Abstract
Objective
Although masticatory performance is affected by age-related reduction in number of teeth (or treatment), the relationship between longitudinal changes in masticatory performance and diabetes mellitus is unknown. This longitudinal study investigated the association between changes in masticatory performance and new-onset diabetes mellitus among community-dwelling Japanese older adults.
Methods
The data of 214 older adults living in Ohnan Town, Shimane, Japan, who participated in two surveys conducted between 2012 and 2017 were analyzed. Diabetes mellitus was defined as a hemoglobin A1c level ≥ 6.5% or self-reported diabetes mellitus. The masticatory performance (measured by number of gummy jelly pieces collected after chewing) was evaluated by dental hygienists. Masticatory performance was categorized into two groups (high or low) based on the median in each survey; further, four groups (Group A: remained consistently high, Group B: changed from low to high, Group C: remained consistently low, Group D: changed from high to low) were used to determine longitudinal changes in masticatory performance. Logistic regression was used to analyze the association between changes in masticatory performance and new-onset diabetes mellitus.
Results
Overall, 10.3% of participants had diabetes mellitus at the follow-up survey. Multivariate analysis showed that Group D (odds ratio 8.69, 95% confidence interval 1.98–38.22) was positively associated with the development of diabetes mellitus compared with Group A after adjusting for sex, age, body mass index, alcohol consumption, physical activity, and eating speed.
Conclusions
Deteriorating masticatory performance for 5 years may cause diabetes mellitus among older adults.
Keywords: Masticatory performance, Diabetes mellitus, Periodontal disease, Longitudinal study
Introduction
Periodontal disease reportedly worsens the oral environment resulting in a reduction in the number of teeth [1]. A reduced number of teeth inhibits the ability to chew food [2] and worsens nutritional status [3, 4]. For example, avoiding fruits and vegetables leads to a chronic lack of nutrients, such as dietary fiber and vitamins, and a preference for refined carbohydrates for their softness [5–7]. Thus, the poor oral environment could exacerbate diabetes mellitus by causing in the individual’s diets. Masticatory performance is an aspect of the oral environment that is affected by periodontal disease and the number of teeth. Although lost teeth can never be regained, masticatory performance can be corrected with suitable treatment, including implants or dental bridges.
An interventional study with a crossover design found a short-term relationship between mastication and glucose metabolism [8]. In this study, thorough mastication induced lower postprandial plasma glucose concentration by enhancing insulin secretion. This finding suggests that favorable masticatory performance can prevent the onset of diabetes mellitus by improving postprandial glucose metabolism. Previous studies demonstrated that favorable masticatory performance is associated with the prevention of diabetes mellitus [9, 10]. However, this finding is limited to evidence-based on cross-sectional studies. Furthermore, masticatory performance is affected by an age-related reduction in the number of teeth (or treatment), which can change over time. Masticatory performance over time can be classified into four categories: consistently high performance, improved performance, consistently low performance, and deteriorated performance. Thus, compared to individuals with consistently high masticatory performance, individuals with consistently low performance or deteriorated performance may be at an increased risk of developing diabetes mellitus. Therefore, we aimed to determine how longitudinal changes in masticatory performance are related to diabetes mellitus in community-dwelling older adults by conducting a 5-year longitudinal study.
Materials and methods
Study design
The present longitudinal study was conducted as part of the Shimane Center for Community-Based Healthcare Research and Education (CoHRE) study in Ohnan Town (as of 2020, area: 419 km2, population: 10,163), Shimane, Japan, based on the guidance of the Ministry of Health, Labor and Welfare in collaboration with specific health checkups conducted by the local government [11]. Residents were informed about the study at least once before it began. They provided signed consent to participate in the study after receiving written and oral explanations of the study. The study protocol was approved by the Medical Research Ethics Committee, Shimane University Faculty of Medicine (#20051214-3).
