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Fungal infection associated with gastroduodenal ulceration: Endoscopic and pathologic appearances
GASTROENTEROLOGY 78:350-354, 1980
Fungal Infection Associated with Gastroduodenal Ulceration: Endoscopic and Pathologic Appearances MARION
PETERS,
JOHN
WEINER,
and
GREGORY
WHELAN
St. Vincent’s Hospital, Melbourne, Australia
Three patients with peptic ulcers diagnosed at upper gastrointestinal endoscopy are reported. All were seriously ill (2 debilitated alcoholics) and died soon afterwards. Fungi were recognized in the antemortem specimen of one of the two ulcers biopsied at the time of endoscopy and in the postmortem specimens of all. In two, demise appears to have been precipitated by erosion of the wall of a major artery by fungal invasion. Culture of the ulcer based as well as throat swabs and stool examination for mycelial and yeast forms of fungus in susceptible patients may allow a more accurate diagnosis to be made and therapy to be instituted.
While oral and even esophageal moniliasis is common in gravely ill patients,‘-” the recognition of fungal ulceration of the stomach and duodenum is far less frequent and rarely diagnosed antemortem. The finding of a gastric ulcer with unusual endoscopic features from which fungi were recognized by histologic examination of an antemortem biopsy sample prompted this report. In 2 patients with peptic ulcers fungi were directly implicated in their death.
Case Report Case 1 A 47-yr-old woman under treatment for chronic alcoholism was referred with a 6-mo history of weakness, weight loss, diarrhea, recent fecal incontinence, and ankle swelling. On examination she looked ill, was febrile at 38°C with a tachycardia of 144 beats per minute and a systolic blood pressure of 77 mmHg. She had glossitis and angular stomatitis. White plaques noted on her palate and
Received March 13, 1978. Accepted August 29, 1979. Address requests for reprints to: Dr. G. Whelan, University of Melbourne, Department of Medicine, St. Vincent’s Hospital, Fitzroy 3065, Victoria, Australia.
0 1980 by the American Gastroenterological Association 0016~5085/80/020350-05$02.25
pharynx were typical of candidiasis. Her abdomen was distended with ascitic fluid; an enlarged firm liver (6 cm below the right costal margin) was palpable; there were pressure sores over her sacral area and pitting edema to mid-calf on both legs. Investigations revealed a plasma sodium of 119 ymol/liter; potassium 4.3 pmol/liter; urea 1.1 pmol/liter; albumin 14 g/liter; bilirubin 27 pmol/liter; serum aspartate transaminase 231 III/liter; serum alkaline phosphatase 556 III/liter; and thrombotest 18%. Packed cell volume was 24%. A provisional diagnosis of alcoholic liver disease, septicemia, and oral moniliasis was made. An intravenous line was established, and glucose was given. Concentrated albumin, gentamicin, cephalothin, and nystatin were also administered. She remained hypotensive and peripherally vasoconstricted despite volume expansion. She subsequently had two large melenas of about 1000 ml. Upper gastrointestinal endoscopy revealed diffuse superficial erosions of esophagus, stomach, and duodenum. In addition there was a gastric ulcer on the anterior wall of the stomach approximately 50 cm from the incisor teeth measuring z cm in diameter which felt hard and woody when grasped with the biopsy forceps. Its edges were smooth and sharply demarcated from the surrounding mucosa. Despite vigorous attempts at resuscitation, she died 36 hr after admission. The endoscopic biopsy specimen of this gastric ulcer showed an acute on chronic inflammatory reaction, infiltrated with budding yeasts and septate fungal hyphae (Figure 1). This was confirmed in the sections taken at autopsy with fungal infiltration extending into the submucosa (Figure 2). In addition there were several shallow ulcers in the fundus of the stomach and acute alcoholic hepatitis with portal fibrosis. Blood cultures, taken before the institution of antibiotic therapy, failed to grow an organism. Case 2 A 51-yr-old professed alcoholic presented to the Casualty Department with a l-wk history of epigastric pain followed by hematemesis and melena for the z days before admission. On examination he was dirty, unkempt, and pale with an unrecordable blood pressure and a tachycardia of 120 beats per minute. Abdominal examination
February
1980
FUNGAL
INFECTION
ASSOCIATED
WITH
Figure
showed epigastric tenderness, and melena was noted on rectal examination. Resuscitation was commenced with intravenous plasma and whole blood. Six hours after admission an upper gastrointestinal endoscopy was performed. This revealed extensive ulceration of the duodenal cap with some fresh ad-
