Basidiobolus ranarum

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Basidiobolus ranarum
Basidiobolus (257 20).jpg
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Fungi
Division: Entomophthoromycota
Class: Entomophthoromycetes
Order: Entomophthorales
Family: Basidiobolaceae
Genus: Basidiobolus
Species:
B. ranarum
Binomial name
Basidiobolus ranarum
Eidam (1886)
Synonyms
  • Basidiobolus haptosporusDrechsler (1947)
  • Basidiobolus meristosporusDrechsler (1955)

Basidiobolus ranarum is a filamentous fungus with worldwide distribution. [1] The fungus was first isolated by Eidam in 1886. It can saprophytically live in the intestines of mainly cold-blooded vertebrates and on decaying fruits and soil. The fungus prefers glucose as a carbon source and grows rapidly at room temperature. [2] Basidiobolus ranarum is also known as a cause of subcutaneous zygomycosis, [3] [4] usually causing granulomatous infections on a host's limbs. [5] Infections are generally geographically limited to tropical and subtropical regions such as East and West Africa. [6] Subcutaneous zygomycosis caused by B. ranarum is a rare disease and predominantly affects children and males. [5] Common subcutaneous zygomycosis shows characteristic features and is relatively easy to be diagnosed; while, certain rare cases might show non-specific clinical features that might pose a difficulty on its identification. [7] Although disease caused by this fungus is known to resolve spontaneously on its own, there are a number of treatments available. [8]

Contents

History

In 1886, the fungus was first isolated from the dung and intestinal contents of frogs by Eidam. [9] In 1927, it was found in the intestines of toads, slowworms, and salamanders by Levisohn. [10] In 1956, Joe et al. reported and described the first four cases of zygomycosis in Indonesia. [3] Since then, hundreds of the cases of this infection have been reported. In 1955, Drechsler isolated it from decaying plants material in North America. [11] In 1971, it was first isolated by Nickerson and Hutchison from aquatic animals, suggesting that B. ranarum can survive in a wild range of ecological situations. [12]

Physiology

At room temperature (25–30 °C), colonies of B. ranarum show very rapid growth and are able to reach a diameter of 75–80 mm in a week on suitable growth media. [2] The favored carbohydrate source of this fungus is glucose that can stimulate the growth of its mycelium. [13] Generally, asexual reproduction is favored by glucose and sexual reproduction is favored by acid amines. [14] Primary asexual spores are singly formed on the apices of unbranched hyphae and will then be discharged to form ballistic spores. [15] Secondary asexual spores are singly developed from a hypha that was generated from a geminated ballistic spore. [1] [15] Also, sporangiospores can be generated by internal cleave of the cytoplasm and can then be dispersed when the sporangial wall is dissolved. As a result, the ejected asexual spores can form satellite colonies in a distance. After around 10 days of growth, sexual spores, zygospores with 20–50 μm diameters can also be produced. [16] This fungus is believed to have significant protease and lipase activity. [17] [18] Its lipase has a maximum activity at 35 °C and pH 6.0 [18] while its protease has maximum activity at 30 °C and pH 5.5. [17] Both enzymes might be involved in pathogenesis. [17] [18] Light does not affect hyphal growth light but may influence certain aspects of physiology. [19] First, light may stimulate the production of the asexual spores, and certain blue lights (wavelengths 440 nm and 480 nm) may further stimulate the discharge of those spores. [20] Second, light may also stimulate the induction of aerial hyphae and favor the unicellular configuration of the hyphae while darkness may favor their bicellular configuration. [19]

Morphology

Gustav Lindau illustration of Basidiobolus ranarum Basidiobolus ranarum Linder illustration.jpg
Gustav Lindau illustration of Basidiobolus ranarum

Colonies of B. ranarum are round, flat, waxy, glabrous and radially folded. And, their color is in a range of yellowish-grey to whitish-grey. [15] [21] A one-week-old colony can reach 75–80 mm in diameter. [2] A white bloom, consisting of mycelia and sporangiospores, covers the colonies. [2] Under microscope, younger hyphae are wide and have few septa. Older cultures have colorless zygospores (20–50 μm) with smooth, thick walls and abundant large, spherical, darkly coloured chlamydospores. [1] [15] The colonies commonly produce a strong Streptomyces-like or benzene hexachloride-like odour. [21]

