Cochlear implants

Sensory Integration Functions of Children With Cochlear Implants AnjaLi Carrasco Koester, Zoe Mailloux, Gina Geppert Coleman, Annie Baltazar Mori, Steven M. Paul, Erna Blanche, Jill A. Muhs, Deborah Lim, Sharon A. Cermak

MeSH TERMS  cochlear implants  sensation  sensation disorders  sensory aids  vestibular diseases

AnjaLi Carrasco Koester, OTD, OTR/L, is Occupational Therapist, Pediatric Therapy Network and KidAbilities, 1815 West 213th Street, No. 100, Torrance, CA 90501; [email protected]

OBJECTIVE. We investigated sensory integration (SI) function in children with cochlear implants (CIs). METHOD. We analyzed deidentified records from 49 children ages 7 mo to 83 mo with CIs. Records included Sensory Integration and Praxis Tests (SIPT), Sensory Processing Measure (SPM), Sensory Profile (SP), Developmental Profile 3 (DP–3), and Peabody Developmental Motor Scales (PDMS), with scores depending on participants’ ages. We compared scores with normative population mean scores and with previously identified patterns of SI dysfunction.

RESULTS. One-sample t tests revealed significant differences between children with CIs and the normative population on the majority of the SIPT items associated with the vestibular and proprioceptive bilateral integration and sequencing (VPBIS) pattern. Available scores for children with CIs on the SPM, SP, DP–3, and PDMS indicated generally typical ratings. CONCLUSION. SIPT scores in a sample of children with CIs reflected the VPBIS pattern of SI dysfunction, demonstrating the need for further examination of SI functions in children with CIs during occupational therapy assessment and intervention planning. Koester, A. C., Mailloux, Z., Coleman, G. G., Mori, A. B., Paul, S. M., Blanche, E., . . . Cermak, S. A. (2014). Sensory integration functions of children with cochlear implants. American Journal of Occupational Therapy, 68, 562– 569. http://dx.doi.org/10.5014/ajot.2014.012187

Zoe Mailloux, OTD, OTR/L, FAOTA, is Program and Professional Development Consultant, Private Practice, Redondo Beach, CA. Gina Geppert Coleman, MA, OTR/L, is Occupational Therapist, KidAbilities, El Segundo, CA. Annie Baltazar Mori, OTD, OTR/L, is Occupational Therapist and Owner, PlaySense Inc., Redondo Beach, CA. Steven M. Paul, PhD, is Principal Statistician, University of California San Francisco School of Nursing, San Francisco. Erna Blanche, PhD, OTR/L, FAOTA, is Associate . Professor of Clinical Practice, Division of Occupational Science and Occupational Therapy, University of Southern California, Los Angeles. Jill A. Muhs, MSE, MEd, is Vice President, Programs, John Tracy Clinic, Los Angeles, CA. Deborah Lim, MA, CCC-SLP, is Speech–Language Pathologist, Pediatric Therapy Network, Redondo Beach, CA. Sharon A. Cermak, EdD, OTR/L, FAOTA, is Professor of Occupational Science and Occupational Therapy, University of Southern California, Los Angeles.

C

ochlear 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

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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,

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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: 1. Will children with CIs exhibit deficits on the SIPT associated with the VPBIS pattern of sensory integrative dysfunction? 2. 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

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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 onesample t test, a two-tailed 5% level of significance was used to interpret p values (a 5 .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. 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. Onesample 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. 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 5 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 5 20) for visual, 55%:45% (n 5 20) for tactile, and 60%:40% (n 5 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 Table 1. Assessments and Number of Records for Each Assessment (N 5 49) Clinical Assessment Sensory Processing Measure, Sensory Profile

Retrieved Data Records 20

Developmental Profile 3

32

Sensory Integration and Praxis Tests

18

Peabody Developmental Motor Scales

32

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Table 2. Comparison of SIPT Scores of 18 Children With Cochlear Implants Ages 50 to 83 Mo With Normative Sample n

Mean Score, CI Group

CI SD

ta

p

Oral Praxis Standing and Walking Balanceb

17 17

20.39 22.20

1.219 0.794

21.309 211.427

.209