European Annals of Otorhinolaryngology, Head and Neck diseases 133S (2016) S31–S35

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Original article

Active inhibition of the first over the second ear implanted

sequentially
S. Burdo a,∗ , A. Giuliani b , L. Dalla Costa a
a
ICP Milano and Audiovestibology Center, Varese, Italy
b
U.O.D Audiovestibologia Ospedale di Circolo, Varese, Italy

a r t i c l e i n f o a b s t r a c t

Keywords: Objective: To identify the influence of the first implanted ear on the performance of the delayed sequen-
Bilateral cochlear implants tially implanted ear in pediatric patients.
Sequential surgery Study design: Retrospective case series review.
Hearing deprivation
Setting: Outpatient Cochlear Implant (CI) center.
Hearing inhibition
Patients: Congenitally deaf children who underwent unilateral implant at various ages followed by
sequential implant of the contralateral ear with various delays were enrolled in the study. Children were
divided into two groups based on the retention of the first implant or its removal, creating a sequential
unilateral user group (USG) and a sequential bilateral user group (BSG). Both groups reflect differing
durations of auditory deprivation in each ear, being relatively longer for the USG group for each ear than
for the BSG group.
Intervention: Rehabilitative.
Main outcome measures: All patients underwent periodic speech recognition testing for two years after
the second surgery. The results for each implanted ear in both groups were evaluated and an index score
representing the Difference Between the Ears, (DBE), was calculated.
Results: A statistically significant difference results was obtained between the groups. Both groups
reached interaural equivalence (i.e. DBE = 0%), after two years post-sequential implant. The USG patients
achieved interaural equivalence at a faster rate than the BSG patients with 85% USG subjects demon-
strating it at 6 months compared to the majority of BSG patients demonstrating equivalence at one-year
post-sequential implant.
Conclusions: The performance of the sequentially implanted ear depends to an extent on a negative
influence, which could be considered as a type of inhibition, of the first implanted ear over the second
ear. It appears that the role of the unilateral auditory deprivation is not the primary influencing factor.
These findings have driven us clinically to redefine some important considerations for rehabilitation
management of the deaf children in the cases of delayed sequential implant.
© 2016 Elsevier Masson SAS. All rights reserved.

1. Introduction Bilateral implantation can be accomplished simultaneously

Today, bilateral cochlear implant surgery is considered to be
the treatment of choice, rather than single cochlear implant, in
bilateral hearing loss. This is especially important for young, early
deafened children with severe to profound bilateral hearing loss,
who need complete listening (re)habilitation as a basis for speech
and language development and daily functioning, as opposed to
restoration of sufficient hearing in only one ear through a unilateral
surgery [1–4].
∗ Corresponding author at: Audiovestibology Center, via G. D’arezzo 8, 21100
Varese, Italy. Tel.: +393485725178.
E-mail address: sanburdo@tin.it (S. Burdo).
within the same surgery, or at two different times sequen-
tially.
The majority of Authors report better and faster postoperative
results in simultaneous CI surgeries compared to sequential pro-
cedures, when the second ear is implanted after a relatively long
time (e.g. > 4 years), due to sensory deprivation [5–7]. Long periods
of unilateral stimulation may hinder the activation of the binaural
auditory processing. There seems to be a sort of “critical period”
[8–11].
Logical as it may sound considering the general physiopathology
of hearing, clinical experience suggests there are other confounding
complex factors and not only a simple sensorial deprivation that
influence the hearing development in the second ear implanted
sequentially.

http://dx.doi.org/10.1016/j.anorl.2016.04.009
1879-7296/© 2016 Elsevier Masson SAS. All rights reserved.
S32 S. Burdo et al. / European Annals of Otorhinolaryngology, Head and Neck diseases 133S (2016) S31–S35

