AJR 2000; 175:1439-1444
© American Roentgen Ray Society
CT of Patients with Right-Sided Colon Cancer and Distal Ileal Thickening
Ah Young Kim1,
Hyun Kwon Ha1,
Bo Kyoung Seo1,
Eun-Sil You2,
Kyoung Sik Cho1,
Pyo Nyun Kim1,
Moon-Gyu Lee1,
Hoon Yong Jeong3,
Suck Kyun Yang3 and
Young II Min3
1
Department of Diagnostic Radiology, Asan Medical Center, University of Ulsan
College of Medicine, 388-1, Poongnap-Dong, Songpa-Ku, Seoul, 138-736,
Korea.
2
Department of Pathology, Asan Medical Center, University of Ulsan College of
Medicine, Seoul, 138-736, Korea.
3
Department of Gastroenterology, Asan Medical Center, University of Ulsan
College of Medicine, Seoul, 138-736, Korea.
Received February 21, 2000;
accepted after revision April 26, 2000.
Address correspondence to H. K. Ha.
Abstract
OBJECTIVE. The purpose of this study was to analyze the incidence
and primary causes of distal ileal wall thickening in 131 patients with
right-sided colon cancer.
SUBJECTS AND METHODS. During a 2-year period, 131 patients underwent
surgical resection for right-sided colon cancer. Of these patients, we
analyzed 13 who had distal ileal wall thickening on CT before surgery and also
had the cause determined at pathology. CT findings were analyzed with regard
to the morphologic features of colonic tumors, bowel wall involvement patterns
of the distal ileum, and changes in the pericolic space.
RESULTS. Distal ileal wall thickening occurred in 13 (10%) of the
131 patients who had right-sided colon cancer. Three patients had polypoid
colon cancer, whereas the other 10 had infiltrative colon cancer. The mean
thickness of the involved colonic segments was 1.6 cm (range, 1.0-2.2 cm) with
a mean length of 5.2 cm (range, 2.5-10.0 cm). Pericolic infiltration was mild
in six patients and moderate in four patients. The mean length and thickness
of the affected ileal segments were 3.2 cm (range, 1.5-6.0 cm) and 1.1 cm
(range, 0.7-2.0 cm), respectively. On histopathologic examination, neoplastic
processes involved the distal ileum in nine (69%) of the 13 patients. This
involvement was caused by either direct tumor invasion in seven patients or
lymphatic spread in two. In four patients (31%), nonneoplastic processes with
edema and congestion involved the distal ileum.
CONCLUSION. The distal ileum may be abnormally thickened in about
10% of patients with right-sided colon cancer; this thickening results from
tumor extension (69%) or a nontumorous process (31%).
Introduction
As shown by other researchers
[1,
2], the colon proximal to an
obstructing colon cancer can become thickened because of ischemic changes
associated with bowel distention. However, to our knowledge, there are few
reports regarding the changes in the distal ileum in patients with colon
cancer, especially of the cecum or ascending colon
[3]. When the wall of the
distal ileum is thickened in patients with known colon cancer, it is unclear
whether this thickening represents a neoplastic or nonneoplastic process.
Moreover, if the CT reviewers do not know a patient's colon cancer history,
the presence of both colonic and distal ileal wall thickening might be
misinterpreted as another neoplastic or inflammatory condition, such as
lymphoma or inflammatory bowel disease.
According to previous reports
[4,
5], the incidence of distal
small-bowel involvement is much lower in colon cancer than that in lymphoma or
chronic inflammatory bowel diseases; in patients with primary colonic
lymphoma, the literature indicates that concomitant involvement of the distal
ileum is as frequent as 27-38%
[5]. The lower incidence of
distal ileal involvement in colon cancer may occur because the tumor usually
does not extend beyond an anatomic barrier such as the ileocecal valve.
The purpose of this study was to determine the incidence and causes of
distal ileal thickening in patients with right-sided colon cancer.
