Auditory Brainstem Implants—Hearing Restoration in Congenitally Deaf Children
Background: Children who are born deaf can learn to hear and to speak with the aid of a cochlear implant (CI). If the implantation of a CI is not possible for anatomical reasons, an auditory brainstem implant (ABI) is the only surgical option for auditory rehabilitation. It is estimated that about 5 to 45 children could potentially benefit from this treatment in Germany each year. In this article, we present and discuss the current state of the scientific evidence.
Methods: The PubMed and Embase databases were searched for relevant publications from 2010 onward. 15 articles reporting at least 10 cases with at least one year of auditory follow-up were included in the analysis. The results, including CAP (“categories of auditory performance”) scores on a scale of 0 to 7, are presented and compared with the authors’ own findings in a series of 38 patients.
Results: All of the publications show that children who do not suffer from impairments of other kinds hear significantly better with an ABI than those with additional handicaps. Early implantation is advantageous, under the age of three years if possible. The results vary widely across publications and from patient to patient. The mean CAP score in all publications is 3.57 (standard deviation [SD], 1.04). 38.24% of the patients (SD 18.68) achieved the ability to understand spoken language (CAP ≥= 5), more specifically, the ability to communicate in everyday life without lip reading, in person and some even succeed in conversing over the telephone.
Conclusion: ABI is a safe and effective treatment for sensorineural deafness in congenitally deaf children who cannot be treated with a cochlear implant. In particular, children without any other impairments have a good chance of developing the ability to understand spoken language, especially if the implantation is performed early.
Conventional hearing aids rely on an intact connection between the peripheral auditory organ and the brain. Cochlear implants (CI), too, rely on an intact auditory nerve to restore the patient’s capacity for auditory communication, or even enable congenitally deaf children to hear (1, 2, 3). Yet some children with congenital sensorineural deafness lack a cochlea in which a CI could be placed, or else suffer from aplasia or hypoplasia of the auditory nerves (or have both problems at once). Such persons make up 1–10% of the congenitally deaf; they can learn to hear if they are given an auditory brainstem implant (ABI).
As there is not even a CI registry in Germany, let alone an ABI registry, no precise statistics on CI or ABI surgery are available. In Switzerland, 45 children aged 0–3 years and 22 aged 3–12 years received a CI in 2015 (4). The population of Germany being some 10 times higher than that of Switzerland, we may roughly estimate, considering only children aged 0 to 3, that 450 congenitally deaf children in Germany would be eligible for a CI each year. Among these, then, an estimated 5 to 45 children might be provided with an ABI.
Unlike CI, the electrodes of an ABI are implanted directly on the surface of the cochlear nucleus of the brainstem, resulting in the creation of an electro-neural interface directly into the brain (Figure 1). An audio processor transmits impulses via these electrodes into the cochlear nucleus, so that deaf children without any residual peripheral sensory input whatsoever can still learn to hear to a degree that promotes communication, i.e., they can still develop what is called functional hearing. Higher, integrative sensory function is enabled solely by technically generated impulses that flow directly into the brain.
The ABI was first developed for patients with neurofibromatosis type 2 (NF-2); its origins date back to 1979. House and Hitselberger successfully implanted the first, technically very simple ABI in an NF-2 patient (5, 6). Technical advancement led to electronically highly integrated, multichannel systems, which were used in NF-2 patients from the 1990s onward (7, 8, 9, 10, 11, 12) and in congenitally deaf children starting in the first decade of the 21st century (13) (for details see eMethods).
CI has seen widespread application to date: according to one estimate, 32 454 CI were implanted in Germany from 2005 to 2016 (4, 14). In contrast, ABI are still too rarely considered or even unknown, especially for children with prelingual deafness, i.e., deafness that began before language acquisition. In this article, we provide an up-to-date overview of the state of the scientific evidence on this topic.
The experience of the treatment team is a major determinant of the outcome of any type of therapy that is both highly specialized and rare. It follows that, in a cohort study, minimum case numbers must be set, in order for the findings to be valid and comparable across centers. We required at least ten cases per center. Moreover, each patient should have at least one year of auditory follow-up after implantation, as the hearing outcome changes markedly over time. We identified relevant studies by searching in the PubMed and Embase databases for the period from 1 January 2010 to 25 January 2021. The search criteria are given in Box 1.
