Developing Policies for Avian Flu in Bangladesh

4046 words (16 pages) Essay

23rd Mar 2018 Health Reference this

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Introduction:

Highly pathogenic H5N1 was first reported in 2007 and since then the disease has devastated effect on poultry industry of Bangladesh. Since its introduction into Bangladesh, the H5N1 has evolved continuously. H5N1-H9N2 co-infection and reassortment event in H5N1 has been documented in Bangladesh. All those provide evidence of emergence of novel viruses, due to reassortment, in Bangladesh. For example H7N9 has been reported as a reassortant strain which have pandemic potential i.e deadly for human life (1).

Objectives of the project:

  • To develop policies for both low and high pathogenic avian influenza viruses present or at risk of entering Bangladesh,
  • The economic analysis for the high pathogenic strains assume that their economic effects are similar to those of H5N1.

In this review I emphasized on the population at risk and occurrence and distribution of HPAI and LPAI in Bangladesh.

Population at risk:

H5N1 has been reported in chicken, duck, pigeon, goose, quail, turkeys, pet birds (2-10) and wild bird (2, 11) such as lesser whistling ducks (4) and crow (5, 10). H5N1 has also been documented in the poultry samples of live bird market (LBM) (12), commercial farms (FAO classified the farming system: three (3)) (13) and local chicken (14). In LBM, chicken, ducks and quail were the three species of LBM from H5N1 has been isolated most (4). AI virus has been reported also from environmental samples (4-6). In human (15), H5N1 has been documented in children (16, 17) workers of poultry market (18-20) and poultry farm (19).

H7N9 has been reported in chicken, quail, goose, duck and pigeon (8).

H9N2 was reported in chicken (Parent stock (layer) (21)), duck, goose, pigeon and quail (8). A study reported that H9N2 was more prevalent in chickens while H5N1 was reported dominantly in ducks and goose in compare to chicken (8).

Occurrence and distribution

Geographic distribution in your country:

HPAI H5N1 and LPAI H9N2 is an endemic poultry disease in Bangladesh and has been occurred throughout the country (2, 4, 20, 22). Those two HPAI and LPAI two have been circulated together at poultry market since 2008 (4). LPAI H9N2 has been circulated persistently in bird markets (4) while H5N1 have sporadic infection among LBM workers in Bangladesh (20). The disease has been distributed in retail market such as live poultry market, pet bird market, commercial farms (4, 6, 12, 13, 20) and wetland of Bangladesh such as Baikka Beel Hakaluki hoar, Tanguar Haors of Sylhet division and Jahangirnagar university lake of Dhaka division (11, 23).

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In Bangladesh, clade 2.3.2.1 was in reported from crow and bird market (4, 5) whereas clades 2.2.2 was reported in bird markets (4). Clade 2.2 reported in northwest–southeast direction whereas clade 2.3.2.1 reported mainly in north–south direction of central Bangladesh(24). Jamalpur district (Sarishari upazilla) reported as the HPAI outbreak epicentre for indigenous poultry in Bangladesh (25). H5N1 has followed Northwest–Southeast oblique line during phase I outbreak. The disease has reported nearly from all over the country with an exception in south region in phase II outbreak. In phase III outbreak, the disease has been extended to new areas from where there was no HPAI has been reported in earlier two phases (11).

Fig.: Distribution H5N1 HPAI between 2007 and 2012 (1)

Geographic distribution in other countries where epidemiology of the disease is likely to be similar:

Khan et al. (2014) found close similarities in avian influenza virus clade 2.3.2.1 of Bangladesh, India, Nepal and Myanmar and proposed a common AI antecedent in the area (5). Three clades such as clades 1, 2.3.4 and 2.3.2.1 has been linked with human outbreak in Vietnam (18) and there was a changes in clade circulation over the time in Vietnam and also in China (26).

In other countries, H5N1 has been reported commonly from Red River Delta area and sporadically from highland areas of Vietnam(27). H5N1 has been reported in live bird market workers of Vietnam (18) and Hong Kong (20). H5N1 has also been reported in lower-Northern of Thailand (27). In India, the AI occurred mostly in backyard chicken of West Bengal (97%) and Assam (94%) states, while in Tripura state the AI reported only in 37% of backyard chicken (28).

