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How to obtain diagnostic planes of the fetal central nervous system using three-dimensional ultrasound and a context-preserving rendering technology

Published:November 14, 2018DOI:https://doi.org/10.1016/j.ajog.2018.11.1088
      The antenatal evaluation of the fetal central nervous system (CNS) is among the most difficult tasks of prenatal ultrasound (US), requiring technical skills in relation to ultrasound and image acquisition as well as knowledge of CNS anatomy and how this changes with gestation. According to the International Guidelines for fetal neurosonology, the basic assessment of fetal CNS is most frequently performed on the axial planes, whereas the coronal and sagittal planes are required for the multiplanar evaluation of the CNS within the context of fetal neurosonology. It can be even more technically challenging to obtain “nonaxial” views with 2-dimensional (2D) US. The modality of 3-dimensional (3D) US has been suggested as a panacea to overcome the technical difficulties of achieving nonaxial views. The lack of familiarity of most sonologists with the use of 3D US and its related processing techniques may preclude its use even where it could play an important role in complementing antenatal 2D US assessment. Furthermore, once a 3D volume has been acquired, proprietary software allows it to be processed in different ways, leading to multiple ways of displaying and analyzing the same anatomical imaging or plane. These are difficult to learn and time consuming in the absence of specific training. In this article, we describe the key steps for volume acquisition of a 3D US volume, manipulation, and processing with reference to images of the fetal CNS, using a newly developed context-preserving rendering technique.

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      References

        • Chaoui R.
        • Heling K.S.
        Three-dimensional ultrasound in prenatal diagnosis.
        Curr Opin Obstet Gynecol. 2006; 18: 192-202
        • Benacerraf B.R.
        • Shipp T.D.
        • Bromley B.
        How sonographic tomography will change the face of obstetric sonography: a pilot study.
        J Ultrasound Med. 2005; 24: 371-378
        • Benacerraf B.R.
        • Shipp T.D.
        • Bromley B.
        Three-dimensional US of the fetus: volume imaging.
        Radiology. 2006; 238: 988-996
        • Gonçalves L.F.
        • Lee W.
        • Espinoza J.
        • Romero R.
        Three- and 4-dimensional ultrasound in obstetric practice: does it help?.
        J Ultrasound Med. 2005; 24: 1599-1624
        • Abuhamad A.Z.
        Standardization of 3-dimensional volumes in obstetric sonography: a required step for training and automation.
        J Ultrasound Med. 2005; 24: 397-401
        • Mercé L.T.
        • Barco M.J.
        • Bau S.
        Three-dimensional volume sonographic study of fetal anatomy: intraobserver reproducibility and effect of examiner experience.
        J Ultrasound Med. 2008; 27: 1053-1063
        • Pilu G.
        • Ghi T.
        • Carletti A.
        • Segata M.
        • Perolo A.
        • Rizzo N.
        Three-dimensional ultrasound examination of the fetal central nervous system.
        Ultrasound Obstet Gynecol. 2007; 30: 233-245
        • Rizzo G.
        • Abuhamad A.Z.
        • Benacerraf B.R.
        • et al.
        Collaborative study on 3-dimensional sonography for the prenatal diagnosis of central nervous system defects.
        J Ultrasound Med. 2011; 30: 1003-1008
        • Pooh R.K.
        Normal anatomy by three-dimensional ultrasound in the second and third trimesters.
        Semin Fetal Neonatal Med. 2012; 17: 269-277
        • Leibovitz Z.
        • Shkolnik C.
        • Haratz K.K.
        • Malinger G.
        • Shapiro I.
        • Lerman-Sagie T.
        Assessment of fetal midbrain and hindbrain in mid-sagittal cranial plane by three-dimensional multiplanar sonography. Part 1: comparison of new and established nomograms.
        Ultrasound Obstet Gynecol. 2014; 44: 575-580
        • Leibovitz Z.
        • Shkolnik C.
        • Haratz K.K.
        • Malinger G.
