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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, Ames, IA 50010; and
American Protein Corporation, Ames, IA 50010
4To whom correspondence and reprint requests should be addressed.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: • immunoglobulins • urea • growth • amino acid catabolism • weanling pigs
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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,
Gatnau and Zimmerman 1990
, Hansen et al. 1993
, de Rodas et al. 1995
) and in some cases,
improved food conversion efficiency (Kats et al. 1994a
and 1994b
). An explanation for the increased consumption of diets
containing SDP has not been firmly established, although increased
palatability may be a factor (Ermer et al. 1994
). This
in itself will lead to an increased growth rate. However, the
biological effects underlying the improved food conversion efficiency
in animals fed plasma protein are poorly understood.
Spray-dried plasma protein is a complex mixture, containing fibrinogen
immunoglobulin and albumin. It has not been established that these
proteins retain their biological activity after the spray-drying
process. However, the improvement in growth rate and food conversion in
mice fed SDP can be reproduced by including only the immunoglobulin
fraction of SDP, and not the fibrinogen or albumin fractions
(Godfredson-Kisic and Johnson 1997
). This suggests that
the immunoglobulin fraction of SDP is responsible for the improved
growth. Consistent with this, the growth response to SDP was greater in
pigs housed in a commercial nursery (presumably with a higher exposure
to pathogens) than in pigs housed in a controlled experimental nursery
environment (Coffey and Cromwell 1995
). Although it is
unlikely that the immunoglobulins present in SDP are absorbed across
the intestinal wall in 3- to 4-wk-old pigs, they may affect the
intestinal microflora and or the local intestinal immune responses
associated with the weaning transition.
Immunoglobulin preparations derived from animal products have been
shown to contain measurable titers of antibodies against a variety of
bacterial pathogens (Rump et al. 1992
). Studies indicate
that nonspecific immunoglobulin G (IgG) preparations reduce the
incidence of diarrhea when given orally to human immunodeficiency virus
patients infected with Cryptosporidium parvum
(Greenberg and Cello 1996
); they also reduced the rate
of bacterial infection when given intravenously to preterm infants
(Baker et al. 1992
). Thus, it is conceivable that
immunoglobulins derived from spray-dried animal plasma also contain
antibodies against pathogens present in the environment of weanling
pigs and hence have an antimicrobial effect. Although the antimicrobial
action of spray-dried plasma has not been established, it has been
shown to reduce small intestinal mass and increase nitrogen retention
in weanling mice (Thomson et al. 1995
); both of these
responses are characteristic of those observed in animals fed
antibiotics (Visek 1978
). However, the effects of
dietary plasma protein on intestinal growth in weanling pigs have not
been reported.
The objectives of this study were to quantify the effects of dietary plasma protein on small intestinal mass and mucosal morphology in weanling pigs. We hypothesized that dietary plasma protein would lower small intestinal mass in weanling pigs. To eliminate the potentially confounding effect of increased food intake on these endpoints of intestinal growth, one group of pigs was given free access to the plasma protein–containing diet and another group was pair-fed the same diet to the intake level of the pigs fed the control diet.
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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 (NRC 1985
). A total of 96 pigs from multiple litters
of commercial crossbred pigs were purchased from the Texas Department
of Criminal Justice (Huntsville, TX) and transported to the Children’s
Nutrition Research Center in Houston when they were 14 d old
[~4.0 kg in body weight (BW)]. Pigs were received in the evening,
deprived of food overnight and then immediately fed their respective
diets the next day (15 d old) without an adaptation period. Pigs were
assigned into a 3 x 4 randomized complete block design with three
dietary treatment groups and four time periods. There were eight
replicates of this design. The dietary treatments were as follows:
1) the control diet (C), in which pigs were allowed free
access to the control diet; 2) the plasma protein diet
(P), in which pigs were allowed free access to the same diet with the
protein replaced by porcine plasma protein concentrate; and
3) plasma protein pair-fed (PPF), in which pigs were
fed the P diet at the intake level (per unit of body weight) of the C
group mean. The diet compositions are shown in Table 1
. Both the control and plasma protein diets were formulated to meet or
exceed the nutrient requirements of 5- to 10-kg pigs (NRC 1998
) and balanced for lysine and methionine, the first and
second limiting amino acids. The diets were isocaloric, but the plasma
diet contained slightly less (22 vs. 24%) crude protein than the
control diet. Within a dietary regimen, subgroups of pigs were killed
at 2, 4, 8 or 16 d. Within each replicated block of animals, one
pig was killed on the initial day of the study (d 0). Pigs were weighed
daily and fed twice daily. Food intake of the PPF group was adjusted to
match that of the C group on the basis of body weight. Pigs were housed
individually and had free access to water in cages, which were not
cleaned regularly to simulate an "unclean" environment similar to
that in some swine production facilities. Collection pans were changed
every 2 d for removal of urine and feces. The room was maintained
at 30°C. Lights were off between 1800 and 0600 h.
