Checkpoint inhibition therapy as possible frontline therapy for Hodgkin lymphoma

References

• Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA A Cancer J Clin. 2019;69:7–34.
   PubMed Web of Science ®Google Scholar
• Hodgkin L. Cancer stat facts; [cited 2019 Jul 12]. Available from: https://seer.cancer.gov/statfacts/html/hodg.html
   Google Scholar
• Brenner H, Gondos A, Pulte D. Ongoing improvement in long-term survival of patients with Hodgkin disease at all ages and recent catch-up of older patients. Blood. 2008;111:2977–2983.
   PubMed Web of Science ®Google Scholar
• Glaser SL, Jarrett RF. The epidemiology of Hodgkin’s disease. Baillieres Clin Haematol. 1996;9:401–416.
   PubMed Web of Science ®Google Scholar
• Ansell SM. Hodgkin lymphoma: 2018 update on diagnosis, risk-stratification, and management. Am J Hematol. 2018;93:704–715.
   PubMed Web of Science ®Google Scholar
• Borchmann P, Haverkamp H, Lohri A, et al. Progression-free survival of early interim PET-positive patients with advanced stage Hodgkin’s lymphoma treated with BEACOPPescalated alone or in combination with rituximab (HD18): an open-label, international, randomised phase 3 study by the German Hodgkin Study Group. Lancet Oncol. 2017;18:454–463.
   PubMed Web of Science ®Google Scholar
• Casasnovas R-O, Bouabdallah R, Brice P, et al. PET-adapted treatment for newly diagnosed advanced Hodgkin lymphoma (AHL2011): a randomised, multicentre, non-inferiority, phase 3 study. Lancet Oncol. 2019;20:202–215.
   PubMed Web of Science ®Google Scholar
• Johnson P, Federico M, Kirkwood A, et al. Adapted treatment guided by interim PET-CT scan in advanced Hodgkin’s lymphoma. N Engl J Med. 2016;374:2419–2429.
   PubMed Web of Science ®Google Scholar
• Evens AM, Hong F, Gordon LI, et al. The efficacy and tolerability of adriamycin, bleomycin, vinblastine, dacarbazine and Stanford V in older Hodgkin lymphoma patients: a comprehensive analysis from the North American intergroup trial E2496. Br J Haematol. 2013;161:76–86.
   PubMed Web of Science ®Google Scholar
• Canellos GP, Anderson JR, Propert KJ, et al. Chemotherapy of advanced Hodgkin’s disease with MOPP, ABVD, or MOPP alternating with ABVD. N Engl J Med. 1992;327:1478–1484.
   PubMed Web of Science ®Google Scholar
• Santoro A, Bonadonna G, Valagussa P, et al. Long-term results of combined chemotherapy-radiotherapy approach in Hodgkin’s disease: superiority of ABVD plus radiotherapy versus MOPP plus radiotherapy. J Clin Oncol. 1987;5:27–37.
   PubMed Web of Science ®Google Scholar
• Schaapveld M, Aleman BMP, van Eggermond AM, et al. Second cancer risk up to 40 years after treatment for Hodgkin's lymphoma. N Engl J Med. 2015;373:2499–2511.
   PubMed Web of Science ®Google Scholar
• van Leeuwen FE, Ng AK. Long-term risk of second malignancy and cardiovascular disease after Hodgkin lymphoma treatment. Hematology Am Soc Hematol Educ Program. 2016;2016:323–330.
   PubMed Web of Science ®Google Scholar
• Al-Juhaishi T, Khurana A, Shafer D. Therapy-related myeloid neoplasms in lymphoma survivors: reducing risks. Best Pract Res Clin Haematol. 2019;32:47–53.
   PubMed Web of Science ®Google Scholar
• 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;36:1428–1439.
   PubMed Web of Science ®Google Scholar
• Ansell SM, Lesokhin AM, Borrello I, et al. PD-1 blockade with nivolumab in relapsed or refractory Hodgkin’s lymphoma. N Engl J Med. 2015;372:311–319.
