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Complementing RNA Detection with Pharmaceutical Monitoring for Early Warning of Viral Outbreaks through Wastewater-Based Epidemiology

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Download Hi-Res ImageDownload to MS-PowerPointCite This:Environ. Sci. Technol. Lett. 2022, 9, 6, 567-574
    Ecotoxicology and Public Health

    Complementing RNA Detection with Pharmaceutical Monitoring for Early Warning of Viral Outbreaks through Wastewater-Based Epidemiology
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    • Lahiruni M. Halwatura
      Lahiruni M. Halwatura
      Department of Chemistry, University at Buffalo, The State University of New York, Buffalo, New York 14260, United States
      More by Lahiruni M. Halwatura
    • Isabella S. Mclerran
      Isabella S. Mclerran
      Department of Civil, Structural and Environmental Engineering, University at Buffalo, The State University of New York, Buffalo, New York 14260, United States
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    • Daniel L. Weglarski
      Daniel L. Weglarski
      Department of Chemistry, University at Buffalo, The State University of New York, Buffalo, New York 14260, United States
      More by Daniel L. Weglarski
    • Zia U. Ahmed
      Zia U. Ahmed
      Research and Education in Energy, Environment, and Water (RENEW) Institute, University at Buffalo, State University at New York, Buffalo, New York 14260, United States
      More by Zia U. Ahmed
    • Yinyin Ye
      Yinyin Ye
      Department of Civil, Structural and Environmental Engineering, University at Buffalo, The State University of New York, Buffalo, New York 14260, United States
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      Orcidhttps://orcid.org/0000-0003-0625-9657
    • Ian M. Bradley
      Ian M. Bradley
      Department of Civil, Structural and Environmental Engineering, University at Buffalo, The State University of New York, Buffalo, New York 14260, United States
      Research and Education in Energy, Environment, and Water (RENEW) Institute, University at Buffalo, State University at New York, Buffalo, New York 14260, United States
      More by Ian M. Bradley
      Orcidhttps://orcid.org/0000-0001-5338-1167
    • Diana S. Aga*
      Diana S. Aga
      Department of Chemistry, University at Buffalo, The State University of New York, Buffalo, New York 14260, United States
      Research and Education in Energy, Environment, and Water (RENEW) Institute, University at Buffalo, State University at New York, Buffalo, New York 14260, United States
      *Email: [email protected]
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      Orcidhttps://orcid.org/0000-0001-6512-7713
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    Environmental Science & Technology Letters

    Cite this: Environ. Sci. Technol. Lett. 2022, 9, 6, 567–574
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    https://doi.org/10.1021/acs.estlett.2c00259
    Published May 18, 2022
    Copyright © 2022 American Chemical Society
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    Abstract

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    Wastewater-based epidemiology using viral nucleic acids to predict community viral outbreaks has many challenges, including differences in viral shedding of infected individuals and interference from the wastewater matrix. In this study, we demonstrate that monitoring pharmaceutical residues in untreated sewage provides complementary information that correlates with future occurrences of viral outbreaks. We monitored 63 pharmaceutically active compounds, including antivirals used to treat COVID-19 and influenza and over-the-counter drugs commonly used to relieve the symptoms of infection. Weekly sampling was conducted at four municipal sewage treatment plants in Western New York. Residues of drugs associated with managing COVID-19 symptoms were detected, including azithromycin (1.99–5.00 μg/L), chloroquine (0.01–33.00 μg/L), hydroxychloroquine (0.05–30.54 μg/L), and lopinavir (13.75–181.20 μg/L). A significant correlation (p < 0.001) was observed between the total COVID-19-related drugs detected and the 5-day rolling averages of reported cases. Acetaminophen concentrations spiked approximately 2.5 weeks before a spike in SARS-CoV-2 RNA copies in all wastewater treatment plants sampled. The results suggest over-the-counter analgesic concentrations, in particular, acetaminophen in raw sewage to be used to complement viral RNA data as an early warning system for effective management of viral outbreaks at the community level.

    Copyright © 2022 American Chemical Society

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    Supporting Information

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.estlett.2c00259.

    • Methods of pharmaceutical analysis, including chemicals and reagents, the sample extraction procedure, chromatographic conditions, and quality control, method of RNA extraction and RT-qPCR analysis, details of sampling locations, pre- and post-outbreak fluctuations of wastewater-based targeted drug concentrations, RT-qPCR data, and clinical data of COVID-19 infections (PDF)

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    This article is cited by 19 publications.

