Achieving the cure of follicular lymphoma: is it time to finalize treatment strategies to reach this goal in a subset of patients?
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Follicular lymphoma, very long responders
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1. Bachy E, Seymour JF, Feugier P, Offner F, López-Guillermo A, Belada D, Xerri L, Catalano JV, Brice P, Lemonnier F, Martin A, Casasnovas O, Pedersen LM, Dorvaux V, Simpson D, Leppa S, Gabarre J, da Silva MG, Glaisner S, Ysebaert L, Vekhoff A, Intragumtornchai T, Le Gouill S, Lister A, Estell JA, Milone G, Sonet A, Farhi J, Zeuner H, Tilly H, Salles G. Sustained Progression-Free Survival Benefit of Rituximab Maintenance in Patients With Follicular Lymphoma: Long-Term Results of the PRIMA Study. J Clin Oncol. 2019 Nov 1;37(31):2815-2824. doi: 10.1200/JCO.19.01073. Epub 2019 Jul 24.
2. Bruna R, Benedetti F, Boccomini C, Patti C, Barbui AM, Pulsoni A, Musso M, Liberati AM, Gini G, Castellino C, Rossini F, Ciceri F, Rota-Scalabrini D, Stelitano C, Di Raimondo F, Tucci A, Devizzi L, Zoli V, Zallio F, Narni F, Dondi A, Parvis G, Semenzato G, Lanza F, Perrone T, Angrilli F, Billio A, Gueli A, Mantoan B, Rambaldi A, Gianni AM, Corradini P, Passera R, Ladetto M, Tarella C. Prolonged survival in the absence of disease-recurrence in advanced-stage follicular lymphoma following chemo-immunotherapy: 13-year update of the prospective, multicenter randomized GITMO-IIL trial. Haematologica. 2019 Nov;104(11):2241-2248.
3. Rummel MJ, Niederle N, Maschmeyer G, Banat GA, von Grünhagen U, Losem C, Kofahl-Krause D, Heil G, Welslau M, Balser C, Kaiser U, Weidmann E, Dürk H, Ballo H, Stauch M, Roller F, Barth J, Hoelzer D, Hinke A, Brugger W; Study group indolent Lymphomas (StiL). Bendamustine plus rituximab versus CHOP plus rituximab as first-line treatment for patients with indolent and mantle-cell lymphomas: an open-label, multicentre, randomised, phase 3 non-inferiority trial. Lancet. 2013 Apr 6;381(9873):1203-10.
4. Luminari S, Ferrari A, Manni M, Dondi A, Chiarenza A, Merli F, Rusconi C, Tarantino V, Tucci A, Vitolo U, Kovalchuk S, Angelucci E, Pulsoni A, Arcaini L, Angrilli F, Gaidano G, Stelitano C, Bertoldero G, Cascavilla N, Salvi F, Ferreri AJM, Vallisa D, Marcheselli L, Federico M. Long-Term Results of the FOLL05 Trial Comparing R-CVP Versus R-CHOP Versus R-FM for the Initial Treatment of Patients With Advanced-Stage Symptomatic Follicular Lymphoma. J Clin Oncol. 2018 Mar 1;36(7):689-696.
5. Brice P., Bastion Y., Lepage E., Brousse N., Haioun C., Moreau P., Straetmans N., Tilly H., Tabah I., Solal-Céligny P. Comparison in low-tumor-burden follicular lymphomas between an initial no-treatment policy, prednimustine, or interferon alfa: A randomized study from the Groupe d’Etude des Lymphomes Folliculaires. Groupe d’Etude des Lymphomes de l’Adulte. J. Clin. Oncol. 1997;15:1110–1117. doi: 10.1200/JCO.1997.15.3.1110.
6. Rossi C, Tosolini M, Gravelle P, Pericart S, Kanoun S, Evrard S, Gilhodes J, Franchini DM, Amara N, Syrykh C, Bories P, Oberic L, Ysebaert L, Martin L, Ramla S, Robert P, Tabouret-Viaud C, Casasnovas RO, Fournié JJ, Bezombes C, Laurent C. Baseline SUVmax is related to tumor cell proliferation and patient outcome in follicular lymphoma. Haematologica. 2022 Jan 1;107(1):221-230. doi: 10.3324/haematol.2020.263194. PMID: 33327711; PMCID: PMC8719066.
7. Hiddemann W, Barbui AM, Canales MA, Cannell PK, Collins GP, Dürig J, Forstpointner R, Herold M, Hertzberg M, Klanova M, Radford J, Seymour JF, Tobinai K, Trotman J, Burciu A, Fingerle-Rowson G, Wolbers M, Nielsen T, Marcus RE. Immunochemotherapy With Obinutuzumab or Rituximab for Previously Untreated Follicular Lymphoma in the GALLIUM Study: Influence of Chemotherapy on Efficacy and Safety. J Clin Oncol. 2018 Aug 10;36(23):2395-2404. doi: 10.1200/JCO.2017.76.8960. Epub 2018 Jun 1. PMID: 29856692.
