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Research ArticlePediatric Neuroimaging
Open Access

Global and Regional Changes in Cortical Development Assessed by MRI in Fetuses with Isolated Nonsevere Ventriculomegaly Correlate with Neonatal Neurobehavior

N. Hahner, O.M. Benkarim, M. Aertsen, M. Perez-Cruz, G. Piella, G. Sanroma, N. Bargallo, J. Deprest, M.A. Gonzalez Ballester, E. Gratacos and E. Eixarch
American Journal of Neuroradiology September 2019, 40 (9) 1567-1574; DOI: https://doi.org/10.3174/ajnr.A6165
N. Hahner
aFrom the Fetal i+D Fetal Medicine Research Center (N.H., M.P.-C., E.G., E.E.), BCNatal–Barcelona Center for Maternal-Fetal and Neonatal Medicine (Hospital Clínic and Hospital Sant Joan de Déu), Institut Clínic de Ginecologia, Obstetricia i Neonatologia, Institut d'Investigacions Biomèdiques August Pi i Sunyer, Universitat de Barcelona, Barcelona, Spain
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O.M. Benkarim
eBCN MedTech (O.M.B., G.P., G.S., M.A.G.B.), Universitat Pompeu Fabra, Barcelona, Spain
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M. Aertsen
gDepartments of Radiology (M.A.)
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M. Perez-Cruz
aFrom the Fetal i+D Fetal Medicine Research Center (N.H., M.P.-C., E.G., E.E.), BCNatal–Barcelona Center for Maternal-Fetal and Neonatal Medicine (Hospital Clínic and Hospital Sant Joan de Déu), Institut Clínic de Ginecologia, Obstetricia i Neonatologia, Institut d'Investigacions Biomèdiques August Pi i Sunyer, Universitat de Barcelona, Barcelona, Spain
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G. Piella
eBCN MedTech (O.M.B., G.P., G.S., M.A.G.B.), Universitat Pompeu Fabra, Barcelona, Spain
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G. Sanroma
eBCN MedTech (O.M.B., G.P., G.S., M.A.G.B.), Universitat Pompeu Fabra, Barcelona, Spain
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N. Bargallo
cMagnetic Resonance Image Core Facility (N.B.), Institut d'Investigacions Biomediques August Pi i Sunyer, Barcelona, Spain
dDepartment of Radiology (N.B.), Centre de Diagnòstic per la Imatge, Hospital Clínic, Barcelona, Spain
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J. Deprest
hObstetrics (J.D.), UZ Leuven, Leuven, Belgium
iInstitute for Women's Health (J.D.), University College London, London, UK.
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M.A. Gonzalez Ballester
eBCN MedTech (O.M.B., G.P., G.S., M.A.G.B.), Universitat Pompeu Fabra, Barcelona, Spain
fICREA (M.A.G.B.), Barcelona, Spain
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E. Gratacos
aFrom the Fetal i+D Fetal Medicine Research Center (N.H., M.P.-C., E.G., E.E.), BCNatal–Barcelona Center for Maternal-Fetal and Neonatal Medicine (Hospital Clínic and Hospital Sant Joan de Déu), Institut Clínic de Ginecologia, Obstetricia i Neonatologia, Institut d'Investigacions Biomèdiques August Pi i Sunyer, Universitat de Barcelona, Barcelona, Spain
bCentre for Biomedical Research on Rare Diseases (E.G., E.E.), Barcelona, Spain
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E. Eixarch
aFrom the Fetal i+D Fetal Medicine Research Center (N.H., M.P.-C., E.G., E.E.), BCNatal–Barcelona Center for Maternal-Fetal and Neonatal Medicine (Hospital Clínic and Hospital Sant Joan de Déu), Institut Clínic de Ginecologia, Obstetricia i Neonatologia, Institut d'Investigacions Biomèdiques August Pi i Sunyer, Universitat de Barcelona, Barcelona, Spain
bCentre for Biomedical Research on Rare Diseases (E.G., E.E.), Barcelona, Spain
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    Fig 1.

    Assessment of sulcal depth and cortical grading. Sulcal depth: The bold white interhemispheric line is used as reference for all the measurements and the thin white line shows the measurement of the sulcus of interest, including the insula and Sylvian fissure (dotted line) in the axial transthalamic plane (A), parieto-occipital sulcus in the axial transventricular plane (B), cingulate sulcus in the coronal transthalamic view (C), and the calcarine sulcus in the coronal transcerebellar plane (D). Cortical grading: Curved lines indicate the areas, and arrows point out the sulci of interest. In the transthalamic plane frontal and temporal area (E), the Sylvian fissure and superior temporal sulcus were evaluated. In the transventricular plane (F), the parieto-occipital sulcus and frontal area were assessed, and in the plane superior to it (G), the central sulcus and frontal and parietal areas were assessed. The mesial area and cingulate sulcus were evaluated in the coronal transthalamic plane (H), and the calcarine sulcus was assessed in the coronal transcerebellar plane (I). Scheme: grading scale for Sylvian fissure (J), cortical areas (K) and sulci (L) by Pistorius et al.20

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    Fig 2.

