AJA

Research Article

Prospective Evaluation of Cognitive

Functions After Rehabilitation With Cochlear
Implant or Hearing Aids: Preliminary Results
of a Multicentric Study on Elderly Patients
Roberta Anzivino,a Guido Conti,a Walter Di Nardo,a Anna Rita Fetoni,a Pasqualina Maria Picciotti,a
Camillo Marra,b Valeria Guglielmi,c Susanna Fortunato,d Francesca Forli,d
Gaetano Paludetti,a and Stefano Berrettinid

Objective: Recent literature has shown a growing interest post-rehabilitation scores were reported in physical and
in the relationship between presbycusis and cognitive emotional impacts in life, general global health, vitality, and
decline, but significant evidence about the long-term benefit social activities. MMSE and RAVLT scores were significantly
of rehabilitation on cognitive functions has not been reported improved in both groups after 6 months of follow-up,
yet. The aim of the study was to analyze audiological and suggesting a global involvement of memory domain.
neuropsychological performances in patients with cochlear Mnesic performances remained unchanged between the
implant (CI) or hearing aids (HAs) over time. first and second follow-up, but a further significant
Materials and Method: Forty-four bilaterally deaf patients improvement in executive functions (Stroop Test) was
aged more than 60 years (25 with CI candidacy and 19 with detected in patients with CI reevaluated 12 months after
HA candidacy) were enrolled. Patients were subjected to implantation. A significant correlation of the RAVLT with
audiological evaluation, to a battery of neuropsychological signal-to-noise ratio at +10 dB speech-in-noise scores and
tests (Mini-Mental State Examination [MMSE], Rey Auditory the MMSE with signal-to-noise ratio at 0 dB speech-in-noise
Verbal Learning Task [RAVLT], Rey–Osterreith Complex scores suggests the pivotal role of executive functions in
Figure Test, Digit/Corsi Span Forward and Backward, recognition in noisy environment.
Multiple Features Target Cancellation, Trail-Making Test, Conclusions: Our preliminary data confirm that hearing
Stroop Test, and Phonological and Semantic Word deprivation in aged patients represents a truly modifiable
Fluency), and to a quality of life assessment (Short Form risk factor for cognitive decline, which can be positively
36, Glasgow Benefit Inventory, Glasgow Health Status faced by acoustic rehabilitation. The improvement of short-
Inventory) at the baseline and after a long-term follow-up and long-term memory performances and the amelioration
(6–12 months). of executive and attentive functions suggest that hearing
Results: Speech recognition scores in quiet and in noise restoration with both HAs and CI may provide a recovery of
were significantly improved even 6 months after auditory superior cognitive domains probably through a reallocation of
rehabilitation. Significant differences between pre- and cortical resources altered by hearing deprivation.

W
ith the gradual increase of life expectancy, the
a
Institute of Otorhinolaryngology, Catholic University of Sacred prevalence of both cognitive and hearing perfor-
Heart, Fondazione Policlinico “A Gemelli,” IRCCS Rome, Italy mance impairment in older adults is growing
b
Memory Clinic, Catholic University of Sacred Heart, Fondazione
(Lin, Niparko, & Ferrucci, 2011). Dementia currently affects
Policlinico “A Gemelli,” IRCCS Rome, Italy
c 50 million people worldwide, and one in three cases appears
Neurology Unit, Catholic University of Sacred Heart, Fondazione
Policlinico “A. Gemelli,” IRCCS Rome, Italy to be associated with hearing loss (HL; Alzheimer’s Disease
d
ENT Audiology and Phoniatrics Unit, University Hospital of Pisa, Italy International, 2018). The putative correlation between de-
Correspondence to Camillo Marra: camillo.marra@policlinicogemelli.it mentia and HL emerged in the late 1980s (Ohta, Carlin, &
Editor-in-Chief: Gabriella Tognola
Harmon,1981; Peters, Potter, & Scholer, 1988; Uhlmann,
Larson, & Koepsell, 1986; Uhlmann, Larson, Rees, Koepsell,
Received November 13, 2018
Revision received March 29, 2019 & Duckert, 1989); so far, cross-sectional and longitudinal
Accepted April 3, 2019
https://doi.org/10.1044/2019_AJA-HEAL18-18-0176
Publisher Note: This article is part of the Special Issue: Select Papers Disclosure: The authors have declared that no competing interests existed at the
From the Hearing Across the Lifespan (HEAL) 2018 Conference. time of publication.

762 American Journal of Audiology • Vol. 28 • 762–774 • October 2019 • Copyright © 2019 American Speech-Language-Hearing Association

Downloaded from: https://pubs.asha.org Iberoamericana- Instituto Universitaria on 04/05/2024, Terms of Use: https://pubs.asha.org/pubs/rights_and_permissions
 population-based studies involving large cohorts of pa- D’Agostino, & Wolf, 2002; Lin, 2011; Peters et al., 1988;
tients suggest that auditory dysfunction is associated with Viljanen et al., 2009), it has been suggested that the evalua-
impairment in several cognitive domains and accelerated tion of hearing impairment and the adequate acoustic reha-
cognitive decline, up to incident dementia in older adults bilitation (hearing aids [HAs] and cochlear implant [CI]) are
(Dawes, Cruickshanks, et al., 2015; Kiely, Gopinath, Mitchell, essential not only to maintain long-term quality of life but
Luszcz, & Anstey, 2012; Lin et al., 2013; Tay et al., 2006; van also to safeguard the brain function (Bernabei et al., 2014).
Hooren et al., 2005; Wallhagen, Strawbridge, & Shema, 2008). However, the percentage of HA use remains very low:
Recently, a longitudinal study on about 155,000 peo- In the United States, 26.7 million adults over 50 years old
ple aged 65 years and older demonstrated that bilateral HL suffer from presbycusis, but only 3.8 million use HAs
is associated with a 43% increase in the possibility to develop (Chien & Lin, 2012). Overall, about 70% of the presbycusis
dementia whereas unilateral HL can be associated with an population seems to refuse hearing rehabilitation.
increase of about 20% (Fritze et al., 2016). Specifically, the At present, few articles provided evidence for the
risk of developing dementia was reported to be 2.7-fold improvement in cognitive performance after hearing res-
higher for every 10 dB of HL (Gallacher et al., 2012). toration (Amieva et al., 2015; Cosetti et al., 2016; Dawes,
Indeed, Lin and colleagues monitored for 12 years a Cruickshanks, et al., 2015; Dawes, Emsley, et al., 2015;
large population of older adults with no initial diagnosis of Kalluri & Humes, 2012; Mosnier et al., 2015, 2018; Rönnberg
dementia and found that a mild, moderate, or severe HL was et al., 2011; Sonnet et al., 2017). It has already been dem-
associated with a risk of cognitive decline that was respec- onstrated that auditory rehabilitation is significantly associ-
tively twofold, threefold, and fivefold higher than in people ated with the reduction of a major depressive disorder after
without hearing disorders (Lin, Metter, et al., 2011). Inter- only 6 months of use (J. S. Choi et al., 2016; Mener, Betz,
estingly, presbycusis has been reported to be associated Genther, Chen, & Lin, 2013). Interestingly, some reports
with the modification of several specific cognitive domains, showed that the use of HAs in older adults is associated
including verbal episodic memory (Lin, Ferrucci, et al., with better scores in neuropsychological tests (Dawes,
2011), semantic memory (Rönnberg et al., 2011), and exec- Cruickshanks, et al., 2015; Dawes, Emsley, et al., 2015;
utive functions (Lin, 2011; Lin, Ferrucci, et al., 2011). Lin, 2011) and a delayed cognitive decline over a 25-year
However, the mechanism underlying the correlation period if compared with progression in untreated patients
between cognitive impairment and HL is still debuted (Amieva et al., 2015).
(Fortunato et al., 2016; Thomson, Auduong, Miller, & However, data on the ability of hearing rehabilita-
Gurgel, 2017), as reported by a recent meta-analysis (Taljaard, tion in preventing or decreasing cognitive decline are con-
Olaithe, Brennan-Jones, Eikelboom, & Bucks, 2016). troversial, and evidence is obtained by using questionnaires
Several hypotheses about the causative relationship (Amieva et al., 2015; Mulrow et al., 1990) and not stan-
between these two conditions have been described: (a) Re- dardized batteries of tests on several domains, such as
duced auditory input linked to defective consolidation of reaction time, pair matching, and fluid intelligence (Dawes,
memory tracks and altered activation of compensatory Cruickshanks, et al., 2015; Dawes, Emsley, et al., 2015).
mechanism for comprehension could lead to a reallocation By reviewing the literature, articles showing objective re-
of alternative (mnesic and executive) neuronal resources sults have been obtained measuring the Mini-Mental State
for hearing function with changes in synaptic plasticity and Examination (MMSE) overall score (Acar, Yurekli,
early onset of cognitive damage (“hypothesis of signal Babademez, Karabulut, & Karasen, 2011), or in the con-
degradation” by Peelle, Troiani, Grossman, & Wingfield, trary, dedicated tests (A. Y. Choi, Shim, Lee, Yoon, & Joo,
2011, or “hypothesis of sensory deprivation” by Lin, 2011; 2011; Lin, 2011) have been administered to elderly pa-
Lin et al., 2013); (b) the weariness caused by decoding tients in order to focus on one single neurocognitive func-
sounds typical of HL might provide cortical adjustment by tion (such as memory), without any comparison with the other
enrolling accessory neural networks, ultimately resulting domains. Furthermore, in many cases, cognitive assessment
in constant “cognitive load,” to such an extent as to make was performed before device fitting; therefore, cognitive
the brain more vulnerable to cognitive decline (with a fur- reserve reduction could be confused with the effects of HL.
ther negative effect on hearing capacity and brain skills, as Despite increasing evidence for the effectiveness of
reported by Cardin, 2016); (c) the trigger of both problems HAs on cognition, very few data have been published on
may be represented by a “common etiopathological mech- the effects of CIs on cognitive impairment: Mosnier et al.
anism,” such as microvascular conditions (Helzner et al., (2015, 2018) have reported a remarkable improvement in
2011; Lin & Albert, 2014); (d) social isolation and related all cognitive abilities, that is, attention, memory, mental
communication difficulties could cause solitude and im- flexibility, and executive functions (none of the specific
paired self-esteem, well-known risk factors for cognitive dis- cognitive skills was highlighted over the others) in 81% of
orders due to increased transcription of proinflammatory patients observed 12 months after the implantation and a
genes (Cole, Hawkley, Arevalo, & Cacioppo, 2011). protective effect of cochlear implantation in a 6.8-year
In the light of the association between HL and some follow-up, with no incidence of mild cognitive impairment
critical aspects of the aging process, from cognitive decline or dementia among healthy patients recruited.
to real dementia, even to falls (Barrett-Connor, Weiss, Although the slowdown of age-related cognitive decline
McHorney, Miller, & Siris, 2009; Gates, Beiser, Rees, is a suggested beneficial effect of auditory rehabilitation,

