Abstract
This paper is based on a literature review from 2011 to 2016. The paper is divided into two main sections. The first section relates to technical advances in fetal imaging techniques, including fetal motion compensation, imaging at 3.0 T, 3-D T2-weighted MRI, susceptibility-weighted imaging, computed tomography, morphometric analysis, diffusion tensor imaging, spectroscopy and fetal behavioral assessment. The second section relates to clinical updates, including cerebral lamination, migrational anomalies, midline anomalies, neural tube defects, posterior fossa anomalies, sulcation/gyration and hypoxic–ischemic insults.
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References
Mailath-Pokorny M, Kasprian G, Mitter C et al (2012) Magnetic resonance methods in fetal neurology. Semin Fetal Neonatal Med 17:278–284
Malamateniou C, Malik SJ, Counsell SJ et al (2013) Motion-compensation techniques in neonatal and fetal MR imaging. AJNR Am J Neuroradiol 34:1124–1136
Yen C (2016) Correlation between maternal breakfast and fetal motion during fetal MRI. Pediatr Radiol 46:S138
Malamateniou C, McGuinness AK, Allsop JM et al (2011) Snapshot inversion recovery: an optimized single-shot T1-weighted inversion-recovery sequence for improved fetal brain anatomic delineation. Radiology 258:229–235
Keraudren K, Kuklisova-Murgasova M, Kyriakopoulou V et al (2014) Automated fetal brain segmentation from 2D MRI slices for motion correction. NeuroImage 101:633–643
Victoria T, Jaramillo D, Roberts TP et al (2014) Fetal magnetic resonance imaging: jumping from 1.5 to 3 tesla (preliminary experience). Pediatr Radiol 44:376–386
Krishnamurthy U, Neelavalli J, Mody S et al (2015) MR imaging of the fetal brain at 1.5T and 3.0T field strengths: comparing specific absorption rate (SAR) and image quality. J Perinat Med 43:209–220
Neelavalli J, Krishnamurthy U, Jella PK et al (2016) Magnetic resonance angiography of fetal vasculature at 3.0 T. Eur Radiol 26:4570–4576
Jarvis D, Griffiths PD, Majewski C (2016) Demonstration of normal and abnormal fetal brains using 3D printing from in utero MR imaging data. AJNR Am J Neuroradiol 37:1757–1761
Dai Y, Dong S, Zhu M et al (2014) Visualizing cerebral veins in fetal brain using susceptibility-weighted MRI. Clin Radiol 69:e392–e397
Neelavalli J, Mody S, Yeo L et al (2014) MR venography of the fetal brain using susceptibility weighted imaging. J Magn Reson Imaging 40:949–957
Neelavalli J, Jella PK, Krishnamurthy U et al (2014) Measuring venous blood oxygenation in fetal brain using susceptibility-weighted imaging. J Magn Reson Imaging 39:998–1006
Robinson AJ, Blaser S, Vladimirov A et al (2015) Foetal "black bone" MRI: utility in assessment of the foetal spine. Br J Radiol 88:20140496
Macé G, Sonigo P, Cormier-Daire V et al (2013) Three-dimensional helical computed tomography in prenatal diagnosis of fetal skeletal dysplasia. Ultrasound Obstet Gynecol 42:161–168
Victoria T, Epelman M, Coleman BG et al (2013) Low-dose fetal CT in the prenatal evaluation of skeletal dysplasias and other severe skeletal abnormalities. AJR Am J Roentgenol 200:989–1000
Studholme C (2015) Mapping the developing human brain in utero using quantitative MR imaging techniques. Semin Perinatol 39:105–112
Gholipour A, Limperopoulos C, Clancy S et al (2014) Construction of a deformable spatiotemporal MRI atlas of the fetal brain: evaluation of similarity metrics and deformation models. Med Image Comput Comput Assist Interv 17:292–299
Zhan J, Dinov ID, Li J et al (2013) Spatial-temporal atlas of human fetal brain development during the early second trimester. NeuroImage 82:115–126
Clouchoux C, Guizard N, Evans AC et al (2012) Normative fetal brain growth by quantitative in vivo magnetic resonance imaging. Am J Obstet Gynecol 206:173.e1–173.e8
Gholipour A, Akhondi-Asl A, Estroff JA, Warfield SK (2012) Multi-atlas multi-shape segmentation of fetal brain MRI for volumetric and morphometric analysis of ventriculomegaly. NeuroImage 60:1819–1831
Wright R, Kyriakopoulou V, Ledig C et al (2014) Automatic quantification of normal cortical folding patterns from fetal brain MRI. NeuroImage 91:21–32
Clouchoux C, Kudelski D, Gholipour A et al (2012) Quantitative in vivo MRI measurement of cortical development in the fetus. Brain Struct Funct 217:127–139
Wu J, Awate SP, Licht DJ et al (2015) Assessment of MRI-based automated fetal cerebral cortical folding measures in prediction of gestational age in the third trimester. AJNR Am J Neuroradiol 36:1369–1374
