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
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.
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).
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.
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
Lum J, Wang R, Lassiter K, Srinivasan B, Abi-Ghanem D,Berghman L, Hargis B, Tung S, Lu H, Li Y. 2012. Rapiddetection of avian influenza H5N1 virus using impedancemeasurement of immuno-reaction coupled with RBCamplification. Biosensors & Bioelectronics, 38, 67-73
Magalhaes R J S, Ortiz-Pelaez A, Kim L L T, Quoc H D, Otte J,Pfeiffer D U. 2010. Associations between attributes of livepoultry trade and HPAI H5N1 outbreaks: a descriptive andnetwork analysis study in northern Vietnam. BMC VeterinaryResearch, 6. doi: 10.1186/1746-6148-6-10Marin M J, Rashid A, Rejzek M, Fairhurst S A, Wharton S A,Martin S R, McCauley J W, Wileman T, Field R A, RussellD A. 2013. Glyconanoparticles for the plasmonic detectionand discrimination between human and avian influenzavirus. Organic & Biomolecular Chemistry, 11, 7101-7107
McLeod A, Kobayashi M, Gilman J, Siagian A, Young M. 2009.The use of poultry value chain mapping in developing HPAIcontrol programmes. Worlds Poultry Science Journal, 65,217-223
Mendoza L G, McQuary P, Mongan A, Gangadharan R,Brignac S, Eggers M. 1999. High-throughput microarraybasedenzyme-linked immunosorbent assay (ELISA).Biotechniques, 27, 778-780, 782–786, 788
MOA (Ministry of Agriculture of the People’s Republic of China).2013. Circular of the Ministry of Agriculture on Printing andDistributing the Emergency Surveillance Program for H7N9Avian Influenza and Guidance for Emergency Response toH7N9 Avian Influenza (Trial). Ministay of Agriculture of thePeople’s Republic of China, China. (in Chinese)
Monne I, Fusaro A, Nelson M I, Bonfanti L, Mulatti P, Hughes J,Murcia P R, Schivo A, Valastro V, Moreno A, Holmes E C,Cattolia G. 2014. Emergence of a highly pathogenic avianinfluenza virus from a low-pathogenic progenitor. Journalof Virology, 88, 4375-4388
NCC (The National Chicken Council, USA). 2012. Verticalintegration. [2014-09-01]. http://www.nationalchickencouncil. org/industry-issues/vertical-integration/
Newton D W, Treanor J J, Menegus M A. 2000. Clinical andlaboratory diagnosis of influenza virus infections. AmericanJournal of Managed Care, 6, S265-S275.
OIE (World Organisation for Animal Health/Office Internationaldes Epizooties). 2000. Highly pathogenic avian influenza.In: Manual of Standards for Diagnostic Tests and Vaccines.Office International des Epizooties, Paris, France.
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.
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
Lum J, Wang R, Lassiter K, Srinivasan B, Abi-Ghanem D,Berghman L, Hargis B, Tung S, Lu H, Li Y. 2012. Rapiddetection of avian influenza H5N1 virus using impedancemeasurement of immuno-reaction coupled with RBCamplification. Biosensors & Bioelectronics, 38, 67-73
Magalhaes R J S, Ortiz-Pelaez A, Kim L L T, Quoc H D, Otte J,Pfeiffer D U. 2010. Associations between attributes of livepoultry trade and HPAI H5N1 outbreaks: a descriptive andnetwork analysis study in northern Vietnam. BMC VeterinaryResearch, 6. doi: 10.1186/1746-6148-6-10Marin M J, Rashid A, Rejzek M, Fairhurst S A, Wharton S A,Martin S R, McCauley J W, Wileman T, Field R A, RussellD A. 2013. Glyconanoparticles for the plasmonic detectionand discrimination between human and avian influenzavirus. Organic & Biomolecular Chemistry, 11, 7101-7107
McLeod A, Kobayashi M, Gilman J, Siagian A, Young M. 2009.The use of poultry value chain mapping in developing HPAIcontrol programmes. Worlds Poultry Science Journal, 65,217-223
Mendoza L G, McQuary P, Mongan A, Gangadharan R,Brignac S, Eggers M. 1999. High-throughput microarraybasedenzyme-linked immunosorbent assay (ELISA).Biotechniques, 27, 778-780, 782–786, 788
MOA (Ministry of Agriculture of the People’s Republic of China).2013. Circular of the Ministry of Agriculture on Printing andDistributing the Emergency Surveillance Program for H7N9Avian Influenza and Guidance for Emergency Response toH7N9 Avian Influenza (Trial). Ministay of Agriculture of thePeople’s Republic of China, China. (in Chinese)
Monne I, Fusaro A, Nelson M I, Bonfanti L, Mulatti P, Hughes J,Murcia P R, Schivo A, Valastro V, Moreno A, Holmes E C,Cattolia G. 2014. Emergence of a highly pathogenic avianinfluenza virus from a low-pathogenic progenitor. Journalof Virology, 88, 4375-4388
NCC (The National Chicken Council, USA). 2012. Verticalintegration. [2014-09-01]. http://www.nationalchickencouncil. org/industry-issues/vertical-integration/
Newton D W, Treanor J J, Menegus M A. 2000. Clinical andlaboratory diagnosis of influenza virus infections. AmericanJournal of Managed Care, 6, S265-S275.
