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Journal of Clinical Microbiology, February 2001, p. 740-742, Vol. 39, No. 2
0095-1137/01/$04.00+0 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
Fernández,2
Ruben
Abrantes,1
Cristina
Canteros,1
Laura
Rodero,1
Carlos
Sztern,3 and
Diego
Perrotta1
Departamento Micología, INEI, ANLIS
Dr. Carlos G. Malbrán, Buenos Aires,1 and
Hospital San Juan de Dios2 and
Fundación José María Mainetti, Centro
Oncológico,3 La Plata, Argentina
Received 11 August 2000/Returned for modification 19 September
2000/Accepted 16 November 2000
 |
ABSTRACT |
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.
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TEXT |
An 11-year-old female patient, being
neither diabetic nor human immunodeficiency virus positive, without
evident underlying disease, but with slight leukopenia, was brought to
a specialist about left-eye epiphora. On physical examination, the
patient reported serosanguinous nasal discharge and decreased sinus
ventilation lasting 2 months. A magnetic resonance imaging (MRI) study
revealed left pansinusitis, and nonspecific treatment was initiated.
One month after the first clinical examination, the patient
spontaneously expelled seromucous material during a cough. The presence
of coenocytic hyphae in a direct examination of this sample, culturing
of mucoraceous fungi, and opacification of the left maxillary sinus
observed by MRI dictated the need for surgical cleaning of the
paranasal sinuses. All the surgical specimens were sent to laboratories for mycological and histopathological studies. Direct microscopy of KOH
preparations and tissue sections of the left maxillary sinus showed
broad hyphae, typically coenocytic, characteristic of mucoraceous
fungi. No evidence of osseous tissue invasion or eosinophils was observed.
The results of histopathological and mycological examinations of the
surgical specimens from ethmoid, sphenoid, and frontal sinuses were
negative for fungi.
The same fungus was isolated from the seromucous material and from the
maxillary sinus. The fungus was isolated as a single microorganism from
both samples.
In addition to the surgical cleaning, the patient was treated with
amphotericin B administered intravenously (1 mg/kg of body weight/day)
and by irrigation of the maxillary antrum (5 mg/day), both for 42 days.
The patient was monitored bimonthly by MRI for 6 months after surgery.
Although persistence of the opacity in the left maxillary sinus was
observed, monthly clinical studies to date have shown an asymptomatic
patient with negative mycological study results.
Mycological findings.
The spontaneously expelled seromucous
material and a portion of each tissue biopsy from the paranasal sinuses
were inoculated on Sabouraud glucose agar with 5% (vol/vol) blood and
Sabouraud glucose-honey agar supplemented with chloramphenicol and
0.5% (wt/vol) yeast extract and incubated at 28 and 37°C.
In both samples, several cottony, white colonies were evident after
48 h of incubation, and microscopic examination showed that they
consisted of coenocytic, branched hyphae of variable widths (10 to 25 µm), characteristic of mucoraceous fungi. After 7 days, the same
colonies developed globose to subglobose sporangia. The colonies were
more exuberant on Sabouraud glucose agar with 5% blood.
The fungus was sent to Departamento Mycologia, INEI, ANLIS "Dr.
Carlos G. Malbrán," Buenos Aires, Argentina, for
identification.
Subcultures on potato dextrose agar (PDA), Sabouraud
glucose agar,
2% malt extract agar, Czapek's solution agar (Cz), and
oatmeal
agar were incubated at 25 to 28°C in darkness. Subcultures
were
examined at 4, 7, and 14
days.
Cultures on PDA yielded fast-growing, cottony, almost white colonies.
After 4 days, the colonies measured 75 mm in diameter
and became
olive-buff, with an abundant aerial mycelium over 1
cm in height and a
colorless reverse. Under a dissecting microscope,
the colonies showed
whorled branched sporangiophores, originating
at a short distance below
the terminal sporangia and bearing secondary
sporangia subtended by
cross walls (Fig.
