Infant Behavior and Development 49 (2017) 70–82

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Infant Behavior and Development

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

Microcephaly and Zika virus: Neuroradiological aspects, clinical MARK

findings and a proposed framework for early evaluation of child
development
⁎
Nelci Adriana Cicuto Ferreira Rochaa, , Ana Carolina de Camposa,
Fellipe Cicuto Ferreira Rochab, Fernanda Pereira dos Santos Silvaa
a
Department of Physical Therapy, Child Development Analysis Laboratory (LADI), Federal University of São Carlos (UFSCar), Rodovia Washington
Luis, km 235, São Carlos, SP, 13565-905, Brazil
b
Medical School, Pontifical Catholic University of Campinas (PUC-Campinas), Av. John Boyd Dunlop, s/n – Jardim Ipaussurama, Campinas, SP,
13060-904, Brazil

AR TI CLE I NF O AB S T R A CT

Keywords: Background and aims: As the recent outbreak of microcephaly cases caused by Zika virus has been
Microcephaly declared a global health emergency, providing assessment guidelines for multidisciplinary teams
Zika virus providing early developmental screening and stimulation to infants with microcephaly is much
Early development needed. Thus, the aim of this manuscript is to provide an overview on what is known about
Infant
neuroradiological aspects and clinical findings in infants with microcephaly caused by Zika virus
International Classification of Functionality
and to propose a framework for early evaluation of child development.
Disability and Health
Methods: The keywords “Zika virus” and “microcephaly” were searched in PubMed database for
articles published from incept to May 2017. These texts were reviewed, and the ones addressing
neuroradiological and clinical findings in infants were selected. Recommendations for early as-
sessment were made based on the International Classification of Functionality Disability and
Health (ICF) model.
Outcomes and results: The database search yielded 599 publications and 36 were selected. The
studies detected microcephaly with diffuse brain malformations and calcifications, ven-
triculomegaly, optic nerve hypoplasia, macular atrophy, cataracts, impaired visual and hearing
function, arthrogryposis, spasticity, hyperreflexia, irritability, tremors, and seizures, but very
little is known about early development. Early assessments were described based on the ICF
domains (Body Function and Structures, Activities and Participation and Contextual factors).
Conclusion and implications: Studies published showed abnormal brain, optic, neurologic and
orthopedic findings, but very little is known about other aspects of functioning in infants with
microcephaly caused by Zika virus. The biopsychosocial model based on the ICF paradigm
provides an adequate framework to describe the condition of the infant with microcephaly re-
ceiving rehabilitative efforts to minimize disability. Efforts towards early identification of de-
velopmental delays should be taken within the first six months of life.

1. Introduction

Microcephaly is usually defined as a developmental defect of the brain, characterized by a significant reduction in the occipital-

⁎
Corresponding author at: Rua: José Riga, n.310 - Residencial Samanbaia, São Carlos, SP, 13565-560, Brazil.
E-mail address: acicuto@gmail.com (N.A. Cicuto Ferreira Rocha).

http://dx.doi.org/10.1016/j.infbeh.2017.07.002
Received 1 September 2016; Received in revised form 30 May 2017; Accepted 14 July 2017
0163-6383/ © 2017 Elsevier Inc. All rights reserved.
N.A. Cicuto Ferreira Rocha et al. Infant Behavior and Development 49 (2017) 70–82

