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Increase in Ghrelin Levels After Weight Loss in Obese Zucker Rats is Prevented by Gastric Banding

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Abstract

Background

Gastric banding is thought to decrease appetite in addition to the mechanical effects of food restriction, although this has been difficult to demonstrate in human studies. Our aim was to investigate the changes in orexigenic signals in the obese Zucker rat after gastric banding.

Methods

Obese Zucker rats (fa/fa) were submitted to gastric banding (GBP), sham gastric banding fed ad libitum (sham), or sham operation with food restriction, pair-fed to the gastric banding group (sham-PF). Lean Zucker rats (fa/+) were used as additional controls. Body weight and food intake were daily recorded for 21 days after surgery when epididymal fat was weighed and fasting ghrelin and hypothalamic NPY mRNA expression were measured.

Results

Gastric banding in obese Zucker rats resulted in a significant decrease of cumulative body weight gain and food intake. Furthermore, gastric banded rats were leaner than Sham-PF, as expressed by a significantly lower epididymal fat weight. Ghrelin levels of gastric banded rats were not increased when compared to sham-operated animals fed ad libitum and were significantly lower than the levels of weight matched sham-PF rats (1116.9 ± 103.3 g GBP vs 963.2 ± 54.3 g sham, 3,079.5 ± 221.6 sham-PF and 2,969.9 ± 150.9 g lean rats, p < 0.001); hypothalamic NPY mRNA expression was not increased in GBP when compared to sham-operated rats.

Conclusion

In obese Zucker rats, GBP prevents the increase in orexigenic signals that occur during caloric deprivation. Our data support the hypothesis that sustained weight loss observed after gastric banding does not depend solely on food restriction.

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References

  1. Silventoinen K, Sans S, Tolonen H, et al. Trends in obesity and energy supply in the WHO MONICA Project. Int J Obes Relat Metab Disord 2004;28:710–8.

    Article  PubMed  CAS  Google Scholar 

  2. do Carmo I, dos Santos O, Camolas J, et al. Prevalence of obesity in Portugal. Obes Rev 2006;7:233–7.

    Article  PubMed  Google Scholar 

  3. Schneider BE, Mun EC. Surgical management of morbid obesity. Diabetes Care 2005;28:475–80.

    Article  PubMed  Google Scholar 

  4. Kushner R. Diets, drugs, exercise, and behavioral modification: where these work and where they do not. Surg Obes Relat Dis 2005;1:120–2.

    Article  PubMed  Google Scholar 

  5. Martin LF, Tan TL, Horn JR, et al. Comparison of the costs associated with medical and surgical treatment of obesity. Surgery 1995;118:599–606.

    Article  PubMed  CAS  Google Scholar 

  6. Halmi KA, Mason E, Falk JR, et al. Appetitive behavior after gastric bypass for obesity. Int J Obes 1981;5:457–64.

    PubMed  CAS  Google Scholar 

  7. Dixon AF, Dixon JB, O’Brien PE. Laparoscopic adjustable gastric banding induces prolonged satiety: a randomized blind crossover study. J Clin Endocrinol Metab 2005;90:813–9.

    Article  PubMed  CAS  Google Scholar 

  8. Lang T, Hauser R, Buddeberg C, et al. Impact of gastric banding on eating behavior and weight. Obes Surg 2002;12:100–7.

    Article  PubMed  Google Scholar 

  9. Schindler K, Prager G, Ballaban T, et al. Impact of laparoscopic adjustable gastric banding on plasma ghrelin, eating behaviour and body weight. Eur J Clin Invest 2004;34:549–54.

    Article  PubMed  CAS  Google Scholar 

  10. Korner J, Inabnet W, Conwell IM, et al. Differential effects of gastric bypass and banding on circulating gut hormone and leptin levels. Obesity (Silver Spring) 2006;14:1553–61.

    CAS  Google Scholar 

  11. Flancbaum L, Choban PS, Bradley LR, et al. Changes in measured resting energy expenditure after Roux-en-Y gastric bypass for clinically severe obesity. Surgery 1997;122:943–9.

