Therapy for Vitreous Seeding Caused by Retinoblastoma. A Review
Authors:
Martina Kodetová 1; Karel Švojgr 2; Jakub Širc 3; Jaroslav Vaněček 1; Pavel Pochop 1
Published in:
Čes. a slov. Oftal., 80, 2024, No. 3, p. 123-127
Category:
Review
doi:
https://doi.org/10.31348/2023/35
Overview
Retinoblastoma is the most common primary malignant intraocular tumor in children. Seeding, specifically the dispersion of the tumor into the adjacent compartments, represents a major parameter determining the degree of retinoblastoma according to the International Classification of Retinoblastoma. In this article we focused on vitreous seeding, one of the main limiting factors in the successful “eye preservation treatment” of retinoblastoma. This article presents an overview of the history of vitreous seeding of retinoblastoma, established treatment procedures and new-research modalities. The introduction of systemic chemotherapy in the treatment of retinoblastoma at the end of the 1990s represented a significant breakthrough, which enabled the progressive abandonment of radiotherapy with its attendant side effects. However, the attained concentrations of chemotherapeutics in the vitreous space during systemic chemotherapy are not sufficient for the treatment of vitreous seeding, and the toxic effects of systemic chemotherapy are not negligible. A significant change came with the advent of chemotherapy in situ, with the targeted administration of chemotherapeutic drugs, namely intra-arterial and intravitreal injections, contributing to the definitive eradication of external radiotherapy and a reduction of systemic chemotherapy. Although vitreous seeding remains the most common reason for the failure of intra-arterial chemotherapy, this technique has significantly influenced the original treatment regimen of children with retinoblastoma. However, intravitreal chemotherapy has made the greatest contribution to increasing the probability of preservation of the eyeball and visual functions in patients with advanced findings. Novel local drug delivery modalities, gene therapy, oncolytic viruses and immunotherapy from several ongoing preclinical and clinical trials may represent promising approaches in the treatment of vitreous retinoblastoma seeding, though no clinical trials have yet been completed for routine use.
Keywords:
retinoblastoma – vitreous seeding – eye preservation treatment – intravitreal chemotherapy
Sources
1. Stacey AW, Bowman R, Foster A, et al. Global Retinoblastoma Study Group. Incidence of Retinoblastoma Has Increased: Results from 40 European Countries. Ophthalmology. 2021 Sep;128(9):1369-1371.
2. Švojgr K. Retinoblastom, Onkologie 2016;10(5):215-217.
3. Abramson DH, Schefler AC. Update on retinoblastoma. Retina. 2004 Dec;24(6):828-848.
4. Shields JA, Shields CL. Intraocular tumors: atlas and textbook. 2nd ed. Philadelphia: Lippincott Wiliams & Wilkins, a Wolters Kluwer business; 2008. Chapter 15, Retinoblastoma: Introduction, Genetics, Clinical Features, Classification; 294-295.
5. Shields JA, Shields CL, Materin M. Diffuse infiltrating retinoblastoma presenting as a spontaneous hyphema. J Pediatr Ophthalmol Strabismus 2000;37:311-312.
6. Shields CL, Mashayekhi A, Au AK, et al. The International Classification of Retinoblastoma predicts chemoreduction success, Ophthalmology 2006;113:2276-2280.
7. Munier FL. Classification and management of seeds in retinoblastoma. Ellsworth Lecture Ghent August 24th 2013. Ophthalmic Genet. 2014 Dec;35(4):193-207.
8. Francis JH, Abramson DH, Gaillard MC, Marr BP, Beck-Popovic M, Munier FL. The classification of vitreous seeds in retinoblastoma and response to intravitreal melphalan. Ophthalmology. 2015 Jun;122(6):1173-1179.
9. Abramson DH. Retinoblastoma in the 20th century: past success and future challenges the Weisenfeld lecture. Invest Ophthalmol Vis Sci. 2005 Aug;46(8):2683-2691.
10. Munier FL, Beck-Popovic M, Chantada GL, et al. Conservative management of retinoblastoma: Challenging orthodoxy without compromising the state of metastatic grace. “Alive, with good vision and no comorbidity”. Prog Retin Eye Res. 2019 Nov;73:100764.
11. Rizzuti AE, Dunkel IJ, Abramson DH. The adverse events of chemotherapy for retinoblastoma: what are they? Do we know? Arch Ophthalmol. 2008 Jun;126(6):862-865.
