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1
Capturing Hyperprogressive disease with immune checkpoint inhibitors using RECIST
1.1 criteria.
Ignacio Matos1,2*
, Juan Martin-Liberal1, Alonso García-Ruiz
3, Cinta Hierro
1, Maria Ochoa de
Olza1, Cristina Viaplana
4, Analia Azaro
1, Maria Vieito
1, Irene Braña
1, Gemma Mur
5, Javier
Ros1, Jose Mateos
6, Guillermo Villacampa
4, Roger Berché
4, Mafalda Oliveira
1, Maria
Alsina1, Elena Elez
1, Ana Oaknin
1, Eva Muñoz-Couselo
1, Joan Carles
1, Enriqueta Felip
1,2,
Jordi Rodón1, Josep Tabernero
1,2, Rodrigo Dienstmann
4, Raquel Perez-Lopez
3, and Elena
Garralda1*
.
1. Department of Medical Oncology, Vall d’Hebron University Hospital. Vall d'Hebron Institute of Oncology (VHIO), Barcelona, Spain
2. Deparment of Medicine. Universidad Autónoma de Barcelona
3. Radiomics Group, Vall d’Hebron Institute of Oncology (VHIO), Barcelona, Spain
4. Oncology Data Science (OdysSey) Group, Vall d'Hebron Institute of Oncology (VHIO), Barcelona, Spain.
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
1. Hodi FS, O'Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010;363(8):711-23. 2. Larkin J, Chiarion-Sileni V, Gonzalez R, Grob JJ, Cowey CL, Lao CD, et al. Combined Nivolumab and Ipilimumab or Monotherapy in Untreated Melanoma. N Engl J Med. 2015;373(1):23-34. 3. Schachter J, Ribas A, Long GV, Arance A, Grob JJ, Mortier L, et al. Pembrolizumab versus ipilimumab for advanced melanoma: final overall survival results of a multicentre, randomised, open-label phase 3 study (KEYNOTE-006). Lancet (London, England). 2017;390(10105):1853-62. 4. Borghaei H, Paz-Ares L, Horn L, Spigel DR, Steins M, Ready NE, et al. Nivolumab versus Docetaxel in Advanced Nonsquamous Non-Small-Cell Lung Cancer. N Engl J Med. 2015;373(17):1627-39. 5. Herbst RS, Baas P, Kim DW, Felip E, Perez-Gracia JL, Han JY, et al. Pembrolizumab versus docetaxel for previously treated, PD-L1-positive, advanced non-small-cell lung cancer (KEYNOTE-010): a randomised controlled trial. Lancet (London, England). 2016;387(10027):1540-50. 6. Rittmeyer A, Barlesi F, Waterkamp D, Park K, Ciardiello F, von Pawel J, et al. Atezolizumab versus docetaxel in patients with previously treated non-small-cell lung cancer (OAK): a phase 3, open-label, multicentre randomised controlled trial. Lancet (London, England). 2017;389(10066):255-65. 7. Hellmann MD, Ciuleanu TE, Pluzanski A, Lee JS, Otterson GA, Audigier-Valette C, et al. Nivolumab plus Ipilimumab in Lung Cancer with a High Tumor Mutational Burden. N Engl J Med. 2018;378(22):2093-104. 8. Socinski MA, Jotte RM, Cappuzzo F, Orlandi F, Stroyakovskiy D, Nogami N, et al. Atezolizumab for First-Line Treatment of Metastatic Nonsquamous NSCLC. N Engl J Med. 2018;378(24):2288-301. 9. Ferris RL, Blumenschein G, Jr., Fayette J, Guigay J, Colevas AD, Licitra L, et al. Nivolumab for Recurrent Squamous-Cell Carcinoma of the Head and Neck. N Engl J Med. 2016;375(19):1856-67. 10. Burtness B, Harrington KJ, Greil R, Soulières D, Tahara M, De Castro JG, et al. LBA8_PRKEYNOTE-048: Phase III study of first-line pembrolizumab (P) for recurrent/metastatic head and neck squamous cell carcinoma (R/M HNSCC). Annals of Oncology. 2018;29(suppl_8):mdy424.045-mdy424.045. 11. Bellmunt J, de Wit R, Vaughn DJ, Fradet Y, Lee J-L, Fong L, et al. Pembrolizumab as Second-Line Therapy for Advanced Urothelial Carcinoma. New England Journal of Medicine. 2017;376(11):1015-26. 12. Powles T, Durán I, van der Heijden MS, Loriot Y, Vogelzang NJ, De Giorgi U, et al. Atezolizumab versus chemotherapy in patients with platinum-treated locally advanced or metastatic urothelial carcinoma (IMvigor211): a multicentre, open-label, phase 3 randomised controlled trial. The Lancet. 2018;391(10122):748-57. 13. Motzer RJ, Escudier B, McDermott DF, George S, Hammers HJ, Srinivas S, et al. Nivolumab versus Everolimus in Advanced Renal-Cell Carcinoma. N Engl J Med. 2015;373(19):1803-13.
