Early Human Development 103 (2016) 183187

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Early Human Development

journal homepage: www.elsevier.com/locate/earlhumdev

Growth in very preterm children: Head growth after discharge is the best
independent predictor for cognitive outcome
Karen Lidzba, PhD a,, Susanne Rodemann, M.D. a, Rangmar Goelz, M.D. b,
Ingeborg Krgeloh-Mann, M.D., PhD a, Andrea Bevot, M.D. a
a
University Children's Hospital Tbingen, Department of Pediatric Neurology and Developmental Medicine, Hoppe-Seyler-Str. 1, 72076 Tbingen, Germany
b
University Children's Hospital Tbingen, Department of Neonatology, Calwerstr. 7, 72076 Tbingen, Germany

a r t i c l e i n f o a b s t r a c t

Article history: Background: The contribution of growth parameters to the cognitive outcome of very low birth weight (VLBW)/
Received 15 August 2016 very preterm (VP) infants is difcult to disentangle from other preterm-birth related factors.
Accepted 27 September 2016 Aims: We hypothesized that long-term cognitive and motor outcome of VLBW/VP infants is most strongly asso-
Available online xxxx ciated with growth in head circumference after hospital discharge.
Study design: Single-centre prospective longitudinal study: anthropometric measures at different time points
Keywords:
(birth, discharge, school-age).
Preterm infants
Child development
Subjects: 136 VLBW/VP infants (b 32 weeks gestation/birth weight b 1.500 g).
Head growth Outcome measures: Cognitive and motor function (Kaufman Assessment Battery for Children; Movement Assess-
Cognitive development ment Battery for Children) at school-age (6.710.0 years, mean = 8.2).
Results: In hierarchical multiple regression analyses, growth from birth to discharge signicantly predicted cog-
nitive outcome (weight: R2change = 0.063, p = 0.014; length: R2change = 0.078, p = 0.007; HC: R2change = 0.050,
p = 0.030), as well as weight gain (R2change = 0.096, p = 0.001) and head growth (R2change = 0.134, p b 0.001)
from discharge to school-age. While most growth parameters, especially those from birth to discharge, were sig-
nicantly inuenced by prenatal growth and immaturity related morbidity (R2 = 0.151 to 0.605, all p 0.001),
head growth after discharge was not (R2 = 0.029, p = 0.461).
Conclusions: Amongst all anthropometric measures, head growth between discharge and school-age is the best
independent predictor for cognitive outcome in VLBW/VP infants. Determinants of head growth after discharge
need further studies to identify targets for intervention.
2016 Published by Elsevier Ireland Ltd.

1. Introduction to be at risk for impaired growth during hospitalization [2], childhood

1.1. Growth in preterm infants
Very or extremely low birth weight preterm infants (VLBW; ELBW)
are at risk for impaired physical growth: Up to 40% are born small for
gestational age (SGA) when compared to foetuses in utero [1], indicat-
ing sub-optimal nutritional supply already prenatally. They continue
[3], and adolescence [4]. Preterm infants born SGA demonstrated de-
layed cognitive development into the preschool [5,6] and early school
years [7], especially if SGA birth was followed by postnatal failure to
thrive [8]. Across the group of preterm infants, early postnatal growth
(i.e., during hospitalization) has been associated with neurological and
cognitive outcome in infancy and preschool-age [912].
1.2. Growth and cognitive development

Abbreviations: BPD, bronchopulmonary dysplasia; CP, cerebral palsy; ELBW,
extremely low birth weight; HC, head circumference; ICH, intracranial haemorrhage; K-
ABC, Kaufmann Assessment Battery for Children; M-ABC, Movement Assessment Battery
for Children; MPC, Mental Processing Composite; SDS, standard deviation score; SGA,
small for gestational age; TIS, total impairment score; VP, very preterm; VLBW, very low
birth weight.
Corresponding author.
E-mail addresses: karen.lidzba@med.uni-tuebingen.de (K. Lidzba),
susanne.rodemann@freenet.de (S. Rodemann), rangmar.goelz@med.uni-tuebingen.de
(R. Goelz), ingeborg.kraegeloh-mann@med.uni-tuebingen.de (I. Krgeloh-Mann),
andrea.bevot@med.uni-tuebingen.de (A. Bevot).
Amongst the parameters of physical growth, i.e., weight, length, and
head circumference (HC), HC seems to be the principal determinant of
cognitive and, less consistently, motor development [13,14]. Catch-up
growth during the rst post-term months of life [1517] and during
childhood [18] was positively correlated with later cognitive develop-
ment. Recent publications report that antenatal head growth in pre-
term-born infants was only little related to preschool cognitive
performance, while a positive association has been shown for head
growth between birth and two years [19], and between birth and ve

