Abstract
Background/purpose
We suspected that there might be an interaction between sugar intake and tobacco exposure on the risk of dental caries. The study aimed to investigate the associations of sugar intake or tobacco exposure with the risk of dental caries.
Materials and methods
This cross-sectional study obtained data of 18804 participants from National Health and Nutrition Examination Survey (NHANES) between 2011 and 2018. Weighted univariable and multivariable logistic regression models were applied to explore the associations of total sugar intake or tobacco exposure with the risk of dental caries. The relative excess risk of interaction (RERI), attributable proportion of interaction (API), and synergy index (SI) evaluated the interaction between total sugar intake and tobacco exposure on the risk of dental caries. The effect size of odds ratio (OR), and 95% confidence interval (CI) was inputted.
Results
The OR of dental caries in adults with cotinine >10 ng/mL was 1.59 (95%CI: 1.38–1.82). The increased risk of dental caries was found in people with total sugar >19.5%E compared to those with total sugar ≤19.5%E (OR = 1.55, 95%CI: 1.34–1.78). Compared to people with cotinine ≤10 ng/mL and total sugar ≤19.5%E, adults with cotinine >10 ng/mL and total sugar >19.5%E were correlated with elevated risk of dental caries (OR = 2.76, 95%CI: 2.29–3.33). The interaction indicators RERI was 0.980 (95%CI: 0.413–1.547), API was 0.355 (95%CI: 0.192–0.517), and SI was 2.250 (95%CI: 1.344–3.767).
Conclusion
There might be interaction between sugar intake and tobacco exposure on the occurrence of dental caries in adults.
Keywords: Sugar intake, Tobacco exposure, Dental caries
Introduction
Dental caries, also known as dental cavities or tooth decay, is a global public health problem and poses a substantial economic burden all over the world.1 The Global Burden of Disease Study revealed that untreated caries exhibited the highest prevalence impacting about 3.1 billion individuals worldwide among the 291 medical conditions assessed.2,3 Dental caries can cause pain and discomfort, and eventually lead to tooth loss, which results in a major impact on quality of life and high costs for individuals, families and society.4 To identify more modifiable risk factors associated with the risk of dental caries is necessary for the management of this disease.
High sugar intake was widely accepted as an important risk factor for dental caries, and there is a dose-response relationship between sugar and sugar-sweetened beverage intake and the risk of dental caries.5 On the other hand, dental caries is regarded as a non-communicable disease, and factors associated with a non-communicable disease were considered to be related to dental caries.6 There were studies demonstrated that smoking was associated with an increased risk of dental caries.7,8 In addition, the results of a study in children showed that compared with the control group, the decayed, missing and filled tooth (DMFT) score, the colonization amount of Streptococcus mutans and Lactobacillus in saliva were increased, and the pH value, flow rate and buffer capacity of saliva were decreased in passive smoking children.9 This may be due to increased tooth adhesion by Streptococcus mutans, an important cariogenic bacterium metabolizing sucrose in the presence of nicotine.10 Therefore, we suspected that there might be an interaction between sugar intake and tobacco exposure on the risk of dental caries.
This aim of our study was to investigate the associations of sugar intake or tobacco exposure with the risk of dental caries in adults using the data from National Health and Nutrition Examination Survey (NHANES). Whether there was an interaction between sugar intake and tobacco exposure on the risk of dental caries was also evaluated. Subgroup analysis was performed in participants in different age, gender and body mass index (BMI) groups.
Materials and methods
Study design and population
This cross-sectional study obtained the data of 21501 participants aged ≥18 years with dental status data from the NHANES between 2011 and 2018. The NHANES is a continuous study evaluating the nutrition and health of adults and children in the U.S using a stratified, multistage probability design. The survey obtained the data via personal structured interviews at home, health examinations at a mobile examination center, and specimen analyses in the laboratory.11 The records of participants were extracted if they met the following criteria: 1) ≥ 18 years; 2) with data on total sugar intake; 3) with data on serum cotinine; 4) with the measurement for coronal caries. Those without data of important covariates were excluded. Finally, 18804 participants were included. The requirement of ethical approval for this was waived by the Institutional Review Board of The Affiliated Nantong Stomatological Hospital of Nantong University, because the data was accessed from NHANES (a publicly available database). The need for written informed consent was waived by the Institutional Review Board of The Affiliated Nantong Stomatological Hospital of Nantong University due to retrospective nature of the study.
Potential confounding factors
Age (years), gender (male or female), race (non-Hispanic White, non-Hispanic Black or others), education (<high school, high school, or > high school), poverty-to-income ratio (PIR) (<1.0, or ≥1.0), drinking (<once/week, or ≥ once/week), physical activity [<450 metabolic equivalent of task (MET) × minutes/week, ≥450 MET × minutes/week, or unknown), hypertension or not, diabetes or not, dyslipidemia or not, cardiovascular disease (CVD) or not, bone loss around teeth or not, body mass index (BMI) (kg/m2), white blood cell (WBC) (1000 cells/uL), carbohydrate (gm), fiber intake (gm), last dental visit (<1 year, 1–5 years, or ≥5 years), dental care or not, and frequency of using dental floss (<7 times/week, ≥7 times/week or unknown) were covariates analyzed in this study.
