pubs.acs.org/est Viewpoint Environmental Engineers and Scientists Have Important Roles to Play in Stemming Outbreaks and Pandemics Caused by Enveloped Viruses Krista R. Wigginton* and Alexandria B. Boehm Cite This: https://dx.doi.org/10.1021/acs.est.0c01476 Read Online Metrics & More Article Recommendations ACCESS further onward transmission (i.e., indirect transmission). This includes viruses responsible for inﬂuenza and measles. The primary transmission routes for SARS-CoV-2 (the virus that causes COVID-19) are believed to be person-to-person contact and by exposure to large droplets produced from sneezing, coughing or talking, but indirect transmission routes may also play a role. This potential role of the environment in the spread of COVID-19 highlights the multitude of applied research needs that must be addressed to eﬀectively control outbreaks and pandemics as novel enveloped viruses emerge. Environmental engineers and scientists are well positioned to apply their unique skill sets and experience with interdiscipli- nary research to address these needs. Virus particles in the air and on fomites are exposed to a range of environmental conditions that inﬂuence their persistence. Relative humidity, fomite material, and air temperature can greatly impact enveloped virus inactivation 2−5 rates. Even the medium in which the virus is suspended can greatly impact persistence. For example, chlorine-based solutions and hydrogen peroxide gas are eﬀective at 7,8 inactivating the enveloped virus surrogate Phi6 on fomites, but the presence of blood requires much higher hydrogen peroxide gas doses. Future mechanistic studies should probe nvironmental engineers and scientists have played pivotal how speciﬁc constituents in the matrix, temperature, humidity, E roles in protecting the public from viral illnesses, and and solar radiation each impact inactivation. Furthermore, continue to do so today. We develop drinking water and research quantifying the transfer of enveloped viruses between municipal wastewater treatment technologies, make discoveries fomites and skin, and determining eﬀective hand washing and that inform related regulations and policies, and conduct surface sanitizing methods, is needed to inform agent-based critical research on the presence, persistence, and transport of risk assessment models. viruses in the environment. A wide range of impactful research Viruses have a direct connection to wastewater and drinking in our ﬁeld has focused mainly on nonenveloped human water puriﬁcation when they are excreted in feces or urine enteric viruses such as human noroviruses and enteroviruses. (Table 1), but there is limited data on the concentration of More recently, a number of high-proﬁle outbreaks such as enveloped viruses in feces and urine. The human coronavirus Ebola virus, measles, Zika virus, avian inﬂuenzas, SARS, MERS, responsible for the 2003 SARS outbreak was able to replicate and the ongoing COVID-19 pandemic have been caused by in the human GI tract and infective particles were detected in enveloped viruses. In addition to the RNA or DNA genomes stool samples. In fact, aerosolized fecal particles are believed and protective protein capsids that are common to all viruses, enveloped virus structures are also wrapped in bilipid Received: March 9, 2020 membranes. The primary mode of transmission for many enveloped viruses is by close contact with infected individuals. Some enveloped viruses, however, are released to the environment by the host and persist on surfaces (i.e., fomites), in the air, or in water, long enough to come into contact with another host for https://dx.doi.org/10.1021/acs.est.0c01476 © XXXX American Chemical Society Environ. Sci. Technol. XXXX, XXX, XXX−XXX A Environmental Science & Technology pubs.acs.org/est Viewpoint Table 1. Mean or Median Viral Loads in the Feces and Despite the research outlined above, enveloped viruses are Urine of Infected Individuals for Three Enveloped Viruses extremely diverse, with a range of genome types, structures, and Two Nonenveloped Viruses replication cycles, and pathogenicities. For example, of the 158 identiﬁed human RNA viruses species as of 2018, 122 species urine feces feces (gc/ from 11 virus families were enveloped and 36 species from 6 virus enveloped? (gc/mL) (gc/g) swab) source families were nonenveloped. Consequently, enveloped b 1.3 6.1 SARS yes 10 10 NA 21 viruses likely display a diverse range of environmental behavior, 4.5 cytomegalovirus yes 10 NA NA 22 persistence, and fate. The limited studies on enveloped-virus (CMV) d 5 SARS-CoV-2 yes ND NA 10 13 fate, transport, and inactivation have focused on only a small 8.5 human norovirus no NA 10 NA 23 fraction of human viruses or their proxies including animal GII coronaviruses and bacteriophage phi6. Although studies using 4.6 JC polyomavirus no 10 NA NA 24 animal coronaviruses have been valuable for the current 3,15,27 “gc” is gene copy. NA = not analyzed in study, ND = analyzed, but COVID-19 outbreak, it is essential to consider an not detected in study. Samples from approximately 100 patients with expanded set of enveloped viruses that better represent lab-conﬁrmed illness, mean. Samples from 36 children with lab- human enveloped virus diversity. conﬁrmed illness, median. Rectal swab samples from 9 patients with Future studies on enveloped viruses should seek to carefully lab-conﬁrmed illness during ﬁrst week of illness, mean. Samples from f characterize and even standardize the conditions under which 627 patients with gastroenteritis symptoms, median Samples from 71 measurements are conducted. Media composition, the purity health blood donors that tested positive or JC polyomavirus, median. of virus stock, and when possible, virus concentrations in both gene copies and infective units, should be described. When to have played a major role in spreading the virus at a Hong