Introduction

Over 50 million people worldwide and 1.2 million Americans are living with severe or profound hearing loss [1]. Etiologies are broad and include presbycusis, noise, ototoxicity and tumors such as vestibular schwannomas (VS). A study of VS symptoms identified that 85.8% of patients had hearing loss, and 40.1% had tinnitus among other complaints of ataxia, facial numbness, and paralysis [2]. The vast majority of VS (95%) are sporadic and unilateral; the remaining 5% of VS are typically bilateral as a part of a Neurofibromatosis Type 2 (NF2) associated schwannomatosis phenotype [3]. The etiology of sensorineural hearing loss (SNHL) in VS is multi-factorial and includes auditory nerve damage from tumor growth , mechanical compression from the tumor, and cochlear cellular damage from tumor secreted factors such as tumor necrosis factor alpha and extracellular vesicles [4].

Although more patients with VS are being observed than undergoing active treatment such as surgery or radiation, hearing loss remains an important factor in patients’ quality-of-life. Furthermore, the progression of SNHL in the non-tumor ear has been shown to be significantly greater than expected for age-related hearing loss in the general population [4]. The increased risk of hearing loss affecting both the ear ipsilateral to the tumor and the contralateral ear further highlights the importance of hearing rehabilitation. Despite this tremendous burden, hearing devices are not utilized to their full potential in the VS population. In a survey of patients with unilateral VS, less than one third of the respondents had ever used a hearing rehabilitation device, and 88% of patients had profound hearing loss in the affected ear [5]. In light of this, the aim of this review is to highlight the recent literature on cochlear implantation in the VS population, both in sporadic VS and in NF2-related schwannomatosis (NF2-SWN), and ultimately identify research areas where more work is warranted.

Hearing Rehabilitation in VS Patients with Single-Sided Deafness

Patients with unilateral sporadic VS typically experience asymmetric SNHL in the affected ear with decline in speech discrimination scores. Treatment of hearing loss in cases of single-sided deafness (SSD) includes traditional hearing aids if they have mild-to-moderately severe SNHL. However, conventional amplification may offer little to no benefit in patients with severe to profound unilateral hearing loss or those with poor (< 50%) word discrimination scores. In these cases, contralateral routing of signals (CROS) hearing aids may serve as better rehabilitative options. CROS systems involve capturing sound from the worsened ear with an external microphone and routing to the better, unaffected ear. Similarly, BiCROS hearing devices can be applied to patients with mild-to-moderate hearing loss in the non-tumor, contralateral ear to provide additional amplification. Nonetheless, only a small proportion of patients with SSD had significant improvement in their quality-of-life using CROS.

Additionally, surgically implanted bone-anchored conduction systems can be considered for patients with VS-associated SSD. The bone conduction device is fixated and/or osseointegrated into the skull on the side of the affected ear and connected to an external bone oscillator either transcutaneously or percutaneously. Sound information is transformed by the oscillator and transmitted through the device to directly vibrate the bony labyrinth. Compared to CROS hearing aids, bone conduction devices are best suited for patients with good contralateral hearing. Similar to CROS, bone conduction devices are limited by their inability to provide binaural hearing, which is critical to provide speech perception in noise, localization, and tinnitus mitigation [6•, 7].

Historically, patients with hearing loss due to NF2-SWN that are no longer aidable can undergo placement of auditory brainstem implants (ABIs). An ABI bypasses the cochlear nerve and is placed near the dorsal cochlear nucleus to directly stimulate the cochlear nucleus to restore hearing. The performance of an ABI is quite variable, as most patients have some degree of sound awareness, but accomplishing open-speech after ABI is rare [8]. While it is a great option for patients where the cochlear nerve is absent or not intact, further research is needed to select candidates most appropriate for ABI.

