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The effect of maternal nutrition level during the periconception period on fetal muscle development and plasma hormone concentrations in sheep

Published online by Cambridge University Press:  06 May 2016

U. Sen ,
E. Sirin ,
S. Yildiz ,
Y. Aksoy ,
Z. Ulutas  and
M. Kuran
U. Sen*
Affiliation:
Department of Agricultural Biotechnology, Faculty of Agriculture, Ahi Evran University, TR40100 Asikpasa, Kirsehir, Turkey
E. Sirin
Affiliation:
Department of Agricultural Biotechnology, Faculty of Agriculture, Ahi Evran University, TR40100 Asikpasa, Kirsehir, Turkey
S. Yildiz
Affiliation:
Department of Physiology, Faculty of Medicine, Inonu University, 44280 Malatya, Turkey
Y. Aksoy
Affiliation:
Department of Animal Science, Faculty of Agriculture, Osmangazi University, 26160 Eskisehir, Turkey
Z. Ulutas
Affiliation:
Department of Animal Production and Technologies, Ayhan Sahenk Faculty of Agriculture Science and Technologies, Nigde University, 51240 Nigde, Turkey
M. Kuran
Affiliation:
Department of Agricultural Biotechnology, Faculty of Agriculture, Ondokuz Mayis University, TR55139 Atakum, Samsun, Turkey
*
†E-mail: [email protected]
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Abstract

The effect of maternal nutrition level during the periconception period on the muscle development of fetus and maternal–fetal plasma hormone concentrations in sheep were examined. Estrus was synchronized in 55 Karayaka ewes and were either fed ad libitum (well-fed, WF, n=23) or 0.5×maintenance (under-fed, UF, n=32) 6 days before and 7 days after mating. Non-pregnant ewes (WF, n=13; UF, n=24) and ewes carrying twins (WF, n=1) and female (WF, n=1; UF, n=3) fetuses were removed from the experiment. The singleton male fetuses from well-fed (n=8) and under-fed (n=5) ewes were collected on day 90 of gestation and placental characteristics, fetal BWs and dimensions, fetal organs and muscles weights were recorded. Maternal (on day 7 after mating) and fetal (on day 90 of pregnancy) blood samples were collected to analyze plasma hormone concentrations. Placental characteristics, BW and dimensions, organs and muscles weights of fetuses were not affected by maternal feed intake during the periconception period. Maternal nutrition level did not affect fiber numbers and the muscle cross-sectional area of the fetal longissimus dorsi (LD), semitendinosus (ST) muscles, but the cross-sectional area of the secondary fibers in the fetal LD and ST muscles from the UF ewes were higher than those from the WF ewes (P<0.05). Also, the ratio of secondary to primary fibers in the ST muscle were tended to be lower in the fetuses from the UF ewes (P=0.07). Maternal nutrition level during the periconception period did not cause any significant changes in fetal plasma insulin and maternal and fetal plasma IGF-I, cortisol, progesterone, free T3 and T4 concentrations. However, maternal cortisol concentrations were lower while insulin concentrations were higher in the WF ewes than those in the UF ewes (P<0.05). These results indicate that the reduced maternal feed intake during the periconception period may alter muscle fiber diameter without affecting fiber types, fetal weights and organ developments and plasma hormone concentrations in the fetus.

Keywords

sheepnutritionpericonceptionhormone statusfetal muscle fiber diameter
Type
Research Article
Information
animal , Volume 10 , Issue 10 , October 2016 , pp. 1689 - 1696
Copyright
© The Animal Consortium 2016 

