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Effects of vitamin E supply during late gestation and early lactation upon colostrum composition, milk production and quality in nutritional restricted ewes
Small Ruminant Research 133 (2015) 77–81
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Effects of vitamin E supply during late gestation and early lactation upon colostrum composition, milk production and quality in nutritional restricted ewes C.A. Rosales Nieto a,∗ , C.A. Meza-Herrera b , F.J. Morón Cedillo c , M.J. Flores Najera d , H.G. Gámez Vázquez a , V. Cuevas Reyes e , S.M. Liu f a
Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias, Campo Experimental San Luis, San Luis Potosí 78431, Mexico Universidad Autónoma Chapingo, Unidad Regional Universitaria de Zonas Áridas, Universidad Autónoma Chapingo 35230, Mexico c Facultad de Agronomía y Veterinaria, Universidad Autónoma de San Luis Potosí, San Luis Potosí 78321, Mexico d Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias, Campo Experimental Zacatecas, Calera de Víctor Rosales, Zacatecas 98500, Mexico e Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias, Campo Experimental Valle de México, 56250 Mexico f UWA Institute of Agriculture, The University of Western Australia, Crawley, WA 6009, Australia b
a r t i c l e
i n f o
Article history: Received 21 July 2015 Received in revised form 23 September 2015 Accepted 24 September 2015 Available online 30 September 2015 Keywords: Nutritional restriction Vitamin E Colostrum composition Milk production and composition
a b s t r a c t The aim of this study was to test if supplemental vitamin E during late gestation and early lactation to ewes facing a moderate nutritional restriction and suckling lambs from different litter size and sex would affect colostrum composition and milk yield and composition. Mature Rambouillet ewes (n = 37, 22◦ N) receiving 70% of energy and 80% of protein requirements were randomly assigned to either of two treatments: intramuscular injections of vitamin E (VitE; n = 20, 4 IU vitamin E kg−1 of live weight) in weekly intervals from 50 days before partition until 60 days of lactation, and control (CON; n = 17, without VitE treatment). While colostrum protein and fat concentrations did not differ between treatments (P > 0.05), lactose content favoured to the VitE-ewes (1.9% vs. 1.2%, P < 0.001). Colostrum protein concentration was affected by litter size favouring to twin lambs (14.3% vs. 17.3%, P < 0.05). In addition, litter size tended to affect lactose content, favouring to those ewes suckling twins (1.4% vs. 1.8%, P = 0.08). The average milk yield was 2039 g day−1 , without differences (P > 0.05) between treatments and litter size. The average milk concentrations of protein, lactose and solids-non-fat did not differ (P > 0.05) between treatments. Yet, milk fat content favour to the VitE-ewes (5.7% vs. 5.2%, P < 0.05). Milk concentrations of protein, fat, lactose and solids-non-fat were not affected (P > 0.05) by litter size. Non-significant treatment × litter size interactions (P > 0.05) were observed for milk yield, milk compositions of protein, fat and lactose and solids-non-fat. When the nutritional requirements are not met, treatment of vitamin E to ewes during late gestation and early lactation might be an strategy to improve the quality of both colostrum (>lactose) and milk (>fat). © 2015 Elsevier B.V. All rights reserved.
1. Introduction Maternal undernutrition during pregnancy impairs fetal nutrient supply and, depending on the level of restriction, may cause fetal losses or it may compromise the growth rate of lambs (Rumball et al., 2009; Jenkinson et al., 2012; Meza-Herrera and Tena-Sempere, 2012). Furthermore, maternal undernutrition is also associated with reduced colostrum and milk production (O’Doherty and Crosby, 1996; Nørgaard et al., 2008). Newborn’
∗ Corresponding author. E-mail address: nieto [email protected] (C.A. Rosales Nieto). http://dx.doi.org/10.1016/j.smallrumres.2015.09.014 0921-4488/© 2015 Elsevier B.V. All rights reserved.
colostrum intake is associated with survival and daily weight gain (Meza-Herrera and Tena-Sempere, 2012; Decaluwé et al., 2014; Hernández-Castellano et al., 2015). Therefore, failure to produce sufficient colostrum and milk, reduces maternal bond (Dwyer et al., 2003) and increases lamb mortality (Scales et al., 1986; Hashemi et al., 2008), with twin born lambs being the most at risk (Coop et al., 1972). Undernutrition also affects cell-mediated immunity, which is responsible for protection against several infections (McFarlane and Hamid, 1973). Vitamin E functions primarily as an antioxidant and maintenance of immune function (Burton et al., 1980; Turner and Finch, 1990). Inclusion of vitamin E in the diet has been associated with improvements in both immune competence and animal
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performance (Finch and Turner, 1996). Transfer of nutrients from dam to offspring occurs either by placental transfer or through colostrum/milk consumption. Yet, since vitamin E does not cross the placenta in any appreciate amount, newborns are highly susceptible to vitamin E deficiency if ewes have low vitamin E status (van Saun et al., 1989). Thus, pre-partum treatment of vitamin E is very important to provide to newborns sufficient amounts of vitamin E both in colostrum and milk (Hidiroglou, 1989; Njeru et al., 1994; Cuesta et al., 1995). Lambs reared by ewes treated with vitamin E in late gestation have shown a better productive performance (Koyuncu and Yerlikaya, 2007). However, it is not known whether vitamin E treatment in late gestation and during lactation will have the same effect when protein and energy requirements are not met; a recurrent scenario observed during late gestation and early lactation in marginal small ruminant production systems (Gonzalez-Bulnes et al., 2011; Meza-Herrera and Tena-Sempere, 2012). Based on that rationale, we tested whether supplemental vitamin E during late gestation in ewes facing a moderate nutritional restriction and suckling lambs from different litter size would affect colostrum composition and milk production and composition.
