the natural history of aiv wild birds and the epidemiology of … · wild birds and the...
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Wild birds and the epidemiology of
avian influenza
The Natural History of AIV
There is a little more to it than this!
Avian Reservoirs: Ducks, Geese, and Swans
�Very diverse order
�Very diverse gene pool
�High prevalence of infection
on an annual basis
Who is infected?
What viruses are they infected with?
When and where are they infected?
What species are infected?
Mallard #1
Open water/pelagic
habitats
Atypical migration
patterns
Habitat use variation
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Olsen et al. Global patterns of Influenza A virus in wild birds.
Science 312:384-388. (limited to studies where specific species
given)
36 species 3,275/34,503 (9.5%)
8 species 47/4,806 (1.0%)
3 species 94/5,009 (1.4%)
Mallard (12.9%), northern pintail (11.2%), blue-
winged teal (11.5%), American black duck (18.1%),
common teal (4%)
When and where does infection occur?Is there a temporal pattern?
SEASONAL AND GEOGRAPHIC VARIATION in North American
Mallards
Sample period Location % Positive
July-August Quebec 37%August Alberta 30%August New York 42%
Aug.-Sept. Minnesota 36%September Minnesota 13%September Minnesota 12%Oct.-Nov Minnesota 2%November Maryland 1%Nov-Jan. Arkansas 1%Nov.-May Pennsylvania 0%
From: Boudreault et al., 1980; Hinshaw et al., 1980; Diebel et al.,1985;
Karunakaran et al.,1983; Bahl et al.,1977; Nettles et al.,1985; Webster et al., 1986,
Hanson et al, 2003
Is there a spatial pattern?
30%
5-30%
<5%
10% infection late winter/early spring
H2, H7, H8
AIV transmission on the
wintering grounds
Early migrating teal 8%,
transmission on
wintering grounds as
determined by isolations
from mottled ducks
Some other spatial/temporal interactions?
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Avian Influenza maintenance and migration?
�Do blue-winged teal escape the force of infection on the breeding grounds and provide a susceptible population on the wintering grounds?�Is this species one we should look at for movement of AIVs between North and South America?�A similar relationship has be proposed for garganey teal in Europe/Africa?
HA diversity in AIVs isolated from ducks
Alberta (Kawaoka et al, 1988) (n=2599), H3 (33%), H4 (19%), H6 (42%)
New York (Diebel et al, 1985) (n=160) H3 (33%), H4 (38%), H6 (12%)
Pennsylvania (Hinshaw et al, 1986)(n=171) H3(20%), H4 (28%), H6 (50%)
Germany (Ottis and Bachman, 1983)(n=65) H3(28%), H4 (27%), H11(21%)
Canada (Boudreault et al., 1980)(n=114) H1(82%), H4 (10%), H6(5%)
Ohio (Slemons et al., 1991)(n=55) H3(26%), H6(11%), H11(22%)
Louisiana (Stallknecht et al, 1991)(n=27) H4(41%), H6(15%), H11(11%)
Minnesota (Hanson et al, 2003)(n=154) H3 (14%), H4(27%), H6(14%)
Alberta (Kawaoka et al, 1988) (n=2599) H5(0.2%), H7(0.6%), H9(0.3%)
New York (Diebel et al, 1985) (n=160) H5(0.6%), H7(0%), H9(0%)
Pennsylvania (Hinshaw et al, 1986)(n=171) H5(0.5%), H7(0%), H9(0%)
Germany (Ottis and Bachman, 1983)(n=65) H5(0%), H7(2%), H9(0.%)
Canada (Boudreault et al., 1980)(n=114) H5(1%), H7(0%), H9(0%)
Ohio (Slemons et al., 1991)(n=55) H5(7%), H7(2%), H9(0%)
Louisiana (Stallknecht et al, 1991)(n=27) H5(0%), H7(0%), H9(0%)
H5, H7, and H9 AIVs from ducks (These are the
subtypes that have been involved in direct domestic
bird to human transmission
Based on 3,109 isolates
H5 0.25%
H7 0.61%
H9 0.22% of
Alberta (Krauss et al., 2004,
Vector-Borne and Zoonotic
Diseases (no H5, H7, or H9
isolations in ducks 1998-2000)
Minnesota (Hanson et al., 2003,
Avian Diseases) (H5, H7, and H9
viruses each recovered 2 out of 3
years 1998-2000)
Is location important in relation to subtype diversity?
Different locations and different populations?
4
Olsen et al. Global patterns of Influenza A virus in wild birds.
Science 312:384-388. (limited to studies where specific species
given)
9 species 199/14,505 (1.5%)
10 species 21/2,637 (1%)
9 species 24/2,521 (1%)
Dunlin 1/377 (<1%)
Red Knot 15/1,993 (<1%)
Sanderling 8/745 (1%)
Semipalmated 3/435 (<1%)
Ruddy turnstone 262/2,358 (11%)
S-B dowitcher 1/157 (<1%)
AIV isolations DE Bay 2000-2005
10%30H3
7%22H12
1%4H4
14%41H11
27%80H10
14%41H9
1%3H7
6%19H6
4%13H5
15%43H2
%Number isolations
HA subtype
296 AIV isolates
Subtype diversity: Shorebirds DE Bay
Extreme variation in predominant subtypes between years
No isolations of H1, H8, H13
H11N8,H11N6H11N2,H11N3
H11N4,H11N9
H11N2,H11N7H11N6
H12N4,H12N5,
H12N9.
