A light and scanning electron microscope study

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Ann Anat 190 (2008) 531—540
www.elsevier.de/aanat
RESEARCH ARTICLE
A light and scanning electron microscope study of
the albino rat ileum after partial obstruction
Tarek Mahdy, Gamal Mohamed, Adel Elhawary
Mansoura Faculty of Medicine, Egypt
Received 28 May 2008; accepted 27 July 2008
KEYWORDS
Light and scanning
electron
microscope;
Ileum;
Partial obstruction;
Short bowel disease
Summary
Purpose: Induction of an obstruction could be resorted to as a definitive line of
management in some cases of short bowel syndrome (SBS). The goal of this study has
been to elucidate histological and morphometric alterations in the albino rat ileum
after surgically induced partial obstruction.
Methods and materials: Thirty adult male albino rats (240–250 g) were used in this
investigation. They were divided into two equal groups: control and experimental.
Small pieces of the ileum of the control and experimental animals were processed
for histological and scanning electron microscope study.
Results: The ileum of the experimental animals proximal to the site of obstruction
showed an apparent enlargement in the Peyer’s patches and an increase in the
thickness of both the mucosa and muscle layers. The villi showed significant
elongation and thickening. Both widening and deepening of the crypts were
detected. There was an apparent increase in the goblet cell number and lymphocytic
infiltration in both the corium and submucosa. In scanning electron microscopic
examination, the microvilli showed scattered areas of shortening and irregular
orientation. The surface was more frequently interrupted by goblet cell orifices.
Conclusions: Partial ileal obstruction resulted in hypertrophy of the ileal wall with
considerable structural alterations oral to the obstruction site. Thus, the procedure
apparently increased the absorptive surface area together with reduction in the
speed of intestinal transit. These effects could support taking this technique into
consideration as one of the suggested lines of treatment of some cases of SBS to
eliminate the patient’s need for parenteral nutrition and all of its associated
complications.
& 2008 Elsevier GmbH. All rights reserved.
Corresponding author.
E-mail address: [email protected] (T. Mahdy).
0940-9602/$ - see front matter & 2008 Elsevier GmbH. All rights reserved.
doi:10.1016/j.aanat.2008.07.009
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Introduction
The small intestine is the site of terminal food
digestion. It is also constituted for absorption of
nutrients. This function is enhanced by several
structural devices responsible for a 600-fold increase in the total intestinal surface area compared
to the simple flat intestinal surface, i.e. without
these structural devices. These are the plicae
circulares, the myriad villi and the microvilli on
the epithelial cells (Fawcett and Jensh, 2002;
Junqueira and Carneiro, 2005). Another important
function of the small intestine is the transport of its
luminal content to the colon. Any condition that
interferes with this is classified as obstruction. The
latter may be complete or partial; its causes may
be vascular, neural or mechanical. The latter may
be attributed to factors within the lumen, in the
wall or outside it, as a result of compression (Woolf,
1998; Rubin and Farber, 1999; Ross and Pawlina,
2006).
Although any portion of the gut may be obstructed due to its narrow lumen, the small
intestine is most commonly affected (Williams
et al., 1993; Kumar et al., 2003). In the human,
mechanical intestinal obstruction is a common
surgical problem which is most often caused by
post-operative adhesions or by hernia (Sabiston and
Lyerly, 1997; Suri et al., 1999). The causes of
intestinal obstruction also differ in children, where
necrotizing enteritis and ascariasis are the common
causes in tropical countries (Elhinnawy, 2004).
Congenital bands, urachal remnants, annular pancreas and multiple segmental muscular defects are
also among the causes of intestinal obstruction in
children. (Itagaki et al., 2005; Hulvat et al., 2006;
Kella and Rathi, 2006). In animals, such as horses,
the ileum is the most common site for small bowel
obstruction, while in cattle, obstruction may be
duodenal, jejunal or ileal. There are several
reasons for intestinal obstruction in small animals
such as linear foreign bodies, focal intestinal
neoplasia, feline infections, peritonitis and megacolon (Macphail, 2002; Nuss et al., 2006).
Induced partial intestinal obstruction has been
thought to be a last resort as a definitive line of
treatment in short bowel syndrome (SBS) resulting
from extensive bowel resections, in order to avoid
the necessity of lifelong use of parenteral nutrition
(Tannuri, 2003; Keller et al., 2004; Chang et al.,
2006). The primary goal of such a surgical intervention in SBS is to optimize the intestinal function
(Di Baise et al., 2004; Park et al., 2004). Thus,
partial intestinal obstruction could be regarded
as a surgical disorder or a suggested remedy for
another disorder. Hence, the idea of the current
T. Mahdy et al.
investigation arose with the intent of presenting a
vivid picture of the histological and morphometric
alterations in the albino rat ileum after induced
partial obstruction.
