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Poult Sci 2007. 86:488-495
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METABOLISM AND NUTRITION

Supplementation of Glutamine and Vitamin E on the Morphometry of the Intestinal Mucosa in Broiler Chickens

A. E. Murakami*,1, M. I. Sakamoto*, M. R. M. Natali{dagger}, L. M. G. Souza* and J. R. G. Franco*

* Department of Animal Science, and {dagger} Department of Morphophysiological Sciences, State University of Maringá, 87020-900 Paraná, Brazil

1 Corresponding author: aemurakami{at}uem.br or mizumiss{at}yahoo.com.br


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The objective of this experiment was to evaluate the influence of Gln and vitamin E (VE) supplementation in the diet of broiler chickens (Cobb-Vantress) on the morphometry of the intestinal mucosa. The design was completely randomized in a 2 x 3 (VE x periods of administering Gln) factorial arrangement. The levels of VE used were 10 and 500 mg/kg of diet and 3 periods of administering (1%) Gln-supplemented starter diet (for the first 7 or 14 d of life or for no added Gln), totaling 6 treatments with 5 replicates of 50 birds per experimental unit. In the growth period (d 22 to 41 posthatch), the treatments consisted only in the respective levels of VE. On d 7, 14, 21, and 41 posthatch, 2 birds per replicate were killed, and samples of the duodenum, jejunum, and ileum were subsequently removed, fixed in Bouin solution, and later embedded in paraffin and stained with hematoxylin-eosin. The parameters analyzed were villus height and crypt depth. An ANOVA was applied to the obtained data, and the means were compared using Tukey’s test (5% significance level). Greater development was observed in the duodenum, followed by the jejunum and ileum. On 41 d of life, diets with 10 mg of VE/kg supplemented with Gln (for the first 7 d of life) provided better development of the intestinal mucosa in broiler chickens.

Key Words: broiler chicken • crypt depth • small intestine • villus height


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The egg supplies nutrients during embryonic development. After hatching, the birds start to have exogenous diets. This change necessitates an adaptation period for the gastrointestinal tract (GIT) of the birds, because the GIT undergoes a posthatch maturation process that can significantly affect performance, mainly in the first 2 wk posthatch, which represents approximately 30% of the useful life of the bird.

The GIT of the birds possesses the functions of food content storage, secretion digestion, and absorption of nutrients. Morphological studies point out that at the moment of hatching, the weight of the small intestine represents 1.2 to 2.6% of the BW of the bird and 6.2 to 6.6% at maximum development. The development peak of the small intestine is shown to be between d 5 and 7 posthatch (Sell, 1996). However, Noy and Sklan (1998) reported d 6 to 8 posthatch as the growth peak for the small intestine, which strengthens the premise that adequate feeding in the first week posthatch of the chick has a relevant role in broiler chicken performance.

The immaturity of the GIT in the first week posthatch is a limiting factor in the development of the bird, because the great capacity to secrete enzymes, the increase in the area of absorption through the longitudinal growth of the intestine, and the increase in the height of the villi are events yet to happen. Up to d 4 to 5 posthatch, the young chicken also receives nutrients from the yolk sac, in the peritoneal cavity (Macari, 1998).

Nir (1998) observed that broiler chicks present a negative correlation between food ingestion and nutrient digestibility during wk 1 posthatch. This author stated that this correlation becomes positive in wk 2 posthatch and may be related to the optimization of intestinal growth and enzyme activity. Starting from wk 3 posthatch, the relationship between feed intake and digestibility ends, probably because the GIT has reached its maximum digestive development.

The small intestine (duodenum, jejunum, and ileum) has a primordial function in the processes of digestion and nutrient absorption. The structure and the function of the intestinal mucosa, which has the highest turnover rate of all the tissues of the body, depend on the balance among proliferation, cell migration, and apoptosis. According to Macari (1998), total turnover of the mucosa takes about 90 to 96 h in broiler chickens; however, turnover time differs among the segments. In the duodenum, turnover is faster (about 48 h).

According to Uni et al. (1998) and Applegate et al. (1999), mucosa development consists in the increase in the height and density of the villi, which corresponds to an increase in the number of their epithelial cells.

Research has suggested that the stimulation of the GIT by different substrates, soon after hatching, can accelerate its development. According to Noy and Sklan (1995), the digestion of N in the small intestine of broiler chickens increases from 78% on d 4 posthatch to 92% on d 21 posthatch.

