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Published in: Obesity Surgery 2/2018

01-02-2018 | Original Contributions

Glucagon-Like Peptides 1 and 2 Are Involved in Satiety Modulation After Modified Biliopancreatic Diversion: Results of a Pilot Study

Authors: Everton Cazzo, José Carlos Pareja, Elinton Adami Chaim, Cláudio Saddy Rodrigues Coy, Daniéla Oliveira Magro

Published in: Obesity Surgery | Issue 2/2018

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Abstract

Background

This paper aimed to evaluate the influence of modified biliopancreatic diversion (BPD) on the levels of GLP-1 and GLP-2 and correlate them with satiety regulation.

Methods

This is a pilot prospective cohort study that evaluated six mildly obese individuals with type 2 diabetes mellitus, which underwent modified BPD and were followed-up for 12 months. Levels of GLP-1 and GLP-2 after a standard meal tolerance test were determined and correlated with satiety scores obtained by means of a visual analogue scale (VAS).

Results

There were significant changes in BMI (33 ± 2.2 versus 26.3 ± 2.2 kg/m2; p < 0.001), HbA1c (7.9 ± 1.6 versus 5.8 ± 1.2%; p = 0.026), total cholesterol (172.3 ± 11.1 versus 134.7 ± 16.1 mg/dL; p < 0.001), LDL-c (103.3 ± 13 versus 64.6 ± 12.2 mg/dL; p < 0.001), and postprandial GLP-2 (972.7 ± 326.2 versus 1993.2 ± 1024.7; p = 0. 044). None of the scores obtained in the VAS significantly changed after surgery. After surgery, there were significant correlations of VAS scores and GLP-1 levels in question 01 (“how hungry do you feel?”; R = −0.928; p = .008) and GLP-2 levels in questions 02 (“how full do you feel?” R = 0.943; p = 0.005) and 04 (“how much do you think you can eat now? R = −0.829; p = 0.042).

