quantitative evaluation of experimental ischemic colitis correlated with the degree of artificial...

Gastroenterologia Japonica Vol. 22, No. 5 Copyright �9 1987 by The Japanese Society of Gastroenterology Printed in Japan

- -Or ig ina l Ar t i c l e - -

QUANTITATIVE EVALUATION OF EXPERIMENTAL ISCHEMIC COLITIS CORRELATED WITH THE DEGREE OF ARTIFICIAL

BOWEL OBSTRUCTION IN RATS

Yoichi WATANABE, M.D.

First Department of Pathology, Nippon Medical School, Tokyo 113, Japan

Summary

Experimental ischemic colitis proximal to artificial bowel obstruction was produced under poor regional circulatory conditions in rats. Only the vessels o f the left hemi.colon were l igated to obtain poor circulation (ischemia). Two types of aluminum rings were used to obstruct the bowel at the most distal portion of the ischemic colon. One, with a 4 mm internal diameter, was used for the model of partial colon obstruction with ischemia (partial obstruction, n=25) and the other, with a 2 mm internal diameter, was used for complete colon obstruction with ischemia (complete obstruction, n=25). The circumference of the dilated bowel was larger in complete obstruction than in partial obstruction. Ischemic colitis developed in 9 of 25 rats (34.0%) with partial obstruction and 16 of 25 (64.0%) with complete obstruction. In terms of morphometry, over half o f the ischemic lesions in complete obstruction were more than 1.0 cm 2, but such a large size in partial obstruction was not observed. It was demonstrated that the depth of ischemic lesions gradually increased in extensive lesions. In conclusion, complete colon obstruction with ischemia frequently caused severer ischemic colitis, together with marked distention of the proximal bowel, than partial colon obstruction with ischemia.

Key Words: Bowel distention, Ischemia, Ischemic colitis, Partial and complete colon obstruction, Morphometry.

I n t r o d u c t i o n

I schemic lesions in the area proximal to

co lon carc inoma, a l though rarely reported,

are similar to ischemic colitis descr ibed by

Mars ton and col leagues 1). It is difficult to

d iagnose ischemic colitis proximal to co lon

ca rc inoma preoperat ively since pr imary car-

Received February 25, 1987. Accepted June 8, 1987. Address for correspondence: Yoichi Watanabe, M.D.,

The First Depart_ment of Pathology, Nippon Medical School, 1-1-5 Sendagi, Bunkyo-ku, Tokyo 113,Japan.

The author wishes to thank Prof. Yozo Masugi, the First Department of Pathology, Nippon Medical School for his valuable guidance and encouragement throughout this investigation. The author is also indebted to Mr. Takashi Arai for his technical assistance.

c inoma may mask the presence o f this lesion

and interfere with the clinical examinat ion. I n

recent years, the repor ted occurrence o f this

colitis has gradual ly increased 2) possibly be-

cause absolute n u m b e r s o f co lon ca r c inoma

have increased progressively. In 1907, Van Zwalenburg 3) demons t ra ted by

microscopic observat ions that b lood flow o f

the hol low visceral organs disappeared due

to raised in t ra luminal pressure. ~. O t h e r au-

thors 4-16) studied the relat ionship be tween

bowel d is tent ion and b lood flow experi-

mental ly and conc luded that b lood flow o f the

bowel was r emarkab ly impeded by h ighe r

int ra luminal pressure. O n the contrary, lower

pressure hardly in f luenced the bowel circula-

October 1987 Experimental ischemic colitis with obstruction 579

tion. The factors of colon obstruction which produce ischemic colitis have been little studied. In 1966, Glotzer et al. ~71 produced experimental obstructive colitis, for the first time, in dogs and reported that the degree o f bowel dilatation was varied and seemed to be unrelated to the extent o f ischemic lesions. Alternatively it was suggested that bowel peristalsis would elevate localized intraluminal pressure 9,1s-21) and decrease blood flow in the dilated boweW, l~( Therefore , the purpose of this study is to clarify the pathophysiology of ischemic colitis proximal to colon obstruction with morphometry to measure the ulcerated areas in ischemic colitis.

