951

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The Radiologic Diagnosis of Barrett Esophagus: Importance of Mucosal Air-Contrast

Seth N. Glick1 Steven K. Teplick2 Peter S. Amenta3

with Barrett esophagus are predisposed to the development of esophageal Identification of these patients before this complication develops is essential. We prospectively made the diagnosis of Barrett esophagus on routine biphasic upper gastrointestinal series in nine patients in whom a mucosal surface pattern alteration was the only radiologic abnormality on the esophagogram. The diagnosis was confirmed by biopsy in eight patients and during surgery in one patient. Only a third of the patients had symptoms related to the esophagus. Two types of surface changes were noted. A reticular pattern was present in six cases and a villous pattern in five cases. Both patterns were noted in two patients. This series was obtained in a 5-year interval during which there were 15 additional patients with Barrett esophagus and corresponding esophagograms. None of these patients had normal results on esophagograms. Recognition of these subtle surface patterns, particularly in the absence of other

AJR

revision

I Department of Diagnostic Radiology. Hahnemann University Hospital, Broad and Vine Sts., Philadelphia, PA 19102. Address reprint requests to S. N. Glick. 2 Department of Diagnostic Radiology, University

of Arkansas

for Medical

ham, Little Rock,

Science,

4301

W. Mark-

AR 72205.

Department of Pathology, Robert Wood Johnson University-University of Medicine and Dentistry of New Jersey, 1 Robert Wood Johnson Place, New Brunswick, NJ 08903-0019.

abnormalities,

may

improve

of patients for subsequent November

157:951-954,

detection

of

Barrett

esophagus

and

aid

in

surveillance.

1991

Columnar metaplasia of the esophageal mucosa (Barrett esophagus) associated with gastroesophageal reflux is recognized as a premalignant condition. Definitive diagnosis of Barrett esophagus usually occurs during endoscopic examination of patients with severe symptoms of gastroesophageal reflux or dysphagia from associated stricture. However, many patients do not undergo endoscopic examination unless the characteristic radiologic findings of a midesophageal stricture or a deep ulcer are discovered. A reticular mucosal pattern also has been described [1 ] as highly predictive of Barrett esophagus, but almost all previously reported cases were associated with the typical abnormalities. During a 5-year period, we examined nine patients in whom an abnormal mucosal surface pattern was the only structural finding on the esophagogram. In each case, the diagnosis of Barrett esophagus was made prospectively on the basis of the radiographs. Thus, the radiologic sensitivity for Barrett esophagus can be improved by recognition of these features, particularly in the absence of other suggestive findings.

Subjects During

and Methods a 5-year period,

patients

solely

contrast

esophagogram.

3

0361 -803X/91/1 575-0951 C American Roentgen Ray Society

on

Patients

reflux-induced

after

Abnormalities Studies

adenocarcinoma.

the selection

Received April 1 5, 1991 : accepted June6, 1991.

Surface Barium

old (mean, symptoms,

on

the

a radiologic

basis

of

diagnosis

detection

of

an

of Barrett abnormal

esophagus mucosal

was made in nine

surface

pattern

on

air-

34 to 68 years 55 years). Four were younger than 50 years old. Only three (33%) had esophageal and

The

in only

two

heartburn

or regurgitation).

remaining

six

(66%)

patients

patients

of these The

third were

were

could patient being

six

the

men

and

symptoms had

studied

three

women

be directly

hiccups

and

vague

for

nonesophageal

from

attributed chest signs

to reflux

(i.e.,

discomfort. or

symptoms,

The

952

GLICK

including with

upper

The upper

(one

esophagus

distinct

was

or discomfort

evaluated series.

as

The

(five

of surface

patterns

part

of

studies

a special interest

with

types

pain

cases)

and

anemia

case).

gastrointestinal

radiologist

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abdominal

indigestion

the

were

routine

in gastrointestinal were

noted.

biphasic

interpreted

The

by

radiology. first

was

one

Two

a reticular

pattern similar to that reported by Levine et al. [1]. This pattern was present in six patients and it appeared as a course network of intersecting

lines

configuration scribed patients

and to

barium 1 A).

producing

The

other

an

angular

or

round

which

has

not

pattern,

was termed the villous pattern.

before,

similar

of

(Fig.

it appeared

the

villi

of

as tiny, the

uniform,

duodenum

1 B).

shown in two patients. Eight of the nine patients

had endoscopy

within

study.

