Baseline peripheral blood biomarkers associated with clinical outcome of advanced melanoma patients treated with ipilimumab

Clinical Cancer Research

Volumn 22, Issue 12, 2016, Pages 2908-2918

  Martens, Alexander ^a   Wistuba Hamprecht, Kilian ^a   Foppen, Marnix Geukes ^b   Yuan, Jianda ^c   Postow, Michael A ^c,d   Wong, Phillip ^c   Romano, Emanuela ^e   Khammari, Amir ^f   Dreno, Brigitte ^f   Capone, Mariaelena ^g   Ascierto, Paolo A ^g   Di Giacomo, Anna Maria ^h   Maio, Michele ^h   Schilling, Bastian ^i,j   Sucker, Antje ^i,j   Schadendorf, Dirk ^i,j   Hassel, Jessica C ^j,k   Eigentler, Thomas K ^a   Martus, Peter ^l   Wolchok, Jedd D ^c,d   Blank, Christian ^b   Pawelec, Graham ^a   Garbe, Claus ^a   Weide, Benjamin ^a,l   more..

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^b NETHERLANDS CANCER INSTITUTE   (Netherlands)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

^e INSTITUT CURIE   (France)

^f INSERM   (France)

^g NATIONAL CANCER INSTITUTE   (Italy)

^h UNIVERSITY HOSPITAL OF SIENA   (Italy)

ⁱ UNIVERSITY HOSPITAL ESSEN   (Germany)

^j GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^k UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^l UNIVERSITY OF TÜBINGEN   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

IPILIMUMAB; LACTATE DEHYDROGENASE; TRANSCRIPTION FACTOR FOXP3; IMMUNOLOGICAL ANTINEOPLASTIC AGENT; TUMOR MARKER;

ADULT; ADVANCED CANCER; ARTICLE; BLOOD; BLOOD CELL COUNT; CALIBRATION; CANCER PROGNOSIS; CANCER STAGING; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CLINICAL FEATURE; COHORT ANALYSIS; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; EOSINOPHIL COUNT; FEMALE; FLOW CYTOMETRY; HELPER CELL; HUMAN; KAPLAN MEIER METHOD; LACTATE DEHYDROGENASE BLOOD LEVEL; LYMPHOCYTE COUNT; MAJOR CLINICAL STUDY; MALE; MELANOMA; MONOCYTE; OVERALL SURVIVAL; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROPORTIONAL HAZARDS MODEL; PROSPECTIVE STUDY; REGULATORY T LYMPHOCYTE; SURVIVAL ANALYSIS; T LYMPHOCYTE ACTIVATION; VALIDATION PROCESS; AGED; CYTOLOGY; ERYTHROCYTE COUNT; MORTALITY; MYELOID-DERIVED SUPPRESSOR CELL; PATHOLOGY; SKIN TUMOR; TREATMENT OUTCOME;

AGED; ANTINEOPLASTIC AGENTS, IMMUNOLOGICAL; BIOMARKERS, TUMOR; ERYTHROCYTE COUNT; FEMALE; HUMANS; IPILIMUMAB; L-LACTATE DEHYDROGENASE; LYMPHOCYTE COUNT; MALE; MELANOMA; MYELOID-DERIVED SUPPRESSOR CELLS; SKIN NEOPLASMS; T-LYMPHOCYTES, REGULATORY; TREATMENT OUTCOME;

EID: 84970047228     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-15-2412     Document Type: Article

References (50)

