Cell Apical Surface Area in Enterocytes from Chicken Small
and Large Intestine During Development1
RUTH FERRER,2 JUANA M. PLANAS, and MIQUEL MORETO
Grup d'Absorcid Intestinal, Unitat de Fisiologia, Facultat de Farmacia,
Universitat de Barcelona, Av. Joan XXIII s/n, 08028 Barcelona, Spain
1995 Poultry Science 74:1995-2002
source of nutrients rich in lipids, is
replaced by a carbohydrate-rich solid diet
Nutritional demands during early de- (Buddington and Diamond, 1989). The
velopment are fulfilled by adaptive yolk sac content is then progressively
changes in gastrointestinal morphology consumed until the 2nd wk of age, when it
and function. In mammals, the transition is exhausted.
from a milk diet to a solid diet at weaning
The capacity to transport sugars and
is accompanied by an increase in mucosal amino acids by the chicken intestine
mass and nutrient absorption capacity to during early development is well
adapt the intestine to the new dietary documented (Shehata et ah, 1981; Planas et
requirements (Ferraris, 1994). In birds, al, 1986; Esteban et al, 1991; Moret6 et al.,
there is an abrupt change in the source of 1991; Obst and Diamond, 1992; Rovira et
nutrients from the 1st d after hatch, when al., 1994). However, studies on the morthe yolk sac, an embryonic parenteral phology of the developing digestive system are restricted to measurements at
either the macroscopic level (Baranyiova,
1972; Gheri Bryk and Gheri, 1990; KonarReceived for publication January 21, 1995.
zewski
et al., 1990) or to the level of the
Accepted for publication July 25, 1995.
1
This work was subsidized by grants PB91/0159 villus (Bayer et al., 1975; Yamauchi and
and PB91/0274 from Direcci6n General de Investiga- Isshiki, 1991). Microvillus evolution is
ci6n Cientifica y Tecnica, Ministerio de Educaci6n y only documented in the embryonic period
Ciencia, Spain.
2
To whom correspondence should be addressed. (Overton and Shoup, 1964; Chambers and
INTRODUCTION
1995
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ABSTRACT The absorptive surface of epithelial cells from chicken small and
large intestine was studied at the day of hatch (1 d group) and at 2 and 6 wk after
hatch. The segments considered were duodenum, jejunum, ileum, cecum
(proximal, medial, and distal regions), and rectum. The length, diameter, and
density of microvilli as well as cell apical diameter were measured in tip-villous
enterocytes by transmission electron microscopy. The results obtained showed
that during development: 1) microvillus length remained constant in duodenum and jejunum and decreased in the other segments; 2) microvillus diameter
increased only in the jejunum and the rectum; 3) microvillus density increased
in duodenum, ileum, distal cecum, and rectum (especially from 1 d to 2 wk) and
did not change in the other segments; 4) cell apical diameter did not change; 5)
apical surface area increased both in the duodenum (2nd to 6th wk) and in the
jejunum (1 d to 2 wk) but did not change in the ileum. In the proximal-medial
cecum and in the rectum there was a decrease in apical surface, whereas no
changes were observed in distal cecum. Results indicated that microvillus
length and density are the variables that best explain the changes observed in
apical surface that occurred during development.
{Key words: absorptive cell, microvillus amplification factor, transmission electron microscopy, ultrastructure, mucosa)
1996
FERRER ET AL.
MATERIALS AND METHODS
Male White Leghorn chickens 1 d
(about 8 h after hatch), 2 wk, and 6 wk of
age were used (three birds per age group).
Animals were obtained from Cooperativa
Comarcal d'Avicultura de Reus3 and
maintained in standardized temperature
and humidity conditions, with free access
to a commercial diet (Gallina BlancaPurina:* 21.8% protein and 2,900 kcal ME/
kg). Birds were killed in the morning by
neck fracture without previous starvation
and a segment of the duodenum (pancreatic loop), jejunum (yolk sac region),
ileum (the region connected with mesentery to ceca), proximal, medial, and distal
cecum (Ferrer et al, 1991), and the rectum
were removed. Once the mesenteric tissue
had been trimmed off, the intestinal segments were opened lengthwise and
washed with ice-cold saline (NaCl, 9 g/L).
