AJR 2005; 184:803-811
© American Roentgen Ray Society
Gastrointestinal Stromal Tumors: Clinical, Radiologic, and Pathologic Features
Kumaresan Sandrasegaran1,
Arumugam Rajesh1,
Jonas Rydberg1,
Daniel A. Rushing2,
Fatih M. Akisik1 and
John D. Henley3
1 Department of Radiology, University Medical Center, UH 0279, 550 N University
Blvd., Indianapolis, IN 46202.
2 Department of Oncology, Indiana University Medical Center, Indianapolis, IN
46202.
3 Department of Pathology, Indiana University Medical Center, Indianapolis, IN
46202.
Received May 24, 2004;
accepted after revision July 23, 2004.
Address correspondence to K. Sandrasegaran
(ksandras{at}iupui.edu).
Introduction
Gastrointestinal stromal tumors (GISTs) are the most common mesenchymal
tumors to arise from the gastrointestinal tract. They are characterized by
expression of a tyrosine kinase growth factor receptor, also called kit
receptor or CD117. This expression allows unchecked growth of tumor and
resistance to apoptosis. These tumors differ immunohistologically and
behaviorally from other mesenchymal tumors such as leiomyosarcomas, which do
not express kit antigen. In the past, GISTs were misdiagnosed as smooth muscle
tumors because on light microscopy the two tumors share many features. We
reviewed the imaging findings of 29 patients with GIST seen at our affiliated
institutions. The tumors were predominantly of gastric (11 patients) or
enteric (13 patients) origin. Two patients each had duodenal or rectal tumors,
and one had a primary mesenteric tumor. In this essay, we discuss the imaging
findings of these patients at presentation and after chemotherapy. We also
describe the clinical and pathologic literature of this recently recognized
tumor.
Clinical Features
The incidence of GIST is difficult to estimate because of previous
diagnostic inconsistencies. There are probably 1,000–2,000 new cases per
year in the United States [1,
2]. The average patient with
GIST is 40–70 years old. Male to female incidence is now considered to
be equal; some earlier articles purported a higher male incidence
[2–6].
Despite being the most common mesenchymal tumor, GISTs only account for
1–3% of all gastrointestinal tumors and are dwarfed in numbers by the
more common epithelial and lymphomatous tumors.
The clinical presentation depends on the size and site of tumor. Large
series have shown the stomach to be the most common site, accounting for
60–70% [1,
4,
7–9].
Approximately one-third occur in the small bowel, with rare occurrence in the
colon and rectum (5%), esophagus (< 2%), and appendix
[10]. Some GISTs primarily
arise in the omentum, mesentery, or retroperitoneum and are unrelated to the
tubular gastrointestinal tract. Apart from their occurrence in the esophagus,
GISTs are more prevalent in the gastrointestinal tract compared with true
smooth muscle tumors such as leiomyosarcomas.
Clinical presentation is often vague. Abdominal pain or distention is the
most common presentation of GISTs
[2]. Gastrointestinal bleeding
or unexplained anemia is the next most common presentation. Duodenal tumors
present with obstructive jaundice and may be confused with pancreatic cancer.
Surprisingly, despite the large size of duodenal tumors, bowel obstruction is
rare. The exophytic and cavitary nature of the tumor may delay luminal
constriction.
In the absence of metastatic disease, complete surgical excision is
undertaken and offers the best hope of cure
[3,
6]. Unlike carcinomas,
resection of GISTs does not require wide bowel excision
[8]. Lymphadenectomy is usually
not required because these tumors do not show lymph node metastases
[8,
11]. However, despite
apparently complete resection with clear margins, the recurrence rate is high;
hepatic or mesenteric recurrence occurs in 40–90% of patients undergoing
apparently curative surgery [4,
12]. This may be partly due to
tumor rupture leading to mesenteric implants; hence, the risk of recurrence
emphasizes the importance of having meticulous surgical technique
[11]. For this reason,
percutaneous biopsy is best avoided
[2].
Radiation therapy and standard chemotherapy have not been found to be
successful in treating this disease
[4,
13,
14]. Unlike more common
breast, lung, and colon cancers, in which tumor development requires multiple
mutations of several genes, GIST occurs because of gain-of-function mutation
of a single kit gene found on chromosome 4. The resultant increase in tyrosine
kinase activity allows the tumor to grow unchecked. In 1999, a new agent was
found to be effective against GIST by selectively inhibiting tyrosine kinase
enzyme. This agent was recently approved for clinical use in United States as
imatinib mesylate (Gleevec, Novartis)
[15]. It is a new breed of
targeted molecular therapy that has minimal toxicity. Recent studies report a
median disease-free survival rate in malignant nonmetastatic GIST of about 5
years and only 10–20 months if metastases are present
[3,
4,
12,
14,
16]. In our experience, nearly
all patients with metastatic disease show good response to imatinib therapy,
with most being in remission at 24 months.