The aim of our retrospective clinical review is to verify if audi-
tory deprivation is indeed the only cause of poorer performance
observed for the delayed sequentially implanted ear compared
with the contralateral ear, and in particular, if the first implanted
ear may even worsen the influence of long deprivation via the cen-
tral auditory pathways.
To clarify the issue, we compared two groups of sequentially
implanted patients. In group 1, patients were using only the second
implant because the first had been explanted due to medical rea-
sons, while in group 2, the first implant was kept active for bilateral
stimulation.
The two groups shared a period of unilateral stimulation in one
ear followed by a sequential surgery in the opposite ear, while the
difference was in the presence/absence of an active first implant,
thus allowing us to evaluate the influence of the first ear over the
performance of the second implanted ear.
2. Materials and methods
2.1. Subjects
The study is a retrospective evaluation of two groups of congen-
itally deaf implanted children who underwent sequential cochlear
implant surgery in the second ear in Varese, Italy.
In the first group (Unilateral Sequential Group, USG), a num-
ber of unilateral CI users underwent second implant surgery in the
opposite ear after the first implant had been removed due to med-
ical reasons, and thus continued with unilateral stimulation in the
opposite ear. In the second group (Bilateral Sequential Group, BSG),
all children were initially unilateral CI users who underwent a sec-
ond implant procedure in the contralateral ear to provide bilateral
stimulation.
All surgeries, except for the first implant for three USG patients,
were performed by the same surgeon (first author of this paper), all
resulting in complete electrode insertion and fully working devices
over the longitudinal two-year evaluation period.
USG children served as reference group and were compared to
a selection of BSG children, in order to match patient and thera-
peutic criteria as closely as possible thus reducing the number of
additional influencing variables upon the group performance. USG
children represent all subjects who underwent sequential unilat-
eral implant contralaterally, following explant of the first ipsilateral
implant in the Varese clinic within 2006, out of an overall number
of 797 implantees at that time.
BSG children were selected in a group of 130 bilaterally sequen-
tially implanted in the same clinic over the same time interval,
using defined criteria. Consideration was given to ensure matching
of characteristics between the groups such as: age at onset of bilat-
eral hearing loss, age at the beginning of oral habilitation therapy,
surgeons, surgical experience and methods, therapists and their
training for assessment and implementation of the rehabilitation
program. Furthermore, matching of technical issues of the sound
processor and speech coding strategies used was implemented for
both groups.
Conversely, ages at first and second implant as well as inter-
implant intervals varied largely between the USG and BSG groups,
because bilateral patients were implanted earlier for both the sur-
geries. Therefore poorer results were expected for subjects with
longer periods of deprivation (i.e. USG group). Details for each sub-
ject in each group are shown in Table 1.
2.2. Unilateral Sequential Group (USG)
The USG group consisted of seven deaf patients (5 males and
2 females) implanted unilaterally at the mean age of 5.3 years
between the years 1993 and 2000. The diagnosis of deafness was
made within 24 months of age (mean, 15 months), and all subjects
were enrolled in oral rehabilitation programs within 48 months of
birth (mean 20 months). All patients were congenitally profoundly
deaf except one patient, AR, who had a progressive hearing loss
from severe to profound at the time of the first surgery.
All but two USG children received their second CI at the
same time as the explant with two exceptions who received the
second implant one month after explant. The reason for explanta-
tion/reimplantation was receiver extrusion in one case and chronic
otitis media with cholesteatoma caused by exposure of the elec-
trode array in the external auditory canal in six patients (four from
the middle of the canal and two from the annulus fibrosus and the
tympanic membrane caused by an initial episode of adhesive otitis).
Patients received the second contralateral CI before early 2006
within the age of 13 years (mean age 11.16 years) with a period of
3–12 years since the first surgery (mean 6 years). All CI recipients
used a Nucleus implant and were programmed with the ACE strat-
egy, five with ADRO and two without preprocessing algorithms.
For the second implant, the USG patients followed the usual audi-
tory training that consisted of “at home” training, for 20 minute
intervals twice weekly, via video conference with the Varese Cen-
ter therapists, until equivalent performance between the ears was
reached.
2.3. Bilateral sequential group (BSG)
This group consisted of seven patients (4 females and 3 males),
congenitally, profoundly deaf, operated sequentially between 2005
and 2006 and matched in terms of technical, surgical and rehabili-
tation aspects to the existing USG patients. The BSG group received
the first CI at the mean age of 24 months and the second after a
mean of 4 years. All patients used Nucleus implants. All recipients
used the ACE processing strategy in the second implant with ADRO.
The BSG patients followed the same rehabilitation program as
used with the USG patients, which was performed until inter-
aural equivalence was reached. The sound processor of the first
implanted ear was removed both during the rehabilitative sessions
and continuously when the patient stayed at home and replaced
for all activities outside the home (e.g. at school).
2.4. Speech Tracking as the Outcome Measure
All patients were evaluated with Speech Tracking in word per
minutes (W.p.M.) at scheduled intervals after surgery: at CI acti-
vation and after 1, 6, 12, and 24 months. In BSG patients, speech
recognition performance was evaluated and compared for both
ears at each test interval. In USG patients, performance for the
sequentially implanted ear was assessed at the same intervals, and
compared to performance in the first implanted ear recorded at
the last test prior to explant. Data for both groups was compared
to reference speech tracking data for normally hearing children of
the lab.
Before each evaluation, the implants were examined acousti-
cally with the Hearing Aid Test Box and electrically via impedance
telemetry in order to confirm the normal functioning of the devices.
Speech Tracking (ST) is based on connected discourse [12,13],
following the De Filippo and Scott [14] methodology modified by
the Varese Group [15]. This test is commonly used for the evaluation
of hearing-impaired patients, to optimize the fitting of devices and
during long-term rehabilitation to record the patients’ progress,
without any “ceiling effect” [16]. Being a live voice test, Speech
Tracking may be blamed of poor reliability due to the examiner
effect [17]. The potential variability was reduced by providing the
examiners with specific training and certification, to ensure the
desired skills to perform the tests were met. Speech samples were
 S. Burdo et al. / European Annals of Otorhinolaryngology, Head and Neck diseases 133S (2016) S31–S35 S33

