Obesity Surgery

, Volume 23, Issue 1, pp 39–49

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

  • Helene Johannessen
  • Yosuke Kodama
  • Chun-Mei Zhao
  • Mirta M L Sousa
  • Geir Slupphaug
  • Bård Kulseng
  • Duan Chen
Animal Research

Abstract

Background

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.

Methods

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.

Results

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.

Conclusions

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.

Keywords

Food intake GLP-1 Ileal interposition Ileum Pancreatic islets Sleeve gastrectomy Energy expenditure Respiratory exchange ratio 

References

  1. 1.
    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.PubMedCrossRefGoogle Scholar
  2. 2.
    Buchwald H, Avidor Y, Braunwald E, et al. Bariatric surgery: a systematic review and meta-analysis. JAMA. 2004;292:1724–37.PubMedCrossRefGoogle Scholar
  3. 3.
    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.PubMedCrossRefGoogle Scholar
  4. 4.
    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.PubMedCrossRefGoogle Scholar
  5. 5.
    Mason EE. Ilial transposition and enteroglucagon/GLP-1 in obesity (and diabetic?) Surgery. Obes Surg. 1999;9:223–8.PubMedCrossRefGoogle Scholar
  6. 6.
    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.PubMedCrossRefGoogle Scholar
  7. 7.
    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.PubMedCrossRefGoogle Scholar
  8. 8.
    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.PubMedCrossRefGoogle Scholar
  9. 9.
    Russell W, Burch R. The principles of humane experimental technique. London: Methuen; 1959.Google Scholar
  10. 10.
    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.PubMedCrossRefGoogle Scholar
  11. 11.
    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.PubMedCrossRefGoogle Scholar
  12. 12.
    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.Google Scholar
  13. 13.
    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.Google Scholar
  14. 14.
    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.PubMedGoogle Scholar
  15. 15.
    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.CrossRefGoogle Scholar
  16. 16.
    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.Google Scholar
  17. 17.
    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.PubMedCrossRefGoogle Scholar
  18. 18.
    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.PubMedCrossRefGoogle Scholar
  19. 19.
    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.PubMedCrossRefGoogle Scholar
  20. 20.
    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.PubMedCrossRefGoogle Scholar
  21. 21.
    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.PubMedCrossRefGoogle Scholar
  22. 22.
    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.PubMedCrossRefGoogle Scholar
  23. 23.
    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.PubMedCrossRefGoogle Scholar
  24. 24.
    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.PubMedCrossRefGoogle Scholar
  25. 25.
    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.PubMedCrossRefGoogle Scholar
  26. 26.
    DeSesso JM, Jacobson CF. Anatomical and physiological parameters affecting gastrointestinal absorption in humans and rats. Food Chem Toxicol. 2001;39:209–28.PubMedCrossRefGoogle Scholar
  27. 27.
    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.Google Scholar
  28. 28.
    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.PubMedCrossRefGoogle Scholar
  29. 29.
    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.PubMedCrossRefGoogle Scholar
  30. 30.
    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.Google Scholar
  31. 31.
    Kararli TT. Comparison of the gastrointestinal anatomy, physiology, and biochemistry of humans and commonly used laboratory animals. Biopharm Drug Dispos. 1995;16:351–80.PubMedCrossRefGoogle Scholar
  32. 32.
    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.Google Scholar
  33. 33.
    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.PubMedCrossRefGoogle Scholar
  34. 34.
    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.PubMedCrossRefGoogle Scholar
  35. 35.
    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.PubMedCrossRefGoogle Scholar
  36. 36.
    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.PubMedCrossRefGoogle Scholar
  37. 37.
    Bueter M, Löwenstein C, Olbers T, et al. Gastric bypass increases energy expenditure in rats. Gastroenterology. 2010;138:1845–53. e1.PubMedCrossRefGoogle Scholar
  38. 38.
    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.CrossRefGoogle Scholar
  39. 39.
    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.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science + Business Media, LLC 2012

Authors and Affiliations

  • Helene Johannessen
    • 1
  • Yosuke Kodama
    • 1
  • Chun-Mei Zhao
    • 1
    • 2
  • Mirta M L Sousa
    • 1
  • Geir Slupphaug
    • 1
  • Bård Kulseng
    • 1
    • 2
  • Duan Chen
    • 1
    • 2
  1. 1.Department of Cancer Research and Molecular MedicineNorwegian University of Science and TechnologyTrondheimNorway
  2. 2.Department of SurgerySt. Olav’s University HospitalTrondheimNorway

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