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The effect of starvation on the duodenal epithelium.

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THE EFFECT O F STARVATION ON
THE DUODENAL EPITHELIUM
S. LESHER, A. SALLESE AND G. SACHER
Division of Biological and Medical Research
Argonne National Laboratory
Lemont, Illinois
SIX FIGURES
INTRODUCTION
Sun ('27) and Diller and Blauch ('46) studying the histological changes in the small intestine of starved mice described pronounced lesions at the tips of the villi by 40
hours. Since lesions similar to those described by Sun are
produced in the small intestine by high doses of ionizing
radiation (Lesher '57, Lesher and Vogel '58, Montagna and
Wilson '55) and since the food intake of the irradiated animal is greatly reduced it became necessary to re-examine the
effect of starvation on the small intestine of mice maintained
under normal laboratory conditions.
MATERIALS AND METHODS
Mice were housed individually in plastic cages either with
wire bottoms or with wood shavings. Equal numbers of male
and female LAF', mice were placed in 4 experimental groups :
(1)no food, free access to water, wire-bottom cages; (2) no
food, no water, wire-bottom cages; (3) no food, free access
to water, cages with wood shavings, and (4) no food, no
water, cages with wood shavings. The mice were 100 days
old at the start of the experiment.
One male and one female mouse were killed at 1, 2, 3, 4, 5 ,
and 6 days and a segment of duodenum immediately distal to
*This work was performed under the auspices of the U. S. Atomic Energy
Commission.
677
678
S. LESHER, A. SdLLESE AND 0. SACHER
the pyloric sphincter was fixed in Tellyesnicky 's solution.
All tissues were sectioned at 7 p and stained with hematoxylin and eosin, toluidine blue (1:1000 solution buffered
to pH 4.5 with McIlvaine's buffer), periodic acid-Schiff reaction (PAS), and the Feulgen reaction. The same techniques were carried out on a similar number of control mice
allowed free access to food and water.
Twenty additional mice (10 male, 10 female) were assigned to each of the 4 groups. These mice were used to
determine the survival curves (fig. 2). 811 animals were
weighed daily.
OBSERVATIONS AND DISCUSSION
The animals were checked every 4 hours during the
entire course of the experiment. The mice of all 4 groups
lost weight rapidly with approximately 50 per cent of the
total weight lost in 4 days occurring during the first day
(fig. 1). Those in groups 1 and 2 (on wire) were in constant
DAYS
STARVATION
Fig. 1 Cumulative weight loss in per cent.
0-u
wire; A-A
no food, no water, on wire; 0
shavings; 0-0
no food, no water, on shavings.
4
no food, with water, on
no food, with water, on
STABVATION EFFECTS ON DUODENUM
679
movement. By 48 hours the entire intestine of all mice was
devoid of food.
The mice in groups I, 2, and 4 began to die on the third
day and all were dead by the end of the sixth day (fig. 2).
The first of the mice in group 3, which were maintained on
wood shavings and allowed free access to water, did not die
until the fourth day and survivors lasted into the 13th day.
DAYS OF STARVATION
Fig. 2 Cumulative mortality in per cent plotted against days of starvation.
0-0
no food, with water, on wire; A--A
no food, no water, on wire;
o---+
no food, with water, on shavings; 0-0
no food, no water, on
shavings.
There was no significant difference in the cumulative mortality of groups 1, 2, and 4 nor between sexes of all 4 groups.
An examination of the daily body weight loss reveals the
same relationship : weight loss was approximately equal in
groups 1, 2, and 4 ; however the reduction was not so great
in group 3 (fig.1). The reason for this unexpected result is
not clear; however, it would appear improbable that the
680
S. LESHER, A. SALLESE AND G. SACHER
mouse could derive any nutritional benefit from wood shavings. Since mice in groups 1, 2, and 4 were extremely active
while those of group 3 remained quietly burrowed into the
wood shavings and since intussusception was common in the
former groups and not in the latter, the increased energy
demands and the greatly retarded circulation could possibly
account for the earlier deaths.
