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Journal of Clinical Microbiology, April 1999, p. 1154-1160, Vol. 37, No. 4
0095-1137/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Fatal Disseminated Trichoderma
longibrachiatum Infection in an Adult Bone Marrow Transplant
Patient: Species Identification and Review of the Literature
S.
Richter,1
M. G.
Cormican,1
M. A.
Pfaller,1,*
C. K.
Lee,2
R.
Gingrich,2
M. G.
Rinaldi,3,4 and
D. A.
Sutton3
Departments of
Pathology1 and
Medicine,2 University of Iowa College of
Medicine, Iowa City, Iowa 52242, and Fungus Testing Laboratory,
Department of Pathology, University of Texas Health Science Center at
San Antonio,3 and Audie L. Murphy
Division, South Texas Veterans Health Care
System,4 San Antonio, Texas 78284
Received 5 October 1998/Returned for modification 7 November
1998/Accepted 25 November 1998
 |
ABSTRACT |
Trichoderma longibrachiatum was recovered from stool
surveillance cultures and a perirectal ulcer biopsy specimen from a
29-year-old male who had received an allogeneic bone marrow transplant
for acute lymphoblastic leukemia. The amphotericin B (2.0 µg/ml) and itraconazole (1.0 µg/ml) MICs for the organism were elevated. Therapy
with these agents was unsuccessful, and the patient died on day 58 posttransplantation. At autopsy, histologic sections from the lungs,
liver, brain, and intestinal wall showed infiltration by branching
septate hyphae. Cultures were positive for Trichoderma longibrachiatum. While Trichoderma species have been
recognized to be pathogenic in profoundly immunosuppressed hosts with
increasing frequency, this is the first report of probable acquisition
through the gastrointestinal tract. Salient features regarding the
identification of molds in the Trichoderma longibrachiatum
species aggregate are presented.
| |
TEXT |
The significant rise in profoundly
immunocompromised patients in recent years has resulted in a
concomitant escalation in opportunistic fungal infections (1, 6,
10, 22, 27, 30). In addition to the increased frequency of
infection, the variety of species implicated has also broadened such
that it is now apparent that the concept of nonpathogenic fungi has
little meaning in the setting of the immunocompromised host. This
report of a case of a fatal, disseminated Trichoderma
longibrachiatum infection in an adult bone marrow transplant
recipient is the fifth report documenting this species of
Trichoderma as an etiologic agent of infection in an
immunocompromised host and the first to suggest the gastrointestinal
tract as a portal of entry. Given its potential pathogenicity and
predilection for dissemination in profoundly neutropenic hosts,
cultural characteristics useful for the presumptive identification in
routine mycology laboratories of molds in the T. longibrachiatum species aggregate, and specifically T. longibrachiatum, will be addressed.
Case report.
A 29-year-old white male was diagnosed with acute
lymphoblastic leukemia (ALL; L1 subtype, T-cell immunotype) in June
1993. He received treatment according to the Cancer and Leukemia Group B 9111 protocol for induction and maintenance. A bone marrow
examination 28 days after induction showed remission. Five months after
initial presentation, he had one central nervous system (CNS) relapse requiring intrathecal chemotherapy and whole-brain irradiation. One
week prior to a planned admission for bone marrow transplantation, he
experienced a second CNS relapse. A short course of irradiation and
intrathecal chemotherapy resulted in a high level of partial remission.
The patient was admitted to the University of Iowa Hospitals and
Clinics in May 1994 for a bone marrow transplant and was conditioned
with total body irradiation, high-dose etoposide, and intrathecal
1-
-D-arabinofuranosylcytosine. At admission, he was
placed on oral clotrimazole, oral nystatin,
trimethoprim-sulfamethoxazole, amphotericin B nasal spray, and
intravenous fluconazole (200 mg once a day [q.d.]) for antimicrobial
prophylaxis. Ceftazidime and vancomycin were added 1 week later when
the patient's neutrophil count declined to 300/mm3. Ten
days after admission, an unrelated allogeneic bone marrow transplant
was performed. Acyclovir and metronidazole had been added to the
antimicrobial regimen by day 3 posttransplantation. The patient's
initial course posttransplantation was uneventful except for the
development of severe oral mucositis.