Main and outcome variables
Tobacco exposure was one of the main variables, which was evaluated based on the serum cotinine level. According to the previous studies, the serum cotinine cut-off value of active smoking is 10 ng/mL.12 Total sugar intake was another main variable, which was calculated based on the first day's energy intake and supplement energy intake. The data were converted into energy supply ratio via total sugar × 4/total energy × 100 (%E). Total sugar intake was divided into the ≤19.5%E group and the 19.5%E group based on the median.
Dental caries was the outcome which was evaluated according to data from the examination by licensed dentists on a DMFT count. The DMFT scores were dichotomized into the DMFT>0 group and the DMFT = 0 group.13
The additive interaction model
The relative excess risk of interaction (RERI), attributable proportion of interaction (API), and synergy index (SI) are indexes of the addictive model evaluating the interaction between total sugar intake and tobacco exposure on the risk of dental caries. RERI=R11-R10-R01 + 1, which shows the difference between the sum of the combined effects of the two factors and the sum of the separate effects. API=RERI/R11, which represents the proportion of total effects attributed to interaction. SI=R11 (R10 × R01), which has the same meaning as RERI. When 0 was involved in the confidence intervals (CIs) of RERI and API and 1 was included in the CIs of SI, there was no interaction.
Statistical analysis
The measurement data were described as Mean (standard error) [Mean (SE)], and independent sample t-test was used for comparisons between the two groups. The enumeration data were described as the number and percentage of cases [n (%)], and Chi-square test was used for comparisons between groups, and rank sum test was used for rank data. The missing values of physical activity and frequency of using dental floss were more than 20%, and the missing data were classified into the unknown group. Other missing variables were manipulated via the random forest multiple interpolation using the miceforest package in python (Supplementary Table 1). Sensitivity analysis was performed to evaluate the differences of data before and after missing values manipulation (Supplementary Table 2). The study was subjected to a weighted manner and a set of weights WTDRD1 was used. A weighted univariable logistic regression model was used to explore the covariates associated with dental caries. Weighted univariable and multivariable logistic regression models were applied to explore the associations of total sugar intake or tobacco exposure with the risk of dental caries, and the interaction between tobacco exposure and total sugar intake on the risk of dental caries. The multivariable logistic regression model adjusted for age, gender, race, education, PIR, drinking, physical activity, hypertension, diabetes, dyslipidemia, CVD, bone loss around teeth, BMI, fiber intake, last dental visit, and dental care. The effect size of odds ratio (OR), 95%CI, RERI, API and SI was inputted. All statistical tests were conducted using a two-sided test. SAS 9.4 (SAS Institute Inc., Cary, NC, USA) was used for statistical analysis and interaction test.
Results
The characteristics of participants with or without dental caries
A total of 21501 participants ≥18 years from the NHANES between 2011 and 2018 were identified. Participants without the assessment of total sugar intake (n = 1580), serum cotinine (n = 948), and without data on BMI (n = 169) were excluded. Finally, 18804 participants were included. The flow diagram for the identification of final participants was shown in Fig. 1.
Figure 1.
The flow diagram for the identification of final participants in this study.
The percentage of people with cotinine level >10 ng/mL in the non-dental caries group was lower than the dental caries group (17.20% vs 25.38%). The percentage of participants with total sugar >19.5%E in the non-dental caries group was lower than the dental caries group (42.42% vs 52.18%). The mean age of subjects in the non-dental caries group was lower than the dental caries group (36.39 years vs 49.75 years). The mean total energy intake in the non-dental caries group was higher than the dental caries group (2219.15 kcal vs 2146.97 kcal). More information on the characteristics of participants with or without dental caries was presented in Table 1.
Table 1.
The characteristics of participants with or without dental caries.
