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Acta Pædiatrica ISSN 0803-5253

REGULAR ARTICLE

Discriminant ability of the Infant Neurological International Battery


(INFANIB) as a screening tool for the neurological follow-up of high-risk
infants in Colombia
Nathalie Charpak (ncharpak@gmail.com)1, Ana Marıa de la Hoz2,3, Julieta Villegas1, Fabian Gil2,3
1.Fundacio n Canguro, Bogota, Colombia
2.Pontificia Universidad Javeriana, Bogota, Colombia
3.Hospital Universitario San Ignacio, Bogota, Colombia

Keywords ABSTRACT
Follow-up studies, Kangaroo Mother Care, Aim: The aim of this study was to assess the discriminative ability of the Infant Neurological
Low birthweight, Neurological examination,
Premature infant International Battery (INFANIB), applied at 3, 6 and 9 months of corrected age (CA), on
neurological outcomes at 1 year of CA.
Correspondence
n Canguro, Calle 56A
Nathalie Charpak, Fundacio Method: An observational analytic study was conducted on a cohort of 5857 infants,
No 50-36 Bloque A13, Apto 416, Pablo VI Azul. followed up to 1 year of CA in a Kangaroo Mother Care programme from 1993 to 2010 in
Bogota, Colombia.
Bogota, Colombia. Infants were included if they had two complete INFANIB results at 3 or 6
Tel: +57 1 2210731 |
Fax: +57 1 2210731 | or 9 months of CA and at 12 months of CA, including the Griffiths Scale. The outcome was
Email: ncharpak@gmail.com defined as the presence of a neurological abnormality, as evidenced by the results of both
Received the INFANIB and Griffiths Scale.
26 July 2015; revised 3 January 2016; Results: The sensitivity of the INFANIB at 3 months was 62.2%, and specificity was 76.1%,
accepted 18 February 2016.
with a receiver operating characteristic (ROC) area of 0.69. At 6 months, the results were
DOI:10.1111/apa.13377 77.5% for sensitivity and 74.4% for specificity (ROC 0.76), and at 9 months, they were
77.2% for sensitivity and 91.1% for specificity (ROC 0.84).
Conclusion: The INFANIB was an appropriate neurological screening test with regard to
determining which Colombian infants would benefit from a timely intervention for
neuromotor disorders.

INTRODUCTION neurodevelopment keeps evolving and infants that are


Advances in neonatal care during the last decade have apparently normal at a given age can demonstrate abnor-
increased the survival of premature infants. Those surviving malities in future evaluations (7,10,11). A systematic
prematurity and extreme prematurity are high-risk infants neurological evaluation by a neuropaediatrician is expen-
facing significant risks for somatic growth and neuropsy- sive and not readily available, particularly in resource-
chomotor development abnormalities, as well as the pres- restricted settings. To ration resources and maximise ben-
ence of chronic diseases during their lifetime (1). The most efits for high-risk infants, it is necessary to identify a
frequently diagnosed neurological disorders are motor simplified but effective and valid assessment tool that is able
impairments (1–4) such as cerebral palsy and developmen- to promptly detect abnormal results in the neurological
tal coordination disorders that can generate high levels of
disability and dysfunction in the life of affected infants and
their families.
Postdischarge high-risk follow-up during the first year
Key notes
should systematically evaluate the neurological develop-
 This study assessed the discriminative ability of the
ment with the purpose of early identification of neuromotor
Infant Neurological International Battery (INFANIB),
alterations, resulting in timely intervention and treatment
applied at 3, 6 and 9 months of corrected age (CA),
(3,5–6,8–11). Periodic evaluation is fundamental given that
on neurological outcomes at 1 year of CA.
 An observational analytic study was conducted on a
Abbreviations cohort of 5857 infants in a Kangaroo Mother Care
CA, Corrected age; INFANIB, Infant Neurological International programme in Bogota , Colombia.
Battery; IVH, Intraventricular haemorrhage; KMC, Kangaroo  The INFANIB proved useful in determining which
Mother Care; KMCP, Kangaroo Mother Care programme; LBW, infants would benefit from timely intervention for
Low birth weight; NICU, Neonatal intensive care unit; ROC,
neuromotor disorders.
Receiver operating characteristic.

