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Environmental Surveillance Can Dynamically Track Ecological Changes in Enteroviruses.

ABSTRACT: Environmental surveillance can be used to trace enteroviruses shed from human stool using a sewer network that is independent of symptomatic or asymptomatic infection. In this study, the local transmission of enteroviruses was analyzed using two wastewater treatment plants, which were relatively close to each other (15 km), designated as sentinels. Influent was collected at both sentinels once a month from 2013 to 2016, and viruses were isolated. Using neutralizing tests with type-specific polyclonal antisera and molecular typing, 933 isolates were identified as enteroviruses. Our results showed that the frequency of virus isolation varied for each serotype at the two sentinels in a time-dependent manner. Because echovirus 11 (Echo11) and coxsackievirus B5 isolates showed a high frequency and were difficult to distinguish, they were further grouped into various lineages based on the VP1 amino acid sequences. The prevalence of each lineage was visualized using multidimensional scaling. The results showed that Echo11 isolates of the same lineage were isolated continuously, similar to coxsackievirus B5 isolates of three lineages. Conversely, Echo1, Echo13, Echo18, Echo19, Echo20, Echo29, and Echo33 were isolated only once each. Our findings suggested that if an enterovirus is imported into the population, it may result in small-scale transmission, whereas if there are initially many infected individuals, it may be possible for the virus to spread to a wide area, beyond the local community, over time. In addition, our findings could provide insights into risk assessment of transmission for importation of poliovirus in polio-free countries and regions.IMPORTANCE In this study, we showed that environmental enterovirus surveillance can be used to monitor the propagation of nonpolio enteroviruses in addition to poliovirus detection. Since epidemiological studies of virus transmission based on the past were performed using specimens from humans, there were limitations to research design, such as specimen collection for implementation on a large-scale target population. However, environmental monitoring can dynamically track the ecological changes in enteroviruses in the region by monitoring viruses in chronological order and targeting the population within the area by monitoring viruses over time. We observed differences in the transmission of echovirus 11 and coxsackievirus B5 in the region according to lineage in a time-dependent manner and with a multidimensional scaling pattern.

SUBMITTER: Ozawa H

PROVIDER: S-EPMC6881801 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:In the context of poliomyelitis eradication, a reinforced supplementary laboratory surveillance of enteroviruses was implemented in Greece. Between 2008 and 2014, the Hellenic Polioviruses/Enteroviruses Reference Laboratory performed detailed supplementary surveillance of circulating enteroviruses among healthy individuals in high-risk population groups, among immigrants from countries in which poliovirus is endemic, and in environmental samples. In total, 722 stool samples and 179 sewage water samples were included in the study. No wild-type polioviruses were isolated during these 7 years of surveillance, although two imported vaccine polioviruses were detected. Enterovirus presence was recorded in 25.3 and 25.1% of stool and sewage water samples, respectively. Nonpolio enteroviruses isolated from stool samples belonged to species A, B, or C; coxsackievirus A24 was the most frequently identified serotype. Only enteroviruses of species B were identified in sewage water samples, including four serotypes of echoviruses and four serotypes of coxsackie B viruses. Phylogenetic analysis revealed close genetic relationships among virus isolates from sewage water samples and stool samples, which in most cases fell into the same cluster. To the best of our knowledge, this is the first study to compare enterovirus serotypes circulating in fecal specimens of healthy individuals and environmental samples, emphasizing the burden of enterovirus circulation in asymptomatic individuals at high risk. Given that Greece continues to receive a large number of short-term arrivals, students, migrants, and refugees from countries in which poliovirus is endemic, it is important to guarantee high-quality surveillance in order to maintain its polio-free status until global eradication is achieved.IMPORTANCE This article summarizes the results of supplementary poliovirus surveillance in Greece and the subsequent characterization of enteroviral circulation in human feces and the environment. The examination of stool samples from healthy refugees and other individuals in "high-risk" groups for poliovirus enables the identification of enterovirus cases and forms the basis for further investigation of the community-level risk of viral transmission. In addition, the examination of composite human fecal samples through environmental surveillance links poliovirus and nonpoliovirus isolates from unknown individuals to populations served by the sewage or wastewater system. Supplementary surveillance is necessary to comply with the prerequisites imposed by the World Health Organization for monitoring the emergence of vaccine-derived polioviruses, reemergence of wild polioviruses, or disappearance of all vaccine-related strains in order for countries such as Greece to maintain their polio-free status and contribute to global poliovirus eradication.

Project description:In the global strategy for polio eradication, environmental surveillance (ES) has been established worldwide to monitor polioviruses. In addition, nonpolio enteroviruses are simultaneously isolated from wastewater under this ES program. Hence, ES can be used to monitor enteroviruses in sewage to supplement clinical surveillance. In response to the coronavirus disease 2019 (COVID-19) pandemic, we also monitored severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in sewage using the polio ES system in Japan. Enterovirus and SARS-CoV-2 were detected in sewage from January 2019 to December 2021 and from August 2020 to November 2021, respectively. Enterovirus species such as echoviruses and coxsackieviruses were frequently detected by ES in 2019, indicating the circulation of these viruses. After the onset of the COVID-19 pandemic, sewage enterovirus detection and related patient reports were notably reduced in 2020 to 2021, suggesting changes in the hygiene behaviors of the human population in response to the pandemic. Our comparative experiment with a total of 520 reverse transcription-quantitative PCR (RT-qPCR) assays for SARS-CoV-2 detection demonstrated that the solid-based method had a significantly higher detection rate than that of the liquid-based method (24.6% and 15.9%, respectively). Moreover, the resulting RNA concentrations were correlated with the number of new COVID-19 cases (Spearman's r = 0.61). These findings indicate that the existing polio ES system can be effectively used for enterovirus and SARS-CoV-2 sewage monitoring using different procedures such as virus isolation and molecular-based detection. IMPORTANCE Long-term efforts are required to implement surveillance programs for the ongoing COVID-19 pandemic, and they will be required even in the postpandemic era. We adopted the existing polio environmental surveillance (ES) system for SARS-CoV-2 sewage monitoring in Japan as a practical and cost-effective approach. Moreover, the ES system routinely detects enteroviruses from wastewater and, therefore, can be used for enterovirus monitoring. The liquid fraction of the sewage sample is used for poliovirus and enterovirus detection, and the solid fraction can be used for SARS-CoV-2 RNA detection. The present study demonstrates how the existing ES system can be used for monitoring enteroviruses and SARS-CoV-2 in sewage.

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Environmental Surveillance Can Dynamically Track Ecological Changes in Enteroviruses.

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