Stability of Cognitive Outcome From 2 to 5 Years of Age in Very Low Birth

Weight Children
Petriina Munck, Pekka Niemi, Helena Lapinleimu, Liisa Lehtonen, Leena Haataja and
the PIPARI Study Group
Pediatrics 2012;129;503; originally published online February 27, 2012;
DOI: 10.1542/peds.2011-1566

The online version of this article, along with updated information and services, is
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ARTICLE

Stability of Cognitive Outcome From 2 to 5 Years of Age

in Very Low Birth Weight Children
AUTHORS: Petriina Munck, MA,a,b Pekka Niemi, PhD,b
Helena Lapinleimu, MD, PhD,a,c Liisa Lehtonen, MD, PhD,a,c
Leena Haataja, MD, PhD,c,d and the PIPARI Study Group
Departments of aPediatrics and dPediatric Neurology, Turku
University Hospital, Turku, Finland; and Departments of
bPsychology and cMedicine, University of Turku, Turku, Finland
KEY WORDS
intelligent quotient, Mental Development Index, very preterm
ABBREVIATIONS
BSID-IIBayley Scales of Infant Development, Second Edition
FSIQfull-scale IQ
MDIMental Development Index
VLBWvery low birth weight
WPPSI-RWechsler Preschool and Primary Scale of Intelligence
Revised
Ms Munck contributed substantially in designing the study,
acquisition of data, data analysis, drafting the article, and in the
nal approval of the version to be submitted; and Drs Niemi,
Lapinleimu, Lehtonen, and Haataja contributed substantially in
designing the study, revising the content of the draft critically,
and in the nal approval of the version to be submitted.
www.pediatrics.org/cgi/doi/10.1542/peds.2011-1566
doi:10.1542/peds.2011-1566
Accepted for publication Nov 11, 2011
Address correspondence to Petriina Munck, MA, Department of
Pediatrics, Turku University Hospital, Kiinamyllynkatu 4-8, 20520
Turku, Finland. E-mail: petmun@utu.
PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).
Copyright 2012 by the American Academy of Pediatrics
FINANCIAL DISCLOSURE: The authors have indicated they have
no nancial relationships relevant to this article to disclose.
FUNDING: This work was supported by grants from Sundells
Stiftelse, The Finnish Cultural Foundation, The Eemil Aaltonen
Foundation, and the Foundation for Paediatric Research/SouthWestern Finnish Fund of Neonatal Research.

WHATS KNOWN ON THIS SUBJECT: Very preterm children are at

risk for developmental problems and, therefore, a systematic
follow-up is important. However, the relevance of early follow-up
of cognitive development has been questioned because of the
divergent data on the prognostic value of early measures.
WHAT THIS STUDY ADDS: Good stability of cognitive development
was found between the ages of 2 and 5 years. Well-conducted
assessment of cognitive development in infancy is both reliable to
anticipate later development and clinically valuable to identify
those children who need developmental support.

abstract
OBJECTIVE: This study assessed the stability of cognitive outcomes of
premature, very low birth weight (VLBW; #1500 g) children.
METHODS: A regional cohort of 120 VLBW children born between 2001
and 2004 was followed up by using the Bayley Scales of Infant Development, Second Edition, at 2 years of corrected age and the Wechsler
Preschool and Primary Scale of IntelligenceRevised at the age of 5
years. The Mental Development Index (MDI) and the full-scale IQ (FSIQ)
were measured, respectively. A total of 168 randomly selected healthy
term control children born in the same hospital were assessed for
MDI and FSIQ.
RESULTS: In the VLBW group, mean 6 SD MDI was 101.2 6 16.3 (range:
50128), mean FSIQ was 99.3 6 17.7 (range: 39132), and the correlation between MDI and FSIQ was 0.563 (P , .0001). In the term group,
mean MDI was 109.8 6 11.7 (range: 54128), mean FSIQ was 111.7 6
14.5 (range: 73150), and the correlation between MDI and FSIQ was
0.400 (P , .0001). Overall, 83% of those VLBW children who had
signicant delay (2 SD or less) according to MDI had it also in FSIQ.
Similarly, 87% of those children who were in the average range in MDI
were within the average range in FSIQ as well.
CONCLUSIONS: Good stability of cognitive development over time was
found in VLBW children and in term children between the ages of 2
and 5 years. This conclusion stresses the value and clinical signicance of early assessment at 2 years of corrected age. However, we
also emphasize the importance of a long-term follow-up covering a
detailed neuropsychological prole of these at-risk children. Pediatrics
2012;129:503508

