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Effects of organic forms of zinc on growth performance, tissue zinc distribution, and immune response of weanling pigs^1,2

E. van Heugten^*,3, J. W. Spears^*, E. B. Kegley⁴, J. D. Ward⁵ and M. A. Qureshi

^* Department of Animal Science and Interdepartmental Nutrition Program and and Department of Poultry Science and Interdisciplinary Program of Immunology, North Carolina State University, Raleigh 27695-7621

	Abstract

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This study was conducted to determine the effect of zinc level and source on growth performance, tissue Zn concentrations, intracellular distribution of Zn, and immune response in weanling pigs. Ninety-six 3-wk-old crossbred weanling pigs (BW = 6.45 ± 0.17 kg) were assigned to one of six dietary treatments (four pigs per pen, four replicates per treatment) based on weight and litter origin. Treatments consisted of the following: 1) a corn-soybean meal-whey diet (1.2% lysine) with a basal level of 80 ppm of supplemental Zn from ZnSO₄ (control; contained 104 ppm total Zn); 2) control + 80 ppm added Zn from ZnSO₄; 3) control + 80 ppm added Zn from Zn methionine (ZnMet); 4) control + 80 ppm added Zn from Zn lysine (ZnLys); 5) control + 40 ppm added Zn from ZnMet and 40 ppm added Zn from ZnLys (ZnML); and 6) control + 160 ppm added Zn from ZnSO₄. Zinc supplementation of the control diet had no effect on ADG or ADFI. Gain efficiency was less (P < 0.05) for pigs fed 80 ppm of Zn from ZnSO₄ than for control pigs and pigs fed 160 ppm of Zn from ZnSO₄. Organ weights, Zn concentration, and intracellular distribution of Zn in the liver, pancreas, and spleen were not affected (P = 0.12) by Zn level or source. Skin thickness response to phytohemagglutinin (PHA) was not affected (P = 0.53) by dietary treatment. Lymphocyte proliferation in response to PHA was greater (P < 0.05) in pigs fed ZnLys than in pigs fed the control diet or the ZnML diet; however, when pokeweed mitogen was used, lymphocyte proliferation was greatest (P < 0.05) in pigs fed the ZnMet diet than pigs fed the control, ZnLys, ZnML, or 160 ppm ZnSO₄ diets. Antibody response to sheep red blood cells was not affected by dietary treatments. Supplementation of 80 ppm of Zn from ZnSO₄ or ZnMet and 160 ppm of Zn from ZnSO₄ decreased (P < 0.05) the antibody response to ovalbumin on d 7 compared with control pigs, but not on d 14. Phagocytic capability of peritoneal exudate cells was increased (P < 0.05) when 160 ppm of Zn from ZnSO₄ was supplemented to the diet. The number of red blood cells ingested per phagocytic cell was increased (P < 0.05) in pigs fed the diet supplemented with a combination of ZnMet and ZnLys and the diet with 160 ppm of Zn from ZnSO₄. Results suggest that the level of Zn recommended by NRC for weanling pigs was sufficient for optimal growth performance and immune responses, although macrophage function may be enhanced at greater levels of Zn. Source of Zn did not alter these measurements.

Key Words: Growth • Immune Response • Macrophage Activation • Pigs • Zinc

	Introduction

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Supplementation of Zn to diets in the swine industry is often greater than levels suggested to be required (NRC, 1998). In addition, pharmacological levels of Zn are frequently included in the first diet of pigs after weaning; however, this practice may not be sustainable from an environmental perspective (van Heugten and van Kempen, 2000). Alternatively, organic complexes of Zn have been proposed to provide a more available source of Zn in chicks (Wedekind et al., 1992), although improvements in Zn availability and growth performance in pigs have not been consistently demonstrated (Hill et al., 1986; Swinkels et al., 1996; Cheng et al., 1998). Others have suggested that organic Zn complexes may be metabolized differently (Spears, 1989; Kidd et al., 1996).

