School Performance in Adolescents With and
Without Periventricular–Intraventricular
Hemorrhage in the Neonatal Period
Margot van de Bor* and Lya den Ouden†
Long-term sequelae of preterm birth have been studied extensively up until the age of 5 to 8 years.
However, the cognitive development of adolescents born preterm has received limited attention. The
objective of this study is to determine school performance in adolescents born very preterm. We have
followed up a cohort of 484 infants born before 32 weeks of gestation in whom cranial ultrasound was
routinely and systematically performed. School performance was assessed in the surviving adolescents at 14 years of age. The outcome variable divided the adolescents into three groups: (1) normal,
(2) slow learners, and (3) special education. School performance data were obtained from 278 of 304
surviving adolescents; 129 performed normally, while 107 were slow learners, and 42 needed special
education. From the unadjusted odds ratios for the need of special education by the various perinatal
factors, only the odds ratio for periventricular–intraventricular hemorrhage was significantly associated (2.56, 95% confidence interval 1.17-4.86). Logistic regression analysis revealed that, after
correction for possible confounding factors, the odds ratios for special education were significantly
higher for adolescents with all grades of periventricular–intraventricular hemorrhage. Less than 50%
of adolescents born before 32 weeks gestation perform normally in school. Periventricular–intraventricular hemorrhage, including the lower grades, does have an unfavorable additional effect on
school performance.
© 2004 Elsevier Inc. All rights reserved.
eriventricular–intraventricular hemorrhage
(PIVH) in preterm infants has received ample attention in the past two decades. Due to a
better understanding of the etiology and improved clinical management and treatment, the
incidence of PIVH has declined over the past
two decades from 30 to 40% in the early 1980s to
less than 20% in the 1990s.1-5 Long-term sequelae of PIVH have been studied extensively up
until the age of 5 to 8 years.6-9 The outcome data
of children with more severe grades of PIVH are
rather consistent. These children suffer mental
retardation and cerebral palsy.6,7 However, the
outcome of children with lower grades of PIVH
is subject for discussion. Some authors report no
independent effect of lower grades of PIVH on
long-term outcome,10,11 while other researchers
describe that children with lower grades of PIVH
do have more disabilities and/or handicaps than
children without PIVH in the neonatal period.8,12
PIVH impact on the academic achievement of
adolescents remains to be explored. We reported before on the neurodevelopmental outcome at the age of 2 and 5 years of very preterm
born children with and without PIVH in the
P
neonatal period, as part of the Project on Preterm and Small for gestational age infants in the
Netherlands (POPS).6,13 The aim of this study is
to assess school performance at the age of 14
years in the same study cohort.
Methods
During 1983, infants born in the Netherlands
with a gestational age of less than 32 completed
weeks and/or a birth weight below 1500 g participated in a prospective national survey on
morbidity and mortality, which had a compliance rate of 94%.14 At that time, cranial ultraFrom the *Department of Pediatrics, University of Nijmegen Medical
Center, Nijmegen, The Netherlands; and †TNO Prevention and
Health, Leiden, The Netherlands.
Address reprint requests to Margot van de Bor, MD, PhD,
Department of Pediatrics, University of Nijmegen Medical Center,
P.O. Box 9101, 6500 HB Nijmegen, The Netherlands; e-mail:
m.vandebor@cukz.umcn.nl
This study is part of the Project on Preterm and Small for gestational
infants in the Netherlands (POPS).
© 2004 Elsevier Inc. All rights reserved.
