Abstract
The experiment was conducted at Araí & Zumbi farm on sixty healthy Dorper ewes to compare blood glucose, hormonal profile, and insulin resistance evaluation in sheep from conception until 48 h postpartum in single and twin pregnancies. All experimental ewes raised under semi-intensive management system. Sixty animals were selected from 150 estrous synchronized and pregnant ewes. The animals were divided into two groups based on single (G1, n = 30) and twin pregnancies (G2, n = 30). Blood samples were collected at nine time points: immediately after fixed-time artificial insemination (D0); at 30 days (D30), 90 days (D90), 120 days (D120), 130 days (D130), and 140 days (D140) of pregnancy; on the delivery day (DD); and at 24 h (PD1) and 48 h (PD2) postpartum. The results of blood glucose, insulin, glucagon, cortisol, and thyroid hormones (T3 and T4) levels showed significant differences over the analyzed sample times; however, only cortisol showed differences within groups, with the G1 having higher values than the G2 group. The interaction of the groups × nine sample times showed a significant result (P = 0.001) only for glucagon. The number of fetuses directly interfered with the glucagon profile throughout gestation. The glucose, cortisol, glucagon, and the homeostatic model assessment for insulin resistance (HOMA IR) concentrations increased at DD and decreased at PD1 and PD2. T3 and T4 showed different behaviors among the sample times. T3 values presented a decrease from D0 to D90, followed by an increase from D90 to DD. Otherwise, for T4 values, a decrease from D90 to D130 was observed, followed by an increase from D130 to D140. Despite the changes found in the endocrine system and metabolism in Dorper ewes throughout pregnancy, the nutritional management ensured a healthy status during pregnancy, delivery, and postpartum in single and twin gestation, whose HOMA IR profiles remained identical.
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References
Adhikari B., Khanal P., Nielsen M.O., 2018. Impacts of pre and postnatal nutrition on glucagon regulation and hepatic signaling in sheep. Journal of Endocrinology, 238(1): 1–12. https://doi.org/10.1530/JOE-17-0705
Araújo C.A.S.C., Nikolaus J.P., Morgado A.A., Monteiro B.M., Rodrigues F.A.M.L., Vechiato T.A.F., Soares P.C., Sucupira M.C.A., 2014. Energetic and hormonal profile of Santa Ines ewes in the middle of gestation to postpartum. Pesquisa Veterinária Brasileira, 34(12): 1249-1255. https://doi.org/10.1590/S0100-736X2014001200019
Bani Ismail Z., Al-Majali A.M., Amireh F., Al-Rawashdeh O.F., 2008. Metabolic profiles in goat does in late pregnancy with and without subclinical pregnancy toxaemia. Veterinary Clinical Pathology, 37(4): 434–437. https://doi.org/10.1111/j.1939-165X.2008.00076.x
Brondani W.C., Lemes J.S., Ferreira O.G.L., Roll V.F.B., Del Pino F.A.B., 2016. Metabolic profile in pregnant sheep. Archivos de Zootecnia, 65: 1-6.
Caldeira R.M., Vazques M.I., Portugal A.V., 2000. Daily profiles of blood insulin, insulin-like growth factor-I, thyroxine and triiodothyronine in ewes under three levels of feed intake. Asian-Australian Journal of Animal Science, 13: 1121-1126.
