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Современная стратегия и перспективы лечения фолликулярной лимфомы. Значение результатов исследования BENEFIT
Современная стратегия и перспективы лечения фолликулярной лимфомы. Значение результатов исследования BENEFIT
Бабичева Л.Г., Поддубная И.В. Современная стратегия и перспективы лечения фолликулярной лимфомы. Значение результатов исследования BENEFIT. Современная Онкология. 2017; 19 (4): 7–15.
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Аннотация
Фолликулярная лимфома (ФЛ), как правило, характеризуется индолентным течением с высокой частотой общего ответа на терапию 1-й линии. При постановке диагноза у 80% пациентов выявляются генерализованные стадии заболевания. Инициация и выбор тактики лечения в основном обусловлены наличием В-симптомов, опухолевой нагрузкой, стадией лимфомы, сопутствующими заболеваниями и предпочтениями пациентов. При развитии ранних рецидивов и резистентном течении прогноз крайне неблагоприятный, необходимы новые терапевтические подходы. Режим бендамустин + ритуксимаб (BR), согласно большинству международных рекомендаций, является одним из основных вариантов лечения рецидивов ФЛ. Целью программы BENEFIT стала оценка эффективности и безопасности схемы BR с последующей поддерживающей терапией ритуксимабом у пациентов с рецидивами или рефрактерными вариантами индолентных неходжкинских лимфом в Российской Федерации. C июня 2012 по октябрь 2015 г. в программу включены 102 пациента, среди них 30 (36%) больных ФЛ. Общий эффект в подгруппе ФЛ составил 73,3%: полная ремиссия – 36,6% (подтвержденных – 23,3%, неподтвержденных – 13,3%), частичная ремиссия – 36,7%. Комбинация BR продемонстрировала высокую клиническую эффективность у пациентов с рецидивами и рефрактерными вариантами ФЛ и является одним из наиболее часто применяемых терапевтических подходов у данной категории пациентов. Тем не менее рецидивы и рефрактерные варианты ФЛ остаются неизлечимыми, что требует внедрения в программы лечения новых препаратов направленного действия.
Ключевые слова: фолликулярная лимфома, рецидив, рефрактерное течение, ритуксимаб, бендамустин, индолентная лимфома.
Key words: follicular lymphoma, relapse, refractory disease, rituximab, bendamustin, indolent lymphoma.
Ключевые слова: фолликулярная лимфома, рецидив, рефрактерное течение, ритуксимаб, бендамустин, индолентная лимфома.
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Key words: follicular lymphoma, relapse, refractory disease, rituximab, bendamustin, indolent lymphoma.
Полный текст
Список литературы
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2. Solal-Celigny P, Roy P, Colombat P et al. Follicular Lymphoma International Prognostic Index. Blood 2004; 104 (5): 1258–65.
3. Federico M, Bellei M, Marcheselli L et al. 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; 27 (27): 4555–62.
4. Pastore A, Jurinovic V, Kridel R et al. Integration of gene mutations in risk prognostication for patients receiving first-line immunochemotherapy for follicular lymphoma: a retrospective analysis of a prospective clinical trial and validation in a population-based registry. Lancet Oncol 2015; 16 (9): 1111–22.
5. Dave SS, Wright G, Tan B et al. Prediction of survival in follicular lymphoma based on molecular features of tumor-infiltrating immune cells. N Engl J Med 2004; 351 (21): 2159–69.
6. Wang W, Corrigan-Cummins M, Hudson J et al. MicroRNA profiling of follicular lymphoma identifies microRNAs related to cell proliferation and tumor response. Haematologica 2012; 97 (4): 586–94.
7. Scott DW, Gascoyne RD. The tumour microenvironment in B cell lymphomas. Nat Rev Cancer 2014; 14 (8): 517–34.
8. Sugimoto T, Watanabe T. Follicular lymphoma: the role of the tumor microenvironment in prognosis. J Clin Exp Hematop 2016; 56 (1): 1–19.
9. Canioni D, Salles G, Mounier N et al. High numbers of tumor-associated macrophages have an adverse prognostic value that can be circumvented by rituximab in patients with follicular lymphoma enrolled onto the GELA-GOELAMS FL-2000 trial. J Clin Oncol 2008; 26 (3): 440–6.
10. Kridel R, Xerri L, Gelas-Dore B et al. The prognostic impact of CD163-positive macrophages in follicular lymphoma: a study from the BC Cancer Agency and the Lymphoma Study Association. Clin Cancer Res 2015; 21 (15): 3428–35.
11. Smeltzer JP, Jones JM, Ziesmer SC et al. Pattern of CD14+ follicular dendritic cells and PD1+ T cells independently predicts time to transformation in follicular lymphoma. Clin Cancer Res 2014; 20 (11): 2862–72.
12. Sohani AR, Pitcher B, Chadburn A et al. Interfollicular CD10 expression and follicular PD1 tumor-infiltrating lymphocytes as biologic risk factors in patients with previously untreated follicular lymphoma receiving rituximab-based biologic therapy: an Alliance Correlative Science Study (CALGB 50901, 50402, 50701, 50803, 50401). Blood 2015; 126 (23): 334.