1. Robert C, Thomas L, Bondarenko I, O'Day S, M DJ, Garbe C, et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 2011;364:2517-26.
2. 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;363:711-23.
3. Schadendorf D, Hodi FS, Robert C, Weber JS, Margolin K, Hamid O, et al. Pooled analysis of long-term survival data from phase II and phase III trials of ipilimumab in unresectable or metastatic melanoma. J Clin Oncol 2015Feb 9; doi: 10.1200/JCO.2014.56.2736.
4. Robert C, Karaszewska B, Schachter J, Rutkowski P, Mackiewicz A, Stroiakovski D, et al. Improved overall survival in melanoma with combined dabrafenib and trametinib. N Engl J Med 2015;372:30-9.
5. Robert C, Ribas A, Wolchok JD, Hodi FS, Hamid O, Kefford R, et al. Antiprogrammed-death-receptor-1 treatment with pembrolizumab in ipilimumab-refractory advanced melanoma: a randomised dose-comparison cohort of a phase 1 trial. Lancet 2014;384:1109-17.
6. Ascierto PA, Kalos M, Schaer DA, Callahan MK, Wolchok JD. Biomarkers for immunostimulatory monoclonal antibodies in combination strategies for melanoma and other tumor types. Clin Cancer Res 2013;19:1009-20.
7. Attia P, Phan GQ, Maker AV, Robinson MR, Quezado MM, Yang JC, et al. Autoimmunity correlates with tumor regression in patients with metastatic melanoma treated with anti-cytotoxic T-lymphocyte antigen-4. J Clin Oncol 2005;23:6043-53.
8. Downey SG, Klapper JA, Smith FO, Yang JC, Sherry RM, Royal RE, et al. Prognostic factors related to clinical response in patients with metastatic melanoma treated by CTL-associated antigen-4 blockade. Clin Cancer Res 2007;13:6681-8.
9. Simeone E, Gentilcore G, Giannarelli D, Grimaldi AM, Caraco C, Curvietto M, et al. Immunological and biological changes during ipilimumab treatment and their potential correlation with clinical response and survival in patients with advanced melanoma. Cancer Immunol Immunother 2014; 63:675-83.
10. Kitano S, Postow MA, Ziegler CG, Kuk D, Panageas KS, Cortez C, et al. Computational algorithm-driven evaluation of monocytic myeloid-derived suppressor cell frequency for prediction of clinical outcomes. Cancer Immunol Res 2014;2:812-21.
11. Kelderman S, Heemskerk B, van Tinteren H, van den Brom RR, Hospers GA, van den Eertwegh AJ, et al. Lactate dehydrogenase as a selection criterion for ipilimumab treatment in metastatic melanoma. Cancer Immunol Immunother 2014;63:449-58.
12. Delyon J, Mateus C, Lefeuvre D, Lanoy E, Zitvogel L, Chaput N, et al. Experience in daily practice with ipilimumab for the treatment of patients with metastatic melanoma: an early increase in lymphocyte and eosinophil counts is associated with improved survival. Ann Oncol 2013;24:1697-703.
13. Di Giacomo AM, Danielli R, Calabro L, Bertocci E, Nannicini C, Giannarelli D, et al. Ipilimumab experience in heavily pretreated patients with melanoma in an expanded access program at the University Hospital of Siena (Italy). Cancer Immunol Immunother 2011;60:467-77.
14. Hannani D, Vetizou M, Enot D, Rusakiewicz S, Chaput N, Klatzmann D, et al. Anticancer immunotherapy by CTLA-4 blockade: obligatory contribution of IL-2 receptors and negative prognostic impact of soluble CD25. Cell Res 2015;25:208-24.
15. Braumuller H, Wieder T, Brenner E, Assmann S, Hahn M, Alkhaled M, et al. T-helper-1-cell cytokines drive cancer into senescence. Nature 2013; 494:361-5.
16. Kvistborg P, Shu CJ, Heemskerk B, Fankhauser M, Thrue CA, Toebes M, et al. TIL therapy broadens the tumor-reactive CD8(+) T cell compartment in melanoma patients. Oncoimmunology 2012;1:409-18.
17. + T-cell responses correlate with clinical benefit in advanced melanoma patients treated with ipilimumab. Proc Natl Acad Sci U S A 2011;108:16723-8.
18. Weide B, Zelba H, Derhovanessian E, Pflugfelder A, Eigentler TK, Di Giacomo AM, et al. Functional T cells targeting NY-ESO-1 or Melan-A are predictive for survival of patients with distant melanoma metastasis. J Clin Oncol 2012;30:1835-41.
19. Snyder A, Makarov V, Merghoub T, Yuan J, Zaretsky JM, Desrichard A, et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N Engl J Med 2014;371:2189-99.
20. van Rooij N, van Buuren MM, Philips D, Velds A, Toebes M, Heemskerk B, et al. Tumor exome analysis reveals neoantigen-specific T-cell reactivity in an ipilimumab-responsive melanoma. J Clin Oncol 2013;31:e439-42.
21. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012;366:2443-54.
22. Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012;366:2455-65.
23. Wilgenhof S, Du Four S, Vandenbroucke F, Everaert H, Salmon I, Lienard D, et al. Single-center experience with ipilimumab in an expanded access program for patients with pretreated advanced melanoma. J Immunother 2013;36:215-22.
24. Ku GY, Yuan J, Page DB, Schroeder SE, Panageas KS, Carvajal RD, et al. Single-institution experience with ipilimumab in advanced melanoma patients in the compassionate use setting: lymphocyte count after 2 doses correlates with survival. Cancer 2010;116:1767-75.
25. Valpione S, Martinoli C, Fava P, Mocellin S, Campana LG, Quaglino P, et al. Personalised medicine: Development and external validation of a prognostic model for metastatic melanoma patients treated with ipilimumab. Eur J Cancer 2015;51:2086-94.
