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Surgical Endoscopy

Published in:

01-04-2012

Gastric bypass surgery restores meal stimulation of the anorexigenic gut hormones glucagon-like peptide-1 and peptide YY independently of caloric restriction

Authors: Sarah Evans, Zehra Pamuklar, Jonathan Rosko, Patrick Mahaney, Ning Jiang, Chan Park, Alfonso Torquati

Published in: Surgical Endoscopy | Issue 4/2012

Abstract

Background

The effects of gastric bypass surgery on the secretion of the anorexigenic gut-derived hormones glucagon-like peptide-1 (GLP-1) and peptide YY (PYY), independent of caloric restriction and due to different dietary macronutrients, is not well characterized. This study examines the effects of a mixed-nutrient or high-fat liquid meal on the postprandial stimulation of GLP-1 and PYY following gastric bypass or equivalent hypocaloric diet.

Methods

Total PYY and active GLP-1 were measured fasting and at multiple points after standardized mixed-nutrient and high-fat liquid meals in two matched groups of obese subjects. The meal stimulation tests were performed before and 14.6 ± 3.3 days after gastric bypass (GBP, n = 10) and before and after a 7-day hypocaloric liquid diet matching the post-GBP diet (control, n = 10).

Results

Mixed-nutrient and high-fat postprandial GLP-1 levels increased following GBP (mixed-nutrient peak: 85.0 ± 28.6–323 ± 51 pg/ml, P < 0.01; high-fat peak: 81.8 ± 9.6–278 ± 49 pg/ml, P < 0.01), but not after diet (mixed-nutrient peak: 104.4 ± 9.4–114.9 ± 15.8 pg/ml, P = NS; high-fat peak: 118.1 ± 16.4–104.4 ± 10.8 pg/ml, P = NS). The postprandial PYY response also increased after GBP but not diet, though the increase in peak PYY did not reach statistical significance (GBP mixed-nutrient peak: 134.8 ± 26.0–220.7 ± 52.9 pg/ml, P = 0.09; GBP high-fat peak: 142.1 ± 34.6–197.9 ± 12.7 pg/ml, P = 0.07; diet mixed-nutrient peak: 99.8 ± 8.0–101.1 ± 13.3 pg/ml, P = NS; diet high-fat peak: 105.0 ± 8.8–103.1 ± 11.8 pg/ml, P = NS). The postprandial GLP-1 response was not affected by the macronutrient content of the meal. However, following GBP the mixed-nutrient PYY total area under the curve (AUC_0–120) was significantly greater than the high-fat PYY AUC_0–120 (22,081 ± 5,662 pg/ml min vs. 18,711 ± 1,811 pg/ml min, P = 0.04).

Conclusions

Following GBP there is an increase in the postprandial stimulation of PYY and GLP-1 that is independent of caloric restriction. The phenomenon of “bariatric surgery-induced anorexia” may be linked to the increased levels after GBP.

Sturm R (2007) Increases in morbid obesity in the USA: 2000–2005. Public Health 121:492–496PubMedCrossRef

Brolin RE (1996) Update: NIH consensus conference. Gastrointestinal surgery for severe obesity. Nutrition 12:403–404PubMedCrossRef

Buchwald H, Avidor Y, Braunwald E, Jensen MD, Pories W, Fahrbach K, Schoelles K (2004) Bariatric surgery: a systematic review and meta-analysis. JAMA 292:1724–1737PubMedCrossRef

Doucet E (2008) Gastrointestinal peptides after bariatric surgery and appetite control: are they in tuning? Curr Opin Clin Nutr Metab Care 11:645–650PubMedCrossRef

Jayasena CN, Bloom SR (2008) Role of gut hormones in obesity. Endocrinol Metab Clin North Am 37(3): 769–787, xi

Frezza EE, Wachtel MS, Chiriva-Internati M (2007) The multiple faces of glucagon-like peptide-1–obesity, appetite, and stress: what is next? A review. Dig Dis Sci 52:643–649PubMedCrossRef

Karhunen LJ, Juvonen KR, Huotari A, Purhonen AK, Herzig KH (2008) Effect of protein, fat, carbohydrate and fibre on gastrointestinal peptide release in humans. Regul Pept 149:70–78PubMedCrossRef

Batterham RL, Cohen MA, Ellis SM, Le Roux CW, Withers DJ, Frost GS, Ghatei MA, Bloom SR (2003) Inhibition of food intake in obese subjects by peptide YY3–36. N Engl J Med 349:941–948PubMedCrossRef

le Roux CW, Batterham RL, Aylwin SJ, Patterson M, Borg CM, Wynne KJ, Kent A, Vincent RP, Gardiner J, Ghatei MA, Bloom SR (2006) Attenuated peptide YY release in obese subjects is associated with reduced satiety. Endocrinology 147:3–8PubMedCrossRef

10.