The PubMed search yielded 205 hits and 13 duplicates; all of the 99 references retrieved from Embase had already been found by the PubMed search. Among the hits from the searches, 48 publications were judged to be relevant to the topic and were then further narrowed down by the criteria of a minimum caseload (at least 10 cases) and a minimum duration of follow-up (at least one year); there remained 15 original papers meeting these inclusion criteria (15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29). Not all of the publications were mainly concerned auditory outcomes. Some focused on complications, anatomic variants, quality of life, and intraoperative measurements. Hearing outcomes were sometimes reported only qualitatively, or with quantitative values as a range, without any average value. Nor was the duration of follow-up the same in all studies. All of the relevant and available quantitative information was extracted from the publications and is presented together with the qualitative data (Table) as a comprehensive overview of the findings; in interpreting these findings, one must take the above limitations into account.
Our patient cohort comprises 43 ABI operations in 41 children (two revisions) from 2009 to 2020. Data from 38 children were analyzed with the criteria described above. The mean age was 3.3 years (range, 1.25–11), and the mean follow-up duration (mFU) was 3.7 years (SD 1.4) – 2.7 (SD 1.2) years in the subgroup of children who had additional disabilities. The children’s parents or guardians gave their informed consent for the operations, subsequent follow-up visits, implant readjustments, and data analysis. Hearing outcomes were quantified on the widely accepted “categories of auditory performance” (CAP) scale (Box 2) (30). For statistical analysis, t-tests were used where applicable.
The Table contains the main findings of the 15 studies, and of our own patient cohort, with respect to postoperative hearing performance, numbers of patients, age range, pathology, method, follow-up, and drop-out rates. There have been no prospective, randomized, controlled trials in this field—understandably, as these would be ethically problematic. The data are thus largely derived from retrospective cohort analyses. Three prospectively designed single-center studies (19, 23, 28) involved patients with varying pathologies who were followed up for as long as 12 years. The studies selected for the present analysis concerned a total of 366 congenitally deaf children who received an ABI.
Serious complications associated with ABI surgery in non-tumor patients included meningitis, cerebellar contusion, and local infection, in 1 of 29 patients each (15). No further infections were reported, and we did not encounter any in our own series. When major complications occurred, such as cranial nerve lesions, they were attributable to concomitant tumor removal (15). 17% of non-tumor patients with congenital deafness sustained minor complications, such as a wound seroma (in 4 of 29 patients) (15), which also occurs with CI (15). We expected ABI to be associated with a higher frequency of postoperative cerebrospinal fluid collections under the scalp than CI, because the electrode cable passes through the dura mater; five of our own patients developed this problem and could all be managed conservatively.
The duration of follow-up was variable, up to 12 years at the longest. Follow-up is most important in the year after implantation and the two years thereafter. At one year, a clear trend in the development of hearing was already apparent, and the hearing outcome could be almost definitively assessed at three years. It made a difference whether the children had an additional disability or a syndrome associated with deafness, e.g., CHARGE or Goldenhar syndrome: these patients responded markedly less well to treatment (19, 20, 21). The timing of implantation was important as well: ABI before age 3 led to a better outcome (16, 19, 21, 24, 31). Similar results were obtained in our patient cohort (Figure 2). The mean CAP was 5.5 (SD 0.75) in patients under age 3 and 4.73 (SD 0.64) in patients over age 3 (p < 0.05).
As shown in Box 2, CAP 4 is the lowest outcome score associated with the recognition and understanding of speech sounds and thus with the capacity for simple verbal communication. Persons with CAP 5 are capable of open language comprehension, i.e., correct understanding of previously unknown sentences without recourse to lip-reading.
The mean CAP score of all children with no further disability at their last evaluation, 1–3 years after implantation, was 3.57 (SD 1.04; median 3.33). There was a wide variation in mean CAP scores across studies, with a range of 2.4 to 5. For children with additional disabilities, CAP scores ranged from 2.0 to 3.14; no mean CAP scores were computed because of the sparseness of the data.