26. Ferrucci PF, Gandini S, Battaglia A, Alfieri S, Di Giacomo AM, Giannarelli D, et al. Baseline neutrophil-to-lymphocyte ratio is associated with outcome of ipilimumab-treated metastatic melanoma patients. Br J Cancer 2015;112:1904-10.
27. Wang W, Yu D, Sarnaik AA, Yu B, Hall M, Morelli D, et al. Biomarkers on melanoma patient T cells associated with ipilimumab treatment. J Transl Med 2012;10:146.
28. Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 2012;12:253-68.
29. Weide B, Martens A, Zelba H, Stutz C, Derhovanessian E, Di Giacomo AM, et al. Myeloid-derived suppressor cells predict survival of patients with advanced melanoma: comparison with regulatory T cells and NY-ESO-1- or melan-A-specific T cells. Clin Cancer Res 2014;20:1601-9.
30. Meyer C, Cagnon L, Costa-Nunes CM, Baumgaertner P, Montandon N, Leyvraz L, et al. Frequencies of circulating MDSC correlate with clinical outcome of melanoma patients treated with ipilimumab. Cancer Immunol Immunother 2014;63:247-57.
31. Gebhardt C, Sevko A, Jiang H, Lichtenberger R, Reith M, Tarnanidis K, et al. Myeloid cells and related chronic inflammatory factors as novel predictive markers in melanoma treatment with ipilimumab. Clin Cancer Res 2015;21:5453-9.
32. Balch CM, Gershenwald JE, Soong SJ, Thompson JF, Atkins MB, Byrd DR, et al. Final version of 2009 AJCC melanoma staging and classification. J Clin Oncol 2009;27:6199-206.
33. Camp RL, Dolled-Filhart M, Rimm DL. X-tile: a new bio-informatics tool for biomarker assessment and outcome-based cut-point optimization. Clin Cancer Res 2004;10:7252-9.
34. 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. Clin Cancer Res 2009;15: 7412-20.
35. Harrell FE Jr, Lee KL, Mark DB. Multivariable prognostic models: issues in developing models, evaluating assumptions and adequacy, and measuring and reducing errors. Stat Med 1996;15:361-87.
36. Schindler K, Harmankaya K, Postow MA, Frantal S, Bello D, Ariyan CE, et al. Pretreatment levels of absolute and relative eosinophil count to improve overall survival (OS) in patients with metastatic melanoma under treatment with ipilimumab, an anti CTLA-4 antibody. ASCO Meeting Abstracts 2013;31:9024.
37. Schmidt H, Bastholt L, Geertsen P, Christensen IJ, Larsen S, Gehl J, et al. Elevated neutrophil and monocyte counts in peripheral blood are associated with poor survival in patients with metastatic melanoma: a prognostic model. Br J Cancer 2005;93:273-8.
38. Rochet NM, Kottschade LA, Grotz TE, Porrata LF, Markovic SN. The prognostic role of the preoperative absolute lymphocyte count and absolute monocyte count in patients with resected advanced melanoma. Am J Clin Oncol 2015;38:252-8.
39. + cells acquire a myeloid-derived suppressor cell phenotype through COX-2-dependent mechanisms. Cancer Res 2013;73:3877-87.
40. Veltman JD, Lambers ME, van Nimwegen M, Hendriks RW, Hoogsteden HC, Aerts JG, et al. COX-2 inhibition improves immunotherapy and is associated with decreased numbers of myeloid-derived suppressor cells in mesothelioma. Celecoxib influences MDSC function. BMC Cancer 2010; 10:464:464.
41. Serafini P, Meckel K, Kelso M, Noonan K, Califano J, Koch W, et al. Phosphodiesterase-5 inhibition augments endogenous antitumor immunity by reducing myeloid-derived suppressor cell function. J Exp Med 2006;203:2691-702.
42. Tarhini AA, Edington H, Butterfield LH, Lin Y, Shuai Y, Tawbi H, et al. Immune monitoring of the circulation and the tumor microenvironment in patients with regionally advanced melanoma receiving neoadjuvant ipilimumab. PLoS One 2014;9:e87705.
43. Simson L, Ellyard JI, Dent LA, Matthaei KI, Rothenberg ME, Foster PS, et al. Regulation of carcinogenesis by IL-5 and CCL11: a potential role for eosinophils in tumor immune surveillance. J Immunol 2007;178:4222-9.
44. Carretero R, Sektioglu IM, Garbi N, Salgado OC, Beckhove P, Hammerling GJ. Eosinophils orchestrate cancer rejection by normalizing tumor vessels and enhancing infiltration of CD8(+) T cells. Nat Immunol 2015;16:609-17.
45. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009;9:162-74.
46. Diem S, Kasenda B, Martin-Liberal J, Lee A, Chauhan D, Gore M, et al. Prognostic score for patients with advanced melanoma treated with ipilimumab. Eur J Cancer 2015;51:2785-91.
47. Altman DG, McShane LM, Sauerbrei W, Taube SE. Reporting Recommendations for Tumor Marker Prognostic Studies (REMARK): explanation and elaboration. PLoS Med 2012;9:e1001216.
48. Kotsakis A, Harasymczuk M, Schilling B, Georgoulias V, Argiris A, Whiteside TL. Myeloid-derived suppressor cell measurements in fresh and cryopreserved blood samples. J Immunol Methods 2012;381:14-22.
49. Ascierto PA, Simeone E, Sileni VC, Pigozzo J, Maio M, Altomonte M, et al. Clinical experience with ipilimumab 3 mg/kg: real-world efficacy and safety data from an expanded access programme cohort. J Transl Med 2014;12:116.
50. Schindler K, Harmankaya K, Kuk D, Mangana J, Michielin O, Hoeller C, et al. Correlation of absolute and relative eosinophil counts with immunerelated adverse events in melanoma patients treated with ipilimumab. ASCO Meeting Abstracts 2014;32:9096.