Skip to main content
NCBI home page
NIHPA Author Manuscripts logoLink to NIHPA Author Manuscripts
. Author manuscript; available in PMC: 2015 Nov 4.
Published in final edited form as: Audiol Neurootol. 2014 Nov 4;19(6):386–394. doi: 10.1159/000363684

The Development of Auditory Perception in Children Following Auditory Brainstem Implantation

Liliana Colletti *, Robert V Shannon #, Vittorio Colletti *
PMCID: PMC4289463  NIHMSID: NIHMS598196  PMID: 25377987

Abstract

Auditory brainstem implants (ABI) can provide useful auditory perception and language development in deaf children who are not able to use a cochlear implant (CI). We prospectively followed-up a consecutive group of 64 deaf children up to 12 years following ABI implantation. The etiology of deafness in these children was: cochlear nerve aplasia in 49, auditory neuropathy in 1, cochlear malformations in 8, bilateral cochlear post-meningitic ossification in 3, NF2 in 2, and bilateral cochlear fractures due to a head injury in 1. Thirty five children had other congenital non-auditory disabilities. Twenty two children had previous CIs with no benefit. Fifty eight children were fitted with the Cochlear 24 ABI device and six with the MedEl ABI device and all children followed the same rehabilitation program. Auditory perceptual abilities were evaluated on the Categories of Auditory Performance (CAP) scale. No child was lost to follow-up and there were no exclusions from the study. All children showed significant improvement in auditory perception with implant experience. Seven children (11%) were able to achieve the highest score on the CAP test; they were able to converse on the telephone within 3 years of implantation. Twenty children (31.3%) achieved open set speech recognition (CAP score of 5 or greater) and 30 (46.9%) achieved a CAP level of 4 or greater. Of the 29 children without non-auditory disabilities, 18 (62%) achieved a CAP score of 5 or greater with the ABI. All children showed continued improvements in auditory skills over time. The long-term results of ABI implantation reveal significant auditory benefit in most children, and open set auditory recognition in many.

Keywords: Auditory perception, Prelingually deaf children, Cochlear malformation, ossification, fracture, cochlear nerve aplasia, auditory brainstem implant, Outcome, Auditory perception

Introduction

The time course for the development of auditory perception extends over many years even in normal hearing children. Following an intervention such as a cochlear implant (CI) or auditory brainstem implant (ABI) long-term studies are necessary to evaluate the outcome [Nikolopoulos and O’Donaghue, 1998]. It is well known that prelingually deaf children make remarkable advances in auditory perception following CI [Svirsky et al, 2000, 2004; Govaerts et al., 2002; Robbins et al., 2004; Manrique et al., 2004; Schauwers et al., 2004; Geers, 2004; Nickolas and Geers, 2007; Dettman et al., 2007; Colletti et al., 2011]. However, children with no auditory nerve, who are not candidates for a CI, are a more difficult population because the central auditory regions of their brain may have never received input from the auditory periphery. In cases of developmental malformations it is not clear if the remaining auditory system is sufficiently intact to support sound input from a prosthesis. Recent papers have shown encouraging results [Colletti, 2007; Eisenberg et al., 2007; Sennaroglu et al., 2009] from children receiving an auditory brainstem implant (ABI). The present paper provides results assessing the development of auditory perception in 64 young deaf children up to 12 years following an ABI.

Methods

A consecutive group of 64 deaf children has been prospectively followed for up to 12 years following implantation with an ABI. Sixty of the children were prelingually deaf, and the age at implantation was less than 10 years. Four children were deafened from trauma or severe ossification after the onset of hearing. The radiological pre-operative evaluation included a computed tomography (CT) scan and/or magnetic resonance imaging (MRI) scan showing the absence of a cochlear nerve. A thorough medical evaluation was performed before the decision for implantation. All parents were informed of the risks and potential benefits of the ABI and provided informed consent as approved by the local hospital human subjects review board. The etiology of deafness in these children was: cochlear nerve aplasia in 49 (twenty one of whom had been previously fitted elsewhere with a CI with no sound detection), auditory neuropathy in 1 (previously fitted with CI elsewhere with no sound detection), cochlear malformations with VIIIn dysplasia in 3 (2 with Mondini type 2 bilateral incomplete cochlear partition and 1 with common cavity), one of these with Crouzon syndrome, and 5 with severe cochlear abnormalities (4 cochlear aplasia and 1 child with only the cochlear basal turn), bilateral post-meningitic cochlear ossification in 3, bilateral cochlear fractures due to a head injury in 1, NF2 in 2. Thirty five children had additional non-auditory disabilities and among these 9 had more than one disability: eight children had mild motor disability, 8 behavioural impairment, 16 cognitive (8 with cognitive + other disabilities), 4 language and 2 visual impairment.