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503

Very preterm birth has been shown to

relate strongly with cognitive impairments through childhood.18 However,
a positive trend for improvement in
cognitive development has been reported,911 but follow-up data of these
promising ndings are not yet available.
Because very preterm children are at
risk for developmental problems, many
hospitals have follow-up programs that
include assessment of cognitive abilities. However, timing of the follow-up,
the length of the follow-up period, and
the applied methods vary between
countries and centers, thus making
international comparisons difcult. The
relevance of early cognitive measures
(usually at 2 years of corrected age)
for prediction of long-term outcome
has been questioned because of divergent data on their prognostic value.
Some longitudinal studies have shown
that early measures give too pessimistic a view of the long-term cognitive
outcome, and it has been suggested
that preterm children would gradually
close the gap to their term peers, at
least to some degree.12,13 It has also
been suggested that the number of
preterm children without any early
cognitive decits would decrease over
the years and at the same time, the
number of children having early moderate to severe disabilities would diminish,
both of which would increase the number of children with minor problems.14
Conversely, good stability of the scores
measuring cognitive development over
time has been reported.1518
In the current study population, a good
cognitive outcome was found at the age
of 2 years.11 The aims of the current
study were: (1) to study the clinical
signicance of the assessment conducted at the age of 2 years by studying
the stability of cognitive development in
a regional very low birth weight (VLBW)
cohort between the ages of 2 and 5
years; and (2) to compare the stability
with term controls. Our hypothesis was
504

that a well-conducted assessment of

cognitive development at the corrected
age of 2 years would show good correlation with assessment at the age of
5 years.

METHODS
Participants
This study is a part of a multidisciplinary follow-up study, PIPARI (Development and Functioning of Very Low Birth
Weight Infants from Infancy to School
Age). All VLBW (#1500 g and preterm)
infants born at Turku University Hospital in the period between 2001 and
2006 and living in the catchment area
were eligible. The current study sample
consisted of infants born to families
speaking either Finnish and/or Swedish
(the ofcial languages of Finland) between 2001 and 2004. Infants with severe
congenital anomalies or a diagnosed
syndrome affecting their development
were excluded.
A total of 199 healthy term infants born
at the same hospital between 2001 and
2003 were recruited to the control
group. Term infants were born at or
above 37 gestational weeks into Finnish
and/or Swedish-speaking families and
were not admitted to a NICU during their
rst week of life. The exclusion criteria
werecongenitalanomaliesorsyndromes,
mothers self-reported use of illicit drugs
or alcohol during the pregnancy, and
birth weight 2.0 SD or less (small for
gestational age) according to age and
gender-specic Finnish growth charts.
The research psychologist (Ms Munck)
recruited the term group by asking the
parents of the rst boy and the rst girl
born in each week to participate. At refusal, the parents of the next boy/girl of
the week were approached.
The ethics review committee of the
Hospital District of the South-West
Finland approved the PIPARI study protocol in December 2000. All parents
who agreed to participate gave written

informed consent after written and oral

information was provided.
Assessment of Cognitive
Development
Bayley Scales of Infant Development,
Second Edition
At 2 years of corrected age (from 1
week to 1 month), cognitive development was assessed by using Finnish
translation11 of the Mental Development
Index (MDI) of the Bayley Scales of Infant
Development, Second Edition (BSID-II).19
MDI was used both as a continuous
variable (mean 6 SD: 100 6 15) and as
a categorized variable. A signicant delay was dened as an MDI ,70 (2 SD or
less) and a mild delay as 70 to 84 (2 SD
, MDI , 1 SD). MDI $85 (1 SD or
more) was considered average.
Wechsler Preschool and Primary
Scale of IntelligenceRevised
At the age of 5 years (from 1 week to 2
months), cognitive development was
assessed with the short version of
Wechsler Preschool and Primary Scale
of IntelligenceRevised (WPPSI-R), Finnish
translation (1995).20 Three verbal (information, sentences, and arithmetic) and 3 performance (block design,
geometric design, and picture completion) subscales were selected based on
the strongest correlation with the fullscale IQ (FSIQ). FSIQ was used both as
a continuous variable (mean: 100 6 15)
and as a categorized variable. A signicant delay was dened as FSIQ ,70 (2
SD or less) and a mild delay as 70 to 84
(2 SD , FSIQ , 1 SD). FSIQ $85 (1
SD or more) was considered average.
The psychologist who assessed the
children at the age of 5 years was blinded to childrens perinatal history and
to MDI status to avoid the bias of information of the previous assessment.
Statistical Analysis
Statistical analyses were conducted by
using SAS version 9.2 (SAS Institute, Inc,

