Whole-Brain DTI Assessment of White Matter Damage in Children with Bilateral Cerebral Palsy: Evidence of Involvement beyond the Primary Target of the Anoxic Insult

Arrigoni, Filippo; Peruzzo, Denis; Gagliardi, Chiara; Maghini, Cristina; Colombo, Paola; Iammarrone, F. Servodio; Pierpaoli, Carlo; Triulzi, Fabio; Turconi, Anna Carla

doi:10.3174/ajnr.a4717

Cited by 35 publications

(38 citation statements)

References 33 publications

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“…This component comprised mainly basal ganglia and thalamic connections with primary sensorimotor areas, frontal and parietal areas, as well as fronto‐parietal and intraparietal connections. These results match those found in spastic CP in which thalamocortical and fronto‐parietal projections were associated with GMFCS, MACS, and other sensorimotor measures [Arrigoni et al, ; Pannek et al, ; Tsao et al, ]. If we compare this component with that found when compared with the control group, there are some points worth noting.…”

Section: Discussionsupporting

confidence: 85%

“…In the first place, this is in agreement with a previous study analyzing FA in several manually-drawn ROIs in people with dyskinetic CP that found a reduced FA in projection fibers connecting sensorimotor areas such as the posterior limb of the internal capsule or the posterior thalamic radiation [Yoshida et al, 2011]. Similar results, highlighting the involvement of the sensorimotor areas, have been found in spastic forms of CP [Arrigoni et al, 2016;Nagae et al, 2007;Pannek et al, 2014;Tsao et al, 2015], although with two remarkable differences: the contribution of basal ganglia and corticospinal connections. Although some alterations in basal ganglia have been described in cases with spastic CP [Kr€ ageloh-Mann et al, 2002], these are not very common Himmelmann and Uvebrant, 2011] and most connectivity studies so far have not focused on these nuclei.…”

Section: White Matter Involvement In Dyskinetic Cpsupporting

confidence: 91%

“…Our a priory hypothesis is that brain connectivity would be reduced in dyskinetic CP compared to healthy controls reflecting an impaired WM organization, specifically among sensorimotor areas. Our second hypothesis is that the degree of impairment of some of these connections would correlate with measures of motor function [Arrigoni et al, ]. Finally, we further hypothesize that intelligence quotient (IQ) would correlate with connectivity measures in fronto‐striatal and parieto‐frontal connections, in accordance with a previous study [Ballester‐Plané et al, ].…”

Section: Introductionsupporting

confidence: 86%

“…Second, we observe a greater number of connections to the frontal lobe, specifically prefrontal areas, the left temporal lobe and the occipital lobe. As these areas are not solely or directly responsible for motor functions, they could be responsible for the diverse associated deficits observed in this population, as noted by some authors on cognitive impairment [Rai et al, ; Scheck et al, ; Tsao et al, ], visuoperceptual deficits [Arrigoni et al, ; Ego et al, ], or communication disturbances [Harlaar et al, ; Sigurdardottir and Vik, ]. This would also explain why the more severe the motor impairment, the larger the percentage of associated deficits [Himmelmann et al, ; Krägeloh‐Mann et al, ].…”

Section: Discussionmentioning

confidence: 85%

“…This component mainly comprised basal ganglia and thalamocortical projections to sensorimotor areas, fronto‐parietal and parieto‐parietal connections. Arrigoni et al [] also found a bigger component in which FA values correlated with GMFCS than with MACS in subjects with bilateral spastic CP, with a similar overlap in thalamocortical and fronto‐parietal connections although with a greater presence of corticospinal projections.…”

Section: Discussionmentioning

confidence: 95%

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Whole-brain structural connectivity in dyskinetic cerebral palsy and its association with motor and cognitive function

et al. 2017

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Dyskinetic cerebral palsy (CP) has long been associated with basal ganglia and thalamus lesions. Recent evidence further points at white matter (WM) damage. This study aims to identify altered WM pathways in dyskinetic CP from a standardized, connectome-based approach, and to assess structure-function relationship in WM pathways for clinical outcomes. Individual connectome maps of 25 subjects with dyskinetic CP and 24 healthy controls were obtained combining a structural parcellation scheme with whole-brain deterministic tractography. Graph theoretical metrics and the network-based statistic were applied to compare groups and to correlate WM state with motor and cognitive performance. Results showed a widespread reduction of WM volume in CP subjects compared to controls and a more localized decrease in degree (number of links per node) and fractional anisotropy (FA), comprising parieto-occipital regions and the hippocampus. However, supramarginal gyrus showed a significantly higher degree. At the network level, CP subjects showed a bilateral pathway with reduced FA, comprising sensorimotor, intraparietal and fronto-parietal connections. Gross and fine motor functions correlated with FA in a pathway comprising the sensorimotor system, but gross motor also correlated with prefrontal, temporal and occipital connections. Intelligence correlated with FA in a network with fronto-striatal and parieto-frontal connections, and visuoperception was related to right occipital connections. These findings demonstrate a disruption in structural brain connectivity in dyskinetic CP, revealing general involvement of posterior brain regions with relative preservation of prefrontal areas. We identified pathways in which WM integrity is related to clinical features, including but not limited to the sensorimotor system. Hum Brain Mapp 38:4594-4612, 2017. © 2017 Wiley Periodicals, Inc.