OIE (World Organisation for Animal Health/Office Internationaldes Epizooties). 2000. Highly pathogenic avian influenza.In: Manual of Standards for Diagnostic Tests and Vaccines.Office International des Epizooties, Paris, France.
OIE (World Organisation for Animal Health/Office Internationaldes Epizooties). 2001. International Animal Health Code.Office International des Epizooties, Paris, France.
Pantin-Jackwood M J, Miller P J, Spackman E, Swayne D E,Susta L, Costa-Hurtado M, Suarez D L. 2014. Role of poultryin the spread of novel H7N9 influenza virus in China. Journalof Virology, 88, 5381-5390
Papenburg J, Baz M, Hamelin M E, Rheaume C, CarbonneauJ, Ouakki M, Rouleau I, De Serres G, Boivin G. 2011.Evaluation of serological diagnostic methods for the 2009pandemic influenza A (H1N1) virus. Clinical and VaccineImmunology, 18, 520-522
Plague F, Aviaire G. 2010. High Pathogenicity Avian Influenza.The Center for Food Security and Public Health, Iowa, USA.Prince H E, Leber A L. 2003. Comparison of complementfixation and hemagglutination inhibition assays for detectingantibody responses following influenza virus vaccination.Clinical and Diagnostic Laboratory Immunology, 10,481-482
Qi X P, Jiang D, Wang H L, Zhuang D F, Ma J Q, Fu J Y, Qu JD, Sun Y, Yu S C, Meng Y J, Huang Y H, Xia L F, Li Y Y,Wang Y, Wang G H, Xu K, Zhang Q, Wan M, Su X M, FuG, et al. 2014. Calculating the burden of disease of avianoriginH7N9 infections in China. BMJ Open, 4. doi: 10.1136/bmjopen-2013-004189
Rebel J M J, Peeters B, Fijten H, Post J, Cornelissen J,Vervelde L. 2011. Highly pathogenic or low pathogenic avianinfluenza virus subtype H7N1 infection in chicken lungs:Small differences in general acute responses. VeterinaryResearch, 42, 10.
Rosenqvist E, Tjade T, Froholm L O, Frasch C E. 1983. AnELISA study of the antibody response after vaccinationwith a combined meningococcal group B polysaccharideand serotype 2 outer membrane protein vaccine. NIPHAnnals, 6, 139-149
Rowe T, Abernathy R A, Hu-Primmer J, Thompson W W, Lu XH, Lim W, Fukuda K, Cox N J, Katz J M. 1999. Detectionof antibody to avian influenza A (H5N1) virus in humanserum by using a combination of serologic assays. Journalof Clinical Microbiology, 37, 937-943
Sakhatskiy M I, Abdullaieva E. 2014. Broiler meat productionin the world. TEXHA Production Association. [2014-11-10].http://texha.com/en/press-center/articles/broiler-meatproduction-in-the-world.html
Sanchez-Vizcaino F, Perez A, Lainez M, Sanchez-Vizcaino JM. 2010. A quantitative assessment of the risk for highlypathogenic avian influenza introduction into spain via legaltrade of live poultry. Risk Analysis, 30, 798-807
Shin J, Cherstvy A G, Metzler R. 2014. Sensing viruses bymechanical tension of DNA in responsive hydrogels.Physical Review X, 4, doi: 10.1103/PhysRevX.4.021002
Sonaiya E B. 2007. Family poultry, food security and the impactof HPAI. Worlds Poultry Science Journal, 63, 132-138
Spackman E, Senne D A, Myers T J, Bulaga L L, Garber LP, Perdue M L, Lohman K, Daum L T, Suarez D L. 2002.Development of a real-time reverse transcriptase PCRassay for type A influenza virus and the avian H5 and H7hemagglutinin subtypes. Journal of Clinical Microbiology,40, 3256-3260
Suarez D L, Das A, Ellis E. 2007. Review of rapid moleculardiagnostic tools for avian influenza virus. Avian Diseases,51, 201-208
Swayne D E, DA S, Suarez D L. 2008. Avian influenza. In:Dufour-Zavala L ed., A Laboratory Mannual for the Isolation,Identification, and Characterization of Avian Pathogens.American Association of Avian Pathologists, GA, USA.
