Advertisement

Obesity Surgery

, Volume 19, Issue 10, pp 1424–1429 | Cite as

Dissociation of Thyrotropin and Leptin Secretion in Acute Surgical Stress in Severely Obese Patients

  • Marina MichalakiEmail author
  • Apostolos G. Vagenakis
  • Marianna Argentou
  • Panagiotis Mylonas
  • Fotis Kalfarentzos
  • Venetsana Kyriazopoulou
Clinical Research
  • 120 Downloads

Abstract

Background

During illness, thyroid parameters undergo acute changes, which are known as non-thyroidal illness syndrome, the cause of which has not been elucidated. In vitro and in vivo data demonstrate that leptin regulates the expression of thyrotropin-releasing hormone (TRH)—mRNA in the paraventricular nucleus as well as the secretion of thyrotropin (TSH) in response to fasting in humans and animals. Moreover, in healthy adults, TSH and leptin have almost identical circadian rhythms. Our aim was to investigate the secretion of leptin and TSH, and their probable interaction, during the acute stress that is induced by surgery.

Methods

We studied 18 severely obese but otherwise healthy men. All participants were admitted to the hospital in the morning after an overnight fast. On the following day, 14 of the participants underwent bariatric surgery at 0900. The remaining four participants did not undergo surgery and served as controls. Serum samples to measure the levels of TSH and leptin were collected from all participants, as follows: upon admission to the hospital (baseline values) and on the following day at 0900 and every 10 min, thereafter for 9 h.

Results

The serum TSH increased during the first hour after skin incision (si) and then decreased gradually throughout the rest of the observation period. In contrast, during the first hour after si, the leptin levels remained unaltered. The leptin levels then decreased and reached a nadir at 4 h and 10 min post si after which they remained constant for approximately 1 h. Thereafter, while TSH continued to decrease, leptin started to increase and reached baseline values at 9 h post si. In control subjects, the TSH and leptin profiles seemed parallel each other.

Conclusions

During acute surgical stress, the secretion of TSH and leptin in severely obese men is asynchronous and causality could not be proven.

