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Journal of Integrative Agriculture  2015, Vol. 14 Issue (11): 2296-2308    DOI: 10.1016/S2095-3119(15)61122-4
Section 2: Detection methods and technologies Advanced Online Publication | Current Issue | Archive | Adv Search |
Methods to detect avian influenza virus for food safety surveillance
 SHI Ping, Shu Geng, LI Ting-ting, LI Yu-shui, FENG Ting, WU Hua-nan
1 School of Environment and Energy, Peking University Shenzhen Graduate School, Shenzhen 518055, P.R.China
2 Sino-US Joint Food Safety Research Center, Northwest A&F University, Yangling 712100, P.R.China
3 Department of Plant Science, University of California, Davis, CA 95616, USA
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摘要  Avian influenza (AI), caused by the influenza A virus, has been a global concern for public health. AI outbreaks not only impact the poultry production, but also give rise to a risk in food safety caused by viral contamination of poultry products in the food supply chain. Distinctions in AI outbreak between strains H5N1 and H7N9 indicate that early detection of the AI virus in poultry is crucial for the effective warning and control of AI to ensure food safety. Therefore, the establishment of a poultry surveillance system for food safety by early detection is urgent and critical. In this article, methods to detect AI virus, including current methods recommended by the World Health Organization (WHO) and the World Organisation for Animal Health (Office International des Epizooties, OIE) and novel techniques not commonly used or commercialized are reviewed and evaluated for feasibility of use in the poultry surveillance system. Conventional methods usually applied for the purpose of AI diagnosis face some practical challenges to establishing a comprehensive poultry surveillance program in the poultry supply chain. Diverse development of new technologies can meet the specific requirements of AI virus detection in various stages or scenarios throughout the poultry supply chain where onsite, rapid and ultrasensitive methods are emphasized. Systematic approaches or integrated methods ought to be employed according to the application scenarios at every stage of the poultry supply chain to prevent AI outbreaks.

Abstract  Avian influenza (AI), caused by the influenza A virus, has been a global concern for public health. AI outbreaks not only impact the poultry production, but also give rise to a risk in food safety caused by viral contamination of poultry products in the food supply chain. Distinctions in AI outbreak between strains H5N1 and H7N9 indicate that early detection of the AI virus in poultry is crucial for the effective warning and control of AI to ensure food safety. Therefore, the establishment of a poultry surveillance system for food safety by early detection is urgent and critical. In this article, methods to detect AI virus, including current methods recommended by the World Health Organization (WHO) and the World Organisation for Animal Health (Office International des Epizooties, OIE) and novel techniques not commonly used or commercialized are reviewed and evaluated for feasibility of use in the poultry surveillance system. Conventional methods usually applied for the purpose of AI diagnosis face some practical challenges to establishing a comprehensive poultry surveillance program in the poultry supply chain. Diverse development of new technologies can meet the specific requirements of AI virus detection in various stages or scenarios throughout the poultry supply chain where onsite, rapid and ultrasensitive methods are emphasized. Systematic approaches or integrated methods ought to be employed according to the application scenarios at every stage of the poultry supply chain to prevent AI outbreaks.
Keywords:  avian influenza       food safety       detection methods       poultry supply chain       surveillance system  
Received: 26 December 2014   Accepted:
Fund: 

This research is supported by the National Natural Science Foundation of China (21405008), the Shenzhen Municipal Government Subsidies for Postdoctoral Research, the Special Fund for Sino-US Joint Research Center for Food Safety in Northwest A&F University, China (A200021501) and the Start-up Funds for Talents in Northwest A&F University, China (Z111021403).

Corresponding Authors:  WU Hua-nan,Tel: +86-755-26032670, Fax: +86-755-26035332,E-mail: wuhn@pkusz.edu.cn     E-mail:  wuhn@pkusz.edu.cn
About author:  SHI Ping, E-mail: shiping@pkusz.edu.cn; Shu Geng,E-mail: gengxu@pkusz.edu.cn;* These authors contributed equally to this study.