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ARTICLE

Cary, NC). The association between MDI

and FSIQ was studied by using Pearsons
correlation. Independent sample t tests
were used when continuous MDI and
FSIQ values were compared between
VLBW and term children. Cohens
weighted k was calculated to estimate
the agreement between of categorized
MDI and categorized FSIQ. Receiver operating characteristic curve analysis was
performed to study the sensitivity and
specicity of MDI on categorized FSIQ.
MDI was used as a continuous variable and FSIQ as a categorized variable
(signicant delay and mild/signicant
delay).

RESULTS
Characteristics
A total of 184 VLBW infants were born in
the period between 2001 and 2004. Of
these, 28 (15%) died during the neonatal period. Finnish and/or Swedish
were not the only languages of the
families of 15 infants (10%). One infant
was excluded because of multiple
anomalies. The families of 4 of the 140
eligible infants (3%) refused to participate or were withdrawn from the study.
A total of 136 VLBW infants were
assessed at the corrected age of 2
years. Of these, 124 children (91%) were
also assessed at the age of 5 years. Four
of these children were too severely
handicapped to be assessed. However,
they were included in the analysis of the
categorized data and were classied as
having a signicant cognitive delay at
the age of 5 years. Families of 8 term
infants (4%) refused to participate in
the follow-up at the age of 2 years. Of the
remaining 191 children, 168 (88%) were
also assessed at the age of 5 years. The
characteristics of the children and
parents, along with the neonatal data of
VLBW infants, are shown in Table 1.
Cognitive Development
In the VLBW group, mean 6 SD MDI
was 101.2 6 16.3 (range: 50128), mean

TABLE 1 Infant Characteristics of VLBW and Term Children and the Length of Parental Education
Variable

VLBW (n = 124)

Term (n = 168)

Prenatal corticosteroids
Multiple birth
Birth weight (g)
Mean (SD) [min, max]
Gestational age (weeks)
Mean (SD) [min, max]
Small for gestational agea
Male
Apgar ,6 at 5 min
Days on ventilator
Mean 6 SD [min, max]
Postnatal steroids
Chronic lung diseasec
Ductal ligation
Sepsis or meningitis
Intestinal perforation (NEC included)
Retinopathy of prematurity $grade III
Hydrocephalus with a shunt
Days in hospital, mean 6 SD [min, max]
Maternal educationd
9y
.912 y
.12 y
Paternal educatione
9y
.912 y
.12 y

117 (94)
38 (31)

1 (1)

1061 (260) [400, 1500]

3659 (454) [2570, 4980]

28.7 (2.8) [23.3, 35.9]

49 (40)
67 (54)
28 (23)b

40.1 (1.2) [37.1, 42.3]

0
81 (48)
0

9.4 (12.7) [0, 50]

21 (17)
19 (15)
17 (14)
30 (24)
7 (6)
3 (2)
4 (3)
59.6 (32.8) [3, 183]

14 (11)
36 (29)
123 (59)

6 (4)
53 (36)
89 (60)

12 (10)
69 (56)
42 (34)

15 (11)
59 (41)
69 (48)

Data are presented as frequency (percentage) if not otherwise indicated. min, minimum; max, maximum; NEC, necrotizing
enterocolitis. , indicates that treatments, morbidities, and operations were valid only for the VLBW data.
a Dened as a birth weight of 2.0 SD or less, according to the age- and gender-specic Finnish growth charts.
b Missing, n = 2.
c Dened as a need for supplemental oxygen at the age of 36 gestational weeks.
d Missing 1 patient and 20 patients, respectively, from each group.
e Missing 1 patient and 25 patients, respectively, from each group.

