J. Anim. Sci. 2003. 81:1806-1813
© 2003 American Society of Animal Science
The effect of supplementing microbial phytase and organic acids to a corn-soybean based diet fed to early-weaned pigs1
F. O. Omogbenigun,
C. M. Nyachoti2 and
B. A. Slominski
Department of Animal Science, University of Manitoba, Winnipeg, Manitoba R3T 2N2, Canada
2 Correspondence—phone:
(204) 474-7323; fax: (204) 474-7628; E-mail:
martin_nyachoti{at}umanitoba.ca.
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Abstract
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The effect of microbial phytase (MP) and organic acids (OA) supplementation in diets for early-weaned pigs was investigated in an in vitro assay and a growth performance and digestibility trial involving 96 pigs (18 d old). The experimental diets were: 1) a control (C) formulated according to NRC (1998); 2) a negative control (NC) that was similar to diet C except that available P was reduced by 0.19%; 3) NC plus MP (500 U/kg); and 4) NC+MP and OA (NC+MPOA). In the in vitro assay, the four diets were incubated under simulated gut conditions. Addition of MP increased (P = 0.003) phytate hydrolysis from 34 (NC) to 87.5% (NC+MP); this was further increased to 90.1% due to the addition of OA (NC+MPOA). In the 4-wk growth trial, each diet was randomly assigned to six pens each with four pigs. At the end of wk 3, a mobility test was conducted on one pig randomly selected from each pen. Pigs fed the NC diet tended to have a lower (P = 0.06) mobility score compared with those fed the other diets. At the end of wk 4, six pigs per treatment were killed and samples of digesta from different sections of the gut and the third metatarsal bone were collected for nutrient digestibility and bone ash measurements, respectively. There were no differences in ADFI, ADG, and gain:feed ratio among treatments (P > 0.05); however, ADG was 6.5% higher in piglets fed the NC+MPOA diet compared with those fed the C diet. Bone ash content was lower (P = 0.003) in NC fed pigs than in those fed the other treatments. Supplementing NC with MP and MP+OA improved bone ash content to the same level as C. Apparent ileal digestibility (AID) of DM and CP did not differ (P > 0.10) among treatments and averaged 80.7 and 79.4%, respectively. Of all AA, only AID of isoleucine, histidine, and aspartic acid was increased (P < 0.05) by MP+OA supplementation. Overall, there were slight numerical improvements in AID of AA due to MP and OA supplementation, with AID of essential AA averaging 79.4, 77.7, 80.1, and 81.6% for C, NC, NC+MP, and NC+MPOA, respectively. The AID of P was increased (P = 0.0001) by 21 percentage units, and the amount of P excreted was decreased (P = 0.03) by 19.4% as a result of MP+OA supplementation compared with C. In conclusion, addition of MP and OA to pig starter diets improved P digestion and utilization, thereby leading to a reduction in P excretion. Addition of MP and OA to corn–soybean meal diets fed to young pigs had only a slight effect on ileal amino acid digestibilities.
Key Words: Digestibility • Early Weaning • Nutrients • Organic Acids • Phosphorus • Pigs
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Introduction
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About 60 to 70% of P in plant-based ingredients commonly used in swine rations occurs as phytate P, a form that is only partly available to pigs due to their inability to produce enough phytase to fully hydrolyze the phytate molecule (Cromwell, 1992; Ravindran et al., 1994; 1995). Consequently, the addition of microbial phytase (MP) to swine diets to release the bound P has been an area of intensive research (Jongbloed et al., 1992; Lei et al., 1993a, b; Kornegay and Qian, 1996). Many of these studies also suggest potential environmental benefits through a 30 to 40% reduction in P excretion.
It has been shown that gut pH has a significant influence on MP and that maximal MP activity is realized at pH 5.5 and 2.5 to 3.0 when Aspergillus niger phytase is used. (Shieh et al., 1969; Eeckhout and De Paepe, 1996). Furthermore, at pH 2.5, phytate is dissociated from its complex with other nutrients, which is why acidification of diets with MP has been shown to increase phytate hydrolysis in vitro (Maenz et al., 1999). However, addition of organic acids (OA) to pig starter diets to enhance MP activity by lowering gut pH has produced inconsistent results, especially when digestibility of nutrients other than P is of interest.
