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PHYSIOLOGY, ENDOCRINOLOGY, AND REPRODUCTION |
* Department of Zoology and Department of Wildlife Ecology, University of Wisconsin-Madison, Madison 53706
1 Corresponding author: fassbinderor{at}wisc.edu
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key Words: food restriction • realimentation • digestive efficiency • mucosal immune system • compensatory growth
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Although feed efficiency (BW gain/feed consumption) during feed restriction and realimentation periods has been well studied in poultry (Plavnik and Hurwitz, 1985, 1988; Santoso et al., 1995; Lee and Leeson, 2001), few studies address whether changes in feed efficiency are related to changes in the enzymatic or absorptive capacity of the gut or changes in postabsorptive processes. The secondary goal of this study was to investigate the effects of food restriction-realimentation protocols on the digestive efficiency of the gut. In birds, assimilation efficiency is used as a proxy for digestive efficiency, because both urine and feces are excreted together (Karasov, 1990). In this study, assimilation efficiency of chicks was estimated by determining the difference between intake rates and excretory loss rates of DM during periods of ad libitum feeding, feed restriction, and realimentation.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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One-day-old White Leghorn chicken cockerels were obtained from Sunnyside Inc. (Beaver Dam, WI). Chicks were housed individually in metal batteries in an environmentally controlled room with constant illumination and controlled temperature (25°C), and they were fed a standard starter chick diet that met the National Research Council (1994) requirements for both 17-d experiments. Chicks were weighed daily. At 7 d of age, chicks were divided into 3 treatment groups, with 10 chicks per group. Grouping was determined by BW, with each group having an average BW of 53 to 55 g/chick, but was otherwise random. Treatment groups and feeding schedules are shown in Figure 1
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Assimilation Efficiency Measurements
Because endogenous wastes mix with undigested material in the cloaca, the assimilable mass coefficient (AMC; a measure of assimilation efficiency) is an underestimate of the true assimilable mass coefficient (National Research Council, 1981). Therefore, we express the values as an apparent AMC, which is calculated as (Qi –Qe)/Qi, where Qi = the rate of food intake (g of DM/d); and Qe = the rate of excreta production (g of DM/d; Vohra, 1972; Miller and Reinecke, 1984). Collection trials began at 0800 h and ran for 3 consecutive days, when the chicks were 14 to 16 d of age. Subsamples of food from trial days were dried at 54°C for 48 h and weighed. The DM intake was determined as wet mass ingested x percentage dry mass. To collect excreta, the floor of each chick’s cage was lined with plastic-coated paper, such that the plastic liner formed the contact surface with the chicks. Excreta were collected from the liners every 24 h for 3 d. Following collection, excreta were dried at 54°C for 48 h then promptly weighed.
Organ Analysis
Immediately following euthanasia, the gut (small intestine, large intestine, and ceca) was removed from each bird. Gut flush samples for measurement of total IgA content were obtained according to Genton et al. (2004). Briefly, the entire gut of each bird was flushed with 10 mL of Hanks’ balanced salt solution (CMF-HBSS, Sigma-Aldrich, St. Louis, MO) the samples were centrifuged at 8,000 rpm for 5 min, then the supernatant was frozen at –80°C for 1 mo. The gut of each bird was then weighed to the nearest 0.01 g and measured for length. Next, the gizzard (Experiment 2 only), liver (Experiment 2 only), pancreas, spleen, and bursa of Fabricius of each bird were promptly removed and weighed.
