Introduction

Ageing involves physiological cognitive impairment, and maintaining a high level of cognitive function is a key component of successful aging [1]. Aging-related cognitive impairment diminishes the competence to perform activities in daily living, decreases the quality of life, and imposes a tremendous socioeconomic burden [2]. The number of people with dementia is expected to exceed 1 million by 2024 in Korea [3]. Those who received treatment for mild cognitive impairment have increased 8.4 times over the past 10 years, and 10-15% of those with mild cognitive impairment develop dementia every year [4]. There is an urgent need to manage cognitive impairment. Even though aging will inevitably lead to cognitive impairment, over one-third of cases of cognitive impairment may be caused by modifiable risk factors, suggesting that the onset of cognitive impairment may be delayed or prevented [5]. Longitudinal studies indicated linear declines in episodic memory from age 60, but there is also evidence of declines in processing speed and spatial processing occurring earlier [6]. Midlife is an important transitional period for cognitive aging [7]. Therefore, the various research should focus on identifying factors that may prevent and delay the cognitive impairment among middle and older adults in community nursing settings.

Hearing difficulty is one possible risk factor that rises quickly with age, similar to cognitive impairment [8,9]. Over 1.23 billion individuals worldwide suffer from hearing difficulty, which is a prevalent and frequently incapacitating condition that may even cause a wide range of age-related mental health problems [10]. According to estimates, hearing difficulty accounts for up to 8% of dementia cases worldwide, and it is the primary modifiable risk factor for dementia [11]. In a study using the Korea National Health and Nutrition Examination Survey, the hearing difficulty rate was 16.8% in the 50-69 age group and 36.5% in those aged 70 and older [12], so the hearing difficulty needs to be considered a modifiable risk factor to prevent the cognitive impairment in middle and old age. One study pointed out that the possibility of sensory deprivation brought on by age-related peripheral hearing difficulty may reduce cortical brain volumes that are comparable to those brought on by cognitive impairment [13].

According to the results of the Korea National Health and Nutrition Survey, the rate of masticatory difficulty rapidly increased to 13.3% in those 40s and 25.4% in those 50s, and to 33.1% in those aged 65 or older [14]. Several studies have demonstrated that the loss of masticatory function caused by teeth is linked to a sharper rate of global cognitive impairment [15], and a higher risk of dementia [16]. A cross-sectional investigation discovered that the differences in episodic memory were linked to complaints regarding masticatory function [17]. Cognitive impairment is far more likely to occur when masticatory problems and multiple tooth loss occur [18]. Furthermore, new data points to a mechanism involving decreased mechanical sensory input from poor mastication brought on by tooth loss as the reason for the correlation between tooth loss and cognitive deterioration [15,17]. Masticatory dysfunction has been linked to decreased cerebral blood flow and brain activity, which may hasten cognitive decline [19]. Additionally, a nutritional imbalance brought on by discomfort during mastication is probably associated with cognitive deterioration in old age [20].

Hearing is also influenced by dental health. A systemic review and meta - analysis reported the pooled prevalence of dental caries to be 58% among the hearing difficulty individuals; those with hearing difficulty have bad oral health conditions when compared with normal individuals [21]. Dental-hearing is the term for the process by which sound stimuli that pass through the teeth and jaw reach the cochlea by bone conduction [22]. Due to its fibrous-elastic nature, the skull can transmit vibrations when subjected to a sound source [23]. The correlation between dental and hearing health has been demonstrated by some studies [24,25]. Those who have masticatory difficulty with losing more than half of their teeth are 1.64 times more likely to suffer hearing difficulty than those who haven’t [24]. In addition, implants were found to increase bone conduction in a manner comparable to that of teeth in research assessing hearing one month following implant insertion in persons who were entirely edentulous [25].

More recent work showed that a greater number of sensory impairments was associated with increasing risk of dementia in a graded fashion, which included a combination of hearing, smell, touch, and vision assessments [26]. Compared to those with single difficulty (hearing difficulty or masticatory difficulty) and those without any hearing or masticatory difficulty, those with dual difficulty (hearing difficulty and masticatory difficulty) may have a high risk of cognitive impairment. To date, hearing difficulty and masticatory difficulty are independently associated with cognitive impairment [8,9,15,16], but the impact of coexistence of hearing and masticatory difficulty on risk of cognitive impairment is not well understood. Therefore, it is needed to quantify the effects of concurrent hearing and masticatory difficulty on cognitive impairment risk.