Figure 2. Autopsy
specimen
GASTRODUODENAL
ULCERATION
351
1. Endoscopic biopsy specimen of a gastric ulcer showing budding yeasts and hyphae (Silver Methenaminc, x 128).
herent blood clot. There was a small amount of dark blood in his stomach, and his esophagus was normal. After endoscopy he had two further massive hematemeses. On the second of these he aspirated blood into his lungs. He was unable to be resuscitated from the resulting cardiac arrest.
of gastric ulcer with fungi (arrows) in ulcer base (Silver Methenamine,
x 32).
352
PETERS
ET AL.
GASTROENTEROLOGY
At autopsy, a large chronic duodenal ulcer 3 cm in diameter was noted with massive amounts of blood in the gastrointestinal tract. The gastroduodenal artery, situated in the base of the ulcer, was eroded. Histology revealed a chronic ulcer penetrating pancreatic tissue. The internal elastic lamina of the artery was disrupted (Figure 3), and special stains showed the presence of broad branching septate hyphae infiltrating the wall (Figure 4). At one edge, a moderate mononuclear cell infiltrate was associated with the fungus. Liver histology confirmed the presence of alcoholic liver disease, severe fatty change, some periportal fibrosis, and occasional foci of single liver cell necrosis.
Case 3 An 82-yr-old woman had been tired for several weeks and presented to Casualty having vomited a large volume of blood. She had two further hematemeses but no abdominal pain. On admission she was pale and sweaty with a blood pressure of 110 systolic and pulse rate of 96 beats per minute. She was transfused with 2 units of blood. Upper gastrointestinal endoscopy was performed next morning and revealed old blood in the esophagus, stomach, and duodenum. On the lesser curve of the stomach at 40-45 cm from the incisor teeth there were two ulcers, one of which had debris in its base and elevated edges. Biopsies were taken from this ulcer because of the suspi-
Figure 3. Autopsy specimen of gastroduodenal X 32).
Vol. 78.
No. 2
cion of malignancy. Biopsies showed ulcerated gastric mucosa with a marked acute inflammatory cell infiltrate. There was no evidence of malignancy and a Grocott-Gamori methenamine silver stain and PAS stain failed to reveal fungi. The patient was transfused with blood and commenced on cimetidine 1 g orally per day. Two days after admission she had a sudden massive hematemesis and died. At autopsy a large amount of fresh blood was present in the stomach and bowel. Straddling the midportion of the lesser curve of the stomach was an irregular ulcer measuring 6X4 cm. The splenic artery protruded from the base of the ulcer and its wall was eroded (Figure 5A). There was some superficial gastric ulceration adjacent to the main ulcer. Histology revealed extensive benign chronic ulceration. Fungal infiltration, consisting of branching septate hyphae (Figure 5B), was found in the perforated edges of the splenic artery. The artery’s internal elastic lamina was disrupted with fungal extension into the media. There were a few scattered lymphocytes in the vessel wall.