FSIQ was 99.3 6 17.7 (range: 39132),

and the correlation between MDI and
FSIQ was 0.563 (P , .0001). In the term
group, mean MDI was 109.8 6 11.7
(range: 54128), mean FSIQ was 111.7
6 14.5 (range: 73150), and the correlation between MDI and FSIQ was
0.400 (P , .0001). VLBW children had
lower mean MDI and FSIQ (both comparisons: P , .001) compared with
term controls.
MDI and FSIQ were studied as categorized variables, and the stability of the
developmental category was calculated
between the 2 time-points. Four VLBW
children who were too severely handicapped to be assessed at the age of
5 years were added to the signicant
delay group. A total of 83% of the children
with signicant delay in MDI (n = 6) also
had signicant delay in FSIQ. Similarly,

87% of the children in the average range

in MDI (n = 113) were within the average
range also in FSIQ. Children with mild
developmental delay at the age of 2
years (n = 5) were distributed in all
groups at the age of 5 years. Cohens k
was 0.61, showing a substantial agreement of stability. Data are presented in
Table 2. Receiver operating characteristic curve analysis reveals a sensitivity
and specicity of MDI on signicant delay (Fig 1) and mild delay (Fig 2).
There were no term children with signicant developmental delay at either
age point. Of the term children within
the average range at the age of 2 years
(n = 164), 97% were within the average
range also at the age of 5 years. Of
those 4 term children who had mild
delay at the age of 2 years, 3 had improved in their development and only

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505

TABLE 2 VLBW Children and Term Children With a Signicant Delay (,70), Mild Delay (7084),
and Cognitive Development Within the Average Range ($85) on the Basis of MDI Scores
Study Group
VLBW
MDI ,70
MDI 7084
MDI $85
Total
Term
MDI ,70
MDI 70-84
MDI $85
Total

FSIQ ,70

FSIQ 7084

FSIQ $85

Total

5 (83)
2 (40)
2 (2)
9

1 (17)
1 (20)
13 (11)
15

0
2 (40)
98 (87)
100

6
5
113
124

0
0
0
0

0
1 (25)
5 (3)
15

0
3 (75)
159 (97)
100

0
4
164
168

Data are presented as number and (percentage). Four VLBW children who were too severely handicapped to be assessed at
the age of 5 years were added to the group of signicant delay. Cohens k was 0.61 for the VLBW population, showing
a substantial agreement of stability, and 0.18 for the term population, showing a slight agreement of stability.

FIGURE 1
Receiver operating characteristic curve analysis of the sensitivity and specicity of MDI on severe delay in
FSIQ.

1 child remained in the mild delay

group. Cohens k was 0.18, showing
a slight agreement of stability. Data are
presented in Table 2.

DISCUSSION
Opinions regarding the stability of early
measures of cognitive outcome have
varied largely, suggesting that there is
a poor predictive validity to later assessments12,13 and that early measures
can predict the later cognitive outcome
quite reliably.1518 In the current study,
a strong correlation was found between
MDI measured at 2 years of age and
FSIQ measured at the age of 5 years,
506

suggesting that early assessment of

cognitive development is signicantly
associated with cognitive development
at least up to the age of 5 years. The
stability of the classication of cognitive outcome was high in normally developing and in signicantly delayed
groups. This nding implies that early
assessment of cognitive development
is clinically important. Children with signicant developmental problems should
be addressed to appropriate diagnostic, etiologic, and rehabilitation services
as early as possible in their development. Conversely, parents of children
with milder problems should also be

provided with counseling to support

their childs possible specic needs.
Cognitive development of the current
study population has been shown to be
relatively good, as the mean value of MDI
has been at the level of BSID-II norms at
the age of 2 years.11 Our study conrmed this developmental pattern because VLBW children performed at the
level of WPPSI-R norms. Despite this
nding, the difference to control group
was almost 1 SD also at the age of 5
years. Our control group was, however,
selected because it included only
healthy-born infants excluding all preterm and small for gestational age
infants, those requiring NICU admission
for any reason, and those who were
exposed antenatally to alcohol or illicit
drugs. In addition, the average education level in Finnish society is high, free
health care is provided to all, and the
variation in socioeconomic background
is smaller than in many other countries.
Therefore, these ndings may not be
directly generalized to other populations. Importantly, however, the socioeconomic background factors (level of
parental education, which correlates
strongly with socioeconomic status)
did not differ between VLBW and term
infants, which served to differentiate
the VLBW population in the current
study from those of many other countries. This condition makes it possible
to study the impact of prematurity
without the confounding effects of socioeconomic factors.
Children did not take part in any
structured intervention program in this
study. However, all of the infants who
had a signicant motor delay received
physiotherapy. If there were any concerns about the development or the
behavior of the child either at the age
of 2 or 5 years, he or she was referred
to appropriate local rehabilitation services. In Finland, most children enter the
communal day care system. This system provides appropriate support for

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ARTICLE

more specic neuropsychological problems. Therefore, other methods are also

needed to complement follow-up of
at-risk preterm children. Long-term
follow-up is needed to identify specic
problems that may become evident only
later in the development. However, it is
important to offer families with as
accurate information as it is possible
to gain at the childs different developmental stages.

