Eur J Epidemiol DOI 10.1007/s10654-013-9876-x
META-ANALYSIS
Dietary fiber intake and risk of type 2 diabetes: a dose–response analysis of prospective studies Baodong Yao • Hong Fang • Wanghong Xu Yujie Yan • Huilin Xu • Yinan Liu • Miao Mo • Hua Zhang • Yanping Zhao
•
Received: 4 July 2013 / Accepted: 27 December 2013 Ó Springer Science+Business Media Dordrecht 2014
Abstract Observational studies suggest an association between dietary fiber intake and risk of type 2 diabetes, but the results are inconclusive. We conducted a meta-analysis of prospective studies evaluating the associations of dietary fiber intake and risk of type 2 diabetes. Relevant studies were identified by searching EMBASE (from 1974 to April 2013) and PubMed (from 1966 to April 2013). The fixed or random-effect model was selected based on the homogeneity test among studies. In addition, a 2-stage random-effects dose–response meta-analysis was performed. We identified 17 prospective cohort studies of dietary fiber intake and risk of type 2 diabetes involving 19,033 cases and 488,293 participants. The combined RR (95 % CI) of type 2 diabetes for intake of total dietary fiber, cereal fiber, fruit fiber and insoluble fiber was 0.81 (0.73–0.90), 0.77 (0.69–0.85), 0.94 (0.88–0.99) and 0.75 (0.63–0.89), respectively. A nonlinear relationship was found of total dietary fiber intake with risk of type 2 diabetes (Pfor nonlinearity \ 0.01), and the RRs (95 % CI) of type 2 diabetes were 0.98 (0.90–1.06), 0.97 (0.87–1.07), 0.89 (0.80–0.99), 0.76 (0.65–0.88), and 0.66 (0.53–0.82) for 15, 20, 25, 30, and 35 g/day. The departure from nonlinear relationship was not significant (Pfor nonlinearity = 0.72), and the risk of type 2 diabetes decreased by 6 % (RR 0.94, 95 % CI 0.93–0.96) for 2 g/day increment in
Baodong Yao and Hong Fang have contributed equally to this work. B. Yao H. Fang Y. Yan H. Xu Y. Liu Y. Zhao (&) Shanghai Minhang Center for Disease Control and Prevention, 965 Zhongyi Road, Shanghai 201101, China e-mail: [email protected] W. Xu M. Mo H. Zhang The Key Laboratory of Public Health Safety of Ministry of Education, Department of Epidemiology, School of Public Health, Fudan University, Shanghai, China
cereal fiber intake. Findings from this meta-analysis indicate that the intakes of dietary fiber may be inversely associated with risk of type 2 diabetes. Keywords Dietary fiber Type 2 diabetes Prospective studies Meta-analysis
Introduction Diabetes mellitus are rising globally becoming one of the major non-communicable diseases [1]. It was estimated the number of people with diabetes increased from 153 (127–182) million in 1980, to 347 (314–382) million in 2008 globally [1].Type 2 diabetes causes substantial morbidity and mortality in those affected and is associated with enormous health care costs [2, 3]. And in Germany the annual costs of diabetes were predicted to reach a level of €21.1 billion in 2040 [3]. Moreover, type 2 diabetes has been implicated as a risk factor for other chronic illnesses, including ischemic heart disease [4] and some specific site cancers [5]. Therefore, there is considerable public health importance for preventive action reducing the burden of type 2 diabetes. Although the development of type 2 diabetes is complicated, some dietary factors are believed to be associated with increased risk of type 2 diabetes, for example low fiber intake [6]. To date, many epidemiological studies have examined type 2 diabetes risk in relation to dietary fiber intake, with some suggesting a protective association [7, 8], but not all [9, 10]. Thus, we would like to summarize the results from prospective studies of the association between dietary fiber intake and risk of type 2 diabetes. However, categories of dietary fiber intake differed between studies, which might complicate the interpretation
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of the pooled results across study populations with different categories. In this respect, a dose–response meta-analysis with restricted cubic spline functions provides a solution to the problem [11]. In addition, a linear dose–response relation between a continuous exposure and an outcome in epidemiologic research can rarely be assumed a priori [11]. No previous meta-analyses have been conducted to investigate the shape of the dose–response relationship about dietary fibre intake and type 2 diabetes and it is still unclear whether there is a nonlinear relation.Therefore, we conducted a dose–response meta-analysis of prospective studies with the aim of clarifying (1) the association between dietary fibre intake and type 2 diabetes risk, (2) the dose–response relationship between dietary fibre intake and type 2 diabetes risk, and (3) whether there is a nonlinear relation between dietary fiber intake and type 2 diabetes risk.
Methods Data sources and searches We systematically identified studies through searching EMBASE (from 1974 to April 2013) and PubMed (from 1966 to April 2013) using the following key words fiber or fibre combined with diabetes. No language restrictions were imposed. We also manually reviewed the reference lists of relevant publications to search for additional studies. All studies were included, if they met the following criteria: (1) cohort study; (2) the exposure of interest was dietary fiber intake (total dietary fiber, cereal fiber, fruit fiber, vegetable fiber, soluble fiber or insoluble fiber); (3) the outcome of interest was type 2 diabetes and (4) multivariate adjusted RR estimates or hazard ratios with 95 % confidence interval (CI). Data extraction The following data were collected from all studies: the first author’s name, year of publication, country where the study was performed, years of follow-up, study period, sex, participant age at baseline, sample size, number of cases, methods for measurement and categories of exposure, variables adjusted for in the multivariable analysis, as well as multivariate adjusted RRs with their 95 % CIs for each category of dietary fiber intake. We extracted the RRs that reflected the greatest degree of adjustment for potentially confounding variables. Data extraction was conducted by two investigators, with disagreements being resolved by consensus.
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For every study, the median or mean dietary fiber intake for each category was assigned to each corresponding RR. When the levels of dietary fiber intake were given by a range, the value of exposure was assigned as the midpoints of the ranges of the reported categories of dietary fiber intake. If the upper boundary of the highest category was not provided, we assumed that the boundary had the same amplitude as the adjacent category. When the lowest category was open-ended, we set the lower boundary to zero. Statistical analysis A combined measure was calculated as the inverse variance-weighted mean of the natural logarithm of multivariate adjusted RR with 95 % CI to assess the association of dietary fiber intake with type 2 diabetes risk for the highest versus lowest levels. The I2 of Higgins and Thompson was used to assess heterogeneity among studies [12]. I2 describes the proportion of total variation attributable to between-study heterogeneity as opposed to random error or chance. In the presence of substantial heterogeneity (I2 [ 50 %) [13], the DerSimonian and Laird randomeffect model was adopted as the combining method; otherwise, the fixed-effect model was used as the combining method. In an attempt to evaluate the possible publication bias, Egger’s test (linear regression method) was used [14]. An analysis of influence was conducted [15], which describes how robust the combined estimator is to the removal of individual study. An individual study is suspected of excessive influence, if the point estimate of its omitted analysis lies outside the 95 % CI of the combined analysis. Subgroup analyses and meta-regression models were carried out to investigate potential sources of between-study heterogeneity. For the dose–response analysis, studies included must provide the following information: the number of cases and participants (person-years), and RR with 95 % CI for each category of dietary fiber intake. A 2-stage random-effects dose–response meta-analysis was performed proposed by Orsini et al. [16] to compute the trend from the correlated log RR estimates across categories of dietary fiber intake taking into account the between-study heterogeneity. Briefly, a restricted cubic spline model, with three knots at the 25th, 50th, and 75th percentiles [17] of dietary fiber intake levels, was estimated using generalized least square regression taking into account the correlation within each set of published RRs [18]. Then the restricted maximum likelihood method in a multivariate random-effects metaanalysis [19] was used to combine the study-specific estimates. A P value for nonlinearity was calculated by testing the null hypothesis that the coefficient of the second spline is equal to 0 [20]. All statistical analyses were performed with STATA version 12 (Stata Corporation, College
Dietary fiber intake and risk of type 2 diabetes
articles), body mass index (BMI) (14 articles), physical activity (14 articles), and energy intake (11 articles). Total dietary fiber High versus low analysis
Fig. 1 Selection of studies in the meta-analysis
Station, TX, USA). P value less than 0.05 was considered statistically significant.
