Wild birds & spread H5N1 Asia_OIE meeting - OIE Asia-Pacific

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Wild birds & spread H5N1 Asia_OIE meeting - OIE Asia-Pacific

Possible role of wild birds in the

spread of HPAI H5N1 in Asia,

preventative & control measures

4 th OIE Regional Expert Group Meeting, Tokyo, Japan

Nichola Hill, PhD &

Scott Newman, PhD

EMPRES Wildlife Unit

FAO-HQ, Rome, Italy


Timeline of H5N1 outbreaks in wild birds

1996

• First detection in domestic goose, Guangdong, China

1997

• First human death reported in Hong Kong

2002

2005

• First infection wild birds (captive) Hong Kong waterfowl park

• Largest wild bird outbreak, Qinghai Lake killing 6,300 birds

followed by north- & westward spread into Europe

2006-10

• Recurrent (but smaller) outbreaks along Central Asia Flyway

Now

• Clade 2.3.2 becomes dominant strain in wild birds


Five years after Qinghai outbreak

2005

2006

2009

2010

April

May

June

July

August


Epidemiology & ecology of avian influenza

Adaptation

LPAIV

(H1-H16)

Re-adaptation

Key: Exchange

between wild and

domestic birds

LPAIV

(H1-16)

HA

Mutation

HPAIV

(H5/H7/H9)

Swayne,D. (2008). Avian Influenza, pp. 59-86


Domestic ducks as a reservoir

• Free-ranging domestic ducks

act as silent carriers of H5N1

in South-East Asia

(Gilbert et al., 2007 & 2008)

• Show few clinical signs and

shed virus for up to 17 days

(Hulse-Post et al., 2005)

• Difficult to vaccinate: 1) logistics of treating millions of ducks on rural

landscape & 2) lower vaccination efficiency compared to chickens

• Hypothesis: two-host system of H5N1 spread. 1) Domestic ducks act

as reservoir and seed infection in wild birds, 2) wild birds act as

temporary agents for dispersal at continental scale

Gilbert et al., EcoHealth. 2011, in press


Flyways in Asia

• 2-3 flyways are recognized

in East Asia, but they are not

well-defined

• Mix of shorebird (East Asian-

Australasian Flyway) &

waterfowl flyways


Using satellite telemetry to unravel the role of

wild birds in transmission of AIV…


Habitat preferences at

breeding & wintering sites

Migration pathways

& timing

Interaction with poultry

(or ‘poultry contact risk’)

Satellite telemetry

Flight performance of

infected birds

Connectivity between

regions of outbreak

Spatial or temporal correlation of

migration with outbreaks


Turkey

2010

West Mongolia

2008/2009

East Mongolia

2006/2008

Kazakhstan

2007/2008

Egypt

2009

Nepal

2005

Qinghai China

2007/2009

Hong Kong

2008/2009

Poyang China

2007

Mali

2007

Nigeria

2007/2009

India

2008/2009/2011

Bangladesh

2010/2011

Malawi

2007

557 transmitters deployed

on 23 species in 11

countries


Can telemetry explain pattern of outbreaks in Asia?


East Mongolia

2006/2008

West Mongolia

2008/2009

Poyang, China

2007

Nepal

2005

Qinghai, China

2007/2009

Hong Kong

2008/2009

India

2008/2009/2011

Bangladesh

2008/2009/2011


Wild birds are not involved in

the spread of H5N1


Wild birds are not involved in

the spread of H5N1


Migration of Whooper Swans from East Mongolia

A

B


Spatial correlation with wild bird outbreaks in winter…

A

B

Newman et al., PLoS ONE. 2009, 4: e5729


Spatial correlation with wild bird outbreaks in winter…

Outbreaks of

HPAI in

migratory

waterbirds ( )

& wild nonwaterbirds

( )

Newman et al., PLoS ONE. 2009, 4: e5729


… but temporal mismatch between outbreaks & wintering

Outbreaks of HPAI in

poultry , migratory

birds & wild nonwaterbirds

Newman et al., PLoS ONE. 2009, 4: e5729


Poyang,

China


Intermixing of wild and domestic birds at Poyang

Rice fields

Domestic ducks with wild

Chinese spotbill

Takekawa et al., Avian Dis. 2010, 54: 466-476


Spatial correlation between migration & outbreaks?

Takekawa et al., Avian Dis. 2010, 54: 466-476


Spatial correlation between migration & outbreaks?

Brownian Bridge

Utilization Distribution

of waterfowl during

spring migration

Outbreaks not

correlated with

core migration

corridor

Density of poultry (brown

coloration gradient)

Outbreaks of HPAI

in poultry (▲) &

wild birds (○)

Takekawa et al., Avian Dis. 2010, 54: 466-476


Temporal correlation between migration & outbreaks?