Measurement of IgA Production
Total IgA production was determined from excreta samples in Experiment 1 and from gut flush samples in Experiment 2. Excreta samples were obtained from refed and control groups in Experiment 1, according to Holt et al. (1999). Briefly, feces were collected on d 16, dried, and 1 g of dry feces was diluted 1:10 with sterile Ca- and Mg-free Hanks’ balanced salt solution (CMF-HBSS; Sigma-Aldrich), pH 7.4. The samples were vortexed vigorously, processed as described above for the gut flush samples, then assayed for total IgA content. Gut flush samples from all 3 treatment groups in Experiment 2 were obtained as mentioned above and assayed for total IgA content. For assay, enzyme-linked immunosorbent plates were initially coated with 50 µL of a 1:100 dilution of goat anti-chicken IgA (Bethyl Laboratories, Montgomery, TX) in coating buffer (0.05 M carbonate-bicarbonate buffer, pH 9.6) and allowed to incubate for 60 min. Following incubation, wells were washed 3 times with a wash solution (50 mM Tris, 0.14 M NaCl, 0.05% Tween 20, pH 8.0). One hundred microliters of blocking buffer (50 mM Tris, 0.14 M NaCl, 1% BSA, pH 8.0) was then added to each well, incubated at 20°C for 30 min, then washed as above. Next, serial dilutions (2-fold) of samples were made in sample diluent (50 mM Tris, 0.14 M NaCl, 1% BSA, 0.05% Tween 20, pH 8.0), and 50 µL was added to each well. All samples were added in duplicate. Blanks (no test sample) and chicken IgA standards (Bethyl Laboratories) were also included on each plate. Following incubation, plates were washed 5 times with wash solution, and 50 µL of horse-radish peroxidase-conjugated goat anti-chicken IgA (Bethyl Laboratories), diluted 1:10,000 in sample diluent, were applied to each well. After a 60-min incubation and washing as above, plates were developed with 50 µL of tetramethylbenzidine-peroxidase substrate (Bethyl Laboratories) for 6.5 min. The reactions were stopped with 50 µL of 2 M H2SO4, and the optical density of each well was read at 450 nm with a spectrophotometer (model DU-64, Beckman Instruments, Fullerton, CA). A standard curve was created from the chicken standard samples using a 4-parameter logistic curve-fit (SYSTAT, Systat Inc., Evanston, IL; Wilkinson, 1999). The concentration of IgA for each test sample was calculated from the standard curve and expressed as nanograms of IgA/gram of intestinal flush contents or nanograms of IgA/gram of feces.
Enzyme Analysis
After flushing out the contents of the gut, tissue sections for enzyme analysis were obtained from the duodenum at the apex of the pancreas, the jejunum at a position midway between Meckel’s diverticulum and the entrance of the bile ducts, and the ileum at a position midway between Meckel’s diverticulum and the ileumcecal junction. Sections were dissected lengthwise to measure nominal surface area, and they were placed in 1.5-mL cryovials. The vials were then weighed and immediately frozen in liquid nitrogen, before being transferred to a –80°C freezer, where they were stored until further use. Before analysis, samples were thawed and homogenized with quantities of cold 300 mM mannitol in 1 mM N-2-hydro xyethylpiperazine-N'-2-ethanesulfonic acid-KOH buffer (pH 7.5) that resulted in a concentration of approximately 80 to 100 mg of intestine/mL of homogenate. Homogenizing was done by using a homogenizer (Ultra-Turrax T25 basic homogenizer, IKA-Werke GmbH, Staufen, Germany) at 24,000 rpm for 15 s.
Intestinal brush border enzyme activity was assessed using maltase and aminopeptidase-N, because they index the majority of brush border carbohydrate and peptide hydrolysis, respectively. Maltase activities were measured according to Dahlqvist (1984) as modified by Martinez del Rio et al. (1995). Briefly, gut homogenates (30 'µL) diluted with 300 mM mannitol in 1 mM hydroxyethylpiperazine-N'-2-ethanesulfonic acid-KOH were incubated with 30 µL of 56 mM maltose in 0.1 M maleate and NaOH buffer, pH 6.5, at 40°C for 20 min. Next, 400 µL of a stop-develop reagent (glucose assay kit; Sigma-Ald-rich, St. Louis, MO) was added to each tube, vortexed, and incubated at 40°C for 30 min. Lastly, 400 µL of 12 N H2SO4 was added to each tube, and the absorbance was read at 540 nm. Apparent Michaelis constant (Km) and optimal pH for intestinal maltase activity were 9.1 ± 1.8 mM (mean ± SE, n = 6) and 6.5, respectively. Activity was normalized by intestinal wet mass.
Aminopeptidase-N activity was measured according to Caviedes-Vidal and Karasov (2001), with some modifications. Briefly, 10 µL of gut homogenate was added to 200 µL of assay mix (2.0 mM L-alanine p-nitroanilide in 1 part 0.2 M NaH2PO4-Na2HPO4, pH 7.0, and 1 part deionized H2O) previously heated to 40°C. The reaction solution was incubated for 25 min at 40°C, 600 µL of ice-cold 2 N acetic acid was added, and absorbance was measured at 384 nm. Apparent Michaelis constant (Km) and optimal pH for intestinal aminopeptidase-N activity were 1.1 ± 0.2 mM (mean ± SE, n = 6) and 7.5, respectively. Activity was normalized by intestinal wet mass.
