History
A 2-year-old 120-g (0.26-lb) sexually intact female sugar glider was evaluated at a veterinary teaching hospital because of lethargy and anorexia of 1 day's duration. The sugar glider had been obtained along with another female 1 month prior to the evaluation. Both sugar gliders were housed in the same cage and fed a diet of pelleted food with fruits, vegetables, yogurt, mealworms, and a reptilian calcium supplement. The cagemate appeared clinically normal. On arrival at the hospital, the sugar glider was dehydrated with generalized weakness. Supportive care including SC fluid administration, oral supplementation with glucose and calcium gluconate, and oral administration of buprenorphine was provided but the patient died during the night before diagnostic tests were performed.
Gross Findings
At necropsy, the nutritional status of the sugar glider appeared to be good with adequate adipose tissues and skeletal muscles. All liver lobes contained multifocal to coalescing, random, pale, small (0.1- to 0.2-cm-diameter), relatively well-delineated foci with friable texture, flat contour, and soft consistency (Figure 1). The foci were visible on the surface as well as throughout the hepatic parenchyma. The intestines were diffusely distended by gas. The remaining visceral organs were unremarkable. Bones were grossly normal.
Formulate differential diagnoses from the history, clinical findings, and Figure 1—then turn the page→
Photograph of the liver from a 2-year-old sugar glider that had lethargy and anorexia of 1 day's duration and died despite supportive treatments. Notice the multifocal to coalescing, pale tan, small (0.1- to 0.2-cm-diameter) foci with flat contours and palpably soft to friable consistency randomly scattered throughout all lobes.
Citation: Journal of the American Veterinary Medical Association 250, 10; 10.2460/javma.250.10.1109
Photograph of the liver from a 2-year-old sugar glider that had lethargy and anorexia of 1 day's duration and died despite supportive treatments. Notice the multifocal to coalescing, pale tan, small (0.1- to 0.2-cm-diameter) foci with flat contours and palpably soft to friable consistency randomly scattered throughout all lobes.
Citation: Journal of the American Veterinary Medical Association 250, 10; 10.2460/javma.250.10.1109
Photograph of the liver from a 2-year-old sugar glider that had lethargy and anorexia of 1 day's duration and died despite supportive treatments. Notice the multifocal to coalescing, pale tan, small (0.1- to 0.2-cm-diameter) foci with flat contours and palpably soft to friable consistency randomly scattered throughout all lobes.
Citation: Journal of the American Veterinary Medical Association 250, 10; 10.2460/javma.250.10.1109
Histopathologic, Microbial, and Immunohistochemical Findings
Randomly scattered within the hepatic parenchyma were numerous multifocal and occasionally coalescing areas of coagulative necrosis surrounded by variable amounts of viable and degenerate neutrophils and macrophages mixed with fibrin and eosinophilic cellular and pyknotic and karyorrhectic nuclear debris (liquefactive necrosis [Figure 2]). Within the foci of necrosis, there were large numbers of primarily intracellular, basophilic, rod-shaped bacteria and multifocal fibrin thrombi. Adjacent, less affected hepatocytes contained variable amounts of clear discrete cytoplasmic vacuoles (lipid) and pale yellow, granular intracytoplasmic material (lipofuscin). Similar suppurative and necrotic areas were obscuring both the red and white pulp within the spleen as well as the cortices of the tracheal and mesenteric lymph nodes. The splenic white pulp contained numerous necrotic and apoptotic lymphocytes. The gastric and ileac lumens contained similar bacteria without any reactive inflammatory cells. Additionally, pulmonary alveolar septae and perivascular connective tissue were thickened by edema, and alveolar spaces contained foamy macrophages.
Aerobic bacterial culture of liver tissue samples was performed and yielded a heavy growth of Listeria monocytogenes. Immunohistochemical analysis for Listeria spp was performed on sections of liver with routinely used protocols, antibodies, and counterstains. Within the foci of necrosis, free bacterial colonies and surrounding macrophages had strong staining with anti-listerial antibody (Figure 3).
Photomicrographs of sections of the liver from the sugar glider in Figure 1. A—The liver has multifocal to coalescing foci of liquefactive and coagulative necrosis. H&E stain; bar = 200 μm. B—Notice that the foci of necrosis are characterized by both coagulative (arrowheads) and liquefactive (arrows) necrosis with retention of cellular architecture or replacement of normal architecture by cellular debris, respectively. Additionally, necrotic foci contain and are surrounded by neutrophils, macrophages, and clusters of primarily intracellular bacilli (asterisk). H&E stain; bar = 20 μm.
