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M. Gilbert 
Université Libre de Bruxelles 
Livestock Systems and Environment (LSE) Seminar 
ILRI, Nairobi, 23 January 2014 
Spatial epidemiology of avian influenza in Asia and intensifying poultry production systems
Spatial epidemiology of avian influenza in Asia and intensifying poultry production systems 
M. Gilbert 
Biological control and spatial ecology, 
Université Libre de Bruxelles 
http://lubies.ulb.ac.be/Spatepi.html
HPAI H5N1 (FAO Empres-I): 2004-2012
A moving target #1: distribution in Thailand 
1 Jan 2004 – 1 Jul 2004 
1 Jul 2004 – 1 Jul 2005 
1 Jul 2005 – end 2008
A moving target #2: distribution in Indonesia 
2004 - 2008 
2009 
2010 
2011
2006 A moving target #3: distribution in India & Bangladesh 
2007-2011 
2012
Outbreaks 
A moving target #3: distribution in China 
Human cases 
Positive markets
How to deal with those different situations ? 
Pattern of spread 
•Absence can be suitable 
Pattern of surveillance and control 
•What is an absence ? 
Analysis 
•Break down by country / epidemic phase 
Comparative analysis 
•Gain a general understanding from multiple studies
Focus on a limited set of factors 
•What animal is infected 
•Pattern of excretion (quantity, duration) 
•Contacts with other hosts 
Hosts 
•How host are moved; 
•How fomites are moved; 
•Surveillance, prevention, control 
Anthropogenic 
•How and where the virus persists outside the host 
•How and where poultry are raised 
Environment
Time line 
0 
200 
400 
600 
800 
1000 
1200 
1400 
2004 
2005 
2006 
2007 
2008 
2009 
2010 
2011 
2012 
EMPRES-I HPAI H5N1 records (Asia) 
THA 
IDN 
CHN 
IND 
BGD 
VNM
2004 First steps: firefighting in Thailand
HPAI H5N1 & ducks in Thailand 
Farm chicken 
Native chicken 
HPAI H5N1 Gilbert et al. (2006) EID 12(2):227-234
HPAI H5N1 & ducks in Thailand 
Farm ducks 
Free grazing ducks 
HPAI H5N1 Gilbert et al. (2006) EID 12(2):227-234
Free-grazing ducks can be mapped using 
remotely sensed indicators 
Gilbert et al. (2007) Ag., Eco. Env. 119:409-415
Thailand and Vietnam model
• Cropping intensity, domestick duck density, human population 
density, chicken density (VNM) as main risk factors 
• In Thailand: Paul et al. (2010); Tiensin et al. (2009) 
• In Vietnam: Pfeiffer et al. (2007) 
Spatial model: building and validation 0.0 0.2 0.4 0.6 0.8 1.0 
0.0 1 - Specificity 
0.0 0.2 0.4 0.6 0.8 1.0 
0.0 1 - Specificity 
0.0 0.2 0.4 0.6 0.8 1.0 
0.0 0.4 0.8 
1 - Specificity 
Sensitivity 
AUC = 0.66 +/- 0.0081 
Vietnam: Wave I 
0.0 0.2 0.4 0.6 0.8 1.0 
0.0 0.4 0.8 
1 - Specificity 
Sensitivity 
AUC = 0.742 +/- 0.0142 
Vietnam: Wave II 
0.8 
0.8 
1.0 
0.0 0.2 0.4 0.6 0.8 1.0 
0.0 0.2 0.4 0.6 0.8 1.0 
1 - Specificity 
Sensitivity 
Vietnam 
Wave I 
Wave II 
Wave III 
Gilbert et al. (2008) PNAS 105: 4769-4774
Spatial model: predictions 
Gilbert et al. (2008) PNAS 105: 4769-4774
Predictions in Indonesia 
Loth et al. (2011) Prev. Vet. Medecine. Doi:10.1016/j.prevetmed.2011.06.006
Predictions in South Asia Gilbert et al. (2010) Ecohealth 7(4):448-58
Outbreak density profile in Thailand 
Thailand 
Outbreak Density 
0.0 - 0.2 
0.2 - 0.5 
0.5 - 0.8 
0.8 - 1.0 
1.0 - 1.2 
1.2 - 1.5 
1.5 - 1.8 
1.8 - 2.0 
2.0 - 2.2 
2.2 - 2.5 
2.5 - 2.8 
2.8 - 3.0 
3.0 - 3.2 
3.2 - 3.5 
3.5 - 3.8 
3.8 - 4.0 
0.000 0.004 0.008 0.012 
Gilbert et al. (2010) Ecohealth 7(4):448-58
Outbreak density profile in Thailand vs. 