Results Study characteristic The search strategy identified 1615 articles, of which 1,591 articles were excluded after review of the title or abstract (Fig. 1). Twenty-four full-text articles were reviewed [7–10, 21–40]. Two articles were excluded because data from the cohorts were reported in other publications [22, 34]. Two studies were excluded because they assessed the association between dietary fiber intake and risk of the metabolic syndrome [36, 37]. One study was excluded because it assessed association between lifestyle factors and diabetes [38]. We further excluded two articles that evaluated the association between dietary glycemic index and glycemic load and the risk of diabetes [39, 40]. Thus, the meta-analysis included 17 independent prospective articles that contained 488,293 subjects and published between 1997 and 2013 (Table 1). 19,033 diabetes cases were included among the 17 reported articles. Seven studies were conducted in Europe, seven in the United States, one in Taiwan, and two in Australia. Most studies provided RR estimates that were adjusted for age (all 17 articles), smoking (13 articles), alcohol consumption (9
Data from 11 publications [7–10, 21, 24, 26, 27, 30, 32, 33] with 12 studies including 359,167 subjects were used, because one publication [32] provided two separate results (for men and women). The combined RR for high versus low intake was 0.81 (95 % CI 0.73–0.90) with moderate between-study heterogeneity (Pheterogeneity = 0.014, 2 I = 53.6 %) (Fig. 2). We did a separate analysis by including four publications [23, 25, 28, 31] only reported continuous results. Inclusion of these studies attenuated the association between total dietary fiber intake and type 2 diabetes (RR 0.91, 95 % CI 0.87–0.95; Pheterogene2 ity \ 0.001, I = 76.4 %). We then conducted subgroup analyses by gender, geographic locations and years of follow-up to explore the sources of heterogeneity. Analyses stratified by gender showed that the association between total dietary fiber and type 2 diabetes risk was somewhat stronger among studies including both male and female participants (RR 0.71, 95 % CI 0.60–0.84) than studies including only male or female participants (RR 0.78, 95 % CI 0.71–0.87; RR 0.90, 95 % CI 0.82–0.98). In stratified analysis by geographic locations, the RRs were 0.85 (95 % CI 0.76–0.96) for studies in USA and 0.76 (95 % CI 0.64–0.89) for studies in Europe. Results were consistent for studies with follow-up time of below 10 years (RR 0.82, 95 % CI 0.73–0.91) and for studies with follow-up time of 10 years or above (RR 0.81, 95 % CI 0.69–0.94). Univariate meta-regression analysis, with the covariates publication year, ethnicity (categorized as Europeans, Asians, and Americans), sex (categorized as males, females and both males and females), years of follow-up and cohort size, showed that no covariates had a significant impact on between-study heterogeneity. In the sensitivity analysis in which one study at a time was excluded and the rest were analyzed, we detected significantly inverse association between total dietary fiber and type 2 diabetes (range of summary RRs 0.78–0.82 with the larger limit of the 95 % CI never crossing 1.0).There was no indication of a publication bias from Egger’s test (P = 0.204). Dose–response analysis Five publications [7, 8, 10, 27, 30] were available to evaluate the dose–response association of total dietary fiber intake with type 2 diabetes risk. A nonlinear relationship
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Country and study period
US (1986–1992)
US (1986–1992)
US (1986–1992)
Finland
US (1991–1999)
Germany (1994–2005)
US (1995–2003)
US (1993–2007)
Taiwan
Sweden
Finland
Sweden (1991–2006)
Britain (1998–2006)
References
Salmeron [9]
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Meyer [7]
Salmeron [21]
Montonen [24]
Schulze [10]
Schulze [27]
Krishnan [29]
Hopping [32]
Weng [8]
Wirstrom [35]
Lindstrom [26]
Hindy [33]
Wannamethee [30] M
M/F
M/F
M/F
M/F
M/F
F
M/F
F
M/F
F
F
M
Sex
60–79
45–74
40–64
35–56
C30
45–75
21–69
35–65
26–46
40–69
40–65
55–69
40–75
Age, y
3428
13571
500
5477
1604
75512
40078
25067
91249
4316
65173
35988
42759
Cohort size
7
11.8
4.1
8–10
4.6
14
8
11
8
10
6
6
6
Years of follow-up
Table 1 Main characteristics of cohort studies included in the meta-analysis
162
741
114
165
141
8587
1938
844
741
156
915
1141
523
No. of cases
Self-report
Diabetes register/ HbA1c register
OGTT
OGTT
Fasting plasma glucose level/ Self-report
Self-report/ Medical records
Self-report
Self-report
Self-report
Social insurance institution register on drugtreated diabetes
Self-report
Self-report
Self-report
Case assessment
7-day recall FFQ
FFQ
3-day food record
FFQ
FFQ
FFQ
FFQ
FFQ
FFQ
Dietary history
FFQ
FFQ
FFQ
Exposure measurement
Quartiles
Quintiles
Quartiles
Tertiles
Quintiles
Quintiles
Quintiles
Quintiles
Quintiles
Quartiles
Quintiles
Quintiles
Quintiles
Exposure categories
Age, waist circumference, smoking, physical activity, social class, alcohol intake, total calorie intake and other factors
Age, sex, BMI, total energy intake, season and method
Age, sex, baseline weight, baseline 2-h glucose, physical activity, explanatory nutrient, weight change and intervention assignment
Age, family history of diabetes, BMI, physical activity, smoking, education, blood pressure and sex
Age, sex, caloric intake, family history of diabetes, BMI, smoking drinking, activity, and other factors
Age, ethnicity, BMI, physical activity, education, and calories
Age, BMI, energy intake, family history of diabetes, physical activity, cigarette use, and other factors
Age, sex, education, cycling, smoking, alcohol consumption, total energy intake, BMI, magnesium intake and other factors
Age, BMI, energy intake, alcohol, physical activity, family history of diabetes, smoking and other factors
Age, sex, geographic area, smoking, BMI, intakes of energy, and dietary factors
Age, BMI, alcohol intake, smoking, physical activity, and family history of diabetes
Age, total energy intake, BMI, WHR, education, smoking, alcohol, and physical activity