12. Weintraub M, Revel-Vilk S, Charit M, Aker M, Pe’er J. Secondary acute myeloid leukemia after etoposide therapy for retinoblastoma. J Pediatr Hematol Oncol. 2007 Sep;29(9):646-648.
13. Qaddoumi I, Bass JK, Wu J, et al. Carboplatin-associated ototoxicity in children with retinoblastoma. J Clin Oncol. 2012 Apr;30(10):1034-1041.
14. Abramson DH, Marr BP, Dunkel IJ, et al. Intra-arterial chemotherapy for retinoblastoma in eyes with vitreous and/or subretinal seeding: 2-year results. Br J Ophthalmol. 2012 Apr;96(4):499-502.
15. Francis JH, Abramson DH, Gobin YP, et al. Electroretinogram monitoring of dose-dependent toxicity after ophthalmic artery chemosurgery in retinoblastoma eyes: six year review. PLoS One. 2014 Jan 20;9(1):e84247.
16. Abramson DH. Retinoblastoma: saving life with vision. Annu Rev Med. 2014;65:171-184.
17. Munier FL, Beck-Popovic M, Balmer A, Gaillard MC, Bovey E, Binaghi S. Occurrence of sectoral choroidal occlusive vasculopathy and retinal arteriolar embolization after superselective ophthalmic artery chemotherapy for advanced intraocular retinoblastoma. Retina. 2011 Mar;31(3):566-573.
18. Suzuki S, Yamane T, Mohri M, Kaneko A. Selective ophthalmic arterial injection therapy for intraocular retinoblastoma: the long-term prognosis. Ophthalmology. 2011 Oct;118(10):2081-2087.
19. Schaiquevich P, Francis JH, Cancela MB, Carcaboso AM, Chantada GL, Abramson DH. Treatment of Retinoblastoma: What Is the Latest and What Is the Future. Front Oncol. 2022 Apr 1;12:822330.
20. Abramson DH, Dunkel IJ, Brodie SE, Kim JW, Gobin YP. A phase I/II study of direct intraarterial (ophthalmic artery) chemotherapy with melphalan for intraocular retinoblastoma initial results. Ophthalmology. 2008 Aug;115(8):1398-404, 1404.e1.
21. Shields CL, Bianciotto CG, Jabbour P, et al. Intra-arterial chemotherapy for retinoblastoma: report No. 2, treatment complications. Arch Ophthalmol. 2011 Nov;129(11):1407-1415.
22. Abramson DH. Super selective ophthalmic artery delivery of chemotherapy for intraocular retinoblastoma: ‘chemosurgery’ the first Stallard lecture. Br J Ophthalmol. 2010 Apr;94(4):396-399.
23. Inomata M, Kaneko A. Chemosensitivity profiles of primary and cultured human retinoblastoma cells in a human tumor clonogenic assay. Jpn J Cancer Res 1987;78:858-868.
24. Taich P, Ceciliano A, Buitrago E, et al. Clinical pharmacokinetics of intra-arterial melphalan and topotecan combination in patients with retinoblastoma. Ophthalmology. 2014 Apr;121(4):889-897.
25. Abramson DH, Daniels AB, Marr BP,et al. Intra-Arterial Chemotherapy (Ophthalmic Artery Chemosurgery) for Group D Retinoblastoma. PLoS One. 2016 Jan 12;11(1):e0146582.
26. Abramson DH, Dunkel IJ, Brodie SE, Marr B, Gobin YP. Superselective ophthalmic artery chemotherapy as primary treatment for retinoblastoma (chemosurgery). Ophthalmology. 2010 Aug;117(8):1623-1629.
27. Scharoun JH, Han JH, Gobin YP. Anesthesia for Ophthalmic Artery Chemosurgery. Anesthesiology. 2017 Jan;126(1):165-172.
28. De la Huerta I, Seider MI, Hetts SW, Damato BE. Delayed Cerebral Infarction Following Intra-arterial Chemotherapy for Retinoblastoma. JAMA Ophthalmol. 2016 Jun 1;134(6):712-714.
29. Kaneko A, Suzuki S. Eye-preservation treatment of retinoblastoma with vitreous seeding. Jpn J Clin Oncol. 2003 Dec;33(12):601-607.
