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Behavioraland Socioemotional Developmentinpretermchildren
Behavioraland Socioemotional Developmentinpretermchildren
Socioemotional
D e v e l o p m e n t in Pret e r m C h i l d ren
Myriam Peralta-Carcelen, MD, MPHa,*, Justin Schwartz, MD
a
,
Andrea C. Carcelen, MPHb
KEYWORDS
Socioemotional Behavior Prematurity Autism ADHD
KEY POINTS
Development of socioemotional competence is crucial for optimal long-term neurodeve-
lopmental outcomes in preterm children.
Preterm children are at increased risk for behavior and socioemotional difficulties
(including attention deficit disorder, attention deficit/hyperactivity disorder and autism
spectrum disorder) given brain vulnerability, which is sensitive to environmental stressors
during critical periods of brain development.
Clinicians, researchers, and parents should recognize that a complete assessment of out-
comes on prematurity should include behavioral and socioemotional functioning.
Accessibility to early-intervention programs to improve socioemotional functioning and
behavioral problems can potentially improve long-term neurodevelopmental outcomes
on preterm children.
INTRODUCTION
Advances in technology and health care delivery have resulted in an increased number
of preterm infants at lower gestational ages surviving, both with and without clinical
complications.1 However, these children develop significant morbidities at higher
rates than their term counterparts. Preterm children are at risk for neurologic injury
associated with immaturity, hypoxia, inflammation, painful procedures, and stressful
treatments. These injuries can have long-lasting effects, including cognitive, behav-
ioral, motor language, and neurosensory impairment. Given the increased survival
Disclosure Statement: The authors have no commercial or financial conflicts of interests and no
funding sources for all authors.
a
Division of Developmental and Behavioral Pediatrics, Department of Pediatrics, University of
Alabama at Birmingham, Dearth Tower Suite 5602, McWane. 1600 7th Avenue South, Bir-
mingham, AL 35233-1711, USA; b International Health Department, John Hopkins Bloomberg
School of Public Health, 615 North Wolfe Street, Room 5517, Baltimore, MD, USA
* Corresponding author.
E-mail address: mperalta@peds.uab.edu
rate of preterm children, clinicians should be made aware of the behavioral and socio-
emotional difficulties experienced by preterm children and their families in addition to
other traditional outcomes.
Definitions
It has been reported that children born preterm have decreased socioemotional func-
tioning.2–5 Socioemotional functioning involves the ability to learn to successfully
interact and communicate within a social context and to efficiently deal with emotions.
It requires skillful coordination of multiple psychological processes.6,7 Furthermore,
the term “social competence” refers to a variety of mental mechanisms aimed at sup-
porting successful social functioning, including emotional self-regulation, social
cognitive processing, positive communication, and prosocial social relationships.8
The term “social cognition” refers to the fundamental abilities to perceive, store,
analyze, process, categorize, reason with, and behave toward others.9
To develop effective social interactions and social adjustments, it is important to
recognize facial emotional expressions. Deficits in emotional understanding are asso-
ciated with socioemotional and psychiatric disorders.10 Preterm children have diffi-
culties recognizing emotion.11,12 A study in 8-year-old to 11-year-old very preterm
children described problems interpreting each other’s emotions using a complex
test of social perceptual skills.13
Emotion regulation has increasingly been recognized as a potential crucial marker of
later psychosocial risk.14,15 Emotion regulation refers to a child’s ability to modulate
his or her emotions in response to people and situations, using a range of cognitive,
physiologic, and behavioral processes and strategies, allowing for empathic and so-
cially appropriate behavior. Emotional regulation was longitudinally tested in a group
of very preterm children at 2 and 4 years. Higher mean levels of emotional dysregula-
tion emerged at both time points in the very preterm group compared with controls.8,16
Social cognitive skills related to theory of mind are also impaired in preterm chil-
dren.17,18 Theory of mind is defined as the ability to understand that other people
may have different motivations and emotions from one’s own and that people’s
behavior is guided by their inner states.19 Impaired theory of mind has been described
as a core deficit in autism spectrum disorder (ASD) and has been linked to social anx-
iety and low popularity with peers.7
The developmental regulation process initially involves physiologic regulation during
the neonatal period, emotional regulation during infancy, attention regulation during
toddlerhood, and self-regulation during preschool years.20 Specific brain networks
have been found to subserve these processes and to form the so-called “social brain.”21
The cornerstone of successful social adjustment is social competence achieved in the
context of its typically developing neural substrates.
