DOI:10.2214/AJR.05.0095
AJR 2006; 186:1618-1626
© American Roentgen Ray Society
Bloodborne Metastatic Tumors to the Gastrointestinal Tract: CT Findings with Clinicopathologic Correlation
So Yeon Kim1,
Kyoung Won Kim1,
Ah Young Kim1,
Hyun Kwon Ha1,
Jung-Sun Kim2,
Seong Ho Park1,
Jeong Kon Kim1,
Mi-Jung Kim2,
Sung Won Park1 and
Moon-Gyu Lee1
1 Department of Radiology, Asan Medical Center, University of Ulsan College of
Medicine, 388-1, Pungnap-2 dong, Songpa-ku, Seoul, South Korea 138-736.
2 Department of Pathology, Asan Medical Center, University of Ulsan College of
Medicine, Seoul, South Korea.
Received January 18, 2005;
accepted after revision March 22, 2005.
Address correspondence to K. W. Kim
(kimkw{at}amc.seoul.kr).
Abstract
OBJECTIVE. In this essay, we illustrate the CT features of
bloodborne metastases to the gastrointestinal tract from various malignancies
with an emphasis on clinicopathologic correlation.
CONCLUSION. Familiarity with CT findings of bloodborne metastases to
the gastrointestinal tract and an understanding of the disease spread pattern
in common primary cancers will be helpful not only in detecting metastatic
disease but also in minimizing the possibility of mistaking metastasis for
another metachronous malignancy.
Keywords: bloodborne metastatic tumor • gastrointestinal radiology • oncologic imaging • radiologic-pathologic correlation
Introduction
Bloodborne metastases to the gastrointestinal tract are commonly
observed in patients with malignancies. Most lesions are from malignant
melanoma and carcinoma of the breast or lung, and they most commonly involve
the stomach and small bowel because of their rich blood supply. The radiologic
appearance of a hematogenous gastrointestinal metastasis mainly depends on the
histologic characteristics of the lesion, including the degree of vascularity
relative to the growth rate and the desmoplastic capability
[1]. Although CT has been
widely used for evaluating gastrointestinal tract diseases, few reports have
focused on the CT features of metastatic tumors to the gastrointestinal tract.
In this essay, we illustrate the CT features of bloodborne metastases to the
gastrointestinal tract from various malignancies with an emphasis on
clinicopathologic correlation.
Metastases to the Gastrointestinal Tract: Common Primary Cancers
Malignant Melanoma
Malignant melanoma is a common malignancy with an increasing prevalence. It
is the most common tumor that metastasizes to the gastrointestinal tract,
representing about one third of all metastases to the gastrointestinal tract
[2]. The small bowel is the
most common site of gastrointestinal tract involvement; in an autopsy series,
small-bowel metastases were found in 38-58% of patients with malignant
melanomas [3,
4]. Gastric metastases are less
frequently seen and were noted during autopsies in 23-26% of cases
[3,
4]. Clinically, patients with
metastatic malignant melanomas in the stomach or small bowel are usually
symptomatic and may present with abdominal pain, nausea and vomiting, weight
loss, or gastrointestinal bleeding, but 3-22% of patients may be asymptomatic
[5,
6]. Approximately 10% of
metastatic melanomas in the small bowel may act as leading points for
intussusceptions and result in small-bowel obstruction
[4,
7].
Metastatic gastric and duodenal melanomas classically appear as multiple
small submucosal nodules that may ulcerate to produce the well-known target or
bull's-eye lesions on barium studies
[8] and may be seen as diffuse
bowel wall thickening or intraluminal polypoid masses on CT scans (Figs.