Carr RD, Larsen MO, Jelic K, Lindgren O, Vikman J, Holst JJ, Deacon CF, Ahren B (2010) Secretion and dipeptidyl peptidase-4-mediated metabolism of incretin hormones after a mixed meal or glucose ingestion in obese compared to lean, nondiabetic men. J Clin Endocrinol Metab 95:872–878PubMedCrossRef

11.

Verdich C, Toubro S, Buemann B, Lysgard Madsen J, Juul Holst J, Astrup A (2001) The role of postprandial releases of insulin and incretin hormones in meal-induced satiety–effect of obesity and weight reduction. Int J Obes Relat Metab Disord 25:1206–1214PubMedCrossRef

12.

le Roux CW, Aylwin SJ, Batterham RL, Borg CM, Coyle F, Prasad V, Shurey S, Ghatei MA, Patel AG, Bloom SR (2006) Gut hormone profiles following bariatric surgery favor an anorectic state, facilitate weight loss, and improve metabolic parameters. Ann Surg 243:108–114PubMedCrossRef

13.

Neary NM, Small CJ, Druce MR, Park AJ, Ellis SM, Semjonous NM, Dakin CL, Filipsson K, Wang F, Kent AS, Frost GS, Ghatei MA, Bloom SR (2005) Peptide YY3–36 and glucagon-like peptide-17–36 inhibit food intake additively. Endocrinology 146:5120–5127PubMedCrossRef

14.

Holdstock C, Zethelius B, Sundbom M, Karlsson FA, Eden Engstrom B (2008) Postprandial changes in gut regulatory peptides in gastric bypass patients. Int J Obes (Lond) 32:1640–1646CrossRef

15.

Karamanakos SN, Vagenas K, Kalfarentzos F, Alexandrides TK (2008) Weight loss, appetite suppression, and changes in fasting and postprandial ghrelin and peptide-YY levels after Roux-en-Y gastric bypass and sleeve gastrectomy: a prospective, double blind study. Ann Surg 247:401–407PubMedCrossRef

16.

Korner J, Bessler M, Inabnet W, Taveras C, Holst JJ (2007) Exaggerated glucagon-like peptide-1 and blunted glucose-dependent insulinotropic peptide secretion are associated with Roux-en-Y gastric bypass but not adjustable gastric banding. Surg Obes Relat Dis 3:597–601PubMedCrossRef

17.

le Roux CW, Welbourn R, Werling M, Osborne A, Kokkinos A, Laurenius A, Lonroth H, Fandriks L, Ghatei MA, Bloom SR, Olbers T (2007) Gut hormones as mediators of appetite and weight loss after Roux-en-Y gastric bypass. Ann Surg 246:780–785PubMedCrossRef

18.

Morinigo R, Moize V, Musri M, Lacy AM, Navarro S, Marin JL, Delgado S, Casamitjana R, Vidal J (2006) Glucagon-like peptide-1, peptide YY, hunger, and satiety after gastric bypass surgery in morbidly obese subjects. J Clin Endocrinol Metab 91:1735–1740PubMedCrossRef

19.

Adrian TE, Ferri GL, Bacarese-Hamilton AJ, Fuessl HS, Polak JM, Bloom SR (1985) Human distribution and release of a putative new gut hormone, peptide YY. Gastroenterology 89:1070–1077PubMed

20.

Batterham RL, Heffron H, Kapoor S, Chivers JE, Chandarana K, Herzog H, Le Roux CW, Thomas EL, Bell JD, Withers DJ (2006) Critical role for peptide YY in protein-mediated satiation and body-weight regulation. Cell Metab 4:223–233PubMedCrossRef

21.

Beckman LM, Beckman TR, Earthman CP (2010) Changes in gastrointestinal hormones and leptin after Roux-en-Y gastric bypass procedure: a review. J Am Diet Assoc 110:571–584PubMedCrossRef

22.

