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Cochlear implants and tinnitus
B. Langguth, G. Hajak, T. Kleinjung, A. Cacace & A.R. Møller (Eds.) Progress in Brain Research, Vol. 166 ISSN 0079-6123 Copyright r 2007 Elsevier B.V. All rights reserved
CHAPTER 33
Cochlear implants and tinnitus David M. Baguley1,2, and Marcus D. Atlas2 1 Audiology, Addenbrooke’s Hospital, Hills Road, Cambridge, CB2 2QQ, UK Ear Sciences Centre, School of Surgery and Pathology, University of Western Australia, Perth, Australia
2
Abstract: The clinical observation that multichannel intra-cochlear cochlear implants have a suppressive effect on tinnitus in profoundly deaf patients is supported by many published studies. Whilst there are problems with that literature, specifically in the way that tinnitus outcomes are reported, the finding of tinnitus benefit is consistent. New developments in this area include the use of functional imaging to investigate tinnitus suppression by cochlear implant stimulation and consideration of a reported worsening effect on tinnitus of binaural implantation. Following work on hearing aids, it is suggested that optimization of the benefit of monaural cochlear implantation on tinnitus in a tinnitus-specific electrode configuration might include the use of a low knee point compression algorithm and disabling directional microphone function: these strategies are potentially also of benefit in patients whose tinnitus results in sleep disturbance. Opportunities for stimulation strategies for tinnitus suppression that bypass speech processing are also identified. Keywords: tinnitus; cochlear implant; auditory brainstem implant development of novel treatment strategies for tinnitus that utilize electrical stimulation of the cochlea (auditory nerve). The purpose of the present paper is to draw out the themes evident in published research in the area of cochlear implants and tinnitus, and then to consider developments in the field, specifically binaural cochlear implantation, modified electrode arrays and cochlear implantation for tinnitus in patients with unilateral severe profound sensorineural hearing loss (SNHL).
Introduction Clinicians working with cochlear implant patients have often reported that implant use can have a beneficial effect on tinnitus (Miyamoto and Bichey, 2003). Indeed, considerable published research supports this observation. Thus a recent review (Quaranta et al., 2004) identified 32 published papers (of which 12 were from the peerreview literature) that explicitly discussed the effect of cochlear implants on tinnitus. Whilst this body of literature has inconsistencies, it does provide useful material for a scientific consideration of tinnitus, and may potentially guide us towards optimizing the inhibitory effect of a cochlear implant on tinnitus. Further, it may facilitate the
The prevalence of tinnitus in cochlear implant candidates Many papers reporting series of patients undergoing cochlear implantation indicate the number reporting tinnitus, but unfortunately there are no
Corresponding author. Tel.: 01223 217594;
Fax: 01223 596101; E-mail: [email protected] DOI: 10.1016/S0079-6123(07)66033-6
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consistent definitions of that tinnitus. One might therefore expect some authors to be reporting patients with any tinnitus experience at all, and others patients with tinnitus that was severe enough to be troublesome. Further, such papers have not utilized the validated questionnaires that are in regular use in the tinnitus field, such as the Tinnitus Handicap Inventory (THI) (Newman et al., 1996) or the Tinnitus Questionnaire (Hallam, 1996), so one is unable to determine the extent to which tinnitus is bothersome in this population. Despite these concerns, there is relative consistency in the reported prevalence of tinnitus in patients about to undergo cochlear implantation. The existing data is summarized in Table 1, and indicates that in 18 research papers reporting a total of 1104 cochlear implant candidates, a range of prevalence data from 67 to 100% with a mean of 80% is demonstrated. In general terms therefore one can observe that one in five of the patient population who have acquired severe to profound hearing loss or deafness either have tinnitus that is only mildly troublesome, or no tinnitus at all. In this analysis papers have been considered that were published from 1990 to 2006. It should be
Table 1. Prevalence of tinnitus in cochlear implant candidates Author
Tinnitus prevalence (%)
Tyler and Kelsey (1990) McKerrow et al. (1991) Bredberg et al. (1992) Souliere et al. (1992) Gibson (1992) Tyler (1994) Kou et al. (1994) Hazell et al. (1995) Ito (1997) Miyamoto et al. (1997) Aschendorff et al. (1998) Demajumdar et al. (1999) Greimel et al. (2002) McKinney et al. (2002) Mo et al. (2002)
42/52 (81) 6 (100) 18/21 (86) 28/33 (85) 42/52 (85) 30/41 (73) 14/23 (70) 202/256 (79) 54/60 (90) 48/64 (75) 32/47 (68) 80/99 (80) 26/39 (67) 46/56 (82) 59/74 (80); ‘troublesome’ in 29 (35) 59/91 (65) 44/61 (72) 21/29 (72)
De Coninck et al. (2006) Kompis et al. (2006) Yonehara et al. (2006)
noted that candidacy criteria for cochlear implantation are changing, and becoming less constraining. In particular, patients with severe SNHL became considered as candidates during this time period, rather than only those with a profound hearing loss only being considered initially. Candidates with severe acquired SHNL may have differences in prevalence and severity of tinnitus than the traditional cohort: robust published data is not yet available in this regard.
Effect of surgery The insertion of an intra-cochlear implant electrode is potentially traumatic to any remaining functional cochlear structures (Adunka and Kiefer, 2006), and is believed to involve both necrotic and apoptotic mechanisms of cell death (Eshraghi and Van de Water, 2006) and such electrode insertion may influence tinnitus. Intriguingly however, in the small number of papers which consider this issue there are indications that for some patients there may be an improvement in tinnitus associated with electrode insertion (Gibson, 1992; Kim et al., 1995; Greimel et al., 2002), though the positive expectations of the patient regarding the implant may be a factor in this regard. There are also reports of small numbers of patients in whom electrode insertion exacerbates tinnitus (>10%) (Gibson, 1992) or precipitates it being heard for the first time (>4%) (McKerrow et al., 1991; Tyler, 1994; Miyamoto et al., 1997). Changes in tinnitus pitch and timbre have also been reported (Souliere et al., 1992).
