History
During 2017 and 2018, 3 disease outbreaks occurred among a group of 7 lorikeets (Trichoglossus moluccanus) at an enclosed aviary and wildlife center that was accessible to park visitors. In total, 3 adult male and 4 adult female lorikeets were submitted for necropsy. In January 2017, a mated pair of birds died suddenly, and in March 2017, a male bird died suddenly after development of general signs of lethargy. In January 2018, 3 females and 1 male bird died suddenly. Of this latter group, only 1 female lorikeet developed weakness and lethargy; however, an abrupt diet change from seed to nectar prior to all 4 deaths occurred as a result of a delayed shipment of the birds’ usual food.
Clinical and Gross Findings
An antemortem CBC and plasma biochemical analysis were performed for the male bird that died in March 2017. The CBC revealed leukocytosis, polycythemia, heterophilia, and monocytosis. The plasma biochemical analysis panel revealed hypoproteinemia, high aspartate aminotransferase activity, hyperphosphatemia, hypocalcemia, high creatine kinase activity, and hyperuricemia. At necropsy, all 7 birds were in fair body condition with adequate body fat stores and moderate hepatomegaly. Livers were friable and moderately pale yellow to brown. Five livers contained multifocal, randomly distributed, 0.5- to 2-mm-diameter, tan and white foci that extended deep into the parenchyma on cut surface (Figure 1). The birds’ lungs had no observable gross changes and were spongy in texture and floated in neutral-buffered 10% formalin. The lungs of 4 birds were diffusely dark red to brown, and the lungs of 3 birds were diffusely pale pink to red. The proventriculus was mildly dilated in 4 of the 7 birds.
Representative photograph of the heart and liver of 1 of 7 lorikeets (Trichoglossus moluccanus) at an enclosed aviary and wildlife center that died suddenly during 3 disease outbreaks in 2017 and 2018. This lorikeet was a male. Notice the moderate hepatomegaly. The liver is friable, pale yellow, and contains multifocal pinpoint tan and white foci (arrow).
Citation: Journal of the American Veterinary Medical Association 259, 7; 10.2460/javma.259.7.737
Representative photograph of the heart and liver of 1 of 7 lorikeets (Trichoglossus moluccanus) at an enclosed aviary and wildlife center that died suddenly during 3 disease outbreaks in 2017 and 2018. This lorikeet was a male. Notice the moderate hepatomegaly. The liver is friable, pale yellow, and contains multifocal pinpoint tan and white foci (arrow).
Citation: Journal of the American Veterinary Medical Association 259, 7; 10.2460/javma.259.7.737
Representative photograph of the heart and liver of 1 of 7 lorikeets (Trichoglossus moluccanus) at an enclosed aviary and wildlife center that died suddenly during 3 disease outbreaks in 2017 and 2018. This lorikeet was a male. Notice the moderate hepatomegaly. The liver is friable, pale yellow, and contains multifocal pinpoint tan and white foci (arrow).
Citation: Journal of the American Veterinary Medical Association 259, 7; 10.2460/javma.259.7.737
Histopathologic Findings
For all 7 lorikeets, sections of all major visceral organs, the brain, and skeletal muscles were prepared and evaluated. All birds had similar histologic changes. The liver of each bird had multifocal random areas of hepatocellular necrosis with a central accumulation of necrotic and cellular debris admixed with fibrin and dense colonies of coccobacilli surrounded by large numbers of heterophils and fewer histiocytes (Figure 2). Moderate to severe hepatic lipidosis was present in all livers, as supported by the presence of oil red O stain–positive vacuoles. The lungs contained multifocal random areas of necrosis similar to those described for the liver. Similar bacterial colonies were randomly scattered in the lungs and various other organs. In the kidneys, bacteria were mostly in the glomeruli. In the spleen, bacteria were located in the red and white pulp. In the intestinal mucosae and lumens, bacteria were located throughout the mucosae. Gram staining was performed and revealed dense gram-negative coccobacillary colonies amid variable amounts of fibrin centered in areas of necrotic parenchyma.
