Abstract
Objectives
Tooth loss, which usually leads to malnutrition, is common in the elderly. However, limited information is available regarding its association with sarcopenia. This study aimed to investigate the relationship between loss of occlusal pairs of tooth and sarcopenia.
Design
A cross-sectional retrospective study was performed.
Setting
The elderly who participated in the National Basic Public Health Project in the Maigaoqiao Community Medical Center in Nanjing, Jiangsu Province, China.
Participants
A total of 2850 individuals aged ≥60 years were enrolled.
Measurements
Sarcopenia was defined according to the criteria proposed by the Asian Working Group for Sarcopenia. A trained dentist assessed oral health status and counted the number of present teeth. Logistic regression analyses were performed to evaluate the association between the loss of occlusal pairs and sarcopenia.
Results
The prevalence of sarcopenia was 7.1% (201/2850). Univariate logistic regression analysis showed that loss of occlusal pairs was associated with sarcopenia [anterior occlusal pairs (AOPs): odd ratio (OR) = 1.292, 95% confidence interval (CI) = 1.158–1.442; posterior occlusal pairs (POPs): OR = 1.147, 95% CI = 1.018–1.221]. Multivariate logistic regression analysis indicated that loss of POPs was still an independent risk for sarcopenia (OR = 1.108, 95% CI = 1.007–1.220) after adjustment for traditional confounders. Subgroup analysis showed that loss of POPs was more significantly linked to sarcopenia in those with advanced age (≥80years) (OR = 1.307, 95% CI = 1.116–1.532) and in females (OR = 1.165, 95%CI = 1.038–1.308). Compared to individuals with ≥5 occluding pairs of POPs, those with <5 occluding pairs of POPs had a higher incidence of sarcopenia.
Conclusions
Loss of POPs is associated with an increased risk of sarcopenia in the elderly in a Chinese population. Further research on the mechanism of the observed causal relationship is needed.
Key words: Tooth loss, occlusal pairs, elderly, sarcopenia
Introduction
Sarcopenia Sarcopenia is an age-related progressive disease, which leads to adverse outcomes including frailty, disabilities, poor quality of life, and mortality in the elderly (1). Malnutrition has been considered as one of the most important risk factors for the pathogenesis of sarcopenia (1). The oral cavity has various functions, including mastication, swallowing, articulation, vocalization, and breathing (2). Poor oral health problems are highly prevalent among the elderly and have been implicated as important contributors of malnutrition both in community-dwelling (3, 4) and in hospitalized older adults (5). Of note, recent studies also indicated that poor oral function could increase the risk of sarcopenia (6, 7, 8). The importance of oral function has therefore received more attention from clinicians and researchers than ever before.
Most of the current oral health studies use periodontal indexes, such as dental probing, to assess oral functional status (9). However, the differences of definitions and methods applied for determining periodontal status in different studies restrict the accuracy of research conclusions (10). By contrast, the “number of teeth lost” may be a reliable and flexible indicator of oral health status for the elderly (11). The tooth is one of the most important sections for the maintenance of normal oral function (12). Tooth loss, especially loss of occlusal pairs, can inevitably cause decreased masticatory function which in turn affects food intake and nutritional status (13). Epidemiological data showed that the annual incidence of the loss of one or more teeth ranges from 1.3% to 13.7% and the number of teeth lost varied from 3 to 38 per 100 subjects/year (14). Prevalence of complete tooth loss among adults aged ≥65 years was 12.9% and increased with age: 8.9% (ages 65–69), 10.6% (ages 70–74), and 17.8% (ages 75 and over) (15). Previous studies have demonstrated a significant association of tooth loss with frailty and cognitive impairment (16, 17). Interestingly, tooth loss is also related to low handgrip strength (8) and slow gait speed (18), both of which are key features of sarcopenia. However, to date, few studies had been performed to investigate the relationship between tooth loss and sarcopenia (19, 20). Furthermore, studies on the specific functional orientation of missing teeth are limited. Therefore, this study aimed to investigate the association of number and orientation of tooth loss with sarcopenia in a community-dwelling population of Chinese elderly.
