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High mineral and vitamin E intake by pregnant ewes lowers colostral immunoglobulin G absorption by the lamb¹

T. M. Boland^*, N. Keane^*, P. Nowakowski, P. O. Brophy^* and T. F. Crosby^*,2

^* Department of Animal Science, University College Dublin, Newcastle, Ireland; and and Department of Sheep Breeding, Wroclaw, Poland

	Abstract

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A 2 x 2 factorial arrangement of treatments with 78 mature ewes was used to evaluate the effects of supplementing the pregnant ewe’s diet with high levels of minerals and vitamin E on immunoglobulin G (IgG) absorption by the lamb and whether any altered efficacy of IgG absorption was due to the colostrum or to the lamb. The ewes were estrus-synchronized in October and housed in wk 10 of gestation. In the final 7 wk of gestation, a grass silage-based diet, offered ad libitum, was supplemented with 500 g of a 19% CP concentrate, and from 1 wk later until lambing, half the ewes was offered 48 g of a mineral/vitamin supplement containing 6.5 g of Ca, 4.9 g of P, 5.9 g of Mg, 4.0 g of Na, 790 mg of Zn, 3.5 mg of Se, 40 mg of I, 200 mg of Mn, 20 mg of Co, and 40 IU of vitamin E. At birth, the lambs were allocated to one of four treatments in a 2 x 2 factorial arrangement, with lamb origin and colostrum origin as the two factors. The lambs born to ewes not offered the mineral supplement were fed colostrum obtained from their own dams or from ewes in the mineral-supplemented treatment, whereas lambs born to ewes given supplemental minerals were fed colostrum obtained either from their dams or from ewes in the control treatment. The ewes were milked at 1, 10, and 18 h postpartum and the lambs were fed using a stomach tube. A 5-mL blood sample was taken from each lamb at 24 h postpartum for IgG analysis. The level of fecal adhesion to the upper tail/rump area of the lamb was subjectively scored at 72 h postpartum. There was no difference in gestation length, lamb birth weight, colostrum yield, or IgG production (P = 0.16 to 0.82). When ewes were fed supplemental minerals, the serum IgG content of the progeny was lower than in their control counterparts (6.8 vs. 16.1 g/L; P < 0.001), regardless of whether the lamb received colostrum from ewes with or without access to supplementary minerals. The difference in serum IgG concentrations at 24 h postpartum was a direct reflection of a compromised efficiency in IgG absorption. The progeny of ewes with access to minerals had higher (P < 0.05) levels of fecal adhesion, which was not related to the origin of the colostrum, indicating altered digestive function in these lambs. We conclude, using the sheep as a model, that high mineral intakes in late pregnancy not only lower serum IgG concentrations in the lamb, but also that high mineral intakes result in the neonate being preprogrammed at birth so that it is born with a compromised ability to absorb colostral IgG.

Key Words: Colostrum • Element • Immunoglobulin • Immunoglobulin Absorption • Sheep

	Introduction

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Mineral elements, considered essential for sheep, consist of seven major elements and 12 trace elements (Underwood, 1981; Lee et al., 2002). The concentration of these elements usually must be maintained within narrow limits if the functional and structural activities of the tissues are to be safeguarded, and the growth, health, and productivity of the animal are to remain unimpaired (Underwood and Suttle, 1999). There are no reports in the literature relating to the toxic effects of minerals on immunoglobulin (Ig) transfer from colostrum to the neonate. The main immunoglobulin subclass present in the ewe colostrum is IgG (Smith et al., 1975). We have recently shown that high mineral/vitamin intakes by pregnant sheep lower both the lamb serum IgG values and the efficiency of IgG absorption (Boland et al., 2004a). Unlike the situation in the human (Van de Perre, 2003), the placenta acts as a barrier to the in utero transmission of Ig in ungulates and the lamb (O’Doherty and Crosby, 1997), calf (Schultz et al., 1973), piglet (Porter, 1969), and foal (Rejnek et al., 1973); all are born with negligible quantities of IgG in the serum. These animals are therefore reliant on the successful transfer of colostral IgG to provide them with immunity in the early days and weeks of life, and following the ingestion of colostrum an increase in serum IgG titers was observed in these ungulates (Machado-Neto et al., 1987; O’Doherty and Crosby, 1997; Quigley et al., 2000). We hypothesize that high mineral plus vitamin E intakes by ewes lower the lamb’s ability to absorb colostral Ig. The current study was undertaken to determine whether high mineral/vitamin intakes result in the colostrum being altered, rendering its IgG unavailable to the lamb, or whether the lamb is preprogrammed by the time it is born to have a lowered ability to transmit colostral IgG into its blood circulatory system.

