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Journal of Clinical Microbiology, May 1999, p. 1606-1609, Vol. 37, No. 5
0095-1137/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Invasive Aspergillosis Caused by Aspergillus
ustus: Case Report and Review
Paul E.
Verweij,1,*
Marjolein F. Q.
van den Bergh,1
Peter M.
Rath,2
Ben E.
de
Pauw,3
Andreas
Voss,1 and
Jacques F. G. M.
Meis1
Departments of Medical
Microbiology1 and
Hematology,3 University Hospital
Nijmegen, Nijmegen, The Netherlands, and Institut für
Medizinische Mikrobiologie, Universität-GH Essen, Essen,
Germany2
Received 21 September 1998/Returned for modification 21 October
1998/Accepted 26 January 1999
 |
ABSTRACT |
A case of invasive pulmonary aspergillosis in an allogeneic bone
marrow transplant recipient caused by Aspergillus ustus is presented. A. ustus was also recovered from the hospital
environment, which may indicate that the infection was nosocomially
acquired. A literature review revealed seven cases of invasive
infections caused by A. ustus, and three of these were
primarily cutaneous infections. In vitro susceptibility testing of 12 A. ustus isolates showed that amphotericin B and
terbinafine had fungicidal activity and that itraconazole and
voriconazole had fungistatic activity.
| |
TEXT |
Invasive pulmonary aspergillosis is
an important cause of morbidity and mortality in immunocompromised
patients, especially those who receive hematopoetic stem cell
transplants (25). Besides Aspergillus fumigatus,
at least 20 species of Aspergillus have been reported to
cause invasive infections, including A. terreus (8), A. nidulans (21), and A. niger (10). Here we report on a case of invasive
pulmonary infection caused by A. ustus in a patient with
chronic myeloid leukemia during treatment for graft-versus-host disease
following allogeneic bone marrow transplantation (BMT). Furthermore, we
report on a review of the literature for descriptions of cases of
invasive aspergillosis caused by A. ustus and the in vitro
activities of antifungal agents against A. ustus isolates.
Case report.
A 38-year-old male received T-cell-depleted bone
marrow from a matched unrelated donor as therapy for chronic myeloid
leukemia which had been diagnosed 5 years previously. The conditioning regimen consisted of cyclophosphamide and total-body irradiation, and
he received cyclosporine A for immunoprophylaxis. Antifungal prophylaxis included amphotericin B suspension and aerosol spray. Two
days after BMT the patient developed a high fever, and treatment with
ceftazidime was begun. A chest X ray showed no infiltrates, and blood
cultures remained sterile. Acute graft-versus-host disease of the skin,
liver, and intestine (grade IV) became apparent, but this responded to
methylprednisolone sodium succinate (Solu-Medrol) at 1 g/day, and the
dose was gradually reduced. Marrow engraftment was rapid, and the
neutrophil count exceeded 1.0 × 109/liter on day 15. A second febrile episode developed 17 days after BMT, but pulmonary
infiltrates were not evident on a chest X ray. Acute graft-versus-host
disease relapsed on day 23 and the dosage of methylprednisolone was
increased. The patient had seizures, but computed tomography of the
brain showed no abnormalities. The patient was seropositive for
toxoplasma, and magnetic resonance imaging of the brain on day 33 showed multiple hyperdense lesions. These lesions were suspected to
result from toxoplasmosis or cerebral aspergillosis. At that time a
pulmonary infiltrate had developed in the right upper lobe of the lung.
A mucus plug was obtained during bronchoscopy on day 35, and culture
yielded non-A. fumigatus Aspergillus species. Treatment with
amphotericin B at a dosage of 1 mg/kg of body weight/day was begun, but
the clinical condition of the patient deteriorated. The patient died 51 days after BMT from massive bleeding from the gastrointestinal tract.
At autopsy, a large infiltrate was found in the upper lobe of the right
lung. Mycelia with dichotomous branching were seen in the tissues of
the right lung, and an olive-gray filamentous fungus was recovered by
culture on Sabouraud agar containing 10% chloramphenicol after 2 days
of incubation. The reverse showed the production of a yellow diffusing
pigment. Microscopic examination revealed biseriate conidiogenous cells
bearing very rough walled dark-yellow to brown conidia (Fig.
1). Irregular to elongate Hülle cells are characteristic for this fungus but are formed only by a
minority of isolates. The isolate was identified as A. ustus by the Centraalbureau voor Schimmelcultures (CBS; Baarn, The
Netherlands). There was no evidence of the dissemination of the
Aspergillus infection. Microscopic examination of the brain
showed several hypoxia-induced lesions but no evidence of toxoplasmosis
or cerebral aspergillosis.
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FIG. 1.
Brown and smooth-walled conidiophore of A. ustus. The vesicle bears a double series of sterigmata. The
conidia are rough and greenish brown to dark yellow-brown.
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|
Air sampling with a Casella sampler is performed systematically in
selected areas of our hospital with high-risk patients.