Effect of use of monaural intra-cochlear devices Studies that have reported the effect on tinnitus of the use of monaural multichannel cochlear implants are summarized in Table 2. Whilst there are marked inconsistencies in the way that tinnitus outcomes are reported, it can be seen that for the overwhelming proportion of patients, cochlear implant use has a very significantly beneficial effect on tinnitus. The possibility that this is not only an auditory phenomenon but also linked with
349 Table 2. The influence of multichannel cochlear implants upon tinnitus Author
Cases
Type of implant
Tinnitus effect ipsilateral
Mixed (single and multichannel)
34 (81%) improved 7 (17%) same 1 (2%) worse 5 (83%) abolished 1 (17%) same 20 (77%) improved 25 (61%) better 16 (39%) same 25 (83%) improved 5 (17%) same 73/127 (57%) better 43/127 (44%) same 11/127 (9%) worse Group data indicates statistically significant decrease in loudness and annoyance 12 (86%) partial or complete elimination of tinnitus when CI on 5 (36%) complete elimination 6 (26% of total series) developed tinnitus as a result of implant surgery 10 (77%) better 3 (23%) same 40 (74%) very effective 10 (19%) effective 4 (7%) unchanged 22 (46%) better 24 (50%) same 2 (4%) worse 22 (69%) better 10 (31%) no change 62 (78%) abolished 17 (45%) abolished 19 (50%) reduced 3 (5%) unchanged 15.4% abolished 26.7% decreased 50% unchanged 32 (54%) better 21 (36%) no change 5 (8%) worse 1 (2%) abolished 11 (55%) complete inhibition 5 (25%) significant attenuation 4 (20%) no change 29% abolished 30% reduced loudness 36 (72%) improved 2 (5%) unchanged 6 (13%) worsened 2 of 15 patients (15%) who do not have preoperative tinnitus developed it in the first 6 months of device use 7 (33%) total suppression 8 (37%) partial suppression
Tyler and Kelsey (1990)
42
McKerrow et al. (1991)
6
UCSF/Storz 4 channels
Souliere et al. (1992) Gibson (1992)
28 41
Multichannel (Nucleus) Multichannel (Nucleus)
Tyler (1994)
30
Multichannel (Ineraid and Nucleus)
Hazell et al. (1995)
127
Mixed
Bredberg et al. (1992)
18
Mixed
Kou et al. (1994)
14
Nucleus 22 channel
Kim et al. (1995)
13
Multichannel (Nucleus)
Ito (1997)
54
Multichannel (Nucleus)
Miyamoto et al. (1997)
48
Multichannel 55 (Nucleus and Clarion) Single channel 9
Aschendorff et al. (1998)
32
Multichannel (Nucleus)
Demajumdar et al. (1999) Ruckenstein et al. (2001)
80 38
Multichannel (Nucleus) Multichannel (Nucleus and Clarion)
Greimel et al. (2002)
26
Not stated
Mo et al. (2002)
59
Multichannel intracochlear
Daneshi et al. (2005)
20
Multichannel
De Coninck et al. (2006)
91
Multichannel (Nucleus and Hires, Laura)
Kompis et al. (2006)
44
Not stated
Yonehara et al. (2006)
21
Nucleus 24K
350 Table 3. The influence of multichannel cochlear implants upon tinnitus in the contralateral ear Authors
Contralateral improvement
McKerrow et al. (1991) Souliere et al. (1992) Hazell et al. (1995) Kim et al. (1995) Fukuda and Mangabeira Albernaz (1998) Demajumdar et al. (1999)
67% 42% 52% better 71% 20% suppressed 20% decreased Tinnitus abolished in 14/70 (20%) 86% ‘‘totally suppressed or decreased’’
Yonehara et al. (2006)
neurophysiological model of tinnitus (Jastreboff, 1990), and the benefit from the use of Tinnitus Retraining Therapy (Jastreboff and Hazell, 1993), it is a reminder that a particular model may not cover all aspects of the functions of a complex system such as the auditory nervous system and that model predictions may not be supported exactly by experimental or empirical evidence. This also applies to other models (Baguley, 2006) such as the model of psychological aspects of tinnitus described by Hallam et al. (1984).
Optimization increased quality of life has been noted (McKinney et al., 2002, Mo et al., 2002). Several trends have been observed. The first (Quaranta et al., 2004) is that intra-cochlear multichannel devices (cochlear implants appear to have a more positive effect on tinnitus than the initially available extracochlear single channel devices, which were also less effective in providing auditory abilities (House, 1976; Berliner et al., 1987). Second, it appears that the use of a monaural cochlear implant may improve tinnitus in the contralateral ear (Quaranta et al., 2004). Data summarized in Table 3 indicate that for many patients, utilizing a cochlear implant in one ear can markedly reduce the perceived intensity of tinnitus in the contralateral ear. It has been suggested that this is due to masking (Battmer et al., 1989) or due to plastic reorganization of the auditory system, both of the ipsilateral and contralateral pathways, following cochlear implant use (Quaranta et al., 2004). Additionally, there is experimental evidence of the influence of contralateral auditory stimulation on neural activity evoked by sound in the ipsilateral pathways (Davis, 2005); this has been demonstrated to be both inhibitory (Ingham et al., 2006) and excitatory (Sumner et al., 2005). The finding of contralateral inhibition of tinnitus disagrees with the prediction of Jastreboff (2000) that in a patient with tinnitus, asymmetric or unilateral sound stimulation should exacerbate tinnitus contralateral to that of stimulation. While it does not affect other aspects of Jastreboff’s
It should be noted that cochlear implant stimulation strategies are designed to optimize speech discrimination, but they may not be optimal for tinnitus inhibition (Andersson et al., 2005). There has been little preliminary work in this area. A study of two individuals with tinnitus who had cochlear implants by Dauman and Tyler (1993) attempted to identify the optimal stimulation rate and electrode location that was most effective in suppression of tinnitus. Rubinstein et al. (2003) studied the effect of electrical stimulation with 5000 pps pulse trains via cochlear implant in 3 individuals and via a transtympanic electrode in 11 individuals, and found that ‘‘between a third and a half of them achieve clinically significant tinnitus suppression without a sustained percept’’. Vernon (2000) reported that masking with noise (6–14 kHz) via a Nucleus 22 cochlear implant was beneficial to an individual with bilateral tinnitus, leading to some residual inhibition lasting 2–3 min and some contralateral suppression. A preliminary report of the use of a commercialized extracochlear device delivering electrical stimulation to the oval window showed beneficial effect on tinnitus (Frachet et al., 2006). This remains an interesting area. Aspects of programming of a hearing aid for optimal suppression of tinnitus benefit may have some relevance for cochlear implant programming (see Chapter 32). Searchfield (2005) suggests that low compression knee points should be used when programming hearing aids for tinnitus relief and directional microphone technology should be
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disabled. Both of these changes will increase the amount of ambient and environmental sound that is delivered to the ear by the hearing aid. These tactics are variously feasible in current cochlear implant devices. If a patient has sleep disturbance and troublesome tinnitus (see Chapter 21), one might consider programming a cochlear implant device for nighttime use. There are two possibilities: first one might utilize a program that facilitates night-time use of an environmental sound generator, with sounds such as wind, rain, or the ocean — devices that have been shown effective in tinnitus therapy in individuals with hearing (Andersson et al., 2005; Handscomb, 2006). Second, one might consider an implant electrode configuration that gives barely suprathreshold stimulation through the night to reduce the awareness of tinnitus. As with hearing aids, optimizing a cochlear implant for tinnitus may involve programming that reduces speech discrimination abilities. The tinnitus program should therefore be addition to the program that is in general use of the cochlear implant (speech communication). There are two areas of interest where the existing literature is deficient. The first is consideration of the time course of tinnitus inhibition associated with cochlear implant use, about which there is little or no mention in the literature. This is potentially of some interest, as it may shed light on the mechanism by which tinnitus benefit is achieved. If the benefit is immediate one might consider that masking of the tinnitus by the new auditory information is occurring. If, however, the tinnitus suppression occurs over time, then some process of plastic reorganization of the auditory system following implant use can be inferred. These mechanisms are not mutually exclusive, and a longitudinal study would not resolve this completely, but might shed some light on this matter. The second area is that of children. The existing literature relates to adults, and there is minimal information regarding children with cochlear implants and tinnitus. This is anomalous, as hearing impaired children are known to have prevalent and occasionally severe tinnitus (see Baguley and McFerran, 2002 for review), and the response of
that tinnitus to cochlear implantation would be of some interest, both clinically and scientifically. New developments Binaural cochlear implants In a study by Summerfield et al. (2006) of selfreported benefits from successive cochlear implantation in post-lingually deafened adults, receipt of a second implant led to significant improvements in self-reported abilities in spatial hearing, quality of hearing and in speech perception, but, counterintuitively, to non-significant changes in quality of life. The essential aim of the study was to determine the incremental benefit (or otherwise) of a second implant. The study had 24 adult participants who were implanted with Nucleus CI24 devices. The participants were randomized either to receive a second implant immediately or to wait 12 months; this latter group acting as a control for emerging benefits of the second device. Multivariate analysis indicated that any improvement in quality of life associated with improved auditory abilities was offset by negative changes associated with worsening of their tinnitus. Of 16 patients with pre-operative tinnitus, 7 reported a worsening (44%), and of 8 patients who did not report tinnitus pre-operatively, 4 (50%) reported that the second implant had induced tinnitus. While the incidences of tinnitus are higher than those generally reported for unilateral implantation (see Table 2) they are not statistically significantly different from normal (Summerfield et al., 2006). Worsened tinnitus following sequential binaural implantation may therefore be sufficient to offset other benefits following surgery. Functional imaging and cochlear implants Mirz et al. (2002) used positron emission tomography (PET) to demonstrate the suppressive effect of a cochlear implant in a patient with distressing tinnitus. The use of the cochlear implants not only reduced signs of tinnitus-related activity in primary auditory and associate cortices, but also in areas of the CNS associated with emotion
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(limbic system) and attention (dorsolateral prefrontal cortices). PET in three patients (Osaki et al., 2005) in whom there was a marked residual inhibitory effect of cochlear implant use on tinnitus, showed that the right anterior middle and superior temporal gyri (Brodmann areas 21 and 38) were activated during residual inhibition after device use, whereas the right cerebellum was activated during tinnitus perception in the tinnitus patients. Such residual inhibition of tinnitus with cochlear implant use is common (Kim et al., 1995), but may be fleeting (Souliere et al., 1992). The authors concluded that tinnitus, and the residual inhibition of the tinnitus, are associated with central processes of auditory higher order processing, memory and attention. This hypothesis requires significant further research before conclusions can be drawn.