Table 1 Ingredient composition (as % in diet, DM basis), nutrient composition (DM basis) and nutritional requirement (NRC) of the experimental diet offering of gestation diet for a 60-kg ewe. Parameter
NRC requirement
Ingredient composition (% in diet) Alfalfa hay Oat hay Maize silage Nutrient composition CP (%) ME (Mcal/kg) Calcium (%) Phosphorus (%)
10.7 2.1 0.35 0.23
Experimental diet (as fed basis) 24.2 45.5 30.3 8.9 1.5 0.35 0.23
Lambs were weighed with a Torino® hanging scale with a capacity of 10 kg and a minimal graduation of 20 g. Ewes were weighed with a Ohaus Defender® digital scale with a capacity of 150 kg and a minimal graduation of 300 g.
2. Materials and methods
2.2. Sample collection and analysis
The experimental procedures reported in the current paper complied with the Official Mexican Rule for the technical specifications for the production, care and use of laboratory animals (NOM-062-ZOO-1999; SAGARPA 2001).
Immediately after parturition, a sample (about 10 mL) of colostrum was obtained by hand from one half of the udder. Samples from each ewe were kept in a plastic vial with a preservative of 0.6 mg mL−1 potassium dichromate and then frozen at −20 ◦ C until analysis for colostrum constituents. Colostrum samples were analysed for protein, fat and lactose using a Milkoscan 133B (Foss Electric, Hillerød, Denmark). One week after parturition, milk production and quality were measured weekly. The ewes were milked prior feeding on the same day of the week and starting at the same time, using the oxytocin protocol (McCance, 1959; Bencini, 1995). In brief, the ewes were drafted from the lambs, penned separately, and then hand-milked. To elicit milk let-down, ewes received an intramuscular injection of 3 mL of commercially available product and contained 20 IU mg−1 oxytocin (PiSA agropecuaria, Hidalgo; Mexico); the amount of oxytocin administrated was selected according to manufacturer’s guidelines. After five minutes, ewes were milked and the time of the first milking was recorded. The ewes were re-milked approximately 3 h later, in the same order as the initial milking, following the same oxytocin protocol. The weight of the milk collected at the second milking and the time between milkings were recorded to obtain an estimate of milk production per day. A sample (10 mL) of milk from each ewe was preserved with 0.6 mg mL−1 potassium dichromate and then frozen at −20 ◦ C until analysis of milk composition. After the second milking, the lambs and the ewes were reunited in their pen. Milk composition (protein, fat, lactose and solids-non-fat) was determined using a Milkoscan 133B (Foss Electric, Hillerød, Denmark).
2.1. Location, animals, management, treatments and feeding The study was conducted at the Faculty of Agronomy and Veterinary, University of San Luis Potosi, Mexico (22◦ N). Multiparous pregnant Rambouillet ewes (n = 37 ewes, ≥3 years old and ≥2 lactations) born and raised in these facilities mated to a single Rambouillet sire, of proven libido and fertility. During the mating period, the exact date of mating was recorded by the assistant. Starting on the last third of pregnancy (d-50), ewes were randomly divided in two treatments: (1) control (CON; n = 17, no vitamin E treatment) and (2) vitamin E-supplemented (VitE; n = 20, receiving 4 IU vitamin E kg−1 of live weight. VE-injections considered a commercial product and contained 27.2 IU mg−1 of ␣-tocopherol (vitamin E; Laboratorio Tornel, Estado de Mexico; Mexico). Intramuscular injections were given weekly on the same day of the week and at (0800 h), from late gestation (d-50) to early lactation (d + 60). Ewes were allocated by treatment in a separate common pen and after lambing, ewes and lambs were allocated in a separate common pen according to their treatment. Lambs were maintained with their dams until weaned. Ewes were fed alfalfa hay, oat hay and maize silage and each ewe (with lambs) was fed this diet in an individual pen (2.0 × 2.0 × 1.0 m), no more than 1 h and half, until total feed disappearance. The ewes spent the rest of the day in their respective common pen where clean water and minerals were provided ad libitum. In order to simulate a marginal rangeland scenario, treatment diet considered around of 70% and 80% of the requirements for energy and protein, respectively (NRC, 2007; Table 1). Dietary treatment started the last third of pregnancy (d-50) and continued until day 60 of lactation (d + 60). Diet and concentration of vitamin E treatment was adjusted every 14 days based on the recorded live weight. Each ewe gave birth to one or two lambs, 10 single and 10 set of twins from VitE and 12 single and 5 sets of twins from control, for a total of 52 lambs born, 21 females and 31 males. At lambing, birth weight, sex and litter size were recorded; Ewe´ıs live weight was recorded every two weeks from the last third of pregnancy (d-50) to day 60 of lactation (d + 60).
2.3. Statistical analysis Data analyses considered the SAS statistical package SAS version 9.3 (SAS Institute Inc., Cary, NC, USA). The data for colostrum quality (protein, lactose and fat) and milk quantity (at 24 h) and quality (fat, protein, lactose, solids-non-fat) were analysed using linear mixed model procedures and estimation technique of restricted maximum likelihood (PROC MIXED). Fixed effects were treatments and litter size. Lamb birth weight was included as covariate; ewes were considered as a random effect. The interaction between treatment and litter size was included in each model.