Subjects and Methods
From a review of the surgical records at our institution, we collected data
on 131 patients who had undergone both right hemicolectomy and partial
resection of the distal ileum due to colon cancer between September 1997 and
August 1999. A retrospective review of the preoperative CT scans of these 131
patients revealed 15 patients in whom the distal ileal wall was thickened.
Pathologic review after surgery of the distal ileum in these 15 patients
revealed positive findings in 13 and negative findings in the other two.
Therefore, these 13 patients provided the basis for our study. There were four
women and nine men (age range, 28-70 years; mean age, 56 years). The duration
between preoperative CT and surgical resection was 3-22 days (mean duration, 8
days).
We performed CT with commercially available equipment (Somatom Plus-S,
Plus-4, and Plus-40; Siemens, Erlangen, Germany), using an 8- or 10- mm slice
thickness at 8- or 10-mm intervals from the diaphragm to the symphysis pubis.
All patients routinely received both oral and IV contrast material. All
patients drank 600 mL of 2% barium sulfate suspension (E-Z-Cat; E-Z-Em,
Westbury, NY) 1 hr before scanning and an additional 300 mL just before the
examination. Contrast-enhanced CT was performed after a bolus injection of
100-120 mL of IV contrast material (Ultravist; Schering, Berlin, Germany) at a
rate of 3.0 mL/sec. Scanning was initiated 65 sec after the start of the
injection. Among these patients, we performed 5-mm thin-section helical CT
with a pitch of 1.0, focusing on the lower abdomen after an injection of IV
contrast material.
All CT scans were analyzed with regard to the location, length, thickness,
type (polypoid/infiltrative), and contrast-enhancement pattern
(homogenous/heterogeneous) of each colon cancer; the degree of pericolic
infiltration; and the presence or absence of lymphadenopathy and regional
vascular engorgement. CT scans of the ileum were evaluated for the thickness,
length, and contrast-enhancement pattern of all affected segments and for the
presence or absence of bowel obstruction and ileocecal valve involvement.
Target was considered present when the thickened bowel wall showed
multilayered concentric enhancement. The degree of pericolic infiltration was
considered mild when infiltration was less than 1 cm from the outer margin of
the involved colonic segment, it was moderate when infiltration was from 1 to
2 cm, and it was considered severe with infiltration of greater than 2 cm. The
thickness of the distal ileal wall was considered diseased on CT when it
exceeded 5 mm [6]. The lymph
nodes were considered enlarged when they exceeded 6 mm in the shortest axis
diameter [7,
8]. The mesenteric vessels were
engorged when they exceeded 3 mm in diameter or were in an area of localized
increase in the number of vessels
[9]. Small-bowel obstruction
was considered present when small-bowel loops were diffusely dilated and had a
diameter of greater than 2.5 cm
[10]. Two experienced
radiologists reviewed CT scans in consensus.
The pathologist reviewed the pathologic slides regarding the presence or
absence of distal ileal disease. However, she was blinded to the CT
interpretation.
After the primary causes of distal ileal wall thickening were determined by
pathologic review, the CT features of patients with neoplastic ileal
involvement were compared with those of patients with nonneoplastic ileal
thickening.
Results
On CT, colon cancers were located in the ascending colon in one patient, in
the cecum in four, and in both in eight. The tumors were 5.2 cm in mean length
(range, 2.5-10.0 cm), and the mean thickness of the involved colonic segments
was 1.6 cm (range, 1.0-2.2 cm). The tumor types were polypoid in three
patients and infiltrative in the other 10 patients. The colonic tumors
enhanced homogeneously in six patients and heterogeneously in seven; one of
the seven patients who showed heterogeneous enhancement showed the target sign
with a marked enhancing inner layer and a poorly enhancing outer layer.
Pericolic infiltration was absent in three patients, mild in six, and moderate
in four.
