Avian influenza at the poultry-human interface: Bangladesh

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Avian influenza at the poultry-human interface: Bangladesh Syed Sayeem Uddin Ahmed, PhD Senior International Fellow Infectious Diseases Division Programme on Emerging Infections icddr,b Solving public health problems through innovative scientific research www.icddrb.org

First reported in February 2007 Bangladesh reported 550 poultry outbreaks in poultry 8 human cases Close interaction between human and poultry Novel influenza viruses may evolve at poultry human interfaces Source: OIE

H5N1 reported outbreaks in Bangladesh (2007-2016) 100 90 Number of reported outbreaks 80 70 60 50 40 30 20 10 0 JFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASOND 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 Time

Avian Influenza Surveillances Avian Influenza Surveillance in Bangladesh Live bird market (LBM) surveillance Community-based surveillance among backyard poultry flocks Surveillance for human infections with avian influenza A viruses among live bird market (LBM) workers in Dhaka city area, Bangladesh

Avian Influenza Surveillance in Bangladesh Live bird market (LBM) surveillance Objective: Surveillance sites To identify and characterize circulating avian influenza A viruses in domestic poultry To identify avian influenza A viruses in the environment of LBM 29 LBMs from 12 geographical areas

Sampling 275 Individual poultry samples: Cloacal and tracheal swabs from 80 waterfowl per month 145 commercial chickens per month 50 backyard chicken per month 29 Environmental pool samples Demographic, management & health data

% rrt-pcr confirmed influenza 25% 20% 15% 10% 5% 0% Surveillance findings Summary of influenza A surveillance in waterfowl from live bird markets (Oct'2007 to May 2016) Total sample tested: 7400 Influenza A positive: 409 (6%) H5 positive: 167 (41% among infl. A positive specimens) ONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAM 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 90 80 70 60 50 40 30 20 10 0 Number of samples tested Influenza A/H5 & H9 Influenza A/unsubtypeable Influenza A/H7 Influenza A/H9 Influenza A/H5 Number of samples tested Note: Subtyping for H7 and H9 was started on September 2013

Summary of influenza A surveillance in Commercial chicken from live bird markets (Sep 2013 to May 2016) Total sample tested: 4605 Influenza A positive: 129 (3%) H5 positive: 20 (16% among infl. A positive specimens) % rrt-pcr confirmed influenza 10% 9% 8% 7% 6% 5% 4% 3% 2% 1% 0% S O N D J F M A M J J A S O N D J F M A M J J A S O N D J F M A M 2013 2014 2015 2016 160 140 120 100 80 60 40 20 0 Number of samples tested Influenza A/H5 & H9 Influenza A/unsubtypeable Influenza A/H7 Influenza A/H9 Influenza A/H5 Number of samples tested

Summary of influenza A surveillance in backyard chicken from live bird markets (Sep 2013 to May 2016) Total sample tested: 1550 Influenza A positive: 28 (2%) H5 positive: 18 (64% among infl. A positive specimens) % rrt PCR confirmed influenza 18% 16% 14% 12% 10% 8% 6% 4% 2% 0% S O N D J F M A M J J A S O N D J F M A M J J A S O N D J F M A M 2013 2014 2015 2016 Influenza A/H5 & H9 Influenza A/unsubtypeable Influenza A/H7 Influenza A/H9 Influenza A/H5 Number of samples tested 60 50 40 30 20 10 0 Number of samples tested

% rrt-pcr confirmed influenza 120% 100% 80% 60% 40% 20% 0% Live bird market pooled environmental samples for influenza A surveillance (May 2009-May 2016) Total sample tested: 1733 Influenza A positive: 498 (29%) H5 positive: 189 (38% among infl. A positive specimens) MJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAM 2009 2010 2011 2012 2013 2014 2015 2016 2009 2010 2011 2012 2013 2014 2015 2016 35 30 25 20 15 10 5 0 Number of samples tested Influenza A/H5 & H9 Influenza A/unsubtypeable Influenza A/H7 Influenza A/H9 Influenza A/H5 Number of samples tested Note: Subtyping for H7 and H9 was started on September 2013