A retrosigmoid surgical approach was used in all children, all were fitted with either a Cochlear 24 ABI device (N=58) or a MedEl ABI device (N=6), and all followed the same rehabilitation program. Intraoperative and post-operative electrically-evoked auditory brainstem responses (EABRs) were performed in all children. No child was lost to follow-up and there were no exclusions from the study. All 64 children had reached the 1-year post-implant stage and 56, 53, 43, 35, 28, 22, 15, 14, 10, 5, and 2 were at the 2–12-year intervals, respectively.

Auditory perception was assessed with the Categories of Auditory Perception (CAP) test [Archbold et al., 1995, 1998], an eight-point hierarchical scale of auditory performance. The CAP scale ranges from no awareness of environmental sound (Category 0) to conversational use of the telephone with a known speaker (Category 7). The CAP was selected for this analysis because it is simple, easily administered and easily understood by speech therapists and audiologists as well as parents without experience in assessment methods for deaf children. Moreover it has been found to be highly reproducible across independent observers [Archbold et al., 1998] and it is an outcome measure able to cover the extremely wide range of the auditory performance observed in our preliminary studies on ABI in children. It can be completed for all children, even the very young, taking also into consideration the different rate of development in these children. The ESP and GASP tests were used to evaluate auditory performance of the 21 children implanted in other institutions outside Italy. The outcomes of these children were pooled together with the outcomes of the other 43 children by converting ESP and GASP scores into equivalent CAP scores according to performance level, e.g., discrimination of words in the ESP test was assumed to be equivalent to category 4 on the CAP.

Results

The overall progress of the children fitted with ABI is shown in Table I, which shows the CAP score for the 64 children at each time interval. All children showed improvement in auditory perception with implant experience. There was considerable variability in outcomes and further analysis was undertaken to determine the causes. ABI outcome was analysed as a function of the top score obtained, the age at implantation, the presence or absence of non-auditory disabilities, and etiology.

Table 1.

CAP scores across years grouped by primary diagnosis (*=prior CI).

CAP scores over time for all individual ABI children, grouped by primary diagnosis. CAP scores are presented by year, up to 12 years post implant.