Cite this article: 

SHI Ping, Shu Geng, LI Ting-ting, LI Yu-shui, FENG Ting, WU Hua-nan. 2015. Methods to detect avian influenza virus for food safety surveillance. Journal of Integrative Agriculture, 14(11): 2296-2308.

Abdelwhab E M, Selim A A, Arafa A, Galal S, Kilany W H,Hassan M K, Aly M M, Hafez M H. 2010. Circulation ofavian influenza H5N1 in live bird markets in Egypt. AvianDiseases, 54, 911-914

Van Borm S, Steensels M, Ferreira H L, Boschmans M, DeVriese J, Larnbrecht B, van den Berg T. 2007. A universalavian endogenous real-time reverse transcriptasepolymerasechain reaction control and its applicationto avian influenza diagnosis and quantification. AvianDiseases, 51, 213-220

 Brown J D, Luttrell M P, Berghaus R D, Kistler W, Keeler S P,Howey A, Wilcox B, Hall J, Niles L, Dey A, Knutsen G, FritzK, Stallknecht D E. 2010. Prevalence of antibodies to typea influenza virus in wild avian species using two serologicassays. Journal of Wildlife Diseases, 46, 896-911

Butt K M, Smith G J D, Chen H L, Zhang L J, Leung Y H C, XuK M, Lim W, Webster R G, Yuen K Y, Peiris J S M, GuanY. 2005. Human infection with an avian H9N2 influenza Avirus in Hong Kong in 2003. Journal of Clinical Microbiology,43, 5760-5767

Cattoli G, Capua I. 2006. Molecular diagnosis of avian influenzaduring an outbreak. Developments in Biologicals, 124,99-105

Cattoli G, Drago A, Maniero S, Toffan A, Bertoli E, FassinaS, Terregino C, Robbi C, Vicenzoni G, Capua I. 2004.Comparison of three rapid detection systems for type Ainfluenza virus on tracheal swabs of experimentally andnaturally infected birds. Avian Pathology, 33, 432-437

Chen Y, Liang W, Yang S, Wu N, Gao H, Sheng J, Yao H, WoJ, Fang Q, Cui D, Li Y, Yao X, Zhang Y, Wu H, Zheng S,Diao H, Xia S, Zhang Y, Chan K H, Tsoi H W, et al. 2013.Human infections with the emerging avian influenza AH7N9 virus from wet market poultry: Clinical analysis andcharacterisation of viral genome. Lancet, 381, 1916-1925

Chmielewski R, Swayne D E. 2011. Avian influenza: Publichealth and food safety concerns. Annual Review of FoodScience and Technology, 2, 37-57

Conly J M, Johnston B L. 2004. Avian influenza - The nextpandemic? Canadian Journal of Infectious DiseasesMedical Microbiology, 15, 252-254

Costales A, Gerber P, Steinfeld H. 2006. Underneath thelivestock revolution. In: Mcleod A, ed., Livestock Report2006. Animal Production and Health Divison of FAO, Rome.Cox N J. 1999. Prevention and control of influenza. Lancet,354, 30-30

Das A, Spackman E, Senne D, Pedersen J, Suarez D L.2006. Development of an internal positive control for rapiddiagnosis of avian influenza virus infections by real-timereverse transcription-PCR with lyophilized reagents. Journalof Clinical Microbiology, 44, 3065-3077

Ding X X, Hu D M, Chen Y, Di B A, Jin J, Pan Y X, Qiu L W, WangY D, Wen K, Wang M, Che X Y. 2011. Full serotype- andgroup-specific NS1 capture enzyme-linked immunosorbentassay for rapid differential diagnosis of dengue virusinfection. Clinical and Vaccine Immunology, 18, 430-434

El Zowalaty M E, Abin M, Raju S, Chander Y, Redig P T, AbdEl Latif H K, El Sayed M A, Goyal S M. 2011. Isolationof avian influenza virus from polymerase chain reactionnegativecloacal samples of waterfowl. Journal of VeterinaryDiagnostic Investigation, 23, 87-90

El Zowalaty M E, Bustin S A, Husseiny M I, Ashour H M. 2013.Avian influenza: virology, diagnosis and surveillance. FutureMicrobiology, 8, 1209-1227

Elci C. 2006. The impact of HPAI of the H5N1 strain oneconomies of affected countries. In: Esen A, Ogus A, eds.,Proceedings of the Conference on Human and EconomicResources. Papers of the Annual Cortland Conference inEconomics. Izmir University of Economics, Turkey.

