A Systematic Review and Meta-Analysis of the Seroprevalence of Influenza A(H9N2) Infection Among Humans
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INTRODUCTION: Given that influenza A(H9N2) is recognized as a pandemic threat, we evaluated the overall burden of influenza A(H9N2) infections among avian-exposed human populations. METHODS: We performed a systematic search of PubMed, AGRICOLA, and CAB Abstracts databases for literature published during 1997-2013. Studies reporting serological evidence of human influenza A(H9N2) infection among avian-exposed populations were included. We used a World Health Organization (WHO)-recommended case definition for serological evidence of infection based on results of hemagglutination inhibition (HI) and microneutralization (MN) assays. We calculated overall seroprevalence through a random effects meta-analysis model. RESULTS: Seroprevalence data reported by the studies ranged from 1% to 43% (median, 9%) by HI, which was not significantly different from the seroprevalence estimated through the WHO-recommended case definition (median, 1.3%; range, 0.5%-42.6%). Reported seroprevalence by MN ranged from 0.6% to 9% (median, 2.7%), which was greater than the seroprevalence estimated through the WHO-recommended case definition (median, 0.3%; range, 0.1%-1.4%). CONCLUSIONS: A small proportion of avian-exposed humans had evidence of influenza A(H9N2) infection. As the virus has a near global distribution in poultry, it seems likely that present surveillance efforts are missing mild or asymptomatic infections among avian-exposed persons. It seems prudent to closely monitor avian-exposed populations for influenza A(H9N2) infection to provide prepandemic warnings.
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Given the rarity of H9, H6 and H10 human infections, the binding antibodies likely represent heterosubtypic immunity elicited by vaccination or exposure to other influenza A subtypes.
“Given the rarity of H9, H6 and H10 human infections23–25 it is likely the binding antibodies represent heterosubtypic immunity elicited by vaccination or exposure to other influenza A subtypes.”
From Clade 2.3.4.4b but not historical clade 1 HA replicating RNA vaccine protects against bovine H5N1 challenge in mice (2025) · cites this paper as [23]
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Cites
Preferred Reporting Items for Systematic Reviews and Meta-Analyses: the PRISMA statement
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & for the PRISMA Group (2009) · BMJ · doi:10.1136/bmj.b2535 · Cited by 83,823 · see citing works
Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & The PRISMA Group (2009) · PLoS Medicine · doi:10.1371/journal.pmed.1000097 · Cited by 64,042 · see citing works
Measuring inconsistency in meta-analyses
Higgins, J. P. T., Thompson, S. G., Deeks, J. J., & Altman, D. G. (2003) · BMJ · doi:10.1136/bmj.327.7414.557 · Cited by 63,139 · see citing works
Preferred reporting items for systematic reviews and meta-analyses: the PRISMA Statement.
(2009) · PubMed Central · Cited by 44,859 · see citing works
Wang, G., Ma, R., Qiao, G., Wada, K., Aizawa, Y., & Satoh, T. (2015) · Integrative Medicine International · doi:10.1159/000368408 · Cited by 18,762 · see citing works
Evaluation of the Quality of Prognosis Studies in Systematic Reviews
Hayden, J. A., Côté, P., & Bombardier, C. (2006) · Annals of Internal Medicine · doi:10.7326/0003-4819-144-6-200603210-00010 · Cited by 1,452 · see citing works
Human infection with influenza H9N2
Peiris, M. J. S., Yuen, K., Leung, C., et al. (1999) · The Lancet · doi:10.1016/s0140-6736(99)03311-5 · Cited by 1,035 · see citing works
