Skip to main content
Top
Published in: Brain Structure and Function 6/2021

01-07-2021 | Original Article

Mapping fetal brain development based on automated segmentation and 4D brain atlasing

Authors: Haotian Li, Guohui Yan, Wanrong Luo, Tingting Liu, Yan Wang, Ruibin Liu, Weihao Zheng, Yi Zhang, Kui Li, Li Zhao, Catherine Limperopoulos, Yu Zou, Dan Wu

Published in: Brain Structure and Function | Issue 6/2021

Login to get access

Abstract

Fetal brain MRI has become an important tool for in utero assessment of brain development and disorders. However, quantitative analysis of fetal brain MRI remains difficult, partially due to the limited tools for automated preprocessing and the lack of normative brain templates. In this paper, we proposed an automated pipeline for fetal brain extraction, super-resolution reconstruction, and fetal brain atlasing to quantitatively map in utero fetal brain development during mid-to-late gestation in a Chinese population. First, we designed a U-net convolutional neural network for automated fetal brain extraction, which achieved an average accuracy of 97%. We then generated a developing fetal brain atlas, using an iterative linear and nonlinear registration approach. Based on the 4D spatiotemporal atlas, we quantified the morphological development of the fetal brain between 23 and 36 weeks of gestation. The proposed pipeline enabled the fully automated volumetric reconstruction for clinically available fetal brain MRI data, and the 4D fetal brain atlas provided normative templates for the quantitative characterization of fetal brain development, especially in the Chinese population.
Appendix
Available only for authorised users
Literature
go back to reference Alexander B, Murray AL, Loh WY, Matthews LG, Adamson C, Beare R, Chen J, Kelly CE, Rees S, Warfield SK (2017) A new neonatal cortical and subcortical brain atlas: the Melbourne Children’s Regional Infant Brain (M-CRIB) atlas. Neuroimage 147:841–851PubMedCrossRef Alexander B, Murray AL, Loh WY, Matthews LG, Adamson C, Beare R, Chen J, Kelly CE, Rees S, Warfield SK (2017) A new neonatal cortical and subcortical brain atlas: the Melbourne Children’s Regional Infant Brain (M-CRIB) atlas. Neuroimage 147:841–851PubMedCrossRef
go back to reference Avants BB, Epstein CL, Grossman M, Gee JC (2008) Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med Image Anal 12(1):26–41PubMedCrossRef Avants BB, Epstein CL, Grossman M, Gee JC (2008) Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med Image Anal 12(1):26–41PubMedCrossRef
go back to reference Bendersky M, Musolino PL, Rugilo C, Schuster G, Sica RE (2006) Normal anatomy of the developing fetal brain Ex vivo anatomical–magnetic resonance imaging correlation. J Neurol Sci 250(1–2):20–26PubMedCrossRef Bendersky M, Musolino PL, Rugilo C, Schuster G, Sica RE (2006) Normal anatomy of the developing fetal brain Ex vivo anatomical–magnetic resonance imaging correlation. J Neurol Sci 250(1–2):20–26PubMedCrossRef
go back to reference Breu M, Reisinger D, Wu D, Zhang Y, Fatemi A, Zhang J (2013) In vivo diffusion tensor imaging of the neonatal rat brain development. Neuropediatrics 44(S01):A11 Breu M, Reisinger D, Wu D, Zhang Y, Fatemi A, Zhang J (2013) In vivo diffusion tensor imaging of the neonatal rat brain development. Neuropediatrics 44(S01):A11
go back to reference Chartier AL, Bouvier MJ, McPherson DR, Stepenosky JE, Taysom DA, Marks RM (2019) The safety of maternal and fetal MRI at 3 T. Am J Roentgenol 213(5):1170–1173CrossRef Chartier AL, Bouvier MJ, McPherson DR, Stepenosky JE, Taysom DA, Marks RM (2019) The safety of maternal and fetal MRI at 3 T. Am J Roentgenol 213(5):1170–1173CrossRef