Vietnam 
Thailand 
Outbreak Density 
0.0 - 0.2 
0.2 - 0.5 
0.5 - 0.8 
0.8 - 1.0 
1.0 - 1.2 
1.2 - 1.5 
1.5 - 1.8 
1.8 - 2.0 
2.0 - 2.2 
2.2 - 2.5 
2.5 - 2.8 
2.8 - 3.0 
3.0 - 3.2 
3.2 - 3.5 
3.5 - 3.8 
3.8 - 4.0 
0.000 0.004 0.008 0.012 
THA 
Vietnam 
0.004 0.008 
VNM
Outbreak density profiles 
Thailand 
Outbreak Density 
0.0 - 0.2 
0.2 - 0.5 
0.5 - 0.8 
0.8 - 1.0 
1.0 - 1.2 
1.2 - 1.5 
1.5 - 1.8 
1.8 - 2.0 
2.0 - 2.2 
2.2 - 2.5 
2.5 - 2.8 
2.8 - 3.0 
3.0 - 3.2 
3.2 - 3.5 
3.5 - 3.8 
3.8 - 4.0 
0.000 0.004 0.008 0.012 
Vietnam 
Outbreak Density 
0.0 - 0.2 
0.2 - 0.5 
0.5 - 0.8 
0.8 - 1.0 
1.0 - 1.2 
1.2 - 1.5 
1.5 - 1.8 
1.8 - 2.0 
2.0 - 2.2 
2.2 - 2.5 
2.5 - 2.8 
2.8 - 3.0 
3.0 - 3.2 
3.2 - 3.5 
3.5 - 3.8 
3.8 - 4.0 
0.000 0.004 0.008 
India 
Outbreak Density 
0.0 - 0.2 
0.2 - 0.5 
0.5 - 0.8 
0.8 - 1.0 
1.0 - 1.2 
1.2 - 1.5 
1.5 - 1.8 
1.8 - 2.0 
2.0 - 2.2 
2.2 - 2.5 
2.5 - 2.8 
2.8 - 3.0 
3.0 - 3.2 
3.2 - 3.5 
3.5 - 3.8 
3.8 - 4.0 
0e+00 4e-04 
Bangladesh 
Outbreak Density 
0.0 - 0.2 
0.2 - 0.5 
0.5 - 0.8 
0.8 - 1.0 
1.0 - 1.2 
1.2 - 1.5 
1.5 - 1.8 
1.8 - 2.0 
2.0 - 2.2 
2.2 - 2.5 
2.5 - 2.8 
2.8 - 3.0 
3.0 - 3.2 
3.2 - 3.5 
3.5 - 3.8 
3.8 - 4.0 
0.000 0.002 0.004 
Gilbert et al. (2010) Ecohealth 7(4):448-58
Production structure in Thailand Van Boeckel et al. (2012) Ag., Eco. Env. 10.1016/j.agee.2011.12.019
Disagregating poultry data Van Boeckel et al. (2012) Ag., Eco. Env. 10.1016/j.agee.2011.12.019
BRT model in Thailand Van Boeckel et al. PLOS ONE 7(11): e49528. doi:10.1371/journal.pone.0049528
Different duck systems 
Delineate areas where HPAI can persist 
Free-grazing, local movements e.g. Bangladesh, India, Indonesia, Nigeria 
Free-grazing intensive movements e.g. Central plain of Thailand, Vietnam deltas 
Farmed e.g. North- eastern Thailand
Review paper on HPAI H5N1 risk factors
Review paper on HPAI H5N1 risk factors 
•Factors have been studied at various scale: farm to country level; 
•Factors were very different from one study to another: real difficulty in comparing studies outcomes; 
•Overall, some factors showed consistent association with the risk of HPAI H5N1 presence across countries and scales: 
•Domestick duck density; 
•Anthropogenic (Human pop. density, distance to roads, markets) 
•Indicators of water presence 
•The effect of chicken density is variable, most likely due to differences in production systems
Review of HPAI H5N1 risk factors 
•Factors have been overlooked: 
•Socio-economic; 
•Trade and market networks; 
•Wild bird distribution and movement;
Duck distribution
Intensification of duck production in China 
First report of H5N1
China: 75% of ducks 
•Outbreaks (mainly in chicken farms) 
•H5N1 positives from markets Martin et al. (2011) Plos Pathogens 7(3): e1001308
BRT model 
•Outbreaks 
•Chicken and human pop. density; 
•More emphasis on the intensive productions areas 
•Market surveillance 
•Hpop, duck density, and % water. 
