Sensory processing in preterm preschoolers and its association with executive function
Introduction
Sensory processing is the organization and interpretation of sensory stimuli from the body and surrounding environment. Symptoms of atypical sensory processing manifest as abnormal behavioral reactions in response to sensory stimulation. Behavioral reactions that are greater than expected are referred to as hypersensitivity; a child with hypersensitivity may respond negatively to bright lights or loud noises. Behavioral reactions that are less than expected are referred to as hyposensitivity; a child with hyposensitivity may have decreased awareness of pain or temperature [1]. Differences in sensory processing have been thought to cause children to exhibit sensation-seeking or sensation-avoiding behaviors [1], both of which could interfere with normal functioning. No consensus has been reached on whether symptoms of sensory processing problems constitute a unique disorder, or whether they represent behavioral characteristics coinciding with other conditions. Although no formal definition or diagnosis of sensory processing problems has been widely accepted in the medical and psychological fields, sensory processing symptoms are commonly identified in a wide range of clinical populations using a diverse set of methodologies, including neurophysiological testing and behavioral questionnaires [2], [3], [4], [5], [6].
Children born preterm (< 34 weeks gestational age) have been documented to have deficits spanning numerous cognitive domains [7], though sensory processing within the preterm population has not been thoroughly investigated. Research to date has found elevated levels of sensory symptoms to be associated with premature birth [8], [9], [10], and has primarily focused on preterm infants and toddlers. Sensory differences in preterm and late preterm (34–36 weeks of gestation) infants have been found to be modest to substantial, measured through both behavioral questionnaires and interactive sensory exams [11], [12], [13]. A study of preterm toddlers found impaired sensory profile patterns across all sensory modalities on a parent-report measure, including behaviors such as sensation seeking, sensation avoiding, sensory sensitivity, and low registration [8]. Atypical sensory profiles were also observed in a broad age range of preterm infants and children, ranging from 1 to 8 years of age [9]. A study of 9-year-old preterm children found reduced electrophysiological responses to auditory stimuli compared to the responses of full term children [14]. To our knowledge, sensory processing has not been evaluated specifically in preterm preschoolers, though the preschool period is important for consolidating development in multiple domains including communication, social development, and pre-academic skills.
Elevated levels of sensory symptoms in preterm children could be attributable to several factors associated with preterm birth. First, abnormal sensory exposure in the neonatal intensive care unit (NICU) during the critical period of sensory neurodevelopment has been postulated to alter and impair neural structures essential to processing sensory information [15], [16]. In addition, brain injury, including periventricular leukomalacia (PVL), periventricular hemorrhage (PVH), and accompanying widespread neural and axonal disease, could disrupt the normal functioning of the sensory systems or association areas, leaving the preterm child with extreme or diminished reactions to sensory stimuli [17]. Finally, abnormal sensory processing could be part of a larger symptom complex of neurodevelopmental conditions that affect the preterm population. Measures of sensory processing have been found to correlate with measures of cognition and language in preterm toddlers [18].
The relationship between sensory processing in preterm preschoolers and other domains potentially impacted by sensory processing, specifically executive function and adaptive function, has not been investigated. Deficits in executive function and adaptive function have been well documented in preterm preschoolers and children [7], [19]. Executive function is a composite of skills involved in higher order and goal-directed thinking; it includes skills such as working memory, inhibition, and planning [20]. Sensory processing may be associated with executive function because sensory processing has been shown to be influenced by higher order cognitive control [21], [22]. Adaptive function describes how a child functions within the environment, completes personal tasks, and demonstrates social skills necessary for success in daily life [23]. Sensory processing may be associated with adaptive function because adverse behavioral reactions to sensory stimuli have been hypothesized to interfere with a child's ability to efficiently or effectively perform age-appropriate functional skills [1].
Associations between atypical sensory processing and impairment in either executive function or adaptive function have been found in several other clinical populations [2], [5], [24], [25]. Reduced auditory sensory gating has been found to coincide with poorer performance on executive function tasks in adults with autism [25] and Alzheimer's disease [24]. In toddlers with autism, sensory scores significantly predicted adaptive behavior scores, over and above the severity of autism symptoms [2]. Finally, in a study of children with Williams syndrome, children classified as having high sensory impairment had poorer scores on both executive function and adaptive function measures than children classified as having low sensory impairment [5].
The first aim of the current study is to evaluate sensory processing in preschool-aged children born preterm. We hypothesized that preterm children have more symptoms of abnormal sensory processing than full term children, and that a higher proportion of preterm compared to full term children meet the criteria for having elevated numbers of sensory symptoms, as defined by classification from the Short Sensory Profile.
The second aim of the current study was to investigate the association between sensory processing and both executive function and adaptive function within the preterm sample. We hypothesized that preterm children with elevated numbers of sensory symptoms have poorer executive function and lower adaptive function than do preterm children with typical numbers of sensory symptoms.
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Participants
Participants were recruited from Palo Alto, California, and the surrounding communities. Preterm children were specifically recruited by letters sent to the families of children who were evaluated at High Risk Infant Follow-up Services at Lucile Packard Children's Hospital in Palo Alto, California. Full term children were recruited by distributing flyers in general pediatric clinics. Both groups were also recruited by postings on local parent message boards and by word of mouth. The sample
Demographics
Demographic information is presented in Table 1. There were no significant differences between the preterm and full term groups in regard to age, sex, or race. Maternal education level, used as a marker for socioeconomic status, was lower in the preterm group than the full term group. The preterm group also had more children as part of a twin set than the full term sample. By design, preterm children had lower gestational age and birth weight than full term controls. No significant differences
Discussion
To our knowledge, this study is the first to specifically evaluate sensory processing in preterm preschoolers. As hypothesized, preterm preschoolers had significantly more sensory processing symptoms than full term children. These results were consistent with previous studies investigating the association between premature birth and sensory processing at younger and older ages [8], [9], [11], [12]. The preterm group had lower mean scores compared to the full term group for the SSP total score
Conclusions
In this sample, over one-third of preschool age preterm children exhibited parent-reported elevated numbers of sensory processing symptoms. The findings fill a gap in previous research regarding the ages in which sensory processing has been studied in preterm children [8], [9], [11], [12]. The association found between sensory processing and executive function suggests that elevated numbers of sensory symptoms in preterm children are related to specific neurodevelopmental deficits [18], rather
Financial disclosure
The authors have no financial relationships relevant to this article to disclose.
Conflict of interest
The authors have no conflicts of interest relevant to this article to disclose.
Acknowledgments
This work was supported by the Child Health Research Institute and Lucile Packard Foundation for Children's Health under a Pilot Early Career Grant (1111239-128-JHACT), the Society for Developmental–Behavioral Pediatrics under the Young Investigator Award, and the Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, under the Mentored Patient-oriented Research Career Development Award Grant (K23HD071971) to Irene M. Loe. This work was
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