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Academic Achievement of Small-for-Gestational-Age Children at Age 10 Years
Outi Hollo, MD, PhD;
Päivi Rautava, MD, PhD;
Tapio Korhonen, PhD;
Hans Helenius, MSc;
Pentti Kero, MD, PhD;
Mattiä Sillanpää, MD, PhD
Arch Pediatr Adolesc Med. 2002;156:179-187.
ABSTRACT
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Objectives To provide current information on the academic achievement of small-for-gestational-age
(SGA) children at age 10 years, to analyze predictors, and to evaluate the
smallness of a newborn as a risk factor for school failure.
Design Prospective, population-based birth cohort study with 10-year follow-up.
Participants The SGA group consisted of 106 children born in 1985 whose birth weight
had been below the 2.5th percentile on the population-based fetal growth chart.
The control group consisted of 105 appropriate-for-gestational-age (AGA) children
born as closely as possible in time to SGA infants and matched for gestational
age and mode of delivery. Both groups were evaluated at age 10 years.
Main Outcome Measure Academic achievement.
Results Twenty-five percent of SGA children were school failures (vs 14% of
AGA children; P = .05). There were significantly
more SGA than AGA children with unfavorable backgrounds and deficient performances
associated with poor academic achievement. Independent predictors of poor
academic achievement in SGA and AGA children were inattention-passiveness
as rated by their teachers (masked to grouping; corresponding to a 1-point
increase in inattention-passiveness score: odds ratio, 5.1; 95% confidence
interval, 2.1-12.1), a low verbal IQ score (psychologists masked; corresponding
to a 10-point decrease in IQ score: odds ratio, 3.2; 95% confidence interval,
1.6-6.2), and restlessness at the follow-up visit (one examiner masked and
the other not; odds ratio, 14.3; 95% confidence interval, 2.1-97.3).
Conclusion Being SGA at birth has a clinically significant impact on the academic
achievement of a 10-year-old child.
INTRODUCTION
SUCCESS IN school is an excellent marker of general adolescent well-being.
School failure—poor academic performance often together with conduct
problems—is a powerful sign of other high-risk behaviors, with possible
subsequent school dropout and social marginalization. There are several well-recognized
risk factors associated with school difficulties, for instance, behavioral
disorders, low self-esteem about one's academic ability, and a disadvantaged
home background.1
Newborns can be small for many reasons. As long as an unequivocal criterion
that is easily applicable in the clinical setting for malnourishment of a
newborn is not available, the consensus is the lightness of a newborn (birth
weight for gestational age >2 SDs below the mean birth percentile). On the
whole, it is crucial that the intrauterine growth of a newborn is assessed
because small-for-gestational-age (SGA) infants as a group are at risk for
developmental disorders,2 for remaining smaller
than their peers,3 and for chronic diseases
in older age.4 Currently, approximately two
thirds of SGA children are born without any suspicion of their potential intrauterine
growth failure,5 and many SGA infants are discharged
from obstetric units without any diagnosis of potential growth failure.6 Therefore, it is not reasonable to suppose that those
in primary care will pay enough attention to the intrauterine growth retardation
(IUGR) of an infant or child. Previous studies7
seem to support the fact that SGA children are prone to cognitive deficits.
Evaluations of the success of SGA children in school beyond the preschool
years are few, with different definitions of SGA and varying information on
the predictors of academic achievement. Studies have focused on different
populations, for example, preterm, very low-birth-weight SGA children8-10; preterm and full-term
SGA children as one group11 or as separate
groups with different definitions12 or the
same definition13 of SGA for preterm and full-term
children; clinically intrauterine malnourished, full-term children14; and full-term SGA adolescents only.15
Our follow-up study was undertaken in 1985. The perinatal risk factors
and neonatal complications have been reported previously.16-17
The aim of the present phase of the study is to investigate the academic achievement
of SGA children and control appropriate-for-gestational-age (AGA) children
at age 10 years and to evaluate the associations of perinatal history, sociodemographics,
neurological status, head growth, several neurocognitive abilities, and behavior
with academic achievement. Does the smallness of a newborn need to be recognized
as a potential risk factor for poor school performance?