Unilateral SNHL and tinnitus Idiopathic unilateral sudden SNHL has an incidence of 2–20/100,000 adults per year (Byl, 1984), leading to estimates of 2835–9540 cases per year in the UK alone (Baguley et al., 2006). The hearing loss does not recover in more than 60% of cases in spite of therapy, mainly because the cause and pathogenesis of sudden deafness is unknown (Merchant et al., 2005). When hearing loss remains severe, tinnitus in the same ear may be disabling as shown by Chiossoine-Kerdel et al. (2000) using the THI (Newman et al., 1996). The same authors also demonstrated a significant hearing handicap in the majority (86%) of these unilaterally affected patients when assessed with the Hearing Handicap Inventory for Adults (Newman et al., 1990). Therefore, tinnitus consecutive to sudden deafness with poor recovery remains a therapeutic challenge (Andersson et al., 2005). Contralateral routing of signal (CROS) and bone-anchored hearing aids (BAHA) can be utilized in auditory rehabilitation, with varying degrees of success (Baguley et al., 2006), but little or nothing can be offered for relief of the tinnitus. A cochlear implant on the affected side may benefit and not only reduce the hearing handicap
but it may also provide relief for the tinnitus. The application of a cochlear implant to such individuals has so far only been reported in a conference report where Van de Heyning et al. (2006) described a series of 10 patients with a unilateral profound SNHL, associated with ‘‘incapacitating and refractive tinnitus’’ and with normal hearing in the contralateral ear. These individuals were implanted with the Medel Combi 40+ device. On individuals whose tinnitus could be reduced by at least 50% by electrical promontory stimulation were included in the study. Statistically significant improvements in measures of tinnitus loudness (visual analog scale) and impact (Tinnitus Questionnaire, Hallam, 1996) were achieved in all these individuals and all were reported to have used the device all their waking hours for the 12-month duration of the study. In a further report from the same group, Vermeire et al. (2006) describe 18 similar patients (probably including those from the initial report). An additional inclusion criteria described is a >50% inhibition of the tinnitus by electrical promontory stimulation. Programming strategies and outcome measures are not described, but the authors stated ‘‘there was no conflict between the hearing with the CI and the hearing in the opposite ear’’. It has been reported that it is possible to integrate regular hearing with cochlear implant stimulation (Dunn et al., 2005) though such auditory fusion may not be possible in all individuals. Optimizing the device for tinnitus inhibition might however involve non-speech related stimulation, and an approach such as the pulse train stimulation trialed by Rubinstein et al. (2003) becomes an option. The development of modified electrode arrays, which aim to preserve lowfrequency acoustic hearing and allow mid, and high-frequency electrical stimulation (Gantz and Turner, 2004; Gantz et al., 2006; James et al., 2006; Briggs et al., 2006, for example) may offer some benefit for such patients, many of whom experience troublesome tinnitus. Soussi and Otto (1994) studied 10 patients who had received an auditory brainstem implant (ABI) following removal of a vestibular schwannoma in patients with neurofibromatosis type 2. Of these, seven used their implant daily, and six of these
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‘‘reported noticeable tinnitus reduction’’ — this represents 86% of the daily user group. This finding is of some potential interest, as the dorsal cochlear nucleus (DCN) (Kuroki and Møller, 1995; Kaltenbach, 2006; Shepherd and McCreery, 2006) has been implicated in tinnitus perception. The electrode array of the ABI is inserted into the lateral recess of the fourth ventricle and placed over the surface of the ventral and dorsal cochlear nuclei (Kuroki and Møller, 1995; Fayad et al, 2006; Shepherd and McCreery, 2006). Progress toward a midbrain implant is also evident (Lenarz et al., 2006; Colletti et al., 2007) and provides further opportunity for the investigation of the possibility of using electrical stimulation of the central auditory system in controlling tinnitus. Conclusions This paper has reviewed current observational evidence regarding the effects of cochlear implants on tinnitus. The current literature supports the clinical observation that cochlear implants have a marked suppressive effect on tinnitus in most cochlear implant users. The situation may be different for binaural cochlear implants where auditory benefits of a second implant may be offset by an exacerbation of tinnitus in some patients. Cochlear and brainstem implants can also seems to provide reduction of tinnitus but the experience of such implants is much smaller than that of cochlear implants. Acknowledgment This paper was written while David Baguley was a Raine Visiting Professor at the Ear Sciences Institute, University of Western Australia. The support of the Raine Foundation, of Phonak Pty, of the British Tinnitus Association and of Deafness Research UK is gratefully acknowledged. References Adunka, O. and Kiefer, J. (2006) Impact of electrode insertion depth on intracochlear trauma. Audiol. Neurootol., 11(Suppl. 1): 57–62.