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Section: Discussionsupporting

confidence: 85%

Section: White Matter Involvement In Dyskinetic Cpsupporting

confidence: 91%

Section: Introductionsupporting

confidence: 86%

Section: Discussionmentioning

confidence: 85%

Section: Discussionmentioning

confidence: 95%

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Whole-brain structural connectivity in dyskinetic cerebral palsy and its association with motor and cognitive function

et al. 2017

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Exploring structural connectomes in children with unilateral cerebral palsy using graph theory

Radwan

Decraene

Dupont

et al. 2023

Human Brain Mapping

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We explored structural brain connectomes in children with spastic unilateral cerebral palsy (uCP) and its relation to sensory‐motor function using graph theory. In 46 children with uCP (mean age = 10 years 7 months ± 2 years 9 months; Manual Ability Classification System I = 15, II = 16, III = 15) we assessed upper limb somatosensory and motor function. We collected multi‐shell diffusion‐weighted, T1‐weighted and T2‐FLAIR MRI and identified the corticospinal tract (CST) wiring pattern using transcranial magnetic stimulation. Structural connectomes were constructed using Virtual Brain Grafting‐modified FreeSurfer parcellations and multi‐shell multi‐tissue constrained spherical deconvolution‐based anatomically‐constrained tractography. Graph metrics (characteristic path length, global/local efficiency and clustering coefficient) of the whole brain, the ipsilesional/contralesional hemisphere, and the full/ipsilesional/contralesional sensory‐motor network were compared between lesion types (periventricular white matter (PWM) = 28, cortical and deep gray matter (CDGM) = 18) and CST‐wiring patterns (ipsilateral = 14, bilateral = 14, contralateral = 12, unknown = 6) using ANCOVA with age as covariate. Using elastic‐net regularized regression we investigated how graph metrics, lesion volume, lesion type, CST‐wiring pattern and age predicted sensory‐motor function. In both the whole brain and subnetworks, we observed a hyperconnectivity pattern in children with CDGM‐lesions compared with PWM‐lesions, with higher clustering coefficient (p = [<.001–.047], ηp2=[0.09–0.27]), characteristic path length (p = .003, ηp2=0.19) and local efficiency (p = [.001–.02], ηp2=[0.11–0.21]), and a lower global efficiency with age (p = [.01–.04], ηp2=[0.09–0.15]). No differences were found between CST‐wiring groups. Overall, good predictions of sensory‐motor function were obtained with elastic‐net regression (R2 = .40–.87). CST‐wiring pattern was the strongest predictor for motor function. For somatosensory function, all independent variables contributed equally to the model. In conclusion, we demonstrated the potential of structural connectomics in understanding disease severity and brain development in children with uCP.

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White matter changes associated with cognitive visual dysfunctions in children with cerebral palsy: A diffusion tensor imaging study

Galli

Ambrosi

Micheletti

et al. 2018

J of Neuroscience Research

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Children with cerebral palsy often present with cognitive-visual dysfunctions characterized by visuo-perceptual and/or visuo-spatial deficits associated with a malfunctioning of visual-associative areas. The neurofunctional model of this condition remains poorly understood due to the lack of a clear correlation between cognitive-visual deficit and morphological brain anomalies. The aim of our study was to quantify the pattern of white matter abnormalities within the whole brain in children with cerebral palsy, and to identify white matter tracts sub-serving cognitive-visual functions, in order to better understand the basis of cognitive-visual processing. Nine subjects (three males, mean age 8 years 9 months) with cerebral palsy underwent a visual and cognitive-visual evaluation. Conventional brain MRI and diffusion tensor imaging were performed. The fractional anisotropy maps were calculated for every child and compared with data from 13 (four males, mean age 10 years 7 months) healthy children. Children with cerebral palsy showed decreased fractional anisotropy (a marker of white matter integrity) in corticospinal tract bilaterally, left superior longitudinal fasciculus and bilateral hippocampus. Focusing on the superior longitudinal fasciculus, the mean fractional anisotropy values were significantly lower in children affected by cerebral palsy with cognitive-visual deficits than in those without cognitive-visual deficits. Our findings reveal an association between cognitive-visual profile and the superior longitudinal fasciculus integrity in children with cerebral palsy, supporting the hypothesis that visuo-associative deficits are related to changes in fibers connecting the occipital cortex with the parietal-frontal cortices. Decreased fractional anisotropy within the superior longitudinal fasciculus could be considered a biomarker for cognitive-visual dysfunctions.

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Whole-Brain DTI Assessment of White Matter Damage in Children with Bilateral Cerebral Palsy: Evidence of Involvement beyond the Primary Target of the Anoxic Insult

Cited by 35 publications

References 33 publications

Whole-brain structural connectivity in dyskinetic cerebral palsy and its association with motor and cognitive function

Whole-brain structural connectivity in dyskinetic cerebral palsy and its association with motor and cognitive function

Exploring structural connectomes in children with unilateral cerebral palsy using graph theory

White matter changes associated with cognitive visual dysfunctions in children with cerebral palsy: A diffusion tensor imaging study

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