The mean length of the affected distal ileal segment was 3.2 cm (range,
1.5-6.0 cm) and the mean bowel wall thickness was 1.1 cm (range, 0.7-2.0 cm).
These ileal segments enhanced homogeneously in 10 patients (Fig.
1A,1B,1C)
and heterogeneously with a target sign in the other three patients (Fig.
2A,2B,2C).
The mean thickness of the ileocecal valve was 11.5 mm (range, 6-20 mm).
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Fig. 1A. —70-year-old man with right-sided colon cancer invading distal ileum.
Contrast-enhanced CT scan shows homogeneous enhancement of distal ileal wall
thickening (straight arrow) and mesenteric vascular engorgement
(curved arrow), which is associated with polypoid mass (m) involving
ascending colon and cecum.
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Fig. 1B. —70-year-old man with right-sided colon cancer invading distal ileum.
Contrast-enhanced CT scan shows moderate pericolic infiltration (solid
arrows) and continuous concentric distal ileal wall thickening (open
arrows).
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Fig. 1C. —70-year-old man with right-sided colon cancer invading distal ileum.
Photomicrograph of histopathologic specimen of distal ileum shows subserosal
tumor invasion (arrows) from primary colon cancer (C) and prominent
submucosal edema (SM). (H and E, x 100)
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Fig. 2A. —63-year-old man with right-sided colon cancer spreading to distal
ileum. Contrast-enhanced CT scan shows infiltrative right-sided colon cancer
(M), which is accompanied by heterogeneous enhancement of distal ileal wall
thickening (arrows).
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Fig. 2C. —63-year-old man with right-sided colon cancer spreading to distal
ileum. Photomicrograph of histopathologic specimen of distal ileum reveals
subserosal lymphatic spread of tumor cells (arrow) and marked
subserosal edematous swelling (SS). Note lymphoid follicle (F). (H and E,
x 10)
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Lymphadenopathy was shown in 10 (77%) of our 13 patients (Fig.
3A,3B);
pericolic lymphadenopathy, in three; ileocecal lymphadenopathy, in five; and
both, in two. Vascular engorgement of the adjacent mesenteric vessels was
shown in seven patients (54%) (Fig.
4A,4B,4C),
and small-intestine obstruction was seen in four (31%) (Figs.
3A,3B,4A,4B,4C,5A,5B,5C).
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Fig. 3A. —63-year-old man with right-sided colon cancer invading distal ileum.
Contrast-enhanced CT scan shows infiltrative cecal tumor invading ileocecal
valve (curved arrow). Note ileocecal necrotic lymphadenopathy
(solid arrows) and mesenteric vascular engorgement (open
arrow).
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Fig. 3B. —63-year-old man with right-sided colon cancer invading distal ileum.
Contrast-enhanced CT scan shows contiguous irregular bowel wall thickening of
adjacent distal ileum (arrows) beyond ileocecal valve with
small-bowel obstruction (asterisk). Pathology report of resected
distal ileum after surgery revealed direct tumor invasion from cecal tumor
through thickness of small-bowel wall.
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Fig. 4A. —58-year-old man with cecal tumor invading distal ileum.
Contrast-enhanced CT scan shows cecal mass (C) invading ileocecal valve
(curved arrow) and engorged ileocecal vessels (open
arrows).
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Fig. 4B. —58-year-old man with cecal tumor invading distal ileum.
Contrast-enhanced CT scan shows targetlike layered enhancement of distal ileal
wall thickening (arrows) and small-bowel obstruction
(asterisk).
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Fig. 4C. —58-year-old man with cecal tumor invading distal ileum.
Photomicrograph of histopathologic specimen of thickened distal ileal segment
reveals lymphatic permeation (arrows) by carcinoma cells in all
layers, including submucosal (sm), subserosal (ss), and muscular (m) layers.
(H and E, x 100)
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Fig. 5B. —60-year-old woman with cecal cancer and obstructive ischemic
ileitis. Contrast-enhanced CT scan reveals irregular distal ileal wall
thickening (arrows), which shows homogeneous enhancement.
