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433

Progress in Barrett’s Esophagus: A Radiologic


Radiology Diagnosis?

Marc S. Levine1 Barrett’s esophagus is a well-recognized condition characterized by a progres-


sive columnar metaplasia of the distal esophagus caused by chronic reflux esoph-
agitis. Despite its frequency, Barrett’s esophagus would not be important if it were
a benign entity. However, there is now considerable evidence that it is a premalig-
nant condition associated with a significantly increased risk of developing esopha-
American Journal of Roentgenology 1988.151:433-438.

geal adenocarcinoma. Unfortunately, the diagnosis of Barrett’s esophagus has


been limited on barium studies by a lack of clearly defined radiologic criteria that
are both sensitive to and specific for this condition. As a result, endoscopy and
biopsy generally have been advocated in order to make a definitive diagnosis.
However, recent data suggest that double-contrast esophagography may be a
valuable technique in determining the relative need for endoscopy and biopsy in
patients with reflux disease. The current status of Barrett’s esophagus is therefore
reviewed in this article, with particular emphasis on the role of radiology in
diagnosing this condition.

Pathogenesis and Prevalence

Barrett himself originally hypothesized that the underlying abnormality in Barrett’s


esophagus was a congenitally short esophagus with an attenuated intrathoracic
stomach masquerading as the columnar-lined lower esophagus [1 Subsequently,
].

it was postulated that this condition resulted from abnormal embryologic develop-
ment with incomplete squamous reepithelialization of the columnar-lined fetal
esophagus [2]. However, there is now considerable evidence that Barrett’s esoph-
agus is almost always an acquired condition with progressive columnar metaplasia
of the distal esophagus due to long-standing gastroesophageal reflux and reflux
esophagitis [3-8]. It is unclear why some patients with reflux esophagitis develop
Barrett’s esophagus and others do not. Nevertheless, recurrent episodes of
ulceration due to chronic reflux esophagitis apparently may cause the normal
squamous epithelium in the esophagus to be denuded and subsequently replaced
by a columnar epithelial lining.
Recent data suggest that this condition is more common than has previously
been recognized. In various studies, the prevalence of Barrett’s esophagus in
patients with refiux esophagitis has ranged from 8% to 20%, with an overall
prevalence of about 10% [9-12]. This figure may be skewed in favor of Barrett’s
esophagus, because patients with reflux symptoms who undergo endoscopy are
Received Apnl 6, 1988; accepted after revision . ..

May 17, 1988. likely to have significant reflux disease. Nevertheless, Barrett s esophagus is being
‘Department of Radiology, Hospital of the - diagnosed with greater frequency as the number of patients who undergo endos-
versity of Pennsylvania, 3400 Spruce St., Ptiiladel- copy increases.
phia, PA 19104. Address reprint requests to M. S. An association between Barrett’s esophagus and scleroderma has also been
Levine. .
recognized [13-151. In a recent study, 37% of all patients with scleroderma who
eber 1988 underwent endoscopy for symptoms of reflux esophagitis had biopsy-proved
© American Roentgen Ray Society Barrett’s esophagus [16]. The high prevalence of Barrett’s esophagus in patients
434 LEVINE AJR:1 51, September1988

