Abstract
This systematic review of multidisciplinary literature synthesizes evidence of the prevalence and patterns of sensory processing disorder (SPD) in children ages birth–3 yr born preterm. Forty-five articles including physiological, behavioral, temperament, and SPD research met the inclusion criteria and provided 295 findings related to SPD—130 (44%) positive (evidence of SPD) and 165 (56%) negative (no evidence of SPD). The majority of findings related to sensory modulation disorder (SMD; 43% positive). The most prevalent subcategory of SMD was sensory overresponsivity (82% of findings positive). Evidence of sensory underresponsivity and sensory-seeking SMD, sensory discrimination disorder, and sensory-based motor disorder was limited. This study supports the education of neonatologists, pediatricians, and caregivers about the symptoms and potential consequences of SPD and helps justify the need for follow-up screening for SPD in children ages birth–3 yr born preterm. Research using measures based on sensory processing theory is needed.
Infants born preterm may be at risk for difficulty processing sensory information. Not only is their in utero neurosensory development cut short (Graven & Browne, 2008), but they may also experience intense stimuli in the neonatal intensive care unit (NICU) that could alter sensory system development and function (Nair, Gupta, & Jatana, 2003). Sensory processing dysfunction, in turn, could influence the development of play, social participation, education, and self-care occupations (Miller, Anzalone, Lane, Cermak, & Osten, 2007; Schaaf et al., 2010). Despite these problems, research is limited on the prevalence and patterns of dysfunction in infants and children born prematurely from the perspective of sensory integration theory. The aims of this review were to examine a variety of literature for evidence of sensory processing dysfunction in children ages birth–3 yr born prematurely and to identify the types of sensory processing deficits that are apparent.
In 2007, Miller and colleagues proposed adoption of the new term sensory processing disorder (SPD) in place of the term sensory integration dysfunction, presenting a new taxonomy in diagnosing subtypes of SPD. This classification system was developed using focus groups and empirical evidence, with the expectation of continued scholarly dialogue and research based on the taxonomy. This systematic review contributes to the discussion of the nosology and explores its validity for use with children ages birth–3 yr born preterm by examining the literature to determine whether the proposed patterns of SPD can be identified in this population. Such identification could help justify occupational therapy assessment, follow-up, and intervention for this population and specifically support an approach based on sensory integration theory. Our two research questions were (1) What does evidence in the literature suggest about the prevalence of SPD in children ages birth–3 yr born preterm? and (2) What types of SPD are evident in the literature describing these children?
Background Literature
All motor, behavior, emotional, and attention responses are a result of how the brain processes sensory information. Sensory information serves as an important foundation for adaptive behaviors such as self-control, learning, and the ability to organize (Schaaf et al., 2010). Sensory integration theory explains how sensations are processed and organized to facilitate adaptive behaviors.
A. Jean Ayres developed the concepts of sensory integration theory in 1963 to help explain learning problems and behaviors in children (Miller et al., 2007). Ayres (1989) defined sensory integration as “the neurological process that organizes sensations from one’s body and from the environment and makes it possible to use the body effectively in the environment” (p. 22). She described sensory integration dysfunction as impaired sensory processing resulting in functional problems.
On the basis of patterns observed in children diagnosed with sensory integration dysfunction, the term sensory processing disorder was proposed to increase diagnostic precision. This nomenclature change was recommended because of the paradigm shift that has occurred as sensory integration theory has evolved. SPD is defined as the brain’s inability to organize sensory input for appropriate use, and it may be associated with learning, developmental, and emotional disabilities (Miller et al., 2007).
According to the new nomenclature, SPD consists of three categories: sensory modulation disorder (SMD), sensory discrimination disorder (SDD), and sensory-based motor disorder (SBMD). Sensory modulation is the ability of the central nervous system to effectively alter neural messages from sensory input; it allows a person to focus on some stimuli and ignore others, therefore responding appropriately to the demands of a particular situation. In SMD, a mismatch occurs between the demands of the environment and a person’s emotional and attentional responses.