http://dx.doi.org/10.1016/j.earlhumdev.2016.09.016
0378-3782/ 2016 Published by Elsevier Ireland Ltd.
184 K. Lidzba et al. / Early Human Development 103 (2016) 183187
years of age [20]. This suggests that head growth beyond discharge from
the neonatal unit may play a decisive role for cognitive development.
1.3. Factors inuencing growth in preterm infants
The growth of preterm infants is inuenced by a complex conglom-
erate of interrelated factors, mainly immaturity, morbidity, and nutri-
tion [2,14,21,22]. Both immaturity and morbidity, however, are widely
accepted to also determine the preterm infant's developmental out-
come [2325]. Impairment in postnatal growth and in cognitive devel-
opment could, therefore, be the effect of the same causal variables,
namely, immaturity at birth and/or neonatal morbidity. The preterm
infant's nutrition has received much interest and the introduction of
special preterm formulas has signicantly improved preterm infants'
early weight gain [22] and cognitive outcome [26]. Currently, there is
an ongoing endeavour to further optimize preterm nutrition by setting
standards for individualized nutritional care [27]. While there is evi-
dence that increased nutrition during hospital stay may increase the
likelihood of survival without neurodevelopmental impairment, the di-
rect relationship between early nutrition and neurodevelopmental out-
come remains elusive [28]. Disentangling the unique contribution of
growth during different phases from the effects of immaturity and mor-
bidity could help to better identify targets for nutritional intervention.
1.4. Study scope and hypotheses
The aim of our study was to investigate the relationship between
growth and cognitive/motor development at early school-age. We pos-
tulated that (H1) growth, and more specically, head growth after dis-
charge has more inuence on cognitive and motor development until
early school-age than anthropometric measures at birth or growth dur-
ing hospital stay. Beyond that, we hypothesized that (H2) growth dur-
ing hospital stay is largely determined by anthropometric measures at
birth, immaturity and morbidity.
2. Patients and methods
2.1. Patients
All 141 participants took part in a prospective follow-up study
aiming to investigate the relationship between growth and cognitive
and motor development in a cohort of very preterm (VP)/very low
birth weight (VLBW) infants (b32 weeks gestation or b 1.500 g) born
between 07/01/1995 and 12/07/1997, treated in one neonatal intensive
care unit of a tertiary centre (University Children's Hospital, Tbingen,
Germany). At school-age follow-up, the children were between 6.7
and 10.0 years old (mean [SD] = 8.23 [0.74] years).
2.2. Anthropometry
Anthropometric data (body length, weight, and HC) were measured
at birth, on the day of discharge and on the day of follow-up examina-
tion, using suitable equipment for infants or children [29]. The largest
possible (fronto-occipital) circumference was measured with a exible,
but not extensible tape (measuring error 0.30.4 cm) [29,30]. The an-
thropometric measurements were expressed in standard deviation
scores (SDS) = (subject parameter reference mean) / (reference
standard deviation). At birth and discharge, the references of Niklasson
[31] were used, adapting the data to gestational age until 42 weeks. At
school-age, the Swiss standard charts by Prader [32] were used as refer-
ences, since they best reect the regional population.
Catch-up growth from birth to discharge (SDSD-B) was dened as
difference between age-standardized measures at discharge (SDSD)