with scleroderma is probably related to the severe esophagitis Thus, many investigators advocate periodic endoscopic sur-
that occurs in these individuals as a result of marked lower veillance with biopsy and cytology at 6-month or yearly inter-
esophageal sphincter dysfunction and poor clearance of re- vals for early detection of cancer in Barrett’s esophagus [5-
fluxed peptic acid from the esophagus [1 7]. Patients who 9, 1 8, 24-30]. However, it is unclear what measures should
have scleroderma therefore appear to be at even greater nsk be taken when endoscopy reveals dysplasia in these patients.
for developing Barrett’s esophagus than are other patients Although the presence of high-grade dysplasia or carcinoma-
who have reflux esophagitis. in-situ probably warrants an immediate esophagectomy, the
frequency with which low-grade dysplasia progresses to in-
vasive carcinoma is uncertain. Thus, many questions remain
Relationship to Adenocarcinoma
about endoscopic surveillance and the subsequent manage-
Barrett’s esophagus is important because it is a premalig- ment of patients who have known Barrett’s esophagus.
nant condition associated with a significantly increased risk Much less frequently, the development of cancer in Bar-
of developing esophageal adenocarcinoma. In various stud- rett’s esophagus results from an adenoma-carcinoma se-
ies, the prevalence of adenocarcinoma in patients who have quence similar to thatfound in the colon. Benign adenomatous
Barrett’s esophagus has ranged from 2.4% to 46.5%, with polyps have occasionally been seen in patients who have
an overall prevalence of about 15% [9, 1 1 12, 18-20].
, Barrett’s mucosa, with or without focal areas of invasive
Prevalence data may exaggerate the risk of cancer, because adenocarcinoma [20, 31 32]. Because malignant degenera-
,

most patients with Barrett’s esophagus do not seek medical tion of adenomatous tissue represents another potential path-
attention until complications such as ulcers, strictures, or way for the development of adenocarcinoma, endoscopic
malignancy develop. Nevertheless, recent studies that used resection of these polyps may decrease the risk of cancer.
incidence data rather than prevalence data indicate that the Early adenocarcinomas arising in Barrett’s esophagus may
American Journal of Roentgenology 1988.151:433-438.

risk of developing adenocarcinoma is perhaps 30-40 times appear on double-contrast esophagography as plaquelike
greater in patients who have Barrett’s esophagus than in the lesions or as flat, sessile polyps with a smooth or slightly
general population [21, 22]. lobulated contour [33]. Early carcinomas may also be mani-
The sequence of events leading to the development of fested by focal irregularity, nodulanty, flattening, and/or ul-
adenocarcinoma in Barrett’s esophagus has been the subject ceration of the esophageal wall (Fig. 1A). Thus far, most early
of considerable interest. In numerous studies, histologic ex- lesions reported in the radiologic literature have been discov-
amination of resected specimens has revealed dysplasia and/ ered fortuitously during radiologic evaluation of reflux symp-
or carcinoma-in-situ within Barrett’s mucosa adjacent to or toms [33]. However, asymptomatic lesions could also be
remote from the primary tumor [8, 20, 23-28]. It therefore is detected by radiologic surveillance of patients who have
widely believed that adenocarcinoma evolves through a se- known Barrett’s esophagus. In my opinion, an optimal screen-
quence of progressively severe epithelial dysplasia, carci- ing program for these patients therefore might alternate dou-
noma-in-situ, and invasive carcinoma in preexisting areas of ble-contrast esophagography and endoscopy at 6-month in-
columnar metaplasia. These dysplastic or carcinomatous tervals in the hopes of detecting early cancer and/or dysplasia
changes can be recognized by endoscopic biopsy or cytology. in Barrett’s esophagus at the earliest possible stage.

Fig. 1.-Adenocarcinoma in three


patients who have Barrett’s esopha-
gus.
A, Relatively long peptic stricture
in distal esophagus with irreguiar flat-
tening of one wali of stricture (arrows).
At surgery, patient had early adenocar-
cinema in Barrett’s esophagus with ma#{149}
iignant involvement confined to mu-
cosa (Reprinted from Levine et al.
[33].)
B, Advanced, Infiltrating lesion in
distal esophagus.
C, Polypold lesion (white arrow) In
distal esophagus, invading stomach.
Note how normal anatomic landmarks
at cardia have been obliterated and
replaced by irregular areas of ulcera-
tion (black arrows). At surgery, this pa-
tient had a primary adenocarcinoma
arising in Barrett’s esophagus with sec-
ondary gastric involvement.
AJR:151, September1988 BARRETT’S ESOPHAGUS 435

