Environmental surveillance of a circulating vaccine-derived poliovirus type 2 outbreak in Israel between 2022 and 2023: a genomic epidemiology study

IF 20.9 1区 生物学 Q1 INFECTIOUS DISEASES Lancet Microbe Pub Date : 2024-10-01 DOI:10.1016/S2666-5247(24)00116-2
Neta S Zuckerman PhD , Efrat Bucris PhD , Hagar Morad-Eliyahu BSc , Leah Weiss BSc , Rinat Vasserman MSc , Ilana S Fratty PhD , Ira Aguvaev BSc , Zvi Cohen-Said BSc , Rua Matar BSc , Oran Erster PhD , Prof Lester M Shulman PhD , Ruth Yishai PhD , Lior Hecht-Sagie MD , Sharon Alroy-Preis MD , Prof Ella Mendelson PhD , Yaniv Lustig PhD , Danit Sofer PhD , Itay Bar-Or PhD , Merav Weil PhD
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Abstract

Background

Similarly to wild poliovirus, vaccine-derived poliovirus (VDPV) strains can cause acute flaccid paralysis, posing a considerable challenge to public health and the eradication of poliovirus. VDPV outbreaks, particularly VDPV type 2 (VDPV2), are increasing worldwide, including in high-income countries with high vaccine coverage. We aimed to conduct a comprehensive analysis of the molecular epidemiology of a widespread VDPV2 outbreak in Israel in 2022–23 using conventional polio identification techniques and whole-genome sequencing.

Methods

In this genomic epidemiology study, we monitored and identified poliovirus type 2 (PV2) through the surveillance of stool samples from individuals with acute flaccid paralysis and related contacts, as well as environmental surveillance of sewage samples. Environmental surveillance involved 15 routine surveillance sites and an additional 30 sites dedicated to monitoring this outbreak, covering approximately 70% of Israel's population between April 1, 2022, and June 30, 2023. Additionally, we performed phylogenetic and mutation analyses using whole-genome, next-generation sequencing of PV2 isolates to identify recombination events, characterise VDPV2 lineages according to the capsid region, and establish the geographical distribution and linkage of PV2 isolates.

Findings

We detected 256 genetically linked samples from environmental surveillance, as well as one case of acute flaccid paralysis and four positive contacts associated with the Sabin type 2 oral vaccine strain. Most affected locations showed a high-density population of Jewish Ultra-Orthodox communities. Through high-resolution genomic characterisation and phylogenetic analysis of 202 representative sequences with complete capsid coverage, including isolates from both environmental surveillance and the case of acute flaccid paralysis, a conclusive linkage was established among all detections, confirming them to be part of a single VDPV2 outbreak. This strategy enabled the characterisation of three distinct lineages and established connections between different locations in Israel, including linking the case of acute flaccid paralysis and nearby environmental surveillance detections from the northern region with detections in the geographically distant central region.

Interpretation

This study highlights the role of environmental surveillance in the early detection and monitoring of poliovirus circulation, enabling a prompt public health response involving enhanced surveillance and a catch-up campaign with inactivated polio vaccine. Whole-genome sequencing offered valuable insights into the origins of the outbreak, linkage across detections, and the geographical distribution of the virus, with higher resolution than would have been possible with the standard analysis of the VP1 gene alone.

Funding

None.
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对 2022 年至 2023 年以色列爆发的疫苗衍生型 2 型脊髓灰质炎病毒疫情进行环境监测:基因组流行病学研究。
背景:与野生脊髓灰质炎病毒类似,疫苗衍生脊髓灰质炎病毒(VDPV)毒株也可导致急性弛缓性麻痹,这对公共卫生和根除脊髓灰质炎病毒构成了巨大挑战。疫苗衍生脊髓灰质炎病毒(VDPV)疫情,尤其是 2 型疫苗衍生脊髓灰质炎病毒(VDPV2)疫情,正在全球范围内不断增加,包括在疫苗覆盖率较高的高收入国家。我们的目标是利用传统的脊髓灰质炎鉴定技术和全基因组测序技术,对 2022-23 年以色列大范围 VDPV2 型疫情的分子流行病学进行全面分析:在这项基因组流行病学研究中,我们通过监测急性弛缓性麻痹患者和相关接触者的粪便样本以及污水样本的环境监测来监测和鉴定脊髓灰质炎病毒 2 型 (PV2)。在 2022 年 4 月 1 日至 2023 年 6 月 30 日期间,环境监测涉及 15 个常规监测点和另外 30 个专门监测疫情的监测点,覆盖以色列约 70% 的人口。此外,我们还利用 PV2 分离物的全基因组下一代测序技术进行了系统发育和突变分析,以确定重组事件,根据囊膜区域确定 VDPV2 系的特征,并确定 PV2 分离物的地理分布和联系:我们从环境监测中检测到 256 份基因关联样本,以及一例急性弛缓性麻痹病例和四名与 Sabin 2 型口服疫苗株相关的阳性接触者。大多数受影响地区都有高密度的犹太极端正统派社区人口。通过对 202 个具有完整囊盖覆盖范围的代表性序列(包括来自环境监测和急性弛缓性麻痹病例的分离物)进行高分辨率基因组特征描述和系统进化分析,在所有检测物之间建立了确凿的联系,证实它们是单一 VDPV2 爆发的一部分。通过这一策略,确定了三个不同品系的特征,并建立了以色列不同地区之间的联系,包括将北部地区的急性弛缓性麻痹病例和附近的环境监测检测结果与地理位置遥远的中部地区的检测结果联系起来:本研究强调了环境监测在早期发现和监测脊髓灰质炎病毒循环中的作用,从而能够迅速采取公共卫生应对措施,包括加强监测和开展脊髓灰质炎灭活疫苗补种活动。全基因组测序为了解疫情的起源、不同检测结果之间的联系以及病毒的地理分布提供了宝贵的信息,其分辨率高于仅对 VP1 基因进行标准分析的结果:无。
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来源期刊
Lancet Microbe
Lancet Microbe Multiple-
CiteScore
27.20
自引率
0.80%
发文量
278
审稿时长
6 weeks
期刊介绍: The Lancet Microbe is a gold open access journal committed to publishing content relevant to clinical microbiologists worldwide, with a focus on studies that advance clinical understanding, challenge the status quo, and advocate change in health policy.
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