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Abstract

Assessing influenza A virus strains circulating in animals and their potential to cross the species barrier and cause human infections is important to improve human influenza surveillance and preparedness. We reviewed studies describing serological evidence of human exposure to animal influenza viruses. Comparing serological data is difficult due to a lack of standardisation in study designs and in laboratory methods used in published reports. Therefore, we designed a scoring system to assess and weigh specificity of obtained serology results in the selected articles. Many studies report reliable evidence of antibodies to swine influenza viruses among persons occupationally exposed to pigs. Most avian influenza studies target H5, H7 and H9 subtypes and most serological evidence of human exposure to avian influenza viruses is reported for these subtypes. Avian influenza studies receiving a low grade in this review often reported higher seroprevalences in humans compared with studies with a high grade. Official surveillance systems mainly focus on avian H5 and H7 viruses. Swine influenza viruses and avian subtypes other than H5 and H7 (emphasising H9) should be additionally included in official surveillance systems. Surveillance efforts should also be directed towards understudied geographical areas, such as Africa and South America.

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2016-11-03
2024-11-08
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2016.21.44.30388
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References

  1. Cox NJ, Subbarao K. Global epidemiology of influenza: past and present. Annu Rev Med. 2000;51(1):407-21.  https://doi.org/10.1146/annurev.med.51.1.407  PMID: 10774473 
  2. Cleaveland S, Haydon DT, Taylor L. Overviews of pathogen emergence: which pathogens emerge, when and why? Curr Top Microbiol Immunol. 2007;315:85-111.  https://doi.org/10.1007/978-3-540-70962-6_5  PMID: 17848062 
  3. Kuiken T, Fouchier R, Rimmelzwaan G, Osterhaus A. Emerging viral infections in a rapidly changing world. Curr Opin Biotechnol. 2003;14(6):641-6.  https://doi.org/10.1016/j.copbio.2003.10.010  PMID: 14662395 
  4. Reperant LA. Applying the theory of island biogeography to emerging pathogens: toward predicting the sources of future emerging zoonotic and vector-borne diseases. Vector Borne Zoonotic Dis. 2010;10(2):105-10.  https://doi.org/10.1089/vbz.2008.0208  PMID: 19589061 
  5. Kuiken T, Holmes EC, McCauley J, Rimmelzwaan GF, Williams CS, Grenfell BT. Host species barriers to influenza virus infections. Science. 2006;312(5772):394-7.  https://doi.org/10.1126/science.1122818  PMID: 16627737 
  6. Freidl GS, Meijer A, de Bruin E, de Nardi M, Munoz O, Capua I, et al. FLURISK Consortium. Influenza at the animal-human interface: a review of the literature for virological evidence of human infection with swine or avian influenza viruses other than A(H5N1). Euro Surveill. 2014;19(18):20793.  https://doi.org/10.2807/1560-7917.ES2014.19.18.20793  PMID: 24832117 
  7. Carrat F, Vergu E, Ferguson NM, Lemaitre M, Cauchemez S, Leach S, et al. Time lines of infection and disease in human influenza: a review of volunteer challenge studies. Am J Epidemiol. 2008;167(7):775-85.  https://doi.org/10.1093/aje/kwm375  PMID: 18230677 
  8. Stephenson I, Das RG, Wood JM, Katz JM. Comparison of neutralising antibody assays for detection of antibody to influenza A/H3N2 viruses: an international collaborative study. Vaccine. 2007;25(20):4056-63.  https://doi.org/10.1016/j.vaccine.2007.02.039  PMID: 17412461 
  9. Wood JM, Gaines-Das RE, Taylor J, Chakraverty P. Comparison of influenza serological techniques by international collaborative study. Vaccine. 1994;12(2):167-74.  https://doi.org/10.1016/0264-410X(94)90056-6  PMID: 8147099 
  10. Meijer A, Bosman A, van de Kamp EE, Wilbrink B, van Beest Holle MDR, Koopmans M. Measurement of antibodies to avian influenza virus A(H7N7) in humans by hemagglutination inhibition test. J Virol Methods. 2006;132(1-2):113-20.  https://doi.org/10.1016/j.jviromet.2005.10.001  PMID: 16271401 
  11. Wibawa H, Henning J, Waluyati DE, Usman TB, Lowther S, Bingham J, et al. Comparison of serological assays for detecting antibodies in ducks exposed to H5 subtype avian influenza virus. BMC Vet Res. 2012;8(1):117.  https://doi.org/10.1186/1746-6148-8-117  PMID: 22823985 
  12. Wang TT, Parides MK, Palese P. Seroevidence for H5N1 influenza infections in humans: meta-analysis. Science. 2012;335(6075):1463.  https://doi.org/10.1126/science.1218888  PMID: 22362880 
  13. Van Kerkhove MD. Brief literature review for the WHO global influenza research agenda--highly pathogenic avian influenza H5N1 risk in humans. Influenza Other Respi Viruses. 2013;7(Suppl 2):26-33.  https://doi.org/10.1111/irv.12077  PMID: 24034480 
