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Feb 14, 2017 - In response to the 2014/15 Ebola virus disease (EVD) epidemic, both the World Health Organization and the. United States Centers for Di...
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Research Needs for Wastewater Handling in Virus Outbreak Response Kyle Bibby,*,†,‡ Nathalia Aquino de Carvalho,† and Krista Wigginton§ †

Department of Civil and Environmental Engineering and ‡Department of Computational and Systems Biology, University of Pittsburgh, Pittsburgh, Pennsylvania 15261, United States § Department of Civil and Environmental Engineering, University of Michigan, Ann Arbor, Michigan 48109, United States To summarize research conducted on Ebola virus in wastewater with extension to future viral outbreaks, we organized a U.S. National Science Foundation sponsored workshop in May 2016. The goal of this workshop was to summarize current research findings on the behavior of Ebola virus and its surrogates in the environment, and to move toward a consensus on recommendations for outbreak response and research needs. Resulting from this workshop, several key areas of research need for handling highly infectious liquid waste became apparent, including the following: 1. Move toward a Mechanistic Model of Viral Inactivation. Mechanistic, rather than descriptive, models will enable the more rapid extension of observed inactivation behavior to emerging pathogens and exposure scenarios. Historical models of environmental virus inactivation were mostly descriptive, but recent efforts have focused on providing more mechanistic models for inactivation.3 Specific mechanisms that should be further explored include the role of pH, ammonia, biological activity, temperature, and solids found in wastewater matrices. Furthermore, the impact that viral lipid envelopes have on inactivation mechanisms should be explored due to the fact that many emerging human viruses are enveloped. We note that this n response to the 2014/15 Ebola virus disease (EVD) task will be challenging when working with Biosafety Level epidemic, both the World Health Organization and the (BSL) 3 and 4 microorganisms, due to the challenges United States Centers for Disease Control advised direct associated with access time and space. For example, there are disposal of Ebola-contaminated liquid waste into sewage currently only 13 current or planned BSL4 facilities in the US, systems (wastewater collection and treatment systems) and and environmental persistence efforts must fit within other latrines without disinfection.1 This recommendation was made priorities, including vaccine development and investigations of due to the presumed short survival of the enveloped Ebola virus the basic biology of BSL4 agents. in the environment, expected inactivation and dilution in 2. Better Characterization of Exposure and Transmission Pathways in the Wastewater Environment. Potential exposure wastewater systems, and the perceived hazards of additional pathways for both wastewater workers and the general public to waste handling and toxic byproduct formation due to chlorine untreated wastewater are poorly characterized. Specific areas of addition. Subsequently, concern was raised regarding approresearch needs include defining specific exposure scenarios, priate handling of Ebola virus contaminated liquid waste and potential exposure following unintended releases (e.g., the potential for secondary (environmental) transmission of the combined sewer overflows), and the differential fate of disease. Key unknowns that fueled this uncertainty included the structurally diverse viruses in existing sewage treatment environmental persistence of Ebola virus, efficacy of disinfrastructure. Specific questions regarding the fate of infection approaches against Ebola virus, and potential for structurally diverse viruses include how structure impacts exposure to Ebola virus within wastewater infrastructure. virus partitioning between wastewater solids, liquid, and air, Ultimately, studies found that Ebola virus persisted longer and how structure impacts viral survival in wastewater and than expected in the wastewater environment with an through wastewater treatment processes. approximate T90 (time for 90% inactivation) of 2.1 days in 3. Reconsider Surrogate Evaluation of Emerging Pathogens. sterilized wastewater.2 While the most recent Ebola virus Historically, surrogates−physiologically similar microorganoutbreak has ended, this experience has exposed a critical isms−have been used to study the fate and persistence of shortcoming in knowledge and regulation about appropriate handling of wastewater contaminated with highly infectious pathogens, such as Ebola virus, in both resource-rich and Received: December 21, 2016 Published: February 14, 2017 resource-poor outbreak settings.