There is growing evidence that CIs are able to mitigate the deficits that patients experience with SSD [9]. A retrospective study of 41 patients VS who underwent simultaneous VS resection and cochlear implantation revealed that auditory perception was achieved in 80.5% of patients with improved hearing outcomes in the users group compared to the non-users groups [10]. Further support of CI benefits was provided by a study of 13 VS patients which reported auditory sensation in all patients and speech perception in 12 of the 13 patients (92%) with a median follow-up time of 14 months [11]. Another study of 7 sporadic VS patients reported auditory perception in 100% of patients (n = 7). Speech perception testing in these 5 patients showed improvement in sentence testing-in-noise; however, there was no improvement in the consonant-nucleus-consonant (CNC) word assessment of speech perception [12]. Thus CI is an undeniably an effective modality for hearing rehabilitation in the VS patient population, but further research is needed to reconcile some of the discrepancies between studies.

Historical Perspectives on CI

Historically, CI was reserved for patients with bilateral severe-to-profound hearing loss; however, CI indication expansion has been an ongoing process over the past nearly 30 years [13]. Since the 2014 Food and Drug Administration (FDA) approval for the Cochlear Nucleus Hybrid CI (Cochlear Limited, Sydney, Australia) and the 2016 approval for the MED-EL Electro-acoustic Stimulation (EAS) device (MED-EL, Innsbruck, Austria), there has been a greater emphasis on audiometric testing results from the ear to be implanted rather than the best-aided condition. These approvals expanded CI indications to patients with low-frequency residual hearing in the normal range, and it based candidacy on aided word scores from each ear instead of the best-aided [14]. It became clear to surgeons that CI placement with residual hearing allowed for potentially improved CI outcomes. In 2019, the FDA approved CI for patients with asymmetric hearing loss (AHL) and SSD [15]. These expansions reflect surgeons’ off-label use of CI as reported in a survey of the American Neurotology Society where 78% of respondents indicated CI off-label use including for SSD (46%) and ipsilateral VS (35%) [16].

Patients with SSD experience a loss of binaural which leads to problems with sound localization and speech recognition in noisy environments and results in a significant level of handicap [17]. Auditory and speech related benefits of CI are widely reported in both unilateral and bilateral implantation, as well as in bimodal use where a hearing aid is used in the contralateral ear [17, 18]. Such benefits include improved sound localization, reduction of the head blocking sound effect (head shadow benefit), and enhanced speech perception when speech and noise are presented concurrently from the front of a patient (summation improvement). The effectiveness of CI in patients has been under intensive investigation over the past 10 years. A study of 60 patients with SSD due to a variety of pathologies such as tumors or Meniere’s disease reported multiple binaural benefits after implantation [19]. Specifically in the VS patient population, Thompson et al. provided compelling evidence for benefits of concurrent translabyrinthine tumor excision and CI insertion. Their systematic review showed that the majority of patients (85%) achieved audibility, and, of patients with open-set speech recognition, most (75%) were classified as either intermediate or high performers [20].

Current literature validates significant improvements in speech perception scores in quiet and noise, tinnitus control, sound localization, and quality-of-life after cochlear implantation, as evidenced by a systematic review on cochlear implantation in the SSD population involving 674 patients [9]. In a study involving 12 adult patients, CNC scores in quiet improved by an average of 54%. In noise, there was an average signal-to-noise (SNR) reduction of 2.0 dB when noise was presented to the CI ear and 4.6 dB when noise was presented to the better hearing ear [21]. Similar positive outcomes were reported from a prospective study of 10 SSD-CI patients at 6 months post-activation. CNC improvement in this cohort was high, averaging 84%. Additionally, there was improvement in the Hearing-in-Noise Test (HINT) sentence recognition in quiet, with an improvement of 51% relative to the binaural baseline. Other reported benefits included enhanced localization accuracy (root mean square error [RMSE] reduction by 11.5 degrees), reduced tinnitus severity (visual analog scale scores significantly lower with the CI on than with the CI off), and improved quality-of-life (mean scores of the Speech, Spatial, and Qualities of Hearing scale (SSQ) sub-tests were 5.7, 5.5, and 6.8, respectively) [22]. Nevertheless, disparities exist in results and testing modalities across these studies, underscoring the necessity for additional research to validate the findings of these studies. From a quality-of-life standpoint, CI in SSD patients allows for significant improvement in tinnitus [17, 23, 24]. Tolisano et al. found that SSD patients showed improvement in objective measures, such as speech-in-quiet (SIQ), speech-in-noise (SIN), sound localization and improvement in subjective measures of quality-of-life following CI. However, there was no relationship between the timelines in improvement of objective and subjective measures [25].