Pathologic Features
Histology
GISTs have a tendency to exophytic growth. They commonly involve the
muscularis propria and, in 50% of cases, may show mucosal ulceration
[17]. On light microscopy,
GIST can simulate leiomyosarcoma, and hence in the past, it was labeled as
such. However, the two tumors have different origins; GISTs are thought to
originate from a stem cell that normally expresses CD117.
The histologic classification is based on the predominant cell type, either
spindle or epithelioid cell [1,
18] (Figs.
1A and
1B). The former accounts for
about 75% of gastric GISTs
[19] and is also the most
common type of GIST at other sites. Gastric GISTs in the greater curvature
have a low malignant potential despite reaching a large size
[8]. In general, 20–30%
of GISTs are malignant at presentation
[1,
20].
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Fig. 1A. —50-year-old woman with small-bowel gastrointestinal stromal tumor
(GIST). Photomicrograph of histopathologic slide shows typical GIST composed
of fascicles of nondescript spindle cells. Appearance on H and E stain is
similar to that of smooth muscle tumor.
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Fig. 1B. —50-year-old woman with small-bowel gastrointestinal stromal tumor
(GIST). Photomicrograph of histopathologic slide shows that in appropriate
clinicopathologic setting, c-kit positivity (brown staining) is diagnostic of
gastrointestinal stromal tumor.
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It is difficult to predict malignant potential. Features associated with
worse prognosis include distal bowel location, tumor size, and high mitotic
activity [7]. Tumor necrosis,
cystic change, nuclear atypia, tumor vascularity, and degree of staining for
CD117 do not reliably indicate the malignant potential of GISTs
[8]. Tumor size is the single
most predictive factor of metastatic potential
[4,
12]; thus, the radiologist has
a role in predicting malignancy. Tumors of less than 2 cm are usually benign,
whereas those over 5 cm are usually malignant
[11]. However, many
pathologists believe that all GISTs will eventually become malignant, and
smaller tumors should be classified as at lower risk for malignancy rather
than as benign [20].
Immunohistochemistry
Mesenchymal tumors are currently classified not only from their light
microscopic appearance but also using immunochemistry.
Table 1 shows a simplified
version of the current classification. Specific markers for glial tumors
include S-100 protein and glial fibrillary acidic protein. For smooth muscle
tumors, specific markers include 
–smooth muscle antigen and
desmin; for fibrous tumors, the specific marker is vimentin. In the future,
molecular genetics may help to determine which GISTs will become malignant. In
general, certain mutations, such as the gain-of-function mutation in exon 11
of c-kit antigen and an increased number of mutations are associated with
malignant potential [7,
8].
Radiologic Features
Tumor at Presentation
At presentation, most GISTs are large, usually between 3 and 10 cm. The
predominant pattern seen in our cohort of patients and reported in another
radiologic series [21] was a
heterogeneously enhancing exophytic mass
(Fig. 2). Small gastric GISTs
may show intense enhancement with IV contrast administration
(Fig. 3); this is a less common
finding in the small bowel, probably because enteric tumors are larger and
more malignant at presentation
[22]. Hemorrhage can be seen
in larger tumors on unenhanced images. An intraluminal component can
occasionally be seen on CT (Fig.
4). Mucosal ulceration occurs in 50% of gastric tumors (Figs.
5A and
5B) shown by the presence of
air or oral contrast material within the mass. Many cases of exophytic gastric
GISTs in our series were initially misdiagnosed as a pancreatic mucinous tumor
or pseudocyst (Figs. 6A and
6B).
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Fig. 3. —30-year-old man with gastric gastrointestinal stromal tumor. Axial
contrast enhanced CT scan of upper abdomen shows intense homogenous
enhancement of tumor arising from gastric wall (arrow).
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Fig. 5A. —Gastric gastrointestinal stromal tumor (GIST). Axial
contrast-enhanced CT scan of upper abdomen of 69-year-old woman shows large
intraluminal component of tumor with pocket of gas (arrow).
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Fig. 5B. —Gastric gastrointestinal stromal tumor (GIST). In 63-year-old woman
with gastric GIST, axial contrast-enhanced CT scan of upper abdomen shows
large heterogeneously enhancing tumor in stomach and ulcer filled with oral
contrast agent (arrow).
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Fig. 6A. —30-year-old man with gastric gastrointestinal stromal tumor. Axial
contrast-enhanced CT scan of upper abdomen shows large exophytic and necrotic
tumor (arrow, A and B) in region of body and tail of
pancreas (arrowheads, B). This tumor was originally mistaken
for infected pancreatic pseudocyst.
