RESEARCH PAPER
Warning Signs on Short Hammersmith Neonatal Neurological
Examination and Correlation With Hammersmith Infant Neurological
Examination Global Score in Preterm Infants: A Prospective Cohort Study
MANISHA BHANDANKAR, DEEPA METGUD
Department of Pediatrics, Jawaharlal Nehru Medical College, Belgaum, Karnataka.
Correspondence to: Dr Manisha Bhandankar, Professor of Pediatrics, Jawaharlal Nehru Medical College, Belgaum, Karnataka.
manisha.bhandankar1970@gmail.com
Received: April 22, 2022; Initial review: June 1, 2022; Accepted: March 3, 2023.
Objective: To describe the findings of short Hammersmith Neona-
tal Neurologic examination (HNNE) in preterm small for gestational
age (SGA) and appropriate for gestational age (AGA) infants at
term equivalent age (TEA) and to correlate it with the global score of
Hammersmith Infant Neurologic Examination (HINE) performed at
4-6 months of corrected age.
Methods: This prospective cohort study was conducted at the high
risk follow-up clinic of our center. 52 preterm infants born <35
weeks gestation were examined using HNNE at TEA and followed-
up till 4-6 months of corrected age to estimate HINE.
Results: 20 infants (38.5%) had warning signs and 9 (17.3%) had
P
reterm infants are known to be at high risk for
developmental delays because of their gestatio-
nal age, morbidities associated with prematurity,
and consequences of interventions in the neonatal
intensive care unit (NICU) [1]. Additionally, adequate
intrauterine growth of fetus is essential for normal extra-
uterine growth and development [2,3]. Early recognition of
abnormal neurologic signs as predictors of neurodevelop-
mental delay in infants at risk due to prematurity and related
morbidities is essential to introduce early intervention [4-6].
Several tools are available to screen infants from
neonatal period to identify those at risk of developmental
delay. Hammersmith neonatal neurological examination
(HNNE), initially developed by Dubowitz in 1981, has 34
items assessing tone, motor patterns, observation of
spontaneous movements, reflexes, visual and auditory
attention, and behavior. Short Hammersmith neonatal
neurological examination is a screening tool consisting of 12
items modified from original complete HNNE. This tool is
used to assess the posture, tone, movement, reflexes, and
motor milestones in the both term and preterm infants at term
equivalent age (TEA). The proforma has a central grey
column that covers the spectrum of neurologic findings
INDIAN PEDIATRICS
abnormal signs on short HNNE. 12 (37.5%) AGA infants and 6
(30%) SGA infants had global score <65 at mean corrected age
(SD) of 4.3 (0.7) weeks and 4.5 (0.8) weeks, respectively. Very
preterm, birth weight <1000 g and SGA was significantly associated
with global scores <65.
Conclusion: Early identification of warning signs among SGA in-
fants using Short HNNE screening at TEA can be useful to initiate
early intervention. There was no statistically significant difference in
global scores by HINE among AGA and SGA infants in early in-
fancy.
Keywords: Low birth weight, Prognosis, Small for gestational age.
Published online: March 20, 2023; PII: S097475591600513
within the reference range (90%); the lateral columns include
all the warning signs and the last line indicates abnormal
signs. The authors have reported that the short HNNE was
able to identify 98.5% preterm infants with an abnormal full
neurologic examination (complete HNNE) at term [7,8]. The
Hammersmith infant neurological examination (HINE) has
been proposed as a simple and scorable early neurological
examination tool for the diagnosis of cerebral palsy for
evaluating infants between 2 months and 24 months of age.
Significant correlation between the HNNE and HINE score
to predict infants at risk of cerebral palsy in early infancy has
been reported [9]. Similar data regarding short HNNE has
not been reported.
Invited Commentary:Page 619
India is a major contributor of preterm and low birth
weight infants with intrauterine growth restriction. A quick
and reliable screening tool such as short HNNE can be of
significant help in identification of infants in the busy follow-
up clinics.
In this study, we intended to examine preterm infants
(born <35 weeks gestational age) at TEA using short HNNE
637 VOLUME 60__AUGUST 15, 2023
30 SHORT HNNE AND HINE IN PRETERMS

and then at four to six months of corrected age using HINE. Kerala. The findings were recorded in the standardized form
The primary objective was to describe the preterm infants and scored as per the protocol.
using short HNNE at TEA and to correlate it with the HINE
Neurosonogram was done as part of routine protocol at
global score performed at four to six months of corrected
TEA. All the infants received early stimulation and inter-
age. The secondary objective was to compare this finding
vention as deemed necessary during follow-up from trained
among small for gestational age (SGA) and adequate for
psychologists and physiotherapists.
gestational age (AGA) infants.
