Microstructural changes in human ingestive behavior after Roux-en-Y gastric bypass during liquid meals

Abstract

BACKGROUNDRoux-en-Y gastric bypass (RYGB) decreases energy intake and is, therefore, an effective treatment of obesity. The behavioral bases of the decreased calorie intake remain to be elucidated. We applied the methodology of microstructural analysis of meal intake to establish the behavioral features of ingestion in an effort to discern the various controls of feeding as a function of RYGB.METHODSThe ingestive microstructure of a standardized liquid meal in a cohort of 11 RYGB patients, in 10 patients with obesity, and in 10 healthy-weight adults was prospectively assessed from baseline to 1 year with a custom-designed drinkometer. Statistics were performed on log-transformed ratios of change from baseline so that each participant served as their own control, and proportional increases and decreases were numerically symmetrical. Data-driven (3 seconds) and additional burst pause criteria (1 and 5 seconds) were used.RESULTSAt baseline, the mean meal size (909.2 versus 557.6 kCal), burst size (28.8 versus 17.6 mL), and meal duration (433 versus 381 seconds) differed between RYGB patients and healthy-weight controls, whereas suck volume (5.2 versus 4.6 mL) and number of bursts (19.7 versus 20.1) were comparable. At 1 year, the ingestive differences between the RYGB and healthy-weight groups disappeared due to significantly decreased burst size (P = 0.008) and meal duration (P = 0.034) after RYGB. The first-minute intake also decreased after RYGB (P = 0.022).CONCLUSIONRYGB induced dynamic changes in ingestive behavior over the first postoperative year. While the eating pattern of controls remained stable, RYGB patients reduced their meal size by decreasing burst size and meal duration, suggesting that increased postingestive sensibility may mediate postbariatric ingestive behavior.TRIAL REGISTRATIONNCT03747445; https://ichgcp.net/clinical-trials-registry/NCT03747445.FUNDINGThis work was supported by the University of Zurich, the Swiss National Fund (32003B_182309), and the Olga Mayenfisch Foundation. Bálint File was supported by the Hungarian Brain Research Program Grant (grant no. 2017-1.2.1-NKP-2017-00002).

Keywords: Behavior; Endocrinology; Metabolism; Obesity; Surgery.

Conflict of interest statement

Conflict of interest: RES is employed by DSM Nutritional Products. MB reports personal fees from Johnson & Johnson and Medtronic, outside the submitted work. The Resource 2.0+Fibre nutritional products were provided free of charge by Nestlé Suisse S.A.

Figures

Figure 1. Study flowchart.

RYGB, Roux-en-Y gastric bypass.

Figure 2. Change in body mass index.

Change in body mass index over time expressed as group mean (bold lines) and individual curves (pale lines). Blue, Roux-en-Y gastric bypass group; red, normal-weight control group; green, obese control group. Post hoc test: RYGB baseline versus RYGB 1-year difference: –16.35 (95% CI, –23.15 to –9.5), Padj < 0.0001.

Figure 3. Probability density function (PDF) of loge transformed ISI to identify the optimal burst pause criterion.

(A) All recorded drinkometer sessions in RYGB patients, normal-weight controls and obese controls. (B) RYGB group and normal-weight controls only. Gaussian mixture models aim to distinguish 2 normally distributed populations: the shorter ones represent the ISI, whereas the longer ones represent the IBI. The optimal burst pause criterion between ISIs and IBIs is where the 2 Gaussian curves meet, which was observed at the following: (A) 0.122 loge units, representing 1.13 seconds; (B) 1.631 loge units, representing 5.1 seconds.

Figure 4. Graphical illustration of different drinking sessions of a single representative participant from each group at different time points.

(A) Normal-weight control baseline. (B) Normal-weight control 12 months. (C) Obese control baseline. (D) Obese control 3 months. (E) Preoperative RYGB. (F) One week postoperative. (G) Three months postoperative. (H) Twelve months postoperative. Triangles show the peak of each suck.

