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Peritonitis Due to Thermoascus taitungiacus (Anamorph Paecilomyces taitungiacus)

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0095-1137/01/$04.00⫹0 DOI: 10.1128/JCM.39.2.720–724.2001

Copyright © 2001, American Society for Microbiology. All Rights Reserved.

Peritonitis Due to

Thermoascus taitungiacus

(Anamorph

Paecilomyces taitungiacus

)

ASHER KORZETS,1,2MIRIAM WEINBERGER,2,3* AVRY CHAGNAC,1,2

ANNA GOLDSCHMIED-REOUVEN,2,4MICHAEL G. RINALDI,5,6 ANDDEANNA A. SUTTON6

Department of Nephrology, Golda Campus,1and Department of Internal Medicine C & Infectious Diseases, Beilinson Campus,3Rabin Medical Center, Petach-Tikva, Mycology Unit, Chaim Sheba Medical Center, Tel-Hashomer,4and

The Sackler School of Medicine, Tel-Aviv University, Ramat-Aviv,2Israel, and Audie L. Murphy Division, South Texas Veterans Health Care System,5and Fungus Testing Laboratory, Department of Pathology,

University of Texas Health Science Center,6San Antonio, Texas

Received 21 August 2000/Returned for modification 19 September 2000/Accepted 1 December 2000

The first case of human disease due to the thermophilic ascomycete Thermoascus taitungiacus(the

teleo-morph of Paecilomyces taitungiacus) is presented. T. taitungiacus was recovered from four dialysate fluid

specimens of a 57-year-old patient undergoing chronic peritoneal dialysis. Identification was based upon cylindrical conidia, reddish orange nonostiolate ascomata, lack of growth at 20°C, thermotolerance, and ascospores that appeared pale yellow, elliptical, thick walled, and predominately echinulate by light microscopy but irregularly verrucose by scanning electron microscopy.

Paecilomycesspecies are found worldwide in soil, water, and decaying vegetation (13, 29) and are microscopically similar to

Penicilliumand some Aspergillusspecies. While they are un-common human pathogens, they have been associated with serious infections in both immunosuppressed and immuno-competent patients, especially those with defects in the ana-tomic barriers or with a foreign body. Five species in the genus

Paecilomyceshave been reported to cause infection, including

Paecilomyces variotii, Paecilomyces lilacinus, Paecilomyces mar-quandii, Paecilomyces viridis, andPaecilomyces javanicus(13). The most commonly reported infections are keratitis, endoph-thalmitis, and cutaneous infections. Fungemia, prosthetic valve endocarditis, lung infections, sinusitis, and peritonitis are less frequently reported (11, 20, 23, 24, 26, 29).Thermoascus crus-taceushas been reported from monocyte cultures of patients with AIDS (14). We report what we believe to be the first case of human mycosis due to the ascomycetous fungus Thermoas-cus taitungiaThermoas-cus causing peritonitis in a patient undergoing chronic peritoneal dialysis (CPD).

Case report.A 57-year-old man presented on 25 October

1998 with a 5-day history of abdominal pain. Since 1994 the patient had been treated with CPD for end-stage renal failure due to chronic glomerulonephritis and malignant hyperten-sion. He had had two episodes of bacterial peritonitis in 1996. Physical examination on admission revealed diffuse abdominal tenderness compatible with peritonitis. Empirical intraperito-neal treatment with cefazolin, 0.5 g/2 liters, and aztreonam, 0.6 g/2 liters, was started following a cell count of the turbid dia-lysate effluent that revealed 250 white blood cells/mm3(35%

neutrophils, 10% lymphocytes, and 55% monocytes). Three additional dialysate fluids were collected on October 27 and 29

and November 1. Each was plated onto blood, MacConkey, chocolate, and Sabouraud dextrose agar (SDA) plates (Hy Laboratories, Rehovot, Israel), as well as Lo¨wenstein-Jensen medium agar tubes (Heipha Diagnostika, Heidelberg, Germany), and incubated at 35°C. All bacterial cultures were negative, but by early November a tan-colored mould grew in pure culture on the Sabouraud agar plates from the four sep-arate dialysate fluid specimens. Intravenous amphotericin B (40 mg/day) was started, and the indwelling Tenckhoff catheter was removed. Hemodialysis was thereafter maintained via a temporary central vein catheter.

