1. Introduction
By 2050, the number of people affected by dementia is predicted to double to over 131 million [
1]. In addition to the development of pharmacological preventions or treatments for dementia, modifiable risk factors need to be examined and addressed. Age-related hearing loss (hearing thresholds greater than 25 dB HL; [
2]) is highly prevalent in older adults from middle age, with a doubling of incidence reported with each decade [
3]. The incidence of reported hearing loss ranges from 30%–60% for people aged over 65 years to 70%–90% over 85 years [
4,
5,
6]. Hearing loss is associated with many co-morbidities, including poorer physical health, anxiety, depression, loneliness and isolation [
7,
8,
9,
10]. Despite its high prevalence and significant negative impact on quality of life and burden to society, hearing loss is undertreated. A recent report in the U.S showed only one in seven adults aged 50 and older used hearing aids, with fewer than 1 in 20 working adults aged 50–70 years doing so [
11].
A number of individual studies and meta-analyses have reported an association between hearing loss, cognitive decline and dementia, with both peripheral hearing loss and central auditory dysfunction associated with accelerated risks of cognitive decline and incident dementia (e.g., [
12,
13,
14,
15]). Hearing loss has recently been recognized as a risk factor for dementia and is estimated to account for up to 9.1% of the modifiable risk for this disease [
16]. While most studies to date have focused on the association between hearing loss and cognitive decline in older adults, two recent population-based cohort studies have reported that people with the highest dementia risk were adults with the onset of hearing loss in middle age. The first of these studies reported an increased rate of dementia diagnosis before age 60 with mid-life hearing loss (adjusted hazard ratio = 1.90; [
17]), while the second study observed that the strongest association between hearing loss and dementia was for adults with hearing loss diagnosed between 45 and 64 years (hazard ratio = 1.40 for incident dementia; [
18]). The findings of these recent studies support the position of the Lancet Commissions [
16] that the increased risk of cognitive decline associated with hearing loss does not only apply to older adults (50–70 years), and that the strongest midlife risk factor for dementia is hearing loss.
Although two-thirds of dementia risk has been identified as genetic, it is estimated that over one-third of dementia cases may be preventable through lifestyle measures such as improved education, reduced smoking and the management of hearing loss, diabetes and obesity [
16]. Given the reduced quality of life and other costs for affected individuals and their families, as well as the significant financial burden for society, if the onset of functional impairment could even be delayed by only a few years for some people, this would be a significant achievement. Given the association between hearing loss and increased rate of cognitive decline, there has been developing interest in whether the remediation of hearing loss could mediate the observed risk of accelerated cognitive decline for adults with hearing loss. However, the effect of hearing aid use on cognition is still unclear, as reports to date of the effects of hearing aid use have yielded mixed results. Although some cross-sectional cohort studies have reported either improved cognition from baseline or a slower rate of decline with hearing aid use [
13,
19,
20,
21,
22], others have found no significant effect [
20,
23,
24]. Further, a narrative review concluded that although hearing aid use could impact immediate cognitive function, there was no evidence long-term usage affected long-term cognition [
25]. However, the first systematic review and meta-analysis of 30 studies (including 40 samples) concluded that while people with hearing loss had poorer cognition overall when compared to those with normal hearing, those who used hearing aids had better cognition than those who remained untreated [
12]. It is important to note, however, that although the size of the difference in cognitive performance was less than half in treated versus untreated samples, this effect was based on data from only four studies, with evidence of publication bias. It was suggested that after adjusting for publication bias, the effect size found may in fact have been closer to half of the original effect size (0.23). Further, the conclusion that cognition was better for treated versus untreated people was based on the results of only three studies.