Fu Y, Callaway Z, Lum J, Wang R, Lin J, Li Y. 2014. Exploitingenzyme catalysis in ultra-low ion strength media forimpedance biosensing of avian influenza virus using abare interdigitated electrode. Analytical Chemistry, 86,1965-1971

Gao G F. 2014. Influenza and the live poultry trade. Science,344, 235-235

Gao R B, Cao B, Hu Y W, Feng Z J, Wang D Y, Hu W F, ChenJ, Jie Z J, Qiu H B, Xu K, Xu X W, Lu H Z, Zhu W F, GaoZ C, Xiang N J, Shen Y Z, He Z B, Gu Y, Zhang Z Y, YangY, et al. 2013. Human infection with a novel avian-origininfluenza a (H7N9) virus. New England Journal of Medicine,368, 1888-1897

Ge Y Y, Cui L B, Qi X, Shan J, Shan Y F, Qi Y H, Wu B, WangH, Shi Z Y. 2010. Detection of novel swine origin influenzaA virus (H1N1) by real-time nucleic acid sequence-basedamplification. Journal of Virological Methods, 163, 495-497

Ge Y, Wu B, Qi X, Zhao K, Guo X, Zhu Y, Qi Y, Shi Z, ZhouM, Wang H, Cui L. 2013. Rapid and sensitive detectionof novel avian-origin influenza a (H7N9) virus by reversetranscription loop-mediated isothermal amplificationcombined with a lateral-flow device. PLOS ONE, 8. doi:10.1371/journal.pone.0069941

Grabowska I, Stachyra A, Gora-Sochacka A, Sirko A,Olejniczak A B, Lesnikowski Z J, Radecki J, Radecka H.2014. DNA probe modified with 3-iron bis(dicarbollide) forelectrochemical determination of DNA sequence of AvianInfluenza Virus H5N1. Biosensors & Bioelectronics, 51,170-176

Guo D, Zhuo M, Zhang X, Xu C, Jiang J, Gao F, Wan Q, LiQ, Wang T. 2013. Indium-tin-oxide thin film transistorbiosensors for label-free detection of avian influenza virusH5N1. Analytica Chimica Acta, 773, 83-88

Harder T C, Werner O. 2006. Chapter two: Avian influenza. In:Kamps B S, Hofmann C, Preiser W, eds., Influenza Report2006. Flying Publisher, Paris. pp. 48-86

He Y, Liu P H, Tang S Z, Chen Y, Pei E L, Zhao B H, Ren H,Li J, Zhu Y Y, Zhao H J, Pan Q C, Gu B K, Yuan Z G, WuF. 2014. Live poultry market closure and control of avianinfluenza A (H7N9), Shanghai, China. Emerging InfectiousDiseases, 20, 1565-1566

Hideshima S, Hinou H, Ebihara D, Sato R, Kuroiwa S, NakanishiT, Nishimura S I, Osaka T. 2013. Attomolar detectionof influenza a virus hemagglutinin human H1 and avianH5 using glycan-blotted field effect transistor biosensor.Analytical Chemistry, 85, 5641-5644

Higgins D A. 1998. Comparative immunology of avian species.In: Davison T F, Morris T R, Payne L N, eds., PoultyImmunology. Carfax Publishing Company, Abingdon, UK.

