History

A juvenile (unspecified age) male red-tailed hawk (Buteo jamaicensis) was presented to the Southeastern Raptor Center, unable to fly.

Clinical and Gross Findings

The animal was thin and dehydrated, with muffled heart sounds and head tilt. After clinical examination, the patient was put on SC fluids, assisted feeding, and analgesics (Meloxicam). Ancillary blood tests revealed low lead concentration (< 40 µg/dL or 0.4 ppm), ruling out lead poisoning; PCV, 32% (reference value, 24.0% to 50.0%); and total protein, 4.2 g/dL (reference value, 2.00 g/dL to 5.00 g/dL). After 4 days of hospitalization, the animal died overnight.

On postmortem examination, the hawk was in good nutritional condition, characterized by having a robust muscular pectoral mass. The left pectoral muscle had multifocal to coalescent tan discoloration. The coelomic cavity was filled with approximately 3 mL of translucent to pale amber gelatinous fluid mostly surrounding the hepatic left and right lobes and within the hilum (Figure 1). The pericardium had small amounts of translucent fluid, < 0.1 mL. The liver was diffusely dark brown and oozed moderate amounts of blood on cut surface, indicating congestion. The heart was mottled tan and dark red, especially on the right ventricle. No other significant alterations were grossly noted at necropsy.

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Photographs of the coelomic cavity with abundant gelatinous yellowish fluid surrounding the congested liver, accompanied by mild hydropericardium (A) and right ventricle with extensive subepicardial hemorrhage (B) of a juvenile male red-tailed hawk.

Citation: Journal of the American Veterinary Medical Association 261, 2; 10.2460/javma.22.08.0376

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Histopathologic and Microbiological Findings

Microscopic evaluation of the heart revealed abundant lymphocytes, plasma cells, and histiocytes expanding the myocardial interstitium, disrupting cardiomyocytes, and extending onto the endocardium, epicardium, and epicardial adipose tissue of the left and right ventricular free walls, as well as the interventricular septum (Figure 2). The cardiomyocytes were hypereosinophilic and/or fragmented with loss of cross striations, with pyknotic or karyolytic nuclei (necrosis). Similar inflammatory cells obscured the cardiac plexi ganglia.

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Photomicrographs of sections of formalin-fixed paraffin-embedded tissues from the red-tailed hawk in Figure 1. A—The myocardial interstitium is infiltrated by mononuclear cells. H&E stain; bar = 100 µm. Mononuclear infiltrate is composed by lymphocytes, plasma cells, and histiocytes (inset). H&E stain; bar = 20 µm. B—The cardiomyocytes are hypereosinophilic and fragmented with loss of cross striations. H&E stain; bar = 10 µm.

Citation: Journal of the American Veterinary Medical Association 261, 2; 10.2460/javma.22.08.0376

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In the pectoral muscle, there were multiple degenerate and necrotic myocytes accompanied by moderate numbers of histiocytes and lymphocytes infiltrating the endomysium and perimysium. In the cloaca and caudal coelomic wall, focal aggregates of similar mononuclear inflammation obscured the muscular layers, and bursal follicles were markedly depleted. Within the liver, there was multifocal mild lymphoplasmacytic portal hepatitis. No inflammatory changes were observed within the eyes or brain. The remaining evaluated tissues were histologically unremarkable.

Reverse transcriptase PCR for West Nile virus (WNV) performed on a pool of heart and brain tissue was positive (cycle threshold value of 16.2). Avian influenza matrix was not detected on real-time reverse transcriptase PCR of oropharyngeal swab.

Morphologic Diagnosis and Case Summary

Morphologic diagnosis and case summary: (1) lymphoplasmacytic and histiocytic necrotizing pancarditis, (2) lymphohistiocytic and necrotizing pectoral myositis, (3) lymphoplasmacytic portal hepatitis, and (4) bursal lymphoid depletion, associated with WNV infection.

Comments

West Nile virus is an arthropod-borne virus belonging to the genus Flavivirus, family Flaviviridae.¹ The virus was introduced in the US for the first time in 1999.¹ It is transmitted by ornithophilic mosquitoes as competent vectors, within an enzootic cycle. Culicidae mosquitoes are the group predominantly responsible for maintaining the sylvatic cycle of the virus.¹ Birds play an important role in the flavivirus spread and epidemiology. Wild birds are amplifying hosts and contribute to the dissemination of these agents through their migratory behavior. Besides birds, WNV can infect a wide variety of vertebrates, including amphibians, reptiles, and mammals; however, other vertebrates represent dead-end hosts.¹ The bird-mosquito-bird transmission cycle sporadically results in epidemics that can affect horses and humans.¹ Flaviviral infection has been implicated as a cause of encephalitis and mortality in wild birds, humans, and horses.¹ Humans and horses are incidental hosts and develop a fatal disease.² West Nile virus is considered one of the most important pathogens causing viral neurological disease in humans.¹