Prevalence in your country:

Overall 0.87%-22.05% samples were positive for Avian influenza virus (AIV) Type A in Bangladesh (2, 3, 6, 8, 14, 23). AIV has been documented in migratory bird (3.93%), LBM chicken (7.06%), duck (1.68%-39.76%) (2, 3, 8, 23), pigeon (5.26%) (2), quail (8.5%)(3) and goose (9.09%) (8) of Bangladesh. Among chickens, AIV has been reported in broiler (12%-12.5%), layer (15%-62.5%) and local (0%-25%) chicken (8, 29). One study documented higher AI prevalence in hens (10.83%) in compare to cocks (8.65%) (14). AI was more prevalent in >34 weeks bird (12.80%) than 8-16 weeks birds (14). Avian influenza Type A virus was detected with Antigen test kit and reported, prevalence was high in Dhaka district and Gazipur district while lowest was reported in Mymensingh (0.0%) (29).

H5N1 antibodies has been documented at low level in wild birds (0.09%) of wetlands such as Tanguar Haor and Hakaluki Haor (23). A study reported 5% H5N1 seroprevalence in live bird market (LBM) worker (20) while another study documented no farm workers and bird market worker in positive for H5N1 in Bangladesh even though they had history of regular contact with sick and moribund poultry (19). About 2% seroconversion per year has been documented in poultry worker of Bangladesh (20).

Khatun et al. (2013) documented the AIV type A winter season sero-prevalence during December 2009-February 2012 period and documented highest rate in December 2009-February 2010 (43.8 9%) which followed by December 2010-February 2011 (38.50% ) and December 2011-February 2012 (34.8 3%). The seasonal prevalence of AIV type A from Dec’2009-Feb’2010 (26 .89%), Dec’2010-Feb’2011 (18.50%) and December 2011-February 2012 (18.33%) respectively (page 3). The overall sero-prevalence of AIV type A in three successive winter seasons was recorded as 39.76% (23). In Feni district, overall 0%-25% AIV type A seroprevalence has been documented at union level (14).

Co-infection (H5N1-H9N2) in poultry has been reported in Bangladesh (4, 6). For example, a study isolated 975 H9N2 and 66 H5N1 from a total of 19897 samples (4) while another study isolated H5N1 (92), H9N2 (734) and 62 other strain such as from 17,438 samples in Bangladesh (23). Of 22 avian influenza sample, a study identified 8 sample positive for H5N1, 4 samples positive for H7N9 and 10 samples positive for H9N2) positive samples (8). H10N7, H1N2, H1N3, H4N2, H3N6 and H3N8 has also been detected in duck population of Bangladesh (4, 23). Avian influenza virus Type A co-infected with new castle virus (9.90 %) has also been documented in Bangladesh (23).

Prevalence in other countries where epidemiology of the disease is likely to be similar:

Nasreen et al. (2013) H5N1 seroprevalence in bird market worker of Bangladesh study findings had similarities with Nigera, Indonesia and Vietnam study findings where no farm workers and bird market worker were found positive for H5N1 (19).

AI was more prevalent in >34 weeks poultry (12.80%) than 8-16 weeks poultry in Bangladesh (14). Similar pattern has been documented in duck of Nepal for example duck >1 year older was 2 times more seropositive to AI virus than duck <6 months. In Nepal, 27.2% [95% CI: 24.6–29.5] of ducks were positive for AIV. At individual duck level, the true prevalence and apparent prevalence were 27.2% and 26.1% while at farm level the true prevalence and apparent prevalence were 41.9% and 51.6%. AIV seroprevalence has been estimated for different duck farm: small (19.8%), medium (29.9%) and large (37.5%). Male duck (19.8%) was more seropositive than female duck (32,3%) (7).

Incidence:

In Bangladesh, Nasreen et al. (2015) estimated that “the H5N1 incidence: 7 cases per 100 bird worker–years and annual incidence 50 cases per 721 enlisted poultry workers” (20). Biswas et al. (2011) estimated the higher mortality rate in backyard chickens (0.0703/day) followed by broiler (0.0341/day), breeder (0.0215/day), layer (0.0179/day) and suggested that higher mortality in backyard chicken due to scavenging feeding and co-infection with other disease. In addition Biswas et al. (2011) stated that the findings did not provide evidence to the people faith that local chickens are less prone to H5N1 infection than hybrids chicken (30).

Reference

1.Islam MR. Global and local challenges in the control of avian influenza. 9th International Poultry Show & Seminar; Dhaka, Bangladesh: World Poultry Science Association-Bangladesh Branch; 2015. p. 5-14.

