CASE IV: S884/20 (JPC 4166939)



Adult, male raccoon (Procyon lotor)



The animal was shot due to central nervous signs and submitted for necropsy to clarify the cause of disease.


Gross Pathology:

At necropsy, the animal was in a moderate nutritional status. In addition to a hemaskos and generalized swollen lymph nodes, the lungs exhibited multifocal greyish nodular lesions up to 3 mm in diameter that are slightly raised above the pulmonary surface. The liver had slightly rounded edges and a firm consistency. The spleen was slightly swollen. The stomach was empty.


Laboratory Results:

Fungal structures were identified as Emmonsia crescens using qPCR (target ITS-2/28s). Using Immunofluorescence, canine distemper virus antigen was found in the lung, urinary bladder, spleen and brain. Immunohistochemistry of the lung revealed low to moderate numbers of CDV antigen-containing bronchial and bronchiolar epithelial cells, peribronchial glandular epithelial cells, interstitial cells, and typ II-pneumocytes. Using antibodies against CD3 and CD20, low numbers of T- and B- lymphocytes were seen in the pulmonary interstitium. In addition, CD204-expressing macrophages were found immunohistochemically in low numbers in the pulmonary interstitium and in moderate numbers in fungal-associated granulomas. Moreover, Staphylococcus spp. was isolated via bacterial culture of lung tissue.


Microscopic Description:

In the lung, affecting about 60% of the tissue, there is a multifocal loss of parenchymatous architecture by concentrically arranged granulomas. Granulomas measure up to 500 µm in diameter and often show a central, fungal adiaspore. These fungal structures have a diameter of up to 150 µm and a thick (up to 8 µm), round, eosinophilic to non-dyeable, non-birefringent cell wall and contain finely stippled, amphophilic material. The adiaspore cell wall stains purple with the Periodic Acid-Schiff (PAS) reaction and black with Grocott´s methenamine silver method. The fungal elements are embedded into low to moderate amounts of cellular debris that is surrounded by several layers of epitheloid macrophages and eosinophils as well as low numbers of lymphocytes and plasma cells. Occasionally, multinucleated giant cells of foreign body type are present in the granulomatous wall.


Additionally, the remaining alveolar septae are diffusely, mildly thickened by an infiltration of mostly macrophages and lymphocytes. Multifocally, there is a mild hyperplasia of type II pneumocytes. Furthermore, bronchial and bronchiolar epithelial cells are slightly hypertrophic and infrequently contain small, cytoplasmic, eosinophilic inclusion bodies.


Contributor's Morphologic Diagnoses:

Lung, pneumonia, granulomatous and eosinophilic, severe, chronic, multifocal, with intralesional fungal conidia (adiaspores) and pneumonia, broncho-interstitial, lymphohistiocytic, mild, subacute, diffuse with eosinophilic, cytoplasmic inclusion bodies in bronchial epithelial cells.


Contributor's Comment:

Fungal infections are most commonly seen in animals that are immunocompromised due to infections, malnutrition, stress or various other reasons. Therefore, the respiratory tract is predisposed due to the direct contact with the environment. In the presented case, the morphological changes in the lung with granuloma formation together with the described intralesional fungal elements match the histological characteristics of an adiaspiromycosis. This fungal infection is reported from different continents (e.g. Europe, Northern America and Africa) and occurs in various mammals, including humans, otters, beavers, deer, rabbits and rodents. Inhalation of conidia leads to granulomatous or pyogranulomatous pneumonia with or without inflammatory involvement of the local lymph nodes.1,7,10,12 Inhaled conidia enlarge and form nonreplicating adiaspores.1 The underlying dimorphic fungus Emmonsia spp. is closely related to Blastomyces spp. and has two important pathogenic subspecies. In Europe, E. crescens characterized by adiaspores measuring up to 500 µm in diameter is more frequently found than E. parva, which forms smaller seized spores of up to 40 µm in diameter.3, 5 The latter is more commonly seen in xerothermic regions like Africa, Asia and partially America.3,5 Pathological findings are granulomatous to pyogranulomatous pneumonia, as the infection is restricted to the lower respiratory tract.3,7,10


As a differential diagnosis, coccidioidomycosis due to infection with Coccidioides spp. is also characterized by (pyo-) granulomas up to 200 µm in diameter and fungal spherules, which contain numerous, 2-5 µm seized endospores.5


