Controlling highly pathogenic avian influenza, Bangladesh.
Article Type: Letter to the editor
Authors: Mondal, Shankar P.
Tardif-Douglin, David
Ryan-Silva, Robert
Magnani, Rich
Pub Date: 12/01/2012
Publication: Name: Emerging Infectious Diseases Publisher: U.S. National Center for Infectious Diseases Audience: Academic; Professional Format: Magazine/Journal Subject: Health Copyright: COPYRIGHT 2012 U.S. National Center for Infectious Diseases ISSN: 1080-6040
Issue: Date: Dec, 2012 Source Volume: 18 Source Issue: 12
Accession Number: 313345671
Full Text: To the Editor: Highly pathogenic avian influenza (HPAI) A(H5N1) virus is a deadly zoonotic pathogen. Since 2003, HPAI infections have been reported in millions of poultry and wild birds from 63 countries (1) and in 598 humans, among whom there have been 352 reported deaths in 15 countries (2). HPAI (H5N1) virus is endemic in Bangladesh, and the first outbreak occurred in March 2007. Since then, the virus has spread to 49 of 64 districts in Bangladesh, and samples from 536 farms have tested positive for the virus. Bangladesh now ranks among countries worldwide with the highest reported number of HPAI outbreaks (1). Intermittent outbreaks in Bangladesh and clusters of disease across the border in northeastern India are dramatic reminders that the emergence of new, mutant viruses in developing countries could lead to a pandemic among humans. Six cases of nonfatal HPAI (H5N1) infection have been reported in Bangladesh (2). Live bird markets that are in poor physical condition and that lack or have poor biosecurity are probable sources of HPAI transmission to humans and for bird-to-bird transmission (3-5).

In 2008, a global project of the United States Agency for International Development, Stamping Out Pandemic and Avian Influenza (STOP AI), was initiated in Bangladesh. The project began with biosecurity training for veterinarians and livestock science graduates on some large-scale commercial farms. The local STOP AI office was established in Dhaka, the capital of Bangladesh, in February 2009, and the organization managed the project through its completion in September 2010 (online Technical Appendix Figure 1, wwwnc.cdc. gov/EID/pdfs/12-0635-Techapp.pdf). STOP AI initially organized 7 highly successful live bird market biosecurity training programs in 5 geographic divisions of Bangladesh; later, STOP AI piloted cleaning and disinfection activities in 2 live bird markets, Mohammadpur and Kaptan Bazaar, in Dhaka by working closely with the United Nations' Food and Agriculture Organization. The Food and Agriculture Organization subsequently conducted cleaning and disinfection activities in 24 other markets within Dhaka and other districts in Bangladesh.

We focused on understanding the inter-relationships among household poultry producers, commercial farmers, suppliers, transporters, processors, and consumers that facilitate the process of producing and moving poultry, i.e., the entire poultry value chain (PVC). We describe how improved biosecurity on poultry farms and hygienic standards in live bird markets can reduce HPAI outbreaks. In resource-limited countries, like Bangladesh, these improvements can be made through training, technical support, financial assistance for infrastructure renovations, and incentivedriven trust-building between service providers and key PVC stakeholders. To determine whether interventions would reduce the number of HPAI infections, we implemented changes during 2009-2010 in 2 districts in Bangladesh, Gazipur and Dinajpur, that had a high number of cases (online Technical Appendix Figure 2).

Using field-tested questionnaires, we conducted a baseline survey during in-person interviews with 1,372 poultry stakeholders (Table). Stakeholder workshops were held in each district to share survey findings and design biosecurity improvement programs. STOP AI implemented biosecurity training for 1,319 people in 53 subsector-specific 1-day sessions in Gazipur and Dinajpur (online Technical Appendix Table). We created biosecurity improvement models (e.g., farm boundary, footbath) in 12 commercial farms in Gazipur and selected 2 live bird markets in each dis trict for infrastructure improvements, including biogas and compost plants, that were needed for the cleaning and disinfection activities (online Technical Appendix Figure 3). We provided technical support and [less than or equal to] 25% ($750) of the cost for each farm and [less than or equal to] 50% ($10,000) for each market on a costsharing basis.

After completion of all interventions, we conducted a final survey of 514 poultry stakeholders, including 70% of the original trainees from both districts (Table). We analyzed pre- and post-intervention survey data by using GraphPad Software (www.graphpad.com/quickcalcs/index.cfm). The results indicated that awareness of the proper disposal of birds that were culled or died because of HPAI had increased in both districts (p<0.0001); awareness of human HPAI cases rose substantially (p<0.0001); an understanding of how HPAI is spread (e.g., through sick or wild birds) changed (p<0.001); use of personal protective equipment (masks, gloves) and other precautionary measures (washing hands) increased (p<0.0001); awareness of protecting birds from HPAI (e.g., separately housing chickens and ducks) increased (p<0.05); and a preference for purchasing slaughtered birds instead of live birds at the markets increased (p<0.0001).