PT # Primary Diag Other Disorders Age at ABI before ABI 1y 2y 3y 4y 5y 6y 7y 8y 9y 10y 11y 12y
Cochlear Malformation
39 C.Malf SLI 6.1 0 1
64 C.Malf (cogn) 7 0 1 2 3
62 C.Malf ADHD 2.1 0 1 2 2 2
60 C.Malf 2.1 0 5 7 7 7 7
63 C.Malf SLI 4.5 0 0 1 1 1 1
61 C.Malf 3.7 0 2 2 4 4 4 4 4
17 C.Malf 4.4 0 2 3 3 3 3 3 3
10 C.Malf Crouzon 6.5 0 3 3 4 5 5 5 5 5 5
Number 8 8 7 7 6 5 3 3 1 1
Median 0 1.5 2 3 3.5 4 4 4 5 5
Prior Hearing
29 C.Ossif 6.6 0 3 5 5
18 C.Ossif 4 0 4 5 5 6 6 6
6 C.Ossif 2.8 0 5 6 7 7 7 7 7 7 7 7
5 H. TR. 16 0 6 7 7 7 7 7 7 7 7 7 7
Number 4 4 4 4 3 3 3 2 2 2 2 1
Median 0 4.5 5.5 6 7 7 7 7 7 7 7 7
VIIIn Aplasia plus other Disorders
37 VIIIn Aplasia (cogn) 3.7 0 1
38 VIIIn Aplasia (cogn+…) 3 0 1
40 VIIIn Aplasia Goldenhar 2.8 0 2
41 VIIIn Aplasia LADD S 2.5 0 3
30 VIIIn Aplasia Autism dis 5.9 0 1 1 2
31 VIIIn Aplasia ODD 2.6 0 1 4 4
32 VIIIn Aplasia Autism dis 5.7 0 0 1 2
26 VIIIn Aplasia Autism dis 1.8 0 0 1 1 1
25 VIIIn Aplasia Digeorge 2.7 0 1 2 3 4
27* VIIIn Aplasia MOEBIUS 3.3 0 2 2 3 4
44* VIIIn Aplasia (cogn) 4.5 0 2 3 3 3
45* VIIIn Aplasia (cogn+…) 5 0 2 3 3 3 3
48* VIIIn Aplasia (cogn+SLI) 2.1 0 1 2 3 3 3
47 VIIIn Aplasia (mild motor) 2.9 0 2 3 3 3 3
19* VIIIn Aplasia (cogn+visual) 10 0 1 2 2 2 2 2
20* VIIIn Aplasia (cogn+motor) 2.7 0 2 2 2 2 4 4
21* VIIIn Aplasia down 4.1 0 0 0 0 1 2 2
22 VIIIn Aplasia Goldenhar 3.5 0 1 1 3 4 5 5
46* VIIIn Aplasia (cogn+motor) 3 0 1 1 2 3 3 3 3
14 VIIIn Aplasia (cogn+motor) 2.1 0 2 3 5 5 5 5 5
15 VIIIn Aplasia ODD 5.5 0 1 2 2 2 2 2 2
49* VIIIn Aplasia (cogn) 4 0 2 2 2 3 3 3 3 3 3
9 VIIIn Aplasia down 4 0 0 0 1 1 2 2 2 2 2 2
8 VIIIn Aplasia kabuki 4.8 0 1 1 1 1 1 1 1 1 1 1
12 VIIIn Aplasia VCFS 4.1 0 1 1 2 2 2 3 3 3 3 3
4 VIIIn Aplasia cerebellar s facial n pl 1 0 0 1 1 1 1 1 1 1 1 1 1
3* VIIIn Aplasia sphrintzen 3 0 0 1 1 2 2 2 2 2 2 2 2
2 VIIIn Aplasia (cogn) 4.4 0 1 1 2 2 3 4 4 4 4 4 4 4
1 VIIIn Aplasia Autism dis 3.5 0 0 0 1 1 1 1 1 1 1 1 1 1
Number 29 29 25 25 22 18 15 11 8 8 7 4 2
Median 0 1 1 2 2 2.5 2 2 2 2 2 1.5 2.5
VIIIn Aplasia only
42 VIIIn Aplasia 1.4 0 2
43 VIIIn Aplasia 1.6 0 1
24 VIIIn Aplasia 1.9 0 6
52* VIIIn Aplasia 3 1 2 5
36 VIIIn Aplasia 0.9 0 1 3
56* VIIIn Aplasia 3 1 4 6
33* VIIIn Aplasia 1.7 0 1 3 4
34* VIIIn Aplasia 1.9 0 3 5 7
35 VIIIn Aplasia 2.3 0 4 6 6
55* VIIIn Aplasia 2.8 1 3 4 6
53* VIIIn Aplasia 4 1 1 3 5
57* VIIIn Aplasia 2.9 1 4 5 6 6
28 VIIIn Aplasia 4.9 0 2 3 4 4
58* VIIIn Aplasia 2.4 2 3 4 7 7
59* VIIIn Aplasia 2.2 2 3 5 7 7 7
23 VIIIn Aplasia 2.5 0 4 7 7 7 7
50* VIIIn Aplasia 3 1 2 3 3 4 4 4
51 VIIIn Aplasia 2.6 0 1 1 2 3 3 4 4
13 VIIIn Aplasia 2.5 0 1 2 2 3 4 4 5 5
54* VIIIn Aplasia 3 1 2 3 4 5 5 5 5 5 5
Number 20 20 17 14 9 6 4 3 2 1
Median 0 2 4 5.5 5 4.5 4 5 5 5
NF2 or AN
16 NF2 13.2 0 1 1 1 1 1 1 1
11 NF2 16 0 1 1 1 1 1 1 1 1 1
7 A/N ADHD+SLI 7.9 0 1 1 2 2 2 2 2 2 2 2
Number 3 3 3 3 3 3 3 3 2 2 1
Median 0 1 1 1 1 1 1 1 1.5 1.5 2
Open in a new tab

An asterisk (*) after the patient number indicates that this patient had a prior cochlear implant. List of Etiology abbreviations: C. Malf = cochlear malformation, C. Ossif = cochlear ossification, H.TR = head trauma, NF2 = neurofibromatosis type 2, A/N = auditory neuropathy.

Figure 1 shows the median CAP scores as a function of time, grouped by the top score achieved by each child. The seven children (11%) who ultimately were able to converse on the telephone (CAP level 7) all achieved this level by three years post-ABI. The five children (8%) who achieved a CAP level of 6 also mostly achieved this level at 3 years post-ABI. The 8 children (12.5%) who achieved the lowest open set speech recognition CAP score of 5 took longer to achieve this level of performance – about 4 years. And the ten children (16%) who achieved closed set discrimination of words (CAP level 4) took 4–6 years to achieve this score. A total of 20 children (31%) achieved some level of open set speech recognition with the ABI (CAP levels 5, 6, and 7) and almost half of the children (30/64 = 47%) achieved CAP scores or 4 or better.

Figure 1.

Figure 1

Open in a new tab

Median pediatric ABI scores on the CAP test over time. Results are grouped by the highest score ultimately achieved for categories 4–7.