The patient
rooms and corridors in the hematology ward are sampled
every month. All
Aspergillus isolates recovered from the environment
are
identified to the species level and stored. The database was
searched
for
Aspergillus species which had been cultured from
patients and the hospital environment between January 1991 and
August
1998.
Antigen detection.
The presence of the Aspergillus
antigen galactomannan was determined in the serum by the latex
agglutination (LA) test (Pastorex Aspergillus) (24) and by a
sandwich enzyme-linked immunosorbent assay (ELISA; Platelia
Aspergillus; Sanofi Diagnostics Pasteur, Marnes-La-Coquette, France)
(19). Both kits use the same monoclonal antibody (monoclonal
antibody EB-A2) and are available commercially outside the United
States. The LA test and ELISA were performed according to the
manufacturers' instructions. A titer was obtained for the LA test by
testing serially diluted serum samples. For the ELISA, a ratio was
calculated by dividing the optical density of the serum sample by that
of a threshold control sample which contained 1 ng of galactomannan per
ml. Galactomannan was detected by the LA test in 3 of 18 serum samples,
while the sandwich ELISA was positive for 13 samples (Fig.
2). The first serum sample with ELISA
reactivity was obtained 1 week after BMT (day 7) and 28 days before
A. ustus was cultured from a mucus plug and treatment with
amphotericin B was begun. The course of the antigen titer is shown in
Fig. 2.
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FIG. 2.
Results of antigen detection by sandwich ELISA and LA
test with serum from the patient infected with A. ustus.
 , ratio for galactomannan in serum;  , leukocyte count
(109/liter); ---, cutoff for a positive
ELISA result. The LA test result is given at the bottom. The different
treatments are indicated at the top.
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In vitro susceptibility testing.
The in vitro activities of
amphotericin B (Bristol Myers-Squibb, Woerden, The Netherlands),
itraconazole (Janssen-Cilag B.V., Tilburg, The Netherlands),
voriconazole (Pfizer Central Research, Sandwich, United Kingdom), and
terbinafine (Novartis, Basel, Switzerland) were determined by a broth
microdilution method according to the standardized procedure for
antifungal susceptibility testing proposed by the National Committee
for Clinical Laboratory Standards (NCCLS) Subcommittee on Antifungal
Susceptibility Testing (12). That procedure was modified for
the testing of filamentous fungi. An itraconazole-susceptible A. fumigatus control isolate (isolate AF71), an
itraconazole-resistant A. fumigatus control isolate (isolate
AF90), and Paecilomyces variotii ATCC 22319 were included in
each test. For amphotericin B and terbinafine, the MIC endpoint was
defined as complete inhibition of visible growth, and for the azoles,
75% growth inhibition compared with the growth of the controls. Wells
without visible growth were subcultured onto Sabouraud glucose agar and
were incubated at 35°C for 48 h. Subcultures from the wells with
the lowest drug concentrations showing a 99.9% reduction from the
initial inoculum size were judged to contain the minimal fungicidal
concentration (MFC). Both terbinafine and amphotericin B showed
fungicidal activity against A. ustus, but the MICs and MFCs
of terbinafine were approximately threefold lower than those of
amphotericin B (Table 1). The azoles itraconazole and voriconazole were
less active in vitro, and for most isolates fungicidal activity was not
achieved at concentrations of 
32 µg/ml.
Literature review.
The literature for the years 1960 to 1998 was reviewed with the use of MEDLINE for case reports of invasive
infections caused by A. ustus. Seven cases of invasive
A. ustus infections have been described (Table
2).
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TABLE 1.
Characteristics of 12 A. ustus isolates and in
vitro susceptibility to amphotericin B, itraconazole, voriconazole,
and terbinafine
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|
Invasive infections caused by
A. ustus are uncommon, and
including the present case, only eight cases have been documented
in
the literature since 1960. Information from the reported cases
show
that
A. ustus may cause a variable spectrum of disease.
Among
the case patients, three patients were described as having
primarily
cutaneous infections. In patient 4 (Table
2) cutaneous
lesions
developed on an arm and leg which had been stabilized. Both
devices
had occluded the skin and had caused local irritation
(
18).
In patient 6 the infection started as erosion of the
skin from
a plastic identification bracelet (
15). Cutaneous
infections
caused by opportunistic fungi related to occlusion of the
skin
have been described previously (
11). Occlusion of the
skin creates
a warm and humid environment that allows fungal spores,
which
may be present in nonsterile material or the environment, to
germinate
and invade the skin, especially when it is disrupted. The
third
case of cutaneous infection occurred in a patient (patient 2)
with excessive burns to the skin (
16). Although the skin was
not occluded, application of a prednisone-containing emulsion
and the
presence of excessive burns could have predisposed the
patient to
infection. These cases suggest that
A. ustus infection
may
be of nosocomial origin. We succeeded in culturing
A. ustus from the hospital environment, but over an 8-year period of systematic
sampling,
A. ustus was recovered only three times in the
hematology
ward. The mold was cultured on two different occasions
shortly
after the case patient died (Table
1). Very little is known about
the
diversity of
Aspergillus species within the hospital
environment
since most studies fail to identify
Aspergillus
species other
than
A. fumigatus and
A. flavus
(
7). However in one hospital,
A. ustus
represented 5% of all
Aspergillus isolates cultured from
the air (
13).
