e u r o p e a n j o u r n a l o f p a e d i a t r i c n e u r o l o g y 1 7 ( 2 0 1 3 ) 1 9 2 e1 9 8

Official Journal of the European Paediatric Neurology Society

Original article

Neurological assessment in infants discharged from

a neonatal intensive care unit

Domenico M.M. Romeo a, Matteo Cioni b,*, Filippo Palermo c, Salvo Cilauro d,
Mario G. Romeo d
a
Paediatric Neurology Unit, Catholic University, Rome, Italy
b
Gait and Motion Analysis Laboratory, Department of Clinical and Experimental Biomedicine, University of Catania, viale A. Doria 6,
95125 Catania, Italy
c
Department of Internal and Specialist Medicine, Section of Infectious Disease, University of Catania, Italy
d
Neonatal Intensive Care Unit, Department of Paediatrics, University of Catania, Italy

article info abstract

Article history: Background: Longitudinal motor assessment in infants at different neurodevelopmental risk
Received 15 April 2012 has not been previously evaluated using structured assessments.
Received in revised form Aim: To verify if the Hammersmith Infant Neurological Examination (HINE) is a good tool to
10 September 2012 predict the neuromotor outcome in infants discharged from a level IIeIII Neonatal Inten-
Accepted 15 September 2012 sive Care Unit (NICU)
Methods: In this cohort analysis, 1541 infants discharged from our NICU between January of
Keywords: 2002 and the April 2006 were enrolled and assessed using the HINE at 3, 6, 9, 12 months. At
Hammersmith infant neurological two years, these infants were further assessed, and grouped into infants with normal
examination outcome (1150), with mild disability (321) and with cerebral palsy (70),
Prediction Results: Correlation analysis of Spearman showed a significant ( p < 0.0001) and moderate
NICU (r2 ¼ 0.55 to 0.73) negative correlation between HINE scores (3, 6, 9, 12 months) and
Neurological outcome neurological outcome at two years. Cut-off scores for each assessment’ age were provided
as predictive value for cerebral palsy.
Discussion: This study mainly showed that HINE, as soon as the first months of life, helps in
the process of prediction of neurological outcome at two years of age in a heterogeneous
population of infants discharged from an NICU.
ª 2012 European Paediatric Neurology Society. Published by Elsevier Ltd. All rights
reserved.

1. Introduction infants, because of transitory neurological abnormalities

(involving posture, fine and gross motor control, coordination
The possibility to differentiate a normal by an abnormal motor and reflexes), detected in the 40e80% of cases but disappear-
performance at early age is of interest for infants at risk for ing during the second year of life.2,3 In order to follow up these
neurodevelopmental disabilities.1 During the first year of age, infants, a specific evaluation tool can represent a good
special attention should be given to motor progresses of these response to the parents requests for a correct valuation and

* Corresponding author. Tel.: þ39 095 7384079; fax: þ39 095 738 4238.
E-mail address: [email protected] (M. Cioni).
1090-3798/$ e see front matter ª 2012 European Paediatric Neurology Society. Published by Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.ejpn.2012.09.006
 e u r o p e a n j o u r n a l o f p a e d i a t r i c n e u r o l o g y 1 7 ( 2 0 1 3 ) 1 9 2 e1 9 8 193

prognosis. Several methods are used for the neurological due to the presence of congenital anomalies, other 34 infants
assessment of the risk infants after the neonatal period.1,3e6 because of transferring to II level hospitals in their own native
In 1981, Dubowitz et al.7,8 developed a neurological examina- towns, after stabilization of the clinical condition, and 258
tion for the neonatal assessment of preterm and term infants infants because they did not complete the follow-up program.
to identify those at risk for neurological abnormalities. Later The study protocol was previously approved by the Ethics
on, the same authors9 developed the Hammersmith Infant Committee of our Institutions and informed consent was ob-
Neurological Examination (HINE), based on the same princi- tained from all the parents.
ples, to be used during the first two years from birth. This tool
is performed quickly and easily in a clinical setting and a high 2.1. Neurological examination
concordance with the severity of locomotor functioning has
been demonstrated.9e12 The HINE9 was used for the assessment of all infants enrolled
Recently, we used the HINE in specific groups of high risk in this study. This is a simple and scorable method for
newborns,13e16 providing detailed information on neurolog- assessing infants between 2 and 24 months of age, including
ical assessment in these infants, but the experimental design items for cranial nerve function, posture, movements, tone
did not allow us to give a significance of prediction to the and reflexes. An optimality score is obtained by calculating
results for children at different neurodevelopmental risk the distribution of the frequency of the scores in the normal
using specific cut-off scores. This topic could be worthy of population, defining as optimal all the scores found in at least
interest since prediction of a neurodevelopmental abnor- 90% of the cohort. The overall score ranges from a minimum
mality could allow a precocious rehabilitation intervention of 0 to a maximum of 78. At 9 or 12 months, the scores equal or
resulting in promotion and acceleration of motor develop- above 73 are regarded as optimal, if below 73 as suboptimal;
ment.17 Infants admitted to Neonatal Intensive Care Unit while at 3 and 6 months healthy term infants scored equal or
(NICU) are at different risk for neurodevelopmental disabil- above 67 and 70 (median) respectively.9,20 In this retrospective
ities due to possible brain damage related to prematurity, study, we analysed files of patients investigated by the HINE at
asphyxia, haemorrhage, etc. 3, 6, 9 and 12 months (corrected for prematurity) with the
Therefore, the aim of this study was to test the hypothesis that score of single subsections of items and a global optimality
the HINE score within a specific range, from the age of 3 months, score for each period, according to the clinical protocol
could be used to predict later neurodevelopmental outcomes at 2 routinely performed in our NICU. Global cut-off scores were
year from birth in newborns discharged from an NICU. used as previously reported.11e13