It is well known that age at implantation is an important factor in the success of cochlear implants [Colletti et al., 2001; Dettman et al., 2007; Kirk et al., 2002; Manrique et al., 2004; Robbins et al., 2004; Svirsky et al., 2004]. It is important to supply sensory information to the developing brain while developmental plasticity is still strong. The present results were analysed to see if the information provided by an ABI also shows a sensitivity to age at implantation. Figure 2 shows the best CAP score achieved as a function of the age at ABI surgery. Only the 53 children who had used their ABI for at least 3 years are included in this plot to insure that performance was at or near asymptotic level. Filled symbols show results from children without other disorders, while open symbols show results from children who had other disorders beyond deafness, such as motor or cognitive delays. As expected, there is a trend for better performance in children implanted at a younger age (Kendall’s tau=−.21, p=.027). This is particularly clear in the children with no other disorders; many of these children implanted around age 2 were able to achieve a CAP score of 7. It is also clear that children without other disorders achieved higher asymptotic levels on the CAP than those with additional disorders (Cox regression time to event, additional disorders Wald = 34.2, p<.001). It is possible that some of this difference is caused by children with additional disabilities needing more than 3 years to achieve asymptotic performance. However 21 of the 30 children in this category had used the ABI more than 5 years (see Table 1).

Figure 2.

Figure 2

Open in a new tab

Best ABI CAP scores as a function of the age at implantation. Open symbols represent children with additional disabilities. Filled symbols indicate children with no additional disabilities. Only the 53 children who had the ABI at least 3 years and were under 10 years of age at the time of implantation are included.

One of the concerns with ABIs in congenitally deaf children is whether the congenital problems have involved the auditory portion of the brainstem. If there are developmental anomalies in the cochlear nucleus, then ABI stimulation may not be effective. In addition, some children with cognitive or other central processing disorders may not be able to effectively use the auditory information provided by the ABI [Pisoni, 2000]. We divided the results into two groups to investigate the effect of non-auditory complications on ABI performance: those children with other congenital abnormalities (N=35) and those without other complications (N=29). Figure 3 shows the median CAP score for these two groups as a function of years post-ABI. Children with no other disorders showed significantly higher CAP scores as a function of time (Kendall’s tau=−0.57, p<0.001). At 3 years post ABI there was a 3 category difference in the median CAP score between the two groups. This suggests that at least some non-auditory congenital anomalies can limit the potential benefit of an ABI, either from direct effect on the auditory brainstem, or on central processing necessary to make use of the ABI information. Although children with other disabilities achieved low scores on the CAP, they still showed improved awareness of their environment and improvements in cognitive development [Colletti and Zoccante, 2008]. Also note that while the median CAP score was only 2 for those children with additional disabilities, a few children in this category did obtain CAP scores of 4 or 5 (see Table 1).

Figure 3.

Figure 3

Open in a new tab

Median pediatric ABI CAP scores over time grouped according to other disorders. Children with no other disorders only had cochlea or cochlear nerve pathologies. Other disorders include a variety of congenital disorders listed in Table 1. The numbers of children at each follow up year for the two groups are as follows. For the group “No Other Disorders”: 29, 29, 26, 23, 17, 14, 11, 9, 5, 4, 2 for years 0–10, respectively, and for the group “Other Disorders”: 35, 35, 30, 30, 26, 21, 17, 13, 10, 10, 8 for years 0–10, respectively.

Probably the most important issue in the application of ABI in children is the effect of etiology on outcomes. We divided the 64 cases into five etiology groups: children who had prior hearing but lost it due to trauma or severe ossification (N=4), children with congenital deafness due to cochlear nerve aplasia (N=20), cochlear malformations (N=8), cochlear nerve aplasia with other non-auditory disabilities (N=29) and neurofibromatosis type 2 and auditory neuropathy (N=3). Children in this last category were considerably older at the time of ABI implantation (average age 9 years) than children in other categories. Figure 4 shows the median CAP score for each etiology group as a function of years of ABI use. While there appear to be clear differences in the median CAP scores between etiology groups, the top and bottom curves have too few subjects to achieve statistical significance, and the middle three curves did not achieve significant differences due to the high variability in performance within each etiology group. The four children who had prior hearing (3 cochlear ossification, 1 trauma) clearly had the best outcomes, increasing in performance rapidly over the first three years and ultimately reaching the highest CAP level. The dashed line reproduces data from a study reporting CAP results for 53 children with cochlear implants [Archbold et al., 1995], showing a similar trajectory of improvement compared to ABI recipients with prior hearing. This suggests that the highest performing ABI children can advance in auditory development at a rate similar to children with CIs. Similar observations have been reported in two ABI children by Eisenberg et al. [2012].

Figure 4.

Figure 4

Open in a new tab

Median pediatric ABI scores on the CAP test over time grouped by primary diagnosis. The numbers in parenthesis after each category indicates the number of children in that category at 1 year post implant. Numbers of children in each category diminish with years. Actual numbers at each year are found in Table 1. The dashed line reproduces CAP scores over time from 53 children with a CI from Archbold et al., 1995.