Anzivino et al.: Cognitive Function After Auditory Rehabilitation 763

Downloaded from: https://pubs.asha.org Iberoamericana- Instituto Universitaria on 04/05/2024, Terms of Use: https://pubs.asha.org/pubs/rights_and_permissions
 some aspects still remain to be clarified, such as the specific Audiological Assessment
cognitive domains predominantly involved, the long-term
Baseline (T0)
stability of the effects obtained, and the most likely under-
Peripheral auditory function was evaluated at the
lying mechanism. These factors could be fundamental for
time of recruitment by means of ear, nose, and throat check
personalized prescription of hearing rehabilitation and
and collection of clinical history, tympanometry, and
prosthesis fitting.
cochleostapedial reflex study, in order to exclude other con-
The aim of the present multicentric research is to
ditions linked to HL. The determination of auditory threshold
analyze the relationship between audiological and neuro-
was performed through pure-tone and speech audiometry
psychological performances in elderly patients who had
with Turrini et al. dysillabic words and Burdo/Orsi open-set
undergone acoustic rehabilitation with CI or HAs. This is
sentences (female speaker) using headphones and in free-
a longitudinal, prospective study investigating every cogni-
field and supraliminar tests for discomfort-level measure.
tive skill (examined individually) at the baseline (T0 = HA
HA candidates were also subjected to a speech-in-
indication or CI activation) and after short- and long-term
noise test, which detected the maximum intelligibility level
follow-ups (T1= 6 months and T2= 12 months, respectively),
in presence of a “cocktail party” competitive signal with
in order to provide significant evidence about an endur-
signal-to-noise ratios (SNRs) at +10, 0, and −10 dB. Elec-
ing benefit of a correct auditory rehabilitative intervention
trophysiological tests (e.g., Auditory Brainstem Response)
on specific neurocognitive functions.
and otoacoustic emissions (e.g., transient evoked otoacoustic
emissions and distortion product otoacoustic emissions)
concluded the audiological investigation.
Material and Method At the baseline, patients with CI showed a mean
Study Population pure-tone average (PTA) value in free field of 102.09 dB
and a mean word recognition score of 8.75% without HA.
Among patients followed for periodic hearing evalua- Patients with HAs showed moderate-to-severe sensorineural
tions at Gemelli Hospital of Rome and University Hospital symmetric HL, with mean PTAs of 48.21 dB on the left
of Pisa, 25 candidates for CI and 19 subjects with HA indi- side and 52.88 dB on the right side. Word recognition mean
cation were enrolled for this study between January 2016 scores at 60 dB were 74.28% in the left ear, 65.71% in the
and March 2018. right ear, and 64.28% in free field, while sentence compre-
Inclusion criteria were as follows: age > 60 years, hension mean score in free field was 67.21%. Finally, regard-
not known diagnosis of neurological disease (such as ing the recognition of words in noise, the average scores
Alzheimer’s disease, Parkinson’s disease, multiple sclerosis) calculated were 63.92% with SNR at +10 dB, 46% with
or cognitive impairment (MMSE > 24/30), education and SNR at 0 dB, and 18% with SNR at −10 dB. These data
cultural level ≥ 8 years, no other disabilities (such as visual confirmed the indication to HAs.
impairment), and real motivation to hearing rehabilitation.
Candidates for cochlear implantation (patients with T1 (6 months) and T2 (12 months)
CI), 14 women and 11 men (Mage = 66.4 ± 5.8 years), were An audiological follow-up was performed 6 months
postlingually deafened patients with bilateral severe-to- after the intervention for each of the 25 patients with CI,
profound sensorineural HL, with mean age of onset of verifying the stability and adequacy of the fitting and the
47 ± 12.3 years and various etiologies (cochlear otosclerosis, gain obtained. The same audiological evaluation was re-
sudden HL, idiopathic or autoimmune diseases); three out peated 12 months after CI activation in 11 of 25 patients.
of 25 patients received a Med-EL Synchrony device, and Sixteen of 19 patients with HAs were studied 6 months
22 out of 25 patients received a Cochlear CI512 device. The after the first application, performing fitting session at the
majority of the candidates (64%) used contralateral HA, referral center a few days before the audiological evalua-
with an average time of use before surgical intervention tions. All patients, regardless of the type of rehabilitation,
of 206.4 ± 149.75 months. All patients with CI have con- were subjected to pure-tone audiometry in free field to
cluded the audiological and neuropsychological short-term determine the amount of gain obtained on the auditory
follow-up (T1 = 6 months), whereas 11 out of 25 have under- threshold and by means of headphones to monitor residual
gone a second evaluation (T2 = 12 months postintervention); hearing without device.
nevertheless, one patient was considered an outlier, conse-
quentially excluded from data analysis due to the onset of a
psychiatric pathology with major implication on cognitive Cognitive Ability Assessment
status between T1 and T2. An extensive neuropsychological test battery was ar-
All 19 candidates to HAs (patients with HAs), 11 women ranged to specifically explore various cognitive domains in
and eight men (Mage = 74.92 ± 5.4 years), affected by bi- both patients with CI and patients with HA (see Table 1).
lateral moderate–severe sensorineural HL, were treated
with bilateral retroauricular HAs. Sixteen out of 19 patients General Cognitive Status
have reached first audiological and cognitive evaluation The MMSE (Magni, Binetti, Bianchetti, Rozzini, &
(T1 = 6 months). Trabucchi, 1996) is a widely used test in clinical practice

