International Journal of Audiology 2014; Early Online: 1–8
Original Article
Long-term outcome after cochlear implantation in children with additional developmental disabilities
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Nathalie Wakil*, Elizabeth M. Fitzpatrick*,†, Janet Olds†, David Schramm†,‡ & JoAnne Whittingham† *Faculty of Health Sciences, University of Ottawa, Ontario, Canada, †Children’s Hospital of Eastern Ontario Research Institute, Ontario, Canada, and ‡Department of Otolaryngology, University of Ottawa, Ottawa, Ontario, Canada
Abstract Objective: Candidacy criteria for cochlear implants have expanded to include children with complex developmental disabilities. The aim of this study was to determine the long-term benefits of cochlear implantation for this clinical population. Design: The study involved a retrospective chart review. Study sample: The review identified 21 children with complex disabilities who had received cochlear implants in a pediatric center prior to 2004. Length of cochlear implant use was between 7.3 and 19.0 years. Long-term functional auditory abilities were assessed pre and post-operatively using measures appropriate to the child’s level of functioning. Cognitive assessments and developmental data were also available for the children. Results: Children’s long-term speech recognition outcomes depended highly on their developmental status. Children with severe developmental delay showed no open-set speech recognition abilities while children with mild to moderate delays achieved open-set scores ranging from 48 to 94% on open-set word testing. Five of 13 (38%) children with complex needs had discontinued use of their cochlear implant. Conclusions: Long-term speech recognition abilities following cochlear implantation for children with complex developmental issues seem to be highly related to their developmental profile. Developmental status is an important consideration in counselling families as part of the cochlear implant decision process.
Key Words: Children; hearing loss; cochlear implants; additional disabilities; outcomes
Cochlear implants have become a standard intervention for children with severe to profound hearing loss. As this intervention has become more common, more candidates for implants present with increasingly complex medical and developmental profiles in addition to severe to profound hearing loss (Edwards, 2007; Berrettini et al, 2008; Birman et al, 2012; Meinzen-Derr et al, 2011; Steven et al, 2011). Early cochlear implantation criteria generally excluded individuals with additional disabilities due to the uncertainty around auditory and communication benefits for this population and possibly due to the perceived difficulties related to pre- and post-implant management of these children. For example, in the UK, more than a decade ago, children with cochlear implants were reported to have fewer additional disabilities compared to other children with hearing loss (Fortnum et al, 2002). A survey of all Canadian pediatric centers indicated that only six children with complex developmental needs received cochlear implants prior to 2000, but that there was a substantial increase after that time (Fitzpatrick & Brewster, 2008).
Birman et al (2012) recently reported that one-third of 96 children receiving implants in a large pediatric center in Australia over a oneyear period had additional disabilities. It is well documented that a substantial proportion of children with hearing loss also have additional developmental disabilities, although the prevalence varies depending on the definition of complex disabilities. Studies have generally reported that up to 40% of children with sensorineural hearing loss have multiple medical issues or developmental disabilities (Van Naarden et al, 1999; Picard, 2004; Gallaudet Research Institute, 2011). Given the trend towards universal newborn hearing screening and earlier cochlear implantation (12 months of age or less), it is possible that an increasing number of children receive implants before certain disabilities and conditions that affect spoken language development are identified (Birman et al, 2012). This is likely due to the difficulty of diagnosing some developmental disabilities in the early years. For example, a substantial number of children with autism spectrum disorder are diagnosed
Correspondence: Elizabeth M. Fitzpatrick, Faculty of Health Sciences, University of Ottawa, Children’s Hospital of Eastern Ontario Research Institute, 451 Smyth Road, Ottawa, ON K1H 8M5, Canada. E-mail: [email protected] (Received 26 November 2013; accepted 14 March 2014 ) ISSN 1499-2027 print/ISSN 1708-8186 online © 2014 British Society of Audiology, International Society of Audiology, and Nordic Audiological Society DOI: 10.3109/14992027.2014.905716
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Abbreviation
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IT-MAIS Infant toddler meaningful auditory integration scale.
after age 3 years, and over 40% have been identified after 5 years of age in some geographic regions (Ouellette-Kuntz et al, 2009; Centers for Disease Control and Prevention, 2012). There is also some evidence indicating that some children with additional disabilities receive implants later than their typically developing peers as the decision process is likely more complicated due to difficulties around assessment as well as parent and professional uncertainty (Berrettini et al, 2008; McCracken & Turner, 2012). Encouraging results from pediatric cochlear implants have likely motivated both parents and professionals to advocate for early access to hearing through cochlear implantation for all children including those with complex developmental profiles. These trends have led to expanded criteria and to adjustments in expectations for outcomes which may include auditory and quality of life benefits but not necessarily spoken language acquisition for all children with complex needs (Meinzen-Derr et al, 2011; Edwards et al, 2012; McCracken & Turner, 2012). All of these issues make this population of children unique. There has been increasing interest in understanding auditory, communication, and other benefits such as social development and quality of life for these children following cochlear implantation. Consequently, there is a growing body of literature with a specific focus on outcomes of cochlear implants in children with additional disabilities. Given the heterogeneity of this population and the complexity of developmental profiles, these studies tend to encompass children with a vast spectrum of disabilities and complex needs (e.g. cerebral palsy, autism, meningitis, learning disabilities, global developmental delays, CHARGE syndrome). Given the wide range of disabilities, it is not surprising that considerable variability in speech recognition scores, communication skills, and impact on quality of life have been reported (Edwards, 2007; Schramm et al, 2007; Eze et al, 2013). Overall, the literature indicates that auditory and communication outcomes for children with developmental disabilities in addition to hearing loss are poorer than those obtained for children with hearing loss who have no additional disorders (Edwards, 2007; MeinzenDerr et al, 2010; Beer et al, 2012; Cruz et al, 2012; Eze et al, 2013). Predicting outcomes in auditory and communication development after cochlear implantation, given the complexity and diversity of disabilities in children who have received implants, remains challenging (Meinzen-Derr et al, 2011). There is a growing awareness that for children with complex needs, in addition to clinical characteristics such as onset and age of hearing loss identification and age at implantation, severity of developmental delay may have an important impact on outcomes. Edwards et al (2007) noted that speech perception scores reflected the degree of developmental delay in that more severe delays were associated with poorer speech recognition results. More recently, Steven et al (2011) provided additional evidence by examining speech perception outcomes in relation to severity of cognitive impairment for 35 children with cerebral palsy who had received cochlear implants. Scores for children with mild cognitive delay were significantly better than for those with severe delays. However, there was no relationship between speech perception and degree of physical impairment. Other researchers have reported similar interactions or tendencies between severity of cognitive delay and auditory or language outcomes in children with diverse disabilities (Dettman et al, 2004; Meinzen-Derr et al, 2010).
In addition, Nikolopoulos et al (2008) reported a significant relationship between the number of disabilities a child exhibited and speech intelligibility scores. Meinzen-Derr et al (2011) also documented considerably lower scores for children with cochlear implants and additional disabilities than might be expected for their cognitive level compared to peers with normal hearing and developmental disabilities. Taken together, these studies have suggested that the extent of developmental delay may be a strong predictor of auditory and communication outcomes in these children. Several studies also provide evidence that even though children with additional severe developmental disabilities may not achieve consistent speech recognition or oral communication, cochlear implants can enhance broader communication abilities and improve quality of life (Filipo et al, 2004; Olds et al, 2007; Berrettini et al, 2008; Edwards et al, 2012). Donaldson et al (2004) reported that after implantation, children with autism made some progress in areas such as behaviour and interaction. Although there is considerable literature on this population of children who receive cochlear implants, there is still relatively little information from long-term studies as confirmed by Eze et al (2013) in a recent systematic review of the evidence. Long-term data are essential for evaluating children’s functioning with cochlear implants over time, and should provide useful information for counselling parents about the potential benefits and risks of cochlear implantation. This is particularly important due to the increasing number of children with various complex needs and developmental delays who receive cochlear implants. The present study explored long-term outcomes in these individuals. In previous research, we reported outcomes for a group of children with complex medical and developmental needs who had received cochlear implants (Olds et al, 2005). The primary purpose of the present study was to document longterm progress in auditory abilities following cochlear implantation for these children with additional disabilities. Our clinical sample permitted us to examine the differences between children who had been identified with severe developmental delay and those with a mild to moderate developmental delay.
Method Design This study involved a detailed retrospective chart review that involved extracting auditory outcomes and communication outcomes data from medical charts. Data pertaining to the clinical characteristics of the children were collected prospectively as part of a database for all children identified with hearing loss at the Children’s Hospital of Eastern Ontario, and these details were extracted from the database. This study was approved by the Children’s Hospital of Eastern Ontario and the University of Ottawa Research Ethics Boards.
Participants and setting This study was undertaken at the Children’s Hospital of Eastern Ontario in Ottawa, Canada, a tertiary care pediatric medical facility where comprehensive cochlear implant services including assessment, surgery, audiologic and rehabilitation intervention have been in place since 1993. As part of standard care, children considered potential candidates for cochlear implants undergo a comprehensive interdisciplinary team assessment with professionals representing audiology, speech-language intervention, otolaryngology, radiology, and psychology as well as other developmental and medical services (e.g. developmental pediatrician) if required.
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Cochlear implants in children with additional disabilities In 2005, a retrospective chart review was undertaken of the 195 children implanted at the hospital from 1993 to 2004 to identify patients with complex medical and developmental profiles at the time of implantation. Of the 88 children who continued to receive services through the hospital’s cochlear implant program at the time, 25 children were identified as having complex disabilities at implantation. Outcome data were not available for three of the children, as they had not reached the first follow-up interval, leaving 22 children. Children were classified into three groups based on developmental functioning. Consistent with clinical practice standards, all children underwent a cognitive or developmental assessment with a pediatric neuropsychologist or developmental pediatrician. Children who were diagnosed with a global developmental, or cognitive, disability in the mild to moderate category obtained a standard score below 70 (2nd percentile, or more than 2 standard deviations below the average of 100) on a standardized measure of nonverbal functioning (such as the Wechsler scales, or Leiter-R). Children with severe to profound delays were typically seen by a developmental pediatrician or neuropsychologist, and were very limited in their abilities, including in participating in age-appropriate direct assessments. The three groups in the 2005 study included children with: (1) complex medical issues without developmental delay (n ⫽ 4), (2) severe developmental delay (n ⫽ 11), (3) mild to moderate developmental delay (n ⫽ 7). The current study reported in this paper involved an update of the auditory and communication results for the 11 children with severe cognitive delay and the seven children with mild to moderate cognitive delay. Information was not updated for the children with complex medical issues and absence of developmental delay as the auditory benefits documented (Olds et al, 2005) were consistent with those expected for typical developing children who used cochlear implants. Three additional children implanted prior to 2004, but not included in the previous study due to unavailable data, were added to the current long-term-user group. Therefore, a total of 21 children were entered in this study and their medical charts were subjected to a detailed review.