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At 0, 2, 4, 8 and 16 d, pigs were given an intraperitoneal injection of 5-bromodeoxyuridine (BrdU, 50 mg/kg, Sigma-Aldrich Chemical, St. Louis, MO) 4 h before killing to label intestinal crypt cells in S-phase. Before killing, venous blood samples were collected for the measurement of blood urea nitrogen, cortisol and blood cell counting. Subsequently, pigs were killed with pentobarbital (50 mg/kg BW). The small intestine, from the ligament of Treitz to the ileocecal junction, was removed and flushed with ice-cold saline and then divided into four segments (proximal jejunum, distal jejunum, proximal ileum and distal ileum) of equal length and weighed. The length of each segment was also measured. A 2- to 3-cm section of the proximal portion of each segment was removed and stored in 4% paraformaldehyde in PBS for subsequent histologic analysis. The remainder of each segment was frozen in liquid nitrogen. Stomachs were flushed with ice-cold saline and weighed. Liver and spleen were also weighed.
Morphometry.
After dehydration in 70% alcohol, paraformaldehyde-fixed intestinal samples were embedded in paraffin sliced to ~5 µm and stained with hematoxylin and eosin. Villous height, crypt depth, muscularis thickness and total cells in the intravillous lamina propria were measured by using an Axiophot microscope (Carl Zeiss, Scarsdale, NY) with NIH Image software version 1.60 (National Institutes of Health, Bethesda, MD) in 15 vertically well-oriented villi and crypts. Cell density in the intravillous lamina propria was expressed as the number of visibly stained nuclei per square millimeter. The area from which cell numbers were counted was quantified using the image analysis program. Crypt to villous cell ratio was calculated by dividing villous height by crypt depth. Gut wall thickness was calculated as the sum of villous height, crypt depth and muscularis thickness. All morphometric analysis was done by the same person, who was unaware of treatment groups.
BrdU immunohistochemistry.
Sections (5 µm) of paraformaldehyde-fixed paraffin-embedded intestinal segments were mounted on ProbeOn Plus (Fisher Scientific, Pittsburgh, PA) slides at 60°C for 30 min. Slides were incubated at 70°C in a humidified chamber for 10 min. Then slides were rehydrated through a series of xylene and ethanol solutions, rinsed with H2O 1X PBS and incubated in prewarmed 1X Target Unmasking Fluid (Boehringer, Mannheim, Germany) at 90°C for 10 min. Slides were incubated with blocking serum (1% sheep serum, The Binding Site, San Diego, CA) in a humidified chamber at 40°C for 15 min. The blocking serum was removed, and the slides were incubated with undiluted mouse anti-BrdU nuclease reagent (Amersham Life Science, Arlington Heights, IL) at 40°C for 45 min.