Four pieces about 1 mm2 were obtained
from each segment, fixed in 25 mL/L
glutaraldehyde in .1 mmol/L phosphate
buffer (pH 7.4), and then washed in .2
mmol/L phosphate buffer. The tissues
3
Cooperativa Comarcal d'Avicultura, 43280 Reus,
Spain.
Gallina Blanca-Purina, 08730 Els Monjos, Spain.
were then postfixed in .2 mmol/L phosphate buffer containing 20 g Os0 4 /L,
dehydrated in acetone, and further embedded in Araldite. Of the four Araldite
blocks prepared for each animal and
segment, one was randomly selected to
make ultrathin sections (60 nm). Sections
were then stained with uranyl-acetate and
lead citrate according to Reynolds (1963).
Specimens were examined in a Philips EM
200 electron microscope, operating at 100
kV. Sample processing and observation
were carried out at the Servei de
Microsc6pia Electronica of Universitat de
Barcelona.
Micrographs of known magnification
were used for measurement of morphometric parameters. Cell apical surface was
estimated at the tip of the villus avoiding
the extrusion zones by measuring the
following parameters: 1) cell apical diameter (in micrometers), taken as the
distance between two junctional complexes in sections parallel to the long cell
axis; 2) length and diameter of microvilli,
measured using their longitudinal and
transversal sections, respectively; and 3)
microvillus density (number of microvilli
per square micrometer of tissue), measured on transversal sections. A number of
pictures, as indicated in figure legends,
were obtained from each intestinal sample
of three birds. The results of morphometric determinations were obtained from at
least 10 structures in every picture and the
average value for each micrograph was
calculated. These data were then pooled to
calculate the mean value of each variable,
and expressed as mean ± SE, n = number
of pictures.
Microvillus amplification factor (MAF),
a dimensionless ratio by which microvilli
increase the absorptive surface area (Ferraris et al, 1989), was calculated as: MAF =
i x l x d x D + 1 where 1, d, and D are,
respectively, microvillus length, diameter,
and density. This formula assumes each
microvillus to be a circular cylinder. Mean
values of three birds were used in the
formula, as no differences among such
birds were found.
The cell apical flat surface area was
calculated from cell diameter (C<j) assuming that the section of enterocytes is
Downloaded from http://ps.oxfordjournals.org/ at Penn State University (Paterno Lib) on May 11, 2016
Grey, 1979) and no information is available on possible changes in absorptive
surface area in the posthatch period.
The purpose of the present study was
to quantify the apical surface of enterocytes of small and large intestine of the
chicken, because this variable may influence the capacity of absorptive cells to
take up nutrients. The study was carried
out at three relevant stages of development: the day of hatch, at 2 wk after the
hatch, when yolk reserves were exhausted,
and at 6 wk after the hatch, when feather
molt reached its peak. Cell apical surface
area was determined in enterocytes of the
upper part of the villus because these cells
have the maximal transport capacity for
nonelectrolytes (Stirling and Kinter, 1967;
Hwang et al, 1991; Ferraris et al, 1992;
Takata et al, 1992).
CELL APICAL SURFACE IN CHICKEN INTESTINE DURING DEVELOPMENT
circular. Calculation of cell apical surface
area was done as follows:
1997
were compared by Student's t test. Confidence intervals of estimations were fixed
at 95%.
S = 7T x Q2/4 x MAF
RESULTS
Figure 1A shows that microvillus
length of enterocytes from the duodenum
and from the jejunum remained unchanged in the three age groups studied (1
d, 2 wk, and 6 wk of age). In the other
segments this variable decreased from 1 d
to 2 wk, showing a further decrease in
E
x
u
55
E
c
m
w
H
s
<
5
E
4
>•
55
z
u
Q
I
PC
MC
DC
INTESTINAL SEGMENTS
FIGURE 1. Microvillus length (A), diameter (B), and density (C) of absorptive cells of the tip-villus zone of
duodenum (D), jejunum (J), ileum (I), proximal cecum (PC), medial cecum (MC), distal cecum (DC), and
rectum (R) of 1-d-old, 2-wk-old, and 6-wk-old chickens. The asterisks mark the age group that shows
significant differences with respect to the other two groups. Means within the regions of the small and large
intestines with no common superscript differ (P < .05): a,b for 1 d, m-o for 2 wk, and w-z for 6 wk. Results are
expressed as mean ± SE of 6 to 21 pictures. The results of J, PC, MC, and DC of 6-wk-old animals are from
Planas et al. (1987). Microvillus length and diameter were measured using their longitudinal and transversal
sections respectively, and microviUus density was determined on transversal sections.
