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The Journal of Nutrition

Recent Advances in Nutritional Sciences

Metabolic Effects of Dietary Fiber Consumption


and Prevention of Diabetes1
Martin O. Weickert* and Andreas F. H. Pfeiffer

Department of Clinical Nutrition, German Institute of Human Nutrition, Potsdam-Rehbruecke, Germany and Department of
Endocrinology, Diabetes, and Nutrition, Charité-University-Medicine-Berlin, Campus Benjamin Franklin, Berlin, Germany

Definition and types of DF


Abstract DF are highly complex substances that can be described as any
A high dietary fiber (DF) intake is emphasized in the recommendations nondigestible carbohydrates and lignins not degraded in the
of most diabetes and nutritional associations. It is accepted that vis-
upper gut (4). Commonly, DF are classified according to their
solubility in water, even though grading according to viscosity,
cous and gel-forming properties of soluble DF inhibit macronutrient
gel-forming capabilities, or fermentation rate by the gut micro-
absorption, reduce postprandial glucose response, and beneficially in- biota might be physiologically more relevant. Most DF is fer-
fluence certain blood lipids. Colonic fermentation of naturally available mented to some degree. However, fermentation rates of DF
high fiber foods can also be mainly attributed to soluble DF, whereas no widely vary, with soluble DF (i.e., pectin, inulin, and b-glucans)
difference between soluble and insoluble DF consumption on the and insoluble resistant starch and oligosaccharides tending to be
more readily fermented than cereal DF (i.e., cellulose and
regulation of body weight has been observed. However, in prospective
hemicelluloses) (5). Foods are assumed to be whole grains if all
cohort studies, it is primarily insoluble cereal DF and whole grains, and components of the kernel (i.e., bran, germ, and endosperm) are
not soluble DF, that is consistently associated with reduced diabetes present in their natural proportions. Whole grain food products
risk, suggesting that further, unknown mechanisms are likely to be generally contain some 12% of total (mainly insoluble cereal)
involved. Recent research indicates that DF consumption contributes DF, and there is a strong correlation between whole grain and
to a number of unexpected metabolic effects independent from
cereal DF intake (2). Some bran derived food products contain
up to 25% of DF. Importantly, definition of whole grain both in
changes in body weight, which include improvement of insulin sensi-
cohort studies and on labels of commercially available cereal
tivity, modulation of the secretion of certain gut hormones, and effects products typically does not require an intact kernel (3). In U.S.
on various metabolic and inflammatory markers that are associated cohorts, whole grain and bran products from corn and wheat are
with the metabolic syndrome. In this review, we briefly summarize the main sources of cereal DF. Main sources of soluble DF are
novel findings from recent interventions and prospective cohort fruits and vegetables (6) and, to a smaller extent, products from
oat and barley that are rich in both insoluble DF and soluble
studies. We discuss concepts and potential mechanisms that might
b-glucans. It is, however, important to state that most naturally
contribute to the further understanding of the involved processes. available high-fiber foods contain both soluble and insoluble
fiber in varying amounts (6).
Background
Consumption of soluble dietary fiber (DF)2 reduces postprandial DF and risk of diabetes in prospective cohort studies
glucose responses after carbohydrate-rich meals, as well as It is commonly assumed that beneficial effects of high fiber diets
lowering total and LDL cholesterol levels (1). These effects are [fiber intake .25 g/d in women and .38 g/d in men (7)] can
likely explained the viscous and/or gel-forming properties of mainly be attributed to viscous and/or gel-forming properties of
soluble DF, which thereby slow gastric emptying and macronu- soluble DF (1). Therefore, analyzing results from prospective
trient absorption from the gut. However, it is not soluble DF, but cohort studies separately for foods high in ‘‘active’’ soluble DF
mainly the consumption of insoluble cereal DF and whole and ‘‘inactive’’ insoluble DF should be expected to show stronger
grains, that is consistently associated with reduced risk of type 2 protective associations for soluble DF. However, this hypothesis
diabetes in large prospective cohort studies (2,3). A number of is not supported by the available data. A recent meta-analysis
recent studies give novel insights that might help establish a that included 328,212 subjects showed no association with
metabolic link between insoluble DF consumption and reduced reduced diabetes risk both for fruit [relative risk for extreme
diabetes risk. Potential candidates are improved insulin sensi- quintiles (RR) 0.96; 95% CI 0.88–1.04] and vegetable (RR 1.04;
tivity and the modulation of inflammatory markers, as well as 95% CI 0.94–1.15) DF intake (2). In contrast, a high intake of
direct and indirect influences on the gut microbiota (Fig. 1). cereal DF was significantly associated with markedly reduced
diabetes risk in most studies (RR 0.67; 95% CI 0.62–0.72) (2).
Pooled data for 6 prospective cohort studies including 286,125
1
Author disclosures: M. O. Weickert and A. F. H. Pfeiffer, no conflicts of interest. subjects indicate that a 2-serving-per-day increment in whole
2
Abbreviations used: DF, dietary fiber; GIP, glucose dependent insulinotropic grain consumption might remarkably reduce diabetes risk by
polypeptide; GPR, G protein-coupled receptors; LPS, lipopolysaccharide; RR,
relative risk for extreme quintiles; SCFA, short-chain fatty acids.
21% (3). Interestingly, associations for consumption of the outer
Manuscript received 15 October 2007. bran portion of the kernel, but not germ intake, were compa-
* To whom correspondence should be addressed. E-mail: m.weickert@dife.de. rable to those of whole grain intake (3).
0022-3166/08 $8.00 ª 2008 American Society for Nutrition. J. Nutr. 138: 439–442, 2008. 439
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urally high in DF and fiber supplements (7). Therefore, reduced
body weight in subjects consuming high DF diets is likely to
contribute to reduced diabetes risk, but it cannot explain the
observed stronger associations for insoluble DF.