    Article  PubMed  CAS  Google Scholar 

  12. Galtier F, Farret A, Verdier R, et al. Resting energy expenditure and fuel metabolism following laparoscopic adjustable gastric banding in severely obese women: relationships with excess weight lost. Int J Obes (Lond) 2006;30:1104–10.

    Article  CAS  Google Scholar 

  13. Benedetti G, Mingrone G, Marcoccia S, et al. Body composition and energy expenditure after weight loss following bariatric surgery. J Am Coll Nutr 2000;19:270–4.

    PubMed  CAS  Google Scholar 

  14. Cummings DE, Weigle DS, Frayo RS, et al. Plasma ghrelin levels after diet-induced weight loss or gastric bypass surgery. N Engl J Med 2002;346(21):1623–30.

    Article  PubMed  Google Scholar 

  15. le Roux CW, Aylwin SJ, Batterham RL, et al. Gut hormone profiles following bariatric surgery favor an anorectic state, facilitate weight loss, and improve metabolic parameters. Ann Surg 2006;243:108–14.

    Article  PubMed  Google Scholar 

  16. Fruhbeck G, Rotellar F, Hernandez-Lizoain JL, et al. Fasting plasma ghrelin concentrations 6 months after gastric bypass are not determined by weight loss or changes in insulinemia. Obes Surg 2004;14:1208–15.

    Article  PubMed  Google Scholar 

  17. Hanusch-Enserer U, Cauza E, Brabant G, et al. Plasma ghrelin in obesity before and after weight loss after laparoscopical adjustable gastric banding. J Clin Endocrinol Metab 2004;89:3352–8.

    Article  PubMed  CAS  Google Scholar 

  18. Langer FB, Reza Hoda MA, Bohdjalian A, et al. Sleeve gastrectomy and gastric banding: effects on plasma ghrelin levels. Obes Surg 2005;15:1024–9.

    Article  PubMed  CAS  Google Scholar 

  19. Mariani LM, Fusco A, Turriziani M, et al. Transient increase of plasma ghrelin after laparoscopic adjustable gastric banding in morbid obesity. Horm Metab Res 2005;37:242–5.

    Article  PubMed  CAS  Google Scholar 

  20. da Silva BA, Bjorbaek C, Uotani S, et al. Functional properties of leptin receptor isoforms containing the gln→pro extracellular domain mutation of the fatty rat. Endocrinology 1998;139:3681–90.

    Article  PubMed  Google Scholar 

  21. Wang T, Hartzell DL, Flatt WP, et al. Responses of lean and obese Zucker rats to centrally administered leptin. Physiol Behav 1998;65:333–41.

    Article  PubMed  CAS  Google Scholar 

  22. Yamashita T, Murakami T, Iida M, et al. Leptin receptor of Zucker fatty rat performs reduced signal transduction. Diabetes 1997;46:1077–80.

    Article  PubMed  CAS  Google Scholar 

  23. Farooqi IS, Wangensteen T, Collins S, et al. Clinical and molecular genetic spectrum of congenital deficiency of the leptin receptor. N Engl J Med 2007;356:237–47.

    Article  PubMed  CAS  Google Scholar 

  24. Halaas JL, Gajiwala KS, Maffei M, et al. Weight-reducing effects of the plasma protein encoded by the obese gene. Science 1995;269:543–6.

    Article  PubMed  CAS  Google Scholar 

  25. Oberkofler H, Beer A, Breban D, et al. Human obese gene expression: alternative splicing of mRNA and relation to adipose tissue localization. Obes Surg 1997;7:390–6.

    Article  PubMed  CAS  Google Scholar 

  26. Prolo P, Wong ML, Licinio J. Leptin. Int J Biochem Cell Biol 1998;30:1285–90.

    Article  PubMed  CAS  Google Scholar 

  27. Monteiro MP, Monteiro JD, Aguas AP, et al. Rats submitted to gastric banding are leaner and show distinctive feeding patterns. Obes Surg 2006;16:597–602.

    Article  PubMed  Google Scholar 

  28. Monteiro MP, Monteiro JD, Aguas AP, et al. A rat model of restrictive bariatric surgery with gastric banding. Obes Surg 2006;16:48–51.