Statistical analysis: Data were analyzed using statistical
METHODS
software R version 4.0.2 and Microsoft Excel. Continuous
This prospective observational study was conducted among variables were represented by mean (SD)/median (range)
a cohort of preterm infants less than 35 weeks who were and categorical variables represented by frequency and
identified to be SGA or AGA at birth and followed-up in the percentage. Chi-square test was used to check the association
high-risk follow-up clinic of a tertiary care hospital in between categorical variables and t test/Mann-Whitney test
Karnataka from October, 2019 to September, 2020. to compare mean/distributions between groups. Monte-
Carlo simulation used in chi-square test was used to assess
Ethical clearance was obtained from the ethics
the primary and secondary objectives of the study.
committee of Jawaharlal Nehru Medical College and a
written informed consent was obtained from the parents. RESULTS
Preterm infants born <35 weeks gestation discharged from
Out of total 99 infants who were examined at 40 weeks of
the NICU and followed-up at the high-risk baby clinic of the
gestation (39+1 to 41+6 weeks), 52 infants were examined
hospital were included. Infants with proven intrauterine
using both short HNNE and HINE during the study period
infection, major congenital malformations requiring surgery,
and were included in the analysis (Fig. 1). Twenty infants
proven inborn errors of metabolism, and proven genetic/
were SGA and 32 infants were in AGA group. Table I gives
syndromic condition known to be associated with
the demographic details of the infants enrolled in the study.
developmental delay before enrolment were excluded. The
infants were categorized based on birthweight into SGA Among 52 infants, 20 (38.4%) had warning signs and 9
(below 10th centile) and AGA (between 10th to 90th centile) (17.3%) had abnormal signs using Short HNNE at TEA.
based on Fenton preterm growth chart [9]. Sixteen (80%) of these infants with warning signs were very
preterm, and rest four were extreme preterm. Fourteen
Based on previous studies of 15% abnormal findings
infants had single warning sign and six infants (11.5%) had
among preterm infants using complete HNNE, the sample
≥2 warning signs. Maximum number of infants had warning
size with percentage of maximum error as 10% at 95%CI
signs in the spontaneous activity and head control. The mean
was calculated as 49 [8,11,12].
(SD) age of assessment for HINE was 4.4 (0.7) months and
Demographic details, antenatal risk factors and anthro- the median (range) HINE Global score was 66 (35-74). Most
pometry were recorded in a structured form at the time of infants scored low on reflexes and reactions component of
follow-up. Both the examinations were done by either of the HINE.
two examiners, who were not blinded to the records. The
examiners learnt the examination from the educational Table I Demographic Details of the Enrolled Infants
videos available at the Hammersmith neurological exami-
AGA (n=32) SGA (n=20)
nation website, and received additional training at CDC,
Female 12 (37.5) 11 (55)
Gestational age (wk)a 31.56 (2.26) 32.11 (2.26)
99 neonates examined at term equivalent age using HNNE Weight at birth (g)a,b 1562.16 1169.75
(492.4) (333.3)
→ 20 infants not brought for follow-up FC at birth (cm) a 29.97 (1.99) 28.73 (2.01)
Length at birth (cm) a 41.65 (3.78) 40.79 (4.01)
→ 17 infants followed-up till 3 mo corrected age
Ventilated 4 (12.5) 5 (25)
→ 10 infants followed-up at 6 mo corrected age Culture proven sepsis 4 (12.5) 5 (25)
Maternal chorioamnionitis 1 (3.12) 1 (5)
52 infants examined at 4-6 mo corrected
→ age using HINE
Two doses of antenatal steroid 10 (31.2) 14 (70)
IVH (Grade I-II) 2 (6.25) 2 (10)
Fig. 1 Flow chart of participants. Values in no. (%) or amean (SD). All P >0.05 except bP <0.001.

INDIAN PEDIATRICS 638 VOLUME 60__AUGUST 15, 2023

BHANDANKAR AND METGUD
SGA: small for gestational age, AGA:appropriate for gestational age.
Fig. 2 Box and whisker plot of distribution of median global score
in both SGA and AGA group.
