Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2023 Jun;15(2):176-191.
doi: 10.1007/s12560-023-09553-4. Epub 2023 Apr 14.

Genotype Diversity of Enteric Viruses in Wastewater Amid the COVID-19 Pandemic

Sheikh Ariful Hoque  1   2 , Tomohiro Kotaki  3 , Ngan Thi Kim Pham  1 , Yuko Onda  1 , Shoko Okitsu  1 , Shintaro Sato  3   4 , Yoshikazu Yuki  5 , Takeshi Kobayashi  3 , Niwat Maneekarn  6 , Hiroshi Kiyono  5   7   8 , Satoshi Hayakawa  1 , Hiroshi Ushijima  9
Affiliations

Genotype Diversity of Enteric Viruses in Wastewater Amid the COVID-19 Pandemic

Sheikh Ariful Hoque et al. Food Environ Virol. 2023 Jun.

Abstract

Viruses remain the leading cause of acute gastroenteritis (AGE) worldwide. Recently, we reported the abundance of AGE viruses in raw sewage water (SW) during the COVID-19 pandemic, when viral AGE patients decreased dramatically in clinics. Since clinical samples were not reflecting the actual state, it remained important to determine the circulating strains in the SW for preparedness against impending outbreaks. Raw SW was collected from a sewage treatment plant in Japan from August 2018 to March 2022, concentrated by polyethylene-glycol-precipitation method, and investigated for major gastroenteritis viruses by RT-PCR. Genotypes and evolutionary relationships were evaluated through sequence-based analyses. Major AGE viruses like rotavirus A (RVA), norovirus (NoV) GI and GII, and astrovirus (AstV) increased sharply (10-20%) in SW during the COVID-19 pandemic, though some AGE viruses like sapovirus (SV), adenovirus (AdV), and enterovirus (EV) decreased slightly (3-10%). The prevalence remained top in the winter. Importantly, several strains, including G1 and G3 of RVA, GI.1 and GII.2 of NoV, GI.1 of SV, MLB1 of AstV, and F41 of AdV, either emerged or increased amid the pandemic, suggesting that the normal phenomenon of genotype changing remained active over this time. This study crucially presents the molecular characteristics of circulating AGE viruses, explaining the importance of SW investigation during the pandemic when a clinical investigation may not produce the complete scenario.

Keywords: COVID-19 pandemic; Enteric viruses; Genotypes; Raw sewage.

PubMed Disclaimer

Conflict of interest statement

The authors have no financial or proprietary interests in any material discussed in this article.