Materials and methods
Thirty adult male albino rats (240–250 g) were
used in the current study. They were categorized
in two equal groups: control and experimental.
The animals were handled in accordance with
guidelines of animal welfare prior to the experiment. The animals of the experimental group
were subjected to ketamine hydrochloride anaesthesia (45 mg/kg). Under aseptic techniques, the
abdomen was opened via a midline incision and a
loop of ileum approximately 2–4 cm from ileocecal junction was exposed and placed on sterile
gauze soaked in warm sterile saline solution.
Through an incision in the mesentery between
two blood vessels close to the gut, a plastic ring
was tied around the intestine. The ring diameter
exceeds that of ileum by 1–2 mm leaving the
ring free to turn initially (Plate A, Figure 1).
The intestine was then returned back into the
abdominal cavity and the abdominal incision was
closed. The animals were operated in the morning
and solid food was not allowed until the following
morning. Postoperatively, the animals were monitored daily with regard to body weight and
abdominal distension. The control rats were subjected to sham operation where the plastic ring
was placed around the ileum as in the experimental
animals but it was removed before closing the
abdominal cavity (Williams et al., 1993; Bertoni
and Gabella, 2001).
Two weeks after the operation, under the same
form of anaesthesia, skin of the control and
experimental rats was incised along the ventral
midline and the chest was exposed. Through the
wall of the left ventricle, a cannula was inserted,
the right auricle was cut to allow drainage and
vascular perfusion was begun. About 100 ml of
100 mM phosphate-buffered saline (PBS) (pH 7.3)
were injected via syringe and under manual
pressure, through the cannula into the ascending
aorta. The abdominal cavity was then opened with
a midline incision and the small intestine excised
and immersed in PBS. A 10 cm long segment of
maximally hypertrophic ileum of the experimental
rats (Plate A, Figure 2) and a similar segment of the
control ileum were cleared of their contents by
injection of PBS into the lumen then draining it.
Each segment was cut into two equal loops, which
were isolated with cotton thread ligature at both
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Table 1. Comparison of data from the control (shamoperated) and experimental animals
Body weight (g)
Mean
SEM
P
Control
Experimental
245.6
0.9
258.4
1.0
o0.05
Circumference of the wall (mm)
Mean
15.2
SEM
0.2
P
43.1
0.4
o0.05
Surface index
Mean
SEM
P
8.9
0.1
o0.05
4.9
0.01
Length of ileal villi (mm)
Mean
479.1
SEM
2.4
P
710.0
6.3
o0.05
Width of the base of ileal villi (mm)
Mean
108.1
SEM
0.3
P
115.4
0.2
o0.05
Density of the ileal villi (mm2)
Mean
15
SEM
0.5
P
6.9
0.2
o0.05
Height of the columnar absorptive cells (mm)
Mean
27.0
27.7
SEM
0.04
0.11
P
o0.05
Height of the microvilli (mm)
Mean
1.1
SEM
0.01
P
Plate A. Figure 1: A photograph showing the cecum (C)
and the terminal part of ileum (I) of an adult male albino
rat. Notice the site of partial intestinal obstruction
(arrow) at the commencement of the experiment. Figure
2: A photograph, 2 weeks after the initial partial ileal
obstruction, showing the cecum (C), the distended part
of ileum (I) proximal to the obstruction site (arrow).
Notice the engorged blood vessels in the mesentery (V).
Figure 3: A photograph showing the method of determination of the surface index by dividing the surface length
(1) by the section length (2) for the control (C) and the
experimental (E) groups.
1.1
0.01
0.2
Density of the microvilli (mm2)
Mean
77.5
SEM
1.9
P
98.8
0.7
o0.05
Diameter of the crypts (mm)
Mean
64.3
SEM
0.8
P
92.3
1.0
o0.05
Thickness of the muscle layer (mm)
Mean
54.4
SEM
1.5
P
178.9
3.2
o0.05
ends and distended by injecting fluid into the
lumen through a small needle piercing the wall at a
small angle (Bertoni and Gabella, 2001).
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Tissue preparation
Results
Small pieces of the ileum of the control and
experimental animals were fixed in 10% neutral
formalin, dehydrated, cleared and embedded in
paraffin wax. Paraffin sections (6 mm) were prepared and stained with Hx&E and periodic acid
Schiff (PAS) (Bancroft and Stevens, 1982). Other
rectangular specimens of ileum 1 mm in thickness
and 3–8 mm in size were fixed in 2% glutaraldehyde
in phosphate buffer at pH 7.3 and proceeded for
scanning electron microscopic study. The specimens were examined and photographed with the
JEOL JSM 5300 scanning electron microscope.
