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Journal of Clinical Microbiology, July 1998, p. 2157-2163, Vol. 36, No. 7
0095-1137/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Fatal Hormonema dematioides Peritonitis
in a Patient on Continuous Ambulatory Peritoneal Dialysis:
Criteria for Organism Identification and Review of Other Known
Fungal Etiologic Agents
Jong Hee
Shin,1
Sang Ku
Lee,1
Soon Pal
Suh,1
Dong Wook
Ryang,1
Nam Ho
Kim,1
Michael G.
Rinaldi,2,3 and
Deanna A.
Sutton3,*
Departments of Clinical Pathology and
Internal Medicine, Chonnam University Medical School, Kwangju,
Korea,1 and
Audie L. Murphy Division,
South Texas Veterans Health Care System,2 and
Fungus Testing Laboratory, Department of Pathology,
University of Texas Health Science Center at San
Antonio,3 San Antonio, Texas 78284
Received 2 January 1998/Returned for modification 9 March
1998/Accepted 7 April 1998
 |
ABSTRACT |
We report a fatal case a fungal peritonitis caused by the
yeast-like dematiaceous mould Hormonema dematioides in a
45-year-old woman. The woman had a 13-year history of insulin-dependent
diabetes mellitus and had been on continuous ambulatory peritoneal
dialysis for chronic renal failure. H. dematioides was
repeatedly isolated from the dialysate culture specimens collected on
days 3, 9, 16, and 20 of her hospital stay. Preliminary culture reports
on day 7 of the growth of a yeast-like fungus, a probable
Candida species, prompted the administration of fluconazole
(FLU). Intraperitoneal and intravenous FLU failed to eliminate the
mould, and the patient expired on day 21 of her hospital stay. We use
this case to present what appears to be the first report of fungal
peritonitis due to H. dematioides, to provide laboratorians
with criteria for differentiating this organism from the similar mould
Aureobasidium pullulans and from various yeast genera, and
to provide a review of known fungal taxa inciting peritonitis.
| |
TEXT |
Fungal peritonitis is a serious and
potentially life-threatening complication of both intermittent
peritoneal dialysis and continuous ambulatory peritoneal dialysis
(CAPD). Investigators reviewing significant numbers of CAPD-associated
fungal peritonitis episodes cite yeasts, particularly
Candida species, as the predominant etiologic agents
(10, 12, 13, 20, 29, 37, 38, 50, 52, 53, 54, 58, 61, 63, 65, 66,
68, 73, 78). Filamentous fungi complicating CAPD, although
reported less frequently and fewer in number, encompass a wide array of
agents, from the classic, systemic pathogens (4, 42, 45) to
zygomycetous species (55, 64) and members of numerous
moniliaceous (3, 11, 16, 25, 27, 30, 33, 39, 40, 48, 51, 57, 67,
71, 75, 76, 77) and dematiaceous genera (1, 2, 6, 7, 14, 21,
28, 31, 34, 43, 44, 59, 69, 80). See Table
1 for a listing of reported etiologic
agents of fungal peritonitis. Filamentous CAPD-associated fungi
displaying cream-colored (moniliaceous) colonies and yeast-like
synanamorphs may initially be considered Candida or
Cryptococcus species. Two such organisms, Hormonema
dematioides Lagerberg et Melin [teleomorph, Sydowia
polyspora (von Tavel) Müller], the subject of this report, and Aureobasidium pullulans (deBary) Arnaud, an agent
previously reported in fungal peritonitis (7, 14), are both
initially somewhat mucoid, yeast-like (both macroscopically and
microscopically), and hyaline. As they mature, their filamentous nature
becomes evident and colonies become dematiaceous, with the production of brown, thick-walled hyphae. McCarthy et al. observed that when tested by conventional yeast identification systems, specifically API
20C yeast identification system strips (bio Mérieux, Marcy l'Etoile, France), A. pullulans usually fails to give a
code while H. dematioides may code as Cryptococcus
albidus (49). Both organisms may present diagnostic or
identification difficulties in the setting of the CAPD-associated
fungal peritonitis patient.
Case report.
