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Developmental Morphology of the Small Intestine of African Ostrich Chicks

College of Animal Science and Veterinary Medicine, Huazhong Agricultural University, Wuhan 430070, P. R. China

¹ Corresponding author: kmpeng{at}sohu.com

	ABSTRACT

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The objective of this study was to investigate the morphological development of the small intestine of African ostrich chicks and to examine the changes in the number of goblet cells therein by observing the gross anatomy and performing histochemistry and morphometry. The BW; length, height, and width of the villi; muscle thickness; depth of the crypts; and number of goblet cells in the intestinal villi and crypts were measured on neonatal d 1, 45, 90, and 334. Our results revealed that the weights of the duodenum, jejunum, and ileum (relative to the BW) peaked on d 90, 45, and 45, respectively, and tended to decline thereafter. The villus height and width and muscle thickness in the small intestine were positively correlated with the age of the birds. The ratio of the villus height to the crypt depth differed among the segments of the small intestine and at the different time points. The number of goblet cells in the intestinal villi and crypts increased rapidly up to postnatal d 45 and then decreased rapidly between d 45 and 90. The number of goblet cells in the villi was greatest in the jejunum on d 1 and in the ileum on d 45, whereas that in the crypt was greatest in the ileum on d 1 and 90 and in the duodenum on d 45. These results suggest that the small intestine develops gradually from postnatal d 1 to 90 and that the period up to postnatal d 45 is marked by significant developmental changes in the parameters reflective of the digestive capacity, such as the weight, length, and surface area of the intestine and the number of goblet cells. Therefore, in reared African ostrich chicks, feed management should be enhanced between postnatal d 1 and 45.

Key Words: goblet cell • small intestine • African ostrich chick • postnatal development

	INTRODUCTION

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Nutrient absorption is important at all stages of life. The small intestine, especially the crypts and villi of the absorptive epithelium, play significant roles in the final stages of nutrient digestion and assimilation. Studies on the small intestine have revealed that the size of the small intestine and its digestive activities are altered during development in animals (King et al., 2000; Fan et al., 2002; Wang et al., 2003; Adeola and King, 2006; Olukosi et al., 2007a, b). Only a few studies performed thus far have investigated the small intestine of the ostrich. The histological features of the ostrich small intestine have recently been reported: the villi are described to be long and profusely branched, forming a labyrinthine structure (Bezuidenhout and Van Aswegen, 1990; Wang et al., 2007). Iji et al. (2003) reported the development of the digestive tract of African ostrich chicks as follows: the relative weight of the small intestine peaks at the age of 41 d and subsequently tends to decline, and the digestive enzymatic activity is altered during development.

In general, to understand or speculate on the capacity of the small intestines to absorb nutrients, it is important to examine the morphological changes occurring therein and the digestive enzymatic activity during development. However, as mentioned above, some studies have focused on changes in the size of the small intestine and the activity of digestive enzymes during development, but none have investigated the morphological changes occurring in the small intestine. Therefore, in this study, we examined the morphological changes occurring in the small intestine during the development of African ostrich chicks, to understand or speculate on the capacity of the small intestine to absorb nutrients.

	MATERIALS AND METHODS

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Birds and Experimental Design

African ostrich chicks (12 females and 12 males) were obtained from a standard ostrich farm in Guangdong, China, on postnatal d 1 (newly hatched chicks) and were transported within 10 h to a battery house, where feed and water were made available ad libitum. The 24 birds were divided into 4 groups (3 male and 3 female ostriches per group) on the basis of their BW and equalizing BW and the variance among groups. All the birds were maintained in a heated room with slatted plastic flooring and were fed a starter diet, which was formulated according to the specifications of the Elsenburg Ostrich Feed Databases (Brand, 2000), on postnatal d 1 to 334. Water and feed were provided ad libitum. All procedures were approved by the Animal Care and Welfare Committee of our institute.