        • Shapiro I.
        • Lerman-Sagie T.
        Assessment of fetal midbrain and hindbrain in mid-sagittal cranial plane by three-dimensional multiplanar sonography. Part 2: application of nomograms to fetuses with posterior fossa malformations.
        Ultrasound Obstet Gynecol. 2014; 44: 581-587
        • Leibovitz Z.
        • Haratz K.K.
        • Malinger G.
        • Shapiro I.
        • Pressman C.
        Fetal posterior fossa dimensions: normal and anomalous development assessed in mid-sagittal cranial plane by three-dimensional multiplanar sonography.
        Ultrasound Obstet Gynecol. 2014; 43: 147-153
        • Ghi T.
        • Contro E.
        • De Musso F.
        • et al.
        Normal morphometry of fetal posterior fossa at midtrimester: brainstem-tentorium angle and brainstem-vermis angle.
        Prenat Diagn. 2012; 32: 440-443
        • Contro E.
        • Salsi G.
        • Montaguti E.
        • et al.
        Sequential analysis of the normal fetal fissures with three-dimensional ultrasound: a longitudinal study.
        Prenat Diagn. 2015; 35: 493-499
        • Pistorius L.R.
        • Stoutenbeek P.
        • Groenendaal F.
        • et al.
        Grade and symmetry of normal fetal cortical development: a longitudinal two- and three-dimensional ultrasound study.
        Ultrasound Obstet Gynecol. 2010; 36: 700-708
        • Alves C.M.
        • Araujo Júnior E.
        • Nardozza L.M.
        • et al.
        Reference ranges for fetal brain fissure development on 3-dimensional sonography in the multiplanar mode.
        J Ultrasound Med. 2013; 32: 269-277
        • Contro E.
        • Nanni M.
        • Bellussi F.
        • et al.
        The hippocampal commissure: a new finding at prenatal 3D ultrasound in fetuses with isolated complete agenesis of the corpus callosum.
        Prenat Diagn. 2015; 35: 919-922
        • Miguelote R.F.
        • Vides B.
        • Santos R.F.
        • et al.
        Feasibility and reproducibility of transvaginal, transabdominal, and 3D volume reconstruction sonography for measurement of the corpus callosum at different gestational ages.
        Fetal Diagn Ther. 2012; 31: 19-25
        • Miguelote R.F.
        • Vides B.
        • Santos R.F.
        • Palha J.A.
        • Matias A.
        • Sousa N.
        The role of three-dimensional imaging reconstruction to measure the corpus callosum: comparison with direct mid-sagittal views.
        Prenat Diagn. 2011; 31: 875-880
        • Pilu G.
        • Segata M.
        • Ghi T.
        • et al.
        Diagnosis of midline anomalies of the fetal brain with the three-dimensional median view.
        Ultrasound Obstet Gynecol. 2006; 27: 522-529
        • Bault J.P.
        Visualization of the fetal optic chiasma using three-dimensional ultrasound imaging.
        Ultrasound Obstet Gynecol. 2006; 28: 862-864
        • Paladini D.
        • Birnbaum R.
        • Donarini G.
        • Maffeo I.
        • Fulcheri E.
        Assessment of fetal optic chiasm: an echoanatomic and reproducibility study.
        Ultrasound Obstet Gynecol. 2016; 48: 727-732
        • De Jong-Pleij E.A.
        • Ribbert L.S.
        • Tromp E.
        • Bilardo C.M.
        Three-dimensional multiplanar ultrasound is a valuable tool in the study of the fetal profile in the second trimester of pregnancy.
        Ultrasound Obstet Gynecol. 2010; 35: 195-200
        • Tutschek B.
        • Blaas H.K.
        • Abramowicz J.
        • et al.
        Three-dimensional ultrasound imaging of the fetal skull and face.
        Ultrasound Obstet Gynecol. 2017; 50: 7-16
        • Campbell S.
        • Lees C.C.