  14. Consortium for the Standardization of Influenza Seroepidemiology (CONSISE). Investigation of Zoonotic Respiratory Infection in Humans Exposed to a Confirmed Source. CONSISE; 2013. Available from: https://consise.tghn.org
  15. World Health Organization (WHO). WHO case definitions for human infections with influenza A(H5N1) virus. Geneva: WHO; 2006. Available from: http://www.who.int/influenza/resources/documents/case_definition2006_08_29/en/
  16. World Health Organization (WHO). Recommendations and laboratory procedures for detection of avian influenza A(H5N1) virus in specimens from suspected human cases. Geneva: WHO; 2007. Available from: http://www.who.int/influenza/resources/documents/RecAIlabtestsAug07.pdf
  17. Hancock K, Veguilla V, Lu X, Zhong W, Butler EN, Sun H, et al. Cross-reactive antibody responses to the 2009 pandemic H1N1 influenza virus. N Engl J Med. 2009;361(20):1945-52.  https://doi.org/10.1056/NEJMoa0906453  PMID: 19745214 
  18. Coman A, Maftei DN, Krueger WS, Heil GL, Friary JA, Chereches RM, et al. Serological evidence for avian H9N2 influenza virus infections among Romanian agriculture workers. J Infect Public Health. 2013;6(6):438-47.  https://doi.org/10.1016/j.jiph.2013.05.003  PMID: 23999337 
  19. Beaudoin A, Gramer M, Gray GC, Capuano A, Setterquist S, Bender J. Serologic survey of swine workers for exposure to H2N3 swine influenza A. Influenza Other Respi Viruses. 2010;4(3):163-70.  https://doi.org/10.1111/j.1750-2659.2009.00127.x  PMID: 20409213 
  20. World Health Organization (WHO). Sex, gender and influenza in achieving gender equality and health equity. Geneva: WHO; 2010. Available from: http://apps.who.int/iris/bitstream/10665/44401/1/9789241500111_eng.pdf
  21. Corti D, Suguitan AL Jr, Pinna D, Silacci C, Fernandez-Rodriguez BM, Vanzetta F, et al. Heterosubtypic neutralizing antibodies are produced by individuals immunized with a seasonal influenza vaccine. J Clin Invest. 2010;120(5):1663-73.  https://doi.org/10.1172/JCI41902  PMID: 20389023 
  22. Oshansky CM, Wong SS, Jeevan T, Smallwood HS, Webby RJ, Shafir SC, et al. Seasonal influenza vaccination is the strongest correlate of cross-reactive antibody responses in migratory bird handlers. MBio. 2014;5(6):e02107.  https://doi.org/10.1128/mBio.02107-14  PMID: 25491354 
  23. Corti D, Voss J, Gamblin SJ, Codoni G, Macagno A, Jarrossay D, et al. A neutralizing antibody selected from plasma cells that binds to group 1 and group 2 influenza A hemagglutinins. Science. 2011;333(6044):850-6.  https://doi.org/10.1126/science.1205669  PMID: 21798894 
  24. Roozendaal R, Tolboom J, Roos A, Riahi S, Theeuwsen J, Bujny MV, et al. Transient humoral protection against H5N1 challenge after seasonal influenza vaccination of humans. PLoS One. 2014;9(7):e103550.  https://doi.org/10.1371/journal.pone.0103550  PMID: 25075622 
  25. Gioia C, Castilletti C, Tempestilli M, Piacentini P, Bordi L, Chiappini R, et al. Cross-subtype immunity against avian influenza in persons recently vaccinated for influenza. Emerg Infect Dis. 2008;14(1):121-8.  https://doi.org/10.3201/eid1401.061283  PMID: 18258091 
  26. Sui J, Sheehan J, Hwang WC, Bankston LA, Burchett SK, Huang CY, et al. Wide prevalence of heterosubtypic broadly neutralizing human anti-influenza A antibodies. Clin Infect Dis. 2011;52(8):1003-9.  https://doi.org/10.1093/cid/cir121  PMID: 21460314 
  27. Lynch GW, Selleck P, Church WB, Sullivan JS. Seasoned adaptive antibody immunity for highly pathogenic pandemic influenza in humans. Immunol Cell Biol. 2012;90(2):149-58.  https://doi.org/10.1038/icb.2011.38  PMID: 21647170 
  28. World Health Organization (WHO) Global Influenza Surveillance Network. 2.G. Serological diagnosis of influenza by microneutralization assay. Part 2. The laboratory diagnosis and virological surveillance of influenza. In: Manual for the laboratory diagnosis and virological surveillance of influenza. Geneva: WHO; 2011. ISBN 978 92 4 154809 0.
  29. Masurel N, Mulder J. Studies on the content of antibodies for equine influenza viruses in human sera. Bull World Health Organ. 1966;34(6):885-93. PMID: 5296537 
  30. Tümová B, Svandová E, Stumpa G. Findings of antibodies to animal influenza viruses in human sera and their significance for the study of interviral antigenic relationship. J Hyg Epidemiol Microbiol Immunol. 1968;12(3):284-95. PMID: 4306517 
  31. Schnurrenberger PR, Woods GT, Martin RJ. Serologic evidence of human infection with swine influenza virus. Am Rev Respir Dis. 1970;102(3):356-61. PMID: 5465431 
  32. Cuneo-Crovari P, Gasparini R, Pellegrino C. Sero-epidemiological survey on human and swine influenza A. Situation at the onset of summer 1976. Boll Ist Sieroter Milan. 1976;55(5):463-70. PMID: 189788 