Tissue Sampling

On postnatal d 1, 45, 90, and 334, the birds were weighed, deeply anesthetized with 10% urethane (Chaoyang Secondary School Chemical Plant, Shanghai, China) at a dose of 1 g/kg of BW, and perfused, initially with 1,000 mL of 0.85% normal saline (containing 0.075% sodium citrate) and thereafter with 1,500 mL of 4% paraformaldehyde PBS (0.1 mol/L, pH 7.4) at 4°C. The abdomen was cut open, and the entire small intestine, from the pylorus to the ileocecal sphincter, was removed. The small intestine comprises 3 segments. The first segment, termed the duodenum, extends from the pylorus to the pancreas and forms a loop surrounding most of the pancreas. The second segment is the jejunum that extends from the distal portion of the duodenal loop to Meckel’s diverticulum. The third segment is the ileum that extends from Meckel’s diverticulum to the ileocecal junction, with its distal portion connected to a pair of ceca via mesenteric tissue. The total weight, length, and diameter of the duodenum, jejunum, and ileum were determined in ostrich chicks of different ages. Furthermore, tissue samples (approximately 2 cm) were obtained from the midpoints of the 3 segments, gently flushed with 0.85% normal saline to remove the intestinal content, and postfixed for more than 24 h with the same fixative solution (4% paraformaldehyde PBS).

Morphological Examination

The intestinal tissue samples were dehydrated, cleared, and embedded in paraffin. Serial sections (5 µm) were cut on a Leica microtome (Nussloch GmbH, Nussloch, Germany), mounted on slides, and stained with hematoxylin and eosin and periodic acid-Schiff (PAS) stain. For all the assays, the sections were deparaffinized in xylene, rehydrated in a graded alcohol series, and examined under a light microscope.

Mucin Staining

Neutral mucin was detected by staining the sections with PAS reagent (McManus, 1948; American Forces Institute of Pathology, 1992). The slides holding the fixed tissue sections were deparaffinized, rehydrated, incubated with 5 g/L of periodic acid solution for 15 min, washed, and finally incubated with Schiff’s reagent (1 g of basic fuchsin, 200 mL of distilled water, 20 mL of 1 mol/L of HCl, 6 g of sodium pyrosulfite) for 30 min. The sections were then washed in distilled water, dehydrated, and mounted. The goblet cells present along the villi and crypt were counted and photographed under a Nikon microscope (Nikon Corp., Tokyo, Japan).

Measurements

For each intestinal tissue sample (9 samples obtained for each of the 3 intestinal segments per day of analysis), 3 cross-sections were prepared after the samples had been stained with hematoxylin and eosin and PAS stain. Further, for each intestinal cross-section, 10 intact, well-oriented crypt-villus units were selected for experiments conducted in triplicate (30 measurements for each sample, corresponding to a total of 270 measurements for each of the 3 intestinal segments per day of analysis). The villus height was measured from the tip of the villus to the villus-crypt junction. The villus width was defined as the distance from the outside epithelial edge to the outside of the opposite epithelial edge along a line passing through the vertical midpoint of the villus. The crypt depth was defined as the depth of the invagination between adjacent villi. The surface area of the villus was calculated on the basis of its height and width. The density of the goblet cells was calculated as the number of goblet cells per unit of the surface area (mm²). The muscle thickness was measured from the junction between the submucosal and muscular layers to that between the muscular layer and the tunica serosa. All the measurements were performed under an Olympus light microscope, using the HMIAS-2000 high-definition chromatic color medical science figure analysis program (Qianping, Wuhan, China).

Statistical Analyses

An ANOVA was performed using the GLM procedures of the SAS Institute (Cary, NC) to examine the differences between the samples examined at various time points. Contrasts between treatments means were evaluated by Duncan’s multiple range test at a significance level of 5%.

	RESULTS

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All results presented are those obtained for both the female and male chicks: no sex-specific effects were observed.

BW and Gross Anatomy of the Small Intestine

The chick BW and the weight and length of the small intestine (Table 1 and Table 2) increased from d 1 to 90 (P < 0.05). The increase in BW was greater (P < 0.05) from d 45 to 90 than from d 1 to 45 (Table 1). Further, the total intestinal weight increased more rapidly from d 45 to 90 than from d 1 to 45 (P < 0.05). The relative weight (intestinal weight:BW) of the duodenum increased from d 1 to 90 and peaked on d 90 (P < 0.05). The relative weights of the jejunum and ileum increased from d 1 to 45, peaked on d 45, and subsequently decreased slightly from d 45 to 90 (P < 0.05). The total intestinal length increased more rapidly from d 1 to 45 than from d 45 to 90 (Table 2).