Figure 5. Changes in overall ingestive parameters over time expressed as proportion of baseline.

Group means, bold lines; individual curves, pale lines. (A) Calorie intake (1 mL of the stimulus contained 2 kCal), post hoc test: RYGB 1 year versus normal-weight control 1 year difference: –0.37 (95% CI, –0.63 to –0.14), Padj = 0.0003. (B) Meal duration, post hoc test: RYGB 1-month versus normal-weight control 3-months difference: 0.33 (95% CI, 0.01–0.65), Padj = 0.036. (C) Average drinking speed, post hoc test: RYGB 3-month versus normal-weight control 1-year difference: 0.34 (95% CI, 0.07–0.62), Padj = 0.007. (D) Total number of sucks, post hoc test: RYGB 1-year versus normal-weight control 1-year difference: –0.3 (95% CI, –0.56–0.06), Padj = 0.008. Blue, Roux-en-Y gastric bypass group; red, normal-weight control group; green, obese control group.

Figure 6. Changes in microstructural parameters over time expressed as proportion of baseline.

Group means, bold lines; individual curves, pale lines; burst pause criterion, 3 seconds. (A) Suck volume, post hoc test: nonsignificant. (B) Mean burst size, post hoc test: RYGB 3-month versus normal-weight control 1-year difference: 0.51 (95% CI, 0.05–0.96), Padj = 0.02. (C) Total number of bursts, post hoc test: nonsignificant. (D) IBI, post hoc test: nonsignificant. Blue, Roux-en-Y gastric bypass group; red, normal-weight control group; green, obese control group.

Figure 7. Mean burst size within the first 20 consecutive bursts within a meal according to subgroups.

Normal-weight control group (n = 39) (red); obese control group (n = 29) (green); RYGB group pre-RYGB (n = 11); and 1 week (n = 8)/1 month (n = 10)/3 months (n = 10)/6 months (n = 10)/1 year (n= 10) after RYGB (shades of blue) at PC of 3 seconds. The proportion of participants per subgroups and per consecutive burst number is shown in the lower part of the plot.

Figure 8. Changes in meal intake between the first and second half of bursts within each ingestive session.

Blue, Roux-en-Y gastric bypass group; red, normal-weight control group; green, obese control group.

Figure 9. Changes in microstructural parameters at the beginning of the meal expressed as proportion of baseline.

Group means, bold lines; individual curves, pale lines. (A) Size of the first burst (PC = 3 seconds), post hoc test: RYGB 1-year versus normal-weight control 3-month difference: –1.14 (95% CI, -2.24 to –0.04), Padj = 0.04. (B) Intake in the first 15 seconds. (C) Intake in the first 60 seconds, post hoc test: RYGB 1-month versus normal-weight control 3-month difference: 0.34 (95% CI, 0.04–0.64) Padj = 0.02. (D) Number of sucks within the first minute, post hoc test: RYGB 1-month versus normal-weight control 1-year difference: 0.24 (95% CI, 0.002–0.466), Padj = 0.046. Blue, Roux-en-Y gastric bypass group; red, normal-weight control group; green, obese control group.

Figure 10. Self-reported periingestive feelings, expressed as absolute values.

Group means, bold lines; individual curves, pale lines. (A) Premeal hunger. (B) Premeal thirst. (C) Liking of the stimulus. (D) Nausea 30 minutes after the meal session. Blue, Roux-en-Y gastric bypass group; red, normal-weight control group; green, obese control group; VAS, visual analogue scale (100 mm).

Figure 11. Oral contrast material swallow series in a patient after Roux-en-Y gastric bypass.

(A) Baseline: oral cavity is filled. (B) At 4 seconds: contrast present in distal esophagus. (C) At 10 seconds: contrast fills the gastric pouch. (D) At 12 seconds: contrast reaches the alimentary limb. (E) At 45 seconds: contrast present in the common channel.