Some nutrients are essential for intestinal homeostasis. According to Ruemmele et al. (1999), the lack of Gln and polyamines inhibit proliferation, migration, and apoptosis. In addition, Gln is an essential substrate in the construction of the passive barrier of mucin to bacteria because it is necessary for the synthesis of N bases and amino sugars of the extracellular matrix, N-acetylglucosamine and N-acetylgalactosamine, and for the glycosylation of mucins (Reeds and Burrin, 2001).

Glutamine is a neutral free amino acid that is found in large quantity in muscle tissue and plasma, in concentrations that represent approximately 50 to 80% of the free amino acid total in the body. Because it has 2 mobilizable N groups in its structure, Gln can function as a vehicle for the tissue exchange of N and perform a crucial role in several important metabolic pathways (Marliss et al., 1971; Smith, 1990). It is responsible for mucosa structure maintenance, which is mucin synthesis and the maintenance of a barrier against bacteria attacks (Khan et al., 1999), in addition to promoting the maturity and integrity of the intestinal flora associated with the immune system (Yi et al., 2005).

The effect of Gln on the reconstitution of the intestinal mucosa, after some damage, has been investigated because this amino acid is the main metabolite that nourishes the enterocytes. Glutamine is recognized as a vital energy substrate in cells that divide rapidly (e.g., intestinal; Lacey and Wilmore, 1990; Newsholme, 2001).

Recent studies have demonstrated that the cells of the intestinal mucosa of the crypts and villi synthesize Gln, suggesting that it may not have a strictly metabolic role in the intestine (Reeds and Burrin, 2001). This indicates that Gln has a more regulatory than metabolic role in the activation of a series of genes associated with the cycle of progression of the cells and that the inhibition of Gln synthesis inhibits both the proliferation and the differentiation of the cells of the mucosa (Rhoads et al., 1997; Blikslager et al., 1999; Reeds and Burrin, 2001).

The natural exposure of chickens to endemic pathogens in the production environment (due to intensive rearing) challenges the immune system and stimulates the production of cytokines by macrophages, which act on the central nervous system, causing anorexia, lethargy, and neuroendocrine alterations (Klasing, 1988). Phagocytes can also liberate free radicals, with the objective of eliminating the invading infectious agent. However, these free radicals react aggressively in the living tissue of the animal itself, causing damage like lipid peroxidation and alteration in cell membrane permeability.

The ingestion of high doses of antioxidant nutrients, for example vitamin E (VE), is considered a preventative measure against cell damage caused by immunological cells (Barbi et al., 1999). Vitamin E acts as a biological antioxidant at the cell membrane level, and Gln can act in the elimination of free radicals by being a precursor of glutathione synthesis (Wu, 1998). The good performance of the animal is due to better use of the nutrients supplied in the diets.

From the point of view of chicken production, the maintenance of the development and health of agents in the GIT is fundamental. The GIT is the entry point of nutrients that can better the performance of the bird. Considering that feed represents 70 to 80% of the production cost and that the integrity of the epithelial cells of the mucosa insure good performance and production, this experiment was carried out with the objective of evaluating the influence of nutrition (supplementation of Gln and VE) on the morphometry of the intestinal mucosa in broiler chickens.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Birds and Installations
The experiment was conducted in the poultry sector of the Iguatemi Experimental Farm and in the Laboratory of Animal Histology of the Department of Morphophysiological Sciences with the approval of the Animal Experimentation Ethics Committee of the State University of Maringá.

A total of 1,500 male Cobb-Vantress broiler chicks (d 1 posthatch) were housed in a conventional shed with French roof, a concrete floor, and lateral walls of wood (height: 40 cm) and wire mesh (up to the roof) with mobile curtains. The mean temperatures inside the shed were 30°C (maximum) and 22°C (minimum). Mean RH was 30%. The percentage of mortality recorded during the entire experimental period was 1.50%.

The experimental design was completely randomized in a 2 x 3 (VE x periods of administering Gln) factorial arrangement, whose levels of VE used were 10 and 500 mg/kg of diet, and 3 periods of administering (1%) a Gln-supplemented starter diet (for the first 7 or 14 d of life or for no added Gln), totaling 6 treatments and 5 replicates of 50 birds per experimental unit. In the growth period (d 22 to 41 posthatch), the treatments consisted only in the respective levels of VE. The vitamin-mineral premix used in the diet was free of VE. The diets were formulated based on corn and soybean meal (Tables 1Go and 2Go), which meets the nutritional requirements of the birds according to Rostagno et al. (2000).