The villus height (Table 3 and Figure 1A) in all the small intestinal segments increased with age (P < 0.05). The villus width (Table 4 and Figure 1B) increased from d 1 to 90 (P < 0.05) and was greater on d 90 than on d 334. The crypt depth (Table 4) in the duodenum and jejunum (Figure 1D) increased as the birds grew older (P < 0.05), whereas that in the ileum (Table 4 and Figure 1C) increased from d 1 to 45 but decreased thereafter up to d 90 (P < 0.05). The muscle thickness in each segment of the small intestine increased linearly with the age of the birds, from d 1 to 90 (Table 2 and Figure 1A). The ratio of the villus height to the crypt depth (V:C) in the jejunum decreased from d 1 to 90, whereas that in the duodenum and ileum decreased from d 1 to 45 and increased from d 45 to 90 (Table 3).

View larger version (157K): [in this window] [in a new window]   Figure 1. Representative photomicrograph showing the small intestine segments of African ostrich chicks on postnatal d 90 (stained with hematoxylin and eosin stain). Goblet cell production (arrows) could be observed at every segment. (A and B) Duodenum; (C) jejunum; (D) ileum. CY = crypt; SL = smooth muscle layer; VI = villi. (A, C, D) Bar = 100 µm; (B) bar = 10 µm. Magnification: (A) 4 x 10; (B) 40 x 10; (C and D) 10 x 10.

The number of goblet cells in the intestinal villi (Table 5) was greatest in the jejunum and lowest in the duodenum on postnatal d 1 (P < 0.05), greatest in the ileum and lowest in the duodenum on d 45 (P < 0.05), and no difference was found on d 90. The number of the goblet cells per unit area (Table 5) in the tissue samples harvested from the duodenum, jejunum, and ileum increased from d 1 to 45 (P < 0.05; Figure 2A and 2B) and decreased from d 45 to 90 (P < 0.05; Figure 2B and 2C). The goblet cell density in the duodenum increased rapidly from d 1 to 45, attaining a value of 50%. The number of goblet cells in the crypts of the small intestine (Table 5) was greatest in the ileum on postnatal d 1 (P < 0.05), greatest in the duodenum and lowest in the jejunum on d 45 (P < 0.05), and greatest in the ileum and lowest in the duodenum on d 90 (P < 0.05). In the jejunum and ileum, the number of the goblet cells per unit area (Table 5) increased as the chicks developed (P < 0.05), whereas in the duodenum, it increased from d 1 to 45 but decreased from d 45 to 90 (P < 0.05). The goblet cell density increased rapidly in the duodenum, attaining a value of 200%. The number of goblet cells was greater in the small intestinal villi on the same time than the crypts.

View larger version (138K): [in this window] [in a new window]   Figure 2. Representative photomicrograph showing the villi in the ileum of African ostrich chicks on postnatal d 1, 45, 90, and 334 (stained with periodic acid-Schiff stain). Goblet cell production (arrows) could be observed at every time point. Panels A, B, C, and D correspond to d 1, 45, 90, and 334, respectively. (A, B, C, D) Bar = 10 µm.

	DISCUSSION

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The intestinal weight is reported to increase in direct proportion to the BW in the case of ducks (King et al., 2000), pigs (Fan et al., 2002), broiler chickens (Wang et al., 2008), and rats (Pacha et al., 2003; Sabat and Veloso, 2003). Previous studies on avian species have demonstrated that intestinal growth is directly proportional to the age-related increase in the rate of metabolism (Soriano et al., 1993; Wang et al., 2008). Furthermore, some researchers have reported that the whole-body growth rates are partly determined by the tissue distribution in the gastrointestinal tract (Konarzewski et al., 1989; Obst and Diamond, 1992). In the present study, we demonstrated that the intestinal weight increases with the BW. The ostrich chick BW and the weight and length of the small intestine increased from d 1 to 90, and the whole-body growth rates also increased from d 1 to 90. The relative weight of the duodenum peaked on d 90, whereas that of the jejunum and ileum peaked on d 45. These results were consistent with those reported previously by Iji et al. (2003). In a previous study on chickens, the intestinal weight, surface area, and length relative to the BW were maximal during the first week of development and declined rapidly with age (Soriano et al., 1993). In pigs, development of the gastrointestinal tract commences early during fetal life and progresses rapidly after birth; the latter period is marked by significant events in the development of the gastrointestinal tract in providing the neonate with nutrients and protection by processes of digestion and absorption (Cranwell, 1995). These results reveal that the timing of gastrointestinal development differs among species.