Slides were rinsed with 1X PBS to remove excess primary antibody and incubated with a 1:500 dilution of biotinylated universal second antibody (anti-mouse IgG2a, The Binding Site) in a humidified chamber at 40°C for 30 min after incubation with 1X PBS containing 0.3% H2O2 (Fisher Scientific) and 0.1% NaN3 (EM Science, Gibbstown, NJ) for 10 min at room temperature. Staining of BrdU-labeled cells was achieved using an ABC Reagents Kit (Avidin-Biotin horseradish peroxidase macromolecular complex; Vector Labs, Burlingame, CA) and a DAB (3,3'-diaminobenzidine) Substrate Kit for peroxidase (Vector Labs). Briefly, slides were incubated in a solution containing the avidin-biotin complex, followed by a solution containing hydrogen peroxide, DAB and nickel, which formed a black precipitate to improve the contrast. Slides were counterstained with 0.1% Mayer’s hematoxylin solution for 45 s. Crypt cell proliferation index was quantified by a single observer, who was unaware of treatment groups, by counting the number of BrdU-labeled nuclei in 15 vertically well-oriented crypts under a microscope. The percentage of BrdU-labeled cells relative to the total number of crypt cells was calculated.
Total and differential leukocyte counts.
Total leukocyte counts were determined from EDTA-treated whole-blood samples with an electronic cell counter (Danam Electronics, Dallas, TX).
DNA and protein analysis.
Tissue samples (100–200 mg) were homogenized in water. Aliquots were
removed for analysis of DNA and protein using bis-benzimide
(Labarca and Paigen 1980
) and a BCA kit (Pierce,
Rockford, IL), respectively.
Cortisol and urea concentrations in plasma.
Plasma cortisol (ICN Biomedicals, Costa Mesa, CA) and urea (Sigma Diagnostics, St. Louis, MO) concentrations were measured with the use of commercially available assays.
Statistical analysis.
Data were subjected to two-way ANOVA with dietary treatment and days of treatment as the independent variables. Differences between dietary treatment groups on a given day were compared using the Fisher’s protected multiple comparison test. Significance was assigned at P < 0.05. All data were expressed as means ± SD.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). Body weight gain did not differ in the C and PPF groups. Pigs in the
P group consumed 33% more (P < 0.05) dietary protein
than those in the PPF (Table 2)
. No significant difference in protein
intake was observed either between the C and P groups or between the C
and PPF groups. Dietary protein conversion efficiencies in both plasma
protein treatment groups were not significantly different but both were
~18% greater (P < 0.05) than those in the control
group.
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), and in DNA and protein masses (Table 3
) associated with treatment and age. Small intestinal mass increased
significantly with age; however, there was an interaction with
treatment. By 16 d, small intestinal masses per BW in the P and
PPF groups were 13% (P < 0.05) and 11% (P
< 0.05) lower than those in the control group, respectively, but
no significant differences were observed at other time periods. Both
jejunal and ileal protein and DNA masses increased significantly with
age. Between 0 and 8 d, there were no significant differences in
intestinal protein and DNA masses (Table 3)
. After 16 d of dietary
treatment, jejunal protein masses were lower (P < 0.05) in the P (-13%) and PPF (-18%) treatment groups than in the C
group. Similarly, after 16 d of dietary treatment, both jejunal
and ileal DNA masses were 15–20% lower (P < 0.05) in
the P and PPF groups than in the C group. Dietary plasma protein had no
effect on small intestinal length or the mass of the stomach, liver or
spleen (results not shown).
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). However, there were no significant treatment differences in these
endpoints. There were significant increases in intravillous lamina
propria cell density associated with age; however, there was an
interaction with treatment (Fig. 2
). The intravillous lamina propria cell density was significantly lower
(P < 0.05) in both the P and PPF groups than in C pigs
at 4, 8 and 16 d. We did not quantify the specific phenotype of
the intravillous lamina propria cells. However, on the basis of the
cellular morphology, we found that most of the intravillous lamina
propria cells were lymphocytes with lesser amounts of macrophages.
