Maxillary Sinusitis Caused by Pleurophomopsis lignicola
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JOURNAL OF CLINICAL MICROBIOLOGY, Aug. 1997, p. 2136–2141 Vol. 35, No. 8
0095-1137/97/$04.0010
Copyright © 1997, American Society for Microbiology
Maxillary Sinusitis Caused by Pleurophomopsis lignicola
ARVIND A. PADHYE,1* R. W. GUTEKUNST,2 D. J. SMITH,2 AND E. PUNITHALINGAM3
Emerging Bacterial and Mycotic Diseases Branch, Division of Bacterial and Mycotic Diseases, National Center for
Infectious Diseases, Centers for Disease Control and Prevention, Public Health Service, U.S. Department of
Health and Human Services, Atlanta, Georgia 303331; Community Hospital, Munster, Indiana 463212;
and International Mycological Institute, Egham, Surrey TW20 9TY, United Kingdom3
Received 24 January 1997/Returned for modification 4 March 1997/Accepted 28 April 1997
An immunocompetent 59-year-old man developed sinusitis over a 6- to 8-month period after cutting down a
rotted maple tree (Acer sp.). A polypoid obstruction with a bloody drainage was evident in his right nasal cavity.
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A computed tomographic scan showed an opacification of the maxillary sinus. Surgery was performed to
remove a fungus ball that had extended into the patient’s medial sinus cavity. Sections of the sinonasal mucosa
revealed marked acute and chronic sinusitis with inflammation, congestion, and hemorrhage. Sections from
the pasty brown to black debrided material revealed a fungus ball consisting of an extensive network of
brown-pigmented, septate, profusely branched hyphae. When grown on oat agar, the phaeoid fungus produced
pycnidia and was identified as Pleurophomopsis lignicola. The genus Pleurophomopsis includes seven species,
which are all known from plant material. This report documents for the first time a coelomycetous fungus,
P. lignicola, causing sinusitis in an immunocompetent patient.
Chronic sinusitis and allergic sinusitis caused by phaeoid crotic material. Tissue sections were stained with hematoxylin
(dematiaceous) (12, 16) fungi have usually been reported for and eosin, periodic acid and Schiff’s reagent, and Grocott’s
patients who are immunologically intact (6, 10). Some of the methenamine silver nitrate stains.
patients had been treated with intranasal steroids, resulting in Tissue sections of the sinonasal mucosa showed marked
possible secondary fungal colonization (1, 26). A number of acute-to-chronic sinusitis with inflammation, congestion, and
patients with sinusitis were often swimmers, implicating water hemorrhage. There was no invasion of mucosa by the fungal
as a possible source of fungal infection (1, 6, 25). The most elements. Sections from the pasty brown to black material
common phaeoid etiologic agents of sinusitis include species of revealed a fungus ball composed of interwoven, profusely
the genera Alternaria, Bipolaris, Cladosporium, Curvularia, and branched, septate, light to dark brown hyphae, 2.5 to 5.0 mm in
Exserohilum (6, 10, 11, 14, 21). We describe a coelomycetous diameter (Fig. 1). Some hyphal walls were roughened or ver-
fungus, Pleurophomopsis lignicola Petrak, causing maxillary si- rucose.
nusitis in an immunocompetent man. Mycological studies. A portion of the biopsy tissue was cul-
(Preliminary results of this study were presented previously tured on Sabouraud dextrose agar and cornmeal agar (Difco
[15a].) Laboratories, Detroit, Mich.). Several velvety, olivaceous grey
Case report. A 59-year-old man was first seen in January
1992 with a complaint of having intermittent sinus problems
after cutting down a rotten maple tree (Acer sp.) 6 to 8 months
prior to his admission to the hospital. The patient had a pol-
ypoid obstruction with bloody drainage in the right nasal cav-
ity. A computer tomographic scan showed an opacification of
the maxillary sinus. He was admitted for a Caldwell-Luc oper-
ation and nasal airway reconstruction as well as a bilateral
inferior turbinectomy. He had no history of diabetes mellitus,
use of steroids, or hypertension. The patient underwent surgi-
cal removal of a fungus ball that had extended into his medial
sinus cavity.