PARTICIPANTS AND METHODS
PARTICIPANTS
SGA Group
The SGA group consisted of all 118 SGA infants from the original birth
cohort born in 1985 in the catchment area of the Turku University Central
Hospital in southwestern Finland (Figure 1). The only recruitment criterion was birth weight for gestational
age below the 2.5th percentile (corresponding to a birth weight >2 SD below
the mean birth percentile) on the regional population-based fetal growth chart.18 The mean birth weight of SGA infants was 2452 g (range,
540-2930 g), and the mean gestational age was 38.8 weeks (range, 27.0-42.0
weeks). Eight SGA infants (7%) were born prematurely. Forty-six SGA infants
(39%) were born at community hospitals, and the remainder were born at the
Turku University Central Hospital, which serves as a tertiary-level perinatal
center in the region concerned. Thirteen SGA infants were born from twin pregnancies.
None of the infants had a history of intrauterine infection. Except one Indian
father and one Portuguese mother, all the parents were ethnically homogeneous,
that is, Finnish, with 4% having Swedish as their first language.
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Figure 1. Follow-up profile of small-for-gestational-age
(SGA) and appropriate-for-gestational-age (AGA) children.
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After the exclusions (Figure 1),
the total number of eligible survivors in the SGA group was 112; 106 (95%)
of them were available for study at age 10 years. Their gestational ages ranged
from 27 to 42 weeks (mean, 38.8 weeks). The attrition analysis showed that
neither the age (P = .28) nor the basic education
(P = .85) of the mothers or the degree of domicile
urbanization (P = .22) in participants differed significantly
from those in the 6 nonparticipants, whereas the birth weight (P = .03) and the SGA index (P = .002) were
significantly higher in nonparticipants, indicating less severe IUGR. The
SGA index was calculated by dividing actual birth weight by a 50th percentile
reference birth weight, and it is presented as a percentage.
Control AGA Group
The control AGA group was randomly selected and consisted of 118 singletons
matched for gestational age (mean, 38.8 weeks; range, 27-42 weeks) and mode
of delivery and born at the Turku University Central Hospital as closely as
possible in time to the study group SGA infants (Figure 1). The birth weight was appropriate for gestational age,
that is, between the 10th and 90th percentiles on the same fetal growth chart
(mean birth weight, 3378 g; range, 1210-4100 g). Eight AGA children were born
prematurely. None of the infants had evidence of chromosomal or congenital
abnormality at birth.
The total of 105 AGA children were evaluated at age 10 years. Their
mean gestational age was 38.9 weeks (range, 27.0-42.0 weeks). Participants
and nonparticipants did not differ significantly regarding maternal age (P = .58), maternal basic education (P = .09), or degree of domicile urbanization (P
= .25).
METHODS
The perinatal history of SGA and AGA children was evaluated in 1995
by means of hospital records (Table 1).
Although the birth weight of SGA children was less than the 2.5th percentile,
the degree of the severity of IUGR was further evaluated as an SGA index (mean,
70.7%; range, 46.1%-78.4%).
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Table 1. Assessment Battery and 10-Year Follow-up Data Available for
Analysis*
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All the children were examined at the mean (SD) age of 10.1 (0.2) years
(range, 9.4-10.8 years) during outpatient clinic visits at the Turku University
Central Hospital. Table 1 gives
the assessment battery and the amount of data available for analysis. In addition
to routine pediatric examination, neurological examination was performed by
one of us (O.H.). Head circumference was measured using a flexible metallic
measuring tape as the maximum circumference between the supraorbital ridge
and the occiput. The classification of subnormal head circumference (>2 SDs
below the reference percentile) was based on the reference data of the Finnish
growth charts.26 To obtain sociodemographic
information, the parent(s) was interviewed by one of us (O.H.).
