Login to MyKarger

New to MyKarger? Click here to sign up.



Login with Facebook

Forgot your password?

Authors, Editors, Reviewers

For Manuscript Submission, Check or Review Login please go to Submission Websites List.

Submission Websites List

Institutional Login
(Shibboleth or Open Athens)

For the academic login, please select your country in the dropdown list. You will be redirected to verify your credentials.

Original Paper

Cerebrospinal Fluid and Parenchymal Brain Development and Growth in the Healthy Fetus

Andescavage N.N.a, e · DuPlessis A.b, e · McCarter R.c · Vezina G.d, f · Robertson R.g, h · Limperopoulos C.b,d-f

Author affiliations

aDivision of Neonatology, bDivision of Fetal and Translational Medicine, cDivision of Biostatistics and Informatics, and dDivision of Diagnostic Imaging and Radiology, Children's National Health System, and Departments of ePediatrics and fRadiology, George Washington University School of Medicine, Washington, DC, gDepartment of Radiology, Children's Hospital Boston, Boston, MA, and hDepartment of Radiology, Harvard Medical School, Cambridge, MA, USA

Related Articles for ""

Dev Neurosci 2016;38:420-429

Do you have an account?

Login Information





Contact Information












By signing up for MyKarger you will automatically participate in our year-End raffle.
If you Then Do Not wish To participate, please uncheck the following box.

Yes, I wish To participate In the year-End raffle And Get the chance To win some Of our most interesting books, And other attractive prizes.


I have read the Karger Terms and Conditions and agree.



Login Information





Contact Information












By signing up for MyKarger you will automatically participate in our year-End raffle.
If you Then Do Not wish To participate, please uncheck the following box.

Yes, I wish To participate In the year-End raffle And Get the chance To win some Of our most interesting books, And other attractive prizes.


I have read the Karger Terms and Conditions and agree.



To view the fulltext, please log in

To view the pdf, please log in

Buy

  • FullText & PDF
  • Unlimited re-access via MyKarger
  • Unrestricted printing, no saving restrictions for personal use
read more

CHF 9.00 *
EUR 8.00 *
USD 9.00 *

Select

KAB

Buy a Karger Article Bundle (KAB) and profit from a discount!

If you would like to redeem your KAB credit, please log in.


Save over 20% compared to the individual article price.
Learn more

Rent/Cloud

  • Rent for 48h to view
  • Buy Cloud Access for unlimited viewing via different devices
  • Synchronizing in the ReadCube Cloud
  • Printing and saving restrictions apply

Rental: USD 8.50
Cloud: USD 20.00


Select

Subscribe

  • Access to all articles of the subscribed year(s) guaranteed for 5 years
  • Unlimited re-access via Subscriber Login or MyKarger
  • Unrestricted printing, no saving restrictions for personal use
read more

Subcription rates


Select

* The final prices may differ from the prices shown due to specifics of VAT rules.

Article / Publication Details

First-Page Preview
Abstract of Original Paper

Received: August 19, 2016
Accepted: January 17, 2017
Published online: March 18, 2017
Issue release date: June 2017

Number of Print Pages: 10
Number of Figures: 5
Number of Tables: 0

ISSN: 0378-5866 (Print)
eISSN: 1421-9859 (Online)

For additional information: https://www.karger.com/DNE

Abstract

Objective: The objective of this study was to apply quantitative magnetic resonance imaging to characterize absolute cerebrospinal fluid (CSF) development, as well as its relative development to fetal brain parenchyma in the healthy human fetus. Design: We created three-dimensional high-resolution reconstructions of the developing brain for healthy fetuses between 18 and 40 weeks' gestation, segmented the parenchymal and CSF spaces, and calculated the volumes for the lateral, third, and fourth ventricles; extra-axial CSF space; and the cerebrum, cerebellum, and brainstem. From these data, we constructed normograms of the resulting volumes according to gestational age and described the relative development of CSF to fetal brain parenchyma. Results: Each CSF space demonstrated major increases in volumetric growth during the second half of gestation: third ventricle (23-fold), extra-axial CSF (11-fold), fourth ventricle (8-fold), and lateral ventricle (2-fold). Total CSF volume was related to total brain volume (p < 0.01), as was lateral ventricle to cerebral volume (p < 0.01); however, the fourth ventricle was not related to cerebellar or brainstem volume (p = 0.18-0.19). Relevance: Abnormalities of the CSF spaces are the most common anomalies of neurologic development detected on fetal screening using neurosonography. Normative values of absolute CSF volume, as well as relative growth in comparison to intracranial parenchyma, provide valuable insight into normal fetal neurodevelopment. These data may provide important biomarkers of early deviations from normal growth, better distinguish between benign variants and early disease, and serve as reference standards for postnatal growth and development in the premature infant.

