JPC SYSTEMIC PATHOLOGY

INTEGUMENTARY SYSTEM

October 2022

I-P05 (NP)

 

Signalment (JPC# 994833):  Cynomolgus macaque (Macaca fascicularis)

 

HISTORY:  None

 

HISTOPATHOLOGIC DESCRIPTION:  Mucosa and haired skin, nares:  Multifocally, the mucosal epithelium is ulcerated with occasional replacement by serocellular crust that blends into luminal exudate composed of many sloughed epithelial cells, degenerate neutrophils, abundant mucus, necrotic debris, and hemorrhage with few colonies of mixed bacteria. The adjacent intact epithelium contains numerous intraepithelial tunnels with multiple tangential and cross-sections of adult female and male nematodes that are 100-200 µm diameter and have a 2 µm thick cuticle, paired bacillary bands, polymyarian-coelomyarian musculature, a pseudocoelom, a stichosome esophagus or digestive tract lined by uninucleate cuboidal cells, and either a testis with sperm or a uterus with larvae. There are rare eggs that are 70µm in diameter, have a 5µ anisotropic shell and contain a coiled larva. The mucosal epithelium exhibits squamous metaplasia, 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 and blood vessels. 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 spp., Cynomolgus macaque (Macaca fasicularis), nonhuman primate. 

 

ETIOLOGIC DIAGNOSIS:  Nasal anatrichosomiasis

 

CAUSE:  Anatrichosoma sp.

 

GENERAL DISCUSSION:  

• Anatrichosoma sp. are 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, subcutaneous nodules with edema around the joints of the extremities, and serpiginous blisters of the palms and soles of monkeys 
• Anatrichosoma cynomolgi (A. cutaneum) is the most common species involved

 

PATHOGENESIS:  

 

LIFE CYCLE:

• 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 mucosal hyperplasia and parakeratosis 
• Moderate lymphoplasmacytic and eosinophilic infiltrate
• Aphasmid nematode 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  sp. 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, have bipolar opercula, and are embryonated 

 

ADDITIONAL DIAGNOSTIC TESTS:  

 

DIFFERENTIAL DIAGNOSIS:

• Grossly: cutaneous lesions resemble hookworm larval migration (Ancylostoma sp.)
• Histologically: Presence of a nematode with stichosomes, paired bacillary bands, and bipolar larvated eggs is diagnostic
• Ancylostoma sp. have small lateral double alae
• Capillaria and Trichuris lack larvated eggs
• Filarids (Dipetalonema sp., Onchocerca sp., Dirofilaria sp.) lack stichosomes

 

COMPARATIVE PATHOLOGY:  

• 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 sp.:  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

 

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. Bowman DD. Georgis' Parasitology for Veterinarians. 10th ed. St. Louis, MO: Elsevier; 2014: 227, 429. 
3. 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. St. Louis, MO: Elsevier; 2015: 316. 
4. Gardiner CH, Poynton SL. An Atlas of Metazoan Parasites in Animal Tissues. Washington, DC: Armed Forces Institute of Pathology; 1999: 40-43. 
5. Jitsamai W, Kesdangsakonwut S, Srirat T, Taweethavonsawat P. Case Report: Molecular and Pathological Investigations of Zoonotic Anatrichosoma Spp.-Induced Ulcerative Pododermatitis in a Domestic Cat in Thailand. Front Vet Sci. 2021; Oct 14(8):759814. 
6. Matz-Rensing K, Lowenstine LJ. New World and Old World Monkeys. In: Pathology of Wildlife and Zoo Animals. Eds. Terio KA, McAloose D, St. Leger J. San Diego, CA: Elsevier; 2018:368.e10.
7. 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.   
8. Miller WH, Griffin CE, Campbell KL. Muller and Kirk's Small Animal Dermatology. 7th ed.  Philadelphia, PA: Saunders; 2013:291. 
9. 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. 

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