Caudate and hippocampal volumes, intelligence, and motor impairment in 7-year-old children who were born preterm

ABSTRACT Children who survive very preterm birth without major disability have a high prevalence of learning difficulty, attention deficit, and minor motor impairment (MMI). To determine

whether these difficulties are associated with structural brain abnormalities, we studied 105 preterm children (<32 wk) at 7 y with tests of IQ and MMI (Movement ABC) and detailed

magnetic resonance brain scans. Scans were assessed qualitatively for visible cerebral lesions. Volume measurements of the caudate nuclei and hippocampal formations were made. Total brain

volume (TBV) was estimated from the head circumference. Qualitative assessment of the scans showed evidence of cerebral lesions in 20 (19%), which were associated with lower IQ and more

frequent MMI. IQ correlated with right and left caudate volume (Spearman's ρ 0.304 and 0.349; _p_ < 0.01). This association persisted (except for verbal IQ) when caudate volume was

expressed as a percentage of estimated TBV to allow for overall brain size. No significant correlations with hippocampal volumes were observed. These differences persisted when only scans

from children without visible lesions on scan were considered. MMI was significantly associated only with TBV and was more common in children with evidence of thinning of the posterior

corpus callosum, although most children with MMI have a normal corpus callosum. Lower IQs in children who were born preterm are related to poorer development of the caudate relative to the

rest of the brain, independent of other lesions. These findings suggest abnormal brain development after perinatal injury or postnatal nutritional deficits is responsible for cognitive

deficits in preterm children. SIMILAR CONTENT BEING VIEWED BY OTHERS CORPUS CALLOSUM LONG-TERM BIOMETRY IN VERY PRETERM CHILDREN RELATED TO COGNITIVE AND MOTOR OUTCOMES Article Open access

15 January 2024 LANGUAGE PERFORMANCE AND BRAIN VOLUMES, ASYMMETRY, AND CORTICAL THICKNESS IN CHILDREN BORN EXTREMELY PRETERM Article Open access 03 November 2023 ASSOCIATION BETWEEN CORTICAL

THICKNESS AND COGNITIVE ABILITY IN VERY PRETERM SCHOOL-AGE CHILDREN Article Open access 29 January 2024 MAIN Ten to 15% of children who were born in the United Kingdom at very low birth

weight (<1500 g) will have major physical impairments that usually require special educational provision, but the majority will enter mainstream school (1). Studies of these children have

shown that as many as 40% may show learning difficulties, often associated with problems of visuospatial perception, minor motor impairments (MMIs), and behavioral difficulties (2, 3). The

origin of these difficulties has been attributed to a delay in neurologic maturation, early cerebral injury, social factors, or poor early growth (4). Magnetic resonance imaging (MRI) has

proved to be a useful tool for the investigation of anomalies of cerebral maturation in a minimally invasive way. Very low birth weight (VLBW) infants show a relatively high prevalence of

MRI-defined cerebral lesions later in childhood (5). Most of these represent degrees of periventricular leukomalacia or more diffuse white matter atrophy. Although evidence of extensive

white matter damage correlates well with major neurologic impairment, there seems to be little if any correlation between signs of lesser damage and intellectual, motor, and behavioral

problems at school age (5). With the introduction of volumetric methods to MRI during the past decade, correlations have been noted between the volumes of parts of the brain and school

performance in children. Associations between the volumes of the caudate nuclei and the hippocampus and learning difficulties and attention deficit have been demonstrated in school-age

children who were born at term (6, 7). Results in children who were born very preterm have been conflicting and have described differences in cerebellar, basal ganglia, total brain, and gray

matter volumes (8–12). This study was designed to test the hypothesis that children who were born very preterm and have cognitive deficits and associated MMIs at school age would show

different caudate and hippocampal volumes from those who were doing well. METHODS As part of a study of school performance of all very preterm children who were born to mothers who resided

in a geographically defined area of Merseyside, UK, during a 2-y period, parents were asked whether they would allow their child to have a cerebral MRI scan (13). The study was approved by