A 45-year-old woman on CAPD presented at the
emergency room of Chonnam University Hospital on 19 March 1996 with
nausea, anorexia, increased body weight (from 56 to 74 kg), abdominal
distention, and pitting edema. She had a 13-year history of
insulin-dependent diabetes mellitus and had had an arteriovenous shunt
inserted in February of 1995. Malfunction of the shunt required
switching from hemodialysis to CAPD in April 1995. On 1 March 1996, the patient developed abdominal pain and her dialysate became cloudy. Cefazolin and vancomycin were administered intraperitoneally for 20 days without clinical improvement. Upon admission from the emergency
room, the patient's dialysate cell count was 306/µl, with a
predominance of polymorphonuclear neutrophils (70%). The hemoglobin
level was 6.6 g/dl, the leukocyte count was 6,700/µl, the blood urea
nitrogen level was 12.1 mg/dl, and the serum creatinine level was 5.0 mg/dl. The patient was initially treated with intraperitoneal ceftazidime and imipenem. Fluconazole therapy was started on hospital day 7, following a preliminary culture report indicating the presence of a yeast-like fungus, probably a Candida species, in the
dialysate. Dialysate cell counts on day 6 were 2,600/µl, with a
predominance of polymorphonuclear neutrophils. On day 8, the patient's
abdominal pain and fever slightly improved, but vasopressive drug and
O2 therapies were started due to the occurrence of
respiratory insufficiency and hypotension. Dialysate cell counts were
675 and 441/µl on days 9 and 17, respectively. The same yeast-like
fungus was cultured from the dialysate on days 3, 9, 16, and 20. Fluconazole was administered intraperitoneally (200 mg/day) for 15 days
and intravenously (800 mg/day) for the last 2 days. The catheter tip
was removed on day 20. On day 21 the patient began to lose
consciousness, appeared to have signs of acute respiratory
insufficiency due to hypoxia and septic shock, and expired. Blood
cultures for the causative organism remained negative.
Mycology.
All four peritoneal fluid culture specimens
collected during the patient's hospital stay (on days 3, 9, 16, and
20) revealed the same organism. Three of the dialysates were inoculated
onto Sabouraud dextrose agar (SDA) (Becton Dickinson, Cockeysville, Md.), prepared in-house (Fig. 1), while
one was inoculated into BACTEC 16A and 17A bottles (Becton Dickinson,
Towson, Md.). Only the BACTEC 16A bottle (aerobic medium) was positive
after 48 h of incubation. Pure growth of cream-colored mucoid
colonies was observed on SDA and on the blood agar plate subculture
from the BACTEC 16A in 24 to 48 h at 35°C. Growth at 35°C was
slow, and a Gram stain of organisms from the colony revealed
oval-shaped yeast forms. API 20C yeast identification system strips,
tested a total of seven times with identical results, indicated
assimilation of glucose, glycerol, 2-keto-gluconate,
L-arabinose, D-xylose, adonitol, xylitol,
galactose, inositol, sorbitol, cellobiose, maltose, saccharose,
trehalose, melibiose, and raffinose, giving a numerical code of
6773277. The API database, which provides a list of species and their
probabilities, with a confidence estimate for each identification,
indicated the code as an unacceptable profile with no identification.
Ancillary testing on cornmeal agar (Difco Laboratories, Detroit, Mich.)
by the Dalmau method (17) indicated the presence of hyphae
and blastic conidia. Conidia occurred asynchronously from the hyphae as
viewed under the coverslip after 72 h of incubation at 25°C
(Fig. 2). Prolonged incubation of the
isolates for 1, 2, and 3 weeks on SDA revealed their dematiaceous nature (Fig. 3). Subsequent subcultures
of the isolate at 25°C were totally brown to black. A 5-day slide
culture revealed the presence of moniliaceous blastic conidia being
produced from dematiaceous hyphae (Fig.
4).
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FIG. 2.
Basipetal, hyaline blastic conidia of H. dematioides produced asynchronously (one at a time) from hyaline
hyphae on cornmeal agar by the Dalmau method (72 h; 25°C).
Magnification, ×710.
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FIG. 3.
Macroscopic morphology of H. dematioides on
SDA (1 week [A], 2 weeks [B], and 3 weeks [C]; 25°C).
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FIG. 4.
Moniliaceous blastic conidia of H. dematioides being produced from conidiogenous loci (arrows) on
dematiaceous hyphae. Magnification, ×280.
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Pathogenicity and identifying features.
