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A convolutional neural network with self-attention for fully automated metabolic tumor volume delineation of head and neck cancer in [Formula: see text] F]FDG PET/CT

PURPOSE: PET-derived metabolic tumor volume (MTV) and total lesion glycolysis of the primary tumor are known to be prognostic of clinical outcome in head and neck cancer (HNC). Including evaluation of lymph node metastases can further increase the prognostic value of PET but accurate manual delineat...

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Autores principales: Nikulin, Pavel, Zschaeck, Sebastian, Maus, Jens, Cegla, Paulina, Lombardo, Elia, Furth, Christian, Kaźmierska, Joanna, Rogasch, Julian M. M., Holzgreve, Adrien, Albert, Nathalie L., Ferentinos, Konstantinos, Strouthos, Iosif, Hajiyianni, Marina, Marschner, Sebastian N., Belka, Claus, Landry, Guillaume, Cholewinski, Witold, Kotzerke, Jörg, Hofheinz, Frank, van den Hoff, Jörg
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Berlin Heidelberg 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10317885/
https://www.ncbi.nlm.nih.gov/pubmed/37079128
http://dx.doi.org/10.1007/s00259-023-06197-1
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author Nikulin, Pavel
Zschaeck, Sebastian
Maus, Jens
Cegla, Paulina
Lombardo, Elia
Furth, Christian
Kaźmierska, Joanna
Rogasch, Julian M. M.
Holzgreve, Adrien
Albert, Nathalie L.
Ferentinos, Konstantinos
Strouthos, Iosif
Hajiyianni, Marina
Marschner, Sebastian N.
Belka, Claus
Landry, Guillaume
Cholewinski, Witold
Kotzerke, Jörg
Hofheinz, Frank
van den Hoff, Jörg
author_facet Nikulin, Pavel
Zschaeck, Sebastian
Maus, Jens
Cegla, Paulina
Lombardo, Elia
Furth, Christian
Kaźmierska, Joanna
Rogasch, Julian M. M.
Holzgreve, Adrien
Albert, Nathalie L.
Ferentinos, Konstantinos
Strouthos, Iosif
Hajiyianni, Marina
Marschner, Sebastian N.
Belka, Claus
Landry, Guillaume
Cholewinski, Witold
Kotzerke, Jörg
Hofheinz, Frank
van den Hoff, Jörg
author_sort Nikulin, Pavel
collection PubMed
description PURPOSE: PET-derived metabolic tumor volume (MTV) and total lesion glycolysis of the primary tumor are known to be prognostic of clinical outcome in head and neck cancer (HNC). Including evaluation of lymph node metastases can further increase the prognostic value of PET but accurate manual delineation and classification of all lesions is time-consuming and prone to interobserver variability. Our goal, therefore, was development and evaluation of an automated tool for MTV delineation/classification of primary tumor and lymph node metastases in PET/CT investigations of HNC patients. METHODS: Automated lesion delineation was performed with a residual 3D U-Net convolutional neural network (CNN) incorporating a multi-head self-attention block. 698 [Formula: see text] F]FDG PET/CT scans from 3 different sites and 5 public databases were used for network training and testing. An external dataset of 181 [Formula: see text] F]FDG PET/CT scans from 2 additional sites was employed to assess the generalizability of the network. In these data, primary tumor and lymph node (LN) metastases were interactively delineated and labeled by two experienced physicians. Performance of the trained network models was assessed by 5-fold cross-validation in the main dataset and by pooling results from the 5 developed models in the external dataset. The Dice similarity coefficient (DSC) for individual delineation tasks and the primary tumor/metastasis classification accuracy were used as evaluation metrics. Additionally, a survival analysis using univariate Cox regression was performed comparing achieved group separation for manual and automated delineation, respectively. RESULTS: In the cross-validation experiment, delineation of all malignant lesions with the trained U-Net models achieves DSC of 0.885, 0.805, and 0.870 for primary tumor, LN metastases, and the union of both, respectively. In external testing, the DSC reaches 0.850, 0.724, and 0.823 for primary tumor, LN metastases, and the union of both, respectively. The voxel classification accuracy was 98.0% and 97.9% in cross-validation and external data, respectively. Univariate Cox analysis in the cross-validation and the external testing reveals that manually and automatically derived total MTVs are both highly prognostic with respect to overall survival, yielding essentially identical hazard ratios (HR) ([Formula: see text] ; [Formula: see text] vs. [Formula: see text] ; [Formula: see text] in cross-validation and [Formula: see text] ; [Formula: see text] vs. [Formula: see text] ; [Formula: see text] in external testing). CONCLUSION: To the best of our knowledge, this work presents the first CNN model for successful MTV delineation and lesion classification in HNC. In the vast majority of patients, the network performs satisfactory delineation and classification of primary tumor and lymph node metastases and only rarely requires more than minimal manual correction. It is thus able to massively facilitate study data evaluation in large patient groups and also does have clear potential for supervised clinical application. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00259-023-06197-1.