Like squamous cell carcinomas, advanced adenocarcino- Endoscopic and Histologic Diagnosis
mas arising in Barrett’s esophagus may appear grossly as
infiltrating, polypoid, ulcerated, or, less frequently, varicoid In Barrett’s esophagus, the squamocolumnar mucosaljunc-
lesions (Figs. 1 B and 1C) [20, 34, 35]. However, these tumors tion is located above the proximal border of the lower esoph-
can be differentiated from squamous cell carcinomas by their ageal sphincter, and the columnar mucosa can extend proxi-
frequent tendency to invade the stomach (Fig. 1C). At one mally as a continuous sheet, fingerlike projections, or isolated
time, tumors involving the gastroesophageal junction were islands of columnar epithelium [8]. These islands of Barrett’s
almost always thought to arise in the stomach and were mucosa may be separated from the gastroesophageal junc-
classified as primary gastric carcinomas that had secondarily tion by residual areas of normal squamous epithelium, so that
invaded the lower end of the esophagus [36-39]. Thus, random biopsies of the distal esophagus can be misleading.
esophageal adenocarcinoma was thought to be a rare entity. Although Barrett’s metaplasia is often confined to the distal
However, recent studies suggest that as many as 20-50% third of the esophagus, it may extend as far proximally as the
of these tumors involving the gastroesophageal junction arise aortic arch.
in Barrett’s mucosa and subsequently spread into the stom- The endoscopic diagnosis of Barrett’s esophagus is based
ach [20, 34, 35]. Although Barrett’s esophagus could con- on characteristic changes in the texture and color of the
ceivably occur as a fortuitous finding in patients with primary epithelium, as Barrett’s mucosa typically has a velvety, pink-
gastric carcinomas invading the esophagus, examination of ish-red appearance in contrast to the flat, relatively pale
resected specimens has usually revealed one or more areas appearance of the normal squamous epithelium above. Al-
of esophageal dysplasia and/or carcinoma-in-situ adjacent to though biopsies are required for a definitive diagnosis, endos-
or remote from the proximal margin of the tumor [20, 23, copy has a sensitivity of greater than 90% in diagnosing
34]. Because one would not expect to find dysplastic changes Barrett’s esophagus solely on the basis of the endoscopic
American Journal of Roentgenology 1988.151:433-438.

beyond the leading edge of a gastric carcinoma invading the appearance [40, 41].
esophagus, the pathologic evidence strongly suggests an Histologically, the columnar-epithelial lining in Barrett’s
esophageal origin of these lesions with subsequent spread esophagus is not simply gastric mucosa but a mosaic of
into the stomach. When these cases have been classified intimately admixed glandular and cell types from the stomach
correctly, adenocarcinomas arising in Barrett’s mucosa ac- and small bowel, induding a gastric-fundic type epithelium
count for 5-20% of all esophageal cancers [20, 35]. This with parietal and chief cells, a junctional type epithelium with
disease has therefore become an important problem in mod- cardiac mucous glands, and a specialized columnar or intes-
em medical practice. tinal type epithelium with a villiform configuration, mucous
glands, and intestinal-like goblet cells [23, 42]. The latter
epithelium is particularly important, because it permits Bar-
Clinical Aspects rett’s mucosa to be differentiated unequivocally from mad-
vertent gastric biopsies. One or more foci of low- or high-
Barrett’s esophagus may occur in adults of all ages but is grade dysplasia, carcinoma-in-situ, or invasive carcinoma may
more common in older individuals with long-standing reflux be present in Barrett’s mucosa. However, some investigators
esophagitis. There is no apparent sex predilection. These believe that the risk of malignant degeneration is greatest in
individuals may be asymptomatic, they may have reflux- preexisting areas of intestinal metaplasia [26].
related symptoms (i.e., heartburn, substemal chest pain, and
regurgitation) or low-grade upper gastrointestinal bleeding
due to underlying reflux esophagitis, or they may have dys- Radiologic Diagnosis
phagia due to the development of benign strictures [4, 5]. As
these superimposed strictures progress, dysphagia may be- The classic radmologic features of Barrett’s esophagus con-
come the dominant clinical feature and reflux symptoms may sist of a high esophageal stricture or ulcer associated with a
completely disappear. sliding hiatai hernia and/or gastroesophageal reflux [4, 43-
The development of adenocarcinoma is not confined to the 45]. The unusual location of these strictures and ulcers has
middle-aged or elderly patient with Barrett’s esophagus but been attributed to the fact that they often occur in the most
may occur in young people with this disease [18, 20, 29]. proximal segment of columnar epithelium at or near the
Clinicians therefore should not be lulled into a false sense of squamocolumnar junction [44]. However, others have found
security about the possibility of malignancy because of the that strictures may occur in squamous epithelium above the
patient’s age. The most common presenting findings (i.e., level of the squamocolumnar junction [45]. Whatever their
dysphagia, weight loss, and upper gastrointestinal bleeding) precise location, the pathologic basis of these strictures is
may be indistinguishable from those of patients with reflux uncertain.
esophagitis or benign peptic strictures. However, patients High strictures in Barrett’s esophagus usually appear radio-
with adenocarcinoma arising in Barrett’s esophagus fre- graphically as ringlike constrictions or as smooth, tapered
quently have long-standing reflux symptoms, such as heart- areas of narrowing in the midesophagus (Fig. 2) [43]. So-
burn and regurgitation, so that any individual with chronic called “Barrett’s ulcers” tend to be relatively deep ulcer craters
reflux symptoms should be followed closely for the develop- within Barrett’s mucosa at a considerable distance from the
ment of Barrett’s esophagus and subsequent adenocarci- gastroesophageal junction (Fig. 3) [46]. When such strictures
noma. or ulcers are detected in patients with sliding hiatal hernias
436 LEVINE AJR:151, September1988

