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The effect of dietary protein and fermentable carbohydrates levels on growth performance and intestinal characteristics in newly weaned piglets¹

P. Bikker^*,2, A. Dirkzwager^*,3, J. Fledderus^*, P. Trevisi^,4, I. le Huërou-Luron, J. P. Lallès and A. Awati^,5

^* Schothorst Feed Research, Lelystad, the Netherlands; and Institut National de la Recherche Agronomique, UMR SENAH, 35590, Saint-Gilles, France; and and Department of Animal Nutrition, Wageningen University and Research Centre, Wageningen, the Netherlands

	Abstract

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Reducing the CP content and increasing the fermentable carbohydrates (FC) content of the diet may counteract the negative effects of protein fermentation in newly weaned piglets fed high-CP diets. To study the synergistic effects of CP and FC on gut health and its consequences for growth performance, 272 newly weaned piglets (26 d of age, 8.7 kg of BW) were allotted to 1 of 4 dietary treatments in a 2 x 2 factorial arrangement, with low and high CP and low and high FC content as the factors. Eight piglets from each dietary treatment were killed on d 7 postweaning. Feces and digesta from ileum and colon were collected to determine nutrient digestibility, fermentation products, and microbial counts. In addition, jejunum tissues samples were collected for intestinal morphology and enzyme activity determination. During the entire 4-wk period, interactions between the dietary CP and FC contents were found for ADFI (P = 0.022), ADG (P = 0.001), and G:F (P = 0.033). The high-FC content reduced ADFI, ADG, and G:F in the low-CP diet, whereas the FC content did not affect growth performance in the high-CP diet. Lowering the CP content of the low-FC diet improved ADFI and ADG, whereas lowering the CP content of the high-FC diet did not influence growth performance. The low-CP diets resulted in a lower concentration of ammonia in the small intestine (P = 0.003), indicating reduced protein fermentation. In the small intestine, the high FC content increased the number of lactobacilli (P = 0.047), tended to decrease the number of coliforms (P = 0.063), tended to increase the lactic acid content (P = 0.080), and reduced the concentration of ammonia (P = 0.049). In the colon, the high-FC diets increased the concentration of total VFA (P = 0.009), acetic acid (P = 0.003), and butyric acid (P = 0.018), and tended to decrease the ammonia concentration (P = 0.076). Intestinal morphology and activity of brush border enzymes were not affected by the diet, although maltase activity tended to decrease with increasing dietary FC (P = 0.061). We concluded that an increase in the dietary FC content, and to a lesser extent a decrease in the CP content, reduced ammonia concentrations and altered the microflora and fermentation patterns in the gastrointestinal tract of weaned piglets. However, these effects were not necessarily reflected by an increased growth performance of the piglets.

Key Words: fermentable carbohydrate • growth • intestinal health • piglet • protein • weaning

	INTRODUCTION

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
High amounts of CP in the diet of newly weaned piglets may predispose them to postweaning coli-bacillosis because of the high buffering capacity of dietary protein in the stomach (Prohaszka and Baron, 1980). Furthermore, high dietary protein levels may also stimulate protein fermentation and encourage proliferation of pathogenic bacteria in the gastrointestinal tract (GIT; Ball and Aherne, 1987). The end products of protein fermentation (e.g., amines and ammonia) are considered to be detrimental for the host animal (Nollet et al., 1999).

Protein fermentation can be reduced by either lowering the amount of CP in the diet (Nyachoti et al., 2006) or by inclusion of fermentable carbohydrates (FC) in the diet, such as fructooligosaccharides (Houdijk, 1998), lactitol (Piva et al., 1996), resistant starch, and wheat bran (Govers et al., 1999). With increased supply of FC as an energy source, an excess of indigestible protein is more likely to be incorporated into bacterial protein rather than being fermented to be used as a source of energy (Houdijk, 1998). Inclusion of FC in the diet influences the composition and activity of the GIT microbiota (Williams et al., 2001). As a result, dietary fiber may provide some protection against postweaning coli-bacillosis (Aumaitre et al., 1995). However, the consequences of inclusion of greater amounts of FC on growth performance of the piglets remain unclear.

Therefore, the aim of this experiment was to determine whether the beneficial effects of dietary FC can be realized with mainly commonly used feed ingredients under farm-like circumstances. Furthermore, the additional objective was to determine whether the effects of CP reduction and FC inclusion are synergistic and whether these effects are reflected by gut epithelial integrity and growth performance of newly weaned piglets.