Morphological Characteristics of the Small Intestine

Variations occurring in the villus height and width during the development of the small intestine have been studied in various animals. In the present study, the villus height and width in all segments of the small intestine increased with age, and these results were similar to those of previous studies (Fry et al., 1962; Holt et al., 1984; Miller et al., 2007; Wang et al., 2008). The villus widths increased from d 1 to 90, and the values on d 90 were greater (P < 0.05) than those on d 334. An increase in the villus width increases the surface area available for nutrient absorption. Many undifferentiated cells originate in the crypts of Lieberkuhn (Klein, 1989). Poole et al. (2003) reported that in lambs, the crypt depth increases linearly with age and is accompanied by an increase in the villus height and width, particularly in the jejunum, which contains the largest villi. These researchers considered that the crypt depth may be an important factor that determines the ability of the crypt to sustain the increase in the villus height and width as well as to maintain the villus structure. In the present study, the crypt depth in the duodenum and jejunum increased with age. On the other hand, that in the ileum increased from d 1 to 45 but decreased thereafter up to d 90. These results indicate that differential changes among the duodenum, jejunum, and ileum were evident in crypt depth. The crypt is the region where stem cells divide for renewal of the villus; thus, the presence of a large crypt is reflective of fast tissue turnover and a high demand for tissue synthesis (Xia et al., 2004). In the present study, the thickness in the muscle of each small intestinal segment increased with the age of the birds, from d 1 to 90.

The most interesting result obtained in our study was with regard to the differences in the V:C ratio: it decreased from d 1 to 90 in the jejunum, decreased from d 1 to 45, and increased from d 45 to 90 in the duodenum and ileum. Wang et al. (2008) reported that in broiler chickens, the V:C ratio in the duodenum is lower at the age of 42 d than at the age of 22 d (P < 0.001); however, age was not noted to affect the ratio in the jejunum and ileum. It is not a similar pattern with that of the broiler chickens. Wu et al. (2004) reported that an increase in the V:C ratio is associated with better nutrient absorption, decreased secretion in the gastrointestinal tract, improved disease resistance, and faster growth. A possible explanation for this is that the secretory functions differ in different segments of the intestine. Taken together, these results suggest that the nutrient absorption capacity of the intestine increases with age. It has been suggested that the intestine gradually develops from d 1 to 90 and is in a primitive state before d 45. Therefore, in reared fowl, feed management should be enhanced between postnatal d 1 and 45.

Morphological Changes in the Intestinal Goblet Cells

The intestinal goblet cells secrete high-molecular weight glycoproteins known as mucins (Specian and Oliver, 1991). The mucus layer in the small intestine plays an important role in protecting the epithelial cells of the small intestine and in nutrient transport between the lumen and the brush border membrane. In broiler chicks, the number of goblet cells increases with age, from postnatal d 0 to 7, in all regions of the small intestine (Uni et al., 2000, 2003; Geyra et al., 2001). In the present study, the number of goblet cells increased from d 1 to 45 in the villi and increased from d 1 to 90 in the crypts of the jejunum and the ileum. This finding is similar to those of previous studies (Uni et al., 2000, 2003; Geyra et al., 2001; Smirnov et al., 2006).

The number of goblet cells in the different segments of the small intestine differed at the same time points. On d 1, the number of goblet cells in the villi of the small intestine was greatest in the jejunum and lowest in the duodenum. On d 45, the number of goblet cells in the crypts of the small intestine was greatest in the duodenum and lowest in the jejunum. This pattern was not similar to that noted in previous studies on poultry, wherein the density of the goblet cells was found to increase distally along the duodenal-ileal axis (Uni et al., 2000, 2003; Geyra et al., 2001). Furthermore, from d 45 to 90, the number of goblet cells decreased in the villi of all segments of the small intestine and in the crypts of duodenum. This finding was different from those of previous studies (Uni et al., 2000, 2003; Deplanske and Gaskins, 2001; Geyra et al., 2001). In the case of the African ostrich chicks examined in our study, the number of goblet cells was greater on d 45 than on d 1 and 90. These results indicate that the goblet cell density in the small intestine during development in ostrich chicks is not similar to that in broiler chicks.

It has been suggested that sulfated acid mucins provide protection against bacterial translocation, because they are relatively resistant to degradation by bacterial glycosidases and host proteases (Fontaine et al., 1996; Robertson and Wright, 1997). Changes in the populations of acidic and sulfuric goblet cells may provide neonates protection against enteric infections (Brown et al., 2006). The results of the present study indicate that the number of goblet cells in the small intestine increases between d 1 and 45 in the life of an African ostrich. Thus, the protective functions of the small intestine increase gradually during this period, and feed management in reared fowl should accordingly be enhanced between d 0 and 45 to decrease the risk of enteric disease.