•Duck/rice ecosystem in the south Martin et al. (2011) Plos Pathogens 7(3): e1001308
•Poyang lake: main lake for migratory watefowls
•Poyang lake: wild geese farms
•Poyang lake: main lake for migratory watefowls 
Poyang lake populations 
0.5 million wild birds (75 species); 
3 millions « farmed » wild birds; 
Surrounded by 10 counties with 
26 million ducks and geese in farms; 
21 million domestic chicken in farms; 
6 million people;
Temporal patterns in Poyang lake Cappelle et al. (in revision)
Spatial patterns in Poyang lake Cappelle et al. (in revision)
Live-bird market networks Martin et al. (2011)
Intensified poultry production rapidly, duck population that outweights all other coutries 
In regions with extensive interface with the wild avifauna 
Connectivity between regions is facilitated by long-distance trade between live-bird markets 
Relevance to H7N9 ? 
China
A quick virtual tour in Huzhou 
Detailed investigation for all 12 confirmed H7N9 cases in Huzhou, Zhejiang province (http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20481). Linked to markets with: Chickens infection rate of samples = 36 / 129 = 27% Pigeon infection rate of samples = 2 / 6 = 33%
A quick virtual tour in Huzhou
A quick virtual tour in Huzhou
A quick virtual tour in Huzhou
A quick virtual tour in Huzhou
H7N9 in China: geographic space
H7N9 in China: var space 
•Human population 
•Duck population 
•Chicken population 
•% of land occupied by water 
•% of land occupied by rice paddy fields 
•Accessibilit y(travel time to major cities) 
•Live-bird market density
BRT profiles
H7N9 risk maps
Combined risk
Live bird markets 
•Important and widespread in China, Vietnam, Bangladesh, Indonesia, Cambodia 
•Can allow disease spread and persistence through the meta-population of live-bird markets 
•Social Network Analysis combined with mathematical modelling shows potential for targetting markets where intervention would be most beneficial (Fournie et al. 2012, 2013) 
•The current missing elements to understand AI (H5N1/H7N9) persistence and spread ?
Intensification of duck production in China 
First report of H5N1
Global trends 
0500,000,0001,000,000,0001,500,000,0002,000,000,0002,500,000,000 1961196519691973197719811985198919931997200120052009Heads Cattle & BuffaloesSheep and GoatsChicken (/10)Pork
Where are we going ? 
•On-going intensification in China, extensive wild bird interface, high LBM density 
•India / Bangladesh: intensification, duck population, extensive interface with wild birds, live bird markets 
•Is large-scale farming with high biosafety the only way to intensify production safely ? 
•Can subsistance and commercial poultry farming co- exist ?