In subset analysis, warning signs were present among 11
(34.4%) and nine infants (45%) from AGA group and SGA
group, respectively but there was no significant difference
between the two groups in median (IQR) HINE global score
[66 (35,74) vs 67.5 (38,72); P=0.43].
Eighteen infants had global score ≤65 of whom 12 were
AGA and six were SGA infants. Seven infants out of 18 had
single warning sign and three had ≥2 signs on short HNNE
(all SGA). Presence of even single warning sign on short
HNNE examination in SGA group was significantly
associated with global score of ≤65 (P=0.004).
On neurosonogram, resolving germinal matrix bleed
was reported among three infants but none of the infants
had ventriculomegaly. Periventricular hyperechogeni-
cities were reported in three infants during the follow-up.
DISCUSSION
Short HNNE is a screening tool which takes few minutes to
perform if the infant is alert and active (Brazelton stage 4-5)
compared to that of complete HNNE, which requires 10-15
minutes [13]. In our study, six infants (11.5%) had ≥2
warning signs with no significant correlation between
warning signs, abnormal signs on short HNNE and HINE
global score. Romeo, et al. [7] reported that in the 380 very
pre-term infants, 5% had two and 1% had >2 warning signs
with good correlation to lower optimality score on complete
HNNE. Among the infants with warning signs three each
were very preterm and extreme preterm infants. Spittle, et al.
[14] have reported that 25% of infants who were born
moderately or late preterm scored suboptimal on complete
HNNE score.
Though, we found a non-significant association between
the findings of short HNNE among preterm infants and the
INDIAN PEDIATRICS
31
HINE global score at 4-6 months, it helped us in early
identification of infants with warning signs. Literature review
gives HINE global score cutoff levels in the range of 57 to
66; separately for preterm and term infants from 3 to 12
months of age to predict cerebral palsy [9,14,15]. To explore
the correlation of warning signs with low HINE global
scores, we analyzed the short HNNE data in infants with
HINE global score of ≤65 and noted a trend towards lower
HINE global score (≤65) among SGA infants who had
warning signs on short HNNE. Follow-up data of these
infants to know how many continue to have lower global
scores by the end of two years is pivotal for this study.
The ‘visual orientation’ assessment from HNNE form
was affected by the iatrogenic pupillary dilatation of the
infants done for ROP examination prior to the neurologic
examination in the high risk follow-up clinic in ten infants;
hence, we did not analyze this warning sign. This
compromised our understanding of development of infant’s
visual function and the final analysis of number of warning
signs in all infants, which is a major limitation of the study.
The hyperechogenicities reported in neurosonogram in
our study could be evolving periventricular leukomalacia
(Grade 1), which were detected in three infants, of whom two
infants had >2 warning signs [15]. This is not significant with
respect to neurodevelopmental outcome as studies have
reported absence of obvious abnormal findings in neuro-
sonogram, even in presence of cellular insult [17,18].
The major limitation of this study is loss of data due to
difficulties in follow-up of infants within the study period
secondary to the restrictions of the COVID-19 pandemic,
and iatrogenic pupillary dilatation affecting the assessment
of visual orientation during HNNE.
We assessed the utility of short HNNE in recording
warning signs among preterm infants. This may be useful in a
busy resource-limited setting to identify infants (SGA in
particular) who require regular follow-up and may thus be
benefited from timely early intervention [6,15]. Further
research through large studies, and long-term follow-up till
minimal two years corrected age is necessary to understand
which warning and/or abnormal signs on short HNNE during
infancy have correlation with low global scores by two years
of age.
Ethics clearance: EIC, Jawaharlal Nehru Medical College
Institutional Ethics Committee on Human subjects’ research; No.
MDC/DOME/226 dated Dec 28, 2019.
Contributors: MB: designed and conducted the study, analyzed
and interpreted the data, drafted the manuscript. DM: substantial
contributions to the conception or design of the work, inter-
pretation of data for the work and revising the manuscript critically.
Both authors approved the version to be published and agree to be
accountable for all aspects of the work in ensuring that questions
639 VOLUME 60__AUGUST 15, 2023
32
WHAT THIS STUDY ADDS?
• Preterm infants with one or more warning signs on short Hammersmith Neonatal Neurological Examination may
have lower global score by Hammersmith Infant Neurological Examination during early infancy.
related to the accuracy or integrity of any part of the work are
appropriately investigated and resolved.
Funding: None; Competing interests: None stated.
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