Ethem Mutlu TEMİZEL, Hüseyin CİHAN, Pınar LEVENT, Ahmet SARIL, Yeşim ÖZARDA, Zeki YILMAZ

Comparison of pre- and postpartum serum leptin, ghrelin, and lipid levels in sheep

Serum leptin and ghrelin play important roles in energy metabolism and inducing appetite during pregnancy and lactation. We investigated the serum levels of leptin and ghrelin and their relationship with the duration of lactation and serum biochemical responses during the prepartum (last week before lambing) and postpartum periods in sheep. They were also evaluated between pregnant and nonpregnant (control ewes) ewes. For these purposes, pregnant (n = 15) and control Awassi ewes (n = 15) that were 2 years of age were used in this study. Blood samples were collected 1 week before the expected date of lambing (baseline) and for 12 weeks after parturitions. Serum leptin, ghrelin, cholesterol, triglyceride, VLDL, LDL, HDL, NEFA, and phospholipid levels were assayed. Leptin and ghrelin levels of the prepartum period in pregnant and control ewes were 4.5 ng/mL and 3.4 ng/mL (P < 0.05) and 75 pg/mL and 166 pg/mL (P < 0.01), respectively. The baseline value of ghrelin (81 pg/mL) decreased to 43 pg/mL within 1 week after parturition (P < 0.01). Serum ghrelin levels increased after 1 week. There was also a significant difference in serum ghrelin levels between control ewes and those a week before parturition in pregnant ewes (P < 0.001). The NEFA level was higher in pregnant than in control sheep (P < 0.001). In conclusion, leptin levels tended to decrease during the lactation period, which could be associated with a negative energy balance. Additionally, ghrelin levels tended to gradually increase during lactation to adapt to a negative energy balance. We think that variations in serum leptin and ghrelin might be used to monitor metabolic adaptation during lactation.

Keywords:

