The Laryngoscope
C 2014 The American Laryngological,
V
Rhinological and Otological Society, Inc.
Evidence for a Right Cochlear Implant Advantage in Simultaneous
Bilateral Cochlear Implantation
Yael Henkin, PhD; Riki Taitelbaum Swead, PhD; Daphne Ari-Even Roth, PhD; Liat Kishon-Rabin, PhD;
Yisgav Shapira, MD; Lela Migirov, MD; Minka Hildesheimer, PhD; Ricky Kaplan-Neeman, PhD
Objectives/Hypothesis: To compare speech perception performance with right versus left cochlear implants (CIs) in
children with bilateral CIs implanted simultaneously.
Study Design: Prospective case series of patients undergoing simultaneous bilateral cochlear implantation.
Methods: Speech perception performance was tested in 10, right-handed children who received bilateral CIs simultaneously between 11 and 36 months (mean, 21 months), had at least 18 months of bilateral CI use, and were 5.3 years of age
during testing. All children exhibited bilateral symmetrical severe-to-profound hearing loss prior to implantation and did not
benefit from hearing aids. Speech perception performance was evaluated with the right CI and the left CI by means of an
open-set monosyllabic word test in quiet presented at 45 dB HL in a sound field.
Results: All children exhibited higher performance with the right CI compared to the left CI. Group mean performance
with the right CI was 66.5% compared to 52% with the left CI (P 5.002), yielding a 14.5% difference. With increasing duration of bilateral CI use and age at evaluation, the right–left difference increased (r 5 0.72, P 5.019 and r 5 0.74, P 5.014,
respectively).
Conclusions: Current preliminary data indicate that children with bilateral CIs implanted simultaneously exhibit a significant right ear advantage for speech. Similarly to reports on normal-hearing children, right ear preference for speech
increased with increasing age and auditory–linguistic experience. Thus, simultaneous bilateral cochlear implantation may lead
to normal development of auditory pathways and may be an important contributor to the superior auditory, language, and
communication skills reported in children with bilateral versus unilateral CIs.
Key Words: Cochlear implant, bilateral simultaneous cochlear implantation, right ear advantage, speech perception,
children.
Level of Evidence: 4.
Laryngoscope, 124:1937–1941, 2014
INTRODUCTION
Over two decades of experience have shown that
unilateral cochlear implants (CIs) substantially improve
sound and speech perception thereby promoting development of speech, language, and communication skills.1–3
Despite these benefits, unilaterally implanted children
are denied of the binaural advantages including summation, redundancy, squelch, and have limited access to
interaural time and level differences. In addition, maximal benefit from the head shadow effect is restricted.
From the Department of Communication Disorders (Y.H., D.A.-E.R.,
Sackler Faculy of Medicine, Tel Aviv University, Tel
Aviv; and the Hearing, Speech, and Language Center (Y.H., R.T.S.,
D.A.-E.R., M.H., R.K.-N.), and Department of Otolaryngology–Head and
Neck Surgery (Y.S., L.M.), Sheba Medical Center, Tel Hashomer, Ramat
Gan, Israel.
Editor’s Note: This Manuscript was accepted for publication
January 24, 2014.
This work was performed at the Department of Communication
Disorders, Sackler Faculy of Medicine, Tel Aviv University, and the
Hearing, Speech, and Language Center, Sheba Medical Center, Tel
Hashomer, Israel.
The authors have no funding, financial relationships, or conflicts
of interest to disclose.
Send correspondence to Yael Henkin, PhD, Department of Communication Disorders, Sheba Medical Center, Tel Hashomer, Ramat Gan,
Israel 52621. E-mail: henkin@post.tau.ac.il
L.K.-R., M.H., R.K.-N.),
DOI: 10.1002/lary.24635
Laryngoscope 124: August 2014
Consequently, they exhibit difficulties in speech understanding in noise4 and sound localization5,6 and may
show inferior expressive and receptive language skills7,8
compared to those of bilaterally implanted children and
normal-hearing peers.