frontal head circumference (HC) at birth (Opitz & Holt, 1990) of at least 2 standard deviations (SD) below the mean for gestational
age and gender (Ashwal, Michelson, Plawner, & Dobyns, 2009; Mochida, 2009; Thornton & Woods, 2009).
Microcephaly can be categorized as either congenital (primary) or of postnatal onset (secondary) (Ashwal et al., 2009;
Gilmore & Walsh, 2013; Seltzer & Paciorkowski, 2014; Woods & Parker, 2013). Primary microcephaly may occur especially by 34
weeks of gestation (Woods & Parker, 2013), and may be caused by reduced neuronal proliferation or accelerated apoptosis, leading to
simplification of the gyral pattern (Barkovich, Guerrini, Kuzniecky, Jackson, & Dobyns, 2012). Other forms of microcephaly are
consistently associated with abnormal brain structure due to failure in neuronal migration in the 3rd–5th month of gestation (mi-
crolissencephaly, lissencephaly, schizencephaly, pachygyria, polymicrogyria) (Volpe, 2001). The causes are numerous, including
genetic, syndromic, disruptive injuries, exposure to toxic substances during pregnancy, severe maternal malnutrition/deprivation
(Baptista, Quaghebeur, & Alarcon, 2016; Woods & Parker, 2013), and intrauterine infections, such as toxoplasmosis, rubella, cyto-
megalovirus, herpes simplex and syphilis (Ashwal et al., 2009). Secondary microcephaly refers to acquired insults of the central
nervous system (CNS) or to progressive metabolic/genetic disorders apparent in the first 1–2 years after birth (Ashwal et al., 2009;
Gilmore & Walsh, 2013; Seltzer & Paciorkowski, 2014; Woods & Parker, 2013). It may be caused by disruptive injuries, infections,
deprivation or genetic disorders affecting postnatal brain growth (Ashwal et al., 2009; Woods & Parker, 2013).
Currently, the Zika virus (ZikaV), a flavivirus transmitted by several species of Aedes mosquitoes, has been associated with an
increased incidence of microcephaly in endemic areas in the Northeastern states of Brazil (Nunes et al., 2016).
The history of a ZikaV outbreak in Brazil in 2015 and the notifications of an unusual increase in microcephaly cases (Victora et al.,
2016) have motivated studies aiming to identify a possible causal relationship between microcephaly and ZikaV infection
(Rasmussen, Jamieson, Honein, & Petersen, 2016). Evidence supporting this hypothesis includes the temporal and geographic as-
sociation between the ZikaV outbreak and the cases of microcephaly (Oliveira Melo et al., 2016; Rasmussen et al., 2016). The
Brazilian Ministry of Health (MOH) issued an epidemiology bulletin confirming 1.271 cases of microcephaly and others alterations in
CNS from October 2015 to April 2016, suggesting congenital infection as the probable cause. Similar temporal association has also
been identified in Colombia during epidemiologic weeks (January 31–November 12) in 2016 (Cuevas et al., 2016).
Several studies have supported a causal relationship between ZikaV infection and brain abnormalities. In humans, ZikaV RNA was
detected in amniotic fluid (Calvet et al., 2016), fetal brain tissue and placenta (Bhatnagar et al., 2017), and in blood and other tissues
(PAHO & WHO, 2015), indicating that Brazilian ZikaV crosses the placental barrier causing microcephaly. Recent experimental
studies by Garcez et al. (2016) and Souza et al. (2016) demonstrated that ZikaV induces cell death in human neural stem cells,
disrupts the formation of neurospheres, reduces the growth of organoids and reduces cell proliferation. Furthermore, ZikaV seems to
infect preferentially more precursor cells than neurons (Retallack et al., 2016), indicating that infection in the first trimester of brain
development may result in severe damage. Evidence from an animal model showed ZikaV genomic RNA in several tissues of newborn
mice, especially in the brain, with findings of cortical malformations, reduced cell number and cortical layer thickness, whole-body
growth delay, intra-uterine growth restriction, lower skull length, cranial height and biparietal diameter (Cugola et al., 2016).
Altogether, these studies support a strong causal relation between ZikaV infection and brain abnormalities and reinforce the idea
that ZikaV not only causes microcephaly, but a congenital syndrome. Although there is confirmation of affinity of ZikaV to brain
tissue (Tang et al., 2016), other studies are necessary to further characterize the consequences of ZikaV infection during different
stages of fetal development and post natal.
This critical review has been motivated by the alarming scenario of microcephaly caused by ZikaV in Brazil, and the urgent need
to identify the main clinical findings in infants so developmental delays can be detected early. Thus, the aims of this study are to
provide an overview on what is known about neonatal neuroradiological aspects and clinical findings in infants with microcephaly
caused by ZikaV, and to propose a framework for early evaluation of child development.
The Center for Diseases Control (CDC) has recently published recommendations for the evaluation and management of infants
with possible congenital ZikaV infections (Russell et al., 2016). However, the guidance emphasizes the biomedical model of disease,
with a focus on laboratory testing and clinical evaluation. It is known that field of pediatric rehabilitation has undergone major
conceptual changes in the past few decades with the introduction of a new framework to explain human functioning, provided by the
ICF (Camargo, 2016). The ICF uses a biopsychosocial approach to describe functioning and disability as the dynamic interactions
between body functions/structures, activities and participation domains. Contextual factors such as environmental and personal
factors also have major influence on disability and health (WHO, 2001). The main implication of this new framework is that the
traditional biomedical model, which focuses on disability, abnormality and limitation, no longer meets the health professionals’
needs towards understanding the complexity of individual’s lives. In this context, current assessment and rehabilitation approaches
should take biopsychosocial factors into account in order to promote optimal capacity and full participation of the individual in all
aspects of life (dos Santos, Pavão, de Campos, & Rocha, 2012; Palisano et al., 2012; Rosenbaum & Gorter, 2012).
The surveillance status recommended by the WHO due to the unknown features of ZikaV infection requires the implementation of
precautionary and preparatory measures. Among these measures, a central point is to design a framework to be used by multi-
disciplinary teams when providing developmental screening and stimulation to infants with microcephaly. Therefore, in this review,
the International Classification of Functioning, Disability and Health (ICF) model will be used as guidance for clinicians and re-
searchers to identify relevant outcomes during assessment that will support early intervention planning and family-centered actions.

