Combinations of radiation therapy and immunotherapy for melanoma: A review of clinical outcomes

International Journal of Radiation Oncology Biology Physics

Volumn 88, Issue 5, 2014, Pages 986-997

  Barker, Christopher A ^a   Postow, Michael A ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL TRANSFER; CLINICAL OUTCOME; CLINICAL STUDY; CLINICAL TRIAL; CYTOKINES; INTERLEUKIN-2; MELANOMA CELLS; PILOT STUDIES;

DERMATOLOGY; MONOCLONAL ANTIBODIES; ONCOLOGY;

RADIOTHERAPY;

CANCER VACCINE; IMMUNOMODULATING AGENT; INTERFERON; INTERLEUKIN 2; IPILIMUMAB;

ADVANCED CANCER; CANCER IMMUNOTHERAPY; CANCER PATIENT; CANCER RADIOTHERAPY; CASE STUDY; CELL TRANSFER; CLINICAL TRIAL (TOPIC); HUMAN; MELANOMA; METASTATIC MELANOMA; MULTIMODALITY CANCER THERAPY; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; REVIEW; TREATMENT OUTCOME;

ADOPTIVE TRANSFER; ANIMALS; ANTIBODIES, MONOCLONAL; CANCER VACCINES; CLINICAL TRIALS AS TOPIC; COMBINED MODALITY THERAPY; CTLA-4 ANTIGEN; HUMANS; IMMUNOMODULATION; IMMUNOTHERAPY; INTERFERONS; INTERLEUKIN-2; MELANOMA; MICE; SKIN NEOPLASMS; TREATMENT OUTCOME;

EID: 84897832209     PISSN: 03603016     EISSN: 1879355X     Source Type: Journal    
DOI: 10.1016/j.ijrobp.2013.08.035     Document Type: Review

References (82)

