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      Maternal Metabolic Demands Caused by Pregnancy and Lactation: Association with Productivity and Offspring Phenotype in High-Yielding Dairy Ewes

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          Abstract

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          This study assessed the effects of metabolic load imposed by pregnancy and lactation on productivity and offspring performance in high-yielding dairy sheep. Productivity was assessed in terms of offspring and maternal milk yield, metabolic profile, and body condition. Our results show that maternal productivity and lamb body weight and growth are not compromised by pregnancy and lactation because dairy sheep, when appropriately managed, seem to be able to cover metabolic demands of pregnancy and high milk production without losing productivity.

          Abstract

          Pregnancy and lactation, especially when concurrent, create a rather metabolically demanding situation in dairy ruminants, but little is known about their effects on offspring phenotype and milk yield. Here, we evaluated the impact of pregnancy and lactation on the metabolic traits and productive performance of Lacaune dairy sheep and their offspring. Productive performance was measured in terms of milk yield, body weight (BW), body condition score (BCS), and size. Productivity was assessed during mid-pregnancy (75 ± 5 d) and late pregnancy (142 ± 4 d) and at 52 ± 5 d in the postpartum period. During pregnancy, high-yielding ewes had higher BW, BCS, plasma glucose, cholesterol, β-OHB, and NEFA than low-yielding ewes, but lower levels of lactate and urea. High-yielding animals had lower BCS after lambing, but their lambs showed greater growth. Productivity during lactation was affected by ewe age and parity: Mature ewes (but not maiden sheep) whose BCS increased steeply during pregnancy yielded more milk in the subsequent lactation than those whose BCS did not increase. Lamb BW and size were positively associated with milk yield in the subsequent lactation. Mature ewes had higher yields than maiden sheep, and mature ewes with multiple pregnancies produced more milk than those with singleton pregnancies. Ewes with male singleton pregnancies also showed higher yield than those with female singletons. These results demonstrate that high-yielding dairy sheep, when appropriately fed and managed, can adequately cover the metabolic demands of pregnancy and high milk production (even when concurrent) without losing productivity.

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          Adaptations of glucose metabolism during pregnancy and lactation.

          Increased glucose requirements of the gravid uterus during late pregnancy and even greater requirements of the lactating mammary glands necessitate major adjustments in glucose production and utilization in maternal liver, adipose tissue, skeletal muscle, and other tissues. In ruminants, which at all times rely principally on hepatic gluconeogenesis for their glucose supply, hepatic glucose synthesis during late pregnancy and early lactation is increased to accommodate uterine or mammary demands even when the supply of dietary substrate is inadequate. At the same time, glucose utilization by adipose tissue and muscle is reduced. In pregnant animals, these responses are exaggerated by moderate undernutrition and are mediated by reduced tissue sensitivity and responsiveness to insulin, associated with decreased tissue expression of the insulin-responsive facilitative glucose transporter, GLUT4. Peripheral tissue responses to insulin remain severely attenuated during early lactation but recover as the animal progresses through mid lactation. Specific homeorhetic effectors of decreased insulin-mediated glucose metabolism during late pregnancy have yet to be conclusively identified. In contrast, somatotropin is almost certainly a predominant homeorhetic influence during lactation because its exogenous administration causes specific changes in glucose metabolism (and many other functions) of various nonmammary tissues which faithfully mimic normal adaptations to early lactation.
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            Prepartal plane of nutrition, regardless of dietary energy source, affects periparturient metabolism and dry matter intake in Holstein cows.

            Previous research in our laboratory showed that dietary fat supplementation during the dry period was associated with decreased peripartum hepatic lipid accumulation. However, fat supplementation decreased dry matter (DM) intake and thereby confounded results. Consequently, 47 Holstein cows with body condition scores (BCS) < or = 3.5 at dry-off were used to determine whether source or amount of energy fed to dry cows was responsible for the decreased hepatic lipid content. Moderate grain- or fat-supplemented diets [1.50 Mcal of net energy for lactation (NE(L))/kg] were fed from dry-off (60 d before expected parturition) to calving at either ad libitum (160% of NE(L) requirement) or restricted (80% of NE(L) requirement) intakes. Postpartum, cows were fed a single lactation diet for ad libitum intake and performance was measured for 105 d. Prepartum intakes of DM and NE(L) were significantly lower for feed-restricted cows as designed. During the first 21 d postpartum, previously restricted cows had higher intakes of DM and NE(L). Body weights and BCS were lower prepartum for restricted cows but groups converged to similar nadirs postpartum. Restricted-fed cows had lower concentrations of glucose and insulin and increased concentrations of NEFA in plasma during the dry period. Peripartum NEFA rose markedly for all treatments but were higher postpartum for cows previously fed ad libitum. Plasma concentrations of NEFA and BHBA remained lower in cows restricted-during the dry period. Postpartum concentrations of total lipid and triglyceride in liver were lower in cows previously feed-restricted. Across dietary treatments, activity of carnitine palmitoyltransferase (CPT) in hepatic mitochondria was lowest at - 21 d, highest at 1 d, and decreased at 21 and 65 d relative to parturition. The activity of CPT at d 1 tended to be higher for previously feed-restricted cows; thereafter, CPT activity declined more rapidly than in cows fed ad libitum. Nutrient intake during the dry period had more pronounced effects on peripartal lipid metabolism and DMI than did composition of the prepartum diet.
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              Relevance of apolipoproteins in the development of fatty liver and fatty liver-related peripartum diseases in dairy cows.

