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Imbalance of Hormones Involved in Energy Balance Regulation in Obese Patients: a Study of Its Relationship with Disturbed Eating Behavior and Abnormal Metabolic Parameters

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Abstract

In healthy people, postprandial status is characterized by a particular dynamics of the level of hormones involved in the regulation of eating behavior and energy balance. However, data obtained from obese patients are heterogeneous. The aim of this work was to study the pattern of dynamic changes in the level of hormones—leptin, ghrelin, glucagon-like peptide 1 (GLP-1), glucose-dependent insulinotropic peptide (GIP)—and to elucidate their relationship with factors characterizing metabolic status and eating behavior. Sixty six obese patients (12 men and 54 women, mean age 37.8 ± 10.8 years, mean body weight 105.2 ± 16.7 kg, body mass index (BMI) 37.3 ± 4.8 kg/m2) were included in the study. All patients underwent anthropometric examination and had their blood pressure, as well as parameters of carbohydrate and lipid metabolism, determined. Hormone levels (leptin, GIP, GLP-1, ghrelin) were assessed fasting and 60 min after a standard breakfast containing 60 g of carbohydrates. It was found that different obese patients demonstrated multidirectional changes in the study hormone levels. Some patients retained the dynamics typical for healthy people, while the majority exhibited a decrease in postprandial peaks (GLP-1 in 48.2%, GIP in 50% of patients), or an abnormal dynamics (no decrease in postprandial ghrelin levels in 60.8%, no increase in postprandial leptin levels in 83.3%). The abnormal postprandial dynamics of hormone levels was associated with more pronounced changes in parameters corresponding to the metabolically unhealthy obesity (elevated glucose and triglyceride levels, increased HOMA-IR index) and disturbed eating behavior. The postprandial dynamics of hormones involved in the regulation of appetite and energy balance suggests the presence of different subtypes of obesity. Those subtypes, which probably reflect the resistance to these hormones and/or their deficiency developing in obesity, are characterized by the worse characteristics of metabolic health.

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REFERENCES

  1. Kemps E, Herman CP, Hollitt S, Polivy J, Prichard I, Tiggemann M (2016) The role of expectations in the effect of food cue exposure on intake. Appetite 103: 259–264. https://doi.org/10.1016/j.appet.2016.04.026

    Article  PubMed  Google Scholar 

  2. Travagli RA, Anselmi L (2016) Vagal neurocircuitry and its influence on gastric motility. Nat Rev Gastroenterol Hepatol 13(7): 389–401. https://doi.org/10.1038/nrgastro.2016.76

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Tichonenko EV, Tsoi UA, Vasilieva EY, Babenko AYu (2018) Characteristics of eating behavior and the level of hormones regulating the appetite in patients with type 2 diabetes mellitus and body mass index more than 35 kg/m2. Obesity and metabolism 15(1): 30–38. https://doi.org/10.14341/omet2018130-38

    Article  Google Scholar 

  4. Klok MD, Jakobsdottir S, Drent ML (2007) The role of leptin and ghrelin in the regulation of food intake and body weight in humans: a review. Obes Rev 8(1): 21–34. https://doi.org/10.1111/j.1467-789X.2006.00270.x

    Article  CAS  PubMed  Google Scholar 

  5. Monteleone P, Martiadis V, Fabrazzo M, Serritella C, Maj M (2003) Ghrelin and leptin responses to food ingestion in bulimia nervosa: implications for binge-eating and compensatory behaviours. Psychol Med 33(8): 1387–1394. https://doi.org/10.1017/s0033291703008316

    Article  CAS  PubMed  Google Scholar 

  6. Adamska-Patruno E, Ostrowska L, Goscik J, Fiedorczuk J, Moroz M, Kretowski A, Gorska M (2019) The Differences in Postprandial Serum Concentrations of Peptides That Regulate Satiety/Hunger and Metabolism after Various Meal Intake, in Men with Normal vs. Excessive BMI. Nutrients 11(3): 493. https://doi.org/10.3390/nu11030493