Hou S T T. 2013. Food safety: H7N9 risks and prevention.City Weekend. 2013-05-06. [2014-06-07]. http://www.cityweekend.com.cn/beijing/blog/food-safety-h7n9-risksand-prevention/

Huang H L, Dan H B, Zhou Y J, Yu Z J, Fan H Y, Tong T Z, Jin M L, Chen H C. 2007. Different neutralization efficiency ofneutralizing monoclonal antibodies against avian influenzaH5N1 virus to virus strains from different hosts. MolecularImmunology, 44, 1052-1055

Imai M, Ninomiya A, Minekawa H, Notomi T, Ishizaki T,Tashiro M, Odagiri T. 2006. Development of H5-RT-LAMP(loop-mediated isothermal amplification) system for rapiddiagnosis of H5 avian influenza virus infection. Vaccine,24, 6679-6682

Jin M L, Wang G H, Zhang R H, Zhao S T, Li H C, Tan Y D, ChenH C. 2004. Development of enzyme-linked immunosorbentassay with nucleoprotein as antigen for detection ofantibodies to avian influenza virus. Avian Diseases, 48,870-878

Julkunen I, Pyhälä R, Hovi T. 1985. Enzyme immunoassay,complement fixation and hemagglutination inhibition tests inthe diagnosis of influenza A and B virus infections. Purifiedhemagglutinin in subtype-specific diagnosis. Journal ofVirological Methods, 10, 75-84

Kashyap A K, Steel J, Oner A F, Dillon M A, Swale R E, Wall KM, Perry K J, Faynboym A, Illhan M, Horowitz M, HorowitzL, Palese P, Bhatt R R, Lerner R A. 2008. Combinatorialantibody libraries from survivors of the Turkish H5N1 avianinfluenza outbreak reveal virus neutralization strategies.Proceedings of the National Academy of Sciences of theUnited States of America, 105, 5986-5991

Kaverin N V, Rudneva I A, Smirnov Y A, Finskaya N N.1988. Human-avian influenza-virus reassortants: effect ofreassortment pattern on multi-cycle reproduction in MDCKcells. Archives of Virology, 103, 117-126

Kim J Y, Choi K, Moon D I, Ahn J H, Park T J, Lee S Y, Choi YK. 2013. Surface engineering for enhancement of sensitivityin an underlap-FET biosensor by control of wettability.Biosensors & Bioelectronics, 41, 867-870

Lai W A, Lin C H, Yang Y S, Lu M S C. 2012. Ultrasensitiveand label-free detection of pathogenic avian influenzaDNA by using CMOS impedimetric sensors. Biosensors &Bioelectronics, 35, 456-460

Lau L T, Banks J, Aherne R, Brown I H, Dillon N, Collins R A,Chan K Y, Fung Y W W, Xing J, Yu A C H. 2004. Nucleicacid sequence-based amplification methods to detect avianinfluenza virus. Biochemical and Biophysical ResearchCommunications, 313, 336-342

Lee M S, Chang P C, Shien J H, Cheng M C, Shieh H K. 2001.Identification and subtyping of avian influenza viruses byreverse transcription-PCR. Journal of Virological Methods,97, 13-22

Li D J, Wang J P, Wang R H, Li Y B, Abi-Ghanem D, BerghmanL, Hargis B, Lu H G. 2011. A nanobeads amplified QCMimmunosensor for the detection of avian influenza virusH5N1. Biosensors & Bioelectronics, 26, 4146-4154

Li J, Zou M, Chen Y, Xue Q, Zhang F, Li B, Wang Y, Qi X, YangY. 2013. Gold immunochromatographic strips for enhanceddetection of avian influenza and Newcastle disease viruses.Analytica Chimica Acta, 782, 54-58

Li Y, Bostick D L, Sullivan C B, Myers J L, Griesemer SB, Stgeorge K, Plotkin J B, Hensley S E. 2013. Singlehemagglutinin mutations that alter both antigenicity andreceptor binding avidity influence influenza virus antigenicclustering. Journal of Virology, 87, 9904-9910

Li Y, Hong M, Qiu B, Lin Z, Cai Z, Chenb Y, Chen G. 2013. Ahighly sensitive chemiluminescent metalloimmunoassayfor H1N1 influenza virus detection based on a silvernanoparticle label. Chemical Communications, 49,10563-10565

Li Y, Hong M, Qiu B, Lin Z, Chen Y, Cai Z, Chen G. 2014.Highly sensitive fluorescent immunosensor for detectionof influenza virus based on Ag autocatalysis. Biosensors& Bioelectronics, 54, 358-364

