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A tryptophan-enriched diet improves feed intake and growth performance of susceptible weanling pigs orally challenged with Escherichia coli K88¹

P. Trevisi^*, D. Melchior, M. Mazzoni^*, L. Casini^*, S. De Filippi^*, L. Minieri^*, G. Lalatta-Costerbosa and P. Bosi^*,2

^* DIPROVAL, University of Bologna, 42100 Reggio Emilia, Italy; and Ajinomoto Eurolysine S.A.S., 75017 Paris, France; and DIMORFIPA, University of Bologna, 40064 Ozzano dell’Emilia, Italy

	Abstract

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We tested the effect of Trp addition to a standard weaning diet and oral challenge with enterotoxigenic Escherichia coli K88 (ETEC) on growth and health of piglets susceptible or nonsusceptible to the intestinal adhesion of ETEC. Sixty-four pigs weaned at 21 d of age were divided into 3 groups based on their ancestry and BW: a control group of 8 pigs fed a basal diet (B), the first challenged group of 28 pigs fed B diet (BCh), and the second challenged group of 28 pigs fed a diet with Trp (TrpCh). The Trp diet was produced by the addition of 1 g of L-Trp/kg to the basal diet. On d 5, pigs were orally challenged with 1.5 mL suspension containing 10¹⁰ cfu ETEC/mL or placebo, and killed on d 9 or 23. Based on in vitro villus adhesion assay, the pigs (except the B group) were classified as susceptible (s⁺) or nonsusceptible (s^–) to the intestinal ETEC adhesion. Thus, after the challenge, treatments were B, BChs^–, BChs⁺, TrpChs^–, and TrpChs⁺. Pigs susceptible to ETEC were 50.0% in the BChs⁺ group (3 pigs lost included) and 46.4% in the TrpChs ⁺ group (1 pig lost included). During the first 4 d after challenge, the challenge reduced ADG (P < 0.05), and this reduction was greater in susceptible pigs (P < 0.05) than nonsusceptible ones. Tryptophan increased ADG and feed intake in susceptible pigs (P < 0.05) from challenge to d 4, but not thereafter. Tryptophan supplementation did not improve the fecal consistency and did not reduce the number of pigs positive for ETEC in feces on d 4 after the challenge. The K88-specific immunoglobulin A activity in blood serum tended to be greater in challenged pigs (P = 0.102) and was not affected by the addition of Trp. Villous height was affected by the addition of Trp and challenge in different ways, depending on the site of small intestine. The need to consider the phenotype for the adhesion of the ETEC in studies with different supply of Trp was clearly evident. When compared with practical weaning standard diets, Trp supplementation allowed susceptible pigs to partially compensate for the effects of ETEC challenge by increasing feed intake and maintaining an adequate BW growth. This is of practical importance for the formulation of diets for pigs selected for lean growth because of the presence of an association between this trait and the susceptibility to the intestinal adhesion of ETEC.

Key Words: diet • enterotoxigenic Escherichia coli K88 • pig • tryptophan • weaning

	INTRODUCTION

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Weaning per se is a stressful condition, and pigs reared in unsanitary conditions without dietary antibiotics show decreased growth rate and plasma Trp than those fed a medicated feed and housed in sanitary rooms (Le Floc’h et al., 2006). This may indicate that Trp requirement increases in subclinical infections. Plasma Trp concentration decreases during chronic lung inflammation of pigs, and it is associated with increased Trp catabolism, as indicated by the greater induction of indoleamine 2,3 dioxygenase activity (Melchior et al., 2005). Consequently, under poor sanitary conditions, plasma Trp concentration can be linked to its specific functions. Thus, competition could occur among the different Trp pathways, and consequently, it may have an impact on the Trp requirement.

Enterotoxigenic Escherichia coli K88 (ETEC) is the pathogen most frequently isolated in piglets and associated with colibacillosis. Oral challenge with ETEC has often been used in pig feeding trials to assess the ability of a diet to reduce the infection or its consequences (Bosi et al., 2004a,b). The susceptibility to colibacillosis depends on the presence of receptors for the fimbriae of ETEC in pig intestine. In ETEC-challenged pigs, the susceptibility could also indicate possible interactions between the diet and the phenotype. In fact, susceptible pigs in general show slower growth, greater specific immune response against the enteropathogen and greater fecal ETEC excretion, prolonged diarrhea, and often, shortened intestinal villi, as compared with nonsusceptible pigs (Bosi et al., 2004a,b; Geenen et al., 2007). The aim of the present study was to assess the effect of the Trp addition to a diet containing presumably adequate supply of Trp on growth performance and health of newly weaned pigs that differed in the phenotype for susceptibility to ETEC intestinal adhesion and are orally challenged with ETEC.