All utilized rats survived throughout the entire
period of the present study. Variable degrees of
abdominal distension were observed in the experimental animals. The mean body weight of the
control rats and that of the experimental group at
the end of the second week was 245.670.9 and
258.471.0 g, respectively. Thus a significant
weight gain was achieved (Po0.05).
Macroscopically, at the final laparotomy, there
was an obvious uniform distension of about 15 cm
long segment of ileum proximal to the obstruction
location. This distension was gradually less evident
in the more oral parts. Distal to the obstruction,
the terminal segment of ileum more or less
resembled that of the control (Plate A, Figures 1
and 2). The outer circumference of the ileal wall
significantly increased (Po0.05) from 15.27
0.2 mm in the control animals to 43.170.4 mm oral
to the partial obstruction site in the experimental
rats after the elapse of 2 weeks (Table 1).
Light microscopic examination of the ileum of
the experimental group proximal to the obstruction
site, 2 weeks after the operation, revealed an
apparent shortening of the villi over Peyer’s
patches (Plate B, Figures 4, Table 1). There was
also an apparent thickening of the mucosa. Some
villi ended in small knobs. Fusion between adjacent
ileal villi might take place. The mean villous length
and basal width were 710.076.3 and 115.47
0.2 mm, respectively. Goblet cell number apparently increased in the villous and crypt epithelium.
The lamina propria housed a considerable cellular
infiltration (Plate B, Figure 5, Table 1). The fused
adjacent villi contained a marked amount of
lymphocytic infiltration in their core and a very
large number of goblet cells in their covering
epithelium. The mean height of the columnar
absorptive cells was 27.770.1 mm (Plate B, Figure
6, Table 1). The ileal crypts showed an apparent
widening with a mean luminal diameter of 92.37
1.0 mm and the nearby blood vessels looked
congested (Plate C, Figure 7, Table 1). Apparently
long ileal villi with a concomitant deepening of the
Statistical analysis
Measurement of the outer circumference of the
wall of the ileum was achieved by applying a plastic
ring around and in close contact with the wall at 10
points for each animal. Measurement of the villous
length (from the tip to base), the width of ileal villi
at the base, height of enterocytes (from the
surface to the base passing through the nucleus),
the diameter of the intestinal glands (crypt lumen)
as well as the thickness of the muscle layer was
performed using a Leitz micrometer eye piece, on
10 randomly selected sections for each animal.
Density of the ileal villi/mm2 and also the height of
the microvilli and their density/um2 were estimated on scanning electron micrographs. The
surface index is defined as surface length divided
by the section (intestinal) length. This index was
calculated from digital images using a personal
computer. Surface length was the length of a line
drawn over the surface of the intestine, outlining
the villi, but not extending into the crypts. The
intestinal length was the length along which the
surface length was measured (Collins et al., 1996)
(Plate A, Figure 3). The measurements obtained
from the control and experimental animals were
expressed as mean7SEM. They were subjected to
the test for significance, in Mansoura University
Computer Center, according to the formula of
Daniel (1987).
Plate B. Figure 4: A photomicrograph of a paraffin section of the albino rat ileum proximal to the obstruction site 2
weeks after the operation showing a part of Peyer’s patch (P), a short villus (V) and a crypt (C) (Hx&E, 100). Figure 5:
A photomicrograph of a paraffin section of the albino rat ileum proximal to the obstruction site 2 weeks after the
operation showing an apparent thickening of the mucosa. The apical parts of some villi end with small knobs (K). Fusion
of adjacent villi may be seen (F). Goblet cell (G) number apparently increases in the villous and crypt epithelium with
appearance of small subepithelial spaces (crossed arrows). The lamina propria lodges considerable cellular infiltration
(asterix). The muscle layer shows separation of the individual smooth muscle fibres (head arrows) (Hx&E, 100). Figure
6: A high power magnification of Figure 5 showing fusion of the adjacent villi which show marked lymphocytic
infiltration (asterix) in their core and a very large number of goblet cells (arrows) in their covering epithelium (Hx&E,
250).
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T. Mahdy et al.