Despite evidence supporting the efficacy of cochlear implantation, CI utilization rates remain low. A recent analysis estimates that only 12.1% of individuals with severe-to-profound SNHL in the better hearing ear (traditional CI indication) ultimately undergo implantation. Furthermore, only 2.1% of individuals with SSD or AHL with severe-to-profound SNHL in the worse ear undergo implantation [26]. Not surprisingly, barriers to CI uptake include socieioeconomic status and patients’ concerns such as fear of surgical complications, concern over the loss of residual hearing, financial burden, social stigma, and gaps in knowledge [27,28,29]. However, providers, including general practitioners and audiologists, also expressed lack in knowledge about CI which may impact their referral rates [18, 27].

VS and Hearing Loss

Current estimates of prevalence of sporadic VS are approximately 1 in 2000 adults (up to 1 in 500 in the elderly population, age ≥ 70 years) with an incidence around 1–2 per 100,000 (up to 21 per 100,000 person-years in the elderly) [30, 31]. With the rise in incidence of VS over the past decades, the role of hearing loss management in this population has increasingly grown in importance. Most patients with VS present with progressive asymmetric SNHL. Multiple studies demonstrate a similar pattern of hearing loss in their observational cohorts, with rates of serviceable hearing at 1, 3, 5, 7, and 10 years to be 94%, 77%, 66%, 56%, and 44% respectively [32,33,34]. Tumor volume was also associated with worse hearing as indicated by higher pure tone averages (PTA) and decreased word recognition scores [35]. Worse hearing at presentation was also independently associated with the risk of progressing to non-serviceable hearing, with every 10 dB increase in PTA doubling the risk and every 10% decrease in WRS increasing risk 1.5 fold [33].

In a systemic review including 2,100 unique sporadic VS patients, on average, half the patients had preserved good and/or serviceable hearing after five years of observation [36]. Elliot et al. demonstrated no significant differences in hearing survival in patients who underwent stereotactic radiosurgery (SRS) versus observation (35 months vs 48 months, p = 0.276) [37]. Similarly, for both observation and SRS, the risk of hearing loss increases with time [38]. In contrast, the risk of hearing loss is much higher following microsurgical resection, but postoperative hearing preservation is much more durable compared to the other two interventions [38]. Prognostic predictors for better postoperative hearing including better preoperative PTA and WRS, small tumor size (< 1cm), and the presence of a cerebrospinal fluid fundal cap in the internal auditory canal [38]. In contrast, in patients with NF2-SWN, tumors are more likely to grow during observation, can be less responsive to radiation, and result in more complications following surgery due to more adhesions and higher difficulty with tumor resection [39,40,41].

