Apophysomyces variabilis

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Apophysomyces variabilis
Apophysomyces variabilis.jpg
Scientific classification
Kingdom:
Fungi
Division:
Zygomycota
Class:
Zygomycetes
Order:
Mucorales
Family:
Saksenaeaceae
Genus:
Apophysomyces
Species:
A. variabilis
Binomial name
Apophysomyces variabilis
E.Àlvarez, Stchigel, Cano, D.A.Sutton & Guarro (2010)

Apophysomyces variabilis is an emerging fungal pathogen that can cause serious and sometimes fatal infection in humans. [1] This fungus is a soil-dwelling saprobe with tropical to subtropical distribution. [1] [2] It is a zygomycete that causes mucormycosis, an infection in humans brought about by fungi in the order Mucorales. Infectious cases have been reported globally in locations including the Americas, Southeast Asia, India, and Australia. [1] [2] Apophysomyces variabilis infections are not transmissible from person to person. [3]

Contents

Apophysomyces variabilis is one of four species in the genus Apophysomyces , which also includes A. elegans, A. ossiformis, and A. trapeziformis. [4] In the past, Apophysomyces elegans was believed to be the species responsible for most cases of cutaneous mucormycosis attributed to Apophysomyces , but recently, some of the other species have been shown to be important in human infection. [5] Since the new species have only recently been recognized, much remains to be learned about their relative clinical importance, comparative virulence, epidemiology, and anti-fungal drug susceptibilities. [1]

History

Apophysomyces variabilis (CBS 658.93; FMR 10381 Archived 2016-03-04 at the Wayback Machine ) was first identified by Alvarez et al. in 2010 from a human osteomyelitis patient in the Netherlands Antilles. The genus Apophysomyces was first published in 1979 by Misra et al. who isolated A. elegans from soil in northern India. Apophysomyces variabilis was considered to be the same species as Apophysomyces elegans until September 2012 when Alvarez et al. determined that 16 strains of A. elegans were actually a complex of species in the genus Apophysomyces . Based on genetic, physiological, and morphological analyses, the authors concluded that the sixteen environmental and clinical strains of A. elegans could be divided in four clades corresponding to the species; A. elegans, A. trapeziformis, A. ossiformis, and A. variabilis. The species were differentiated based on the sporangiospore shape, sporangiophore type, and apophyseal shape. As well, carbon fixation ability aided in species differentiation with only A. elegans strains being able to assimilate the glycoside esculin. [4] Alvarez et al. analysed three loci: the H3 gene, the internal transcribed spacer (ITS) regions of the nuclear rRNA gene, and the D1 and D2 domains of the 28S rRNA gene. This analysis resulted in a phylogeny containing the four clades. None of the disease strains that had been identified as "A. elegans" clustered with taxonomically important strains of A. elegans in molecular phylogenetic analyses. Accordingly, the role of A. elegans (in the strict sense) as a human pathogen may warrant reconsideration. [1]

Ecology

Apopysomyces variabilis is a soil fungus found in tropical and subtropical regions. [6] Though the majority of A. variabilis infections have been reported from India, the fungus has also been found in North and South America, Australia, and Southeast Asia. [4] [7] Apophysomyces variabilis is thermotolerant and grows optimally at 35–42 °C. It cannot grow at or above 50 °C. The minimum temperature for growth is 15 °C. [4]

Morphology

Apophysomyces variabilis resembles the other three members of the genus Apophysomyces but is characterized by the variable appearance of its sporangiospores and sporangiophores which range from club-shaped to trapezoidal to flattened spheres. The sporangiophore can measure up to 400 μm in length and has a funnel-shaped apophysis or swelling below the columella. Hyphae are smooth-walled, aseptate, and branched. [4]

Growth and reproduction

Unlike most members of the Mucorales, Apophysomyces species often fail to sporulate under standard clinical laboratory culture conditions. These fungi require Czapek's agar (CZA), a nutrient-defined medium. [2] Colonies grow rapidly at 37 °C on CZA and initially appear white and woolly becoming greyish brown with age. [4] [7] [6] Colonies are grey and floccose, will grow on the lid of the petri dish, and are colourless on reverse. [8] Sporangiosphores are unbranched, smooth-walled, and light brown. [4] Sporangia are apophyseal, pyriform, beginning as whitish and turning brown with maturity. Sporangiospores are variable in size and shape. [7] Sexuality has not been observed in A. variabilis. [8]

