Inner ear malformations frequently necessitate cochlear or auditory brainstem implantation (ABI) for hearing habilitation in children. ABI is indicated in certain severe inner ear malformations (IEM). In this chapter definite and probable ABI indications are explained in detail. In children with hypoplastic cochlear nerve there is still a debate on choosing the best method of rehabilitation. A review of literature is provided for this topic. Age limit in pediatric ABI has decreased considerably and this is also highlighted. Pediatric ABI necessitates a very good collaboration between otolaryngology, neurosurgery and audiology. Importance of the team work is explained. Main surgical approach is retrosigmoid approach. This is described in detail. Translabyrinthine and retrolabyrinthine approaches are also discussed and compared. Intraoperative monitoring is very important to determine the position of ABI electrode to provide maximum benefit. Finally, complications related to this approach are provided.
Key wordsauditory brainstem implantation – inner ear malformations – surgery – complete labyrinthine aplasia – cochlear aplasia – cochlear nerve aplasia – cochlear aperture aplasia – indications – cochlear nerve hypoplasia
8 Auditory Brainstem Implantation in Children: Evaluation and Surgery
The first auditory brainstem implantation was performed in 1979 at House Ear Institute (HEI) in Los Angeles, by Drs. William House and William Hitselberger after removal of an acoustic neuroma. 1 In 2001, Colletti et al 2 reported their auditory brainstem implant (ABI) experience in two children with severe inner ear malformations and no apparent cochlear nerve (CN), for the first time in literature. Until that time, no appropriate habilitation was possible as cochlear implant (CI) surgery was contraindicated in these patients. Use of ABI for children opened a new era in the habilitation of patients, in whom CI surgery was contraindicated due to cochlear, labyrinthine, or CN aplasia. In their initial paper, they reported that both patients had achieved good environmental sound awareness and some speech detection. After a period of time, other centers also started to use ABI for rehabilitation of these children.
As Hacettepe team we started ABI surgery in children in 2006. Until now, we have performed 128 pediatric ABI surgeries. Hacettepe implant team organized the first consensus meeting in 2009 where indications were discussed and determined for pediatric ABI. 3 In 2013, long-term results of ABI in children were discussed in the second consensus meeting. 4
ABI can be used in children with severe malformations and complete ossification of cochlea after meningitis. Inner ear malformations constitute the main group. ABI is not required in all cochleovestibular malformations. Patients with incomplete partition types II and III, and enlarged vestibular aqueduct almost always have cochlear and CN development to a certain extent and therefore, they can be (re)habilitated with CI. In a consensus paper, Sennaroglu et al divided the indications into two groups: definite and probable indications. Recently rudimentary otocyst was defined and added to definite indications. 3 , 5
8.2.1 Definite Indications
Complete labyrinthine aplasia (Michel aplasia): In this anomaly cochlea, vestibule, vestibular aqueduct, and cochlear aqueduct are absent.
Rudimentary otocyst: Incomplete millimetric representation of otic capsule without an internal auditory canal.
Cochlear aplasia: Cochlea is absent. The accompanying vestibular system may be normal or there may be an enlarged vestibule.
CN aplasia: This is the absence of the CN.
Cochlear aperture aplasia: This is the absence of the bony channel transmitting the CN from the internal auditory canal (IAC) to the cochlea.
8.2.2 Probable Indications
Hypoplastic cochlea with hypoplastic cochlear aperture: Hypoplastic cochlea may have different audiological presentation. Some patients may be aided with hearing aids and they may have excellent speech and language development. If they are accompanied by hypoplastic cochlear aperture and narrow IAC on high-resolution computed tomography (HRCT), usually CN is hypoplastic or absent and they commonly have severe to profound hearing loss. In the latter group, the CN entering the cochlea may be hypoplastic and ABI may be indicated according to audiological findings.
Common cavity and incomplete partition type I cases where CN is apparently missing: The nerve entering the common cavity is common cochleovestibular nerve (CVN). As cochlea and vestibule are separate in IP-I, the nerve entering the cochlea in IP-I is CN. If CVN and CN are present, they are candidates for cochlear implantation. If these nerves are absent, they are candidates of ABI.
Common cavity and incomplete partition type I cases if the CN is present: Even if CVN and CN are present, the distribution of the neural tissue in common cavity or IP-I cochlea is unpredictable, and ABI may be indicated in such cases if CI fails to elicit an auditory sensation.
The presence of an unbranched cochleovestibular nerve (CVN) is a challenge in these cases. In this situation, it is not possible to determine the amount of cochlear fibers travelling in the CVN. If there is a suspicion, a CI can be used in the first instance, and ABI can be reserved for the patients in whom there is insufficient progress with CI.
