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Post-prandial anorexigenic gut peptide, appetite and glucometabolic responses at different eating rates in obese patients undergoing laparoscopic sleeve gastrectomy

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Abstract

Although different hypotheses have been proposed, the underlying mechanism(s) of the weight loss induced by laparoscopic sleeve gastrectomy (LSG) is still unknown. The aim of this study was to determine whether eating the same meal at different rates (fast vs. slow feeding) evokes different post-prandial anorexigenic gut peptide responses in ten obese patients undergoing LSG. Circulating levels of GLP-1, PYY, glucose, insulin and triglycerides were measured before and 3 months after LSG. Visual analogue scales were used to evaluate the subjective feelings of hunger and satiety. Irrespective of the operative state, either fast or slow feeding did not stimulate GLP-1 release (vs. 0 min); plasma levels of PYY were increased (vs. 0 min) by fast and slow feeding only after LSG. There were no differences in post-prandial levels of GLP-1 when comparing fast to slow feeding or pre-to-post-operative state. Plasma levels of PYY after fast or slow feeding were higher in post, rather than pre-operative state, with no differences when comparing PYY release after fast and slow feeding. Hunger and satiety were decreased and increased, respectively, (vs. 0 min) by food intake. Fast feeding evoked a higher satiety than slow feeding in both pre- and post-operative states, with no differences in hunger. In both pre- and post-operative states, there were similar responses for hunger and satiety after food intake. Finally, LSG improved insulin resistance after either fast or slow feeding. These (negative) findings would suggest a negligible contribution of the anorexigenic gut peptide responses in LSG-induced weight loss.

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References

  1. P. Behary, J. Cegla, T.M. Tan, S.R. Bloom, Obesity: lifestyle management, bariatric surgery, drugs, and the therapeutic exploitation of gut hormones. Postgrad. Med. 127(5), 494–502 (2015)

    Article  PubMed  Google Scholar 

  2. D.S. Hess, D.W. Hess, Biliopancreatic diversion with a duodenal switch. Obes. Surg. 8(3), 267–282 (1998)

    Article  CAS  PubMed  Google Scholar 

  3. A. Baltasar, C. Serra, N. Pérez, R. Bou, M. Bengochea, L. Ferri, Laparoscopic sleeve gastrectomy: a multi-purpose bariatric operation. Obes. Surg. 15(8), 1124–1128 (2005)

    Article  PubMed  Google Scholar 

  4. F.B. Langer, A. Bohdjalian, F.X. Felberbauer, E. Fleischmann, M.A.R. Hoda, B. Ludvik, J. Zacherl, R. Jakesz, G. Prager, Does gastric dilation limit the success of sleeve gastrectomy as a sole operation for morbid obesity? Obes. Surg. 16(2), 166–171 (2006)

    Article  PubMed  Google Scholar 

  5. J. Papailiou, K. Albanopoulos, K.G. Toutouzas, C. Tsigris, N. Nikiteas, G. Zografos, Morbid obesity and sleeve gastrectomy: how does it work? Obes. Surg. 20(10), 1448–1455 (2010)

    Article  PubMed  Google Scholar 

  6. B. Anderson, N.J. Switzer, A. Almamar, X. Shi, D.W. Birch, S. Karmali, The impact of laparoscopic sleeve gastrectomy on plasma ghrelin levels: a systematic review. Obes. Surg. 23(9), 1476–1480 (2013)

    Article  PubMed  Google Scholar 

  7. A. Kokkinos, C.W. le Roux, K. Alexiadou, N. Tentolouris, R.P. Vincent, D. Kyriaki, D. Perrea, M.A. Ghatei, S.R. Bloom, N. Katsilambros, Eating slowly increases the postprandial response of the anorexigenic gut hormones, peptide YY and glucagon-like peptide-1. J. Clin. Endocrinol. Metab. 95(1), 333–337 (2010)

    Article  CAS  PubMed  Google Scholar 

  8. A. De Silva, S.R. Bloom, Gut hormones and appetite control: a focus on PYY and GLP-1 as therapeutic targets in obesity. Gut. Liver. 6(1), 10–20 (2012)

    Article  PubMed  PubMed Central  Google Scholar 

  9. J.H. Ledikwe, J.A. Ello-Martin, B.J. Rolls, Portion sizes and the obesity epidemic. J. Nutr. 135(4), 905–909 (2005)

    CAS  PubMed  Google Scholar 

  10. R. Rising, D.E. Larson, E. Ravussin, Do obese eat faster than lean subjects? Food intake studies in Pima Indian men. Obes. Res. 2(1), 19–23 (1994)

    Article  CAS  PubMed  Google Scholar 

  11. S. Sasaki, A. Katagiri, T. Tsuji, T. Shimoda, K. Amano, Self-reported rate of eating correlates with body mass index in 18-y-old Japanese women. Int. J. Obes. Relat. Metab. Disord. 27(11), 1405–1410 (2003)

