The association between cognitive impairment and oral health or oral hygiene behaviors among multiethnic older adults in Western China: a cross-sectional multicenter study
Cognitive impairment in older adults presents a significant public health challenge amid the accelerating aging of the global population . The global prevalence of mild cognitive impairment (MCI) is estimated at 15.56%, and MCI is considered an intermediate stage between normal aging and dementia . Dementia, the seventh leading cause of death worldwide, imposes a substantial burden on global public health. The number of individuals with dementia is projected to increase from 57.4 million in 2019 to 152.8 million by 2050 . The societal economic burden of Alzheimer's disease and related dementia is projected to increase significantly with global aging, reaching an estimated $16.9 trillion by 2050, encompassing direct medical costs and intangible costs, such as reduced productivity and premature mortality . In the absence of a cure for dementia, early detection of cognitive impairment in older adults, followed by timely intervention, might be the most cost-effective strategy to prevent or delay progression to dementia. Therefore, identifying risk factors associated with cognitive impairment is crucial for preserving cognitive functioning and promoting healthy aging in older adults. Research on the impact of oral health on the overall health in older adults has been emerging, including its effects on cognitive function . Although studies have indicated an association between cognitive function and oral health (e.g., tooth loss, periodontitis) , as well as oral hygiene behaviors (e.g., tooth brushing) , the conclusions remain inconsistent . This calls for large-scale, multicenter studies to better establish the link between oral health and cognitive function in older populations. China accounts for nearly one quarter of the global dementia population . Notably, the western region of China reported a relatively higher overall prevalence of dementia (7.2%)  and rate of MCI among older adults (14.33%)  than other regions in the country. Fitzpatrick  and Gupta et al.  reported differences in cognitive status among racial groups in the United States. In fact, China's minority population is mostly concentrated in the western region , making it highly representative of the country’s ethnic diversity. Differences in dietary habits , religious beliefs , educational levels , and healthcare resources  among ethnic groups may lead to variations in oral hygiene behaviors, which can impact oral health . Therefore, this study focused on older individuals from diverse ethnic backgrounds in Western China, aiming to explore whether their oral health and oral hygiene behaviors are associated with their cognitive health. This study hypothesized that deteriorating oral health and inadequate oral hygiene behaviors may be associated with cognitive impairment in older adults. We also examined whether ethnicity is a significant factor that influences the relationship between cognitive impairment and oral health or oral hygiene behaviors in Western China. The current study aims to identify modifiable risk factors related to cognitive impairment from the perspective of oral health, which may facilitate enhancing public awareness of oral health for successful aging.   Study design and sample selection This cross-sectional study obtained data from the West China Health and Trend (WCHAT) study, a multiethnic, multicenter observational cohort study designed to explore aging and health status in older adults residing in community settings. This study was conducted between July and December 2018. Data were collected by well-trained research staffs. This study was approved by the ethics committees of the West China Hospital of Sichuan University (Number: 2017–445) and was registered at the Chinese Clinical Trial Registry (Number: 1800018895). Informed consent was obtained from all participants before they officially participated in the study. Details of the study have been published elsewhere . A total of 7,536 participants from 18 ethnic groups in Sichuan, Yunnan, Guizhou and Xinjiang Provinces were initially recruited, and 6,529 participants were included based on the following criteria: 1) aged 50 years or older and 2) had no missing data on cognitive function, oral health, oral hygiene behaviors, or other variables (Fig. ). Assessment of oral health and oral hygiene behaviors Oral health conditions were assessed based on self-reported oral health conditions, the number of residual teeth, and the use of dentures. Oral hygiene behaviors were evaluated through the frequency of toothbrushes, toothpicks, and toothpaste usage, as well as dental history, the latest time of dental care, and the reasons for performing the latest dental care, which are closely related to oral health . The number of residual teeth and denture use were examined by a professional dentist. Furthermore, other data were collected via a self-made oral health and oral hygiene behaviors