The hypoplastic CN presents a dilemma for the implant team. A hypoplastic nerve is defined as less than 50% of the usual size of the CN or less than the diameter of the facial nerve. Radiology of these patients should be carefully reviewed with an experienced neuroradiologist. If sufficient amount of neural tissue cannot be followed into the cochlear space, an ABI may be indicated.
Children with hypoplastic CN or thin unbranched CVN constitute the most controversial group in decision-making between CI and ABI. It must be kept in mind that children with hypoplastic nerves usually do not reach levels of those with normal cochlea, in terms of hearing and language development. It is obvious that radiology may not predict the presence of the CN accurately in these above-mentioned challenging five groups of patients. In all these subjects, audiological findings, as well as radiological findings, should be taken into consideration in order to decide between CI and ABI. If an experienced pediatric audiologist detects a slight response with insert of ear phones on either side of these cases, this information is very valuable in the side selection of CI. In such cases, family should be carefully counseled about the possibility of ABI surgery in future, if insufficient progress with CI is encountered during postoperative follow-up.
Some cases of pneumococcal meningitis produce total cochlear ossification where a CI cannot be placed satisfactorily into the scala timpani. Different surgical techniques (such as drill-out cochleostomy) have been described and electrode options (double or split array implants) are provided for total ossification. These usually result in suboptimal results. ABI is another option for patients with total ossification because the electrode can be placed in a normal location. In partial ossification however, every effort should be made to place the CI electrode in the scala tympani or vestibuli. If the electrode is not satisfactorily placed into either scala tympani or scala vestibuli, ABI may be another option.
8.3 CI versus ABI in Children with Hypoplastic Cochlear Nerve
Management of patients with hypoplastic CN is still controversial. Although it may rarely be possible to obtain good hearing and language development in certain cases with hypoplastic CN, majority of the patients have insufficient hearing, and limited language development with CI. These patients become candidates for ABI. It is important to correctly diagnose this subset of children and proceed with ABI directly when required; however, for the present time, preoperative and intraoperative audiological tests are not precise enough to enable correct diagnosis.
Bradley et al 6 reported their long-term experience in six children with hypoplastic CN. Preoperatively, they observed clear response to sound with hearing aids. Although initially all children demonstrated auditory thresholds within normal range, after using CI for 2 to 6 years, they demonstrated unsatisfactory outcome: five were at Categories of Auditory Perception (CAP) level 2 and one was at level 4. They concluded that even if they obtained thresholds similar to other CI users, the benefit of CI in children with hypoplastic CN is very limited.
Warren et al 7 reported three cases with narrow IACs bearing two nerves, one of them facial nerve and the other entering vestibule. Two of the families reported responses to auditory stimuli with amplification over time. They all underwent cochlear implantation. Early results after CI (4, 5, and 9 months, respectively) showed responses to auditory stimuli. They tried to explain the mechanism of sound transmission by a very tiny cochlear branch which could not be visualized due to extremely narrow distal IAC. It may also be possible that the nerve enters the vestibule and then turns toward cochlea. Regarding similar cases, our group observed that progress with CI usually reaches a plateau, and language development usually does not reach the level of CI use in normal cochlea. In general, hearing levels after CI may not be usually sufficient for appropriate language development.
Valero et al 8 recorded abnormal electrically evoked responses in the majority of CI recipients with hypoplastic CN. The atypical amplitude and latencies of these responses suggested nonauditory generators and should not be misread as typical evoked auditory brainstem response (EABR) peaks. There was no relationship between auditory pathway size and evoked brainstem response to determine whether they will be good CI candidates with these structural defects, and the unpredictable evoked responses observed here would make it difficult to predict auditory outcomes. Although there was limited initial improvement in speech perception outcomes, children with stenotic IAC and hypoplastic CN did not achieve comparable behavioral results with their CIs compared with children with an uncompromised CN. This poor outcome persisted in the long-term follow-up. Their scores at 120th month were comparable to 24th month scores of children with normal anatomy. They concluded that along with abnormal electrophysiological findings, children with hypoplasia of the CN are not good candidates for cochlear implantation. If the decision is made to proceed with cochlear implantation, families should be counseled that expectations of auditory and spoken language development should be tempered.
Buchman et al 9 reported CI results in patients with labyrinthine anomalies. They concluded that the peripheral neural populations in patients with CN deficiency are insufficient for the development of synchronized auditory stimulation in most instances. They proposed initial use of CI before ABI in these situations. One of the important findings of this study was that intracochlear eight nerve compound action potential (ECAP) testing results were associated with the development of speech perception abilities.
