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RNA in Municipal Wastewater Reveals Magnitudes of COVID-19 Outbreaks across Four Waves Driven by SARS-CoV-2 Variants of Concern

  • Yuwei Xie*
    Yuwei Xie
    Toxicology Centre, University of Saskatchewan, Saskatoon, Saskatchewan S7N 5B3, Canada
    *Email: [email protected]
    More by Yuwei Xie
  • Jonathan K. Challis
    Jonathan K. Challis
    Toxicology Centre, University of Saskatchewan, Saskatoon, Saskatchewan S7N 5B3, Canada
  • Femi F. Oloye
    Femi F. Oloye
    Toxicology Centre, University of Saskatchewan, Saskatoon, Saskatchewan S7N 5B3, Canada
  • Mohsen Asadi
    Mohsen Asadi
    Department of Civil, Geological and Environmental Engineering, College of Engineering, University of Saskatchewan, Saskatoon, Saskatchewan S7N 5A9, Canada
    More by Mohsen Asadi
  • Jenna Cantin
    Jenna Cantin
    Toxicology Centre, University of Saskatchewan, Saskatoon, Saskatchewan S7N 5B3, Canada
    More by Jenna Cantin
  • Markus Brinkmann
    Markus Brinkmann
    Toxicology Centre, University of Saskatchewan, Saskatoon, Saskatchewan S7N 5B3, Canada
    School of Environment and Sustainability, University of Saskatchewan, Saskatoon, Saskatchewan S7N 5B3, Canada
    Global Institute for Water Security, University of Saskatchewan, Saskatoon, Saskatchewan S7N 3H5, Canada
  • Kerry N. McPhedran
    Kerry N. McPhedran
    Department of Civil, Geological and Environmental Engineering, College of Engineering, University of Saskatchewan, Saskatoon, Saskatchewan S7N 5A9, Canada
    Global Institute for Water Security, University of Saskatchewan, Saskatoon, Saskatchewan S7N 3H5, Canada
  • Natacha Hogan
    Natacha Hogan
    Toxicology Centre, University of Saskatchewan, Saskatoon, Saskatchewan S7N 5B3, Canada
    College of Agriculture and Bioresources, Department of Animal and Poultry Sciences, University of Saskatchewan, Saskatoon, Saskatchewan S7N 5A8, Canada
  • Mike Sadowski
    Mike Sadowski
    Wastewater Treatment Plant, Saskatoon Water Department, City of Saskatoon, Saskatoon, Saskatchewan S7M 1X5, Canada
  • Paul D. Jones
    Paul D. Jones
    Toxicology Centre, University of Saskatchewan, Saskatoon, Saskatchewan S7N 5B3, Canada
    School of Environment and Sustainability, University of Saskatchewan, Saskatoon, Saskatchewan S7N 5B3, Canada
  • Chrystal Landgraff
    Chrystal Landgraff
    Division of Enteric Diseases, National Microbiology Laboratory, Public Health Agency of Canada, Winnipeg, Manitoba R3E 3R2, Canada
    Food Science Department, University of Guelph, Guelph, Ontario N1G 2W1, Canada
  • Chand Mangat
    Chand Mangat
    Antimicrobial Resistance and Nosocomial Infections, National Microbiology Laboratory, Public Health Agency of Canada, Winnipeg, Manitoba R3E 3R2, Canada
    More by Chand Mangat
  • Mark R. Servos
    Mark R. Servos
    Department of Biology, University of Waterloo, Waterloo, Ontario N2L 3G1, Canada
  • , and 
  • John P. Giesy*
    John P. Giesy
    Toxicology Centre, University of Saskatchewan, Saskatoon, Saskatchewan S7N 5B3, Canada
    Department of Veterinary Biomedical Sciences, University of Saskatchewan, Saskatoon, Saskatchewan S7N 5B4, Canada
    Department of Environmental Sciences, Baylor University, Waco, Texas 76706, United States
    Department of Zoology and Center for Integrative Toxicology, Michigan State University, East Lansing, Michigan 48824, United States
    *Email: [email protected]
Cite this: ACS EST Water 2022, 2, 11, 1852–1862
Publication Date (Web):February 23, 2022
https://doi.org/10.1021/acsestwater.1c00349
Copyright © 2022 American Chemical Society