Photomicrographs of liver tissue sections obtained from the bird in Figure 1. All birds had similar histologic changes. A—There is hepatocellular necrosis with severe infiltration of heterophils and fewer histiocytes centered on a focus of coccobacillary bacterial colonies admixed with variable amounts of fibrin. H&E stain; bar = 20 µm. B—In another liver section, dense coccobacillary gram-negative bacterial colonies amid variable amounts of fibrin are centered in areas of necrotic parenchyma. Gram stain; bar = 20 µm.
Citation: Journal of the American Veterinary Medical Association 259, 7; 10.2460/javma.259.7.737
Photomicrographs of liver tissue sections obtained from the bird in Figure 1. All birds had similar histologic changes. A—There is hepatocellular necrosis with severe infiltration of heterophils and fewer histiocytes centered on a focus of coccobacillary bacterial colonies admixed with variable amounts of fibrin. H&E stain; bar = 20 µm. B—In another liver section, dense coccobacillary gram-negative bacterial colonies amid variable amounts of fibrin are centered in areas of necrotic parenchyma. Gram stain; bar = 20 µm.
Citation: Journal of the American Veterinary Medical Association 259, 7; 10.2460/javma.259.7.737
Photomicrographs of liver tissue sections obtained from the bird in Figure 1. All birds had similar histologic changes. A—There is hepatocellular necrosis with severe infiltration of heterophils and fewer histiocytes centered on a focus of coccobacillary bacterial colonies admixed with variable amounts of fibrin. H&E stain; bar = 20 µm. B—In another liver section, dense coccobacillary gram-negative bacterial colonies amid variable amounts of fibrin are centered in areas of necrotic parenchyma. Gram stain; bar = 20 µm.
Citation: Journal of the American Veterinary Medical Association 259, 7; 10.2460/javma.259.7.737
Photomicrographs of liver tissue sections obtained from the bird in Figure 1. All birds had similar histologic changes. A—There is hepatocellular necrosis with severe infiltration of heterophils and fewer histiocytes centered on a focus of coccobacillary bacterial colonies admixed with variable amounts of fibrin. H&E stain; bar = 20 µm. B—In another liver section, dense coccobacillary gram-negative bacterial colonies amid variable amounts of fibrin are centered in areas of necrotic parenchyma. Gram stain; bar = 20 µm.
Citation: Journal of the American Veterinary Medical Association 259, 7; 10.2460/javma.259.7.737
Photomicrographs of liver tissue sections obtained from the bird in Figure 1. All birds had similar histologic changes. A—There is hepatocellular necrosis with severe infiltration of heterophils and fewer histiocytes centered on a focus of coccobacillary bacterial colonies admixed with variable amounts of fibrin. H&E stain; bar = 20 µm. B—In another liver section, dense coccobacillary gram-negative bacterial colonies amid variable amounts of fibrin are centered in areas of necrotic parenchyma. Gram stain; bar = 20 µm.
Citation: Journal of the American Veterinary Medical Association 259, 7; 10.2460/javma.259.7.737
Additional laboratory Test Findings
Immunohistochemical staining for Chlamydia spp and Listeria spp was performed on liver sections; sections of gastrointestinal tissues were stained for avian bornavirus. Immunohistochemical findings were negative. Liver and lung tissue specimens from all 7 birds were submitted for bacterial culture. A final confirmatory diagnosis was based on isolation of Yersinia pseudotuberculosis from liver and lung tissue cultures.
Morphologic diagnosis and Case Summary
Morphologic diagnosis: severe multifocal, random, necrotizing heterophilic and histiocytic hepatitis with intralesional bacterial colonies; moderate hepatic lipidosis; and moderate multifocal, random, necrotizing heterophilic and histiocytic pneumonia with intralesional bacterial colonies.
Case summary: septicemia attributable to Y pseudotuberculosis infection in 7 lorikeets.
Comments
For the lorikeets of the present report, results of bacterial culture of liver and lung tissue specimens indicated infection of liver and lung tissues with Y pseudotuberculosis. Gross and histopathologic findings of severe acute, random, necrotizing hepatitis with central dense bacterial colonies were consistent with this diagnosis.
