Seropositivity for avian influenza H6 virus among humans, China.
During 2009-2011, a total of 15,689 serum samples were collected from live poultry market workers, backyard poultry farmers, large-scale poultry farmers, poultry-slaughter factory workers, and wild bird habitat workers in 22 provinces in mainland China. A/chicken/Y94/ Guangdong/2011 (H6N2), a representative isolate of predominant H6 viruses in mainland China, was used for the serologic testing (online Technical Appendix Table 1, Figures 1, 2, http://wwwnc.cdc.gov/EID/article/21/7/15-0135Techapp1.pdf). Hemagglutination inhibition (HI) assay was performed for all serum samples, and samples with an HI titer [greater than or equal to] 20 were verified by a microneutralization (MN) assay, as indicated by World Health Organization guidelines (8). An MN result of [greater than or equal to] 20 was considered positive.
The HI result was [greater than or equal to] 20 for H6N2 virus in 298 of the 15,689 specimens, and the MN result was positive in 63 of the 298 specimens (overall seropositivity range 20-320, mean 32.7, 0.4%) (online Technical Appendix Table 2). The proportion of group members who were seropositive differed significantly according to occupational exposure (p = 0.0125). Seropositivity was highest among workers in live poultry markets, backyard poultry farmers, and workers in wild bird habitats (0.66%, 0.42%, and 0.51%, respectively) (Table). According to [chi square] test results, seropositivity among workers in live poultry markets was significantly higher than that among large-scale poultry farmers (p = 0.0015, adjusted [alpha] = 0.005. Analysis by unconditional logistic regression model showed that exposure to live poultry markets was a risk factor for human infection with avian influenza H6 virus (odds ratio 2.1, 95% CI 1.27-3.47).
Seropositivity did not differ significantly among male and female persons tested (p = 0.08) (Table). No children were positive for the H6N2 virus. For other age groups, seropositivity ranged from 0.25% to 0.45%, but differences were not significant (p > 0.05) (Table).
Of the 22 provinces from which serum specimens were collected, 11 were northern provinces and 11 were southern provinces. Positive specimens were detected in all southern provinces. In northern China, no seropositive results were detected in Henan, Liaoning, or Jilin Provinces. According to [chi square] test results, seropositivity in southern China was significantly higher than seropositivity in northern China (p = 0.0375) (Table).
Human infection with influenza H6 virus in mainland China has not been reported, but 63 serum specimens tested in our study were positive for the H6 virus. This level of seropositivity is much higher than that for highly pathogenic avian influenza A(H5N1) virus, for which only 2 of the serum specimens we tested were positive (data not shown), but much lower than the seropositivity level for low pathogenicity avian influenza A(H9N2) virus; 3.4% of the samples tested were positive for A/Chicken/Hong Kong/ G9/1997(H9N2)-like virus (data not shown). A previous US study has reported H6N2-positive antibodies in veterinarians (9). Our results and the veterinarian study indicate that the H6N2 virus could infect humans.
In our study, positive samples were detected in 19 of 22 provinces and in all tested worker populations, suggesting that the H6 virus has been broadly circulating in birds in China. Live poultry market exposure is the major risk factor for human infection with avian influenza H6 virus. The limitation of this study is that antigen selection may not accurately detect neutralization antibodies for different subtypes of H6 viruses. Surveillance of the H6 virus in birds and occupationally exposed populations should be strengthened for pandemic preparedness.
This study was performed under the serology surveillance system of occupationally exposed populations in China. We are deeply thankful for the contributions of all National Influenza Surveillance Network members, including the China Centers for Disease Control and Prevention in the provinces and in the prefects, all of which collected samples for years. We also thank Ms. Qiao-hong Liao for providing consultation on statistical analysis.
This study was supported in part by the China-United States cooperation project "Developing sustainable influenza surveillance networks and response to avian and pandemic influenza in China" and by the China National Mega-projects for Infectious Diseases (2014ZX10004002).