questionnaire adapted from previous studies . An additional file shows this in more detail [see Additional file 1 (Table A. 1)]. The questionnaire consisted of 9 questions, each with only one possible answer. Assessment of cognitive health Cognitive status was evaluated via the Chinese version of the Short Portable Mental Status Questionnaire (SPMSQ), which has been widely used as a well-established scale in the Chinese elderly population  and comprises ten items that encompass short-term memory, long-term memory, orientation, and attention. Higher scores on the SPMSQ indicate more severe cognitive impairment. SPMSQ scores were categorized into four levels according to Pfeiffer's criteria : 0–2 errors indicated normal mental functioning, 3–4 errors indicated mild cognitive impairment, 5–7 errors indicated moderate impairment, and 8 or more errors indicated severe impairment. The final score was adjusted based on participants’ educational level. Covariates The demographic and living condition information included 1) age, 2) gender, 3) ethnicity (Han, Qiang, Yi, Uyghur, Tibetan, and Others), 4) educational level, 5) occupation (Farmer, Blue-collar, White-collar, Others), 6) spouse status, 7) religious belief, 8) longevity families(parents, grandparents, brothers, sisters and children, if any, aged 90 or over), 9) nutritional status, 10) type of drinking water (Tap water, Well water, Spring water, Others), 11) smoking habits (smoking at least one cigarette daily for a continuous period of six months or longer), 12) alcohol use (at least once a week), and 13) tea-drinking habits (at least four days per week). Ethnic groups with fewer than 200 participants were combined into the "Others" category, including Zhuang, Kyrgyz, Dong, Hui, Mongolian, Miao, Uzbek, Man, Lisu, and Bai. Nutritional status was evaluated via the widely validated and reliable Mini Nutrition Assessment Short Form (MNA-SF) scale , with increasing scores indicating malnutrition, risk of malnutrition, and normal nutritional status . Statistical analysis The one-sample Kolmogorov‒Smirnov test was used to determine the normalized distribution of variables. The data are presented as medians (interquartile ranges, IQRs), means (standard deviations, SDs) or frequencies. Pearson’s chi-square test was used examine the difference in the composition ratio of categorical variables in different cognitive function groups, and the Kruskal‒Wallis H test or one-way analysis of variance (ANOVA) was used to examine the difference of continuous variables in different cognitive function groups. The associations between oral health and oral hygiene behaviors factors and the cognitive score were analyzed via multiple generalized linear regression analyzes via three single models as follows: In Model 1, univariate generalized linear analysis was used without adjustment, followed by further utilization of multivariate generalized linear analysis in Model 2 (adjusted by some nonmodifiable factors, such as age, sex, ethnic group, and longevity families) and in Model 3 (adjusted by some nonmodifiable factors and some modifiable factors, such as educational level, occupation, spouse status, MNA-SF score, MNA-SF assessment status, type of drinking water, history of smoking, history of alcohol use, and history of drinking tea). To test for differences in ethnic groups, we stratified for ethnic groups and then performed linear regression analysis via the same method as above. R (version 4.1.3) was used for statistical analysis of the data. A two-tailed p < 0.05 was regarded as statistically significant.   This cross-sectional study obtained data from the West China Health and Trend (WCHAT) study, a multiethnic, multicenter observational cohort study designed to explore aging and health status in older adults residing in community settings. This study was conducted between July and December 2018. Data were collected by well-trained research staffs. This study was approved by the ethics committees of the West China Hospital of Sichuan University (Number: 2017–445) and was registered at the Chinese Clinical Trial Registry (Number: 1800018895). Informed consent was obtained from all participants before they officially participated in the study. Details of the study have been published elsewhere . A total of 7,536 participants from 18 ethnic groups in Sichuan, Yunnan, Guizhou and Xinjiang Provinces were initially recruited, and 6,529 participants were included based on the following criteria: 1) aged 50 years or older and 2) had no missing data on cognitive function, oral health, oral hygiene behaviors, or other variables (Fig. ). Assessment of oral health and oral hygiene behaviors Oral health conditions were assessed based on self-reported oral health conditions, the number of residual teeth, and the use of dentures. Oral hygiene behaviors were evaluated through the frequency of toothbrushes, toothpicks, and toothpaste usage, as well as dental history, the latest time of dental care, and the reasons for performing the latest dental care, which are