Downloaded from http://ps.oxfordjournals.org/ at Penn State University (Paterno Lib) on May 11, 2016
The statistical analysis of data from
microvillus length, diameter, and density,
and cell apical diameter was made using a
two-way ANOVA of the appropriate
model and Snedecor's F test (Guttman,
1982). On the basis of the final model, the
hypotheses were rejected at an a-risk level
of .05. MAF and cell apical surface area
1998
FERRER ET AL.
Alt,/
•
• • •
;
:
FIGURE 2. Microvillus longitudinal sections from chicken proximal cecum of 1-d-old (A),
2-wk-old (B), and 6-wk-old animals (C). The magnification is the same for all the micrographs (scale bar = 1
lim).
proximal cecum at 6 wk (Figure 2). most significant observation was a reducMicrovillus length also differed among tion in microvillus length in ileum and
regions. At the day of hatch, the intestinal proximal cecum.
Microvillus diameter showed few
segments could be distributed into three
groups according to the degree of changes during development. Differences
microvillus development: first, duode- were found only in jejunum and rectum,
num, jejunum, ileum, and proximal ce- where this parameter increased with age
cum, with long microvilli; second, medial (Figure IB). Results also showed that
and distal cecum, with short microvilli, microvilli were, at any age, broader in the
and finally the rectum, with microvilli of jejunum and in the medial-distal cecum
intermediate height. At 6 wk of age, the than in the other intestinal regions.
TABLE 1. Microvillus amplification factor of absorptive cells from the tip-villus region of the small
and large intestines during development1
Segment
1 d
Duodenum
27.2
(18)
26.2
(8)
28.1
(10)
28.5
(9)
16.7
(7)
12.9
(11)
17.9
(14)
Jejunum
Ileum
Proximal cecum
Medial cecum
Distal cecum
Rectum
± .82*.y
± .90a-y
± 1.25<>
± l^O3-*
± 1.1/*."
± .73"
± 1.06b.*
2 wk
6 wk
29.8
(19)
33.7
(8)
24.3
(9)
25.7
(6)
11.2
(8)
10.7
(6)
18.3
(9)
37.4
(10)
38.4
(6)
28.6
(16)
19.4
(16)
11.7
(7)
12.7
(6)
13.8
(21)
± 1.1 W
± 1.69a."
± .94b
± 1.79b-*
± .90^
± 1.2d
± \2&*
± 2.40a>*
± 2.16a'*
± 1.37b
± 1.28cy
± .77d,y
± .80d
± 1.01d-y
a
-dMeans within a column (region of the small and large intestines) with no common superscript differ (P
< .05).
x
<yMeans within a row (age) with no common superscript differ (P < .05).
Results are expressed as mean ± SE. The number of data is indicated in parentheses.
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-
CELL APICAL SURFACE IN CHICKEN INTESTINE DURING DEVELOPMENT
1.0
FIGURE 3. Microvillus length [V], diameter [•],
and density [•] of absorptive cells of the tip-villus
zone of duodenum (D), jejunum (J), ileum (I),
proximal cecum (PC), medial cecum (MC), distal
cecum (DC), and rectum (R) as a function of the
Microvillus Amplification Factor (MAF). All variables are expressed as the 6 wk:l d ratio.
Microvillus density (Figure 1C) showed no
differences during development in jejunum, proximal cecum, and medial cecum
and increased in duodenum, ileum, distal
cecum, and rectum. The regional analysis
of the results indicated that the density of
microvilli was lower in medial and distal
cecum than in the other segments.
