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Published in: European Radiology 9/2021

01-09-2021 | Metastasis | Magnetic Resonance

Robust performance of deep learning for automatic detection and segmentation of brain metastases using three-dimensional black-blood and three-dimensional gradient echo imaging

Authors: Yae Won Park, Yohan Jun, Yangho Lee, Kyunghwa Han, Chansik An, Sung Soo Ahn, Dosik Hwang, Seung-Koo Lee

Published in: European Radiology | Issue 9/2021

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Abstract

Objectives

To evaluate whether a deep learning (DL) model using both three-dimensional (3D) black-blood (BB) imaging and 3D gradient echo (GRE) imaging may improve the detection and segmentation performance of brain metastases compared to that using only 3D GRE imaging.

Methods

A total of 188 patients with brain metastases (917 lesions) who underwent a brain metastasis MRI protocol including contrast-enhanced 3D BB and 3D GRE were included in the training set. DL models based on 3D U-net were constructed. The models were validated in the test set consisting of 45 patients with brain metastases (203 lesions) and 49 patients without brain metastases.

Results

The combined 3D BB and 3D GRE model yielded better performance than the 3D GRE model (sensitivities of 93.1% vs 76.8%, p < 0.001), and this effect was significantly stronger in subgroups with small metastases (p interaction < 0.001). For metastases < 3 mm, ≥ 3 mm and < 10 mm, and ≥ 10 mm, the sensitivities were 82.4%, 93.2%, and 100%, respectively. The combined 3D BB and 3D GRE model showed a false-positive per case of 0.59 in the test set. The combined 3D BB and 3D GRE model showed a Dice coefficient of 0.822, while 3D GRE model showed a lower Dice coefficient of 0.756.

Conclusions

The combined 3D BB and 3D GRE DL model may improve the detection and segmentation performance of brain metastases, especially in detecting small metastases.

