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Deep-learning-based reconstruction of undersampled MRI to reduce scan times: a multicentre, retrospective, cohort study - 27/02/24

Doi : 10.1016/S1470-2045(23)00641-1 
Aditya Rastogi, PhD a, b, Gianluca Brugnara, MD a, b, Martha Foltyn-Dumitru, MD a, b, Mustafa Ahmed Mahmutoglu, MD a, b, Chandrakanth J Preetha, MSc a, b, Erich Kobler, PhD h, Irada Pflüger, MD a, b, Marianne Schell, MD a, b, Katerina Deike-Hofmann, MD h, ab, Tobias Kessler, MD d, m, Martin J van den Bent, ProfMD i, Ahmed Idbaih, MD j, Michael Platten, ProfMD k, l, Alba A Brandes, ProfMD n, Burt Nabors, ProfMD o, p, Roger Stupp, ProfMD q, r, s, Denise Bernhardt, MD t, Jürgen Debus, ProfMD c, e, f, Amir Abdollahi, ProfMD c, e, f, Thierry Gorlia, PhD u, Jörg-Christian Tonn, ProfMD v, w, Michael Weller, ProfMD x, Klaus H Maier-Hein, ProfPhD y, aa, Alexander Radbruch, ProfMD h, Wolfgang Wick, ProfMD d, m, Martin Bendszus, ProfMD b, Hagen Meredig, MD a, b, Felix T Kurz, ProfMD PhD g, z, Philipp Vollmuth, ProfMD a, b, h, y,
a Division for Computational Neuroimaging, Department of Neuroradiology, Heidelberg University Hospital, Heidelberg, Germany 
b Department of Neuroradiology, Heidelberg University Hospital, Heidelberg, Germany 
c Department of Radiation Oncology, Heidelberg University Hospital, Heidelberg, Germany 
d Neurology Clinic, Heidelberg University Hospital, Heidelberg, Germany 
e Heidelberg Institute of Radiation Oncology, Heidelberg University Hospital, Heidelberg, Germany 
f Heidelberg Ion-Beam Therapy Center, Heidelberg University Hospital, Heidelberg, Germany 
g Division of Diagnostic and Interventional Neuroradiology, Geneva University Hospitals, Geneva, Switzerland 
h Department of Neuroradiology, University Medical Center Bonn, Rheinische Friedrich-Wilhelms-Universität Bonn, Bonn, Germany 
i Brain Tumor Center at Erasmus MC Cancer Institute, Rotterdam, Netherlands 
j Assistance Publique-Hôpitaux de Paris, Service de Neurologie 1, Hôpital Pitié-Salpêtrière, Sorbonne Université, Paris, France 
k Department of Neurology, Medical Faculty Mannheim, Mannheim Center for Translational Neuroscience, University of Heidelberg, Mannheim, Germany 
l Clinical Cooperation Unit Neuroimmunology and Brain Tumor Immunology, German Cancer Consortium within German Cancer Research Center, Heidelberg, Germany 
m Clinical Cooperation Unit Neurooncology, German Cancer Consortium within German Cancer Research Center, Heidelberg, Germany 
n Department of Medical Oncology, Azienda UnitàSanitaria Locale of Bologna, Bologna, Italy 
o Department of Neurology, Division of Neuro-Oncology, University of Alabama at Birmingham, Birmingham, AL, USA 
p O’Neal Comprehensive Cancer Center, University of Alabama at Birmingham, Birmingham, AL, USA 
q Lou and Jean Malnati Brain Tumor Institute, Robert H Lurie Comprehensive Cancer Center, Northwestern Medicine and Northwestern University, Chicago, USA 
r Department of Neurological Surgery, Northwestern Medicine and Northwestern University, Chicago, USA 
s Department of Neurology, Northwestern Medicine and Northwestern University, Chicago, USA 
t Department of Radiation Oncology, School of Medicine and Klinikum rechts der Isar, Technical University of Munich, Munich, Germany 
u European Organization for Research and Treatment of Cancer, Brussels, Belgium 
v Department of Neurosurgery, Ludwig-Maximilians-University, Munich, Germany 
w German Cancer Consortium within German Center Research Center, partner site Munich, Germany 
x Department of Neurology, University Hospital and University of Zurich, Zurich, Switzerland 
y Medical Image Computing, German Cancer Research Center, Heidelberg, Germany 
z Department of Radiology, German Cancer Research Center, Heidelberg, Germany 
aa Pattern Analysis and Learning Group, Department of Radiation Oncology, Heidelberg University Hospital, Heidelberg, Germany 
ab German Center for Neurodegenerative Diseases, Bonn, Germany 

