Experimental transmission in guinea pigs of H9N2 avian influenza viruses from indoor air of chicken houses

Virus Research

Volumn 170, Issue 1-2, 2012, Pages 102-108

  Lv, Jing ^a,b,c,d   Wei, Baozhi ^a,b,c,d   Yang, Yan ^a,b,c,d   Yao, Meiling ^e   Cai, Yumei ^a,b,c,d   Gao, Yuwei ^f   Xia, Xianzhu ^f   Zhao, Xiaonan ^a,b,c,d   Liu, Zhihao ^a,b,c,d   Li, Xinxian ^a,b,c,d   Wang, Hao ^a,b,c,d   Yang, Huili ^g   Roesler, Uwe ^h   Miao, Zengmin ⁱ   Chai, Tongjie ^a,b,c,d  

^a SHANDONG AGRICULTURAL UNIVERSITY   (China)

^b Sino German Cooperative Research Centre for Zoonosis of Animal Origin   (China)

^c Key Laboratory of Animal Biotechnology and Disease Control and Prevention of Shandong Province   (China)

^d TSINGHUA UNIVERSITY   (China)

^e Zaozhuang Vocational College   (China)

^f Institute of Military Veterinary PLA   (China)

^g Disease Control Centre   (China)

^h FREIE UNIVERSITÄT BERLIN   (Germany)

ⁱ TAISHAN MEDICAL UNIVERSITY   (China)

Author keywords

Guinea pigs; H9N2 AIV; Transmission; Viral aerosol infective dose

Indexed keywords

AEROSOL; ANIMAL HOUSING; ARTICLE; AVIAN INFLUENZA VIRUS; CHICKEN; GUINEA PIG; INDOOR AIR POLLUTION; INFLUENZA VIRUS A H9N2; LUNG PARENCHYMA; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; VIRUS TRANSMISSION;

AIR MICROBIOLOGY; ANIMALS; CHICKENS; FEMALE; GUINEA PIGS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; INFLUENZA A VIRUS, H9N2 SUBTYPE; ORTHOMYXOVIRIDAE INFECTIONS; PHYLOGENY;

ANIMALIA; AVIAN INFLUENZA VIRUS; CAVIA; MAMMALIA;

EID: 84870474969     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2012.09.003     Document Type: Article

References (51)

