|
|
Experimental Infection of
North American Birds with the New York 1999 Strain of West Nile Virus
Nicholas Komar,* Stanley Langevin,* Steven Hinten,* Nicole Nemeth,*
Eric Edwards,* Danielle Hettler,* Brent Davis,* Richard Bowen, and
Michel Bunning*
*Centers for Disease Control and Prevention, Fort Collins, Colorado, USA;
Colorado State University, Fort Collins, Colorado, USA; and Office of
the Surgeon General, United States Air Force, Bolling Air Force Base,
Washington, D.C., USA
| Table
1. Classification, sample sizes, types of transmission studies
and sources for 25 species of birds infected experimentally with West
Nile virus |
|
|
Common name
|
Latin name
|
Family
|
Order
|
# used
|
Transmission trialsa
|
Source type
|
|
|
Canada Goose
|
Branta canadensis
|
Anatidae
|
Anseriformes
|
3
|
M
|
Wild
|
|
Mallard
|
Anas platyrhynchos
|
Anatidae
|
Anseriformes
|
3
|
M, C
|
Commercial
|
|
American Kestrel
|
Falco sparverius
|
Falconidae
|
Falconiformes
|
5
|
M, O
|
Rehabilitator
|
|
Northern Bobwhite
|
Colinus virginianus
|
Odontophoridae
|
Galliformes
|
6
|
M, C, O
|
Commercial
|
|
Japanese Quail
|
Coturnix japonicus
|
Odontophoridae
|
Galliformes
|
6
|
M, C, O
|
Commercial
|
|
Ring-necked Pheasant
|
Phasianus colchicus
|
Phasianidae
|
Galliformes
|
3
|
M
|
Commercial
|
|
American Coot
|
Fulica americana
|
Rallidae
|
Gruiformes
|
2
|
M, C
|
Wild
|
|
Killdeer
|
Charadrius vociferus
|
Charadriidae
|
Charadriiformes
|
2
|
M
|
Wild
|
|
Ring-billed Gull
|
Larus delawarensis
|
Laridae
|
Charadriiformes
|
7
|
M, C
|
Wild
|
|
Mourning Dove
|
Zenaida macroura
|
Columbidae
|
Columbiformes
|
6
|
M, C, O
|
Wild
|
|
Rock Dove
|
Columba livia
|
Columbidae
|
Columbiformes
|
12
|
M, C
|
Commercial
|
|
Monk Parakeet
|
Myiopsitta monachus
|
Psittacidae
|
Psittaciformes
|
6
|
M, C, O
|
Commercial
|
|
Budgerigar
|
Melopsittacus undulatus
|
Psittacidae
|
Psittaciformes
|
6
|
M, C, O
|
Commercial
|
|
Great Horned Owl
|
Bubo virginianus
|
Strigidae
|
Strigiformes
|
2
|
M, O
|
Rehabilitator
|
|
Northern Flicker
|
Colaptes auratus
|
Picidae
|
Piciformes
|
5
|
M, O
|
Wild
|
|
Blue Jay
|
Cyanocitta cristata
|
Corvidae
|
Passeriformes
|
6
|
M, C
|
Wild
|
|
Black-billed Magpie
|
Pica hudsonia
|
Corvidae
|
Passeriformes
|
8
|
M, C, O
|
Wild
|
|
American Crow
|
Corvus brachyrhynchos
|
Corvidae
|
Passeriformes
|
22
|
M, C, O
|
Wild
|
|
Fish Crow
|
Corvus ossifragus
|
Corvidae
|
Passeriformes
|
20
|
M, C, O
|
Wild
|
|
American Robin
|
Turdus migratorius
|
Turdidae
|
Passeriformes
|
6
|
M, C, O
|
Wild
|
|
European Starling
|
Sturnus vulgaris
|
Sturnidae
|
Passeriformes
|
8
|
M, C
|
Wild
|
|
Red-winged Blackbird
|
Agelaius phoeniceus
|
Icteridae
|
Passeriformes
|
4
|
M
|
Wild
|
|
Common Grackle
|
Quiscalus quiscula
|
Icteridae
|
Passeriformes
|
12
|
M, C, O
|
Wild
|
|
House Finch
|
Carpodacus mexicanus
|
Fringillidae
|
Passeriformes
|
3
|
M, C, O
|
Wild
|
|
House Sparrow
|
Passer domesticus
|
Passeridae
|
Passeriformes
|
15
|
M, C, O
|
Wild
|
|
| aM, mosquito-exposed;
C, contact-exposed; O, orally exposed. |
| Table
2. Mean West Nile virus viremia levels (shown as log10
PFU/mL serum, with ranges) for each of 7 days postinoculation by mosquito
bite, and mean duration of detectable viremia (days, with ranges)a,b |
|
|
Species
|
Day postinoculation
|
Duration of viremia
|
| |
|
|
n
|
1
|
2
|
3
|
4
|
5
|
6
|
7
|
|
|
Canada Goose