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Plate D. Figure 11: A scanning electron micrograph of the mucosal surface of the terminal part of albino rat ileum
proximal to the obstruction site 2 weeks after the operation showing hypertrophy of the villi (V) with focal detachment
of their epithelial layer (arrow) (scale bar 100 mm). Figure 12: A scanning electron micrograph of the mucosal surface of
the terminal part of albino rat ileum proximal to the obstruction site 2 weeks after the operation showing, in addition to
the villous hypertrophy, noticeable detachments of parts of the epithelial layer (arrows) (scale bar 100 mm). Figure 13:
A scanning electron micrograph of the mucosal surface of the terminal part of albino rat ileum proximal to the
obstruction site 2 weeks after the operation showing a more pebbled mucosal surface (arrows) which contains the
orifices of several goblet cells that may be seen extruding mucus (M) or not (crossed arrow) (scale bar 1 mm). Figure 14:
A scanning electron micrograph of a fractured columnar absorptive epithelial cell of albino rat ileum proximal to the
obstruction site 2 weeks after the operation offering a side view of the mircovilli showing focal shortening and irregular
orientation (arrows). Notice the luminal mucous debris (asterix) (scale bar 1 mm).
crypts could be observed proximal to the obstruction site (Plate C, Figure 8, Table 1). Small spaces
intervened between the individual smooth muscle
fibres of the hypertrophied muscle layer which
became 178.973.2 mm thick (Plate C, Figure 9,
Table 1). The obviously increased number of goblet
cells and their intensely positive PAS reaction were
noticed (Plate C, Figure 10).
The scanning electron microscopic examination of the ileal mucosal surface of this experimental group proximal to the obstruction
site showed hypertrophy of the villi with focal
Plate C. Figure 7: A photomicrograph of a paraffin section of the albino rat ileum proximal to the obstruction site 2
weeks after obstruction showing an apparent widening of the crypts (C) and congestion of the blood vessels (V) (Hx&E,
250). Figure 8: A photomicrograph of a paraffin section of the albino rat ileum proximal to the obstruction site 2
weeks after the operation showing apparently long villi (arrows) with a concomitant deepening of the crypts (Hx&E,
100). Figure 9: A photomicrograph of a paraffin section of the albino rat ileum proximal to the obstruction site 2
weeks after the operation showing a thickening of the muscle layer with small spaces intervening between its individual
smooth muscle fibres (arrows) (Hx&E, 400). Figure 10: A photomicrograph of a paraffin section of the albino rat ileum
proximal to the obstruction site 2 weeks after the operation showing an obviously increased number of goblet cells with
intensely positive PAS reaction (arrows) (PAS 100).
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detachment of some apical epithelial cells (Plate D,
Figures 11 and 12). The mean density of the ileal
villi and microvilli were 6.970.2/mm2 and
98.870.7/ mm2, respectively. The mucosal surface
exhibited a more pebbled appearance. This surface
was more frequently broken by small orifices of
goblet cells which may or may not contain mucus
(Plate D, Figure 13, Table 1). A fractured columnar
absorptive epithelial cell offered a side view of the
microvilli which showed focal shortening and
irregular orientation at multiple sites. The mean
height of these microvilli was 1.170.01 mm (Plate
D, Figure 14, Table 1).
Discussion
Intestinal obstruction is a common surgical
problem caused by several etiologic factors (Kumar
et al., 2003). Then again, an induced partial
intestinal obstruction could be resorted to as a
supposed eventual line of treatment of SBS (Chang
et al., 2006; Sukhotnik et al., 2006). The present
study has been performed to evaluate the histological and morphometric alterations in the albino rat
ileum after its surgically induced partial obstruction utilizing the light and scanning electron
microscopes.
The mean body weight of the experimental rats,
2 weeks after the partial ileal obstruction in the
current study, significantly increased as compared
with that of the control animals. This could be due
to distension of the intestine with the retained
contents together with intestinal hypertrophy. Such
a finding contradicted that obtained by Collins et
al. (1996), who denied any increase in the body
weight of the animals with partially obstructed
intestine. This controversy could be attributed to
differences in the experimental animals used and in
the surgical technique applied.
At the final laparotomy, the experimental rats in
the present work exhibited an obviously uniform
distension of a segment of the ileum oral to the site
of partial obstruction. The outer circumference of
this distended segment increased several times in
comparison to that of the control group. This
distension could be due to both stagnation of
intestinal contents and thickening of the wall.
Similar observations have been reported by Collins
et al. (1996), Shoenberg and Kluth (2002) and
Archer et al. (2006).