	MATERIALS AND METHODS

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Animals and Dietary Treatments
The experimental protocol used in this study was approved by the ethical committee of Schothorst Feed Research, Lelystad, the Netherlands. The experiment was conducted with 272 Yorkshire x Landrace piglets, with initial BW of 8.7 ± 0.2 kg at weaning at 26 ± 1 d of age. At weaning, piglets were allotted to 1 of 4 dietary treatments with low and high CP and low and high FC according to a 2 x 2 factorial arrangement, with 10 replicates for each dietary treatment. Piglets were blocked on the basis of litter and BW. Littermates of similar BW were randomly allocated to the treatments. Four replicates began with 8 piglets per pen and 6 replicates with 6 piglets per pen. Replicates contained equal numbers of females and castrated males.

Four pelleted experimental diets were formulated with low (15%) or high (22%) CP content, combined with low (7.5%) or high (13.4%) FC content (Table 1). Fermentable carbohydrates were defined as the sum of the fermentable nonstarch polysaccharides (NSP) and the ileal indigestible fraction of native starch. Fat was included in the high-FC diets to balance the NE content of the diets. Synthetic amino acids were added to obtain equal amounts of digestible amino acids in all diets. Chromic oxide and AIA (Diamol, D1 100G, Poortershaven, Rotterdam, the Netherlands) were added as markers for determination of nutrient digestibility. Piglets had free access to feed and water throughout the experimental period. Feed was supplied in a dry feeder with a wide trough, which allowed all piglets to consume feed simultaneously.

Measurements and Analyses
Piglets in each pen were weighed as a group on d 0 (weaning), 7, 14, and 28. Feed intake was recorded weekly, and ADG, ADFI, and G:F were calculated per pen.

In addition, piglets in the 4 replicates, with 8 piglets per pen, were weighed individually on d 0 and 6. Two representative piglets (based on BW) from each of these pens (in total 8 piglets per dietary treatment) were selected for determination of digestibility and intestinal characteristics. From these piglets, fecal samples (approximately 20 g) were collected rectally once daily on d 6 and 7 and stored for analysis at 4°C. Aliquots of these samples were mixed, freeze-dried, and analyzed to determine nutrient digestibility.

On d 7 these piglets were sedated with an i.m. injection of a ketamin-xylazine combination (3.5 mL of Ketamin 10%, Alfasan, Woerden, the Netherlands, and 1.5 mL of Rompun, Bayer, Leverkussen, Germany), killed by an intracardiac injection of a lethal dose of embutramide (4 mL of T-61, Intervet Nederland B.V., Boxmeer, the Netherlands), and dissected. Different segments of the digestive tract were located and tied off to avoid mixing of digesta of different segments of the GIT during the handling. The length of the small intestine was recorded. Digesta were collected from the last 2 m of the small intestine before the ileocecal junction, which was designated ileum, and from the flexura centralis of the colon. Digesta were collected in aluminium trays and subsampled in glass beakers on ice for VFA and ammonia analyses and in buffered peptone for bacterial counting. An intestinal segment of about 20 cm was obtained at the midpoint of the small intestine and designated jejunum. The mucosa and muscularis mucosa from this segment were separated and weighed. The specific activities of disaccharidases (maltase and sucrase) and aminopeptidase-N were determined in the small intestinal mucosa (Marion et al., 2005). Maltose, sucrose, and leucine-p-nitroanilide were used as the respective substrates.

For morphometry, the small intestinal segments were opened, washed with saline and fixed in buffered formalin (10%) for 24 h at 4°C. Thereafter the samples were rehydrated, stained with Schiff’s reagent and dissected under a microscope, according to the methods of Goodlad et al. (1991). Villi and crypts were observed under a light microscope at a magnification of 10x and 16x, respectively, using an optical microscope (Eclipse E400), a camera (Digital camera DXM1200, Nikon), and an image analyzer (Lucia Software; Lucia, 2001). A total of 20 villi and 10 crypts were measured for each sample, and averages were calculated for each piglet as described by Piel et al. (2005).

The experimental diets were analyzed for moisture (ISO, 1999b), CP (N x 6.25; ISO, 2004), crude fiber (NEN, 1988), crude ash (ISO, 2003b), crude fat with acid hydrolysis (ISO, 1999a), starch (ISO, 2005), total sugar (NEN, 1974), AIA (ISO, 2003a), and Cr (spectrophotometer) contents. The pellet hardness was analyzed with the Schleuninger method, as described by Thomas and van der Poel (1996).