	ACKNOWLEDGMENTS

 
We would like to thank Liu Huazhen of the Department of Anatomy, Histology and Embryology, College of Animal Science and Veterinary Medicine, Huazhong Agricultural University, for her valuable comments on the experiments. This study was supported by the National Natural Science Foundation Project of China, No. 30471249 and No. 39970547.

Received for publication April 21, 2008. Accepted for publication August 7, 2008.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Adeola, O., and D. E. King. 2006. Developmental changes in morphometry of the small intestine and jejunal sucrase activity during the first nine weeks of postnatal growth in pigs. J. Anim. Sci. 84:112–118.[Abstract/Free Full Text]

American Forces Institute of Pathology. 1992. Laboratory Methods in Histotechnology. E. B. Prophet, B. Mills, J. B. Arrington, and L. H. Sobin, ed. American Registry of Pathology, Washington, DC.

Bezuidenhout, A. J., and G. Van Aswegen. 1990. A light microscopic and immunocytochemical study of the gastrointestinal tract of the ostrich (Struthio camelus L). Onderstepoort J. Vet. Res. 57:37–48.[Medline]

Brand, T. S. 2000. Elsenburg Ostrich Feed Databases. Elsenburg Agricultural Research Centre, Elsenburg, South Africa.

Brown, D. C., C. V. Maxwell, G. F. Erf, M. E. Davis, S. Singh, and Z. B. Johnson. 2006. The influence of different management systems and age on intestinal morphology, immune cell numbers and mucin production from goblet cells in post-weaning pigs. Vet. Immunol. Immunopathol. 111:187–198.[CrossRef][Medline]

Cranwell, P. D. 1995. Development of the neonatal gut and enzyme systems. Pages 99–154 in the Neonatal Pig: Development and Survival. M. A. Varley, ed. CAB International, Wallingford, UK.

Deplanske, B., and H. R. Gaskins. 2001. Microbial modulation of innate defense: Goblet cells and the intestinal mucus layer. Am. J. Clin. Nutr. 73:1131S–1141S.[Web of Science][Medline]

Fan, M. Z., O. Adeola, E. K. Asem, and D. King. 2002. Postnatal ontogeny of kinetics of porcine jejunal brush border membrane bound alkaline phosphatase, aminopeptidase N and sucrase activities. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 132:599–607.[Medline]

Fontaine, N., J. C. Meslin, C. Lory, and C. Andrieux. 1996. Intestinal mucin distribution in the germ-free rat and in heteroxenic rat harbouring a human bacterial flora: Effect on inulin in the diet. Br. J. Nutr. 75:882–892.

Fry, R. J. M., S. Lesher, and H. I. Kohn. 1962. Influence of age on the transit time of cells of mouse intestinal epithelium. III. Ileum. Lab. Invest. 11:289–293.

Geyra, A., Z. Uni, and D. Sklan. 2001. The effect of fasting at different ages on growth and tissue dynamics in the small intestine of the young chick. Br. J. Nutr. 86:53–61.[Web of Science][Medline]

Holt, P. R., R. R. Pascal, and D. P. Kotler. 1984. Effect of aging upon small intestinal structure in the Fischer rat. J. Gerontol. 39:642–647.[Abstract/Free Full Text]

Iji, P. A., J. G. van der Walt, T. S. Brand, E. A. Boomker, and D. Booyse. 2003. Development of the digestive tract in the ostrich (Struthio camelus). Arch. Tierernahr. 57:217–228.[Medline]

King, D. E., E. K. Asem, and O. Adeola. 2000. Ontogenetic development of intestinal digestive functions in White Pekin ducks. J. Nutr. 130:57–62.[Abstract/Free Full Text]

Klein, R. M. 1989. Small intestinal cell proliferation during development. Pages 367–392 in Human Gastrointestinal Development. E. Lebenthal, ed. Raven Press, New York, NY.

Konarzewski, M., K. Kozlowski, and M. Ziolko. 1989. Optimal allocation of energy to growth of alimentary tract in birds. Funct. Ecol. 3:589–596.[CrossRef]

McManus, J. F. A. 1948. Histological and histochemical uses of periodic acid. Stain Technol. 23:99–108.[Medline]

Miller, H. M., S. M. Carroll, F. H. Reynolds, and R. D. Slade. 2007. Effect of rearing environment and age on gut development of piglets at weaning. Livest. Sci. 108:124–127.