Materials and Methods
Study participants
This study was based on the National Basic Public Health Project, which provides annual physical examinations for the elderly in China. Data were extracted from the elderly who participated in the project in the Maigaoqiao Community Medical Center in Nanjing, Jiangsu Province in 2019. In addition to the annual routine geriatric health examinations, an oral health examination and sarcopenia-related examinations were conducted. The inclusion criteria included: 1. Age ≥60 years; 2. Clear mind without eating disorder; 3. Normal hearing and speech ability; 4. Sign the informed consent form and be able to cooperate to complete the inspection. Exclusion criteria included those who had a history of malignant tumors, dementia, impaired renal function, implanted a permanent pacemaker, amputees or complete denture wearer. Finally, 2,850 individuals were included (Supplementary Figure 1). This study was performed in accordance with the principles outlined in the Declaration of Helsinki (21) and approved by the Ethics Committee of Sir Run Run Hospital, Nanjing Medical University (approval number 2019-SR-S041). Written informed consent was obtained from each participant.
Figure 1.
The relationship between incidence rate of sarcopenia and number of missing POPs. POPs, posterior occlusal pairs
Oral status assessment
A trained dentist assessed oral health status and counted the number of present teeth. We defined the maximum number of teeth as 28, excluding third molars. The total number of occlusal pairs in a healthy adult is 14.
Diagnosis of sarcopenia
Bioelectrical impedance analysis (Inbody S10) was used to measure muscle mass. Fasting was required before the examination, and participants were required to maintain a supine position for the duration. Appendicular muscle mass index (AMSI) was defined as the appendicular skeletal muscle (ASM) mass divided by height squared (ASM [kg]/height [m]2). The cutoffs for height-adjusted muscle mass are <7.0 kg/m2 in men and <5.7 kg/m2 in women. A hand dynamometer was used to measure muscle strength by taking the maximum reading of at least 2 trials using either both hands or the dominant hand in a maximum-effort isometric contraction. Low muscle strength is defined as handgrip strength <28 kg for men and <18 kg for women. Criteria for low physical performance are 6m gait speed <1.0 m/s. Sarcopenia is defined as a decrease in muscle mass with a decrease in grip strength or gait speed (22).
Nutrition evaluation
Nutritional Risk Screening 2002 (NRS 2002) was used to identify patients at risk of malnutrition. Nutritional status was divided into two classifications by the NRS 2002, where ≥3 points indicates malnutrition, 0–2 points indicates well-nourished (23). A self-administrated questionnaire was used to collect information on lifestyle, dietary behaviors, chronic disease history, and current status.
Statistical Analysis
The Kolmogorov-Smirnov test was used to test the normality of continuous variables. Independent sample t test or Mann-Whitney U test was used for continuous variables, depending on the distribution. Fisher's exact test or Chi-square test was used for categorical variables. Continuous variables were reported as mean ± standard deviation or median and interquartile range. Categorical variables were reported as frequencies and proportions. Logistic regression analysis was performed to analyzed the association between loss of occlusal pairs and sarcopenia. Odds ratios (ORs) and 95% confidence intervals (CIs) were calculated. The variance inflation factor (VIF) was used to quantify the severity of multicollinearity. Statistical analyses were performed using R software, version 3.6.2 (the R Foundation for Statistical Computing). A p-value of < 0.05 was considered statistically significant.
Results
Characteristics of participants
Among 2,850 enrolled subjects, 201 old people were diagnosed as sarcopenia (7.1%) with 6.4% in males and 7.8% in females. The subjects with sarcopenia were older and had a high prevalence of diabetes mellitus and cerebrovascular diseases, lower levels of BMI, hemoglobin, platelet, and TG, but higher levels of creatinine. Importantly, patients with sarcopenia had a higher number of missing teeth, especially the occlusal pairs, when compared to those non-sarcopenia subjects (Table 1).
