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The effect of vertical sleeve gastrectomy on food choice in rats

Abstract

OBJECTIVE:

Diets high in fat are implicated in the development and maintenance of obesity, and obese individuals display greater preferences for high-fat foods than do their lean counterparts. Weight-reduction bariatric surgery is associated with changes in food choice. In particular, after Roux-en-Y gastric bypass (RYGB), humans and rodents select or prefer foods that are lower in fat content. We asked whether a bariatric surgical procedure limited to the stomach, vertical sleeve gastrectomy (VSG), causes a similar reduction of fat intake/preference.

RESEARCH DESIGN AND METHODS:

Rats received VSG or Sham surgery or remained surgically naïve, and were assessed for food preference using three diet-choice paradigms. Using progressive-ratio (PR) and conditioned taste aversion paradigms, we further asked whether surgically induced changes in food choice are secondary to changes in the reward value of food and/or to the formation of a food aversion. Finally, food choice was compared between VSG- and RYGB-operated rats.

RESULTS:

VSG rats decreased their intake of dietary fat, and shifted their preference toward lower caloric-density foods. This change in food choice was not associated with changes in motivated responding on a PR schedule for either a fat or a carbohydrate food reinforcer. When VSG and RYGB were compared directly, both procedures caused comparable changes in food choice. The conditioned taste aversion paradigm revealed that VSG rats form an aversion to an intra-gastric oil administration whereas RYGB rats do not.

CONCLUSIONS:

VSG and RYGB, two anatomically distinct bariatric procedures, produce similar changes in food choice.

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References

  1. Winzell MS, Ahren B . The high-fat diet-fed mouse: a model for studying mechanisms and treatment of impaired glucose tolerance and type 2 diabetes. Diabetes 2004; 53 (Suppl 3): S215–S219.

    Article  Google Scholar 

  2. Hill JO, Melanson EL, Wyatt HT . Dietary fat intake and regulation of energy balance: implications for obesity. J Nutr 2000; 130 (2S Suppl): 284S–288S.

    Article  CAS  Google Scholar 

  3. Lissner L, Heitmann BL . Dietary fat and obesity: evidence from epidemiology. Eur J Clin Nutr 1995; 49: 79–90.

    CAS  Google Scholar 

  4. de Wit NJ, Boekschoten MV, Bachmair EM, Hooiveld GJ, de Groot PJ, Rubio-Aliaga I et al. Dose-dependent effects of dietary fat on development of obesity in relation to intestinal differential gene expression in C57BL/6J mice. PLoS One 2011; 6: e19145.

    Article  CAS  Google Scholar 

  5. Drewnowski A, Kurth C, Holden-Wiltse J, Saari J . Food preferences in human obesity: carbohydrates versus fats. Appetite 1992; 18: 207–221.

    Article  CAS  Google Scholar 

  6. Drewnowski A, Brunzell JD, Sande K, Iverius PH, Greenwood MR . Sweet tooth reconsidered: taste responsiveness in human obesity. Physiol Behav 1985; 35: 617–622.

    Article  CAS  Google Scholar 

  7. Thomas JR, Marcus E . High and low fat food selection with reported frequency intolerance following Roux-en-Y gastric bypass. Obes Surg 2008; 18: 282–287.

    Article  Google Scholar 

  8. Thirlby RC, Bahiraei F, Randall J, Drewnoski A . Effect of Roux-en-Y gastric bypass on satiety and food likes: the role of genetics. J Gastrointest Surg 2006; 10: 270–277.

    Article  Google Scholar 

  9. Ernst B, Thurnheer M, Wilms B, Schultes B . Differential changes in dietary habits after gastric bypass versus gastric banding operations. Obes Surg 2009; 19: 274–280.

    Article  Google Scholar 

  10. Lindroos AK, Lissner L, Sjostrom L . Weight change in relation to intake of sugar and sweet foods before and after weight reducing gastric surgery. Int J Obes Relat Metab Disord 1996; 20: 634–643.

    CAS  PubMed  Google Scholar 

  11. Zheng H, Shin AC, Lenard NR, Townsend RL, Patterson LM, Sigalet DL et al. Meal patterns, satiety, and food choice in a rat model of Roux-en-Y gastric bypass surgery. Am J Physiol Regul Integr Comp Physiol 2009; 297: R1273–R1282.

