Abstract
Vitamin D and fiber intake are nutritional factors that could affect the development of type 2 diabetes (T2D), potentially by reducing insulin resistance. Therefore, we hypothesized that the influence of vitamin D on T2D might depend on fiber intake. This study investigated the association between vitamin D status and T2D according to fiber intake. The present study analyzed data from 9,656 American adults (≥20 years old) who participated in the National Health and Nutrition Examination Survey (NHANES) 2007–2010. The serum concentration of 25-hydroxyvitamin D [25(OH)D] was used as a biomarker for vitamin D status. The T2D classification was based on two criteria: T2Da was identified using only self-reported questionnaire data and T2Db was identified based on both survey and laboratory data. The deficient vitamin D status (<50 nmol/L) was used as the reference group. After controlling for sociodemographic, behavioral, and dietary factors, the odds ratios (ORs) were 0.72 (95% confidence interval [CI]: 0.58, 0.90) for T2Da and 0.60 (0.50, 0.80) for T2Db in the sufficient vitamin D status (≥75 nmol/L). Furthermore, the total vitamin D concentration exhibited dose-dependent associations with lower OR values for T2Da (P for trend = .005) and T2Db (P for trend <.001). Among participants with high-fiber intake, the OR values for T2Db were 0.60 (95% CI: 0.42, 0.90) at suboptimal vitamin D status and 0.49 (95% CI: 0.31, 0.77) at sufficient vitamin D status. Moreover, the significant dose-dependent association persisted in the high-fiber-intake subgroup (P for trend = .004). Therefore, combining vitamin D plus high-fiber intake would help reduce the prevalence of diabetes, although the interaction analysis results were not statistically significant.
Introduction
Based on U.S. survey data, the prevalence of diabetes in adults is 12–14%, 1 which may lead to growth in related morbidity, mortality, and economic costs. 2 Therefore, it is essential to manage and treat type 2 diabetes (T2D), for preventing the development of cardiovascular disease, 3 premature death, and all-cause mortality. 4
Fiber intake is a well-known dietary factor that could reduce the risk of T2D 5 and insulin resistance. 6 One meta-analysis also revealed that dietary fiber intake may help reduce the prevalence of T2D. 7 Despite these results, most Americans consume less than the recommended daily amount of dietary fiber (14 g of total fiber per 1000 kcal, women; 25 g/day, men; 38 g/day). 8
The National Health and Nutrition Examination Survey (NHANES) 2011–2014 revealed a risk of vitamin D insufficiency in 18% of the U.S. population that was ≥1 year old. 9 Vitamin D has also been investigated as a relevant factor for preventing the development of T2D. 10 For example, Bourlon et al. reported that the active form of vitamin D is involved in promoting the biosynthesis of beta cells. 11 Also, Kjalarsdottir et al. suggested that vitamin D could increase insulin secretion in the pancreas. 12 A recent review also indicated that sufficient vitamin D concentrations have a positive effect on T2D. 13
Previous studies have revealed that sufficient vitamin D concentrations reduce insulin resistance, 14,15 and dietary fiber has also been reported to be involved in reducing insulin resistance. 16,17 However, previous studies have only evaluated these as separate factors. Therefore, we hypothesized that the coexistence of sufficient vitamin D concentrations and sufficient fiber intake might have a synergistic effect on reducing insulin resistance and thereby reducing the prevalence of T2D. The present study conducted the joined effects of vitamin D concentration and fiber intake on the prevalence of diabetes among American adults.
Methods
Study population
Data in this study includes participants ≥20 years of age from the NHANES 2007–2010, conducted by the Centers for Disease Control and Prevention (CDC). The NHANES is a health-related survey program to assess the health and nutritional status from a representative sample of the civilian noninstitutionalized U.S. population. The survey uses a complex, multistaged, stratified, and clustered design and included household interview such as demographic, socioeconomic, behavioral, and dietary questionnaires. Oversampled participants included Hispanics, non-Hispanic blacks, low-income Whites, and persons who were ≥80 years old. Demographic and health history information were collected through extensive household interviews, and a mobile examination center (MEC) was used to collect blood and urine samples and to perform standardized physical examinations.
