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 Table of Contents  
ORIGINAL ARTICLE
Year : 2019  |  Volume : 7  |  Issue : 1  |  Page : 1-9

Gastrointestinal basidiobolomycosis: An emerging potentially lethal fungal infection


1 Department of Surgery, Armed Forces Hospital, Southern Region, Khamis Mushait, Saudi Arabia
2 Department of Pathology, Armed Forces Hospital, Southern Region, Khamis Mushait, Saudi Arabia
3 Department of Pathology, King Fahad Hospital, Jazan, Saudi Arabia; Department of Pathology, Alexandria University, Alexandria, Egypt
4 Department of Surgery, King Fahad Hospital, Jazan, Saudi Arabia
5 Department of Paediatric Surgery, Armed Forces Hospital, Southern Region, Khamis Mushait, Saudi Arabia; Department of Paediatric Surgery, Al Galaa Teaching Hospital, Cairo, Egypt
6 Department of Gastroenterology, Armed Forces Hospital, Southern Region, Khamis Mushait, Saudi Arabia

Date of Web Publication14-Mar-2019

Correspondence Address:
Dr. M Ezzedien Rabie
Department of Surgery, Armed Forces Hospital, Southern Region, P. O. Box 101, Khamis Mushait
Saudi Arabia
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ssj.ssj_7_18

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  Abstract 

Background: Gastrointestinal basidiobolomycosis (GIB) is a newly emerging rare tropical fungal infection which affects immunocompetent individuals.
Patients and Methods: Our database was reviewed to identify patients with biopsy-proven gastrointestinal basidiobolomycosis.
Results: Six patients were recognized, two females and four males, with a median age of 23.5 years (range 11–70). All patients came from the same region and all had eosinophilia and they were all immunocompetent. The clinical and radiological features simulated colorectal malignancy in four patients, inflammatory bowel disease in one patient, and left iliac fossa mass in another patient. The diagnosis was established after extensive colonic surgery in four patients, after open biopsy in one patient and after ultrasound-guided biopsy in another. All patients received prolonged antifungal treatment. In those who received extensive colonic surgery, one patient died, two patients recovered, and one is still receiving antifungal treatment. Patients in whom the diagnosis was established by biopsy only, one patient recovered while the other is showing steady improvement.
Conclusion: GIB is a potentially lethal fungal infection, which affects immunocompetent individuals in temperate and hot arid regions of the world, including Saudi Arabia, Iraq, Iran, and Arizona desert in the United States. The patient usually presents with features suggestive of colonic malignancy, inflammatory bowel disease, or abdominal mass. Establishing the diagnosis by endoscopic- or radiology-guided biopsy, serological tests, fungal cultures, or molecular techniques enables the institution of antifungal treatment, which may lead to complete cure without surgery. With or without surgery prolonged antifungal therapy is always required.

Keywords: Antifungal agents, Arizona, basidiobolomycosis, colonoscopy, Saudi Arabia, surgery


How to cite this article:
Rabie M E, Al Qahtani AS, Jamil S, Mikhail NT, El Hakeem I, Hummadi A, Elshaar KE, Abdelraheem I, Saudi D. Gastrointestinal basidiobolomycosis: An emerging potentially lethal fungal infection. Saudi Surg J 2019;7:1-9

How to cite this URL:
Rabie M E, Al Qahtani AS, Jamil S, Mikhail NT, El Hakeem I, Hummadi A, Elshaar KE, Abdelraheem I, Saudi D. Gastrointestinal basidiobolomycosis: An emerging potentially lethal fungal infection. Saudi Surg J [serial online] 2019 [cited 2019 Sep 16];7:1-9. Available from: http://www.saudisurgj.org/text.asp?2019/7/1/1/254116


  Introduction Top


Gastrointestinal fungal infections are an uncommon encounter for the surgeon, gastroenterologist, and radiologist alike. The unfamiliarity with this entity, usually leads to much confusion and diagnostic delay.

An emerging fungal infection is gastrointestinal basidiobolomycosis (GIB) caused by Basidiobolus species, which belong to the order Entomophthorales. Entomophthorales and Mucoralesare the two orders of the fungal class Zygomycete. The pathogenic potentials of both orders are totally different, with the first affecting the immunocompetent patients and the later affecting immunocompromised individuals, causing a mortality of >60%. In the order Entomophthorales, two genera are included, namely, Basidiobolus and Conidiobolus.[1]

Of emerging surgical significance is the fungus Basidiobolus ranarum, which is present in soil and inhabits the intestine of reptiles, amphibians, and insectivorous bats.[1],[2] Surprisingly, it has been detected as a part of the mycobiota, normally inhabiting the gastrointestinal tract of the humans.[3]


  Patients and Methods Top


Our histopathology records were reviewed to identify patients with biopsy-proven GIB. Patients' records were retrieved and their demographic features, geographic residence, clinical course, and antifungal treatment were extracted. Data missing from the records were obtained through telephone communication with the patients.

