Serum analytes as predictors of disease recurrence and the duration of invasive disease-free survival in patients with triple negative breast cancer enrolled in the OXEL trial treated with immunotherapy, chemotherapy, or chemoimmunotherapy

Background The OXEL study (NCT03487666) was a phase II trial of patients with triple negative breast cancer (TNBC) with residual disease following neoadjuvant chemotherapy, randomized to receive immunotherapy (anti-programmed cell death protein 1, nivolumab), chemotherapy (capecitabine), or chemoimm...

Full description

Saved in:
Bibliographic Details
Main Authors: Renee N Donahue, Jeffrey Schlom, Nicole J Toney, Claudine Isaacs, Filipa Lynce, Candace Mainor, Megan T Lynch
Format: Article
Language:English
Published: BMJ Publishing Group 2025-04-01
Series:Journal for ImmunoTherapy of Cancer
Online Access:https://jitc.bmj.com/content/13/4/e011379.full
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850206317279444992
author Renee N Donahue
Jeffrey Schlom
Nicole J Toney
Claudine Isaacs
Filipa Lynce
Candace Mainor
Megan T Lynch
author_facet Renee N Donahue
Jeffrey Schlom
Nicole J Toney
Claudine Isaacs
Filipa Lynce
Candace Mainor
Megan T Lynch
author_sort Renee N Donahue
collection DOAJ
description Background The OXEL study (NCT03487666) was a phase II trial of patients with triple negative breast cancer (TNBC) with residual disease following neoadjuvant chemotherapy, randomized to receive immunotherapy (anti-programmed cell death protein 1, nivolumab), chemotherapy (capecitabine), or chemoimmunotherapy. We previously reported on the primary endpoint of the OXEL trial, demonstrating that a peripheral immunoscore based on circulating immune cells reflecting immune activation was increased in patients treated with immunotherapy. However, compared with cell-based immune assays, sera assays are more cost-effective, less labor-intensive, and samples easier to obtain. Here, we report on differences in serum analytes between treatment arms and associations with clinical response.Methods Patients (n=38) were assayed for 97 serum analytes before and after 6 and 12 weeks of therapy. Serum analytes were assessed for changes with therapy, and as predictors of disease recurrence and the duration of invasive disease-free survival (iDFS) in both single analyte analyses and machine learning models.Results Levels of specific analytes at baseline and changes in levels at early time points on treatment preceding recurrence were associated with eventual development of disease recurrence and/or the duration of iDFS. These associations varied based on the therapy patients received. Immunotherapy led to enrichment in pro-inflammatory analytes following treatment, whereas chemotherapy resulted in overall decreases. Changes seen in patients receiving chemoimmunotherapy more closely resembled those observed in patients receiving immunotherapy alone as opposed to chemotherapy alone. Furthermore, logistic regression and Cox proportional hazard models, developed using machine learning methods, demonstrated that combinations of serum analytes were more predictive of disease recurrence and iDFS duration than analyses of single serum analytes. Notably, the multivariable models that predicted patient outcomes were highly specific to the class of treatment patients received.Conclusions In patients with TNBC with residual disease after neoadjuvant chemotherapy, treatment with immunotherapy alone or chemoimmunotherapy resulted in enhanced immune activation compared with chemotherapy alone as measured by changes in serum analyte levels. Distinct serum analytes, both at baseline and as changes after therapy, predicted clinical outcomes for patients receiving immunotherapy alone, chemotherapy alone, or chemoimmunotherapy.Trial registration number NCT03487666.
format Article
id doaj-art-923cc4f6367d4af298fe0a642aa0d20c
institution OA Journals
issn 2051-1426
language English
publishDate 2025-04-01
publisher BMJ Publishing Group
record_format Article
series Journal for ImmunoTherapy of Cancer
spelling doaj-art-923cc4f6367d4af298fe0a642aa0d20c2025-08-20T02:10:53ZengBMJ Publishing GroupJournal for ImmunoTherapy of Cancer2051-14262025-04-0113410.1136/jitc-2024-011379Serum analytes as predictors of disease recurrence and the duration of invasive disease-free survival in patients with triple negative breast cancer enrolled in the OXEL trial treated with immunotherapy, chemotherapy, or chemoimmunotherapyRenee N Donahue0Jeffrey Schlom1Nicole J Toney2Claudine Isaacs3Filipa Lynce4Candace Mainor5Megan T Lynch61Center for Immuno-Oncology, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, MD, USACenter for Immuno-Oncology, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, Maryland, USACenter for Immuno-Oncology, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda, Maryland, USA9Lombardi Cancer Center, Georgetown University Medical Center, Washington, DC, USA4Harvard Medical School, Boston, MA, USA4MedStar Georgetown University Hospital, Washington, DC, USA1National Institutes of Health, Silver Spring, MD, USABackground The OXEL study (NCT03487666) was a phase II trial of patients with triple negative breast cancer (TNBC) with residual disease following neoadjuvant chemotherapy, randomized to receive immunotherapy (anti-programmed cell death protein 1, nivolumab), chemotherapy (capecitabine), or chemoimmunotherapy. We previously reported on the primary endpoint of the OXEL trial, demonstrating that a peripheral immunoscore based on circulating immune cells reflecting immune activation was increased in patients treated with