Keywords

TSH Leptin Severe obesity Surgery Non-thyroidal illness syndrome Acute stress 

References

  1. 1.
    Van den Berghe G, de Zegher F, Bouillon R. Clinical review 95: acute and prolonged critical illness as different neuroendocrine paradigms. J Clin Endocrinol Metab. 1998;83:1827–34.PubMedGoogle Scholar
  2. 2.
    Kaptein EM, Grieb DA, Spencer CA, et al. Thyroxine metabolism in the low thyroxine state of critical nonthyroidal illnesses. J Clin Endocrinol Metab. 1981;53:764–71.CrossRefGoogle Scholar
  3. 3.
    Adler SM, Wartofsky L. The nonthyroidal illness syndrome. Endocrinol Metab Clin North Am. 2007;36:657–72.CrossRefGoogle Scholar
  4. 4.
    Romijn JA, Wiersinga WM. Decreased nocturnal surge of thyrotropin in nonthyroidal illness. J Clin Endocrinol Metab. 1990;70:35–42.CrossRefGoogle Scholar
  5. 5.
    Michalaki M, Vagenakis AG, Makri M, et al. Dissociation of the early decline in serum T(3) concentration and serum IL-6 rise and TNFalpha in nonthyroidal illness syndrome induced by abdominal surgery. J Clin Endocrinol Metab. 2001;86:4198–205.PubMedGoogle Scholar
  6. 6.
    Fekete C, Lechan RM. Negative feedback regulation of hypophysiotropic thyrotropin-releasing hormone (TRH) synthesizing neurons: role of neuronal afferents and type 2 deiodinase. Front Neuroendocrinol. 2007;28:97–114.CrossRefGoogle Scholar
  7. 7.
    Fliers E, Alkemade A, Wiersinga WM, et al. Hypothalamic thyroid hormone feedback in health and disease. Prog Brain Res. 2006;153:189–207.CrossRefGoogle Scholar
  8. 8.
    Blake NG, Eckland DJ, Foster OJ, et al. Inhibition of hypothalamic thyrotropin-releasing hormone messenger ribonucleic acid during food deprivation. Endocrinology. 1991;129:2714–8.CrossRefGoogle Scholar
  9. 9.
    Arancibia S, Rage F, Astier H, et al. Neuroendocrine and autonomous mechanisms underlying thermoregulation in cold environment. Neuroendocrinology. 1996;64:257–67.CrossRefGoogle Scholar
  10. 10.
    Boelen A, Wiersinga WM, Fliers E. Fasting-induced changes in the hypothalamus–pituitary–thyroid axis. Thyroid. 2008;18:123–9.CrossRefGoogle Scholar
  11. 11.
    Mantzoros CS, Ozata M, Negrao A, et al. Synchronicity of frequently sampled thyrotropin (TSH) and leptin concentrations in healthy adults and leptin-deficient subjects: evidence for possible partial TSH regulation by leptin in humans. J Clin Endocrinol Metab. 2001;86:3284–91.CrossRefGoogle Scholar
  12. 12.
    Bornstein SR. Is leptin a stress related peptide? Nat Med. 1997;3:937.CrossRefGoogle Scholar
  13. 13.
    Ahima RS, Prabakaran D, Mantzoros C, et al. Role of leptin in the neuroendocrine response to fasting. Nature. 1996;382:250–2.CrossRefGoogle Scholar
  14. 14.
    Licinio J, Mantzoros C, Negrao AB, et al. Human leptin levels are pulsatile and inversely related to pituitary–adrenal function. Nat Med. 1997;3:575–9.CrossRefGoogle Scholar
  15. 15.
    Kain ZN, Zimolo Z, Heninger G. Leptin and the perioperative neuroendocrinological stress response. J Clin Endocrinol Metab. 1999;84:2438–42.PubMedGoogle Scholar
  16. 16.
    Harris M, Aschkenasi C, Elias CF, et al. Transcriptional regulation of the thyrotropin-releasing hormone gene by leptin and melanocortin signaling. J Clin Invest. 2001;107:111–20.CrossRefGoogle Scholar
  17. 17.
    Nillni EA, Vaslet C, Harris M, et al. Leptin regulates prothyrotropin-releasing hormone biosynthesis. Evidence for direct and indirect pathways. J Biol Chem. 2000;275:36124–33.CrossRefGoogle Scholar
  18. 18.
    Fekete C, Singru PS, Sanchez E, et al. Differential effects of central leptin, insulin, or glucose administration during fasting on the hypothalamic-pituitary-thyroid axis and feeding-related neurons in the arcuate nucleus. Endocrinology. 2006;147:520–9.CrossRefGoogle Scholar
  19. 19.
    Morton GJ, Cummings DE, Baskin DG, et al. Central nervous system control of food intake and body weight. Nature. 2006;443:289–95.CrossRefGoogle Scholar
  20. 20.
    Legradi G, Emerson CH, Ahima RS, et al. Leptin prevents fasting-induced suppression of prothyrotropin-releasing hormone messenger ribonucleic acid in neurons of the hypothalamic paraventricular nucleus. Endocrinology. 1997;138:2569–76.CrossRefGoogle Scholar
  21. 21.
    Cho YM, Kim MS, Shin CS, et al. Dynamic change in plasma leptin level during the perioperative period. Horm Res. 2003;59:100–4.PubMedGoogle Scholar
  22. 22.
    Montalban C, Del Moral I, Garcia-Unzueta MT, et al. Perioperative response of leptin and the tumor necrosis factor alpha system in morbidly obese patients. Influence of cortisol inhibition by etomidate. Acta Anaesthesiol Scand. 2001;45:207–12.CrossRefGoogle Scholar
  23. 23.
    Elimam A, Tjader I, Norgren S, et al. Total parenteral nutrition after surgery rapidly increases serum leptin levels. Eur J Endocrinol. 2001;144:123–8.CrossRefGoogle Scholar
  24. 24.
    Boden G, Chen X, Mozzoli M, et al. Effect of fasting on serum leptin in normal human subjects. J Clin Endocrinol Metab. 1996;81:3419–23.PubMedGoogle Scholar
  25. 25.
    Considine RV. Regulation of leptin production. Rev Endocr Metab Disord. 2001;2:357–63.CrossRefGoogle Scholar
  26. 26.
    Scriba D, Aprath-Husmann I, Blum WF, et al. Catecholamines suppress leptin release from in vitro differentiated subcutaneous human adipocytes in primary culture via beta1- and beta2-adrenergic receptors. Eur J Endocrinol. 2000;143:439–45.CrossRefGoogle Scholar
  27. 27.
    Couillard C, Mauriege P, Prud'homme D, et al. Plasma leptin response to an epinephrine infusion in lean and obese women. Obes Res. 2002;10:6–13.CrossRefGoogle Scholar
  28. 28.
    Fellander G, Nordenstrom J, Tjader I, et al. Lipolysis during abdominal surgery. J Clin Endocrinol Metab. 1994;78:150–5.PubMedGoogle Scholar
  29. 29.
    Faggioni R, Feingold KR, Grunfeld C. Leptin regulation of the immune response and the immunodeficiency of malnutrition. Faseb J. 2001;15:2565–71.CrossRefGoogle Scholar
  30. 30.
    Kok P, Roelfsema F, Frolich M, et al. Spontaneous diurnal thyrotropin secretion is enhanced in proportion to circulating leptin in obese premenopausal women. J Clin Endocrinol Metab. 2005;90:6185–91.CrossRefGoogle Scholar
  31. 31.
    Chan JL, Heist K, DePaoli AM, et al. The role of falling leptin levels in the neuroendocrine and metabolic adaptation to short-term starvation in healthy men. J Clin Invest. 2003;111:1409–21.CrossRefGoogle Scholar
  32. 32.
    Schurgin S, Canavan B, Koutkia P, et al. Endocrine and metabolic effects of physiologic r-metHuLeptin administration during acute caloric deprivation in normal-weight women. J Clin Endocrinol Metab. 2004;89:5402–9.CrossRefGoogle Scholar
  33. 33.
    Börner U, Klimek M, Schoengen H, et al. The influence of various anesthetics on the release and metabolism of thyroid hormones: results of two clinical studies. Anesth Analg. 1995;81:612–8.PubMedGoogle Scholar
  34. 34.
    Marana E, Scambia G, Colicci S, et al. Leptin and perioperative neuroendocrine stress response with two different anaesthetic techniques. Acta Anaesthesiol Scand. 2008;52:541–6.CrossRefGoogle Scholar

Copyright information

© Springer Science + Business Media, LLC 2009

Authors and Affiliations

  • Marina Michalaki
    • 1
    Email author
  • Apostolos G. Vagenakis
    • 1
  • Marianna Argentou
    • 2
  • Panagiotis Mylonas
    • 1
  • Fotis Kalfarentzos
    • 2
  • Venetsana Kyriazopoulou
    • 1
  1. 1.Department of Internal MedicineDivision of Endocrinology, University HospitalRion-PatrasGreece
  2. 2.Division of Nutritional Support and Morbid ObesityUniversity Hospital PatrasPatrasGreece

Personalised recommendations