Procedures Prior to receiving cochlear implants, all children had been fitted with hearing aids and enrolled in therapy after confirmation of hearing loss. Children were also followed for auditory rehabilitation in the hospital’s cochlear implant program and were seen more frequently for audiologic care in conjunction with these visits as required. Depending on other medical needs and disabilities, children also received services through other medical/developmental programs in the hospital. Following cochlear implantation, as part of standard clinical procedures, children in this study received annual post-implant clinical audiologic services consisting of speech processor programming and auditory and speech recognition assessment. Consistent with clinical protocols, children’s functional auditory abilities were measured through an auditory questionnaire as well as closed- and/or openset speech recognition tests when possible. Speech recognition tests were selected to establish baseline measures and to monitor progress based on the child’s cognitive and linguistic abilities. Therefore, there was some variation in the test measures used in the clinic due to the range and complexity of developmental profiles in this group of children. The group of children with severe developmental delays was generally evaluated pre- and post-cochlear implantation with the Infant Toddler Meaningful Auditory Integration Scale (IT-MAIS) (Zimmerman-Phillips et al, 2000) with attempts made to conduct
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speech recognition tests when judged clinically appropriate. Auditory abilities for children in the mild to moderate delay group were assessed with closed- and/or open-set speech recognition tests at pre- and post-cochlear implantation. The IT-MAIS is a widely used parent questionnaire for infants and toddlers that probes 10 auditory behaviors in the areas of vocalizations, alerting to sounds, and deriving meaning from sounds. The early speech perception test (ESP) (Moog & Geers, 1990), a closed-set test of pattern perception, spondee and monosyllabic word identification was administered in this study. Assessment of open-set speech understanding included (1) the Glendonald auditory screening procedure (auditory identification of words subtest) which assesses the child’s ability to identify a set of 12 common words (Erber, 1982); (2) the phonetically balanced monosyllabic word list - Kindergarten (PBK) (Haskins, 1949), a word recognition test that requires the child to repeat monosyllabic words; and (3) the hearing in noise test (HINT) (Nilsson et al, 1996), presented in quiet to obtain a measure of open-set sentence recognition. The open-set measures except the GASP (live voice administration) were presented using recorded material at a fixed input level of 70 dB SPL. In addition to speech recognition data, clinical characteristics related to hearing loss (age of diagnosis, severity, etiology), amplification (age cochlear implant, type of device), and other disabilities were recorded using a study-specific form. Information related to disabilities such as syndromes or other medical conditions were only recorded if documented in the child’s medical chart by a specialist such as a neurologist or developmental paediatrician.
Data analysis Given the small sample size, the data are presented primarily descriptively using means, medians, or proportions as appropriate. Statistical analyses were conducted using Statistical Package for the Social Sciences, version 21 (SPSS Inc., Chicago, USA). For the group with severe delay, pre- and post-implant IT-MAIS results were tested for statistical significance with a student’s t-test. Differences between communication mode for the two groups (severe versus mild-moderate delay) were tested for significance using x2 analysis. Statistical significance was accepted at p ⬍ 0.05 and p values are two tailed.
Results Table 1 presents clinical characteristics for the 21 children (15 male, 6 female) in the study. Children were implanted at a median age of 4.3 years (IQR 2.8, 6.5) and were between 1.6 to 11.7 years of age at the time of cochlear implant surgery. Time since cochlear implantation ranged from 7.3 to 19.0 years (mean 11.3 years, SD 3.5). No child in this group had received bilateral cochlear implants, as it was not standard care in the clinic at the time. As shown in Table 1, etiology was known for 18 of the 21 children, seven of whom had a documented syndrome (five of whom spent time in the neonatal intensive care unit (NICU). A summary of the syndromes in this group of children is provided with Table 1. Another five children without syndromes were graduates of the NICU. Two had acquired hearing loss secondary to meningitis, and the remaining four had various etiologies. Table 1 provides details available related to the NICU length of stay, gestational age, and birth weight for children from the NICU. The large majority (16) of the children received a Clarion cochlear implant system while the remaining five had a Nucleus device. Four children, all in the severe developmental delay group also had a diagnosis of cerebral palsy and one had a visual impairment. As shown in Table
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Table 1 Demographic data for 21 participants.
ID
Sex
Age HL confirmed (months)
Age CI (years)
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Children with severe developmental delay CH-277 M 9.6 1.6 CH-222 M 6.7 1.6 CH-287 M 4.3 1.7 CH-272 M 0.5 2.0 CH-252 M 2.8 2.8
CH-253 CH-279 CH-257
F M M
CH-285 CH-246 CH-301 CH-131* CH-200*
M F F M M
Median IQR Children with mild to CH-122 M CH-110 F CH-135 M CH-113 F CH-228 M CH-240 F CH-266 M M CH-184** Median IQR
1.4 4.2 5.3
2.8 4.1 4.3
Years post CI
Device
Etiology
8.5 10.8 8.1 8.6 9.7
Clarion Clarion Clarion Clarion Clarion
NICU graduate Syndromic1 NICU graduate Syndromic Hyperbilirubinemia
18 19 No info 8 2
26 40 33 37 35
No info 3500 2605 2900 2490
9.7 8.4 9.4
Clarion Clarion Nucleus
Syndromic NICU graduate NICU graduate
16 5 No info
38 37 36
2300 2710 2030
Clarion Clarion Clarion Nucleus Clarion
Meningitis Syndromic Syndromic Meningitis Syndromic
NA 1 No info NA NA
NA 40 37 NA NA
NA 3178 2469 NA NA
Clarion Nucleus Clarion Nucleus Clarion Clarion Clarion Nucleus
ENT anomaly Unknown Unknown Syndromic NICU graduate Unknown Familial/genetic Prenatal rubella
NA NA NA NA 17 NA NA NA
NA NA NA NA 25 NA NA NA
NA NA NA NA 707 NA NA NA
4.4 4.8 8.1 0.8 6.6 9.9 11.2 11.3 7.3 16.4 1.8 15.5 18.4 4.4 11.6 4.4 2.8 9.4 (2.8, 9.6) (1.8, 4.4) (8.4, 9.9) moderate developmental delay 13.9 3.2 16.8 15.8 4.3 19.0 29.4 5.0 15.2 25.8 6.5 18.3 8.8 6.8 10.5 11.6 7.2 10.1 71.4 11.7 8.9 2.0 5.8 12.2 14.9 6.2 13.7 (10.9, 26.7) (4.8, 6.9) (10.4, 17.2)
NICU LOS (weeks) GA (weeks) BW (grams)
Additional conditions
Cerebral palsy Cerebral palsy Cerebral palsy, auditory neuropathy Cerebral palsy Auditory neuropathy
HL: Hearing loss; CI: Cochlear implant; NICU: Neonatal intensive care unit; ENT: Ear, nose, and throat; LOS: Length of stay; GA: Gestational age; BW: Birth weight; NA: Not applicable; IQR: Interquartile range. 1Syndromes in this sample included one Moebius, one Goldenhar, one Refsum, and four CHARGE. *Two children with complex profiles (insufficient diagnostic clarity), not categorized on basis of a developmental assessment. **Child with complex profile (insufficient diagnostic clarity), not categorized on basis of a developmental assessment.
1, children in the severe group were younger at implantation (median 2.8 years, IQR 1.8, 4.4) and had used their implant for a shorter period of time at the time of the study. The children in the mildmoderate group received their implants at a median age of 6.2 years (IQR 4.8, 6.9), and all had used their implants for more than 8.9 years (range 8.9 to 19.0). These differences likely reflect program practices in the early years of cochlear implantation whereby children with severe disabilities were less likely to undergo cochlear implantation (Fitzpatrick & Brewster, 2008). Since the measures used and the results documented showed important differences between the groups with severe and mild to moderate delays, our findings are presented separately for these two groups of children. Medical chart documentation for the three additional children with long-term cochlear-implant use (CH-131, CH-200, and CH-184) was carefully reviewed. All three children had undergone assessments and had complex developmental profiles, however, there was insufficient diagnostic clarity to retrospectively classify them in a specific group. For presentation purposes, data for two children (CH-131 and CH-200) are included with the severe group data (n ⫽ 13) (based on auditory function), and for the other child (CH-184) with the mild-moderate group (n ⫽ 8).
