Moderate-to-severe eosinophilia induced by treatment with immune checkpoint inhibitors: 37 cases from a national reference center for hypereosinophilic syndromes and the French pharmacovigilance database

References

• Mellman I, Coukos G, Dranoff G. Cancer immunotherapy comes of age. Nature. 2011;480(7378):480–9. doi:10.1038/nature10673.
   PubMed Web of Science ®Google Scholar
• Champiat S, Lambotte O, Barreau E, Belkhir R, Berdelou A, Carbonnel F, Cauquil C, Chanson P, Collins M, Durrbach A, et al. Management of immune checkpoint blockade dysimmune toxicities: a collaborative position paper. Ann Oncol. 2016;27(4):559–574. doi:10.1093/annonc/mdv623.
   PubMed Web of Science ®Google Scholar
• Michot JM, Bigenwald C, Champiat S, Collins M, Carbonnel F, Postel-Vinay S, Berdelou A, Varga A, Bahleda R, Hollebecque A, et al. Immune-related adverse events with immune checkpoint blockade: a comprehensive review. Eur J Cancer. 2016;54:139–148. doi:10.1016/j.ejca.2015.11.016.
   PubMed Web of Science ®Google Scholar
• Reck M, Rodríguez-Abreu D, Robinson AG, Hui R, Csőszi T, Fülöp A, Gottfried M, Peled N, Tafreshi A, Cuffe S, et al. Pembrolizumab versus chemotherapy for PD-L1–positive non–small-cell lung cancer. 2016 Oct 8. [accessed 2019 Feb 22]. https://www.nejm.org/doi/10.1056/NEJMoa1606774?url_ver=Z39.88-2003&rfr_id=ori%3Arid%3Acrossref.org&rfr_dat=cr_pub%3Dwww.ncbi.nlm.nih.gov.
   Google Scholar
• Brahmer JR, Lacchetti C, Schneider BJ, Atkins MB, Brassil KJ, Caterino JM, Chau I, Ernstoff MS, Gardner JM, Ginex P, et al. Management of immune-related adverse events in patients treated with immune checkpoint inhibitor therapy: American society of clinical oncology clinical practice guideline. J Clin Oncol. 2018;36(17):1714–1768. doi:10.1200/JCO.2017.77.6385.
   PubMed Web of Science ®Google Scholar
• Bernard-Tessier A, Jeanville P, Champiat S, Lazarovici J, Voisin A-L, Mateus C, Lambotte O, Annereau M, Michot J-M. Immune-related eosinophilia induced by anti-programmed death 1 or death-ligand 1 antibodies. Eur J Cancer. 2017;81:135–137. doi:10.1016/j.ejca.2017.05.017.
   PubMed Web of Science ®Google Scholar
• Postow MA, Sidlow R, Hellmann MD. Immune-related adverse events associated with immune checkpoint blockade. N Engl J Med. 2018;378(2):158–168. doi:10.1056/NEJMra1703481.
   PubMed Web of Science ®Google Scholar
• Delyon J, Mateus C, Lefeuvre D, Lanoy E, Zitvogel L, Chaput N, Roy S, Eggermont AMM, Routier E, Robert C. 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(6):1697–1703. doi:10.1093/annonc/mdt027.
   PubMed Web of Science ®Google Scholar
• Schindler K, Harmankaya K, Postow MA, Frantal S, Bello D, Ariyan CE, Michielin OA, Hoeller C, Pehamberger H, Wolchok JD. 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. J Clin Oncol. 2013;31(15_suppl):9024. doi:10.1200/jco.2013.31.15_suppl.9024.
   Web of Science ®Google Scholar
• Martens A, Wistuba-Hamprecht K, Foppen MG, Yuan J, Postow MA, Wong P, Romano E, Khammari A, Dreno B, Capone M, et al. Baseline peripheral blood biomarkers associated with clinical outcome of advanced melanoma patients treated with ipilimumab. Clin Cancer Res. 2016;22(12):2908–2918. doi:10.1158/1078-0432.CCR-15-2412.
   PubMed Web of Science ®Google Scholar
• Weide B, Martens A, Hassel JC, Berking C, Postow MA, Bisschop K, Simeone E, Mangana J, Schilling B, Giacomo AMD, et al. Baseline biomarkers for outcome of melanoma patients treated with pembrolizumab. Clin Cancer Res. 2016;22(22):5487–5496. doi:10.1158/1078-0432.CCR-16-0127.
   PubMed Web of Science ®Google Scholar
• Hude I, Sasse S, Bröckelmann PJ, Tresckow BV, Momotow J, Engert A, Borchmann S. Leucocyte and eosinophil counts predict progression-free survival in relapsed or refractory classical Hodgkin lymphoma patients treated with PD1 inhibition. Br J Haematol. 2018;181(6):837–840. doi:10.1111/bjh.14705.