|
3
|
2.8
(<1.73.0)
|
5.3
(3.25.8)
|
4.5
(3.54.8)
|
3.4
(<1.73.8)
|
1.9
(<1.72.0)
|
<1.7
|
<1.7
|
4.0
(35)
|
|
Mallard
|
2
|
6.1
(<1.76.4)
|
5.7
(5.55.9)
|
6.7
(3.47.0)
|
5.1
(1.75.4)
|
4.7
(<1.75.0)
|
<1.7
|
<1.7
|
4.0
(44)
|
|
American Kestrel
|
2
|
6.2
(5.56.4)
|
8.4
(5.88.7)
|
6.6
(6.16.8)
|
3.8
(3.64.0)
|
2
(<1.72.3)
|
<1.7
|
<1.7
|
4.5
(45)
|
|
Northern Bobwhite
|
3
|
2.8
(1.73.1)
|
2.9
(2.33.3)
|
2.0
(1.72.2)
|
1.9
(<1.72.4)
|
1.2
(<1.71.7)
|
<1.7
|
<1.7
|
4.0
(35)
|
|
Japanese Quail
|
3
|
<1.7
|
<1.7
|
2.8
(<1.73.3)
|
3.4
(<1.73.9)
|
3.1
(<1.73.6)
|
2.2
(<1.7-2.7)
|
<1.7
|
1.3
(04)
|
|
Ring-necked Pheasant
|
3
|
2.1
(<1.72.3)
|
2.8
(<1.73.2)
|
2.6
(1.73.0)
|
1.8
(1.72.0)
|
1.2
(<1.71.7)
|
<1.7
|
<1.7
|
3.7
(34)
|
|
American Coot
|
1
|
<1.7
|
3.4
|
4.5
|
4.6
|
2.8
|
<1.7
|
<1.7
|
4.0
|
|
Killdeer
|
2
|
6.2
(5.96.4)
|
7.5
(6.57.8)
|
8.1
(4.38.4)
|
4.9
(2.15.2)
|
2.6
(<1.72.9)
|
<1.7
|
<1.7
|
4.5
(45)
|
|
Ring-billed Gull
|
2
|
5.4
(5.45.4)
|
7.8
(6.58.1)
|
8.0
(5.48.3)
|
7.4
(2.97.7)
|
7.2
|
5.3
|
4.1
|
5.5
(47)
|
|
Mourning Dove
|
3
|
4.8
(3.05.3)
|
5.9
(3.96.3)
|
5.6
(3.45.9)
|
3.3
(<1.73.6)
|
<1.7
|
<1.7
|
<1.7
|
3.7
(34)
|
|
Rock Dove
|
6
|
3.5
(<1.74.0)
|
4.3
(3.54.8)
|
4.2
(3.54.5)
|
2.9
(<1.73.7)
|
NT
|
NT
|
NT
|
3.2
(34)
|
|
Monk Parakeet
|
3
|
2.8
(<1.73.0)
|
3.6
(<1.74.0)
|
3.5
(<1.73.9)
|
1.7
(<1.72.0)
|
<1.7
|
<1.7
|
<1.7
|
2.7
(04)
|
|
Budgerigar
|
3
|
2.3
(<1.72.8)
|
1.9
(<1.72.4)
|
2.8
(<1.73.3)
|
2.9
(<1.73.4)
|
2.1
(<1.72.6)
|
<1.7
|
<1.7
|
1.7
(04)
|
|
Great Horned Owl
|
1
|
3.9
|
6.2
|
7.6
|
6.0
|
5.6
|
3.5
|
<1.7
|
6.0
|
|
Northern Flicker
|
1
|
3.9
|
4.9
|
5.4
|
3.9
|
<1.7
|
<1.7
|
<1.7
|
4.0
|
|
Blue Jay
|
4
|
8.5
(5.68.8)
|
11.1
(7.811.6)
|
12.1
(7.512.6)
|
10.5 (5.011.0)
|
2.2
|
<1.7
|
<1.7
|
4.0
(35)
|
|
Black-billed Magpie
|
3
|
5.3
(3.75.7)
|
8.3
(7.78.6)
|
8.8
(8.49.1)
|
4.9
(4.85.0)
|
4.0
(3.94.0)
|
|
|
5.0
(55)
|
|
American Crow
|
8
|
5.8
(<1.76.6)
|
8.7
(<1.79.6)
|
9.9
(6.710.6)
|
10.2
(9.210.8)
|
10.0
(8.210.4)
|
|
|
3.8
(35)
|
|
Fish Crow
|
9
|
5.4
(3.06.2)
|
6.8
(5.67.4)
|
7.8
(5.58.7)
|
8.9
(<1.79.9)
|
8.5
(<1.79.5)
|
4.0
(0-4.9)
|
1.3
(<1.7-2.0)
|
5.0
(47)
|
|
American Robin
|
2
|
5.8
(5.65.9)
|
8.9
(7.89.2)
|
7.3
(6.87.5)
|
4.6
(3.74.9)
|
2.0
(<1.72.3)
|
<1.7
|
<1.7
|
4.5
(45)
|
|
European Starling
|
6
|
5.3
(3.56.0)
|
6.1
(5.36.5)
|
4.9
(2.05.4)
|
2.3
(<1.73.1)
|
<1.7
|
<1.7
|
<1.7
|
3.2
(34)
|
|
Red-winged Blackbird
|
3
|
5.9
(5.56.1)
|
8.6
(7.59.0)
|
6.0
(5.56.3)
|
<1.7
|
<1.7
|
<1.7
|
<1.7
|
3.0
(33)
|
|
Common Grackle
|
6
|
6.1
(3.36.8)
|
10.2
(5.411.0)
|
11.8
(4.712.5)
|
11.8
(<1.712.5)
|
<1.7
|
<1.7
|
<1.7
|
3.3
(34)
|
|
House Finch
|
2
|
5.4
(2.35.7)
|
5.8
(5.66.0)
|
8.8
(8.68.9)
|
6.6
(6.06.8)
|
6.0
(5.96.1)
|
6.2
|
6.3
|
6.0
(57)
|
|
House Sparrow
|
6
|
7.8
(3.98.6)
|
9.8
(7.610.5)
|
10.3
(4.811.0)
|
10.3
(2.411.0)
|
8.4
(<1.79.0)
|
1.8
(<1.7-2.1)
|
<1.7
|
4.5
(26)
|
|
| aNT, not tested;
, no birds survived to be sampled. |
| bLog10-transformed
mean peak viremias ranged from 3.0 for Ring-necked Pheasants (range
2.03.2) and Budgerigars (range <1.73.4) to 12.1 for Blue Jays
(range 7.812.6). Mean duration (in days) of detectable viremias ranged
from 1.3 in Japanese Quail to 6.0 in House Finches and a Great Horned
Owl. |
| Table
3. Daily viremia determinations for nine Fish Crows infected with
West Nile virus by mosquito bitea |
|
|
Bird no.