Caldeira R.M., Belo A.T., Santos C.C., Vazques M.I., Portugal A.V., 2007. The effect of body condition score on blood metabolites and hormonal profiles in ewes. Small Ruminant Research, 68(3): 233-241. https://doi.org/10.1016/j.smallrumres.2005.08.027
Campos A.G., Afonso J.A.B., Santos R.A., Mendonça C.L., Guimarães J.A., 2010. Clinical and laboratorial study of pregnancy toxaemia in ewes: retrospective analysis. Ciência Animal Brasileira, 11(3): 623-628. https://doi.org/10.5216/cab.v11i3.5499
Caroprese M., Albenzio M., Marzano A., Schena L., Annicchiarico G., Sevi A., 2010. Relationship between cortisol response to stress and behavior, immune profile, and production performance of dairy ewes. Journal of Dairy Science, 93(6): 2395–2403. https://doi.org/10.3168/jds.2009-2604
Celi P., Di Trana A. & Claps S. (2008). Effects of perinatal nutrition on lactational performance, metabolic and hormonal profiles of dairy goats and respective kids. Small Ruminant Research, 79(2-3): 129-136. https://doi.org/10.1016/j.smallrumres.2008.07.010
Dias I.R., Viegas C.A., Silva A.M., Pereira H.F., Sousa C.P., Carvalho P.P., Cabrita A.S., Fontes P.J., Silva S.R., Azevedo J.M.T., 2010. Haematological and biochemical parameters in Churra-da-Terra-Quente ewes from the northeast of Portugal. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 62(2): 265-272. https://doi.org/10.1590/S0102-09352010000200004
Duckett S.K., Volpi-Lagreca G., Alende M., Long N.M., 2014. Palmitoleic acid reduces intramuscular lipid and restores insulin sensitivity in obese sheep. Diabetes, Metabolic Syndrome and Obesity: Targets and Therapy, 7: 553–563. https://doi.org/10.2147/DMSO.S72695
Duehlmeier R., Fluegge I., Schwert B., Ganter M., 2013. Insulin Sensitivity during Late Gestation in Ewes Affected by Pregnancy Toxemia and in Ewes with High and Low Susceptibility to this Disorder. Journal of Veterinary Internal Medicine, 27(2): 359–366. https://doi.org/10.1111/jvim.12035
Firat A., Özpinar A., 2002. Metabolic Profile of Pre-Pregnancy, Pregnancy and Early Lactation in Multiple Lambing Sakiz Ewes 1. Changes in plasma glucose, 3-hydroxybutyrate and Cortisol Levels. Annals of Nutrition and Metabolism, 46(2): 57–61. https://doi.org/10.1159/000057641
Ford E.J., Evans J., Robinson I., 1990. Cortisol in pregnancy toxemia of sheep. British Veterinary Journal, 146(6): 539-542. https://doi.org/10.1016/0007-1935(90)90057-A
Frise C.J., Mackillop L., Joash K., Williamson C., 2013. Starvation ketoacidosis in pregnancy. European Journal of Obstetrics & Gynecology and Reproductive Biology, 167(1): 1-7. https://doi.org/10.1016/j.ejogrb.2012.10.005
Gui L-S, Raza S.H.A., Zhou L., Garcia M., El-Aziz A.H.A., Wei D., Hou S., Jia J., Wang Z., 2020. Association between single nucleotide polymorphisms in SIRT1 and SIRT2 loci and growth in Tibetan sheep. Animals, 10(8):1362. https://doi.org/10.3390/ani10081362
Gui L-S, Raza SHA, Alam FAEA, Zhou L., Hou S., Khan I., Kakan I.U., El-Azuz A.H.A., Jia J., Sun Y., Wang Z., 2021. Altered milk yield and rumen microbial abundance in response to concentrate supplementation during the cold season in Tibetan sheep. Electronic Journal of Biotechnology, 53: 80-86. https://doi.org/10.1016/j.ejbt.2021.07.001
Hefnawy A.E., Shousha S., Youssef S., 2011. Hematobiochemical profile of pregnant and experimentally pregnancy toxemic goats. Journal of Basic and Applied Chemistry, 1: 65-69.