	MATERIALS AND METHODS

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The procedures complied with the Italian law pertaining to experimental animals and were approved by the Ethic-Scientific Committee for Experiments on Animals of the University of Bologna.

Diets and Treatments

A standard prestarter basal diet without antimicrobials, zinc oxide, or growth promotants was formulated without the addition of synthetic Trp (Table 1). The second diet was the basal plus 1 g of L-Trp/kg of feed. The analyzed AA are presented in Table 2. The following treatments were used: piglets that received the basal diet without challenge with ETEC (B), piglets that received the basal diet and challenged with ETEC (BCh), and piglets that received the basal plus Trp diet and challenged with ETEC (TrpCh).

Sixty-four crossbred piglets, weaned at 21 d of age and balanced for litter and BW were assigned to the treatments as follows: 8 piglets to the B; 28 piglets to the BCh; and 28 piglets to the TrpCh. The pigs were housed in weaning rooms with controlled temperature and ventilation. Continuous access to feed and water was allowed throughout the trial. Pigs were individually penned in cages, except the first 2 d when they were kept in groups of 4 to stimulate a quick resumption of feed intake after weaning.

The actual individual feed intake was calculated from the difference of the feed supplied and the residuals that were collected every day. For the first 2 d, when pigs were in group and feed intake was very low, the average value of the pen was added to individual intake for the remainder of the trial.

Experimental Procedure

The trial was conducted in 2 batches (32 pigs per batch). All the pigs were fed diets with colistin (250 mg/kg) for 4 d (d 0 to 3 of the morning) to ensure similar health conditions in the gut. On d 5, each pig from groups BCh and TrpCh was orally dosed with 1.5 mL suspension containing 10¹⁰ cfu of E. coli K88ac O149/mL. The bacteria solution (Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia, Reggio Emilia, Italy) was prepared as described by Bosi et al. (2004a). Pigs in treatment B received a placebo solution. Severity of diarrhea was characterized by using the fecal consistency score system (1 to 5): 1 = hard feces, and 5 = watery feces.

Thirty-two of the 64 pigs were killed on d 9 (that is, 4 d after challenge) and the remaining 32 pigs were killed on d 23 (i.e., 18 d after challenge). The animals were deeply anaesthetized with sodium thiopenthal (10 mg/kg of BW) and killed by an intracardiac injection of a commercial solution (0.5 mL/kg of BW) with 3 components (embutramide, mebenzonium iodide, and tetracaine hydrochloride; Tanax; Intervet Italia, Peschiera Borromeo, Italy).

Experimental Observations and Measurements

Pigs were weighed individually at the start of the trial and on d 5, 9 (first slaughter), and 23 (second slaughter). Individual feed intake of each pig was recorded. Blood and fecal samples were obtained immediately before the challenge and at the first and second slaughter days. Blood samples were collected by venipuncture of a vena cava, centrifuged at 3,000 x g for 10 min, and then serum removed. Serum was incubated at 56°C for 30 min and stored at –20°C until analysis. The ETEC-specific immunoglobulin A (IgA) titers in serum were determined by ELISA according to Van den Broeck et al. (1999), using K88 fimbriae isolated from ETEC cultures as reported by Bosi et al. (2004a).

At slaughter, stomach and small intestine were removed and weighed full and empty. Segments of the jejunum, at 25 and 75% of the small intestine length (defined as proximal and distal, respectively), were stored for histological measurements (villous height and crypt depth) and phenotyping for adhesion of ETEC to the villi (on scrapings of distal jejunum). Samples of ileal content were collected for the determination of total E. coli and ETEC plate counts as previously reported (Bosi et al., 2004a, b). For ETEC, fecal or ileal samples in Ringer’s solution were serially diluted and grown on a violet red bile agar medium (containing 0.1 g/L of 4-methyl-umbelliferyl-β-glucoronide). A slide agglutination test with rabbit immune sera against ETEC was used to assess the presence of the K88 antigen.

In Vitro Villus Adhesion Assay

The phenotype for susceptibility to ETEC adhesion was assessed with the procedure of Van den Broeck et al. (1999). Briefly, the villi are examined by phase-contrast microscopy after incubation with ETEC. The number of bacteria adhering along a 50-µm length of villous brush border is counted in 20 fields, and pigs are considered positive (s⁺) when showing values 6, and others were considered negative (s^–).