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Li Xin, Tian Bai, Jian Fang Zhou, Yong Kun Chen, Xiao Dan Li, Wen Fei Zhu, Yan Li, Jing Tang, Tao Chen, Kun Qin, Jing Hong Shi, Rong Bao Gao, Da Yan Wang, Ji Ming Chen, Yue Long Shu
Author affiliations: National Institute of Viral Disease Control and Prevention, Beijing, China (L. Xin, T. Bai, J.F. Zhou, Y.K. Chen, X.D. Li, W.F. Zhu, Y Li, J. Tang, T Chen, K. Qin, J.H. Shi, R.B. Gao, D.Y. Wang, Y.L. Shu); China Animal Health and Epidemiology Center, Qingdao, China (J.M. Chen)
Address for correspondence: Yue Long SHU, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Key Laboratory for Medical Virology, Ministry of Health, Beijing, 102206, China; email: firstname.lastname@example.org
Table. Seropositivity of occupationally exposed populations for the influenza (H6N2) virus, China, 2009-2011 * Population Total no. Mean titer for serum MN [greater than samples or equal to] 20 Total 15,689 32.70 Occupation Live poultry market 3,950 43.08 Poultry farm 3,762 25.71 Backyard poultry farm 4,324 26.67 Poultry slaughter factory 1,235 30.00 Wild bird habitat 788 20.00 Other 1,630 23.33 Sex F 7,620 24.29 M 8,069 39.39 Age group, y Children, [less than or equal to] 14 74 -- Youth, 15-24 1,168 20.00 Adult, 25-59 1,2450 34.07 Elderly, [greter than or equal to] 60 1,748 13.33 No age record 249 -- Geographic distribution South 10,522 32.00 North 5,167 35.38 Population No. serum samples with MN [greater than or equal to]20 Total 63 Occupation Live poultry market 26 Poultry farm 7 Backyard poultry farm 18 Poultry slaughter factory 2 Wild bird habitat 4 Other 6 Sex F 28 M 35 Age group, y Children, [less than or equal to] 14 0 Youth, 15-24 3 Adult, 25-59 54 Elderly, [greter than or equal to] 60 6 No age record 0 Geographic distribution South 50 North 13 Population Seropositivity (95% CI) Total 0.40 (0.40-0.41) Occupation Live poultry market 0.66 (0.64-0.68) Poultry farm 0.19 (0.18-0.19) Backyard poultry farm 0.42 (0.40-0.43) Poultry slaughter factory 0.16 (0.15-0.17) Wild bird habitat 0.51 (0.47-0.54) Other 0.37 (0.35-0.39) Sex F 0.37 (0.36-0.38) M 0.43 (0.42-0.44) Age group, y Children, [less than or equal to] 14 0 Youth, 15-24 0.26 (0.24-0.27) Adult, 25-59 0.43 (0.43-0.44) Elderly, [greter than or equal to] 60 0.34 (0.33-0.36) No age record 0 Geographic distribution South 0.48 (0.47-0.48) North 0.25 (0.24-0.26) Population Odds ratiof (95% CI) Total Occupation Live poultry market 2.10 (1.27-3.47) Poultry farm 0.40 (0.18-0.87) Backyard poultry farm 1.05 (0.61-1.82) Poultry slaughter factory 0.38 (0.09-1.57) Wild bird habitat 1.28 (0.47-3.54) Other 0.91 (0.39-2.11) Sex F Reference M 1.18 (0.72-1.94) Age group, y Children, [less than or equal to] 14 0 (0) Youth, 15-24 0.75 (0.19-3.00) Adult, 25-59 1.27 (0.54-2.94) Elderly, [greter than or equal to] 60 Reference No age record -- Geographic distribution South Reference North 0.59 (0.30-1.15) * MN, microneutralization; --, not applicable. ([dagger]) Odds ratios were calculated by using unconditional logistic regression model (SPSS 17.0, Armonk, NY, USA).
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|Author:||Xin, Li; Bai, Tian; Zhou, Jian Fang; Chen, Yong Kun; Li, Xiao Dan; Zhu, Wen Fei; Li, Yan; Tang, Jing|
|Publication:||Emerging Infectious Diseases|
|Date:||Jul 1, 2015|
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