    Article  CAS  PubMed  Google Scholar 

  12. C.H. Llewellyn, C.H. van Jaarsveld, D. Boniface, S. Carnell, J. Wardle, Eating rate is a heritable phenotype related to weight in children. Am. J. Clin. Nut. 88(6), 1560–1566 (2008)

    Article  CAS  Google Scholar 

  13. A.E. Rigamonti, F. Agosti, E. Compri, M. Giunta, N. Marazzi, E.E. Muller, S.G. Cella, A. Sartorio, Anorexigenic postprandial responses of PYY and GLP1 to slow ice cream consumption: preservation in obese adolescents, but not in obese adults. Eur. J. Endocrinol. 168(3), 429–436 (2013)

    Article  CAS  PubMed  Google Scholar 

  14. D.M. Garner, M.P. Olmsted, Y. Bohr, P.E. Garfinkel, The eating attitudes test: psychometric features and clinical correlates. Psychol. Med. 12(4), 871–878 (1982)

    Article  CAS  PubMed  Google Scholar 

  15. R.J. Stubbs, D.A. Hughes, A.M. Johnstone, E. Rowley, C. Reid, M. Elia, R. Stratton, H. Delargy, N. King, J.E. Blundell, The use of visual analogue scales to assess motivation to eat in human subjects: a review of their reliability and validity with an evaluation of new hand-held computerized systems for temporal tracking of appetite ratings. Br. J. Nutr. 84(4), 405–415 (2000)

    Article  CAS  PubMed  Google Scholar 

  16. T.E. Adrian, G.L. Ferri, A.J. Bacarese-Hamilton, H.S. Fuessl, J.M. Polak, S.R. Bloom, Human distribution and release of a putative new gut hormone, peptide YY. Gastroenterology. 89(5), 1070–1077 (1985)

    Article  CAS  PubMed  Google Scholar 

  17. M.A. Ghatei, L.O. Uttenthal, M.G. Bryant, N.D. Christofides, A.J. Moody, S.R. Bloom, Molecular forms of glucagon-like immunoreactivity in porcine intestine and pancreas. Endocrinology. 112(3), 917–923 (1983)

    Article  CAS  PubMed  Google Scholar 

  18. C. Orskov, L. Rabenhøj, A. Wettergren, H. Kofod, J.J. Holst, Tissue and plasma concentrations of amidated and glycine-extended glucagon-like peptide I in humans. Diabetes. 43(4), 535–539 (1994)

    Article  CAS  PubMed  Google Scholar 

  19. M. Gutniak, C. Orskov, J.J. Holst, B. Ahrén, S. Efendic, Antidiabetogenic effect of glucagon-like peptide-1 (7-36)amide in normal subjects and patients with diabetes mellitus. N. Engl. J. Med. 326(20), 1316–1322 (1992)

    Article  CAS  PubMed  Google Scholar 

  20. B. Willms, J. Werner, J.J. Holst, C. Orskov, W. Creutzfeldt, M.A. Nauck, Gastric emptying, glucose responses, and insulin secretion after a liquid test meal: effects of exogenous glucagon-like peptide-1 (GLP-1)-(7-36) amide in type 2 (noninsulin-dependent) diabetic patients. J. Clin. Endocrinol. Metab. 81(1), 327–332 (1996)

    CAS  PubMed  Google Scholar 

  21. R.L. Batterham, M.A. Cowley, C.J. Small, H. Herzog, M.A. Cohen, C.L. Dakin, A.M. Wren, A.E. Brynes, M.J. Low, M.A. Ghatei, R.D. Cone, S.R. Bloom, Gut hormone PYY(3-36) physiologically inhibits food intake. Nature. 418(6898), 650–654 (2002)

    Article  CAS  PubMed  Google Scholar 

  22. R.L. Batterham, M.A. Cohen, S.M. Ellis, C.W. Le Roux, D.J. Withers, G.S. Frost, M.A. Ghatei, S.R. Bloom, Inhibition of food intake in obese subjects by peptide YY3-36. N. Engl. J. Med. 349(10), 941–948 (2003)

    Article  CAS  PubMed  Google Scholar 

  23. C.R. Abbott, M. Monteiro, C.J. Small, A. Sajedi, K.L. Smith, J.R. Parkinson, M.A. Ghatei, S.R. Bloom, The inhibitory effects of peripheral administration of peptide YY(3-36) and glucagon-like peptide-1 on food intake are attenuated by ablation of the vagalbrainstem-hypothalamic pathway. Brain. Res. 1044(1), 127–131 (2005)

    Article  CAS  PubMed  Google Scholar 

  24. J.E. Blevins, P.K. Chelikani, A.C. Haver, R.D. Reidelberger, PYY(3-36) induces Fos in the arcuate nucleus and in both catecholaminergic and non-catecholaminergic neurons in the nucleus tractus solitarius of rats. Peptides. 29(1), 112–119 (2008)