Key Points

• The combined 3D BB and 3D GRE model yielded better performance for the detection of brain metastases than the 3D GRE model (p < 0.001), with sensitivities of 93.1% and 76.8%, respectively.
• The combined 3D BB and 3D GRE model showed a false-positive rate per case of 0.59 in the test set.
• The combined 3D BB and 3D GRE model showed a Dice coefficient of 0.822, while the 3D GRE model showed a lower Dice coefficient of 0.756.
Appendix
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Literature
1.
go back to reference Bradley KA, Mehta MP (2004) Management of brain metastases. Semin Oncol 31(5). WB Saunders, 2004 Bradley KA, Mehta MP (2004) Management of brain metastases. Semin Oncol 31(5). WB Saunders, 2004
2.
go back to reference Loeffler J, Patchell R, Sawaya R (1997) Metastatic brain cancer. Cancer 2523 Loeffler J, Patchell R, Sawaya R (1997) Metastatic brain cancer. Cancer 2523
3.
go back to reference Kondziolka D, Patel A, Lunsford LD, Kassam A, Flickinger JC (1999) Stereotactic radiosurgery plus whole brain radiotherapy versus radiotherapy alone for patients with multiple brain metastases. Int J Radiat Oncol Biol Phys 45:427–434CrossRef Kondziolka D, Patel A, Lunsford LD, Kassam A, Flickinger JC (1999) Stereotactic radiosurgery plus whole brain radiotherapy versus radiotherapy alone for patients with multiple brain metastases. Int J Radiat Oncol Biol Phys 45:427–434CrossRef
4.
go back to reference Patchell RA, Tibbs PA, Walsh JW et al (1990) A randomized trial of surgery in the treatment of single metastases to the brain. N Engl J Med 322:494–500CrossRef Patchell RA, Tibbs PA, Walsh JW et al (1990) A randomized trial of surgery in the treatment of single metastases to the brain. N Engl J Med 322:494–500CrossRef
5.
go back to reference Mehta MP, Rodrigus P, Terhaard C et al (2003) Survival and neurologic outcomes in a randomized trial of motexafin gadolinium and whole-brain radiation therapy in brain metastases. J Clin Oncol 21:2529–2536CrossRef Mehta MP, Rodrigus P, Terhaard C et al (2003) Survival and neurologic outcomes in a randomized trial of motexafin gadolinium and whole-brain radiation therapy in brain metastases. J Clin Oncol 21:2529–2536CrossRef
6.
go back to reference Growcott S, Dembrey T, Patel R, Eaton D, Cameron A (2020) Inter-observer variability in target volume delineations of benign and metastatic brain tumours for stereotactic radiosurgery: results of a national quality assurance programme. Clin Oncol (R Coll Radiol) 32:13–25CrossRef Growcott S, Dembrey T, Patel R, Eaton D, Cameron A (2020) Inter-observer variability in target volume delineations of benign and metastatic brain tumours for stereotactic radiosurgery: results of a national quality assurance programme. Clin Oncol (R Coll Radiol) 32:13–25CrossRef
7.
go back to reference Kamnitsas K, Ledig C, Newcombe VFJ et al (2017) Efficient multi-scale 3D CNN with fully connected CRF for accurate brain lesion segmentation. Med Image Anal 36:61–78CrossRef Kamnitsas K, Ledig C, Newcombe VFJ et al (2017) Efficient multi-scale 3D CNN with fully connected CRF for accurate brain lesion segmentation. Med Image Anal 36:61–78CrossRef
8.
go back to reference Charron O, Lallement A, Jarnet D, Noblet V, Clavier JB, Meyer P (2018) Automatic detection and segmentation of brain metastases on multimodal MR images with a deep convolutional neural network. Comput Biol Med 95:43–54CrossRef Charron O, Lallement A, Jarnet D, Noblet V, Clavier JB, Meyer P (2018) Automatic detection and segmentation of brain metastases on multimodal MR images with a deep convolutional neural network. Comput Biol Med 95:43–54CrossRef
9.
go back to reference Grøvik E, Yi D, Iv M, Tong E, Rubin D, Zaharchuk G (2020) Deep learning enables automatic detection and segmentation of brain metastases on multisequence MRI. J Magn Reson Imaging 51:175–182CrossRef Grøvik E, Yi D, Iv M, Tong E, Rubin D, Zaharchuk G (2020) Deep learning enables automatic detection and segmentation of brain metastases on multisequence MRI. J Magn Reson Imaging 51:175–182CrossRef
11.
