The abscopal effect of local radiotherapy: Using immunotherapy to make a rare event clinically relevant

Cancer Treatment Reviews

Volumn 41, Issue 6, 2015, Pages 503-510

  Reynders, Kobe ^a   Illidge, Tim ^b   Siva, Shankar ^c,d   Chang, Joe Y ^e   De Ruysscher, Dirk ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c PETER MACCALLUM CANCER CENTRE   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Abscopal effect; Immune therapy; Irradiation; Radiotherapy

Indexed keywords

ABSCOPAL EFFECT; CANCER GROWTH; CANCER IMMUNOLOGY; CANCER IMMUNOTHERAPY; CANCER RADIOTHERAPY; FOLLOW UP; HUMAN; IMMUNE RESPONSE; IMMUNOGENICITY; PATIENT SAFETY; PATIENT SELECTION; RADIATION DOSE FRACTIONATION; RADIATION RESPONSE; REVIEW; SYSTEMATIC REVIEW; ADULT; AGED; FEMALE; IMMUNOLOGY; IMMUNOTHERAPY; MALE; MIDDLE AGED; NEOPLASMS; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; DOSE FRACTIONATION; FEMALE; HUMANS; IMMUNOTHERAPY; MALE; MIDDLE AGED; NEOPLASMS;

EID: 84937640449     PISSN: 03057372     EISSN: 15321967     Source Type: Journal    
DOI: 10.1016/j.ctrv.2015.03.011     Document Type: Review

References (69)

