Clinical Aspects of West Nile Virus Infection in a Zoological Collection
IAAAM Archive
Paul P. Calle1, VMD, DACZM; George V. Ludwig2, PhD; Jonathan F. Smith2, PhD; Bonnie L. Raphael1, DVM, DACZM; Tracy L. Clippinger1, DVM, DACZM; Elizabeth M. Rush, DVM; Tracey McNamara1, DVM, DACVP; Rosandra Manduca1, DVM; Michael Linn1, DVM; Michael J. Turell2, PhD; Randal J. Schoepp2, PhD; Tom Larsen2; Joe Mangiafico2, MPH; Keith E. Steele2, DVM, DACVP; Robert A. Cook1, VMD
1Wildlife Health Sciences, Wildlife Conservation Society, Bronx, NY, USA; 2United States Army Medical Research Institute of Infectious Diseases, Frederick, MD, USA


During the summer and fall of 1999 an outbreak of human viral encephalitis occurred in New York City, with the earliest case onset 5 August 1999.2 This was later determined to result from infection with a strain of West Nile virus (WNV), a mosquito transmitted flavivirus, that was identical to a strain that circulated in Israel in 1998 and was the first documented occurrence of WNV in the Western Hemisphere.4 Human cases were preceded by a WNV epornitic in free ranging birds [especially common crows (Corvus brachyrhynchos) and fish crows (Corvus ossifragus)] in New York, with later involvement of birds in Connecticut and New Jersey.1,4,5 Later, nondomestic captive birds in the collections of the Wildlife Conservation Society/Bronx Zoo (WCS) were infected with WNV with resulting morbidity and mortality.4,5 Illnesses and deaths also occurred in horses (Equus caballus) in New York.3,4

A WNV serologic survey of the WCS collection was performed to confirm infection of clinical cases, assess the extent of WNV exposure, and to investigate when the virus was introduced to the collection. Heparinized plasma or serum samples were tested by a plaque reduction neutralization assay. There were no differences in test results between serum or plasma samples.

Avian serologic testing was conducted on 315 samples obtained between 6 June 1999 and 8 February 2000 from 277 individual birds (74 species in 16 orders). WNV specific antibodies were not detected in any of the 36 birds housed indoors, while 39% (94/241) of birds (34 species in 13 orders) housed in enclosures with a potential for mosquito exposure had WNV specific antibodies (Table 1). Based on these serologic results, avian WNV infections were most often asymptomatic (78.7%; 74/94). Clinical illness was recognized in 21.3% (20/94) of infected birds, with a high case fatality rate (nine of these 20 birds recovered and 11 died). Most of the birds that recovered only had mild clinical signs. This serologic survey underestimates the actual avian collection mortality, since some birds died peracutely without serologic testing. None of the archived samples from 39 individual seropositive birds (obtained between 17 February 1995 and 27 May 1999) were confirmed to have WNV specific antibodies. The earliest serologic confirmation of WNV infection at WCS was in a bird on 9 August 1999, after the outbreak had already been recognized in free ranging crows and in humans. All six of the birds imported by the WCS in 1999 had completed the federally mandated 30-day quarantine at a USDA quarantine facility remote from the outbreak origin. When sampled in October 1999 (3-4 mo after arrival at WCS), none had WNV specific antibodies.

The clinical signs of WNV infection in WCS collection birds were usually nonspecific. Some were found dead with no premonitory signs. Many exhibited depression, anorexia, weakness, weight loss, and recumbency. However, several birds had neurologic abnormalities including abnormal head or neck posture, ataxia, tremors, circling, disorientation, unilateral or bilateral posterior paresis, and impaired vision. The course of clinical illness was usually less than 1 wk, but ranged from 1-24 days before recovery or death. Hematologic and biochemical changes were variable and nonspecific.

Mammalian serologic testing was conducted on 116 samples obtained between 5 August 1999 and 31 January 2000 from 104 individual mammals (33 species in seven orders). None of the three mammals housed indoors, but 5.9 % (6/101) of mammals housed outdoors, had WNV specific antibody. These included five Asian species in four Orders [two Indian elephants (Elephas maximus indicus), one greater Indian rhinoceros (Rhinoceros unicornis), one babirusa (Babyrousa babyrussa), one lesser panda (Ailurus fulgens fulgens), and one snow leopard (Panthera uncia)]. Retrospective analysis of banked samples demonstrated seroconversion of one elephant between 12 August 1999 and 24 September 1999. An archived sample from the rhinoceros obtained in September 1994 was negative. None of the eight equids of three species [donkey (Equus asinus asinus), domestic miniature horse, or Przewlaski's horse (Equus przewalskii)] tested had WNV specific antibody.

