Histopathological and immunological spectrum in response evaluation of talimogene laherparepvec treatment and correlation with durable response in patients with cutaneous melanoma.
Journal
Melanoma research
ISSN: 1473-5636
Titre abrégé: Melanoma Res
Pays: England
ID NLM: 9109623
Informations de publication
Date de publication:
01 08 2022
01 08 2022
Historique:
pubmed:
22
4
2022
medline:
6
7
2022
entrez:
21
4
2022
Statut:
ppublish
Résumé
Talimogene laherparepvec (T-VEC) is an intralesional oncolytic virotherapy for patients with irresectable stage III-IVM1a cutaneous melanoma. Although this treatment is considered to mainly act through T cell-mediated mechanisms, prominent numbers of plasma cells after T-VEC treatment have been described. The aim was to investigate how often these plasma cells were present, whether they were relevant in the response to treatment, and if these or other histopathological features were associated with durable response to treatment. Histopathological (granulomas, perineural inflammation, etc.) and immunological features [e.g. B cells/plasma cells (CD20/CD138) and T cells (CD3,CD4,CD8)] were scored and correlated with durable tumor response [i.e. complete response (CR) persisting beyond 6 months after treatment]. Plasmacellular infiltrate was examined with next-generation sequencing and immunohistochemistry (IgG, IgM, IgA, and IgD). Plasma cells were present in all T-VEC injected biopsies from 25 patients with melanoma taken at 3-5 months after starting treatment. In patients with a durable response ( n = 12), angiocentric features and granulomas were more frequently identified compared with patients without a (durable) response ( n = 13); 75% versus 29% for angiocentric features ( P = 0.015) and 58% versus 15% for granulomas ( P = 0.041). There was a class switch of IgM to IgG with skewing to certain dominant Ig heavy chain clonotypes. An angiocentric granulomatous pattern in T-VEC injected melanoma lesions was associated with a durable CR (>6 months). Plasma cells are probably a relevant feature in the mechanism of response but were not associated with durable response.
Identifiants
pubmed: 35446267
doi: 10.1097/CMR.0000000000000824
pii: 00008390-202208000-00005
pmc: PMC9245556
doi:
Substances chimiques
Biological Products
0
Immunoglobulin G
0
Immunoglobulin M
0
talimogene laherparepvec
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
249-259Informations de copyright
Copyright © 2022 The Author(s). Published by Wolters Kluwer Health, Inc.
Références
Andtbacka RHI, Collichio F, Harrington KJ, Middleton MR, Downey G, Ӧhrling K, Kaufman HL. Final analyses of OPTiM: a randomized phase III trial of talimogene laherparepvec versus granulocyte-macrophage colony-stimulating factor in unresectable stage III-IV melanoma. J Immunother Cancer. 2019; 7:145.
Hamid O, Ismail R, Puzanov I. Intratumoral immunotherapy-update 2019. Oncologist. 2020; 25:e423–e438.
Andtbacka RH, Kaufman HL, Collichio F, Amatruda T, Senzer N, Chesney J, et al. Talimogene laherparepvec improves durable response rate in patients with advanced melanoma. J Clin Oncol. 2015; 33:2780–2788.
Franke V, Berger DMS, Klop WMC, van der Hiel B, van de Wiel BA, Ter Meulen S, et al. High response rates for T-VEC in early metastatic melanoma (stage IIIB/C-IVM1a). Int J Cancer. 2019; 145:974–978.
Perez MC, Miura JT, Naqvi SMH, Kim Y, Holstein A, Lee D, et al. Talimogene laherparepvec (TVEC) for the treatment of advanced melanoma: a single-institution experience. Ann Surg Oncol. 2018; 25:3960–3965.
Stahlie EHA, Franke V, Zuur CL, Klop WMC, van der Hiel B, Van de Wiel BA, et al. T-VEC for stage IIIB-IVM1a melanoma achieves high rates of complete and durable responses and is associated with tumor load: a clinical prediction model. Cancer Immunol Immunother. 2021; 70:2291–2300.
Harrington KJ, Andtbacka RH, Collichio F, Downey G, Chen L, Szabo Z, Kaufman HL. Efficacy and safety of talimogene laherparepvec versus granulocyte-macrophage colony-stimulating factor in patients with stage IIIB/C and IVM1a melanoma: subanalysis of the phase III OPTiM trial. Onco Targets Ther. 2016; 9:7081–7093.
Postow MA, Sidlow R, Hellmann MD. Immune-related adverse events associated with immune checkpoint blockade. N Engl J Med. 2018; 378:158–168.
Greco A, Safi D, Swami U, Ginader T, Milhem M, Zakharia Y. Efficacy and adverse events in metastatic melanoma patients treated with combination BRAF Plus MEK inhibitors versus BRAF inhibitors: a systematic review. Cancers (Basel). 2019; 11:E1950.
Conry RM, Westbrook B, McKee S, Norwood TG. Talimogene laherparepvec: first in class oncolytic virotherapy. Hum Vaccin Immunother. 2018; 14:839–846.
Liu BL, Robinson M, Han ZQ, Branston RH, English C, Reay P, et al. ICP34.5 deleted herpes simplex virus with enhanced oncolytic, immune stimulating, and anti-tumour properties. Gene Ther. 2003; 10:292–303.
Hu JC, Coffin RS, Davis CJ, Graham NJ, Groves N, Guest PJ, et al. A phase I study of OncoVEXGM-CSF, a second-generation oncolytic herpes simplex virus expressing granulocyte macrophage colony-stimulating factor. Clin Cancer Res. 2006; 12:6737–6747.
Hughes T, Coffin RS, Lilley CE, Ponce R, Kaufman HL. Critical analysis of an oncolytic herpesvirus encoding granulocyte-macrophage colony stimulating factor for the treatment of malignant melanoma. Oncolytic Virother. 2014; 3:11–20.