Stool surveillance studies were negative for fungi until days 8 and 10 posttransplantation, when a mold consistent with a Trichoderma species was identified. In response to the
positive stool cultures and a small right upper lobe lung opacity
identified on a chest computed tomography scan, amphotericin B (49 mg
q.d.) was started on day 13. On day 15, methyl prednisolone sodium
(Solu-Medrol; 70 mg every 12 h) was initiated for stage II skin
graft-versus-host disease (GVHD). The amphotericin B was increased to
83 mg q.d. on day 18 due to slight enlargement of the nodular pulmonary
infiltrate. On day 26, amphotericin B was discontinued because of
deteriorating renal function, and itraconazole (600-mg loading dose,
maintenance dosage of 400 mg q.d.) was introduced. A
Trichoderma species was again isolated from a stool
surveillance culture on day 27. The patient developed diarrhea, and a
perianal ulcer was noted. A stool culture was positive for
Clostridium difficile, and therapy with oral vancomycin was
started on day 31. Itraconazole was discontinued because of the
patient's inability to take the oral medication, and amphotericin B
(65 mg q.d.) was restarted on day 33.
By day 34, the leukocyte count had not recovered and it became apparent
that the engraftment had failed. Plans were made for
a second
transplant. The perianal ulcer was enlarging, and a punch
biopsy on day
35 showed a necrotic lesion infiltrated with branching
septate hyphae
(Fig.
1). A culture was positive for
Trichoderma species. Daily granulocyte infusions were
initiated, and the amphotericin
B was increased to 100 mg q.d. on day
37. Ablation therapy was
initiated on day 43. Due to declining renal
function, liposomal
amphotericin B (335 mg q.d.) was introduced on day
47. A second
unrelated allogeneic bone marrow transplant was performed
49 days
after the initial graft. The patient began to have spiking
temperatures
of up to 40°C 2 days later. The perianal ulcer continued
to enlarge,
and abdominal distention was noted. Progression of the
pulmonary
infiltrate was demonstrated radiographically, with multiple
nodules
involving both lungs. An abdominal film showed small-bowel
distention
with thickening of the intestinal wall. The patient's
condition
continued to deteriorate, and he died 9 days after the second
transplant.
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FIG. 1.
Methenamine silver stain of the perianal ulcer biopsy
specimen shows necrosis and infiltration by branching septate hyphal
forms. Magnification, ×100.
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An autopsy revealed a disseminated fungal infection. Multiple areas of
infarction with infiltration by branching septate hyphae
were
identified on Gomori methenamine silver-stained sections
of the liver
and both lungs. Sections of exophytic ulcerations
of the sigmoid colon
and the ileocecal valve showed transmural
necrosis with invasion by
septate branching fungal forms. The
heaped ileocecal valve lesion was
partially blocking the lumen
and probably caused the small-bowel
obstruction that had been
observed clinically. Focal cerebritis with
invasive septate hyphae
was identified in the right parietal cortex.
Postmortem cultures
of liver, lung, and sigmoid colon specimens were
positive for
a
Trichoderma species. Complications of sepsis
were identified
and included intravascular thrombi suggesting
disseminated intravascular
coagulopathy, massive pulmonary edema
consistent with extensive
capillary leakage, and acute tubular
necrosis. The possibility
of residual leukemia was suggested by a few
clusters of atypical
mononuclear cells in the
spleen.
Mycology.
All specimens for fungal culture were cultured on
Sabouraud dextrose agar (SDA; Becton Dickinson, Cockeysville, Md.) and
Mycosel agar (Baltimore Biological Laboratory, Cockeysville, Md.) at
30°C. Isolates were identified as Trichoderma species on
the basis of their macroscopic morphology (rapidly growing flat green
colonies) and microscopic characteristics (branching divergent tufts of conidiophores). Isolates were submitted to the Fungus Testing Laboratory, Department of Pathology, University of Texas Health Science
Center, San Antonio (accession no. 94-1620), for species identification.