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
14. Motzer RJ, Tannir NM, McDermott DF, Aren Frontera O, Melichar B, Choueiri TK, et al. Nivolumab plus Ipilimumab versus Sunitinib in Advanced Renal-Cell Carcinoma. N Engl J Med. 2018;378(14):1277-90. 15. Kaufman HL, Russell J, Hamid O, Bhatia S, Terheyden P, D'Angelo SP, et al. Avelumab in patients with chemotherapy-refractory metastatic Merkel cell carcinoma: a multicentre, single-group, open-label, phase 2 trial. The Lancet Oncology. 2016;17(10):1374-85. 16. Chung HC, Schellens JHM, Delord J-P, Perets R, Italiano A, Shapira-Frommer R, et al. Pembrolizumab treatment of advanced cervical cancer: Updated results from the phase 2 KEYNOTE-158 study. Journal of Clinical Oncology. 2018;36(15_suppl):5522-. 17. Le DT, Uram JN, Wang H, Bartlett BR, Kemberling H, Eyring AD, et al. PD-1 Blockade in Tumors with Mismatch-Repair Deficiency. N Engl J Med. 2015;372(26):2509-20. 18. Le DT, Durham JN, Smith KN, Wang H, Bartlett BR, Aulakh LK, et al. Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade. Science (New York, NY). 2017;357(6349):409-13. 19. Diaz L, Marabelle A, Kim TW, Geva R, Van Cutsem E, André T, et al. 386PEfficacy of pembrolizumab in phase 2 KEYNOTE-164 and KEYNOTE-158 studies of microsatellite instability high cancers. Annals of Oncology. 2017;28(suppl_5):mdx367.020-mdx367.020. 20. Chiou VL, Burotto M. Pseudoprogression and Immune-Related Response in Solid Tumors. Journal of clinical oncology : official journal of the American Society of Clinical Oncology. 2015;33(31):3541-3. 21. Wolchok JD, Hoos A, O'Day S, Weber JS, Hamid O, Lebbe C, et al. Guidelines for the Evaluation of Immune Therapy Activity in Solid Tumors: Immune-Related Response Criteria. Clinical Cancer Research. 2009;15(23):7412-20. 22. Nishino M, Giobbie-Hurder A, Gargano M, Suda M, Ramaiya NH, Hodi FS. Developing a common language for tumor response to immunotherapy: immune-related response criteria using unidimensional measurements. Clin Cancer Res. 2013;19(14):3936-43. 23. Seymour L, Bogaerts J, Perrone A, Ford R, Schwartz LH, Mandrekar S, et al. iRECIST: guidelines for response criteria for use in trials testing immunotherapeutics. The Lancet Oncology. 2017;18(3):e143-e52. 24. Champiat S, Ferrara R, Massard C, Besse B, Marabelle A, Soria J-C, et al. Hyperprogressive disease: recognizing a novel pattern to improve patient management. Nature Reviews Clinical Oncology. 2018. 25. Borcoman E, Kanjanapan Y, Champiat S, Kato S, Servois V, Kurzrock R, et al. Novel patterns of response under immunotherapy. Annals of oncology : official journal of the European Society for Medical Oncology. 2019. 26. Reck M, Rodriguez-Abreu D, Robinson AG, Hui R, Csoszi T, Fulop A, et al. Pembrolizumab versus Chemotherapy for PD-L1-Positive Non-Small-Cell Lung Cancer. N Engl J Med. 2016;375(19):1823-33. 27. Champiat S, Dercle L, Ammari S, Massard C, Hollebecque A, Postel-Vinay S, et al. Hyperprogressive Disease Is a New Pattern of Progression in Cancer Patients Treated by Anti-PD-1/PD-L1. Clin Cancer Res. 2017;23(8):1920-8. 28. Saada-Bouzid E, Defaucheux C, Karabajakian A, Coloma VP, Servois V, Paoletti X, et al. Hyperprogression during anti-PD-1/PD-L1 therapy in patients with recurrent and/or metastatic head and neck squamous cell carcinoma. Annals of oncology : official journal of the European Society for Medical Oncology. 2017;28(7):1605-11.