Disease in humans

Mucormycosis is commonly contracted via inhalation of spores resulting in rhinocerebral and pulmonary mucormycoses but infection with Apophysomyces variabilis is contracted cutaneously. [2] [9] Apophysomyces species cause infections of the skin and soft-tissue following injuries such as burns, automotive accidents, surgeries, and injections both intramuscular and subcutaneous. [10] Cutaneous mucormycosis is acquired when the sporangiospores from contaminated soil and water come into contact with broken skin. [1] [7] [11] For this reason, disease is seen in burn patients, injured persons, and injection-drug users. [2] The infection may take clinical forms such as necrotizing fasciitis, cerebritis, rhinoorbital infections, and kidney infections. [7] Successful treatment depends on early detection of infection, surgical debridement of necrotic tissues, and anti-fungal therapy with drugs such as posaconazole and amphotericin B. [2] [7] [12] Members of the order Mucorales generally infect immunocompromised patients but A. variabilis infections tend to occur in immunocompetent healthy hosts. [1] [7] [5]

Necrotic lesions are caused by invasion of blood vessels leading to thrombosis and infarction. Though uncommon, cutaneous infections can become disseminated infections. Lesions extend into muscle, tendon, bone, and ultimately spread by the bloodstream to other organs. The brain is the most common site of secondary infection but necrotic lesions may also form in the spleen and heart. [2] [9]

Risk factors for infection

Any penetrating injury that breaks the skin barrier including; burns, injections, intravenous catheterization, and surgical wounds creates risk for developing mucormycosis. These types of situations, in combination with exposure to contaminated material, create opportunity for infection. In many cases of cutaneous mucormycosis, there exists no underlying medical condition. [2]

There is elevated risk for developing mucormycosis in diabetic individuals. Patients with uncontrolled diabetes may develop diabetic ketoacidosis. This condition results in an acidic pH which makes serum iron more available, permitting the growth of Mucorales. [9]

Laboratory detection

Tissue samples from necrotic lesions are examined by microscopy. [12] The presence of aseptate branched hyphae in tissue is a hallmark of mucormycosis. [2] Normally, culture of material from a biopsied lesion is used to recover and identify members of the Mucorales although blood cultures are often negative for these fungi. [9] Cultures may be sterile despite clearing visible fungi in histological preparations. This may be due to hyphae becoming damaged during biopsy or ground up during laboratory procedures making growth in culture very difficult. [13] Unlike many members of the Mucorales, species of Apophysomyces are often slow to sporulate, further complicating rapid culture-based identification. Definitive identification of A. variabilis requires phenotypic and genotypic analysis. Most modern case reports of A. variabilis infection have confirmed identifications against known strains by sequence similarity. [7] [1]

Treatment

Amphotericin B is the most potent antifungal drug available to treat mucormycosis. When given intravenously in the deoxycholate form, amphotericin B is associated with toxic side effects. For this reason, it is often replaced with liposomal amphotericin B, a lipid-based formulation with fewer adverse side effects. [9] Treatment of A. variabilis infections usually involves aggressive antifungal therapy and often surgical removal of necrotic tissue. [12] In mouse models of infection, posaconazole has shown efficacy both in vivo and in vitro . Amphotericin B may also be used to reduce fungal load. In the mouse study, both drugs decreased the amount of hyphae in infected tissues but posaconazole had better survival outcomes than amphotericin B. [5]

In vitro antifungal susceptibility tests of the entire genus Apophysomyces have revealed that amphotericin B and posaconazole are the most effective against A. variabilis infections when compared to itraconazole, ravuconazole, and voriconazole. Testing data has also showed that caspofungin and anidulafungin are inactive antifungal agents against all strains of the genus Apophysomyces . [4]

Epidemiology

Infections from these species are rare. In the United States, for example, the Apophysomyces species complex represents 0.5% of Mucorales isolates from clinical samples. [1] The incidence of mucormycoses due to Apophysomyces is unknown and extent of infection remains uncertain. This is mainly due to the lack of properly preserved isolates from clinical cases and the necessity of genetic analyses for species determination. [1] [7]

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.

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

Sporotrichosis, also known as rose handler's disease, is a fungal infection that may be localised to skin, lungs, bone and joint, or become systemic. It presents with firm painless nodules that later ulcerate. Following initial exposure to Sporothrix schenckii, the disease typically progresses over a period of a week to several months. Serious complications may develop in people who have a weakened immune system.

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

The Mucorales is the largest and best-studied order of zygomycete fungi. Members of this order are sometimes called pin molds. The term mucormycosis is now preferred for infections caused by molds belonging to the order Mucorales.

<i>Apophysomyces</i> Genus of fungi

Apophysomyces is a genus of filamentous fungi that are commonly found in soil and decaying vegetation. Species normally grow in tropical to subtropical regions.