the Local Children's Research Ethics Committee, and written informed parental consent was obtained. All children who were born in 1991 and 1992, whose mothers resided in Liverpool

postal districts, and who were born at <32 completed weeks of gestation were included in the study. Those who were known to be alive at discharge from any of the eight hospitals that

serve the area were traced through their general practitioner to confirm their current health status before their parents were approached. Children who were attending mainstream schools,

with or without special provision, and whose parents agreed to their being studied were matched by sex, age, and first language to a full-term classmate control. Depending on parental and

school wishes, the children were tested at 7–8 y of age, at school or at the Institute of Child Health, Royal Liverpool Children's Hospital. Intelligence was tested using the short form

of the Wechsler Intelligence Scales for Children Version III (14). Motor impairments were tested for using the Movement ABC (15). Measurements of height, weight, and head circumference and

a standardized neurologic examination were done. These tests were performed by an occupational therapist and a graduate psychologist who were used as research assistants for the project. A

parental questionnaire collected demographic data, and a perinatal data sheet was completed from the clinical case notes by a clerical assistant. Cranial ultrasound results were as reported

by the local consultant radiologists. A score below the fifth percentile on the Movement ABC was considered indicative of MMI. MRI scans were performed on a subset of the subjects in the

main study whose parents consented to scanning in addition to the other studies. Payment of travel expenses only was made. Magnetic resonance brain scans were performed on a Philips Gyroscan

NT5 scanner with a field strength of 0.5 Tesla (Philips Medical Systems, Best, Netherlands). The scans consisted of five sequences: sagittal T1 weighted spin-echo, axial T1-weighted

spin-echo, axial T2-weighted turbo spin-echo, coronal fluid-attenuated inversion recovery, and a T1-weighted fast field echo volume acquisition. The fast-field echo sequence (TR = 200 ms, TE

= 30 ms, TI = 13 ms, flip angle = 30 degrees) was used to produce a coronal volume acquisition with a slice thickness of 2 mm and a 1-mm overlap. From this sequence, caudate and hippocampal

volumes were measured on a Easivision workstation (Philips Medical Systems). For reducing scan times during volume acquisition only, the scans did not always include the entire brain, so

total brain volume (TBV) could not be measured from MRI. Instead, an estimate of TBV was calculated using the head circumference measured at the time of testing. We used a published formula

that relates brain size at postmortem examination to occipitofrontal head circumference (OFC) (16). This cannot allow for differences in extracerebral space or ventricular volume but is an

approximation. Caudate and hippocampal volumes could then be expressed as a percentage of estimated TBV to allow for differences in brain size. QUALITATIVE ASSESSMENT OF MAGNETIC RESONANCE

BRAIN SCANS. Scans were systematically assessed for visible lesions consistent with thinning of the corpus callosum (Fig. 1), ventricular enlargement (Fig. 2), periventricular leukomalacia

(Fig. 3), and porencephaly (Fig. 4) by an experienced pediatric radiologist (L.A.). Periventricular leukomalacia was recognized by a characteristic triad of abnormalities: abnormally high

signal within the periventricular white matter on T2-weighted turbo spin-echo and fluid-attenuated inversion recovery images; loss of periventricular white matter, particularly in the

periatrial regions; and compensatory focal ventricular enlargement adjacent to regions of abnormal signal intensity (17). Porencephaly was recognized as a well-defined cavity within the

brain substance, communicating with the lateral ventricle and containing fluid with identical signal characteristics to cerebrospinal fluid (CSF). QUANTITATIVE ANALYSIS OF MAGNETIC RESONANCE

