Tumor-Promoted Changes in Pediatric Brain Histology Can Be Distinguished from Normal Parenchyma by Desorption Electrospray Ionization Mass Spectrometry Imaging

Authors

Ana L Seidinger
Felipe L T Silva
Mayara F Euzébio
Anna C Krieger
João Meidanis
Junier M Gutierrez
Thais M S Bezerra
Luciano Queiroz
Alex A Rosini Silva
Iva L Hoffmann
Camila M M Daiggi
Helder Tedeschi
Marcos N Eberlin
Livia S Eberlin
José A Yunes
Andreia M Porcari
Izilda A Cardinalli

Publication Date

11-13-2024

Journal

Biomedicines

DOI

10.3390/biomedicines12112593

PMID

39595159

PMCID

PMC11592165

PubMedCentral® Posted Date

11-13-2024

PubMedCentral® Full Text Version

Post-print

Published Open-Access

yes

Keywords

pediatric oncology, brain tumor, intraoperative tool, mass spectrometry imaging, DESI

Abstract

Background: Central nervous system (CNS) tumors are the second most frequent type of neoplasm in childhood and adolescence, after leukemia. Despite the incorporation of molecular classification and improvement of protocols combining chemotherapy, surgery, and radiotherapy, CNS tumors are still the most lethal neoplasm in this age group. Mass spectrometry imaging (MSI) is a powerful tool to map the distribution of molecular species in tissue sections. Among MSI techniques, desorption electrospray ionization (DESI-MSI) has been demonstrated to enable reliable agreement with the pathological evaluation of different adult cancer types, along with an acceptable time scale for intraoperative use.

Methods: In the present work, we aimed to investigate the chemical profile obtained by DESI-MSI as an intraoperative surgical management tool by profiling 162 pediatric brain biopsies and reporting the results according to the histopathology and molecular profile of the tumors.

Results: The 2D chemical images obtained by DESI-MSI allowed us to distinguish tumor-transformed tissue from non-tumor tissue with an accuracy of 96.8% in the training set and 94.3% in the validation set after statistical modeling of our data using Lasso. In addition, high-grade and low-grade tumors also displayed a distinct chemical profile when analyzed by DESI-MSI. We also provided evidence that the chemical profile of brain tumors obtained by DESI-MSI correlates with methylation-based molecular classes and specific immunophenotypes found in brain biopsies.

Conclusions: The results presented herein support the incorporation of DESI-MSI analysis as an intraoperative assistive tool in prospective clinical trials for pediatric brain tumors management in the near future.