The present study included two cycles from NHANES (2007–2008, 2009–2010), and NHANES data from 1999 to 2006 were omitted because the serum 25-hydroxyvitamin D [25(OH)D] concentrations were measured using a different method (i.e., radioimmunoassay). During 2007–2010, the NHANES enrolled 20,686 participants, 11,766 adults (≥20 years old) had completed data on both interview and examination. The present study excluded participants with missing information regarding serum 25(OH)D concentrations (n = 1,435) or other covariates (n = 672), and a total of 9,659 participants were included to our analysis (Fig. 1).

Description of the study population.
The NCHS Research Ethics committee reviewed and approved the study protocol (continuation of protocol #2005-06). Written informed consent was obtained from all NHANES participants. The NHANES dataset is publicly available, and additional details regarding the study procedures, data documentation, and questionnaires are available elsewhere. 18,19
Measurement of 25(OH)D concentrations
Blood samples for measurement of vitamin D status were collected from each participant at the MEC. Those blood samples were immediately frozen at −30°C and shipped to the National Center for Environmental Health (CDC, Atlanta, GA) for analysis. Serum samples were subjected to ultra high-performance liquid chromatography–tandem mass spectrometry (ThermoElectron Corp., West Palm Beach, FL) for the quantitative detection of 25-hydroxyvitamin D3 [25(OH)D3], 25-hydroxyvitamin D2 [25(OH)D2], and 3-epi-25-hydroxyvitamin D3 [3-epi-25(OH)D3] concentrations. 20,21
The total vitamin D status was defined as the sum of the 25(OH)D3 and 25(OH)D2 concentrations in SI units of nmol/L, but did not include the 3-epi-25(OH)D3 concentration, which is the predominant form in infants (<1 year old). 22 For the statistical analyses, the total vitamin D status was classified into three groups based on the cutoff points suggested by the U.S. Endocrine Society 23 : <50 nmol/L (deficient), 50–74.99 nmol/L (suboptimal), and ≥75 nmol/L (sufficient).
Fiber intake
Information regarding fiber intake for the previous 24-hour period was collected via a dietary recall interview at the MEC. The daily fiber intake was adjusted by the total energy intake using the residual method, 24 and categorized as high or low intake based on the average value (15.3 g/day).
Identification and classification of T2D
T2D was identified based on two sets of criteria, with positive results classified as T2Da and T2Db. T2Da was identified based only on self-reported questionnaire data indicating (1) a physician diagnosis of diabetes, (2) the current use of antidiabetes medication, or (3) the current use of insulin. T2Db was identified based on the subject fulfilling the criteria for T2Da plus one or more of following laboratory criteria: (1) glycosylated hemoglobin A1c concentration of ≥6.5%, (2) fasting glucose concentration of ≥126 mg/dL, or (3) an oral glucose tolerance test result of ≥200 mg/dL.
Covariates
As potential confounders, we considered the participants' age, sex, race/ethnicity, education, season of examination, physical activity, smoking status, dietary intakes (total food energy and energy-adjusted protein, vitamin D, and calcium values), body mass index (BMI), household income, family history, and supplement use. Age was categorized as 20–29 years, 30–39 years, 40–49 years, 50–59 years, 60–69 years, and ≥70 years. Race/ethnicity was categorized as non-Hispanic white (reference), Mexican American, non-Hispanic black, and other. We categorized education as completion of less than 9th grade (reference), high school graduate or less, and more than high school graduate. Smoking status was categorized as never (reference), former, and current smoker. Season of examination was classified as November–April (reference) or May–October. Physical activity was self-reported for the three levels of activity intensity (walking, moderate, and vigorous activity) and computed using metabolic equivalent (MET) value. 25
Information regarding dietary intakes (total food energy, protein, vitamin D, and calcium) was collected for the previous 24-hour period through a dietary recall interview immediately before the interview at the MEC. Dietary factors (protein, vitamin D, and calcium) were adjusted based on total energy intake using the residual method.