Andersson, G., Baguley, D.M., McKenna, L. and McFerran, D. (2005) Tinnitus: a multidisciplinary approach. Whurr, London. Aschendorff, A., Pabst, G., Klenzner, T. and Laszig, R. (1998) Tinnitus in cochlear implant users: the Freiburg experience. Int. Tinnitus J., 4: 162–164. Baguley, D.M. (2006) What progress have we made with tinnitus? Acta Otolaryngol. Suppl., 556: 4–8. Baguley, D.M., Bird, J., Humphriss, R.L. and Prevost, A.T. (2006) The evidence base for the application of contralateral bone anchored hearing aids in acquired unilateral sensorineural hearing loss in adults. Clin. Otolaryngol., 31(1): 6–14. Baguley, D.M. and McFerran, D. (2002) Current perspectives on tinnitus. Arch. Dis. Child., 86: 141–143. Battmer, R.D., Heermann, R. and Laszig, R. (1989) Suppression of tinnitus by electric stimulation in cochlear implant patients. HNO, 37: 148–152. Berliner, R.I., Cunningham, J.K., House, W.F. and House, J. (1987) Effect of the cochlear implant on tinnitus in profoundly deaf patients. In: Feldman, H. (Ed.), Proceedings of the Third International Tinnitus Seminar, Karlsruhe Harsh, Munster, Germany, pp. 451–453. Bredberg, G., Walden, J. and Lindstro¨m, B. (1992) Tinnitus after cochlear implantation. In: Aran J.M. and Dauman R. (Eds.), Proceedings of the Fourth International Seminar, Bordeaux. Kugler, Amsterdam/New York, pp. 417–422. Briggs, R.J., Tykocinski, M., Xu, J., Risi, F., Svehla, M., Cowan, R., Stover, T., Erfurt, P. and Lenarz, T. (2006) Comparison of round window and cochleostomy approaches with a prototype hearing preservation electrode. Audiol. Neurootol., 11(Suppl. 1): 42–48. Byl, F.M. (1984) Sudden hearing loss: eight years experience and suggested prognostic table. Laryngoscope, 94(1): 647–661. Chiossoine-Kerdel, J.A., Baguley, D.M., Stoddart, R.L. and Moffat, D.A. (2000) An investigation of the audiologic handicap associated with unilateral sudden sensorineural hearing loss. Am. J. Otol., 21(5): 645–651. Colletti, V., Shannon, R., Carner, M., Sacchetto, L., Turazzi, S., Masotto, B. and Colletti, L. (2007) The first successful case of hearing produced by electrical stimulation of the human midbrain. Otol. Neurotol., 28(1): 39–43. Daneshi, A., Mahmoudian, S., Farhadi, M., Hasanzadeh, S. and Ghalebaghi, B. (2005) Auditory electrical tinnitus suppression in patients with and without implants. Int. Tinnitus J., 11(1): 85–91. Dauman, R. and Tyler, R.S. (1993) Tinnitus suppression in cochlear implant users. Adv. Otorhinolaryngol., 48: 168–173. Davis, K.A. (2005) Contralateral effects and binaural interactions in dorsal cochlear nucleus. J. Assoc. Res. Otolaryngol., 6(3): 280–296. De Coninck, L., Zarowski, A., Schatteman, I., Verstreken, M., Somers, T., Peeters, S. and Offeciers, E. (2006) Tinnitus suppression by electrical stimulation with cochlear implants: study of 100 patients. In: Baumgartner W.D. (Ed.), 9th International Conference on Cochlear Implants and Related Sciences. Wein Med. Wochenschr. 156(Suppl. 118), p. 59.
354 Demajumdar, R., Stoddart, R., Donaldson, I. and Proops, D.W. (1999) Tinnitus, cochlear implants and how they affect patients. J. Laryngol. Otol. Suppl., 24: 24–26. Dunn, C.C., Tyler, R.S. and Witt, S.A. (2005) Benefit of wearing a hearing aid on the unimplanted ear in adult users of a cochlear implant. J. Speech Lang. Hear. Res., 48(3): 668–680. Eshraghi, A.A. and Van de Water, T.R. (2006) Cochlear implantation trauma and noise-induced hearing loss: apoptosis and therapeutic strategies. Anat. Rec. A Discov. Mol. Cell. Evol. Biol., 288(4): 473–481. Fayad, J.N., Otto, S.R. and Brackmann, D.E. (2006) Auditory brainstem implants: surgical aspects. Adv. Otorhinolaryngol., 64: 144–153. Frachet, B., Pean, V., Vormes, E., Philippoon, B. and Veran, D. (2006) Tinnelec: tinnitus reduction implant by electrical stimulation of the oval window. In: Baumgartner W.D. (Ed.), 9th International Conference on Cochlear Implants and Related Sciences. Wein Med. Wochenschr. 156(Suppl. 118), p. 60. Fukuda, Y. and Mangabeira Albernaz, P.L. (1998) The all hear cochlear implant and tinnitus. Int. Tinnitus J., 4(2): 159–161. Gantz, B.J. and Turner, C. (2004) Combining acoustic and electrical speech processing: Iowa/Nucleus hybrid implant. Acta Otolaryngol., 124(4): 344–347. Gantz, B.J., Turner, C. and Gfeller, K.E. (2006) Acoustic plus electric speech processing: preliminary results of a Multicenter Clinical Trial of the Iowa/Nucleus hybrid implant. Audiol. Neurotol., 11(Suppl. 1): 63–68. Gibson, W.P.R. (1992) The effect of electrical stimulation and cochlear implantation on tinnitus. In: Aran J.M. and Dauman R. (Eds.), Proceedings of the Fourth International Seminar, Bordeaux, 1991. Kugler, Amsterdam/New York, pp. 403–408. Greimel, K.V., Meco, C., Kohlbock, F., Mair, A. and Albegger, K. (2002) Changes in tinnitus after cochlear implantation. In: Patuzzi R. (Ed.), Proceedings of the Seventh International Tinnitus Seminar. University Western Australia, Australia, p. 6. Hallam, R.S. (1996) Manual of the tinnitus questionnaire, The Psychological Corporation. Brace & Co, London. Hallam, R., Rachman, S. and Hinchcliffe, R. (1984) Psychological aspects of tinnitus. In: Rachman S. (Ed.), Contributions to Medical Psychology, Vol. 3. Pergamon Press, Oxford, pp. 31–53. Handscomb, L. (2006) Use of bedside sound generators by patients with tinnitus-related sleeping difficulty: which sounds are preferred and why? Acta Otolaryngol. Suppl., 556: 59–63. Hazell, J.W.P., McKinney, C.J. and Aleksy, W. (1995) Mechanisms of tinnitus in profound deafness. Ann. Otol. Rhinol. Laryngol. Suppl., 166: 418–420. House, W.F. (1976) Cochlear implants. Ann. Otol. Rhinol. Laryngol. Suppl., 185: 185–193. Ingham, N.J., Bleeck, S. and Winter, I.M. (2006) Contralateral inhibitory and excitatory frequency response maps in the mammalian cochlear nucleus. Eur. J. Neurosci., 24(9): 2515–2529. Ito, J. (1997) Tinnitus suppression in cochlear implant patients. Otolaryngol. Head Neck Surg., 117: 701–703.