Henze P., Bickhardt K., Fuhrmann H., Sallmann H.P., 1998. Spontaneous pregnancy toxaemia (Ketosis) in sheep and the role of insulin. Zentralbl Veterinarmed A, 45(5), 225-226. https://doi.org/10.1111/j.1439-0442.1998.tb00825.x
Husted S.M., Nielsen M.O., Blache D., Ingvartsen K.L., 2008. Glucose homeostasis and metabolic adaptation in the pregnant and lactating sheep are affected by the level of nutrition previously provided during her late fetal life. Domestic Animal Endocrinology, 34: 419-431. https://doi.org/10.1016/j.domaniend.2007.12.002
Jiang G., Zhang B.B., 2003. Glucagon and regulation of glucose metabolism. American Journal of Physiology-Endocrinology and Metabolism, 284: 671-678. https://doi.org/10.1152/ajpendo.00492.2002
Jones A.K., Reed S.A., 2017. Benefits of ultrasound scanning during gestation in the small ruminant. Small Ruminant Research, 149: 163-171. https://doi.org/10.1016/j.smallrumres.2017.02.008
Kalyesubula M., Mopuri R., Rosov A., Alon T., Edery N., Moallem U., Dvir H., 2020. Hyperglycemia-stimulating diet induces liver steatosis in sheep. Scientific Reports. Nature Research. 10:12189. https://doi.org/10.1038/s41598-020-68909-z
Kalyesubula M., Rosov A., Alon T., Moallem U., Dvir H., 2019. Intravenous infusions of glycerol versus propylene glycol for the regulation of negative energy balance in sheep: A randomized trial. Animals. 9(10): 731. https://doi.org/10.3390/ani9100731
Kaneko J.J., Harvey J.W., Bruss M.L., 2008. Clinical biochemistry of domestic animals. 6.ed. San Diego: Academic. 916p.
Liggins G.C., 1994. The role of cortisol in preparing the fetus for birth. Reprod. Fertil. Dev. 6:141–150. https://doi.org/10.1071/RD9940141
Matthews D., Hosker J.P., Rudenski A.S., Naylor B.A., Treacher D.F., Turner R.C., 1985. Homeostasis model assessment: insulin resistance and β-cell function from fasting glucose and insulin concentrations in man. Diabetologia. 28: 412-419. https://doi.org/10.1007/BF00280883
NRC, 2007. Nutrient Requirements of Small Ruminants: sheep, goats, cervids and New World camelids. Natl Acad. Press, Washington, DC. 384p.
Oikawa S., Oetzel G.R., 2006. Decreased insulin response in dairy cows following a four-day fast to induce hepatic lipidosis. Journal of Dairy Science, 89: 2999- 3005. https://doi.org/10.3168/jds.S0022-0302(06)72572-3
Oliveira E.P., Souza M.L.A., Lima M.D.A., 2005. HOMA (homeostasis model assessment) index in clinical practice: a review. Jornal Brasileiro de Patologia e Medicina Laboratorial, 41(4): 237-243. https://doi.org/10.1590/S1676-24442005000400004
Polizel D.M., Susin I., Gentil R.S., Ferreira E.M., de Souza R.A., Freire A.P.A., Pires A.V., Ferraz M.V.C., Rodrigues, P.H.M., Eastridge M.L., 2017. Crude glycerin decreases nonesterified fatty acid concentration in ewes during late gestation and early lactation, Journal of Animal Science, 95(2): 875-883. https://doi.org/10.2527/jas.2016.0999
Regnault T.R.H., Oddy H.V., Nancarrow C., Sriskandarajad N., Scaramuzzi R.J., 2004. Glucose-stimulated insulin response in pregnant sheep following acute suppression of plasma non-esterified fatty acid concentrations. Reproductive Biology and Endocrinology, 2: 1-10. https://doi.org/10.1186/1477-7827-2-64
Reid R.L, 1950. Studies on the carbohydrate metabolism of sheep. I. The range of blood-sugar values under several conditions. Australian Journal of Agricultural Research, 1(2): 182-199.
Russel A., 1991. Body condition scoring of sheep. In: E. Boden (Ed.) Sheep and Goat Practice. Bailliere Tindall, Philadelphia. p3.
Sadegzadeh-Sadat M., Anassori E., Khalilvandi-Behroozyar H., Asri-Rezaei S., 2021. The effects of Zinc-Methionine on glucose metabolism and insulin resistance during late pregnancy in ewes. Domestic Animal Endocrinology, 77: 106647. https://doi.org/10.1016/j.domaniend.2021.106647.
