Download PDF
Tierarztl Prax Ausg K Kleintiere Heimtiere 2017; 45(02): 95-101
DOI: 10.15654/TPK-160333
Original Article
Schattauer GmbH

Leptin and ghrelin concentration in hyperthyroid cats before and after radioactive iodine therapy compared to euthyroid control cats[*]

Leptin- and Ghrelinkonzentration bei hyperthyreoten Katzen vor und nach Radioiodtherapie im Vergleich zu euthyreoten Kontrollkatzen
Sina Marsilio   *
1   Department of Small Animal Internal Medicine, Small Animal Clinic, Justus-Liebig University, Giessen, Germany
5   Gastrointestinal Laboratory, Department of Small Animal Clinical Science, Texas A&M University, College Station, TX USA
,
Barbara Glanemann
2   Department of Clinical Science and Services, Royal Veterinary College, North Mymms, Hatfield, UK
,
Lucile Martin
3   Department of Biology, Pathology and Food Science, Oniris, National College of Veterinary Medicine, Food Science and Engineering, France
,
Balazs Szladovits
4   Department of Pathology and Pathogen Biology, Royal Veterinary College, North Mymms, Hatfield, UK
,
Reto Neiger
1   Department of Small Animal Internal Medicine, Small Animal Clinic, Justus-Liebig University, Giessen, Germany
› Author Affiliations
Further Information

Publication History

Received: 15 May 2016

Accepted after revision: 09 February 2016

Publication Date:
08 January 2018 (online)

    Permissions and Reprints

Summary

Objective: Leptin and ghrelin, two peptide hormones with antagonistic effects on satiety and energy balance, could be involved in the pathogenesis of weight loss and polyphagia in cats with hyperthyroidism. Leptin generally decreases appetite and increases energy expenditure, while ghrelin exerts the opposite effects. Materials and methods: Leptin and ghrelin were measured in 42 client owned hyperthyroid cats with a body condition score (BCS) 5/9 before (T0) and 4 weeks after radioactive iodine treatment (RAIT) (T1). Dependent on the serum total thyroxine concentration concentration at T1, cats were sub-classified as still hyperthyroid (ht-ht) (n = 4), euthyroid (ht-eu) (n = 10) or hypothyroid (ht-hypo) (n = 28). Results were compared to those of 22 healthy, euthyroid control cats with a comparable BCS ( 5/9) and age ( 8 years) to hyperthyroid cats. Results: At T0, there were no significant differences between hyperthyroid and control cats for leptin (p = 0.06) or ghrelin concentrations (p = 0.27). At T1, leptin significantly decreased in ht-hypo cats compared to T0 (p = 0.0008) despite a significantly increased body weight in this group (p = 0.0001). Serum ghrelin concentrations did not differ between hyperthyroid cats with a history of polyphagia compared to non-polyphagic cats (p = 0.42). After RAIT, ghrelin concentration significantly increased in all hyperthyroid cats (p < 0.0001), as well as in the subgroups ht-eu (p = 0.014) and ht-hypo (p < 0.0001) compared to their respective T0 baseline concentrations. Conclusion: Leptin and ghrelin fluctuations may be indicative of changes in metabolic functions in cats with thyroid dysfunction. Leptin fluctuations occurred independently of body weight in different states of thyroid dysfunction; increasing ghrelin concentrations after RAIT suggest a ghrelin-independent mechanism for polyphagia in hyperthyroid cats.