1). The sporangiophores
arose opposite from the branched rhizoids. Branched stolons were
also
present. The microscopic examination showed that all of the
sporangia
were spherical, 16 to 72 µm in diameter, and slightly
colored (cream
to buff), had many spores, and were slightly spinous,
with
elongate-oval (4 to 6 by 30 to 34 µm) columellae but without
apophyses. The branched sporangiophores were slightly cream to
buff,
septate, smooth walled, and 4 to 18 µm in diameter. Stolons
and
rhizoids were septate, smooth walled, and colorless.
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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, ×120. (B) Stolons and rhizoids, repeatedly
branched. Magnification, ×60. Phase-contrast microscopy was used.
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In old cultures, chlamydospores were present. The sporangiospores were
globose and smooth walled and showed high size variability
in different
culture media. We randomly measured the diameters
of 52 sporangiospores
from a 14-day PDA culture; the values ranged
between 4 and 12 µm, the
arithmetic mean and standard deviation
was 7.33 ± 0.16 µm, and
the mode was 7.6 µm.
Subcultures on the other culture media, incubated at 25 to 28°C in
darkness, grew very fast and luxuriantly, as on PDA, except
that Cz
that did not support good growth. On PDA, the fungus grew
at 37°C but
not at 40°C. Based on these morphological characteristics,
we
identified the isolate as
Actinomucor elegans (
1,
2).
This identification was confirmed by E. Piontelli, Facultad
de
Medicina, Universidad de Valparaiso, Valparaiso, Chile, and J.
D. David, CABI Bioscience, Egham, United Kingdom. This isolate
has been
preserved in IMI and Universidad de Valparaiso herbaria
under the
designations IMI383277 and CMUV.171,
respectively.
The in vitro susceptibility of the isolate to amphotericin B and
fluconazole was evaluated by use of the National Committee
for Clinical
Laboratory Standards reference method for antifungal
susceptibility
testing of conidium-forming filamentous fungi (
4).
The
MICs obtained were 2 µg/ml for amphotericin B and 1 µg/ml
for
itraconazole.
Mucoraceous fungi are the most common group of fungi of the
Zygomycetes and are an ever-expanding group of organisms
capable
of causing human diseases. The main categories of infections
caused
by mucoraceous fungi are sinusitis and rhinocerebral, pulmonary,
cutaneous or subcutaneous, gastrointestinal, and disseminated
zygomycoses (
3,
5).
The incidence of fungal sinusitis, particularly in immunocompetent
patients, appears to be increasing. Paranasal sinus mucormycosis
usually has been reported for patients with diabetes mellitus
but also
has been detected in patients without any evident underlying
disease.
Most of the cases are caused by species of
Rhizopus,
Absidia,
Rhizomucor, and
Mucor.
Infections due to other genera
of the
Mucoraceae are less
frequent (
3,
5). We report the
first case of
maxillary sinusitis due to
A. elegans in a young
female
patient without evident underlying disease but with slight
leukopenia. To our knowledge, this fungus has never been isolated
from
a human
source.
Actinomucor, one of several genera of the family
Mucoraceae, was originally described by
Schostakowish in 1898 (
1). This
genus differs from the
other mucoraceous fungal genera, except
for
Rhizomucor,
Rhizopus, and
Absidia, in
having branched stolons
that give rise to rhizoids and sporangiophores.
Actinomucor is
further separated from
Rhizopus
and
Absidia, two other stoloniferous
genera, because of
differences in the formation of collumellae
and sporangiophores and the
limited growth of the stolons. Although
Actinomucor
resembles
Rhizomucor, it differs from that genus by
having
hyaline to faintly colored sporangia and by temperature
requirements
for growth. At present, the genus
Actinomucor includes
two
species:
A. taiwanensis, which is used in the manufacture
of
sufu, a traditional oriental food made from soybean milk, and
A. elegans, the type species of the genus
Actinomucor,
which is
found in soil and other natural substrata from different
countries
but which has never been isolated from a human source
(
1,
2).
These two species are very similar, but the major difference between
them is the sporangiospore size;
A. elegans has smaller
sporangiospores (6 to 8 µm) than
A. taiwanensis (7 to 15 µm, even
up to 20 µm). Although our isolate had some spores larger
than
those described for
A. elegans, the mean and the mode
for the
spore sizes are included in the spore size range of this
species.