SMD has three subtypes: sensory overresponsivity (SOR), sensory underresponsivity (SUR), and sensory seeking (SS). SOR is characterized by faster and more intense responses to sensory input from one or more sensory systems. These responses may appear uninhibited, aversive, or defensive and occur for a longer duration than expected. People with SUR often demonstrate a lack of response to sensory input. This inability to detect and respond to sensory input results in low arousal levels, causing a person to seem sluggish, passive, and apathetic. SUR is often associated with other SPDs, particularly SDD and dyspraxia (discussed later in this article). People who demonstrate SS behaviors seek out an abnormal type or amount of sensory input. Their insatiable desire for sensory input can lead to extreme behaviors that are disruptive, socially unacceptable, or unsafe. SMD can involve any sensory system and more than one sensory system (Miller et al., 2007).
SDD is characterized by the inability to interpret qualities of sensory stimuli, such as the location of stimuli or similarities and differences between stimuli. Some people have difficulty identifying stimuli. People with SDD can present with motor, learning, or language disorders depending on the sensory systems affected (Miller et al., 2007).
SBMD results in postural instability or deficits in voluntary movement caused by problems processing sensory input in one or more sensory systems (Miller et al., 2007). The two subtypes of SBMD are postural disorder (PD) and dyspraxia. PD occurs when sensory processing deficits result in poor postural stability. Dyspraxia is defined as “an impaired ability to conceive of, plan, sequence, or execute novel actions” (Miller et al., 2007, p. 138). People with dyspraxia may have difficulty generating ideas for action, move awkwardly and in a disorganized manner, demonstrate inaccurate timing and sequencing of movement, and fail to anticipate the movement needed in a particular situation. These three categories of SPD are not mutually exclusive; a person may demonstrate one or more SPD.
Prematurity
Premature birth is birth before the 37th week of gestation. Premature delivery occurs in 13% of all pregnancies (Rais-Bahrami & Short, 2013). A child can also be classified as premature on the basis of low, very low, or extremely low birthweight. Low birthweight is defined as <2,500 g, very low birthweight as <1,500 g, and extremely low birthweight as <1,000 g (Rais-Bahrami & Short, 2013).
Risk of Sensory Processing Disorder in Infants Born Prematurely
The majority of neurosensory development usually occurs in the last 16–20 wk of gestation (Graven & Browne, 2008). Premature birth could therefore preclude much of the typical development of sensory systems that occurs in utero, resulting in difficulty processing sensory input and in one or more types of SPD. As described by Graven and Browne (2008), “Preterm birth does not accelerate any of the early sensory development processes but can retard or interfere with the sensory development when exposed to stimuli” (p. 170).
Many babies who are born prematurely are admitted to the NICU. Stimuli in the NICU are both unusual and much more intense than stimuli experienced by infants in utero (Als & McAnulty, 2011). Bright lights may deter them from opening their eyes and taking in the environment around them. Babies in the NICU are also subjected to necessary aversive procedures such as needle sticks and nasogastric intubation. Handling of the infant can lead to behavioral stress, and touch may be stressful rather than soothing (Nair et al., 2003). Exposure to high-pitched sounds can cause physiological changes such as tachycardia, tachypnea, apnea, oxygen desaturation, sudden increases in blood pressure, the release of stress hormones, and disturbed sleep (Graven & Browne, 2008; Nair et al., 2003). Rapid-eye-movement sleep deprivation in itself could alter the development of sensory systems (Graven & Browne, 2008).
Research Based on a Sensory Processing Perspective
Only four published studies have examined sensory processing in infants and young children born preterm from a sensory integration theoretical basis (i.e., Bart, Shayevits, Gabis, & Morag, 2011; Case-Smith, Butcher, & Reed, 1998; Wickremasinghe et al., 2013; Wiener, Long, DeGangi, & Battaile, 1996), with three of the four including a comparison group of children born at term (i.e., Bart et al., 2011; Case-Smith et al., 1998; Wiener et al., 1996). Two of the studies were published before the SPD nosology was proposed (i.e., Case-Smith et al., 1998; Wiener et al., 1996), and their findings were somewhat contradictory. Case-Smith and colleagues found little evidence of SPD except for tactile overresponsivity. Wiener and colleagues, however, found evidence of vestibular–proprioceptive overresponsivity and some evidence of PD (i.e., 1 of 3 findings was positive). Somewhat consistent with Case-Smith and colleagues, Wiener and colleagues also reported some evidence of tactile overresponsivity (i.e., 3 of 6 findings were positive). Although both studies tested children in the age range of 7–18 mo, they used different instruments to measure sensory processing (i.e., the Test of Sensory Functions in Infants [TSFI; DeGangi & Greenspan, 1989] in Wiener et al. and the Sensory Rating Scale [SRS; Provost & Oetter, 1993] in Case-Smith et al.). In both studies, limitations of the instruments were identified as factors that may have influenced the results.