2.Rahman MH, Giasuddin M, Islam MR, Hasan M, Mahmud MS, Hoque MA, et al. Bio-molecular Diagnosis of Avian Influenza Virus from Different Species of Birds in Bangladesh. Immunology and Infectious Diseases. 2015 2015;3(1):7-10.

3.Shanmuganatham K, Feeroz MM, Jones-Engel L, Walker D, Alam S, Hasan M, et al. Genesis of avian influenza H9N2 in Bangladesh. Emerging Microbes & Infections. 2014 2014;3(12).

4.Marinova-Petkova A, Feeroz MM, Alam SMR, Hasan MK, Akhtar S, Jones-Engel L, et al. Multiple introductions of highly pathogenic avian influenza H5N1 viruses into Bangladesh. Emerging Microbes & Infections. 2014 2014;3(2).

5.Khan SU, Berman L, Haider N, Gerloff N, Rahman MZ, Shu B, et al. Investigating a crow die-off in January–February 2011 during the introduction of a new clade of highly pathogenic avian influenza virus H5N1 into Bangladesh. Archives of virology. 2014 2014;159(3):509-18.

6.Shanmuganatham K, Feeroz MM, Jones-Engel L, Smith GJD, Fourment M, Walker D, et al. Antigenic and molecular characterization of avian influenza A (H9N2) viruses, Bangladesh. Emerging infectious diseases. 2013 2013;19(9).

7.Karki S, Lupiani B, Budke CM, Manandhar S, Ivanek R. Cross-sectional Serosurvey of Avian Influenza Antibodies Presence in Domestic Ducks of Kathmandu, Nepal. Zoonoses and public health. 2014 2014;61(6):442-8.

8.Haque ME. Detection and differentiation of avian influenza and newcastle disease viruses from healthy farm birds in bangladesh by conventional and molecular techniques. Mymensingh, Bangladesh: Bangladesh Agricultural University; 2014.

9.Khaleda S, Murayama Y. Geographic Concentration and Development Potential of Poultry Microenterprises and Value Chain: A Study Based on Suitable Sites in Gazipur, Bangladesh. Social Sciences. 2013 2013;2(3):147-67.

10.Islam MR, Haque ME, Giasuddin M, Chowdhury EH, Samad MA, Parvin R, et al. New introduction of clade 2.3. 2.1 avian influenza virus (H5N1) into Bangladesh. Transboundary and emerging diseases. 2012 2012;59(5):460-3.

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11.Parvin R, Kamal AHM, Haque ME, Chowdhury EH, Giasuddin M, Islam MR, et al. Genetic characterization of highly pathogenic H5N1 avian influenza virus from live migratory birds in Bangladesh. Virus genes. 2014 2014;49(3):438-48.

12.Monne I, Yamage M, Dauphin G, Claes F, Ahmed G, Giasuddin M, et al. Reassortant avian influenza A (H5N1) viruses with H9N2-PB1 gene in poultry, Bangladesh. Emerging infectious diseases. 2013 2013;19(10).

13.Biswas PK, Rahman MH, Das A, Ahmed SSU, Giasuddin M, Christensen JP. Risk for Highly Pathogenic Avian Influenza H5N1 Virus Infection in Chickens in Small-Scale Commercial Farms, in a High-Risk Area, Bangladesh, 2008. Transboundary and emerging diseases. 2011 2011;58(6):519-25.

14.Nooruddin GM, Hossain MT, Mohammad M, Rahman MM. Sero-epidemiology of avian influenza virus in native chicken in Bangladesh. Int J Poult Sci. 2006 2006;5:1029-33.

15.Kerkhove MD. Brief literature review for the WHO global influenza research agenda–highly pathogenic avian influenza H5N1 risk in humans. Influenza and other respiratory viruses. 2013 2013;7(s2):26-33.

16.icddr b. First confirmed human infection with avian influenza A (H5N1) virus in Bangladesh. Health and Science Bulletin. 2008;6:1-6.

17.Brooks WA, Alamgir ASM, Sultana R, Islam MS, Rahman M, Fry AM, et al. Avian influenza virus A (H5N1), detected through routine surveillance, in child, Bangladesh. Emerging infectious diseases. 2009 2009;15(8).

18.Dung TC, Dinh PN, Nam VS, Tan LM, Hang NLK, Thanh LT, et al. Seroprevalence survey of avian influenza A (H5N1) among live poultry market workers in northern Viet Nam, 2011. Western Pacific surveillance and response journal: WPSAR. 2014 2014;5(4).