2. Methods

This was a non-systematic review article conducted by a panel of experts. The keywords “Zika virus” and “microcephaly” were
searched in PubMed database for articles published from incept to May 2017. Manuscripts were excluded if they addressed the

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pathogenesis of ZikaV; mechanisms of infection; epidemiological or molecular aspects; if animal models were used; and if they were
review studies. Manuscripts were considered relevant if they reported neonatal neuroradiological aspects and/or clinical findings in
infants with microcephaly related to ZikaV. The main findings of these studies were summarized and described in the Results section.
Measurement tools addressing all ICF domains that are applicable and relevant to infants with microcephaly were selected based
on in systematic reviews (Pavao, Silva, Dusing, & Rocha, 2017; Schiariti et al., 2014; Silva, 2016). Additional assessments addressing
particular aspects of this condition were recommended based on guidelines from de Center for Diseases Control (Russell et al., 2016).

3. Results and discussion

The database search yielded 599 publications. These texts were reviewed, and 36 articles were selected that addressed neuror-
adiological aspects and clinical findings. Their results were summarized and described below. Additional recommendations for early
assessment will be made based on the ICF model.

3.1. Neuroradiological findings

Fetal autopsy and neuroimaging in infants detected microcephaly with diffuse cerebral cortical thinning, polymicrogyria, pa-
chygyria or lissencephaly; hemimegaloencephaly, ventriculomegaly, hypoplasia of the corpus callosum, cerebellum and brainstem,
calcifications in the cortex and sub-cortical white matter in the frontal, parietal, and occipital lobes and basal ganglia (Besnard et al.,
2016; Culjat et al., 2016; Carvalho et al., 2017; Cavalheiro et al., 2016; de Fatima Vasco Aragao et al., 2016; Driggers et al., 2016;
Guillemette-Artur, Besnard, Eyrolle-Guignot, Jouannic, & Garel, 2016; Hazin et al., 2016; Mlakar et al., 2016; Martines et al., 2016;
Rocha et al., 2016; Sarno et al., 2016; Soares de Oliveira-Szejnfeld et al., 2016; Sousa et al., 2017; Štrafela et al., 2016; Vesnaver et al.,
2017; Werner et al., 2016), and pontine atrophy (Štrafela et al., 2016).
Visual findings included optic nerve hypoplasia and macular atrophy, microphthalmia, and cataracts (Campos, Lira, & Arantes,
2016; Schuler-Faccini et al., 2016; Ventura, Maia, Bravo-Filho, Góis, & Belfort, 2016), low visual acuity regardless of retina and/or
optic nerve abnormalities (de Paula Freitas et al., 2016; Ventura, Maia, Ventura et al., 2016); chorioretinal abnormalities (de Paula
Freitas et al., 2016; Miranda et al., 2016; van der Linden et al., 2016) and a spectrum of pigmentary retinopathy, torpedo and
torpedo-like maculopathy, vascular absence, and hemorrhagic retinopathy (Miranda et al., 2016). Reports of pulmonary hypoplasia
and lymphocytic infiltration in liver and lungs confirmed not only virus neurotropism, but also multiple organ infection (Sousa et al.,
2017).
These imaging studies and findings reinforce the need for a comprehensive neuroradiological investigation in infants with mi-
crocephaly, which will be helpful in further assessment of areas involved with the infection.

3.2. Clinical findings

Before the appearance of ZikaV as a causal factor of neurological dysfunction, retrospective reviews had found that children with
microcephaly are at risk for developmental disability and that there is a correlation between the degree of microcephaly and the
severity of cognitive impairment (Ashwal et al., 2009; Dolk, 1991; Mahmood, Ahmad, & Hassan, 2011). Currently, Schuler-Faccini
et al. (2016) emphasize that the consequences of microcephaly depend on underlying brain anomalies and can range from mild
developmental delays to severe motor and intellectual deficits. These and several other authors (Carvalho et al., 2016; Moura da Silva
et al., 2016; van der Linden et al., 2016) have shown abnormal neurologic findings, such as spasticity, hyperreflexia, irritability,
tremors, and seizures. Dysphagia (van der Linden et al., 2016) and low birth weight (Abreu, Novais, & Guimarães, 2016) were also
reported. Most of the newborns presented low birth weight (< 2500 g), that is the single most important risk factor for childhood
morbidity and mortality. It can inhibit growth and cognitive development, bringing on appearance of chronic diseases during life
(Abreu et al., 2016).
Regarding hearing testing, although van der Linden et al. (2016) have reported normal findings in a sample of 11 infants with
microcephaly, Leal et al. (2016) have shown sensorineural hearing loss in 6% of a sample of 60 infants with microcephaly, prevalence
similar to that seen in association with other congenital viral infections. Ocular involvement in infants with presumed ZikaV con-
genital infection were more often seen in infants with smaller cephalic diameter at birth and in infants whose mothers reported
symptoms during the first trimester (Ventura, Maia, Ventura et al., 2016).
Regarding head circumference, based on these review findings, it is not possible to rely on this measure as the major hallmark for
altered brain development among infants with evidence of ZikaV infection. While several studies have clearly shown the high
incidence of reduced head perimeter (Chimelli et al., 2017; França et al., 2016; Moura da Silva et al., 2016; Vargas et al., 2016), there
are reports of normal head circumference (Adhikari et al., 2017) in infants with possible ZikaV infection; several other brain ab-
normalities may be seen in the absence of microcephaly (França et al., 2016; Soares de Oliveira-Szejnfeld et al., 2016), besides
morphologic changes typical of microcephaly with normal head circumference (Sousa et al., 2017). Moreover, van der Linden et al.
(2016) have documented decelerated head growth as early as 5 months of age. These findings indicate the need for a more precise
assessment of cranial characteristics and recommendation developmental follow-up, even in the absence of altered head cir-
cumference.
Arthrogryposis was reported in several studies (Chimelli et al., 2017; Martines et al., 2016; Melo et al., 2016; Sarno et al., 2016;
Sousa et al., 2017), often present in both arms and legs; additional orthopedic findings included bilateral hip dislocation, and
subluxation of the knee associated with genu valgus (van der Linden et al., 2016).