2.2. Outcome
2. Methods
At two years corrected age all infants were assessed with
All the infants described in this study were part of a follow-up a structured neurologic examination6,21 and using the Bayley
research project carried out at the NICU of the Department of Scales of Infant Development second edition (BSID-II).22
Paediatrics of the University of Catania. This is a level II Although BSID-II comprises three separate scales (Mental,
(specialty care) and level III (subspecialty) neonatal intensive Motor and Behaviour Scales), for the purpose of the present
care center,18 admitting patients affected by prematurity, study, only the Motor Scale was administered. The BSID-II has
twins, low birth-weight, asphyxia, cardiopathy, cerebral been shown to be a comprehensive and appropriate instru-
malformations as well as surgery newborns. All patients were ment for assessing motor performance.23 The motor scale of
enrolled routinely on a two-year follow-up research protocol. the BSID-II assesses gross and fine motor skills. Raw scores on
Between January 2002 and December 2006, 1853 consecutive this scale were converted to a psychomotor developmental
patients were discharged from the NICU. A cranial ultrasound index (PDI) with a mean of 100 and a standard deviation of 15.
(US) was performed in all the infants within the 6th day from Scores 115 are considered as accelerated performance,
birth in both preterm and term born infants and at least a score of 85e114 as within normal limits, a PDI of
another one at term age for preterm newborns. The US per- 70e84 as mildly delayed performance, whereas a score of not
formed at term age were classified as follows: (i) no abnormal more than 69 is defined as significantly delayed motor
signal or transient flare (periventricular echodensity lasting performance.22
less than 14 days) or isolated intraventricular haemorrhage According to the motor outcome, infants were classified in:
grade I according to Volpe19; (ii) persistent flare (bilateral normal outcome (N) for those without neurological abnor-
periventricular echodensity persisting more than 14 days) malities and a PDI85, with mild disability (MD) with a PDI < 85
without haemorrhage; (iii) isolated ventricular dilation; (iv) and/or mild neurological signs, but no cerebral palsy (CP), and
intraventricular haemorrhage grade II or III according to in cerebral palsy (CP) according to the criteria proposed by
Volpe19; (v) cystic periventricular leukomalacia with or Himmelmann et al.24 The latter children were further fol-
without haemorrhage or unilateral intraparenchymal echo- lowed until the age of 5 years, to confirm the diagnosis.
density. For the purpose of the present study, we included
those infants with a detailed clinical follow-up consisting of 5 2.3. Statistical analysis
evaluations (3, 6, 9, 12, 24 months). The exclusion criteria were
the presence of congenital anomalies, transfer to another The anthropometric variables (weight and gestational age)
hospital, or an incomplete follow-up program. Then, 312 were reported as mean  SD. Values of HINE scores were re-
infants out of 1853 were excluded from the study: 20 infants ported as median and range at different ages, for each group of
194 e u r o p e a n j o u r n a l o f p a e d i a t r i c n e u r o l o g y 1 7 ( 2 0 1 3 ) 1 9 2 e1 9 8

Table 1 e Characteristics of the population and neurological outcome.

Number Gender Gestational age Weight

Male Female Median (weeks) Range (weeks) Median (GR) Range (GR)

N 1150 601 549 36 25e42 2420 920e5350

MD 321 170 151 37þþþ 26e43 2450þþþ 630e4570
CP 70 45 25 33*** 26e41 1880*** 880e3900
TOT 1541 816 725 36 25e43 2500 630e5350

N, normal outcome; MD, minor neurological dysfunction; CP, cerebral palsy.