0146-0005/04/2804-0000$30.00/0
doi:10.1053/j.semperi.2004.08.007
Seminars in Perinatology, Vol 28, No 4 (August), 2004: pp 295-303
295
296
van de Bor and den Ouden
sound was routinely and systematically performed in 6 of the 8 neonatal intensive care
units in the country. We studied prospectively
the incidence of PIVH and subsequent neurodevelopmental outcome in a cohort of 484 infants
born before 32 completed weeks, ie, all infants
within that gestational age group who were admitted to any of the 6 neonatal intensive care
units with cranial ultrasound scanning.15 Infants
with congenital malformations were excluded
from the study. Follow-up data for the surviving
children at 2 and 5 years of age have been reported before.6,13
Cranial ultrasound was performed as soon as
possible after admission to the neonatal intensive care unit. Further examinations were performed at least twice in the first week of life and
weekly thereafter until discharge.2 Each hemorrhage was graded according to its maximal size
during the first 2 weeks of life. The grading as
described by Papile and coworkers was used:
grade I, subependymal hemorrhage; grade II,
intraventricular hemorrhage; grade III, intraventricular hemorrhage with ventricular distension; grade IV, parenchymal hemorrhage.15
Three infants in whom no hemorrhage was detected had dilated lateral ventricles on follow-up
ultrasound scans and were excluded from the
study cohort because they may have had periventricular leukomalacia.6
Serum total bilirubin determinations were
done for all infants. They were initiated based
on clinical criteria and repeated based on clinical and chemical criteria. The highest observed
neonatal serum total bilirubin concentrations
were used for our analyses.16
Neurodevelopmental outcome at 5 years was
assessed during a home visit by one of three
specially trained pediatricians, who were not familiar with the medical history of the child.17,18
Validated standardized tests were used to detect
abnormalities in mental development, neurological status, vision and visual functions, hearing,
and language and speech. Definitions of normal
and abnormal findings in the various fields of
neurodevelopment have been described in detail before.18 The World Health Organization
classification of impairment, disability, and
handicap was used.19 Impairment was defined as
any loss or abnormality of psychological, physiological, or anatomical structures or functions. A
disability was defined as any restriction or lack
(resulting from an impairment) of ability to perform an activity in the manner or within the
range considered normal for a human being. A
handicap was defined as a disadvantage for a
given individual, resulting from an impairment
or a disability, that limits or prevents the fulfillment of a role that is normal (depending on age,
gender, and social and cultural factors) for that
individual. A handicap indicates the disadvantage experienced in society by an individual who
lacks orientation, physical independence, mobility, or social integration. A handicap was defined
as minor if it interfered, but not seriously, with
everyday life and did not require extensive caretaking. A handicap was defined as major if it
interfered seriously with everyday life and imposed a severe burden on the child, the caretakers, and society.
School attendance at 5 years of age. Since compulsory education starts at the age of 5 years, school
attendance (mainstream primary education or
special education) was registered at the neurodevelopmental outcome assessment.
Maternal education when the child was 5 years of age.
The highest obtained diploma or certificate was
used to categorize maternal education. A low
educational level was defined as either only primary school education or secondary school education for a maximum of 4 years; a middle
educational level was defined as a minimum of
5-6 years of secondary school education and less
than 4 years of education after the completion of
secondary school; a high level of education was
considered to be at least 4 years of education
after the completion of secondary school (including university degrees).
School performance at 9 years of age. The assessment of the school performance at 9 years of age
has been described extensively before.20 Questionnaires were sent to the parents of all children who participated in the follow-up study at 5
years of age. The questionnaire dealt with the
following items: kind of school (mainstream education or special education), grade, and need
for special assistance in school (extra help by
teacher, remedial teaching, or speech therapy).
One overall school outcome variable was created. The outcome variable divided the children
into three groups: (1) normal: children in mainstream education at the appropriate level, either
with or without special assistance; (2) slow learners: children in mainstream education one or
297
School Performance in Adolescents Born Preterm
more grades below the appropriate level for age,
either with or without special assistance; and (3)
special education: children in special education.
School performance at 14 years of age. Questionnaires regarding school performance were sent
to the adolescents. They were requested to complete the questionnaires themselves. If the adolescent was unable to complete the questionnaire, the parents were asked to do so. In the
Netherlands, after completing primary school at
the age of 12 years, pupils choose one of the
three levels of secondary school: (1) university
preparatory education (VWO), (2) senior general secondary education (HAVO), or (3) preparatory secondary vocational training (VMBO).
The school placement system aims to keep every
adolescent in mainstream education. VWO lasts
6 years, HAVO 5 years, and VMBO 4 years. Special secondary education is limited and exists of
education for adolescents with either cognitive
and behavioral, motor, sensory, or multiple
handicaps. One overall school outcome variable
was created. This variable divided the adolescents into three groups: (1) normal: adolescents
in the appropriate grade for age in one of the
three levels of mainstream secondary education;
(2) slow learners: adolescents in one of the three
levels of mainstream secondary education one
or more grades below the appropriate level for
age; and (3) special education: adolescents in
special education.