In a more recent study, Bart and colleagues (2011) used both the Infant/Toddler Sensory Profile (Dunn, 2002) and the TSFI to assess sensory modulation of infants born from 34–35 6/7 wk gestational age. Similar to Wiener and colleagues (1996), they found some evidence of SMD in the tactile (i.e., 2 of 3 findings were positive) and vestibular–proprioceptive systems (i.e., 1 of 2 findings was positive). These positive findings tended to be in the direction of SOR. In addition, Bart and colleagues found evidence of SMD in the auditory system (i.e., 1 of 1 finding was positive) and of dyspraxia (i.e., 1 of 1 finding was positive).
Wickremasinghe et al. (2013) found atypical overall scores on the Sensory Profile (either the Infant/Toddler Sensory Profile or the Sensory Profile [Dunn, 1999], depending on child’s age) in 39% of a group of children ages 1–8 yr born preterm. Consistent with Bart and colleagues (2011), auditory, tactile, and vestibular deficits were most common, with relatively few atypical Sensory Profile scores on the oral sensory processing and visual processing sections. Wickremasinghe and colleagues also found that a larger-than-expected proportion of children born preterm had atypical scores in each of the four quadrants of the Sensory Profile (i.e., low registration, sensory seeking, sensory sensitivity, and sensory avoiding); however, unlike the other three studies, the largest percentage of participants (24%) in Wickremasinghe and colleagues’ study demonstrated low registration, which is consistent with SUR rather than SOR. In the other three quadrants, 10%–11% of participants had atypical scores.
This systematic review could add to the literature in several ways. Compilation of evidence from multiple studies may provide a more reliable representation of the sensory processing characteristics of infants and young children born preterm than evidence from a single study with a relatively small number of participants. Findings from the studies discussed previously show some similar trends but also inconsistencies.
Further, Bart and colleagues (2011) reported a difference in their findings based on the instrument used to gather the data (the TSFI vs. the Infant/Toddler Sensory Profile). Scores on the TSFI reflect ratings of observed behaviors, whereas scores on the Infant/Toddler Sensory Profile are derived from parent responses to a questionnaire. Consideration of a variety of types of evidence from multiple disciplines, including behavioral observations, parent reports, and physiological data, may allow for a broader picture of the prevalence and patterns of SPD in infants and young children born preterm.
This review could lend further support for NICU adaptations such as reducing sound and light and modifying touch stimuli. Implementation of these adaptations may help prevent SPD. Moreover, if preterm infants are at risk for developing SPD, pediatricians need to be educated to recognize the disorder’s symptoms and provide appropriate referrals for occupational therapy intervention. If children born prematurely were regularly screened for SPD, early intervention could be implemented to address dysfunction and potentially prevent future disability, which has both quality-of-life and financial implications.
Method
Sources
We independently searched multidisciplinary literature using electronic databases, including CINAHL, PsycINFO, Medline, Scopus, and PubMed, from 1990 to present. A medical research librarian also assisted in developing the search strategy and conducting the search. In addition, we examined references cited by articles included in the review for potential articles. Key search terms, used in a variety of combinations, included sensory processing disorder, sensory processing dysfunction, sensory integration, sensory underresponsiveness, sensory overresponsiveness, sensory seeking, visual processing, tactile processing, auditory processing, proprioception, vestibular processing, premature, preterm, low birth weight, regulatory disorders, developmental coordination disorder, temperament, evoked potentials, and 0–3 yr.