The effect of MP and OA supplementation on protein and AA digestibilities in early-weaned pigs has not been fully investigated. Also, there is no consensus as to the effect of MP supplementation on protein and AA digestibility in swine. For instance, in some studies (O’Quinn et al., 1997; Valaja et al., 1998; Peter and Baker, 2001), MP supplementation had no effect on protein and AA utilization, whereas in others (Kemme et al., 1995; Kornegay et al., 1998), improvements were reported. Therefore, the objective of the present study was to determine the impact of MP and MP plus OA on in vitro phytate hydrolysis, in vivo phytate P availability, protein and AA digestibilities and P excretion in early-weaned pigs fed a corn–soybean meal-based diet.
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Materials and Methods
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Experimental Diets
Four corn–soybean meal-based diets consisting of a positive control (C) formulated according to NRC (1998); a negative control (NC) that was the same as diet C except that available phosphorus was reduced by 0.19 percentage units; NC plus MP (NC+MP; 500 U/kg); and NC+MP and OA (Nutri-acid; NC+MPOA) (Table 1
). Microbial phytase and Nutri-acid were provided by Canadian Bio-Systems Inc., Calgary, Alberta. The unit of phytase activity was defined as the amount of enzyme that liberates 1 µmol of phosphate/min at 37°C and pH 5.5. Nutri-acid was a broad-spectrum gut acidifier composed of citric, malic, phosphoric, sorbic, tartaric, and lactic acids and aluminate. Chromic oxide was used as an indigestible marker. All diets were pelleted.
In Vitro Experiment
The extent of phytate hydrolysis was assessed in an in vitro experiment using procedures similar to those described previously by Slominski et al. (1999; Figure 1). Four samples of phase-2 diets, finely ground to pass through a 1-mm screen, were incubated at 40°C in an incubator shaker set (New Brunswick Scientific, Edison, NJ) at 20 rpm for the appropriate time length. After incubation, hydrolyzed samples were freeze dried, and along with diet samples, were analyzed for phytate content (Haug and Lantzsch, 1983).
Animal Experiment
Ninety-six Cotswold piglets averaging 6.41 ± 0.71 (mean ± SD) kg of BW and weaned at 18 ± 1 d (mean ± SD) were blocked on the basis of sex and BW, and then assigned randomly from within block to the four dietary treatments. Each dietary treatment was assigned to six replicate pens (four pigs per pen). Pigs had unlimited access to feed and water. Individual BW and pen feed disappearance were monitored weekly. Room temperature was initially set at 29.5°C and gradually reduced by 1.5°C/wk. The trial lasted 28 d and was divided into two phases, with phase 1 and 2 lasting from d 0 to 14 and d 15 to 28, respectively. At the end of wk 3, a mobility test (Han et al., 1998) was carried out on six pigs per treatment by two swine specialists who were unaware of the dietary treatments using the following scale: 1 = unable to walk or stand, 2 = walks with great difficulty, 3 = walks with slight difficulty, 4 = good movement, 5 = very mobile.
At the end of the trial, one pig was selected at random from each pen, held under halothane general anesthesia, and killed by an intracardiac injection of sodium pentobarbital (50 mg/kg of BW). Digesta was collected from the stomach and terminal ileum and feces was collected from the rectum. Diet and digesta pH (Table 2) were determined and used as a basis to simulate the GIT conditions used in the in vitro study. The third metartarsal bone of the left hind leg was recovered from each pig and along with digesta samples kept frozen at -20°C until required for analysis. All experimental procedures were reviewed and approved by the University of Manitoba Animal Care Committee, and pigs were cared for according to the guidelines of the Canadian Council on Animal Care (CCAC, 1993).