13. Cheson BD, Fisher RI, Barrington SF et al. Recommendations for initial evaluation, staging, and response assessment of Hodgkin and non-Hodgkin lymphoma: the Lugano classification. J Clin Oncol 2014; 32 (27): 3059–68.
14. Ansell SM, Armitage JO. Positron emission tomographic scans in lymphoma: convention and controversy. Mayo Clin Proc 2012; 87 (6): 571–80.
15. Meignan M, Cottereau AS, Versari A et al. Baseline metabolic tumor volume predicts outcome in high-tumor-burden follicular lymphoma: a pooled analysis of three multicenter studies. J Clin Oncol 2016; 34 (30): 3618–26.
16. Adams HJ, Kwee TC. Overestimated value of baseline total metabolic tumor volume at 18F-labeled fluorodeoxyglucose positron emission tomography in follicular lymphoma. J Clin Oncol 2017; 35 (8): 918–9.
17. Schöder H, Moskowitz C. Metabolic tumor volume in lymphoma: hype or hope? J Clin Oncol 2016; 34 (30): 3591–4.
18. Parraga I, Gimeno E, Pallerols FG et al. PET-CT and Bone Marrow Biopsy in staging Follicular Lymphoma in a single institution. Abstract PB1874; EHA Learning Center 2017 May18,182588. https://learningcenter.ehaweb.org/eha/2017/ 22nd/182588/ivonne.parraga. pet-ct.and.bone.marrow.biopsy.in. staging.folicular.lymphoma.in.html Assessed 4.12.2017.
19. López-Guillermo A, Cabanillas F, McLaughlin P et al. Molecular response assessed by PCR is the most important factor predicting failure-free survival in indolent follicular lymphoma: update of the MDACC series. Ann Oncol 2000; 11 (Suppl. 1): S137–S140.
20. Zohren F, Bruns I, Pechtel S et al. Prognostic value of circulating Bcl-2/IgH levels in patients with follicular lymphoma receiving first-line immunochemotherapy. Blood 2015; 126 (12): 1407–14.
21. Pott C, Hoster E, Kehden B et al. Minimal residual disease in patients with follicular lymphoma treated with obinutuzumab or rituximab as first-line induction Immunochemotherapy and maintenance in the phase 3 GALLIUM study. Blood 2016; 128 (22): 613.
22. Luminari S, Galimberti S, Versari A et al. Positron emission tomography response and minimal residual disease impact on progression-free survival in patients with follicular lymphoma. A subset analysis from the FOLL05 trial of the Fondazione Italiana Linfomi. Haematologica 2016; 101 (2): e66–8.
23. Conconi A, Ponzio C, Lobetti-Bodoni C et al. Incidence, risk factors and outcome of histological transformation in follicular lymphoma. Br J Haematol 2012; 157 (2): 188–96.
24. Link BK, Maurer MJ, Nowakowski GS et al. Rates and outcomes of follicular lymphoma transformation in the immunochemotherapy era: a report from the University of Iowa/MayoClinic Specialized Program of Research Excellence Molecular Epidemiology Resource. J Clin Oncol 2013; 31 (26): 3272–8.
25. Brice P, Bastion Y, Lepage E et al. 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 (3): 1110–7.
26. Young RC, Longo DL, Glatstein E et al. The treatment of indolent lymphomas: watchful waiting v aggressive combined modality treatment. Semin Hematol 1988; 25 (2 Suppl. 2): 11–6.
27. Al-Tourah AJ, Gill KK, Hoskins PJ et al. The impact of initial treatment of advanced stage indolent lymphoma on the risk of transformation. J Clin Oncol 2006; 24 (18): 7510.
28. Gine E, Montoto S, Bosch F et al. The Follicular Lymphoma International Prognostic Index (FLIPI) and the histological subtype are the most important factors to predict histological transformation in follicular lymphoma. Ann Oncol 2006; 17 (10): 1539–45.
29. Cheson BD, Horning SJ, Coiffier B et al. Report of an International workshop to standardize response criteria for non-Hodgkin’s lymphomas. NCI Sponsored International Working Group. J Clin Oncol 1999; 17 (4): 1244.
30. Advani R, Rosenberg SA, Horning SJ. Stage I and II follicular non-Hodgkin's lymphoma: long-term follow-up of no initial therapy. J Clin Oncol 2004; 22 (8): 1454–9.
31. Guadagnolo BA, Li S, Neuberg D et al. Long-term outcome and mortality trends in early-stage, Grade 1–2 follicular lymphoma treated with radiation therapy. Int J Radiat Oncol Biol Phys 2006; 64 (3): 928–34.
32. Skvortsova I, Popper BA, Skvortsov S et al. Pretreatment with rituximab enhances radiosensitivity of non-Hodgkin's lymphoma cells. J Radiat Res 2005; 46 (2): 241–8.
33. Ardeshna KM, Qian W, Smith P et al. Rituximab versus a watch-and-wait approach in patients with advanced-stage, asymptomatic, non-bulky follicular lymphoma: an open-label randomised phase 3 trial. Lancet Oncol 2014; 15 (4): 424–35.
34. Witzig TE, Vukov AM, Habermann TM et al. Rituximab therapy for patients with newly diagnosed, advanced-stage, follicular grade I non-Hodgkin's lymphoma: a phase II trial in the North Central Cancer Treatment Group. J Clin Oncol 2005; 23 (6): 1103–8.