The increase of the apical surface area
of enterocytes due to microvilli was estimated from MAF. The results obtained
(Table 1) indicated that during development, this variable increased in duodenum
and jejunum; it did not change in the
ileum and distal cecum, and it declined in
proximal cecum, medial cecum, and in the
rectum. The regional analysis of 1-d-old
chicks indicated that the small intestine
and proximal cecum had a greater MAF
than the other segments; however, in
6-wk-old birds, the higher MAF was
found in duodenum and jejunum, which
progressively decreased to lower values in
the mid-distal cecum and in the rectum.
To quantify the contribution of microvillus length, diameter, and density to
MAF, the ratio between the data of the
6-wk-old group and of the 1-d-old group
was calculated for each variable as a
function of MAF (Figure 3). The results
indicated a tendency to form three groups.
The first group included the segments of
the large intestine showing a reduction in
MAF; in this group the variable determining the major modifications in MAF was
microvillus length. In the second group,
700
S
•
1d
V7\ 2 wk
^ B 6 wk
-3= 600 -
<
a
<
500
w
y
400 -
S
300
*
i
CO
<
u
<
200
°
100
J
j
a
u
I
PC
v
r1-!
Mm
MC
DC
INTESTINAL SEGMENTS
FIGURE 4. Cell apical surface area of absorptive cells of the tip-villus zone of duodenum (D), jejunum (J),
ileum (I), proximal cecum (PC), medial cecum (MC), distal cecum (DC), and rectum (R) of
1-d-old, 2-wk-old, and 6-wk-old chickens. The asterisks mark the age group that shows significant differences
with respect to the other two groups. Means within regions of the small and large intestines with no common
superscript differ (P < .05): a-c for 1 d, m - o for 2 wk, and w-y for 6 wk. Results are expressed as mean ± SE of
6 to 21 pictures.
Downloaded from http://ps.oxfordjournals.org/ at Penn State University (Paterno Lib) on May 11, 2016
MAF CHANGES
1999
2000
FERRER ET AL.
DISCUSSION
The process of enterocyte maturation is
accompanied by a progressive growth of
microvilli. In chicken jejunum and cecum,
the MAF increases along the crypt-villous
axis (Ferrer et al, 1991). This pattern has
also been described in mammals for
microvillus length (Madara and Trier,
1994). Studies on nutrient absorption indicate that the upper villus has the maximal
transport capacity, suggesting that the tipvillus enterocytes are better endowed for
nonelectrolyte transport (Stirling and
Kinter, 1967; Hwang et al, 1991; Ferraris et
al, 1992; Takata et al, 1992). For these
reasons we have studied cell apical surface
area in enterocytes of the upper part of the
villus in order to better understand the
absorptive functions of the chicken intestine.
Morphometrlc Measurements
of Microvilli
In terms of regional comparison, the
longer microvilli occurred in the more
proximal segments and in the younger
animals. Microvillus length showed a distinct degree of development in the different
regions studied when 1-d-old and 6-wk-old
groups were compared. The statistical analysis demonstrated that the intestinal segments of 1-d-old birds can be divided into
two populations; one with the longer
microvilli, which included duodenum, jejunum, ileum, and proximal cecum, and the
other with the shorter microvilli (medialdistal cecum and rectum). This pattern was
not maintained by the 6-wk-old animals
because at this age, a reduction in microvillus length was observed in the distal
direction, i.e., the duodenum and jejunum
maintained their length with age, whereas
the other regions experienced a reduction in
microvillus length. This compares well with
the results of Humphrey and Turk (1974)
showing longer microvilli in the duodenum
than in the ileum in 4- to 7-wk-old chickens.
The segment showing the greatest reduction in microvillus length (illustrated in
Figure 2), with a 40% decline from 1 d to 6
wk, was the proximal cecum. It is worth
noting that Chambers and Grey (1979)
described an increase in microvillus length
in the duodenum during the 1st wk of life.
