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Mucormycosis and Entomophthoramycosis: a Review of the Clinical Manifestations, Diagnosis and Treatment R View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Mucormycosis and entomophthoramycosis: a review of the clinical manifestations, diagnosis and treatment R. M. Prabhu1 and R. Patel1,2 1Division of Infectious Diseases and 2Division of Clinical Microbiology, Mayo Clinic College of Medicine, Rochester, Minnesota 55905, USA ABSTRACT The class Zygomycetes is divided into two orders, Mucorales and Entomophthorales. These two orders produce dramatically different infections. Genera from the order Mucorales (Rhizopus, Mucor, Rhizomucor, Absidia, Apophysomyces, Cunninghamella and Saksenaea) cause an angioinvasive infection called mucormycosis. Mucormycosis presents with rhino-orbito-cerebral, pulmonary, disseminated, cutaneous, or gastrointestinal involvement. Immunocompromising states such as haematological malignancy, bone marrow or peripheral blood stem cell transplantation, neutropenia, solid organ transplantation, diabetes mellitus with or without ketoacidosis, corticosteroids, and deferoxamine therapy for iron overload predispose patients to infection. Mucormycosis in immunocompetent hosts is rare, and is often related to trauma. Mortality rates can approach 100% depending on the patient’s underlying disease and form of mucormycosis. Early diagnosis, along with treatment of the underlying medical condition, surgery, and an amphotericin B product are needed for a successful outcome. Genera from the order Entomophthorales produce a chronic subcutaneous infection called entomophthoramy- cosis in immunocompetent patients. This infection occurs in tropical and subtropical climates. The genus Basidiobolus typically produces a chronic subcutaneous infection of the thigh, buttock, and ⁄ or trunk. Rarely, it has been reported to involve the gastrointestinal tract. The genus Conidiobolus causes a chronic infection of the nasal submucosa and subcutaneous tissue of the nose and face. This paper will review the clinical manifestations, diagnosis and treatment of mucormycosis and entomophthoramycosis. Keywords Mucormycosis, entomophthoramycosis, zygomycetes, Mucorales, Entomophthorales, Mucor, Rhizopus, Apophysomyces, Conidiobolus, Basidiobolus Clin Microbiol Infect 2004; 10 (Suppl. 1): 31–47 The terms phycomycosis and zygomycosis have INTRODUCTION previously been used to describe both forms of The class Zygomycetes is divided into two orders, infection. Given their distinct clinical presenta- Mucorales and Entomophthorales (Table 1). Mem- tions, the term ‘mucormycosis’ should be reserved bers of these two orders produce dramatically for those infections caused by Mucorales, and the different infections. In general, members of the term ‘entomophthoramycosis’ for those caused by order Mucorales cause acute, angioinvasive infec- Entomophthorales [2]. This paper will review the tions in immunocompromised patients with mor- clinical manifestations, diagnosis and treatment of tality rates exceeding 60% [1]. In contrast, members mucormycosis, and briefly, those of entomoph- of the order Entomophthorales cause chronic thoramycosis. subcutaneous infections in immunocompetent patients from subtropical and tropical regions. MUCORMYCOSIS After aspergillosis and candidiasis, mucormycosis Corresponding author and reprint requests: R. Patel, Division is the third most common invasive fungal infection of Infectious Diseases, Mayo Clinic College of Medicine, 200 [3]. It represents 8.3–13% of all fungal infections First Street SW, Rochester, Minnesota 55905, USA encountered at autopsy in haematology patients Tel: + 1 507 255 6482 Fax: + 1 507 255 7767 [4,5]. The most commonly recovered genera in- E-mail: [email protected] clude Mucor, Rhizopus, Rhizomucor, Absidia, Ó 2004 Copyright by the European Society of Clinical Microbiology and Infectious Diseases 32 Clinical Microbiology and Infection, Volume 10 Supplement 1, 2004 Table 1. Fungi from the class Class: Zygomycetes Zygomycetes reported as causing Order: Mucorales Entomophthorales infections in humans (older nomen- Genus: Mucor Basidiobolus clature in parentheses) M. racemosus, B. ranarum,(B. haptosporus) M. circinelloides M. ramosissimus Conidiobolus M. indicus C. coronatus M. hiemalis (Entomopthora coronata) C. incongruus Rhizopus R. arrhizus (R. oryzae) R. rhizopodiformis R. azygosporus R. stolonifer R. schipperae R. microsporus var. microsporus var. rhizopodiformis var. oligosporus Rhizomucor R. pusillus Absidia A. corymbifera Apophysomyces A. elegans Cunninghamella C. bertholletiae Saksenaea S. vasiformis Cokeromyces C. recurvatus Adapted from Ribes et al. [9]. Apophysomyces, Cunninghamella, and Saksenaea [3,6]. Table 2. Major risk factors for mucormycosis Mortierella wolfi and Syncephalastrum