35. Colombat P, Salles G, Brousse N et al. 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 2001; 97 (1): 101–6.
36. Martinelli G, Schmitz SF, Utiger U et al. Long-term follow-up of patients with follicular lymphoma receiving single-agent rituximab at two different schedules in trial SAKK 35/98. J Clin Oncol 2010; 28 (29): 4480–4.
37. Taverna C, Martinelli G, Hitz F et al. Rituximab Maintenance for a Maximum of 5 Years After Single-Agent Rituximab Induction in Follicular Lymphoma: Results of the Randomized Controlled Phase III Trial SAKK 35/03. J Clin Oncol 2016; 34 (5): 495–500.
38. Federico M, Luminari S, Dondi A et al. R-CVP versus R-CHOP versus R-FM for the initial treatment of patients with advanced-stage follicular lymphoma: results of the FOLL05 trial conducted by the Fondazione Italiana Linfomi. J Clin Oncol 2013; 31 (12): 1506–13.
39. Rummel MJ, Niederle N, Maschmeyer G et al. 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; 381 (9873): 1203–10.
40. Mondello P, Steiner N, Willenbacher W et al. Bendamustine plus rituximab versus R-CHOP as first-line treatment for patients with indolent non-Hodgkin’s lymphoma: evidence from a multicenter, retrospective study. Ann Hematol 2016; 95 (7): 1107–14.
41. Galimberti G, Ciabatti E, Ercolano G at al. The combination of rituximab and bendamustine as first-line treatment is highly effective in the eradicating minimal residual disease in follicular lymphoma: an Italian retrospective study. Front Pharmacol 2017; 8: 413.
42. Leonard JP, Jung SH, Johnson J et al. Randomized Trial of Lenalidomide Alone Versus Lenalidomide Plus Rituximab in Patients With Recurrent Follicular Lymphoma: CALGB 50401 (Alliance). J Clin Oncol 2015; 33 (31): 3635–40.
43. Zucca E, Vanazzi A, Ostenstad B et al. Independent review of CT responses in the trial SAKK 35/10 comparing rituximab with or without lenalidomide in untreated FL patients in need of therapy. Hematol Oncol 2015; 33 (S1): 105–6.
44. Marcus RE, Davies AJ, Ando K et al. Obinutuzumab-based induction and maintenance prolongs progression-free survival (PFS) in patients with previously untreated follicular lymphoma: primary results of the randomised Phase III GALLIUM study. Abstract 6. 58th Annual American Society of Hematology Meeting, 3–6 December, 2016.
45. Vidal L, Gafter-Gvili A, Leibovici L et al. Rituximab maintenance for the treatment of patients with follicular lymphoma: systematic review and meta-analysis of randomized trials. J Natl Cancer Inst 2009; 101 (4): 248–55.
46. Berinstein NL, Grillo-Lopez AJ, White CA et al. Association of serum Rituximab (IDEC-C2B8) concentration and anti-tumor response in the treatment of recurrent low-grade or follicular non-Hodgkin's lymphoma. Ann Oncol 1998; 9 (9): 995–1001.
47. Hochster H, Weller E, Gascoyne RD et al. Maintenance rituximab after cyclophosphamide, vincristine, and prednisone prolongs progression-free survival in advanced indolent lymphoma: results of the randomized phase III ECOG1496 Study. J Clin Oncol 2009; 27 (10): 1607–14.
48. Schaaf M, Reiser M, Borchmann P et al. High-dose therapy with autologous stem cell transplantation versus chemotherapy or immuno-chemotherapy for follicular lymphoma in adults. Cochrane Database Syst Rev 2012; 1.
49. http://med4share.ru/media/files/events/2015/conf_ 20151022/pres/ Trneny.pdf
50. Casulo C, Byrtek M, Dawson K et al. Early Relapse of Follicular Lymphoma After Rituximab Plus Cyclophosphamide, Doxorubicin, Vincristine, and Prednisone Defines Patients at High Risk for Death: An Analysis From the National LymphoCare Study. J Clin Oncol 2015; 33 (23): 2516–22.
51. Kahl BS, Bartlett NL, Leonard JP et al. Bendamustine is effective therapy in patients with rituximab-refractory, indolent B-cell non-Hodgkin lymphoma: results from a Multicenter Study. Cancer 2010; 116 (1): 106–14.
52. Sehn LH, Chua N, Mayer J et al. Obinutuzumab plus bendamustine versus bendamustine monotherapy in patients with rituximab-refractory indolent non-Hodgkin lymphoma (GADOLIN): a randomised, controlled, open-label, multicentre, phase 3 trial. Lancet Oncol 2016; 17 (8): 1081–93.
53. Tuscano JM, Dutia M, Chee K et al. Lenalidomide plus rituximab can produce durable clinical responses in patients with relapsed or refractory, indolent non-Hodgkin lymphoma. Br J Haematol 2014; 165 (3): 375–81.
54. Morschhauser FA, Salles G, Le Gouill S et al. A Phase Ib Study of Obinutuzumab Combined with Lenalidomide for Relapsed/Refractory Follicular B-Cell Lymphoma. Blood 2014; 124 (21): 4458.