H12N5H12N5H12N4, H12N5
H10N7H10N7H10N7H10N7
H9N2,H9N5,H9N7,
H9N8,H9N9
H9N4,H9N5,
H9N9
H7N3H7N9
H6N8H6N8H6N4, H6N8H6N2, H6N5H6N1, H6N4
H5N7H5N2,H5N9H5N9H5N2, H5N7,
H5N8
H5N3
H4N6H4N6
H3N6, H3N8
H2N6,H2N9H2N3, H2N4, H2N9
200520042003200220012000
Avian influenza prevalence is
dependent on ruddy turnstone
weight gains at Delaware Bay
(P = 0.001)
0
2
4
6
8
10
12
14
16
18
<102 102-124 125-145 >145
Weight (grams)
AIV
prevale
nce
n=176
n=179
n=174
n=176
5
0.00
5.00
10.00
15.00
20.00
25.00
30.00
1 2 3 4 5 6 7 8 9 10 11 12 13
HA subtypes
Pe
rce
nta
ge Kawaoka
Krauss
SCWDS
Temporal variation and study duration. Why long-
term studies are essential
Kawaoka et al. 1988. Virology 163:247. (Short-term)
Krauss et al. 2004. Vector Borne and Zoonotic Diseases 4:177 (Long-term)
Is there a spatial pattern?With all of the work on
AIV in shorebirds to date,
a high prevalence of
infection has been
identified in only one
species at only one area at
only one time of year.
Least sandpiperH3N8
Ringed-billed
gull H6N4, H11N6
Red knot H10N7
Laughing gull H6N1,H6N4,H7N3
Herring gull H2N3
Eight isolations from
>3,000 (these include
>600 shorebirds birds
sampled in Argentina
and Chile
Avian influenza habitat? Environmental effects on transmission
Transmission: Fecal/Oral route
Heavy fecal shedding by infected ducks
Long term persistence in water
Isolation of AIVs from surface water
Maintenance: Bird to bird
Persistence in environment
Persistence of AIVs in Water
Proof of concept (Webster et al. 1978): A/duck/Memphis/546/74 (H3N2)
at an initial dose of 106.8 EID50 remained infective for at least 32 days in
river water
�Wild type AIVs can persist in water
for extended time (months) at 4C,
17C, and 28C
�Persistence is virus and
temperature dependent
�Persistence is dependent on basic
water chemistry (pH and salinity at
ranges that are consistent with
normal surface water)
�Individual viruses differ in their
response to pH and salinity.
The best treatment combination for persistence in water. 17C/0ppt salinity/8.2 pH
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Results: Persistence of H5 and H7 AIV at 17CEstimated infectivity of 106 TCID50 in days
11518294Duck meat/Anyang (H5N1)
8283158WSwan/Mongolia (H5N1)
171143667LGull/DE (H7N3)
105140194RUTU/DE (H7N3)
107133176BWT/TX (H7N4)
92133214Mallard/MN (H7N3)
58125268RUTU/NJ (H5N8)
85375231RUTU/NJ (H5N7)
113333316Mallard/MN (H5N3)
63128429Mallard/MN (H5N2)
30 ppt15 ppt0 pptVirus
While this sounds encouraging keep in mind that the infective dose for
these viruses may be very low
HPAI H5N1 1997 Hong Kong-And Beyond
The Unnatural History of AIV
Wild birds can be infected with HPAI H5N1
A virus isolation does not make a reservoir!
HPAI H5N1 has
been isolated
from many
species that are
most likely dead
ends.
Can such isolations be
explained?
The details ARE
important!
Field reports of wild bird mortality
�Hong Kong (2002-2003) Black-headed gull, little egret, grey heron,
greater flamingo, pigeon, tree sparrow, various waterfowl
�Hong Kong (2003 and 2004) Peregrine falcon, Grey Heron
�Cambodia (2004) (Zoo collection) raptors and psittacines
�Japan and Korea (2004) Crows and magpies
�Thailand (2004) Pigeons, open-billed storks, little cormorant, red
collared dove, scaly-breasted munia, black drongo
�China (2004) grey heron and Chinese pond heron
�China/Mongolia (2005) Bar-headed goose,whooper swan, brown-headed
gull, Greater black-backed gull
�Russia (Siberia) (2005) Wild birds?
�Kazakhstan (2005) Wild birds?
�Turkey, Romania, Croatia (2005)
�Europe (14 EU countries) (2006) Almost all anseriforms; mostly mute
swans
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Why the difference in species affected ?
Domestic birds sharing habitat with wildlife
Wild birds visiting domestic bird habitat
New species/new pathogens/new issues (disease)
A new window from which to few this system
The transmission of AIV from free living (wild)
to free-ranging (domestic) birds is well
established.
Infections in captive wild birds are well documented
�Indicator species
�New transmission routes
North American Ducks
Wood ducks:
Anyang: 2/3 with clinical signs, 1 death
Mongolia: 2/3 with clinical signs, 2 deaths
Other species: No clinical signs, low viral titers,
short duration of viral shedding, infection
associated with respiratory system
Conclusions:
Species, populations, and communities and the environments they utilize
are important in the epidemiology of wild-type AIVs and they will be
important in the epidemiology of HPAI H5N1
Wild birds can be infected and they can move these viruses, but it is not
known if a HPAI H5N1 will persist in wild bird populations (The big test is
coming in a few months)
With regard to developing efficient and effective control and surveillance
strategies:
�Understand and define the species and population you are surveying
�Concentrate on birds normally associated with AIV
�Consider the known temporal and spatial relationships
�Plan for a low prevalence of infection when designing surveillance
strategies
�Keep the environment as well as the host in mind
�Concentrate on mortality for initial detection