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Table 2 Colostrum composition (protein, fat and lactose) of sheep received vitamin E supplementation (VitE) or control nursed single or twin lambs1 .
Protein (%) Fat (%) Lactose (%)
VitE
Control
SEM
P values
16.2 9.9 1.9
14.3 8.9 1.2
1.8 1.3 0.18
0.15 0.27 0.001
Litter size
Single (n = 22)
Twin (n = 30)
SEM
P values
Protein (%) Fat (%) Lactose (%)
14.6 9.7 1.5
17.3 8.9 1.8
1.9 1.4 0.25
0.05 0.4 0.08
1 Birth weight of the lambs and interactions between treatment and little size were included in the analyses. For little size, data are combined for treatment and for males and females.
Table 3 Milk production and composition (protein, fat, lactose, density and solids-non-fat) for ewes received vitamin E supplementation (VitE) or control nursed single or twin lambs1 . VitE
Control
SEM
P values
Milk production (g/day) Protein (%) Fat (%) Lactose (%) SNF (%)
2202 3.6 6.1 5.4 10
1983 3.8 5.4 5.7 10.5
499 0.15 0.4 0.2 0.4
0.5 0.18 0.04 0.2 0.16
Litter size Milk production (g/day) Protein (%) Fat (%) Lactose (%) Solids-Non-Fat (%)
Single (n = 22) 2008 3.7 5.5 5.5 10.2
Twin (n = 30) 2170 3.8 6.1 5.6 10.3
489 0.18 0.5 0.27 0.5
0.6 0.4 0.1 0.5 0.6
1 Live weight of the ewes, lamb birth weight, and interactions between treatment and little size were included in the analyses. For little size, data are combined for treatment and for males and females.
3. Results 3.1. Colostrum composition The average colostrum protein concentration was 15.5 ± 0.6%, being affected by litter size (P < 0.05). Yet, protein content was not affected by treatments (P > 0.05) (Table 2). The interaction of treatment × litter size was not significant (P > 0.05). The average for colostrum fat concentration was 9.5 ± 0.4%, with no differences between treatments (P > 0.05), neither ewes suckling single or twin lambs (P > 0.05) (Table 2). The interaction of treatment × litter size was not significant (P > 0.05). The average colostrum lactose concentration was 1.6 ± 0.08%, observing a treatment effect (P < 0.001; Table 2). Interestingly, there was observed a trend (P = 0.08) for more lactose content in those ewes suckling twins, 1.4% for singles and 1.8% for twins. The interaction between treatment × litter size was not significant (P > 0.05). 3.2. Milk production and composition The average amount of milk produced was 2039 ± 73 g day−1 . No differences (P > 0.05) were observed neither between treatments nor litter size (P > 0.05; Table 3). Live weight of the ewes did not affect milk production (P > 0.05; Fig. 1). The average milk protein concentration was 3.6 ± 0.03%, without differences (P > 0.05) between treatments. In the same way, milk protein content was not affected (P > 0.05) by litter size (P > 0.05; Table 3). The average concentration of fat in the milk was 5.5 ± 0.1%, being affected (P < 0.01) by treatment, favouring to the VitE ewes (5.7% vs. 5.2%) but without differences between litter size (P > 0.05) (Table 3).
Fig. 1. Weekly milk production (solid line) and live weight (dashed line) of ewes that received vitamin E supplementation (VitE; black) or control (grey) during lactation.
The average concentration of lactose in the milk was 3.6 ± 0.03%, without differences between treatments (P > 0.05) and litter size (P > 0.05) (Table 3). The average content of solids-non-fat in milk composition was 10.1 ± 0.09% and similarly to the other milk components, no differences occurred between treatments, neither by litter size (P > 0.05; Table 3). The interaction of treatment × litter size was not significant for milk production, concentration of protein, fat and lactose in milk and content of solids-non-fat in milk composition (P > 0.05). Weekly changes in milk production (g day−1 ) and the live weight of ewes are shown in Fig. 1. Date of lactation affected the milk protein percentage (P < 0.05), fat content (P = 0.07), lactose content (P < 0.05), and the solids-non-fat content (P < 0.05). Live weight of the ewes did not influence concentrations of protein, fat, lactose and the solids-non-fat in milk. 4. Discussion According to our results, when nutritional requirements are not met, treatment to ewes with vitamin E during late gestation and early lactation could be an effective strategy to increase the quality of both colostrum (>lactose) and milk (>fat). Such outcomes are of key importance from an energetic view point during the early life (colostrum) and prior weaning (milk) of lambs whose mothers faced a mild nutritional restriction. Our results are in line with Capper et al. (2006) who observed that treatment of vitamin E in late pregnancy improved the quality of colostrum. Additionally, we observed that the composition of colostrum was not affected by the undernutrition subjected in the ewes, since our results are within the range to those reported elsewhere in Merino-type ewes (Banchero et al., 2004). This is an important issue, because foetal requirements for energy and protein are significant, particularly during the last trimester of gestation (Sykes and Field, 1972; Robinson, 1977). Therefore, our results suggest that concentration of major constituents in colostrum can be influenced by vitamin E treatment even when ewes face a nutritional restriction of protein and energy during late pregnancy. Little is the information about the effect of treatment of vitamin E on colostrum quality (e.g. protein, lactose, and fat content). Since vitamin E does not cross the placenta in any appreciable amounts, its content is concentrated in colostrum (van Saun et al., 1989). The increased concentration of vitamin E in colostrum improves the immune system of the newborn by increasing the amounts available of immunoglobulin (Finch and Turner, 1996; Rooke et al., 2004). To better understand the mechanism by which colostrum quality may be increased by treatment of vitamin E, more studies are required. Yet, we hypothesized that such results may be due to the antioxidant effects of vitamin E upon the immune system, since vitamin E treatment reduced both symptoms and incidence of