For an overall measure of intellectual ability, the Finnish or Swedish
version of the revised Wechsler Intelligence Scale for Children–Revised
(WISC-R) was used.27 The tests were conducted
by 2 psychologists who were masked to grouping. The WISC-R subtests were also
grouped into 3 domains according to Kaufman.28
A comprehensive battery of tests was administered to test visuomotor perception,
fine motor abilities, memory, and attention (Table 1).
The classroom teachers were asked to rate the child's behavior at school
by completing the Conners' Abbreviated Teacher Rating Scale34
(4-point scale: "not at all true" to "very true" of the child). The teachers
were masked to grouping. The child's behavior at home was assessed by the
mother, the father, or both by means of the Conners' Abbreviated Parent Rating
Scale.34 When both maternal and paternal ratings
were available, the mean score was taken as representative. The child's behavior
was also evaluated during the follow-up visit by the pediatrician (O.H.) and
the psychologists (behavior scale: timid, restless, or appropriate).
In Finland, there were no standardized achievement tests available in
1995. Therefore, to rate the academic achievement of a child, the type of
education (special vs mainstream) was first taken into account. All the children
in special education were intellectually disabled, that is, they had an intellectual
impairment instead of physical, sensory, or behavioral impairments as a reason
for not attending mainstream school. The children in mainstream education
were divided according to whether they were in an appropriate grade level
or not. The academic achievement of the children in an appropriate grade level
was assessed on the basis of their school reports. The classroom teacher was
asked to post a copy of a child's school report on which mathematics and reading
and writing were assessed. The school report assessments were rescored as
good (knowledge or skill attained) or poor (knowledge or skill not attained).
Among school failures were children (1) who were in special education; (2)
who were in an inappropriate grade level, that is, they had either repeated
a grade or started basic education later than their peers; or (3) whose achievements
in mathematics, reading and writing, or both were rescored as poor.
In Finland, basic education starts in August for children turning 7
years of age during the year concerned. The comprehensive school education
has been a 9-year course since the early 1970s. The school system aims to
keep every child in mainstream education, if necessary with remedial teaching
or school assistants. If children still cannot keep up with the others in
class, they are referred to a class or school for special education. The school
performance rating system is based on assessments by a teacher expressed either
numerically (scale: fail = 4 to excellent pass = 10) or in words (indicating
whether a pupil has attained a certain skill or knowledge or not).
STATISTICAL ANALYSIS
To test the differences between SGA and AGA children, the 2-sample t test (parental age, head growth, auditory memory, visual
memory, and fine motor abilities), Fisher exact test (perinatal history, neurological
status, intelligence, and academic achievement), Mann-Whitney test (attention,
memory and verbal learning, visuomotor integration, and questionnaires on
behavior), and Pearson  2 test (socioeconomic status, parental
basic education, and behavior at the follow-up visit) were applied. Evaluations
of the univariate association between academic achievement and predicting
variables were performed using cross tabulation and the 2
test. This univariate analysis was followed by multivariate analysis with
stepwise logistic regression. The variables were classified into subgroups,
and the analyses were initially carried out for variables within one subgroup
at a time and afterward for all statistically significant variables irrespective
of grouping. P<.05 was used as the cutoff point
of significance. Odds ratios and 95% confidence intervals were calculated
from the logistic regression models.
The study was approved by the Joint Commission on Ethics of the University
of Turku and the Turku University Central Hospital. Informed written consent
was obtained from the parent(s) of the children.
RESULTS
PERINATAL HISTORY
The frequency of the perinatal risk factors was 18% in the SGA group
and 12% in the AGA group (P = .27). Two SGA children
had 5-minute Apgar scores of 0 to 3, 2 SGA children had umbilical artery pH
less than 7.0, 10 SGA and 13 AGA full-term children had bilirubin levels greater
than 12 mg/dL (>205 µmol/L) and 1 AGA preterm child had a bilirubin
level greater than 15 mg/dL (>255 µmol/L), and 8 SGA children had blood
glucose levels less than 30 mg/dL (<1.7 mmol/L). Blood glucose and bilirubin
levels were determined only if clinically indicated.
