Abstract
Objectives
No method is available to determine the non-perfused volume (NPV) repeatedly during magnetic resonance–guided high-intensity focused ultrasound (MR-HIFU) ablations of uterine fibroids, as repeated acquisition of contrast-enhanced T1-weighted (CE-T1w) scans is inhibited by safety concerns. The objective of this study was to develop and test a deep learning–based method for translation of diffusion-weighted imaging (DWI) into synthetic CE-T1w scans, for monitoring MR-HIFU treatment progression.
Methods
The algorithm was retrospectively trained and validated on data from 33 and 20 patients respectively who underwent an MR-HIFU treatment of uterine fibroids between June 2017 and January 2019. Postablation synthetic CE-T1w images were generated by a deep learning network trained on paired DWI and reference CE-T1w scans acquired during the treatment procedure. Quantitative analysis included calculation of the Dice coefficient of NPVs delineated on synthetic and reference CE-T1w scans. Four MR-HIFU radiologists assessed the outcome of MR-HIFU treatments and NPV ratio based on the synthetic and reference CE-T1w scans.
Results
Dice coefficient of NPVs was 71% (± 22%). The mean difference in NPV ratio was 1.4% (± 22%) and not statistically significant (p = 0.79). Absolute agreement of the radiologists on technical treatment success on synthetic and reference CE-T1w scans was 83%. NPV ratio estimations on synthetic and reference CE-T1w scans were not significantly different (p = 0.27).
Conclusions
Deep learning–based synthetic CE-T1w scans derived from intraprocedural DWI allow gadolinium-free visualization of the predicted NPV, and can potentially be used for repeated gadolinium-free monitoring of treatment progression during MR-HIFU therapy for uterine fibroids.
Key Points
• Synthetic CE-T1w scans can be derived from diffusion-weighted imaging using deep learning.
• Synthetic CE-T1w scans may be used for visualization of the NPV without using a contrast agent directly after MR-HIFU ablations of uterine fibroids.
Similar content being viewed by others
Abbreviations
- CE-T1w:
-
Contrast-enhanced T1-weighted
- cGAN:
-
Conditional generative adversarial network
- DL:
-
Deep learning
- DWI:
-
Diffusion-weighted imaging
- FA:
-
Flip angle
- Gd:
-
Gadolinium
- MAE:
-
Mean absolute error
- MR-HIFU:
-
Magnetic resonance–guided high-intensity focused ultrasound
- MSE:
-
Mean squared error
- NPV:
-
Non-perfused volume
- TE:
-
Echo time
- TR:
-
Repetition time
- UF:
-
Uterine fibroid
References
Verpalen IM, Anneveldt KJ, Nijholt IM et al (2019) Magnetic resonance-high intensity focused ultrasound (MR-HIFU) therapy of symptomatic uterine fibroids with unrestrictive treatment protocols: a systematic review and meta-analysis. Eur J Radiol 120:108700
Fennessy FM, Tempany CM, McDannold NJ et al (2007) Uterine leiomyomas: MR imaging-guided focused ultrasound surgery - results of different treatment protocols. Radiology 243:885–893
Park MJ, Kim YS, Rhim H, Lim HK (2014) Safety and therapeutic efficacy of complete or near-complete ablation of symptomatic uterine fibroid tumors by MR imaging-guided high-intensity focused US Therapy. J Vasc Interv Radiol 25:231–239
Al Hilli MM, Stewart EA (2010) Magnetic resonance-guided focused ultrasound surgery. Semin Reprod Med 28:242–249
Stewart EA, Gostout B, Rabinovici J, Kim HS, Regan L, Tempany CMC (2007) Sustained relief of leiomyoma symptoms by using focused ultrasound surgery. Obstet Gynecol 110:279–287
Verpalen IM, de Boer JP, Linstra M et al (2020) The Focused Ultrasound Myoma Outcome Study (FUMOS); a retrospective cohort study on long-term outcomes of MR-HIFU therapy. Eur Radiol 30:2473–2482
Keserci B, Duc NM (2017) The role of T1 perfusion-based classification in magnetic resonance-guided high-intensity focused ultrasound ablation of uterine fibroids. Eur Radiol 27:5299–5308