1A,
1B,
1C and
2A and
2B). Small-bowel lesions are
categorized radiologically as polypoid, cavitary, infiltrating, or exoenteric
lesions, and radiologic patterns may reflect pathologic features of these
tumors [6]. Because
hematogenous deposition usually occurs in the submucosal layer, it may be seen
early as small mural nodules on luminal studies. Hematogenous dissemination
causes multiple metastatic lesions more often than it causes a single lesion,
and disseminated metastases are often variable in size. Although small
polypoid lesions are rarely seen on CT, larger lesions may be seen as
intraluminal masses, commonly with intussusceptions (Fig.
3A,
3B,
3C and
3D). Central ulceration is
especially common as the metastasis outgrows its blood supply, and usually
there is no significant desmoplastic response, leading to the appearance of a
cavitary lesion on CT (Fig. 4A
and 4B). To the contrary, if
the submucosal metastasis grows at a slow rate, it may be seen as an
infiltrating lesion possibly through local lymphatic spread. The serosal
metastatic deposits, according to their growth rates, may result in a cavitary
or exoenteric appearance on CT
[6].
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Fig. 1A —44-year-old woman with metastatic malignant melanoma to stomach.
Contrast-enhanced CT scan shows diffuse wall thickening and strong contrast
enhancement (arrowheads) along gastric body. Hepatic metastases are
also seen (asterisk).
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Fig. 1B —44-year-old woman with metastatic malignant melanoma to stomach.
Photograph from gastrofiberscope shows small elevated lesions with
brown-to-black pigmentation. Linear fissures (arrowheads) radiating
distinctly to central ulceration are noted over surface, producing spoked
wheel pattern.
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Fig. 1C —44-year-old woman with metastatic malignant melanoma to stomach.
Immunohistochemical study for HMB 45 shows positive staining of tumor cells
(arrowheads), supporting diagnosis of malignant melanoma.
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Fig. 2A —58-year-old man with metastatic malignant melanoma to duodenum.
Radiograph from upper gastrointestinal barium examination shows multiple
submucosal masses in second and third part of duodenum, one of which has
target or bull's-eye appearance (arrowheads) produced by
ulceration.
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Fig. 3B —51-year-old man with metastatic malignant melanoma to jejunum. Large
intraluminal fungating mass (arrows) is seen in distal end of
intussusceptum, presumed as leading point of intussusception.
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Fig. 3D —51-year-old man with metastatic malignant melanoma to jejunum.
Photograph of gross specimen also shows large intraluminal fungating mass as
leading point (arrows). Multiple small tumor implants with dark
brown-to-black pigmentation (arrowheads) are scattered in jejunum,
suggesting periodic embolic shower as pathogenesis. Scale: cm.
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Fig. 4A —69-year-old woman with metastatic malignant melanoma to ileum.
Contrast-enhanced CT scan shows large cavitary mass (arrows) with
low-grade enhancement in ileum. Mild perienteric infiltration is also seen
(arrowheads).
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Lung Cancer
The gastrointestinal tract has been a rare site for metastatic lung cancer.
However, further studies suggest that gastrointestinal metastases from lung
cancer may not be as rare as previously thought
[9,
10]. In an autopsy series,
they were found to exist in 14% of patients who died of lung cancer. The small
bowel was the most frequently involved organ by bloodborne metastases (34%),
and the esophagus was most commonly involved by direct invasion (57%)
[9]. In another series, the
most common histologic type of lung cancer causing small-bowel metastases was
squamous cell carcinoma (33%), followed by large cell carcinoma (28%),
adenocarcinoma (26%), and small cell carcinoma (13%). The patients with small
bowel metastases may have at least one other metastatic site, the most common
site being the lymph nodes (48%)
[10].
Lung cancer metastases to the small bowel often clinically present as
intestinal perforations [9,
10]. It appears that
small-bowel perforation is a more frequent result of metastasis from lung
cancer than from other primary cancers, and it seems that there may be a
greater tendency for these tumors to undergo necrosis before attaining enough
bulk, although the exact pathogenesis of the perforation is not clearly
understood. It has been proposed that when a metastatic tumor is unexpectedly
found on laparotomy for a perforated small bowel in a heavy smoker after the
fifth decade, lung cancer should be considered a potential primary cancer;
conversely, the cause of small-bowel perforation in patients with lung cancer
is likely to be metastasis
[10].