Treatment with amphotericin B was initiated. His postoper-
ative course was complicated by a spinal fluid leak that re-
quired rehospitalization. He received a total of 1.0 g of am-
photericin B without further complications. When examined in
April 1992 and later in June 1993, he was found to be healthy
with no evidence of any sinus tenderness. A biopsy taken from
the nasal area was negative for fungi. A checkup 1 year later
showed that he was healthy without any evidence of sinusitis.
Histologic examination. The biopsied tissue labelled “thick-
ened membrane from the right maxillary sinus” consisted of
several small fragments of pasty, brown to black, partially ne-
FIG. 1. Tissue section of the synovial mucosa showing profuse growth of
* Corresponding author. Mailing address: Mail Stop G-11, Centers septate, branched hyphae of P. lignicola. Staining was with Grocott’s methana-
for Disease Control and Prevention, Atlanta, GA 30333. mine silver. Magnification, 3580.
2136VOL. 35, 1997 NOTES 2137
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FIG. 2–6. (2) Vertical section of pycnidium of P. lignicola on oat agar. Magnification, 3164. (3) Vertical section of the pycnidium of P. lignicola. Magnification,
3320. (4) Vertical section of bilocular pycnidium of P. lignicola. Magnification, 3320. (5) Part of pycnidial wall, conidiophores, conidiogenous cells and conidia.
Magnification, 3650. (6) Roughened or verrucose hyphae. Magnification, 31,620.
colonies were evident after 7 days of incubation at 25 and 37°C. was sent through the Indiana State Board of Health to the
A microscopic examination of the colonies showed that they Fungus Reference Laboratory, Centers for Disease Control
consisted of septate, branched, yellowish brown hyphae with- and Prevention (CDC), for specific identification. At the CDC,
out any conidia. A subculture of the isolate and tissue slides several media such as cornmeal, V8 juice, Pablum cereal, lac-2138 NOTES J. CLIN. MICROBIOL.
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FIG. 7–10. (7) Innermost cell layer lining the floor of the convoluted pycnidial cavity with conidiophores, conidiogenous cells, and conidia. Magnification, 3650.
(8) Innermost cell layer lining the pycnidial cavity with conidiophores, conidiogenous cells, and conidia. Magnification, 31,620. (9) Conidiophores, conidiogenous cells,
and conidia. Magnification, 31,620. (10) Conidia. Magnification, 31,620.
tritmel, and oatmeal salt agars (13, 23) were used to induce aerial mycelium. The reverse of the colony was moderate red-
sporulation. Subcultures on the above-mentioned media were dish brown. The mycelium was composed of septate, smooth-
incubated at 25°C and were alternately exposed to 12 h of to-roughened-to-verrucose, yellowish brown-to-reddish brown
daylight and 12 h of darkness to induce sporulation but without hyphae (Figs. 2–6). Conidiophores, condiogenous cells, and
success. A subculture was sent to the International Mycological conidia were produced inside pycnidia. The pycnidia were scat-
Institute (IMI), Egham, United Kingdom, for further studies. tered on the surface, and some were partially immersed in the
At the IMI, subcultures on oat agar in petri dishes were agar. They were reddish brown, subglobose, and chiefly uni-
subjected to a regimen of near-UV (black light) irradiation for loculate, though occasionally biloculate, with the floor of the
12 h and incubation for 12 h in darkness to induce sporulation cavity sometimes being convoluted, with prominent necks be-
(24). After 4 weeks, cultures on oat agar were floccose, light set with flexous hyphae (Fig. 2 to 5). They were ostiolate and
yellowish brown becoming greyish sepia, with an abundant measured 220 to 250 mm wide and 300 to 600 mm high. Osti-Downloaded from http://jcm.asm.org/ on February 5, 2021 by guest
TABLE 1. Comparison of some Phoma, Pleurophoma, Pleurophomopsis, and Pyrenochaeta species isolated in culture from human infection
Characteristicsa of:
Species
Conidiomata Setae on or around ostiole Conidiophores Conidiogenous cells Conidia Culture
Phoma cava (see Pleu-
rophoma cava)
Phoma species
P. cruris-hominis Pycnidia globose, 100–160 mm in diam, bay 2b 2 Hyaline, globose to doliiform, in- Hyaline, aseptate, globose to Colony initially floccose,
