Fetal indusium griseum is a possible biomarker of the regularity of brain midline development in 3T MR imaging: A retrospective observational study.
corpus callosum
extracellular matrix
indusium griseum
malformations of cortical development
prenatal diagnosis
subplate
ultrasound
Journal
Acta obstetricia et gynecologica Scandinavica
ISSN: 1600-0412
Titre abrégé: Acta Obstet Gynecol Scand
Pays: United States
ID NLM: 0370343
Informations de publication
Date de publication:
09 Feb 2024
09 Feb 2024
Historique:
revised:
04
12
2023
received:
21
09
2023
accepted:
03
01
2024
medline:
10
2
2024
pubmed:
10
2
2024
entrez:
10
2
2024
Statut:
aheadofprint
Résumé
This study aimed to assess the visibility of the indusium griseum (IG) in magnetic resonance (MR) scans of the human fetal brain and to evaluate its reliability as an imaging biomarker of the normality of brain midline development. The retrospective observational study encompassed T2-w 3T MR images from 90 post-mortem fetal brains and immunohistochemical sections from 41 fetal brains (16-40 gestational weeks) without cerebral pathology. Three raters independently inspected and evaluated the visibility of IG in post-mortem and in vivo MR scans. Weighted kappa statistics and regression analysis were used to determine inter- and intra-rater agreement and the type and strength of the association of IG visibility with gestational age. The visibility of the IG was the highest between the 25 and 30 gestational week period, with a very good inter-rater variability (kappa 0.623-0.709) and excellent intra-rater variability (kappa 0.81-0.93). The immunochemical analysis of the histoarchitecture of IG discloses the expression of highly hydrated extracellular molecules in IG as the substrate of higher signal intensity and best visibility of IG during the mid-fetal period. The knowledge of developmental brain histology and fetal age allows us to predict the IG-visibility in magnetic resonance imaging (MRI) and use it as a biomarker to evaluate the morphogenesis of the brain midline. As a biomarker, IG is significant for post-mortem pathological examination by MRI. Therefore, in the clinical in vivo imaging examination, IG should be anticipated when an assessment of the brain midline structures is needed in mid-gestation, including corpus callosum thickness measurements.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Austrian Science Fund (FWF)
ID : FWF grant: I 3925-B27
Organisme : Medicinski Fakultet, Sveučilište u Zagrebu
ID : 10106-22-3116
Organisme : Medicinski Fakultet, Sveučilište u Zagrebu
ID : 10106-23-2487
Organisme : Medicinski Fakultet, Sveučilište u Zagrebu
ID : BM0054
Organisme : Hrvatska Zaklada za Znanost
ID : IP-2019-04-3182
Organisme : European Regional Development Fund
ID : GA KK01.1.1.01.0007
Informations de copyright
© 2024 The Authors. Acta Obstetricia et Gynecologica Scandinavica published by John Wiley & Sons Ltd on behalf of Nordic Federation of Societies of Obstetrics and Gynecology (NFOG).
Références
Di Ieva A, Fathalla H, Cusimano MD, Tschabitscher M. The indusium griseum and the longitudinal striae of the corpus callosum. Cortex. 2015;62:34-40.
Ren T, Anderson A, Shen WB, et al. Imaging, anatomical, and molecular analysis of callosal formation in the developing human fetal brain. Anat Rec A Discov Mol Cell Evol Biol. 2006;288(2):191-204.
Bobić Rasonja M, Orešković D, Knezović V, et al. Histological and MRI study of the development of the human Indusium Griseum. Cereb Cortex. 2019;29(11):4709-4724.
Abbie AA. Cortical lamination in the Monotremata. J Comp Neurol. 1940;72(3):429-467.
Sturrock RR. Development of the indusium griseum. II. A semithin light microscopic and electron microscopic study. J Anat. 1978;125(Pt 3):433-445.
Wyss JM, Sripanidkulchai K. The indusium griseum and anterior hippocampal continuation in the rat. J Comp Neurol. 1983;219(3):251-272.
Ino T, Yasui Y, Itoh K, et al. Direct projections from Ammon's horn to the septum in the cat. Exp Brain Res. 1987;68(1):179-188.
Kunzle H. The hippocampal continuation (indusium griseum): its connectivity in the hedgehog tenrec and its status within the hippocampal formation of higher vertebrates. Anat Embryol. 2004;208(3):183-213.
Jinno S, Klausberger T, Marton LF, et al. Neuronal diversity in GABAergic long-range projections from the hippocampus. J Neurosci. 2007;27(33):8790-8804.
Laplante F, Mnie-Filali O, Sullivan RM. A neuroanatomical and neurochemical study of the indusium griseum and anterior hippocampal continuation: comparison with dentate gyrus. J Chem Neuroanat. 2013;50-51:39-47.
Kier EL, Fulbright RK, Bronen RA. Limbic lobe embryology and anatomy: dissection and MR of the medial surface of the fetal cerebral hemisphere. Am J Neuroradiol. 1995;16(9):1847-1853.
Tubbs RS, Prekupec M, Loukas M, Hattab EM, Cohen-Gadol AA. The indusium griseum: anatomic study with potential application to callosotomy. Neurosurgery. 2013;73(2):312-315; discussion 316.