55. Gopal AK, Kahl BS, de Vos S et al. PI3Kδ Inhibition by Idelalisib in Patients with Relapsed Indolent Lymphoma. N Engl J Med 2014; 370: 1008–18.
56. de Vos S, Wagner-Johnston ND, Coutre SE et al. Durable responses following treatment with the PI3K-delta inhibitor Idelalisib in combination with rituximab, bendamustine, or both, in recurrent indolent non-Hodgkin lymphoma: phase I/II results. Blood 2014; 124 (21): 3063.
57. Zinzani PL, Santoro A, Leppa S et al. Efficacy and safety of Copanlisib in Patients with Relapsed/Refractory Follicular Lymphoma: A Subset Analysis of the CHRONOS-1 Study. EHA Learning Center 2017 Jun 25; 182063 (Abstract release date: May 18, 2017) https://learningcenter. ehaweb.org/eha/2017/22nd/182063/pier.luigi.zinzani.efficacy.and.safety.of.copanlisib.in.patients.with.relapsed.html
58. Bartlett N, Costello BA, LaPlant BR et al. Single-Agent Ibrutinib in Relapsed or Refractory Follicular Lymphoma: A Phase 2 Consortium Trial. Blood 2017; blood-2017-09-804641.
59. Fowler N, Kahl BS, Lee P et al. Bortezomib, bendamustine, and rituximab in patients with relapsed or refractory follicular lymphoma: the phase II VERTICAL study. J Clin Oncol 2011; 29 (25): 3389–95.
60. Zinzani PL, Topp MS, Yuen S et al. Phase 2 Study of Venetoclax Plus Rituximab or Randomized Ven Plus Bendamustine+Rituximab (BR) Versus BR in Patients with Relapsed/Refractory Follicular Lymphoma: Interim Data. Blood 2016; 128 (22): 617.
61. Laport GG. Hematology. Am Soc Hematol Educ Program 2012; 2012: 417–25.
62. Poddubnaja I.V., Babicheva L.G. i dr. Rezul'taty prospektivnoj mnogocentrovoj nabljudatel'noj programmy BENEFIT «Ocenka rutinnogo primenenija kombinirovannoj terapii bendamustinom i rituksimabom s posledujushhej podderzhivajushhej terapiej rituksimabom u pacientov s recidivami ili refrakternymi indolentnymi B-kletochnymi nehodzhkinskimi limfomami (iNHL)». Prakticheskaja onkologija. 2017; 4 (18): 376–88. [in Russian]
2. Solal-Celigny P, Roy P, Colombat P et al. Follicular Lymphoma International Prognostic Index. Blood 2004; 104 (5): 1258–65.
3. Federico M, Bellei M, Marcheselli L et al. 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; 27 (27): 4555–62.
4. Pastore A, Jurinovic V, Kridel R et al. Integration of gene mutations in risk prognostication for patients receiving first-line immunochemotherapy for follicular lymphoma: a retrospective analysis of a prospective clinical trial and validation in a population-based registry. Lancet Oncol 2015; 16 (9): 1111–22.
5. Dave SS, Wright G, Tan B et al. Prediction of survival in follicular lymphoma based on molecular features of tumor-infiltrating immune cells. N Engl J Med 2004; 351 (21): 2159–69.
6. Wang W, Corrigan-Cummins M, Hudson J et al. MicroRNA profiling of follicular lymphoma identifies microRNAs related to cell proliferation and tumor response. Haematologica 2012; 97 (4): 586–94.
7. Scott DW, Gascoyne RD. The tumour microenvironment in B cell lymphomas. Nat Rev Cancer 2014; 14 (8): 517–34.
8. Sugimoto T, Watanabe T. Follicular lymphoma: the role of the tumor microenvironment in prognosis. J Clin Exp Hematop 2016; 56 (1): 1–19.
9. Canioni D, Salles G, Mounier N et al. High numbers of tumor-associated macrophages have an adverse prognostic value that can be circumvented by rituximab in patients with follicular lymphoma enrolled onto the GELA-GOELAMS FL-2000 trial. J Clin Oncol 2008; 26 (3): 440–6.
10. Kridel R, Xerri L, Gelas-Dore B et al. The prognostic impact of CD163-positive macrophages in follicular lymphoma: a study from the BC Cancer Agency and the Lymphoma Study Association. Clin Cancer Res 2015; 21 (15): 3428–35.
11. Smeltzer JP, Jones JM, Ziesmer SC et al. Pattern of CD14+ follicular dendritic cells and PD1+ T cells independently predicts time to transformation in follicular lymphoma. Clin Cancer Res 2014; 20 (11): 2862–72.
12. Sohani AR, Pitcher B, Chadburn A et al. Interfollicular CD10 expression and follicular PD1 tumor-infiltrating lymphocytes as biologic risk factors in patients with previously untreated follicular lymphoma receiving rituximab-based biologic therapy: an Alliance Correlative Science Study (CALGB 50901, 50402, 50701, 50803, 50401). Blood 2015; 126 (23): 334.
13. Cheson BD, Fisher RI, Barrington SF et al. Recommendations for initial evaluation, staging, and response assessment of Hodgkin and non-Hodgkin lymphoma: the Lugano classification. J Clin Oncol 2014; 32 (27): 3059–68.