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
29. Ferrara R, Mezquita L, Texier M, Lahmar J, Audigier-Valette C, Tessonnier L, et al. Hyperprogressive Disease in Patients With Advanced Non–Small Cell Lung Cancer Treated With PD-1/PD-L1 Inhibitors or With Single-Agent Chemotherapy. JAMA Oncology. 2018. 30. Kato S, Goodman A, Walavalkar V, Barkauskas DA, Sharabi A, Kurzrock R. Hyperprogressors after Immunotherapy: Analysis of Genomic Alterations Associated with Accelerated Growth Rate. Clin Cancer Res. 2017;23(15):4242-50. 31. Ferte C, Fernandez M, Hollebecque A, Koscielny S, Levy A, Massard C, et al. Tumor growth rate is an early indicator of antitumor drug activity in phase I clinical trials. Clinical cancer research : an official journal of the American Association for Cancer Research. 2014;20(1):246-52. 32. Long GV, Weber JS, Larkin J, Atkinson V, Grob JJ, Schadendorf D, et al. Nivolumab for Patients With Advanced Melanoma Treated Beyond Progression: Analysis of 2 Phase 3 Clinical Trials. JAMA Oncol. 2017;3(11):1511-9. 33. Escudier B, Motzer RJ, Sharma P, Wagstaff J, Plimack ER, Hammers HJ, et al. Treatment Beyond Progression in Patients with Advanced Renal Cell Carcinoma Treated with Nivolumab in CheckMate 025. European urology. 2017;72(3):368-76. 34. Mateo J, Chakravarty D, Dienstmann R, Jezdic S, Gonzalez-Perez A, Lopez-Bigas N, et al. A framework to rank genomic alterations as targets for cancer precision medicine: the ESMO Scale for Clinical Actionability of molecular Targets (ESCAT). Annals of oncology : official journal of the European Society for Medical Oncology. 2018;29(9):1895-902. 35. Mezquita L, Auclin E, Ferrara R, Charrier M, Remon J, Planchard D, et al. Association of the Lung Immune Prognostic Index With Immune Checkpoint Inhibitor Outcomes in Patients With Advanced Non-Small Cell Lung Cancer. JAMA oncology. 2018;4(3):351-7. 36. Rodriguez Freixinos V, Garcia A, Fasani R, Castellvi J, Ruiz-Pace F, Viaplana C, et al. Immune profile and outcomes of patients (pts) with gynecological malignancies (GYN) enrolled in early phases immunotherapy (IO) trials. American Society of Clinical Oncology; 2018. 37. Suárez C, Morales-Barrera R, Garcia-Ruiz A, Gonzalez M, Ligero M, Valverde C, et al. Hyperprogressive disease in patients with metastatic genitourinary tumors treated with immune checkpoint inhibitors. American Society of Clinical Oncology; 2019. 38. Ferte C, Koscielny S, Albiges L, Rocher L, Soria JC, Iacovelli R, et al. Tumor growth rate provides useful information to evaluate sorafenib and everolimus treatment in metastatic renal cell carcinoma patients: an integrated analysis of the TARGET and RECORD phase 3 trial data. European urology. 2014;65(4):713-20. 39. Patnaik A, Kang SP, Rasco D, Papadopoulos KP, Elassaiss-Schaap J, Beeram M, et al. Phase I Study of Pembrolizumab (MK-3475; Anti-PD-1 Monoclonal Antibody) in Patients with Advanced Solid Tumors. Clin Cancer Res. 2015;21(19):4286-93. 40. Brahmer JR, Drake CG, Wollner I, Powderly JD, Picus J, Sharfman WH, et al. Phase I study of single-agent anti-programmed death-1 (MDX-1106) in refractory solid tumors: safety, clinical activity, pharmacodynamics, and immunologic correlates. J Clin Oncol. 2010;28(19):3167-75. 41. Herbst RS, Soria JC, Kowanetz M, Fine GD, Hamid O, Gordon MS, et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature. 2014;515(7528):563-7. 42. Fairman D, Narwal R, Liang M, Robbins PB, Schneider A, Chavez C, et al. Pharmacokinetics of MEDI4736, a fully human anti-PDL1 monoclonal antibody, in patients with advanced solid tumors. Journal of Clinical Oncology. 2014;32(15_suppl):2602-.