This research has been conducted in accordance with the International Standards of Ethics as stated in the Helsinki Declaration and its various modifications, and it has been approved by the research ethics committee, xxxxx: code: AFHSRMREC/2015/GEN. SURGERY/062. Date: 7-6-2015.

All patients or patient's guardians gave their informed consent for the study.

Statistical analysis

As a small case series encompassing 6 cases, no advanced statistical analysis was necessary.


  Results Top


We identified six patients with GIB, two females and four males, with a median age of 23.5 years (range 11–70). All patients came from the hot zone in the Southwestern region of Saudi Arabia (the hot zone of Aseer and Jazan). Three patients came from Jazan, two from Tohama, and one from Mohayel. They were all immunocompetent and eosinophilia was present in all of them except the 6th patient, in whom the differential white blood count was not requested.

The diagnosis was established after extensive colonic surgery in four patients, after open biopsy in one patient and after ultrasound (US)-guided biopsy in another [Table 1]. After establishing the diagnosis, all patients received prolonged antifungal treatment. In those who received extensive colonic surgery, one patient died, two patients recovered, and one is still receiving antifungal treatment. The patient in whom the diagnosis was established by open biopsy recovered under antifungal treatment only, while that in whom the diagnosis was established with US-guided biopsy no surgery was recommended and is showing steady improvement under antifungal treatment.
Table 1: Nature of biopsy and its success in establishing the diagnosis

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The site of the disease as well as its presentation, treatment given, and its result are shown in [Table 2]. The antifungal regimen is shown in [Table 3].
Table 2: Site of the disease, presentation, treatment provided, positive biopsy modality, and outcome

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Table 3: Antifungal treatment, its route, dose, and duration

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Representative cases

First case

A 22-year-old male, referred with a bleeding rectal mass, discovered on colonoscopy [Figure 1]. As malignancy was suspected, multiple biopsies were taken.
Figure 1: Colonoscopic view of the anorectal mass with ulcerating surface

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On examination, the patient looked well and rectal examination revealed multiple nodular masses in the upper part of the anal canal and lower rectum.

His blood picture showed low haemoglobin (10.2 g/dl, reference range 14–18) and eosinophilia (22%, reference range <7). Computed tomography (CT) scan showed diffuse thickening of the rectal wall with multiple paraaortic and pelvic lymphadenopathy. Histopathology of colonoscopic biopsies showed an inflammatory process with no malignant cells detected, and the histopathologist advised for deeper biopsy. Multiple deep proctoscopic biopsies were taken for histopathology examination and culture for acid–fast bacilli (AFB). The histopathology reported eosinophilic proctitis and the culture for AFB came negative.

Due to the high clinical suspicious of rectal malignancy, we decided to repeat the tissue biopsy, where a nodule along with the deeper tissues of the rectal wall was excised [Figure 2]. Meanwhile, serological tests for schistosomiasis and amoebiasis were requested and came negative.
Figure 2: Excision biopsy of an anorectal mass

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Finally, the histopathological examination showed fungal proctitis with transmural acute inflammatory cells, mainly neutrophils and many eosinophils and chronic granulomatous inflammation with foreign body type multinucleated giant cells, some of which are engulfing fungal hyphae. The free fungi were surrounded by intense eosinophilic material that clearly demonstrates the presence of the fungus (Splendore–Hoeppli phenomenon). The fungi have thin wall and irregular outline and can be seen collapsed or twisted forming enlargement like small balls. They are pauciseptate and branches at acute angles. They stain with hematoxylin and eosin, Periodic acid–Schiff, and Gomori methenamine silver stains very well, features highly suggestive of basidiobolomycosis [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7].
Figure 3: Fungal form surrounded by dense eosinophilic reaction (yellow oval, H and E ×40)

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Figure 4: Fungi stained with Gomori's methenamine silver ×400

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Figure 5: Fungi stained with Periodic acid–Schiff ×400

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Figure 6: Multinucleated foreign body giant cells engulfing fungi (H and E, ×400)

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Figure 7: Eosinophils and neutrophils around fungi as well as chronic inflammatory cells (H and E, ×100)

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The patient was started on itraconazole 200 mg IV for 2 weeks, then shifted to voriconazole 200 mg IV for 4 weeks, and then oral voriconazole 200 mg BID was started to complete 1 year of antifungal treatment, with regular monitoring of blood picture, liver, and renal functions.

In his last OPD visit, few months later, the patient looked in good health with complete disappearance of the anorectal masses.