Children with severe developmental delay Results for the majority of children (10 of 13) with severe/complex developmental delay consisted of IT-MAIS auditory questionnaires only, as they were unable to complete speech recognition tests. Figure 1 presents questionnaire scores for the 13 children at preimplant, one year post-implant and at the most recent test session and shows that there was considerable variability in the results obtained. At the pre-implant assessment, scores ranged from 0% to 60% with a mean score of 11.8% (SD: 19). After one year of implant use, 11 children (84.6%) showed improvement in scores, although results varied greatly across participants with a mean of 36.9% (SD 27.6). Comparison of pre- and post-implant results at the most recent ITMAIS testing for the group showed a significant improvement in scores (p ⬍.001). At the most recent testing the mean score had improved to 44.8% (SD 30.7), again with wide variability across participants (range 0–85%). Five children (38.5%) showed 10% or more improvement in scores between one year post-implant and later testing, while three children seemed to reach a plateau after the first year, and, in one case (CH-287), a deterioration from 60% at oneyear post-implant to 25% at most recent testing was noted. There was no explanation documented for this decrease in performance. Five of 13 (38.5%) children achieved more than 70% on the IT-MAIS at
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Cochlear implants in children with additional disabilities
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chart for CH-131 and CH-200) and the last chart-recorded information on communication mode or implant status (for non-users). As shown, all of the children were using and continue to use total communication or sign language and/or a form of augmentative communication; in other words, their primary communication mode was non-oral. As shown in Table 2, a total of 5 of the 13 (38.5%) participants were non-users of their device at the time of their last clinical assessment. Two children discontinued implant use within the first 1.5 years and the remaining three within 3 to 4 years after surgery. All of these children were implanted after age 4 years with the exception of one child (child with complex developmental profile), who underwent surgery at age 1.8 years. On closer examination, two of the non-users (CH-246 and CH-200) had syndromes with inner ear anomalies that may have affected auditory performance, and one of these children has since undergone explantation of the cochlear implant. One child (CH-131) had meningitis, but there was no report of ossification in the cochlea, and a full insertion of the electrode array was achieved. Figure 1. Auditory outcomes (IT-MAIS in percent correct) in 13 children with severe developmental delay at pre-implant, one year post-implant, and at most recent assessment. most recent testing but none showed consistent auditory responses for all (100%) of the items on the IT-MAIS despite more than seven years (range 7.3 to 15.5 years) of cochlear implant experience. Two children (CH-279 and CH-131) (15.4%) who had no documented auditory skills pre-implant appeared to have made no progress in auditory skills following cochlear implantation, and a third (CH-200) reached only 15% on the IT-MAIS. In the 2005 study, no child with severe developmental delay had been able to complete closed-set speech recognition testing. In this follow-up study, three children eventually obtained closed-set test scores on the low-verbal version of the early speech perception test. Table 2 also shows the primary mode of communication that children were using at the 2005 test session (and as documented in the Table 2. Communication status for children with severe developmental delay/complex profiles. Participant ID
Age CI (years)
CH-277 CH-222 CH-287 CH-272 CH-252 CH-253 CH-279 CH-257 CH-285 CH-246 CH-301 **CH-200 **CH-131
1.6 1.6 1.7 2.0 2.8 2.8 4.1 4.3 4.8 6.6 11.3 4.4 1.8
Years post CI* 6.4 8.1 3.7 5.9 7.0 8.0 2.8 1.5 1.8 1.9 5.4 3.0 4.0
Communication mode/status, 2005
Communication mode/status, current
AC TC TC TC AC TC/AC TC/non-user TC TC Sign/non-user TC TC Sign
AC TC TC/Non-verbal TC AC/ Sign AC/TC non-user non-user TC non-user TC non-user non-user
CI: Cochlear implant; AC: Augmentative communication; TC ⫽ Total communication; Years post CI: refers to time since implantation at most recent documentation of communication mode/status. *Number of years post-implant at time of last chart documentation of communication mode. **Two complex cases with insufficient diagnostic clarity to specifically classify developmental delay status.
Children with mild to moderate developmental delay Prior to implantation, the children in the mild to moderate developmental delay group (includes one child with unclassified diagnosis) had little or no open-set speech recognition. At the most recent follow-up, ranging from 5.8 to 14.7 years post-implantation, all children achieved very good open-set speech recognition scores ranging from 48% to 94% on the PBK-words monosyllabic words test (Table 3). Only one child scored below 76% on the PBK test. This child (CH-184), who had an etiology of prenatal rubella, did not receive a cochlear implant until age 5.8 years due to geographical location despite very early age of diagnosis of bilateral profound hearing loss. Scores on the HINT sentence test administered in quiet ranged from 60% to 96%. As shown in Table 3, the majority (6 of 8) of children used primarily oral communication while two continued to use a total communication approach, combining sign and oral language to communicate. An examination of communication mode (oral versus non-oral) as a function of category of delay showed a significant difference (p ⬍.001, Fisher’s exact test) between the two groups of children.
Discussion Since the number of children with additional disabilities who receive cochlear implants has substantially increased in recent years, it is important to accumulate evidence about continuing benefits from this technology. The purpose of this study was to document longterm auditory outcomes of all children with developmental delays in one pediatric program who received cochlear implants prior to 2004. Results obtained from children with severe/complex developmental delay showed a range of performance, but most demonstrated relatively limited progress in auditory abilities despite several years of cochlear implant use. In contrast, children who had mild to moderate developmental delay demonstrated open-set speech recognition, consistent with results reported for children without additional disabilities who receive cochlear implants (Fitzpatrick et al, 2012). These findings are in keeping with our earlier findings for this cohort (Olds et al, 2005) and suggest that the degree of developmental delay has a considerable impact on children’s ability to develop auditory skills following cochlear implantation despite many years of implant experience. Despite limited progress in measurable auditory skills, it is important to note that the majority of children with severe delay developed
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N. Wakil et al. Table 3. Speech perception outcomes in children with mild-moderate developmental delay. Most recent ID #
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CH-122 CH-110 CH-135 CH-113 CH-228 CH-240 CH-266 *CH-184
Age CI (years) 3.2 4.3 5.0 6.5 6.8 7.2 11.7 5.8
Pre-CI PBK (%) HINT
PBK
Years post-CI (most recent follow-up)
60% 80% 96% 60% 84% 76% 84% N/A
94% 79% 94% 84% 89% 76% 94% 48%
14.7 11.0 12.4 11.2 9.6 7.5 6.1 11.0
0% PBK 0% PBK 0% PBK 50% GASP-W 16% PBK-W 17% GASP-W 4% PBK-W 0% PBK
Current communication mode TC TC Oral Oral Oral Oral Oral Oral
CI: Cochlear implant; HINT: Hearing in noise test; PBK: Phonetically balanced kindergarten test (words); TC: Total communication; N/A: Not available; *insufficient diagnostic clarity to specifically classify developmental delay status.
some level of basic auditory skills including sound awareness, association of meaning with specific sounds, and vocalization behaviour. These findings are aligned with the information gleaned from a subset of these parents who participated in interviews post-implant and who identified sound awareness, better social engagement, and “connectedness” as observed benefits from cochlear implant use (Olds et al, 2007) and is consistent with other studies (Wiley et al, 2005; McCracken & Turner, 2012). It is noteworthy that in the earlier study, no participants from this severe developmentally delayed group were able to complete closed-set testing but that after several additional years of use, three of the 13 children attained some basic level of closed-set speech recognition. However, three of the 13 children appeared to have made no or minimal progress in basic auditory skills measured by the IT-MAIS. An important finding from this study is that five of the 13 (38%) participants in the severe/complex developmental delay group were documented as non-users at the time of their last assessment. As noted above, all but one of these children were implanted after age 4 years. It is possible that late age at implantation coupled with the presence of a severe developmental disability had an impact on their user status. Previous research from our clinical population suggests that the presence of additional disabilities is one reason accounting for late implantation (Fitzpatrick et al, 2011; McCracken & Turner, 2012). Similarly, O’Brien et al (2010) reported that 15 of 40 children in their clinical population with complex medical issues and comorbid conditions did not achieve consistent cochlear implant use, including seven who became non-users. On closer examination of our data, it is noteworthy that four of the five children who became non-users were either unable to be assessed or had obtained less than 10% on the IT-MAIS questionnaire at one year post-implantation. The other child obtained an IT-MAIS score of 28% by one year post-implant with no further auditory progress measured. Therefore, lack of auditory progress was apparent at an early stage for these children, and our research suggests that early results on an auditory questionnaire such as the IT-MAIS may be useful in predicting longer-term outcomes for this group of children, and our findings also show that these children are unlikely to develop language using oral communication skills alone, as all were using either total communication or augmentative communication methods. This finding is consistent with an earlier study by Pyman et al (2000), which reported that children with a cochlear implant and multiple disabilities have a tendency to use a total communication approach in comparison to children with cochlear implants and no disability.
Examination of chart data for the long-term users with a mild to moderate developmental delay showed markedly different results. These children progressed from little or no speech detection preimplant to high levels of open-set speech recognition, and the majority communicated using spoken language only. These outcomes suggest that cochlear implant technology provides children with a mild to moderate developmental delay with speech understanding and the potential to develop oral communication skills. This study has some limitations that should be considered in interpreting the findings. The retrospective nature and the use of clinical data meant that consistent outcomes data were not available at each follow-up for each child, making it difficult to map out an exact trajectory of auditory development. Although there is a standard protocol in the clinic, data were sometimes not collected likely due to the lack of auditory progress and the inherent difficulties encountered in test sessions with some children with multiple disabilities. A further limitation is the lack of speech-language outcomes available for the group of children with mild to moderate language delays as collection of these long-term data were beyond the scope of this study. It is important to highlight that the age at cochlear implantation for this cohort was later than is typically the current standard in pediatric programs. For some of the older children this is likely due to age criteria that were in place at the time, but for others it is likely related to the longer candidacy decision-making period for children with additional developmental disabilities (Fitzpatrick et al, 2011; McCracken & Turner, 2012). A further potential limitation is that the sample was drawn from only one Canadian pediatric cochlear implant program. However, as one of only three provincial pediatric cochlear implant centers in Ontario, this permitted access to all medical charts and therefore population-based data for this particular catchment area of approximately one million. The findings from this study add to the evidence, particularly contributing long-term data, to support the notion that degree of developmental delay has an important impact on auditory development with a cochlear implant (Edwards, 2007; Eze et al, 2013). Wiley et al (2008) provided support for the relationship between severity of developmental delay and auditory outcomes. While children with an additional disability improved their auditory skills with a cochlear implant, the extent of improvement was highly dependent on their degree of developmental delay. In the study, children with an additional disability and a development quotient of 80 or greater improved similarly to the children with normal development who used cochlear implants, while children with a
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Cochlear implants in children with additional disabilities development quotient inferior to 80 improved at a much slower pace, effectively at half the rate of children with typical development. In a subsequent study of 20 children with additional disabilities, 15 of whom had cognitive delays, Meinzen-Derr et al (2010) also proposed that non-verbal cognitive ability was the best predictor of receptive and expressive language skills after cochlear implantation. In a more recent study comparing language outcomes in children with developmental disabilities who had received cochlear implants and children with normal hearing, Meinzen-Derr et al (2011) concluded that receptive and expressive language levels for the implant group were disproportionate to their cognitive levels. These children had used cochlear implants for various periods up to 68 months. There was a wide discrepancy of 20 quotient points or more between achieved and expected language outcomes for the children with cochlear implants based on language results for the comparison group of children with normal hearing matched for age and non-verbal cognitive abilities. Our study contributes long-term outcomes that, when taken together with the research over the past decade (Eze et al, 2013), provides evidence for an important relationship between auditory and communication abilities and severity of developmental delay. This study adds to the growing body of literature and strengthens the notion that perhaps the most important predictor of potential auditory-based outcomes is severity of cognitive delay. This information may be particularly useful in counselling families of children with additional disabilities who are considering cochlear implants and will help them weigh the potential long-term benefits versus the risks and challenges related to using and maintaining a cochlear implant. It also points to the importance of comprehensive cognitive and developmental assessments for these children in the context of a cochlear implant team evaluation so that parents can make an informed decision. The tendency for some children with severe/complex cognitive issues to become non-users as suggested by our study may also be useful information for health systems. However, given the overall small number in this sample, this information must be interpreted with caution and points to the need for further long-term documentation of use for larger numbers of children. These long-term data are important for establishing realistic outcomes for future candidates. Combined with parent perceptions of benefits obtained from qualitative research (Wiley et al, 2005; Olds et al, 2007; McCracken & Turner, 2012), these studies help define benefits that can be expected from cochlear implants. Further long-term studies should continue to measure progress in these special groups so that realistic expectations and benchmarks can be established. These studies can also add to the dialog about defining appropriate expectations and outcomes for children with severe developmental disabilities. There is ongoing discussion about whether typical assessments conducted with these children provide useful information, and our findings lend support to the need for other instruments that tap auditory and non-auditory development in these children. Several researchers have underscored that for children with additional disabilities who receive cochlear implants, the meaning of success should be redefined and the development of measurement tools expanded to include a range of outcomes (Wiley et al, 2005; Beer et al, 2012; Edwards et al, 2012; Eze et al, 2013; Hayward et al, 2013). Long-term data from our study supports the need for other measurement tools to help practitioners and policy makers define important and broader benefits that extend beyond auditory and spoken communication outcomes for children with severe additional disabilities.
