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Research ArticlePediatric Neuroimaging
Open Access

Automating Quantitative Measures of an Established Conventional MRI Scoring System for Preterm-Born Infants Scanned between 29 and 47 Weeks’ Postmenstrual Age

L. van Eijk, M. Seidel, K. Pannek, J.M. George, S. Fiori, A. Guzzetta, A. Coulthard, J. Bursle, R.S. Ware, D. Bradford, S. Rose, P.B. Colditz, R.N. Boyd and J. Fripp
American Journal of Neuroradiology August 2021, DOI: https://doi.org/10.3174/ajnr.A7230
L. van Eijk
aFrom The Australian e-Health Research Centre (L.v.E., M.S., K.P., D.B., S.R., J.F.), Health and Biosecurity, Commonwealth Scientific and Industrial Research Organisation, Brisbane, Australia
bFaculty of Medicine (L.v.E., M.S.)
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M. Seidel
aFrom The Australian e-Health Research Centre (L.v.E., M.S., K.P., D.B., S.R., J.F.), Health and Biosecurity, Commonwealth Scientific and Industrial Research Organisation, Brisbane, Australia
bFaculty of Medicine (L.v.E., M.S.)
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K. Pannek
aFrom The Australian e-Health Research Centre (L.v.E., M.S., K.P., D.B., S.R., J.F.), Health and Biosecurity, Commonwealth Scientific and Industrial Research Organisation, Brisbane, Australia
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J.M. George
cQueensland Cerebral Palsy and Rehabilitation Research Centre (J.M.G., R.N.B.)
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S. Fiori
fDepartment of Developmental Neuroscience (S.F., A.G.), Istituto di Ricovero e Cura a Carattere Scientifico Stella Maris, Pisa, Italy
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A. Guzzetta
fDepartment of Developmental Neuroscience (S.F., A.G.), Istituto di Ricovero e Cura a Carattere Scientifico Stella Maris, Pisa, Italy
gDepartment of Clinical and Experimental Medicine (A.G.), University of Pisa, Pisa, Italy
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A. Coulthard
dCentre for Children’s Health Research, Discipline of Medical Imaging (A.C.)
hDepartments of Medical Imaging (A.C., J.B.)
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J. Bursle
hDepartments of Medical Imaging (A.C., J.B.)
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R.S. Ware
jMenzies Health Institute Queensland (R.S.W.), Griffith University, Brisbane, Australia.
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D. Bradford
aFrom The Australian e-Health Research Centre (L.v.E., M.S., K.P., D.B., S.R., J.F.), Health and Biosecurity, Commonwealth Scientific and Industrial Research Organisation, Brisbane, Australia
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S. Rose
aFrom The Australian e-Health Research Centre (L.v.E., M.S., K.P., D.B., S.R., J.F.), Health and Biosecurity, Commonwealth Scientific and Industrial Research Organisation, Brisbane, Australia
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P.B. Colditz
ePerinatal Research Centre (P.B.C.), Faculty of Medicine, University of Queensland Centre for Clinical Research, The University of Queensland, Brisbane, Australia
iPerinatal Research Centre (P.B.C.), Royal Brisbane and Women’s Hospital, Brisbane, Australia
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R.N. Boyd
cQueensland Cerebral Palsy and Rehabilitation Research Centre (J.M.G., R.N.B.)
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J. Fripp
aFrom The Australian e-Health Research Centre (L.v.E., M.S., K.P., D.B., S.R., J.F.), Health and Biosecurity, Commonwealth Scientific and Industrial Research Organisation, Brisbane, Australia
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  • FIG 1.
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    FIG 1.

    Automated MR imaging measures of biparietal width (BPW), interhemispheric distance (IHD), thickness of the corpus callosum (CC), transcerebellar diameter (TCD), left and right LVD, and DGMA. IHD, Blue to orange represents the distance (closest and farthest, respectively) for each voxel to the segmentation in the opposite hemisphere. CC, Upper image, T2WI with the CC segmentation border (red); lower panel, segmentation border (blue), skeleton (red), and distance between the upper and lower borders of the segmentation for each voxel on the skeleton (green). R indicates right; L, left; A, anterior; P, posterior.

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    FIG 2.

    Associations between the 6 raw conventional MR imaging measures with postmenstrual age (left) and gestational age at birth (right) in the Pearson r, displayed separately for preterm-born infants at early MR imaging (n = 94) and TEA MR imaging (n = 81), as well as term-born controls at TEA MR imaging (PPREMO, n = 22; dHCP, n = 455). Manual measures were available for PPREMO only. Double asterisks indicate P ≤ .001; asterisk, P ≤ .05. BPW indicates biparietal width; CC, callosal thickness (at the genu (CCg), midbody (CCm), and splenium (CCs)); IHD, interhemispheric distance; TCD, transcerebellar diameter; R, right; L, left.

