JPC SYSTEMIC PATHOLOGY

DIGESTIVE SYSTEM

October 2024

D-P21

 

SLIDE A: Signalment (JPC #2550496): Hare

 

HISTORY: None

 

HISTOPATHOLOGIC DESCRIPTION: Liver: Expanding and effacing 70% of this section and compressing adjacent hepatocytes are multifocal to coalescing granulomas centered on eosinophilic cellular and karyorrhectic debris (lytic necrosis) admixed with numerous aphasmid nematode eggs. These eggs are 40x60 µm, have a 10-15um thick, anisotropic, bioperculated shell with radial striations, and contain either an eosinophilic 15 µm diameter morula or small amounts of granular eosinophilic debris.  The central areas of necrosis are bounded by circumferential layers of numerous degenerate neutrophils and eosinophils, epithelioid macrophages and multinucleated giant cells (foreign body and Langhans types), numerous fibroblasts, numerous eosinophils, fewer lymphocytes and plasma cells, and fibrous connective tissue (fibrosis) with many entrapped bile ductules. The multinucleated giant cells measure up to 200 µm in diameter, contain up to 40 nuclei, and rarely contain a phagocytized nematode egg. The adjacent hepatocytes are multifocally atrophied, occasionally swollen and microvacuolated (degenerate), or rarely shrunken and hypereosinophilic with pyknotic nuclei (necrotic). Multifocally there are increased numbers of haphazardly arranged bile ducts (ductular reaction) as well as occasional ectatic bile ducts. Multifocally there is minimal to mild hemorrhage, fibrin, and edema within the hepatic parenchyma. Portal areas are infiltrated by low numbers of eosinophils, lymphocytes and plasma cells. 

 

MORPHOLOGIC DIAGNOSIS: Liver: Granulomas, eosinophilic, multifocal to coalescing, moderate to marked, with bi-operculate aphasmid nematode eggs, hare (Lepus sp.), lagomorph. 

 

ETIOLOGIC DIAGNOSIS: Hepatic capillariasis

 

CAUSE: Capillaria hepatica (Calodium hepaticum); Capillaria spp. (birds)

 

SLIDE B: Signalment (JPC #3165178): Adult male guinea fowl.

 

HISTORY: This male guinea fowl was one of several group housed at a zoological institution that developed wasting and chronic diarrhea followed by multiple deaths. On autopsy, this bird was in poor nutritional condition and the crop was markedly dilated, the crop wall measured 3-4mm thick, and the mucosa was tan, granular, and rugose.

 

HISTOPATHOLOGIC DESCRIPTION: Esophagus: Diffusely the mucosal epithelium is markedly thickened up to 1.5mm (mucosal hyperplasia), with numerous variably sized papillary projections extending into the lumen that are variably cornified, and the mucosa is moderately undulant (rugose). The mucosal glands are also either moderately hyperplastic or replaced by hyperplastic mucosal epithelium. Multifocally throughout the mucosa there are numerous intact and degenerate cross and tangential sections of adult aphasmid nematodes and eggs. The adult nematodes are 150 µm in diameter, have a 2-3 µm thick cuticle, polymyarian-coelomyarian musculature, hypodermal bacillary bands, stichosome, esophagus, gastrointestinal tract lined by uninucleate cuboidal cells, and reproductive tract often containing numerous eggs. The eggs are 20x40 µm and have a 3-4 µm thick, eosinophilic, anisotropic, bioperculated shell containing eosinophilic flocculent material. Within the lamina propria, the mucosa-associated lymphoid tissue is moderately expanded (reactive) and diffusely there are several scattered lymphocytes, plasma cells, and fewer heterophils admixed with increased clear space (edema). Rarely, heterophils also transmigrate through the mucosa and either form intraepithelial aggregates, aggregate around degenerate nematode sections and eggs with fewer macrophages and lymphocytes, or are found within the lumen admixed with mixed intraluminal bacterial colonies and ingesta. 

 

MORPHOLOGIC DIAGNOSIS: Esophagus: Esophagitis, proliferative, diffuse, marked, with numerous intraepithelial adult aphasmid nematodes and bi-operculate aphasmid nematode eggs, Guinea fowl, avian.