    Article  PubMed  Google Scholar 

  29. Asakawa A, Inui A, Kaga T, et al. Antagonism of ghrelin receptor reduces food intake and body weight gain in mice. Gut 2003;52:947–52.

    Article  PubMed  CAS  Google Scholar 

  30. Small CJ, Liu YL, Stanley SA, et al. Chronic CNS administration of agouti-related protein (Agrp) reduces energy expenditure. Int J Obes Relat Metab Disord 2003;27:530–3.

    Article  PubMed  CAS  Google Scholar 

  31. Hansen TK, Dall R, Hosoda H, et al. Weight loss increases circulating levels of ghrelin in human obesity. Clin Endocrinol (Oxf) 2002;56:203–6.

    Article  CAS  Google Scholar 

  32. Brown LM, Benoit SC, Woods SC, et al. Intraventricular (i3vt) ghrelin increases food intake in fatty Zucker rats. Peptides 2007;28:612–6.

    Article  PubMed  CAS  Google Scholar 

  33. Beck B, Max JP, Fernette B, et al. Adaptation of ghrelin levels to limit body weight gain in the obese Zucker rat. Biochem Biophys Res Commun 2004;318:846–51.

    Article  PubMed  CAS  Google Scholar 

  34. Ariyasu H, Takaya K, Hosoda H, et al. Delayed short-term secretory regulation of ghrelin in obese animals: evidenced by a specific RIA for the active form of ghrelin. Endocrinology 2002;143:3341–50.

    Article  PubMed  CAS  Google Scholar 

  35. Beck B, Richy S, Stricker-Krongrad A. Feeding response to ghrelin agonist and antagonist in lean and obese Zucker rats. Life Sci 2004;76:473–8.

    Article  PubMed  CAS  Google Scholar 

  36. Tovar SA, Seoane LM, Caminos JE, et al. Regulation of peptide YY levels by age, hormonal, and nutritional status. Obes Res 2004;12:1944–50.

    PubMed  CAS  Google Scholar 

  37. Hewson AK, Tung LY, Connell DW, et al. The rat arcuate nucleus integrates peripheral signals provided by leptin, insulin, and a ghrelin mimetic. Diabetes 2002;51:3412–9.

    Article  PubMed  CAS  Google Scholar 

  38. Nijhuis J, van Dielen FM, Buurman WA, et al. Ghrelin, leptin and insulin levels after restrictive surgery: a 2-year follow-up study. Obes Surg 2004;14:783–7.

    Article  PubMed  Google Scholar 

  39. Foschi D, Corsi F, Rizzi A, et al. Vertical banded gastroplasty modifies plasma ghrelin secretion in obese patients. Obes Surg 2005;15:1129–32.

    Article  PubMed  CAS  Google Scholar 

  40. Stoeckli R, Chanda R, Langer I, et al. Changes of body weight and plasma ghrelin levels after gastric banding and gastric bypass. Obes Res 2004;12:346–50.

    Article  PubMed  CAS  Google Scholar 

  41. Ram E, Vishne T, Diker D, et al. Impact of gastric banding on plasma ghrelin, growth hormone, cortisol, DHEA and DHEA-S levels. Obes Surg 2005;15:1118–23.

    Article  PubMed  Google Scholar 

  42. Hanusch-Enserer U, Brabant G, Roden M. Ghrelin concentrations in morbidly obese patients after adjustable gastric banding. N Engl J Med 2003;348:2159–60.

    Article  PubMed  Google Scholar 

  43. Rodriquez de Fonseca F, Navarro M, Alvarez E, et al. Peripheral versus central effects of glucagon-like peptide-1 receptor agonists on satiety and body weight loss in Zucker obese rats. Metabolism 2000;49:709–17.

    Article  PubMed  CAS  Google Scholar 

  44. Stylopoulos N, Davis P, Pettit JD, et al. Changes in serum ghrelin predict weight loss after Roux-en-Y gastric bypass in rats. Surg Endosc 2005;19:942–6.

    Article  PubMed  CAS  Google Scholar 

  45. Pittner RA, Moore CX, Bhavsar SP, et al. Effects of PYY[3-36] in rodent models of diabetes and obesity. Int J Obes Relat Metab Disord 2004;28:963–71.