Conclusions

Modified BPD does not lead to significant changes in satiety evaluated by the VAS; different aspects of satiety regulation are correlated with the postprandial levels of GLP-1 (hunger feeling) and GLP-2 (satiation feeling and desire to eat) 1 year after modified BPD, signaling a specific postoperative gut hormone-related modulation of appetite.
Literature
1.
go back to reference Buchwald H, Avidor Y, Braunwald E, et al. Bariatric surgery: a systematic review and meta-analysis. JAMA. 2004;292(14):1724–37.CrossRefPubMed Buchwald H, Avidor Y, Braunwald E, et al. Bariatric surgery: a systematic review and meta-analysis. JAMA. 2004;292(14):1724–37.CrossRefPubMed
2.
go back to reference Buchwald H, Estok R, Fahrbach K, et al. Weight and type 2 diabetes after bariatric surgery: systematic review and meta-analysis. Am J Med. 2009;122(3):248–56.CrossRefPubMed Buchwald H, Estok R, Fahrbach K, et al. Weight and type 2 diabetes after bariatric surgery: systematic review and meta-analysis. Am J Med. 2009;122(3):248–56.CrossRefPubMed
3.
go back to reference Scopinaro N, Adami GF, Bruzzi P, et al. Prediction of diabetes remission at long term following biliopancreatic diversion. Obes Surg. 2017; doi:10.1007/s11695-017-2555-3. [Epub ahead of print] Scopinaro N, Adami GF, Bruzzi P, et al. Prediction of diabetes remission at long term following biliopancreatic diversion. Obes Surg. 2017; doi:10.​1007/​s11695-017-2555-3. [Epub ahead of print]
4.
go back to reference Marceau P, Biron S, Hould FS, et al. Duodenal switch improved standard biliopancreatic diversion: a retrospective study. Surg Obes Relat Dis. 2009;5(1):43–7.CrossRefPubMed Marceau P, Biron S, Hould FS, et al. Duodenal switch improved standard biliopancreatic diversion: a retrospective study. Surg Obes Relat Dis. 2009;5(1):43–7.CrossRefPubMed
5.
go back to reference Marceau P, Biron S, Marceau S, et al. Long-term metabolic outcomes 5 to 20 years after biliopancreatic diversion. Obes Surg. 2015;25(9):1584–93.CrossRefPubMed Marceau P, Biron S, Marceau S, et al. Long-term metabolic outcomes 5 to 20 years after biliopancreatic diversion. Obes Surg. 2015;25(9):1584–93.CrossRefPubMed
6.
go back to reference Scopinaro N. Biliopancreatic diversion: mechanisms of action and long-term results. Obes Surg. 2006;16(6):683–9.CrossRefPubMed Scopinaro N. Biliopancreatic diversion: mechanisms of action and long-term results. Obes Surg. 2006;16(6):683–9.CrossRefPubMed
7.
go back to reference Scopinaro N. Thirty-five years of biliopancreatic diversion: notes on gastrointestinal physiology to complete the published information useful for a better understanding and clinical use of the operation. Obes Surg. 2012;22(3):427–32.CrossRefPubMed Scopinaro N. Thirty-five years of biliopancreatic diversion: notes on gastrointestinal physiology to complete the published information useful for a better understanding and clinical use of the operation. Obes Surg. 2012;22(3):427–32.CrossRefPubMed
8.
go back to reference Strain GW, Torghabeh MH, Gagner M, et al. Nutrient status 9 years after biliopancreatic diversion with duodenal switch (BPD/DS): an observational study. Obes Surg. 2017; doi:10.1007/s11695-017-2560-6. [Epub ahead of print] Strain GW, Torghabeh MH, Gagner M, et al. Nutrient status 9 years after biliopancreatic diversion with duodenal switch (BPD/DS): an observational study. Obes Surg. 2017; doi:10.​1007/​s11695-017-2560-6. [Epub ahead of print]
9.
go back to reference Topart P, Becouarn G, Delarue J. Weight loss and nutritional outcomes 10 years after biliopancreatic diversion with duodenal switch. Obes Surg. 2017; doi:10.1007/s11695-016-2537-x. [Epub ahead of print] Topart P, Becouarn G, Delarue J. Weight loss and nutritional outcomes 10 years after biliopancreatic diversion with duodenal switch. Obes Surg. 2017; doi:10.​1007/​s11695-016-2537-x. [Epub ahead of print]
10.
go back to reference Sethi M, Chau E, Youn A, et al. Long-term outcomes after biliopancreatic diversion with and without duodenal switch: 2-, 5-, and 10-year data. Surg Obes Relat Dis. 2016;12(9):1697–705.CrossRefPubMed Sethi M, Chau E, Youn A, et al. Long-term outcomes after biliopancreatic diversion with and without duodenal switch: 2-, 5-, and 10-year data. Surg Obes Relat Dis. 2016;12(9):1697–705.CrossRefPubMed
