Vol 11, No 4 (2020)
Guidelines / Expert consensus
Published online: 2021-03-12
Consensus of the Polish Lymphoma Research Group experts on the management of relapsed or refractory classical Hodgkin lymphoma in 2020
1
, 2, 2, 3, 3, 4, 5, 6, 7, 8, 9
, 2, 2, 3, 3, 4, 5, 6, 7, 8, 9
Hematologia 2020;11(4):193-211.
Abstract
In Poland, 800–900 new cases of classical Hodgkin’s lymphoma (cHL) are diagnosed annually. Despite relatively good results of first-line treatment, 20–25% of patients relapse and the chances of their cure become much smaller. The paper presents the consensus of the Polish experts on the management of patients with relapsed and refractory cHL in 2020, taking into account generally accepted international recommendations, approved indications and the Polish reimbursement conditions. The proposed recommendations were voted by all authors. The recommendations that were agreed by the majority are presented in the paper. For each recommendation, the most important information supporting its legitimacy and information justifying the dissenting opinions of the authors of the consensus were quoted.
Keywords: treatment of relapsed/refractory Hodgkin lymphomaconsensusPolish Lymphoma Research Group
References
- https://seer cancer gov/statfacts/html/hodg html dostęp. SEER, National Cancer Institute Surveillance, Epidemiology, and End Results Program. Cancer stat facts: Hodgkin lymphoma (March 5, 2020).
- Subbotin AS, Dolgushin MB, Afanasjeva NG, et al. [18F-FDG-PET/CT imaging of different hystological subtypes of Hodgkin lymphoma] [In Russian]. Journal of Oncology: Diagnostic Radiology and Radiotherapy. 2019; 2(3): 58–62.
- Weiler-Sagie M, Bushelev O, Epelbaum R, et al. (18)F-FDG avidity in lymphoma readdressed: a study of 766 patients. J Nucl Med. 2010; 51(1): 25–30.
- Ramos CA, Torrano V, Bilgi M, et al. CD30-chimeric antigen receptor (CAR) T cells for therapy of hodgkin lymphoma (HL). Abstract #79. Hematology Oncology. 2019; 37(S2): 168.
- Engert A, Aleman BMP, André M, et al. Hodgkin's lymphoma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2018; 29(Suppl 4): iv19–iv29.
- Dykewicz CA. Centers for Disease Control and Prevention (U.S.), Infectious Diseases Society of America, American Society of Blood and Marrow Transplantation. Summary of the guidelines for preventing opportunistic infections among hematopoietic stem cell transplant recipients. Clin Infect Dis. 2001; 33(2): 139–144.
- Armitage JO. Early-stage Hodgkin's lymphoma. N Engl J Med. 2010; 363(7): 653–662.
- Kuruvilla J. Standard therapy of advanced Hodgkin lymphoma. Hematology Am Soc Hematol Educ Program. 2009: 497–506.
- Van Den Neste E, Casasnovas O, André M, et al. Classical Hodgkin's lymphoma: the Lymphoma Study Association guidelines for relapsed and refractory adult patients eligible for transplant. Haematologica. 2013; 98(8): 1185–1195.
- Zaucha JM, Chauvie S, Zaucha R, et al. The role of PET/CT in the modern treatment of Hodgkin lymphoma. Cancer Treat Rev. 2019; 77: 44–56.
- Cheson BD, Fisher RI, Barrington SF, et al. Alliance, Australasian Leukaemia and Lymphoma Group, Eastern Cooperative Oncology Group, European Mantle Cell Lymphoma Consortium, Italian Lymphoma Foundation, European Organisation for Research, Treatment of Cancer/Dutch Hemato-Oncology Group, Grupo Español de Médula Ósea, German High-Grade Lymphoma Study Group, German Hodgkin's Study Group, Japanese Lymphorra Study Group, Lymphoma Study Association, NCIC Clinical Trials Group, Nordic Lymphoma Study Group, Southwest Oncology Group, United Kingdom National Cancer Research Institute. Recommendations for initial evaluation, staging, and response assessment of Hodgkin and non-Hodgkin lymphoma: the Lugano classification. J Clin Oncol. 2014; 32(27): 3059–3068.