© 2017 S. Karger AG, Basel


References

  1. Ramos F, Maia S, Branco M, Raposo J, Sa J, Sousa S, et al: Accuracy of prenatal diagnosis in elective termination of pregnancy: 385 cases from 2000 to 2007. ISRN Obstet Gynecol 2011;2011:458120.
  2. Vaknin Z, Lahat Y, Barel O, Ben-Ami I, Reish O, Herman A, et al: Termination of pregnancy due to fetal abnormalities performed after 23 weeks' gestation: analysis of indications in 144 cases from a single medical center. Fetal Diagn Ther 2009;25:291-296.
  3. De Keersmaecker B, Claus F, De Catte L: Imaging the fetal central nervous system. Facts Views Vis Obgyn 2011;3:135-149.
  4. Pagani G, Thilaganathan B, Prefumo F: Neurodevelopmental outcome in isolated mild fetal ventriculomegaly: systematic review and meta-analysis. Ultrasound Obstet Gynecol 2014;44:254-260.
  5. Westerfield L, Darilek S, van den Veyver IB: Counseling challenges with variants of uncertain significance and incidental findings in prenatal genetic screening and diagnosis. J Clin Med 2014;3:1018-1032.
  6. Melchiorre K, Bhide A, Gika AD, Pilu G, Papageorghiou AT: Counseling in isolated mild fetal ventriculomegaly. Ultrasound Obstet Gynecol 2009;34:212-224.
  7. Girard N, Chaumoitre K, Chapon F, Pineau S, Barberet M, Brunel H: Fetal magnetic resonance imaging of acquired and developmental brain anomalies. Semin Perinatol 2009;33:234-250.
  8. Griffiths PD, Reeves MJ, Morris JE, Mason G, Russell SA, Paley MN, et al: A prospective study of fetuses with isolated ventriculomegaly investigated by antenatal sonography and in utero MR imaging. AJNR Am J Neuroradiol 2010;31:106-111.
  9. Limperopoulos C, Robertson RL, Estroff JA, Barnewolt C, Levine D, Bassan H, et al: Diagnosis of inferior vermian hypoplasia by fetal magnetic resonance imaging: potential pitfalls and neurodevelopmental outcome. Am J Obstet Gynecol 2006;194:1070-1076.
  10. Kim K, Habas PA, Rajagopalan V, Scott JA, Corbett-Detig JM, Rousseau F, et al: Bias field inconsistency correction of motion-scattered multislice MRI for improved 3D image reconstruction. IEEE Trans Med Imaging 2011;30:1704-1712.
  11. Rousseau F, Kim K, Studholme C, Koob M, Dietemann JL: On super-resolution for fetal brain MRI. Med Image Comput Comput Assist Interv 2010;13:355-362.
  12. Clouchoux C, Guizard N, Evans AC, du Plessis AJ, Limperopoulos C: Normative fetal brain growth by quantitative in vivo magnetic resonance imaging. Am J Obstet Gynecol 2012;206:173.e1-8.
  13. Gholipour A, Estroff JA, Barnewolt CE, Connolly SA, Warfield SK: Fetal brain volumetry through MRI volumetric reconstruction and segmentation. Int J Comput Assist Radiol Surg 2011;6:329-339.
  14. Habas PA, Kim K, Rousseau F, Glenn OA, Barkovich AJ, Studholme C: Atlas-based segmentation of developing tissues in the human brain with quantitative validation in young fetuses. Hum Brain Mapp 2010;31:1348-1358.
  15. Habas PA, Kim K, Corbett-Detig JM, Rousseau F, Glenn OA, Barkovich AJ, et al: A spatiotemporal atlas of MR intensity, tissue probability and shape of the fetal brain with application to segmentation. Neuroimage 2010;53:460-470.
  16. Scott JA, Habas PA, Kim K, Rajagopalan V, Hamzelou KS, Corbett-Detig JM, et al: Growth trajectories of the human fetal brain tissues estimated from 3D reconstructed in utero MRI. Int J Dev Neurosci 2011;29:529-536.
  17. Grossman R, Hoffman C, Mardor Y, Biegon A: Quantitative MRI measurements of human fetal brain development in utero. Neuroimage 2006;33:463-470.
  18. Corbett-Detig J, Habas PA, Scott JA, Kim K, Rajagopalan V, McQuillen PS, et al: 3D global and regional patterns of human fetal subplate growth determined in utero. Brain Struct Funct 2011;215:255-263.
  19. Kim K, Habas P, Rajagopalan V, Scott J, Corbett-Detig J, Rousseau F, et al: Non-iterative relative bias correction for 3D reconstruction of in utero fetal brain MR imaging. Conf Proc IEEE Eng Med Biol Soc 2010;2010:879-882.