Fungal peritonitis in
patients on CAPD, although significantly less frequent than bacterial
peritonitis (3 to 15% versus >80%, respectively), is a
well-documented clinical entity (13, 38, 54, 65, 78). Signs
and symptoms are essentially the same in both presentations and may
include cloudy dialysate effluent, dialysate leukocyte counts greater
than 100/mm3, neutrophil counts greater than 50%,
abdominal pain, distension, rigidity, nausea and vomiting, diarrhea,
and fever. Because of these similarities and the higher incidence of
bacterial peritonitis, fungal etiologies may be overlooked and may have
contributed, in part, to a delayed antifungal regimen in the case of
this patient. She received cefazolin and vancomycin intraperitoneally
for 20 days, without improvement, followed by ceftazidine and imipenem intraperitoneally for another 7 days. Not until hospital day 7 (episode
day 28), with the report of a Candida species in the dialysate, was fluconazole therapy started. Although the route of
infection is not clear, several reports have cited altered host flora
due to prior or prolonged use of broad-spectrum antibacterial therapy
as a significant risk factor and/or as being associated with the
development of fungal peritonitis (13, 38, 54, 65, 78).
Fungal cultures taken earlier in the course of this patient's episode
or during the administration of antibacterial agents would have
provided direction for more appropriate or additional antifungal
therapy.
The recovery of cream-colored, mucoid colonies from the dialysate on
hospital day 7 (episode day 28) provided the first evidence
of a fungal
pathogen. Cream-colored mucoid colonies are consistent
with a variety
of fungal genera, both yeast-like and filamentous,
including
Candida,
Cryptococcus,
Aureobasidium,
and
Hormonema.
In the genera
Aureobasidium and
Hormonema, cream-colored colonies
become brownish to
olivaceous black with time, thereby requiring
extended incubation for
recognition of their dematiaceous nature.
The API 20C yeast
identification system utilized with these colonies
failed to provide an
identification, giving an unrecognizable
code of 6773277. McCarthy et
al. recently reported on 4 of 11
isolates of
H. dematioides
coding as
C. albidus by this method
(
49). The
remaining 7 isolates in their group revealed several
different
unrecognizable codes, which did not include this isolate's
number,
6773277. Their results reinforce the necessity of performing
critical
microscopic observations (for blastic conidia, hyphae,
pseudohyphae,
etc.) and demonstrate the futility of relying solely
on binary codes
and/or physiologic characteristics for these similar,
cream-colored,
mucoid taxa. Because the API 20C method failed
to provide an
identification, the case isolate was subsequently
identified by
ancillary testing utilizing the Dalmau method for
determining the
method of conidiogenesis and extended incubation
for revealing its
dematiaceous affinities. Slide culture preparations
normally used for
studying methods of conidiogenesis in filamentous
fungi are generally
less satisfactory than the Dalmau method for
visualizing the
asynchronous or synchronous development of conidia
in
Hormonema and
Aureobasidium species,
respectively.
H. dematioides is an important wood-bluing fungus often
isolated from discolored coniferous wood or needles (
32). It
is
also appears to occupy an ecological niche in moist environments,
as
evidenced by the isolates submitted to the Fungus Testing Laboratory
(FTL) at the University of Texas Health Science Center at San
Antonio
from high-humidity areas. Its pathogenicity in humans
has been
previously documented as an agent of subcutaneous phaeohyphomycosis
of
the hands of an immunocompetent host (
15). Additional human
sites from which the organism has been recovered include cerebrospinal
fluid, blood, stool, pleural fluid, a surgical wound, and a knee
(FTL
isolates [unpublished data]).
Because authors have illustrated
H. dematioides under the
name of
A. pullulans, some cases of infection ascribed to
A. pullulans may actually have been caused by misidentified
isolates of
H. dematioides. Recently Clark et al. described
a case of peritonitis
caused by
A. pullulans in a patient on
CAPD (
14). Caporale et
al. reported
A. pullulans
as an agent of peritoneal catheter colonization
and peritonitis
(
7). The present case demonstrates that
H. dematioides can also cause CAPD-associated peritonitis. The pure
growth of the organism from four separate specimens from a patient
who
had diffuse abdominal pain and turbid dialysates indicates
that it was
the cause of peritonitis and not a contaminant.