go back to reference Chee MW, Chen KH, Zheng H, Chan KP, Isaac V, Sim SK, Chuah LY, Schuchinsky M, Fischl B, Ng TP (2009) Cognitive function and brain structure correlations in healthy elderly East Asians. Neuroimage 46(1):257–269PubMedCrossRef Chee MW, Chen KH, Zheng H, Chan KP, Isaac V, Sim SK, Chuah LY, Schuchinsky M, Fischl B, Ng TP (2009) Cognitive function and brain structure correlations in healthy elderly East Asians. Neuroimage 46(1):257–269PubMedCrossRef
go back to reference Cox RW (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29(3):162–173PubMedCrossRef Cox RW (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29(3):162–173PubMedCrossRef
go back to reference Ebner M, Chung KK, Prados F, Cardoso MJ, Chard DT, Vercauteren T, Ourselin S (2018a) Volumetric reconstruction from printed films: enabling 30 year longitudinal analysis in MR neuroimaging. NeuroImage 165:238–250PubMedPubMedCentralCrossRef Ebner M, Chung KK, Prados F, Cardoso MJ, Chard DT, Vercauteren T, Ourselin S (2018a) Volumetric reconstruction from printed films: enabling 30 year longitudinal analysis in MR neuroimaging. NeuroImage 165:238–250PubMedPubMedCentralCrossRef
go back to reference Ebner M, Wang G, Li W, Aertsen M, Patel PA, Aughwane R, Melbourne A, Doel T, David AL, Deprest J (2018b) An automated localization, segmentation and reconstruction framework for fetal brain MRI. International conference on medical image computing and computer-assisted intervention. Springer, pp 313–320 Ebner M, Wang G, Li W, Aertsen M, Patel PA, Aughwane R, Melbourne A, Doel T, David AL, Deprest J (2018b) An automated localization, segmentation and reconstruction framework for fetal brain MRI. International conference on medical image computing and computer-assisted intervention. Springer, pp 313–320
go back to reference Ebner M, Wang G, Li W, Aertsen M, Patel PA, Aughwane R, Melbourne A, Doel T, Dymarkowski S, De Coppi P (2020) An automated framework for localization, segmentation and super-resolution reconstruction of fetal brain MRI. NeuroImage 206:116324PubMedPubMedCentralCrossRef Ebner M, Wang G, Li W, Aertsen M, Patel PA, Aughwane R, Melbourne A, Doel T, Dymarkowski S, De Coppi P (2020) An automated framework for localization, segmentation and super-resolution reconstruction of fetal brain MRI. NeuroImage 206:116324PubMedPubMedCentralCrossRef
go back to reference Fogliarini C, Chaumoitre K, Chapon F, Fernandez C, Lévrier O, Figarella-Branger D, Girard N (2005) Assessment of cortical maturation with prenatal MRI. Part I: Normal Cortical Matur 15(8):1671–1685 Fogliarini C, Chaumoitre K, Chapon F, Fernandez C, Lévrier O, Figarella-Branger D, Girard N (2005) Assessment of cortical maturation with prenatal MRI. Part I: Normal Cortical Matur 15(8):1671–1685
go back to reference Garel C, Chantrel E, Brisse H, Elmaleh M, Luton D, Oury J-F, Sebag G, Hassan M (2001) Fetal cerebral cortex: normal gestational landmarks identified using prenatal MR imaging. Am J Neuroradiol 22(1):184–189PubMed Garel C, Chantrel E, Brisse H, Elmaleh M, Luton D, Oury J-F, Sebag G, Hassan M (2001) Fetal cerebral cortex: normal gestational landmarks identified using prenatal MR imaging. Am J Neuroradiol 22(1):184–189PubMed
go back to reference Garel C, Chantrel E, Elmaleh M, Brisse H, Sebag G (2003) Fetal MRI: normal gestational landmarks for cerebral biometry, gyration and myelination. Childs Nerv Syst 19(7–8):422–425PubMedCrossRef Garel C, Chantrel E, Elmaleh M, Brisse H, Sebag G (2003) Fetal MRI: normal gestational landmarks for cerebral biometry, gyration and myelination. Childs Nerv Syst 19(7–8):422–425PubMedCrossRef
go back to reference Gholipour A, Estroff JA, Warfield SK (2010) Robust super-resolution volume reconstruction from slice acquisitions: application to fetal brain MRI. IEEE Trans Med Imaging 29(10):1739–1758PubMedPubMedCentralCrossRef Gholipour A, Estroff JA, Warfield SK (2010) Robust super-resolution volume reconstruction from slice acquisitions: application to fetal brain MRI. IEEE Trans Med Imaging 29(10):1739–1758PubMedPubMedCentralCrossRef