Materials and Methods

Male Wistar rats, weighing 290 to 370 g, were used in all experiments. The animals were housed at room temperature and given water ad libitum and standard laboratory fodde r pellets (Oriental Yeast Co., Tokyo) until sacrifice. These animals were made to fast for 18 hours before treatment and were anesthesized intraperitoneally by pentobarbi- tal (40 mg per kg body weight) and excised through the midline o f the abdominal wall. The animals were divided into six groups (Table 1). Group I (n=5) was sham-operated with a midline laparotomy. Group II (n=5) was partially obstructed at the most distal portion of the left hemi-colon by an aluminum

ring of 4 mm internal diameter and fixed retroperitoneally by silk sutures. Group III (n=5) was completely obstructed at a similar port ion of the colon by an aluminum ring of 2 mm internal diameter and fixed similarly. In Group IV (n=lS) the marginal arteries and veins of the left hemi-colon were ligated at two points for a distance of 3 cm and all vasa recti between these two points were also ligated (Fig. 1) under the stereoscopic microscope (Ischemia group). In Group V (n=25), the colon was partially obstructed by the 4 mm ring at the distal portion o f the ischemic left hemi-colon as described in Group IV (Partial colon obstruction with ischemia group). Ac- cordingly, the animals in Group VI (n=25) were completely obstructed by the 2 mm ring toge ther with colonic ischemia (Complete colon obstruction with ischemia group).

Evacuation o f feces was recorded in each group. The animals were sacrificed four days after the first experiment. The rats that died before completion of testing were excluded from each group. The macroscopic findings o f the visceral peri toneum were observed and measurement of the bowel circumference was performed at the most dilated portion of the ischemic region. In non-obstructed Groups I and IV the bowel circumference was measured at the portion containing stool. The resected colon specimen was cut laterally along the axis opposite the mesenteric base

Table 1. Design of experiment

Group No. of rats Procedure

I 5 II 5

III 5

IV 15

V 25 VI 25

Sham operation. Use of aluminum ring, 4 mm in internal diameter, partially obstructing and fixing the distal colon. Use of aluminum ring, 2 mm in internal diameter, completely obstructing and fixing the distal colon. Segmental ligation of the marginal vessels and vasa recti to the left hemi-colon (Ischemia). Methods II plus IV (Partial colon obstruction with ischemia). Methods III plus IV (Complete colon obstruction with ischemia).

580 Y. WATANABE Vol. 22, No. 5

a n d opened. With the image analysis system in

morphome t ry (Micro-Videomat 2, Carl Zeiss

Co., Obe rkochen , West Germany) , the area of

d q

3 c m Fig. 2b. This black silhouette is traced from the

photograph in Fig. 2a and the area is measured by morphometric analysis. ----: at the mesenteric side of the colon.

Fig. 1. Diagram of experimental technique. The marginal vessels and all vesa recti to the left hemi-colon were ligated at intervals of 3 cm and the most distal portion O f this ischemic area was obstructed and fixed by an aluminum ring.

Fig. 2c. A microscopic feature of Fig. 2a shows ulceration due to necrosis of the mucosa (UI-I). The regenerating epithelium partially covers the base of this shallow ulcer. (H & E, X60)

Fig. 2a. This resected specimen of partal colon obstruction with ischemia (Group V) was opened laterally along the axis opposite the mesenteric base. There is a small ischemic lesion (arrowhead) at the mesenteric side. The arrow shows the porton obstructed by the aluminum ring.

the ischemic les ion was measu red after pro-

j ec t ing a p h o t o g r a p h of the resected spec imen

o n the screen a n d t rac ing the si lhouette of

ischemic les ion o n a t r anspa ren t plastic plate

(Figs. 2b, 3b). T h e mult iple sections were

made in areas of ischemic lesion. After fixa-

t ion by 10% fo rma ldehyde a n d e m b e d d i n g in

paraffin, the spec imens were rout ine ly s ta ined

with hematoxyl in a n d eosin. Light micro-

scopic observat ion was done with special em-

phasis paid to the depth of the necrotic area.

Data were r e p r e s e n t e d as m e a n s ___ SE.