Avian Influenza Surveillance in Bangladesh Community-based surveillance To identify backyard poultry die off due to avian influenza and circulating strains at community level Surveillance sites 5 community sites from different geographical areas

Community surveillance 5 Community data collectors visit 200 households (40 from each community) twice a week Collect backyard poultry health data Report unusual die off to the center Field research team travel to the site and collect required specimen

Community surveillance Identified suspected mortality event for HPAI 42 Number of event positive for H5 subtype 12 (29%) 3 Mortality event Event positive for H5 Number of events 2 1 0 MJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJ 2008 2009 2010 2011 2012 2013 2014 2015 2016 2008 2009 2010 2011 2012 2013 2014 2015 2016 Time

LBM workers surveillance Objectives: To identify the incidence of avian influenza A viruses among poultry workers Comparison of currently circulating influenza A subtypes among poultry workers in live bird markets To assess the serological evidence of avian influenza infection among live bird market workers

Methods: Study Cohort Initiated this surveillance in February 2012 in 16 markets Cohort of LBM workers and their household members: LBM workers (n=750) Household members (n = 1,830) Suspected avian influenza infection Identification of suspected cases of avian influenza virus infection: Twice a week follow-up with enrolled LBM workers and ask about illness in previous 3 days among worker or household members

30 LBM PWs surveillance influenza seasonality graph Influenza B Inconclusive Flu A Influenza A/Unsubtypeable Avian Flu (H5+H9) Total number of respiratory illness cases Co infections/co detection Human adapted Flu (H1N1pdm+H3) 100 Number of RT PCR Confirmed Influenza 25 20 15 10 5 90 Total no of Respiratory Illness cases 80 70 60 50 40 30 20 10 0 Feb Apr Jun Aug Oct Dec Feb Apr Jun Aug Oct Dec Feb Apr Jun Aug Oct Dec Feb Apr June Aug Oct Dec 2012 2013 2014 2015 0

Subtypes indentified Both HPAI and LPAI H1N1 H1N3 H3N2 H3N8 H4N1 H4N6 H5N1 H5N2 H6N1 H7N9 H9N2 H11N2 H11N3 HxN1 Six clades of H5N1 2.2 2.3.2.1 2.3.4 2.2.2 2.3.2.2 2.3.4.2

Conclusions Year round circulation avian influenza viruses including H5 subtype observed LBMs serve as a low cost platform for sentinel detection of novel influenza viruses of public health importance Avian influenza viruses contaminate environment of live bird market In heavily contaminated environments, rrt-pcr may detect avian influenza A viral RNA in human respiratory specimens in the absence of infection Difficult to interpret the rrt-pcr data without serological results

Collaboration Directorate General of Health Services Department of Livestock Services Department of Forest

Acknowledgements For funding: US-CDC icddr,b Zakiul Hassan Sukanta Chowdhury M Rahman MZ Rahman E Hossain Sadia Afreen T Azim AA Mamun S Nasreen Salah Uddin Khan IEDCR : M Rahman S Haider Stanford University Steve Luby Core donors of icddr,b DLS FAO US-CDC: Kevin Russell Erin Kennedy K Sturm-Ramirez JD Heffelfinger Berman R Donis K Hancock D Iuliano J Katz ZN Li S Lindstrom F Liu J Miller TM Uyeki Todd Davis

Thanks!

Waterfowl sampling Sites: 4 live bird markets (Chittagong, Netrokona, Rajshahi and Dinajpur) 20 waterfowls sample per market per month (total 80 sample/month) (single visit/month) Cloacal swab/tracheal/fecal specimens Collected demographic, management and health data of sampled waterfowl

Commercial chicken sampling Sites: 24 live bird markets - 16 from Dhaka city - 8 from Chittagong, Rajshahi, Netrokona, Dinajpur, Gazipur and Kishoreganj Total 145 commercial chickens/month Cloacal/tracheal swabs Demographic, management & health data

Backyard chicken sampling Sites: 5 live bird markets Chittagong, Netrokona, Faridpur, Bogra & Jessore Total 50 backyard chicken/month Cloacal/tracheal samples Demographic, management and health data Community surveillance 5 Community data collectors visit 200 households Collect backyard poultry health data Investigated unusual poultry mortality 29 Environmental pool samples from 29 LBMs