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Effects of fish oil supplementation on the performance and the immunological, adrenal, and somatotropic responses of weaned pigs after an Escherichia coli lipopolysaccharide challenge¹

Y. L. Liu^*, D. F. Li^*,2, L. M. Gong^*, G. F. Yi, A. M. Gaines and J. A. Carroll

^* National Feed Engineering Technology Research Center, China Agricultural University, Beijing, P. R. China 100094; and University of Missouri-Columbia; and and Agricultural Research Service, USDA, Columbia, MO

	Abstract

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Seventy-two crossbred pigs (7.58 ± 0.30 kg BW) weaned at 28 ± 3 d of age were used to investigate the effects of fish oil supplementation on pig performance and on immunological, adrenal, and somatotropic responses following an Escherichia coli lipopolysaccharide (LPS) challenge in a 2 x 2 factorial design. The main factors consisted of diet (7% corn oil [CO] or 7% fish oil [FO]) and immunological challenge (LPS or saline). On d 14 and 21, pigs were injected intraperitoneally with either 200 µg/kg BW of LPS or an equivalent amount of sterile saline. Blood samples were collected 3 h after injection for analysis of interleukin-1ß (IL-1ß), prostaglandin E₂ (PGE₂), cortisol, growth hormone (GH), and insulin-like growth factor (IGF)-I. On d 2 after LPS challenge, peripheral blood lymphocyte proliferation (PBLP) was determined. Lipopolysaccharide challenge decreased ADG (487 vs. 586 g; P < 0.05) and ADFI (as-fed, 776 vs. 920 g; P < 0.05) from d 14 to 21 and ADG (587 vs. 652 g; P < 0.10) from d 21 to 28. Fish oil improved ADG (554 vs. 520 g; P < 0.10) and ADFI (891 vs. 805 g; P < 0.10) from d 14 to 21. On d 14, LPS challenge x diet interactions were observed for IL-1ß (P < 0.10), PGE₂ (P < 0.001), and cortisol (P < 0.05) such that these measurements responded to the LPS challenge to a lesser extent (IL-1ß: 93 vs. 114 pg/mL, P < 0.05; PGE₂: 536 vs. 1,285 pg/mL, P < 0.001; cortisol: 143 vs. 206 ng/mL, P < 0.05) in pigs receiving the FO diet than in pigs fed the CO diet. In contrast, among LPS-treated pigs, pigs fed the FO diet had higher IGF-I (155 vs. 101 ng/mL; P < 0.10) than those fed the CO diet. On d 21 among LPS-treated pigs, pigs fed FO had lower IL-1ß (70 vs. 84 pg/mL; P < 0.10) and cortisol (153 vs. 205 ng/mL; P < 0.05) than those fed CO. Pigs fed FO had lower PGE₂ (331 vs. 444 pg/mL; P < 0.05) and higher IGF-I (202 vs. 171 ng/mL; P < 0.10) compared with those fed CO. Lipopolysaccharide challenge decreased GH (0.27 vs. 0.33 ng/mL; P < 0.05) on d 14, whereas it had no effect on GH on d 21. During both LPS challenge periods, the challenge increased PBLP when these cells were incubated with 8 (1.46 vs. 1.32; P < 0.10) or 16 µg/mL (1.46 vs. 1.30; P < 0.05) of concanavalin A. Fish oil had no effect on PBLP. These results suggest that FO alters the release of proinflammatory cytokines, which might lead to improved pig performance during an immunological challenge.

Key Words: Fish Oil • Lipopolysaccharide • Pigs

	Introduction

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It is well documented that an immunological challenge can result in a series of physiological changes, including increased body temperature, depressed feed intake, changes in plasma acute phase protein concentration, activation of the immune system, activation of the hypothalamic-pituitary-adrenal axis, and inhibition of the somatotropic axis (Johnson, 1997). Consequently, the immunological challenge results in the poor growth of livestock and may increase economic loss for animal producers. One emerging view is that these changes are attributed to the release of proinflammatory cytokines (Johnson, 1997; Webel et al., 1997), including tumor necrosis factor, interleukin-1, and interleukin-6. Overproduction of these cytokines can adversely affect growth and feed efficiency. Therefore, the modulation of these cytokines may have benefits in alleviating the negative effects induced by an immunological stress (Lang et al., 1996).