1. Mole R. Whole body irradiation therapy - radiobiology or medicine?. Br J Radiol 1953, 234-241.
2. Andrews JR. Radiobiology of Human Cancer Radiotherapy; 1978.
3. Formenti S.C., Demaria S. Systemic effects of local radiotherapy. Lancet Oncol 2009, 10(7):718-726.
4. Apetoh L., Ghiringhelli F., Tesniere A., Obeid M., Ortiz C., Criollo A., et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 2007, 13(9):1050-1059.
5. Obeid M., Panaretakis T., Joza N., Tufi R., Tesniere A., van Endert P., et al. Calreticulin exposure is required for the immunogenicity of gamma-irradiation and UVC light-induced apoptosis. Cell Death Differ 2007, 14(10):1848-1850.
6. Perez C.A., Fu A., Onishko H., Hallahan D.E., Geng L. Radiation induces an antitumour immune response to mouse melanoma. Int J Radiat Biol 2009, 85(12):1126-1136.
7. Gameiro S.R., Jammeh M.L., Wattenberg M.M., Tsang K.Y., Ferrone S., Hodge J.W. Radiation-induced immunogenic modulation of tumor enhances antigen processing and calreticulin exposure, resulting in enhanced T-cell killing. Oncotarget 2014, 5(2):403-416.
8. Krysko D.V., Garg A.D., Kaczmarek A., Krysko O., Agostinis P., Vandenabeele P. Immunogenic cell death and DAMPs in cancer therapy. Nat Rev Cancer 2012, 12(12):860-875.
9. Kroemer G., Galluzzi L., Kepp O., Zitvogel L. Immunogenic cell death in cancer therapy. Annu Rev Immunol 2013, 31:51-72.
10. Reits E.A., Hodge J.W., Herberts C.A., Groothuis T.A., Chakraborty M., Wansley E.K., et al. Radiation modulates the peptide repertoire, enhances MHC class I expression, and induces successful antitumor immunotherapy. J Exp Med 2006, 203(5):1259-1271.
11. Sharma A., Bode B., Wenger R.H., Lehmann K., Sartori A.A., Moch H., et al. Gamma-radiation promotes immunological recognition of cancer cells through increased expression of cancer-testis antigens in vitro and in vivo. PLoS One 2011, 6(11):e28217.
12. Golden E.B., Pellicciotta I., Demaria S., Barcellos-Hoff M.H., Formenti S.C. The convergence of radiation and immunogenic cell death signaling pathways. Front Oncol 2012, 2:88.
13. Chakraborty M., Abrams S.I., Camphausen K., Liu K., Scott T., Coleman C.N., et al. Irradiation of tumor cells up-regulates Fas and enhances CTL lytic activity and CTL adoptive immunotherapy. J Immunol 2003, 170(12):6338-6347.
14. Burnette B.C., Liang H., Lee Y., Chlewicki L., Khodarev N.N., Weichselbaum R.R., et al. The efficacy of radiotherapy relies upon induction of type i interferon-dependent innate and adaptive immunity. Cancer Res 2011, 71(7):2488-2496.
15. Lim J.Y., Gerber S.A., Murphy S.P., Lord E.M. Type I interferons induced by radiation therapy mediate recruitment and effector function of CD8(+) T cells. Cancer Immunol Immunother 2014, 63(3):259-271.
16. Vacchelli E., Vitale I., Tartour E., Eggermont A., Sautes-Fridman C., Galon J., et al. Trial Watch: anticancer radioimmunotherapy. Oncoimmunology 2013, 2(9):e25595.
17. Rees G.J. Abscopal regression in lymphoma: a mechanism in common with total body irradiation?. Clin Radiol 1981, 32(4):475-480.
18. Prithviraj G., Peter O., Lisa A. Abscopal effect and carcinomatous myelopathy: a case report. Neuro Oncol 2012, 14(Suppl. 6):133-141.
19. Chakravarty P.K., Alfieri A., Thomas E.K., Beri V., Tanaka K.E., Vikram B., et al. Flt3-ligand administration after radiation therapy prolongs survival in a murine model of metastatic lung cancer. Cancer Res 1999, 59(24):6028-6032.
20. Chakravarty P.K., Guha C., Alfieri A., Beri V., Niazova Z., Deb N.J., et al. Flt3L therapy following localized tumor irradiation generates long-term protective immune response in metastatic lung cancer: its implication in designing a vaccination strategy. Oncology 2006, 70(4):245-254.
21. Demaria S., Ng B., Devitt M.L., Babb J.S., Kawashima N., Liebes L., et al. Ionizing radiation inhibition of distant untreated tumors (abscopal effect) is immune mediated. Int J Radiat Oncol Biol Phys 2004, 58(3):862-870.
22. Yasuda K., Nirei T., Tsuno N.H., Nagawa H., Kitayama J. Intratumoral injection of interleukin-2 augments the local and abscopal effects of radiotherapy in murine rectal cancer. Cancer Sci 2011, 102(7):1257-1263.
23. Shiraishi K., Ishiwata Y., Nakagawa K., Yokochi S., Taruki C., Akuta T., et al. Enhancement of antitumor radiation efficacy and consistent induction of the abscopal effect in mice by ECI301, an active variant of macrophage inflammatory protein-1alpha. Clin Cancer Res 2008, 14(4):1159-1166.
24. Demaria S., Kawashima N., Yang A.M., Devitt M.L., Babb J.S., Allison J.P., 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 2005, 11(2):728-734.