Statistical analysis was pe r fo rmed us ing Stu-

dent ' s t a n d Chi-square distribution. A p value


Fig. 3a. This resected specimen of complete colon obstruction with ischemia (Group VI) shows an extensive ischemic lesion (arrowhead), which occupies the entire bowel circumference. The arrow shows the portion obstructed by the aluminum ring.

Fig. 3b. This black silhouette is traced from the photograph in Fig. 3a and the area is measured by morphometric analysis. -- --: at the mesenteric side of the colon.

less t h a n 0.05 was r e g a r d e d as significant.

Results

1. Bowel evacuat ion

T h e r e was a l w a y s d i s c h a r g e o f s m a l l

a m o u n t s o f s tool in G r o u p I I a n d V an ima l s

wh ich h a d a l u m i n u m r i n g o f 4 m m in d iame-

ter, t he r e fo re it was t e r m e d par t ia l co lon

obs t ruc t ion . O n the o t h e r h a n d , t h e r e was n o

evacua t ion o f s tool in G r o u p I I I a n d VI

a n i m a l s with the 2 m m co lon ic r ing, t h e r e f o r e

this was t e r m e d c o m p l e t e co lon obstruct ion.

T h e bowel evacua t ion in Groups I a n d IV

wi thout co lon obs t ruc t ion was normal .

2. Macroscop ic f i nd ing o f the p e r i t o n e u m

Peri toni t is was class i f ied f rom mi ld to mark-

e d o n e acco rd ing to the d e g r e e o f a d h e s i o n o f

the ad j acen t t issues such as the mesen te r ium,

the o m e n t u m , the intes t ines , etc. I t was seen

tha t 1 o f 15 an ima l s in G r o u p IV, 8 o f 25

a n i m a l s in G r o u p V a n d 7 o f 25 an ima l s in

G r o u p VI h a d mi ld pe r i ton i t i s (Table 2). O n e

o f 25 an ima l s in G r o u p V a n d 11 o f 25 an imals

in G r o u p VI showed m o d e r a t e a n d m a r k e d

per i ton i t i s (p<0.05).

3. F r e q u e n c y o f i schemic les ions a n d bowel

c i r cumferences

T h e m e a n c i r cumfe rences o f the bowel in

Groups I a n d IV wi thout co lon obs t ruc t ion

were 1.94 _+ 0.23 cm ( m e a n + SE) a n d 1.89 +

Fig. 3c. A microscopic feature ofPigo 3a shows marked necrosis through the colonic wall (UI-IV) with diffuse neutrophil and histiocyte infiltration. (H & E, X60)

Table 2. Macroscopic finding of the peritoneum

Peritonitis Group (%) Total

Mild Moderate Marked

I (n= 5) none none none none II (n= 5) none none none none

III (n= 5) none none none none IV (n=15) 1 (6.7) none none 1 (6.7) V (n=25) 8 (32.0) 1 ( 4.0)* none* 9 (36.0)**

VI (n=25) 7 (28.0) 3 (12.0) 8 (32.0) 18 (72.0)

*p<0.05 compared with Group VI for moderate and marked peritonitis

**p<0.05 compared with Group VI

582 E WATANABE Vol. 22, No. 5

Table 3. Frequency of ischemic lesions and circumference o f the bowel in each group

Circumference o f Number o f rats Percentage o f rats: Group the bowel with lesions with lesions

(cm, m e a n + SE) (%)

I ( n = 5) 1.94+0.23 none none II ( n = 5) 3.48• none none

III ( n = 5) 4.02+0.26 none none IV (n=lS) 1.89• 1 6.7* V (n=25) 3.68• 9 36.0

VI (n=25) 4.10• 16 64.0

*p<0.05 compared with Groups V and VI **p<0.01 compared with Group VI

4.0

�9 ~ 3.0 _.o

N 2.0-

t.O-

Fig. 4.

_-~- . . . . . . . . . . . . . . -'__; . . . . . . "_ . . . . . . . . . . . . ~ , o

o o e

~ 1 7 6 I ; o

" ~ 3'.0 4.0 510 Circumference of bowel (cm)

Correlation between area o f ischemic lesions and circumference o f the bowel in Group V (�9 Partial colon obstruction with ischemia) and Group VI (O: Complete co lon obstruction with ischemia). All lesions had more than 3.5 cm of bowel circumference. It was noted that all n ine lesions (0.30 + 0.10 cm 2) in Group V and seven lesions o f sixteen animals (0.38 + 0.13 cm 2) in Group VI were less than 1.0 cm 2 and the remain ing n ine lesions (2.31 + 0.39 cm ~) in Group VI were more than 1.0 cm 2 in area (p<0.05). Values are means + SE.