Many neurological disorders demonstrate sex differences, such as females having a higher prevalence of Alzheimer's disease than males of the same age, and they are having a considerably faster loss and worsening of cognition than elderly males [27,28]. Li & Singh reported of sex differences in cognitive function from normal aging to Alzheimer's disease, and sex hormones, along with other genetic factors, significantly affect the risk of Alzheimer's disease [27]. Therefore, there is a need for different approaches to manage cognitive impairment by sex. Understanding the coexistence effects of hearing difficulty and masticatory difficulty on the cognition impairment risk of sex differences is critical for developing sex-specific interventions to prevent cognitive impairment.

Some longitudinal studies have identified separate hearing difficulty [29] and masticatory difficulty [30] as modifiable factors for cognitive impairment in 65 years or older. However, there are very few longitudinal studies to determine the coexistence effects of hearing difficulty and masticatory difficulty on cognitive impairment in middle and old age by sex. Korea Longitudinal Study of Aging (KLoSA) is a large-scale longitudinal survey conducted at the national level and is considered to have high reliability and accuracy in South Korea [31]. Therefore, this study aimed to determine the coexistence cumulative effect of hearing and masticatory difficulty on cognitive impairment risk in middle and old age by sex using panel data from the KLoSA.

Methods

Study design and participants

This was a secondary data analysis study using data from the Korean Longitudinal Study of Aging (KLoSA) of a population-based cohort sample that was followed up every two years for 14 years from 2006 (1^th wave) as a baseline survey to 2020 (8^th wave). 10,254 middle-aged and older adults ≥45 years participated in the KLoSA panel study in 2006, which examined sociodemographic characteristics, family and social networks, economic activities, health habits, health status and comorbidities, cognitive function, and other variables associated with aging and health. Using a multi-stage, stratified sampling technique based on geographic regions and dwelling types nationwide, the Korea Employment Information Service performed the KLoSA survey. Trained interviewers went door-to-door with participants, using computer-assisted in-person interviews to obtain data. All participants supplied written informed consent, and the survey protocol was approved by Statistics Korea's Institutional Review Board [31]. A flowchart of the study sample selection process is shown in Figure 1. A total of 10,254 middle-aged and older adults were included in the initial wave of the KLoSA (2006). We excluded individuals with missing data (n=629) and those exhibiting cognitive impairment, which was defined as having a Korean-Mini Mental State Examination (K-MMSE) score of <24 (n=2,686) in the initial wave (2006), thus resulting in a final sample of 6,939 for analyses, and sex was divided into two groups: male (n=3,483) and female (n=3,501).

Measurements

The Korean Mini-Mental State Examination (K-MMSE) scale, which was developed by Folstein et al. [32] and modified to suit the Korean context [33], was used to test cognitive function. Nineteen questions covering five domains of cognitive function—registration, orientation in time and location, attention and calculation, memory recall, and visual construction—made up the K-MMSE. An overall K-MMSE score, ranging from 0 to 30, was calculated by adding the subscale scores for these categories. Higher scores corresponded to higher cognitive function. Cognitive impairment in this study was defined as a K-MMSE score less than 24 at the time of evaluation. Two groups of participants were identified: those with cognitive impairment (K-MMSE score<24) and those with normal cognition (K-MMSE score≥24).

Hearing function and masticatory function were measured using self-reported evaluation and classification methods. Hearing function was investigated by asking how hearing function was. In the case of hearing aid users, asking how hearing function when using hearing aids was. Masticatory function was assessed by asking if he/she could chew hard foods, such as apples and meats, without difficulty while wearing dentures. Hearing and masticatory function were evaluated using a five-point scale (excellent, very good, good, fair, or bad). We defined ‘fair or bad’ cases as hearing difficulty in hearing function and masticatory difficulty in masticatory function. Self-reported hearing difficulty compare reasonably well in identifying older adults with hearing impairment. Such self-reported measures are also frequently used in national surveys [34] and similar cohorts [35]. One study reported subjective (self-assessed) and objective (color change of two-color chewing gum) assessments of masticatory difficulty are valid, interrelated, and recommended for practice [36] and are used.

