Ethics approval for this study was obtained from The University of Western Australia Human Research Ethics Committee (RA/4/1/7368). All participants provided informed, signed consent forms before participation in the study.
All participants completed a test battery consisting of hearing, speech perception in quiet, and a psychological and a cognitive assessment. CIC completed testing at the baseline, 6 and 12 months while waiting to receive a CI. CIR completed the assessments at the baseline (preop), 6 and 12 months postimplantation.
This was conducted in a soundproof booth by a qualified audiologist. The CIC participants completed a standard unaided pure-tone audiometric (Equinox 2.0 clinical audiometer; Interacoustics A/S, Middelfart, Denmark) and aided free field speech in quiet (consonant–nucleus consonant [CNC] word and phoneme (21) and City University of New York [CUNY] sentence test (22)) assessments with optimized hearing aids at the baseline, 6 and 12 months. Similar to the CIC group, CIR participants also completed unaided pure-tone audiometric assessment and aided free-field speech assessments at the baseline with optimized hearing aids. The CIR participants completed aided free field pure-tone audiometric (Tables 1 and 3) and speech assessments (Table 1—supplementary materials, http://links.lww.com/MAO/A533) with their CI at 6 and 12 months postimplantation.
All three participant groups completed a nonverbal cognitive assessment using the CANTAB (20) installed on a computer with an integrated touch screen (Dell, Inspiron One, with Windows 8.1 platform). Before the cognitive assessment, all participants completed a National Adult Reading Test-Revised (23). The National Adult Reading Test-Revised score was used to calculate premorbid IQ. The following cognitive functions were assessed: cognitive flexibility (Attention Switching Task [AST]), delayed matching to sample, episodic memory and new learning skills (Paired-Associate Learning [PAL]), verbal recognition memory-free recall and recognition in immediate and delayed conditions (Verbal Recognition Memory [VRM]), reaction time-simple and complex (Reaction Time [RTI]), and working memory and executive functions (Spatial Working Memory [SWM]).
- Motor Screening Task (MOT): A brief introductory exercise was used to familiarize participants with the touch screen interface. MOT identifies difficulties in vision, comprehension, and hand movement of the participant (20). Results of MOT were not analyzed as part of the outcome measures for this study but were used as a screening tool to identify potential difficulties for the participant.
- AST: AST is a test of executive functioning and provides a measure of cued attentional set shifting. This activity specifically assesses cognitive flexibility and multitasking capabilities (20). AST is reported to be mediated by prefrontal cortex (24).
- DMS: This task assesses participants’ ability to recognize complex visual patterns at different time intervals (20). This test is sensitive to the damages in the medial-temporal lobe (hippocampus) and frontal lobes (25).
- PAL: PAL is a recall test of memory in which the participant has to learn the location of specific visual patterns (20). This test is sensitive to temporal and parietal lobe dysfunction (26).
- VRM: VRM assesses immediate and delayed memory of verbal information under free recall and forced recognition conditions (20). During this task, the participants were asked to read out loud a list of 12 words that appeared on the computer screen and remember the words at the same time. Then, participants were asked to recall as many words as they could (free recall stage) and to identify the original 12 words from a list containing the original words and distractors (recognition phase). The recall phase of VRM activates areas of the fronto-temporal network,(27) whereas the recognition phase activates the hippocampus (28).
- RTI: RTI is a test of attention and measures the speed of response and movement in single and five choice paradigm. During this task, the participants are required to release a home button and touch either a single stimulus or one of five stimuli that appears on the test screen. Outcome measures include reaction time (time taken to release the home button) and movement latencies (time taken to release the home button and to touch the screen) for both simple and five-choice conditions (20).
- SWM: It measures the retention and manipulation of visuospatial information in areas such as nonverbal working memory, working visuospatial memory, and strategy use is assessed (20). SWM is sensitive to the functions of prefrontal cortex (29,30).
More details of these tests can be found at http://www.cambridgecognition.com/clinicaltrials/cantabsolutions/tests.
Depression Anxiety Stress Scale-21(DASS-21(31))
The DASS-21 was used to measure the current (past 7 days) severity of a range of symptoms common to depression, stress, and anxiety. The DASS-21 contains 21 questions that are scored on a four-point Likert scale ranging from 0 (never apply to me at all over the last week) to 3 (applied to me very much or almost always over the past week). Scores for Depression, Anxiety, and Stress were separately calculated by summing the scores for the relevant items and the final score for each subcategory was multiplied by two (×2) as per the questionnaire scoring instructions.