|
Day postinoculation
|
|
|
1
|
2
|
3
|
4
|
5
|
6
|
7
|
8
|
9
|
10
|
11
|
|
|
015
|
3.6
|
5.6
|
5.7
|
5.7
|
<1.7
|
<1.7
|
<1.7
|
<1.7
|
<1.7
|
<1.7
|
<1.7
|
|
016
|
5.4
|
6.5
|
5.9
|
3.4
|
<1.7
|
<1.7
|
<1.7
|
<1.7
|
<1.7b
|
|
|
|
036
|
4.6
|
5.6
|
5.6
|
3.9
|
4.7
|
4.9
|
2.0
|
<1.7
|
<1.7
|
Dead
|
|
|
038
|
4.3
|
5.9
|
5.5
|
4.6
|
3.0
|
2.8
|
1.7
|
<1.7
|
<1.7
|
<1.7
|
3.3c
|
|
049
|
4.7
|
7.0
|
6.9
|
4.7
|
2.4
|
<1.7
|
<1.7
|
<1.7
|
<1.7
|
<1.7
|
<1.7
|
|
050
|
3.0
|
7.4
|
8.7
|
9.9
|
9.5
|
Dead
|
|
|
|
|
|
|
058
|
5.0
|
6.7
|
6.2
|
5.3
|
3.3
|
2.3
|
<1.7
|
<1.7
|
Dead
|
|
|
|
403
|
6.2
|
6.8
|
5.7
|
3.0
|
<1.7
|
<1.7
|
<1.7
|
NT
|
NT
|
NT
|
NT
|
|
404
|
3.1
|
5.7
|
7.0
|
<1.7
|
3.3
|
<1.7
|
<1.7
|
NT
|
NT
|
NT
|
NT
|
|
| aValues shown
are log10 transformed and represent the number of PFU/mL
serum. |
| bMoribund/euthanized. |
| cDead at 12 days
postinoculation. |
| Table
4. Deaths observed in eight species of birds exposed to West Nile
virus (WNV) by mosquito bitea |
|
|
Species
|
No. exposed
|
No. unexposedb
|
No. fatal infections
(% exposed)
|
Days postinoculation that death occurred
|
Mean no. days to death
(range)
|
|
|
Ring-billed gull
|
2
|
0
|
2 (100)
|
5, 13c
|
9.0 (513)
|
|
Blue Jay
|
4
|
0
|
|
4, 5, 5
|
4.7 (45)
|
|
Black-billed Magpie
|
3
|
0
|
3 (100)
|
6, 6, 6
|
6.0 (66)
|
|
American Crow
|
8
|
8
|
8 (100)
|
4, 4, 5, 5, 5, 6, 6, 6
|
5.1 (46)
|
|
Fish Crow
|
9
|
0
|
5 (55)
|
6, 9, 10, 10,c 13
|
9.6 (613)
|
|
Common Grackle
|
6
|
6
|
2 (33)
|
4, 5
|
4.5 (45)
|
|
House Finch
|
2
|
3
|
2 (100)
|
6, 8
|
7.0 (68)
|
|
House Sparrow
|
6
|
5
|
3 (50)
|
3, 5, 6
|
4.7 (36)
|
|
| aPreliminary mortality
rates were highest in Passerines, especially the corvids. No signs
of clinical illness were observed among species of the following orders:
Anseriformes, Falconiformes, Galliformes, Gruiformes, Columbiformes,
Psittaciformes, Strigiformes, and Piciformes. No obvious differences
in mortality rates were observed among birds exposed to WNV by means
other than mosquito bite (orally exposed and contact-exposed groups;
data not shown). |
| bUnexposed controls
were blood sampled daily for the same period as the exposed birds,
with no resulting illness. |
| cEuthanized. |
| Table
5. West Nile virus cage mate transmission trialsa |
|
|
Species
|
No. of cages
|
No. of mosquito-exposed birds
|
No. of contact-exposed cage mates
|
No. of transmissions (individuals)
|
No. of transmissions (cages)
|
Cage transmission rate
|
|
|
Mallard
|
1
|
2
|
1
|
0
|
0
|
0
|
|
Northern Bobwhite
|
1
|
3
|
3
|
0
|
0
|
0
|
|
Japanese Quail
|
1
|
3
|
3
|
0
|
0
|
0
|
|
American Coot
|
1
|
1
|
1
|
0
|
0
|
0
|
|
Ring-billed Gull
|
1
|
2
|
1
|
1
|
1
|
1.0
|
|
Mourning Dove
|
3
|
3
|
3
|
0
|
0
|
0
|
|
Rock Dove
|
6
|
6
|
6
|
0
|
0
|
0
|
|
Monk Parakeet
|
3
|
3
|
3
|
0
|
0
|
0
|
|
Budgerigar
|
3
|
3
|
3
|
0
|
0
|
0
|
|
Blue Jay
|
2
|
2
|
2
|
2
|
2
|
1.0
|
|
Black-billed Magpie
|
3
|
3
|