Age, BMI, alcohol intake, smoking, physical activity, family history
Adjustment
B. Yao et al.
M male, F female, FFQ food-frequency questionnaire, BMI body mass index, WHR waist-to-hip ratio, OGTT oral-glucose-tolerance test
Age, sex, country of birth, physical activity, family history of diabetes, alcohol intake, education level, weight change in the last 5 years, energy intake, BMI and WHR Continuous FFQ Self-report 365 4 31641 M/F Hodge [25]
Australia
40-69
Age, BMI, sex, field center, education, smoking status, and physical activity Continuous FFQ Fasting plasma glucose level/Self-report/use of diabetes medications 1447 9 12251 M/F Stevens [23]
US
45–64
Age, sex, family history of diabetes, smoking, triglycerides, and other factors Continuous FFQ Fasting plasma glucose level/Self-report/use of diabetes medications 138 1833 M/F Barclay [28]
Australia (1991–2004)
[49
10
Sex, age at recruitment, alcohol consumption, physical activity, waist circumference, BMI, smoking status, mean systolic blood pressure, educational level, family history of diabetes, energy intake and other factors Continuous FFQ Self-report/register of hospital discharge diagnoses 915 10 37846 M/F Sluijs [31]
Netherlands (1993–2006)
49–70
No. of cases Years of follow-up Cohort size
Cereal fiber
Sex
Age, y
was found of total dietary fiber intake with risk of type 2 diabetes (Pfor nonlinearity \ 0.01), and the RRs (95 % CI) of type 2 diabetes were 0.98 (0.90–1.06), 0.97 (0.87–1.07), 0.89 (0.80–0.99), 0.76 (0.65–0.88), and 0.66 (0.53–0.82) for 15, 20, 25, 30, and 35 g/day (Fig. 3). When assuming a linear relationship, there were nine publications [7, 8, 10, 23, 25, 27, 28, 30, 31] available including four articles only reported continuous results. The risk of type 2 diabetes decreased by 6 % (RR 0.94, 95 % CI 0.91–0.97) for 10 g/day increment in total dietary fiber intake.
Country and study period References
Table 1 Main characteristics of cohort studies included in the meta-analysis
Case assessment
Exposure measurement
Exposure categories
Adjustment
Dietary fiber intake and risk of type 2 diabetes
High versus low analysis Data from ten publications [7, 9, 10, 21, 24, 27, 29, 30, 32, 35] with 11 studies including 389,047 subjects were used in the analysis of high versus low cereal fiber intake and type 2 diabetes risk, because one publication [32] provided two separate results (for men and women). The combined RR was 0.77 (95 % CI 0.69–0.85) with moderate betweenstudy heterogeneity (Pheterogeneity = 0.011, I2 = 56.2 %) (Fig. 4). We did a separate analysis by including three articles [23, 25, 28] only reported continuous results. Inclusion of these studies attenuated the association between cereal fiber intake and type 2 diabetes (RR 0.85, 95 % CI 0.79–0.91; Pheterogeneity \ 0.001, I2 = 72.8 %). We conducted subgroup analyses according to gender, geographic locations and years of follow-up. The association between cereal fiber and type 2 diabetes was somewhat stronger among studies including both male and female participants (RR 0.71, 95 % CI 0.58–0.87) than studies including only male or female participants (RR 0.89, 95 % CI 0.81–0.87; RR 0.76, 95 % CI 0.66–0.86). Analyses stratified by geographic locations showed that the RRs were 0.78 (95 % CI 0.70–0.87) for studies in USA and 0.72 (95 % CI 0.60–0.86) for studies in Europe. In stratified analysis by years of follow-up, the RRs were 0.73 (95 % CI 0.67–0.80) for studies with follow-up time of below 10 years and 0.77 (95 % CI 0.70–0.85) for studies with follow-up time of 10 years or above. Univariate metaregression analysis showed that the covariates publication year and years of follow-up had a significant impact on between-study heterogeneity. Sensitivity analysis excluding one study at a time did not substantially modify the findings. Egger’s test for publication bias was statistically significant (P = 0.004). Dose–response analysis Five publications [7, 10, 27, 29, 35] were available to evaluate the dose–response association of cereal fiber
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Fig. 2 Forest plot of relative risk of high versus low analysis for total dietary fiber intake with type 2 diabetes risk. ES effect size, I–V, inverse variance, D ? L DerSimonian and Laird
(0.64–0.82), and 0.67 (0.55–0.82), for 3, 6, 9, 12, and 16 g/day (Fig. 5). When assuming a linear relationship, there were eight publications [7, 10, 23, 25, 27–29, 35] available including three studies only reported continuous results. The risk of type 2 diabetes decreased by 6 % (RR 0.94, 95 % CI 0.93–0.96) for 2 g/day increment in cereal fiber intake. Fruit fiber High versus low analysis
Fig. 3 The dose–response analysis between total dietary fiber intake and risk of type 2 diabetes in prospective studies with restricted cubic splines in a multivariate random-effects dose–response model. The solid line and the long dash line represent the estimated relative risk and its 95 % CI of the nonlinear relationship. Short dash line represents the linear relationship
intake with type 2 diabetes risk. The departure from nonlinear relationship was not significant (Pfor nonlinearity = 0.721). The RRs (95 % CI) of type 2 diabetes were 0.92 (0.88–0.96), 0.85 (0.77–0.91), 0.79 (0.73–0.86), 0.73
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Data from eight publications [7–10, 21, 24, 27, 32] with nine studies including 341,668 subjects were used, because one publication [32] provided two separate results (for men and women). The combined RR for high versus low intake was 0.94 (95 % CI 0.88–0.99) with marginal betweenstudy heterogeneity (Pheterogeneity = 0.192, I2 = 28.5 %). We did a separate analysis by including three articles [23, 25, 28] only reported continuous results. The association between fruit fiber intake and type 2 diabetes was changed and not statistically significant (RR 1.00, 95 % CI 0.99–1.02; Pheterogeneity = 0.162, I2 = 28.0 %). We then conducted subgroup analyses to investigate potential sources of between-study heterogeneity. Overall,
Dietary fiber intake and risk of type 2 diabetes
Fig. 4 Forest plot of relative risk of high versus low analysis for cereal fiber intake with type 2 diabetes risk. ES effect size, I–V inverse variance, D ? L DerSimonian and Laird
summary odds ratio. No significant publication bias was found according to Egger’s test (P = 0. 418). Dose–response analysis
Fig. 5 The dose–response analysis between cereal fiber intake and risk of type 2 diabetes in prospective studies with restricted cubic splines in a multivariate random-effects dose–response model. The solid line and the long dash line represent the estimated relative risk and its 95 % CI of the nonlinear relationship. Short dash line represents the linear relationship
there were no associations between high versus low intake of fruit fiber and type 2 diabetes risk in all strata. Univariate meta-regression analysis, with all covariates, showed that no covariates had a significant impact on between-study heterogeneity. Sensitivity analysis leaving one out at a time produced no statistically significantly increased or decreased
Four publications [7, 8, 10, 27] were included in the dose– response analysis. The range of fruit fiber intake was (0.2–20.6) g/day. The departure from nonlinear relationship was not significant (Pfor nonlinearity = 0.828).The RRs (95 % CI) of type 2 diabetes were 0.97 (0.92–1.03), 0.95 (0.85–1.06), 0.93 (0.83–1.04), 0.90 (0.78–1.04), and 0.82 (0.57–1.20), for 2, 4, 6, 10, and 20 g/day. When assuming a linear relationship, there were seven publications [7, 8, 10, 23, 25, 27, 28] available including three studies only reported continuous results. The summary RR for 2 g/day increment in fruit fiber intake was not statistically significant (RR 0.99, 95 % CI 0.96–1.02). Vegetable fiber High versus low analysis Data from nine publications [7–10, 21, 24, 27, 30, 32] with ten studies including 345,096 subjects were used, because one publication [32] provided two separate results (for men