go back to reference Gholipour A, Limperopoulos C, Clancy S, Clouchoux C, Akhondi-Asl A, Estroff JA, Warfield SK (2014) Construction of a deformable spatiotemporal MRI atlas of the fetal brain: evaluation of similarity metrics and deformation models. International conference on medical image computing and computer-assisted intervention. Springer, pp 292–299 Gholipour A, Limperopoulos C, Clancy S, Clouchoux C, Akhondi-Asl A, Estroff JA, Warfield SK (2014) Construction of a deformable spatiotemporal MRI atlas of the fetal brain: evaluation of similarity metrics and deformation models. International conference on medical image computing and computer-assisted intervention. Springer, pp 292–299
go back to reference Gholipour A, Rollins CK, Velasco-Annis C, Ouaalam A, Akhondi-Asl A, Afacan O, Ortinau CM, Clancy S, Limperopoulos C, Yang E (2017) A normative spatiotemporal MRI atlas of the fetal brain for automatic segmentation and analysis of early brain growth. Sci Rep 7(1):476PubMedPubMedCentralCrossRef Gholipour A, Rollins CK, Velasco-Annis C, Ouaalam A, Akhondi-Asl A, Afacan O, Ortinau CM, Clancy S, Limperopoulos C, Yang E (2017) A normative spatiotemporal MRI atlas of the fetal brain for automatic segmentation and analysis of early brain growth. Sci Rep 7(1):476PubMedPubMedCentralCrossRef
go back to reference Gousias IS, Edwards AD, Rutherford MA, Counsell SJ, Hajnal JV, Rueckert D, Hammers A (2012) Magnetic resonance imaging of the newborn brain: manual segmentation of labelled atlases in term-born and preterm infants. Neuroimage 62(3):1499–1509PubMedCrossRef Gousias IS, Edwards AD, Rutherford MA, Counsell SJ, Hajnal JV, Rueckert D, Hammers A (2012) Magnetic resonance imaging of the newborn brain: manual segmentation of labelled atlases in term-born and preterm infants. Neuroimage 62(3):1499–1509PubMedCrossRef
go back to reference Griffiths PD, Bradburn M, Campbell MJ, Cooper CL, Graham R, Jarvis D, Kilby MD, Mason G, Mooney C, Robson SC (2017) Use of MRI in the diagnosis of fetal brain abnormalities in utero (MERIDIAN): a multicentre, prospective cohort study. Lancet 389(10068):538–546PubMedCrossRef Griffiths PD, Bradburn M, Campbell MJ, Cooper CL, Graham R, Jarvis D, Kilby MD, Mason G, Mooney C, Robson SC (2017) Use of MRI in the diagnosis of fetal brain abnormalities in utero (MERIDIAN): a multicentre, prospective cohort study. Lancet 389(10068):538–546PubMedCrossRef
go back to reference Habas PA, Kim K, Corbett-Detig JM, Rousseau F, Glenn OA, Barkovich AJ, Studholme C (2010) A spatiotemporal atlas of MR intensity, tissue probability and shape of the fetal brain with application to segmentation. Neuroimage 53(2):460–470PubMedPubMedCentralCrossRef Habas PA, Kim K, Corbett-Detig JM, Rousseau F, Glenn OA, Barkovich AJ, Studholme C (2010) A spatiotemporal atlas of MR intensity, tissue probability and shape of the fetal brain with application to segmentation. Neuroimage 53(2):460–470PubMedPubMedCentralCrossRef
go back to reference Iglesias JE, Liu C-Y, Thompson PM, Tu Z (2011) Robust brain extraction across datasets and comparison with publicly available methods. IEEE Trans Med Imaging 30(9):1617–1634PubMedCrossRef Iglesias JE, Liu C-Y, Thompson PM, Tu Z (2011) Robust brain extraction across datasets and comparison with publicly available methods. IEEE Trans Med Imaging 30(9):1617–1634PubMedCrossRef
go back to reference Jarvis DA, Griffiths PD (2019) Current state of MRI of the fetal brain in utero. J Magn Reson Imaging 49(3):632–646PubMedCrossRef Jarvis DA, Griffiths PD (2019) Current state of MRI of the fetal brain in utero. J Magn Reson Imaging 49(3):632–646PubMedCrossRef