* Correspondence to: Prof Philipp Vollmuth, Division for Computational Neuroimaging, Department of Neuroradiology, Heidelberg University Hospital, 69120 Heidelberg, Germany Division for Computational Neuroimaging Department of Neuroradiology Heidelberg University Hospital Heidelberg 69120 Germany

Summary

Background

The extended acquisition times required for MRI limit its availability in resource-constrained settings. Consequently, accelerating MRI by undersampling k-space data, which is necessary to reconstruct an image, has been a long-standing but important challenge. We aimed to develop a deep convolutional neural network (dCNN) optimisation method for MRI reconstruction and to reduce scan times and evaluate its effect on image quality and accuracy of oncological imaging biomarkers.

Methods

In this multicentre, retrospective, cohort study, MRI data from patients with glioblastoma treated at Heidelberg University Hospital (775 patients and 775 examinations) and from the phase 2 CORE trial (260 patients, 1083 examinations, and 58 institutions) and the phase 3 CENTRIC trial (505 patients, 3147 examinations, and 139 institutions) were used to develop, train, and test dCNN for reconstructing MRI from highly undersampled single-coil k-space data with various acceleration rates (R=2, 4, 6, 8, 10, and 15). Independent testing was performed with MRIs from the phase 2/3 EORTC-26101 trial (528 patients with glioblastoma, 1974 examinations, and 32 institutions). The similarity between undersampled dCNN-reconstructed and original MRIs was quantified with various image quality metrics, including structural similarity index measure (SSIM) and the accuracy of undersampled dCNN-reconstructed MRI on downstream radiological assessment of imaging biomarkers in oncology (automated artificial intelligence-based quantification of tumour burden and treatment response) was performed in the EORTC-26101 test dataset. The public NYU Langone Health fastMRI brain test dataset (558 patients and 558 examinations) was used to validate the generalisability and robustness of the dCNN for reconstructing MRIs from available multi-coil (parallel imaging) k-space data.

Findings

In the EORTC-26101 test dataset, the median SSIM of undersampled dCNN-reconstructed MRI ranged from 0·88 to 0·99 across different acceleration rates, with 0·92 (95% CI 0·92–0·93) for 10-times acceleration (R=10). The 10-times undersampled dCNN-reconstructed MRI yielded excellent agreement with original MRI when assessing volumes of contrast-enhancing tumour (median DICE for spatial agreement of 0·89 [95% CI 0·88 to 0·89]; median volume difference of 0·01 cm3 [95% CI 0·00 to 0·03] equalling 0·21%; p=0·0036 for equivalence) or non-enhancing tumour or oedema (median DICE of 0·94 [95% CI 0·94 to 0·95]; median volume difference of –0·79 cm3 [95% CI –0·87 to –0·72] equalling –1·77%; p=0·023 for equivalence) in the EORTC-26101 test dataset. Automated volumetric tumour response assessment in the EORTC-26101 test dataset yielded an identical median time to progression of 4·27 months (95% CI 4·14 to 4·57) when using 10-times-undersampled dCNN-reconstructed or original MRI (log-rank p=0·80) and agreement in the time to progression in 374 (95·2%) of 393 patients with data. The dCNN generalised well to the fastMRI brain dataset, with significant improvements in the median SSIM when using multi-coil compared with single-coil k-space data (p<0·0001).

Interpretation

Deep-learning-based reconstruction of undersampled MRI allows for a substantial reduction of scan times, with a 10-times acceleration demonstrating excellent image quality while preserving the accuracy of derived imaging biomarkers for the assessment of oncological treatment response. Our developments are available as open source software and hold considerable promise for increasing the accessibility to MRI, pending further prospective validation.

Funding

Deutsche Forschungsgemeinschaft (German Research Foundation) and an Else Kröner Clinician Scientist Endowed Professorship by the Else Kröner Fresenius Foundation.

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© 2024  The Author(s). Published by Elsevier Ltd. This is an Open Access article under the CC BY 4.0 license. Publié par Elsevier Masson SAS. Tous droits réservés.
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