   PubMed Web of Science ®Google Scholar
• Younes A, Santoro A, Shipp M, et al. Nivolumab for classical Hodgkin’s lymphoma after failure of both autologous stem-cell transplantation and brentuximab vedotin: a multicentre, multicohort, single-arm phase 2 trial. Lancet Oncol. 2016;17:1283–1294.
   PubMed Web of Science ®Google Scholar
• Chen R, Gopal AK, Smith SE, et al. Five-year survival and durability results of brentuximab vedotin in patients with relapsed or refractory Hodgkin lymphoma. Blood. 2016;128:1562–1566.
   PubMed Web of Science ®Google Scholar
• Armand P, Shipp MA, Ribrag V, et al. Programmed death-1 blockade with pembrolizumab in patients with classical Hodgkin lymphoma after brentuximab vedotin failure. J Clin Oncol. 2016;34:3733–3739.
   PubMed Web of Science ®Google Scholar
• Connors JM, Jurczak W, Straus DJ, et al. Brentuximab vedotin with chemotherapy for stage III or IV Hodgkin's lymphoma. N Engl J Med. 2018;378:331–344.
   PubMed Web of Science ®Google Scholar
• Ramchandren R, Advani RH, Ansell SM, et al. Brentuximab vedotin plus chemotherapy in North American subjects with newly diagnosed stage III or IV Hodgkin lymphoma. Clin Cancer Res. 2019;25:1718–1726.
   PubMed Web of Science ®Google Scholar
• Kanzler H, Küppers R, Hansmann ML, et al. Hodgkin and Reed–Sternberg cells in Hodgkin’s disease represent the outgrowth of a dominant tumor clone derived from (crippled) germinal center B cells. J Exp Med. 1996;184:1495–1505.
   PubMed Web of Science ®Google Scholar
• Ansell SM. Immunotherapy of Hodgkin lymphoma. Cancer J. 2018;24:249–253.
   PubMed Web of Science ®Google Scholar
• Niens M, Visser L, Nolte IM, et al. Serum chemokine levels in Hodgkin lymphoma patients: highly increased levels of CCL17 and CCL22. Br J Haematol. 2008;140:527–536.
   PubMed Web of Science ®Google Scholar
• Steidl C, Connors JM, Gascoyne RD. Molecular pathogenesis of Hodgkin’s lymphoma: increasing evidence of the importance of the microenvironment. J Clin Oncol. 2011;29:1812–1826.
   PubMed Web of Science ®Google Scholar
• Green MR, Monti S, Rodig SJ, et al. Integrative analysis reveals selective 9p24.1 amplification, increased PD-1 ligand expression, and further induction via JAK2 in nodular sclerosing Hodgkin lymphoma and primary mediastinal large B-cell lymphoma. Blood. 2010;116:3268–3277.
   PubMed Web of Science ®Google Scholar
• 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;34:2690–2697.
   PubMed Web of Science ®Google Scholar
• Muenst S, Hoeller S, Dirnhofer S, et al. Increased programmed death-1+ tumor-infiltrating lymphocytes in classical Hodgkin lymphoma substantiate reduced overall survival. Hum Pathol. 2009;40:1715–1722.
   PubMed Web of Science ®Google Scholar
• Steidl C, Shah SP, Woolcock BW, et al. MHC class II transactivator CIITA is a recurrent gene fusion partner in lymphoid cancers. Nature. 2011;471:377–381.
   PubMed Web of Science ®Google Scholar
• Küppers R. The biology of Hodgkin’s lymphoma. Nat Rev Cancer. 2009;9:15–27.
   PubMed Web of Science ®Google Scholar
• Green MR, Rodig S, Juszczynski P, et al. Constitutive AP-1 activity and EBV infection induce PD-L1 in Hodgkin lymphomas and posttransplant lymphoproliferative disorders: implications for targeted therapy. Clin Cancer Res. 2012;18:1611–1618.