In our own cohort, the mean duration of follow-up (mFU) up to the last follow-up evaluation was 3.7 years, with mean CAP values of 5.05 (SD 0.80) without further disability and 3.14 (SD 0.66, p < 0.001) with additional disability (mFU 2.7 years in the latter patient group). The percentage of children with CAP 5 or better at last follow-up ranged from 18.2% to 72% across studies, with a mean of 38.24% (SD 18.68; median 34.28). The relatively large standard deviations are due to the variable follow-up intervals and large interindividual differences.
Before the ABI era, CI was the only kind of surgical implant available to improve hearing. 1–10% of congenitally deaf children were doomed to permanent deafness, because they could not be helped with a CI. The first ABI procedures performed on children (13) were a controversial pioneer effort. As these patients did not require surgery for a tumor, the risk of an operation involving the brainstem was taken not to prolong survival, but rather just in the hope of generating auditory perceptions, whose potential functional utility could not be reliably predicted. Now that more experience has been gained with the technique, the probabilities of various outcomes a few years after implantation can be stated, but reliable prognostication is still impossible in the individual case. It is thus very important that these children’s parents or guardians should receive very comprehensive information before giving their informed consent to the procedure.
The available evidence must be assessed critically, in view of the limitations mentioned in the Methods section. The available studies are mostly retrospective, and hearing outcomes are not always recorded at the same time points, often at temporal intervals. In many publications, postoperative hearing rehabilitation are not explained in detail, and intraoperative problems, exclusion criteria, and drop-outs are not always addressed.
Nevertheless, the results show that this method led to a beneficial hearing outcome, up to the capacity for open speech comprehension, in 38% of cases. Moreover, the rate of complications was low in non-tumor patients.
The main complications were wound seromas, which arose in 4 of 29 patients (15), and cerebrospinal fluid (CSF) collections under the scalp. These problems are attributable to the passage of the ABI electrode cable through the dura mater, despite intensive intraoperative efforts to seal any potential sites of leakage, along with behaviors on the part of the treated children—crying, screaming, Valsalva maneuvers—that transiently raise the intracranial pressure and thereby promote the egress of CSF. The fluid collections were treated with puncture and pressure dressings where necessary. Most of the severe complications (32.3%), cranial nerve deficits in particular, arose in patients who were concomitantly undergoing tumor resection (15). The complication rates of ABI-only procedures were comparable to those of CI procedures (17% in both cases). Nonetheless, intracranial procedures generally carry a higher risk of severe complications. The consensus paper on ABI (32) therefore places an emphasis on the general and specific surgical experience of the implantation team, which is particularly important if a revision operation is needed. In rare cases, the stimulating electrode may become dislocated, or it may cease to function for technical reasons, e.g., after a fall. Determining the indications for revision is a difficult matter, and revisions are also more difficult to perform than primary operations, but they are highly effective in some cases (33). Robust study findings from large cohorts are not yet available.
The implants are magnetic resonance imaging- (MRI-) compatible in principle, but only if restricted MR sequences are used. Implant-related artefact that impairs the interpretability of the MRI is found exclusively in the posterior cranial fossa on the side of the implant. The remainder of the head, and the rest of the body, can be safely and usefully studied with 1.5 T MRI (34, 35). This option is especially important for children who have other medical conditions in addition to their deafness.
Bilateral ABI in children, analogously to bilateral CI (36), is also a matter of current discussion; some authors advocate it (37, 38, 39). Bilateral ABI would enable exploitation of the full capacity of the auditory pathways, maximizing the input of information to the brain. It has been shown to be helpful in some patients with NF-2 (38, 39). In analogy to the improved cognitive performance after bilateral CI (e5), one may expect that bilateral ABI will yield better outcomes than unilateral ABI. This will only become possible if it is reimbursed by health-insurance carriers.
It has been found that practically all children treated with ABI develop the ability to hear, to a greater or lesser extent. Just over one-third (38%) of non-syndromic children achieved open language comprehension. Children with other disabilities in addition to deafness had a markedly worse outcome in all studies in which this question was addressed. Their CAP scores ranged from 2 to 3 (14), and they did not achieve open language comprehension. Nevertheless, they did benefit from auditory perception, in that they became able to perceive environmental sounds and to orient themselves better, as well as to use sounds to support nonverbal communication. Like hearing after CI (e5), hearing after ABI positively affects these children’s cognitive, mental, and social development. ABI has been found to improve children’s quality of life (25).