The increased social vulnerability seen in preterm children occurs as a result of spe-
cific alterations in the social brain, part of the neurodevelopmental sequelae of very
preterm birth.22
showed that 20% of preterm children display moderate to severe white matter abnor-
malities, and another 51% have mild abnormalities. Additionally, gray matter abnor-
malities in certain brain regions have been reported to have a role in behavioral
outcomes.26 Early cerebellar injury noted on cranial ultrasound and confirmed with
MRI of the brain was associated with behavioral, cognitive, language, and motor def-
icits in children born very preterm at 34 months of age.27 The cerebellum has signifi-
cant interconnectedness with cerebral hemispheres; therefore, the cerebellum is vital
in cognitive and emotional functioning.28
Social adjustment and anxiety problems have been associated with smaller volume
of left caudate nucleus29 and right superior temporal lobe.30 Caudate abnormalities
have also been found in children with ASD,31 suggesting the role of the caudate nu-
cleus in reciprocal social and communicative behavior possibly due to its complex
connections within cortical-basal ganglia.
The data of Limperopoulus and colleagues26 suggest that the immature cerebellum
may impact neurologic function through mechanisms that disrupt subsequent devel-
opment of remote regions in the cerebral cortex.26 Injury is not as “static” as previously
thought, as the remote effects of primary cerebellar injury may continue to influence
cerebral development for months and even years. Similar mechanisms are likely to
operate following any premature related brain lesions, including periventricular leuko-
malacia or hemorrhage. It is important to understand how these secondary delayed
effects on brain development are occurring to try to prevent further damage to the
brain. Smith and colleagues32 presented evidence that in 44 children born at less
than 26 weeks’ gestation who underwent a brain MRI, stressors to which the infant
is exposed may be directly associated with decreased frontal and parietal width,
altered diffusion measures, and functional connectivity in the temporal lobes. Addi-
tionally, increased abnormalities in motor behavior were observed during neurobeha-
vioral examinations in this study.
These studies highlight the complex interplay among different brain structures and the
role of their connectivity in maintaining unimpaired social cognition and social behaviors.
children and are not screening for these difficulties. Furthermore, they may not be
aware of the interventions available to address them.
The elucidation of mechanisms linking preterm birth, and socioemotional and psy-
chiatric problems could provide an evidence-based rationale for developing and deliv-
ering new effective interventions meant to specifically reinforce protective factors (for
example, interventions on parental stress) or to target specific risk factors found to be
precursors of socioemotional and psychiatric difficulties in preterm-born individuals.
Interventions for optimal socioemotional development of children born preterm
should be given prenatally, during NICU stay and after discharge. Children born
preterm should be screened frequently for risk factors that may impact their socioemo-
tional development. Prenatally, interventions may include providing optimal maternal
care, including nutrition and social support for the pregnant mother. During the NICU
stay, different approaches can be used. One of these is developmental care, which is
a philosophy that embraces the concept of dynamic interaction among the infant, family,
and surrounding environment. This provides a framework in which the environment and
processes of delivering care are modified. Care of the infant focuses heavily on including
parents in the care of the child; avoids overstimulation, stress, pain, and isolation; and
supports self-regulation, social competence, and goal orientation. A specific program
for developmental care, The Newborn Individualized Developmental Care and Assess-
ment Program (NIDCAP) has published data supporting using the NIDCAP principles to
improve brain development, functional competence, health, and quality of life.47 Other
interventions that have demonstrated efficacy in improving outcomes is Kangaroo
care, which focuses on skin-to-skin contact between the parents and newborns.48
An increasing number of studies in the literature have been focusing on what to do
after hospitalization. Spittle and Treyvaud49 emphasized that interventions that focus
on parent-infant relationship and infant development have the greatest impact on
cognitive development in infancy. The importance of promoting optimal development
by implementing screening for behavioral and emotional problems has been empha-
sized in a clinical report.50 There is strong empirical support for family-focused inter-
ventions for young children with emotional, behavioral, and relationship problems.51
For additional information on interventions refer to the American Academy of Pediat-
rics (AAP) technical report.52
There are a few studies that focused on therapies to enhance the overall functional
development, including socioemotional development in preterm children.49,52,53 How-
ever, it is agreed that to have an impact on long-term neurobehavioral outcomes, inter-
ventions should start early in life, and it is important to involve and support parents,
given the high influence of the parent-infant relationship on developmental outcomes.49
but not hyperactivity.75 Murray and colleagues76 demonstrated that in very preterm/very
low birth weight children, white matter abnormalities, including cystic degeneration,
focal signal abnormalities, delayed myelination, thinning of corpus callosum, dilated
lateral ventricles, and/or reduction of white matter volume, on MRI at term-equivalent
age were predictive of attention and processing speed deficits at 7 years of age. This
study also found that deep gray matter abnormalities also predicted difficulties in shift-
ing attention, divided attention, and processing speed.70 In contrast, a study by Bora
and colleagues77 showed that the severity of white matter abnormalities did not corre-
late with later risk of persistent attention or hyperactivity difficulties at 9 years of age;
rather, persistence of ADHD symptoms was associated with volumetric reductions in
the dorsal prefrontal, orbitofrontal, premotor, sensorimotor, and parieto-occipital subre-
gions of the brain, with the dorsal prefrontal region showing the greatest volumetric
reduction among those with persistent attention difficulties. These results are consistent
with the most widely held model of ADHD neuropathology, which implicates abnormal-
ities of the frontostriatal pathways in disorders of attention and self-regulation.78 Striatal
neurons are particularly susceptible to hypoxic-ischemic injury during the perinatal
period,79 lending support to the notion that the genesis of ADHD in preterm infants
may rely more on perinatal factors than genetic factors, as noted previously.