Outbreaks not

correlated with

wild bird annual

cycle

Takekawa et al., Avian Dis. 2010, 54: 466-476


Wild birds are not involved in

the spread of H5N1


Hong Kong


Few healthy wild birds with HPAI infection

Global active surveillance > 750,000 samples collected only 16 healthy

wild birds detected with HPAI infection

Host species (no.) Location Sampling site Date of outbreak Reference

Wild ducks’ (6) Poyang Lake, China Wetland January 2005 Chen et al., 2006

Great crested grebe Siberia, Russia Wetland July 2005 Lvov et al., 2006

(1)

Common teal (1) Port Said, Egypt Live bird market January 2006 Saad et al., 2007

Bar-headed goose (1)

White-faced whistling

duck (1), spur-winged

goose (1)

Common pochard (1)

Qinghai Province,

China

Hadejia-Hguru

Wetlands

Lake Sempach,

Switzerland

Wetland April 2006 Lei et al., 2007

Wetland February 2007 Gaidet et al., 2008

Wetland March 2008 UN-FAO, 2008

Mallard (1), coot (1) Sazkoy, Turkey Hunting ground January 2008 Newman et al.,

2008

Mallard (1) Starnberg, Germany Hunting ground January 2009 UN-FAO

Mallard (1) Republic of Korea Wetland November 2010 UN-FAO

No wild bird reservoir exists for HPAI H5N1 viruses


Wild birds are involved in

the spread of H5N1


Wild birds are involved in

the spread of H5N1


Qinghai,

China


Spatial correlation between migration & outbreaks

90°E

First evidence of

40°N

connectivity between

outbreak sites

95°E

Qinghai Lake

100°E

Poultry Density

(Individuals/ km 2 )

35°N

0

2,500

HP H5N1 Outbreaks

Breed/Post

Winter

Wild

Poultry

30°N

Lhasa

Spring

90°E

95°E

100°E

Prosser et al., 2011. PLoS ONE, 6: e17622


Winter movements overlap with H5N1 outbreaks

Lhasa

Outbreak:

Jan 2008

1 km

Prosser et al., 2011. PLoS ONE, 6: e17622


Winter movements reveal proximity to captive facility

Prosser et al., 2011. PLoS ONE, 6: e17622


Wild bird outbreaks in spring migration & breeding

Prosser et al., 2011. PLoS ONE, 6: e17622


Phylogenetic support for wild bird dispersal

76

79

89

100

A/great crested grebe/Tyva/22/10

A/whooper swan/Mongolia/2/09

A/bar headed goose/Mongolia/X25/09

A/great crested grebe/Qinghai/1/09

100

A/black headed gull/Tyva/115/09

A/whooper swan/Hokkaido/2/08

73 A/chicken/Hunan/3/07

62

100 A/guinea fowl/North Okkalarpa/834/07

A/quail/Mingalardone/866/07

96

A/shrike/Tibet/13/06

A/chicken/Tibet/6/08

85

A/chicken/Guiyang/3055/05

100

A/chicken/Assam/140187/08

98

100

A/chicken/Bangladesh/364/07

A/grebe/Tyva/Tyv06-8/06

A/whooper swan/Mongolia/2/06

A/common goldeneye/Mongolia/12/06

A/great cormorant/Tibet/12/06

96

A/bar-headed goose/Tibet/8/06

81

80

61

60

A/black headed gull/Qinghai/3/06

A/bar headed goose/Qinghai/F/06

A/mute swan/Astrakhan/Ast05-2-10/05

100

A/whooper swan/Mongolia/244/05

50

A/bar headed goose/Qinghai/0510/05

76

A/brown headed gull/Qinghai/3/05

A/bar-headed goose/Qinghai/3/05

A/duck/Guangxi/50/01

A/migratory duck/Jiangxi/1653/05

67

100

A/duck/Guangxi/2775/05

50

55

A/tree sparrow/Henan/1/04

A/blackbird/Hunan/1/04

A/chicken/Shanxi/2/06

99

A/chicken/Pyigyitagon/204/06

A/duck/Guangxi/1378/04

100

A/duck/Guangxi/2396/04

A/chicken/Hong Kong/SF219/01

A/goose/Guangdong/1/96

100

A/Hong Kong/156/97

0.005

2.3.2

2.3.4

2.3.3

2.2.3

2.2.2

2.2.1

9

6

4

5

3

0

Prosser et al., 2011. PLoS ONE, 6: e17622


Qinghai,

China


Annual cycle of Bar-Headed Goose


Annual cycle of Bar-Headed Goose


Outbreaks correlated in space & time with BHGO

Poultry outbreaks

Wild bird outbreaks

14-day

interval Outbreaks

Proportion in

UD p-value Outbreaks

Proportion in

UD p-value

23-Dec 14 0.455 0.007 0

8-Jan 39 0.862


Migration vs phylogenetic mapping of H5N1 spread

Wild birds are involved in

the spread of H5N1


How can an infected bird fly?

• Fatally-infected birds show neurological disorders such as

imbalance, circling locomotion, lose of neck muscle control

• Do wild birds infected

with HPAI H5N1 have

the capacity to migrate

long-distance?