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disease in ruminant (Reddy et al., 1986). Therefore, if the maternal immune system during gestation is competent, vitamin E treatment may promote the partitioning of additional nutrients towards the udder system, favouring the quality of colostrum. In addition, we observed an increased in the concentration of lactose in colostrum in those ewes treated with vitamin E. Lactose synthesis regulates the amount of colostrum and milk segregated and it has been reported that lactose concentration in colostrum is reduced and increases over time (Linzell and Peaker, 1974; Zabielski et al., 1999; Kehoe et al., 2007). Although, we did not measure production of colostrum, it is probably that the treatment of vitamin E increased colostrum production in treated ewes hence the increase in lactose concentration observed in these ewes. Moreover, immune competence of the ewes may had helped to moderate the negative effect of maternal nutritional restriction upon the quality of colostrum. Therefore, treatment of vitamin E in late pregnancy may be feasible alternative to improve the quality of colostrum and, consequently, decrease the perinatal mortality in marginal sheep production systems. Although, vitamin E treatment neither increased milk production nor the concentrations of protein, lactose and solids-non-fat in milk, such treatment certainly increased the concentration of fat. Extending our results, Casamassima et al. (2014) in Lacaune ewes and Liu et al. (2008) and Tufarelli and Laudadio (2011) in dairy cows, observed an increase in milk fat due to treatment of vitamin E. The lack of any effect of treatment of vitamin E on milk production, milk protein and milk lactose agrees with other studies (Focant et al., 1998; Baldi et al., 2000; Kay et al., 2005). Moreover, the extended maternal undernutrition during pregnancy and lactation appeared not to affect milk production and quality since our results are in line with Ochoa-Cordero et al. (2002). Certainly, the ewes used by Ochoa-Cordero et al. (2002) were genetically similar, under intensive management and proper nutrition; nevertheless, they observed quite similar values for milk yield and concentration of fat, lactose and solids-non-fat in milk as reported in this experiment. Therefore, treatment of vitamin E in late pregnancy and early lactation may moderate the negative effects of maternal undernutrition upon milk production and quality. Despite milk production did not reach significant difference between groups, milk production increased 10% in the VE-ewes during lactation. Extending our results, Casamassima et al. (2014) in sheep, Tufarelli and Laudadio (2011) in goats and Lacetera et al. (1996) in cows observed a similar increase of 10% in milk yield in those vitamin E treated animals. The mechanism by which milk production and quality increased by vitamin E treatment is unclear, as we previously hypothesized, this could be due to the effects of antioxidant vitamins upon the immune system. Hence, the partitioning of additional nutrients towards milk production and quality may have occurred in the VitE-supplemented group. This could have been a positive carry-over effect from gestation upon lactation. The increase in milk fat, probably, was due to the fact that vitamin E is capable of reducing the extent of diet-induced milk fat depression as previously hypothesized (Lacetera et al., 1996; Pottier et al., 2006; Tufarelli and Laudadio, 2011). We did not observe any difference regarding the effect of live weigh of ewes on milk production and composition, yet some studies have pointed out that heavier ewes produce more milk than lighter ewes (Burris and Baugus, 1955; Bencini and Pulina, 1997). To conclude, when nutritional requirements are not met, supplementing ewes with vitamin E during late gestation and early lactation might be an effective strategy to improve the quality of both colostrum (>lactose) and milk (>fat). In addition, and quite interesting, colostrum protein and lactose contents were affected by litter size favouring to twin lambs. Such a strategy exerted by those ewes lambing larger litters seems to be a physiologic, and may be behavioural, wise strategy to counteract any possible
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pathways and milk fat depression in dairy cows fed high-fat diets. J. Dairy Sci. 89, 685–692. Reddy, P.G., Morrill, J.L., Minocha, H.C., Morrill, M.B., Dayton, A.D., Frey, R.A., 1986. Effect of supplemental vitamin E on the immune system of calves. J. Dairy Sci. 69, 164–171. Robinson, J.J., 1977. The influence of maternal nutrition on ovine foetal growth. Proc. Nutr. Soc. 36, 9–16. Rooke, J.A., Robinson, J.J., Arthur, J.R., 2004. Effects of vitamin E and selenium on the performance and immune status of ewes and lambs. J. Agric. Sci. 142, 253–262. Rumball, C.W.H., Bloomfield, F.H., Oliver, M.H., Harding, J.E., 2009. Different periods of periconceptional undernutrition have different effects on growth, metabolic and endocrine status in fetal sheep. Pediatr. Res. 66, 605–613. In SAS Institute, 2010. SAS/Stat User’s guide, Version 9.3. SAS Institute Inc., Cary, NC, USA. Scales, G.H., Burton, R.N., Moss, R.A., 1986. Lamb mortality, birthweight, and nutrition in late pregnancy. N. Z. J. Agric. Res. 29, 75–82. SAGARPA (Secretaría de Agricultura, Ganadería, Desarrollo Rural, Pesca y Alimentación, 2001. NORMA Oficial Mexicana NOM-062-ZOO-1999, Especificaciones técnicas para la producción, cuidado y uso de los animales de laboratorio. Diario Oficial de la Federación, 22 Agosto 2001. Sykes, A.R., Field, A.C., 1972. Effects of dietary deficiencies of energy, protein and calcium on the pregnant ewe. III. Some observations on the use of biochemical parameters in controlling energy undernutrition during pregnancy and on the efficiency of utilization of energy and protein for foetal growth. J. Agric. Sci. 78, 127–133. Tufarelli, V., Laudadio, V., 2011. Dietary supplementation with selenium and vitamin E improves milk yield, composition and rheological properties of dairy Jonica goats. J. Dairy Res. 78, 144–148. Turner, R.J., Finch, J.M., 1990. Immunological malfunctions associated with low selenium-vitamin E diets in lambs. J. Comp. Pathol. 102, 99–109. Zabielski, R., Le Huërou-Luron, I., Guilloteau, P., 1999. Development of gastrointestinal and pancreatic functions in mammalians (mainly bovine and porcine species): influence of age and ingested food. Reprod. Nutr. Dev. 39, 5–26. van Saun, R.J., Herdt, T.H., Stowe, H.D., 1989. Maternal and fetal selenium concentrations and their interrelationships in dairy cattle. J. Nutr. 119, 1128–1137.