CONCLUSIONS

FIGURE 2
Receiver operating characteristic curve analysis of the sensitivity and specicity of MDI on severe and
mild delay in FSIQ.

all children with developmental or

behavioral concerns, and no IQ discrepancy is required for inclusion.
Trained nursery school teachers support their development in daily play
situations.
The strengths of this study include high
coverage of the VLBW children with a
long follow-up period. Standardized
methods were used for follow-up, and
a regional control group was used in
addition to the normative data of the
BSID-II and WPPSI-R. Different psychologists conducted the assessment in 2
different time-points to avoid the bias of
the previous assessment. Strong correlation was found despite the fact that
different methods had to be used to
measure cognitive development at different age point, as both methods cover
only limited age-span. However, both
methods provide information about the
individual development compared with
age-appropriate normative data, and
they use the same scaling. An additional
strength was that all children participated in the assessment within a very
stricttimelimit.Timingoftheassessment
was chosen to be both developmentally
and clinically relevant. From the developmental point of view, 2 years is an

interesting time window as motor development is less dominant and language development is in a very active
phase. Clinically, it is important to
identify those children who have developmental problems as early and
as accurately as possible to provide
them with appropriate services. Five
years is a more reliable age of assessment considering the later academic
performance at school age, but there
is still time for preventive interventions
if child is at risk for academic failure.
Study limitations include that the BSID-II
and WPPSI-R were used instead of the
new versions (the Bayley Scales of Infant and Toddler Development, Third
Edition, and the third edition of the
WPPSI), as these tests were not available in Finland at the time of the study.
It is also important to stress that measures of cognitive development, such
as used here, do not allow inferences
about neuropsychological decits that
can be found with more specic measures or that may become evident only
later in the childs development. Low
cognitive capacity is usually accompanied with neuropsychological difculties, but average cognition does
not imply that one would be free from

The current study revealed that the

cognitive outcome of a regional VLBW
cohort measured at the age of 2 years
was signicantly associated with cognitive outcome at the age of 5 years. We
suggest that a well-conducted assessment is relevant and valuable also at the
early age, making it possible to support
those children with developmental
problems. However, at the same time,
we stress the importance to followup these at-risk children longitudinally and with methods covering both
cognitive and neuropsychological development.

ACKNOWLEDGMENTS
The PIPARI Study Group includes: Satu
Ekblad, RN; Mikael Ekblad, medical student; Eeva Ekholm, MD, PhD; Leena
Haataja, MD, PhD; Mira Huhtala, MD;
Pentti Kero, MD, PhD; Riikka Korja, PhD;
Harry Kujari, MD; Helena Lapinleimu
MD, PhD; Liisa Lehtonen, MD, PhD; Marika
Leppnen, MD; Annika Lind, PhD; Hanna
Manninen, MD; Jaakko Matomki, MSc;
Jonna Maunu, MD, PhD; Petriina Munck,
MA; Pekka Niemi, PhD; Pertti Palo, MD,
PhD; Riitta Parkkola, MD, PhD; Jorma
Piha, MD, PhD; Liisi Rautava, MD, PhD;
Pivi Rautava, MD, PhD; Milla Ylijoki,
MD, PhD; Hellevi Rikalainen, MD, PhD;
Katriina Saarinen, Physiotherapist; Elina
Savonlahti, MD; Matti Sillanp, MD, PhD;
Suvi Stolt, PhD; Pivi Tuomikoski-Koiranen,
RN; Anniina Vliaho, MA; and Tuula
rimaa, MD, PhD.

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Stability of Cognitive Outcome From 2 to 5 Years of Age in Very Low Birth

Weight Children
Petriina Munck, Pekka Niemi, Helena Lapinleimu, Liisa Lehtonen, Leena Haataja and
the PIPARI Study Group
Pediatrics 2012;129;503; originally published online February 27, 2012;
DOI: 10.1542/peds.2011-1566
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