	Materials and Methods

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Animals and Management

The study was conducted over 2 yr. Seventy-eight mature (2 to 5 yr of age), mainly Suffolk-cross ewes, 18 in yr 1 and 60 in yr 2, with an initial BW of 71 ± 7.8 kg, were allocated to this study at wk 7 before the predicted mean lambing date in March. There were 50 single-bearing and 28 twin-bearing ewes. The ewes were estrus-synchronized the previous October using intravaginal progestagen pessaries (Chronogest, Intervet Ltd., Dublin, Ireland) followed by an i.m. injection of pregnant mare serum gonadotropin (Folligon, Intervet Ltd.). The ewes were joined with fertile rams 48 h later. Mid-day (1200) on the day of ram introduction was designated as h 0 of gestation. Following mating, the ewes remained outdoors on permanent grassland until they were group-housed in early December. From housing until lambing, the ewes were offered grass silage ad libitum. The silage was harvested in late May using a precision chop harvester following a 24-h wilt. No additive was used in the preservation of the mainly perennial ryegrass sward. The ewes were shorn and pregnancy scanned in wk 9 and 10 of gestation, respectively. In the final 7 wk of gestation, the basal diet of grass silage was supplemented with 500 g of a 19% CP concentrate daily per ewe. The concentrate included barley (20%), molassed sugar beet pulp nuts (13%), corn gluten meal (20.6%), cane molasses (7.6%), malt combings (7.5%), canola rape extract (12.4%), corn cob pellets (5.1%), West African cotton extract (5.0%), high-protein soybean meal (4.1%), and micronized corn (2.5%) plus 2% minerals/vitamins (as-fed basis). The nutrient content of the grass silage and concentrate is presented in Table 1.

At 7 wk before the expected mean lambing date, the ewes were weighed (initial BW) and allocated to one of two treatments, with each treatment balanced for ewe breed, age, scanned litter size, BW, and BCS (using a scale of 1 to 5; Jeffries, 1961). The ewes were then transferred to 1.4-m² timber-slatted individual pens. Half of the ewes were offered a grass-silage-based diet supplemented with 500 g of concentrate only (C), whereas the remaining half was offered the same dietary ingredients as in C, in addition to a daily allowance of 48 g of a mineral/vitamin supplement (M; Table 2). The 48-g level equates to the level offered to ewes in a recently reported study (Boland et al., 2004a) and approximates the mineral/vitamin intake of 100 g of mineral block recorded for group-housed single and twin-bearing ewes when the blocks were offered ad libitum in a commercial situation (Crosby et al., 2004). Fresh silage and water were available at all times, and the concentrate allowance was offered once daily each morning. At the time of concentrate feeding, the mineral/vitamin supplement was added to the individual ewe’s concentrate allowance on a daily basis and offered to ewes in their individual pens.