3
|
2
|
2
|
0.7
|
|
American Crow
|
4
|
8
|
5
|
5
|
4
|
1.0
|
|
Fish Crow
|
4
|
8
|
9
|
0
|
0
|
0
|
|
American Robin
|
1
|
2
|
1
|
0
|
0
|
0
|
|
European Starling
|
2
|
6
|
2
|
0
|
0
|
0
|
|
Common Grackle
|
6
|
6
|
6
|
0
|
0
|
0
|
|
House Finch
|
1
|
2
|
3
|
0
|
0
|
0
|
|
House Sparrow
|
2
|
6
|
5
|
0
|
0
|
0
|
|
| aUninfected
birds (contact-exposed group) were placed within cages containing
birds (of the same species) that were infected by mosquito bite (mosquito-exposed
group). Transmission to uninfected cage mates was determined by development
of viremia or seroconversion. |
| Table
6. West Nile virus shedding in living birds, as determined by
daily cloacal swabbing of 24 species of birds exposed by mosquito
bitea,b |
|
|
Species
|
n
|
Day postinoculation
|
No. birds
shedding (%)
|
|
|
1
|
2
|
3
|
4
|
5
|
6
|
7
|
|
|
Canada Goose
|
3
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
2.3
(<0.72.7)
|
0.6
(<0.71.0)
|
2.1
(<0.72.6)
|
2 (67)
|
|
Mallard
|
2
|
<0.4
|
<0.4
|
<0.4
|
<0.4
|
<0.4
|
<0.4
|
<0.4
|
0
|
|
American Kestrelc
|
2
|
1.6
(1.61.6)
|
2.8
(2.03.1)
|
4.2
(1.94.5)
|
4.9
(4.05.2)
|
4.2
(3.64.4)
|
2.3
(2.22.4)
|
3.1
(<0.43.4)
|
2 (100)
|
|
Northern Bobwhite
|
3
|
<0.2
|
<0.2
|
0.2
(<0.40.7)
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
1 (33)
|
|
Japanese Quail
|
3
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
0
|
|
Ring-necked Pheasant
|
3
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
0
|
|
American Coot
|
1
|
<0.7
|
<0.7
|
<0.7
|
<0.7
|
2.7
|
<0.7
|
NT
|
1 (100)
|
|
Killdeer
|
2
|
<0.1
|
0.5
(<0.40.8)
|
<0.1
|
1.5
(<0.41.8)
|
<0.1
|
<0.1
|
<0.1
|
1 (50)
|
|
Ring-billed Gull
|
2
|
<0.1
|
<0.1
|
2.4
(0.42.7)
|
2.3
(2.22.5)
|
<0.4
|
1.8
|
<0.4
|
2 (100)
|
|
Mourning Dove
|
3
|
<0.2
|
1.1
(0.81.5)
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
2 (67)
|
|
Rock Dove
|
6
|
<0.5
|
<0.5
|
<0.5
|
<0.5
|
1.2
(<0.41.7)
|
NT
|
NT
|
4 (67)
|
|
Monk Parakeet
|
3
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
0
|
|
Budgerigar
|
3
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
0
|
|
Great Horned Owlc
|
1
|
<0.4
|
2.3
|
2.1
|
3.1
|
2.1
|
3.3
|
2.0c
|
1 (100)
|
|
Northern Flicker
|
1
|
<0.4
|
<0.4
|
<0.4
|
<0.4
|
<0.4
|
<0.4
|
<0.4
|
0
|
|
Blue Jay
|
4
|
<0.3
|
3.0
(<0.43.6)
|
4.3
(2.14.8)
|
6.0
(2.06.4)
|
2.0
|
1.0
|
<0.4
|
4 (100)
|
|
Black-billed Magpie
|
3
|
<0.2
|
1.8
(<0.42.3)
|
2.4
(2.12.5)
|
1.9
(<0.42.3)
|
2.9
(<0.43.4)
|
|
|
3 (100)
|
|
American Crow
|
6
|
0.8
(<0.41.5)
|
3.3
(<0.44.0)
|
5.2
(2.75.8)
|
5.0
(3.85.5)
|
5.7
|
|
|
6 (100)
|
|
Fish Crowd
|
8
|
0.2
(<0.40.7)
|
1.5
(<0.42.1)
|
3.0 (1.03.8)
|
2.5
(<0.43.0)
|
3.3
(<0.44.1)
|
3.9
(<0.44.8)
|
3.6
(<0.44.4)
|
8 (100)
|
|
American Robin
|
2
|
<0.4
|
0.8
(<0.71.1)
|
2.2
(<0.72.5)
|
<0.4
|
<0.4
|
<0.4
|
<0.4
|
1 (50)
|
|
European Starling
|
6
|
<0.5
|
<-0.5
|
-0.5
(<0.40.4)
|
<0.5
|
0.5
(<0.40.4)
|
0.8
(<0.41.5)
|
<0.5
|
3 (50)
|
|
Red-winged blackbird