Table 1.
General characteristics and oral status by sarcopenia status
| Variables | Total (n=2850) | Non-sarcopenia (n=2649) | Sarcopenia (n=201) | p |
|---|---|---|---|---|
| Age, y | 66 (63–72) | 66 (63–71) | 74 (67–81) | <0.001 |
| Males, n (%) | 1460 (51.2) | 1367 (51.6) | 93 (46.3) | 0.164 |
| BMI, kg/m2 | 24.4 (22.5–26.7) | 24.6 (22.6–26.9) | 22.5 (20.7–23.9) | <0.001 |
| Dairy products intake | ||||
| ≥3 times a week, n (%) | 1742 (61.1) | 1616 (61.0) | 126 (62.7) | 0.344 |
| NRS2002 score | ||||
| ≥3 points, n (%) | 120 (4.2) | 110 (4.2) | 10 (5.0) | 0.218 |
| Smoking history, n (%) | 524 (18.4) | 497 (18.8) | 27 (13.4) | 0.071 |
| Hypertension, n (%) | 1533 (53.8) | 1417 (53.5) | 116 (57.7) | 0.268 |
| Diabetes mellitus, n (%) | 772 (27.1) | 702 (26.5) | 70 (34.8) | 0.013 |
| Cerebrovascular diseases, n (%) | 378 (13.3) | 332 (12.5) | 46 (22.9) | <0.001 |
| Hemoglobin, g/L | 144 (135–153) | 144 (135–153) | 140 (130–150) | <0.001 |
| Platelet,×109/L | 204 (174–239) | 205 (174–239) | 192 (161–229) | 0.003 |
| Creatinine, μmol/L | 76.5±28.3 | 75.8±23.5 | 83.4±63.2 | <0.001 |
| BUN, mmol/L | 5.9±6.8 | 5.9±7.0 | 6.3±3.0 | 0.450 |
| TC, mmol/L | 4.9±1.0 | 4.9±1.0 | 4.93±1.07 | 0.610 |
| TG, mmol/L | 1.3 (1.0–1.8) | 1.3 (1.0–1.9) | 1.2 (0.9–1.7) | 0.019 |
| LDL-C, mmol/L | 2.9±0.8 | 2.9±0.8 | 2.9±0.9 | 0.649 |
| HDL-C, mmol/L | 1.37 (1.17–1.62) | 1.37 (1.16–1.62) | 1.42 (1.32–1.63) | 0.020 |
| FBG, mmol/L | 6.5±1.9 | 6.5±1.9 | 6.6±2.1 | 0.457 |
| Number of missing teeth | 1.4±3.3 | 1.3±3.0 | 2.6±5.7 | <0.001 |
| Number of missing occlusal pairs | 1.4±3.4 | 1.3±3.1 | 2.8±6.0 | <0.001 |
| ASMI, kg/m2 | 7.0 (6.3–7.7) | 7.1 (6.3–7.8) | 5.7 (5.3–6.6) | <0.001 |
| Grip strength, kg | 28.4 (22.7–37.5) | 29.0 (23.2–38.0) | 21.3 (16.7–27.2) | <0.001 |
| Gait speed, m/s | 1.1 (1.0–1.3) | 1.1 (1.0–1.3) | 0.9 (0.8–1.0) | <0.001 |
BMI, body mass index; BUN, blood urea nitrogen; TC, total cholesterol; TG, triglyceride; LDL-C, Low density lipoprotein cholesterol; HDL-C, High density lipoprotein cholesterol; FBG, fasting blood glucose; ASMI, appendicular skeletal muscle index.