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.

<i>Pseudallescheria boydii</i> Species of fungus

Pseudallescheria boydii is a species of fungus classified in the Ascomycota. It is associated with some forms of eumycetoma/maduromycosis and is the causative agent of pseudallescheriasis. Typically found in stagnant and polluted water, it has been implicated in the infection of immunocompromised and near-drowned pneumonia patients. Treatment of infections with P. boydii is complicated by resistance to many of the standard antifungal agents normally used to treat infections by filamentous fungi.

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".

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.

<i>Ochroconis gallopava</i> Species of fungus

Ochroconis gallopava, also called Dactylaria gallopava or Dactylaria constricta var. gallopava, is a member of genus Dactylaria. Ochroconis gallopava is a thermotolerant, darkly pigmented fungus that causes various infections in fowls, turkeys, poults, and immunocompromised humans first reported in 1986. Since then, the fungus has been increasingly reported as an agent of human disease especially in recipients of solid organ transplants. Ochroconis gallopava infection has a long onset and can involve a variety of body sites. Treatment of infection often involves a combination of antifungal drug therapy and surgical excision.

Phaeohyphomycosis is a diverse group of fungal infections, caused by dematiaceous fungi whose morphologic characteristics in tissue include hyphae, yeast-like cells, or a combination of these. It can be associated an array of melanistic filamentous fungi including Alternaria species,Exophiala jeanselmei, and Rhinocladiella mackenziei.

<i>Lichtheimia corymbifera</i> Species of fungus

Lichtheimia corymbifera is a thermophilic fungus in the phylum Zygomycota. It normally lives as a saprotrophic mold, but can also be an opportunistic pathogen known to cause pulmonary, CNS, rhinocerebral, or cutaneous infections in animals and humans with impaired immunity.

Thielavia subthermophila is a ubiquitous, filamentous fungus that is a member of the phylum Ascomycota and order Sordariales. Known to be found on plants of arid environments, it is an endophyte with thermophilic properties, and possesses dense, pigmented mycelium. Thielavia subthermophila has rarely been identified as a human pathogen, with a small number of clinical cases including ocular and brain infections. For treatment, antifungal drugs such as amphotericin B have been used topically or intravenously, depending upon the condition.

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>Cunninghamella echinulata</i> Species of fungus

Cunninghamella echinulata is a fungal species in the genus Cunninghamella. It is an asexually reproducing fungus and a mesophile, preferring intermediate temperature ranges. C. echinulata is a common air contaminant, and is currently of interest to the biotechnology industry due to its ability to synthesize γ-linolenic acid as well as its capacity to bioconcentrate metals. This species is a soil saprotroph that forms rhizoids, preferring soils enriched in nitrogen, phosphorus and potassium. It has been reported occasionally an agent of mucormycosis following the inhalation of fungal spores. Czapek's agar is a suitable growth medium for the propagation of C. echinulata.

<i>Rhinocladiella mackenziei</i> Species of fungus

Rhinocladiella mackenziei is a deeply pigmented mold that is a common cause of human cerebral phaeohyphomycosis. Rhinocladiella mackenziei was believed to be endemic solely to the Middle East, due to the first cases of infection being limited to the region. However, cases of R. mackenziei infection are increasingly reported from regions outside the Middle East. This pathogen is unique in that the majority of cases have been reported from immunologically normal people.

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.

Mycotypha microspora, also known as Microtypha microspora, is a filamentous fungus in the division Zygomycota. It was discovered in a Citrus aurantium peel in 1932 by E. Aline Fenner, who proposed a new genus Mycotypha to accommodate it. Mycotypha africana, which is another species in the genus Mycotypha, is closely related to M. microspora. The fungus has subsequently been isolated from both outdoor and indoor settings around the world, and is typically found in soil and dung. The species rarely causes infections in humans, but has recently been involved in the clinical manifestation of the life-threatening disease mucormycosis.

Lichtheimia ramosa is a saprotrophic zygomycete, typically found in soil or dead plant material. It is a thermotolerant fungus that has also been known to act as an opportunistic pathogen–infecting both humans and animals.

Actinomucor elegans was originally described by Schostakowitsch in Siberia in 1898 and reevaluated by Benjamin and Hesseltine in 1957. Commonly found in soil this fungus and commonly used for the commercial production of tofu and other products made by soy fermentation. Its major identifying features are its spine-like projections on the sporangiophore and its ribbon-like hyphal structure when found in the tissue of a host.

