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Research ArticlePediatric Neuroimaging
Open Access

Characterizing White Matter Tract Organization in Polymicrogyria and Lissencephaly: A Multifiber Diffusion MRI Modeling and Tractography Study

F. Arrigoni, D. Peruzzo, S. Mandelstam, G. Amorosino, D. Redaelli, R. Romaniello, R. Leventer, R. Borgatti, M. Seal and J.Y.-M. Yang
American Journal of Neuroradiology August 2020, 41 (8) 1495-1502; DOI: https://doi.org/10.3174/ajnr.A6646
F. Arrigoni
aFrom the Scientific Institute, IRCCS E. Medea (F.A., D.P., G.A., D.R., R.R.), Bosisio Parini, Italy
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D. Peruzzo
aFrom the Scientific Institute, IRCCS E. Medea (F.A., D.P., G.A., D.R., R.R.), Bosisio Parini, Italy
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S. Mandelstam
bMurdoch Children’s Research Institute (S.M., R.L., M.S., J.Y.-M.Y.), Parkville, Australia
cRoyal Children’s Hospital (S.M., R.L.), Parkville, Australia; Neuroscience Advanced Clinical Imaging Suite (NACIS) (J.Y.-M.Y.), Department of Neurosurgery, The Royal Children’s Hospital, Victoria, Australia
dUniversity of Melbourne (S.M., R.L., M.S., J.Y.-M.Y.), Parkville, Australia
eFlorey Institute of Neuroscience and Mental Health (S.M.), Parkville, Australia
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G. Amorosino
aFrom the Scientific Institute, IRCCS E. Medea (F.A., D.P., G.A., D.R., R.R.), Bosisio Parini, Italy
fBruno Kessler Foundation (G.A.), Trento, Italy
gUniversity of Trento, Center for Mind/Brain Sciences (G.A.), Rovereto, Italy
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D. Redaelli
aFrom the Scientific Institute, IRCCS E. Medea (F.A., D.P., G.A., D.R., R.R.), Bosisio Parini, Italy
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R. Romaniello
aFrom the Scientific Institute, IRCCS E. Medea (F.A., D.P., G.A., D.R., R.R.), Bosisio Parini, Italy
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R. Leventer
bMurdoch Children’s Research Institute (S.M., R.L., M.S., J.Y.-M.Y.), Parkville, Australia
cRoyal Children’s Hospital (S.M., R.L.), Parkville, Australia; Neuroscience Advanced Clinical Imaging Suite (NACIS) (J.Y.-M.Y.), Department of Neurosurgery, The Royal Children’s Hospital, Victoria, Australia
dUniversity of Melbourne (S.M., R.L., M.S., J.Y.-M.Y.), Parkville, Australia
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R. Borgatti
hIstituto di ricovero e cura a carattere scientifico Mondino Foundation (R.B.), Pavia, Italy
iUniversity of Pavia (R.B.), Pavia, Italy.
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M. Seal
bMurdoch Children’s Research Institute (S.M., R.L., M.S., J.Y.-M.Y.), Parkville, Australia
dUniversity of Melbourne (S.M., R.L., M.S., J.Y.-M.Y.), Parkville, Australia
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J.Y.-M. Yang
bMurdoch Children’s Research Institute (S.M., R.L., M.S., J.Y.-M.Y.), Parkville, Australia
cRoyal Children’s Hospital (S.M., R.L.), Parkville, Australia; Neuroscience Advanced Clinical Imaging Suite (NACIS) (J.Y.-M.Y.), Department of Neurosurgery, The Royal Children’s Hospital, Victoria, Australia
dUniversity of Melbourne (S.M., R.L., M.S., J.Y.-M.Y.), Parkville, Australia
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    Fig 1.

    Tractography findings in selected patients with lissencephaly and polymicrogyria. T1WI, direction-encoded color maps, and tractography reconstructions in 2 patients with LIS (A and B) and 2 with PMG (C and D) are shown. For each patient, a comparable tractography reconstruction from the age-matched healthy control template is shown in the last column for comparison. A, An irregular (shorter and smaller) bilateral cingulum (arrows on DEC map) in a patient with pachygyria and thick subcortical band heterotopia. B, A bilateral, irregular (smaller and distorted) superior longitudinal fasciculus (arrows on DEC map) in a patient with posterior-quadrant pachygyria and a thick SBH. C, Bilateral irregular (smaller and thinner) CG (arrows on DEC map) in a patient with generalized PMG. D, An irregular (shorter and distorted) right inferior fronto-occipital fasciculus (IFOF; arrows) in a patient with unilateral right peri-Sylvian PMG. The left IFOF (arrowheads) has a normal appearance. r. indicates right.

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    Fig 2.