Household income was calculated based on the poverty-to-income ratio (PIR) with family size-specific thresholds, and was categorized as <1 (below the poverty line), 1 to <3, and ≥3. Use of supplements within the previous 30 days (vitamins, minerals, herbal supplements, or other dietary supplements) was self-reported and categorized as user (reference) or nonuser. The risk factors for diabetes were classified as yes (reference) or no based on the following question: “Have you ever been told by a doctor or other health professional that you have health conditions or a medical or family history that increases your risk of diabetes?” HOMA-IR was calculated using the following formula: HOMA-IR = [fasting serum insulin (mU/L) × fasting plasma glucose (mmol/L)]/22.5.
Statistical analyses
Data analyses were performed using the SAS survey procedure (version 9.4; SAS Institute, Inc., Cary, NC) to account for the complex survey design and the sample weights of the 2007–2010 NHANES. We calculated the 4-year sample weights from the 2-year weights for 2007–2008 and the 2-year weights for 2009–2010 according to the NHANES analysis guideline. P-values were two sided and considered statistically significant at <.05. In the descriptive analyses, we presented the weighted means and standard error of the mean for continuous variables, and the weighted percentages (%) for categorical variables. Continuous variables were analyzed using the survey t-test and categorical variables were analyzed using the survey (Rao-Scott) χ 2 test.
The association between the prevalence of T2D and vitamin D concentrations was analyzed for a self-reported diagnosis of T2Da and for a confirmed diagnosis of T2Db. The analysis was also performed according to fiber intake. Four survey logistic regression models (PROC SURVEYLOGISTIC) were used to assess the influence of potential confounding factors. Model A considered age, sex, race/ethnicity, education, smoking status, season of examination, and physical activity. Model B considered the covariates from Model A plus BMI. Model C considered the covariates from Model B plus energy-adjusted dietary covariates (i.e., intakes of total energy, protein, vitamin D, and calcium). In Supplementary Tables 3 and 4, model D considered the covariates from Model C plus household income, supplement use, and family history. Odds ratios (ORs) and 95% confidence intervals (CIs) were calculated to estimate the association between total 25(OH)D concentration and the prevalence of T2D, with the deficient group (serum 25(OH)D of <50 nmol/L) defined as the reference group. Tests of trend were conducted for total vitamin D concentration as the ordinal variable in logistic regression models using integer values (1–3). In addition, we examined the multiplicative interaction between total vitamin D concentration and fiber intake on the prevalence of T2D, and calculated the interaction P-value using Wald tests. We confirmed the multicollinearity, and except for the factors (intake of carbohydrate, fat, and fiber) that show multicollinearity (variance inflation factor >10).
Adjusted Odds Ratio and 95% Confidence Interval of Type 2 Diabetes Stratified According to Total 25(OH)D Concentration
P < .001, ** P < .01, * P < .05 compared with reference group (vitamin levels <50 nmol/L).
Diabetes was diagnosed based on survey only.
Diabetes was diagnosed based on survey and lab data.
Model A was adjusted for age, sex, race/ethnicity, education level, smoking status, season of examination, physical activity.
Model B: model A+ further adjusted for BMI.
Model C: model B+ further adjusted for intake of total energy and energy adjusted dietary factor (protein, calcium, vitamin D).
Results
Descriptive characteristics
Table 1 summarizes the participants' physical and dietary characteristics according to their total vitamin D status. Relative to the deficient, participants with sufficient total vitamin D were more likely to be older, taller, have a lower body weight, and have a higher physical activity. For diet-related factors, intakes of total energy, energy-adjusted protein, fiber, vitamin D, and calcium were higher in participants with sufficient total vitamin D. Table 2 presents the participants' demographic characteristics stratified by total vitamin D. Participants with sufficient total vitamin D compared with the deficient were more high likely to be non-Hispanic white, former smokers, highly educated, evaluated during May–October, have a higher household income, and use supplements. In contrast, participants with deficient total vitamin D were to have a BMI of ≥30 kg/m2 and to have a high risk of T2D.
Physical and Dietary Characteristic Stratified According to Total 25(OH)D Concentration
Survey regression for continuous variable were used.
25(OH)D, 25-hydroxyvitamin D; MET, metabolic equivalent.
General Characteristic Stratified According to Total 25(OH)D Concentration
Survey (Rao-Scott) χ 2 test for categorical variable were used.
BMI, body mass index; PIR, poverty-to-income ratio.
