Blood based immune biomarkers associated with clinical frailty scale in older patients with melanoma receiving checkpoint inhibitor immunotherapy

Abstract Introduction Immunotherapy with checkpoint inhibition (ICI) is increasingly prescribed to older patients with cancer. High age, especially in combination with frailty, has been associated to immune senescence, which is the age-related decline in immune function, thereby possibly hindering I...

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Main Authors: Estelle Tran Van Hoi, Saskia J. Santegoets, Simon P. Mooijaart, Diana Van Heemst, Asli Özkan, Elizabeth M. E. Verdegaal, Marije Slingerland, Ellen Kapiteijn, Sjoerd H. van der Burg, Johanneke E. A. Portielje, Marij J. P. Welters, Nienke A. de Glas
Format: Article
Language:English
Published: BMC 2024-11-01
Series:Immunity & Ageing
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Online Access:https://doi.org/10.1186/s12979-024-00463-y
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author Estelle Tran Van Hoi
Saskia J. Santegoets
Simon P. Mooijaart
Diana Van Heemst
Asli Özkan
Elizabeth M. E. Verdegaal
Marije Slingerland
Ellen Kapiteijn
Sjoerd H. van der Burg
Johanneke E. A. Portielje
Marij J. P. Welters
Nienke A. de Glas
author_facet Estelle Tran Van Hoi
Saskia J. Santegoets
Simon P. Mooijaart
Diana Van Heemst
Asli Özkan
Elizabeth M. E. Verdegaal
Marije Slingerland
Ellen Kapiteijn
Sjoerd H. van der Burg
Johanneke E. A. Portielje
Marij J. P. Welters
Nienke A. de Glas
author_sort Estelle Tran Van Hoi
collection DOAJ
description Abstract Introduction Immunotherapy with checkpoint inhibition (ICI) is increasingly prescribed to older patients with cancer. High age, especially in combination with frailty, has been associated to immune senescence, which is the age-related decline in immune function, thereby possibly hindering ICI effectiveness. This cross-sectional study aimed to assess whether blood cell immune senescence markers are associated with age, frailty and response to anti-PD-1 treatment in older patients with metastatic melanoma. Methods In a prospective observational study, sixty patients with stage IIIC or IV melanoma undergoing anti-PD1 treatment were categorized into young (< 65 years; n = 22), old (> 65 years) without frailty (n = 19), and old with frailty (n = 19). In-depth immune cell phenotyping was performed in baseline blood samples (prior to treatment) using multispectral flow cytometry and compared between groups and with immunotherapy treatment response. Antigen-presenting cell capacity was evaluated using mixed lymphocyte reaction and T cell proliferative potential was assessed using PHA proliferation assay. Results No significant differences in treatment response rates were observed across age groups. Older patients, irrespective of frailty, showed lower levels of naïve CD8 + T cells, with the old and frail group also exhibiting reduced tissue-resident effector memory CD8 + T cells and CD8 + mucosal associated invariant T (MAIT) cells. These differences were not associated with treatment outcomes. T cell proliferation and antigen-presenting cell capacities did not differ across groups. Conclusion Several ageing and frailty associated changes were detected among circulating immune cells in blood but were not associated with response to immunotherapy in our study. While these findings suggest that the level of frailty and ageing may not necessarily preclude the efficacy of ICI therapy, further investigation is needed to fully understand the impact of frailty and ageing on immunotherapy.