Studies in turkeys have indicated a beneficial effect of zinc methionine (ZnMet) complex on immune function. Ferket and Qureshi (1992) reported increased substrate adherence potential of Sephadex-elicited abdominal exudate cells, increased phagocytic capacity of macrophages, and enhanced tumorcidal activity when 40 ppm of ZnMet and manganese methionine were added to the diet. Kidd et al. (1994a) observed increased macrophage recruitment and adherence and improved ability to clear i.v. administered Escherichia coli from blood in turkeys fed 40 ppm of supplemental ZnMet. In a subsequent trial, cutaneous basophil hypersensitivity to phytohemagglutinin-P, clearance of Salmonella arizona from the spleen, and in vitro phagocytosis of S. enteritidis by Sephadex-elicited abdominal exudate cells were improved when ZnMet was supplemented to diets of young turkeys (Kidd et al., 1994b). However, potential benefits of organic Zn complexes on the immune function of pigs have not been critically evaluated.

The objectives of this experiment were to evaluate the effects of supplementation of organic complexes of Zn or ZnSO₄ to diets containing adequate levels of Zn on weanling pig performance, tissue and cellular distribution of Zn, and immune response.

	Materials and Methods

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General Procedures
The experimental protocols used in this study were approved by the North Carolina State University Institutional Animal Care and Use Committee. A total of 96 3-wk-old crossbred ([Landrace x Yorkshire] x [Hampshire x Duroc]) weanling pigs (initial BW = 6.45 ± 0.17 kg) were blocked by weight, regardless of sex, and allotted to one of six dietary treatments (four pigs per pen, four replicates). When pigs of the same litter were allocated to the same pen, pigs were switched within block to ensure that littermates were distributed across treatments as much as possible. Pigs were housed four pigs per pen (1.73 x 0.83 m) in an environmentally controlled nursery with raised slatted flooring. Initial temperature in the nursery was 27°C and was lowered by 1°C each week. Treatments consisted of: 1) control (supplemented with a mineral premix that supplied 80 ppm of Zn from ZnSO₄; contained 104 ppm total Zn; Table 1); 2) control + 80 ppm of additional Zn from ZnSO₄; 3) control + 80 ppm of additional Zn from ZnMet; 4) control + 80 ppm of additional Zn from Zn-lysine (ZnLys); 5) control + 40 ppm of additional Zn from ZnMet and 40 ppm of additional Zn from ZnLys; and 6) control + 160 ppm of additional Zn from ZnSO₄. Diets met or exceeded NRC (1998) requirements for all nutrients for pigs of 10 to 20 kg. Feed and water were freely available throughout the study. Body weight and feed consumption were determined weekly for the 5-wk experimental period.

All cell fractionation procedures were conducted at 0 to 4°C. Tissue samples (2.5 g) of liver, spleen, and pancreas were taken and minced with scissors. Samples of each tissue were then homogenized in 15 mL of an ice-cold 0.25 M sucrose solution in a 30-mL Potter-Elvehjem tissue grinder fitted with a Teflon pestle (Fisher Scientific, Pittsburg, PA). The pestle was mechanically driven at approximately 1,000 rpm and was moved up and down a minimum of five times until all tissue was broken up.

Fractionation was conducted as previously described (Porter et al., 1961) with slight modifications. Ten milliliters of the homogenate was centrifuged at 600 x g for 10 min to separate the debris pellet containing primarily nuclei, plasma membranes, and some unbroken cells. The supernatant was collected and the pellet was gently mixed with 2.5 mL of 0.25 M sucrose and centrifuged again at 600 x g. The supernatant from the second centrifugation of the debris pellet was collected and added to the first supernatant. The debris pellet was brought up to a total volume of exactly 3 mL. The supernatants obtained from the debris pellets were then centrifuged at 8,500 x g for 10 min to collect the large granular pellet consisting of mitochondria and lysosomes. This pellet was washed as described previously and brought to a 3-mL volume. A similar procedure was followed with the second supernatant obtained from the large granular fraction, which was centrifuged at 105,000 x g to separate the microsomal pellet (endoplasmatic reticulum, golgi apparatus, and ribosomes) from the cytosol. All cell fractions were stored at -20°C until they were analyzed.

Different fractions were verified by enzyme analysis using acid phosphatase (Bowers et al., 1967) for the large granular fraction, glucose-6-phosphatase (Harper, 1965) for the microsomal fraction, and lactic dehydrogenase (Bergmeyer et al., 1965) for the cytosol fraction.

Zinc Analyses and Immune Response Measurements
Tissue samples and cellular fractions were analyzed for Zn by atomic absorption spectophotometry (model 5000, Perkin-Elmer, Norwalk, CT). Approximately 0.5 g of each tissue and the debris pellet was digested with nitric acid (70%) and hydrogen peroxide (30%) in a microwave digester (model MDS-81D, CEM, Matthews, NC). Zinc concentrations in the other cell fractions were determined in the undigested sample.