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© 2017 American Chemical Society

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DOI: 10.1021/acs.est.6b06492 Environ. Sci. Technol. 2017, 51, 2534−2535

Environmental Science & Technology

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ACKNOWLEDGMENTS This study was supported by National Science Foundation award 1612429.

pathogens in the environment, e.g. MS2 bacteriophage to model enteric virus fate. A recent review demonstrated that the persistence of enveloped viral pathogens in water can vary from hours to months to achieve 90% inactivation.4 As highlighted in workshop discussions, it has become apparent that a limited suite of surrogates will be inadequate for a fine-scale, mechanistic understanding of viral persistence and inactivation in the wastewater environment. The variability of viral persistence within enveloped viruses4 suggests that where possible, it is best practice to use the pathogen of interest. Where direct use of the pathogen is not possible, the use of multiple surrogates is ideal to capture multiple aspects of target pathogen physiology. Furthermore, in the cases where the environmental fate of BSL3 and BSL4 viruses can be studied, experiments should include a surrogate virus in the same samples that contain the pathogenic viruses, so that the experimental results can be directly compared with other studies. We recommend that bacteriophage MS2 be included whenever possible in experiments with BSL3 and BSL4 viruses as this virus has been widely used as a persistence model and would facilitate cross-lab comparison and validation of persistence studies. 4. Appropriate Disinfection Approaches of High-Strength Waste. Infectious virus will be excreted from individuals in high-strength (i.e., high organic content) waste, such as blood, vomit, and feces. Clearly, control of pathogen release at the source (i.e., disinfection) would be desirable to limit potential downstream exposure and public concern; however, hyperchlorination of high organic content wastes insufficiently ensures pathogen inactivation.5 Evaluation of alternative disinfection methods, such as pH adjustment or heat, as well as a more mechanistic understanding of chlorine action in high strength waste, are necessary. A mechanistic understanding of disinfection will enable the effective extension of disinfection techniques to novel waste streams and pathogens that have not been extensively studied. 5. Communication. A critical shortcoming revealed in the Ebola response was the need for better communication between the wastewater and medical sectors, as well as with the general public. Forthcoming and accurate risk communication will be necessary to build both industry and public trust in infectious waste management. Multiple factors must be addressed, including the public’s ability to understand risk, and regionally and socially appropriate risk communication. The emergence of multiple high consequence viral pathogen outbreaks in recent years (e.g., SARS, Ebola, MERS, Lassa) has highlighted the value of continued investigation into viral pathogen fate and inactivation in the water environment, as well as appropriate wastewater handling and disinfection. Continued investment and attention in this critical research area is necessary to better inform future outbreak response, both minimizing the potential for secondary transmission of high consequence pathogens and public concern.



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REFERENCES

(1) Bibby, K.; Casson, L. W.; Stachler, E.; Haas, C. N. Ebola Virus Persistence in the Environment: State of the Knowledge and Research Needs. Environ. Sci. Technol. Lett. 2015, 2 (1), 2−6. (2) Bibby, K.; Fischer, R. J.; Casson, L. W.; Stachler, E.; Haas, C. N.; Munster, V. J. Persistence of Ebola Virus in Sterilized Wastewater. Environ. Sci. Technol. Lett. 2015, 2 (9), 245−249. (3) Decrey, L.; Kazama, S.; Udert, K. M.; Kohn, T. Ammonia as an In Situ Sanitizer: Inactivation Kinetics and Mechanisms of the ssRNA Virus MS2 by NH3. Environ. Sci. Technol. 2015, 49 (2), 1060−1067. (4) Wigginton, K. R.; Ye, Y.; Ellenberg, R. M. Emerging Investigators Series: The source and fate of pandemic viruses in the urban water cycle. Environmental Science: Water Research & Technology 2015, 1, 735. (5) Sozzi, E.; Fabre, K.; Fesselet, J.-F.; Ebdon, J. E.; Taylor, H. Minimizing the Risk of Disease Transmission in Emergency Settings: Novel In Situ Physico-Chemical Disinfection of Pathogen-Laden Hospital Wastewaters. PLoS Neglected Trop. Dis. 2015, 9 (6), e0003776.

AUTHOR INFORMATION

Corresponding Author

*Phone: 412-624-9207; e-mail: [email protected]. ORCID

Kyle Bibby: 0000-0003-3142-6090 Notes

The authors declare no competing financial interest. 2535

DOI: 10.1021/acs.est.6b06492 Environ. Sci. Technol. 2017, 51, 2534−2535