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spelling doaj-art-6b9b79aef64e4aa1babf70adc5e34c332025-08-20T02:49:16ZengBMCImmunity & Ageing1742-49332024-11-0121111210.1186/s12979-024-00463-yBlood based immune biomarkers associated with clinical frailty scale in older patients with melanoma receiving checkpoint inhibitor immunotherapyEstelle Tran Van Hoi0Saskia J. Santegoets1Simon P. Mooijaart2Diana Van Heemst3Asli Özkan4Elizabeth M. E. Verdegaal5Marije Slingerland6Ellen Kapiteijn7Sjoerd H. van der Burg8Johanneke E. A. Portielje9Marij J. P. Welters10Nienke A. de Glas11Department of Gerontology and Geriatrics, Leiden University Medical CenterDepartment of Medical Oncology, Leiden University Medical CenterDepartment of Gerontology and Geriatrics, Leiden University Medical CenterDepartment of Gerontology and Geriatrics, Leiden University Medical CenterDepartment of Medical Oncology, Leiden University Medical CenterDepartment of Medical Oncology, Leiden University Medical CenterDepartment of Medical Oncology, Leiden University Medical CenterDepartment of Medical Oncology, Leiden University Medical CenterDepartment of Medical Oncology, Leiden University Medical CenterDepartment of Medical Oncology, Leiden University Medical CenterDepartment of Medical Oncology, Leiden University Medical CenterDepartment of Medical Oncology, Leiden University Medical CenterAbstract Introduction Immunotherapy with checkpoint inhibition (ICI) is increasingly prescribed to older patients with cancer. High age, especially in combination with frailty, has been associated to immune senescence, which is the age-related decline in immune function, thereby possibly hindering ICI effectiveness. This cross-sectional study aimed to assess whether blood cell immune senescence markers are associated with age, frailty and response to anti-PD-1 treatment in older patients with metastatic melanoma. Methods In a prospective observational study, sixty patients with stage IIIC or IV melanoma undergoing anti-PD1 treatment were categorized into young (< 65 years; n = 22), old (> 65 years) without frailty (n = 19), and old with frailty (n = 19). In-depth immune cell phenotyping was performed in baseline blood samples (prior to treatment) using multispectral flow cytometry and compared between groups and with immunotherapy treatment response. Antigen-presenting cell capacity was evaluated using mixed lymphocyte reaction and T cell proliferative potential was assessed using PHA proliferation assay. Results No significant differences in treatment response rates were observed across age groups. Older patients, irrespective of frailty, showed lower levels of naïve CD8 + T cells, with the old and frail group also exhibiting reduced tissue-resident effector memory CD8 + T cells and CD8 + mucosal associated invariant T (MAIT) cells. These differences were not associated with treatment outcomes. T cell proliferation and antigen-presenting cell capacities did not differ across groups. Conclusion Several ageing and frailty associated changes were detected among circulating immune cells in blood but were not associated with response to immunotherapy in our study. While these findings suggest that the level of frailty and ageing may not necessarily preclude the efficacy of ICI therapy, further investigation is needed to fully understand the impact of frailty and ageing on immunotherapy.https://doi.org/10.1186/s12979-024-00463-yMelanoma cancerImmunotherapy by checkpoint inhibitionFrailtyImmune biomarkers
spellingShingle Estelle Tran Van Hoi
Saskia J. Santegoets
Simon P. Mooijaart
Diana Van Heemst
Asli Özkan
Elizabeth M. E. Verdegaal
Marije Slingerland
Ellen Kapiteijn
Sjoerd H. van der Burg
Johanneke E. A. Portielje
Marij J. P. Welters
Nienke A. de Glas
Blood based immune biomarkers associated with clinical frailty scale in older patients with melanoma receiving checkpoint inhibitor immunotherapy
Immunity & Ageing
Melanoma cancer
Immunotherapy by checkpoint inhibition
Frailty
Immune biomarkers
title Blood based immune biomarkers associated with clinical frailty scale in older patients with melanoma receiving checkpoint inhibitor immunotherapy
title_full Blood based immune biomarkers associated with clinical frailty scale in older patients with melanoma receiving checkpoint inhibitor immunotherapy
title_fullStr Blood based immune biomarkers associated with clinical frailty scale in older patients with melanoma receiving checkpoint inhibitor immunotherapy
title_full_unstemmed Blood based immune biomarkers associated with clinical frailty scale in older patients with melanoma receiving checkpoint inhibitor immunotherapy
title_short Blood based immune biomarkers associated with clinical frailty scale in older patients with melanoma receiving checkpoint inhibitor immunotherapy
title_sort blood based immune biomarkers associated with clinical frailty scale in older patients with melanoma receiving checkpoint inhibitor immunotherapy
topic Melanoma cancer
Immunotherapy by checkpoint inhibition
Frailty
Immune biomarkers
url https://doi.org/10.1186/s12979-024-00463-y
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