In vitro lymphocyte blastogenesis was measured on d 21 of the experiment in one randomly selected pig per pen as described previously (van Heugten et al., 1994). Mitogens (Sigma Chemical, St. Louis, MO) used were phytohemagglutinin (PHA) at a concentration of 10 µg/mL, pokeweed mitogen (PWM) at a concentration of 10 µg/mL, and E. coli lipopolysaccharide (LPS) at a concentration of 10 µg/mL. Fetal calf serum (FCS, Sigma Chemical) or autologous serum (AUT) was added to the plates to provide a final concentration of 10% in the assay. Uptake of [³H]thymidine served as a measure of cell proliferation.

To evaluate the humoral immune response, two randomly selected pigs per pen were injected with a 1 mL of a 20% suspension of sheep red blood cells (SRBC) in PBS on d 21 of the experiment. The other two pigs received an injection of 1 mL of a solution of 0.5 mg/mL of ovalbumin in a mixture of 0.5 mL of PBS and 0.5 mL of Freunds incomplete adjuvant (Sigma Chemical). Blood samples were taken by venipuncture immediately prior to antigen injections and 7 and 14 d later. Serum was collected after centrifugation at 600 x g and stored at -20°C until it was analyzed.

Antibody titers to SRBC were determined using the microtiter hemagglutination assay as described by Wegmann and Smithies (1966). Twofold serial dilutions of heat-inactivated serum (30 min at 56°C) were made in PBS in V-bottom microtiter plates. A 1% suspension of SRBC was added and plates were incubated for 30 min at 37°C. Antibody titers were expressed as log₂ of the reciprocal of the highest dilution showing agglutination of SRBC.

An ELISA was used to determine antibody response to ovalbumin as described previously (van Heugten et al., 1994). Serum was added to microtiter plates coated with ovalbumin at a dilution of 1:1,000 in PBS.

In vivo cellular immune response was evaluated by a PHA skin test (Blecha et al., 1983) on d 28 of the experiment. Two pigs per pen (the same pigs that were used for the determination of antibody response to SRBC) were injected with 0.1 mL of a 1.5-mg/mL solution of PHA in the right flank. Skin thickness response was measured 0, 6, 12, 24, and 48 h after injection.

Macrophage function was assessed in six pigs per treatment (one pig per pen from two blocks and two pigs per pen from the other two blocks; pigs selected were balanced for the immunological assays performed previously to avoid confounding). Pigs were injected i.p. with 50 mL of a 3% Sephadex suspension to elicit peritoneal macrophages (Trembicki et al., 1984). The solution was prepared by soaking Sephadex G 50 superfine (Sigma Chemical) in distilled water overnight. Sephadex was then washed in sterile distilled water and a 3% suspension was prepared in sterile PBS. On d 35 of the experiment pigs were injected i.p. with 50 mL of the Sephadex solution. Forty-two hours after injection, pigs were immobilized by an i.v. injection of 0.25 mL of xylazine (Rompun, Miles Laboratories, Shawnee, KS) and 0.25 mL of ketamine hydrochloride (Ketaset, Bristol Laboratories, Syracuse, NY). Peritoneal exudate cells were collected by flushing the peritoneal cavity with 150 mL of sterile PBS containing 0.5 IU/mL of heparin. An 18-gauge needle was inserted into the peritoneal cavity and fluid was collected into siliconized bottles by gravity flow. In some cases, insufficient amounts of fluid could be collected from pigs, resulting in missing observations. These instances did not appear to be related to dietary treatment. Peritoneal exudate cells were harvested following centifugation at 100 x g and were washed twice in sterile RPMI 1640 (Gibco, Grand Island, NY). Cells were then resuspended in RPMI 1640 containing 100 U/mL of penicillin, 50 µg/mL of streptomycin and 5% FCS at a concentration of 5 x 10⁶ cells/mL. Phagocytic capacity of peritoneal exudate cells was evaluated as described by Qureshi et al. (1986). One milliliter of the cell suspension was added to culture dishes containing three round sterile coverslips (18 mm in diameter) and then incubated at 37°C in a 5% CO₂ atmosphere for 1 h. Culture media was then removed and 1 mL of fresh RPMI 1640 plus antibiotics and FCS was added. Cells were incubated at 37°C for an additional 16 h. Coverslips were then washed with sterile PBS to remove nonadherent cells. Coverslips were transferred into clean Petri dishes and 1 mL of a 1% suspension of opsonized or unopsonized SRBC in RPMI 1640 with antibiotics and FCS was added. Opsonization was accomplished by incubation of SRBC with a subagglutinating concentration of specific antiserum made in line II Japanese quail. Following a 30-min incubation at 37°C, cell cultures were washed with PBS and stained (Leukostat, Fisher Scientific, Orangesburg, NY) to microscopically determine the number of macrophages, phagocytic macrophages, and the number of SRBC ingested per macrophage.

