JPC SYSTEMIC PATHOLOGY

INTEGUMENTARY SYSTEM

November 2022

I-P18

 

Signalment (JPC# 2416085):  Adult female African clawed frog (Xenopus laevis)

 

HISTORY:  This frog was submitted for necropsy.  The frog had become thin and lethargic and had an area of brown discoloration on its dorsum.

 

MICROSCOPIC DESCRIPTION:  Skin: The epidermis is diffusely thickened up to four times normal with acanthosis and spongiosis. Multifocally within the epidermis there are numerous adult aphasmid nematodes that are often degenerate and surrounded by a cystic space (tunnel) admixed with cellular debris; occasional viable nematodes measure up to 100µm in diameter with a thin eosinophilic cuticle, a stichosome, inapparent musculature and bacillary bands, a uterus containing many eggs or testis with sperm, and an intestine lined by multiple cuboidal cells. Basal keratinocytes are occasionally swollen with a clear vacuole (hydropic degeneration) and rarely cells within the stratum spinosum are rounded with intensely eosinophilic cytoplasm (dyskeratosis). Occasionally, granulocytes transmigrate the epidermis, and there are a few lymphocytes and plasma cells in the dermis. There is orthokeratotic hyperkeratosis with few degenerating nematode fragments within the stratum corneum. There is a focal area of sub-basilar erosion with clefting at the basement membrane zone; the cleft contains a moderate amount of homogenous eosinophilic to fibrillar fluid (serum, fibrin).

  

MORPHOLOGIC DIAGNOSIS: Skin: Hyperplasia, epidermal, diffuse, moderate, with viable and degenerate intraepithelial aphasmid nematodes, and orthokeratotic hyperkeratosis, African clawed frog (Xenopus laevis), amphibian. 

 

ETIOLOGIC DIAGNOSIS:  Cutaneous capillariasis

 

ETIOLOGY:  Pseudocapillaroides xenopi 

 

ETIOLOGY SYNONYMS:  Capillaria xenopodis 

 

CONDITION:  Capillariasis

 

CONDITION SYNONYMS: Flaky skin disease, gray skin disease

 

GENERAL: 

• Common parasite of wild caught and captive bred clawed frogs, including those in research colonies
• Causes a wasting syndrome characterized by anorexia, changes to skin color, and excessive epidermal desquamation which often results in death
• May be asymptomatic until stressed
• Parasites typically found in dorsal skin; ventral lesions usually associated with bacterial infection from secondary invaders

 

LIFE CYCLE:

• Not completely understood but thought to be direct, and completed within the epidermis
• Transmission via ingestion of eggs in desquamated skin or through autoinfection

 

PATHOGENESIS:

• Epithelial damage predisposes to secondary bacterial infection, which may progress to septicemia
• In amphibians, the skin is important in maintaining hydration, osmoregulation, thermoregulation, and respiration; therefore, excessive epidermal desquamation can result in death
• Dependent on thymus-mediated immune response

 

TYPICAL CLINICAL AND GROSS FINDINGS:

• Dry, rough, flaky, dull gray skin usually over the dorsum with varying degrees of ventral erythema
• Excess mucus, ulceration, and sloughing of the skin
• Small (2-4mm x 1mm) white, sigmoid shaped nematodes in mucus overlying epidermis 
• Anorexia and emaciation
• Gradual onset, may take up to 12-18 months after infection for clinical signs to develop

 

TYPICAL MICROSCOPIC FINDINGS:

• Aphasmid nematodes:

• Adults and larvated eggs within epidermal tunnels and subepidermal clefts; degenerate parasites within the superficial epidermis, viable adults within the deeper layers

• Adults: 100-200µm diameter, thin cuticle, inapparant musculature, esophagus with stichosome glands, hypodermal/bacillary bands, lacks sensory papillae

• Females are twice as large as males, and contain embryonated and larvated eggs within uteri (unique feature to this species)
• Males have a caudal spicule

• Eggs are thin-walled with bipolar plugs and contain embryonated larvae

• Epidermis: Acanthosis, parakeratosis, dyskeratosis, epidermal ulcerations and erosions, variable granulocytic and monocytic inflammation surrounding parasites
• Dermis: Variable granulocytic and monocytic inflammation within the superficial dermis; granular degeneration of dermal glands in severe cases 

 

ADDITIONAL DIAGNOSTIC TESTS:

• Direct examination of the skin of a live frog under dissecting microscope
• Microscopic examination of skin scrape or wet smear of desquamated skin
• qPCR reported for detection of organism in aquarium sediment

 

DIFFERENTIAL DIAGNOSIS:

Gross:

• Red-leg syndrome (commonly attributed to Aeromonas hydrophila, but can be due to septicemia caused by a wide variety of Gram-negative and a few Gram-positive bacteria) — causes acute septicemia manifested as cutaneous hyperemia, cutaneous hemorrhages, and death; affects limbs, digits, and ventral abdomen
• Opportunistic fungal dermatitis – Zygomycetes (broad, irregular, rarely septate hyphae; includes Basidiobolus ranarum, Mucor spp., Rhizopus spp.) and Fusarium spp.
• Batrachochytrium dendrobatidis (I-F10, chytridiomycosis)—causes cutaneous erythema and orthokeratotic hyperkeratosis of the hind legs, feet, and ventrum; fungal thalli have distinct discharge papillae 
• Chromomycosis—dematiaceous fungi of the genera Fonsecaea, Phialophora, Cladosproium, Rhinocladiella and Scolecosbasidium cause disseminated disease in amphibians and have dark-brown hyphae or thick walled muriform cells (sclerotic bodies)

 

Histologic:

 

COMPARATIVE PATHOLOGY:

Other nematodes that localize in the epithelium include:

• Trichosomoides crassicauda (U-P10) in urothelium of rats
• Pearsonema sp. in the urothelium of cats, mink, dogs
• Gongylonema sp. in the esophagus of ruminants, does not elicit an inflammatory response; in the tongue and infrequently the esophagus of nonhuman primates and small mammals where it often elicits considerable inflammation 
• Anatrichosoma sp. (I-P05) in the nasal mucosa of nonhuman primates
• Eucoleus boehmi in the nasal mucosa of dogs
• Eucoleus aerophila (P-P15) in the tracheal and bronchial mucosa of wild canids, domestic dogs, and cats

 

REFERENCES:

1. Abee CR, Mansfield K, Tardif S, Morris T. Nonhuman Primates in Biomedical Research Diseases. Vol 2. 2nd  ed. San Diego, CA: Academic Press; 2012:245-246,575. 
2. Barthold SW, Griffey SM, Percy DH. Pathology of Laboratory Rodents and Rabbits. 4th ed. Ames, IA: Wiley Blackwell Publishing; 2016:152-3.
3. Caswell JL, Williams KJ. Respiratory system.  In: Maxie MG, ed. Jubb, Kennedy, and Palmer’s Pathology of Domestic Animals. 6th ed. Vol 2. St. Louis, MO: Elsevier; 2016:585.
4. Gardiner CH, Poynton SL. An Atlas of Metazoan Parasites in Animal Tissues. Washington, DC: Armed Forces Institute of Pathology; 1999: 40-43. 
5. Pessier AP. Amphibia. In: Terio KA, McAloose D, St. Leger J, eds. Pathology of Wildlife and Zoo Animals. Cambridge, MA: Elsevier; 2018:928, 930-932, 934, 936.

 

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