   PubMed Web of Science ®Google Scholar
• Roemer MGM, Redd RA, Cader FZ, et al. Major histocompatibility complex class II and programmed death ligand 1 expression predict outcome after programmed death 1 blockade in classic Hodgkin lymphoma. J Clin Oncol. 2018;36:942–950.
   PubMed Web of Science ®Google Scholar
• Haabeth OAW, Tveita AA, Fauskanger M, et al. How do CD4+ T cells detect and eliminate tumor cells that either lack or express MHC class II molecules? Front Immunol. 2014;5:174.
   PubMed Web of Science ®Google Scholar
• Carey CD, Gusenleitner D, Lipschitz M, et al. Topological analysis reveals a PD-L1-associated microenvironmental niche for Reed–Sternberg cells in Hodgkin lymphoma. Blood. 2017;130:2420–2430.
   PubMed Web of Science ®Google Scholar
• Rengstl B, Schmid F, Weiser C, et al. Tumor-infiltrating HLA-matched CD4 + T cells retargeted against Hodgkin and Reed–Sternberg cells. Oncoimmunology. 2016;5:e1160186.
   PubMed Web of Science ®Google Scholar
• Roemer MGM, Advani RH, Redd RA, et al. Classical Hodgkin lymphoma with reduced 2M/MHC class I expression is associated with inferior outcome independent of 9p24.1 status. Cancer Immunol Res. 2016;4:910–916.
   PubMed Web of Science ®Google Scholar
• Nijland M, Veenstra RN, Visser L, et al. HLA dependent immune escape mechanisms in B-cell lymphomas: implications for immune checkpoint inhibitor therapy? Oncoimmunology. 2017;6:e1295202.
   PubMed Web of Science ®Google Scholar
• Vari F, Arpon D, Keane C, et al. Immune evasion via PD-1/PD-L1 on NK cells and monocyte/macrophages is more prominent in Hodgkin lymphoma than DLBCL. Blood. 2018;131:1809–1819.
   PubMed Web of Science ®Google Scholar
• Rouas-Freiss N, Moreau P, Lemaoult J, et al. The dual role of HLA-G in cancer. J Immunol Res. 2014;2014:1–10.
   Web of Science ®Google Scholar
• Wilson EB, El-Jawhari JJ, Neilson AL, et al. Human tumour immune evasion via TGF-β blocks NK cell activation but not survival allowing therapeutic restoration of anti-tumour activity. PLoS One. 2011;6:e22842.
   PubMed Web of Science ®Google Scholar
• Aldinucci D, Borghese C, Casagrande N. Formation of the immunosuppressive microenvironment of classic Hodgkin lymphoma and therapeutic approaches to counter it. Int J Mol Sci. 2019;20:2416.
   PubMed Web of Science ®Google Scholar
• Cader FZ, Schackmann RCJ, Hu X, et al. Mass cytometry of Hodgkin lymphoma reveals a CD4+ exhausted T-effector and T-regulatory cell rich microenvironment. Blood. 2018;132:825–843714.
   PubMed Web of Science ®Google Scholar
• Chen R, Zinzani PL, Fanale MA, et al. Phase II study of the efficacy and safety of pembrolizumab for relapsed/refractory classic Hodgkin lymphoma. J Clin Oncol. 2017;35:2125–2132.
   PubMed Web of Science ®Google Scholar
• Zinzani PL, Chen RW, Lee HJ, et al. Two-year follow-up of Keynote-087 Study: pembrolizumab monotherapy in relapsed/refractory classic Hodgkin lymphoma. Blood. 2018;132:2900.
   Google Scholar
• Ansell S, Gutierrez ME, Shipp MA, et al. A phase 1 study of nivolumab in combination with ipilimumab for relapsed or refractory hematologic malignancies (CheckMate 039). Blood. 2016;128:183.
   Web of Science ®Google Scholar
• 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;131:1183–1194.