Inclusion Criteria
The review included peer-reviewed research articles published in English since 1990 that provided evidence of SPD in children ages birth–3 yr born preterm or with low birthweight, or both. Studies compared children born preterm either with a control group of children born full term or with normative data. Articles that focused on sensory impairments (e.g., deafness or blindness) or major motor impairment such as cerebral palsy were excluded. Data from presentations, conference proceedings, non-peer-reviewed research literature, dissertations, and theses were also excluded. To reach consensus, the five authors discussed whether articles met the inclusion criteria.
Data Extraction and Analysis
We composed an evidence table of all articles, summarizing participant characteristics (chronological age, gestational age, and birthweight), outcome measures used, findings related to SPD, level of evidence, and study limitations. We used SPD categories and their descriptions from Miller and colleagues (2007) and descriptions and explanations of outcome measures provided in each study to categorize data on the basis of SPD type and sensory system involved. We consulted additional literature describing the study instruments when necessary. For 23 articles, we used group discussion and consensus to classify the findings according to SPD type. The first author (Mitchell) classified the remaining 22 articles. The number of positive (evidence of SPD) and negative (evidence of typical sensory processing) findings in each category were tallied, and total percentages were calculated.
Results
Initially, the searches found 81 articles, 45 of which met inclusion criteria. Most (91%) of these 45 articles provided Level II evidence (nonrandomized two-group design), whereas 9% provided Level III evidence (nonrandomized one-group design). Randomized controlled trials were not expected because of the nature of the research questions.
The total number of preterm study participants was 2,584, with an age range of 1 day to 3 yr, 1 mo; gestational age from 22 to 37 wk; and birthweight from 450 to 2,865 g. Mean values cannot be reported because some articles lacked necessary information. Study instruments included physiological measures, temperament questionnaires (Intensity, Approach/Withdrawal, and Threshold subtests), and behavioral measures (Table 1). Only 3 studies included measures based on theories of sensory processing.
Sensory Processing Measures Used by Systematic Review Studies
Within the 45 studies, 295 findings related to SPD. Of these, 130 (44%) were positive and 165 (56%) were negative. These findings were categorized according to sensory system affected, SPD, and SPD subtype (Table 2). The majority of findings related to SMD. Because of the nature of the assessment tools used in the studies, many of these findings could not be classified according to SMD subtype. For example, neurobehavioral and temperament assessments often did not describe the direction of differences in sensory responses (greater vs. lesser responsivity); therefore, these findings were considered unclassified SMD. Negative findings in this category were not considered negative findings for each SMD subtype because this conclusion would result in overrepresentation of negative findings. For all three categories (unclassified SMD, SOR, and SUR) in total, 43% of findings were positive and 57% were negative. Numbers and total percentages of positive and negative findings in different sensory systems for each SMD category were tallied and calculated (Table 3). Of the SMD findings that could be classified, the majority were positive for SOR. Very few findings of SUR were identified, and no findings were classified as SS.
Sensory Processing Disorder and Typical Sensory Processing Findings According to Sensory System Affected and Sensory Processing Disorder Subtype
Note. PD = postural disorder; SBMD = sensory-based motor disorder; SMD = sensory modulation disorder; SOR = sensory overresponsivity; SUR = sensory underresponsivity.
Number of Positive (+) and Negative (–) Findings of Sensory Modulation Disorder and Sensory Discrimination Disorder in Different Sensory Systems
Note. SDD = sensory discrimination disorder; SMD = sensory modulation disorder; SOR = sensory overresponsivity; SUR = sensory underresponsivity.
Again, because of the assessment tools used in the studies (e.g., temperament questionnaires, neurobehavioral assessments), a majority (64%) of the SMD findings could not be classified according to sensory system. These findings were therefore labeled “unspecific.” Of those that could be categorized by sensory system, the largest number of findings related to the tactile (30) and visual (29) systems. Whereas 79% of the visual system findings were negative for SPD, more than half of the tactile system findings were positive. All but 2 of the positive tactile system findings reflected SOR.
There were far fewer findings of SDD and SBMD than of SMD. Evidence of SDD was found in 6 studies (see Table 2). Most of the findings related to the auditory, visual, and tactile systems. Whereas the majority of findings for visual discrimination were negative, there were more positive than negative findings for auditory discrimination. For tactile discrimination, there were close to equal numbers of positive and negative findings (see Table 3).