30. Munier FL, Gaillard MC, Balmer A, et al. Intravitreal chemotherapy for vitreous disease in retinoblastoma revisited: from prohibition to conditional indications. Br J Ophthalmol. 2012 Aug;96(8):1078-1083.
31. Munier FL, Soliman S, Moulin AP, Gaillard MC, Balmer A, Beck-Popovic M. Profiling safety of intravitreal injections for retinoblastoma using an anti-reflux procedure and sterilisation of the needle track. Br J Ophthalmol. 2012 Aug;96(8):1084-1087.
32. Francis JH, Brodie SE, Marr B, Zabor EC, Mondesire-Crump I, Abramson DH. Efficacy and Toxicity of Intravitreous Chemotherapy for Retinoblastoma: Four-Year Experience. Ophthalmology. 2017 Apr;124(4):488-495.
33. Ghassemi F, Shields CL, Ghadimi H, Khodabandeh A, Roohipoor R. Combined intravitreal melphalan and topotecan for refractory or recurrent vitreous seeding from retinoblastoma. JAMA Ophthalmol. 2014 Aug;132(8):936-941.
34. Shields CL, Douglass AM, Beggache M, Say EA, Shields JA. Intravitreous chemotherapy for active vitreous seeding from retinoblastoma: Outcomes After 192 Consecutive Injections. The 2015 Howard Naquin Lecture. Retina. 2016 Jun;36(6):1184-1190. 35. Francis JH, Schaiquevich P, Buitrago E, et al. Local and systemic toxicity of intravitreal melphalan for vitreous seeding in retinoblastoma: a preclinical and clinical study. Ophthalmology. 2014 Sep;121(9):1810-1817.
36. Schaiquevich P, Francis JH, Cancela MB, Carcaboso AM, Chantada GL, Abramson DH. Treatment of Retinoblastoma: What Is the Latest and What Is the Future. Front Oncol. 2022 Apr 1;12:822330.
37. Buitrago E, Lagomarsino E, Mato G, Schaiquevich P. Stability of Melphalan Solution for Intravitreal Injection for Retinoblastoma. JAMA Ophthalmol. 2014;132(11):1372-1373.
38. Francis JH, Marr BP, Abramson DH. Classification of Vitreous Seeds in Retinoblastoma: Correlations with Patient, Tumor, and Treatment Characteristics. Ophthalmology. 2016 Jul;123(7):1601-1605.
39. Smith SJ, Smith BD, Mohney BG. Ocular side effects following intravitreal injection therapy for retinoblastoma: a systematic review. Br J Ophthalmol. 2014 Mar;98(3):292-297.
40. Schlüter S, Bornfeld N, Valiyev E, et al. Combination of Brachytherapy and Intravitreal Chemotherapy in the Treatment of Retinoblastoma with Vitreous Seeding. Ocul Oncol Pathol. 2022 Feb;8(1):64-70.
41. Francis JH, Marr BP, Brodie SE, Abramson DH. Anterior Ocular Toxicity of Intravitreous Melphalan for Retinoblastoma. JAMA Ophthalmol. 2015 Dec;133(12):1459-1463.
42. Francis JH, Abramson DH, Ji X, et al. Risk of Extraocular Extension in Eyes With Retinoblastoma Receiving Intravitreous Chemotherapy. JAMA Ophthalmol. 2017 Dec 1;135(12):1426-1429.
43. Ghassemi F, Shields CL. Intravitreal melphalan for refractory or recurrent vitreous seeding from retinoblastoma. Arch Ophthalmol. 2012 Oct;130(10):1268-1271.
44. Shields CL, Manjandavida FP, Arepalli S, Kaliki S, Lally SE, Shields JA. Intravitreal melphalan for persistent or recurrent retinoblastoma vitreous seeds: preliminary results. JAMA Ophthalmol. 2014 Mar;132(3):319-325.
45. Buitrago E, Del Sole MJ, Torbidoni A, et al. Ocular and systemic toxicity of intravitreal topotecan in rabbits for potential treatment of retinoblastoma. Exp Eye Res. 2013 Mar;108:103-109. 46. Del Sole MJ, Clausse M, Nejamkin P, et al. Ocular and systemic toxicity of high-dose intravitreal topotecan in rabbits: Implications for retinoblastoma treatment. Exp Eye Res. 2022 May;218:109026.
47. Nadelmann J, Francis JH, Brodie SE, Muca E, Abramson DH. Is intravitreal topotecan toxic to retinal function? Br J Ophthalmol. 2021 Jul;105(7):1016-1018.