- Zaucha JM, Deptała A, Zaucha R. Wczesna diagnostyka i leczenie postaci opornych i nawrotowych klasycznego chłoniaka Hodgkina. Acta Haematol Pol. 2016; 47(1): 1–9.
- Josting A, Nogová L, Franklin J, et al. Salvage radiotherapy in patients with relapsed and refractory Hodgkin’s lymphoma: A Retrospective Analysis From the German Hodgkin Lymphoma Study Group. J Clin Oncol. 2005; 23(7): 1522–1529.
- NCCN Clinical Practice Guidelines in Oncology — Hodgkin lymphoma v. www.nccn.org (April 15, 2020).
- Wróbel T. Chłoniak Hodgkina. Onkol Klin Prakt. 2020; 6(Suppl A): 505–523.
- Linch DC, Goldstone AH, McMillan A, et al. Dose intensification with autologous bone-marrow transplantation in relapsed and resistant Hodgkin's disease: results of a BNLI randomised trial. The Lancet. 1993; 341(8852): 1051–1054.
- Schmitz N, Pfistner B, Sextro M, et al. Aggressive conventional chemotherapy compared with high-dose chemotherapy with autologous haemopoietic stem-cell transplantation for relapsed chemosensitive Hodgkin's disease: a randomised trial. The Lancet. 2002; 359(9323): 2065–2071.
- Morschhauser F, Brice P, Fermé C, et al. GELA/SFGM Study Group. Risk-adapted salvage treatment with single or tandem autologous stem-cell transplantation for first relapse/refractory Hodgkin's lymphoma: results of the prospective multicenter H96 trial by the GELA/SFGM study group. J Clin Oncol. 2008; 26(36): 5980–5987.
- Vassilakopoulos TP, Asimakopoulos JV, Konstantopoulos K, et al. Optimizing outcomes in relapsed/refractory Hodgkin lymphoma: a review of current and forthcoming therapeutic strategies. Ther Adv Hematol. 2020; 11: 2040620720902911.
- Paszkiewicz-Kozik E, Walewski J. Hodgkin lymphoma — closer to failure-free treatment. Oncol Clin Pract. 2015; 11: 199–210.
- Moskowitz AJ, Herrera AF, Beaven AW. Relapsed and refractory classical Hodgkin Lymphoma: keeping pace with novel agents and new options for salvage therapy. Am Soc Clin Oncol Educ Book. 2019; 39: 477–486.
- Santoro A, Mazza R, Pulsoni A, et al. Bendamustine in combination with gemcitabine and vinorelbine is an effective regimen as induction chemotherapy before autologous stem-cell transplantation for relapsed or refractory Hodgkin lymphoma: final results of a multicenter phase II study. J Clin Oncol. 2016; 34(27): 3293–3299.
- Knopińska-Posłuszny W, Kulikowski W, Paszkiewicz-Kozik E, et al. Zastosowanie bendamustyny z gemcytabiną i deksametazonem w leczeniu pierwotnie opornej i nawrotowej postaci chłoniaka Hodgkina – wieloośrodkowe badanie obserwacyjne Polskiej Grupy Badawczej Chłoniaków (PLRG). Acta Haemat Pol. 2015; 46(Suppl): 58–59.
- PLRG, Polska Grupa Badawcza Chłoniaków, badanie PLRG-R26. http://www.plrg.pl/images/stories/file/badania_plrg/PLRG-R26.pdf (August 5, 2020).
- Sasse S, Rothe A, Goergen H, et al. Brentuximab vedotin (SGN-35) in patients with transplant-naive relapsed/refractory Hodgkin lymphoma. Leuk Lymphoma. 2013; 54(10): 2144–2148.
- Walewski J, Hellmann A, Siritanaratkul N, et al. Prospective study of brentuximab vedotin in relapsed/refractory Hodgkin lymphoma patients who are not suitable for stem cell transplant or multi-agent chemotherapy. Br J Haematol. 2018; 183(3): 400–410.
- Bröckelmann PJ, Zagadailov EA, Corman SL, et al. Brentuximab vedotin in patients with relapsed or refractory Hodgkin lymphoma who are Ineligible for autologous stem cell transplant: A Germany and United Kingdom retrospective study. Eur J Haematol. 2017; 99(6): 553–558.