immunotherapy. However, compared with cell-based immune assays, sera assays are more cost-effective, less labor-intensive, and samples easier to obtain. Here, we report on differences in serum analytes between treatment arms and associations with clinical response.Methods Patients (n=38) were assayed for 97 serum analytes before and after 6 and 12 weeks of therapy. Serum analytes were assessed for changes with therapy, and as predictors of disease recurrence and the duration of invasive disease-free survival (iDFS) in both single analyte analyses and machine learning models.Results Levels of specific analytes at baseline and changes in levels at early time points on treatment preceding recurrence were associated with eventual development of disease recurrence and/or the duration of iDFS. These associations varied based on the therapy patients received. Immunotherapy led to enrichment in pro-inflammatory analytes following treatment, whereas chemotherapy resulted in overall decreases. Changes seen in patients receiving chemoimmunotherapy more closely resembled those observed in patients receiving immunotherapy alone as opposed to chemotherapy alone. Furthermore, logistic regression and Cox proportional hazard models, developed using machine learning methods, demonstrated that combinations of serum analytes were more predictive of disease recurrence and iDFS duration than analyses of single serum analytes. Notably, the multivariable models that predicted patient outcomes were highly specific to the class of treatment patients received.Conclusions In patients with TNBC with residual disease after neoadjuvant chemotherapy, treatment with immunotherapy alone or chemoimmunotherapy resulted in enhanced immune activation compared with chemotherapy alone as measured by changes in serum analyte levels. Distinct serum analytes, both at baseline and as changes after therapy, predicted clinical outcomes for patients receiving immunotherapy alone, chemotherapy alone, or chemoimmunotherapy.Trial registration number NCT03487666.https://jitc.bmj.com/content/13/4/e011379.full
spellingShingle Renee N Donahue
Jeffrey Schlom
Nicole J Toney
Claudine Isaacs
Filipa Lynce
Candace Mainor
Megan T Lynch
Serum analytes as predictors of disease recurrence and the duration of invasive disease-free survival in patients with triple negative breast cancer enrolled in the OXEL trial treated with immunotherapy, chemotherapy, or chemoimmunotherapy
Journal for ImmunoTherapy of Cancer
title Serum analytes as predictors of disease recurrence and the duration of invasive disease-free survival in patients with triple negative breast cancer enrolled in the OXEL trial treated with immunotherapy, chemotherapy, or chemoimmunotherapy
title_full Serum analytes as predictors of disease recurrence and the duration of invasive disease-free survival in patients with triple negative breast cancer enrolled in the OXEL trial treated with immunotherapy, chemotherapy, or chemoimmunotherapy
title_fullStr Serum analytes as predictors of disease recurrence and the duration of invasive disease-free survival in patients with triple negative breast cancer enrolled in the OXEL trial treated with immunotherapy, chemotherapy, or chemoimmunotherapy
title_full_unstemmed Serum analytes as predictors of disease recurrence and the duration of invasive disease-free survival in patients with triple negative breast cancer enrolled in the OXEL trial treated with immunotherapy, chemotherapy, or chemoimmunotherapy
title_short Serum analytes as predictors of disease recurrence and the duration of invasive disease-free survival in patients with triple negative breast cancer enrolled in the OXEL trial treated with immunotherapy, chemotherapy, or chemoimmunotherapy
title_sort serum analytes as predictors of disease recurrence and the duration of invasive disease free survival in patients with triple negative breast cancer enrolled in the oxel trial treated with immunotherapy chemotherapy or chemoimmunotherapy
url https://jitc.bmj.com/content/13/4/e011379.full
work_keys_str_mv AT reneendonahue serumanalytesaspredictorsofdiseaserecurrenceandthedurationofinvasivediseasefreesurvivalinpatientswithtriplenegativebreastcancerenrolledintheoxeltrialtreatedwithimmunotherapychemotherapyorchemoimmunotherapy
AT jeffreyschlom serumanalytesaspredictorsofdiseaserecurrenceandthedurationofinvasivediseasefreesurvivalinpatientswithtriplenegativebreastcancerenrolledintheoxeltrialtreatedwithimmunotherapychemotherapyorchemoimmunotherapy
AT nicolejtoney serumanalytesaspredictorsofdiseaserecurrenceandthedurationofinvasivediseasefreesurvivalinpatientswithtriplenegativebreastcancerenrolledintheoxeltrialtreatedwithimmunotherapychemotherapyorchemoimmunotherapy
AT claudineisaacs serumanalytesaspredictorsofdiseaserecurrenceandthedurationofinvasivediseasefreesurvivalinpatientswithtriplenegativebreastcancerenrolledintheoxeltrialtreatedwithimmunotherapychemotherapyorchemoimmunotherapy
AT filipalynce serumanalytesaspredictorsofdiseaserecurrenceandthedurationofinvasivediseasefreesurvivalinpatientswithtriplenegativebreastcancerenrolledintheoxeltrialtreatedwithimmunotherapychemotherapyorchemoimmunotherapy
AT candacemainor serumanalytesaspredictorsofdiseaserecurrenceandthedurationofinvasivediseasefreesurvivalinpatientswithtriplenegativebreastcancerenrolledintheoxeltrialtreatedwithimmunotherapychemotherapyorchemoimmunotherapy
AT megantlynch serumanalytesaspredictorsofdiseaserecurrenceandthedurationofinvasivediseasefreesurvivalinpatientswithtriplenegativebreastcancerenrolledintheoxeltrialtreatedwithimmunotherapychemotherapyorchemoimmunotherapy