Hepatic basidiobolomycosis masquerading as cholangiocarcinoma: a case report and literature review

Article information

J Liver Cancer. 2023;23(2):389-396

Publication date (electronic) : 2023 August 17

doi : https://doi.org/10.17998/jlc.2023.06.07

Roopali Sehrawat¹, Nalini Bansal^,1, Ajitabh Srivastava², Dharmender Malik³, Vivek Vij⁴

¹Department of Pathology, SGT University, Budhera, Gurugram, India

²Department of Liver Transplant Surgery, Aakash Healthcare Super Speciality Hospital, Dwarka, New Delhi, India

³Department of Nuclear Medicine & PET-CT, Fortis Memorial Research Institute (FMRI), Gurugram, India

⁴Department of Liver Transplant Surgery, Fortis Healthcare, Budhera, Gurugram, India

Corresponding author: Nalini Bansal, Department of Pathology, SGT University, Gurgaon-Badli Road Chandu, Budhera, Gurugram 122505, India Tel. +91-999-037-0677 E-mail: drnalinibansal@gmail.com

Received 2023 January 12; Revised 2023 February 13; Accepted 2023 June 7.

Abstract

INTRODUCTION

Basidiobolomycosis is a rare infection caused by the fungus Basidiobolus ranarum (B. ranarum) belongs to the class Zygomycetes and the family Entomophthoraceae. It is commonly found in warm rural regions of Sub-Saharan Africa, South America, and Asia (Saudi Arabia, Kuwait, Iran, India, Indonesia, and Burma). Basidiobolomycosis mainly affects immunocompetent humans of all age groups, and the infection is usually aggressive and sometimes fatal. The infection often presents with non-specific clinical and radiological features; therefore, it should be considered in the differential diagnosis in endemic regions.1 We report a rare case of basidiobolomycosis in a 16-year-old male with liver and gastrointestinal involvement.

CASE REPORT

A 16-year-old male from Iran presented with multiple episodes of vomiting and low oral intake. The patient had a history of seizures and type II diabetes mellitus. On examination, the patient was afebrile; blood pressure was 120/70 mmHg, heart rate was 130/min, respiratory rate was 20/min, oxygen saturation was 98% at room air, and chest was clear bilaterally.

Abdominal ultrasonography revealed a borderline enlarged liver with a hypoechoic lesion measuring 6.7×6.1 cm in the portal confluence region involving segments 5, 6, and 7. Color Doppler imaging revealed mild color flow within the lesion. Magnetic resonance imaging (MRI) also revealed an enlarged liver (17 cm in size). A lesion with heterogeneous signal intensity showing areas of diffuse restriction measuring 8×7×6.7 cm was seen involving the right lobe of the liver. There was a mass effect on the central intrahepatic biliary tree with consequent non-visualization of the right and left main hepatic ducts, their confluence, and the proximal common hepatic duct. The proximal parts of the intrahepatic biliary radicles were observed within the lesion. Diffusionweighted imaging and the corresponding apparent diffusion coefficient (ADC) images showed areas of diffusion restriction with low ADC values in and around the lesion involving the right hepatic lobe. In pre- and post-contrast mDIXON (T1W) studies, heterogeneous enhancement with a few central non-enhancing areas was observed within the lesion. These findings were suggestive of hilar cholangiocarcinoma, and surgical resection was considered. Coronal post-contrast mDIXON images showed thickening and enhancement of the cecum and ascending colon and heterogeneously enhancing lesions in the liver (Fig. 1). A positron emission tomography-computed tomography (CT) scan showed an enlarged liver measuring 18 cm in the maximum craniocaudal extent. A large, fluorodeoxyglucose (FDG)-avid hypodense lesion was seen in the right lobe of the liver (segments 5-8), measuring approximately 7.0×8.0×6.4 cm. Ulceration with irregular thickening was observed in the cecum, distal ileum and ascending colon, with a maximum mural thickness of 1.5 cm. A few enlarged FDG-avid paracecal lymph nodes were also noted, the largest measuring 1.9 cm along the short axis (Fig. 2).

