Localized low-dose radiotherapy for follicular lymphoma: History, clinical results, mechanisms of action, and future outlooks

International Journal of Radiation Oncology Biology Physics

Volumn 78, Issue 4, 2010, Pages 975-982

  Ganem, Gérard ^a   Cartron, Guillaume ^b   Girinsky, Théodore ^c   Haas, Rick L M ^d   Cosset, Jean Marc ^e   Solal Celigny, Philippe ^a  

^a CENTRE JEAN BERNARD   (France)

^b LAPEYRONIE HOSPITAL   (France)

^c INSTITUT GUSTAVE ROUSSY   (France)

^d NETHERLANDS CANCER INSTITUTE   (Netherlands)

^e INSTITUT CURIE   (France)

Author keywords

indolent lymphoma; Low dose radiotherapy; mechanisms of action of radiotherapy

Indexed keywords

CELL DEATH; ONCOLOGY; PATIENT MONITORING; POPULATION STATISTICS;

APOPTOSIS; APOPTOTIC CELL DEATH; CLINICAL OBSERVATION; COMPLETE RESPONSE; DENDRITIC CELLS; FOLLICULAR LYMPHOMA; HIGH EFFICACY; IDEAL MODEL; IMMUNE RESPONSE; INDOLENT LYMPHOMA; LOW DOSE; LYMPHOMA CELLS; NON-HODGKIN'S LYMPHOMA; RADIATION DOSE; TOTAL BODY IRRADIATION;

RADIOTHERAPY;

CASPASE 8; CXCL9 CHEMOKINE; PROTEIN BAX; PROTEIN P53;

APOPTOSIS; BONE MARROW TRANSPLANTATION; CANCER CELL; CANCER IMMUNOTHERAPY; CANCER RELAPSE; CANCER SURVIVAL; CELL DEATH; CLINICAL EVALUATION; CLINICAL FEATURE; DENDRITIC CELL; FOLLICULAR LYMPHOMA; GENE EXPRESSION; HUMAN; IMMUNE RESPONSE; IN VITRO STUDY; LARGE CELL LYMPHOMA; MACROPHAGE; NONHODGKIN LYMPHOMA; PRIORITY JOURNAL; RADIATION DOSE; REVIEW; TREATMENT DURATION; WHOLE BODY RADIATION; FORECASTING; IMMUNITY; IMMUNOTHERAPY; LYMPHOMA, FOLLICULAR; LYMPHOMA, NON-HODGKIN; PATHOLOGY; PROCEDURES; RADIATION RESPONSE;

APOPTOSIS; FORECASTING; HUMANS; IMMUNITY; IMMUNOTHERAPY; LYMPHOMA, FOLLICULAR; LYMPHOMA, NON-HODGKIN; RADIATION TOLERANCE; RADIOTHERAPY DOSAGE;

EID: 77958495889     PISSN: 03603016     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijrobp.2010.06.056     Document Type: Review

References (68)

