J Am Acad Audiol 11 : 309-315 (2000)

Cochlear Implantation of Auditory Neuropathy Patricia G. Trautwein* Yvonne S. Sininger* Ralph Nelson*

Abstract

Auditory neuropathy (AN) is a hearing disorder that presents with a grossly abnormal or

absent neural response as measured by evoked potentials in the presence of normal outer

hair cell function evidenced by present otoacoustic emissions or cochlear microphonics .

Rehabilitation for patients with AN is challenging due to abnormal temporal encoding at the

auditory nerve leading to severely impaired speech perception . Although patients with AN

may demonstrate improvement in thresholds with amplification, temporal encoding dys-

function, and consequently speech perception degradation, is not alleviated by amplification .

Another issue is the heterogeneity of the AN population in terms of audiologic and neuro-

logic findings, in addition to uncertain etiology and pathophysiology. For children with prelingual

onset of AN, development of auditory and oral communication skills is particularly compro-

mised . All children with hearing loss in the severe-to-profound range who do not benefit from

conventional amplification can be considered candidates for a cochlear implant (CI) . This

paper presents a case study of a child with AN who received a CI . Whereas no synchronous

neural response auditory brainstem response could be elicited to acoustic stimuli, an elec-

trically evoked auditory nerve action potential was evident following implantation, suggesting

restoration to some degree of neural synchrony. Significant improvement in speech percep-

tion was found post-CI . Recommendation to implant all patients with AN would be premature,

but these findings suggest that electrical stimulation in some cases of auditory neuropathy

can be a viable option .

Key Words: Auditory neuropathy, cochlear implant, electrically evoked compound action potential, speech perception

Abbreviations : AN = auditory neuropathy, CI = cochlear implant, CM = cochlear microphonic, DSL = desired sensation level, EAP = electrically evoked compound action potential, ESP =

Early Speech Perception test, IHC = inner hair cells, LTASS = long-term average speech

spectrum, NRT = neural response telemetry, OAE = otoacoustic emission, TAC = Test of Auditory Comprehension, TEOAE = transient evoked otoacoustic emission

A

uditory neuropathy (AN) is a term used

to describe a recently recognized type of

hearing disorder (Berlin et al, 1993 ; Sininger et al, 1995 ; Starr et al, 1996; Deltenre

et al, 1997 ; Doyle et al, 1998 ; Rance et al, 1999) . Symptoms of AN include (1) hearing loss, usu-

ally bilateral of any degree ; (2) normal outer

hair cell function evidenced by present otoa-

coustic emissions (OAEs) and/or cochlear micro-

phonic (CM) ; (3) abnormal evoked potentials

*Department of Children's Auditory Research and Evaluation . House Ear Institute, Los Angeles, California

Reprint requests : Patricia G . Trautwein, House Ear Institute CARE Center . 2100 West Third St ., Los Angeles, CA 90057

beginning with wave I of the auditory brain-

stem response (ABR); and (4) poor speech per-

ception . The site of lesion for patients with AN

remains unknown. The possibilities include the

inner hair cells (IHC), synaptic junction between

the IHC and auditory nerve, and the auditory

nerve itself. Rehabilitation for patients with AN is chal-

lenging due to the heterogeneity of the popu-

lation in terms of audiologic and neurologic findings, in addition to the uncertain etiology and pathophysiology. One pervasive observation with AN is poor temporal encoding (Starr et al, 1996 ; Zeng et al, in press) and, consequently, degraded speech perception ranging from lim-ited to no open-set discrimination . Since

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Journal of the American Academy of Audiology/Volume 11, Number 6, June 2000

conventional amplification cannot address tem-poral function, trials with hearing aids, FM systems, or tactile aids have demonstrated only limited success (Rance et al, 1999). Data from our laboratory indicate that approximately one-third of patients with AN have audiomet-ric thresholds in the severe-to-profound range and, therefore, could be considered candidates for cochlear implantation .

Cochlear implantation is routinely performed in children and adults with hearing losses in which the cochlea is the primary site of dys-function and the status of the auditory nerve remains elusive. However, for patients with AN, the efficacy of implantation could be questioned because of the suspected disease of the auditory nerve, which could be axonal degeneration, demyelination, or both (Starr et al, 1996). If the nerve is the site of dysfunction, electrical stim-ulation provided by the cochlear implant (CI) may promote neural survival (Araki et al, 1998 ; Mitchell et al, 1997) and restore temporal encod-ing (Shannon, 1993). Even more promising, Zhou et al (1995a, b) report that electrical stimulation produces synchronous ABRs in the presence of peripheral auditory nerve demyelination. This suggests that the stimulation provided by a CI may, in fact, provide reliable, consistent neural firing even in the presence of a diseased nerve. If the site of dysfunction is cochlear, that is, IHC or the synapse (Harrison, 1998), a CI may be a viable compensation as it is in patients not diagnosed with AN who are routinely implanted as treatment for cochlear hearing losses .