    Article  CAS  PubMed Central  Google Scholar 

  7. Larsen MA, Isaksen VT, Paulssen EJ, Goll R, Florholmen JR (2019) Postprandial leptin and adiponectin in response to sugar and fat in obese and normal weight individuals. Endocrine 66(3): 517–525. https://doi.org/10.1007/s12020-019-02102-9

    Article  CAS  PubMed  Google Scholar 

  8. Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H, Kangawa K (1999) Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 402(6762): 656–660. https://doi.org/10.1038/45230

    Article  CAS  PubMed  Google Scholar 

  9. Williams DL, Cummings DE (2005) Regulation of ghrelin in physiologic and pathophysiologic states. J Nutr 135(5): 1320–1325. https://doi.org/10.1093/jn/135.5.1320

    Article  CAS  PubMed  Google Scholar 

  10. Zwirska-Korczala K, Konturek SJ, Sodowski M, Wylezol M, Kuka D, Sowa P, Adamczyk-Sowa M, Kukla M, Berdowska A, Rehfeld JF, Bielanski W, Brzozowski T (2007) Basal and postprandial plasma levels of PYY, ghrelin, cholecystokinin, gastrin and insulin in women with moderate and morbid obesity and metabolic syndrome. J Physiol Pharmacol 58 (Suppl 1): 13–35.

    PubMed  Google Scholar 

  11. McLaughlin T, Abbasi F, Lamendola C, Frayo RS, Cummings DE (2004) Plasma ghrelin concentrations are decreased in insulin-resistant obese adults relative to equally obese insulin-sensitive controls. J Clin Endocrinol Metab 89(4): 1630–1635. https://doi.org/10.1210/jc.2003-031572

    Article  CAS  PubMed  Google Scholar 

  12. Callahan HS, Cummings DE, Pepe MS, Breen PA, Matthys CC, Weigle DS (2004) Postprandial suppression of plasma ghrelin level is proportional to ingested caloric load but does not predict intermeal interval in humans. J Clin Endocrinol Metab 89(3): 1319–1324. https://doi.org/10.1210/jc.2003-031267

    Article  CAS  PubMed  Google Scholar 

  13. Holst JJ, Deacon CF (2005) Glucagon-like peptide-1 mediates the therapeutic actions of DPP-IV inhibitors. Diabetologia 48(4): 612–615. https://doi.org/10.1007/s00125-005-1705-7

    Article  CAS  PubMed  Google Scholar 

  14. Spreckley E, Murphy KG (2015) The L-Cell in Nutritional Sensing and the Regulation of Appetite. Front Nutr 2: 23. https://doi.org/10.3389/fnut.2015.00023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Hagemann D, Holst JJ, Gethmann A, Banasch M, Schmidt WE, Meier JJ (2007) Glucagon-like peptide 1 (GLP-1) suppresses ghrelin levels in humans via increased insulin secretion. Regul Pept 143(1–3): 64–68. https://doi.org/10.1016/j.regpep.2007.03.002

    Article  CAS  PubMed  Google Scholar 

  16. Hong X, Zhang H, Liang H, Li D, Huang J, Li Z, Jiang S, Zhang W, Xu G (2016) Exendin-4 decreases ghrelin levels through mTOR signaling. Mol Cell Endocrinol 437: 201–212. https://doi.org/10.1016/j.mce.2016.08.039

    Article  CAS  PubMed  Google Scholar 

  17. Clemmensen C, Chabenne J, Finan B, Sullivan L, Fischer K, Küchler D, Sehrer L, Ograjsek T, Hofmann SM, Schriever SC, Pfluger PT, Pinkstaff J, Tschöp MH, Dimarchi R, Müller TD (2014) GLP-1/glucagon coagonism restores leptin responsiveness in obese mice chronically maintained on an obesogenic diet. Diabetes 63(4): 1422–1427. https://doi.org/ 10.2337/db13-1609