Colostrum and Immunoglobulin

Continuous supervision was provided during the lambing period. At birth, the lambs underwent navel treatment with iodine to prevent joint ill, a disease associated with bacterial infection of the joints, after which they were weighed and tagged with an individually numbered ear tag. The lambs were weighed again 5 wk later. The time and date of parturition was recorded to calculate gestation length. At the time of parturition, the ewe’s udder was covered with an apron to prevent suckling by their progeny and the ewes were subsequently hand milked at 1, 10, and 18 h postpartum. Before milking, 1 mL of oxytocin (Oxytocin-S; Intervet Ltd.) was administered i.m. to ensure complete milk let down (Doney et al., 1979). After 3 min, each side of the udder was completely milked out by hand and colostrum yield recorded. A 5-mL colostrum sample was taken at each milking and frozen at –20°C until analyzed for IgG concentration, using single radial immunodiffusion kits (Bethyl Laboratories, Montgomery, TX) by the method of Fahey and McKelvey (1965). Following each milking, the lambs were fed fresh colostrum at a rate of up to 50 mL/kg of lamb birth weight, depending on the colostrum yield of individual ewes. When less than 20 mL of colostrums/kg of birth weight was available, the lambs were fed substitute colostrum and removed from further IgG studies. In total, three lambs from the C ewes and one lamb from the M ewes were removed. A 5-mL blood sample was taken from lambs at 24 h postpartum using jugular venipuncture and collected in nonheparinized Vacutainer tubes (Becton Dickinson, Plymouth, U.K.). Following storage at 4°C for 24 h, the blood samples were centrifuged to obtain the serum fraction, and the serum frozen until analyzed for IgG concentrations using the zinc sulfate turbidity test (McEwan et al., 1970). The radial immunodiffusion plates used in this study measure IgG only, whereas the zinc sulfate turbidity test measures total immunoglobulin content. Consequently, the Ig concentrations of the serum were decreased by 9% to equate with the IgG only values (Larson et al., 1974) measured in colostrum. When calculating IgG absorption, it was assumed that lamb blood plasma volume at 7.5% of BW is similar to that of the human (Ganong, 1977). The following equation was then used to calculate the IgG absorption efficiency:

Fecal Adhesion

Any adhesion of fecal material to upper tail/anal region of the lamb was subjectively scored at 72 h postpartum to obtain a "fecal adhesion" or "soil score" for each lamb. This characteristic was subjectively scored on a scale of 1 to 4 (1 = no fecal adhesion, 2 = light fecal adhesion, 3 = moderate fecal adhesion; and 4 = heavy fecal adhesion). We used the fecal adhesion score because we observed in earlier studies (Keane, 2001) that when ewes had ad libitum access to mineral blocks in late pregnancy, their progeny displayed a higher level of tail-end soiling by the time they were 3 to 4 d old.

Statistics

Ewe data were analyzed using PROC GLM of SAS (v. 6.12; SAS Inst., Inc., Cary, NC). The model included the effects of mineral supplementation, year, and initial ewe BW as a covariate. The lamb data were analyzed as a 2 x 2 factorial using PROC GLM. The two factors were lamb origin and colostrum origin. The model used to analyze the IgG and growth data included the effects of year, lamb origin, colostrum origin, and interaction between lamb origin and colostrum origin.

	Results

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There was no effect (P = 0.23 to 0.49) of year on any of the data measured; hence, the data presented were averaged over years. Flock health was good throughout the feeding period, and there were no treatment ill health effects observed in any of the ewes during pregnancy. The mineral treatment lowered silage DMI (0.92 vs. 0.98 kg; P < 0.05). As expected, the M ewes had higher mineral intakes than did the control ewes (P < 0.001), with the increase in mineral intakes attributable to the mineral supplement (Table 3). The silage/concentrate portion of the diet supplied 48% of the major element intake and 11.3% of the trace element intake. The average gestation length was 147.8 ± 0.30 d, which is normal for winter-shorn mature ewes. Mineral supplementation had no effect on gestation length (P = 0.52) or on lamb birth weight (P = 0.63). Similarly, there was no effect of treatment on colostrum yield at 1, 10, or 18 h postpartum (P = 0.09 to 0.53) or on total colostrum yield to 18 h postpartum (P = 0.32; Table 4).

	Discussion

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The major findings of this study indicate that the diet offered to the ewe in late pregnancy can result not only in the lamb having a lower serum IgG value, but that the lamb seems to be preprogrammed in utero and its ability to absorb colostral antibodies is compromised in the first 24 h of life. These findings, which potentially have major implications, were unexpected, and to our knowledge, have not been reported previously in the literature. The progeny of the mineral/ vitamin E-supplemented ewes had a serum IgG level at 24 h postpartum that was approximately 40% of their nonsupplemented counterparts (6.8 vs. 16.1 g/L).