Figure 1.

(A) An ultrasonography image shows a large hypoechoic lesion measuring 6.7×6.1 cm in the region of portal confluence involving segments 5, 6, and 7 of the liver (red arrow). (B) Color doppler reveals mild color flow within the lesion. (C) Transverse relaxation time fatsaturation magnetic resonance imaging of the liver demonstrates heterogeneously hyperintense signal intensity lesion (red arrow). (D) Magnetic resonance cholangiopancreatography sequence shows the mass effect with markedly dilated intrahepatic biliary radicles. (E, F) Diffusion-weighted imaging and corresponding ADC images show areas of diffusion restriction with low ADC in and around the lesion involving the right lobe of the liver (red arrows). On (G) pre- and (H) post-contrast mDIXON (T1W) studies, heterogeneous enhancement with few central non-enhancing areas was seen within the lesion (red arrows). These findings were suggestive of hilar cholangiocarcinoma. (I) Coronal post-contrast mDIXON images show thickening with an enhancement of the cecum, ascending colon, and heterogeneously enhancing lesion in the liver. ADC, apparent diffusion coefficient.

Figure 2.

(A-C) Whole-body FDG positron emission tomography-computed tomography scan demonstrates FDG avid mass like ulcerated irregular thickening involving the cecum, distal ileum, and proximal ascending colon (red and black arrows) along with FDG avid paracecal lymph nodes. (D, E) A large, FDG-avid hypodense lesion showing heterogeneous post-contrast enhancement in the right lobe of the liver involving segments 5, 6, and 7 (red and black arrows) measuring approximately 7.0×8.0×6.4 cm in size. FDG, fluorodeoxyglucose.

Percutaneous transhepatic biliary drainage and liver biopsy were performed, and the biopsy specimen was sent for histopathological examination and fungal culture. The biopsy specimen was mostly composed of fibrocollagenous tissue with inflammatory infiltrates and granulomatous reactions. Fungal spores were observed within some giant cells (Fig. 3).

Figure 3.

Liver biopsy shows mainly fibrocollagenous tissue with inflammatory infiltrate and granulomatous reaction. Fungal spores are noted within giant cells. (A) H&E (×4), (B) H&E (×10), and (C) H&E (×20). H&E, hematoxylin and eosin.

Colonoscopy revealed a deformed and edematous ascending colon and cecum, with ulcers measuring up to 1 cm in diameter (Fig. 4). Multiple biopsies were obtained from the ulcerated lesions. Histopathological examination revealed an ulcerated surface covered with an acute inflammatory exudate containing eosinophils. A Splendore-Hoeppli phenomenon was observed around the fungal spores. Periodic acidSchiff (PAS) and Grocott methenamine silver (GMS) stains highlighted the presence of fungal spores (Fig. 5).

Figure 4.

(A, B) Colonoscopy shows deformed, edematous ascending colon and cecum along with deep ulcers in the colon (measuring up to 1 cm in diameter).

Figure 5.

Section from colonic tissue biopsy shows an area of ulceration and a dense infiltrate of eosinophils. Splendore-Hoeppli phenomenon noted around fungal spores. (A) H&E (×4), (B) H&E (×10). Periodic acid-Schiff (PAS) and Grocott methenamine silver (GMS) stains show fungal spores (black arrow) with Splendore-Hoeppli phenomenon. (C) PAS (×20), (D) GMS (×10). H&E, hematoxylin and eosin.

Based on the histology and fungal culture studies, a final diagnosis of basidiobolomycosis was made. Thus, surgical resection was deferred, and the patient was placed on oral voriconazole 6 mg/kg 12 hourly. The patient is doing currently well at 2 years follow-up visit. A multiphase follow-up contrast-enhanced CT scan demonstrated interval resolution of the irregular ileocecal thickening and paracecal lymph nodes. Moreover, there was an interval reduction in the size of hepatic lesions (Fig. 6).

Figure 6.

(A, B) The triphasic follow-up contrast-enhanced computed tomography scan demonstrates interval resolution of the irregular, ileocecal thickening and paracecal lymph nodes (porto-venous phase). (C) Arterial, (D) porto-venous phase. There was an interval reduction in the size of the liver lesions.