James, C.J., Fraysse, B., Deguine, O., Lenarz, T., Mawman, D., Ramos, A., Ramsden, R. and Sterkers, O. (2006) Combined electroacoustic stimulation in conventional candidates for cochlear implantation. Otolaryngol. Head Neck Surg., 135(3): 374–382. Jastreboff, P.J. (1990) Phantom auditory perception (tinnitus): mechanism of generation and perception. Neurosci. Res., 8: 221–254. Jastreboff, P.J. (2000) Tinnitus Habituation Therapy (THT) and Tinnitus Retraining Therapy (TRT). In: Tyler R.S. (Ed.), Tinnitus Handbook. Singular, San Diego, CA, pp. 357–376. Jastreboff, P.J. and Hazell, J.W. (1993) A neurophysiological approach to tinnitus: Clinical implications. Br. J. Audiol., 27(1): 7–17. Kaltenbach, J.A. (2006) The dorsal cochlear nucleus as a participant in the auditory, attentional and emotional components of tinnitus. Hear. Res., 216–217: 224–234. Kim, H.N., Shim, Y.J., Kim, Y.M. and Kim, E.S. (1995) Effect of electrical stimulation on tinnitus in the profoundly deaf. In: Reich G.E. and Vernon J. (Eds.), Proceedings of the Fifth International Tinnitus Seminar. American Tinnitus Association, Portland OR. Kompis, M., Pelizzpne, M., Diller, N., Allum, J. and Demin, N. (2006) Swiss multi-centre study on tinnitus and cochlear implantation. In: Baumgartner W.D. (Ed.), 9th International Conference on Cochlear Implants and Related Sciences. Wein Med. Wochenschr. 156(Suppl. 118), p. 59. Kou, B.S., Shipp, D.B. and Nedzelski, J.M. (1994) Subjective benefits reported by adult Nucleus 22-channel cochlear implant users. J. Otolaryngol., 23(1): 8–14. Kuroki, A. and Møller, A.R. (1995) Microsurgical anatomy around the foramen of Luschka in relation to intraoperative recording of auditory evoked potentials from the cochlear nuclei. J. Neurosurg., 82(6): 933–939. Lenarz, T., Lim, H.H., Reuter, G., Patrick, J.F. and Lenarz, M. (2006) The auditory midbrain implant: a new auditory prosthesis for neural deafness-concept and device description. Otol. Neurotol., 27(6): 838–843. McKerrow, W.S., Schreiner, C.E., Snyder, R.L., Merzenich, M.M. and Toner, J.G. (1991) Tinnitus suppression by cochlear implants. Ann. Otol. Rhinol Laryngol., 100: 552–558. McKinney, C.J., Nunn, T.B., Archer, K.A.M. and FitzgeraldO’Connor, A. (2002) Factors influencing tinnitus severity in cochlear implant patients In: Patuzzi R. (Ed.), Proceedings of the Seventh International Tinnitus Seminar. University Western Australia, Australia, pp. 176–181. Merchant, S.N., Adams, J.C. and Nadol, J.B. (2005) Pathology and pathophysiology of idiopathic sudden sensorineural hearing loss. Otol. Neurotol., 26(2): 151–160. Mirz, F., Mortensen, M.V., Gjedde, A. and Pederson, C.B. (2002) Positron emission tomography of tinnitus suppression by cochlear implantation. In: Patuzzi R. (Ed.), Proceedings of the Seventh International Tinnitus Seminar. University Western Australia, Australia, pp. 136–140. Miyamoto, R.T. and Bichey, B.G. (2003) Cochlear implantation for tinnitus suppression. Otolaryngol. Clin. N. Am., 36(2): 345–352.
355 Miyamoto, R.T., Wynne, M.K., McKnight, C. and Bichey, B. (1997) Electrical suppression of tinnitus via cochlear implants. Int. Tinnitus J., 3: 35–38. Mo, B., Harris, S. and Lindbaek, M. (2002) Tinnitus in cochlear implant patients — a comparison with other hearing impaired patients. Int. J. Audiol., 41: 527–534. Newman, C.W., Jacobson, G.P. and Spitzer, J.B. (1996) Development of the tinnitus handicap inventory. Arch. Otolaryngol. Head Neck Surg., 122(2): 143–148. Newman, C.W., Weinstein, B.E., Jacobson, G.P. and Hug, G.A. (1990) The hearing handicap inventory for adults: psychometric adequacy and audiometric correlates. Ear Hear., 11: 430–433. Osaki, Y., Nishimura, H., Takasawa, M., Imaizumi, M., Kawashima, T., Iwaki, T., Oku, N., Hashikawa, K., Doi, K., Nishimura, T., Hatazawa, J. and Kubo, T. (2005) Neural mechanism of residual inhibition of tinnitus in cochlear implant users. Neuroreport, 16(15): 1625–1628. Quaranta, N., Wagstaff, S. and Baguley, D.M. (2004) Tinnitus and cochlear implantation. Int. J. Audiol., 43(5): 245–251. Rubinstein, J.T., Tyler, R.S., Johnson, A. and Brown, C.J. (2003) Electrical suppression of tinnitus with high-rate pulse trains. Otol. Neurotol., 24(3): 478–485. Ruckenstein, M.J., Hedgepeth, C., Rafter, K.O., Montes, M.L. and Bigelow, D.C. (2001) Tinnitus suppression in patients with cochlear implants. Otol. Neurotol., 22: 200–204. Searchfield, G.D. (2005) Hearing aids and tinnitus. In: Tyler R.S. (Ed.), Tinnitus Treatment: Clinical Protocols. Thieme, New York, pp. 161–175. Shepherd, R.K. and McCreery, D.B. (2006) Basis of electrical stimulation of the cochlea and the cochlear nucleus. Adv. Otorhinolaryngol., 64: 186–205. Souliere Jr., C.R., Kileny, P.R., Zwolan, T.A. and Kemink, J.L. (1992) Tinnitus suppression following cochlear implantation. A multifactorial investigation. Arch. Otolaryngol. Head Neck Surg., 118: 1291–1297.
Soussi, T. and Otto, S.R. (1994) Effects of electrical brainstem stimulation on tinnitus. Acta Otolaryngol., 114(2): 135–140. Summerfield, A.Q., Barton, G.R., Toner, J., McAnallen, C., Proops, D., Harries, C., Cooper, H., Court, I., Gray, R., Osborne, J., Doran, M., Ramsden, R., Mawman, D., O’Driscoll, M., Graham, J., Aleskey, W., Meerton, L., Verschurre, C., Ashcroft, P. and Pringle, M. (2006) Self-reported benefits from successive bilateral cochlear implantation in post-lingually deafened adults: randomised controlled trial. Int. J. Audiol., 45(Suppl. 1): S99–S107. Sumner, C.J., Tucci, D.L. and Shore, S.E. (2005) Responses of ventral cochlear nucleus neurons to contralateral sound after conductive hearing loss. J. Neurophysiol., 94(6): 4234–4243. Tyler, R.S. (1994) Advantages and disadvantages expected and reported by cochlear implant patients. Am. J. Otol., 15: 523–531. Tyler, R.S. and Kelsey, D. (1990) Advantages and disadvantages reported by some of the better cochlear implant patients. Am. J. Otol., 11(4): 282–289. Van de Heyning, P., Vermiere, K. and De Ridder D. (2006) Tinnitus treatment with CI in unilateral deafness. In: Baumgartner W.D. (Ed.), 9th International Conference on Cochlear Implants and Related Sciences. Wein Med. Wochenschr. 156(Suppl. 118), p. 58. Vermeire, K., Schleich, P. and Ven de Heyning, P. (2006) Hearing capabilities after CI in unilateral sensorineural deafness and tinnitus. In: Baumgartner W.D. (Ed.), 9th International Conference on Cochlear Implants and Related Sciences. Wein Med. Wochenschr. 156(Suppl. 118), p. 59. Vernon, J.A. (2000) Masking of tinnitus through a cochlear implant. J. Am. Acad. Audiol., 11(6): 293–294. Yonehara, E., Mezzalira, R., Porto, P.R., Bianchini, W.A., Calonga, L., Curi, S.B. and Stoler, G. (2006) Can cochlear implants decrease tinnitus? Int. Tinnitus J., 12(2): 172–174.
