AJR 2003; 181:785-793
© American Roentgen Ray Society
Imaging in Oncology from The University of Texas M. D. Anderson
Cancer Center |
Diagnosis, Staging, and Follow-Up of Esophageal Cancer
Revathy B. Iyer1,
Paul M. Silverman,
Eric P. Tamm,
Joel S. Dunnington and
Ronelle A. DuBrow
1 All authors: Department of Diagnostic Radiology, The University of Texas M. D.
Anderson Cancer Center, 1515 Holcombe Blvd., Unit 57, Houston, TX 77030.
Received June 28, 2002;
accepted after revision March 14, 2003.
Address correspondence to R. B. Iyer.
Introduction
Cancer of the esophagus is not as prevalent in the United States as other
tumors of the gastrointestinal tract. However, the overall mortality from this
disease is extremely high. Esophageal cancer accounts for only about 7% of all
tumors arising from the hollow viscera, with approximately 12,000 new cases
reported in 2000 [1]. The
5-year survival rate is less than 10%
[2].
The esophagus is lined by squamous epithelium, and therefore the prevalent
histology of esophageal tumors is squamous cell carcinoma, accounting for
approximately 85% of cases [3].
Barrett's esophagus is a columnar metaplasia of the squamous epithelium of the
esophagus likely related to gastroesophageal reflux disease. Barrett's
esophagus is considered a premalignant condition, predisposing patients to the
development of adenocarcinoma of the esophagus
[2,
4] (Figs.
1 and
2). Barrett's esophagus
increases the risk of developing adenocarcinoma by at least 30-fold over the
general population, and there has been a significant increase in the incidence
of adenocarcinoma arising in Barrett's mucosa over the past few decades
[2]. Other histologic types,
such as sarcomas, occur but are extremely rare.
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Fig. 2. —63-year-old man with history of gastroesophageal reflux
disease and biopsy-proven Barrett's esophagus. Reticular pattern of
intersecting barium-filled grooves (arrow) that may be seen in
Barrett's esophagus is shown on esophagram.
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The greatest risk factors for the development of esophageal cancer are
chronic abuse of tobacco and alcohol. Other conditions that may also
predispose to the development of squamous cell malignancy of the esophagus
include achalasia, lye strictures, celiac disease, Plummer-Vinson syndrome,
and tylosis [2,
4]. Patients with achalasia
have a 30-fold greater likelihood of developing esophageal cancer than the
general population [3] (Figs.
3A, and
3B).
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Fig. 3A. —66-year-old man with achalasia. Esophagram shows multiple
tertiary contractions and beaked appearance (arrow) of distal
esophagus near gastroesophageal junction, compatible with achalasia.
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This review outlines the imaging findings that may be encountered in the
diagnosis, staging, and follow-up of esophageal carcinoma.
Staging
The two most important prognostic indicators for esophageal cancer are
depth of tumor penetration and nodal involvement. T1 tumors invade the lamina
propria or submucosa, T2 tumors invade the muscularis propria, T3 tumors
involve the adventitia, and T4 tumors directly invade adjacent structures
(Fig. 4). The TNM staging of
esophageal cancer [2,
3] is summarized in
Table 1. The 5-year survival
rate for patients with tumors remaining in the esophageal wall is
approximately 40% [3]. Those
with tumors involving the adventitia of the esophagus have only a 5-year
survival rate of 4%, possibly because the lack of a serosal surface to the
esophagus allows lateral spread or mediastinal invasion to occur more readily
[3].
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Fig. 4. —Illustration shows stages of esophageal malignancy. T1 lesion
involves mucosa (m) or submucosa (s), T2 lesion invades muscularis propria
(mp), T3 lesion invades adventitia (a), and T4 lesion involves adjacent organ
(A). N indicates metastatic lymph node.
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The likelihood of nodal spread increases with increasing tumor (T) stage,
and nodal involvement also portends a poor prognosis. When tumors are limited
to the mucosa, the likelihood of nodal disease is less than 1%, increasing to
50% when there is submucosal involvement by the primary tumor. The 5-year
survival rate for patients without nodal involvement is approximately 40%,
diminishing to approximately 3% for those with nodal metastases
[3]. Regional nodal metastases
(N1) for squamous carcinoma of the esophagus include spread to the cervical,
mediastinal, and perigastric nodes. If celiac lymph nodes are involved by
squamous cell carcinoma, the disease is considered distant metastases or M1
disease. For esophageal adenocarcinoma, on the other hand, celiac adenopathy
is considered N1 disease [5].
The pathways of nodal metastases are illustrated in
Figure 5.