go back to reference Xue J, Wang B, Ming Y et al (2020) Deep learning-based detection and segmentation-assisted management of brain metastases. Neuro Oncol 22:505–514CrossRef Xue J, Wang B, Ming Y et al (2020) Deep learning-based detection and segmentation-assisted management of brain metastases. Neuro Oncol 22:505–514CrossRef
12.
go back to reference Zhou Z, Sanders JW, Johnson JM et al (2020) Computer-aided detection of brain metastases in T1-weighted MRI for stereotactic radiosurgery using deep learning single-shot detectors. Radiology 295:407–415CrossRef Zhou Z, Sanders JW, Johnson JM et al (2020) Computer-aided detection of brain metastases in T1-weighted MRI for stereotactic radiosurgery using deep learning single-shot detectors. Radiology 295:407–415CrossRef
13.
go back to reference Lin X, DeAngelis LM (2015) Treatment of brain metastases. J Clin Oncol 33:3475–3484CrossRef Lin X, DeAngelis LM (2015) Treatment of brain metastases. J Clin Oncol 33:3475–3484CrossRef
14.
go back to reference Park J, Kim J, Yoo E, Lee H, Chang J-H, Kim EY (2012) Detection of small metastatic brain tumors: comparison of 3D contrast-enhanced whole-brain black-blood imaging and MP-RAGE imaging. Invest Radiol 47:136–141CrossRef Park J, Kim J, Yoo E, Lee H, Chang J-H, Kim EY (2012) Detection of small metastatic brain tumors: comparison of 3D contrast-enhanced whole-brain black-blood imaging and MP-RAGE imaging. Invest Radiol 47:136–141CrossRef
15.
go back to reference Park J, Kim EY (2010) Contrast-enhanced, three-dimensional, whole-brain, black-blood imaging: application to small brain metastases. Magn Reson Med 63:553–561CrossRef Park J, Kim EY (2010) Contrast-enhanced, three-dimensional, whole-brain, black-blood imaging: application to small brain metastases. Magn Reson Med 63:553–561CrossRef
16.
go back to reference Park YW, Ahn SJ (2018) Comparison of contrast-enhanced T2 FLAIR and 3D T1 black-blood fast spin-echo for detection of leptomeningeal metastases. Investig Magn Reson Imaging 22:86–93CrossRef Park YW, Ahn SJ (2018) Comparison of contrast-enhanced T2 FLAIR and 3D T1 black-blood fast spin-echo for detection of leptomeningeal metastases. Investig Magn Reson Imaging 22:86–93CrossRef
17.
go back to reference Suh CH, Jung SC, Kim KW, Pyo J (2016) The detectability of brain metastases using contrast-enhanced spin-echo or gradient-echo images: a systematic review and meta-analysis. J Neurooncol 129:363–371CrossRef Suh CH, Jung SC, Kim KW, Pyo J (2016) The detectability of brain metastases using contrast-enhanced spin-echo or gradient-echo images: a systematic review and meta-analysis. J Neurooncol 129:363–371CrossRef
18.
go back to reference Kaufmann TJ, Smits M, Boxerman J et al (2020) Consensus recommendations for a standardized brain tumor imaging protocol for clinical trials in brain metastases. Neuro Oncol 22:757–772CrossRef Kaufmann TJ, Smits M, Boxerman J et al (2020) Consensus recommendations for a standardized brain tumor imaging protocol for clinical trials in brain metastases. Neuro Oncol 22:757–772CrossRef
19.
go back to reference Roy S, Butman JA, Pham DL (2017) Robust skull stripping using multiple MR image contrasts insensitive to pathology. Neuroimage 146:132–147CrossRef Roy S, Butman JA, Pham DL (2017) Robust skull stripping using multiple MR image contrasts insensitive to pathology. Neuroimage 146:132–147CrossRef
20.
go back to reference Ronneberger O, Fischer P, Brox T (2015) U-net: Convolutional networks for biomedical image segmentation. International conference on medical image computing and computer-assisted intervention. Springer, Cham Ronneberger O, Fischer P, Brox T (2015) U-net: Convolutional networks for biomedical image segmentation. International conference on medical image computing and computer-assisted intervention. Springer, Cham
21.
go back to reference Myronenko A (2018) 3D MRI brain tumor segmentation using autoencoder regularization. International MICCAI Brain Lesion Workshop. Springer, Cham Myronenko A (2018) 3D MRI brain tumor segmentation using autoencoder regularization. International MICCAI Brain Lesion Workshop. Springer, Cham
22.
go back to reference Maas AL, Hannun AY, Ng AY (2013) Rectifier nonlinearities improve neural network acoustic models. Proc icml 3(1) Maas AL, Hannun AY, Ng AY (2013) Rectifier nonlinearities improve neural network acoustic models. Proc icml 3(1)
