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Language and reading skills in school-aged children and adolescents born preterm are associated with white matter properties on diffusion tensor imaging.

ABSTRACT: Children born preterm are at risk for deficits in language and reading. They are also at risk for injury to the white matter of the brain. The goal of this study was to determine whether performance in language and reading skills would be associated with white matter properties in children born preterm and full-term. Children born before 36 weeks gestation (n=23, mean±SD age 12.5±2.0 years, gestational age 28.7±2.5 weeks, birth weight 1184±431 g) and controls born after 37 weeks gestation (n=19, 13.1±2.1 years, 39.3±1.0 weeks, 3178±413 g) underwent a battery of language and reading tests. Diffusion tensor imaging (DTI) scans were processed using tract-based spatial statistics to generate a core white matter skeleton that was anatomically comparable across participants. Fractional anisotropy (FA) was the diffusion property used in analyses. In the full-term group, no regions of the whole FA-skeleton were associated with language and reading. In the preterm group, regions of the FA-skeleton were significantly associated with verbal IQ, linguistic processing speed, syntactic comprehension, and decoding. Combined, the regions formed a composite map of 22 clusters on 15 tracts in both hemispheres and in the ventral and dorsal streams. ROI analyses in the preterm group found that several of these regions also showed positive associations with receptive vocabulary, verbal memory, and reading comprehension. Some of the same regions showed weak negative correlations within the full-term group. Exploratory multiple regression in the preterm group found that specific white matter pathways were related to different aspects of language processing and reading, accounting for 27-44% of the variance. The findings suggest that higher performance in language and reading in a group of preterm but not full-term children is associated with higher fractional anisotropy of a bilateral and distributed white matter network.

SUBMITTER: Feldman HM

PROVIDER: S-EPMC3631607 | biostudies-literature | 2012 Dec

REPOSITORIES: biostudies-literature

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Language and reading skills in school-aged children and adolescents born preterm are associated with white matter properties on diffusion tensor imaging.

Feldman Heidi M HM Lee Eliana S ES Yeatman Jason D JD Yeom Kristen W KW

Neuropsychologia 20121023 14

Children born preterm are at risk for deficits in language and reading. They are also at risk for injury to the white matter of the brain. The goal of this study was to determine whether performance in language and reading skills would be associated with white matter properties in children born preterm and full-term. Children born before 36 weeks gestation (n=23, mean±SD age 12.5±2.0 years, gestational age 28.7±2.5 weeks, birth weight 1184±431 g) and controls born after 37 weeks gestation (n=19, ...[more]

PMID: 23088817

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Project description:AimTo assess associations between white matter properties and pre-reading skills (phonological awareness and receptive and expressive language) in children born preterm and at term at the onset of reading acquisition.MethodSix-year-old children born preterm (n=36; gestational age 22-32wks) and at term (n=43) underwent diffusion magnetic resonance imaging and behavioural assessments. Tracts were selected a priori based on findings from a study of 6-year-old children born at term: the left-hemisphere arcuate fasciculus and superior longitudinal fasciculus, and right-hemisphere uncinate fasciculus. Using linear regression, we assessed associations between fractional anisotropy of tracts and phonological awareness and receptive and expressive language scores. We investigated whether associations were moderated by prematurity.ResultsFractional anisotropy of the left-hemisphere arcuate fasciculus contributed unique variance to phonological awareness across birth groups. The association between fractional anisotropy of the right-hemisphere uncinate fasciculus and receptive and expressive language was significantly moderated by prematurity.InterpretationA left-hemisphere tract was associated with phonological awareness in both birth groups. A right-hemisphere tract was associated with language only in the term group, suggesting that expressive and receptive language is mediated by different white matter pathways in 6-year-old children born preterm. These findings provide novel insights into similarities and differences of the neurobiology of pre-reading skills between children born preterm and at term at reading onset.What this paper addsWhite matter properties and pre-reading abilities were associated in children born preterm at the onset of reading. The neurobiology of phonological awareness was similar in children born preterm versus children born at term at 6 years. The neurobiology of language was different in children born preterm versus children born at term at 6 years.