Jong and Yuan (
2) described other different
characteristics,
such as maximum growth temperatures and the ability to
grow on
Cz. According to these authors,
A. elegans shows
better growth
on Cz than does
A. taiwanensis; on the other
hand, the maximum
growth temperature for
A. taiwanensis is
37°C, while
A. elegans does not grow at this temperature.
Under these criteria, our isolate
may be identified as
A. taiwanensis because it grows at 37°C and
develops less on Cz
than on PDA. However, Benjamin and Hesseltine
(
1), who
have studied a larger number of strains, observed
that several isolates
of
A. elegans showed smaller amounts of
growth on Cz than on
PDA and that the maximum temperature of growth
was approximately
32°C; however, their results were not conclusive.
It is evident that
more strains are needed to evaluate 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 considered that this isolate, with intermediate
characteristics, could be a more mesophilic ecotype of
A. elegans with some pathogenic properties. Molecular data are
required to
determine if these two species represent distinct taxons or
could
be recognized at an appropriate infraspecific
rank.
Standardization of in vitro susceptibility testing for filamentous
fungi has recently been proposed by the National Committee
for Clinical
Laboratory Standards (
4); therefore, data about
the
susceptibility or resistance of mucoraceous fungi are still
lacking. In
this case, as this was the first clinical isolation
of the fungus, it
was important to determine the MICs of current
antifungal drugs.
Although we cannot determine the meaning of
the amphotericin B and
itraconazole MICs found for our isolate,
future clinical isolations may
yield more useful
results.
Fungal sinusitis has been broadly divided into four categories: the
acute fulminant form, the indolent form, the mycetoma
form, and the
allergic form (
3). In this case, as the patient
was
immunocompetent, with chronic noninvasive colonization of
a maxillary
sinus by a fungus and without an eosinophilic reaction,
this clinical
presentation was diagnosed as the indolent
form.
Within the expanding group of susceptible hosts, new fungal
opportunists are increasing in number; therefore, diagnosis and
management of the infections that they cause can be difficult
and will
require a greater understanding of mycological details.
As an aid to
the laboratory identification of this fungus, the
most relevant
characteristics are as follows. The genus
Actinomucor resembles
Rhizomucor in having rhizoids, stolons, and
spherical
sporangia with columellae but without apophyses.
Actinomucor has
projections of whorls of short branches
below the terminal sporangia
of the sporangiophores, which are absent
in
Rhizomucor; a lighter
pigmentation of sporangiospores;
and a lack of growth at 40°C.
| |
ACKNOWLEDGMENTS |
We thank E. Piontelli and J. D. David for the confirmation of
fungal identification and M. Soria for helpful comments.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Departamento
Micología, Instituto Nacional de Enfermedades Infecciosas,
ANLIS Dr. Carlos G. Malbrán, Av. Velez Sarsfield 563 (1281),
Buenos Aires, Argentina. Phone: 54-11-4302-5066. Fax: 54-11-4302-5066. E-mail: gdavel{at}anlis.gov.ar.
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Benjamin, C. R., and C. W. Hesseltine.
1957.
The genus Actinomucor.
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| 2.
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Jong, S. C., and G. F. Yuan.
1985.
Actinomucor taiwanensis sp. nov., for manufacture of fermented soybean food.
Mycotaxon
23:261-264.
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Lawson, W., and A. Blitzer.
1993.
Fungal infections of the nose and paranasal sinuses. Part I, p. 1007-1035.
In
W. Lawson, and A. Blitzer (ed.), The otolaryngologic clinics of North America 1993. W. B. Saunders Co., Philadelphia, Pa.
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National Committee for Clinical Laboratory Standards.
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Reference method for broth dilution antifungal susceptibility testing of conidium-forming filamentous fungi. Proposed standard. Document M38-P.
National Committee for Clinical Laboratory Standards, Wayne, Pa.
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C. L. Vanover-Sams, and D. J. Baker.
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Zygomycetes in human disease.
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13:236-301[Abstract/Free Full Text].
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Journal of Clinical Microbiology, February 2001, p. 740-742, Vol. 39, No. 2
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.2.740-742.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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