  33. Masurel N. Swine influenza virus and the recycling of influenza-A viruses in man. Lancet. 1976;2(7979):244-7.  https://doi.org/10.1016/S0140-6736(76)91038-2  PMID: 59252 
  34. Pyhälä R. Antibodies to influenza A/swine-like viruses (Hsw1N1) in human sera: antigenic stimulation and changes in antibody status. Acta Pathol Microbiol Scand B. 1976;84B(6):373-8. PMID: 998257 
  35. Smith JW. Letter: Swine influenza in Hodgkin’s disease. N Engl J Med. 1976;295(13):732.  https://doi.org/10.1056/NEJM197609232951315  PMID: 958251 
  36. Thompson RL, Sande MA, Wenzel RP, Hoke CH Jr, Gwaltney JM Jr. Swine-influenza infection in civilians. Report of two cases. N Engl J Med. 1976;295(13):714-5.  https://doi.org/10.1056/NEJM197609232951307  PMID: 958246 
  37. Gaydos JC, Hodder RA, Top FH Jr, Soden VJ, Allen RG, Bartley JD, et al. Swine influenza A at Fort Dix, New Jersey (January-February 1976). I. Case finding and clinical study of cases. J Infect Dis. 1977;136(Suppl):S356-62.  https://doi.org/10.1093/infdis/136.Supplement_3.S356  PMID: 606759 
  38. Hodder RA, Gaydos JC, Allen RG, Top FH Jr, Nowosiwsky T, Russell PK. Swine influenza A at Fort Dix, New Jersey (January-February 1976). III. Extent of spread and duration of the outbreak. J Infect Dis. 1977;136(Suppl):S369-75.  https://doi.org/10.1093/infdis/136.Supplement_3.S369  PMID: 606761 
  39. O’Brien RJ, Noble GR, Easterday BC, Kendal AP, Shasby DM, Nelson DB, et al. Swine-like influenza virus infection in a Wisconsin farm family. J Infect Dis. 1977;136(Suppl):S390-6.  https://doi.org/10.1093/infdis/136.Supplement_3.S390  PMID: 564374 
  40. Olson JG. Epizootic swine influenza with evidence of a low rate of human infection associated with occupational exposure to swine. Southeast Asian J Trop Med Public Health. 1977;8(3):368-70. PMID: 204060 
  41. Măgureanu E, Busuioc C, Ionescu V, Tisu A, Stoicescu A, Guguianu E, et al. Investigations on the involvement of swine influenza A virus (Hsw1N1) in the influenza outbreak recorded in a town of Romania during the 1976--1977 winter season. Virologie. 1978;29(3):199-202. PMID: 567886 
  42. Tan DS, Omar M, Yap TC. Influenza HI antibodies in pig and man in Malaysia (with special reference to swine influenza). Med J Malaysia. 1979;34(2):159-62. PMID: 548720 
  43. Woods GT, Schnurrenberger PR, Martin RJ, Tompkins WA. Swine influenza virus in swine and man in Illinois. J Occup Med. 1981;23(4):263-7. PMID: 6260919 
  44. Sinnecker H, Sinnecker R, Zilske E, Strey A, Leopoldt D. Influenza virus A/swine-outbreaks in domestic pigs and antibody findings in human sera. Zentralbl Bakteriol Mikrobiol Hyg A. 1983;255(2-3):209-13. PMID: 6316691 
  45. Profeta ML, Palladino G. Serological evidence of human infections with avian influenza viruses. Brief report. Arch Virol. 1986;90(3-4):355-60.  https://doi.org/10.1007/BF01317384  PMID: 3729733 
  46. Wells DL, Hopfensperger DJ, Arden NH, Harmon MW, Davis JP, Tipple MA, et al. Swine influenza virus infections. Transmission from ill pigs to humans at a Wisconsin agricultural fair and subsequent probable person-to-person transmission. JAMA. 1991;265(4):478-81.  https://doi.org/10.1001/jama.1991.03460040054028  PMID: 1845913 
  47. Shortridge KF. Pandemic influenza: a zoonosis? Semin Respir Infect. 1992;7(1):11-25. PMID: 1609163 
  48. Shu LL, Zhou NN, Sharp GB, He SQ, Zhang TJ, Zou WW, et al. An epidemiological study of influenza viruses among Chinese farm families with household ducks and pigs. Epidemiol Infect. 1996;117(1):179-88.  https://doi.org/10.1017/S0950268800001291  PMID: 8760967 
  49. Zhou N, He S, Zhang T, Zou W, Shu L, Sharp GB, et al. Influenza infection in humans and pigs in southeastern China. Arch Virol. 1996;141(3-4):649-61.  https://doi.org/10.1007/BF01718323  PMID: 8645101 
  50. Peiris M, Yuen KY, Leung CW, Chan KH, Ip PL, Lai RW, et al. Human infection with influenza H9N2. Lancet. 1999;354(9182):916-7.  https://doi.org/10.1016/S0140-6736(99)03311-5  PMID: 10489954 
  51. Mayahi M. Detection of Antibody Against Influenza A Subtype H9N2 in Human Sera in Iran. The 11th International Symposium Of the World Association of Veterinary Laboratory Diagnosticians and OIE Seminar on Biotechnology; Ahvaz, Iran; 2003.
  52. Ayora-Talavera G, Cadavieco-Burgos JM, Canul-Armas AB. Serologic evidence of human and swine influenza in Mayan persons. Emerg Infect Dis. 2005;11(1):158-61.  https://doi.org/10.3201/eid1101.040554  PMID: 15705345 
  53. Puzelli S, Di Trani L, Fabiani C, Campitelli L, De Marco MA, Capua I, et al. Serological analysis of serum samples from humans exposed to avian H7 influenza viruses in Italy between 1999 and 2003. J Infect Dis. 2005;192(8):1318-22.  https://doi.org/10.1086/444390  PMID: 16170747 