   PubMed Web of Science ®Google Scholar
• Gaba L, Victoria I, Pineda E, Fernandez A, Aya F, Prat A, Arance AM. Changes in blood eosinophilia during anti-PD1 therapy as a predictor of long term disease control in metastatic melanoma. J Clin Oncol. 2015;33(15_suppl):9069. doi:10.1200/jco.2015.33.15_suppl.9069.
   Web of Science ®Google Scholar
• Gebhardt C, Sevko A, Jiang H, Lichtenberger R, Reith M, Tarnanidis K, Holland-Letz T, Umansky L, Beckhove P, Sucker A, et al. Myeloid cells and related chronic inflammatory factors as novel predictive markers in melanoma treatment with ipilimumab. Clin Cancer Res. 2015;21(24):5453–5459. doi:10.1158/1078-0432.CCR-15-0676.
   PubMed Web of Science ®Google Scholar
• Umansky V, Utikal J, Gebhardt C. Predictive immune markers in advanced melanoma patients treated with ipilimumab. Oncoimmunology. 2016;5:6. doi:10.1080/2162402X.2016.1158901.
   Web of Science ®Google Scholar
• Moreira A. Eosinophilic count as a biomarker for prognosis of melanoma patients and its importance in the response to immunotherapy. Immunotherapy. 2017;9(2):115–121. doi:10.2217/imt-2016-0138.
   PubMed Web of Science ®Google Scholar
• Simon SCS, Utikal J, Umansky V. Opposing roles of eosinophils in cancer. Cancer Immunol Immunother. 2018 Oct 9. doi:10.1007/s00262-018-2255-4.
   Web of Science ®Google Scholar
• Carretero R, Sektioglu IM, Garbi N, Salgado OC, Beckhove P, Hämmerling GJ. Eosinophils orchestrate cancer rejection by normalizing tumor vessels and enhancing infiltration of CD8+ T cells. Nat Immunol. 2015;16(6):609–617. doi:10.1038/ni.3159.
   PubMed Web of Science ®Google Scholar
• Reichman H, Karo-Atar D, Munitz A. Emerging roles for eosinophils in the tumor microenvironment. Trends Cancer. 2016;2(11):664–675. doi:10.1016/j.trecan.2016.10.002.
   PubMed Web of Science ®Google Scholar
• Gatault S, Legrand F, Delbeke M, Loiseau S, Capron M. Involvement of eosinophils in the anti-tumor response. Cancer Immunol Immunother. 2012;61(9):1527–1534. doi:10.1007/s00262-012-1288-3.
   PubMed Web of Science ®Google Scholar
• Kahn JE, Groh M, Lefèvre G. (A critical appraisal of) Classification of hypereosinophilic disorders. Front Med. 2017:4. doi:10.3389/fmed.2017.00216.
   Web of Science ®Google Scholar
• Terminology Criteria for Adverse Events (CTCAE). Version 5.0. U.S. Department of Health and Human Services. National Institutes of Health. National Cancer Institute. Novembre 27, 2017.
   Google Scholar
• Belum VR, Benhuri B, Postow MA, Hellmann MD, Lesokhin AM, Segal NH, Motzer RJ, Wu S, Busam KJ, Wolchok JD, et al. Characterisation and management of dermatologic adverse events to agents targeting the PD-1 receptor. Eur J Cancer. 2016;60:12–25. doi:10.1016/j.ejca.2016.02.010.
   PubMed Web of Science ®Google Scholar
• Phillips GS, Wu J, Hellmann MD, Postow MA, Rizvi NA, Freites-Martinez A, Chan D, Dusza S, Motzer RJ, Rosenberg JE, et al. Treatment outcomes of immune-related cutaneous adverse events. J Clin Oncol. 2019 Jun 19:JCO.18.02141. doi:10.1200/JCO.18.02141.
   Google Scholar
• Mirza S, Hill E, Ludlow S, Nanjappa S. Checkpoint inhibitor-associated drug reaction with eosinophilia and systemic symptom syndrome. Melanoma Res. 2017;27(3):271–273. doi:10.1097/CMR.0000000000000326.
   PubMed Web of Science ®Google Scholar
• Lu J, Thuraisingam T, Chergui M, Nguyen K. Nivolumab-associated DRESS syndrome: A case report. JAAD Case Rep. 2019;5(3):216–218. doi:10.1016/j.jdcr.2018.11.017.
   PubMedGoogle Scholar
• Toussaint F, Hammon M, Erdmann M, Moreira A, Kirchberger MC, Schuler G, Schett G, Heinzerling L. Checkpoint inhibitor-induced eosinophilic fasciitis following high eosinophilia associated with complete response. Rheumatology. 2019;58(10):1875–1877. doi:10.1093/rheumatology/kez164.