764 American Journal of Audiology • Vol. 28 • 762–774 • October 2019

Downloaded from: https://pubs.asha.org Iberoamericana- Instituto Universitaria on 04/05/2024, Terms of Use: https://pubs.asha.org/pubs/rights_and_permissions
 Table 1. Neuropsychological test battery.
sequence is presented, the participant is asked to recall
the sequence in either the normal or reverse order.
Global cognitive profile Mini-Mental State Examination
(screening)
The Corsi Span Forward and Backward (Monaco
Episodic memory Rey Auditory Verbal Learning Task et al., 2013) block-tapping test is a psychological test that
(Immediate Recall, Delayed Recall, assesses visuospatial short-term working memory. It involves
Recognition) mimicking an examiner as he or she taps a sequence of up
Rey–Osterreith Complex Figure (Recall)
Working memory Digit Span Forward and Backward
to nine identical spatially separated blocks. The sequence
Corsi Span Forward and Backward starts out simple, usually using two blocks, but becomes
Attention Multiple Features Target Cancellation more complex until the subject’s performance suffers.
Trail-Making Tests A and B Attentional tasks. The Multiple Features Target
Executive functions Stroop Test
Cancellation (Marra et al., 2013) is a demanding test of
Rey–Osterreith Complex Figure (Copy)
Semantic memory Phonological Verbal Fluency visual attention that requires the identification and cancel-
Categorical Semantic Fluency lation of 13 targets arrayed in a random way among
67 distractors. Three scores are obtained: time of execu-
tion, number of false alarms, and accuracy.
for cognitive function screening because of its speed of ad- The Trail-Making Test (Tombaugh, 2004) investi-
ministration (10–15 min) and ease in scoring and consists gates visual attention speed of processing, mental flexi-
of 11 tests that provide a scale of scores from a minimum of bility, and task switching and consists of two parts in
0 (maximum cognitive impairment) to a maximum of 30 (no which the subject is instructed to connect in the correct
cognitive impairment). The cognitive areas investigated are order a set of 25 targets (first, only numbers and then num-
orientation in time and in space, recording of words, atten- bers and letters) as quickly as possible while maintaining
tion and calculation, language, and constructive praxia. The accuracy.
“threshold” score that distinguishes a healthy patient from Specific executive tasks. The Stroop Color and Word
one with an initial or advanced cognitive impairment is 24. Interference Test short form (Caffarra, Vezzadini, Dieci,
Zonato, & Venneri, 2002b), particularly suitable to study
frontal lobe damage, assesses the ability to inhibit cogni-
Memory Tasks tive interference, which occurs when the processing of a
The Rey Auditory Verbal Learning Task (RAVLT; stimulus’ feature affects the simultaneous processing of an-
Carlesimo, Caltagirone, & Gainotti, 1996) consists of im- other attribute of the same stimulus. Subjects are required to
mediate and 15-min delayed recall of 15 high-frequency se- read three different tables as fast as possible: Two of
mantically unrelated words and successive recognition of them represent the “congruous condition” in which partici-
the 15 RAVLT words among 30 distractors after another pants are required to read names of colors (henceforth
15 min (recognition test does not only evaluate episodic referred to as color words) printed in black ink (W) and
memory but also involves executive functions). name different color patches (C). On the contrary, in the
The Rey–Osterreith Complex Figure Test (Caffarra, third table, named color word (CW) condition, color words
Vezzadini, Dieci, Zonato, & Venneri, 2002a) is a neuro- are printed in an inconsistent colored ink (for instance, the
psychological task in which examinees are asked to copy word “red” is printed in green ink): Participants have to
a complex line drawing figure and then to draw it from name the ink instead of the printed word; thus, they are re-
memory (recall) after a 15-min delay. Many different cog- quired to perform a less automated task (i.e., naming ink
nitive abilities are needed for a correct performance; therefore, color) and to inhibit a more interfering and automated task
this test is useful to evaluate long-term visual memory after (i.e., reading).
15 min, but also visuospatial abilities, attention, planning, and The Phonological Word Fluency Task (Harrison,
working memory (executive functions) during the copy. Buxton, Husain, & Wise, 2000) evaluates lexical skills and
semantic knowledge, together with executive function. It
requires the production of as many words as possible be-
Executive Functions ginning with a given letter (F, A, S) in a minute of time.
This domain is broadly defined as an overall control Semantic memory. The Semantic Word Fluency Task
process responsible for planning, assembling, coordinating, (Quaranta et al., 2016) requires the production of as many
sequencing, and monitoring other cognitive operations and words as possible belonging to two semantic categories in
therefore involves many other cognitive variables. a given time. Neuropsychological abilities were evaluated
Working memory. The Digit Span Forward and at T0 at first and then at every follow-up period concluded
Backward (Monaco, Costa, Caltagirone, & Carlesimo, by patients with CI and HAs.
2013) is used to measure working memory’s number stor-
age capacity and integrity of the phonological loop. Par-
ticipants listen to a sequence of numerical digits and are Quality of Life Assessment
asked to recall the sequence correctly, with increasingly Outcomes related to the quality of life of patients under-
longer sequences being tested in each trial. Digit span tasks going rehabilitation were assessed using two types of question-
can be given forward or backward, meaning that once the naires. Short Form 36 (SF-36) is a questionnaire on patient’s

Anzivino et al.: Cognitive Function After Auditory Rehabilitation 765

Downloaded from: https://pubs.asha.org Iberoamericana- Instituto Universitaria on 04/05/2024, Terms of Use: https://pubs.asha.org/pubs/rights_and_permissions
 health status, characterized by brevity and precision and Neuropsychological Profile at T0 and T1 in Patients
composed of 36 questions that refer to eight domains: physical With CI and HAs
activities, role limitations due to physical state, physical pain,
general health status, vitality, social activities, role limitations Neuropsychological data were acquired and analyzed
due to emotional state, and mental health status (Apolone & through a two-way multivariate variance analysis for repeated
Mosconi, 1998). The questionnaire was administered to measures, providing a comparison between cognitive per-
patients with CI and HAs, both at the baseline and after formances at baseline T0 and those obtained at T1 (short-
follow-up. The answers obtained have been elaborated through term follow-up in both groups).
a specific software in the ACCESS language developed by The overall cognitive evaluation did not show a signif-
the San Giacomo Hospital of Ponte dell’Olio (Piacenza), icant effect of group factor (Wilk’s λ = 0.297), F(10, 20) =
which allows to obtain for each domain a numerical score 1.18, p < .407, as there were no differences in neuropsycho-
with a minimum value of 0 (very poor performance) and a logical behavior between patients with CI and patients
maximum of 100 (excellent performance). with HAs. On the contrary, a significant effect of test–retest
The Glasgow Benefit Inventory (GBI) is a postopera- factor (baseline vs. follow-up; Wilk’s λ = 0.138), F(10, 20) =
tive questionnaire that verifies the consequences of surgery 3.123, p < .03, was reported, demonstrating that there was
on patient’s state of health (Hendry, Chin, Swan, Akeroyd, & a statistically significant difference in neuropsychological
Browning, 2016). Because of its specificity, this question- behavior as a whole between tests performed at T0 and
naire was distributed to the group of patients with CI (25) those performed at T1 considering all the study samples. No
to verify the effects of the intervention on quality of life, group interaction (patients with CI vs. patients with HAs)
both a few days after activation and at a distance of 12 months in test–retest analysis was observed (Wilk’s λ = 0.448),
from the intervention. F(10, 20) = 0.534, p < .89, suggesting a similar trend of
The Glasgow Health Status Inventory (GHSI) detects improvement in the two groups.
the effects of a health problem on quality of life in a spe- Univariate test analyses for each task showed signifi-
cific moment (Hawthorne & Hogan, 2002) and was there- cantly better performances after rehabilitation in patients
fore administered to the group of 19 patients with HAs at with CI and HAs in the MMSE ( p = .005) and in the
the time of indication and after 6-month follow-up. Both RAVLT Immediate Recall ( p = .003) and Delayed Recall
questionnaires contain 18 questions and provide a total ( p = .003) tests. These results suggested an improvement
score ranging from −100 to +100 in the case of the GBI of the overall cognitive domain of memory (see Table 2),
and from 0 to 100 in the case of GHSI, where 100 refers while the other cognitive domains were not influenced by
to the optimal state of health. acoustic rehabilitation.

Neuropsychological Profile at T1 and T2

Results in Patients With CI
Audiological Performances Cognitive performances have been analyzed in patients
Pure-tone audiometry performed at T1 demonstrated with CI who concluded T2 follow-up (12 months), thus
in patients with CI (n = 25) a significant improvement in providing a comparison between scores obtained at T1 and
perceptive skills even in the first 6 months, with a mean T2. Univariate analysis of specific effects for each single
PTA value of 29.71 dB. Speech audiometry results sug- test reported unmodified results in almost all tests but an
gested increased performance, with mean scores of 62.58% improvement in an executive test (Stroop Interference Test)
in sentence recognition and 66.47% in disyllabic word that showed a decrease in interference inhibition time
recognition at 60 dB, while speech-in-noise tests showed ( p = .01). Only a trend toward a significant improvement
mean comprehension values of 57.58% with SNR at +10 dB, in the Phonological Verbal Fluency Test ( p = .08) and
28.59% with SNR at 0 dB, and 16.89% with SNR at −10 dB in Trail-Making Test A ( p = .07) was also detected (see
(see Figures 1A and 1B). Table 3).
In those patients with HAs who completed the first
follow-up (n = 16), speech performances significantly
Correlation Between Neuropsychological
improved in comparison with the baseline (see Figure 2A),
with mean score rising from 75% (T0) to 92% (T1) in word and Audiological Variables in Patients With CI
recognition and from 77.69% (T0) to 95% (T1) in sentence The percentage of cognitive improvement (Δ improve-
comprehension. ment in the MMSE and in the RAVLT) and audiological
Moreover, significant benefits were also found in word results in noisy conditions (speech-in-noise test scores with
recognition in the presence of background noise, since there SNRs at + 10, 0, and −10 dB) collected after 6-month
was a progression from mean scores of 63.3% with SNR at follow-up in patients with CI were analyzed by means of
+10 dB, 45% with SNR at 0 dB, and 6.6% with SNR at multiple regression analyses in order to identify a relation-
−10 dB collected at T0 to mean scores of 91.6% with SNR ship between perceptive and neuropsychological performance.
at +10 dB, 76.6% with SNR at 0 dB, and 20% with SNR at Two statistically significant positive correlations were
−10 dB after rehabilitation (see Figure 2B). reported: (a) between word recognition score with SNR