14. Ansell SM, Armitage JO. Positron emission tomographic scans in lymphoma: convention and controversy. Mayo Clin Proc 2012; 87 (6): 571–80.
15. Meignan M, Cottereau AS, Versari A et al. Baseline metabolic tumor volume predicts outcome in high-tumor-burden follicular lymphoma: a pooled analysis of three multicenter studies. J Clin Oncol 2016; 34 (30): 3618–26.
16. Adams HJ, Kwee TC. Overestimated value of baseline total metabolic tumor volume at 18F-labeled fluorodeoxyglucose positron emission tomography in follicular lymphoma. J Clin Oncol 2017; 35 (8): 918–9.
17. Schöder H, Moskowitz C. Metabolic tumor volume in lymphoma: hype or hope? J Clin Oncol 2016; 34 (30): 3591–4.
18. Parraga I, Gimeno E, Pallerols FG et al. PET-CT and Bone Marrow Biopsy in staging Follicular Lymphoma in a single institution. Abstract PB1874; EHA Learning Center 2017 May 18,182588. https://learningcenter.ehaweb.org/eha/2017/ 22nd/182588/ivonne.parraga. pet-ct.and.bone.marrow.biopsy.in. staging.folicular.lymphoma.in.html Assessed 4.12.2017.
19. López-Guillermo A, Cabanillas F, McLaughlin P et al. Molecular response assessed by PCR is the most important factor predicting failure-free survival in indolent follicular lymphoma: update of the MDACC series. Ann Oncol 2000; 11 (Suppl. 1): S137–S140.
20. Zohren F, Bruns I, Pechtel S et al. Prognostic value of circulating Bcl-2/IgH levels in patients with follicular lymphoma receiving first-line immunochemotherapy. Blood 2015; 126 (12): 1407–14.
21. Pott C, Hoster E, Kehden B et al. Minimal residual disease in patients with follicular lymphoma treated with obinutuzumab or rituximab as first-line induction Immunochemotherapy and maintenance in the phase 3 GALLIUM study. Blood 2016; 128 (22): 613.
22. Luminari S, Galimberti S, Versari A et al. Positron emission tomography response and minimal residual disease impact on progression-free survival in patients with follicular lymphoma. A subset analysis from the FOLL05 trial of the Fondazione Italiana Linfomi. Haematologica 2016; 101 (2): e66–8.
23. Conconi A, Ponzio C, Lobetti-Bodoni C et al. Incidence, risk factors and outcome of histological transformation in follicular lymphoma. Br J Haematol 2012; 157 (2): 188–96.
24. Link BK, Maurer MJ, Nowakowski GS et al. Rates and outcomes of follicular lymphoma transformation in the immunochemotherapy era: a report from the University of Iowa/MayoClinic Specialized Program of Research Excellence Molecular Epidemiology Resource. J Clin Oncol 2013; 31 (26): 3272–8.
25. Brice P, Bastion Y, Lepage E et al. 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 (3): 1110–7.
26. Young RC, Longo DL, Glatstein E et al. The treatment of indolent lymphomas: watchful waiting v aggressive combined modality treatment. Semin Hematol 1988; 25 (2 Suppl. 2): 11–6.
27. Al-Tourah AJ, Gill KK, Hoskins PJ et al. The impact of initial treatment of advanced stage indolent lymphoma on the risk of transformation. J Clin Oncol 2006; 24 (18): 7510.
28. Gine E, Montoto S, Bosch F et al. The Follicular Lymphoma International Prognostic Index (FLIPI) and the histological subtype are the most important factors to predict histological transformation in follicular lymphoma. Ann Oncol 2006; 17 (10): 1539–45.
29. Cheson BD, Horning SJ, Coiffier B et al. Report of an International workshop to standardize response criteria for non-Hodgkin’s lymphomas. NCI Sponsored International Working Group. J Clin Oncol 1999; 17 (4): 1244.
30. Advani R, Rosenberg SA, Horning SJ. Stage I and II follicular non-Hodgkin's lymphoma: long-term follow-up of no initial therapy. J Clin Oncol 2004; 22 (8): 1454–9.
31. Guadagnolo BA, Li S, Neuberg D et al. Long-term outcome and mortality trends in early-stage, Grade 1–2 follicular lymphoma treated with radiation therapy. Int J Radiat Oncol Biol Phys 2006; 64 (3): 928–34.
32. Skvortsova I, Popper BA, Skvortsov S et al. Pretreatment with rituximab enhances radiosensitivity of non-Hodgkin's lymphoma cells. J Radiat Res 2005; 46 (2): 241–8.
33. Ardeshna KM, Qian W, Smith P et al. Rituximab versus a watch-and-wait approach in patients with advanced-stage, asymptomatic, non-bulky follicular lymphoma: an open-label randomised phase 3 trial. Lancet Oncol 2014; 15 (4): 424–35.
34. Witzig TE, Vukov AM, Habermann TM et al. Rituximab therapy for patients with newly diagnosed, advanced-stage, follicular grade I non-Hodgkin's lymphoma: a phase II trial in the North Central Cancer Treatment Group. J Clin Oncol 2005; 23 (6): 1103–8.