1. S.C. Formenti, and S. Demaria Combining radiotherapy and cancer immunotherapy: A paradigm shift J Natl Cancer Inst 105 2013 256 265
2. S. Wang, Z. Zhao, and B. Barber et al. Surgery, radiation, and systemic therapies in patients with metastatic melanoma J Clin Oncol 30 2012 A232 A233
3. C.M. Balch, J.E. Gershenwald, and S.J. Soong et al. Final version of 2009 AJCC melanoma staging and classification J Clin Oncol 27 2009 6199 6206
4. Collaborative Ocular Melanoma Study G The COMS randomized trial of iodine 125 brachytherapy for choroidal melanoma: V. Twelve-year mortality rates and prognostic factors: COMS report No. 28 Arch Ophthalmol 124 2006 1684 1693
5. B.S. Hawkins, and Collaborative Ocular Melanoma Study G The Collaborative Ocular Melanoma Study (COMS) randomized trial of pre-enucleation radiation of large choroidal melanoma: IV. Ten-year mortality findings and prognostic factors. COMS report number 24 Am J Ophthalmol 138 2004 936 951
6. M. Mihajlovic, S. Vlajkovic, and P. Jovanovic et al. Primary mucosal melanomas: A comprehensive review Int J Clin Exp Pathol 5 2012 739 753
7. C.A. Barker, and N.Y. Lee Radiation therapy for cutaneous melanoma Dermatol Clin 30 2012 525 533
8. L.M. Jampol, C.S. Moy, and T.G. Murray 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 109 2002 2197 2206
9. D.H. Char, J.M. Quivey, and J.R. Castro et al. Helium ions versus iodine 125 brachytherapy in the management of uveal melanoma: A prospective, randomized, dynamically balanced trial Ophthalmology 100 1993 1547 1554
10. P.U. Huguenin, S. Kieser, and C. Glanzmann et al. Radiotherapy for metastatic carcinomas of the kidney or melanomas: an analysis using palliative end points Int J Radiat Oncol Biol Phys 41 1998 401 405
11. R.N. Shen, N.B. Hornback, and H. Shidnia et al. A comparison of lung metastases and natural killer cell activity in daily fractions and weekly fractions of radiation therapy on murine B16a melanoma Radiat Res 114 1988 354 360
12. C.A. Perez, A. Fu, and H. Onishko et al. Radiation induces an antitumour immune response to mouse melanoma Int J Radiat Biol 85 2009 1126 1136
13. Y. Lee, S.L. Auh, and Y. Wang et al. Therapeutic effects of ablative radiation on local tumor require CD8+ T cells: Changing strategies for cancer treatment Blood 114 2009 589 595
14. D.P. Kingsley An interesting case of possible abscopal effect in malignant melanoma Br J Radiol 48 1975 863 866
15. R.H. Mole Whole body irradiation; radiobiology or medicine? Br J Radiol 26 1953 234 241
16. S. Demaria, B. Ng, and M.L. Devitt et al. Ionizing radiation inhibition of distant untreated tumors (abscopal effect) is immune mediated Int J Radiat Oncol Biol Phys 58 2004 862 870
17. H.E. Teulings, E.P. Tjin, and K.J. Willemsen et al. Radiation-induced melanoma-associated leucoderma, systemic antimelanoma immunity and disease-free survival in a patient with advanced-stage melanoma: A case report and immunological analysis Br J Dermatol 168 2013 733 738
18. A. Abood, D.B. Saleh, and D.A. Watt Malignant melanoma and vitiligo: Can radiotherapy shed light on the subject? J Plast Reconstr Aesthet Surg 62 2009 e119 e120
19. R.J. Sullivan, D.P. Lawrence, and J.A. Wargo et al. Case 21-2013 N Engl J Med 369 2013 173 183
20. C. Yee, J.A. Thompson, and P. Roche et al. Melanocyte destruction after antigen-specific immunotherapy of melanoma: Direct evidence of T cell-mediated vitiligo J Exp Med 192 2000 1637 1644
21. J.L. Federman, N.T. Felberg, and J.A. Shields Effect of local treatment on antibody levels in malignant melanoma of the choroid Trans Ophthalmol Soc U K 97 1977 436 439
22. P. Toivonen, and T. Kivela Infiltrating macrophages in extratumoural tissues after brachytherapy of uveal melanoma Acta Ophthalmol 90 2012 341 349
23. T.H. Vu, I.H. Bronkhorst, and M. Versluis et al. Analysis of inflammatory cells in uveal melanoma after prior irradiation Invest Ophthalmol Vis Sci 54 2013 360 369