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    Abstract

    Abstract Image

    There are no standardized protocols for quantifying severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in wastewater to date, especially for population normalization. Here, a pipeline was developed, applied, and assessed to quantify SARS-CoV-2 and key variants of concern (VOCs) RNA in wastewater at Saskatoon, Canada. Normalization approaches using recovery ratio and extraction efficiency, wastewater parameters, or population indicators were assessed by comparing to daily numbers of new cases. Viral load was positively correlated with daily new cases reported in the sewershed. Wastewater surveillance (WS) had a lead time of approximately 7 days, which indicated surges in the number of new cases. WS revealed the variant α and δ driving the third and fourth wave, respectively. The adjustment with the recovery ratio and extraction efficiency improved the correlation between viral load and daily new cases. Normalization of viral concentration to concentrations of the artificial sweetener acesulfame K improved the trend of viral load during the Christmas and New Year holidays when populations were dynamic and variable. Acesulfame K performed better than pepper mild mottle virus, creatinine, and ammonia for population normalization. Hence, quality controls to characterize recovery ratios and extraction efficiencies and population normalization with acesulfame are promising for precise WS programs supporting decision-making in public health.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acsestwater.1c00349.

    • Protocol of wastewater sampling, transport, and storage, ddPCR method, thermal cycling conditions, method of chemical tracer analyses, catchment area of the Saskatoon Wastewater Treatment Plant, scatter diagram of the relation of the viral concentration in the N1 and N2 assay and in the N.L3.CTA and N.L3.A28271del assay, characteristics of wastewater, correlations between SARS-CoV-2 concentrations and daily new case numbers, longitudinal profiles of cell phone mobility and concentrations of acesulfame K, local alignment of the nonlinear curve fitting models for each climbing stage of the COVID-19 waves, raw wastewater characteristics, sequences of primers and probes, RT-qPCR assay parameters, whole genome sequencing data, and nonlinear curve fitting data (PDF)

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    Cited By

    This article is cited by 10 publications.