Obst, B. S., and J. M. Diamond. 1992. Ontogenesis of intestinal nutrient transport in domestic chickens (Gallus gallus) and its relation to growth. Auk 109:451–464.[Web of Science]

Olukosi, O. A., A. J. Cowieson, and O. Adeola. 2007a. Age-related influence of a cocktail of xylanase, amylase, and protease or phytase individually or in combination in broilers. Poult. Sci. 86:77–86.[Abstract/Free Full Text]

Olukosi, O. A., J. S. Sands, and O. Adeola. 2007b. Supplementation of carbohydrases or phytase individually or in combination to diets for weanling and growing-finishing pigs. J. Anim. Sci. 85:1702–1711.[Abstract/Free Full Text]

Pacha, J., R. Vagnerova, and J. Bryndova. 2003. Carbenoxolone accelerates maturation of rat intestine. Pediatr. Res. 53:808–813.[CrossRef][Web of Science][Medline]

Poole, C. A., E. A. Wong, A. P. McElroy, H. P. Veit, and K. E. Webb Jr. 2003. Ontogenesis of peptide transport and morphological changes in the ovine gastrointestinal tract. Small Rumin. Res. 50:163–176.[CrossRef]

Robertson, A. M., and D. P. Wright. 1997. Bacterial glycosulfatases and sulfomucin degradation. Can. J. Gastroenterol. 11:361–366.[Web of Science][Medline]

Sabat, P., and C. Veloso. 2003. Ontogenic development of intestinal disaccharidases in the precocial rodent Octodon degus (Octodontidae). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 134:393–397.[Medline]

Smirnov, A., E. Tako, P. R. Ferket, and Z. Uni. 2006. Mucin gene expression and mucin content in the chicken intestinal goblet cells are affected by in ovo feeding of carbohydrates. Poult. Sci. 85:669–673.[Abstract/Free Full Text]

Soriano, M. E., N. Rovira, N. Pedros, and J. M. Planas. 1993. Morphometric changes in chicken small intestine during development. Z. Gastroenterol. 31:578. (Abstr.)

Specian, R. D., and M. G. Oliver. 1991. Functional biology of intestinal goblet cells. Am. J. Physiol. Cell Physiol. 260:C183–C193.[Abstract/Free Full Text]

Uni, Z., A. Geyra, H. Ben-Hur, and D. Sklan. 2000. Small intestinal development in the young chick: Crypt formation and enterocyte proliferation and migration. Br. Poult. Sci. 39:544–551.

Uni, Z., A. Smirnov, and D. Sklan. 2003. Pre- and posthatch development of goblet cells in the broiler small intestine: Effect of delayed access to feed. Poult. Sci. 82:320–327.[Abstract/Free Full Text]

Wang, L., J. Li, Y. M. Chen, and X. L. Duan. 2003. Morphological change in rat jejunal mucosal epithelia and cell proliferation and apoptosis in different months. Acta Zool. Sin. 49:91–97. (in Chinese)

Wang, H. Y., Y. M. Guo, and C. H. Jason. 2008. Effects of dietary supplementation of keratinase on growth performance, nitrogen retention and intestinal morphology of broiler chickens fed diets with soybean and cottonseed meals. Anim. Feed Sci. Technol. 140:376–384.

Wang, J. X., K. M. Peng, A. N. Du, L. Tang, L. Wei, E. H. Jin, Y. Wang, S. H. Li, and H. Song. 2007. Histological study on the digestive ducts of African ostrich chicks. Chin. J. Zool. 42:131–135. (in Chinese)

Wu, Y. B., V. Ravindran, D. G. Thomas, M. J. Birtles, and W. H. Hendriks. 2004. Influence of method of whole wheat inclusion and xylanase supplementation on the performance, apparent metabolisable energy, digestive tract measurements and gut morphology of broilers. Br. Poult. Sci. 45:385–394.[CrossRef][Web of Science][Medline]

Xia, M. S., C. H. Hu, and Z. R. Xu. 2004. Effects of copper-bearing montmorillonite on growth performance, digestive enzyme activities, and intestinal microflora and morphology of male broilers. Poult. Sci. 83:1868–1875.[Abstract/Free Full Text]

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Wang, J. X. Articles by Peng, K. M. Search for Related Content PubMed PubMed Citation Articles by Wang, J. X. Articles by Peng, K. M.