BRAIN SCANS. Hippocampal volumes were measured using the technique previously described by Jack _et al._ (18, 19). The anterior and posterior boundaries were defined, including the whole of

the head of the hippocampus anteriorly and using the crus of the fornix as the posterior anatomic landmark. The in-plane boundaries were then traced sequentially on each slice. The head of

the hippocampus was separated from the amygdala by the uncal recess of the temporal horn of the lateral ventricle; in cases in which the uncal recess was not patent, an arbitrary horizontal

line was drawn through the most superomedial portion of the temporal horn. The boundaries of the hippocampal body and tail were defined laterally by CSF in the temporal horn of the lateral

ventricle, superiorly by CSF in the choroid fissure, medially by CSF in the uncal and ambient cistern, and inferiorly by the interface between the gray matter of the subiculum and the white

matter of the parahippocampal gyrus (Fig. 5). These anatomic landmarks have been shown to define reliably 90–95% of the total hippocampal volume (20). Volumes of the caudate nuclei were

measured using a similar technique. The boundaries of the caudate nucleus were defined anteriorly and laterally by the interface with the white matter of the frontal lobe and the anterior

limb of the internal capsule, and medially by CSF in the lateral ventricle (Fig. 6). The posterior boundary was arbitrarily defined by the most anterior coronal section to show the crus of

the fornix, as used to define the posterior boundary of the hippocampus. The slender tail of the caudate nucleus, which extends around the posterior part of the lateral ventricle, was not

measured. Once boundaries had been drawn on each coronal image, volumes were calculated automatically by the workstation using a volume of interest function. The ratio of the volumes of the

structures (left:right) was calculated as a percentage. The reliability of this technique was assessed as follows. Volume measurements on a convenience sample of 25 scans were made

independently by two observers. Intraobserver and interobserver variation was calculated by the Bland-Altman method (21). For volume measurements of the hippocampal formations, 95%

confidence intervals of agreement (intraobserver) were between −161 and 165 mm3. For interobserver variation, 95% confidence intervals of agreement were between −145 and 163 mm3. These

results (<±7%) are comparable with those in previous studies (18, 20) that have indicated that MRI-based measurements of these brain structures can be made with a high degree of

reproducibility. All volume measurements were made by one of the authors (L.A.), who was blind to the clinical assessments. Statistical analysis of the data were performed using SPSS version

10. RESULTS A total of 382 children had been discharged from the eight hospitals that serve the area during the period covered by the study, and 335 were alive and attending mainstream

school at 7 y. A total of 286 parents permitted their children to be tested at school, and 126 parents initially consented to their children's undergoing MRI scans; 15 later changed

their minds or failed to attend, three were unable to cooperate and satisfactory scans were not obtained, scan data were lost for two children because of a technical failure, and in one

child artifact from fixed dental braces prevented accurate volume measurement. A total of 105 children had satisfactory scans. No sedation was used. Scans were completed within 6 mo of

testing at school. Mean age at testing was 7 y 4 mo. The perinatal characteristics of children who were scanned are shown in Table 1. The characteristics of the children who were scanned and

not scanned at age 7 y are similar, although children who were scanned had a significantly smaller head circumference and higher performance IQ (PIQ; Table 2). Of the 105 preterm children

scanned, 20 (19%) showed a cerebral lesion on MRI. Lesions consistent with periventricular leukomalacia were present in 14 (12%), any ventricular dilation in 14 (11%), thinning of the

posterior part of the corpus callosum in eight (9%), and with porencephaly in two (2%) (Table 3). Several children had more than one lesion type. Mean and median values for IQ and ABC scores

are given in Table 2. Mean estimated TBV was 1,225,000 (138,000) mm3. TBV was correlated with ABC (_r_ = −0.233, _p_ = 0.02) but not when children with visible MRI abnormalities were

excluded. When only children with “normal” scans were considered, TBV was correlated with PIQ (_r_ = 0.252, _p_ = 0.029). Mean (SD) right and left caudate volumes were 4633 (807) and 5425

(789) mm3, and right and left hippocampal volumes were 2906 (490) and 2813 (429) mm3, respectively. Median (interquartile range) right and left caudate volumes as a percentage of TBV were

3.8 (3.4–4.1) and 3.7 (3.2–4.1) and for the right and left hippocampus were 2.4 (2.1–2.6) and 2.3 (2.0–2.6). Table 4 shows the mean values for volumes in children with IQs above and below

