Epidemiological, phylogenetic, and pathogenicity analysis of H4 subtype avian influenza viruses in China, 2011-2022

Qiuyan Mao; Junfeng Zhu; Shuo Liu; Cheng Peng; Tiantian Wu; Jie Tian; Xiaoqi Li; Jizhe Yang; Jinping Li; Guangyu Hou; Wenming Jiang; Hualei Liu

doi:10.1016/j.virs.2025.09.005

October 2025

Qiuyan Mao, Junfeng Zhu, Shuo Liu, Cheng Peng, Tiantian Wu, Jie Tian, Xiaoqi Li, Jizhe Yang, Jinping Li, Guangyu Hou, Wenming Jiang and Hualei Liu. Epidemiological, phylogenetic, and pathogenicity analysis of H4 subtype avian influenza viruses in China, 2011-2022[J]. Virologica Sinica, 2025, 40(5): 722-734. doi: 10.1016/j.virs.2025.09.005

Citation: Qiuyan Mao, Junfeng Zhu, Shuo Liu, Cheng Peng, Tiantian Wu, Jie Tian, Xiaoqi Li, Jizhe Yang, Jinping Li, Guangyu Hou, Wenming Jiang, Hualei Liu. Epidemiological, phylogenetic, and pathogenicity analysis of H4 subtype avian influenza viruses in China, 2011-2022 .VIROLOGICA SINICA, 2025, 40(5) : 722-734. http://dx.doi.org/10.1016/j.virs.2025.09.005

2011-2022年中国H4亚型禽流感病毒的流行病学、遗传进化及致病性分析

毛秋艳 ^a ,
朱峻锋 ^b ,
刘朔 ^a ,
彭程 ^a ,
吴恬恬 ^c ,
田杰 ^a ,
李晓奇 ^a ,
杨吉喆 ^a ,
李金平 ^a ,
侯广宇 ^a ,
蒋文明 ^a,, ,
刘华雷 ^a,,

a 中国动物卫生与流行病学中心;
b. 中国兽医药品监察所;
c. 北京市房山区农业技术综合服务中心

通讯作者： 蒋文明, civcul@163.com; 刘华雷, liuhualei@cahec.cn
收稿日期： 2025-05-07
录用日期： 2025-09-19

摘要

H4亚型禽流感病毒在全球范围内广泛流行，常因对家禽的致病性较低而缺乏关注。因此，对于H4亚型AIV是否会对家禽养殖业及人类公共卫生安全构成潜在性的威胁在很大程度上也是未知的。在2011-2022年期间，我们通过主动监测从各省采集的154762份拭子样本中检测到了427株H4病毒，阳性率为0.28%。所有H4病毒都是从家禽中分离出来的，主要来自活家禽市场上的鸭子。随后，本研究对H4亚型AIV在中国的流行现状及筛选出的20种H4Nx病毒的遗传进化特点及致病性进行了系统性地分析。系统发育分析表明，在2011-2022年分离到的20种具有代表性的H4病毒的八条基因片段均属于欧亚谱系，因经历复杂而频繁的重组而形成了19个基因型（G1-G19）。分子特征分析显示所有病毒含有增强与人源受体结合相关的突变，说明可能具备双受体结合的特性。同时部分病毒中存在多个潜在的哺乳动物适应性分子标记。动物感染性试验表明，H4病毒对鸭无致病性或致病性较低，仅能在少数鸭的口咽部或泄殖腔拭子中检测到病毒脱落。值得注意的是，一些病毒未经提前适应就可在小鼠的肺脏和鼻甲中有效复制，并引起感染小鼠的体重下降，其中DK/AH/AG61/11(H4N6)可在MDCK细胞中有效复制，具备感染哺乳动物的潜在风险。这些结果强调了加强对我国家禽中H4亚型AIV持续监测的必要性，为进一步了解病毒的生物学特性提供宝贵的数据资源。
- H4亚型禽流感病毒
- , 流行病学
- , 系统发育学
- , 致病性
- , 鸭
- , 小鼠

Epidemiological, phylogenetic, and pathogenicity analysis of H4 subtype avian influenza viruses in China, 2011-2022

Qiuyan Mao ^a ,
Junfeng Zhu ^b ,
Shuo Liu ^a ,
Cheng Peng ^a ,
Tiantian Wu ^c ,
Jie Tian ^a ,
Xiaoqi Li ^a ,
Jizhe Yang ^a ,
Jinping Li ^a ,
Guangyu Hou ^a ,
Wenming Jiang ^a,, ,
Hualei Liu ^a,,

a. Avian Diseases Surveillance Laboratory, China Animal Health and Epidemiology Center, Qingdao 266032, China;
b. China Institute of Veterinary Drug Control, Beijing 100081, China;
c. Agricultural Technology Comprehensive Service Center of Fangshan District, Beijing 102488, China

Corresponding author: Wenming Jiang, civcul@163.com Hualei Liu, liuhualei@cahec.cn
Received Date: 07 May 2025
Accepted Date: 19 September 2025

Abstract

The H4 subtype of avian influenza virus (AIV) is prevalent worldwide, but only receives little attention due to its low pathogenicity in poultry. Consequently, it remains largely unclear whether H4 AIVs pose a potential threat to the poultry industry and public health. During the period from 2011 to 2022, we conducted an active surveillance programm. A total of 154,762 swab samples were collected across various provinces, and 427 H4 viruses were detected, resulting in a positivity rate of 0.28%. All H4 viruses were isolated from poultry, primarily from ducks in live poultry markets. We further investigated the genetic evolutionary characteristics and pathogenicity of 20 H4Nx viruses isolated in our program. Phylogenetic analysis revealed that the 20 H4Nx viruses belonged to the Eurasian lineage and exhibited significant genetic diversity, with 19 distinct genotypes identified. Molecular characterization indicated that these viruses were low-pathogenicity AIVs with limited binding affinity to human receptors, yet they contained mutations associated with enhanced viral replication and pathogenicity in mammals. Pathogenicity tests conducted in ducks demonstrated that H4 viruses were weakly pathogenic, exhibiting limited replication and transmission capabilities. However, some viruses were able to replicate effectively in mice and induce weight loss. For instance, DK/AH/AG61/11(H4N6) can replicate efficiently in MDCK cells, indicating a potential threat to mammals. These findings underscore the importance of ongoing surveillance of H4 AIVs to better understand their evolution and transmission dynamics and to prevent potential public health risks.
- H4 avian influenza viruses (H4 AIVs)
- , Epidemiology
- , Phylogenetic
- , Pathogenicity
- , Ducks
- , Mice

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