- Forero-Torres A, Fanale M, Advani R, et al. Brentuximab vedotin in transplant-naive patients with relapsed or refractory hodgkin lymphoma: analysis of two phase I studies. Oncologist. 2012; 17(8): 1073–1080.
- Viviani S, Guidetti A, Dalto S, et al. Brentuximab vedotin (BV) an effective treatment for transplant ineligible patients with relapsed/refractory (R/R) Hodgkin lymphoma (HL). https://library.ehaweb.org/eha/2015/20th/100326/simonetta.viviani.brentuximab.vedotin.%28bv%29.an.effective.treatment.for.html (December 10, 2020).
- Zinzani PL, Sasse S, Radford J, et al. Brentuximab vedotin in relapsed/refractory Hodgkin lymphoma: An updated review of published data from the named patient program. Crit Rev Oncol Hematol. 2016; 104: 65–70.
- EPAR, European Public Assessment Report, CHMP. https://www.ema.europa.eu/en/documents/assessment-report/adcetris-epar-public-assessment-report_en.pdf (August 5, 2020).
- Moskowitz CH, Matasar MJ, Zelenetz AD, et al. Normalization of pre-ASCT, FDG-PET imaging with second-line, non-cross-resistant, chemotherapy programs improves event-free survival in patients with Hodgkin lymphoma. Blood. 2012; 119(7): 1665–1670.
- Kuruvilla J, Ramchandren R, Santoro A, et al. KEYNOTE-204: randomized, open-label, phase III study of pembrolizumab (pembro) versus brentuximab vedotin (BV) in relapsed or refractory classic Hodgkin lymphoma (R/R cHL). J Clin Oncol. 2020; 38(15_Suppl): 8005–8005.
- Salas C, Niembro A, Lozano V, et al. Persistent genomic instability in peripheral blood lymphocytes from Hodgkin lymphoma survivors. Environ Mol Mutagen. 2012; 53(4): 271–280.
- Herrera AF, Palmer J, Martin P, et al. Results of a multicenter phase II trial of brentuximab vedotin as second-line therapy before autologous transplantation in relapsed/refractory Hodgkin lymphoma. Biol Blood Marrow Transplant. 2015; 21(12): 2136–2140.
- Moskowitz AJ, Schöder H, Yahalom J, et al. PET-adapted sequential salvage therapy with brentuximab vedotin followed by augmented ifosamide, carboplatin, and etoposide for patients with relapsed and refractory Hodgkin's lymphoma: a non-randomised, open-label, single-centre, phase 2 study. Lancet Oncol. 2015; 16(3): 284–292.
- Moskowitz AJ, Schöder H, Yahalom J, et al. PET-adapted therapy with brentuximab vedotin and augmented ICE for relapsed/refractory Hodgkin lymphoma — lack of improvement with 3 versus 2 cycles of weekly brentuximab vedotin. Haematologica. 2016; 101(Suppl 5): abstract P088.
- Herrera A, et al. Posttransplant outcomes in a multicenter phase II study of brentuximab vedotin as first line salvage therapy in relapsed or refractory Hodgkin lymphoma prior to autologous stem-cell transplantation. Haematologica. 2016; 101(Suppl 5): abstract P086.
- Cassaday RD, Fromm J, Cowan AJ, et al. Safety and activity of brentuximab vedotin (BV) plus ifosfamide, carboplatin, and etoposide (ICE) for relapsed/refractory (rel/ref) classical Hodgkin lymphoma (cHL): initial results of a phase I/II trial. Blood. 2016; 128(22): 1834–1834.
- Herrera AF, Palmer J, Martin P, et al. Autologous stem-cell transplantation after second-line brentuximab vedotin in relapsed or refractory Hodgkin lymphoma. Ann Oncol. 2018; 29(3): 724–730.
- Herrera AF, Moskowitz AJ, Bartlett NL, et al. Interim results of brentuximab vedotin in combination with nivolumab in patients with relapsed or refractory Hodgkin lymphoma. Blood. 2018; 131(11): 1183–1194.