| Variables | Total (n = 18804) | People without dental caries (n = 3387) | People with dental caries (n = 15417) | Statistics | P |
|---|---|---|---|---|---|
| Cotinine, n (%) | χ2 = 63.72 | <0.001 | |||
| ≤10 ng/mL | 14320 (76.42) | 2779 (82.80) | 11541 (74.62) | ||
| >10 ng/mL | 4484 (23.58) | 608 (17.20) | 3876 (25.38) | ||
| Total sugar, n (%) | χ2 = 44.36 | <0.001 | |||
| ≤19.5%E | 9166 (49.97) | 1877 (57.58) | 7289 (47.82) | ||
| >19.5%E | 9638 (50.03) | 1510 (42.42) | 8128 (52.18) | ||
| Cotinine and total sugar level, n (%) | χ2 = 100.48 | <0.001 | |||
| Cotinine ≤10 ng/mL and total sugar ≤19.5%E | 7095 (38.84) | 1533 (47.24) | 5562 (36.47) | ||
| Cotinine >10 ng/mL and total sugar ≤19.5%E | 2071 (11.13) | 344 (10.34) | 1727 (11.35) | ||
| Cotinine ≤10 ng/mL and total sugar >19.5%E | 7225 (37.58) | 1246 (35.56) | 5979 (38.15) | ||
| Cotinine >10 ng/mL and total sugar >19.5%E | 2413 (12.45) | 264 (6.85) | 2149 (14.03) | ||
| Age, years, Mean (S.E) | 46.81 (0.35) | 36.39 (0.53) | 49.75 (0.31) | t = −26.95 | <0.001 |
| Gender, n (%) | χ2 = 7.24 | 0.007 | |||
| Male | 9230 (48.89) | 1712 (51.92) | 7518 (48.04) | ||
| Female | 9574 (51.11) | 1675 (48.08) | 7899 (51.96) | ||
| Race, n (%) | χ2 = 9.16 | 0.010 | |||
| Non-Hispanic White | 7215 (64.93) | 1208 (64.79) | 6007 (64.97) | ||
| Non-Hispanic Black | 4162 (10.98) | 615 (8.93) | 3547 (11.56) | ||
| Others | 7427 (24.09) | 1564 (26.28) | 5863 (23.47) | ||
| Education, n (%) | χ2 = 95.68 | <0.001 | |||
| <high school | 3832 (13.40) | 392 (6.85) | 3440 (15.24) | ||
| high school | 4218 (22.75) | 611 (18.19) | 3607 (24.04) | ||
| >high school | 10754 (63.85) | 2384 (74.95) | 8370 (60.72) | ||
| PIR, n (%) | χ2 = 7.19 | 0.007 | |||
| <1.0 | 4192 (15.48) | 631 (12.68) | 3561 (16.27) | ||
| ≥1.0 | 14612 (84.52) | 2756 (87.32) | 11856 (83.73) | ||
| Drinking, n (%) | χ2 = 8.14 | 0.004 | |||
| <Once/week | 14610 (73.00) | 2711 (76.51) | 11899 (72.01) | ||
| ≥Once/week | 4194 (27.00) | 676 (23.49) | 3518 (27.99) | ||
| Physical activity, n (%) | χ2 = 98.31 | <0.001 | |||
| <450 MET × minutes/week | 1848 (9.28) | 277 (7.70) | 1571 (9.72) | ||
| ≥450 MET × minutes/week | 12402 (69.98) | 2599 (79.18) | 9803 (67.38) | ||
| Unknown | 4554 (20.74) | 511 (13.12) | 4043 (22.89) | ||
| Hypertension, n (%) | χ2 = 244.58 | <0.001 | |||
| No | 10439 (59.53) | 2622 (76.89) | 7817 (54.64) | ||
| Yes | 8365 (40.47) | 765 (23.11) | 7600 (45.36) | ||
| Diabetes, n (%) | χ2 = 103.15 | <0.001 | |||
| No | 15296 (85.49) | 3131 (93.14) | 12165 (83.33) | ||
| Yes | 3508 (14.51) | 256 (6.86) | 3252 (16.67) | ||
| Dyslipidemia, n (%) | χ2 = 143.35 | <0.001 | |||
| No | 6074 (32.24) | 1613 (44.31) | 4461 (28.84) | ||
| Yes | 12730 (67.76) | 1774 (55.69) | 10956 (71.16) | ||
| CVD, n (%) | χ2 = 194.53 | <0.001 | |||
| No | 15026 (82.68) | 3130 (91.73) | 11896 (80.13) | ||
| Yes | 3778 (17.32) | 257 (8.27) | 3521 (19.87) | ||
| Bone loss around teeth, n (%) | χ2 = 67.31 | <0.001 | |||
| No | 16485 (87.89) | 3223 (94.95) | 13262 (85.90) | ||
| Yes | 2319 (12.11) | 164 (5.05) | 2155 (14.10) | ||
| BMI, kg/m2, Mean (S.E) | 29.18 (0.12) | 28.76 (0.24) | 29.30 (0.12) | t = −2.23 | 0.029 |
| WBC, 1000 cells/uL, Mean (S.E) | 7.34 (0.04) | 7.31 (0.05) | 7.35 (0.04) | t = −0.66 | 0.510 |
| Carbohydrate, gm, Mean (S.E) | 254.38 (1.27) | 252.00 (3.30) | 255.05 (1.50) | t = −0.79 | 0.432 |
| Fiber intake, gm, Mean (S.E) | 17.43 (0.19) | 18.06 (0.34) | 17.26 (0.19) | t = 2.32 | 0.023 |
| Last dental visit, n (%) | χ2 = 17.35 | <0.001 | |||
| <1 year | 10336 (60.25) | 2003 (63.31) | 8333 (59.39) | ||
| 1–5 years | 5377 (26.25) | 932 (26.25) | 4445 (26.25) | ||
| ≥5 years | 3091 (13.51) | 452 (10.45) | 2639 (14.37) | ||
| Dental care, n (%) | χ2 = 59.23 | <0.001 | |||
| No | 14683 (81.63) | 2958 (88.75) | 11725 (79.63) | ||
| Yes | 4121 (18.37) | 429 (11.25) | 3692 (20.37) | ||
| Frequency of using dental floss, n (%) | χ2 = 478.93 | <0.001 | |||
| <7 times/week | 9915 (52.33) | 1229 (40.11) | 8686 (55.77) | ||
| ≥7 times/week | 4913 (25.87) | 579 (17.65) | 4334 (28.19) | ||
| Unknown | 3976 (21.80) | 1579 (42.24) | 2397 (16.04) | ||
| Total energy, kcal, Mean (S.E) | 2162.92 (9.14) | 2219.55 (24.46) | 2146.97 (11.15) | t = 2.48 | 0.016 |
S.E: standard error; PIR: poverty-to-income ratio; MET: metabolic equivalent of task; CVD: cardiovascular disease; BMI: body mass index; WBC: white blood cell.
