Improvement of Cognitive Function After Cochlear Implantation in Elderly Patients

 
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Improvement of Cognitive Function After Cochlear Implantation in Elderly Patients
Research

                  Original Investigation

                  Improvement of Cognitive Function After Cochlear
                  Implantation in Elderly Patients
                  Isabelle Mosnier, MD; Jean-Pierre Bebear, MD; Mathieu Marx, MD, PhD; Bernard Fraysse, MD; Eric Truy, MD; Geneviève Lina-Granade, MD;
                  Michel Mondain, MD, PhD; Françoise Sterkers-Artières, MD; Philippe Bordure, MD; Alain Robier, MD; Benoit Godey, MD, PhD; Bernard Meyer, MD;
                  Bruno Frachet, MD; Christine Poncet-Wallet, MD; Didier Bouccara, MD; Olivier Sterkers, MD, PhD

                                                                                                                                       Supplemental content at
                     IMPORTANCE The association between hearing impairment and cognitive decline has been                              jamaotolaryngology.com
                     established; however, the effect of cochlear implantation on cognition in profoundly deaf
                     elderly patients is not known.

                     OBJECTIVE To analyze the relationship between cognitive function and hearing restoration
                     with a cochlear implant in elderly patients.

                     DESIGN, SETTING, AND PARTICIPANTS Prospective longitudinal study performed in 10 tertiary
                     referral centers between September 1, 2006, and June 30, 2009. The participants included
                     94 patients aged 65 to 85 years with profound, postlingual hearing loss who were evaluated
                     before, 6 months after, and 12 months after cochlear implantation.

                     INTERVENTIONS Cochlear implantation and aural rehabilitation program.

                     MAIN OUTCOMES AND MEASURES Speech perception was measured using disyllabic word
                     recognition tests in quiet and in noise settings. Cognitive function was assessed using a
                     battery of 6 tests evaluating attention, memory, orientation, executive function, mental
                     flexibility, and fluency (Mini-Mental State Examination, 5-word test, clock-drawing test,
                     verbal fluency test, d2 test of attention, and Trail Making test parts A and B). Quality of life
                     and depression were evaluated using the Nijmegen Cochlear Implant Questionnaire and the
                     Geriatric Depression Scale-4.

                     RESULTS Cochlear implantation led to improvements in speech perception in quiet and in
                     noise (at 6 months: in quiet, 42% score increase [95% CI, 35%-49%; P < .001]; in noise, at
                     signal to noise ratio [SNR] +15 dB, 44% [95% CI, 36%-52%, P < .001], at SNR +10 dB, 37%
                     [95% CI 30%-44%; P < .001], and at SNR +5 dB, 27% [95% CI, 20%-33%; P < .001]), quality
                     of life, and Geriatric Depression Scale-4 scores (76% of patients gave responses indicating no
                     depression at 12 months after implantation vs 59% before implantation; P = .02). Before
                     cochlear implantation, 44% of the patients (40 of 91) had abnormal scores on 2 or 3 of 6
                     cognition tests. One year after implant, 81% of the subgroup (30 of 37) showed improved
                     global cognitive function (no or 1 abnormal test score). Improved mean scores in all cognitive
                     domains were observed as early as 6 months after cochlear implantation. Cognitive
                     performance remained stable in the remaining 19% of the participants (7 of 37). Among
                     patients with the best cognitive performance before implantation (ie, no or 1 abnormal
                     cognitive test score), 24% (12 of 50) displayed a slight decline in cognitive performance.
                     Multivariate analysis to examine the association between cognitive abilities before
                     implantation and the variability in cochlear implant outcomes demonstrated a significant
                     effect only between long-term memory and speech perception in noise at 12 months
                                                                                                                                  Author Affiliations: Author
                     (SNR +15 dB, P = .01; SNR +10 dB, P < .001; and SNR +5 dB, P = .02).                                         affiliations are listed at the end of this
                                                                                                                                  article.
                     CONCLUSIONS AND RELEVANCE Rehabilitation of hearing communication through cochlear                           Corresponding Author: Isabelle
                     implantation in elderly patients results in improvements in speech perception and cognitive                  Mosnier, MD, Assistance Publique-
                                                                                                                                  Hôpitaux de Paris, Groupe Hospitalier
                     abilities and positively influences their social activity and quality of life. Further research is
                                                                                                                                  Pitié-Salpêtrière, Unité Otologie,
                     needed to assess the long-term effect of cochlear implantation on cognitive decline.                         Implants Auditifs et Chirurgie de la
                                                                                                                                  base du crâne, Bâtiment Castaigne,
                                                                                                                                  47-83 Boulevard de l’Hôpital, 75651
                     JAMA Otolaryngol Head Neck Surg. doi:10.1001/jamaoto.2015.129                                                Paris CEDEX 13, France (isabelle
                     Published online March 12, 2015.                                                                             .mosnier@psl.aphp.fr).

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Research Original Investigation                                                                    Cognitive Function After Cochlear Implantation

