Eating Behavior and Glucagon-Like Peptide-1-Producing Cells in Interposed Ileum and Pancreatic Islets in Rats Subjected to Ileal Interposition Associated with Sleeve Gastrectomy
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Ileal interposition–sleeve gastrectomy (II–SG) has been developed as a metabolic surgery based on the hindgut hypothesis. The aim of the present study was to test this hypothesis by studying the eating behavior, metabolic changes, and glucagon-like peptide-1 (GLP-1)-producing cells in rat models.
Male Sprague–Dawley rats were subjected to laparotomy, II, SG, or II–SG. Eating behavior and metabolic parameters were monitored by an open-circuit indirect calorimeter designed for a comprehensive laboratory animal monitoring system. GLP-1-producing cells were examined by quantitative immunohistochemistry.
After II alone, satiety ratio, i.e., intermeal interval/meal size, was reduced, while calorie intake was increased at 2 and 6 weeks postoperatively. Respiratory exchange ratio, VCO2/VO2, was increased to above 1.0 (i.e., carbohydrate metabolism) during both daytime and nighttime at 2 weeks postoperatively. After SG alone, GLP-1-producing cells were increased in the pancreatic islets (in terms of volume density), but not in the ileum (number/mm). After II–SG, the rate of eating was reduced, while meal duration (min) was increased during both daytime and nighttime at 2 weeks postoperatively. GLP-1-producing cells were increased by about 2.5-fold in the interposed ileum and also increased to the same extent in the pancreatic islets as seen after SG alone. The increased GLP-1-producing cells in the pancreatic islets after SG or II–SG were located around the insulin-producing β cells.
The present study provides evidence supporting the hindgut hypothesis. II–SG increased GLP-1 production both in the interposed ileum and in the pancreatic islets, leading to metabolic beneficial effects and altered eating behavior.
- Rubino F, R’bibo SL, del Genio F, et al. Metabolic surgery: the role of the gastrointestinal tract in diabetes mellitus. Nat Rev Endocrinol. 2010;6:102–9. CrossRef
- Buchwald H, Avidor Y, Braunwald E, et al. Bariatric surgery: a systematic review and meta-analysis. JAMA. 2004;292:1724–37. CrossRef
- Mingrone G, Panunzi S, De Gaetano A, et al. Bariatric surgery versus conventional medical therapy for type 2 diabetes. N Engl J Med. 2012;366:1577–85. CrossRef
- Schauer PR, Kashyap SR, Wolski K, et al. Bariatric surgery versus intensive medical therapy in obese patients with diabetes. N Engl J Med. 2012;366:1567–76. CrossRef
- Mason EE. Ilial transposition and enteroglucagon/GLP-1 in obesity (and diabetic?) Surgery. Obes Surg. 1999;9:223–8. CrossRef
- Patriti A, Facchiano E, Sanna A, et al. The enteroinsular axis and the recovery from type 2 diabetes after bariatric surgery. Obes Surg. 2004;14:840–8. CrossRef
- Patriti A, Facchiano E, Annetti C, et al. Early improvement of glucose tolerance after ileal transposition in a non-obese type 2 diabetes rat model. Obes Surg. 2005;15:1258–64. CrossRef
- Cummings BP, Strader AD, Stanhope KL, et al. Ileal interposition surgery improves glucose and lipid metabolism and delays diabetes onset in the UCD-T2DM rat. Gastroenterology. 2010;138:2437–46. CrossRef
- Russell W, Burch R. The principles of humane experimental technique. London: Methuen; 1959.
- Lopez PP, Nicholson SE, Burkhardt GE, et al. Development of a sleeve gastrectomy weight loss model in obese Zucker rats. J Surg Res. 2009;157:243–50. CrossRef
- Kotler DP, Koopmans HS. Preservation of intestinal structure and function despite weight loss produced by ileal transposition in rats. Physiol Behav. 1984;32:423–7. CrossRef
- Chen DC, Stern JS, Atkinson RL. Effects of ileal transposition on food intake, dietary preference, and weight gain in Zucker obese rats. Am J Physiol-Reg I. 1990;27:R269–73.
- Atkinson RL, Whipple JH, Atkinson SH, et al. Role of the small bowel in regulating food intake in rats. Am J Physiol-Reg I. 1982;11:R429–33.
- Koopmans HS, Sclafani A, Fichtner C, et al. The effects of ileal transposition on food intake and body weight loss in VMH-obese rats. Am J Clin Nutr. 1982;35:284–93.
- Arch J, Hislop D, Wang S, et al. Some mathematical and technical issues in the measurement and interpretation of open-circuit indirect calorimetry in small animals. Int J Obesity. 2006;30:1322–31. CrossRef
- Strader AD, Vahl TP, Jandacek RJ, et al. Weight loss through ileal transposition is accompanied by increased ileal hormone secretion and synthesis in rats. Am J Physiol-Endoc M. 2004;288:E447–53.