Fish oil, a rich source of n-3 polyunsaturated fatty acids, has been used as an immune modulator (Xi et al., 1998). Many studies have shown that fish oil could attenuate inflammation in many diseases. The protective mechanism of fish oil as an antiinflammatory agent is associated with its inhibitory effects on the overproduction of proinflammatory cytokines (Xi et al., 1998). According to the above-mentioned studies, fish oil supplementation may affect pig performance by regulating the production of proinflammatory cytokines. However, little research has been conducted to investigate these effects in weaned piglets. In the present experiment, Escherichia coli lipopolysaccharide (LPS) was administered as an inflammatory agent following the model of Johnson and von Borell (1994). Our objective was to evaluate the effects of fish oil supplementation on pig performance and to test the immunological, adrenal, and somatotropic responses of weaned pigs.

	Materials and Methods

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Animal Care and Diets
The animal protocol for this research was approved by the China Agricultural University Animal Care and Use Committee. Seventy-two crossbred pigs (Large White x Landrace x Piétrain) weaned at 28 ± 3 d of age (7.58 ± 0.30 kg BW), were balanced for initial body weight and ancestry across four treatment groups in a 2 x 2 factorial design that included a dietary treatment (fish oil or corn oil supplementation) and an E. coli LPS challenge (challenged or not challenged).

Pigs were housed in 1.80- x 1.25-m² pens with six replicate pens (three pens of females and three pens of males) per treatment and three pigs per pen. Each pen was equipped with a feeder and a nipple waterer to allow pigs ad libitum access to feed and water. The experimental diets differed according to the sources of oil, fish oil (menhaden fish oil, Fujian Gaolong Co., Fujian, China), or corn oil (Beijing Red Star Starch Co., Beijing, China). The diets (Table 1) were formulated to meet or exceed NRC (1998) requirements for all nutrients. The corn gluten meal and cornstarch were used to minimize the amount of corn oil in the basal diet. The fatty acid composition (Table 2) of the fish oil diet and the corn oil diet was measured according to the method of Thies et al. (1999).

Blood Collection and Analysis
On d 14 and 21, 3 h following injection with LPS or saline, blood samples (one pig per pen) were collected into heparinized vacuum tubes (Becton Dickinson Vacutainer Systems, Franklin Lakes, NJ) and centrifuged (3,500 x g for 10 min) to separate plasma. The plasma from each pig was stored at -80°C until analysis. All blood-related measurements were analyzed in duplicate. The same pigs were used for the blood samples on d 14 and 21.

Plasma interleukin-1ß was analyzed using a commercially available swine interleukin-1ß ELISA kit (BioSource, Camarillo, CA). Minimum detectability of swine interleukin-1ß was 15 pg/mL with an interassay CV of less than 10%.

Plasma prostaglandin E₂ was analyzed using a commercially available ¹²⁵I RIA kit (College of Medical Science of Suzhou University, Jiansu, China). Minimum detectability of porcine plasma prostaglandin E₂ was 6.25 pg/mL with an intraassay CV less than 10%.

Plasma cortisol was analyzed using a commercially available ¹²⁵I RIA kit (Beijing Beimian Dongya Institute of Biological Technology, Beijing, China). Minimum detectable dose of cortisol was 1 ng/mL with an intraassay coefficient of variation of 5%.

Plasma GH was measured using a commercially available ¹²⁵I RIA kit (Beijing North Institute of Biological Technology, Beijing, China). The assay used human GH and antibodies against human GH as the standard. The assay was sensitive to 0.1 ng/mL of GH with an intraassay CV less than 10%.

Plasma IGF-I was analyzed using a commercially available ¹²⁵I RIA kit (Biocode S.A., Liege, Belgium). In the assay, recombinant human IGF-I and mouse anti-IGF-I monoclonal antibody were used as the standard. Recovery ranged from 92.3 to 110.0%. The within-assay CV was less than 10%, and the minimum detectable concentration of IGF-I was 5 ng/mL.