  20. Gholipour A, Estroff JA, Warfield SK: Robust super-resolution volume reconstruction from slice acquisitions: application to fetal brain MRI. IEEE Trans Med Imaging 2010;29:1739-1758.
  21. Rousseau F, Gounot D, Studholme C: On high-resolution image estimation using low-resolution brain MRI. Conf Proc IEEE Eng Med Biol Soc 2013;2013:1081-1084.
  22. Henrich W, Stupin JH: 3D volume contrast imaging (VCI) for the visualization of placenta previa increta and uterine wall thickness in a dichorionic twin pregnancy. Ultraschall Med 2011;32:406-411.
  23. Gibson KS, Stetzer B, Catalano PM, Myers SA: Comparison of 2- and 3-Dimensional Sonography for Estimation of Birth Weight and Neonatal Adiposity in the Setting of Suspected Fetal Macrosomia. J Ultrasound Med 2016;35:1123-1129.
  24. Garel C: The role of MRI in the evaluation of the fetal brain with an emphasis on biometry, gyration and parenchyma. Pediatr Radiol 2004;34:694-699.
  25. Clouchoux C, Kudelski D, Gholipour A, Warfield SK, Viseur S, Bouyssi-Kobar M, et al: Quantitative in vivo MRI measurement of cortical development in the fetus. Brain Struct Funct 2012;217:127-139.
  26. Kostovic I, Vasung L: Insights from in vitro fetal magnetic resonance imaging of cerebral development. Semin Perinatol 2009;33:220-233.
  27. Limperopoulos C, Tworetzky W, McElhinney DB, Newburger JW, Brown DW, Robertson RL Jr, et al: Brain volume and metabolism in fetuses with congenital heart disease: evaluation with quantitative magnetic resonance imaging and spectroscopy. Circulation 2010;121:26-33.
  28. Vossough A, Limperopoulos C, Putt ME, du Plessis AJ, Schwab PJ, Wu J, et al: Development and validation of a semiquantitative brain maturation score on fetal MR images: initial results. Radiology 2013;268:200-207.
  29. Clouchoux C, du Plessis AJ, Bouyssi-Kobar M, Tworetzky W, McElhinney DB, Brown DW, et al: Delayed cortical development in fetuses with complex congenital heart disease. Cereb Cortex 2013;23:2932-2943.
  30. Rousseau F, Oubel E, Pontabry J, Schweitzer M, Studholme C, Koob M, et al: BTK: an open-source toolkit for fetal brain MR image processing. Comput Methods Programs Biomed 2013;109:65-73.
  31. Serag A, Kyriakopoulou V, Rutherfod MA, Edwards AD, Hajnal JV, Aljabar P, Counsel SJ, Boardmen JP, Rueckert D: A multi-channel 4D probabilistic atlas of the devloping brain: application to fetuses and neonates. The British Machine Vision Association and Society for Pattern Recognition 2012;2012:1-14.
  32. Tustison NJ, Avants BB, Cook PA, Zheng Y, Egan A, Yushkevich PA, et al: N4ITK: improved N3 bias correction. IEEE Trans Med Imaging 2010;29:1310-1320.
  33. Serag A, Aljabar P, Ball G, Counsell SJ, Boardman JP, Rutherford MA, et al: Construction of a consistent high-definition spatio-temporal atlas of the developing brain using adaptive kernel regression. Neuroimage 2012;59:2255-2265.
  34. Rueckert D, Sonoda L, Hayes C, Hill DLG, Leach MO, Hawkes DJ: Nonrigid registration using free-form deformations. IEEE Trans Image Process 1999;18:712-721.
  35. Bradley CJ: The Algebra of Geometry: Cartesian, Areal and Projective Co-ordinates. Bath, Highperception Ltd, 2007.
  36. Kuklisova-Murgasova M, Aljabar P, Srinivasan L, Counsell SJ, Doria V, Serag A, et al: A dynamic 4D probabilistic atlas of the developing brain. Neuroimage 2011;54:2750-2763.
  37. Yushkevich PA, Piven J, Hazlett HC, Smith RG, Ho S, Gee JC, et al: User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 2006;31:1116-1128.
  38. Wax JR, Bookman L, Cartin A, Pinette MG, Blackstone J: Mild fetal cerebral ventriculomegaly: diagnosis, clinical associations, and outcomes. Obstet Gynecol Surv 2003;58:407-414.
  39. Melchiorre K, Liberati M, Celentano C, Domizio S, Puglielli C, Buoni S, et al: Neurological outcome following isolated 10-12 mm fetal ventriculomegaly. Arch Dis Child Fetal Neonatal Ed 2009;94:F311-F312.
  40. Garel C: MRI of the Fetal Brain: Normal Development and Cerebral Pathologies. Berlin, Springer, 2004.