Essah PA, Levy JR, Sistrun SN, Kelly SM, Nestler JE (2007) Effect of macronutrient composition on postprandial peptide YY levels. J Clin Endocrinol Metab 92:4052–4055PubMedCrossRef

23.

Feinle C, Chapman IM, Wishart J, Horowitz M (2002) Plasma glucagon-like peptide-1 (GLP-1) responses to duodenal fat and glucose infusions in lean and obese men. Peptides 23:1491–1495PubMedCrossRef

24.

Helou N, Obeid O, Azar ST, Hwalla N (2008) Variation of postprandial PYY 3–36 response following ingestion of differing macronutrient meals in obese females. Ann Nutr Metab 52:188–195PubMedCrossRef

25.

Flint A, Raben A, Blundell JE, Astrup A (2000) Reproducibility, power and validity of visual analogue scales in assessment of appetite sensations in single test meal studies. Int J Obes Relat Metab Disord 24:38–48PubMedCrossRef

26.

Vidal J, Nicolau J, Romero F, Casamitjana R, Momblan D, Conget I, Morinigo R, Lacy AM (2009) Long-term effects of Roux-en-Y gastric bypass surgery on plasma glucagon-like peptide-1 and islet function in morbidly obese subjects. J Clin Endocrinol Metab 94:884–891PubMedCrossRef

27.

Valderas JP, Irribarra V, Boza C, de la Cruz R, Liberona Y, Acosta AM, Yolito M, Maiz A (2010) Medical and surgical treatments for obesity have opposite effects on peptide YY and appetite: a prospective study controlled for weight loss. J Clin Endocrinol Metab 95:1069–1075PubMedCrossRef

28.

Olivan B, Teixeira J, Bose M, Bawa B, Chang T, Summe H, Lee H, Laferrere B (2009) Effect of weight loss by diet or gastric bypass surgery on peptide YY3–36 levels. Ann Surg 249:948–953PubMedCrossRef

29.

Laferrere B, Teixeira J, McGinty J, Tran H, Egger JR, Colarusso A, Kovack B, Bawa B, Koshy N, Lee H, Yapp K, Olivan B (2008) Effect of weight loss by gastric bypass surgery versus hypocaloric diet on glucose and incretin levels in patients with type 2 diabetes. J Clin Endocrinol Metab 93:2479–2485PubMedCrossRef

30.

Campos GM, Rabl C, Peeva S, Ciovica R, Rao M, Schwarz JM, Havel P, Schambelan M, Mulligan K (2010) Improvement in peripheral glucose uptake after gastric bypass surgery is observed only after substantial weight loss has occurred and correlates with the magnitude of weight lost. J Gastrointest Surg 14:15–23PubMedCrossRef

31.

Pfluger PT, Kampe J, Castaneda TR, Vahl T, D’Alessio DA, Kruthaupt T, Benoit SC, Cuntz U, Rochlitz HJ, Moehlig M, Pfeiffer AF, Koebnick C, Weickert MO, Otto B, Spranger J, Tschop MH (2007) Effect of human body weight changes on circulating levels of peptide YY and peptide YY3–36. J Clin Endocrinol Metab 92:583–588PubMedCrossRef

32.

Adam TC, Jocken J, Westerterp-Plantenga MS (2005) Decreased glucagon-like peptide 1 release after weight loss in overweight/obese subjects. Obes Res 13:710–716PubMedCrossRef

Title: Gastric bypass surgery restores meal stimulation of the anorexigenic gut hormones glucagon-like peptide-1 and peptide YY independently of caloric restriction
Authors: Sarah Evans
Zehra Pamuklar
Jonathan Rosko
Patrick Mahaney
Ning Jiang
Chan Park
Alfonso Torquati
Publication date: 01-04-2012
Publisher: Springer-Verlag
Published in: Surgical Endoscopy / Issue 4/2012
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI: https://doi.org/10.1007/s00464-011-2004-7

At a glance: The STEP trials

Springer Medicine

Gastric bypass surgery restores meal stimulation of the anorexigenic gut hormones glucagon-like peptide-1 and peptide YY independently of caloric restriction

Abstract

Background

Methods

Results

Conclusions

At a glance: The STEP trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

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