A Lowly Digestible-Starch Diet after Weaning Enhances Exogenous Glucose Oxidation Rate in Female, but Not in Male, Mice

Abstract

Starches of low digestibility are associated with improved glucose metabolism. We hypothesise that a lowly digestible-starch diet (LDD) versus a highly digestible-starch diet (HDD) improves the capacity to oxidise starch, and that this is sex-dependent. Mice were fed a LDD or a HDD for 3 weeks directly after weaning. Body weight (BW), body composition (BC), and digestible energy intake (dEI) were determined weekly. At the end of the intervention period, whole-body energy expenditure (EE), respiratory exchange ratio (RER), hydrogen production, and the oxidation of an oral ¹³C-labelled starch bolus were measured by extended indirect calorimetry. Pancreatic amylase activity and total ¹³C hepatic enrichment were determined in females immediately before and 4 h after administration of the starch bolus. For both sexes, BW, BC, and basal EE and RER were not affected by the type of starch, but dEI and hydrogen production were increased by the LDD. Only in females, total carbohydrate oxidation and starch-derived glucose oxidation in response to the starch bolus were higher in LDD versus HDD mice; this was not accompanied by differences in amylase activity or hepatic partitioning of the ¹³C label. These results show that starch digestibility impacts glucose metabolism differently in females versus males.

Keywords: 13C-starch; C57BL mice; amylase; amylopectin; amylose; glucose oxidation; glycaemic index; indirect calorimetry.

Figure 1

Cumulative 24 h H₂ production on highly digestible-starch diet (HDD) or lowly digestible-starch diet (LDD). (a) Males (n = 5; PW 4), (b) females (n = 6; PW 3). Data are presented as mean and SD. Student’s t-test, * P < 0.05. HDD, highly digestible-starch diet; LDD, lowly digestible-starch diet; PW, post-weaning week.

Figure 2

Whole-body substrate oxidation after oral administration of a ¹³C-labelled starch bolus to HDD and LDD mice in PW 4. (a,d) respiratory exchange ratio (RER) evolution after administration of the starch bolus. (b,e) iAUC and (c,f) AUC of the RER response over 4 h from administration of the bolus. (a–c) Males (n = 5), (d–f) females (n = 6). Data are presented as mean and SD. Student’s t-test, * P < 0.05, *** P < 0.001. HDD, highly digestible-starch diet; iAUC, incremental area under the curve; LDD, lowly digestible-starch diet; PW, post-weaning week; RER, respiratory exchange ratio.

Figure 3

Glucose oxidation kinetics after oral administration of a ¹³C-labelled starch bolus to HDD and LDD mice in PW 4. (a,d) Instantaneous starch-derived glucose oxidation rate. (b,e) Total glucose oxidation rate. (c,f) Cumulative starch-derived glucose oxidation. (a–c) Males (n = 5), (d–f) females (n = 6). Data are presented as mean and SD. Bonferroni’s post hoc test for multiple comparisons, ** P < 0.01, *** P < 0.001. HDD, highly digestible-starch diet; LDD, lowly digestible-starch diet; PW, post-weaning week.

Figure 4

(a) Amylase levels, assayed as activity, per unit of small intestinal contents from HDD and LDD females in PW 4, without (t = 0 h; n = 3) and 4 h after (t = 4 h; n = 6) oral administration of a ¹³C-labelled starch bolus. (b) Total weight of small intestinal contents from females in panel (a); note 1 missing value in each group (t = 0 h) that failed to be recorded. (c) Estimated total amylase activity in the entirety of the small intestinal contents, based on data from panels (a) and (b). Data are presented as mean and SD. Student’s t-test. HDD, highly digestible-starch diet; LDD, lowly digestible-starch diet; PW, post-weaning week.

Figure 5

Total ¹³C enrichment in liver tissue from HDD and LDD females 4 h after oral administration of a ¹³C-labelled starch bolus in PW 4. Data (n = 6) is expressed relative to females that did not receive the ¹³C starch bolus (n = 3) and presented as mean and SD. Student’s t-test. DOB, delta over baseline; HDD, highly digestible-starch diet; LDD, lowly digestible-starch diet; PW, post-weaning week.