24. C.S. Lee, I.H. Jun, and T.I. Kim et al. Expression of 12 cytokines in aqueous humour of uveal melanoma before and after combined Ruthenium-106 brachytherapy and transpupillary thermotherapy Acta Ophthalmol 90 2012 e314 e320
25. A.M. Sarici, S.U. Shah, and C.L. Shields et al. Cutaneous halo nevi following plaque radiotherapy for uveal melanoma Arch Ophthalmol 129 2011 1499 1501
26. D.L. Morton, R.A. Malmgren, and E.C. Holmes et al. Demonstration of antibodies against human malignant melanoma by immunofluorescence Surgery 64 1968 233 240
27. D.J. Schwartzentruber, D.H. Lawson, and J.M. Richards et al. gp100 peptide vaccine and interleukin-2 in patients with advanced melanoma N Engl J Med 364 2011 2119 2127
28. W.H. Kruit, S. Suciu, and B. Dreno et al. Selection of immunostimulant AS15 for active immunization with MAGE-A3 protein: Results of a randomized phase II study of the European Organisation for Research and Treatment of Cancer melanoma group in metastatic melanoma J Clin Oncol 31 2013 2413 2420
29. E.C. Hsueh, R. Essner, and L.J. Foshag et al. Active immunotherapy by reinduction with a polyvalent allogeneic cell vaccine correlates with improved survival in recurrent metastatic melanoma Ann Surg Oncol 9 2002 486 492
30. D.L. Morton, N. Mozzillo, and J.F. Thompson et al. An international, randomized, phase III trial of bacillus Calmette-Guerin (BCG) plus allogeneic melanoma vaccine (MCV) or placebo after complete resection of melanoma metastatic to regional or distant sites J Clin Oncol 25 2008 8508
31. R.L. Ikonopisov, M.G. Lewis, and I.D. Hunter-Craig et al. Autoimmunization with irradiated tumour cells in human malignant melanoma Br Med J 2 1970 752 754
32. D.H. Deacon, K.T. Hogan, and E.M. Swanson et al. The use of gamma-irradiation and ultraviolet-irradiation in the preparation of human melanoma cells for use in autologous whole-cell vaccines BMC Cancer 8 2008 360
33. R.O. Dillman, A.N. Cornforth, and C. Depriest et al. Tumor stem cell antigens as consolidative active specific immunotherapy: A randomized phase II trial of dendritic cells versus tumor cells in patients with metastatic melanoma J Immunother 35 2012 641 649
34. R.O. Dillman, G.B. Fogel, and A.N. Cornforth et al. Features associated with survival in metastatic melanoma patients treated with patient-specific dendritic cell vaccines Cancer Biother Radiopharm 26 2011 407 415
35. J.M. Kirkwood, M.H. Strawderman, and M.S. Ernstoff et al. Interferon alfa-2b adjuvant therapy of high-risk resected cutaneous melanoma: the Eastern Cooperative Oncology Group Trial EST 1684 J Clin Oncol 14 1996 7 17
36. J.M. Kirkwood, J.G. Ibrahim, and J.A. Sosman et al. High-dose interferon alfa-2b significantly prolongs relapse-free and overall survival compared with the GM2-KLH/QS-21 vaccine in patients with resected stage IIB-III melanoma: Results of intergroup trial E1694/S9512/C509801 J Clin Oncol 19 2001 2370 2380
37. P.B. Chapman Counterpoint: The case against adjuvant high-dose interferon-alpha for melanoma patients J Natl Compr Canc Netw 2 2004 69 72
38. A. Dritschilo, K. Mossman, and M. Gray et al. Potentiation of radiation injury by interferon Am J Clin Oncol 5 1982 79 82
39. H. Schmidberger, M. Rave-Frank, and J. Lehmann et al. The combined effect of interferon beta and radiation on five human tumor cell lines and embryonal lung fibroblasts Int J Radiat Oncol Biol Phys 43 1999 405 412
40. A.Y. Chang, and P.C. Keng Potentiation of radiation cytotoxicity by recombinant interferons, a phenomenon associated with increased blockage at the G2-M phase of the cell cycle Cancer Res 47 1987 4338 4341
41. S. McDonald, P. Rubin, and A.Y. Chang et al. Pulmonary changes induced by combined mouse beta-interferon (rMuIFN-beta) and irradiation in normal mice: Toxic versus protective effects Radiother Oncol 26 1993 212 218