***p < 0.0001 Statistical difference between normal vs cerebral palsy.
þþþp < 0 .0001 Statistical difference between MD vs cerebral palsy.
No statistical difference between normal vs MD.

infants. Inter-group comparisons have been done by a non- a hemiplegia and 5 a dyskinetic type. Infants with CP showed
parametric test (Kruskall-Wallis test followed by Dunn’s post a significant lower mean gestational age than those with
test). The Spearman Rank Correlation test was used to corre- normal outcome ( p < 0.0001) and children with MD ( p < 0.0001).
late the HINE scores obtained at 3e12 months and the US Similarly, infants with CP had a significant lower mean birth-
findings with the severity of the outcome at two years of age. weight ( p < 0.0001) than the other two groups of infants.
Comparison between HINE scores of term born infants and
preterm was done by using the non-parametric test of Man- 3.2. US scan findings
neWitney U. The level of significance was set at p < 0.05.
Sensitivity and specificity were further used to assess the No abnormal signals or transient flares were present in 1185
predictive value of cut-off scores. infants (60 very preterm, 645 late-preterm, 480 term born
infants); persistent flares in 226 infants (51 very preterm, 85
late-preterm, 90 term born infants); isolated ventricular dila-
3. Results tation in 95 infants (29 very preterm, 15 late-preterm, 51 term
born infants); intraventricular haemorrhage grade II or III in 19
3.1. Characteristics of population infants (6 very preterm, 3 late-preterm, 10 term born infants);
cystic periventricular leukomalacia in 16 (6 very preterm, 6
A total of 1541 infants were included in the study: 149 were very late-preterm, 4 term born infants).
preterm (gestational age (GA) 25e32 weeks); 754 were late-
preterm (GA 33e36 weeks); 638 were born at term (GA 37e43 3.3. Infant neurologic examination
weeks). Table 1 shows the general characteristics of the pop-
ulation related to neurological outcome at 2 years. Of the 70 At 3 months of age (Table 2) all infants with normal outcome
children with CP, 26 showed a diplegia, 20 a quadriplegia, 19 scored above 48 (median 64) and namely between 48 and 66

Table 2 e Global scores of the Hammersmith infant neurological examination and neurological outcome.
Total number Score median Range of scores Score 73 Score 67e72 Score 40e66 Score <40

N
3 Months 1150 64* 48e71 0 135 (12%) 1017 (88%) 0
6 Months 1150 68* 54e76 28 (2%) 641 (56%) 483 (42%) 0
9 Months 1150 70* 59e78 429 (37%) 613 (53%) 110 (10%) 0
12 Months 1150 73* 63e78 581 (50%) 559 (49%) 12 (1%) 0

MD
3 Months 321 58# 40e65 0 0 319 (100%) 0
6 Months 321 63# 43e70 0 37 (12%) 282 (88%) 0
9 Months 321 66# 46e74 8 (3%) 128 (40%) 183 (57%) 0
12 Months 321 67# 47e75 19 (6%) 155 (49%) 145 (45%) 0

CP
3 Months 70 35.5þ 14e62 0 0 32 (46%) 38 (54%)
6 Months 70 40þ 16e65 0 0 37 (53%) 33 (47%)
9 Months 70 44þ 22e69 0 4 (6%) 44 (63%) 22 (31%)
12 Months 70 45.5þ 24e70 0 5 (7%) 47 (67%) 18 (26%)

N, normal outcome; MD, minor neurological dysfunction; CP, cerebral palsy.

*Normal vs MD ( p < 0.001).
þNormal vs cerebral palsy ( p < 0.001).
#MD vs cerebral palsy ( p < 0.001).
 e u r o p e a n j o u r n a l o f p a e d i a t r i c n e u r o l o g y 1 7 ( 2 0 1 3 ) 1 9 2 e1 9 8 195

