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Gastrointestinal Basidiobolomycosis -- Arizona, 1994-1999

In March 1999, the Arizona Department of Health Services (ADHS) notified CDC about six cases of gastrointestinal basidiobolomycosis (GIB), an invasive fungal infection. Three cases were reported during January-March 1999, compared with three cases reported during the previous 5 years. This report describes two persons who had representative clinical presentations and summarizes the findings of the investigation of these cases, which indicate that this unusual fungal infection causes severe illness and may be misdiagnosed initially.

Case Reports

Case 1. In November 1998, a 37-year-old woman sought medical care at an emergency department for abdominal pain of 1 weeks' duration. She had no physical signs of abdominal disease, but her medical history was notable for 1 year of pica. She was treated empirically with an H2-antagonist agent and subsequently with omeprazole for presumed peptic ulcer disease (PUD), but she continued to have intermittent abdominal pain. In January 1999, a computerized tomography scan of her abdomen showed thickened gastric walls and enlarged intra-abdominal lymph nodes. She was hospitalized with a presumptive diagnosis of gastric cancer and underwent partial gastrectomy. Her preoperative white blood cell count (WBC) was 26.4x106 cells/mL (normal: 4-10x106 cells/mL), and absolute eosinophil count was 2.6x106 cells/mL (normal: 0.4-0.5x106 cells/mL). Pathologic examination revealed an inflammatory mass involving the stomach and extending to the pancreas. Microscopic examination of mass tissue showed a chronic inflammatory infiltrate with abundant eosinophils and broad, thin-walled, pleomorphic hyphae consistent with zygomycosis. On the basis of histologic examination, basidiobolomycosis was diagnosed and she received antifungal therapy with itraconazole. She is continuing her therapy and is recovering.

Case 2. In December 1998, a 59-year-old man sought medical care at an emergency department for abdominal pain and mucus in his stool for 3 weeks. He underwent colonoscopy and inflammatory bowel disease was diagnosed based on biopsies showing acute and chronic inflammation. He subsequently developed colonic obstruction; probable colon cancer was diagnosed using barium enema and he underwent rectosigmoid resection in February 1999. His WBC was 12.1x106 cells/mL, and absolute eosinophil count was 0.7x106 cells/mL. Pathologic examination of the colon mass showed a chronic inflammatory infiltrate with abundant eosinophils and occasional granulomas. Hyphae consistent with zygomycosis were observed in the tissues. Culture of surgical specimens grew Basidiobolus ranarum, and he was started on itraconazole. He is continuing his therapy and is recovering.

Epidemiologic Investigation

Because of the increased number of cases reported in 1999, ADHS and CDC conducted a case-control study to identify potential risk factors and to determine modes of acquisition. A case of GIB was defined as B. ranarum cultured from any surgical specimen from the GI tract, or if culture was not performed, pathologic examination revealing histology consistent with basidiobolomycosis. Investigators reviewed hospital records of all case-patients. To identify additional cases, a letter was sent to all pathologists in Arizona describing the typical pathologic findings of basidiobolomycosis and asking them to notify ADHS of any potential cases. Local dermatologists were asked about cases consistent with subcutaneous basidiobolomycosis. No additional cases were found. Four age-matched controls per case were selected--two clinic-based controls and two neighborhood controls. All case-patients and controls were interviewed using a standardized questionnaire about past medical history, daily activities, environmental exposures, and diet. Informed consent was obtained from all participants.

During April 1994-March 1999, six cases were identified. All case-patients underwent surgery with partial resection of the GI tract, and all received postsurgical treatment with itraconazole for a median of 7.5 months (range: 3-19 months); five had elevated eosinophil counts before surgery. Four case-patients had B. ranarum cultured from surgical specimens, and four had a positive serologic result using an immunodiffusion test at CDC (1). Four case-patients were men, and five were white; median age was 50 years (range: 37-59 years). The median length of time from onset of symptoms to diagnosis was 113 days (range: 15-243 days), and the median number of physicians consulted before diagnosis was six (range: three to eight). No patients died.

Because demographic, socioeconomic, or underlying illness data were similar for the two control groups, the control groups were combined for the analysis of the case-control study. Case-patients had lived in Arizona significantly longer than controls (odds ratio [OR]=1.1 per additional year of residence, p=0.03). Smoking more years (OR=1.2 per additional year of smoking, p=0.10) and using H2-antagonists (OR=9.5, p=0.06) before onset of symptoms were of borderline significance. Case-patients were more likely than controls to have amphibians or reptiles outside their homes (five [83%] versus 16 [67%]), camped near a lake or river during the previous year (three [50%] versus eight [33%]), had previous steroid use (two [33%] versus two [8%]), and owned a dog (four [67%] versus eight [33%]); fewer case-patients washed vegetables before eating them (four [67%] versus 21 [88%]). However, these differences were not statistically significant.