Although the potential benefits of cochlear implantation for patients with auditory neu-ropathy are exciting, drawbacks do exist. The standard risk of the surgical procedure and anesthesia obviously remain . However, these risks are no greater for children with auditory neuropathy than children with cochlear hearing loss routinely being implanted. Studies have suggested that the insertion of the electrode array may damage cochlear structures and destroy residual hearing (O'Leary et al, 1991 ; Gstoettner et al, 1997). Therefore, the implan-tation procedure may damage structures in the cochlea, that is, the outer hair cells, which are functioning normally.

The following case presentation details the cochlear implantation of a child with AN. The case study serves as one example of the poten-tial benefits a child with AN may experience from cochlear implantation .

CASE REPORT

A n 18-month-old boy was referred to the House Ear Institute CARE Center for the dispensing of hearing aids following a no-response ABR at another local center. The parents reported a healthy, full-term pregnancy. Developmental milestones with the exception of speech were reached at age-appropriate times. The patient is an only child, and a family history of hearing loss was denied . Behavioral audiologic assess-ment revealed audiometric thresholds in the severe-to-profound range (Fig . 1) . Immittance

Right Ear

250 500 1000 2000 4000 8000 Frequency (Hz)

Left Ear

d 50 d

60

F ca 70 d x

80 m a

90

N z a

40

100

110

120 250 500 1000 2000 4000 8000

Frequency (Hz)

Figure l Audiologic assessment demonstrated thresholds in the severe-to-profound range for both ears . Aided thresh-olds with conventional amplification for both ears represented as "A." 310

Cochlear Implantation of Auditory Neuropathy7l7rautwein et al

Baseline corrected Probe Current Level Baseline corrected Rate

40

60

80

Recording Parameters : Stimulating Electrode 10 Recording Electrode 12 Averages = 100 Recording Delay = 60 psec

Probe : Current Level = variable Pulse Width = 25 psec/phase Rate = 80 Hz

Recording Parameters : Stimulating Electrode 10 Recording Electrode 12 Averages = 100 Recording Delay = 60 psec

Probe: Current Level = Fixed 210 units Pulse Width = 25 psec/phase Rate = variable

Masker: Current Level = fixed (210 units) Pulse Width = 25 psec/phase Advance = 500 psec

0 0.5 1 1 .5 2 2.5 Time in msec

Figure 6 EAP waveforms recorded with NRT testing at variable current levels (in current level units) .

compared for the child with AN and a set of 10 children with cochlear hearing loss (Figs. 8, 9, 10) . The children were selected from the patient database at the House Ear Institute CARE Cen-ter. The children with cochlear hearing loss were similar to the AN patient in that all were implanted between the ages of 2 .8 and 4.0 years with the Nucleus 22 or C124M device and use the SPEAK processing strategy. Speech perception testing data at 1 year postimplantation for the child with AN were compared to the speech per-ception scores of the 10 children with cochlear hearing loss .

Figure 8 plots the preimplantation and 1 year postimplantation score for each child on the Ling Six Sounds Test (Ling, 1978). This test assesses a patient's ability to either detect or dis-criminate the phonemes /a, u, i, s, sh, m/ when presented auditory only (i .e ., no visual cues). Each phoneme is presented five times in a ran-dom order for a maximum score of 30 . Prior to receiving the CI, the child with AN actually had better detection of the sounds than the children with cochlear hearing loss . However, the child with AN could only detect these sounds and demonstrated no discrimination of the sounds without the visual cue of lip reading. One-year postimplantation, the child with AN could

Masker: Current Level = Fixed 210 units Pulse Width = 25 psec/phase Rate = 500 psec

0 0.5 1 1 .5 2 2.5 Time in msec

Figure 7 EAP waveforms recorded at variable stimulus presentation rates (in Hz).

discriminate the sounds with accuracy as did most of the children with cochlear hearing loss .