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Fig. 5C. —60-year-old woman with cecal cancer and obstructive ischemic
ileitis. Resected specimen shows cecal mass (M) invading ileocecal valve
(arrow) with submucosal edema and patchy congestion of distal ileum
(IL). No evidence of microscopic cancer—cell infiltration into
small-bowel segment was seen.
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Histopathologically, distal ileal involvement was caused by a neoplastic
process in nine patients (69%); the tumor cells were predominantly seen in the
submucosal layer of the ileal wall in two, in the subserosal layer in three,
and in all layers in the remaining four patients. Tumor spread in these
patients was by way of direct tumor invasion in five patients (Fig.
1A,1B,1C),
by lymphatic spread in two (Figs.
2A,2B,2C
and
4A,4B,4C),
and by both modes in two patients. In the four remaining patients (31%), ileal
wall thickening was caused by congestion and edema without tumor-cell
infiltration (Fig.
5A,5B,5C).
In the four patients with small-bowel obstruction, ileal wall thickening was a
neoplastic process in three and a nonneoplastic process (congestion and edema)
in one.
When comparing the CT features of patients with neoplastic ileal thickening
and those of patients with nonneoplastic ileal wall thickening, we found that
the group with neoplastic ileal involvement had larger tumors, longer affected
segments, more severe involvement of the ileocecal valve, and a higher
incidence of lymphadenopathy, vascular engorgement, small-intestinal
obstruction, and pericolonic infiltration than the group with nonneoplastic
ileal thickening. However, statistical analysis could not be obtained because
of the limited number of patients.
Discussion
Our study showed that the distal small bowel was affected in 10% of
patients with right-sided colon cancer. The distal ileum was affected by two
major disease processes (i.e., the neoplastic process by direct tumor invasion
or lymphatic spread and the nonneoplastic process with congestion and edema).
The incidence of neoplastic involvement (n = 9) was higher than that
of non-neoplastic involvement (n = 4). Direct tumor invasion appears
to be related mainly to whether the tumor involves the ileocecal valve and to
tumor size; in other words, distal ileal involvement occurs when a tumor grows
sufficiently to invade the ileocecal valve.
Theoretically, tumors may invade the small intestine indirectly by
implanted lesions in the pericolonic or perienteric spaces, but we have not
experienced such cases. As shown by other researchers
[3,
11], lymphatic spread also
plays a role in the neoplastic involvement of the distal ileum. These patterns
of tumor spread are similar to those of tumor extension of gastric cancer into
the duodenum and esophagus; according to pathology reports
[12,
13], 11-25% of gastric cancers
show duodenal extension microscopically, with the tumor extension developing
first in the submucosal or subserosal lymphatics and extending outward into
the lymphatics in the muscle layers. The lymphatic spread of colon cancer
takes place through the submucosal, muscularis propria, and subserosal
lymphatics. Tumor cells then spread in order through the epicolic, paracolic,
intermediate, and principal nodes
[14]. However, complete
blockage of a more remote node can occur from cellular impaction, with
retrograde passage along other afferent channels to involve a segment of bowel
adjacent to, or at some distance from, the primary carcinoma
[15]. In its initial stages,
the deranged lymph flow may be radiologically shown as edema in the bowel wall
and is often mistaken for inflammatory bowel disease
[3,
11].
