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Spatial Omics Imaging of Fresh-Frozen Tissue and Routine FFPE Histopathology of a Single Cancer Needle Core Biopsy: A Freezing Device and Multimodal Workflow

SIMPLE SUMMARY: Routine clinical approaches for cancer diagnosis demand fast, cost-efficient, and reliable methods, and the implementation of these methods within clinical settings. Currently, histopathology is the gold standard for tissue-based clinical diagnosis. Recently, spatially resolved molec...

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Autores principales: Rittel, Miriam F., Schmidt, Stefan, Weis, Cleo-Aron, Birgin, Emrullah, van Marwick, Björn, Rädle, Matthias, Diehl, Steffen J., Rahbari, Nuh N., Marx, Alexander, Hopf, Carsten
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10216670/
https://www.ncbi.nlm.nih.gov/pubmed/37345020
http://dx.doi.org/10.3390/cancers15102676
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author Rittel, Miriam F.
Schmidt, Stefan
Weis, Cleo-Aron
Birgin, Emrullah
van Marwick, Björn
Rädle, Matthias
Diehl, Steffen J.
Rahbari, Nuh N.
Marx, Alexander
Hopf, Carsten
author_facet Rittel, Miriam F.
Schmidt, Stefan
Weis, Cleo-Aron
Birgin, Emrullah
van Marwick, Björn
Rädle, Matthias
Diehl, Steffen J.
Rahbari, Nuh N.
Marx, Alexander
Hopf, Carsten
author_sort Rittel, Miriam F.
collection PubMed
description SIMPLE SUMMARY: Routine clinical approaches for cancer diagnosis demand fast, cost-efficient, and reliable methods, and the implementation of these methods within clinical settings. Currently, histopathology is the gold standard for tissue-based clinical diagnosis. Recently, spatially resolved molecular profiling techniques such as mass spectrometry imaging (MSI) or infrared spectroscopy imaging (IRI) have increasingly contributed to clinical research, e.g., by differentiating cancer subtypes using molecular fingerprints. However, the adoption of the corresponding workflows in clinical routines remains challenging, especially for fresh-frozen tissue specimens. Here, we present a novel device based on 3D-printing technology, which facilitates the sample preparation of needle biopsies for correlated clinical tissue analysis. It enables the use of a combination of MSI and IRI on fresh-frozen clinical samples, with a histopathological examination of the same needle core after formalin fixation and paraffin embedding (FFPE). This device and workflow can pave the way for a more profound understanding of biomolecular processes in cancer and, thus, facilitate more accurate diagnosis. ABSTRACT: The complex molecular alterations that underlie cancer pathophysiology are studied in depth with omics methods using bulk tissue extracts. For spatially resolved tissue diagnostics using needle biopsy cores, however, histopathological analysis using stained FFPE tissue and the immunohistochemistry (IHC) of a few marker proteins is currently the main clinical focus. Today, spatial omics imaging using MSI or IRI is an emerging diagnostic technology for the identification and classification of various cancer types. However, to conserve tissue-specific metabolomic states, fast, reliable, and precise methods for the preparation of fresh-frozen (FF) tissue sections are crucial. Such methods are often incompatible with clinical practice, since spatial metabolomics and the routine histopathology of needle biopsies currently require two biopsies for FF and FFPE sampling, respectively. Therefore, we developed a device and corresponding laboratory and computational workflows for the multimodal spatial omics analysis of fresh-frozen, longitudinally sectioned needle biopsies to accompany standard FFPE histopathology of the same biopsy core. As a proof-of-concept, we analyzed surgical human liver cancer specimens using IRI and MSI with precise co-registration and, following FFPE processing, by sequential clinical pathology analysis of the same biopsy core. This workflow allowed for a spatial comparison between different spectral profiles and alterations in tissue histology, as well as a direct comparison for histological diagnosis without the need for an extra biopsy.