As inflammation has been proposed as an important modulator of white matter
injury, interventions to reduce inflammation theoretically have the potential to lessen
the risk of ADHD symptoms. However, use of antenatal glucocorticoids, antibiotics,
or magnesium sulfate have not yet been shown to reduce the risk of attention prob-
lems.69 Scarce data are available to suggest that reductions in leading causes of post-
natal inflammation (bacteremia, mechanical ventilation, and necrotizing enterocolitis)
would be successful at reducing attention problems as well.69 At the time of writing,
no postnatal interventions to reduce inflammation have documented long-term effects
on outcomes, including attention. However, many interventions, including hypother-
mia, magnesium sulfate, and erythropoietin, have shown promise as neuroprotective
in the short term.80–83
The public health implications of increased attention problems among preterm in-
fants have necessitated heightened surveillance and treatment in this population
throughout the life span. Several studies have documented the continuing burden of
ADHD symptoms on individuals born preterm.45,84,85 Breeman and colleagues86
observed that although attention regulation in very preterm/very low birth weight
individuals improved from childhood to adulthood, there was moderate stability of
ADHD diagnosis in this group as compared with term-born individuals. Krasner and
colleagues87 showed 3 different trajectories of ADHD symptoms among low birth-
weight/preterm children: most (44%) had no symptoms by 9 years of age, 39% had
symptoms at 9 but that they slowly declined by age 16, and 17% showed a persistent
inattentive symptom burden while hyperactivity declined. Those with persistent inat-
tention had poorer outcomes, including increased experiences of bullying, depressive
symptoms, and poorer adaptive functioning. Symptoms at school age were shown to
increase likelihood of special education services and below-expected grade perfor-
mance. Consistent with the results of this study, several prior studies had previously
described the ADHD phenotype of children born preterm as a primarily inattentive pre-
sentation,4,45,88 which may predispose these children’s difficulties to be underappre-
ciated. Mainstays of treatment of ADHD include both behavioral (parent training,
classroom accommodations) and pharmacologic approaches.89 However, data are
scarce on the efficacy of these treatments in populations of individuals born preterm.
Due to the theoretic differences in underlying neuropathology and documented differ-
ences in neuropsychological presentation, this remains an area ripe for further study.
8 Peralta-Carcelen et al
need supplementation with other screening measures.101 The M-CHAT has been
revised to the M-CHAT-R/F and now includes a follow-up interview that should
be used together with the M-CHAT screen to improve the predictive value of the
screening. It has been recommended that both parts of the screening should be
completed.102 Stephens and colleagues103 reported the use of 3 screening
methods (Pervasive Developmental Disorders Screening Test, second edition,
Stage 2 and the response to name and joint attention items from the Autism Diag-
nostic Observation Schedule), on 554 extremely preterm children who did not have
severe neurodevelopmental impairment (severe cerebral palsy, deafness, and
blindness) at 18 to 22 months of age. Twenty percent of children had at least 1
positive screen for ASD consistent with prevalence in the literature; however,
only 1% had all 3 screens positive, which caution us against this increase in prev-
alence using different screening instruments.
A few studies have focused on accurate prevalence of clinically diagnosed ASD
in the preterm population. Johnson and colleagues104 screened 11-year-old former
preterm children with the Social Communication Questionnaire (SCQ) and ASD
was confirmed using a semistructured diagnostic interview: the Development
and Well-Being Assessment. Eight percent of former extremely preterm infants
born at less than 26 weeks’ gestation were diagnosed with autism, whereas
none of the children in the term gestation control group had autism. Pinto-Martin
and colleagues105 studied a regional birth cohort of children with birth weights
less than 2000 g and followed them with periodic assessments until 21 years of
age. A subset of the sample was assessed using the Autism Diagnostic Observa-
tion Schedule (ADOS) and/or the Autism Diagnostic Interview-Revised (ADI-R) and
estimated diagnostic prevalence of autism was 5%.106 In a retrospective cohort
study of infants born in the Kaiser Permanente Healthcare system, the prevalence
of clinically diagnosed ASD in children born at less than 27 weeks’ gestation was 3
times more prevalent compared with children born at term. Each week of shorter
gestation was associated with an increased risk of ASD.106 In a study of 889
extremely low gestational age children (<28 weeks’ gestation) the estimated prev-
alence of ASD was 7.1% using the SCQ for screening, followed by the ADI-R and
the ADOS-2.107
Best Practices
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