Abstract
Cochlear implants (CIs) are devices that allow people with severe sensorineural hearing loss (SNHL) to perceive sound. Services for children who receive CIs have generally revolved around audiology and language and speech development. These services are typically aimed at improving speech through audition. However, emerging research suggests that sensory integrative challenges—in particular, differences in vestibular functions—may be common in children who receive this intervention (Bharadwaj, Daniel, & Matzke, 2009; Bharadwaj, Matzke, & Daniel, 2012). Therefore, exploration of sensory integrative patterns, including skills related to vestibular function, in children with cochlear implants is warranted.
Literature Review
SNHL results from permanent damage to the tonotopically organized hair cells in the ear, which typically stimulate the auditory nerve. CIs bypass the outer and middle ear to stimulate the auditory nerve electrically using an array of electrodes inserted into the cochlea. With the CI, a microphone picks up sound and delivers it to the externally worn speech processor. The speech processor, in turn, converts the sound to electrical inputs and transmits the data to the implant by telemetry. The implant delivers information to the auditory nerve through an electrode array or lead. Learning to listen using a CI is a process that takes time, especially for children who are prelingually deaf (i.e., lost their hearing before they began to speak; Chorost, 2005; Clark, 2003; Wolfe & Schafer, 2010). After CI surgery, follow-up treatment may include audiometry sessions; auditory verbal therapy; and, in some cases, speech–language therapy.
CIs have become an option at younger and younger ages for children with profound hearing loss (“Cochlear Implants,” 2011, para. 3; Connor, Craig, Raudenbush, Heavner, & Zwolan, 2006). Children with hearing loss often experience developmental challenges such as difficulties in academic achievement, poor social development, and delayed verbal skills (Carney & Moeller, 1998; Khairi Md Daud, Noor, Rahman, Sidek, & Mohamad, 2010; Matkin & Wilcox, 1999; Quittner, Leibach, & Marciel, 2004). Some evidence has indicated that children with hearing loss also show significantly lower scores on tests of motor abilities and balance function than their hearing peers (Engel-Yeger & Weissman, 2009; Gheysen, Loots, & Van Waelvelde, 2008).
It is also well documented that children with hearing loss have demonstrated vestibular dysfunction, typically hypoexcitability of the vestibular sense (Jacot, Van Den Abbeele, Debre, & Wiener-Vacher, 2009; Jerome, Kannan, Lakhani, & Palekar, 2013). Vestibular evoked myogenic potentials show significantly higher thresholds or absent responses of the vestibular system in children with severe SNHL (Shall, 2009; Zhou, Kenna, Stevens, & Licameli, 2009). The etiology for decreased vestibular function could be related to the embryological connection between the vestibular and cochlear end organs (Bharadwaj et al., 2012) or the surgical technique of inserting the electrode into the cochlea during CI surgery (Basta, Todt, Goepel, & Ernst, 2008; Todt, Basta, & Ernst, 2008).
Young children with SNHL and vestibular dysfunction have been reported to experience delayed motor and balance development (Rine et al., 2000). Abnormal vestibular function in children with profound SNHL has also been associated with delayed development of head control and independent walking (Inoue et al., 2013). Vestibular dysfunction in children with hearing loss can be exacerbated by cochlear implantation surgery (Krause et al., 2009; Licameli, Zhou, & Kenna, 2009). The process of inserting the electrode into the cochlea can impair vestibular receptor integrity as evaluated by vestibular evoked myogenic potentials and caloric irrigation, which measures the vestibulo–ocular reflex (Basta et al., 2008; Todt et al., 2008). In fact, studies have found decreases in vestibular function after cochlear implantation (Jacot et al., 2009; Jin, Nakamura, Shinjo, & Kaga, 2006; Krause et al., 2009). Decreased vestibular function in children with hearing loss and CIs is also thought to have an impact on gaze stability, which is vital for learning to read and for developing standing and walking balance (Potter & Silverman, 1984; Rine et al., 2004).