- Hagenbeek A, et al. Combining brentuximab vedotin with DHAP as salvage treatment in relapsed/refractory Hodgkin lymphoma: the phase II HOVON/LLPC transplant BRaVE study. Blood. 2018; 132(Suppl 1): 2923.
- Cole PD, McCarten KM, Pei Q, et al. Brentuximab vedotin with gemcitabine for paediatric and young adult patients with relapsed or refractory Hodgkin's lymphoma (AHOD1221): a Children's Oncology Group, multicentre single-arm, phase 1-2 trial. Lancet Oncol. 2018; 19(9): 1229–1238.
- Garcia-Sanz R, Sureda A, de la Cruz F, et al. Brentuximab vedotin and ESHAP is highly effective as second-line therapy for Hodgkin lymphoma patients (long-term results of a trial by the Spanish GELTAMO Group). Ann Oncol. 2019; 30(4): 612–620.
- Stamatoullas A, Ghesquieres H, filliatre LC, et al. Brentuximab vedotin in first refractory/relapsed classical Hodgkin lymphoma patients treated by chemotherapy (ICE) before autologous transplantation. Final analysis of phase II study. Blood. 2019; 134(Suppl_1): 132–132.
- Abuelgasim KA, Alzahrani M, Alsharhan Y, et al. Chemoimmunotherapy with brentuximab vedotin combined with ifosfamide, gemcitabine, and vinorelbine is highly active in relapsed or refractory classical Hodgkin lymphoma. Bone Marrow Transplant. 2019; 54(7): 1168–1172.
- Advani R, Moskowitz A, Bartlett N, et al. Phase 1/2 study of brentuximab vedotin in combination with nivolumab in patients with relapsed or refractory classic Hodgkin lymphoma: part 3 (concurrent dosing) results and updated progression-free survival results from parts 1 and 2 (staggered dosing). Blood. 2018; 132(Suppl 1): 1635–1635.
- LaCasce AS, Bociek RG, Sawas A, et al. Three-year outcomes with brentuximab vedotin plus bendamustine as first salvage therapy in relapsed or refractory Hodgkin lymphoma. Br J Haematol. 2020; 189(3): e86–e90.
- Czyz A, Lojko-Dankowska A, Joks M, et al. Brentuximab vedotin alone and in combination with bendamustine as salvage therapy for primary refractory or relapsed Hodgkin lymphoma: multicentre experience of the Polish Lymphoma Research Group (PLRG). Blood. 2018; 132(Suppl 1): 5375–5375.
- Summary of Product Characteristic Keytruda. https://www.ema.europa.eu/en/documents/product-information/keytruda-epar-product-information_en.pdf (August 5, 2020).
- Chen R, Zinzani P, Lee H, et al. Pembrolizumab in relapsed or refractory Hodgkin lymphoma: 2-year follow-up of KEYNOTE-087. Blood. 2019; 134(14): 1144–1153.
- Charakterystyka Produktu Leczniczego Opdivo. https://www.ema.europa.eu/en/documents/product-information/opdivo-epar-product-information_pl.pdf (August 5, 2020).
- Chen R, Gopal A, Smith S, et al. Five-year survival and durability results of brentuximab vedotin in patients with relapsed or refractory Hodgkin lymphoma. Blood. 2016; 128(12): 1562–1566.
- Gopal AK, Bartlett NL, Forero-Torres A, et al. Brentuximab vedotin in patients aged 60 years or older with relapsed or refractory CD30-positive lymphomas: a retrospective evaluation of safety and efficacy. Leuk Lymphoma. 2014; 55(10): 2328–2334.
- Constine LS, Yahalom J, Ng AK, et al. The role of radiation therapy in patients with relapsed or refractory hodgkin lymphoma: guidelines from the International Lymphoma Radiation Oncology Group. Int J Radiation Oncol Biol Phys. 2018; 100(5): 1100–1118.
- Specht L, Yahalom J, Illidge T, et al. Modern radiation therapy for hodgkin lymphoma: field and dose guidelines from the International Lymphoma Radiation Oncology Group (ILROG). Int J Radiat Oncol Biol Phys. 2014; 89(4): 854–862.
- Brada M, Eeles R, Ashley S, et al. Salvage radiotherapy in recurrent Hodgkin's disease. Ann Oncol. 1992; 3(2): 131–135.