8. Armitage JO, Weisenburger DD. New approach to classifying non-Hodgkin's lymphomas: clinical features of the major histologic subtypes. Non-Hodgkin's Lymphoma Classification Project. J Clin Oncol. 1998 Aug;16(8):2780-95. doi: 10.1200/JCO.1998.16.8.2780. PMID: 9704731.
9. Federico M, Bellei M, Marcheselli L, Luminari S, Lopez-Guillermo A, Vitolo U, Pro B, Pileri S, Pulsoni A, Soubeyran P, Cortelazzo S, Martinelli G, Martelli M, Rigacci L, Arcaini L, Di Raimondo F, Merli F, Sabattini E, McLaughlin P, Solal-Céligny P. Follicular lymphoma international prognostic index 2: a new prognostic index for follicular lymphoma developed by the international follicular lymphoma prognostic factor project. J Clin Oncol. 2009 Sep 20;27(27):4555-62. doi: 10.1200/JCO.2008.21.3991. Epub 2009 Aug 3. PMID: 19652063.
10. Friedberg JW. Toward a Cure for Follicular Lymphoma. Hematol Oncol Clin North Am. 2020 Aug;34(4):xiii-xiv. doi: 10.1016/j.hoc.2020.05.001. Epub 2020 May 20. PMID: 32586582.
11. Assanto GM, Ciotti G, Brescini M, et al. High Basal Maximal Standardized Uptake Value (SUVmax) in Follicular Lymphoma Identifies Patients with a Low Risk of Long-Term Relapse. Cancers (Basel). 2021;13(12):2876. Published 2021 Jun 9. doi:10.3390/cancers13122876
12. Pulsoni A., Tosti ME, Ferrero S, Luminari S, Liberati AM at al; EARLY STAGE Follicular Lymphoma: First Results of the FIL “Miro” Study, a Multicenter Phase II Trial Combining Local Radiotherapy and MRD-Driven Immunotherapy. Blood 2019; 134 (Supplement_1): 124.
13. Ladetto M, Ferrero S, Del Giudice I, Galimberti S, et al; A Comprehensive and Systematic Analysis of Minimal Residual Disease (MRD) Monitoring in Follicular Lymphoma: Results from the Fondazione Italiana Linfomi (FIL) FOLL12 Trial. Blood 2021; 138 (Supplement 1)
14. Major A, Hammes A, Schmidt MQ, Morgan R, Abbott D, Kamdar M. Evaluating Novel PET-CT Functional Parameters TLG and TMTV in Differentiating Low-grade Versus Grade 3A Follicular Lymphoma. Clin Lymphoma Myeloma Leuk. 2020 Jan;20(1):39-46. doi: 10.1016/j.clml.2019.09.609. Epub 2019 Sep 28. PMID: 31761712.
15. Jacobson CA, Chavez JC, Sehgal AR, William BM, Munoz J, Salles G, Munshi PN, Casulo C, Maloney DG, de Vos S, Reshef R, Leslie LA, Yakoub-Agha I, Oluwole OO, Fung HCH, Rosenblatt J, Rossi JM, Goyal L, Plaks V, Yang Y, Vezan R, Avanzi MP, Neelapu SS. Axicabtagene ciloleucel in relapsed or refractory indolent non-Hodgkin lymphoma (ZUMA-5): a single-arm, multicentre, phase 2 trial. Lancet Oncol. 2022 Jan;23(1):91-103. doi: 10.1016/S1470-2045(21)00591-X. Epub 2021 Dec 8. PMID: 34895487.
16. Budde LE, Assouline S, Sehn LH, Schuster SJ, Yoon SS, Yoon DH, Matasar MJ, Bosch F, Kim WS, Nastoupil LJ, Flinn IW, Shadman M, Diefenbach C, O'Hear C, Huang H, Kwan A, Li CC, Piccione EC, Wei MC, Yin S, Bartlett NL. Single-Agent Mosunetuzumab Shows Durable Complete Responses in Patients With Relapsed or Refractory B-Cell Lymphomas: Phase I Dose-Escalation Study. J Clin Oncol. 2022 Feb 10;40(5):481-491. doi: 10.1200/JCO.21.00931. Epub 2021 Dec 16. PMID: 34914545; PMCID: PMC8824395.
17. Giudice ID, Starza ID, Foà R. Does MRD have a role in the management of iNHL? Hematology Am Soc Hematol Educ Program. 2021 Dec 10;2021(1):320-330. doi: 10.1182/hematology.2021000312. PMID: 34889425.