    Article  CAS  PubMed  Google Scholar 

  25. K. Michalakis, C. le Roux, Gut hormones and leptin: impact on energy control and changes after bariatric surgery–what the future holds. Obes. Surg. 22(10), 1648–1657 (2012)

    Article  PubMed  Google Scholar 

  26. S. Oesch, C. Rüegg, B. Fischer, L. Degen, C. Beglinger, Effect of gastric distension prior to eating on food intake and feelings of satiety in humans. Physiol. Behav. 87(5), 903–910 (2006)

    Article  CAS  PubMed  Google Scholar 

  27. G.H. Ballantyne, Peptide YY(1-36) and peptide YY(3-36): part I. Distribution, release and actions. Obes. Surg. 16(5), 651–658 (2006)

    Article  PubMed  Google Scholar 

  28. E. Dimitriadis, M. Daskalakis, M. Kampa, A. Peppe, J.A. Papadakis, J. Melissas, Alterations in gut hormones after laparoscopic sleeve gastrectomy: a prospective clinical and laboratory investigational study. Ann. Surg. 257(4), 647–654 (2013)

    Article  PubMed  Google Scholar 

  29. J.J. Holst, The physiology of glucagon-like peptide 1. Physiol. Rev. 87(4), 1409–1439 (2007)

    Article  CAS  PubMed  Google Scholar 

  30. J. Schirra, M. Katschinski, C. Weidmann, T. Schäfer, U. Wank, R. Arnold, B. Göke, Gastric emptying and release of incretin hormones after glucose ingestion in humans. J. Clin. Invest. 97(1), 92–103 (1996)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. A. Patriti, E. Facchiano, N. Gullà, M.C. Aisa, C. Annetti, Gut hormone profiles following bariatric surgery favor an anorectic state, facilitate weight loss, and improve metabolic parameters. Ann. Surg. 245(1), 157–158 (2007)

    Article  PubMed  PubMed Central  Google Scholar 

  32. J. Melissas, S. Koukouraki, J. Askoxylakis, M. Stathaki, M. Daskalakis, K. Perisinakis, N. Karkavitsas, Sleeve gastrectomy: a restrictive procedure? Obes. Surg. 17(1), 57–62 (2007)

    Article  PubMed  Google Scholar 

  33. A. Raben, A. Tagliabue, A. Astrup, The reproducibility of subjective appetite scores. Br. J. Nutr. 73(4), 517–530 (1995)

    Article  CAS  PubMed  Google Scholar 

  34. J.M. Cho, H.J. Kim, E.L. Menzo, S. Park, S. Szomstein, R.J. Rosenthal, Effect of sleeve gastrectomy on type 2 diabetes as an alternative treatment modality to Roux-en-Y gastric bypass: systemic review and meta-analysis. Surg. Obes. Relat. Dis. S1550–7289(15), 00056–00058 (2015)

    Google Scholar 

  35. S.N. Karamanakos, K. Vagenas, F. Kalfarentzos, T.K. Alexandrides. 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. 247(3), 401–407 (2008)

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors wish to thank students from the School of Medicine, University of Milan Bicocca, Monza, Italy, and the dieticians and the nursing staff working at the Division of Internal Medicine, San Gerardo Hospital, University of Milan Bicocca, Monza, Italy, for their skilful assistance during the execution of the experiments.

Authors’ contributions

Antonello E Rigamonti, Angela I Pincelli and Alessandro Sartorio designed the study and wrote the clinical protocol. Angela I Pincelli, Maria Cristina Rocco, Mario Perotti and Maria Grazia Crippa enrolled the subjects and performed the experiments together with Silvia Bini and Vincenzo Cimino. Surgical evaluation and laparascopic sleeve gastrectomy were performed by Diego Massimini and Vittorio Giardini. Silvia Bini, Antonella Saluzzi and Vincenzo Cimino elaborated the database and, together with Marco Casati, performed the analysis of all biochemical parameters. Antonello E Rigamonti analysed data and, together with Angela I Pincelli and Alessandro Sartorio, wrote the manuscript. Silvia Bini and Nicoletta Marazzi contributed to data interpretation and discussion writing. All Authors contributed to the manuscript revision.

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Correspondence to Antonello Emilio Rigamonti.

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The authors declare that there is no conflict of interest that could be perceived as prejudicing the impartiality of the research reported.

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All procedures performed in the present study involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments.

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The study was partially supported by Progetti di Ricerca Corrente, Istituto Auxologico Italiano, IRCCS, Milan, Italy.

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Informed consent was obtained from all individual participants included in the study.

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Rigamonti, A.E., Bini, S., Rocco, M.C. et al. Post-prandial anorexigenic gut peptide, appetite and glucometabolic responses at different eating rates in obese patients undergoing laparoscopic sleeve gastrectomy. Endocrine 55, 113–123 (2017). https://doi.org/10.1007/s12020-016-0933-6

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  • DOI: https://doi.org/10.1007/s12020-016-0933-6

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