Second case

A 17-year-old previously healthy female presented with extensive bilateral perianal and gluteal brawny swellings. She underwent incision and drainage of perianal abscess twice in the preceding 2 months.

Her laboratory investigations were normal apart from leukocytosis and eosinophilia. Crohn's disease was suspected and colonoscopy was performed, but colonoscopic biopsy showed chronic nonspecific inflammation. CT scan showed extensive perianal collection extending up in the retroperitoneum with the right perinephric collection. Incision and drainage of both the gluteal regions and perinephric collections were done. The general condition of the patient continued to deteriorate with progressive muscle wasting, which culminated into hemiparesis. Locally, the skin overlying the sacrum sloughed exposing the underlying unhealthy looking muscles [Figure 8].
Figure 8: Skin sloughing, exposing the underlying partially necrotic gluteal muscles and sacrum

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Diagnostic laparoscopy showed a mass involving the ileocecal region, for which ileocecal resection with end ileostomy was performed to divert the stools away from the perianal and gluteal regions.

Histopathological examination showed features suggestive of basidiobolomycosis [Figure 9]. Upon this, intravenous fluconazole 200 mg OD, then voriconazole 100 mg PO BD were added to the antibiotics agents. Repeated debridement of the perianal and gluteal regions was carried out, with a seemingly favourable response [Figure 10].
Figure 9: Splendore–Hoeppli phenomenon (yellow circle): central fungal forms surrounded by a thick eosinophilic cuff (H and E, ×40)

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Figure 10: Apparently healthy-looking gluteal muscles

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Unfortunately, after 3 months of her hospital stay, heavy trickling of blood from the gluteal region started and the patient was shifted immediately to the operation theater. On exploration, profuse bleeding from an unrecognized source deep in the pelvis started. The infection appeared to excavate and destroy the region, including the vessels and nerves, under the apparently intact gluteal muscles. Control of bleeding failed due to extensive tissue maceration and despite the surgical efforts and massive transfusions, the patient expired.


  Discussion Top


Basidiobolomycosis is a known, though rare, infection caused by the fungus B. ranarum. Seen mainly in the tropics, it affects the skin and subcutaneous tissue of the limbs and trunk of immunocompetent individuals, following minor trauma or insect bites.[4],[5] Relatively recently, GIB has been reported and new cases were discovered, probably due to increased awareness of the condition.

In their review of the English literature from 1964 to 2013, Geramizadeh et al. were able to identify only 71. Most of them came from the US (23 cases), Saudi Arabia (23 cases), Iran (17 cases), Iraq (6 cases), Kuwait, and the Nederland (one case each).[6] In another report from Mayo Clinic published in 2015, 73 cases were identified worldwide.[7] The disease affects the adult as well as the pediatric populations and most pediatric cases came from Saudi Arabia. Out of 27 reported pediatric cases, 19 came from Saudi Arabia.[8]

The rarity of this disease, added to the unfamiliarity of the concerned physicians with it and its clinical, endoscopic, and radiologic similarity to the more common abdominal malignancy, inflammatory bowel disease or tuberculosis[7],[9],[10],[11],[12],[13],[14] often delays the diagnosis and lead to an extensive and probably unnecessary surgery. In this series, the diagnosis was established after extensive colonic resection in three cases, the 2nd, 3rd, and 4th patient, while it was established by transanal incisional biopsy, after failure of repeated colonoscopic biopsies, in the 1st patient, and by US-guided biopsy in the 5th patient. In only one patient in this series, the 6th patient, was the diagnosis established by colonoscopic biopsy.

Obviously, the identification of basidiobolomycosis on biopsy specimens may avoid an unnecessary and often major surgery as the organism responds well to the antifungal treatment.[14],[15] This was the case in our 1st and 5th patient. However, despite that, the diagnosis was established by colonoscopic biopsy in the 6th patient, the fear of imminent colonic obstruction led us to perform right hemicolectomy. In this regard, colonoscopic biopsy may only show nonspecific inflammation or granulomatous reaction, as seen in the 1st, 2nd, and 4th patient in this series. Only exceptionally may it reveal fungal forms,[14] as seen in our 6th patient. This failure of endoscopic biopsy to establish the diagnosis has been reported in the majority of published cases.[6],[15] It is probable that the fungi reside deep to the mucosa, rendering its retrieval within the biopsy specimen difficult.