and age-standardized measures at birth (SDSB). Catch-up growth from
discharge to school-age (SDSS-D) was dened as difference between
standardized measures at school-age (SDSS) and at discharge.
2.3. Neurological examination and assessment of neuromotor function
Neurological status at follow-up was classied as abnormal when
cerebral palsy (CP; denition according to Surveillance of Cerebral
Palsy in Europe [33]) was present. Children with CP were excluded.
Neuromotor function was assessed with the Movement Assessment
Battery for Children (M-ABC) [34]. This test comprises eight tasks mea-
suring manual dexterity, ball skills, and balance. Raw scores range from
zero to ve, zero indicating no impairment. The sum of all scores consti-
tutes the total impairment score (TIS).
2.4. Assessment of cognitive function
Cognitive function was assessed with the Kaufmann Assessment
Battery for Children (K-ABC) [35]. This test battery assesses cognitive
functioning in children aged 3 to 12 years. The Mental Processing Com-
posite Score (MPC) is calculated from the simultaneous processing scale
(visuo-spatial and logical abilities) and the sequential processing scale
(measuring auditory and visual short term memory and attention).
2.5. Socio-economic status and parental education
Maternal education is considered the strongest socio-economic pre-
dictor for intelligence in children born preterm [36]. Thus, we extracted
the data on maternal education from a standardized questionnaire on
parental education and socio-economic status (Hoffmeyer-Zlotnik-
Index [37]). Maternal education is expressed in an ordinal scale on edu-
cation and professional qualication ranging from one (lowest) to eight
(highest).
2.6. Statistical analysis
To test hypothesis H1, we conducted three sets of independent hier-
archical multiple regression analyses for weight, length, and HC. To re-
duce collinearity within the model, the multiple confounding factors
related to preterm birth (gestational age, bronchopulmonary dysplasia
(BPD; yes/no), days of ventilation, postnatal corticosteroids (yes/no),
intracranial haemorrhage (ICH; grade IIV), sepsis (yes/no)) were rst
subjected to a principal axis factor analysis with varimax-rotation,
resulting in one factor (immaturity: gestational age, days of ventila-
tion, corticosteroids, BPD). Standardized factor scores (large scores im-
plicating high degree of immaturity) were calculated with the
Anderson-Rubin-Method. Since neither ICH nor sepsis correlated with
the other variables, they were retained as independent predictors. Anal-
yses were conducted with K-ABC MPC or M-ABC TIS as dependent var-
iables, and potential confounding factors (maternal education,
immaturity, ICH, sepsis), anthropometric data at birth (SDSB), growth
between birth and discharge (SDSD-B), and growth between discharge
and school-age (SDSS) as predictors introduced in a hierarchical man-
ner. To test hypothesis H2, we conducted independent simultaneous re-
gression analyses with immaturity, ICH, and sepsis as predictors, and
growth data (SDSD-B; SDSS-D) as outcome.
2.7. Ethics
The internal review board of University Tbingen's Medical Faculty
approved of the study. Informed consent was obtained from the par-
ents, and children assented to the procedures performed at school-age.
3. Results
Table 1 lists the cohort's demographic, pregnancy-/birth-related and
neonatal characteristics. In the neurological examination, 130 (92%) of
the children were rated as normal, six as clumsy (4%), and ve (4%)
were excluded from further analyses due to CP.
 K. Lidzba et al. / Early Human Development 103 (2016) 183187 185