Lymphocyte Proliferation
Two days after the first and the second LPS or saline administration, lymphocytes were isolated from peripheral blood from one pig (a pig different from the one used for plasma sample analysis above) per pen. Lymphocyte proliferation was measured by using a colorimetric test with 3-(4,5-dimethlthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) (M-2128, Sigma Chemical) in cultures of purified peripheral blood mononuclear cells according to the method of Mosmann (1983). Briefly, mononuclear cells were isolated by gradient centrifugation from peripheral blood. The cells were washed three times in RPMI-1640 culture medium supplemented with 10% (vol/vol) heat-inactivated fetal calf serum, 100 U/mL of penicillin, 100 µg/mL of streptomycin and 25 mM N - (2 - hydroxyethyl) - piperazine - N' - 2 - ethane - sulfonic acid. Following a final wash, cell activity was detected by trypan blue dye exclusion, the cells were counted, and the cell density was adjusted to 2 x 10⁶ cells /mL culture medium. After that, the cells were cultured in 96-well microtiter plates with a total culture volume of 200 µL.

Lymphocyte mitogen concanavalin A (Type IV, C-2010, Sigma Chemical) was added at a final concentration of 0, 8, or 16 µg/mL culture medium, and then the plates were incubated at 37°C in a 5% CO₂ incubator for 66 h. Subsequently, 10 µL of MTT solution (5 mg MTT /mL in 1/15 M phosphate-buffered saline, pH 7.6) was added to each well and the plates were incubated at 37°C for another 6 h. Following incubation, 100 µL of a 10% sodium dodecyl sulfate in 0.04 M HCl solution was added to lyse the cells and solubilize the MTT crystals. Plates were read at 570 nm using an automated microplate reader (Bio-Rad, model 550, Hercules, CA). The value of lymphocyte proliferation was expressed as a stimulation index, which was calculated as absorbance of wells incubated with concanavalin A divided by absorbance of wells incubated without concanavalin A.

Bovine Serum Albumin Antibody Analysis
Two days after the first LPS challenge, one pig per pen (again, pigs different from the pigs used for the analysis of plasma samples and lymphocyte proliferation above) was injected intramuscularly with 1 mg/kg BW bovine serum albumin (Sigma Chemical) to determine humoral immune response. The bovine serum albumin was dissolved in a 0.9% (wt/vol) NaCl solution. Blood samples were collected before (defined as d 0) as well as 7 and 12 d after the injection of bovine serum albumin. Serum was separated by centrifugation (3,500 x g for 10 min) and was stored at -80°C until analysis.

Antibody response against bovine serum albumin was measured using ELISA. Briefly, 96-well microtiter plates were coated with 100 µL of a solution containing 40 µg bovine serum albumin in 1 mL of carbonate buffer (0.06 M, pH 9.6) and left overnight at 4°C. Plates were then washed four times with 0.01 M phosphate-buffered saline (pH 7.2) containing 0.05% Tween 20 (Sigma Chemical). Serum samples were diluted with 0.01 M phosphate-buffered saline (pH 7.2) containing 10% horse serum at a dilution of 1:40. The diluted serum samples were added to the plates and incubated at 37°C for 1 h. Plates were then washed four times with 0.01 M phosphate-buffered saline (pH 7.2) containing 0.05% Tween 20. After washing, a 100-µL solution of rabbit anti-swine immunoglobulin G conjugated to horseradish peroxidase (Sigma Chemical) was added to each well. After incubation at 37°C for 1 h, the plates were washed and 100 µL of substrate, which contained 10 mL of citric acid buffer (0.05 M, pH 4.0), 100 µL of 27 mM 2,2'-azino-bis-(3-ethyl-benzthiazoline-6-sulfonic acid) (Sigma Chemical) and 40 µL of 1% H₂O₂ was added to the wells. After incubation for 15 min at room temperature, the plates were read at an absorbance of 405 nm using an automated microplate reader (Bio-Rad, Model 550).

Statistical Analysis
Data were analyzed by ANOVA using the GLM procedures of SAS (SAS Inst. Inc., Cary, NC) appropriate for a factorial arrangement of treatments in a randomized complete block design. The statistical model included the effects of challenge (saline or LPS), diet (corn oil or fish oil), and their interactions. Pen was used as experimental unit for the performance data, whereas individual pig data were used as the experimental unit in the blood analysis, lymphocyte proliferation, and bovine serum albumin antibody analysis. Differences between treatments were analyzed using a t-test following a significant F-test. An alpha level of P < 0.10 was used as the criterion for statistical significance.