0.13 cm, respectively (Table 3). The a luminum ring made the dilatation of the proximal colon in all animals proport ional to colon obstruc-

tion. The mean circumference of the bowel with the 2 m m ring was 4.10 + 0.08 cm in Group VI, significantly greater than the mean value of 3.68 • 0.08 cm in Group V with the 4

m m ring (p<0.01). Ischemic lesions were

observed in 9 of 25 animals (36.0%) in Group V and 16 of 25 animals (64.0%)t 'nGroup VI as compared with 1 of 15 animals (6.7%) in

Group IV with only colonic ischemia (p<0.05).

In addition, 3 o f 9 animals in Group V and 2 of 16 animals in Group VI had multiple ischemic lesions. No lesions were seen at the

portion of the colon mechanically obstructed

by the a luminum ring in any group. 4. Correlation between area of ischemic

lesions and circumference of the bowel

It was noted that all ischemic lesions in

Groups V and VI were seen in areas o f the bowel with a circumference of more than 3.5 cm (Fig. 4). T h e area of ischemic lesions in

animals with multiple foci was represented as the sum total o f the areas of all lesions. It was

characteristic that the lesions of all 9 animals (0.30 • 0.10 cm ~) in Group V and 7 o f 16 animals (0.38 • 0.13 cm ~) in Group VI were less than 1.0 cm ~, and the remaining 9 lesions (2.31 • 0.39 cm 2) in Group VI were more than

1.0 cm 2 in area (p<0.05).

5. Correlation between area and depth of ischemic lesions

According to the depth of ulceration due to


4.0-

~3,0

=E

"S 2.0

r

1.0

o �9

UI- l UI- II UI" I11 UI - IV

Depth of ischemic lesions

Fig. 5. Correlation between area and depth of ischemic lesions in Group V (O: Partial colon obstruction with ischemia) and Group VI (0: Complete colon obstruction with ischemia). Tissue necroses were observed to reach the mucosa (UI-I), the submucosa (UI-II), the muscularis propria (UI-III) and the serosa (UI-IV). Eleven UI-IV lesions (1.98 + 0.39 cm =) in Group VI were larger than three UI-IV lesions (0.66 + 0.08 cm =) in Group V (p<0.05). It was noted that the depth of ischemic lesions increased gradually as these lesions were extensive. Values are means + SE.

tissue necrosis, ischemic lesions were clas- sified as follows: areas o f tissue necrosis reaching the mucosa, the submucosa, the muscularis propria and the serosa, were clas- sified as Ulcer I (Ul-I), Ulcer II (Ul-II), Ulcer III (Ul-III) and Ulcer 1V (Ui-IV), respectively. The deepest point o f ischemic lesion was con- sidered as the depth of this lesion. About half o f the Group V animals had shallow ulcers (Ul-I, II) as compared with many deeper ulcers (Ul-III, IV) in Group VI (Fig. 5). It was noted that the depth of ischemic lesions in Groups V and VI increased gradually in accordance with the lateral extent of these lesions. Further- more, 11 Ui-IV lesions of 16 animals in Group

VI had lesions with a mean value of 1.98 + 0.39 cm ~ in area, significantly higher than 3 UI-IV lesions of 9 animals with a mean value of 0.66 + 0.08 cm ~ in Group V (p<0.05). Microscopically the ulcerated necrotic area o f the bowel wall was surrounded by a large amount of neutrophil and histiocyte infiltration with beginning fibrosis and edema (Fig. 3c). The regenerating epithelium was seen at the margin of ulcers, partially covering the

base (Fig. 2c).

40!

5 v 3.0-

.',2_

�9 ~ 2.0 "6

L

1.0

Fig. 6.