Back to Thailand 
One of the highest density of domestick ducks; 
Extensive irrigated land; 
Large commercial sector; 
Smallholders & native chickens; 
High human population density; 
Few or no live-bird markets
Conclusion 
•Key role of ducks => differ according to production systems 
•Intensification of duck production in contact with WB genetic pool of viruses 
•Spread to other poultry and human exposure facilitated by LBM networks 
•Try not having both
Thank you 
Acknowledgments: J. Cappelle, L. Hogerwerf, L. Loth, V. Martin, S. Newman, M. Paul, D. Pfeiffer, D. Prosser, T. Robinson, J. Slingenbergh, K. Stevens, W. Thapongtharm, T. Boeckel, R. Wallace, W. Wint, X. Xiao ,

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Spatial epidemiology of avian influenza in Asia and intensifying poultry production systems

  • 1. M. Gilbert Université Libre de Bruxelles Livestock Systems and Environment (LSE) Seminar ILRI, Nairobi, 23 January 2014 Spatial epidemiology of avian influenza in Asia and intensifying poultry production systems
  • 2. Spatial epidemiology of avian influenza in Asia and intensifying poultry production systems M. Gilbert Biological control and spatial ecology, Université Libre de Bruxelles http://lubies.ulb.ac.be/Spatepi.html
  • 3. HPAI H5N1 (FAO Empres-I): 2004-2012
  • 4. A moving target #1: distribution in Thailand 1 Jan 2004 – 1 Jul 2004 1 Jul 2004 – 1 Jul 2005 1 Jul 2005 – end 2008
  • 5. A moving target #2: distribution in Indonesia 2004 - 2008 2009 2010 2011
  • 6. 2006 A moving target #3: distribution in India & Bangladesh 2007-2011 2012
  • 7. Outbreaks A moving target #3: distribution in China Human cases Positive markets
  • 8. How to deal with those different situations ? Pattern of spread •Absence can be suitable Pattern of surveillance and control •What is an absence ? Analysis •Break down by country / epidemic phase Comparative analysis •Gain a general understanding from multiple studies
  • 9. Focus on a limited set of factors •What animal is infected •Pattern of excretion (quantity, duration) •Contacts with other hosts Hosts •How host are moved; •How fomites are moved; •Surveillance, prevention, control Anthropogenic •How and where the virus persists outside the host •How and where poultry are raised Environment
  • 10. Time line 0 200 400 600 800 1000 1200 1400 2004 2005 2006 2007 2008 2009 2010 2011 2012 EMPRES-I HPAI H5N1 records (Asia) THA IDN CHN IND BGD VNM
  • 11. 2004 First steps: firefighting in Thailand
  • 12. HPAI H5N1 & ducks in Thailand Farm chicken Native chicken HPAI H5N1 Gilbert et al. (2006) EID 12(2):227-234
  • 13. HPAI H5N1 & ducks in Thailand Farm ducks Free grazing ducks HPAI H5N1 Gilbert et al. (2006) EID 12(2):227-234
  • 14. Free-grazing ducks can be mapped using remotely sensed indicators Gilbert et al. (2007) Ag., Eco. Env. 119:409-415
  • 16. • Cropping intensity, domestick duck density, human population density, chicken density (VNM) as main risk factors • In Thailand: Paul et al. (2010); Tiensin et al. (2009) • In Vietnam: Pfeiffer et al. (2007) Spatial model: building and validation 0.0 0.2 0.4 0.6 0.8 1.0 0.0 1 - Specificity 0.0 0.2 0.4 0.6 0.8 1.0 0.0 1 - Specificity 0.0 0.2 0.4 0.6 0.8 1.0 0.0 0.4 0.8 1 - Specificity Sensitivity AUC = 0.66 +/- 0.0081 Vietnam: Wave I 0.0 0.2 0.4 0.6 0.8 1.0 0.0 0.4 0.8 1 - Specificity Sensitivity AUC = 0.742 +/- 0.0142 Vietnam: Wave II 0.8 0.8 1.0 0.0 0.2 0.4 0.6 0.8 1.0 0.0 0.2 0.4 0.6 0.8 1.0 1 - Specificity Sensitivity Vietnam Wave I Wave II Wave III Gilbert et al. (2008) PNAS 105: 4769-4774