Moreover, the observed, bronchointerstitial pneumonia in association with the presence of eosinophilic, cytoplasmic inclusion bodies suggests an infection with canine distemper virus (CDV). This viral infection was confirmed by both, immunohistochemistry and immunofluorescence. CDV-antigen was observed in various cell types in the lung as well as in the brain, spleen and urinary bladder of the raccoon. CDV, a pantropic morbillivirus of the family Paramyxoviridae, can infect a wide range of terrestric carnivores and marine mammals and leads to various forms of disease.2 Pathological findings include bronchointerstitial pneumonia, gastroenteritis, demyelinating encephalomyelitis, chorioretinitis, hyperkeratosis (hard pad disease), metaphyseal bone lesions and enamel hypoplasia.6 Furthermore, CDV compromises the immune response of the affected host by infecting lymphocytes leading to severe lymphocytolysis.4,13 The concomitant immunosuppression represents a predisposing factor for various secondary infections including viral, bacterial, fungal or parasitic infections. In the present case, the CDV infection is considered more likely as a secondary event superimposed on the adiaspiromycosis, because the fully developed fungal granulomas represent more chronic lesions. However, the CDV infection represents the most probable cause of the central nervous signs of the animal.


Contributing Institution:

Department of Pathology

University of Veterinary Medicine Hannover

Buenteweg 17

D-30559 Hannover


JPC Diagnosis:

1.     Lung: Pneumonia, eosinophilic and granulomatous, multifocal, severe, with numerous adiaspores.

2.     Lung: Pneumonia, interstitial, histiocytic, diffuse, moderate, with rare cytoplasmic viral inclusions.


JPC Comment:

The contributor provides a succinct and insightful summary of Emmonsia parva and E. crescens. These dimorphic fungi cause adiaspiromycosis, a disease that primarily affects rodents but is also rarely reported in other species and humans. In addition, the contributor provides a concise review of canine distemper virus (CDV), a morbillivirus capable of infecting multiple domestic and wildlife species, including a recent report14 describing CDV infections in multiple 2-toed sloths (Choloepus didactylus). As noted by the contributor, CDV infection is commonly associated with clinical signs involving the respiratory, gastrointestinal, integumentary, and central nervous systems. Furthermore, this entity was previously discussed at length during 21-22 WSC 5, Case 2.


Emmonsia spp. bear the name of Dr. Chester Wilson Emmons, an internationally recognized 'founding father' of medical mycology in the United States. After receiving his Ph.D from Columbia University in 1931, Dr. Emmons began his long and storied career by collecting, observing, and classifying dermatophytes based on their spores and accessory organs, resulting in redefining genera Trichophyton, Microsporum and Epidermophyton based on mycological terms and the elimination chaotic pre-existing taxonomic nomenclature. Dr. Emmons later collaborated with Dr. Carrion at the School of Tropical Medicine at the University of Puerto Rico and unequivocally confirmed Actinomyces bovis is a normal commensal of the human mouth in 1935. He was recruited the following year as the first medical mycologist at the National Institutes of Health (NIH) in an attempt by the institution to expand its investigative and surveillance capabilities in regard to infectious diseases in the United States. During his tenure, Dr. Emmons devoted his professional career toward the development of the medical community's recognition of saprophytic organisms as being significant causes of disease, an underappreciated concept at the time. Examples of these efforts include overseeing the discovery of coccidiomycois in rodents in the desert southwest of the United States, original research in establishing the importance of histoplasmosis, the initial isolations of Histoplasma capsulatum and Cryptococcus neoformans from their natural habits, the isolation and identification of new agents of fungal diseases (such as Emmonsia spp.), and assisting in the development of the antifungal medication amphotericin B. Dr. Emmons retired from the National Institutes of Allergy and Infectious Diseases (NIAID), NIH as the head of the medical mycology division three decades later in 1966. Retirement did not suite Dr. Emmons, as he was later appointed as a faculty member of Arizona State University from 1973-1977, where he lectured, continued writing, and searched for C. immitis in the soil, amongst other academic endeavors.11


Emmons and Jellison first described Emmonsia crescens in a 1960 report in which they reclassified Haplosporangium parvum to Emmsonsia parvum; E. crescens was then segregated on the basis of its greater size in the adiaspore form. At the time, Emmonsia parva's known range was the arid southwestern United States whereas E. crescens had been identified throughout North, Central, and South America, Europe, and Asia. Interestingly, the etiology previously known as H. parvum had not identified until 1942 to the puzzlement of Emmons and Jellison, who commented how it seemed "improbable that a fungus that so frequently invades the lungs of rodents to have escaped the notice of mammalogists and mycologists until 1942." The same report describes Jellison identifying the fungus in preserved lung tissue from a rodent (Microtus agrestis) trapped in Sweden in 1845.8