11.
go back to reference Cazzo E, Pareja JC, Chaim EA. Liver failure following biliopancreatic diversions: a narrative review. Sao Paulo Med J. 2017;135(1):66–70.CrossRefPubMed Cazzo E, Pareja JC, Chaim EA. Liver failure following biliopancreatic diversions: a narrative review. Sao Paulo Med J. 2017;135(1):66–70.CrossRefPubMed
12.
go back to reference Geerts A, Darius T, Chapelle T, et al. The multicenter Belgian survey on liver transplantation for hepatocellular failure after bariatric surgery. Transplant Proc. 2010;42(10):4395–8.CrossRefPubMed Geerts A, Darius T, Chapelle T, et al. The multicenter Belgian survey on liver transplantation for hepatocellular failure after bariatric surgery. Transplant Proc. 2010;42(10):4395–8.CrossRefPubMed
13.
go back to reference Angrisani L, Santonicola A, Iovino P, et al. Bariatric surgery and endoluminal procedures: IFSO worldwide survey 2014. Obes Surg. 2017; doi:10.1007/s11695-017-2666-x. [Epub ahead of print] Angrisani L, Santonicola A, Iovino P, et al. Bariatric surgery and endoluminal procedures: IFSO worldwide survey 2014. Obes Surg. 2017; doi:10.​1007/​s11695-017-2666-x. [Epub ahead of print]
14.
go back to reference Neff KJ, O'Shea D, le Roux CW. Glucagon like peptide-1 (GLP-1) dynamics following bariatric surgery: a signpost to a new frontier. Curr Diabetes Rev. 2013;9(2):93–101.PubMed Neff KJ, O'Shea D, le Roux CW. Glucagon like peptide-1 (GLP-1) dynamics following bariatric surgery: a signpost to a new frontier. Curr Diabetes Rev. 2013;9(2):93–101.PubMed
15.
go back to reference Tsoli M, Chronaiou A, Kehagias I, et al. Hormone changes and diabetes resolution after biliopancreatic diversion and laparoscopic sleeve gastrectomy: a comparative prospective study. Surg Obes Relat Dis. 2013;9(5):667–77.CrossRefPubMed Tsoli M, Chronaiou A, Kehagias I, et al. Hormone changes and diabetes resolution after biliopancreatic diversion and laparoscopic sleeve gastrectomy: a comparative prospective study. Surg Obes Relat Dis. 2013;9(5):667–77.CrossRefPubMed
16.
go back to reference Cazzo E, Pareja JC, Geloneze B, et al. Biliopancreatic diversion decreases postprandial apolipoprotein A-IV levels in mildly obese individuals with type 2 diabetes mellitus: a prospective study. Obes Surg. 2017;27(4):1008–12.CrossRefPubMed Cazzo E, Pareja JC, Geloneze B, et al. Biliopancreatic diversion decreases postprandial apolipoprotein A-IV levels in mildly obese individuals with type 2 diabetes mellitus: a prospective study. Obes Surg. 2017;27(4):1008–12.CrossRefPubMed
17.
go back to reference Borg CM, le Roux CW, Ghatei MA, et al. Biliopancreatic diversion in rats is associated with intestinal hypertrophy and with increased GLP-1, GLP-2 and PYY levels. Obes Surg. 2007;17(9):1193–8.CrossRefPubMed Borg CM, le Roux CW, Ghatei MA, et al. Biliopancreatic diversion in rats is associated with intestinal hypertrophy and with increased GLP-1, GLP-2 and PYY levels. Obes Surg. 2007;17(9):1193–8.CrossRefPubMed
18.
go back to reference García-Unzueta MT, Fernández-Santiago R, Domínguez-Díez A, et al. Fasting plasma ghrelin levels increase progressively after biliopancreatic diversion: one-year follow-up. Obes Surg. 2005;15(2):187–90.CrossRefPubMed García-Unzueta MT, Fernández-Santiago R, Domínguez-Díez A, et al. Fasting plasma ghrelin levels increase progressively after biliopancreatic diversion: one-year follow-up. Obes Surg. 2005;15(2):187–90.CrossRefPubMed
19.
go back to reference Garcia-Fuentes E, Garrido-Sanchez L, Garcia-Almeida JM, et al. Different effect of laparoscopic roux-en-Y gastric bypass and open biliopancreatic diversion of Scopinaro on serum PYY and ghrelin levels. Obes Surg. 2008;18(11):1424–9.CrossRefPubMed Garcia-Fuentes E, Garrido-Sanchez L, Garcia-Almeida JM, et al. Different effect of laparoscopic roux-en-Y gastric bypass and open biliopancreatic diversion of Scopinaro on serum PYY and ghrelin levels. Obes Surg. 2008;18(11):1424–9.CrossRefPubMed
20.
go back to reference Dib N, Kiciak A, Pietrzak P, et al. Early-effect of bariatric surgery (Scopinaro method) on intestinal hormones and adipokines in insulin resistant Wistar rat. J Physiol Pharmacol. 2013;64(5):571–7.PubMed Dib N, Kiciak A, Pietrzak P, et al. Early-effect of bariatric surgery (Scopinaro method) on intestinal hormones and adipokines in insulin resistant Wistar rat. J Physiol Pharmacol. 2013;64(5):571–7.PubMed