19.Nasreen S, Khan SU, Azziz-Baumgartner E, Hancock K, Veguilla V, Wang D, et al. Seroprevalence of antibodies against highly pathogenic avian influenza A (H5N1) virus among poultry workers in Bangladesh, 2009. PloS one. 2013 2013;8(9).

20.Nasreen S, Khan SU, Luby SP, Gurley ES, Abedin J, Zaman RU, et al. Highly Pathogenic Avian Influenza A (H5N1) Virus Infection among Workers at Live Bird Markets, Bangladesh, 2009–2010. Emerging Infectious Diseases. 2015;21(4):629-37.

21.Jannat N, Chowdhury EH, Parvin R, Begum JA, Giasuddin M, Khan MA, et al. Investigation of an Outbreak of Low Pathogenic Avian Influenza in Poultry in Bangladesh. International Journal of Livestock Research. 2013 2013;3(4):21-32.

22.Loth L, Gilbert M, Osmani MG, Kalam AM, Xiao X. Risk factors and clusters of highly pathogenic avian influenza H5N1 outbreaks in Bangladesh. Preventive veterinary medicine. 2010 2010;96(1):104-13.

23.Khatun A, Giasuddin M, Islam KM, Khanom S, Samad MA, Islam MR, et al. Surveillance of avian influenza virus type A in semi-scavenging ducks in Bangladesh. BMC veterinary research. 2013 2013;9(1).

24.Osmani MG, Ward MP, Giasuddin M, Islam MR, Kalam A. The spread of highly pathogenic avian influenza (subtype H5N1) clades in Bangladesh, 2010 and 2011. Preventive veterinary medicine. 2014 2014;114(1):21-7.

25.Biswas PK, Christensen JP, Ahmed SSU, Barua H, Das A, Rahman MH, et al. Avian influenza outbreaks in chickens, Bangladesh. Emerging infectious diseases. 2008 2008;14(12).

26.Haque ME, Giasuddin M, Chowdhury EH, Islam MR. Molecular evolution of H5N1 highly pathogenic avian influenza viruses in Bangladesh between 2007 and 2012. Avian Pathology. 2014 2014;43(2):183-94.

27.Paul MC, Gilbert M, Desvaux S, Andriamanivo HR, Peyre M, Khong NV, et al. Agro-environmental determinants of avian influenza circulation: A multisite study in Thailand, Vietnam and Madagascar. PloS one. 2014 2014;9(7).

28.Dhingra MS, Dissanayake R, Negi AB, Oberoi M, Castellan D, Thrusfield M, et al. Spatio-temporal epidemiology of highly pathogenic avian influenza (subtype H5N1) in poultry in eastern India. Spatial and spatio-temporal epidemiology. 2014 2014;11:45-57.

29.Rahman S, Rabbani MG, Uddin MJ, Chakrabartty A, Her M. Prevalence of Avian Influenza and Newcastle Disease Viruses Using Rapid Antigen Detection Kit in Poultry in Some Areas of Bangladesh. Acta Microbiologica. 2012 2012;3(1).

30.Biswas PK, Christensen JP, Ahmed SSU, Barua H, Das A, Rahman MH, et al. Mortality rate and clinical features of highly pathogenic avian influenza in naturally infected chickens in Bangladesh. Rev sci tech Off int Epiz. 2011 2011;30(3):871-8.

1

Introduction:

Highly pathogenic H5N1 was first reported in 2007 and since then the disease has devastated effect on poultry industry of Bangladesh. Since its introduction into Bangladesh, the H5N1 has evolved continuously. H5N1-H9N2 co-infection and reassortment event in H5N1 has been documented in Bangladesh. All those provide evidence of emergence of novel viruses, due to reassortment, in Bangladesh. For example H7N9 has been reported as a reassortant strain which have pandemic potential i.e deadly for human life (1).

Objectives of the project:

  • To develop policies for both low and high pathogenic avian influenza viruses present or at risk of entering Bangladesh,
  • The economic analysis for the high pathogenic strains assume that their economic effects are similar to those of H5N1.

In this review I emphasized on the population at risk and occurrence and distribution of HPAI and LPAI in Bangladesh.