23.
go back to reference Wu Y, He K (2018) Group normalization. Proceedings of the European conference on computer vision (ECCV) Wu Y, He K (2018) Group normalization. Proceedings of the European conference on computer vision (ECCV)
24.
go back to reference Abadi M, Barham P, Chen J et al (2016) TensorFlow: a system for large-scale machine learning. 12th {USENIX} symposium on operating systems design and implementation ({OSDI} 16) Abadi M, Barham P, Chen J et al (2016) TensorFlow: a system for large-scale machine learning. 12th {USENIX} symposium on operating systems design and implementation ({OSDI} 16)
25.
go back to reference Kingma DP, Ba J (2014) Adam: a method for stochastic optimization. arXiv preprint arXiv:14126980 22 Kingma DP, Ba J (2014) Adam: a method for stochastic optimization. arXiv preprint arXiv:14126980 22
26.
go back to reference Zeger SL, Liang KY, Albert PS (1988) Models for longitudinal data: a generalized estimating equation approach. Biometrics 44:1049–1060CrossRef Zeger SL, Liang KY, Albert PS (1988) Models for longitudinal data: a generalized estimating equation approach. Biometrics 44:1049–1060CrossRef
27.
go back to reference Consul P, Famoye F (1992) Generalized Poisson regression model. Commun Stat Theory Methods 21:89–109CrossRef Consul P, Famoye F (1992) Generalized Poisson regression model. Commun Stat Theory Methods 21:89–109CrossRef
28.
go back to reference Lin NU, Lee EQ, Aoyama H et al (2015) Response assessment criteria for brain metastases: proposal from the RANO group. Lancet Oncol 16:e270–e278CrossRef Lin NU, Lee EQ, Aoyama H et al (2015) Response assessment criteria for brain metastases: proposal from the RANO group. Lancet Oncol 16:e270–e278CrossRef
29.
go back to reference Sunwoo L, Kim YJ, Choi SH et al (2017) Computer-aided detection of brain metastasis on 3D MR imaging: observer performance study. PLoS One 12:e0178265CrossRef Sunwoo L, Kim YJ, Choi SH et al (2017) Computer-aided detection of brain metastasis on 3D MR imaging: observer performance study. PLoS One 12:e0178265CrossRef
30.
go back to reference Chang K, Beers AL, Bai HX et al (2019) Automatic assessment of glioma burden: a deep learning algorithm for fully automated volumetric and bidimensional measurement. Neuro Oncol 21:1412–1422CrossRef Chang K, Beers AL, Bai HX et al (2019) Automatic assessment of glioma burden: a deep learning algorithm for fully automated volumetric and bidimensional measurement. Neuro Oncol 21:1412–1422CrossRef
31.
go back to reference Kickingereder P, Isensee F, Tursunova I et al (2019) Automated quantitative tumour response assessment of MRI in neuro-oncology with artificial neural networks: a multicentre, retrospective study. Lancet Oncol 20:728–740CrossRef Kickingereder P, Isensee F, Tursunova I et al (2019) Automated quantitative tumour response assessment of MRI in neuro-oncology with artificial neural networks: a multicentre, retrospective study. Lancet Oncol 20:728–740CrossRef
32.
go back to reference Bakas S, Reyes M, Jakab A et al (2018) Identifying the best machine learning algorithms for brain tumor segmentation, progression assessment, and overall survival prediction in the BRATS challenge. arXiv preprint arXiv:181102629 Bakas S, Reyes M, Jakab A et al (2018) Identifying the best machine learning algorithms for brain tumor segmentation, progression assessment, and overall survival prediction in the BRATS challenge. arXiv preprint arXiv:181102629
33.
go back to reference Weninger L, Rippel O, Koppers S, Merhof D (2018) Segmentation of brain tumors and patient survival prediction: methods for the BraTS 2018 challenge. International MICCAI Brain Lesion Workshop. Springer, Cham Weninger L, Rippel O, Koppers S, Merhof D (2018) Segmentation of brain tumors and patient survival prediction: methods for the BraTS 2018 challenge. International MICCAI Brain Lesion Workshop. Springer, Cham
34.