21.
go back to reference Cazzo E, Pareja JC, Geloneze B, et al. Postprandial GLP-2 levels are increased after Biliopancreatic diversion in diabetic individuals with class I obesity: a prospective study. Obes Surg. 2017; doi:10.1007/s11695-017-2554-4. [Epub ahead of print] Cazzo E, Pareja JC, Geloneze B, et al. Postprandial GLP-2 levels are increased after Biliopancreatic diversion in diabetic individuals with class I obesity: a prospective study. Obes Surg. 2017; doi:10.​1007/​s11695-017-2554-4. [Epub ahead of print]
22.
go back to reference Meek CL, Lewis HB, Reimann F, et al. The effect of bariatric surgery on gastrointestinal and pancreatic peptide hormones. Peptides. 2016;77:28–37.CrossRefPubMed Meek CL, Lewis HB, Reimann F, et al. The effect of bariatric surgery on gastrointestinal and pancreatic peptide hormones. Peptides. 2016;77:28–37.CrossRefPubMed
23.
go back to reference Cazzo E, Pareja JC, Chaim EA, et al. GLP-1 and GLP-2 levels are correlated with satiety regulation after roux-en-Y gastric bypass: results of an exploratory prospective study. Obes Surg. 2017;27(3):703–8.CrossRefPubMed Cazzo E, Pareja JC, Chaim EA, et al. GLP-1 and GLP-2 levels are correlated with satiety regulation after roux-en-Y gastric bypass: results of an exploratory prospective study. Obes Surg. 2017;27(3):703–8.CrossRefPubMed
24.
go back to reference Campbell JE, Drucker DJ. Pharmacology, physiology, and mechanisms of incretin hormone action. Cell Metab. 2013;17(6):819–37.CrossRefPubMed Campbell JE, Drucker DJ. Pharmacology, physiology, and mechanisms of incretin hormone action. Cell Metab. 2013;17(6):819–37.CrossRefPubMed
25.
go back to reference Drucker DJ, Yusta B. Physiology and pharmacology of the enteroendocrine hormone glucagon-like peptide-2. Annu Rev Physiol. 2014;76:561–83.CrossRefPubMed Drucker DJ, Yusta B. Physiology and pharmacology of the enteroendocrine hormone glucagon-like peptide-2. Annu Rev Physiol. 2014;76:561–83.CrossRefPubMed
26.
go back to reference Garber AJ, Abrahamson MJ, Barzilay JI, et al. American Association of Clinical Endocrinologists' comprehensive diabetes management algorithm 2013 consensus statement—executive summary. Endocr Pract. 2013;19(3):536–57.CrossRefPubMedPubMedCentral Garber AJ, Abrahamson MJ, Barzilay JI, et al. American Association of Clinical Endocrinologists' comprehensive diabetes management algorithm 2013 consensus statement—executive summary. Endocr Pract. 2013;19(3):536–57.CrossRefPubMedPubMedCentral
27.
go back to reference Matthews DR, Hosker JP, Rudenski AS, et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28:412–9.CrossRefPubMed Matthews DR, Hosker JP, Rudenski AS, et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28:412–9.CrossRefPubMed
28.
go back to reference Flint A, Raben A, Blundell JE, et al. Reproducibility, power and validity of visual analogue scales in assessment of appetite sensations in single test meal studies. Int J Obes Relat Metab Disord. 2000;24(1):38–48.CrossRefPubMed Flint A, Raben A, Blundell JE, et al. Reproducibility, power and validity of visual analogue scales in assessment of appetite sensations in single test meal studies. Int J Obes Relat Metab Disord. 2000;24(1):38–48.CrossRefPubMed
30.
go back to reference Pardina E, López-Tejero MD, Llamas R, et al. Ghrelin and apolipoprotein AIV levels show opposite trends to leptin levels during weight loss in morbidly obese patients. Obes Surg. 2009;19(10):1414–23.CrossRefPubMed Pardina E, López-Tejero MD, Llamas R, et al. Ghrelin and apolipoprotein AIV levels show opposite trends to leptin levels during weight loss in morbidly obese patients. Obes Surg. 2009;19(10):1414–23.CrossRefPubMed
31.
go back to reference Rowston W, McCluskey S, Gazet JC, et al. Eating behavior, physical symptoms and psychological factors associated with weight reduction following the Scopinaro operation as modified by Gazet. Obes Surg. 1992;2(4):355–60.CrossRefPubMed Rowston W, McCluskey S, Gazet JC, et al. Eating behavior, physical symptoms and psychological factors associated with weight reduction following the Scopinaro operation as modified by Gazet. Obes Surg. 1992;2(4):355–60.CrossRefPubMed