80, and Table 5 shows the mean values in children with ABC scores above and below the fifth percentile. Table 6 shows the correlations between the volume data and ABC and IQ scores for all

children, and Table 7 shows the correlations for only children who did not have a visible lesion on MRI scan. Significant correlations between IQ scores and caudate volumes are seen, which

largely persist when children without visible lesions alone are considered. Significant correlations for caudate volumes as a percentage of TBV persist only for PIQ. No significant

correlations between hippocampal volumes and ABC or IQ scores were observed. This was also true when hippocampal volumes were correlated with subsets of the IQ test used. DISCUSSION In our

previous work (5), we described the results of MRI brain scans in a cohort of adolescents (age 15–17 y) who had a history of VLBW (<1500 g) but no major disability and were born between

1980 and 1983. There was a high prevalence (42.5%) of structural brain abnormalities, although these abnormalities showed poor correlation with IQ and attention-deficit/hyperactivity

disorder (12). Similar results have been found in other studies. Skranes _et al._ (8) found no correlation between MRI abnormality and IQ in VLBW children without disability at 6 y of age,

and Krageloh-Mann _et al._ (9) found no difference in performance in intelligence tests in very preterm children, with and without MRI abnormalities. Stewart _et al._ (10) and Rushe _et al._

(11) reported the results of MRI brain scans and neuropsychological outcome at age 14–15 y of a cohort of 75 participants who were born at <33 wk gestation; 55% of this group had

structural brain abnormalities demonstrated on MRI brain scans, but those with abnormal MRI brain scans did not perform less well on any measure of cognitive function. There was also a lack

of correlation of gestational age and birth weight with neuropsychological outcome but a significant correlation between abnormal MRI scans and behavioral problems. In the group of VLBW

children that we studied at age 15–17 y, we found positive associations between full-scale IQ and caudate volumes, and attention-deficit/hyperactivity disorder and hippocampal volumes (12).

The subjects of our present study were born in 1991 and 1992. The selection of subjects was geography and gestation based rather than hospital and birth weight based. The prevalence of

structural brain abnormalities was 18.5%, much lower than in our previous study. The reason for this difference is uncertain. Recruitment criteria for the two groups were different, and

improvements in neonatal care may have had an effect on the prevalence of perinatal brain injury. Table 1 shows the perinatal characteristics of the present cohort, which shows that most

were not particularly ill in the neonatal period, but they are more likely to represent the population as a whole than a hospital-based cohort from a referral center. In both studies, there

was self-selection, in that the children and their parents had to consent to be scanned. Table 2 suggests that those who were scanned were broadly similar at age 7 y to the rest, although

those who were scanned had significantly smaller OFC and higher PIQ. In this cohort, volumes of the right and left caudate nuclei were significantly correlated with IQ but not with ABC

scores (Tables 4–6). There was no significant correlation between IQ and ABC scores and hippocampal volume measurements. The relationship between IQ and caudate volume could simply represent

the well-known correlation between brain size and IQ. When caudate volumes were expressed as a percentage of estimated TBV, the correlations remained significant except for that between

verbal IQ and right caudate volume percentage, suggesting that this was not the case (Table 6). When only the 85 children with apparently normal MRI scans were examined, the correlations

were weaker yet remained significant for most comparisons (Table 7). Volumes as a percentage of TBV remained significantly correlated only with PIQ (Table 7). Isaacs _et al._ (22) reported

the results of a study of 11 adolescents with a history of prematurity (<30 wk gestation). They had significantly smaller hippocampal volumes bilaterally and showed specific defects in

certain aspects of everyday memory. Regression analyses indicated that hippocampal volume was the best predictor of performance in tests of everyday memory. Some of the subscales of the IQ

test that we used involve aspects of short-term memory, but we were unable to show a correlation between them and hippocampal size. The hippocampal volumes measured in our present cohort

were not smaller than would be expected for an age of 7 y. Peterson _et al._ (23) studied a group of 25 preterm children at 8 y of age with quantitative MRI scans and found that regional