Supplementary Tables S1 and S2 summarize the participants' characteristics according to fiber intake. Participants with high-fiber intake were more likely to be older, shorter, have a lower body weight, have high total vitamin D, have lower physical activity, have lower intake of total energy, and have higher energy-adjusted values for carbohydrate, protein, fiber, vitamin D, and calcium intake. In addition, significant differences according to fiber intake were observed according to sex, race/ethnicity, smoking status, education level, and BMI category.
Total 25(OH)D and T2D
Table 3 shows the ORs for T2D according to total vitamin D status in the various models. Total vitamin D was significantly associated with the ORs of T2D in all models. In the fully adjusted model (model C), and relative to participants with deficient total vitamin D, the ORs for T2Da were 0.90 (95% CI: 0.72, 1.13) for participants with suboptimal total vitamin D and 0.72 (95% CI: 0.58, 0.90) for participants with sufficient total vitamin D. A significant dose-dependent association was observed between total vitamin D and T2Da (P for trend = .005). Furthermore, the ORs for T2Db were 0.76 (95% CI: 0.60, 0.97) for participants with suboptimal total vitamin D and 0.60 (95% CI: 0.50, 0.80) for participants with sufficient total vitamin D. A significant dose-dependent association was also found between total vitamin D and T2Db (P for trend <.001).
Total vitamin D, fiber intake, and T2D b
Table 4 presents the ORs for T2D according to total vitamin D and fiber intake in the various models. Among the group with low-fiber intake, the ORs for T2Db were 0.89 (95% CI: 0.65, 1.21) for participants with suboptimal total vitamin D and 0.70 (95% CI: 0.48, 1.01) for participants with sufficient vitamin D. The dose-dependent association showed a marginal trend in the fully adjusted model (P for trend = .056). Similarly, among the group with high-fiber intake, the ORs for T2Db were 0.60 (95% CI: 0.40, 0.90) for participants with suboptimal vitamin D and 0.49 (95% CI: 0.31, 0.77) for participants with sufficient total 25(OH)D. These dose-dependent association was significant in the fully adjusted model (P for trend = .004). However, there was no significance in the result from the interaction analysis (P = .197).
Adjusted Odds Ratio and 95% Confidence Interval for Type 2 Diabetes Diagnosed Based on Survey and Laboratory Data with Stratification According to Fiber Intake
P < .001, ** P < .01, * P < .05, † P < .1 compared with reference group (vitamin levels <50 nmol/L).
Diabetes was diagnosed based on survey and lab data.
Model A was adjusted for age, sex, race/ethnicity, education level, smoking status, season of examination, physical activity.
Model B: model A+ further adjusted for BMI.
Model C: model B+ further adjusted for intake of total energy and energy adjusted dietary factor (protein, calcium, vitamin D).
Total 25(OH)D and HOMA-IR
Supplementary Table S3 shows the results for the associations between total vitamin D and the HOMA-IR findings in the various models. In the Model C, relative to participants with deficient total vitamin D, the HOMA-IR values were significantly lower for participants with suboptimal total vitamin D (−0.59, 95% CI: −0.95, −0.23) and participants with sufficient total vitamin D (−1.03, 95% CI: −1.36, −0.66). These dose-dependent associations were statistically significant (P for trend <.001). When we controlled for additional confounders (household income, supplement use, and family history), these associations became less significant but remained generally consistent with the unadjusted results.
Discussion
The present study evaluated a representative sample of American adults and the findings suggest that vitamin D concentrations (based on total 25(OH)D as a surrogate biomarker) and fiber intake were related to the prevalence of T2D, even after adjusting for potential confounding factors. Thus, strategies that involve vitamin D supplementation and high-fiber intake may more effectively reduce the prevalence of diabetes. In the fully adjusted models, the ORs for diabetes in participants with sufficient total 25(OH)D were 0.49 (95% CI: 0.31, 0.77) for participants with high-fiber intake and 0.70 (95% CI: 0.48, 1.01) for participants with low-fiber intake, although the interaction analysis results were not significant.