  54. Barbour EK, Sagherian VK, Sagherian NK, Dankar SK, Jaber LS, Usayran NN, et al. Avian influenza outbreak in poultry in the Lebanon and transmission to neighbouring farmers and swine. Vet Ital. 2006;42(2):77-85. PMID: 20429054 
  55. Gill JS, Webby R, Gilchrist MJ, Gray GC. Avian influenza among waterfowl hunters and wildlife professionals. Emerg Infect Dis. 2006;12(8):1284-6.  https://doi.org/10.3201/eid1708.060492  PMID: 16965717 
  56. Myers KP, Olsen CW, Setterquist SF, Capuano AW, Donham KJ, Thacker EL, et al. Are swine workers in the United States at increased risk of infection with zoonotic influenza virus? Clin Infect Dis. 2006;42(1):14-20.  https://doi.org/10.1086/498977  PMID: 16323086 
  57. Ramirez A, Capuano AW, Wellman DA, Lesher KA, Setterquist SF, Gray GC. Preventing zoonotic influenza virus infection. Emerg Infect Dis. 2006;12(6):996-1000.  https://doi.org/10.3201/eid1206.051576  PMID: 16707061 
  58. Gray GC, McCarthy T, Capuano AW, Setterquist SF, Olsen CW, Alavanja MC, et al. Swine workers and swine influenza virus infections. Emerg Infect Dis. 2007;13(12):1871-8.  https://doi.org/10.3201/eid1312.061323  PMID: 18258038 
  59. Myers KP, Setterquist SF, Capuano AW, Gray GC. Infection due to 3 avian influenza subtypes in United States veterinarians. Clin Infect Dis. 2007;45(1):4-9.  https://doi.org/10.1086/518579  PMID: 17554693 
  60. Ortiz EJ, Kochel TJ, Capuano AW, Setterquist SF, Gray GC. Avian influenza and poultry workers, Peru, 2006. Influenza Other Respi Viruses. 2007;1(2):65-9.  https://doi.org/10.1111/j.1750-2659.2007.00009.x  PMID: 18167521 
  61. Robinson JL, Lee BE, Patel J, Bastien N, Grimsrud K, Seal RF, et al. Swine influenza (H3N2) infection in a child and possible community transmission, Canada. Emerg Infect Dis. 2007;13(12):1865-70.  https://doi.org/10.3201/eid1312.070615  PMID: 18258037 
  62. Skowronski DM, Li Y, Tweed SA, Tam TW, Petric M, David ST, et al. Protective measures and human antibody response during an avian influenza H7N3 outbreak in poultry in British Columbia, Canada. CMAJ. 2007;176(1):47-53.  https://doi.org/10.1503/cmaj.060204  PMID: 17200390 
  63. Gray GC, McCarthy T, Capuano AW, Setterquist SF, Alavanja MC, Lynch CF. Evidence for avian influenza A infections among Iowa’s agricultural workers. Influenza Other Respi Viruses. 2008;2(2):61-9.  https://doi.org/10.1111/j.1750-2659.2008.00041.x  PMID: 18941621 
  64. Lu CY, Lu JH, Chen WQ, Jiang LF, Tan BY, Ling WH, et al. Potential infections of H5N1 and H9N2 avian influenza do exist in Guangdong populations of China. Chin Med J (Engl). 2008;121(20):2050-3. PMID: 19080274 
  65. Ogata T, Yamazaki Y, Okabe N, Nakamura Y, Tashiro M, Nagata N, et al. Human H5N2 avian influenza infection in Japan and the factors associated with high H5N2-neutralizing antibody titer. J Epidemiol. 2008;18(4):160-6.  https://doi.org/10.2188/jea.JE2007446  PMID: 18603824 
  66. Alizadeh EHS, Kheiri MT, Mazaheri V, Bashar R, Tabatabaeian M. Avian Influenza (H9N2) among poultry workers in Iran. Iran J Microbiol. 2009;1(3):3-6.
  67. Jia N, de Vlas SJ, Liu YX, Zhang JS, Zhan L, Dang RL, et al. Serological reports of human infections of H7 and H9 avian influenza viruses in northern China. J Clin Virol. 2009;44(3):225-9.  https://doi.org/10.1016/j.jcv.2008.12.014  PMID: 19186101 
  68. Wang M, Fu CX, Zheng BJ. Antibodies against H5 and H9 avian influenza among poultry workers in China. N Engl J Med. 2009;360(24):2583-4.  https://doi.org/10.1056/NEJMc0900358  PMID: 19516044 
  69. Yamazaki Y, Doy M, Okabe N, Yasui Y, Nakashima K, Fujieda T, et al. Serological survey of avian H5N2-subtype influenza virus infections in human populations. Arch Virol. 2009;154(3):421-7.  https://doi.org/10.1007/s00705-009-0319-7  PMID: 19189196 
  70. Hadipour M. H9N2 Avian Influenza Virus Antibody Titres in Human Population in Fars Province, Iran. Brazilian Journal of Poultry Science.2010;12(3):161-4.
  71. Kayali G, Ortiz EJ, Chorazy ML, Gray GC. Evidence of previous avian influenza infection among US turkey workers. Zoonoses Public Health. 2010;57(4):265-72.  https://doi.org/10.1111/j.1863-2378.2009.01231.x  PMID: 19486492 
  72. Krumbholz A, Lange J, Dürrwald R, Hoyer H, Bengsch S, Wutzler P, et al. Prevalence of antibodies to swine influenza viruses in humans with occupational exposure to pigs, Thuringia, Germany, 2008-2009. J Med Virol. 2010;82(9):1617-25.  https://doi.org/10.1002/jmv.21869  PMID: 20648619 
  73. Qin PZ, Ming W, Liu Y, editors. Surveillance of human infections with Avian influenza in Guangzhou during 1997—2006. 14th International Congress on Infectious Diseases (ICID); 2010 Mar 9-12; Miami (FL, United States). Brookline (MA, United States): International Society for Infectious Diseases. Abstracts; 2010.
