Adult, female and male, thirteen-lined ground squirrels (Spermophilus tridecemlineatus)Selected tissue samples were collected from approximately fifty wild rodents as part of a plague surveillance project in Colorado during a plague outbreak in prairie dogs in July 2006. The animals were humanely trapped, euthanized, and selected fresh tissue samples were collected for PCR, ECL, microbial culture, histopathology, and immunohistochemistry.
No gross lesions were observed during necropsy
Scattered throughout all lung lobes are coalescing pyogranulomas that disrupt and efface up to 20% of alveolar septae and bronchioles.Â The pygranulomas (Fig 4-1) are up to 1mm in diameter and are centered upon an adiaspore which is surrounded by degenerate and nondegenerate neutrophils, epithelioid macrophages, and foreign body and Langhans multinucleate giant cells in varying proportion.Â Lymphocytes and plasma cells are rare.Â The inflammatory cells extend into and expand adjacent alveolar septae.Â The adiaspores are round, up to 250 micrometer in diameter with a 20-30 Î¼m thick refractile non-staining cell wall (Fig.Â 4-2).Â The center contains amophophilic globular material.Â The cell wall stains dark purple with the Periodic Acid-Schiff (PAS) stain (fig.Â 4-3) and black with Grocotts Methenamine Silver (GMS) (Fig.Â 4-4) .
Lung: Bronchopneumonia, pyogranulomatous, multifocal, mild, with fungal conidia (adiaspores), etiology consistent with Chrysosporium parvum (adiaspiromycosis).
Immunonegative for Yersinia pestis
Adiaspiromycosis is primarily a pulmonary fungal infection of small animals.1 Infection occurs when the conidia (spores) are inhaled.1 The name, adiaspore, refers to a spore that grows in size without replicating in tissues.2 Therefore, the degree of infection is determined by the number of spores inhaled.Â The inhaled conidia simply enlarge in the lung tissue and are eventually removed by the immune system; thus, the disease is not contagious.Â 1,3 The most susceptible animals are those that live in close contact with soil that contains the saprophytic stage of the fungus, such as burrowing rodents.1
Two varieties of the fungal genus Chrysosporium, formerly known as Emmonsia, cause adiaspiromyosis: C.Â parvum var.Â parvum and C.Â parvum var.Â crescens.Â The latter has the widest host range and distribution.Â 1 C.Â parvum var.Â crescens is a dimorphic fungus with spores that are 2-4Î¼m in the environment.Â They enlarge to 200-400Î¼m when inhaled and incubated at body temperature.Â At lower temperature (20-30oC) the spores will develop into a mycelial form.3
The typical pathologic feature of the infection is the granuloma or pyogranuloma which appear grossly as gray white nodules in the lungs.1 The lung is the only organ known to be infected.4 Histologically, these nodules contain a central adiaspore surrounded by varying degrees granulomatous to pyogranulomatous inflammation.Â Ruptured spores incite the most severe reactions.1 Adiaspores range from 200-400Î¼m in diameter for C.Â parvum var.Â crescens and 20-40Î¼m C.Â parvum var.Â parvum.2 C.Â parvum var.Â crescens has a characteristic thick cell wall that is up to 70Î¼m thick.3 The center of the adiaspore contains a mass of amphophilic to basophilic small globules.2 There is a single nucleus in spores of C.Â parvum var.Â parvum, however C.Â parvum var.Â crescens develops multiple nuclei as it enlarges.2 There is no budding or endosporulation.1
Differential diagnosis includes other fungi of similar size and morphology, such as Coccidioides immitis and Rhinosporidium seeberi.Â Morphologically, C.Â parvum (20-70Î¼m) has a thick capsule while C.Â immitis (12Î¼m) and R.Â seeberi (35Î¼m) have relatively thin capsules.3 The presence of endospores occurs with C.immitis and R.Â seeberi, but not C.Â parvum.3 C.Â parvum infection does not produce hyphae, unlike C.Â immitis. 3 Histochemically, the capsules of all three stain with PAS and GMS.3 The capsule of R.Â seeberi also stains with mucicarmine, unlike the other two.3
The infection has been reported in mice, moles, rats, rabbits, ground squirrels, weasels, martens, minks, armadillos, wallabies, skunks, opossums, dogs, cats, raccoons, and humans.4
The disease in immunocompetent animals (including humans) is typically benign, self-limiting, and confined to the lungs.Â However, clinical signs can occur with heavy infections.1 Most infections are considered incidental findings during the course of histopathologic evaluation of the lungs as in these ground squirrels.Â
Of the 20 ground squirrels examined during this study, adiaspiromycosis was detected in 13 of them (60.5%).Â Interestingly, only 1 of 18 (5.1%) prairie dogs in this study was infected.Â The reasons that two species of burrowing rodents from the same geographical area had such different prevalences of infection were not determined.Â
1.Â Lung: Pneumonia, pyogranulomatous, multifocal, moderate with fungal conidia, thirteen-lined ground squirrels (Spermophilus tridecemlineatus), rodent.