|
3
|
0.2
|
0.4
(<0.40.8)
|
<0.2
|
0.2
(<0.40.7)
|
<0.2
|
<0.2
|
<0.2
|
1 (33)
|
|
Common Grackle
|
6
|
<0.5
|
>2.0
(<0.4>2.7)
|
4.5
(0.75.3)
|
5.6 (<0.46.4)
|
5.2
(<0.45.9)
|
0.8
(<0.41.4)
|
0.1
(<0.40.7)
|
6 (100)
|
|
House Finch
|
2
|
<0.4
|
<0.4
|
<0.4
|
<0.4
|
<0.4
|
<0.7
|
<0.7
|
0
|
|
House Sparrowe
|
6
|
NT
|
<0.5
|
NT
|
>1.9
(<0.4>2.7)
|
1.3
(<0.42.1)
|
NT
|
NT
|
2 (33)
|
|
| aPresented as
mean log10 PFU/swab, with ranges. |
| bNT, not tested;
, no birds survived the infection to be sampled. |
| cAmerican Kestrels
and the Great Horned Owl were tested at 911 days postinoculation,
with no detectable virus in swabs. |
| dSurviving Fish
Crows were tested at 8 and 9 days postinoculation with the following
results for day 8 and day 9, respectively: 1.2 (<0.41.8); 1.5
(<0.42.1). |
| eThese House Sparrows
were inoculated by needle rather than by mosquito bite. |
| Table
7. West Nile virus shedding in living birds, as determined by
plaque assay of oral swabs collected daily from 14 species of birds
exposed by mosquito bitea,b |
|
|
Species
|
n
|
Day postinoculation
|
No. birds shedding (%)
|
|
|
1
|
2
|
3
|
4
|
5
|
6
|
7
|
|
|
American Kestrelc
|
2
|
1.2
(1.01.3)
|
1.9
(1.62.1)
|
3.9
(3.04.2)
|
4.1
(2.84.4)
|
4.9
(4.65.1)
|
5.1
(4.65.3)
|
3.3
(3.13.4)
|
2 (100)
|
|
Northern Bobwhite
|
3
|
<0.2
|
<0.2
|
0.2
(<0.40.3)
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
1 (33)
|
|
Japanese Quail
|
3
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
2.5
(<0.43.0)
|
1.9
(<0.42.4)
|
1 (33)
|
|
Killdeer
|
2
|
NT
|
<0.1
|
0.4
(<0.40.7)
|
0.1
(<0.40.4)
|
0.8
(<0.41.1)
|
0.1
(<0.40.4)
|
0.4
(<0.40.7)
|
1 (50)
|
|
Ring-billed Gulld
|
2
|
NT
|
3.1
(2.03.3)
|
2.8
(1.83.0)
|
3.3
(2.63.6)
|
3.5
|
3.5
|
3.4
|
2 (100)
|
|
Mourning Dove
|
3
|
NT
|
<0.2
|
0.8
(<0.41.2)
|
0.5
(<0.40.8)
|
0.5
(<0.40.8)
|
<0.2
|
<0.2
|
2 (67)
|
|
Monk Parakeet
|
3
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
0 (0)
|
|
Budgerigar
|
3
|
NT
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
<0.2
|
0 (0)
|
|
Great Horned Owl
|
1
|
<0.4
|
1.3
|
3.1
|
<0.4
|
5.8
|
4.9
|
2.8
|
1 (100)
|
|
Northern Flicker
|
1
|
<0.4
|
<0.4
|
<0.4
|
<0.4
|
<0.4
|
<0.4
|
<0.4
|
0 (0)
|
|
Blue Jaye
|
2
|
0.9
(<0.41.2)
|
4.0
(1.44.3)
|
3.9
(2.54.2)
|
3.6
|
3.7
|
2.2
|
1.2
|
2 (100)
|
|
Black-billed Magpie
|
3
|
<0.2
|
0.8
(<0.41.0)
|
2.1
(1.42.5)
|
3.1
(2.53.3)
|
4.0
(<0.44.4)
|
|
|
3 (100)
|
|
American Crow
|
6
|
<0.5
|
2.3
(<0.42.5)
|
5.0
(1.65.5)
|
4.3
(3.14.7)
|
5.7
|
|
|
6 (100)
|
|
Fish Crowf
|
8
|
<0.6
|
1.0
(<0.41.7)
|
3.4
(1.34.2)
|
3.6
(<0.44.1)
|
3.8
(1.84.4)
|
3.8
(1.64.6)
|
3.5
(1.94.1)
|
8 (100)
|
|
| aPresented as
mean log10 PFU/swab, with ranges. |
| bNT, not tested;
, no birds survived the infection to be sampled. |
| cAmerican Kestrels
were tested at 9, 10, and 11 days postinoculation, with the following
results for days 9 and 10, respectively: 2.3 (1.82.5); 1.8 (<0.42.1).