Hijnen NM, Elevelt A, Pikkemaat J, Bos C, Bartels LW, Grüll H (2013) The magnetic susceptibility effect of gadolinium-based contrast agents on PRFS-based MR thermometry during thermal interventions. J Ther Ultrasound 1:8
Hijnen NM, Elevelt A, Grüll H (2013) Stability and trapping of magnetic resonance imaging contrast agents during high-intensity focused ultrasound ablation therapy. Invest Radiol 48:517–524
Hectors SJCG, Jacobs I, Heijman E et al (2015) Multiparametric MRI analysis for the evaluation of MR-guided high intensity focused ultrasound tumor treatment. NMR Biomed 28:1125–1140
Zimmerman BE, Johnson S, Odeen H et al (2021) Learning multiparametric biomarkers for assessing MR-guided focused ultrasound treatment of malignant tumors. IEEE Trans Biomed Eng 68:1737–1747
Morochnik S, Ozhinsky E, Rieke V, Bucknor MD (2019) T2 mapping as a predictor of nonperfused volume in MRgFUS treatment of desmoid tumors. Int J Hyperthermia 36:1272–1277
Jacobs MA, Herskovits EH, Kim HS (2005) Uterine fibroids: diffusion-weighted MR imaging for monitoring therapy with focused ultrasound surgery - preliminary study. Radiology 236:196–203
Giles SL, Winfield JM, Collins DJ et al (2018) Value of diffusion-weighted imaging for monitoring tissue change during magnetic resonance-guided high-intensity focused ultrasound therapy in bone applications: an ex-vivo study. Eur Radiol Exp 2:10
Chetan MR, Lyon PC, Wu F et al (2019) Role of diffusion-weighted imaging in monitoring treatment response following high-intensity focused ultrasound ablation of recurrent sacral chordoma. Radiol Case Rep 14:1197–1201
Walker MR, Zhong J, Waspe AC et al (2019) Acute MR-guided high-intensity focused ultrasound lesion assessment using diffusion-weighted imaging and histological analysis. Front Neurol 10:1069
Jacobs MA, Ouwerkerk R, Kamel I, Bottomley PA, Bluemke DA, Kim HS (2009) Proton, diffusion-weighted imaging, and sodium (23Na) MRI of uterine leiomyomata after MR-guided high intensity focused ultrasound: a preliminary study. J Magn Reson Imaging 29:649
Jacobs MA, Gultekin DH, Kim HS (2010) Comparison between diffusion-weighted imaging, -weighted, and postcontrast -weighted imaging after MR-guided, high intensity, focused ultrasound treatment of uterine leiomyomata: preliminary results. Med Phys 37:4768–4776
Pilatou MC, Stewart EA, Maier SE et al (2009) MRI-based thermal dosimetry and diffusion-weighted imaging of MRI-guided focused ultrasound thermal ablation of uterine fibroids. J Magn Reson Imaging 29:404
Verpalen I, Boomsma M, Edens M, Heijman E (2019) The evaluation of the non-perfused volume after MR-HIFU treatment of uterine fibroids using quantitative T2-mapping and diffusion weighted imaging. In: 19th International Symposium of ISTU and 5th European Symposium of EUFUS. Barcelona, p 143
Ikink ME, Voogt MJ, Van Den Bosch MAAJ et al (2014) Diffusion-weighted magnetic resonance imaging using different b-value combinations for the evaluation of treatment results after volumetric MR-guided high-intensity focused ultrasound ablation of uterine fibroids. Eur Radiol 24:2118–2127
Ikink ME, Van Breugel JMM, Nijenhuis RJ, et al (2014) Intravoxel incoherent motion MRI for the characterization of uterine fibroids before MR-guided high-intensity focused ultrasound ablation. In: Proceedings of the Joint Annual Meeting International Society for Magnetic Resonance In Medicine - European Society for Magnetic Resonance in Medicine and Biology. Milan, p 3693
Verpalen IM (2021) Diffusion-weighted imaging to monitor treatment progression of magnetic resonance guided focused ultrasound fibroid ablation. In: Improving treatment efficacy of MR-HIFU fibroid ablation, Thesis. pp 131–148
Iima M, Le Bihan D (2016) Clinical intravoxel incoherent motion and diffusion MR imaging: past, present, and future. Radiology 278:13–32
Le Bihan D, Turner R (1992) The capillary network: a link between ivim and classical perfusion. Magn Reson Med 27:171–178
