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Chapter 119 : Agents of Systemic and Subcutaneous Mucormycosis and Entomophthoromycosis

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Abstract:

Mucormycosis and entomophthoromycosis are invasive fungal infections caused by environmental nonseptate filamentous fungi. Mucormycosis is caused by the ubiquitous Mucorales fungi and occurs mostly in immunocompromised patients or those with diabetes mellitus. Entomophthoromycosis is caused by the Entomophthorales fungi, found mostly in warm climates. According to the classification proposed by Hibbet et al. the subphylum Entomophthoromycotina contains the order Entomophthorales, which is subdivided into two families: the Ancylistaceae and Basidiobolaceae, containing the genera and , respectively. There are 27 species in the genus , but only two ( and ) have been recovered from clinical specimens, while in the genus , is the only species known to cause human disease. Several recent reports have suggested that the incidence of mucormycosis is increasing, based on single-center studies. Mucormycosis represents 2% of invasive fungal infections following solid organ transplantion (SOT), mostly after kidney transplantation. Mucormycosis can also develop in human immunodeficiency virus-infected patients or intravenous drug abusers. Blood cultures have no diagnostic value, as they are almost always negative, despite the fact that mucormycosis is an angioinvasive disease. Demonstration of hyphae in clinical samples is important for the diagnosis of mucormycosis. In summary, new molecular tools have been developed for the diagnosis of mucormycosis and the identification of Mucorales fungi in tissues. Culture results should always be interpreted in light of the clinical presentation and along with the results of direct examination and histopathology.

Citation: Garcia-Hermoso D, Dannaoui E, Lortholary O, Dromer F. 2011. Agents of Systemic and Subcutaneous Mucormycosis and Entomophthoromycosis, p 1880-1901. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch119

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Figures

Image of FIGURE 1
FIGURE 1

Flow diagram following the processing of a sample in the mycology/microbiology laboratory or the histopathology laboratory. PE, paraffin embedded; HE, hematoxylin-eosin stain; PAS, periodic acid-Schiff stain; GMS, Gomori methenamine silver stain.

Citation: Garcia-Hermoso D, Dannaoui E, Lortholary O, Dromer F. 2011. Agents of Systemic and Subcutaneous Mucormycosis and Entomophthoromycosis, p 1880-1901. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch119
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Image of FIGURE 2
FIGURE 2

Schematic drawings of morphological structures observed in Mucorales. Sporangiophores (A) bear sporangia containing sporangiospores (D), can be anchored to the substrate by rhizoids (B), and expand by the means of stolons (C). The columella (E) is produced at the apex of the sporangiophore, and in some species an apophysis (G) is present. (F) For some species, after liberation of sporangiospores, a thin sporangium membrane may be visible. Sporangia with single or few spores are called sporangiola (H), and sporangia with few spores aligned in rows are called merosporangia (I). Thick-walled chlamydospores (J) and oidia (thin-walled swollen vesicles) (K) can be observed. (Drawings by Dea Garcia-Hermoso.)

Citation: Garcia-Hermoso D, Dannaoui E, Lortholary O, Dromer F. 2011. Agents of Systemic and Subcutaneous Mucormycosis and Entomophthoromycosis, p 1880-1901. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch119
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Image of FIGURE 3
FIGURE 3

Culture variability of some of the genera of Mucorales and their branching development.

Citation: Garcia-Hermoso D, Dannaoui E, Lortholary O, Dromer F. 2011. Agents of Systemic and Subcutaneous Mucormycosis and Entomophthoromycosis, p 1880-1901. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch119
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Image of FIGURE 4
FIGURE 4

Flow diagram for the identification of the different genera of Mucorales. Data from references and .

Citation: Garcia-Hermoso D, Dannaoui E, Lortholary O, Dromer F. 2011. Agents of Systemic and Subcutaneous Mucormycosis and Entomophthoromycosis, p 1880-1901. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch119
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Image of FIGURE 5
FIGURE 5

. (A) Branched sporangiophores; (B) hemispheric columellae and sporangiospores; (C) pyriform multispored sporangium and marked conical apophysis; (D) sporangiospores.

Citation: Garcia-Hermoso D, Dannaoui E, Lortholary O, Dromer F. 2011. Agents of Systemic and Subcutaneous Mucormycosis and Entomophthoromycosis, p 1880-1901. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch119
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Image of FIGURE 6
FIGURE 6

Typical microscopic features of . (A) Melanized sporangiophore arising opposite rhizoids; (B) striate angular sporangiospores.

Citation: Garcia-Hermoso D, Dannaoui E, Lortholary O, Dromer F. 2011. Agents of Systemic and Subcutaneous Mucormycosis and Entomophthoromycosis, p 1880-1901. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch119
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Image of FIGURE 7
FIGURE 7

Short pigmented sporangiophores arising in pairs in . (A and C) Rhizoids; (B) conical columella; (D) chlamydospores.

Citation: Garcia-Hermoso D, Dannaoui E, Lortholary O, Dromer F. 2011. Agents of Systemic and Subcutaneous Mucormycosis and Entomophthoromycosis, p 1880-1901. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch119
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Image of FIGURE 8
FIGURE 8

. Sporangiophores with apical branching (A), simple rhizoids (B), and globose sporangia with round and smooth-walled sporangiospores (C and D) are shown.