Along with these vestibular issues identified in the literature, sensory integration theory, originally described by A. Jean Ayres in the early 1960s, asserts that active and adaptive engagement in everyday activities and learning requires the organization of sensory information. Sensory information, including proprioceptive, vestibular, tactile, visual, auditory, taste, and olfactory input, when integrated effectively, allows children to participate to their full potential in learning and other childhood occupations. Together these senses contribute to the development of many abilities, including motor planning, body awareness, visual–motor skills, language development, and regulation of level of activity (Schaaf et al., 2010). The vestibular sense detects head position, movement, and gravity through receptors in the inner ears, whereas proprioceptive input comes from the muscles and joints and informs a person of body position. Together, vestibular and proprioceptive inputs contribute to body schema and perception of active movement and are associated with many important skills and functions such as balance, equilibrium responses, muscle tone, postural and ocular control, ability to cross midline, development of laterality and hand dominance, and navigational and directionality functions (Lane, 2002; Parham & Mailloux, 2010).
The gold standard for assessing sensory integrative function in children is the Sensory Integration and Praxis Tests (SIPT; Ayres, 1989), a comprehensive set of 17 tests that evaluate abilities associated with sensory perception, praxis, and related motor functions such as bilateral integration and balance. On the basis of numerous factor and cluster analyses, Ayres (1965, 1966, 1972, 1977, 1989) and others (Mailloux et al., 2011; Mulligan, 1998) described consistent patterns of sensory integrative dysfunction, including visuodyspraxia, somatodyspraxia, vestibular bilateral integration and sequencing (BIS) deficits, somatosensory deficits, and tactile hypersensitivity associated with problems in attention and activity level. Each pattern is associated with a particular constellation of test scores or, in the case of tactile sensitivity, scores on questionnaires and observations of the child’s behavior.
As the vestibular system’s role was clarified and more refined testing methods were developed, the understanding of vestibular BIS pattern evolved from its original description in the 1960s (Ayres, 1965). Although the specific tests associated with this pattern have varied somewhat over time, the core underlying features of postural, ocular, and bilateral functions known to be associated with vestibular sensory processing have remained the key indicators of this pattern (Mailloux et al., 2011). In 1989, Ayres named this pattern bilateral integration and sequencing deficit, identified by low scores on the following SIPT tests: Oral Praxis, Graphesthesia, Standing and Walking Balance, Sequencing Praxis, Postural Praxis, and Bilateral Motor Coordination. Ayres (1989) also stated that short durations of postrotary nystagmus (PRN) are often associated with these deficits.
In 2011, Mailloux et al. reported on a pattern they called vestibular and proprioceptive bilateral integration and sequencing (VPBIS). Low PRN had a significant loading on this pattern, as had been previously hypothesized by Ayres (1989), as did the tests of Oral Praxis, Standing and Walking Balance, Bilateral Motor Coordination, Graphesthesia, Motor Accuracy, and Sequencing Praxis. This constellation of scores strengthened the association between shortened-duration PRN and the bilateral and sequencing tests (Mailloux et al., 2011). Clinical reports and previous research suggest that children who have characteristics of the VPBIS pattern often demonstrate other clinical signs of inefficient vestibular function, including poor postural and ocular mechanisms, low muscle tone, difficulty with antigravity positions, and problems in directionality and laterality, as well as the absence of more pronounced problems in praxis and tactile perception characteristic of somatodyspraxia (Ayres, 1989; Jerome et al., 2013; Parham & Mailloux, 2010).
Although developmental and vestibular functions have been considered for children with CI, broader examination of sensory integrative function and dysfunction has been limited. Bharadwaj et al. (2012) administered 11 of the 17 tests in the SIPT to 12 young children with CIs and compared their mean scores with those of the normative sample. They concluded that children with CIs demonstrated vestibular dysfunction as shown by significantly shortened durations of PRN and low scores on the Standing and Walking Balance test. This study also identified decreased performance on the proprioceptive and tactile test items, including the Kinesthesia and Graphesthesia tests, which require processing of tactile and proprioceptive input without the use of visual cues (e.g., reproducing shapes drawn on the back of the hand). Because we did not apply all of the SIPT tests in this study, however, consideration of previously identified sensory integration patterns of dysfunction was not possible.
Given the important relationships between vestibular functions and participation in daily life (Schaaf et al., 2010) and the potential for vestibular dysfunction in children who receive CIs, we sought to further explore and characterize sensory integration functions and difficulties in children who had received CIs. Specifically, the study aimed to determine whether children with CIs demonstrated similarities to the VPBIS pattern and whether they showed signs of other sensory integration deficits as well. The research questions for this study were as follows:
Will children with CIs exhibit deficits on the SIPT associated with the VPBIS pattern of sensory integrative dysfunction?
Will children with CIs show signs of other sensory integrative or developmental deficits?