    1. Alexander Mitranescu, Anna Uchaikina, Anna-Sonia Kau, Claudia Stange, Johannes Ho, Andreas Tiehm, Christian Wurzbacher, Jörg E. Drewes. Wastewater-Based Epidemiology for SARS-CoV-2 Biomarkers: Evaluation of Normalization Methods in Small and Large Communities in Southern Germany. ACS ES&T Water 2022, 2 (12) , 2460-2470. https://doi.org/10.1021/acsestwater.2c00306
    2. Teresa Kumblathan, Yanming Liu, Yuanyuan Qiu, Lilly Pang, Steve E. Hrudey, X. Chris Le, Xing-Fang Li. An efficient method to enhance recovery and detection of SARS-CoV-2 RNA in wastewater. Journal of Environmental Sciences 2023, 130 , 139-148. https://doi.org/10.1016/j.jes.2022.10.006
    3. Mohsen Asadi, Femi F. Oloye, Yuwei Xie, Jenna Cantin, Jonathan K. Challis, Kerry N. McPhedran, Warsame Yusuf, David Champredon, Pu Xia, Chantel De Lange, Seba El-Baroudy, Mark R. Servos, Paul D. Jones, John P. Giesy, Markus Brinkmann. A wastewater-based risk index for SARS-CoV-2 infections among three cities on the Canadian Prairie. Science of The Total Environment 2023, 876 , 162800. https://doi.org/10.1016/j.scitotenv.2023.162800
    4. Stefano Ciannella, Cristina González-Fernández, Jenifer Gomez-Pastora. Recent progress on wastewater-based epidemiology for COVID-19 surveillance: A systematic review of analytical procedures and epidemiological modeling. Science of The Total Environment 2023, 878 , 162953. https://doi.org/10.1016/j.scitotenv.2023.162953
    5. Marco A. Lopez Marin, K. Zdenkova, J. Bartackova, E. Cermakova, A. Dostalkova, K. Demnerova, L. Vavruskova, Z. Novakova, P. Sykora, M. Rumlova, J. Bartacek. Monitoring COVID-19 spread in selected Prague's schools based on the presence of SARS-CoV-2 RNA in wastewater. Science of The Total Environment 2023, 871 , 161935. https://doi.org/10.1016/j.scitotenv.2023.161935
    6. Yabing Li, Brijen Miyani, Liang Zhao, Maddie Spooner, Zach Gentry, Yangyang Zou, Geoff Rhodes, Hui Li, Andrew Kaye, John Norton, Irene Xagoraraki. Surveillance of SARS-CoV-2 in nine neighborhood sewersheds in Detroit Tri-County area, United States: Assessing per capita SARS-CoV-2 estimations and COVID-19 incidence. Science of The Total Environment 2022, 851 , 158350. https://doi.org/10.1016/j.scitotenv.2022.158350
    7. Askar Gafurov, Andrej Baláž, Fabian Amman, Kristína Boršová, Viktória Čabanová, Boris Klempa, Andreas Bergthaler, Tomáš Vinař, Broňa Brejová. VirPool: model-based estimation of SARS-CoV-2 variant proportions in wastewater samples. BMC Bioinformatics 2022, 23 (1) https://doi.org/10.1186/s12859-022-05100-3
    8. William Johnson, Katelyn Reeves, Jennifer Liebig, Antonio Feula, Claire Butler, Michaela Alkire, Samiha Singh, Shelby Litton, Kerry O'Conor, Keaton Jones, Nikolas Ortega, Trace Shimek, Julia Witteman, , Elle Coe, Heidi Heuer, Jeffrey Jones, Sara Key, Jacob Lilienfeld, Juniper Maggi, Lauren Nelson, Kevin Pulley, Paul Wilkerson, Bailey Vigil, Gordon Zak, Kiersten Maxwell, Madeline Karr, Nicholas Freeman, Emily Saldana, Lewis Salveson, Kate Tomlinson, Jorge Vargas-barriga, Kristen K Bjorkman, Cresten Mansfeldt. Effectiveness of building-level sewage surveillance during both community-spread and sporadic-infection phases of SARS-CoV-2 in a university campus population. FEMS Microbes 2022, 3 https://doi.org/10.1093/femsmc/xtac024
    9. Femi F. Oloye, Yuwei Xie, Mohsen Asadi, Jenna Cantin, Jonathan K. Challis, Markus Brinkmann, Kerry N. McPhedran, Kevin Kristian, Mark Keller, Mike Sadowski, Paul D. Jones, Chrystal Landgraff, Chand Mangat, Meghan Fuzzen, Mark R. Servos, John P. Giesy. Rapid transition between SARS-CoV-2 variants of concern Delta and Omicron detected by monitoring municipal wastewater from three Canadian cities. Science of The Total Environment 2022, 841 , 156741. https://doi.org/10.1016/j.scitotenv.2022.156741
    10. Steve E. Hrudey, Heather N. Bischel, Jeff Charrois, Alex H. S. Chik, Bernadette Conant, Rob Delatolla, Sarah Dorner, Tyson E. Graber, Casey Hubert, Judy Isaac-Renton, Wendy Pons, Hannah Safford, Mark Servos, Christopher Sikora, . Wastewater Surveillance for SARS-CoV-2 RNA in Canada. FACETS 2022, 7 , 1493-1597. https://doi.org/10.1139/facets-2022-0148