Yersinia pseudotuberculosis is a gram-negative, non–spore-forming, facultative aerobic intracellular coccobacillus and an important zoonotic agent. It has been identified in more than 110 species, including mammals, birds, reptiles, and fish.1 Rodents and wild birds act as reservoir hosts. Infection with Y pseudotuberculosis typically occurs via the oral route.2 Once ingested, the bacteria cross the epithelial barrier through M cells, infect associated lymphoid tissues, and disseminate throughout the body via mesenteric lymph nodes. The main virulence of the bacterium is the type III secretion system (T3SS), which is encoded by a 70-kilobase virulence plasmid. The T3SS enables the translocation of virulence effector proteins directly into the cytosol of the target host cell, thereby disrupting host cell signaling. Neutrophils are major targets for the T3SS effectors. As a result, phagocytosis of the Yersinia bacteria by immune cells is inhibited, the overall proinflammatory response is downregulated, and the early immune response is suppressed in Y pseudotuberculosis–infected animals.3
In the lorikeets of the present report, disease outbreaks occurred during the colder seasons, namely winter and early spring. In 2018, 4 birds had a diet change, which in any situation is a stress factor that may facilitate infection. Infection with Y pseudotuberculosis results in systemic lesions, primarily in the liver, lungs, spleen, and kidneys. Lesions are characterized by severe inflammation and numerous dense colonies of intralesional bacteria in affected organs.1
Yersinia pseudotuberculosis–related disease in humans and other mammals often manifests as self-limiting gastroenteritis but can occasionally progress to lymphadenitis and chronic infection.1 In avian practice, diagnosis can be made on the basis of isolation and identification of the organisms in cloacal swab samples4 by culture methods (cold enrichment) or a real-time PCR assay.5 Yersinia pseudotuberculosis infection is common among caged birds, particularly during the winter and spring seasons.2 Generally, stress factors, such as a colder environment, improper nutrition, or transport, can be contributing factors to development of infection.4 Yersiniosis outbreaks in zoo epidemics have been described.5 Commonly, infected birds die suddenly with vague clinical signs. Antimicrobial treatment can be effective and should be based on results of bacterial culture and antimicrobial susceptibility testing of appropriate specimens. Different strains of Y pseudotuberculosis can have variable antimicrobial susceptibility, but most are susceptible to third-generation cephalosporins, fluoroquinolones, and chloramphenicol. Because birds can serve as a reservoir for this infection, the focus for many zoos has been toward precluding transmission of Y pseudotuberculosis. Prevention of Y pseudotuberculosis infection includes effective sanitary husbandry and hygiene protocols and minimization of stress among captive birds.6
References
- 1. ↑
Stoute ST, Cooper GL, Bickford AA, et al. Yersinia pseudotuberculosis in Eurasian Collared Doves (Streptopelia decaocto) and retrospective study of avian yersiniosis at the California Animal Health and Food Safety Laboratory System (1990–2015). Avian Dis 2016;60:82–86.
- 2. ↑
Obwolo MJ. The pathogenesis of yersiniosis. In: Montali RJ, Migaki G, eds. The comparative pathology of zoo animals. Washington, DC: Smithsonian Institute Press, 1980;225–229.
- 3. ↑
Avican U, Doruk T, östberg T, et al. The Tat substrate SufI is critical for the ability of Yersinia pseudotuberculosis to cause systemic infection. Infect Immun 2017;85:e00867–16.
- 4. ↑
Nakamura S, Hayashidani H, Sotohira Y, et al. Yersiniosis caused by Yersinia pseudotuberculosis in captive toucans (Ramphastidae) and a Japanese squirrel (Sciurus lis) in zoological gardens in Japan. J Vet Med Sci 2016;78:297–299.
- 5. ↑
Ceccolini ME, Macgregor SK, Spiro S, et al. Yersinia pseudotuberculosis infections in primates, artiodactyls, and birds within a zoological facility in the United Kingdom. J Zoo Wildl Med 2020;51:527–538.
- 6. ↑
Gamble KC, Clancy MM, eds. Infectious diseases of concern to captive and free ranging animals in North America. 2nd ed. Yulee, Fla: Infectious Disease Committee, American Association of Zoo Veterinarians, 2013;1098.
