Abstract
H9N2 avian influenza virus has been circulating widely in birds, with occasional infection among humans. Poultry workers are considered to be at high risk of infection with avian influenza due to their frequent exposure to chickens, but the frequency of H9N2 avian influenza virus infections among them is still indistinct. This study was carried out in order to identify the seroprevalence of H9N2 avian influenza virus among poultry workers in Shandong, China. During the period from December 2011 to February 2012, a total of 482 subjects took part in this study, including 382 poultry workers and 100 healthy residents without occupational poultry exposure. Serum samples were collected and tested for the presence of antibodies against H9N2 avian influenza virus by hemagglutination inhibition (HI) and microneutralization (MN) assays. Nine subjects (9/382 = 2.3 %) were positive for antibodies against H9N2 avian influenza virus among poultry workers by either HI or MN assays using ≥40 cut-off, while none of the 100 healthy residents were seropositive. In conclusion, our study identified H9N2 avian influenza infections among poultry workers in Shandong, China, and continuous surveillance of H9N2 avian influenza virus infection in humans should be carried out to evaluate the threat to public health.
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References
Alexander DJ (2000) A review of avian influenza in different bird species. Vet Microbiol 74:3–13
Brown IH, Banks J, Manvell RJ, Essen SC, Shell W, Slomka M et al (2006) Recent epidemiology and ecology of influenza A viruses in avian species in Europe and the Middle East. Dev Biol (Basel) 124:45–50
Lee YJ, Shin JY, Song MS, Lee YM, Choi JG, Lee EK et al (2007) Continuing evolution of H9 influenza viruses in Korean poultry. Virology 359:313–323
Li C, Yu K, Tian G, Yu D, Liu L, Jing B et al (2005) Evolution of H9N2 influenza viruses from domestic poultry in Mainland China. Virology 340:70–83
Xu KM, Smith GJ, Bahl J, Duan L, Tai H, Vijaykrishna D et al (2007) The genesis and evolution of H9N2 influenza viruses in poultry from southern China, 2000 to 2005. J Virol 81:10389–10401
Ji K, Jiang WM, Liu S, Chen JM, Chen J, Hou GY et al (2010) Characterization of the hemagglutinin gene of subtype H9 avian influenza viruses isolated in 2007–2009 in China. J Virol Methods 163:186–189
Zhou JP, Ge FF, Liu J, Ju HB, Yang DQ, Wang J et al (2012) Epidemiological survey and genetic evolution of H9 subtype influenza viruses in Shanghai, China, from 2006 to 2010. Arch Virol 157:1193–1198
Guo YJ, Krauss S, Senne DA, Mo IP, Lo KS, Xiong XP et al (2000) Characterization of the pathogenicity of members of the newly established H9N2 influenza virus lineages in Asia. Virology 267:279–288
Liu H, Liu X, Cheng J, Peng D, Jia L, Huang Y (2003) Phylogenetic analysis of the hemagglutinin genes of twenty-six avian influenza viruses of subtype H9N2 isolated from chickens in China during 1996–2001. Avian Dis 47:116–127
Alexander DJ, Brown IH (2000) Recent zoonoses caused by influenza A viruses. Rev Sci Tech 19:197–125
Peiris M, Yuen KY, Leung CW, Chan KH, Ip PL, Lai RW et al (1999) Human infection with influenza H9N2. Lancet 354:916–917
Guo Y, Li J, Cheng X, Wang M, Zhou Y, Li C et al (1999) Discovery of men infected by avian influenza A (H9N2) virus. Chinese J Exp Clin Virol 13:105–108
Butt KM, Smith GJ, Chen H, Zhang LJ, Leung YH, Xu KM et al (2005) Human infection with an avian H9N2 influenza A virus in Hong Kong in 2003. J Clin Microbiol 43:5760–5767
Matrosovich MN, Krauss S, Webster RG (2001) H9N2 influenza A viruses from poultry in Asia have human virus-like receptor specificity. Virology 281:156–162
Ha Y, Stevens DJ, Skehel JJ, Wiley DC (2001) X-ray structures of H5 avian and H9 swine influenza virus hemagglutinins bound to avian and human receptor analogs. Proc Natl Acad Sci USA 98:11181–11186
Choi YK, Ozaki H, Webby RJ, Webster RG, Peiris JS, Poon L et al (2004) Continuing evolution of H9N2 influenza viruses in Southeastern China. J Virol 78:8609–8614
Deng G, Bi J, Kong F, Li X, Xu Q, Dong J et al (2010) Acute respiratory distress syndrome induced by H9N2 virus in mice. Archi Virol 155:187–195
Wan H, Sorrell EM, Song H, Hossain MJ, Ramirez-Nieto G, Monne I et al (2008) Replication and transmission of H9N2 influenza viruses in ferrets: evaluation of pandemic potential. PLoS One 3:e2923. doi:10.1371/journal.pone.0002923
Perdue ML, Swayne DE (2005) Public health risk from avian influenza viruses. Avian Dis 49:317–327. doi:10.1637/7390-060305R.1
Wong SS, Yuen KY (2006) Avian influenza virus infections in humans. Chest 129:156–168