closely related to oral health . The number of residual teeth and denture use were examined by a professional dentist. Furthermore, other data were collected via a self-made oral health and oral hygiene behaviors questionnaire adapted from previous studies . An additional file shows this in more detail [see Additional file 1 (Table A. 1)]. The questionnaire consisted of 9 questions, each with only one possible answer. Assessment of cognitive health Cognitive status was evaluated via the Chinese version of the Short Portable Mental Status Questionnaire (SPMSQ), which has been widely used as a well-established scale in the Chinese elderly population  and comprises ten items that encompass short-term memory, long-term memory, orientation, and attention. Higher scores on the SPMSQ indicate more severe cognitive impairment. SPMSQ scores were categorized into four levels according to Pfeiffer's criteria : 0–2 errors indicated normal mental functioning, 3–4 errors indicated mild cognitive impairment, 5–7 errors indicated moderate impairment, and 8 or more errors indicated severe impairment. The final score was adjusted based on participants’ educational level. Covariates The demographic and living condition information included 1) age, 2) gender, 3) ethnicity (Han, Qiang, Yi, Uyghur, Tibetan, and Others), 4) educational level, 5) occupation (Farmer, Blue-collar, White-collar, Others), 6) spouse status, 7) religious belief, 8) longevity families(parents, grandparents, brothers, sisters and children, if any, aged 90 or over), 9) nutritional status, 10) type of drinking water (Tap water, Well water, Spring water, Others), 11) smoking habits (smoking at least one cigarette daily for a continuous period of six months or longer), 12) alcohol use (at least once a week), and 13) tea-drinking habits (at least four days per week). Ethnic groups with fewer than 200 participants were combined into the "Others" category, including Zhuang, Kyrgyz, Dong, Hui, Mongolian, Miao, Uzbek, Man, Lisu, and Bai. Nutritional status was evaluated via the widely validated and reliable Mini Nutrition Assessment Short Form (MNA-SF) scale , with increasing scores indicating malnutrition, risk of malnutrition, and normal nutritional status .   Oral health conditions were assessed based on self-reported oral health conditions, the number of residual teeth, and the use of dentures. Oral hygiene behaviors were evaluated through the frequency of toothbrushes, toothpicks, and toothpaste usage, as well as dental history, the latest time of dental care, and the reasons for performing the latest dental care, which are closely related to oral health . The number of residual teeth and denture use were examined by a professional dentist. Furthermore, other data were collected via a self-made oral health and oral hygiene behaviors questionnaire adapted from previous studies . An additional file shows this in more detail [see Additional file 1 (Table A. 1)]. The questionnaire consisted of 9 questions, each with only one possible answer.   Cognitive status was evaluated via the Chinese version of the Short Portable Mental Status Questionnaire (SPMSQ), which has been widely used as a well-established scale in the Chinese elderly population  and comprises ten items that encompass short-term memory, long-term memory, orientation, and attention. Higher scores on the SPMSQ indicate more severe cognitive impairment. SPMSQ scores were categorized into four levels according to Pfeiffer's criteria : 0–2 errors indicated normal mental functioning, 3–4 errors indicated mild cognitive impairment, 5–7 errors indicated moderate impairment, and 8 or more errors indicated severe impairment. The final score was adjusted based on participants’ educational level.   The demographic and living condition information included 1) age, 2) gender, 3) ethnicity (Han, Qiang, Yi, Uyghur, Tibetan, and Others), 4) educational level, 5) occupation (Farmer, Blue-collar, White-collar, Others), 6) spouse status, 7) religious belief, 8) longevity families(parents, grandparents, brothers, sisters and children, if any, aged 90 or over), 9) nutritional status, 10) type of drinking water (Tap water, Well water, Spring water, Others), 11) smoking habits (smoking at least one cigarette daily for a continuous period of six months or longer), 12) alcohol use (at least once a week), and 13) tea-drinking habits (at least four days per week). Ethnic groups with fewer than 200 participants were combined into the "Others" category, including Zhuang, Kyrgyz, Dong, Hui, Mongolian, Miao, Uzbek, Man, Lisu, and Bai. Nutritional status was evaluated via the widely validated and reliable Mini Nutrition Assessment Short Form (MNA-SF) scale , with increasing scores indicating malnutrition, risk of malnutrition, and normal nutritional status .   