Mashayekhi A, Freire J, Emrich J, Reiff J, et al. Plaque radiotherapy for juxtapapillary choroidal melanoma overhanging the optic disc in 141 consecutive patients. Arch Ophthalmol. 2008;126:1515–22.

    Article  PubMed  Google Scholar 

  124. Mossböck G, Rauscher T, Winkler P, Kapp KS, Langmann G. Impact of dose rate on clinical course in uveal melanoma after brachytherapy with ruthenium-106. Strahlenther Onkol. 2007;183:571–5.

    Article  PubMed  Google Scholar 

  125. Sagoo MS, Shields CL, Mashayekhi A, Freire J, Emrich J, Reiff J, et al. Plaque radiotherapy for choroidal melanoma encircling the optic disc (circumpapillary choroidal melanoma). Arch Ophthalmol. 2007;125:1202–9.

    Article  PubMed  Google Scholar 

  126. Dendale R, Lumbroso-Le Rouic L, Noel G, Feuvret L, Levy C, Delacroix S, et al. Proton beam radiotherapy for uveal melanoma: results of Curie Institut-Orsay proton therapy center (ICPO). Int J Radiat Oncol Biol Phys. 2006;65:780–7.

    Article  PubMed  Google Scholar 

  127. Isager P, Ehlers N, Urbak SF, Overgaard J. Visual outcome, local tumour control, and eye preservation after 106Ru/Rh brachytherapy for choroidal melanoma. Acta Oncol. 2006;45:285–93.

    Article  PubMed  Google Scholar 

  128. Puusaari I, Damato B, Kivelä T. Transscleral local resection versus iodine brachytherapy for uveal melanomas that are large because of tumour height. Graefes Arch Clin Exp Ophthalmol. 2007;245:522–33.

    Article  PubMed  Google Scholar 

  129. Bergman L, Nilsson B, Lundell G, Lundell M, Seregard S. Ruthenium brachytherapy for uveal melanoma, 1979-2003: survival and functional outcomes in the Swedish population. Ophthalmology. 2005;112:834–40.

    Article  PubMed  Google Scholar 

  130. Damato B, Patel I, Campbell IR, Mayles HM, Errington RD. Local tumor control after 106Ru brachytherapy of choroidal melanoma. Int J Radiat Oncol Biol Phys. 2005;63:385–91.

    Article  PubMed  Google Scholar 

  131. Damato B, Kacperek A, Chopra M, Campbell IR, Errington RD. Proton beam radiotherapy of choroidal melanoma: the Liverpool-Clatterbridge experience. Int J Radiat Oncol Biol Phys. 2005;62:1405–11.

    Article  PubMed  Google Scholar 

  132. Jensen AW, Petersen IA, Kline RW, Stafford SL, Schomberg PJ, Robertson DM. Radiation complications and tumor control after 125I plaque brachytherapy for ocular melanoma. Int J Radiat Oncol Biol Phys. 2005;63:101–8.

    Article  PubMed  Google Scholar 

  133. Lotayef MM, Othman IS, Shelil AE, Kerima H. Ru106 brachytherapy for management of choroidal melanoma: do we need to adjust total dose according to the new NIST calibration measurement? J Egypt Natl Canc Inst. 2005;17:211–7.

    PubMed  Google Scholar 

  134. Stack R, Elder M, Abdelaal A, Hidajat R, Clemett R. New Zealand experience of I125 brachytherapy for choroidal melanoma. Clin Exp Ophthalmol. 2005;33:490–4.

    Article  PubMed  Google Scholar 

  135. Egger E, Zografos L, Schalenbourg A, Beati D, Böhringer T, Chamot L, et al. Eye retention after proton beam radiotherapy for uveal melanoma. Int J Radiat Oncol Biol Phys. 2003;55:867–80.

    Article  PubMed  Google Scholar 

  136. Georgopoulos M, Zehetmayer M, Ruhswurm I, Toma-Bstaendig S, Ségur-Eltz N, Sacu S, et al. Tumour regression of uveal melanoma after ruthenium-106 brachytherapy or stereotactic radiotherapy with gamma knife or linear accelerator. Ophthalmologica. 2003;217:315–9.

    Article  PubMed  Google Scholar 

  137. Novak-Andrejcic K, Jancar B, Hawlina M. Echographic follow-up of malignant melanoma of the choroid after brachytherapy with 106Ru. Klin Monbl Augenheilkd. 2003;220:853–60.

    Article  PubMed  Google Scholar 

  138. Gragoudas ES, Lane AM, Munzenrider J, Egan KM, Li W. Long-term risk of local failure after proton therapy for choroidal/ciliary body melanoma. Trans Am Ophthalmol Soc. 2002;100:43–48.

    PubMed  PubMed Central  Google Scholar 

  139. Egger E, Schalenbourg A, Zografos L, Bercher L, Boehringer T, Chamot L, et al. Maximizing local tumor control and survival after proton beam radiotherapy of uveal melanoma. Int J Radiat Oncol Biol Phys. 2001;51:138–47.

    Article  CAS  PubMed  Google Scholar 

  140. Fuss M, Loredo LN, Blacharski PA, Grove RI, Slater JD. Proton radiation therapy for medium and large choroidal melanoma: preservation of the eye and its functionality. Int J Radiat Oncol Biol Phys. 2001;49:1053–9.