Histological Analysis

To optimize the distension of the intestinal wall, samples were pinned to balsa wood and immersed in 100 mL/L of buffered formalin (pH 7.4). Formalin-fixed and paraffin wax-embedded samples were prepared as reported by Bosi et al. (2007). Four-micron-thick sections were deparaffinized in xylene and stained with hematoxylineosin. For each sample, the height of 10 villi and the depth of 10 crypts were measured; only villi and crypts perpendicular to the mucosa surface were considered suitable for morphometry. The sections were examined at low magnification with a conventional microscope interfaced with a digital camera and a personal computer equipped with Cytometric software (Byk Gulden, Milan, Italy). The dimensions of the digitized images were 513 x 463 pixels.

Villus height was measured as the distance from the crypt opening to the top of the villus, whereas crypt depth was measured from the base of the crypt to the level of the crypt opening. To estimate the mucosal surface area, the mucosal-to-serosal amplification ratio M was calculated as indicated by Kisielinski et al. (2002). The number is based on mean values of villus surface (calculated using length and width of the villus), mucosal unit bottom (determined by villus and crypt width), and villus bottom (determined by villus width): M = (villus surface + unit bottom – villus bottom)/unit bottom, where villus surface = · (villus length · villus width), unit bottom = · (villus width/2 + crypt width/2)², and villus bottom = · (villus width/2)².

Statistical Analysis

All the individual data were analyzed by ANOVA using the GLM procedure (SAS Inst. Inc., Cary, NC). For the growth performance data, the initial model included the treatment (B, BCh, and TrpCh), the time after challenge (d 4 and 18), batch, litter within batch, and treatment x time after challenge, treatment x batch, and time after challenge x batch interactions. The initial analysis of the data indicated that the 2-factor interactions with batch were not an important source of variation; thus, they were removed from the final model. Orthogonal contrasts were used to assess the effect of treatments.

Furthermore, on the basis of previous results using the same pig lines (Bosi et al., 2007), a similar frequency of susceptibility of the pig to ETEC infection was expected. Therefore, it was planned to split the pigs of each of the 2 challenged groups into 2 different subgroups: positive or negative for the sensitivity of intestinal villus to ETEC adhesion based on the results of the in vitro adhesion test as suggested by Geenen et al. (2007). This was not done for the control pigs because the susceptibility to ETEC was presumed to be irrelevant for pigs treated with colistin and not challenged with ETEC. Consequently, the data obtained after the challenge were analyzed with the model that included the treatment [B, BChs^– (nonsusceptible), BChs⁺ (susceptible), TrpChs^– (nonsusceptible), and TrpChs⁺ (susceptible)], batch, and litter within batch. For the data obtained at 2 different slaughter days, the time after challenge (4 vs. 18 d) and its interaction with treatment and susceptibility to ETEC were added to the model. For the comparisons among the treatment and susceptibility, the following contrasts were used: B vs. BCh and TrpCh, BChs^– and TrpChs^– vs. BChs⁺ and TrpChs⁺, BChs^– vs. TrpChs^–, and BChs⁺ vs. TrpChs⁺. Chi-square analysis was used to assess the difference in the proportion of pigs with feces positive for ETEC within susceptible and nonsusceptible pigs.

	RESULTS

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ETEC Susceptibility

In Table 3, the numbers of pigs positive or negative for ETEC intestinal adhesion and pigs lost in each experimental group are presented. Four pigs died of causes related to colibacillosis, which was confirmed by the presence of ETEC. All the pigs were from challenged groups (3 from BChs⁺ and 1 from TrpChs⁺). Because these pigs could not be phenotyped for ETEC adhesion, their data were excluded from all the statistical analyses. The frequency of pigs susceptible or unsusceptible to ETEC was very similar, especially if pigs that died of colibacillosis are included. The frequency was also similar among the 3 treatment groups. Within pigs challenged and susceptible, the percentage of pigs lost was 21% (3/14) and 8% (1/13) for BCh and TrpCh, respectively.

The growth performance data before and after challenge are presented in Table 4. The interaction between the treatment and time after challenge was not statistically significant, and consequently, the values for treatments are the means of the 2 time periods. Before the challenge (d 0 to 5), the feed intake and the ADG were decreased and not affected by the treatment. In the period after the challenge, pigs that were not challenged tended to have a greater ADG (P = 0.070), whereas the supplementation with Trp improved growth in challenged pigs (P < 0.05). In this period, feed intake was not affected by the challenge, but in the stimulated pigs, a trend to increase daily feed consumption was observed with the Trp diet (P = 0.089). A trend for the effect of the Trp addition on ADG was also observed during the whole period (P = 0.061).

