Pathology Case of the Month - Black Racer Snake

By National Wildlife Health Center October 31, 2019

History: In May 2015, a Black Racer snake (Coluber constrictor priapus) with obvious multifocal cutaneous sores was observed at a basking site in Dutchess County, New York. One week later, the snake was found freshly deceased.

Other snakes, such as Eastern Ratsnakes (Pantherophis alleghaniensis), Common Garter snakes (Thamnophis sirtalis), and Timber Rattlesnakes (Crotalus horridus) at this site also showed signs of necrotizing skin lesions.

Gross Findings: Over much of the body, the epidermis is sloughing. Neck, dorsum, and tail have multifocal to coalescing dull to grayish-tan foci on the epidermis. On the head and upper body, the dorsal skin is diffusely light tan, rough and thickened (Figure 1). On the ventral skin are multifocal coalescing, up to 8 mm dull white or grey foci with occasional central indentation. On internal examination, no subcutaneous or visceral fat is present. Internal organs were grossly unremarkable.

Photos of a black racer snake with snake fungal disease on head and body. — Figure 1: Black Racer snake (A) The epidermis over much of the body, but cranially pronounced, has multifocal to coalescing dull white to pale gray foci. (B) Multiple scales around the head are thickened and roughened. (C) Ventrally, there are multiple dull white to grey foci of up to 8 mm size, occasionally with central indentations. (Credit: Saskia Keller, National Wildlife Health Center. Public domain.)

Histopathological Findings: Multifocally, the epidermis is ulcerated and replaced by thick serocellular crusts which contain myriad up to 5 µm wide, parallel walled, occasionally septate, and branching fungal hyphae (Fig. 2A, C, E). Numerous heterophils and lesser numbers of macrophages infiltrate the underlying dermis and occasionally the musculature as well (Fig. 2A). The older generation of epidermis remains attached to the newer generation through necrotic debris (dysecdysis), whereas fungal hyphae can be detected in the β-layers of the outer and inner generation as well as occasionally infiltrating the α-layer and stratum germinativum (Fig. 2B). Typical rectangular arthroconidia are often found at the air-lesion interface (Fig. 2D).

Photos of histology of snake fungal disease lesions in purple and white. — Figure 2: (A) Underneath the β-layer of the epidermis is an accumulation of hypereosinophilic necrotic debris. The remaining epidermis is extensively ulcerated. Heterophils and macrophages infiltrate the underlying dermis. Skin, PAS. (B) Necrotic debris is found above the β-layer of the outer generation (BO) and between the BO and the β-layer of inner generation (BI). Fungal hyphae are widespread within the necrotic debris but are also found infiltrating the BI and within the mesos layer (ML, arrow head). Skin AS. (C) Arthroconidia (asterisk) are found superficially and myriad fungal hyphae (arrows) infiltrate the necrotic debris. Skin, PAS (D) Rectangular 2 x 5 µm arthroconidia (asterisk) are often found on the air-lesion interface (asterisk). Skin, PAS. (D). PAS-positive fungal hyphae (arrow) are parallel walled, of up to 5 µm in width and exhibit occasional septations and non-dichotomous branching. Skin, PAS. (β-Layer of outer generation (BO), β-Layer of inner generation (BI), ML Mesos layer (ML), α-layer (AL), Stratum germinativum (SG) (Credit: Saskia Keller, National Wildlife Health Center. Public domain.)

Morphologic Diagnosis/es: Necroulcerative dermatitis, severe, subacute, multifocal to coalescing with dysecdysis and intralesional fungal hyphae and arthroconidia

Disease: Snake fungal disease (SFD)

Etiology: Ophidiomyces ophiodiicola (OO), keratinophilic ascomycete fungus.

Clinical signs: Increased shedding of the skin or dysecdysis is common in infected snakes. Also, abnormal behavior, such as increased basking time are often observed, since higher temperature seem to slow fungal growth.

Gross findings: Skin lesions can be widespread and start with swelling and increased pallor and dullness of scales. Later they become thickened and yellow before progressing to rough brown crusts. If lesions are present on the head, infections can lead to severe facial and oral disfigurations due to subepidermal infiltrates and granulomas.

Diagnosis: Confirmation of SFD requires a combination of histopathology and detection of OO (either by culture or molecular analysis such as PCR or DNA sequencing) to avoid confusion with other concurrent saprophytic or opportunistic pathogens.

Distribution: Snake Fungal Disease can be found in wild snakes of the eastern and midwestern United States and Canada. A new fungal clade, reported from wild snakes of Europe, grows slower and is commonly associated with milder lesions. In captive snakes, the fungus has been reported globally.

Host range: As the name suggest, SFD affects only snakes, mainly crotalids (Rattlesnakes) and sympatric colubrids (i.e. Rat Snakes, Milk Snakes, Water Snakes).

Pathogenesis: Transmission and pathogenesis remains poorly understood. It is assumed that Ophidiomyces ophiodiicola (OO) is present within the environment. It can also be found on skin of snakes without clinical signs of SFD, but OO is not reported as a common constituent of the normal snake skin mycobiota. Skin abrasion seems to predispose the snake to fungal invasion, but infections have been known to occur in their absence. With deeper invasion of the fungus, extensive inflammation and granuloma development can lead to facial deformities, interfering with food uptake and decreasing the general fitness. Systemic spread is rare.

Public health concerns: None.

Wildlife population impacts: The significance of SFD in free-ranging snakes is currently under investigation. After 2008, increased numbers of snake with SFD have been reported, raising concern about SFD and its potential impacts on some snake populations.

Management: When SFD is already known to occur in a region, snakes whose skin lesions appear to resolve with supportive care and/or antifungal therapy may be candidates for release at their capture site, but these individuals should not be released in an area where the disease has not been previously documented as it is not known if treated snakes may still harbor viable fungus.

References:

Franklinos LH, Lorch JM, Bohuski E, Fernandez JR, Wright ON, Fitzpatrick L, Petrovan S, Durrant C, Linton C, Baláž V, Cunningham AA. 2017. Emerging fungal pathogen Ophidiomyces ophiodiicola in wild European snakes. Scientific reports 7:3844.

Lorch JM, Lankton JS, Werner K, Falendysz EA, McCurley K, Blehert DS. 2015. Experimental infection of snakes with Ophidiomyces ophiodiicola causes pathological changes that typify snake fungal disease. MBio 6, 1-9.

Lorch JM, Knowles S, Lankton JS, Michell K, Edwards JL, Kapfer JM, Staffen RA, Wild ER, Schmidt KZ, Ballmann AE, Blodgett D, Farrell TM, Glorioso BM, Last LA, Price SJ, Schuler KL, Smith CE, Wellehan JFX, Bleher DS. 2016. Snake fungal disease: an emerging threat to wild snakes. Phil Trans R Soc B 371:20150547.

Joint Pathology Center, Veterinary Pathology Services. 2018. Wednesday Slide Conference 2018-2019, Conference 8, Case 4. www.askjpc.org/wsco/wscarchives.php. Accessed October 2019.

Ossiboff RJ. 2018. Serpentes. In: Pathology of Wildlife and Zoo Animals, Terio KA, McAloose D, St. Leger J, editors. Academic Press, pp. 897-919.