©2016 Foundation Acta Pædiatrica. Published by John Wiley & Sons Ltd 2016 105, pp. e195–e199 e195
Neurological screening of high-risk infants Charpak et al.

examination, leading to a timely intervention and referral to Eligible subjects were preterm and/or LBW infants at a
a neuropaediatrician. KMC outpatient clinic in Bogota , from hospital discharge
A number of reliable measurement scales used for up to 1 year of CA, between the years 1993 and 2009. The
assessment, screening and diagnostic purposes for neuro- patients had complete information regarding their neuro-
logical disorders have been widely used in high-risk infants logical outcome at 1 year of CA, namely the Griffiths
(12–14). Most of these instruments are time-consuming and Mental Development Scale and the INFANIB evaluation,
need specialised training for application. However, the and information regarding at least two of three possible
Infant Neurological International Battery (INFANIB) is a neurological evaluations at 3, 6 or 9 months of CA with the
standardised neuromotor examination, which is less time- INFANIB.
consuming and easily fits into the routine of a paediatric The excluded patients were those with incomplete or
evaluation. invalid information on their neurological evaluation at
The INFANIB was developed by Ellison (15) and was 1 year of CA or those with severe sensorial impairment,
designed to provide information on age-specific motor such as blindness and deafness, which would hamper the
development impairment during the first 18 months of life performance and interpretation of the gold standard
and to identify which infants could benefit from early tests. On this basis, we excluded 624 infants. The sample
intervention. The INFANIB consists of the assessment of was composed of all eligible infants during the study
five factors: spasticity, head and trunk, vestibular functions, period.
legs and French angles. This study assessed the performance of the INFANIB in a
At the Kangaroo Mother Care programme (KMCP) in KMC outpatient clinic in real-life circumstances in which
Bogota , Colombia, the INFANIB has been used as a different paediatricians administered the test and different
neuromotor simplified evaluation tool since 1993 for providers undertook physical therapy. During the standard
premature and/or low birthweight (LBW) infants (16). In KMC follow-up, all subjects had an INFANIB test admin-
our KMCP, INFANIB scores were assigned according to istered by a paediatrician at the visits at 3, 6, 9 and
the corrected age (CA) for gestational age at birth. 12 months of CA and the results were registered in their
During each INFANIB test administration, the infant was clinical records. Infants were classified as normal, tran-
classified as abnormal, transiently abnormal or normal. siently abnormal or abnormal, according to the obtained
Infants with abnormal and transient results subsequently INFANIB score for their CA, using the cut-off points
received physical therapy and additional care as needed, published by the test developers (15).
such as diagnostic tests and images and referrals to INFANIB can be used in children from 40 weeks of
specialists. gestational age onwards, evaluating global motor develop-
To date, no comprehensive assessment of a strategy based ment, tone and primitive reflexes and assessing up to 20
on the routine administration of the INFANIB has been items in five factors (Table 1). Furthermore, during the
reported in the Colombian context. These results could be yearly visit, a properly trained infant psychologist applied
used to inform decisions about the use of the INFANIB in the Griffiths Scale for assessing psychomotor development,
all follow-up programmes of high-risk infants in Colombia, which generated an overall score and specific scores for five
particularly in countries with similar profiles in the Latin domains, most of which were affected by any motor
American and Caribbean region. impairment (17).
The objective of the study was to assess the ability of the
INFANIB test, performed at 3, 6 and 9 months of CA, to
discriminate neurological status at 1 year of CA in normal,
abnormal or transient preterm and/or LBW infants, allow- Table 1 Factors and items evaluated by the INFANIB scale
ing for a timely intervention when needed. Factors Items

Factor I Hands Tonic Tonic Asymmetric


METHODS Spasticity held labyrinthine labyrinthine tonic neck
A historical cohort study was assembled to evaluate the open or in supine in prone reflex
closed
performance of the INFANIB, a neurological screening
Factor II Body All fours Pulled to Sitting
tool. All risk factors related to inadequate neurological
Head and derotative sitting
examination results at 1 year were collected: birth weight trunk
gestational age at birth; acute foetal distress, which was Factor III Body Sideways Forward Backwards
defined as abnormal monitoring before delivery; oxygen Vestibular rotative parachute parachute parachute
dependency, which was defined as more than 28 days of Factor IV Positive Dorsiflexion Foot grasp Standing
oxygen requirement; neonatal intensive care unit (NICU) Legs support of the foot
admission; length of NICU stay; intrauterine growth reflex
restriction, defined as a weight below the 10th percentile Factor V Abductor’s Popliteal Heel-to-ear Scarf sign
for the gestational age; asphyxia at birth, defined as an French angle angle
angles
Apgar score of less than three at five minutes, and
intraventricular haemorrhage (IVH) of any grade.