1. Bachy E, Seymour JF, Feugier P, Offner F, López-Guillermo A, Belada D, Xerri L, Catalano JV, Brice P, Lemonnier F, Martin A, Casasnovas O, Pedersen LM, Dorvaux V, Simpson D, Leppa S, Gabarre J, da Silva MG, Glaisner S, Ysebaert L, Vekhoff A, Intragumtornchai T, Le Gouill S, Lister A, Estell JA, Milone G, Sonet A, Farhi J, Zeuner H, Tilly H, Salles G. Sustained Progression-Free Survival Benefit of Rituximab Maintenance in Patients With Follicular Lymphoma: Long-Term Results of the PRIMA Study. J Clin Oncol. 2019 Nov 1;37(31):2815-2824. doi: 10.1200/JCO.19.01073. Epub 2019 Jul 24.
2. Bruna R, Benedetti F, Boccomini C, Patti C, Barbui AM, Pulsoni A, Musso M, Liberati AM, Gini G, Castellino C, Rossini F, Ciceri F, Rota-Scalabrini D, Stelitano C, Di Raimondo F, Tucci A, Devizzi L, Zoli V, Zallio F, Narni F, Dondi A, Parvis G, Semenzato G, Lanza F, Perrone T, Angrilli F, Billio A, Gueli A, Mantoan B, Rambaldi A, Gianni AM, Corradini P, Passera R, Ladetto M, Tarella C. Prolonged survival in the absence of disease-recurrence in advanced-stage follicular lymphoma following chemo-immunotherapy: 13-year update of the prospective, multicenter randomized GITMO-IIL trial. Haematologica. 2019 Nov;104(11):2241-2248.
3. Rummel MJ, Niederle N, Maschmeyer G, Banat GA, von Grünhagen U, Losem C, Kofahl-Krause D, Heil G, Welslau M, Balser C, Kaiser U, Weidmann E, Dürk H, Ballo H, Stauch M, Roller F, Barth J, Hoelzer D, Hinke A, Brugger W; Study group indolent Lymphomas (StiL). Bendamustine plus rituximab versus CHOP plus rituximab as first-line treatment for patients with indolent and mantle-cell lymphomas: an open-label, multicentre, randomised, phase 3 non-inferiority trial. Lancet. 2013 Apr 6;381(9873):1203-10.
4. Luminari S, Ferrari A, Manni M, Dondi A, Chiarenza A, Merli F, Rusconi C, Tarantino V, Tucci A, Vitolo U, Kovalchuk S, Angelucci E, Pulsoni A, Arcaini L, Angrilli F, Gaidano G, Stelitano C, Bertoldero G, Cascavilla N, Salvi F, Ferreri AJM, Vallisa D, Marcheselli L, Federico M. Long-Term Results of the FOLL05 Trial Comparing R-CVP Versus R-CHOP Versus R-FM for the Initial Treatment of Patients With Advanced-Stage Symptomatic Follicular Lymphoma. J Clin Oncol. 2018 Mar 1;36(7):689-696.
5. Brice P., Bastion Y., Lepage E., Brousse N., Haioun C., Moreau P., Straetmans N., Tilly H., Tabah I., Solal-Céligny P. Comparison in low-tumor-burden follicular lymphomas between an initial no-treatment policy, prednimustine, or interferon alfa: A randomized study from the Groupe d’Etude des Lymphomes Folliculaires. Groupe d’Etude des Lymphomes de l’Adulte. J. Clin. Oncol. 1997;15:1110–1117. doi: 10.1200/JCO.1997.15.3.1110.
6. Rossi C, Tosolini M, Gravelle P, Pericart S, Kanoun S, Evrard S, Gilhodes J, Franchini DM, Amara N, Syrykh C, Bories P, Oberic L, Ysebaert L, Martin L, Ramla S, Robert P, Tabouret-Viaud C, Casasnovas RO, Fournié JJ, Bezombes C, Laurent C. Baseline SUVmax is related to tumor cell proliferation and patient outcome in follicular lymphoma. Haematologica. 2022 Jan 1;107(1):221-230. doi: 10.3324/haematol.2020.263194. PMID: 33327711; PMCID: PMC8719066.
7. Hiddemann W, Barbui AM, Canales MA, Cannell PK, Collins GP, Dürig J, Forstpointner R, Herold M, Hertzberg M, Klanova M, Radford J, Seymour JF, Tobinai K, Trotman J, Burciu A, Fingerle-Rowson G, Wolbers M, Nielsen T, Marcus RE. Immunochemotherapy With Obinutuzumab or Rituximab for Previously Untreated Follicular Lymphoma in the GALLIUM Study: Influence of Chemotherapy on Efficacy and Safety. J Clin Oncol. 2018 Aug 10;36(23):2395-2404. doi: 10.1200/JCO.2017.76.8960. Epub 2018 Jun 1. PMID: 29856692.
