ANGIODYSPLASIA ANGIOG AJR 1977

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Am J Rontg.nol 129:789-794, Nevembr 1977 789
Angiodysplasia of the Right Colon: A Cause of Gastrointestinal Bleeding
STANLEY BAUM,1’2 CHRISTOS A. ATHANASOULIS,1 ARTHUR C. WALTMAN,1 JAMES GALDABINI,3
ROBERT H. SCHAPIRO,4 ANDREW L. WARSHAW,5 AND LESLIE W. OTTINGER5
Thirty-four patients with Intermittent lower gastrointestinal
bleedIng were diagnosed anglographically as having anglo-
dysphasla of the cecum and rIght colon. Repeated barIum and
endoscopic examinatIons were negative. Right colectomy was
performed on 17 patIents, who were followed postoperatively
for up to 7 years. Of these, four patlentes rebled, two of whom
had anglographic evidence of related lesions Involving other
parts of the colon and terminal Ileum. SIlIcone rubber InjectIon
and tissue-clearIng techniques on the specimens have faclhl-
tated the pathologic IdentIficatIon of these lesions. Hlstologl-
cally, they are dIlated submucosal veins and arterIes assocl-
ated wIth areas of overlying mucosal thInnIng and occasional
ulcerations. Although the pathogenesls of the lesIon Is un-
known, we think they are acquired rather than congenItal and
result from chronic submucosal arterlovenous shunting sec-
ondary to mucosal Ischemla. Of the 34 patIents, 17 had a
hIstory of cardIac disease.
Vascular ectasia or angiodysphasia of the right colon is
being recognized with increasing frequency in patients
with lower gastrointestinal hemorrhage of unexplained
etiology [1-10]. Typically, these patients are elderly and
present with either chronic low-grade or intermittent
acute massive lower gastrointestinal bleeding. Because
the lesions are small and focal in distribution, they can-
not be detected by conventional barium studies of the
bowel, and are only rarely seen with cohonoscopy. The
surgeon almost never finds these lesions at laparotomy,
and the pathologist has difficulty demonstrating them
unless guided by preliminary specimen injections [4, 9,
10]. This report describes our clinical experience with
this lesion and emphasizes the diagnostic importance of
mesenteric arteriography in patients with chronic lower
gastrointestinal blood loss.
Subjects and Methods
The angiographic diagnosis of cecal and ascending colon
angiodysplasia was made in 34 patients studied over the past 7
years. Twenty of these patients were examined within the past 2
years. The 19 women and 15 men ranged in age from 50 to 81
years (average, 64). Seventeen patients had a history of previous
cardiac disease: nine had aortic stenosis, three had combined
valvular disease, and five had atherosclerotic coronary vascular
disease.
Superior mesenteric arteriography was performed using 50-
60 ml of meglumine diatrozoate injected at 5-6 mI/sec. Rapid
serial radiographs were exposed over a sufficient time (30 sec)
to include the arterial, capillary, and venous phases of the
arteriogram. In some cases, the colon was distended with air
immediately prior to the injection. The left colon was examined
with inferior mesenteric artery injections to exclude other p0-
tential sources of bleeding. Direct serial magnification was uti-
hized to portray smaller vessels in the cecum and any other areas
which were not well demonstrated in the initial arteriograms.
Subselective catheterization of the branches of the mesenteric
artery was not routinely performed . (Catheterization of relatively
small vessels can result in partial obturation of the catheter in
the origin of the ileocolic or right colic artery, and when this
occurs, early venous opacification can be artifactually induced.)
The angiographic diagnosis of angiodysplasia was based on
the following findings:
1 . Abnormal clusters of small arteries seen during the arterial
phase of the arteriogram along the antimesenteric border of the
cecum and the ascending colon (fig. 1).
2. Accumulation of contrast material in vascular spaces and
intense opacification of the bowel wall during the capillary
phase (fig. 2).
3. Early opacification of the veins draining the cecum and the
ascending colon (fig. 3).
4. Intense opacification of the veins persisting hate into the
venous phase (fig. 1).
Based on these angiographic findings, laparotomy was per-
formed on 24 of the 34 patients.