CI Outcomes in Sporadic VS

CI indication expansion to SSD and AHL population has made this treatment modality more common in sporadic VS patients. Emerging literature increasingly validates hearing improvements and tinnitus reduction following cochlear implantation during sporadic VS resection. Previously, numerous studies on CI outcomes focused on NF2-SWN; however, most VS patients present with sporadic unilateral tumors with hearing loss in the ipsilateral ear [42]. To better identify individuals who would benefit from simultaneous VS resection and CI, intraoperative assessment of cochlear nerve function should be performed [43,44,45,46,47]. Cochlear implantation can be done concurrent with or subsequent to tumor resection, but there is a potential risk of cochlear ossification if CI was not implanted simultaneously [48]. A systematic review found that sporadic VS tumors were smaller in size than NF2 tumors, had better pre-operative hearing, were most commonly resected through the translabyrinthine approach, and achieved superior CI performance level in 80% of patients [49]. A prospective study of 13 patients undergoing simultaneous translabyrinthine resection and cochlear implantation revealed improvement in speech perception at 12-month follow-up with 75% of patients having high (67%‐100%) CNC score, 16.7% intermediate (34%‐66%), and 8.3% low (0%-33%) CNC score with most gains achieved within 3 months [6•]. Conway et al. also reported improvement of Arizona Biomedical Sentence Test (AzBIO) + 5 dB SNR from 82% preoperatively to 94% postoperatively as well as improvement in tinnitus based on Tinnitus Handicap Index (THI) scores decreasing from 41 preoperatively to 23 at 3-month follow-up [50].

The management strategy for VS also appears to impact CI outcomes. Urban et al. compared CI outcomes in observation versus SRS with two patients in each group. The reported CNC scores post-implantation were 64% and 22% in the observation group, compared to 70% and 78% in the SRS group. Pre-implantation CNC scores were not reported; however, SRS therapy may offer more favoarble CI outcomes compared to tumors observation [51]. Further evidence of CI outcomes following observation was provided by Longino et al. This study identified 7 patients with non-growing sporadic tumors. CI outcomes without tumor resection or radiation resulted in CNC improvement from 6% pre-op to 55% 12 months post-op [52]. These studies shed light on less invasive treatment options of VS; however, surgical management remains a common management modality, especially for large tumors [53]. A prospective study of simultaneous CI and translabyrinthine VS resection of tumors ≤ 2 cm by Doerfer et al. followed patients for 12 months following implantation. These patients experienced improvement in speech perception in quiet (CNC improved from 39% preop to 69% post-op) and noise (AzBio + 10 SNR improved from 90% pre-op to 98.8% post-op), as well as reduction in tinnitus (THI from 32.5 to 14.0) [6•]. While both observation and surgical management studies report speech perception improvment, CNC score improved by 49% in Longino’s observation group and only 30% in Doerfer’s surgical group. These outcomes are further supported by a Dornhoffer et al. study that examined CI outcomes according to VS management modality in 49 patients, 21 of whom have sporadic VS. All patients managed with observation (n = 7) or radiosurgery (n = 8) achieved open-set speech. Whereas 4 of 6 patients who underwent microsurgery achieved open-set speech recognition [54]. These findings suggest that VS management strategy may significantly impact CI outcomes, and less invasive treatment such as observation or radiosurgery may be considered for patients interested in CI.

CI Outcomes in NF2-SWN

Surgical advancements to preserve the auditory nerve during NF2 resection allows for cochlear implantations in some NF2 patients with potentially  favorable hearing outcomes. NF2 patients usually have multiple tumors that are more aggressive. Tumors are also likely to be larger and growing compared to non-NF2 VS. The larger tumor size, multifocality, and invasion of neurovasculature may contribute to the less favorable CI outcomes in this population compared to non-NF2 patients. In a cohort of 48 patients, 77% of CI recipients achieved open-set speech perception compared to only 12% in the ABI cohort. While tumor management modality varied in this cohort and 3 patients received both a CI and an ABI, hearing outcomes with CI greatly surpass ABI [54]. A retrospective study reported 100% open-set speech recognition (n = 5) with a CI at an average of 38 months follow-up [55]. Another long-term study reported that of 12 patients with bilateral VS, 75% could communicate with lip-reading and 50% could communicate by telephone at an average follow-up time of 20 months [56].

A retrospective study found that 4 out of 12 NF2-SWN patients achieved open-set speech discrimination without lip-reading. Ipsilateral tumors of these 4 patients were managed by Bevacizumab post-CI, SRS (n = 2) or fractionated stereotactic radiotherapy prior to CI. Another four patients achieved speech discrimination with the aid of lip-reading; ipsilateral tumors of these patients were managed by Bevacizumab post-CI (n = 2) or SRS prior to implant (n = 2). The remaining 4 patients who did not achieve speech discrimination were managed by surgical excision concurrent with implant, partial tumor resection and radiotherapy prior to implant, retrosigmoid debulking, or observation [57]. Based on these results, tumors managed with radiotherapy may be associated with improved CI performance.