We have recently shown that high mineral intakes do not affect colostral IgG production in the first 18 h after birth (Boland et al., 2004a; Crosby et al., 2004). In sheep, IgG constitutes 92% of the total colostral Ig content, whereas approximately 6% is IgA and 2% is IgM (Smith et al., 1975). Once the lamb is 24 h old, transport of IgG across the intestinal epithelium is virtually complete (Parker and Nicol, 1990), with no further possibility of significant IgG absorption from colostrum. Such a decrease in the level of circulating antibodies renders these animals more susceptible to disease (Guinan et al., 2004). Others have reported that the type of substitute colostrum can affect lamb serum IgG concentration (Goodman et al., 2004). In the present study, colostral yield and IgG concentration in the colostrum were similar in all treatments. This response suggests that the IgG contained in the colostrum produced by the M ewes was available to the lambs for transmission into their blood stream; however, the lambs were incapable of doing this efficiently if their dam’s diet had been supplemented with minerals + vitamin E of the kind and level used in the present study. We postulate that the lamb is preprogrammed, most likely in utero, for this decreased ability to transmit colostral IgG, and that the decrease is brought about either by the accelerated closure of the gut to IgG absorption or by the fact that the functioning of the absorptive process is altered so as to operate at a greatly reduced level over the time period when absorption is normally high. Furthermore, the increased level of fecal adhesion in the lambs with the lowered serum IgG concentrations indicates that there may be a breakdown in the digestive process in the gut of these lambs, resulting in incomplete digestion of the colostrum and/or an accelerated rate of passage of colostrum through the intestine.

Colostrum is a laxative (Campbell, 1974) that helps remove the meconium from the gut of the newborn lamb (Treacher, 1973). Although the characteristics of colostrum normally give efficient passage through the digestive system, the phenomenon of IgG absorption is known to take place quickly, with IgG present in the serum of the lamb as early as 4 h after feeding (Yvon et al., 1993). Therefore, we believe it to be unlikely that the compromised IgG absorption in lambs from M ewes could be due solely to an increased rate of digesta passage in affected lambs. Initially we were surprised that a 6-wk supplementation period with minerals + vitamin E at the end of the gestation period would elicit such a dramatic response in preprogramming the lamb because it is fully accepted that cell differentiation takes place at a much earlier stage in pregnancy. Ongoing studies at this laboratory indicate that supplementation with a high level of minerals + vitamin E for just the final 2 wk of pregnancy can elicit an equally pronounced response in terms of decreased serum IgG concentrations (Guinan et al., 2004), and that a similar result will not occur following a 2-wk mineral + vitamin E supplementation period earlier in pregnancy.

Dietary supplementation with major and trace elements is common practice in animal production (Church, 1991), but we express major concerns that excessive dietary inclusions may have significant implications in terms of increased disease susceptibility and lowered performance in many animal species. Although this study concentrated on IgG absorption in the lamb, where IgG is the predominant subclass present in the ewe’s colostrum (Smith et al., 1975) and is normally efficiently transported across the intestinal epithelium into the neonatal circulation, the situation is similar with the cow (Porter, 1971), sow (Karlsson, 1966), mare (Rumbaugh et al., 1979), and bitch (Ricks et al., 1970), and this predominance of IgG is reflected in the serum of their offspring in the hours and days following the consumption of colostrum.

In the puppy and kitten, in addition to the farm animals, IgG is transported across the intestinal epithelium into the neonatal circulation. This transport is located at the duodenal and jejunal level, where enterocytes express a surface membrane receptor able to bind to the fragment crystallizable portion of IgG and to facilitate transcytosis of IgG. In these animals, fragment crystallizable -R, which is very similar to the placenta receptor responsible for the active transplacental transfer of IgG in humans, binds to IgG but not to other isotypes (Van de Perre, 2003). If, as it seems in the current study, the transport mechanism has been upset, and because fragment crystallizable -R is very similar to the placenta receptor responsible for the active transplacental transfer of IgG in humans, we raise the question as to whether transplacental IgG transfer in the unborn child could be lowered as a result of high mineral intakes by the mother.