Evidence of SBMD was found in 8 articles (see Table 2). One finding could not be classified by subtype and therefore was considered unclassified SBMD. This finding was negative. For PD, there were 7 positive and 3 negative findings, and for dyspraxia, there were 5 positive and 4 negative findings.
Findings from research articles that used the three most common types of instruments—physiological measures, temperament questionnaires, and neurobehavioral assessments (see Table 1)—were examined separately. Findings from the physiological measures and neurobehavioral assessments mirrored the overall findings; however, the large majority (46 of 57, or 81%) of findings from temperament questionnaires were negative. Of the 11 positive findings, 9 suggested SOR and 2 suggested SUR.
In summary, of the 295 findings from the 45 articles included in the review, 44% were positive and 56% were negative for SPD. The majority of findings related to SMD, with 43% of those being positive. The most prevalent subcategory of SMD was SOR, and the majority of these findings were positive. Evidence of SUR and SS, SDD, and SBMD was limited.
Discussion
Although the results of this systematic review appear mixed, a substantive proportion of the findings suggests children ages birth–3 yr born preterm may be at risk for sensory processing dysfunctions such as those defined by Miller et al. (2007). Evidence of SMD, specifically SOR, was most prominent, which seems logical considering the immaturity of newborns’ sensory systems and the potentially overwhelming and aversive stimuli to which they may be exposed in the NICU. These results are also consistent with studies by Case-Smith and colleagues (1998), Wiener and colleagues (1996), and Bart and colleagues (2011), who based their research on a sensory integration theoretical perspective and reported SOR in infants and young children born preterm.
The preponderance of SOR findings in this review is in contrast to Wickremasinghe and colleagues’ (2013) study, which found a greater incidence of SUR in children ages 1–8 yr born preterm. Several explanations are possible for this difference. For example, this review included studies published as early as 1990; therefore, some of the participants in the early studies may have been exposed to NICUs that had not yet implemented developmental care and environmental modification. Changes in NICU environments over the years may have resulted in differences in sensory processing outcomes for infants and young children born prematurely. However, a more recent study by Bart and colleagues (2011) found evidence of SOR in children born preterm, which is consistent with this review.
Another potential explanation for the difference in Wickremasinghe and colleagues’ (2013) findings could involve the outcome measures used. This review included a variety of measures—including evoked potentials, behavioral observations, and temperament questionnaires completed by parents—whereas Wickremasinghe and colleagues used the Sensory Profile, which involves only parent responses to a questionnaire. Some parents in Wickremasinghe and colleagues’ study may not have recognized behaviors indicating SOR. For example, some children who are overresponsive may shut down as a way of coping with their overresponsivity (Schaaf et al., 2010). Therefore, what may have appeared to a parent to be underresponsivity may actually have been overresponsivity. This review’s inclusion of studies that used physiological measures and behavioral observations may have provided a clearer picture of sensory processing than a single study using one type of outcome measure. Finally, this review focused on children ages birth–3 yr, whereas Wickremasinghe and colleagues’ participants ranged in age from 1 to 8 yr. Wickremasinghe and colleagues reported a trend toward a greater incidence of atypical Sensory Profile scores in older children and suggested SPD may become more evident with age.
The SS pattern was not found in the literature included in this review, except for a mention in 1 study. On the basis of analysis of two SRS items, Case-Smith and colleagues (1998) reported that SS behaviors were common in children born preterm; however, they considered these to be age-appropriate behaviors. This lack of SS findings may also be related to the tools used in the studies. For example, Wickremasinghe and colleagues’ (2013) study used the Sensory Profile, which does identify the SS pattern, and found that a statistically larger proportion of participants than expected (11%) demonstrated SS behaviors. Further research using standardized measures that identify the SS pattern is needed before drawing conclusions about its prevalence in children ages birth–3 yr born preterm.