go back to reference Jenkinson M, Pechaud M, Smith S (2005) BET2: MR-based estimation of brain, skull and scalp surfaces. In: Eleventh annual meeting of the organization for human brain mapping, vol 17, pp 167 Jenkinson M, Pechaud M, Smith S (2005) BET2: MR-based estimation of brain, skull and scalp surfaces. In: Eleventh annual meeting of the organization for human brain mapping, vol 17, pp 167
go back to reference Jiang S, Xue H, Glover A, Rutherford M, Rueckert D, Hajnal JV (2007) MRI of moving subjects using multislice snapshot images with volume reconstruction (SVR): application to fetal, neonatal, and adult brain studies. IEEE Trans Med Imaging 26(7):967–980PubMedCrossRef Jiang S, Xue H, Glover A, Rutherford M, Rueckert D, Hajnal JV (2007) MRI of moving subjects using multislice snapshot images with volume reconstruction (SVR): application to fetal, neonatal, and adult brain studies. IEEE Trans Med Imaging 26(7):967–980PubMedCrossRef
go back to reference Kainz B, Steinberger M, Wein W, Kuklisova-Murgasova M, Malamateniou C, Keraudren K, Torsney-Weir T, Rutherford M, Aljabar P, Hajnal JV (2015) Fast volume reconstruction from motion corrupted stacks of 2D slices. IEEE Trans Med Imaging 34(9):1901–1913PubMedPubMedCentralCrossRef Kainz B, Steinberger M, Wein W, Kuklisova-Murgasova M, Malamateniou C, Keraudren K, Torsney-Weir T, Rutherford M, Aljabar P, Hajnal JV (2015) Fast volume reconstruction from motion corrupted stacks of 2D slices. IEEE Trans Med Imaging 34(9):1901–1913PubMedPubMedCentralCrossRef
go back to reference Khalili N, Lessmann N, Turk E, Claessens N, de Heus R, Kolk T, Viergever M, Benders M, Išgum I (2019) Automatic brain tissue segmentation in fetal MRI using convolutional neural networks. Mag Reson Imaging 64(77):89 Khalili N, Lessmann N, Turk E, Claessens N, de Heus R, Kolk T, Viergever M, Benders M, Išgum I (2019) Automatic brain tissue segmentation in fetal MRI using convolutional neural networks. Mag Reson Imaging 64(77):89
go back to reference Khan S, Vasung L, Marami B, Rollins CK, Afacan O, Ortinau CM, Yang E, Warfield SK, Gholipour A (2019) Fetal brain growth portrayed by a spatiotemporal diffusion tensor MRI atlas computed from in utero images. Neuroimage 185:593–608PubMedCrossRef Khan S, Vasung L, Marami B, Rollins CK, Afacan O, Ortinau CM, Yang E, Warfield SK, Gholipour A (2019) Fetal brain growth portrayed by a spatiotemporal diffusion tensor MRI atlas computed from in utero images. Neuroimage 185:593–608PubMedCrossRef
go back to reference Kleesiek J, Urban G, Hubert A, Schwarz D, Maier-Hein K, Bendszus M, Biller A (2016) Deep MRI brain extraction: a 3D convolutional neural network for skull stripping. Neuroimage 129:460–469PubMedCrossRef Kleesiek J, Urban G, Hubert A, Schwarz D, Maier-Hein K, Bendszus M, Biller A (2016) Deep MRI brain extraction: a 3D convolutional neural network for skull stripping. Neuroimage 129:460–469PubMedCrossRef
go back to reference Klein A, Andersson J, Ardekani BA, Ashburner J, Avants B, Chiang M-C, Christensen GE, Collins DL, Gee J, Hellier P (2009) Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration. Neuroimage 46(3):786–802PubMedPubMedCentralCrossRef Klein A, Andersson J, Ardekani BA, Ashburner J, Avants B, Chiang M-C, Christensen GE, Collins DL, Gee J, Hellier P (2009) Evaluation of 14 nonlinear deformation algorithms applied to human brain MRI registration. Neuroimage 46(3):786–802PubMedPubMedCentralCrossRef
go back to reference Kochunov P, Castro C, Davis D, Dudley D, Brewer J, Zhang Y, Kroenke CD, Purdy D, Fox PT, Simerly C (2010) Mapping primary gyrogenesis during fetal development in primate brains: high-resolution in utero structural MRI study of fetal brain development in pregnant baboons. Front Neurosci 4:20PubMedPubMedCentral Kochunov P, Castro C, Davis D, Dudley D, Brewer J, Zhang Y, Kroenke CD, Purdy D, Fox PT, Simerly C (2010) Mapping primary gyrogenesis during fetal development in primate brains: high-resolution in utero structural MRI study of fetal brain development in pregnant baboons. Front Neurosci 4:20PubMedPubMedCentral