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Acknowledgements We would like to acknowledge the assistance of Julia Ham in the preparation of this manuscript. We also thank the audiologists at the Children’s Hospital of Eastern Ontario for their contributions in clarifying chart data. Declaration of interest: The authors report no conflict of interest. The content and writing of the paper were solely the work of the authors. This study was supported in part by a Canadian Institutes of Health Research Grant and a Canadian Child Health Clinician Scientist Career Enhancement Award to E.F. Funding for the Child Hearing Lab is gratefully acknowledged from the Masonic Foundation of Ontario.
References Beer J., Harris M.S., Kronenberger W.G., Holt R.F. & Pisoni D.B. 2012. Auditory skills, language development, and adaptive behavior of children with cochlear implants and additional disabilities. Int J Audiol, 51, 491–498. Berrettini S., Forli F., Genovese E., Santarelli R., Arslan E. et al. 2008. Cochlear implantation in deaf children with associated disabilities: Challenges and outcomes. Int J Audiol, 47, 199–208. Birman C.S., Elliott E.J. & Gibson W.P.R. 2012. Pediatric cochlear implants: Additional disabilities prevalence, risk factors, and effect on language outcomes. Otol Neurotol, 33, 1347–1352. Centers for Disease Control and Prevention. 2012. Prevalence of autism spectrum disorders - Autism and Developmental Disabilities Monitoring Network, 14 sites, United States. MMWR, 61, 1–19. Cruz I., Vicaria I., Wang N.Y., Niparko J., Quittner A.L. et al. 2012. Language and behavioral outcomes in children with developmental disabilities using cochlear implants. Otol Neurotol, 33, 751–760. Dettman S.J., D Costa W.A., Dowell R.C., Winton E.J., Hill K.L. et al. 2004. Cochlear implants for children with significant residual hearing. Arch Otolaryngol Head Neck Surg, 130, 612–618. Donaldson A.I., Heavner K.S. & Zwolan T.A. 2004. Measuring progress in children with autism spectrum disorder who have cochlear implants. Arch Otolaryngol Head Neck Surg, 130, 666–671. Edwards L., Hill T. & Mahon M. 2012. Quality of life in children and adolescents with cochlear implants and additional needs. Int J Ped Otorhinolaryngol, 76, 851–857. Edwards L.C. 2007. Children with cochlear implants and complex needs: A review of outcome research and psychological practice. J Deaf Studies Deaf Educ, 12, 258–268. Erber N.P. 1982. Auditory Training. Washington, DC: A.G. Bell Association. Eze N., Ofo E., Jiang D. & O’Connor A.F. 2013. Systematic review of cochlear implantation in children with developmental disability. Otol Neurotol, 34, 1385–1393. Filipo R., Bosco E., Mancini P. & Ballantyne D. 2004. Cochlear implants in special cases: Deafness in the presence of disabilities and/or associated problems. Acta Otolaryngol Suppl, 552, 74–80. Fitzpatrick E. & Brewster L. 2008. Pediatric cochlear implantation in Canada: Results of a survey. Can J Speech-lang Pathol Audiol, 32, 29–35. Fitzpatrick E.M., Johnson E. & Durieux-Smith A. 2011. Exploring factors that affect the age of cochlear implantation in children. Int J Ped Otorhinolaryngol, 75, 1082–1087. Fitzpatrick E.M., Olds J., Gaboury I., McCrae R., Schramm D. et al. 2012. Comparison of outcomes in children with hearing aids and cochlear implants. Cochlear Implants Int, 13, 5–15. Fortnum H.M., Marshall D. & Summerfield A.Q. 2002. Epidemiology of the United Kingdom population of hearing-impaired children including characteristics of those with and without cochlear implants: Audiology, aetiology, comorbidity, and affluence. Int J Audiol, 41, 170–179.
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Gallaudet Research Institute. 2011. Regional and National Summary Report of Data from the 2009-2010 Annual Survey of Deaf and Hard of Hearing Children and Youth. Washington. DC: GRI, Gallaudet University. Haskins H.A. 1949. A Phonetically Balanced Test of Speech Discrimination for Children. Unpublished master’s thesis. Evanston, USA: Northwestern University. Hayward D.V., Ritter K., Grueber J. & Howarth T. 2013. Outcomes that matter for children with severe multiple disabilities who use cochlear implants: The first step in an instrument development process. Can J Speech-lang Pathol Audiol, 37, 58–69. McCracken W. & Turner O. 2012. Deaf children with complex needs: Parental experience of access to cochlear implants and ongoing support. Deaf Educ Int, 14, 22–35. Meinzen-Derr J., Wiley S., Grether S. & Choo D.I. 2010. Language performance in children with cochlear implants and additional disabilities. Laryngoscope, 120, 405–413. Meinzen-Derr J., Wiley S., Grether S. & Choo D.I. 2011. Children with cochlear implants and developmental disabilities: A language skills study with developmentally matched hearing peers. Res Dev Disabil, 32, 757–767. Moog J.S. & Geers A.E. 1990. Early Speech Perception Test (ESP). St. Louis, USA: Central Institute for the Deaf. Nikolopoulos T.P., Archbold S.M., Wever C.C. & Lloyd H. 2008. Speech production in deaf implanted children with additional disabilities, and comparison with age-equivalent implanted children without such disorders Int J Ped Otorhinolaryngol, 72, 1823–1828. Nilsson M.J., Soli S.D. & Gelnett D.J. 1996. Development of the Hearing in Noise Test for Children (HINT-C). Los Angeles: House Ear Institute, pp. 1–9. O’Brien L.C.G., Kenna M., Neault M., Clark T.A., Kammerer B. et al. 2010. Not a “sound” decision: Is cochlear implantation always the best choice? Int J Ped Otorhinolaryngol, 74, 1144–1148. Olds J., Fitzpatrick E., Schramm D. & McLean J. 2005. Outcome of Cochlear Implantation in Children with Complex Disabilities. Paper
presented at the Ninth Symposium on Cochlear Implants in Children, Dallas, USA. Olds J., Fitzpatrick E.M., Steacie J., McLean J. & Schramm D. 2007. Parental Perspectives of Outcome after Cochlear Implantation in Children with Complex Disabilities. Paper presented at the 11th International Conference on Cochlear Implants in Children, Charlotte, USA. Ouellette-Kuntz H.M.J., Coo H., Lam M., Yu C.T., Bretenbach M.M. et al. 2009. Age at diagnosis of autism spectrum disorders in four regions of Canada. Can J Public Health, 100, 268–273. Picard M. 2004. Children with permanent hearing loss and associated disabilities: Revisiting current epidemiological data and causes of deafness. Volta Rev, 104, 221–236. Pyman B., Blamey P., Lacy P., Clark G. & Dowell R. 2000. The development of speech perception in children using cochlear implants: Effects of etiologic factors and delayed milestones. Am J Otol, 21, 57–61. Schramm D., Fitzpatrick E., Olds J. & Sampson M. 2007. Systematic Review of Cochlear Implants in Children with Multiple Disabilities. Paper presented at the 11th International Conference on Cochlear Implants in Children, Charlotte, USA. Steven R.A., Green K.M.J., Broomfield S.J., Henderson L.A., Ramsden R.T. et al. 2011. Cochlear implantation in children with cerebral palsy. Int J Ped Otorhinolaryngol, 75, 1427–1430. Van Naarden K., Decoufle P. & Caldwell K. 1999. Prevalence and characteristics of children with serious hearing impairment in metropolitan Atlanta, 1991–1993. Pediatrics, 103, 570–575. Wiley S., Jahnke M., Meinzen-Derr J. & Choo D. 2005. Perceived qualitative benefits of cochlear implants in children with multi-handicaps. Int J Ped Otorhinolaryngol, 69, 791–798. Wiley S., Meinzen-Derr J. & Choo D. 2008. Auditory skills development among children with developmental delay and cochlear implants. Ann Otol Rhinol Laryngol, 117, 711–718. Zimmerman-Phillips S., Robbins A.M. & Osberge M.J. 2000. Assessing cochlear implant benefit in very young children. Annals Otol Rhinol Laryngol, 109 (Suppl. 185), 42–43.
