Phylogenetic Study of Local Patterns Influenza A(H3N2) Virus Transmission in a Semi-Isolated Population in a Remote Island in Japan Between 2011 and 2013

IF 4.2 4区医学 Q1 INFECTIOUS DISEASES

Influenza and Other Respiratory Viruses Pub Date : 2025-03-10 DOI:10.1111/irv.70089

Su Myat Han, Teiichiro Shiino, Shingo Masuda, Yuki Furuse, Takahiro Yasaka, Satoshi Kanda, Kazuhiri Komori, Nobuo Saito, Yoshiano Kubo, Chris Smith, Akira Endo, Alexis Robert, Marc Baguelin, Koya Ariyoshi

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Abstract

Background

Influenza A outbreak risk is impacted by the potential for importation and local transmission. Reconstructing transmission history with phylogenetic analysis of genetic sequences can help assess outbreak risk but relies on regular collection of genetic sequences. Few influenza genetic sequences are collected in Japan, which makes phylogenetic analysis challenging, especially in rural, remote settings. We generated influenza A genetic sequences from nasopharyngeal swabs (NPS) samples collected using rapid influenza diagnostic tests and used them to analyze the transmission dynamics of influenza in a remote island in Japan.

Methods

We generated 229 whole genome sequences of influenza A/H3N2 collected during 2011/12 and 2012/13 influenza seasons in Kamigoto Island, Japan, of which 178 sequences passed the quality check. We built time-resolved phylogenetic trees from hemagglutinin sequences to classify the circulating clades by comparing the Kamigoto sequences to global sequences. Spatiotemporal transmission patterns were then analyzed for the largest local clusters.

Results

Using a time-resolved phylogenetic tree, we showed that the sequences clustered in six independent transmission groups (1 in 2011/12, 5 in 2012/13). Sequences were closely related to strains from mainland Japan. All 2011/12 strains were identified as clade 3C.2 (n = 29), while 2012/13 strains fell into two clades: clade 3C.2 (n = 129) and 3C.3a (n = 20). Clusters reported in 2012/13 circulated simultaneously in the same regions. The spatiotemporal analysis of the largest cluster revealed that while the first sequences were reported in the busiest district of Kamigoto, the later sequences were scattered across the island.

Conclusion

Kamigoto Island was exposed to repeated importations of Influenza A(H3N2), mostly from mainland Japan, sometimes leading to local transmission and ultimately outbreaks. As independent groups of sequences overlapped in time and space, cases may be wrongly allocated to the same transmission group in the absence of genomic surveillance, thereby underestimating the risk of importations. Our analysis highlights how NPS could be used to better understand influenza transmission patterns in little-studied settings and improve influenza surveillance in Japan.

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2011年至2013年日本某偏远岛屿半隔离人群中甲型流感（H3N2）病毒本地模式传播的系统发育研究

背景：甲型流感爆发风险受到输入和本地传播可能性的影响。通过基因序列的系统发育分析重建传播史有助于评估疫情风险，但依赖于定期收集基因序列。在日本收集的流感基因序列很少，这使得系统发育分析具有挑战性，特别是在农村和偏远地区。我们从使用快速流感诊断测试收集的鼻咽拭子（NPS）样本中生成了甲型流感基因序列，并利用它们分析了日本一个偏远岛屿的流感传播动力学。方法对2011/12和2012/13流感季节在日本神本岛采集的流感A/H3N2全基因组序列进行测序，其中178条序列通过质量检查。我们从血凝素序列中建立了时间分辨的系统发育树，通过比较Kamigoto序列和全局序列对循环进化枝进行分类。然后分析了最大的局部集群的时空传输模式。结果利用时间分辨系统进化树，我们发现这些序列聚集在6个独立的传播群中（1个在2011/12年，5个在2012/13年）。序列与来自日本大陆的菌株密切相关。所有2011/12菌株均鉴定为3C.2支（n = 29），而2012/13菌株分为两个支系：支系3C.2（n = 129）和3C。3a （n = 20）。2012/13年度报告的聚集性病例在同一区域同时传播。对最大集群的时空分析表明，虽然第一个序列报告在最繁忙的神本地区，但后来的序列分散在全岛各地。结论神本岛存在甲型流感（H3N2）的反复输入，主要来自日本大陆，有时导致本地传播并最终爆发。由于独立的序列组在时间和空间上重叠，在没有基因组监测的情况下，病例可能被错误地分配到同一传播组，从而低估了输入风险。我们的分析强调了如何利用NPS更好地了解在研究较少的环境中的流感传播模式，并改善日本的流感监测。

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来源期刊

Influenza and Other Respiratory Viruses 医学-病毒学

CiteScore

7.20

自引率

4.50%

发文量

120

审稿时长

6-12 weeks

期刊介绍： Influenza and Other Respiratory Viruses is the official journal of the International Society of Influenza and Other Respiratory Virus Diseases - an independent scientific professional society - dedicated to promoting the prevention, detection, treatment, and control of influenza and other respiratory virus diseases. Influenza and Other Respiratory Viruses is an Open Access journal. Copyright on any research article published by Influenza and Other Respiratory Viruses is retained by the author(s). Authors grant Wiley a license to publish the article and identify itself as the original publisher. Authors also grant any third party the right to use the article freely as long as its integrity is maintained and its original authors, citation details and publisher are identified.