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and women). The combined RR for high versus low intake was 0.95 (95 % CI 0.84–1.07) with moderate betweenstudy heterogeneity (Pheterogeneity = 0.008, I2 = 59.4 %). We did a separate analysis by including two articles [25, 28] only reported continuous results. The association between vegetable fiber intake and type 2 diabetes was not changed greatly (RR 0.93, 95 % CI 0.84–1.02; Pheterogene2 ity = 0.007, I = 56.0 %). We then conducted subgroup analyses. Overall, there were no associations between high versus low intake of vegetable fiber and type 2 diabetes risk in all strata, but the associations were statistically significant in studies including only male participants (RR 0.83, 95 % CI 0.74–0.92) and in studies with follow-up time of 10 years or above (RR 0.88, 95 % CI 0.82–0.95). Univariate metaregression analysis showed that the covariates publication year and cohort size had a significant impact on betweenstudy heterogeneity. Sensitivity analysis excluding one study at a time did not substantially modify the findings. We found no evidence of publication bias (Egger’s test: P = 0.776). Dose–response analysis Four publications [7, 8, 10, 27] were included in the dose– response analysis. The range of fruit fiber intake was (0.7–15.8) g/day. The departure from nonlinear relationship was not significant (Pfor nonlinearity = 0.180). The RRs (95 % CI) of type 2 diabetes were 1.03 (0.96–1.11), 1.05 (0.93–1.18), 1.00 (0.89–1.13), 0.95 (0.83–1.10), and 0.88 (0.70–1.11), for 3, 6, 9, 12, and 15 g/day. When assuming a linear relationship, there were six publications [7, 8, 10, 25, 27, 28] available including two studies only reported continuous results. The summary RR for 2 g/day increment in vegetable fiber intake was not statistically significant (RR 0.99, 95 % CI 0.97–1.02). Soluble and insoluble fiber For soluble and insoluble fiber, data from three publications [7, 24, 27] including 65,371 subjects were used. The combined RRs for high versus low intake were 0.85 (95 % CI 0.72–1.01, I2 = 0.0 %, Pheterogeneity = 0.457) for soluble fiber and 0.75 (95 %CI 0.63–0.89, I2 = 35.0 %, Pheterogeneity = 0.215) for insoluble fiber. Sensitivity analysis excluding one study at a time did not substantially modify the findings. Egger’s test was conducted to assess the publication bias of the literature. There was no evidence of bias (Egger’s test: P = 0.217 for soluble fiber and P = 0.767 for insoluble fiber). Only two publications [7, 27] were eligible for dose–response analysis. The range of soluble fiber intake was (4.19–9.60) g/day and the range of insoluble fiber intake was
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(9.93–19.84) g/day. Then dose–response analysis for soluble and insoluble fiber was not conducted.
Discussion The findings from this meta-analysis of prospective studies support an inverse association between intake of total dietary fiber, cereal fiber, fruit fiber or insoluble fiber and risk of type 2 diabetes in a comparison of the highest with the lowest categories. Furthermore, a nonlinear relationship of total fiber intake with type 2 diabetes risk was found and a linear relationship of cereal fiber intake with type 2 diabetes risk was found. In our analysis, we found an inverse association between fruit fiber intake and type 2 diabetes risk in high versus low analysis, which was different from the previous result [27]. However, when including studies only reported continuous results no association between fruit fiber intake and type 2 diabetes risk in high versus low analysis was found. In addition, a dose–response relation of fruit fiber intake with type 2 diabetes risk was not found. The lack of a dose– response relation revealed that future studies are needed to assess whether this association in high versus low analysis is causal. To our knowledge, this is the first meta-analysis to explore a dose–response association of dietary fiber intake with type 2 diabetes risk. We found a nonlinear association of total fiber intake with type 2 diabetes risk, which has important public health implications. The nonlinear association showed that total dietary fiber consumption might have a threshold effect on risk of type 2 diabetes. When the intake of total dietary fiber was achieving 25 g/day or more, it was inversely associated with risk of type 2 diabetes. Currently the adequate intakes for fiber in the United States are 14 g per 1,000 calories, or 25 g/day for women and 38 g/day for men [41]. Most Americans greatly under consume dietary fiber, and usual intake averages only 15 g/day [41]. The Shanghai Women’s study [42] reported that the highest quintile of dietary fiber intake was 16.3 g/day. Then increased consumption of fiber-rich foods may bring great benefits in type 2 diabetes prevention, especially in those at high risk. Several potential mechanisms may explain an inverse association between dietary fiber intake and risk of type 2 diabetes. Observational studies showed that high intake of dietary fiber may reduce the risk of overweight/obesity [43], which is an established risk factor for type 2 diabetes. Consumption of soluble fiber could delay gastric emptying and decrease absorption of macronutrients, resulting in lower postprandial blood glucose and insulin level [44]. However, our study found insoluble fiber not soluble fiber was inverse associated with risk of type 2 diabetes. Earlier study showed that an increased intake of total dietary fiber
Dietary fiber intake and risk of type 2 diabetes
was inversely associated with markers of insulin resistance [45]. And subjects consuming diets high in insoluble fiber may reduce diabetes risk through improving insulin resistance [46]. Our study had some important strength. All the original articles included used a prospective cohort study design, which greatly reduced the selection bias and recall bias. Many articles in this meta-analysis had a large sample and a long duration of follow-up which enhanced the power to detect a significant association and provided more reliable estimates. Moreover, we found a significant dose–response relation between total dietary fiber and cereal fiber intake and risk of type 2 diabetes, which were more precise. Our study also has several limitations. First, a meta-analysis is not able to address problems with confounding factors that could be inherent in the original studies. Although most articles included in this meta-analysis had adjusted for major potential confounders, including age, smoking, alcohol consumption, BMI, physical activity, and energy intake. However, only two studies adjusted for magnesium, which has been shown to decrease the incidence of type 2 diabetes [27]. In addition, residual or unknown confounding cannot be excluded as a potential explanation for the observed findings. Second, our results are likely to be affected by some degree of misclassification of exposure. Most of the original articles included in our meta-analysis used a validated food-frequency questionnaire, but only one reports updated the information on dietary fiber intake during follow-up [26]. Third, publication bias could also be of a concern. Although yet little evidence of publication bias was observed, it is noteworthy that these tests were based on a relatively small number of articles. In conclusion, this meta-analysis of prospective cohort studies provides evidence of a significant inverse association between dietary fiber and risk of type 2 diabetes. Our findings support current recommendations that consumption of at least 25 g/day total dietary fiber may prevent type 2 diabetes. Further studies elucidating mechanisms underlying the beneficial effects of dietary fiber intake for the prevention of type 2 diabetes are warranted. Acknowledgments
None.