The average CAP scores and the percentages of open speech comprehension varied widely, both across studies and interindividually. Precise implantation, with intensive use of electrophysiological methods (electrical brainstem response audiometry, E-BERA), seems necessary for the best possible outcome. Precise placement leads to better pitch recognition, lower electrical stimulation intensity, and higher stimulation frequency for each individual electrode. These parameters are positively correlated with better open speech comprehension (40).
Hearing also improved over time, as described in almost all studies (15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29). Among our patients, CAP scores improved from 0 to an average of 5 (implying open speech comprehension) after 24–36 months of ABI hearing experience. Children whose deafness was in the setting of a congenital syndrome achieved only CAP 3 (p < 0.001).
An important finding of the studies analyzed here, and of our own experience as well, is that hearing outcomes become significantly worse (p < 0.05) with increasing age at the time of implantation, from age 3 onward, even though the patients are still helped by ABI to some extent (Figure 2). Some patients can still achieve open speech comprehension even after receiving an ABI after age 3. An analogous finding is already known from CI (31) and has to do with the development, plasticity, and maturation of the auditory pathway.
In view of these findings, another important aspect becomes apparent. CI has generally been preferred over ABI until now in cases where the presurgical diagnostic evaluation, with its limitations, does not conclusively reveal whether an auditory nerve is hypo- or aplastic, or whether the anatomy of the inner ear, which is often dysmorphic, would still be compatible with CI. Such decisions should be taken by an experienced CI otosurgeon as early as possible. If the patient, after receiving a CI, makes no discernible or only minimal progress, then an ABI should be considered as soon as possible, in order to promote the early development of the auditory pathway and the integration of neural functioning. Parents should be informed about this strategy from the very beginning of the otosurgical decision-making process. Studies from 2013 and 2014 (17, 18) show that early ABI after failed CI can markedly improve hearing if performed without an excessive delay in between. Parents may be understandably reluctant to have their child undergo a second operation, and a brain operation at that; yet studies have shown (15, 19, 21) that ABI is both effective and very safe. It can also be pointed out that, if no ABI is performed in such cases, then the preceding CI operation will have had no value either as a diagnostic test or as a treatment.
Intraoperative cochlear stimulation with electrical brainstem response audiometry (e6, e7) is a recently introduced aid for the determination whether a CI or ABI would be more beneficial to the patient, if other (presurgical) diagnostic tests cannot reliably answer this question. This technique requires a cochleostomy through which an atraumatic test probe is inserted. If stimulation yields positive responses, CI surgery proceeds as planned; if not, an ABI is indicated and the operation can be extended to auditory brainstem implantation.
It is clear that, in diagnostically difficult cases, the decision between primary CI and ABI must always be made by an experienced team, no matter whether it is made preoperatively or during the surgical procedure. The early recognition of a poor therapeutic response to a CI is crucial in this regard (17,18). ABI after failed CI should be carried out in the child’s second year of life if possible, but no later than the third.
In conclusion, although ABI is not yet as widely known and established for children as it is for adult tumor patients, it is indeed a dependable therapeutic means of restoring hearing in special cases where CI is not an option.
Conflict of interest statement
Prof. Behr has received support for database research, consulting fees, lecture honoraria, and reimbursement of meeting participation fees and travel expenses from MedEl, Innsbruck, Austria.The remaining authors state that they have no conflict of interest.
Manuscript received on 29 April 2021, revised version accepted on 13 December 2021.
Translated from the original German by Ethan Taub, M.D.
Prof. Dr. med. habil. Robert Behr
Klinik für Neurochirurgie, Klinikum Fulda gAG
Pacelliallee 4, 36043 Fulda, Germany
Cite this as:
Behr R, Schwager K, Hofmann E: Auditory brainstem implants—hearing restoration in congenitally deaf children. Dtsch Arztebl Int 2022; 119: 135–41. DOI: 110.3238/arztebl.m2022.0090
University Medicine Marburg Campus Fulda, Clinic for ear, nose and throat diseases, head, neck and plastic facial surgery, communication disorders (hearing, voice and speech disorders): Prof. Dr. med. Dr. med. habil. Konrad Schwager
University Medicine Marburg Campus Fulda, Clinic for Diagnostic and Interventional Neuroradiology: Emeritus: Prof. Dr. med. Dr. med. habil. Erich Hofmann
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