Ferrucci PF, Pala L, Conforti F, Cocorocchio E. Talimogene laherparepvec (T-VEC): an intralesional cancer immunotherapy for advanced melanoma. Cancers (Basel). 2021; 13:1383.
Rehman H, Silk AW, Kane MP, Kaufman HL. Into the clinic: talimogene laherparepvec (T-VEC), a first-in-class intratumoral oncolytic viral therapy. J Immunother Cancer. 2016; 4:53.
Kaufman HL, Amatruda T, Reid T, Gonzalez R, Glaspy J, Whitman E, et al. Systemic versus local responses in melanoma patients treated with talimogene laherparepvec from a multi-institutional phase II study. J Immunother Cancer. 2016; 4:12.
Richtig G, Cerroni L, Schmidt H, Beham-Schmid C, Deinlein T, Vallant C, Richtig E. Talimogene laherparepvec can initiate plasma cell invasion into infiltrated melanoma lesions – a case series. J Eur Acad Dermatol Venereol. 2021; 35:e209-e211.
Henning A, Agnese D, Chung CG. Talimogene laherparepvec pseudolymphomatous reaction mimicking metastatic melanoma. J Cutan Pathol. 2021; 48:1423–1426.
Everett AS, Pavlidakey PG, Contreras CM, De Los Santos JF, Kim JY, McKee SB, et al. Chronic granulomatous dermatitis induced by talimogene laherparepvec therapy of melanoma metastases. J Cutan Pathol. 2018; 45:48–53.
Lee K, Pouldar D, Shiu J, Elsensohn A, de Feraudy S. The histological spectrum of talimogene laherparepvec (TVEC) injections-neutrophilic and chronic granulomatous dermatitis. J Cutan Pathol. 2019; 46:165–167.
Helmink BA, Reddy SM, Gao J, Zhang S, Basar R, Thakur R, et al. B cells and tertiary lymphoid structures promote immunotherapy response. Nature. 2020; 577:549–555.
Sautès-Fridman C, Verneau J, Sun CM, Moreira M, Chen TW, Meylan M, et al. Tertiary lymphoid structures and B cells: clinical impact and therapeutic modulation in cancer. Semin Immunol. 2020; 48:101406.
Carlson JA, Chen KR. Cutaneous vasculitis update: neutrophilic muscular vessel and eosinophilic, granulomatous, and lymphocytic vasculitis syndromes. Am J Dermatopathol. 2007; 29:32–43.
Scheijen B, Meijers RWJ, Rijntjes J, van der Klift MY, Möbs M, Steinhilber J, et al.; EuroClonality-NGS Working Group. Next-generation sequencing of immunoglobulin gene rearrangements for clonality assessment: a technical feasibility study by EuroClonality-NGS. Leukemia. 2019; 33:2227–2240.
Bystry V, Reigl T, Krejci A, Demko M, Hanakova B, Grioni A, et al.; EuroClonality-NGS. ARResT/interrogate: an interactive immunoprofiler for IG/TR NGS data. Bioinformatics. 2017; 33:435–437.
Stavnezer J, Schrader CE. IgH chain class switch recombination: mechanism and regulation. J Immunol. 2014; 193:5370–5378.
Weedon D. Skin pathology. 3th ed. Churchill Livingstone Elsevier; 2009.
Jacquelot N, Tellier J, Nutt SL, Belz GT. Tertiary lymphoid structures and B lymphocytes in cancer prognosis and response to immunotherapies. OncoImmunology. 2021; 10:1900508.
Ramelyte E, Tastanova A, Balázs Z, Ignatova D, Turko P, Menzel U, et al. Oncolytic virotherapy-mediated anti-tumor response: a single-cell perspective. Cancer Cell. 2021; 39:394–406.e4.
Shi Y, Liu CH, Roberts AI, Das J, Xu G, Ren G, et al. Granulocyte-macrophage colony-stimulating factor (GM-CSF) and T-cell responses: what we do and don’t know. Cell Res. 2006; 16:126–133.
Tijtgat J, De Munck J, Dufait I, Schwarze JK, Van Riet I, Franceschini L, et al. Unraveling the effects of a talimogene laherparepvec (T-VEC)-induced tumor oncolysate on myeloid dendritic cells. Front Immunol. 2021; 12:733506.
Looker KJ, Magaret AS, May MT, Turner KME, Vickerman P, Gottlieb SL, et al. Global and regional estimates of prevalent and incident herpes simplex virus type 1 infections in 2012. PLoS One. 2015; 10:e0140765.
Dummer R, Gyorki DE, Hyngstrom J, Berger AC, Conry R, Demidov L, et al. Neoadjuvant talimogene laherparepvec plus surgery versus surgery alone for resectable stage IIIB-IVM1a melanoma: a randomized, open-label, phase 2 trial. Nat Med. 2021; 27:1789–1796.
Long G, Dummer R, Johnson D, Michielin O, Martin-Algarra S, Treichel S, et al. 429 Long-term analysis of MASTERKEY-265 phase 1b trial of talimogene laherparepvec (T-VEC) plus pembrolizumab in patients with unresectable stage IIIB-IVM1c melanoma. J Immunother Cancer. 2020; 8 (Suppl 3):A261-A261.
Sun L, Funchain P, Song JM, Rayman P, Tannenbaum C, Ko J, et al. Talimogene laherparepvec combined with anti-PD-1 based immunotherapy for unresectable stage III-IV melanoma: a case series. J Immunother Cancer. 2018; 6:36.
Bai R, Lv Z, Xu D, Cui J. Predictive biomarkers for cancer immunotherapy with immune checkpoint inhibitors. Biomark Res. 2020; 8:34.