Citation: Garcia-Hermoso D, Dannaoui E, Lortholary O, Dromer F. 2011. Agents of Systemic and Subcutaneous Mucormycosis and Entomophthoromycosis, p 1880-1901. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch119
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Image of FIGURE 9
FIGURE 9

Micromorphology of . (A) Sporangiophore; (B) sporangia; (B and C) ellipsoidal sporangiospores; (D) oidia.

Citation: Garcia-Hermoso D, Dannaoui E, Lortholary O, Dromer F. 2011. Agents of Systemic and Subcutaneous Mucormycosis and Entomophthoromycosis, p 1880-1901. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch119
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Image of FIGURE 10
FIGURE 10

. (A) Unbranched sporangiophores bearing multispored sporangia with a vase-shaped apophysis (B and C); (D) cylindrical sporangiospores.

Citation: Garcia-Hermoso D, Dannaoui E, Lortholary O, Dromer F. 2011. Agents of Systemic and Subcutaneous Mucormycosis and Entomophthoromycosis, p 1880-1901. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch119
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Image of FIGURE 11
FIGURE 11

. (A and B) Mostly unbranched sporangiophores without rhizoids; (C) young sporangiolum; (D to F) recurved stalks arising from terminal vesicles and bearing few spored sporangiola.

Citation: Garcia-Hermoso D, Dannaoui E, Lortholary O, Dromer F. 2011. Agents of Systemic and Subcutaneous Mucormycosis and Entomophthoromycosis, p 1880-1901. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch119
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Image of FIGURE 12
FIGURE 12

. (A, B, and D) Development of single-spored sporangiola on the surfaces of globose vesicles, with frequent apical branching (C); (E) mature sporangiola grow to be single echinulate sporangiospores; (F) rhizoids.

Citation: Garcia-Hermoso D, Dannaoui E, Lortholary O, Dromer F. 2011. Agents of Systemic and Subcutaneous Mucormycosis and Entomophthoromycosis, p 1880-1901. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch119
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Image of FIGURE 13
FIGURE 13

Short sporangiophores arising from rhizoids (A), terminal vesicles covered by merosporangia (B, C, and E), and merospores (D) characteristic of .

Citation: Garcia-Hermoso D, Dannaoui E, Lortholary O, Dromer F. 2011. Agents of Systemic and Subcutaneous Mucormycosis and Entomophthoromycosis, p 1880-1901. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch119
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Image of FIGURE 14
FIGURE 14

. (A and B) Unbranched sporangiophores with dark rhizoids and typical multispored flask-shaped sporangia.

Citation: Garcia-Hermoso D, Dannaoui E, Lortholary O, Dromer F. 2011. Agents of Systemic and Subcutaneous Mucormycosis and Entomophthoromycosis, p 1880-1901. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch119
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Image of FIGURE 15
FIGURE 15

. (A) Ten-day-old powdery colony on PDA medium; (B) primary conidia with papilla; (C) passively released secondary conidium (arrow); (D) villose conidium.

Citation: Garcia-Hermoso D, Dannaoui E, Lortholary O, Dromer F. 2011. Agents of Systemic and Subcutaneous Mucormycosis and Entomophthoromycosis, p 1880-1901. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch119
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Image of FIGURE 16
FIGURE 16

. (A) Ten-day-old wrinkled colony on PDA medium; (B) uninucleated hyphal elements; (C) young zygospores.

Citation: Garcia-Hermoso D, Dannaoui E, Lortholary O, Dromer F. 2011. Agents of Systemic and Subcutaneous Mucormycosis and Entomophthoromycosis, p 1880-1901. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch119
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Tables

Generic image for table
TABLE 1

Species of Mucorales (subphylum Mucoromycotina Benny, subphylum nova) involved in human mucormycosis

Data from references and .

Implication in human infection is not confirmed.

Citation: Garcia-Hermoso D, Dannaoui E, Lortholary O, Dromer F. 2011. Agents of Systemic and Subcutaneous Mucormycosis and Entomophthoromycosis, p 1880-1901. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch119
Generic image for table
TABLE 2

Differential characteristics of zygospores in genera involved in mucormycosis

Data from reference .

Citation: Garcia-Hermoso D, Dannaoui E, Lortholary O, Dromer F. 2011. Agents of Systemic and Subcutaneous Mucormycosis and Entomophthoromycosis, p 1880-1901. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch119
Generic image for table
TABLE 3

Main characteristics allowing distinction between species and varieties

Data from references and

Citation: Garcia-Hermoso D, Dannaoui E, Lortholary O, Dromer F. 2011. Agents of Systemic and Subcutaneous Mucormycosis and Entomophthoromycosis, p 1880-1901. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch119
Generic image for table
TABLE 4

Macroscopic and microscopic features of species involved in human infection

Data from reference .

Citation: Garcia-Hermoso D, Dannaoui E, Lortholary O, Dromer F. 2011. Agents of Systemic and Subcutaneous Mucormycosis and Entomophthoromycosis, p 1880-1901. In Versalovic J, Carroll K, Funke G, Jorgensen J, Landry M, Warnock D (ed), Manual of Clinical Microbiology, 10th Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816728.ch119

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