Liu D, Gao G F. 2014. The new emerging H7N9 influenza virusindicates poultry as new mixing vessels. Science China (LifeSciences), 57, 731-732

Liu J, Liu H, Kang H, Donovan M, Zhu Z, Tan W. 2012. Aptamerincorporatedhydrogels for visual detection, controlleddrug release, and targeted cancer therapy. Analytical andBioanalytical Chemistry, 402, 187-194

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Van Borm S, Steensels M, Ferreira H L, Boschmans M, DeVriese J, Larnbrecht B, van den Berg T. 2007. A universalavian endogenous real-time reverse transcriptasepolymerasechain reaction control and its applicationto avian influenza diagnosis and quantification. AvianDiseases, 51, 213-220

 Brown J D, Luttrell M P, Berghaus R D, Kistler W, Keeler S P,Howey A, Wilcox B, Hall J, Niles L, Dey A, Knutsen G, FritzK, Stallknecht D E. 2010. Prevalence of antibodies to typea influenza virus in wild avian species using two serologicassays. Journal of Wildlife Diseases, 46, 896-911

Butt K M, Smith G J D, Chen H L, Zhang L J, Leung Y H C, XuK M, Lim W, Webster R G, Yuen K Y, Peiris J S M, GuanY. 2005. Human infection with an avian H9N2 influenza Avirus in Hong Kong in 2003. Journal of Clinical Microbiology,43, 5760-5767

Cattoli G, Capua I. 2006. Molecular diagnosis of avian influenzaduring an outbreak. Developments in Biologicals, 124,99-105

Cattoli G, Drago A, Maniero S, Toffan A, Bertoli E, FassinaS, Terregino C, Robbi C, Vicenzoni G, Capua I. 2004.Comparison of three rapid detection systems for type Ainfluenza virus on tracheal swabs of experimentally andnaturally infected birds. Avian Pathology, 33, 432-437

Chen Y, Liang W, Yang S, Wu N, Gao H, Sheng J, Yao H, WoJ, Fang Q, Cui D, Li Y, Yao X, Zhang Y, Wu H, Zheng S,Diao H, Xia S, Zhang Y, Chan K H, Tsoi H W, et al. 2013.Human infections with the emerging avian influenza AH7N9 virus from wet market poultry: Clinical analysis andcharacterisation of viral genome. Lancet, 381, 1916-1925

Chmielewski R, Swayne D E. 2011. Avian influenza: Publichealth and food safety concerns. Annual Review of FoodScience and Technology, 2, 37-57

Conly J M, Johnston B L. 2004. Avian influenza - The nextpandemic? Canadian Journal of Infectious DiseasesMedical Microbiology, 15, 252-254

Costales A, Gerber P, Steinfeld H. 2006. Underneath thelivestock revolution. In: Mcleod A, ed., Livestock Report2006. Animal Production and Health Divison of FAO, Rome.Cox N J. 1999. Prevention and control of influenza. Lancet,354, 30-30

Das A, Spackman E, Senne D, Pedersen J, Suarez D L.2006. Development of an internal positive control for rapiddiagnosis of avian influenza virus infections by real-timereverse transcription-PCR with lyophilized reagents. Journalof Clinical Microbiology, 44, 3065-3077

Ding X X, Hu D M, Chen Y, Di B A, Jin J, Pan Y X, Qiu L W, WangY D, Wen K, Wang M, Che X Y. 2011. Full serotype- andgroup-specific NS1 capture enzyme-linked immunosorbentassay for rapid differential diagnosis of dengue virusinfection. Clinical and Vaccine Immunology, 18, 430-434

El Zowalaty M E, Abin M, Raju S, Chander Y, Redig P T, AbdEl Latif H K, El Sayed M A, Goyal S M. 2011. Isolationof avian influenza virus from polymerase chain reactionnegativecloacal samples of waterfowl. Journal of VeterinaryDiagnostic Investigation, 23, 87-90

El Zowalaty M E, Bustin S A, Husseiny M I, Ashour H M. 2013.Avian influenza: virology, diagnosis and surveillance. FutureMicrobiology, 8, 1209-1227

Elci C. 2006. The impact of HPAI of the H5N1 strain oneconomies of affected countries. In: Esen A, Ogus A, eds.,Proceedings of the Conference on Human and EconomicResources. Papers of the Annual Cortland Conference inEconomics. Izmir University of Economics, Turkey.