    1. Zihang Wang, Huan He, William A. Arnold. Occurrence and Removal of Antibiotics in Wastewater Treatment Plants during the COVID-19 Pandemic. ACS ES&T Water 2024, 4 (12) , 5720-5731. https://doi.org/10.1021/acsestwater.4c00720
    2. Xixi Lv, Ruilong Dai, Nan Wang, Ruiping Liu. Photocatalytic Degradation of Antiviral Drugs Chloroquine Phosphate and Lamivudine by Bi2O3–TiO2/PAC under a Xe Lamp: Insights into Reactive Oxygen Species’ Action and Toxicity Reduction. ACS ES&T Water 2024, 4 (12) , 5776-5786. https://doi.org/10.1021/acsestwater.4c00760
    3. Emily J. Vogel, Milagros Neyra, David A. Larsen, Teng Zeng. Target and Nontarget Screening to Support Capacity Scaling for Substance Use Assessment through a Statewide Wastewater Surveillance Network in New York. Environmental Science & Technology 2024, 58 (19) , 8518-8530. https://doi.org/10.1021/acs.est.4c01251
    4. Shengchao Hu, Shangbiao Fang, Jian Zhao, Guowei Wang, Weixiao Qi, Gong Zhang, Cunrui Huang, Jiuhui Qu, Huijuan Liu. Toxicity Evaluation and Effect-Based Identification of Chlorine Disinfection Products of the Anti-COVID-19 Drug Chloroquine Phosphate. Environmental Science & Technology 2023, 57 (21) , 7913-7923. https://doi.org/10.1021/acs.est.2c08260
    5. Gregor R. Posadas, Joshua C. Baker, Abigail S. Ryan, Sondra M. Miller. Resiliency through Applied Research into Emerging Constituents. Water Resources Management 2025, 6 https://doi.org/10.1007/s11269-025-04140-7
    6. Xue-Ting Shao, Hao-Yang Li, Zhen-Fang Gong, Jian-Guo Lin, De-Gao Wang. Screening potential biomarkers for acute respiratory infectious diseases from antipyretics, antiviral, and antibiotics in wastewater. Science of The Total Environment 2024, 954 , 176714. https://doi.org/10.1016/j.scitotenv.2024.176714
    7. Stephan Baumgartner, Michelle Salvisberg, Patrick Schmidhalter, Timothy R Julian, Christoph Ort, Heinz Singer. Parallel Analysis of Pharmaceuticals and Viruses in Wastewater: An Untargeted Approach to Tracking Population-Level Respiratory Illness Burden. 2024https://doi.org/10.1101/2024.10.16.24315620
    8. Ruth Silvana Cortés-Lagunes, Andrea-Lorena Garduño-Jiménez, Alonso Romero-Solano, Rodolfo Zanella, Blanca Prado, O. Zamora, Juan C. Durán-Álvarez. Optimizing solid phase extraction and HPLC-MS/MS parameters for reliable quantification of COVID-19 pharmaceuticals in Mexico City’s wastewater: A design of experiments approach. Microchemical Journal 2024, 200 , 110493. https://doi.org/10.1016/j.microc.2024.110493
    9. Cheng-Shiuan Lee, Mian Wang, Deepak Nanjappa, Yi-Ta Lu, Jaymie Meliker, Sean Clouston, Christopher J. Gobler, Arjun K. Venkatesan. Monitoring of over-the-counter (OTC) and COVID-19 treatment drugs complement wastewater surveillance of SARS-CoV-2. Journal of Exposure Science & Environmental Epidemiology 2024, 34 (3) , 448-456. https://doi.org/10.1038/s41370-023-00613-2
    10. Shengchao Hu, Jian Zhao, Shangbiao Fang, Kehui Guo, Weixiao Qi, Huijuan Liu. Neurotoxic effects of chloroquine and its main transformation product formed after chlorination. Science of The Total Environment 2024, 908 , 168043. https://doi.org/10.1016/j.scitotenv.2023.168043
    11. Yuwei Zhang, Junjiang Guo, Bin Li, Zhiwei Wang, Zunzhu Xu. Red mud-based heterogeneous catalyst for hydrothermal resource-based degradation of norfloxacin in pharmaceutical wastewater by hydrogen peroxide. Journal of Water Process Engineering 2023, 56 , 104257. https://doi.org/10.1016/j.jwpe.2023.104257
    12. Chen Chen, Jie Song, Qian Pu, Xingcheng Liu, Jin Yan, Xuedong Wang, Huili Wang, Qiuhui Qian. Azithromycin induces neurotoxicity in zebrafish by interfering with the VEGF/Notch signaling pathway. Science of The Total Environment 2023, 903 , 166505. https://doi.org/10.1016/j.scitotenv.2023.166505
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    14. Juan C. Durán-Álvarez, Blanca Prado, Rodolfo Zanella, Mario Rodríguez, Suhaila Díaz. Wastewater surveillance of pharmaceuticals during the COVID-19 pandemic in Mexico City and the Mezquital Valley: A comprehensive environmental risk assessment. Science of The Total Environment 2023, 900 , 165886. https://doi.org/10.1016/j.scitotenv.2023.165886
