JPC SYSTEMIC PATHOLOGY
HEMOLYMPHATIC SYSTEM
April 2024
H-P09
SIGNALMENT: Southern masked weaver (Ploceus velatus) .
HISTORY: 19-year-old intact male with a chronic history of abnormal mentation and posture and difficulty flying. There were multiple exacerbations of suspected neurologic signs (head down, wings spread, decreased flying ability and occasional open mouth breathing). Previous episodes responded to hospitalization and empirical treatment with antibiotics, antifungals and anthelmintics to return to baseline status. During a final episode there was decreased responsiveness, head-down/wings-out posture, no attempts to fly, dilated pupils, subjectively thickened lower eyelids, areas of feather loss on the head, and a left cranial coelomic mass effect. Euthanasia was requested due to the increasing frequency of these episodes. Significant reported gross findings included adequate body fat stores and pectoral muscling; a moderately distended coelomic cavity with the gizzard and intestinal loops extending into the distended area; multifocal to coalescing, random, <1x1 mm up to 9x9 mm, minimally raised, firm, tan masses on the heart, right ventral lung, bilateral anterior thoracic air sacs, liver and pleura.
HISTOPATHOLOGIC DESCRIPTION:
Intestines: Diffusely infiltrating and severely expanding the lamina propria and extending transmurally, there is a marked leukocytic infiltrate composed predominantly of lymphocytes, with fewer histiocytes, plasma cells, and granulocytes. The majority of lymphocytes contain intracytoplasmic, oval, 1-2-µm-diameter, basophilic merozoites surrounded by a halo often indenting the nucleus. Within the mucosal epithelial cells there are occasional up to 14-µm-diameter coccidia at various stages of development, to include macrogamonts characterized by a peripheral ring of large eosinophilic granules, fewer microgamonts that are smaller with more densely packed basophilic cytoplasmic granules, schizonts that contain merozoites, and unsporulated oocysts with a thin capsule and homogenous finely granular amphophilic cytoplasm. There is multifocal degeneration and necrosis of mucosal epithelium..
Liver, esophagus, proventriculus, kidney: Multifocally, the interstitium is infiltrated and expanded by moderate numbers of mononuclear inflammatory infiltrates composed predominantly of lymphocytes with fewer histiocytes and plasma cells. The majority of these lymphocytes contain merozoites as previously described.
Pancreas, heart, ventriculus: No significant findings.
MORPHOLOGIC DIAGNOSIS:
1. Intestines, liver, proventriculus, kidney, esophagus: Lymphocytic infiltration, multifocal, moderate to severe, with intraleukocytic apicomplexan merozoites and enterocyte degeneration, Southern masked weaver, avian.
2. Intestines: Intra-epithelial gamonts and schizonts.
3. Pancreas, heart, ventriculus: Essentially normal tissue.
ETIOLOGIC DIAGNOSIS: Systemic isosporosis.
CAUSE: Isospora sp.
CONDITION: Systemic isosporosis, Atoxoplasmosis
GENERAL DISCUSSION:
- Coccidian (apicomplexan) protozoan that primarily parasitizes passerines
- Has a controversial taxonomic history; Isospora sp. is suggested over using the term Atoxoplasma sp.
