Clinical Aspects of West Nile Virus Infection in a Zoological Collection
IAAAM 2000
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

Abstract

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

Asymptomatic

Morbidity

Seroconversion
and recovery

Mortality

Anseriformes

Abbysinian blue-winged goose

Cyanochen cyanopterus

 

X

   

Roseybill duck

Netta peposcaca

X

     

Domestic goose

Anser anser

 

X

X

 

Trumpeter swan

Cygnus cygnus buccinator

 

X

   

Charadriiformes

Grey gull

Larus modesta

 

X

   

Laughing gull

Larus atricilla

 

X

X

X

Inca tern

Larosterna inca

 

X

   

Ciconiiformes

Waldrapp ibis

Geronticus eremita

 

X

   

Black crowned night heron

Nycticorax nycticorax

 

X

   

Lesser adjutant stork

Leptoptilos javanicus

 

X

   

Columbiformes

Bleeding heart pigeon

Gallicolumba luzonica

 

X

   

Mauritius pink pigeon

Columba mayeri

   

X

 

Cuculiformes

Lady Ross' plantain eater

Musophaga rossae

 

X

   

Falconiformes

King vulture

Sarcorhamphus papa

 

X

   

Galliformes

Blythes Tragopan

Tragopan blythi

X

     

Domestic chicken

Gallus gallus

 

X

   

Green junglefowl

Gallus varius

 

X

   

Kenya crested guineafowl

Guttera pucherani

 

X

X

 

Bulwar's wattled pheasant

Lophura bulweri

 

X

   

Himalayan impeyan pheasant

Lophophorus impeyanus

 

X

   

Mountain peacock pheasant

Polyplectron inopinatum

 

X

   

Green crested wood partridge

Rollulus roulroul

X

     

Gruiformes

Manchurian crane

Grus japonensis

 

X

   

Hooded crane

Grus monacha

 

X

   

White naped crane

Grus vipio

 

X

   

Passeriformes

Brown sicklebill bird of paradise

Epimachus meyeri

 

X

   

Pelecaniformes

Guanay cormorant

Phalacrocorax bougainvillei

 

X

X

 

American white pelican

Pelecanus erythrorhynchos

 

X

   

Brown pelican

Pelecanus occidentalis

 

X

   

Phoenicopteriformes

Chilean flamingo Phoenicopterus chilensis

 

X

X

X

 

Sphenisciformes

Megellanic penguin

Spheniscus magellanicus

 

X

   

Strigiformes

Barred Owl

Strix varia

 

X

   

Milky eagle owl

Bubo lacteus

 

 

X

 

Snowy owl

Nyctea scandiaca

 

 

X

 

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.

Acknowledgments

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.

References

1.  Anderson JF, TG Andreadis, CR Vossbrinck, S Tirrell, EM Wakem, RA French, AE Garmendia, HJVan Kruiningen. 1999. Isolation of West Nile virus from mosquitoes, crows, and a cooper's hawk in Connecticut. Science 286: 2331-2333.

2.  Asnis D, Conetta R, Waldman G, Teixeira A, McNamara T, Fine A, Layton M, Miller J, Cimini D, et al. 1999. Outbreak of West Nile-like viral encephalitis B New York, 1999. Morbidity and Mortality Weekly Report 48 (38): 845-849.

3.  Komar N. 2000. West Nile encephalitis. Revue Scientifique et Techhique-Office International des Epizooties 19(1): 166-176.

4.  Lanciotti RS, JT Roehrig, V Deubel, J Smith, M Parker, K Steele, B Crise, KE Volpe, MB Crabtree, JH Scherret, RA Hall, JS MacKenzie, CB Cropp, B Panigrahy, E Ostlund, B Schmitt, M Malkinson, C Banet, J Weissman, N Komar, HM Savage, W Stone, T McNamara, DJ Gubler. 1999. Origin of the West Nile virus responsible for an outbreak of encephalitis in the Northeastern United States. Science 286: 2333-2337.

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
(click the speaker's name to view other papers and abstracts submitted by this speaker)

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


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