Associations of tobacco exposure or total sugar intake with the risk of dental caries
According to the data in Table 2, age, gender, race, education, PIR, drinking, physical activity, hypertension, diabetes, dyslipidemia, CVD, bone loss around teeth, BMI, last dental visit, dental care, and frequency of using dental floss were potential covariates associated with the risk of dental caries in adults (Table 2). Multivariable logistic regression depicted that age, gender, race, education, PIR, drinking, physical activity, hypertension, diabetes, dyslipidemia, CVD, bone loss around teeth, BMI, fiber intake, last dental visit, dental care, and frequency of using dental floss were covariates.
Table 2.
Potential covariates associated with the occurrence of dental caries.
| Variables | OR (95%CI) | P |
|---|---|---|
| Age | 1.05 (1.05–1.06) | <0.001 |
| Gender | ||
| Male | Ref | |
| Female | 1.17 (1.04–1.31) | 0.009 |
| Race | ||
| Non-Hispanic White | Ref | |
| Non-Hispanic Black | 1.29 (1.05–1.59) | 0.016 |
| Others | 0.89 (0.75–1.06) | 0.178 |
| Education | ||
| <high school | Ref | |
| high school | 0.59 (0.48–0.74) | <0.001 |
| >high school | 0.36 (0.30–0.45) | <0.001 |
| PIR | ||
| <1.0 | Ref | |
| ≥1.0 | 0.75 (0.60–0.93) | 0.008 |
| Drinking, n (%) | ||
| <Once/week | Ref | |
| ≥Once/week | 1.27 (1.07–1.49) | 0.006 |
| Physical activity, n (%) | ||
| <450 MET × minutes/week | Ref | |
| ≥450 MET × minutes/week | 0.67 (0.54–0.84) | <0.001 |
| Unknown | 1.38 (1.08–1.77) | 0.012 |
| Hypertension | ||
| No | Ref | |
| Yes | 2.76 (2.40–3.17) | <0.001 |
| Diabetes | ||
| No | Ref | |
| Yes | 2.72 (2.20–3.35) | <0.001 |
| Dyslipidemia | ||
| No | Ref | |
| Yes | 1.96 (1.73–2.22) | <0.001 |
| CVD | ||
| No | Ref | |
| Yes | 2.75 (2.35–3.21) | <0.001 |
| Bone loss around teeth | ||
| No | Ref | |
| Yes | 3.09 (2.34–4.07) | <0.001 |
| BMI | 1.01 (1.01–1.02) | 0.034 |
| WBC | 1.00 (0.99–1.02) | 0.590 |
| Carbohydrate | 1.00 (1.00–1.00) | 0.436 |
| Fiber intake | 0.99 (0.99–0.99) | 0.019 |
| Last dental visit | ||
| <1 year | Ref | |
| 1–5 years | 1.07 (0.92–1.23) | 0.375 |
| ≥5 years | 1.47 (1.22–1.76) | <0.001 |
| Dental care | ||
| No | Ref | |
| Yes | 2.02 (1.69–2.42) | <0.001 |
| Frequency of using dental floss | ||
| <7 times/week | Ref | |
| ≥7 times/week | 1.15 (0.97–1.36) | 0.112 |
| Unknown | 0.27 (0.23–0.32) | <0.001 |
OR: odds ratio; CI: confidence interval; Ref: reference.
In the crude model, cotinine >10 ng/mL might be associated with elevated risk of dental caries in adults (OR = 1.64, 95%CI: 1.44–1.87). In the adjusted model 2, the OR of dental caries in adults with cotinine >10 ng/mL was 1.59 (95%CI: 1.38–1.82). There might be increased risk of dental caries in people with total sugar >19.5%E (OR = 1.48, 95%CI: 1.31–1.67). After adjusting for confounding factors, the increased risk of dental caries was also found in people with total sugar >19.5%E compared to those with total sugar ≤19.5%E (OR = 1.55, 95%CI: 1.34–1.78) (Table 3).
Table 3.
Associations of tobacco exposure or total sugar intake with the risk of dental caries.
| Crude model |
Model 1 |
Model 2 |
||||
|---|---|---|---|---|---|---|
| Variables | OR (95% CI) | P | OR (95% CI) | P | OR (95% CI) | P |
| Cotinine | ||||||
| ≤10 ng/mL | Ref | Ref | Ref | |||
| >10 ng/mL | 1.64 (1.44–1.87) | <0.001 | 1.83 (1.60–2.09) | <0.001 | 1.59 (1.38–1.82) | <0.001 |
| Total sugar | ||||||
| ≤19.5%E | Ref | Ref | Ref | |||
| >19.5%E | 1.48 (1.31–1.67) | <0.001 | 1.50 (1.31–1.71) | <0.001 | 1.55 (1.34–1.78) | <0.001 |
OR: odds ratio; CI: confidence interval; Ref: Reference.