to dark brick, thin walled, with very distinguishable from cells lining obovoid, 2–4 by 1–1.5 mm finally cinnabar red,
short necks the pycnidial cavity, phialidic chlamydospores absent
P. eupyrena Pycnidia variable, nearly globose, 110–250 2 2 Hyaline, subglobose to ampulli- Hyaline, aseptate, cylindrical to Colony initially dense, fi-
mm wide, dark brown or black, thin form, indistinguishable from oblong, 3–5 by 2 mm nally black with abundant
walled, with distinct necks cells lining the pycnidial cavity, chlamydospores
phialidic
P. herbarum Pycnidia globose, 90–180 mm in diam, light 2 2 Hyaline, globose to doliiform, Hyaline, aseptate, cylindrical to Colony variable with sparse
brown to reddish brown indistinguishable from cells oblong, 4–6 by 2–2.5 mm mycelia, olive brown to
lining the pycnidial cavity, grey green, pycnidial exu-
phialidic date buff to pink, chlamy-
dospores absent
P. hibernica Pycnidia 100–200 mm in diam, fawn to 2 2 Hyaline, globose, indistinguish- Hyaline, aseptate, ellipsoid to Colony with sparse mycelia,
dark brown, thin walled, without necks able from cells lining the pyc- oblong, 5–8.5 by 2–3.5 mm fawn to dark brown, pyc-
nidial cavity, phialidic nidial exudate pinkish,
chlamydospores absent
P. minutella Pycnidia subglobose, 100–150 mm wide, dark 2 2 Hyaline, ampulliform, phialidic Hyaline, aseptate, allantoid to Isolate from human infec-
brown, thick walled, with short necksc cylindrical, 3.5–5 by 0.7–1 mm tion not examined
P. minutispora Pycnidia globose, 120–200 mm, dark brown 2 2 Hyaline, globose, indistinguish- Hyaline, aseptate, globose to Colony grey olivaceous to
to black, thin walled, mainly without able from cells lining the pyc- oblong, 2–3 by 1.5–2 mm vinaceous buff or pinkish
necks nidial cavity, phialidic at the periphery with sim-
ple sparse chlamydospores
P. oculo-hominis Pycnidia subglobose, obpyriform, 120–200 2 2 Hyaline, globose to obpyriform, Hyaline to straw yellow to Colony fuscous black,
mm in diam, vinaceous to fuscous black, indistinguishable from cells brown, aseptate conidia, 3–7 chlamydospores absent
thick walled with necks lining the pycnidial cavity, by 1–2 mm, 1-septum conidia
2139
phialidic 9–16 by 3–4.5 mm
P. sorghina Pycnidia subglobose to globose, 60–140 mm 2 2 Hyaline, subglobose to ampulli- Variable, hyaline chiefly asep- Colony floccose to greyish
in diam, yellowish brown to dark or pur- form, indistinguishable from tate, rarely 1-septum, ellipsoid or rose to pink, chlamy-
plish brown, thin walled, with very prom- cells lining the pycnidial cavity, or shortly cylindrical, 4–7 by dospores simple or com-
inent necks phialidic 2–2.5 mm plex
Pleurophoma species
P. cava Pycnidia subglobose, 180–280 mm wide, 2 Filiform, septate with very short Hyaline, subglobose to shortly Hyaline, variable, straight or Colony variable, felty, oliva-
yellowish brown, thick walled, with or lateral branches or openings cylindrical, borne on conidio- slightly curved, mainly 2.5–3.5 ceous grey chlamydos-
without short necks below septa phores or arising directly from by 0.5–1.5 mm pores present
cells lining the pycnidial cavity
P. pleurospora Pycnidia subglobose, up to 300 mm in 2 Filiform, multiseptate with very Hyaline, borne on conidiophores Usually hyaline, some isolates Colony floccose to dark
diam, dark brown to black, thick walled, short lateral branches or open- just below the transverse septa, produce yellowish brown, grey or dark brown,
with or without short necks ings just below septa phialidic shortly cylindrical-to-oblong chlamydospores absent
conidia, 3.5–4 by 1.5 mm
Pleurophomopsis Pycnidia subglobose, 200–250 by 300–600 2 Septate with distinct branches Hyaline, cylindrical, conidiog- Hyaline, shortly cylindrical, Colony floccose, becoming
lignicola mm, brown to reddish brown, thick walled (not openings) immediately enous loci terminal on lateral aseptate, 2.5–3 by 1.5 mm greyish sepia, chlamydos-
with short prominent necks below septa branches, phialidic pores absent
Pyrenochaeta species
P. mackinnonii Pycnidia globose, up to 140 mm in diam, Septate, long Hyaline, septate with short lat- Hyaline, cylindrical, conidiog- Pale yellow to saffron yellow in Colony grey, smooth vel-