8. Armitage JO, Weisenburger DD. New approach to classifying non-Hodgkin's lymphomas: clinical features of the major histologic subtypes. Non-Hodgkin's Lymphoma Classification Project. J Clin Oncol. 1998 Aug;16(8):2780-95. doi: 10.1200/JCO.1998.16.8.2780. PMID: 9704731.
9. Federico M, Bellei M, Marcheselli L, Luminari S, Lopez-Guillermo A, Vitolo U, Pro B, Pileri S, Pulsoni A, Soubeyran P, Cortelazzo S, Martinelli G, Martelli M, Rigacci L, Arcaini L, Di Raimondo F, Merli F, Sabattini E, McLaughlin P, Solal-Céligny P. Follicular lymphoma international prognostic index 2: a new prognostic index for follicular lymphoma developed by the international follicular lymphoma prognostic factor project. J Clin Oncol. 2009 Sep 20;27(27):4555-62. doi: 10.1200/JCO.2008.21.3991. Epub 2009 Aug 3. PMID: 19652063.
10. Friedberg JW. Toward a Cure for Follicular Lymphoma. Hematol Oncol Clin North Am. 2020 Aug;34(4):xiii-xiv. doi: 10.1016/j.hoc.2020.05.001. Epub 2020 May 20. PMID: 32586582.
11. Assanto GM, Ciotti G, Brescini M, et al. High Basal Maximal Standardized Uptake Value (SUVmax) in Follicular Lymphoma Identifies Patients with a Low Risk of Long-Term Relapse. Cancers (Basel). 2021;13(12):2876. Published 2021 Jun 9. doi:10.3390/cancers13122876
12. Pulsoni A., Tosti ME, Ferrero S, Luminari S, Liberati AM at al; EARLY STAGE Follicular Lymphoma: First Results of the FIL “Miro” Study, a Multicenter Phase II Trial Combining Local Radiotherapy and MRD-Driven Immunotherapy. Blood 2019; 134 (Supplement_1): 124.
13. Ladetto M, Ferrero S, Del Giudice I, Galimberti S, et al; A Comprehensive and Systematic Analysis of Minimal Residual Disease (MRD) Monitoring in Follicular Lymphoma: Results from the Fondazione Italiana Linfomi (FIL) FOLL12 Trial. Blood 2021; 138 (Supplement 1)
14. Major A, Hammes A, Schmidt MQ, Morgan R, Abbott D, Kamdar M. Evaluating Novel PET-CT Functional Parameters TLG and TMTV in Differentiating Low-grade Versus Grade 3A Follicular Lymphoma. Clin Lymphoma Myeloma Leuk. 2020 Jan;20(1):39-46. doi: 10.1016/j.clml.2019.09.609. Epub 2019 Sep 28. PMID: 31761712.
15. Jacobson CA, Chavez JC, Sehgal AR, William BM, Munoz J, Salles G, Munshi PN, Casulo C, Maloney DG, de Vos S, Reshef R, Leslie LA, Yakoub-Agha I, Oluwole OO, Fung HCH, Rosenblatt J, Rossi JM, Goyal L, Plaks V, Yang Y, Vezan R, Avanzi MP, Neelapu SS. Axicabtagene ciloleucel in relapsed or refractory indolent non-Hodgkin lymphoma (ZUMA-5): a single-arm, multicentre, phase 2 trial. Lancet Oncol. 2022 Jan;23(1):91-103. doi: 10.1016/S1470-2045(21)00591-X. Epub 2021 Dec 8. PMID: 34895487.
16. Budde LE, Assouline S, Sehn LH, Schuster SJ, Yoon SS, Yoon DH, Matasar MJ, Bosch F, Kim WS, Nastoupil LJ, Flinn IW, Shadman M, Diefenbach C, O'Hear C, Huang H, Kwan A, Li CC, Piccione EC, Wei MC, Yin S, Bartlett NL. Single-Agent Mosunetuzumab Shows Durable Complete Responses in Patients With Relapsed or Refractory B-Cell Lymphomas: Phase I Dose-Escalation Study. J Clin Oncol. 2022 Feb 10;40(5):481-491. doi: 10.1200/JCO.21.00931. Epub 2021 Dec 16. PMID: 34914545; PMCID: PMC8824395.
17. Giudice ID, Starza ID, Foà R. Does MRD have a role in the management of iNHL? Hematology Am Soc Hematol Educ Program. 2021 Dec 10;2021(1):320-330. doi: 10.1182/hematology.2021000312. PMID: 34889425.
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Feb 28, 2023
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Passucci, M., Assanto, G. and Pulsoni, A. (2023) “Achieving the cure of follicular lymphoma: is it time to finalize treatment strategies to reach this goal in a subset of patients?”, Mediterranean Journal of Hematology and Infectious Diseases, 15(1), p. e2023018. doi: 10.4084/MJHID.2023.018.
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