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Research ArticlePediatric Neuroimaging

Development of an Ultrasound Scoring System to Describe Brain Maturation in Preterm Infants

A. Stein, E. Sody, N. Bruns and U. Felderhoff-Müser
American Journal of Neuroradiology June 2023, DOI: https://doi.org/10.3174/ajnr.A7909
A. Stein
aFrom the Department of Pediatrics I, Neonatology, University Duisburg-Essen, University Hospital Essen, Essen, Germany
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E. Sody
aFrom the Department of Pediatrics I, Neonatology, University Duisburg-Essen, University Hospital Essen, Essen, Germany
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N. Bruns
aFrom the Department of Pediatrics I, Neonatology, University Duisburg-Essen, University Hospital Essen, Essen, Germany
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U. Felderhoff-Müser
aFrom the Department of Pediatrics I, Neonatology, University Duisburg-Essen, University Hospital Essen, Essen, Germany
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  • FIG 1.
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    FIG 1.

    Flowchart of patient recruitment.

  • FIG 2.
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    FIG 2.

    Ultrasound identification of the structures evaluated for the USBD in an infant with a PMA of 26 weeks. A, Midcoronal view at the level of the foramina of Monro: interopercular opening* (1), height of the insular cortex—curved measurement (2) and straight measurement* (3), depth of the Sylvian fissure (4), thickness of the corpus callosum (5), height of the cingulate gyrus (6), depth of cingulate sulcus* (7). B, Midsagittal view: circumferent length of corpus callosum (8), thickness of corpus callosum (midsagittal) at the genu (9a) and at the body (9b), and height of cingulate gyrus (10). Asterisks indicate structures selected for the USBD (bold lines, A).

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    FIG 3.

    Progression of opercularization with lengthening of insular cortex and closure of interopercular opening in the midcoronal view at different PMAs. A, PMA 22 + 6/7 weeks. B, PMA 30 + 0/7 weeks. C, PMA 34 + 2/7 weeks.

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    FIG 4.

    Scatterplot of measurements of selected structures for the USBD and trajectories with 25th and 75th percentiles, regression curves, and selected cutoff values for USBD marked as lines. A, Interopercular opening. B, Height of insular cortex. C, Depth of cingulate sulcus in the midcoronal plane.

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    FIG 5.

    Boxplot of USBD score points by postmenstrual age grouped by day of scan: light gray including only scorable scans from DOL 1–3 (n = 88); dark gray including all scorable scans (n = 312).

Tables

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    Table 1:

    Patient characteristics

    VariablePatients (n = 94)
    Sex (No.)Male48
    Female46
    PMA at birth (weeks)aMean27.8 (SD, 2.2)
    Range (min–max)23 + 3/7 to 32 + 0/7
    PMA at time of scan (weeks)Mean30.9 (SD, 3.4)
    Range (min–max)23 + 4/7 to 39 + 1/7
    Birth weight (g)Mean1034 (SD, 349)
    Range (min–max)340–1810
    Birth weight percentile< 3rd (No.) (%)3 (3.2%)
    3rd to 10th (No.) (%)16 (17.0%)
    Head circumference at birth (cm)Mean25.3 (SD, 2.7)
    Range (min–max)18.4–31.0
    Head circumference at birth percentile< 3rd (No.) (%)2 (2.1%)
    3rd to 10th (No.) (%)21 (22.3%)
    • Note:—Min indicates minimum; max, maximum.

    • ↵a PMA at birth was determined by ultrasound measurement of fetal crown rump length in the first trimester.

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    Table 2:

    Linear regression analysis of the measured structure and PMA at time of scan

    No.RβP Value
    Interopercular openinga343–0.74–0.06<.001
    Height of insular cortex, curved measurement3430.840.09<.001
    Height of insular cortex, straight measurementa3430.850.09<.001
    Depth of Sylvian fissure3410.190.06<.001
    Thickness of CC (midcoronal)3420.260.003<.001
    Height of cingulate gyrus (midcoronal)3130.720.06<.001
    Depth of cingulate sulcusa3150.830.05<.001
    Circumferent length of CC3110.680.17<.001
    Thickness of CC (midsagittal)
     Genu3350.320.01<.001
     Body3390.180.002<.001
    Height of cingulate gyrus (midsagittal)2600.440.02<.001
    Total USBD (all scans)3120.880.43<.001
    Total USBD (DOL 1–3)870.760.41<.001
    • Note:—No. indicates the number of scans in which the structure could be measured; CC, corpus callosum.

    • ↵a Structures selected for the USBD.

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    Table 3:

    USBDa

    Score Points012
    Interopercular opening (cm)≥ 0.550.15–0.54< 0.15
    Height of insular cortex (cm)≤ 1.251.26–1.74≥ 1.75
    Depth of cingulate sulcus (cm)< 0.100.11–0.44≥ 0.45
    • ↵a Score points from each structure add to a total score, which can range from a minimum of 0 points to a maximum of 6 points (a higher total score reflects a higher PMA).

    • View popup
    Table 4:

    PMA mean and range for each USBD score value

    ScoreNo. of Scans with Score AssignedPMA (Weeks)(mean)PMA (Weeks)(range)
    02025.8 (SD, 1.4)23 + 4/7 to 29 + 0/7
    12526.9 (SD, 1.6)23 + 5/7 to 29 + 5/7
    25328.9 (SD, 1.3)25 + 0/7 to 32 + 0/7
    35630.4 (SD, 1.5)27 + 0/7 to 35 + 0/7
    46732.1 (SD, 1.6)27 + 1/7 to 36 + 0/7
    56734.4 (SD, 1.9)30 + 2/7 to 39 + 1/7
    62436.1 (SD, 1.6)33 + 2/7 to 39 + 1/7
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Cite this article
A. Stein, E. Sody, N. Bruns, U. Felderhoff-Müser
Development of an Ultrasound Scoring System to Describe Brain Maturation in Preterm Infants
American Journal of Neuroradiology Jun 2023, DOI: 10.3174/ajnr.A7909

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Development of an Ultrasound Scoring System to Describe Brain Maturation in Preterm Infants
A. Stein, E. Sody, N. Bruns, U. Felderhoff-Müser
American Journal of Neuroradiology Jun 2023, DOI: 10.3174/ajnr.A7909
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