go back to reference Kuklisova-Murgasova M, Quaghebeur G, Rutherford MA, Hajnal JV, Schnabel JA (2012) Reconstruction of fetal brain MRI with intensity matching and complete outlier removal. Med Image Anal 16(8):1550–1564PubMedPubMedCentralCrossRef Kuklisova-Murgasova M, Quaghebeur G, Rutherford MA, Hajnal JV, Schnabel JA (2012) Reconstruction of fetal brain MRI with intensity matching and complete outlier removal. Med Image Anal 16(8):1550–1564PubMedPubMedCentralCrossRef
go back to reference Lee JS, Lee DS, Kim J, Kim YK, Kang E, Kang H, Kang KW, Lee JM, Kim J-J, Park H-J (2005) Development of Korean standard brain templates. J Korean Med Sci 20(3):483–488PubMedPubMedCentralCrossRef Lee JS, Lee DS, Kim J, Kim YK, Kang E, Kang H, Kang KW, Lee JM, Kim J-J, Park H-J (2005) Development of Korean standard brain templates. J Korean Med Sci 20(3):483–488PubMedPubMedCentralCrossRef
go back to reference Liang P, Shi L, Chen N, Luo Y, Wang X, Liu K, Mok VC, Chu WC, Wang D, Li K (2015) Construction of brain atlases based on a multi-center MRI dataset of 2020 Chinese adults. Sci Rep 5:18216PubMedPubMedCentralCrossRef Liang P, Shi L, Chen N, Luo Y, Wang X, Liu K, Mok VC, Chu WC, Wang D, Li K (2015) Construction of brain atlases based on a multi-center MRI dataset of 2020 Chinese adults. Sci Rep 5:18216PubMedPubMedCentralCrossRef
go back to reference Lin G, Adiga U, Olson K, Guzowski JF, Barnes CA, Roysam B (2003) A hybrid 3D watershed algorithm incorporating gradient cues and object models for automatic segmentation of nuclei in confocal image stacks. Cytom Part A: J Int Soc Anal Cytol 56(1):23–36CrossRef Lin G, Adiga U, Olson K, Guzowski JF, Barnes CA, Roysam B (2003) A hybrid 3D watershed algorithm incorporating gradient cues and object models for automatic segmentation of nuclei in confocal image stacks. Cytom Part A: J Int Soc Anal Cytol 56(1):23–36CrossRef
go back to reference Makropoulos A, Gousias IS, Ledig C, Aljabar P, Serag A, Hajnal JV, Edwards AD, Counsell SJ, Rueckert D (2014) Automatic whole brain MRI segmentation of the developing neonatal brain. IEEE Trans Med Imaging 33(9):1818–1831PubMedCrossRef Makropoulos A, Gousias IS, Ledig C, Aljabar P, Serag A, Hajnal JV, Edwards AD, Counsell SJ, Rueckert D (2014) Automatic whole brain MRI segmentation of the developing neonatal brain. IEEE Trans Med Imaging 33(9):1818–1831PubMedCrossRef
go back to reference Makropoulos A, Aljabar P, Wright R, Hüning B, Merchant N, Arichi T, Tusor N, Hajnal JV, Edwards AD, Counsell SJ (2016) Regional growth and atlasing of the developing human brain. Neuroimage 125:456–478PubMedPubMedCentralCrossRef Makropoulos A, Aljabar P, Wright R, Hüning B, Merchant N, Arichi T, Tusor N, Hajnal JV, Edwards AD, Counsell SJ (2016) Regional growth and atlasing of the developing human brain. Neuroimage 125:456–478PubMedPubMedCentralCrossRef
go back to reference Makropoulos A, Counsell SJ, Rueckert D (2018) A review on automatic fetal and neonatal brain MRI segmentation. Neuroimage 170:231–248PubMedCrossRef Makropoulos A, Counsell SJ, Rueckert D (2018) A review on automatic fetal and neonatal brain MRI segmentation. Neuroimage 170:231–248PubMedCrossRef
go back to reference Monteagudo A, Timor-Tritsch I (1997) Development of fetal gyri, sulci and fissures: a transvaginal sonographic study. Ultrasound Obstet Gynecol: off J Int Soc Ultrasound Obstet Gynecol 9(4):222–228CrossRef Monteagudo A, Timor-Tritsch I (1997) Development of fetal gyri, sulci and fissures: a transvaginal sonographic study. Ultrasound Obstet Gynecol: off J Int Soc Ultrasound Obstet Gynecol 9(4):222–228CrossRef