CHAPTER 33
Cochlear implants and tinnitus David M. Baguley1,2, and Marcus D. Atlas2 1 Audiology, Addenbrooke’s Hospital, Hills Road, Cambridge, CB2 2QQ, UK Ear Sciences Centre, School of Surgery and Pathology, University of Western Australia, Perth, Australia
2
Abstract: The clinical observation that multichannel intra-cochlear cochlear implants have a suppressive effect on tinnitus in profoundly deaf patients is supported by many published studies. Whilst there are problems with that literature, specifically in the way that tinnitus outcomes are reported, the finding of tinnitus benefit is consistent. New developments in this area include the use of functional imaging to investigate tinnitus suppression by cochlear implant stimulation and consideration of a reported worsening effect on tinnitus of binaural implantation. Following work on hearing aids, it is suggested that optimization of the benefit of monaural cochlear implantation on tinnitus in a tinnitus-specific electrode configuration might include the use of a low knee point compression algorithm and disabling directional microphone function: these strategies are potentially also of benefit in patients whose tinnitus results in sleep disturbance. Opportunities for stimulation strategies for tinnitus suppression that bypass speech processing are also identified. Keywords: tinnitus; cochlear implant; auditory brainstem implant development of novel treatment strategies for tinnitus that utilize electrical stimulation of the cochlea (auditory nerve). The purpose of the present paper is to draw out the themes evident in published research in the area of cochlear implants and tinnitus, and then to consider developments in the field, specifically binaural cochlear implantation, modified electrode arrays and cochlear implantation for tinnitus in patients with unilateral severe profound sensorineural hearing loss (SNHL).
Introduction Clinicians working with cochlear implant patients have often reported that implant use can have a beneficial effect on tinnitus (Miyamoto and Bichey, 2003). Indeed, considerable published research supports this observation. Thus a recent review (Quaranta et al., 2004) identified 32 published papers (of which 12 were from the peerreview literature) that explicitly discussed the effect of cochlear implants on tinnitus. Whilst this body of literature has inconsistencies, it does provide useful material for a scientific consideration of tinnitus, and may potentially guide us towards optimizing the inhibitory effect of a cochlear implant on tinnitus. Further, it may facilitate the
The prevalence of tinnitus in cochlear implant candidates Many papers reporting series of patients undergoing cochlear implantation indicate the number reporting tinnitus, but unfortunately there are no
Corresponding author. Tel.: 01223 217594;
Fax: 01223 596101; E-mail: [email protected] DOI: 10.1016/S0079-6123(07)66033-6
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consistent definitions of that tinnitus. One might therefore expect some authors to be reporting patients with any tinnitus experience at all, and others patients with tinnitus that was severe enough to be troublesome. Further, such papers have not utilized the validated questionnaires that are in regular use in the tinnitus field, such as the Tinnitus Handicap Inventory (THI) (Newman et al., 1996) or the Tinnitus Questionnaire (Hallam, 1996), so one is unable to determine the extent to which tinnitus is bothersome in this population. Despite these concerns, there is relative consistency in the reported prevalence of tinnitus in patients about to undergo cochlear implantation. The existing data is summarized in Table 1, and indicates that in 18 research papers reporting a total of 1104 cochlear implant candidates, a range of prevalence data from 67 to 100% with a mean of 80% is demonstrated. In general terms therefore one can observe that one in five of the patient population who have acquired severe to profound hearing loss or deafness either have tinnitus that is only mildly troublesome, or no tinnitus at all. In this analysis papers have been considered that were published from 1990 to 2006. It should be
Table 1. Prevalence of tinnitus in cochlear implant candidates Author
Tinnitus prevalence (%)
Tyler and Kelsey (1990) McKerrow et al. (1991) Bredberg et al. (1992) Souliere et al. (1992) Gibson (1992) Tyler (1994) Kou et al. (1994) Hazell et al. (1995) Ito (1997) Miyamoto et al. (1997) Aschendorff et al. (1998) Demajumdar et al. (1999) Greimel et al. (2002) McKinney et al. (2002) Mo et al. (2002)
42/52 (81) 6 (100) 18/21 (86) 28/33 (85) 42/52 (85) 30/41 (73) 14/23 (70) 202/256 (79) 54/60 (90) 48/64 (75) 32/47 (68) 80/99 (80) 26/39 (67) 46/56 (82) 59/74 (80); ‘troublesome’ in 29 (35) 59/91 (65) 44/61 (72) 21/29 (72)
De Coninck et al. (2006) Kompis et al. (2006) Yonehara et al. (2006)
noted that candidacy criteria for cochlear implantation are changing, and becoming less constraining. In particular, patients with severe SNHL became considered as candidates during this time period, rather than only those with a profound hearing loss only being considered initially. Candidates with severe acquired SHNL may have differences in prevalence and severity of tinnitus than the traditional cohort: robust published data is not yet available in this regard.
Effect of surgery The insertion of an intra-cochlear implant electrode is potentially traumatic to any remaining functional cochlear structures (Adunka and Kiefer, 2006), and is believed to involve both necrotic and apoptotic mechanisms of cell death (Eshraghi and Van de Water, 2006) and such electrode insertion may influence tinnitus. Intriguingly however, in the small number of papers which consider this issue there are indications that for some patients there may be an improvement in tinnitus associated with electrode insertion (Gibson, 1992; Kim et al., 1995; Greimel et al., 2002), though the positive expectations of the patient regarding the implant may be a factor in this regard. There are also reports of small numbers of patients in whom electrode insertion exacerbates tinnitus (>10%) (Gibson, 1992) or precipitates it being heard for the first time (>4%) (McKerrow et al., 1991; Tyler, 1994; Miyamoto et al., 1997). Changes in tinnitus pitch and timbre have also been reported (Souliere et al., 1992).
Effect of use of monaural intra-cochlear devices Studies that have reported the effect on tinnitus of the use of monaural multichannel cochlear implants are summarized in Table 2. Whilst there are marked inconsistencies in the way that tinnitus outcomes are reported, it can be seen that for the overwhelming proportion of patients, cochlear implant use has a very significantly beneficial effect on tinnitus. The possibility that this is not only an auditory phenomenon but also linked with
349 Table 2. The influence of multichannel cochlear implants upon tinnitus Author
Cases
Type of implant
Tinnitus effect ipsilateral
Mixed (single and multichannel)
34 (81%) improved 7 (17%) same 1 (2%) worse 5 (83%) abolished 1 (17%) same 20 (77%) improved 25 (61%) better 16 (39%) same 25 (83%) improved 5 (17%) same 73/127 (57%) better 43/127 (44%) same 11/127 (9%) worse Group data indicates statistically significant decrease in loudness and annoyance 12 (86%) partial or complete elimination of tinnitus when CI on 5 (36%) complete elimination 6 (26% of total series) developed tinnitus as a result of implant surgery 10 (77%) better 3 (23%) same 40 (74%) very effective 10 (19%) effective 4 (7%) unchanged 22 (46%) better 24 (50%) same 2 (4%) worse 22 (69%) better 10 (31%) no change 62 (78%) abolished 17 (45%) abolished 19 (50%) reduced 3 (5%) unchanged 15.4% abolished 26.7% decreased 50% unchanged 32 (54%) better 21 (36%) no change 5 (8%) worse 1 (2%) abolished 11 (55%) complete inhibition 5 (25%) significant attenuation 4 (20%) no change 29% abolished 30% reduced loudness 36 (72%) improved 2 (5%) unchanged 6 (13%) worsened 2 of 15 patients (15%) who do not have preoperative tinnitus developed it in the first 6 months of device use 7 (33%) total suppression 8 (37%) partial suppression
Tyler and Kelsey (1990)
42
McKerrow et al. (1991)
6
UCSF/Storz 4 channels
Souliere et al. (1992) Gibson (1992)
28 41
Multichannel (Nucleus) Multichannel (Nucleus)
Tyler (1994)
30
Multichannel (Ineraid and Nucleus)
Hazell et al. (1995)
127
Mixed
Bredberg et al. (1992)
18
Mixed
Kou et al. (1994)
14
Nucleus 22 channel
Kim et al. (1995)
13
Multichannel (Nucleus)
Ito (1997)
54
Multichannel (Nucleus)
Miyamoto et al. (1997)
48
Multichannel 55 (Nucleus and Clarion) Single channel 9
Aschendorff et al. (1998)
32
Multichannel (Nucleus)
Demajumdar et al. (1999) Ruckenstein et al. (2001)
80 38
Multichannel (Nucleus) Multichannel (Nucleus and Clarion)
Greimel et al. (2002)
26
Not stated
Mo et al. (2002)
59
Multichannel intracochlear
Daneshi et al. (2005)
20
Multichannel
De Coninck et al. (2006)
91
Multichannel (Nucleus and Hires, Laura)
Kompis et al. (2006)
44
Not stated
Yonehara et al. (2006)
21
Nucleus 24K
350 Table 3. The influence of multichannel cochlear implants upon tinnitus in the contralateral ear Authors
Contralateral improvement
McKerrow et al. (1991) Souliere et al. (1992) Hazell et al. (1995) Kim et al. (1995) Fukuda and Mangabeira Albernaz (1998) Demajumdar et al. (1999)
67% 42% 52% better 71% 20% suppressed 20% decreased Tinnitus abolished in 14/70 (20%) 86% ‘‘totally suppressed or decreased’’
Yonehara et al. (2006)
neurophysiological model of tinnitus (Jastreboff, 1990), and the benefit from the use of Tinnitus Retraining Therapy (Jastreboff and Hazell, 1993), it is a reminder that a particular model may not cover all aspects of the functions of a complex system such as the auditory nervous system and that model predictions may not be supported exactly by experimental or empirical evidence. This also applies to other models (Baguley, 2006) such as the model of psychological aspects of tinnitus described by Hallam et al. (1984).