766 American Journal of Audiology • Vol. 28 • 762–774 • October 2019

Downloaded from: https://pubs.asha.org Iberoamericana- Instituto Universitaria on 04/05/2024, Terms of Use: https://pubs.asha.org/pubs/rights_and_permissions
 Figure 1. (A) Speech audiometry in free field in patients with cochlear implant. (B) Speech-in-noise test in patients with cochlear implant.
SNR = signal-to-noise ratio.

at +10 dB and Δ improvement in RAVLT delayed recall Statistical differences between mean scores collected
( p = .02) and (b) between word recognition score with pre- and post-rehabilitation were reported in role limitation
SNR at 0 dB and Δ improvement in the MMSE ( p = .04; due to physical state from 32.25 ± 29.71 to 86.53 ± 21.25
see Figures 3A and 3B). ( p = .044), general health status from 47.48 ± 16.96 to
69.23 ± 12.20 ( p = .022), vitality from 50.16 ± 17.72 to
73.84 ± 11.75 ( p = .047), social activities from 48.22 ±
Quality of Life Assessment at T0 and T1 27.15 to 84.78 ± 11.35 ( p = .044), and role limitations
in Patients with CI and HAs due to emotional state from 33.22 ± 42.11 to 96.76 ±
SF-36 scores at T0 and T1 were compared through a ( p = .021). Indeed, the general index of global mental
two-way multivariate analysis of variance for repeated mea- health status increased from 56.77 ± 21.35 at T0 to 83.69
sures in CI (n = 25) and HA (n = 16) users (see Table 4). This ± 13.51 at T1 ( p = .049). On the contrary, physical activi-
analysis did not show any significant effect of group factor ties (mean values of 67.3 ± 25.21 vs. 80.38 ± 19.83) and
(Wilk’s λ = 0.98), F(2, 28) = 0.16, p < .85, thus confirming physical pain (mean values of 74.45 ± 29.17 vs. 78.35 ±
that both groups scored similar answers at the questionnaire. 27.72) did not show statistically significant improvement
A significant effect of test–retest factor was reported at follow-up (see Figure 4).
between baseline and follow-up (Wilk’s λ = 0.640), F(2, 28) = These data were confirmed by GBI and GHSI results.
7.84, p < .002, concerning the statistically different trend of GBI mean total score switched from 21.5 ± 5.04 immediately
questionnaire answers at T0 and T1 in both groups. The postactivation to 47.8 ± 17.8 after 6 months of use of CI.
effect of group interaction (patients with CI vs. patients Among the HA group, an increase in GHSI mean total score
with HAs) in test–retest analysis showed no further signifi- from 37.77 ± 11.8 before rehabilitation to 58.09 ± 8.5 after
cant differences (Wilk’s λ = 0.93), F(2, 28) = 1.09, p < .370, 6-month rehabilitation was detected (see Figures 5A and 5B).
thus providing evidence that the improvement profile be-
tween the groups was not dissimilar. In addition, statistical
analysis through two-tailed Student’s t test for paired vari- Discussion
ables was used in order to compare mean scores for each Data collected in this longitudinal study, even if pre-
SF-36 subdomain at the baseline and 6-month follow-up. liminary, provide evidence for positive effects of hearing

Figure 2. (A) Free-field speech audiometry in hearing aid users. (B) Speech-in-noise test in hearing aid users. SNR = signal-to-noise ratio.

Anzivino et al.: Cognitive Function After Auditory Rehabilitation 767

Downloaded from: https://pubs.asha.org Iberoamericana- Instituto Universitaria on 04/05/2024, Terms of Use: https://pubs.asha.org/pubs/rights_and_permissions
 Table 2. Neuropsychological tests’ scores (with standard deviation) at baseline ( T0) and at 6-month follow-up ( T1) in patients with cochlear
implant (CI) and hearing aids (HAs).

Baseline 1st follow-up

(T0) (T1 = 6 months)
Univariate
Cognitive CI HA CI HA factor Group
domain Test (n = 25) (n =16) p (n = 25) (n =16) p pre/post interaction

Cognitive MMSE 25.36 0.50 26.0 1.03 ns 26.58 0.39 27.66 0.80 ns 0.005 0.65
status
Episodic RAVLT Immediate Recall 36.20 1.86 32.6 3.80 ns 39.96 1.63 36.6 3.33 ns 0.003 0.923
memory RAVLT Delayed Recall 6.95 0.55 6.50 1.14 ns 7.88 0.52 8.16 1.0 ns 0.003 0.372
RAVLT Recognition 13.20 0.43 12.16 0.89 ns 13.57 0.58 13.0 1.19 ns 0.383 0.742
Correct
RAVLT Recognition 1.28 0.39 1.6 0.8 ns 0.59 0.2 1.6 0.4 .02 0.454 0.454
False
Rey’s Figure Recall 12.3 1.34 10.65 2.74 ns 13.0 1.24 6.66 2.53 .03 0.184 0.062
Working Digit Span Forward 5.03 0.24 4.3 0.4 ns 4.8 0.2 4.5 0.48 ns 0.969 0.429
memory Digit Span Backward 3.64 0.23 3.33 0.51 ns 3.56 0.24 2.8 0.49 ns 0.137 0.290
Corsi Span Forward 4.33 0.16 4.00 0.3 ns 4.44 0.16 4.33 0.34 ns 0.225 0.525
Corsi Span Backward 3.90 0.18 3.8 0.38 ns 3.83 0.15 3.83 0.32 ns 0.867 0.867
Attention MFTC Accuracy 0.89 0.01 0.8 0.03 ns 0.89 0.01 0.91 0.04 ns 0.485 0.711
MFTC Errors 0.40 0.22 1.00 0.46 ns 0.36 0.17 0.66 0.34 ns 0.456 0.557
MFTC Time 77.84 7.34 77.5 14.9 ns 62.36 5.90 76.16 12.0 ns 0.190 0.268
TMT-A 75.16 10.7 92.07 22.03 ns 78.46 13.7 101.6 27.97 ns 0.486 0.733
TMT-B 182.0 17.4 188.0 35.67 ns 166.6 17.05 202.8 34.82 ns 0.985 0.284
Executive Phonological Verbal 27.59 2.18 29.16 4.45 ns 28.28 2.03 27.6 4.1 ns 0.831 0.567
functions Fluency
Stroop Test Interference 11.66 2.44 25.08 4.99 ns 15.32 2.95 29.1 6.03 ns 0.162 0.938
Stroop Test Errors 2.80 1.2 2.75 2.64 ns 1.28 0.80 4.33 1.64 ns 0.982 0.292
Rey’s Figure-Copy 29.20 1.50 27.1 1.71 ns 24.39 3.07 24.0 3.50 ns 0.091 0.651
Semantic Categorical Semantic 16.99 1.03 16.5 2.1 ns 16.9 1.00 17.6 2.05 ns 0.528 0.474
memory Fluency

Note. Significant values are in bold. MMSE = Mini-Mental State Examination; ns = not significant; RAVLT = Rey Auditory Verbal Learning
Task; Rey’s Figure = Rey–Osterreith Complex Figure Test; MFTC = Multiple Features Target Cancellation; TMT-A = Trail-Making Test A;
TMT-B = Trail-Making Test B.

