Abstract
Waterborne enteric viruses are an emerging cause of disease outbreaks and represent a major threat to global public health. Enteric viruses may originate from human wastewater and can undergo rapid transport through aquatic environments with minimal decay. Surveillance and source apportionment of enteric viruses in environmental waters is therefore essential for accurate risk management. However, individual monitoring of the >100 enteric viral strains that have been identified as aquatic contaminants is unfeasible. Instead, viral indicators are often used for quantitative assessments of wastewater contamination, viral decay and transport in water. An ideal indicator for tracking wastewater contamination should be (i) easy to detect and quantify, (ii) source-specific, (iii) resistant to wastewater treatment processes, and (iv) persistent in the aquatic environment, with similar behaviour to viral pathogens. Here, we conducted a comprehensive review of 127 peer-reviewed publications, to critically evaluate the effectiveness of several viral indicators of wastewater pollution, including common enteric viruses (mastadenoviruses, polyomaviruses, and Aichi viruses), the pepper mild mottle virus (PMMoV), and gut-associated bacteriophages (Type II/III FRNA phages and phages infecting human Bacteroides species, including crAssphage). Our analysis suggests that overall, human mastadenoviruses have the greatest potential to indicate contamination by domestic wastewater due to their easy detection, culturability, and high prevalence in wastewater and in the polluted environment. Aichi virus, crAssphage and PMMoV are also widely detected in wastewater and in the environment, and may be used as molecular markers for human-derived contamination. We conclude that viral indicators are suitable for the long-term monitoring of viral contamination in freshwater and marine environments and that these should be implemented within monitoring programmes to provide a holistic assessment of microbiological water quality and wastewater-based epidemiology, improve current risk management strategies and protect global human health.
Highlights
We considered enteric viruses, pepper mild mottle virus (PMMoV) and human gut bacteria-associated bacteriophages, including F-specific RNA bacteriophages (FRNAP) infecting E. coli, and bacteriophages of human gut commensal Bacteroides spp
The viruses reviewed here have all been shown to have potential to indicate wastewater-derived pollution in the aquatic environment (Table 3). Due to their wide distribution, they may be implemented in water quality risk assessments worldwide
CrAssphages and other phages, which infect commensal bacteria associated with human gut, and PMMoV, which is a plant virus found in the human gut due to the consumption of infected plantderived food, are associated primarily with domestic wastewater contamination
Summary
Waterborne diarrheal diseases account for approximately 4 billion cases annually, resulting in 2 million deaths, most of which occur in children under five (WHO, 2010). Some PyVs, including BKPyV, WUPyV, KIPyV, MCPyV and JCPyV have been detected at high concentrations (up to 108 genome copies (gc)/l) in wastewater, river and seawater and sediment, in swimming pools and in tap water (Di Bonito et al, 2017; Dias et al, 2018a, b; Farkas et al, 2018a; Fratini et al, 2014; Hamza and Hamza, 2018; Rachmadi et al, 2016) As these viruses are commonly asymptomatic in healthy individuals, the route of transmission is not yet clear, waterborne infections are likely (Fratini et al, 2014). Enveloped viruses degrade in water rapidly (Gundy et al, 2009; Lebarbenchon et al, 2011), human infections from waterborne corona- and influenza viruses (e.g. SARS-CoV-2) are unlikely
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