DF and hormonal responses. DF consumption affects the


secretion of various gut hormones that may act as satiety factors
(8,16–19). However, in many of the experiments in humans, hor-
monal changes were not linked to acute feelings of satiety. A guar
gum DF supplement produced a heightened postprandial chole-
cystokinin response, but did not alter satiety ratings (16). Insoluble
wheat DF-induced changes of orexigenic ghrelin and anorexigenic
peptide YY (PYY) were not associated with acute changes in
hunger and satiety (8) but may have affected satiety upon the
consumption of a subsequent meal (8,20). Highly fermentable DF
increase glucagon-like peptide 1 levels and may play a role in
the regulation of postprandial satiety in diverse animal species.
However, in humans, no fiber-induced changes of circulating
glucagon-like peptide 1 levels have been observed (17,18,21), and
ingestion of a fermentable (pectin, b-glucan) vs. a nonfermentable
(methylcellulose) DF supplement was found to be less, rather than
more, satiating (9). Glucose dependent insulinotropic polypeptide
(GIP) is another incretin hormone that appears to be involved in
the regulation of fat metabolism. Effects of DF consumption on
circulating GIP yielded mixed results. Soluble DF reduced circu-
lating GIP in diabetic humans (19), probably because of reduced
FIGURE 1 Potential effects of DF consumption. Colonic fermenta- carbohydrate absorption, whereas insoluble cereal DF consump-
tion with the production of SCFA can be observed with most types of tion yielded accelerated responses of both biologically active GIP
DF to some extent, but it tends to be more pronounced with soluble (17) and insulin (17,22) in healthy subjects. In a cross-sectional
DF in naturally available foods. analysis, high intakes of cereal DF were positively associated with
plasma adiponectin after adjusting for lifestyle factors and dietary
glycemic load (23). Adiponectin may act as a peripheral starva-
A causal relationship can not be stated, and estimation of tion signal promoting the storage of triglycerides preferentially in
food intake on the basis of semiquantitative FFQ is a known adipose tissue (24). As a consequence, reduced triglyceride accu-
limitation (2). Moreover, even after statistical adjustment for mulation in the liver and in the skeletal muscle might convey
potentially confounding factors, residual confounding by addi- improved systemic insulin sensitivity (25). In summary, various
tional unmeasured or inaccurately measured factors can not be changes in circulating concentrations of gut and adipocyte
excluded. However, the consistency of the results clearly indi- derived hormones can be observed in humans that ingest a high
cates that the consumption of insoluble cereal DF could play an DF diet. However, no obvious mechanism can be derived ex-
important role in the prevention of diabetes. plaining stronger associations for insoluble DF with diabetes risk.

Potential mechanisms DF and insulin sensitivity. An increased intake of total DF was