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Small Ruminant Research journal homepage: www.elsevier.com/locate/smallrumres
Effects of vitamin E supply during late gestation and early lactation upon colostrum composition, milk production and quality in nutritional restricted ewes C.A. Rosales Nieto a,∗ , C.A. Meza-Herrera b , F.J. Morón Cedillo c , M.J. Flores Najera d , H.G. Gámez Vázquez a , V. Cuevas Reyes e , S.M. Liu f a
Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias, Campo Experimental San Luis, San Luis Potosí 78431, Mexico Universidad Autónoma Chapingo, Unidad Regional Universitaria de Zonas Áridas, Universidad Autónoma Chapingo 35230, Mexico c Facultad de Agronomía y Veterinaria, Universidad Autónoma de San Luis Potosí, San Luis Potosí 78321, Mexico d Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias, Campo Experimental Zacatecas, Calera de Víctor Rosales, Zacatecas 98500, Mexico e Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias, Campo Experimental Valle de México, 56250 Mexico f UWA Institute of Agriculture, The University of Western Australia, Crawley, WA 6009, Australia b
a r t i c l e
i n f o
Article history: Received 21 July 2015 Received in revised form 23 September 2015 Accepted 24 September 2015 Available online 30 September 2015 Keywords: Nutritional restriction Vitamin E Colostrum composition Milk production and composition
a b s t r a c t The aim of this study was to test if supplemental vitamin E during late gestation and early lactation to ewes facing a moderate nutritional restriction and suckling lambs from different litter size and sex would affect colostrum composition and milk yield and composition. Mature Rambouillet ewes (n = 37, 22◦ N) receiving 70% of energy and 80% of protein requirements were randomly assigned to either of two treatments: intramuscular injections of vitamin E (VitE; n = 20, 4 IU vitamin E kg−1 of live weight) in weekly intervals from 50 days before partition until 60 days of lactation, and control (CON; n = 17, without VitE treatment). While colostrum protein and fat concentrations did not differ between treatments (P > 0.05), lactose content favoured to the VitE-ewes (1.9% vs. 1.2%, P < 0.001). Colostrum protein concentration was affected by litter size favouring to twin lambs (14.3% vs. 17.3%, P < 0.05). In addition, litter size tended to affect lactose content, favouring to those ewes suckling twins (1.4% vs. 1.8%, P = 0.08). The average milk yield was 2039 g day−1 , without differences (P > 0.05) between treatments and litter size. The average milk concentrations of protein, lactose and solids-non-fat did not differ (P > 0.05) between treatments. Yet, milk fat content favour to the VitE-ewes (5.7% vs. 5.2%, P < 0.05). Milk concentrations of protein, fat, lactose and solids-non-fat were not affected (P > 0.05) by litter size. Non-significant treatment × litter size interactions (P > 0.05) were observed for milk yield, milk compositions of protein, fat and lactose and solids-non-fat. When the nutritional requirements are not met, treatment of vitamin E to ewes during late gestation and early lactation might be an strategy to improve the quality of both colostrum (>lactose) and milk (>fat). © 2015 Elsevier B.V. All rights reserved.
1. Introduction Maternal undernutrition during pregnancy impairs fetal nutrient supply and, depending on the level of restriction, may cause fetal losses or it may compromise the growth rate of lambs (Rumball et al., 2009; Jenkinson et al., 2012; Meza-Herrera and Tena-Sempere, 2012). Furthermore, maternal undernutrition is also associated with reduced colostrum and milk production (O’Doherty and Crosby, 1996; Nørgaard et al., 2008). Newborn’
∗ Corresponding author. E-mail address: nieto [email protected] (C.A. Rosales Nieto). http://dx.doi.org/10.1016/j.smallrumres.2015.09.014 0921-4488/© 2015 Elsevier B.V. All rights reserved.