(90%). A progressive increase of score was observed until 12 91%), and 65 (se 91%; sp 90%), respectively at 6, 9 and 12
months. At this age the 50% of infants gained an optimality months. Considering the type of CP, at 3 months the cut-off
score  73. On the other hand, all infants with MD scored in score of 39 showed the higher prediction for a severe CP
the range of 40e66 at 3 months of age. In this group of infants, (quadriplegia/diplegia/diskinetic) with a sensitivity of 100%
a progressive improvement of score from 3 months onward and a specificity of 99%; the same power prediction was
was observed, but with minimal changing from 9 months. Few observed using a cut-off of 41, 45 and 47, respectively at 6, 9
infants only gained at 9 and 12 months scores 73 (3 and 6% and 12 months. For infants with hemiplegia at 3 months the
respectively). The group of infants with CP showed the lowest cut-off score of 49 shows the higher prediction with a sensi-
scores with a median global score from 35.5 at 3 months to tivity <10% and a specificity of 99%; the same power predic-
45.5 at 12 months; no one of them gained the scores 73 at 9 or tion was observed using a cut-off of 55, 61 and 63, respectively
12 months, considered as optimal. Global and subsection at 6, 9 and 12 months.
scores’ details of infants with CP were previously reported.13 When considering examinations longitudinally, the
A statistical inter-group comparison showed that, at all assessments showed to be not always consistent in classi-
ages, infants with N scored significantly ( p < 0.001) higher fying children results as suboptimal, according to the age
than those with MD and CP. specific cut-off value. In 61/256 infants with suboptimal
Table 3 showed that at 3, 6, 9 and 12 months of age, infants scores at the first evaluation, the assessment was not
with N scored significantly higher ( p < 0.01) than infants with consistent across the other three examinations, becoming
MD for all subsection but posture at 3 months. Infants with N optimal in at least one assessment; 46 of them were classified
scored significantly higher ( p < 0.001) than those with CP in all as normal at 2 years. In 13/1285 infants with optimal scores at
subsections at every age; infants with MD scored significantly the first evaluation, the assessment was not consistent
higher ( p < 0.001) than those with CP except for cranial nerve across the other three examinations, becoming suboptimal in
at 3 and 6 months of age. at least one assessment; four of them were classified as
Fig. 1 showed the correlation analysis of Spearman with normal at 2 years.
a moderate to strong and significant ( p < 0.0001) negative All the children with CP and almost the 20% of those with
correlation between HINE scores (3, 6, 9, 12 months) and MD were under a treatment in several services of rehabilita-
outcome at two years; according to the GA, very preterm tion (3e5 times/week) at 2 years. There were no significant
showed a better correlation (0.72 to 0.76) than term born differences of HINE scores for children with MD between
infants (0.58 to 0.72) at every ages. At 3 months, the cut-off those under treatment or not.
score of 56 reported the higher prediction for CP with a sensi- Irrespective of the neurological classification, very preterm
tivity of 96% and a specificity of 85%; similar results were infants (GA32 weeks) showed significantly lower global
observed using a cut-off of 59 (se 90%; sp 89%), 62 (se 90%; sp scores at all ages than term born ones.

Table 3 e Subsection’s score of the Hammersmith infant neurological examination.

Age Cranial nerve Posture Movements Tone Reflexes

Median (range) Median (range) Median (range) Median (range) Median (range)

3 Months
N 14 (11e15)*** 14 (6e18)ns 6 (3e6)*** 20 (13e24)*** 9 (3e15)**
MD 13 (6e15)ns 14 (7e17)# 5 (0e6)# 18 (14e23)# 8 (3e13)#
CP 12 (7e15)þ 10 (3e16)þ 1 (0e5)þ 12.5 (3e22)þ 4 (1e9)þ

6 Months
N 15 (11e15)*** 15 (6e18)*** 6 (3e6)*** 21 (13e24)*** 11 (5e15)***
MD 14 (6e15)ns 14 (9e18)# 5 (1e6)# 20 (14e24)# 10 (4e13)#
CP 13 (7e15)þ 11 (4.5e16)þ 1 (0e5)þ 13 (3.5e22)þ 4 (1e9)þ

9 Months
N 15 (12e15)*** 16 (7e18)*** 6 (3e6)*** 22 (15e24)*** 12 (5e15)***
MD 15 (7e15)# 15 (10e18)# 5 (2e6)# 20 (15e24)# 11 (5e14)#
CP 13 (9e15)þ 12 (6e17)þ 1 (0e5)þ 14 (6e23)þ 5 (1e10)þ

12 Months
N 15 (13e15)*** 17 (8e18)*** 6 (3e6)*** 23 (17e24)*** 13 (6e16)***
MD 15 (7e15)# 16 (10e18)# 5 (2e6)# 21 (15e24)# 11 (5e14)#
CP 13.5 (9e15)þ 13 (6e18)þ 1 (0e5)þ 15 (7e23)þ 5 (1e11)þ

N, normal outcome; MD, minor neurological dysfunction; CP, cerebral palsy.

*Normal vs MD (**p < 0.01; ***p < 0.001).
#MD vs cerebral palsy ( p < 0.001).
þNormal vs cerebral palsy ( p < 0.001).
196 e u r o p e a n j o u r n a l o f p a e d i a t r i c n e u r o l o g y 1 7 ( 2 0 1 3 ) 1 9 2 e1 9 8

Fig. 1 e HINE, Hammersmith infant neurological examination; N, normal outcome; MD, minor neurological dysfunction; CP,
cerebral palsy.