Conflict of interest No conflict of interest existed for any of the authors.
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META-ANALYSIS
Dietary fiber intake and risk of type 2 diabetes: a dose–response analysis of prospective studies Baodong Yao • Hong Fang • Wanghong Xu Yujie Yan • Huilin Xu • Yinan Liu • Miao Mo • Hua Zhang • Yanping Zhao
•
Received: 4 July 2013 / Accepted: 27 December 2013 Ó Springer Science+Business Media Dordrecht 2014
Abstract Observational studies suggest an association between dietary fiber intake and risk of type 2 diabetes, but the results are inconclusive. We conducted a meta-analysis of prospective studies evaluating the associations of dietary fiber intake and risk of type 2 diabetes. Relevant studies were identified by searching EMBASE (from 1974 to April 2013) and PubMed (from 1966 to April 2013). The fixed or random-effect model was selected based on the homogeneity test among studies. In addition, a 2-stage random-effects dose–response meta-analysis was performed. We identified 17 prospective cohort studies of dietary fiber intake and risk of type 2 diabetes involving 19,033 cases and 488,293 participants. The combined RR (95 % CI) of type 2 diabetes for intake of total dietary fiber, cereal fiber, fruit fiber and insoluble fiber was 0.81 (0.73–0.90), 0.77 (0.69–0.85), 0.94 (0.88–0.99) and 0.75 (0.63–0.89), respectively. A nonlinear relationship was found of total dietary fiber intake with risk of type 2 diabetes (Pfor nonlinearity \ 0.01), and the RRs (95 % CI) of type 2 diabetes were 0.98 (0.90–1.06), 0.97 (0.87–1.07), 0.89 (0.80–0.99), 0.76 (0.65–0.88), and 0.66 (0.53–0.82) for 15, 20, 25, 30, and 35 g/day. The departure from nonlinear relationship was not significant (Pfor nonlinearity = 0.72), and the risk of type 2 diabetes decreased by 6 % (RR 0.94, 95 % CI 0.93–0.96) for 2 g/day increment in
Baodong Yao and Hong Fang have contributed equally to this work. B. Yao H. Fang Y. Yan H. Xu Y. Liu Y. Zhao (&) Shanghai Minhang Center for Disease Control and Prevention, 965 Zhongyi Road, Shanghai 201101, China e-mail: [email protected] W. Xu M. Mo H. Zhang The Key Laboratory of Public Health Safety of Ministry of Education, Department of Epidemiology, School of Public Health, Fudan University, Shanghai, China
cereal fiber intake. Findings from this meta-analysis indicate that the intakes of dietary fiber may be inversely associated with risk of type 2 diabetes. Keywords Dietary fiber Type 2 diabetes Prospective studies Meta-analysis
Introduction Diabetes mellitus are rising globally becoming one of the major non-communicable diseases [1]. It was estimated the number of people with diabetes increased from 153 (127–182) million in 1980, to 347 (314–382) million in 2008 globally [1].Type 2 diabetes causes substantial morbidity and mortality in those affected and is associated with enormous health care costs [2, 3]. And in Germany the annual costs of diabetes were predicted to reach a level of €21.1 billion in 2040 [3]. Moreover, type 2 diabetes has been implicated as a risk factor for other chronic illnesses, including ischemic heart disease [4] and some specific site cancers [5]. Therefore, there is considerable public health importance for preventive action reducing the burden of type 2 diabetes. Although the development of type 2 diabetes is complicated, some dietary factors are believed to be associated with increased risk of type 2 diabetes, for example low fiber intake [6]. To date, many epidemiological studies have examined type 2 diabetes risk in relation to dietary fiber intake, with some suggesting a protective association [7, 8], but not all [9, 10]. Thus, we would like to summarize the results from prospective studies of the association between dietary fiber intake and risk of type 2 diabetes. However, categories of dietary fiber intake differed between studies, which might complicate the interpretation
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of the pooled results across study populations with different categories. In this respect, a dose–response meta-analysis with restricted cubic spline functions provides a solution to the problem [11]. In addition, a linear dose–response relation between a continuous exposure and an outcome in epidemiologic research can rarely be assumed a priori [11]. No previous meta-analyses have been conducted to investigate the shape of the dose–response relationship about dietary fibre intake and type 2 diabetes and it is still unclear whether there is a nonlinear relation.Therefore, we conducted a dose–response meta-analysis of prospective studies with the aim of clarifying (1) the association between dietary fibre intake and type 2 diabetes risk, (2) the dose–response relationship between dietary fibre intake and type 2 diabetes risk, and (3) whether there is a nonlinear relation between dietary fiber intake and type 2 diabetes risk.
Methods Data sources and searches We systematically identified studies through searching EMBASE (from 1974 to April 2013) and PubMed (from 1966 to April 2013) using the following key words fiber or fibre combined with diabetes. No language restrictions were imposed. We also manually reviewed the reference lists of relevant publications to search for additional studies. All studies were included, if they met the following criteria: (1) cohort study; (2) the exposure of interest was dietary fiber intake (total dietary fiber, cereal fiber, fruit fiber, vegetable fiber, soluble fiber or insoluble fiber); (3) the outcome of interest was type 2 diabetes and (4) multivariate adjusted RR estimates or hazard ratios with 95 % confidence interval (CI). Data extraction The following data were collected from all studies: the first author’s name, year of publication, country where the study was performed, years of follow-up, study period, sex, participant age at baseline, sample size, number of cases, methods for measurement and categories of exposure, variables adjusted for in the multivariable analysis, as well as multivariate adjusted RRs with their 95 % CIs for each category of dietary fiber intake. We extracted the RRs that reflected the greatest degree of adjustment for potentially confounding variables. Data extraction was conducted by two investigators, with disagreements being resolved by consensus.
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For every study, the median or mean dietary fiber intake for each category was assigned to each corresponding RR. When the levels of dietary fiber intake were given by a range, the value of exposure was assigned as the midpoints of the ranges of the reported categories of dietary fiber intake. If the upper boundary of the highest category was not provided, we assumed that the boundary had the same amplitude as the adjacent category. When the lowest category was open-ended, we set the lower boundary to zero. Statistical analysis A combined measure was calculated as the inverse variance-weighted mean of the natural logarithm of multivariate adjusted RR with 95 % CI to assess the association of dietary fiber intake with type 2 diabetes risk for the highest versus lowest levels. The I2 of Higgins and Thompson was used to assess heterogeneity among studies [12]. I2 describes the proportion of total variation attributable to between-study heterogeneity as opposed to random error or chance. In the presence of substantial heterogeneity (I2 [ 50 %) [13], the DerSimonian and Laird randomeffect model was adopted as the combining method; otherwise, the fixed-effect model was used as the combining method. In an attempt to evaluate the possible publication bias, Egger’s test (linear regression method) was used [14]. An analysis of influence was conducted [15], which describes how robust the combined estimator is to the removal of individual study. An individual study is suspected of excessive influence, if the point estimate of its omitted analysis lies outside the 95 % CI of the combined analysis. Subgroup analyses and meta-regression models were carried out to investigate potential sources of between-study heterogeneity. For the dose–response analysis, studies included must provide the following information: the number of cases and participants (person-years), and RR with 95 % CI for each category of dietary fiber intake. A 2-stage random-effects dose–response meta-analysis was performed proposed by Orsini et al. [16] to compute the trend from the correlated log RR estimates across categories of dietary fiber intake taking into account the between-study heterogeneity. Briefly, a restricted cubic spline model, with three knots at the 25th, 50th, and 75th percentiles [17] of dietary fiber intake levels, was estimated using generalized least square regression taking into account the correlation within each set of published RRs [18]. Then the restricted maximum likelihood method in a multivariate random-effects metaanalysis [19] was used to combine the study-specific estimates. A P value for nonlinearity was calculated by testing the null hypothesis that the coefficient of the second spline is equal to 0 [20]. All statistical analyses were performed with STATA version 12 (Stata Corporation, College
Dietary fiber intake and risk of type 2 diabetes
articles), body mass index (BMI) (14 articles), physical activity (14 articles), and energy intake (11 articles). Total dietary fiber High versus low analysis
Fig. 1 Selection of studies in the meta-analysis
Station, TX, USA). P value less than 0.05 was considered statistically significant.