Analysis was performed with IBM SPSS Statistics version 22 (IBM Corp, New York, NY). Independent-sample t tests were conducted to determine if the differences in CANTAB test modules scores and DASS-21 questionnaire scores between baseline and 6 months, and between baseline and12 months obtained for were significantly different between the CIC and CIR groups.
At the baseline, partial correlation was performed to investigate the correlation between baseline 4PTA of the implanted or the ear selected for CI surgery, duration of hearing loss and CANTAB and DASS-21 test scores of the CI candidates and recipients. Partial correlation was also performed on a CIR group to investigate the correlation between 4PTA of the implanted ear, aided speech-perception scores and CANTAB and DASS-21 scores 12 months postimplantation. Age, and premorbid IQ scores were controlled during this analysis.
Independent-sample t test results obtained for the changes observed between baseline and 6 months revealed a significant difference between both participant groups for RTI simple reaction time (p = 0.01), SWM between errors (p = 0.02], and SWM between errors four to eight boxes (p = 0.04] tasks (Table 2).
Differences observed between baseline and 12 months revealed a significant difference between the CIR and CIC groups for AST mean latency (p = 0.04), PAL total errors (p = 0.03), RTI simple accuracy score (p = 0.03), SWM between errors (p = 0.03), SWM between errors four to eight boxes (p = 0.05) and SWM strategy (p = 0.02) tasks.
In comparison with the implant candidates, the CIR group showed a significant decline in stress scores between baseline to 12 months (p = 0.02] postimplantation (Table 3, Fig. 1). Over time we have observed a trend in decline in depression, anxiety, and stress scores of the CIR group. However, two CIR participants have gone through life changing events that had negative impact on their mental health which was reflected in their DASS-21 scores (Table 2—supplementary materials, http://links.lww.com/MAO/A534). The CIC group showed a trend in increase in depression, anxiety, and stress scores over time. However, there were no significant changes in anxiety and depression for either group.
Partial correlation analysis results revealed that duration of hearing loss positively correlated with baseline AST mean correct latency (r = 0.37, p = 0.02) and baseline SWM between errors (r = 0.36, p = 0.02) scores.
Twelve-months postimplantation, CUNY sentence scores negatively correlated with AST mean correct latency (r = −0.75, p = 0.02) and CNC-words scores negatively correlated with SWM strategy scores (r = −0.74, p = 0.03).
This study investigated the impact of cochlear implantation on cognitive functions and mental health of postlingually hearing impaired CI recipients. It revealed that 6 months postimplantation, CI recipients showed a significant improvement in spatial working memory and strategy use (SWM) and simple RTI tasks. Twelve months of CI use had a positive impact on cognitive flexibility (AST), PAL, alongside SWM and strategy use and simple RTI tasks consistent with the 6-month findings.
Simple RTI is a measure of attention and processing speed. It measures speed of response and movement in single and five-choice paradigms (20). Processing speed, attention, working memory, and executive functions decline with age (4) and contribute to difficulties in speech understanding in older adults (32). Increase in RTI accuracy scores observed in the CIR group may be attributed to the fact that the improved hearing may have assisted in reducing the cognitive load, and therefore improving information processing speed. RTI is considered the primary cognitive ability underlying more complex cognitive abilities, including executive functioning and working memory (4).
AST is a test of executive functioning and provides a measure of cued attentional set shifting (20). The correlation analysis results of the current study revealed that duration of hearing loss positively correlates with the AST mean latency at the baseline. This suggests that the longer the duration of hearing loss, the greater the time required to rapidly switch attention between auditory objects. These findings are consistent with Shinn–Cunnigham's (33) findings that hearing loss impairs one's ability to switch attention rapidly by increasing the time required to form auditory objects. It is posited that the improvement observed in postimplantation speech perception scores may have facilitated improved attention.
Studies suggest that the PAL is affected by temporal lobe damage in humans (34). Positron emission tomography studies conducted on CI recipients have observed cortical activation in the temporal lobe regardless of the side of the implantation. In addition, a positive correlation has been observed between the degree of cortical activation and speech therapy (35). The results of the current study showed a significant improvement in PAL total errors (p = 0.03). In light of the improved postimplantation speech scores observed in the CIR group (Table 1), we posit that these changes could have helped improve PAL error scores.