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Fig. 5. —Illustration shows cancers of mid and distal esophagus and
lymphatic drainage. Nodes involved by tumor (purple) typically occur
at same level as primary tumor (arrowheads); however, skip metastases
to nodes at other levels may be seen. Nodes below diaphragm at gastrohepatic
ligament (curved arrow) typically drain distal esophageal tumors but
may also be involved in middle and upper thirds of esophagus. Spread to
cervical and supraclavicular nodes (straight arrow) may occur, as
draining lymphatics follow vessels cranially.
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Radiologic Evaluation
Barium studies are often used to detect esophageal carcinomas in patients
with dysphagia. Esophageal cancer may present as polypoid, infiltrative,
varicoid, or ulcerative lesions (Figs.
6,
7,
8,
9). Superficial spreading
lesions tend to show a nodular mucosal pattern without a well-defined mass.
Early esophageal cancers may have subtle findings on barium studies, and
therefore endoscopic follow-up of any suspected abnormality should be
performed [4]. Once a diagnosis
of esophageal malignancy has been established, barium studies may be used to
evaluate the morphology and size of tumors before and after treatment.
Radiographic findings may also vary with the histology of the primary tumor.
Adenocarcinomas occurring in the distal esophagus have a propensity to invade
the gastric cardia and fundus, which is a most unusual finding with squamous
cell carcinomas that typically occur more proximally
(Fig. 10). Complications such
as tracheoesophageal fistula formation from locally advanced disease are well
shown on barium studies (Fig.
11).
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Fig. 6. —64-year-old man with polypoid adenocarcinoma (straight
arrow) of distal esophagus shown on esophagram. Tumor is on thickened
fold (curved arrow) and invades wall of esophagus
(arrowheads).
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Fig. 11. —60-year-old woman with squamous cell carcinoma of esophagus
(black arrows) complicated by tracheoesophageal fistula (white
arrow) shown on esophagram. Tracheal lumen (T) is outlined by barium.
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The main purpose of cross-sectional imaging studies in patients with known
esophageal carcinoma is to stage the disease as accurately as possible to
determine which patients may be suitable candidates for surgical resection. CT
is considered complementary to endoscopy and barium studies and may be used to
stage and follow up esophageal tumors. CT may be used to define the local
extent of tumor by showing the extent of involvement of the esophageal wall by
tumor and tumor invasion of the periesophageal fat. CT cannot reliably
delineate the individual layers of the esophageal wall and therefore cannot
distinguish between T1 and T2 lesions. Infiltration of the tumor into the
periesophageal fat as seen on CT denotes a T3 tumor and adversely affects
prognosis, although en bloc resection for a cure may still be attempted
[5]. The reported accuracy of
CT in diagnosing mediastinal invasion ranges from 59% to 82%
[3]. Tumor infiltration to
involve adjacent mediastinal structures such as the aorta or tracheobronchial
tree denotes a T4 lesion that is considered inoperable
(Fig. 12). Contiguous invasion
of adjacent structures may be difficult to predict when tumor is seen to abut
other structures in the mediastinum. MRI provides little advantage over CT in
staging esophageal tumors [3].
MRI also cannot reliably distinguish the different layers of the esophageal
wall, which is crucial for accurate local staging. Nodal disease and distant
metastases can also be shown on CT (Figs.
13A, and
13B). Nodes that are larger
than 1 cm in short-axis dimension are considered suggestive of metastatic
disease, although size is known to be an insensitive parameter for determining
nodal spread because tumor can be present in subcentimeter nodes.
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Fig. 13B. —47-year-old man with adenocarcinoma of distal esophagus.
Axial CT scan of upper abdomen shows associated metastatic lymph node
(asterisk) in gastrohepatic ligament along course of left gastric
vessels.
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Endoscopic sonography has been used to define the layers of the esophageal
wall and thereby distinguish the depth of tumor penetration. The frequency of
most endoscopic sonography transducers is 7.5 or 12 MHz. The overall accuracy
of endoscopic sonography is greater than CT and is reported to be between 85%
and 90% [5]. Overstaging may
occur because peritumoral edematous changes may be mistaken for tumor and
understaging may occur when tumor penetration is below the resolution of
sonography [5]. The normal
esophagus has five layers, as depicted by endoscopic sonography. The innermost
layer is hyperechoic and corresponds to the superficial mucosa. The second
layer is hypoechoic and corresponds to the deep mucosa and muscularis mucosae.
The third layer is again hyperechoic and corresponds to the submucosa and its
interface with the muscularis propria. The next layer is hypoechoic and
corresponds to the muscularis propria, and the fifth layer is hyperechoic and
corresponds to the adventitia
[6]
(Fig. 14). Endoscopic
sonography may be difficult to perform in patients with stenotic tumors in
which the endoscope cannot be passed through the luminal tumor.