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References

AFRC 1993. Energy and protein requirements of ruminants. An advisory manual prepared by the agricultural and food research council technical committee on responses to nutrients. CAB International, Wallingford, UK.Google Scholar
Annett, RW and Carson, AF 2006. Effects of plane of nutrition during the first month of pregnancy on conception rate, foetal development and lamb output of mature and adolescent ewes. Animal Science 82, 947–954.CrossRefGoogle Scholar
Bispham, J, Gopalakrishnan, GS, Dandrea, J, Wilson, V, Budge, H, Keisler, DH, Broughton Pipkin, F, Stephenson, T and Symonds, ME 2003. Maternal endocrine adaptation throughout pregnancy to nutritional manipulation: consequences for maternal plasma leptin and cortisol and the programming of fetal adipose tissue development. Endocrinology 144, 3575–3585.CrossRefGoogle ScholarPubMed
Brameld, JM, Greenwood, PL and Bell, AW 2010. Biological mechanisms of fetal development relating to postnatal growth, efficiency and carcass characteristics in ruminants. In Managing the prenatal environment to enhance livestock productivity (ed. Greenwod PL, Bell AW, Vercoe PE and Viljoen GJ), pp. 93–119. Springer, the Netherlands.CrossRefGoogle Scholar
Branca, A, Molle, G, Sitzia, M, Decandia, M and Landau, S 2000. Short-term dietary effects on reproductive wastage after induced ovulation and artificial insemination in primiparous lactating Sarda ewes. Animal Reproduction Science 58, 59–71.CrossRefGoogle ScholarPubMed
Brooke, MH and Kaiser, KK 1970. Muscle fiber types: how many and what kind? Archives of Neurology 23, 369–379.CrossRefGoogle ScholarPubMed
Cam, MA, Kuran, M, Yildiz, S and Selcuk, E 2002. Fetal growth and reproductive performance in ewes administered GnRH agonist on day 12 post-mating. Animal Reproduction Science 72, 73–82.CrossRefGoogle ScholarPubMed
Costello, PM, Rowlerson, A, Astaman, NA, Anthony, FEW, Sayer, AA, Cooper, C, Hanson, MA and Green, LR 2008. Peri-implantation and late gestation maternal undernutrition differentially affect fetal sheep skeletal muscle development. The Journal of Physiology 586, 2371–2379.CrossRefGoogle ScholarPubMed
Crosier, AE, Farin, CE, Rodriguez, KF, Blondin, P, Alexander, JE and Farin, PW 2002. Development of skeletal muscle and expression of candidate genes in bovine fetuses from embryos produced in vivo or in vitro. Biology of Reproduction 67, 401–408.CrossRefGoogle ScholarPubMed
Dwyer, CM, Stickland, NC and Fletcher, JM 1994. The influence of maternal nutrition on muscle fiber number development in the porcine fetus and on subsequent postnatal growth. Journal of Animal Science 72, 911–917.CrossRefGoogle ScholarPubMed
Edwards, LJ and McMillen, IC 2002. Impact of maternal undernutrition during the periconceptional period, fetal number, and fetal sex on the development of the hypothalamo-pituitary adrenal axis in sheep during late gestation. Biology of Reproduction 66, 1562–1569.CrossRefGoogle ScholarPubMed
Fahey, AJ, Brameld, JM, Parr, T and Buttery, PJ 2005. The effect of maternal undernutrition before muscle differentiation on the muscle fiber development of the newborn lamb. Journal of Animal Science 83, 2564–2571.CrossRefGoogle ScholarPubMed
Gallaher, BW, Breier, BH, Keven, CL, Harding, JE and Gluckman, PD 1998. Fetal programming of insulin-like growth factor (IGF)-I and IGF-binding protein-3: evidence for an altered response to undernutrition in late gestation following exposure to periconceptual undernutrition in the sheep. Journal of Endocrinology 159, 501–508.CrossRefGoogle ScholarPubMed
Greenwood, PL, Slepetis, RM, Hermanson, JW and Bell, AW 1999. Intrauterine growth retardation is associated with reduced cell cycle activity, but not myofibre number, in ovine fetal muscle. Reproduction, Fertility and Development 11, 281–291.CrossRefGoogle Scholar
Jaquiery, AL, Oliver, MH, Honeyfield-Ross, M, Harding, JE and Bloomfield, FH 2012. Periconceptional undernutrition in sheep affects adult phenotype only in males. Journal of Nutrition and Metabolism 2012, doi:10.1155/2012/123610.CrossRefGoogle ScholarPubMed
Kenyon, PR and Blair, HT 2014. Foetal programming in sheep: effects on production. Small Ruminant Research 118, 16–30.CrossRefGoogle Scholar
Kleemann, DO, Walker, SK, Hartwich, KM, Fong, L, Seamark, RF, Robinson, JS and Owens, JA 2001. Fetoplacental growth in sheep administered progesterone during the first three days of pregnancy. Placenta 22, 14–23.CrossRefGoogle ScholarPubMed
Laporte-Broux, B, Roussel, S, Ponter, AA, Perault, J, Chavatte-Palmer, P and Duvaux-Ponter, C 2011. Short-term effects of maternal feed restriction during pregnancy on goat kid morphology, metabolism, and behavior. Journal of Animal Science 89, 2154–2163.CrossRefGoogle ScholarPubMed