25. McDermott D., Lebbe C., Hodi F.S., Maio M., Weber J.S., Wolchok J.D., et al. Durable benefit and the potential for long-term survival with immunotherapy in advanced melanoma. Cancer Treat Rev 2014, 40(9):1056-1064.
26. Deng L., Liang H., Burnette B., Beckett M., Darga T., Weichselbaum R.R., et al. Irradiation and anti-PD-L1 treatment synergistically promote antitumor immunity in mice. J Clin Invest 2014, 124(2):687-695.
27. Kumar T., Patel N., Talwar A. Spontaneous regression of thoracic malignancies. Respir Med 2010, 104(10):1543-1550.
28. Lin T.J., Liao L.Y., Lin C.L., Shih L.S., Chang T.A., Tu H.Y., et al. Spontaneous regression of hepatocellular carcinoma: a case report and literature review. Hepatogastroenterology 2004, 51(56):579-582.
29. Huz J.I., Melis M., Sarpel U. Spontaneous regression of hepatocellular carcinoma is most often associated with tumour hypoxia or a systemic inflammatory response. HPB (Oxford) 2012, 14(8):500-505.
30. Ricci S.B., Cerchiari U. Spontaneous regression of malignant tumors: Importance of the immune system and other factors (Review). Oncol Lett 2010, 1(6):941-945.
31. Nobler M.P. The abscopal effect in malignant lymphoma and its relationship to lymphocyte circulation. Radiology 1969, 93(2):410-412.
32. Grimaldi A.M., Simeone E., Giannarelli D., Muto P., Falivene S., Borzillo V., et al. Abscopal effects of radiotherapy on advanced melanoma patients who progressed after ipilimumab immunotherapy. Oncoimmunology 2014, 3:e28780.
33. Golden E.B., Demaria S., Schiff P.B., Chachoua A., Formenti S.C. An abscopal response to radiation and ipilimumab in a patient with metastatic non-small cell lung cancer. Cancer Immunol Res 2013, 1(6):365-372.
34. Hiniker S.M., Chen D.S., Reddy S., Chang D.T., Jones J.C., Mollick J.A., et al. A systemic complete response of metastatic melanoma to local radiation and immunotherapy. Transl Oncol 2012, 5(6):404-407.
35. Postow M.A., Callahan M.K., Barker C.A., Yamada Y., Yuan J., Kitano S., et al. Immunologic correlates of the abscopal effect in a patient with melanoma. N Engl J Med 2012, 366(10):925-931.
36. Stamell E.F., Wolchok J.D., Gnjatic S., Lee N.Y., Brownell I. The abscopal effect associated with a systemic anti-melanoma immune response. Int J Radiat Oncol Biol Phys 2013, 85(2):293-295.
37. Kachikwu E.L., Iwamoto K.S., Liao Y.P., DeMarco J.J., Agazaryan N., Economou J.S., et al. Radiation enhances regulatory T cell representation. Int J Radiat Oncol Biol Phys 2011, 81(4):1128-1135.
38. Strigari L., Mancuso M., Ubertini V., Soriani A., Giardullo P., Benassi M., et al. Abscopal effect of radiation therapy: interplay between radiation dose and p53 status. Int J Radiat Biol 2014, 90(3):248-255.
39. Camphausen K., Moses M.A., Menard C., Sproull M., Beecken W.D., Folkman J., et al. Radiation abscopal antitumor effect is mediated through p53. Cancer Res 2003, 63(8):1990-1993.
40. Yuan J., Adamow M., Ginsberg B.A., Rasalan T.S., Ritter E., Gallardo H.F., et al. Integrated NY-ESO-1 antibody and CD8+ T-cell responses correlate with clinical benefit in advanced melanoma patients treated with ipilimumab. Proc Natl Acad Sci USA 2011, 108(40):16723-16728.
41. Ohba K., Omagari K., Nakamura T., Ikuno N., Saeki S., Matsuo I., et al. Abscopal regression of hepatocellular carcinoma after radiotherapy for bone metastasis. Gut 1998, 43(4):575-577.
42. Waters J.P., Pober J.S., Bradley J.R. Tumour necrosis factor and cancer. J Pathol 2013, 230(3):241-248.
43. Nakanishi M., Chuma M., Hige S., Asaka M. Abscopal effect on hepatocellular carcinoma. Am J Gastroenterol 2008, 103(5):1320-1321.
44. Ledezma B., Binder S., Hamid O. Atypical clinical response patterns to ipilimumab. Clin J Oncol Nurs 2011, 15(4):393-403.
45. Dovedi S.J., Adlard A.L., Lipowska-Bhalla G., McKenna C., Jones S., Cheadle E.J., et al. Acquired resistance to fractionated radiotherapy can be overcome by concurrent PD-L1 blockade. Cancer Res 2014, 74(19):5458-5468.
46. Park H.J., Griffin R.J., Hui S., Levitt S.H., Song C.W. Radiation-induced vascular damage in tumors: implications of vascular damage in ablative hypofractionated radiotherapy (SBRT and SRS). Radiat Res 2012, 177(3):311-327.
47. Barker C.A., Postow M.A., Khan S.A., Beal K., Parhar P.K., Yamada Y., et al. Concurrent radiotherapy and ipilimumab immunotherapy for patients with melanoma. Cancer Immunol Res 2013, 1(2):92-98.
48. Kanegasaki S., Matsushima K., Shiraishi K., Nakagawa K., Tsuchiya T. Macrophage inflammatory protein derivative ECI301 enhances the alarmin-associated abscopal benefits of tumor radiotherapy. Cancer Res 2014, 74(18):5070-5078.
