Signalment and History

Between end of September and beginning of October two juvenile, intact male coyotes were received for necropsy from different submitters and locations. The first coyote (coyote #1) was found dead in a yard, and the second coyote (coyote #2) was found roadside non-responsive and was euthanized at a wildlife rehabilitation clinic. Both animals were submitted for postmortem examination.

Gross Findings

Both coyotes were emaciated. The lung lobes were voluminous, heavy, wet, and mottled dark red to tan, with multifocal to coalescing areas of consolidation involving approximately 40–60% of the pulmonary parenchyma, most prominent in the cranioventral regions. On cut section of the lungs from coyote #2, pus oozed from the consolidated areas.

Figure 1: Coyote#1 – The cranioventral lung lobes were red to dark red, voluminous and consolidated.

Histopathology

Lung (Figure 2. A&B): Approximately 40–60% of the pulmonary parenchyma is affected by a severe, multifocal to coalescing, necrotizing, suppurative to fibrinous bronchopneumonia. Affected bronchiolar lumina and adjacent alveolar spaces are variably filled with large numbers of degenerate and non-degenerate neutrophils, abundant fibrin, hemorrhage, proteinaceous fluid, and aggregates of bacteria. The bronchiolar epithelium is frequently attenuated to absent, and bronchiolar walls are multifocally necrotic and disrupted. In severely affected regions, the alveolar septa are obscured, fragmented, or effaced, resulting in marked destruction of normal pulmonary architecture.

Stomach (coyote #1, Figure 3): Within the gastric mucosa, numerous epithelial cells contain large, round to ovoid, intranuclear and intracytoplasmic eosinophilic inclusion bodies.

Figure 2: A. Lung, alveoli spaces are filled with numerous neutrophils, H&E. B. Lung, numerous degenerated neutrophils with myriads of bacterial aggregates, H&E. C. Strong cytoplasmic immunolabeling for canine distemper virus antigen, IHC-DAB.

Figure 3. Stomach mucosa, epithelial cells contain numerous intranuclear (black arrow) and intracytoplasmic (red arrow) eosinophilic, inclusion bodies, H&E.

Ancillary Testing

• Aerobic bacterial culture: Predominant growth of Salmonella spp. isolated from lung. Coyote #2: Salmonella spp. was also isolated from the liver sample.
• Immunohistochemistry (IHC): Coyote #1 - Abundant and strong immunolabelling for CDV antigen was present in the lungs (Figure 2. C) and brain. Coyote #2 - CDV antigen was not detected in the analyzed sections of lung.
• Virology (coyote #1 and 2): Samples of brain were negative for rabies virus antigen by direct fluorescent antibody (DFA) test (performed at the Minnesota Department of Health).
• Molecular diagnostics (only coyote #1): A bronchial swab was negative for influenza A virus (matrix gene) by PCR.

Morphologic Diagnosis

1. Lung (coyote #1 and 2): bronchopneumonia, necrotizing and suppurative, acute, marked.
2. Stomach (coyote #1 and 2), intranuclear and intracytoplasmic eosinophilic inclusion bodies in epithelial cells.

Etiology

Coyote #1 - Dual infection with Canine Distemper Virus (Morbillivirus) and Salmonella enterica serovar typhimurium (Salmonella sp. serotyping was performed at the USDA-NVSL).

Coyote #2 – Infection with Salmonella enterica serovar Dublin (Salmonella sp. serotyping was performed at the USDA-NVSL).

Comments

Canine distemper virus (CDV) is a morbillivirus affecting a wide range of carnivores and mustelids (among others). Due to its ability to infect multiple tissues (pantropism), as in domestic dogs, CDV infection in nondomestic canids, including coyotes, commonly results in respiratory and neurologic disease and can cause immunosuppression, ultimately predisposing infected animals to secondary infections, mostly by bacteria or protozoa. Characteristic microscopic lesions include broncho-interstitial pneumonia with epithelial necrosis, syncytial cell formation, and both intracytoplasmic and intranuclear inclusion bodies within e.g. respiratory epithelium, gastric epithelial cells, neurons, glial cells, and ependymal cells. In one of the cases described here, the secondary bacterial infection was sufficiently severe to cause extensive pulmonary parenchymal destruction, obscuring and overlapping the primary lesions attributable to CDV. However, inclusion bodies within the gastric mucosa raised the concern about the possible distemper virus infection which was then confirmed by immunohistochemistry.

Isolation of Salmonella spp. from the lungs in association with bronchopneumonia in coyotes was unexpected. However, Salmonella has been isolated from approximately 32% of coyote fecal samples in a study conducted along the U.S.–Mexican border. In Coyote #1, immunosuppression due to canine distemper virus (CDV) infection was considered the most likely predisposing factor for the secondary bacterial infection and resultant bronchopneumonia. In contrast, the absence of detection of inclusion bodies and the immunonegativity for CDV antigen in the second coyote indicates that clinically important Salmonella infection can occur independent of CDV-associated immunosuppression. Although splenic lymphoid depletion was observed in coyote #2, a definitive underlying cause of immunosuppression was not identified in the present case.

Coyotes may be exposed to Salmonella via access to garbage, landfills, irrigation ditches, sediment basins, and campsites, particularly in areas where natural food and water sources are limited. The coyote’s proximity to urban and agricultural environment and their hunting and scavenging behaviors may increase exposure to contaminated prey and carrion.

References

1. Jay-Russel et al.: Prevalence and Characterization of Escherichia coli and Salmonella Strains Isolated from Stray Dog and Coyote Feces in a Major Leafy Greens Production Region at the United States-Mexico Border. PLos One November 2014; https://doi.org/10.1371/journal.pone.0113433