Table 1
Patients characteristics for USG (n = 7) and BSG (n = 7) subjects.

Characteristics of the subjects in monthsa First ear

Group ID Gender Etiology Age at Starting Age Side Nucleus model Last speech Strategy Preprocessing
diagnosisa rehabilitationa 1st ICa 1st IC 1st IC processor

USG
USG AR M Unknown 24 24 48 L CI 24 M Sprint ACE ADRO
USG BR M Genetic 24 48 60 R CI 24 RCS Sprint ACE ADRO
USG CA M Ototoxicity 14 14 36 L CI 22 Sprint M. Peak None
USG FA F CMV 7 7 48 L CI 22 Sprint M. Peak None
USG FR M Neonatal meningitis 8 9 60 L CI 24 M Sprint ACE ADRO
USG GI M Unknown 13 24 48 L CI 22 Sprint ACE ADRO
USG RO F Unknown 15 15 132 L CI 24 M Esprit 3G ACE None
Mean 15 20 62
SD 7 14 32

BSG
BSG BU F Perinatal distress 9 9 19 L CI24RCA Freedom ACE ADRO
BSG TO F Genetic 14 19 26 R CI 24 RCS Freedom ACE ADRO
BSG CO M Genetic 24 24 24 R CI 24 RCS SPrint ACE ADRO
BSG CR M Unknown 8 8 24 L CI 24 M Freedom ACE ADRO
BSG LA M Genetic 2 2 18 R CI 24 RCS SPrint ACE ADRO
BSG Ri F Genetic 14 14 36 L CI 24 RCS Freedom ACE ADRO
BSG SC F Genetic 17 17 24 R CI 24 RCS Freedom ACE ADRO
Mean 13 13 24
SD 7 7 6