Rowe, T., Abernathy, R. A., Hu‐Primmer, J., Thompson, W., Lu, X., Lim, W., Fukuda, K., Cox, N. J., & Katz, J. M. (1999) · Journal of Clinical Microbiology · doi:10.1128/jcm.37.4.937-943.1999 · Cited by 812 · see citing works
Guan, Y., Shortridge, K. F., Krauss, S. L., et al. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.16.9363 · Cited by 738 · see citing works
Chen, H., Yuan, H., Gao, R., Zhang, J., Wang, D., Xiong, Y., Fan, G., Yang, F., Li, X., Zhou, J., et al. (2014) · The Lancet · doi:10.1016/s0140-6736(14)60111-2 · Cited by 648 · see citing works
Liu, D., Shi, W., Shi, Y., et al. (2013) · The Lancet · doi:10.1016/s0140-6736(13)60938-1 · Cited by 554 · see citing works
The genesis and source of the H7N9 influenza viruses causing human infections in China
Lam, T. T., Wang, J., Shen, Y., Zhou, B., Duan, L., Cheung, C.-L., Ma, C., Lycett, S., Leung, C. Y. H., Chen, X., et al. (2013) · Nature · doi:10.1038/nature12515 · Cited by 465 · see citing works
Guo, Y. J., Krauss, S. L., Senne, D. A., et al. (2000) · Virology · doi:10.1006/viro.1999.0115 · Cited by 463 · see citing works
Li, K., Xu, K., Peiris, M. J. S., Poon, L. L. M., Yu, K. Z., Yuen, K., Shortridge, K. F., Webster, R. G., & Guan, Y. (2003) · Journal of Virology · doi:10.1128/jvi.77.12.6988-6994.2003 · Cited by 256 · see citing works
[Discovery of men infected by avian influenza A (H9N2) virus].
Guo, Y., Li, J., & Cheng, X. (1999) · PubMed · Cited by 222 · see citing works
Iqbal, M., Yaqub, T., Reddy, K., & McCauley, J. W. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005788 · Cited by 181 · see citing works
Infection Due to 3 Avian Influenza Subtypes in United States Veterinarians
Myers, K. P., Setterquist, S. F., Capuano, A. W., et al. (2007) · Clinical Infectious Diseases · doi:10.1086/518579 · Cited by 127 · see citing works
Antibodies against H5 and H9 Avian Influenza among Poultry Workers in China
Wang, M., Fu, C.-X., & Zheng, B. (2009) · New England Journal of Medicine · doi:10.1056/nejmc0900358 · Cited by 124 · see citing works
Avian influenza viruses in humans
Peiris, M. J. S. (2009) · Scientific and Technical Review (World Organisation for Animal Health) · doi:10.20506/rst.28.1.1871 · Cited by 117 · see citing works
DECLINING T-CELL IMMUNITY TO INFLUENZA, 1977-82
McMichael, A. J., Dongworth, D. W., Gotch, F., et al. (1983) · The Lancet · doi:10.1016/s0140-6736(83)92297-3 · Cited by 110 · see citing works
Infection of immunocompromised patients by avian H9N2 influenza A virus
Cheng, V. C., Chan, J. F., Wen, X., et al. (2011) · Journal of Infection · doi:10.1016/j.jinf.2011.02.007 · Cited by 105 · see citing works
Uyeki, T. M., Chong, Y.-H., Katz, J. M., et al. (2002) · Emerging infectious diseases · doi:10.3201/eid0802.010148 · Cited by 103 · see citing works
Kinetics of Neutralizing Antibodies in Patients Naturally Infected by H5N1 Virus
Buchy, P., Vong, S., Chu, S., Garcia, J., Hien, T. T., Hien, V. M., Mey, C., Ha, D. Q., Châu, N. V. V., Simmons, C. P., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010864 · Cited by 101 · see citing works
Evidence of Previous Avian Influenza Infection among US Turkey Workers
Kayali, G., Ortiz, E. J., Chorazy, M. L., et al. (2009) · Zoonoses and Public Health · doi:10.1111/j.1863-2378.2009.01231.x · Cited by 91 · see citing works
Avian Influenza H9N2 Seroprevalence among Poultry Workers in Pune, India, 2010
Pawar, S. D., Tandale, B. V., Raut, C. G., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036374 · Cited by 88 · see citing works
Evidence for Subclinical Avian Influenza Virus Infections Among Rural Thai Villagers
Khuntirat, B., Yoon, I., Blair, P. J., et al. (2011) · Clinical Infectious Diseases · doi:10.1093/cid/cir525 · Cited by 73 · see citing works