Original Article
Long-term outcome after cochlear implantation in children with additional developmental disabilities
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Nathalie Wakil*, Elizabeth M. Fitzpatrick*,†, Janet Olds†, David Schramm†,‡ & JoAnne Whittingham† *Faculty of Health Sciences, University of Ottawa, Ontario, Canada, †Children’s Hospital of Eastern Ontario Research Institute, Ontario, Canada, and ‡Department of Otolaryngology, University of Ottawa, Ottawa, Ontario, Canada
Abstract Objective: Candidacy criteria for cochlear implants have expanded to include children with complex developmental disabilities. The aim of this study was to determine the long-term benefits of cochlear implantation for this clinical population. Design: The study involved a retrospective chart review. Study sample: The review identified 21 children with complex disabilities who had received cochlear implants in a pediatric center prior to 2004. Length of cochlear implant use was between 7.3 and 19.0 years. Long-term functional auditory abilities were assessed pre and post-operatively using measures appropriate to the child’s level of functioning. Cognitive assessments and developmental data were also available for the children. Results: Children’s long-term speech recognition outcomes depended highly on their developmental status. Children with severe developmental delay showed no open-set speech recognition abilities while children with mild to moderate delays achieved open-set scores ranging from 48 to 94% on open-set word testing. Five of 13 (38%) children with complex needs had discontinued use of their cochlear implant. Conclusions: Long-term speech recognition abilities following cochlear implantation for children with complex developmental issues seem to be highly related to their developmental profile. Developmental status is an important consideration in counselling families as part of the cochlear implant decision process.
Key Words: Children; hearing loss; cochlear implants; additional disabilities; outcomes
Cochlear implants have become a standard intervention for children with severe to profound hearing loss. As this intervention has become more common, more candidates for implants present with increasingly complex medical and developmental profiles in addition to severe to profound hearing loss (Edwards, 2007; Berrettini et al, 2008; Birman et al, 2012; Meinzen-Derr et al, 2011; Steven et al, 2011). Early cochlear implantation criteria generally excluded individuals with additional disabilities due to the uncertainty around auditory and communication benefits for this population and possibly due to the perceived difficulties related to pre- and post-implant management of these children. For example, in the UK, more than a decade ago, children with cochlear implants were reported to have fewer additional disabilities compared to other children with hearing loss (Fortnum et al, 2002). A survey of all Canadian pediatric centers indicated that only six children with complex developmental needs received cochlear implants prior to 2000, but that there was a substantial increase after that time (Fitzpatrick & Brewster, 2008).
Birman et al (2012) recently reported that one-third of 96 children receiving implants in a large pediatric center in Australia over a oneyear period had additional disabilities. It is well documented that a substantial proportion of children with hearing loss also have additional developmental disabilities, although the prevalence varies depending on the definition of complex disabilities. Studies have generally reported that up to 40% of children with sensorineural hearing loss have multiple medical issues or developmental disabilities (Van Naarden et al, 1999; Picard, 2004; Gallaudet Research Institute, 2011). Given the trend towards universal newborn hearing screening and earlier cochlear implantation (12 months of age or less), it is possible that an increasing number of children receive implants before certain disabilities and conditions that affect spoken language development are identified (Birman et al, 2012). This is likely due to the difficulty of diagnosing some developmental disabilities in the early years. For example, a substantial number of children with autism spectrum disorder are diagnosed
Correspondence: Elizabeth M. Fitzpatrick, Faculty of Health Sciences, University of Ottawa, Children’s Hospital of Eastern Ontario Research Institute, 451 Smyth Road, Ottawa, ON K1H 8M5, Canada. E-mail: [email protected] (Received 26 November 2013; accepted 14 March 2014 ) ISSN 1499-2027 print/ISSN 1708-8186 online © 2014 British Society of Audiology, International Society of Audiology, and Nordic Audiological Society DOI: 10.3109/14992027.2014.905716
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Abbreviation
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IT-MAIS Infant toddler meaningful auditory integration scale.
after age 3 years, and over 40% have been identified after 5 years of age in some geographic regions (Ouellette-Kuntz et al, 2009; Centers for Disease Control and Prevention, 2012). There is also some evidence indicating that some children with additional disabilities receive implants later than their typically developing peers as the decision process is likely more complicated due to difficulties around assessment as well as parent and professional uncertainty (Berrettini et al, 2008; McCracken & Turner, 2012). Encouraging results from pediatric cochlear implants have likely motivated both parents and professionals to advocate for early access to hearing through cochlear implantation for all children including those with complex developmental profiles. These trends have led to expanded criteria and to adjustments in expectations for outcomes which may include auditory and quality of life benefits but not necessarily spoken language acquisition for all children with complex needs (Meinzen-Derr et al, 2011; Edwards et al, 2012; McCracken & Turner, 2012). All of these issues make this population of children unique. There has been increasing interest in understanding auditory, communication, and other benefits such as social development and quality of life for these children following cochlear implantation. Consequently, there is a growing body of literature with a specific focus on outcomes of cochlear implants in children with additional disabilities. Given the heterogeneity of this population and the complexity of developmental profiles, these studies tend to encompass children with a vast spectrum of disabilities and complex needs (e.g. cerebral palsy, autism, meningitis, learning disabilities, global developmental delays, CHARGE syndrome). Given the wide range of disabilities, it is not surprising that considerable variability in speech recognition scores, communication skills, and impact on quality of life have been reported (Edwards, 2007; Schramm et al, 2007; Eze et al, 2013). Overall, the literature indicates that auditory and communication outcomes for children with developmental disabilities in addition to hearing loss are poorer than those obtained for children with hearing loss who have no additional disorders (Edwards, 2007; MeinzenDerr et al, 2010; Beer et al, 2012; Cruz et al, 2012; Eze et al, 2013). Predicting outcomes in auditory and communication development after cochlear implantation, given the complexity and diversity of disabilities in children who have received implants, remains challenging (Meinzen-Derr et al, 2011). There is a growing awareness that for children with complex needs, in addition to clinical characteristics such as onset and age of hearing loss identification and age at implantation, severity of developmental delay may have an important impact on outcomes. Edwards et al (2007) noted that speech perception scores reflected the degree of developmental delay in that more severe delays were associated with poorer speech recognition results. More recently, Steven et al (2011) provided additional evidence by examining speech perception outcomes in relation to severity of cognitive impairment for 35 children with cerebral palsy who had received cochlear implants. Scores for children with mild cognitive delay were significantly better than for those with severe delays. However, there was no relationship between speech perception and degree of physical impairment. Other researchers have reported similar interactions or tendencies between severity of cognitive delay and auditory or language outcomes in children with diverse disabilities (Dettman et al, 2004; Meinzen-Derr et al, 2010).
In addition, Nikolopoulos et al (2008) reported a significant relationship between the number of disabilities a child exhibited and speech intelligibility scores. Meinzen-Derr et al (2011) also documented considerably lower scores for children with cochlear implants and additional disabilities than might be expected for their cognitive level compared to peers with normal hearing and developmental disabilities. Taken together, these studies have suggested that the extent of developmental delay may be a strong predictor of auditory and communication outcomes in these children. Several studies also provide evidence that even though children with additional severe developmental disabilities may not achieve consistent speech recognition or oral communication, cochlear implants can enhance broader communication abilities and improve quality of life (Filipo et al, 2004; Olds et al, 2007; Berrettini et al, 2008; Edwards et al, 2012). Donaldson et al (2004) reported that after implantation, children with autism made some progress in areas such as behaviour and interaction. Although there is considerable literature on this population of children who receive cochlear implants, there is still relatively little information from long-term studies as confirmed by Eze et al (2013) in a recent systematic review of the evidence. Long-term data are essential for evaluating children’s functioning with cochlear implants over time, and should provide useful information for counselling parents about the potential benefits and risks of cochlear implantation. This is particularly important due to the increasing number of children with various complex needs and developmental delays who receive cochlear implants. The present study explored long-term outcomes in these individuals. In previous research, we reported outcomes for a group of children with complex medical and developmental needs who had received cochlear implants (Olds et al, 2005). The primary purpose of the present study was to document longterm progress in auditory abilities following cochlear implantation for these children with additional disabilities. Our clinical sample permitted us to examine the differences between children who had been identified with severe developmental delay and those with a mild to moderate developmental delay.
Method Design This study involved a detailed retrospective chart review that involved extracting auditory outcomes and communication outcomes data from medical charts. Data pertaining to the clinical characteristics of the children were collected prospectively as part of a database for all children identified with hearing loss at the Children’s Hospital of Eastern Ontario, and these details were extracted from the database. This study was approved by the Children’s Hospital of Eastern Ontario and the University of Ottawa Research Ethics Boards.
Participants and setting This study was undertaken at the Children’s Hospital of Eastern Ontario in Ottawa, Canada, a tertiary care pediatric medical facility where comprehensive cochlear implant services including assessment, surgery, audiologic and rehabilitation intervention have been in place since 1993. As part of standard care, children considered potential candidates for cochlear implants undergo a comprehensive interdisciplinary team assessment with professionals representing audiology, speech-language intervention, otolaryngology, radiology, and psychology as well as other developmental and medical services (e.g. developmental pediatrician) if required.
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Cochlear implants in children with additional disabilities In 2005, a retrospective chart review was undertaken of the 195 children implanted at the hospital from 1993 to 2004 to identify patients with complex medical and developmental profiles at the time of implantation. Of the 88 children who continued to receive services through the hospital’s cochlear implant program at the time, 25 children were identified as having complex disabilities at implantation. Outcome data were not available for three of the children, as they had not reached the first follow-up interval, leaving 22 children. Children were classified into three groups based on developmental functioning. Consistent with clinical practice standards, all children underwent a cognitive or developmental assessment with a pediatric neuropsychologist or developmental pediatrician. Children who were diagnosed with a global developmental, or cognitive, disability in the mild to moderate category obtained a standard score below 70 (2nd percentile, or more than 2 standard deviations below the average of 100) on a standardized measure of nonverbal functioning (such as the Wechsler scales, or Leiter-R). Children with severe to profound delays were typically seen by a developmental pediatrician or neuropsychologist, and were very limited in their abilities, including in participating in age-appropriate direct assessments. The three groups in the 2005 study included children with: (1) complex medical issues without developmental delay (n ⫽ 4), (2) severe developmental delay (n ⫽ 11), (3) mild to moderate developmental delay (n ⫽ 7). The current study reported in this paper involved an update of the auditory and communication results for the 11 children with severe cognitive delay and the seven children with mild to moderate cognitive delay. Information was not updated for the children with complex medical issues and absence of developmental delay as the auditory benefits documented (Olds et al, 2005) were consistent with those expected for typical developing children who used cochlear implants. Three additional children implanted prior to 2004, but not included in the previous study due to unavailable data, were added to the current long-term-user group. Therefore, a total of 21 children were entered in this study and their medical charts were subjected to a detailed review.