Takahashi T, Kawakami T, Mizuno T, Minami A, Uchida Y, SaitoT, Matsui S, Ogata M, Usui T, Sriwilaijaroen N, HiramatsuH, Suzuki Y, Suzuki T. 2013. Sensitive and direct detectionof receptor binding specificity of highly pathogenic avianinfluenza a virus in clinical samples. PLOS ONE, 8. doi:10.1371/journal.pone.0078125
Tesh M J, McCammon J R. 1979. Detection of arbovirusantibodies in avian sera by the complement fixationinhibitiontest. American Journal of Veterinary Research,40, 299-301
Van Thuan N, Nimse S B, Song K S, Kim J, Van Thao T, SungH W, Kim T. 2012. HPAI 9G DNAChip: Discriminationof highly pathogenic influenza virus genes. ChemicalCommunications, 48, 4582-4584
To K K W, Tsang A K L, Chan J F W, Cheng V C C, Chen H,Yuen K Y. 2014. Emergence in China of human disease dueto avian influenza A (H10N8)-Cause for concern? Journalof Infection, 68, 205-215
Tong S X, Li Y, Rivailler P, Conrardy C, Castillo D A A, Chen LM, Recuenco S, Ellison J A, Davis C T, York I A, TurmelleA S, Moran D, Rogers S, Shi M, Tao Y, Weil M R, TangK, Rowe L A, Sammons S, Xu X Y, et al. 2012. A distinctlineage of influenza A virus from bats. Proceedings of theNational Academy of Sciences of the United States ofAmerica, 109, 4269-4274
Tong S X, Zhu X Y, Li Y, Shi M, Zhang J, Bourgeois M, YangH, Chen X F, Recuenco S, Gomez J, Chen L M, JohnsonA, Tao Y, Dreyfus C, Yu W L, McBride R, Carney P J,Gilbert A T, Chang J, Guo Z, et al. 2013. New world batsharbor diverse influenza A viruses. PLOS Pathogens, 9.doi: 10.1371/journal.ppat.1003657
Uyeki T M, Cox N J. 2013. Global concerns regarding novelinfluenza A (H7N9) virus infections. New England Journalof Medicine, 368, 1862-1864
Wang J, Tai W, Angione S L, John A R, Opal S M, ArtensteinA W, Tripathia A. 2013. Subtyping Clinical specimens ofinfluenza a virus by use of a simple method to amplify RNAtargets. Journal of Clinical Microbiology, 51, 3324-3330
Wang R, Li Y. 2013. Hydrogel based QCM aptasensorfor detection of avian influenza virus. Biosensors &Bioelectronics, 42, 148-155
Wang R, Lin J, Lassiter K, Srinivasan B, Lin L, Lu H, Tung S,Hargis B, Bottje W, Berghman L, Li Y. 2011. Evaluationstudy of a portable impedance biosensor for detection ofavian influenza virus. Journal of Virological Methods, 178,52-58
Wang R, Zhao J, Jiang T, Kwon Y M, Lu H, Jiao P, Liao M, LiY. 2013. Selection and characterization of DNA aptamersfor use in detection of avian influenza virus H5N1. Journalof Virological Methods, 189, 362-369
Wong C K S, Zhu H, Li O T W, Leung Y H C, Chan M C W, GuanY, Peiris J S M, Poon L L M. 2013. Molecular detection ofhuman H7N9 influenza A virus causing outbreaks in China.Clinical Chemistry, 59, 1062-1067
Woolcock P R. 2008. Avian influenza virus isolation andpropagation in chicken eggs. Methods in Molecular Biology,436, 35-46
Xie Z, Huang J, Luo S, Xie Z, Xie L, Liu J, Pang Y, Deng X, FanQ. 2014. Ultrasensitive electrochemical immunoassay foravian influenza subtype H5 using nanocomposite. PLOSONE, 9. doi: 10.1371/journal.pone.0094685
Ye W W, Tsang M K, Liu X, Yang M, Hao J. 2014. Upconversionluminescence resonance energy transfer (LRET)-basedbiosensor for rapid and ultrasensitive detection of avianinfluenza virus H7 subtype. Small, 10, 2390-2397