    15. Jangwoo Lee, Nicole Acosta, Barbara J. Waddell, Kristine Du, Kevin Xiang, Jennifer Van Doorn, Kashtin Low, Maria A. Bautista, Janine McCalder, Xiaotian Dai, Xuewen Lu, Thierry Chekouo, Puja Pradhan, Navid Sedaghat, Chloe Papparis, Alexander Buchner Beaudet, Jianwei Chen, Leslie Chan, Laura Vivas, Paul Westlund, Srijak Bhatnagar, September Stefani, Gail Visser, Jason Cabaj, Stefania Bertazzon, Shahrzad Sarabi, Gopal Achari, Rhonda G. Clark, Steve E. Hrudey, Bonita E. Lee, Xiaoli Pang, Brendan Webster, William Amin Ghali, Andre Gerald Buret, Tyler Williamson, Danielle A. Southern, Jon Meddings, Kevin Frankowski, Casey R.J. Hubert, Michael D. Parkins. Campus node-based wastewater surveillance enables COVID-19 case localization and confirms lower SARS-CoV-2 burden relative to the surrounding community. Water Research 2023, 244 , 120469. https://doi.org/10.1016/j.watres.2023.120469
    16. Sung Ho Chae, Seung Ji Lim, Mingizem Gashaw Seid, Wondesen Workneh Ejerssa, Aseom Son, Heejong Son, Sangki Choi, Woongbae Lee, Yunho Lee, Seok Won Hong. Predicting micropollutant fate during wastewater treatment using refined classical kinetic model based on quantitative monitoring in multi-metropolitan regions of South Korea. Water Research 2023, 245 , 120627. https://doi.org/10.1016/j.watres.2023.120627
    17. N. Lopez-Herguedas, M. Irazola, I. Alvarez-Mora, G. Orive, U. Lertxundi, M. Olivares, O. Zuloaga, A. Prieto. Comprehensive micropollutant characterization of wastewater during Covid-19 crisis in 2020: Suspect screening and environmental risk prioritization strategy. Science of The Total Environment 2023, 873 , 162281. https://doi.org/10.1016/j.scitotenv.2023.162281
    18. Jangwoo Lee, Nicole Acosta, Barbara J. Waddell, Kristine Du, Kevin Xiang, Jennifer Van Doorn, Kashtin Low, Maria A. Bautista, Janine McCalder, Xiaotian Dai, Xuewen Lu, Thierry Chekouo, Puja Pradhan, Navid Sedaghat, Chloe Papparis, Alexander Buchner Beaudet, Jianwei Chen, Leslie Chan, Laura Vivas, Paul Westlund, Srijak Bhatnagar, September Stefani, Gail Visser, Jason Cabaj, Gopal Achari, Rhonda G. Clark, Steve E. Hrudey, Bonita E. Lee, Xiaoli Pang, Brandan Webster, William Amin Ghali, Andre Gerald Buret, Tyler Williamson, Danielle A. Southern, Jon Meddings, Kevin Frankowski, Casey R.J. Hubert, Michael D. Parkins. Spatially-resolved wastewater-based surveillance enables COVID-19 case localization across a university campus, and confirms lower SARS-CoV-2 RNA burden relative to the surrounding community. 2023https://doi.org/10.1101/2023.03.03.23286756
    19. Nicole Acosta, Xiaotian Dai, Maria A. Bautista, Barbara J. Waddell, Jangwoo Lee, Kristine Du, Janine McCalder, Puja Pradhan, Chloe Papparis, Xuewen Lu, Thierry Chekouo, Alexander Krusina, Danielle Southern, Tyler Williamson, Rhonda G. Clark, Raymond A. Patterson, Paul Westlund, Jon Meddings, Norma Ruecker, Christopher Lammiman, Coby Duerr, Gopal Achari, Steve E. Hrudey, Bonita E. Lee, Xiaoli Pang, Kevin Frankowsk, Casey R.J. Hubert, Michael D. Parkins. Wastewater-based surveillance can be used to model COVID-19-associated workforce absenteeism. 2023https://doi.org/10.1101/2023.01.22.23284878
    20. Mina Aghaei, Masud Yunesian, Hosna Janjani, Mohammad Hadi Dehghani. Wastewater-based epidemiology: Evidence mapping toward identifying emerging areas of research. 2023, 1-32. https://doi.org/10.1016/B978-0-443-19172-5.00012-3
    21. Brian A. Wartell, Sudheer Ballare, Shahrzad Saffari Ghandehari, Patricia Dotingco Arcellana, Camila Proano, Devrim Kaya, Debra Niemeier, Birthe V. Kjellerup. Relationship between SARS-CoV-2 in wastewater and clinical data from five wastewater sheds. Journal of Hazardous Materials Advances 2022, 8 , 100159. https://doi.org/10.1016/j.hazadv.2022.100159
    22. Diana S. Aga, Lahiruni M. Halwatura. Wastewater Surveillance of Pharmaceuticals and Genes: Challenges and Opportunities. LCGC North America 2022, , 351-354. https://doi.org/10.56530/lcgc.na.vk9190q2
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    Environmental Science & Technology Letters

    Cite this: Environ. Sci. Technol. Lett. 2022, 9, 6, 567–574
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.estlett.2c00259
    Published May 18, 2022
    Copyright © 2022 American Chemical Society
    Request reuse permissions

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