        The three-dimensional reverse face (3D RF) view for the diagnosis of cleft palate.
        Ultrasound Obstet Gynecol. 2003; 22: 552-554
        • Campbell S.
        • Lees C.
        • Moscoso G.
        • Hall P.
        Ultrasound antenatal diagnosis of cleft palate by a new technique: the 3D ‘reverse face’ view.
        Ultrasound Obstet Gynecol. 2005; 25: 12-18
        • Pilu G.
        • Segata M.
        A novel technique for visualization of the normal and cleft fetal secondary palate: angled insonation and three-dimensional ultrasound.
        Ultrasound Obstet Gynecol. 2007; 29: 166-169
        • Faure J.M.
        • Captier G.
        • Baumler M.
        • Boulot P.
        Sonographic assessment of normal fetal palate using three-dimensional imaging: a new technique.
        Ultrasound Obstet Gynecol. 2007; 29: 159-165
        • Rotten D.
        • Levaillant J.M.
        • Benouaiche L.
        • Nicot R.
        • Couly G.
        Visualization of fetal lips and palate using a surface-rendered oropalatal (SROP) view in fetuses with normal palate or orofacial cleft lip with or without cleft palate.
        Ultrasound Obstet Gynecol. 2016; 47: 244-246
        • Platt L.D.
        • Devore G.R.
        • Pretorius D.H.
        Improving cleft palate/cleft lip antenatal diagnosis by 3-dimensional sonography: the “flipped face” view.
        J Ultrasound Med. 2006; 25: 1423-1430
        • Tonni G.
        • Lituania M.
        OmniView algorithm: a novel 3-dimensional sonographic technique in the study of the fetal hard and soft palates.
        J Ultrasound Med. 2012; 31: 313-318
        • Dall'Asta A.
        • Paramasivam G.
        • Lees C.C.
        Qualitative evaluation of Crystal Vue rendering technology in assessment of fetal lip and palate.
        Ultrasound Obstet Gynecol. 2017; 49: 549-552
        • Paladini D.
        Fetal micrognathia: almost always an ominous finding.
        Ultrasound Obstet Gynecol. 2010; 35: 377-384
        • Thellier E.
        • Levaillant J.M.
        • Roume J.
        • Quarello E.
        • Bault J.P.
        Cornelia de Lange syndrome: specific features for a prenatal diagnosis.
        Ultrasound Obstet Gynecol. 2017; 49: 668-670
        • David A.L.
        • Turnbull C.
        • Scott R.
        • et al.
        Diagnosis of Apert syndrome in the second-trimester using 2D and 3D ultrasound.
        Prenat Diagn. 2007; 27: 629-632
        • Chen C.P.S.Y.
        • Hsu C.Y.
        • Tsai F.J.
        • et al.
        Abnormally flat facial profile on two- and three-dimensional ultrasound and array comparative genomic hybridization for the diagnosis of Pallister-Killian syndrome.
        Taiwan J Obstet Gynecol. 2010; 49: 124-128
        • Clark D.M.S.I.
        • Deardorff M.A.
        • Byrne J.L.
        • et al.
        Identification of a prenatal profile of Cornelia de Lange syndrome (CdLS): a review of 53 CdLS pregnancies.
        Am J Med Genet A. 2012; 158A: 1848-1856
        • Mahieu-Caputo D.S.P.
        • Amiel J.
        • Simon I.
        • et al.
        Prenatal diagnosis of sporadic Apert syndrome: a sequential diagnostic approach combining three-dimensional computed tomography and molecular biology.
        Fetal Diagn Ther. 2001; 16: 10-12
        • Levaillant J.-M.
        • Gérard-Blanluet M.
        • Holder-Espinasse M.
        • et al.
        Prenatal phenotypic overlap of Costello syndrome and severe Noonan syndrome by tri-dimensional ultrasonography.
        Prenat Diagn. 2006; 26: 340-344
        • Guzelmansur I.
        • C G.
        • Ceylaner S.
        • Ceylan N.
