JPC SYSTEMIC PATHOLOGY
Signalment (JPC 994833): Cynomolgus macaque (Macaca fascicularis)
HISTOPATHOLOGIC DESCRIPTION: Mucosa and haired skin, nares: Multifocally, the mucosal epithelium is ulcerated and contains numerous intraepithelial tunnels with multiple tangential and cross-sections of 100-200 µm diameter, adult female and male nematodes. Nematodes have a 2 µm wide cuticle, paired bacillary bands, a pseudocoelom, stichosome, polymyarian-coelomyarian musculature and either a testis with sperm or a uterus with larvae. The mucosal epithelium exhibits spongiosis, hydropic degeneration, and transmigrating neutrophils. Multifocally within the subepithelial connective tissue and the dermis, there are numerous perivascular viable and degenerate neutrophils, lymphocytes, plasma cells, fewer eosinophils, and macrophages. Rarely, previously described adult nematodes are within lymphatics. Diffusely there is an exudate composed of many sloughed epithelial cells, degenerate neutrophils, abundant mucus, necrotic debris, and hemorrhage with few colonies of mixed bacteria and 50 x 75 µm, bi-operculate, embryonated nematode eggs with 3 µm wide, yellow, anisotropic shells. Within the epidermis, there is a focally extensive, mild parakeratotic hyperkeratosis with an intracorneal pustule composed of numerous viable and degenerate neutrophils, necrotic debris, and serum.
MORPHOLOGIC DIAGNOSIS: Mucosa and haired skin, nares: Rhinitis and dermatitis, ulcerative, neutrophilic and lymphoplasmacytic, multifocal, moderate, with intraepithelial and intralymphatic adult nematodes and rare eggs, etiology consistent with Anatrichosoma sp., Cynomolgus macaque (Macaca fasicularis), nonhuman primate.
ETIOLOGIC DIAGNOSIS: Nasal anatrichosomiasis
CAUSE: Anatrichosoma sp.
- Anatrichosoma intraepithelial aphasmid nematodes
- Typically found in the nasal epithelium of Old World and New World monkeys, great apes, and humans
- Can cause cutaneous larval migrans of the face and extremities and subcutaneous nodules with edema about the joints of the extremities and to serpiginous blisters of the palms and soles of monkeys
- Anatrichosoma cynomolgi (A. cutaneum) is the most common species involved
- Epithelial damage predisposes to secondary bacterial infection
- Reside in nasal mucosa near basal layer of the skin
- Female worms migrate through squamous epithelium, forming tunnels > depositing embryonated egg > tunnels slough releasing eggs > eggs in nasal discharge or passed in feces
- Male worms are typically found in the deep subcutis
TYPICAL CLINICAL/GROSS FINDINGS:
- Asymptomatic or only mild inflammation: mild serous discharge may occur
- Cutaneous lesions have serpiginous tracts with subcutaneous foreign body reaction
- White tracks on skin on soled and/or palms of hands and soles of feet
- Regional lymphadenopathy
TYPICAL LIGHT MICROSCOPIC FINDINGS:
- Nasal mucosa hyperplasia and parakeratosis
- Moderate lymphoplasmacytic and eosinophilic infiltrate
- Aphasmid structure:
- Thick cuticle, stichosome (esophageal gland cells that surround the esophagus), paired bacillary bands (hypodermal bands), polymyarian- coelomyarian musculature
- Females approximately 300 µm in diameter and males are approximately 100 µm
- Anatrichosoma and Trichosomoides sp. eggs are unique, containing a fully formed larva
- Eggs are approximately 50 x 75 µm with a yellow, barrel-shaped, anisotropic shell, and have bipolar opercula, embryonated
ADDITIONAL DIAGNOSTIC TESTS:
- Egg identification from nasal swab; eggs rarely present in fecal samples
- Grossly cutaneous lesions resemble hookworm larval migration (Ancylostoma)
- Histologically: Presence of a nematode with stichosomes, paired bacillary bands and bipolar larvated eggs is diagnostic
- Ancylostoma have small lateral double alae
- Capillaria and Trichuris lack larvated eggs
- Filarids (Dipetalonema, Onchocerca sp., Dirofilaria sp.) lack stichosomes
- Cat: Few case reports of larval migrans; all cases reported in footpads causing lameness with necrosis, ulceration, and sloughing of multiple pawpads
- Dog: Rare cause of otitis externa and erythematous nodular scaling
- Tree shrew (Tupaia glis): Anatrichosoma ocularis infects cornea and conjunctiva
- Opossum (Didelphis virginiana): Anatrichosoma buccalis infects oral mucosa
Intraepithelial nematodes in animals:
- Trichosomoides crassicauda: Urothelium of rats
- Gongylonema : Esophagus of ruminants and nonhuman primates; associated with esophageal squamous cell carcinoma
- Eucoleus boehmi: Nasal mucosa of dogs
- Capillaria xenopodis (Pseudocapillaroides xenopi): Skin of clawed frogs
- Capillaria annulata, Capillaria contorta: Crop and esophagus of birds
- Eucoleus aerophilus (Capillaria aerophilia): Respiratory tract of foxes and other canids
- Abee CR, Mansfield K, Tardif S, Morris T. Nonhuman Primates in Biomedical Research Diseases. Vol 2. 2nd San Diego, CA: Academic Press; 2012: 245-246,575.
- Bleier T, Huetzel U, Bauder C, Behlert O, Burkhardt E. Gongylonema pulchrum infection and esophageal squamous cell carcinoma in a vari (Lemur macaca variegata; Kehr 1792). J Zoo Wildl Med. 2005;36(2):342-345.
- Bowman DD. Georgis' Parasitology for Veterinarians. 10th ed. St. Louis, MO: Elsevier; 2014: 227, 429.
- Calle PP, Joslin JO. Chapter 37 New World and Old World Monkeys. In: Miller RE, Fowler M, eds. Fowler’s Zoo and Wild Animal Medicine. Vol 8. Louis, MO: Elsevier; 2015: 312.
- Gardiner CH, Poynton SL. An Atlas of Metazoan Parasites in Animal Tissues. Washington, DC: Armed Forces Institute of Pathology; 1999: 40-43.
- Maudlin EA, Peters-Kennedy J. Integumentary system. In: Maxie MG, ed. Jubb, Kennedy, and Palmer’s Pathology of Domestic Animals. Vol 1. 6th ed. Philadelphia, PA: Elsevier Saunders; 2016: 690.
- Meyers WM. Pathology of Infectious Diseases. 1. Washington, DC: Armed Forces Institute of Pathology; 2000: 367.
- Miller WH, Griffin CE, Campbell KL. Muller and Kirk's Small Animal Dermatology. 7th ed. Philadelphia, PA: Saunders; 2013:291.
- Noden BH, Du Plessis EC, Morkel C, Tubbesing U, Soni M. Bowman DD. Anatrichosoma sp. in the footpads of a cat: diagnosis and pathology of Namibian case. Vet Parasitol. 2013; 191 (3-4):386-389.
- Ramiro-Ibanez F, Winston J, O'Donnell E, Mansell J. Ulcerative pododermatitis in a cat associated with Anatrichosoma J Vet Diagn Invest. 2002; 14(1):80-83.