While the overall conclusion of the meta-analysis of research regarding the effects of hearing aid use on cognition was that treatment of hearing loss appeared to improve cognition [
12], it was noted by the authors that methodological limitations in the published research to date do not allow for conclusions about whether the relationship between hearing loss and cognitive decline is causal. Limitations in the current literature include small sample size, retrospective design, and self-report of hearing loss and/or hearing aid use (often a single question), with no measurement of either hearing aid benefit or frequency of use [
5,
13,
19]. If hearing loss was measured objectively at baseline, which was frequently not the case, further changes in hearing were not assessed over time. Other factors known to affect cognition such as education, social participation, mood, exercise, and diet were also not considered in some studies. With regard to cognition, further limitations include limited assessment of cognitive abilities, for example through the use of bedside dementia rating instruments, which are insensitive, or only one cognitive task assessed, and/or assessments administered using verbal instructions, which introduces a confounding factor for people with hearing loss, who are disadvantaged even with mild-moderate loss [
5,
21,
26]. Finally, a further factor that has received limited attention is sex. There is currently no consensus regarding the influence of sex on the incidence of dementia, with contradictory evidence of dementia risk for females versus males [
27]. Given the reported differences in the incidence of clinical sub-types of cognitive impairment, the greater effect of the apoloipoprotein APOE E4 allele on dementia risk for females, and the fact that education, an established risk factor for dementia, is often lower for females, it has been recommended that the investigation of risk factors for cognitive decline should be conducted separately for males and females [
28]. In summary, for many studies, information about change in cognitive function and the rate of such change over time was not available. The same limitation applies to change in hearing loss, with a particular lack of information about benefits from hearing aids and frequency of device use. Without this information it is not possible to examine the relation between the rate of decline in hearing and rate of cognitive decline. Without information about frequency of device use and benefit, it is not possible to know whether the treatment is effective, and therefore what the effect, if any, on cognition would be. The effects of treatment of hearing loss with hearing aids have not yet been examined in a comprehensive study that objectively assesses both hearing loss and benefits of hearing aid use over time, controlling for the effects of other factors associated with cognitive decline. Although a randomized control trial is always going to be the preferred option in terms of study design, this is not feasible for a study including people with significant hearing loss; given the significant adverse effects of greater than mild hearing loss, it is not ethical to deny treatment.
The current study examined cognition over time in a prospectively recruited cohort of older adults with hearing loss in Australia who were first time users of hearing aids. Preliminary results at 18 months in a study which will follow participants for a long time interval are presented. Gold standard audiological hearing assessments were conducted prior to hearing aid fitting and at the first follow-up interval of 18 months, and cognitive function was measured using a computerized tool and visual instructions only. Hearing aid use and both objective and subjective benefits of treatment (speech perception and ease of listening) were also assessed. Data for other factors likely to influence cognition, such as physical health, social isolation, loneliness, mood, exercise, quality of life and sex were assessed so that their effects on cognition could be considered in the analysis. When ongoing data collection in a healthy aging comparison group of older Australians with typical hearing for their age yields a sample size large enough for meaningful comparison, cognitive and other outcomes will be compared between the hearing aid users and the group who are representative of Australian older adults. The present study investigated the relationship between degree of hearing loss and the extent of cognitive impairment prior to hearing aid fitting. The effect of hearing aid use over time on cognition was also examined, in addition to the effects of hearing aid use on quality of life. This longitudinal study will provide the most rigorous and expansive evidence to date of the effects of hearing aid use on cognition for older adults with hearing loss.
2. Experimental Section
2.1. Procedures
This study was carried out in accordance with the recommendations of the Australian National Health and Medical Research Council guidelines for ethical research conduct. The study protocol was approved by the University of Melbourne Behavioural and Social Sciences Human Ethics Sub-Committee (Ethics ID: 1646925). All participants gave written informed consent in accordance with the Declaration of Helsinki.
2.2. Participants
Ninety-nine adults aged 60–84 years, with hearing loss (mean better ear Pure Tone Average of 0.5, 1, 2 and 4 KHz of 31 dB) and no previously diagnosed or suspected cognitive impairment, participated in this study. Seventy-one percent of participants were retired, and 67% had postgraduate tertiary education. Participants had sufficient English to be able to give informed consent, comprehend test instructions and complete questionnaires. The participants were all clients of the University of Melbourne Academic Hearing Aids Clinic and had been identified as suitable to proceed with hearing aid fitting at the time of recruitment.
Table 1 shows participant audiometric and demographic information.
All participants completed a pre-operative (baseline) assessment battery comprising audiometry, speech perception testing, cognitive screening and assessment, and health, quality of life, lifestyle and ease of listening questionnaires. A subset of participants assessed at the 18 month post-operative point completed an identical assessment battery and reported on their hearing aid use.
