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Research ArticlePediatrics

New Ultrasound Measurements to Bridge the Gap between Prenatal and Neonatal Brain Growth Assessment

I.V. Koning, J.A. Roelants, I.A.L. Groenenberg, M.J. Vermeulen, S.P. Willemsen, I.K.M. Reiss, P.P. Govaert, R.P.M. Steegers-Theunissen and J. Dudink
American Journal of Neuroradiology September 2017, 38 (9) 1807-1813; DOI: https://doi.org/10.3174/ajnr.A5278
I.V. Koning
aFrom the Department of Obstetrics and Gynecology (I.V.K., J.A.R., I.A.L.G., S.P.W., R.P.M.S.-T.), Division of Obstetrics and Prenatal Medicine
cDepartment of Pediatrics (I.V.K., J.A.R., M.J.V., I.K.M.R., P.P.G., R.P.M.S.-T., J.D.), Division of Neonatology, Erasmus MC–Sophia Children's Hospital, Rotterdam, the Netherlands
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J.A. Roelants
aFrom the Department of Obstetrics and Gynecology (I.V.K., J.A.R., I.A.L.G., S.P.W., R.P.M.S.-T.), Division of Obstetrics and Prenatal Medicine
cDepartment of Pediatrics (I.V.K., J.A.R., M.J.V., I.K.M.R., P.P.G., R.P.M.S.-T., J.D.), Division of Neonatology, Erasmus MC–Sophia Children's Hospital, Rotterdam, the Netherlands
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I.A.L. Groenenberg
aFrom the Department of Obstetrics and Gynecology (I.V.K., J.A.R., I.A.L.G., S.P.W., R.P.M.S.-T.), Division of Obstetrics and Prenatal Medicine
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M.J. Vermeulen
cDepartment of Pediatrics (I.V.K., J.A.R., M.J.V., I.K.M.R., P.P.G., R.P.M.S.-T., J.D.), Division of Neonatology, Erasmus MC–Sophia Children's Hospital, Rotterdam, the Netherlands
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S.P. Willemsen
aFrom the Department of Obstetrics and Gynecology (I.V.K., J.A.R., I.A.L.G., S.P.W., R.P.M.S.-T.), Division of Obstetrics and Prenatal Medicine
bDepartment of Biostatistics (S.P.W.), Erasmus MC, University Medical Center, Rotterdam, the Netherlands
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I.K.M. Reiss
cDepartment of Pediatrics (I.V.K., J.A.R., M.J.V., I.K.M.R., P.P.G., R.P.M.S.-T., J.D.), Division of Neonatology, Erasmus MC–Sophia Children's Hospital, Rotterdam, the Netherlands
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P.P. Govaert
cDepartment of Pediatrics (I.V.K., J.A.R., M.J.V., I.K.M.R., P.P.G., R.P.M.S.-T., J.D.), Division of Neonatology, Erasmus MC–Sophia Children's Hospital, Rotterdam, the Netherlands
dDepartment of Neonatology (P.P.G.), ZNA Koningin Paola Ziekenhuis, Antwerp, Belgium
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R.P.M. Steegers-Theunissen
aFrom the Department of Obstetrics and Gynecology (I.V.K., J.A.R., I.A.L.G., S.P.W., R.P.M.S.-T.), Division of Obstetrics and Prenatal Medicine
cDepartment of Pediatrics (I.V.K., J.A.R., M.J.V., I.K.M.R., P.P.G., R.P.M.S.-T., J.D.), Division of Neonatology, Erasmus MC–Sophia Children's Hospital, Rotterdam, the Netherlands
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J. Dudink
cDepartment of Pediatrics (I.V.K., J.A.R., M.J.V., I.K.M.R., P.P.G., R.P.M.S.-T., J.D.), Division of Neonatology, Erasmus MC–Sophia Children's Hospital, Rotterdam, the Netherlands
eDepartment of Neonatology (J.D.), Wilhelmina's Children's Hospital, University Medical Center Utrecht, Utrecht, the Netherlands.
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    Fig 1.

    Prenatal measurement of CC and CCF lengths. 1, Corpus callosum length, outer-outer border. 2, Corpus callosum–fastigium length, from the genu of the corpus callosum to the fastigium (roof of the fourth ventricle).

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    Fig 2.

    Growth curves. A, Reference curves between 22 and 42 weeks of gestation for CCF (left) and CC (right) length, with the 5th, 10th, 50th, 90th, and 95th percentiles. B, Individual growth trajectories of CCF (left) and CC (right) length between 22 and 42 weeks of gestation. C, Growth trajectories for controls (black) and fetuses with FGR (striped blue) and CHD (dotted red).