Crude model: Weighted univariable logistic regression model.
Model 1: Weighted multivariable logistic regression model adjusted for age, gender, race, education, and PIR.
Model 2: Weighted multivariable logistic regression model adjusted for age, gender, race, education, PIR, drink, physical activity, hypertension, diabetes, dyslipidemia, CVD, bone loss around teeth, BMI, fiber intake, last dental visit, dental care, frequency of using dental floss.
Interaction between tobacco exposure and total sugar intake on the risk of dental caries in adults
The additive interaction terms of tobacco exposure and total sugar intake included cotinine ≤10 ng/mL and total sugar ≤19.5%E, cotinine >10 ng/mL and total sugar ≤19.5%E, cotinine ≤10 ng/mL and total sugar >19.5%E, and cotinine >10 ng/mL and total sugar >19.5%E. Compared to people with cotinine ≤10 ng/mL and total sugar ≤19.5%E, adults with cotinine >10 ng/mL and total sugar >19.5%E were correlated with elevated risk of dental caries (OR = 2.76, 95%CI: 2.29–3.33) (Table 4).
Table 4.
Interaction between tobacco exposure and total sugar intake on the risk of dental caries in adults.
| Crude model |
Model 1 |
Model 2 |
||||
|---|---|---|---|---|---|---|
| OR (95%CI) | P | OR (95%CI) | P | OR (95%CI) | P | |
| Cotinine and total sugar level | ||||||
| Cotinine ≤10 ng/mL and total sugar ≤19.5%E | Ref | Ref | Ref | |||
| Cotinine >10 ng/mL and total sugar ≤19.5%E | 1.42 (1.18–1.71) | <0.001 | 1.56 (1.28–1.90) | <0.001 | 1.34 (1.09–1.65) | 0.006 |
| Cotinine ≤10 ng/mL and total sugar >19.5%E | 1.39 (1.21–1.59) | <0.001 | 1.39 (1.19–1.63) | <0.001 | 1.44 (1.23–1.69) | <0.001 |
| Cotinine >10 ng/mL and total sugar >19.5%E | 2.65 (2.19–3.21) | <0.001 | 3.05 (2.55–3.64) | <0.001 | 2.76 (2.29–3.33) | <0.001 |
| RERI | 0.840 (0.276–1.404) | 1.094 (0.487–1.701) | 0.980 (0.413–1.547) | |||
| API | 0.317 (0.147–0.487) | 0.359 (0.202–0.516) | 0.355 (0.192–0.517) | |||
| SI | 2.037 (1.248–3.323) | 2.148 (1.363–3.384) | 2.250 (1.344–3.767) | |||
OR: odds ratio; CI: confidence interval; Ref: Reference; RERI: relative excess risk of interaction; SI: the synergy index; API: attributable proportion of interaction.
Crude model: Weighted univariable logistic regression model.
Model 1: Weighted multivariable logistic regression model adjusted for age, gender, race, education, and PIR.
Model 2: Weighted multivariable logistic regression model adjusted for age, gender, race, education, PIR, drink, physical activity, hypertension, diabetes, dyslipidemia, CVD, bone loss around teeth, BMI, fiber intake, last dental visit, dental care, frequency of using dental floss.
The interaction indicators RERI was 0.980 (95%CI: 0.413–1.547) and API was 0.355 (95%CI: 0.192–0.517). The CIs of RERI and API did not contain 0 and were both >0. The SI was 2.250 (95%CI: 1.344–3.767), and the CI did not contain 1 and were >1. The results indicated that there was synergic interaction between tobacco exposure and total sugar intake on the risk of dental caries in adults. The API was 0.355, indicating in our study, tobacco exposure and total sugar intake attributed to 35.5% risk of dental caries (Table 4).
Subgroup analysis of the interaction between tobacco exposure and total sugar intake on the risk of dental caries in adults
Based on the results from Table 5, the interaction between tobacco exposure and total sugar intake on the risk of dental caries was identified in adults <45 years with RERI of 0.781 (95%CI: 0.258–1.304), API of 0.328 (95%CI: 0.145–0.510), and SI of 2.294 (95%CI: 1.196–4.401). In male people, the interaction between tobacco exposure and total sugar intake on the risk of dental caries was also observed. The RERI was 1.046 (95%CI: 0.308–1.784), API was 0.384 (95%CI: 0.178–0.591), and SI was 2.544 (95%CI: 1.237–5.234). In participants with BMI <25 kg/m2, the interaction between tobacco exposure and total sugar intake on the risk of dental caries was significant [(RERI = 1.546, 95%CI: 0.393–2.699), API = 0.481 (95%CI: 0.263–0.699), and SI = 3.311 (95%CI: 1.403–7.814)]. The RERI was 0.722 (95%CI: 0.103–1.342), API was 0.279 (95%CI: 0.071–0.487), and SI was 1.833 (95%CI: 1.027–3.274) in adults with BMI≥25 kg/m2, suggesting that the interaction between tobacco exposure and total sugar intake on the risk of dental caries was significant.
Table 5.
