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Published in: Alzheimer's Research & Therapy 1/2021

01-12-2021 | Magnetic Resonance Imaging | Research

Enhancing magnetic resonance imaging-driven Alzheimer’s disease classification performance using generative adversarial learning

Authors: Xiao Zhou, Shangran Qiu, Prajakta S. Joshi, Chonghua Xue, Ronald J. Killiany, Asim Z. Mian, Sang P. Chin, Rhoda Au, Vijaya B. Kolachalama

Published in: Alzheimer's Research & Therapy | Issue 1/2021

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Abstract

Background

Generative adversarial networks (GAN) can produce images of improved quality but their ability to augment image-based classification is not fully explored. We evaluated if a modified GAN can learn from magnetic resonance imaging (MRI) scans of multiple magnetic field strengths to enhance Alzheimer’s disease (AD) classification performance.

Methods

T1-weighted brain MRI scans from 151 participants of the Alzheimer’s Disease Neuroimaging Initiative (ADNI), who underwent both 1.5-Tesla (1.5-T) and 3-Tesla imaging at the same time were selected to construct a GAN model. This model was trained along with a three-dimensional fully convolutional network (FCN) using the generated images (3T*) as inputs to predict AD status. Quality of the generated images was evaluated using signal to noise ratio (SNR), Blind/Referenceless Image Spatial Quality Evaluator (BRISQUE) and Natural Image Quality Evaluator (NIQE). Cases from the Australian Imaging, Biomarker & Lifestyle Flagship Study of Ageing (AIBL, n = 107) and the National Alzheimer’s Coordinating Center (NACC, n = 565) were used for model validation.

Results

The 3T*-based FCN classifier performed better than the FCN model trained using the 1.5-T scans. Specifically, the mean area under curve increased from 0.907 to 0.932, from 0.934 to 0.940, and from 0.870 to 0.907 on the ADNI test, AIBL, and NACC datasets, respectively. Additionally, we found that the mean quality of the generated (3T*) images was consistently higher than the 1.5-T images, as measured using SNR, BRISQUE, and NIQE on the validation datasets.