    Steps of fetal brain MR imaging reconstruction and tissue segmentation. Columns A and B, The raw stacks, including the image obtained as a reference (Column A, axial, and Column B, coronal) and the orthogonal views (note the low quality of these images). Column C, The 3 orthogonal planes of the final reconstruction. Column D, The segmentation into cortical gray matter (green), white matter (blue), lateral ventricles (yellow), CSF outside the ventricles (red), cerebellum (turquoise), and brain stem (purple).

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    Fig 3.

    Brain tissue volumes in study groups. Cerebral tissue volumes including both hemispheres in INSVM (circles) and control (rhombuses) cohorts. A, Supratentorial volumes. B, Volumes of the lateral ventricles. C, Cortical gray matter volumes. D, White matter volumes. Volume measures are in cubic millimeters.

Tables

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    Table 1:

    Clinical characteristics of the study groupsa

    Controls (n = 29)INSVM (n = 32)P
    Maternal age (yr)33.7 ± 4.232.4 ± 5.5.32
    Birth weight (g)3414 ± 5173406 ± 553.96
    Gestational age at birth (wk)39.8 ± 0.939.8 ± 1.2.81
    Gestational age at MRI (wk)27.7 ± 0.927.7 ± 0.9.91
    Lateral ventricular widtha4.6 ± 1.410.6 ± 1.1<.01b
    Fetus sex.02d
        Male58.6% (17)87.5% (28)
        Female41.4% (12)12.5% (4)
    Laterality of ventriculomegaly
        Bilateral–34.4% (11)
        Unilateral left–34.4% (11)
        Unilateral right–31.2% (10)
    Evolution of lateral ventricular widthc
        Regressive–25% (8)
        Stable–75% (24)
        Progressive–0% (0)
    Classification according to atrial width
        Mild (10.0–11.9 mm)–84.3% (27)
        Moderate (12.0–13.9 mm)–16.7% (5)
    • Note:— – indicates that these characteristics do not apply for the control group.

    • ↵a Comparison of clinical characteristics between the control and case cohort. Results are expressed as means or percentage and number of subjects as appropriate.

    • ↵b Measurement of the more dilated lateral ventricle by ultrasound at diagnosis.

    • ↵c Evolution of lateral ventricular width until term of pregnancy.

    • ↵d Significant (≤.05).

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    Table 2:

    Sulcal depth and grading scores of the study groupsa

    VariableControls (n = 29)INSVM (n = 32)P
    Left hemisphere depths
        Insula29.4 ± 1.529.7 ± 1.8.03b
        Sylvian fissure16.7 ± 1.617.2 ± 2.4.15
        Parieto-occipital sulcus10.2 ± 2.38.1 ± 2.6<.01b
        Cingulate sulcus3.8 ± 1.34.3 ± 2.5.29
        Calcarine sulcus12.5 ± 2.710.9 ± 2.1<.01b
    Right hemisphere depths
        Insula29.6 ± 1.429.7 ± 1.7.04b
        Sylvian fissure16.8 ± 1.916.0 ± 1.6.01b
        Parieto-occipital sulcus11.1 ± 2.49.0 ± 2.8<.01b
        Cingulate sulcus3.6 ± 1.14.0 ± 1.5.33
        Calcarine sulcus13.5 ± 2.211.8 ± 4.8<.02b
    Sum of grading scores
        Left hemisphere21.1 ± 5.318.2 ± 5.1.01b
        Right hemisphere21.8 ± 5.119.6 ± 5.3.03b
        Total cortex42.9 ± 10.237.8 ± 9.9.01b
    • ↵a Comparison of sulcal depth measurements between the control and case cohort. Depth measurements (in millimeters) were normalized by BPD and multiplied by 100. Results are expressed as means. P values were adjusted by gestational age at examination and sex.

    • ↵b Values ≤ .05.

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N. Hahner, O.M. Benkarim, M. Aertsen, M. Perez-Cruz, G. Piella, G. Sanroma, N. Bargallo, J. Deprest, M.A. Gonzalez Ballester, E. Gratacos, E. Eixarch
Global and Regional Changes in Cortical Development Assessed by MRI in Fetuses with Isolated Nonsevere Ventriculomegaly Correlate with Neonatal Neurobehavior
American Journal of Neuroradiology Sep 2019, 40 (9) 1567-1574; DOI: 10.3174/ajnr.A6165

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Global and Regional Changes in Cortical Development Assessed by MRI in Fetuses with Isolated Nonsevere Ventriculomegaly Correlate with Neonatal Neurobehavior
N. Hahner, O.M. Benkarim, M. Aertsen, M. Perez-Cruz, G. Piella, G. Sanroma, N. Bargallo, J. Deprest, M.A. Gonzalez Ballester, E. Gratacos, E. Eixarch
American Journal of Neuroradiology Sep 2019, 40 (9) 1567-1574; DOI: 10.3174/ajnr.A6165
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