colostrum intake is associated with survival and daily weight gain (Meza-Herrera and Tena-Sempere, 2012; Decaluwé et al., 2014; Hernández-Castellano et al., 2015). Therefore, failure to produce sufficient colostrum and milk, reduces maternal bond (Dwyer et al., 2003) and increases lamb mortality (Scales et al., 1986; Hashemi et al., 2008), with twin born lambs being the most at risk (Coop et al., 1972). Undernutrition also affects cell-mediated immunity, which is responsible for protection against several infections (McFarlane and Hamid, 1973). Vitamin E functions primarily as an antioxidant and maintenance of immune function (Burton et al., 1980; Turner and Finch, 1990). Inclusion of vitamin E in the diet has been associated with improvements in both immune competence and animal
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performance (Finch and Turner, 1996). Transfer of nutrients from dam to offspring occurs either by placental transfer or through colostrum/milk consumption. Yet, since vitamin E does not cross the placenta in any appreciate amount, newborns are highly susceptible to vitamin E deficiency if ewes have low vitamin E status (van Saun et al., 1989). Thus, pre-partum treatment of vitamin E is very important to provide to newborns sufficient amounts of vitamin E both in colostrum and milk (Hidiroglou, 1989; Njeru et al., 1994; Cuesta et al., 1995). Lambs reared by ewes treated with vitamin E in late gestation have shown a better productive performance (Koyuncu and Yerlikaya, 2007). However, it is not known whether vitamin E treatment in late gestation and during lactation will have the same effect when protein and energy requirements are not met; a recurrent scenario observed during late gestation and early lactation in marginal small ruminant production systems (Gonzalez-Bulnes et al., 2011; Meza-Herrera and Tena-Sempere, 2012). Based on that rationale, we tested whether supplemental vitamin E during late gestation in ewes facing a moderate nutritional restriction and suckling lambs from different litter size would affect colostrum composition and milk production and composition.
Table 1 Ingredient composition (as % in diet, DM basis), nutrient composition (DM basis) and nutritional requirement (NRC) of the experimental diet offering of gestation diet for a 60-kg ewe. Parameter
NRC requirement
Ingredient composition (% in diet) Alfalfa hay Oat hay Maize silage Nutrient composition CP (%) ME (Mcal/kg) Calcium (%) Phosphorus (%)
10.7 2.1 0.35 0.23
Experimental diet (as fed basis) 24.2 45.5 30.3 8.9 1.5 0.35 0.23
Lambs were weighed with a Torino® hanging scale with a capacity of 10 kg and a minimal graduation of 20 g. Ewes were weighed with a Ohaus Defender® digital scale with a capacity of 150 kg and a minimal graduation of 300 g.
2. Materials and methods
2.2. Sample collection and analysis
The experimental procedures reported in the current paper complied with the Official Mexican Rule for the technical specifications for the production, care and use of laboratory animals (NOM-062-ZOO-1999; SAGARPA 2001).
Immediately after parturition, a sample (about 10 mL) of colostrum was obtained by hand from one half of the udder. Samples from each ewe were kept in a plastic vial with a preservative of 0.6 mg mL−1 potassium dichromate and then frozen at −20 ◦ C until analysis for colostrum constituents. Colostrum samples were analysed for protein, fat and lactose using a Milkoscan 133B (Foss Electric, Hillerød, Denmark). One week after parturition, milk production and quality were measured weekly. The ewes were milked prior feeding on the same day of the week and starting at the same time, using the oxytocin protocol (McCance, 1959; Bencini, 1995). In brief, the ewes were drafted from the lambs, penned separately, and then hand-milked. To elicit milk let-down, ewes received an intramuscular injection of 3 mL of commercially available product and contained 20 IU mg−1 oxytocin (PiSA agropecuaria, Hidalgo; Mexico); the amount of oxytocin administrated was selected according to manufacturer’s guidelines. After five minutes, ewes were milked and the time of the first milking was recorded. The ewes were re-milked approximately 3 h later, in the same order as the initial milking, following the same oxytocin protocol. The weight of the milk collected at the second milking and the time between milkings were recorded to obtain an estimate of milk production per day. A sample (10 mL) of milk from each ewe was preserved with 0.6 mg mL−1 potassium dichromate and then frozen at −20 ◦ C until analysis of milk composition. After the second milking, the lambs and the ewes were reunited in their pen. Milk composition (protein, fat, lactose and solids-non-fat) was determined using a Milkoscan 133B (Foss Electric, Hillerød, Denmark).
2.1. Location, animals, management, treatments and feeding The study was conducted at the Faculty of Agronomy and Veterinary, University of San Luis Potosi, Mexico (22◦ N). Multiparous pregnant Rambouillet ewes (n = 37 ewes, ≥3 years old and ≥2 lactations) born and raised in these facilities mated to a single Rambouillet sire, of proven libido and fertility. During the mating period, the exact date of mating was recorded by the assistant. Starting on the last third of pregnancy (d-50), ewes were randomly divided in two treatments: (1) control (CON; n = 17, no vitamin E treatment) and (2) vitamin E-supplemented (VitE; n = 20, receiving 4 IU vitamin E kg−1 of live weight. VE-injections considered a commercial product and contained 27.2 IU mg−1 of ␣-tocopherol (vitamin E; Laboratorio Tornel, Estado de Mexico; Mexico). Intramuscular injections were given weekly on the same day of the week and at (0800 h), from late gestation (d-50) to early lactation (d + 60). Ewes were allocated by treatment in a separate common pen and after lambing, ewes and lambs were allocated in a separate common pen according to their treatment. Lambs were maintained with their dams until weaned. Ewes were fed alfalfa hay, oat hay and maize silage and each ewe (with lambs) was fed this diet in an individual pen (2.0 × 2.0 × 1.0 m), no more than 1 h and half, until total feed disappearance. The ewes spent the rest of the day in their respective common pen where clean water and minerals were provided ad libitum. In order to simulate a marginal rangeland scenario, treatment diet considered around of 70% and 80% of the requirements for energy and protein, respectively (NRC, 2007; Table 1). Dietary treatment started the last third of pregnancy (d-50) and continued until day 60 of lactation (d + 60). Diet and concentration of vitamin E treatment was adjusted every 14 days based on the recorded live weight. Each ewe gave birth to one or two lambs, 10 single and 10 set of twins from VitE and 12 single and 5 sets of twins from control, for a total of 52 lambs born, 21 females and 31 males. At lambing, birth weight, sex and litter size were recorded; Ewe´ıs live weight was recorded every two weeks from the last third of pregnancy (d-50) to day 60 of lactation (d + 60).