A Cox time series survival analysis evaluated the time it took to achieve a CAP score of 5 – the lowest level of open set speech recognition. Sixty-one of the patients were grouped in two different ways: cochlear vs neural point of origin, and no additional disabilities vs additional disabilities. Three patients who were more than 10 years old at the time of ABI implantation were not included in the analysis. The time needed to achieve CAP level 5 was not significantly related to the point of origin of the hearing loss: cochlear vs neural. However, the presence of additional disabilities was a significant predictor of the time to achieve CAP level 5 (p<0.0001), regardless of whether the main deficit was of cochlear origin or nerve origin.

Twenty one children with cochlear and cochlear nerve aplasia had been previously fitted with a CI and subsequently received an ABI. These children all showed significant improvements with the ABI compared to the CI: median CAP score of 1 with CI vs 4 with ABI (p < 0.001). Nine of the 21 (43%) achieved open set speech recognition (CAP scores 5, 6, or 7) with the ABI, while none of the 21 had achieved this level with a CI.

Discussion

A consecutive group of 64 deaf children were followed up to 12 years following ABI implantation. Within 1 year of activation 87.5% of children had obtained awareness of environmental sounds and 48.4% responded to speech sounds. Within two years of activation 23.4% of children were able to identify environmental sounds and discriminate among speech sounds (CAP Level 4). Of the 53 children with 3 year follow-up data, 26.4% were able to understand common phrases without the aid of lip reading and 13.2% of the children could use the telephone with a known speaker. This study confirms previous findings that the ABI is an appropriate device for auditory (re)habilitation in children with cochlear and cochlear nerve malfunctions that cannot benefit from CIs.

A comparison of the ABI outcomes obtained from this series of children vs a large group of children fitted with CIs clearly shows better performance outcomes obtained in a shorter time period in the CI group [Niparko et al., 2010]. However, when CI results are compared with ABI children who have heard before, then performance is comparable and the developmental trajectory is comparable (Figure 4, top curves). In addition, when ABI performance is compared with congenitally deaf children who received a CI at the same age then performance levels and trajectory over time are similar [Eisenberg et al., 2012]. This group of ABI children had previous hearing but lost their auditory nerve from head trauma or severe ossification following meningitis. This result suggests that the ABI could be considered as a next step for children with progressive ossification. In some cases a cochlear implant can provide adequate hearing for a time, but then the ossification may progress to damage the spiral ganglion in the modiolus and CI performance may drop dramatically. These children may regain open set speech recognition with an ABI.

Developmental Urgency

In our sample, none of the children with cochlear nerve aplasia or hypoplasia who had a CI first showed satisfactory auditory development with a CI. In such cases the time spent trying out the CI was not only time (and expense) wasted but also caused a prolongation of the period of auditory deprivation. Physiological sensory deprivation studies have demonstrated that in the absence of auditory stimulation, neural structures show a failure to mature and can degenerate [Nadol et al., 1989; Moore et al., 1994; Ponton et al, 1996; Shepherd et al., 1997] and auditory cortical areas can be reallocated to other modalities [Lee et al., 2001; Giraud & Lee, 2007].

When should a trial with a cochlear implant be skipped and move directly to an ABI? Under what conditions can we be confident that a CI will not provide useful hearing? Recent studies of CI outcomes in children have shown clear etiologies where CI results can be poor [Buchman et al., 2011; Young et al., 2012]. In cases where no auditory nerve is visible on high resolution CT images of the internal auditory meatus (IAM) and when the EABR evoked by the CI is distorted or absent, auditory results were very poor. In such cases, an ABI may provide better performance than a CI. We recommend high resolution CT imaging of the IAM [Govaerts et al., 2003; Casselman et al., 2008; Carner et al., 2009] and EABRs, stimulated either through an existing CI or from a wick electrode on the round window. In cases where the auditory nerve is not visible and there is no reliable EABR it may be a waste of time and expense to implant a CI or to continue to wait for auditory progress.

Neural Plasticity

It is of critical importance to have auditory input during the period of greatest neural plasticity in order to develop speech perception. There is compelling evidence that outcomes are better when cochlear implants are provided at the youngest age [Svirsky et al., 2000, 2004; Kirk et al., 2002; Govaerts et al., 2002; Robbins et al., 2004; Schauwers et al., 2004; Manrique et al., 2004; Waltzman et al., 2005; Dettman et al., 2007; Colletti et al., 2011]. We assume that this plasticity is primarily determined in the central system (e.g., auditory cortex) and so we assume that a similar time pressure exists for children to receive the ABI as early as possible. Children who receive cochlear implants below the age of one have clearly better and more rapid auditory development than children who receive cochlear implants between one and two years of age. And cochlear implants in 2–3 year olds give better outcomes than children implanted at ages greater than 3 years. So if a cochlear implant is tried initially, clinicians must remain vigilant for the early signs of CI efficacy. If no progress is being made on simple auditory tasks then it may be necessary to move to an ABI as soon as possible to make the best use of that early neural plasticity. It is necessary to explant the CI, re-evaluate the child with neuroimaging studies and perform ABI surgery as soon as possible after the lack of progress with a CI is evident. Children previously fitted with CIs and subsequently with ABI may demonstrate a slower development of auditory perception, possibly because of the major difference in the neural pattern of activation from the two devices and possibly because the time window of plasticity has partially closed.