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    Table 1:

    Six manual measures of distance and area

    MeasureHow to Measure
    Biparietal widthGreatest distance between left and right parietal cortices, measured on a single coronal slice identifying bilateral
     cochlea and basilar truncus
    Interhemispheric distanceDistance between crowns of superior frontal gyri, measured on the same coronal slice as biparietal width
    Callosal thicknessThinning at the genu, midbody, splenium
    Transcerebellar diameterSingle coronal slice at level of ventricular atrium
    Lateral ventricular diameterSame coronal slice as transcerebellar diameter
    Deep grey matter areaSingle axial slice showing caudate heads, lentiform nuclei, and thalami
    • View popup
    Table 2:

    Automated measures of distance and area

    MeasureHow to Measure
    Biparietal widthIdentify most lateral sagittal slices of parietal GM (regionprops3)
    For each GM voxel, calculate distance to voxels in opposite hemisphere
    Calculate maximum distance
    Interhemispheric distanceCalculate distance from each voxel of superior frontal gyrus label in left hemisphere to each voxel label in right hemisphere (bwmorph3, bwdist)
    Derive minimum distance
    Callosal thicknessCombine 2D corpus callosum segmentation of the 11 most medial slices
    Increase resolution (imresize) and improve mask (bwmorph3, bwmorph)
    Derive skeleton (bwskel); for every voxel, calculate normal vector, identify intersection with borders of segmentation (points2contour, polyfit)
    Derive distance between upper/lower segmentation borders for every voxel
    Apply smoothing (nanfastsmooth), make 3 divisions
    Obtain 97th percentile for each division (prctile)
    Transcerebellar diameterModel cerebellum segmentation as 3D ellipsoid (bwmorph3, regionprops3)
    Calculate length of principal axis (regionprops3)
    Lateral ventricular dilationIdentify coronal slice at level of ventricular atrium (regionprops3): find maximum surface area using ventricle label (bwmorph, regionprops)
    Model 2D ventricle as ellipse, calculate length of minor axes (regionprops)
    Deep grey matter areaIdentify axial slice: centroid of caudate, thalamus, and lentiform nucleus (bwmorph, regionprops)
    Combine labels to calculate area (regionprops)
    • Note:—Matlab package used is provided in brackets.

    • View popup
    Table 3:

    Demographic and clinical characteristics

    PPREMO (n = 197)dHCP
    Preterm, Early MR ImagingPreterm, TEA MR ImagingControl, TEA MR Imaging
    No.94 of 12181 of 10522 of 27455 of 506 (95 preterm)
    Sex (female)61%63%50%45%
    PMA at MR imaging (wk)a31.86 ± 1.96 (29–35)40.71 ± 1.43 (38–47)41.29 ± 1.25 (39–44)40.71 ± 2.86 (29–45)
    GA (wk)a28.40 ± 2.00 (23–31)28.50 ± 2.20 (24–31)40.00 ± 0.98 (38–41)39.71 ± 2.82 (24–42)
    Birth weight (g)a1107 ± 368 (494–1886)1061 ± 391 (494–1886)3516 ± 157 (2932–4200)3250 ± 928 (540–4800)
    • ↵a P < .05 for 2-sided t test comparing preterm infants at 40 weeks with term-born controls (PPREMO). Continuous variables are given as median ± interquartile range (range). Scans with poor quality (PPREMO, n = 39), realignment errors (PPREMO, n = 1; dHCP, n = 39), and severe pathology (PPREMO, n = 16; dHCP, n = 12) were excluded.

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L. van Eijk, M. Seidel, K. Pannek, J.M. George, S. Fiori, A. Guzzetta, A. Coulthard, J. Bursle, R.S. Ware, D. Bradford, S. Rose, P.B. Colditz, R.N. Boyd, J. Fripp
Automating Quantitative Measures of an Established Conventional MRI Scoring System for Preterm-Born Infants Scanned between 29 and 47 Weeks’ Postmenstrual Age
American Journal of Neuroradiology Aug 2021, DOI: 10.3174/ajnr.A7230

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Automating Quantitative Measures of an Established Conventional MRI Scoring System for Preterm-Born Infants Scanned between 29 and 47 Weeks’ Postmenstrual Age
L. van Eijk, M. Seidel, K. Pannek, J.M. George, S. Fiori, A. Guzzetta, A. Coulthard, J. Bursle, R.S. Ware, D. Bradford, S. Rose, P.B. Colditz, R.N. Boyd, J. Fripp
American Journal of Neuroradiology Aug 2021, DOI: 10.3174/ajnr.A7230
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