2.3. Statistical analysis Data analyses considered the SAS statistical package SAS version 9.3 (SAS Institute Inc., Cary, NC, USA). The data for colostrum quality (protein, lactose and fat) and milk quantity (at 24 h) and quality (fat, protein, lactose, solids-non-fat) were analysed using linear mixed model procedures and estimation technique of restricted maximum likelihood (PROC MIXED). Fixed effects were treatments and litter size. Lamb birth weight was included as covariate; ewes were considered as a random effect. The interaction between treatment and litter size was included in each model.
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Table 2 Colostrum composition (protein, fat and lactose) of sheep received vitamin E supplementation (VitE) or control nursed single or twin lambs1 .
Protein (%) Fat (%) Lactose (%)
VitE
Control
SEM
P values
16.2 9.9 1.9
14.3 8.9 1.2
1.8 1.3 0.18
0.15 0.27 0.001
Litter size
Single (n = 22)
Twin (n = 30)
SEM
P values
Protein (%) Fat (%) Lactose (%)
14.6 9.7 1.5
17.3 8.9 1.8
1.9 1.4 0.25
0.05 0.4 0.08
1 Birth weight of the lambs and interactions between treatment and little size were included in the analyses. For little size, data are combined for treatment and for males and females.
Table 3 Milk production and composition (protein, fat, lactose, density and solids-non-fat) for ewes received vitamin E supplementation (VitE) or control nursed single or twin lambs1 . VitE
Control
SEM
P values
Milk production (g/day) Protein (%) Fat (%) Lactose (%) SNF (%)
2202 3.6 6.1 5.4 10
1983 3.8 5.4 5.7 10.5
499 0.15 0.4 0.2 0.4
0.5 0.18 0.04 0.2 0.16
Litter size Milk production (g/day) Protein (%) Fat (%) Lactose (%) Solids-Non-Fat (%)
Single (n = 22) 2008 3.7 5.5 5.5 10.2
Twin (n = 30) 2170 3.8 6.1 5.6 10.3
489 0.18 0.5 0.27 0.5
0.6 0.4 0.1 0.5 0.6
1 Live weight of the ewes, lamb birth weight, and interactions between treatment and little size were included in the analyses. For little size, data are combined for treatment and for males and females.
3. Results 3.1. Colostrum composition The average colostrum protein concentration was 15.5 ± 0.6%, being affected by litter size (P < 0.05). Yet, protein content was not affected by treatments (P > 0.05) (Table 2). The interaction of treatment × litter size was not significant (P > 0.05). The average for colostrum fat concentration was 9.5 ± 0.4%, with no differences between treatments (P > 0.05), neither ewes suckling single or twin lambs (P > 0.05) (Table 2). The interaction of treatment × litter size was not significant (P > 0.05). The average colostrum lactose concentration was 1.6 ± 0.08%, observing a treatment effect (P < 0.001; Table 2). Interestingly, there was observed a trend (P = 0.08) for more lactose content in those ewes suckling twins, 1.4% for singles and 1.8% for twins. The interaction between treatment × litter size was not significant (P > 0.05). 3.2. Milk production and composition The average amount of milk produced was 2039 ± 73 g day−1 . No differences (P > 0.05) were observed neither between treatments nor litter size (P > 0.05; Table 3). Live weight of the ewes did not affect milk production (P > 0.05; Fig. 1). The average milk protein concentration was 3.6 ± 0.03%, without differences (P > 0.05) between treatments. In the same way, milk protein content was not affected (P > 0.05) by litter size (P > 0.05; Table 3). The average concentration of fat in the milk was 5.5 ± 0.1%, being affected (P < 0.01) by treatment, favouring to the VitE ewes (5.7% vs. 5.2%) but without differences between litter size (P > 0.05) (Table 3).
Fig. 1. Weekly milk production (solid line) and live weight (dashed line) of ewes that received vitamin E supplementation (VitE; black) or control (grey) during lactation.