               L
                      arge prospective studies have established an indepen-                This study was approved by the ethics committee (Comité
                      dent association between hearing impairment and                  Consultatif de Protection des Personnes dans la Recherche Bio-
                      cognitive decline.1,2 Individuals with mild to severe            médicale, Groupe Hospitalier, Pitié-Salpêtrière, Paris, 2007).
               hearing loss have a 2- to 5-fold increased risk of developing           Written informed consent was obtained from each patient be-
               dementia compared with those with normal hearing.1 More-                fore their enrollment in the study. Participants did not re-
               over, neuroimaging studies3,4 report an association between             ceive financial compensation.
               peripheral hearing impairment and temporal lobe cortex and
               whole brain atrophy. A combination of several interdepen-               Participants
               dent mechanisms could account for this association, such as             Ninety-four patients were enrolled between September 1, 2006,
               vascular risk factors, neurodegenerative processes affecting            and June 30, 2009, in 10 tertiary referral centers in this pro-
               both peripheral auditory pathways and the cerebral cortex,              spective study. The mean age at implantation was 72 years
               social isolation, and reduced cognitive stimulation. Based on           (range, 65-85 years; median, 71 years). Demographic data, hear-
               these reports, hearing rehabilitation using conventional                ing loss information, and the educational level of all patients
               hearing aids has logically been proposed as a treatment to              are summarized in eTable 1 in the Supplement.
               help improve neurocognitive performance; however, the                        Ninety-three patients underwent a unilateral cochlear im-
               impact of the rehabilitation generated controversial results,           plantation (50 in the right ear, 43 in the left ear), and 1 patient
               with a beneficial effect reported in only half of the elderly           received simultaneous bilateral implantation. Four implant de-
               groups presented in the 6 published analyses.5-10                       vices were used (Neurelec, 29 patients MED-EL, 26; Cochlear,
                    In cases of acquired severe to profound hearing loss with          23; and Advanced Bionics, 17). The brand of the device was de-
               no benefit from conventional amplification, cochlear                    cided primarily by each referral center during patient coun-
               implantation that uses direct electrical stimulation of the             seling, with a view to ensure adequate representation of each
               auditory nerve has proved to be successful; patients 80 years           of the 4 devices available across the study group. Cochlear im-
               or older are one of the groups receiving benefit.11,12 Retro-           plants were activated 2 to 4 weeks after the operation, and sub-
               spective studies 13-2 4 in the geriatric population report              sequent programming sessions were planned to optimize the
               improvement for auditory performance in quiet and noise                 individual map. All patients entered a postactivation aural re-
               despite prolonged duration of deafness, as well as age-                 habilitation program that consisted of individual sessions with
               related degeneration of the spiral ganglion and central audi-           a speech therapist, twice weekly, for at least 6 months. This
               tory pathways. Moreover, similar to younger patients with               training was based on speech perception tasks and on seman-
               cochlear implants, most elderly patients who have received              tic and cognition tasks that engage memory, attention span,
               implants show an increase in social activities and improved             speed of processing, and mental flexibility.
               confidence.15,20,25 To the best of our knowledge, the relation-
               ship between hearing benefit following cochlear implanta-               Speech Perception Measures
               tion and cognitive abilities in elderly patients has not been           Speech perception was scored before implantation and at 6 and
               investigated.                                                           12 months after activation in quiet with the device only (hear-
                    The objective of this prospective, longitudinal multi-             ing aid or cochlear implant) and in best-aided conditions in
               center study was to assess speech perception, cognitive abili-          quiet and in noise. The best-aided condition reflected the pa-
               ties, and quality-of-life scores before implantation and at 6 and       tient’s daily listening condition, defined as cochlear implant
               12 months after cochlear implant activation in patients 65 years        and a contralateral hearing aid when available or cochlear im-
               or older. The focus was to determine the effect of hearing re-          plant alone, if no contralateral hearing aid was used. Measure-
               habilitation including the cochlear implant on cognitive func-          ments were assessed in a sound-treated room using recorded
               tion in addition to the influence of cognitive factors on coch-         materials presented at 60 dB sound pressure level from a loud-
               lear implantation outcomes over time.                                   speaker placed at 0° azimuth. Tests in noise were adminis-
                                                                                       trated at a signal to noise ratio (SNR) ranging from +15 dB to 0
                                                                                       dB, with the speech stimuli and a competing white-noise sig-
                                                                                       nal presented from the front speaker. Test materials con-
               Methods                                                                 sisted of lists of 10 open-set disyllabic words (Fournier lists26).
               Selection Criteria                                                      Two lists of words were presented at each level and re-
               Patients enrolled in this study were postlingually deafened, 65         sponses were scored as the percentage of words correctly iden-
               years or older, and candidates for cochlear implantation (ie,           tified. The ability of patients to communicate on the tele-
               bilateral severe to profound sensorineural hearing loss and             phone with familiar speakers or with strangers was assessed
               speech recognition scores of ≤50% for French open-set disyl-            by the use of a questionnaire developed specifically for the
               labic words presented at 60 dB sound pressure level in quiet,           study.
               in the best-aided condition after verification of the optimal
               hearing aid fitting). Patients were excluded from the study if          Cognitive Measures, Quality-of-Life Assessment,
               they were unable to complete the required procedures owing              and Depression Scale
               either to evidence of severe cognitive or medical disorders di-         Evaluations were performed before implantation and at 6 and
               agnosed during routine medical and psychological evalua-                12 months after cochlear implant activation. Participants were
               tion performed before implantation.                                     assessed by a neuropsychologist with a battery of cognitive

        E2     JAMA Otolaryngology–Head & Neck Surgery Published online March 12, 2015 (Reprinted)                                     jamaotolaryngology.com

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Cognitive Function After Cochlear Implantation                                                                                           Original Investigation Research

                  Figure 1. Mean Speech Perception Scores for Disyllabic Word Tests in Quiet and Noise

                                                         100

                                                         80                                                                  In quiet

                                  Correct Responses, %
                                                                                                                                   Best-aided
                                                                                                                   a               Device only
                                                         60                                                        a         In noise
                                                                                                                                   SNR +15 dB
                                                                                                                                   SNR +10 dB
                                                         40                                                                        SNR +5 dB
                                                                                                                                   SNR 0 dB
                                                         20
                                                                                                                                                     In quiet, patients were tested twice:
                                                                                                                                                     with the device only (hearing aid or
                                                          0
                                                                 Before              6 mo After            12 mo After                               cochlear implant) and in best-aided
                                                               Implantation         Implantation          Implantation                               conditions, with any contralateral
                         No. of patients                                                                                                             hearing aid. In noise, patients were
                         In quiet                                                                                                                    tested only in best-aided conditions.
                            Best-aided                             92                   93                    94
                            Device only                            94                   91                    94
                                                                                                                                                     Test material was open-set disyllabic
                                                                                                                                                     words presented at 60 dB sound
                         In noise
                            SNR +15 dB                             82                   73                    78                                     pressure level. Values are means,
                            SNR +10 dB                             83                   73                    78                                     with error bars indicating SEs. SNR
                            SNR +5 dB                              83                   74                    78                                     indicates signal to noise ratio.
                            SNR 0 bB                               83                   75                    78                                     a
                                                                                                                                                         Speech perception improved in
                                                                                                                                                         quiet between 6 and 12 months.