32.
go back to reference Adami GF, Gandolfo P, Cocchi FH, et al. Binge eating following biliopancreatic diversion for obesity. Appetite. 1995;25(2):177–88.CrossRefPubMed Adami GF, Gandolfo P, Cocchi FH, et al. Binge eating following biliopancreatic diversion for obesity. Appetite. 1995;25(2):177–88.CrossRefPubMed
33.
go back to reference Kamiji MM, Troncon LE, Suen VM, et al. Gastrointestinal transit, appetite, and energy balance in gastrectomized patients. Am J Clin Nutr. 2009;89(1):231–9.CrossRefPubMed Kamiji MM, Troncon LE, Suen VM, et al. Gastrointestinal transit, appetite, and energy balance in gastrectomized patients. Am J Clin Nutr. 2009;89(1):231–9.CrossRefPubMed
34.
go back to reference Jeon TY, Lee S, Kim HH, et al. Long-term changes in gut hormones, appetite and food intake 1 year after subtotal gastrectomy with normal body weight. Eur J Clin Nutr. 2010;64(8):826–31.CrossRefPubMed Jeon TY, Lee S, Kim HH, et al. Long-term changes in gut hormones, appetite and food intake 1 year after subtotal gastrectomy with normal body weight. Eur J Clin Nutr. 2010;64(8):826–31.CrossRefPubMed
35.
go back to reference Kotidis EV, Koliakos G, Papavramidis TS, et al. The effect of biliopancreatic diversion with pylorus-preserving sleeve gastrectomy and duodenal switch on fasting serum ghrelin, leptin and adiponectin levels: is there a hormonal contribution to the weight-reducing effect of this procedure? Obes Surg. 2006 May;16(5):554–9.CrossRefPubMed Kotidis EV, Koliakos G, Papavramidis TS, et al. The effect of biliopancreatic diversion with pylorus-preserving sleeve gastrectomy and duodenal switch on fasting serum ghrelin, leptin and adiponectin levels: is there a hormonal contribution to the weight-reducing effect of this procedure? Obes Surg. 2006 May;16(5):554–9.CrossRefPubMed
36.
go back to reference Plourde CÉ, Grenier-Larouche T, Caron-Dorval D, et al. Biliopancreatic diversion with duodenal switch improves insulin sensitivity and secretion through caloric restriction. Obesity (Silver Spring). 2014;22(8):1838–46.CrossRef Plourde CÉ, Grenier-Larouche T, Caron-Dorval D, et al. Biliopancreatic diversion with duodenal switch improves insulin sensitivity and secretion through caloric restriction. Obesity (Silver Spring). 2014;22(8):1838–46.CrossRef
37.
go back to reference Gutzwiller JP, Drewe J, Göke B, et al. Glucagon-like peptide-1 promotes satiety and reduces food intake in patients with diabetes mellitus type 2. Am J Phys. 1999;276(5 Pt 2):R1541–4. Gutzwiller JP, Drewe J, Göke B, et al. Glucagon-like peptide-1 promotes satiety and reduces food intake in patients with diabetes mellitus type 2. Am J Phys. 1999;276(5 Pt 2):R1541–4.
38.
go back to reference Baggio LL, Huang Q, Brown TJ, et al. A recombinant human glucagon-like peptide (GLP)-1-albumin protein (albugon) mimics peptidergic activation of GLP-1 receptor-dependent pathways coupled with satiety, gastrointestinal motility, and glucose homeostasis. Diabetes. 2004;53(9):2492–500.CrossRefPubMed Baggio LL, Huang Q, Brown TJ, et al. A recombinant human glucagon-like peptide (GLP)-1-albumin protein (albugon) mimics peptidergic activation of GLP-1 receptor-dependent pathways coupled with satiety, gastrointestinal motility, and glucose homeostasis. Diabetes. 2004;53(9):2492–500.CrossRefPubMed
39.
go back to reference ten Kulve JS, Veltman DJ, van Bloemendaal L, et al. Endogenous GLP-1 mediates postprandial reductions in activation in central reward and satiety areas in patients with type 2 diabetes. Diabetologia. 2015;58(12):2688–98.CrossRefPubMedPubMedCentral ten Kulve JS, Veltman DJ, van Bloemendaal L, et al. Endogenous GLP-1 mediates postprandial reductions in activation in central reward and satiety areas in patients with type 2 diabetes. Diabetologia. 2015;58(12):2688–98.CrossRefPubMedPubMedCentral
40.
go back to reference Schmidt PT, Näslund E, Grybäck P, et al. Peripheral administration of GLP-2 to humans has no effect on gastric emptying or satiety. Regul Pept. 2003;116(1–3):21–5.CrossRefPubMed Schmidt PT, Näslund E, Grybäck P, et al. Peripheral administration of GLP-2 to humans has no effect on gastric emptying or satiety. Regul Pept. 2003;116(1–3):21–5.CrossRefPubMed
41.