A commercial sandwich ELISA which detects
Aspergillus
galactomannan has been evaluated in several institutes outside the
United
States (
1,
23). This assay allows the detection of
low levels
of galactomannan in body fluids and has a higher sensitivity
than
the LA test (
1,
23). Galactomannan is produced by
Aspergillus species involved in human disease
(
20) and was detected in the
serum of patients infected with
A. fumigatus (
23),
A. flavus (
1),
A. niger (
1), and
A. nidulans (
21) and one patient
infected with
A. ustus (
1). The finding of galactomannan in
serum
samples from our patient confirms the reactivity of the
assay for
patients infected with
A. ustus. Twice-weekly collection
of
serum samples allowed the detection of galactomannan at an
early stage
of infection. The antigen titer increased continuously,
despite
treatment with amphotericin B, and the titer increase
corresponded to
the clinical failure of
therapy.
For the treatment of invasive aspergillosis, voriconazole is a
promising antifungal azole that is fungicidal against
A. fumigatus (
6). Patients with invasive aspergillosis,
including those
infected with non-
A. fumigatus Aspergillus
isolates (
21), have
been reported to show a favorable
response to treatment with voriconazole
(
3,
5). Voriconazole
has been shown to be active in vitro
against several non-
A.
fumigatus Aspergillus species including
A. flavus,
A. nidulans,
A. versicolor, and
A. niger (
14). Our
results suggest that the drug is less
active in vitro against
A. ustus than it is against
A. fumigatus. The effect appears to
be fungistatic and similar to
that of itraconazole. Terbinafine
is active in vitro against several
Aspergillus species (
17),
and the drug is under
evaluation for the treatment of invasive
aspergillosis. Among the drugs
tested, terbinafine proved to be
the most active in vitro and was also
the most fungicidal. These
results and previous in vitro susceptibility
data (
17) indicate
that terbinafine may be a promising agent
for the treatment of
invasive aspergillosis, including those infections
caused by non-
A. fumigatus Aspergillus species. The results
of in vitro susceptibility
testing add to the evidence that different
Aspergillus species
have variable susceptibilities to
antifungal agents (
4,
22),
which underscores the importance
of susceptibility testing of
clinically significant
isolates.
| |
ACKNOWLEDGMENTS |
We thank Stephane Bretagne, Laboratoire de Parasitologie-Mycologie,
Hôpital Henri Mondor, Créteil, France, for providing clinical data and A. ustus A252 and Ton Rijs for excellent
technical assistance.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Medical Microbiology, University Hospital Nijmegen, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands. Phone: 31-24-3614356. Fax: 31-24-3540216. E-mail: p.verweij{at}mmb.azn.nl.
| |
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Journal of Clinical Microbiology, May 1999, p. 1606-1609, Vol. 37, No. 5
0095-1137/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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Espinel-Ingroff, A., Bartlett, M., Chaturvedi, V., Ghannoum, M., Hazen, K. C., Pfaller, M. A., Rinaldi, M., Walsh, T. J.
(2001). Optimal Susceptibility Testing Conditions for Detection of Azole Resistance in Aspergillus spp.: NCCLS Collaborative Evaluation. Antimicrob. Agents Chemother.
45: 1828-1835
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Moore, C. B., Walls, C. M., Denning, D. W.
(2001). In Vitro Activities of Terbinafine against Aspergillus Species in Comparison with Those of Itraconazole and Amphotericin B. Antimicrob. Agents Chemother.
45: 1882-1885
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Espinel-Ingroff, A.
(2001). Comparison of the E-test with the NCCLS M38-P Method for Antifungal Susceptibility Testing of Common and Emerging Pathogenic Filamentous Fungi. J. Clin. Microbiol.
39: 1360-1367
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Espinel-Ingroff, A.
(2001). In Vitro Fungicidal Activities of Voriconazole, Itraconazole, and Amphotericin B against Opportunistic Moniliaceous and Dematiaceous Fungi. J. Clin. Microbiol.
39: 954-958
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Gené, J., Azón-Masoliver, A., Guarro, J., De Febrer, G., Martínez, A., Grau, C., Ortoneda, M., Ballester, F.
(2001). Cutaneous Infection Caused by Aspergillus ustus, an Emerging Opportunistic Fungus in Immunosuppressed Patients. J. Clin. Microbiol.
39: 1134-1136
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Espinel-Ingroff, A.
(2001). Germinated and Nongerminated Conidial Suspensions for Testing of Susceptibilities of Aspergillus spp. to Amphotericin B, Itraconazole, Posaconazole, Ravuconazole, and Voriconazole. Antimicrob. Agents Chemother.
45: 605-607
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