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Based on these results, although there is some information on neurodevelopmental disability in infants with microcephaly, very
little is known about early development. It is of especial relevance that future studies also inform about functioning and the role of
contextual factors in this population, as described in the ICF, in order to guide preventative and rehabilitative services that might
improve outcomes.

3.3. An assessment framework based on the biopsychosocial model

Under the biopsychosocial framework, as many of the daily experiences children have are within the family context, assessment
should be based on patient and family needs and intervention should have an empowering focus on functional independence and
quality of life (Rosenbaum & Gorter, 2012). To properly address the complex needs of the child and his or her family, a multi-
disciplinary team is required to work together (Howle, 2002).
These aspects become of even greater importance in the face of new challenges such as the recent outbreak of microcephaly cases
recently observed in Brazil. A global health emergency of this magnitude (Heymann et al., 2016) requires that policy makers, health
care professionals and society act together to promote the best quality of life for individuals with microcephaly and their families, and
also to decrease the impact of this condition on the public health system. The surveillance status recommended by the WHO due to
the unknown features of ZikaV infection requires the implementation of precautionary and preparatory measures. Among these
measures, a central point is to design a framework to be used by multidisciplinary teams when providing developmental screening
and stimulation to infants with microcephaly.
There is evidence in the literature supporting the need for the earliest possible intervention for infants at high risk for neuro-
disability, the main reason being to take advantage of the remarkable brain plasticity during the first few months of life. In a
systematic review, Blauw-Hospers and Hadders-Algra (2005) have found substantial evidence for developmental programs to pro-
duce a positive effect on motor development. It is therefore highly recommended a shift from acting after impairments are seen to a
referral as soon as the risk is detected (McIntyre, Morgan, Walker, & Novak, 2011). According to Herskind, Greisen, and Nielsen
(2015), early interventions should be initiated within the first 6 months after term age. Thus, appropriate assessment should be
delivered and early intervention cannot be delayed!
Following the biopsychosocial approach, guidelines for assessment of infants with microcephaly based on the ICF dimensions are
suggested in Fig. 1.

3.3.1. Assessing activities and participation

It is highly recommended that assessment begins looking first at the Activities and Participation domains, because this will inform
about the infant’s functionality. Evaluation in infants during the first 6 months of life should include the involvement in life situa-
tions, and the description of his or her capacity and performance. Capacity describes what a child does in his or her current en-
vironment with some personal help or with the use of assistive devices, for example sitting with the use of adapted chair or visual
tracking with the use of high contrast objects. The performance qualifier describes an individual’s ability to execute a task or an action
without any personal help (WHO, 2001).
During the assessment, it is important to describe what the infants do and how they are doing. Thus, performance and capacity
should be described including motor activities as indicated in Table 1 (Bly, 1994; Campbell, 2001). It is important that health care
professionals have a thorough knowledge about typical child development, especially the neurosensory and biomechanics changes in
the first months of life to identify early atypical patterns of movements and stereotypies.
Self-care activities appropriate for the developmental stage should also be checked, such as offering a leg or arm in anticipation of
dressing, maintaining a level of interest and motivation to engage in the interaction (Howle, 2002), holding the bottle, extending
hands to be washed or to be picked up, allowing to have nose wiped, eating mashed food and quality of parent–child interactions and
relationships.
Objective description may require the use of standardized tools to register the limitation or restriction between the observed and
the expected performance.
Developmental monitoring and screening can be done by a number of health care professionals, at clinical, community, and
school settings. Using standardized tools prevents that different professionals are inconsistent in their referral patterns for children
with possible developmental delays (Radecki, Sand-Loud, O’Connor, Sharp, & Olson, 2011). When using a validated assessment tool,
professionals can be assured that it measures what it purports in a specific population and that it is reliable (Kimberlin & Winterstein,
2008).
There are numerous assessment scales, however, we will highlight the most used and suitable tools, which have good psycho-
metric indices in the assessment of children up to 6 months, detecting delays early on (Table 2). Early detection is important as it
allows referral to early interventions aimed at maximizing motor and cognitive outcomes in children and providing support to
families (McIntyre et al., 2011).
After assessing the capabilities and functional limitations, it is necessary to identify the deficiency of the systems, based on the
dimensional of body structure and function.