2.3. Audiological Assessment
Participants were assessed at baseline by an audiologist in a sound-proof booth, as part of the standard clinical pre-fitting workup. Hearing aids were chosen during a needs discussion with participants based on type and degree of hearing loss, personal aesthetic and technological preferences and communication needs. The NAL-NL2 prescription [
29] was used for all hearing aid fitting unless clients preferred otherwise. All fittings were verified with real ear insertion gain measures using the Interacoustics Affinity AC440 module and adjusted to optimize individual preferences and listening comfort. Participants attended a review appointment within two to four weeks after fitting, with further review appointments made as necessary. All participants returned for a routine 12 month follow up appointment with their managing clinician. They were evaluated again 18 months after their initial hearing aid fitting by a research team audiologist. Audiometric assessment included air and bone conduction thresholds, speech discrimination assessment, and tympanometry. Speech perception ability was assessed using both word and sentence level materials. Consonant-vowel-consonant (CVC) monosyllabic words (50 word lists; scored for words and phonemes correct) were presented at 65 dB SPL in quiet in the left ear, right ear and binaurally in the unaided condition at baseline and in the best aided condition for participants who were assessed 18 months after hearing aid fitting. Speech Reception Threshold testing (SRT) was conducted using 20 Bamford-Kowal-Bench-like sentence lists in four-talker babble background noise. The test sentence was presented at 65 dB SPL, while the noise level was adaptive; the noise level was altered depending on the score achieved for each sentence. Both the target sentence and background noise were presented 1 m in front of the participant via a single speaker in the free field. The non-test ear was masked in the unilateral listening conditions using white noise set at 30 dB above the average of the 1 and 2 kHz thresholds. Correctly repeated target words were scored for each sentence, and the mean performance score in signal to noise ratio was used to calculate the participants’ ability to perceive speech in noise for the right ear, left ear and binaurally, with the final score reflecting the signal-to-noise ratio at which 50% of the key words were correctly identified.
2.4. Cognitive Assessment
Screening for dementia prior to commencing in the study was conducted using the Mini Mental State Examination (MMSE; [
30]), a brief bedside dementia assessment. In accordance with the current (2011) National Institute for Health and Care Excellence (NICE) guidelines, a cut-off score of 24/30 was used to identify people with cognitive impairment.
Cognition in this study was assessed using five subtests from the CogState Cognitive Battery [
31,
32,
33,
34]. These included assessments of psychomotor function (Detection test), attention (Identification test), working memory (One Back Test), visual learning (One Card Learning test) and executive function (Groton Maze Learning test). Cognitive assessments were administered by trained audiologists both pre- and 18 months post-hearing aid fitting. The CogState Battery is a computerized test battery developed for repeated assessment of cognitive performance. The battery is highly reliable (test-retest reliability for each measure ranges between 0.84 and 0.94), facilitates minimal practice effects [
31], and is relatively quick to administer (approx. 30 min, depending on ability). The CogState Battery can detect decline in cognitive function that does not affect function in everyday life over even a 6 month period [
35]. It has been used extensively in supervised settings to repeatedly evaluate cognition in clinical trials, with concussed patients, and with individuals with mild cognitive impairment and dementia. In older adults, CogState measures of information processing speed, attention and memory have been shown to be highly sensitive to the cognitive dysfunction and longitudinal cognitive decline [
36,
37]. The battery is visually presented and is therefore highly suitable for use with people with hearing loss. Both the speed and accuracy of responses are recorded and transformed on a centralised platform to yield normalised data distributions [
31,
32].
The Groton Maze Learning Test (GML) assesses executive function, taking 5 min to administer on average. Using a maze learning paradigm, the total number of errors made when attempting to learn the same hidden pathway across five trials presented consecutively is calculated.
The Detection Test (DET) assesses psychomotor function and takes 2 min to administer on average. The participant is asked to respond “yes” when a card in the centre of the screen turns over until either 25 correct responses are obtained, or the maximum time limit (2 min) is reached (whichever occurs first). Performance speed (milliseconds) taken to complete the test is recorded.
The Identification Test (IDN) assesses visual attention and takes approximately 3 min to administer. A playing card in the center of the screen that turns over is used to create a choice reaction paradigm in which the participant must answer “yes” or “no” to the question “Is the card red?” Performance speed (milliseconds) to complete the test is recorded.
The One Card Learning Test (OCL) assesses visual learning and takes on average 5 min to administer. A playing card in the center of the screen that turns over is used to create a pattern separation paradigm in which the participant is required to answer “yes” or “no” to the question “Have you seen this card before in this test?” The test measures performance accuracy.
The One Back Test (ONB) assesses working memory and takes 3 min to administer on average. A playing card in the center of the screen turns over to create an n-back paradigm in which the participant must answer “yes” or “no” to the question “Is the previous card the same?” Both speed and accuracy of performance on this task are measured.
2.5. Medical Health History
A detailed health history, including medical history, was taken, (including family history of mental and other neurological illnesses), a personal health history, including smoking, current and past alcohol use, illicit drug and medication use.
2.6. Anxiety and Depression
The Hospital Anxiety and Depression Scale (HADS) [
38] measures levels of depressive and anxiety symptoms. This tool generates ordinal data and was designed for use with people who have physical health problems. For anxiety, specificity is 0.78, with sensitivity of 0.9, and for depression, 0.79 and 0.83 respectively.