In an attempt to diminish the negative effects of
unilateral auditory deprivation and provide deaf children with binaural advantages, there is an increasing
trend toward bilateral cochlear implantation. A recent
worldwide survey indicated that 70% of bilateral implantations occur in children, with the highest representation of the 3- to 10-year-old age group (33% of all
bilateral implantations), and children under 3 years
(26%).9 In most cases, bilateral implants are provided
sequentially, with variable periods between the first and
second implantation. Nonetheless, there is growing
agreement that “the infant or child with unambiguous
cochlear implant candidacy should receive bilateral cochlear implants simultaneously as soon as possible after
definitive diagnosis of deafness to permit optimal auditory development” (European Bilateral Pediatric Cochlear Implant Forum consensus statement).10
Although current guidelines have substantially
reduced the minimal age at implantation, congenitally
deaf children continue to experience various periods of
bilateral and unilateral auditory deprivation prior to
Henkin et al.: Right Ear Advantage and Bilateral CIs
1937
implantation, which may affect normal neurodevelopment and lead to reorganization of the central auditory
system.11,12 In the normal auditory system, numerous
functional imaging, electrophysiological, and behavioral
studies have shown that although the auditory cortex
receives sensory input from both ears, it is excited most
strongly by stimulation of the contralateral ear.13–17
When stimulated by speech, stronger contralateral activation is manifested in the “right ear advantage” phenomenon using dichotic listening tasks, and is ascribed
to stronger crossed auditory pathways from the right ear
ascending to the speech-dominant left hemisphere.18
This asymmetry has been exhibited through the lifespan, from 4-day-old neonates19,20 to adulthood,21–25 to
various speech stimuli (e.g., consonant–vowel syllables,
stop consonants, and words).26–28
Recently published data indicate that unilateral
cochlear implantation may alter the development of normal auditory pathways and result in cortical reorganization11,29; nevertheless, limited data exist regarding ear
advantage patterns in unilateral CI recipients. Based on
the well-substantiated right ear advantage for speech in
normal-hearing listeners, it was speculated that the right
ear should be the preferred ear for implantation30 in an
attempt to maximize speech perception performance. This
assertion has been tested in postlingually deafened adults
and in prelingually deafened children, all implanted unilaterally. Data suggest that postlingually deafened elderly
CI recipients implanted in the right ear outperformed
those implanted in the left ear in speech perception tests
in quiet (words) and in noise (sentences).31 Nonetheless,
the right CI advantage was not evident in young postlingually deafened adults, with right versus left CI showing
similar improvement on speech perception tests by 12
months of implant use.32 In prelingually deafened children, we reported data from a cohort of 71 children, 30
implanted in the right and 41 implanted in the left, indicating a slight yet significant right CI advantage that
was evident throughout a 3-year follow-up and was independent of age at implantation.33 These results are in
keeping with our earlier electrophysiological data showing differential brain activation patterns during speech
processing in children with right versus left CI.34 Based
on the recording of the P3 event-related potential known
to reflect discrimination and categorization of stimuli,
children implanted in the right ear exhibited bilateral
temporal and frontal lobe activation while processing consonant–vowel syllables, similarly to normal-hearing controls. In contrast, children implanted in the left ear
showed differential patterns characterized by enhanced
ipsilateral temporal lobe activation.
Following this line of investigation, we asked whether
a right CI advantage for speech is evident in children with
bilateral CI implanted simultaneously. The working premise was that children who experienced relatively short
duration bilateral auditory deprivation and received simultaneous bilateral cochlear implants thereafter, may exhibit
a right CI advantage for speech. For this purpose, we studied a group of children with bilateral CI who were
implanted simultaneously, had substantial duration of CI
use, and could fully cooperate in a speech perception test.
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1938
MATERIALS AND METHODS
Subjects
Among the 497 children who were implanted at Sheba Medical Center, Tel Hashomer, between 1991 and 2013, 147 (30%)
were implanted bilaterally. Of these, 48 received bilateral CIs
simultaneously between 2007 and 2013, with the majority
implanted between 2010 and 2013. Among the simultaneously
implanted children, 10 children who were old enough to cooperate
in speech perception testing and had at least 18 months of bilateral CI use participated in the study. They were implanted
between 11 and 36 months of age (mean, 21.2 months) and used
their CIs regularly for 18 to 75 months (mean, 44.2 months). Individual background information is presented in Table I. All children were diagnosed with bilateral severe-to-profound sensory
neural hearing loss based on auditory brainstem response measurements and behavioral testing, and were habilitated bilaterally
with high-power digital hearing aids shortly after diagnosis. They
showed limited benefit from hearing aids as detailed in Table I.
All were healthy, right-handed based on parental report, with
fully inserted electrodes, and without cochlear malformations
based on radiographic evaluation. All children were using oral
communication and mainstreamed in regular educational settings.
Seven children were congenitally deaf, whereas three children were deafened as a result of meningitis at 27, 33, and 20
months (Table I, subjects 1, 3, and 7, respectively). These three
children were implanted 3, 4, and 6 months postmeningitis,
respectively. Postoperative reports indicated complete cochlear
ossification in the right ear and partial ossification in the left
ear in patient 3, partial ossification in the basal turn especially
in the right ear in patient 1, and no ossification in patient 7.
The age at testing of all children ranged between 30 and
108 months (mean, 64.3 months). Seven children were
implanted with MedEl devices, two with Cochlear devices, and
one with Advanced Bionics devices. All electrodes were activated in all patients excluding three patients using MedEl
devices: patient 3, electrode 12 bilaterally; patient 1, electrode
12 (left); patient 10, electrode 12 (right) and 11 (left).