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). Plasma urea decreased with age; however, there was an interaction
with treatment. Plasma urea concentrations were significantly lower in
both the P and PPF groups compared with the C group on the basis of the
two-way ANOVA of time x treatment and means comparison test
of values at d 16. Weaning is associated with increased stress and
inflammation; thus we measured the plasma cortisol and white cell count
during the 16-d period. Over the 16-d period, plasma cortisol and white
blood cell concentrations did not differ among the three treatment
groups. However, plasma cortisol concentrations decreased significantly
(age effect P < 0.05) between 2 and 16 d of
treatment in all three groups [126, 129, 45 and 78 at 2, 4, 8 and
16 d, respectively, mean (nmol/L) pooled SD = 99].
The total plasma white cell count increased significantly (age effect
P < 0.05) between 2 and 16 d of treatment in all
groups [8400, 11800, 15600 and 17200 at 2, 4, 8 and 16 d,
respectively, mean (cells/µL) and pooled SD =
5275].
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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, de Rodas et al. 1995
, Gatnau and Zimmerman 1990
, Hansen et al. 1993
, Kats et al. 1994a
and 1994b
). It is apparent from most of these
studies that dietary plasma protein stimulates the growth rate largely
by increasing food intake. This stimulation of food intake is a
beneficial response because anorexia is an important factor limiting
growth rate during the weaning transition (Leibbrandt et al. 1975
, Seve 1982
). However, the explanation for
observed improvements in food conversion efficiency is less obvious.
Among the possible biological effects of dietary plasma protein are
increased villous surface area and intestinal absorptive function,
which may translate into increased efficiency of dietary nutrient
utilization (Thomson et al. 1995
). To determine whether
dietary plasma protein affects small intestinal structure, we measured
the temporal changes in small intestinal growth and mucosal morphology
in weanling pigs during a 16-d period. During the 16-d weaning period, several endpoints of intestinal growth were significantly increased in all treatment groups. The intestinal protein and DNA masses, the crypt depth and proliferation rate, and the intravillous lamina propria cell density all increased ~50–100%. In contrast, despite the transient reduction between 2 and 8 d after weaning, villous height was not significantly different at 0 and 16 d. Thus the increase in intestinal growth during the 16-d period was largely a result of increased cellularity in the crypt and lamina propria regions of the mucosa, whereas the ratio of villous to crypt cells decreased significantly.
Feeding plasma protein progressively decreased the relative growth of
the small intestine, with a significant effect after 16 d. The
reduction in intestinal mass is consistent with a previous study with
mice (Thomson et al. 1995
). The reduction in intestinal
growth was similar in both plasma protein groups, despite significant
differences in protein intake, suggesting that this response was a
function of dietary plasma protein. However, we did not observe any
significant differences in mucosal villous height, crypt depth or cell
proliferation index that would explain the reduced intestinal protein
and DNA masses in the plasma protein–fed groups. This is contrary to
previous studies with pigs, which demonstrated that dietary plasma
protein increases villous height and thus, perhaps, absorptive surface
area (Cain 1995, Spencer et al. 1997
).
Therefore, our results suggest that dietary plasma protein reduces
intestinal mass but does not increase villous height or absorptive
surface area.
Studies have shown that weaning is associated with increased intestinal
inflammation (Cummins et al. 1991
, McCracken et al. 1999
, Zijlstra et al. 1999
); thus, the
differences we observed in total intestinal protein and DNA content
could also reflect changes in cellularity of the lamina propria as well
as the epithelial cell layer. We observed a significant increase in
total blood leukocyte numbers during the 16-d period, suggestive of a
systemic proinflammatory response, but found no differences among the
dietary groups. In addition, we found that the intestinal intravillous
lamina propria cell density increased during the 16-d period. Although
the specific cell phenotypes were not quantified, we found that most of
the cells in this intravillous region were lymphocytes. Thus, the
increase in cell density may be a consequence of increased local
intestinal inflammation. The lamina propria cell density was
significantly lower in both groups fed plasma protein than in the
control group. Therefore, we speculate that dietary plasma protein may
suppress the local intestinal proinflammatory response associated with
weaning and thereby reduce leukocytic infiltration into the mucosal
lamina propria.
