Sensitive liquid biopsy monitoring correlates with outcome in the prospective international GPOH-DCOG high-risk neuroblastoma RT-qPCR validation study

Abstract Background Liquid biopsies offer less burdensome sensitive disease monitoring. Bone marrow (BM) metastases, common in various cancers including neuroblastoma, is associated with poor outcomes. In pediatric high-risk neuroblastoma most patients initially respond to treatment, but in the majo...

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Main Authors: Lieke M. J. van Zogchel, Boris Decarolis, Esther M. van Wezel, Lily Zappeij‐Kannegieter, Nina U. Gelineau, Roswitha Schumacher‐Kuckelkorn, Thorsten Simon, Frank Berthold, Max M. van Noesel, Marta Fiocco, C. Ellen van der Schoot, Barbara Hero, Janine Stutterheim, Godelieve A. M. Tytgat
Format: Article
Language:English
Published: BMC 2024-12-01
Series:Journal of Experimental & Clinical Cancer Research
Online Access:https://doi.org/10.1186/s13046-024-03261-y
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author Lieke M. J. van Zogchel
Boris Decarolis
Esther M. van Wezel
Lily Zappeij‐Kannegieter
Nina U. Gelineau
Roswitha Schumacher‐Kuckelkorn
Thorsten Simon
Frank Berthold
Max M. van Noesel
Marta Fiocco
C. Ellen van der Schoot
Barbara Hero
Janine Stutterheim
Godelieve A. M. Tytgat
author_facet Lieke M. J. van Zogchel
Boris Decarolis
Esther M. van Wezel
Lily Zappeij‐Kannegieter
Nina U. Gelineau
Roswitha Schumacher‐Kuckelkorn
Thorsten Simon
Frank Berthold
Max M. van Noesel
Marta Fiocco
C. Ellen van der Schoot
Barbara Hero
Janine Stutterheim
Godelieve A. M. Tytgat
author_sort Lieke M. J. van Zogchel
collection DOAJ
description Abstract Background Liquid biopsies offer less burdensome sensitive disease monitoring. Bone marrow (BM) metastases, common in various cancers including neuroblastoma, is associated with poor outcomes. In pediatric high-risk neuroblastoma most patients initially respond to treatment, but in the majority the disease recurs with only 40% long-term survivors, stressing the need for more sensitive detection of disseminated disease during therapy. Methods To validate sensitive neuroblastoma mRNA RT-qPCR BM testing, we prospectively assessed serial BM samples from 345 international high‐risk neuroblastoma patients, treated in trials NB2004 (GPOH) or NBL2009 (DCOG), using PHOX2B, TH, DDC, CHRNA3, and GAP43 RT-qPCR mRNA markers and BM GD2-immunocytology. Association between BM-infiltration levels and event-free survival (EFS) and overall survival (OS) was estimated by using Cox regression models and Kaplan-Meier’s methodology. Results BM infiltration >10% by RT-qPCR at diagnosis was prognostic for survival (adjusted hazard ratio (HR) 1.82 [95%CI 1.25‐2.63] and 2.04 [1.33‐3.14] for EFS and OS, respectively). Any post-induction RT-qPCR positivity correlated with poor EFS and OS, with a HR of 2.10 [1.27-3.49] and 1.76 [1.01-3.08] and 5-years EFS of 26.6% [standard error 5.2%] versus 60.4% [6.7] and OS of 43.8% [5.9] versus 65.7% [6.6] for RT-qPCR-positive patients versus RT-qPCR-negative patients. In contrast, post-induction immunocytology positivity was not associated with EFS or OS (HR 1.22 [0.68-2.19] and 1.26 [0.54-2.42]). Conclusion This study validates the association of not clearing of BM metastases by sensitive RT-qPCR detection with very poor outcome. We therefore propose implementation of RT-qPCR for minimal residual disease testing in neuroblastoma to guide therapy.