Amphotericin B was discontinued after 2 weeks of therapy due to intolerance (severe and repeated vomiting), liver toxic-ity (elevated serum alkaline phosphatase levels), and the de-velopment of a deep vein thrombosis of the upper limb. Oral ketoconazole (200 mg/day) was then given for 2 weeks but was stopped due to the appearance of fever, the accumulation of ascitic fluids, and worsening abdominal pain. The patient be-came severely catabolic with an accompanying weight loss of 5 kg and hypoalbuminemia of 24 g/liter. Amphotericin B therapy was restarted on December 6 and was given thrice weekly at the end of each hemodialysis session together with intradialytic parenteral nutrition. Fever abated and abdominal pain im-proved; however, no improvement was seen in either the ascitic fluid volume or the ascitic white cell count. On 20 January 1999, oral itraconazole (400 mg/day) was substituted for am-photericin B, resulting in a gradual decrease in the accumula-tion of ascitic fluid and complete disappearance of the abdom-inal pain. The patient started to gain weight, and his serum albumin level increased to 37 g/liter. Itraconazole was discon-tinued after 5 months of therapy. Repeated dialysate fluid cultures since November 1 were all sterile.

In July 1999, one month after the discontinuation of itra-conazole therapy, an enlarging right kidney mass, diagnosed histologically as renal cell carcinoma, was removed at nephrec-* Corresponding author. Mailing address: Internal Medicine C &

Infectious Diseases, Rabin Medical Center, Beilinson Campus, Petach-Tikva 49100, Israel. Phone: 9378210. Fax: 972-3-9221605.

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tomy. Two years later the patient is doing well on hemodialysis and remains asymptomatic.

Mycologic studies.The mould isolated from the peritoneal

fluids was initially identified as aPaecilomycesspecies at the Mycology Unit, Chaim Sheba Medical Center, Tel-Hashomer, Israel. It was then referred to the Fungus Testing Laboratory, Department of Pathology, University of Texas Health Science Center at San Antonio, San Antonio, Texas, where the final identification of T. taitungiacus was made and susceptibility tests were performed. The isolate was accessioned as UTHSC R-3084, subcultured onto in-house-made (21) potato flakes agar (PFA) and SDA (Remel, Lenexa, Kans.), and incubated at 25, 35, and 42°C. A slide culture was also prepared on PFA and incubated at 25°C. Growth of the isolate on PFA (Fig. 1A) and SDA revealed colonies that were initially flat and buff colored but that quickly (within 6 days) became yellowish or-ange with a brownish yellow reverse. Sparse conidial structures of thePaecilomycesanamorph were evident between 3 and 4 days at 25°C on PFA. Conidia were initially cylindrical to rectangular, approximately 7 to 7.8 by 2.9 to 3.9␮m, and then became elliptical to subglobose (Fig. 1C). With the formation of aPaecilomycesanamorph, additional subcultures onto Cza-pek Dox and malt extract agar (MEA) (Remel) at 35°C were made in an attempt to induce ascospore formation. Colonies on MEA became reddish orange and granular to crust-like with a brownish orange reverse (Fig. 1B). Globose, nonostio-late ascomata occurred within 7 days on Czapek Dox agar (Fig. 1D) and contained asci that were approximately 15.6 by 11.7

␮m (Fig. 1E). Ascospores were elliptical, pale yellow, thick walled, approximately 4 to 5 by 6.8␮m, and predominately echinulate by light microscopy (Fig. 1F). Ascospores were sub-sequently examined by scanning electron microscopy (SEM). Briefly, stubs were mounted with Spot-O-Glue Avery labels (Diamond Bar, Calif.) and touched to the fungal culture. Prep-arations were coated with gold-palladium using a Denton Bench Top Turbo III vacuum evaporator (Morristown, N.J.) and were examined with a LEO 435 VP digital scanning electron microscope (Thornwood, N.Y.). When viewed by scanning electron microscope, ascospores appeared irregularly verrucose (Fig. 1G).