                  tests currently used in the elderly population to explore epi-                                   sis, each independent factor was tested and included in a mul-
                  sodic memory visuospatial abilities, attention span, speed of                                    tivariate model if P < .20. Backward selection was then per-
                  processing, mental flexibility, rule of compliance, and execu-                                   formed, keeping variables with a significance level of α = .05;
                  tive function: Mini-Mental State Examination (MMSE), 5-word                                      P < .05 was considered significant. All analyses were per-
                  test (FWT), clock-drawing test, verbal fluency test, d2 test of                                  formed using SAS, version 9.2 (SAS Institute Inc).
                  attention, and Trail Making Test parts A and B (TMT-A and
                  TMT-B) (descriptions of the tests and relevant references are
                  presented in the eMethods in the Supplement). Before test-
                  ing, written instructions were given to participants to avoid an
                                                                                                                   Results
                  overdiagnosis of cognitive impairment due to a misunder-                                         Auditory Rehabilitation
                  standing of the test procedure in this hearing-impaired popu-                                    Twelve months after cochlear implantation, 97% of the pa-
                  lation. Results of each test were expressed as normal or ab-                                     tients (n = 91) used their cochlear implant all day long. The 3%
                  normal with respect to the published normative data.                                             (3 of 94) who did not use it throughout the day wanted to save
                       Quality of life was assessed using the Nijmegen Cochlear                                    battery life. Fifty-seven percent of the patients (54 of 94) still
                  Implant Questionnaire (NCIQ)27 (eMethods in the Supple-                                          used their hearing aid in the contralateral, nonimplanted ear
                  ment). Depressive symptoms were evaluated using the 4-item                                       compared with 64% (60 of 94) before implantation (Fisher ex-
                  version of the Geriatric Depression Scale (GDS-4), which is a                                    act test, P = .46). Mean speech perception for disyllabic words
                  widely used validated questionnaire for the detection of these                                   in quiet and in noise are shown in Figure 1. In quiet, mean
                  symptoms.27,28                                                                                   speech perception clearly improved 6 months after cochlear
                                                                                                                   implantation compared with the preimplantation scores, both
                  Statistical Analysis                                                                             with the cochlear implant only (paired difference, 52% score
                  Patients’ characteristics and clinical data are reported as the                                  increase [95% CI, 45%-57%; P < .001]) and in best-aided con-
                  mean (SD) or median (first through third quartiles) for con-                                     ditions (paired difference, 42% [95% CI, 35%-49%; P < .001]).
                  tinuous variables and as percentages and 95% CIs for categori-                                   Between 6 and 12 months, speech perception scores contin-
                  cal variables. The χ2 and Fisher exact tests (for categorical vari-                              ued to improve with the cochlear implant alone (paired dif-
                  ables) and paired t test (for continuous variables) were                                         ference, 6% score increase [95% CI, 1%-10.3%; P = .02]) and in
                  computed to compare the audiologic, cognitive, and quality-                                      best-aided conditions (paired difference, 6.7% [95% CI, 2.05%-
                  of-life scores measured at the different time intervals. All com-                                11%; P = .005]). In noise, speech perception scores increased
                  parisons were 2-tailed, and the level of significance was set at                                 6 months after cochlear implantation compared with preim-
                  P < .05. The Spearman correlation coefficient was used to iden-                                  plantation scores at each SNR (SNR +15 dB: difference, 44%
                  tify and quantify relationships between NCIQ scores and speech                                   score increase [95% CI, 36%-52%; P < .001], SNR +10 dB: dif-
                  perception scores. For each variable of interest (cognitive                                      ference, 37% [95% CI, 30%-44%; P < .001], SNR +5 dB: differ-
                  scores), a univariate analysis followed by a multivariate analy-                                 ence, 27% [95% CI, 20%-33%; P < .001], and SNR 0 dB: differ-
                  sis was performed using a generalized linear model to ex-                                        ence, 18% [95% CI, 12%-25%; P < .001]). No further significant
                  plain the audiologic results (speech perception in quiet and                                     improvement was observed between 6 and 12 months. Speech
                  noise) at 12 months after implantation. For univariate analy-                                    perception scores at 12 months in quiet and in noise were simi-

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Research Original Investigation                                                                                               Cognitive Function After Cochlear Implantation

                                                                                                                   tation results are detailed in Figure 2B. Among the group of
               Figure 2. Cognitive Test Results Before and After Cochlear Implantation
                                                                                                                   50 patients with good cognitive abilities before implantation
                                                        No. of abnormal test results before implantation
                                                                                                                   (no or 1 abnormal test score), 24% (12 of 50) obtained poorer
                 No. of abnormal test results

                                                                                                                   results on cognitive tests 12 months after implantation. This
                  12 mo after implantation