contrast esophagography if a reticular mucosal pattern is


used as the primary radiologic criterion for diagnosing this
condition.
Because Barrett’s esophagus develops as the sequela of
long-standing reflux esophagitis, it is not surprising that these
patients often have radiologic evidence of hiatal hernias,
gastroesophageal reflux, reflux esophagitis, and/or peptic
strictures (Fig. 5) [44, 45, 47-51]. In one study, 97% of
patients with Barrett’s esophagus had esophagitis or stric-
tures on double-contrast esophagrams [45]. However, these
findings frequently occur in patients with uncomplicated reflux
disease. As a result, inclusion of these findings as criteria for
Barrett’s esophagus increases the sensitivity of the radiologic
examination but decreases its specificity, so that many pa-
tients would be referred unnecessarily for endoscopy and
biopsy [51]. Thus, radiographic findings that are relatively
specific for Barrett’s esophagus are not sensitive, and those
that are sensitive are not specific. Many investigators there-
fore believe that esophagography has limited value as a
screening examination for Barrett’s esophagus and that en-
doscopy and biopsy are required to diagnose this condition.
American Journal of Roentgenology 1988.151:433-438.

Recently, however, Gilchrist et al. [53] performed a blinded,


retrospective study in 200 patients who had both double-
contrast esophagrams and endoscopy because of severe
reflux symptoms. The patients were classified into high-,
moderate-, and low-risk groups for Barrett’s esophagus on
the basis of the radiographic findings. Patients were classified
Fig. 2.-A and B, Barrett’s esophagus with high strictures appearing as as high risk for Barrett’s esophagus if the radiographs re-
ringlike constriction (arrow in A) and as a smooth, tapered area of narrow- vealed a high stricture or ulcer or a reticular mucosal pattern,
ing (arrow in B). When associated hiatai hernia, gastroesophageal refiux,
and/or reflux esophagitis are present, Barrett’s esophagus should be at moderate risk if the radiographs revealed a distal peptic
strongly suggested. stricture and/or reflux esophagitis (because previous studies
have shown that about 45% of patients with peptic strictures
[54] and 1 0% with reflux esophagitis [9-1 2] have Barrett’s
and/or gastroesophageal reflux, a confident diagnosis of Bar- esophagus), and at low risk if none of these findings were
rett’s esophagus can be made on radiologic grounds. How- present. When these radiologic criteria were used, 1 0 patients
ever, recent studies have found that strictures are actually (5%) were thought to be at high risk, 73 (37%) at moderate
more common in the distal esophagus and that the majority risk, and 1 1 7 (58%) at low risk for Barrett’s esophagus.
of cases do not fit the classic description of a high stricture Endoscopic correlation revealed biopsy-proved Barrett’s mu-
or ulcer [47-50]. Thus, esophagography is an inadequate cosa in nine (90%) of 1 0 patients at high risk, in 1 2 (1 6%) of
screening examination when the diagnosis is restricted to 73 at moderate risk, and only one (<1 %) of 1 17 at low risk
patients who have the classic radiologic features of this for Barrett’s esophagus.
condition. Although the overall sensitivity in diagnosing reflux esoph-