At the histological and cytological levels the duodenum of
all 4 groups appeared essentially the same, and after 4
days starvation the epithelial continuity was unbroken. Although the mitotic index was slightly lower than that of the
control animals the production of new cells was sufficient to
maintain the epithelial covering of the duodenal villi. I n
none of the animals were the drastic changes described by
Sun ( ’27) observed. However, the two experiments differ
in that the mice used by Sun were small and probably quite
young while the mice used in this experiment were healthy,
100-day old, LAF, hybrids with an average body weight of
22.5 gm for the females and 25.0 gm for the males, or approximately double the weights of Sun’s animals. I n addition
the physical conditions of Sun’s experiments, e.g., temperature, humidity, caging, etc., were extremely variable.
To determine the sensitivity of young mice, 22 30-day-old
animals were divided into two groups: (I) no food, with
water, on wire, and (2) no food, no water, on wire. The results of this experiment:
Hours:
Deaths
Deaths
72’
6
Sf
(1)
3
96
1
108
1
(2)
2
3
5
1
suggest that young mice are more susceptible to starvation
and if Sun’s mice were approximately 30 days old his results
would be explainable. However, even in the young mouse
the duodenum was microscopically intact and death was not
a result of lesions in mucosal epithelium. This agrees with
the observations of Hooper and Blair (’58) who found that
mucosal thickness, shape of the villi, and epithelial continuity
of the rat duodenum were unaffected by starvation.
S T A R V A T I O N E F F E C T S O N DUODENUM
681
Histochemically it is possible to detect well defined changes
in the starved mice. The amount of PAS-positive material
in Brunner's glands and goblet cells and the cytoplasmic
stainability of the epithelial cells, particularly those cells
near the tips of the villi, was considerably reduced. There
was no reduction in the intensity of the Feulgen reaction:
however, the cytoplasmic basophilia with toluidine blue was
extremely low. There is little change in intracellular structural components such as the cuticular border or the nucleus
and its chromatin material, but materials which the cell synthesizes, for example the mucin of goblet cells, are greatly
reduced.
SUMMARY
Environment plays an important role in the survival time
of starved mice. Under normal laboratory conditions starvation produces very little structural damage in the small intestine ; however, following prolonged starvation there is a
reduction in the stainability of the cells.
L I T E R A T U R E CITED
DILLER,I. C., A N D 13. M. BLAUCH 1946 Influence of diet on mitotic division
in the intestinal epithelium of the mouse. Growth, 10: 331-341.
HOOPER,C., A N D M. BLAIR 1955 The effect of starvation on epithelial renewal
in the r a t duodenum. Exper. Cell Research, 14: 175-181.
LESHER, S. 1957 Cytologic changes in the mouse intestine iinder daily exposure to gamma rags. J . Katl. Cancer Iiist., 79: 419--449.
LESHER,S., A N D H. H. VOGEL 1958 A comparative histological study of
duodenal d:nnage produced b y fission neutrons arid Co"' gamma rays.
Radiation Research, 9 .- 560-571.
MONTAGNA,
W., AND J. W. WILSON 1955 A cytologic study of the intestinal
epithelium of the mouse after total-hody X-irradiation. J. Natl. Cancer
Inst., 1 5 : 1703-1735.
SUN, T. P. 1927 Histophysiologiral study of the epithelial changes in the
small intestine of the albino mouse after starvation and refeeding.
Anat. Rec., 5 4 : 341-349.
PLATE 1
EXPLlNATION O F F I G U K R S
Transverse sections through the duodenal region of the small intestine showing
the intact villi and associated crypts. Notc t h a t the shape of the villi and the
continuity of the epithelial covering has not been disturbed. Sections cut at
7 p and stained with lirmatoxylin and eosin. X 75.
3
Duodenum of control mousr.
4
Duodrnum after 48 hours starvation.
5
Duodenum a f t e r 7 2 hours starvation
G
Duodenum after 96 hours starvation.
I Photoriiicrograplis
by A . Trnryl
STARVATION EFFECTS ON DITODEKUM
S
LESIIXIL, A . SALLESE AND G. SACHEX
PLATE 1
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