Live bird markets as evolutionary epicentres of H9N2 low pathogenicity avian influenza viruses in Korea

Live bird markets (LBMs) in Korea have been recognized as a reservoir, amplifier, and source of avian influenza viruses (AIVs); however, little was known about the role of LBMs in the epidemiology of AIVs in Korea until recently. Through 10 years of surveillance (2006–2016) we have isolated and sequenced H9N2 viruses in Korean LBMs. To understand how H9N2 evolves and spreads in Korea, a statistical Bayesian phylogenetic model was used. Phylogenetic analysis suggests that three separate introductions of progenitor gene pools, Korean domestic duck-origin and two wild aquatic bird-origin AIVs, contributed to the generation of the five genotypes of H9N2 viruses in Korea. Phylogenetic reconstruction of ecological states infer that the LBMs are where chickens become infected with the virus, with domestic ducks playing a major role in the transmission and evolution of the H9N2 viruses. Three increases in the genetic diversity of H9N2 viruses were observed and coincided with transitions in host species and the locations (domestic farm, LBM, slaughterhouse, and wild aquatic bird habitat) where the viruses were isolated, accompanying genetic reassortment. Following the introduction of a wild aquatic bird-origin AIVs in 2008, six genes of the Korean lineage H9N2 virus were replaced with genes originating from wild aquatic birds, and viruses with this new genotype became predominant in Korean LBMs.

韩国的活禽市场（Live bird markets, LBMs）已被证实是禽流感病毒（Avian Influenza Viruses, AIVs）的储存库、扩增宿主与传播源头；然而直至近年，学界对韩国活禽市场在禽流感病毒流行病学中所扮演的角色仍知之甚少。本研究通过2006至2016年长达十年的监测工作，从韩国活禽市场中分离并测序得到H9N2亚型病毒。为解析H9N2病毒在韩国境内的演化与传播路径，研究采用了贝叶斯系统发育统计模型。系统发育分析结果显示，共有三支独立引入的祖先基因库参与了韩国境内H9N2病毒五种基因型的形成，其来源分别为韩国家鸭源性以及两株野生水鸟源性的禽流感病毒。生态状态的系统发育重建结果表明，活禽市场是鸡群感染该病毒的主要场所，而家鸭在H9N2病毒的传播与演化过程中发挥了核心作用。研究共观测到H9N2病毒遗传多样性的三次显著提升，其时间节点与病毒分离时的宿主种类、分离位点（家养农场、活禽市场、屠宰场及野生水鸟栖息地）的转变相吻合，且伴随基因重配事件。2008年一株野生水鸟源性禽流感病毒引入后，韩国谱系H9N2病毒的六个基因片段被替换为野生水鸟来源的对应基因，携带该新型基因型的病毒随即成为韩国活禽市场中的优势流行毒株。