go back to reference Park YW, Han K, Ahn SS et al (2018) Prediction of IDH1-mutation and 1p/19q-codeletion status using preoperative MR imaging phenotypes in lower grade gliomas. AJNR Am J Neuroradiol 39:37–42CrossRef Park YW, Han K, Ahn SS et al (2018) Prediction of IDH1-mutation and 1p/19q-codeletion status using preoperative MR imaging phenotypes in lower grade gliomas. AJNR Am J Neuroradiol 39:37–42CrossRef
35.
go back to reference Anzalone N, Essig M, Lee SK et al (2013) Optimizing contrast-enhanced magnetic resonance imaging characterization of brain metastases: relevance to stereotactic radiosurgery. Neurosurgery 72:691–701CrossRef Anzalone N, Essig M, Lee SK et al (2013) Optimizing contrast-enhanced magnetic resonance imaging characterization of brain metastases: relevance to stereotactic radiosurgery. Neurosurgery 72:691–701CrossRef
36.
go back to reference Nagao E, Yoshiura T, Hiwatashi A et al (2011) 3D turbo spin-echo sequence with motion-sensitized driven-equilibrium preparation for detection of brain metastases on 3T MR imaging. AJNR Am J Neuroradiol 32:664–670CrossRef Nagao E, Yoshiura T, Hiwatashi A et al (2011) 3D turbo spin-echo sequence with motion-sensitized driven-equilibrium preparation for detection of brain metastases on 3T MR imaging. AJNR Am J Neuroradiol 32:664–670CrossRef
37.
go back to reference Kato Y, Higano S, Tamura H et al (2009) Usefulness of contrast-enhanced T1-weighted sampling perfection with application-optimized contrasts by using different flip angle evolutions in detection of small brain metastasis at 3T MR imaging: comparison with magnetization-prepared rapid acquisition of gradient echo imaging. AJNR Am J Neuroradiol 30:923–929CrossRef Kato Y, Higano S, Tamura H et al (2009) Usefulness of contrast-enhanced T1-weighted sampling perfection with application-optimized contrasts by using different flip angle evolutions in detection of small brain metastasis at 3T MR imaging: comparison with magnetization-prepared rapid acquisition of gradient echo imaging. AJNR Am J Neuroradiol 30:923–929CrossRef
38.
go back to reference Woo I, Lee A, Jung SC et al (2019) Fully automatic segmentation of acute ischemic lesions on diffusion-weighted imaging using convolutional neural networks: comparison with conventional algorithms. Korean J Radiol 20:1275–1284CrossRef Woo I, Lee A, Jung SC et al (2019) Fully automatic segmentation of acute ischemic lesions on diffusion-weighted imaging using convolutional neural networks: comparison with conventional algorithms. Korean J Radiol 20:1275–1284CrossRef
39.
go back to reference Xue Y, Farhat FG, Boukrina O et al (2020) A multi-path 2.5 dimensional convolutional neural network system for segmenting stroke lesions in brain MRI images. Neuroimage Clin 25:102118CrossRef Xue Y, Farhat FG, Boukrina O et al (2020) A multi-path 2.5 dimensional convolutional neural network system for segmenting stroke lesions in brain MRI images. Neuroimage Clin 25:102118CrossRef
40.
go back to reference Cagney DN, Martin AM, Catalano PJ et al (2017) Incidence and prognosis of patients with brain metastases at diagnosis of systemic malignancy: a population-based study. Neuro Oncol 19:1511–1521CrossRef Cagney DN, Martin AM, Catalano PJ et al (2017) Incidence and prognosis of patients with brain metastases at diagnosis of systemic malignancy: a population-based study. Neuro Oncol 19:1511–1521CrossRef
41.
go back to reference Jun Y, Eo T, Kim T et al (2018) Deep-learned 3D black-blood imaging using automatic labelling technique and 3D convolutional neural networks for detecting metastatic brain tumors. Sci Rep 8:1–11 Jun Y, Eo T, Kim T et al (2018) Deep-learned 3D black-blood imaging using automatic labelling technique and 3D convolutional neural networks for detecting metastatic brain tumors. Sci Rep 8:1–11
Metadata
Title
Robust performance of deep learning for automatic detection and segmentation of brain metastases using three-dimensional black-blood and three-dimensional gradient echo imaging
Authors
Yae Won Park
Yohan Jun
Yangho Lee
Kyunghwa Han
Chansik An
Sung Soo Ahn
Dosik Hwang
Seung-Koo Lee
Publication date
01-09-2021
Publisher
Springer Berlin Heidelberg
Keyword
Metastasis
Published in
European Radiology / Issue 9/2021
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-021-07783-3

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