Results Study characteristic The search strategy identified 1615 articles, of which 1,591 articles were excluded after review of the title or abstract (Fig. 1). Twenty-four full-text articles were reviewed [7–10, 21–40]. Two articles were excluded because data from the cohorts were reported in other publications [22, 34]. Two studies were excluded because they assessed the association between dietary fiber intake and risk of the metabolic syndrome [36, 37]. One study was excluded because it assessed association between lifestyle factors and diabetes [38]. We further excluded two articles that evaluated the association between dietary glycemic index and glycemic load and the risk of diabetes [39, 40]. Thus, the meta-analysis included 17 independent prospective articles that contained 488,293 subjects and published between 1997 and 2013 (Table 1). 19,033 diabetes cases were included among the 17 reported articles. Seven studies were conducted in Europe, seven in the United States, one in Taiwan, and two in Australia. Most studies provided RR estimates that were adjusted for age (all 17 articles), smoking (13 articles), alcohol consumption (9
Data from 11 publications [7–10, 21, 24, 26, 27, 30, 32, 33] with 12 studies including 359,167 subjects were used, because one publication [32] provided two separate results (for men and women). The combined RR for high versus low intake was 0.81 (95 % CI 0.73–0.90) with moderate between-study heterogeneity (Pheterogeneity = 0.014, 2 I = 53.6 %) (Fig. 2). We did a separate analysis by including four publications [23, 25, 28, 31] only reported continuous results. Inclusion of these studies attenuated the association between total dietary fiber intake and type 2 diabetes (RR 0.91, 95 % CI 0.87–0.95; Pheterogene2 ity \ 0.001, I = 76.4 %). We then conducted subgroup analyses by gender, geographic locations and years of follow-up to explore the sources of heterogeneity. Analyses stratified by gender showed that the association between total dietary fiber and type 2 diabetes risk was somewhat stronger among studies including both male and female participants (RR 0.71, 95 % CI 0.60–0.84) than studies including only male or female participants (RR 0.78, 95 % CI 0.71–0.87; RR 0.90, 95 % CI 0.82–0.98). In stratified analysis by geographic locations, the RRs were 0.85 (95 % CI 0.76–0.96) for studies in USA and 0.76 (95 % CI 0.64–0.89) for studies in Europe. Results were consistent for studies with follow-up time of below 10 years (RR 0.82, 95 % CI 0.73–0.91) and for studies with follow-up time of 10 years or above (RR 0.81, 95 % CI 0.69–0.94). Univariate meta-regression analysis, with the covariates publication year, ethnicity (categorized as Europeans, Asians, and Americans), sex (categorized as males, females and both males and females), years of follow-up and cohort size, showed that no covariates had a significant impact on between-study heterogeneity. In the sensitivity analysis in which one study at a time was excluded and the rest were analyzed, we detected significantly inverse association between total dietary fiber and type 2 diabetes (range of summary RRs 0.78–0.82 with the larger limit of the 95 % CI never crossing 1.0).There was no indication of a publication bias from Egger’s test (P = 0.204). Dose–response analysis Five publications [7, 8, 10, 27, 30] were available to evaluate the dose–response association of total dietary fiber intake with type 2 diabetes risk. A nonlinear relationship
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Country and study period
US (1986–1992)
US (1986–1992)
US (1986–1992)
Finland
US (1991–1999)
Germany (1994–2005)
US (1995–2003)
US (1993–2007)
Taiwan
Sweden
Finland
Sweden (1991–2006)
Britain (1998–2006)
References
Salmeron [9]
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Meyer [7]
Salmeron [21]
Montonen [24]
Schulze [10]
Schulze [27]
Krishnan [29]
Hopping [32]
Weng [8]
Wirstrom [35]
Lindstrom [26]
Hindy [33]
Wannamethee [30] M
M/F
M/F
M/F
M/F
M/F
F
M/F
F
M/F
F
F
M
Sex
60–79
45–74
40–64
35–56
C30
45–75
21–69
35–65
26–46
40–69
40–65
55–69
40–75
Age, y
3428
13571
500
5477
1604
75512
40078
25067
91249
4316
65173
35988
42759
Cohort size
7
11.8
4.1
8–10
4.6
14
8
11
8
10
6
6
6
Years of follow-up
Table 1 Main characteristics of cohort studies included in the meta-analysis
162
741
114
165
141
8587
1938
844
741
156
915
1141
523
No. of cases
Self-report
Diabetes register/ HbA1c register
OGTT
OGTT
Fasting plasma glucose level/ Self-report
Self-report/ Medical records
Self-report
Self-report
Self-report
Social insurance institution register on drugtreated diabetes
Self-report
Self-report
Self-report
Case assessment
7-day recall FFQ
FFQ
3-day food record
FFQ
FFQ
FFQ
FFQ
FFQ
FFQ
Dietary history
FFQ
FFQ
FFQ
Exposure measurement
Quartiles
Quintiles
Quartiles
Tertiles
Quintiles
Quintiles
Quintiles
Quintiles
Quintiles
Quartiles
Quintiles
Quintiles
Quintiles
Exposure categories
Age, waist circumference, smoking, physical activity, social class, alcohol intake, total calorie intake and other factors
Age, sex, BMI, total energy intake, season and method
Age, sex, baseline weight, baseline 2-h glucose, physical activity, explanatory nutrient, weight change and intervention assignment
Age, family history of diabetes, BMI, physical activity, smoking, education, blood pressure and sex
Age, sex, caloric intake, family history of diabetes, BMI, smoking drinking, activity, and other factors
Age, ethnicity, BMI, physical activity, education, and calories
Age, BMI, energy intake, family history of diabetes, physical activity, cigarette use, and other factors
Age, sex, education, cycling, smoking, alcohol consumption, total energy intake, BMI, magnesium intake and other factors
Age, BMI, energy intake, alcohol, physical activity, family history of diabetes, smoking and other factors
Age, sex, geographic area, smoking, BMI, intakes of energy, and dietary factors
Age, BMI, alcohol intake, smoking, physical activity, and family history of diabetes
Age, total energy intake, BMI, WHR, education, smoking, alcohol, and physical activity