- Uematsu M, Tarbell NJ, Silver B, et al. Wide-field radiation therapy with or without chemotherapy for patients with Hodgkin disease in relapse after initial combination chemotherapy. Cancer. 1993; 72(1): 207–212, doi: 10.1002/1097-0142(19930701)72:1<207::aid-cncr2820720137>3.0.co;2-a.
- Leigh BR, Fox KA, Mack CF, et al. Radiation therapy salvage of Hodgkin's disease following chemotherapy failure. Int J Radiat Oncol Biol Phys. 1993; 27(4): 855–862.
- Pezner RD, Lipsett JA, Vora N, et al. Radical radiotherapy as salvage treatment for relapse of Hodgkin's disease initially treated by chemotherapy alone: prognostic significance of the disease-free interval. Int J Radiat Oncol Biol Phys. 1994; 30(4): 965–970.
- MacMillan CH, Bessell EM. The effectiveness of radiotherapy for localized relapse in patients with Hodgkin's disease (IIB-IVB) who obtained a complete response with chemotherapy alone as initial treatment. Clin Oncol (R Coll Radiol). 1994; 6(3): 147–150.
- Wirth A, Corry J, Laidlaw C, et al. Salvage radiotherapy for Hodgkin's disease following chemotherapy failure. Int J Radiat Oncol Biol Phys. 1997; 39(3): 599–607.
- Smeltzer JP, Cashen AF, Zhang Q, et al. Prognostic significance of FDG-PET in relapsed or refractory classical Hodgkin lymphoma treated with standard salvage chemotherapy and autologous stem cell transplantation. Biol Blood Marrow Transplant. 2011; 17(11): 1646–1652.
- Gentzler RD, Evens AM, Rademaker AW, et al. F-18 FDG-PET predicts outcomes for patients receiving total lymphoid irradiation and autologous blood stem-cell transplantation for relapsed and refractory Hodgkin lymphoma. Br J Haematol. 2014; 165(6): 793–800.
- Adams HJA, Nievelstein RAJ, Kwee TC. Systematic review and meta-analysis on the prognostic value of complete remission status at FDG-PET in Hodgkin lymphoma after completion of first-line therapy. Ann Hematol. 2016; 95(1): 1–9.
- Kahraman D, Theurich S, Rothe A, et al. 18-Fluorodeoxyglucose positron emission tomography/computed tomography for assessment of response to brentuximab vedotin treatment in relapsed and refractory Hodgkin lymphoma. Leuk Lymphoma. 2014; 55(4): 811–816.
- Moskowitz CH, Nademanee A, Masszi T, et al. AETHERA Study Group. Brentuximab vedotin as consolidation therapy after autologous stem-cell transplantation in patients with Hodgkin's lymphoma at risk of relapse or progression (AETHERA): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet. 2015; 385(9980): 1853–1862.
- Taleb B A. Tumour flare reaction in cancer treatments: a comprehensive literature review. Anticancer Drugs. 2019; 30(9): 953–958.
- Wolchok JD, Hoos A, O'Day S, et al. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin Cancer Res. 2009; 15(23): 7412–7420.
- Cheson BD, Ansell S, Schwartz L, et al. Refinement of the Lugano classification lymphoma response criteria in the era of immunomodulatory therapy. Blood. 2016; 128(21): 2489–2496.
- Liu Y, Dong Y, Kong Li, et al. Abscopal effect of radiotherapy combined with immune checkpoint inhibitors. J Hematol Oncol. 2018; 11(1): 104.
- Bentolila G, Pavlovsky A, et al. Relapse or refractory Hodgkin lymphoma: determining risk of relapse or progression after autologous stem-cell transplantation. Leuk Lymphoma. Leuk Lymphoma. 2020; 61(7): 1548–1554.
- Bröckelmann PJ, Müller H, Casasnovas O, et al. Risk factors and a prognostic score for survival after autologous stem-cell transplantation for relapsed or refractory Hodgkin lymphoma. Ann Oncol. 2017; 28(6): 1352–1358.
- Moskowitz CH, Walewski J, Nademanee A, et al. Five-year PFS from the AETHERA trial of brentuximab vedotin for Hodgkin lymphoma at high risk of progression or relapse. Blood. 2018; 132(25): 2639–2642.