References

  1. 1 2 3 4 5 6 7 8 9 10 Guarro, Josep; Chandler J; Alvarez E; Stchigel AM; Robin K; Dalal U; Rani H; Punia RS; Cano JF (January 2011). "Apophysomyces variabilis infections in humans". Emerging Infectious Diseases. 17 (1): 134–135. doi:10.3201/eid1701.101139. PMC   3204648 . PMID   21192877.
  2. 1 2 3 4 5 6 7 8 9 Lyon, Errol Reiss, H. Jean Shadomy, G. Marshall (2012). Fundamental medical mycology. Hoboken: Wiley-Blackwell. pp. 431–455. ISBN   9781118101773.{{cite book}}: CS1 maint: multiple names: authors list (link)
  3. ↑ "Sources of Mucormycosis". Center for Disease Control and Prevention. Retrieved 24 October 2013.
  4. 1 2 3 4 5 6 7 8 Alvarez, Eduardo; Stchigel, Alberto M.; Cano, Josep; Sutton, Deanna A.; Fothergill, Annette W.; Chander, Jagdish; Salas, Valentina; Rinaldi, Michael G.; Guarro, Josep (1 April 2010). "Molecular phylogenetic diversity of the emerging mucoralean fungus Apophysomyces: Proposal of three new species". Revista Iberoamericana de Micología. 27 (2): 80–89. doi:10.1016/j.riam.2010.01.006. PMID   20199897.
  5. 1 2 3 Salas, V.; Pastor, F. J.; Calvo, E.; Sutton, D. A.; Chander, J.; Mayayo, E.; Alvarez, E.; Guarro, J. (16 March 2012). "Efficacy of posaconazole in a murine model of disseminated infection caused by Apophysomyces variabilis". Journal of Antimicrobial Chemotherapy. 67 (7): 1712–1715. doi: 10.1093/jac/dks090 . PMID   22427614.
  6. 1 2 Kirk, Paul M. (2008). "Apophysomyces elegans". IMI Descriptions of Fungi and Bacteria (1772). doi:10.1079/DFB/20083311561.
  7. 1 2 3 4 5 6 7 8 9 dela Cruz, W. P.; Calvano, T. P.; Griffith, M. E.; White, C. E.; Kim, S. H.; Sutton, D. A.; Thompson, E. H.; Fu, J.; Wickes, B. L.; Guarro, J.; Hospenthal, D. R. (23 May 2012). "Invasive Apophysomyces variabilis Infection in a Burn Patient". Journal of Clinical Microbiology. 50 (8): 2814–2817. doi:10.1128/JCM.00671-12. PMC   3421509 . PMID   22622444.
  8. 1 2 Campbell, Colin K. (2013). Identification of pathogenic fungi (2nd ed.). Chichester: Wiley. ISBN   978-1-4443-3070-0.
  9. 1 2 3 4 5 Richardson, Malcolm; Warnock, David W. (2010). Fungal infection : diagnosis and management (4th ed.). Oxford: Wiley-Blackwell. ISBN   978-1-4051-7056-7.
  10. ↑ Lewis, Russell E. (27 September 2011). "Cutaneous Mucormycosis in Tornado Survivors". Current Fungal Infection Reports. 5 (4): 187–189. doi:10.1007/s12281-011-0068-4. S2CID   71669702.
  11. ↑ Etienne, Kizee A.; Gillece, John; Hilsabeck, Remy; Schupp, Jim M.; Colman, Rebecca; Lockhart, Shawn R.; Gade, Lalitha; Thompson, Elizabeth H.; Sutton, Deanna A.; Neblett-Fanfair, Robyn; Park, Benjamin J.; Turabelidze, George; Keim, Paul; Brandt, Mary E.; Deak, Eszter; Engelthaler, David M.; Jordan, I. King (27 November 2012). "Whole Genome Sequence Typing to Investigate the Apophysomyces Outbreak following a Tornado in Joplin, Missouri, 2011". PLOS ONE. 7 (11): e49989. doi: 10.1371/journal.pone.0049989 . PMC   3507928 . PMID   23209631.
  12. 1 2 3 Johnson, Malcolm D. Richardson, Elizabeth M. (2006). Pocket Guide to Fungal Infection (2. ed.). Oxford: Blackwell Pub. pp.  75–82. ISBN   1405122188.{{cite book}}: CS1 maint: multiple names: authors list (link)
  13. ↑ Chander, J; Kaur, J; Attri, A; Mohan, H (June 2010). "Primary cutaneous zygomycosis from a tertiary care centre in north-west India". The Indian Journal of Medical Research. 131: 765–70. PMID   20571164.
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