go back to reference Nielsen BW, Scott RC (2017) Brain abnormalities in fetuses: in-utero MRI versus ultrasound. Lancet 389(10068):483–485PubMedCrossRef Nielsen BW, Scott RC (2017) Brain abnormalities in fetuses: in-utero MRI versus ultrasound. Lancet 389(10068):483–485PubMedCrossRef
go back to reference Ou Y, Akbari H, Bilello M, Da X, Davatzikos C (2014) Comparative evaluation of registration algorithms in different brain databases with varying difficulty: results and insights. IEEE Trans Med Imaging 33(10):2039–2065PubMedPubMedCentralCrossRef Ou Y, Akbari H, Bilello M, Da X, Davatzikos C (2014) Comparative evaluation of registration algorithms in different brain databases with varying difficulty: results and insights. IEEE Trans Med Imaging 33(10):2039–2065PubMedPubMedCentralCrossRef
go back to reference Rao NP, Jeelani H, Achalia R, Achalia G, Jacob A, dawn Bharath R, Varambally S, Venkatasubramanian G, Yalavarthy PK (2017) Population differences in brain morphology: Need for population specific brain template. Psychiatr Res: Neuroimaging 265:1–8CrossRef Rao NP, Jeelani H, Achalia R, Achalia G, Jacob A, dawn Bharath R, Varambally S, Venkatasubramanian G, Yalavarthy PK (2017) Population differences in brain morphology: Need for population specific brain template. Psychiatr Res: Neuroimaging 265:1–8CrossRef
go back to reference Rolo LC, Araujo E, Nardozza LMM, de Oliveira PS, Ajzen SA, Moron AF (2011) Development of fetal brain sulci and gyri: assessment through two and three-dimensional ultrasound and magnetic resonance imaging. Arch Gynecol Obstet 283(2):149–158PubMedCrossRef Rolo LC, Araujo E, Nardozza LMM, de Oliveira PS, Ajzen SA, Moron AF (2011) Development of fetal brain sulci and gyri: assessment through two and three-dimensional ultrasound and magnetic resonance imaging. Arch Gynecol Obstet 283(2):149–158PubMedCrossRef
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, pp 234–241 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, pp 234–241
go back to reference Rousseau F, Glenn OA, Iordanova B, Rodriguez-Carranza C, Vigneron DB, Barkovich JA, Studholme C (2006) Registration-based approach for reconstruction of high-resolution in utero fetal MR brain images. Acad Radiol 13(9):1072–1081PubMedCrossRef Rousseau F, Glenn OA, Iordanova B, Rodriguez-Carranza C, Vigneron DB, Barkovich JA, Studholme C (2006) Registration-based approach for reconstruction of high-resolution in utero fetal MR brain images. Acad Radiol 13(9):1072–1081PubMedCrossRef
go back to reference Rousseau F, Kim K, Studholme C, Koob M, Dietemann J-L (2010) On super-resolution for fetal brain MRI. International conference on medical image computing and computer-assisted intervention. Springer, pp 355–362 Rousseau F, Kim K, Studholme C, Koob M, Dietemann J-L (2010) On super-resolution for fetal brain MRI. International conference on medical image computing and computer-assisted intervention. Springer, pp 355–362
go back to reference Rousseau F, Oubel E, Pontabry J, Schweitzer M, Studholme C, Koob M, Dietemann J-L (2013) BTK: An open-source toolkit for fetal brain MR image processing. Comput Methods Programs Biomed 109(1):65–73PubMedCrossRef Rousseau F, Oubel E, Pontabry J, Schweitzer M, Studholme C, Koob M, Dietemann J-L (2013) BTK: An open-source toolkit for fetal brain MR image processing. Comput Methods Programs Biomed 109(1):65–73PubMedCrossRef
go back to reference Salehi SSM, Erdogmus D, Gholipour A (2017) Auto-context convolutional neural network (auto-net) for brain extraction in magnetic resonance imaging. IEEE Trans Med Imaging 36(11):2319–2330PubMedCentralCrossRef Salehi SSM, Erdogmus D, Gholipour A (2017) Auto-context convolutional neural network (auto-net) for brain extraction in magnetic resonance imaging. IEEE Trans Med Imaging 36(11):2319–2330PubMedCentralCrossRef