Sturrock RR. Development of the indusium griseum. I. A quantitative light microscopic study of neurons and glia. J Anat. 1978;125(Pt 2):293-298.
Sanders M, Petrasch-Parwez E, Habbes HW, Düring MV, Förster E. Postnatal developmental expression profile classifies the Indusium Griseum as a distinct subfield of the hippocampal formation. Front Cell Dev Biol. 2021;8:615571.
Lippa CF, Smith TW. The indusium griseum in Alzheimer's disease: an immunocytochemical study. J Neurol Sci. 1992;111(1):39-45.
Fuzik J, Rehman S, Girach F, et al. Brain-wide genetic mapping identifies the indusium griseum as a prenatal target of pharmacologically unrelated psychostimulants. Proc Natl Acad Sci U S A. 2019;116(51):25958-25967.
Richards LJ, Plachez C, Ren T. Mechanisms regulating the development of the corpus callosum and its agenesis in mouse and human. Clin Genet. 2004;66(4):276-289.
Jovanov-Milošević N, Benjak V, Kostović I. Transient cellular structures in developing corpus callosum of the human brain. Coll Antropol. 2006;30(2):375-381.
Jovanov-Milošević N, Čuljat M, Kostović I. Growth of the human corpus callosum: modular and laminar morphogenetic zones. Front Neuroanat. 2009;3:6.
Jovanov-Milošević N, Petanjek Z, Petrović D, Judaš M, Kostović I. Morphology, molecular phenotypes and distribution of neurons in developing human corpus callosum. Eur J Neurosci. 2010;32(9):1423-1432.
Culjat M, Milošević NJ. Callosal septa express guidance cues and are paramedian guideposts for human corpus callosum development. J Anat. 2019;235(3):670-686.
Paul LK. Developmental malformation of the corpus callosum: a review of typical callosal development and examples of developmental disorders with callosal involvement. J Neurodev Disord. 2011;3(1):3-27.
Mark LP, Daniels DL, Naidich TP, Borne JA. Limbic system anatomy: an overview. Am J Neuroradiol. 1993;14(2):349-352.
Nakada T. High-field, high-resolution MR imaging of the human indusium griseum. Am J Neuroradiol. 1999;20(3):524-525.
Bayer S, Altman J. The Human Brain During the Second Trimester. CRC Press, Francis and Taylor Group; 2005.
Ebner M, Wang G, Li W, et al. An automated framework for localization, segmentation and super-resolution reconstruction of fetal brain MRI. NeuroImage. 2020;206:116324.
Jovanov Milošević N, Judaš M, Aronica E, Kostovic I. Neural ECM in laminar organization and connectivity development in healthy and diseased human brain. Prog Brain Res. 2014;214:159-178.
Luna LG. Chapter 10: methods for carbohydrates and Mucoproteins. In: Luna LG, ed. Manual of Histologic Staining Methods of the Armed Forces Institute of Pathology. 3rd ed. McGraw-Hill Book Company; 1968.
Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics. 1977;33(1):159-174.
Corroenne G, Grevent D, Kasprian G, et al. Corpus callosal reference ranges: systematic review of methodology of biometric chart construction and measurements obtained. Ultrasound Obstet Gynecol. 2023;62:175-184.
Barkovich AJ, Kjos BO. Normal postnatal development of the corpus callosum as demonstrated by MR imaging. Am J Neuroradiol. 1988;9(3):487-491.
Rakic P, Yakovlev PI. Development of the corpus callosum and cavum septi in man. J Comp Neurol. 1968;132(1):45-72.
Malinger G, Zakut H. The corpus callosum: normal fetal development as shown by transvaginal sonography. AJR Am J Roentgenol. 1993;161(5):1041-1043.
Pashaj S, Merz E, Wellek S. Biometry of the fetal corpus callosum by three-dimensional ultrasound: biometry of the fetal corpus callosum. Ultrasound Obstet Gynecol. 2013;42(6):691-698.
Lerman-Sagie T, Ben-Sira L, Achiron R, et al. Thick fetal corpus callosum: an ominous sign? Ultrasound Obstet Gynecol. 2009;34(1):55-61.
Rollins NK. Diffusion imaging of the congenitally thickened corpus callosum. Am J Neuroradiol. 2013;34(3):660-665.
Schwartz E, Diogo MC, Glatter S, et al. The prenatal morphomechanic impact of agenesis of the corpus callosum on human brain structure and asymmetry. Cereb Cortex. 2021;31(9):4024-4037.
Wang X, Pettersson DR, Studholme C, Kroenke CD. Characterization of laminar zones in the mid-gestation primate brain with magnetic resonance imaging and histological methods. Front Neuroanat. 2015;9:147.
Widjaja E, Geibprasert S, Zarei Mahmoodabadi S, Brown NE, Shannon P. Corroboration of normal and abnormal fetal cerebral lamination on post-mortem MR imaging with post-mortem examination. Am J Neuroradiol. 2010;31(10):1987-1993.
Wang R, Dai G, Takahashi E. High-resolution MRI reveals detailed layer structures in early human fetal stages: in vitro study with histologic correlation. Front Neuroanat. 2015;9:150.