• Use satellite telemetry to

estimate how far different

species can travel before

clinical symptoms appear


Dispersal potential of 11 waterfowl species

100%

• Potential for rapid

movement of H5N1

during asymptomatic

period

90%

80%

70%

60%

50%

40%

• Maximum dispersal

was 300-1600 km in

1-4 days

D0

Dmax1

Dmax2

Dmax3

Dmax4

Dmax5

Dmax6

Dmax7

Dmax8

Dmax9

Dmax10

Dmax11

Dmax12

Dmax13

Dmax14

Dmax15

Dmax16

30%

20%

10%

0%

Dmax17

Spring Migration

Baikal Teal

Bar-headed Goose

Common Shelduck

Common Teal

Eurasian Wigeon

Falcated Teal

Garganey

Northern Pintail

Northern Shoveler

Ruddy Shelduck

Swan Goose

Gaidet et al. 2010. Journal of Applied Ecology, 47: 1169-1179


Significance of stopover sites

• Species such as the teal can migrate over 1,000 km within

period of asymptomatic infection

• Likelihood for long-distance dispersal by individuals is low:

we estimated only 4 -10 days of infection per year would

result in a dispersal of HPAI H5N1 virus > 500 km

• However spread is most through

relay transmission between a

series of successively infected

migratory birds

Gaidet et al. 2010. Journal of Applied Ecology, 47: 1169-1179


Lessons from wild bird studies…


Lessons from wild bird studies

Wild birds do not (currently) act as a reservoir for H5N1

• Spread of H5N1 over long distances is limited spring / autumn migration

• Most birds do not achieve

speeds to transport virus in a

single migration, so relay

transmission is likely mode

of spread

90%

80%

70%

60%

50%

40%

30%

20%

10%

0%

Central Asia

Dmax4 >100

Dmax4 >500

JAN FEB MAR APR MAY JUN JUL AUG SEP OCT NOV DEC

(63) (54) (53) (53) (42) (30) (39) (37) (57) (57) (50) (66)


Lessons from wild bird studies

• Regional differences exist in the likelihood of wild birds to disperse virus

i.e. Central Asian Flyway has emerged

as H5N1 ‘thoroughfare’

• Generally, no crossover of birds

between Central Asian and

East Asian flyways, but exceptions occur

• Overlap between domestic duck

(reservoir) and wild birds (agents for

dispersal) at agricultural wetlands is a

precursor for spread

Wild bird outbreaks often follow rather

than precede poultry i.e. they are a

symptom


What data is needed to assess wild bird role?

◈Surveillance of wild birds, especially negative results & sample sizes

◈Detailed information about outbreaks (GPS locations, species, proximity

to human settlements/agriculture)

Wild bird ecology data (population counts, distribution, habitat use,

migratory routes, wintering sites, breeding areas)

Wild-domestic bird association (location, timing, duration of interactions)

◈Live bird markets (how many, which species,

volume traded) & market chains where

wild and domestic birds mix

◈Trade of wildlife across borders & for cultural

practices


Gaps in understanding movements in East Asian Flyway

Bangladesh ?

Vietnam ?

Indonesia ?

Thailand ?


Prevention & control…in the face of growing population

Population-skewed Earth 2050, 9 Billion and climbing?

1.4B

1.6B

6 Billion (2/3) in South Asia, East Asia, and Africa


Acknowledgements

USGS Western Ecological Research Center (S. Schwarzbach, S. Iverson, S. W. Perry, K. Spragens, E.

Palm, A. Schultz); USGS Patuxent Wildlife Research Center (D. Prosser, B. Collins, S. Heath , G.

Olsen, G. Smith, J. Howell); USGS Alaska Science Center (D. Douglas); Food & Agriculture

Organization of the United Nations (T. McCracken, A. George)

CHINA: Chinese Academy of Sciences (B. Yan, F. Lei, Z. Luo, T. Li), Qinghai and Poyang Lake

National Nature Reserves (S. Li, Y. Hou, Z. Xing, W. Ji), University of Oklahoma (X. Xiao, D. Zhao),

Ohio State University (D. Janies), Hong Kong University (M. Peiris, C. Leung), World Wildlife Fund HK

(P. Leader, B. Smith)

INDIA: UAE Env. Agency (S. Javed), Bombay Natural History Society (S. Balachandran, A. Rahmani,

A. Sathyaselvam), Wetlands International (T. Mundkur, W. Hagemeijer)

MONGOLIA: Wildlife Science and Conservation Center (N. Batbayar), Mongolian Academy of

Sciences (T. Natsagdorjiin), University of Wales, Bangor (C. Bishop, P. Butler, L. Hawkes, P. Frappell,

B. Milsom, G. Scott, M. Wikelski)

NEPAL: NepalNature (R. Suwal), BBC (M. Games-Hughes)


Building global partnerships in surveillance

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