Although radiologic features of metastatic lung cancer to the small bowel
have been rarely reported
[11], to our knowledge, CT
scans can reveal grossly necrotic small-bowel masses sometimes with evidence
of perforation and associated lymphadenopathy (Figs.
5A,
5B,
5C,
5D,
5E and
6A,
6B,
6C,
6D and
6E).
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Fig. 5A —78-year-old man with metastatic small cell carcinoma of lung to
ileum. Contrast-enhanced CT scan shows intraluminal fungating mass
(arrow) in ileum with large surface ulceration (arrowhead).
Adjacent, conglomerate mesenteric masses encasing mesenteric vessels are also
seen (curved arrow).
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Fig. 5B —78-year-old man with metastatic small cell carcinoma of lung to
ileum. Photograph of gross specimen reveals intraluminal ulcerated fungating
tumor (arrows) and mesenteric mass (curved arrow). Scale:
cm.
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Fig. 5C —78-year-old man with metastatic small cell carcinoma of lung to
ileum. Photograph of cut surface shows communication of intraluminal mass
(arrowheads) and mesenteric mass (curved arrow) through
large ulcer crater on surface (asterisk). Scale: cm.
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Fig. 5E —78-year-old man with metastatic small cell carcinoma of lung to
ileum. Immunohistochemical staining for synaptophysin shows positive staining,
supporting diagnosis of small cell carcinoma.
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Fig. 6A —56-year-old man with metastatic poorly differentiated non-small cell
carcinoma of lung to jejunum. Contrast-enhanced CT scan shows luminal
encircling mass with poor contrast enhancement (arrow) in
jejunum.
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Fig. 6B —56-year-old man with metastatic poorly differentiated non-small cell
carcinoma of lung to jejunum. Another jejunal mass is noted (arrow),
and small mesenteric nodules (curved arrow) are adjacent to thickened
bowel loop. Extraluminal air bubbles (arrowhead) and perienteric
infiltration are present, suggestive of bowel perforation.
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Fig. 6C —56-year-old man with metastatic poorly differentiated non-small cell
carcinoma of lung to jejunum. Photograph of gross specimen reveals multiple
ulcerative masses (arrows) in jejunum. Scale: cm.
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Fig. 6D —56-year-old man with metastatic poorly differentiated non-small cell
carcinoma of lung to jejunum. Photograph of cut surface of specimen shows
grossly submucosal location of tumor and focal disruption of muscle and serosa
(arrowheads). Scale: cm.
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Fig. 6E —56-year-old man with metastatic poorly differentiated non-small cell
carcinoma of lung to jejunum. Low-power photomicrograph shows tumor cells
(asterisk) are mainly confined to serosa, muscularis propria (MP),
and submucosa (SM), in contrast with intact mucosa (m). These findings suggest
possible mechanism of disease spread is secondary invasion of small bowel that
may have occurred from metastatic deposits in mesentery (H and E,
x20).
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Breast Cancer
Autopsy series record an incidence as high as 8-16% of breast cancer
metastases to the gastrointestinal tract. The stomach is the organ most
frequently involved with metastatic disease. Occasionally, it may occur many
years after treatment of the primary lesion. The predominant mode of
dissemination depends on the histologic type of the tumor. Lobular carcinomas,
which account for only 10-14% of all breast carcinomas
[12], metastasize
significantly more often to the gastrointestinal tract than infiltrating
ductal carcinomas [13].