WNV was not isolated from oral swabs collected on day 11. |
| dOne Ring-billed
Gull developed signs of illness after 7 days postinoculation and was
euthanized at 13 days postinoculation, at which time an oral swab
contained 10 PFU WNV. |
| eOne Blue Jay
was sampled at 8 and 9 days postinoculation. No virus was isolated
from oral swabs. |
| fSurviving Fish
Crows were tested at 8 and 9 days postinoculation with the following
results for days 8 and 9, respectively: 3.6 (2.04.3); 2.1 (<0.52.5). |
| Table
8. Viral load, determined by Vero plaque assay, in organs harvested
from fatal cases of West Nile virus infection in experimentally infected
birdsa |
|
|
Species
|
ID no.
|
Sex
|
Mode of
infection
|
Organ (log10 PFU/0.5
cm3)
|
|
|
Br
|
Ki
|
He
|
Sp
|
Li
|
Lu
|
In
|
Es
|
Go
|
Sk
|
Ey
|
|
|
Ring-billed Gull
|
BDG
|
M
|
M
|
2.7
|
2.8
|
1.0
|
3.3
|
3.0
|
3.2
|
<1.0
|
2.7
|
1.6
|
3.0
|
2.0
|
|
Ring-billed Gull
|
LG
|
F
|
C
|
3.0
|
2.4
|
1.7
|
1.3
|
<1.0
|
<1.0
|
<1.0
|
2.3
|
3.0
|
2.4
|
3.0
|
|
American Crow
|
21
|
M
|
C
|
7.2
|
7.6
|
5.4
|
7.9
|
7.5
|
8.5
|
7.6
|
7.8
|
6.8
|
4.4
|
7.7
|
|
American Crow
|
24
|
F
|
M
|
6.0
|
8.2
|
7.7
|
7.0
|
7.3
|
7.1
|
8.4
|
7.4
|
7.0
|
4.6
|
6.6
|
|
American Crow
|
25
|
F
|
M
|
5.9
|
7.2
|
5.7
|
6.7
|
6.8
|
6.7
|
10.6
|
6.2
|
7.9
|
3.8
|
6.9
|
|
American Crow
|
34
|
F
|
C
|
8.3
|
8.2
|
7.8
|
7.9
|
7.7
|
8.3
|
9.0
|
8.2
|
8.1
|
5.3
|
7.9
|
|
American Crow
|
37
|
NR
|
C
|
7.2
|
8.2
|
7.7
|
7.8
|
7.4
|
8.5
|
10.0
|
7.3
|
NT
|
5.3
|
7.7
|
|
American Crow
|
41
|
F
|
M
|
8.3
|
9.1
|
8.5
|
8.7
|
8.7
|
10.3
|
6.6
|
8.8
|
9.4
|
5.6
|
8.5
|
|
American Crow
|
42
|
F
|
M
|
8.1
|
9.1
|
8.4
|
7.8
|
8.1
|
8.4
|
10.3
|
8.6
|
8.3
|
5.8
|
7.9
|
|
American Crow
|
529
|
F
|
M
|
6.1
|
7.2
|
7.0
|
6.5
|
5.3
|
7.7
|
5.7
|
5.9
|
6.9
|
6.8
|
5.7
|
|
American Crow
|
543
|
F
|
M
|
8.3
|
8.4
|
8.4
|
7.2
|
7.4
|
9.6
|
8.7
|
8.0
|
8.7
|
5.9
|
8.6
|
|
American Crow
|
562
|
NR
|
M
|
8.3
|
8.2
|
6.9
|
7.7
|
7.7
|
8.1
|
10.2
|
7.4
|
8.1
|
5.8
|
7.3
|
|
American Crow
|
574
|
M
|
C
|
8.3
|
8.1
|
8.2
|
8.0
|
8.6
|
8.1
|
9.7
|
6.3
|
7.8
|
6.1
|
7.5
|
|
American Crow
|
805
|
M
|
M
|
8.1
|
6.5
|
7.3
|
5.9
|
6.3
|
9.2
|
8.3
|
8.0
|
6.3
|
6.4
|
8.7
|
|
Fish Crow
|
005
|
M
|
M
|
6.9
|
4.0
|
<2.0
|
3.3
|
3.5
|
4.0
|
4.5
|
8.5
|
4.4
|
3.0
|
6.2
|
|
Fish Crow
|
016
|
M
|
M
|
2.7
|
3.2
|
6.6
|
1.0
|
1.0
|
4.6
|
5.2
|
5.1
|
3.6
|
4.0
|
4.8
|
|
Fish Crow
|
036
|
NR