    Article  CAS  PubMed  Google Scholar 

  18. Iepsen EW, Lundgren J, Dirksen C, Jensen JE, Pedersen O, Hansen T, Madsbad S, Holst JJ, Torekov SS (2014) Treatment with a GLP-1 receptor agonist diminishes the decrease in free plasma leptin during maintenance of weight loss. Int J Obes (Lond) 39(5): 834–841. https://doi.org/10.1038/ijo.2014.177

  19. Shestakova EA, Il’in AV, Shestakova MV, Dedov II (2015) Glucose-dependent insulinotropic polypeptide—a new link in the development of obesity. Obesity and metabolism 12(1): 16–19. https://doi.org/10.14341/omet2015116-19

    Article  Google Scholar 

  20. Simpson KA, Martin NM, Bloom SR (2008) Hypothalamic regulation of appetite. Expert Rev Endocrinol Metab 3(5): 577–592. https://doi.org/10.1586/17446651.3.5.577

    Article  CAS  PubMed  Google Scholar 

  21. Yamaoka-Tojo M, Tojo T, Takahira N, Matsunaga A, Aoyama N, Masuda T, Izumi T (2010) Elevated circulating levels of an incretin hormone, glucagon-like peptide-1, are associated with metabolic components in high-risk patients with cardiovascular disease. Cardiovasc Diabetol 9: 17. https://doi.org/10.1186/1475-2840-9-17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Finan B, Müller TD, Clemmensen C, Perez-Tilve D, DiMarchi RD, Tschöp MH (2016) Reappraisal of GIP Pharmacology for Metabolic Diseases. Trends Mol Med 22(5): 359–376. https://doi.org/10.1016/j.molmed.2016.03.005

    Article  CAS  PubMed  Google Scholar 

  23. Møller CL, Vistisen D, Færch K, Johansen NB, Witte DR, Jonsson A, Pedersen O, Hansen T, Lauritzen T, Jørgensen ME, Torekov SS, Holst JJ (2016) Glucose-Dependent Insulinotropic Polypeptide Is Associated With Lower Low-Density Lipoprotein But Unhealthy Fat Distribution, Independent of Insulin: The ADDITION-PRO Study. J Clin Endocrinol Metab 101(2): 485–493. https://doi.org/10.1210/jc.2015-3133

    Article  CAS  PubMed  Google Scholar 

  24. Verdich C, Toubro S, Buemann B, Lysgård Madsen J, Juul Holst J, Astrup A (2001) The role of postprandial releases of insulin and incretin hormones in meal-induced satiety—effect of obesity and weight reduction. Int J Obes Relat Metab Disord 25(8): 1206–1214. https://doi.org/ 10.1038/sj.ijo.0801655

    Article  CAS  PubMed  Google Scholar 

  25. Carr RD, Larsen MO, Jelic K, Lindgren O, Vikman J, Holst JJ, Deacon CF, Ahrén B (2009) Secretion and dipeptidyl peptidase-4-mediated metabolism of incretin hormones after a mixed meal or glucose ingestion in obese compared to lean, nondiabetic men. J Clin Endocrinol Metab 95(2): 872–878. https://doi.org/10.1210/jc.2009-2054

    Article  CAS  PubMed  Google Scholar 

  26. Góralska J, Raźny U, Polus A, Dziewońska A, Gruca A, Zdzienicka A, Dembińska-Kieć A, Solnica B, Micek A, Kapusta M, Słowińska-Solnica K, Malczewska-Malec M (2020) Enhanced GIP Secretion in Obesity Is Associated with Biochemical Alteration and miRNA Contribution to the Development of Liver Steatosis. Nutrients 12(2): 476. https://doi.org/10.3390/nu12020476

    Article  CAS  PubMed Central  Google Scholar 

  27. Yamaoka-Tojo M, Tojo T, Takahira N, Matsunaga A, Aoyama N, Masuda T, Izumi T (2010) Elevated circulating levels of an incretin hormone, glucagon-like peptide-1, are associated with metabolic components in high-risk patients with cardiovascular disease. Cardiovasc Diabetol 9: 17. https://doi.org/10.1186/1475-2840-9-17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Ganley RM (1989) Emotion and eating in obesity: A review of the literature. Int J Eat Disord 8 (3): 343–361. https://doi.org/10.1002/1098-108X(198905)8:3<343::AID-EAT2260080310>3.0.CO;2-C