--o-- o o T o-~-

- ~ - om

oo%,m Mesenteric Almost annur Annular

Situation of ischemic lesions

Correlation between area and situation of ischemic lesions in Group V (O: Partial colon obstruction with ischemia) and Group VI (0: Complete colon obstruction with ischemia). "Mesenter ic" lesions localized at or near the mesenteric base of the bowel. "Almost annular" lesions occupied more than $/, o f the bowel circumference, while "annular" lesions occupied the entire bowel circumference. There were five "annular" lesions (3.18 + 0.35 cm 2) in Group VI, b u t none in Group V. It was noted that ischemic lesions in Group VI extended from the "mesenteric" to the "annular" region whenever these lesions increased in lateral extent (*p<0.01, **p<0.001 compared with "mesenteric" lesions). Values are means +

SE.


Fig. 7.

Partial colon obstruction with ischemia (~b 4ram-sized aluminum ring)

�9 Peristalsis

Moderate distention of bowel

Complete colon obstruction with ischemia (~ 2ram-sized aluminum ring)

, Peristalsis

Marked distention of bowel

Hypothetical representation of the mechanism of producing ischemic colitis associated with the degree of bowel obstruction in this experiment. Periodic propulsive peristalsis may produce a raised intraluminal pressure which strongly impedes the bowel circulation with marked distention of the proximal bowel in complete colon obstruction (Group VI) as compared with partial colon obstruction with ischemia (Group V).

6. Correlation between area and situation of ischemic lesions

ischemic lesions localized at or near the mesenteric base of the bowel were called "mesenteric". Lesions occupying more than 3/4

or the entire bowel c ircumference were termed "almost annular" or "annular", respectively (Fig. 6). "Mesenteric" lesions were found in 8 of 9 cases (0.24 + 0.09 cm ~) in Group V (Figs. 2a, b) and 8 of 16 cases in Group VI. On the

o ther hand, "annular" lesions accounted for 5 of 16 animals in Group VI (Figs. 3a, b), but none in Group V. It was noted that ischemic lesions in 'Group VI extended f rom the "mesenteric" to the "annular" region in accordance with t h e lateral extent o f these

lesions. These mean values were as follows:

0.44 + 0.14 cm ~ in the "mesenteric" lesions, 1.29 _ 0.09 cm 2 in the "almost annular" lesions and 3.18 + 0.35 cm 2 in the "annular" lesions.

Discuss ion

Ischemic colitis proximal to acute obstruc-

tion of the bowel in rats was produced by

app l ica ton of the a luminum ring in a distal portion of artificial colonic ischemia. Only ligadon of the bowel vessels which supply the

left hemi-colon rarely caused ischemic colids, but through the use of the a luminum ring together with such colonic ischemia, a high rate of ischemic colitis was induced. In 1966,

Glotzer et al. 17) presented the first experimental model o f obstructive colitis in dogs using surgical tape, but this took a relatively longer dme, i.e., 11 days to 5 months to produce ischemic lesions. Furthermore, the

inflammatory changes of the colon proximal to the obstruction did not seem to depend on

the degree of bowel distention. On the other hand, the present experiment in which find-

ings were observed four days after the surgical procedure showed that the bowel distention of complete colon obstruction was more dilat- able in the proximal ischemic region and

frequently led to severer ischemic colitis than that of partial colon obstruction.

Reports o f ischemic lesions observed in the

proximal area of colon carcinoma are rare, but the occurrence of these lesions has re-

cently increased 2) as the incidence of colon

carcinomas has increased progressively. These lesions have been variously termed as "gangrene ''~2-~4), "acute necrotizing colitis ''25-~'), "ulcerative colitis"~s, 29), "ulcerating colitis ''s~

"acute proximal ulcerative colitis ''sl), "pseudo-

ulcerat ive colitis ''32), " p s e u d o m e m b r a n o u s colitis ss~ or enterocolitis ''s4), "colitis ''ss,sS), "ob-

structive colitis 1~,s7) or "enterocolitis ''ss), "is-


chemic colitis ''2,sg-4s), "colonic ulceration ''44-48), "ulcerative disease '''7,*s), "ischemic lesions ''4~) and "infarction ''~~ It is obvious that these ischemic lesions proximal to colon carcinoma are analogous ~,29,s~,sg,41,49) to ischemic colitis proposed by Marston et al. 11, since the clinical, radiologic, and microscopic appearances re- semble another. The left side of the colon is the preponderant portion of i~chemic colitis associated with colon carcinoma 2) with occa- sional invasion to the pelvic cavity and the retroperitoneum in man. Therefore, this experimental model of ischemic colitis with obstruction and fixation at the distal portion of the left colon would reflect the clinical state of advanced colon carcinoma physiologically.