Statistical Analyses
Data were analyzed by ANOVA as a randomized complete block design using the GLM procedure of SAS (SAS Inst., Inc., Cary, NC). The model included the fixed effects of dietary treatment and block. Pen served as the experimental unit for growth performance data, organ weights, tissue zinc concentrations, and intracellular zinc distribution, whereas individual pig data were used to analyze immune response measurements. Initial skin thickness was used as a covariate in the analysis of the PHA skin thickness response data. Significance of differences between treatments was determined by using the least significant difference method. Least squares means are reported and differences were considered statistically significant at P < 0.05.

	Results and Discussion

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The basal diet in the current experiment was supplemented with 80 ppm of Zn from a mineral premix (total Zn concentration of 104 ppm) to meet the suggested NRC (1998) requirement. Additional Zn supplementation, at levels considered to be close to the physiological needs of the pig, had no effect (P = 0.17) on ADG or ADFI (Table 2). Pharmacological levels of Zn (e.g., levels of approximately 300 to 3,000 ppm) are often used in the swine industry in the diets of nursery pigs immediately following weaning and have been reported to enhance growth performance (Hill et al., 2000; Case and Carlson, 2002). Levels of Zn used in the current study were much lower than these pharmacological levels and represent concentrations close to those fed to nursery pigs 2 to 3 wk following weaning in the swine industry. In addition, organic forms of Zn are used in the animal production industry at low levels (40 to 80 ppm of Zn) in diets already containing supplemental Zn (inorganic) from a mineral premix. Feed efficiency for the entire experimental period was poorest (P < 0.05) for pigs fed 80 ppm of Zn from ZnSO₄ compared to control pigs and pigs fed 160 ppm of Zn from ZnSO₄. No clear explanation is evident for this observation, and it is unlikely to expect reduced feed efficiency at 80 ppm of supplemental Zn, but not at 160 ppm of Zn. Supplementation of pigs with ZnLys decreased feed efficiency compared to pigs fed 160 ppm of Zn from ZnSO₄; however, no other effects of organic sources of Zn on feed efficiency were observed. The results of this experiment indicate that the current NRC (1998) recommendations for Zn (100 ppm for pigs between 5 and 10 kg of BW and 80 ppm for pigs between 10 and 20 kg of BW) were sufficient to maximize growth performance in weanling pigs. In addition, supplementation of diets with ZnMet or ZnLys did not improve growth performance of weanling pigs. Similarly, Wedekind et al. (1994) did not observe an improvement in performance when ZnMet or ZnLys were supplemented to diets of growing and finishing pigs. Cheng et al. (1998) reported that supplementation of a weanling pig basal diet containing 32 ppm of Zn with 100 ppm of Zn from either ZnSO₄ or ZnLys improved pig performance; however, no differences between Zn sources could be detected. Swinkels et al. (1996) supplemented Zn-depleted pigs with either ZnSO₄ or a Zn amino acid chelate and observed that both sources of Zn were equally effective in restoring Zn status of pigs and had similar effects on pig performance. Schell and Kornegay (1996) reported no benefit from ZnMet or ZnLys when supplemented at pharmacological levels to nursery pig diets. In the present experiment, we chose to evaluate Zn supplementation levels commonly used in the swine industry compared to NRC (1998) recommendations to determine if there was a benefit of organic Zn complexes when supplying Zn above the Zn requirement. Results demonstrate that the Zn sources used in this experiment did not improve pig performance and are in general agreement with studies investigating effects of organic forms of Zn in Zn-depleted pigs (Hill et al., 1986; Swinkels et al., 1996) or pigs fed pharmacological levels of Zn (Hahn and Baker, 1993; Schell and Kornegay, 1996).