racemosum Haematological malignancy play questionable roles as human pathogens [7–9]. Leukaemia Five major forms of infection exist—rhino- Lymphoma orbito-cerebral, pulmonary, disseminated, cuta- Multiple myeloma neous, and gastrointestinal. Mucorales enter the Neutropenia Pharmacologic immunosuppression human host through inhalation, percutaneous Antineoplastic chemotherapy inoculation or ingestion [9]. Mucormycosis typ- Corticosteroid therapy ically affects patients with at least one of the Antirejection therapy following immunocompromising states—haema- Diabetes mellitus (Types I and II) with or without tologic malignancy, neutropenia, receipt of high- diabetic ketoacidosis Solid organ transplantation dose corticosteroids, diabetes mellitus, diabetic Bone marrow and peripheral blood stem cell ketoacidosis, organ transplantation, deferoxamine transplantation therapy, trauma and burns (Table 2) [10,11]. Deferoxamine therapy Immunocompetent patients rarely develop Burns Trauma mucormycosis [12]. Malnutrition in children The diagnosis of mucormycosis is challenging. Intravenous drug use In a review of 185 cases of disseminated mucormycosis, Ingram et al. found that an ante mortem diagnosis was made in only 9% of cases reported single institutional series of mucormy- [13,14]. The site of infection influences physicians’ cosis cases [129 over a 10-year period (1990–99)], abilities to make a diagnosis. In pulmonary Chakrabarti et al. observed that rhino-orbito-cer- mucormycosis, 28–74% of cases were diagnosed ebral (91%) and cutaneous (100%) mucormycosis while patients were alive [5,10,11,15]. In the largest were most reliably diagnosed ante mortem, Ó 2004 Copyright by the European Society of Clinical Microbiology and Infectious Diseases, CMI, 10 (Suppl. 1), 31–47 Prabhu and Patel Mucormycosis and entomophthoramycosis 33 compared to pulmonary (31%), renal (44%), liver transplants from 11 to 42%, with heart gastrointestinal (0%) and disseminated (0%) transplants from 2.2 to 6.3%, and with lung forms [16]. A high index of clinical suspicion transplants from 9 to 27.5% [24–39]. Singh et al. and biopsy accessibility influence physicians’ reported that 80% of cases in solid organ trans- diagnostic abilities as well. plant recipients occurred within 6 months of transplantation [40]. Mucormycosis has been reported from all Epidemiology corners of the world. A few papers have com- The clinical presentation of mucormycosis mented on a possible seasonal variation in Mu- depends on the patient’s underlying medical con- corales infection [5,41]. In Israel, Talmi et al. noted dition. Overall, rhino-orbito-cerebral mucormyco- that 16 of their 19 cases of rhino-orbito-cerebral sis is the most common form (44–49%), followed by mucormycosis occurred between August and cutaneous (10–16%), pulmonary (10–11%), dis- November [41]. In Japan, Funada and Matsuda seminated (6–11.6%) and gastrointestinal (2–11%) noted a similar seasonal variation among haema- presentations [2,17,18]. In patients with haem- tology patients, with six of seven cases of pul- atological malignancy, pulmonary, followed monary mucormycosis having developed by disseminated and rhino-orbtio-cerebral pres- between August and September [5]. entations, are the most common [6]. Diabetics usually develop rhino-orbito-cerebral or pulmon- Microbiological diagnosis ary mucormycosis [11,18]. Some studies have suggested a rising incidence Mucorales are ubiquitous saprophytes found in of mucormycosis. At M. D. Anderson Cancer soil and decaying organic matter [42,43]. They Center in Texas, for example, the number of cases grow on most routine bacterial (i.e. sheep blood increased from eight per 100 000 admissions agar, chocolate agar) and fungal culture media during 1989–93 to 17 per 100 000 admissions (i.e. Sabouraud dextrose agar, inhibitory mould during 1994–98 [6]. The overall incidence of agar, potato dextrose agar) at a wide range of mucormycosis at autopsy at M. D. Anderson temperatures, 25–55 °C [44]. Mucorales present in Cancer Center was 0.7% (12 of 1765 autopsies) clinical specimens will grow at 37 °C [45] and during the period 1989–98 [6]. Among those with form fluffy white, grey, or brownish colonies that haematological malignancies it was 1.9% (12 of rapidly fill the Petri dish within 1–7 days [9,18]. 624 autopsies) [6]. In Japan, Funada and Matsuda Mechanical homogenization of tissue specimens found a similar incidence of 2.1% at autopsy in can lower the yield of cultures [9,11,46]. patients with acute leukaemia [5]. At the Memor- Several different techniques (e.g. treatment with ial Sloan-Kettering Cancer Center in New York, 20% potassium hydroxide, Gomori’s methenam- Meyer et al. reported an incidence of 4% at ine silver staining, haematoxylin & eosin staining, autopsy among patients with
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