The effect of luminal distention on the regional blood flow of the intestine has been amply described. Many authors s-s,l~ ex- plained that the bowel circulation would be considerably disturbed by higher intraluminal

pressure due to mechanically inflated air or fluid. On the other hand, bowel distention by less than 30 mm Hg of intraluminal pressure may affect the bowel c i rcula t ion slight- ly ~,7,n,~4,~6~ or transiently sll. Furthermore, the blood circulation of the colon is less sus- ceptible to bowel distention than that of the small intestine at the same pressure 5,1nl. Wan- gensteen 9~ reported sustained pressures between 12 and 52 cm H~O in acute colon obstruction in human beings. Alternatively it has been demonstrated that bowel motility might be intimately related to intraluminal pressure ~ The motility of the colon in human beings was grouped into four patterns according to Code et al.~a); normal patterns consisting of type I, II and III waves can be seen in a healthy state, but type IV wave in a pathological state such as ulcerative colitis. On the other hand, the motility of the small intestine was grouped into two patterns; type I wave being the pendular movement and type

III wave being the propulsive movement. Active peristalsis of the dilated segment due to mechanical obstruction was observed to con- tinue until the end stage in the small intestine 9,19,53), regardless of association with peritonitis 5~1. Under these conditions, the propulsive movement is said to be prominent, but the pendular movement was inactive. However, the type of motility in the obstructed colon has not yet been identified. Periodic spontaneous burst of modlity is said to be an etiologic factor of ischemic colitis proximal to colon obstruction 1~), since it may produce a segmental high pressure which results in a decrease of blood flow of the dilated bowel. Therefore, from the result of this experiment it can be postulated that the periodic propulsive peristalsis may produce a raised intraluminal pressure which induces a remarkable distention of the proximal bowel and strongly hampers its blood circulation in complete colon obstruction as compared with partial colon obstruction with ischemia (Fig. 7).

Bowel movement transports the intestinal content through the ileocecal valve from the ileum into the cecum without any reflux. Colon obstruction in man and animals often results in a closed loop since the ileocecal valve is normally competentg,~~ It is commonly said that the circulation of the intestinal mucosal layer may be more influenced by bowel distention than that of the external layers~~ Therefore, increasing pressure into the closed loop may disturb the mucosal circulation and subsequently lead to massive gangrene of the colon if the cecum does not rupture. The initial point of ischemic change of the dilated bowel begins at the anti- mesenteric side 4,9~. In addition, in this experiment, the area ofischemic colitis was observed to extend from the mesenteric side to the annular region as the depth of these lesions increased in both the partial and complete


colon obstruction with ischemia groups. The method by which the image analysis system for morphometry measured the area o f ischemic lesions appeared to be more accu- rate than that reported previously 541.

It has been said that there is no difference in quality or quantity of bacterial flora whether the colon was obstructed or notl'k However, since the permeability and viability of marked- ly dilated bowels usually diminished ~,4~ regional bacterial proliferation might have another important role in the pathogenesis of ischemic colitis 25,sl,351. Teasdale et alY ) suggested that acute necrotizing colitis proximal to colon carcinoma was possibly due to an anaerobic organism (clostridia) although this was not proven by culture.

An experimental model of acute ischemic colitis in rats was produced by the installation of different aluminum rings with a segmental devascularization of the left hemi-colon to clarify the pathophysiology of this disease. Complete colon obstruction in comparison with partial co lon obstruction frequently caused severe ischemic colitis together with marked distention of the proximal bowel under a precarious circulatory state. Clinically, attention should be paid to the possible occurrence of ischemic colitis proximal to colon carcinoma, especially in cases showing remarkable distention due to the extreme bowel obstruction.

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quantitative evaluation of experimental ischemic colitis correlated with the degree of artificial...

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