Population at risk:

H5N1 has been reported in chicken, duck, pigeon, goose, quail, turkeys, pet birds (2-10) and wild bird (2, 11) such as lesser whistling ducks (4) and crow (5, 10). H5N1 has also been documented in the poultry samples of live bird market (LBM) (12), commercial farms (FAO classified the farming system: three (3)) (13) and local chicken (14). In LBM, chicken, ducks and quail were the three species of LBM from H5N1 has been isolated most (4). AI virus has been reported also from environmental samples (4-6). In human (15), H5N1 has been documented in children (16, 17) workers of poultry market (18-20) and poultry farm (19).

H7N9 has been reported in chicken, quail, goose, duck and pigeon (8).

H9N2 was reported in chicken (Parent stock (layer) (21)), duck, goose, pigeon and quail (8). A study reported that H9N2 was more prevalent in chickens while H5N1 was reported dominantly in ducks and goose in compare to chicken (8).

Occurrence and distribution

Geographic distribution in your country:

HPAI H5N1 and LPAI H9N2 is an endemic poultry disease in Bangladesh and has been occurred throughout the country (2, 4, 20, 22). Those two HPAI and LPAI two have been circulated together at poultry market since 2008 (4). LPAI H9N2 has been circulated persistently in bird markets (4) while H5N1 have sporadic infection among LBM workers in Bangladesh (20). The disease has been distributed in retail market such as live poultry market, pet bird market, commercial farms (4, 6, 12, 13, 20) and wetland of Bangladesh such as Baikka Beel Hakaluki hoar, Tanguar Haors of Sylhet division and Jahangirnagar university lake of Dhaka division (11, 23).

In Bangladesh, clade 2.3.2.1 was in reported from crow and bird market (4, 5) whereas clades 2.2.2 was reported in bird markets (4). Clade 2.2 reported in northwest–southeast direction whereas clade 2.3.2.1 reported mainly in north–south direction of central Bangladesh(24). Jamalpur district (Sarishari upazilla) reported as the HPAI outbreak epicentre for indigenous poultry in Bangladesh (25). H5N1 has followed Northwest–Southeast oblique line during phase I outbreak. The disease has reported nearly from all over the country with an exception in south region in phase II outbreak. In phase III outbreak, the disease has been extended to new areas from where there was no HPAI has been reported in earlier two phases (11).

Fig.: Distribution H5N1 HPAI between 2007 and 2012 (1)

Geographic distribution in other countries where epidemiology of the disease is likely to be similar:

Khan et al. (2014) found close similarities in avian influenza virus clade 2.3.2.1 of Bangladesh, India, Nepal and Myanmar and proposed a common AI antecedent in the area (5). Three clades such as clades 1, 2.3.4 and 2.3.2.1 has been linked with human outbreak in Vietnam (18) and there was a changes in clade circulation over the time in Vietnam and also in China (26).

In other countries, H5N1 has been reported commonly from Red River Delta area and sporadically from highland areas of Vietnam(27). H5N1 has been reported in live bird market workers of Vietnam (18) and Hong Kong (20). H5N1 has also been reported in lower-Northern of Thailand (27). In India, the AI occurred mostly in backyard chicken of West Bengal (97%) and Assam (94%) states, while in Tripura state the AI reported only in 37% of backyard chicken (28).

Prevalence in your country:

Overall 0.87%-22.05% samples were positive for Avian influenza virus (AIV) Type A in Bangladesh (2, 3, 6, 8, 14, 23). AIV has been documented in migratory bird (3.93%), LBM chicken (7.06%), duck (1.68%-39.76%) (2, 3, 8, 23), pigeon (5.26%) (2), quail (8.5%)(3) and goose (9.09%) (8) of Bangladesh. Among chickens, AIV has been reported in broiler (12%-12.5%), layer (15%-62.5%) and local (0%-25%) chicken (8, 29). One study documented higher AI prevalence in hens (10.83%) in compare to cocks (8.65%) (14). AI was more prevalent in >34 weeks bird (12.80%) than 8-16 weeks birds (14). Avian influenza Type A virus was detected with Antigen test kit and reported, prevalence was high in Dhaka district and Gazipur district while lowest was reported in Mymensingh (0.0%) (29).

H5N1 antibodies has been documented at low level in wild birds (0.09%) of wetlands such as Tanguar Haor and Hakaluki Haor (23). A study reported 5% H5N1 seroprevalence in live bird market (LBM) worker (20) while another study documented no farm workers and bird market worker in positive for H5N1 in Bangladesh even though they had history of regular contact with sick and moribund poultry (19). About 2% seroconversion per year has been documented in poultry worker of Bangladesh (20).