    Article  Google Scholar 

  29. Frayn M, Knäupe B (2018) Emotional Eating and Weight in Adults: a Review. Curr Psychol 37: 924–933. https://doi.org/10.1007/s12144-017-9577-9

    Article  Google Scholar 

  30. López-Guimerà G, Dashti HS, Smith CE, Sánchez-Carracedo D, Ordovas JM (2014) CLOCK 3111 T/C SNP Interacts with Emotional Eating Behavior for Weight-Loss in a Mediterranean Population. PLOS One 9(6): e99152. https://doi.org/10.1371/journal.pone.0099152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Delahanty LM, Peyrot M, Shrader PJ, Williamson DA, Meigs JB, Nathan DM (2013) DPP Research Group. Pretreatment, psychological, and behavioral predictors of weight outcomes among lifestyle intervention participants in the Diabetes Prevention Program (DPP). Diabetes Care 36(1): 34–40. https://doi.org/10.2337/dc12-0733

    Article  PubMed  Google Scholar 

  32. van Ruiten CC, Ten Kulve JS, van Bloemendaal L, Nieuwdorp M, Veltman DJ, IJzerman RG (2022) Eating behavior modulates the sensitivity to the central effects of GLP-1 receptor agonist treatment: a secondary analysis of a randomized trial. Psychoneuroendocrinology137: 105667. https://doi.org/10.1016/j.psyneuen.2022.105667

    Article  CAS  PubMed  Google Scholar 

  33. Canetti L, Berry EM, Elizur Y (2009) Psychosocial predictors of weight loss and psychological adjustment following bariatric surgery and a weight-loss program: the mediating role of emotional eating. Int J Eat Disord 42(2): 109–117. https://doi.org/10.1002/eat.20592

    Article  PubMed  Google Scholar 

  34. Shufen Li, Xi Li (2016) Leptin in normal physiology and leptin resistance, Sci Bull 61(19): 1480–1488. https://doi.org/10.1007/s11434-015-0951-4

  35. Hagemann D, Holst JJ, Gethmann A, Banasch M, Schmidt WE, Meier JJ (2007) Glucagon-like peptide 1 (GLP-1) suppresses ghrelin levels in humans via increased insulin secretion. Regul Pept 143(1–3): 64–68. https://doi.org/10.1016/j.regpep.2007.03.002

    Article  CAS  PubMed  Google Scholar 

  36. Mesgari-Abbasi M, Abbasalizad-Farhangi M (2020) Serum concentrations of cholecystokinin, peptide YY, ghrelin and high sensitive C-reactive protein in association with metabolic syndrome ingredients in obese individuals. Acta Endocrinol (Buchar) 16(1): 37–42. https://doi.org/10.4183/aeb.2020.37

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Funding

This work was supported by the Ministry of Science and Higher Education of the Russian Federation (Agreement no. 075-15-2022-301 of April 20, 2022).

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Conceptualization and experimental design (A.Yu.B.); patient recruiting, data collection and statistical processing (G.A.M.); writing and editing of the manuscript (A.Yu.B., G.A.M.).

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Correspondence to A. Yu. Babenko.

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The authors declare that they have neither evident nor potential conflict of interest related to the publication of this article.

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Translated by A. Polyanovsky

Russian Text © The Author(s), 2022, published in Rossiiskii Fiziologicheskii Zhurnal imeni I.M. Sechenova, 2022, Vol. 108, No. 9, pp. 1159–1174https://doi.org/10.31857/S0869813922090047.

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Babenko, A.Y., Matveev, G.A. Imbalance of Hormones Involved in Energy Balance Regulation in Obese Patients: a Study of Its Relationship with Disturbed Eating Behavior and Abnormal Metabolic Parameters. J Evol Biochem Phys 58, 1491–1502 (2022). https://doi.org/10.1134/S0022093022050192

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