Subgroup analysis of the interaction between tobacco exposure and total sugar intake on the risk of dental caries in adults.
| Subgroup | n (%) | Model |
n (%) | Model |
||
|---|---|---|---|---|---|---|
| OR (95%CI) | P | OR (95%CI) | P | |||
| Subgroup I: Age | Age<45 (n = 8452) | Age≥45 (n = 10352) | ||||
| Cotinine ≤10 ng/mL and total sugar ≤19.5%E | 3073 (37.55%) | Ref | 4022 (39.95%) | Ref | ||
| Cotinine >10 ng/mL and total sugar ≤19.5%E | 993 (12.38%) | 1.15 (0.91–1.46) | 0.242 | 1078 (10.05%) | 1.60 (0.90–2.85) | 0.106 |
| Cotinine ≤10 ng/mL and total sugar >19.5%E | 3062 (35.15%) | 1.45 (1.25–1.70) | <0.001 | 4163 (39.68%) | 1.34 (1.01–1.79) | 0.049 |
| Cotinine >10 ng/mL and total sugar >19.5%E | 1324 (14.92%) | 2.38 (1.97–2.89) | <0.001 | 1089 (10.32%) | 4.50 (2.33–8.70) | <0.001 |
| RERI | 0.781 (0.258–1.304) | 2.562 (−0.392–5.516) | ||||
| API | 0.328 (0.145–0.510) | 0.569 (0.229–0.908) | ||||
| SI |
2.294 (1.196–4.401) |
3.719 (1.005–13.762) |
||||
| Subgroup II: Gender |
Male (n = 9230) |
Female (n = 9574) |
||||
| Cotinine ≤10 ng/mL and total sugar ≤19.5%E | 3459 (38.79%) | Ref | 3636 (38.89%) | Ref | ||
| Cotinine >10 ng/mL and total sugar ≤19.5%E | 1368 (14.30%) | 1.20 (0.95–1.53) | 0.128 | 703 (8.10%) | 1.64 (1.20–2.24) | 0.002 |
| Cotinine ≤10 ng/mL and total sugar >19.5%E | 3026 (32.59%) | 1.47 (1.20–1.82) | <0.001 | 4199 (42.35%) | 1.40 (1.12–1.76) | 0.004 |
| Cotinine >10 ng/mL and total sugar >19.5%E | 1377 (14.32%) | 2.72 (2.14–3.46) | <0.001 | 1036 (10.66%) | 2.75 (1.91–3.98) | <0.001 |
| RERI | 1.046 (0.308–1.784) | 0.710 (−0.299–1.719) | ||||
| API | 0.384 (0.178–0.591) | 0.258 (−0.038–0.554) | ||||
| SI |
2.544 (1.237–5.234) |
1.680 (0.840–3.360) |
||||
| Subgroup III: BMI |
BMI<25 kg/m2 (n = 5519) |
BMI≥25 kg/m2 (n = 13285) |
||||
| Cotinine ≤10 ng/mL and total sugar ≤19.5%E | 1968 (35.72%) | Ref | 5127 (40.14%) | Ref | ||
| Cotinine >10 ng/mL and total sugar ≤19.5%E | 699 (11.50%) | 1.35 (0.96–1.92) | 0.088 | 1372 (10.97%) | 1.36 (1.03–1.80) | 0.030 |
| Cotinine ≤10 ng/mL and total sugar >19.5%E | 2006 (37.61%) | 1.31 (1.07–1.62) | 0.011 | 5219 (37.57%) | 1.50 (1.24–1.82) | <0.001 |
| Cotinine >10 ng/mL and total sugar >19.5%E | 846 (15.17%) | 3.22 (2.20–4.70) | <0.001 | 1567 (11.32%) | 2.59 (2.11–3.18) | <0.001 |
| RERI | 1.546 (0.393–2.699) | 0.722 (0.103–1.342) | ||||
| API | 0.481 (0.263–0.699) | 0.279 (0.071–0.487) | ||||
| SI | 3.311 (1.403–7.814) | 1.833 (1.027–3.274) | ||||
OR: odds ratio; CI: confidence Interval; Ref: reference; RERI: relative excess risk of interaction; SI: the synergy index; API: attributable proportion of interaction; BMI: body mass index.
OR: odds ratio; CI: confidence interval; Ref: Reference.
Crude model: Weighted univariable logistic regression model.
Model: Weighted multivariable logistic regression model, if not stratified, adjusted for age, gender, race, education, PIR, drink, physical activity, hypertension, diabetes, dyslipidemia, CVD, bone loss around teeth, BMI, fiber intake, last dental visit, dental care, frequency of using dental floss.
Discussion
The present study evaluated the associations of sugar intake or tobacco exposure with the risk of dental caries in adults, and further assessed the interaction between sugar intake and tobacco exposure on the risk of dental caries was also evaluated. The results showed that high levels of tobacco exposure or high total sugar intake were related to increased risk of dental caries. Additionally, a synergic interaction between sugar intake and tobacco exposure was identified to be associated with the risk of dental caries. The findings might provide a reference for the management of oral health in common people, and offer a direction for future prospective studies to explore the roles of sugar intake and tobacco exposure on the risk of dental caries.