Complications Second ear

Group Complication Age Year Age Intertime Side Nucleus model 2nd IC Speech Strategy Preprocessing
explantationa 2nd CI 2nd ICa 2nd IC processor

USG
USG Cholesteatoma 144 2006 144 96 R FREEDOM CI24RE (CA) Freedom ACE None
USG Cholesteatoma 108 2003 108 48 L CI 24 RCS Sprint ACE ADRO
USG Cholesteatoma 96 1998 96 60 R CI 24 M Sprint Mpeak/ACE None/ADRO
USG Cholesteatoma 84 2002 132 84 R CI 24 RCS Sprint Mpeak/ACE ADRO
USG Cholesteatoma 132 2003 132 72 R CI 24 RCS ESPrit 3G ACE None
USG Cholesteatoma 192 2001 156 108 R CI 24 RCS Sprint ACE ADRO
USG Extrusion 168 2001 144 12 R CI 24 RCS ESPrit 3G ACE None
Mean 132 130 69
SD 39 21 32

BSG
BSG None – 2006 48 29 R FREEDOM CI24RE (CA) Freedom ACE ADRO
BSG None – 2005 74 29 L FREEDOM CI24RE (CA) Freedom ACE ADRO
BSG None – 2006 72 USD48 L FREEDOM CI24RE (CA) Freedom ACE ADRO
BSG None – 2005 80 USD48 R FREEDOM CI24RE (CA) Freedom ACE ADRO
BSG None – 2006 48 USD56 L FREEDOM CI24RE (CA) Freedom ACE ADRO
BSG None – 2006 60 USD30 R FREEDOM CI24RE (CA) Freedom ACE ADRO
BSG None – 2006 60 USD24 L FREEDOM CI24RE (CA) Freedom ACE ADRO
Mean 63 39
SD 13 12
a
Related to the age units of the table.

preselected according to the age and memory span of each patient,
thus excluding the cognitive load involved in speech comprehen-
sion and focusing on evaluation of speech recognition through
audition.
2.5. Data Analysis
In this paper, we have reviewed and considered the analysis
of the performance of each ear assessed monaurally over time to
compare the interaural differences between the USG and the BSG
groups. Bilateral stimulation results are not presented because the
assessment of binaural listening is not the aim of this report.
Using the ST results for each ear implanted, we calculated
an index referred to as the Difference Between Ears (DBE) and
expressed as a percentage between 0 to 100%.
The value was calculated with following formula:
100 × (WPM of 1st CI − WPM of 2nd CI ear)/WPM of 1st CI.
DBE allows the evaluation of the interaural difference in each
patient. A DBE value of 0% as the ultimate target value indicates
interaural equivalence (i.e. no interaural difference) in individual
ear speech recognition scores. Inequivalence between the ears can
reach a maximum of 100%, which means complete absence of inter-
aural equivalence.
When choosing which data should be included in our statistical
analysis, only two main independent variables proved interesting:
the age at surgery and the presence/absence of the first implant.
Issues like the kind of deafness, surgeon, CI internal parts, process-
ors and training strategies were indeed similar in the two groups.
Moreover, patients in the BSG group were chosen among those
who had significantly earlier surgeries, in order to warrant better
DBE results, therefore only a strong influence of the first implant
could have reversed the expected results in favour of the BSG group.
Hence, the ultimate independent variable considered for the
statistical analysis is the presence/absence of the first implant.
The series of DBE index was examined via the Kolmogorov-
Smirnov Test for Normal Distribution. Between-group comparisons
at any given point in time were performed by means of the Inde-
pendent Samples t-test (assuming equal variances) for the samples
S34 S. Burdo et al. / European Annals of Otorhinolaryngology, Head and Neck diseases 133S (2016) S31–S35

Table 2
Individual Speech Tracking results and DBE for USG (n = 7) and BSG (n = 7) subjects at each evaluation interval. Recognition scores in words per minute (W.p.M.).

