Meal patterns, satiety, and food choice in a rat model of Roux-en-Y gastric bypass surgery

Abstract

Gastric bypass surgery efficiently and lastingly reduces excess body weight and reverses type 2 diabetes in obese patients. Although increased energy expenditure may also play a role, decreased energy intake is thought to be the main reason for weight loss, but the mechanisms involved are poorly understood. Therefore, the aim of this study was to characterize the changes in ingestive behavior in a rat model of Roux-en-Y gastric bypass surgery (RYGB). Obese (24% body fat compared with 18% in chow-fed controls), male Sprague-Dawley rats maintained for 15 wk before and 4 mo after RYGB or sham-surgery on a two-choice low-fat/high-fat diet, were subjected to a series of tests assessing energy intake, meal patterning, and food choice. Although sham-operated rats gained an additional 100 g body wt during the postoperative period, RYGB rats lost approximately 100 g. Intake of a nutritionally complete and palatable liquid diet (Ensure) was significantly reduced by approximately 50% during the first 2 wk after RYGB compared with sham surgery. Decreased intake was the result of greatly reduced meal size with only partial compensation by meal frequency, and a corresponding increase in the satiety ratio. Similar results were obtained with solid food (regular or high-fat chow) 6 wk after surgery. In 12- to 24-h two-choice liquid or solid diet paradigms with nutritionally complete low- and high-fat diets, RYGB rats preferred the low-fat choice (solid) or showed decreased acceptance for the high-fat choice (liquid), whereas sham-operated rats preferred the high-fat choices. A separate group of rats offered chow only before surgery completely avoided the solid high-fat diet in a choice paradigm. The results confirm anecdotal reports of "nibbling" behavior and fat avoidance in RYGB patients and provide a basis for more mechanistic studies in this rat model.

Fig. 1.

Changes in body weight and composition after Roux-en-Y gastric bypass surgery (RYGB) or sham surgery. A: body weight change of RYGB (n = 5–8) and sham-operated (n = 7) rats over the 150-day observation period. The use of different maintenance diets and behavioral testing paradigms is indicated on top. All rats were made obese on high fat during 16–20 wk and weighed ∼480 g before surgery. Body weights between RYGB and sham-operated rats were significantly different starting 5 days after surgery (data not shown) B and C: Body composition assessed before high-fat diet and before and after surgery using magnetic resonance relaxometry expressed in absolute and relative values. Bars that do not share the same letters are significantly (P < 0.05) different from each other, based on ANOVA followed by Bonferroni's multiple comparisons.

Fig. 2.

Food intake during the first 3 wk and water intake 5 wk after RYGB (n = 8) or sham surgery (n = 8). A: intake of complete liquid nutrient (Ensure) during first 10 days postsurgery. B: total calorie intake for weeks 2 and 3 postsurgery when offered a 3-choice diet consisting of Ensure, normal chow, and high-fat diet. C: Water intake measured on 5 consecutive days, 5 wk postsurgery, when on 2-choice diet. Water intake of lean control rats without any surgical intervention is shown for comparison. *P < 0.05.

Fig. 3.

Liquid meal patterns during the acute and chronic phases after RYGB or sham surgery. A and B: examples of typical 24-h meal records, 18 days after RYGB or sham-surgery, demonstrating the smaller but more frequent meals taken by RYGB rats. C: average meal size, meal frequency, meal duration, within-meal ingestion rate, intermeal interval, satiety ratio, and total intake during the acute (weeks 2–3) and chronic (weeks 18–20) phases after RYGB (filled bars) or sham surgery (open bars). Bars that do not share the same letters are significantly different from each other (P < 0.05), based on 2-way ANOVA.

Fig. 4.

Solid food intake with either powdered normal chow or high fat as sole diets 5–7 wk after RYGB or sham surgery. A: effect on energy intake when switching RYGB (n = 6) and sham-operated (n = 6) rats from 2-choice diet to chow (days 1–6) and from chow to high-fat diet (days 7–11). Gray shaded boxes indicate time covered by meal pattern analysis in Fig. 6. B: 22-h cumulative intake of powdered high-fat diet in RYGB (n = 6) and sham-operated (n = 5) rats, showing the relative hypophagia of RYGB rats during mainly the dark period as analyzed in Fig. 6. *P < 0.05, based on repeated-measure ANOVA followed by Bonferroni-adjusted multiple comparisons.

Fig. 5.

Solid meal patterns for powdered chow and high-fat diets, measured 5–7 wk after RYGB (n = 6) or sham surgery (n = 6). Average meal size, meal frequency, rate of eating, meal duration, intermeal interval, and satiety ratio for sham-operated obese rats (open bars) and RYGB (filled bars). Bars that do not share the same letters are significantly different from each other (P < 0.05), based on separate 1-way ANOVAs followed by Tukey's multiple-comparisons tests. #P < 0.05 compared with sham-operated rats on the same diet, based on repeated-measures ANOVA.

Fig. 6.

Food choice and fat acceptance of RYGB and sham-operated, obese and lean rats. A and B: gradual development of high-fat avoidance in RYGB rats. Total calorie intake from chow and high-fat diet in 2-choice paradigm, showing the gradual increase of intake from chow in RYGB rats (A) and the corresponding fat preference (B). C: decreased fat acceptance of RYGB rats in liquid 2-choice paradigm. D: total high-fat avoidance in lean rats subjected to RYGB surgery. Bars that do not share the same letters are significantly different from each other (P < 0.05), based on 2-way ANOVA. *P < 0.01 compared with sham rats, based on 1-way (presurgery) or 2-way (postsurgery) ANOVA.

Fig. 7.

Energy expenditure (EE) and respiratory exchange rate (RER) measured during 3 consecutive days with the CLAMS system, 10 wk after RYGB or sham surgery. A: EE expressed per total body weight. B: relationship between 24-h EE and lean body mass indicates similar EE/lean body mass. ANCOVA analysis revealed that there is a common slope. C and D: RER is significantly higher in RYGB rats (*P < 0.05), based on 1-way ANOVA, indicating increased capacity of carbohydrate oxidation.