Association of loss of occlusal pairs with the presence of sarcopenia
Univariate logistic regression analysis showed the extraoral factors associated with a high risk of sarcopenia included older age, lower BMI, history of diabetes mellitus and cerebrovascular diseases, lower levels of hemoglobin, platelet, and TG, and higher levels of creatine and HDL-C. Moreover, the presence of sarcopenia was also associated with the increased number of missing teeth (OR=1.079; 95%CI=1.050–1.110), missing anterior occlusal pairs (AOPs) (OR=1.292; 95%CI=1.158–1.442), and missing posterior occlusal pairs (POPs) (OR=1.147; 95%CI=1.078–1.221) (Supplementary Table1). Multivariate logistic regression analysis indicated that older age (OR=1.151; 95%CI=1.127–1.176), lower BMI (OR=0.817; 95%CI=0.778–0.857), diabetes mellitus (OR=1.434; 95%CI=1.055–1.950), higher level of creatine (OR=1.010; 95%CI=1.004–1.016) and lower level of TG (OR=0.831; 95%CI=0.699–0.989) are still independent risk factors for sarcopenia. Interestingly, although univariate logistic analysis showed that number of missing teeth was related to the risk of sarcopenia, only loss of POPs remained significant after adjustment for confounding factors (OR=1.108; 95%CI=1.007–1.220) (Table 2).
Table 2.
Multivariate logistic regression models for the sarcopenia and related characteristics
| Variables | OR (95%CI) | p |
|---|---|---|
| Age | 1.155 (1.122–1.189) | <0.001 |
| BMI | 0.775 (0.722–0.831) | <0.001 |
| Diabetes mellitus | 1.542 (1.049–2.269) | 0.028 |
| Cerebrovascular diseases | 1.057 (0.637–1.752) | 0.831 |
| Hemoglobin | 1.014 (0.999–1.029) | 0.054 |
| Platelet | 0.999 (0.996–1.003) | 0.765 |
| Creatine | 1.006 (1.002–1.010) | 0.005 |
| TG | 0.831 (0.699–0.989) | 0.037 |
| HDL-C | 1.312 (0.739–2.329) | 0.354 |
| Number of missing occlusal pairs | ||
| AOPs | 0.991 (0.814–1.205) | 0.925 |
| POPs | 1.108 (1.007–1.220) | 0.036 |
OR, odds ratio; CI, confidence interval; BMI, body mass index; TG, triglyceride; HDL-C, High density lipoprotein cholesterol. AOPs, anterior occlusal pairs; POPs, posterior occlusal pairs.
Stratified analyses were conducted according to age and sex. Multivariable logistic regression analyses indicated that loss of POPs was correlated to a high risk of sarcopenia (adjusted OR=1.307; 95%CI=1.116–1.532) in the elderly older than 80 years even after adjustment for other confounding factors. Similar results were observed in the females (adjusted OR=1.165; 95%CI=1.038–1.308) (Table 3).
Table 3.
Stratification analysis for the relationship between sarcopenia and loss of POPs
| Model 1 | Model 2 | Model 3 | |||||||
|---|---|---|---|---|---|---|---|---|---|
| OR | 95%CI | p | OR | 95%CI | p | OR | 95%CI | p | |
| Age | |||||||||
| 60–69years | 1.029 | 0.900–1.176 | 0.676 | 1.056 | 0.923–1.209 | 0.428 | 1.061 | 0.926–1.215 | 0.394 |
| 70–79years | 1.083 | 0.976–1.203 | 0.133 | 1.083 | 0.975–1.203 | 0.139 | 1.076 | 0.968–1.197 | 0.176 |
| ≥80years | 1.256 | 1.098–1.437 | 0.001 | 1.298 | 1.111–1.517 | 0.001 | 1.307 | 1.116–1.532 | 0.001 |
| Sex | |||||||||
| Male | 1.104 | 1.000–1.218 | 0.049 | 1.058 | 0.952–1.174 | 0.295 | 0.996 | 0.881–1.126 | 0.951 |
| Female | 1.178 | 1.087–1.276 | <0.001 | 1.131 | 1.131–1.199 | 0.007 | 1.165 | 1.038–1.308 | 0.009 |
Model 1, unadjusted; Model 2, adjusted for BMI, and sex (for age stratification analysis) or age (for sex stratification analysis); Model 3, adjusted for BMI, diabetes mellitus, cerebrovascular diseases, hemoglobin, platelet, creatine, TG, HDL-C, and sex (for age stratification analysis) or age (for sex stratification analysis); OR, odds ratio; CI, confidence interval; POPs, posterior occlusal pairs.