1. Alford R.H., Kasel J.A., Gerone P.J., Knight V. Human influenza resulting from aerosol inhalation. Proceedings of the Society for Experimental Biology and Medicine 1966, 122:800-804.
2. Banks J., Speidel E.S., Moore E., Plowright L., Piccirillo A., Capua I., Cordioli P., Fioretti A., Alexander D.J. Changes in the haemagglutinin and the neuraminidase genes prior to the emergence of highly pathogenic H7N1 avian influenza viruses in Italy. Archives of Virology 2001, 146:963-973.
3. Bano S., Naeem K., Malik S.A. Evaluation of pathogenic potential of avian influenza virus serotype H9N2 in chickens. Avian Diseases 2003, 47:817-822.
4. Blachere F.M., Lindsley W.G., Pearce T.A., Anderson S.E., Fisher M., Khakoo R., Meade B.J., Lander O., Davis S., Thewlis R.E., Celik I., Chen B.T., Beezhold D.H. Measurement of airborne influenza virus in a hospital emergency department. Clinical Infectious Diseases 2009, 48:438-440.
5. Brachman P.S., Ehrlich R., Eichenwald H.F., Gabelli V.J., Kethley T.W., Madin S.H., Maltman J.R., Middlebrook G., Morton J.D., Silver I.H. Standard sampler for assay of airborne microorganisms. Science 1964, 144:1295.
6. Butt K.M., Smith G.J., Chen H., Zhang L.J., Leung Y.H., Xu K.M., Lim W., Webster R.G., Yuen K.Y., Peiris J.S., Guan Y. Human infection with an avian H9N2 influenza A virus in Hong Kong in 2003. Journal of Clinical Microbiology 2005, 43:5760-5767.
7. Castrucci M.R., Kawaoka Y. Biologic importance of neuraminidase stalk length in influenza A virus. Journal of Virology 1993, 67:759-764.
8. Che F.X., Chai T.J., Li J.S. Principle and Application of Aerobiology 2004, Science Press, Beijing.
9. Choi Y.K., Ozaki H., Webby R.J., Webster R.G., Peiris J.S., Poon L., Butt C., Leung Y.H., Guan Y. Continuing evolution of H9N2 influenza viruses in Southeastern China. Journal of Virology 2004, 78:8609-8614.
10. Els M.C., Air G.M., Murti K.G., Webster R.G., Laver W.G. An 18-amino acid deletion in an influenza neuraminidase. Virology 1985, 142:241-247.
11. Fabian P., McDevitt J.J., DeHaan W.H., Fung R.O., Cowling B.J., Chan K.H., Leung G.M., Milton D.K. Influenza virus in human exhaled breath: an observational study. PLoS One 2008, 3:e2691.
12. Gao Y., Zhang Y., Shinya K., Deng G., Jiang Y., Li Z., Guan Y., Tian G., Li Y., Shi J., Liu L., Zeng X., Bu Z., Xia X., Kawaoka Y., Chen H. Identification of amino acids in HA and PB2 critical for the transmission of H5N1 avian influenza viruses in a mammalian host. PLoS Pathogens 2009, 5:e1000709.
13. Guo Y., Li J., Cheng X. Discovery of men infected by avian influenza A (H9N2) virus. Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi 1999, 13:105-108.
14. Guo Y.J., Krauss S., Senne D.A., Mo I.P., Lo K.S., Xiong X.P., Norwood M., Shortridge K.F., Webster R.G., Guan Y. Characterization of the pathogenicity of members of the newly established H9N2 influenza virus lineages in Asia. Virology 2000, 267:279-288.
15. Haghighat-Jahromi M., Asasi K., Nili H., Dadras H., Shooshtari A.H. Coinfection of avian influenza virus (H9N2 subtype) with infectious bronchitis live vaccine. Archives of Virology 2008, 153:651-655.
16. Hoffmann E., Stech J., Guan Y., Webster R.G., Perez D.R. Universal primer set for the full-length amplification of all influenza A viruses. Archives of Virology 2001, 146:2275-2289.
17. Homme P.J., Easterday B.C. Avian influenza virus infections. I. Characteristics of influenza A-turkey-Wisconsin-1966 virus. Avian Diseases 1970, 14:66-74.
18. Jarnych V.S. Aerosole in der Veterinaermedizin 1976, VEB Deutscher Landwirtschaftsverlag, Berlin, pp. S74-S88.
19. Kawaoka Y., Webster R.G. Sequence requirements for cleavage activation of influenza virus hemagglutinin expressed in mammalian cells. Proceedings of the National Academy of Sciences of the United States of America 1988, 85:324-328.
20. Li C., Yu K., Tian G., Yu D., Liu L., Jing B., Ping J., Chen H. Evolution of H9N2 influenza viruses from domestic poultry in mainland China. Virology 2005, 340:70-83.
21. Liu H., Liu X., Cheng J., Peng D., Jia L., Huang Y. Phylogenetic analysis of the hemagglutinin genes of twenty-six avian influenza viruses of subtype H9N2 isolated from chickens in China during 1996-2001. Avian Diseases 2003, 47:116-127.
22. Liu S., Ji K., Chen J., Tai D., Jiang W., Hou G., Chen J., Li J., Huang B. Panorama phylogenetic diversity and distribution of type A influenza virus. PLoS One 2009, 4:e5022.
23. Lowen A.C., Mubareka S., Steel J., Palese P. Influenza virus transmission is dependent on relative humidity and temperature. PLoS Pathogens 2007, 3:1470-1476.
24. Lowen A.C., Mubareka S., Tumpey T.M., Garcia-Sastre A., Palese P. The guinea pig as a transmission model for human influenza viruses. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:9988-9992.
25. Lu J.H., Liu X.F., Shao W.X., Liu Y.L., Wei D.P., Liu H.Q. Phylogenetic analysis of eight genes of H9N2 subtype influenza virus: a mainland China strain possessing early isolates' genes that have been circulating. Virus Genes 2005, 31:163-169.
26. Lu X., Tumpey T.M., Morken T., Zaki S.R., Cox N.J., Katz J.M. A mouse model for the evaluation of pathogenesis and immunity to influenza A (H5N1) viruses isolated from humans. Journal of Virology 1999, 73:5903-5911.
27. Luo G., Chung J., Palese P. Alterations of the stalk of the influenza virus neuraminidase: deletions and insertions. Virus Research 1993, 29:321.