Previous studies with early-weaned pigs (Kats et al. 1994a
and 1994b
) and mice (Thomson et al. 1995
) have
reported that dietary plasma protein enhances food conversion
efficiency and specifically improves nitrogen retention, thereby
suggesting an increase in the efficiency of dietary protein
utilization. Consistent with previous reports, we found a significant
increase in the dietary protein conversion efficiency in both plasma
protein–fed groups. A contributing factor that may explain the
increased efficiency of dietary protein utilization was the marked
reduction in plasma urea concentrations observed in both groups of pigs
fed plasma protein. We should note that the plasma protein diet
contained slightly less protein (22 vs. 24%) and may explain in part
the lower circulating urea concentration in the plasma of PPF pigs than
in C pigs. However, the increased efficiency of protein use and the
decrease in circulating urea concentrations were observed in both
groups fed SDP, despite the fact that the protein intake was
significantly higher in P than in PPF pigs. This suggests that these
effects were independent of protein intake and were a specific effect
of dietary plasma protein. Taken together, these findings suggest that
feeding plasma protein suppressed amino acid catabolism, and this
contributed to the increased nitrogen utilization.
Although the precise nature of this response is unclear, it is tempting
to speculate that the reduction in intestinal mass and cellularity is
linked to the reduction in circulating urea concentrations. The
presence of plasma protein in the intestinal lumen may have
antimicrobial effects, which suppress the catabolism of amino acids to
ammonia and subsequently to urea. Indeed, antimicrobials, notably the
antibiotic neomycin, have been shown to significantly decrease
intestinal ammonia release when fed to pigs (van Berlo et al. 1988
).
Given the evidence that the intestine is an important site of dietary
amino acid catabolism (Stoll et al. 1998
), it will be
important in future studies to establish whether feeding plasma protein
affects intestinal nitrogen metabolism directly.
In summary, our results indicate that supplementing SDP in weanling pig diets enhanced dietary protein conversion efficiency, reduced intestinal mass and the density of intravillous lamina propria cells, and also markedly reduced the circulating urea concentrations. These effects were independent of food intake and suggest a specific biological effect of plasma protein. Although it is possible that these findings are not directly related, together they suggest that plasma protein increases the efficiency of protein utilization, perhaps by minimizing amino acid catabolism and increasing the systemic availability of dietary amino acids for growth.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Supported in large part by a grant from the L. G. Laboratories, Incorporated, Ames, IA.
3 Supported in part by federal funds from the U.S. Department of Agriculture, Agricultural Research Service under
Cooperative Agreement number 58–6250-6001. The contents of this publication do not necessarily reflect the views or policies of the U.S. Department of Agriculture, nor does mention of trade names,
commercial products, or organizations imply endorsement by the U.S. Government.
5 Abbreviations used: BrdU, 5-bromo-2'-deoxyuridine; BW, body weight; C, control diet; IgG,
immunoglobulin G; P, plasma protein diet. PPF, plasma protein pair-fed to C; SDP, spray-dried porcine plasma.
Manuscript received June 25, 1999. Initial review completed July 22, 1999. Revision accepted October 8, 1999.
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A. Owusu-Asiedu, S. K. Baidoo, C. M. Nyachoti, and R. R. Marquardt Response of early-weaned pigs to spray-dried porcine or animal plasma-based diets supplemented with egg-yolk antibodies against enterotoxigenic Escherichia coli J Anim Sci, November 1, 2002; 80(11): 2895 - 2903. [Abstract] [Full Text] [PDF]
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P. A. Ludden, T. L. Wechter, and B. W. Hess Effects of oscillating dietary protein on nutrient digestibility, nitrogen metabolism, and gastrointestinal organ mass in sheep J Anim Sci, November 1, 2002; 80(11): 3021 - 3026. [Abstract] [Full Text] [PDF]
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R. Jiang, X. Chang, B. Stoll, K. J. Ellis, R. J. Shypailo, E. Weaver, J. Campbell, and D. G. Burrin Dietary Plasma Protein Is Used More Efficiently than Extruded Soy Protein for Lean Tissue Growth in Early-Weaned Pigs J. Nutr., August 1, 2000; 130(8): 2016 - 2019. [Abstract] [Full Text]
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