Similar outcomes are reported by a more recent study by Deep et al. which followed 24 NF2 patients whose ipsilateral VS were managed with microsurgery (n = 12), SRS (n = 5), and observation (n = 7). Amongst 12 patients undergoing microsurgical resection, 7 of 7 patients with tumors less than 1.5 cm achieved open-set speech discrimination. By contrast, only 1 out of 5 (20%) whose tumor was larger than 1.5 cm achieved open-set speech. In patients who underwent SRS, 5 of 5 patients (100%) achieved open-set speech regardless of tumor size. Finally, 6 of 7 (87%) patients whose tumor was observed achieved open-set speech discrimination [58••]. Taken together, the successful performance of CI in NF2-SWN patients is dependent on factors including appropriate patient selection, treatment strategy, and tumor size [54, 58••, 59].

In the discussion of CI outcomes, it's crucial to acknowledge that the duration and timeline of performance improvement may vary between NF2 and non-NF2 patients with CI. A retrospective study of 17 patients, 9 with NF2, showed that compared to sporadic VS (n = 8), NF2 cases had worse early postoperative results at 3 months but continued to improve within 6–24 months with consistent CI use [60]. It is possible that worse CI outcomes are influenced by patients becoming non-users following disappointing results in the initial period. This underscores the importance of educating patients and setting realistic expectations.

Considerations for NF2 Patient Selection

To best select NF2-SWN patients who may benefit from CI, several factors should be considered. Pre-operatively, larger tumor size [49, 58••, 61] and good contralateral hearing [56, 60] might compromise results post-implantation. In the study by Deep et al., patients who achieved open-set speech following CI (n = 19) exhibited smaller tumors (mean size 1.2cm, SD 0.7) compared to those who only attained auditory perception (n = 5; mean size 2.5cm, SD 0.4), regardless of management modality [58••]. Seo et al. conducted a longitudinal study on the use of CI in NF2-SWN patients. Tumor size was the sole variable influencing CI outcomes: CI non-users had a significantly larger tumors compared to CI users (32 vs. 16 mm) [61]. The larger tumor size may be associated with worse cochlear nerve degeneration, multicentricity along the nerve and increased ototoxic secretions. Regarding contralateral hearing, Sorrentino et al. found that patients with impaired pre-operative contralateral hearing (AAO-HNS Hearing Classes C-D) showed improved CI outcomes at 24-months. Conversely, patients with non-impaired pre-operative contralateral hearing (Classes A/B) exhibited poorer audiometric outcomes (PTA 78.8 dB) [60]. These results indicating good contralateral hearing may be a negative prognostic factor, while unexpected, could be linked to the challenges patients face in integrating normal acoustic signals with electrical stimulation, potentially hindering daily CI use. However, it remains curcial to emphasize consistent CI use and implement a multidisciplinary approach to support effective patient adaption to hearing with an implant.

Intraoperatively, cochlear nerve monitoring is the most important factor in determining CI outcomes. Electrical promontory stimulation or electrically evoked auditory brainstem response (eABR) can be used to monitor cochlear nerve intraoperatively and predict cochlear implant performance [45, 47, 62,63,64]. Butler et al. performed a small retrospective study of 3 patients specifically addressing eABR functionality in predicting CI outcomes. Two patients had a reliable eABR signal intraoperatively. The signal in the third patient was lost due to technical difficulties intraoperatively. Only one of the patients (who had a reliable eABR signal) achieved open-set speech discrimination. The other patient with eABR signal became a non-user and did not achieve open-set speech signal [62]. This is a small sample size and more studies are needed to elucidate the benefit of eABR; however, it is a helpful tool to ensure cochlear nerve function before CI placement.