Clinically, symptoms may be subtle or nonspecific (e.g., anorexia, vomiting,
and epigastric pain). Pathologically, the most common and characteristic
appearance of metastatic lobular carcinoma of the breast to the
gastrointestinal tract is a linitis plastica-like appearance, showing tumor
infiltration along the bowel wall with diffuse mural thickening of the
involved segment. Although no desmoplastic response is elicited by metastatic
tumor, the highly cellular submucosal deposits may narrow and deform the lumen
and produce a scirrhous appearance at radiologic examinations, which is most
commonly seen in the stomach. Rigidity and gastric thickening with markedly
diminished or absent peristalsis are associated with spiculation and
angulation of the folds. It may be indistinguishable from primary scirrhous
carcinoma of the stomach, appearing as diffuse bowel wall thickening on CT
[14] (Fig.
7A,
7B,
7C and
7D).
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Fig. 7A —66-year-old woman with metastatic lobular carcinoma of breast to
stomach. Radiograph from upper gastrointestinal examination shows diffuse wall
thickening and rigidity of lower body of stomach (arrows)
representing typical linitis plastica pattern.
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Fig. 7D —66-year-old woman with metastatic lobular carcinoma of breast to
stomach. High-power photomicrograph reveals cords of infiltrating neoplastic
cells arranged in single-file formation (ellipse), which is identical
to primary lobular carcinoma of breast (H and E, x100).
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Metastases to the Gastrointestinal Tract: Uncommon Primary Cancers
Uncommon malignancies that can metastasize to the gastrointestinal tract
include renal cell carcinoma (RCC), hepatocellular carcinoma (HCC), and,
rarely, choriocarcinoma.
Although metastases may develop in more than 60% of patients with RCC,
gastrointestinal metastasis is uncommon, with only a few sporadically reported
cases in the English-language literature. Batson's vertebral venous plexus is
considered a possible route in some cases. The reported clinical presentation
of metastatic RCC was gastrointestinal bleeding or obstruction. Typically,
metastatic RCC to the gastrointestinal tract presents as a solitary, bulky,
and hyper-vascular lesion on cross-sectional imaging
[15]
(Fig. 8).
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Fig. 8 —64-year-old woman with metastatic renal cell carcinoma (RCC) to
duodenum. Contrast-enhanced CT scan shows intraluminal fungating mass with
strong enhancement (arrows) in third portion of duodenum. Patient had
history of right nephrectomy for RCC.
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Fig. 9C —51-year-old woman with metastatic choriocarcinoma to jejunum.
Low-power photomicrograph shows tumor with hemorrhagic necrosis is mainly
confined to proper muscle and submucosa and is only focally extended to mucosa
(curved arrow) (H and E, x40).
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Fig. 9D —51-year-old woman with metastatic choriocarcinoma to jejunum.
High-power photomicrograph shows tumor consists of two different types of
cells, cytotrophoblast (arrowheads) and syncytiotrophoblast
(arrows), supporting diagnosis of choriocarcinoma (H and E,
x100).
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HCC with gastrointestinal metastasis is also an uncommon condition, and
patients are usually asymptomatic. The hematogenous spread of HCC to the
gastrointestinal tract may be caused by tumor thrombi via the portal system
and may progress through hepatofugal portal flow to the gastrointestinal
tract, but CT scans usually do not reveal any gross venous thrombi
[16].
Although it is rare, choriocarcinoma can metastasize to the
gastrointestinal tract. Because of the hypervascularity of the lesion, a
patient with metastatic choriocarcinoma to the gastrointestinal tract can
present with gastrointestinal bleeding (Fig.
9A,
9B,
9C and
9D).
Conclusion
Although most gastrointestinal metastases are encountered in patients with
widespread metastases and known primary lesions, they may occasionally present
as the initial manifestation of an occult primary lesion, leading to
diagnostic difficulty. Therefore, familiarity with CT findings of bloodborne
metastases to the gastrointestinal tract and an understanding of the disease
spread pattern in common primary cancers will be helpful not only in detecting
metastatic disease but also in minimizing the possibility of mistaking
metastasis for another metachronous malignancy.
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Abstract
Introduction
