Improvement of Cognitive Function After Cochlear Implantation in Elderly Patients
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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). (Reprinted) E1 Copyright 2015 American Medical Association. All rights reserved. Downloaded From: http://archotol.jamanetwork.com/ by Lisa Taylor on 03/16/2015
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 Copyright 2015 American Medical Association. All rights reserved. Downloaded From: http://archotol.jamanetwork.com/ by Lisa Taylor on 03/16/2015
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- jamaotolaryngology.com (Reprinted) JAMA Otolaryngology–Head & Neck Surgery Published online March 12, 2015 E3 Copyright 2015 American Medical Association. All rights reserved. Downloaded From: http://archotol.jamanetwork.com/ by Lisa Taylor on 03/16/2015
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- E4 JAMA Otolaryngology–Head & Neck Surgery Published online March 12, 2015 (Reprinted) jamaotolaryngology.com Copyright 2015 American Medical Association. All rights reserved. Downloaded From: http://archotol.jamanetwork.com/ by Lisa Taylor on 03/16/2015
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- E6 JAMA Otolaryngology–Head & Neck Surgery Published online March 12, 2015 (Reprinted) jamaotolaryngology.com Copyright 2015 American Medical Association. All rights reserved. Downloaded From: http://archotol.jamanetwork.com/ by Lisa Taylor on 03/16/2015
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 Copyright 2015 American Medical Association. All rights reserved. Downloaded From: http://archotol.jamanetwork.com/ by Lisa Taylor on 03/16/2015
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? 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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, INSERM 1, Université Paris 6 Pierre et Marie Curie), Duckert LG. Relationship of hearing impairment to provided helpful comments during manuscript 1180-1183. dementia and cognitive dysfunction in older adults. preparation, and Arach Madjlessi, MD (Service de 18. Friedland DR, Runge-Samuelson C, Baig H, JAMA. 1989;261(13):1916-1919. Gériatrie Aiguë Clinique Alleray Labrouste et Centre Jensen J. Case-control analysis of cochlear implant Médical Luxembourg, Paris), provided continuing performance in elderly patients. Arch Otolaryngol 34. Valentijn SA, van Boxtel MP, van Hooren SA, support. No financial reimbursement was provided. Head Neck Surg. 2010;136(5):432-438. et al. Change in sensory functioning predicts change in cognitive functioning: results from a 19. 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