In previous studies, smoking was reported to be associated with higher caries prevalence and more severe periodontal disease.14 Liu et al. reported that residents of Liaoning, China with a history of smoking habits were more susceptible to dental caries.15 Another Sweden cohort study indicated that smoking and use of smokeless tobacco were determinants of dental caries increment in young adults.16 In our study, we found that cotinine level >10 ng/mL was associated with increased risk of dental caries in adults. This might because tobacco smoking was associated with elevated levels of Streptococcus mutans and Lactobacilli.9 Streptococcus mutans is the major cariogenic microorganism in the oral cavity.17 While nicotine increases the biofilm formation and metabolic activity of Streptococcus mutans.18 Nicotine also enhances extracellular polysaccharides, which attract other microorganisms, such as Candida albicans, onto the dental plaque.19 Another possible reason might be that smokers had decreased levels of secretory immunoglobulin A (SIgA) that was associated with the prevalence of dental caries.20
Growing numbers of studies indicated the risk of dental caries might due to sugar intake, and sugar consumption is one of the main aetiological factors for dental caries.21 A systematic review indicated that the between-meal consumption of processed sugar-containing foods was consistently associated with greater caries experience.22 A position paper of the Brazilian Academy of Dentistry demonstrated that excessive sugar consumption is the main cause of dental caries.23 Herein, high total sugar intake was related to elevated risk of dental caries in adults. The role of sugars as well as its aetiology in oral health is well established.24,25 Sugar can be used as a substrate for oral bacteria, and oral bacteria metabolized acid, which reduces PH value and exceeds the buffer adjustment capacity of saliva, thus increasing the favorable conditions for dental demineralization.26 The WHO recommended that for minimising lifelong risk of dental caries, free sugars intake should be limited to below 5% of energy intake.27 Addressing the universally high free sugars intake, is an important part of the Global Strategy on Oral Health.
Additionally, the synergistic interaction of cotinine level and sugar intake was identified on the occurrence of dental caries. These suggested that people with both smoking habits and high sugar intake might have higher risk of dental caries. Increasing knowledge of the role of risk factors, namely smoking, and high sugar intake might enable public health policies to be implemented that reduce the probability of progression to pathology. Dental health professionals should incorporate anti-smoking activities, and sugar limiting in their preventive strategies. Active disease prevention strategies and multidisciplinary actions may help achieve early pathological detection and thereby early treatment.14,28
The present study initially evaluated the interaction between sugar intake and tobacco exposure on dental caries in adults, which might provide a reference for the formulation of more specific prevention and control strategies. The sample size of this study is large, and multi-stage complex sampling was conducted, which has a good representation of the American population. Also, the use of cotinine level as a marker can more objectively reflect tobacco exposure in individuals. Several limitations existed in this study. Firstly, the current study was a cross-sectional study, and no causal relationship between cotinine level or total sugar intake and dental caries could be identified. Secondly, although the influence of possible confounding factors such as floss use was considered, there were still some missing points due to database limitations.
In conclusion, this study identified that there might be interaction between sugar intake and tobacco exposure on dental caries in adults. The findings suggested that less tobacco exposure and sugar intake might be policies worth promoting and benefit for oral health in adults.
Declaration of competing interest
The authors have no conflicts of interest relevant to this article.
Acknowledgments
Thanks for the funding from Project of Nantong Municipal Health Commission: A three-dimensional finite element analysis of the onlay restoration in the mandibular molar remnant crown (MS2022092).
References
- 1.Qayyum A., Tahir A., Butt M.A., et al. Dental caries detection using a semi-supervised learning approach. Sci Rep. 2023;13:749. doi: 10.1038/s41598-023-27808-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Marcenes W., Kassebaum N.J., Bernabé E., et al. Global burden of oral conditions in 1990-2010: a systematic analysis. J Dent Res. 2013;92:592–597. doi: 10.1177/0022034513490168. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Kassebaum N.J., Bernabé E., Dahiya M., Bhandari B., Murray C.J., Marcenes W. Global burden of untreated caries: a systematic review and metaregression. J Dent Res. 2015;94:650–658. doi: 10.1177/0022034515573272. [DOI] [PubMed] [Google Scholar]
- 4.Zewdu T., Abu D., Agajie M., Sahilu T. Dental caries and associated factors in Ethiopia: systematic review and meta-analysis. Environ Health Prev Med. 2021;26:21. doi: 10.1186/s12199-021-00943-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Valenzuela M.J., Waterhouse B., Aggarwal V.R., Bloor K., Doran T. Effect of sugar-sweetened beverages on oral health: a systematic review and meta-analysis. Eur J Publ Health. 2021;31:122–129. doi: 10.1093/eurpub/ckaa147. [DOI] [PubMed] [Google Scholar]