Freeze-dried ileal digesta and feces were analyzed for moisture content, CP, crude fiber, crude fat, and starch. Ash and AIA contents of feces, and Cr₂O₃ content of ileal digesta were determined. Fecal digestibility of nutrients was calculated based on the content of AIA as a marker in feed and feces, whereas ileal digestibility of nutrients was calculated based on the Cr₂O₃ content as a marker in feed and ileal digesta.

In the fresh digesta samples from ileum and colon, bacterial cell counts of coliform bacteria and lactobacilli, along with the concentration of NH₃, lactic acid, and the VFA profile were determined. The VFA concentrations in the fermentation liquids were analyzed by gas chromatography (Fisons HRGC Mega 2, CE Instruments, Milan, Italy), using a glass column fitted with Chromosorb 101 (Supelco, Bellefonte, PA), and N₂ saturated with methanoic acid as the carrier gas, at 190°C, and using isocaproic acid as an internal standard. The lactic acid concentration of the digesta was analyzed according to the method described by Voragen et al. (1986) using HPLC (Jasco Benelux BV, Maarssen, the Netherlands) with a Supelcogel HPLC column (C-610 H, ID 30 cm x 7.8 mm, Sigma-Aldrich Chemie BV, Zwijndrecht, the Netherlands). Ammonia was determined according to the method described by Searle (1984).

For bacterial counts, fresh digesta samples were suspended (10%, wt/vol) in a buffered peptone solution and subsequently homogenized with a dispersing instrument (Ultra Turrax T25, Janke & Kunkel, IKA-labortechnik, Staufen, Germany). Thereafter, 10-fold dilutions were made with a buffered peptone physiological salt solution (CM509, Oxoid Ltd., Basingstoke, Hampshire, UK; containing peptone 10.0 g/L, sodium chloride 5.0 g/L, di-sodium phosphate 3.5 g/L, and potassium dihydrogen phosphate 1.5 g/L). For the enumeration of lactobacilli, 20 µL of each dilution was pipetted as a drop on Man Rogosa Sharpe agar. The plates were incubated anaerobically for 24 h at 37°C. The compact or feathery, opaque, and white lactobacilli colonies were counted. For the enumeration of E. coli and total coliforms, 1 mL of solution was pipetted onto an E. coli/coliform count plate (3M Petrifilm, Europe Laboratoires 3M Santé, Cergy-Pontoise, France) with Violet Red Bile gel and an indicator of glucuronidase activity. The plates were incubated for 48 h at 37°C, and all blue E. coli colonies and total coliform colonies were counted following method 147.1993 of the NMKL (Nordic Committee on Food Analysis).

Statistical Analysis
Pen was the experimental unit for ADFI, ADG, and G:F. Analysis of variance was performed using GenStat (2000). Data were analyzed as a 2 x 2 factorial arrangement of treatments, with dietary CP and FC content as the factors, in 10 randomized blocks. Statistical analysis of digestibility, bacteriology, fermentation products, histology, and enzymology was performed using the data from 8 dissections per treatment, with piglet as the experimental unit. Differences were considered significant at P < 0.05. Tendencies for 0.05 < P < 0.10 are also presented. There were no interactions between CP and FC for digestibility or intestinal characteristics, and therefore the main effects of CP and FC have been presented.

	RESULTS

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Animal Performance
Piglets remained healthy throughout the experiment. In Table 2, ADFI, ADG, and G:F are presented. For the entire period of 4 wk after weaning, interactions between dietary CP and FC content were found for ADFI (P = 0.022), ADG (P = 0.001), and G:F (P = 0.033), indicating that the effects of CP and FC on performance were not synergistic. Increasing the FC content of the low-CP diet reduced ADFI, ADG, and G:F, whereas increasing the FC content of the high-CP diet did not affect ADFI, ADG, or G:F. Furthermore, the reduction in CP content improved ADFI and ADG for piglets fed the low-FC diet, but not for piglets fed the high-FC diet. These interactions were already observed in wk 2 and wk 3 to 4 for ADFI and ADG, but not significantly for G:F. In wk 1, no effects of dietary treatment on ADFI, ADG, or G:F were observed.