Data Analysis
Values are given as mean ± 1 SE. Body masses, maltase activity, aminopeptidase-N activity, and apparent AMC were tested by ANOVA (GLM in SYSTAT; Wilkinson, 1999) according to experimental group (control, feed-restricted, and refed) for both Experiment 1 and 2. To compare assimilation efficiency differences between experimental groups, excreta production was tested by analysis of covariance (ANCOVA) for an effect of an experimental group using intake as a covariate. No significant interactions between intake and experimental groups were found. Organ masses and total IgA production were tested first by ANOVA, according to experimental group, then by ANCOVA, using body mass as a covariate (Lee et al., 2002). No significant interactions between body mass and groups were found. The F-values for the ANCOVA are presented in the text with the relevant degrees of freedom as subscripts. Subsequent post hoc comparisons among experimental groups were made on the adjusted least squares means from the ANOVA or AN-COVA, using the Tukey honestly significant difference test. The significance level was set at P < 0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The mean body mass of feed-restricted birds in Experiment 1 was significantly less than that of control birds (P < 0.003) on the final day of the experiment (Figure 2, panel A). However, no significant difference was found between the body mass of the refed birds and the control birds in Experiment 1. In Experiment 2, the final body mass of control birds was significantly greater than both restricted and refed birds (P < 0.01), but no significant difference existed between the mass of refed and restricted birds in Experiment 2 (Figure 2, panel B).
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, panel A). During the first day of realimentation for the refed group (d 13), chicks gained an average of 17.7 ± 1.4 g. This rapid weight increase was followed by 3 d of growth that paralleled (i.e., did not exceed; F1,19 = 1.3, P > 0.25) the control group. In Experiment 2, a 34% ad libitum feed restriction resulted in minimal growth (0.8 ± 0.3 g/d; Figure 2, panel B). Upon realimentation on d 13, refed birds gained an average of 17.3 ± 1.4 g, followed once again by 3 d of growth parallel to control chicks (F1,17 = 0.43, P > 0.5). Digestive Efficiency Measurements
Dry excreta production was significantly correlated with intake for both Experiment 1 (F1,17 = 39.9, P < 0.001) and 2 (F1,25 = 30.2, P < 0.001; data not shown). In Experiment 1, refed chicks produced significantly less excreta per unit of intake compared with control chicks (F1,17 =20.9, P < 0.001). The AMC for refed birds was significantly higher than the AMC for control birds (P < 0.001; Figure 3, panel A). Excreta were not collected from feed-restricted birds in Experiment 1.
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, panel D). Enzyme Analysis
Maltase activity was highest in the jejunum for all groups in both experiments (P < 0.001; Figure 4). In Experiment 1 (Figure 4, panel A), duodenal maltase activity was significantly higher in the refed birds than the control or feed-restricted birds (P < 0.01). There were no significant differences among groups for jejunal or ileal maltase activity in Experiment 1. In Experiment 2 (Figure 4, panel B), no significant differences in maltase activity among groups were found in any intestinal section.
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Organ Analysis and Measurement of IgA Production
Because of the differences among groups in body mass, we will discuss organ masses and IgA production corrected for body mass differences by ANCOVA.
In Experiment 1, intestine and pancreas masses of refed birds were significantly higher than both control and feed-restricted birds (P < 0.05; Figure 3, panels B and C). In Experiment 2, intestine and pancreas masses of the refed group were significantly higher than those of the feed-restricted group (P < 0.006; Figure 3, panels E and F). However, intestine and pancreas masses of refed and feed-restricted birds were not significantly different from control birds in Experiment 2. Gizzard masses were measured in Experiment 2, with the following mean values obtained: feed-restricted: 4.11 ± 0.19 g, refed: 4.31 ± 0.15 g, and control: 4.55 ± 0.2 g. No significant differences in gizzard masses existed among groups (F2,24 = 5.89, P > 0.41). The following liver masses were also recorded in Experiment 2: feed-restricted: 2.81 ± 0.22 g, refed: 3.75 ± 0.10 g, and control: 3.60 ± 0.24 g. Although the liver masses of the refed group were significantly higher than those of the feed-restricted group (P < 0.006), liver masses of refed and feed-restricted birds were not significantly different from control birds in Experiment 2.