Discussion Mycotic infection of the gastrointestinal tract is relatively uncommon. It is seen in l-4% of routine autopsies4 and 20% of autopsies of patients with leukemia or lymphoma.‘,5 In a recent review of 109 cases of gastrointestinal fungal infection Eras et al.
artery with fungal infiltration (arrows) of the ruptured edge (Aldehyde Fuchsin-Gamori,
February
1980
Figure 4. High-power
FUNGAL
view
of Figure
INFECTION
3 showing
ASSOCIATED
broad
found that all but 2 patients had malignancy.’ Although one-quarter of the patients had gastric involvement, the pathologic findings at autopsy of gastric invasion by fungi did not conform to a uniform pattern. Two cases of fungal infections have previously been noted in alcoholics.” These patients had disseminated candidiasis. However, there appears to be no previous reports of gastric or duodenal invasive fungal infections in alcoholics. Chronic alcoholics are often malnourished and debilitated. They have a depressed immune response and altered granulocyte function,fi both of which may well promote fungal invasion of their tissues. Erosion of a large blood vessel, the wall of which contained fungi, was the cause of death in 2 of our patients. This erosion has been described to be associated with candida ulceration of the esophagus in patients with malignancy.‘,’ There are also reports of aspergillus” and histoplasma” in the base of a peptic ulcer and erosion of an artery that caused fatal hematemesis. The diagnosis of fungal infection in such patients is often difficult and is uncommon premortem. Bodey recommends pharyngeal swab and stool culture to isolate an organism.’ However, the finding of monilia in mouth washings, saliva, and feces is combe mon in normal people’” and thus alone cannot used to establish fungal infection of the gastrointestinal tract. Nevertheless, mucosal invasion by fungi
scptate
WITH
branching
GASTRODUODENAL
hyphae
(Silver
LJLCIiRATION
Methenamine,
353
x 512).
(as occurred in our 3 cases) is a pathological condition and is often associated with the appearance of mycelia in the stools.11 We believe mycelia should be searched for in endoscopic biopsy samples and endoscopic scraping. At necropsy of such patients, the finding of fungi might be improved by culture of swabs from the ulcer bed and histologic staining for fungi with particular attention to the perforated ends of any obvious vessels. It should be noted that to invade blood vessels candida must exhibit dimorphism, i.e., both yeasts and mycelial forms must be present together. Endoscopic diagnosis of gastrointestinal fungal infections is more difficult. Candida esophagitis can be diagnosed by the presence of (a) white plaques observed endoscopically, (b) yeasts seen on direct smear from plaques, and (c) a serum agglutinin titer of at least 1: 160.” Fungal infection of the stomach recognized endoscopically must be however far less common. The authors were unable to find endoscopic descriptions of such lesions in the literature. Since cultures of the ulcers of our patients were not performed, it is not possible to state the type of fungus involved in each case. However Candida albicans was almost certainly the cause in the first case as the patient had extensive oral and pharyngeal moniliasis. The histologic appearances cannot differentiate the cause in the other 2 cases. For monilial esophagitis, it is recommended that Nystatin be given for 4 ~ks.~,” However, this is unlikely to be ef-
354
PETERS
ET AL.
GASTROENTEROLOGY
specimen of splenic Fig:“I .e 5. A. Autopsy view of (A)(Silver Methenamine
artery with X 128).
fungal
infiltation
fective in deep-seated infection involving the stomach and duodenum. In such cases the use of an agent such as amphotericin B would be more rational. Perhaps the lesion from these cases is that fungal infection should be sought in patients who have unusual peptic ulcers when examined by upper gastrointestinal endoscopy, as in the first case. This could have been a primary fungal lesion with secondary ulceration. Lewis’s original description of gastric candidiasis’” may well have been of a primary fungal ulcer since chronic peptic ulceration should not occur in a patient with achlorhydria due to pernicious anemia, and there was no mention of malignant change. Continued bleeding obscured the ulcer in the second patient, and thus the endoscopic features were unable to be described accurately. The latter 2 cases, however, appear to illustrate a different problem, in that they had classic peptic ulcers complicated by fungal invasion. In addition we should consider that malnourished alcoholics as well as patients with leukemia, lymphoma, or tumor are at risk from complicating fungal disease and seek evidence for it by the methods recommended above.
(yarrows) of its wall (Silver Methenamine,
2. Eras
3. 4. 5.
6.
7.
8.
9.
10.
11. 12.