go back to reference Schuh A, Murgasova M, Makropoulos A, Ledig C, Counsell SJ, Hajnal JV, Aljabar P, Rueckert D (2014) Construction of a 4D brain atlas and growth model using diffeomorphic registration. International workshop on spatio-temporal image analysis for longitudinal and time-series image data. Springer, pp 27–37 Schuh A, Murgasova M, Makropoulos A, Ledig C, Counsell SJ, Hajnal JV, Aljabar P, Rueckert D (2014) Construction of a 4D brain atlas and growth model using diffeomorphic registration. International workshop on spatio-temporal image analysis for longitudinal and time-series image data. Springer, pp 27–37
go back to reference Schuh A, Makropoulos A, Robinson EC, Cordero-Grande L, Hughes E, Hutter J, Price AN, Murgasova M, Teixeira RPA, Tusor N (2018) Unbiased construction of a temporally consistent morphological atlas of neonatal brain development. https://doi.org/10.1101/251512 Schuh A, Makropoulos A, Robinson EC, Cordero-Grande L, Hughes E, Hutter J, Price AN, Murgasova M, Teixeira RPA, Tusor N (2018) Unbiased construction of a temporally consistent morphological atlas of neonatal brain development. https://​doi.​org/​10.​1101/​251512
go back to reference Scott JA, Habas PA, Kim K, Rajagopalan V, Hamzelou KS, Corbett-Detig JM, Barkovich AJ, Glenn OA, Studholme C (2011) Growth trajectories of the human fetal brain tissues estimated from 3D reconstructed in utero MRI. Int J Dev Neurosci 29(5):529–536PubMedPubMedCentralCrossRef Scott JA, Habas PA, Kim K, Rajagopalan V, Hamzelou KS, Corbett-Detig JM, Barkovich AJ, Glenn OA, Studholme C (2011) Growth trajectories of the human fetal brain tissues estimated from 3D reconstructed in utero MRI. Int J Dev Neurosci 29(5):529–536PubMedPubMedCentralCrossRef
go back to reference Serag A, Aljabar P, Ball G, Counsell SJ, Boardman JP, Rutherford MA, Edwards AD, Hajnal JV, Rueckert D (2012a) Construction of a consistent high-definition spatio-temporal atlas of the developing brain using adaptive kernel regression. Neuroimage 59(3):2255–2265PubMedCrossRef Serag A, Aljabar P, Ball G, Counsell SJ, Boardman JP, Rutherford MA, Edwards AD, Hajnal JV, Rueckert D (2012a) Construction of a consistent high-definition spatio-temporal atlas of the developing brain using adaptive kernel regression. Neuroimage 59(3):2255–2265PubMedCrossRef
go back to reference Serag A, Kyriakopoulou V, Rutherford M, Edwards A, Hajnal J, Aljabar P, Counsell S, Boardman J, Rueckert D (2012b) A multi-channel 4D probabilistic atlas of the developing brain: application to fetuses and neonates. Ann BMVA 2012(3):1–14 Serag A, Kyriakopoulou V, Rutherford M, Edwards A, Hajnal J, Aljabar P, Counsell S, Boardman J, Rueckert D (2012b) A multi-channel 4D probabilistic atlas of the developing brain: application to fetuses and neonates. Ann BMVA 2012(3):1–14
go back to reference Taimouri V, Gholipour A, Velasco-Annis C, Estroff JA, Warfield SK (2015) A template-to-slice block matching approach for automatic localization of brain in fetal MRI. In: 2015 IEEE 12th international symposium on biomedical imaging (ISBI). IEEE, pp 144–147 Taimouri V, Gholipour A, Velasco-Annis C, Estroff JA, Warfield SK (2015) A template-to-slice block matching approach for automatic localization of brain in fetal MRI. In: 2015 IEEE 12th international symposium on biomedical imaging (ISBI). IEEE, pp 144–147
go back to reference Tang Y, Hojatkashani C, Dinov ID, Sun B, Fan L, Lin X, Qi H, Hua X, Liu S, Toga AW (2010) The construction of a Chinese MRI brain atlas: a morphometric comparison study between Chinese and Caucasian cohorts. Neuroimage 51(1):33–41PubMedPubMedCentralCrossRef Tang Y, Hojatkashani C, Dinov ID, Sun B, Fan L, Lin X, Qi H, Hua X, Liu S, Toga AW (2010) The construction of a Chinese MRI brain atlas: a morphometric comparison study between Chinese and Caucasian cohorts. Neuroimage 51(1):33–41PubMedPubMedCentralCrossRef