    The superior longitudinal fasciculus involvement in peri-Sylvian polymicrogyria. T1WI, direction-encoded color maps, and tractography reconstructions of the SLF in 3 patients with exemplary peri-Sylvian PMG (A–C). Sagittal T1-weighted images and tractography refer to the right hemisphere. A comparable SLF tractography reconstruction from the age-matched healthy control template is shown in the last row for comparison (D). Patient A has bilateral focal peri-Sylvian PMG in the opercular regions (arrows on T1WI). Both SLFs look normal on both the DEC map (arrows on DEC map) and tractography reconstruction. Patient B has bilateral diffuse peri-Sylvian PMG (arrows on T1WI). Both SLFs (arrows on DEC maps) are irregular in appearance. The right SLF tractography is notably shorter and smaller compared with the right SLF from a control. Patient C has bilateral diffuse peri-Sylvian PMG extending to adjacent cortical regions. The right SLF is absent and could not be reconstructed (symbolized by the X), and the left SLF is irregular in appearance (smaller compared with the left SLF from a control).

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    Fig 3.

    Thickened superior fronto-occipital fasciculus. T1WI, direction-encoded color maps with associated fiber orientation distribution glyph profiles, and tractography reconstructions in 3 patients with thickened SFOFs (A–C) and in the age-matched healthy control template for comparison (D). Patient A has bilateral peri-Sylvian PMG plus a left schizencephaly and a thickened right SFOF (arrowheads). The left SFOF cannot be recognized. Patients B and C demonstrate pachygyria and subcortical band heterotopia and bilateral thickened SFOF (arrowheads). On FOD glyphs maps, 1 indicates the SFOF (green, predominately anterior-posterior oriented fibers), and 2, the corpus callosum (red, predominately left-right oriented fibers).

Tables

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    Table 1:

    Study patients by the MCD subgroups and their conventional structural MR imaging findings

    MCD Subgroups/VariantsNo. of CasesUnilateral MCDPrenatal CMV InfectionAssociated Brain Anomalies
    VentriclesBGTHippocampusBrain StemCerebellumCC
    PMG
     Peri-Sylvian1641935245
     Frontoparietal724200222
     Generalized400414023
     Focala720423235
     Parieto-occipital110100001
     Multifocal620303015
     With schizencephaly100111111
     Total421152471671322
    LISb
     Pachygyria with SBH500523224
     Pachygyria without SBH100012122
     SBH without pachygyria200100002
     Total800635348
    • Note:—BGT indicates basal ganglia and thalami; CC, corpu callosum.

    • ↵a All located in frontal lobe.

    • ↵b All LIS cases were bilateral.

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    Table 2:

    Summary of the white matter tract appearance in all study patients presented by each MCD subgroupa

    MCD SubgroupsNo. of PatientsSLFCGSFOFIFOFOR-PCRILF
    Peri-Sylvian PMG168/16/0/827/5/0/031/1/0/027/5/0/020/12/0/021/11/0/0
    Frontoparietal PMG74/6/0/413/1/0/012/2/0/012/2/0/06/8/0/07/7/0/0
    Frontal PMG73/10/0/15/9/0/012/1/0/112/2/0/010/4/0/011/3/0/0
    Generalized PMG40/2/0/61/5/0/22/2/0/42/6/0/00/8/0/00/8/0/0
    Multifocal PMG69/3/0/07/5/0/010/0/0/212/0/0/09/3/0/011/1/0/0
    Parieto-occipital PMG12/0/0/02/0/0/02/0/0/02/0/0/01/1/0/02/0/0/0
    PMG and schizenchephaly10/0/0/20/2/0/00/0/1/10/2/0/00/2/0/00/2/0/0
    Pachygyria with SBH50/6/0/42/8/0/02/4/4/02/8/0/00/10/0/00/10/0/0
    SBH (no pachygyria)20/4/0/02/2/0/04/0/0/02/2/0/00/4/0/00/4/0/0
    Pachygyria (no SBH)10/2/0/00/2/0/02/0/0/00/2/0/02/0/0/02/0/0/0
    All PMG4227/36/0/2155/27/0/269/6/1/867/17/0/046/38/0/052/32/0/0
    All LIS80/12/0/44/12/0/08/4/4/04/12/0/02/14/0/02/14/0/0
    • ↵a For each white matter tract, the number of tract appearances classified as grades I/IIA/IIB/III is reported.

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F. Arrigoni, D. Peruzzo, S. Mandelstam, G. Amorosino, D. Redaelli, R. Romaniello, R. Leventer, R. Borgatti, M. Seal, J.Y.-M. Yang
Characterizing White Matter Tract Organization in Polymicrogyria and Lissencephaly: A Multifiber Diffusion MRI Modeling and Tractography Study
American Journal of Neuroradiology Aug 2020, 41 (8) 1495-1502; DOI: 10.3174/ajnr.A6646

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Characterizing White Matter Tract Organization in Polymicrogyria and Lissencephaly: A Multifiber Diffusion MRI Modeling and Tractography Study
F. Arrigoni, D. Peruzzo, S. Mandelstam, G. Amorosino, D. Redaelli, R. Romaniello, R. Leventer, R. Borgatti, M. Seal, J.Y.-M. Yang
American Journal of Neuroradiology Aug 2020, 41 (8) 1495-1502; DOI: 10.3174/ajnr.A6646
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