The mean length and the basal width of the villi
showed significant increases oral to the obstruction
site in the experimental animals compared to their
corresponding control values. Thus the mean villous
length became six to seven times the mean villous
T. Mahdy et al.
basal width in the experimental rats, while in the
control this mean villous length was four times the
mean villous basal width. This finding was supported by the significantly increased surface index
in the experimental rats. Scanning electron microscopic examination also confirmed the hypertrophy
of the ileal villi. The whole mucosal surface
became more pebbled and exhibited more numerous orifices of goblet cells. In turn, the density of
the villi significantly decreased in the experimental
group. These observations in addition to the
significant widening and the apparent deepening
of the crypts denoted the occurrence of mucosal
hypertrophy. The latter was accompanied by a
significant increase in the height of the columnar
absorptive cells. On the contrary, mucosal hypertrophy without changes in the size of epithelial
cells has been observed by Riecken (1988) in the
ileum after its partial resection and by Bertoni and
Gabella (2001) in the ileum following its partial
obstruction.
The mechanisms involved in mucosal hypertrophy
are obscure. Intraluminal nutrients are perhaps the
most important trophic inducers to intestinal
mucosa. This mucosa becomes atrophic in the
absence of intraluminal nutrients (Wilmore et al.,
1971; Morgan et al., 1987). Moreover, Gabella
(1984) hypothesized that intestinal distension
stretches sensitive elements in the mucosa. Both
the altered innervation and the increased blood
supply may exert additional trophic influences. In
addition, Snider and Johnson (1989) offered a
similar interpretation and postulated that some
local growth factors are liberated within the gut
wall. Uchiyama et al (2000) explained the changes
in gut after a valve construction to be a compensatory mechanism to maintain the bowel contents
and to increase the intestinal absorption. Scolapio
(2001) proposed that the luminal nutrients, beside
their direct trophic effect, could stimulate both
pancreatic and intestinal peptide secretion, which
also promotes growth and function of the intestine.
The mean height of the microvilli, in the present
investigation, exhibited insignificant variation between control and experimental rats. Meanwhile,
the density of the microvilli per mm2 showed a
significant increase proximal to the partial obstruction site in comparison with the controls. The
obtained mean microvillous height, more or less,
was similar to that obtained by Mayhew and
Middleton (1985) and Bertoni and Gabella (2001),
whereas the packing density was vividly different.
Variations amongst these studies could be owed to
differences in strain, age and weight of the
experimental rats and also in the methodology
employed. However, Penzes and Regius (1985)
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A light and scanning electron microscope study of the albino rat ileum after partial obstruction
denied the occurrence of large-scale changes in the
microvilli dimension through the entire life of the
animal except possibly during pregnancy.
The ileal muscle layer proximal to the partial
obstruction site showed a significant increase in the
mean thickness, recording a three-fold increment
compared to the control value. Such a change could
be attributed to muscle hypertrophy because of the
extra effort exerted to push the luminal contents
via the partial obstruction. The small spaces
between the individual smooth muscle fibres of
this layer could be owed to interstitial oedema.
This finding is in accordance with that of Williams
et al. (1993) who observed that a hypertrophied
segment of the same unit length had an approximately 10-fold increase in the weight of the
muscularis externa layer. Bertoni and Gabella
(2001) also stated that distension of the obstructed
ileum is a passive mechanical effect of the
accumulated ingesta, while hypertrophy is an
active process of growth of the intestinal wall,
mainly the musculature. A similar observation was
made by Bettini et al. (2006) in the obstructed
intestine of cats. They attributed that finding to
stimulating factors in the intestinal wall. Moreover,
Meylan et al. (2003) reported that the myoelectric
activity in the ileum of cows immediately oral to
the obstruction site was characterized by abolition
of the migrating myoelectric complex. A constant
pattern of strong spike bursts of long duration was
recorded. Furthermore, Bertoni et al. (2004)
announced that intestinal hypertrophy is a dynamic
process entailing adaptation of both the smooth
muscle and the neuronal structure to the increased
functional load imposed by the obstruction. Additionally, Turan and Osdemir (2004) reported that
extra mucosal intestinal plication retarded intestinal transit. They added that such a technique does
not entail any morbidity or mortality risk. Eventually, Munoz et al. (2006) detected disrupted
muscle bundles and severe degenerative changes
in the myocytes, but no alterations were seen in
the submucosal and myenteric plexus neurons
following intestinal pseudo-obstruction from visceral myopathy.
In light of the present results, it could be
concluded that partial ileal obstruction resulted
in hypertrophy of the ileal wall with considerable
structural alterations oral to the obstruction site.
Such a procedure apparently increased the absorptive surface area in conjunction with slowing of
intestinal transit. These effects could support
taking this technique into consideration as a
promising line of treatment in some cases of SBS
to eliminate patient dependence on parenteral
nutrition and its associated complications.
539
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