  74. Terebuh P, Olsen CW, Wright J, Klimov A, Karasin A, Todd K, et al. Transmission of influenza A viruses between pigs and people, Iowa, 2002-2004. Influenza Other Respi Viruses. 2010;4(6):387-96.  https://doi.org/10.1111/j.1750-2659.2010.00175.x  PMID: 20958933 
  75. Dawood FS, Dong L, Liu F, Blau DM, Peebles PJ, Lu X, et al. A pre-pandemic outbreak of triple-reassortant swine influenza virus infection among university students, South Dakota, 2008. J Infect Dis. 2011;204(8):1165-71.  https://doi.org/10.1093/infdis/jir502  PMID: 21917888 
  76. Donahue JG, Coleman LA, Bender J, Kempf D, Vandermause MF, McGraw PJ, et al. Prospective study of avian influenza infection in backyard poultry flocks and flock handlers in Wisconsin. Vector Borne Zoonotic Dis. 2011;11(9):1293-7.  https://doi.org/10.1089/vbz.2010.0260  PMID: 21612537 
  77. Gerloff NA, Kremer JR, Charpentier E, Sausy A, Olinger CM, Weicherding P, et al. Swine influenza virus antibodies in humans, western Europe, 2009. Emerg Infect Dis. 2011;17(3):403-11.  https://doi.org/10.3201/eid1703.100851  PMID: 21392430 
  78. Gray GC, Ferguson DD, Lowther PE, Heil GL, Friary JA. A national study of US bird banders for evidence of avian influenza virus infections. J Clin Virol. 2011;51(2):132-5.  https://doi.org/10.1016/j.jcv.2011.03.011  PMID: 21530384 
  79. Hadipour M. Seroprevalence of H9N2 Avian Influenza Virus in Human Population in Boushehr Province, Iran. Asian J Anim Vet Adv. 2011;6(2):196-200 . https://doi.org/10.3923/ajava.2011.196.200 
  80. Kayali G, Barbour E, Dbaibo G, Tabet C, Saade M, Shaib HA, et al. Evidence of infection with H4 and H11 avian influenza viruses among Lebanese chicken growers. PLoS One. 2011;6(10):e26818.  https://doi.org/10.1371/journal.pone.0026818  PMID: 22046370 
  81. Khuntirat BP, Yoon IK, Blair PJ, Krueger WS, Chittaganpitch M, Putnam SD, et al. Evidence for subclinical avian influenza virus infections among rural Thai villagers. Clin Infect Dis. 2011;53(8):e107-16.  https://doi.org/10.1093/cid/cir525  PMID: 21921216 
  82. Kitikoon P, Sreta D, Tuanudom R, Amonsin A, Suradhat S, Oraveerakul K, et al. Serological evidence of pig-to-human influenza virus transmission on Thai swine farms. Vet Microbiol. 2011;148(2-4):413-8.  https://doi.org/10.1016/j.vetmic.2010.09.019  PMID: 20965670 
  83. Kohls A, Hafez HM, Harder T, Jansen A, Lierz P, Lüschow D, et al. Avian influenza virus risk assessment in falconry. Virol J. 2011;8(1):187.  https://doi.org/10.1186/1743-422X-8-187  PMID: 21513552 
  84. Leibler JH, Silbergeld EK, Pekosz A, Gray GC. No evidence of infection with avian influenza viruses among US poultry workers in the Delmarva Peninsula, Maryland and Virginia, USA. J Agromed. 2011;16(1):52-7.  https://doi.org/10.1080/1059924X.2011.533612  PMID: 21213164 
  85. Shtjefni V, Kumbe I, , Cabeli P, Shoshi N, Atipi I, Shtylla T. Serologic evidence of H1N1 and H3N2 swine influenza virus in swine workers. CR Acad Bulg sci. 2011;64(11):1549-54.
  86. Arzey GG, Kirkland PD, Arzey KE, Frost M, Maywood P, Conaty S, et al. Influenza virus A (H10N7) in chickens and poultry abattoir workers, Australia. Emerg Infect Dis. 2012;18(5):814-6.  https://doi.org/10.3201/eid1805.111852  PMID: 22516302 
  87. Di Trani L, Porru S, Bonfanti L, Cordioli P, Cesana BM, Boni A, et al. Serosurvey against H5 and H7 avian influenza viruses in Italian poultry workers. Avian Dis. 2012;56(4) Suppl;1068-71.  https://doi.org/10.1637/10184-041012-ResNote.1  PMID: 23402138 
  88. López-Robles G, Montalvo-Corral M, Caire-Juvera G, Ayora-Talavera G, Hernández J. Seroprevalence and risk factors for swine influenza zoonotic transmission in swine workers from northwestern Mexico. Transbound Emerg Dis. 2012;59(2):183-8.  https://doi.org/10.1111/j.1865-1682.2011.01250.x  PMID: 21801341 
  89. Pawar SD, Tandale BV, Raut CG, Parkhi SS, Barde TD, Gurav YK, et al. Avian influenza H9N2 seroprevalence among poultry workers in Pune, India, 2010. PLoS One. 2012;7(5):e36374.  https://doi.org/10.1371/journal.pone.0036374  PMID: 22623954 
  90. Shafir SC, Fuller T, Smith TB, Rimoin AW. A national study of individuals who handle migratory birds for evidence of avian and swine-origin influenza virus infections. J Clin Virol. 2012;54(4):364-7.  https://doi.org/10.1016/j.jcv.2012.05.001  PMID: 22632900 
  91. Uyeki TM, Nguyen DC, Rowe T, Lu X, Hu-Primmer J, Huynh LP, et al. Seroprevalence of antibodies to avian influenza A (H5) and A (H9) viruses among market poultry workers, Hanoi, Vietnam, 2001. PLoS One. 2012;7(8):e43948.  https://doi.org/10.1371/journal.pone.0043948  PMID: 22928049 
  92. Wong KK, Greenbaum A, Moll ME, Lando J, Moore EL, Ganatra R, et al. Outbreak of influenza A (H3N2) variant virus infection among attendees of an agricultural fair, Pennsylvania, USA, 2011. Emerg Infect Dis. 2012;18(12):1937-44.  https://doi.org/10.3201/eid1812.121097  PMID: 23171635 
  93. Yang P, Ma C, Shi W, Cui S, Lu G, Peng X, et al. A serological survey of antibodies to H5, H7 and H9 avian influenza viruses amongst the duck-related workers in Beijing, China. PLoS One. 2012;7(11):e50770.  https://doi.org/10.1371/journal.pone.0050770  PMID: 23226380 
  94. Yang P, Shi W, Cui S, Zhang Y, Liu X, Wang Q. Infection with multiple avian influenza viruses in a man without poultry-handling practices suggesting an increased probability of emergent pandemic influenza virus in general population. Clin Infect Dis. 2012;54(2):307.  https://doi.org/10.1093/cid/cir844  PMID: 22144542 
  95. Luetteke N, Gerloff NA, Gohrbandt S, Weicherding P, van Reeth K, Muller CP. Neutralizing antibodies against pandemic, seasonal and avian-like H1N1 swine influenza virus in swine contacts and swine, Western-Europe. Int J Infect Dis. 2012;16(Suppl 1):e136 . https://doi.org/10.1016/j.ijid.2012.05.308  PMID: 22197748 
  96. Ahad A, Rabbani M, Yaqub T, Younus M, Mahmood A, Shabbir MZ, et al. Serosurveillance to H9 and H7 Avian Influenza Virus among Poultry Workers in Punjab Province, Pakistan. Pak Vet J. 2012;33(1):107-12.