The average concentration of lactose in the milk was 3.6 ± 0.03%, without differences between treatments (P > 0.05) and litter size (P > 0.05) (Table 3). The average content of solids-non-fat in milk composition was 10.1 ± 0.09% and similarly to the other milk components, no differences occurred between treatments, neither by litter size (P > 0.05; Table 3). The interaction of treatment × litter size was not significant for milk production, concentration of protein, fat and lactose in milk and content of solids-non-fat in milk composition (P > 0.05). Weekly changes in milk production (g day−1 ) and the live weight of ewes are shown in Fig. 1. Date of lactation affected the milk protein percentage (P < 0.05), fat content (P = 0.07), lactose content (P < 0.05), and the solids-non-fat content (P < 0.05). Live weight of the ewes did not influence concentrations of protein, fat, lactose and the solids-non-fat in milk. 4. Discussion According to our results, when nutritional requirements are not met, treatment to ewes with vitamin E during late gestation and early lactation could be an effective strategy to increase the quality of both colostrum (>lactose) and milk (>fat). Such outcomes are of key importance from an energetic view point during the early life (colostrum) and prior weaning (milk) of lambs whose mothers faced a mild nutritional restriction. Our results are in line with Capper et al. (2006) who observed that treatment of vitamin E in late pregnancy improved the quality of colostrum. Additionally, we observed that the composition of colostrum was not affected by the undernutrition subjected in the ewes, since our results are within the range to those reported elsewhere in Merino-type ewes (Banchero et al., 2004). This is an important issue, because foetal requirements for energy and protein are significant, particularly during the last trimester of gestation (Sykes and Field, 1972; Robinson, 1977). Therefore, our results suggest that concentration of major constituents in colostrum can be influenced by vitamin E treatment even when ewes face a nutritional restriction of protein and energy during late pregnancy. Little is the information about the effect of treatment of vitamin E on colostrum quality (e.g. protein, lactose, and fat content). Since vitamin E does not cross the placenta in any appreciable amounts, its content is concentrated in colostrum (van Saun et al., 1989). The increased concentration of vitamin E in colostrum improves the immune system of the newborn by increasing the amounts available of immunoglobulin (Finch and Turner, 1996; Rooke et al., 2004). To better understand the mechanism by which colostrum quality may be increased by treatment of vitamin E, more studies are required. Yet, we hypothesized that such results may be due to the antioxidant effects of vitamin E upon the immune system, since vitamin E treatment reduced both symptoms and incidence of
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disease in ruminant (Reddy et al., 1986). Therefore, if the maternal immune system during gestation is competent, vitamin E treatment may promote the partitioning of additional nutrients towards the udder system, favouring the quality of colostrum. In addition, we observed an increased in the concentration of lactose in colostrum in those ewes treated with vitamin E. Lactose synthesis regulates the amount of colostrum and milk segregated and it has been reported that lactose concentration in colostrum is reduced and increases over time (Linzell and Peaker, 1974; Zabielski et al., 1999; Kehoe et al., 2007). Although, we did not measure production of colostrum, it is probably that the treatment of vitamin E increased colostrum production in treated ewes hence the increase in lactose concentration observed in these ewes. Moreover, immune competence of the ewes may had helped to moderate the negative effect of maternal nutritional restriction upon the quality of colostrum. Therefore, treatment of vitamin E in late pregnancy may be feasible alternative to improve the quality of colostrum and, consequently, decrease the perinatal mortality in marginal sheep production systems. Although, vitamin E treatment neither increased milk production nor the concentrations of protein, lactose and solids-non-fat in milk, such treatment certainly increased the concentration of fat. Extending our results, Casamassima et al. (2014) in Lacaune ewes and Liu et al. (2008) and Tufarelli and Laudadio (2011) in dairy cows, observed an increase in milk fat due to treatment of vitamin E. The lack of any effect of treatment of vitamin E on milk production, milk protein and milk lactose agrees with other studies (Focant et al., 1998; Baldi et al., 2000; Kay et al., 2005). Moreover, the extended maternal undernutrition during pregnancy and lactation appeared not to affect milk production and quality since our results are in line with Ochoa-Cordero et al. (2002). Certainly, the ewes used by Ochoa-Cordero et al. (2002) were genetically similar, under intensive management and proper nutrition; nevertheless, they observed quite similar values for milk yield and concentration of fat, lactose and solids-non-fat in milk as reported in this experiment. Therefore, treatment of vitamin E in late pregnancy and early lactation may moderate the negative effects of maternal undernutrition upon milk production and quality. Despite milk production did not reach significant difference between groups, milk production increased 10% in the VE-ewes during lactation. Extending our results, Casamassima et al. (2014) in sheep, Tufarelli and Laudadio (2011) in goats and Lacetera et al. (1996) in cows observed a similar increase of 10% in milk yield in those vitamin E treated animals. The mechanism by which milk production and quality increased by vitamin E treatment is unclear, as we previously hypothesized, this could be due to the effects of antioxidant vitamins upon the immune system. Hence, the partitioning of additional nutrients towards milk production and quality may have occurred in the VitE-supplemented group. This could have been a positive carry-over effect from gestation upon lactation. The increase in milk fat, probably, was due to the fact that vitamin E is capable of reducing the extent of diet-induced milk fat depression as previously hypothesized (Lacetera et al., 1996; Pottier et al., 2006; Tufarelli and Laudadio, 2011). We did not observe any difference regarding the effect of live weigh of ewes on milk production and composition, yet some studies have pointed out that heavier ewes produce more milk than lighter ewes (Burris and Baugus, 1955; Bencini and Pulina, 1997). To conclude, when nutritional requirements are not met, supplementing ewes with vitamin E during late gestation and early lactation might be an effective strategy to improve the quality of both colostrum (>lactose) and milk (>fat). In addition, and quite interesting, colostrum protein and lactose contents were affected by litter size favouring to twin lambs. Such a strategy exerted by those ewes lambing larger litters seems to be a physiologic, and may be behavioural, wise strategy to counteract any possible
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