Statistical Analysis
Chi-square tests and analyses of variance were
used to study the relationship between school
performance at 14 years and various perinatal
factors (gestational age, birth weight, gender,
ethnicity, PIVH, need of assisted ventilation,
maximum serum total bilirubin concentration),
neurodevelopmental outcome data at 5 years,
and school performance at 5 and 9 years. These
tests were also used to determine the relationship between the various PIVH groups and the
above-mentioned perinatal, follow-up, and
school performance data. Logistic regression
analysis was used to estimate the risk for the
need of special education in adolescents with
PIVH in the neonatal period. The following factors were considered as confounding factors and
corrected for in the analysis: gestational age,
birth weight, small for gestational age (⬍10th
percentile), gender, ethnicity (Western European or other), days of assisted ventilation, maximum serum total bilirubin concentration, and
maternal education. A P value of ⬍0.05 was considered to be statistically significant.
Results
School performance data at the age of 14 years
were obtained from 278 (91.5%) of the 304
surviving adolescents. One hundred and twentynine (46.4%) adolescents performed normally
in school; 107 (38.5%) appeared to be slow
learners, whereas 42 (15.1%) participated in
special education. The level of secondary education in relation to school performance is presented in Table 1. When compared with slow
learners, adolescents with a normal school performance attended more frequently level A education.
No significant relationship, respectively, between gestational age, birth weight, gender, eth-
Table 1. School Type in Relation to School Performance at 14 Years of Age in Adolescents
Born Very Preterm
School Type
A. VWO
B. HAVO
C. VMBO
Cognitive/Behavioral
Motor
Sensory
Multiple
Unspecified
Normal
n ⫽ 129 (46.4%)
Slow Learner
n ⫽ 107 (38.5%)
29
35
65
5
26
76
Special Education
n ⫽ 42 (15.1%)
19
6
4
3
10
298
van de Bor and den Ouden
nicity, or mean days of assisted ventilation and
school performance at 14 years was observed
(Table 2). However, adolescents born at a gestational age of 26-27 completed weeks had a
poorer school performance than adolescents
born after ⱖ28 weeks of gestation. Less than
30% of the adolescents born at 26-27 weeks had
a normal school performance, 51.2% were slow
learners, and 19.5% needed special education,
whereas approximately 50% of the adolescents
born after a longer gestation performed normally in school. Adolescents with a PIVH in the
neonatal period participated significantly more
in special education than adolescents without
PIVH. The mean maximum serum total bilirubin concentration in the neonatal period was
significantly lower among the slow learners
when compared with the other two school performance groups.
Adolescents whose mothers had a higher level
of education (assessed when the child was 5
years of age) were more likely to be without
school problems at the age of 14 years; the difference, however, did not reach statistical significance (Table 3). From the adolescents that were
disabled or handicapped at the age of 5 years,
significantly more attended special education at
14 years of age than from those that were not
handicapped, irrespective of the neurodevelopmental domain. Special education at 14 years of
age was strongly related to the participation in
special education at 5 as well as at 9 years.
The unadjusted odds ratios for the need of
special education at 14 years of age by the various perinatal factors are presented in Table 4. It
appeared that from the perinatal factors only
the unadjusted odds ratio for PIVH was significantly associated with the need of special education (OR 2.56, 95% confidence interval 1.174.86). Maternal education was not associated
with the need of special education at 14 years
(Table 5). The presence of a disability or handicap at 5 years of age as well as the need for
special education at 5 and 9 years of age were all
highly associated with the need of special education at 14 years of age.