	Results

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Performance
Performance data are presented in Table 3. There was no LPS challenge x diet interaction for ADG, ADFI, and gain/feed observed throughout the 28-d trial. During the first challenge period (from d 14 to 21), LPS challenge reduced ADG (P < 0.05) by 16.9% and ADFI (P < 0.05) by 17.2% compared with the saline-treated pigs. During the second LPS challenge, pigs challenged with LPS had 10.0% lower ADG (P < 0.10) than saline-treated pigs during d 21 to 28, but ADFI was not affected, which indicated that the response of pigs to the first LPS injection was stronger than the response to the second injection. Lipopolysaccharide administration did not affect feed efficiency during any stage of the experiment.

Cellular and Humoral Responses
Lymphocyte proliferation was measured in cultures of purified peripheral blood mononuclear cells after the first and the second LPS challenge, and the data are presented in Table 4. There were no LPS challenge x diet interactions observed for lymphocyte proliferation during both the first and the second LPS challenge periods. During both the first and the second LPS challenge periods, LPS challenge resulted in increased blood lymphocyte proliferation when incubated with either 8 (P < 0.10) or 16 µg/mL (P < 0.05) concanavalin A. Fish oil had no effect on lymphocyte proliferation. The humoral immune response was measured by specific antibody response to bovine serum albumin, and there was neither LPS challenge nor diet effect on serum antibody response to bovine serum albumin (Table 5).

Plasma Cortisol, IGF-I, and GH Concentrations
As indicated by Table 6, both on d 14 and 21, a LPS challenge x diet interaction was observed for plasma cortisol (P < 0.05) such that the cortisol response to LPS challenge was lower in those pigs receiving fish oil compared with pigs fed corn oil. Thus, in pigs challenged with LPS, pigs fed the fish oil diet reduced (P < 0.05) plasma cortisol by 30.4% relative to pigs fed the corn oil diet, although no difference existed among saline-treated pigs fed the different diets. On d 14, there was a LPS challenge x diet interaction observed for plasma IGF-I, in which pigs fed fish oil had higher plasma IGF-I (P < 0.10) compared with pigs fed corn oil among LPS-treated pigs, whereas there was no difference among saline-treated pigs in plasma IGF-I. There was no LPS challenge x diet interaction observed for plasma GH. However, LPS administration reduced plasma GH by 16.5% (P < 0.05) regardless of dietary treatment. On d 21, the LPS challenge reduced plasma IGF-I (P < 0.01) regardless of dietary treatment, but no diet or LPS challenge effect was observed for plasma GH.

	Discussion

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An immunological challenge results in reduced feed intake, lean muscle accretion, and growth. Recent studies suggest that these changes observed in animals subjected to an immunological challenge are mediated by proinflammatory cytokines (Johnson, 1997). These cytokines can act locally to amplify the cellular immune response, but they also can act systemically on a number of targets, such as viscera and liver, adipose tissue, skeletal muscles, and brain, to change behavior, metabolism, and neuroendocrine secretions and consequently inhibit growth (Johnson, 1997). Thus, regulation of cytokines production has great benefits in swine production system where pigs are exposed to an immunological stress.

To evaluate whether fish oil supplementation could alter the negative effects of an immunological stress, we took advantage of a well-documented model for inducing sickness in pigs by injecting LPS (Johnson and von Borell, 1994). Lipopolysaccharide is a molecule found in the membrane of all gram-negative bacteria. In pigs, LPS induces symptoms of acute bacterial infection, including anorexia, hypersomnia, and fever. The effects of LPS are due to its ability to stimulate macrophages to synthesize and secrete proinflammatory cytokines (Johnson and von Borell, 1994). Whether LPS is indicative of on-farm conditions is a subject of much debate; however, it is obvious that its administration activates several immune defenses, which allows one to better understand the physiology of infection and inflammation due to an immunological challenge.