Santarosa B.P., Dantas G.N., Ferreira D.O.L., Santos B., Takahira R.K., Carvalho M.G., Silva A.A., Gonçalves R.C., 2019a. Comparison of biochemical parameters between single and twin pregnancies of Dorper breed ewes during gestation, lambing and postpartum. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 71(4): 1307-1315. https://doi.org/10.1590/1678-4162-10699
Santarosa B.P., Dantas G.N., Ferreira D.O.L., Carvalho M.G., Rodrigues M., Pereira P.F.V., Silva A.A., Gonçalves R.C. 2019b. Comparison of electrolyte and acid-base balances of Dorper breed ewes between single and twin pregnancies. Pesquisa Veterinária Brasileira, 39(10): 789-795. https://doi.org/10.1590/1678-5150-PVB-5952
Santos F.C.O., Mendonça C.L., Silva Filho A.P., Carvalho C.C.D., Soares P.C., Afonso J.A.B., 2011. Biochemical and hormonal indicators of natural cases of pregnancy toxaemia of in sheep. Pesquisa Veterinária Brasileira, 31(11): 974-980. https://doi.org/10.1590/S0100-736X2011001100006
Schlumbohm C., Harmeyer J., 2003. Hypocalcemia reduces endogenous glucose production in hyperketonemic sheep. Journal of Dairy Science, 86(6): 1953-1962. https://doi.org/10.3168/jds.S0022-0302(03)73783-7
Schmitt E., Schneider A., Gourlat M.A., Schwegler E., Pereira R.A., Hoffmann D.C.A., Lopes M.S., Hax L.T., Del Pino F.A.B., Correa M.N., 2012. Calcium and insulin correlation during the glucose tolerance test in pregnant and non-pregnant ewes. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 64(5): 1127-1132. https://doi.org/10.1590/S0102-09352012000500006
Shorten P.R., Pleasants A.B., Buckels E.J., Jaquiery A.L., Boston R.C., Alsweiler J.M., 2016. Determining insulin sensitivity from glucose tolerance tests in sheep. Journal of Animal Science, 94(9): 3711-3721. https://doi.org/10.2527/jas.2016-0521
Sivan E., Boden G., 2003. Free fatty acids, insulin resistance, and pregnancy. Current Diabetes Reports, 3: 319-322. https://doi.org/10.1007/s11892-003-0024-y
Souto R.C.J., Afonso J.A.B., Mendonça C.L., Carvalho C.C.D., Silva Filho A.P., Cajueiro J.F.P., Lima E.H.F., Soares P.C., 2013. Biochemical, electrolytic and hormonal findings in goats affected with pregnancy toxemia. Pesquisa Veterinária Brasileira, 33(10): 1174-1182. https://doi.org/10.1590/S0100-736X2013001000002
Souto R.C.J., Afonso J.A.B., Mendonça C.L., Dantas A.F.M., Cajueiro J.F.P., Gonçalves D.N.A., Oliveira Filho E.F., Soares P.C., 2019. Biochemical, endocrine, and histopathological profile of liver and kidneys of sheep with pregnancy toxemia. Pesquisa Veterinária Brasileira, 39(10): 780-788. https://doi.org/10.1590/1678-5150-PVB-6400
Todini L., Malfatti A., Valbonesi A., Trabalza-marinucci M., Debenedetti A., 2007. Plasma total T3 and T4 concentrations in goats at different physiological stages, as affected by energy intake. Small Ruminant Research, 68(3): 285-290. https://doi.org/10.1016/j.smallrumres.2005.11.018
Todini L. 2007. Thyroid hormones in small ruminants: effects of endogenous, environmental, and nutritional factors. Animals, 1: 997–1008. https://doi.org/10.1017/S1751731107000262
Van Soest P.J., Robertson J.B., Lewis, B.A., 1991. Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science, 74: 3583– 3597. https://doi.org/10.3168/jds.S0022-0302(91)78551-2
Vasques A.C.J., Rosado L.E.F.P.L., Alfenas R.C.G., Geloneze B., 2008. Critical analysis on the use of the homeostasis model assessment (HOMA) indexes in the evaluation of the insulin resistance and the pancreatic beta cells functional capacity. Arquivo Brasileiro de Endocrinologia e Metabologia, 52(1): 32-39. https://doi.org/10.1590/S0004-27302008000100006
