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Disseminated Trichosporonosis in a Murine Model of Chronic Granulomatous Disease

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Disseminated Trichosporonosis in a Murine Model of Chronic Granulomatous Disease Comparative Medicine Vol 53, No 3 Copyright 2003 June 2003 by the American Association for Laboratory Animal Science Pages 303-308 Disseminated Trichosporonosis in a Murine Model of Chronic Granulomatous Disease Shannon H. Lacy,1 Donald J. Gardner, DVM,1 Leonard C. Olson, DVM,1 Li Ding, MD,2 Steven M. Holland, MD,2 and Mark A. Bryant, DVM1,* Over a period of ten months, five mice submitted to our service (the Pathology Section of the Veterinary Re- sources Program, Office of Research Services at the National Institutes of Health, Bethesda, Md.) were diagnosed with disseminated trichosporonosis. These mice had pyogranulomatous inflammation in multiple organs, includ- ing lung, liver, lymph nodes, salivary gland, and skin. Fungal elements in many of the lesions were identified, using special histochemical stains, and Trichosporon beigelii was obtained by use of culture of specimens at affected sites. This saprophytic fungus has caused disseminated disease in immunosuppressed humans. However, despite widespread use of immunosuppressed rodents in research, to the authors’ knowledge, this organism had not previ- ously been reported to cause spontaneous disseminated disease in laboratory mice. All affected mice had a geneti- cally engineered defect in p47phox, a critical component of the nicotinamide dinucleotide phosphate (NADPH) oxi- dase, the enzyme responsible for generating the phagocyte oxidative burst. These animals are used as a murine model of human chronic granulomatous disease. We discuss the lesions, differential diagnosis, identification of the organism, and the role of NADPH oxidase in protecting against disseminated trichosporonosis. Trichosporon species are ubiquitous soil saprophytes present ism (1, 2, 6, 8, 12, 18, 27, 28). To our knowledge, there have been no in small numbers as normal flora of human skin and gastrointes- published reports of spontaneous disseminated trichosporonosis in tinal mucosa. In immunocompetent human hosts, these yeast- laboratory mice. like fungi can cause a nodular infection of the hair shafts called white piedra (T. beigelii, formerly T. cutaneum [3]), and summer- Case Reports type hypersensitivity pneumonitis (T. asahii [22]). The organism Animals. Between August 2000 and May 2001, disseminated is now emerging as an important opportunist; deep-seated infec- trichosporonosis was diagnosed in five mice at postmortem ex- tions in immunocompromised hosts are reported with increasing amination. There were two female and three male mice, with frequency (14, 18). Disseminated trichosporonosis is characterized age at necropsy ranging from 18 to 68 weeks. All mice were by a wide variety of disease manifestations, including endocarditis C57BL/6Nai-[KO] P47PHOX, a line that is homozygously defi- (4), endophthalmitis (21), brain abscess (25), pneumonia, fever, cient for p47phox (10). The p47phox is a critical component of the fungemia, funguria (24), and high mortality (23, 24). Granulocy- NADPH oxidase, and deficiency of p47phox leads to CGD (10). As topenia is the most commonly recognized risk factor for this in- early as 1997, there was inapparent and undetected genetic con- fection (18). Disseminated trichosporonosis is most commonly tamination of the C57BL/6Nai strain with the C57BL/6IFN-γ reported in patients receiving cytotoxic therapy for hematologic knockout strain. Polymerase chain reaction (PCR) analysis de- malignancy (8), but is also seen in intravenous drug users and termined the presence of one interferon-gamma (IFN-γ) knockout HIV patients. Recipients of organ transplants, prosthetic limbs, allele in three of the five p47phox mice submitted for necropsy. and artificial heart valves are also at increased risk for dissemi- Therefore, all animals were homozygous for p47phox deficiency, nated trichosporonosis (6). The infection has also been reported and three were heterozygous for IFN-γ deficiency. in patients with chronic granulomatous disease (CGD), a he- Care and husbandry. The animal holding room was on a reditary defect in neutrophil function (20). 