    Article  CAS  Google Scholar 

  12. Stefater MA, Perez-Tilve D, Chambers AP, Wilson-Perez HE, Sandoval DA, Berger J et al. Sleeve gastrectomy induces loss of weight and fat mass in obese rats, but does not affect leptin sensitivity. Gastroenterology 2010; 138: 2426–2436 e1–e3.

    Article  CAS  Google Scholar 

  13. Peterli R, Wolnerhanssen B, Peters T, Devaux N, Kern B, Christoffel-Courtin C et al. Improvement in glucose metabolism after bariatric surgery: comparison of laparoscopic Roux-en-Y gastric bypass and laparoscopic sleeve gastrectomy: a prospective randomized trial. Ann Surg 2009; 250: 234–241.

    Article  Google Scholar 

  14. Karamanakos SN, Vagenas K, Kalfarentzos F, Alexandrides TK . 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 2008; 247: 401–407.

    Article  Google Scholar 

  15. Saelens BE, Epstein LH . Reinforcing value of food in obese and non-obese women. Appetite 1996; 27: 41–50.

    Article  CAS  Google Scholar 

  16. Temple JL, Legierski CM, Giacomelli AM, Salvy SJ, Epstein LH . Overweight children find food more reinforcing and consume more energy than do nonoverweight children. Am J Clin Nutr 2008; 87: 1121–1127.

    Article  CAS  Google Scholar 

  17. Clark EN, Dewey AM, Temple JL . Effects of daily snack food intake on food reinforcement depend on body mass index and energy density. Am J Clin Nutr 2010; 91: 300–308.

    Article  CAS  Google Scholar 

  18. Hill C, Saxton J, Webber L, Blundell J, Wardle J . The relative reinforcing value of food predicts weight gain in a longitudinal study of 7--10-y-old children. Am J Clin Nutr 2009; 90: 276–281.

    Article  CAS  Google Scholar 

  19. Abell TL, Minocha A . Gastrointestinal complications of bariatric surgery: diagnosis and therapy. Am J Med Sci 2006; 331: 214–218.

    Article  Google Scholar 

  20. Tack J, Arts J, Caenepeel P, De Wulf D, Bisschops R . Pathophysiology, diagnosis and management of postoperative dumping syndrome. Nat Rev Gastroenterol Hepatol 2009; 6: 583–590.

    Article  Google Scholar 

  21. Chambers AP, Jessen L, Ryan KK, Sisley S, Wilson-Perez HE, Stefater MA et al. Weight-independent changes in blood glucose homeostasis after gastric bypass or vertical sleeve gastrectomy in rats. Gastroenterology 2011; 141: 950–958.

    Article  CAS  Google Scholar 

  22. Tracy AL, Clegg DJ, Johnson JD, Davidson TL, Benoit SC . The melanocortin antagonist AgRP (83-132) increases appetitive responding for a fat, but not a carbohydrate, reinforcer. Pharmacol Biochem Behav 2008; 89: 263–271.

    Article  CAS  Google Scholar 

  23. Wilson-Perez HE, Seeley RJ . The effect of vertical sleeve gastrectomy on a rat model of polycystic ovarian syndrome. Endocrinology 2011; 152: 3700–3705.

    Article  CAS  Google Scholar 

  24. Inoue K, Kiriike N, Fujisaki Y, Kurioka M, Yamagami S . Effects of fluvoxamine on food intake during rebound hyperphagia in rats. Physiol Behav 1997; 61: 603–608.

    Article  CAS  Google Scholar 

  25. Vickers SP, Webster LJ, Wyatt A, Dourish CT, Kennett GA . Preferential effects of the cannabinoid CB1 receptor antagonist, SR 141716, on food intake and body weight gain of obese (fa/fa) compared to lean Zucker rats. Psychopharmacology (Berl) 2003; 167: 103–111.

    Article  CAS  Google Scholar 

  26. Schreiber R, Selbach K, Asmussen M, Hesse D, de Vry J . Effects of serotonin(1/2) receptor agonists on dark-phase food and water intake in rats. Pharmacol Biochem Behav 2000; 67: 291–305.

    Article  CAS  Google Scholar 

  27. Smith BK, Berthoud HR, York DA, Bray GA . Differential effects of baseline macronutrient preferences on macronutrient selection after galanin, NPY, and an overnight fast. Peptides 1997; 18: 207–211.