There the isolate was subcultured onto potato flakes agar (PFA), which
was prepared in house, and SDA at 25, 35, and 42°C,
with good growth
occurring at all temperatures. Colonies were
initially smooth, somewhat
glabrous, translucent, and a watery
white but very rapidly became light
green to olivaceous green
and woolly with distinct tufts of
conidiophores in a zonal radial
pattern (Fig.
2a). A striking lemon yellow diffusible
pigment
was evident throughout the agar (Fig.
2b). Microscopically, the
hyphae were smooth, septate, and ramified (branched) and bore
conidiophores with long main branches (Fig.
3). The main branches
in turn produced
relatively few, short, often slightly curved
side branches at right
angles, each terminating in a phialide.
Phialides were bottle shaped,
mostly solitary, often somewhat
inflated in the middle and bent at the
apex, and slightly constricted
at the base and measured mostly 5 to 11 by 2 to 3 µm (Fig.
4 and
5). Terminal phialides were more
elongate, were not constricted
at the base, and were up to 14 µm long
(Fig.
5). Phialoconidia
were smooth walled, ellipsoidal to cylindrical,
and green and
measured 3.4 to 6.4 by 2.4 to 3.0 µm (Fig.
6). Occasional smooth,
thick-walled,
subglobose to ellipsoidal chlamydoconidia that measured
from 5 to 10 µm in diameter were also observed (Fig.
7). On the
basis of the characteristics
described above and our experience
with similar
Trichoderma
isolates, this organism was placed in
the section
Longibrachiatum (
2) and was tentatively
identified
as
T. longibrachiatum. Species confirmation was
provided by Gary
Samuels (Agricultural Research Service, U.S.
Department of Agriculture,
Beltsville, Md.) on the basis of analysis of
ribosomal DNA internal
transcribed spacer ITS-1 and ITS-2 sequences.
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FIG. 2.
(a) T. longibrachiatum on SDA (left) and PFA
(right), 5 days, 25°C. (b) Yellow diffusable pigment produced by
T. longibrachiatum on reverse of SDA, 5 days, 25°C.
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FIG. 3.
Long main branch of T. longibrachiatum
producing shorter side branches terminating in phialides.
Magnification, ×320.
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Antifungal susceptibility testing.
Broth microdilution testing
was performed in the Department of Pathology at the University of Iowa
Hospitals and Clinics according to National Committee for Clinical
Laboratory Standards (NCCLS) proposed standard guidelines as described
previously (21, 23). An inoculum concentration of 0.4 × 104 to 5 × 104 CFU/ml and RPMI 1640 medium buffered to pH 7.0 with 0.165 M morpholinepropanesulfonic acid
buffer (Sigma, St. Louis, Mo.) were used (21, 23).
Antifungal agents were obtained from their respective manufacturers and
included amphotericin B, flucytosine (5FC), fluconazole, and
itraconazole. Fungal inocula (100 µl) were added to each well of the
microdilution tray, and each well contained 100 µl of drug solution
(2× final concentration). The tray was incubated in air at 35°C and
was read after 48 h of incubation. The MIC endpoints were read
visually. For 5FC, fluconazole, and itraconazole the MIC endpoints were defined as the lowest concentration in which a prominent decrease in
turbidity (approximately 50% inhibition) was observed, and for
amphotericin B the MIC endpoint was defined as the lowest concentration
that produced complete inhibition of growth (21, 23).
Drug-free and fungus-free controls were included, and quality control
was ensured by testing Candida parapsilosis ATCC 22019, a
strain recommended for this purpose (21, 24).
The MICs of amphotericin B (2.0 µg/ml), itraconazole (1.0 µg/ml),
fluconazole (16 µg/ml), and 5FC (>256 µg/ml) for the organism
were
elevated (
23). These values were comparable to those
previously
reported in the literature for this species (Table
1).
Discussion.
Disseminated fungal infections continue to cause
significant morbidity and mortality in bone marrow transplant
recipients, despite advances in patient management (33, 37).
Risk factors for invasive fungal infections in this population include
neutropenia, administration of broad-spectrum antimicrobial agents,
steroid therapy for GVHD, mucosal barrier disruption, an allogeneic
transplant, and an unrelated donor (5, 13, 19). All of these
risk factors were present in the patient described here.