Zusammenfassung

Gegenstand und Ziel: Leptin und Ghrelin, zwei Peptidhormone mit antago nistischem Effekt auf Sättigung und Energiebilanz, könnten bei Katzen mit Hyperthyreose in die Pathogenese von Gewichtsverlust und Polyphagie involviert sein. Leptin führt allgemein zu vermindertem Appetit und erhöhtem Energieverbrauch, Ghrelin bewirkt entgegengesetzte Effekte. Material und Methoden: Bei 42 Katzen mit spontan auftretender Hyperthyreose und einem Body Condition Score (BCS) 5/9 wurden Leptin und Ghrelin vor (T0) und nach Radioiodtherapie (RAIT) (T1) bestimmt. Abhängig von der Gesamt-T4-Konzentration zum Zeitpunkt T1 erfolgte eine Subklassifizierung der Tiere als weiterhin hyperthyreot (ht-ht) (n = 4), euthyreot (ht-eu) (n = 10) oder hypothyreot (ht-hypo) (n = 28). Die Resultate wurden mit denen 22 gesunder, euthyreoter Katzen mit ähnlichem BCS ( 5/9) and Alter ( 8 Jahre) ver glichen. Ergebnisse: Zum Zeitpunkt T0 ergaben sich bei hyperthyreo ten und Kontrollkatzen keine signifikanten Unterschiede hinsichtlich der Leptin- (p = 0,06) oder Ghrelinkonzentration (p = 0,27). Die Leptinkonzentration der Gruppe ht-hypo war an T1 signifikant niedriger als an T0 (p = 0,0008), trotz eines signifikant höhe ren Körpergewichts (p = 0,0001). Die Ghrelinkonzentrationen von Katzen mit und ohne Polyphagie differierten nicht signifikant (p = 0,42). Nach RAIT stieg die Ghrelinkonzentration signifikant in der gesamten Gruppe zuvor hyperthyreoter Katzen (p < 0,0001) sowie in den Subgruppen ht-eu (p = 0,014) und ht-hypo (p < 0,0001) im Ver gleich zu T0. Schlussfolgerung: Fluktuationen der Leptin- und Ghrelinkonzentration könnten bei Katzen mit Schilddrüsendysfunktion auf metabolische Veränderun gen hindeuten. In verschiedenen Phasen der Schilddrüsendysfunktion zeigten sich Fluktuationen der Leptinkonzentration unabhängig vom Körpergewicht. Erhöhte Ghrelinkonzentrationen nach RAIT deuten auf einen ghrelinunabhängigen Mechanismus für Polyphagie hin.

Keywords

Thyroid dysfunction - thyroid hormones - feline

Schlüsselwörter

Schilddrüsendysfunktion - Schilddrüsenhormone - Katze

* Presented in abstract form at the 22. Annual Meeting of the Professional Group of Internal Medicine and Clinical Pathology of the German Veterinary Society, Giessen, Germany, February 2014. Data from this study were presented as a poster at the ACVIM Forum, June 4–7, 2014, Nashville, TN, USA.


 