Skin thickness response to PHA measures infiltration of primarily mononuclear cells into the injection site (Kelley et al., 1982; Blecha et al., 1983) and was not affected (P = 0.53) by dietary treatment (Table 5). In contrast, Kidd et al. (1994b) reported increased toe web swelling after intradermal injection with PHA in turkeys supplemented with 30 or 45 ppm of Zn from ZnMet compared to turkeys fed a basal diet containing 130 ppm of Zn.

	Implications

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	Footnotes

 
¹ The use of trade names in this publication does not imply endorsement by the North Carolina Agricultural Research Service of the products named or criticism of similar ones not mentioned.

² Appreciation is expressed to Zinpro Corp. (Eden Prairie, MN) for partial financial support.

⁴ Present address: Department of Animal Science, University of Arkansas, Fayetteville 72701.

⁵ Present address: Louisiana State University AgCenter, Southeast Research Station, Franklinton 70438.

³ Correspondence: Box 7621 (phone: 919-513-1116; fax: 919-515-6316; E-mail: Eric_vanHeugten{at}ncsu.edu).

Received for publication October 2, 2002. Accepted for publication May 2, 2002.

	Literature Cited

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Bergmeyer, H. U., E. Bernt, and B. Hess. 1965. Lactic dehydrogenase. Pages 736–743 in Methods of Enzymatic Analysis. H. U. Bergmeyer, ed. Academic Press, New York.

Blecha, F., D. S. Pollmann, and D. A. Nichols. 1983. Weaning pigs at an early age decreases cellular immunity. J. Anim. Sci. 56:396–400.

Bowers, W. E., J. T. Finkenstaed, and C. deDuve. 1967. Lysosomes in the lymphoid tissue: I. The measurement of hydrolytic activities in whole homogenate. J. Cell. Biol. 32:325–337.[Abstract/Free Full Text]

Case, C. L., and M. S. Carlson. 2002. Effect of feeding organic and inorganic sources of additional zinc on growth performance and zinc balance in nursery pigs. J. Anim. Sci. 80:1917–1924.[Abstract/Free Full Text]

Cheng, J., E. T. Kornegay, and T. Schell. 1998. Influence of dietary lysine on the utilization of zinc from zinc sulfate and a zinc-lysine complex by young pigs. J. Anim. Sci. 76:1064–1074.[Abstract/Free Full Text]

Ferket, P. R., and M. A. Qureshi. 1992. Effect of level of inorganic and organic zinc and manganese on the immune function of turkey toms. Poultry Sci. 71(Suppl. 1):60.

Hahn, J. D., and D. H. Baker. 1993. Growth and plasma zinc responses of young pigs fed pharmacologic levels of zinc. J. Anim. Sci. 71:3020–3024.[Abstract]

Hall, V. L., R. C. Ewan, and M. J. Wannemuehler. 1993. Effect of zinc deficiency and zinc source on performance and immune response in young pigs. J. Anim. Sci. 71(Suppl. 1):173.

Harper, A. E. 1965. Glucose-6-phosphatase. Pages 788–792 in Methods in Enzymatic Analysis. H. U. Bergmeyer, ed. Academic Press, New York.

Hill, D. A., E. R. Peo Jr., A. J. Lewis, and J. D. Crenshaw. 1986. Zinc-amino acid complexes for swine. J. Anim. Sci. 63:121–130.

Hill, G. M., G. L. Cromwell, T. D. Crenshaw, C. R. Dove, R. C. Ewan, D. A. Knabe, A. J. Lewis, G. W. Libal, D. C. Mahan, G. C. Shurson, L. L. Southern, and T. L. Veum. 2000. Growth promotion effects and plasma changes from feeding high dietary concentrations of zinc and copper to weanling pigs (regional study). J. Anim. Sci. 78:1010–1016.[Abstract/Free Full Text]

Johnson, R. W., J. Escobar, and D. M. Webel. 2001. Nutrition and immunology of swine. Pages 545–562 in Swine Nutrition, 2nd ed. A. J. Lewis and L. L. Southern, ed. CRC Press, Washington, DC.

Kelley, K. W., R. E. Greenfield, J. F. Evermann, S. M. Parish, and L. E. Perryman. 1982. Delayed-type hypersensitivity, contact sensitivity, and phytohemagglutitnin skin-test responses of heat- and cold-stressed calves. Am. J. Vet. Res. 43:775–779.[Medline]

Kidd, M. T., P. R. Ferket, and M. A. Qureshi. 1996. Zinc metabolism with special reference to its role in immunity. World Poultry Sci. J. 52:309–324.