Uyeki, T. M., Nguyen, D. C., Rowe, T., Lu, X., Hu‐Primmer, J., Huynh, L. P. T., Hằng, N. L. K., & Katz, J. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0043948 · Cited by 72 · see citing works
Seroprevalence of avian influenza H9N2 among poultry workers in Shandong Province, China
Huang, R., Wang, A.-R., Liu, Z.-H., et al. (2013) · European Journal of Clinical Microbiology & Infectious Diseases · doi:10.1007/s10096-013-1888-7 · Cited by 65 · see citing works
Evidence for avian influenza A infections among Iowa’s agricultural workers
Gray, G. C., McCarthy, T. A., Capuano, A. W., et al. (2008) · Influenza and Other Respiratory Viruses · doi:10.1111/j.1750-2659.2008.00041.x · Cited by 61 · see citing works
Self-citationEvidence for avian H9N2 influenza virus infections among rural villagers in Cambodia
Blair, P. J., Putnam, S. D., Krueger, W. S., et al. (2013) · Journal of Infection and Public Health · doi:10.1016/j.jiph.2012.11.005 · Cited by 55 · see citing works
Potential infections of H5N1 and H9N2 avian influenza do exist in Guangdong populations of China
Lu, C., Lu, J., Chen, W., et al. (2008) · Chinese Medical Journal · doi:10.1097/00029330-200810020-00020 · Cited by 53 · see citing works
Serological reports of human infections of H7 and H9 avian influenza viruses in northern China
Jia, N., de Vlas, S. J., Liu, Y., et al. (2009) · Journal of Clinical Virology · doi:10.1016/j.jcv.2008.12.014 · Cited by 48 · see citing works
Shelton, H. A., Ayora‐Talavera, G., Ren, J., et al. (2010) · Journal of Virology · doi:10.1128/jvi.01822-10 · Cited by 48 · see citing works
Garcia, J., Pépin, S., Lagarde, N., Ma, E. S. K., Vogel, F. R., Chan, K. H., Chiu, S. S. S., & Peiris, M. J. S. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007918 · Cited by 46 · see citing works
Serological evidence for avian H9N2 influenza virus infections among Romanian agriculture workers
Coman, A., Maftei, D. N., Krueger, W. S., et al. (2013) · Journal of Infection and Public Health · doi:10.1016/j.jiph.2013.05.003 · Cited by 42 · see citing works
Powell, T. J., Fox, A., Peng, Y., Mai, L. T. Q., Lien, V. T. K., Hằng, N. L. K., Wang, L., Lee, L. Y.-H., Simmons, C. P., McMichael, A. J., et al. (2011) · The Journal of Infectious Diseases · doi:10.1093/infdis/jir689 · Cited by 41 · see citing works
Bangladesh (2011) · Cited by 41 · see citing works
Yang, P., Ma, C., Shi, W., Cui, S., Lu, G., Peng, X., Zhang, D., Liu, Y., Liang, H., Zhang, Y., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0050770 · Cited by 40 · see citing works
A national study of US bird banders for evidence of avian influenza virus infections
Gray, G. C., Ferguson, D. D., Lowther, P. E., et al. (2011) · Journal of Clinical Virology · doi:10.1016/j.jcv.2011.03.011 · Cited by 39 · see citing works
Self-citationSerologic evidence of avian influenza virus infections among Nigerian agricultural workers
Okoye, J. O. A., Eze, D. C., Krueger, W. S., et al. (2013) · Journal of Medical Virology · doi:10.1002/jmv.23520 · Cited by 35 · see citing works
Bashashati, M., Marandi, M. V., & Sabouri, F. (2013) · Archives of Virology · doi:10.1007/s00705-013-1699-2 · Cited by 31 · see citing works
Epidemic Enhancement in Partially Immune Populations
Pulliam, J. R. C., Dushoff, J. G., Levin, S. A., et al. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000165 · Cited by 26 · see citing works
Ahad, A., Rabbani, M., Yaqub, T., et al. (2013) · Pakistan Veterinary Journal · Cited by 22 · see citing works
Prospective Study of Avian Influenza Virus Infections among Rural Thai Villagers
Krueger, W. S., Khuntirat, B., Yoon, I., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0072196 · Cited by 20 · see citing works
Avian influenza (H9N2) among poultry workers in Iran.