Khatun et al. (2013) documented the AIV type A winter season sero-prevalence during December 2009-February 2012 period and documented highest rate in December 2009-February 2010 (43.8 9%) which followed by December 2010-February 2011 (38.50% ) and December 2011-February 2012 (34.8 3%). The seasonal prevalence of AIV type A from Dec’2009-Feb’2010 (26 .89%), Dec’2010-Feb’2011 (18.50%) and December 2011-February 2012 (18.33%) respectively (page 3). The overall sero-prevalence of AIV type A in three successive winter seasons was recorded as 39.76% (23). In Feni district, overall 0%-25% AIV type A seroprevalence has been documented at union level (14).

Co-infection (H5N1-H9N2) in poultry has been reported in Bangladesh (4, 6). For example, a study isolated 975 H9N2 and 66 H5N1 from a total of 19897 samples (4) while another study isolated H5N1 (92), H9N2 (734) and 62 other strain such as from 17,438 samples in Bangladesh (23). Of 22 avian influenza sample, a study identified 8 sample positive for H5N1, 4 samples positive for H7N9 and 10 samples positive for H9N2) positive samples (8). H10N7, H1N2, H1N3, H4N2, H3N6 and H3N8 has also been detected in duck population of Bangladesh (4, 23). Avian influenza virus Type A co-infected with new castle virus (9.90 %) has also been documented in Bangladesh (23).

Prevalence in other countries where epidemiology of the disease is likely to be similar:

Nasreen et al. (2013) H5N1 seroprevalence in bird market worker of Bangladesh study findings had similarities with Nigera, Indonesia and Vietnam study findings where no farm workers and bird market worker were found positive for H5N1 (19).

AI was more prevalent in >34 weeks poultry (12.80%) than 8-16 weeks poultry in Bangladesh (14). Similar pattern has been documented in duck of Nepal for example duck >1 year older was 2 times more seropositive to AI virus than duck <6 months. In Nepal, 27.2% [95% CI: 24.6–29.5] of ducks were positive for AIV. At individual duck level, the true prevalence and apparent prevalence were 27.2% and 26.1% while at farm level the true prevalence and apparent prevalence were 41.9% and 51.6%. AIV seroprevalence has been estimated for different duck farm: small (19.8%), medium (29.9%) and large (37.5%). Male duck (19.8%) was more seropositive than female duck (32,3%) (7).

Incidence:

In Bangladesh, Nasreen et al. (2015) estimated that “the H5N1 incidence: 7 cases per 100 bird worker–years and annual incidence 50 cases per 721 enlisted poultry workers” (20). Biswas et al. (2011) estimated the higher mortality rate in backyard chickens (0.0703/day) followed by broiler (0.0341/day), breeder (0.0215/day), layer (0.0179/day) and suggested that higher mortality in backyard chicken due to scavenging feeding and co-infection with other disease. In addition Biswas et al. (2011) stated that the findings did not provide evidence to the people faith that local chickens are less prone to H5N1 infection than hybrids chicken (30).

Reference

1.Islam MR. Global and local challenges in the control of avian influenza. 9th International Poultry Show & Seminar; Dhaka, Bangladesh: World Poultry Science Association-Bangladesh Branch; 2015. p. 5-14.

2.Rahman MH, Giasuddin M, Islam MR, Hasan M, Mahmud MS, Hoque MA, et al. Bio-molecular Diagnosis of Avian Influenza Virus from Different Species of Birds in Bangladesh. Immunology and Infectious Diseases. 2015 2015;3(1):7-10.

3.Shanmuganatham K, Feeroz MM, Jones-Engel L, Walker D, Alam S, Hasan M, et al. Genesis of avian influenza H9N2 in Bangladesh. Emerging Microbes & Infections. 2014 2014;3(12).

4.Marinova-Petkova A, Feeroz MM, Alam SMR, Hasan MK, Akhtar S, Jones-Engel L, et al. Multiple introductions of highly pathogenic avian influenza H5N1 viruses into Bangladesh. Emerging Microbes & Infections. 2014 2014;3(2).

5.Khan SU, Berman L, Haider N, Gerloff N, Rahman MZ, Shu B, et al. Investigating a crow die-off in January–February 2011 during the introduction of a new clade of highly pathogenic avian influenza virus H5N1 into Bangladesh. Archives of virology. 2014 2014;159(3):509-18.