restoration with HAs and CI on cognitive functions—first be deeply impacted; in particular, among patients with
of all mnesic abilities and then executive tasks—analyzed hearing impairment, a decreased “learning,” a higher
by a targeted, reproducible, and easily consulted battery of “forgetting score,” and an increase in the “recency effect”
neuropsychological tests. In addition, we confirm the im- were detected, suggesting that mnesic disorders are due
provement in terms of communicative skills and quality of to sensorial deficit and consequent difficult encoding
life after acoustic rehabilitation in elderly patients. of verbal signal, in addition to a weakened postproces-
Many reports in the literature had as their primary objec- sing mechanism necessary for consolidation of learned
tive to investigate the correlation between auditory dys- information.
function and the onset of dementia (Amieva et al., 2015; Furthermore, a close relationship between hearing
Gallacher et al., 2012; Lin, 2011; Lin et al., 2013). On the functions and executive abilities has been reported (Gates
other hand, some studies have been focused on the rela- et al., 2002, 2010; Idrizbegovic et al., 2011). In order to ex-
tionship between hearing impairment and cognitive func- plain attentional and executive efforts, electrophysiological
tions analyzing single cognitive domains. Namely, Lin, and morphological studies have suggested that signal
Ferrucci, et al. (2011) reported the effects of HL in cogni- deprivation could lead to neuronal re-placement and simul-
tively intact deaf subjects on different cognitive functions taneous compensatory activation of new networks to safe-
demonstrating significantly worse performance in the guard a sufficient level of language understanding (Cardin,
MMSE, in episodic memory tests (Free and Cued Selective 2016; Chang et al., 2004; Glick & Sharma, 2017; Lin et al.,
Remaindin Test Delayed Recall subtest), and in executive 2014; Peng, Yu, Chen, Jing, & Liang, 2015; Shafto, Randall,
tests (Trail-Making Test B and Stroop Test). Similarly, in Stamatakis, Wright, & Tyler, 2012).
a previous work, we also investigated cognitive profile of As the mechanisms that link hearing deprivation and
patients with hearing impairment, showing worse perfor- cognition are still debated, scientific reports on neuropsy-
mances on long-term memory RAVLT and immediate chological impact of acoustic rehabilitation provide inconsis-
and delayed recall proportionally related to the degree of tent and not universally accepted results and are mainly
HL (Guglielmi et al., in press). Moreover, we demon- based on simple questionnaires, too rough or not vali-
strated that some qualitative aspect of memory seemed to dated neuropsychological tests battery, and, in some cases,

768 American Journal of Audiology • Vol. 28 • 762–774 • October 2019

Downloaded from: https://pubs.asha.org Iberoamericana- Instituto Universitaria on 04/05/2024, Terms of Use: https://pubs.asha.org/pubs/rights_and_permissions
 Table 3. Neuropsychological tests’ scores (with standard deviation) at 6-month follow-up ( T1) and 12-month follow-up ( T2) in patients with
cochlear implant.

Test 1st follow-up (T1 = 6 months) 2nd follow-up (T2 = 12 months) p

MMSE 27.66 1.65 27.00 2.59 .40

RAVLT Immediate Recall 41.44 8.86 39.33 15.29 .55
RAVLT Delayed Recall 8.55 2.24 7.22 3.52 .15
Recognition Correct 14.00 0.86 12.66 2.29 .09
Recognition False 1.11 1.36 2.77 2.77 .14
Digit Span Forward 5.44 1.33 5.66 1.50 .51
Digit Span Backward 3.55 1.66 3.11 0.78 .56
Corsi Span Forward 4.55 1.33 4.57 0.71 .96
Corsi Span Backward 4.22 1.09 4.14 0.73 .81
MFTC Accuracy 0.89 0.07 0.93 0.07 .10
MFTC Errors 0.22 0.66 1.77 4.26 .31
MFTC Time 48.33 16.28 46.00 21.97 .91
Phonological Verbal Fluency 29.00 10.96 33.88 13.11 .08
Semantic Verbal Fluency 17.55 4.03 18.44 3.24 .39
Stroop Test Interference 25.27 8.08 12.93 9.36 .01
Stroop Test Errors 0.11 0.33 0.27 0.56 .19
Rey’s Figure-Copy 28.44 10.53 29.15 7.02 .84
Rey’s Figure-Recall 11.16 7.87 12.50 5.73 .57
TMT-A 60.11 36.72 68.92 38.08 .07
TMT-B 146.44 73.93 154.31 77.98 .55

Note. Significant values are in bold. MMSE = Mini-Mental State Examination; RAVLT = Rey Auditory Verbal Learning Task; MFTC = Multiple
Features Target Cancellation; Rey’s Figure = Rey–Osterreith Complex Figure Test; TMT-A = Trail-Making Test A; TMT-B = Trail-Making Test
B.

assessment of one single neurocognitive domain (Amieva HAs and cognitive abilities. However, this datum is contro-
et al., 2015; Cosetti et al., 2016; Dawes, Cruickshanks, et al., versial, and some lines of research have not shown the
2015; Lin, 2011; Mosnier et al., 2015, 2018; Rönnberg presence of an improvement from the cognitive point of
et al., 2011; Sonnet et al., 2017). view after 6/12 months of use of HAs (Van Hooren et al.,
Several decades ago, Mulrow et al. (1990), in a ran- 2005; Wong, 2011). Therefore, as noted in the review of
domized case–control trial, showed an improvement of Kalluri and Humes (2012), there is currently no evidence
cognitive functions after 4 months of using HAs in only for a protective effect of hearing rehabilitation on age-
13 patients with hearing impairment aged more than 70 years. related cognitive decline.
Twenty years later, two studies reported similar results In this perspective, even if data are still referred to a
(Acar et al., 2011; A. Y. Choi et al., 2011) in a small cohort small sample of patients, in this study, we performed a
of patients. The only works with an adequate sample are multivariate analysis of overall cognitive profile by means
attributable to Lin (2011), Rönnberg et al. (2011), and Amieva of the MMSE and the involvement of every single cognitive
et al. (2015), with positive association between the use of function basing on complete neuropsychological evaluation,

Figure 3. Significant correlations between neuropsychological and audiological scores at T1: (A) Rey Auditory Verbal Learning Task Delayed
Recall (RAVLT DR) and (B) Mini-Mental State Examination (MMSE). SNR = signal-to-noise ratio.

Anzivino et al.: Cognitive Function After Auditory Rehabilitation 769

Downloaded from: https://pubs.asha.org Iberoamericana- Instituto Universitaria on 04/05/2024, Terms of Use: https://pubs.asha.org/pubs/rights_and_permissions
 Table 4. Quality of life comparison at baseline ( T0) versus 6-month follow-up ( T1) in patients with cochlear implant (CI) and hearing aids (HAs).

Baseline ( T0) 1st follow-up ( T1 = 6 months ) Test ×

Health Retest Group
domain CI (n = 25) HA (n = 16) p CI (n = 25) HA (n = 16) p interaction interaction

SF-36 Generic 48.3 3.57 55.3 7.2 .397 59.9 2.82 59.1 5.77 .384 0.02 0.260
SF-36 Mental 57.1 4.42 66.0 9.03 .912 71.8 3.79 73.1 7.73 .878 0.0003 0.174

Note. SF-36 = Short Form 36. Significant values are in bold.

demonstrating a positive effect of acoustic rehabilitation domain, as a first step, could benefit from auditory reha-
with both HAs and CIs. In fact, even at the early time bilitation (even after only 6 months of use). These data
point (6 months of follow-up), a statistically significant im- suggest that the replacement of verbal encoding due to the
provement in cognitive status was detected, without differ- recovery of auditory threshold could erase the mismatch
ences in general neuropsychological behavior between the between real and perceived stimuli and improve the consoli-
two groups. Interestingly, as shown in Table 2, the auditory dation of the information, passing it to memory systems.
rehabilitation technique did not affect the trend of cogni- The impact of cochlear implantation on cognitive de-
tive improvement over time. Our data suggest that the cline has been studied by Mosnier et al. (2015) on 94 sub-
presence of hearing deprivation during senescence repre- jects evaluated with a battery of six neuropsychological
sents a modifiable risk factor for cognitive decline and re- tests (investigating attention, memory, orientation, executive
quires rehabilitative intervention regardless of the prevalent functions, mental flexibility, and fluency). They reported
underlying pathogenic mechanism. that 81% of subjects evaluated after 12 months (30 of 37)
Both groups of patients showed 6 months (T1) after showed a global improvement in performance in all tests
cochlear implantation or HA application an improvement administered; in addition, an improvement in social activi-
in global cognitive profile (MMSE) and in the long-term ties and quality of life was found. Among patients with
memory (RAVLT Immediate and Delayed Recall). Both the best cognitive performance before implantation, 76%
these aspects might be explained as the result of the gradual remained stable and only 24% showed a very slight decline.
reversibility of neuronal reallocation process due to hearing As reported by Castiglione et al. (2016) in a study on sub-
deprivation, previously described as “hypothesis of the jects with hearing impairment screened through the Montreal
degradation of the signal.” Memory deficit could be con- Cognitive Assessment Test, a correct auditory treatment
sidered the earliest neuropsychological marker of cognitive provided a long-term positive effect, first, on memory tasks
impairment, because cognitive resources recruited to com- and, second, on visuospatial and logical executive skills. Ac-
pensate for hearing impairment belong to memory systems, cordingly with previous results, in another work, pre- and
first of all; it is therefore reasonable to think that the same postimplant cognitive performances were evaluated with a

Figure 4. Short Form 36 (SF-36) subdomain scores before and after rehabilitation with cochlear implant and hearing aids.

