Molecular, Cellular, and Developmental Biology
Developmental Morphology of the Small Intestine of African Ostrich Chicks
J. X. Wang and K. M. Peng1
College of Animal Science and Veterinary Medicine, Huazhong Agricultural University,
Wuhan 430070, P. R. China
ABSTRACT 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
2008 Poultry Science 87:2629–2635
doi:10.3382/ps.2008-00163
INTRODUCTION
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
©2008 Poultry Science Association Inc.
Received April 21, 2008.
Accepted August 7, 2008.
1
Corresponding author: [email protected]
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
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
2629
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Wang and Peng
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
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
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DEVELOPMENTAL MORPHOLOGY OF AFRICAN OSTRICH
Table 1. Effects of age on the BW and gross anatomy of African ostrich chicks
Intestinal weight (g)
Age (d)
0
45
90
334
BW (kg)
0.75
5.65
14.05
90.05
±
±
±
±
Duodenum
d
0.38
0.93c
2.12b
6.42a
0.75
50.02
150.21
300.00
±
±
±
±
Jejunum
d
0.24
3.77c
15.23b
20.03a
4.86
250.03
500.45
700.78
±
±
±
±
Intestinal weight:BW (g/100 g of BW)
Ileum
d
0.56
16.89c
35.12b
15.56a
0.58
30.42
61.34
50.87
±
±
±
±
Duodenum
d
0.03
4.35c
13.12a
3.45b
0.10
0.89
1.07
0.33
±
±
±
±
Jejunum
d
0.63
0.41b
0.72a
0.31c
0.65
4.42
3.56
0.79
±
±
±
±
Ileum
c
0.15
1.82a
1.66b
0.24c
0.08
0.54
0.44
0.06
±
±
±
±
0.01b
0.47a
0.62a
0.05b
a–d
Different letters within the same column indicate significant differences among ages according to Duncan’s multiple range (P ≤ 0.05).
(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).
Morphometric Measurements
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).
Mucin Staining
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.
DISCUSSION
Gross Anatomical Characteristics
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
Table 2. Regional development of the small intestine of African ostrich chickens at different ages
Thickness of the muscle (μm)
Age (d)
1
45
90
334
Duodenum
0.28
0.52
1.45
1.67
a–d
±
±
±
±
d
0.12
0.13c
0.23b
0.35a
Jejunum
0.30
0.50
1.49
1.68
±
±
±
±
Intestinal length (cm)
Ileum
d
0.02
0.03c
0.67b
0.61a
0.18
0.70
1.01
1.50
±
±
±
±
Duodenum
d
0.03
0.06c
0.02b
0.24a
17.34
72.25
74.56
141.89
±
±
±
±
Jejunum
c
1.32
4.67b
10.03b
12.67a
43.21
190.00
294.45
257.65
±
±
±
±
Ileum
d
5.65
12.45c
23.43a
23.12b
7.90
40.50
47.65
34.97
±
±
±
±
Different letters within the same column indicate significant differences among ages according to Duncan’s multiple range (P ≤ 0.05).
1.07d
8.97b
7.35a
5.67c
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Wang and Peng
Table 3. Regional development of the small intestine of African ostrich chickens at different ages
Villus height (μm)
Age (d)
1
45
90
334
Duodenum
371.00
1,816.67
2,983.33
4,233.00
±
±
±
±
Villus height:crypt depth
Jejunum
d
53.74
84.98c
154.56b
62.36a
283.33
1,562.44
1,700.23
2,312.44
±
±
±
±
Ileum
c
70.05
99.33b
81.65b
99.33a
506.67
1,400.32
2,101.56
1,809.33
±
±
±
±
Duodenum
d
12.47
16.33c
23.42a
20.45b
28.43
16.49
24.79
19.02
±
±
±
±
Jejunum
a
70.71
10.40d
4.09b
3.49c
22.36
9.66
8.85
6.42
±
±
±
±
Ileum
a
140.10
9.67b
1.95b
1.35c
18.88
6.21
19.54
11.63
±
±
±
±
15.20a
0.29c
2.82a
0.44b
a–d
Different letters within the same column indicate significant differences among ages according to Duncan’s multiple range (P ≤ 0.05).
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,
Table 4. Villus width and crypt depth development of the small intestine of African ostrich chickens at different ages
Villus width (μm)
Age(d)
1
45
90
334
a–c
Duodenum
90.02
110.23
142.52
132.53
±
±
±
±
19.30b
25.50ab
14.79a
19.20a
Jejunum
65.03
225.45
205.12
97.25
±
±
±
±
4.42b
35.34a
20.61a
14.75b
Crypt depth (μm)
Ileum
54.75
98.75
184.75
188.25
±
±
±
±
7.32c
8.54b
4.11a
8.42a
Duodenum
13.05
110.20
120.35
222.53
±
±
±
±
0.76c
8.17b
37.82b
17.85a
Jejunum
12.67
161.67
192.03
360.06
±
±
±
±
0. 50c
10.27b
41.67b
73.48a
Ileum
26.83
225.36
107.52
155.56
±
±
±
±
Different letters within the same column indicate significant differences among ages according to Duncan’s multiple range (P ≤ 0.05).
0.82c
55.90a
8.29b
45.55b
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DEVELOPMENTAL MORPHOLOGY OF AFRICAN OSTRICH
1
Table 5. Means of goblet cell of villus and crypts of the small intestine of African ostrich chickens on postnatal d 1, 45, 90, and
334
Goblet cell of villus (cells/mm2)
Age (d)
1
45
90
334
Duodenum
750.00
1,600.03
1,000.15
1,356.67
±
±
±
±
Jejunum
d,C
40.82
81.65a,B
81.65c,A
40.41b,B
1,250.05
1,643.33
1,150.08
1,663.33
±
±
±
±
Goblet cell of crypts (cells/mm2)
Ileum
b,A
40.82
32.99a,AB
40.82c,A
26.25a,A
1,100.00
1,751.33
1,098.33
1,661.67
±
±
±
±
Duodenum
b,B
81.65
35.64a,A
77.71b,A
34.72a,A
21.33
110.00
71.08
83.33
±
±
±
±
c,B
2.62
8.16a,A
2.94b,C
6.64b,C
Jejunum
24.67
41.67
88.28
119.45
±
±
±
±
Ileum
d,B
3.68
3.09c,C
2.16b,B
3.29a,B
41.33
72.03
110.00
170.33
±
±
±
±
2.62d,A
5.89c,B
8.16b,A
4.49a,A
a–d
Different letters within the same column indicate significant differences among ages according to Duncan’s multiple range (P ≤ 0.05).
Different letters within the same column indicate significant differences among segments according to Duncan’s multiple range (P ≤ 0.05).
1
Means ± SEM.
A–C
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 in-
testine (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,
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 × 10; (B) 40 × 10; (C and
D) 10 × 10.
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Wang and Peng
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.
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.
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