Future Implications

CI in the VS population has been met with strong enthusiasm given its potential for substantially altering the care of patients; however, the implications and nuances of this therapy warrant future study. Better assessment of cochlear neural integrity after resection is required. Intraoperatively, anatomic integrity is typically utilized as a surrogate marker for whether to proceed with implantation, but this is decidedly different from neural integrity. In the authors’ experience, there are instances of inadequate results or non-functional implants despite anatomic integrity. Postoperatively, cochlear promontory stimulation has shown predictive ability [11, 65,66,67], but integration of this into surgical management could prove difficult given the technical limitations of using this intraoperatively and the risk of labyrinthine fibrosis if implantation is performed in a delayed fashion [68]. Future investigation should focus on identifying biomarkers of neural integrity which could allow for more consistent CI performance.

An additional area of consideration is tumor surveillance after CI placement. In the past, magnet removal was required for MRIs, but recent advancements both in imaging techniques and implant technology have made it more feasible to perform MRI without substantial magnetic interference with image quality [69, 70]. However, high-definition imaging is required for tumor or postoperative surveillance, where small changes in size or shape may denote growth and dictate the need for future treatment (Fig. 1). Notably, a recent study by Dornhoffer et al. has noted no issues with surveillance after implantation in a relatively sizeable cohort of patients [71••]. Homogenization of imaging technique across centers may allow for adequate tumor surveillance despite potential artifact, but long-term assessment of tumor surveillance in this setting is required to assure that even small amounts of change can be accurately observed.

Fig. 1
figure 1

Representative magnetic resonance images from a patient with a history of a left-sided sporadic vestibular schwannoma status post translabyrinthine approach and resection. A. showcases a T1-weight MRI with contrast and B. depicts a T2-weight MRI. Note the distortion associated with the cochlear implant magnet, which mandates close evaluation of the surgical cavity through multiple sequences and slices

Full size image

Data on non-tumor CIs has noted that limiting the duration of deafness prior to implantation portends better audiologic outcomes [72]. Although the pathophysiology of hearing decline in VS patients remains to be completely elucidated [73], it is likely that the duration of hearing loss in VS could affect CI performance. With results in the study by Dornhoffer et al. [71••], investigation into the implantation of observed VS is warranted, with the potential for patients to be rehabilitated even if tumor treatment is not indicated. An additional consideration is the effect of timing of implantation on outcomes after microsurgical resection. Simultaneous implantation is typically recommended given the risk of cochlear ossification [68], but both clinical and billing considerations may prevent this from occurring. Delayed implantation can be performed as evidenced by small series [62, 71••], but further study is needed to assess the implications of this delay on the ultimate hearing result.

Moreover, within CI literature at-large, there has been an increasing focus on outcomes such as quality-of-life [74,75,76,77,78]. CI-specific quality-of-life tools have been formulated and applied to various CI populations, but implementation of these measures in the VS population has not yet occurred. When considering NF2 patients, who are at high risk of bilateral profound hearing loss, benefits such as sound awareness are of particular importance and may be better suited for evaluation via quality-of-life measures than traditional audiometric testing. Similarly, the benefits of restoring binaural hearing in the sporadic VS population serves as an area of further quality-of-life study as has been noted in the SSD population [25]. In combination, this area appears ripe for further research as the field attempts to understand the marriage of this technology into the care of VS patients.

Conclusion

In conclusion, CI outcomes in patients with VSs greatly vary depending on management strategies, with less invasive strategies like observation or radiosurgery consistently being associated with superior audiometric outcomes. In patients with NF2, hearing outcomes with CI exceed those with the traditional ABIs, but patient specific factors, including tumor size and treatment strategy, are critical in selecting patients who could benefit from this modality. Future directions include investigation into biomarkers for neural integrity to optimize postoperative CI performance, tumor surveillance technology, and quality-of-life measurements in the VS population.