  97. Bai T, Zhou J, Shu Y. Serologic study for influenza A (H7N9) among high-risk groups in China. N Engl J Med. 2013;368(24):2339-40.  https://doi.org/10.1056/NEJMc1305865  PMID: 23718151 
  98. Blair PJ, Putnam SD, Krueger WS, Chum C, Wierzba TF, Heil GL, et al. Evidence for avian H9N2 influenza virus infections among rural villagers in Cambodia. J Infect Public Health. 2013;6(2):69-79.  https://doi.org/10.1016/j.jiph.2012.11.005  PMID: 23537819 
  99. Huang R, Wang AR, Liu ZH, Liang W, Li XX, Tang YJ, et al. Seroprevalence of avian influenza H9N2 among poultry workers in Shandong Province, China. Eur J Clin Microbiol Infect Dis. 2013;32(10):1347-51.  https://doi.org/10.1007/s10096-013-1888-7  PMID: 23733318 
  100. Khurelbaatar N, Krueger WS, Heil GL, Darmaa B, Ulziimaa D, Tserennorov D, et al. Sparse evidence for equine or avian influenza virus infections among Mongolian adults with animal exposures. Influenza Other Respi Viruses. 2013;7(6):1246-50.  https://doi.org/10.1111/irv.12148  PMID: 23941547 
  101. Krueger WS, Khuntirat B, Yoon IK, Blair PJ, Chittagarnpitch M, Putnam SD, et al. Prospective study of avian influenza virus infections among rural Thai villagers. PLoS One. 2013;8(8):e72196.  https://doi.org/10.1371/journal.pone.0072196  PMID: 23977250 
  102. Okoye J, Eze D, Krueger WS, Heil GL, Friary JA, Gray GC. Serologic evidence of avian influenza virus infections among Nigerian agricultural workers. J Med Virol. 2013;85(4):670-6.  https://doi.org/10.1002/jmv.23520  PMID: 23400898 
  103. Su S, Chen J, Cao Z, Lai A, Gu H, Ke C, et al. Detection of antibodies against Avian influenza virus subtypes H7 and H9 among veterinarians in Guangdong province, China. J Clin Microbiol. 2013;51(12):4272-4.  https://doi.org/10.1128/JCM.01812-13  PMID: 24048542 
  104. Yu Q, Liu L, Pu J, Zhao J, Sun Y, Shen G, et al. Risk perceptions for avian influenza virus infection among poultry workers, China. Emerg Infect Dis. 2013;19(2):313-6.  https://doi.org/10.3201/eid1902.120251  PMID: 23343592 
  105. Zu R, Dong L, Qi X, Wang D, Zou S, Bai T, et al. Virological and serological study of human infection with swine influenza A H1N1 virus in China. Virology. 2013;446(1-2):49-55.  https://doi.org/10.1016/j.virol.2013.07.022  PMID: 24074566 
  106. Krueger WS, Heil GL, Yoon KJ, Gray GC. No evidence for zoonotic transmission of H3N8 canine influenza virus among US adults occupationally exposed to dogs. Influenza Other Respi Viruses. 2014;8(1):99-106.  https://doi.org/10.1111/irv.12208  PMID: 24237615 
  107. Anvar E, Hosseini SM, Tavasoti Kheiri M, Mazaheri V, Fazaei K, Shabani M, et al. Serological Survey of Avian Influenza (H9N2) Among Different Occupational Groups in Tehran and Qazvin Provinces in IR Iran. Jundishapur J Microbiol. 2013;6(4):e5441.
  108. Khurelbaatar N, Krueger WS, Heil GL, Darmaa B, Ulziimaa D, Tserennorov D, et al. Little evidence of avian or equine influenza virus infection among a cohort of Mongolian adults with animal exposures, 2010-2011. PLoS One. 2014;9(1):e85616.  https://doi.org/10.1371/journal.pone.0085616  PMID: 24465622 
  109. Krumbholz A, Lange J, Dürrwald R, Walther M, Müller TH, Kühnel D, et al. Prevalence of antibodies to European porcine influenza viruses in humans living in high pig density areas of Germany. Med Microbiol Immunol (Berl). 2014;203(1):13-24.  https://doi.org/10.1007/s00430-013-0309-y  PMID: 24013183 
  110. Yang S, Chen Y, Cui D, Yao H, Lou J, Huo Z, et al. Avian-origin influenza A(H7N9) infection in influenza A(H7N9)-affected areas of China: a serological study. J Infect Dis. 2014;209(2):265-9.  https://doi.org/10.1093/infdis/jit430  PMID: 23935201 
  111. Zhou P, Zhu W, Gu H, Fu X, Wang L, Zheng Y, et al. Avian influenza H9N2 seroprevalence among swine farm residents in China. J Med Virol. 2014;86(4):597-600.  https://doi.org/10.1002/jmv.23869  PMID: 24390939 
  112. Qi W, Su S, Xiao C, Zhou P, Li H, Ke C, et al. Antibodies against H10N8 avian influenza virus among animal workers in Guangdong Province before November 30, 2013, when the first human H10N8 case was recognized. BMC Med. 2014;12(1):205.  https://doi.org/10.1186/s12916-014-0205-3  PMID: 25348464 
  113. Zhou H, Zheng Y, Wang L, Cui J, Fu X, He S, et al. First serologic study for influenza A (H7N9) virus among veterinarians in Guangdong, China. J Clin Virol. 2014;60(2):182-3.  https://doi.org/10.1016/j.jcv.2014.03.007  PMID: 24717773 
  114. Pawar SD, Tandale BV, Gurav YK, Parkhi YK, Kode SS. Immunity status against influenza A subtype H7N9 and other avian influenza viruses in a high-risk group and the general population in India. J Infect Dis. 2014;210(1):160-1.  https://doi.org/10.1093/infdis/jiu033  PMID: 24453261 
  115. Yin X, Yin X, Rao B, Xie C, Zhang P, Qi X, et al. Antibodies against avian-like A (H1N1) swine influenza virus among swine farm residents in eastern China. J Med Virol. 2014;86(4):592-6.  https://doi.org/10.1002/jmv.23842  PMID: 24497077 