   Web of Science ®Google Scholar
• Khoja L, Maurice C, Chappell M, MacMillan L, Al-Habeeb AS, Al-Faraidy N, Butler MO, Rogalla P, Mason W, Joshua AM, et al. Eosinophilic fasciitis and acute encephalopathy toxicity from pembrolizumab treatment of a patient with metastatic melanoma. Cancer Immunol Res. 2016;4(3):175–178. doi:10.1158/2326-6066.CIR-15-0186.
   PubMed Web of Science ®Google Scholar
• Lidar M, Giat E, Garelick D, Horowitz Y, Amital H, Steinberg-Silman Y, Schachter J, Shapira-Frommer R, Markel G. Rheumatic manifestations among cancer patients treated with immune checkpoint inhibitors. Autoimmun Rev. 2018;17(3):284–289. doi:10.1016/j.autrev.2018.01.003.
   PubMed Web of Science ®Google Scholar
• Andrés‐Lencina -J-J, Burillo‐Martínez S, Aragón‐Miguel R, Calleja‐Algarra A, Rodríguez‐Peralto J-L, Ortiz‐Romero P-L, Gargallo‐Moneva V. Eosinophilic fasciitis and lichen sclerosus in a patient treated with nivolumab. Australas J Dermatol. 2018;59(4):e302–e304. doi:10.1111/ajd.12836.
   PubMed Web of Science ®Google Scholar
• Roger A, Groh M, Lorillon G, Pendu CL, Maillet J, Arangalage D, Tazi A, Lebbe C, Baroudjian B, Delyon J. Eosinophilic granulomatosis with polyangiitis (Churg-Strauss) induced by immune checkpoint inhibitors. Ann Rheum Dis. 2019;78(8):e82–e82. doi:10.1136/annrheumdis-2018-213857.
   PubMed Web of Science ®Google Scholar
• Haanen JBAG, Carbonnel F, Robert C, Kerr KM, Peters S, Larkin J, Jordan K. Management of toxicities from immunotherapy: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2017;28(suppl_4):iv119–iv142. doi:10.1093/annonc/mdx225.
   PubMed Web of Science ®Google Scholar
• Puzanov I, Diab A, Abdallah K, Bingham CO, Brogdon C, Dadu R, Hamad L, Kim S, Lacouture ME, LeBoeuf NR, et al. Managing toxicities associated with immune checkpoint inhibitors: consensus recommendations from the Society for Immunotherapy of Cancer (SITC) toxicity management working group. J Immunother Cancer. 2017;5. doi:10.1186/s40425-017-0300-z.
   Web of Science ®Google Scholar
• Maxwell R, Luksik AS, Garzon-Muvdi T, Hung AL, Kim ES, Wu A, Xia Y, Belcaid Z, Gorelick N, Choi J, et al. Contrasting impact of corticosteroids on anti-PD-1 immunotherapy efficacy for tumor histologies located within or outside the central nervous system. Oncoimmunology. 2018;7:12. doi:10.1080/2162402X.2018.1500108.
   Web of Science ®Google Scholar
• Fucà G, Galli G, Poggi M, Lo Russo G, Proto C, Imbimbo M, Ferrara R, Zilembo N, Ganzinelli M, Sica A, et al. Modulation of peripheral blood immune cells by early use of steroids and its association with clinical outcomes in patients with metastatic non-small cell lung cancer treated with immune checkpoint inhibitors. ESMO Open. 2019;4:1. doi:10.1136/esmoopen-2018-000457.
   Web of Science ®Google Scholar
• Vial T. French pharmacovigilance: missions, organization and perspectives. Therapie. 2016;71(2):143–150. doi:10.1016/j.therap.2016.02.029.
   PubMed Web of Science ®Google Scholar
• Théophile H, Dutertre J-P, Gérardin M, Valnet-Rabier M-B, Bidault I, Guy C, Haramburu F, Hillaire-Buys D, Méglio C, Arimone Y. Validation and reproducibility of the updated french causality assessment method: an evaluation by pharmacovigilance centres & pharmaceutical companies. Thérapie. 2015;70(5):465–476. doi:10.2515/therapie/2015028.
   PubMed Web of Science ®Google Scholar
• Brown EG, Wood L, Wood S. The medical dictionary for regulatory activities (MedDRA). Drug Saf. 1999;20(2):109–117. doi:10.2165/00002018-199920020-00002.
   PubMed Web of Science ®Google Scholar
• Simon H-U, Rothenberg ME, Bochner BS, Weller PF, Wardlaw AJ, Wechsler ME, Rosenwasser LJ, Roufosse F, Gleich GJ, Klion AD. Refining the definition of hypereosinophilic syndrome. J Allergy Clin Immunol. 2010;126(1):45–49. doi:10.1016/j.jaci.2010.03.042.
   PubMed Web of Science ®Google Scholar