- Young birds can die acutely; older birds may be chronically infected with no signs
PATHOGENESIS:
- Fecal-oral transmission with oocysts shed in feces; infection occurs after the ingestion of sporulated oocysts
- Merogenic phase: Mainly lymphocytes, also monocytes
- Vertical transmission possible
- In captive species, infection is influenced by husbandry conditions (crowding, exposure to wild birds, stress, poor sanitation)
LIFECYCLE:
- There are intestinal and extra-intestinal (reticuloendothelial) forms with a prolonged life cycle
- Asexual reproduction (merogony): Occurs in the enterocytes and circulating mononuclear leukocytes (lymphocytes, but macrophages have been described also)
- Sexual (gametogony): Occurs within enteric epithelium resulting in production of oocysts
TYPICAL CLINICAL FINDINGS:
- Mortality most common in fledglings, but adults can also be affected
- Anorexia, weight loss, ruffled feathers, diarrhea, hepatomegaly with distention of the coelomic cavity, and muscular atrophy
TYPICAL GROSS FINDINGS:
- Primarily splenomegaly, hepatomegaly is also seen
- Less common gross findings: Edematous, congested small intestines and atrophy of adipose and skeletal muscle
- In acute cases, body condition may be normal
- Birds with myositis may have streaking in cardiac and skeletal muscle
TYPICAL LIGHT MICROSCOPIC FINDINGS:
- Small, round ~2-5µm lightly basophilic, protozoal merozoites with a clear halo in the cytoplasm of affected mononuclear cells
- Spleen: Lymphoid hyperplasia; lymphohistiocytic splenitis with 3-5-μm, poorly stained intracytoplasmic merozoites that indent the host nucleus
- Small intestine: Transmural (mucosa, muscularis, ganglia, serosa) lymphohistiocytic inflammation; lymphocytic infiltration can resemble lymphoma; loss of villar architecture with severe inflammation
- Liver: Lymphohistiocytic inflammation; +/- cholangiohepatitis and random necrosis
- Intestinal mucosa (enterocytes): Oocysts often present
CLINICAL PATHOLOGY:
- Fecal: Sporulated oocysts have two sporocysts and four sporozoites
- Mononuclear cells: Parasite causes a clear notch in the host nucleus (indented nucleus) due to intracytoplasmic merozoites
- Exfoliate cytology imprints of the spleen and lung are particularly rewarding for parasite identification.
- In vivo diagnosis: FNA of enlarged livers
- While cytology is useful for identifying the extra-intestinal life stages, histopathology is best for identifying the intestinal life stages
ADDITIONAL DIAGNOSTIC TESTS:
- IHC
- Fecal
- PCR
DIFFERENTIAL DIAGNOSIS:
- Must be differentiated from Toxoplasma; anti-Toxoplasma gondii antibodies do not stain Isospora/Atoxoplasma
- Gross lesions may resemble Mycobacterium sp. infections
COMPARATIVE PATHOLOGY:
- Incidental finding in an East African crowned crane
- Reported in numerous passerines: House sparrows, canaries, finches, starlings, siskins, tanagers, weavers, and jays
- Reported in endangered species: Bali mynah and blue-crowned laughing thrush
- Fringillids (finches), especially canaries, marked thickening of the duodenum is the most consistent gross finding; splenomegaly also seen
- White-rumped shama (Wong, Vet Pathol, 2022): Nodular aggregates of atypical epithelioid macrophages containing few intracytoplasmic organisms with or without lymphocytic infiltration; most have systemic lesions and all have skin involvement (suggesting a unique predilection for the skin in this species).
REFERENCES:
- Abdul-Aziz T, Fletcher OJ. Chapter 2: Lymphoid System. In: Abdul-Aziz T, Fletcher OJ, Barns HJ, eds. Avian Histopathology. 4th ed. Madison, WI: Omnipress; 2016: 21.
- Abdul-Aziz T, Fletcher OJ. Chapter 8: Hepatobiliary System. In: Abdul-Aziz T, Fletcher OJ, Barns HJ, eds. Avian Histopathology. 4th ed. Madison, WI: Omnipress; 2016: 359.
- Fitz-Coy SH. Parasitic Diseases. In: Boulianne M, ed. Avian Disease Manual. 8th ed. Jacksonville, FL: American Association of Avian Pathologists, Inc; 2019:132.
- Schmidt R, Reavill DR, Phalen DN. Pathology of Pet and Aviary Birds. 2nd ed. Ames, IA: John Wiley & Sons, Inc.; 2015: 187-188.
- Trupkiewicz J, Garner MM, Juan-Salles C. Passeriformes, Caprimulgiformes, Coraciiformes, Piciformes, Bucerotiformes, and Apodiformes. In: Terio KA, McAloose D, St. Leger J, eds. Pathology of Wildlife and Zoo Animals. London, UK: Academic Press; 2018:815-817.
- Wong TS, Stalis IH, Witte C, Kubiski SV. Unique Isospora-associated histologic lesions in white-rumped shama (Copsychus malabaricus). Vet Pathol. 2022;59(5):869-872.
- Wunschmann A, Armien AG, Hofle U, Kinne J, Lowenstine LL, Shivaprasad HL. Birds of Prey. In: Terio KA, McAloose D, St. Leger J, eds. Pathology of Wildlife and Zoo Animals. London, UK: Academic Press; 2018:717.