Table 1 3.1. Missing data

Demographic, pregnancy-/birth-related, and neonatal characteristics of the cohort.

Characteristic Preterm Not all datasets were complete due to missing parent questionnaires
cohort or skipped follow-up assessments (missing data: maternal education
(n = 136) n = 37; K-ABC n = 25; M-ABC n = 18; SDSD [weight] n = 10; SDSD
Male, n (%) 73 (54) [length] n = 12; SDSD [HC] n = 13; SDSB [length] n = 6; SDSS [HC]
Multiplets, n (%) 35 (26) n = 2; all perinatal data n = 1). Groups with missing vs. complete
Maternal education, n (%), HZIa
data were comparable with respect to most indicator variables. Children
12 4 (4)
34 39 (39) with missing vs. available data on length and weight at discharge had
56 34 (25) signicantly lower gestational age (SDSD [weight]: 27.44 vs. 29.30
78 22 (16) weeks, p = 0.013; SDSD [length]: 27.85 vs. 29.29 weeks, p = 0.031).
Antenatal corticosteroids, n (%) 90 (66) Children with missing vs. available K-ABC data were signicantly lighter
Antenatal corticosteroid treatment, mean (SD), cyclesb 1.01 (1.09)
Gestational age, mean (SD), weeks 29.2 (2.6)
at birth (mean weight SDSB = 0.980 vs. 0.414, p = 0.049). Children
SGA, n (%)c 42 (30) with missing vs. complete data on maternal education scored signi-
ICH, n (%)d cantly lower in K-ABC (mean MPC = 85.35 vs. 94.08, p = 0.034).
Grade I 6 (4)
Grade II 5 (4)
3.2. Predictive strength of antenatal, early postnatal, and discharge-to-
Grade III 2 (2)
Grade IV 3 (2) school-age growth
Birth weight, mean (SD), g 1149 (360)
Birth weight, mean (SD), SDS Niklasson 0.50 (1.01) Full datasets containing K-ABC data were available for 80 (length)
Birth length, mean (SD), SDS Niklassone 0.19 (1,77) and 83 (weight, HC) children. Table 2 contains the details of the three
Birth orbitofrontal head circumference, mean (SD), SDS 0.36 (1.39)
independent regression analyses with weight, length, and HC data as
Niklassond
Mean parental height, mean (SD) SDSf 0.04 (0.81) predictors. None of the analyses was biased by positive or negative in-
Need for ventilation, n (%)d 121 (90) tercorrelations (Durbin-Watson test: dweight = 2.003; dlength = 1.780;
Ventilation, mean (SD), days 28.3 (21.0) dHC = 1.861; dL80,6 = 1.338, dU80,6 = 1.653; dU b d b 4-dU for all pa-
BPD, n (%)d, g 7 (5)
rameters [38]). As expected, the rst set of regression analyses demon-
Postnatal corticosteroids, n (%)d 29 (22)
Postnatal corticosteroids, mean (SD), daysh 16.4 (16.0) strated that the predictor set of possible confounding factors accounted
Surgery within rst six weeks of life, n (%)d 4 (3) for a signicant amount of variance (18%) in the K-ABC MPC at school-
Sepsis, n (%)d, i 15 (11) age. The anthropometric data at birth did not add signicant predictive
HZI = maternal education from Hoffmeyer-Zlotnik Index. value. Instead, growth in weight, length, and HC from birth to discharge
a
Data available for 99 infants. explained additional 48% of the variance. Finally, post-discharge
b
One cycle are 2 injections of 12 mg betamethasone in 24 h (repeated after 10 days if growth in weight and HC, but not in length, explained a signicant
needed).
c amount of additional variance (weight: 10%, HC: 13%).
Birth weight b 10th percentile.
d
Data available for 135 infants. Full datasets containing M-ABC data were available for 78 (length)
e
Data available for 130 infants. to 82 (weight) children. Table 2 (lower part) contains the details of
f
Data available for 133 infants. the three independent regression analyses with weight, length, and
g
Oxygen requirement N21% after 36 weeks of gestational age. HC data as predictors. None of the analyses was biased by positive or
h
Initial dosage of dexamethasone 5 mg/kg/day for 3 days, dosage reductions every
2 days until 0.1 mg/kg/day [38].
negative intercorrelations (Durbin-Watson test: dweight = 2.017;
i
Dened as conrmed/clinical sepsis or as systemic inammatory response syndrome dlength = 2.202, dHC = 2.252; dU80,6 = 1.653; dU b d b 4-dU for all pa-
[3943]. rameters). Neither the predictor set of possible confounding factors
nor the anthropometric data at birth accounted for a signicant amount
of variance in the M-ABC TIS at school-age. Weight SDSD-B and length

Table 2
Independent hierarchical regression analyses on the predictive effects of weight, length, and head circumference data on K-ABC MPC (top) and on M-ABC TIS (bottom).

Outcome: K-ABC MPC

Predictors Weight Length Head circumference

R2 F(df) p R2change pF R2 F(df) p R2change pF R2 F(df) p R2change pF

change change change

1) Maternal education, 0.183 4.376(4,78) 0.003 0.178 4.057(4,75) 0.005 0.175 4.143(4,78) 0.004
immaturitya, ICHb, sepsisc
2) SDSB 0.187 3.547(5,77) 0.006 0.004 0.544 0.183 3.305(5,74) 0.009 0.005 0.518 0.175 3.272(5,77) 0.010 0.000 0.982
3) SDSD-B 0.250 4.227(6,76) 0.001 0.063 0.014 0.260 4.278(6,73) 0.001 0.078 0.007 0.225 3.676(6,76) 0.003 0.050 0.030
4) SDSS-D 0.346 5.666(7,75) b0.001 0.096 0.001 0.295 4.295(7,72) 0.001 0.034 0.065 0.359 6.009(7,75) b0.001 0.134 b0.001