2.Â Kidney: Essentially normal tissue.
Adiaspiromycosis caused by the dimorphic fungi Emmonsia parva (=Chrysosporium parvum var.Â parvum) or Emmonsia crescens (=C.Â parvum var.Â crescens) is a rare mycotic condition in small mammals and humans worldwide.Â In the literature, the names Emmonsia and Chrysosporium are considered synonyms with significant controversy occurring concerning their appropriate use.Â In 1962, Charmichael reclassified Emmonsia as a Chrysosporium and reduced the two species to a variety of E.Â parva.9,10 This was later refuted by von Arx who retained Emmonsia as a single species with two varieties based on the reasoning that Emmonsia produces blastic conidia and adiaspores, and Chrysosporium produces thallic conidia and no adiaspore at elevated temperature.9,10 To confuse taxonomic matters further, it has recently been found that E.Â parva is phylogenetically closer to Blastomyces dermatitidis (the anamorph of Ajellomyces dermatitidis) than it is to Emmonsia crescens.7 At this time, both genera names continue to be used in the literature.
Inhaled dust-borne aleurioconidia (2-4 um) do not germinate in the host, but instead dramatically enlarge into thick-walled adiaspores.Â Clinically, infection may range from asymptomatic to severe necrogranulomatous pneumonia depending on adiaspore load and immunocompetence of the host.5 Infection is not considered transmissible between individuals.7,8
1.Â Burek K: Bacterial and mycotic diseases.Â In: Infectious Diseases of Wild Animals.Â 3rd ed., pp 522-523, London, Manson Publishing, 2001
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3.Â Chandler FW, Kalpan W, Ajello L: Adiaspiromycosis.Â In: Color Atlas and Text of the Histopathology of Mycotic Diseases, pp.Â 3033.Â Year Book Medical Publishers, Chicago, IL, 1980
4.Â Chandler FW, Watts JC: Adiaspiromycosis.Â In: Pathologic Diagnosis of Fungal Infections, pp.Â 3541.Â ASCP Press, Chicago, IL, 1987
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6.Â Hamir AN: Pulmonary adiaspiromycosis in raccoons (Procyon lotor) from Oregon.Â J Vet Diagn Invest 11:565567, 1999
7.Â Hub+ï¿½-ï¿½lek Z, Burda H, Scharff A, Heth G, Nevo E, _umbera R, Pe_ko J, Zima J: Emmonsiosis of subterranean rodents (Bathyergidae, Spalacidae) in Africa and Israel.Â Med Mycol 43:691-697, 2005
8.Â Hub+ï¿½-ï¿½lek Z: Emmonsiosis of wild rodents and insectivores in Czechland.Â J Wild Dis 35:243-249, 1999
9.Â Kwon-Chung KJ, Bennett JE: Infections due to miscellaneous molds.Â In: Medical Mycology, pp.Â 733-739.Â Lea & Febiger, Philadelphia, PA, 1992
10.Â Sigler L: Ajellomyces crescens sp.Â nov., taxonomy of Emmonsia spp., and relatedness with Blastomyces dermatitidis (telomorph Ajellomyces dermatitidis).Â J Med Vet Mycol 34:303-314, 1996
11.Â Sun Y, Bhuiya T, Wasil T, Macias A, Wasserman PG: Fine needle aspiration of pulmonary adiaspiromycosis.Â Acta Cytol 51:217-221, 2007