Sample Preparation and Chemical Analysis
All analyses were performed in duplicate. Digesta and fecal samples were freeze dried, and along with diet samples, finely ground to pass through a 1-mm mesh prior to chemical analyses. Bone samples were thawed and cleaned to remove all adhering tissue and then carefully broken into smaller pieces. Broken bones were wrapped in Whatman’s No. 42 filter paper, stapled at the tip, and then defatted in hexane for 48 h. The bones were then air-dried and ashed in the furnace at 600°C for 12 h. Bone ash was expressed as a percentage of dry fat-free bone weight (modified from Spencer et al., 2000). Diet, digesta, and fecal samples were analyzed for DM according to AOAC procedures (1990). Phytate content in the diet, digesta, and fecal samples was determined using the method of Haug and Lantzsch (1983). Briefly 10 mL of 0.2 N HCl was added to 100 mg of diet or 30 mg of feces and the mixture was shaken for 3 h at room temperature and then filtered. Distilled water (0.5 mL) and 2 mL of ferric solution were then added to 0.5 mL of filtrate. The mixture was boiled for 30 min, centrifuged at 2,400 x g, after which 1.5 mL of bipyridine solution was added to 1 mL of the supernatant. The absorbance of the mixture was read against distilled water at 519 nm with a Pharmacia Ultrospec 2000 spectrophotometer. Total phosphorus (percentage) was determined according to the AOAC (1990) procedure. Chromic oxide was analyzed according to the procedure described by Williams et al. (1962). Diet and ileal digesta CP (N x 6.25) content were determined using a Leco NS 2000 nitrogen analyzer (Leco Corp., St. Joseph, MI.). A 100-mg sample of diet or ileal digesta was prepared by acid hydrolysis according to AOAC procedures (1984) and analyzed for AA as modified by Mills et al. (1989). The method involved digestion in 4 mL of 6 N HCl in vaccuo for 24 h at 110°C, followed by neutralization with 4 mL of 25% (wt/vol) NaOH, and then cooling to room temperature. The mixture was then made into a 50-mL volume with sodium citrate buffer (pH 2.2). Amino acids were then analyzed using a LK 4151 Alpha analyzer (LKB Biochrom, Cambridge, U.K.). The sulfur AA and tryptophan were not analyzed.
Calculation and Statistical Analysis
Digestibility coefficients and phytate hydrolysis were calculated using the following formula:
where Nf = Nutrient concentration in digesta (percentage of DM); Nd = Nutrient concentration in diet (percentage of DM); Cf = Cr2O3 concentration in digesta (percentage of DM); and Cd = Cr2O3 concentration in diet (percentage of DM). Phosphorus excretion (kg/t of feed consumed) was determined based on the analyzed P content of the rectal feces and was calculated as:
Data were analyzed as a completely randomized design using the GLM procedures of SAS (SAS Inst., Inc., Cary, NC). When a significant F-value for treatment means (P < 0.05) was observed in the ANOVA, treatment means were compared with Duncan’s multiple range test (Duncan, 1955).
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Results and Discussion
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Animal Performance
The analyzed nutrient composition of experimental diets (Table 3) was close to the calculated values in Table 1
. In phase 1, piglets fed the NC diet tended (P = 0.07) to have lower ADG than those fed the C, NC+MP, and NC+MPOA diets, which in turn were all similar (P > 0.10). Average daily gains in phase 2 and overall were similar irrespective of dietary treatment (Table 4). This observation is in agreement with results of Radcliffe et al. (1998) that showed no significant improvement in performance of piglets fed corn–soybean meal-based diets supplemented with MP and citric acid. Similarly, Han et al. (1998) failed to show a positive effect of plant phytase, MP, and citric acid on ADG and ADFI of young pigs. Significant differences in feed efficiency (gain:feed ratio) were observed during both phases of the experiment. In phase 1, NC+MP- and NC+MPOA-fed pigs had higher (P = 0.03) feed efficiency compared with NC fed pigs. In phase 2, piglets fed the NC and NC+MP diets had lower (P < 0.05) feed efficiency compared with pigs fed the C diet. However, piglets fed the NC+MPOA diet had similar (P > 0.05) feed efficiency as those fed the C diet. Similar effects of MP and or OA on feed efficiency in young pigs have been reported (Han et al., 1998).