Association of loss of POPs with the severity of sarcopenia
By using the locally weighted regression (loess) method, we found that the cutoff value of the number of missing POPs for the prediction of sarcopenia was 5 pairs (p=0.036; 95%CI=1.007–1.220). The incidence rate of sarcopenia significantly increased when the number of missing POPs was ≥ 5 pairs (Figure 1). When compared to those with fewer missing POPs, the elderly with more than 5 pairs of missing POPs were older and had a higher risk of malnutrition as indicated by higher NRS 2002 scores. Moreover, the elderly with more missing POPs had a higher prevalence of sarcopenia, along with lower grip strength, gait speed, and ASMI (Table 4). Interestingly, the elderly with more missing POPs also had a higher proportion of severe sarcopenia (21.7% vs. 19.3%).
Table 4.
Association of loss of POPs with sarcopenia
| Number of missing POPs | |||
|---|---|---|---|
| 1–4 (n=786) | 5–8 (n=152) | p | |
| Age, y | 66 (63–72) | 70 (65–76) | <0.001 |
| Male, n (%) | 415 (54.1) | 72 (47.4) | 0.414 |
| BMI, kg/m2 | 24.6 (22.7–26.9) | 24.4 (22.3–26.3) | 0.113 |
| NRS 2002 score | 1 (0–1) | 1 (0–1) | 0.003 |
| Eat the following foods ≥3 times a week | |||
| Dairy products, n (%) | 310(39.4%) | 69(45.4%) | 0.629 |
| Fruits, n (%) | 315(40.1%) | 73(48.0%) | 0.884 |
| Nuts, n (%) | 118(15.0%) | 30(19.7%) | 0.242 |
| Sarcopenia, n (%) | 57(7.3%) | 23(15.1%) | <0.001 |
| Upper extremity sarcopenia, n (%) | 15(1.9%) | 8(5.3%) | 0.054 |
| Lower extremity sarcopenia, n (%) | 118(15.0%) | 28(18.4%) | <0.001 |
| Severe sarcopenia, n (%) | 11(1.4%) | 5(3.3%) | 0.046 |
BMI = body mass index; POPs, posterior occlusal pairs.
Discussion
With global population aging, more and more attention has been paid to the health problems of the elderly. Recently, clinical and research focused on sarcopenia has burgeoned internationally. The prevalence of sarcopenia in our present study population aged ≥60 years is 7.1%, which generally coincides with the prevalence of sarcopenia in Asian countries ranged from 5.5% to 25.7% (22). Similarly, according to the report of European Working Group on Sarcopenia in Older People (EWGSOP), the prevalence in 60–70 years elderly is 5–13%, while the prevalence increases from 11 to 50% in subjects older than 80 years (24, 25). Although a variety of risk factors have been identified for sarcopenia, we here showed for the first time that loss of POPs was correlated with the risk and severity of sarcopenia in a community-dwelling population of Chinese elderly. Our results therefore further highlight the importance of dental status which is likely to be overlooked in general health among the elderly.
Mastication is regarded as the most important function of the stomatognathic system, including crushing, grinding, and mixing food with saliva (26). In theory, the food bitten by incisors and torn by canines is transported by the tongue to the premolars and molars, and then crushed and grinded by posterior teeth. Morphologically, the occlusal surface of molars is composed of many grooves and ridges, which are conducive to grating food. Premolars may play a significant role in crushing food; however, the role may not be as large as molars (27). Therefore, missing POPs could abate chewing ability, leading to changes in food choices as a consequence of the decreased pleasure in eating (28). Indeed, people with fewer teeth have a significant tendency to eat fewer vegetables, fruits, fiber, protein, vitamins, and minerals (29, 30, 31), most of which are important for the maintenance of muscle mass and physical performance (32, 33, 34, 35). Our results showed the NRS 2002 score was higher in the population with more POPs missing, indicating a higher nutritional risk. Besides, periodontitis and tooth anomalies have been reported to be related to a reduction in the number of erythrocytes and hemoglobin, leading to anemia eventually (36). Therefore, the association of loss of POPs with sarcopenia may also attribute to anemia, which reduces the oxygen-carrying capacity of the blood, potentially restricting oxygen delivery and limiting the synthesis of new proteins (37).