Method
Research Design
The research design for this study was a retrospective de-identified record review. The University of Southern California institutional review board granted approval for this study.
Participants and Procedures
Therapists with advanced training in sensory integration (Sensory Integration Certification) and pediatric assessment administered assessments to children at the John Tracy Clinic in Los Angeles, CA. These assessments aimed at evaluating sensory integration function, fine and gross motor skills, and other aspects of development with the aim of achieving a greater understanding of children with CIs and providing appropriate education and training for the parents, teachers, and therapists interacting with these children. Children ages 4 yr, 0 mo, to 8 yr, 11 mo, were given the SIPT (except for the Praxis on Verbal Command Test because this test is heavily dependent on language and the children had hearing issues). Children ages 7 to 47 mo, who were too young for the SIPT, were administered the Peabody Developmental Motor Scales (PDMS; Folio & Fewell, 2000). The parents of all 49 children were asked to complete two standardized caregiver questionnaires: the Developmental Profile 3 (DP–3; Alpern, 2007) and the Sensory Profile (SP; Dunn, 1999) or Sensory Processing Measure (SPM; Parham & Ecker, 2010). All assessments were completed over a 6-mo period in 2009 and 2010.
Data Handling and Analysis
This investigation involved deidentified record reviews of assessments and caregiver questionnaires that had been completed for the 49 children. The exact sample size and age range for each assessment and questionnaire varied because of the number of parents who returned the questionnaires and the number of tests the children were able to complete (e.g., some children were able to complete only some of the tests of the SIPT or the PDMS).
We examined the scores on the SIPT, SP, and SPM to determine whether these children with CIs demonstrated notable or recognizable patterns of sensory integrative dysfunction, namely visuo- and somatodyspraxia, tactile and visual discrimination, tactile defensiveness and attention, and vestibular and proprioceptive bilateral integration and sequencing (Mailloux et al., 2011). The SIPT scores of 18 children ages 4–7 yr with CIs were compared with the normative data using one-sample t tests. The one-sample t test allowed for evaluation of the group’s performance on each test (sample sizes varied for each test because some children could not complete the entire SIPT). For the one-sample t test, a two-tailed 5% level of significance was used to interpret p values (α = .05). Because the initial review of the mean SIPT scores for the CI sample revealed many low mean scores on tests that have been associated with the vestibular bilateral patterns, we divided the 16 administered tests of the SIPT into two groups: those tests that (1) did and (2) did not load on the BIS or VPBIS factor (Ayres, 1989; Mailloux et al., 2011) to answer the research questions.
The SP and SPM are both standardized questionnaires asking primarily about the presence of unusual reactions (over- or underresponsiveness). The SP was used for children younger than age 5 because the SPM was not normed for that age group at the time of data collection. These two measures include four overlapping categories—auditory, visual, tactile, and vestibular processing—and a similar scoring system for attaining subscores for parent responses about these categories. We analyzed only the four scores from overlapping categories. The sample included 11 SP records and 9 SPM records. For each of the four overlapping categories, we determined the number and percentage of children with CIs who were scored as having typical responses, some problems, or definite problems.
The PDMS is a developmental assessment of motor skills, and the DP–3 is a developmental assessment questionnaire. For each domain of the PDMS and DP–3, children are scored or rated as well above average, above average, average or typical, below average, or well below average. For both the PDMS and the DP–3, we determined the number and percentage of children with CI who were rated or who scored in each of these categories.
Results
Participants
The deidentified records included in this analysis were from 49 children ages 7 to 83 mo who received services at a center specializing in programs for children with hearing loss or CI. All children assessed used at least one cochlear implant (unilateral); records indicated that 6 of the 18 children assessed with the SIPT used bilateral implants. All children in the analysis had mild to severe hearing loss, which is a prerequisite for cochlear implantation. Table 1 shows the number of retrieved records for each assessment from the 49 children.
Assessments and Number of Records for Each Assessment (N = 49)
Sensory Integration and Praxis Tests
The mean score for the normative sample on each of the SIPT tests is zero because individual scores are represented by z scores, which by definition have a mean of zero. One-sample t tests revealed significant differences in mean scores between the children with CIs and the normative sample on six of the eight tests of the SIPT associated with the VPBIS pattern of sensory integration, as shown in Table 2. The CI sample scored significantly lower than the normative sample on the tests of Motor Accuracy, Sequencing Praxis, Bilateral Motor Coordination, Standing and Walking Balance, Manual Form Perception, and Postrotary Nystagmus.