e196 ©2016 Foundation Acta Pædiatrica. Published by John Wiley & Sons Ltd 2016 105, pp. e195–e199
Charpak et al. Neurological screening of high-risk infants

Data processing and analysis The neurodevelopmental outcome at 1 year of CA can be


The main outcome was the discriminant ability defined as seen by the distribution of both the Griffiths Scale and
the sensitivity, specificity and area under the receiver the INFANIB score results at 1 year of CA (Table 3).
operator characteristics (ROC) curve of the INFANIB test The discriminant ability of the INFANIB evaluations at
applied at 3, 6 and 9 months of CA, as compared to the 3 months was normal in 4326 of 5812 infants (73.9%)
neurological status, which is the gold standard, using the transiently abnormal in 1438 (24.6%) and clearly abnormal
results of both the Griffiths Scale and the INFANIB score in the remaining 48 (0.8%) subjects. At 6 months, 4185 of
obtained at the 1 year of CA visit. 5801 (71.5%) infants were normal and 1532 (26.2%) and
The Griffiths Scale overall score was dichotomised into 84 (1.4%) were transient and abnormal, respectively. At
normal (≥90) and abnormal (<90), and the INFANIB’s 9 months, normal, transient and abnormal results were
three categories were reduced to two, normal and abnor- 5142 of 5833 (87.8%), 609 (0.4%) and 82 (1.4%),
mal, the latter including both transient and abnormal respectively.
results. A neurological evaluation at 1 year of CA was A total of 256 infants (4.4%) had abnormal neurological
classified as normal when both tests were normal. Any results at 1 year of CA. NICU admission, IVH, birth
abnormal results in either test classified the subject as asphyxia, weight and gestational age at birth were indepen-
abnormal at 1 year of CA. dently related to the outcome (chi-square p = 0.000).
Data were analysed using Stata/MP version 11 (Stata The sensitivity of the INFANIB at 3 months was 62.2%,
Corporation, College Station, TX, USA). with a 95% confidence interval (CI) of 55.8–68.2, specificity
The study was reviewed and approved by the Scientific of 76.1% (74.9–77.2) and an ROC area of 0.69 (0.66–0.72).
Committee of the Kangaroo Foundation. The study was At 6 months, sensitivity and specificity were 77.5%
considered to pose minimal risk, and anonymity of the data (71.8–82.5) and 74.4% (73.2–75.5), respectively, with an
was guaranteed. ROC area of 0.76 (0.73–0.78). At 9 months, sensitivity was
77.2% (71.5–82.2), specificity was 91.1% (90.4–91.9), and
the ROC area was 0.84 (0.81–0.87). The sensitivity of the
RESULTS INFANIB increased at the expense of specificity at three,
The analysis included 5857 study participants who had a six and most notably at 9 months in high-risk groups: at
complete neuromotor evaluation at 1 year of CA and who 9 months, IVH rose to 96%, neonatal anoxia to 97.4%,
had information on at least two INFANIB evaluations at 3, birthweight under 1000 g to 93% and gestational age of up
6 or 9 months visits. There were 5812 (99.2%), 5801 (99%) to 30 weeks to 87%. The discriminant ability of test results
and 5833 (99.5%) INFANIB tests available at 3, 6 and at each test age is described in Table 4.
9 months, respectively. The main characteristics of the
study participants are described in Table 2.
DISCUSSION
The results of the present study appear to confirm that early
evaluation with INFANIB may have an acceptable discrim-
Table 2 General characteristics of study participants inant ability to classify neurological outcome at 1 year of
Characteristic No (%) Mean (Min–Max) age.
Soleimani et al. (18) reported the evaluation of the
Birthweight (g) 1795.5 (500–2687)
INFANIB as a screening tool for the early detection of
Categorical birthweight (g)
<1000 g 269 (4.6) gross motor developmental delay in Iran. The study
1000–1500 g 1085 (18.5) reported 90% sensitivity and 83% specificity in infants of
1501–2000 g 283 (48.4) four to 18 months, and it concluded that the INFANIB was
>2000 g 1668 (28.5)
GA at birth (week) – 33.7 (25–41)
Categorical GA at birth (weeks)
<30 738 (12.6) Table 3 Classification of neurodevelopmental status according to the results of
31–32 860 (14.7) INFANIB and Griffiths Scale at 1 year of CA
33–34 1748 (29.8) Characterization of adverse outcome at 1 year CA No/total (%)
35–36 1922 (32.8)
>37 534 (9.1) Normal result in both tests 5601/5857 (95.6)
C section 4448 (75.9) Infants with abnormal result in the 256/5857 (4.4)
Male 2878 (49.1) neurological evaluation
Acute foetal distress 2044 (34.9) Abnormal result in both tests 45/256 (17.6)
Oxygen dependency 1293 (22.1) Abnormal and a transient result 56/256 (21.9)
Neonatal intensive care unit (NICU) 1495 (25.5) Abnormal and normal result 59/256 (23.0)
Intrauterine growth restriction (IUGR) 1537 (26.2) Griffiths abnormal – INFANIB normal 50/256 (19.5)
Anoxia 759 (32.9) Griffiths normal – INFANIB abnormal 9/256 (3.5)
Intraventricular hemorrhage (IVH) 300 (5.1) Transient result INFANIB – Griffiths normal 96/256 (37.5)