The one-sample Kolmogorov‒Smirnov test was used to determine the normalized distribution of variables. The data are presented as medians (interquartile ranges, IQRs), means (standard deviations, SDs) or frequencies. Pearson’s chi-square test was used examine the difference in the composition ratio of categorical variables in different cognitive function groups, and the Kruskal‒Wallis H test or one-way analysis of variance (ANOVA) was used to examine the difference of continuous variables in different cognitive function groups. The associations between oral health and oral hygiene behaviors factors and the cognitive score were analyzed via multiple generalized linear regression analyzes via three single models as follows: In Model 1, univariate generalized linear analysis was used without adjustment, followed by further utilization of multivariate generalized linear analysis in Model 2 (adjusted by some nonmodifiable factors, such as age, sex, ethnic group, and longevity families) and in Model 3 (adjusted by some nonmodifiable factors and some modifiable factors, such as educational level, occupation, spouse status, MNA-SF score, MNA-SF assessment status, type of drinking water, history of smoking, history of alcohol use, and history of drinking tea). To test for differences in ethnic groups, we stratified for ethnic groups and then performed linear regression analysis via the same method as above. R (version 4.1.3) was used for statistical analysis of the data. A two-tailed p < 0.05 was regarded as statistically significant.   The sample characteristics are presented in Table [see the end of the document text file]. Among the included participants, the median (IQR) age was 62.4 (55, 68) years, and 62.5% were women. Finally, 1,005 participants (15.4%) were assessed as having cognitive impairment, and 1,670 (25.6%) were classified as having poor oral health status. Among the different ethnic groups, the Yi group had the highest prevalence of cognitive impairment (28.9%), followed by the Tibetan (19.0%) and “Others” (19.2%) groups. The median (IQR) number of residual teeth was 25 (16, 18). Compared with participants with normal cognitive conditions, those with cognitive impairment had worse self-rated oral health, fewer residual teeth, worse oral hygiene behaviors (i.e., infrequent use of toothbrushes, toothpicks, and toothpaste), and fewer frequent dental visits and receiving dental treatment or dental care ( p < 0.05). Additionally, older adults with cognitive impairment were older, more likely to be female, had lower education levels, were more often farmers, were mostly without a spouse, did not have longevity families, had poorer nutritional status, drank more spring water, smoked, drank alcohol, and consumed tea less frequently ( p < 0.01), an additional file shows this in more detail [see Additional file 1 (Table A. 2)]. The three regression models revealed a significant correlation between oral health and oral hygiene behaviors factors and cognitive impairment, adjusted for nonmodifiable and modifiable factors (Table ). A significant positive correlation between poor self-rated oral health and cognitive impairment was observed in the three models (model 1: β = 0.291, 95% CI 0.209–0.374; model 2: β = 0.199, 95% CI 0.119–0.278; model 3: β = 0.123, 95% CI 0.050–0.196). Cognitive impairment was negatively associated with the number of residual teeth in the unadjusted model and remained significant in the adjusted models when the number of residual teeth exceeded 16 (model 3: 17–24 group β = −0.132, 95% CI = −0.242–0.023; 25–32 group β = −0.177, 95% CI = −0.281–0.073). Participants who reported a lower frequency of toothbrushes (model 3 β = −0.524, 95% CI −0.650 to −0.398) and toothpaste usage (model 3 β = −0.381, 95% CI −0.488 to −0.273) seemed more prone to cognitive impairment after adjustment. Participants who received dental care within the past 6–12 months had a lower risk of cognitive impairment (model 3: β = −0.176, 95% CI −0.323 to −0.029). We conducted additional regression analyzes based on different ethnic groups to investigate the disparities in the associations between oral health and oral hygiene behaviors and cognitive impairment (Fig. and Table A. 3 [see Additional file 1]). In most ethnic groups (Han, Tibetan, Yi), cognitive impairment was significantly negatively correlated with the number of residual teeth and toothpaste usage ( β < 0, p < 0.05). In the Han, Tibetan, and Qiang groups, poor self-rated oral health was significantly associated with cognitive impairment ( β > 0, p < 0.05). In the Han group, participants who did not use dentures ( β = −0.156, p = 0.003) and those who used toothbrushes ( β = −0.732, p < 0.001) or toothpicks ( β = −0.203, p = 0.001) daily had a lower risk of cognitive impairment. Compared with Tibetan participants who brushed their teeth daily, those who never used toothbrushes were more prone to cognitive impairment ( β = −0.967, p < 0.001). In the Qiang and Yi groups, participants who used toothpicks had a lower risk of cognitive impairment (Qiang: β = −0.311, p = 0.008; Yi: β = −0.499, p = 0.024). In the Uyghur group, most oral health and oral hygiene behavior factors, except for toothpaste and teeth cleaning, were not significantly associated with cognitive impairment ( p > 0.05). The disparities of SPMSQ scores among multiethnic older adults are shown in Fig. . The error rates for SPMSQ items 1, 2, 4, 6, 7, 8, and 10 were higher and more scattered than those for items 3, 5, and 9 among all ethnic groups with cognitive impairment. Moreover, item 10 had the highest error rate (Fig. a). The Yi group generally had the highest error rates across most items, whereas the Uyghur and Han groups had comparatively lower error rates among participants with cognitive impairment. The Uyghur group showed heterogeneous performance across different items, with lower error rates for items 1, 2, and 7 than for the other items in both the mild and moderate to severe cognitive impairment groups. (Fig. b and c).   