Study population
The inclusion criteria for the present study included participants residing in Ohnan Town and having participated in the survey in June−July 2012 (baseline) and June−July 2017 (follow-up). Figure 1 presents a flowchart of the study. The baseline survey included 517 participants; the follow-up survey only included 240 of these participants, as the other 277 did not participate. After excluding 26 participants with missing data and diabetes mellitus at baseline survey, we included 214 participants in the analysis. The basic characteristics of the included and excluded participants (n; 214 vs. 303) were compared (age, sex, body mass index [BMI], hemoglobin A1c [HbA1c], and masticatory performance); however, no statistically significant differences were observed in the age (mean; 62.5 vs. 62.1 years, P = 0.50), sex (men; 40.2 vs. 40.3%, P = 0.99), and BMI (mean; 22.6 vs. 23.1 kg/m2, P = 0.08). HbA1c (mean; 5.7 vs. 5.9%, P < 0.001) and masticatory performance (median; 24.5 vs. 17 pieces, P = 0.001) were significantly different between the included and excluded participants.
Fig. 1.
Flowchart of the study
Measurements
We assessed diabetes mellitus in the baseline and follow-up surveys. HbA1c was assessed as the standard item in specific health checkups [11]. Diagnosis of diabetes mellitus by a physician (yes or no) was determined through face-to-face interviews by trained nurses or public health nurses during health checkups [11]. Diabetes mellitus was defined as HbA1c levels ≥ 6.5% (NGSP) or diabetes mellitus diagnosis by a physician, based on self-reporting [12].
Oral health status in terms of the masticatory performance was assessed in the baseline and follow-up surveys by trained dental hygienists. Masticatory performance was assessed based on the number of gummy jelly pieces ≥ 3 mm in size, collected 15 s after they were chewed with maximal effort [10, 13]. Based on the median number of pieces, the participants were divided into two masticatory performance groups at the baseline (high: ≥ 24.5 pieces and low: < 24.5 pieces) and follow-up (high: ≥ 27 pieces and low: < 27 pieces) surveys. Changes in masticatory performance were categorized into four groups from baseline to follow-up surveys as follows: Group A: remained high (as consistently high performance), Group B: low to high (as improved performance), Group C: remained low (as consistently low performance), Group D: high to low (as deteriorated performance).
The parameters of sex (male/female) and age were used as basic characteristics. In addition, the following specific health checkup measurements were used: smoking was assessed as “yes” or “no”; alcohol consumption was assessed according to participants’ responses to the question, “How often do you drink alcohol?” (Never or rarely/sometimes/daily); physical activity was assessed based on responses to the question, “Do you walk or engage in equivalent physical activity for at least one hour per day?” (yes/no); eating speed was assessed with the question, “How fast do you eat compared to others around the same age?” (faster/normal/slower) and based on these responses, participants were classified as fast or not fast [14]; BMI was calculated by dividing body weight with the square of height (kg/m2).
Statistical analyses
For the characteristics of the study participants at baseline survey by diabetes mellitus status, frequency data are reported as numbers and percentages, and continuous data are presented as mean ± standard deviation (SD) or median and interquartile range. Cases and percentages of new-onset diabetes mellitus were calculated separately by masticatory performance status during each survey. The associations between diabetes mellitus and masticatory performance status were analyzed using the Chi-squared (χ2) test. Logistic regression analysis was used to examine new-onset diabetes mellitus in the four groups (Group A = reference, Group B, Group C, and Group D) after adjusting in Model 1 (crude model), Model 2 (after adjusting for sex, age, and BMI), Model 3 (Model 2, or Model 2 plus alcohol consumption, physical activity, and eating speed), and Model 4 (Model 3, or Model 3 plus HbA1c). In this case, since the events per predictor variables were few, we confirmed the goodness-of-fit of each model using the Hosmer–Lemeshow test [15]. Statistical analyses were conducted using the software Stata/BE17.0. The level of statistical significance was defined as P < 0.05.