Colonies on SDA at 25°C are white to cream, smooth, and soon covered
with a light slimy mass of blastoconidia. Poorly conidiating
cultures
are olivaceous black with a wooly mycelial mat. The optimum
temperature
for growth is 24°C, with a daily growth rate of >6
mm; no growth is
observed on media containing cycloheximide. Isolates
that have been
subcultured repeatedly conidiate poorly and tend
to grow faster than
freshly isolated strains (
32). Microscopically,
hyphae are
septate, hyaline, and initially thin walled and soon
become brown and
thick walled, with cells wider than they are
long. Hyaline, smooth,
ellipsoidal blastic conidia (4.5 to 12
µm by 3 to 4.5 µm) are borne
asynchronously by percurrent proliferation
(each successive conidium
growing through the tip of the conidiogenous
cell) from mostly
intercalary conidiogenous loci on hyaline as
well as dematiaceous
hyphae (Fig.
4). Older conidia often swell
and become brown and are
frequently two celled. Endoconidia (conidia
formed inside hyphal cells)
may be present. The method of conidiogenesis
for both
A. pullulans and
H. dematioides is best studied by the
Dalmau method.
H. dematioides is differentiated from
A. pullulans by asynchronous, basipetal (youngest conidium
at the base) conidial
formation from both hyaline and dematiaceous
hyphae rather than
synchronous (all at the same time) conidial
formation from only
hyaline hyphae. Synchronous conidia appear as a
cluster, with
each member attached to a separate denticle, while
asynchronous
conidia appear as a detached cluster around an individual
conidiogenous
aperture. Also note that several other
Hormonema species exist,
but all grow <6 mm per day at
24°C. Both
H. dematioides and
A. pullulans are
differentiated from hyaline, mucoid yeasts by the
formation of
dematiaceous hyphae (Table
2).
Therapy.
Fungal peritonitis is associated with significant
morbidity and mortality. In the patient this report, intraperitoneal
fluconazole (200 mg/day for 15 days) followed by intravenous
fluconazole (800 mg/day for 2 days) therapy failed to improve the
clinical conditions. Retrospectively, higher empiric doses earlier may
have been more efficacious, as judged by data from yeast isolates that
exhibit dose-dependent susceptibility to fluconazole and that therefore require maximum dosing regimens (70). Catheter removal,
considered a necessary adjunct to antifungal therapy (11, 37, 38,
54, 77), was delayed because there was no other therapeutic
option for renal failure in this patient. The patient had severe,
frequent hypotension histories associated with the arteriovenous shunt, severe malnutrition, and extensive peritoneal adhesions. Treatment of
fungal peritonitis caused by rare fungi such as H. dematioides is complicated by problems in identification, the lack
of in vitro antifungal susceptibility data, empiric therapy which may
not be appropriate (24), and the reluctance to initiate
amphotericin B therapy until a final identification is made. Although
standardization of susceptibility testing for filamentous fungi is only
commencing (23) and in vivo-in vitro correlations are
lacking, a significant number of dematiaceous moulds appear to be
susceptible, in vitro, to itraconazole (74). Although the
case isolate was not available for testing against antifungal agents,
data from the FTL for five similar dematiaceous A. pullulans
isolates tested by a modified National Committee for Clinical
Laboratory Standards reference method (56) suggest greater
in vitro susceptibility to itraconazole. Had the filamentous and
dematiaceous nature of the etiologic agent been known earlier, the
institution of itraconazole therapy, with or without amphotericin B,
may have facilitated defervescence. Several reports cite its use in
CAPD-associated fungal peritonitis (12, 22, 28, 39, 67, 77).
Although filamentous fungal organisms in CAPD-associated peritonitis
are low in incidence, they are often associated with
significant
morbidity and/or mortality. As this case emphasizes,
consideration of a
fungal etiology early in the course of the
disease, particularly in
patients unresponsive to antibacterial
therapy, is crucial. Early
recognition and identification of the
etiologic agent, coupled with
appropriate, aggressive therapy
(antifungal therapy and catheter
removal, when possible), appear
tantamount to a successful outcome.
H. dematioides is yet another
dematiaceous agent that
incites CAPD-associated fungal peritonitis.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Fungus Testing
Laboratory, Department of Pathology, University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Dr., San Antonio, TX 78284-7750. Phone: (210) 567-4131. Fax: (210) 567-4076. E-mail:
suttond{at}uthscsa.edu
| |
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Journal of Clinical Microbiology, July 1998, p. 2157-2163, Vol. 36, No. 7
0095-1137/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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