Age, BMI, alcohol intake, smoking, physical activity, family history
Adjustment
B. Yao et al.
M male, F female, FFQ food-frequency questionnaire, BMI body mass index, WHR waist-to-hip ratio, OGTT oral-glucose-tolerance test
Age, sex, country of birth, physical activity, family history of diabetes, alcohol intake, education level, weight change in the last 5 years, energy intake, BMI and WHR Continuous FFQ Self-report 365 4 31641 M/F Hodge [25]
Australia
40-69
Age, BMI, sex, field center, education, smoking status, and physical activity Continuous FFQ Fasting plasma glucose level/Self-report/use of diabetes medications 1447 9 12251 M/F Stevens [23]
US
45–64
Age, sex, family history of diabetes, smoking, triglycerides, and other factors Continuous FFQ Fasting plasma glucose level/Self-report/use of diabetes medications 138 1833 M/F Barclay [28]
Australia (1991–2004)
[49
10
Sex, age at recruitment, alcohol consumption, physical activity, waist circumference, BMI, smoking status, mean systolic blood pressure, educational level, family history of diabetes, energy intake and other factors Continuous FFQ Self-report/register of hospital discharge diagnoses 915 10 37846 M/F Sluijs [31]
Netherlands (1993–2006)
49–70
No. of cases Years of follow-up Cohort size
Cereal fiber
Sex
Age, y
was found of total dietary fiber intake with risk of type 2 diabetes (Pfor nonlinearity \ 0.01), and the RRs (95 % CI) of type 2 diabetes were 0.98 (0.90–1.06), 0.97 (0.87–1.07), 0.89 (0.80–0.99), 0.76 (0.65–0.88), and 0.66 (0.53–0.82) for 15, 20, 25, 30, and 35 g/day (Fig. 3). When assuming a linear relationship, there were nine publications [7, 8, 10, 23, 25, 27, 28, 30, 31] available including four articles only reported continuous results. The risk of type 2 diabetes decreased by 6 % (RR 0.94, 95 % CI 0.91–0.97) for 10 g/day increment in total dietary fiber intake.
Country and study period References
Table 1 Main characteristics of cohort studies included in the meta-analysis
Case assessment
Exposure measurement
Exposure categories
Adjustment
Dietary fiber intake and risk of type 2 diabetes
High versus low analysis Data from ten publications [7, 9, 10, 21, 24, 27, 29, 30, 32, 35] with 11 studies including 389,047 subjects were used in the analysis of high versus low cereal fiber intake and type 2 diabetes risk, because one publication [32] provided two separate results (for men and women). The combined RR was 0.77 (95 % CI 0.69–0.85) with moderate betweenstudy heterogeneity (Pheterogeneity = 0.011, I2 = 56.2 %) (Fig. 4). We did a separate analysis by including three articles [23, 25, 28] only reported continuous results. Inclusion of these studies attenuated the association between cereal fiber intake and type 2 diabetes (RR 0.85, 95 % CI 0.79–0.91; Pheterogeneity \ 0.001, I2 = 72.8 %). We conducted subgroup analyses according to gender, geographic locations and years of follow-up. The association between cereal fiber and type 2 diabetes was somewhat stronger among studies including both male and female participants (RR 0.71, 95 % CI 0.58–0.87) than studies including only male or female participants (RR 0.89, 95 % CI 0.81–0.87; RR 0.76, 95 % CI 0.66–0.86). Analyses stratified by geographic locations showed that the RRs were 0.78 (95 % CI 0.70–0.87) for studies in USA and 0.72 (95 % CI 0.60–0.86) for studies in Europe. In stratified analysis by years of follow-up, the RRs were 0.73 (95 % CI 0.67–0.80) for studies with follow-up time of below 10 years and 0.77 (95 % CI 0.70–0.85) for studies with follow-up time of 10 years or above. Univariate metaregression analysis showed that the covariates publication year and years of follow-up had a significant impact on between-study heterogeneity. Sensitivity analysis excluding one study at a time did not substantially modify the findings. Egger’s test for publication bias was statistically significant (P = 0.004). Dose–response analysis Five publications [7, 10, 27, 29, 35] were available to evaluate the dose–response association of cereal fiber
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Fig. 2 Forest plot of relative risk of high versus low analysis for total dietary fiber intake with type 2 diabetes risk. ES effect size, I–V, inverse variance, D ? L DerSimonian and Laird
(0.64–0.82), and 0.67 (0.55–0.82), for 3, 6, 9, 12, and 16 g/day (Fig. 5). When assuming a linear relationship, there were eight publications [7, 10, 23, 25, 27–29, 35] available including three studies only reported continuous results. The risk of type 2 diabetes decreased by 6 % (RR 0.94, 95 % CI 0.93–0.96) for 2 g/day increment in cereal fiber intake. Fruit fiber High versus low analysis
Fig. 3 The dose–response analysis between total dietary fiber intake and risk of type 2 diabetes in prospective studies with restricted cubic splines in a multivariate random-effects dose–response model. The solid line and the long dash line represent the estimated relative risk and its 95 % CI of the nonlinear relationship. Short dash line represents the linear relationship
intake with type 2 diabetes risk. The departure from nonlinear relationship was not significant (Pfor nonlinearity = 0.721). The RRs (95 % CI) of type 2 diabetes were 0.92 (0.88–0.96), 0.85 (0.77–0.91), 0.79 (0.73–0.86), 0.73
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Data from eight publications [7–10, 21, 24, 27, 32] with nine studies including 341,668 subjects were used, because one publication [32] provided two separate results (for men and women). The combined RR for high versus low intake was 0.94 (95 % CI 0.88–0.99) with marginal betweenstudy heterogeneity (Pheterogeneity = 0.192, I2 = 28.5 %). We did a separate analysis by including three articles [23, 25, 28] only reported continuous results. The association between fruit fiber intake and type 2 diabetes was changed and not statistically significant (RR 1.00, 95 % CI 0.99–1.02; Pheterogeneity = 0.162, I2 = 28.0 %). We then conducted subgroup analyses to investigate potential sources of between-study heterogeneity. Overall,
Dietary fiber intake and risk of type 2 diabetes
Fig. 4 Forest plot of relative risk of high versus low analysis for cereal fiber intake with type 2 diabetes risk. ES effect size, I–V inverse variance, D ? L DerSimonian and Laird
summary odds ratio. No significant publication bias was found according to Egger’s test (P = 0. 418). Dose–response analysis
Fig. 5 The dose–response analysis between cereal fiber intake and risk of type 2 diabetes in prospective studies with restricted cubic splines in a multivariate random-effects dose–response model. The solid line and the long dash line represent the estimated relative risk and its 95 % CI of the nonlinear relationship. Short dash line represents the linear relationship
there were no associations between high versus low intake of fruit fiber and type 2 diabetes risk in all strata. Univariate meta-regression analysis, with all covariates, showed that no covariates had a significant impact on between-study heterogeneity. Sensitivity analysis leaving one out at a time produced no statistically significantly increased or decreased
Four publications [7, 8, 10, 27] were included in the dose– response analysis. The range of fruit fiber intake was (0.2–20.6) g/day. The departure from nonlinear relationship was not significant (Pfor nonlinearity = 0.828).The RRs (95 % CI) of type 2 diabetes were 0.97 (0.92–1.03), 0.95 (0.85–1.06), 0.93 (0.83–1.04), 0.90 (0.78–1.04), and 0.82 (0.57–1.20), for 2, 4, 6, 10, and 20 g/day. When assuming a linear relationship, there were seven publications [7, 8, 10, 23, 25, 27, 28] available including three studies only reported continuous results. The summary RR for 2 g/day increment in fruit fiber intake was not statistically significant (RR 0.99, 95 % CI 0.96–1.02). Vegetable fiber High versus low analysis Data from nine publications [7–10, 21, 24, 27, 30, 32] with ten studies including 345,096 subjects were used, because one publication [32] provided two separate results (for men