- Kanate AS, Kumar A, Dreger P, et al. Maintenance therapies for Hodgkin and non-Hodgkin lymphomas after autologous transplantation: a Consensus Project of ASBMT, CIBMTR, and the Lymphoma Working Party of EBMT. JAMA Oncol. 2019; 5(5): 715–722.
- Bonthapally V, Wu E, Macalalad A, et al. Brentuximab vedotin in relapsed/refractory Hodgkin lymphoma post-autologous transplant: meta-analysis versus historical data. Curr Med Res Opin. 2015; 31(5): 993–1001.
- Bonthapally V, Yang H, Ayyagari R, et al. Brentuximab vedotin compared with other therapies in relapsed/refractory Hodgkin lymphoma post autologous stem cell transplant: median overall survival meta-analysis. Curr Med Res Opin. 2015; 31(7): 1377–1389.
- Dada R, Zekri J, Al Saadi R. Brentuximab vedotin in pretreated Hodgkin lymphoma patients: a systematic review and meta-analysis. Expert Opin Biol Ther. 2016; 16(6): 739–745.
- Tsirigotis P, Vassilakopoulos T, Batsis I, et al. Positive impact of brentuximab vedotin on overall survival of patients with classical Hodgkin lymphoma who relapse or progress after autologous stem cell transplantation: A nationwide analysis. Hematol Oncol. 2018; 36(4): 645–650.
- Kaloyannidis P, Hertzberg M, Webb K, et al. Positive impact of brentuximab vedotin on overall survival of patients with classical Hodgkin lymphoma who relapse or progress after autologous stem cell transplantation: A nationwide analysis. Hematol Oncol. 2018; 36(4): 645–650.
- Czyz A, Lojko-Dankowska A, Giza A, et al. Improved treatment outcomes for patients with Hodgkin lymphoma relapsing after autologous hematopoietic stem cell transplantation in the brentuximab vedotin era — the Real-Life Report from the Polish Lymphoma Research Group. Blood. 2019; 134(Suppl_1): 5276.
- Sureda A, Robinson S, Canals C, et al. Reduced-intensity conditioning compared with conventional allogeneic stem-cell transplantation in relapsed or refractory Hodgkin's lymphoma: an analysis from the Lymphoma Working Party of the European Group for Blood and Marrow Transplantation. J Clin Oncol. 2008; 26(3): 455–462.
- Anderlini P, Saliba R, Acholonu S, et al. Reduced-intensity allogeneic stem cell transplantation in relapsed and refractory Hodgkin's disease: low transplant-related mortality and impact of intensity of conditioning regimen. Bone Marrow Transplant. 2005; 35(10): 943–951.
- Thomson KJ, Peggs KS, Smith P, et al. Superiority of reduced-intensity allogeneic transplantation over conventional treatment for relapse of Hodgkin's lymphoma following autologous stem cell transplantation. Bone Marrow Transplant. 2008; 41(9): 765–770.
- Carella AM, Cavaliere M, Lerma E, et al. Autografting followed by nonmyeloablative immunosuppressive chemotherapy and allogeneic peripheral-blood hematopoietic stem-cell transplantation as treatment of resistant Hodgkin's disease and non-Hodgkin's lymphoma. J Clin Oncol. 2000; 18(23): 3918–3924.
- Peggs KS, Sureda A, Qian W, et al. UK and Spanish Collaborative Groups. Reduced-intensity conditioning for allogeneic haematopoietic stem cell transplantation in relapsed and refractory Hodgkin lymphoma: impact of alemtuzumab and donor lymphocyte infusions on long-term outcomes. Br J Haematol. 2007; 139(1): 70–80.
- Sureda A. Classical Hodgkin’s lymphoma. Chapter 88. In: Carreras E. ed. The EBMT Handbook: hematopoietic stem cell transplantation and cellular therapies. 7th edition. Springer, Cham 2019.
- Moskowitz CH. Should all patients with HL who relapse after ASCT be considered for allogeneic SCT? A consult, yes; a transplant, not necessarily. Blood Adv. 2018; 2(7): 821–824.