        • Daplan T.
        Prenatal diagnosis of Goldenhar syndrome with unusual features by 3D ultrasonography.
        Genet Couns. 2013; 24: 319-325
        • Dall'Asta A.
        • Schievano S.
        • Bruse J.L.
        • et al.
        Quantitative analysis of fetal facial morphology using 3D ultrasound and statistical shape modeling: a feasibility study.
        Am J Obstet Gynecol. 2017; 217: 76.e1-76.e8
        • Achiron R.
        • Gindes L.
        • Zalel Y.
        • Lipitz S.
        • Weisz B.
        Three- and four-dimensional ultrasound: new methods for evaluating fetal thoracic anomalies.
        Ultrasound Obstet Gynecol. 2008; 32: 36-43
        • Dall'Asta A.
        • Paramasivam G.
        • Lees C.C.
        Crystal Vue technique for imaging fetal spine and ribs.
        Ultrasound Obstet Gynecol. 2016; 47: 383-384
        • Zheng L.P.
        • Gong L.L.
        • Guo F.C.
        • Chang H.B.
        • Liu G.H.
        Application research on three-dimensional ultrasonic skeletal imaging mode in detecting fetal upper jaw bone.
        Int J Clin Exp Med. 2015; 8: 12219-12225
        • Chaoui R.
        • Heling K.S.
        New developments in fetal heart scanning: three- and four-dimensional fetal echocardiography.
        Semin Fetal Neonatal Med. 2005; 10: 567-577
        • Chaoui R.
        • Hoffmann J.
        • Heling K.S.
        Three-dimensional (3D) and 4D color Doppler fetal echocardiography using spatio-temporal image correlation (STIC).
        Ultrasound Obstet Gynecol. 2004; 23: 535-545
        • Yeo L.
        • Romero R.
        Color and power Doppler combined with fetal intelligent navigation echocardiography (FINE) to evaluate the fetal heart.
        Ultrasound Obstet Gynecol. 2017; 50: 476-491
        • Yeo L.
        • Luewan S.
        • Markush D.
        • Gill N.
        • Romero R.
        Prenatal diagnosis of dextrocardia with complex congenital heart disease using fetal intelligent navigation echocardiography (FINE) and a literature review.
        Fetal Diagn Ther. 2018; 43: 304-316
        • Yeo L.
        • Romero R.
        How to acquire cardiac volumes for sonographic examination of the fetal heart: part 1.
        J Ultrasound Med. 2016; 35: 1021-1042
        • Yeo L.
        • Romero R.
        How to acquire cardiac volumes for sonographic examination of the fetal heart: part 2.
        J Ultrasound Med. 2016; 35: 1043-1066
        • Hamill N.
        • Yeo L.
        • Romero R.
        • et al.
        Fetal cardiac ventricular volume, cardiac output, and ejection fraction determined with 4-dimensional ultrasound using spatiotemporal image correlation and virtual organ computer-aided analysis.
        Am J Obstet Gynecol. 2011; 205: 76.e1-76.e10
        • Gonçalves L.F.
        • Lee W.
        • Espinoza J.
        • Romero R.
        Examination of the fetal heart by four-dimensional (4D) ultrasound with spatio-temporal image correlation (STIC).
        Ultrasound Obstet Gynecol. 2006; 27: 336-348
        • Gonçalves L.F.
        • Lee W.
        • Chaiworapongsa T.
        • et al.
        Four-dimensional ultrasonography of the fetal heart with spatiotemporal image correlation.
        Am J Obstet Gynecol. 2003; 189: 1792-1802
        • Nishizawa C.
        • Cajusay-Velasco S.
        • Mashima M.
        • et al.
        HDlive imaging of fetal enteric duplication cyst.
        J Med Ultrason (2001). 2014; 41: 511-514
        • Volpe N.
        • Mazzone E.
        • Muto B.
        • et al.
        3D assessment of the umbilical vein deviation angle (UVDA) for the prediction of liver herniation in left congenital diaphragmatic hernia.