770 American Journal of Audiology • Vol. 28 • 762–774 • October 2019

Downloaded from: https://pubs.asha.org Iberoamericana- Instituto Universitaria on 04/05/2024, Terms of Use: https://pubs.asha.org/pubs/rights_and_permissions
 Figure 5. Quality of life scores (A) in patients with cochlear implant measured by Glasgow Benefit Inventory and (B) in patients
with hearing aids measured by Glasgow Health Status Inventory.

3-year follow-up (Cosetti et al., 2016) even if in only seven preliminary data suggest that part of the physical process
patients, demonstrating a greater gain in 70% of verbal and is carried out by the postprocessing mechanisms of hear-
memory tests administered. Finally, Sonnet et al. (2017) ing information; therefore, it is reasonable to think that
reported in 16 patients from 65 to 80 years old that MMSE auditory rehabilitation could provide an improvement in
score evaluations remained stable and executive functions the consolidation of the memory track and the passage
seemed to increase after cochlear implantation. from short- to long-term memory. These modifications of
However, long-term data on the stability of neuro- cognitive areas in favor of memory processes could con-
psychological effects over time after auditory rehabilitation tribute to the stability over time (12 months) of memory
in particular with CI are still poor and mainly focused on test results. To explain the significant increase in executive
the relationship with the incidence of dementia. In a recent functions, we must remember the already considered hy-
work, Mosnier et al. (2018) described results on a pro- pothesis that the presence of hearing impairment requires
longed follow-up (M = 6.8 years) after cochlear implan- the use of additional cognitive (strategic and attentional)
tation in older adults, demonstrating that, among patients resources in order to ensure auditory comprehension. In
with mild cognitive impairment at the baseline, 2% the presence of HL, there is a 24% probability that neuro-
progressed to dementia and 32% recovered to normal nal resources are inevitably subtracted from other cogni-
cognitive status, while none of the healthy patients at the tive processes (Lin et al., 2013) with a phenomenon of
baseline developed dementia during follow-up. Interestingly, cortical plasticity (Fetoni, Troiani, Petrosini, & Paludetti,
these results seem to demonstrate that cochlear implantation 2015), particularly in tests that require a higher commitment
can decrease and sometimes reverse the process of cogni- of executive control. It is probable that a longer time is
tive decline. needed to restore the original neuronal circuits assigned
Some controversial aspects are not yet clarified, such to higher cognitive functions due to a re-reallocation of
as specific cognitive domains that are improved by rehabilita- attentive resources from auditory perception to executive
tion, long-term stability of the effects obtained, and putative functions.
pathophysiological mechanisms (Claes et al., 2016). Regarding audiological performance, results obtained
Therefore, this study had the aim to investigate the confirmed the undoubted CI benefit among elderly patients,
importance of preserving the physiological auditory function as already demonstrated in recent literature and in a previ-
following acoustic rehabilitation and observe over time the ous article (Di Nardo, Anzivino, Giannantonio, Schinaia, &
neuropsychological behavior that follows the reversibility of Paludetti, 2014). A significant gain in word and sentence
the condition of hearing disability. Ten out of the 25 partici- comprehension was reported in comparison to preintervention
pants with CI were subjected to neuropsychological and threshold. Moreover, as previously described (Di Nardo
audiological reevaluation at 12 months (T2), while currently et al., 2014; Vermeire et al., 2005), in this work, SF-36, GBI
no patient with HA completed the 1-year observation period. (in patients with CI), and GHSI (in patients with HAs)
The accurate comparison between data at T1 and T2 post-rehabilitation scores confirm besides the beneficial
showed that cognitive levels acquired in the first 6 months impact that hearing rehabilitation determines quality of
remain stable in the 1-year assessment but, in addition, ex- life. It is worth noting that, while parameters of general
ecutive function results significantly improved. In particu- physical and mental health, vitality, social activities, and
lar, the reduction of the “Time of execution” at the Stroop physical and emotional limitations in daily life differed
Test interference subset proves the improvement of selec- significantly from follow-up to the baseline condition,
tive attention demanding tasks in these subjects. subdomains concerning physical pain and physical activity
A major finding is that hearing rehabilitation pro- remained almost similar, and it could be related to the
vides stability of auditory–verbal memory activities and aging processes involved in the senescence, rather than
improves executive functions and selective attention. These hearing level and/or cognitive impairment.

Anzivino et al.: Cognitive Function After Auditory Rehabilitation 771

Downloaded from: https://pubs.asha.org Iberoamericana- Instituto Universitaria on 04/05/2024, Terms of Use: https://pubs.asha.org/pubs/rights_and_permissions
 Regardless of the type of acoustic device, recognition of Helsinki) for experiments involving humans. Every enrolled
in noise was greatly improved after only 6 months of use, subject gave us informed consent for experimentation.
depending strictly on the amount of background signal.
Recent studies (Anderson, White-Schwoch, Parbery-Clark,
& Kraus, 2013) suggested that not only hearing threshold References
but also predominantly cognitive factors such as central in- Acar, B., Yurekli, M. F., Babademez, M. A., Karabulut, H., &
formation processing, cognitive functions, and even experi- Karasen, R. M. (2011). Effects of hearing aids on cognitive
ence in everyday life are involved in this task. The perceptive functions and depressive signs in elderly people. Archives
difficulty in noise and in the presence of a degraded signal of Gerontology and Geriatrics, 52(3), 250–252. https://doi.org/
is attributed to the presence of regressive processes in the 10.1016/j.archger.2010.04.013
Alzheimer’s Disease International. (2018). World Alzheimer report.
cortical areas that entail a qualitative deficit, often coexist- Retrieved from http://www.alz.co.uk
ing with the quantitative sensory deficit linked to the pe- Amieva, H., Ouvrard, C., Giulioli, C., Meillon, C., Rullier, L., &
ripheral structures. Positive correlations found in this work Dartigues, J. F. (2015). Self-reported hearing loss, hearing aids,
between the speech-in-noise test performances with SNR and cognitive decline in elderly adults: A 25-year study. Journal
at +10 dB and the long-term verbal memory (RAVLT) test of the American Geriatrics Society, 63(10), 2099–2104.
scores and between speech-in-noise test performance with Anderson, S., White-Schwoch, T., Parbery-Clark, A., & Kraus, N.
SNR at 0 dB and the MMSE score must be taken into ac- (2013). A dynamic auditory–cognitive system supports speech-
count in this perspective. in-noise perception in older adults. Hearing Research, 300, 18–32.
Apolone, G., & Mosconi, P. (1998). The Italian SF-36 Health Survey:
Since only a limited sample has completed a substan-
Translation, validation and norming. Journal of Clinical Epi-
tial follow-up to date, the data just discussed are still pre- demiology, 51(11), 1025–1036.
liminary and need to be confirmed by continuing follow-up Barrett-Connor, E., Weiss, T. W., McHorney, C. A., Miller, P. D.,
and recruitment of other patients. However, our encouraging & Siris, E. S. (2009). Predictors of falls among postmenopausal
findings lay the foundations for a new personalized reha- women: Results from the National Osteoporosis Risk Assess-
bilitation approach that encourages an accurate study of ment (NORA). Osteoporosis International, 20(5), 715–722.
cognitive functions prior to application and device selec- Bernabei, R., Bonuccelli, U., Maggi, S., Marengoni, A., Martini, A.,
tion, as the different baseline neuropsychological profiles Memo, M., . . . Lin, F. R. (2014). Hearing loss and cognitive
of patients could influence the outcome achieved. decline in older adults: Questions and answers. Aging Clinical
and Experimental Research, 26(6), 567–573.
Caffarra, P., Vezzadini, G., Dieci, F., Zonato, F., & Venneri, A.
(2002a). Rey–Osterrieth complex figure: Normative values in
Conclusion an Italian population sample. Neurological Sciences, 22(6),
Alongside a consistent literature about the relation- 443–447.
ship between auditory and cognitive function, recent studies Caffarra, P., Vezzadini, G., Dieci, F., Zonato, F., & Venneri, A.
are trying to provide long-term evidence of the benefit of (2002b). Una versione abbreviata del test di Stroop: Dati norma-
rehabilitation through hearing solutions on delaying the tivi nella popolazione italiana. Nuova Rivista di Neurologia,
12, 111–115.
natural history of cognitive decline while maintaining good
Cardin, V. (2016). Effects of aging and adult-onset hearing loss on
cerebral function in late life. In this perspective, our results cortical auditory regions. Frontiers in Neuroscience, 10, 199.
constitute interesting findings about the trend over time in Carlesimo, G. A., Caltagirone, C., & Gainotti, G. (1996). The
neuropsychological profile of patients with hearing im- mental deterioration battery: Normative data, diagnostic reli-
pairment after rehabilitation, demonstrating the stability ability and qualitative analyses of cognitive impairment. The
of memory activities over 12-month follow-up and the group for the standardization of the mental deterioration battery.
additional executive and attentive function improvement in European Neurology, 36, 378–384.
the long-term evaluation. Castiglione, A., Benatti, A., Velardita, C., Favaro, D., Padoan, E.,
Although further studies are needed to confirm our Severi, D., . . . Martini, A. (2016). Aging, cognitive decline and
hearing loss: Effects of auditory rehabilitation and training
data, this work supports the hypothesis that early hearing
with hearing aids and cochlear implants on cognitive function
restoration is essential in older adults because it allows to and depression among older adults. Audiology and Neuro-Otology,
counteract, at least in part, the effects of aging, bringing 21(Suppl. 1),, 21–28.
notable benefits not only for sensory input recovery but Chang, Y., Lee, S. H., Lee, Y. J., Hwang, M. J., Bae, S. J., Kim,
also for cognitive profile and quality of life. According to M. N., . . . Kang, D. S. (2004). Auditory neural pathway eval-
the theory that sensory de-afferentation causes plastic neuro- uation on sensorineural hearing loss using diffusion tensor
cortical rearrangements, auditory rehabilitation may pro- imaging. NeuroReport, 15(11), 1699–1703.
vide a recovery of superior cognitive domains probably Chien, W., & Lin, F. R. (2012). Prevalence of hearing aid use
through a reallocation of cortical resources altered by among older adults in the United States. Archives of Internal
Medicine, 172(3), 292–293.
hearing deprivation. Choi, A. Y., Shim, H. J., Lee, S. H., Yoon, S. W., & Joo, E. J.
(2011). Is cognitive function in adults with hearing impairment
improved by the use of hearing aids? Clinical and Experimental
Acknowledgments Otorhinolaryngology, 4(2), 72–76.
This work has been carried out in accordance with the Choi, J. S., Betz, J., Li, L., Blake, C. R., Sung, Y. K., Contrera,
Code of Ethics of the World Medical Association (Declaration K. J., & Lin, F. R. (2016). Association of using hearing aids or