14/10-h light/dark cycle, with ambient temperature range of 20 Trichosporon spp. are rarely mentioned as animal pathogens. to 23°C. Room air pressure was negative to the corridor, with 15 Trichosporon beigelii was recently reported as a cause of masti- to 30 air exchanges of 100% non-circulated air per hour. The tis in dairy cows (7), and was previously implicated in a case of relative humidity of the air in the animal room was maintained cystitis in a cat (11). Murine models to simulate human dis- between 35 and 55%. The mice were group housed on autoclaved seminated trichosporonosis typically require profound immuno- hardwood bedding in Micro-Isolator™ cages, located on conven- suppression with cyclophosphamide and/or corticosteroids, tional racks. After the animal cages were washed, bedding and followed by intravenous inoculation of large doses of the organ- feed were added, a wire cage top and Micro-Isolator™ top were put on the cages, then the entire cage unit was autoclaved. The Received: 9/24/02. Revision requested: 11/12/02. Accepted: 1/22/03. animals received acidified water within a pH range of 2.8 to 3.0 1Veterinary Pathology Section, Veterinary Resources Program, Office of Research in sterile bottles with added trimethoprim/sulfamethoxazole 2 Services and Laboratory of Host Defenses, National Institutes of Allergy and (7.6 ml/480 ml), and an autoclaved rodent diet (Zeigler Bros., Infectious Diseases, National Institutes of Health, Bethesda, Maryland 20892. *Corresponding author. Inc., Gardners, Pa.) was available ad libitum. Serum samples 303 Vol 53, No 3 Comparative Medicine June 2003 Table 1. Postmortem findings in five mice with disseminated trichosporonosis Animal information Gross findings Histologic findings Culture results ID Accession Sex Age Skin Splenomegaly Lung Lung Hepatitis Lymphadenitis Splenitis Sialoadenitis (wk) Lesion Lesion Lesion f281 MS0007786 F 18 X X, N PG P* S PG* Trichosporon sp. Skin Pyogranuloma f354 MS0103625 M 30 X X, N X NS BP* NS* PG PG* Trichosporon sp. Spleen f283 MS0007035 M 13 X X X PG P* PG* PG* T. beigelii Skin Skin Pyogranuloma e749 MS0105320 F 68 X X PG PL* PG* PG* T. beigelii Lung Pyogranuloma f558 MS0105320 M 28 X X T. beigelii Skin Skin Pyogranuloma X = lesion present; P = pneumonia; PG = pyogranulomatous; N = nodule; BP = bronchopneumonia; NS = necrosuppurative; * = intralesional fungi; PL = pleuropneumonia; S = suppurative; F = female; M = male from sentinel animals in the animal colony were tested quar- arthroconidia along with septate hyphae and yeast-like cells in terly; twice yearly, a full panel of tests was performed, and an the tissue sections are histologic findings consistent with abbreviated panel of tests was performed during the other two trichosporonosis (3). These histologic findings allowed one to quarters. The full panel of serologic tests included evaluation rule out the higher bacteria as the sole cause of the lesions and for the presence of antibodies to: cilia-associated respiratory other organisms were presumptively ruled out on the basis of bacillus, ectromelia virus, epizootic diarrhea of infant mice vi- their morphologic appearance in tissue sections. However, in rus, Theiler’s mouse encephalomyelitis virus, mouse adenovirus, this study, definitive diagnosis of trichosporonosis relied on iso- lymphocytic choriomeningitis, mouse cytomegalovirus, mouse lation of the organism in culture. hepatitis virus, minute virus of mice, Mycoplasma pulmonis, Candida sp. was the principal suspect in the differential diag- parvovirus, polyoma virus, pneumonia virus of mice, reovirus 3, nosis. Candida sp. has caused disseminated infection in and Sendai virus. Results of the serologic tests were negative immunocompromised mice (6, 28), and is frequently falsely diag- during the period of study. The institute’s animal care- and-use nosed in humans with disseminated trichosporonosis (9). Pre- committee approved the animal study protocol. The animal care sumptive differentiation between the two relies on the presence and husbandry practices in the facility were consistent with the of arthroconidia and yeast-like Trichosporon cells that are larger guidelines set forth in the Guide for the Care and Use of Labora- and more pleiomorphic than those of Candida sp. (3). Unlike tory Animals (15). Candida sp., Trichosporon spp. produce arthroconidia by fragmen- Postmortem findings. A summary of the postmortem find- tation of the septate hyphae. However, these are often not seen in ings is provided in Table 1. All five mice were submitted alive; tissue, leaving yeast-like and hyphal elements similar to those of one died prior to examination. The other four mice were hu- Candida sp. Direct immunofluorescent testing and culturing are manely euthanized in a carbon dioxide gas chamber. On gross valuable tools for differentiating the two organisms (9). In addi- examination, four mice had ulcerated, purulent skin lesions tion, a nested PCR assay has recently been developed to achieve about the ventral aspect of the neck. Lung lesions were seen early and accurate diagnosis of disseminated trichosporonosis (23). grossly in three of the mice; one mouse had pleural adhesions Aspergillus spp. are ubiquitous saprophytes that cause oppor- and a soft white exudate within the pulmonary parenchyma, tunistic infections in immunocompromised hosts. In a national and the other two had multifocal-to-coalescing, tan-gray consoli- registry of human patients with chronic granulomatous disease, dated areas
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