Habitat and ecology

Basidiobolus ranarum has a worldwide distribution [1] and is capable of living saprotrophically in a broad range of ecological situations, [12] indicating its great ecological and physiological tolerance as well as its ubiquity. [6] Basidiobolus ranarum was widely reported from all parts of the world, especially Asia and Africa. [1] It can saprophytically live in the intestines of vertebrates including amphibians (e.g. frogs, toads, salamanders, mudpuppy), reptiles (e.g. chameleons, wall geckoes, snakes, lizards, turtles), and fishes (e.g. sturgeon). [9] [10] [12] [6] [22] [23] [24] [25] In addition, studies also reported occasional presence of B. ranarum in the intestinal contents of mammals such as one bat in India [26] and the kangaroos in Australia. [27] Moreover, other habitats including compost heaps, decaying plant material and soil can also be their place to live. [11] [22] [28] However, the habitat for B. ranarum is not fixed and a life-cycle illustration of it might provide a better idea of the variation of its habitats. First, insects might eat feces and decaying plant materials in which B. ranarum might be present, [9] [10] or insects might have physical contact with the strains so that the strains can attach to the insects externally. [6] Then, those insects might be devoured by predators, such as frogs. [9] [10] [6] Next, the fungi will travel through the predator's gastrointestinal tract and might either stay a little bit longer (as long as 18 days) at or leave from the intestine along with the feces. Eventually, the strains in those feces will end up in the soil and some of them will be further transported to decaying plant materials or other organic contents. [6] Also, the tissues that the pathogenic strains of B. ranarum infect can also be considered as its habitats, B. ranarum can also live in both human and non-human animal (e.g. horses, [29] frogs [30] ) tissues. However, instead of a worldwide distribution, the pathogenic lifestyle of B. ranarum only exists in tropical and subtropical regions. [6]

Pathology

Subcutaneous zygomycosis (also known as "entomophthoromycosis basidiobolae", subcutaneous phycomycosis, and basidiobolomycosis) [5] [3] [4] is a both human and non-human animal disease or lesion caused by the granulomatous infection of subcutaneous tissue by B. ranarum. [5] Several enzymes produced by B. ranarum, including lipase and protease, might hydrolyze and utilize the fatty tissues of the host and contribute to the pathogenesis of the infection. [17] [18] [31]

Prevalence, mode of transmission

Considering the broad-range distribution of B. ranarum and its high ubiquity, subcutaneous zygomycosis is not really prevalent. In addition, the fact that infections were only reported at tropical and subtropical regions [32] [33] further limits its prevalence. Currently, the reason why the infections were limited to those regions is not fully understood. [6] However, the low prevalence [7] might be explained by the speculations that the widespread immunity of other species was developed against its infection or the number of the B. ranarum strains with pathogenic characteristics is much lower than the saprophytic strains. [5] Its transmission mode has not been fully understood though certain general ideas about its transmission are widely accepted. Ingestion of B. ranarum is thought to help disperse the agent through the deposition of feces at a distant place where human and other non-human animals might be exposed. [6] [25] As well, the agent may transmit through traumas or insect bites on skin. [5] [34]

Vulnerable groups

Most of the reported cases were from Nigeria and Uganda in Africa as well as Indonesia [35] [36] [37] and thus the residents there might be considered as one of the vulnerable groups. Over 90% of the reported infections occurred on the people under 20 years old; thus the young are thought to be a particularly vulnerable group for this agent. [5] [32] [33] Based on the skewed male to female ratio of infection reported in Nigeria (3:1) and Uganda (3:2), [36] [35] males are substantially more vulnerable to infection. One explanation that has been offered for this observation suggests that male children in endemic regions areas were likely to use decayed leaves which might be associated with pathogenic B. ranarum strains as toilet paper following defecation. [37] Although rarely, the agent can cause gastrointestinal disease which does not show specific vulnerable groups or risk factors. [38]