48. Smith SJ, Pulido JS, Salomão DR, Smith BD, Mohney B. Combined intravitreal and subconjunctival carboplatin for retinoblastoma with vitreous seeds. Br J Ophthalmol. 2012 Aug;96(8):1073-1077.
49. Yousef YA, Al Jboor M, Mohammad M, et al. Safety and Efficacy of Intravitreal Chemotherapy (Melphalan) to Treat Vitreous Seeds in Retinoblastoma. Front Pharmacol. 2021 Jul 12;12:696787.
50. Mendelsohn M, Abramson DH, Madden T, et al. Intraocular concentrations of chemotherapeutic agents after systemic or local administration. Arch Ophthalmol. 1998;116:1209-1212.
51. Abramson DH, Frank CM, Dunkel IJ. A phase I/II study of subconjunctival carboplatin for intraocular retinoblastoma. Ophthalmology 1999;106:1947-1950
52. Martin NE, Kim JW, Abramson DH. Fibrin sealant for retinoblastoma: where are we? J Ocul Pharmacol Ther. 2008 Oct;24(5):433-438.
53. Carcaboso AM, Chiappetta DA, Opezzo JA, et al. Episcleral implants for topotecan delivery to the posterior segment of the eye. Invest Ophthalmol Vis Sci. 2010 Apr;51(4):2126-2134.
54. Hobzova R, Kodetova M, Pochop P, et al. Hydrogel implants for transscleral diffusion delivery of topotecan: In vivo proof of concept in a rabbit eye model. Int J Pharm. 2021 Sep 5;606:120832.
55. Kodetova M, Hobzova R, Sirc J, et al. The Role of Cryotherapy in Vitreous Concentrations of Topotecan Delivered by Episcleral Hydrogel Implant. Pharmaceutics. 2022 Apr 20;14(5):903.
56. Hayden BC, Jockovich ME, Murray TG, et al. Pharmacokinetics of systemic versus focal Carboplatin chemotherapy in the rabbit eye: possible implication in the treatment of retinoblastoma. Invest Ophthalmol Vis Sci. 2004 Oct;45(10):3644-3649.
57. Schmack I, Hubbard GB, Kang SJ, et al. Ischemic necrosis and atrophy of the optic nerve after periocular carboplatin injection for intraocular retinoblastoma. Am J Ophthalmol 2006;142:310-315.
58. National Library of Medicine. Topotecan Episcleral Plaque for Treatment of Retinoblastoma – Full Text (2020). ClinicalTrials.gov. Available from: https:clinicaltrials.gov/ct2/show/NCT04428879 (Accessed October 26, 2021)
59. Chévez-Barrios P, Chintagumpala M, Mieler W, et al. Response of retinoblastoma with vitreous tumor seeding to adenovirus-mediated delivery of thymidine kinase followed by ganciclovir. J Clin Oncol. 2005 Nov 1;23(31):7927-7935.
60. Pascual-Pasto G, Bazan-Peregrino M, Olaciregui NG, et al. Therapeutic targeting of the RB1 pathway in retinoblastoma with the oncolytic adenovirus VCN-01. Sci Transl Med. 2019 Jan 23;11(476):eaat9321.
61. Laurent VE, Otero LL, Vazquez V, et al. Optimization of molecular detection of GD2 synthase mRNA in retinoblastoma. Mol Med Rep. 2010 Mar-Apr;3(2):253-259. 62. Chantada GL, Rossi J, Casco F, et al. An aggressive bone marrow evaluation including immunocytology with GD2 for advanced retinoblastoma. J Pediatr Hematol Oncol. 2006 Jun;28(6):369-373.
63. Mora J. Dinutuximab for the treatment of pediatric patients with high-risk neuroblastoma. Expert Rev Clin Pharmacol. 2016;9(5):647-653.
64. Andersch L, Radke J, Klaus A, et al. CD171- and GD2-specific CAR-T cells potently target retinoblastoma cells in preclinical in vitro testing. BMC Cancer. 2019 Sep 9;19(1):895.
65. Wang K, Chen Y, Ahn S, et al. GD2-specific CAR T cells encapsulated in an injectable hydrogel control retinoblastoma and preserve vision. Nat Cancer. 2020 Oct;1(10):990-997.
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Czech and Slovak Ophthalmology
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