    Article  CAS  PubMed  Google Scholar 

  141. Egan KM, Ryan LM, Gragoudas ES. Survival implications of enucleation after definitive radiotherapy for choroidal melanoma: an example of regression on time-dependent covariates. Arch Ophthalmol. 1998;116:366–70.

    Article  CAS  PubMed  Google Scholar 

  142. Char DH, Kroll SM, Castro J. Long-term follow-up after uveal melanoma charged particle therapy. Trans Am Ophthalmol Soc. 1997;95:171–87.

    CAS  PubMed  PubMed Central  Google Scholar 

  143. Summanen P, Immonen I, Kivelä T, Tommila P, Heikkonen J, Tarkkanen A. Radiation related complications after ruthenium plaque radiotherapy of uveal melanoma. Br J Ophthalmol. 1996;80:732–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Kleineidam M, Guthoff R, Bentzen SM. Rates of local control, metastasis, and overall survival in patients with posterior uveal melanomas treated with ruthenium-106 plaques. Radiother Oncol. 1993;28:148–56.

    Article  CAS  PubMed  Google Scholar 

  145. Seddon JM, Gragoudas ES, Egan KM, Glynn RJ, Howard S, Fante RG, et al. Relative survival rates after alternative therapies for uveal melanoma. Ophthalmology. 1990;97:769–77.

    Article  CAS  PubMed  Google Scholar 

  146. Lommatzsch PK. Results after beta-irradiation (106Ru/106Rh) of choroidal melanomas. Twenty years’ experience. Am J Clin Oncol. 1987;10:146–51.

    Article  CAS  PubMed  Google Scholar 

  147. Wang Z, Nabhan M, Schild SE, Stafford SL, Petersen IA, Foote RL, et al. Charged particle radiation therapy for uveal melanoma: a systematic review and meta-analysis. Int J Radiat Oncol Biol Phys. 2013;86:18–26.

    Article  PubMed  Google Scholar 

  148. Hungerford JL. Current trends in the treatment of ocular melanoma by radiotherapy. Clin Exp Ophthalmol. 2003;31:8–13.

    Article  PubMed  Google Scholar 

  149. Ophthalmic Oncology Task Force. Local recurrence significantly increases the risk of metastatic uveal melanoma. Ophthalmology. 2016;123:86–91.

    Article  Google Scholar 

  150. Buonanno F, Conson M, de Almeida Ribeiro C, Oliviero C, Itta F, Liuzzi R, et al. Local tumor control and treatment related toxicity after plaque brachytherapy for uveal melanoma: a systematic review and a data pooled analysis. Radiother Oncol. 2022;166:15–25.

    Article  PubMed  Google Scholar 

  151. Mishra KK, Daftari IK. Proton therapy for the management of uveal melanoma and other ocular tumors. Chin Clin Oncol. 2016;5:50.

    Article  PubMed  Google Scholar 

  152. Schulz-Ertner D, Jäkel O, Schlegel W. Radiation therapy with charged particles. Semin Radiat Oncol. 2006;16:249–59.

    Article  PubMed  Google Scholar 

  153. Mathis T, Cassoux N, Tardy M, Piperno S, Gastaud L, Dendale R, et al. [Management of uveal melanomas, guidelines for oncologists]. Bull Cancer. 2018;105:967–80.

    Article  PubMed  Google Scholar 

  154. Daftari IK, Char DH, Verhey LJ, Castro JR, Petti PL, Meecham WJ, et al. Anterior segment sparing to reduce charged particle radiotherapy complications in uveal melanoma. Int J Radiat Oncol* Biol* Phys. 1997;39:997–1010.

    Article  CAS  PubMed  Google Scholar 

  155. Seibel I, Riechardt AI, Heufelder J, Cordini D, Joussen AM. Adjuvant ab interno tumor treatment after proton beam irradiation. Am J Ophthalmol. 2017;178:94–100.

    Article  PubMed  Google Scholar 

  156. Borenstein M, Hedges L, Higgins J, Rothstein H. Introduction to meta-analysis. Chichester, UK: John Wiley & Sons. Ltd. 2009.

Download references

Author information

Authors and Affiliations

  1. Department of Medical Education, Taipei Veterans General Hospital, Taipei, 11217, Taiwan

    Yu-Hsuan Tseng

  2. Department of Ophthalmology, Taipei Veterans General Hospital, Taipei, 11217, Taiwan

    Chia-An Hsu & Yu-Bai Chou

  3. School of Medicine, National Yang Ming Chiao Tung University, Taipei, Taiwan

    Yu-Bai Chou

  4. Institute of Public Health, National Yang Ming Chiao Tung University, Taipei, Taiwan

    Yu-Bai Chou

Authors
  1. Yu-Hsuan Tseng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chia-An Hsu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yu-Bai Chou
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YHT, CAH and YBC were responsible for designing the review protocol, screening potentially eligible studies, and interpreting results. YHT and CAH were responsible for conducting the search, extracting and analyzing the data, updating reference lists and drafting the original article. YBC supervised and provided feedback on the report. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Yu-Bai Chou.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tseng, YH., Hsu, CA. & Chou, YB. Comparing efficacy of charged-particle therapy with brachytherapy in treatment of uveal melanoma. Eye (2024). https://doi.org/10.1038/s41433-024-03035-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41433-024-03035-y

  • Springer Nature Limited

Search

Navigation