  41. Scott JA, Habas PA, Rajagopalan V, Kim K, Barkovich AJ, Glenn OA, et al: Volumetric and surface-based 3D MRI analyses of fetal isolated mild ventriculomegaly: brain morphometry in ventriculomegaly. Brain Struct Funct 2013;218:645-655.
  42. Gholipour A, Akhondi-Asl A, Estroff JA, Warfield SK: Multi-atlas multi-shape segmentation of fetal brain MRI for volumetric and morphometric analysis of ventriculomegaly. Neuroimage 2012;60:1819-1831.
  43. Nadel AS, Benacerraf BR: Lateral ventricular atrium: larger in male than female fetuses. Int J Gynaecol Obstet 1995;51:123-126.
  44. McAllister JP 2nd: Pathophysiology of congenital and neonatal hydrocephalus. Semin Fetal Neonatal Med 2012;17:285-294.
  45. McKechnie L, Vasudevan C, Levene M: Neonatal outcome of congenital ventriculomegaly. Semin Fetal Neonatal Med 2012;17:301-307.
  46. Gandolfi Colleoni G, Contro E, Carletti A, Ghi T, Campobasso G, Rembouskos G, et al: Prenatal diagnosis and outcome of fetal posterior fossa fluid collections. Ultrasound Obstet Gynecol 2012;39:625-631.
  47. Wood NS, Marlow N, Costeloe K, Gibson AT, Wilkinson AR: Neurologic and developmental disability after extremely preterm birth. EPICure Study Group. N Engl J Med 2000;343:378-384.
  48. Volpe JJ: Neurology of the Newborn, ed 5. Philadelphia, Saunders/Elsevier, 2008, vol xiv, p 1094.
  49. Mukerji A, Shah V, Shah PS: Periventricular/intraventricular hemorrhage and neurodevelopmental outcomes: a meta-analysis. Pediatrics 2015;136:1132-1143.
  50. Beaino G, Khoshnood B, Kaminski M, Pierrat V, Marret S, Matis J, et al: Predictors of cerebral palsy in very preterm infants: the EPIPAGE prospective population-based cohort study. Dev Med Child Neurol 2010;52:e119-e125.
  51. Bolisetty S, Dhawan A, Abdel-Latif M, Bajuk B, Stack J, Lui K: Intraventricular hemorrhage and neurodevelopmental outcomes in extreme preterm infants. Pediatrics 2014;133:55-62.
  52. Limperopoulos C, Robertson RL, Sullivan NR, Bassan H, du Plessis AJ: Cerebellar injury in term infants: clinical characteristics, magnetic resonance imaging findings, and outcome. Pediatr Neurol 2009;41:1-8.
  53. Christian EA, Jin DL, Attenello F, Wen T, Cen S, Mack WJ, et al: Trends in hospitalization of preterm infants with intraventricular hemorrhage and hydrocephalus in the United States, 2000-2010. J Neurosurg Pediatr 2016;17:260-269.
  54. Shooman D, Portess H, Sparrow O: A review of the current treatment methods for posthaemorrhagic hydrocephalus of infants. Cerebrospinal Fluid Res 2009;6:1.
  55. Laptook AR, O'Shea TM, Shankaran S, Bhaskar B: Adverse neurodevelopmental outcomes among extremely low birth weight infants with a normal head ultrasound: prevalence and antecedents. Pediatrics 2005;115:673-680.
  56. Marlow N, Wolke D, Bracewell MA, Samara M: Neurologic and developmental disability at six years of age after extremely preterm birth. N Engl J Med 2005;352:9-19.
  57. Hack M: Young adult outcomes of very-low-birth-weight children. Semin Fetal Neonatal Med 2006;11:127-137.
  58. Johnson S, Fawke J, Hennessy E, Rowell V, Thomas S, Wolke D, et al: Neurodevelopmental disability through 11 years of age in children born before 26 weeks of gestation. Pediatrics 2009;124:e249-e257.
  59. Huppi PS, Schuknecht B, Boesch C, Bossi E, Felblinger J, Fusch C, et al: Structural and neurobehavioral delay in postnatal brain development of preterm infants. Pediatr Res 1996;39:895-901.
  60. Peterson BS, Anderson AW, Ehrenkranz R, Staib LH, Tageldin M, Colson E, et al: Regional brain volumes and their later neurodevelopmental correlates in term and preterm infants. Pediatrics 2003;111:939-948.

Article / Publication Details

First-Page Preview
Abstract of Original Paper

Received: August 19, 2016
Accepted: January 17, 2017
Published online: March 18, 2017
Issue release date: June 2017

Number of Print Pages: 10
Number of Figures: 5
Number of Tables: 0

ISSN: 0378-5866 (Print)
eISSN: 1421-9859 (Online)

For additional information: https://www.karger.com/DNE


Copyright / Drug Dosage / Disclaimer

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.