Results
Characteristics of the study participants
Characteristics of the study participants (n = 236) at baseline survey are shown in Table 1. At baseline, the participants were 62.9 ± 7.0 years old; they included 138 females (58.5%) and 98 males (41.5%). The number of cases and percentages of diabetes mellitus were 22/236 (9.3%) at the baseline and 22/214 (10.3%) at the follow-up surveys. Among the analyzed participants (n = 214), the median number of gummy jelly pieces at the baseline and follow-up surveys were 24.5 and 27, respectively. Participants were divided into four groups based on masticatory performance: Group A (remained high), Group B (changed from low to high performance), Group C (remained low), and Group D (changed from high to low performance), including 86 (40.2%), 26 (12.1%), 79 (36.9%), and 23 (10.7%) participants, respectively. The mean and SD values of HbA1c were 5.6 ± 0.3%.
Table 1.
Characteristics of study participants at baseline survey
| Variables | Total (N = 236) | Diabetes mellitusc at baseline | Diabetes mellitusc at follow-up | |||
|---|---|---|---|---|---|---|
| No (n = 214) | Yes (n = 22) | No (n = 192) | Yes (n = 22) | |||
| Mean (SD), median (IQR), n (%) | Mean (SD), median (IQR), n (%) | Mean (SD), median (IQR), n (%) | Mean (SD), median (IQR), n (%) | Mean (SD), median (IQR), n (%) | ||
| Age, years | Mean, SD | 62.9 (7.0) | 62.5 (7.1) | 66.1 (4.6) | 62.5 (7.3) | 63.1 (5.5) |
| Sex | Female; n, % | 138 (58.5) | 128 (59.8) | 10 (45.5) | 117 (60.9) | 11 (50.0) |
| Body mass index, kg/m2 | Mean, SD | 22.7 (3.2) | 22.6 (3.1) | 24.0 (4.3) | 22.4 (3.0) | 24.0 (3.1) |
| Smoking | Yes; n, % | 30 (12.7) | 26 (12.1) | 4 (18.2) | 23 (12.0) | 3 (13.6) |
| Alcohol consumption | Sometimes; n, % | 50 (21.2) | 47 (22.0) | 3 (13.6) | 44 (22.9) | 3 (13.6) |
| Daily; n, % | 72 (30.5) | 66 (30.8) | 6 (27.3) | 58 (30.2) | 8 (36.4) | |
| Physical activity | Yes; n, % | 96 (40.7) | 88 (41.1) | 8 (36.4) | 81 (42.2) | 7 (31.8) |
| Eating speed | Not fast; n, % | 172 (72.9) | 160 (74.8) | 12 (54.5) | 148 (77.1) | 12 (54.5) |
| Masticatory performancea | ||||||
| At baseline | Median, IQR | 23 (9, 33) | 24.5 (10, 33) | 18 (5, 24) | 25 (10, 34) | 19.5 (5, 32) |
| At follow-up | Median, IQR | 27 (17, 35) | 27 (17, 35) | 21.5 (13, 28) | 28 (17.5, 36) | 23 (7, 30) |
| Changes in masticatory performanceb | Group A; n, % | 90 (38.1) | 86 (40.2) | 4 (18.2) | 82 (42.7) | 4 (18.2) |
| Group B; n, % | 28 (11.9) | 26 (12.1) | 2 (9.1) | 24 (12.5) | 2 (9.1) | |
| Group C; n, % | 93 (39.4) | 79 (36.9) | 14 (63.6) | 69 (35.9) | 10 (45.5) | |
| Group D; n, % | 25 (10.6) | 23 (10.7) | 2 (9.1) | 17 (8.9) | 6 (27.3) | |
| HbA1c, % | Mean, SD | 5.7 (0.5) | 5.6 (0.3) | 6.8 (0.5) | 5.6 (0.3) | 6.1 (0.3) |
| Self-reported diabetes mellitus | Yes; n, % | 16 (6.8) | 0 (0) | 16 (72.7) | 0 (0) | 0 (0) |
SD standard deviation, IQR interquartile range
aMasticatory performance (high or low) was categorized by the median, assessed using the number of chewed gummy jelly pieces
bChanges in masticatory performance were based on masticatory performance (high or low) from baseline to follow-up survey, categorized as follows: Group A: stay high, Group B: low to high, Group C: stay low, Group D: high to low
cDiabetes mellitus was defined as an HbA1c value ≥ 6.5% or self-reported diabetes mellitus
Associations between the masticatory performance status and diabetes mellitus
Table 2 shows the results of the associations between masticatory performance status and diabetes mellitus in participants without diabetes mellitus at baseline (n = 214). Although a significant difference was not observed between new-onset diabetes mellitus at baseline (P = 0.59) and masticatory performance (high or low) at baseline, there was a significant difference between new-onset diabetes mellitus in the masticatory performance groups (Groups A, B, C, and D = 4.7%, 7.7%, 12.7%, and 26.1%, respectively; P = 0.02).