Procedures Prior to receiving cochlear implants, all children had been fitted with hearing aids and enrolled in therapy after confirmation of hearing loss. Children were also followed for auditory rehabilitation in the hospital’s cochlear implant program and were seen more frequently for audiologic care in conjunction with these visits as required. Depending on other medical needs and disabilities, children also received services through other medical/developmental programs in the hospital. Following cochlear implantation, as part of standard clinical procedures, children in this study received annual post-implant clinical audiologic services consisting of speech processor programming and auditory and speech recognition assessment. Consistent with clinical protocols, children’s functional auditory abilities were measured through an auditory questionnaire as well as closed- and/or openset speech recognition tests when possible. Speech recognition tests were selected to establish baseline measures and to monitor progress based on the child’s cognitive and linguistic abilities. Therefore, there was some variation in the test measures used in the clinic due to the range and complexity of developmental profiles in this group of children. The group of children with severe developmental delays was generally evaluated pre- and post-cochlear implantation with the Infant Toddler Meaningful Auditory Integration Scale (IT-MAIS) (Zimmerman-Phillips et al, 2000) with attempts made to conduct
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speech recognition tests when judged clinically appropriate. Auditory abilities for children in the mild to moderate delay group were assessed with closed- and/or open-set speech recognition tests at pre- and post-cochlear implantation. The IT-MAIS is a widely used parent questionnaire for infants and toddlers that probes 10 auditory behaviors in the areas of vocalizations, alerting to sounds, and deriving meaning from sounds. The early speech perception test (ESP) (Moog & Geers, 1990), a closed-set test of pattern perception, spondee and monosyllabic word identification was administered in this study. Assessment of open-set speech understanding included (1) the Glendonald auditory screening procedure (auditory identification of words subtest) which assesses the child’s ability to identify a set of 12 common words (Erber, 1982); (2) the phonetically balanced monosyllabic word list - Kindergarten (PBK) (Haskins, 1949), a word recognition test that requires the child to repeat monosyllabic words; and (3) the hearing in noise test (HINT) (Nilsson et al, 1996), presented in quiet to obtain a measure of open-set sentence recognition. The open-set measures except the GASP (live voice administration) were presented using recorded material at a fixed input level of 70 dB SPL. In addition to speech recognition data, clinical characteristics related to hearing loss (age of diagnosis, severity, etiology), amplification (age cochlear implant, type of device), and other disabilities were recorded using a study-specific form. Information related to disabilities such as syndromes or other medical conditions were only recorded if documented in the child’s medical chart by a specialist such as a neurologist or developmental paediatrician.
Data analysis Given the small sample size, the data are presented primarily descriptively using means, medians, or proportions as appropriate. Statistical analyses were conducted using Statistical Package for the Social Sciences, version 21 (SPSS Inc., Chicago, USA). For the group with severe delay, pre- and post-implant IT-MAIS results were tested for statistical significance with a student’s t-test. Differences between communication mode for the two groups (severe versus mild-moderate delay) were tested for significance using x2 analysis. Statistical significance was accepted at p ⬍ 0.05 and p values are two tailed.
Results Table 1 presents clinical characteristics for the 21 children (15 male, 6 female) in the study. Children were implanted at a median age of 4.3 years (IQR 2.8, 6.5) and were between 1.6 to 11.7 years of age at the time of cochlear implant surgery. Time since cochlear implantation ranged from 7.3 to 19.0 years (mean 11.3 years, SD 3.5). No child in this group had received bilateral cochlear implants, as it was not standard care in the clinic at the time. As shown in Table 1, etiology was known for 18 of the 21 children, seven of whom had a documented syndrome (five of whom spent time in the neonatal intensive care unit (NICU). A summary of the syndromes in this group of children is provided with Table 1. Another five children without syndromes were graduates of the NICU. Two had acquired hearing loss secondary to meningitis, and the remaining four had various etiologies. Table 1 provides details available related to the NICU length of stay, gestational age, and birth weight for children from the NICU. The large majority (16) of the children received a Clarion cochlear implant system while the remaining five had a Nucleus device. Four children, all in the severe developmental delay group also had a diagnosis of cerebral palsy and one had a visual impairment. As shown in Table
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Table 1 Demographic data for 21 participants.
ID
Sex
Age HL confirmed (months)
Age CI (years)
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Children with severe developmental delay CH-277 M 9.6 1.6 CH-222 M 6.7 1.6 CH-287 M 4.3 1.7 CH-272 M 0.5 2.0 CH-252 M 2.8 2.8
CH-253 CH-279 CH-257
F M M
CH-285 CH-246 CH-301 CH-131* CH-200*
M F F M M
Median IQR Children with mild to CH-122 M CH-110 F CH-135 M CH-113 F CH-228 M CH-240 F CH-266 M M CH-184** Median IQR
1.4 4.2 5.3
2.8 4.1 4.3
Years post CI
Device
Etiology
8.5 10.8 8.1 8.6 9.7
Clarion Clarion Clarion Clarion Clarion
NICU graduate Syndromic1 NICU graduate Syndromic Hyperbilirubinemia
18 19 No info 8 2
26 40 33 37 35
No info 3500 2605 2900 2490
9.7 8.4 9.4
Clarion Clarion Nucleus
Syndromic NICU graduate NICU graduate
16 5 No info
38 37 36
2300 2710 2030
Clarion Clarion Clarion Nucleus Clarion
Meningitis Syndromic Syndromic Meningitis Syndromic
NA 1 No info NA NA
NA 40 37 NA NA
NA 3178 2469 NA NA
Clarion Nucleus Clarion Nucleus Clarion Clarion Clarion Nucleus
ENT anomaly Unknown Unknown Syndromic NICU graduate Unknown Familial/genetic Prenatal rubella
NA NA NA NA 17 NA NA NA
NA NA NA NA 25 NA NA NA
NA NA NA NA 707 NA NA NA
4.4 4.8 8.1 0.8 6.6 9.9 11.2 11.3 7.3 16.4 1.8 15.5 18.4 4.4 11.6 4.4 2.8 9.4 (2.8, 9.6) (1.8, 4.4) (8.4, 9.9) moderate developmental delay 13.9 3.2 16.8 15.8 4.3 19.0 29.4 5.0 15.2 25.8 6.5 18.3 8.8 6.8 10.5 11.6 7.2 10.1 71.4 11.7 8.9 2.0 5.8 12.2 14.9 6.2 13.7 (10.9, 26.7) (4.8, 6.9) (10.4, 17.2)
NICU LOS (weeks) GA (weeks) BW (grams)
Additional conditions
Cerebral palsy Cerebral palsy Cerebral palsy, auditory neuropathy Cerebral palsy Auditory neuropathy
HL: Hearing loss; CI: Cochlear implant; NICU: Neonatal intensive care unit; ENT: Ear, nose, and throat; LOS: Length of stay; GA: Gestational age; BW: Birth weight; NA: Not applicable; IQR: Interquartile range. 1Syndromes in this sample included one Moebius, one Goldenhar, one Refsum, and four CHARGE. *Two children with complex profiles (insufficient diagnostic clarity), not categorized on basis of a developmental assessment. **Child with complex profile (insufficient diagnostic clarity), not categorized on basis of a developmental assessment.
1, children in the severe group were younger at implantation (median 2.8 years, IQR 1.8, 4.4) and had used their implant for a shorter period of time at the time of the study. The children in the mildmoderate group received their implants at a median age of 6.2 years (IQR 4.8, 6.9), and all had used their implants for more than 8.9 years (range 8.9 to 19.0). These differences likely reflect program practices in the early years of cochlear implantation whereby children with severe disabilities were less likely to undergo cochlear implantation (Fitzpatrick & Brewster, 2008). Since the measures used and the results documented showed important differences between the groups with severe and mild to moderate delays, our findings are presented separately for these two groups of children. Medical chart documentation for the three additional children with long-term cochlear-implant use (CH-131, CH-200, and CH-184) was carefully reviewed. All three children had undergone assessments and had complex developmental profiles, however, there was insufficient diagnostic clarity to retrospectively classify them in a specific group. For presentation purposes, data for two children (CH-131 and CH-200) are included with the severe group data (n ⫽ 13) (based on auditory function), and for the other child (CH-184) with the mild-moderate group (n ⫽ 8).
