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*
U.S. Department of Agriculture/ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, TX 77030;
L. G. Laboratories, Inc. and
**
American Protein Corporation, Ames, IA 50010
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: • plasma protein • lean tissue growth • amino acid catabolism • urea metabolism • weanling pigs
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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, Kats et al. 1994
). However, increased food
consumption can often account for the stimulation of growth rate in
pigs fed diets containing SDP. Some studies with early-weaned pigs
(Kats et al. 1994
) and mice (Thomson et al. 1995
) have demonstrated that dietary plasma not only enhances
food conversion efficiency but specifically improves nitrogen
retention, thereby implying an increase in the efficiency of dietary
protein utilization. Consistent with this interpretation, we recently
found that the dietary protein conversion efficiency (weight gain per
unit of protein intake) of pigs fed a diet containing 10% SDP was
~18% greater than that of pigs fed a control diet without animal
plasma, despite the fact that the protein intake was 30% higher in
pigs fed SDP (Jiang et al. 2000
). The circulating plasma
urea concentration was significantly lower (~40%) in pigs fed a diet
containing 10% SDP compared with those fed a control, corn–soy
protein diet (Jiang et al. 2000
). These results suggest
that feeding SDP increases the efficiency of growth; however, it is not
clear whether the increased growth takes the form of lean or fat
tissue. We wished to test the hypothesis that supplementing the diet of early-weaned pigs with animal plasma rather than extruded soy protein (ESP) increased the efficiency of dietary protein utilization for lean tissue growth. To test this, we pair-fed young pigs either a diet containing 10% SDP or a control diet where SDP was replaced with ESP. Pigs in both dietary groups were fed a protein intake that was limiting for maximum lean tissue deposition and were measured for the effect on the rate of weight gain and body composition.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The protocol was approved by the Animal Care and Use Committee of
Baylor College of Medicine and was conducted in accordance with NIH
guidelines (National Research Council 1985
). A total of
24 pigs from multiple litters of commercial crossbred pigs were
purchased from Texas Department of Criminal Justice (Huntsville, TX)
and transported to the Children’s Nutrition Research Center when they
were 14 days old (~4.0 kg body weight). Pigs were randomly assigned
to receive either a control diet (C) or a diet containing animal plasma
(P). SDP was derived from porcine and bovine blood (APC 920, American
Protein Corporation, Ames, IA). The diet ingredients and calculated
macronutrient compositions are described in Table 1
. Food intake in both the control and plasma groups was restricted to
~80% of the observed ad libitum intake in similar-age pigs fed
the control diet in our previous study (Jiang et al. 2000
). The targeted food intake in both the C and P pigs was
~48 g/kg body weight. Based on this dry matter intake, the daily
protein intake was ~75–85% of the National Research Council
requirement for pigs ranging from 4 to 10 kg body weight
(National Research Council 1998
). Pigs were weighed
every other day and fed twice daily. Food intake was adjusted every
2 d to maintain equal intake per kg of body weight. Pigs were
housed individually with free access to water. Collection pans were
changed every 2 d to remove urine/feces. The room was maintained
at 26–28°C. Lights were off between 1800 h and 0600 h.
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At d 24, the pigs were offered 50% of their daily intake 2 h before killing. Prior to killing, venous blood samples were drawn, immediately transferred to Na2-EDTA tubes and centrifuged (1200 x g, 10 min, 4°C). The plasma was frozen in liquid nitrogen and stored at -70°C until used for analysis of urea and amino acids. Subsequently, pigs were killed with pentobarbital (50 mg/kg body weight). The small intestine, from the pylorus to the ileocecal junction, was removed, flushed with ice-cold saline and weighed. The stomach was flushed with ice-cold saline and weighed along with the liver and spleen.
Analysis of plasma amino acids and urea concentrations.
Samples (0.5 mL) for amino acid concentration measurements were mixed with an equal volume of aqueous solution of methionine sulfone (internal standard) and centrifuged, at room temperature through a 3 kDa-molecular-weight cutoff filter. The filtrate was lyophilized and the amino acids were analyzed by reverse-phase high performance liquid chromatography for their phenylisothiocyanate derivatives (PicoTag, Waters, Woburn, MA). Plasma urea levels were assayed with the BUN (endpoint) Kit (Sigma Diagnostics, St. Louis, MO).
Body composition analysis.
Body composition was determined by dual-energy X-ray absorptiometry
(DXA) using a Hologic QDR-2000 DXA as described previously
(Ellis and Shypailo 1993
). The stomach and small
intestinal contents were removed as mentioned above, all dissected
organs were placed back in the abdominal cavity and the pig carcasses
were frozen at -20°C. The frozen carcasses were scanned using the
single-beam infant whole body mode (version 5.71p). Scan results
provided values for total body bone mineral content (BMC), bone mineral
density (BMD), nonbone lean tissue and total body fat mass. Summing BMC
and lean tissue values provides a measure of fat-free mass (FFM).
The composition of the frozen carcasses was also determined by total
body potassium (TBK) based on 40K analysis as described
previously (Ellis and Shypailo 1993
).
Statistical analysis.
