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JOURNAL OF CLINICAL MICROBIOLOGY, Feb. 2001, p. 740–742 0095-1137/01/$04.00ϩ0 DOI: 10.1128/JCM.39.2.740–742.2001 Copyright 2001, American Society for Microbiology. All Rights Reserved.
Maxillary Sinusitis Caused by Actinomucor elegans GRACIELA DAVEL,1* PATRICIA FEATHERSTON,2 ANIBAL FERNA CRISTINA CANTEROS,1 LAURA RODERO,1 CARLOS SZTERN,3 AND DIEGO PERROTTA1 Departamento Micologı´a, INEI, ANLIS Dr. Carlos G. Malbra´n, Buenos Aires,1 and Hospital San Juan de Dios2 and Fundacio´n Jose´ Marı´a Mainetti, Centro Oncolo´gico,3 La Plata, Argentina Received 11 August 2000/Returned for modification 19 September 2000/Accepted 16 November 2000 We report the first case of maxillary sinusitis caused by Actinomucor elegans in an 11-year-old patient.
Histopathological and mycological examinations of surgical maxillary sinuses samples showed coenocytic
hyphae characteristic of mucoraceous fungi. The fungi recovered had stolons and rhizoids, nonapophyseal and
globose sporangia, and whorled branched sporangiophores and was identified as A. elegans. After surgical
cleaning and chemotherapy with amphotericin B administered intravenously and by irrigation, the patient
became asymptomatic and the mycological study results were negative.
An 11-year-old female patient, being neither diabetic nor paranasal sinuses were inoculated on Sabouraud glucose agar human immunodeficiency virus positive, without evident un- with 5% (vol/vol) blood and Sabouraud glucose-honey agar derlying disease, but with slight leukopenia, was brought to a supplemented with chloramphenicol and 0.5% (wt/vol) yeast specialist about left-eye epiphora. On physical examination, extract and incubated at 28 and 37°C.
the patient reported serosanguinous nasal discharge and de- In both samples, several cottony, white colonies were evident creased sinus ventilation lasting 2 months. A magnetic reso- after 48 h of incubation, and microscopic examination showed nance imaging (MRI) study revealed left pansinusitis, and non- that they consisted of coenocytic, branched hyphae of variable specific treatment was initiated. One month after the first widths (10 to 25 ␮m), characteristic of mucoraceous fungi.
clinical examination, the patient spontaneously expelled sero- After 7 days, the same colonies developed globose to subglo- mucous material during a cough. The presence of coenocytic bose sporangia. The colonies were more exuberant on Sab- hyphae in a direct examination of this sample, culturing of mucoraceous fungi, and opacification of the left maxillary sinus The fungus was sent to Departamento Mycologia, INEI, observed by MRI dictated the need for surgical cleaning of the ANLIS “Dr. Carlos G. Malbra´n,” Buenos Aires, Argentina, for paranasal sinuses. All the surgical specimens were sent to lab- identification. Subcultures on potato dextrose agar (PDA), Sa- oratories for mycological and histopathological studies. Direct bouraud glucose agar, 2% malt extract agar, Czapek’s solution microscopy of KOH preparations and tissue sections of the left agar (Cz), and oatmeal agar were incubated at 25 to 28°C in maxillary sinus showed broad hyphae, typically coenocytic, darkness. Subcultures were examined at 4, 7, and 14 days.
characteristic of mucoraceous fungi. No evidence of osseous Cultures on PDA yielded fast-growing, cottony, almost white tissue invasion or eosinophils was observed.
colonies. After 4 days, the colonies measured 75 mm in diam- The results of histopathological and mycological examina- eter and became olive-buff, with an abundant aerial mycelium tions of the surgical specimens from ethmoid, sphenoid, and over 1 cm in height and a colorless reverse. Under a dissecting frontal sinuses were negative for fungi.
microscope, the colonies showed whorled branched sporangio- The same fungus was isolated from the seromucous material phores, originating at a short distance below the terminal spo- and from the maxillary sinus. The fungus was isolated as a rangia and bearing secondary sporangia subtended by cross single microorganism from both samples.
walls (Fig. 1). The sporangiophores arose opposite from the In addition to the surgical cleaning, the patient was treated branched rhizoids. Branched stolons were also present. The with amphotericin B administered intravenously (1 mg/kg of microscopic examination showed that all of the sporangia were body weight/day) and by irrigation of the maxillary antrum (5 spherical, 16 to 72 ␮m in diameter, and slightly colored (cream to buff), had many spores, and were slightly spinous, with The patient was monitored bimonthly by MRI for 6 months elongate-oval (4 to 6 by 30 to 34 ␮m) columellae but without after surgery. Although persistence of the opacity in the left apophyses. The branched sporangiophores were slightly cream maxillary sinus was observed, monthly clinical studies to date to buff, septate, smooth walled, and 4 to 18 ␮m in diameter.
have shown an asymptomatic patient with negative mycological Stolons and rhizoids were septate, smooth walled, and color- Mycological findings. The spontaneously expelled seromu-
In old cultures, chlamydospores were present. The sporan- cous material and a portion of each tissue biopsy from the giospores were globose and smooth walled and showed high size variability in different culture media. We randomly mea- sured the diameters of 52 sporangiospores from a 14-day PDA * Corresponding author. Mailing address: Departamento Micologı´a, culture; the values ranged between 4 and 12 ␮m, the arithmetic Instituto Nacional de Enfermedades Infecciosas, ANLIS Dr. Carlos G.
mean and standard deviation was 7.33 Ϯ 0.16 ␮m, and the Malbra´n, Av. Velez Sarsfield 563 (1281), Buenos Aires, Argentina.