3.3.2. Assessing body function and structures

After identifying the functional limitations in the Activities and Participation dimension, it is necessary to identify impairments in
the body systems, based on the ICF dimension of body structure and functions. It is important to highlight that, besides the afore-
mentioned conceptual changes in the models of human functioning, theoretical and scientific progresses have also transformed the

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(caption on next page)

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Fig. 1. Overview of International Classification of Functioning, Disability and Health (ICF) domains and corresponding assessment tools.
Legend – MHO: Ministry of Health; PAHO: Pan American Health Organization; WHO: World Health Organization; ROM: Range of Movement; TU: Transcranial
Ultrasound; MRI: Magnetic Resonance Imaging; CT: Computed Tomography; MAI: Movement Assessment of Infants; GMs: General Movements Assessment; HINE: The
Hammersmith infant neurologic exam, Bayley: Bayley Scales of Infant and Toddler Development; TIMP: Test of Infant Motor Performance; AIMS: Alberta Infant Motor
Scale; NSMDA: Neuro-Sensory-Motor Development Assessment; LIFE-H: Assessment of Life Habits; DMC: Dyadic Mutuality Code; HOME: Home Observation for
Measurement of the Environment; NCATS: Nursing Child Assessment Teaching Scale. *Precaution: the AIMS should not be used if the infant is diagnosed with a severe
motor disorder involving abnormal patterns of movement.

Table 1
Main items observed throughout the first 6 months of life.

Head and trunk control Upper and Lower Extremities Abilities

- Head and neck position (midline orientation,
symmetry or asymmetry, amount of attempts or
time sustaining head upright) and active rotation
in different positions (i.e., suspensions, forward
and backward inclinations) and support
conditions (i.e, with high, middle and low trunk
support or hold by hands);
- Visual and auditory tracking in different positions
(visually attends, degrees of movement and
speed);
- Control of weight shift during head and body
movement;
- Weight bearing base and area;
- Active trunk rotation in different positions with and
without stimulation;
- Postural reactions when pulled to sit and lowered
from sitting (if attempts to assist with head or
arms; head and trunk with symmetrical
antigravity flexor and extensor muscle control);
-Postural stability/equilibrium in prone (observed by
reaching, grasping, pivoting, swimming posture),
supine (observed reaching, grasping, hands to the
feet, feet to the mouth), sitting (uses hands to
maintain unsupported sitting or sits erect without
support) and standing (maintains the upright
position by being held by the hands).
- Observe position and individual movement of
each joint, in different body positions
(spontaneous and elicited movements);
- Symmetrical mirroring of extremity activities;
- Acquisition of dissociated movement with
weight shifting control in prone and supine, but
sits using a ring position of the lower extremities
for stability;
- Control of antigravity extension, flexion and
rotation;
- Shoulder girdle and upper extremity muscle
control during the execution of motor skills;
- Increased active pelvic mobility and lower
extremity control during the execution of motor
skills;
- Forearm weight bearing in prone;
- Extended arm weight bearing in prone and
sitting associated with head and trunk control;
- Observed patterns of task-related movement
and posture.
- Hand-mouth coordination;
- Hand-hand coordination;
- Hands in different parts of body (bring the hands
to face, belly, knee, hands to feet, feet to the
mouth);
- Eye-hand coordination (unimanual and bimanual
reaching in different postures);
- Grasping;
- Amount, quality and kind of exploration with
objects of different properties (mouthing, visual or
hand exploration, i.e., grasping, shaking,
transferring the toy to the other hand);
- Reciprocal kicking;
- Rolling to side lying (symmetric or asymmetric
trunk and extremities);
- Rolling from supine to prone and vice-versa;
- Pivoting in prone (first displacement of body in
space);
- Beginning bouncing.