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  		Table 1. Percentage composition of diets for broiler chickens in the starter phase (d 1 to 21 posthatch)
 

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  		Table 2. Percentage composition of diets for broiler chickens in the growth phase (d 22 to 41 posthatch)
 
Intestinal Morphometry
On d 7, 14, 21, and 41 posthatch, 2 birds per replicate (removed at random) were electrically stunned and then killed by exsanguination. Fragments of approximately 5 cm in length were obtained from each of the 3 regions of the small intestine: duodenum, from the pylorus to the distal portion of the duodenal loop; jejunum, from the distal portion of the duodenal loop to Meckel’s diverticulum; and ileum, anterior portion of the ileocecal junction. Segments were then placed on polystyrene sheets, opened longitudinally, washed in saline solution, fixed in Bouin’s solution for 24 h, and processed until paraffin embedding, according to what has been described by Beçak and Paulete (1976). Each fragment was submitted to semiseriate cuts (5 µm thick) and stained using the hematoxylin-eosin method.

In the morphometric study, images were captured using a light microscope and a system that analyzes computerized images (Image Pro-Plus, Version 5.2, Média Cibernética, São Paulo, Brazil). The height of 30 villi and the depth of 30 crypts were measured from each replicate per segment. The mean was obtained from these values.

Statistical Analysis
The obtained data were submitted to ANOVA using the GLM program of SAS Institute (2000). Contrasts between treatments means were evaluated by Tukey’s test at a significance level of 5%.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The intestinal development of the broiler chickens fed a standard diet (Gln-free and supplemented with 10 mg of VE/kg of diet), independent of age, revealed that the intestinal mucosa of the duodenum presented the greatest development (villus height and crypt depth), followed by the jejunum and the ileum. These results indicate that the development of the duodenum is complete at d 21 posthatch, whereas gradual growth of the villi was observed in the jejunum and the ileum (Table 3Go and Figure 1Go) until the end of the experimental period (d 41 posthatch).


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  		Table 3. Regional development of the small intestine of broiler chickens at different ages
 

Figure 1
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  		Figure 1. Photomicrography of segments of the small intestine of broiler chickens on d 21 posthatch fed 10 mg of vitamin E/kg, without and with Gln (1%). Panels A, B, and C represent duodenum, jejunum, and ileum, respectively, without Gln. Panels D, E, and F represent the same segments with Gln. Hematoxylin-eosin staining. Bar = 200 µm.

 
In relation to the treatments, the morphometric parameters are presented in Tables 4Go and 5Go. The duodenum presented deeper crypts at d 7 posthatch in the interaction (P = 0.038) 10 mg of VE/kg x without Gln. On d 14 posthatch, in respect of villus height and the villus:crypt, there was an interaction (P = 0.041 and P = 0.002, respectively) in the birds treated with 500 mg of VE/kg x Gln (d 1 to 14 posthatch) that presented mean values of 1,394 µm and 9.2, respectively. After d 21 posthatch, only a maintenance in relation to duodenal villus height was observed; however, there was a VE effect (P = 0.022) regarding crypt depth, in which deeper crypts were observed at 10 mg/kg. Nevertheless, this effect cannot be observed by d 41 posthatch due to complete development.


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  		Table 4. Means1 of villus height (µm), crypt depth (µm), and villus:crypt of segments of the small intestine of broiler chickens on d 7 and 14 posthatch fed diets containing Gln and Vitamin E (VE)
 

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  		Table 5. Means1 of villus height (µm), crypt depth (µm), and villus:crypt of segments of the small intestine of broiler chickens on d 21 and 41 posthatch fed diets containing Gln and Vitamin E (VE)
 
In the mucosa of the jejunum, the crypt depth presented an effect (P = 0.017) at 10 mg of VE/kg on d 7 posthatch. However, on d 14 posthatch, there was the interaction (P = 0.030) 10 mg of VE/kg x Gln (d 1 to 7 posthatch) as regards the crypts. In this same period, a greater villus:crypt was obtained for the birds fed 500 mg of VE/ kg x Gln (d 1 to 7 posthatch), but on d 21 posthatch, only 500 mg of VE/kg presented an effect (P = 0.011) on the villus:crypt. On d 41 posthatch, the villi were higher in the interaction (P = 0.001) 500 mg of VE/kg x without Gln. The mean height was 1,364 µm, which, in turn, did not differ from the birds fed 10 mg/kg with the supplementation of Gln, independent of the period of use (1 or 2 wk).

