Manipulation of starch bioaccessibility in wheat endosperm to regulate starch digestion, postprandial glycemia, insulinemia, and gut hormone responses: a randomized controlled trial in healthy ileostomy participants

Abstract

Background: Cereal crops, particularly wheat, are a major dietary source of starch, and the bioaccessibility of starch has implications for postprandial glycemia. The structure and properties of plant foods have been identified as critical factors in influencing nutrient bioaccessibility; however, the physical and biochemical disassembly of cereal food during digestion has not been widely studied.

Objectives: The aims of this study were to compare the effects of 2 porridge meals prepared from wheat endosperm with different degrees of starch bioaccessibility on postprandial metabolism (e.g., glycemia) and to gain insight into the structural and biochemical breakdown of the test meals during gastroileal transit.

Design: A randomized crossover trial in 9 healthy ileostomy participants was designed to compare the effects of 55 g starch, provided as coarse (2-mm particles) or smooth (<0.2-mm particles) wheat porridge, on postprandial changes in blood glucose, insulin, C-peptide, lipids, and gut hormones and on the resistant starch (RS) content of ileal effluent. Undigested food in the ileal output was examined microscopically to identify cell walls and encapsulated starch.

Results: Blood glucose, insulin, C-peptide, and glucose-dependent insulinotropic polypeptide concentrations were significantly lower (i.e., 33%, 43%, 40%, and 50% lower 120-min incremental AUC, respectively) after consumption of the coarse porridge than after the smooth porridge (P < 0.01). In vitro, starch digestion was slower in the coarse porridge than in the smooth porridge (33% less starch digested at 90 min, P < 0.05, paired t test). In vivo, the structural integrity of coarse particles (∼2 mm) of wheat endosperm was retained during gastroileal transit. Microscopic examination revealed a progressive loss of starch from the periphery toward the particle core. The structure of the test meal had no effect on the amount or pattern of RS output.

Conclusion: The structural integrity of wheat endosperm is largely retained during gastroileal digestion and has a primary role in influencing the rate of starch amylolysis and, consequently, postprandial metabolism. This trial was registered at isrctn.org as ISRCTN40517475.

Keywords: bioaccessibility; digestion; glycemia; ileostomy; postprandial; starch; structure.

Figures

FIGURE 1

Blood and effluent collection time points and meal times. Fasting blood samples for baseline measurements were collected at −15 min (glucose only) and, for all analytes, immediately before the test meal (0 min). Blood samples thereafter were collected at regular intervals up to 4 h, and ileal effluent was collected every 2 h up to 10 h. Overnight effluent samples (between 2200 and 1100 the next day) were collected at variable time points, at the participants’ convenience. Effluent samples were preserved in ethanol or by freezing at the time of collection to inhibit enzymatic and chemical deterioration of carbohydrates (e.g., starch).

FIGURE 2

Starch digestibility (A) and HI (B) of smooth and coarse porridge endosperm relative to pure starch assessed in vitro. Digestibility curves show percentage of hydrolyzable starch digested for smooth and coarse endosperm and a highly digestible reference (i.e., pure, gelatinized durum wheat starch). In these curves, each experimental point represents the mean value from analysis performed in triplicate with vertical error bars showing SEMs. Digestibility curves of smooth and coarse porridge were significantly different (paired t test for incremental AUC at 60 min, P < 0.001). HI is the percentage of hydrolyzable starch digested at 90 min, and was calculated with the use of the previously described logarithm of slope model (18). HI values were significantly different between smooth and coarse porridge (paired t test, P = 0.03). HI, hydrolysis index; REF, reference.

FIGURE 3

Postprandial changes in blood glucose (A), insulin (B), C-peptide (C), and GIP (D) concentrations after smooth and coarse porridge meals. Each meal provided 55.4 g of starch. Values are mean deviations from baseline ± SEMs (n = 9 for glucose, insulin, and C-peptide and n = 8 for GIP) and were analyzed by ANOVA with meal and time as factors. Meal, time, and meal × time were significant for glucose (P = 0.038, <0.001, and <0.001), insulin (P = 0.046, <0.001, and 0.035), C-peptide (P = 0.018, <0.001, and <0.001), and GIP (P = 0.024, <0.001, and <0.001) responses, respectively. Time points at which values differed significantly, *P < 0.05, **P < 0.01, and ***P < 0.001 (paired t test with Bonferroni corrections). Insets show the iAUC between 0 and 120 min. GIP, glucose-dependent insulinotropic polypeptide; iAUC, incremental AUC.

FIGURE 4

Postprandial changes in serum TAG (A) and NEFA (B) concentrations after smooth and coarse porridge meals. Each meal provided 1.56 g fat. Values are mean deviations from baseline ± SEMs (n = 9) and were analyzed by ANOVA with meal and time as factors. Time effects were highly significant for both TAGs (P = 0.004) and NEFAs (P < 0.001), but meal and meal × time were not significant (P = 0.074 and 0.100 for TAGs and P = 0.969 and 0.249 for NEFAs). NEFA, nonesterified fatty acid; TAG, triacylglycerol.

FIGURE 5

Sections of wheat endosperm particles from coarse porridge at various stages of digestion. All panels are light microscopic micrographs in which the starch was stained with 2.5% (wt:vol) Lugol’s iodine. Starch-filled wheat endosperm tissue from the cooked coarse porridge before digestion (A). Low-magnification view of a typical 2-mm wheat particle recovered in ileal effluent after 4 h (B). The staining pattern suggests a progressive digestion of starch from the particle periphery toward the core. A higher-magnification view than in panel B shows the digested edge of a particle collected from effluent after 4 h (C). Starch in the outermost cell layers (toward the right) has been digested, leaving empty cells. Typical particle remnant recovered in ileal effluent during the night (22-h gut residence time) (D). In the overnight samples, remnants of endosperm tissue were observed only when attached to adjacent outer tissue layers (aleurone, pericarp, and testa), and most of the starch had been digested.