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Table 4. Effect of supplemental microbial phytase and organic acids on performance of early-weaned pigs fed a corn–soybean-based diet
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The lack of improvement in piglet performance as a result of phytase and OA supplementation, despite some improvement in digestibilities of phytate P and other nutrients, has been reported in several studies (Thacker et al., 1992; Inborr et al., 1993; Radcliffe et al., 1998). In general, the effectiveness of phytase and OA in diets for young pigs has been poor and quite variable. This could be attributed to various factors, including age, diet, and enzyme preparation (i.e., single vs. multi-enzyme activities), which are known to influence phytate hydrolysis (Jongbloed and Kemme, 1990; Edwards, 1993). For example, phytase supplementation was found to improve performance in growing and finishing pigs more than in early-weaned pigs (Harper et al., 1997); an observation that could be explained by the low gastric acidity and increased microbial fermentation in the gut of older pigs. In the present study, the lack of improvement in piglet performance as a result of enzyme and OA supplementation could be explained by the fact that the NC diet was formulated to contain adequate levels of all other nutrients except for P to meet the piglets’ requirements for growth. In that case, MP and OA addition, as in the NC+MP, and NC+MPOA diets, might have only improved phytate P utilization, but not of other nutrients with no consequent improvement in growth. However, the fact that overall performance was similar among dietary treatments suggests that phytate P was well utilized to support growth in pigs fed the phosphorus-deficient diets. It is also possible that because only a single enzyme activity was used in the current experiment, improvement in the utilization of dietary nutrients other than phytate P was not high enough to impact a better piglet performance.
In Vitro and In Vivo Phytate Hydrolysis
The extent of phytate hydrolysis in the in vitro and in vivo studies is shown in Table 5. Phytate hydrolysis was higher in NC+MP and NC+MPOA diets compared with the C and NC diets in both the in vitro (P = 0.003) and in vivo (P = 0.0001) studies. Except at the feces level, addition of OA to the NC+MP diet did not further increase phytate hydrolysis (P > 0.10). Results of our study are in close agreement with that of Nernberg (1998), who observed a 90% in vitro phytate hydrolysis in a wheat canola-based diet supplemented with phytase at 1,100 U/kg. The maximal extent of in vitro phytate hydrolysis in the current study was 90.1%, which is slightly less than the 100% hydrolysis of rapeseed meal phytate by MP and acid phosphatase at 40°C reported by Zyla and Koreleski (1993). However, in subsequent studies by the same authors, phytase addition could not completely dephosphorylate phytates in corn–soybean meal diets under simulated turkey gastrointestinal tract conditions (Zyla et al., 1995). The lack of intestinal microorganisms in the in vitro system and the high calcium content of the diet could explain the incomplete in vitro phytate hydrolysis in the current study and that of Zyla et al. (1995). It has been reported that phytate hydrolysis is greatly reduced as calcium content of the diet is increased (Ballam et al., 1985).
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Table 5. Effects of supplemental microbial phytase and organic acids on in vitro and in vivo hydrolysis of phytate in phase 2 diets
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In the in vivo trial, phytate hydrolysis followed a trend similar to that of the in vitro study, with a higher (P = 0.0001) amount of phytate molecule being hydrolyzed with the inclusion of MP and OA to the NC diet (Table 5). However, phytate hydrolysis in the ileum and feces for the C and NC diets were higher than the levels seen in vitro (Table 5). Although not determined in the current study, this observation may be indicative of the action of endogenous phytase in the feed ingredients (Ravindran et al., 1995), the influence of intestinal microorganisms on nutrient digestion (Vogt et al., 1981), and/or the presence of appreciable endogenous phytase activities in the gut of pigs as observed for chickens (Bitar and Reinhold, 1972; Maenz et al., 1997).