Cognitive Factors

We cannot explain why some children with the ABI can detect and discriminate environmental sounds but do not develop speech perception and language. It may be hypothesized that one or more of the following conditions are responsible for the poor or low progression in speech perception abilities: incorrect positioning of the ABI array, incomplete development of the cochlear nuclei and auditory areas undetected by MRI, degeneration of cochlear nuclear cells specialized for processing speech, programming difficulties and inadequate encoder strategy, or other negative psychological and cognitive factors.

Pisoni [2000] has suggested that psychological and cognitive factors might play as important a role as perception in the development of speech perception. Most of the children in this study who had associated psychological and cognitive deficits could perceive the sounds and discriminate some speech patterns only a few months after ABI fitting. However, their overall auditory perceptual development has been very slow and they continue to have trouble translating the electrical stimulation into speech and language development. Additional intervention by psychologists and psycholinguists may be necessary to design specific rehabilitative strategies to help these children convert the new auditory sensations from the ABI into speech and language.

Even if children are not able to achieve open set speech recognition with the ABI they may receive cognitive benefits. Access to auditory information from the ABI has been demonstrated [Colletti, 2007; Colletti and Zoccante, 2008] to influence the development of specific cognitive functions. Scores on two tests evaluating cognitive function (form completion and repeated patterns) increased significantly during the first 12 months of ABI use. These data demonstrated that the fitting of the ABI in preverbal children with activation of the auditory sensory channel, previously absent, facilitated the development of cognitive parameters related to selective visual-spatial attention and fluid (multisensory) reasoning.

Safety and Complications

It is clear that the potential for surgical complications are greater for an ABI than for a CI. ABI implantation is an intra-dural procedure with some compression of the cerebellum in the retro-sigmoid approach. For this reason we recommend that ABIs in children only be attempted in centers with trained pediatric surgical teams with experience in the retro-sigmoid approach. In our clinic we found that the actual rate of surgical and device complications for an ABI were similar to those seen in CI surgery [Colletti et al., 2010]. The higher rate of complications observed in ABI surgery in adults was primarily related to NF2, the most common etiology for adult ABIs. In non-NF2 adults and in children, the complication rate was low – comparable to the complication rate observed for the same surgical approach for microvascular decompression. From the long-term follow up in the present data set we can report that we have observed no additional long-term complications from ABI placement and stimulation. To ensure this excellent safety record we stress that ABI in children only be undertaken in experienced centers trained specifically for ABI in children.

Conclusions

The ABI can provide beneficial auditory sensations to congenitally deaf children. The best outcomes with the ABI are in children who have heard before, either following severe meningitic ossification or trauma. Open set speech recognition was also observed in children with cochlear nerve aplasia and in children with severe cochlear malformations. Significant auditory benefit, but without open set speech recognition, was observed in children with cochlear nerve aplasia plus syndromic non-auditory disabilities. In some cases of severe cochlear ossification the ABI may provide better access to the remaining auditory nerve and superior performance to a cochlear implant. In cases of retrocochlear damage the ABI provides access to sound and allows steady improvements in sound discrimination and recognition. In all cases the ABI provides additional auditory input that allows improvements in auditory and cognitive development. It is important to implant the ABI as early as possible to take advantage of the powerful developmental plasticity of the brain. The ABI should be considered as a valuable tool in restoring auditory function to children for whom a CI is not an option.

Acknowledgments

We thank the children and their families for their commitment and persistence in this trial. We also thank Laurel Fisher for her help with statistical analysis of the data. RVS was partially supported by a grant from NIDCD.