Citation: Journal of the American Veterinary Medical Association 250, 10; 10.2460/javma.250.10.1109
Photomicrographs of sections of the liver from the sugar glider in Figure 1. A—The liver has multifocal to coalescing foci of liquefactive and coagulative necrosis. H&E stain; bar = 200 μm. B—Notice that the foci of necrosis are characterized by both coagulative (arrowheads) and liquefactive (arrows) necrosis with retention of cellular architecture or replacement of normal architecture by cellular debris, respectively. Additionally, necrotic foci contain and are surrounded by neutrophils, macrophages, and clusters of primarily intracellular bacilli (asterisk). H&E stain; bar = 20 μm.
Citation: Journal of the American Veterinary Medical Association 250, 10; 10.2460/javma.250.10.1109
Photomicrographs of sections of the liver from the sugar glider in Figure 1. A—The liver has multifocal to coalescing foci of liquefactive and coagulative necrosis. H&E stain; bar = 200 μm. B—Notice that the foci of necrosis are characterized by both coagulative (arrowheads) and liquefactive (arrows) necrosis with retention of cellular architecture or replacement of normal architecture by cellular debris, respectively. Additionally, necrotic foci contain and are surrounded by neutrophils, macrophages, and clusters of primarily intracellular bacilli (asterisk). H&E stain; bar = 20 μm.
Citation: Journal of the American Veterinary Medical Association 250, 10; 10.2460/javma.250.10.1109
Comments
The case described in the present report illustrates the macroscopic and microscopic lesions associated with septicemia secondary to listeriosis in a sugar glider. Sugar gliders (Petaurus breviceps) are small marsupials native to New Guinea and the eastern coast of Australia and are popular captive exotic pets in the United States. Sugar gliders are monogastric animals, with complex and largely unknown dietary requirements.1 Most of the common illnesses such as malnutrition, obesity, and nutritional osteodystrophy in captive sugar gliders can be attributed to inadequate husbandry.1 Published nutritional recommendations include providing nectar and varied sources of protein as well as small amounts of fresh fruits and vegetables.1 Providing fresh fruit or dairy products (as a source of protein) could presumably introduce the possibility of infection from foodborne pathogens, including L monocytogenes. To our knowledge, there is only 1 reported case of listeriosis in a captive sugar glider.2
Listeria monocytogenes is a non–spore-forming gram-positive bacterium that is ubiquitous in the environment, has a worldwide distribution, and can survive and multiply in a wide range of environmental temperatures and conditions. The pathogenesis of listeriosis is complex and not completely understood because there are various species-specific and strain-specific factors involved.3 Listeria monocytogenes is a facultative anaerobe and replicates inside host cells. Following consumption of Listeria-contaminated material or food, the bacteria are able to penetrate the mucosal barrier through interactions of internalin and E-cadherin4 as well as other non-internalin proteins.5 When phagocytized by the host immune cells, the organism is able to lyse the phagosome and enter the cytosol via activation of pore-forming proteins such as listeriolysin O.3,6 Listeria monocytogenes replicates in the host cell cytoplasm and uses the host cell actin filaments to migrate to the cell membrane and induce protrusions of the cell membrane for transfer to adjacent cells, thereby avoiding exposure to the host's extracellular immune system.4,6 Presumably, the bacteria are then able to spread to the liver, spleen, and mesenteric lymph nodes where attempts to clear and inactivate the organisms are made by the resident macrophages, neutrophils, natural killer cells, and cytotoxic T cells.3 If the immune system is unsuccessful, L monocytogenes is able to disseminate and infect other organs including the brain and uterus.5,6 Additionally, in cases of listerial encephalitis in ruminants, the bacteria can breach the oral mucosa and travel directly to the brain via axons of the trigeminal nerve.6
Photomicrographs of a section of the liver from the sugar glider in Figure 1 following Listeria-specific immunohistochemical staining. Bacterial colonies and macrophages within and surrounding foci of necrosis are strongly stained (dark brown) with anti-listerial antibody. Listeria-specific immunohistochemical reaction; bar = 200 μm. Inset—At higher magnification, the specific targeting of the stain is more evident. Listeria-specific immunohistochemical reaction; bar = 20 μm.