28. Lv J., Wei B., Chai T., Xia X., Miao Z., Yao M., Gao Y., Huang R., Yang H., Roesler U. Development of a real-time RT-PCR method for rapid detection of H9 avian influenza virus in the air. Archives of Virology 2011, 156:1795-1802.
29. MacInnes H., Zhou Y., Gouveia K., Cromwell J., Lowery K., Layton R.C., Zubelewicz M., Sampath R., Hofstadler S., Liu Y., Cheng Y.S., Koster F. Transmission of aerosolized seasonal H1N1 influenza A to ferrets. PLoS One 2011, 6:e24448.
30. Maines T.R., Chen L.M., Matsuoka Y., Chen H., Rowe T., Ortin J., Falcon A., Nguyen T.H., Mai le Q., Sedyaningsih E.R., Harun S., Tumpey T.M., Donis R.O., Cox N.J., Subbarao K., Katz J.M. Lack of transmission of H5N1 avian-human reassortant influenza viruses in a ferret model. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:12121-12126.
31. Matrosovich M., Tuzikov A., Bovin N., Gambaryan A., Klimov A., Castrucci M.R., Donatelli I., Kawaoka Y. Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals. Journal of Virology 2000, 74:8502-8512.
32. Matrosovich M.N., Krauss S., Webster R.G. H9N2 influenza A viruses from poultry in Asia have human virus-like receptor specificity. Virology 2001, 281:156-162.
33. Mubareka S., Lowen A.C., Steel J., Coates A.L., Garcia-Sastre A., Palese P. Transmission of influenza virus via aerosols and fomites in the guinea pig model. Journal of Infectious Diseases 2009, 199:858-865.
34. Munster V.J., de Wit E., van den Brand J.M., Herfst S., Schrauwen E.J., Bestebroer T.M., van de Vijver D., Boucher C.A., Koopmans M., Rimmelzwaan G.F., Kuiken T., Osterhaus A.D., Fouchier R.A. Pathogenesis and transmission of swine-origin 2009 A(H1N1) influenza virus in ferrets. Science 2009, 325:481-483.
35. Nili H., Asasi K. Natural cases and an experimental study of H9N2 avian influenza in commercial broiler chickens of Iran. Avian Pathology 2002, 31:247-252.
36. Ohuchi M., Orlich M., Ohuchi R., Simpson B.E., Garten W., Klenk H.D., Rott R. Mutations at the cleavage site of the hemagglutinin after the pathogenicity of influenza virus A/chick/Penn/83 (H5N2). Virology 1989, 168:274-280.
37. Peiris M., Yuen K.Y., Leung C.W., Chan K.H., Ip P.L., Lai R.W., Orr W.K., Shortridge K.F. Human infection with influenza H9N2. Lancet 1999, 354:916-917.
38. Shi H., Ashraf S., Gao S., Lu J., Liu X. Evaluation of transmission route and replication efficiency of H9N2 avian influenza virus. Avian Diseases 2010, 54:22-27.
39. Sorrell E.M., Wan H., Araya Y., Song H., Perez D.R. Minimal molecular constraints for respiratory droplet transmission of an avian-human H9N2 influenza A virus. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:7565-7570.
40. Steel J., Lowen A.C., Mubareka S., Palese P. Transmission of influenza virus in a mammalian host is increased by PB2 amino acids 627K or 627E/701N. PLoS Pathogens 2009, 5:e1000252.
41. Steinhauer D.A. Role of hemagglutinin cleavage for the pathogenicity of influenza virus. Virology 1999, 258:1-20.
42. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 2007, 24:1596-1599.
43. Tellier R. Aerosol transmission of influenza A virus: a review of new studies. Journal of the Royal Society Interface 2009, 6(Suppl. 6):S783-S790.
44. van Elden L.J., Nijhuis M., Schipper P., Schuurman R., van Loon A.M. Simultaneous detection of influenza viruses A and B using real-time quantitative PCR. Journal of Clinical Microbiology 2001, 39:196-200.
45. Van Hoeven N., Pappas C., Belser J.A., Maines T.R., Zeng H., Garcia-Sastre A., Sasisekharan R., Katz J.M., Tumpey T.M. Human HA and polymerase subunit PB2 proteins confer transmission of an avian influenza virus through the air. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:3366-3371.
46. Wan H., Sorrell E.M., Song H., Hossain M.J., Ramirez-Nieto G., Monne I., Stevens J., Cattoli G., Capua I., Chen L.M., Donis R.O., Busch J., Paulson J.C., Brockwell C., Webby R., Blanco J., Al-Natour M.Q., Perez D.R. Replication and transmission of H9N2 influenza viruses in ferrets: evaluation of pandemic potential. PLoS One 2008, 3:e2923.
47. Xie X., Li Y., Chwang A.T., Ho P.L., Seto W.H. How far droplets can move in indoor environments - revisiting the Wells evaporation-falling curve. Indoor Air 2007, 17:211-225.
48. Xu K.M., Li K.S., Smith G.J., Li J.W., Tai H., Zhang J.X., Webster R.G., Peiris J.S., Chen H., Guan Y. Evolution and molecular epidemiology of H9N2 influenza A viruses from quail in southern China, 2000 to 2005. Journal of Virology 2007, 81:2635-2645.
49. Xu K.M., Smith G.J., Bahl J., Duan L., Tai H., Vijaykrishna D., Wang J., Zhang J.X., Li K.S., Fan X.H., Webster R.G., Chen H., Peiris J.S., Guan Y. The genesis and evolution of H9N2 influenza viruses in poultry from southern China, 2000 to 2005. Journal of Virology 2007, 81:10389-10401.
50. Yao M., Zhang X., Gao J., Chai T., Miao Z., Ma W., Qin M., Li Q., Li X., Liu J., Zhang H. The occurrence and transmission characteristics of airborne H9N2 avian influenza virus. Berliner und Munchener Tierarztliche Wochenschrift 2011, 124:136-141.
51. Zhou H., Yu Z., Hu Y., Tu J., Zou W., Peng Y., Zhu J., Li Y., Zhang A., Yu Z., Ye Z., Chen H., Jin M. The special neuraminidase stalk-motif responsible for increased virulence and pathogenesis of H5N1 influenza A virus. PLoS One 2009, 4:e6277.