- 6.Pitts N.B., Twetman S., Fisher J., Marsh P.D. Understanding dental caries as a non-communicable disease. Br Dent J. 2021;231:749–753. doi: 10.1038/s41415-021-3775-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Andayasari L., Mubasyiroh R., Nurlinawati I., Sufiawati I. Association between tobacco smoking and dental caries in the Indonesian population: results of a national study in 2018. J Prev Med Public Health. 2023;56:357–367. doi: 10.3961/jpmph.22.417. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Jiang X., Jiang X., Wang Y., Huang R. Correlation between tobacco smoking and dental caries: a systematic review and meta-analysis. Tob Induc Dis. 2019;17:34. doi: 10.18332/tid/106117. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Avşar A., Darka O., Topaloğlu B., Bek Y. Association of passive smoking with caries and related salivary biomarkers in young children. Arch Oral Biol. 2008;53:969–974. doi: 10.1016/j.archoralbio.2008.05.007. [DOI] [PubMed] [Google Scholar]
- 10.Chanea K.P.A. Smoking and candy on oral bacteria, Streptococcus mutans, adherence. California State Polytechnic University Pomona. 2014. https://hdl.handle.net/10211.3/118316
- 11.Qiu Z., Chen X., Geng T., et al. Associations of serum carotenoids with risk of cardiovascular mortality among individuals with type 2 diabetes: results from NHANES. Diabetes Care. 2022;45:1453–1461. doi: 10.2337/dc21-2371. [DOI] [PubMed] [Google Scholar]
- 12.Shen Q., Xu Q., Li G., et al. Joint effect of 25-hydroxyvitamin D and secondhand smoke exposure on hypertension in non-smoking women of childbearing age: NHANES 2007-2014. Environ Health. 2021;20:117. doi: 10.1186/s12940-021-00803-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Bidinotto A.B., Martinez-Steele E., Cunha-Cruz J., et al. Food processing and its association with dental caries: data from NHANES 2011-2014. Community Dent Oral Epidemiol. 2021;49:565–573. doi: 10.1111/cdoe.12628. [DOI] [PubMed] [Google Scholar]
- 14.Beklen A., Sali N., Yavuz M.B. The impact of smoking on periodontal status and dental caries. Tob Induc Dis. 2022;20:72. doi: 10.18332/tid/152112. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Liu L., Wu W., Zhang S.Y., et al. Dental caries prediction based on a survey of the oral health epidemiology among the geriatric residents of Liaoning, China. BioMed Res Int. 2020;2020 doi: 10.1155/2020/5348730. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Petersson G.H., Twetman S. Tobacco use and caries increment in young adults: a prospective observational study. BMC Res Notes. 2019;12:218. doi: 10.1186/s13104-019-4253-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Lemos J.A., Quivey R.G., Koo H., Abranches J. Streptococcus mutans: a new Gram-positive paradigm? Microbiology (Read) 2013;159:436–445. doi: 10.1099/mic.0.066134-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Huang R., Li M., Gregory R.L. Effect of nicotine on growth and metabolism of Streptococcus mutans. Eur J Oral Sci. 2012;120:319–325. doi: 10.1111/j.1600-0722.2012.00971.x. [DOI] [PubMed] [Google Scholar]
- 19.Liu S., Qiu W., Zhang K., et al. Nicotine enhances interspecies relationship between streptococcus mutans and Candida albicans. BioMed Res Int. 2017;2017 doi: 10.1155/2017/7953920. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Golpasand Hagh L., Zakavi F., Ansarifar S., Ghasemzadeh O., Solgi G. Association of dental caries and salivary sIgA with tobacco smoking. Aust Dent J. 2013;58:219–223. doi: 10.1111/adj.12059. [DOI] [PubMed] [Google Scholar]
- 21.Lagerweij M., van Loveren C. Chapter 7: sugar and dental caries. Monogr Oral Sci. 2020;28:68–76. doi: 10.1159/000455373. [DOI] [PubMed] [Google Scholar]
- 22.Hancock S., Zinn C., Schofield G. The consumption of processed sugar- and starch-containing foods, and dental caries: a systematic review. Eur J Oral Sci. 2020;128:467–475. doi: 10.1111/eos.12743. [DOI] [PubMed] [Google Scholar]
- 23.Feldens C.A., Pinheiro L.L., Cury J.A., et al. Added sugar and oral Health: a position paper of the Brazilian academy of dentistry. Front Oral Health. 2022;3 doi: 10.3389/froh.2022.869112. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Kassebaum N.J., Smith A.G.C., Bernabé E., et al. Global, regional, and national prevalence, incidence, and disability-adjusted life years for oral conditions for 195 countries, 1990-2015: a systematic analysis for the global burden of diseases, injuries, and risk factors. J Dent Res. 2017;96:380–387. doi: 10.1177/0022034517693566. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Moores C.J., Kelly S.A.M., Moynihan P.J. Systematic review of the effect on caries of sugars intake: ten-year update. J Dent Res. 2022;101:1034–1045. doi: 10.1177/00220345221082918. [DOI] [PubMed] [Google Scholar]
- 26.Touger-Decker R., van Loveren C. Sugars and dental caries. Am J Clin Nutr. 2003;78 doi: 10.1093/ajcn/78.4.881S. [DOI] [PubMed] [Google Scholar]
- 27.WHO guidelines approved by the guidelines review committee. Guideline: sugars intake for adults and children. World Health Organization Copyright © World Health Organization; Geneva: 2015. p. 2015. [Google Scholar]
- 28.Martignon S., Roncalli A.G., Alvarez E., Aránguiz V., Feldens C.A., Buzalaf M.A.R. Risk factors for dental caries in Latin American and Caribbean countries. Braz Oral Res. 2021;35 doi: 10.1590/1807-3107bor-2021.vol35.0053. [DOI] [PubMed] [Google Scholar]