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Fig. 6B. —30-year-old man with gastric gastrointestinal stromal tumor. Axial
contrast-enhanced CT scan of upper abdomen shows large exophytic and necrotic
tumor (arrow, A and B) in region of body and tail of
pancreas (arrowheads, B). This tumor was originally mistaken
for infected pancreatic pseudocyst.
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Unlike adenocarcinoma, GIST does not involve the bowel wall concentrically.
As a result bowel obstruction is rare, despite the large size of the GIST. The
intraluminal component accounts for a small proportion of tumors. Unlike
carcinoid tumors, the primary lesion is large and is the predominant finding.
Mesenteric masses at presentation are usually well defined with a smooth
surface and do not show spiculation or indrawing of mesentery
(Fig. 7). Like lymphoma, GIST
can also show aneurysmal dilation of the bowel (Figs.
8A and
8B). This may be partly
because the cavitary nature of these fast-growing tumors allows enlargement of
the apparent lumen. The tumors may also damage the myenteric plexus, allowing
dilatation of lumen. The cavitation may allow air to collect in the
nondependent aspect of larger tumors, described as the
"Toricelli-Bernouilli" crescentic necrosis sign
(Fig. 9). Calcification was
not seen in any tumor at presentation but was occasionally seen in metastases
after specific chemotherapy.
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Fig. 7. —76-year-old man with small-bowel gastrointestinal stromal tumor.
Axial contrast-enhanced CT scan of pelvis shows smooth mesenteric metastasis
(arrowheads) at presentation. There is no indrawing or spiculation of
mesentery.
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Fig. 8A. —45-year-old man with small-bowel gastrointestinal stromal tumor.
Axial contrast-enhanced CT scans of mid abdomen show large mass
(arrow) arising from small bowel, causing aneurysmal dilatation of
bowel. Proximal (arrowheads) and distal segments of small bowel were
of normal caliber.
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Fig. 8B. —45-year-old man with small-bowel gastrointestinal stromal tumor.
Axial contrast-enhanced CT scans of mid abdomen show large mass
(arrow) arising from small bowel, causing aneurysmal dilatation of
bowel. Proximal (arrowheads) and distal segments of small bowel were
of normal caliber.
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Fig. 9. —54-year-old man with gastric gastrointestinal stromal tumor. Axial
contrast-enhanced CT scan of upper abdomen shows area of crescent-shaped
necrosis (arrowheads) in tumor, "Toricelli-Bernouilli"
sign.
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We did not see vascular invasion or venous thrombosis associated with GIST,
even if a large tumor was close to mesenteric or splenic veins.
Metastatic Disease
Lymphadenopathy.—Lymph node metastases were not seen in any
of our patients; unlike adenocarcinoma or lymphoma, the lymphatic route does
not appear to be a common mode of tumor spread. The presence of significant
adenopathy should raise the possibility of an alternative diagnosis.
Mesenteric–omental disease.—Mesenteric metastases are
common at relapse. These may be related to peritoneal spill of tumor content
at surgery. However, they can also be found at presentation in large enteric
tumors and, much less commonly, in gastric tumors. Many mesenteric masses have
a low-density center, even when the primary tumor is hypervascular. Our
experience is that these metastases are missed because they may be small and
distant from primary tumor (Fig.
10). Differentiation from unopacified bowel may be difficult, and
a meticulous attention to all parts of the mesentery is required. CT is better
at depicting mesenteric metastases than MRI. This may partly be due to bowel
motion artifact and partly because we did not use oral contrast agents for MRI
examinations. Large mesenteric masses may grow around the mesenteric vessels
but do not tend to cause distal venous thrombosis
(Fig. 11).
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Fig. 10. —76-year-old man with small-bowel gastrointestinal stromal tumor.
Axial contrast-enhanced CT scan of mid abdomen shows rounded nodule
(arrowhead) in mesentery in keeping with metastases. Metastasis is
far from site of resected tumor (arrow). Note that differentiation
from unopacified bowel is difficult and requires meticulous attention.
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Fig. 11. —75-year-old woman with small-bowel gastrointestinal stromal tumor.
Axial contrast-enhanced CT scan of mid abdomen shows large mesenteric mass
(arrow) growing around mesenteric vessels (arrowheads).
There is no thrombosis of mesenteric vessels.
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Omental disease is seen less frequently than mesenteric disease. Omental
masses are usually small (< 2 cm) and homogeneously enhancing. Omental
caking was seen in only one of 29 patients (Figs.
12A and
12B). Because of the mobility
of the omentum, some masses may appear in different positions on subsequent
scans. Despite a high risk of solid mesenteric metastases, ascites is rare and
is more likely to be a result of chemotherapy
[15].
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Fig. 12A. —76-year-old man with small-bowel gastrointestinal stromal tumor.
Axial contrast-enhanced CT scan (A) and axial T2-weighted
fat-suppressed fast spin-echo MRI (B) of pelvis show omental caking
(arrows).