Average fecal scores during the first 4 d after challenge (Table 6) did not vary between untreated and challenged pigs, but within challenged pigs, susceptible pigs tended to have greater or worse scores (P = 0.093) than nonsusceptible pigs. The Trp addition did not affect fecal scores.

Figure 1 presents the effect of diet, challenge, susceptibility to ETEC, and time after challenge on Escherichia coli ileal counts. There was a trend for an interaction between the treatment and the time after challenge (P = 0.085). On d 4 postchallenge, susceptible pigs had greater Escherichia coli numbers than nonsusceptible pigs (P < 0.01). Within positive pigs, supplemental Trp tended to reduce the Escherichia coli count (P = 0.080). On d 18 after challenge, no effect was observed. On d 4 after challenge, 7 and 8 pigs respectively from BChs+ and TrpChs+ groups were also positive for ETEC in the ileum (data not shown). Pigs at d 18 after challenge were all negative for the presence of ETEC in ileum.

View larger version (13K): [in this window] [in a new window]   Figure 1. Effect of treatments in the different phenotypes for Escherichia coli K88 (ETEC) intestinal adhesion and of time after oral challenge with ETEC on E. coli ileal counts (bar = least-squares mean ± SEM). B = basal diet; BCh = basal diet with challenge; TrpCh = Trp diet with challenge; s+ = susceptible to the intestinal ETEC adhesion; and s– = nonsusceptible to the intestinal ETEC adhesion. Treatment x time after challenge, P = 0.085. At 4 d: s– vs. s+, P < 0.01; BChs+ vs. TrpChs+, P = 0.080.

View larger version (20K): [in this window] [in a new window]   Figure 2. Effect of different times (A), and of treatments in the different phenotypes for Escherichia coli K88 (ETEC) intestinal adhesion (B) on K88-specific immunoglobulin A (IgA) activity (ln arbitrary units/mL) in blood serum collected before the oral challenge with ETEC and at the end (bar = least-squares mean ± SEM). B = basal diet; BCh = basal diet with challenge; TrpCh = Trp diet with challenge; s+ = susceptible to the intestinal ETEC adhesion; and s– = nonsusceptible to the intestinal ETEC adhesion. Data of the 2 times after challenge are pooled. At end: between different times after challenge, P < 0.01. Before challenge: BChs– vs. TrpChs–, P = 0.057. At end: B vs. (BCh + TrpCh), P = 0.102. For the value obtained at the end of the experiment, the value before challenge was used as a covariate (P = 0.135).

The effect of treatments in the different phenotypes for ETEC intestinal adhesion on gut weights and lengths, expressed per 100 g of BW, are presented in Table 7. No statistically significant interaction of the treatment and the time after challenge was observed. As compared with the control, the challenge did not affect any response criteria. However, in pigs susceptible to ETEC intestinal adhesion, the proportion of the weight of gastric content was reduced by 40.0% (P < 0.01), whereas the proportion of colon tissue increased by 9% (P < 0.01) compared with the nonsusceptible pigs. Within the nonsusceptible pigs, the addition of Trp caused only a trend to increase the proportion of colon tissue (P = 0.093). However, Trp addition to the diet fed to pigs susceptible to ETEC reduced (P < 0.01) the proportion of small intestine and colon lengths to BW by 20.4 and 21.2%, respectively, when compared with pigs fed unsupplemented diet. A trend to increase the relative weight of small intestine was also observed (P = 0.102) with the addition of Trp, whereas the density of the intestine (g/cm) also increased (P = 0.01; data not shown).

	DISCUSSION

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

In general, after oral challenge with ETEC in the early weaning period, susceptible pigs may show reduced growth, as compared with nonsusceptible pigs (Bosi et al., 2004b). This was confirmed by the data on d 4 after challenge in the present trial. However, pigs with high dietary ratio of Trp to Lys were stimulated to increase their feed intake and were able to partially maintain their growth. In nonsusceptible pigs, Trp addition did not stimulate feed intake and growth compared with the basal diet.

The importance of Trp to control feed intake in pig is well known (Sève et al., 1991). Tryptophan can maintain adequate brain 5-hydroxytryptamine concentrations. Our results indicated that Trp concentration above the standard requirement is necessary to maintain feed intake in piglets that are prone to an intestinal infection, such as nonsusceptible pigs affected by ETEC in the present study.