- Wang TT, Hu SY, Gao HD, et al. Ileal transposition controls diabetes as well as modified duodenal jejunal bypass with better lipid lowering in a nonobese rat model of type 2 diabetes by increasing GLP-1. Ann Surg. 2008;247:968–75. CrossRef
- Yan Z, Chen W, Liu S, et al. Myocardial insulin signaling and glucose transport are up-regulated in Goto–Kakizaki type 2 diabetic rats after ileal transposition. Obes Surg. 2012;22:493–501. CrossRef
- Chen W, Yan Z, Liu S, et al. The changes of pro-opiomelanocortin neurons in type 2 diabetes mellitus rats after ileal transposition: the role of POMC neurons. J Gastrointest Surg. 2011;15:1618–24. CrossRef
- Chelikani PK, Shah IH, Taqi E, et al. Comparison of the effects of Roux-en-Y gastric bypass and ileal transposition surgeries on food intake, body weight, and circulating peptide YY concentrations in rats. Obes Surg. 2010;20:1281–8. CrossRef
- Patriti A, Aisa MC, Annetti C, et al. How the hindgut can cure type 2 diabetes. Ileal transposition improves glucose metabolism and beta-cell function in Goto–Kakizaki rats through an enhanced Proglucagon gene expression and L-cell number. Surgery. 2007;142:74–85. CrossRef
- Kindel TL, Yoder SM, Seeley RJ, et al. Duodenal–jejunal exclusion improves glucose tolerance in the diabetic, Goto–Kakizaki rat by a GLP-1 receptor-mediated mechanism. J Gastrointest Surg. 2009;13:1762–77. CrossRef
- Ikezawa F, Shibata C, Kikuchi D, et al. Effects of ileal interposition on glucose metabolism in obese rats with diabetes. Surgery. 2012;151:822–30. CrossRef
- Culnan DM, Albaugh V, Sun M, et al. Ileal interposition improves glucose tolerance and insulin sensitivity in the obese Zucker rat. Am J Physiol Gastrointest Liver Physiol. 2010;299:G751–60. CrossRef
- Zhang GY, Wang TT, Cheng ZQ, et al. Resolution of diabetes mellitus by ileal transposition compared with biliopancreatic diversion in a nonobese animal model of type 2 diabetes. Can J Surg. 2011;54:243–51. CrossRef
- DeSesso JM, Jacobson CF. Anatomical and physiological parameters affecting gastrointestinal absorption in humans and rats. Food Chem Toxicol. 2001;39:209–28. CrossRef
- Tsuchiya T, Kalogeris TJ, Tso P. Ileal transposition into the upper jejunum affects lipid and bile salt absorption in rats. Am J Physiol-Gastr L. 1996;34:G681–91.
- DePaula AL, Macedo ALV, Rassi N, et al. Laparoscopic treatment of metabolic syndrome in patients with type 2 diabetes mellitus. Surg Endosc. 2008;22:2670–8. CrossRef
- DePaula AL, Stival A, Halpern A, et al. Thirty-day morbidity and mortality of the laparoscopic ileal interposition associated with sleeve gastrectomy for the treatment of type 2 diabetic patients with BMI <35: an analysis of 454 consecutive patients. World J Surg. 2011;35:102–8. CrossRef
- DePaula AL, Stival A, Halpern A, Vencio S. Surgical treatment of morbid obesity: mid-term outcomes of the laparoscopic ileal interposition associated to a sleeve gastrectomy in 120 patients. Obes Surg 2010.
- Kararli TT. Comparison of the gastrointestinal anatomy, physiology, and biochemistry of humans and commonly used laboratory animals. Biopharm Drug Dispos. 1995;16:351–80. CrossRef
- Gagner M. La transposition ileale avec ou sans gastrectomie par laparoscopie chez l'homme (TIG): la troisieme generation de chirurgie bariatrique. J Coeliochirurgie 2005:4-10.
- DePaula AL, Macedo ALV, Schraibman V, et al. Hormonal evaluation following laparoscopic treatment of type 2 diabetes mellitus patients with BMI 20–34. Surg Endosc. 2009;23:1724–32. CrossRef
- De Paula A, Stival A, Halpern A, et al. Improvement in insulin sensitivity and Β-cell function following ileal interposition with sleeve gastrectomy in type 2 diabetic patients: potential mechanisms. J Gastrointest Surg. 2011;15:1344–53. CrossRef
- Kodama Y, Zhao CM, Kulseng B, et al. Eating behavior in rats subjected to vagotomy, sleeve gastrectomy, and duodenal switch. J Gastrointest Surg. 2010;14:1502–10. CrossRef
- Furnes M, Tømmerås K, Arum CJ, et al. Gastric bypass surgery causes body weight loss without reducing food intake in rats. Obes Surg. 2008;18:415–22. CrossRef
- Bueter M, Löwenstein C, Olbers T, et al. Gastric bypass increases energy expenditure in rats. Gastroenterology. 2010;138:1845–53. e1. CrossRef
- Stylopoulos N, Hoppin AG, Kaplan LM. Roux-en-Y gastric bypass enhances energy expenditure and extends lifespan in diet-induced obese rats. Obesity (Silver Spring). 2009;17:1839–47. CrossRef
- Hansen L, Deacon CF, Ørskov C, et al. Glucagon-like peptide-1-(7–36)amide is transformed to glucagon-like peptide-1-(9–36)amide by dipeptidyl peptidase IV in the capillaries supplying the L cells of the porcine intestine. Endocrinology. 1999;140:5356–63. CrossRef
- Eating Behavior and Glucagon-Like Peptide-1-Producing Cells in Interposed Ileum and Pancreatic Islets in Rats Subjected to Ileal Interposition Associated with Sleeve Gastrectomy
Volume 23, Issue 1 , pp 39-49
- Cover Date
- Print ISSN
- Online ISSN
- Additional Links
- Food intake
- Ileal interposition
- Pancreatic islets
- Sleeve gastrectomy
- Energy expenditure
- Respiratory exchange ratio
- Industry Sectors
- Author Affiliations
- 1. Department of Cancer Research and Molecular Medicine, Norwegian University of Science and Technology, Trondheim, Norway
- 2. Department of Surgery, St. Olav’s University Hospital, Trondheim, Norway