Vernon R.G., 2005. Lipid metabolism during lactation: A review of adipose tissue-liver interactions and the development of fatty liver. Journal of Dairy Research, 72(4): 460–469. https://doi.org/10.1017/S0022029905001299
Yildiz A., Balikci E., Gurdogan F., 2005. Serum Mineral Levels at Pregnancy and Postpartum in Single and Twin Pregnant Sheep. Biological Trace Element Research, 107(3): 247-258. https://doi.org/10.1385/BTER:107:3:247
Zhang L., Long N.M., Hein S.M., Ma Y., Nathanielsz P.W., Ford S.P., 2011. Maternal obesity in ewes results in reduced foetal pancreatic β-cell numbers in late gestation and decreased circulating insulin concentration at term. Domestic Animal Endocrinology, 40(1): 30–39. https://doi.org/10.1016/j.domaniend.2010.08.004
Zhou L., Raza S.H.A., Ma B., Shater A.F., Mohammedsaleh Z.M., Jahejo, A.R., Li J., Gui L., 2021a. Mutations in FGFR1 were associated with growth traits in sheep (Ovis aries), Animal Biotechnology, https://doi.org/10.1080/10495398.2021.1929271
Zhou L., Raza S.H.A., Gao Z., Sayed S.M., Shukry M., El-Aziz A.H.A., Alotaibi M.A., Jaheio A.R., Simal-Gandara J., Hou S., Gui L-S., 2021b Variations in the insulin receptor substrate 1 (IRS1) and its association with growth traits in Chinese black Tibetan sheep (Ovis aries). Animal Biotechnology, 32: 786-791. https://doi.org/10.1080/10495398.2021.1957687
Acknowledgements
The authors thank the School of Veterinary Medicine and Animal Science of São Paulo State University (FMVZ/UNESP) and the Laboratory of Experimental Research on Gynecology and Obstetrics, Botucatu Medical School, São Paulo State University (FMB/UNESP), Botucatu, São Paulo State, for the infrastructure and equipment used to conduct the experiment and the Araí & Zumbi farm, Pardinho, São Paulo State, for the use of the animals and for assistance with sample collection.
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The study was financially supported by the São Paulo State Research Support Foundation (FAPESP) through regular grant to the research project [Process 2015/08714–8] and covering all the laboratory costs, including commercial ELISA kits, cartridge for portable blood gas analyzer (blood glucose), and other consumables and the Coordination of Improvement of Personal Higher Education (CAPES) for the PhD Scholarship granted that guaranteed the exclusivity and financial support for doctoral student (Santarosa, B.P.) to execute the project.
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B.P. Santarosa: data curation, formal analysis, investigation, methodology, and writing—original draft. D.O.L. Ferreira: conceptualization, investigation, and methodology. H.B. Hooper: translation and writing—review & editing. Y.K. Sinzato: formal analysis, investigation, and methodology. D.C. Damasceno: data curation, formal analysis, investigation, and methodology. D.M. Polizel: statistical analysis. E.G. Fioratti: writing—review & editing. V.H. Santos: data curation, formal analysis, investigation, and methodology. A.A. da Silva: visualization, supervision, and writing—review & editing. R.C. Gonçalves: funding acquisition, visualization, and supervision. All the authors read and approved the final manuscript.
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Santarosa, B.P., Ferreira, D.O.L., Hooper, H.B. et al. Endocrine-metabolic adaptations in Dorper ewes: comparison between single and twin pregnancies during gestation, parturition, and postpartum. Trop Anim Health Prod 54, 307 (2022). https://doi.org/10.1007/s11250-022-03306-4
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DOI: https://doi.org/10.1007/s11250-022-03306-4