Comparison of SIPT Scores of 18 Children With Cochlear Implants Ages 50 to 83 Mo With Normative Sample
Note. BIS = bilateral integration and sequencing deficit (Ayres, 1989); CI = cochlear implant; CI SD = standard deviation of the sample of children with CIs; SIPT = Sensory Integration and Praxis Tests; VPBIS = vestibular and proprioceptive bilateral integration and sequencing (Mailloux et al., 2011).
Degrees of freedom = n−1 for each test.
Test sample is significantly different from normative sample.
The CI sample mean scores were not significantly different from the normative sample on two tests associated with BIS or VPBIS, the Graphesthesia and Oral Praxis tests. The CI sample mean scores were significantly different on only one test that was not associated with the BIS or VPBIS pattern, the Design Copying test. These results suggest that the children with CI share many features of the BIS or VPBIS pattern. In addition, as a group, the sample of children with CI in this study did not show indications of other sensory integrative patterns of dysfunction.
Sensory Processing Measure and Sensory Profile
Table 3 shows the number and percentage of children with CI who scored in each descriptive category (i.e., typical, some or probable difference, or definite difference) for the auditory, visual, tactile, and vestibular categories on the SPM and SP. Half of the 20 children with CI scored in the typical range on the auditory category, with the remaining 50% (n = 10) rated as having some or definite differences. For the other sensory areas, the ratios of typical to some or definite differences were 65%:35% (n = 20) for visual, 55%:45% (n = 20) for tactile, and 60%:40% (n = 20) for vestibular. Because the SP and SPM include questions about over- and underresponsiveness to sensation, as well as questions related to more general functions of the sensory systems, the interpretation of subscores requires careful consideration and review of individual responses. As a group, the majority of children with CIs in this study did not appear to have a clear pattern of sensory modulation problems on the basis of test scales, with at least half of the children being rated as typical.
Combined Sensory Processing Measure (n = 9) and Sensory Profile (n = 11) Test Results for Children With Cochlear Implants
Note. In a normal distribution, 16% of the sample would fall into the combined some or probable difference to definite difference range.
Developmental Profile 3 and Peabody Developmental Motor Scale
Table 4 shows the percentage of children with CI in each descriptive category (i.e., well above average, above average, average or typical, below average, or much below average) on the DP–3 and PDMS. The majority (59%–100%, n = 1–32) of the CI sample scored in the average or typical to above average range on all subscores of both tests, except for the Communication subscore on the DP–3 (44% typical and 56% below or much below average, n = 32). The next category with the largest percentage of children falling below average to much below average was in the Cognitive subscore (41%, n = 32), followed by the General Development subscore (32%, n = 32) of the DP–3, the Locomotion subscore on the PDMS (31%, n = 12), and the Adaptive Behavior subscore on the DP–3 (25%, n = 32). These results suggest that the majority of our sample of children with CI did not, as a whole, demonstrate significant developmental delays on the basis of direct testing or parent report.
Percentage of Children With Cochlear Implants Scoring in Each Category on the DP–3 and PDMS
Note. DP–3 = Developmental Profile 3; PDMS = Peabody Developmental Motor Scales.
Discussion
Previous studies have shown that children with hearing loss may also experience vestibular dysfunction, most commonly reported as hyporesponsivity of the vestibular sense (Bharadwaj et al., 2012; Jacot et al., 2009; Jerome et al., 2013), and the results of this study are consistent with these findings. Of the 18 children with CIs who were tested with the SIPT, 15 had PRN duration at least 1 standard deviation below the mean.
In addition, the children with CIs also showed significantly low performance on other tests on the SIPT, especially on tests associated with the VPBIS pattern of sensory integration dysfunction. Although lower performance on Standing and Walking Balance and the depressed PRN scores were not surprising, given previous research (Jacot et al., 2009; Jerome et al., 2013; Shall, 2009; Zhou et al., 2009), the significantly lower scores on the other tests associated with the VPBIS pattern (i.e., Bilateral Motor Coordination, Sequencing Praxis, and Motor Accuracy) and the significantly poorer performance on Design Copying suggest that children with CIs may have a pattern of sensory integration dysfunction that has not been fully understood and addressed.