The exact mechanism of the relationship between dental number abnormity and sarcopenia remains unclear; however, there are several possible explanations. One of the hallmarks of aging is chronic low-grade sterile inflammation, which is closely linked to age-related diseases (38). Recent evidence demonstrated that inflammatory cytokines like interlukine-6 (IL-6) and tumor necrosis factor-α (TNF-α) might activate many of the molecular pathways related to skeletal muscle wasting (39). A previous study showed that A20, a protein encoded by the TNF-α-induced protein 3 gene (TNFAIP3), is a ubiquitin-editing enzyme that mainly functions through the termination of nuclear factors (NF)-ϰB activation (40). Intriguingly, A20 has also been implicated as an essential endogenous regulator of inflammatory reaction in the oral cavity, particularly in the pathogenesis of periodontitis (41). Coincidentally, it was reported that the major cause of tooth loss in the middle-aged and elderly is periodontitis (42). Moreover, we also found that the elderly with more missing POPs also had a higher proportion of severe sarcopenia. A cohort of community-dwelling elderly subjects with higher IL-6 levels was associated with slow gait at baseline and faster decline in gait speed (43), illustrating the loss of POPs probably set off muscle hypofunction through inflammatory mediators. Further studies based on animal and cell models are required to elucidate the precise mechanism governing the pathological impact of missing POPs on the onset and progression of sarcopenia.
Although our study demonstrated a correlation of miss POPs with sarcopenia, there are still some limitations. Firstly, it was hard to exclude the possibility of causality bias as a result of the cross-sectional nature. Thus, further studies with more diverse regions will be needed to corroborate our findings. Secondly, other indicators related to oral conditions, such as community periodontal index and occlusal force, were not evaluated in our study. Thirdly, we did not estimate the connection between missing POPs and markers of systemic inflammation to verify the hypothesis that tooth loss leads to severe sarcopenia through an inflammatory pathway.
Conclusions
In conclusion, the present study showed a correlation between missing POPs and the severity of sarcopenia among community-dwelling Chinese elderly individuals. The advanced-aged female groups with loss of POPs should be more alert to the occurrence of sarcopenia. Improving long-term oral health should be taken into consideration for the prevention of sarcopenia in the elderly.
Acknowledgments
The authors would like to thank the participating elderly and the clinicians who conducted the physical examination.
Contributor Information
Jin-Shui Xu, Email: 353112354@qq.com.
Wei Gao, Email: gaowei84@njmu.edu.cn.
Ethical standards
The protocol of present study confirmed by the Medical Ethics Committee at the Shoushtar Faculty of Medical Sciences, considering to the 2013 Helsinki Declaration guidelines with registration Number: (IR.SHOUSHTAR.REC.1399.027). All participants also signed a consent form.
Conflict of interest
The authors declare no conflicts of interest.
Funding Sources
This work was supported by grants from the National Key Research and Development Plan of China (No. 2020YFC2008505 to Xiang Lu), the National Natural Science Foundation of China (No. 81970218 to Xiang Lu and No. 81970217 to Wei Gao), the Six Talent Peaks Project of Jiangsu Province (No. WSN- 175 to Wei Gao), and Jiangsu Geriatrics Society (JGS2019ZXYY06 to Xiang Lu).
Electronic Supplementary Material
Supplementary material is available for this article at https://doi.org/10.1007/s12603-022-1784-x and is accessible for authorized users.
Supplementary material, approximately 1.46 MB.
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