772 American Journal of Audiology • Vol. 28 • 762–774 • October 2019

Downloaded from: https://pubs.asha.org Iberoamericana- Instituto Universitaria on 04/05/2024, Terms of Use: https://pubs.asha.org/pubs/rights_and_permissions
 cochlear implants with changes in depressive symptoms in validity and test–retest reliability. British Journal of Clinical
older adults. JAMA Otolaryngology—Head & Neck Surgery, Psychology, 39(Pt. 2), 181–191.
142(7), 652–657. Hawthorne, G., & Hogan, A. (2002). Measuring disability-specific
Claes, A. J., Mertens, G., Gilles, A., Hofkens-Van den Brandt, A., patient benefit in cochlear implant programs: Developing a
Fransen, E., Van Rompaey, V., & Van de Heyning, P. (2016). short form of the Glasgow Health Status Inventory, the Hear-
The Repeatable Battery for the Assessment of Neuropsycho- ing Participation Scale. International Journal of Audiology,
logical Status for Hearing Impaired Individuals (RBANS-H) 41(8), 535–544.
before and after cochlear implantation: A protocol for a pro- Helzner, E. P., Patel, A. S., Pratt, S., Sutton-Tyrrell, K., Cauley,
spective, longitudinal cohort study. Frontiers in Neuroscience, J. A., & Talbott, E. (2011). Hearing sensitivity in older adults:
10, 512. Associations with cardiovascular risk factors in the health,
Cole, S. W., Hawkley, L. C., Arevalo, J. M., & Cacioppo, J. T. aging and body composition study. Journal of the American
(2011). Transcript origin analysis identifies antigen-presenting Geriatrics Society, 59, 972–979.
cells as primary targets of socially regulated gene expression in Hendry, J., Chin, A., Swan, I. R., Akeroyd, M. A., & Browning,
leukocytes. Proceedings of the National Academy of Sciences G. G. (2016). The Glasgow Benefit Inventory: A systematic re-
of the United States of America, 108(7), 3080–3085. view of the use and value of an otorhinolaryngological generic
Cosetti, M. K., Pinkston, J. B., Flores, J. M., Friedmann, D. R., patient-recorded outcome measure. Clinical Otolaryngology,
Jones, C. B., Roland, J. T., Jr., & Waltzman, S. B. (2016). 41(3), 259–275.
Neurocognitive testing and cochlear implantation: Insights into Idrizbegovic, E., Hederstierna, C., Dahlquist, M., Kämpfe Nordström,
performance in older adults. Clinical Interventions in Aging, C., Jelic, V., & Rosenhall, U. (2011). Central auditory function
11, 603–613. in early Alzheimer’s disease and in mild cognitive impairment.
Dawes, P., Cruickshanks, K. J., Fischer, M. E., Klein, B. E., Klein, Age and Ageing, 40(2), 249–254.
R., & Nondahl, D. M. (2015). Hearing-aid use and long-term Kalluri, S., & Humes, L. E. (2012). Hearing technology and cogni-
health outcomes: Hearing handicap, mental health, social engage- tion. American Journal of Audiology, 21(2), 338–343. https://
ment, cognitive function, physical health, and mortality. Inter- doi.org/10.1044/1059-0889(2012/12-0026)
national Journal of Audiology, 54(11), 838–844. Kiely, K. M., Gopinath, B., Mitchell, P., Luszcz, M., & Anstey, K. J.
Dawes, P., Emsley, R., Cruickshanks, K. J., Moore, D. R., Fortnum, (2012). Cognitive, health, and sociodemographic predictors of
H., Edmondson-Jones, M., . . . Munro, K. J. (2015). Hearing loss longitudinal decline in hearing acuity among older adults.
and cognition: The role of hearing aids, social isolation and Journals of Gerontology: Series A: Biological Sciences and
depression. PLOS ONE, 10(3), e0119616. Medical Sciences, 67(9), 997–1003.
Di Nardo, W., Anzivino, R., Giannantonio, S., Schinaia, L., & Lin, F. R. (2011). Hearing loss and cognition among older adults
Paludetti, G. (2014). The effects of cochlear implantation on in the United States. Journals of Gerontology: Series A: Biological
quality of life in the elderly. European Archives of Oto-Rhino- Sciences and Medical Sciences, 66, 1131–1136.
Laryngology, 271(1), 65–73. Lin, F. R., & Albert, M. (2014). Hearing loss and dementia—Who
Fetoni, A. R., Troiani, D., Petrosini, L., & Paludetti, G. (2015). is listening? Aging & Mental Health, 18(6), 671–673.
Cochlear injury and adaptive plasticity of the auditory cortex. Lin, F. R., Ferrucci, L., An, Y., Goh, J. O., Doshi, J., Metter, E. J.,
Frontiers in Aging Neuroscience, 7, 8. . . . Resnick, S. M. (2014). Association of hearing impairment
Fortunato, S., Forli, F., Guglielmi, V., De Corso, E., Paludetti, G., with brain volume changes in older adults. NeuroImage, 90,
Berrettini, S., & Fetoni, A. R. (2016). A review of new insights 84–92.
on the association between hearing loss and cognitive decline Lin, F. R., Ferrucci, L., Metter, E. J., An, Y., Zonderman, A. B.,
in ageing. Acta Otolaryngologica Italica, 36(3), 155–166. & Resnick, S. M. (2011). Hearing loss and cognition in the
Fritze, T., Teipel, S., Óvári, A., Kilimann, I., Witt, G., & Doblhammer, Baltimore Longitudinal Study of Aging. Neuropsychology, 25,
G. (2016). Hearing impairment affects dementia incidence. An 763–770.
analysis based on longitudinal health claims data in Germany. Lin, F. R., Metter, E. J., O’Brien, R. J., Resnick, S. M., Zonderman,
PLOS ONE, 11(7), e0156876. A. B., & Ferrucci, L. (2011). Hearing loss and incident dementia.
Gallacher, J., Ilubaera, V., Ben-Shlomo, Y., Bayer, A., Fish, M., Archives of Neurology, 68, 214–220.
Babisch, W., & Elwood, P. (2012). Auditory threshold, phono- Lin, F. R., Niparko, J. K., & Ferrucci, L. (2011). Hearing loss
logic demand, and incident dementia. Neurology, 79, 1583–1590. prevalence in the United States. Archives of Internal Medicine,
Gates, G. A., Beiser, A., Rees, T. S., D’Agostino, R. B., & Wolf, P. A. 171(20), 1851–1852.
(2002). Central auditory dysfunction may precede the onset of Lin, F. R., Yaffe, K., Xia, J., Xue, Q. L., Harris, T. B., Purchase-
clinical dementia in people with probable Alzheimer’s disease. Helzner, E., . . . Simonsick, E. M. (2013). Hearing loss and cog-
Journal of the American Geriatrics Society, 50, 482–488. nitive decline in older adults. JAMA Internal Medicine, 173(4),
Gates, G. A., Gibbons, L. E., McCurry, S. M., Crane, P. K., Feeney, 293–299.
M. P., & Larson, E. B. (2010). Executive dysfunction and pres- Magni, E., Binetti, G., Bianchetti, A., Rozzini, R., & Trabucchi, M.
bycusis in older persons with and without memory loss and (1996). Mini-Mental State Examination: A normative study
dementia. Cognitive and Behavioral Neurology, 23, 218–223. in Italian elderly population. European Journal of Neurology,
Glick, A., & Sharma, A. (2017). Cross-modal plasticity in develop- 3(3), 198–202.
mental and age-related hearing loss: Clinical implications. Marra, C., Gainotti, G., Scaricamazza, E., Piccininni, C., Ferraccioli,
Hearing Research, 343, 191–201. M., & Quaranta, D. (2013). The Multiple Features Target Can-
Guglielmi, V., Marra, C., Picciotti, P. M., Masone Iacobucci, G., cellation (MFTC): An attentional visual conjunction search test.
Giovannini, S., Quaranta, D., . . . Conti, G. (in press). Does Normative values for the Italian population. Neurological
hearing loss in the elderly conform to an impairment of specific Science, 34(2), 173–180.
cognitive domains? Journal of Geriatric Psychiatry and Neurology. Mener, D. J., Betz, J., Genther, D. J., Chen, D., & Lin, F. R. (2013).
Harrison, J. E., Buxton, P., Husain, M., & Wise, R. (2000). Short Hearing loss and depression in older adults. Journal of the
test of semantic and phonological fluency: Normal performance, American Geriatrics Society, 61(9), 1627–1629.