|
M
|
3.0
|
3.1
|
6.6
|
3.3
|
1.5
|
5.3
|
3.0
|
6.5
|
3.3
|
4.9
|
3.1
|
|
Fish Crow
|
038
|
M
|
M
|
4.1
|
3.9
|
4.7
|
1.3
|
1.0
|
4.4
|
2.0
|
5.4
|
4.5
|
2.8
|
5.0
|
|
Fish Crow
|
050
|
F
|
M
|
6.9
|
8.1
|
8.5
|
8.2
|
7.8
|
7.6
|
8.6
|
7.7
|
8.0
|
5.5
|
6.9
|
|
Fish Crow
|
058
|
M
|
M
|
4.5
|
5.1
|
6.9
|
2.4
|
1.6
|
5.8
|
6.0
|
5.1
|
2.7
|
5.0
|
5.3
|
|
Fish Crow
|
402
|
M
|
U
|
4.7
|
3.6
|
3.8
|
3.7
|
1.5
|
3.0
|
2.8
|
7.4
|
1.8
|
3.7
|
5.8
|
|
Blue Jay
|
124
|
NR
|
M
|
7.4b
|
7.8
|
9.0
|
8.3
|
8.8
|
9.1
|
6.3
|
NT
|
7.1
|
NT
|
NT
|
|
Blue Jay
|
125
|
NR
|
M
|
7.3b
|
8.6
|
9.1
|
8.3
|
8.9
|
9.2
|
7.3
|
NT
|
7.3
|
NT
|
NT
|
|
Blue Jay
|
908
|
M
|
C
|
8.2
|
9.0
|
8.8
|
8.6
|
8.5
|
9.0
|
8.0
|
8.7
|
9.1
|
6.9
|
7.9
|
|
Blue Jay
|
909
|
M
|
C
|
2.7
|
6.1
|
6.6
|
5.5
|
4.3
|
5.8
|
3.4
|
4.5
|
5.0
|
5.9
|
7.1
|
|
Blue Jay
|
910
|
F
|
M
|
8.2
|
9.0
|
9.0
|
8.1
|
8.4
|
9.1
|
7.9
|
8.9
|
9.1
|
6.0
|
8.0
|
|
Black-billed Magpie
|
LG
|
M
|
M
|
4.7
|
6.6
|
6.6
|
3.9
|
5.4
|
6.5
|
4.8
|
6.7
|
5.9
|
5.5
|
6.3
|
|
Black-billed Magpie
|
RBLG
|
M
|
M
|
5.9
|
5.5
|
5.0
|
4.0
|
4.8
|
4.4
|
2.7
|
5.9
|
4.8
|
4.1
|
4.6
|
|
Black-billed Magpie
|
NB
|
M
|
C
|
5.8
|
6.2
|
7.2
|
5.9
|
6.4
|
5.7
|
5.1
|
5.9
|
6.5
|
4.8
|
5.5
|
|
Black-billed Magpie
|
RB
|
M
|
C
|
5.0
|
7.7
|
6.2
|
4.5
|
6.8
|
6.3
|
5.2
|
5.8
|
4.7
|
5.9
|
5.3
|
|
Black-billed Magpie
|
RG
|
F
|
M
|
6.4
|
5.4
|
6.7
|
4.7
|
1.9
|
6.1
|
1.0
|
6.6
|
4.5
|
5.9
|
4.7
|
|
Common Grackle
|
120
|
M
|
M
|
3.5
|
>3.6
|
>3.6
|
>3.6
|
>3.6
|
>3.6
|
<1.0
|
5.0
|
<1.0
|
4.0
|
5.0
|
|
Common Grackle
|
123
|
M
|
M
|
2.4
|
>3.3
|
NT
|
NT
|
NT
|
NT
|
<1.0
|
4.9
|
5.1
|
4.6
|
4.9
|
|
House Finch
|
0
|
F
|
M
|
3.9
|
3.8
|
5.9
|
3.6
|
3.8
|
3.9
|
<1.0
|
5.5
|
3.8
|
4.1
|
6.2
|
|
House Finch
|
1
|
M
|
M
|
4.9
|
3.0
|
6.1
|
3.5
|
2.7
|
6.0
|
<1.0
|
5.7
|
3.2
|
5.8
|
6.3
|
|
| aB, brain; Ki,
kidney; He, heart; Sp, spleen; Li, liver; Lu, lung; In, intestine;
Es, esophagus; Go, gonad; Sk, skin; Ey, eye; M, mosquito-exposed;
C, contact-exposed; U, undetermined mode of transmission; NR, not
recorded; and NT, not tested. |
| bThese Blue Jay
brains were evaluated for viral load in both cerebellum and cortex.
In both cases, cerebellum was negative. |
| Table
9. Viral load, determined by Vero plaque assay in organs harvested
from surviving birds 14 days after West Nile virus (WNV) infection
by mosquito bitea,b |
|
|
Species
|
ID no.