Fu Y, Callaway Z, Lum J, Wang R, Lin J, Li Y. 2014. Exploitingenzyme catalysis in ultra-low ion strength media forimpedance biosensing of avian influenza virus using abare interdigitated electrode. Analytical Chemistry, 86,1965-1971

Gao G F. 2014. Influenza and the live poultry trade. Science,344, 235-235

Gao R B, Cao B, Hu Y W, Feng Z J, Wang D Y, Hu W F, ChenJ, Jie Z J, Qiu H B, Xu K, Xu X W, Lu H Z, Zhu W F, GaoZ C, Xiang N J, Shen Y Z, He Z B, Gu Y, Zhang Z Y, YangY, et al. 2013. Human infection with a novel avian-origininfluenza a (H7N9) virus. New England Journal of Medicine,368, 1888-1897

Ge Y Y, Cui L B, Qi X, Shan J, Shan Y F, Qi Y H, Wu B, WangH, Shi Z Y. 2010. Detection of novel swine origin influenzaA virus (H1N1) by real-time nucleic acid sequence-basedamplification. Journal of Virological Methods, 163, 495-497

Ge Y, Wu B, Qi X, Zhao K, Guo X, Zhu Y, Qi Y, Shi Z, ZhouM, Wang H, Cui L. 2013. Rapid and sensitive detectionof novel avian-origin influenza a (H7N9) virus by reversetranscription loop-mediated isothermal amplificationcombined with a lateral-flow device. PLOS ONE, 8. doi:10.1371/journal.pone.0069941

Grabowska I, Stachyra A, Gora-Sochacka A, Sirko A,Olejniczak A B, Lesnikowski Z J, Radecki J, Radecka H.2014. DNA probe modified with 3-iron bis(dicarbollide) forelectrochemical determination of DNA sequence of AvianInfluenza Virus H5N1. Biosensors & Bioelectronics, 51,170-176

Guo D, Zhuo M, Zhang X, Xu C, Jiang J, Gao F, Wan Q, LiQ, Wang T. 2013. Indium-tin-oxide thin film transistorbiosensors for label-free detection of avian influenza virusH5N1. Analytica Chimica Acta, 773, 83-88

Harder T C, Werner O. 2006. Chapter two: Avian influenza. In:Kamps B S, Hofmann C, Preiser W, eds., Influenza Report2006. Flying Publisher, Paris. pp. 48-86

He Y, Liu P H, Tang S Z, Chen Y, Pei E L, Zhao B H, Ren H,Li J, Zhu Y Y, Zhao H J, Pan Q C, Gu B K, Yuan Z G, WuF. 2014. Live poultry market closure and control of avianinfluenza A (H7N9), Shanghai, China. Emerging InfectiousDiseases, 20, 1565-1566

Hideshima S, Hinou H, Ebihara D, Sato R, Kuroiwa S, NakanishiT, Nishimura S I, Osaka T. 2013. Attomolar detectionof influenza a virus hemagglutinin human H1 and avianH5 using glycan-blotted field effect transistor biosensor.Analytical Chemistry, 85, 5641-5644

Higgins D A. 1998. Comparative immunology of avian species.In: Davison T F, Morris T R, Payne L N, eds., PoultyImmunology. Carfax Publishing Company, Abingdon, UK.