Citation: Journal of the American Veterinary Medical Association 250, 10; 10.2460/javma.250.10.1109
Photomicrographs of a section of the liver from the sugar glider in Figure 1 following Listeria-specific immunohistochemical staining. Bacterial colonies and macrophages within and surrounding foci of necrosis are strongly stained (dark brown) with anti-listerial antibody. Listeria-specific immunohistochemical reaction; bar = 200 μm. Inset—At higher magnification, the specific targeting of the stain is more evident. Listeria-specific immunohistochemical reaction; bar = 20 μm.
Citation: Journal of the American Veterinary Medical Association 250, 10; 10.2460/javma.250.10.1109
Photomicrographs of a section of the liver from the sugar glider in Figure 1 following Listeria-specific immunohistochemical staining. Bacterial colonies and macrophages within and surrounding foci of necrosis are strongly stained (dark brown) with anti-listerial antibody. Listeria-specific immunohistochemical reaction; bar = 200 μm. Inset—At higher magnification, the specific targeting of the stain is more evident. Listeria-specific immunohistochemical reaction; bar = 20 μm.
Citation: Journal of the American Veterinary Medical Association 250, 10; 10.2460/javma.250.10.1109
For unknown reasons, typically only 1 of the 3 recognized syndromes—septicemia, encephalitis, and infection of the uterus or abortion—develops in an infected animal.6 Nonclinical carriers as well as infected, sick animals shed bacteria in the feces, and the organisms can survive in the environment for up to 2 years.7 Susceptibility to infection and development of syndromes are highly variable among species. Cattle, lagomorphs, and chinchillas are highly susceptible to listeriosis; unless immunocompromised, infected dogs, cats, guinea pigs, and rats are less likely to develop clinical signs.3 Ruminants are typically infected after ingestion of contaminated silage, which results in listerial encephalitis or late-term abortion.3,6 Dogs, cats, and captive small mammals (including chinchillas, rabbits, rats, and guinea pigs) have been infected with L monocytogenes from contaminated habitats and food sources.2,3 Septicemia is the most common finding in these species following infection.3 There are reports of listeriosis in several different marsupials in Australia including Antechinus sp, a ringtail possum (Pseudocheirus peregrinus), a rednecked wallaby (Macropus rufogriseus), a cuscus, and a rufous bettong (Aepyprymnus rufescens).4 Gross and histologic findings in Australian marsupials, including multifocal hepatic necrosis with infiltration by neutrophils and macrophages,2,4 are consistent with those for the sugar glider of the present report.
The source of infection for the sugar glider of the present report was not determined. Contaminated food items were considered a likely source, but were unavailable for testing. The incubation period of listeriosis in animals is variable depending on the species and can be as long as 70 days in humans.8 Because the incubation period of Listeria spp in sugar gliders is not known,5 it is also possible that the animal was infected with L monocytogenes prior to acquisition by the client. It is unknown whether the cagemate developed similar clinical signs, but it appeared clinically normal when the ill sugar glider was initially evaluated.
References
1. Ness RD, Johnson-Delaney CA. Chapter 29: Sugar gliders. In: Ferrets, rabbits and rodents, clinical medicine and surgery. 3rd ed. St Louis: Saunders, 2012; 393–410.
2. Nichols M, Takacs N, Ragsdale J, et al. Listeria monocytogenes infection in a sugar glider (Petaurus breviceps) – New Mexico, 2011. Zoonoses Public Health 2015: 62:254–257.
3. Hoelzer K, Pouillot R, Dennis S. Animal models of listeriosis: a comparative review of the current state of the art and lessons learned. Vet Res 2012; 43: 18.
4. Ladds PW. Chapter 7: Bacterial diseases in terrestrial mammals. In: Pathology of Australian native wildlife. Collingwood, VIC, Australia: CSIRO, 2009: 65–113.
5. Carvalho F, Sousa S, Cabanes D. How Listeria monocytogenes organizes its surface for virulence. Front Cell Infect Microbiol 2014: 4:48.
6. Maxie MG, Youssef S. Nervous system. In: Maxie MG, ed. Jubb, Kennedy, and Palmer's pathology of domestic animals. Vol 1. 5th ed. Philadelphia: Elsevier Saunders; 2007: 405–408.
7. Schlafer DH, Miller RB. Female genital system. In: Maxie MG, ed. Jubb, Kennedy, and Palmer's pathology of domestic animals. Vol 1. 5th ed. Philadelphia: Elsevier Saunders; 2007: 429–564.
8. Greene CE. Listeriosis: streptococcal and other gram positive bacterial infections. In: Greene's infectious disease of the dog and cat. 3rd ed. St Louis: Elsevier, 2006; 311–312.