References 1. Bodey Chron
CP: Fungal infections Dis 19:667-687, 1966
complicating
acute
leukemia.
J
13.
Vol. 78, No. 2
x 32). B. High-power
P, Goldstein MJ, Sherlock P: Candida infection of the gastrointestinal tract. Medicine (Baltimore) 51:367-379, 1972 Louria DB, Stiff DP, Bennett B: Disseminated moniliasis in the adult. Medicine (Baltimore) 41:307-337, 1962 Smith JMB: Mycoses of the alimentary tract. Progress Report. Gut 10:1035-1040, 1969 Pedraza MA: Mycotic infections at autopsy. A comparative study in two University Hospitals. Am J Clin Path01 51:470476, 1969 Brayton RG, Stokes PE, Schwartz MS: Effect of alcohol and various diseases on leukocyte mobilisation phagocytosis and intracellular bacterial killing. N Engl J Med 282:123-128,197O Lefkowitz M, Elsas JL, Levine RJ: Candida infections complicating peptic esophageal ulcer. Arch Intern Med 113:672-675, 1964 Welsh RA, McClinton LT: Aspergillosis of lungs and duodenum with fatal intestinal hemorrhage. Arch Path01 57:379382, 1954 Fitzpatrick TJ, Neiman BH: Histoplasma capsulatum infection associated with gastric ulcer and fatal hemorrhage. Arch Intern Med 91:49-55, 1953 Gorbach SL, Nahas L. Lerner PI, et al: Studies of intestinal microflora. I. Effect of diet, age and periodic sampling on numbers of fecal micro-organisms in man. Gastroenterology 53845-855, 1967 Kozinn PJ, Taschdjian CL: Enteric candidiasis. Paediatrics 30:71-85, 1962 Kodsi BE, Wickremesinghe PC, Kozinn PJ, et al: Candida esophagitis. A prospective study of 27 cases. Gastroenterology 71:715-719, 1976 Lewis SJ: Moniliasis of the lung and stomach. Case Report with autopsy. Am J Clin Path01 3:367-374, 1933.
Fungal Infection Associated with Gastroduodenal Ulceration: Endoscopic and Pathologic Appearances MARION
PETERS,
JOHN
WEINER,
and
GREGORY
WHELAN
St. Vincent’s Hospital, Melbourne, Australia
Three patients with peptic ulcers diagnosed at upper gastrointestinal endoscopy are reported. All were seriously ill (2 debilitated alcoholics) and died soon afterwards. Fungi were recognized in the antemortem specimen of one of the two ulcers biopsied at the time of endoscopy and in the postmortem specimens of all. In two, demise appears to have been precipitated by erosion of the wall of a major artery by fungal invasion. Culture of the ulcer based as well as throat swabs and stool examination for mycelial and yeast forms of fungus in susceptible patients may allow a more accurate diagnosis to be made and therapy to be instituted.
While oral and even esophageal moniliasis is common in gravely ill patients,‘-” the recognition of fungal ulceration of the stomach and duodenum is far less frequent and rarely diagnosed antemortem. The finding of a gastric ulcer with unusual endoscopic features from which fungi were recognized by histologic examination of an antemortem biopsy sample prompted this report. In 2 patients with peptic ulcers fungi were directly implicated in their death.
Case Report Case 1 A 47-yr-old woman under treatment for chronic alcoholism was referred with a 6-mo history of weakness, weight loss, diarrhea, recent fecal incontinence, and ankle swelling. On examination she looked ill, was febrile at 38°C with a tachycardia of 144 beats per minute and a systolic blood pressure of 77 mmHg. She had glossitis and angular stomatitis. White plaques noted on her palate and
Received March 13, 1978. Accepted August 29, 1979. Address requests for reprints to: Dr. G. Whelan, University of Melbourne, Department of Medicine, St. Vincent’s Hospital, Fitzroy 3065, Victoria, Australia.
