1

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

2

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?

3

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