    Article  CAS  Google Scholar 

  28. Thouzeau C, Le Maho Y, Larue-Achagiotis C . Refeeding in fasted rats: dietary self-selection according to metabolic status. Physiol Behav 1995; 58: 1051–1058.

    Article  CAS  Google Scholar 

  29. Welch CC, Grace MK, Billington CJ, Levine AS . Preference and diet type affect macronutrient selection after morphine, NPY, norepinephrine, and deprivation. Am J Physiol 1994; 266 (2 Pt 2): R426–R433.

    CAS  PubMed  Google Scholar 

  30. Le Roux CW, Bueter M, Theis N, Werling M, Ashrafian H, Lowenstein C et al. Gastric bypass reduces fat intake and preference. Am J Physiol Regul Integr Comp Physiol 2011; 301: R1057–R1066.

    Article  CAS  Google Scholar 

  31. Ramirez I, Tordoff MG, Friedman MI . Satiety from fat? Adverse effects of intestinal infusion of sodium oleate. Am J Physiol 1997; 273 (5 Pt 2): R1779–R1785.

    CAS  PubMed  Google Scholar 

  32. Peters CT, Choi YH, Brubaker PL, Anderson GH . A glucagon-like peptide-1 receptor agonist and an antagonist modify macronutrient selection by rats. J Nutr 2001; 131: 2164–2170.

    Article  CAS  Google Scholar 

  33. Aziz A, Anderson GH . Exendin-4, a GLP-1 receptor agonist, modulates the effect of macronutrients on food intake by rats. J Nutr 2002; 132: 990–995.

    Article  CAS  Google Scholar 

  34. Stanley BG, Daniel DR, Chin AS, Leibowitz SF . Paraventricular nucleus injections of peptide YY and neuropeptide Y preferentially enhance carbohydrate ingestion. Peptides 1985; 6: 1205–1211.

    Article  CAS  Google Scholar 

  35. Shimbara T, Mondal MS, Kawagoe T, Toshinai K, Koda S, Yamaguchi H et al. Central administration of ghrelin preferentially enhances fat ingestion. Neurosci Lett 2004; 369: 75–79.

    Article  CAS  Google Scholar 

  36. Egecioglu E, Jerlhag E, Salome N, Skibicka KP, Haage D, Bohlooly YM et al. Ghrelin increases intake of rewarding food in rodents. Addict Biol 2010; 15: 304–311.

    Article  CAS  Google Scholar 

  37. Li F, Zhang G, Liang J, Ding X, Cheng Z, Hu S . Sleeve gastrectomy provides a better control of diabetes by decreasing ghrelin in the diabetic Goto-Kakizaki rats. J Gastrointest Surg 2009; 13: 2302–2308.

    Article  Google Scholar 

  38. Thaler JP, Cummings DE . Minireview: hormonal and metabolic mechanisms of diabetes remission after gastrointestinal surgery. Endocrinology 2009; 150: 2518–2525.

    Article  CAS  Google Scholar 

  39. Burge JC, Schaumburg JZ, Choban PS, DiSilvestro RA, Flancbaum L . Changes in patients’ taste acuity after Roux-en-Y gastric bypass for clinically severe obesity. J Am Diet Assoc 1995; 95: 666–670.

    Article  CAS  Google Scholar 

  40. Scruggs DM, Buffington C, Cowan Jr GS . Taste acuity of the morbidly obese before and after gastric bypass surgery. Obes Surg 1994; 4: 24–28.

    Article  CAS  Google Scholar 

  41. Ochner CN, Kwok Y, Conceicao E, Pantazatos SP, Puma LM, Carnell S et al. Selective reduction in neural responses to high calorie foods following gastric bypass surgery. Ann Surg 2011; 253: 502–507.

    Article  Google Scholar 

  42. Patti ME, Houten SM, Bianco AC, Bernier R, Larsen PR, Holst JJ et al. Serum bile acids are higher in humans with prior gastric bypass: potential contribution to improved glucose and lipid metabolism. Obesity (Silver Spring) 2009; 17: 1671–1677.

    Article  CAS  Google Scholar 

  43. Asztalos BF, Swarbrick MM, Schaefer EJ, Dallal GE, Horvath KV, Ai M et al. Effects of weight loss, induced by gastric bypass surgery, on HDL remodeling in obese women. J Lipid Res 2010; 51: 2405–2412.