This study of the diameter of microvilli
shows only slight changes during development, as were also described by Ferraris et
al (1989) when comparing different species,
along the intestine and in the crypt-villus
axis (Ferrer et al, 1991), and during embryonic development (Chambers and Grey,
1979). The ratio of microvillus length to
microvillus diameter indicates that changes
in both variables run parallel during development. In most ultrastructural studies,
changes in microvillus length are not accompanied by any change or reduction in
microvillus diameter (Overton and Shoup,
1964; Merril et al, 1967; Ferraris et al, 1989;
Ferrer et al, 1991). However, in this study,
the ratio between microvillus length and
diameter indicates there is a reduction in
this ratio from 1 d to 2 wk in all segments
except in the duodenum, confirming that in
the chicken intestine, the patterns followed
by these two variables are different. Our
results in 6-wk-old birds also show that
microvilli of the jejunum have a larger
diameter and lesser density than those of
the duodenum, similar to what was found
by Humphrey and Turk (1974) in animals of
similar age.
Apical Surface Area
The values of MAF obtained in the
present study fell between 11 (medial
cecum) and 38 (jejunum), and were consistent with the values calculated by Strong et
Downloaded from http://ps.oxfordjournals.org/ at Penn State University (Paterno Lib) on May 11, 2016
which includes the distal cecum and
ileum, there was no modification in MAF
because changes in length and density
were mutually compensated. In the third
group, modifications in MAF were determined by density (duodenum) and diameter (jejunum).
Cell apical diameter was also measured
to calculate the cell flat apical surface area.
The results showed that mean values were
comprised between 3.25 and 5.2 pm,
without any developmental or regional
differences. We next calculated cell apical
surface area (Figure 4) and the results
showed that this variable had a similar
developmental pattern to that of MAF.
The regional analysis indicated that
duodenum and ileum were the segments
with the greatest apical surface area,
followed by jejunum, the cecum (with a
proximo-distal reduction), and the rectum.
CELL APICAL SURFACE IN CHICKEN INTESTINE DURING DEVELOPMENT
Surface Area and Nutrient
Absorption During Development
The present study shows an increase in
apical surface area of the jejunal cells from 1
d to 2 wk, which could be attributed to the
greater development of microvilli. In the
jejunum, a peak in monosaccharide transport has been described in the 2nd wk after
the hatch (Buddington and Diamond, 1989;
Obst and Diamond, 1992) due to an increase
in maximal transport velocity (Rovira et al,
1994). In the other segments of the small
intestine, however, no significant changes
in nonelectrolyte transport were observed
in this period (Rovira et al, 1994). The
increase in jejunal surface area taking place
at the time when the growth of intestinal
mass and metabolic demands are maximal
(Obst and Diamond, 1992) may be indicative of morphological adaptation.
In the cecum, there is also a correlation
between structure and function: thus, the
proximal region showed greater development of microvilli at any age, consistent
with the view that enterocytes from these
regions have a considerable capacity to
transport nonelectrolytes, an ability that is
retained in adult animals (Ferrer et al, 1986;
Planas et al, 1986; Moret6 et al, 1991).
Medial cecum can accumulate sugars only
on the day of hatch and this capacity is lost
in 2-wk-old chickens (Planas et al, 1986), an
observation consistent with the decrease in
MAF in the same period described in the
present study. Finally, the distal cecum, a
region incapable of transporting hexose at
any stage of development, was also the
segment that had the smaller microvilli.
From a regional point of view, the small
intestine showed a considerable homogeneity in MAF at the day of hatch but in
6-wk-old chickens the duodenum and jejunum increased their surface area whereas
the ileum remained unchanged. Isolated
enterocytes from proximal segments
(duodenum, jejunum) of 4- to 7-wk-old
chickens, were shown to be better suited for
apical hexose uptake than the ileum (Ferrer
et al, 1994). Both observations suggested a
morphological and functional correlation,
which had to be considered to understand
the physiology of the digestive system.
In conclusion, our results show that the
process of intestinal maturation is associated with changes of the mucosa. These
changes would contribute to meeting the
increasing metabolic demands during early
development.
ACKNOWLEDGMENTS
The authors are indebted to the staff of
the Servei de Microsc6pia Electr6nica,
Universitat de Barcelona, for their valuable help.
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