Figures

Fig. 1
Fig. 1
Phylogenetic analysis of RVA based on partial VP7 region. The tree was constructed by the Neighbor-Joining method and drawn to scale, with branch lengths in the same units as those of the evolutionary distances used to infer the phylogenetic tree. The tree is rooted by the G18 strain and constructed with the study strains (bold, underlined with sampling time and accession number in the first bracket) and the reference strains obtained from the GenBank database. Bootstrap values ≥ 75% are shown at the branch nodes
Fig. 2
Fig. 2
Phylogenetic analysis of NoV GI (a), NoV GII (b), and SV (c) based on partial capsid region. The trees were constructed by the Neighbor-Joining method and drawn to scale, with branch lengths in the same units as those of the evolutionary distances used to infer the phylogenetic trees. The strains detected in this study are shown with the collection time and accession number in bold and underlined. Bootstrap values ≥ 75% are shown at the branch nodes. Asterisks represent the prototypes
Fig. 2
Fig. 2
Phylogenetic analysis of NoV GI (a), NoV GII (b), and SV (c) based on partial capsid region. The trees were constructed by the Neighbor-Joining method and drawn to scale, with branch lengths in the same units as those of the evolutionary distances used to infer the phylogenetic trees. The strains detected in this study are shown with the collection time and accession number in bold and underlined. Bootstrap values ≥ 75% are shown at the branch nodes. Asterisks represent the prototypes
Fig. 2
Fig. 2
Phylogenetic analysis of NoV GI (a), NoV GII (b), and SV (c) based on partial capsid region. The trees were constructed by the Neighbor-Joining method and drawn to scale, with branch lengths in the same units as those of the evolutionary distances used to infer the phylogenetic trees. The strains detected in this study are shown with the collection time and accession number in bold and underlined. Bootstrap values ≥ 75% are shown at the branch nodes. Asterisks represent the prototypes
Fig. 3
Fig. 3
Phylogenetic analysis of AdV (a), AstV (b), and EV (c) based on partial hexon, ORF-1b, and 5’UTR regions, respectively. The trees were constructed by the Neighbor-Joining method and drawn to scale, with branch lengths in the same units as those of the evolutionary distances used to infer the phylogenetic trees. The strains detected in this study are shown with the isolation time in bold, underlined. Bootstrap values ≥ 75% are shown at the branch nodes. The name of the disease other than AGE has been mentioned if available
Fig. 3
Fig. 3
Phylogenetic analysis of AdV (a), AstV (b), and EV (c) based on partial hexon, ORF-1b, and 5’UTR regions, respectively. The trees were constructed by the Neighbor-Joining method and drawn to scale, with branch lengths in the same units as those of the evolutionary distances used to infer the phylogenetic trees. The strains detected in this study are shown with the isolation time in bold, underlined. Bootstrap values ≥ 75% are shown at the branch nodes. The name of the disease other than AGE has been mentioned if available
Fig. 3
Fig. 3
Phylogenetic analysis of AdV (a), AstV (b), and EV (c) based on partial hexon, ORF-1b, and 5’UTR regions, respectively. The trees were constructed by the Neighbor-Joining method and drawn to scale, with branch lengths in the same units as those of the evolutionary distances used to infer the phylogenetic trees. The strains detected in this study are shown with the isolation time in bold, underlined. Bootstrap values ≥ 75% are shown at the branch nodes. The name of the disease other than AGE has been mentioned if available
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

References

    1. Adachi Katayama Y, Hayase S, Ando Y, Kuroita T, Okada K, Iwamoto R, et al. COPMAN: a novel high-throughput and highly sensitive method to detect viral nucleic acids including SARS-CoV-2 RNA in wastewater. Science of the Total Environment. 2023;856(Pt 1):158966. doi: 10.1016/j.scitotenv.2022.158966. - DOI - PMC - PubMed
    1. Akane Y, Tsugawa T, Fujii Y, Honjo S, Kondo K, Nakata S, et al. Molecular and clinical characterization of the equine-like G3 rotavirus that caused the first outbreak in Japan, 2016. Journal of General Virology. 2021 doi: 10.1099/jgv.0.001548. - DOI - PubMed
    1. Araki K, Hara M, Sakanishi Y, Shimanoe C, Nishida Y, Matsuo M, Tanaka K. Estimating rotavirus vaccine effectiveness in Japan using a screening method. Human Vaccines & Immunotherapeutics. 2016;12(5):1244–1249. doi: 10.1080/21645515.2015.1121337. - DOI - PMC - PubMed
    1. Armistead I, Tran A, White AE, Wilson E, Scallan Walter EJ. Trends in outpatient medical-care seeking for acute gastroenteritis during the COVID-19 Pandemic, 2020. Foodborne Pathogens and Disease. 2022;19(4):290–292. doi: 10.1089/fpd.2021.0099. - DOI - PubMed
    1. Braeckman T, Van Herck K, Meyer N, Pircon JY, Soriano-Gabarro M, Heylen E, et al. Effectiveness of rotavirus vaccination in prevention of hospital admissions for rotavirus gastroenteritis among young children in Belgium: Case-control study. BMJ. 2012;345:e4752. doi: 10.1136/bmj.e4752. - DOI - PMC - PubMed

Publication types