Anzivino et al.: Cognitive Function After Auditory Rehabilitation 773

Downloaded from: https://pubs.asha.org Iberoamericana- Instituto Universitaria on 04/05/2024, Terms of Use: https://pubs.asha.org/pubs/rights_and_permissions
 Monaco, M., Costa, A., Caltagirone, C., & Carlesimo, G. A. (2013). Sonnet, M. H., Montaut-Verient, B., Niemier, J. Y., Hoen, M.,
Forward and backward span for verbal and visuo-spatial data: Ribeyre, L., & Parietti-Winkler, C. (2017). Cognitive abilities
Standardization and normative data from an Italian adult popu- and quality of life after cochlear implantation in the elderly.
lation. Neurological Sciences, 34(5), 749–754. Otolology & Neurotology, 38(8), e296–e301.
Mosnier, I., Bebear, J. P., Marx, M., Fraysse, B., Truy, E., Taljaard, D. S., Olaithe, M., Brennan-Jones, C. G., Eikelboom,
Lina-Granade, G., . . . Sterkers, O. (2015). Improvement of R. H., & Bucks, R. S. (2016). The relationship between hearing
cognitive function after cochlear implantation in elderly patients. impairment and cognitive function: A meta-analysis in adults.
JAMA Otolaryngology—Head & Neck Surgery, 141(5), Clinical Otolaryngology, 41(6), 718–729.
442–450. Tay, T., Kifley, A., Lindley, R., Landau, P., Ingham, N., Mitchell,
Mosnier, I., Vanier, A., Bonnard, D., Lina-Granade, G., Truy, E., P., & Wang, J. J. (2006). Are sensory and cognitive declines
Bordure, P., . . . Belmin, J. (2018). Long-term cognitive prog- associated in older persons seeking aged care services? Find-
nosis of profoundly deaf older adults after hearing rehabilitation ings from a pilot study. Annals of the Academy of Medicine,
using cochlear implants. Journal of the American Geriatrics Singapore, 35(4), 254–259.
Society, 66(8), 1553–1561. Thomson, R. S., Auduong, P., Miller, A. T., & Gurgel, R. K.
Mulrow, C. D., Aguilar, C., Endicott, J. E., Velez, R., Tuley, M. R., (2017). Hearing loss as a risk factor for dementia: A systematic
Charlip, W. S., & Hill, J. A. (1990). Association between hear- review. Laryngoscope Investigative Otolaryngology, 2(2), 69–79.
ing impairment and the quality of life of elderly individuals. Tombaugh, T. N. (2004). Trail Making Test A and B: Normative
Journal of the American Geriatrics Society, 38(1), 45–50. data stratified by age and education. Archives of Clinical Neuro-
Ohta, R. J., Carlin, M. F., & Harmon, B. M. (1981). Auditory psychology, 19(2), 203–214.
acuity and performance on the mental status questionnaire in Uhlmann, R. F., Larson, E. B., & Koepsell, T. D. (1986). Hearing
the elderly. Journal of the American Geriatrics Society, 29(10), impairment and cognitive decline in senile dementia of the
476–478. Alzheimer’s type. Journal of the American Geriatrics Society,
Peelle, J., Troiani, V., Grossman, M., & Wingfield, A. (2011). 34(3), 207–210.
Hearing loss in older adults affects neural systems supporting Uhlmann, R. F., Larson, E. B., Rees, T. S., Koepsell, T. D., &
speech comprehension. Journal of Neuroscience, 31(35), Duckert, L. G. (1989). Relationship of hearing impairment to
12638–12643. dementia and cognitive dysfunction in older adults. Journal of
Peng, L., Yu, S., Chen, R., Jing, Y., & Liang, J. (2015). Correla- the American Medical Association, 261(13), 1916–1919.
tion of diffusion tensor imaging between the cerebral cortex van Hooren, S. A., Anteunis, L. J., Valentijn, S. A., Bosma, H.,
and speech discrimination in presbycusis. Lin Chung Er Bi Yan Ponds, R. W., Jolles, J., & van Boxtel, M. P. (2005). Does
Hou Tou Jing Wai Ke Za Zhi, 29(18), 1605–1609. cognitive function in older adults with hearing impairment
Peters, C. A., Potter, J. F., & Scholer, S. G. (1988). Hearing im- improve by hearing aid use? International Journal of Audiol-
pairment as a predictor of cognitive decline in dementia. Journal ogy, 44(5), 265–271.
of the American Geriatrics Society, 36(11), 981–986. Vermeire, K., Brokx, J. P., Wuyts, F. L., Cochet, E., Hofkens, A.,
Quaranta, D., Caprara, A., Piccininni, C., Vita, M. G., Gainotti, G., & Van de Heyning, P. H. (2005). Quality-of-life benefit from
& Marra, C. (2016). Standardization, clinical validation, and cochlear implantation in the elderly. Otology & Neurotology,
typicality norms of a new test assessing semantic verbal fluency. 26(2), 188–195.
Archives of Clinical Neuropsychology, 31(5), 434–445. Viljanen, A., Kaprio, J., Pyykkö, I., Sorri, M., Koskenvuo, M., &
Rönnberg, J., Danielsson, H., Rudner, M., Arlinger, S., Sternäng, Rantanen, T. (2009). Hearing acuity as a predictor of walking
O., Wahlin, A., & Nilsson, L. G. (2011). Hearing loss is nega- difficulties in older women. Journal of the American Geriatrics
tively related to episodic and semantic long-term memory but Society, 57(12), 2282–2286.
not to short-term memory. Journal of Speech, Language, and Wallhagen, M. I., Strawbridge, W. J., & Shema, S. J. (2008). The
Hearing Research, 54, 705–726. relationship between hearing impairment and cognitive function:
Shafto, M., Randall, B., Stamatakis, E. A., Wright, P., & Tyler, A 5-year longitudinal study. Research in Gerontological Nursing,
L. K. (2012). Age-related neural reorganization during spoken 1(2), 80–86.
word recognition: The interaction of form and meaning. Journal Wong, L. L. (2011). Evidence on self-fitting hearing aids. Trends
of Cognitive Neuroscience, 24, 1434–1446. in Amplification, 15(4), 215–225.

774 American Journal of Audiology • Vol. 28 • 762–774 • October 2019

Downloaded from: https://pubs.asha.org Iberoamericana- Instituto Universitaria on 04/05/2024, Terms of Use: https://pubs.asha.org/pubs/rights_and_permissions