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Fig. 14. —55-year-old man with T2 esophageal tumor (m) shown on
endoscopic sonogram. Note alternating hyperechoic and hypoechoic layers
(arrowheads) of normal esophageal wall as seen on sonography.
Innermost layer is hyperechoic and corresponds to superficial mucosa. Second
layer is hypoechoic and corresponds to deep mucosa and muscularis mucosae.
Third layer is again hyperechoic and corresponds to submucosa and its
interface with muscularis propria. Fourth layer is hypoechoic and corresponds
to muscularis propria, and outer fifth layer is hyperechoic and corresponds to
adventitia.
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Positron emission tomography (PET) with FDG is being used to stage
esophageal cancer. The primary tumor can be identified on the PET image,
although the overall spatial resolution is limited, and, therefore, local
staging of the disease is limited
[3]. However, PET has the
advantage of total body coverage that may show distant sites of metastatic
disease in nodes, liver, lung, bone, adrenal glands, and other organs, which
would then obviate surgery (Figs.
15A, and
15B).
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Fig. 15A. —61-year-old man with long history of gastroesophageal reflux
with subsequent development of adenocarcinoma of distal esophagus. Axial CT
scan of abdomen shows indeterminate nodule (arrow) inseparable from
left adrenal gland.
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Fig. 15B. —61-year-old man with long history of gastroesophageal reflux
with subsequent development of adenocarcinoma of distal esophagus. Positron
emission tomography image shows uptake of FDG in primary esophageal tumor (T)
and in nodule (arrow) corresponding to lesion shown on CT scan
(A), subsequently proven to be metastasis.
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Treatment
Several treatment options, including surgery, radiation, and chemotherapy,
are available to patients with esophageal cancer, although none has proven
ideal at this time. Most patients with esophageal carcinoma present with
dysphagia, which generally indicates advanced disease. Treatment may be aimed
at palliation in those patients with advanced disease versus resection for a
cure in those with limited disease. Surgical resection with curative intent
may include en bloc resection of tumor and all the associated nodes. En bloc
resection may be performed through a right thoracotomy with laparotomy, such
as the Ivor-Lewis esophagogastrectomy; a left thoracotomy with a
thoracoabdominal incision; or two separate abdominal and cervical incisions
without a thoracotomy [2].
After resection of the esophageal tumor, the continuity of the upper digestive
tract may be reestablished by pulling the stomach into the chest and
performing an anastomosis with the residual proximal esophagus. Colonic and
small intestinal interpositions may also be performed, although these
procedures are less common [2]
(Fig. 16).
Complications after esophageal resection are not rare (Figs.
17 and
18A,
18B). Some acute complications
include anastomotic leaks, torsion of the pulled-up segment, hemorrhage, wound
infections, and subphrenic abscesses. More delayed complications include
anastomotic strictures, dumping syndrome, and reflux esophagitis
[2].
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Fig. 17. —66-year-old man after resection of esophageal cancer.
Postoperative esophagram shows linear collection of contrast material
(arrowheads) from esophagogastric anastomosis (arrow),
compatible with leak.
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Neoadjuvant protocols using preoperative chemotherapy and radiotherapy have
been tried on potentially resectable tumors in patients with more advanced
disease to downstage tumors before surgery
[7]. However, many patients are
not considered candidates for resection because of tumor stage or comorbid
conditions that would preclude surgery. Palliation is therefore attempted in
these patients to relieve dysphagia. Dilatation and stent placement may
provide some relief to patients with severe dysphagia. Endoscopic laser
ablation of obstructing intraluminal masses has also been attempted with some
success [8]. Radiation therapy
may also be used to palliate or definitively treat esophageal cancer in
patients who may not be surgical candidates. External beam radiation doses of
45-60 Gy are typically used
[9].
Follow-Up
Imaging is often requested to follow up tumors during therapy and to
document response. Endoscopy is limited in identifying tumor response; and in
one study, 41% of patients thought to have a complete pathologic response had
residual tumor identified at surgery
[10]. Barium studies may show
response of intraluminal tumor (Figs.
19A,
19B, and
19C) but are limited because
they cannot show mural disease and surrounding adenopathy. CT and endoscopic
sonography have also been used to document response. Decrease in wall
thickness and lymph node size may be shown on endoscopic sonography; however,
fibrosis may be indistinguishable from residual tumor. PET may also have a
role in documenting tumor response
[3].
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Fig. 19A. —69-year-old man with diagnosis of adenocarcinoma of
esophagus. Baseline esophagram shows polypoid mass (arrow) in mid
esophagus with distal Barrett's stricture (arrowheads) that is most
likely related to gastroesophageal reflux and hiatal hernia.