Since from the perinatal factors only PIVH
was significantly related to participation in special education at 14 years of age, the study population was divided into three groups according
to the presence and severity of PIVH. Table 6
shows the perinatal data in the various PIVH
groups. Adolescents with PIVH had a significantly shorter gestational age and needed assisted ventilation significantly longer than those
without PIVH. No differences between the vari-
Table 2. Perinatal Data in Relation to School Performance at 14 Years of Age
Gestational Age (wks)
26-27⫹6
28-29⫹6
30-31⫹6
Birth Weight (g)
⬍ 1000
1000-1249
1250-1499
⬎1500
Gender
Female
Male
Ethnicity (n ⫽ 274)
Western European
Other
PIVH
None
All grades
Assisted ventilation (days; mean ⫾ SD)
Bilirubin (␮Mol/L; mean ⫾ SD)
Normal
n ⫽ 129 (46.4)
Slow Learner
n ⫽ 107 (38.5)
Special Education
n ⫽ 42 (15.1)
12 (29.3)
52 (49.0)
65 (49.6)
21 (51.2)
39 (36.8)
47 (35.9)
8 (19.5)
15 (14.2)
19 (14.5)
NS
19 (35.2)
34 (45.3)
39 (47.6)
37 (55.2)
27 (50.0)
29 (38.7)
29 (35.3)
22 (32.8)
8 (14.8)
12 (16.0)
14 (17.1)
8 (11.9)
NS
64 (47.8)
65 (45.1)
52 (38.8)
55 (38.2)
18 (13.4)
24 (16.7)
NS
104 (45.0)
24 (55.8)
91 (39.4)
14 (32.6)
36 (15.6)
5 (11.6)
NS
97 (44.9)
32 (51.6)
6.8 ⫾ 8.9
190.6 ⫾ 42.0
93 (43.1)
14 (22.6)
8.3 ⫾ 10.3
177.2 ⫾ 39.1
26 (12.0)
16 (25.8)
8.8 ⫾ 10.4
196.8 ⫾ 47.6
*Chi-square test or analysis of variance where appropriate.
Percentages within each perinatal factor subgroup are shown between brackets.
P*
0.005
NS
0.01
299
School Performance in Adolescents Born Preterm
Table 3. Maternal Education, Handicaps at 5 Years, and Primary School Performance at 5 and 9 Years in
Relation to Secondary School Performance at 14 Years of Age
Maternal Education (n ⫽ 255)
Low
Middle
High
Disability or Handicap at 5 years (n ⫽ 274)
Overall
None
Disability
of which Handicap
Minor
Major
Disability†/Handicap‡
Mental
Neurological
Vision
Hearing
Language/Speech
School Performance at 5 Years (n ⫽ 250)
Mainstream
Special Education
School Performance at 9 Years (n ⫽ 248)
Normal
Slow Learner
Special Education
Normal
n ⫽ 129 (46.4)
Slow Learner
n ⫽ 107 (38.5)
Special Education
n ⫽ 42 (15.1)
49 (45.0)
35 (45.5)
41 (59.4)
46 (42.2)
33 (42.9)
18 (26.1)
14 (12.8)
9 (11.6)
10 (14.5)
115 (56.4)
12 (17.1)
4 (10.5)
1
3
80 (39.2)
27 (38.6)
9 (23.7)
7
2
9 (4.4)
31 (44.3)
25 (65.8)
12
13
2/1
4/3
-/2/5/1
6/2
1/-/1/1
18/2
20/13
10/8
2/1
4/2
24/12
0.00
0.00
0.00
0.01
0.00
121 (54.8)
-
88 (39.8)
9 (31.0)
12 (5.4)
20 (69.0)
0.00
111 (86.6)
7 (10.6)
3 (6.5)
22 (16.2)
55 (83.3)
19 (41.3)
3 (2.2)
4 (6.1)
24 (52.2)
0.00
P*
NS
0.00
*Chi-square test.
†Including handicap.
‡A child could be diagnosed as having a disability or handicap in more than one field of neurodevelopment.
Percentages within education or handicap subgroups are shown between brackets.
ous PIVH groups, respectively, in birth weight,
gender, ethnicity, and maximum serum total bilirubin concentration were observed. Table 7
shows data on maternal education and follow-up
at 5 years of age in the various PIVH groups.
Maternal education did not differ between the
PIVH groups. Major handicaps, especially neurological, were observed significantly more in
adolescents with grade III/IV PIVH. Significantly more adolescents with PIVH attended special education at 5, 9, as well as at 14 years of age,
irrespective of the severity of PIVH (Table 8).
Table 9 presents the level of secondary education in relation to school performance in the
PIVH groups. With regard to performance in
mainstream education, no striking differences
between the groups were observed.