focus of developmental assessment and intervention. Current approaches to infant development do not emphasize the hierarchical
nature of the CNS nor neuromaturation as the main event leading to developmental changes. Rather, the role of multiple factors is
acknowledged, which is in line with a more comprehensive view of human functioning. In this context, the exam of muscle tone and
primitive reflexes, although important to inform about brain impairments, is no longer used to guide interventions directed to
promote infant development (Stuberg & Harbourne, 1994).
In areas where Zika virus is present, clinicians should perform ophthalmologic exams on all microcephalic babies, but it is still
unclear whether the eye lesions occur in the absence of microcephaly (McCarthy, 2016). In this way, as head circumference varies by
race, sex, and gestational age (PAHO & WHO, 2015), the World Health Organization (WHO) recommends the use of child growth
standard tables on head circumference for age and gender, with percentiles (available at: http://www.who.int/childgrowth/
standards/hc_for_age/en/). However, there are conflicting opinions regarding the head circumference cutoff values to determine
microcephaly, such as below 2 or 3 SD (Nunes et al., 2016; Woods & Parker, 2013). Given this controversy, additional measures such
as biparietal diameter may provide relevant information, as animal models indicate it may also be reduced due to fetal exposition to
ZikaV (Cugola et al., 2016).
In addition, the clinical and radiological findings described in this review reinforce the need to perform extensive ophthalmo-
logical and hearing testing to exclude visual and hearing impairments. The findings from the review also support the need for
standardized physical and neurological assessment.
Examples of standardized tools to assess domains of Body Structure and Function are shown on Table 3.

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 Table 2
Standardized tools to measure Activities and Participation in infants.

Tool Authors Purpose and Focus Administration Procedures Items tested Scoring system Age Range

TIMP Campbell Early identification of neuromotor
(2001) disturbances by measuring postural
and selective control needed for
functional movement in infancy.
Direct testing or scoring videotaped
tests.
28 observed items of spontaneous
movements such as head centering,
reaching, and individual finger
movements. 31 elicited items that
assess the child’s motor responses to
Observed items: 1 (behavior is 32-weeks’ post-
present) or 0 (behavior not observed conception age to 4
during the test). Elicited items: each months corrected age.
item is scored according to specific
criteria on a rating scale from 0 to 6
N.A. Cicuto Ferreira Rocha et al.

placement in various positions and to (higher score indicates better

visual or auditory stimulation. performance).
NSMDA Burns, Ensbey, To evaluate and document the neuro- Observation of selected tasks or Gross motor and fine motor The item scoring ranged from 1 1–24 months (25 months
and Norrie sensory motor developmental activities, holding the child in performance, neurological and muscle- (definitely abnormal) to 4 (above corrected age).
(1989) integrity and progress of ‘high risk’ specific positions, and providing skeletal status, posture and balance average).
and very low birth weight infants.a specific tactile or proprioceptive reactions and motor response to
input. relevant sensory input. The number of
items drifts in each age group.
AIMS Piper and To evaluate and monitor gross motor Observational tool. The AIMS 58 items divided into 4 subscales: a) Item are scored as either Observed or 0–18 months old
Darrah (1994) function of infants and to assist should not be used if the infant is prone, b) supine, c) sit, d) stand. All Not Observed. Total scores are used
physiotherapists and occupational diagnosed with a severe motor items include analysis of weight to plot a developmental percentile
therapists to measure motor disorder involving abnormal bearing, postural alignment and chart.
development in infants at high risk of patterns of movement. antigravity movements.
motor delay.
Bayley - III Bayley (2005) Developmental milestones Direct testing or video recording of Cognitive Scale: 91 items that assess: Each test item is scored as “passed” or 16 days–42 months
assessment. the assessment. Sensorimotor development, “not passed.” Raw scores for 15 days
Exploration and manipulation, Object cognition, receptive communication,

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relatedness, Concept formation, expressive communication, fine
Memory. motor, and gross motor are converted
Language Scale: 49 items of receptive into a scaled score (a mean of 10 and
communication and 48 items of a SD of 3) and further transformed
expressive communication. into cognitive, language, and motor
Motor Scale: 66 fine motor items, 72 composite scores (a mean of 100 and
gross motor items. a SD of 15).
Social-Emotional Scale: 35 items.
Adaptive Behavior Scale: 241 items.
LIFE-H Noreau et al. To assess the social participation of Three modes: 1) in an autonomous 11 Dimensions of Daily activities Both versions use an item score From birth to 4 years of
(2007) children with disabilities way by the person, a relative or a (Communication, Personal care, ranging from 0 to 9, where 0 age, and from 5 to 13
significant close relation; 2) by the Housing, Mobility, Nutrition, and indicates total impairment (the years of age.
person with the support of a Fitness), and of Social roles activity or social role is not
relative, of a significant other or a (Recreation, Responsibility, accomplished or achieved) and 9
service provider; 3) by a service Education, Community life and indicates optimal social participation
provider. Interpersonal relationships). Version (the activity or social role is
0–4 = 61 items. Long version performed without difficulty and
5–13 = 197 items. without assistance). The measure also
comprises a second scale that
evaluates the individual’s level of
satisfaction with the accomplishment
of life habits: 1 (very unsatisfied) to 5
(very satisfied).
DMC Censullo, To evaluate mutuality in Observations of how the mother 6 global behavior items: mutual All items are scored as 1 or 2 points, 0–6 months.
Bowler, Lester, mother–child interaction. interacts with her infant while attention, positive affect, pauses in with a maximum aggregate score of
and Brazelton playing in a natural way. maternal stimulation, turn-taking, 12. Total scores are rated as low
(continued on next page)
Infant Behavior and Development 49 (2017) 70–82
 Table 2 (continued)

