Avian Diseases 47(3):602-610. 2003
doi: 10.1637/6088

Clinical and Pathologic Features of West Nile Virus Infection in Native North American Owls (Family Strigidae)

S. D. Fitzgerald, J. S. Patterson, M. Kiupel, H. A. Simmons, S. D. Grimes, C. F. Sarver, R. M. Fulton, B. A. Steficek, T. M. Cooley, J. P. Massey, and J. G. Sikarskie

aDiagnostic Center for Population and Animal Health and Department of Small Animal Clinical Sciences, College of Veterinary Medicine, Michigan State University, East Lansing, MI 48824

bAnimal Disease Diagnostic Laboratory, Division of Animal Industry, Ohio Department of Agriculture, Reynoldsburg, OH 43068

cWildlife Disease Laboratory, Michigan Department of Natural Resources, East Lansing, MI 48823

dMolecular Biology Section, Michigan Department of Community Health, Lansing, MI 48909

Abstract

Since the initial report of West Nile virus in the northeastern United States in 1999, the virus has spread rapidly westward and southward across the country. In the summer of 2002, several midwestern states reported increased cases of neurologic disease and mortality associated with West Nile virus infection in various native North American owl species. This report summarizes the clinical and pathologic findings for 13 captive and free-ranging owls. Affected species were all in the family Strigidae and included seven snowy owls (Nyctea scandiaca), four great-horned owls (Bubo virginianus), a barred owl (Strix varia), and a short-eared owl (Asio flammeus). Neurologic signs identified included head tilt, uncoordinated flight, paralysis, tremors, and seizures. Owls that died were screened for flaviviral proteins by immunohistochemical staining of formalin-fixed tissues, followed by specific polymerase chain reaction assay to confirm West Nile virus with fresh tissues when available. Microscopic lesions were widespread, involving brain, heart, liver, kidney, and spleen, and were typically nonsuppurative with infiltration by predominantly lymphocytes and plasma cells. Lesions in owls were much more severe than those previously reported in corvids such as crows, which are considered highly susceptible to infection and are routinely used as sentinel species for monitoring for the presence and spread of West Nile virus. This report is the first detailed description of the pathology of West Nile virus infection in Strigiformes and indicates that this bird family is susceptible to natural infection with West Nile virus.

Resumen

Características clínicas y patológicas de la infección por el virus del Nilo en búhos nativos de Norteamérica (familia Strigidae).

Después del reporte inicial de la presencia del virus del Nilo en Estados Unidos en 1999, el mismo se ha diseminado rápidamente hacia el este y sur del país. En el verano del 2002, algunos estados de la región del oeste medio de los Estados Unidos reportaron un aumento de los casos de enfermedades neurológicas y mortalidad asociadas a infecciones por el virus del Nilo en varias especies de búhos nativos de Norteamérica. En este reporte se describen los hallazgos clínicos y patológicos encontrados en 13 búhos en cautiverio y silvestres. Todas las especies afectadas pertenecían a la familia Strigidae, incluyendo siete búhos nivales (Nyctea scandiaca), cuatro búhos de Virginia (Bubo virginianus), un cárabo de franjas (Strix varia) y una lechuza campestre (Asio flammeus). Los signos neurológicos observados incluyeron inclinación de la cabeza, incoordinación en el vuelo, parálisis, temblores y convulsiones. Los tejidos de las aves que murieron fueron utilizados para la detección de proteínas del flavivirus mediante el uso de la técnica de inmunohistoquímica, después de que los mismos fueron fijados en formalina. También se utilizó la prueba de reacción en cadena por la polimerasa para confirmar la presencia del virus en tejidos frescos en los casos en donde este tipo de muestra fue accesible. Se encontraron lesiones microscópicas en varios órganos, incluyendo el cerebro, corazón, hígado, riñones y bazo, las cuales fueron en su mayoría de tipo no supurativo con infiltraciones de linfocitos y células plasmáticas principalmente. Las lesiones en los búhos fueron mucho más severas que las reportadas previamente en aves pertenecientes a la familia de los córvidos, tales como los cuervos, los cuales son considerados como altamente susceptibles a la infección y son rutinariamente utilizados como aves centinelas para la detección de la presencia y diseminación del virus del Nilo. Este reporte es el primero en ofrecer una descripción detallada de la patología de la infección por el virus del Nilo en aves pertenecientes al grupo de los Strigiformes, y se concluye que esta familia de aves es susceptible a la infección natural por el virus del Nilo.

Abbreviations: Ct = threshold cycle number, DCPAH = Diagnostic Center for Population and Animal Health, ELISA = enzyme-linked immunosorbent assay, FAM = fluorescent detector molecule, H&E = hematoxylin and eosin, IHC = immunohistochemical, MDCH = Michigan Department of Community Health, PCR = polymerase chain reaction, RT = reverse transcriptase, TAMRA = fluorescent quencher molecule, WNV = West Nile virus

Received: November 4, 2002



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Fig. 1. Photomicrographs of tissues from owls with West Nile virus infection. (a) Heart with severe necrotizing myocarditis, heavy mixed mononuclear leukocyte infiltrates, and remnants of necrotic cardiomyocytes. Hematoxylin and eosin (H&E). Bar = 60 μm. (b) Brain with moderate perivascular cuffing of a large cerebral vessel by mononuclear leukocytes. H&E. (c) Kidney with expansion of the cortical interstitium by mixed mononuclear leukocyte infiltrates. H&E

Fig. 2. Photomicrographs of owl tissues exhibiting positive IHC staining against West Nile virus antigen. (a) Myocardium with extensive dark immunostaining of cardiomyocytes and histiocytes. Bar = 60 μm. (b) Kidney with scattered dark immunostaining of histiocytes and tubular epithelial cells (arrowheads). Bar = 60 μm. (c) Brain containing a single neuron (arrow) exhibiting diffuse cytoplasmic immunostaining. Bar = 40 μm

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