Utilization of Phytate Phosphorus
Phosphorus released from phytate hydrolysis is utilized for body functions, especially for bone development. In the current study, a mobility scoring system and bone ash percentage were used as indicators of bone development (Han et al., 1998). The mobility score and bone ash content were lower (P < 0.05) in pigs fed the NC vs. C diet (Table 6). This might be due to the fact that no inorganic P was added to the NC diet (phase 2), thereby reducing the amount of P that could be used for bone development. This also increased the ratio of Ca to available P (4.38:1; Table 1), which has been shown to reduce the rate of P absorption and metabolism (Qian et al. 1996). Supplementing the negative control diet with MP or MP+OA improved both the mobility score (P = 0.06) and bone ash content (P = 0.003; Table 6) to the same levels as those for the control. The observed improvement in mobility score and bone ash content for pigs fed the NC+MP and NC+MPOA diets relative to those fed the negative control diet indicate that the phosphate groups liberated due to improved phytate hydrolysis were utilized for bone development. It is also possible that, by increasing P availability, MP+OA supplementation reduced the Ca:P ratio, thus contributing to increased P utilization (Qian et al., 1996). The present results suggest that addition of MP alone or MPOA may completely replace the use of inorganic phosphorus in diets of young pigs. This is in close agreement with the findings of Han et al. (1998), which indicated that supplementing a corn–soybean meal-based diet with microbial phytase (1,200 U/kg) and endogenous wheat phytase (15% of diet) improved (P = 0.002) mobility of early-weaned pigs relative to diets without phytase.
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Table 6. Mobility score and bone ash values of early-weaned pigs fed corn-soybean meal diets supplemented with microbial phytase and organic acids
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Digestibility of DM, Phosphorus, and Phosphorus Excretion
Digestibility of DM and P, P excretion, and the percentage reduction in P excretion are shown in Table 7. There were no differences (P = 0.23) in DM digestibility among treatments. Harper et al. (1997) and Jongbloed et al. (1996) were also unable to demonstrate an effect on DM digestibility as a result of supplementing weanling and growing pig diets with phytase or phytase plus lactic acid. Pigs fed the NC diet had a lower (P = 0.0001) P digestibility than those fed the C diet. This is because the inorganic P in the C diet is more digestible than the P from plant sources in the NC diet. The diets supplemented with MP or MP+OA had similar P digestibilities, which were higher (P = 0.0001) than those of the C and NC diets. Addition of phytase in the NC+MP diet only led to a numerical reduction (P > 0.10) in the amount of P excreted when compared to the C and NC diets. However, with the inclusion of OA (NC+MPOA diet), there was a significant reduction (P = 0.03) in the amount of P excreted per metric ton of feed consumed compared with the C diet.
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Table 7. Effect of supplementing corn–soybean meal-based diet with microbial phytase and organic acids on ileal DM, P digestibility, and P excretion
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The results of the current study indicating 39.8 and 85.4% increases in P digestibility with the addition of MP+OA compared with the C and NC diets, respectively (Table 7), are higher than the findings of Harper et al. (1997) and that of O’Quinn et al. (1997), which showed a 33 to 44% improvement in total-tract P digestibility when MP (500 U/ kg diet) was added to a sorghum–soybean meal-based diet fed to growing pigs. However, results obtained from short-term digestibility trials using weanling or very young pigs have indicated increases in P digestibility from 30 to 190%, depending on levels of phytase in the diet (Simons et al., 1990; Jongbloed et al., 1992; Lei et al., 1993a,b; Mroz et al., 1994; Kornegay and Qian, 1996).
Furthermore, the reduction in P excretion when pigs were fed the NC+MP and NC+MPOA diets was 12.9 and 19.4%, respectively, relative to pigs fed the control diet. This level of reduction in fecal P excretion is in close agreement with the values reported by Harper et al. (1997), who found a 21.5% reduction in P excretion when diets were supplemented with MP (500 U/kg diet). However, these values are somewhat lower than the levels (35 to 42%) reported by Lei et al. (1993a) and Kornegay and Qian (1996) in studies of younger pigs fed diets supplemented with higher levels of phytase than those used in the present study.