Phone: 54-11-4302-5066. Fax: 54-11-4302-5066. E-mail: gdavel@anlis Subcultures on the other culture media, incubated at 25 to FIG. 1. Slide cultures (4 days old) on PDA at 25 to 28°C in darkness. The specimen was stained with cotton blue. (A) Whorled branched sporangiophore, originating at a short distance below the terminal sporangium and bearing secondary sporangia subtended by cross walls.
Magnification, ϫ120. (B) Stolons and rhizoids, repeatedly branched. Magnification, ϫ60. Phase-contrast microscopy was used.
28°C in darkness, grew very fast and luxuriantly, as on PDA, any evident underlying disease. Most of the cases are caused by except that Cz that did not support good growth. On PDA, the species of Rhizopus, Absidia, Rhizomucor, and Mucor. Infec- fungus grew at 37°C but not at 40°C. Based on these morpho- tions due to other genera of the Mucoraceae are less frequent logical characteristics, we identified the isolate as Actinomucor (3, 5). We report the first case of maxillary sinusitis due to elegans (1, 2). This identification was confirmed by E. Piontelli, A. elegans in a young female patient without evident underly- Facultad de Medicina, Universidad de Valparaiso, Valparaiso, ing disease but with slight leukopenia. To our knowledge, this Chile, and J. D. David, CABI Bioscience, Egham, United fungus has never been isolated from a human source.
Kingdom. This isolate has been preserved in IMI and Univer- Actinomucor, one of several genera of the family Muco- sidad de Valparaiso herbaria under the designations IMI383277 raceae, was originally described by Schostakowish in 1898 (1). This genus differs from the other mucoraceous fungal The in vitro susceptibility of the isolate to amphotericin B genera, except for Rhizomucor, Rhizopus, and Absidia, in hav- and fluconazole was evaluated by use of the National Commit- ing branched stolons that give rise to rhizoids and sporangio- tee for Clinical Laboratory Standards reference method for phores. Actinomucor is further separated from Rhizopus and antifungal susceptibility testing of conidium-forming filamen- Absidia, two other stoloniferous genera, because of differences tous fungi (4). The MICs obtained were 2 ␮g/ml for ampho- in the formation of collumellae and sporangiophores and the tericin B and 1 ␮g/ml for itraconazole.
limited growth of the stolons. Although Actinomucor resem- Mucoraceous fungi are the most common group of fungi of bles Rhizomucor, it differs from that genus by having hyaline to the Zygomycetes and are an ever-expanding group of organisms faintly colored sporangia and by temperature requirements for capable of causing human diseases. The main categories of growth. At present, the genus Actinomucor includes two spe- infections caused by mucoraceous fungi are sinusitis and rhi- cies: A. taiwanensis, which is used in the manufacture of sufu, nocerebral, pulmonary, cutaneous or subcutaneous, gastroin- a traditional oriental food made from soybean milk, and A. testinal, and disseminated zygomycoses (3, 5).
elegans, the type species of the genus Actinomucor, which is The incidence of fungal sinusitis, particularly in immuno- found in soil and other natural substrata from different coun- competent patients, appears to be increasing. Paranasal sinus tries but which has never been isolated from a human source mucormycosis usually has been reported for patients with di- abetes mellitus but also has been detected in patients without These two species are very similar, but the major difference between them is the sporangiospore size; A. elegans has smaller Fungal sinusitis has been broadly divided into four catego- sporangiospores (6 to 8 ␮m) than A. taiwanensis (7 to 15 ␮m, ries: the acute fulminant form, the indolent form, the myce- even up to 20 ␮m). Although our isolate had some spores toma form, and the allergic form (3). In this case, as the patient larger than those described for A. elegans, the mean and the was immunocompetent, with chronic noninvasive colonization mode for the spore sizes are included in the spore size range of of a maxillary sinus by a fungus and without an eosinophilic this species. Jong and Yuan (2) described other different char- reaction, this clinical presentation was diagnosed as the indo- acteristics, such as maximum growth temperatures and the ability to grow on Cz. According to these authors, A. elegans Within the expanding group of susceptible hosts, new fungal shows better growth on Cz than does A. taiwanensis; on the opportunists are increasing in number; therefore, diagnosis other hand, the maximum growth temperature for A. taiwan- and management of the infections that they cause can be dif- ensis is 37°C, while A. elegans does not grow at this tempera- ficult and will require a greater understanding of mycological ture. Under these criteria, our isolate may be identified as A. details. As an aid to the laboratory identification of this fungus, taiwanensis because it grows at 37°C and develops less on Cz the most relevant characteristics are as follows. The genus than on PDA. However, Benjamin and Hesseltine (1), who Actinomucor resembles Rhizomucor in having rhizoids, stolons, have studied a larger number of strains, observed that several and spherical sporangia with columellae but without apophy- isolates of A. elegans showed smaller amounts of growth on Cz ses. Actinomucor has projections of whorls of short branches than on PDA and that the maximum temperature of growth below the terminal sporangia of the sporangiophores, which was approximately 32°C; however, their results were not con- are absent in Rhizomucor; a lighter pigmentation of sporangio- clusive. It is evident that more strains are needed to evaluate spores; and a lack of growth at 40°C.
these characteristics in order to compare these two species.
Based on spore size, which seems to be a major taxonomic criterion, our isolate was identified as A. elegans. We consid- We thank E. Piontelli and J. D. David for the confirmation of fungal ered that this isolate, with intermediate characteristics, could identification and M. Soria for helpful comments.
be a more mesophilic ecotype of A. elegans with some patho- genic properties. Molecular data are required to determine if REFERENCES
these two species represent distinct taxons or could be recog- 1. Benjamin, C. R., and C. W. Hesseltine. 1957. The genus Actinomucor. Myco-
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