6.Shanmuganatham K, Feeroz MM, Jones-Engel L, Smith GJD, Fourment M, Walker D, et al. Antigenic and molecular characterization of avian influenza A (H9N2) viruses, Bangladesh. Emerging infectious diseases. 2013 2013;19(9).

7.Karki S, Lupiani B, Budke CM, Manandhar S, Ivanek R. Cross-sectional Serosurvey of Avian Influenza Antibodies Presence in Domestic Ducks of Kathmandu, Nepal. Zoonoses and public health. 2014 2014;61(6):442-8.

8.Haque ME. Detection and differentiation of avian influenza and newcastle disease viruses from healthy farm birds in bangladesh by conventional and molecular techniques. Mymensingh, Bangladesh: Bangladesh Agricultural University; 2014.

9.Khaleda S, Murayama Y. Geographic Concentration and Development Potential of Poultry Microenterprises and Value Chain: A Study Based on Suitable Sites in Gazipur, Bangladesh. Social Sciences. 2013 2013;2(3):147-67.

10.Islam MR, Haque ME, Giasuddin M, Chowdhury EH, Samad MA, Parvin R, et al. New introduction of clade 2.3. 2.1 avian influenza virus (H5N1) into Bangladesh. Transboundary and emerging diseases. 2012 2012;59(5):460-3.

11.Parvin R, Kamal AHM, Haque ME, Chowdhury EH, Giasuddin M, Islam MR, et al. Genetic characterization of highly pathogenic H5N1 avian influenza virus from live migratory birds in Bangladesh. Virus genes. 2014 2014;49(3):438-48.

12.Monne I, Yamage M, Dauphin G, Claes F, Ahmed G, Giasuddin M, et al. Reassortant avian influenza A (H5N1) viruses with H9N2-PB1 gene in poultry, Bangladesh. Emerging infectious diseases. 2013 2013;19(10).

13.Biswas PK, Rahman MH, Das A, Ahmed SSU, Giasuddin M, Christensen JP. Risk for Highly Pathogenic Avian Influenza H5N1 Virus Infection in Chickens in Small-Scale Commercial Farms, in a High-Risk Area, Bangladesh, 2008. Transboundary and emerging diseases. 2011 2011;58(6):519-25.

14.Nooruddin GM, Hossain MT, Mohammad M, Rahman MM. Sero-epidemiology of avian influenza virus in native chicken in Bangladesh. Int J Poult Sci. 2006 2006;5:1029-33.

15.Kerkhove MD. Brief literature review for the WHO global influenza research agenda–highly pathogenic avian influenza H5N1 risk in humans. Influenza and other respiratory viruses. 2013 2013;7(s2):26-33.

16.icddr b. First confirmed human infection with avian influenza A (H5N1) virus in Bangladesh. Health and Science Bulletin. 2008;6:1-6.

17.Brooks WA, Alamgir ASM, Sultana R, Islam MS, Rahman M, Fry AM, et al. Avian influenza virus A (H5N1), detected through routine surveillance, in child, Bangladesh. Emerging infectious diseases. 2009 2009;15(8).

18.Dung TC, Dinh PN, Nam VS, Tan LM, Hang NLK, Thanh LT, et al. Seroprevalence survey of avian influenza A (H5N1) among live poultry market workers in northern Viet Nam, 2011. Western Pacific surveillance and response journal: WPSAR. 2014 2014;5(4).

19.Nasreen S, Khan SU, Azziz-Baumgartner E, Hancock K, Veguilla V, Wang D, et al. Seroprevalence of antibodies against highly pathogenic avian influenza A (H5N1) virus among poultry workers in Bangladesh, 2009. PloS one. 2013 2013;8(9).

20.Nasreen S, Khan SU, Luby SP, Gurley ES, Abedin J, Zaman RU, et al. Highly Pathogenic Avian Influenza A (H5N1) Virus Infection among Workers at Live Bird Markets, Bangladesh, 2009–2010. Emerging Infectious Diseases. 2015;21(4):629-37.

21.Jannat N, Chowdhury EH, Parvin R, Begum JA, Giasuddin M, Khan MA, et al. Investigation of an Outbreak of Low Pathogenic Avian Influenza in Poultry in Bangladesh. International Journal of Livestock Research. 2013 2013;3(4):21-32.

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