  • References

  • 1 Appleton DJ, Rand JS, Sunvold GD. Plasma leptin concentrations in cats: reference range, effect of weight gain and relationship with adiposity as measured by dual energy X-ray absorptiometry. J Feline Med Surg 2000; 2: 191-199.
    CrossrefPubMedGoogle Scholar
  • 2 Backus RC, Havel PJ, Gingerich RL, Rogers QR. Relationship between serum leptin immunoreactivity and body fat mass as estimated by use of a novel gas-phase Fourier transform infrared spectroscopy deuterium dilution method in cats. Am J Vet Res 2000; 61: 796-801.
    CrossrefPubMedGoogle Scholar
  • 3 Backus RC, Cave NJ, Keisler DH. Gonadectomy and high dietary fat but not high dietary carbohydrate induce gains in body weight and fat of domestic cats. Br J Nutr 2007; 98: 641-650.
    CrossrefPubMedGoogle Scholar
  • 4 Boag AK, Neiger R, Slater L, Stevens KB, Haller M, Church DB. Changes in the glomerular filtration rate of 27 cats with hyperthyroidism after treatment with radioactive iodine. Vet Rec 2007; 161: 711-715.
    CrossrefPubMedGoogle Scholar
  • 5 Caminos JE, Seoane LM, Tovar SA, Casanueva FF, Dieguez C. Influence of thyroid status and growth hormone deficiency on ghrelin. Eur J Endocrinol 2002; 147: 159-163.
    CrossrefPubMedGoogle Scholar
  • 6 Cheung CC, Clifton DK, Steiner RA. Proopiomelanocortin neurons are direct targets for leptin in the hypothalamus. Endocrinology 1997; 138: 4489-4492.
    CrossrefPubMedGoogle Scholar
  • 7 Dornonville de la Cour C, Lindqvist A, Egecioglu E, Tung YC, Surve V, Ohlsson C, Jansson JO, Erlanson-Albertsson C, Dickson SL, Hakanson R. Ghrelin treatment reverses the reduction in weight gain and body fat in gastrectomised mice. Gut 2005; 54: 907-913.
    CrossrefPubMedGoogle Scholar
  • 8 German AJ, Holden SL, Moxham GL, Holmes KL, Hackett RM, Rawlings JM. A simple, reliable tool for owners to assess the body condition of their dog or cat. J Nutr 2006; 136: 2031s-2033s.
    CrossrefPubMedGoogle Scholar
  • 9 Gimenez-Palop O, Gimenez-Perez G, Mauricio D, Berlanga E, Potau N, Vilardell C, Arroyo J, Gonzalez-Clemente JM, Caixas A. Circulating ghrelin in thyroid dysfunction is related to insulin resistance and not to hunger, food intake or anthropometric changes. Eur J Endocrinol 2005; 153: 73-79.
    CrossrefPubMedGoogle Scholar
  • 10 Hosoda H, Kojima M, Matsuo H, Kangawa K. Ghrelin and des-acyl ghrelin: two major forms of rat ghrelin peptide in gastrointestinal tissue. Biochem Biophys Res Commun 2000; 279: 909-913.
    CrossrefPubMedGoogle Scholar
  • 11 Hsieh CJ, Wang PW, Wang ST, Liu RT, Tung SC, Chien WY, Lu YC, Chen JF, Chen CH, Kuo MC. Serum leptin concentrations of patients with sequential thyroid function changes. Clin Endocrinol 2002; 57: 29-34.
    CrossrefPubMedGoogle Scholar
  • 12 Ida T, Miyazato M, Naganobu K, Nakahara K, Sato M, Lin XZ, Kaiya H, Doi K, Noda S, Kubo A, Murakami N, Kangawa K. Purification and characterization of feline ghrelin and its possible role. Domestic animal endocrinology 2007; 32: 93-105.
    CrossrefPubMedGoogle Scholar
  • 13 Iglesias P, Alvarez Fidalgo P, Codoceo R, Diez JJ. Serum concentrations of adipocytokines in patients with hyperthyroidism and hypothyroidism before and after control of thyroid function. Clinical Endocrinol 2003; 59: 621-629.
    CrossrefPubMedGoogle Scholar
  • 14 Ishii S, Kamegai J, Tamura H, Shimizu T, Sugihara H, Oikawa S. Hypothalamic neuropeptide Y/Y1 receptor pathway activated by a reduction in circulating leptin, but not by an increase in circulating ghrelin, contributes to hyperphagia associated with triiodothyronine-induced thyrotoxicosis. Neuroendocrinol 2003; 78: 321-330.
    CrossrefPubMedGoogle Scholar
  • 15 Jaillardon L, Burger M, Siliart B. Leptin levels in hyperthyroid cats before and after treatment. Vet Rec 2012; 170: 155.
    PubMedGoogle Scholar
  • 16 Kang K, Zmuda E, Sleeman MW. Physiological role of ghrelin as revealed by the ghrelin and GOAT knockout mice. Peptides 2011; 32: 2236-2241.
    CrossrefPubMedGoogle Scholar
  • 17 Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H, Kangawa K. Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 1999; 402: 656-660.