49. Dewan M.Z., Galloway A.E., Kawashima N., Dewyngaert J.K., Babb J.S., Formenti S.C., et al. Fractionated but not single-dose radiotherapy induces an immune-mediated abscopal effect when combined with anti-CTLA-4 antibody. Clin Cancer Res 2009, 15(17):5379-5388.
50. Akutsu Y., Matsubara H., Urashima T., Komatsu A., Sakata H., Nishimori T., et al. Combination of direct intratumoral administration of dendritic cells and irradiation induces strong systemic antitumor effect mediated by GRP94/gp96 against squamous cell carcinoma in mice. Int J Oncol 2007, 31(3):509-515.
51. Teitz-Tennenbaum S., Li Q., Rynkiewicz S., Ito F., Davis M.A., McGinn C.J., et al. Radiotherapy potentiates the therapeutic efficacy of intratumoral dendritic cell administration. Cancer Res 2003, 63(23):8466-8475.
52. Nikitina E.Y., Gabrilovich D.I. Combination of gamma-irradiation and dendritic cell administration induces a potent antitumor response in tumor-bearing mice: approach to treatment of advanced stage cancer. Int J Cancer 2001, 94(6):825-833.
53. Siva S., Callahan J., MacManus M.P., Martin O., Hicks R.J., Ball D.L. Abscopal effects after conventional and stereotactic lung irradiation of non-small-cell lung cancer. J Thorac Oncol 2013, 8(8):e71-e72.
54. Ishiyama H., Teh B.S., Ren H., Chiang S., Tann A., Blanco A.I., et al. Spontaneous regression of thoracic metastases while progression of brain metastases after stereotactic radiosurgery and stereotactic body radiotherapy for metastatic renal cell carcinoma: abscopal effect prevented by the blood-brain barrier?. Clin Genitourin Cancer 2012, 10(3):196-198.
55. Tubin S., Casamassima F., Menichelli C., Pastore G., Fanelli A., Crisci R. A case report on metastatic thyroid carcinoma: radiation-induced bystander or abscopal effect?. J Cancer Sci Ther 2012, 4:408-411.
56. Okuma K., Yamashita H., Niibe Y., Hayakawa K., Nakagawa K. Abscopal effect of radiation on lung metastases of hepatocellular carcinoma: a case report. J Med Case Rep 2011, 5:111.
57. Cotter S.E., Dunn G.P., Collins K.M., Sahni D., Zukotynski K.A., Hansen J.L., et al. Abscopal effect in a patient with metastatic Merkel cell carcinoma following radiation therapy: potential role of induced antitumor immunity. Arch Dermatol 2011, 147(7):870-872.
58. Lakshmanagowda P.B., Viswanath L., Thimmaiah N., Dasappa L., Supe S.S., Kallur P. Abscopal effect in a patient with chronic lymphocytic leukemia during radiation therapy: a case report. Cases J 2009, 2:204.
59. Takaya M., Niibe Y., Tsunoda S., Jobo T., Imai M., Kotani S., et al. Abscopal effect of radiation on toruliform para-aortic lymph node metastases of advanced uterine cervical carcinoma - a case report. Anticancer Res 2007, 27(1):499-503.
60. Wersall P.J., Blomgren H., Pisa P., Lax I., Kalkner K.M., Svedman C. Regression of non-irradiated metastases after extracranial stereotactic radiotherapy in metastatic renal cell carcinoma. Acta Oncol 2006, 45(4):493-497.
61. Nam S.W., Han J.Y., Kim J.I., Park S.H., Cho S.H., Han N.I., et al. Spontaneous regression of a large hepatocellular carcinoma with skull metastasis. J Gastroenterol Hepatol 2005, 20(3):488-492.
62. Sham R.L. The abscopal effect and chronic lymphocytic leukemia. Am J Med 1995, 98(3):307-308.
63. MacManus M.P., Harte R.J., Stranex S. Spontaneous regression of metastatic renal cell carcinoma following palliative irradiation of the primary tumour. Ir J Med Sci 1994, 163(10):461-463.
64. Rees G.J., Ross C.M. Abscopal regression following radiotherapy for adenocarcinoma. Br J Radiol 1983, 56(661):63-66.
65. Fairlamb D.J. Spontaneous regression of metastases of renal cancer: a report of two cases including the first recorded regression following irradiation of a dominant metastasis and review of the world literature. Cancer 1981, 47(8):2102-2106.
66. Antoniades J., Brady L.W., Lightfoot D.A. Lymphangiographic demonstration of the abscopal effect in patients with malignant lymphomas. Int J Radiat Oncol Biol Phys 1977, 2(1-2):141-147.
67. Kingsley D.P. An interesting case of possible abscopal effect in malignant melanoma. Br J Radiol 1975, 48(574):863-866.
68. Ehlers G., Fridman M. Abscopal effect of radiation in papillary adenocarcinoma. Br J Radiol 1973, 46(543):220-222.
69. Kodama K., Higashiyama M., Okami J., Tokunaga T., Inoue N., Akazawa T., et al. A possible abscopal effect of post-irradiation immunotherapy in two patients with metastatic lung tumors. Int Cancer Conf J 2014, 3(2):122-127.