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Fig. 12B. —76-year-old man with small-bowel gastrointestinal stromal tumor.
Axial contrast-enhanced CT scan (A) and axial T2-weighted
fat-suppressed fast spin-echo MRI (B) of pelvis show omental caking
(arrows).
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Liver metastases.—Small liver metastases are usually
hypervascular on CT and MRI before chemotherapy. Dual-phase CT or MRI with
gadolinium may show bright homogeneous enhancement in the late arterial
(portal venous inflow) phase and almost complete washout on the hepatic venous
phase (Figs. 13A and
13B). Consequently, untreated
liver metastasis may be missed on a single venous phase CT study. However, not
all metastases have similar vascularity. In the same liver, there may be hypo-
and hypervascular masses (Fig.
14), possibly indicating different generations of metastases. On
MRI, the masses are usually of low or intermediate signal on T1-weighted
sequences and marginally bright on T2-weighted sequences. When MRI is used to
assess liver metastases, we routinely perform a multiphasic volumetric
fat-suppressed gadolinium-enhanced series. Necrosis is common in larger
masses. Hemorrhage is rare within the liver metastases but may manifest as
increased signal on T1-weighted sequence. Purely cystic metastases are rare
before therapy but are a common finding on CT after specific chemotherapy.
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Fig. 13A. —78-year-old woman with small-bowel gastrointestinal stromal tumor.
Axial breath-hold 3D fat-suppressed gradient-echo MRI of liver with gadolinium
shows bright homogenous enhancement of metastasis (arrow) in late
arterial phase. Smaller hypovascular metastases are also evident
(arrowheads).
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Fig. 13B. —78-year-old woman with small-bowel gastrointestinal stromal tumor.
In venous phase, MRI of large metastasis shows complete washout of contrast
material (arrow). Smaller hypovascular metastases are also evident
(arrowheads).
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Other metastases.—Lung metastases are extremely rare in
GIST, even in the presence of extensive liver and peritoneal metastases. This
is a major difference in the metastatic pattern between GIST and
leiomyosarcoma. It appears that GISTs, unlike leiomyosarcomas
[13,
16], preferentially spread via
the portal vein. We have not come across brain or bone metastases and are not
aware of confirmed reports of these.
Appearance After Therapy
Mesenteric and liver metastatic diseases become hypovascular and, in some
cases, completely cystic on CT, even after 1 month of targeted chemotherapy
(Figs. 15A and
15B). This finding has also
been reported by others [23].
We have noted that a few patients with apparently completely cystic masses on
CT showed subsequent relapse with increase in the size of metastases. Some of
these metastases showed enhancement on MRI (Figs.
16A and
16B). Overall, MRI is likely
to be better than single-phase CT in assessing the viability of
metastases.
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Fig. 15A. —78-year-old woman with small-bowel gastrointestinal stromal tumor.
Axial contrast-enhanced CT scan of liver obtained before treatment shows
predominantly low-attenuation metastasis (arrow) with hyperdense
foci.
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Fig. 15B. —78-year-old woman with small-bowel gastrointestinal stromal tumor.
Axial contrast-enhanced CT scan obtained after treatment with imatinib
mesylate (Gleevec, Novartis) shows cystic change in metastasis
(arrow).
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Fig. 16A. —50-year-old woman with small-bowel gastrointestinal stromal tumor
Axial contrast-enhanced single-phase CT scan of liver shows low-density
well-defined cystic mass (arrow), which was treated metastasis,
simulating simple cyst.
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Fig. 16B. —50-year-old woman with small-bowel gastrointestinal stromal tumor
Gadolinium-enhanced T1-weighted fat-suppressed gradient-echo image, obtained
at same level as A, shows peripheral and nodular enhancement
(arrows) in metastasis. MRI was performed 1 month before CT
(A). Patient relapsed 2 months later while still on imatinib mesylate
(Gleevec, Novartis) therapy.
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Conclusion
GIST is a new classification for a group of mesenchymal tumors that
predominantly exhibit an altered oncogene, kit (CD 117). These tumors are
different in behavior and immunology from the better known smooth muscle
tumors of the gastrointestinal tract. Specific molecular therapy, with
imatinib mesylate, is now available. Radiologists can often predict the
correct diagnosis at presentation by the appearances of a large exophytic
bowel mass, which may show necrosis or hemorrhage. Hypervascular liver
metastases and smooth low-density mesenteric masses suggest metastatic
disease. Adenopathy, concentric bowel involvement, large-volume ascites, and
spiculated mesenteric masses suggest an alternative diagnosis. The radiologic
appearances can change drastically after therapy. Previously solid
hypervascular masses may become completely cystic on CT even within 1 month of
treatment. MRI can better evaluate liver metastases than CT. However, CT is
superior in detecting mesenteric metastases.
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Introduction
Clinical Features