Aspergillus and Candida species are the most
common invasive fungal pathogens identified in bone marrow transplant
recipients; however, disseminated Fusarium and
Trichosporon infections are being reported with increasing frequency (4, 27, 37).
Five species of the genus
Trichoderma (
T. harzianum,
T. koningii,
T. longibrachiatum,
T. pseudokoningii, and
T. viride) have
been
identified as etiologic agents of infections in immunocompromised
hosts. The lack of pathogenicity of
Trichoderma species for
the
immunocompetent host is well illustrated by a report of the
inadvertent
infusion of
T. viride via contaminated
intravenous fluid (
31).
The patient was treated with
amphotericin B for 24 h and remained
well except for transient
bacteremia.
Ten cases of
Trichoderma species infections have been
reported in immunocompromised hosts. The report of the initial case
from 1976 described the isolation of
T. viride from a
pulmonary
mycetoma in a patient with chronic lung disease
(
7). Four cases
of peritonitis have been reported in
continuous ambulatory peritoneal
dialysis patients, with
T. koningii (
25),
T. harzianum (
11),
T. viride (
16), and
T. longibrachiatum
(
34) identified as
the etiologic agents. Only the patient
with
T. koningii peritonitis
survived.
T. viride
infection of a perihepatic hematoma in a liver
transplant recipient has
also been described (
12). Although
the fungal infection was
not the principal cause of death,
T. viride was present at
autopsy, despite surgical drainage and amphotericin
B therapy. An
erythroleukemia patient died from a disseminated
T. pseudokoningii infection 43 days after bone marrow transplantation
(
9). A
T. longibrachiatum brain abscess in a
17-year-old with
ALL was successfully treated with antifungal therapy
after surgical
resection (
32). An 11-year-old patient with
aplastic anemia
recovered from a
T. longibrachiatum skin
infection after receiving
3 months of antifungal therapy and a bone
marrow transplant (
20).
Invasive
T. longibrachiatum sinusitis in a liver and small-bowel
transplant
recipient was successfully treated with debridement
and antifungal
agents (
8). The present report is the fifth
report of
T. longibrachiatum as a cause of infection in an
immunocompromised
host and the first to suggest the gastrointestinal
tract as the
portal of
entry.
The recovery of
T. longibrachiatum from stool surveillance
cultures early in the course of the posttransplantation period
(day 8)
suggests that acquisition of the fungus was through the
gastrointestinal tract. Prolonged therapy with fluconazole in
addition
to antibiotics may have selectively favored the occurrence
of this
filamentous organism. The progression of disease despite
therapy with
amphotericin B, itraconazole, and liposomal amphotericin
B in
appropriate dosage regimens demonstrates the inadequacy of
current
approaches to therapy of hyalohyphomycosis in this group
of patients.
In vitro antifungal susceptibility data for this
patient correlated
with the outcome and lend further credence
to the usefulness of
antifungal susceptibility testing in the
determination of resistance to
currently available antifungal
agents. Unfortunately, no other
therapeutic options were available
at the time of this patient's
infection. Previous reports of
T. longibrachiatum infections
have also documented elevated MICs
for most antifungal agents (
2,
20,
32,
34), although
a favorable outcome was obtained when the
administration of amphotericin
B was coupled with surgical resection
(Table
1).