35. Colombat P, Salles G, Brousse N et al. 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 2001; 97 (1): 101–6.
36. Martinelli G, Schmitz SF, Utiger U et al. Long-term follow-up of patients with follicular lymphoma receiving single-agent rituximab at two different schedules in trial SAKK 35/98. J Clin Oncol 2010; 28 (29): 4480–4.
37. Taverna C, Martinelli G, Hitz F et al. Rituximab Maintenance for a Maximum of 5 Years After Single-Agent Rituximab Induction in Follicular Lymphoma: Results of the Randomized Controlled Phase III Trial SAKK 35/03. J Clin Oncol 2016; 34 (5): 495–500.
38. Federico M, Luminari S, Dondi A et al. R-CVP versus R-CHOP versus R-FM for the initial treatment of patients with advanced-stage follicular lymphoma: results of the FOLL05 trial conducted by the Fondazione Italiana Linfomi. J Clin Oncol 2013; 31 (12): 1506–13.
39. Rummel MJ, Niederle N, Maschmeyer G et al. 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; 381 (9873): 1203–10.
40. Mondello P, Steiner N, Willenbacher W et al. Bendamustine plus rituximab versus R-CHOP as first-line treatment for patients with indolent non-Hodgkin’s lymphoma: evidence from a multicenter, retrospective study. Ann Hematol 2016; 95 (7): 1107–14.
41. Galimberti G, Ciabatti E, Ercolano G at al. The combination of rituximab and bendamustine as first-line treatment is highly effective in the eradicating minimal residual disease in follicular lymphoma: an Italian retrospective study. Front Pharmacol 2017; 8: 413.
42. Leonard JP, Jung SH, Johnson J et al. Randomized Trial of Lenalidomide Alone Versus Lenalidomide Plus Rituximab in Patients With Recurrent Follicular Lymphoma: CALGB 50401 (Alliance). J Clin Oncol 2015; 33 (31): 3635–40.
43. Zucca E, Vanazzi A, Ostenstad B et al. Independent review of CT responses in the trial SAKK 35/10 comparing rituximab with or without lenalidomide in untreated FL patients in need of therapy. Hematol Oncol 2015; 33 (S1): 105–6.
44. Marcus RE, Davies AJ, Ando K et al. Obinutuzumab-based induction and maintenance prolongs progression-free survival (PFS) in patients with previously untreated follicular lymphoma: primary results of the randomised Phase III GALLIUM study. Abstract 6. 58th Annual American Society of Hematology Meeting, 3–6 December, 2016.
45. Vidal L, Gafter-Gvili A, Leibovici L et al. Rituximab maintenance for the treatment of patients with follicular lymphoma: systematic review and meta-analysis of randomized trials. J Natl Cancer Inst 2009; 101 (4): 248–55.
46. Berinstein NL, Grillo-Lopez AJ, White CA et al. Association of serum Rituximab (IDEC-C2B8) concentration and anti-tumor response in the treatment of recurrent low-grade or follicular non-Hodgkin's lymphoma. Ann Oncol 1998; 9 (9): 995–1001.
47. Hochster H, Weller E, Gascoyne RD et al. Maintenance rituximab after cyclophosphamide, vincristine, and prednisone prolongs progression-free survival in advanced indolent lymphoma: results of the randomized phase III ECOG1496 Study. J Clin Oncol 2009; 27 (10): 1607–14.
48. Schaaf M, Reiser M, Borchmann P et al. High-dose therapy with autologous stem cell transplantation versus chemotherapy or immuno-chemotherapy for follicular lymphoma in adults. Cochrane Database Syst Rev 2012; 1.
49. http://med4share.ru/media/files/events/2015/conf_ 20151022/pres/ Trneny.pdf
50. Casulo C, Byrtek M, Dawson K et al. Early Relapse of Follicular Lymphoma After Rituximab Plus Cyclophosphamide, Doxorubicin, Vincristine, and Prednisone Defines Patients at High Risk for Death: An Analysis From the National LymphoCare Study. J Clin Oncol 2015; 33 (23): 2516–22.
51. Kahl BS, Bartlett NL, Leonard JP et al. Bendamustine is effective therapy in patients with rituximab-refractory, indolent B-cell non-Hodgkin lymphoma: results from a Multicenter Study. Cancer 2010; 116 (1): 106–14.
52. Sehn LH, Chua N, Mayer J et al. Obinutuzumab plus bendamustine versus bendamustine monotherapy in patients with rituximab-refractory indolent non-Hodgkin lymphoma (GADOLIN): a randomised, controlled, open-label, multicentre, phase 3 trial. Lancet Oncol 2016; 17 (8): 1081–93.
53. Tuscano JM, Dutia M, Chee K et al. Lenalidomide plus rituximab can produce durable clinical responses in patients with relapsed or refractory, indolent non-Hodgkin lymphoma. Br J Haematol 2014; 165 (3): 375–81.
54. Morschhauser FA, Salles G, Le Gouill S et al. A Phase Ib Study of Obinutuzumab Combined with Lenalidomide for Relapsed/Refractory Follicular B-Cell Lymphoma. Blood 2014; 124 (21): 4458.
55. Gopal AK, Kahl BS, de Vos S et al. PI3Kδ Inhibition by Idelalisib in Patients with Relapsed Indolent Lymphoma. N Engl J Med 2014; 370: 1008–18.