Group Patients Activation 1st month 6 months 12 months 24 months

First CI 2nd CI DBE First CI 2nd CI DBE First CI 2nd CI DBE First CI 2nd CI DBE First CI 2nd CI DBE

USG
USG AR 47 15 68 47 20 57 47 33 30 47 42 11 47 53 −13
USG BR 36 17 53 36 36 0 36 36 0 36 36 0 36 36 0
USG CA 42 9 79 42 28 33 42 42 0 42 42 0 42 45 −7
USG FA 48 12 75 48 21 56 48 46 4 48 46 4 48 52 −8
USG FR 12 4 67 12 12 0 12 12 0 12 12 0 12 12 0
USG GI 49 12 76 49 35 29 49 49 0 49 49 0 49 48 2
USG RO 38 5 87 38 14 63 38 25 34 38 26 32 38 35 8
Mean 39 11 72 39 24 34 39 35 10 39 36 7 39 40 −3
SD 13 5 11 13 10 27 13 13 15 13 13 12 13 14 7

BSG
BSG BU 43 8 81 43 10 77 48 15 69 48 34 29 55 53 4
BSG TO 38 8 79 41 15 63 43 33 23 50 46 8 50 48 4
BSG CO 49 18 63 49 20 59 49 26 47 42 41 2 56 52 7
BSG CR 42 16 62 43 20 53 45 27 40 48 47 2 52 49 6
BSG LA 59 15 75 63 20 68 68 45 34 69 51 26 73 68 7
BSG Ri 29 7 76 30 14 53 30 24 20 39 38 3 43 43 0
BSG SC 40 17 58 40 23 43 37 29 22 44 42 5 46 46 0
Mean 43 13 70 44 17 60 46 28 36 49 43 11 54 51 4
SD 9 5 9 10 5 11 12 9 17 10 6 12 10 8 3

with Normal Distribution and Mann-Whitney test for independent

samples for the samples without Normal Distribution. Significance
was accepted for P-values < 0.05.

