Differential effects of laparoscopic sleeve gastrectomy and laparoscopic gastric bypass on appetite, circulating acyl-ghrelin, peptide YY3-36 and active GLP-1 levels in non-diabetic humans

Abstract

Laparoscopic Roux-en-Y gastric bypass (LRYGBP) reduces appetite and induces significant and sustainable weight loss. Circulating gut hormones changes engendered by LRYGBP are implicated in mediating these beneficial effects. Laparoscopic sleeve gastrectomy (LSG) is advocated as an alternative to LRYGBP, with comparable short-term weight loss and metabolic outcomes. LRYGBP and LSG are anatomically distinct procedures causing differential entero-endocrine cell nutrient exposure and thus potentially different gut hormone changes. Studies reporting the comparative effects of LRYGBP and LSG on appetite and circulating gut hormones are controversial, with no data to date on the effects of LSG on circulating peptide YY3-36 (PYY3-36) levels, the specific PYY anorectic isoform. In this study, we prospectively investigated appetite and gut hormone changes in response to LRYGBP and LSG in adiposity-matched non-diabetic patients. Anthropometric indices, leptin, fasted and nutrient-stimulated acyl-ghrelin, active glucagon-like peptide-1 (GLP-1), PYY3-36 levels and appetite were determined pre-operatively and at 6 and 12 weeks post-operatively in obese, non-diabetic females, with ten undergoing LRYGBP and eight adiposity-matched females undergoing LSG. LRYGBP and LSG comparably reduced adiposity. LSG decreased fasting and post-prandial plasma acyl-ghrelin compared to pre-surgery and to LRYGBP. Nutrient-stimulated PYY3-36 and active GLP-1 concentrations increased post-operatively in both groups. However, LRYGBP induced greater, more sustained PYY3-36 and active GLP-1 increments compared to LSG. LRYGBP suppressed fasting hunger compared to LSG. A similar increase in post-prandial fullness was observed post-surgery following both procedures. LRYGBP and LSG produced comparable enhanced satiety and weight loss. However, LSG and LRYGBP differentially altered gut hormone profiles.

Fig. 1

Fasting and nutrient-stimulated appetite, gut hormones, glucose and insulin for the LRYGBP and LSG groups pre-operatively. (A) Temporal hunger visual analogue scales (VAS) ratings for the LRYGBP (red, filled squares) and LSG (blue, filled circles). (B) Temporal fullness VAS for the LRYGBP (red, filled squares) and LSG (blue, filled circles) groups. (C) Plasma acyl-ghrelin temporal profile for the LRYGBP (red, filled squares) and LSG (blue, filled circles) groups. (D) Plasma PYY3-36 temporal profile for the LRYGBP (red, filled squares) and LSG (blue, filled circles) groups. (E) Plasma active GLP-1 temporal profile for the LRYGBP (red, filled squares) and LSG (blue, filled circles) groups. (F) Plasma glucose temporal profile for the LRYGBP (red, filled squares) and LSG (blue, filled circles) groups. (G) Plasma insulin temporal profile for the LRYGBP (red, filled squares) and LSG (blue, filled circles) groups. Results are expressed as mean ± SEM

Fig. 2

The effects of LRYGBP and LSG on plasma fasting, meal-stimulated acyl-ghrelin and acyl-ghrelinAUC_0–180. Plasma acyl-ghrelin temporal profile in response to the test-meal for LRYGBP (a) and LSG (b) groups at pre-surgery (black, solid squares), and at 6w and 12w post-operatively (red, solid circles and green, solid triangles, respectively). c Acyl-ghrelinAUC_0–180 for LRYGBP (black, solid columns) and LSG groups (grey, solid columns) at pre-surgery and at 6w and 12w post-operatively. Results are expressed as mean ± SEM. *p < 0.05, within-group at 6w post-operatively compared to pre-surgery; ^† p < 0.05, within-group comparisons at 12w post-operatively versus pre-surgery; ^‡ p < 0.05, within-group 6w versus 12w comparison. The p values at the right upper corner of c indicate one-way ANOVA within-group analysis. Within-group Bonferroni post hoc and between-group t test significance is indicated over the corresponding bars

Fig. 3

The effects of LRYGBP and LSG on fasting, meal-stimulated plasma concentrations and area-under-the curve (AUC_0–180) for PYY_3–36 and active GLP-1. Plasma PYY_3-36 temporal profile in response to the test-meal for LRYGBP (a) and LSG (b) groups at pre-surgery (black, solid squares) and at 6w and 12w post-operatively (red, solid circles and green, solid triangles, respectively). Plasma active GLP-1 temporal profile in response to the test-meal for LRYGBP (c) and LSG (d) groups at pre-surgery (black, solid squares) and at 6w and 12w post-operatively (red, solid circles and green, solid triangles, respectively). PYY_3-36AUC_0-180 (e) and active GLP-1AUC_0-180 (f) for LRYGBP (black, solid columns) and LSG groups (grey, solid columns) at pre-surgery and at 6w and 12w post-operatively. Results are expressed as mean ± SEM. *p < 0.05, **p < 0.01 and ***p < 0.001 within-group at 6w post-operatively compared to pre-surgery. ^† p < 0.05, ^†† p < 0.01 and ^††† p < 0.001 for within-group comparisons at 12w post-operatively versus pre-surgery. The p values at the right upper corner of e and f indicate one-way ANOVA within-group analysis. Within-group Bonferroni post hoc and between-group t test significance is indicated over the corresponding bars

Fig. 4

The effects of LRYGBP and LSG on fasting, meal-stimulated and area-under the curve (AUC_0–180) for subjective hunger and fullness VAS ratings. Hunger VAS temporal profile in response to the test-meal for LRYGBP (a) and LSG (b) groups at pre-surgery (black, solid squares), and at 6w and 12w post-operatively (red, solid circles and green, solid triangles, respectively). Fullness VAS temporal profile in response to the test-meal for LRYGBP (c) and LSG (d) groups at pre-surgery (black, solid squares) and at 6w and 12w post-operatively (red, solid circles and green, solid triangles, respectively). HungerAUC_0-180 (e) and fullnessAUC_0-180 (f) for LRYGBP (black, solid columns) and LSG groups (grey, solid columns) at pre-surgery and at 6w and 12w post-operatively. Results are expressed as mean ± sem. *p < 0.05, **p < 0.01 and ***p < 0.001 within-group at 6w post-operatively compared to pre-surgery. ^† p < 0.05, ^†† p < 0.01 and ^††† p < 0.001 for within-group comparisons at 12w post-operatively versus pre-surgery. The p values at the right upper corner e and f indicate one-way ANOVA within-group analysis. Within-group Bonferroni post hoc and between-group t test significance is indicated over the corresponding bars