                                                             0           1           2            3        Total
                                                                                                                   decline was slight, with only 1 test (2% [1 of 50 patients]) or 2
                                                 0          17           9           8            1         35
                                                                                                                   tests (4% [2 of 50]) becoming abnormal. In contrast, among the
                                                 1           6          12           6            5         29
                                                                                                                   group of 37 patients with 2 or 3 abnormal test scores before im-
                                                 2           0           4           5           10         19
                                                                                                  2         4
                                                                                                                   plantation, 81% (n = 30) obtained better results 12 months af-
                                                 3           0           2           0
                                                Total       23          27           19          18         87
                                                                                                                   ter implantation, and 19% (7) displayed stable scores. The per-
                                                                                                                   centage of patients with 2 and 3 abnormal tests at 12 months
                                                                                                                   after implantation was similar between patients aged 65 to 74
               Individual cognitive outcomes at 12 months plotted in relation to the data
                                                                                                                   years and those older than 75 years (26% and 31%, respec-
               obtained before cochlear implantation. Among the 91 patients who underwent
               the 6 cognitive tests before implantation, data were missing at 12 months after                     tively). The number of patients with abnormal cognitive scores
               implantation for 4 individuals: 3 patients with 2 abnormal test scores, and 1                       for each test is detailed in Table 1.
               patient with 1 abnormal test score before implantation. Tan shading indicates                            Table 2 summarizes the mean scores for each test before
               better cognitive results after implantation; light blue, unchanged results; and
                                                                                                                   and after cochlear implantation. In patients with abnormal test
               light orange, poorer results.
                                                                                                                   scores before implantation, paired t test analysis demon-
                                                                                                                   strated an improvement of cognitive performance on most
               lar between patients aged 65 to 74 years and those older than                                       tests. This improvement was significant as early as 6 months
               75 years (unpaired t test).                                                                         for the MMSE, the FWT, the d2 test of attention (speed), and
                    Before cochlear implantation, 23 of the 94 patients (22%)                                      the TMT-B, and became significant at 12 months for the TMT-A
               used the telephone only with familiar speakers. Twelve months                                       and the number of errors on the d2 test. Although the mean
               after cochlear implantation, 65% of the patients (n = 61) indi-                                     score for the clock-drawing test improved at 12 months, the dif-
               cated that they were able to use the telephone (P < .001, Fisher                                    ference was not significant, presumably because of the small
               exact test), and half of these could do so with unfamiliar speak-                                   number of patients with abnormal scores before implanta-
               ers. Sixty-one percent (37) of the 61 telephone users were fe-                                      tion (n = 4). In patients with normal cognitive performance be-
               male (P = .03, Fisher exact test).                                                                  fore implantation, scores for the MMSE, the number of errors
                                                                                                                   on the d2 test of attention, TMT-A, and TMT-B remained stable
               Cognitive Tests                                                                                     over time. We observed, however, a significant decline in re-
               Data for 91 of the 94 participants (97%) were included in the                                       sults of the FWT, a test that explores episodic anterograde
               data analysis: the interpretation of 2 tests was not possible for                                   memory, at 6 and 12 months. When evaluating verbal flu-
               1 patient with an unknown educational level, and 2 patients                                         ency, the lists of words (ie, names of animals, vegetables, and
               refused to continue with the evaluations after having abnor-                                        furniture) and letters (P, R, and V) were changed at each test
               mal scores on 3 tests; all 3 of these patients were withdrawn                                       session to avoid a learning effect from familiarity to the items
               from the cognitive study as a consequence. Before cochlear im-                                      used; consequently, comparison of the mean scores between
               plantation, 23 patients (25% of the population) obtained nor-                                       the preimplantation and postimplantation evaluations was not
               mal scores on all 6 cognitive tests, 28 patients (31%) had 1 ab-                                    possible because normative data differed according to each list.
               normal test score, 22 patients (24%) had 2 abnormal test scores,                                         To evaluate the influence of cognitive function on coch-
               and 18 patients (20%) had 3 abnormal test scores (Figure 2A).                                       lear implantation outcomes, all cognitive factors assessed in
               The mean age at implantation was similar between the groups                                         this study, which may have had an effect on speech percep-
               of patients with and without abnormal cognitive scores. Fur-                                        tion in quiet and in noise, were studied in a multivariate analy-
               thermore, no significant difference (P = .46) was observed in                                       sis 12 months after implantation. Performance on the verbal
               the proportion of each age group with 2 or 3 cognitive tests                                        fluency test for letters as test items was identified as the sole
               scores: 46% (31 of 68) of 64- to 75-year-old individuals and 46%                                    predictor of improvements in speech perception in noise (SNR
               (12 of 26) of those older than 75 years. Among the 91 patients                                      +15 dB, P = .01; SNR +10 dB, P < .001; and SNR +5 dB, P = .02).
               who completed preimplantation cognitive testing, 4 individu-                                        Moreover, no other significant difference in the mean speech
               als (4%) had missing data during the postimplantation test in-                                      perception scores at 12 months was observed between the 17
               tervals: 3 patients (3%) had only 6-month results, with all ob-                                     patients who had the poorest cognitive abilities (2 and 3 ab-
               taining higher scores at the 6-month interval, and 1 patient (1%)                                   normal test scores before and after implantation) and the 64
               who had 2 abnormal test scores before implantation com-                                             patients who obtained no or 1 abnormal cognitive test score
               pleted only the MMSE and the FWT at 12 months. Twelve                                               at 12 months (unpaired t tests).
               months after cochlear implantation, the percentage of 87 pa-
               tients with normal results of cognitive tests increased to 40%                                      Quality of Life and Depression
               (n = 35), the number of patients with 1 abnormal cognitive test                                     The NCIQ scores showed significant improvements in all 6
               remained stable at 33% (29 of 87), and the number of patients                                       subdomain scores at 6 months after implantation (basic
               with 2 and 3 tests with abnormal scores decreased to 22% (19                                        sound perception: difference, 27% score increase; [95% CI,
               of 87) and 5% (4 of 87), respectively (P = .001, χ2 test). Indi-                                    22%-33%; P < .001]; advanced sound perception: difference,
               vidual available cognitive outcomes in relation to preimplan-                                       14% [95% CI, 9%-19%; P < .001]; speech production: differ-

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Cognitive Function After Cochlear Implantation                                                                                             Original Investigation Research

                  Table 1. Abnormal Test Scores 12 Months After Cochlear Implantation in 94 Patients