Song et al 10 reported their results of intracochlear EABR versus extracochlear EABR in predicting long-term outcomes of patients with narrow IAC. They concluded that intracochlear EABR measured either intraoperatively or in the early postoperative period may play an important role in deciding whether to continue with auditory rehabilitation with a CI or to switch to an ABI so as not to miss the optimal timing for language development. They concluded that for those cases in which cochlear implantation has been performed initially, considering the limited prognostic value of preoperative extracochlear electrophysiologic testing or imaging, intracochlear EABR measured either intraoperatively or in the early postoperative period may provide valuable prognostic information to predict long-term outcomes.
Song et al 11 concluded that residual response on pure tone audiometry and behavioral response to environmental sounds appeared to be more accurate markers for predicting the presence or absence of the CVN compared to imaging or electrophysiologic testing because all three patients who showed a response to sound stimuli demonstrated thin CVNs during surgery. Our team also reached to a similar conclusion, that is, behavioral audiological tests seemed to be more important in decision-making between CI and ABI. However, in our series, patients with hypoplastic CN demonstrated certain progress initially with CI, but could not carry on when more sophisticated learning processes were required.
Recently, Birman et al 12 reported better outcomes of auditory performance with CI in patients with aplastic/hypoplastic CN. Pediatric CI surgery in CN aplasia/hypoplasia is associated with variable outcomes. Overall, approximately 75% of children were able to use some verbal language. After CI, nearly 50% of those with CN aplasia and 90% of those with CN hypoplasia gained some speech understanding (CAP score 5–7). Their findings may be useful for preoperative counseling regarding the likelihood of CI outcomes in CN aplasia/hypoplasia. However, a comment that mentions “50% of cases with CN aplasia obtains CAP scores between 5–7” must be taken very cautiously.
Kutz et al 13 also reported their results after CI in children with hypoplastic CN. Seven children underwent CI in an ear without any CN on magnetic resonance imaging (MRI). One child developed early closed-set speech recognition. The other six children developed only speech detection or pattern perception. Two children with hypoplastic nerve were also implanted. One developed consistent closed-set word recognition and the other developed early closed-set word recognition. They concluded that CN deficiency is a common cause for profound sensorineural hearing loss and children with a deficient but visible CN on MRI can expect to show some speech understanding after cochlear implantation. However, these children do not develop speech understanding to the level of implanted children with normal CNs. Children with an absent CN determined by MRI can be expected to have limited sound and speech awareness after CI surgery.
Promontory stimulation or stimulation via round window is difficult to provide in cases with severe inner ear malformations (IEM). In Hacettepe University, we tested an Intracochlear Test Electrode (ITE) to simulate a CI to make the intraoperative decision between CI and ABI. 14 ITE has three intracochlear contact points of 18 mm length and one extracochlear ground electrode. Intracochlear part is inserted into the cochlea up to the ring as needed. It was used in 11 subjects with various inner ear malformations. In cases with normal anatomy or IP-II, excellent wave morphology was obtained. If there were no EABR, decision for an ABI was made. There were two cases with conflicting results. One was an IP-I with definite CN on MRI. The test result was negative but CI surgery was done and CI provided very good language development on long-term follow-up. The second conflicting result was from a child with common cavity. He had benefit from CI but he developed facial stimulation which was present on all contacts. During revision procedure, ITE was used but there was no response during surgery. In this particular patient with common cavity who had good progress with a CI, ITE failed to produce EABR. As a result, it appears that, if there is a positive response, ITE is reliable. A negative response, however, has to be considered very carefully and radiology and preoperative audiological test methods should be used together to make the decision between CI and ABI.
As can be seen, majority of the literature report unsuccessful outcome with CI in CN hypoplasia. As a result, it is still a problematic issue to decide between CI and ABI in patients with narrow IAC and hypoplastic CN. Intracochlear EABR might be a better indicator compared to preoperative electrophysiological tests.
8.4 Members of ABI Team
ABI surgery is a technically demanding operation. The team has to be experienced regarding the surgery, audiological follow-up, and rehabilitation of CI patients. An experienced pediatric neurosurgeon is key to achieve success and also to avoid possible complications as much as possible. He or she is responsible for accurate identification of the exact location of the foramen of Luschka. We have encountered many situations where the foramen was not apparent and careful dissection was necessary to identify its location. This is one of the most important factors to obtain successful outcome by preventing malposition of the electrode which may lead to unsuccessful results. An experienced neurosurgeon is the key to avoid this complication.