References

  1. Archbold SM, Lutman E, Marshall D. Categories of Auditory Performance. Ann Otol Rhinol Laryngol. 1995;104 (Suppl 166):312–314. [PubMed] [Google Scholar]
  2. Archbold SM, Lutman E, Nikolopoulos T. Categories of auditory performance: inter-user reliability. Br J Audiol. 1998;32:7–12. doi: 10.3109/03005364000000045. [DOI] [PubMed] [Google Scholar]
  3. Buchman CA, Teagle HF, Roush PA, Park LR, Hatch D, Woodard J, Zdanski C, Adunka OF. Cochlear implantation in children with labyrinthine anomalies and cochlear nerve deficiency: implications for auditory brainstem implantation. Laryngoscope. 2011;121(9):1979–88. doi: 10.1002/lary.22032. [DOI] [PubMed] [Google Scholar]
  4. Carner M, Colletti V, Shannon R, Cerini R, Barillari M, Colletti L. Imaging in 28 Children with Cochlear Nerve Aplasia. Acta Otolaryngologica. 2009;129(4):458–61. doi: 10.1080/00016480902737978. [DOI] [PubMed] [Google Scholar]
  5. Casselman J, Mermuys K, Delanote J, Ghekiere J, Coenegrachts K. MRI of the cranial nerves--more than meets the eye: technical considerations and advanced anatomy. Neuroimaging Clin N Am. 2008;18(2):197–231. doi: 10.1016/j.nic.2008.02.002. [DOI] [PubMed] [Google Scholar]
  6. Colletti L. Beneficial auditory and cognitive effects of auditory brainstem implantation in children. Acta Oto-Laryngologica. 2007;127:943–946. doi: 10.1080/00016480601110253. [DOI] [PubMed] [Google Scholar]
  7. Colletti L, Zoccante L. Nonverbal cognitive abilities and auditory performance in children fitted with auditory brainstem implants: preliminary report. Laryngoscope. 2008;118(8):1443–8. doi: 10.1097/MLG.0b013e318173a011. [DOI] [PubMed] [Google Scholar]
  8. Colletti V, Shannon RV, Carner M, Veronese S, Colletti L. Complications in auditory brainstem implant surgery in adults and children. Otology and Neurotology. 2010;31(4):558–64. doi: 10.1097/MAO.0b013e3181db7055. [DOI] [PubMed] [Google Scholar]
  9. Colletti L, Mandalà M, Zoccante L, Shannon RV, Colletti V. Infants versus older children fitted with cochlear implants: performance over 10 years. Int J Pediatr Otorhinolaryngol. 2011;75(4):504–9. doi: 10.1016/j.ijporl.2011.01.005. [DOI] [PubMed] [Google Scholar]
  10. Dettman L, Pinder D, Briggs R, Dowell R, Leigh J. Communication Development in Children Who Receive the Cochlear Implant Younger than 12 Months: Risks versus Benefits. Ear & Hearing. 2007;28:11S–18S. doi: 10.1097/AUD.0b013e31803153f8. [DOI] [PubMed] [Google Scholar]
  11. Eisenberg LS, Johnson KC, Martinez AS, DesJardin JL, Stika CL, Dzubak D, Mahalak ML, Rector EP. Comprehensive Evaluation of a Child with an Auditory Brainstem Implant. Otol Neurotol. 2008;29(2):251–7. doi: 10.1097/mao.0b013e31815a352d. [DOI] [PubMed] [Google Scholar]
  12. Eisenberg LS, Johnson KC, Martinez AS, Visser-Dumont L, Ganguly DH, Still JF. Studies in pediatric hearing loss at the House Research Institute. J Am Acad Audiol. 2012;23(6):412–21. doi: 10.3766/jaaa.23.6.4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Geers AE. Speech, language, and reading skills after early cochlear implantation. Arch Otolaryngol Head Neck Surg. 2004;130:634–8. doi: 10.1001/archotol.130.5.634. [DOI] [PubMed] [Google Scholar]
  14. Giraud AL, Lee HJ. Predicting cochlear implant outcome from brain organisation in the deaf. Restor Neurol Neurosci. 2007;25(3–4):381–90. [PubMed] [Google Scholar]
  15. Govaerts PJ, De Beukelaer C, Daemers K, De Ceulaer G, Yperman M, Somers T, Schatteman I, Offeciers FE. Outcome of cochlear implantation at different ages from 0 to 6 years. Otol Neurotol. 2002;23(6):885–90. doi: 10.1097/00129492-200211000-00013. [DOI] [PubMed] [Google Scholar]
  16. Govaerts PJ, Casselman J, Daemers K, De Beukelaer C, Yperman M, De Ceulaer G. Cochlear implants in aplasia and hypoplasia of the cochleovestibular nerve. Otol Neurotol. 2003;24(6):887–91. doi: 10.1097/00129492-200311000-00011. [DOI] [PubMed] [Google Scholar]
  17. Kirk KI, Miyamoto RT, Lento CL, Ying E, O’Neill T, Fears B. Effects of age at implantation in young children. Ann Otol Rhinol Laryngol. 2002;(Suppl 189):69–73. doi: 10.1177/00034894021110s515. [DOI] [PubMed] [Google Scholar]
  18. Lee DS, Lee JS, Oh SH, Kim SK, Kim JW, Chung JK, Lee MC, Kim CS. Cross-modal plasticity and cochlear implants. Nature. 2001;409(6817):149–50. doi: 10.1038/35051653. [DOI] [PubMed] [Google Scholar]