1 month

of the

barium

In the

de-

This was noted in five

confluent,

(Fig.

mosaic been

round Both

and biopsy remaining

lucencies,

patterns

were

performed

patient,

esoph-

ageal adenocarcinoma developed 9 months later, and Barrett mucosa was found adjacent to the neoplasm (Figs. 2A and 2B). No falsepositive the

radiologic

diagnoses

of Barrett

basis of these criteria. The pathology records were reviewed

the

cases

of Barrett

esophagus

esophagus

were

in order

to determine

diagnosed

by

biopsy

made

on all of

during

this

5-

year interval. Twenty-two cases were noted, and 15 had esophagograms obtained before this disease was documented. The films and initial

reports

of these

alence of isolated inclusion

of this

the diagnosis The

studies

mucosal

group

were

reviewed

abnormalities

of patients

to determine

the

and to ascertain

affected

our

overall

prey-

whether

sensitivity

for

of Barrett esophagus.

radiographs

were

obtained

by

using

air-contrast

technique

after the patient had ingested E-Z HO barium (250% w/v, E-Z-EM, Inc., Westbury, NY) and E-Z Gas (E-Z-EM, Inc.). Studies were performed with high-speed, double-contrast, blue-sensitive film and mr 400 rare-earth screens (Agfa Corp., Ridgefield Park, NJ). The focal spot of the fluoroscopic equipment varied from 0.3 mm to 1 .2 mm, but in most of the cases was 0.6 mm.

Results In all six patients in whom the villous pattern was seen, the distal 5 cm of the esophagus was involved in a diffuse (four cases) or circumscribed (two cases, Fig. 3) manner. In three of the four in whom the changes were diffuse, they extended proximally to the level of the carina. The reticular pattern was confined to the mid esophagus and was focal in two of the

ET AL.

AJR:157,

November

1991

five patients in whom it occurred (Fig. 4). In two other patients, this pattern was present in the mid esophagus but extended throughout the esophagus, including the distal portion in both. In one patient, the reticular pattern was isolated to the distal 5 cm of the esophagus. In the two patients in whom both patterns were present, the villous pattern was located distal to the reticular pattern. In two patients with the diffuse villous pattern, fine linear striations parallel to the long axis of the esophagus were noted when the esophagus was slightly less distended (Fig. 5). All ofthe patients had marked gastroesophageal reflux. The region of the lower esophageal sphincter was patulous in all cases. A hiatal hernia was noted n only two patients, but maneuvers to show this were not done. The endoscopic results suggested Barrett esophagus in all eight cases. In four patients, this was the only abnormality observed. Two patients had mild friability or erythema, and the remaining two patients each had one superficial erosion. Biopsy in each case showed columnar metaplasia. A review of the histologic subtypes revealed five patients with both the intestinal and cardia types, one of whom had high-grade dysplasia. Two patients had only the cardia type, and one patient had the intestinal type. In the patient with adenocarcinoma, only the fundal type was present; however, the possibility that the other types had been obliterated by the malignant process could not be excluded. Fifteen additional patients with histologically proved Barrett esophagus had recent prior esophagograms. Five (33%) of these patients had midesophageal strictures, and the accurate prospective diagnosis of Barrett esophagus was made. The remaining 1 0 patients had esophagitis and/or distal stricture on the barium study. Thus, patients with isolated abnormalities of surface pattern constituted 38% of all patients with Barrett esophagus. The overall radiologic sensitivity for this diagnosis was 58%, and no patient with Barrett esophagus had a normal esophagus. All had either abnormal surface patterns or reflux-induced pathologic changes.

Discussion The concept that Barrett esophagus is a sequela of gastroesophageal reflux and that patients with this condition are predisposed to the development of adenocarcinoma of the

Fig. 1.-A, Reticular pattern. Air-contrast esophagogram of 48-year-old man with discomfort in right upper quadrant shows a network of intersecting lines of barium in mid esophagus, producing angular and round mosaic pattern. These changes extended to gastroesophageal junction. Biopsy showed columnar epithelium of cardia type. B, Villous pattern. 68-year-old woman with anemia. Air-contrast esophagogram at level of left main bronchus shows diffusely distributed, tiny, confluent, round lucencies resembling villi of small intestine. Both specialized and cardia types of Barrett mucosa were noted on biopsy.