The SWM test assesses visuospatial working memory and strategy use (20). It is also sensitive to executive functions (20). SWM is influenced by pathological conditions in the frontal lobe, especially dorsolateral and ventrolateral areas (29). The dorsolateral prefrontal cortex is involved in executive functions, such as the maintenance and manipulation of items in working memory (36). Working memory is defined as a “limited capacity system for temporarily storing and processing the information required to carry out complex cognitive tasks such as comprehension, learning, and reasoning” (Rönnberg et al. (37), p. 2). Preimplantation, the CI recipients of this study had severe-profound hearing loss and performed poorly in speech perception in quiet in optimally aided condition. Existing research suggests a role of working memory in speech understanding (38). CI recipients’ reliance on working memory and strategy use and executive functions to understand speech signal was reflected in reduced SWM error scores and improved strategy use, postimplantation.
A review of existing literature has revealed that to date only a handful of studies have examined the impact of cochlear implantation on cognitive functions of older adults (8,39–41). All of these studies have used cognitive assessments with verbal test materials and some also included cognitive assessments with written and pictorial information. Holden et al. (8) reported that when age, sex, and ethnicity were controlled, duration of severe-profound hearing loss remained significantly correlated with the cognitive standardised data (ρs = −0.206, p = 0.028). Collison et al. (40) failed to find any significant correlation between cognitive and linguistic test scores and word recognition abilities. Even though Heydebrand et al. (41) failed to observe significant improvement in postimplant speech perception scores and general cognitive scores, verbal learning could account for 42% of the variance in 6-month postimplant monosyllabic word scores. Mosnier et al. (42) also reported an improvement in mean scores of all cognitive domains as measured by MMSE, five-word test, clock-drawing test, verbal fluency test, d2 test of attention, and Trail Making Test parts A and B as early as 6 months postimplantation. Our findings are in line with both Heydebrand et al. (41) and Mosnier et al. (42) in that we observed significantly negative correlation between 12 months postimplantation CUNY sentence scores and AST mean correct latency (r = −0.75, p = 0.02) and CNC-words scores and SWM strategy scores (r = −0.74, p = 0.03).
Postimplantation, CI recipients have shown baseline to 12 months postop improvement in mean hearing thresholds (64 dB), mean speech in quiet (68% in CUNY sentences, 32% in CNC-Word, 50% in CNC-Phoneme scores) tasks. These findings are consistent with previous studies that examined the improvement in speech perception in quiet (8,42,43) in older adults. All CI recipients scored between 23.75 dB and 40 dBHL for their postop 4PTA in the implanted ear, suggesting that all CI recipients had access to sound with a well-fitted CI. Cochlear implantation seems to reduce cognitive load by improving speech perception abilities of the implant recipients (42). Further, based on significant decline in stress scores observed in implant recipients compared with the implant candidates, we posit that access to better hearing could have a positive impact on mental health of hearing impaired older adults.
As mentioned above, all the participants in the current study were selected as suitable candidates for cochlear implantation by the established hearing loss and poor aided speech perception criteria (6). Subsequently, a number of these participants received a CI. The CIR group included only those who were implanted at the start of the 12 month data collecting phase. The remainder were not implanted over the 12-month period, and became the CIC group. Any participant who was initially included in the CIC group and was subsequently implanted after several months during the study was excluded. We commenced by assuming that both the groups were comparative and the CIC group were not significantly different to the CIR group in cognitive and psychological measures. During the waiting period, those candidates who had optimized hearing aids continued to use them.
The results of the current study suggest that significantly better results observed in working memory and strategy use, cognitive flexibility and attention, paired associate learning and simple reaction time tasks of CI recipients compared with CI candidates, could reflect lesser cognitive load imposed on working memory and executive functions due to improved postimplantation hearing and speech perception scores.
The small sample size in this study is a limitation. Despite this study measuring changes in some cognitive functions, these may require a longer period of time to confirm that these are sustained, and other cognitive functions may need a longer period of time to occur. A longitudinal assessment with a large sample size may provide further information regarding what other cognitive functions are improved/not improved as a function of cochlear implantation.
The authors thank Dr Peter Busby and Prof Robert Eikelboom for reviewing the manuscript.
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Anxiety; Cochlear implantation; Cognition; Depression; Hearing loss; Stress
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