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    Table 1:

    Baseline characteristicsa

    CharacteristicsControls (n = 157)FGR (n = 22)CHD (n = 20)Missing
    Maternal
        Age at enrollment (yr)32.3 (21–44)29.7 (21–41)33.0 (22–48)7
        Nulliparous69 (44)13 (68)11 (58)6
        Mode of conception (IVF/ICSI)48 (31)2 (10)2 (11)3
        Geographic background6
            Western126 (81)15 (79)18 (90)
            Non-Western29 (19)4 (21)2 (10)
        Educational level8
            Low20 (13)4 (20)0
            Intermediate56 (36)12 (60)7 (39)
            High79 (51)4 (20)11 (61)
    Prepregnancy BMI (kg/m2)22.9 (15.2–39.7)22.9 (17.6–43.4)23.4 (18.0–35.8)19
    Periconception folic acid initiation (yes)149 (96)15 (79)18 (95)6
    Periconception smoking (yes)25 (16)3 (16)3 (16)8
    Periconception alcohol consumption (yes)44 (29)4 (21)10 (53)9
    Neonatal
        Birth weight (g)3345 (2035–4380)1400 (400–2900)3420 (1650–4140)2
        Gestational age at birth (wk)39+1 (37+0–41+5)34+2 (26+3–39+3)38+6 (28+4–41+5)2
        Males82 (52)11 (50)13 (65)0
    • Note:—BMI indicates body mass index; IVF/ICSI, in vitro fertilization with or without intracytoplasmic sperm injection; ICSI, intracytoplasmic sperm injection.

    • ↵a Data are presented as median and range or number and percentage. Missing data were due to incomplete questionnaires.

    • View popup
    Table 2:

    Success rates and means of corpus callosum and corpus callosum–fastigium length per gestational agea

    Length (mm)/GA (wk)US Scans (No.)Measurements (No.)Success Rate (%)Mean (SD) (mm)
    CC
        221661247526.35 (1.22)
        261881387334.33 (1.86)
        321881156141.56 (2.19)
        421431389748.09 (3.15)
    CCF
        22124897233.09 (1.61)
        26138825939.39 (1.92)
        32115817045.86 (2.07)
        421431389752.26 (3.12)
    • ↵a Presented are the success rates, means, and corresponding SD values of the CC and CCF measurements per full week of gestation. The success rates for CC length and postnatal CCF length were calculated by the number of successful measurements divided by the total number of US images. Success rates of prenatal CCF measurements were calculated by dividing the number of successful CCF measurements by the number of midsagittal images eligible for CC length.

    • View popup
    Table 3:

    Intraobserver and interobserver reliability for prenatal measurements of corpus callosum and corpus callosum–fastigium lengtha

    Absolute DifferenceRelative DifferenceICC
    Mean Difference (mm)95% CI Mean Difference (mm)P95% Limits of Agreement (mm)Mean Difference (%)95% Limits of Agreement (%)
    Intraobserver
        CC0.011−0.228 to 0.250.923−1.373, 1.3960.1−4.1, 4.3>0.99
        CCF0.180−0.157 to 0.517.284−1.711, 2.0710.4−4.7, 5.4>0.99
    Interobserver
        CC−1.109−1.702 to −0.515.001−4.546, 2.329−3.4−14.9, 8.10.97
        CCF−0.125−0.741 to 0.492.684−3.589, 3.340−0.4−9.5, 8.60.97
    • Note:—ICC indicates intraclass correlation coefficient.

    • ↵a Intra- and interobserver reliability analyses for prenatal CC and CCF measurements in a random selection of 30 ultrasound scans.

    • View popup
    Table 4:

    Linear mixed models—growth trajectories of CC and CCF influenced by the presence of fetal growth restriction and congenital heart defectsa

    Model 1Model 2
    β95% CIP Valueβ95% CIP Value
    CC
        FGR−2.384−3.26 to −1.505<.01b−2.295−3.320 to −1.270<.01b
        CHD−1.252−1.954 to −0.549<.01b−1.267−1.972 to −0.562<.01b
    CCF
        FGR−1.413−2.500 to −0.326.01b−1.295−2.595 to 0.003.05
        CHD0.012−0.829 to 0.963.980.000−0.835 to 0.835.99
    • ↵a Data are presented in β values with corresponding 95% CI and P values, compared with controls. Model 1 represents the crude model with GA and its polynomials as predictor and type of case as covariate of interest. Model 2 is the fully adjusted model for the covariates in model 1 and for serial measurements of fetal weight and sex.

    • ↵b Significant.

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American Journal of Neuroradiology: 38 (9)
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I.V. Koning, J.A. Roelants, I.A.L. Groenenberg, M.J. Vermeulen, S.P. Willemsen, I.K.M. Reiss, P.P. Govaert, R.P.M. Steegers-Theunissen, J. Dudink
New Ultrasound Measurements to Bridge the Gap between Prenatal and Neonatal Brain Growth Assessment
American Journal of Neuroradiology Sep 2017, 38 (9) 1807-1813; DOI: 10.3174/ajnr.A5278

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New Ultrasound Measurements to Bridge the Gap between Prenatal and Neonatal Brain Growth Assessment
I.V. Koning, J.A. Roelants, I.A.L. Groenenberg, M.J. Vermeulen, S.P. Willemsen, I.K.M. Reiss, P.P. Govaert, R.P.M. Steegers-Theunissen, J. Dudink
American Journal of Neuroradiology Sep 2017, 38 (9) 1807-1813; DOI: 10.3174/ajnr.A5278
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