Lassoued, N, Rekik, M, Mahouachi, M and Ben Hamouda, M 2004. The effect of nutrition prior to and during mating on ovulation rate, reproductive wastage, and lambing rate in three sheep breeds. Small Ruminant Research 52, 117–125.CrossRefGoogle Scholar
Lie, S, Morrison, JL, Williams-Wyss, O, Suter, CM, Humphreys, DT, Ozanne, SE, Zhang, S, MacLaughlin, SM, Kleemann, DO, Walker, SK, Roberts, CT and McMillen, IC 2015. Impact of periconceptional and preimplantation undernutrition on factors regulating myogenesis and protein synthesis in muscle of singleton and twin fetal sheep. Physiological Reports 3, e12495.Google ScholarPubMed
MacLaughlin, SM, Walker, SK, Roberts, CT, Kleemann, DO and McMillen, IC 2005. Periconceptional nutrition and the relationship between maternal body weight changes in the periconceptional period and feto-placental growth in the sheep. The Journal of Physiology 565, 111–124.CrossRefGoogle ScholarPubMed
Maltin, CA, Delday, MI, Sinclair, KD, Steven, J and Sneddon, AA 2001. Impact of manipulations of myogenesis in utero on the performance of adult skeletal muscle. Reproduction 122, 359–374.CrossRefGoogle ScholarPubMed
Maxfield, EK, Sinclair, KD, Broadbent, PJ, McEvoy, TG, Robinson, JJ and Maltin, CA 1998a. Short-term culture of ovine embryos modifies fetal myogenesis. American Journal of Physiology 274, 1121–1123.Google ScholarPubMed
Maxfield, EK, Sinclair, KD, Dunne, LD, Broadbent, PJ, Robinson, JJ, Stewart, E, Kyle, DG and Maltin, CA 1998b. Temporary exposure of ovine embryos to an advanced uterine environment does not affect fetal weight but alters fetal muscle development. Biology of Reproduction 59, 321–325.CrossRefGoogle Scholar
Oliver, MH, Hawkins, P, Breier, BH, Van Zijl, PL, Sargison, SA and Harding, JE 2001. Maternal undernutrition during the periconceptual period increases plasma taurine levels and insulin response to glucose but not arginine in the late gestational fetal sheep. Endocrinology 142, 4576–4579.CrossRefGoogle Scholar
Parr, RA, Davis, IF, Fairclough, RJ and Miles, MA 1987. Overfeeding during early pregnancy reduces peripheral progesterone concentration and pregnancy rate in sheep. Journal of Reproduction and Fertility 80, 317–320.CrossRefGoogle ScholarPubMed
Picciano, MF 2003. Pregnancy and lactation: physiological adjustments, nutritional requirements and the role of dietary supplements. Journal of Nutrition 133, 1997–2002.CrossRefGoogle ScholarPubMed
Quigley, SP, Kleeman, DO, Kakar, MA, Owens, JA, Nattrass, GS, Maddocks, S and Walker, SK 2005. Myogenesis in sheep is altered by maternal feed intake during the peri-conception period. Animal Reproduction Science 87, 241–251.CrossRefGoogle ScholarPubMed
Rae, MT, Rhind, SM, Kyle, CE, Miller, DW and Brooks, AN 2002. Maternal undernutrition alters triiodothyronine concentrations and pituitary response to GnRH in fetal sheep. Journal of Endocrinology 173, 449–455.CrossRefGoogle ScholarPubMed
Rhind, SM, McKelvey, WAC, McMillen, S, Gunn, RG and Elston, DA 1989. Effect of restricted food intake, before and/or after mating, on the reproductive performance of Greyface ewes. Animal Production 48, 149–155.CrossRefGoogle Scholar
Rumball, CW, Bloomfield, FH, Oliver, MH and Harding, JE 2009. Different periods of periconceptional undernutrition have different effects on growth, metabolic and endocrine status in fetal sheep. Pediatric Research 66, 605–613.CrossRefGoogle ScholarPubMed
Sen, U, Sirin, E, Aksoy, Y, Ensoy, U, Ulutas, Z and Kuran, M 2015. The effect of maternal nutrition level during mid-gestation on post-natal muscle fiber composition and meat quality in lambs. Animal Production Science 56, 834–843.CrossRefGoogle Scholar
Sen, U, Sirin, E and Kuran, M 2013. The effect of maternal nutritional status during mid-gestation on placental characteristics in ewes. Animal Reproduction Science 137, 31–36.CrossRefGoogle ScholarPubMed
Todini, L 2007. Thyroid hormones in small ruminants: effects of endogenous, environmental and nutritional factors. Animal 1, 997–1008.CrossRefGoogle ScholarPubMed
Viñoles, C, Forsberg, M, Martin, GB, Cajarville, C, Repetto, J and Meikle, A 2005. Short-term nutritional supplementation of ewes in low body condition affects follicle development due to an increase in glucose and metabolic hormones. Reproduction 129, 299–309.CrossRefGoogle Scholar
Wigmore, PM and Stickland, NC 1983. Muscle development in large and small pig fetuses. Journal of Anatomy 137, 235–245.Google ScholarPubMed
Wu, G, Bazer, FW, Wallace, JM and Spencer, TE 2006. Board-invited review: intrauterine growth retardation: implications for the animal sciences. Journal of Animal Science 84, 2316–2337.CrossRefGoogle ScholarPubMed