Avian Influenza A Viruses among Occupationally Exposed Populations, China, 2014-2016

Abstract

To determine the seroprevalence and seroconversion of avian influenza virus (AIV) antibodies in poultry workers, we conducted a seroepidemiologic study in 7 areas of China during December 2014-April 2016. We used viral isolation and reverse transcription PCR to detect AIVs in specimens from live poultry markets. We analyzed 2,124 serum samples obtained from 1,407 poultry workers by using hemagglutination inhibition and microneutralization assays. We noted seroprevalence of AIV antibodies for subtypes H9N2, H7N9, H6N1, H5N1-SC29, H5N6, H5N1-SH199, and H6N6. In serum from participants with longitudinal samples, we noted seroconversion, with >4-fold rise in titers, for H9N2, H7N9, H6N1, H5N1-SC29, H6N6, H5N6, and H5N1-SH199 subtypes. We found no evidence of H10N8 subtype. The distribution of AIV antibodies provided evidence of asymptomatic infection. We found that AIV antibody prevalence in live poultry markets correlated with increased risk for H7N9 and H9N2 infection among poultry workers.

Keywords: China; avian influenza virus; influenza; influenza A; occupational health; poultry worker; respiratory infections; seroepidemiology; seroprevalence; viruses; zoonoses.

Figure 1

Temporal and spatial distribution of human infections with avian influenza A virus subtypes before and during serosurveillance, China. A) Geographic distribution of avian influenza A(H7N9) virus infection among humans in China during May 1997–October 2016. The number of case-patients in each province is based on data published by the World Health Organization and the National Health (https://www.who.int/influenza/human_animal_interface/avian_influenza/archive/en/) and Family Planning Commission of the Republic of China (http://www.nhc.gov.cn/jkj/s2907/new_list.shtml?tdsourcetag=s_pcqq_aiomsg). Density of shading represents the number of reported avian influenza H7N9 cases in humans in each province. Cases of other AIV subtype infections are represented by other symbols. B) Density of live poultry markets per 10,000 persons in each province included in the study, from data collected during 2013–2014. Red flags indicate locations of poultry markets selected for the serosurveillance study. C) Distribution of biweekly cases of human H7N9 infection before and during serosurveillance study. Orange bars indicate the number of biweekly cases of human H7N9 infection. Dashed lines indicate initial survey and follow-up dates for serosurveys, which were conducted before and after the third and fourth wave H7N9 epidemics. Reported cases of H5N1, H5N6, H6N1, H9N2, and H10N8 infection are noted with symbols as in panel A. AIV, avian influenza virus.

Figure 2

Flowchart of initial participant enrollment and follow-up distribution in 7 areas of China in a study of avian influenza virus seroprevalence during December 2014–April 2016.

Figure 3

Avian influenza virus seroprevalence in the studied regions of China during December 2014–April 2016. A) Geographic areas included for serosurveillance: 1 municipality, Shanghai, and 6 provinces, Guangdong, Henan, Jiangsu, Jiangxi, Shandong, and Sichuan. B) Seroprevalence against avian influenza A virus subtypes in 4 cross-sectional surveys. Colors on map correspond to colors in bar graphs. *Seasonal influenza virus subtype.

Figure 4

Seroconversion and persistent positivity for avian influenza virus (AIV) A subtypes based on HI titers in a cohort study in China during December 2014–April 2016. Each dot and line connection represents 1 participant. Red dashed lines represent positive cutoff for the HI titers; HI–positive samples were confirmed by a microneutralization assay. A) Comparison of paired samples from participants during 2 surveillance periods showing seroconversion for 6 AIV subtypes. Weighted lines and dots represent participants with seroconversion. B) Number of participants with >2 positive sample who were persistently seropositive for 6 AIV subtypes. Weighted lines and dots represent number of participants with seropositivity. C) Antibody titers of representative participants with >1 positive sample in the 4 serosurveys. HI, hemagglutinin inhibition.