Table 2.
The associations between masticatory performance and new-onset diabetes mellitus among Japanese older adults without diabetes mellitus at baseline (n = 214)
| Diabetes mellitusa, cases/n | |||
|---|---|---|---|
| Follow-up | % | P value | |
| (New onset) | |||
| Masticatory performance at baselineb | |||
| High | 10/109 | 9.2 | 0.59 |
| Low | 12/105 | 11.4 | |
| Changes in masticatory performancec | |||
| Group A | 4/86 | 4.7 | 0.02 |
| Group B | 2/26 | 7.7 | |
| Group C | 10/79 | 12.7 | |
| Group D | 6/23 | 26.1 | |
aDiabetes mellitus was defined as an HbA1c value ≥ 6.5% or self-reported diabetes mellitus
bMasticatory performance (high or low) was categorized by the median of the number of chewed gummy jelly pieces
cChanges in masticatory performance were based on masticatory performance (high or low) from baseline to follow-up survey, categorized as follows: Group A: stay high, Group B: low to high, Group C: stay D low, Group: high to low
Diabetes mellitus was examined using the χ2 test
Longitudinal associations between the changes in the masticatory performance and new-onset diabetes mellitus among Japanese older adults
Table 3 shows the association between the changes in the masticatory performance and new-onset diabetes mellitus in participants without diabetes mellitus at baseline. Considering the common results from Model 1 to Model 3, there were significant associations between new-onset diabetes mellitus and Group D (OR 7.24 to 8.69) with reference to Group A. In Model 4, Group B (OR 12.44; 95% CI 1.16–133.75) and Group D (OR 17.36; 95% CI 2.03–148.55) were associated with new-onset diabetes mellitus compared with Group A. P values based on the Hosmer–Lemeshow test indicated 1.00, 0.62, 0.42, and < 0.001 in Models 1, 2, 3, and 4, respectively.
Table 3.
The longitudinal association between changes in masticatory performance and new-onset diabetes mellitus among Japanese older adults without diabetes mellitus at baseline (n = 214)
| Model 1† | Model 2‡ | Model 3§ | Model 4§ | |||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| OR | (95% CI) | P value | OR | (95% CI) | P value | OR | (95% CI) | P value | OR | (95% CI) | P value | |
| Changes in masticatory performancea | ||||||||||||
| Group A | 1.00 | (reference) | 1.00 | (Reference) | 1.00 | (Reference) | 1.00 | (Reference) | ||||
| Group B | 1.71 | (0.29, 9.90) | 0.55 | 1.85 | (0.31, 10.99) | 0.50 | 1.70 | (0.27, 10.53) | 0.57 | 12.44 | (1.16, 133.75) | 0.04 |
| Group C | 2.97 | (0.89, 9.89) | 0.08 | 2.89 | (0.84, 9.97) | 0.09 | 3.18 | (0.89, 11.30) | 0.07 | 4.93 | (0.92, 26.60) | 0.06 |
| Group D | 7.24 | (1.84, 28.43) | < 0.01 | 7.79 | (1.88, 32.25) | < 0.01 | 8.69 | (1.98, 38.22) | < 0.01 | 17.36 | (2.03, 148.55) | < 0.01 |
| Hosmer–Lemeshow testb | 1.00 | 0.62 | 0.42 | < 0.001 | ||||||||
Diabetes mellitus outcome was analyzed with changes in masticatory performance using logistic regression. Analyses were conducted in Model 1† (crude model), Model 2‡ (after adjusting for sex, age, and body mass index), Model 3§ (Model 2, or Model 2 plus alcohol consumption, physical activity, and eating speed), and Model 4§ (Model 3, or Model 3 plus HbA1c
OR Odds ratio, CI confidence interval
aChanges in masticatory performance were based on masticatory performance (high or low) from baseline to follow-up survey, categorized as follows: Group A: stay high, Group B: low to high, Group C: stay low, Group D: high to low
bThe Hosmer–Lemeshow test is a statistical test for goodness-of-fit for logistic regression models
Discussion