1. E.B. Hicks, H. Rappaport, and W.J. Winter Follicular lymphoma: A re-evaluation of its position in the scheme of malignant lymphoma, based on a survey of 253 cases Cancer 9 1956 792 821
2. S.E. Jones, Z. Fuks, and H.S. Kaplan Non-Hodgkin's lymphomas. V. Results of radiotherapy Cancer 32 1973 682 691
3. M.V. Peters The contribution of radiation therapy in the control of early lymphomas Am J Roentgenol Radium Ther Nucl Med 90 1963 956 967
4. S.C. Carabell, J.T. Chaffey, and D.S. Rosenthal Results of total body irradiation in the treatment of advanced non-Hodgkin's lymphomas Cancer 43 1979 994 1000
5. R.T. Hoppe, P. Kushlan, and H.S. Kaplan The treatment of advanced stage favorable histology non-Hodgkin's lymphoma: A preliminary report of a randomized trial comparing single agent chemotherapy, combination chemotherapy, and whole body irradiation Blood 58 1981 592 598
6. R.E. Johnson Management of generalized malignant lymphomata with "systemic" radiotherapy Br J Cancer Suppl 2 1975 450 455
7. S. Hellman, J.T. Chaffey, and D.S. Rosenthal The place of radiation therapy in the treatment of non-Hodgkin's lymphomas Cancer 39 1977 843 851 (Pubitemid 8060274)
8. M.G. Chen, L.R. Prosnitz, and A. Gonzalez-Serva Results of radiotherapy in control of stage I and II non-Hodgkin's lymphoma Cancer 43 1979 1245 1254
9. R.T. Hoppe The role of radiation therapy in the management of the non-Hodgkin's lymphomas Cancer 55 1985 2176 2183
10. M.K. Gospodarowicz, R.S. Bush, and T.C. Brown Prognostic factors in nodular lymphomas: A multivariate analysis based on the Princess Margaret Hospital experience Int J Radiat Oncol Biol Phys 10 1984 489 497
11. S.B. Sutcliffe, M.K. Gospodarowicz, and R.S. Bush Role of radiation therapy in localized non-Hodgkin's lymphoma Radiother Oncol 4 1985 211 223
12. M.P. MacManus, and R.T. Hoppe Is radiotherapy curative for stage I and II low-grade follicular lymphoma? Results of a long-term follow-up study of patients treated at Stanford University J Clin Oncol 14 1996 1282 1290
13. S.B. Paryani, R.T. Hoppe, and R.S. Cox Analysis of non-Hodgkin's lymphomas with nodular and favorable histologies, stages I and II Cancer 52 1983 2300 2307
14. B. Vaughan Hudson, G. Vaughan Hudson, and K.A. Mac Lennan Clinical stage I non Hodgkin's lymphoma: Long-term follow-up of patients treated by the British National Lymphoma Investigation with radiotherapy alone as initial therapy Br J Cancer 69 1994 1088 1093
15. S. Pendlebury, M. el Awadi, and S. Ashley Radiotherapy results in early stage low grade nodal non-Hodgkin's lymphoma Radiother Oncol 36 1995 167 171
16. R.B. Wilder, D. Jones, and S.L. Tucker Long-term results with radiotherapy for stage I-II follicular lymphomas Int J Radiat Oncol Biol Phys 51 2001 1219 1227
17. J.D. Cox, R.H. Koehl, and W.M. Turner Irradiation in the local control of malignant lymphoreticular tumors (non-Hodgkin's malignant lymphoma) Radiology 112 1974 179 185
18. K. Musshoff, and H. Leopold On the question of the tumoricidal dose in non-Hodgkin's lymphomas Recent Results Cancer Res 65 1978 203 206
19. M.L. Lybeert, J.H. Meerwaldt, and W. Deneve Long-term results of low dose total body irradiation for advanced non-Hodgkin lymphoma Int J Radiat Oncol Biol Phys 13 1987 1167 1172
20. N.P. Mendenhall, W.D. Noyes, and R.R. Million Total body irradiation for stage II-IV non-Hodgkin's lymphoma: Ten-year follow-up J Clin Oncol 7 1989 67 74
21. G.M. Duchesne, and C.L. Harmer Hemibody irradiation in lymphomas and related malignancies Int J Radiat Oncol Biol Phys 11 1985 2003 2006
22. C.W. Scarantino, K.M. Greven, and D.H. Buss Single high dose-large field irradiation in drug resistant non-Hodgkin's lymphoma Int J Radiat Oncol Biol Phys 14 1988 1001 1005
23. J.J. Cohen, R.C. Duke, and R. Chervenak DNA fragmentation in targets of CTL: An example of programmed cell death in the immune system Adv Exp Med Biol 184 1985 493 508