Potential covariates chosen included self-reported baseline characteristics of socio-demographics, health risk behaviors, and chronic conditions. Baseline age was categorized into 2 groups by sex. Participants were asked to report on education level, marital status, residential area, and employment. Household income was separated into quartiles, and then classified into three groups (i.e., quartile 1 as low, quartiles 2 and 3 as moderate, and quartile 4 as high). Responding to a single question for each chosen health risk behavior, participants reported smoking, drinking: no (never, past), yes (current), non - regular exercise, and non-eating breakfast (yes or no). Obesity was divided into two groups: no (<24.9 kg/m²), yes (≥25 kg/m²). Health risk behaviors at baseline included smoking, drinking, regular exercise, eating breakfast, and obesity, the sum number of which was also presented as 0, 1, or ≥2. Restriction in activities of daily living and instrumental ADL categorized into yes or no. Self-rated health was graded as very good, good, neural, bad, or very bad and categorized into good (very good, good, neural) and bad (bad, very bad). Depression (using CES-D 10 scores), hypertension, diabetes, cardiac disease, cerebrovascular disease, cancer, and arthritis categorized as yes or no. Chronic diseases at baseline included depression, hypertension, diabetes, cardiac disease, cerebrovascular disease, cancer, and arthritis, the total number was also shown as 0, 1, 2 or ≥3.

Data analysis

With the descriptive analysis, we examined the cognitive function, main independent variables (hearing difficulty, masticatory difficulty), and potential covariates (characteristics of socio-demographics, health risk behaviors, and chronic conditions) of the study participants by sex in the 1st wave (2006) for the baseline data. And the study participants who developed cognitive impairment during the follow-up period (from 2008 to 2020) were considered as having developed the event (cognitive impairment onset: yes), and the study participants who did not develop cognitive impairment until the end of the follow-up period (2020) were considered as having been censored (cognitive impairment onset: no). Chi-square tests were utilized to analyze the occurrence of cognitive impairment according to the characteristics of the study participants. Cox’s proportional hazards model is a method of estimating the survival function by considering the covariates of each study participant [37]. To compare the risk of cognitive impairment occurrence according to the hearing difficulty and masticatory difficulty by considering potential covariates, Cox’s proportional hazards model was used. After adjusting the sets of chosen potential covariates, the adjusted hazard ratios (HRs) and 95% confidence intervals (CIs) were estimated to evaluate the effects of the hearing function and masticatory function on cognitive impairment. The time interval between the date of enrollment and the date of cognitive impairment onset or censoring (up to 14 years) was assessed as the outcome variable. Kaplan - Meier survival analysis is a method to calculate the occurrence rate of an event at the time the event occurred based on the observation time [38]. To compare the survival function of the cumulative incidence of cognitive impairment according to the hearing difficulty and masticatory difficulty of the study participants at some arbitrary time point, Kaplan–Meier survival analysis was used. The log-rank test is a hypothesis test to analyze the survival distribution of two or more groups over time [39]. To analyze the differences in the cumulative incidence of cognitive impairment of three groups of study participants (none: no hearing difficulty and masticatory difficulty, single: hearing difficulty or masticatory difficulty, dual: hearing difficulty and masticatory difficulty), log - rank test was used. Kaplan – Meier survival analysis and the log-rank test was graphically analyzed. Data analyses were two-sided at alpha=0.05 and carried out with SPSS version 27.0 (IBM, Armonk, NY, USA).

Ethical considerations

The National Statistical Office (permission No. 33602) approved the KLoSA study, which was carried out with the participants' written informed consent and in accordance with the principles of the Declaration of Helsinki. This study was conducted after gaining permission to utilize data from the website of the KLoSA, and approval of exemption from institutional review board (IRB No: 1041386-202407-HR-84-02).