Optimization increased quality of life has been noted (McKinney et al., 2002, Mo et al., 2002). Several trends have been observed. The first (Quaranta et al., 2004) is that intra-cochlear multichannel devices (cochlear implants appear to have a more positive effect on tinnitus than the initially available extracochlear single channel devices, which were also less effective in providing auditory abilities (House, 1976; Berliner et al., 1987). Second, it appears that the use of a monaural cochlear implant may improve tinnitus in the contralateral ear (Quaranta et al., 2004). Data summarized in Table 3 indicate that for many patients, utilizing a cochlear implant in one ear can markedly reduce the perceived intensity of tinnitus in the contralateral ear. It has been suggested that this is due to masking (Battmer et al., 1989) or due to plastic reorganization of the auditory system, both of the ipsilateral and contralateral pathways, following cochlear implant use (Quaranta et al., 2004). Additionally, there is experimental evidence of the influence of contralateral auditory stimulation on neural activity evoked by sound in the ipsilateral pathways (Davis, 2005); this has been demonstrated to be both inhibitory (Ingham et al., 2006) and excitatory (Sumner et al., 2005). The finding of contralateral inhibition of tinnitus disagrees with the prediction of Jastreboff (2000) that in a patient with tinnitus, asymmetric or unilateral sound stimulation should exacerbate tinnitus contralateral to that of stimulation. While it does not affect other aspects of Jastreboff’s
It should be noted that cochlear implant stimulation strategies are designed to optimize speech discrimination, but they may not be optimal for tinnitus inhibition (Andersson et al., 2005). There has been little preliminary work in this area. A study of two individuals with tinnitus who had cochlear implants by Dauman and Tyler (1993) attempted to identify the optimal stimulation rate and electrode location that was most effective in suppression of tinnitus. Rubinstein et al. (2003) studied the effect of electrical stimulation with 5000 pps pulse trains via cochlear implant in 3 individuals and via a transtympanic electrode in 11 individuals, and found that ‘‘between a third and a half of them achieve clinically significant tinnitus suppression without a sustained percept’’. Vernon (2000) reported that masking with noise (6–14 kHz) via a Nucleus 22 cochlear implant was beneficial to an individual with bilateral tinnitus, leading to some residual inhibition lasting 2–3 min and some contralateral suppression. A preliminary report of the use of a commercialized extracochlear device delivering electrical stimulation to the oval window showed beneficial effect on tinnitus (Frachet et al., 2006). This remains an interesting area. Aspects of programming of a hearing aid for optimal suppression of tinnitus benefit may have some relevance for cochlear implant programming (see Chapter 32). Searchfield (2005) suggests that low compression knee points should be used when programming hearing aids for tinnitus relief and directional microphone technology should be
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disabled. Both of these changes will increase the amount of ambient and environmental sound that is delivered to the ear by the hearing aid. These tactics are variously feasible in current cochlear implant devices. If a patient has sleep disturbance and troublesome tinnitus (see Chapter 21), one might consider programming a cochlear implant device for nighttime use. There are two possibilities: first one might utilize a program that facilitates night-time use of an environmental sound generator, with sounds such as wind, rain, or the ocean — devices that have been shown effective in tinnitus therapy in individuals with hearing (Andersson et al., 2005; Handscomb, 2006). Second, one might consider an implant electrode configuration that gives barely suprathreshold stimulation through the night to reduce the awareness of tinnitus. As with hearing aids, optimizing a cochlear implant for tinnitus may involve programming that reduces speech discrimination abilities. The tinnitus program should therefore be addition to the program that is in general use of the cochlear implant (speech communication). There are two areas of interest where the existing literature is deficient. The first is consideration of the time course of tinnitus inhibition associated with cochlear implant use, about which there is little or no mention in the literature. This is potentially of some interest, as it may shed light on the mechanism by which tinnitus benefit is achieved. If the benefit is immediate one might consider that masking of the tinnitus by the new auditory information is occurring. If, however, the tinnitus suppression occurs over time, then some process of plastic reorganization of the auditory system following implant use can be inferred. These mechanisms are not mutually exclusive, and a longitudinal study would not resolve this completely, but might shed some light on this matter. The second area is that of children. The existing literature relates to adults, and there is minimal information regarding children with cochlear implants and tinnitus. This is anomalous, as hearing impaired children are known to have prevalent and occasionally severe tinnitus (see Baguley and McFerran, 2002 for review), and the response of
that tinnitus to cochlear implantation would be of some interest, both clinically and scientifically. New developments Binaural cochlear implants In a study by Summerfield et al. (2006) of selfreported benefits from successive cochlear implantation in post-lingually deafened adults, receipt of a second implant led to significant improvements in self-reported abilities in spatial hearing, quality of hearing and in speech perception, but, counterintuitively, to non-significant changes in quality of life. The essential aim of the study was to determine the incremental benefit (or otherwise) of a second implant. The study had 24 adult participants who were implanted with Nucleus CI24 devices. The participants were randomized either to receive a second implant immediately or to wait 12 months; this latter group acting as a control for emerging benefits of the second device. Multivariate analysis indicated that any improvement in quality of life associated with improved auditory abilities was offset by negative changes associated with worsening of their tinnitus. Of 16 patients with pre-operative tinnitus, 7 reported a worsening (44%), and of 8 patients who did not report tinnitus pre-operatively, 4 (50%) reported that the second implant had induced tinnitus. While the incidences of tinnitus are higher than those generally reported for unilateral implantation (see Table 2) they are not statistically significantly different from normal (Summerfield et al., 2006). Worsened tinnitus following sequential binaural implantation may therefore be sufficient to offset other benefits following surgery. Functional imaging and cochlear implants Mirz et al. (2002) used positron emission tomography (PET) to demonstrate the suppressive effect of a cochlear implant in a patient with distressing tinnitus. The use of the cochlear implants not only reduced signs of tinnitus-related activity in primary auditory and associate cortices, but also in areas of the CNS associated with emotion
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(limbic system) and attention (dorsolateral prefrontal cortices). PET in three patients (Osaki et al., 2005) in whom there was a marked residual inhibitory effect of cochlear implant use on tinnitus, showed that the right anterior middle and superior temporal gyri (Brodmann areas 21 and 38) were activated during residual inhibition after device use, whereas the right cerebellum was activated during tinnitus perception in the tinnitus patients. Such residual inhibition of tinnitus with cochlear implant use is common (Kim et al., 1995), but may be fleeting (Souliere et al., 1992). The authors concluded that tinnitus, and the residual inhibition of the tinnitus, are associated with central processes of auditory higher order processing, memory and attention. This hypothesis requires significant further research before conclusions can be drawn.