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spelling pubmed-103178852023-07-05 A convolutional neural network with self-attention for fully automated metabolic tumor volume delineation of head and neck cancer in [Formula: see text] F]FDG PET/CT Nikulin, Pavel Zschaeck, Sebastian Maus, Jens Cegla, Paulina Lombardo, Elia Furth, Christian Kaźmierska, Joanna Rogasch, Julian M. M. Holzgreve, Adrien Albert, Nathalie L. Ferentinos, Konstantinos Strouthos, Iosif Hajiyianni, Marina Marschner, Sebastian N. Belka, Claus Landry, Guillaume Cholewinski, Witold Kotzerke, Jörg Hofheinz, Frank van den Hoff, Jörg Eur J Nucl Med Mol Imaging Original Article PURPOSE: PET-derived metabolic tumor volume (MTV) and total lesion glycolysis of the primary tumor are known to be prognostic of clinical outcome in head and neck cancer (HNC). Including evaluation of lymph node metastases can further increase the prognostic value of PET but accurate manual delineation and classification of all lesions is time-consuming and prone to interobserver variability. Our goal, therefore, was development and evaluation of an automated tool for MTV delineation/classification of primary tumor and lymph node metastases in PET/CT investigations of HNC patients. METHODS: Automated lesion delineation was performed with a residual 3D U-Net convolutional neural network (CNN) incorporating a multi-head self-attention block. 698 [Formula: see text] F]FDG PET/CT scans from 3 different sites and 5 public databases were used for network training and testing. An external dataset of 181 [Formula: see text] F]FDG PET/CT scans from 2 additional sites was employed to assess the generalizability of the network. In these data, primary tumor and lymph node (LN) metastases were interactively delineated and labeled by two experienced physicians. Performance of the trained network models was assessed by 5-fold cross-validation in the main dataset and by pooling results from the 5 developed models in the external dataset. The Dice similarity coefficient (DSC) for individual delineation tasks and the primary tumor/metastasis classification accuracy were used as evaluation metrics. Additionally, a survival analysis using univariate Cox regression was performed comparing achieved group separation for manual and automated delineation, respectively. RESULTS: In the cross-validation experiment, delineation of all malignant lesions with the trained U-Net models achieves DSC of 0.885, 0.805, and 0.870 for primary tumor, LN metastases, and the union of both, respectively. In external testing, the DSC reaches 0.850, 0.724, and 0.823 for primary tumor, LN metastases, and the union of both, respectively. The voxel classification accuracy was 98.0% and 97.9% in cross-validation and external data, respectively. Univariate Cox analysis in the cross-validation and the external testing reveals that manually and automatically derived total MTVs are both highly prognostic with respect to overall survival, yielding essentially identical hazard ratios (HR) ([Formula: see text] ; [Formula: see text] vs. [Formula: see text] ; [Formula: see text] in cross-validation and [Formula: see text] ; [Formula: see text] vs. [Formula: see text] ; [Formula: see text] in external testing). CONCLUSION: To the best of our knowledge, this work presents the first CNN model for successful MTV delineation and lesion classification in HNC. In the vast majority of patients, the network performs satisfactory delineation and classification of primary tumor and lymph node metastases and only rarely requires more than minimal manual correction. It is thus able to massively facilitate study data evaluation in large patient groups and also does have clear potential for supervised clinical application. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00259-023-06197-1. Springer Berlin Heidelberg 2023-04-20 2023 /pmc/articles/PMC10317885/ /pubmed/37079128 http://dx.doi.org/10.1007/s00259-023-06197-1 Text en © The Author(s) 2023, corrected publication 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Original Article
Nikulin, Pavel
Zschaeck, Sebastian
Maus, Jens
Cegla, Paulina
Lombardo, Elia
Furth, Christian
Kaźmierska, Joanna
Rogasch, Julian M. M.
Holzgreve, Adrien
Albert, Nathalie L.
Ferentinos, Konstantinos
Strouthos, Iosif
Hajiyianni, Marina
Marschner, Sebastian N.
Belka, Claus
Landry, Guillaume
Cholewinski, Witold
Kotzerke, Jörg
Hofheinz, Frank
van den Hoff, Jörg
A convolutional neural network with self-attention for fully automated metabolic tumor volume delineation of head and neck cancer in [Formula: see text] F]FDG PET/CT
title A convolutional neural network with self-attention for fully automated metabolic tumor volume delineation of head and neck cancer in [Formula: see text] F]FDG PET/CT
title_full A convolutional neural network with self-attention for fully automated metabolic tumor volume delineation of head and neck cancer in [Formula: see text] F]FDG PET/CT
title_fullStr A convolutional neural network with self-attention for fully automated metabolic tumor volume delineation of head and neck cancer in [Formula: see text] F]FDG PET/CT
title_full_unstemmed A convolutional neural network with self-attention for fully automated metabolic tumor volume delineation of head and neck cancer in [Formula: see text] F]FDG PET/CT
title_short A convolutional neural network with self-attention for fully automated metabolic tumor volume delineation of head and neck cancer in [Formula: see text] F]FDG PET/CT
title_sort convolutional neural network with self-attention for fully automated metabolic tumor volume delineation of head and neck cancer in [formula: see text] f]fdg pet/ct
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10317885/
https://www.ncbi.nlm.nih.gov/pubmed/37079128
http://dx.doi.org/10.1007/s00259-023-06197-1
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