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Case History: One juvenile European Starling (Sturnus vulgaris) was admitted to a rehabilitation center in the District of Columbia in August 2021. The bird presented with bilateral periocular and third eyelid swelling. No neurological signs were noted on the intake examination. The bird was euthanized the same day, and it was submitted for necropsy examination and diagnostic testing.

Gross Findings: A juvenile male European Starling in good postmortem condition is examined at necropsy. The bird is in fair nutritional condition with scant subcutaneous and epicardial fat stores. The right eye has mild conjunctival swelling, especially of the dorsal conjunctiva. There is mild reddening of the right dorsal conjunctiva and dorsal eyelid. There is a 5 x 3 mm patch of missing feathers above the eye. The left eye has marked swelling of the conjunctiva, especially dorsomedial to the eye. There is moderate reddening of the conjunctiva and eyelids. Internally, the crop and stomach are empty, and the intestines contain a small amount of soft, tan digesta. The cloaca contains a small amount of urates and feces. The bursa of Fabricius and thymus are small. Gonad is identified as testis histologically. All tissues not described are within normal limits.

Histopathological Findings: There is a region of abundant perivascular and moderate random acute hemorrhages present in the brain (Fig. 1A). There is a regionally extensive area in the brain within which are multifocal infiltrates of heterophils, glial cells, macrophages, and multinucleated giant cells effacing the neuropil (Fig. 2B). Scattered within the affected area are poorly staining to light brown pigmented fungal hyphae with thin, parallel walls, acute angle branching, and rare septations (Fig. 2C). Special staining with Grocott methenamine silver (GMS) highlights many fungal hyphae throughout the brain (Fig. 2D). In a cross section of the head, there is abundant acute hemorrhage in the orbit surrounding both eyes. The lower conjunctiva of one eye has a small focus of fibrin and a cluster of degenerate cells replacing the epithelium, and there are a small number of lymphocytes and plasma cells in the upper eyelid. The upper conjunctiva of the opposite eye is infiltrated by a moderate number of lymphocytes and plasma cells. Other microscopic findings include moderate atrophy of mesenteric adipose tissue, segmental cartilaginous and osseous metaplasia of a great vessel of the heart, minimal brown pigment accumulation in hepatocytes (hemosiderin), and a few nematodes in the lumen of the duodenum.

Photomicrographs from a European Starling brain.
Figure 1. Photomicrographs from a European Starling (Sturnus vulgaris) that was euthanized in the District of Columbia, USA. (A) There is an area in the brain with abundant acute hemorrhage (H) surrounding blood vessels and in the neuropil. H&E stain. (B) There are multifocal infiltrates in the neuropil of inflammatory cells (arrows) and rare multinucleated giant cells (arrowhead). H&E stain. (C) Inflammatory infiltrates consist of heterophils, macrophages, and glial cells. Admixed with the inflammation are poorly staining to light brown fungal hyphae (arrows). H&E stain. (D) Many fungal hyphae with parallel walls and acute angle branching (arrow) are highlighted by GMS staining.

Ancillary Tests: Fungal culture and internal transcribed spacer (ITS) sequencing identified the fungus as Verruconis gallopava. A sample of eyelid was PCR positive for Mycoplasma and Mycoplasma sturni was identified by 16S sequencing; this is likely an incidental finding causing the mild changes in the conjunctiva and eyelid. Tracheal and cloacal swabs were negative for avian influenza by matrix RT-PCR.

Morphologic Diagnoses:

  1. Brain: Marked regionally extensive heterophilic and granulomatous encephalitis with multifocal acute hemorrhages and intralesional pigmented fungal hyphae (Verruconis gallopava)
  2. Head: Severe acute bilateral retrobulbar hemorrhage (suspect trauma)
  3. Head: Mild bilateral multifocal fibrinous to lymphoplasmacytic conjunctivitis and mild unilateral lymphoplasmacytic blepharitis and dermatitis (Mycoplasma sturni positive)

Disease: Ochroconosis

Etiology: Ochroconosis is a sporadic fungal encephalitis of birds caused by the dematiaceous (pigmented), thermophilic (heat loving) fungus Ochroconis gallopava (Dactylaria gallopava). Based on genome analysis, this organism has recently been assigned its own genus and renamed Verruconis gallopava.

Distribution: Worldwide. Ochroconis prefers acidic environments with moderately high temperatures, such as decaying vegetation, hot springs, contaminated litter, and egg incubators.

Host range: This disease is well characterized in young domestic poultry. Infection in non-domestic avian species is sporadic and include reports in Gray-winged Trumpeters (Psophia crepitans), Snowy Owls (Nyctea scandiaca), Japanese Quail (Coturnix japonica) chicks, and Elegant Crested Tinamou (Eudromia elegans) chicks.  

Transmission: Inhalation of fungal spores from a contaminated environment is suspected to be a common route of exposure.

Clinical signs: O. gallopava appears to have a distinct tropism for the central nervous system. Neurologic signs commonly seen with ochroconosis include ataxia, tremors, torticollis (head tilt), limb paralysis, opisthotonos, and death.

Pathology: Gross lesions may be seen in the cerebellum or cerebrum as focally extensive, circumscribed, firm areas of gray, red, or cream-colored discoloration; however, external examination of the brain may be unremarkable. Occasionally pulmonary granulomas may be present. Microscopically, the brain lesions consist of multiple areas of necrosis infiltrated with many heterophils, macrophages, and multinucleated giant cells. Associated with the inflammation are thin pigmented fungal hyphae that are poorly staining or yellow to light brown, rarely septate, and have irregular acute angle branching. Special stains such as Grocott methenamine silver (GMS) will highlight the extensive number of hyphae present.

Diagnosis: The microscopic inflammatory lesions in the brain with characteristic pigmented fungal hyphae can be used for a presumptive diagnosis. Fungal culture and identification are needed for a definitive diagnosis.

Public health concerns: Ochroconosis is not considered to be zoonotic, though infections are reported in people, especially immunosuppressed transplant patients.

Wildlife population impacts: Given the sporadic reports, the overall impact of ochroconosis in wild populations of birds is likely low. Ochroconosis should be considered in captive wild birds housed in warm, moist, acidic environments.

Management: Especially in poultry operations, removal of contaminated environmental sources (such as litter) and decontamination of egg incubators by fumigation is recommended to prevent morbidity and mortality.

References:

  • Arné P and Lee MD. 2019. Fungal Infections.  In: Diseases of Poultry. Swayne DE, Boulianne M, Logue CM, McDougald LR, Nair V, Suarez DL, de Wit S, Grimes T, Johnson D, Kromm M, Prajitno TY, Rubinoff I, Zavala G, editors. Wiley-Blackwell, New Jersey, pp. 1127-1128.
  • Ossiboff RJ, Clancy MM, Terio KA, Conley KJ, McAloose D. 2015. Cerebral and ocular Ochroconiasis in 2 Elegant Crested Tinamou (Eudromia elegans) chicks. Veterinary Pathology 52(4):716-719.
  • Samerpitak K, Van der Linde E, Choi H‐J, Gerrits van den Ende AHG, Machouart M, Gueidan C and de Hoog GS. 2014. Taxonomy of Ochroconis, genus including opportunistic pathogens on humans and animals. Fungal Diversity 65:89–126.

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