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

doi:10.3174/ajnr.A6646

Abstract

BACKGROUND AND PURPOSE: Polymicrogyria and lissencephaly may be associated with abnormal organization of the undelying white matter tracts that have been rarely investigated so far. Our aim was to characterize white matter tract organization in polymicrogyria and lissencephaly using constrained spherical deconvolution, a multifiber diffusion MR imaging modeling technique for white matter tractography reconstruction.

MATERIALS AND METHODS: We retrospectively reviewed 50 patients (mean age, 8.3 ± 5.4 years; range, 1.4–21.2 years; 27 males) with different polymicrogyria (n = 42) and lissencephaly (n = 8) subtypes. The fiber direction-encoded color maps and 6 different white matter tracts reconstructed from each patient were visually compared with corresponding images reconstructed from 7 age-matched, healthy control WM templates. Each white matter tract was assessed by 2 experienced pediatric neuroradiologists and scored in consensus on the basis of the severity of the structural abnormality, ranging from the white matter tracts being absent to thickened. The results were summarized by different polymicrogyria and lissencephaly subgroups.

RESULTS: More abnormal-appearing white matter tracts were identified in patients with lissencephaly compared with those with polymicrogyria (79.2% versus 37.3%). In lissencephaly, structural abnormalities were identified in all studied white matter tracts. In polymicrogyria, the more frequently affected white matter tracts were the cingulum, superior longitudinal fasciculus, inferior longitudinal fasciculus, and optic radiation–posterior corona radiata. The severity of superior longitudinal fasciculus and cingulum abnormalities was associated with the polymicrogyria distribution and extent. A thickened superior fronto-occipital fasciculus was demonstrated in 3 patients.

CONCLUSIONS: We demonstrated a range of white matter tract structural abnormalities in patients with polymicrogyria and lissencephaly. The patterns of white matter tract involvement are related to polymicrogyria and lissencephaly subgroups, distribution, and, possibly, their underlying etiologies.

ABBREVIATIONS:

CG: cingulum
CMV: cytomegalovirus
CSD: constrained spherical deconvolution
DEC: direction-encoded color
dMRI: diffusion MRI
FOD: fiber orientation distribution
HARDI: high angular resolution diffusion imaging
IFOF: inferior fronto-occipital fasciculus
ILF: inferior longitudinal fasciculus
LIS: lissencephaly
MCD: malformation of cortical development
OR-PCR: optic radiation–posterior corona radiata
PMG: polymicrogyria
SBH: subcortical band heterotopia
SFOF: superior fronto-occipital fasciculus/Muratoff bundle
SLF: superior longitudinal fasciculus
WMT: white matter tract

Footnotes

This study was funded by the Italian Ministry of Health (Ricerca Corrente 2018 and 2019 to Drs Arrigoni and Borgatti). Dr Arrigoni was also funded by the Australian Government through the Endeavor Research Fellowship program 2018 and by “Fondazione Banca del Monte di Lombardia.” Dr Yang was funded by the Royal Columbian Hospital Foundation (RCH-1000). The research was supported by the Royal Children’s Hospital Foundation, Murdoch Children’s Research Institute, The University of Melbourne Department of Pediatrics, and the Victorian Government’s Operational Infrastructure Support Program. Data used in the preparation of this article were obtained from the Pediatric MRI Data Repository created by the National Institutes of Health MRI Study of Normal Brain Development. This is a multisite, longitudinal study of typically developing children, from ages neonate through young adulthood, conducted by the Brain Development Cooperative Group and supported by the National Institute of Child Health and Human Development, the National Institute on Drug Abuse, the National Institute of Mental Health, and the National Institute of Neurologic Disorders and Stroke (contract Nos. N01-HD02-3343, N01-MH9-0002, and N01-NS-9–2314, −2315, −2316, −2317, −2319 and −2320).
This article reflects the views of the authors and may not reflect the opinions or views of the National Institutes of Health.
Disclosures: Filippo Arrigoni—RELATED: Grant: Australian government, Italian Ministry of Health, Comments: I was funded by the Australian Government through the Endeavour Leadership Program to spend 6 months in Australia (at Murdoch Children’s Research Institute, Melbourne) to complete my research. My living costs during my fellowship in Australia were partially covered by an Italian foundation (Fondazione Banco del Monte di Lombardia). My home Institution (E. Medea Scientific Institute, Bosisio Parini, Italy) received money from the Italian Ministry of Health through the “Ricerca Corrente” program for this research; UNRELATED: Employment: E. Medea Scientific Institute, Comments: I work as full-time neuroradiologist at E. Medea Scientific Institute (Bosisio Parini, Italy); Grants/Grants Pending: Ministry of Health, Italian Association for Research on Cancer, and so forth, Comments: I am participating in several research projects at my home Institution (E. Medea Institute, Bosisio Parini, Italy), which are funded by different public and private agencies like the Italian Ministry of Health, or Italian Association for Research on Cancer.* *Money paid to the institution.
Data previously presented, in part, as posters at: Annual Meeting of the Organization for Human Brain Mapping, June 9-13, 2019, Rome, Italy; and the Annual Meeting of the European Society of Neuroradiology, September 19-22, 2019, Oslo, Norway.