The resected specimens from 15 patients were injected with a
silicone rubber compound (Microfil, Canton Medical Products,
Boulder, Cob.). Immediately upon resection of the specimen, a
cannula is placed in the ileocolic artery and/or right colic artery,
depending on the length of the specimen. After irrigation with
heparinized saline, the radiopaque silicone rubber compound is
injected by gentle manual pressure. Depending on the size of
the specimen, 50-100 ml of solution may be needed for com-
plete filling of the vascular tree. The specimen is subsequently
refrigerated for 24 hr to allow complete polymerization of the
silicone rubber.
After the 24 hr refrigeration, the specimen is bivalved. Gross
examination ensues, and a magnification radiograph is ob-
tamed to facilitate localization of the lesion in the injected
specimen. The specimen is then fixed in formahin and subjected
to a clearing procedure. This involves dehydration of the speci-
men with increasing concentrations of alcohol (40%, 60%, 80%,
and 100% for 24 hr intervals each) and subsequent immersion in
methylsahicylate which has the same defraction index as the
dehydrated tissue. The cleared specimens are viewed under a
dissecting microscope and the lesions identified.
Once the lesions have been recorded and photographed, the
dehydration process is reversed. The specimen is then sent for
Received November 5, 1976; accepted after revision June 30, 1977.
This work was supported in part by U.S. Public Health Service grants AM-16026-03 and 777-7764-5.
S Department of Radiology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts 02114.
Present address: Department of Radiology, Hospital of the University of Pennsylvania, 3400 Spruce Street, Philadelphia, Pennsylvania 19104.
Address reprint requests to S. Baum.
Department of Pathology. Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts 02114.
Department of Medicine, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts 02114.
Department of Surgery, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts 02114.
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Fig. 1 .-Angiodysplasia of cecurn in 71-year-old man with recurrent rectal bleeding. A, Late arterial film from superior mesenteric arteriogram
showing accumulated contrast material in vascular spaces (arrow) with surrounding abnormal clusters of small arteries. B, venous phase showing
retention of contrast material in vascular spaces. Note dense venous opacification.
790 BAUM ET AL.
pathologic sectioning with a pin or pins marking the exact
location.
Results
Ten of the 34 patients with the angiographic diagnosis
of right colonic angiodysplasia were treated medically
since the bleeding was not severe enough to require
surgical intervention. Low grade rectal bleeding has con-
tinued in all of these patients.
Surgery was performed in the remaining 24 patients. At
haparotomy, previously undiagnosed lesions constituting
“alternative explanation” of hemorrhage were found in
seven patients. Two had carcinoma of the cecum and
one each had segmental right colitis, heiomyosarcoma of
the iheum, carcinoma of the pancreas, metastatic ana-
plastic carcinoma, and a duodenal ulcer. With the excep-
tion of the two cecal carcinomas, the right colon was not
resected in this group of patients. The angiographic di-
agnosis of angiodysplasia could therefore not be con-
firmed.
In both cases of carcinoma of the cecum and the case
of segmental colitis, the angiographic locationof angio-
dysphasia corresponded to the area of pathology. These
cases presumably represent errors of angiographic diag-
nosis. The patients with ileal heiomyosarcoma, pan-
creatic carcinoma, and anaplastic metastatic carcinoma
died within months of surgery and their right colon was
not examined. The patient with the duodenal ulcer has
continued to bleed despite subtotal gastrectomy and
vagectomy.
In the remaining 17 patients, haparotomy failed to dem-
onstrate any gross abnormality, and a right hemicolec-
tomy was performed on the basis of the angiographic
findings. Thirteen of these patients have not rebled post-
operatively during follow-up periods ranging from 8
months to 7 years. The remaining four patients contin-
ued to bleed following surgery. Two of the four had
postoperative arteriograms which suggested similar le-
sions in the remaining segments of the colon which were
not appreciated on the earlier examinations. No further
surgical resections were performed on these patients,
however, and the nature of the angiographic findings
remains unclear.