Results

Baseline characteristics of the study participants

Table 1 presents the baseline characteristics of the study participants (1^st wave, 2006). Out of the total study participants of the 6,939 adults aged 45 or older, 49.5% were males (n=3,438) and 50.5% were females (n=3,501). MMSE score was 28.09±1.81 for male, 27.77±1.91 for female. Hearing difficulty was 6.1% for males, 3.3% for females, and 4.7% for the total study sample. Masticatory difficulty was 24.3% for males, 21.4% for females, and 22.8% for the total study sample. Single difficutly (hearing difficulty or masticatory difficulty) was 23.7% for males, 21.5% for females, and 22.6% for the total study sample. Dual difficulty (hearing difficulty and masticatiory difficulty) was 3.3% for males, 1.6% for females, 2.4% for the total study sample. Two or more out of 5 health risk behaviors (smoking, drinking,non- regular exercise, non- eating breakfast, obesity) were 62.2% for males, 28.2% for females, and 45.0% for the total study sample. Three or more out of 7 chronic diseases (hypertension, diabetes mellitus, cardiac disease, cerebrovascular disease, cancer, depression, arthritis) were 2.7% for males, 5.1% for females, and 3.9% for the total study sample.

Differences in cognitive impairment in baseline characteristics

Table 2 presents the differences in cognitive impairment onset (from 2^nd wave, 2008 to 8^th wave 2020) according to the baseline characteristics of the study participants by sex (1^st wave, 2006). The cognitive impairment incidence rate was 34.0% for males, 41.4% for females, and 37.7% for the total study sample, and higher in females (p<.001). Cognitive impairment incidence rate was higher in hearing difficulty than no hearing difficulty (p<.001), in masticatory difficulty than no masticatory difficulty (p<.001) for males and females. Among males, the cognitive impairment incidence rate was 44.7% in single difficulty, and 54.0% in dual difficulty; there was a significant difference (p<.001). The cognitive impairment incidence rate was 56.6% in single difficulty and 76.4% in dual difficulty; there was a significant difference (p<.001). Among the total study sample, the cognitive impairment incidence rate was 50.4% in single difficulty and 61.3% in dual difficulty; there was a significant difference (p<.001).

The cognition incidence rate was significant differnces in education, martial status, residence, income, employment, number of health risk behaviors (smoking, drinking, regular exercise, eating breakfast, obesity), self-rated health, and number of chronic diseases (hypertension, diabetes, cardiac disease, cerebrovascular disease, cancer, depression, arthritis) for male, female, and the total study sample.

Association between hearing difficulty, masticatory difficulty, and cognitive impairment

Table 3 shows the results of Cox's proportional hazards model analysis to confirm the proportional risk of cognitive impairment occurrence according to the hearing difficulty and masticatory difficulty. In the fully adjusted model, the study participants with dual difficulty were 1.26 times more likely to develop cognitive impairment (95% CI: 1.03-1.56) than those without any hearing or masticatory difficulty. Significant association was not present for single difficulty (hearing difficulty or masticatory difficulty) with cognitive impairment as the outcome (HR:1.09, 95% CI: 1.00-1.19). Among females, participants with dual difficulty were 1.52 times more likely to develop cognitive impairment (95% CI: 1.11-2.09) than those without any hearing or masticatory difficulty, but among males, dual difficulty was not associated with cognitive impairment (HR:1.10, 95% CI: 0.83-1.45). Although single difficulty was not associated with the risk of cognitive impairment as compared to none difficulty, associations differed between the type of difficulty and cognitive impairment risk (Table 4). Masticatory difficulty was individually associated with the risk of cognitive impairment after adjusting potenial covariates, with HR of 1.13 (95% CI: 1.08–2.19) in the individual models. With simultaneous inclusion of hearing and masticatory difficulties in one model, masticatory remained significantly associated with risk of cognitive impairment, with HR of 1.10 (95% CI: 1.01-1.21) in the combined model after adjusting for selected covariates. But hearing difficulty was not associated with the risk of cognitive impairment, whether considered individually or after adjusing for masticatory difficulty in the combined model.