Test Measures
Speech perception was evaluated using the prerecorded
Hebrew version of the Arthur Boothroyd (AB)35 open-set monosyllabic, consonant–vowel–consonant word recognition test.
Based on clinical experience, the Hebrew AB test can be administered to young children. Two lists of AB words were presented
in each of the two listening conditions, right CI and left CI, in
random order. The words were presented at 45 dB HL in free
field via two loudspeakers located at 45 on the right and left,
at a distance of 1 m from the subject.
Statistical Methods
The nonparametric Wilcoxon signed rank test was used to
evaluate the difference in performance in the Hebrew AB test
between the right and left CIs, as it was unlikely to be normally
distributed. Furthermore, correlation between the right–left CI
difference in performance and 1) age at implantation, 2) age at
evaluation, and 3) duration of CI use, was evaluated by means
of Pearson correlation coefficients.
RESULTS
Aided thresholds, as measured by voice detection
levels and speech reception thresholds with the right
and left CIs, were comparable (P 5.25 and P 5.2, respectively) and are depicted in Figure 1.
Henkin et al.: Right Ear Advantage and Bilateral CIs
TABLE I.
Background Information of CI Recipients.
Preimplantation ABR
Thresholds to Clicks, 0.5, and
1 kHz Tone Bursts, dB nHL
Patient
Etiology of
Deafness
Aided VDL,
dB HL*
Right
Left
Right
Left
Age at
Implantation, mo
CI Devices
Duration of
CI Use, mo
Age at
Evaluation, mo
1
Meningitis
NR, NR, NR
NR, NR, NR
90
90
30
MedEl
75
105
2
3
Genetic
Meningitis
NR, 90, NR
NR, 80, NR
NR, NR,NR
NR, 80, NR
45
55
40
55
12
36
MedEl
MedEl
18
72
30
108
4
Unknown
NR, NR, NR
85, NR, NR
70
70
35
Cochlear
18
53
5
6
Genetic
Genetic
NR, NR, NR
NR, NR, NR
NR, NR, NR
NR, NR, NR
60
100
70
100
15
12
MedEl
Cochlear
48
18
63
30
7
Meningitis
NR, NR, NR
NR, NR, NR
75
55
26
MedEl
57
83
8
9
Connexin 26
Waardenburg
NR, NR, 100
NR, NR, NR
NR, NR, NR
NR, NR, NR
30
80
55
60
11
13
MedEl
Advanced Bionics
52
48
53
60
10
Genetic
NR, NR, NR
NR, NR, NR
90
90
22
MedEl
36
58
*Aided voice detection levels (VDL) in free field with hearing aids.
ABR 5 auditory brainstem response; CI 5 cochlear implant; NR 5 no response at maximum output.
Figure 2 shows individual performance in the AB
test with the right and left CIs and group mean data.
For all participants, performance with the right CI was
higher than with the left CI. Group mean performance
was significantly higher with the right CI (66.5%) compared with the left CI (52%) (P 5.002) yielding a 14.5%
difference.
Three children who were deafened as a result of
meningitis showed a larger right–left difference of 20%,
30%, and 20% (subjects 1, 3, and 7, respectively) compared to the seven prelingually deafened children who
showed a mean difference of 10.7% (range, 5%–20%).
Testing the right–left difference in the seven prelingually deafened children, yielded a significant right CI
advantage (P 5.016).
Fig. 1. Group mean aided voice detection levels (VDL) and speech
reception thresholds (SRT) with the right (Rt) and left (Lt) cochlear
implants.
Laryngoscope 124: August 2014
The right–left difference in performance was
strongly correlated with 1) age at evaluation (r 5 0.74,
P 5.014) and 2) duration of implant use (r 5 0.72,
P 5.019). These correlations are depicted in Figures 3
and 4 showing that with increasing age at evaluation
and duration of CI use, the right–left difference
increased. The correlation between the right–left difference and age at implantation was moderate yet did not
reach significance (r 5 0.54, P 5.1).
DISCUSSION
The current study provides first-time preliminary
evidence indicating a significant right CI advantage of
Fig. 2. Individual and group mean speech perception performance
with the right (Rt) and left (Lt) cochlear implants (CI).
Henkin et al.: Right Ear Advantage and Bilateral CIs
1939
Fig. 3. Right (Rt)–left (Lt) difference in performance as a function
of age at evaluation. Note that with increasing age at evaluation,
the right–left difference increases. CI 5 cochlear implant.