Leptin, ghrelin, parturition, energy balance, sheep,

PDF

___

Yılmaz O, Kor A, Ertugrul M, Wilson R. The domestic livestock resources of Turkey: goat breeds and types and their conservation status. Anim Gene Res 2012; 51: 105-116.
Fthenakis G, Arsenos G, Brozos C, Fragkou I, Giadinis N, Giannenas I, Mavrogianni VS, Papadopoulos E, Valasi I. Health management of ewes during pregnancy. Anim Reprod Sci 2012; 130: 198-212.
Rook JS. Pregnancy toxemia of ewes, does, and beef cows. Vet Clin North Am Food Anim Pract 2000; 16: 293.
Brozos C, Mavrogianni V, Fthenakis G. Treatment and control of peri-parturient metabolic diseases: pregnancy toxemia, hypocalcemia, hypomagnesemia. Vet Clin North Am Food Anim Pract 2011; 27: 105-113.
Caro JF, Sinha MK, Kolaczynski JW, Zhang PL, Considine RV. Leptin: the tale of an obesity gene. Diabetes 1996; 45: 1455- 1462.
Nowroozi-Asl A, Aarabi N, Rowshan-Ghasrodashti A. Ghrelin and its correlation with leptin, energy related metabolites and thyroidal hormones in dairy cows in transitional period. Pol J Vet Sci 2016; 19: 197-204.
Woodside B, Abizaid A, Walker C. Changes in leptin levels during lactation: implications for lactational hyperphagia and anovulation. Horm Behav 2000; 37: 353-365.
Brogan RS, Mitchell SE, Trayhurn P, Smith MS. Suppression of leptin during lactation: contribution of the suckling stimulus versus milk production. Endocrinol 1999; 140: 2621-2627.
Tomimatsu T, Yamaguchi M, Murakami T, Ogura K, Sakata M, Mitsuda N, Kanzaki T, Kurachi H, Irahara M, Miyake A et al. Increase of mouse leptin production by adipose tissue after midpregnancy: gestational profile of serum leptin concentration. Biochem Biophys Res Commun 1997; 240: 213- 215.
Ehrhardt R, Slepetis R, Bell A, Boisclair Y. Maternal leptin is elevated during pregnancy in sheep. Domestic Animal Endocrinol 2001; 21: 85-96.
Block S, Butler W, Ehrhardt R, Bell A, Van Amburgh M, Boisclair Y. Decreased concentration of plasma leptin in periparturient dairy cows is caused by negative energy balance. J Endocrinol 2001; 171: 339-348.
Liefers S, Veerkamp R, te Pas M, Delavaud C, Chilliard Y, van der Lende T. Leptin concentrations in relation to energy balance, milk yield, intake, live weight, and estrus in dairy cows. J Dairy Sci 2003; 86: 799-807.
Carcangiu V, Giannetto C, Luridiana S, Fazio F, Mura M, Parmeggiani A, Piccione G. Lactation influences the serum level of leptin and growth hormone during the daily bathyphase in ewes. Biol Rhythm Res 2016; 1016: 1-7.
Itoh F, Komatsu T, Yonai M, Sugino T, Kojima M, Kangawa K, Hasegawa Y, Terashima Y, Hodate K. GH secretory responses to ghrelin and GHRH in growing and lactating dairy cattle. Domestic Animal Endocrinol 2005; 28: 34-45.
De Vriese C, Delporte C. Ghrelin: A new peptide regulating growth hormone release and food intake. Int J Biochem Cell Biol. 2008; 40: 1420-1424.
Hayashida T, Murakami K, Mogi K, Nishihara M, Nakazato M, Mondal M, Horii Y, Kojima M, Kangawa K, Murakami N. Ghrelin in domestic animals: Distribution in stomach and its possible role. Domestic Animal Endocrinol 2001; 21: 17-24.
Sugino T, Yamaura J, Yamagishi M, Ogura A, Hayashi R, Kurose Y, Kojima M, Kangawa K, Hasegawa Y, Terashima Y. A transient surge of ghrelin secretion before feeding is modified by different feeding regimens in sheep. Biochem Biophys Res Commun 2002; 298: 785-788.
Takahashi H, Kurose Y, Kobayashi S, Sugino T, Kojima M, Kangawa K, Hasegawa Y, Terashima Y. Ghrelin enhances glucose-induced insulin secretion in scheduled meal-fed sheep. J Endocrinol 2006; 189: 67-75.
Tschöp M, Smiley DL, Heiman ML. Ghrelin induces adiposity in rodents. Nature 2000; 407: 908-913.
Hosoda H, Kojima M, Matsuo H, Kangawa K. Ghrelin and des-acyl ghrelin: two major forms of rat ghrelin peptide in gastrointestinal tissue. Biochemical Biophys Res Commun 2000; 279: 909-913.
Nakai Y, Hosoda H, Nin K, Ooya C, Hayashi H, Akamizu T, Kangawa K. Plasma levels of active form of ghrelin during oral glucose tolerance test in patients with anorexia nervosa. Eur J Endocrinol 2003; 149: R1-3.
Yilmaz Z, Ilcol Y, Golcu E. Serum leptin and ghrelin levels in response to methylprednisolone injection in healthy dogs. Res Vet Sci 2007; 82: 187-194.
Kadokawa H, Blache D, Martin G. Plasma leptin concentrations correlate with luteinizing hormone secretion in early postpartum Holstein cows. J Dairy Sci 2006; 89: 3020-3027.