Project description:Very preterm birth is associated with altered white matter microstructure and language difficulties, which may compromise communication, social function and academic achievement, but the relationship between these two factors is unclear. The aim of this study was to explore associations between white matter microstructure and language domains of semantics, grammar and phonological awareness at 7-years of age on a whole-brain level and within the arcuate fasciculus, an important language pathway, in very preterm and term-born children. Language was assessed in 145 very preterm-born (<30?weeks' gestation and/or <1250?g birth weight) and 33 term-born children aged 7?years. Fractional anisotropy (FA), axial diffusivity (AD), radial diffusivity (RD), mean diffusivity (MD), axon orientation dispersion and axon density were estimated from diffusion magnetic resonance images also obtained at 7?years. The correlation between diffusion values and language was assessed using Tract-Based Spatial Statistics (TBSS). The arcuate fasciculus was delineated using constrained spherical deconvolution tractography and diffusion parameters from this tract were related to language measures using linear regression. While there was evidence for widespread associations between white matter microstructure and language, there was little evidence of differences in these associations between very preterm and term-born groups. TBSS analyses revealed that higher FA and lower AD, RD, and MD in major fibre tracts, including those subserving language, were associated with better semantic, grammar and phonological awareness performance. Higher axon density in widespread fibre tracts was also associated with better semantic performance. The tractography analyses of the arcuate fasciculus showed some evidence for associations between white matter microstructure and language outcomes. White matter microstructural organisation in widespread fibre tracts, including language-relevant pathways, was associated with language performance in whole-brain and tract-based analyses. The associations were similar for very preterm and term-born groups, despite very preterm children performing more poorly across language domains.

Project description:Individuals born very preterm (<32 weeks gestation) have altered brain growth and white matter maturation relative to their full-term peers, and approximately 30% will experience neurodevelopmental impairment. We investigated the relationship between neurodevelopmental impairment and MRI measures of white matter microstructure and brain volume. Children born before 30 weeks' gestation or who had very low birthweight (< 1500 g) underwent neurodevelopmental assessment and MRI at age 7 years as part of the PIANO study, a New Zealand-based cohort study. Fractional anisotropy (FA) and diffusivity measures were derived from diffusion tensor imaging to index white matter microstructure. Volumes were derived from T1-weighted imaging. Neurodevelopmental impairment was defined as a score < 85 on the Wechsler Intelligence Scale for Children, <5th centile on the Movement Assessment Battery for Children or a diagnosis of cerebral palsy by a paediatrician. Relationships between MRI and neurodevelopmental impairment were assessed with general linear models adjusted for sex, gestational age at birth, birthweight z-score, age at assessment, New Zealand Deprivation index score and multiplicity. Children with neurodevelopmental impairment (n = 38) had smaller total brain, cortical grey matter and cerebral white matter volumes compared to children without neurodevelopmental impairment (n = 62) (p < 0.05, false discovery rate corrected), but the regional volume differences did not remain significant after adjustment for total brain volume. Lower FA and higher radial diffusivity were observed in the superior longitudinal fasciculi, uncinate fasciculi and right hemisphere corticospinal tract in children with neurodevelopmental impairment. This may reflect differences in cellular properties such as myelination or axonal packing. Neurodevelopmental impairment may reflect smaller overall brain volume and altered microstructure in white matter tracts that are important for language, cognitive and motor functioning.