Twenty-six adolescents of our initial cohort of
304 survivors6,13 did not return the questionnaires. Therefore, their school performance
data were not obtained. Five of them had suffered from grade I/II PIVH. They were all hand-
icapped at the age of 5 years (4 minor, 1 major),
and 3 of them were in special education at the
age of 9 years (no school performance data were
available from the other 2 at 9 years). One adolescent was diagnosed with grade III/IV PIVH.
He was so severely handicapped at the age of 5
years that he was not enrolled in any school
program. In none of the other 20 nonresponding survivors was PIVH detected. Five of them
were handicapped at the age of 5 years (4 minor
and 1 major), and at the age of 9 years, 12
performed normally in school, 4 were slow learners, and 4 needed special education.
To determine whether the need for special
education at 14 years of age in our study group
had causes other than PIVH in the neonatal
period, stepwise logistic regression analysis was
performed. Special education was used as a dependent variable and gestational age, birth
weight, small for gestational age (⬍10th percentile), gender, ethnicity, length of assisted ventilation, maximum serum total bilirubin concen-
300
van de Bor and den Ouden
Table 4. Unadjusted Odds Ratios and 95%
Confidence Intervals for the Need of Special
Education at 14 Years of Age by Perinatal Factors
Odds Ratio
Gestational Age (wks)
26-27⫹6
28-29⫹6
30-31⫹6
Birth Weight (g)
⬍ 1000
1000-1249
1250-1499
⬎1500
Gender
Male vs. Female
Ethnicity
Other vs. Western
European
PIVH
All grades
Assisted ventilation
ⱖ 15 days vs. ⬍ 15
days
Bilirubin
ⱖ 150 ␮Mol/L vs.
⬍ 150 ␮Mol/L
95% Confidence
Interval
1.43
0.97
1
0.57-3.56
0.43-1.91
1.28
1.41
1.41
1
0.45-3.68
0.54-3.68
0.55-3.64
1.24
0.63-2.41
0.57
0.19-1.70
2.56
1.17-4.86
2.04
0.94-4.43
1.62
0.82-3.22
tration, and maternal school education as
possible confounding factors. They yielded an
estimate of the odds (risk) on the need of special
education when the data were adjusted for the
confounding factors. The overall risk of the
need of special education at 14 years was higher
for adolescents with PIVH in the neonatal period when compared with those without PIVH
(OR 2.33, 95% confidence interval 1.15-4.75).
The OR for adolescents with grade I/II PIVH
was 2.10 (95% confidence interval 1.01-4.35),
whereas the OR for adolescents with grade
III/IV PIVH was 3.99 (95% confidence interval
1.36-11.69).
years of age.21 The worrisome finding that less
than 50% of this very preterm born cohort had
a normal school performance is in accordance
with the literature. Hack and coworkers recently
reported that very low birth weight survivors at
the age of 20 years had an educational disadvantage and were less likely than normal weight
controls to be enrolled in postsecondary study.22
Stjernqvist and Svenningsen reported that 38%
of surviving extremely preterm born (⬍29 weeks
of gestation) children performed at school below grade level at the age of 10 years; 8% performed far below grade level, whereas 30% performed below grade level and received special
education within the normal school system.23
This is the first study to describe the effect of
PIVH in the neonatal period on school performance in adolescents born preterm. We demonstrate that PIVH in preterm infants carries an
increased risk of poor school performance. It
has been frequently reported that the lower
grades of PIVH do not independently affect
long-term outcome.8,12 In this study, however,
we observed that the risk of needing special
education for adolescents with lower grades of
PIVH (grades I/II) increased twofold, when
compared with those without PIVH. When we
had taken into account the poor neurodevelopmental outcome at 5 years and the need for
special education at 9 years of the nonresponders with grade I/II PIVH, the risk would
have been even more pronounced.