  116. Zhou H, Cao Z, Tan L, Fu X, Lu G, Qi W, et al. Avian-like A (H1N1) swine influenza virus antibodies among swine farm residents and pigs in southern China. Jpn J Infect Dis. 2014;67(3):184-90.  https://doi.org/10.7883/yoken.67.184  PMID: 24858607 
  117. Coman A, Maftei DN, Krueger WS, Heil GL, Chereches RM, Sirlincan E, et al. A prospective study of Romanian agriculture workers for zoonotic influenza infections. PLoS One. 2014;9(5):e98248.  https://doi.org/10.1371/journal.pone.0098248  PMID: 24869796 
  118. Gray GC, Krueger WS, Chum C, Putnam SD, Wierzba TF, Heil GL, et al. Little evidence of subclinical avian influenza virus infections among rural villagers in Cambodia. PLoS One. 2014;9(5):e97097.  https://doi.org/10.1371/journal.pone.0097097  PMID: 24819948 
  119. Wang Q, Ju L, Liu P, Zhou J, Lv X, Li L, et al. Serological and virological surveillance of avian influenza A virus H9N2 subtype in humans and poultry in Shanghai, China, between 2008 and 2010. Zoonoses Public Health. 2015;62(2):131-40.  https://doi.org/10.1111/zph.12133  PMID: 24803167 
  120. Shamliyan T, Kane RL, Dickinson S. A systematic review of tools used to assess the quality of observational studies that examine incidence or prevalence and risk factors for diseases. J Clin Epidemiol. 2010;63(10):1061-70.  https://doi.org/10.1016/j.jclinepi.2010.04.014  PMID: 20728045 
  121. Wood JM, Montomoli E, Newman RW, Daas A, Buchheit KH, Terao E. Collaborative study on influenza vaccine clinical trial serology - part 2: reproducibility study. Pharmeur Bio Sci Notes. 2011;2011(1):36-54. PMID: 21619855 
  122. Stephenson I, Heath A, Major D, Newman RW, Hoschler K, Junzi W, et al. Reproducibility of serologic assays for influenza virus A (H5N1). Emerg Infect Dis. 2009;15(8):1252-9.  https://doi.org/10.3201/eid1508.081754  PMID: 19751587 
  123. Wagner R, Pfleiderer M. Reproducibility of assays for influenza vaccine immunogenicity determination: progress towards consistency. Expert Rev Vaccines. 2012;11(8):881-3.  https://doi.org/10.1586/erv.12.62  PMID: 23002967 
  124. Wagner R, Göpfert C, Hammann J, Neumann B, Wood J, Newman R, et al. Enhancing the reproducibility of serological methods used to evaluate immunogenicity of pandemic H1N1 influenza vaccines-an effective EU regulatory approach. Vaccine. 2012;30(27):4113-22.  https://doi.org/10.1016/j.vaccine.2012.02.077  PMID: 22446639 
  125. Buchy P, Vong S, Chu S, Garcia JM, Hien TT, Hien VM, et al. Kinetics of neutralizing antibodies in patients naturally infected by H5N1 virus. PLoS One. 2010;5(5):e10864.  https://doi.org/10.1371/journal.pone.0010864  PMID: 20532246 
  126. WHO. Seroepidemiological studies of pandemic influenza A (H1N1) 2009 virus. Wkly Epidemiol Rec. 2010;85(24):229-35. PMID: 20545056 
  127. Laurie KL, Huston P, Riley S, Katz JM, Willison DJ, Tam JS, et al. Influenza serological studies to inform public health action: best practices to optimise timing, quality and reporting. Influenza Other Respi Viruses. 2013;7(2):211-24.  https://doi.org/10.1111/j.1750-2659.2012.0370a.x  PMID: 22548725 
  128. Nelson MI, Vincent AL. Reverse zoonosis of influenza to swine: new perspectives on the human-animal interface. Trends Microbiol. 2015;23(3):142-53.  https://doi.org/10.1016/j.tim.2014.12.002  PMID: 25564096 
  129. Van Kerkhove MD, Broberg E, Engelhardt OG, Wood J, Nicoll ACONSISE steering committee. The consortium for the standardization of influenza seroepidemiology (CONSISE): a global partnership to standardize influenza seroepidemiology and develop influenza investigation protocols to inform public health policy. Influenza Other Respi Viruses. 2013;7(3):231-4.  https://doi.org/10.1111/irv.12068  PMID: 23280042 
  130. De Marco MA, Porru S, Cordioli P, Cesana BM, Moreno A, Calzoletti L, et al. Evidence of cross-reactive immunity to 2009 pandemic influenza A virus in workers seropositive to swine H1N1 influenza viruses circulating in Italy. PLoS One. 2013;8(2):e57576.  https://doi.org/10.1371/journal.pone.0057576  PMID: 23469029 
  131. Wu J, Yi L, Ni H, Zou L, Zhang H, Zeng X, et al. Anti-Human H1N1pdm09 and swine H1N1 Virus Antibodies among Swine Workers in Guangdong Province, China. Sci Rep. 2015;5:12507.  https://doi.org/10.1038/srep12507  PMID: 26205221 
  132. Vincent A, Awada L, Brown I, Chen H, Claes F, Dauphin G, et al. Review of influenza A virus in swine worldwide: a call for increased surveillance and research. Zoonoses Public Health. 2014;61(1):4-17.  https://doi.org/10.1111/zph.12049  PMID: 23556412 
  133. World Health Organization (WHO). Influenza at the human-animal interface. Summary and assessment, 20 July to 3 October 2016. Geneva: WHO. Available from: http://www.who.int/influenza/human_animal_interface/Influenza_Summary_IRA_HA_interface_10_03_2016.pdf?ua=1