Tool Authors Purpose and Focus Administration Procedures Items tested Scoring system Age Range

(1987) infant clarity of cues, maternal (6–8), moderate (9), and high
sensitive responsiveness. responsivity (10–12 points).
HOME Caldwell and Systematic assessment of the caring Semi-structured interview with the 45 items divided in 6 dimensions: 1) YES or NO. Higher total HOME scores 0–3 years of age.
Bradley (1984) environment in which the child is primary caregiver of the child and emotional and verbal responsivity of indicate a more enriched home
reared. from direct observation of the home the primary caregiver. 2) Avoidance of environment.
environment. restriction and punishment. 3)
N.A. Cicuto Ferreira Rocha et al.

Organization of the physical and

temporal environment. 4) Provision of
appropriate play materials. 5) Parental
involvement with the child. 6)
Opportunities for variety in daily
stimulation.
NCATS Sumner and Assess the quality of the Semi-structured settings and 73 items organized into six subscales. YES or NO. The teaching manual 0–3 years of age.
Spietz (1996) caregiver–child teaching interaction behavior observation. The mother is Four of them assess the caregiver’s provides the user with step-by-step
for children development of the child. required to teach her child how to behavior, such as a caregiver’s scoring instructions. The scores are
play with a novel toy (unfamiliar toy sensitivity to cues, response to the compared to a table provided in the
to her child). child’s distress, fostering of social- manual to determine whether the
emotional growth, and fostering of scores fall under the 10 percentile
cognitive growth. The two child cutoff score.
subscales assess the clarity of the
child’s cues and responsiveness to the
caregiver.
Dunn Dunn (2014) To assess sensory processing skills Parent report measures or interview. 99 items divided into 7 sections: Items are scored on a 1-point to 5- Infant Sensory Profile 2:

77
Sensory and functional performance in Tactile Sensitivity, Taste/Smell point scale. 1 = always: when Caregiver questionnaire
Profile children with disabilities. Sensitivity, Movement Sensitivity, presented with the opportunity, the for babies from Birth to 6
Underresponsive/Seeks Sensation, child responds in the manner months.
Auditory Filtering, Low Energy/Weak, described every time, or 100%, and
and Visual/Auditory Sensitivity. 5 = never: when presented with the
opportunity, the child never responds
in this fashion, or 0%.

Legend – TIMP (Test of Infant Motor Performance); NSMDA (Neuro-Sensory Motor Development Assessment).
a
Besides activity and participation the muscle tone and primitive reflexes testing also informs about Body Function and Structures; AIMS (Alberta Infant Motor Scale); LIFE-H (Assessment of Life Habits); DMC (Dyadic
Mutuality Code); HOME (Home Observation for Measurement of the Environment); NCATS (Nursing Child Assessment Teaching Scale); SD (Standard Deviation).
Infant Behavior and Development 49 (2017) 70–82
 Table 3
Standardized tools to measure infants Body Structure and Functions.

Tool Authors Purpose and Focus Items tested Scoring system Age Range

GMs Einspieler and Early detection of brain dysfunction by NA Characterized as Normal GMs, Poor Up to 2 years
Prechtl (2005) observation of arm, leg, neck and trunk Just observing the movements with the repertoire of GMs, Cramped-synchronized
spontaneous motor activity. unaided eye or by replaying a video GMs, or Chaotic general movements; and by
recording. type to a fidgety movements as Normal,
Absent or Abnormal.
N.A. Cicuto Ferreira Rocha et al.

MAI Chandler, To identify dysfunctions in muscle tone, Muscle tone: 10 items that include passive
Andrews, and primitive reflexes, automatic reactions and motion and observation of infant movements
Swanson (1984) volitional movement. and postures.
Primitive reflexes: 14 items (observed or
elicited);
Automatic reactions: 16 items including
righting, equilibrium and protection
reactions elicited by the examiner;
Volitional movement tests: 25 items with
responses to visual and auditory stimuli and
motor control.
HINE Haataja et al. To detect abnormal neurologic signs, Neurologic signs: 26 items testing cranial
(1999) developmental milestones and behavior. nerve function, posture, movements and
muscle tone; Development of motor function:
8 items testing developmental milestones
and Behavior: 3 items including
consciousness, emotional state and social
Muscle tone: 0–12 months
Primitive reflexes: 1(integrated) to 4
(dominant).
Automatic reactions: 1(complete and
consistent response) to 4 (no response).
Volitional movement: 1 (complete and
consistent response) to 4 (no response).
Items within the neurologic section can be 0–24 months
scored from 0 (absent response) to 3
(complete response); In the developmental
milestones section, diagrams are used to
describe the infant’s performance and the
corresponding developmental age; Behavior