The size of the hemorrhage may have been
rather limited in grade I/II PIVH, but the events
preceding the hemorrhage and the secondary
Table 5. Unadjusted Odds Ratios and 95%
Confidence Intervals for the Need of Special
Education at 14 Years of Age by Follow-Up Data
at 5 Years and Primary School Performance at 5
and 9 Years
Discussion
The compliance rate of our study was very high
(91.5%). The overall school performance of our
study cohort did not differ from the school performance of the remaining POPS cohort. School
performance in our study cohort, however, was
considerably poorer than in the general Dutch
population (46.4% versus 80.6% normal performers, 38.5% versus 14.7% slow learners, and
15.1% versus 4.7% in special education) at 14
Maternal Education
Low vs. middle and high
Disability or Handicap at 5
Years
Special Education at 5
Years
Special Education at 9
Years
Odds
Ratio
95%
Confidence
Interval
1.32
0.61-2.88
17.22
7.60-39.02
22.47
8.96-56.36
29.12
11.22-75.61
301
School Performance in Adolescents Born Preterm
Table 6. Perinatal Data in Adolescents With and Without PIVH in the Neonatal Period
No PIVH
n ⫽ 216 (77.7)
PIVH Grade I/II
n ⫽ 45 (16.2)
PIVH Grade III/IV
n ⫽ 17 (6.1)
P*
29.4 ⫾ 1.5
1297 ⫾ 329
28.8 ⫾ 1.5
1258 ⫾ 291
28.2 ⫾ 1.5
1192 ⫾ 251
0.00
NS
106 (79.1)
110 (76.4)
17 (12.7)
28 (19.4)
11 (8.2)
6 (4.2)
NS
179 (77.5)
33 (76.7)
6.3 ⫾ 8.6
184.6 ⫾ 42.2
38 (16.5)
7 (16.3)
10.9 ⫾ 10.7
190.5 ⫾ 46.5
14 (6.1)
3 (7.0)
15.9 ⫾ 13.7
196.8 ⫾ 29.6
NS
Gestational Age (wks; mean ⫾ SD)
Birth Weight (g; mean ⫾ SD)
Gender [n, (%)]
Female
Male
Ethnicity [n, (%)] (n ⫽ 274)
Western European
Other
Assisted Ventilation (days; mean ⫾ SD)
Bilirubin (␮Mol/L; mean ⫾ SD)
0.00
NS
*Chi-square test or analysis of variance where appropriate.
effect on corticogenesis and connectivity in the
developing brain appear to be more harmful
than previously acknowledged. Stewart and coworkers demonstrated that magnetic resonance
imaging of the brains of 14-year-old adolescents
born very preterm showed more lesions, eg, abnormalities of ventricles, corpus collosum, and
white matter, than were observed by brain ultrasound imaging in the neonatal period.24 In that
study, hemorrhages with parenchymal involvement were associated with permanent sequelae
on magnetic resonance imaging. The observed
abnormalities expressed themselves primarily in
quantitative behavioral abnormalities rather
than more conventional neurological impairments. Maalouf and coworkers detected with
magnetic resonance imaging that all preterm
infants ⬍30 weeks gestation, which had suffered
from PIVH in the first days of life, further developed cerebral abnormalities until term.25 Inder
and coworkers demonstrated that, at the term
equivalent date, preterm infants, even those
without periventricular white matter injury, have
significantly smaller volumes of cerebral cortical
gray matter than term infants.26
The quality of the ultrasound equipment that
Table 7. Maternal Education and Follow-Up Data at 5 Years of Age in Adolescents With and Without PIVH
in the Neonatal Period
Maternal Education (n ⫽ 255)
Low
Middle
High
Disability or Handicaps at 5 Years (n ⫽ 274)
Overall
None
Disability
of which Handicap
Minor
Major
Disability†/Handicap‡
Mental
Neurological
Vision
Hearing
Language/Speech
No PIVH
n ⫽ 216
PIVH Grade I/II
n ⫽ 45
PIVH Grade III/IV
n ⫽ 17
86 (43.7)
56 (28.4)
55 (27.9)
18 (41.9)
15 (34.9)
10 (23.2)
5 (33.3)
6 (40.0)
4 (26.7)
164 (77.0)
49 (23.0)
23 (10.8)
13 (6.1)
10 (4.7)
29 (64.4)
16 (35.6)
11 (24.4)
7 (15.5)
4 (8.9)
11 (68.7)
5 (31.3)
4 (25.0)
4 (25.0)
0.00
18/10
8/4
1/1
5/2
34/11
9/6
4/4
1/2/1
12/4
1/3/3
-/-/1/-
NS
0.00
NS
NS
NS
*Chi-square test.