3.4. Infant neurologic examination and cranial 7 months of age, but with little changes on the scores obtained
ultrasonography at 9 and 12 months. Furthermore the median and range of
scores obtained in the present study by those infants with
Of the 1188 infants with normal ultrasounds or transient normal outcome, were lower than the normative data,9,20
flares only 25 had scores below the cut-off values at all age mainly at earlier ages, whereas at 12 months more similar
periods. All the infants with cystic periventricular leukoma- results were observed. Probably, these differences were
lacia had scores below the cut-off values at all age periods. related to the characteristics of our population. In fact,
Infants who had other ultrasonogram abnormalities had although they showed a normal outcome at two years of age,
widely varying scores, both below and above the cut-off scores they were discharged from an NICU because of prematurity,
at all ages. sepsis, asphyxia etc; therefore they could not be considered
a real low-risk population, with a possible different motor
development at least during the first year of age.10,25e27
4. Discussion Very preterm infants showed lower scores than term born
at each ages, as previously reported10,12,14e16,24e26 and in the
The main results of this study showed that, as soon as the first three sub-groups according to the outcome. Although normal
months of life, the HINE helped to predict the neurological scans or minor lesions tended to be associated with optimal
outcome at two years from birth in a heterogeneous and large scores and cystic periventricular leukomalacia with low
population of infants discharged from an NICU. scores, the HINE scores were not strictly associated with the
In a previous study13 we used the HINE to describe the pattern of US findings, consistent with previous reports.10,15
neuromotor development of infants with CP during the first When we considered the subsection scores, other inter-
year of age and to differentiate infants with diplegia from esting information are observed. In fact, infants with N scored
those with quadriplegia by a lower scoring of the latter in the significantly better in all subsections than both those with CP
subsections tone and posture. In the present study, we and MD, even if the latter and N scored similarly for “posture”
extended these observations in term of prediction assessing at 3 months; this data could reflect a similar early postural
a large population of infants discharged from NICU. As we development in infants, with normal or quite normal motor
expected, infants with N showed higher global and subsec- outcome, who attended an NICU. Infants with MD showed
tions scores at all ages than both those with MD, with the higher scores than those with CP for all subsections except for
exception of posture at 3 months, and with CP. A progressive “cranial nerve” at 3 and 6 months, making this subsection less
increase of motor development is observed during the first sensitive than others in differentiating these two populations
year of from birth. This last result is quite different from the of infants.
findings reported by Haataja et al.,9,20 who also showed, in The HINE global score was correlated with the outcome,
low-risk term born infants, a progressive improvement before with a better correlation for the results at 9 and 12 months and
 e u r o p e a n j o u r n a l o f p a e d i a t r i c n e u r o l o g y 1 7 ( 2 0 1 3 ) 1 9 2 e1 9 8 197

for very preterm infants. It is not surprising that the findings 2. Marlow N. Neurocognitive outcome after very preterm birth.
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infant neurodevelopmental screener with premature infants.
older infants, and some of the items assessing sitting posture
Brain Dev 2006;28:104e8.
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when assessing infants at 3 months.14 However infants with five years of life: a pervasive assessment of neurological
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a CP, at 3 months and 12 months respectively, with scores <40 5. Einspieler C, Prechtl HFR, Bos AF, Ferrari F, Cioni G. Prechtl’s
were reported in CP only. Previous researches reported cut-off method on the qualitative assessment of general movements in
scores similar to those of the present study,10e15 but for the preterm, term and young infants. London: Mac Keith Press; 2004.
6. Touwen BCL. Neurological development in infancy. Clin Dev
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Med 1976;58:1e150.
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high neurological risk. Not surprisingly this correlation is preterm and full term infant. London: Heinemann; 1981.
more stronger in very preterm infants as they show a higher 8. Dubowitz L, Dubowitz V, Mercuri E. In: The neurological
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9. Haataja L, Mercuri E, Regev R, et al. Optimality score for the
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age. J Pediatr 1999;135:153e61.
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Other neurological tools have been used to predict the neurologic optimality score at 9 and 18 months in preterm
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a good sensitivity and specificity (77% and 82% at 4 and 86% 12. Ricci D, Cowan F, Pane M, et al. Neurological examination at 6
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tools showed a lower prediction when assessing infants at low
Romeo MG. Neuromotor development in infants with cerebral
risk.30,31 Compared to these tools, the HINE showed the
palsy investigated by the Hammersmith Infant Neurological
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