Apparent Crude Protein and Amino Acid Digestibility
Apparent ileal CP and AA digestibilities are shown in Table 8. There were no differences in apparent ileal CP digestibility among dietary treatments (P = 0.26). Supplementing the NC diet with MP alone or in combination with OA generally had no effect (P > 0.10) on apparent ileal digestibilities of essential AA, except for isoleucine (P = 0.0004) and histidine (P = 0.08), the digestibilities of which were improved (Table 8). Of all the dispensable AA, only the digestibility of aspartic acid was increased (P = 0.02) due to MP+OA supplementation compared with the C and NC diets. Nonetheless, the current observation is in agreement with that of Peter and Baker (2001) and Traylor et al. (2001) indicating no improvement in AA utilization in growing pigs fed soybean meal-based diets supplemented with MP. Similarly, O’Quinn et al. (1997) and Valaja et al. (1998) reported that MP supplementation had no effect on apparent ileal and total-tract CP and AA digestibilities in finishing pigs. However, others have found significant improvements in AA utilization due to the addition of MP to swine diets. For instance, Kemme et al. (1995) and Kornegay et al. (1998) reported improvements (P < 0.05) in AA digestibilities in growing pigs fed a corn–soybean meal-based diet supplemented with MP.
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Table 8. Effect of phytase and organic acids supplementation on apparent ileal digestibilities (%) of protein and amino acids in corn–soybean meal-based diets
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The primary objective of supplementing swine diets with MP is to facilitate the breakdown of the phytate molecule so as to make the phytate-bound P available for pig utilization. Because phytic acid is naturally associated with proteins in the aleurone layers of cereal grains and the protein bodies of oilseeds (deBoland et al., 1975), and because it is able to bind proteins and divalent cations such as Ca2+, Mg2+, and Zn2+ to form protein–mineral–phytate complexes (Cheryan, 1980; Grynspan and Cheryan, 1983), it is believed that facilitating its breakdown might also improve the availability of proteins and AA and minerals to the pig. In a study with rats, however, Thompson and Serraino (1986) could not demonstrate an effect on digestibility of proteins and absorption of AA in rapeseed flour containing 3 to 6% phytic acid. On the contrary, a recent study by Kornegay et al. (1998) showed improvements (P < 0.05) in AA digestibilities in growing pigs fed a corn–soybean meal-based diet supplemented with MP, suggesting that phytase may release AA that are otherwise bound to the phytate molecule. Although in the current study, AA digestibilities were generally unaffected by MP supplementation, numerical improvements ranging from 1.6 to 7.8% were observed due to MP+OA addition (Table 8). This might be due to the fact that the diets were formulated to be sufficient in protein and AA contents, in which case the effect of phytase addition on protein and AA digestibilities will not be easily detected.
The current study indicates the potential for MP and OA to eliminate the need to add inorganic P to the diets of early-weaned pigs. However, further research is needed to determine if a higher level of MP+OA may further increase phytate P utilization at the ileal level, and other dietary nutrients to enhance piglet performance.
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Implications
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The results of the present study clearly demonstrate that the addition of microbial phytase plus organic acids significantly improves phytate phosphorus utilization in young pigs fed diets low in inorganic phosphorus. Estimates from these data indicate that 500 U/kg of supplemental phytase plus 0.35% Nutri-acid may completely replace phosphorus from inorganic sources, while reducing fecal phosphorus excretion by approximately 20%. This finding is of significant importance to the swine industry since it may offer a means to reduce feed cost and provide a strategy to reduce the risk of environmental pollution that currently limits manure application to agricultural land. The question of whether phytase supplementation affects amino acid digestibilities deserves further investigation.
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Footnotes
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1 This research was financially supported by the Agri-Food Research Development Initiative (ARDI), Canadian Biosystems Inc., and Manitoba Pork Council. The help of R. Stuski with animal care and G. H. Crow with statistical design is gratefully acknowledged. 
Received for publication October 6, 2002.
Accepted for publication March 26, 2003.
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Abstract
Introduction