DF, satiety, and body weight. Potential mechanisms that inversely associated with markers of insulin resistance in several
indicate DF consumption might alter diabetes risk include effects studies (26). Investigating different sorts of soluble and insoluble
on satiety and body weight. A number of studies showed in- DF in randomized controlled intervention studies yielded mixed
creased postmeal satiety or decreased subsequent hunger when results. Consumption of wheat bran for 3 mo did not change
subjects consumed high DF diets, both under conditions of fixed fasting glucose and glycated hemoglobin (HbA1c) levels in
energy intake and when energy intake was consumed ad libitum diabetic subjects (27). High DF rye bread enhanced insulin secre-
(7). However, other studies reported no significant effects (7– tion but did not appear to improve insulin sensitivity in post-
10). Not all studies (11) showed an inverse association between menopausal women, as estimated with the frequently sampled
postprandial glucose and insulin responses and satiety, and no intravenous-glucose-tolerance test (28). However, using a sec-
clear conclusion can be drawn that low vs. high glycemic index ond meal test design, improved markers of insulin resistance
meals are a key factor promoting satiety (12). have been reported after consumption of various other sorts of
Most (7), but not all (13), observational studies showed an insoluble DF (17,18,20,29). When measuring insulin sensitivity
inverse, sometimes dose-dependent (14) relationship between using euglycemic-hyperinsulinemic clamps, consumption of in-
DF consumption and body weight. Effects were moderate, with soluble DF increased whole body glucose disposal independent
individuals in the highest quintile vs. lowest quintile of DF of changes in body weight in both short-term and more pro-
consumption gaining 3.6 kg less over a 10-y period (14). Several longed studies (21,30,31). Insulin resistant subjects are more
(7), but not all (9,15), relatively short-term interventions further likely to eventually develop diabetes. Therefore, improved insu-
indicate that moderate reductions of body weight can be lin sensitivity could be a relevant factor contributing to reduced
achieved with high DF diets. diabetes risk in subjects consuming diets high in insoluble DF.
Generally, in human studies, no clear difference regarding
weight gain has been shown between soluble and insoluble DF DF and inflammation. Recent studies show reductions of inflam-
and fermentable and nonfermentable DF, or between foods nat- matory markers in subjects consuming high DF diets (32). Inter-
440 Weickert and Pfeiffer
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estingly, some sorts of DF have been reported to bind to specific cross-over study in healthy women (17), markers of insulin
receptors on immune cells, suggesting a direct immune–modulatory sensitivity in a second meal test were improved to a similar extent
effect (5). Other potentially involved mechanisms might include with all DF, independent of the rate of colonic fermentation (Fig. 2).
weight loss when consuming high DF diets, as well as antihyper- These experiments indicate that a dose-dependent relation between
glycemic effects and effects on lipid oxidation (32). Both a diet high fermentability of DF and improved markers of insulin sensitivity
in total DF and consumption of a soluble DF supplement signif- was unlikely, even though the limited accuracy of the available
icantly decreased levels of the inflammatory marker C-reactive pro- methods to estimate colonic fermentation rates in humans must
tein (33). Fermentation of soluble DF may also play a role due to be considered (4). Further, SCFA might stimulate adipogenesis
potential antiinflammatory properties of butyrate (32). However, through GPR43 (35), and colonization of germ-free (gnotobiotic)
reductions in inflammatory markers have been reported to be mice with a prominent saccharolytic member of the normal human
comparable with both insoluble DF and more readily fermentable gut microbiota, together with the dominant human methane
soluble DF (34). producing germ, resulted in markedly improved efficacy of colonic
fermentation, associated with increased de novo lipogenesis and
Colonic fermentation and gut bacteria. Short-chain fatty obesity in the host (36). However, it needs to be emphasized that
acids (SCFA) such as acetate, propionate, and butyrate are nutritional habits and physiological effects of DF intake in rodents
produced by bacterial fermentation of indigestible DF polysac- and humans largely differ, with rodents recovering energy from
charides in the colon (1), with the proportion of different SCFA coprophagia (4). In humans, SCFA account for ,10% of daily
not being fixed, depending on the substrate and eventually on energy intake (37).
the gut microflora. Commonly, increased production of SCFA is DF consumption might affect further factors linking the gut
assumed to be beneficial by reducing hepatic glucose output and microbiota with obesity and insulin resistance. Obese subjects
improving lipid homeostasis (32). Further, G protein-coupled have a different composition of the gut microbiota than lean
receptors (GPR)-41 and GPR43 function as direct targets of subjects, and changes toward the ‘‘lean microbiota’’ can be
SCFA. An interesting finding was that oral administration of the observed in obese subjects that lose weight [referenced in (36)].
GPR41 ligand propionate almost doubled plasma concentra- When transplanting the gut microbiota from obese mice or from
tions of anorexigenic leptin in mice, even though no effect on lean mice to germ-free mice, the recipients of the ‘‘obese microbes’’
food intake was detected (35). showed an increased gain of fat mass, even though energy intake
However, data not unequivocally indicate that fermentability of was comparable (36). Interestingly, a high DF diet (oligofructose)
DF per se is a key factor contributing to reduced diabetes risk. reduced gram-negative bacterial content and body weight, whereas
Consumption of low fermentable cereal DF (corn and wheat) show a high fat diet increased the proportion of a gram-negative
stronger associations with reduced diabetes risk than more readily bacterial lipopolysaccharides (LPS) containing microbiota in
fermentable soluble DF from fruit and vegetables (2,3). When humans [referenced in (38)]. Continuous subcutaneous infusion
investigating effects of weakly fermentable insoluble cereal DF of LPS for 4 wk increased weight gain, liver fat, inflammatory
and highly fermentable resistant starch in a randomized controlled markers, and markers of insulin resistance to a similar extent than

FIGURE 2 Effects of insoluble fiber on


postprandial glucose handling in a second
meal test. Postprandial serum insulin and
plasma glucose responses upon the inges-
tion of control white bread in a second meal
test, following the ingestion of 3 portions of
control white bread the previous day, or
white bread enriched with 31.5 g of the
insoluble fraction of nonfermentable wheat
DF, or white bread enriched with 31.8 g of
the insoluble fraction of moderately ferment-
able oat DF (n ¼ 14/group), or white bread
enriched with 31.2 g of highly fermentable
resistant starch (RS) (substudy, n ¼ 9/group).
Test breads were isoenergetic and macronu-
trient matched. Adapted from reference (17),
with permission.

Dietary fiber and risk of diabetes 441


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