                      Cognitive Test                                                                            No. (%) of Patientsa
                      (Missing Data                   Abnormal Scores            Abnormal Scores               Missing          Normal Scores               Abnormal Scores           Missing
                      at Baseline)                   Before Implantation        After Implantation              Data          Before Implantation          After Implantation          Data
                      MMSE (0)                               13 (14)                  3 (3)                      2                    81 (86)                      4 (4)                 2
                      5-Word test (0)                        22 (23)                10 (11)                      2                    72 (77)                     11 (12)                3
                      Clock-drawing test (0)                  4 (4)                  1 (1)                       1                    90 (96)                       0                    4
                      Fluency tests
                        Categories (2)                       10 (7)                  1 (1)                       0                    82 (89)                      2 (2)                 4
                        Letters (2)                           6 (7)                   0                          0                    86 (93)                      1 (1)                 4
                      d2 Test of attention
                        Errors (3)                           11 (12)                 1 (1)                       0                    80 (88)                      3 (3)                 4
                        Speed (3)                            39 (43)                14 (16)                      4                    52 (57)                     13 (13)                0
                      Trail Making Test
                        Part A (1)                           19 (20)                 5 (6)                       0                    74 (80)                      3 (3)                 4
                        Part B (3)                           23 (25)                 6 (7)                       2                    68 (75)                      5 (6)                 2

                  Abbreviation: MMSE, Mini-Mental State Examination.                                           possible. The d2 test of attention was also missing for this patient. Before
                  a
                      The percentages indicate the number of patients with normal and abnormal                 implantation, 2 patients did not complete all cognitive tests. After
                      scores among patients who performed the test before and after implantation.              implantation, cognitive data were missing for 4 patients (including 1 patient
                      Of 94 patients, educational level was unknown for 1 individual, so                       who did not complete all cognitive tests before implantation) and 1 patient
                      interpretation of the verbal fluency test and the Trail Making test was not              performed only the MMSE.

                  Table 2. Effect of Cochlear Implantation on Mean Cognitive Test Scores in 94 Patients
                                                 Before,                          6-mo                 Differences,              P          12-mo                  Differences,          P
                      Cognitive Test            Mean (SD)       Group (No.)a    Mean (SD)             Mean (95% CI)            Valueb      Mean (SD)              Mean (95% CI)        Valueb
                                               22.1 (3.4)       Abnormal (13)   25.8 (2.7)           3.7 (0.6 to 6.8)            .02       26.3 (2.7)        3.8 (1.0 to 6.6)            .01
                      MMSE
                                               27.8 (1.7)       Normal (81)     27.9 (1.8)        0.04 (−0.4 to 0.5)             .85        28 (1.8)         0.2 (−0.3 to 0.6)           .45
                                                8.2 (3.2)       Abnormal (22)    9.6 (0.1)           1.4 (0.5 to 2.3)            .004       9.4 (0.7)        1.3 (0.6 to 1.9)
Research Original Investigation                                                                                                  Cognitive Function After Cochlear Implantation

               Figure 3. Mean Scores of the 6 Subdomains of the Nijmegen Cochlear Implant Questionnaire (NCIQ)
               Before and After Cochlear Implantation

                                    100                            Before implantation    6 mo After implantation        12 mo After Implantation

                                    80
                 Mean NCIQ Scores

                                    60

                                                                                                                                                         Results are expressed as means, with
                                    40                                                                                                                   error bars indicating SD. Mean scores
                                                                                                                                                         in each subdomain ranged from 0
                                                                                                                                                         (very poor) to 100 (optimal).
                                    20
                                                                                                                                                         Individual scores at 6 months were
                                                                                                                                                         compared with preimplantation
                                     0
                                                                                                                                                         scores using paired t tests for all
                                          Basic Sound   Advanced Sound         Speech        Self-esteem            Activity             Social          subdomains (P < .001). Scores
                                          Perception      Perception         Production                                               Interaction        remained stable between 6 and 12
                                                                                                                                                         months.

                                                                                                                 A learning effect through repeated cognitive testing can-
               Discussion                                                                                   not be ruled out, especially for the tests including the clock-
                                                                                                            drawing test and FWT. In any case, scores were observed to
               Impact of Hearing Rehabilitation on Cognitive Functions                                      improve only for 2 patients for the clock-drawing task and de-
               This prospective study demonstrates that cochlear implanta-                                  creased for the FWT task. For verbal fluency tests, lists were
               tion improves speech perception in an elderly population in                                  changed at each session and other cognitive tests are clearly
               quiet and in noise at 6 months after implantation, which is con-                             too complex to be learned; therefore, it is unlikely that a test
               sistent with previously reported research.11-24 Speech percep-                               learning effect could influence the outcome of this study.
               tion continues to improve in quiet between 6 and 12 months,                                       To date, the effect of hearing rehabilitation on cognitive
               and was shown to remain stable for performance in noise af-                                  abilities has been studied only in patients fitted with hearing
               ter 6 months. At the same time, our study provides evidence                                  aids, with a beneficial effect reported in 3 of the 6 published
               that hearing rehabilitation using cochlear implantation is as-                               studies.5,7,8 Heterogeneity in the population and variability in
               sociated with an improvement in cognitive function in all cog-                               methodology across studies are likely to explain the discrep-
               nitive domains as early as 6 months after implantation in el-                                ancies in these results. In our work, despite variability in hear-
               derly patients who had abnormal test scores at baseline. More                                ing loss duration and in hearing aid use before implantation,
               than 80% of the patients (30 of 37) who had the poorest cog-                                 participants represent a homogeneous population character-
               nitive scores before implantation improved their cognitive                                   ized by a preimplantation, severe to profound sensorineural
               function at the 1-year postimplantation interval. In contrast,                               hearing loss, and a similar postimplantation auditory train-
               patients with the best cognitive performance before implan-                                  ing program.
               tation demonstrated stable results (≤1 abnormal test score), al-                                  The association between peripheral hearing loss and cog-
               though a slight decline was observed in 24% of the patients.                                 nitive decline and dementia has been well established in sev-
               Mean age at implantation was similar between patients with                                   eral cross-sectional and longitudinal studies.1,2,9,30-36 Lin36
               poorer cognitive test results and those with stable or better cog-                           showed that a greater level of hearing loss is significantly
               nitive test results. Results indicate that cochlear implanta-                                associated with lower scores on cognitive tests, especially for
               tion is associated with an improvement in impaired cognitive                                 memory and executive function, and concluded that the
               function early on but may not systematically prevent further                                 decline in cognitive performance associated with a 25-dB
               deterioration over time.                                                                     hearing loss is equivalent to the reduction associated with an
                    The effect of cognitive training in older adults has been de-                           older age difference of 7 years. Individuals having hearing
               bated in the literature,29 although, to our knowledge, never in-                             loss demonstrated a 30% to 40% accelerated rate of cognitive
               vestigated specifically in hearing-impaired patients. In the pres-                           decline and a 24% increased risk for incident cognitive
               ent study, we cannot rule out that improvement in cognitive                                  impairment during a 6-year period compared with partici-
               abilities could be affected by a combined effect of speech per-                              pants with normal hearing.9 Mechanisms underlying this
               ception improvement and cognitive training, the latter being                                 association are probably multifactorial. Some studies1-3 sug-
               an integral part of aural rehabilitation performed after coch-                               gest that hearing impairment and cognitive decline may
               lear implantation. A randomized clinical trial, aimed at addi-                               share a neurodegenerative process. Histologic changes
               tionally analyzing the cognitive benefit of cognitive training                               involved in central auditory dysfunction are unknown; none-
               with conventional amplification used prior to implantation,                                  theless, the association between central auditory dysfunction
               could assess the effect of speech therapy alone on cognitive                                 and executive dysfunction and dementia in elderly patients
               abilities in elderly patients with severe to profound hearing loss.                          supports this hypothesis.38,39 The evaluation of central audi-