Substantially fewer HPAI outbreaks were reported and no clusters of infection were found during our intervention, 2009-2010 (online Technical Appendix Figure 1), probably indicating that control measures were effective. The challenge now is to sustain the progress that has been made. Several months after completion of the STOP AI interventions, their effect on the incidence of disease in Bangladesh was limited. However, STOP AI could not be expected in the short term to dramatically reduce the high incidence of HPAI in Bangladesh. We have progressively and dramatically increased the scope and benefits of our pilot PVC implementation program, but additional work is needed. To help spread PVC approaches throughout the country, community leaders, imams of local mosques, and school teachers can be trained to implement awareness programs on safe practices for raising poultry and regular cleaning and disinfection of live bird markets. The strengthening of biosecurity measures will help control the spread of HPAI virus and other zoonotic diseases.

Acknowledgments

We acknowledge Zakaria Noyon and Suman Das-Gupta for providing technical assistance in implementation of the project. We thank Paritosh K. Biswas for assisting with data analysis and for reviewing the manuscript.

This project was funded by the United States Agency for International Development.

Shankar P. Mondal, David Tardif-Douglin, Robert Ryan-Silva, and Rich Magnani

Author affiliations: Development Alternatives Inc., Bethesda, Maryland, USA (S.P. Mondal, D. Tardif-Douglin, R. Ryan-Silva, R. Magnani); and University of Minnesota, St. Paul, Minnesota, USA (S.P. Mondal)

DOI: 10.3201/eid1812.120635

References

(1.) World Health Organization for Animal Health. Update on highly pathogenic avian influenza in animals (type H5 and H7) [cited 2012 Mar 19]. http://www.oie. int/animal-health-in-the-world/update-onavian-influenza/2012/

(2.) World Health Organization. Cumulative number of confirmed human cases of avian influenza A(H5N1) reported to WHO [cited 2012 Mar 19]. http://www.who. int/influenza/human_animal_interface/ H5N1_cumulative_table_archives/en/ index.html

(3.) Biswas PK, Christensen JP, Ahmed SS, Barua H, Das A, Rahman MH. at al. Avian influenza outbreaks in chickens, Bangladesh. Emerg Infect Dis. 2008;14:1909-12. http://dx.doi.org/10.3201/eid1412.071567

(4.) Biswas PK, Christensen JP, Ahmed SS, Das A, Rahman MH, Barua H, et al. Risk for infection with highly pathogenic avian influenza virus (H5N1) in backyard chickens, Bangladesh. Emerg Infect Dis. 2009;15:1931-6. http://dx.doi. org/10.3201/eid1512.090643

(5.) Biswas PK, Rahman MH, Das A, Ahmed SS, Giasuddin M, Christensen JP. Risk for highly pathogenic avian influenza H5N1 virus infection in chickens in small-scale commercial farms, in a highrisk area, Bangladesh, 2008. Transbound Emerg Dis. 2011;58:519-25. http://dx.doi. org/10.1111/j.1865-1682.2011.01235.x

Address for correspondence: Shankar P. Mondal, Department of Veterinary and Biomedical Sciences, College of Veterinary Medicine, University of Minnesota, St. Paul, MN 55108, USA; email: shankarpm@yahoo.com
Table. Analysis of pre- and postintervention survey data for
biosecurity practices for HPAI (H5N1) virus in Gazipur and
Dinajpur districts, Bangladesh, 2009-10 *

                                             No. persons
                                           surveyed (% aware
                                           of practice; 95% CI)

                                              Gazipur

                                           Baseline survey,
Biosecurity practice                       n = 821
Awareness of bird deaths                   191 (23; 21-26)
caused by HPAI
Awareness of bird culling                  163 (20; 17-23)
resulting from HPAI
Awareness of HPAI cases among humans       138 (17; 14-20)
Understand how HPAI is spread
  Do not know how HPAI is spread           209 (25; 23-29)
  Perceive that wild birds are the cause   466 (57; 53-60)
  Recognize sick poultry as a vector       43 (5; 4-7)
Awareness of how to protect people
  Wear masks                               190 (23; 20-26)
  Wear gloves                              122 (15; 13-17)
  Wash hands                               207(25; 23-29)
  Kids should not handle birds             3 (0; 0.1-1)
  No need to protect                       243 (30; 27-33)
Awareness of how to protect birds
  Separate chickens and ducks              28 (3; 3-4)
  Clean and disinfect poultry cages        288 (35; 32-38)
  Restrict entry to farms                  226 (28; 25-31)
  Vaccinate against Newcastle disease      12 (1; 0.8-2)
  Properly dispose of feces                158 (19; 17-22)
  Wear proper clothing                     38 (5; 3-6)
  Clean and disinfect transport vehicles   35 (4; 3-6)
  Keep dogs and cats away from farms       92 (11; 9-14)
  Do not know                              170 (21; 18-24)
Bird purchase preference
  Dead bird (slaughtered at market)        152 (19; 16-21)
  Live bird (slaughtered at home)          652 (79; 77-82)

                                            No. persons
                                           surveyed (% aware
                                            of practice; 95% CI)