DISCUSSION

B. ranarum is a saprophytic fungus found in soil, decomposing plant matter, animal waste, and manure. The mode of infection is through insect bites, contamination of wounds or food with soil, or use of contaminated toilet paper. A review suggested that the pathogenesis of basidiobolomycosis is due to the production of lipases and proteases by the fungus.1,2 Some possible risk factors include ranitidine, a known risk factor for bacterial gastroenteritis, which decreases acidity in the stomach, promoting the survival of the organisms. Another possible risk factor is chronic smoking.3 B. ranarum is known to cause subcutaneous mycoses; subcutaneous infections have been reported mainly in the pediatric population, characterized by firm, painless nodules in the limbs, trunk, perineum, and buttocks.1

Only a handful of cases with liver and gastrointestinal involvement have been reported.4,5-15 The colon and rectum are the most frequently reported gastrointestinal sites, and most affected people are immunocompetent.16 Liver involvement occurs as part of a disseminated infection. Clinical features and radiological findings are often non-specific and therefore pose diagnostic challenges.

In a review, the most common abdominal CT scan finding was a colorectal mass in 48% of cases, followed by a liver mass in 30%.4 Differential diagnoses of colorectal masses include malignancy or Crohns disease in adults and tuberculosis or amebiasis in children.5 Histology and fungal culture help distinguish between these differentials. B. ranarum appears as a faintly stained, broad, sparsely septate pleomorphic fungus on GMS or PAS stains.3 The hyphae range from 5-20 µm in diameter, with a mean of 9 µm.1 Hematoxylin and eosin-stained sections show the characteristic Splendore-Hoeppli phenomenon along with eosinophilic inflammation and zygospores. Splendore-Hoeppli phenomenon is caused by the deposition of eosinophilic and hyaline materials or inert substances around organisms. This eosinophilic material is an antigenantibody complex deposited by inflammatory cells. They are commonly observed in fungal, bacterial, and parasitic infections, although they may sometimes be present in non-infective conditions such as allergic conjunctival granulomas and hypereosinophilic syndrome.6 Zygospores may appear similar to trophozoites of amebae, as they have prominent nucleoli and abundant foamy cytoplasm. Another close differential diagnosis is mucormycosis; this is associated with abundant neutrophilic infiltration unlike the eosinophilic infiltration of basidiobolomycosis, and also often demonstrates vascular invasion and necrosis. The possibility of eosinophilic gastroenteritis can be ruled out based on the presence of fungal hyphae. On culture, fungal colonies appear pale grey along with radial folds on Sabouraud agar after 2-3 days of incubation at 25-30℃.3

Hepatic involvement most commonly mimics a carcinoma; however, as in our case, histological examination and a fungal culture can easily help distinguish between these two. So far, 19 cases of basidiobolomycoses with hepatic involvement have been reported (Table 1).7-17 The patients’ ages ranged from 23 months to 65 years, and the most common clinical presentations were abdominal pain, vomiting, weight loss, and, in some cases, an abdominal mass. The most common colonoscopic findings were obstructive masses involving the cecum and the colon. The most common CT/MRI findings were multiple lesions in the liver, along with a thickened and sometimes edematous intestinal wall. In many cases, cecal masses with or without ascending colon or terminal ileum involvement were noted. Frequent histological findings included eosinophilic infiltration, granuloma formation, the presence of broad aseptate/pauciseptate fungal elements, and Splendore-Hoeppli phenomenon. All patients received antifungal therapy, while surgery was performed in 15 patients. Most patients recovered on follow-up (16 cases), while two died of basidiobolomycosis-associated complications.

Table 1.

Basidiobolomycosis with hepatic involvement: review of literature

Basidiobolomycosis is a rare fungal infection which may also present with gastrointestinal and/or hepatic involvement. As the clinical and radiological features are often nonspecific or suggest the possibility of malignancy, as in this case, its possibility should be considered in the differential diagnosis, especially in endemic regions.

Article information Continued