In relation to the ileum, on d 7 posthatch, in respect to the villus:crypt, there was the interaction (P = 0.015) 10 mg of VE/kg x Gln (d 1 to 7 posthatch). On d 21 posthatch, regarding villus height and the villus:crypt, there was an effect (P = 0.021 and P = 0.001, respectively) at 10 mg of VE/kg, presenting higher mean results. There was the interaction (P = 0.012) 10 mg of VE/kg x Gln (d 1 to 7 posthatch) as regards villus height on d 41 posthatch, presenting a mean height of 921.0 µm.

Although villus height is correlated positively with BW gain and feed intake (Kelly et al., 1991), the same cannot be observed in this experiment because the performance parameters BW gain (g), feed intake (g/bird), and feed:gain (g/g) did not present significant effect in relation to the treatments, whose means are presented in Table 6Go.


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  		Table 6. Means values of performance parameters (BW gain, feed intake, and feed:gain) of broiler chickens at different ages
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
As regards the intestinal development of broiler chickens, independent of treatments, Uni (1999) and Kondo (2003) also observed greater development of the duodenum in relation to other intestinal segments, corroborating the results found in this experiment, which is represented in Figure 1Go. According to Macari (1998), this greater development can be attributed to the fact that it is the segment with the fastest cell renewal and is also the first segment of the small intestine to receive physical, chemical, and hormonal stimuli provoked by the presence of the diet in the lumen.

According to Uni (1999), the complete development of the duodenal villi occurred by d 7 posthatch; however, the villi of the jejunum and the ileum needed until d 14 posthatch. On the other hand, Kondo (2003), in a comparative study between different lineages of broiler chickens, observed gradual development in the different intestinal regions of the chickens until d 36 posthatch.

In relation to the results obtained in this experiment regarding the performance parameters due to the treatments with Gln and VE supplementation, they corroborate Maiorka et al. (2000), who observed no effect of supplementing 1% Gln on the feed intake, BW gain, or feed:gain in any of the development phases in broiler chickens. However, as regards intestinal morphometry, Gln presented an effect on villus height, crypt depth, and the villus:crypt in the duodenum and on villus height in the ileum on d 7 posthatch. These same authors carried out the morphometry of the mucosa on d 14 posthatch and did not find any difference between the treatments. They concluded that Gln contributed to the development of the intestinal mucosa in the first days of life as an energy source for the maturation of the mucosa cells of the chickens.

On the other hand, Yi et al. (2001), evaluating the effect of Gln on the performance and morphometry of the mucosa of the duodenum and the jejunum in broiler chickens until d 21 posthatch, observed that the supply of a diet with Gln (1%) caused a decrease in crypt depth in the duodenum and the jejunum on d 3 posthatch. No difference was observed as regards the villus:crypt in the segments on d 3, 7, or 14 posthatch.

In a recent work, Yi et al. (2005), evaluating the influence of Gln (1%) on groups of chickens fed or fasted soon after being housed, observed that birds fed diets supplemented with Gln immediately after being housed presented better BW, BW gain, and feed:gain during the first 2 wk posthatch compared with the other treatments. As regards intestinal morphometry, they also had greater crypt depth on d 2 posthatch and greater villus height on d 7 posthatch compared with the group that fasted for 48 h + Gln. Thus, a beneficial effect from Gln may be observed in intestinal performance and development in high stress situations or in challenges to the immune system.

Vitamin E may have acted in the protection of cells at the membrane level because the action of tocopheryl acetate is supplemented by the presence of glutathione in the soluble component of the cell, catabolizing the conversion of organic peroxides and H+ peroxides in alcohols or water and avoiding cell lesion (Ewan, 1993).

According to the results obtained in this experiment, small doses of this vitamin were shown to be sufficient in the protection of the cells. Although of performance parameters did not present significant effects, VE, when interacting with Gln, presented better conditions to intestinal development. Deficiency or excess of VE decreases the activity of glutathione peroxidase, unbalancing the antioxidant action in the cells and enabling the increase in the formation of free radicals in the cytosol, thus damaging the immunomodulatory system of the birds (Leshchinsky and Klasing, 2001).

The results of this study indicate that diets with 10 mg of VE/kg of diet, supplemented with Gln (for the first 7 d of life) provided better development of the intestinal mucosa in broiler chickens on 41 d of life. This was proven by the behavior of the villi, which can be attributed to the trophic effect of these nutrients. Shorter villi hinder the absorption of nutrients by reducing the area of the intestinal epithelium cells, as a result of the decrease in the osmotic absorption of water.


   ACKNOWLEDGMENTS
 
We thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for financial support.

Received for publication February 9, 2006. Accepted for publication October 28, 2006.


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 ABSTRACT
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 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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