†Including handicap.
‡A child could be diagnosed as having disability and handicap in more than one field of neurodevelopment.
Percentages within each PIVH subgroup are shown between brackets.
P*
NS
302
van de Bor and den Ouden
Table 8. School Performance at 5, 9 and 14 Years of Age in Preterm Born Adolescents With and Without
PIVH in the Neonatal Period
School Performance at 5 Years (n ⫽ 250)
Mainstream
Special Education
School Performance at 9 Years (n ⫽ 248)
Normal
Slow Learner
Special Education
School Performance at 14 Years (n ⫽ 278)
Normal
Slow Learner
Special Education
No PIVH
n ⫽ 216
PIVH Grade I/II
n ⫽ 45
PIVH Grade III/IV
n ⫽ 17
P*
178 (91.3)
17 (8.7)
31 (77.5)
9 (22.5)
12 (80.0)
3 (20.0)
0.02
107 (55.4)
57 (29.5)
29 (15.0)
22 (55.0)
5 (12.5)
13 (32.5)
7 (46.7)
4 (26.7)
4 (26.7)
0.04
97 (44.9)
93 (43.1)
26 (12.0)
25 (55.6)
10 (22.2)
10 (22.2)
7 (41.2)
4 (23.5)
6 (35.3)
0.00
*Chi-square test.
Percentages within the PIVH subgroups are shown between brackets.
was used in this study in 1983, the year in which
the study population was born, did not meet the
quality standards we apply today. Five-megahertz
transducers were still in use at that time. They
were sensitive enough to detect PIVH reliably,24
but not to diagnose parenchymal cystic lesions.
Therefore, detection of periventricular leukomalacia could not be reliably performed. We
excluded three children from our cohort because they appeared to have dilated lateral ventricles on follow-up ultrasound scans without a
detectable PIVH on the previous scans. Those
infants could very likely have had periventricular
leukomalacia.6
Despite the widely accepted policy in The
Netherlands to withdraw life support from preterm infants with a very poor neurodevelopmental prognosis, eg, infants with severe periven-
tricular hemorrhages, we still observed an
almost fourfold increased risk for the need of
special education in adolescents with grade
III/IV PIVH in the neonatal period when compared with adolescents without PIVH.
The incidence of PIVH in preterm infants
ⱖ26 weeks of gestation has decreased in most
neonatal intensive care units over the past two
decades. The occurrence of PIVH appears to be
gestational age-dependent; the shorter the gestation, the higher the risk of developing PIVH.2
Since survival rates of infants born after extremely short gestational ages (⬍26 weeks) have
increased over the past decade,27 the beneficial
effect of the reduction in PIVH for the longterm outcome may be blunted by the survival of
infants of extremely short gestation. Considering the poor school performance of adolescents
Table 9. Level of Secondary Education in Relation to School Performance at 14 Years of Age in Preterm
Born Adolescents With and Without PIVH in the Neonatal Period
No PIVH
n ⫽ 216
Level
A. VWO
B. HAVO
C. VMBO
Cognitive/behavioral
Motor
Sensory
Multiple
Unspec.
Normal
n ⫽ 97
Slow
learner
n ⫽ 93
23
25
49
5
22
66
PIVH Grade I/II
n ⫽ 45
Special
education
n ⫽ 26
11
4
2
2
7
Normal
n ⫽ 25
Slow
learner
n ⫽ 10
5
8
12
—
4
6
PIVH Grade III/IV
n ⫽ 17
Special
education
n ⫽ 10
5
—
1
1
3
Normal
n⫽7
Slow
learner
n⫽4
1
2
4
—
—
4
Special
education
n⫽6
3
2
1
—
—
School Performance in Adolescents Born Preterm
born between 26 and 32 weeks gestation, the
future academic achievement of infants born
before 26 weeks of gestation is a great concern.
Conclusion
We observed that less than 50% of adolescents
born before 32 weeks gestation have a normal
school performance. While PIVH, even the
lower grades, was related to disability at the age
of 5 years, we now demonstrate that PIVH also
has an unfavorable additional effect on school
performance.
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