2.7. Health Utilities Index-3 (HUI-3) Quality of Life
Health status and health-related quality of life (HRQL) for all participants was assessed using the Health Utilities Index-3 quality of life questionnaire (HUI-3; [
39]), as one means of measuring hearing aid benefit. The HUI-3 measures vision, hearing, speech, ambulation, dexterity, emotion, cognition and pain. It has been a reliable, responsive and valid measure in a number of clinical studies. Utility scores provide an overall assessment of the HRQL of patients, with 0.00 representing the state of being dead, and 1.00 representing a perfect state of health.
2.8. Ease of Communication/Subjective Device Benefit
Ease of communication in everyday situations and subjective benefit from hearing aids were measured using the Abbreviated Profile of Hearing Aid Benefit (APHAB; [
40]), a questionnaire designed to measure self-reported auditory disability in everyday living. The scale covers hearing speech in a variety of competing contexts and different everyday sounds across four subscales: Ease of Communication, Reverberation, Background Noise and Aversiveness. An overall Global Benefit score is also provided. In terms of defining benefit on individual subscales, a change of 22 or more points for any of the EC, RV or BN subscales, or 31 points or more on the AV subscale, is interpreted as significant. For a significant ‘overall picture’ benefit to be defined, each of EC, RV and BN (AV is excluded) must improve by at least 5 points (with a 10% chance of false positive error). A criterion of benefit of at least 10 points reduces the chance of a false positive interpretation of significant benefit to 4%.
2.9. Health and Lifestyle
The International Physical Activity Questionnaire was sued to assess health and lifestyle (IPAQ; long form, 31 items; [
41]). The IPAQ monitors population levels of physical activity and inactivity in adults. It has four domains: (1) during transportation, (2) at work, (3) during household and gardening tasks and (4) during leisure time, including exercise and sport participation.
2.10. Loneliness and Social Participation
The Lubben Social Network Scale (LSNS; [
42]) is a brief instrument designed to gauge social isolation in older adults by measuring perceived support received from family and friends. It typically takes 5–10 min to complete and comprises an equally weighted number of items used to measure size, closeness and frequency of a respondent’s social network.
The Loneliness Scale [
43] is an 11-item scale designed to measure subjective feelings of loneliness as well as feelings of social isolation. Participants rate each item as either O (“I often feel this way”), S (“I sometimes feel this way”), R (“I rarely feel this way”), or N (“I never feel this way”). Typically, scale reliability in the 0.80 to 0.90 range is observed.
2.11. Device Use Compliance
In evaluating treatment effects, it is important to measure compliance with device use. In addition to using the data logging function of the hearing aids, all participants who were assessed at the 18 month post-fitting point completed a brief questionnaire about their use of their hearing aid/s, including how many hours per day they used it.
2.12. Statistical Analysis
Regression was used to quantify differences in hearing loss across education levels. The specification was
where BPTA is the PTA hearing loss in the better ear in decibels, UGrad = 1 if years of education was 13–15 years and 0 otherwise, PGrad = 1 if years of education was 16 years or greater and 0 otherwise, and U is the regression disturbance. This regression was estimated for all participants and for males and females separately. The intercept β
0 is the average hearing for those with education levels of 12 years or fewer. The slope coefficient β
1 is the difference between the averages of the hearing losses for those with 13–15 years education and those with 12 years or fewer. Similarly, the slope coefficient β
2 is the difference between the averages of the hearing losses for those with 16 years or more of education and those with 12 years or fewer.
Relationships between cognition, hearing, age, education and sex were quantified at baseline using regression. For a cognition score Y (one of either GML, IDN, OCL, ONB or OCL), the regression has the form
where BPTA is the PTA hearing loss in the better ear measured in units of 10 dB, Age is age in decades, Female = 1 for a female participant and 0 otherwise. The interpretation of β
1 is that an increase of 10 dB in hearing loss in the better ear corresponds to a change of β
1 in the mean of Y, controlling for age, gender and years of education.
For individual participants, clinically important decline in cognition over the study period was identified using the Reliable Change Index (RCI) procedure [
44,
45], where a reduction in score for GML, DET, ONB, and IDN of more than 16, 0.06, 0.05, or 0.04 points respectively defines a clinically relevant improvement. An increase in those scores by more than those respective amounts defines a deterioration. OCL scores are defined in the opposite direction, with an increase of more than 0.09 defining an improvement. Changes within these ranges are not considered clinically important. Using this criterion, each participant was classified into improving, not changing or deteriorating on each of the five CogState subtests.