go back to reference Sørensen LB, Flint A, Raben A, et al. No effect of physiological concentrations of glucagon-like peptide-2 on appetite and energy intake in normal weight subjects. Int J Obes Relat Metab Disord. 2003;27(4):450–6.CrossRefPubMed Sørensen LB, Flint A, Raben A, et al. No effect of physiological concentrations of glucagon-like peptide-2 on appetite and energy intake in normal weight subjects. Int J Obes Relat Metab Disord. 2003;27(4):450–6.CrossRefPubMed
42.
go back to reference Scopinaro N, Adami GF, Marinari GM, et al. Biliopancreatic diversion. World J Surg. 1998 Sep;22(9):936–46.CrossRefPubMed Scopinaro N, Adami GF, Marinari GM, et al. Biliopancreatic diversion. World J Surg. 1998 Sep;22(9):936–46.CrossRefPubMed
43.
go back to reference Papadia FS, Elghadban H, Weiss A, et al. BPD and BPD-DS concerns and results. In: Huang C, editor. Advanced bariatric and metabolic surgery. Rijeka: Intech Open; 2012. p. 175–210. Papadia FS, Elghadban H, Weiss A, et al. BPD and BPD-DS concerns and results. In: Huang C, editor. Advanced bariatric and metabolic surgery. Rijeka: Intech Open; 2012. p. 175–210.
44.
go back to reference Crea N, Pata G, Di Betta E, et al. Long-term results of biliopancreatic diversion with or without gastric preservation for morbid obesity. Obes Surg. 2011 Feb;21(2):139–45.CrossRefPubMed Crea N, Pata G, Di Betta E, et al. Long-term results of biliopancreatic diversion with or without gastric preservation for morbid obesity. Obes Surg. 2011 Feb;21(2):139–45.CrossRefPubMed
45.
go back to reference Cohen RV, Shikora S, Petry T, et al. The diabetes surgery summit II G7uidelines: a disease-based clinical recommendation. Obes Surg. 2016 Aug;26(8):1989–91.CrossRefPubMed Cohen RV, Shikora S, Petry T, et al. The diabetes surgery summit II G7uidelines: a disease-based clinical recommendation. Obes Surg. 2016 Aug;26(8):1989–91.CrossRefPubMed
46.
go back to reference Rubino F, Nathan DM, Eckel RH, et al. Metabolic surgery in the treatment algorithm for type 2 diabetes: a joint statement by international diabetes organizations. Diabetes Care. 2016 Jun;39(6):861–77.CrossRefPubMed Rubino F, Nathan DM, Eckel RH, et al. Metabolic surgery in the treatment algorithm for type 2 diabetes: a joint statement by international diabetes organizations. Diabetes Care. 2016 Jun;39(6):861–77.CrossRefPubMed
47.
go back to reference Scopinaro N, Adami GF, Papadia FS, et al. The effects of biliopancreatic diversion on type 2 diabetes mellitus in patients with mild obesity (BMI 30-35 kg/m2) and simple overweight (BMI 25-30 kg/m2): a prospective controlled study. Obes Surg. 2011;21(7):880–8.CrossRefPubMed Scopinaro N, Adami GF, Papadia FS, et al. The effects of biliopancreatic diversion on type 2 diabetes mellitus in patients with mild obesity (BMI 30-35 kg/m2) and simple overweight (BMI 25-30 kg/m2): a prospective controlled study. Obes Surg. 2011;21(7):880–8.CrossRefPubMed
48.
go back to reference Astiarraga B, Gastaldelli A, Muscelli E, et al. Biliopancreatic diversion in nonobese patients with type 2 diabetes: impact and mechanisms. J Clin Endocrinol Metab. 2013;98(7):2765–73.CrossRefPubMed Astiarraga B, Gastaldelli A, Muscelli E, et al. Biliopancreatic diversion in nonobese patients with type 2 diabetes: impact and mechanisms. J Clin Endocrinol Metab. 2013;98(7):2765–73.CrossRefPubMed
49.
go back to reference Fried M, Ribaric G, Buchwald JN, et al. Metabolic surgery for the treatment of type 2 diabetes in patients with BMI <35 kg/m2: an integrative review of early studies. Obes Surg. 2010;20(6):776–90.CrossRefPubMed Fried M, Ribaric G, Buchwald JN, et al. Metabolic surgery for the treatment of type 2 diabetes in patients with BMI <35 kg/m2: an integrative review of early studies. Obes Surg. 2010;20(6):776–90.CrossRefPubMed
Metadata
Title
Glucagon-Like Peptides 1 and 2 Are Involved in Satiety Modulation After Modified Biliopancreatic Diversion: Results of a Pilot Study
Authors
Everton Cazzo
José Carlos Pareja
Elinton Adami Chaim
Cláudio Saddy Rodrigues Coy
Daniéla Oliveira Magro
Publication date
01-02-2018
Publisher
Springer US
Published in
Obesity Surgery / Issue 2/2018
Print ISSN: 0960-8923
Electronic ISSN: 1708-0428
DOI
https://doi.org/10.1007/s11695-017-2875-3

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