0 1980 by the American Gastroenterological Association 0016~5085/80/020350-05$02.25
pharynx were typical of candidiasis. Her abdomen was distended with ascitic fluid; an enlarged firm liver (6 cm below the right costal margin) was palpable; there were pressure sores over her sacral area and pitting edema to mid-calf on both legs. Investigations revealed a plasma sodium of 119 ymol/liter; potassium 4.3 pmol/liter; urea 1.1 pmol/liter; albumin 14 g/liter; bilirubin 27 pmol/liter; serum aspartate transaminase 231 III/liter; serum alkaline phosphatase 556 III/liter; and thrombotest 18%. Packed cell volume was 24%. A provisional diagnosis of alcoholic liver disease, septicemia, and oral moniliasis was made. An intravenous line was established, and glucose was given. Concentrated albumin, gentamicin, cephalothin, and nystatin were also administered. She remained hypotensive and peripherally vasoconstricted despite volume expansion. She subsequently had two large melenas of about 1000 ml. Upper gastrointestinal endoscopy revealed diffuse superficial erosions of esophagus, stomach, and duodenum. In addition there was a gastric ulcer on the anterior wall of the stomach approximately 50 cm from the incisor teeth measuring z cm in diameter which felt hard and woody when grasped with the biopsy forceps. Its edges were smooth and sharply demarcated from the surrounding mucosa. Despite vigorous attempts at resuscitation, she died 36 hr after admission. The endoscopic biopsy specimen of this gastric ulcer showed an acute on chronic inflammatory reaction, infiltrated with budding yeasts and septate fungal hyphae (Figure 1). This was confirmed in the sections taken at autopsy with fungal infiltration extending into the submucosa (Figure 2). In addition there were several shallow ulcers in the fundus of the stomach and acute alcoholic hepatitis with portal fibrosis. Blood cultures, taken before the institution of antibiotic therapy, failed to grow an organism. Case 2 A 51-yr-old professed alcoholic presented to the Casualty Department with a l-wk history of epigastric pain followed by hematemesis and melena for the z days before admission. On examination he was dirty, unkempt, and pale with an unrecordable blood pressure and a tachycardia of 120 beats per minute. Abdominal examination
February
1980
FUNGAL
INFECTION
ASSOCIATED
WITH
Figure
showed epigastric tenderness, and melena was noted on rectal examination. Resuscitation was commenced with intravenous plasma and whole blood. Six hours after admission an upper gastrointestinal endoscopy was performed. This revealed extensive ulceration of the duodenal cap with some fresh ad-
Figure 2. Autopsy
specimen
GASTRODUODENAL
ULCERATION
351
1. Endoscopic biopsy specimen of a gastric ulcer showing budding yeasts and hyphae (Silver Methenaminc, x 128).
herent blood clot. There was a small amount of dark blood in his stomach, and his esophagus was normal. After endoscopy he had two further massive hematemeses. On the second of these he aspirated blood into his lungs. He was unable to be resuscitated from the resulting cardiac arrest.
of gastric ulcer with fungi (arrows) in ulcer base (Silver Methenamine,
x 32).
352
PETERS
ET AL.
GASTROENTEROLOGY
At autopsy, a large chronic duodenal ulcer 3 cm in diameter was noted with massive amounts of blood in the gastrointestinal tract. The gastroduodenal artery, situated in the base of the ulcer, was eroded. Histology revealed a chronic ulcer penetrating pancreatic tissue. The internal elastic lamina of the artery was disrupted (Figure 3), and special stains showed the presence of broad branching septate hyphae infiltrating the wall (Figure 4). At one edge, a moderate mononuclear cell infiltrate was associated with the fungus. Liver histology confirmed the presence of alcoholic liver disease, severe fatty change, some periportal fibrosis, and occasional foci of single liver cell necrosis.