  134. Butt KM, Smith GJ, Chen H, Zhang LJ, Leung YH, Xu KM, et al. Human infection with an avian H9N2 influenza A virus in Hong Kong in 2003. J Clin Microbiol. 2005;43(11):5760-7.  https://doi.org/10.1128/JCM.43.11.5760-5767.2005  PMID: 16272514 
  135. Huang Y, Li X, Zhang H, Chen B, Jiang Y, Yang L, et al. Human infection with an avian influenza A (H9N2) virus in the middle region of China. J Med Virol. 2015;87(10):1641-8.  https://doi.org/10.1002/jmv.24231  PMID: 25965534 
  136. Xu KM, Smith GJ, Bahl J, Duan L, Tai H, Vijaykrishna D, et al. The genesis and evolution of H9N2 influenza viruses in poultry from southern China, 2000 to 2005. J Virol. 2007;81(19):10389-401.  https://doi.org/10.1128/JVI.00979-07  PMID: 17652402 
  137. Zhu Y, Yang Y, Liu W, Liu X, Yang D, Sun Z, et al. Comparison of biological characteristics of H9N2 avian influenza viruses isolated from different hosts. Arch Virol. 2015;160(4):917-27.  https://doi.org/10.1007/s00705-015-2337-y  PMID: 25616845 
  138. Cong YL, Pu J, Liu QF, Wang S, Zhang GZ, Zhang XL, et al. Antigenic and genetic characterization of H9N2 swine influenza viruses in China. J Gen Virol. 2007;88(Pt 7):2035-41.  https://doi.org/10.1099/vir.0.82783-0  PMID: 17554038 
  139. Sun X, Xu X, Liu Q, Liang D, Li C, He Q, et al. Evidence of avian-like H9N2 influenza A virus among dogs in Guangxi, China. Infect Genet Evol. 2013;20:471-5.  https://doi.org/10.1016/j.meegid.2013.10.012  PMID: 24161411 
  140. Chen H, Yuan H, Gao R, Zhang J, Wang D, Xiong Y, et al. Clinical and epidemiological characteristics of a fatal case of avian influenza A H10N8 virus infection: a descriptive study. Lancet. 2014;383(9918):714-21.  https://doi.org/10.1016/S0140-6736(14)60111-2  PMID: 24507376 
  141. Gao R, Cao B, Hu Y, Feng Z, Wang D, Hu W, et al. Human infection with a novel avian-origin influenza A (H7N9) virus. N Engl J Med. 2013;368(20):1888-97.  https://doi.org/10.1056/NEJMoa1304459  PMID: 23577628 
  142. Guan Y, Shortridge KF, Krauss S, Webster RG. Molecular characterization of H9N2 influenza viruses: were they the donors of the "internal" genes of H5N1 viruses in Hong Kong? Proc Natl Acad Sci USA. 1999;96(16):9363-7.  https://doi.org/10.1073/pnas.96.16.9363  PMID: 10430948 
  143. Wei SH, Yang JR, Wu HS, Chang MC, Lin JS, Lin CY, et al. Human infection with avian influenza A H6N1 virus: an epidemiological analysis. Lancet Respir Med. 2013;1(10):771-8.  https://doi.org/10.1016/S2213-2600(13)70221-2  PMID: 24461756 
  144. Pepin KM, Wang J, Webb CT, Smith GJ, Poss M, Hudson PJ, et al. Multiannual patterns of influenza A transmission in Chinese live bird market systems. Influenza Other Respi Viruses. 2013;7(1):97-107.  https://doi.org/10.1111/j.1750-2659.2012.00354.x  PMID: 22458429 
  145. Jiao P, Cao L, Yuan R, Wei L, Song Y, Shen D, et al. Complete genome sequence of an H10N8 avian influenza virus isolated from a live bird market in Southern China. J Virol. 2012;86(14):7716.  https://doi.org/10.1128/JVI.00959-12  PMID: 22733881 
  146. Pavade G, Weber‐Vintzel L, Hamilton K, Dehove A, Zepeda C. OFFLU review of avian influenza surveillance and epidemiological projects in some European, African, and Asian countries. OIE/FAO Network of Expertise on Animal Influenza (OFFLU). 2011:11.
  147. Von Dobschuetz S, DE Nardi M, Harris KA, Munoz O, Breed AC, Wieland B, et al. FLURISK Consortium. Influenza surveillance in animals: what is our capacity to detect emerging influenza viruses with zoonotic potential? Epidemiol Infect. 2015;143(10):2187-204.  https://doi.org/10.1017/S0950268814002106  PMID: 25268692 
Weighing serological evidence of human exposure to animal influenza viruses − a literature review
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Reina+Saapke+Sikkema&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Sikkema Reina Saapke</a>, <a href="/search?value1=Gudrun+Stephanie+Freidl&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Freidl Gudrun Stephanie</a>, <a href="/search?value1=Erwin+de+Bruin&option1=author&noRedirect=true" class="nonDisambigAuthorLink">de Bruin Erwin</a>, <a href="/search?value1=Marion+Koopmans&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Koopmans Marion</a></span>. Weighing serological evidence of human exposure to animal influenza viruses − a literature review. <a href="/content/ecdc">Euro Surveill.</a> 2016;21(44):pii=30388. <a href="https://doi.org/10.2807/1560-7917.ES.2016.21.44.30388" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2016.21.44.30388</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 13 Nov 2015;&nbsp;&nbsp; <span class="generated">Accepted</span>: 30 Mar 2016 </span> </p>
/content/10.2807/1560-7917.ES.2016.21.44.30388
/content/10.2807/1560-7917.ES.2016.21.44.30388
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