- Peggs KS. Should all patients with Hodgkin lymphoma who relapse after autologous SCT be considered for allogeneic SCT? Blood Adv. 2018; 2(7): 817–820.
- Merryman RW, Castagna L, Corradini P, et al. Safety and efficacy of allogeneic hematopoietic stem cell transplant after programmed cell ceath 1 (PD-1) / programmed cell death ligand 1 (PD-L1) blockade for classical Hodgkin lymphoma: analysis of a large international cohort. Blood. 2019; 134(Suppl 1): 775.
- Jethava Y, Guru Murthy GS, Hamadani M. Relapse of Hodgkin lymphoma after autologous transplantation: time to rethink treatment? Hematol Oncol Stem Cell Ther. 2017; 10(2): 47–56.
- Bartlett NL, Chen R, Fanale MA, et al. Retreatment with brentuximab vedotin in patients with CD30-positive hematologic malignancies. J Hematol Oncol. 2014; 7: 24.
- Fukuhara N, Yamamoto Go, Tsujimura H, et al. Retreatment with brentuximab vedotin in patients with relapsed/refractory classical Hodgkin lymphoma or systemic anaplastic large-cell lymphoma: a multicenter retrospective study. Leuk Lymphoma. 2020; 61(1): 176–180.
- Armand P, Engert A, Younes A, et al. Nivolumab for relapsed/refractory classic Hodgkin lymphoma after failure of autologous hematopoietic cell transplantation: extended follow-up of the multicohort single-arm phase II CheckMate 205 trial. J Clin Oncol. 2018; 36(14): 1428–1439.
- Roemer MGM, Advani RH, Ligon AH, et al. PD-L1 and PD-L2 genetic alterations define classical Hodgkin lymphoma and predict outcome. J Clin Oncol. 2016; 34(23): 2690–2697.
- Roemer MGM, Advani RH, Redd RA, et al. Classical Hodgkin lymphoma with reduced β2M/MHC class I expression is associated with inferior outcome independent of 9p24.1 status. Cancer Immunol Res. 2016; 4(11): 910–916.
- Zinzani PL, Chen R, Armand P, et al. Pembrolizumab monotherapy in patients with primary refractory classical hodgkin lymphoma who relapsed after salvage autologous stem cell transplantation and/or brentuximab vedotin therapy: KEYNOTE-087 subgroup analysis. Leuk Lymphoma. 2020; 61(4): 950–954.
- Armand P, Kuruvilla J, Michot JM, et al. KEYNOTE-013 4-year follow-up of pembrolizumab in classical Hodgkin lymphoma after brentuximab vedotin failure. Blood Adv. 2020; 4(12): 2617–2622.
- Kasamon YL, de Claro RA, Wang Y, et al. FDA approval summary: nivolumab for the treatment of relapsed or progressive classical Hodgkin lymphoma. Oncologist. 2017; 22(5): 585–591.
- De Philippis C, Legrand-Izadifar F, Bramanti S, et al. Checkpoint inhibition before haploidentical transplantation with posttransplant cyclophosphamide in Hodgkin lymphoma. Blood Adv. 2020; 4(7): 1242–1249.
- Chen R, Zinzani PL, Fanale MA, et al. KEYNOTE-087. Phase II study of the efficacy and safety of pembrolizumab for relapsed/refractory classic Hodgkin lymphoma. J Clin Oncol. 2017; 35(19): 2125–2132.
- Chen R, Zinzani P, Lee H, et al. Pembrolizumab in relapsed or refractory Hodgkin lymphoma: 2-year follow-up of KEYNOTE-087. Blood. 2019; 134(14): 1144–1153.
- Herbaux C, Merryman R, Devine S, et al. Recommendations for managing PD-1 blockade in the context of allogeneic HCT in Hodgkin lymphoma: taming a necessary evil. Blood. 2018; 132(1): 9–16.
- Martínez C, Carpio C, Heras I, et al. Spanish Group of Lymphoma and Bone Marrow Transplantation (GELTAMO). Potential survival benefit for patients receiving allogeneic hematopoietic stem cell transplantation after nivolumab therapy for relapse/refractory Hodgkin lymphoma: real-life experience in Spain. Biol Blood Marrow Transplant. 2020; 26(8): 1534–1542.