go back to reference Tourbier S, Velasco-Annis C, Taimouri V, Hagmann P, Meuli R, Warfield SK, Cuadra MB, Gholipour A (2017) Automated template-based brain localization and extraction for fetal brain MRI reconstruction. Neuroimage 155:460–472PubMedPubMedCentralCrossRef Tourbier S, Velasco-Annis C, Taimouri V, Hagmann P, Meuli R, Warfield SK, Cuadra MB, Gholipour A (2017) Automated template-based brain localization and extraction for fetal brain MRI reconstruction. Neuroimage 155:460–472PubMedPubMedCentralCrossRef
go back to reference Uchiyama HT, Seki A, Tanaka D, Koeda T (2013) A study of the standard brain in Japanese children: Morphological comparison with the MNI template. Brain Develop 35(3):228–235CrossRef Uchiyama HT, Seki A, Tanaka D, Koeda T (2013) A study of the standard brain in Japanese children: Morphological comparison with the MNI template. Brain Develop 35(3):228–235CrossRef
go back to reference Wang J, Perez L (2017) The effectiveness of data augmentation in image classification using deep learning. Convolutional Neural Network Vis Recognit 11 Wang J, Perez L (2017) The effectiveness of data augmentation in image classification using deep learning. Convolutional Neural Network Vis Recognit 11
go back to reference Weisstanner C, Kasprian G, Gruber G, Brugger P, Prayer D (2015) MRI of the fetal brain. Clin Neuroradiol 25(2):189–196PubMedCrossRef Weisstanner C, Kasprian G, Gruber G, Brugger P, Prayer D (2015) MRI of the fetal brain. Clin Neuroradiol 25(2):189–196PubMedCrossRef
go back to reference Wright R, Kyriakopoulou V, Ledig C, Rutherford MA, Hajnal JV, Rueckert D, Aljabar P (2014) Automatic quantification of normal cortical folding patterns from fetal brain MRI. Neuroimage 91:21–32PubMedCrossRef Wright R, Kyriakopoulou V, Ledig C, Rutherford MA, Hajnal JV, Rueckert D, Aljabar P (2014) Automatic quantification of normal cortical folding patterns from fetal brain MRI. Neuroimage 91:21–32PubMedCrossRef
go back to reference Wu D, Lei J, Rosenzweig JM, Burd I, Zhang J (2015) In utero localized diffusion MRI of the embryonic mouse brain microstructure and injury. J Mag Reson Imaging 42(3):717–728CrossRef Wu D, Lei J, Rosenzweig JM, Burd I, Zhang J (2015) In utero localized diffusion MRI of the embryonic mouse brain microstructure and injury. J Mag Reson Imaging 42(3):717–728CrossRef
go back to reference Zhao L, Feng X, Meyer C, Wu Y, Plessis AJd, Limperopoulos C (2019a) Fetal brain automatic segmentation using 3D deep convolutional neural network. In: ISMRM 27th annual meeting, 2019, pp 11–16 Zhao L, Feng X, Meyer C, Wu Y, Plessis AJd, Limperopoulos C (2019a) Fetal brain automatic segmentation using 3D deep convolutional neural network. In: ISMRM 27th annual meeting, 2019, pp 11–16
go back to reference Zhao T, Liao X, Fonov VS, Wang Q, Men W, Wang Y, Qin S, Tan S, Gao J-H, Evans A (2019b) Unbiased age-specific structural brain atlases for Chinese pediatric population. Neuroimage 189:55–70PubMedCrossRef Zhao T, Liao X, Fonov VS, Wang Q, Men W, Wang Y, Qin S, Tan S, Gao J-H, Evans A (2019b) Unbiased age-specific structural brain atlases for Chinese pediatric population. Neuroimage 189:55–70PubMedCrossRef
Metadata
Title
Mapping fetal brain development based on automated segmentation and 4D brain atlasing
Authors
Haotian Li
Guohui Yan
Wanrong Luo
Tingting Liu
Yan Wang
Ruibin Liu
Weihao Zheng
Yi Zhang
Kui Li
Li Zhao
Catherine Limperopoulos
Yu Zou
Dan Wu
Publication date
01-07-2021
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 6/2021
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-021-02303-x

Other articles of this Issue 6/2021

Brain Structure and Function 6/2021 Go to the issue