Several possible explanations indicate why the children with CI were not significantly different from the norms on Oral Praxis and Graphesthesia, two tests that are generally associated with the VPBIS pattern. One is that these two tests are also highly associated with the somatodyspraxia pattern, and the CI group did not show scores that suggested the presence of this pattern. In addition, a possible hypothesis for better performance on the Oral Praxis test in the CI group is that this test requires facial imitation, and both Oral Praxis and Graphesthesia require tactile perception. Both facial imitation and tactile perception may be more highly developed in children who are compensating for the loss of other sensory input, such as hearing.
The SPM and SP results show the majority of children to be in the typical category. In the vestibular section, 60% of the children scored in the typical range, with only 20% in the definite difference category (n = 20). However, because these questionnaire measures tend to reflect responses to sensation as described by parents, rather than actual sensory perception or motor abilities, it would be expected that significant issues with vestibular processing would not be apparent to them. The items regarding vestibular function in the questionnaires tend to reflect hyperresponsivity to sensation—for example, becoming anxious when one’s head is tipped back. Because children with CIs seem to show signs of poor vestibular processing versus heightened reactivity to movement, the questions on the SPM and SP are not likely to capture the type of vestibular dysfunction children with CIs experience.
The results of the PDMS and DP–3 suggest that the children with CI did not show severe or global developmental delays. On both measures, the majority of children were in the typical descriptive category in each subtest. The fact that the Communication subtest of the DP–3 reflected a greater degree of delay is not surprising because this finding would be expected for children with hearing loss. The small to moderate percentage of children with CI who scored in the below average or much below average range on other developmental areas suggests that although some delays may be present in this population, global developmental delays were not a concern overall.
Because the children with CI share characteristics of the VPBIS pattern of sensory integrative dysfunction, this study verifies previous findings that children with CIs are at risk for decreased vestibular function, including difficulties in standing and walking balance and attenuated postrotary nystagmus. The results of this study expand our understanding by suggesting difficulty in additional areas included in the VPBIS pattern, such as postural, ocular, bilateral integration, and sequencing issues. The scores on the SIPT suggest that other sensory integrative patterns such as visuodyspraxia, somatodyspraxia, or somatosensory perception deficits are not prevalent in this population.
Children with poor vestibular processing may have trouble sitting still, often appearing to engage in excessive movement (Schaaf et al., 2010). Adequate vestibular processing is very important for functions including maintenance of postural tone and equilibrium; coordination of head, eye, and hand movements; and stabilization of the eyes while moving the head and sitting upright (Lane, 2002). These difficulties can affect a child’s ability to be successful in other important activities, such as sitting at a desk at school or playing a board game with friends, and as such are best addressed as early as possible.
Limitations and Recommendations for Future Research
This study’s generalizability has some limitations. The sample size was small; only 18 records had SIPT scores, 11 had SP scores, 9 had SPM scores, 32 had DP–3 scores, and 11 to 22 had scores for each subtest of the PDMS. Some children were not able to complete all the tests, and some parents did not return forms, limiting the sample size further. Normative scores were used as a comparison rather than a matched sample. In addition, records were not fully complete in defining individual causes for hearing loss. Future investigation would ideally include a larger sample size, a control group with typically hearing children matched in age and demographics, and a comparison of performance of children before and after CI implantation.
Implications for Occupational Therapy Practice
These findings demonstrate that children with CIs may have functional limitations related to poor vestibular functioning similar to children with VPBIS. Findings from this study also have the following implications for occupational therapy practice:
Occupational therapy practitioners working with children with CIs should consider evaluating sensory integration dysfunction in the assessment process.
The SIPT can be important in identifying patterns such as VPBIS in children with CI.
Practitioners should consider over- or underresponsiveness to various types of sensation (as measured by instruments such as the SP and SPM) during assessment because these issues may be present in some children with CI.
Conclusion
The results of this study suggest that children with CIs may demonstrate challenges that are consistent with the VPBIS pattern of sensory integrative dysfunction. Identification of this pattern requires specific measures of vestibular, postural–ocular, bilateral, and sequencing functions. Because the VPBIS pattern has important implications for occupational performance, occupational therapy practitioners can play an essential role in identifying challenges that have not been routinely addressed in children with CIs. In addition, collaboration with other service providers would be useful in planning and implementing effective and comprehensive interventions.
Footnotes
Acknowledgements
We thank the occupational therapists, physical therapists, speech–language pathologists, audiologists, teachers, and parents who completed assessments for this study.