Case 3 An 82-yr-old woman had been tired for several weeks and presented to Casualty having vomited a large volume of blood. She had two further hematemeses but no abdominal pain. On admission she was pale and sweaty with a blood pressure of 110 systolic and pulse rate of 96 beats per minute. She was transfused with 2 units of blood. Upper gastrointestinal endoscopy was performed next morning and revealed old blood in the esophagus, stomach, and duodenum. On the lesser curve of the stomach at 40-45 cm from the incisor teeth there were two ulcers, one of which had debris in its base and elevated edges. Biopsies were taken from this ulcer because of the suspi-
Figure 3. Autopsy specimen of gastroduodenal X 32).
Vol. 78.
No. 2
cion of malignancy. Biopsies showed ulcerated gastric mucosa with a marked acute inflammatory cell infiltrate. There was no evidence of malignancy and a Grocott-Gamori methenamine silver stain and PAS stain failed to reveal fungi. The patient was transfused with blood and commenced on cimetidine 1 g orally per day. Two days after admission she had a sudden massive hematemesis and died. At autopsy a large amount of fresh blood was present in the stomach and bowel. Straddling the midportion of the lesser curve of the stomach was an irregular ulcer measuring 6X4 cm. The splenic artery protruded from the base of the ulcer and its wall was eroded (Figure 5A). There was some superficial gastric ulceration adjacent to the main ulcer. Histology revealed extensive benign chronic ulceration. Fungal infiltration, consisting of branching septate hyphae (Figure 5B), was found in the perforated edges of the splenic artery. The artery’s internal elastic lamina was disrupted with fungal extension into the media. There were a few scattered lymphocytes in the vessel wall.
Discussion Mycotic infection of the gastrointestinal tract is relatively uncommon. It is seen in l-4% of routine autopsies4 and 20% of autopsies of patients with leukemia or lymphoma.‘,5 In a recent review of 109 cases of gastrointestinal fungal infection Eras et al.
artery with fungal infiltration (arrows) of the ruptured edge (Aldehyde Fuchsin-Gamori,
February
1980
Figure 4. High-power
FUNGAL
view
of Figure
INFECTION
3 showing
ASSOCIATED
broad
found that all but 2 patients had malignancy.’ Although one-quarter of the patients had gastric involvement, the pathologic findings at autopsy of gastric invasion by fungi did not conform to a uniform pattern. Two cases of fungal infections have previously been noted in alcoholics.” These patients had disseminated candidiasis. However, there appears to be no previous reports of gastric or duodenal invasive fungal infections in alcoholics. Chronic alcoholics are often malnourished and debilitated. They have a depressed immune response and altered granulocyte function,fi both of which may well promote fungal invasion of their tissues. Erosion of a large blood vessel, the wall of which contained fungi, was the cause of death in 2 of our patients. This erosion has been described to be associated with candida ulceration of the esophagus in patients with malignancy.‘,’ There are also reports of aspergillus” and histoplasma” in the base of a peptic ulcer and erosion of an artery that caused fatal hematemesis. The diagnosis of fungal infection in such patients is often difficult and is uncommon premortem. Bodey recommends pharyngeal swab and stool culture to isolate an organism.’ However, the finding of monilia in mouth washings, saliva, and feces is combe mon in normal people’” and thus alone cannot used to establish fungal infection of the gastrointestinal tract. Nevertheless, mucosal invasion by fungi
scptate
WITH
branching
GASTRODUODENAL
hyphae
(Silver
LJLCIiRATION
Methenamine,
353
x 512).
(as occurred in our 3 cases) is a pathological condition and is often associated with the appearance of mycelia in the stools.11 We believe mycelia should be searched for in endoscopic biopsy samples and endoscopic scraping. At necropsy of such patients, the finding of fungi might be improved by culture of swabs from the ulcer bed and histologic staining for fungi with particular attention to the perforated ends of any obvious vessels. It should be noted that to invade blood vessels candida must exhibit dimorphism, i.e., both yeasts and mycelial forms must be present together. Endoscopic diagnosis of gastrointestinal fungal infections is more difficult. Candida esophagitis can be diagnosed by the presence of (a) white plaques observed endoscopically, (b) yeasts seen on direct smear from plaques, and (c) a serum agglutinin titer of at least 1: 160.” Fungal infection of the stomach recognized endoscopically must be however far less common. The authors were unable to find endoscopic descriptions of such lesions in the literature. Since cultures of the ulcers of our patients were not performed, it is not possible to state the type of fungus involved in each case. However Candida albicans was almost certainly the cause in the first case as the patient had extensive oral and pharyngeal moniliasis. The histologic appearances cannot differentiate the cause in the other 2 cases. For monilial esophagitis, it is recommended that Nystatin be given for 4 ~ks.~,” However, this is unlikely to be ef-
354
PETERS
ET AL.