Conclusion

This study demonstrates a proof of principle that GAN frameworks can be constructed to augment AD classification performance and improve image quality.
Appendix
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Literature
1.
go back to reference Sperling R, Mormino E, Johnson K. The evolution of preclinical Alzheimer’s disease: implications for prevention trials. Neuron. 2014;84(3):608–22.CrossRef Sperling R, Mormino E, Johnson K. The evolution of preclinical Alzheimer’s disease: implications for prevention trials. Neuron. 2014;84(3):608–22.CrossRef
2.
go back to reference Jack CR, Jr., Bernstein MA, Fox NC, Thompson P, Alexander G, Harvey D, Borowski B, Britson PJ, J LW, Ward C et al: The Alzheimer’s disease neuroimaging initiative (ADNI): MRI methods. J Magn Reson Imaging 2008, 27(4):685–691. Jack CR, Jr., Bernstein MA, Fox NC, Thompson P, Alexander G, Harvey D, Borowski B, Britson PJ, J LW, Ward C et al: The Alzheimer’s disease neuroimaging initiative (ADNI): MRI methods. J Magn Reson Imaging 2008, 27(4):685–691.
3.
go back to reference Ellis KA, Rowe CC, Villemagne VL, Martins RN, Masters CL, Salvado O, Szoeke C, Ames D, group Ar: Addressing population aging and Alzheimer’s disease through the Australian imaging biomarkers and lifestyle study: collaboration with the Alzheimer’s Disease Neuroimaging Initiative. Alzheimers Dement 2010, 6(3):291–296. Ellis KA, Rowe CC, Villemagne VL, Martins RN, Masters CL, Salvado O, Szoeke C, Ames D, group Ar: Addressing population aging and Alzheimer’s disease through the Australian imaging biomarkers and lifestyle study: collaboration with the Alzheimer’s Disease Neuroimaging Initiative. Alzheimers Dement 2010, 6(3):291–296.
4.
go back to reference Beekly DL, Ramos EM, Lee WW, Deitrich WD, Jacka ME, Wu J, Hubbard JL, Koepsell TD, Morris JC, Kukull WA, et al. The National Alzheimer’s Coordinating Center (NACC) database: the uniform data set. Alzheimer Dis Assoc Disord. 2007;21(3):249–58.CrossRef Beekly DL, Ramos EM, Lee WW, Deitrich WD, Jacka ME, Wu J, Hubbard JL, Koepsell TD, Morris JC, Kukull WA, et al. The National Alzheimer’s Coordinating Center (NACC) database: the uniform data set. Alzheimer Dis Assoc Disord. 2007;21(3):249–58.CrossRef
5.
go back to reference Goodfellow IJ, Pouget-Abadie J, Mirza M, Xu B, Warde-Farley D, Ozair S, Courville A, Bengio Y. Generative adversarial nets. In: Proceedings of the 27th International Conference on Neural Information Processing Systems -Volume 2, NIPS’14, page 2672–2680, Cambridge: MIT Press; 2014. Goodfellow IJ, Pouget-Abadie J, Mirza M, Xu B, Warde-Farley D, Ozair S, Courville A, Bengio Y. Generative adversarial nets. In: Proceedings of the 27th International Conference on Neural Information Processing Systems -Volume 2, NIPS’14, page 2672–2680, Cambridge: MIT Press; 2014.
6.
go back to reference Wang J, Chen Y, Wu Y, Shi J, Gee J. Enhanced generative adversarial network for 3D brain MRI super-resolution. In: 2020 IEEE Winter Conference on Applications of Computer Vision (WACV); 2020. p. 3616–25.CrossRef Wang J, Chen Y, Wu Y, Shi J, Gee J. Enhanced generative adversarial network for 3D brain MRI super-resolution. In: 2020 IEEE Winter Conference on Applications of Computer Vision (WACV); 2020. p. 3616–25.CrossRef
7.
go back to reference Gu Y, Zeng Z, Chen H, Wei J, Zhang Y, Chen B, Li Y, Qin Y, Xie Q, Jiang Z, et al. MedSRGAN: medical images super-resolution using generative adversarial networks. Multimed Tools Appl. 2020;79(29–30):21815–40.CrossRef Gu Y, Zeng Z, Chen H, Wei J, Zhang Y, Chen B, Li Y, Qin Y, Xie Q, Jiang Z, et al. MedSRGAN: medical images super-resolution using generative adversarial networks. Multimed Tools Appl. 2020;79(29–30):21815–40.CrossRef
8.
go back to reference Tan C, Zhu J, Lio’ P. Arbitrary Scale Super-Resolution for Brain MRI Images. In: Artificial Intelligence Applications and Innovations. edn; 2020. p. 165–76.CrossRef Tan C, Zhu J, Lio’ P. Arbitrary Scale Super-Resolution for Brain MRI Images. In: Artificial Intelligence Applications and Innovations. edn; 2020. p. 165–76.CrossRef
9.