Children with severe developmental delay Results for the majority of children (10 of 13) with severe/complex developmental delay consisted of IT-MAIS auditory questionnaires only, as they were unable to complete speech recognition tests. Figure 1 presents questionnaire scores for the 13 children at preimplant, one year post-implant and at the most recent test session and shows that there was considerable variability in the results obtained. At the pre-implant assessment, scores ranged from 0% to 60% with a mean score of 11.8% (SD: 19). After one year of implant use, 11 children (84.6%) showed improvement in scores, although results varied greatly across participants with a mean of 36.9% (SD 27.6). Comparison of pre- and post-implant results at the most recent ITMAIS testing for the group showed a significant improvement in scores (p ⬍.001). At the most recent testing the mean score had improved to 44.8% (SD 30.7), again with wide variability across participants (range 0–85%). Five children (38.5%) showed 10% or more improvement in scores between one year post-implant and later testing, while three children seemed to reach a plateau after the first year, and, in one case (CH-287), a deterioration from 60% at oneyear post-implant to 25% at most recent testing was noted. There was no explanation documented for this decrease in performance. Five of 13 (38.5%) children achieved more than 70% on the IT-MAIS at
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Cochlear implants in children with additional disabilities
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chart for CH-131 and CH-200) and the last chart-recorded information on communication mode or implant status (for non-users). As shown, all of the children were using and continue to use total communication or sign language and/or a form of augmentative communication; in other words, their primary communication mode was non-oral. As shown in Table 2, a total of 5 of the 13 (38.5%) participants were non-users of their device at the time of their last clinical assessment. Two children discontinued implant use within the first 1.5 years and the remaining three within 3 to 4 years after surgery. All of these children were implanted after age 4 years with the exception of one child (child with complex developmental profile), who underwent surgery at age 1.8 years. On closer examination, two of the non-users (CH-246 and CH-200) had syndromes with inner ear anomalies that may have affected auditory performance, and one of these children has since undergone explantation of the cochlear implant. One child (CH-131) had meningitis, but there was no report of ossification in the cochlea, and a full insertion of the electrode array was achieved. Figure 1. Auditory outcomes (IT-MAIS in percent correct) in 13 children with severe developmental delay at pre-implant, one year post-implant, and at most recent assessment. most recent testing but none showed consistent auditory responses for all (100%) of the items on the IT-MAIS despite more than seven years (range 7.3 to 15.5 years) of cochlear implant experience. Two children (CH-279 and CH-131) (15.4%) who had no documented auditory skills pre-implant appeared to have made no progress in auditory skills following cochlear implantation, and a third (CH-200) reached only 15% on the IT-MAIS. In the 2005 study, no child with severe developmental delay had been able to complete closed-set speech recognition testing. In this follow-up study, three children eventually obtained closed-set test scores on the low-verbal version of the early speech perception test. Table 2 also shows the primary mode of communication that children were using at the 2005 test session (and as documented in the Table 2. Communication status for children with severe developmental delay/complex profiles. Participant ID
Age CI (years)
CH-277 CH-222 CH-287 CH-272 CH-252 CH-253 CH-279 CH-257 CH-285 CH-246 CH-301 **CH-200 **CH-131
1.6 1.6 1.7 2.0 2.8 2.8 4.1 4.3 4.8 6.6 11.3 4.4 1.8
Years post CI* 6.4 8.1 3.7 5.9 7.0 8.0 2.8 1.5 1.8 1.9 5.4 3.0 4.0
Communication mode/status, 2005
Communication mode/status, current
AC TC TC TC AC TC/AC TC/non-user TC TC Sign/non-user TC TC Sign
AC TC TC/Non-verbal TC AC/ Sign AC/TC non-user non-user TC non-user TC non-user non-user
CI: Cochlear implant; AC: Augmentative communication; TC ⫽ Total communication; Years post CI: refers to time since implantation at most recent documentation of communication mode/status. *Number of years post-implant at time of last chart documentation of communication mode. **Two complex cases with insufficient diagnostic clarity to specifically classify developmental delay status.
Children with mild to moderate developmental delay Prior to implantation, the children in the mild to moderate developmental delay group (includes one child with unclassified diagnosis) had little or no open-set speech recognition. At the most recent follow-up, ranging from 5.8 to 14.7 years post-implantation, all children achieved very good open-set speech recognition scores ranging from 48% to 94% on the PBK-words monosyllabic words test (Table 3). Only one child scored below 76% on the PBK test. This child (CH-184), who had an etiology of prenatal rubella, did not receive a cochlear implant until age 5.8 years due to geographical location despite very early age of diagnosis of bilateral profound hearing loss. Scores on the HINT sentence test administered in quiet ranged from 60% to 96%. As shown in Table 3, the majority (6 of 8) of children used primarily oral communication while two continued to use a total communication approach, combining sign and oral language to communicate. An examination of communication mode (oral versus non-oral) as a function of category of delay showed a significant difference (p ⬍.001, Fisher’s exact test) between the two groups of children.
Discussion Since the number of children with additional disabilities who receive cochlear implants has substantially increased in recent years, it is important to accumulate evidence about continuing benefits from this technology. The purpose of this study was to document longterm auditory outcomes of all children with developmental delays in one pediatric program who received cochlear implants prior to 2004. Results obtained from children with severe/complex developmental delay showed a range of performance, but most demonstrated relatively limited progress in auditory abilities despite several years of cochlear implant use. In contrast, children who had mild to moderate developmental delay demonstrated open-set speech recognition, consistent with results reported for children without additional disabilities who receive cochlear implants (Fitzpatrick et al, 2012). These findings are in keeping with our earlier findings for this cohort (Olds et al, 2005) and suggest that the degree of developmental delay has a considerable impact on children’s ability to develop auditory skills following cochlear implantation despite many years of implant experience. Despite limited progress in measurable auditory skills, it is important to note that the majority of children with severe delay developed
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N. Wakil et al. Table 3. Speech perception outcomes in children with mild-moderate developmental delay. Most recent ID #
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CH-122 CH-110 CH-135 CH-113 CH-228 CH-240 CH-266 *CH-184
Age CI (years) 3.2 4.3 5.0 6.5 6.8 7.2 11.7 5.8
Pre-CI PBK (%) HINT
PBK
Years post-CI (most recent follow-up)
60% 80% 96% 60% 84% 76% 84% N/A
94% 79% 94% 84% 89% 76% 94% 48%
14.7 11.0 12.4 11.2 9.6 7.5 6.1 11.0
0% PBK 0% PBK 0% PBK 50% GASP-W 16% PBK-W 17% GASP-W 4% PBK-W 0% PBK
Current communication mode TC TC Oral Oral Oral Oral Oral Oral
CI: Cochlear implant; HINT: Hearing in noise test; PBK: Phonetically balanced kindergarten test (words); TC: Total communication; N/A: Not available; *insufficient diagnostic clarity to specifically classify developmental delay status.
some level of basic auditory skills including sound awareness, association of meaning with specific sounds, and vocalization behaviour. These findings are aligned with the information gleaned from a subset of these parents who participated in interviews post-implant and who identified sound awareness, better social engagement, and “connectedness” as observed benefits from cochlear implant use (Olds et al, 2007) and is consistent with other studies (Wiley et al, 2005; McCracken & Turner, 2012). It is noteworthy that in the earlier study, no participants from this severe developmentally delayed group were able to complete closed-set testing but that after several additional years of use, three of the 13 children attained some basic level of closed-set speech recognition. However, three of the 13 children appeared to have made no or minimal progress in basic auditory skills measured by the IT-MAIS. An important finding from this study is that five of the 13 (38%) participants in the severe/complex developmental delay group were documented as non-users at the time of their last assessment. As noted above, all but one of these children were implanted after age 4 years. It is possible that late age at implantation coupled with the presence of a severe developmental disability had an impact on their user status. Previous research from our clinical population suggests that the presence of additional disabilities is one reason accounting for late implantation (Fitzpatrick et al, 2011; McCracken & Turner, 2012). Similarly, O’Brien et al (2010) reported that 15 of 40 children in their clinical population with complex medical issues and comorbid conditions did not achieve consistent cochlear implant use, including seven who became non-users. On closer examination of our data, it is noteworthy that four of the five children who became non-users were either unable to be assessed or had obtained less than 10% on the IT-MAIS questionnaire at one year post-implantation. The other child obtained an IT-MAIS score of 28% by one year post-implant with no further auditory progress measured. Therefore, lack of auditory progress was apparent at an early stage for these children, and our research suggests that early results on an auditory questionnaire such as the IT-MAIS may be useful in predicting longer-term outcomes for this group of children, and our findings also show that these children are unlikely to develop language using oral communication skills alone, as all were using either total communication or augmentative communication methods. This finding is consistent with an earlier study by Pyman et al (2000), which reported that children with a cochlear implant and multiple disabilities have a tendency to use a total communication approach in comparison to children with cochlear implants and no disability.
Examination of chart data for the long-term users with a mild to moderate developmental delay showed markedly different results. These children progressed from little or no speech detection preimplant to high levels of open-set speech recognition, and the majority communicated using spoken language only. These outcomes suggest that cochlear implant technology provides children with a mild to moderate developmental delay with speech understanding and the potential to develop oral communication skills. This study has some limitations that should be considered in interpreting the findings. The retrospective nature and the use of clinical data meant that consistent outcomes data were not available at each follow-up for each child, making it difficult to map out an exact trajectory of auditory development. Although there is a standard protocol in the clinic, data were sometimes not collected likely due to the lack of auditory progress and the inherent difficulties encountered in test sessions with some children with multiple disabilities. A further limitation is the lack of speech-language outcomes available for the group of children with mild to moderate language delays as collection of these long-term data were beyond the scope of this study. It is important to highlight that the age at cochlear implantation for this cohort was later than is typically the current standard in pediatric programs. For some of the older children this is likely due to age criteria that were in place at the time, but for others it is likely related to the longer candidacy decision-making period for children with additional developmental disabilities (Fitzpatrick et al, 2011; McCracken & Turner, 2012). A further potential limitation is that the sample was drawn from only one Canadian pediatric cochlear implant program. However, as one of only three provincial pediatric cochlear implant centers in Ontario, this permitted access to all medical charts and therefore population-based data for this particular catchment area of approximately one million. The findings from this study add to the evidence, particularly contributing long-term data, to support the notion that degree of developmental delay has an important impact on auditory development with a cochlear implant (Edwards, 2007; Eze et al, 2013). Wiley et al (2008) provided support for the relationship between severity of developmental delay and auditory outcomes. While children with an additional disability improved their auditory skills with a cochlear implant, the extent of improvement was highly dependent on their degree of developmental delay. In the study, children with an additional disability and a development quotient of 80 or greater improved similarly to the children with normal development who used cochlear implants, while children with a
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Cochlear implants in children with additional disabilities development quotient inferior to 80 improved at a much slower pace, effectively at half the rate of children with typical development. In a subsequent study of 20 children with additional disabilities, 15 of whom had cognitive delays, Meinzen-Derr et al (2010) also proposed that non-verbal cognitive ability was the best predictor of receptive and expressive language skills after cochlear implantation. In a more recent study comparing language outcomes in children with developmental disabilities who had received cochlear implants and children with normal hearing, Meinzen-Derr et al (2011) concluded that receptive and expressive language levels for the implant group were disproportionate to their cognitive levels. These children had used cochlear implants for various periods up to 68 months. There was a wide discrepancy of 20 quotient points or more between achieved and expected language outcomes for the children with cochlear implants based on language results for the comparison group of children with normal hearing matched for age and non-verbal cognitive abilities. Our study contributes long-term outcomes that, when taken together with the research over the past decade (Eze et al, 2013), provides evidence for an important relationship between auditory and communication abilities and severity of developmental delay. This study adds to the growing body of literature and strengthens the notion that perhaps the most important predictor of potential auditory-based outcomes is severity of cognitive delay. This information may be particularly useful in counselling families of children with additional disabilities who are considering cochlear implants and will help them weigh the potential long-term benefits versus the risks and challenges related to using and maintaining a cochlear implant. It also points to the importance of comprehensive cognitive and developmental assessments for these children in the context of a cochlear implant team evaluation so that parents can make an informed decision. The tendency for some children with severe/complex cognitive issues to become non-users as suggested by our study may also be useful information for health systems. However, given the overall small number in this sample, this information must be interpreted with caution and points to the need for further long-term documentation of use for larger numbers of children. These long-term data are important for establishing realistic outcomes for future candidates. Combined with parent perceptions of benefits obtained from qualitative research (Wiley et al, 2005; Olds et al, 2007; McCracken & Turner, 2012), these studies help define benefits that can be expected from cochlear implants. Further long-term studies should continue to measure progress in these special groups so that realistic expectations and benchmarks can be established. These studies can also add to the dialog about defining appropriate expectations and outcomes for children with severe developmental disabilities. There is ongoing discussion about whether typical assessments conducted with these children provide useful information, and our findings lend support to the need for other instruments that tap auditory and non-auditory development in these children. Several researchers have underscored that for children with additional disabilities who receive cochlear implants, the meaning of success should be redefined and the development of measurement tools expanded to include a range of outcomes (Wiley et al, 2005; Beer et al, 2012; Edwards et al, 2012; Eze et al, 2013; Hayward et al, 2013). Long-term data from our study supports the need for other measurement tools to help practitioners and policy makers define important and broader benefits that extend beyond auditory and spoken communication outcomes for children with severe additional disabilities.
