Possible role of wild birds in the spread of HPAI H5N1 in Asia, preventative & control measures

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Regional Expert Group Meeting, Tokyo, Japan Nichola

1 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

2 Timeline of H5N1 outbreaks in wild birds 1996 First detection in domestic goose, Guangdong, China 1997 First human death reported in Hong Kong 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 Recurrent (but smaller) outbreaks along Central Asia Flyway Now Clade becomes dominant strain in wild birds

3 Five years after Qinghai outbreak April May June July August

4 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

6 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

7 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

8 Using satellite telemetry to unravel the role of wild birds in transmission of AIV

9 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

Poyang China 2007 Mali 2007 Nigeria 2007/2009 India 2008/2009/2011

10 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 transmitters deployed on 23 species in 11 countries

11 Can telemetry explain pattern of outbreaks in Asia?

12 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

13 Wild birds are not involved in the spread of H5N1

14 Wild birds are not involved in the spread of H5N1

16 Migration of Whooper Swans from East Mongolia A B

17 Spatial correlation with wild bird outbreaks in winter A B Newman et al., PLoS ONE. 2009, 4: e5729

18 Spatial correlation with wild bird outbreaks in winter Outbreaks of HPAI in migratory waterbirds ( ) & wild nonwaterbirds ( ) Newman et al., PLoS ONE. 2009, 4: e5729

19 but temporal mismatch between outbreaks & wintering Outbreaks of HPAI in poultry, migratory birds & wild nonwaterbirds Newman et al., PLoS ONE. 2009, 4: e5729

20 Poyang, China

22 Intermixing of wild and domestic birds at Poyang Rice fields Domestic ducks with wild Chinese spotbill Takekawa et al., Avian Dis. 2010, 54:

23 Spatial correlation between migration & outbreaks? Takekawa et al., Avian Dis. 2010, 54:

24 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:

25 Temporal correlation between migration & outbreaks? Outbreaks not correlated with wild bird annual cycle Takekawa et al., Avian Dis. 2010, 54:

26 Wild birds are not involved in the spread of H5N1

27 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.

28 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

29 Wild birds are involved in the spread of H5N1

30 Wild birds are involved in the spread of H5N1

31 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 )

32 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 < ,000 1,000-2,500 >2,500 HP H5N1 Outbreaks Breed/Post Winter Wild Poultry 30 N Lhasa Spring 90 E 95 E 100 E Prosser et al., PLoS ONE, 6: e17622

33 Winter movements overlap with H5N1 outbreaks Lhasa Outbreak: Jan km Prosser et al., PLoS ONE, 6: e17622

34 Winter movements reveal proximity to captive facility Prosser et al., PLoS ONE, 6: e17622

35 Wild bird outbreaks in spring migration & breeding Prosser et al., PLoS ONE, 6: e17622

36 Phylogenetic support for wild bird dispersal 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/ A/black headed gull/tyva/115/09 A/whooper swan/hokkaido/2/08 73 A/chicken/Hunan/3/ 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/ A/chicken/Assam/140187/ 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/ A/black headed gull/qinghai/3/06 A/bar headed goose/qinghai/f/06 A/mute swan/astrakhan/ast / 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/ A/duck/Guangxi/2775/ 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/ A/duck/Guangxi/2396/04 A/chicken/Hong Kong/SF219/01 A/goose/Guangdong/1/ A/Hong Kong/156/ Prosser et al., PLoS ONE, 6: e17622

38 Qinghai, China

40 Annual cycle of Bar-Headed Goose

41 Annual cycle of Bar-Headed Goose

42 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 Jan < Mar Apr Jun Newman et al.,. PLoS Pathogens, in revision

43 Migration vs phylogenetic mapping of H5N1 spread Wild birds are involved in the spread of H5N1

44 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

45 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 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 Journal of Applied Ecology, 47:

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

46 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 Journal of Applied Ecology, 47:

47 Lessons from wild bird studies

48 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)

flyways, but exceptions occur Overlap between domestic duck (reservoir) and wild birds (agents for dispersal) at

49 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

50 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

51 Gaps in understanding movements in East Asian Flyway Bangladesh? Vietnam? Indonesia? Thailand?

52 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

53 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)

54 Building global partnerships in surveillance

H5N1 avian influenza: timeline

H5N1 avian influenza: timeline 28 October 2005 Previous events in Asia 1996 Highly pathogenic H5N1 virus is isolated from a farmed goose in Guangdong Province, China. 1997 Outbreaks of highly pathogenic