©2016 Foundation Acta Pædiatrica. Published by John Wiley & Sons Ltd 2016 105, pp. e195–e199 e197
Neurological screening of high-risk infants Charpak et al.

Table 4 Discriminant ability of INFANIB at 3, 6, 9 months of CA


Neurologic status at
1 year CA
Area under the Positive Negative
Abnormal Normal Sensitivity % Specificity % ROC curve Predictive Predictive
INFANIB result n n (95% CI) (95% CI) (95% CI) Value (PPV) Value (NPV)

3 months
Non normal (transient + abnormal) 156 1330 62.2 (56; 68) 76.1 (75; 77) 0.69 (0.66; 0.72) 10% 98%
Normal 95 4231
6 months
Non normal (transient + abnormal) 193 1423 77.5 (71.8; 82.5) 74.4 (73.2; 75.5) 0.76 (0.73; 0.78) 12% 98%
Normal 56 4129
9 months
Non normal (transient + abnormal) 196 495 77.2 (71.5; 82.2) 91.1 (90.4; 91.9) 0.84 (0.81; 0.87) 28% 99%
Normal 58 5084

an appropriate screening test in developing countries such The apparent inability of the INFANIB to fully discrim-
as Iran. inate between subjects with and without an abnormal
Liao et al. (19) reported the reliability and predictive neurodevelopment status at 1 year of corrected age can be
validity using the Chinese version of the INFANIB at three, explained by three factors. Firstly, neurodevelopment
seven and 10 months for at-risk infants. They assessed impairment becomes apparent when a function that should
55 preterm and 49 full-term infants with a high risk of mature and appear at a given time falls short when
neurodevelopmental delay, which led them to conclude compared to a standard. Any clinical test, regardless of its
that the INFANIB can be useful for screening infants with a discriminant ability, will fail to identify a sign or symptom
high risk of neuromotor abnormality in Chinese primary that cannot be present when evaluated. Secondly, in our
care settings. study, infants with an abnormal or transient result at any
Sensitivity of the INFANIB was low at 3 months (62%) age were referred for early intervention. Successful inter-
and statistically significantly different from sensitivities at ventions would improve findings at 1 year, and the appro-
6 and 9 months, which were almost identical (77%). priate transient or abnormal result made by the INFANIB
Specificity increased steadily with age, which is a clearly would be incorrectly classified as a false positive. Lastly,
significant trend. The overall discriminating ability – area this was a real-life 15-year study on the performance of
under the ROC curve – also increased steadily with the INFANIB in a healthcare system in which observers
corrected age. changed frequently and those who remained improved their
These observations are consistent with the fact that performance during the study period. This source of intra-
abnormalities in neurodevelopment might originate early, observer and inter-observer variability may explain some of
for instance due to asphyxia at birth, but manifestations the lack of concordance between the INFANIB classifica-
become evident when the affected structures or functions tion and outcome at 1 year. It may also explain why our
should develop. As a consequence, the more mature the estimation of sensitivity was consistently lower than other
infant when the evaluation is performed, the better the reports in the literature, but reflects the usefulness in
discriminant ability of the INFANIB test. clinical practice in a busy facility.
The ideal sensitivity of a screening test should be as close A normal INFANIB result means that the infant should
as possible to 100%. According to this, the INFANIB could continue under close clinical monitoring, while abnormal
be judged as insufficient. Even if the sensitivity of the or transient results prompt intervention. Therefore, the
INFANIB was higher at 9 months than at 3 months, it is proper use of the INFANIB is not to screen or diagnose, but
still not sensitive enough to capture all motor outcomes at to identify infants who are likely to benefit from early
1 year. Specificity at 9 months was very high (>90%), intervention in a timely fashion. In particular, the INFANIB
meaning that an abnormal result was very likely to be a results at 3 and 6 months helped us to identify infants in
true positive finding. need of early intervention, which was reflected in a sharp
The issue is that one cannot diagnose a problem that has decrease in the observed number of abnormal INFANIB
not appeared yet. Neurodevelopment keeps evolving, and results between 6 months (n = 1616) and 9 months
therefore, there are abnormalities that are not present and (n = 691).
are impossible to detect at certain times using screening or One limitation of the study was that we only carried out
confirmatory tests. For example, one cannot evaluate the follow-up until 1 year of CA and this meant that we
vocabulary and numerical reasoning or walking ability at were not aware of other possible outcomes that might have
3 months of age. occurred after the last follow-up. There was also a high