|
Sex
|
Organ (PFU/0.5 cm3)
|
Days postviremia
|
|
|
Br
|
Ki
|
He
|
Sp
|
Li
|
Lu
|
In
|
Es
|
Go
|
Sk
|
Ey
|
|
|
American Kestrelc
|
F2
|
F
|
d
|
20
|
|
20
|
|
|
|
|
NT
|
30
|
|
10
|
|
American Kestrel
|
F3
|
F
|
|
|
|
10
|
|
|
|
|
NT
|
|
|
11
|
|
Japanese Quail
|
902
|
U
|
10
|
10
|
|
|
|
|
|
|
|
|
|
8
|
|
|
904
|
U
|
|
|
|
10
|
|
|
|
|
10
|
|
|
14
|
|
Japanese Quail
|
907
|
U
|
|
|
20
|
20
|
|
|
|
|
|
|
|
14
|
|
Killdeer
|
|
U
|
|
60
|
|
|
|
|
20
|
|
|
110
|
|
9
|
|
Killdeer
|
WT
|
U
|
|
|
|
550
|
|
|
|
|
|
2x104
|
|
10
|
|
Mourning Dove
|
LCW
|
U
|
|
20
|
|
|
|
|
|
|
|
|
|
10
|
|
Mourning Dove
|
RB
|
M
|
|
100
|
|
|
|
|
|
|
|
|
|
11
|
|
Budgerigar
|
13591
|
U
|
|
|
130
|
|
|
|
|
|
|
|
|
13
|
|
Blue Jay
|
911
|
U
|
20
|
|
|
|
|
|
|
|
|
|
360
|
9
|
|
Fish Crow
|
049
|
U
|
|
|
|
|
|
|
|
|
|
|
30
|
9
|
|
Red-winged Blackbird
|
711
|
M
|
|
|
10
|
|
10
|
|
|
|
|
|
|
11
|
|
Common Grackle
|
119
|
F
|
|
|
|
10
|
|
|
|
10
|
20
|
380
|
150
|
11
|
|
Common Grackle
|
122
|
M
|
|
|
|
|
|
|
|
|
|
|
10
|
10
|
|
House Sparrow
|
011
|
F
|
10
|
50
|
|
|
|
|
40
|
90
|
|
370
|
60
|
8
|
|
House Sparrow
|
012
|
M
|
|
|
|
120
|
|
590
|
10
|
|
|
10
|
|
10
|
|
House Sparrow
|
016
|
M
|
200
|
20
|
|
50
|
|
20
|
|
|
|
|
50
|
8
|
|
| aFor each bird,
the number of days postviremia is indicated. Birds from which no virus
was detected are not included. WNV was isolated from at least one
organ sample from 18 birds, and at least one isolate was made from
each of the 11 different organs. Liver had the fewest isolates with
one; spleen had the most with eight. Titers were generally low. The
highest titered specimen was a skin sample from a Killdeer. Twenty-three
surviving birds had no WNV isolated from tissues at 14 days postinoculation,
including three Northern Bobwhites, three Ring-necked Pheasants, three
Monk Parakeets, two Budgerigars, one Great Horned Owl, one Mourning
Dove, six European Starlings, two Common Grackles, and two Red-winged
Blackbirds. In addition, five Rock Doves were sampled at 64 days postinoculation
and were negative. |
| bM, male; F, female;
U, undetermined gender or gender not recorded; Br, brain; Ki, kidney;
He, heart; Sp, spleen; Li, liver; Lu, lung; In, intestine; Es, esophagus;
Go, gonad; Sk, skin; Ey, eye; and NT, not tested. |
| cKestrels were
tested 15 days postinoculation. |
| d indicates
that no virus was isolated (threshold of detection 10 PFU/0.5 cm3
tissue). |
| Table
10. West Nile virus reservoir competence index values derived
for 25 species of birds |
|
|
Common name
|
Susceptibility (s)
|
Mean infectiousness (i)
|
Mean duration (days) (d)
|
Reservoir competence index (C1)a
|
|
|
Blue Jay
|
1.0
|
|
3.75
|
2.55
|
|
Common Grackle
|
1.0
|
0.68
|
3
|
2.04
|
|
House Finch
|
1.0
|
0.32
|
5.5
|
1.76
|
|
American Crow
|
1.0
|
0.50
|
3.25
|
1.62
|
|
House Sparrow
|
1.0
|
0.53
|
3
|
1.59
|
|
Ring-billed Gull
|
1.0
|
0.28
|
4.5
|
1.26
|
|
Black-billed Magpie
|
1.0
|
0.36
|
3
|
1.08
|
|
American Robin
|
1.0
|
0.36
|
3
|
1.08
|
|
Red-winged Blackbird
|
1.0
|
0.33
|
3
|
0.99
|
|
American Kestrel
|
1.0
|
0.31
|
3
|
0.93
|
|
Great Horned Owl
|
1.0
|
0.22
|
4
|
0.88
|
|
Killdeer
|
1.0
|
0.29
|
3
|
0.87
|
|
Fish Crow
|
1.0
|
0.26
|
2.8
|
0.73
|
|
Mallard
|
1.0
|
0.16
|
3
|
0.48
|
|
European Starling
|
1.0
|
0.12
|
1.8
|
0.22
|
|
Mourning Dove
|
1.0
|
0.11
|
1.7
|
0.19
|
|
Northern Flicker
|
1.0
|
0.06
|
1
|
0.06
|
|
Canada Goose
|
1.0
|
0.10
|
0.3
|
0.03
|
|
Rock Dove
|
1.0
|
0
|
0
|
0
|
|
American Coot
|
1.0
|
0
|
0
|
0
|
|
Japanese Quail
|
1.0
|
0
|
0
|
0
|
|
Northern Bobwhite
|
1.0
|
0
|
0
|
0
|
|
Ring-necked Pheasant
|
1.0
|
0
|
0
|
0
|
|
Monk Parakeet
|
1.0
|
0
|
0
|
0
|
|
Budgerigar
|
0.7
|
0
|
0
|
0
|
|
| aCi = s * i
* d |
|