- Manson G, Mear JB, Herbaux C, et al. LYSA. Long-term efficacy of anti-PD1 therapy in Hodgkin lymphoma with and without allogenic stem cell transplantation. Eur J Cancer. 2019; 115: 47–56.
- Shah GL, Moskowitz CH. Transplant strategies in relapsed/refractory Hodgkin lymphoma. Blood. 2018; 131(15): 1689–1697.
- Carreau NA, Pail O, Armand P, et al. Checkpoint blockade treatment may sensitize Hodgkin lymphoma to subsequent therapy. Oncologist. 2020; 25(10): 878–885.
- Dada R, Usman B. Allogeneic hematopoietic stem cell transplantation in r/r Hodgkin lymphoma after treatment with checkpoint inhibitors: Feasibility and safety. Eur J Haematol. 2019; 102(2): 150–156.
- Herbaux C, Gauthier J, Brice P, et al. Efficacy and tolerability of nivolumab after allogeneic transplantation for relapsed Hodgkin lymphoma. Blood. 2017; 129(18): 2471–2478.
- Haverkos BM, Abbott D, Hamadani M, et al. PD-1 blockade for relapsed lymphoma post-allogeneic hematopoietic cell transplant: high response rate but frequent GVHD. Blood. 2017; 130(2): 221–228.
- Grover NS, Park SI, Ivanova A, et al. A phase Ib/II study of anti-CD30 chimeric antigen receptor T cells for relapsed/refractory CD30+ lymphomas. Biology of Blood and Marrow Transplantation. 2019; 25(3): S66.
- Dickinson M, Johnstone RW, Prince HM. Histone deacetylase inhibitors: potential targets responsible for their anti-cancer effect. Invest New Drugs. 2010; 28(Suppl 1): S3–20.
- Younes A, Sureda A, Ben-Yehuda D, et al. Panobinostat in patients with relapsed/refractory Hodgkin's lymphoma after autologous stem-cell transplantation: results of a phase II study. J Clin Oncol. 2012; 30(18): 2197–2203.
- Hu B, Younes A, Westin JR, et al. Phase-I and randomized phase-II trial of panobinostat in combination with ICE (ifosfamide, carboplatin, etoposide) in relapsed or refractory classical Hodgkin lymphoma. Leuk Lymphoma. 2018; 59(4): 863–870.
- Van Den Neste E, André M, Gastinne T, et al. A phase II study of the oral JAK1/JAK2 inhibitor ruxolitinib in advanced relapsed/refractory Hodgkin lymphoma. Haematologica. 2018; 103(5): 840–848.
- Younes A, Romaguera J, Fanale M, et al. Phase I study of a novel oral Janus kinase 2 inhibitor, SB1518, in patients with relapsed lymphoma: evidence of clinical and biologic activity in multiple lymphoma subtypes. J Clin Oncol. 2012; 30(33): 4161–4167.
- Kim SJ, Kang HJ, Dong-Yeop S, et al. The efficacy of JAK2 inhibitor in heavily pretreated classical Hodgkin lymphoma: a prospective pilot study of ruxolitinib in relapsed or refractory classical Hodgkin lymphoma and primary mediastinal large B-cell lymphoma. Blood. 2016; 128(22): 1820–1820.
- Spina V, Bruscaggin A, Cuccaro A, et al. Circulating tumor DNA reveals genetics, clonal evolution, and residual disease in classical Hodgkin lymphoma. Blood. 2018; 131(22): 2413–2425.
- Schöder H, Moskowitz C. Metabolic tumor volume in lymphoma: hype or hope? J Clin Oncol. 2016; 34(30): 3591–3594.
- Gillies RJ, Kinahan PE, Hricak H. Radiomics: images are more than pictures, they are data. Radiology. 2016; 278(2): 563–577.
- Lue KH, Wu YF, Liu SH, et al. Intratumor heterogeneity assessed by F-FDG PET/CT predicts treatment response and survival outcomes in patients with Hodgkin lymphoma. Acad Radiol. 2020; 27(8): e183–e192.
- Milgrom SA, Elhalawani H, Lee J, et al. A PET radiomics model to predict refractory mediastinal Hodgkin lymphoma. Sci Rep. 2019; 9(1): 1322.