studying oxidants, the demand of the solution and change in Kong apartment complex. Similarly, SARS-CoV-2 genomic oxidant concentration through the experiment should be 12,13 RNA has been detected in feces. Although infective SARS- provided. When studying radiation (UVC and/or sunlight), CoV-2 has not yet been conﬁrmed in stool samples, the SARS- attenuation through the experimental solution should be well- CoV-2 RNA shedding pattern suggests viruses are replicating characterized incorporated into reported doses. Researchers in the GI tract. Other human enveloped viruses, such as should include a well-studied surrogate virus in their cytomegalovirus (CMV), are excreted in urine. Research so far experiments in addition to the enveloped virus of interest to on enveloped viruses in wastewater, including coronaviruses, facilitate cross-study comparisons. We recommend using the suggest these viruses are inactivated at faster rates than most nonenveloped bacteriophage MS2 for this purpose, as it is one 14−18 nonenveloped viruses, that they partition to wastewater of the most studied viruses in environmental systems. solids to a greater extent than nonenveloped viruses, and that Finally, there are emerging research areas in our ﬁeld that we wastewater temperature is positively associated with their believe can inform the current COVID-19 outbreak and future 15,18 inactivation rates. In water puriﬁcation processes, they are novel viral outbreaks. For example, predictive models based on generally more susceptible to oxidant disinfectants than the underlying mechanisms controlling the persistence of 19,20 nonenveloped viruses. The presence of an envelope does enveloped viruses, and other characteristics, may reduce the not appear to impact virus susceptibility to ultraviolet C 14 need to study every virus under every condition. Another (UVC) light, likely because UVC targets virus genomes and promising area of research involves using sewage to monitor lipid membranes do not shield the genomes from UVC virus circulation in communities and detect outbreaks before radiation. clinical cases are identiﬁed. Recently applied to pathogenic What does this mean for the SARS-CoV-2 virus and the 28 29 bacteria and nonenveloped viruses, this will necessitate a ability of our water puriﬁcation plants to produce safe water? better understanding of which enveloped viruses are excreted Our drinking water treatment plants, including those used to in urine and feces and at what levels. produce drinking water from wastewater, were designed using SARS-CoV-2 will certainly not be the last novel virus to microbial risk assessments and process performance data with emerge and seriously threaten global public health. Researchers nonenveloped enteric viruses. Based on the facts that (1) the and funding agencies have a tendency to focus intensely on a closely related 2003 SARS was excreted in feces at lower levels speciﬁc virus during its outbreak, but then move on to other than enteric human noroviruses (Table 1), (2) model topics when the outbreak subsides. Given the historical coronaviruses are inactivated at faster rates in wastewater contributions from our ﬁeld, and the grand challenges that and other waters than nonenveloped viruses, (3) the enveloped lie ahead, environmental science and engineering researchers viruses studied to-date are more susceptible to oxidant should take a broader, long-term, and more quantitative disinfectants than nonenveloped viruses, and (4) the large approach to understanding viruses that are spread through the single-stranded RNA (ssRNA) genome (∼29.8 kb) of SARS- environment. Similar to how we approach chemical pollutants CoV-2 likely renders it more susceptible to UVC inactivation in the environment, we should aim to understand and than enteric ssRNA viruses, the multibarrier wastewater and communicate to our colleagues in medicine and public health drinking water treatment systems are likely eﬀective in the speciﬁc characteristics that drive transport and inactivation protecting against SARS-CoV-2. Nonetheless, there may still of enveloped viruses in solutions, on surfaces, and in the air. be water-related exposures that need to be considered if Likewise, we should seek to understand how environmental infectious SARS-CoV-2 viruses are present in urine or feces. factors shape possible virus transmission routes. That way, Such exposures may occur in communities that experience regardless of the identity of the enveloped virus that causes the combined sewage overﬂows, that do not have sewage next major outbreak, we can provide more informed infrastructure, or that use wastewater for irrigation, as well as buildings that have faulty plumbing systems and occupational descriptions of its persistence and recommendations on how exposures to wastewater and excrement. to mitigate its spread. B https://dx.doi.org/10.1021/acs.est.0c01476 Environ. Sci. Technol. XXXX, XXX, XXX−XXX Environmental Science & Technology pubs.acs.org/est Viewpoint A.; Diaz, G.; Cohn, A.; Fox, L.; Patel, A.; Gerber, S. I.; Kim, L.; Tong, AUTHOR INFORMATION S.; Lu, X.; Lindstrom, S.; Pallansch, M. A.; Weldon, W. C.; Biggs, H. Corresponding Author M.; Uyeki, T. M.; Pillai, S. K. First Case of 2019 Novel Coronavirus in Krista R. Wigginton − Department of Civil and Environmental the United States. N. Engl. J. Med. 2020, 382, 929−936. Engineering, University of Michigan, Ann Arbor, Michigan (13) Woelfel, R., Corman, V. M., Guggemos, W., Seilmaier, M., 48109, United States; Department of Civil and Environmental Zange, S., Mueller, M. A., Niemeyer, D., Vollmar, P., Rothe, C., Engineering, Stanford University, Stanford, California 94305, Hoelscher, M., Bleicker, T., Bruenink, S., Schneider, J., Ehmann, R., United States; orcid.org/0000-0001-6665-5112; Zwirglmaier, K., Drosten, C., Wendtner, C. 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