Temperature studies were also performed by inoculating five plates of MEA (Remel) in triplicate with a 1-mm portion of the case isolate. Plates were incubated at 18 to 20, 25, 30, 35, and 42°C for 6 days, and zone sizes were measured with cali-pers. Temperature studies performed on day 6 indicated mean colony diameters at 20, 25, 30, 35, and 42°C of 0, 16, 85, 85, and 60 mm, respectively. The most abundant ascocarp formation occurred at 30 and 35°C, while maximum conidial production occurred at 42°C.

Susceptibility studies. The case isolate and theP. variotii

control strain UTHSC 90-459 were evaluated for in vitro

an-TABLE 1. Comparison of features of thermophilic Thermoascus species Feature Characteristics of: T. taitungiacus a T. crustaceus b T. aegyptiacus c T. aurantiacus d Conidiogenesis Phialidic Phialidic Phialidic Phialidic Anamorph P. taitungiacus f P. crustaceus P. aegyptiacus g None or evanescent Paecilomyces -like 9 days growth at: 16°C ⫺⫺ ⫺ ⫺ 20°C ⫺⫹ ⫺ ⫺ 25°C ⫹⫹ ⫹ ⫺ 30°C ⫹⫹ ⫹ ⫺ 35°C ⫹⫹ ⫹ ⫹ 40°C ⫹⫹ ⫹ ⫹ 50°C ⫹⫹ ⫹ ⫹ LM h ascospore texture Predominately echinulate i Finely echinulate Nearly smooth Finely echinulate SEM ascospore texture Irregularly verrucose Finely echinulate Slightly verruculose Very minutely verrucose j a T. taitungiacus K. Y. Chen and Z. C. Chen sp. nov. b T. crustaceus (Apinis and Chesters) Stolk. c T. aegyptiacus Ueda and Udagawa. d T. aurantiacus Miehe. e T. thermophilus (Sopp) von Arx. f Conidia of all Paecilomyces anamorphs were initially cylindrical, later becoming elliptical to subglobose or globose at maturity. g Not all authorities believe this is a distinct species (13). h LM, light microscopy. i Echinulate is defined as having sharply pointed spines, delicately spiny. j Verrucose indicates delicately verrucose. k Verruculose is defined as having small, rounded processes or warts.

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been cited as human etiologic agents include P. variotii, P. lilacinus, P. marquandii, P. viridis, andP. javanicus(13). Ho-mothallic Paecilomyces species are reported by their teleo-morph name,Thermoascus(2, 5, 14, 25, 27, 28). As the name implies, these are thermophilic or at least thermotolerant fungi. Their identification in clinical laboratories is based upon growth characteristics, temperature studies, and the micro-scopic morphology of both the anamorph and teleomorph forms, i.e., conidiogenous cells and conidia in the genus Pae-cilomyces, and ascomata, asci, and ascospores in the genus