   PubMed Web of Science ®Google Scholar
• Ramchandren R, Domingo-Domènech E, Rueda A, et al. Nivolumab for newly diagnosed advanced-stage classic Hodgkin lymphoma: safety and efficacy in the Phase II CheckMate 205 Study. J Clin Oncol. 2019;19:1997–2007.
   Google Scholar
• Shi Y, Su H, Song Y, et al. Safety and activity of sintilimab in patients with relapsed or refractory classical Hodgkin lymphoma (ORIENT-1): a multicentre, single-arm, phase 2 trial. Lancet Haematol. 2019;6:e12–e19.
   PubMed Web of Science ®Google Scholar
• Song Y, Gao Q, Zhang H, et al. Treatment of relapsed or refractory classical Hodgkin lymphoma with the anti-PD-1, tislelizumab: results of a phase 2, single-arm, multicenter study. Leukemia. Forthcoming. [2019].
   Google Scholar
• 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;22:585–591.
   PubMed Web of Science ®Google Scholar
• Moskowitz CH, Zinzani PL, Fanale MA, et al. Pembrolizumab in relapsed/refractory classical Hodgkin lymphoma: primary end point analysis of the Phase 2 Keynote-087 Study. Blood. 2016;128:1107–1107.
   Web of Science ®Google Scholar
• Diefenbach CS, Hong F, Cohen JB, et al. Preliminary safety and efficacy of the combination of brentuximab vedotin and ipilimumab in relapsed/refractory Hodgkin lymphoma: a trial of the ECOG-ACRIN Cancer Research Group (E4412). Blood. 2015;126:585–585.
   Web of Science ®Google Scholar
• Diefenbach CS, Hong F, David KA, et al. Title: a phase I study with an expansion cohort of the combination of ipilimumab and nivolumab and brentuximab vedotin in patients with relapsed/refractory Hodgkin lymphoma: a trial of the ECOG-ACRIN Cancer Research Group (E4412 Arms D and E). Blood. 2016;128:1106–1106.
   Web of Science ®Google Scholar
• Diefenbach C, Hong F, Ambinder RF, et al. A phase I study with an expansion cohort of the combinations of ipilimumab, nivolumab and brentuximab vedotin in patients with relapsed/refractory Hodgkin lymphoma: a trial of the ECOG-ACRIN Research Group (E4412: Arms G-I). Blood. 2018;132:679–679.
   Web of Science ®Google Scholar
• Bröckelmann P. Nivolumab and AVD for early-stage unfavorable Hodgkin lymphoma (NIVAHL). Blood. 2019;134(Supplement_1):236.
   Google Scholar
• Ansell S, Ramchandren R, Domingo-Domènech E, et al. Nivolumab plus doxorubicin, vinblastine and dacarbazine for newly diagnosed advanced-stage classical Hodgkin lymphoma: Checkmate 205 Cohort D 2-Year Follow-Up. Hematol Oncol. 2019;37:146–147.
   Google Scholar
• Cottereau A-S, Versari A, Loft A, et al. Prognostic value of baseline metabolic tumor volume in early-stage Hodgkin lymphoma in the standard arm of the H10 trial. Blood. 2018;131:1456–1463.
   PubMed Web of Science ®Google Scholar
• Savas H, Allen P, Evens AM, et al. A phase II study of sequential pembrolizumab (PEM) followed by AVD for frontline treatment of classical Hodgkin lymphoma (CHL): quantifying response following PEM monotherapy with FDG-PET-derived metabolic tumor volume and total lesion glycolysis. Blood. 2018;132:1651.
   Web of Science ®Google Scholar
• Bröckelmann PJ, McMullen S, Wilson JB, et al. Patient and physician preferences for first-line treatment of classical Hodgkin lymphoma in Germany, France and the United Kingdom. Br J Haematol. 2019;184:202–214.
   Google Scholar
• Kreissl S, Goergen H, Müller H, et al. Survivors' perspectives on risks and benefits of Hodgkin lymphoma treatment: results of a survey by the German Hodgkin Study Group. Leuk Lymphoma. 2018;60:1389–1398.