24. K.S. Sellins, and J.J. Cohen Gene induction by gamma-irradiation leads to DNA fragmentation in lymphocytes J Immunol 139 1987 3199 3206
25. G. Ganem, P. Lambin, and G. Socie Potential role for low dose limited-field radiation therapy (2 × 2 Grays) in advanced low-grade non-Hodgkin's lymphomas Hematol Oncol 12 1994 1 8
26. E.J. Sawyer, and A.R. Timothy Low dose palliative radiotherapy in low grade non-Hodgkin's lymphoma Radiother Oncol 42 1997 49 51
27. T. Girinsky, D. Guillot-Vals, and S. Koscielny A high and sustained response rate in refractory or relapsing low-grade lymphoma masses after low-dose radiation: Analysis of predictive parameters of response to treatment Int J Radiat Oncol Biol Phys 51 2001 148 155
28. J. Johannsson, L. Specht, and J. Mejer Phase II study of palliative low-dose local radiotherapy in disseminated indolent non-Hodgkin's lymphoma and chronic lymphocytic leukemia Int J Radiat Oncol Biol Phys 54 2002 1466 1470
29. R.L. Haas, P. Poortmans, and D. de Jong High response rates and lasting remissions after low-dose involved field radiotherapy in indolent lymphomas J Clin Oncol 21 2003 2474 2480
30. R.L. Haas, P. Poortmans, and D. de Jong Effective palliation by low dose local radiotherapy for recurrent and/or chemotherapy refractory non-follicular lymphoma patients Eur J Cancer 41 2005 1724 1730
31. V. Murthy, K. Thomas, and K. Foo Efficacy of palliative low-dose involved-field radiation therapy in advanced lymphoma: A phase II study Clin Lymphoma Myeloma 8 2008 241 245
32. S.K. Luthy, A.K. Ng, and B. Silver Response to low-dose involved-field radiotherapy in patients with non-Hodgkin's lymphoma Ann Oncol 19 2008 2043 2047
33. K.J. Neelis, E.C. Schimmel, and M.H. Vermeer Low-dose palliative radiotherapy for cutaneous B- and T-cell lymphomas Int J Radiat Oncol Biol Phys 74 2009 154 158
34. R.L. Haas, T. Girinsky, and B.M. Aleman Low-dose involved-field radiotherapy as alternative treatment of nodular lymphocyte predominance Hodgkin's lymphoma Int J Radiat Oncol Biol Phys 74 2009 1199 1202
35. B. Dubray, C. Breton, and J. Delic In vitro radiation-induced apoptosis and early response to low-dose radiotherapy in non-Hodgkin's lymphomas Radiother Oncol 46 1998 185 191
36. R.L. Haas, D. de Jong, and R.A. Valdes Olmos In vivo imaging of radiation-induced apoptosis in follicular lymphoma patients Int J Radiat Oncol Biol Phys 59 2004 782 787
37. D.M. Langenau, C. Jette, and S. Berghmans Suppression of apoptosis by bcl-2 overexpression in lymphoid cells of transgenic zebrafish Blood 105 2005 3278 3285
38. L. Knoops, R. Haas, and S. de Kemp In vivo p53 response and immune reaction underlie highly effective low-dose radiotherapy in follicular lymphoma Blood 110 2007 1116 1122
39. L. Knoops, and D. de Jong The role of the p53 pathway in the treatment of follicular lymphoma Cell Cycle 7 2008 436 439
40. D. O'Shea, C. O'Riain, and C. Taylor The presence of TP53 mutation at diagnosis of follicular lymphoma identifies a high-risk group of patients with shortened time to disease progression and poorer overall survival Blood 112 2008 3126 3129
41. K.H. Young, K. Leroy, and M.B. Moller Structural profiles of TP53 gene mutations predict clinical outcome in diffuse large B-cell lymphoma: an international collaborative study Blood 112 2008 3088 3098
42. N. Zainuddin, M. Berglund, and A. Wanders TP53 mutations predict for poor survival in de novo diffuse large B-cell lymphoma of germinal center subtype Leuk Res 33 2009 60 66
43. M. Obeid, T. Panaretakis, and N. Joza Calreticulin exposure is required for the immunogenicity of gamma-irradiation and UVC light-induced apoptosis Cell Death Differ 14 2007 1848 1850
44. L. Zitvogel, L. Apetoh, and F. Ghiringhelli Immunological aspects of cancer chemotherapy Nat Rev Immunol 8 2008 59 73
45. L. Apetoh, F. Ghiringhelli, and A. Tesniere Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy Nat Med 13 2007 1050 1059
