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Original Report |
1 All authors: Department of Radiology, Hospital of the University of Pennsylvania, 3400 Spruce St., Philadelphia, PA 19104.
Received August 16, 1999;
accepted after revision September 22, 1999.
Address correspondence to M. S. Levine.
Abstract
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CONCLUSION. The foamy esophagus was characterized by innumerable tiny (1-3 mm), round lucencies (bubbles) that intermingled with the barium suspension along the top of the barium column, producing a layer of foam. Candida esophagitis should be strongly suspected when a foamy esophagus is detected on double-contrast esophagography, particularly in patients with underlying esophageal involvement by scleroderma.
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The six patients with proven or presumed Candida esophagitis comprised our study group. The average age of our six patients was 51 years (range, 30-72 years). One patient was a man and the other five were women. The radiographs from these six patients were reviewed retrospectively to characterize the radiographic features of the foamy esophagus and assess the presence or absence of associated radiographic findings of Candida esophagitis, including plaques or a "shaggy" esophagus. The radiology reports were also reviewed to determine whether these patients had functional or mechanical obstruction of the esophagus, conditions that can predispose patients to the development of Candida esophagitis [2]. Finally, patient records were reviewed to determine the clinical presentation, treatment, and subsequent patient course. None of the patients in our series had follow-up barium studies after treatment.
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Radiographic Findings
In all six patients, the foamy esophagus was manifested on double-contrast
esophagography by innumerable tiny (1-3 mm), smooth, round lucencies (bubbles)
along the top of the barium column on upright views of the esophagus,
producing a layer of foam that had an average height of 8.2 cm (range, 3-16
cm) (Figs.
1,2,3,4,5).
In all six cases, the bubbles were freely mobile, some traveling down the
esophagus as the barium column emptied into the stomach. In two patients, the
bubbles were also seen in the esophagus on prone single-contrast views as
tiny, rounded lucencies that traveled with the barium column into the
stomach.
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Of the five patients with known scleroderma, double-contrast esophagrams revealed additional evidence of Candida esophagitis in four, with nodular, plaquelike lesions in the mid esophagus above the level of the barium column and intermingling foam in three (Fig. 4) and a finely nodular or lacy appearance of the mucosa in one. One of these five patients also had esophageal intramural pseudodiverticulosis in the distal esophagus (Fig. 4). In all five patients with scleroderma, the barium studies also revealed the typical esophageal motility disorder of scleroderma, with a dilated, flaccid esophagus, absent primary esophageal peristalsis below the level of the aortic arch, a patulous gastroesophageal junction, and free gastroesophageal reflux. All five of these patients had hiatal hernias with smooth, tapered peptic strictures in the distal esophagus above the hernias (Figs. 3 and 4). The strictures had an average width of 1.2 cm (range, 0.7-2.0 cm) and an average length of 2.3 cm (range, 1.5-3.0 cm).
The remaining patient with a foamy esophagus had irregular narrowing of the distal esophagus with ulceration and intramural tracking in this region caused by presumed Candida esophagitis (Fig. 5). This patient also had intermittent weakening of primary peristalsis in the lower thoracic esophagus, possibly because of the underlying esophagitis.
Endoscopic Findings
In all three patients who underwent endoscopy, copious amounts of bubbly
foam were seen to fill the esophagus. In two patients, this foam was adherent
to the esophageal wall. In all three, the underlying esophageal mucosa had a
friable, erythematous appearance. Microbiologic cultures from the esophagus
were positive for candidiasis in all three patients.
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Double-contrast esophagography has been shown to have a sensitivity as high as 90% in the diagnosis of Candida esophagitis in relation to endoscopy [6, 7]. The radiographic findings of this condition have been well documented. Candida esophagitis is usually manifested on barium studies as discrete, linear, or irregular plaquelike lesions separated by segments of normal intervening mucosa [5,6,7]. In more advanced disease, coalescent plaques may produce a "cobblestone" or "snakeskin" appearance [8] or, in severe cases (usually patients with AIDS), a grossly irregular or shaggy esophagus caused by extensive plaque and pseudomembrane formation with trapping of barium between these lesions [5, 6].