In the lamb, it is possible, and indeed we believe likely knowing the large molecular size of other Ig subclasses, that had we measured intestinal transfer of IgA and IgM, we would have observed a similarly compromised absorption of these immunoglobulins. By extension, as there is quite widespread mineral supplementation in animal production programs, of major importance is that analogous results may be occurring in other neonatal ungulates, including the calf, foal, and piglet, given the similar reliance these animals have on the transmission of colostral Ig for passive immunity in early life. Although the puppy (Schneider and Szathmary, 1939) and kitten (Harding et al., 1961) acquire antibodies both before and after birth, the latter is considered more important, and similar problems, as witnessed in the lamb, cannot be ruled out in these young carnivores. Collectively, these animals represent the major species of agricultural importance, the main companion animal groups, and the leading sports animal in the western world. Any decrease in the serum concentrations of IgG immediately after birth may have serious economic implications for the producer and health and welfare implications for the animal in terms of increased disease and mortality. Molecular technology has been applied to studies relating to mineral metabolism and function (O’Dell and Sunde, 1997), advancing our understanding of the complex processes by which some minerals are transported across membranes. Given the huge importance placed on lowering mortality, especially in the neonate of all species, including the human, and the ever-increasing high animal welfare standards being demanded, the factors responsible for the preprogramming of the lamb’s digestive system, which thereby compromise the lamb’s ability to absorb IgG, should be further researched by groups with multidisciplinary inputs, including the use of genomic technology, to chart the mode of action responsible for this compromised IgG absorption.

Recent reports suggest that high vitamin E inclusion (400 mg of vitamin Eewe^–1•d^–1) in the diet of the ewe during late pregnancy had no negative effects on lamb serum IgG concentration and hence IgG absorption efficiency (Daniels et al., 2000). Thus, we assume that the vitamin E inclusion in the present formulation is not responsible for the lowered efficiency of IgG absorption. Although in the present study the effects of the individual elements contained in the mineral supplement on the IgG absorptive process in the newborn lamb were not examined, preliminary evidence from ongoing studies suggests that the high iodine intake might be responsible for decreased IgG absorption (Boland et al., 2004b). Iodine is a constituent of the thyroid hormones, which have been shown to affect the absorption of IgG in both the lamb and calf. Continuous infusion of thyroid hormones during the last 12 d of gestation in the ovine fetus decreased the rate of blood IgG appearance after colostrum feeding and the number of jejunal cells filled with IgG1 12 h postpartum (Cabello et al., 1983). These authors suggested that the infusion of thyroid hormones lead to the premature closure of the intestinal permeability to IgG1. In the calf, a hyperthyroid state at birth decreases the period of intestinal absorption of Ig (Cabello and Levieux, 1978). These findings suggest a link between iodine nutrition of the dam and decreased IgG absorption in the progeny, although further study is required to confirm whether iodine is the causal element in the present study and if so, to identify the mechanism by which it acts.

	Implications

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Lambs experienced lowered immunoglobulin G absorption when pregnant ewes were given free access to mineral blocks and the block intake was variable and frequently high. Because there is widespread mineral supplementation in animal production, of major importance is that analogous results may be occurring in other neonatal ungulates, including the calf, foal, and piglet. Such a response could have serious economic implications for producers, and health and welfare implications for animals in terms of increased disease and mortality. Although the mineral intake in most cases did not reach toxic levels, there is a need to revisit some of the published toxicity values for specific minerals. The problem with free access minerals is that the intakes are uncontrollable, variable, and at times can clearly lead to toxic effects. These findings point to a need for more precise inclusions of minerals, related to requirements/upper tolerance levels and the control of their intake by animals.

	Footnotes

 
¹ This work was partially funded by the Irish Research Council for Science Engineering and Technologies under the Embark initiative. We thank P. Quinn, J. Callan, and S. Lott for assistance with animal care and laboratory analyses.

² Correspondence: Room G18. (phone: +353 1 716 7141; fax: +353 1 716 1103: e-mail: frank.crosby{at}ucd.ie).

Received for publication June 23, 2004. Accepted for publication January 23, 2005.

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