Clinical features and diagnosis

In general, the clinical presentation of subcutaneous zygomycosis is quite identifiable and characteristic and the diagnosis is fairly easy. Human infection is characterized by the single formation of enlarging, painless and firm swelling in soft tissues on extremities e.g. buttocks, thighs, perineum, trunk. [35] [36] However, as the infection worsens, symptoms such a burning sensation or itchiness may develop in the swollen region. In addition to general severe symptoms, one unusual case reported that the severe perineal infection of a led to acute large intestinal obstruction. [32] Moreover, other rare cases also reported the infections happened on other anatomical regions such as the colon in the case of gastrointestinal basidiobolomycosis. [39] Infections may be associated with a diffusive bluish pigmentation generally associated with swelling. [5] Joint function is often not affected; however, a few other cases reported the subcutaneous infection transfect local muscle tissues and lymph nodes. [40] [41]

Definitive diagnosis requires laboratory effort. Culture, histopathology and immunology can be used to for the diagnosis. First, a portion of the infected tissue will be surgically removed and used for a biopsy. Since the fungus can not tolerate refrigeration, the biopsied material needs to be incubated immediately once it is collected. Then, the examination will investigate the presence of thin-walled, wide, hyaline, coenocytic hyphae and internal cleavage for the production of the sporangiospores in H&E (Haemotoxylin and Eosin) stained sections. [1] Other characteristics of its appearance mentioned in the morphology section might also be used to identify the species. [1] Moreover, the histopathology test will expect a granuloma consisting of a variety of immune cells in which hypha or hyphal fragments (4–10 μm diameter) often stain bright pink in H&E sections. When biopsy is not available, immunofluorescent test can also be used to identify B. ranarum strains. Five specific antigens have been identified that can be used measured in the sera of the infected patients using antibodies conjugated to fluorescein dye. The diagnosis of the rare cases, such as gastrointestinal basidiobolomycosis, is challenging given the nonspecific clinical presentation as well as the need for surgical biopsy.

Treatment

Many cases are thought to resolve spontaneously, [8] although surgical intervention may be help to debulk the infected tissue. [7] The most common treatment is taking potassium iodide (KI) on a daily basis for a half of a year to one-year period. For the patients who can not response to KI, some successful cases with other treatments also reported that medications including cotrimoxazole, [42] amphotericin B, [25] itraconazole, [43] and ketoconazole [42] might also show beneficial effects. In addition, given the fact that Conidiobolus coronatus infection causes a similar disease as B. ranarum infection does, coupled with the fact that fluconazole shows great effects on treating C. coronatus infection, there might be a possibility that fluconazole will also be effective in treating B. ranarum infection.

Related Research Articles

<span class="mw-page-title-main">Zygomycosis</span> Medical condition

Zygomycosis is the broadest term to refer to infections caused by bread mold fungi of the zygomycota phylum. However, because zygomycota has been identified as polyphyletic, and is not included in modern fungal classification systems, the diseases that zygomycosis can refer to are better called by their specific names: mucormycosis, phycomycosis and basidiobolomycosis. These rare yet serious and potentially life-threatening fungal infections usually affect the face or oropharyngeal cavity. Zygomycosis type infections are most often caused by common fungi found in soil and decaying vegetation. While most individuals are exposed to the fungi on a regular basis, those with immune disorders (immunocompromised) are more prone to fungal infection. These types of infections are also common after natural disasters, such as tornadoes or earthquakes, where people have open wounds that have become filled with soil or vegetative matter.

Phycomycosis is an uncommon condition of the gastrointestinal tract and skin most commonly found in dogs and horses. The condition is caused by a variety of molds and fungi, and individual forms include pythiosis, zygomycosis, and lagenidiosis. Pythiosis is the most common type and is caused by Pythium, a type of water mould. Zygomycosis can also be caused by two types of zygomycetes, Entomophthorales and Mucorales. The latter type of zygomycosis is also referred to as mucormycosis. Lagenidiosis is caused by a Lagenidium species, which like Pythium is a water mould. Since both pythiosis and lagenidiosis are caused by organisms from the class Oomycetes, they are sometimes collectively referred to as oomycosis.