              Most metabolic diseases in dairy cows occur during the peripartum period and are suggested to be derived from fatty liver initially developed during the nonlactating stage. Fatty liver is induced by hepatic uptake of nonesterified fatty acids that are released in excess by adipose tissues attributable to negative energy balance. The fatty accumulation leads to impairment of lipoprotein metabolism in the liver, and the impairment in turn influences other metabolic pathways in extrahepatic tissues such as the steroid hormone production by the corpus luteum. Detailed understanding of the impaired lipoprotein metabolism is crucial for elucidation of the mechanistic bases of the development of fatty liver and fatty liver-related peripartum diseases. This review summarizes results on evaluation of lipoprotein lipid and protein concentrations and enzyme activity in cows with fatty liver and those with ketosis, left displacement of the abomasum, milk fever, downer syndrome and retained placenta. Obtained data strongly suggest that decreases in serum concentrations of apolipoprotein B-100, apolipoprotein A-I and apolipoprotein C-III, a reduction in activity of lecithin:cholesterol acyltransferase and induction of haptoglobin and serum amyloid A are intimately related to the development of fatty liver and fatty liver-related diseases. Moreover, determination of the apolipoprotein concentrations and enzyme activity during the peripartum period is useful for early diagnoses of these diseases.
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                Author and article information

                Journal
                Animals (Basel)
                Animals (Basel)
                animals
                Animals : an Open Access Journal from MDPI
                MDPI
                2076-2615
                30 May 2019
                June 2019
                : 9
                : 6
                : 295
                Affiliations
                [1 ]School of Veterinary Medicine and Zootechnics, Faculty of Agricultural Sciences, University of Cuenca, Avda. Doce de Octubre, Cuenca 010220, Ecuador; jose.pesantez@ 123456ucuenca.edu.ec
                [2 ]Department of Animal Reproduction, Instituto Nacional de Investigación Agrarias y Alimentarias (INIA), Avda Pta. de Hierro s/n, 28040 Madrid, Spain; andelash@ 123456ucm.es (A.H.-M.); torrerovi@ 123456gmail.com (L.T.-R.); mvsanzfernandez@ 123456gmail.com (M.V.S.-F.); garcia.consolacion@ 123456inia.es (C.G.-C.); bulnes@ 123456inia.es (A.G.-B.)
                [3 ]Faculty of Veterinary Medicine, Complutense University of Madrid (UCM), Avda. Pta. de Hierro s/n, 28040 Madrid, Spain; mvgomez@ 123456ucm.es (M.V.-G.); feyjoo96@ 123456gmail.com (P.F.); elicacer@ 123456ucm.es (E.C.); millanfr@ 123456ucm.es (M.F.-M.); juanvi@ 123456vet.ucm.es (J.V.G.-M.)
                [4 ]Technical Department, Granja Cerromonte SL, San Juan de la Encinilla, 05358 Ávila, Spain; granja@ 123456cerromonte.es
                [5 ]Departamento Producción y Sanidad Animal, Salud Pública Veterinaria y Ciencia y Tecnología de los Alimentos (PASAPTA), Facultad de Veterinaria, Universidad Cardenal Herrera-CEU, Tirant lo Blanc, 7. 46115 Alfara del Patriarca Valencia, Spain; paula.martinez@ 123456uchceu.es
                [6 ]Technical Department, TRIALVET SL, C/Encina 22, Cabanillas de la Sierra, 28721 Madrid, Spain
                Author notes
                [* ]Correspondence: astiz.susana@ 123456inia.es ; Tel.: +34-91-347-37-69
                Author information
                https://orcid.org/0000-0002-5669-6014
                https://orcid.org/0000-0001-7496-9680
                https://orcid.org/0000-0002-0678-1149
                https://orcid.org/0000-0002-8916-2086
                https://orcid.org/0000-0002-0917-4475
                https://orcid.org/0000-0002-9718-0903
                Article
                animals-09-00295
                10.3390/ani9060295
                6617180
                31151216
                baa59d4a-ba7b-4727-9cde-505f6ce7ce1f
                © 2019 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 30 April 2019
                : 28 May 2019
                Categories
                Article

                milk yield,dairy sheep,pregnancy rank,age,metabolic profile,birth weight,sex lamb

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