Outcome: M-ABC TIS

Model (predictors) Weight Length Head circumference
R2 F(df) p R2change pF R2 F(df) p R2change pF R2 F(df) p R2change pF
change change change
1) Maternal education, 0.081 1.702(4,77) 0.158 0.083 1.647(4,73) 0.260 0.104 2.206(4,76) 0.170
immaturitya, ICHb, sepsisc
2) SDSB 0.081 1.347(5,76) 0.254 0.000 0.902 0.089 1410(5,72) 0.300 0.006 0.479 0.106 1.770(5,75) 0.265 0.002 0.723
3) SDSD-B 0.138 1.997(6,75) 0.077 0.056 0.030 0.158 2224(6,71) 0.044 0.069 0.018 0.121 1.695(6,74) 0.277 0.015 0.260
4) SDSS-D 0.193 2.521(7,74) 0.022 0.055 0.028 0.161 1.913(7,70) 0.074 0.002 0.659 0.158 1.951(7,73) 0.109 0.037 0.078

Signicant predictions (p b .05) are printed in bold.

a
Standardized factor score: gestational age, BPD (yes/no), ventilation (days), postnatal corticosteroids (yes/no).
b
Intracranial haemorrhage (grade IIV).
c
Sepsis (yes/no).
186 K. Lidzba et al. / Early Human Development 103 (2016) 183187

SDSD-B signicantly added to the explained variance (5.6% and 7%, re-
spectively), while HC SDSD-B did not. After discharge, only weight
growth added signicant predictive strength to the model (5.5% addi-
tional variance). Overall, the full regression models were only of moder-
ate predictive strength, explaining between 16% and 19% of the variance
in the M-ABC TIS at school-age.
3.3. Effects of anthropometric parameters at birth and preterm-birth related
morbidity on physical growth
Full datasets were available for N = 120 (weight SDSS-D; length
SDSD-B) to N = 126 (weight SDSD-B) children. Table 3 contains the sta-
tistical details of the analyses. Growth during hospital stay was ex-
plained to a signicant extent by SDS of weight, length and HC at birth
and by immaturity-related morbidity. The regression models explained
26% of variance in the growth in weight, 60% in length, and 61% in HC.
Inspection of individual regressors revealed that this effect was driven
by the respective birth SDS (more growth in children with small initial
SDS), and by the immaturity composite (less growth in the more imma-
ture children). Head growth after discharge was not explained signi-
cantly by any of the predictors. The regression models for the other
parameters explained 15% of the variance in weight gain and 18% of
growth in length. While birth SDS and immaturity contributed signi-
cantly to growth in length, only birth SDS contributed signicantly to
weight gain.
4. Discussion
4.1. The importance of growth after discharge
In our sample of VP/VLBW infants, head growth after discharge from
hospital was the strongest single predictor for school-age cognitive out-
come, explaining additional 13% of variance, after accounting for the
prominent risk factors immaturity, neonatal morbidity and maternal
education. In line with the current literature [19,20], standard scores
for weight, length, or HC at birth did not have any predictive value for
later development. In contrast to previous publications [11,39], the pre-
dictive value of our models for motor outcome was low, and only post-
discharge weight gain, but none of the other potential predictors ex-
plained a signicant amount of variance in the children's M-ABC perfor-
mance. This difference might be owed to sampling issues, especially to
the exclusion of children with CP in our study.
4.2. Growth during hospital stay: predicted by immaturity and morbidity
In line with recent publications [12], also growth during hospital
stay explained signicant portions of the variance in K-ABC scores.
Our second analysis, however, aids at putting the ndings into perspec-
tive: Prenatal growth and immaturity-related morbidity signicantly
predict growth during hospital stay, the explained variance reaching
enormous values of approximately 60% for weight and HC. Given that
critical illness exerts a strong negative impact on nutritional intake
and metabolism [40], this nding is plausible. The same predictors ex-
plain signicant, albeit smaller fractions of the variance in post-dis-
charge growth concerning length and weight, but not HC. Thus, it may
be speculated that the signicant effects of pre-discharge growth on
cognitive development are, in reality, the combined effects of immaturi-
ty-related morbidity and smallness at birth, while post-discharge head
growth is truly and independently predictive for cognitive
development.
4.3. Points of intervention
Since head circumference can be considered a proxy for brain vol-
ume [41], we suggest that the predictive value of HC growth reects
brain development more than pure growth. In consequence, the fac-
tors driving head growth in infancy and early childhood need to be fur-
ther explored in order to determine points of action for targeted
intervention. Data supporting positive effects of increased protein in-
take on head growth as compared to weight gain is still limited [22]. De-
spite increased efforts to standardize and optimize post-discharge
nutrition in VLBW infants, also the evidence for benets of post-dis-
charge formulas or fortied human milk on growth or development is
scarce [42], and the nutritional needs of preterm infants seem to be del-
icate and inter-individually variable [27].
4.4. Strengths and limitations
Our sample was collected prospectively and longitudinally, based on
a single centre. The sample size of a single centre will obviously never
reach that of multicentre studies, however, our approach has the strong
advantages of comparable peri- and postnatal management including a
uniformly supported nutrition plan, and of prospective and standard-
ized assessment of all parameters which were fed into our analyses.
Since the reliable and valid assessment of anthropometric data and
standardized growth parameters poses a range of challenges [14], the
uniform approach in a single-centre study aids to strengthen the valid-
ity of analyses and results. Data on maternal education was missing in a
large part of our cohort, and children with missing data scored signi-
cantly below those with complete data in the K-ABC. We could specu-
late that mainly mothers with low educational background failed to
complete the questionnaire (due to comprehension problems or em-
barrassment?), so that the negative effect of low maternal education
would still, although signicant, be underestimated in our sample [36].