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Fig. 2.-A, 65-year-old man with hiccups and vague discomfort in chest. A fine villous pattern was noted in distal esophagus on air-contrast study. Barrett esophagus was suggested, and endoscopy was recommended but not performed. B, 9 months later, patient returned with dysphagia, and an esophagogram showed an ulcerating mass just proximal to gastroesophageal junction. Resected specimen showed infiltrating adenocarcinoma with adjacent fundal-type columnar mucosa. Superficial carcinoma was most likely present when first study was done.

B

A

Fig. 3.-SO-year-old woman with periumbilical discomfort. villous pattern is identified on air-contrast gastroesophageal junction. Remainder of esophagus appeared normal. Biopsy showed specialized-type Fig. 4.-62-year-old man with a 6-month history of heartburn. Patient also had a focal villous patch (not seen here) just proximal types of Barrett epithelium were seen on biopsy.

study as a focal columnar mucosa.

Air-contrast esophagogram shows reticular pattern to gastroesophageal junction. No other abnormalities

(arrow) were

patch

(arrow)

just

proximal

to

confined to mid esophagus. seen. Specialized and cardia

Fig. 5.-Air-contrast esophagograms of a 34-year-old man with pain across upper abdomen. A, With slight underdistension, villous pattern may manifest as fine linear striations parallel to longitudinal axis of esophagus. This should not be confused with longitudinal folds. B, With further distension, villous pattern can be readily seen, producing a velvety texture to normally smooth esophageal surface. Biopsy showed specialized columnar epithelium.

esophagus is well established. The cost-effectiveness of routine endoscopic surveillance of these patients is controversial, and the value of this approach depends on the magnitude of the risk of malignant degeneration. Although initial retrospective studies reported a low incidence of malignant transformation, prospective studies have found an annual incidence of 1 -2% [2, 3]. Although the issue of cost-effectiveness

remains to be clarified, detection of Barrett esophagus surveillance before the development of carcinoma can in a greater number of curable malignant lesions. Unfortunately many cases of Barrett esophagus go tected. The prevalence of this condition in the general lation may be much greater than predicted from clinical ords. Cameron et al. [4] compared the number of cases

and result undepopurecfound

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954

GLICK

at autopsy with the number of clinically diagnosed cases in a defined population and determined that the prevalence of unrecognized cases was 20 times greater than the number of patients who had diagnostic investigation. This may be related to the fact that reflux symptoms are frequently treated empirically. However, in many patients, signs and symptoms of reflux are minimal or nonexistent. Approximately 20-40% of patients with Barrett esophagus do not have reflux symptoms or even symptoms that suggest esophageal disease [5, 6]. It is not surprising that in patients with adenocarcinoma in Barrett esophagus a history of reflux symptoms is absent in 23-58% (mean, 36%) [7, 8]. Our finding of classic reflux symptoms in only two of our nine cases is consistent with these data. In addition, two of our nine patients had malignant or premalignant changes in the absence of signs or symptoms or significant inflammatory pathologic changes. Although endoscopy with biopsy has a major role in the management of patients with Barrett esophagus, initial detection requires appropriate selection for this procedure. The value of barium studies is unclear. A prospective radiologic diagnosis of Barrett esophagus by using suggestive criteria is possible in only 25-45% of cases [9, 1 0]. However, it has been shown that the barium study is highly sensitive in detecting reflux-induced pathologic changes that are severe enough to be associated with Barrett esophagus [9, 1 1]. When nonspecific reflux esophagitis and/or scarring is included with the characteristic appearances, more than 95% of cases of Barrett esophagus can be detected. It is extremely rare for Barrett esophagus to be overlooked when esophagographic findings are normal, making this study an effective tool for predicting which patients can benefit from endoscopy. In one study, 58% of patients with reflux symptoms would have been spared the more invasive procedure [1 1]. We describe two types of mucosal surface patterns that not only are highly predictive for Barrett esophagus but also may be the only structural abnormalities visible on the barium study. The villous pattern has not been described before. The reticular pattern was initially reported by Levine et al. [1 ] and has been seen in 5-30% [1 9, 1 2-i 4] of patients with Barrett esophagus. The specificity ofthis finding has been questioned [1 2], but this discrepancy may represent differences in interpretation. In previous reports, the reticular pattern has almost always been associated with other radiologic abnormalities suggestive of Barrett esophagus. Thus, while further supporting the diagnosis, detection of a reticular pattern under these circumstances would not significantly improve the yield even if the more liberal screening criteria were used. However, the study of Gilchrist et al. [1 1] included only patients with reflux symptoms, and patients with reflux symptoms and/or dysphagia may be more likely to have other findings. This is supported by the presence of classic reflux symptoms in only 22% of our patients. The histologic basis for these mucosal surface patterns remains obscure. Levine et al. [1 ] suggested that the reticular pattern may represent specialized columnar epithelium. Specialized epithelium was present in 75% of our patients (excluding the patient with carcinoma). However, specialized epithelium is the most common histologic subtype and is found in a similar percentage of patients with Barrett esoph,

ET AL.