<span class="mw-page-title-main">Basidiobolomycosis</span> Fungal disease

Basidiobolomycosis is a fungal disease caused by Basidiobolus ranarum. It may appear as one or more painless firm nodules in the skin which becomes purplish with an edge that appears to be slowly growing outwards. A serious but less common type affects the stomach and intestine, which usually presents with abdominal pain, fever and a mass.

<span class="mw-page-title-main">Entomophthorales</span> Order of fungi

The Entomophthorales are an order of fungi that were previously classified in the class Zygomycetes. A new subdivision, Entomophthoromycotina, in 2007, was circumscribed for them.

<span class="mw-page-title-main">Conidiobolomycosis</span> Fungal infection

Conidiobolomycosis is a rare long-term fungal infection that is typically found just under the skin of the nose, sinuses, cheeks and upper lips. It may present with a nose bleed or a blocked or runny nose. Typically there is a firm painless swelling which can slowly extend to the nasal bridge and eyes, sometimes causing facial disfigurement.

Exophiala jeanselmei is a saprotrophic fungus in the family Herpotrichiellaceae. Four varieties have been discovered: Exophiala jeanselmei var. heteromorpha, E. jeanselmei var. lecanii-corni, E. jeanselmei var. jeanselmei, and E. jeanselmei var. castellanii. Other species in the genus Exophiala such as E. dermatitidis and E. spinifera have been reported to have similar annellidic conidiogenesis and may therefore be difficult to differentiate.

<span class="mw-page-title-main">Mucormycosis</span> Fungal infection

Mucormycosis, also known as black fungus, is a serious fungal infection that comes under fulminant fungal sinusitis, usually in people who are immunocompromised. It is curable only when diagnosed early. Symptoms depend on where in the body the infection occurs. It most commonly infects the nose, sinuses, eyes and brain resulting in a runny nose, one-sided facial swelling and pain, headache, fever, blurred vision, bulging or displacement of the eye (proptosis), and tissue death. Other forms of disease may infect the lungs, stomach and intestines, and skin. The fatality rate is about 54%.

<i>Fonsecaea pedrosoi</i> Species of fungus

Fonsecaea pedrosoi is a fungal species in the family Herpotrichiellaceae, and the major causative agent of chromoblastomycosis. This species is commonly found in tropical and sub-tropical regions, especially in South America, where it grows as a soil saprotroph. Farming activities in the endemic zone are a risk factor for the development of chromoblastomycosis.

Saksenaea vasiformis is an infectious fungus associated with cutaneous or subcutaneous lesions following trauma. It causes opportunistic infections as the entry of the fungus is through open spaces of cutaneous barrier ranging in severity from mild to severe or fatal. It lives in soils worldwide, but is considered as a rare human pathogen since only 38 cases were reported as of 2012. Saksenaea vasiformis usually fails to sporulate on the routine culture media, creating a challenge for early diagnosis, which is essential for a good prognosis. Infections are usually treated using a combination of amphotericin B and surgery. Saksenaea vasiformis is one of the few fungi known to cause necrotizing fasciitis or "flesh-eating disease".

<i>Conidiobolus coronatus</i> Species of fungus

Conidiobolus coronatus is a saprotrophic fungus, first described by Costantin in 1897 as Boudierella coronata. Though this fungus has also been known by the name Entomophthora coronata, the correct name is Conidiobolus coronatus. C. coronatus is able to infect humans and animals, and the first human infection with C. coronatus was reported in Jamaica in 1965.

Rhizomucor pusillus is a species of Rhizomucor. It can cause disease in humans. R. pusillus is a grey mycelium fungi most commonly found in compost piles. Yellow-brown spores grow on a stalk to reproduce more fungal cells.

<i>Microsporum canis</i> Species of fungus

Microsporum canis is a pathogenic, asexual fungus in the phylum Ascomycota that infects the upper, dead layers of skin on domesticated cats, and occasionally dogs and humans. The species has a worldwide distribution.