In this multicenter study of 6,529 older adults from Western China, a robust correlation was found between cognitive impairment and suboptimal oral health, as well as inadequate oral hygiene behaviors. Specifically, older adults with lower self-rated oral health, fewer residual teeth, infrequent use of toothbrushes and toothpaste, and irregular dental care were more vulnerable to cognitive impairment than their counterparts were. Stratified analysis by ethnicity revealed variations in the associations between oral health, oral hygiene behaviors, and cognitive impairment. Significant correlations were primarily observed in the Han, Tibetan, Yi, and Qiang populations but not in the Uyghur group. Consistent with previous studies suggesting that maintaining more than 20 residual teeth is essential for cognitive health in older adults , our findings revealed an independent and negative association between having more than 16 residual teeth and cognitive impairment. These findings support the link between the number of residual teeth and cognitive function in older adults. Previous studies have noted that a lower number of residual teeth can impact both the diversity and quantity of food consumption . Tooth loss may lead older adults to consume fewer fruits, vegetables, nuts and meat , which are rich in omega-3 fatty acids, vitamin C, B vitamins, and tyrosine. These nutrients have been demonstrated to have neuroprotective properties . The present study also revealed that poorer nutritional status, reflected by lower MNA-SF scores, was associated with a higher risk of severe cognitive impairment, supporting the hypothesis that nutrition mediates the relationship between oral health and cognitive function . Furthermore, the loss of teeth, particularly posterior occluding teeth, impairs masticatory function in older adults , which may adversely affect cerebral blood flow and cognitive performance . Specifically, it has been reported that calculation ability is significantly and independently associated with the number of natural teeth . The current study revealed that most ethnic groups had higher error rates for item 10 (calculation ability) than for the other items did, highlighting the need for longitudinal prospective studies to further explore the causal relationships and mechanisms between the number of teeth and specific cognitive domains. In addition, inadequate use of toothbrushes and toothpaste was associated with cognitive impairment, which is consistent with the findings of previous studies . Poor oral hygiene behaviors may result in the accumulation of dental plaque and disruption of the oral biofilm, ultimately leading to further tooth loss , which may contribute to cognitive decline in older adults . Therefore, we propose that oral hygiene behaviors could be a modifiable factor for cognitive maintenance in older adults. Moreover, older adults with cognitive impairment may experience memory problems, attention deficits, and impaired motor skills  and may even be unable to express oral discomfort , which may hinder the maintenance of adequate oral hygiene behaviors and the timely treatment of oral problems , ultimately exacerbating cognitive decline. Ethnicity, encompassing differences in genomics , culture , and lifestyle habits , may further contribute to the heterogeneity of diseases development and progression . In this study, the prevalence of cognitive impairment varied among ethnic groups: 28.9% in the Yi, 19.1% in the Tibetan, 15.4% in the Qiang, and 14.3% in the Uyghur, all of which were higher than the observed 9.3% prevalence in Han individuals. This disparity may be attributed to lower income levels and a lack of healthcare knowledge among ethnic minorities, compared to the Han population . Additionally, dietary habits may constitute another contributing factor. A 14-year longitudinal study of individuals aged 80 years and above  revealed that the regular consumption of fruits, vegetables, meat, and soy products could significantly reduce the risk of cognitive impairment. However, minority groups tend to have less diverse diets and limited access to fresh vegetables, fruits and fish than the Han population does, which may contribute to their higher risk of cognitive impairment . Additionally, the Yi group presented the highest prevalence of cognitive