Hou S T T. 2013. Food safety: H7N9 risks and prevention.City Weekend. 2013-05-06. [2014-06-07]. http://www.cityweekend.com.cn/beijing/blog/food-safety-h7n9-risksand-prevention/

Huang H L, Dan H B, Zhou Y J, Yu Z J, Fan H Y, Tong T Z, Jin M L, Chen H C. 2007. Different neutralization efficiency ofneutralizing monoclonal antibodies against avian influenzaH5N1 virus to virus strains from different hosts. MolecularImmunology, 44, 1052-1055

Imai M, Ninomiya A, Minekawa H, Notomi T, Ishizaki T,Tashiro M, Odagiri T. 2006. Development of H5-RT-LAMP(loop-mediated isothermal amplification) system for rapiddiagnosis of H5 avian influenza virus infection. Vaccine,24, 6679-6682

Jin M L, Wang G H, Zhang R H, Zhao S T, Li H C, Tan Y D, ChenH C. 2004. Development of enzyme-linked immunosorbentassay with nucleoprotein as antigen for detection ofantibodies to avian influenza virus. Avian Diseases, 48,870-878

Julkunen I, Pyhälä R, Hovi T. 1985. Enzyme immunoassay,complement fixation and hemagglutination inhibition tests inthe diagnosis of influenza A and B virus infections. Purifiedhemagglutinin in subtype-specific diagnosis. Journal ofVirological Methods, 10, 75-84

Kashyap A K, Steel J, Oner A F, Dillon M A, Swale R E, Wall KM, Perry K J, Faynboym A, Illhan M, Horowitz M, HorowitzL, Palese P, Bhatt R R, Lerner R A. 2008. Combinatorialantibody libraries from survivors of the Turkish H5N1 avianinfluenza outbreak reveal virus neutralization strategies.Proceedings of the National Academy of Sciences of theUnited States of America, 105, 5986-5991

Kaverin N V, Rudneva I A, Smirnov Y A, Finskaya N N.1988. Human-avian influenza-virus reassortants: effect ofreassortment pattern on multi-cycle reproduction in MDCKcells. Archives of Virology, 103, 117-126

Kim J Y, Choi K, Moon D I, Ahn J H, Park T J, Lee S Y, Choi YK. 2013. Surface engineering for enhancement of sensitivityin an underlap-FET biosensor by control of wettability.Biosensors & Bioelectronics, 41, 867-870

Lai W A, Lin C H, Yang Y S, Lu M S C. 2012. Ultrasensitiveand label-free detection of pathogenic avian influenzaDNA by using CMOS impedimetric sensors. Biosensors &Bioelectronics, 35, 456-460

Lau L T, Banks J, Aherne R, Brown I H, Dillon N, Collins R A,Chan K Y, Fung Y W W, Xing J, Yu A C H. 2004. Nucleicacid sequence-based amplification methods to detect avianinfluenza virus. Biochemical and Biophysical ResearchCommunications, 313, 336-342

Lee M S, Chang P C, Shien J H, Cheng M C, Shieh H K. 2001.Identification and subtyping of avian influenza viruses byreverse transcription-PCR. Journal of Virological Methods,97, 13-22

Li D J, Wang J P, Wang R H, Li Y B, Abi-Ghanem D, BerghmanL, Hargis B, Lu H G. 2011. A nanobeads amplified QCMimmunosensor for the detection of avian influenza virusH5N1. Biosensors & Bioelectronics, 26, 4146-4154

Li J, Zou M, Chen Y, Xue Q, Zhang F, Li B, Wang Y, Qi X, YangY. 2013. Gold immunochromatographic strips for enhanceddetection of avian influenza and Newcastle disease viruses.Analytica Chimica Acta, 782, 54-58

Li Y, Bostick D L, Sullivan C B, Myers J L, Griesemer SB, Stgeorge K, Plotkin J B, Hensley S E. 2013. Singlehemagglutinin mutations that alter both antigenicity andreceptor binding avidity influence influenza virus antigenicclustering. Journal of Virology, 87, 9904-9910

Li Y, Hong M, Qiu B, Lin Z, Cai Z, Chenb Y, Chen G. 2013. Ahighly sensitive chemiluminescent metalloimmunoassayfor H1N1 influenza virus detection based on a silvernanoparticle label. Chemical Communications, 49,10563-10565

Li Y, Hong M, Qiu B, Lin Z, Chen Y, Cai Z, Chen G. 2014.Highly sensitive fluorescent immunosensor for detectionof influenza virus based on Ag autocatalysis. Biosensors& Bioelectronics, 54, 358-364

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