The Kaplan – Meier survival charts showing the probability of cognitive impairment-free cumulative survival rate over follow-up time by hearing and masticatory difficulties (none, single, and dual) among male and female were presented in Figure 2. An increasing number of hearing and masticatory difficulties was associated with a risk of cognitive impairment in a graded fashion based on the crude Kaplan-Meier estimate. And log-rank tests showed the significant differences of the cumulative incidence of cognitive impairment according to three groups (none, single, dual) among male and female (p<.001).

Discussion

In this secondary analysis survey, we identified an independent relationship between masticatory difficulty and an elevated risk of cognitive impairment utilizing nationwide population-based data (KLoSA). It is consistent with some longitudinal studies that found masticatory dysfunction to be predictive of subsequent cognitive impairment in older adults [15-17]. In contrast, another study reported that decreased masticatory function and mild cognitive impairment were not associated [40]. A meta-analysis study found that poorer masticatory function was associated with lower cognitive status [41]. Cognitive function is directly linked to physical activity, particularly food chewing. The elderly like soft or easy-to-chew foods. This will have an impact on the lowered activity of the masticatory muscles, resulting in a reduction in blood supply to the brain [42]. Mastication is a crucial part of maintaining cognitive function, masticatory difficulty decreases cerebral blood flow, causing impaired brain function [43]. And masticatory difficulty narrows the range of food alternatives, resulting in poor diet quality and nutritional imbalance, increasing the prevalence of systemic disorders such as cognitive decline [44]. Thus, considering the relationship between masticatory difficulty and cognitive impairment risk, it is necessary to determine whether the patients have masticatory difficulty or not when assessing their health and manage them as a high-risk cognitive function group in community nursing settings. And collaborative studies are required to identify whether early detection and management of masticatory difficulty could minimize cognitive impairment.

Our result reported that hearing difficulty was not independently associated with cognitive impairment, which is in line with some studies reporting that hearing loss was not associated with a greater rate of cognition decline [8-10]. But, in a community sample of older adults, a relatively strong relationship was found between baseline hearing impairment and both existing and new cases of cognitive impairment over a 5-year period [45]. As a result of meta - analysis of 36 studies, age-related hearing loss was significantly associated with multi-domain cognitive impairment and dementia acceleration [46]. These discrepancies may be due to differences in methods for evaluating the presence of hearing difficulty. In a study using the Korea National Health and Nutrition Examination Survey, the prevalence of discrepancies between self-reported hearing difficulty and hearing loss diagnosed by audiometry was 18.2%, and 39.5% of participants with self-reported hearing difficulty had no audiometry hearing difficulty [47]. Increased cognitive load, altered neural networks, and more effortful listening are all possible outcomes of hearing impairment [48]. Persistently compensating for hearing loss can cause brain restructuring and reallocation, as well as the depletion of cognitive resources [49]. Therefore, it is needed to identify the association between the risk of incident cognitive impairment and the severity of an individual’s objective hearing loss in a longitudinal study [50].

We found that dual difficulty was associated with a 52.1% increased risk for cognitive impairment compared to without hearing and masticatory difficulty. But single difficulty was not associated with cognitive impairment. This cumulative dual effect of hearing and masticatory difficulty on cognitive impairment is partially consistent with previous studies in the aspect of simultaneously considering risk factors such as dual sensory impairment of hearing and vision related to the higher risk of cognitive impairment than non- or single sensory impairment [51,52]. Our result of association between hearing difficulty and masticatory difficulty is consistent with previous studies. In the USA, one study observed 1.6 times more hearing impairment in patients shifting from >17 to <17 teeth in the USA [53]. Another cross-sectional study found that a greater degree of tooth loss was associated with an increased prevalence of hearing impairment in Japan [54]. The underlying mechanisms of the association between masticatory difficulty and hearing difficulty have suggested that tooth loss may affect hearing loss through a reduction of the intermaxillary vertical dimension [55]. Implant behaved like a tooth, improving bone conduction through the jaw to the skull and positively impacting hearing ability [25]. Therefore, adults with coexisting hearing and masticatory difficulty represent a high-risk population that could be a target for intervention prior to the onset of cognitive impairment. It is crucial to identify risk variables that could contribute to cognitive impairment in its early stages since interventions would probably be more successful in the early prodromal phase, before neurodegeneration or cognitive damage becomes irreversible [56]. The result that dual difficulty was not associated with cognitive impairment for males may be relevant to a lower incidence of cognitive impairment than females and a shorter follow-up period. Future research is warranted to determine the coexisting effect of hearing and masticatory difficulty on cognitive impairment with longer follow-up periods for males.