Kuklisova-Murgasova M, Cifor A, Napolitano R et al (2013) Registration of 3D fetal neurosonography and MRI. Med Image Anal 17:1137–1150
Qiu A, Mori S, Miller MI (2015) Diffusion tensor imaging for understanding brain development in early life. Annu Rev Psychol 66:853–876
Ouyang A, Jeon T, Sunkin SM et al (2015) Spatial mapping of structural and connectional imaging data for the developing human brain with diffusion tensor imaging. Methods 73:27–37
Takahashi E, Folkerth RD, Galaburda AM, Grant PE (2012) Emerging cerebral connectivity in the human fetal brain: an MR tractography study. Cereb Cortex 22:455–464
Huang H, Vasung L (2014) Gaining insight of fetal brain development with diffusion MRI and histology. Int J Dev Neurosci 32:11–22
Jakab A, Kasprian G, Schwartz E et al (2015) Disrupted developmental organization of the structural connectome in fetuses with corpus callosum agenesis. NeuroImage111:277–288
Simões RV, Sanz-Cortes M, Muñoz-Moreno E et al (2015) Feasibility and technical features of fetal brain magnetic resonance spectroscopy in 1.5 T scanners. Am J Obstet Gynecol 213:741–742
Berger-Kulemann V, Brugger PC, Pugash D et al (2013) MR spectroscopy of the fetal brain: is it possible without sedation? AJNR Am J Neuroradiol 34:424–431
Cetin I, Barberis B, Brusati V et al (2011) Lactate detection in the brain of growth-restricted fetuses with magnetic resonance spectroscopy. Am J Obstet Gynecol 205:350.e1–350.e7
Hayat TT, Nihat A, Martinez-Biarge M et al (2011) Optimization and initial experience of a multisection balanced steady-state free precession cine sequence for the assessment of fetal behavior in utero. AJNR Am J Neuroradiol 32:331–338
Pugash D, Hendson G, Dunham CP et al (2012) Sonographic assessment of normal and abnormal patterns of fetal cerebral lamination. Ultrasound Obstet Gynecol 40:642–651
Lipitz S, Yinon Y, Malinger G et al (2013) Risk of cytomegalovirus-associated sequelae in relation to time of infection and findings on prenatal imaging. Ultrasound Obstet Gynecol 41:508–514
Blondiaux E, Sileo C, Nahama-Allouche C et al (2013) Periventricular nodular heterotopia on prenatal ultrasound and magnetic resonance imaging. Ultrasound Obstet Gynecol 42:149–155
Teixeira SR, Blondiaux E, Cassart M et al (2015) Association of periventricular nodular heterotopia with posterior fossa cyst: a prenatal case series. Prenat Diagn 35:337–341
Fallet-Bianco C, Laquerrière A, Poirier K et al (2014) Mutations in tubulin genes are frequent causes of various foetal malformations of cortical development including microlissencephaly. Acta Neuropathol Commun 2:69
Lacalm A, Nadaud B, Massoud M et al (2016) Prenatal diagnosis of cobblestone lissencephaly associated with Walker-Warburg syndrome based on a specific sonographic pattern. Ultrasound Obstet Gynecol 47:117–122
Bell S, O'Mahony E, Fink AM et al (2015) Antenatal imaging of anomalies of the corpus callosum: a decade of experience. Arch Gynecol Obstet 292:537–542
Kasprian G, Brugger PC, Schöpf V et al (2013) Assessing prenatal white matter connectivity in commissural agenesis. Brain 136:168–179
Vinurel N, Van Nieuwenhuyse A, Cagneaux M et al (2014) Distortion of the anterior part of the interhemispheric fissure: significance and implications for prenatal diagnosis. Ultrasound Obstet Gynecol 43:346–352
Woitek R, Dvorak A, Weber M et al (2014) MR-based morphometry of the posterior fossa in fetuses with neural tube defects of the spine. PLoS One 9:e112585
Mignone Philpott C, Shannon P, Chitayat D et al (2013) Diffusion-weighted imaging of the cerebellum in the fetus with Chiari II malformation. AJNR Am J Neuroradiol 34:1656–1660
Kasprian GJ, Paldino MJ, Mehollin-Ray AR et al (2015) Prenatal imaging of occipital encephaloceles. Fetal Diagn Ther 37:241–248
Dankovcik R, Vyhnalkova V, Muranska S et al (2012) Encephalocystocele — uncommon diagnosis in prenatal medicine. Fetal Diagn Ther 32:295–298
Pugash D, Oh T, Godwin K et al (2011) Sonographic 'molar tooth' sign in the diagnosis of Joubert syndrome. Ultrasound Obstet Gynecol 38:598–602
Quarello E, Molho M, Garel C et al (2014) Prenatal abnormal features of the fourth ventricle in Joubert syndrome and related disorders. Ultrasound Obstet Gynecol 43:227–232
Robinson AJ (2014) Inferior vermian hypoplasia — preconception, misconception. Ultrasound Obstet Gynecol 43:123–136
Bolduc ME, du Plessis AJ, Sullivan N et al (2012) Regional cerebellar volumes predict functional outcome in children with cerebellar malformations. Cerebellum 11:531–542