  • 17. Spatial model: predictions Gilbert et al. (2008) PNAS 105: 4769-4774
  • 18. Predictions in Indonesia Loth et al. (2011) Prev. Vet. Medecine. Doi:10.1016/j.prevetmed.2011.06.006
  • 19. Predictions in South Asia Gilbert et al. (2010) Ecohealth 7(4):448-58
  • 20. Outbreak density profile in Thailand Thailand Outbreak Density 0.0 - 0.2 0.2 - 0.5 0.5 - 0.8 0.8 - 1.0 1.0 - 1.2 1.2 - 1.5 1.5 - 1.8 1.8 - 2.0 2.0 - 2.2 2.2 - 2.5 2.5 - 2.8 2.8 - 3.0 3.0 - 3.2 3.2 - 3.5 3.5 - 3.8 3.8 - 4.0 0.000 0.004 0.008 0.012 Gilbert et al. (2010) Ecohealth 7(4):448-58
  • 21. Outbreak density profile in Thailand vs. Vietnam Thailand Outbreak Density 0.0 - 0.2 0.2 - 0.5 0.5 - 0.8 0.8 - 1.0 1.0 - 1.2 1.2 - 1.5 1.5 - 1.8 1.8 - 2.0 2.0 - 2.2 2.2 - 2.5 2.5 - 2.8 2.8 - 3.0 3.0 - 3.2 3.2 - 3.5 3.5 - 3.8 3.8 - 4.0 0.000 0.004 0.008 0.012 THA Vietnam 0.004 0.008 VNM
  • 22. Outbreak density profiles Thailand Outbreak Density 0.0 - 0.2 0.2 - 0.5 0.5 - 0.8 0.8 - 1.0 1.0 - 1.2 1.2 - 1.5 1.5 - 1.8 1.8 - 2.0 2.0 - 2.2 2.2 - 2.5 2.5 - 2.8 2.8 - 3.0 3.0 - 3.2 3.2 - 3.5 3.5 - 3.8 3.8 - 4.0 0.000 0.004 0.008 0.012 Vietnam Outbreak Density 0.0 - 0.2 0.2 - 0.5 0.5 - 0.8 0.8 - 1.0 1.0 - 1.2 1.2 - 1.5 1.5 - 1.8 1.8 - 2.0 2.0 - 2.2 2.2 - 2.5 2.5 - 2.8 2.8 - 3.0 3.0 - 3.2 3.2 - 3.5 3.5 - 3.8 3.8 - 4.0 0.000 0.004 0.008 India Outbreak Density 0.0 - 0.2 0.2 - 0.5 0.5 - 0.8 0.8 - 1.0 1.0 - 1.2 1.2 - 1.5 1.5 - 1.8 1.8 - 2.0 2.0 - 2.2 2.2 - 2.5 2.5 - 2.8 2.8 - 3.0 3.0 - 3.2 3.2 - 3.5 3.5 - 3.8 3.8 - 4.0 0e+00 4e-04 Bangladesh Outbreak Density 0.0 - 0.2 0.2 - 0.5 0.5 - 0.8 0.8 - 1.0 1.0 - 1.2 1.2 - 1.5 1.5 - 1.8 1.8 - 2.0 2.0 - 2.2 2.2 - 2.5 2.5 - 2.8 2.8 - 3.0 3.0 - 3.2 3.2 - 3.5 3.5 - 3.8 3.8 - 4.0 0.000 0.002 0.004 Gilbert et al. (2010) Ecohealth 7(4):448-58
  • 23. Production structure in Thailand Van Boeckel et al. (2012) Ag., Eco. Env. 10.1016/j.agee.2011.12.019
  • 24. Disagregating poultry data Van Boeckel et al. (2012) Ag., Eco. Env. 10.1016/j.agee.2011.12.019
  • 25. BRT model in Thailand Van Boeckel et al. PLOS ONE 7(11): e49528. doi:10.1371/journal.pone.0049528
  • 26. Different duck systems Delineate areas where HPAI can persist Free-grazing, local movements e.g. Bangladesh, India, Indonesia, Nigeria Free-grazing intensive movements e.g. Central plain of Thailand, Vietnam deltas Farmed e.g. North- eastern Thailand
  • 27. Review paper on HPAI H5N1 risk factors
  • 28. Review paper on HPAI H5N1 risk factors •Factors have been studied at various scale: farm to country level; •Factors were very different from one study to another: real difficulty in comparing studies outcomes; •Overall, some factors showed consistent association with the risk of HPAI H5N1 presence across countries and scales: •Domestick duck density; •Anthropogenic (Human pop. density, distance to roads, markets) •Indicators of water presence •The effect of chicken density is variable, most likely due to differences in production systems
  • 29. Review of HPAI H5N1 risk factors •Factors have been overlooked: •Socio-economic; •Trade and market networks; •Wild bird distribution and movement;
  • 31. Intensification of duck production in China First report of H5N1
  • 32. China: 75% of ducks •Outbreaks (mainly in chicken farms) •H5N1 positives from markets Martin et al. (2011) Plos Pathogens 7(3): e1001308
  • 33. BRT model •Outbreaks •Chicken and human pop. density; •More emphasis on the intensive productions areas •Market surveillance •Hpop, duck density, and % water. •Duck/rice ecosystem in the south Martin et al. (2011) Plos Pathogens 7(3): e1001308
  • 34. •Poyang lake: main lake for migratory watefowls
  • 35.