   Google Scholar
• Hato SV, Khong A, de Vries IJM, et al. Molecular pathways: the immunogenic effects of platinum-based chemotherapeutics. Clin Cancer Res. 2014;20:2831–2837.
   PubMed Web of Science ®Google Scholar
• Apetoh L, Ladoire S, Coukos G, et al. Combining immunotherapy and anticancer agents: the right path to achieve cancer cure? Ann Oncol. 2015;26:1813–1823.
   PubMed Web of Science ®Google Scholar
• Kodumudi KN, Woan K, Gilvary DL, et al. A novel chemoimmunomodulating property of docetaxel: suppression of myeloid-derived suppressor cells in tumor bearers. Clin Cancer Res. 2010;16:4583–4594.
   PubMed Web of Science ®Google Scholar
• Song Z, Yu X, Zhang Y. Altered expression of programmed death-ligand 1 after neo-adjuvant chemotherapy in patients with lung squamous cell carcinoma. Lung Cancer. 2016;99:166–171.
   PubMed Web of Science ®Google Scholar
• Ramakrishnan R, Assudani D, Nagaraj S, et al. Chemotherapy enhances tumor cell susceptibility to CTL-mediated killing during cancer immunotherapy in mice. J Clin Invest. 2010;120:1111–1124.
   PubMed Web of Science ®Google Scholar
• Gandhi L, Rodríguez-Abreu D, Gadgeel S, et al. Pembrolizumab plus chemotherapy in metastatic non-small-cell lung cancer. N Engl J Med. 2018;378:2078–2092.
   PubMed Web of Science ®Google Scholar
• Reck M, Rodríguez-Abreu D, Robinson AG, et al. Pembrolizumab versus chemotherapy for PD-L1-positive non-small-cell lung cancer. N Engl J Med. 2016;375:1823–1833.
   PubMed Web of Science ®Google Scholar
• Cheson BD, Ansell S, Schwartz L, et al. Refinement of the Lugano Classification lymphoma response criteria in the era of immunomodulatory therapy. Blood. 2016;128:2489–2496.
   PubMed Web of Science ®Google Scholar
• 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;15:7412–7420.
   PubMed Web of Science ®Google Scholar
• Cheson BD, Pfistner B, Juweid ME, et al. Revised response criteria for malignant lymphoma. J Clin Oncol. 2007;25:579–586.
   PubMed Web of Science ®Google Scholar
• Tumeh PC, Harview CL, Yearley JH, et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature. 2014;515:568–571.
   PubMed Web of Science ®Google Scholar
• Andersen MD, Kamper P, d’Amore A, et al. The incidence of bleomycin induced lung toxicity is increased in Hodgkin lymphoma patients over 45 years exposed to granulocyte-colony stimulating growth factor. Leuk Lymphoma. 2019;60:927–933.
   PubMed Web of Science ®Google Scholar
• Willenbacher W, Mumm A, Bartsch HH. Late pulmonary toxicity of bleomycin. J Clin Oncol. 1998;16:3205.
   PubMed Web of Science ®Google Scholar
• Martin WG, Ristow KM, Habermann TM, et al. Bleomycin pulmonary toxicity has a negative impact on the outcome of patients with Hodgkin’s lymphoma. J Clin Oncol. 2005;23:7614–7620.
   PubMed Web of Science ®Google Scholar
• Evens AM, Advani RH, Helenowski IB, et al. Multicenter phase II study of sequential brentuximab vedotin and doxorubicin, vinblastine, and dacarbazine chemotherapy for older patients with untreated classical Hodgkin lymphoma. J Clin Oncol. 2018;36:3015–3022.
   PubMed Web of Science ®Google Scholar
• O'Dwyer KM, Friedberg JW. Chemoimmunotherapy in advanced-stage Hodgkin lymphoma: can we define a unified regimen for all ages? Hematologist. 2019;16(5).
   Google Scholar