56. de Vos S, Wagner-Johnston ND, Coutre SE et al. Durable responses following treatment with the PI3K-delta inhibitor Idelalisib in combination with rituximab, bendamustine, or both, in recurrent indolent non-Hodgkin lymphoma: phase I/II results. Blood 2014; 124 (21): 3063.
57. Zinzani PL, Santoro A, Leppa S et al. Efficacy and safety of Copanlisib in Patients with Relapsed/Refractory Follicular Lymphoma: A Subset Analysis of the CHRONOS-1 Study. EHA Learning Center 2017 Jun 25; 182063 (Abstract release date: May 18, 2017) https://learningcenter. ehaweb.org/eha/2017/22nd/182063/pier.luigi.zinzani.efficacy.and.safety.of.copanlisib.in.patients.with.relapsed.html
58. Bartlett N, Costello BA, LaPlant BR et al. Single-Agent Ibrutinib in Relapsed or Refractory Follicular Lymphoma: A Phase 2 Consortium Trial. Blood 2017; blood-2017-09-804641.
59. Fowler N, Kahl BS, Lee P et al. Bortezomib, bendamustine, and rituximab in patients with relapsed or refractory follicular lymphoma: the phase II VERTICAL study. J Clin Oncol 2011; 29 (25): 3389–95.
60. Zinzani PL, Topp MS, Yuen S et al. Phase 2 Study of Venetoclax Plus Rituximab or Randomized Ven Plus Bendamustine+Rituximab (BR) Versus BR in Patients with Relapsed/Refractory Follicular Lymphoma: Interim Data. Blood 2016; 128 (22): 617.
61. Laport GG. Hematology. Am Soc Hematol Educ Program 2012; 2012: 417–25.
62. Поддубная И.В., Бабичева Л.Г. и др. Результаты проспективной многоцентровой наблюдательной программы BENEFIT «Оценка рутинного применения комбинированной терапии бендамустином и ритуксимабом с последующей поддерживающей терапией ритуксимабом у пациентов с рецидивами или рефрактерными индолентными В-клеточными неходжкинскими лимфомами (иНХЛ)». Практическая онкология. 2017; 4 (18): 376–88. / Poddubnaja I.V., Babicheva L.G. i dr. Rezul'taty prospektivnoj mnogocentrovoj nabljudatel'noj programmy BENEFIT «Ocenka rutinnogo primenenija kombinirovannoj terapii bendamustinom i rituksimabom s posledujushhej podderzhivajushhej terapiej rituksimabom u pacientov s recidivami ili refrakternymi indolentnymi B-kletochnymi nehodzhkinskimi limfomami (iNHL)». Prakticheskaja onkologija. 2017; 4 (18): 376–88. [in Russian]
________________________________________________
2. Solal-Celigny P, Roy P, Colombat P et al. Follicular Lymphoma International Prognostic Index. Blood 2004; 104 (5): 1258–65.
3. Federico M, Bellei M, Marcheselli L et al. 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; 27 (27): 4555–62.
4. Pastore A, Jurinovic V, Kridel R et al. Integration of gene mutations in risk prognostication for patients receiving first-line immunochemotherapy for follicular lymphoma: a retrospective analysis of a prospective clinical trial and validation in a population-based registry. Lancet Oncol 2015; 16 (9): 1111–22.
5. Dave SS, Wright G, Tan B et al. Prediction of survival in follicular lymphoma based on molecular features of tumor-infiltrating immune cells. N Engl J Med 2004; 351 (21): 2159–69.
6. Wang W, Corrigan-Cummins M, Hudson J et al. MicroRNA profiling of follicular lymphoma identifies microRNAs related to cell proliferation and tumor response. Haematologica 2012; 97 (4): 586–94.
7. Scott DW, Gascoyne RD. The tumour microenvironment in B cell lymphomas. Nat Rev Cancer 2014; 14 (8): 517–34.
8. Sugimoto T, Watanabe T. Follicular lymphoma: the role of the tumor microenvironment in prognosis. J Clin Exp Hematop 2016; 56 (1): 1–19.
9. Canioni D, Salles G, Mounier N et al. High numbers of tumor-associated macrophages have an adverse prognostic value that can be circumvented by rituximab in patients with follicular lymphoma enrolled onto the GELA-GOELAMS FL-2000 trial. J Clin Oncol 2008; 26 (3): 440–6.
10. Kridel R, Xerri L, Gelas-Dore B et al. The prognostic impact of CD163-positive macrophages in follicular lymphoma: a study from the BC Cancer Agency and the Lymphoma Study Association. Clin Cancer Res 2015; 21 (15): 3428–35.
11. Smeltzer JP, Jones JM, Ziesmer SC et al. Pattern of CD14+ follicular dendritic cells and PD1+ T cells independently predicts time to transformation in follicular lymphoma. Clin Cancer Res 2014; 20 (11): 2862–72.
12. Sohani AR, Pitcher B, Chadburn A et al. Interfollicular CD10 expression and follicular PD1 tumor-infiltrating lymphocytes as biologic risk factors in patients with previously untreated follicular lymphoma receiving rituximab-based biologic therapy: an Alliance Correlative Science Study (CALGB 50901, 50402, 50701, 50803, 50401). Blood 2015; 126 (23): 334.