In the present study, E. coli LPS challenge decreased performance of weanling pigs, which is consistent with Johnson (1997). Dietary treatments had no effect on pig performance before LPS challenge. However, pigs fed the fish oil had higher gain and feed intake compared with pigs fed the corn oil diet independent of LPS challenge between d 14 and 21. Previous studies have demonstrated that menhaden fish oil supplemented to a nursery pig diet modulated the immune system and prevented the growth-suppressive effects observed with an LPS challenge (Gaines et al., 2003). In addition, the study of Korver and Klasing (1997) demonstrated that increasing amounts of fish oil, compared with corn oil, improved body weight and attenuated the growth-suppressing effect in poultry challenged with LPS. In our study, we had the similar results not only in LPS-challenged pigs, but also in unchallenged pigs.

Related to the depression of weight gain and feed intake after an immunological challenge, an activation of the immune system, as indicated by the increased lymphocyte proliferation and interleukin-1ß, was also observed in this study. This response results in partitioning of nutrients away from growth and toward the immune system (Hasselgren, 1993), which will decrease the efficiency of nutrient utilization for growth.

In the present study, the fish oil diet decreased plasma interleukin-1ß concentration compared with corn oil. In a previous study, pigs fed menhaden fish oil had lower tumor necrosis factor- and interferon- compared with pigs fed corn oil (Carroll et al., 2003; Gaines et al., 2003). Therefore, feeding the fish oil diet to the pigs might improve growth performance compared with corn oil partially by suppressing the immune response. Indeed, Hellerstein et al. (1989) have shown that anorexia of rats induced by interleukin-1 and the immune response could be prevented by feeding a diet supplemented with 8% fish oil.

The decrease in plasma interleukin-1ß concentration of pigs fed the 7% fish oil-supplemented diet may be explained by a decrease in eicosanoid production. Fish oil, rich in n-3 long-chain polyunsaturated fatty acids, may inhibit the production of many biologically active metabolites of arachidonic acid (C20:4), among which, prostaglandin E₂ and leukotriene B₄ are the most important products that mediate immune responses (Calder, 1997). In our study, fish oil supplementation reduced the plasma prostaglandin E₂ levels, which is in agreement with a previous report by Thies et al. (1999). However, prostaglandin E₂ was also reported to have the capability of decreasing cytokine production (Calder, 1997). Therefore, it may also be possible that the effects of n-3 fatty acids on immune responses are independent of prostaglandin E₂.

Concurrent with depressed gain and feed intake in response to an immunological challenge, a reduction in plasma IGF-I was also observed during both the first and the second LPS challenge periods. The decreased plasma IGF-I may indicate the repartition of nutrients away from normal growth and toward the immune response (Hasselgren, 1993). The study of Soto et al. (1998) also suggested that the decrease of IGF-I and GH release are important causative factors of growth suppression during an immunological challenge.

In the current study, in those LPS-challenged pigs, feeding the fish oil diet partially alleviated the reduction of plasma IGF-I, which was accompanied by lower plasma interleukin-1ß levels compared with the corn oil diet. Therefore, the effect of fish oil on mitigating plasma IGF-I reduction seems to be closely associated with the decrease of proinflammatory cytokine release, especially interleukin-1ß. Thissen and Verniers (1997) suggested that proinflammatory cytokines impair IGF-I production via several possible mechanisms.

First of all, because IGF-I is a GH-dependent growth factor, proinflammatory cytokines may affect IGF-I secretion through their modulation of GH production. In the present study, the LPS challenge was observed to suppress GH release, which was concurrent with the increase of plasma interleukin-1ß levels. Therefore, GH secretion may have been inhibited by interleukin-1ß (Peisen et al., 1995; Wada et al., 1995). Consequently, the reduced IGF-I may have been associated with the suppressive effect of interleukin-1ß on GH secretion when pigs were challenged with LPS.

In our study, fish oil did not attenuate the decrease of GH in the LPS-challenged pigs. However, a significant effect of feeding fish oil on alleviating plasma IGF-I reduction was observed, which suggests that the uncoupling of the GH/IGF-I axis may occur during an immunological challenge. The uncoupling of the GH/IGF-I axis may be explained by a decrease of GH receptors or IGF-I mRNA expression in liver. The study of Thissen and Verniers (1997) suggested that interleukin-1ß inhibits both IGF-I mRNA and GH receptor mRNA expression in GH-stimulated rat hepatocytes. Therefore, fish oil may mitigate the decrease of IGF-I by attenuating the depression of GH receptors. However, we did not measure GH receptors in the current study.