cortical volumes and basal ganglia and hippocampal volumes were smaller in preterm children than in control subjects. When corrected for TBV, basal ganglia and hippocampal volumes seemed to

be disproportionately reduced. In this group, full-scale IQ seemed to correlate most strongly with regional cortical volume, although some association with basal ganglia volumes was

demonstrated. This is in keeping with our findings in this cohort. The selection criteria for this group differed from our present study in that children were selected on the basis of birth

weight (<1250 g), and children with MMI were not excluded. Our results suggest that the final volume attained by key cerebral structures such as the caudate nuclei are important

determinants of cognitive function in preterm children. We were not able to study many other regions of the brain volumetrically, although recent studies in children who were born preterm

have highlighted volume differences in the cerebellum (24) and in total and gray matter volumes that have correlated with later cognitive function. Any of these differences may represent

evidence for disordered development of the preterm brain after perinatal injury, rather than a focal lesion affecting cognitive function. The hippocampus and basal ganglia are particularly

susceptible to injury in preterm infants; hippocampal abnormalities were found in 67% of autopsies of preterm infants (25). Hypoxia, metabolic disorders, nutritional impairment, and

infections all may affect the developing brain. The hippocampus is known to be selectively vulnerable to hypoxic-ischemic injury (26), hypoglycemia (27), and hypothyroidism (28). Lucas _et

al._ (29) showed that IQ in preterm children at age 7–8 y showed significant differences depending on nutritional intervention shortly after birth. Brain growth is most rapid around the time

of term in human infants, and the period between birth and term is one of relative malnutrition for many preterm infants. Nutritional impairment of these vulnerable infants at this time may

be of particular importance in limiting the development of key cerebral structures. Neonatal interventions to counteract this might lead to improved function later in this group of infants.

ABBREVIATIONS * CSF: cerebrospinal fluid * MMI: minor motor impairment * MRI: magnetic resonance imaging * PIQ: performance IQ * TBV: total brain volume * VLBW: very low birth weight

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preterm babies and later intelligence quotient. _BMJ_ 317: 1481–1487. Article  CAS  Google Scholar  Download references ACKNOWLEDGEMENTS We thank Mrs. G. Hughes and Mrs. D. Garlick, Mrs. J.

Glynn, and Mrs. H. Tyrer for their skill and patience in performing the MRI scans; Mr. David Campling from Philips Medical Systems and Dr. Peter Cole from IRS for technical advice; Dr. M.

Palaniappan for assistance with MRI measurements; and Dr. Gillian Lancaster, Lecturer in Medical Statistics at the University of Liverpool, for statistical advice. Dr. Lynda Foulder-Hughes

and Dr. Lisa Thompson tested the children at school. Special thanks are due to the parents and children who gave their time to help in this study. AUTHOR INFORMATION AUTHORS AND AFFILIATIONS

* Department of Medical Imaging, Royal Liverpool Children's Hospital, Eaton Road, Liverpool, L12 2AP, United Kingdom Laurence J Abernethy * Department of Child Health, University of

Liverpool, Institute of Child Health, Royal Liverpool Children's Hospital (Alder Hey), Liverpool, L12 2AP, UK Richard W I Cooke & Lynda Foulder-Hughes Authors * Laurence J Abernethy

View author publications You can also search for this author inPubMed Google Scholar * Richard W I Cooke View author publications You can also search for this author inPubMed Google Scholar

* Lynda Foulder-Hughes View author publications You can also search for this author inPubMed Google Scholar CORRESPONDING AUTHOR Correspondence to Laurence J Abernethy. RIGHTS AND

PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Abernethy, L., Cooke, R. & Foulder-Hughes, L. Caudate and Hippocampal Volumes, Intelligence, and Motor

Impairment in 7-Year-Old Children Who Were Born Preterm. _Pediatr Res_ 55, 884–893 (2004). https://doi.org/10.1203/01.PDR.0000117843.21534.49 Download citation * Received: 17 July 2002 *

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