Evidence related to SDD and SBMD was also scarce. These patterns were difficult to identify in the current review because of limits in the number and variety of perceptual and motor skills demonstrated by children ages birth–3 yr and tested by the tools for children in this age range. Thus, the outcome measures used often provided limited findings that could be classified as SDD or SBMD. Even if evidence of mild motor disorders was present, it was often difficult to determine whether they were sensory-based disorders because the instruments used in the studies usually did not measure tactile, vestibular, or proprioceptive processing. Again, research using measures consistent with the SPD nosology is needed to clarify the incidence of these patterns in children ages birth–3 yr born preterm.
This review revealed a difference between findings of studies that used temperament measures and findings of studies that used other types of instruments. Although DeSantis, Harkins, Tronick, Kaplan, and Beeghly (2011) found evidence to support the idea that sensory processing assessments and temperament questionnaires may describe the same behaviors using different theoretical perspectives, in this review few positive findings were based on the temperament measures. Although this difference may simply reflect a lack of SPD in infants and young children born preterm, it contrasts with the evidence from studies using other sensory processing measures. However, the difference may relate to the type of SPD most associated with scores on temperament questionnaires.
In a study of children with autism spectrum disorder, Brock et al. (2012) found evidence of commonalities between five of the nine dimensions of a temperament questionnaire and measures of sensory processing. Three of the temperament dimensions related to SUR, and two related to SMD in general. The researchers found no statistically significant effects between SOR or SS and the temperament measure. This may explain the difference between the findings of studies using temperament measures and findings of studies using other types of measures. That is, temperament assessments tend to reflect SUR rather than SOR or SS and infants born preterm are more prone to SOR. Interestingly, in this review, of the few positive findings based on temperament questionnaires, most suggested SOR, which is consistent with the overall findings of the review.
Limitations
The exclusion of unpublished literature and non-English studies may have been a limitation of this review because their inclusion could have changed the proportions of positive and negative findings. In addition, few of the instruments used in the included studies were designed to directly assess any of the SPD categories defined by Miller et al. (2007). Thus, these results were based on inferences drawn from a variety of types of data, described previously. To address this challenge, at least two of the authors examined and appraised findings from a subset of 23 of the 45 studies. All five authors then agreed on the classification of the findings from these 23 studies to ensure the credibility of the classification of the remaining articles. Finally, many of the studies tested relatively small convenience samples, with limited power to detect differences between groups. Despite these limitations, the substantive number of positive SPD findings (particularly in the SMD category) has implications for occupational therapy practice with children ages birth–3 yr born preterm.
Recommendations for Future Research
Further research examining the prevalence of SPD in infants born prematurely would be beneficial. This research should be based on a sensory processing theoretical perspective and use instruments that allow detection of SPD patterns. Multisite studies with large samples of participants and examiners blinded to term or preterm status would also increase the reliability of the findings.
Expansion of the review to include preschool- and school-age children may provide an opportunity to detect SPD patterns difficult to identify in children ages birth–3 yr. Wickremasinghe and colleagues (2013) noted a trend toward increasing frequency of atypical Sensory Profile scores with increasing age; therefore, they argued, SPD may increase in severity or become more evident as children age.
Implications for Occupational Therapy Practice
The results of this review have the following implications for occupational therapy practice:
Children ages birth–3 yr born preterm should be screened for SPD, particularly SOR.
Parents whose infants are born preterm and spend time in the NICU may benefit from education about SPD, including signs and symptoms to be alert for and techniques and approaches to incorporate at home.
Findings of this study could be used to support the need for environmental modification in the NICU.
Education of pediatricians about the risk of SPD in children ages birth–3 yr born preterm is needed to promote follow-up and early intervention services for young children whose subtle dysfunctions may otherwise be overlooked.
Conclusion
The results of this study could help justify the need for children born preterm to be referred for post-NICU follow-up to assess sensory processing. Infants who are born before their sensory systems can fully develop in utero and are exposed to atypical, overwhelming, and aversive stimuli in the NICU appear to be more at risk for SPD, particularly SOR. Occupational therapy can play an important role in intervention with this population. Occupational therapy practitioners can help identify the risks in the NICU and make recommendations for modifications, recognize the signs and symptoms of SPD, and provide treatment of SPD for children born preterm.
Footnotes
Acknowledgments
The authors thank Brenda Green, medical research librarian at the University of Tennessee Health Science Center, for her assistance.
Indicates studies that were systematically reviewed for this article.