The genus
Trichoderma, first discovered by Persoon in the
early 1800s, is a ubiquitous, widely distributed component of the
soil
microflora. Until the revision of the genus
Trichoderma by
Rifai (
28) in 1969, most species were referred to as either
T. viride or
T. koningii, depending upon whether
they produced
globose or oval conidia, respectively. Rifai described
nine groups
of similar species differentiated primarily by conidiophore
branching
patterns and conidium morphology. He termed these groups
"species
aggregates," one of which was the
Trichoderma
longibrachiatum Rifai aggregate (
28). In the 1980s and
early 1990s, Bissett
(
2,
3) proposed an infrageneric
classification of
Trichoderma whereby the genus was divided
into sections:
Trichoderma section
Trichoderma,
Trichoderma section
Pachybasium,
Trichoderma section
Saturnisporum,
Trichoderma section
Longibrachiatum, and
Trichoderma section
Hypocreanum. Key features of
the section
Longibrachiatum included the following: (i)
colonies are rapidly growing and are
6 to 9 cm after 4 days at 20°C;
(ii) the reverse of fresh isolates
is conspicuously yellowish green;
(iii) chlamydospores are present
or absent; (iv) conidiophores are
sparingly branched, primary
branches are long, and secondary branches
are usually short and
rarely rebranched; (v) phialides are mostly
solitary ampulliform
to lageniform or cylindrical; and (vi) conidia are
one celled,
green, smooth walled, and ellipsoidal to obovoid. Species
in the
section
Longibrachiatum included
T. citrinoviride,
T. pseudokoningii,
T. longibrachiatum, and
T. atroviride. While Bissett
(
2,
3)
did define specific characteristics that could be
used to separate
these species, their use without the aid of more
recent molecular
techniques (
14,
15,
17,
18,
35,
36) is
fraught with
uncertainty. Recent molecular characterization of species
previously
identified as
T. pseudokoningii were in fact
found to be
T. longibrachiatum on the basis of analysis of
ribosomal DNA internal transcribed
spacer sequences (
15).
The same investigators also suggest that
the etiologic agent of human
mycoses reported to be
T. pseudokoningii was most likely
T. longibrachiatum because their study of geographic
trends
indicated that
T. pseudokoningii is restricted to Australia
and New Zealand as an anamorph of a
Hypocrea species
(
15,
35).
Many strains that they received as
T. pseudokoningii were found,
by their methods, to be either
T. citrinoviride or
T. longibrachiatum.
Although molecular fingerprinting is necessary for the unequivocal
confirmation of an organism as
T. longibrachiatum, several
characteristics that may be observed in the routine laboratory
are
suggestive of this species. Useful macroscopic characteristics
include
its rapid growth and rapid change from white to green,
its frequent
occurrence in concentric ringlike zones (Fig.
2a),
and its lemon yellow
diffusing pigment on PFA, although all strains
may not be so intense
(Fig.
2b). This species is thermotolerant,
with good growth observed at
both 35 and 42°C. Growth at elevated
temperatures is one of the
well-known virulence factors of neurotropic
fungi, and this organism's
potential neurotropism was documented
by brain abscess formation in the
patient with ALL described in
1995 (
32), as well as focal
cerebritis in the patient in the
present study. Microscopically, this
species is characterized
by sparsely formed, often slightly curved
conidiophores from the
main branch, unlike the pyramidal arrangement in
other species
aggregates, such as those in
T. viride. Unlike
the globose to
subglobose conidia of
T. viride, those in
T. longibrachiatum are
distinctly oval (Fig.
6). Given the
morbidity and mortality associated
with this agent in immunocompromised
hosts, a preliminary report
of a
Trichoderma species in the
section
Longibrachiatum would
alert clinicians to its
potential
pathogenicity.
As the number of profoundly immunosuppressed patients in the hospital
and community has escalated, so too has the diversity
of molds
recognized in association with human infection. It is
increasingly
clear that the concept of pathogenicity of molds
has little meaning in
this patient group and that a wide range
of normally saprobic molds may
cause life-threatening infections
in these individuals. The efficacy of
stool surveillance cultures
for the identification of fungal pathogens
in this population
and the usefulness of antifungal susceptibility
testing for the
determination of resistance are illustrated by the case
of infection
described here.
T. longibrachiatum should be
added to the list
of potentially lethal neurotropic organisms in
immunocompromised
hosts, and early aggressive therapy should be
instituted in patients
with infections whose suspected etiologic agents
resemble those
in the
Trichoderma section
Longibrachiatum.
| |
ACKNOWLEDGMENTS |
We are indebted to Gary Samuels (Agricultural Research Service,
U.S. Department of Agriculture) for DNA fingerprinting of the isolate
and Mary Lindsey for her mycological expertise.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Medical
Microbiology Division, C606 GH, Department of Pathology, University of
Iowa College of Medicine, Iowa City, IA 52242. Phone: (319) 394-9566. Fax: (319) 356-4916. E-mail: michael-pfaller{at}uiowa.edu.
| |
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Journal of Clinical Microbiology, April 1999, p. 1154-1160, Vol. 37, No. 4
0095-1137/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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