In four patients with colon cancer (31%), distal ileal wall thickening
resulted from nonneoplastic processes, such as submucosal edema and congestion
with some perivascular fibrotic changes. According to previous reports
[2,
16], the colon proximal to a
primary colon cancer can be thickened because of ischemic colitis in 1-7% of
patients; the principle cause of ischemia is thought to be the proximal
colonic distention caused by bowel obstruction. Likewise, we assume that if
the ileocecal valve is incapacitated in cases of colonic obstruction, the
small intestine, especially the distal ileum, may be affected by increased
intraluminal pressure and bowel ischemia may subsequently develop. However,
other factors may contribute to the development of the nonneoplastic distal
wall thickening. First, focal ischemia can develop in the distal ileum when
the peripheral branches of the ileocolic vessels are encased by pericolic or
perienteric tumor infiltration. Second, as mentioned previously, we observed
that the distal ileum can become thickened because of the accumulation of
lymphatic fluid caused by blockage of the surrounding lymphatic channels. In
addition, like our two patients who were excluded from this study because of
no demonstrable pathologic alteration, distal ileal wall thickening might be a
false-positive CT finding; in patients with a mildly thickened wall, the bowel
might be interpreted as normal on pathologic examination because of shrinkage
of edematous tissues during fixation and dehydration of the resected surgical
specimen.
As shown in one series by Ko et al.
[1], the bowel wall thickening
patterns differed on CT in the tumoral and ischemic segments in 75% of
patients with obstructed colitis proximal to colon cancer. Ko et al. also
showed that the target or "double halo" sign (20%) seen in the
ischemic segments appeared to be the most specific sign for diagnosing colonic
ischemia. However, because our patient population was limited, we did not find
highly specific CT findings enabling us to differentiate neoplastic from
nonneoplastic involvement of the distal ileum. In contrast to a series by Ko
et al., we confirmed tumor infiltration in all three of our patients who
showed a target sign in the thickened distal ileum. In fact, the target sign
was recently proven to appear in neoplastic conditions eliciting a
desmoplastic reaction, especially in the submucosal layer of the intestinal
wall [17]; the inner layers
were markedly enhanced because of the accumulation of abundant fibrosis seen
in one of our patients. Most typical cases occur in patients with metastatic
involvement of the gastrointestinal tract from gastric
[18] or breast
[19] tumors. However, on the
basis of our data, it is likely that there is a higher incidence of neoplastic
involvement of the distal ileum in patients in advanced stages of colonic
cancer—that is, a larger colonic mass invading the ileocecal valve (>
10 mm-thickness of the ileocecal valve), the presence of small-bowel
obstruction, or mesenteric vascular engorgement.
If CT reviewers are not aware of these patients' histories of colon cancer,
the presence of both colonic and distal ileal wall thickening might be
misinterpreted as another neoplastic or inflammatory conditions such as
lymphoma or inflammatory bowel disease, including intestinal tuberculosis,
Crohn's disease, and Behçet's syndrome. In a
differential diagnosis including intestinal tuberculosis or Crohn's disease,
bowel wall involvement patterns in these inflammatory diseases may be similar
to those of colonic cancer with distal ileal thickening; however, the degree
of bowel wall thickness may differ. In contrast to neoplastic conditions, the
bowel wall thickness in inflammatory bowel diseases generally does not exceed
2 cm [9]. Intestinal
Behçet's syndrome involving the ileocecal
region, which is nonspecific necrotizing vasculitis due to immune complex
deposition disease, can show diffuse bowel wall thickening or polypoid mass
formation in the distal ileum, the right-sided colon, or both
[20]. The contrast-enhancement
patterns in Behçet's syndrome are, however,
somewhat different from those in our patients because the involved intestinal
segments in Behçet's syndrome are markedly
enhanced in many instances
[20]. In cases of lymphomatous
involvement of the gastrointestinal tract, the bowel wall is concentrically
involved and has a symmetric pattern. Furthermore, most of the involved
segments in the lymphoma are poorly enhanced.
In conclusion, the distal ileum may be abnormally thickened in about 10% of
patients with right-sided colon cancer; this thickening results from tumor
extension (69%) or a nontumorous process (31%).
Acknowledgments
We thank Bonnie Hami, Department of Radiology, University Hospitals Health
System, Cleveland, OH, for editorial assistance in preparing the
manuscript.
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Abstract
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