42. L.J. Hazard, W.T. Sause, and R.D. Noyes Combined adjuvant radiation and interferon-alpha 2B therapy in high-risk melanoma patients: The potential for increased radiation toxicity Int J Radiat Oncol Biol Phys 52 2002 796 800
43. N.P. Nguyen, B. Levinson, and S. Dutta et al. Concurrent interferon-alpha and radiation for head and neck melanoma Melanoma Res 13 2003 67 71
44. C. Conill, S. Jorcano, and J. Domingo-Domenech et al. Toxicity of combined treatment of adjuvant irradiation and interferon alpha2b in high-risk melanoma patients Melanoma Res 17 2007 304 309
45. D.E. Gyorki, J. Ainslie, and M.L. Joon et al. Concurrent adjuvant radiotherapy and interferon-alpha2b for resected high risk stage III melanoma: A retrospective single centre study Melanoma Res 14 2004 223 230
46. S.E. Finkelstein, A. Trotti, and N. Rao et al. The Florida Melanoma Trial I: A prospective multicenter phase I/II trial of postoperative hypofractionated adjuvant radiotherapy with concurrent interferon-alfa-2b in the treatment of advanced stage III melanoma with long-term toxicity follow-up ISRN Immunol 2012 2012 10
47. E. Richtig, G. Langmann, and G. Schlemmer et al. [Safety and efficacy of interferon alfa-2b in the adjuvant treatment of uveal melanoma] Ophthalmologe 103 2006 506 511
48. A.M. Lane, K.M. Egan, and D. Harmon et al. Adjuvant interferon therapy for patients with uveal melanoma at high risk of metastasis Ophthalmology 116 2009 2206 2212
49. E. Paul, I. Muller, and H. Renner et al. Treatment of locoregional metastases of malignant melanomas with radiotherapy and intralesional beta-interferon injection Melanoma Res 13 2003 611 617
50. M.B. Atkins, M.T. Lotze, and J.P. Dutcher et al. High-dose recombinant interleukin 2 therapy for patients with metastatic melanoma: Analysis of 270 patients treated between 1985 and 1993 J Clin Oncol 17 1999 2105 2116
51. A. Safwat, N. Aggerholm, and I. Roitt et al. Low-dose total body irradiation augments the therapeutic effect of interleukin-2 in a mouse model for metastatic malignant melanoma J Exp Ther Oncol 3 2003 161 168
52. A. Safwat, N. Aggerholm, and I. Roitt et al. Tumour burden and interleukin-2 dose affect the interaction between low-dose total body irradiation and interleukin 2 Eur J Cancer 40 2004 1412 1417
53. A. Safwat, H. Schmidt, and L. Bastholt et al. A phase II trial of low-dose total body irradiation and subcutaneous interleukin-2 in metastatic melanoma Radiother Oncol 77 2005 143 147
54. R.B. Cameron, P.J. Spiess, and S.A. Rosenberg Synergistic antitumor activity of tumor-infiltrating lymphocytes, interleukin 2, and local tumor irradiation: Studies on the mechanism of action J Exp Med 171 1990 249 263
55. J.R. Lange, A.A. Raubitschek, and B.A. Pockaj et al. A pilot study of the combination of interleukin-2-based immunotherapy and radiation therapy J Immunother (1991) 12 1992 265 271
56. S.K. Seung, B.D. Curti, and M. Crittenden et al. Phase 1 study of stereotactic body radiotherapy and interleukin-2: Tumor and immunological responses Sci Transl Med 4 2012 137ra174
57. D. Okwan-Duodu, B.P. Pollack, and D. Lawson et al. Role of radiation therapy as immune activator in the era of modern immunotherapy for metastatic malignant melanoma Am J Clin Oncol 2014 Jan 18 [Epub ahead of print] doi: 10.1097/COC.0b013e3182940dc3
58. F.S. Hodi, S.J. O'Day, and D.F. McDermott et al. Improved survival with ipilimumab in patients with metastatic melanoma N Engl J Med 363 2010 711 723
59. C. Robert, L. Thomas, and I. Bondarenko et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma N Engl J Med 364 2011 2517 2526
60. S. Demaria, N. Kawashima, and A.M. Yang et al. Immune-mediated inhibition of metastases after treatment with local radiation and CTLA-4 blockade in a mouse model of breast cancer Clin Cancer Res 11 2005 728 734