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spelling pubmed-102166702023-05-27 Spatial Omics Imaging of Fresh-Frozen Tissue and Routine FFPE Histopathology of a Single Cancer Needle Core Biopsy: A Freezing Device and Multimodal Workflow Rittel, Miriam F. Schmidt, Stefan Weis, Cleo-Aron Birgin, Emrullah van Marwick, Björn Rädle, Matthias Diehl, Steffen J. Rahbari, Nuh N. Marx, Alexander Hopf, Carsten Cancers (Basel) Article SIMPLE SUMMARY: Routine clinical approaches for cancer diagnosis demand fast, cost-efficient, and reliable methods, and the implementation of these methods within clinical settings. Currently, histopathology is the gold standard for tissue-based clinical diagnosis. Recently, spatially resolved molecular profiling techniques such as mass spectrometry imaging (MSI) or infrared spectroscopy imaging (IRI) have increasingly contributed to clinical research, e.g., by differentiating cancer subtypes using molecular fingerprints. However, the adoption of the corresponding workflows in clinical routines remains challenging, especially for fresh-frozen tissue specimens. Here, we present a novel device based on 3D-printing technology, which facilitates the sample preparation of needle biopsies for correlated clinical tissue analysis. It enables the use of a combination of MSI and IRI on fresh-frozen clinical samples, with a histopathological examination of the same needle core after formalin fixation and paraffin embedding (FFPE). This device and workflow can pave the way for a more profound understanding of biomolecular processes in cancer and, thus, facilitate more accurate diagnosis. ABSTRACT: The complex molecular alterations that underlie cancer pathophysiology are studied in depth with omics methods using bulk tissue extracts. For spatially resolved tissue diagnostics using needle biopsy cores, however, histopathological analysis using stained FFPE tissue and the immunohistochemistry (IHC) of a few marker proteins is currently the main clinical focus. Today, spatial omics imaging using MSI or IRI is an emerging diagnostic technology for the identification and classification of various cancer types. However, to conserve tissue-specific metabolomic states, fast, reliable, and precise methods for the preparation of fresh-frozen (FF) tissue sections are crucial. Such methods are often incompatible with clinical practice, since spatial metabolomics and the routine histopathology of needle biopsies currently require two biopsies for FF and FFPE sampling, respectively. Therefore, we developed a device and corresponding laboratory and computational workflows for the multimodal spatial omics analysis of fresh-frozen, longitudinally sectioned needle biopsies to accompany standard FFPE histopathology of the same biopsy core. As a proof-of-concept, we analyzed surgical human liver cancer specimens using IRI and MSI with precise co-registration and, following FFPE processing, by sequential clinical pathology analysis of the same biopsy core. This workflow allowed for a spatial comparison between different spectral profiles and alterations in tissue histology, as well as a direct comparison for histological diagnosis without the need for an extra biopsy. MDPI 2023-05-10 /pmc/articles/PMC10216670/ /pubmed/37345020 http://dx.doi.org/10.3390/cancers15102676 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Rittel, Miriam F.
Schmidt, Stefan
Weis, Cleo-Aron
Birgin, Emrullah
van Marwick, Björn
Rädle, Matthias
Diehl, Steffen J.
Rahbari, Nuh N.
Marx, Alexander
Hopf, Carsten
Spatial Omics Imaging of Fresh-Frozen Tissue and Routine FFPE Histopathology of a Single Cancer Needle Core Biopsy: A Freezing Device and Multimodal Workflow
title Spatial Omics Imaging of Fresh-Frozen Tissue and Routine FFPE Histopathology of a Single Cancer Needle Core Biopsy: A Freezing Device and Multimodal Workflow
title_full Spatial Omics Imaging of Fresh-Frozen Tissue and Routine FFPE Histopathology of a Single Cancer Needle Core Biopsy: A Freezing Device and Multimodal Workflow
title_fullStr Spatial Omics Imaging of Fresh-Frozen Tissue and Routine FFPE Histopathology of a Single Cancer Needle Core Biopsy: A Freezing Device and Multimodal Workflow
title_full_unstemmed Spatial Omics Imaging of Fresh-Frozen Tissue and Routine FFPE Histopathology of a Single Cancer Needle Core Biopsy: A Freezing Device and Multimodal Workflow
title_short Spatial Omics Imaging of Fresh-Frozen Tissue and Routine FFPE Histopathology of a Single Cancer Needle Core Biopsy: A Freezing Device and Multimodal Workflow
title_sort spatial omics imaging of fresh-frozen tissue and routine ffpe histopathology of a single cancer needle core biopsy: a freezing device and multimodal workflow
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10216670/
https://www.ncbi.nlm.nih.gov/pubmed/37345020
http://dx.doi.org/10.3390/cancers15102676
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