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Acknowledgements We would like to acknowledge the assistance of Julia Ham in the preparation of this manuscript. We also thank the audiologists at the Children’s Hospital of Eastern Ontario for their contributions in clarifying chart data. Declaration of interest: The authors report no conflict of interest. The content and writing of the paper were solely the work of the authors. This study was supported in part by a Canadian Institutes of Health Research Grant and a Canadian Child Health Clinician Scientist Career Enhancement Award to E.F. Funding for the Child Hearing Lab is gratefully acknowledged from the Masonic Foundation of Ontario.
References Beer J., Harris M.S., Kronenberger W.G., Holt R.F. & Pisoni D.B. 2012. Auditory skills, language development, and adaptive behavior of children with cochlear implants and additional disabilities. Int J Audiol, 51, 491–498. Berrettini S., Forli F., Genovese E., Santarelli R., Arslan E. et al. 2008. Cochlear implantation in deaf children with associated disabilities: Challenges and outcomes. Int J Audiol, 47, 199–208. Birman C.S., Elliott E.J. & Gibson W.P.R. 2012. Pediatric cochlear implants: Additional disabilities prevalence, risk factors, and effect on language outcomes. Otol Neurotol, 33, 1347–1352. Centers for Disease Control and Prevention. 2012. Prevalence of autism spectrum disorders - Autism and Developmental Disabilities Monitoring Network, 14 sites, United States. MMWR, 61, 1–19. Cruz I., Vicaria I., Wang N.Y., Niparko J., Quittner A.L. et al. 2012. Language and behavioral outcomes in children with developmental disabilities using cochlear implants. Otol Neurotol, 33, 751–760. Dettman S.J., D Costa W.A., Dowell R.C., Winton E.J., Hill K.L. et al. 2004. Cochlear implants for children with significant residual hearing. Arch Otolaryngol Head Neck Surg, 130, 612–618. Donaldson A.I., Heavner K.S. & Zwolan T.A. 2004. Measuring progress in children with autism spectrum disorder who have cochlear implants. Arch Otolaryngol Head Neck Surg, 130, 666–671. Edwards L., Hill T. & Mahon M. 2012. Quality of life in children and adolescents with cochlear implants and additional needs. Int J Ped Otorhinolaryngol, 76, 851–857. Edwards L.C. 2007. Children with cochlear implants and complex needs: A review of outcome research and psychological practice. J Deaf Studies Deaf Educ, 12, 258–268. Erber N.P. 1982. Auditory Training. Washington, DC: A.G. Bell Association. Eze N., Ofo E., Jiang D. & O’Connor A.F. 2013. Systematic review of cochlear implantation in children with developmental disability. Otol Neurotol, 34, 1385–1393. Filipo R., Bosco E., Mancini P. & Ballantyne D. 2004. Cochlear implants in special cases: Deafness in the presence of disabilities and/or associated problems. Acta Otolaryngol Suppl, 552, 74–80. Fitzpatrick E. & Brewster L. 2008. Pediatric cochlear implantation in Canada: Results of a survey. Can J Speech-lang Pathol Audiol, 32, 29–35. Fitzpatrick E.M., Johnson E. & Durieux-Smith A. 2011. Exploring factors that affect the age of cochlear implantation in children. Int J Ped Otorhinolaryngol, 75, 1082–1087. Fitzpatrick E.M., Olds J., Gaboury I., McCrae R., Schramm D. et al. 2012. Comparison of outcomes in children with hearing aids and cochlear implants. Cochlear Implants Int, 13, 5–15. Fortnum H.M., Marshall D. & Summerfield A.Q. 2002. Epidemiology of the United Kingdom population of hearing-impaired children including characteristics of those with and without cochlear implants: Audiology, aetiology, comorbidity, and affluence. Int J Audiol, 41, 170–179.
Int J Audiol Downloaded from informahealthcare.com by National University of Singapore on 06/19/14 For personal use only.
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N. Wakil et al.
Gallaudet Research Institute. 2011. Regional and National Summary Report of Data from the 2009-2010 Annual Survey of Deaf and Hard of Hearing Children and Youth. Washington. DC: GRI, Gallaudet University. Haskins H.A. 1949. A Phonetically Balanced Test of Speech Discrimination for Children. Unpublished master’s thesis. Evanston, USA: Northwestern University. Hayward D.V., Ritter K., Grueber J. & Howarth T. 2013. Outcomes that matter for children with severe multiple disabilities who use cochlear implants: The first step in an instrument development process. Can J Speech-lang Pathol Audiol, 37, 58–69. McCracken W. & Turner O. 2012. Deaf children with complex needs: Parental experience of access to cochlear implants and ongoing support. Deaf Educ Int, 14, 22–35. Meinzen-Derr J., Wiley S., Grether S. & Choo D.I. 2010. Language performance in children with cochlear implants and additional disabilities. Laryngoscope, 120, 405–413. Meinzen-Derr J., Wiley S., Grether S. & Choo D.I. 2011. Children with cochlear implants and developmental disabilities: A language skills study with developmentally matched hearing peers. Res Dev Disabil, 32, 757–767. Moog J.S. & Geers A.E. 1990. Early Speech Perception Test (ESP). St. Louis, USA: Central Institute for the Deaf. Nikolopoulos T.P., Archbold S.M., Wever C.C. & Lloyd H. 2008. Speech production in deaf implanted children with additional disabilities, and comparison with age-equivalent implanted children without such disorders Int J Ped Otorhinolaryngol, 72, 1823–1828. Nilsson M.J., Soli S.D. & Gelnett D.J. 1996. Development of the Hearing in Noise Test for Children (HINT-C). Los Angeles: House Ear Institute, pp. 1–9. O’Brien L.C.G., Kenna M., Neault M., Clark T.A., Kammerer B. et al. 2010. Not a “sound” decision: Is cochlear implantation always the best choice? Int J Ped Otorhinolaryngol, 74, 1144–1148. Olds J., Fitzpatrick E., Schramm D. & McLean J. 2005. Outcome of Cochlear Implantation in Children with Complex Disabilities. Paper
presented at the Ninth Symposium on Cochlear Implants in Children, Dallas, USA. Olds J., Fitzpatrick E.M., Steacie J., McLean J. & Schramm D. 2007. Parental Perspectives of Outcome after Cochlear Implantation in Children with Complex Disabilities. Paper presented at the 11th International Conference on Cochlear Implants in Children, Charlotte, USA. Ouellette-Kuntz H.M.J., Coo H., Lam M., Yu C.T., Bretenbach M.M. et al. 2009. Age at diagnosis of autism spectrum disorders in four regions of Canada. Can J Public Health, 100, 268–273. Picard M. 2004. Children with permanent hearing loss and associated disabilities: Revisiting current epidemiological data and causes of deafness. Volta Rev, 104, 221–236. Pyman B., Blamey P., Lacy P., Clark G. & Dowell R. 2000. The development of speech perception in children using cochlear implants: Effects of etiologic factors and delayed milestones. Am J Otol, 21, 57–61. Schramm D., Fitzpatrick E., Olds J. & Sampson M. 2007. Systematic Review of Cochlear Implants in Children with Multiple Disabilities. Paper presented at the 11th International Conference on Cochlear Implants in Children, Charlotte, USA. Steven R.A., Green K.M.J., Broomfield S.J., Henderson L.A., Ramsden R.T. et al. 2011. Cochlear implantation in children with cerebral palsy. Int J Ped Otorhinolaryngol, 75, 1427–1430. Van Naarden K., Decoufle P. & Caldwell K. 1999. Prevalence and characteristics of children with serious hearing impairment in metropolitan Atlanta, 1991–1993. Pediatrics, 103, 570–575. Wiley S., Jahnke M., Meinzen-Derr J. & Choo D. 2005. Perceived qualitative benefits of cochlear implants in children with multi-handicaps. Int J Ped Otorhinolaryngol, 69, 791–798. Wiley S., Meinzen-Derr J. & Choo D. 2008. Auditory skills development among children with developmental delay and cochlear implants. Ann Otol Rhinol Laryngol, 117, 711–718. Zimmerman-Phillips S., Robbins A.M. & Osberge M.J. 2000. Assessing cochlear implant benefit in very young children. Annals Otol Rhinol Laryngol, 109 (Suppl. 185), 42–43.
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