In this report, we describe a new radiographic sign of Candida esophagitis, the foamy esophagus, that was encountered in six patients with this condition. In all six patients, the foamy esophagus was manifested on double-contrast esophagography as innumerable tiny (1-3 mm), round lucencies (bubbles) that intermingled with the barium suspension along the top of the barium column, producing a layer of foam (Figs. 1,2,3,4,5). The bubbles had a relatively uniform size and shape; some traveled with the barium column into the stomach both on upright double-contrast and prone single-contrast views of the esophagus.
Although undissolved effervescent granules could produce a similar appearance on double-contrast esophagography [9], all the esophagrams in our series were obtained before administration of effervescent agent, eliminating this possibility. The foamy esophagus could also be mistaken for a debris-filled esophagus, but retained food and debris would not be expected to appear radiographically as tiny, uniformly round lucencies in the esophagus. Finally, the foamy esophagus could conceivably be confused with a diffusely nodular esophagus on one or more static spot images. However, the mobile nature of these tiny bubbles was readily apparent on fluoroscopy, differentiating this finding from true mucosal nodules. The foamy esophagus of candidiasis therefore can be distinguished from double-contrast artifacts or diffuse nodularity of the mucosa on the basis of the imaging findings.
Although a foamy esophagus was detected radiographically in 10 patients, four did not have adequate clinical follow-up to confirm or refute a diagnosis of Candida esophagitis. Even if we assume that these four patients did not have candidiasis, 60% of our patients with a foamy esophagus on double-contrast esophagography had proven or presumed Candida esophagitis. When this finding is detected on barium studies, further evaluation and treatment for Candida esophagitis therefore seem warranted.
The pathophysiologic basis of the foamy esophagus is uncertain. However, we postulate that the foam is produced directly by the fungal organisms that colonize the esophagus. It is well known that yeasts produce carbon dioxide via oxidative respiration; this is what causes bread to rise and champagne to bubble. In vitro cultures of candidiasis may be associated with extensive production of foam, necessitating routine addition of defoaming agents to the culture medium [10]. In one study from the microbiology literature, investigators found that when Candida organisms are cultured at an acidic pH (3.0-5.6) and body temperature, cell adhesion is altered so that a portion of the yeast grows as a foam that floats on the surface of the medium [11]. Although five patients in our series had gastroesophageal reflux caused by underlying esophageal involvement by scleroderma, it is unknown whether the acidic pH resulting from gastroesophageal reflux contributed in any way to the development of a foamy esophagus in these cases. Perhaps the most compelling evidence about the pathophysiology of this finding comes from two of our patients in whom a bubbly froth or foam adhered to the esophageal mucosa at endoscopy.
If production of foam is a feature of candidiasis, it is unclear why such a small percentage of all patients with Candida esophagitis have a foamy esophagus on esophagography. However, five (83%) of our six patients had esophageal involvement by scleroderma with markedly abnormal esophageal motility, impaired esophageal emptying, and associated peptic strictures in the distal esophagus. The foamy esophagus therefore may be more likely to occur in patients with chronic esophageal candidiasis from esophageal stasis associated with scleroderma or other causes of functional or mechanical obstruction of the esophagus [2].
Conversely, none of our patients had the shaggy esophagus of fulminant Candida esophagitis, which tends to occur in patients who are profoundly immunocompromised, typically from HIV infection [5]. Except for one patient who was known to be neutropenic, fungal colonization of the esophagus was instead related to esophageal stasis associated with scleroderma in patients who had an intact immune system. Thus, the radiographic findings in Candida esophagitis may depend on the underlying factors that predispose patients to the development of this condition.
In conclusion, the foamy esophagus is a new sign of Candida esophagitis on double-contrast esophagography that is usually associated with esophageal stasis due to scleroderma involving the esophagus. The foamy esophagus is characterized by innumerable tiny, rounded bubbles that settle out along the top of the barium column, producing a layer of foam. If the clinical history is suggestive of esophageal stasis or obstruction due to scleroderma or other causes, it is important to avoid using effervescent agent during the initial swallows of barium to differentiate foam from undissolved effervescent granules. This finding can also usually be distinguished radiographically from retained food or debris in the esophagus or diffuse nodularity of the mucosa. Candida esophagitis therefore should be strongly suspected when a foamy esophagus is detected on double-contrast esophagography, particularly in patients with underlying esophageal involvement by scleroderma.
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  M. S. Levine and S. E. Rubesin Diseases of the Esophagus: Diagnosis with Esophagography Radiology, November 1, 2005; 237(2): 414 - 427. [Abstract] [Full Text] [PDF]
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