    CrossrefPubMedGoogle Scholar
  • 18 Leray V, Siliart B, Dumon H, Martin L, Sergheraert R, Biourge V, Nguyen P. Protein intake does not affect insulin sensitivity in normal weight cats. J Nutr 2006; 136: 2028s-2030s.
    CrossrefPubMedGoogle Scholar
  • 19 Maffei M, Halaas J, Ravussin E, Pratley RE, Lee GH, Zhang Y, Fei H, Kim S, Lallone R, Ranganathan S. et al. Leptin levels in human and rodent: measurement of plasma leptin and ob RNA in obese and weight-reduced subjects. Nat Med 1995; 1: 1155-1161.
    CrossrefPubMedGoogle Scholar
  • 20 Martin L, Siliart B, Dumon H, Backus R, Biourge V, Nguyen P. Leptin, body fat content and energy expenditure in intact and gonadectomized adult cats: a preliminary study. J Anim Physiol Anim Nutr 2001; 85: 195-199.
    CrossrefPubMedGoogle Scholar
  • 21 Martin LJ, Siliart B, Dumon HJ, Nguyen P. Spontaneous hormonal variations in male cats following gonadectomy. J Feline Med Surg 2006; 8: 309-314.
    CrossrefPubMedGoogle Scholar
  • 22 Martin LJ, Siliart B, Lutz TA, Biourge V, Nguyen P, Dumon HJ. Postprandial response of plasma insulin, amylin and acylated ghrelin to various test meals in lean and obese cats. Br J Nutr 2010; 103: 1610-1619.
    CrossrefPubMedGoogle Scholar
  • 23 Nakazato M, Murakami N, Date Y, Kojima M, Matsuo H, Kangawa K, Matsukura S. A role for ghrelin in the central regulation of feeding. Nature 2001; 409: 194-198.
    CrossrefPubMedGoogle Scholar
  • 24 Paul DR, Kramer M, Rhodes DG, Rumpler WV. Preprandial ghrelin is not affected by macronutrient intake, energy intake or energy expenditure. Journal of Negative Results in BioMedicine 2005; 4: 1-8.
    CrossrefPubMedGoogle Scholar
  • 25 Pelleymounter MA, Cullen MJ, Baker MB, Hecht R, Winters D, Boone T, Collins F. Effects of the obese gene product on body weight regulation in ob/ob mice. Science (New York, NY) 1995; 269: 540-543.
    CrossrefPubMedGoogle Scholar
  • 26 Peterson ME, Becker DV. Radioiodine treatment of 524 cats with hyperthyroidism. J Am Vet Med Assoc 1995; 207: 1422-1428.
    PubMedGoogle Scholar
  • 27 Peterson ME. Radioiodine treatment of hyperthyroidism. Clin Techn Small Anim Pract 2006; 21: 34-39.
    PubMedGoogle Scholar
  • 28 Ruchala M, Gurgul E, Stangierski A, Wrotkowska E, Moczko J. Individual plasma ghrelin changes in the same patients in hyperthyroid, hypothyroid and euthyroid state. Peptides 2014; 51: 31-34.
    CrossrefPubMedGoogle Scholar
  • 29 Sinha MK, Ohannesian JP, Heiman ML, Kriauciunas A, Stephens TW, Magosin S, Marco C, Caro JF. Nocturnal rise of leptin in lean, obese, and non-insulin-dependent diabetes mellitus subjects. J Clin Invest 1996; 97: 1344-1347.
    CrossrefPubMedGoogle Scholar
  • 30 Theodoropoulou A, Psyrogiannis A, Metallinos IC, Habeos I, Vgenakis AG, Kyriazopoulou V. Ghrelin response to oral glucose load in hyperthyroidism, before and after treatment with antithyroid drugs. J Endocrinol Invest 2009; 32: 94-97.
    CrossrefPubMedGoogle Scholar
  • 31 Tolle V, Bassant MH, Zizzari P, Poindessous-Jazat F, Tomasetto C, Epelbaum J, Bluet-Pajot MT. Ultradian rhythmicity of ghrelin secretion in relation with GH, feeding behavior, and sleep-wake patterns in rats. Endocrinology 2002; 143: 1353-1361.
    CrossrefPubMedGoogle Scholar
  • 32 Tschop M, Smiley DL, Heiman ML. Ghrelin induces adiposity in rodents. Nature 2000; 407.
    PubMedGoogle Scholar
  • 33 Tschop M, Wawarta R, Riepl RL, Friedrich S, Bidlingmaier M, Landgraf R, Folwaczny C. Post-prandial decrease of circulating human ghrelin levels. J Endocrinol Invest 2001; 24: Rc19-21.
    CrossrefPubMedGoogle Scholar
  • 34 Williams TL, Elliott J, Syme HM. Association of iatrogenic hypothyroidism with azotemia and reduced survival time in cats treated for hyperthyroidism. J Vet Intern Med 2010; 24: 1086-1092.
    CrossrefPubMedGoogle Scholar
  • 35 Yoshida T, Monkawa T, Hayashi M, Saruta T. Regulation of expression of leptin mRNA and secretion of leptin by thyroid hormone in 3T3-L1 adipocytes. Biochem Biophys Res Commun 1997; 232: 822-826.
    CrossrefPubMedGoogle Scholar