SOCIOECONOMIC AND NEUROLOGICAL STATUS
The socioeconomic status of the family and parental basic education
were significantly better in AGA than in SGA children (Table 2).
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Table 2. Sociodemographics of the Parents of Small-for-Gestational-Age
(SGA) and Appropriate-for-Gestational-Age (AGA) Children*
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Eleven SGA children and 3 AGA children had major neurological or sensory
impairments (P = .049): 3 had cerebral palsy (2 SGA
and 1 AGA), 1 (SGA) was blind without any known cause, 2 had severe hearing
loss needing hearing aid (1 SGA and 1 AGA), and 8 were intellectually disabled
(7 SGA and 1 AGA). Three neurological assessment domains by Touwen25 showed significant differences between SGA and AGA
children, namely, coordination of the extremities (right fingertip nose test, P = .003; left fingertip nose test, P = .02; and right diadochokinesis, P = .03),
balance of trunk (walking along a straight line, P
= .003), and gross motor functions (standing on left leg, P = .007; standing on right leg, P = .04),
with respect to which SGA children performed poorer.
HEAD GROWTH
The mean head circumference (presented as an SD from reference circumference)
of SGA children (–0.98) was significantly smaller than that of AGA children
(+0.09; P<.001). The percentage of children with
subnormal head growth at age 10 years was significantly greater in the SGA
group than in the AGA group (14% vs 2%; P = .001).
Among the mothers of these 15 children with subnormal head circumference,
3 (2 of SGA children and 1 of AGA children) had similarly subnormal head circumferences.
The head circumferences of the fathers were within the reference range (measurement
was missing for 5 fathers). The SGA index, the degree of the severity of IUGR,
indicated a significant correlation with 10-year head circumference (r = 0.27; P = .008).
NEUROCOGNITIVE ABILITIES
The mean WISC-R verbal, performance, and full-scale IQ scores of SGA
and AGA children are presented in Table
3. According to the results on the WISC-R, 5% of SGA children (vs
1% of AGA children) were mentally retarded (full-scale IQ score <70), 15%
(vs 12%) had borderline IQ scores (full-scale IQ score of 70-84), and 80%
(vs 87%) had normal intelligence (full-scale IQ score  85); the differences
were not statistically significant. Although SGA children showed significantly
lower overall intellectual performance, the profiles of the WISC-R subtests
were similar for SGA and AGA children (Figure
2). The SGA children had significantly poorer short-term auditory
memory and perceptual organization ability and a higher incidence of inattention
than AGA children (Table 3).
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Table 3. Neurocognitive Performance of Small-for-Gestational-Age (SGA)
and Appropriate-for-Gestational-Age (AGA) Children
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Figure 2. Wechsler Intelligence Scale for
Children–Revised (WISC-R) scaled score means (SEMs) for small-for-gestational-age
(SGA) and appropriate-for-gestational-age (AGA) children at age 10.1 years.
Asterisk indicates P<.05.
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BEHAVIOR
Most children behaved themselves in an appropriate manner throughout
the follow-up visit. However, 10% of the SGA children were restless (vs 5%
of AGA children), and 15% were overtly timid (vs 5% of AGA children; P = .02). According to the parents, SGA children had significantly
more learning problems than AGA children; the median scores (and interquartile
ranges [IQR = Q3-Q1, where Q1 and Q3 correspond to the 25th and 75th percentiles,
respectively]) were 0.50 (0.89) and 0.38 (0.53), respectively (P = .007). The teachers' reports revealed more inattention-passiveness
in SGA children than in AGA children (0.63 [0.91] vs 0.44 [0.88]), which was
not significant (P = .07).