Alizadeh, E., Hosseini, S. M., Kheyri, M., et al. (2009) · Cited by 19 · see citing works
Ahad, M. R. A. (2013) · DOAJ (DOAJ: Directory of Open Access Journals) · Cited by 19 · see citing works
Cheng, X., Liu, J., He, J., et al. (2002) · PubMed · Cited by 18 · see citing works
Chen, Y., Zheng, Q., Yang, K., et al. (2011) · Clinical Microbiology and Infection · doi:10.1111/j.1469-0691.2011.03538.x · Cited by 17 · see citing works
Chuan-hua, L., Zhou, X., & Li, M. (2004) · PubMed · Cited by 16 · see citing works
Anvar, E., Hosseini, S. M., Kheiri, M. T., et al. (2013) · Jundishapur Journal of Microbiology · doi:10.5812/jjm.5441 · Cited by 12 · see citing works
Leibler, J. H., Silbergeld, E. K., Pekosz, A. S., et al. (2010) · Journal of Agromedicine · doi:10.1080/1059924x.2011.533612 · Cited by 11 · see citing works
[Avian influenza virus infection in people occupied in poultry fields in Guangzhou city].
Liu, Y., Lu, E., Wang, Y., et al. (2009) · PubMed · Cited by 11 · see citing works
Lv, X., Jiang, C.-Y., & Zhou, Y. (2009) · PubMed · Cited by 3 · see citing works
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- Liu Xing Bing Xue Za Zhi 2009; 30:1111-3.
- Influenza A(H9N2) in Humans: Systematic Review • JID 2015:212 (15 August) • 569 Downloaded from https://academic.oup.com/jid/article/212/4/562/820084 by guest on 30 August 2023
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Hawman, D. W., Tipih, T., Hodge, E., Stone, E. T., Warner, N., McCarthy, N., Granger, B., Meade-White, K., Leventhal, S., Hatzakis, K., et al. (2025) · Nature Communications · doi:10.1038/s41467-024-55546-7 · Cited by 20 · see citing works
- Authors
- Khan, S. U., Anderson, B. D., Heil, G. L., Liang, S., & Gray, G. C.
- Affiliations
- University of Florida Health (US)
- National University of Singapore (SG)
- Corresponding author
- Khan, Salah Uddin
- Venue
- Journal of Infectious Diseases
- Publisher
- Oxford University Press (OUP)
- Published
- 2015-02-23
- Volume
- 212
- Issue
- 4
- Pages
- 562-569
- ISSN
- 0022-1899 (ISSN-L)
- 1537-6613
- PMC
- PMC4598807
- OpenAlex
- W2168554389
- Cited by
- 88
- References
- 53
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 4 · 2023: 4 · 2022: 3 · 2021: 9 · 2020: 12 · 2019: 12 · 2018: 14 · 2017: 13 · 2016: 7 · 2015: 3
- FWCI
- 1.60
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Journal of Infectious Diseases (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Department of Defense
- National Institute of Allergy and Infectious Diseases (R01AI108993)
- Topics
- Health Sciences › Medicine › Epidemiology › Influenza Virus Research Studies
- Health Sciences › Medicine › Epidemiology › Virology and Viral Diseases
- Health Sciences › Medicine › Epidemiology › Respiratory viral infections research
- Keywords
- seroprevalence, human influenza infection, hemagglutination inhibition test, microneutralization, WHO case definition, asymptomatic infection, pandemic preparedness, surveillance (medicine)
- MeSH terms
- Animals, Antibodies, Viral, Humans, Influenza, Human, Zoonoses, Seroepidemiologic Studies, Influenza A Virus, H9N2 Subtype
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