Comba A, Mert H, Coma B. Leptin levels and lipids profile determination in different sheep breeds. Pak Vet J 2016; 36: 169-173.
Delavaud C, Ferlay A, Faulconnier Y, Bocquier F, Kann G, Chilliard Y. Plasma leptin concentration in adult cattle: Effects of breed, adiposity, feeding level, and meal intake. J Anim Sci 2002; 80: 1317-1328.
Zhang Y, Proenca R, Maffei M, Marisa B, Lori L, Friedman J. Positional cloning of the mouse obese gene and its human homologue. Nature 1994; 372: 425-431.
Ahima J, Flier R. Leptin. Annu Rev Physiol 2000; 62: 413-437.
Considine R, Caro J. Leptin and the regulation of body weight. J Biochem Cell Biol 1997; 29: 1255-1272.
Kadokawa H, Blache D, Yamada Y, Martin G. Relationships between changes in plasma concentrations of leptin before and after parturition and the timing of first post-partum ovulation in high-producing Holstein dairy cows. Reprod Fertil Dev 2000; 12: 405-411.
Temizel EM, Batmaz H, Keskin A, Orman A, Gencoglu H, Catik S, Topal O. Butaphosphan and cyanocobalamin treatment of pregnant ewes: metabolic effects and potential prophylactic effect for pregnancy toxaemia. Small Rumin Res 2015; 125: 163-172.
Caldeira RM, Portugal AV. Interrelationships between body condition and metabolic status in ewes. Small Rumin Res 1991; 6: 15-24.
Kurose Y, Iqbal J, Rao A, Murata Y, Hasegawa Y, Terashima Y, Kojima M, Kangawa K, Clarke IJ. Changes in expression of the genes for the leptin receptor and the growth hormone- releasing peptide/ghrelin receptor in the hypothalamic arcuate nucleus with long-term manipulation of adiposity by dietary means. J Neuroendocrinol 2005; 17: 331-340.
Nakahara K, Nakagawa M, Baba Y, Sato M, Toshinai K, Date Y, Nakazato M, Kojima M, Miyazato M, Kaiya H et al. Maternal ghrelin plays an important role in rat fetal development during pregnancy. Endecrinol 2006; 147: 1333-1342.
Maillard V, Ram C, Froment P. Ghrelin in female and male reproduction. Int J Pept 2010; 2010: 2016.
Fuglsang J, Skjærbæk C, Espelund U, Frystyk J, Fisker S, Flyvbjerg A. Ghrelin and its relationship to growth hormones during normal pregnancy. Clin Endocrinol 2005; 554-559.
Di Palo R, Campanile G, Prandi A, Baruselli P, Vecchio D, Carvalho N, Zicarelli L. Plasma leptin levels in Murrah buffalo heifers fed diet with two different energy levels. Ital J Anim Sci 2005; 4: 301-303.
Koh KK, Park SM, Quon MJ. Contemporary reviews in cardiovascular medicine leptin and cardiovascular disease. Circulation 2013; 11: 3238-3249.
Halle M, Berg A, Garwers U, Grathwohl D, Knisel W, Keul J. Concurrent reductions of serum leptin and lipids during weight loss in obese men with type II diabetes. Am J Physiol Endocrinol Metab 1999; 277: 277-282.
Ban-Tokuda T, Orden EA, Barrio AN, Lapitan RM, Delavaud C. Effects of species and sex on plasma hormone and metabolite concentrations in crossbred Brahman cattle and crossbred water buffalo. Livestock Science 2007; 107: 244-252.
Cohen SM, Werrmann JG, Tota MR. 13C NMR study of the effects of leptin treatment on kinetics of hepatic intermediary metabolism. Proceedings of the National Academy of Sciences of the United States of America 1998; 95: 7385-7390.
Prieur X, Tung Y, Griffin J, Farooqi I, O’Rahilly S, Coll A. Leptin regulates peripheral lipid metabolism primarily through central effects on food intake. Endocrinology 2008; 149: 5432- 9.
Berridge M. Cell Signalling Through Phospholipid Metabolism. J Cell Sci 1986; 4: 137-153.
McMurray W, Magee W. Phospholipid metabolism. Annu Rev Biochem 1972; 41: 129-160.
Nielsen M, Jakobsent K. Changes in mammary uptake of free fatty acids, triglyceride, cholesterol and phospholipid in relation to milk synthesis during lactation in goats. Comprehensive Biochemical Physiology 1994; 109: 857-867.
Bitman J, Wood DL. Changes in milk fat phospholipids during lactation. J Dairy Sci 1989; 73: 1208-1216.
Tainturier D, Braun J, Rico A, Thouvenot J. Variations in blood composition in dairy cows during pregnancy and after calving. Res Vet Sci 1984; 37: 129-131.
Krajnicakova M, Bekeova E, Hendrichovscky V, Maracek I. Concentrations of total lipid, cholesterol and progesterone during oestrus synchronization and pregnancy in sheep. Vet Med 1993; 38: 349-357.
Piccione G, Caola G, Giannetto C, Grasso F, Runzo SC, Zumbo A, Pennisi P. Selected biochemical serum parameters in ewes during pregnancy, post-parturition lactation and dry period. Anim Sci Pap Rap 2009; 27: 321-330.