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Cognitive Function After Cochlear Implantation                                                                                  Original Investigation Research

                  tory disorders was not possible in our cochlear implantation                      been clearly demonstrated in the elderly population.48-51 Con-
                  candidates because of the severity of the hearing loss; how-                      sequently, we examined, via multivariate analysis, whether
                  ever, with respect to the significant improvement for speech                      cognitive abilities before implantation can contribute to vari-
                  perception in noise after cochlear implantation, we can                           ability in cochlear implantation outcomes. We observed that
                  speculate that a central auditory dysfunction is unlikely for                     results for the verbal fluency test for letters, which evaluates
                  most of the patients included in this study.                                      long-term memory, was the only cognitive test that corre-
                       In hearing-impaired patients, the listening effort re-                       lated with speech perception scores in noise. Unexpectedly,
                  quired to improve communication leads to mental fatigue with                      neither attention deficit nor executive dysfunction showed a
                  a negative effect on cognitive resources being available for other                correlation with speech perception scores in noise. Very few
                  cognitive tasks, resulting in cognitive decline.22,39 Our results                 studies have evaluated the influence of cognitive factors in
                  suggest that, by improving hearing for verbal communica-                          adult cochlear implant recipients. Heydebrand et al52 found that
                  tion, cochlear implantation decreases the cognitive load and,                     better scores for word recognition in quiet were observed in
                  as a consequence, may have a positive effect on attention, con-                   adults with good verbal working memory and learning before
                  centration, and executive function.                                               implantation (mean age, 54 years; range, 24-80 years). Poorer
                       A socially active lifestyle can prevent cognitive decline in                 speech perception in quiet was observed 2 years after implan-
                  old age, suggesting that social isolation can be an additional                    tation in patients with lower cognitive scores.53 A key limita-
                  causal pathway for cognitive impairment.9,40 Hearing loss im-                     tion of our study is that working memory was not assessed,
                  pairs social relationships, leading to loneliness and degraded                    although it plays a major role in cases of degraded speech in-
                  quality of life in elderly persons.9,41,42 The findings of our study              formation and might account for the correlation between cog-
                  demonstrate an improvement in the NCIQ scores in each of its                      nition and speech perception scores in the aforementioned
                  subdomains as early as 6 months after implantation, corre-                        studies.51,52 Another limitation of the present study is that we
                  lated with the speech perception benefit in quiet and in noise                    applied basic tests used to evaluate cognitive function in the
                  at 12 months. Through these results, which are consistent with                    elderly population. Additional studies more precisely exam-
                  those of previous retrospective studies,15,20,25,43,44 we can hy-                 ining the role of specific cognitive factors involved in speech
                  pothesize that by improving verbal communication, cochlear                        perception in difficult conditions are needed. Finally, one of
                  implantation restores the possibility for social networking and,                  the selection criteria routinely used in the investigating clin-
                  as a consequence, has a positive effect on quality of life and                    ics for cochlear implantation was the absence of major cogni-
                  social activity that contributes to better cognitive function.                    tive impairment; indeed, cognitive problems, as well as low mo-
                       Although an association between hearing impairment and                       tivation, may influence the outcome of hearing rehabilitation.
                  depression in the elderly is still debated, depression has been
                  recognized as a major risk factor for mild cognitive impair-
                  ment and dementia.30,31,45,46 As a consequence, we can also
                  hypothesize that the reduction in depressive symptoms ob-
                                                                                                    Conclusions
                  served 12 months after implantation could contribute to the                       Epidemiologic studies54 demonstrate that the anticipated
                  improvement of cognitive abilities.                                               number of people aged 60 years or older will double by the
                       A limitation of our study is the short postimplantation ob-                  year 2050. As a consequence, the number of people with cog-
                  servation interval. A recent study47 reported that at 13.5 years                  nitive impairment and dementia will dramatically increase,
                  after implantation, 83% of elderly patients who received coch-                    reaching more than 100 million worldwide by 2050. Because
                  lear implants at age 60 years or older continued to use the im-                   there is no curative treatment available for cognitive decline,
                  plant consistently. In another study,23 elderly patients with uni-                clinical research is needed that focuses on identification of
                  lateral implants maintained their earlier speech perception                       risk factors to establish preventive measures that may reduce
                  ability in noise 10 years or more after receiving an implant. Fur-                the burden of the disease. Interventions that could delay
                  ther research is needed within our population to assess the                       dementia onset by 1 year, as well as its progression, would
                  long-term effect of cochlear implant use on cognitive abili-                      lead to a decrease of more than 9 million in the worldwide
                  ties, quality of life, and depression.                                            prevalence of dementia by 2050.55 Our study demonstrates
                                                                                                    that hearing rehabilitation using cochlear implants in the
                  Influence of Cognitive Factors                                                    elderly is associated with improvements in impaired cognitive
                  on Cochlear Implantation Outcomes                                                 function. Further research is needed to evaluate the long-
                  The role of cognitive processing in listening performance in                      term influence of hearing restoration on cognitive decline and
                  noise and hearing-aid benefit for speech perception tasks has                     its effect on public health.