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Fig. 19B. —69-year-old man with diagnosis of adenocarcinoma of
esophagus. Follow-up radiograph obtained 6 months after A and after
chemotherapy and radiation shows no evidence of polypoid tumor. Note minimal
mucosal nodularity in distal esophagus that was proven as Candida
esophagitis at endoscopy.
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Fig. 19C. —69-year-old man with diagnosis of adenocarcinoma of
esophagus. Follow-up radiograph obtained 1 year after patient had completed
therapy shows recurrent polypoid esophageal mass (arrow).
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Radiation changes of the esophagus can be shown on imaging. Abnormal
peristalsis and dysmotility are the earliest and most common changes seen.
Mucosal edema and ulceration may be indistinguishable from other causes of
esophagitis. Esophageal carcinomas that respond to radiotherapy frequently
result in stricture formation that may require peroral dilatation
[11].
The ability to detect local recurrence is variable because inflammation or
fibrosis may cause esophageal wall thickening, mimicking tumor recurrence on
imaging. Mucosal changes at the anastomosis that represent recurrence may be
seen on barium studies. The overall accuracy of CT in detecting recurrence is
reported to be 87% [12] (Figs.
20A,
20B, and
20C). Care should be taken not
to overdiagnose recurrent tumor in an underdistended intrathoracic stomach on
imaging. Endoscopic sonography is reported to have a 20% false-positive rate
in detection of recurrence [3].
PET may be used to image recurrent tumor because it has the advantage of not
only detecting locally recurrent disease but also revealing any distant sites
of metastasis.
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Fig. 20A. —64-year-old woman with squamous cell carcinoma of esophagus.
Esophagram obtained after esophagogastrectomy and gastric pull-through shows
esophagogastric anastomosis (arrowheads). Stomach (S) can be seen in
chest.
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Fig. 20B. —64-year-old woman with squamous cell carcinoma of esophagus.
CT scan of chest obtained 8 months after A shows recurrent mass
(asterisk) in mediastinum at esophagogastric anastomosis with
associated tracheoesophageal fistula (arrowheads).
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In summary, esophageal carcinoma, although less common than other tumors of
the hollow viscera, continues to have a dismal 5-year prognosis. Curative
resection is possible in a small percentage of patients, and imaging studies
are important for determining resectability. Imaging is also helpful for the
evaluation of treatment effectiveness and for surveillance of recurrent
disease.
References
- Greenlee RT, Murray T, Bolden S, Wingo PA. Cancer statistics, 2000.
CA Cancer J Clin2000; 50:7
-33[Abstract]
- Gore RM. Esophageal cancer: clinical and pathologic features.
Radiol Clin North Am1997; 35:243
-263[Medline]
- Rankin S. Oesophageal cancer. In: Husband JES, Reznek RH, eds.
Imaging in oncology. Oxford, UK: Isis Medical Media,1998
: 93-110
- Levine MS. Esophageal cancer radiologic diagnosis.
Radiol Clin North Am1997; 35:265
-279[Medline]
- Saunders HS, Wolfman NT, Ott DJ. Esophageal cancer radiologic
staging. Radiol Clin North Am1997; 35:281
-294[Medline]
- Kimmey MB, Martin RW, Haggitt RC, et al. Histologic correlates of
gastrointestinal ultrasound images. Gastroenterology1989; 96:433
-441[Medline]
- Adelstein DJ, Rice TW, Tefft M, et al. Aggressive concurrent
chemo-radiotherapy and surgical resection for proximal esophageal squamous
cell carcinoma. Cancer1994; 74:1680
-1685[Medline]
- Carter R, Smith JS, Anderson JR. Laser recanalization versus
endoscopic intubation in the palliation of malignant dysphagia: a randomized
prospective study. Br J Surg1992; 79:1167
-1170[Medline]
- Petrovich Z, Langholz B, Formenti S, et al. Management of carcinoma
of the esophagus: the role of radiotherapy. Am J Clin
Oncol 1991;14:80
-86[Medline]
- Stahl M, Wilke H, Fink U, et al. Combined preoperative chemotherapy
and radiotherapy in patients with locally advanced esophageal cancer: interim
analysis of a phase II trial. J Clin Oncol1996; 14:829
-837[Abstract/Free Full Text]
- Lepke RA, Libshitz HI. Radiation-induced injury of the esophagus.
Radiology1983; 148:375
-378[Abstract/Free Full Text]
- Carlisle JG, Quint LE, Francis IR, et al. Recurrent esophageal
carcinoma: CT evaluation after esophagectomy.
Radiology1993; 189:271
-275[Abstract/Free Full Text]
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Introduction
Staging