If the surgery leads to cranial nerve damage and/or brainstem injury which brings forth neurological sequela in otherwise healthy children, this would be a catastrophe both for the family and the team. Besides, this might create negative impact on public opinion regarding ABI surgery. It is very important to avoid any possible complications in these children by working with an appropriate team. Placing the implant in the brainstem involves the close collaboration of an experienced pediatric neurosurgeon, otologist, and audiologist. The otologist must be experienced in implant surgery. Intraoperative EABR test measurements allow placement of the electrode into the most appropriate location. This is not like CI surgery where intracochlear placement is very straightforward. Final position of the electrode plate is determined by intraoperative EABR measurements; experienced audiologist is very important for this part of the surgery.
8.5 The Age Limit for ABI in Children
According to the consensus statement, age limit for ABI in children is similar to CI patients. 15 Better language outcome is expected when the children are operated between 1 and 2 years of age. ABI surgery is more challenging than CI surgery because, young children have less blood volume and cerebrospinal fluid (CSF) in the posterior fossa. From the neurosurgical point of view, in the consensus paper, optimum lower limit was determined as 18 months but, depending on the experience of the center, it was also suggested that it may be done as early as on 12 months old. Our team operated on 12 children of around the age one without any complications. It is without any doubt that early intervention will have better audiological outcome. Although it can be argued that surgical risks will be less when the child is operated later on in their life, the language outcome will not be satisfactory because of the brain plasticity. This will lead to the discredit of the surgery as it will be thought that this intervention will not produce good hearing and language outcome. Therefore, ideal age appears to be between 1 and 2 years of age. As these are prelingually deafened children, this procedure should not be offered to patients older than 5 years old.
8.6 Preoperative Evaluation
All members of the team should evaluate ABI candidates in detail.
Radiological workup involves temporal CT and MRI. Diagnosis and indication for ABI are straightforward with CT in cases such as Michel deformity, rudimentary otocyst, and cochlear aplasia, which are definite indications for ABI. 3 Children with cochlear hypoplasia, hypoplastic cochlear aperture, and narrow IAC need more careful audiological and radiological evaluation with MRI. MRI, on the other hand, demonstrates the neural structures in the IAC. Any vascular abnormality around the lateral recess can be seen on MRI. The side with more developed inner ear or the cochleovestibular nerve should be preferred. As stated in the preceding paragraphs, MRI has limitations in the diagnosis.
Side selection is very important in ABI surgery. The team should try to choose the side which provides more information on the cochlear nucleus, hence, the side with more developed neural structures (e.g., facial nerve presenting unilaterally, or more prominent CVN or vestibular nerve may imply better developed cochlear nucleus area). If equal under all conditions, more developed inner ear should be chosen (if there is a cochlear aplasia on one side and a hypoplastic cochlea on the other side, the latter can be preferred). In addition, the side where the entrance of the lateral recess is more favorable, and the lateral recess is more accessible (where cerebellar retraction will be less) can be chosen.
8.6.1 Audiological Assessment Procedure
For preoperative evaluation of ABI candidates, all audiological test batteries should be conducted. This test battery includes both subjective and objective tests. It is apparent that in patients with complete labyrinthine aplasia and cochlear aplasia no response is expected. But even in these patients sometimes with maximum audiometric limits some response is observed in low frequencies which is in accordance with tactile sensation.
In subjective tests, the candidate should be evaluated with insert phones and if not possible, free field evaluation should be done. According to the age of the child, behavioral observation audiometry (BOA), visual reinforced audiometry, or play audiometry can be used.
For objective evaluation, it is appropriate to start with tympanometry and acoustic reflex tests to show middle ear status for all age groups, especially for infants and children. These tests should be followed by otoacoustic emissions (OAE), and auditory brainstem response (ABR) measurements.
Subjective tests are very important even when no response is obtained by other tests, including the objective ones. In this situation, subjective tests are the only method which give information about hearing status of the patient. Some patients with hypoplastic CN demonstrate behavioral response with pure tone or speech stimulation. These patients are counseled that the ear with best response with insert phone will be selected for CI, and the patient will be followed up for 6 to 9 months with CI. At the end of this period an EABR is also done to see if there is any response with CI. If there is no development in speech perception and no response on EABR, ABI will be offered to the family. It is also very important to take into consideration the observation of the family. In this situation we choose the opposite ear for ABI, thereby providing bilateral amplification to these children. In cases where there is a definite indication on one side, and a probable indication on the contralateral side, CI and ABI can be done simultaneously. Our team has performed six simultaneous CI and ABI surgeries until now.