ACADEMIC ACHIEVEMENT
The academic achievements of 103 of 106 SGA and 100 of 105 AGA children
were assessed. Twenty-six SGA children (25%) and 14 AGA children (14%) were
school failures (P = .05). Seven SGA children (7%)
were in special education owing to intellectual disability compared with 1
AGA child (1%; P = .07). Three SGA children had repeated
a grade, and another 3 had started basic education 1 year later than their
peers, whereas all the AGA children except the child in special education
were in mainstream education at an appropriate grade level (P = .01). There were 13 SGA and 13 AGA children in mainstream education
whose assessments for mathematics, reading and writing, or both were rescored
as poor. According to the behavioral questionnaires, the parents of SGA children
reported significantly more learning problems than those of AGA children.
PREDICTORS OF ACADEMIC ACHIEVEMENT
The adverse perinatal history of SGA children was in association with
their school achievement (P = .049), whereas in AGA
children it was not. Factors such as prematurity, birth weight less than 2000
g, maternal smoking, maternal diseases, and IUGR suspicion during pregnancy
were not associated with poor academic achievement in SGA or AGA children.
The numbers of SGA children with various unfavorable background factors and
deficient performances were significantly greater than the numbers of AGA
children (Figure 3).
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Figure 3. Statistically significantly different
characteristics of small-for-gestational-age (SGA) children compared with
their appropriate-for-gestational-age (AGA) peers.
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According to the univariate analysis, the school failures in both groups
shared several factors significantly associated with poor academic achievement
(Table 4). The subsequent multivariate
logistic regression analysis that was first conducted for significant variables
within every predictor subgroup, each of which having the smallness for gestational
age of a newborn as 1 variable, was followed by the analysis between the predictor
subgroups. The independent predictors of poor academic achievement were inattention-passiveness
as rated by teachers, a low WISC-R verbal IQ score, and restlessness at the
follow-up visit (Table 4).
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Table 4. Analysis of the Association Between the Predictors and Academic
Achievement*
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COMMENT
Our study showed SGA children performing worse at school than matched
AGA controls. The result was derived from a population-based, prospective
follow-up study with nonclinical participants; an internationally agreed-on
definition of SGA; a representative enrollment rate; a high retention rate;
an excellent return rate; use of standard instruments; controls matched for
gestational age; and masking of the developmental assessors except the pediatrician
(O.H.). Because of the lack of standardized achievement tests, academic achievement
was evaluated from 3 points of view: type of education, appropriateness of
grade level, and assessments in school reports. The AGA children approximated
to a normal Finnish population with respect to academic achievement, head
growth, and neurological status. Some predictors of poor academic achievement
concerned only SGA children, such as the adverse perinatal history, whereas
the independent predictors—inattention-passiveness, a low verbal IQ
score, and restlessness—were shared by SGA and AGA children.
The most powerful independent predictor of academic achievement was
the child's inattentive-passive behavior at school. Such internalizing or
withdrawn behavioral problems have been reported in association with IUGR.35 Furthermore, the stability with regard to internalizing
problems, attention problems, and social problems is high in SGA, although
preterm, children.36 The teachers consistently
rated SGA children as more problematic in all 3 domains by Conners. The parents'
ratings varied widely and were inconsistent with those of the teachers, with
the exception that it was agreed that SGA children had more learning problems
(one main domain in the parent rating scale and a single item of the inattention-passiveness
domain in the teacher rating scale) than AGA children. Parents may overreport
as often as underreport problems with their children. It is also possible
that parental attitudes change with time so that parents might be more anxious
in the first years of the lives of their children with a perinatal hazard
but develop a tolerance for problems as their children grow older.36
The second most powerful predictor was verbal IQ score. On average,
the overall intellectual performance of SGA children was lower than that of
AGA children but within the reference range.15, 37
Sameroff38 showed that every environmental
risk factor is able to reduce the child's IQ score by 4 points. To our knowledge,
the rate of mental retardation (full-scale IQ score <70) among SGA children
has not been reported; in our study, 5% of SGA children were mentally retarded
(vs 1% of AGA children). Head growth can be used as an index of overall brain
development.39 We confirmed the trend for children
failing at school having smaller head circumferences than those performing
well at school.9 Ounsted et al40
and Hack et al9 found a significant mother-child
correlation for head circumference. In our study, only 3 of 15 children with
small head circumference had a mother with small head circumference, indicating
the possible genetic effect. Thus, the greater incidence of small head circumference
in SGA children might be a manifestation of IUGR.9, 41-42
Poor head growth may result from hypoxic-ischemic encephalopathy without IUGR.43 Among small-headed children, none had umbilical artery
acidemia, and only 1 had a low 5-minute Apgar score, indicating potential
asphyxia. Magnetic resonance imaging diagnostic for hypoxic-ischemic encephalopathy
was not performed at the time the study children were born.