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spelling doaj-art-4aff26c2b0f04188895371500b0cde782024-12-29T12:52:30ZengBMCJournal of Experimental & Clinical Cancer Research1756-99662024-12-0143111610.1186/s13046-024-03261-ySensitive liquid biopsy monitoring correlates with outcome in the prospective international GPOH-DCOG high-risk neuroblastoma RT-qPCR validation studyLieke M. J. van Zogchel0Boris Decarolis1Esther M. van Wezel2Lily Zappeij‐Kannegieter3Nina U. Gelineau4Roswitha Schumacher‐Kuckelkorn5Thorsten Simon6Frank Berthold7Max M. van Noesel8Marta Fiocco9C. Ellen van der Schoot10Barbara Hero11Janine Stutterheim12Godelieve A. M. Tytgat13Princess Máxima Center for Pediatric OncologyDepartment of Pediatric Oncology and Hematology, University Children’s Hospital of Cologne, and Medical Faculty, University of CologneDepartment of Experimental Immunohematology, Sanquin Research and Landsteiner Laboratory of the Amsterdam UMCDepartment of Immunocytology, Sanquin Research and Landsteiner Laboratory of the Amsterdam UMCPrincess Máxima Center for Pediatric OncologyDepartment of Pediatric Oncology and Hematology, University Children’s Hospital of Cologne, and Medical Faculty, University of CologneDepartment of Pediatric Oncology and Hematology, University Children’s Hospital of Cologne, and Medical Faculty, University of CologneDepartment of Pediatric Oncology and Hematology, University Children’s Hospital of Cologne, and Medical Faculty, University of ColognePrincess Máxima Center for Pediatric OncologyPrincess Máxima Center for Pediatric OncologyDepartment of Experimental Immunohematology, Sanquin Research and Landsteiner Laboratory of the Amsterdam UMCDepartment of Pediatric Oncology and Hematology, University Children’s Hospital of Cologne, and Medical Faculty, University of ColognePrincess Máxima Center for Pediatric OncologyPrincess Máxima Center for Pediatric OncologyAbstract Background Liquid biopsies offer less burdensome sensitive disease monitoring. Bone marrow (BM) metastases, common in various cancers including neuroblastoma, is associated with poor outcomes. In pediatric high-risk neuroblastoma most patients initially respond to treatment, but in the majority the disease recurs with only 40% long-term survivors, stressing the need for more sensitive detection of disseminated disease during therapy. Methods To validate sensitive neuroblastoma mRNA RT-qPCR BM testing, we prospectively assessed serial BM samples from 345 international high‐risk neuroblastoma patients, treated in trials NB2004 (GPOH) or NBL2009 (DCOG), using PHOX2B, TH, DDC, CHRNA3, and GAP43 RT-qPCR mRNA markers and BM GD2-immunocytology. Association between BM-infiltration levels and event-free survival (EFS) and overall survival (OS) was estimated by using Cox regression models and Kaplan-Meier’s methodology. Results BM infiltration >10% by RT-qPCR at diagnosis was prognostic for survival (adjusted hazard ratio (HR) 1.82 [95%CI 1.25‐2.63] and 2.04 [1.33‐3.14] for EFS and OS, respectively). Any post-induction RT-qPCR positivity correlated with poor EFS and OS, with a HR of 2.10 [1.27-3.49] and 1.76 [1.01-3.08] and 5-years EFS of 26.6% [standard error 5.2%] versus 60.4% [6.7] and OS of 43.8% [5.9] versus 65.7% [6.6] for RT-qPCR-positive patients versus RT-qPCR-negative patients. In contrast, post-induction immunocytology positivity was not associated with EFS or OS (HR 1.22 [0.68-2.19] and 1.26 [0.54-2.42]). Conclusion This study validates the association of not clearing of BM metastases by sensitive RT-qPCR detection with very poor outcome. We therefore propose implementation of RT-qPCR for minimal residual disease testing in neuroblastoma to guide therapy.https://doi.org/10.1186/s13046-024-03261-y
spellingShingle Lieke M. J. van Zogchel
Boris Decarolis
Esther M. van Wezel
Lily Zappeij‐Kannegieter
Nina U. Gelineau
Roswitha Schumacher‐Kuckelkorn
Thorsten Simon
Frank Berthold
Max M. van Noesel
Marta Fiocco
C. Ellen van der Schoot
Barbara Hero
Janine Stutterheim
Godelieve A. M. Tytgat
Sensitive liquid biopsy monitoring correlates with outcome in the prospective international GPOH-DCOG high-risk neuroblastoma RT-qPCR validation study
Journal of Experimental & Clinical Cancer Research
title Sensitive liquid biopsy monitoring correlates with outcome in the prospective international GPOH-DCOG high-risk neuroblastoma RT-qPCR validation study
title_full Sensitive liquid biopsy monitoring correlates with outcome in the prospective international GPOH-DCOG high-risk neuroblastoma RT-qPCR validation study
title_fullStr Sensitive liquid biopsy monitoring correlates with outcome in the prospective international GPOH-DCOG high-risk neuroblastoma RT-qPCR validation study
title_full_unstemmed Sensitive liquid biopsy monitoring correlates with outcome in the prospective international GPOH-DCOG high-risk neuroblastoma RT-qPCR validation study
title_short Sensitive liquid biopsy monitoring correlates with outcome in the prospective international GPOH-DCOG high-risk neuroblastoma RT-qPCR validation study
title_sort sensitive liquid biopsy monitoring correlates with outcome in the prospective international gpoh dcog high risk neuroblastoma rt qpcr validation study
url https://doi.org/10.1186/s13046-024-03261-y
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