        Ultrasound Obstet Gynecol. 2018; 51: 214-218
        • Yeo L.
        • Romero R.
        Color and power Doppler combined with fetal intelligent navigation echocardiography (FINE) to evaluate the fetal heart.
        Ultrasound Obstet Gynecol. 2017; 50: 476-491
        • Veronese P.
        • Bogana G.
        • Cerutti A.
        • et al.
        A prospective study of the use of fetal intelligent navigation echocardiography (FINE) to obtain standard fetal echocardiography views.
        Fetal Diagn Ther. 2017; 41: 89-99
        • Garcia M.
        • Yeo L.
        • Romero R.
        • et al.
        Prospective evaluation of the fetal heart using fetal intelligent navigation echocardiography (FINE).
        Ultrasound Obstet Gynecol. 2016; 47: 450-459
        • Yeo L.
        • Romero R.
        Fetal intelligent navigation echocardiography (FINE): a novel method for rapid, simple, and automatic examination of the fetal heart.
        Ultrasound Obstet Gynecol. 2013; 42: 268-284
        • Rizzo G.
        • Capponi A.
        • Persico N.
        • et al.
        5D CNS+ Software for automatically imaging axial, sagittal, and coronal planes of normal and abnormal second-trimester fetal brains.
        J Ultrasound Med. 2016; 35: 2263-2272
        • International Society of Ultrasound in Obstetrics & Gynecology Education Committee
        Sonographic examination of the fetal central nervous system: guidelines for performing the basic examination and the fetal neurosonogram.
        Ultrasound Obstet Gynecol. 2007; 29: 109-116
        • Wax J.
        • Minkoff H.
        • Johnson A.
        • et al.
        Consensus report on the detailed fetal anatomic ultrasound examination: indications, components, and qualifications.
        J Ultrasound Med. 2014; 33: 189-195
        • Abuhamad A.
        • Minton K.K.
        • Benson C.B.
        • et al.
        Obstetric and gynecologic ultrasound curriculum and competency assessment in residency training programs: consensus report.
        Am J Obstet Gynecol. 2018; 218: 29-67
        • Benacerraf B.R.
        • Minton K.K.
        • Benson C.B.
        • et al.
        Proceedings: Beyond Ultrasound First Forum on Improving the Quality of Ultrasound Imaging in Obstetrics and Gynecology.
        Am J Obstet Gynecol. 2018; 218: 19-28
        • Hata T.
        • Hanaoka U.
        • Tenkumo C.
        • Sato M.
        • Tanaka H.
        • Ishimura M.
        Three- and four-dimensional HDlive rendering images of normal and abnormal fetuses: pictorial essay.
        Arch Gynecol Obstet. 2012; 286: 1431-1435
        • Benoit B.
        • Chaoui R.
        Three-dimensional ultrasound with maximal mode rendering: a novel technique for the diagnosis of bilateral or unilateral absence or hypoplasia of nasal bones in second-trimester screening for Down syndrome.
        Ultrasound Obstet Gynecol. 2005; 25: 19-24
        • Timor-Tritsch I.E.
        • Monteagudo A.
        • Santos R.
        Three-dimensional inversion rendering in the first- and early second-trimester fetal brain: its use in holoprosencephaly.
        Ultrasound Obstet Gynecol. 2008; 32: 744-750
        • Pooh R.K.
        Brand new technology of HDlive silhouette and HDlive flow images.
        in: Pooh R.K. Kurjak A. Donald School Atlas of Advanced Ultrasound in Obstetrics and Gynecology. Jaypee Brothers Medical Publishers Private Ltd, New Delhi2015: 1-39
        • Hata T.
        • Ito M.
        • Nitta E.
        • Pooh R.
        • Sasahara J.
        • Inamura N.
        HDlive Flow Silhouette mode for diagnosis of ectopia cordis with a left ventricular diverticulum at 15 weeks' gestation.
        J Ultrasound Med. 2018; 37: 2465-2467
        • Lipa M.