Yu H J, Wu J T, Cowling B J, Liao Q H, Fang V J, Zhou S, WuP, Zhou H, Lau E H Y, Guo D H, Ni M Y, Peng Z B, FengL Z, Jiang H, Luo H M, Li Q, Feng Z J, Wang Y, Yang W Z,Leung G M. 2014. Effect of closure of live poultry marketson poultry-to-person transmission of avian influenza A H7N9virus: An ecological study. Lancet, 383, 541-548
Zhang J, Feng Y, Hu D, Lv H, Zhu J, Cao M, Zheng F, ZhuJ, Gong X, Hao L, Srinivas S, Ren H, Qi Z, Li B, Wang C.2013. Rapid and sensitive detection of H7N9 avian influenzavirus by use of reverse transcription-loop-mediatedisothermal amplification. Journal of Clinical Microbiology,51, 3760-3764
Zhang R Q, Liu S L, Zhao W, Zhang W P, Yu X, Li Y, Li A J, PangD W, Zhang Z L. 2013. A simple point-of-care microfluidicimmunomagnetic fluorescence assay for pathogens.Analytical Chemistry, 85, 2645-2651
Zhang T, Bi Y, Tian H, Li X, Liu D, Wu Y, Jin T, Wang Y, ChenQ, Chen Z, Chang J, Gao G F, Xu B. 2014. Human infectionwith influenza virus A (H10N8) from live poultry markets,China, 2014. Emerg Infectious Diseases, 20. doi: 10.3201/eid2012.140911
Zhang W D, Evans D H. 1991. Detection and identification ofhuman influenza-viruses by the polymerase chain-reaction.Journal of Virological Methods, 33, 165-189
Zhao J, Tang S, Storhoff J, Marla S, Bao Y P, Wang X, Wong EY, Ragupathy V, Ye Z, Hewlett I K. 2010. Multiplexed, rapiddetection of H5N1 using a PCR-free nanoparticle-basedgenomic microarray assay. BMC Biotechnology, 10. doi:10.1186/1472-6750-10-74Zhao J, Wang X, Ragupathy V, Zhang P, Tang W, Ye Z,Eichelberger M, Hewlett I. 2012. Rapid detection anddifferentiation of swine-origin influenza A virus (H1N1/2009)from other seasonal influenza A viruses. Viruses-Basel, 4,3012-3019
Zhao W, Zhang W P, Zhang Z L, He R L, Lin Y, Xie M, Wang H Z,Pang D W. 2012. Robust and highly sensitive fluorescenceapproach for point-of-care virus detection based onimmunomagnetic separation. Analytical Chemistry, 84,2358-2365
Zhou C H, Long Y M, Qi B P, Pang D W, Zhang Z L. 2013.A magnetic bead-based bienzymatic electrochemicalimmunosensor for determination of H9N2 avian influenzavirus. Electrochemistry Communications, 31, 129-132
Zhou C H, Shu Y, Hong Z Y, Pang D W, Zhang Z L. 2013.Electrochemical magnetoimmunosensing approach for thesensitive detection of H9N2 avian influenza virus particles.Chemistry (An Asian Journal), 8, 2220-2226
Zhou C H, Zhao J Y, Pang D W, Zhang Z L. 2014. Enzymeinducedmetallization as a signal amplification strategy forhighly sensitive colorimetric detection of avian influenzavirus particles. Analytical Chemistry, 86, 2752-2759
Zhu Z, Fan H, Qi X, Qi Y, Shi Z, Wang H, Cui L, Zhou M. 2013.Development and evaluation of a SYBR green-based realtime RT-PCR assay for detection of the emerging avianinfluenza A (H7N9) virus. PLOS ONE, 8. doi: 10.1371/journal.pone.0080028
Zhuang Q Y, Wang S C, Wu M L, Liu S, Jiang W M, Hou GY, Li J P, Wang K C, Yu J M, Chen J M, Chen J W. 2013.Epidemiological and risk analysis of the H7N9 subtypeinfluenza outbreak in China at its early stage. ChineseScience Bulletin, 58, 3183-3187
Zou X, Huang H, Gao Y, Su X. 2012. Detection of avianinfluenza virus based on magnetic silica nanoparticlesresonance light scattering system. Analyst, 137, 648-653