An in vitro study has indicated that of vitamin D is involved in promoting the biosynthesis of beta cells 11 and increased insulin secretion in the pancreas. 12 A recent review also noted that epidemiology studies support an association between vitamin D deficiency and the risk of T2D, whereas most randomized intervention studies could not prove the effect of vitamin D supplementation in terms of glucose metabolism among subjects who were at risk of developing diabetes. 13 These discrepancies may be related to differences in the duration and dose of vitamin D supplementation, as well as the subjects' characteristics. Moreover, a recent in vivo study indicated that vitamin D supplementation reduced blood glucose concentrations, increased insulin secretion, and helped prevent diabetes-related complications. 26 Park et al. suggested that the sufficient vitamin D (>50 nmol/L) was necessary to observe the maximum reduction in the risk of T2D in a prospective study. 27 Similarly, the present study revealed that the prevalence of diabetes was significantly lower when the total vitamin D concentrations were >50 nmol/L.
Fiber intake is a well-known dietary factor that may improve the risk of T2D 5 and insulin resistance. 6 The relationship of fiber intake and T2D has been explained by several mechanisms. First, high-fiber intake may improve the risk of overweight/obesity, and indirectly influence the risk of developing T2D. 28 Second, fiber intake may postpone gastric emptying and reduce the absorption of carbohydrates, as a result, the concentrations of postprandial blood glucose decrease. 29 One meta-analysis has suggested that high-fiber intake (≥25 g/day) may prevent T2D. 7
Insulin resistance is a pathological status in which cells or a whole organism is unable to respond normally to a given insulin, and this condition is associated with obesity and T2D. 30 Previous studies demonstrated that sufficient vitamin D status reduces the risk of insulin resistance. 14,15 The present study included an insulin resistance marker (HOMA-IR) to evaluate how vitamin D might reduce the prevalence of T2D. Similar to previously reported results, the present study revealed that insulin resistance was decreased at sufficient vitamin D concentrations. Furthermore, the present study revealed that the OR value for T2D was lower in the group with high-fiber intake (≥15.3 g/day) and sufficient vitamin D status (≥50 nmol/L), relative to the group with low-fiber intake (<15.3 g/day) and deficient vitamin D status (<50 nmol/L). Nevertheless, the results of the interaction analysis were not significant. While our observational findings suggest that these two factors have a synergistic beneficial effect on T2D, further experimental studies are required to understand these related mechanisms.
When we controlled for additional confounders (household income, supplement use, and family history) in model D, the association between vitamin D concentration and T2Db became less significant. Nevertheless, the results remained generally consistent with the results from the unadjusted models (Supplementary Table S4). Moreover, analysis according to fiber intake revealed consistent results relative to the unadjusted results.
The major strengths of this study include a large dataset from a representative sample of American adults. Second, we adjusted the models for a variety of potential confounding factors, including dietary factors, and our major results persisted after the adjustment for those factors. Third, this study used serum 25(OH)D concentration, which is a biomarker that reflects vitamin D derived from sun exposure and obtained from food intake. Nevertheless, this study also has several limitations. First, the cross-sectional design precludes a definitive conclusion regarding the causality of the relationships we observed. Second, residual confounding is possible despite the fact that we controlled for a variety of potential confounders. Third, we were unable to classify fiber as water soluble or insoluble based on the NHANES data. Finally, although total 25(OH)D is a commonly used biomarker for estimating vitamin D status, it may not capture the body's stores of bioavailable vitamin D.
In conclusion, the present study's findings suggest that vitamin D intake (food rich in vitamin D, supplementation, and outdoor activities in sunny days) combined with high-fiber intake may more effectively reduce the prevalence of diabetes. Further studies are needed to explain the potential mechanisms underlying the beneficial effects of dietary fiber intake and vitamin D status on the prevention of T2D.
Ethical Standards Disclosure
This study was conducted in accordance with the Declaration of Helsinki. All procedures in the NHANES protocol were reviewed and approved by the National Center for Health Statistics' Research Ethics Review Board and all participants provided informed consent.
Footnotes
Author Disclosure Statement
No competing financial interests exist.
Funding Information
This work was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF), which is funded by the Korea Ministry of Education (2017R1A6A3A11034504).
Supplementary Material
Supplementary Table S1
Supplementary Table S2
Supplementary Table S3
Supplementary Table S4
References
Supplementary Material
Please find the following supplemental material available below.
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