        • Pooh R.K.
        • Wielgoś M.
        Three-dimensional neurosonography─a novel field in fetal medicine.
        Ginekol Pol. 2017; 88: 215-221
        • Pooh R.K.
        Sonoembryology by 3D HDlive silhouette ultrasound─what is added by the “see-through fashion”?.
        J Perinat Med. 2016; 44: 139-148
      1. Philips Inc. Advanced obstetric visualisation. Tools for photorealistic fetal rendering. Available at: https://www.philips.co.uk/healthcare/resources/feature-detail/ultrasound-truevue-imaging. Accessed January 24, 2019.

      2. Canon Medical Systems. Aplio 500 Platinum Series. Available at: https://anz.medical.canon/products/ul/aplio-500/imaging/. Accessed January 24, 2019.

        • Griffiths P.D.
        • Bradburn M.
        • Campbell M.J.
        • et al.
        Use of MRI in the diagnosis of fetal brain abnormalities in utero (MERIDIAN): a multicentre, prospective cohort study.
        Lancet. 2017; 389: 538-546
        • Paladini D.
        • Malinger G.
        • Pilu G.
        • Timor-Trisch I.
        • Volpe P.
        The MERIDIAN trial: caution is needed.
        Lancet. 2017; 389: 2103
        • Paladini D.
        • Quarantelli M.
        • Sglavo G.
        • et al.
        Accuracy of neurosonography and MRI in clinical management of fetuses referred with central nervous system abnormalities.
        Ultrasound Obstet Gynecol. 2014; 44: 188-196
        • Malinger G.
        • Lev D.
        • Lerman-Sagie T.
        Is fetal magnetic resonance imaging superior to neurosonography for detection of brain anomalies?.
        Ultrasound Obstet Gynecol. 2002; 20: 317-321
        • Rossi A.C.
        • Prefumo F.
        Additional value of fetal magnetic resonance imaging in the prenatal diagnosis of central nervous system anomalies: a systematic review of the literature.
        Ultrasound Obstet Gynecol. 2014; 44: 388-393
        • Mailath-Pokorny M.
        • Kasprian G.
        • Mitter C.
        • et al.
        Magnetic resonance methods in fetal neurology.
        Semin Fetal Neonatal Med. 2012; 17: 278-284
        • Eppes C.
        • Rac M.
        • Dunn J.
        • Versalovic J.
        • et al.
        Testing for Zika virus infection in pregnancy: key concepts to deal with an emerging epidemic.
        Am J Obstet Gynecol. 2017; 216: 209-225
        • Reddy U.M.
        • Abuhamad A.Z.
        • Levine D.
        • Saade G.R.
        • Fetal Imaging Workshop Invited Participants
        Fetal imaging: executive summary of a joint Eunice Kennedy Shriver National Institute of Child Health and Human Development, Society for Maternal-Fetal Medicine, American Institute of Ultrasound in Medicine, American College of Obstetricians and Gynecologists, American College of Radiology, Society for Pediatric Radiology, and Society of Radiologists in Ultrasound Fetal Imaging Workshop.
        Am J Obstet Gynecol. 2014; 210: 387-397
        • Schellen C.
        • Ernst S.
        • Gruber G.M.
        • et al.
        Fetal MRI detects early alterations of brain development in tetralogy of Fallot.
        Am J Obstet Gynecol. 2015; 213: 392.e1-392.e7
        • Sanz Cortes M.
        • Rivera A.M.
        • Yepez M.
        • et al.
        Clinical assessment and brain findings in a cohort of mothers, fetuses and infants infected with ZIKA virus.
        Am J Obstet Gynecol. 2018; 218: 440
        • Cohen-Sacher B.
        • Lerman-Sagie T.
        • Lev D.
        • Malinger G.
        Sonographic developmental milestones of the fetal cerebral cortex: a longitudinal study.
        Ultrasound Obstet Gynecol. 2006; 27: 494-502