Unilateral SNHL and tinnitus Idiopathic unilateral sudden SNHL has an incidence of 2–20/100,000 adults per year (Byl, 1984), leading to estimates of 2835–9540 cases per year in the UK alone (Baguley et al., 2006). The hearing loss does not recover in more than 60% of cases in spite of therapy, mainly because the cause and pathogenesis of sudden deafness is unknown (Merchant et al., 2005). When hearing loss remains severe, tinnitus in the same ear may be disabling as shown by Chiossoine-Kerdel et al. (2000) using the THI (Newman et al., 1996). The same authors also demonstrated a significant hearing handicap in the majority (86%) of these unilaterally affected patients when assessed with the Hearing Handicap Inventory for Adults (Newman et al., 1990). Therefore, tinnitus consecutive to sudden deafness with poor recovery remains a therapeutic challenge (Andersson et al., 2005). Contralateral routing of signal (CROS) and bone-anchored hearing aids (BAHA) can be utilized in auditory rehabilitation, with varying degrees of success (Baguley et al., 2006), but little or nothing can be offered for relief of the tinnitus. A cochlear implant on the affected side may benefit and not only reduce the hearing handicap
but it may also provide relief for the tinnitus. The application of a cochlear implant to such individuals has so far only been reported in a conference report where Van de Heyning et al. (2006) described a series of 10 patients with a unilateral profound SNHL, associated with ‘‘incapacitating and refractive tinnitus’’ and with normal hearing in the contralateral ear. These individuals were implanted with the Medel Combi 40+ device. On individuals whose tinnitus could be reduced by at least 50% by electrical promontory stimulation were included in the study. Statistically significant improvements in measures of tinnitus loudness (visual analog scale) and impact (Tinnitus Questionnaire, Hallam, 1996) were achieved in all these individuals and all were reported to have used the device all their waking hours for the 12-month duration of the study. In a further report from the same group, Vermeire et al. (2006) describe 18 similar patients (probably including those from the initial report). An additional inclusion criteria described is a >50% inhibition of the tinnitus by electrical promontory stimulation. Programming strategies and outcome measures are not described, but the authors stated ‘‘there was no conflict between the hearing with the CI and the hearing in the opposite ear’’. It has been reported that it is possible to integrate regular hearing with cochlear implant stimulation (Dunn et al., 2005) though such auditory fusion may not be possible in all individuals. Optimizing the device for tinnitus inhibition might however involve non-speech related stimulation, and an approach such as the pulse train stimulation trialed by Rubinstein et al. (2003) becomes an option. The development of modified electrode arrays, which aim to preserve lowfrequency acoustic hearing and allow mid, and high-frequency electrical stimulation (Gantz and Turner, 2004; Gantz et al., 2006; James et al., 2006; Briggs et al., 2006, for example) may offer some benefit for such patients, many of whom experience troublesome tinnitus. Soussi and Otto (1994) studied 10 patients who had received an auditory brainstem implant (ABI) following removal of a vestibular schwannoma in patients with neurofibromatosis type 2. Of these, seven used their implant daily, and six of these
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‘‘reported noticeable tinnitus reduction’’ — this represents 86% of the daily user group. This finding is of some potential interest, as the dorsal cochlear nucleus (DCN) (Kuroki and Møller, 1995; Kaltenbach, 2006; Shepherd and McCreery, 2006) has been implicated in tinnitus perception. The electrode array of the ABI is inserted into the lateral recess of the fourth ventricle and placed over the surface of the ventral and dorsal cochlear nuclei (Kuroki and Møller, 1995; Fayad et al, 2006; Shepherd and McCreery, 2006). Progress toward a midbrain implant is also evident (Lenarz et al., 2006; Colletti et al., 2007) and provides further opportunity for the investigation of the possibility of using electrical stimulation of the central auditory system in controlling tinnitus. Conclusions This paper has reviewed current observational evidence regarding the effects of cochlear implants on tinnitus. The current literature supports the clinical observation that cochlear implants have a marked suppressive effect on tinnitus in most cochlear implant users. The situation may be different for binaural cochlear implants where auditory benefits of a second implant may be offset by an exacerbation of tinnitus in some patients. Cochlear and brainstem implants can also seems to provide reduction of tinnitus but the experience of such implants is much smaller than that of cochlear implants. Acknowledgment This paper was written while David Baguley was a Raine Visiting Professor at the Ear Sciences Institute, University of Western Australia. The support of the Raine Foundation, of Phonak Pty, of the British Tinnitus Association and of Deafness Research UK is gratefully acknowledged. References Adunka, O. and Kiefer, J. (2006) Impact of electrode insertion depth on intracochlear trauma. Audiol. Neurootol., 11(Suppl. 1): 57–62.
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Soussi, T. and Otto, S.R. (1994) Effects of electrical brainstem stimulation on tinnitus. Acta Otolaryngol., 114(2): 135–140. Summerfield, A.Q., Barton, G.R., Toner, J., McAnallen, C., Proops, D., Harries, C., Cooper, H., Court, I., Gray, R., Osborne, J., Doran, M., Ramsden, R., Mawman, D., O’Driscoll, M., Graham, J., Aleskey, W., Meerton, L., Verschurre, C., Ashcroft, P. and Pringle, M. (2006) Self-reported benefits from successive bilateral cochlear implantation in post-lingually deafened adults: randomised controlled trial. Int. J. Audiol., 45(Suppl. 1): S99–S107. Sumner, C.J., Tucci, D.L. and Shore, S.E. (2005) Responses of ventral cochlear nucleus neurons to contralateral sound after conductive hearing loss. J. Neurophysiol., 94(6): 4234–4243. Tyler, R.S. (1994) Advantages and disadvantages expected and reported by cochlear implant patients. Am. J. Otol., 15: 523–531. Tyler, R.S. and Kelsey, D. (1990) Advantages and disadvantages reported by some of the better cochlear implant patients. Am. J. Otol., 11(4): 282–289. Van de Heyning, P., Vermiere, K. and De Ridder D. (2006) Tinnitus treatment with CI in unilateral deafness. In: Baumgartner W.D. (Ed.), 9th International Conference on Cochlear Implants and Related Sciences. Wein Med. Wochenschr. 156(Suppl. 118), p. 58. Vermeire, K., Schleich, P. and Ven de Heyning, P. (2006) Hearing capabilities after CI in unilateral sensorineural deafness and tinnitus. In: Baumgartner W.D. (Ed.), 9th International Conference on Cochlear Implants and Related Sciences. Wein Med. Wochenschr. 156(Suppl. 118), p. 59. Vernon, J.A. (2000) Masking of tinnitus through a cochlear implant. J. Am. Acad. Audiol., 11(6): 293–294. Yonehara, E., Mezzalira, R., Porto, P.R., Bianchini, W.A., Calonga, L., Curi, S.B. and Stoler, G. (2006) Can cochlear implants decrease tinnitus? Int. Tinnitus J., 12(2): 172–174.