The present study used a longitudinal design to examine the association between the changes in the masticatory performance and diabetes mellitus over a period of 5 years among community-dwelling Japanese older adults. The main findings of our study were as follows: in the multivariate model that was adjusted for sex, age, BMI, alcohol consumption, physical activity, and eating speed, the group with deteriorated performance (Group D) demonstrated a significantly high prevalence of diabetes mellitus after 5 years compared to the group with consistently high performance (Group A). Model 4 (all-adjusted model) showed that the group with deteriorated performance (Group D) demonstrated a significantly high prevalence of diabetes mellitus after 5 years compared to the group with consistently high performance (Group A), although the Hosmer–Lemeshow test showed that the model had no goodness-of-fit. Thus, our findings suggested that long-term maintenance of favorable masticatory performance may effectively prevent diabetes mellitus.
Considering diabetes mellitus prevention from a long-term perspective, masticatory performance, which affects nutritional status, is a crucial factor that can be improved with standard dental treatments, such as the elimination of toothaches and fabrication of dental prostheses [3, 16, 17]. Two previous cross-sectional studies reported that masticatory function is negatively associated with diabetes mellitus [9, 10]. While our results corroborate the results of these previous studies, we could not find any long-term studies reporting the relationship between the changes in the masticatory ability and diabetes mellitus. Fushida et al. reported that lower masticatory performance at baseline is associated with the development of metabolic syndrome and high fasting plasma glucose in Japanese men [18]. Although the methodology in this study was different from that of the previous studies, our findings supported the notion that poor masticatory performance is related to the development of diabetes mellitus. Therefore, establishing an objective masticatory performance change as a novel indicator of the oral environment may be effective in long-term strategies for preventing diabetes mellitus.
One of our findings was that, similar to the participants in Group C, 36.9% of the individuals suffer from consistently deteriorated the masticatory performance. When many teeth are lost (e.g., when the number of remaining teeth is less than 20), standard dental treatment is unlikely to restore masticatory performance to that of the level of natural teeth [2]. When the loss of remaining teeth hinders mastication, dietary options are limited, thereby impeding nutrition intake [3, 4]. This type of poor oral environment may adversely affect nutrition education for diabetes mellitus. Therefore, nutrition education for diabetes mellitus must consider the oral environment. For patients with particularly weakened masticatory function, early treatment to restore masticatory function leads to improved dietary habits with nutrition education [3].
In the group with deteriorated performance, the long-term relationship with diabetes mellitus could be attributed to several potential mechanisms. First, a reduced number of teeth hinder the chewing of food [2], which is known to worsen nutritional status [4, 19]. Poor nutritional status, such as avoiding fruits and vegetables, leads to a chronic deficiency of micronutrients, such as dietary fiber and vitamins and a preference for refined carbohydrates owing to their softness [5–7]. Chronic deficiency of dietary fiber and magnesium reduces insulin secretion, thereby potentially increasing the risk of diabetes mellitus. Second, periodontal disease could, directly and indirectly, trigger diabetes mellitus. Periodontal disease results in the development and progression of diabetes mellitus; it also leads to the migration of inflammatory chemicals from the periodontal pockets to the bloodstream, diminishing the action of insulin, which reduces the blood glucose levels in the body [20]. Periodontal disease and diabetes mellitus are known to be interrelated [21]. Diabetes mellitus enhances periodontal disease [22] and may trigger a decline in the masticatory function associated with a reduction in the number of teeth. Thus, periodontal disease-induced worsening of the oral environment with the simultaneous progression of diabetes mellitus should be considered.