                  ARTICLE INFORMATION                                  Author Affiliations: Assistance Publique-Hôpitaux       Bordeaux, France (Bebear); Service Oto-rhino-
                  Submitted for Publication: September 6, 2014;        de Paris, Groupe Hospitalier Pitié-Salpêtrière, Unité   laryngologie, Hôpital Purpan, Toulouse, France
                  final revision received December 5, 2014; accepted   Otologie, Implants Auditifs et Chirurgie de la base     (Marx, Fraysse); Service Oto-rhino-laryngologie,
                  December 17, 2014.                                   du crâne, Paris, France (Mosnier, Meyer, Bouccara,      Hôpital Gui de Chauliac, Montpellier, France
                                                                       Sterkers); Unité Mixte de Recherche-Sante, 1159         (Mondain, Sterkers-Artières); Service
                  Published Online: March 12, 2015.                    Inserm/Université Paris 6, Pierre et Marie Curie,       d’Audiophonologie, Institut Saint-Pierre, Palavas les
                  doi:10.1001/jamaoto.2015.129.                        France (Mosnier, Bouccara, Sterkers); Service           Flots, France (Sterkers-Artières); Service Oto-rhino-
                                                                       Oto-rhino-laryngologie, Hôpital Pellegrin,              laryngologie, Hôpital Hôtel Dieu, Nantes, France

                  jamaotolaryngology.com                                           (Reprinted) JAMA Otolaryngology–Head & Neck Surgery Published online March 12, 2015                 E7

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Research Original Investigation                                                                                           Cognitive Function After Cochlear Implantation