Since Emmons and Jellison's 1960 report, adiaspiromycosis has been identified in over 118 species of mammals with a global distribution and is common in both rodents and small terrestrial mammals. For example, a 2009 report found nearly a third of native British mammals to be infected with E. crescens. Humans may also be infected, with the first human case of adiaspiromycosis reported in 1964 and subsequent cases reported worldwide. Both E. crescens and E. parava may result in human infections, with the former being more commonly implicated.15


The term "adiaspiromycosis" itself is derived from the characteristically large adiaspores that arise following marked enlargement of inhaled infective conidia. The term "adiaspore" is in reference to the fact these structures neither replicate nor disseminate from their original site of implantation, for which Emmons and Jellison coined the term from Greek α? (not, without), ?δια? (by, through), and ?σπορα (seed, sowing).8,15 Thus, the severity of disease is determined by the inoculum size and the host's response, which may range from subclinical pneumonia to diffuse pulmonary disease and death.15


As noted by the contributor, Emmonsia's large size and thick PAS-positive wall histologically resemble Coccidioides spp., as well as the mesomycetozoan parasite Rhinosporidium seeberi. However, in contrast the latter two organisms, endosporulation is not a feature of Emmonsia spp.5


The moderator emphasized the diffuse atelectasis in this case, noting the dilated patent alveolar ducts on a background of collapsed alveoli.


Conference participants noted considerable slide variability in regard to intracytoplasmic and intranuclear viral inclusions which made the diagnosis of canine distemper a challenging feature in this case.



  1. Anstead GM, Sutton DA, Graybill JR. Adiaspiromycosis causing respiratory failure and a review of human infections due to Emmonsia and Chrysosporium spp. J Clin Microbiol. 2012;50(4):1346-1354.
  2. Beineke A, Baumgärtner W, Wohlsein P. Cross-species transmission of canine distemper virus-an update. One Health. 2015;1:49-59.
  3. Borman AM, Simpson VR, Palmer MD, Linton CJ, Johnson EM. Adiaspiromycosis due to Emmonsia crescens is widespread in native British mammals. Mycopathologia. 2009;168(4):153-163.
  4. Carvalho OV, Botelho CV, Ferreira CG, et al. Immunopathogenic and neurological mechanisms of canine distemper virus. Adv Virol. 2012;2012:163860.
  5. Caswell JL, Williams KJ. Respiratory system. In: Maxie G, ed. Jubb, Kennedy and Palmer`s Pathology of Domestic Animals. 6th ed. Vol. 2. St. Louis: Elsevier, 2016:583?585.
  6. Deem SL, Spelman LH, Yates RA, Montali RJ. Canine distemper in terrestrial carnivores: a review. J Zoo Wildl Med. 2000;31(4):441-451.
  7. Dolka I, Giżejewska A, Giżejewski Z, Kołodziejska-Lesisz J, Kluciński W. Pulmonary adiaspiromycosis in the Eurasian beaver (Castor fiber) inhabiting Poland. Pol J Vet Sci. 2017;20(3):615-617.
  8. Emmons CW, Jellison WL. Emmonsia crescens sp. n. and adiaspiromycosis (haplomycosis) in mammals. Ann N Y Acad Sci. 1960;89:91-101.
  9. Hamir AN. Pulmonary adiaspiromycosis in raccoons (Procyon lotor) from Oregon. J Vet Diagn Invest. 1999;11(6):565-567.
  10. Hughes K, Borman AM. Adiaspiromycosis in a wild European rabbit, and a review of the literature. J Vet Diagn Invest. 2018;30(4):614-618.
  11. Kwon-Chung KJ, Campbell CC. Chester Wilson Emmons. J Med Vet Mycol. 1986;24(1):89-90.
  12. Matsuda K, Niki H, Yukawa A, et al. First detection of adiaspiromycosis in the lungs of a deer. J Vet Med Sci. 2015;77(8):981-983.
  13. Schobesberger M, Summerfield A, Doherr MG, Zurbriggen A, Griot C. Canine distemper virus-induced depletion of uninfected lymphocytes is associated with apoptosis. Vet Immunol Immunopathol. 2005;104(1-2):33-44.
  14. Schwartz IS, Kenyon C, Feng P, et al. 50 Years of Emmonsia Disease in Humans: The Dramatic Emergence of a Cluster of Novel Fungal Pathogens. PLoS Pathog. 2015;11(11):e1005198.
  15. Watson AM, Cushing AC, Sheldon JD, et al. Natural Canine Distemper Virus Infection in Linnaeus's 2-Toed Sloths (Choloepus didactylus). Vet Pathol. 2020;57(2):311-315.


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