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Integrative histopathological and immunophenotypical characterisation of the inflammatory microenvironment in spitzoid melanocytic neoplasms

AIMS: The role of inflammation in conventional cutaneous melanoma has been extensively studied, whereas only little is known about the inflammatory microenvironment and immunogenic properties of spitzoid melanocytic neoplasms. The composition of infiltrating immune cells and the architectural distri...

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Autores principales: Hillen, Lisa M, Vandyck, Hendrik L D, Leunissen, Daphne J G, de Greef, Bianca T A, Bosisio, Francesca M, zur Hausen, Axel, van den Oord, Joost, Winnepenninckx, Véronique
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7894529/
https://www.ncbi.nlm.nih.gov/pubmed/32970867
http://dx.doi.org/10.1111/his.14259
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author Hillen, Lisa M
Vandyck, Hendrik L D
Leunissen, Daphne J G
de Greef, Bianca T A
Bosisio, Francesca M
zur Hausen, Axel
van den Oord, Joost
Winnepenninckx, Véronique
author_facet Hillen, Lisa M
Vandyck, Hendrik L D
Leunissen, Daphne J G
de Greef, Bianca T A
Bosisio, Francesca M
zur Hausen, Axel
van den Oord, Joost
Winnepenninckx, Véronique
author_sort Hillen, Lisa M
collection PubMed
description AIMS: The role of inflammation in conventional cutaneous melanoma has been extensively studied, whereas only little is known about the inflammatory microenvironment and immunogenic properties of spitzoid melanocytic neoplasms. The composition of infiltrating immune cells and the architectural distribution of the inflammation, in particular, are still obscure. This is the first study, to our knowledge, to systematically characterise the inflammatory patterns and the leucocyte subsets in spitzoid melanocytic lesions. METHODS AND RESULTS: We examined 79 spitzoid neoplasms including banal Spitz naevi (SN, n = 50), atypical Spitz tumours (AST, n = 17) and malignant Spitz tumours (MST, n = 12) using histopathological analysis and immunohistochemistry. Spitzoid melanocytic lesions showed a high frequency (67.1%, n = 53 of 79) of inflammation. Four inflammatory patterns were identified according to architectural composition, distribution and intensity of inflammation. The majority of the inflammatory infiltrate corresponded to CD3(+)/CD8(+) T lymphocytes (56.1%), followed by CD3(+)/CD4(+) T cells (35.7%) and CD68(+) histiocytes (20.3%). CD3(+)/TIA‐1(+) cytotoxic T lymphocytes constituted 3.7% of inflammatory cells. Rarely, CD3(+)/ granzyme B(+) cytotoxic T lymphocytes (2.7%) and CD138(+) plasma cells (0.5%) were detected in the infiltrating immune cells. There was no significant difference in the inflammatory cellular composition among the spitzoid melanocytic subgroups (SN versus AST versus MST). CONCLUSION: Our findings demonstrate that Spitz tumours are highly immunogenic lesions. Inflammation with the presence of lymphocytic aggregates predominated in SN, but was not distinctive for this melanocytic category. A strong and intense inflammation was suggestive of an underlying malignancy. The infiltrating cytotoxic T lymphocyte subsets in Spitz tumours deserve further investigation in larger study cohorts to elucidate prognostic and immuno‐oncological therapeutic relevance.
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spelling pubmed-78945292021-03-02 Integrative histopathological and immunophenotypical characterisation of the inflammatory microenvironment in spitzoid melanocytic neoplasms Hillen, Lisa M Vandyck, Hendrik L D Leunissen, Daphne J G de Greef, Bianca T A Bosisio, Francesca M zur Hausen, Axel van den Oord, Joost Winnepenninckx, Véronique Histopathology Original Articles AIMS: The role of inflammation in conventional cutaneous melanoma has been extensively studied, whereas only little is known about the inflammatory microenvironment and immunogenic properties of spitzoid melanocytic neoplasms. The composition of infiltrating immune cells and the architectural distribution of the inflammation, in particular, are still obscure. This is the first study, to our knowledge, to systematically characterise the inflammatory patterns and the leucocyte subsets in spitzoid melanocytic lesions. METHODS AND RESULTS: We examined 79 spitzoid neoplasms including banal Spitz naevi (SN, n = 50), atypical Spitz tumours (AST, n = 17) and malignant Spitz tumours (MST, n = 12) using histopathological analysis and immunohistochemistry. Spitzoid melanocytic lesions showed a high frequency (67.1%, n = 53 of 79) of inflammation. Four inflammatory patterns were identified according to architectural composition, distribution and intensity of inflammation. The majority of the inflammatory infiltrate corresponded to CD3(+)/CD8(+) T lymphocytes (56.1%), followed by CD3(+)/CD4(+) T cells (35.7%) and CD68(+) histiocytes (20.3%). CD3(+)/TIA‐1(+) cytotoxic T lymphocytes constituted 3.7% of inflammatory cells. Rarely, CD3(+)/ granzyme B(+) cytotoxic T lymphocytes (2.7%) and CD138(+) plasma cells (0.5%) were detected in the infiltrating immune cells. There was no significant difference in the inflammatory cellular composition among the spitzoid melanocytic subgroups (SN versus AST versus MST). CONCLUSION: Our findings demonstrate that Spitz tumours are highly immunogenic lesions. Inflammation with the presence of lymphocytic aggregates predominated in SN, but was not distinctive for this melanocytic category. A strong and intense inflammation was suggestive of an underlying malignancy. The infiltrating cytotoxic T lymphocyte subsets in Spitz tumours deserve further investigation in larger study cohorts to elucidate prognostic and immuno‐oncological therapeutic relevance. John Wiley and Sons Inc. 2020-11-19 2021-03 /pmc/articles/PMC7894529/ /pubmed/32970867 http://dx.doi.org/10.1111/his.14259 Text en © 2020 The Authors. Histopathology published by John Wiley & Sons Ltd This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Articles
Hillen, Lisa M
Vandyck, Hendrik L D
Leunissen, Daphne J G
de Greef, Bianca T A
Bosisio, Francesca M
zur Hausen, Axel
van den Oord, Joost
Winnepenninckx, Véronique
Integrative histopathological and immunophenotypical characterisation of the inflammatory microenvironment in spitzoid melanocytic neoplasms
title Integrative histopathological and immunophenotypical characterisation of the inflammatory microenvironment in spitzoid melanocytic neoplasms
title_full Integrative histopathological and immunophenotypical characterisation of the inflammatory microenvironment in spitzoid melanocytic neoplasms
title_fullStr Integrative histopathological and immunophenotypical characterisation of the inflammatory microenvironment in spitzoid melanocytic neoplasms
title_full_unstemmed Integrative histopathological and immunophenotypical characterisation of the inflammatory microenvironment in spitzoid melanocytic neoplasms
title_short Integrative histopathological and immunophenotypical characterisation of the inflammatory microenvironment in spitzoid melanocytic neoplasms
title_sort integrative histopathological and immunophenotypical characterisation of the inflammatory microenvironment in spitzoid melanocytic neoplasms
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7894529/
https://www.ncbi.nlm.nih.gov/pubmed/32970867
http://dx.doi.org/10.1111/his.14259
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