Discussion
The clinical manifestation of cohonic vascular ectasia
or angiodysplasia has been described as intermittent low
grade lower gastrointestinal bleeding [1-5]. However,
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Fig. 2.-Angiodysplasia of cecum and ascending colon in 75-year-old woman with recurrent rectal bleeding, negative barium enemas, and negative
colonoscopy. A, Arterial phase of selective superior mesenteric arteriogram demonstrating abnormal clusters of small arteries in cecum and ascending
colon (white arrowheads) associated with early draining veins (black arrowheads). B, Late arterial and early capillary phase showing dense opacification
of early filling veins draining cecum and distal ascending colon (arrowheads). Right colectomy extending from cecum to distal transverse colon, was
performed; rectal bleeding has not recurred during 18 months postoperative follow-up.
COLONIC ANGIODYSPLASIA 791
half of our patients presented with acute episodes of
massive rectal bleeding. In most of these patients, the
stool became guaiac negative between the episodes of
hemorrhage.
The incidence of colonic angiodysplasia among var-
ious age groups is difficult to assess. The first descrip-
tion of this entity was recorded in 1839 [11]. Bently [12]
collected 234 cases from the literature since 1949 and
added 110 from the Mayo Clinic files. However, these
reports include a variety of vascular abnormalities of the
intestines, such as congenital arteriovenous malforma-
tions and/or vascular tumors. Since 1960 when Margulis
et al. [13] introduced operative angiography as a tool in
the search of gastrointestinal bleeding sites and 1965
when Baum et al. [14] introduced selective angiography
for the preoperative localization of bleeding sites, the
unique character of colonic angiodysplasia has been
recognized. The lesions have been reported in many
patients with otherwise unexplained gastrointestinal
hemorrhage [1, 10]. One study using vessel injection
techniques on autopsy specimens demonstrated colonic
angiodysplasia in 2% of asymptomatic elderly patients
[15].
Colonic angiodysplasia may coexist with other lesions
of the gastrointestinal tract. This certainly was the case
in seven of our patients, who at exploration were found
to have other previously undiagnosed lesions. Although
angiodysplasia cannot be detected with x-ray barium
studies and only rarely by colonoscopy, these examina-
tions assume great diagnostic importance since other
lesions must be excluded before a right hemicolectomy
is undertaken for angiodysplasia.
Because hemorrhage from angiodysplasia may be epi-
sodic rather than continuous, most patients are not stud-
ied during periods of active bleeding. Thus specific lo-
calization of a bleeding site, shown by the extravasation
of contrast media, is the exception rather than the rule.
Since the surgeon can neither see nor palpate the
colonic angiodysplasia, the decision to resect the as-
cending and proximal transverse colon is generally made
on the basis of preoperative angiographic findings. This
difficulty in detecting angiodysplasia at laparotomy may
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..,‘. =. ,
�
Fig. 3.-Angiodysplasia of cecum in 69-year-old man with intermittent
episodes of acute lower gastrointestinal hemorrhage. Late arterial phase
of superior mesenteric arteriogram demonstrating abnormal clusters of
arteries in cecum (arrows) and intense opacification of early draining vein
(curved arrow).
792 BAUM ET AL.
account for the 53% incidence of negative explorations
and 17% incidence of explorations with indeterminate
findings in patients undergoing surgery for gastrointes-
tinal bleeding of obscure origin [16]. It is likely that the
“cecal erosions” and “benign ulcers of the cecum” re-
ported in the past as the sources of unexplained bleeding
may represent angiodysplasia associated with overlying
mucosal thinning and ulceration [17, 18].
Pathologic identification of these lesions in the re-
sected specimen is difficult because the lesions are small
and focal, and serial sections of the entire specimen are
not practical. Injection of the right colic artery with sili-
cone rubber is helpful, since this material causes the
vessels to remain distended during the tissue fixation.
Since the silicone rubber used can be made radiopaque,
magnification radiographs of the specimen may also be
obtained. After the dehydration and tissue-clearing pro-
cess, the specimen may be viewed under the dissecting
microscope. Normal colonic mucosa appears as a hon-
eycomb network of mucosal capillaries. Angiodysplasia
appears as a conglomeration of vascular spaces, often
multiple, often coalescent, with adjacent arteries and
veins standing as “coral reefs” against the homogene-
ous surface of the normal cohonic mucosa (figs. 4A-4C).