A reticular mucosal pattern has recently been described as agitis was only 53%, most of the cases of reflux esophagitis
a relatively specific sign of Barrett’s esophagus on double- that were missed radiographically were mild, and only one of
contrast esophagography, particularly if located adjacent to those patients had Barrett’s esophagus. The data suggest
a stricture [48]. This reticular pattern is characterized radio- that esophagitis that is severe enough to cause Barrett’s
graphically by innumerable, tiny barium-filled grooves or crev- esophagus can almost always be detected on technically
ices on the esophageal mucosa, often resembling the areae adequate double-contrast examinations. This observation has
gastricae pattern found on double-contrast studies of the important implications for the management of patients, be-
stomach. In most cases, there is an adjacent stricture in the cause unnecessary endoscopy can be avoided when there is
mid or, less frequently, distal esophagus, with the reticular no radiologic evidence of esophagitis or stricture formation.
pattern extending distally a short but variable distance from On the basis of the study by Gilchrist et al. [53], it seems
the stricture (Fig. 4) [48]. When present, this finding should reasonable to classify patients into high-, moderate-, and low-
be highly suggestive of Barrett’s esophagus, and endoscopy risk groups for Barrett’s esophagus by results of double-
and biopsy should be performed for a definitive diagnosis. contrast esophagography. Patients who are at high risk for
However, this finding has been observed in only 5-30% of Barrett’s esophagus because of a high stricture or ulcer or a
patients with Barrett’s esophagus [45, 48-51], and its spec- reticular mucosal pattern should undergo early endoscopy
ificity has also been questioned [52]. Thus, the majority of and biopsy for a definitive diagnosis. A larger group of patients
cases of Barrett’s esophagus will be missed on double- are at moderate risk for Barrett’s esophagus because of
AJR:151, September1988 BARRETT’S ESOPHAGUS 437
American Journal of Roentgenology 1988.151:433-438.

A B

Fig. 3.-Barrett’s esophagus with high ulcer. Note relatively deep ulcer Fig. 5.-A andB, Barrett’sesophagus associated with refiux esophagitis
crater (arrow) at greater distance from gastroesophageal junction than (A) and peptic stricture (B). Note nodular, irregular mucosa and thickened
expected for uncomplicated refiux esophagitls. longitudinal folds in A and smooth, distal stricture (arrow) In B. Because
Fig. 4.-Barren’s esophagus with high stricture and retlcuiar mucosal the latter findings occur in patients with uncomplicated refiux disease,
pattern. Note early stricture with siight flattening (whit. arrows) of one wali Barrett’s esophagus cannot be diagnosed confidently on radlologic
of midesophagus and deilcate reticular pattern (black arrows) adjacent to grounds. However, these patients may be classified radlographicaily into
distai aspect of stricture. This reticular pattern should be highly suggestive various risk groups for Barrett’s esophagus in order to determine the
of Barrett’s esophagus but Is found in only a minority of cases. relativeneed forendoscopy and blopsy(seetext).(Reprlnted from Gilchrist
et ai. [53].)

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