    Article  CAS  Google Scholar 

  44. Zlabek JA, Grimm MS, Larson CJ, Mathiason MA, Lambert PJ, Kothari SN . The effect of laparoscopic gastric bypass surgery on dyslipidemia in severely obese patients. Surg Obes Relat Dis 2005; 1: 537–542.

    Article  Google Scholar 

  45. Stefater MA, Sandoval DA, Chambers AP, Wilson-Perez HE, Hofmann SM, Jandacek R et al. Sleeve gastrectomy in rats improves post-prandial lipid clearance by reducing intestinal triglyceride secretion. Gastroenterology 2011; 141: 939–949. e1-4.

    Article  CAS  Google Scholar 

  46. Nguyen NT, Varela E, Sabio A, Tran CL, Stamos M, Wilson SE . Resolution of hyperlipidemia after laparoscopic Roux-en-Y gastric bypass. J Am Coll Surg 2006; 203: 24–29.

    Article  Google Scholar 

  47. Singer LK, York DA, Bray GA . Macronutrient selection following 2-deoxy-D-glucose and mercaptoacetate administration in rats. Physiol Behav 1998; 65: 115–121.

    Article  CAS  Google Scholar 

  48. Ritter S, Koegler FH, Wiater M . Chapter 13. Effects of metabolic blockade on macronutrient selection. In: Berthoud H-R, Seeley RJ (eds). Neural and Metabolic Control of Macronutrient Intake. CRC Press: New York, 2000.

    Google Scholar 

  49. Langhans W, Leitner C, Arnold M . Dietary fat sensing via fatty acid oxidation in enterocytes: possible role in the control of eating. Am J Physiol Regul Integr Comp Physiol 2011; 300: R554–R565.

    Article  CAS  Google Scholar 

  50. Berger K, Winzell MS, Mei J, Erlanson-Albertsson C . Enterostatin and its target mechanisms during regulation of fat intake. Physiol Behav 2004; 83: 623–630.

    Article  CAS  Google Scholar 

  51. Okada S, York DA, Bray GA, Erlanson-Albertsson C . Enterostatin (Val-Pro-Asp-Pro-Arg), the activation peptide of procolipase, selectively reduces fat intake. Physiol Behav 1991; 49: 1185–1189.

    Article  CAS  Google Scholar 

  52. Erlanson-Albertsson C, Mei J, Okada S, York D, Bray GA . Pancreatic procolipase propeptide, enterostatin, specifically inhibits fat intake. Physiol Behav 1991; 49: 1191–1194.

    Article  CAS  Google Scholar 

  53. Laugerette F, Passilly-Degrace P, Patris B, Niot I, Febbraio M, Montmayeur JP et al. CD36 involvement in orosensory detection of dietary lipids, spontaneous fat preference, and digestive secretions. J Clin Invest 2005; 115: 3177–3184.

    Article  CAS  Google Scholar 

  54. Sclafani A, Ackroff K, Abumrad NA . CD36 gene deletion reduces fat preference and intake but not post-oral fat conditioning in mice. Am J Physiol Regul Integr Comp Physiol 2007; 293: R1823–R1832.

    Article  CAS  Google Scholar 

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Acknowledgements

We thank Jose Berger, April Haller, Alfor Lewis, Kenneth Parks, Kathi Smith and Mouhamadoul Toure for their surgical expertise in conducting the VSG, RYGB and sham surgeries. We also thank Brad Chambers and Jon Davis for technical assistance with the Progressive-Ratio experiments. This work was supported by the NIH grants DK54890 and DK82480 and Ethicon Endo-Surgery. HWP is supported by the NIH training grant T32 HD07463 and a grant from the Ryan Foundation.

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Correspondence to R J Seeley.

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Randy J Seeley—Johnson & Johnson (Ethicon Endo-Surgery), Zafgen, Merck, Pfizer, Mannkind, Roche; Darleen A Sandoval—Johnson & Johnson (Ethicon Endo-Surgery), Pfizer, Mannkind, Novonordisk and Stephen C Benoit—Johnson & Johnson (Ethicon Endo-Surgery).

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Wilson-Pérez, H., Chambers, A., Sandoval, D. et al. The effect of vertical sleeve gastrectomy on food choice in rats. Int J Obes 37, 288–295 (2013). https://doi.org/10.1038/ijo.2012.18

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