Kidd, M. T., M. A. Qureshi, P. R. Ferket, and L. N. Thomas. 1994a. Blood clearance of Escherichia coli and evaluation of mononuclear-phagocytic system as influenced by supplemental dietary zinc methionine in young turkeys. Poultry Sci. 73:1381–1389.[Medline]

Kidd, M. T., M. A. Qureshi, P. R. Ferket, and L. N. Thomas. 1994b. Dietary zinc methionine enhances mononuclear-phagocytic function in young turkeys. Biol. Trace Elem. Res. 42:217–229.[Medline]

Kincaid, R. L., W. J. Miller, R. P. Gentry, M. W. Neathery, and D. L. Hampton. 1975. Intracellular distribution of zinc and zinc-65 in calves receiving high but nontoxic amounts of zinc. J. Dairy Sci. 59:552–555.

Klasing, K. C. 2001. Protecting animal health and well-being: nutrition and immune function. Pages 13–20 in Scientific Advances in Animal Nutrition: Promise for the New Century. NRC. Natl. Acad. Press, Washington, DC.

NRC. 1998. Nutrient Requirements of Swine.10th ed. Natl. Acad. Press, Washington, DC.

Porter, H., W. Wiener, and M. Barker. 1961. The intracellular distribution of copper in immature liver. Biochim. Biophys. Acta 52:419–423.

Qureshi, M. A., R. R. Dietert, and L. D. Bacon. 1986. Genetic variation in the recruitment and activation of chicken peritoneal macrophages. Proc. Soc. Exp. Biol. Med. 181:560–568.[Medline]

Rink, L., and H. Kirchner. 2000. Zinc-altered immune function and cytokine production. J. Nutr. 130:1407S–1411S.[Abstract/Free Full Text]

Saylor, W. W., and R. M. Leach Jr. 1980. Intracellular distribution of copper and zinc in sheep: effect of age and dietary levels of the metals. J. Nutr. 110:448–459.

Schell, T. C., and E. T. Kornegay. 1996. Zinc concentration in tissues and performance of weanling pigs fed pharmacological levels of zinc from ZnO, Zn-methionine, Zn-lysine, or ZnSO₄. J. Anim. Sci. 74:1584–1593.[Abstract]

Spears, J. W. 1989. Zinc methionine for ruminants: Relative bioavailability of zinc in lambs and effects on growth and performance of growing heifers. J. Anim. Sci. 67:835–843.

Swinkels, J. W. G. M., E. T. Kornegay, W. Zhou, M. D. Lindemann, K. E. Webb, Jr., and M. W. A. Verstegen. 1996. Effectiveness of a zinc amino acid chelate and zinc sulfate in restoring serum and soft tissue zinc concentrations when fed to zinc-depleted pigs. J. Anim. Sci. 74:2420–2430.[Abstract]

Trembicki, K. A., M. A. Qureshi, and R. R. Dietert. 1984. Avian peritoneal exudate cells: a comparison of stimulation protocols. Dev. Comp. Immun. 8:395–402.[Medline]

van Heugten, E., J. W. Spears, and M. T. Coffey. 1994. The effect of dietary protein on performance and immune response in weanling pigs subjected to an inflammatory challenge. J. Anim. Sci. 72:2661–2669.[Abstract]

van Heugten, E. and T. van Kempen. 2000. Understanding and applying nutrition concepts to reduce nutrient excretion in swine. North Carolina Coop. Ext. Serv., Pages 1–15 in Pub. No. AG-608.

Wedekind, K. J., A. E. Hortin, and D. H. Baker. 1992. Methodology for assessing zinc bioavailability: Efficacy estimates for zinc methionine, zinc sulfate, and zinc oxide. J. Anim. Sci. 70:178–187.[Abstract]

Wedekind, K. J., A. J. Lewis, M. A. Giesemann, and P. S. Miller. 1994. Bioavailability of zinc from inorganic and organic sources for pigs fed corn-soybean meal diets. J. Anim. Sci. 72:2681–2689.[Abstract]

Wegmann, T. G. and O. Smithies. 1966. A simple hemagglutination system requiring small amounts of red cells and antibodies. Transfusion 6:67–73.

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