AJR:157,

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1991

agus. Furthermore, it is impossible to correlate the biopsy sites precisely with the location of the radiologic surface pattern in all cases, although in those patients with a diffuse distribution, such an association could be assumed. Specialized epithelium may be the only type present or may occur in conjunction with the other types. In the latter setting, it is invariably found most proximally in the esophagus. We noted a tendency for the reticular pattern to be located more proximally than the villous pattern, but whether this is related to histologic differences between the two patterns is unknown. Radiologic studies can make a significant contribution through the appropriate selection of patients for endoscopy. Although implementation of the criteria of Gilchrist makes the value of a specific radiologic diagnosis of Barrett esophagus less crucial, not all patients with nonspecific reflux-related abnormalities, especially when signs and symptoms are mmimal, will be referred for endoscopy. A more definitive radiologic diagnosis may provide the impetus for aggressive management. Furthermore, recognition of an abnormal surface pattern on a barium study as the sole structural abnormality, particularly as an incidental observation not obviously related to the indication for the examination, should improve the detection of a condition whose prevalence is greater than generally is recognized.

REFERENCES 1 . Levine MS. Kressel HY, Caroline DF, Laufer I, Herlinger H, Thompson JJ. Barrett esophagus: reticular pattern of the mocusa. Radiology 1983:147:663-667 2. Hameeteman W, Tytgat GN, Houthoft HJ, van den Tweel JG. Barrett’s esophagus: development of dysplasia and adenocarcinoma. Gastroenterology 1989:96: 1249-1 256 3. Robertson CS, Mayberry JF, Nicholson DA, James PD, Atkinson M. Value of endoscopic surveillance in the detection of neoplastic change in Barrett’s oesophagus. Br J Surg 1988:75:760-763 4. Cameron AJ, Zinsmeister AR, Ballard DJ, Carney JA. Prevelance of columnar-lined Barrett’s esophagus: comparison of population-based clinical and autopsy findings. Gastroenterology 1990:99:918-922 5. Cooper BT, Barbezat GO. Barrett’s oesophagus: a clinical study of 52 patients. 0 J Med 1987:62:97-108 6. Kerlin P. D’MeIIow G, Van Deth A. Barrett’s esophagus: clinical, endoscopic, and histologic spectrum in fifty patients. Aust N Z J Med 1986:16:198-205 7. Saubier EC, Gouillat C, Samaniego C, Guillaud M, Moulinier B. Adenocarcinoma in columnar-lined Barrett’s esophagus: analysis of 1 3 esophagectomies. Am J Surg 198:150:365-369 8. Witt TA, Bains MS, Zaman MB, Martini N. Adenocarcinoma in Barrett’s esophagus. J Thorac Cardiovasc Surg 1983:85:337-345 9. Chen YM, Gelfand DW, Ott DJ, Wu WC. Barrett esophagus as an extension of severe esophagitis: analysis of radiologic signs in 29 cases. AJR 1985:145:275-281 1 0. Winters C, Spurling TJ, Chobanian SJ, et al. Barrett’s esophagus: a prevalent, occult complication of gastroesophageal reflux disease. Gastroenterology 1987:92: 1 18-1 24 1 1 . Gilchrist AM, Levine MS, Can’ AF, et al. Barrett’s esophagus: diagnosis by double-contrast esophagography. AJR 1988:150:97-102 12. Vincent ME, Robbins AH, Spechler SJ, Schwartz A, Does WG, Schimmel EM. The reticular pattern as a radiographic sign of the Barrett esophagus: an assessment. Radiology 1984:153:333-335 13. Shapir J, DuBrow A, Frank P. Barrett oesophagus: analysis of 19 cases. Br J Radiol 1985:58:491-493 14. Agha FP. Radiologic diagnosis of Barrett’s esophagus: critical analysis of 65 cases. Gastrointest Radiol 1986:1 1 :123-1 30