No differences among groups existed in either Experiment 1 or 2 for bursa and spleen masses or total IgA production (Figure 5).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Assimilation efficiency appeared to be increased in re-fed birds, compared with controls, in both experiments. Although increased feed efficiency (BW gain/feed consumption) during feed restriction and realimentation periods has been demonstrated a number of times (Plavnik and Hurwitz, 1985, 1988; Leeson and Zubair, 1997; Lee and Leeson, 2001; Urdaneta-Rincon and Leeson, 2002), ours was the first study, to our knowledge, that found evidence that increased digestive efficiency might play a role in increased feed efficiency. The increased digestive efficiency may be partly explained by a significant increase in digestive organs’ masses (relative to body mass) of refed birds in both Experiment 1 and 2, which would contribute to greater digestive capacity for enzymatic breakdown and absorption. In Experiment 1, there was a significant increase in intestinal and pancreas masses (relative to body mass) of refed birds compared with controls and feed-restricted birds. In Experiment 2, there was a significant increase in intestine, pancreas, and liver masses of refed birds compared with feed-restricted birds. Zubair and Leeson (1994) observed similar results, in which an increase in relative pancreas and liver mass occurred during the realimentation period following a feed restriction. Although intestine, pancreas, and liver masses of refed birds in Experiment 2 were not significantly different from control birds, this may be due to the fact that the digestive organ masses of feed-restricted birds were generally more atrophied in the 34% ad libitum feed restriction (mean feed-restricted intestine mass equaled 71% of control) compared with the 54% ad libitum feed restriction (mean feed-restricted intestine mass equaled 78% of control), delaying, to a greater extent, the completion of recovery of digestive organ mass.
In Experiment 1, the increase in assimilation efficiency may also be partly explained by the increase in duodenal maltase activity in the refed group compared with both control and feed-restricted groups. The results observed in Experiment 1 are in agreement with Palo et al. (1995), in which an increase in intestinal maltase and sucrase activity was observed 7 d after a 4-d, 20% ad libitum feed restriction. Our findings are also in agreement with Pinheiro et al. (2004), in which an increase in intestinal sucrase activity was observed 1 d following a 7-d, 70% ad libitum feed restriction. Nitsan et al. (1974) indicated that the production of intestinal enzymes was largely the result of the mechanical stimulation of chyme passing through the digestive tract. Hyperphagy was observed during the first day of realimentation in the refed birds in both experiments. This may have increased the mechanical stimulation of the intestinal tract, which may have led to the increased production of intestinal enzymes in the refed group.
When chickens are fed increased amounts of particular dietary substrates (e.g., carbohydrates and proteins), the result is a corresponding increase in the activities of relevant brush border enzymes for those substrates (Siddons, 1972; Biviano et al., 1993; Caviedes-Vidal et al., 1994). For example, chickens fed a diet containing 50% carbohydrate exhibit almost twice the level of sucrase and maltase activity compared with chickens on a carbohydrate-free diet (Biviano et al., 1993). This phenomenon may also help explain the increased maltase activity in the refed birds of this study, following the observed hyperphagy during their realimentation phase.
There appeared to be no effect of feed restriction and subsequent realimentation on the weight of selected immune organs (bursa of Fabricius and spleen) or IgA production in the gut of Leghorn chicks. In both experiments, there were no significant differences in spleen or bursa weights among treatment groups. Additionally, total IgA production did not differ among groups in either Experiment 1 or 2. Similar findings were reported by Liew et al. (2003), who found no significant differences in antibody titers or bursa-to-BW ratios between broiler chicks fed ad libitum and chicks fed 60% ad libitum. Our results were in contrast to work done by El Hadri et al. (1998), who found that thymus, spleen, and bursa weights of turkeys were reduced relative to BW when the birds were restricted to maintenance feed intake.
We conclude that the moderate feed restriction and realimentation protocols used in this study did not affect the general immune structure of Leghorn chickens. Also, assimilation efficiency appeared to be increased during the first 3 d of realimentation following a feed restriction. Lastly, the improved assimilation efficiency of the refed birds may be attributed to a relative increase in digestive organ masses and an increase in duodenal maltase activity compared with control and feed-restricted birds.
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ACKNOWLEDGMENTS |
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Received for publication January 27, 2006. Accepted for publication March 27, 2006.
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) feed-restricted (
), and refed (
) groups in Experiment 1 (panel A) and Experiment 2 (panel B). Letters next to the final data points denote statistical differences among mean final body masses; data points not sharing the same letter are different (P < 0.05).