Jejunal Weight and Morphology, and Activity of Enzymes
There was no interaction between CP and FC levels for small intestinal anatomical, morphological, and enzymology characteristics (Table 5). The small intestine tended to be shorter (P = 0.094) when high levels of FC were fed to the piglets. Dietary treatments had no effect on density of the gut wall muscularis + serosa or mucosa, but with high levels of FC, the activity of maltase tended to be lower (P = 0.061). Dietary treatments did not influence the villus height and crypt depth.

	DISCUSSION

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

Lower levels of CP in the diet resulted in a lower ammonia concentration in the small intestine, indicating a lesser degree of protein fermentation. However, the lower ammonia concentration observed with the low-CP diets did not coincide with any effect on coliforms or lactobacilli counts or VFA concentration in jejunum or colon. Nyachoti et al. (2006) also showed that a reduction in the CP content of the feed (from 23 to 17%) reduced the ammonia concentration in the small intestine, but no effects on the microbial population in ileal digesta, including E. coli and coliforms, were observed in their study. This may indicate that although dietary CP content affects protein fermentation and the concentration of fermentation end products, a high CP content per se does not necessarily result in an overgrowth of potentially pathogenic bacteria in the small intestine. Other factors, such as sanitary conditions in the environment, are likely to play a role.

The high FC content resulted in an increase in the number of lactobacilli and a reduction in the number of coliforms in the small intestine. This indicates a beneficial shift in the composition of microbial population in response to dietary FC as also observed by Konstantinov et al. (2004) who used sugar beet pulp, inulin, and lactulose as FC sources. The shift in microbial population was also reflected by fermentation end products, such as a lower ammonia concentration and a comparatively higher lactic acid concentration in the small intestine with the high-FC diet. This was in agreement with observations of Awati (2005). On the other hand, Hopwood et al. (2004) found increased proliferation of beta-hemolytic E. coli in the small and large intestine of piglets fed diets high in NSP from pearl barley. This discrepancy may be explained by the extremely low NSP level in their control diet with cooked white rice and the increase in viscosity of intestinal contents in piglets consuming higher amounts of soluble NSP from barley.

The increase in lactobacilli, with subsequent decrease in the coliforms in the small intestine, as found in our study can be attributed to the phenomenon of colonization resistance (Van der Waaij, 1989). The increased lactobacilli may out-compete the coliforms for space for adhesion and nutrient availability in the GIT. Similar findings also have been reported in humans, showing that lactic acid-producing bacteria suppress the activity of pathogenic bacteria, such as E. coli and clostridia (Gibson and Roberfroid, 1995).

In the large intestine, fermentation was stimulated by the high dietary FC level, as indicated by higher concentrations of total VFA, acetic acid, and butyric acid. Ammonia concentration in the colon tended to be lower with the high-FC diets, which implies that mainly carbohydrates, and not proteins, were fermented. It may also reflect a possible increase in the incorporation of N into bacterial biomass when high-FC diets were fed. A reduction in protein fermentation with FC inclusion in the diet has also been reported in pig studies using lactose and inulin (Pierce et al., 2006) and a combination of sugar beet pulp, native wheat starch, lactulose, and inulin (Awati, 2005).

Many authors have reported that increasing the amount of fermentable fiber in the diet stimulates microbial fermentation and organic acid production in the foregut and in the hindgut of pigs (Williams et al., 2001; Jensen, 2001; O’Doherty et al., 2006). In the small intestine, lactic acid is the main fermentation product, whereas VFA are the major products in the large intestine (Jensen and Jørgensen, 1994; Jensen, 2001, Högberg and Lindberg, 2004). Volatile fatty acids, and especially butyric acid, serve as an energy source for colonocytes and improve the structure and function of the colonic epithelial cells in humans (Roediger, 1980; Young and Gibson, 1995) and pigs (Darcy-Vrillon et al., 1993). It is likely that the increase in the butyric acid content in the colon in the current study was the result of both the inclusion of native (resistant) potato starch and NSP from other ingredients. Topping and Clifton (2001) showed that resistant potato starch is effective in producing butyrate in the colon. Van der Meulen et al. (1997) showed a great increase in butyrate absorption in the portal vein with inclusion of potato starch in the diet. Also, NSP from sugar beet pulp, wheat middlings, and others have been shown to increase VFA production in the large intestine (Govers et al., 1999; Jensen, 2001). The high number of lactobacilli in the jejunum and colon and the low lactic acid content in the large intestine indicate that high levels of lactic acid have been produced and absorbed or used as a substrate for VFA production in the large intestine (MacFarlane and MacFarlane, 2003). Tsukahara et al. (2002) suggested an indirect relationship between lactic acid-producing bacteria and butyrate, i.e., with higher counts of lactic acid producing bacteria, more lactate is produced and converted into butyrate by acid-utilizing bacteria in the gut lumen. Therefore, in our study, butyric acid formation in the colon may have been directly stimulated by the presence of resistant starch and NSP in the diet and by stimulation of lactate-producing bacteria in the gut. This may have beneficial effects for gut wall integrity in the colon. However, small intestinal wall morphology was not affected by dietary treatment in our study.