Project description:IntroductionThis study investigated whether behavioral problems in children were associated with fractional anisotropy (FA) of white matter tracts connecting from other brain regions to right and left frontal lobes. We considered internalizing and externalizing behavioral problems separately and contrasted patterns of associations in children born at term and very preterm.MethodsParents completed the Child Behavior Checklist/6-18 questionnaire to quantify behavioral problems when their children were age 8 years (N=36 FT and 37 PT). Diffusion magnetic resonance scans were collected at the same age and analyzed using probabilistic tractography. We used multiple linear regression to investigate the strength of association between age-adjusted T-scores of internalizing and externalizing problems and mean fractional anisotropy (mean-FA) of right and left uncinate, arcuate, and anterior thalamic radiations, controlling for birth group and sex.ResultsRegression models predicting internalizing T-scores from mean-FA found significant group-by-tract interactions for the left and right arcuate and right uncinate. Internalizing scores were negatively associated with mean-FA of left and right arcuate only in children born at term (pleft AF =0.01, pright AF =0.01). Regression models predicting externalizing T-scores from mean-FA found significant group-by-tract interactions for the left arcuate and right uncinate. Externalizing scores were negatively associated with mean-FA of right uncinate in children born at term (pright UF =0.01) and positively associated in children born preterm (pright UF preterm =0.01). Other models were not significant.ConclusionsIn this sample of children with scores for behavioral problems across the full range, internalizing and externalizing behavioral problems were negatively associated with mean-FA of white matter tracts connecting to frontal lobes in children born at term; externalizing behavioral problems were positively associated with mean-FA of the right uncinate in children born preterm. The different associations by birth group suggest that the neurobiology of behavioral problems differs in the two birth groups.

Project description:Importance:Children born preterm are at an elevated risk of academic underachievement. However, the extent to which performance across domain-specific subskills in reading and mathematics is associated with preterm birth remains unclear. Objective:To conduct a systematic review and meta-analysis of academic outcomes of school-aged children born preterm, compared with children born at term, appraising evidence for higher- and lower-order subskills in reading and mathematics. Data Sources:PubMed/MEDLINE, PsycINFO, and the Cumulative Index of Nursing and Allied Health Literature electronic databases from January 1, 1980, to July 30, 2018, were searched for population, exposure, and outcome terms such as child (population), preterm birth (exposure), and education* (outcome). Study Selection:Peer-reviewed English-language publications that included preterm-born children and a comparison group of term-born children aged 5 to 18 years and born during or after 1980 and that reported outcomes on standardized assessments from cohort or cross-sectional studies were screened. Of the 9833 articles screened, 33 unique studies met the inclusion criteria. Data Extraction and Synthesis:Data were analyzed from August 1 to September 29, 2018. The Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) guidelines were followed. Two reviewers independently screened the databases and extracted sample characteristics and outcomes scores. Pooled mean differences (MDs) were analyzed using random-effects models. Main Outcomes and Measures:Performance on standardized assessment of higher-order subskills of reading comprehension and applied mathematics problems; lower-order reading subskills of decoding, pseudoword decoding, and word identification; and lower-order mathematics subskills of knowledge, calculation, and fluency. Results:Outcomes data were extracted for 4006 preterm and 3317 term-born children, totaling 7323 participants from 33 unique studies. Relative to children born at term, children born preterm scored significantly lower in reading comprehension (mean difference [MD], -7.96; 95% CI, -12.15 to -3.76; I2?=?81%) and applied mathematical problems (MD, -11.41; 95% CI, -17.57 to -5.26; I2?=?91%) assessments. Across the assessments of lower-order skills, children born preterm scored significantly lower than their term-born peers in calculation (MD, -10.57; 95% CI, -15.62 to -5.52; I2?=?92%), decoding (MD, -10.18; 95% CI, -16.83 to -3.53; I2?=?71%), mathematical knowledge (MD, -9.88; 95% CI, -11.68 to -8.08; I2?=?62%), word identification (MD, -7.44; 95% CI, -9.08 to -5.80; I2?=?69%), and mathematical fluency (MD, -6.89; 95% CI, -13.54 to -0.23; I2?=?72%). The associations remained unchanged after sensitivity analyses for reducing heterogeneity. Conclusions and Relevance:These findings provide evidence that preterm birth is associated with academic underperformance in aggregate measures of reading and mathematics, as well as a variety of related subskills.

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Language and reading skills in school-aged children and adolescents born preterm are associated with white matter properties on diffusion tensor imaging.

Publications

Language and reading skills in school-aged children and adolescents born preterm are associated with white matter properties on diffusion tensor imaging.

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