In this trial, we did not measure blood concentrations of Trp; however, it is possible that the ETEC infection induced a decrease of this response criterion as observed in pigs stimulated by the injection of killed Mycobacterium tuberculosis cells (Melchior et al., 2004). The proinflammatory cytokine interferon-gamma in various cells induces the enzyme indoleamine (2,3)-dioxygenase, which converts Trp to kynurenine (Byrne et al., 1986). An increased catabolism of this AA could have occurred in susceptible pigs and could have produced a greater local induction of indoleamine (2,3)-dioxygenase activity, as described for chronic lung inflammation (Melchior et al., 2005).

The addition of Trp and subsequent increase in feed intake could have partially compensated the increased Trp loss and could have made more Trp available for growth. The effect of Trp on appetite regulation could be mediated through the regulation of the central production of serotonin. Tryptophan is a precursor of serotonine and a decrease in brain Trp leads to a decrease in the production of serotonin (Henry et al., 1996; Sève, 1999; Patuszewska et al., 2007). In healthy weaned pigs, a restriction of dietary concentration of Trp has been shown to induce a reduction of the blood orexigenic hormone ghrelin (Zhang et al., 2007). The mechanism has not been established; however, in our experiment, the supplementation with Trp could have restored ghrelin concentation in susceptible pigs, thus stimulating feed intake.

Feed intake and growth were only marginally affected by the challenge after 4 d in susceptible pigs that were reared until d 23. It is possible that during this period the effect of inflammation ended after the challenge and there was no need to compensate Trp loss. Health measurements (fecal score and ETEC content in feces) were moderately affected by the susceptibility to ETEC. The high-Trp diet reduced only the increase in total E. coli count in ileal contents of susceptible pigs at 4 d after challenge. However, the mortality rate associated with colibacillosis was less in Trp-supplemented pigs. Pigs were selected from a standard piggery, and it is not surprising that they were already marginally positive for the IgA activity specific for K88 in blood serum collected before the challenge. Pigs responded to the challenge with a rapid increase of the activity that was more pronounced after 18 d. The response was also observed in negative pigs, which is in agreement with Bosi et al. (2004b) but not with Van den Broeck et al. (1999). A similar increase in anti-K88 IgA activity in nonchallenged pigs, even though less than that of challenged subjects, can be explained by some residual expansion of the plasma cells of pigs already primed before the start of the trial or by some occasional contact with ETEC during the experiment.

At slaughter, a decrease in gastric contents was observed in pigs positive to ETEC intestinal adhesion, and no effect of dietary Trp addition was observed. This was observed at both time periods after the challenge and can be related to an increased gastric emptying rate. During intestinal inflammation, neurons of intrinsic and extrinsic innervation of the whole gut are involved (Collins, 1996). The very high ratio of intestinal length to BW at slaughter in susceptible pigs challenged and fed the basal diet may reflect pig immaturity. On the contrary, the increased intestinal density (g/cm), which was associated with Trp addition to susceptible pigs, might indicate an increase in thickness of the intestinal wall. However, this was not confirmed by the histological measurements. To discuss the morphological characteristics of the small intestinal mucosa in the postweaning phase, the exact sampling location in the tract should be considered. In fact, during the immediate postweaning period, more changes of small intestinal mucosa in the upper tract are observed than in the lower tract, and those changes presumably depend on the shortage of AA available from the gut lumen (Montagne et al., 2007). Consequently, the increased availability of Trp in nonsusceptible pigs fed the high Trp diet could have allowed the increase in villous height at the proximal small intestine. Conversely, at the distal small intestine, where the adhesion of ETEC was maximal, the mucosa of susceptible pigs responded to Trp immediately after the challenged inflammation, showing a compensatory increase in villous height as observed in some other challenge trials (Bosi et al., 2004b). In this instance, most of the response in susceptible pigs was due to the increase of villi in the high-Trp group, even though a statistically significant difference between the 2 diets was not reached.

The trial indicated that the phenotype for the adhesion of the ETEC should be considered when the effects of dietary Trp are studied in weaning pigs. This is of practical relevance because of the variable frequency of the gene in pigs. Furthermore, it can be relevant for improved genotypes because of the association of susceptibility to ETEC with greater lean growth (Edfors-Lilja et al., 1986). The supplementation of Trp to a basal diet allows susceptible pigs to partially compensate for the effects of challenge with ETEC by increasing feed intake and maintaining an adequate body growth.

	Footnotes

 
¹ This work was supported in part by Ajinomoto Eurolysine S.A.S.

² Corresponding author: paolo.bosi{at}unibo.it

Received for publication November 15, 2007. Accepted for publication August 7, 2008.

	LITERATURE CITED

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 


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