    Article  PubMed  CAS  Google Scholar 

  46. Alvarez Bartolome M, Borque M, Martinez-Sarmiento J, et al. Peptide YY secretion in morbidly obese patients before and after vertical banded gastroplasty. Obes Surg 2002;12:324–7.

    Article  PubMed  Google Scholar 

  47. Korner J, Bessler M, Cirilo LJ, et al. Effects of Roux-en-Y gastric bypass surgery on fasting and postprandial concentrations of plasma ghrelin, peptide YY, and insulin. J Clin Endocrinol Metab 2005;90:359–65.

    Article  PubMed  CAS  Google Scholar 

  48. Valverde I, Puente J, Martin-Duce A, et al. Changes in glucagon-like peptide-1 (GLP-1) secretion after biliopancreatic diversion or vertical banded gastroplasty in obese subjects. Obes Surg 2005;15:387–97.

    Article  PubMed  Google Scholar 

  49. Kalra SP, Dube MG, Sahu A, et al. Neuropeptide Y secretion increases in the paraventricular nucleus in association with increased appetite for food. PNAS 1991;88:10931–5.

    Article  PubMed  CAS  Google Scholar 

  50. Lewis DE, Shellard L, Koeslag DG, et al. Intense exercise and food restriction cause similar hypothalamic neuropeptide Y increases in rats. Am J Physiol 1993;264:E279–84.

    PubMed  CAS  Google Scholar 

  51. McKibbin PE, Cotton SJ, McMillan S, et al. Altered neuropeptide Y concentrations in specific hypothalamic regions of obese (fa/fa) Zucker rats. Possible relationship to obesity and neuroendocrine disturbances. Diabetes 1991;40:1423–9.

    Article  PubMed  CAS  Google Scholar 

  52. Beck B, Richy S, Stricker-Krongrad A. Ghrelin and body weight regulation in the obese Zucker rat in relation to feeding state and dark/light cycle. Exp Biol Med (Maywood) 2003;228:1124–31.

    CAS  Google Scholar 

  53. Sanacora G, Kershaw M, Finkelstein JA, et al. Increased hypothalamic content of preproneuropeptide Y messenger ribonucleic acid in genetically obese Zucker rats and its regulation by food deprivation. Endocrinology 1990;127:730–7.

    Article  PubMed  CAS  Google Scholar 

  54. Korner J, Savontaus E, Chua SC Jr, et al. Leptin regulation of Agrp and Npy mRNA in the rat hypothalamus. J Neuroendocrinol 2001;13:959–66.

    Article  PubMed  CAS  Google Scholar 

  55. Quinn R. Comparing rat’s to human’s age: how old is my rat in people years? Nutrition 2005;21:775–7.

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors are very grateful to Antonio Sergio, MD, a surgical expert in human gastric banding for the technical advice regarding how to perform bariatric surgery.

UMIB work is funded by grants from FCT (POCTI/FEDER), Portugal.

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Authors and Affiliations

  1. Department of Anatomy and UMIB (Unit for Multidisciplinary Biomedical Research) of ICBAS (Abel Salazar Institute for the Biomedical Sciences), University of Porto, 4099-003, Porto, Portugal

    Mariana P. Monteiro, Andreia H. Ribeiro, J. Duarte Monteiro & Artur P. Águas

  2. Instituto de Biologia Molecular e Celular-IBMC, University of Porto, 4099-003, Porto, Portugal

    Ana F. Nunes & Mónica M. Sousa

  3. Division of Endocrinology of Santo Antonio General Hospital and Molecular Neurobiology, University of Porto, 4099-003, Porto, Portugal

    M. Helena Cardoso

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  1. Mariana P. Monteiro
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  5. J. Duarte Monteiro
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Correspondence to Mariana P. Monteiro.

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Monteiro, M.P., Ribeiro, A.H., Nunes, A.F. et al. Increase in Ghrelin Levels After Weight Loss in Obese Zucker Rats is Prevented by Gastric Banding. OBES SURG 17, 1599–1607 (2007). https://doi.org/10.1007/s11695-007-9324-7

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  • DOI: https://doi.org/10.1007/s11695-007-9324-7

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