Data obtained at the end of the 24-d period were subjected to one-way ANOVA, with dietary treatment as the independent variable. In the case of protein intake, body weight gain and protein efficiency results, data were analyzed by repeated measures ANOVA with both treatment and days of treatment as main effects but also included the effect of treatment within animal in the model. Significance was assigned at P < 0.05. All data were expressed as mean ± SD
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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); however, in both groups protein intake increased during the 24-d
period (day effect, P < 0.001). We found that feeding
plasma protein significantly increased (treatment effect, P
< 0.05) mean daily weight gain and protein efficiency expressed
as the ratio of weight gain to protein intake (Fig. 1)
. Also, weight
gain, but not protein efficiency, significantly increased during the
24-d period (day effect, P < 0.001). For protein
intake, weight gain and protein efficiency, there were no significant
interactions between treatment and days on treatment. However, the
greatest differences in weight gain (45%) and food conversion
efficiency (43%) were observed between 0 and 8 d of dietary
treatment. Pigs in both groups started with similar initial body weight
(C vs. P = 4.0 ± 0.4 vs. 4.3 ± 0.5 kg), but P pigs
(10.8 ± 1.3 kg) were 16% heavier (P < 0.05)
than the C pigs (9.3 ± 0.9 kg) at 24 d.
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). Lean tissue mass, estimated by both DXA and TBK analysis, was also
significantly (P < 0.05) greater in P pigs than in C
pigs. Moreover, the proportional difference between the treatment
groups was similar using both the DXA (+16%) and TBK (+15%) analysis.
The relative lean body mass per kg carcass and TBK per kg FFM were
similar in both groups. This latter result indicates that the
composition and degree of hydration of the lean tissue mass were
similar in both groups. Feeding plasma protein did not affect the mass
of the small intestine (C vs. P = 46.3 ± 7.3 vs. 42.9
± 4.3 g/kg body weight), stomach (C vs. P = 8.2 ± 0.4
vs. 8.0 ± 1.3 g/kg body weight), liver (C vs. P = 33.2
± 3.4 vs. 33.8 ± 3.7 g/kg body weight) or spleen (C vs. P
= 2.4 ± 0.7 vs. 2.5 ± 0.9 g/kg body weight).
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). Total free amino acid concentrations in plasma were similar
(P > 0.05) between C and P pigs. However, the plasma
concentrations of arginine, citrulline and ornithine, were 44, 57 and
30% lower (P < 0.05), respectively, in P than in C
pigs. Similarly, the branched-chain amino acids, isoleucine and
valine, as well as histidine and asparagine concentrations in plasma
were lower (P < 0.05), respectively, in P pigs than C
pigs, whereas the plasma threonine concentration in the P group was
24% greater (P < 0.05) than in the C group.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). It is apparent
from many of these studies that dietary SDP stimulates growth rate,
largely by increasing food intake. Improvements in food conversion
efficiency have been reported in some studies of young pigs fed SDP,
although there is a limited understanding of biological mechanisms that
explain this response. A study in mice suggested that feeding SDP
increases the efficiency of nitrogen utilization (Thomson et al. 1995
); however, this response has not been reported in pigs.
Our objective in this study was to determine whether supplementing
early-weaned pig diets with animal plasma rather than extruded soy
protein increases the efficiency of dietary protein utilization for
lean tissue growth. The rate of weight gain and dietary protein conversion efficiency was significantly higher in the plasma than in the control group, even though both groups had a similar dietary protein intake. The greatest effects of dietary plasma protein on growth rate and protein efficiency occurred during the first 8 d and tended to diminish between 8 and 24 d of treatment, indicating a maximum benefit occurred during the weaning transition. These differences in dietary protein conversion efficiency, calculated per unit of protein intake, indicate that supplementing SDP rather than ESP increased the efficiency of dietary protein utilization for weight gain. However, we wanted to distinguish whether the stimulation of weight gain in response to feeding SDP was a result of differential rates of fat or lean tissue deposition, or perhaps due to increased tissue hydration. Our results showed that pigs fed SDP had a larger carcass weight and absolute mass of protein and BMC, but their fat mass was not significantly greater. Thus, feeding SDP did not alter the relative carcass composition in either group, indicating that feeding SDP did not preferentially increase either fat or lean tissue growth. An exception to this was the finding that both the BMD and the relative carcass BMC were significantly greater in P versus in C pigs. Taken together, our results demonstrate that supplementing the diet with SDP rather than ESP increased the efficiency of dietary protein utilization for lean tissue growth.
Even though the SDP and ESP represented less than half of the total
dietary protein, the difference in protein utilization between the SDP-
and ESP-supplemented diets could be ascribed to the relatively
lower amino acid availability and increased antigenicity of proteins
normally found in soy products. However, the analyzed amino acid
concentrations were not significantly different between the two diets
(data not shown). Studies show that the moist extrusion process
enhances the quality of soy protein, such that growth and nitrogen
digestibility are similar in young pigs fed diets containing ESP and
dried milk protein (Friesen et al. 1993
, Li et al. 1991
). Furthermore, studies have shown that feeding SDP
increases growth of weaned pigs, even when it replaces a high quality
protein (e.g., skim milk or casein) in the diet (Coffey and Cromwell, 1995
, Thomson et al. 1995
). Thus,
further studies are necessary to establish whether the superior quality
of SDP can be attributed simply to increased amino acid availability or
if indeed it contains biologically active components, such as
immunoglobulins, that enhance the efficiency of dietary protein
utilization.