Although histopathological examination of biopsy specimens is currently the major diagnostic modality, other ancillary means exist. These include fungal cultures, serological tests, and molecular techniques which, when available, may establish the diagnosis with certainty.[16] On histopathology, thin-walled irregularly branching hyphae with occasional septae may be seen surrounded by dense eosinophilic reaction (Splendore–Hoeppli phenomenon).[14],[16],[17] These morphologic characters were seen in all our cases as well as all those reported.[6] It is to be noted that this picture differs from the picture of other invasive gastrointestinal fungi like mucormycosis.[18],[19],[20] Once seen, these features enable an almost certain diagnosis to be made, although some authors have argued that the unequivocal diagnosis requires fungal cultures[21] and/or specific serological tests and molecular techniques. However, in practice, the finding of hyphae showing the morphological features already mentioned may be the only available means as the diagnosis is rarely suspected for tissue cultures to be performed, before immersing the biopsy material in formalin, which destroys all fungal forms. Moreover, fungal culture may be falsely negative in as much as 50% of cases.[6] However, their main value emerges when the tiny biopsy material, whether colonoscopic or CT guided, contain few fungal forms. In these conditions, tissue cultures enable a more detailed study of the fungus to conducted. This recently happened in one of our patients, not included in this series, where the colonoscopic biopsy showed only one fungal form. Fortunately, in anticipation of the diagnosis, part of the specimen was used for tissue culture, which came positive. It must also be mentioned that serological tests including immunodiffusion tests with its reported high sensitivity and specificity,[22],[23] and molecular techniques for identifying fungal DNA,[24],[25] are unavailable in the majority of centers dealing with this rare infection. This leaves the histopathologic examination as the mainstay diagnostic tool.

In any case, with or without surgery, a prolonged antifungal treatment should follow.[10],[14],[15] In this series, the shortest period of antifungal therapy was 6 months and the longest is not known yet, as some patients are still on prolonged antifungal therapy (the 1st, 5th and 6th patient). However, the longest completed course was 18 months (the 3rd patient). In this regard, the choice and duration of the antifungal therapy was at the hands of the physicians in conjunction with the clinical pharmacist, and as the disease is rare with no previous local experience exists, different drugs were chosen without a clear indication of the superiority of one over the other. However, in any circumstance, regular follow-up with periodic liver and renal functions is mandatory, as was customary in this series.

Fungal species form part of the gastrointestinal microflora and contrary to the microbiome, with its known physiologic significance, the function of the mycobiome, if any, remains unknown.[26] This mycobiome includes 390 fungal species living on the skin, vagina, and orodigestive tract and Basidiomycota and Zygomycot a phyla are represented here. Although no sex difference regarding the predominant species was observed, B. ranarum is much more prevalent in male individuals.[3] In this regard, factors which lead to the establishment of this devastating infection remains unknown, and it is notable that all our patients as well as all other reported cases, were immunocompetent.[6]

A notable finding in this study is the area of residence of the patients. The Southwestern region of Saudi Arabia is composed of two provinces, Aseer region and Jazan. Both contain mountainous areas and lowlands, with the lowlands having a hot climate. In this series, three patients came from the lowlands of Jazan and three from the lowlands of Aseer: two from Tohama and the other from Mohayel. The endemicity of these regions with Basidiobolus has been previously reported.[12] This underscores the importance of considering GIB in relevant cases hailing from these areas. Moreover, as eosinophilia was seen in five patients presented here, it might serve as an additional sign to heighten the suspicion. However, as the disease is rare, the significance of knowing its geographical distribution may remain limited.

For completion, we conducted a literature search for published cases till date. Our PubMed search utilizing the term gastrointestinal basidiobolomycosis, yielded 44 reports. Due to the fact that few cases may have been reported more than once, probably in a trial to address the topic from a different angle, the exact number of cases could not be easily known. The results of the search are summarized in [Table 4], [Table 5], [Table 6], where [Table 4] shows reported cases in the pediatric population,[8],[11],[12],[17],[27],[28],[29],[30],[31],[32],[33],[34],[35],[36],[37],[38],[39],[40] [Table 5] shows reported cases in the adult population[9],[10],[13],[14],[15],[16],[21],[41],[42],[43],[44],[45],[46],[47],[48],[49],[50],[51],[52],[53],[54],[55],[56] and [Table 6] shows mixed reports in pediatric and adult populations.[57],[58]
Table 4: Reported cases in the pediatric population

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Table 5: Reported cases in adults

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Table 6: Mixed reports of pediatric and adult patients

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  Conclusion Top


GIB is a potentially lethal fungal infection, which affects immunocompetent individuals in temperate and hot arid regions of the world, including Saudi Arabia, Iraq, Iran, and Arizona desert in the United States. The patient usually presents with features suggestive of colonic malignancy, inflammatory bowel disease, or abdominal mass. Although difficult, establishing the diagnosis by endoscopic- or radiology-guided biopsy, serological tests, fungal cultures, or molecular techniques enables the institution of antifungal treatment, which may lead to complete cure without surgery. Whether surgery is performed or not, prolonged antifungal therapy is always required.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9], [Figure 10]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]



 

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