78
orientation. can be scored from 1 (no response) to 6
(complete response).
The neurologicalexaminationof the full- Prechtl and To detect abnormal neurological signs. Neurological exam of Reflexes (e.g., blink, Reflexes and responses are coded from Newborn
term newborn infant Beintema (1964) tonic neck, with drawal, palmar grasp, absent (−) to very strong or exaggerated (+ period
rooting, etc.) and Responses (e.g., Moro, ++);
sucking, traction test,), Muscle tone Resistance against passive motion, power of
(resistance against passive motion, power of active motion and range of movement are
active motion and range of movement) and coded from: floppy (−) to extremely strong
Spontaneous motor activity in prone, supine, resistance (++++);
and upright. Speed (+slow to +++high), Intensity
(+low to +++ very intensive), and amount
of spontaneous movements (+low to +++
high).
Prechtl Behavioural States Prechtl and Used in two connotations: (1) as a descriptive Eyes open or closed. State 1 = Eyes closed, regular respiration, no Newborn
Beintema (1964) categorization of behavior; and (2) as an movements. period
explanation of brain mechanisms which Regular or irregular breathe. State 2 = Eyes closed, irregular respiration,
modify the responsiveness of the infant. no gross movements.
Absence or presence of continuous gross State 3 = Eyes open, no gross movements.
movements.
Vocalization. State 4 = Eyes open, continual gross
movements, no crying.
State 5 = Eyes open or closed, crying or
fussing.
Ricci scale Ricci et al. (2008) To estimate the level of visual impairment in Spontaneous ocular motility; ocular Percentiles may be obtained by using Newborn
newborns. movements elicited by a target; fixation and reference data from full-term newborns. period
tracking; reaction to a colored target; ability
(continued on next page)
Infant Behavior and Development 49 (2017) 70–82
 Table 3 (continued)

Tool Authors Purpose and Focus Items tested Scoring system Age Range

to discriminate black and white stripes; and

attention at distance.

Legend: GMs: General Movements, MAI: Movement Assessment of Infants, HINE: The Hammersmith Infant Neurologic Exam, NA: Not applicable.
N.A. Cicuto Ferreira Rocha et al.

79
Infant Behavior and Development 49 (2017) 70–82
N.A. Cicuto Ferreira Rocha et al. Infant Behavior and Development 49 (2017) 70–82

3.3.3. Assessing contextual factors

The clinical applications of ICF clearly show that ICF-based functional profiles might be used in the design of biopsychosocial
interventions, such as difficulties that children experience in participating in various social domains, and in identifying environ-
mental factors that may act as barriers or facilitators to the patient’s recovery, well-being and inclusion in society
(Leonardi & Martinuzzi, 2009). There is a systematic relationship between the capacity (what a child does without interacting with
any environmental factors) of an individual and their performance (what a child does interacting with environmental factors) in real
life environments. Often performance is worse than capacity, because there are considerable environmental barriers that are ex-
perienced. The identification of the gap between capacity and performance in clinical settings can help designing interventions that
are targeted either at child capacity or at environmental factors in order to optimize performance.
Evaluation of environmental contexts is important to identify which factors are facilitators or barriers to child development.
Researchers have documented that stimulating home environments are associated with improved infant motor development (Abbott,
Bartlett, Fanning, & Kramer, 2000) and that the regular supportive presence of siblings at home also has a positive effect
(Barr & Hayne, 2003). Thus, it is important that the health care professional observes how is the environmental context, if it is
appropriately motivating, stimulating, what are the modifications in the environments (e.g., using adaptive equipment, if there is
proper bathing, feeding, carrying equipment, appropriate toys to facilitate different types of manipulations), what activities of ev-
eryday life can directly or indirectly affect child development (Howle, 2002). In addition, we recommend checking the family
lifestyle, family support, services support (e.g., transportation services) and availability of financial resources to attend therapies.
Physical aspects of the environment such as house size, comfort and safety factors are also important to support appropriate or-
ientation in daily routine.

4. Conclusion

Studies published showed abnormal brain, optic, neurologic and orthopedic findings, but very little is known about other aspects
of functioning in infants with microcephaly caused by Zika virus.
The biopsychosocial model based on the ICF paradigm can provide the most adequate framework to describe the condition of the
infant with microcephaly receiving rehabilitative efforts to minimize disability. Given the recognition of this alarming and new
scenery starting in Brazil that became an international state of emergency in public health, health care teams need to intensify efforts
towards early identification of developmental delays (i.e., in the first six months of life). Once the condition has been installed, this
careful evaluation may help determining strategies of intervention and family supportive care.

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