  19. Manrique M, Cevera-Paz FJ, Huarte A, Molina M. Advantages of cochlear implantation in prelingual deaf children before 2 years of age when compared to later implantation. Laryngoscope. 2004;114:1462–1469. doi: 10.1097/00005537-200408000-00027. [DOI] [PubMed] [Google Scholar]
  20. Moore JK, Niparko JK, Miller MR, Linthicum FH. Effect of profound hearing loss on a central auditory nucleus. Am J Otol. 1994;15(5):588–95. [PubMed] [Google Scholar]
  21. Nadol JB, Young YS, Glynn RJ. Survival of spiral ganglion cells in profound sensorineural hearing loss: implications for cochlear implantation. Ann Otol Rhinol Laryngol. 1989;98(6):411–6. doi: 10.1177/000348948909800602. [DOI] [PubMed] [Google Scholar]
  22. Nicholas JG, Geers AE. Will they catch up? The role of age at cochlear implantation in the spoken language development of children with severe to profound hearing loss. J Speech Lang Hear Res. 2007;50:1048–62. doi: 10.1044/1092-4388(2007/073). [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nikolopoulos TP, O’Donoghue GM. Cochlear implantation in adults and children. Hosp Med. 1998;59(1):46–49. [PubMed] [Google Scholar]
  24. Niparko JK, Tobey EA, Thal DJ, Eisenberg LS, Wang NY, Quittner AL, Fink NE. CDaCI Investigative Team: Spoken language development in children following cochlear implantation. JAMA. 2010;303(15):1498–506. doi: 10.1001/jama.2010.451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Pisoni D. Cognitive factors and cochlear implants: some thoughts on perception, learning, and memory in speech perception. Ear Hear. 2000;21(1):70–8. doi: 10.1097/00003446-200002000-00010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Ponton CW, Don M, Eggermont JJ, Waring MD, Masuda A. Maturation of human cortical auditory function: differences between normal-hearing children and children with cochlear implants. Ear Hear. 1996;17(5):430–437. doi: 10.1097/00003446-199610000-00009. [DOI] [PubMed] [Google Scholar]
  27. Robbins KM, Koch DB, Osberger MJ, Zimmerman-Phillips S, Kishon-Rabin L. The effect of age at cochlear implantation on auditory skill development in infants and toddlers. Arch Otolaryngol Head Neck Surg. 2004;130:570–574. doi: 10.1001/archotol.130.5.570. [DOI] [PubMed] [Google Scholar]
  28. Schauwers A, Gilis S, Daemers K, DeBeukelar C, Govaerts P. Cochlear implantation between 5 and 20 months of age: The onset of babbling and the audiologic outcome. Otol & Neurotol. 2004;25:263–270. doi: 10.1097/00129492-200405000-00011. [DOI] [PubMed] [Google Scholar]
  29. Sennaroglu L, Ziyal I, Atas A, Sennaroglu G, Yucel E, Sevinc S, Ekin MC, Sarac S, Atay G, Ozgen B, Ozcan OE, Belgin E, Colletti V, Turan E. Preliminary results of auditory brainstem implantation in prelingually deaf children with inner ear malformations including severe stenosis of the cochlear aperture and aplasia of the cochlear nerve. Otol Neurotol. 2009;30(6):708–15. doi: 10.1097/MAO.0b013e3181b07d41. [DOI] [PubMed] [Google Scholar]
  30. Shepherd RK, Hartmann R, Heid S, Hardie N, Klinke R. The central auditory system and auditory deprivation: experience with cochlear implants in the congenitally deaf. Acta Otolaryngol. 1997;(Suppl 532):28–33. doi: 10.3109/00016489709126141. [DOI] [PubMed] [Google Scholar]
  31. Svirsky MA, Robbins AM, Kirk KI, Pisoni DB, Miyamoto RT. Language development in profoundly deaf children with cochlear implants. Psychological Science. 2000;11:153–158. doi: 10.1111/1467-9280.00231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Svirsky MA, Teoh SW, Neuberger H. Development of Language and Speech Perception in Congenitally, Profoundly Deaf Children as a Function of Age at Cochlear Implantation. Audiol Neurotol. 2004;9:224–233. doi: 10.1159/000078392. [DOI] [PubMed] [Google Scholar]
  33. Svirsky MA, Teoh SW, Neuberger H. Development of Language and Speech Perception in Congenitally, Profoundly Deaf Children as a Function of Age at Cochlear Implantation. Audiol Neurotol. 2004;9:224–233. doi: 10.1159/000078392. [DOI] [PubMed] [Google Scholar]
  34. Waltzman S, Roland JT. Cochlear implantation in children younger than 12 months. Pediatrics. 2005;116:487–493. doi: 10.1542/peds.2005-0282. [DOI] [PubMed] [Google Scholar]
  35. Young NM, Kim FM, Ryan ME, Tournis E, Yaras S. Pediatric cochlear implantation of children with eighth nerve deficiency. Int J Pediatr Otorhinolaryngol. 2012;76(10):1442–8. doi: 10.1016/j.ijporl.2012.06.019. [DOI] [PubMed] [Google Scholar]

RESOURCES