Secondly, proinflammatory cytokines induce profound anorexia associated with depressed IGF-I (McCarthy et al., 1995). In our study, fish oil improved feed intake compared with corn oil. Partially relevant to this, fish oil attenuated the reduction of IGF-I in LPS-challenged pigs, especially during the first challenge period. Therefore, the increase of circulating plasma IGF-I levels in LPS-challenged pigs fed fish oil might partially explain why pigs fed fish oil had the higher feed intake compared with pigs fed corn oil.

Thirdly, proinflammatory cytokines may stimulate the release of stress hormones, such as glucocorticoids (Fan et al., 1994), and those stress hormones can induce GH resistance (Luo and Murphy, 1989; Beauloye et al., 1996). In our study, during both the first and the second challenge periods, a decrease of plasma IGF-I after an immunological challenge was concomitant with a rapid elevation of plasma cortisol, which is in agreement with previous studies of Balaji et al. (2000) and Wright et al. (2000). However, feeding the fish oil diet suppressed cortisol, whereas it alleviated IGF-I depression of LPS-challenged pigs compared with the corn oil diet. Similarly, previous studies showed that pigs fed fish oil had lower serum cortisol compared with corn oil (Carroll et al., 2003; Gaines et al., 2003). Therefore, by feeding LPS-challenged pigs the fish oil diet, proinflammatory cytokine release may be altered first, by which these cytokines exert modulatory effects on cortisol production and eventually IGF-I synthesis (Fan et al., 1995). Fan et al. (1995) concluded that glucocorticoids might mediate the interleukin-1ß-induced decrease of IGF-I in plasma and liver. Finally, in addition to the indirect effect on IGF-I, interleukin-1ß may have a direct suppressive effect on IGF-I (Johnson, 1997; Thissen and Verniers, 1997).

In the present study, the responses in pig performance, and the changes in the immune system, adrenal, and somatotropic axes to the first LPS challenge, were more obvious than they were to the second challenge. The different responses can be explained by a tolerance phenomenon (Chedid and Parant, 1971). In addition, fish oil improved feed intake and growth both in challenged and unchallenged pigs but exerted a significant effect on most of physiological measurements only in challenged pigs. The inconsistency might be associated with the different time span when growth performance and physiological measurements were measured. Ideally, we should measure the kinetics of feed intake and growth instead of measuring them weekly, as well as the parallel kinetics of physiological measurements instead of one-time blood sampling after each challenge. Regretfully, it is impractical for us to do this owing to the limitation to fit each pig with a jugular catheter using a nonsurgical procedure (Carroll et al., 1999) in a modern pig farm with a very strict biosecurity system.

In the present study, LPS was chosen as the model for an immunological stress. However, the LPS model has limitations as follows: 1) LPS induces a short duration response rather than a chronic immunological stress (Balaji et al., 2000); 2) pigs develop a tolerance to the multiple, subsequent LPS challenges, which is observed in our study and the study of Kegley et al. (2001); and 3) LPS and live E. coli challenge induce different immunological profiles in the weaned pigs (Zannelli et al., 2000). Therefore, the LPS model does not completely mimic the physiological changes of infection and inflammation that would occur during a bona fide immunological stress in commercial practice (Balaji et al., 2000). Further studies are needed to evaluate the effects of fish oil supplementation on the immune response to pathogens encountered in commercial swine production systems.

	Implications

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Data from the current study demonstrate that immune response was partially depressed in pigs fed a fish oil diet compared to pigs fed a corn oil diet when they are exposed to an Escherichia coli lipopolysaccharide challenge. Concomitantly, lower adrenal and higher somatotropic responses are indicated in pigs fed fish oil after lipopolysaccharide challenge. This finding suggests that pigs fed fish oil might be less susceptible to an immunological challenge. Down-regulation of the immune system activation may be the mechanism by which growth performance is improved when fish oil is supplemented in the diet of weanling pigs. Further studies are needed to evaluate the effects of fish oil on these measurements in pigs that are reared in commercial conditions.

	Footnotes

 
¹ Financial support provided by the National Natural Science Foundation of China.

² Correspondence: No. 2, Yuanmingyuan West Rd. (phone: 8610-62893588; fax: 8610-62893688; E-mail: defali{at}public2.bta.net.cn).

Received for publication December 2, 2002. Accepted for publication July 17, 2003.

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