Dietary treatments had no effects on the anatomy, morphology, and enzyme activities in the jejunum. The tendency for a lower amylase activity in piglets fed the high-FC diets may be related to the lower amount of starch provided by the high-FC diets (Trevisi et al., 2005) and may partly explain the lower starch digestibility as reported by Suvarna et al. (2005) in poultry. These findings confirm the changes in fermentation end product profile in the small intestine do not necessarily contribute to the integrity of the small intestinal wall. This may also be related to the site of fermentation and amount of substrate. Pierce et al. (2006) reported an interactive effect of dietary lactose and inulin in the diet on villus height in the jejunum but not in the ileum.

This study does not confirm the potentially beneficial effects of a lower ammonia concentration on villous height as suggested by Nousiainen (1991). Nyachoti et al. (2006) also found no consistent effects of a dietary CP reduction on villus height and crypt depth in different segments of the small intestine, despite a great reduction in ammonia concentration. However in the current study, morphology of the distal small intestine and colon was not studied. Therefore, it was not possible to assess a potential effect of dietary treatments on the wall integrity of the lower GIT through altered fermentation products.

Despite the effects of dietary FC on fermentation in the GIT, increasing the FC content did not improve growth performance of the weaned piglets. Rather, increasing the FC content of a low-CP diet negatively affected performance, probably because it decreased the availability of dietary nutrients to the host animal. The latter can be due to an increased nutrient usage by the GIT microflora (Jensen, 2001) and by a negative effect of dietary FC on nutrient digestibility as reflected by the lower CP and starch digestibility in piglets fed the high FC diets. The results indicate that a high-FC diet can reduce nutrient availability and growth performance, especially in a low-CP diet. In literature, the influence of FC in diets on growth performance of weaned piglets varies considerably among studies (e.g., Högberg and Lindberg, 2004; O’Doherty et al., 2006). Decreasing the amount of CP in a low-FC diet did enhance ADFI and ADG from wk 2 after weaning, despite the lower CP-digestibility in low-CP diets. Nyachoti et al. (2006) found a linear decrease in ADFI and ADG when dietary CP was reduced from 23 to 17%, probably because 1 or more amino acids became limiting. In their experiment, the diets with higher CP contents also contained higher amounts of crude fiber and NSP, so that CP content and fiber content were confounded in their study. Le Bellego and Noblet (2002) found no adverse effect on piglet performance of lowering the CP content of the diet from 22.4 to 16.9%.

In conclusion, our results indicate that increasing the dietary FC content stimulates lactic acid producing bacteria and lactic acid production, may reduce counts of coliform bacteria and reduce protein fermentation in the small intestine. In the large intestine, FC increases concentrations of VFA, especially acetic acid and butyric acid. FC inclusion is more effective than CP reduction in improving fermentation and microbial composition in weaned piglets. However, the effects on fermentation are not necessarily reflected by growth performance. The present results indicate no beneficial effects of higher dietary FC contents on growth performance of weaned piglets.

	Footnotes

 
¹ This work has been carried out with financial support of the European Community specific RTD programme "Quality of Life and Management of Living Resources" research project HEALTHYPIGUT (QLK5-CT2000-00522). The authors wish to thank C. M. Makkink for her assistance in preparing this manuscript.

³ Present address: Gezondheidsdienst voor Dieren, P.O. Box 9, 7400 AA Deventer, the Netherlands.

⁴ On doctoral leave from DIPROVAL, University of Bologna, via f.lli Rosselli 107, 42100 Reggio Emilia, Italy.

⁵ Present address: Riddet Centre, Massey University, Private bag 11222, Palmerston North, New Zealand.

² Corresponding author: PBikker{at}schothorst.nl

Received for publication February 10, 2006. Accepted for publication July 19, 2006.

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Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 


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