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
43. Osa A, Uenami T, Koyama S, Fujimoto K, Okuzaki D, Takimoto T, et al. Clinical implications of monitoring nivolumab immunokinetics in non-small cell lung cancer patients. JCI insight. 2018;3(19). 44. Scapin G, Yang X, Prosise WW, McCoy M, Reichert P, Johnston JM, et al. Structure of full-length human anti-PD1 therapeutic IgG4 antibody pembrolizumab. Nature structural & molecular biology. 2015;22(12):953-8. 45. Wang C, Thudium KB, Han M, Wang XT, Huang H, Feingersh D, et al. In vitro characterization of the anti-PD-1 antibody nivolumab, BMS-936558, and in vivo toxicology in non-human primates. Cancer immunology research. 2014;2(9):846-56. 46. Zhang T, Song X, Xu L, Ma J, Zhang Y, Gong W, et al. The binding of an anti-PD-1 antibody to FcgammaRIota has a profound impact on its biological functions. Cancer immunology, immunotherapy : CII. 2018;67(7):1079-90. 47. Lo Russo G, Moro M, Sommariva M, Cancila V, Boeri M, Centonze G, et al. Antibody-Fc/FcR Interaction on Macrophages as a Mechanism for Hyperprogressive Disease in Non-Small Cell Lung Cancer Subsequent to PD-1/PD-L1 Blockade. Clin Cancer Res. 2018. 48. Horn L, Mansfield AS, Szczesna A, Havel L, Krzakowski M, Hochmair MJ, et al. First-Line Atezolizumab plus Chemotherapy in Extensive-Stage Small-Cell Lung Cancer. N Engl J Med. 2018. 49. Antonia SJ, Villegas A, Daniel D, Vicente D, Murakami S, Hui R, et al. Durvalumab after Chemoradiotherapy in Stage III Non-Small-Cell Lung Cancer. N Engl J Med. 2017;377(20):1919-29. 50. Frelaut M, Le Tourneau C, Borcoman E. Hyperprogression under Immunotherapy. International Journal of Molecular Sciences. 2019;20(11):2674.
FIGURE LEGENDS
Figure 1. Definition of HPD, according TGR criteria and RECIST criteria
Figure 2. Overall Survival for Hyperprogressive Disease (HPD) Compared With non-HPD
progressors by RECIST and TGR criteria in the ICIs and TAs cohorts. A. RECIST criteria in
ICIs cohort. B. TGR criteria in ICIs cohort. C. RECIST criteria in TAs cohort. D. TGR
criteria in TAs cohort.
Figure 3. Tumor growth rate during the reference and the experimental period of the patients
included in the ICIs and TAs cohorts who were evaluable for HPD following both criteria.
Patients with new lesions are also shown. Patients categorized as HPD following TGR are
marked in red, patients categorized as HPD following RECIST criteria are marked with an R.
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226
Published OnlineFirst November 22, 2019.Clin Cancer Res Ignacio Matos, Juan Martin-Liberal, Alonso Garcia-Ruiz, et al. inhibitors using RECIST 1.1 criteriaCapturing Hyperprogressive disease with immune checkpoint
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Author manuscripts have been peer reviewed and accepted for publication but have not yet been edited. Author Manuscript Published OnlineFirst on November 22, 2019; DOI: 10.1158/1078-0432.CCR-19-2226