               (Bordure); Service Oto-rhino-laryngologie, Hôpital      3. Peelle JE, Troiani V, Grossman M, Wingfield A.            conceptual framework. J Am Geriatr Soc. 2012;60
               Bretonneau, Tours, France (Robier); Service Oto-        Hearing loss in older adults affects neural systems          (10):1936-1945.
               rhino-laryngologie, Hôpital Pontchailloux, Rennes,      supporting speech comprehension. J Neurosci.                 21. Lenarz M, Sönmez H, Joseph G, Büchner A,
               France (Godey); Assistance Publique-Hôpitaux de         2011;31(35):12638-12643.                                     Lenarz T. Cochlear implant performance in geriatric
               Paris, Service Oto-rhino-laryngologie et Centre de      4. Lin FR, Ferrucci L, An Y, et al. Association of           patients. Laryngoscope. 2012;122(6):1361-1365.
               réglage des implants cochléaires, Hôpital               hearing impairment with brain volume changes in
               Rothschild, Paris, France (Frachet, Poncet-Wallet).                                                                  22. Lin FR, Chien WW, Li L, Clarrett DM, Niparko JK,
                                                                       older adults. Neuroimage. 2014;90:84-92.                     Francis HW. Cochlear implantation in older adults.
               Author Contributions: Dr Mosnier had full access        5. Mulrow CD, Aguilar C, Endicott JE, et al.                 Medicine (Baltimore). 2012;91(5):229-241.
               to all the data in the study and takes responsibility   Quality-of-life changes and hearing impairment:
               for the integrity of the data and the accuracy of the                                                                23. Dillon MT, Buss E, Adunka MC, et al. Long-term
                                                                       a randomized trial. Ann Intern Med. 1990;113(3):             speech perception in elderly cochlear implant users.
               data analysis.                                          188-194.
               Study concept and design: Mosnier, Sterkers.                                                                         JAMA Otolaryngol Head Neck Surg. 2013;139(3):
               Acquisition, analysis, or interpretation of data:       6. Tesch-Römer C. Psychological effects of hearing           279-283.
               Mosnier, Bebear, Marx, Lina-Granade,                    aid use in older adults. J Gerontol B Psychol Sci Soc Sci.   24. Roberts DS, Lin HW, Herrmann BS, Lee DJ.
               Sterkers-Artières, Bordure, Robier, Godey, Meyer,       1997;52(3):127-138.                                          Differential cochlear implant outcomes in older
               Poncet-Wallet, Sterkers.                                7. Acar B, Yurekli MF, Babademez MA, Karabulut H,            adults. Laryngoscope. 2013;123(8):1952-1956.
               Drafting of the manuscript: Mosnier.                    Karasen RM. Effects of hearing aids on cognitive             25. Olze H, Gräbel S, Förster U, et al. Elderly
               Critical revision of the manuscript for important       functions and depressive signs in elderly people.            patients benefit from cochlear implantation
               intellectual content: Mosnier, Bebear, Marx, Fraysse,   Arch Gerontol Geriatr. 2011;52(3):250-252.                   regarding auditory rehabilitation, quality of life,
               Truy, Mondain, Bordure, Robier, Godey, Meyer,           8. Choi AY, Shim HJ, Lee SH, Yoon SW, Joo EJ. Is             tinnitus, and stress. Laryngoscope. 2012;122(1):196-
               Frachet, Bouccara, Sterkers.                            cognitive function in adults with hearing                    203.
               Statistical analysis: Mosnier.                          impairment improved by the use of hearing AIDS?
               Administrative, technical, or material support:                                                                      26. Fournier JE. Audiométrie vocale, les épreuves
                                                                       Clin Exp Otorhinolaryngol. 2011;4(2):72-76.                  d'intelligibilité et leurs applications au diagnostic, à
               Mosnier, Bebear, Fraysse, Truy, Mondain, Bordure,
               Robier, Godey, Meyer, Frachet.                          9. Lin FR, Yaffe K, Xia J, et al; Health ABC Study           l'expertise et à la correction prothétique des
               Study supervision: Mosnier.                             Group. Hearing loss and cognitive decline in older           surdités. Paris, France: éditions Maloine; 1951.
                                                                       adults. JAMA Intern Med. 2013;173(4):293-299.                27. Hinderink JB, Krabbe PFM, Van Den Broek P.
               Conflict of Interest Disclosures: None reported.
                                                                       10. van Hooren SA, Anteunis LJ, Valentijn SA, et al.         Development and application of a health-related
               Funding/Support: This work was equally funded by        Does cognitive function in older adults with hearing         quality-of-life instrument for adults with cochlear
               Advanced Bionics AG, Cochlear France, Vibrant Medel     impairment improve by hearing aid use? Int J Audiol.         implants: the Nijmegen cochlear implant
               Hearing Technology, and Oticon Medical/Neurelec.        2005;44(5):265-271.                                          questionnaire. Otolaryngol Head Neck Surg. 2000;
               Role of the Funder/Sponsor: The funding                 11. Carlson ML, Breen JT, Gifford RH, et al. Cochlear        123(6):756-765.
               organizations had no role in the design and conduct     implantation in the octogenarian and                         28. Clement JP, Fray E, Paycin S, Leger JM, Therme
               of the study; collection, management, analysis, and     nonagenarian. Otol Neurotol. 2010;31(8):1343-1349.           JF, Dumont D. Detection of depression in elderly
               interpretation of the data; preparation, review, or                                                                  hospitalized patients in emergency wards in France
               approval of the manuscript; and decision to submit      12. Williamson RA, Pytynia K, Oghalai JS, Vrabec JT.
                                                                       Auditory performance after cochlear implantation             using the CES-D and the mini-GDS: preliminary
               the manuscript for publication.                                                                                      experiences. Int J Geriatr Psychiatry. 1999;14(5):
                                                                       in late septuagenarians and octogenarians. Otol
               Previous Presentations: Some part of this content       Neurotol. 2009;30(7):916-920.                                373-378.
               was presented orally at the 12th International                                                                       29. Willis SL, Tennstedt SL, Marsiske M, et al;
               Conference on Cochlear Implants and other               13. Chatelin V, Kim EJ, Driscoll C, et al. Cochlear
                                                                       implant outcomes in the elderly. Otol Neurotol.              ACTIVE Study Group. Long-term effects of
               implantable auditory technologies, Baltimore,                                                                        cognitive training on everyday functional outcomes
               Maryland; May 4, 2012; at the 13th International        2004;25(3):298-301.
                                                                                                                                    in older adults. JAMA. 2006;296(23):2805-2814.
               Conference on Cochlear Implants and Other               14. Sterkers O, Mosnier I, Ambert-Dahan E,
               Implantable Auditory Technologies; June 18, 2014;       Herelle-Dupuy E, Bozorg-Grayeli A, Bouccara D.               30. Cacciatore F, Napoli C, Abete P, Marciano E,
               Munich, Germany; at the Cochlear Science and            Cochlear implants in elderly people: preliminary             Triassi M, Rengo F. Quality of life determinants and
               Research Seminar on Aging and Implantable               results. Acta Otolaryngol Suppl. 2004;552(552):64-           hearing function in an elderly population:
               Solutions; March 19, 2012; Paris, France; at the        67.                                                          Osservatorio Geriatrico Campano Study Group.
               international MED-EL Workshop on Hearing                                                                             Gerontology. 1999;45(6):323-328.
                                                                       15. Vermeire K, Brokx JP, Wuyts FL, Cochet E,
               Implants for Older Adults; January 16, 2014; New        Hofkens A, Van de Heyning PH. Quality-of-life                31. Naramura H, Nakanishi N, Tatara K, Ishiyama M,
               York, New York; and at the Cochlear Science and         benefit from cochlear implantation in the elderly.           Shiraishi H, Yamamoto A. Physical and mental
               Research Seminar on Aging and Implantable               Otol Neurotol. 2005;26(2):188-195.                           correlates of hearing impairment in the elderly in
               Solutions; June 17, 2014; Munich, Germany.                                                                           Japan. Audiology. 1999;38(1):24-29.
                                                                       16. Leung J, Wang NY, Yeagle JD, et al. Predictive
               Additional Contributions: Amandine Giroux, MS,          models for cochlear implantation in elderly                  32. Mitchell AJ, Bird V, Rizzo M, Meader N. Which
               assisted in the analysis of cognition tests, Blandine   candidates. Arch Otolaryngol Head Neck Surg.                 version of the geriatric depression scale is most
               Pasquet MS (Unité de Recherche Clinique Nord,           2005;131(12):1049-1054.                                      useful in medical settings and nursing homes?
               Groupe Hospitalier Bichat-Claude Bernard, Paris,                                                                     diagnostic validity meta-analysis. Am J Geriatr
               France), assisted with statistical analysis, Evelyne    17. Eshraghi AA, Rodriguez M, Balkany TJ, et al.             Psychiatry. 2010;18(12):1066-1077.
               Ferrary, MD, PhD (Unité Mixte de Recherche-SII59,       Cochlear implant surgery in patients more than
                                                                       seventy-nine years old. Laryngoscope. 2009;119(6):           33. Uhlmann RF, Larson EB, Rees TS, Koepsell TD,
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               Médical Luxembourg, Paris), provided continuing         performance in elderly patients. Arch Otolaryngol            34. Valentijn SA, van Boxtel MP, van Hooren SA,
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                                                                                                                                    change in cognitive functioning: results from a
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