Wild raptors are at the top of the food chain, important in ecosystem diversity and sustainability, and indicators of environmental health.¹ Several species of raptors (orders Falconiformes and Strigiformes) have been reported to be susceptible to WNV infection. Eagles, hawks, and falcons are considered extremely prompt to develop encephalitis.¹ Experimental WNV infections in raptors suggest that numerous species are reservoir competent and develop infectious level viremia and often survive the infection.² The potential impact of WNV infection in raptors in North America is unknown.¹ Although numerous raptors present illness and injuries associated with the virus, the proportion of animals that is infected and dies in the wild is unknown.¹ Thus, in some areas of the US and Canada, high proportions of raptors infected with WNV may jeopardize the wild populations and alter the ecosystems.² Also, 1 study¹ suggests that animals recovered from WNV infection may have a subclinical level of histopathologic damage due to myocarditis and encephalitis that could decrease their longevity in the wild. Predatory birds can acquire the infection by eating infected prey or being bitten by infected mosquitoes.³ For this reason, it is suspected that raptors are exposed to WNV more than other bird species that can only acquire the infection through a mosquito bite.³ Another form of transmission of WNV in wild raptors is contact transmission.¹ When large numbers of birds conglomerate, WNV transmission can occur with direct contact with infected birds through oral and cloacal secretions.¹ Since raptors do not tend to aggregate, this may not be an important form of transmission when compared to predation.¹

Flaviviral infection in raptors causes a broad range of clinical signs. Unspecific clinical manifestations include emaciation and dehydration.¹ Neurological signs are the most common clinical manifestation in captive raptors (golden eagles, great horned owls, and snowy owls), followed by sudden recumbency, mild ataxia, tetraparesis, tremors, nystagmus, seizure, head tilt, and disorientation.¹ Blindness, visual impairment, nystagmus, and abnormal pupillary responses are some of the reported ophthalmologic signs.¹ In this case, the clinical signs were unspecific (dehydration and incapacity to fly), with a head tilt.

Grossly, WNV-positive raptors may show ocular signs and evidence of trauma.⁴ For example, ocular signs like nystagmus, abnormal pupillary response, and blindness are reported in bald eagles, Cooper’s hawks, Northern goshawks, red-tailed hawks, and American kestrels with WNV detection via immunohistochemistry.¹ Concurrent infections with other nonviral pathogens such as bacterial septicemia, aspergillosis, and Leucocytozoon spp may be also detected.¹ Other gross lesions described in raptors are atrophy of pectoral muscles, cachexia with reduced subcutaneous and organ fat deposits, calvarial hemorrhages, meningeal hemorrhages, hepato- and splenomegaly, myocardium discoloration with or without subepicardial hemorrhages, mottled kidneys, serous atrophy of bone marrow, gastrointestinal dilatation, and cerebral atrophy and malacia.¹ Of those, only cardiac lesions were noted in this case, notably subepicardial ecchymoses. Coelomic effusion and hydropericardium from cardiac failure have not been formally reported in cases of WNV infection. The perihepatic and pericardial protein-rich exudate resembled the common lesion of “ascites syndrome” in poultry, caused by pulmonary hypertension. The 4 main mechanisms of ascites include high hydrostatic vascular pressure, decreased oncotic pressure, increased capillary permeability, and impaired lymphatic drainage.⁵ Increased capillary permeability can result from extensive inflammation, like the pancarditis evidenced on histology. Likewise, pulmonary hypertension also results in right ventricular hypertrophy, followed by dilatation, right ventricular failure, passive congestion, and then ascites.⁵ Thus, increased capillary permeability and right ventricular failure are contributing to the origin of ascites.

Histological lesions caused by WNV in raptors are more frequent in the heart and brain. Mononuclear necrotizing myocarditis, pectoral myositis, interstitial nephritis, meningoencephalitis and myelitis, optic neuritis, pectinitis, and iridocyclitis are commonly reported.¹ Other histopathologic findings include histiocytic hepatitis, necrosis of splenic ellipsoids, and lymphoplasmacytic aggregates in the pancreas, thyroid, skin, trachea, gastrointestinal tract (oropharynx, esophagus, ventriculus, proventriculus, and intestine).¹ In this case, the most significant lesion was pancarditis. Hepatitis and pectoral myositis were moderate. No histological lesions were identified in the eye or brain.

This case describes hydropericardium and protein-rich coelomic effusion secondary to severe generalized pancarditis and cardiac failure in a raptor associated with WNV.