 

ETIOLOGIC DIAGNOSIS: Esophageal capillariasis

 

CAUSE: Capillaria spp. (C. contorta or C. annulata)

 

GENERAL DISCUSSION:

• Capillaria spp. (family Trichuridae) are aphasmid nematodes that parasitize diverse epithelia of a wide range of hosts
• Unique morphologic features of aphasmids:
  • Row of esophageal gland cells (stichocytes) that form a stichosome (a series of glands along the esophagus); this structure surrounds the esophagus and is very basophilic
  • Bacillary or hypodermal bands: Pore-like structures on the body surface 
  • Lack a pair of sensory papillae (phasmids) on the caudal end (not identifiable in histologic section)
  • Do not have lateral cords like the phasmids
  • Bioperculate (bipolar plugged), barrel-shaped, thick-shelled and unembryonated eggs (many genera)
• Capillaria hepatica is primarily a disease of wild rodents (ubiquitous in black and Norway rat populations) but has been reported in many mammalian hosts, including the dog, cat, rabbit, vole, chipmunk, groundhog, squirrel, mole, shrew, opossum, weasel, fox, skunk, raccoon, porcupine, mountain gorillas (usually incidental but may be severe in infants), and other primates including humans
  • Only species of nematode that has the adult stage in the liver parenchyma (not in the bile ducts)
• Capillaria spp. are common nematodes in several bird species including free ranging passerines, occasionally leading to severe losses in turkeys and game birds; C. contorta or C. annulata infect the crop and esophagus and cause thickening and inflammation of mucosa

 

PATHOGENESIS:

• Capillaria hepatica is not highly pathogenic 
• Eggs and excreta deposited in the liver provoke granuloma formation and subsequent fibrosis.
• Severe infection may lead to mortality
• Capillaria sp. in birds are often an incidental finding except Capillaria sp. in vulturine guinea fowl (high mortality), raptors (significant esophageal thickening), and occasionally turkeys and game birds

 

LIFE CYCLE:

• Capillaria hepatica: Larvae ingested, hatch and migrate to liver > adults live in liver parenchyma and produce eggs > eggs develop only upon exposure to oxygen when host is eaten by predator or dies and decomposes > eggs pass in feces of predator > passed eggs embryonate in the external environment
• Birds: Larvae are ingested > develop into adults > embed in the lining of the esophagus/crop/intestine > eggs are laid and passed in droppings > embryonate within 6-8 days (some species of capillarids have an earthworm intermediate host)

 

TYPICAL GROSS FINDINGS: 

• Capillaria hepatica: Hepatomegaly with multiple to coalescing white or yellow patches and nodules under the capsule and/or throughout the parenchyma
• Birds: Mucosal thickening

 

TYPICAL LIGHT MICROSCOPIC FINDINGS: 

• Stichosome 
• Bacillary or hypodermal bands
• Polymyarian-coelomyarian musculature (may be inapparent)

• Capillaria hepatica: Multiple hepatic granulomas and fibrosis surrounding bioperculate eggs and/or adult nematodes
• Birds: Mucosal proliferation with numerous intra-epithelial aphasmid nematodes and bioperculate eggs

 

ADDITIONAL DIAGNOSTIC TESTS: 

 

DIFFERENTIAL DIAGNOSIS:

Capillaria hepatica in hares:

• Gross: Hepatic coccidiosis (Eimeria stiedae, D-P02); the #1 cause of white-spotted liver lesions in wild European rabbits; C. hepatica is #2 (Bochynska,J Vet Diagn Invest, 2022).
• Eggs: Schistosoma sp. (D-P20) eggs are also found in liver but have a prominent lateral spine and lack opercula

Capillaria spp. in birds:

• Gross: White plaques in the mouth; avian poxvirus, Candida albicans, Trichomonas gallinae, Vitamin A deficiency
• Eggs: Syngamus trachea also has a large ellipsoid operculated eggs

 

COMPARATIVE PATHOLOGY:

• Capillaria hepatica in primates: New world, old world, great ape, and human granulomatous hepatitis; essentially the same disease and lifecycle as in rodents and lagomorphs
• Capillaria aerophila (synonymous with Eucoleus aerophilus): Bronchial capillariasis; lungs of dogs, cats, and foxes, and responsible for verminous pneumonia in European hedgehogs (Lehmann, Vet Pathol 2024)
• Pearsonema plica, Pearsonema feliscati (formerly Capillaria plica and C. feliscati): Urinary capillariasis; renal pelvis, ureter or urinary bladder of dogs, cats, foxes and wolves, earthworm intermediate host
• Eucoleus boehmi: Uncommon cause of rhinitis in dogs and cats, eggs have a pitted shell
• Capillaria anati: Cecum of birds
• Capillaria bursata, C. caudinflata: Small intestine of birds
• Capillaria xenopodis (Pseudocapillaroides xenopi, I-): Cutaneous capillariasis of South African clawed frogs
• Capillaria pterophylli: in freshwater fish, digestive tract infection and inflammation, chronic wasting

 

REFERENCES:

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