Thus, we were able to confirm the cumulative effect of risk factors on cognitive impairment when hearing and masticatory difficulty occurred simultaneously, rather than the size of their individual effects for females. In community nursing settings such as home visit nursing care and outreach health and welfare services - centered administrative districts, community nurses detect patients with cognitive impairment through dementia screening tests and refer high - risk groups to a mental health welfare center. Considering the cumulative effect of hearing and masticatory difficulty on cognitive impairment risk, nurses can play an important role in assessing hearing and masticatory difficulty so individuals can be referred for further testing and possible early intervention in order to prevent cognitive impairment [50]. Health information emphasizes the need to ensure hearing and masticatory aids are in place, but few nurses learn effective strategies to manage various assistive listening and masticatory devices with older adults who have hearing and masticatory difficulty [57]. Also, barriers to assessing hearing and masticatory function, such as time limits and provider unfamiliarity with screening methodologies, represent wasted opportunities to avoid cognitive damage [58]. Therefore, nurses need to use convenient assessing tools for hearing and masticatory function, which would reduce the barriers to screening for hearing and masticatory difficulty and manage high risk individuals of cognitive impairment in community nursing settings.

This study has some limitations. First, the information for hearing and masticatory problems included in this study was self-reported; therefore, there may be biases in the respondents' responses. Self-reports of trouble with hearing compare reasonably well in identifying older adults with hearing impairment [59]. And subjective evaluation methods of masticatory function using questionnaires have the advantage that they do not require special devices and are easy for anyone to understand [60]. Although self-reported assessments of hearing or masticatory function have been widely used in population-based surveys, they may not represent the individual health condition as is and tend to overestimate or underestimate their hearing and report fewer hearing problems [61]. Therefore, for replicating our findings, investigations should use objective and subjective assessments of hearing and masticatory function. Second, only MMSE was used as a screening indicator for cognitive impairment. In the KLoSA data, MMSE was the only indicator that could check cognitive function. Further studies need to use clinical tools to assess cognitive function. Finally, although we accounted for several possible confounders, some residual confounding may still exist. Third, because 4.6% of the prevalence of hearing difficulty at baseline was low, the association of hearing difficulty with cognitive impairment risk did not seem to be significant, and because 2.4% of the prevalence of dual difficulty was low, the cumulative effect of hearing and masticatory difficulty on cognitive impairment risk seemed to be small. Therefore, considering the low prevalence of dual difficulty related to the low prevalence of hearing difficulty, it is needed to analyze the effects of hearing and masticatory difficulty on cognitive impairment risk by such measure as repeated measures analysis to ensure the validity of research results.

Despite these limitations, this study had a relatively large sample size, is representative of the community-dwelling Korean population aged 45 years and over, and a 14-year long follow-up period. Also, we identified modifiable risk factors such as masticatory difficulty for managing cognitive impairment in various community nursing settings.

Conclusions

Using data from the Korean longitudinal research on aging survey, this study tried to establish the relationship between hearing and masticatory difficulty and cognitive impairment in middle-aged and older people. Our data reveal that coexistence of hearing and masticatory difficulty had a higher risk of cognitive impairment than without hearing and masticatory difficulty in females. Increasing concern about healthy aging as a rapid aging population in Korea, this is a noteworthy result to manage cognitive impairment in community nursing settings. Comprehensive and timely assessment, including hearing and masticatory function, may be useful in finding out high - risk group of cognitive impairment. Our research findings could provide meaningful information about the development of nursing intervention strategies to minimize negative consequences for cognitive function by preventing of hearing and masticatory difficulty.

Figure 1.

Flowchart of the study participants in the 1st wave at baseline year 2006

Figure 2.

Kaplan–Meier estimate (log-rank test) of risk of cognitive impairment by number of hearing difficulty and masticatory difficulty among male and female

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