dark brown, thick walled, with short eral branches enous loci terminal, phialidic mass, aseptate, ellipsoid, vety, with folds, chlamy-
necksd 2.5–3 by 1.5–2 mm dospores absent
P. romeroi Pycnidia subglobose, 80–160 mm in diam, Setae around ostioles, Sparse, with lateral branches Hyaline, borne on branches or Hyaline to yellowish, shortly Colony wooly greyish to
dark brick to fawn, later dark brown, septate, roughened, arising directly from cells lin- cylindrical, 1.5–2 by 1.0 mm fuscous black, simple
with short necks 80–100 by 3 mm ing the pycnidial cavity chlamydospores in chains
in old cultures
P. unguis-hominis Pycnidia of two sizes: simple pycnidia sub- Septate, up to 70 mm Septate with very short lateral Hyaline, borne on branches, ter- Hyaline, aseptate, shortly cylin- Colony floccose, brown vi-
globose, 100–200 mm; compound forms long branches lining pycnidial cavity minal, phialidic drical or slightly curved, 2–3 naceous to fawn, chlamy-
up to 500 mm by 1–1.5 mm dospores absent
a
Details were taken from species grown on oat agar.
b
2, feature absent.
c
From reference material on the plant host.
d
From the original diagnosis.2140 NOTES J. CLIN. MICROBIOL.
oles were circular, surrounded by thick-walled, dark reddish- granulocytopenic patient (15). Two species of the genus Pyre-
brown cell layers. Conidiophores were hyaline, cylindrical, sep- nochaeta, namely, P. mackinnonii and P. romeroi, are known to
tate, and branched at the base. They arose from the cells lining cause eumycotic black grain mycetoma (19).
the floor of the pycnidial cavity and measured 10 to 18 mm The effectiveness of the azoles against subcutaneous and
long. Conidiogenous cells were generally borne on conidio- systemic phaeohyphomycotic infections caused by pycnidial
phores but occasionally arose directly from the cells lining the fungi has not been fully established. Data on the in vitro sus-
pycnidial cavity (Fig. 7, 8). They were hyaline, cylindrical, ceptibilities of pycnidial fungi causing human disease are also
smooth, phialidic (sensu Sutton [24]), and acropleurogenous scanty. Many such infections may go unreported because iso-
(formed at the end and on the sides) (Fig. 9). Conidia were lates of the coelomycetous fungi do not sporulate readily on
hyaline, cylindrical, and aseptate and measured 2.5 to 3.0 by 1.5 the routine mycological media used in clinical laboratories.
mm (Fig. 10). These fungi also pose difficulty in their identification because
The isolate (CDC B-5369 or IMI 354512 or ATCC 90281) many pycnidial fungi are plant pathogens and their morpho-
agreed with the isotype of Pleurophomopsis lignicola, which had logic features are often described on the basis of their devel-
been described on the basis of a sample from rotting hard- opment on natural plant hosts rather than their characteristics
wood, in all essential characters. in culture. Despite the difficulties experienced in the identifi-
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Discussion. It is worth mentioning that Petrak in 1922 (17) cation of species belonging to the genera Phoma, Pleurophoma,
first described the genus Plectophomopsis and in the following Pleurophomopsis, and Pyrenochaeta causing infections in hu-
year distributed specimens labelled Plectophomopsis lignicola mans mentioned above, the species referred to in this paper
as exsiccata Flora Bohemiae et Moraviae exsiccata II. Serie 1. can be identified on the basis of the important characteristics
Abteilung Pilze nr. 1689. There is no record of a formal descrip- enumerated in Table 1. According to the current concepts (24),
tion of Plectophomopsis lignicola having been published by the differences between Pleurophoma and Pleurophomopsis are
Petrak. Subsequently, Petrak (18) described the fungus as in their conidiogenous loci. The conidiogenous loci in Pleuro-
Pleurophomopsis lignicola. At present, the genus Pleuropho- phoma are on very short lateral branches or openings imme-
mopsis includes seven species, which are all known from plant diately below transverse septa, whereas those in Pleuropho-
material. mopsis are terminal on lateral branches and not on openings
To our knowledge, this case represents the first record of a below the septa.
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