61. K.A. Pilones, N. Kawashima, and A.M. Yang et al. Invariant natural killer T cells regulate breast cancer response to radiation and CTLA-4 blockade Clin Cancer Res 15 2009 597 606
62. M.Z. Dewan, A.E. Galloway, and N. Kawashima et al. Fractionated but not single-dose radiotherapy induces an immune-mediated abscopal effect when combined with anti-CTLA-4 antibody Clin Cancer Res 15 2009 5379 5388
63. J.P. Knisely, J.B. Yu, and J. Flanigan et al. Radiosurgery for melanoma brain metastases in the ipilimumab era and the possibility of longer survival J Neurosurg 117 2012 227 233
64. M. Mathew, M. Tam, and P.A. Ott et al. Ipilimumab in melanoma with limited brain metastases treated with stereotactic radiosurgery Melanoma Res 23 2013 191 195
65. A.P. Kiess, J.D. Wolchok, and C.A. Barker et al. Ipilimumab and stereotactic radiosurgery for melanoma brain metastases Int J Radiat Oncol Biol Phys 84 2012 S115 S116
66. S. Du Four, S. Wilgenhof, and J. Duerinck et al. Radiation necrosis of the brain in melanoma patients successfully treated with ipilimumab: Three case studies Eur J Cancer 48 2012 3045 3051
67. T. Muller-Brenne, B. Rudolph, and H. Schmidberger et al. Successful therapy of a cerebral metastasized malign melanoma by whole-brain-radiation and therapy with ipilimumab J Dtsch Dermatol Ges 9 2011 787 788
68. I. Bot, C.U. Blank, and D. Brandsma Clinical and radiological response of leptomeningeal melanoma after whole brain radiotherapy and ipilimumab J Neurol 259 2012 1976 1978
69. M.A. Postow, M.K. Callahan, and C.A. Barker et al. Immunologic correlates of the abscopal effect in a patient with melanoma N Engl J Med 366 2012 925 931
70. E.F. Stamell, J.D. Wolchok, and S. Gnjatic et al. The abscopal effect associated with a systemic anti-melanoma immune response Int J Radiat Oncol Biol Phys 85 2013 293 295
71. S.M. Hiniker, D.S. Chen, and S. Reddy et al. A systemic complete response of metastatic melanoma to local radiation and immunotherapy Transl Oncol 5 2012 404 407
72. C.A. Barker, M.A. Postow, and S.A. Khan et al. Concurrent radiotherapy and ipilimumab immunotherapy for patients with melanoma Cancer Immunol Res 1 2013 92 98
73. S.L. Topalian, F.S. Hodi, and J.R. Brahmer et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer N Engl J Med 366 2012 2443 2454
74. O. Hamid, C. Robert, and A. Daud et al. Safety and tumor responses with lambrolizumab (anti-PD-1) in melanoma N Engl J Med 369 2013 134 144
75. H. Liang, L. Deng, and S. Chmura et al. Radiation-induced equilibrium is a balance between tumor cell proliferation and T cell-mediated killing J Immunol 190 2013 5874 5881
76. J. Zeng, A.P. See, and J. Phallen et al. Anti-PD-1 blockade and stereotactic radiation produce long-term survival in mice with intracranial gliomas Int J Radiat Oncol Biol Phys 86 2013 343 349
77. I. Verbrugge, J. Hagekyriakou, and L.L. Sharp et al. Radiotherapy increases the permissiveness of established mammary tumors to rejection by immunomodulatory antibodies Cancer Res 72 2012 3163 3174
78. S.A. Rosenberg, J.C. Yang, and R.M. Sherry et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy Clin Cancer Res 17 2011 4550 4557
79. C. Wrzesinski, C.M. Paulos, and A. Kaiser et al. Increased intensity lymphodepletion enhances tumor treatment efficacy of adoptively transferred tumor-specific T cells J Immunother 33 2010 1 7
80. M.E. Dudley, J.C. Yang, and R. Sherry et al. Adoptive cell therapy for patients with metastatic melanoma: Evaluation of intensive myeloablative chemoradiation preparative regimens J Clin Oncol 26 2008 5233 5239
81. M.E. Dudley, C.A. Gross, and M.M. Langhan et al. CD8+ enriched "young" tumor infiltrating lymphocytes can mediate regression of metastatic melanoma Clin Cancer Res 16 2010 6122 6131
82. J.D. Wolchok, H. Kluger, and M.K. Callahan et al. Nivolumab plus ipilimumab in advanced melanoma N Engl J Med 369 2013 122 133