The third most powerful predictor was restless behavior during the outpatient
clinic visit as rated by the examiners. Other studies8, 44
also show similar overactive behavioral characteristics in association with
IUGR. The pediatrician involved in examining the 10-year-old study children
practically corresponded with a community pediatrician or school physician
in his or her work. Schoolchildren showing restlessness or difficulties in
concentration in a face-to-face situation should be provided with an overall
evaluation of their school performance.
To prevent adverse sequelae of IUGR, we would like to emphasize not
only potentially preventable risk factors such as fetal challenge to smoking45 but also diagnostic tools for IUGR46
and the best date to deliver the growth-retarded fetus.46
The SGA children are at risk for an adverse outcome. It has been reported
previously12 that full-term SGA children perform
more poorly at school than do preterm AGA children, indicating the significance
of IUGR—and not of gestational age as such. As early as the 1970s, Neligan
et al47 declared that "it is better to be born
too soon than too small." However, there are studies48
concerning the academic achievement of low-birth-weight children that disadvantageously
leave the relation of gestational age to birth weight unaddressed.
Characteristics such as hyperactivity, verbal deficits, and attention
problems recognizable in early childhood can predict school difficulties and
should arouse the attention of those involved in child health. A focus should
be put on school quality and community support, too. Failure in the first
years of school may result in low self-esteem and behavioral problems that
might be antecedents of high-risk behaviors and school dropout. Strauss49 showed that those born SGA not only have increased
academic difficulties persisting into adolescence but also deficits in professional
and economic attainment in adulthood. Prenatal growth failure should be recognized
as a risk factor for school failure, although not only SGA children but all
children at risk need effective programs for managing learning difficulties.
In conclusion, SGA children perform poorer at school than their AGA
peers. Independent predictors of poor academic achievement in SGA and AGA
children are inattention-passiveness as rated by teachers, low verbal IQ score,
and restlessness. There are poorer performances in neurocognitive tests and
less favorable socioeconomic background among SGA children than among AGA
children. The smallness of a newborn is worth recognizing as a risk factor
for school failure.
| What This Study Adds
This prospective, population-based, birth cohort, 10-year follow-up
study shows that SGA children have neurocognitive deficits, behavioral problems,
and less favorable sociodemographic backgrounds associated with poor academic
achievement.
The number of school failures among SGA children is nearly twice as
great as among their AGA peers. Being SGA at birth is worth recognizing as
one of the risk factors for poor school performance.
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AUTHOR INFORMATION
Accepted for publication September 30, 2001.
This study was supported by the Local Turku Fund of the Foundation for
Pediatric Research, the South-West Finnish Fund of Neonatal Research, and
the Turku University Foundation, Turku.
We thank Heikki Lyytinen, PhD, from the University of Jyväskylä,
Finland, who kindly made the computerized test of attention available for
us; Olli Kaleva, BSc, for skillful computation of the statistical analyses;
and Eija Suopajärvi for secretarial assistance.
Corresponding author and reprints: Outi Hollo, Department of Public
Health, University of Turku, Lemminkäisenkatu 1, FIN-20014 Turun Yliopisto,
Finland (e-mail: outi.hollo{at}utu.fi).
From the Department of Public Health (Dr Hollo), the Turku City Hospital
(Dr Rautava); and the Departments of Child Psychiatry and Psychology (Dr Korhonen),
Biostatistics (Mr Helenius), Paediatrics (Dr Kero), and Child Neurology (Dr
Sillanpää), University of Turku, Turku, Finland.
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