Massoud M, Cagneaux M, Garel C et al (2014) Prenatal unilateral cerebellar hypoplasia in a series of 26 cases: significance and implications for prenatal diagnosis. Ultrasound Obstet Gynecol 44:447–454
Fernández-Mayoralas DM, Recio-Rodríguez M, Fernández-Perrone AL et al (2014) In utero diagnosis of PHACE syndrome by fetal magnetic resonance imaging (MRI). J Child Neurol 29:118–121
Manganaro L, Bernardo S, La Barbera L et al (2012) Role of foetal MRI in the evaluation of ischaemic-haemorrhagic lesions of the foetal brain. J Perinat Med 40:419–426
Leroy F, Cai Q, Bogart SL et al (2015) New human-specific brain landmark: the depth asymmetry of superior temporal sulcus. Proc Natl Acad Sci U S A 112:1208–1213
Fink AM, Hingston T, Sampson A et al (2010) Malformation of the fetal brain in thanatophoric dysplasia: US and MRI findings. Pediatr Radiol 40:S134–S137
Pugash D, Lehman AM, Langlois S (2014) Prenatal ultrasound and MRI findings of temporal and occipital lobe dysplasia in a twin with achondroplasia. Ultrasound Obstet Gynecol 44:365–368
Cesaretti C, Spaccini L, Rustico M et al (2014) Prenatal magnetic resonance imaging detection of temporal lobes and hippocampal anomalies in hypochondroplasia. Prenat Diagn 34:1015–1017
Rubio EI, Blask A, Bulas DI (2016) Ultrasound and MR imaging findings in prenatal diagnosis of craniosynostosis syndromes. Pediatr Radiol 46:709–718
Stark Z, McGillivray G, Sampson A et al (2015) Apert syndrome: temporal lobe abnormalities on fetal brain imaging. Prenat Diagn 35:179–182
Ozcan UA, Işik U, Dincer A, Erzen C (2013) Identification of fetal precentral gyrus on diffusion weighted MRI. Brain Dev 35:4–9
Righini A, Parazzini C, Doneda C et al (2012) Early formative stage of human focal cortical gyration anomalies: fetal MRI. AJR Am J Roentgenol 198:439–447
Tarui T, Khwaja OS, Estroff JA et al (2012) Altered fetal cerebral and cerebellar development in twin-twin transfusion syndrome. AJNR Am J Neuroradiol 33:1121–1126
Griffiths PD, Sharrack S, Chan KL et al (2015) Fetal brain injury in survivors of twin pregnancies complicated by demise of one twin as assessed by in utero MR imaging. Prenat Diagn 35:583–591
Merhar SL, Kline-Fath BM, Meinzen-Derr J et al (2013) Fetal and postnatal brain MRI in premature infants with twin-twin transfusion syndrome. J Perinatol 33:112–118
Weisz B, Hoffmann C, Ben-Baruch S et al (2014) Early detection by diffusion-weighted sequence magnetic resonance imaging of severe brain lesions after fetoscopic laser coagulation for twin-twin transfusion syndrome. Ultrasound Obstet Gynecol 44:44–49
Tarui T, Khwaja OS, Estroff JA et al (2011) Fetal MR imaging evidence of prolonged apparent diffusion coefficient decrease in fetal death. AJNR Am J Neuroradiol 32:E126–E128
Wagner MW, Vaught AJ, Poretti A et al (2015) Vein of Galen aneurysmal malformation: prognostic markers depicted on fetal MRI. Neuroradiol J 28:72–75
Schellen C, Ernst S, Gruber GM et al (2015) Fetal MRI detects early alterations of brain development in tetralogy of Fallot. Am J Obstet Gynecol 213:392.e1–392.e7
Clouchoux C, du Plessis AJ, Bouyssi-Kobar M et al (2013) Delayed cortical development in fetuses with complex congenital heart disease. Cereb Cortex 23:2932–2943
Brossard-Racine M, du Plessis AJ, Vezina G et al (2014) Prevalence and spectrum of in utero structural brain abnormalities in fetuses with complex congenital heart disease. AJNR Am J Neuroradiol 35:1593–1599
Mlczoch E, Brugger P, Ulm B et al (2013) Structural congenital brain disease in congenital heart disease: results from a fetal MRI program. Eur J Paediatr Neurol 17:153–160
Sun L, Macgowan CK, Sled JG et al (2015) Reduced fetal cerebral oxygen consumption is associated with smaller brain size in fetuses with congenital heart disease. Circulation 131:1313–1323
Sethi V, Tabbutt S, Dimitropoulos A et al (2013) Single-ventricle anatomy predicts delayed microstructural brain development. Pediatr Res 73:661–667
Li Y, Yin S, Fang J et al (2015) Neurodevelopmental delay with critical congenital heart disease is mainly from prenatal injury not infant cardiac surgery: current evidence based on a meta-analysis of functional magnetic resonance imaging. Ultrasound Obstet Gynecol 45:639–648
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Robinson, A.J., Ederies, M.A. Fetal neuroimaging: an update on technical advances and clinical findings. Pediatr Radiol 48, 471–485 (2018). https://doi.org/10.1007/s00247-017-3965-z
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DOI: https://doi.org/10.1007/s00247-017-3965-z