3. Results

Table 2 shows speech tracking results for individual subjects,

for each CI ear at each test interval, over a 24-month period fol-
lowing the sequential implant in the second ear, for each group. All
patients for both groups were able to perform the speech tracking
task showing significant benefit over the pre-implant condition for
that ear.
Among BSG children, speech tracking scores in each ear
improved over two years of bilateral stimulation experience.
Results are consistent with the reference data obtained from
normal-hearing children using the Varese method, indicating an
improvement rate of 5 wpm per year, from the age of 4 years to 15
years of life. At 15 years of age, the speech tracking reference data
suggests adult performance levels are obtained. Fig. 1. Means with statistical comparison (P-value of Mann-Whitney test for inde-
As reported in Table 2, BSG children showed interaural per- pendent samples) of DBEs for both USG and BSG groups at each evaluation interval
from 1 month to 24 months post-sequential implant. Significance is evident at
formance equivalence two years after the sequential implant.
6 months post-sequential surgery.
However, interaural equivalence (Fig. 1) occurs predominantly
between 12 and 24 months post-sequential implant.
Similarly, USG patients showed equivalent performance USG patients (n = 3), the results after two years of stimulation in the
between the last recorded performance for the explanted ear and second ear were better than the last assessment obtained with the
the sequentially implanted opposite ear, despite the long period of first implanted ear.
hearing deprivation experienced both bilaterally and unilaterally Means and statistical comparison of the DBE index for both
in these cases. groups at each interval as shown in Fig. 1, suggests significantly
Furthermore, we found it very interesting to observe that USG greater interaural performance at 6 months for the USG group com-
patients reached interaural equivalency faster than BSG patients, pared to the BSG group, and marginally better performance up to
and it happened for the majority of USG cases at 6 months post 24 months post-sequential implant.
second surgery (Fig. 1).
The results are more evident when comparing the individual and 4. Discussion
the mean DBE for both groups. Data reported in Table 2 clearly show
that as early as within the first month after sequential implant, Both the USG group and BSG group, in contrast with the suppo-
two USG patients (28%) had reached interaural equivalence. By 6 sition of Graham et al. (2009), demonstrate the ability to obtain
months, four USG patients (57%) demonstrate interaural equiva- significant benefit from auditory stimulation of the sequentially
lence. implanted contralateral ear for speech recognition over time. This
One exception exists for a single USG patient, RO, whose second is possible for patients in both groups with short and long periods of
implanted ear, following 24 months of listening experience, still auditory deprivation in either one or both ears following both short
had poorer performances than the first implanted ear, measured and long intervals of unilateral stimulation in the first implanted
prior to explant following 2 years of listening experience. For some ear. In fact the mean age of the first implant for USG group was
 S. Burdo et al. / European Annals of Otorhinolaryngology, Head and Neck diseases 133S (2016) S31–S35
5.3 years, versus 2 years of the BSG and the mean period between
the surgeries was 6 years for the USG and 4 years for the BSG.
These results suggest that the degree and rate of benefit
achieved in the second implanted ear is not only impacted by age
of the first implant [18], by the duration of unilateral stimulation in
the first ear and the inter-implant interval as previously reported in
the introduction, but also by the presence or absence of active stim-
ulation of the first implanted ear as the second ear attempts to take
advantage of the delayed and newly received electrical stimulation.
Data for our small selected cohorts receiving a sequential
implant in the contralateral ear, in the presence or absence of ongo-
ing stimulation in the first implanted ear, demonstrate a statistical
significant difference between the groups for rate of improvement
in speech tracking performance of the second implant ear over the
first two years of listening experience. The results show that poorer
or slower performance of the sequentially implanted ear is nega-
tively influenced by the presence of an active stimulation from the
first implanted ear for at least the first 12 months and up to 24
months for some individuals, even if the first implant is removed
for short periods of aural rehabilitation on a daily basis.
The results indicate relatively more rapid progression towards
interaural performance equivalency for USG children compared to
BSG children, in spite of the longer deprivation. In fact with the
evident longer periods of auditory deprivation in both ears for the
USG children, the faster rate towards interaural equivalency may be
attributed to the absence of active stimulation in the first implanted
ear while listening skills improve in the second implanted ear. As
some USG children even demonstrated superiority of the second
ear over the first, the potential for influence of cognitive maturation
and or advanced technology for the second implant ear must be
acknowledged, although difficult to quantify in the realm of our
study.
5. Conclusion
The experience described proves the influence of stimulation of
the first ear upon the development of the hearing in the second
ear, as an active inhibition process during the dichotic listening
experience.
In fact, the unexpected relatively rapid development of hearing
performance within the first 6 months of listening experience in the
second sequentially implanted ear as observed in our USG patients
(i.e. explanted ipsilaterally and reimplanted contralaterally) who
had experienced long periods of auditory deprivation, leads us to
conclude that, the interval of auditory deprivation in the second ear
is not the only important issue to consider in explaining the poorer
performance observed for late implanted sequential bilateral CI
users. The concept of the “lazy ear” [19] should thus be revisited
because the adverse effect of prolonged periods of absent stimu-
lation in the sequentially implanted CI ear is also largely impacted
by the increased negative or inhibitory activity produced by the
S35
central auditory pathways of the earlier implanted opposite side,
that presides predominantly.
Therefore our conclusion is that efforts to address the limits of
late sequential implantation should be concentrated on develop-
ing a dedicated and rational rehabilitation strategy [11] aiming at
the better ear in order to “inhibit the inhibitor” and not only to
stimulate the “lazy ear”.
Disclosure of interest
The authors declare that they have no competing interest.
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