Dijkstra H, Oudkerk M, Kappert P, Sijens PE (2017) Assessment of the link between quantitative biexponential diffusion-weighted imaging and contrast-enhanced MRI in the liver. Magn Reson Imaging 38:47–53
Le Bihan D (2019) What can we see with IVIM MRI? Neuroimage 187:56–67
Guo Z, Zhang Q, Li X, Jing Z (2015) Intravoxel incoherent motion diffusion weighted MR imaging for monitoring the instantly therapeutic efficacy of radiofrequency ablation in rabbit VX2 tumors without evident links between conventional perfusion weighted images. PLoS One. https://doi.org/10.1371/journal.pone.0127964
Verpalen IM, Anneveldt KJ, Vos PC et al (2020) Use of multiparametric MRI to characterize uterine fibroid tissue types. MAGMA. https://doi.org/10.1007/s10334-020-00841-9
Klein S, Staring M, Murphy K, Viergever MA, Pluim JPW (2010) Elastix: a toolbox for intensity-based medical image registration. IEEE Trans Med Imaging 29:196–205
Gong E, Pauly JM, Wintermark M, Zaharchuk G (2018) Deep learning enables reduced gadolinium dose for contrast-enhanced brain MRI. J Magn Reson Imaging 48:330–340
Sun H, Liu X, Feng X, et al (2020) Substituting gadolinium in brain MRI using DeepContrast. Proc - Int Symp Biomed Imaging 2020-April:908–912
Zhao J, Li D, Kassam Z et al (2020) Tripartite-GAN: synthesizing liver contrast-enhanced MRI to improve tumor detection. Med Image Anal 63:101667
Kleesiek J, Morshuis JN, Isensee F et al (2019) Can virtual contrast enhancement in brain MRI replace gadolinium? Invest Radiol 54:653–660
Riexinger A, Martin J, Wetscherek A et al (2021) An optimized b-value distribution for triexponential intravoxel incoherent motion (IVIM) in the liver. Magn Reson Med 85:2095–2108
Wang L, Chen W, Yang W, Bi F, Yu FR (2020) A state-of-the-art review on image synthesis with generative adversarial networks. IEEE Access 8:63514–63537
Mongan J, Moy L, Kahn CE (2020) Checklist for Artificial Intelligence in Medical Imaging (CLAIM): a guide for authors and reviewers. Radiol Artif Intell 2:e200029
Keenan KE, Peskin AP, Wilmes LJ et al (2016) Variability and bias assessment in breast ADC measurement across multiple systems. J Magn Reson Imaging 44:846–855
Jafar MM (2016) Diffusion-weighted magnetic resonance imaging in cancer: reported apparent diffusion coefficients, in-vitro and in-vivo reproducibility. World J Radiol 8:21
Funding
The authors state that this work has not received any funding.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Guarantor
The scientific guarantor of this publication is M. F. Boomsma, MD PhD.
Conflict of interest
One of the authors (Edwin Heijman) is an employee of Philips. The remaining authors declare no relationships with any companies whose products or services may be related to the subject matter of the article
Statistics and biometry
One of the authors has significant statistical expertise.
Informed consent
Written informed consent was obtained from all subjects (patients) in the source studies (MASS1 and MASS2). This consent included the authorization to analyse study data outside the scope of the source studies, in the context of MR-HIFU treatments of uterine fibroids. Therefore, no post hoc contact with patients was required for the current retrospective study. Both the source studies and the retrospective study presented here have been approved by the institutional review board (IRB).
Ethical approval
Institutional review board approval was obtained.
Methodology
• retrospective
• method comparison study
• performed at one institution
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
ESM 1
(PDF 291 kb)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Slotman, D.J., Bartels, L.W., Zijlstra, A. et al. Diffusion-weighted MRI with deep learning for visualizing treatment results of MR-guided HIFU ablation of uterine fibroids. Eur Radiol 33, 4178–4188 (2023). https://doi.org/10.1007/s00330-022-09294-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00330-022-09294-1