  • 36.
  • 37.
  • 38. •Poyang lake: wild geese farms
  • 39. •Poyang lake: main lake for migratory watefowls Poyang lake populations 0.5 million wild birds (75 species); 3 millions « farmed » wild birds; Surrounded by 10 counties with 26 million ducks and geese in farms; 21 million domestic chicken in farms; 6 million people;
  • 40. Temporal patterns in Poyang lake Cappelle et al. (in revision)
  • 41. Spatial patterns in Poyang lake Cappelle et al. (in revision)
  • 42. Live-bird market networks Martin et al. (2011)
  • 43. Intensified poultry production rapidly, duck population that outweights all other coutries In regions with extensive interface with the wild avifauna Connectivity between regions is facilitated by long-distance trade between live-bird markets Relevance to H7N9 ? China
  • 44. A quick virtual tour in Huzhou Detailed investigation for all 12 confirmed H7N9 cases in Huzhou, Zhejiang province (http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20481). Linked to markets with: Chickens infection rate of samples = 36 / 129 = 27% Pigeon infection rate of samples = 2 / 6 = 33%
  • 45. A quick virtual tour in Huzhou
  • 46. A quick virtual tour in Huzhou
  • 47. A quick virtual tour in Huzhou
  • 48. A quick virtual tour in Huzhou
  • 49. H7N9 in China: geographic space
  • 50. H7N9 in China: var space •Human population •Duck population •Chicken population •% of land occupied by water •% of land occupied by rice paddy fields •Accessibilit y(travel time to major cities) •Live-bird market density
  • 54. Live bird markets •Important and widespread in China, Vietnam, Bangladesh, Indonesia, Cambodia •Can allow disease spread and persistence through the meta-population of live-bird markets •Social Network Analysis combined with mathematical modelling shows potential for targetting markets where intervention would be most beneficial (Fournie et al. 2012, 2013) •The current missing elements to understand AI (H5N1/H7N9) persistence and spread ?
  • 55. Intensification of duck production in China First report of H5N1
  • 56. Global trends 0500,000,0001,000,000,0001,500,000,0002,000,000,0002,500,000,000 1961196519691973197719811985198919931997200120052009Heads Cattle & BuffaloesSheep and GoatsChicken (/10)Pork
  • 57. Where are we going ? •On-going intensification in China, extensive wild bird interface, high LBM density •India / Bangladesh: intensification, duck population, extensive interface with wild birds, live bird markets •Is large-scale farming with high biosafety the only way to intensify production safely ? •Can subsistance and commercial poultry farming co- exist ?
  • 58. Back to Thailand One of the highest density of domestick ducks; Extensive irrigated land; Large commercial sector; Smallholders & native chickens; High human population density; Few or no live-bird markets
  • 59. Conclusion •Key role of ducks => differ according to production systems •Intensification of duck production in contact with WB genetic pool of viruses •Spread to other poultry and human exposure facilitated by LBM networks •Try not having both
  • 60. Thank you Acknowledgments: J. Cappelle, L. Hogerwerf, L. Loth, V. Martin, S. Newman, M. Paul, D. Pfeiffer, D. Prosser, T. Robinson, J. Slingenbergh, K. Stevens, W. Thapongtharm, T. Boeckel, R. Wallace, W. Wint, X. Xiao ,