go back to reference Delannoy Q, Pham CH, Cazorla C, Tor-Diez C, Dolle G, Meunier H, Bednarek N, Fablet R, Passat N, Rousseau F. SegSRGAN: super-resolution and segmentation using generative adversarial networks - application to neonatal brain MRI. Comput Biol Med. 2020;120:103755.CrossRef Delannoy Q, Pham CH, Cazorla C, Tor-Diez C, Dolle G, Meunier H, Bednarek N, Fablet R, Passat N, Rousseau F. SegSRGAN: super-resolution and segmentation using generative adversarial networks - application to neonatal brain MRI. Comput Biol Med. 2020;120:103755.CrossRef
10.
go back to reference Hagiwara A, Otsuka Y, Hori M, Tachibana Y, Yokoyama K, Fujita S, Andica C, Kamagata K, Irie R, Koshino S, et al. Improving the quality of synthetic FLAIR images with deep learning using a conditional generative adversarial network for pixel-by-pixel image translation. AJNR Am J Neuroradiol. 2019;40(2):224–30.CrossRef Hagiwara A, Otsuka Y, Hori M, Tachibana Y, Yokoyama K, Fujita S, Andica C, Kamagata K, Irie R, Koshino S, et al. Improving the quality of synthetic FLAIR images with deep learning using a conditional generative adversarial network for pixel-by-pixel image translation. AJNR Am J Neuroradiol. 2019;40(2):224–30.CrossRef
11.
go back to reference Kim KH, Do WJ, Park SH. Improving resolution of MR images with an adversarial network incorporating images with different contrast. Med Phys. 2018;45(7):3120–31.CrossRef Kim KH, Do WJ, Park SH. Improving resolution of MR images with an adversarial network incorporating images with different contrast. Med Phys. 2018;45(7):3120–31.CrossRef
12.
go back to reference Fahimi F, Dosen S, Ang KK, Mrachacz-Kersting N, Guan C. Generative adversarial networks-based data augmentation for brain-computer Interface. IEEE Trans Neural Netw Learn Syst. 2020. Fahimi F, Dosen S, Ang KK, Mrachacz-Kersting N, Guan C. Generative adversarial networks-based data augmentation for brain-computer Interface. IEEE Trans Neural Netw Learn Syst. 2020.
13.
go back to reference Li Q, Yu Z, Wang Y, Zheng H. TumorGAN: A multi-modal data augmentation framework for brain tumor segmentation. Sensors (Basel). 2020;20(15):4203. Li Q, Yu Z, Wang Y, Zheng H. TumorGAN: A multi-modal data augmentation framework for brain tumor segmentation. Sensors (Basel). 2020;20(15):4203.
14.
go back to reference Wu W, Lu Y, Mane R, Guan C. Deep learning for neuroimaging segmentation with a novel data augmentation strategy. Annu Int Conf IEEE Eng Med Biol Soc. 2020;2020:1516–9.PubMed Wu W, Lu Y, Mane R, Guan C. Deep learning for neuroimaging segmentation with a novel data augmentation strategy. Annu Int Conf IEEE Eng Med Biol Soc. 2020;2020:1516–9.PubMed
15.
go back to reference Shi Y, Cheng K, Liu Z. Hippocampal subfields segmentation in brain MR images using generative adversarial networks. Biomed Eng Online. 2019;18(1):5.CrossRef Shi Y, Cheng K, Liu Z. Hippocampal subfields segmentation in brain MR images using generative adversarial networks. Biomed Eng Online. 2019;18(1):5.CrossRef
16.
go back to reference Hamghalam M, Wang T, Lei B. High tissue contrast image synthesis via multistage attention-GAN: application to segmenting brain MR scans. Neural Netw. 2020;132:43–52.CrossRef Hamghalam M, Wang T, Lei B. High tissue contrast image synthesis via multistage attention-GAN: application to segmenting brain MR scans. Neural Netw. 2020;132:43–52.CrossRef
17.
go back to reference Shaul R, David I, Shitrit O, Riklin Raviv T. Subsampled brain MRI reconstruction by generative adversarial neural networks. Med Image Anal. 2020;65:101747.CrossRef Shaul R, David I, Shitrit O, Riklin Raviv T. Subsampled brain MRI reconstruction by generative adversarial neural networks. Med Image Anal. 2020;65:101747.CrossRef
18.
go back to reference Do WJ, Seo S, Han Y, Ye JC, Choi SH, Park SH. Reconstruction of multicontrast MR images through deep learning. Med Phys. 2020;47(3):983–97.CrossRef Do WJ, Seo S, Han Y, Ye JC, Choi SH, Park SH. Reconstruction of multicontrast MR images through deep learning. Med Phys. 2020;47(3):983–97.CrossRef
19.