Reported by: T Pasha, J Leighton, J Smilack, MD, Mayo Clinic, Scottsdale; K Komatsu, C Kioski, Arizona Dept of Health Svcs. Infectious Disease Pathology Activity, Div of Viral and Rickettsial Diseases, and Mycotic Diseases Br, Div of Bacterial and Mycotic Diseases, National Center for Infectious Diseases; and an EIS Officer, CDC.

Editorial Note:

B. ranarum rarely causes human disease in the United States. Basidiobolomycosis is a form of zygomycosis caused by the fungus B. ranarum (from the order Entomophthorales), which has been isolated throughout the world from decaying vegetation and soil and from the GI tracts of reptiles, amphibians, fish, and insectivorous bats (1). Basidiobolomycosis is most common in the tropical regions of eastern and western Africa, but cases also have occurred in southeast Asia and South America. The disease most commonly affects males aged less than 20 years and usually manifests as painless, subcutaneous nodules on the lower extremities and buttocks (1). Infection is secondary to traumatic inoculation. GIB is rare, with only six cases previously reported (three cases from Brazil, one from Kuwait, and two from the United States, including one case from the Arizona cluster described in this report) (2-6).

A definitive diagnosis of basidiobolomycosis requires culture of B. ranarum from clinical or surgical specimens, but a probable diagnosis can be made based on histopathologic appearance. The microscopic appearance of B. ranarum in tissues is characterized by scarce, broad, thin-walled, pleomorphic hyphae surrounded by a collar of eosinophilic material (known as the Splendore-Hoeppli phenomenon) (7). The host inflammatory reaction is composed mostly of mononuclear cells with abundant eosinophils and occasional granulomas (7). Typically, the muscular layer of the GI tract is thickened greatly and eosinophilic inflammation is present extending through the serosa into the perigastric or mesenteric fat; the GI mucosa is typically spared (2,3,5,6). The histopathologic appearance of GIB may be confused with Conidiobolus coronatus, another Entomophthorales, or mucormycosis (7). GIB has a nonspecific clinical presentation and may be diagnosed initially as cancer, PUD, gastroenteritis, diverticulitis, or inflammatory bowel disease (1). A specific serologic immunodiffusion test is available through CDC, but its sensitivity is unknown, and antibodies against B. ranarum appear to wane following effective treatment (6,8). The patients described in this report had peripheral eosinophilia, but this laboratory finding has not been reported previously as a feature of basidiobolomycosis.

Successful response to therapy has been reported with ketoconazole, itraconazole, and potassium iodide; however, response to amphotericin B is poor (2-6,9). In the six cases described in this report, the three case-patients in whom GIB was diagnosed before 1999 apparently have been cured following surgery and treatment with itraconazole. The other three patients remained clinically well while taking itraconazole postoperatively. Because all of the Arizona patients underwent surgical excision of the affected parts of their GI tracts, it is difficult to evaluate whether itraconazole therapy alone could have resulted in adequate clinical response.

Ecologic studies in the United States have identified B. ranarum in reptiles and amphibians (10). GIB presumably is acquired through ingestion. However, except for the patient with a history of pica, it is unclear how the other patients acquired the infection. Possible exposures include unintentional ingestion of contaminated soil, especially near rivers or lakes, or eating fruits or vegetables contaminated with soil or feces from reptiles or amphibians. The findings in this report indicate that decreased acidity and other host factors (e.g., underlying disease and use of medication) may increase the risk for acquiring GIB.

The findings in this report are subject to at least two limitations. First, despite active case finding, a small number of cases were available for analysis. Second, because of the extended time between exposure and initial interviews of patients, the findings are subject to recall bias. To minimize this problem, the questionnaire focused on daily activities and usual food preparation methods.

Increased awareness by clinicians and public health surveillance may help identify additional cases, determine the burden of disease, and lead to a better understanding of risk factors for GIB and possible prevention measures. Physicians caring for patients with suspected basidiobolomycosis should contact their state health departments or CDC's Mycotic Diseases Branch, Division of Bacterial and Mycotic Diseases, National Center for Infectious Diseases, telephone (404) 639-2499.


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