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and women). The combined RR for high versus low intake was 0.95 (95 % CI 0.84–1.07) with moderate betweenstudy heterogeneity (Pheterogeneity = 0.008, I2 = 59.4 %). We did a separate analysis by including two articles [25, 28] only reported continuous results. The association between vegetable fiber intake and type 2 diabetes was not changed greatly (RR 0.93, 95 % CI 0.84–1.02; Pheterogene2 ity = 0.007, I = 56.0 %). We then conducted subgroup analyses. Overall, there were no associations between high versus low intake of vegetable fiber and type 2 diabetes risk in all strata, but the associations were statistically significant in studies including only male participants (RR 0.83, 95 % CI 0.74–0.92) and in studies with follow-up time of 10 years or above (RR 0.88, 95 % CI 0.82–0.95). Univariate metaregression analysis showed that the covariates publication year and cohort size had a significant impact on betweenstudy heterogeneity. Sensitivity analysis excluding one study at a time did not substantially modify the findings. We found no evidence of publication bias (Egger’s test: P = 0.776). Dose–response analysis Four publications [7, 8, 10, 27] were included in the dose– response analysis. The range of fruit fiber intake was (0.7–15.8) g/day. The departure from nonlinear relationship was not significant (Pfor nonlinearity = 0.180). The RRs (95 % CI) of type 2 diabetes were 1.03 (0.96–1.11), 1.05 (0.93–1.18), 1.00 (0.89–1.13), 0.95 (0.83–1.10), and 0.88 (0.70–1.11), for 3, 6, 9, 12, and 15 g/day. When assuming a linear relationship, there were six publications [7, 8, 10, 25, 27, 28] available including two studies only reported continuous results. The summary RR for 2 g/day increment in vegetable fiber intake was not statistically significant (RR 0.99, 95 % CI 0.97–1.02). Soluble and insoluble fiber For soluble and insoluble fiber, data from three publications [7, 24, 27] including 65,371 subjects were used. The combined RRs for high versus low intake were 0.85 (95 % CI 0.72–1.01, I2 = 0.0 %, Pheterogeneity = 0.457) for soluble fiber and 0.75 (95 %CI 0.63–0.89, I2 = 35.0 %, Pheterogeneity = 0.215) for insoluble fiber. Sensitivity analysis excluding one study at a time did not substantially modify the findings. Egger’s test was conducted to assess the publication bias of the literature. There was no evidence of bias (Egger’s test: P = 0.217 for soluble fiber and P = 0.767 for insoluble fiber). Only two publications [7, 27] were eligible for dose–response analysis. The range of soluble fiber intake was (4.19–9.60) g/day and the range of insoluble fiber intake was
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(9.93–19.84) g/day. Then dose–response analysis for soluble and insoluble fiber was not conducted.
Discussion The findings from this meta-analysis of prospective studies support an inverse association between intake of total dietary fiber, cereal fiber, fruit fiber or insoluble fiber and risk of type 2 diabetes in a comparison of the highest with the lowest categories. Furthermore, a nonlinear relationship of total fiber intake with type 2 diabetes risk was found and a linear relationship of cereal fiber intake with type 2 diabetes risk was found. In our analysis, we found an inverse association between fruit fiber intake and type 2 diabetes risk in high versus low analysis, which was different from the previous result [27]. However, when including studies only reported continuous results no association between fruit fiber intake and type 2 diabetes risk in high versus low analysis was found. In addition, a dose–response relation of fruit fiber intake with type 2 diabetes risk was not found. The lack of a dose– response relation revealed that future studies are needed to assess whether this association in high versus low analysis is causal. To our knowledge, this is the first meta-analysis to explore a dose–response association of dietary fiber intake with type 2 diabetes risk. We found a nonlinear association of total fiber intake with type 2 diabetes risk, which has important public health implications. The nonlinear association showed that total dietary fiber consumption might have a threshold effect on risk of type 2 diabetes. When the intake of total dietary fiber was achieving 25 g/day or more, it was inversely associated with risk of type 2 diabetes. Currently the adequate intakes for fiber in the United States are 14 g per 1,000 calories, or 25 g/day for women and 38 g/day for men [41]. Most Americans greatly under consume dietary fiber, and usual intake averages only 15 g/day [41]. The Shanghai Women’s study [42] reported that the highest quintile of dietary fiber intake was 16.3 g/day. Then increased consumption of fiber-rich foods may bring great benefits in type 2 diabetes prevention, especially in those at high risk. Several potential mechanisms may explain an inverse association between dietary fiber intake and risk of type 2 diabetes. Observational studies showed that high intake of dietary fiber may reduce the risk of overweight/obesity [43], which is an established risk factor for type 2 diabetes. Consumption of soluble fiber could delay gastric emptying and decrease absorption of macronutrients, resulting in lower postprandial blood glucose and insulin level [44]. However, our study found insoluble fiber not soluble fiber was inverse associated with risk of type 2 diabetes. Earlier study showed that an increased intake of total dietary fiber
Dietary fiber intake and risk of type 2 diabetes
was inversely associated with markers of insulin resistance [45]. And subjects consuming diets high in insoluble fiber may reduce diabetes risk through improving insulin resistance [46]. Our study had some important strength. All the original articles included used a prospective cohort study design, which greatly reduced the selection bias and recall bias. Many articles in this meta-analysis had a large sample and a long duration of follow-up which enhanced the power to detect a significant association and provided more reliable estimates. Moreover, we found a significant dose–response relation between total dietary fiber and cereal fiber intake and risk of type 2 diabetes, which were more precise. Our study also has several limitations. First, a meta-analysis is not able to address problems with confounding factors that could be inherent in the original studies. Although most articles included in this meta-analysis had adjusted for major potential confounders, including age, smoking, alcohol consumption, BMI, physical activity, and energy intake. However, only two studies adjusted for magnesium, which has been shown to decrease the incidence of type 2 diabetes [27]. In addition, residual or unknown confounding cannot be excluded as a potential explanation for the observed findings. Second, our results are likely to be affected by some degree of misclassification of exposure. Most of the original articles included in our meta-analysis used a validated food-frequency questionnaire, but only one reports updated the information on dietary fiber intake during follow-up [26]. Third, publication bias could also be of a concern. Although yet little evidence of publication bias was observed, it is noteworthy that these tests were based on a relatively small number of articles. In conclusion, this meta-analysis of prospective cohort studies provides evidence of a significant inverse association between dietary fiber and risk of type 2 diabetes. Our findings support current recommendations that consumption of at least 25 g/day total dietary fiber may prevent type 2 diabetes. Further studies elucidating mechanisms underlying the beneficial effects of dietary fiber intake for the prevention of type 2 diabetes are warranted. Acknowledgments
None.
Conflict of interest No conflict of interest existed for any of the authors.
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