go back to reference Quan TM, Nguyen-Duc T, Jeong WK. Compressed sensing MRI reconstruction using a generative adversarial network with a cyclic loss. IEEE Trans Med Imaging. 2018;37(6):1488–97.CrossRef Quan TM, Nguyen-Duc T, Jeong WK. Compressed sensing MRI reconstruction using a generative adversarial network with a cyclic loss. IEEE Trans Med Imaging. 2018;37(6):1488–97.CrossRef
20.
go back to reference Yang G, Yu S, Dong H, Slabaugh G, Dragotti PL, Ye X, Liu F, Arridge S, Keegan J, Guo Y, et al. DAGAN: deep De-aliasing generative adversarial networks for fast compressed sensing MRI reconstruction. IEEE Trans Med Imaging. 2018;37(6):1310–21.CrossRef Yang G, Yu S, Dong H, Slabaugh G, Dragotti PL, Ye X, Liu F, Arridge S, Keegan J, Guo Y, et al. DAGAN: deep De-aliasing generative adversarial networks for fast compressed sensing MRI reconstruction. IEEE Trans Med Imaging. 2018;37(6):1310–21.CrossRef
21.
go back to reference Lei Y, Harms J, Wang T, Liu Y, Shu HK, Jani AB, Curran WJ, Mao H, Liu T, Yang X. MRI-only based synthetic CT generation using dense cycle consistent generative adversarial networks. Med Phys. 2019;46(8):3565–81.CrossRef Lei Y, Harms J, Wang T, Liu Y, Shu HK, Jani AB, Curran WJ, Mao H, Liu T, Yang X. MRI-only based synthetic CT generation using dense cycle consistent generative adversarial networks. Med Phys. 2019;46(8):3565–81.CrossRef
22.
go back to reference Nie D, Trullo R, Lian J, Petitjean C, Ruan S, Wang Q, Shen D. Medical image synthesis with context-aware generative adversarial networks. In: Medical Image Computing and Computer Assisted Intervention − MICCAI 2017. edn; 2017. p. 417–25.CrossRef Nie D, Trullo R, Lian J, Petitjean C, Ruan S, Wang Q, Shen D. Medical image synthesis with context-aware generative adversarial networks. In: Medical Image Computing and Computer Assisted Intervention − MICCAI 2017. edn; 2017. p. 417–25.CrossRef
23.
go back to reference Yang Q, Li N, Zhao Z, Fan X, Chang EI, Xu Y. MRI cross-modality image-to-image translation. Sci Rep. 2020;10(1):3753.CrossRef Yang Q, Li N, Zhao Z, Fan X, Chang EI, Xu Y. MRI cross-modality image-to-image translation. Sci Rep. 2020;10(1):3753.CrossRef
24.
go back to reference Uzunova H, Ehrhardt J, Handels H. Memory-efficient GAN-based domain translation of high resolution 3D medical images. Comput Med Imaging Graph. 2020;86:101801.CrossRef Uzunova H, Ehrhardt J, Handels H. Memory-efficient GAN-based domain translation of high resolution 3D medical images. Comput Med Imaging Graph. 2020;86:101801.CrossRef
25.
go back to reference Shiyam Sundar LK, Iommi D, Muzik O, Chalampalakis Z, Klebermass EM, Hienert M, Rischka L, Lanzenberger R, Hahn A, Pataraia E, et al. Conditional Generative Adversarial Networks (cGANs) aided motion correction of dynamic (18) F-FDG PET brain studies. J Nucl Med. 2020. Shiyam Sundar LK, Iommi D, Muzik O, Chalampalakis Z, Klebermass EM, Hienert M, Rischka L, Lanzenberger R, Hahn A, Pataraia E, et al. Conditional Generative Adversarial Networks (cGANs) aided motion correction of dynamic (18) F-FDG PET brain studies. J Nucl Med. 2020.
26.
go back to reference Johnson PM, Drangova M. Conditional generative adversarial network for 3D rigid-body motion correction in MRI. Magn Reson Med. 2019;82(3):901–10.PubMed Johnson PM, Drangova M. Conditional generative adversarial network for 3D rigid-body motion correction in MRI. Magn Reson Med. 2019;82(3):901–10.PubMed
27.
go back to reference Nagasawa T, Sato T, Nambu I, Wada Y. fNIRS-GANs: data augmentation using generative adversarial networks for classifying motor tasks from functional near-infrared spectroscopy. J Neural Eng. 2020;17(1):016068.CrossRef Nagasawa T, Sato T, Nambu I, Wada Y. fNIRS-GANs: data augmentation using generative adversarial networks for classifying motor tasks from functional near-infrared spectroscopy. J Neural Eng. 2020;17(1):016068.CrossRef
28.
go back to reference Petersen RC, Aisen PS, Beckett LA, Donohue MC, Gamst AC, Harvey DJ, Jack CR Jr, Jagust WJ, Shaw LM, Toga AW, et al. Alzheimer’s Disease Neuroimaging Initiative (ADNI): clinical characterization. Neurology. 2010;74(3):201–9.CrossRef Petersen RC, Aisen PS, Beckett LA, Donohue MC, Gamst AC, Harvey DJ, Jack CR Jr, Jagust WJ, Shaw LM, Toga AW, et al. Alzheimer’s Disease Neuroimaging Initiative (ADNI): clinical characterization. Neurology. 2010;74(3):201–9.CrossRef