The Early Speech Perception (ESP) test (Moog and Geers,1990) is designed to be used with children with limited vocabulary and language skills in order to assess speech perception ability. The test consists of three sets of test stimuli and each is administered as a closed set. The results

(3 Pre-cl N Cochlear Hearing Loss ® Auditory Neuropathy

30

25 d 8 20

15 J

10

S1 S2 S3 S4 S5 S6 S7 S8 S9 S10 S11

Subjects

Figure S Ling Six Sounds Test results pre-CI and 1-year postimplantation for the child with AN and 10 chil-dren with cochlear hearing loss . Ling Six Sounds Test = phonemes /a, u, i, s, sh, m/ presented five times live

voice and scored #correct/30 for identification or detection.

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Journal of the American Academy of Audiology/Volume 11, Number 6, June 2000

" Cochlear Hearing Loss ® Auditory Neuropathy

Subjects

Figure 9 ESP test results for the child with AN and 10 children with cochlear hearing loss 1-year post-Cl. Prior to implantation, all children were in category 1. ESP = closed-set task with four-category scoring; category 1: no pattern perception ; category 2: pattern perception ; cat-egory 3: some word identification ; category 4: consistent word identification .

of this test allow the placement of children into four speech perception categories : 1= no pattern perception, 2 = pattern perception, 3 = some word identification, and 4 = consistent word identifi-cation. Figure 9 plots the ESP category placement for each child 1-year post-cochlear implantation . Prior to receiving the CI, all children were in category 1: no pattern perception. After 1 year of CI use, the child with AN is in category 4: con-sistent word identification . Some children with cochlear loss have also reached category 4, whereas others remained below.

Test of Auditory Comprehension (TAC) (Trammell and Owens, 1977) is a comprehensive auditory discrimination test administered in a taped, closed-set format . There are 10 subtests arranged in a hierarchical order evaluating a

6

5

W 4 N N a 3 N °' 2 a

0 Cochlear Hearing Loss ® Auditory Neuropathy

S1 S2 S3 S4 S5 S6 S7 S8 S9 S10 S11 Subjects

Figure 10 TAC results for the child with AN and 10 chil-dren with cochlear hearing loss . This test was not admin-istered to any of the children prior to implantation . TAC: closed-set task of 10 subtests increasing in degree of dif-ficulty. Subtest 1: linguistic/nonlinguistic ; 2: linguis-tic/human nonlinguistic/environmental ; 3: stereotypic messages; 4: single element core noun vocabulary ; 5: recall two critical elements ; 6: recall four critical elements ; 7: sequence three events; 8: recall five details; 9: sequence three events with competing messages ; 10 : recall five details with competing messages .

range of abilities including suprasegmental dis-crimination, memory-sequencing abilities for up to four critical elements, auditory compre-hension, and auditory figure-ground abilities. This test was not administered prior to implan-tation . Figure 10 plots the TAC subtest score for the child with AN against the children with cochlear hearing loss at 1-year postimplantation. The child with AN passed the third subtest, which measures a child's ability to discriminate stereotypic messages . The child with AN scored within the wide range of performance (unable to pass subtest 1 to passing subtest 5) of children with cochlear loss .

As one can see, the child with AN made sig-nificant improvement in speech perception after cochlear implantation. The child's scores are within the wide range of performance noted for children with cochlear hearing loss who are routinely rec-ommended for CI . The child continues to attend an intensive auditory-oral educational program. Subjectively, his therapists report improvement in daily listening skills and an expansion in both receptive and expressive vocabulary. The parents are very pleased with his progress .

DISCUSSION

T his case illustrates one example in which electrical stimulation provided by a CI in a child with AN produced electrically evoked neural responses and significant improvement in speech perception ability. Although the results obtained in this case appear promising, the deci-sion to implant should still be approached cau-tiously. The diagnosis of AN should not be an immediate referral for a CI . Some infants diag-nosed with AN, who initially presented behav-iorally as deaf, show improved or fluctuating auditory responses with increasing age (Berlin et al, 1999). Although few, other patients have experienced benefit with conventional amplifi-cation (Rance et al, 1999). Since no clear rela-tionship between audiometric threshold and performance with conventional amplification has been established, a trial period with ampli-fication is the only way to determine an indi-vidual's benefit. Studying the electrically evoked neural responses and their relation to speech per-ception in patients with AN may offer insight into the pathophysiology of this disease. Continued research in the areas of diagnosis, etiology, and pathophysiology ofAN is needed prior to address-ing the possibility of implanting patients with better audiometric thresholds who obtain no benefit from amplification.

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Acknowledgment. This paper was presented at the American Academy of Audiology 1999 Convention in Miami, FL, May 3-5,1999 .

Miyamoto RT, Kirk KI, Svirsky MA, Sehgal ST. (1999) . Communication skills in pediatric cochlear implant recip-ients. Acta Otolaryngol (Stockh) 119:219-224 .

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