46. S.S. Dave, G. Wright, and B. Tan Prediction of survival in follicular lymphoma based on molecular features of tumor-infiltrating immune cells N Engl J Med 351 2004 2159 2169
47. D. de Jong Molecular pathogenesis of follicular lymphoma: A cross talk of genetic and immunologic factors J Clin Oncol 23 2005 6358 6363
48. A.M. Lee, A.J. Clear, and M. Calaminici Number of CD4+ cells and location of forkhead box protein P3-positive cells in diagnostic follicular lymphoma tissue microarrays correlates with outcome J Clin Oncol 24 2006 5052 5059
49. J. Carreras, A. Lopez-Guillermo, and G. Roncador High numbers of tumor-infiltrating programmed cell death 1-positive regulatory lymphocytes are associated with improved overall survival in follicular lymphoma J Clin Oncol 27 2009 1470 1476
50. S.C. Formenti, and S. Demaria Systemic effects of local radiotherapy Lancet Oncol 10 2009 718 726
51. M.P. Nobler The abscopal effect in malignant lymphoma and its relationship to lymphocyte circulation Radiology 93 1969 410 412
52. J. Antoniades, L.W. Brady, and D.A. Lightfoot Lymphangiographic demonstration of the abscopal effect in patients with malignant lymphomas Int J Radiat Oncol Biol Phys 2 1977 141 147
53. R.L. Sham The abscopal effect and chronic lymphocytic leukemia Am J Med 98 1995 307 308
54. H.I. Robin, J. AuBuchon, and V.R. Varanasi The abscopal effect: demonstration in lymphomatous involvement of kidneys Med Pediatr Oncol 9 1981 473 476
55. S. Kusmartsev, and D.I. Gabrilovich Immature myeloid cells and cancer-associated immune suppression Cancer Immunol Immunother 51 2002 293 298
56. P.K. Chakravarty, A. Alfieri, and E.K. Thomas Flt3-ligand administration after radiation therapy prolongs survival in a murine model of metastatic lung cancer Cancer Res 59 1999 6028 6032
57. S. Demaria, B. Ng, and M.L. Devitt Ionizing radiation inhibition of distant untreated tumors (abscopal effect) is immune mediated Int J Radiat Oncol Biol Phys 58 2004 862 870
58. E.A. Reits, J.W. Hodge, and C.A. Herberts Radiation modulates the peptide repertoire, enhances MHC class I expression, and induces successful antitumor immunotherapy J Exp Med 203 2006 1259 1271
59. K. Shiraishi, Y. Ishiwata, and K. Nakagawa 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 14 2008 1159 1166
60. Y. Lee, S.L. Auh, and Y. Wang Therapeutic effects of ablative radiation on local tumor require CD8+ T cells: Changing strategies for cancer treatment Blood 114 2009 589 595
61. Hovon study Web site. Available from: www.hovon.nl. Accessed September 15, 2010.
62. P. Colombat, G. Salles, and N. Brousse Rituximab (anti-CD20 monoclonal antibody) as single first-line therapy for patients with follicular lymphoma with a low tumor burden: Clinical and molecular evaluation Blood 97 2001 101 106
63. FoRT study. Available from: www.ctc.ucl.ac.uk./TrialDetails.aspx?TrialID= 18. Accessed September 15, 2010.
64. J. Brody, W.Z. Ai, and D. Czerwinski Clinical and immunologic responses to a novel in situ lymphoma vaccine maneuver: Preliminary results of a phase II trial of intra-tumoral CpG 7909 [Abstract] Proc Am Soc Clin Oncol 26 Suppl. 2008 3003
65. G. Cartron, H. Watier, and J. Golay From the bench to the bedside: Ways to improve rituximab efficacy Blood 104 2004 2635 2642
66. S.N. Franki, K.K. Steward, and D.J. Betting Dendritic cells loaded with apoptotic antibody-coated tumor cells provide protective immunity against B-cell lymphoma in vivo Blood 111 2008 1504 1511
67. I. Skvortsova, B.A. Popper, and S. Skvortsov Pretreatment with rituximab enhances radiosensitivity of non-Hodgkin's lymphoma cells J Radiat Res (Tokyo) 46 2005 241 248
68. I. Skvortsova, S. Skvortsov, and B.A. Popper Rituximab enhances radiation-triggered apoptosis in non-Hodgkin's lymphoma cells via caspase-dependent and -independent mechanisms J Radiat Res (Tokyo) 47 2006 183 196