Zhou L, Liao Q, Dong L, Huai Y, Bai T, Xiang N et al (2009) Risk factors for human illness with avian influenza A (H5N1) virus infection in China. J Infect Dis 199:1726–1734
Koopmans M, Wilbrink B, Conyn M, Natrop G, van der Nat H, Vennema H et al (2004) Transmission of H7N7 avian influenza A virus to human beings during a large outbreak in commercial poultry farms in the Netherlands. Lancet 363:587–593
Wang M, Fu CX, Zheng BJ (2009) Antibodies against H5 and H9 avian influenza among poultry workers in China. N Engl J Med 360:2583–2584
Cong YL, Pu J, Liu QF, Wang S, Zhang GZ, Zhang XL et al (2007) Antigenic and genetic characterization of H9N2 swine influenza viruses in China. J Gen Virol 88:2035–2041
Liu JH, Okazaki K, Mweene A, Shi WM, Wu QM, Su JL et al (2004) Genetic conservation of hemagglutinin gene of H9 influenza virus in chicken population in Mainland China. Virus Genes 29:329–334
Hadipour MM (2011) Seroprevalence of H9N2 avian influenza virus in human population in Boushehr Province, Iran. Asian J Anim Vet Adv 6(2):196–200
Ahad A, Rabbani M, Yaqub T, Younus M, Mahmood A, Shabbir MZ et al (2013) Serosurveillance to H9 and H7 avian influenza virus among poultry workers in Punjab Province, Pakistan. Pak Vet J 33:107–112
Pawar SD, Tandale BV, Raut CG, Parkhi SS, Barde TD, Gurav YK et al (2012) Avian influenza H9N2 Seroprevalence among poultry workers in Pune, India, 2010. PLoS One 7(5):e36374. doi:10.1371/journal.pone.0036374
Uyeki TM, Nguyen DC, Rowe T, Lu X, Hu-Primmer J, Huynh LP et al (2012) Seroprevalence of antibodies to avian influenza A (H5) and A (H9) viruses among market poultry workers, Hanoi, Vietnam, 2001. PLoS One 7(8):e43948
Cheng XW, Liu JJ, He JF, Shan FX (2002) Virological and serological surveys for H9N2 subtype of influenza A virus in chickens and men in Shenzhen city. Chinese J Exp Clin Virol 16:319–321
Rowe T, Abernathy RA, Hu-Primmer J, Thompson WW, Lu X, Lim W et al (1999) Detection of antibody to avian influenza A (H5N1) virus in human serum by using a combination of serologic assays. J Clin Microbiol 37(4):937–943
Yao ML, Zhang XX, Gao J, Chai TJ, Miao ZM, Ma WM et al (2011) The occurrence and transmission characteristics of airborne H9N2 avian influenza virus. Berl Munch Tierarztl Wochenschr 124:136–141
Meijer A, Bosman A, van de Kamp EEHM, Wilbrink B, Du Ry van Beest Holle M, Koopmans M (2006) Measurement of antibodies to avian influenza virus A(H7N7) in humans by hemagglutination inhibition test. J Virol Methods 132:113–120
Wu LL, Diao YX, Ju XJ, Yu CM, Cui JT (2012) Analysis on variation of hemagglutinin genes of sixteen H9N2 subtype avian influenza viruses isolated in Shandong area. Chinese J Virol 28:272–277
Ito T, Suzuki Y, Mitnaul L, Vines A, Kida H, Kawaoka Y (1997) Receptor specificity of influenza A viruses correlates with the agglutination of erythrocytes from different animal species. Virology 227:493–499
Suzuki Y, Ito T, Suzuki T, Holland RE Jr, Chambers TM, Kiso M et al (2000) Sialic acid species as a determinant of the host range of influenza A viruses. J Virol 74:11825–11831
Kayali G, Setterquist SF, Capuano AW, Myers KP, Gill JS, Gray GC (2008) Testing human sera for antibodies against avian influenza viruses: horse RBC hemagglutination inhibition vs. microneutralization assays. J Clin Virol 43:73–78
Shinde PV, Koratkar SS, Pawar SD, Kale SD, Rawankar AS, Mishra AC (2012) Serologic evidence of avian influenza H9N2 and paramyxovirus type 1 infection in emus (Dromaius novaehollandiae) in India. Avian Dis 56:257–260
Jia N, de Vlas SJ, Liu YX, Zhang JS, Zhan L, Dang RL et al (2009) Serological reports of human infections of H7 and H9 avian influenza viruses in northern China. J Clin Virol 44:225–229
Acknowledgments
The authors are grateful for the help of Shandong Center for Disease Control and Prevention for its assistance. This study was supported by Projects of the National Natural Science Foundation of China (31270172) (30871865), Chinese International Cooperation Program (2009DFA32890), Shandong Provincial Family Planning Commission Program (2006-2), Shandong Provincial Department of Education Program (J06L27), a Project of the National Natural Science Foundation of Shandong Province, China (Y2007C126), and a Project of the Shandong Province Science & Technology Development Plan (2010GSF10282).
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The authors declare that they have no conflict of interest.
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Huang, R., Wang, AR., Liu, ZH. et al. Seroprevalence of avian influenza H9N2 among poultry workers in Shandong Province, China. Eur J Clin Microbiol Infect Dis 32, 1347–1351 (2013). https://doi.org/10.1007/s10096-013-1888-7
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DOI: https://doi.org/10.1007/s10096-013-1888-7