e198 ©2016 Foundation Acta Pædiatrica. Published by John Wiley & Sons Ltd 2016 105, pp. e195–e199
Charpak et al. Neurological screening of high-risk infants

rotation of paediatricians in the KMCP, typical of a 5. Beckung E, Hagberg G, Uldall P, Cans C. Probability of walking
developing country setting. Nevertheless, the INFANIB in children with cerebral palsy in Europe. Pediatrics 2008; 121:
was shown to be an easily applicable neurological screening 187–92.
6. Taylor F, National Institute of Neurological Disorders and
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Stroke (U.S.), Office of Science and Health Reports. Cerebral
palsy: hope through research. Bethesda, MD: The Institute,
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Periodic INFANIB testing was informative and was easily dysfunction: perspectives emerging from a review of data of the
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8. De Graaf-Peters VB, Hadders-Algra M. Ontogeny of the human
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the test means that an abnormal or transient result will 10. Developmental surveillance and screening of infants and young
children. Pediatrics 2001; 108: 192–6.
enable clinicians to carry out timely interventions to try and
11. Rosenbaum PL, Missiuna C, Echeverria D, Knox SS. Proposed
prevent neuromotor disorders. Therefore, the proper use of motor development assessment protocol for epidemiological
the INFANIB is to identify infants likely to benefit from studies in children. J Epidemiol Community Health 2009; 63:
early intervention in a timely fashion. 27–36.
12. Lee LLS, Harris SR. Psychometric properties and
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ACKNOWLEDGEMENTS and young children: a review. Pediatr Phys Ther 2005; 17:
We are grateful to Dr Juan Gabriel Ruiz for his advice and 140–7.
13. Glascoe FP. Screening for developmental and behavioral
comments on this article.
problems. Ment Retard Dev Disabil Res Rev 2005; 11: 173–9.
14. Heineman KR, Hadders-Algra M. Evaluation of neuromotor
function in infancy-A systematic review of available methods.
FINANCIAL DISCLOSURE J Dev Behav Pediatr 2008; 29: 315–23.
There are no financial statements to disclose. 15. Ellison PH, Horn JL, Browning CA. Construction of an Infant
Neurological International Battery (INFANIB) for the
assessment of neurological integrity in infancy. Phys Ther 1985;
COMPETING INTERESTS 65: 1326–31.

16. Charpak N, Ruız JG, Angel MI, Duque JS, Garcıa C.
The authors have no conflict of interests to declare.
Lineamientos tecnicos para la implementacio  n de Programas
Madre Canguro en Colombia. Ministry of Health and Social
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©2016 Foundation Acta Pædiatrica. Published by John Wiley & Sons Ltd 2016 105, pp. e195–e199 e199

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