29.
go back to reference Beekly DL, Ramos EM, van Belle G, Deitrich W, Clark AD, Jacka ME, Kukull WA, Centers NI-AsD: The National Alzheimer’s Coordinating Center (NACC) database: an Alzheimer disease database. Alzheimer Dis Assoc Disord 2004, 18(4):270–277. Beekly DL, Ramos EM, van Belle G, Deitrich W, Clark AD, Jacka ME, Kukull WA, Centers NI-AsD: The National Alzheimer’s Coordinating Center (NACC) database: an Alzheimer disease database. Alzheimer Dis Assoc Disord 2004, 18(4):270–277.
30.
go back to reference McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM. Clinical diagnosis of Alzheimer’s disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's disease. Neurology. 1984;34(7):939–44.CrossRef McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM. Clinical diagnosis of Alzheimer’s disease: report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's disease. Neurology. 1984;34(7):939–44.CrossRef
31.
go back to reference Qiu S, Joshi PS, Miller MI, Xue C, Zhou X, Karjadi C, Chang GH, Joshi AS, Dwyer B, Zhu S, et al. Development and validation of an interpretable deep learning framework for Alzheimer's disease classification. Brain. 2020;143(6):1920–33.CrossRef Qiu S, Joshi PS, Miller MI, Xue C, Zhou X, Karjadi C, Chang GH, Joshi AS, Dwyer B, Zhu S, et al. Development and validation of an interpretable deep learning framework for Alzheimer's disease classification. Brain. 2020;143(6):1920–33.CrossRef
32.
go back to reference Mittal A, Moorthy AK, Bovik AC. No-reference image quality assessment in the spatial domain. Ieee T Image Process. 2012;21(12):4695–708.CrossRef Mittal A, Moorthy AK, Bovik AC. No-reference image quality assessment in the spatial domain. Ieee T Image Process. 2012;21(12):4695–708.CrossRef
33.
go back to reference Mittal A, Soundararajan R, Bovik AC. Making a “completely blind” image quality analyzer. Ieee Signal Proc Let. 2013;20(3):209–12.CrossRef Mittal A, Soundararajan R, Bovik AC. Making a “completely blind” image quality analyzer. Ieee Signal Proc Let. 2013;20(3):209–12.CrossRef
34.
go back to reference Sheikh HR, Sabir MF, Bovik AC. A statistical evaluation of recent full reference image quality assessment algorithms. IEEE Trans Image Process. 2006;15(11):3440–51.CrossRef Sheikh HR, Sabir MF, Bovik AC. A statistical evaluation of recent full reference image quality assessment algorithms. IEEE Trans Image Process. 2006;15(11):3440–51.CrossRef
35.
go back to reference Wang Z, Bovik AC, Sheikh HR, Simoncelli EP. Image quality assessment: from error visibility to structural similarity. IEEE Trans Image Process. 2004;13(4):600–12.CrossRef Wang Z, Bovik AC, Sheikh HR, Simoncelli EP. Image quality assessment: from error visibility to structural similarity. IEEE Trans Image Process. 2004;13(4):600–12.CrossRef
36.
go back to reference Vina J, Sanz-Ros J. Alzheimer’s disease: only prevention makes sense. Eur J Clin Investig. 2018;48(10):e13005.CrossRef Vina J, Sanz-Ros J. Alzheimer’s disease: only prevention makes sense. Eur J Clin Investig. 2018;48(10):e13005.CrossRef
37.
go back to reference Cummings J, Ritter A, Zhong K. Clinical trials for disease-modifying therapies in Alzheimer’s disease: a primer, lessons learned, and a blueprint for the future. J Alzheimers Dis. 2018;64(s1):S3–S22.CrossRef Cummings J, Ritter A, Zhong K. Clinical trials for disease-modifying therapies in Alzheimer’s disease: a primer, lessons learned, and a blueprint for the future. J Alzheimers Dis. 2018;64(s1):S3–S22.CrossRef
Metadata
Title
Enhancing magnetic resonance imaging-driven Alzheimer’s disease classification performance using generative adversarial learning
Authors
Xiao Zhou
Shangran Qiu
Prajakta S. Joshi
Chonghua Xue
Ronald J. Killiany
Asim Z. Mian
Sang P. Chin
Rhoda Au
Vijaya B. Kolachalama
Publication date
01-12-2021
Publisher
BioMed Central
Published in
Alzheimer's Research & Therapy / Issue 1/2021
Electronic ISSN: 1758-9193
DOI
https://doi.org/10.1186/s13195-021-00797-5

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