Limitations
The present study had certain limitations. This study showed that the percentage of diabetes mellitus was 9.3% at baseline and 10.3% at the follow-up survey in our participants. The National Health and Nutrition Survey in Japan, 2019, reported that the prevalence of strongly suspected diabetes mellitus ranged from 10.7 to 26.4% in older adults aged 60 years and over [23]. The DeSC database showed a definite diagnosis rate of approximately 19% for diabetes mellitus among older adults aged 60 years and over in Japan [24]. Although the prevalence of diabetes mellitus was within the national data range, this study could contain an inclusion bias. For example, excluded participants in this study had a lower masticatory performance (median; 17 vs. 24.5 pieces) and higher HbA1c (mean; 5.9 vs. 5.7%) compared to the analyzed participants. Therefore, the exclusion of these data may lead to result in underestimate associations between diabetes mellitus and masticatory performance. In addition, the sample size was small, which reduced the statistical power and consequently may have underestimated the analysis results. Therefore, generalization of our results will require further investigation with larger sample sizes. However, a longitudinal study with a large sample size would likely be time-consuming and expensive; thus, our longitudinal study findings could be useful. One of the strengths of the present study is that comminution tests with gummy jellies are a simple and objective method of assessing masticatory performance [25]. However, the gummy jellies used in the tests were not made for testing purposes but were developed for chewing training. Gummy jellies vary in hardness depending on the year they are produced. Therefore, by classifying participants into high and low groups for both individual survey years, we treated the change in masticatory performance as an explanatory variable categorized in relative terms (high group or low group). Thus, it is difficult to generalize our findings to settings not studied. In addition, we had no information regarding latent confounders that affect the relationship between masticatory performance and diabetes mellitus; these latent confounders consist of periodontal disease [21, 26, 27], dental caries [28], dental treatment during follow-up [29–31], and lifestyle-related diseases [32]. Future studies must consider these latent effects.
Conclusion
In conclusion, investigation of the longitudinal association between changes in masticatory performance over 5 years and diabetes mellitus revealed that diabetes mellitus was significantly more common among individuals with deteriorated masticatory performance than among individuals with consistently high masticatory performance. This finding suggests that individuals whose masticatory performance deteriorates over time and individuals with consistently low masticatory performance require dental treatment and other interventions to prevent diabetes mellitus over the long term.
Acknowledgements
We greatly appreciate the cooperation from participants in Ohnan Town and thank the Shimane CoHRE study members for their skillful assistance.
Author contributions
MI and TN organized and conducted the study. TA. and TH. collected data. KT, TA, and SY performed the statistical analysis, interpreted the results, proposed the structure of the paper, and formulated the paper. YA and TH made substantial contributions to the data analysis and draft revision. MI and TN critically appraised the paper and made final suggestions. All the authors reviewed and revised the manuscript and agreed to the submission of the final manuscript.
Funding
This study was supported by the Japan Society for the Promotion of Science (KAKENHI; Grant number 16K13029). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Data availability statement
Data are available upon reasonable request. This study used data from the Shimane CoHRE (Center for Community-Based Healthcare Research and Education) study. Some of the data are available from the CoHRE, Organization for Research and Academic Information, Shimane University, 223–8 Enya-cho, Izumo-shi, Shimane 693–8501, Japan.
Declarations
Conflict of interest
Kazumichi Tominaga, Takafumi Abe, Yuichi Ando, Tsuyoshi Hamano, Minoru Isomura, Toru Nabika, and Shozo Yano declare that they have no conflicts of interest.
Human rights
All the procedures followed were in accordance with the ethical standards of the Medical Research Ethics Committee, Shimane University Faculty of Medicine (May 11, 2017/#20051214-3) and with the Helsinki Declaration of 1964 and later versions.
Informed consent to participate
Residents provided consent via signature to participate in the study after receiving written and oral explanations of the study.
Footnotes
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
Data are available upon reasonable request. This study used data from the Shimane CoHRE (Center for Community-Based Healthcare Research and Education) study. Some of the data are available from the CoHRE, Organization for Research and Academic Information, Shimane University, 223–8 Enya-cho, Izumo-shi, Shimane 693–8501, Japan.