14.5% for speech in right-handed children with bilateral
CIs implanted simultaneously at a young age. It is plausible that for this small group of children, all exhibiting
a right CI advantage, simultaneous stimulation of auditory pathways resulted in the restoration of normal
asymmetry. Support for this notion is provided by recent
data collected by Gordon et al.11 showing that cortical
activity, manifested by the P1 potential to biphasic electrical pulses in children who were implanted simultaneously or sequentially with short interimplant delay
(<1.5 years), was similar to that of normal-hearing peers
and lateralized to the hemisphere contralateral to side of
stimulation. In contrast, sequentially implanted children
with long delay (>2 years) showed a different pattern
characterized by enhanced ipsilateral activation. Based
on this finding, the authors concluded that bilateral
auditory stimulation provided with limited delay can
protect the brain from irreversible reorganization found
in unilaterally implanted children or sequentially
implanted children with long interimplant delay. Data
regarding cortical activation patterns to speech stimuli
are required to further clarify lateralization patterns to
speech in CI recipients.
The perceptual asymmetry found in the present
study in CI recipients is not evident in normal-hearing
listeners while performing monaural speech recognition
tasks in quiet due to a ceiling effect. Typically, the right
ear advantage is exhibited in normal-hearing listeners
by means of dichotic listening tasks.25 Increased task
difficulty and stimuli uncertainty, however, were also
found to demonstrate this phenomenon.36 For example,
competing monaural stimulation of words resulted in a
substantial right ear advantage.37 For CI recipients,
monaural speech recognition tasks with low linguistic
redundancy (i.e., monosyllabic words), even in quiet, are
challenging and may therefore suffice to demonstrate
the CI side advantage. Support for this notion is the
remarkably similar magnitude of the right CI advantage
found in children with bilateral CI implanted simultaneously in the current study (14.5%) and that found in
Laryngoscope 124: August 2014
1940
unilaterally implanted recipients with right versus left
CI while performing a monosyllabic word test in quiet
(children: 13.7%33, elderly adults: approximately 13%31).
It should further be noted that the right CI advantage
was persistent over 2 and 3 years of follow-up in children
and in elderly adults, as reported by Henkin et al.33 and
Budenz et al.,31 respectively. Increased contralateral lateralization of cortical activity (during the P1 potential)
toward the linguistically dominant left hemisphere in
children with unilateral right CI,11 together with data
showing similar bilateral activation (during the P3 potential) to speech sounds in children with right CI and
normal-hearing peers,34 may elucidate the differences in
performance between children with a right and left CI.33
Interestingly, the right CI advantage was more
prominent in three perilingually deafened children who
suffered meningitis at 20, 27, and 33 months and were
implanted shortly thereafter (3–6 months), compared to
the remaining seven children who were all prelingually
deafened and implanted at a mean age of 17 months.
The meaning of the magnitude of the right CI advantage
in a monaural speech perception task in quiet is unclear.
Nonetheless, the more pronounced right–left difference
in the perilingual children (23%) compared to the prelingual children (11%) may reflect substantial time in
sound and exposure to language prior to loss of hearing,
together with their older age at evaluation.
For the currently studied group, the duration of CI
use and age at evaluation were strongly correlated with
the right–left difference. In other words, with increasing
duration of implant use from 18 to 75 months and
increasing age at evaluation from 30 to 108 months, the
right CI preference increased. This finding is in agreement with dichotic listening data from normal-hearing
right-handed children showing that the right ear preference for verbal material increased with age from 7 to 13
years.37,38 It has been suggested that developmental
increases in attention, working memory, and language
skills may enlarge the magnitude of ear advantage.25,39
Fig. 4. Right (Rt)–left (Lt) difference in performance as a function
of duration of bilateral cochlear implant (CI) use. Note that with
increasing duration of bilateral CI use, the right–left difference
increases.
Henkin et al.: Right Ear Advantage and Bilateral CIs
Finally, recent data from a multicenter study show
superior expressive and receptive language skills in 25
children with bilateral CI compared to carefully matched
children with unilateral CI after 3 years of CI use. Moreover, eight children who were implanted simultaneously
achieved higher expressive word development scores
compared to those who were implanted sequentially. It
is reasonable to assume that improved sound localization
and speech perception in quiet and in challenging listening environments reported for children with bilateral CI
facilitates incidental learning that is crucial for normal
language development. Moreover, it is plausible that
simultaneous bilateral cochlear implantation led to normal development of auditory pathways and restored the
right ear advantage for speech that is typical in the
presence of normal hearing.
CONCLUSION
Current preliminary data indicate that children with
bilateral CIs implanted simultaneously exhibited a significant right ear advantage for speech presented monaurally in quiet. Similarly to reports on normal-hearing
children, right ear preference for speech increased with
increasing age and auditory–linguistic experience. Thus,
simultaneous bilateral cochlear implantation may lead to
normal development of auditory pathways and may be an
important contributor to the superior auditory, language,
and communication skills reported in children with
bilateral versus unilateral CI.
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