Table 3
Multiple regression analyses on the predictive effects of antenatal growth and immaturity-related morbidity on growth parameters.

Weight Length Head circumference

Birth to discharge Discharge to Birth to discharge Discharge to Birth to discharge Discharge to

school-age school-age school-age

p p p p p p

Predictor strength
Birth SDSa 0.402 b0.001 0.382 b0.001 0.512 b0.001 0.442 b0.001 0.692 b0.001 0.050 0.607
Immaturityb 0.239 0.003 0.093 0.287 0.370 b0.001 0.424 b0.001 0.197 0.002 0.039 0.692
ICH (grade) 0.076 0.338 0.050 0.583 0.039 0.513 0.097 0.267 0.030 0.603 0.077 0.408
Sepsis (yes/no) 0.106 0.169 0.068 0.425 0.000 0.995 0.033 0.696 0.072 0.207 0.151 0.098

Model strength
R2 0.259 0.151 0.599 0.179 0.605 0.029
F(df) 11.009(4126) 5.303(4119) 44.801(4120) 1.727(4116) 47.167(4123) 0.910(4121)
p b0.001 0.001 b0.001 b0.001 b0.001 0.461

Signicant predictions (p b .05) are printed in bold.

a
Standard score for weight, length, or head circumference at birth.
b
Standardized factor score: gestational age, BPD (yes/no), ventilation (days), postnatal corticosteroids (yes/no), large scores indicating high degree of immaturity.
 K. Lidzba et al. / Early Human Development 103 (2016) 183187
5. Conclusions
Our nding that post-discharge head growth has a stronger inu-
ence on school-age intelligence than growth during hospitalization
has implications for the clinical management of VP born children. We
suggest for future studies to focus on the determinants of head growth
after discharge from hospital, when nutrition and education lie mainly
in the caregivers' responsibility.
Financial disclosure
All authors have no nancial relationships relevant to this article to
disclose.
Conicts of interest
All authors report that they have no conicts of interest to disclose.
Acknowledgements
We are grateful to Bernd Michael Ranke for initiating and advancing
the longitudinal study. Thank you to Heidrun Rauscher-Lacher and
Martina Jotzo for conducting the psychological assessments and to
Hartmut Wollmann for data collection in the neonatal period.
Data collection and analysis was conducted without external
funding, manuscript preparation was partially supported by the Ger-
man lay organisation Oliver-Vaihinger-Fonds, Tbingen, Germany
(grant to KL). The sponsor had no inuence on 1) study design; 2)
data collection, analysis, and interpretation; 3) writing of the report;
4) submission.
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