Given the evidence that the efficiency of dietary protein use was
greater in pigs fed the SDP compared with the control diet containing
extruded soy protein, we wished to determine whether this response was
associated with changes in the circulating nitrogen metabolites. In our
previous study, we found that the circulating urea concentration was
markedly lower in pigs fed SDP compared with a control diet, and that
this was independent of dietary protein intake (Jiang et al. 2000
). This result, coupled with the observation of reduced
intestinal mass in our previous study, led us to postulate that feeding
SDP may reduce the catabolism of dietary amino acid within the
intestine, leading to decreased urea production and consequently
increased efficiency of dietary protein utilization. In this study, we
found that feeding plasma reduced the plasma urea concentrations by
~40%, a value strikingly similar to that observed in our previous
study (Jiang et al. 2000
). Contrary to our previous
study, however, in the current study we found that intestinal mass was
similar in the plasma and control groups at 24 d. The reduction in
circulating urea suggests that feeding SDP reduced urea production,
presumably as a result of decreased amino acid catabolism. However,
whether this phenomenon is linked to altered amino acid metabolism in
the gut or perhaps other tissues such as the liver requires further
study, given the current finding that feeding SDP did not significantly
affect gut mass. However, it is notable that the circulating
concentration of threonine was higher, whereas the concentrations of
arginine, citrulline and ornithine, were lower in plasma-fed versus
control pigs. Studies have shown that the intestine is a significant
site of dietary threonine utilization (Stoll et al. 1998
) and of arginine and citrulline synthesis (Wu et al. 1998
). Thus, further studies are necessary to determine
whether feeding SDP affects amino acid catabolism and whether this
occurs in the gut or liver, thereby increasing availability of dietary
amino acids for growth.
In summary, our results indicate that supplementing weaning pig diets
with SDP rather than ESP increased the efficiency of dietary protein
use for lean tissue growth. We also found that feeding SDP reduced the
circulating concentrations of urea, arginine, citrulline and ornithine.
These results, coupled with the findings from our previous study
(Jiang et al. 2000
), suggest that feeding SDP may reduce
the catabolism of amino acids to urea and that this results in
increased availability of dietary amino acids for lean tissue growth.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Address to whom reprint requests should be addressed.
3 Abbreviations: BMC, bone mineral content; BMD, bone mineral density; DXA, dual-energy X-ray absorptiometry; ESP, extruded soy protein; FFM, fat-free mass; SDP, spray-dried porcine and bovine plasma; TBK, total body potassium
Manuscript received January 4, 2000. Revision accepted March 30, 2000.
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REFERENCES |
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1. Coffey R. D., Cromwell G. L. The impact of environment and antimicrobial agents on the growth response of early-weaned pigs to spray-dried porcine plasma. J. Anim. Sci. 1995;73:2532-2539[Abstract]
2. Ellis K. J., Shypailo R. J. Whole body potassium measurements independent of body size. Ellis K. J. Eastman J. D. eds. Human Body Composition 1993;vol. 60:371-375 Plenum Press New York.
3. Freisen K. G., Nelssen J. L., Goodband R. D., Behnke K. C., Kats L. J. The effect of moist extrusion of soy products on growth performance and nutrient utilization in the early-weaned pig. J. Anim. Sci. 1993;71:2099-2109[Abstract]
4.
Jiang R., Chang X., Stoll B., Fan M. Z., Arthington J., Weaver E., Campbell J., Burrin D. G. Dietary plasma protein reduces small intestinal growth and lamina propria cell density in early-weaned pigs. J. Nutr. 2000;130:21-26
5. Kats L. J., Nelssen J. L., Tokach M. D., Goodband R. D., Weeden T. L., Dritz S. S., Hansen J. A., Friesen K. G. The effects of spray-dried blood meal on growth performance of the early-weaned pig. J. Anim. Sci. 1994;72:2860-2869[Abstract]
6. Li D. F., Nelssen J. L., Reddy P. G., Blecha F., Klemm R. D., Giesting D. W., Hancock J. D., Allee G. L., Goodband R. D. Measuring suitability of soybean products for early-weaned pigs with immunological criteria. J. Anim. Sci. 1991;69:3299-3307[Abstract]
7. National Research Council Guide for the Care and Use of Laboratory Animals. Publication No. 85–23(rev.) 1985 National Institutes of Health Bethesda, MD.
8. National Research Council Nutrient Requirements of Swine 10th ed. 1998 National Academy Press Washington, DC.
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Stoll B., Henry J., Reeds P. J., Yu H., Jahoor F., Burrin D. G. Catabolism dominates the first-pass intestinal metabolism of dietary essential amino acids in milk protein-fed piglets. J. Nutr. 1998;128:606-614
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