13. Cheson BD, Fisher RI, Barrington SF et al. Recommendations for initial evaluation, staging, and response assessment of Hodgkin and non-Hodgkin lymphoma: the Lugano classification. J Clin Oncol 2014; 32 (27): 3059–68.
14. Ansell SM, Armitage JO. Positron emission tomographic scans in lymphoma: convention and controversy. Mayo Clin Proc 2012; 87 (6): 571–80.
15. Meignan M, Cottereau AS, Versari A et al. Baseline metabolic tumor volume predicts outcome in high-tumor-burden follicular lymphoma: a pooled analysis of three multicenter studies. J Clin Oncol 2016; 34 (30): 3618–26.
16. Adams HJ, Kwee TC. Overestimated value of baseline total metabolic tumor volume at 18F-labeled fluorodeoxyglucose positron emission tomography in follicular lymphoma. J Clin Oncol 2017; 35 (8): 918–9.
17. Schöder H, Moskowitz C. Metabolic tumor volume in lymphoma: hype or hope? J Clin Oncol 2016; 34 (30): 3591–4.
18. Parraga I, Gimeno E, Pallerols FG et al. PET-CT and Bone Marrow Biopsy in staging Follicular Lymphoma in a single institution. Abstract PB1874; EHA Learning Center 2017 May18,182588. https://learningcenter.ehaweb.org/eha/2017/ 22nd/182588/ivonne.parraga. pet-ct.and.bone.marrow.biopsy.in. staging.folicular.lymphoma.in.html Assessed 4.12.2017.
19. López-Guillermo A, Cabanillas F, McLaughlin P et al. Molecular response assessed by PCR is the most important factor predicting failure-free survival in indolent follicular lymphoma: update of the MDACC series. Ann Oncol 2000; 11 (Suppl. 1): S137–S140.
20. Zohren F, Bruns I, Pechtel S et al. Prognostic value of circulating Bcl-2/IgH levels in patients with follicular lymphoma receiving first-line immunochemotherapy. Blood 2015; 126 (12): 1407–14.
21. Pott C, Hoster E, Kehden B et al. Minimal residual disease in patients with follicular lymphoma treated with obinutuzumab or rituximab as first-line induction Immunochemotherapy and maintenance in the phase 3 GALLIUM study. Blood 2016; 128 (22): 613.
22. Luminari S, Galimberti S, Versari A et al. Positron emission tomography response and minimal residual disease impact on progression-free survival in patients with follicular lymphoma. A subset analysis from the FOLL05 trial of the Fondazione Italiana Linfomi. Haematologica 2016; 101 (2): e66–8.
23. Conconi A, Ponzio C, Lobetti-Bodoni C et al. Incidence, risk factors and outcome of histological transformation in follicular lymphoma. Br J Haematol 2012; 157 (2): 188–96.
24. Link BK, Maurer MJ, Nowakowski GS et al. Rates and outcomes of follicular lymphoma transformation in the immunochemotherapy era: a report from the University of Iowa/MayoClinic Specialized Program of Research Excellence Molecular Epidemiology Resource. J Clin Oncol 2013; 31 (26): 3272–8.
25. Brice P, Bastion Y, Lepage E et al. 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 (3): 1110–7.
26. Young RC, Longo DL, Glatstein E et al. The treatment of indolent lymphomas: watchful waiting v aggressive combined modality treatment. Semin Hematol 1988; 25 (2 Suppl. 2): 11–6.
27. Al-Tourah AJ, Gill KK, Hoskins PJ et al. The impact of initial treatment of advanced stage indolent lymphoma on the risk of transformation. J Clin Oncol 2006; 24 (18): 7510.
28. Gine E, Montoto S, Bosch F et al. The Follicular Lymphoma International Prognostic Index (FLIPI) and the histological subtype are the most important factors to predict histological transformation in follicular lymphoma. Ann Oncol 2006; 17 (10): 1539–45.
29. Cheson BD, Horning SJ, Coiffier B et al. Report of an International workshop to standardize response criteria for non-Hodgkin’s lymphomas. NCI Sponsored International Working Group. J Clin Oncol 1999; 17 (4): 1244.
30. Advani R, Rosenberg SA, Horning SJ. Stage I and II follicular non-Hodgkin's lymphoma: long-term follow-up of no initial therapy. J Clin Oncol 2004; 22 (8): 1454–9.
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Авторы
Л.Г.Бабичева*, И.В.Поддубная
ФГБОУ ДПО «Российская медицинская академия непрерывного профессионального образования» Минздрава России. 125993, Россия, Москва, ул. Баррикадная, д. 2/1
*lalibabicheva@mail.ru
Russian Medical Academy of Continuous Professional Education of the Ministry of Health of the Russian Federation. 125993, Russian Federation, Moscow, ul. Barrikadnaia, d. 2/1
*lalibabicheva@mail.ru
ФГБОУ ДПО «Российская медицинская академия непрерывного профессионального образования» Минздрава России. 125993, Россия, Москва, ул. Баррикадная, д. 2/1
*lalibabicheva@mail.ru
________________________________________________
Russian Medical Academy of Continuous Professional Education of the Ministry of Health of the Russian Federation. 125993, Russian Federation, Moscow, ul. Barrikadnaia, d. 2/1
*lalibabicheva@mail.ru
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