Most mammal WNV infections were asymptomatic. A greater Indian rhinoceros developed depression, anorexia, and a lip droop and spontaneously recovered. A second greater Indian rhinoceros developed similar clinical signs and also recovered, but a blood sample was not obtained from that animal.

WCS halted shipments of birds to other institutions at the onset of the collection bird epornitic, before the cause of the outbreak had been identified. When shipments were resumed, only indoor birds without mosquito exposure or outdoor birds seronegative after the mosquito exposure season ended were approved for shipment. The source of WNV responsible for the New York outbreak is unknown but it is speculated that it may have entered the United States by way of an infected person, an illegally imported bird or domestic pet, or an unintentionally introduced virus-infected tick or mosquito.4 WNV is documented to have persisted throughout the winter in both a bird and mosquitoes. It is therefore widely feared that there might be future, recurrent outbreaks of WNV infection in people, horses, and both captive and free-ranging birds in the Northeastern United States. In addition, there is a potential for dissemination of WNV to other parts of the country through the movements of infected people, captive or domestic mammals or birds, free-ranging migratory birds, or virus infected mosquitoes.

Table 1. Results of West Nile virus infection in seropositive avian species at the Wildlife Conservation Society.

Order / Common name

Latin name

Result of avian West Nile virus infection



and recovery



Abbysinian blue-winged goose

Cyanochen cyanopterus




Roseybill duck

Netta peposcaca



Domestic goose

Anser anser





Trumpeter swan

Cygnus cygnus buccinator





Grey gull

Larus modesta




Laughing gull

Larus atricilla





Inca tern

Larosterna inca





Waldrapp ibis

Geronticus eremita




Black crowned night heron

Nycticorax nycticorax




Lesser adjutant stork

Leptoptilos javanicus





Bleeding heart pigeon

Gallicolumba luzonica




Mauritius pink pigeon

Columba mayeri





Lady Ross' plantain eater

Musophaga rossae





King vulture

Sarcorhamphus papa





Blythes Tragopan

Tragopan blythi



Domestic chicken

Gallus gallus




Green junglefowl

Gallus varius




Kenya crested guineafowl

Guttera pucherani





Bulwar's wattled pheasant

Lophura bulweri




Himalayan impeyan pheasant

Lophophorus impeyanus




Mountain peacock pheasant

Polyplectron inopinatum




Green crested wood partridge

Rollulus roulroul




Manchurian crane

Grus japonensis




Hooded crane

Grus monacha




White naped crane

Grus vipio





Brown sicklebill bird of paradise

Epimachus meyeri





Guanay cormorant

Phalacrocorax bougainvillei





American white pelican

Pelecanus erythrorhynchos




Brown pelican

Pelecanus occidentalis





Chilean flamingo Phoenicopterus chilensis







Megellanic penguin

Spheniscus magellanicus





Barred Owl

Strix varia




Milky eagle owl

Bubo lacteus





Snowy owl

Nyctea scandiaca





Editor's Note: From the original pdf it is impossible to tell where the last 2 x's belong. Does Morbidity belong with seroconversion, i.e., only three x columns.


The authors acknowledge and thank the WCS veterinary technicians; the WCS Departments of Education, Mammalogy, and Ornithology; and the technical staff of the Research Serology Branch and Pathology Division, USAMRIID, whose assistance made this project possible.


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5.  Steele KE, MJ Linn, RJ Schoepp, N Komar, TW Geisbert, RM Manduca, PP Calle, BL Rapheal, TL Clippinger, T Larsen, J Smith, RS Lanciotti, NA Panella, TS McNamara. 2000. Pathology of fatal West Nile virus infections in native and exotic birds during the 1999 outbreak in New York City. Veterinary Pathology 37(3): 208-224.

Speaker Information
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Paul P. Calle, VMD, DACZM
Wildlife Health Sciences, Wildlife Conservation Society
Bronx, NY, USA

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