Thermoascus. The case isolate was initially identified in San Antonio asT. crustaceusbased upon its yellow-orange to red-dish orange colonies, the Paecilomyces anamorph displaying cylindrical to rectangular-shaped conidia, growth at 25, 30, 35, and 42°C, and nonostiolate, reddish yellow ascomata produc-ing thick-walled, slightly roughened ascospores as viewed by light microscopy. Ascospores measured 6.5 to 8 by 4.5 to 5␮m. However, in preparation for submission of this paper, SEM studies of the ascospores did not match those reported forT. crustaceusin that they were irregularly verrucose (Fig. 1G) rather than finely echinulate. Recently, Chen and Chen (5) reported a new thermophilic species ofThermoascusthat failed to grow at 20°C and produced ascospores that were echinulate by light microscopy but irregularly verrucose by SEM. The irregularly verrucose ascospores in the case isolate matched those described by Chen and Chen (5) forT. taitungiacus. An identification ofT. crustaceuswas eliminated due to the asco-spore morphology and lack of growth at 20°C (5). Other Ther-moascus species excluded from consideration were Thermo-ascus aegyptiacus with slightly verrucose ascospores and no growth at 20°C (27),Thermoascus aurantiacusthat frequently lacks an anamorphic state, has minutely verrucose ascospores, and fails to grow at 30°C (5, 28), andThermoascus thermophilus

with nearly smooth ascospores and aPolypaeciliumanamorph (2). Features of thermophilic Thermoascus species are dis-played in Table 1. The etymology for the species name T. taitungiacuscomes from the region Taitung in Taiwan, where the organism was isolated from field soils (5). The recovery of this organism from Israel broadens the geographic region for this new species.T. taitungiacushas not been previously asso-ciated with human disease.

Laboratory contamination is unlikely in the case presented, asT. taitungiacuswas isolated in pure growth from four differ-ent dialysate fluids over a period of 8 days. Moreover, our patient had clinical and laboratory evidence of CPD-associated peritonitis and considerable morbidity due to a protracted

symptomatic disease course and the development of a hyper-catabolic state. In addition to Tenckhoff catheter removal, he required an extended period of systemic antifungal therapy and parenteral alimentation. Paecilomyces and Thermoascus

species are a rare cause of fungal peritonitis (E. Bibashi, L. Sigler, E. Mitsopoulos, E. Roilides, M. Rinaldi, D. Sutton, D. Tsakiris, and M. Papadimitriou, Abstr. 13th Congr. Int. Soc. Hum. Anim. Mycol., abstr. P142, 1997). The first case was reported in 1990 by Lye (16). Since then only 14 additional cases have been published, 13 of which were identified asP. variotii(1, 3, 6, 8, 12, 15–18, 22). Paecilomyces peritonitis is associated with substantial morbidity. Ten of 14 reported pa-tients had to be removed from CPD and were placed on he-modialysis (1, 6, 8, 12, 16–18); however, no fatalities were associated withPaecilomycesperitonitis. This stands in contrast with the high mortality rate (up to one-third of cases) reported in CPD-related peritonitis due to other fungi (4). The optimal approach for the treatment ofPaecilomycesperitonitis is dif-ficult to derive from the published data. Removal of the Tenck-hoff catheter was the rule in the majority of the patients (1, 3, 6, 8, 12, 16–18); however, the antifungal regimens differed widely among the patients, even within the same center (17). Of note, one patient did not receive any antifungal therapy (18), while another received fluconazole despite the fact that hisPaecilomycesisolate appeared resistant, in vitro, to the drug (8). All eight tested Paecilomycesisolates from the reported cases appeared susceptible, in vitro, to itraconazole (1, 3, 12, 17; Bibashi et al., Abstr. 13th Congr. Int. Soc. Hum. Anim. Mycol.). Eight of nine tested isolates were susceptible to am-photericin B (1, 8, 12, 17, 18, 22; Bibashi et al., Abstr. 13th Congr. Int. Soc. Hum. Anim. Mycol.), five of five to flucytosine (1, 3, 17), and only two of ten to fluconazole (1, 3, 8, 12, 17, 22; Bibashi et al., Abstr. 13th Congr. Int. Soc. Hum. Anim. My-col.).T. taitungiacuscan be added to an enlarging list of op-portunistic filamentous fungi associated with human infection in general and CPD-associated peritonitis in particular. Fur-ther case studies are required to elucidate the clinical course of infection and the optimal treatment strategies.

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Figure

TABLE 1. Comparison of features of thermophilic Thermoascus species

References

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