                                               Gazipur

                                           Final survey,
Biosecurity practice                       n = 300 ([dagger])
Awareness of bird deaths                   219 (73; 68-78)
caused by HPAI
Awareness of bird culling                  186 (62; 56-67)
resulting from HPAI
Awareness of HPAI cases among humans       172 (57; 52-63)
Understand how HPAI is spread
  Do not know how HPAI is spread           42 (14; 11-18)
  Perceive that wild birds are the cause   207 (69; 64-74)
                                           ([double dagger])

  Recognize sick poultry as a vector       140 (47; 41-52)
Awareness of how to protect people
  Wear masks                               204 (68; 63-73)
  Wear gloves                              136 (45; 40-50)
  Wash hands                               166(55; 50-60)
  Kids should not handle birds             203 (68; 62-73)
  No need to protect                       0 (0)
Awareness of how to protect birds
  Separate chickens and ducks              92 (31; 26-36)
  Clean and disinfect poultry cages        182 (61; 55-66)
  Restrict entry to farms                  131(44; 38-49)
  Vaccinate against Newcastle disease      67 (22; 18-27)
  Properly dispose of feces                79 (26; 22-32) ([section])
  Wear proper clothing                     67 (22; 18-27)
  Clean and disinfect transport vehicles   105 (35; 30-40)
  Keep dogs and cats away from farms       99 (33; 28-39)
  Do not know                              46 (15; 12-20) ([paragraph])
Bird purchase preference
  Dead bird (slaughtered at market)        136 (45; 40-51)
  Live bird (slaughtered at home)          167 (56; 50-61)

                                           No. persons surveyed
                                          (% aware of practice; 95% CI)

                                              Dinajpur

                                           Baseline survey,
Biosecurity practice                       n = 525
Awareness of bird deaths                   116 (22; 19-26)
caused by HPAI
Awareness of bird culling                  56 (11; 8-14)
resulting from HPAI
Awareness of HPAI cases among humans       21 (4; 3-6)
Understand how HPAI is spread
  Do not know how HPAI is spread           286 (54; 50-59)
  Perceive that wild birds are the cause   134 (26; 22-29)
  Recognize sick poultry as a vector       53 (10; 8-13)
Awareness of how to protect people
  Wear masks                               44 (8; 6-11)
  Wear gloves                              54 (10; 8-13)
  Wash hands                               58 (11; 9-14)
  Kids should not handle birds             1 (0; 0.01-1)
  No need to protect                       294 (56; 52-60)
Awareness of how to protect birds
  Separate chickens and ducks              18 (3; 2-5)
  Clean and disinfect poultry cages        39 (7; 5-10)
  Restrict entry to farms                  56 (11; 8-14)
  Vaccinate against Newcastle disease      7 (1; 0.6-3)
  Properly dispose of feces                16 (3; 2-5)
  Wear proper clothing                     29 (6; 4-9)
  Clean and disinfect transport vehicles   10 (2; 1-4)
  Keep dogs and cats away from farms       22 (4; 3-6)
  Do not know                              267 (51; 47-55)
Bird purchase preference
  Dead bird (slaughtered at market)        50 (10; 7-12)
  Live bird (slaughtered at home)          484 (92; 90-94)

                                           No. persons surveyed (%
                                           aware of practice; 95% CI)

                                              Dinajpur

                                           Final survey,
Biosecurity practice                       n = 209 ([dagger])
Awareness of bird deaths                   88 (42; 36-49)
caused by HPAI
Awareness of bird culling                  47 (22; 17-29)
resulting from HPAI
Awareness of HPAI cases among humans       113 (54; 47-61)
Understand how HPAI is spread
  Do not know how HPAI is spread           21 (10; 7-15)
  Perceive that wild birds are the cause   154 (74; 67-80)
  Recognize sick poultry as a vector       61 (29; 23-36)
Awareness of how to protect people
  Wear masks                               94 (45; 38-52)
  Wear gloves                              75 (36; 30-43)
  Wash hands                               139 (67; 60-73)
  Kids should not handle birds             54 (26; 20-32)
  No need to protect                       4 (2; 0.6-5)
Awareness of how to protect birds
  Separate chickens and ducks              36 (17; 13-23)
  Clean and disinfect poultry cages        99 (47; 41-54)
  Restrict entry to farms                  56 (27; 21-33)
  Vaccinate against Newcastle disease      47 (22; 17-29)
  Properly dispose of feces                117 (56; 49-63)
  Wear proper clothing                     43 (21; 16-27)
  Clean and disinfect transport vehicles   20 (10; 6-14)
  Keep dogs and cats away from farms       33 (16; 11-21)
  Do not know                              2 (1; 0.04-4)
Bird purchase preference
  Dead bird (slaughtered at market)        70 (33; 27-40)
  Live bird (slaughtered at home)          136 (65; 58-71)

* HPAI, highly pathogenic avian influenza.

([dagger]) Two-sided x test of significance compared with baseline data
had p value of <0.0001, except as noted.

([double dagger]) p = 0.0002.

([section]) p = 0.013.

([paragraph]) p = 0.049.
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