impairment among the ethnic groups, potentially because of their stronger preference for sugary and pickled foods  and their more conservative and isolated social activities . In contrast, Uyghurs had a lower prevalence of cognitive impairment, particularly in terms of temporal orientation questions, which may be attributed to 1) a higher educational level , 2) the unique role of the Uyghur language in brain plasticity , and 3) the higher proportion of archaic introgression segments relative to other minorities , all of which may benefit the maintenance of cognitive functioning. Genetic differences may also account for the lack of significant correlations between cognitive impairment and oral health or oral hygiene behaviors among Uyghurs. Furthermore, it is important to consider that the oral microbiome affects both oral health  and cognitive function . Compared with Han and Tibetan individuals, Uyghurs have different oral colonizing bacterial species , which could impact cognition as well as oral health. Moreover, older adults with advanced age, lower educational levels, primary engagement in farming, single status, absence of longevity families, poorer nutritional status, higher consumption of spring water, and lower tea consumption were found to have a higher risk of cognitive impairment. Notably, older adults with longevity families appear to have a lower incidence of cognitive impairment than their counterparts do, which could be partially explained by genetics  or family lifestyles . In this study, individuals with cognitive impairment were less likely to report a history of smoking and alcohol use, which contrasts with findings from previous reports . However, some studies have not identified a significant association between cognition and smoking or alcohol consumption , highlighting a research gap in understanding these relationships. Although a European multinational cohort study  reported that religious rituals and prayers are associated with better cognitive functioning, our study did not find a significant relationship between religious belief and cognitive impairment. These conflicting findings may arise from variations in religious practices and the age at which individuals are exposed to religious education. Previous studies have predominantly examined the association between the oral microbiome and dementia, with relatively little focus on the relationship between early cognitive impairment and oral health or oral hygiene behaviors. This study, which targeted multiethnic older adults in Western China, explored the correlations between different domains of mild to moderate cognitive impairment and oral health or oral hygiene behaviors from the perspective of preventive healthcare. Our findings suggest that healthcare providers should routinely screen older adults for cognitive function and oral health. Additionally, the study advocated incorporating these medical services into basic health insurance plans, thereby extending coverage to older adults residing in remote and multiethnic regions. Finally, this study has several limitations. First, the cross-sectional design cannot establish a causal relationship between cognitive impairment and oral health or oral hygiene behaviors. Second, limited information on cultural, socioeconomic, and lifestyle factors necessitates caution when interpreting differences among ethnic groups. Third, the potential role of participants' income in relation to cognition was limited by its lack of inclusion. However, collecting income information is challenging because of its sensitive and private nature, particularly in many Asian countries . Fourth, given that our WHCAT cohort initially included a large sample size of 7,536 older adults, many indicators were assessed via simple and rapid tools (e.g., oral health and oral hygiene behavior variables and general cognition measured by the SPMSQ), which may limit the robustness of these findings to some extent. Therefore, future studies should incorporate long-term longitudinal follow-ups, combining both quantitative and qualitative methods, while collecting detailed cultural variables related to customs among minority groups. Additionally, including income variables, objective oral examinations (e.g., salivary microbiota and periodontal disease), and comprehensive cognitive assessments (e.g., neuropsychological assessment battery ) would enrich the study’s content and strengthen the evidence.   Inadequate oral hygiene behaviors and poor oral health are associated with cognitive impairment in multiethnic groups in Western China, with some degree of ethnic heterogeneity. Significant variations in the prevalence of cognitive impairment were also observed among these groups, potentially influenced by factors such as dietary habits and education levels. Therefore, exploring factors related to ethnic variability and promoting oral health and oral hygiene behaviors could be an alternative approach to preventing cognitive impairment among multiethnic older adults.   Supplementary Material 1.   