GASTROENTEROLOGY
specimen of splenic Fig:“I .e 5. A. Autopsy view of (A)(Silver Methenamine
artery with X 128).
fungal
infiltation
fective in deep-seated infection involving the stomach and duodenum. In such cases the use of an agent such as amphotericin B would be more rational. Perhaps the lesion from these cases is that fungal infection should be sought in patients who have unusual peptic ulcers when examined by upper gastrointestinal endoscopy, as in the first case. This could have been a primary fungal lesion with secondary ulceration. Lewis’s original description of gastric candidiasis’” may well have been of a primary fungal ulcer since chronic peptic ulceration should not occur in a patient with achlorhydria due to pernicious anemia, and there was no mention of malignant change. Continued bleeding obscured the ulcer in the second patient, and thus the endoscopic features were unable to be described accurately. The latter 2 cases, however, appear to illustrate a different problem, in that they had classic peptic ulcers complicated by fungal invasion. In addition we should consider that malnourished alcoholics as well as patients with leukemia, lymphoma, or tumor are at risk from complicating fungal disease and seek evidence for it by the methods recommended above.
(yarrows) of its wall (Silver Methenamine,
2. Eras
3. 4. 5.
6.
7.
8.
9.
10.
11. 12.
References 1. Bodey Chron
CP: Fungal infections Dis 19:667-687, 1966
complicating
acute
leukemia.
J
13.
Vol. 78, No. 2
x 32). B. High-power
P, Goldstein MJ, Sherlock P: Candida infection of the gastrointestinal tract. Medicine (Baltimore) 51:367-379, 1972 Louria DB, Stiff DP, Bennett B: Disseminated moniliasis in the adult. Medicine (Baltimore) 41:307-337, 1962 Smith JMB: Mycoses of the alimentary tract. Progress Report. Gut 10:1035-1040, 1969 Pedraza MA: Mycotic infections at autopsy. A comparative study in two University Hospitals. Am J Clin Path01 51:470476, 1969 Brayton RG, Stokes PE, Schwartz MS: Effect of alcohol and various diseases on leukocyte mobilisation phagocytosis and intracellular bacterial killing. N Engl J Med 282:123-128,197O Lefkowitz M, Elsas JL, Levine RJ: Candida infections complicating peptic esophageal ulcer. Arch Intern Med 113:672-675, 1964 Welsh RA, McClinton LT: Aspergillosis of lungs and duodenum with fatal intestinal hemorrhage. Arch Path01 57:379382, 1954 Fitzpatrick TJ, Neiman BH: Histoplasma capsulatum infection associated with gastric ulcer and fatal hemorrhage. Arch Intern Med 91:49-55, 1953 Gorbach SL, Nahas L. Lerner PI, et al: Studies of intestinal microflora. I. Effect of diet, age and periodic sampling on numbers of fecal micro-organisms in man. Gastroenterology 53845-855, 1967 Kozinn PJ, Taschdjian CL: Enteric candidiasis. Paediatrics 30:71-85, 1962 Kodsi BE, Wickremesinghe PC, Kozinn PJ, et al: Candida esophagitis. A prospective study of 27 cases. Gastroenterology 71:715-719, 1976 Lewis SJ: Moniliasis of the lung and stomach. Case Report with autopsy. Am J Clin Path01 3:367-374, 1933.