<i>Exophiala dermatitidis</i> Species of fungus

Exophiala dermatitidis is a thermophilic black yeast, and a member of the Herpotrichiellaceae. While the species is only found at low abundance in nature, metabolically active strains are commonly isolated in saunas, steam baths, and dish washers. Exophiala dermatitidis only rarely causes infection in humans, however cases have been reported around the world. In East Asia, the species has caused lethal brain infections in young and otherwise healthy individuals. The fungus has been known to cause cutaneous and subcutaneous phaeohyphomycosis, and as a lung colonist in people with cystic fibrosis in Europe. In 2002, an outbreak of systemic E. dermatitidis infection occurred in women who had received contaminated steroid injections at North Carolina hospitals.

Histoplasma duboisii is a saprotrophic fungus responsible for the invasive infection known as African histoplasmosis. This species is a close relative of Histoplasma capsulatum, the agent of classical histoplasmosis, and the two occur in similar habitats. Histoplasma duboisii is restricted to continental Africa and Madagascar, although scattered reports have arisen from other places usually in individuals with an African travel history. Like, H. capsulatum, H. duboisii is dimorphic – growing as a filamentous fungus at ambient temperature and a yeast at body temperature. It differs morphologically from H. capsulatum by the typical production of a large-celled yeast form. Both agents cause similar forms of disease, although H. duboisii predominantly causes cutaneous and subcutaneous disease in humans and non-human primates. The agent responds to many antifungal drug therapies used to treat serious fungal diseases.

Cunninghamella bertholletiae is a species of zygomycetous fungi in the order Mucorales. It is found globally, with increased prevalence in Mediterranean and subtropical climates. It typically grows as a saprotroph and is found in a wide variety of substrates, including soil, fruits, vegetables, nuts, crops, and human and animal waste. Although infections are still rare, C. betholletiae is emerging as an opportunistic human pathogen, predominantly in immunocompromised people, leukemia patients, and people with uncontrolled diabetes. Cunninghamella bertholletiae infections are often highly invasive, and can be more difficult to treat with antifungal drugs than infections with other species of the Mucorales, making prompt and accurate recognition and diagnosis of mycoses caused by this fungus an important medical concern.

<i>Phialophora verrucosa</i> Species of fungus

Phialophora verrucosa is a pathogenic, dematiaceous fungus that is a common cause of chromoblastomycosis. It has also been reported to cause subcutaneous phaeohyphomycosis and mycetoma in very rare cases. In the natural environment, it can be found in rotting wood, soil, wasp nests, and plant debris. P. verrucosa is sometimes referred to as Phialophora americana, a closely related environmental species which, along with P. verrucosa, is also categorized in the P. carrionii clade.

Arthrographis kalrae is an ascomycetous fungus responsible for human nail infections described in 1938 by Cochet as A. langeronii. A. kalrae is considered a weak pathogen of animals including human restricted to the outermost keratinized layers of tissue. Infections caused by this species are normally responsive to commonly used antifungal drugs with only very rare exceptions.

Cladophialophora arxii is a black yeast shaped dematiaceous fungus that is able to cause serious phaeohyphomycotic infections. C. arxii was first discovered in 1995 in Germany from a 22-year-old female patient suffering multiple granulomatous tracheal tumours. It is a clinical strain that is typically found in humans and is also capable of acting as an opportunistic fungus of other vertebrates Human cases caused by C. arxii have been reported from all parts of the world such as Germany and Australia.

Scytalidium hyalinum is an ascomycete fungus currently in the genus Scytalidium. It causes dermatomycosis and systemic infections in humans and it is widespread throughout the world.

Basidiobolus haptosporus belongs to the Kingdom Fungi and is a member of a grouping known as the "zygomycetes". This classification comprises two Phyla- the Mucoromycota and the Zoopagomycota, which are characterized by the production of sexual zygospores and suspensor cells. B. haptosporus is a filamentous fungus with distribution concentrated in Tropical and Subtropical regions. This fungus is largely associated with the gastrointestinal tract of amphibians and reptiles but has also been reported on mite bristles. B. haptosporus has caused disease in humans as well, including Gastrointestinal entomophthoromycosis and subcutaneous phycomycosis. Closely related species include Basidiobolus ranarum, B. meristosporus, B. microsporus, and B. magnus.

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