Histologically, the dilated vascular spaces correspond
to thin-walled channels in the submucosa. Small
amounts of smooth muscle may be present in the walls of
some of these channels, but in most instances they are
lined only by endothehium [19] (fig. 4D). The channels
appear to represent clusters of dilated thin-walled veins
similar to those described in 1956 by Rutter [20] in his
report of a patient with ‘ ‘submucosal telangiectasis of
the colon.”
The apparent association of vascular malformations or
angiodysphasia of the colon with hemorrhage in patients
with aortic stenosis has been controversial [6, 21-26].
Williams [23] found a high incidence (25%) of aortic
stenosis among patients with unexplained gastrointes-
tinal bleeding, while McNamara and Austen [25] reported
that patients with valvuhar disease did not have a striking
propensity for gastrointestinal bleeding. More recently,
Cody et al. [27] reported an incidence of 2.6% of idi-
opathic gastrointestinal bleeding in patients with aortic
stenosis, an incidence significantly higher (pectasias
represent congenital arteriovenous malformations, espe-
cially since they are seen almost exclusively in older age
groups and are not associated with arteriovenous mal-
formations in other parts of the body. If the vascular
supply of the gut is thought to consist of separate mu-
cosal, submucosal, and muscular components, it is un-
derstandable that factors capable of decreasing mucosal
blood flow need not interfere with submucosal flow.
There may actually be an inverse relationship between
the amount of perfusion of the mucosa and quantity of
blood flowing in the submucosa [28].
Mechanical factors producing a sustained or intermit-
tent elevation in the intraluminal pressure may signifi-
canthy interfere with mucosal blood flow. Injection stud-
ies of the bowel show that there is a decrease in mucosal
blood flow under conditions of increased intrahuminal
pressure associated with an increase in submucosal flow
[29]. It has been experimentally shown that transient
increases in intraluminal pressure capable of causing
submucosal arteriovenous shunting may occur in other-
wise healthy individuals during episodes of partial bowel
obstruction associated with peristalsis or straining at
stool. The net effect of these pressures may be further
increased by rises in the intraabdominal extraenteric
pressures that occur during defecation. It is tempting to
speculate that the submucosal vascular ectasias are ac-
tually a result of chronic submucosal arteriovenous
shunting, therefore representing a chronic form of is-
chemic bowel disease [30].
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Fig. 4.-Pathologic specimens demonstrating microvascular anatomy of angiodysplasia of cecum.A, Photograph (x40) of angiodysplasia as viewed
under dissecting microscope after silicone rubber injection into right colic artery and tissue clearing with methylsalicilate. Note large feeding arteries
and draining veins in submucosa. B, Another angiodysplasia seen as cluster of tortuous and dilated vessels against homogenous background of normal
colonic mucosa. c, Photograph after use of more viscous silicone rubber preparation. Only arteries and veins are opacified. D, Histologic section (x40)
of cecal angiodysplasia. Note collection of large thin-walled vascular channels in colonic wall, predominantly in submucosa. Smaller thin-walled
channels distort adjacent mucosa.
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794 BAUM ET AL.
The basic initiating mechanism of nonocclusive mes-
enteric ischemia has long been thought to be an intense
peripheral vasoconstriction and redistribution of
sphanchnic blood flow secondary to low cardiac output.
This may partially explain the high incidence of angio-
dysphasia in patients with valvular heart disease.
If chronic increases in intrahuminal pressure are con-
sidered a possible etiology, the right colon would be a
logical location for the development of these lesions. In
keeping with Laplace’s law, the increased diameter of
the right colon would account for a higher mural tension.
This is certainly true in patients with distal cohonic ob-
struction who present with cecal rupture.
On the basis of the available information, our current
approach to the management of lower gastrointestinal
bleeding in patients with an angiographic diagnosis of
right cohonic angiodysphasia is as follows. If conventional
barium examinations of the bowel and colonoscopy fail
to reveal any lesions in the gastrointestinal tract, and if
the bleeding is sufficiently severe or recurrent, we rec-
ommend surgery on the basis of the angiographic find-
ings. At the time of laparotomy, if no lesion is found to
account for the gastrointestinal bleeding , a right hemico-
lectomy should be performed.
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